☆ 4.8 Review

Animal models for COVID-19 and tuberculosis

FRONTIERS IN IMMUNOLOGY (2023)

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Murine Coronavirus Disease 2019 Lethality Is Characterized by Lymphoid Depletion Associated with Suppressed Antigen-Presenting Cell Functionality

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Multimodal profiling of lung granulomas in macaques reveals cellular correlates of tuberculosis control

Hannah P. Gideon et al.

Summary: This study focuses on tuberculosis lung infection and its complex multicellular structure, the granuloma. Through various techniques, the study identifies factors that influence bacterial control in granulomas. It shows that granulomas with bacterial persistence are enriched with different cell types that communicate through immune and wound-healing pathways. On the other hand, granulomas that drive bacterial control are characterized by diverse cell populations engaged in pro-inflammatory signaling networks. The study also finds that granulomas that arise later in infection display characteristics of restrictive granulomas and are more effective at killing Mycobacterium tuberculosis.

IMMUNITY (2022)

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Comparative characterization of SARS-CoV-2 variants of concern and mouse-adapted strains in mice

Qi Chen et al.

Summary: This study systematically investigated the infectivity and pathogenicity of three SARS-CoV-2 variants (Alpha, Beta, and Delta) in mice and found that the Beta variant had the strongest infectivity and pathogenicity, while the Delta variant had weaker replication and pathogenic changes. These results highlight the risk of SARS-CoV-2 spillover from humans to mice and suggest that key amino acid mutations in mouse-adapted strains can be used as an early-warning indicator for predicting the risk of newly emerging SARS-CoV-2 variants.

JOURNAL OF MEDICAL VIROLOGY (2022)

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Risk of SARS-CoV-2 reinfection and COVID-19 hospitalisation in individuals with natural and hybrid immunity: a retrospective, total population cohort study in Sweden

Peter Nordstrom et al.

Summary: This retrospective cohort study investigated the effectiveness of COVID-19 vaccination in individuals who had previously been infected with SARS-CoV-2. The study found that natural immunity provided protection against SARS-CoV-2 infection and COVID-19 hospitalization for up to 20 months. Vaccination further reduced the risk of reinfection and hospitalization for up to 9 months, although the differences in absolute numbers, especially in hospitalizations, were small.

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Safety, tolerability and viral kinetics during SARS-CoV-2 human challenge in young adults

Ben Killingley et al.

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NATURE MEDICINE (2022)

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Domestic pigs experimentally infected with Mycobacterium bovis and Mycobacterium tuberculosis exhibit different disease outcomes

Nirajan Niroula et al.

Summary: The domestic pig is a suitable animal model for studying human tuberculosis due to its similarities with humans in anatomy, physiology, and immunology. This study compared the disease outcomes in pigs challenged with either Mycobacterium tuberculosis or Mycobacterium bovis, and found that pigs challenged with M. bovis exhibited more severe symptoms and pathology compared to pigs challenged with M. tb. However, the peripheral IFN-gamma responses were similar in both groups. These findings suggest that both M. bovis and M. tb can be used to model different aspects of human tuberculosis in pigs.

TUBERCULOSIS (2022)

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Article Cell Biology

Topologically associating domains are disrupted by evolutionary genome rearrangements forming species-specific enhancer connections in mice and humans

Sarah E. Gilbertson et al.

Summary: Distinguishing between conserved and divergent regulatory mechanisms is crucial for translating preclinical research from mice to humans. Evolutionary genome rearrangements disrupt TAD boundaries, enabling sequence-conserved enhancer elements from divergent genomic locations between species to create unique regulatory modules.

CELL REPORTS (2022)

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Article Microbiology

Mice infected with Mycobacterium tuberculosis are resistant to acute disease caused by secondary infection with SARS-CoV-2

Oscar Rosas Mejia et al.

Summary: This study found that Mtb infection can enhance resistance to CoV2 infection, which is associated with the expansion of T and B cell subsets in the lungs.

PLOS PATHOGENS (2022)

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Article Microbiology

Distinct spatial arrangements of ACE2 and TMPRSS2 expression in Syrian hamster lung lobes dictates SARS-CoV-2 infection patterns

Ilhan Tomris et al.

Summary: Analysis on Syrian hamster lung lobes shows that SARS-CoV-2 infection is restricted to areas where both ACE2 and TMPRSS2 are present, with ACE2 predominantly expressed in bronchioles and alveoli, while TMPRSS2 is in primary and secondary bronchi. Infections overlap where ACE2 and TMPRSS2 co-localize, in tertiary bronchi, bronchioles, and alveoli.

PLOS PATHOGENS (2022)

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Article Immunology

A tandem-repeat dimeric RBD protein-based covid-19 vaccine zf2001 protects mice and nonhuman primates

Yaling An et al.

Summary: This study reports the preclinical studies of ZF2001, a protein subunit vaccine against COVID-19. The vaccine showed high immunogenicity and protection efficacy in both mice and non-human primates, inducing balanced cellular immune responses. Additionally, no evidence of disease enhancement was observed in animal models.

EMERGING MICROBES & INFECTIONS (2022)

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Article Immunology

Porcine Respiratory Coronavirus as a Model for Acute Respiratory Coronavirus Disease

Sarah Keep et al.

Summary: In response to the SARS-CoV-2 pandemic, a porcine respiratory coronavirus (PRCV) model has been developed for in-depth evaluation of the pathogenesis, virology, and immune responses of this virus family. Pigs, which share similar physiology and immunology with humans, were used as a natural host for PRCV. The study found that different PRCV strains induced varying degrees of lung pathology, with those causing more severe lung damage being able to replicate in ex vivo tracheal organ cultures, as well as in the trachea and lung in vivo.

FRONTIERS IN IMMUNOLOGY (2022)

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Article Immunology

Mild SARS-CoV-2 infection in rhesus macaques is associated with viral control prior to antigen-specific T cell responses in tissues

Christine E. Nelson et al.

Summary: This study used rhesus macaques to model mild COVID-19 and found that SARS-CoV-2 replication decreases in the lungs, nasal, and oral mucosa before antigen-specific effector T cells arrive, suggesting that innate immunity efficiently restricts viral replication during mild COVID-19.

SCIENCE IMMUNOLOGY (2022)

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Article Veterinary Sciences

Video Endoscopy-Guided Intrabronchial Spray Inoculation of Mycobacterium bovis in Goats and Comparative Assessment of Lung Lesions With Various Imaging Methods

Nadine Wedlich et al.

Summary: This study describes the refinement of an animal model for bovine tuberculosis (bTB) in goats. The researchers established a method for intrabronchial inoculation via video-guided endoscopy, as well as lung imaging using computed tomography (CT). Results showed successful infection of goats with M. bovis and CT proved to be a highly sensitive method for quantifying the extent of pulmonary lesions.

FRONTIERS IN VETERINARY SCIENCE (2022)

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Article Multidisciplinary Sciences

Immunopathogenic overlap between COVID-19 and tuberculosis identified from transcriptomic meta-analysis and human macrophage infection

Dylan Sheerin et al.

Summary: Current and previous tuberculosis (TB) increase the risk of COVID-19 mortality and severe disease. Mechanisms of immunopathogenic interaction between COVID-19 and TB were explored through transcriptomic analysis. Aberrant expression of specific gene signatures was found in active TB and latent TB progressors, correlating with higher COVID-19 risk. Enrichment of specific macrophages was observed in severe COVID-19 and active TB patients, indicating shared disease exacerbation. In vitro validation demonstrated increased SARS-CoV-2 infection in macrophages cultured in the inflammatory milieu of Mtb-infected macrophages.

ISCIENCE (2022)

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Article Immunology

Single-cell transcriptome analysis of the in vivo response to viral infection in the cave nectar bat Eonycteris spelaea

Akshamal M. Gamage et al.

Summary: Bats are reservoir hosts of zoonotic viruses with pandemic potential. This study utilized single-cell transcriptome sequencing to analyze the immune response in bat lungs upon infection with a double-stranded RNA virus. The study revealed the presence of neutrophils, NK cells, and T cells as the main immune cells in the lung tissue. Different subpopulations of CD8+ effector T cells and NK and T cells expressing genes involved in T cell activation and effector function were identified.

IMMUNITY (2022)

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Article Virology

SARS-CoV-2 Omicron (B.1.1.529) Infection of Wild White-Tailed Deer in New York City

Kurt J. Vandegrift et al.

Summary: There is growing evidence of SARS-CoV-2 spillover from humans to various animal species, including deer. This study investigated the active and asymptomatic infection of the Omicron variant in free-ranging deer in New York City. The findings revealed that a small number of deer had been exposed to SARS-CoV-2, with two deer showing evidence of reinfection or early seroconversion. This suggests that variants of concern are still circulating and may reestablish transmission cycles in US deer populations, highlighting the need for a coordinated One Health response.

VIRUSES-BASEL (2022)

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Review Immunology

Correlates of protection against SARS-CoV-2 infection and COVID-19 disease

David Goldblatt et al.

Summary: Antibodies against S1 epitopes provide the most accurate prediction of infection by SARS-CoV-2 coronavirus. Binding antibody titers have the highest statistical correlation. Besides neutralization, antibodies also have multiple protective functions. Cellular responses, including CD4(+) T cells and CD8(+) cells, play a significant role in antibody augmentation and viral replication control, especially in the presence of insufficient antibodies. More research is needed on mucosal responses.

IMMUNOLOGICAL REVIEWS (2022)

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Article Cell Biology

SARS-CoV-2 infection in hamsters and humans results in lasting and unique systemic perturbations after recovery

Justin J. Frere et al.

Summary: This study compared the short- and long-term systemic responses after SARS-CoV-2 and influenza A virus (IAV) infection, and found that SARS-CoV-2 caused more severe and lasting lung and kidney damage compared to IAV. It also uniquely affected the olfactory bulb and olfactory epithelium. Despite viral clearance, the olfactory bulb and epithelium showed sustained transcriptional changes and correlated with behavioral changes, providing insights into the persistent symptoms of COVID-19.

SCIENCE TRANSLATIONAL MEDICINE (2022)

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Article Microbiology

Bacterial Strain-Dependent Dissociation of Cell Recruitment and Cell-to-Cell Spread in Early M. tuberculosis Infection

B. Shoshana Zha et al.

Summary: In the early stages of tuberculosis infection, the interactions between different strains of Mycobacterium tuberculosis and lung leukocytes can shape the adaptive immune responses.

MBIO (2022)

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Article Microbiology

A Multitrait Locus Regulates Sarbecovirus Pathogenesis

Alexandra Schafer et al.

Summary: Host genetic variation plays an important role in predicting disease outcomes following coronavirus infection. Using a mouse model, researchers identified several genetic loci that control different disease outcomes in the context of SARS-CoV infection. They also found a conserved locus on mouse chromosome 9 that shares homology with a human GWAS locus for severe SARS-CoV-2 disease. Two candidate genes, CCR9 and CXCR6, were identified as key regulators of disease severity in multiple coronavirus infections across species.

MBIO (2022)

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Article Multidisciplinary Sciences

A third vaccination with a single T cell epitope confers protection in a murine model of SARS-CoV-2 infection

Iris N. Pardieck et al.

Summary: Repeated booster vaccinations with a three dose regimen of a synthetic peptide vaccine significantly enhance the CD8(+) T cell response, leading to protection against lethal SARS-CoV-2 infection. Understanding the mechanisms and impact of booster vaccinations is crucial for vaccine design and delivery.

NATURE COMMUNICATIONS (2022)

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Article Cell Biology

Vaccine-associated enhanced respiratory pathology in COVID-19 hamsters after TH2-biased immunization

Aileen Ebenig et al.

Summary: In this study, the potential for vaccine-associated enhanced respiratory disease (VAERD) in COVID-19 was investigated using a severe hamster infection model. Two vaccine candidates were evaluated, one derived from a T helper type 1 (T(H)1)-biased measles vaccine and another comprising a T(H)2-biased, alum-adjuvanted, non-stabilized spike protein. The measles vaccine protected the animals, while the protein lead induced VAERD, which could be alleviated with dexamethasone treatment. Transcriptomic and single-cell RNA sequencing analyses identified the cytokine drivers and cellular contributors involved in VAERD.

CELL REPORTS (2022)

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Article Immunology

Ferrets as a model for tuberculosis transmission

Tuhina Gupta et al.

Summary: Despite the COVID-19 pandemic, tuberculosis remains a leading cause of human death. Ferrets have been successfully used as a model to study the transmission of Mycobacterium tuberculosis, with their infection leading to clinical signs and pathological features similar to acute disease in larger animals. Infected ferrets can transmit the bacteria to other ferrets, and the efficiency of transmission is higher when the transmitting animal has a well-established acute infection. This study supports further assessment of the ferret model for tuberculosis transmission and testing prevention measures and vaccine efficacy.

FRONTIERS IN CELLULAR AND INFECTION MICROBIOLOGY (2022)

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Article Immunology

Monocyte biology conserved across species: Functional insights from cattle

Stephanie C. Talker et al.

Summary: This study investigates the transcriptome profiles and functions of bovine monocytes. The findings reveal three subtypes of monocytes in bovine, each with distinct functional roles. Classical monocytes are involved in pro-inflammatory and antibacterial responses, while nonclassical and intermediate monocytes are specialized in regulatory/anti-inflammatory functions, tissue repair, antiviral responses, and T-cell immunomodulation. Furthermore, heterogeneity within classical monocytes is discovered, and intermediate monocytes are proposed as a transient differentiation stage between classical and nonclassical monocytes.

FRONTIERS IN IMMUNOLOGY (2022)

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Article Respiratory System

A pulmonologist's guide to perform and analyse cross-species single lung cell transcriptomics

Peter Pennitz et al.

Summary: Single-cell RNA sequencing is important for studying biological processes, especially in lung research. We compared single-cell transcriptomes from six different species' lungs and identified marker genes using integrative approaches. This method helps identify transcriptomic signatures in different species' lung tissue and select appropriate models for future respiratory research.

EUROPEAN RESPIRATORY REVIEW (2022)

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Article Biochemistry & Molecular Biology

Vaccine-Induced Subcutaneous Granulomas in Goats Reflect Differences in Host-Mycobacterium Interactions between BCG- and Recombinant BCG-Derivative Vaccines

Elisabeth M. Liebler-Tenorio et al.

Summary: This study compares the development of tuberculous granulomas at the site of BCG vaccination and its recombinant derivatives in goats. The results show that granulomas with central caseous necrosis are induced by both BCG and its recombinant derivatives, although the size and extent of necrosis differ between vaccine strains. The recombinant derivatives induce fewer CD4(+) T and B cells and more CD8(+) cells in the granulomas compared to the parental BCG strain. Furthermore, the numbers of multinucleated giant cells (MNGCs) and cells with lipid bodies are significantly lower in groups administered with the recombinant BCG strains. These findings suggest that the granulomas induced by BCG and its recombinant derivatives in goats can serve as suitable models to compare reactions to different mycobacteria or tuberculosis vaccines.

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2022)

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Article Immunology

Impaired immune response drives age-dependent severity of COVID-19

Julius Beer et al.

Summary: The study reveals that advanced age is correlated with severe COVID-19 due to impaired immune response, specifically the diminished IFN-gamma response and excessive virus replication. It suggests that immunotherapy combining IFN-gamma and IFN-lambda could benefit highly vulnerable individuals.

JOURNAL OF EXPERIMENTAL MEDICINE (2022)

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Article Microbiology

Comparative Assessment of Severe Acute Respiratory Syndrome Coronavirus 2 Variants in the Ferret Model

Joanna A. Pulit-Penaloza et al.

Summary: Continued surveillance and risk assessment of emerging SARS-CoV-2 variants are crucial in pandemic response. The study found that the Delta variant showed enhanced transmissibility compared to other strains. Prior infection with SARS-CoV-2 provided varied levels of protection against reinfection.

MBIO (2022)

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Article Microbiology

Multiple Introductions of SARS-CoV-2 Alpha and Delta Variants into White-Tailed Deer in Pennsylvania

Andrew D. Marques et al.

Summary: White-tailed deer in Pennsylvania were found to have a high level of infection with SARS-CoV-2, indicating that they may serve as a potential reservoir for the virus to transmit back to humans. The variants of the virus in deer show significant differences from those in humans.

MBIO (2022)

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Article Cell Biology

Landscape and age dynamics of immune cells in the Egyptian rousette bat

Virginia Friedrichs et al.

Summary: Using single-cell RNA sequencing and flow cytometry, we characterized the immune cell landscape in Egyptian rousette bats and found age-related differences in immune cell subsets. We also observed similarities in immune functions between juvenile and adult bats.

CELL REPORTS (2022)

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Article Microbiology

Mouse models of COVID-19 recapitulate inflammatory pathways rather than gene expression

Cameron R. Bishop et al.

Summary: The debate on how well mouse models recapitulate the transcriptional profiles seen in humans is ongoing. While there are differences in gene overlap, analyses of immune signatures and inflammatory pathways indicate a significant concordance between species.

PLOS PATHOGENS (2022)

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Article Microbiology

Superinfection with SARS-CoV-2 Has Deleterious Effects on Mycobacterium bovis BCG Immunity and Promotes Dissemination of Mycobacterium tuberculosis

Rachel E. Hildebrand et al.

Summary: Prior to SARS-CoV-2, tuberculosis was a major global health issue with a significant number of infections and deaths. This study shows that SARS-CoV-2 superinfection in mice with tuberculosis leads to increased bacterial spread, immune changes, and pathology. It also reveals that SARS-CoV-2 can impact the effectiveness of BCG vaccine in mice, resulting in decreased IL-17 levels without providing protection against SARS-CoV-2. These findings suggest that SARS-CoV-2 may worsen the tuberculosis pandemic and limit the efficacy of BCG vaccine.

MICROBIOLOGY SPECTRUM (2022)

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Letter Immunology

Experimental Infection of Mink with SARS-COV-2 Omicron Variant and Subsequent Clinical Disease

Jenni Virtanen et al.

Summary: We report an experimental infection of American mink with SARS-CoV-2 Omicron variant, which showed that mink remained positive for viral RNA, experienced clinical signs and histopathologic changes, and transmitted the virus to uninfected recipients. Preparedness is crucial to prevent the spread among mink and spillover to human populations.

EMERGING INFECTIOUS DISEASES (2022)

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Article Immunology

Risk Factors for Coronavirus Disease 2019 (COVID-19) Death in a Population Cohort Study from the Western Cape Province, South Africa

Andrew Boulle et al.

Summary: In South Africa, living with HIV and having current tuberculosis were independently associated with increased COVID-19 mortality. These findings highlight the impact of these two diseases on COVID-19 risk and demonstrate the associations between age, sex, and other comorbidities with COVID-19 mortality.

CLINICAL INFECTIOUS DISEASES (2021)

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Article Microbiology

Ultra-low Dose Aerosol Infection of Mice with Mycobacterium tuberculosis More Closely Models Human Tuberculosis

Courtney R. Plumlee et al.

Summary: The study successfully developed a tuberculosis model in mice that more closely resembles human disease by infecting them with an ultra-low dose of bacteria, resulting in highly heterogeneous bacterial burdens and granulomas similar to those in humans. By identifying blood RNA signatures, it was possible to predict infection outcomes in mice and infer the risk of progression to active tuberculosis in humans.

CELL HOST & MICROBE (2021)

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Letter Immunology

SARS-CoV-2 infection in K18-ACE2 transgenic mice replicates human pulmonary disease in COVID-19

Victor M. Arce et al.

CELLULAR & MOLECULAR IMMUNOLOGY (2021)

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Article Veterinary Sciences

Overview of Nonhuman Primate Models of SARS-CoV-2 Infection

Anita M. Trichel

Summary: Research has shown that NHPs are more closely related to humans physiologically, genetically, and immunologically, making them a suitable model for studying the SARS-CoV-2 virus. While current animal models may not fully represent the full spectrum of human COVID-19 disease, they still play a crucial role in vaccine and therapeutic development.

COMPARATIVE MEDICINE (2021)

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Article Multidisciplinary Sciences

Correlates of protection against SARS-CoV-2 in rhesus macaques

Katherine McMahan et al.

Summary: Adoptive transfer of purified IgG from convalescent macaques protects naive macaques against SARS-CoV-2 infection, and cellular immune responses contribute to protection against rechallenge with SARS-CoV-2. The findings suggest that relatively low antibody titres are sufficient for protection against SARS-CoV-2 in macaques, while higher antibody titres are required for treatment of SARS-CoV-2 infection.

NATURE (2021)

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Article Cell Biology

Single-cell RNA sequencing reveals SARS-CoV-2 infection dynamics in lungs of African green monkeys

Emily Speranza et al.

Summary: This study utilized African green monkeys as models to investigate the dynamics of SARS-CoV-2 virus replication in the respiratory tract. It was found that virus replication mainly occurred in pneumocytes in the lungs, while macrophages drove the inflammatory response. By combining single-cell RNA sequencing and new analysis methods, important cells in the host response to virus infection were identified and their roles elucidated.

SCIENCE TRANSLATIONAL MEDICINE (2021)

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Article Virology

Neuroinvasion and Encephalitis Following Intranasal Inoculation of SARS-CoV-2 in K18-hACE2 Mice

Pratima Kumari et al.

Summary: The study demonstrated that SARS-CoV-2 infection can lead to neuroinvasion and encephalitis in K18-hACE2 mice, resulting in mortality. While the highest virus titers were observed in the lungs, high levels of infectious virus were also found in the brains of the infected mice. The severity of the disease in infected mice correlated with peak viral levels in the brain.

VIRUSES-BASEL (2021)

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Article Microbiology

K18-hACE2 mice develop respiratory disease resembling severe COVID-19

Claude Kwe Yinda et al.

Summary: The study demonstrates that humanized transgenic mice developed dose-dependent disease when inoculated with SARS-CoV-2, showing upper and lower respiratory tract infection with viral replication also in the brain. The pathological and immunological manifestations observed in these mice resemble human COVID-19, suggesting the model's usefulness in elucidating COVID-19 pathogenesis and testing countermeasures.

PLOS PATHOGENS (2021)

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Article Immunology

Susceptibility of rabbits to SARS-CoV-2

Anna Z. Mykytyn et al.

Summary: The susceptibility of rabbits to SARS-CoV-2 is a potential public health concern as they can excrete infectious virus from the nose and throat. Therefore, investigations on the presence of SARS-CoV-2 in farmed rabbits should be considered.

EMERGING MICROBES & INFECTIONS (2021)

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Correction Microbiology

Responses to acute infection with SARS-CoV-2 in the lungs of rhesus macaques, baboons and marmosets (vol 6, pg 73, 2021)

Dhiraj Kumar Singh et al.

NATURE MICROBIOLOGY (2021)

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Article Immunology

Intravenous administration of BCG protects mice against lethal SARS-CoV-2 challenge

Kerry L. Hilligan et al.

JOURNAL OF EXPERIMENTAL MEDICINE (2021)

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Article Infectious Diseases

Coinfection of tuberculosis and COVID-19 limits the ability to in vitro respond to SARS-CoV-2

Linda Petrone et al.

Summary: The study revealed that COVID-19 patients with TB or LTBI have a diminished immune response to SARS-CoV-2 but retain the ability to respond to Mtb-specific antigens.

INTERNATIONAL JOURNAL OF INFECTIOUS DISEASES (2021)

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Article Biochemistry & Molecular Biology

Animal models for human group 1 CD1 protein function

Emmelie Eckhardt et al.

Summary: The CD1 antigen presenting system is evolutionarily conserved and can be found in mammals, birds, and reptiles. Research on the role of CD1a, CD1b, and CD1c in mice has been hindered by their lack of expression in mice, but alternative animal models have provided valuable insights into CD1-dependent antimicrobial immune functions. Transgenic mouse models have also contributed to a better understanding of the mechanisms involved in CD1-restricted T cell responses.

MOLECULAR IMMUNOLOGY (2021)

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Article Multidisciplinary Sciences

SARS-CoV-2 spike D614G change enhances replication and transmission

Bin Zhou et al.

Summary: Research has shown that the D614G substitution in the spike protein of SARS-CoV-2 leads to increased binding and replication potential in humans, as well as significantly higher replication and transmissibility in different animal models, providing an explanation for the global prevalence of this variant in the COVID-19 pandemic.

NATURE (2021)

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Article Multidisciplinary Sciences

Comparison of rhesus and cynomolgus macaques as an infection model for COVID-19

Francisco J. Salguero et al.

Summary: This study demonstrates that SARS-CoV-2 replicates in the upper and lower respiratory tract of both rhesus and cynomolgus macaques, causing pulmonary lesions. Immune responses against SARS-CoV-2 are similar in both species, suggesting that both macaque species authentically represent mild to moderate forms of COVID-19. The findings provide valuable insights for evaluating interventions against SARS-CoV-2.

NATURE COMMUNICATIONS (2021)

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Review Multidisciplinary Sciences

Immunogenicity of clinically relevant SARS-CoV-2 vaccines in nonhuman primates and humans

P. J. Klasse et al.

Summary: This article summarizes the progress of multiple preventive vaccines being developed to counter the COVID-19 pandemic, including results from animal and human trials as well as challenge experiments. The focus is on comparing the immunogenicity performance of the vaccines and summarizing the press releases on vaccine efficacy trials.

SCIENCE ADVANCES (2021)

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Article Pathology

Coronavirus Activates an Altruistic Stem Cell-Mediated Defense Mechanism that Reactivates Dormant Tuberculosis Implications in Coronavirus Disease 2019 Pandemic

Lekhika Pathak et al.

Summary: Adult stem cells may exhibit an altruistic defense mechanism to protect their niche, similar to bacteria, and demonstrate altruistic behavior against coronavirus infection in vivo. Reprogrammed stem cells in a mouse model showed direct antiviral activity, reducing viral load and promoting survival/proliferation of alveolar epithelial cells. In a Mycobacterium tuberculosis dormancy model, increased altruistic stem cells led to lower viral loads and potential reactivation of tuberculosis.

AMERICAN JOURNAL OF PATHOLOGY (2021)

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Article Immunology

Low Dose Pig Anti-Influenza Virus Monoclonal Antibodies Reduce Lung Pathology but Do Not Prevent Virus Shedding

Basudev Paudyal et al.

Summary: Prophylactic intravenous administration of specific monoclonal antibodies in pigs showed significant reduction in lung pathology and virus loads, but not consistent reduction in nasal shedding. The effect on lung pathology and virus load is consistent across different doses, suggesting that lower doses may be effective in reducing disease severity.

FRONTIERS IN IMMUNOLOGY (2021)

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Article Immunology

Respiratory and Intramuscular Immunization With ChAdOx2-NPM1-NA Induces Distinct Immune Responses in H1N1pdm09 Pre-Exposed Pigs

Eleni Vatzia et al.

Summary: Aerosol delivery boosted local lung T-cell and antibody responses, while intramuscular immunization boosted peripheral blood immunity, providing insights into optimizing protective immune responses.

FRONTIERS IN IMMUNOLOGY (2021)

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Review Veterinary Sciences

Animal Models of COVID-19. I. Comparative Virology and Disease Pathogenesis

Caroline J. Zeiss et al.

Summary: The COVID-19 pandemic has driven the development of animal models to study disease pathogenesis, therapeutic testing, and vaccine development. Different animal models have been used to study viral shedding and transmission, with distinct characteristics and abilities. These models have provided a consistent template for testing therapeutics, understanding immune responses, and testing vaccine approaches.

ILAR JOURNAL (2021)

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Review Biochemistry & Molecular Biology

Neutrophils in Tuberculosis: Cell Biology, Cellular Networking and Multitasking in Host Defense

Rachana R. Borkute et al.

Summary: Neutrophils play a complex role in tuberculosis, with both beneficial and detrimental effects on disease outcomes. Recent studies have revealed the phenotypic heterogeneity of neutrophils and their interactions with other cells in TB pathophysiology.

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2021)

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Article Immunology

Immune memory from SARS-CoV-2 infection in hamsters provides variant-independent protection but still allows virus transmission

Shu Horiuchi et al.

Summary: The study found that the innate immune response to SARS-CoV-2 infection was delayed but followed by a pronounced adaptive response, with T cell adoptive transfer reducing virus levels and rapidly inducing specific B cells. SARS-CoV-2-specific T and B cells were able to control infection, but failed to prevent transmission to both naive and vaccinated animals.

SCIENCE IMMUNOLOGY (2021)

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Article Virology

Light Sheet Microscopy-Assisted 3D Analysis of SARS-CoV-2 Infection in the Respiratory Tract of the Ferret Model

Luca M. Zaeck et al.

Summary: This study demonstrates the utility of volumetric three-dimensional immunofluorescence imaging to investigate host-pathogen interactions of SARS-CoV-2 in ferrets, providing detailed quantification of infection foci and suggesting clustering of infection foci in close proximity. The study presents the first specific 3D visualization of SARS-CoV-2 infection, providing valuable insights into spatial tissue morphology of critically important respiratory pathogens.

VIRUSES-BASEL (2021)

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Article Biochemical Research Methods

SARS-CoV-2 viral dynamics in non-human primates

Antonio Goncalves et al.

Summary: Non-human primates infected with SARS-CoV-2 develop mild infection similar to asymptomatic human infection. Viral load rapidly declines after peak, with within-host reproduction numbers suggesting a prophylactic therapy with 90% efficacy could prevent viral growth. Mathematical model characterization in 31 cynomolgus macaques shows rapid loss of infected cells after peak with no significant association between cytokine elevation and clearance, predicting prophylactic treatment blocking 90% of viral production or infection could prevent viral growth.

PLOS COMPUTATIONAL BIOLOGY (2021)

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Article Microbiology

Macrophage-specific responses to human- and animal-adapted tubercle bacilli reveal pathogen and host factors driving multinucleated cell formation

Christophe J. Queval et al.

Summary: The study revealed that Mbv and Mtb exhibit different behaviors in host cells, with Mbv infection leading to multinucleated cell formation in bovine macrophages. It was identified that MPB70 from Mbv and bovine macrophage extracellular vesicles are mechanistic drivers of multinucleated cell formation. In vivo confirmation of differential multinucleated cell formation in cattle models further supports the role of these factors in host tropism in human/bovine tuberculosis.

PLOS PATHOGENS (2021)

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Article Immunology

Vasculitis and Neutrophil Extracellular Traps in Lungs of Golden Syrian Hamsters With SARS-CoV-2

Kathrin Becker et al.

Summary: Neutrophil extracellular traps (NETs) play a crucial role in severe COVID-19 cases, and the Syrian hamster model could serve as a useful tool to further investigate the impact of vascular lesions and NETs in the pathogenesis of COVID-19.

FRONTIERS IN IMMUNOLOGY (2021)

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Article Multidisciplinary Sciences

Experimental and natural evidence of SARS-CoV-2-infection-induced activation of type I interferon responses

Arinjay Banerjee et al.

Summary: Recent studies have shown that SARS-CoV-2 proteins can inhibit human type I interferon responses, and the timing and extent of interferon production are associated with COVID-19 severity. SARS-CoV-2 infection induces a type I interferon response in vitro and in moderate cases of COVID-19, with physiological levels of IFNa being sufficient to suppress SARS-CoV-2 replication in human airway cells.

ISCIENCE (2021)

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Article Multidisciplinary Sciences

In vivo monoclonal antibody efficacy against SARS-CoV-2 variant strains

Rita E. Chen et al.

Summary: Cell culture experiments showed reduced or abrogated neutralizing activity of monoclonal antibodies against SARS-CoV-2 variant strains, but low prophylactic doses of antibody combinations protected against infection in vivo without resistance emergence. Higher doses of several monoclonal antibody cocktails also provided protection against viruses with a B.1.351 spike gene in vivo. Many antibody products with Emergency Use Authorization should therefore retain substantial efficacy against prevailing variant strains of SARS-CoV-2.

NATURE (2021)

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Article Multidisciplinary Sciences

Immune correlates of protection by mRNA-1273 vaccine against SARS-CoV-2 in nonhuman primates

Kizzmekia S. Corbett et al.

Summary: In nonhuman primates (NHPs), vaccination with mRNA-1273 induces dose-dependent antibody responses, leading to a significant reduction in viral replication post SARS-CoV-2 challenge. Replication of the virus correlates strongly with antibody levels and neutralizing activity, with lower levels required in the lower airway than in the upper airway. Passive transfer of mRNA-1273-induced IgG is sufficient to provide protection, indicating that humoral immune responses induced by mRNA-1273 vaccine are effective against SARS-CoV-2 in NHPs.

SCIENCE (2021)

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Article Microbiology

Sex Differences in Lung Imaging and SARS-CoV-2 Antibody Responses in a COVID-19 Golden Syrian Hamster Model

Santosh Dhakal et al.

Summary: Male and female golden Syrian hamsters infected with SARS-CoV-2 exhibit different pathophysiological characteristics, with males experiencing more severe illness, slower recovery, and females generating stronger antibody responses. This animal model provides insights into COVID-19 sex differences and vaccine-induced immunity.

MBIO (2021)

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Article Multidisciplinary Sciences

Temporal omics analysis in Syrian hamsters unravel cellular effector responses to moderate COVID-19

Geraldine Nouailles et al.

Summary: The immune response is crucial in determining disease severity in COVID-19. Research has found that in the early stages of infection, monocyte-derived macrophages in the lungs exhibit the earliest and strongest transcriptional response to infection.

NATURE COMMUNICATIONS (2021)

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Article Multidisciplinary Sciences

More than 50 long-term effects of COVID-19: a systematic review and meta-analysis

Sandra Lopez-Leon et al.

Summary: This study aimed to identify studies assessing the long-term effects of COVID-19, estimating that 80% of infected patients will develop one or more long-term symptoms, with the most common being fatigue, headache, attention disorder, hair loss, and dyspnea.

SCIENTIFIC REPORTS (2021)

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Article Cell Biology

CD4 T cell help prevents CD8 T cell exhaustion and promotes control of Mycobacterium tuberculosis infection

Yu-Jung Lu et al.

Summary: CD4 T cells play a crucial role in immunity to tuberculosis by enhancing CD8 effector functions and preventing exhaustion, promoting the survival of infected mice. Vaccines that elicit both CD4 and CD8 T cells are more likely to be successful in generating protective responses against M. tuberculosis infection.

CELL REPORTS (2021)

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Article Microbiology

ACE2-lentiviral transduction enables mouse SARS-CoV-2 infection and mapping of receptor interactions

Daniel J. Rawle et al.

Summary: This study identified key amino acids in mouse ACE2 that prevent SARS-CoV-2 infection and developed a lentivirus system to express human ACE2 in mouse lungs, leading to a model with inflammatory responses similar to human COVID-19. The importance of interferon signaling in driving inflammatory responses was shown using genetically modified mice, and the hACE2-lentivirus system was demonstrated to be useful for vaccine evaluation in mouse models, highlighting its potential for SARS-CoV-2 research.

PLOS PATHOGENS (2021)

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Article Microbiology

CXCL1: A new diagnostic biomarker for human tuberculosis discovered using Diversity Outbred mice

Deniz Koyuncu et al.

Summary: The study identified five protein biomarker candidates using a Diversity Outbred mouse population, with CXCL1 and MMP8 being the most promising. Through statistical and machine learning analysis, CXCL1 was found to meet the World Health Organization's criteria for a triage diagnostic test to distinguish active TB from other conditions in human patients.

PLOS PATHOGENS (2021)

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Article Public, Environmental & Occupational Health

Difference in mortality among individuals admitted to hospital with COVID-19 during the first and second waves in South Africa: a cohort study

Waasila Jassat et al.

Summary: The second wave of COVID-19 in South Africa had higher incidence rates, a more rapid increase in hospital admissions, and increased in-hospital mortality compared to the first wave. Individuals admitted in the second wave were more likely to be older, of Mixed race, admitted in the public sector, and had a decreased likelihood of having a comorbid condition. After adjusting for weekly COVID-19 hospital admissions, there was a 31% increased risk of in-hospital mortality in the second wave.

LANCET GLOBAL HEALTH (2021)

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Review Agriculture, Dairy & Animal Science

SARS-CoV-2 Clinical Outcome in Domestic and Wild Cats: A Systematic Review

Sebastian Giraldo-Ramirez et al.

Summary: The study reveals that domestic cats are mostly asymptomatic when infected with SARS-CoV-2, while wild felines primarily exhibit respiratory symptoms, with up to 96.5% of affected animals presenting with coughing. Symptomatic animals belong to different subfamilies within the Felidae family.

ANIMALS (2021)

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Article Immunology

Adaptive immune determinants of viral clearance and protection in mouse models of SARS-CoV-2

Benjamin Israelow et al.

Summary: Research demonstrates that both humoral and cellular immunity play a role in clearing SARS-CoV-2, and convalescent mice or mice vaccinated with mRNA are protected from infection with both the wild type virus and the B.1.351 variant. This protection is mainly mediated by antibody response rather than cellular immunity.

SCIENCE IMMUNOLOGY (2021)

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Article Veterinary Sciences

Mycobacterial Infection of Precision-Cut Lung Slices Reveals Type 1 Interferon Pathway Is Locally Induced by Mycobacterium bovis but Not M. tuberculosis in a Cattle Breed

Aude Remot et al.

Summary: The study utilized precision-cut lung slices (PCLS) model in cattle to investigate early lung response to mycobacterial infection, revealing striking differences between cattle breeds and mycobacterial strains.

FRONTIERS IN VETERINARY SCIENCE (2021)

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Article Medicine, Research & Experimental

WNT6/ACC2-induced storage of triacylglycerols in macrophages is exploited by Mycobacterium tuberculosis

Julius Brandenburg et al.

Summary: This study demonstrates that Mycobacterium tuberculosis exploits the storage of TAGs in macrophages induced by WNT6/ACC2 to facilitate its intracellular survival. Treatment of Mtb-infected mice with a combination of an ACC2 inhibitor and the anti-TB drug isoniazid reduces bacterial numbers and cell infiltrates in the liver.

JOURNAL OF CLINICAL INVESTIGATION (2021)

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Article Medicine, Research & Experimental

Relationship of SARS-CoV-2-specific CD4 response to COVID-19 severity and impact of HIV-1 and tuberculosis coinfection

Catherine Riou et al.

Summary: This study found that the attributes of SARS-CoV-2-specific CD4(+) T cells were associated with the severity of COVID-19, with severe cases showing poor polyfunctional potential, reduced proliferation capacity, and enhanced HLA-DR expression. HIV-1 and TB coinfection can alter the SARS-CoV-2 T cell response, with HIV-1 causing CD4(+) T cell depletion and active TB leading to decreased polyfunctional capacity of SARS-CoV-2-specific CD4(+) T cells in COVID-19 patients. Moreover, COVID-19 patients displayed a reduced frequency of Mycobacterium tuberculosis-specific CD4(+) T cells, which may affect TB disease progression.

JOURNAL OF CLINICAL INVESTIGATION (2021)

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Article Immunology

Type I interferon signaling mediates Mycobacterium tuberculosis-induced macrophage death

Li Zhang et al.

Summary: Research findings indicate that macrophage-derived type I interferons play a crucial role in the death of Mtb-infected macrophages in vitro, and blocking this signaling pathway may enhance the efficacy of TB drugs like rifampin. Further defining the pathway of type I interferon-mediated macrophage death may lead to more selective host-directed therapy for tuberculosis.

JOURNAL OF EXPERIMENTAL MEDICINE (2021)

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Article Multidisciplinary Sciences

Transmission of SARS-CoV-2 on mink farms between humans and mink and back to humans

Bas B. Oude Munnink et al.

Summary: Animal experiments have shown that various animals can be infected by SARS-CoV-2, with evidence of animal-to-human transmission within mink farms. Investigation into mink farm outbreaks revealed that the virus was initially introduced by humans and has since evolved, causing transmission between mink farms. Despite enhanced biosecurity measures and culling, transmission occurred between farms in three large clusters with unknown modes of transmission, resulting in a high percentage of infections among mink farm residents and employees.

SCIENCE (2021)

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Article Multidisciplinary Sciences

COVID-19 treatments and pathogenesis including anosmia in K18-hACE2 mice

Jian Zheng et al.

Summary: The COVID-19 pandemic is associated with significant morbidity and mortality. Experimental studies in animals infected with SARS-CoV-2 have revealed severe lung and brain damage, as well as early onset anosmia in mice. Excitingly, infusion of convalescent plasma from recovered patients has shown to protect against lethal disease, though it does not prevent anosmia.

NATURE (2021)

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Article Critical Care Medicine

A Human Lung Challenge Model to Evaluate the Safety and Immunogenicity of PPD and Live Bacillus Calmette-Guerin

Malika Davids et al.

AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE (2020)

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Article Immunology

Inoculum size and traits of the infecting clinical strain define the protection level against Mycobacterium tuberculosis infection in a rabbit model

Liana Tsenova et al.

EUROPEAN JOURNAL OF IMMUNOLOGY (2020)

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Editorial Material Infectious Diseases

Note from the editors: World Health Organization declares novel coronavirus (2019-nCoV) sixth public health emergency of international concern

EUROSURVEILLANCE (2020)

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Article Immunology

Mycobacterium tuberculosis HN878 Infection Induces Human-Like B-Cell Follicles in Mice

Jose Alberto Choreno-Parra et al.

JOURNAL OF INFECTIOUS DISEASES (2020)

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Article Multidisciplinary Sciences

Prevention of tuberculosis in macaques after intravenous BCG immunization

Patricia A. Darrah et al.

NATURE (2020)

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Article Multidisciplinary Sciences

A new coronavirus associated with human respiratory disease in China

Fan Wu et al.

NATURE (2020)

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Article Multidisciplinary Sciences

A systematic approach to simultaneously evaluate safety, immunogenicity, and efficacy of novel tuberculosis vaccination strategies

Visai Muruganandah et al.

SCIENCE ADVANCES (2020)

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Article Biochemistry & Molecular Biology

Imbalanced Host Response to SARS-CoV-2 Drives Development of COVID-19

Daniel Blanco-Melo et al.

CELL (2020)

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Article Biochemistry & Molecular Biology

Mycobacterium tuberculosis Sulfolipid-1 Activates Nociceptive Neurons and Induces Cough

Cody R. Ruhl et al.

CELL (2020)

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Article Immunology

Simulation of the Clinical and Pathological Manifestations of Coronavirus Disease 2019 (COVID-19) in a Golden Syrian Hamster Model: Implications for Disease Pathogenesis and Transmissibility

Jasper Fuk-Woo Chan et al.

CLINICAL INFECTIOUS DISEASES (2020)

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Article Multidisciplinary Sciences

Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS-coronavirus 2

Jianzhong Shi et al.

SCIENCE (2020)

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Article Multidisciplinary Sciences

Mycobacterium tuberculosis associated with severe tuberculosis evades cytosolic surveillance systems and modulates IL-1β production

Jeremy Sousa et al.

NATURE COMMUNICATIONS (2020)

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Article Microbiology

The Diversity Outbred Mouse Population Is an Improved Animal Model of Vaccination against Tuberculosis That Reflects Heterogeneity of Protection

Sherry L. Kurtz et al.

MSPHERE (2020)

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Article Multidisciplinary Sciences

Pathogenesis and transmission of SARS-CoV-2 in golden hamsters

Sin Fun Sia et al.

NATURE (2020)

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Article Multidisciplinary Sciences

Respiratory disease in rhesus macaques inoculated with SARS-CoV-2

Vincent J. Munster et al.

NATURE (2020)

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Article Immunology

Mouse transcriptome reveals potential signatures of protection and pathogenesis in human tuberculosis

Lucia Moreira-Teixeira et al.

NATURE IMMUNOLOGY (2020)

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Article Pharmacology & Pharmacy

Protective Efficacy of Inhaled BCG Vaccination Against Ultra-Low Dose Aerosol M. tuberculosis Challenge in Rhesus Macaques

Andrew D. White et al.

PHARMACEUTICS (2020)

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Article Biochemistry & Molecular Biology

Severe COVID-19 Is Marked by a Dysregulated Myeloid Cell Compartment

Jonas Schulte-Schrepping et al.

CELL (2020)

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Article Biochemistry & Molecular Biology

A SARS-CoV-2 Infection Model in Mice Demonstrates Protection by Neutralizing Antibodies

Ahmed O. Hassan et al.

CELL (2020)

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Article Immunology

Mouse model of SARS-CoV-2 reveals inflammatory role of type I interferon signaling

Benjamin Israelow et al.

JOURNAL OF EXPERIMENTAL MEDICINE (2020)

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Article Immunology

Transient Lymphopenia and Interstitial Pneumonia With Endotheliitis in SARS-CoV-2-Infected Macaques

Bon-Sang Koo et al.

JOURNAL OF INFECTIOUS DISEASES (2020)

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Article Biochemistry & Molecular Biology

Vascular Disease and Thrombosis in SARS-CoV-2-Infected Rhesus Macaques

Malika Aid et al.

CELL (2020)

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Review Microbiology

ACTIVating Resources for the COVID-19 Pandemic: In Vivo Models for Vaccines and Therapeutics

Judith A. Hewitt et al.

CELL HOST & MICROBE (2020)

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Article Multidisciplinary Sciences

Syrian hamsters as a small animal model for SARS-CoV-2 infection and countermeasure development

Masaki Imai et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2020)

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Article Multidisciplinary Sciences

Primary exposure to SARS-CoV-2 protects against reinfection in rhesus macaques

Wei Deng et al.

SCIENCE (2020)

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Article Virology

Age-Dependent Progression of SARS-CoV-2 Infection in Syrian Hamsters

Nikolaus Osterrieder et al.

VIRUSES-BASEL (2020)

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Article Microbiology

CD11cHi monocyte-derived macrophages are a major cellular compartment infected by Mycobacterium tuberculosis

Jinhee Lee et al.

PLOS PATHOGENS (2020)

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Article Microbiology

SIV andMycobacterium tuberculosissynergy within the granuloma accelerates the reactivation pattern of latent tuberculosis

Collin R. Diedrich et al.

PLOS PATHOGENS (2020)

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Article Microbiology

Contained Mycobacterium tuberculosis infection induces concomitant and heterologous protection

Johannes Nemeth et al.

PLOS PATHOGENS (2020)

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Article Immunology

SARS-CoV-2-triggered neutrophil extracellular traps mediate COVID-19 pathology

Flavio Protasio Veras et al.

JOURNAL OF EXPERIMENTAL MEDICINE (2020)

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Type I IFN exacerbates disease in tuberculosis-susceptible mice by inducing neutrophil-mediated lung inflammation and NETosis

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Laboratory mice born to wild mice have natural microbiota and model human immune responses

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Alveolar macrophages generate a noncanonical NRF2-driven transcriptional response to Mycobacterium tuberculosis in vivo

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Goats Primed with Mycobacterium bovis BCG and Boosted with a Recombinant Adenovirus Expressing Ag85A Show Enhanced Protection against Tuberculosis

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Combination of Host Susceptibility and Virulence of Mycobacterium tuberculosis Determines Dual Role of Nitric Oxide in the Protection and Control of Inflammation

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Biphasic Kill Curve of Isoniazid Reveals the Presence of Drug-Tolerant, Not Drug-Resistant, Mycobacterium tuberculosis in the Guinea Pig

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Protection and Polyfunctional T Cells Induced by Ag85B-TB10.4/IC31® against Mycobacterium tuberculosis Is Highly Dependent on the Antigen Dose

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PLOS ONE (2009)

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2009)

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ESAT-6-specific CD4 T cell responses to aerosol Mycobacterium tuberculosis infection are initiated in the mediastinal lymph nodes

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2008)

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The American cotton rat: A novel model for pulmonary tuberculosis

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NK cell-derived IFN-γ differentially regulates innate resistance and neutrophil response in T cell-deficient hosts infected with Mycobacterium tuberculosis

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VACCINE (2006)

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Genetically determined susceptibility to tuberculosis in mice causally involves accelerated and enhanced recruitment of granulocytes

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CLINICAL AND VACCINE IMMUNOLOGY (2006)

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Dissection of ESAT-6 system 1 of Mycobacterium tuberculosis and impact on immunogenicity and virulence

P Brodin et al.

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Hypervirulent M-tuberculosis W/Beijing strains upregulate type IIFNs and increase expression of negative regulators of the Jak-Stat pathway

C Manca et al.

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Vaccine-induced cytokine responses in a guinea pig model of pulmonary tuberculosis

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Differential organization of the local immune response in patients with active cavitary tuberculosis or with nonprogressive tuberculoma

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Ipr1 gene mediates innate immunity to tuberculosis

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NATURE (2005)

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Fatal Mycobacterium tuberculosis infection despite adaptive immune response in the absence of MyD88

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ANNUAL REVIEW OF IMMUNOLOGY (2004)

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Human tuberculous granulomas induce peripheral lymphoid follicle-like structures to orchestrate local host defence in the lung

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Widespread bronchogenic dissemination makes DBA/2 mice more susceptible than C57BL/6 mice to experimental aerosol infection with Mycobacterium tuberculosis

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RESPIRATORY MEDICINE (2003)

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Coordinate cytokine gene expression in vivo following induction of tuberculous pleurisy in guinea pigs

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Immunopathogenesis of pulmonary granulomas in the guinea pig after infection with Mycobacterium tuberculosis

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INFECTION AND IMMUNITY (2003)

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Conservation of CD1 intracellular trafficking patterns between mammalian species

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Characterization of guinea-pig group 1 CD1 proteins

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Divergent effect of bacillus Calmette-Guerin (BCG) vaccination on Mycobacterium tuberculosis infection in highly related macaque species:: Implications for primate models in tuberculosis vaccine research

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2001)

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Depletion of alveolar macrophages exerts protective effects in pulmonary tuberculosis in mice

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Depletion of CD4+ T cells causes reactivation of murine persistent tuberculosis despite continued expression of interferon γ and nitric oxide synthase 2

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