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Applications of organoid technology to brain tumors

CNS NEUROSCIENCE & THERAPEUTICS (2023)

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Article Genetics & Heredity

Midbrain organoids mimic early embryonic neurodevelopment and recapitulate LRRK2-p.Gly2019Ser-associated gene expression

Alise Zagare et al.

Summary: Human brain organoids are a valuable tool for studying neurodegenerative diseases like Parkinson's disease. This study shows that the in vitro model of human midbrain organoids accurately recapitulates the developmental path and cellular composition of the in vivo midbrain. The researchers also discovered that a specific genetic variant affects neurodevelopment and identified potential candidate genes associated with this variant.

AMERICAN JOURNAL OF HUMAN GENETICS (2022)

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Article Cell Biology

Quiescent human glioblastoma cancer stem cells drive tumor initiation, expansion, and recurrence following chemotherapy

Xuanhua P. Xie et al.

Summary: This study confirms the existence of quiescent cancer stem cells in glioblastoma that can evade anti-proliferative therapies. By analyzing the functional characteristics of glioblastomas from genetically engineered mice, essential quiescent stem-like cells that can be directly isolated from tumors were identified. A specific gene expression signature related to quiescent cancer stem cells was found in both primary and recurrent human glioblastomas. These findings provide insights into the failure of conventional treatment and lay the foundation for alternative therapies.

DEVELOPMENTAL CELL (2022)

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Article Oncology

Effect of duty cycles of tumor-treating fields on glioblastoma cells and normal brain organoids

Eunbi Ye et al.

Summary: TTFields at 75% and 100% duty cycle can inhibit the proliferation and induce apoptosis of glioma cells. However, high duty cycle has higher neurotoxicity on normal brain organoids. These findings provide meaningful evidence for the further development of TTFields in cancer treatment.

INTERNATIONAL JOURNAL OF ONCOLOGY (2022)

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Article Medicine, General & Internal

Association Between Maternal Hormonal Contraception Use and Central Nervous System Tumors in Children

Marie Hargreave et al.

Summary: The incidence of central nervous system tumors in children in Denmark appears to be increasing, but few risk factors have been confirmed. This study found no significant association between maternal hormonal contraception use and the risk of central nervous system tumors in children.

JAMA-JOURNAL OF THE AMERICAN MEDICAL ASSOCIATION (2022)

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Article Oncology

Establishment of patient-derived organoid models of lower-grade glioma

Kalil G. Abdullah et al.

Summary: An optimized protocol was developed to establish organoids from LGG primary tissue samples, producing the first suite of these models. Patient-derived organoids recapitulated key biological features of their respective parental tumor specimens, demonstrating fidelity and potential for preclinical studies and personalized treatment assessments.

NEURO-ONCOLOGY (2022)

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Article Multidisciplinary Sciences

Amplification of human interneuron progenitors promotes brain tumors and neurological defects

Oliver L. Eichmueller et al.

Summary: The evolutionary development of the human brain involves the expansion of different brain regions. This study focuses on the specific developmental processes in humans that lead to malformations of cortical development, resulting in developmental delay and epilepsy in children. By creating a human cerebral organoid model for tuberous sclerosis complex (TSC), researchers identified a neural stem cell type called caudal late interneuron progenitor (CLIP) cells that overproliferate in TSC, leading to excessive interneurons, brain tumors, and cortical malformations. Inhibiting the epidermal growth factor receptor has potential therapeutic effects for TSC and related disorders. The discovery of CLIP cells highlights the vulnerability to disease in the extended generation of interneurons in the human brain, while also demonstrating the importance of analyzing malformations of cortical development in gaining insights into human-specific aspects of brain development.

SCIENCE (2022)

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Article Oncology

Three-dimensional organoid culture unveils resistance to clinical therapies in adult and pediatric glioblastoma

Swetha J. Sundar et al.

Summary: This study utilizes GBM organoid culture system to explore drug resistance, revealing diverse and spatial patterns of cell proliferation as well as relative insensitivity to conventional therapy, highlighting the potential of organoid cultures in understanding therapeutic mechanisms.

TRANSLATIONAL ONCOLOGY (2022)

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Article Multidisciplinary Sciences

Expression of the transcription factor PU.1 induces the generation of microglia-like cells in human cortical organoids

Bilal Cakir et al.

Summary: The study develops a method to generate functional microglia in human cortical organoids and investigates their role in amyloid-beta-induced inflammation. It provides insights into the function of microglia in neurodevelopmental and neurodegenerative disorders.

NATURE COMMUNICATIONS (2022)

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Article Oncology

MEOX2 homeobox gene promotes growth of malignant gliomas

Anna Schoenrock et al.

Summary: In this study, the researchers identified MEOX2 as an oncogenic transcription regulator in GBM. MEOX2 enhances ERK signaling through a feed-forward mechanism and increases cell proliferation in GBM cerebral organoid models.

NEURO-ONCOLOGY (2022)

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Article Oncology

Glioblastoma-Derived Three-Dimensional Ex Vivo Models to Evaluate Effects and Efficacy of Tumor Treating Fields (TTFields)

Vera Nickl et al.

Summary: In glioblastoma treatment, tumor recurrence is common and prognosis is poor. TTFields have shown efficacy, but their molecular effects in patient tissue samples have not been well studied. This study presents three reliable three-dimensional ex vivo models that can predict patients' treatment responses and provide insights into important cellular and molecular alterations under TTFields.

CANCERS (2022)

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Review Cell & Tissue Engineering

Engineering Brain Organoids: Toward Mature Neural Circuitry with an Intact Cytoarchitecture

Hyunsoo Jang et al.

Summary: The emergence of brain organoids as a model system has provided exciting opportunities for studying human-specific neurogenesis. However, current culture methods need improvement to achieve levels similar to an in vivo human developing brain.

INTERNATIONAL JOURNAL OF STEM CELLS (2022)

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Review Pharmacology & Pharmacy

Tumor organoid models in precision medicine and investigating cancer-stromal interactions

Ren Xu et al.

Summary: Tumor development and progression rely on signals from the tumor microenvironment, and recent advances in 3D culture and patient-derived tumor organoid models provide valuable tools for studying cancer development, treatment, and drug response.

PHARMACOLOGY & THERAPEUTICS (2021)

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Article Cell Biology

The epidermal growth factor receptor variant type III mutation frequently found in gliomas induces astrogenesis in human cerebral organoids

Hyun-Mun Kim et al.

Summary: The study found that EGFRvIII mutation promotes astrogenesis and cell proliferation while inhibiting neurogenesis in a human brain development model. These results provide new insights into the mechanisms of EGFRvIII mutation-mediated gliogenesis and gliomagenesis.

CELL PROLIFERATION (2021)

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Article Biochemistry & Molecular Biology

Biobanked Glioblastoma Patient-Derived Organoids as a Precision Medicine Model to Study Inhibition of Invasion

Emilie Darrigues et al.

Summary: This study screened potential GBM therapeutic drugs using patient-derived 3D models, finding that tubulin inhibitor had the best efficacy in U-251 MG cells but showed highly variable results in patient organoids. The efficacy of compounds was found to be closely related to patient tumor heterogeneity, suggesting that such models can be used to evaluate individualized cancer treatment strategies.

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2021)

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Article Biochemistry & Molecular Biology

Assessment of Normal Tissue Radiosensitivity by Evaluating DNA Damage and Repair Kinetics in Human Brain Organoids

Jovana Bojcevski et al.

Summary: This study explored the generation of normal brain 3D organoids from human induced pluripotent stem cells combined with detection of DNA damage repair for developing personalized models to determine normal tissue radiosensitivity. The findings suggest that assessment of DNA damage repair kinetics in hiPSC derived cerebral organoids is feasible and further development may lead to personalized assessment of radiosensitivity in healthy neuronal tissue.

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2021)

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Article Clinical Neurology

Establishment and characterization of meningioma patient-derived organoid

Henry Siu Cheung Chan et al.

Summary: 2D cell culture is widely used in tumor research, but may not fully replicate the in vivo tumor structure. Organoid culture is seen as an alternative platform due to its ability to better model tumors. This study established a protocol for culturing cells from patient meningioma tissue in vitro 3D environment, demonstrating the feasibility and potential of organoid technology for meningioma research.

JOURNAL OF CLINICAL NEUROSCIENCE (2021)

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Article Oncology

Proteogenomic and metabolomic characterization of human glioblastoma

Liang-Bo Wang et al.

Summary: Understanding the molecular pathogenesis of glioblastoma is crucial for improving diagnosis and treatment. Integrated analysis of genomic, proteomic, and metabolomic data on treatment-naive glioblastomas has identified key phosphorylation events and potential targets for specific tumor alterations. Immune subtypes with distinct immune cell types were discovered, and specific histone acetylation patterns were correlated with these subtypes, providing insights for stratification of patients for more effective treatment.

CANCER CELL (2021)

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Article Oncology

A novel integrated system using patient-derived glioma cerebral organoids and xenografts for disease modeling and drug screening

Liyang Zhang et al.

Summary: Researchers developed an integrated system using patient-derived glioma cerebral organoids and xenograft models to understand glioma biology and predict response to chemotherapy drugs, providing a new strategy for personalized treatment of this deadly disease.

CANCER LETTERS (2021)

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Article Virology

Effect of Serial Systemic and Intratumoral Injections of Oncolytic ZIKVBR in Mice Bearing Embryonal CNS Tumors

Raiane Oliveira Ferreira et al.

Summary: Research indicates that the Zika virus has potential oncolytic effects against embryonal CNS tumors, with different administration routes and virus load playing crucial roles in treatment safety and effectiveness. Systemic injections of ZIKV(BR) showed tropism to the brain in mice with subcutaneous tumors, and serial injections at the site of brain tumor effectively destroyed the tumor without causing neurological or organ damage, leading to increased survival rates in mice.

VIRUSES-BASEL (2021)

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Article Multidisciplinary Sciences

Comparative epigenetic analysis of tumour initiating cells and syngeneic EPSC-derived neural stem cells in glioblastoma

Claire Vinel et al.

Summary: This study compares patient-matched glioma-initiating cells with neural stem cells, enabling the discovery of patient-specific disease mechanisms and identification of effective drugs.

NATURE COMMUNICATIONS (2021)

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Article Multidisciplinary Sciences

The novel BET inhibitor UM-002 reduces glioblastoma cell proliferation and invasion

Anna M. Jermakowicz et al.

Summary: UM-002 is a novel brain-penetrant BET inhibitor that reduces GBM cell proliferation and alters the transcriptional landscape of GBM tumors. It shows potential for GBM treatment and provides important insights for designing combination therapies.

SCIENTIFIC REPORTS (2021)

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Article Biochemistry & Molecular Biology

A Drug Screening Pipeline Using 2D and 3D Patient-Derived In Vitro Models for Pre-Clinical Analysis of Therapy Response in Glioblastoma

Sakthi Lenin et al.

Summary: This study conducted a systematic review on the molecular mechanisms driving glioblastoma progression, identifying 65 drugs/inhibitors for screening their efficacy on patient-derived glioma stem cells. Costunolide, a TERT inhibitor, was found effective in reducing cell viability in both primary and pre-treated tumor models. This novel workflow could lead to personalized and effective treatment for recurrent glioblastoma.

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2021)

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Review Biology

Towards organoid culture without Matrigel

Mark T. Kozlowski et al.

Summary: Organoids, cellular aggregates derived from stem or progenitor cells that recapitulate organ function in miniature, have gained growing interest in developmental biology and medicine. This review discusses promising alternatives to Matrigel for the generation and maintenance of organoids, utilizing decellularized ECM, synthetic hydrogels, and gel-forming recombinant proteins.

COMMUNICATIONS BIOLOGY (2021)

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Review Cell Biology

The Role of Neurodevelopmental Pathways in Brain Tumors

Rachel N. Curry et al.

Summary: Disruptions in developmental cell signaling pathways and transcriptional cascades are linked to tumor progression; resurgence of aberrant neurodevelopmental programs shares similarities with developmental and oncologic mechanisms; understanding how dysregulated developmental factors contribute to brain tumor oncogenesis and disease progression can help identify therapeutic targets.

FRONTIERS IN CELL AND DEVELOPMENTAL BIOLOGY (2021)

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Review Oncology

Patient-derived organoids as a predictive biomarker for treatment response in cancer patients

G. Emerens Wensink et al.

Summary: This study focuses on the use of patient-derived organoids (PDOs) as a potential predictive biomarker in the treatment of cancer patients, emphasizing the importance of individualized tumor response testing.

NPJ PRECISION ONCOLOGY (2021)

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Article Oncology

Brain and other central nervous system tumor statistics, 2021

Kimberly D. Miller et al.

Summary: Brain and other CNS tumors are highly fatal cancers in the United States, with different incidence rates and survival rates among different races and age groups. Survival disparities, especially in childhood tumors, highlight the importance of providing more resources to advance research and understand the reasons behind differences in brain tumor occurrence, especially among rarer subtypes and understudied populations.

CA-A CANCER JOURNAL FOR CLINICIANS (2021)

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Article Oncology

Newly established patient-derived organoid model of intracranial meningioma

Shintaro Yamazaki et al.

Summary: This study established 18 organoid models of meningiomas and identified upregulated FOXM1 as a potential treatment target for meningioma. Overexpression of FOXM1 in benign meningiomas increased proliferation, while depletion of FOXM1 in malignant meningiomas decreased proliferation. FOXM1 inhibitor thiostrepton combined with radiation therapy significantly inhibited the proliferation of malignant meningioma organoid models.

NEURO-ONCOLOGY (2021)

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Article Multidisciplinary Sciences

Microfluidic device with brain extracellular matrix promotes structural and functional maturation of human brain organoids

Ann-Na Cho et al.

Summary: This study demonstrates the use of human brain extracellular matrix and a microfluidic device to improve human brain organoid culture, resulting in enhanced neurogenesis and structural and functional maturation of the organoids.

NATURE COMMUNICATIONS (2021)

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Article Clinical Neurology

Innovations in Neuro-Oncology

Rajiv S. Magge et al.

Summary: Significant advances have been made in understanding and treating brain tumors, with molecular profiling, cerebral organoid development, and new radiology techniques improving clinical practice. Adaptive trial platforms are rapidly testing therapies and biomarkers with good scientific rationale, while the growth of neuro-oncology clinical care teams aims to enhance patient outcomes and symptoms.

WORLD NEUROSURGERY (2021)

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Article Cell Biology

A pan-cancer organoid platform for precision medicine

Brian M. Larsen et al.

Summary: A robust pan-cancer tumor organoid platform with chemically defined media has been established and neural-network-based high-throughput method has been demonstrated to predict patient-specific heterogeneity in drug responses. These resources are expected to accelerate the broad implementation of organoid models in precision medicine research and personalized therapeutic profiling programs.

CELL REPORTS (2021)

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Article Cell & Tissue Engineering

Generation of caudal-type serotonin neurons and hindbrain-fate organoids from hPSCs

Parvin Valiulahi et al.

Summary: This study introduces a novel strategy to generate hindbrain 5-HT neurons from human pluripotent stem cells, achieving successful conversion of 30%-40% of cells. By utilizing a caudalizing agent, the majority of cells acquired a caudal identity. The research also optimized the differentiation system to generate organoid cultures enriched with 5-HT neurons.

STEM CELL REPORTS (2021)

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Article Immunology

The N6-Methyladenosine-Modified Pseudogene HSPA7 Correlates With the Tumor Microenvironment and Predicts the Response to Immune Checkpoint Therapy in Glioblastoma

Rongrong Zhao et al.

Summary: By studying the lncRNA m(6)A modification patterns in GBM tissues, we identified HSPA7 as a novel prognostic risk factor in GBM patients, playing important roles in immunophenotype and tumor microenvironment. We also confirmed the impact of HSPA7 on macrophage infiltration and the efficacy of ICB therapy.

FRONTIERS IN IMMUNOLOGY (2021)

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Article Neurosciences

Altered lipid metabolism marks glioblastoma stem and non-stem cells in separate tumor niches

Sajina Shakya et al.

Summary: Glioblastoma displays significant cellular and metabolic heterogeneity, with striking differences in lipid metabolism across different microenvironments, and cancer stem cells (CSCs) also show altered lipid metabolism. The differences in lipid metabolism may not only be a product of the microenvironment, but also a reflection of cellular state, providing new insights into therapeutic targets for GBM.

ACTA NEUROPATHOLOGICA COMMUNICATIONS (2021)

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Article Oncology

PTEN deficiency leads to proteasome addiction: a novel vulnerability in glioblastoma

Jorge A. Benitez et al.

Summary: The study identified a potential therapeutic strategy for GBM by targeting proteasome inhibition, which showed high sensitivity in GSCs due to their reliance on increased protein synthesis rate and loss of autophagy. Combinatorial inhibition of proteasome and autophagy resulted in enhanced cytotoxicity in PTEN-expressing GSCs, suggesting a synthetic lethal approach for this subset of GBM patients.

NEURO-ONCOLOGY (2021)

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Article Cell Biology

Brain Organoids: A Promising Living Biobank Resource for Neuroscience Research

Shuang Li et al.

BIOPRESERVATION AND BIOBANKING (2020)

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Article Biochemistry & Molecular Biology

A Patient-Derived Glioblastoma Organoid Model and Biobank Recapitulates Inter- and Intra-tumoral Heterogeneity

Fadi Jacob et al.

CELL (2020)

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Article Cell & Tissue Engineering

Zika Virus Targets Glioblastoma Stem Cells through a SOX2-Integrin αvβ5 Axis

Zhe Zhu et al.

CELL STEM CELL (2020)

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Article Multidisciplinary Sciences

Modeling medulloblastoma in vivo and with human cerebellar organoids

Claudio Ballabio et al.

NATURE COMMUNICATIONS (2020)

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Review Oncology

Patient-Derived Orthotopic Xenograft Models of Pediatric Brain Tumors: In a Mature Phase or Still in Its Infancy?

Eva Hermans et al.

FRONTIERS IN ONCOLOGY (2020)

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Hypothalamic Contribution to Pituitary Functions Is Recapitulated In Vitro Using 3D-Cultured Human iPS Cells

Takatoshi Kasai et al.

CELL REPORTS (2020)

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Shengchao Xu et al.

CANCER LETTERS (2020)

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Sliced Human Cortical Organoids for Modeling Distinct Cortical Layer Formation

Xuyu Qian et al.

CELL STEM CELL (2020)

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Celine S. Goncalves et al.

CELLULAR AND MOLECULAR LIFE SCIENCES (2020)

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Immersion Bioprinting of Tumor Organoids in Multi-Well Plates for Increasing Chemotherapy Screening Throughput

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Patient-derived tumor organoid predicts drugs response in glioblastoma: A step forward in personalized cancer therapy?

Herbert H-F Loong et al.

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Human iPSC-Derived Neurons and Cerebral Organoids Establish Differential Effects of Germline NF1 Gene Mutations

Corina Anastasaki et al.

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Teresa G. Krieger et al.

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Rapid Processing and Drug Evaluation in Glioblastoma Patient-Derived Organoid Models with 4D Bioprinted Arrays

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ISCIENCE (2020)

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Multiplatform genomic profiling and magnetic resonance imaging identify mechanisms underlying intratumor heterogeneity in meningioma

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CRISPRi-based radiation modifier screen identifies long non-coding RNA therapeutic targets in glioma

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Cerebral organoids at the air-liquid interface generate diverse nerve tracts with functional output

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A bioprinted human-glioblastoma-on-a-chip for the identification of patient-specific responses to chemoradiotherapy

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Specification of positional identity in forebrain organoids

Gustav Y. Cederquist et al.

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Gene signatures of quiescent glioblastoma cells reveal mesenchymal shift and interactions with niche microenvironment

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Quinn T. Ostrom et al.

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Humsa S. Venkatesh et al.

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Synaptic proximity enables NMDAR signalling to promote brain metastasis

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Complex Oscillatory Waves Emerging from Cortical Organoids Model Early Human Brain Network Development

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NPI-0052 and γ-radiation induce a synergistic apoptotic effect in medulloblastoma

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C-Myc and β-catenin cooperate with loss of p53 to generate multiple members of the primitive neuroectodermal tumor family in mice

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