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Ubiquitin Engineering for Interrogating the Ubiquitin-Proteasome System and Novel Therapeutic Strategies

CELLS (2023)

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Article Biochemistry & Molecular Biology

Molecular Glues: The Adhesive Connecting Targeted Protein Degradation to the Clinic

Janet M. Sasso et al.

Summary: Targeted protein degradation is an emerging drug discovery strategy that utilizes small molecules to selectively degrade disease-causing proteins, particularly those that are difficult to target. The advent of molecular glue-type protein degraders has simplified and strengthened the connection between E3 ligases and disease-causing proteins, leading to the development of new therapies for unmet medical needs. This paper provides comprehensive insights into targeted protein degraders, with a focus on molecular glues, and discusses their advantages and the advances in drug discovery practices for these degraders.

BIOCHEMISTRY (2023)

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Article Multidisciplinary Sciences

Development of a versatile nuclease prime editor with upgraded precision

Xiangyang Li et al.

Summary: Strategies to improve the specificity of nuclease-based prime editor (PEn) are needed. Here the authors report a 53BP1-inhibitory ubiquitin variant-assisted PEn platform (uPEn) to inhibit NHEJ and enable precise prime editing for generation of insertions, deletions, and replacements.

NATURE COMMUNICATIONS (2023)

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Article Medicine, Research & Experimental

Suppression of USP7 negatively regulates the stability of ETS proto-oncogene 2 protein

Hong-Beom Park et al.

Summary: Ubiquitin-specific protease 7 (USP7) is a deubiquitinating enzyme that removes mono and polyubiquitin chains from target proteins. It has opposing roles as an oncogene or tumor suppressor in different cancer types. USP7 is involved in various cellular processes such as cell cycle, apoptosis, DNA repair, chromatin remodeling, and epigenetic regulation, through deubiquitination of substrates including p53, MDM2, Myc, and PTEN. In this study, a novel substrate of USP7 was identified and its potential role in cancer related to ETS2 dysregulation was proposed.

BIOMEDICINE & PHARMACOTHERAPY (2023)

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Article Oncology

Over-expression of USP15/MMP3 predict poor prognosis and promote growth, migration in non-small cell lung cancer cells

Weiwei Chen et al.

Summary: Aberrant ubiquitin modifications caused by an imbalance in the activities of ubiquitinases and de-ubiquitinases are important mechanisms underlying non-small cell lung cancer (NSCLC) progression. The deubiquitinating enzyme USP15 plays a key role in NSCLC tumorigenesis and is a potential therapeutic target. Knocking down USP15 expression in NSCLC cells leads to suppressed cell proliferation, reduced migration and invasion abilities, and decreased tumor size in animal models. USP15 knockdown also inhibits the expression of MMP3 and MMP9, and high levels of USP15 and MMP3 are associated with poor prognosis in NSCLC.

CANCER GENETICS (2023)

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Article Multidisciplinary Sciences

TRAF6 as a potential target in advanced breast cancer: a systematic review, meta-analysis, and bioinformatics validation

Feier Zeng et al.

Summary: TRAF6 has been identified as a key regulator in breast cancer. Inhibition of TRAF2/4 or TRAF6 reduces BCa cell migration and invasion, with only TRAF6 inhibition reducing cell growth. Animal models and studies in BCa patients support these findings. Overall, TRAF6 inhibitors show promise for the treatment of metastatic BCa, although limited study numbers and scarcity of evidence from animal and human studies may hinder clinical translation.

SCIENTIFIC REPORTS (2023)

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Article Oncology

USP15 Represses Hepatocellular Carcinoma Progression by Regulation of Pathways of Cell Proliferation and Cell Migration: A System Biology Analysis

Yiyue Ren et al.

Summary: Expression levels of USP15 are associated with slow proliferation and migration of HCC cells. High expression of USP15 in tumor tissue is associated with decreased risk of mortality and cancer relapse in HCC patients. USP15 regulates tumor-related proteins indirectly through protein interactions.

CANCERS (2023)

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Review Multidisciplinary Sciences

TRAF6 as a potential target in advanced breast cancer: a systematic review, meta-analysis, and bioinformatics validation

Feier Zeng et al.

Summary: TRAF6 has emerged as a key regulator of breast cancer (BCa), and the inhibition of TRAF6 shows promise in the treatment of metastatic BCa. However, the low number of studies and scarcity of evidence from animal and human studies may limit the translation of these findings into clinical practice.

SCIENTIFIC REPORTS (2023)

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Article Biochemistry & Molecular Biology

The E2 ubiquitin-conjugating enzyme HIP2 is a crucial regulator of quality control against mutant SOD1 proteotoxicity

Yeong Jin Tak et al.

Summary: HIP2 interacts with mutant SOD1 and mediates its degradation through the ubiquitin-proteasome system, protecting cells from mutant SOD1-induced toxicity. Modulating HIP2 may represent a novel therapeutic strategy for the treatment of ALS.

BIOCHIMICA ET BIOPHYSICA ACTA-MOLECULAR BASIS OF DISEASE (2022)

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Review Biotechnology & Applied Microbiology

PROTAC targeted protein degraders: the past is prologue

Miklos Bekes et al.

Summary: Targeted protein degradation (TPD) is a new therapeutic modality that can tackle disease-causing proteins which are difficult to target with conventional small molecules. PROTAC molecules, utilizing the ubiquitin-proteasome system to degrade target proteins, has achieved clinical proof-of-concept and attracted significant industry activity. Future directions include identifying target classes suitable for TPD, expanding the use of ubiquitin ligases for precision medicine, and extending the modality beyond oncology.

NATURE REVIEWS DRUG DISCOVERY (2022)

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Article Biochemistry & Molecular Biology

Rational Development and Characterization of a Ubiquitin Variant with Selectivity for Ubiquitin C-Terminal Hydrolase L3

Chad S. Hewitt et al.

Summary: This study demonstrates the successful design of a selective activity-based probe for UCHL3, which shows high selectivity and potency in cellular assays.

BIOMOLECULES (2022)

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Article Biochemistry & Molecular Biology

Panel of Engineered Ubiquitin Variants Targeting the Family ofHuman Ubiquitin Interacting Motifs

Gianluca Veggiani et al.

Summary: Researchers have developed Ub variants that bind to 42 UIMs with high affinity and specificity. The structural analysis of a UbV:UIM complex has revealed the molecular determinants of enhanced affinity and specificity. Furthermore, they have demonstrated that a UbV targeting a UIM in the cancer-associated Ub-specific protease 28 can effectively inhibit its catalytic activity. This study highlights the versatility of UbVs in targeting short alpha-helical Ub receptors and provides a strategy for the systematic development of probes for Ub-binding domains.

ACS CHEMICAL BIOLOGY (2022)

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Article Cell Biology

USP15 negatively regulates lung cancer progression through the TRAF6-BECN1 signaling axis for autophagy induction

Mi-Jeong Kim et al.

Summary: The study reveals that USP15 is significantly downregulated in lung cancer patients, and its knockout leads to increased migration, invasion, and autophagy induction in lung cancer cells. USP15 interacts with BECN1 and deubiquitinates it, thereby attenuating autophagy induction. Additionally, the expression of USP15 is associated with the upregulation of certain oncogenes and downregulation of tumor suppressor genes in lung cancer patients.

CELL DEATH & DISEASE (2022)

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Article Biochemistry & Molecular Biology

Targeted Degradation of 53BP1 Using Ubiquitin Variant Induced Proximity

Bayonle Aminu et al.

Summary: The Ubiquitin Variant Induced Proximity (UbVIP) technology allows for targeted degradation of proteins, showing potential as a therapeutic approach for human diseases. By utilizing synthetic UbV binders and designing multi-domain fusion proteins, researchers were able to induce proteasomal degradation of a nucleus-localized protein 53BP1. This study demonstrates the suitability of UbV technology for developing protein-based molecules for targeted degradation and identifying novel E3 ligases.

BIOMOLECULES (2022)

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Article Biochemistry & Molecular Biology

A Designer Nanoparticle Platform for Controlled Intracellular Delivery of Bioactive Macromolecules: Inhibition of Ubiquitin-Specific Protease 7 in Breast Cancer Cells

Wynton D. McClary et al.

Summary: Biological therapeutics are important in new drug development, however, the controlled intracellular delivery of biologics remains a challenge. In this study, a semi-synthetic particle platform was developed to achieve controlled intracellular delivery of biological macromolecules. The platform was shown to effectively deliver an inhibitor of USP7, a potential target for cancer treatment, into specific cells. The internalized particles retained their therapeutic activity and impacted the metabolic and proteomic landscapes of the cells.

ACS CHEMICAL BIOLOGY (2022)

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Article Microbiology

Ubiquitin variants potently inhibit SARS-CoV-2 PLpro and viral replication via a novel site distal to the protease active site

Vera J. E. van Vliet et al.

Summary: In this study, researchers have identified ubiquitin variants (UbVs) that can specifically and effectively block the activity of the papain-like protease (PLpro) in SARS-CoV-2. These UbVs inhibit the essential cleavage activities of the protease, reducing viral replication and providing a potential therapeutic approach for combating coronaviruses.

PLOS PATHOGENS (2022)

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Review Biochemistry & Molecular Biology

Structural and Functional Basis of JAMM Deubiquitinating Enzymes in Disease

Xin Pan et al.

Summary: Deubiquitinating enzymes (DUBs) are proteases that maintain cell homeostasis by regulating ubiquitination and deubiquitination. JAB1/MPN/Mov34 metalloenzymes (JAMMs), the only known metalloproteinase family of DUBs, are specifically associated with tumorigenesis and immunological and inflammatory diseases. JAMMs' smaller numbers and distinct catalytic mechanism make them attractive drug targets. Several JAMM inhibitors have been developed and show promising therapeutic efficacy, setting the stage for potential treatments of various diseases.

BIOMOLECULES (2022)

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Review Biochemistry & Molecular Biology

Targeted protein degradation: mechanisms, strategies and application

Lin Zhao et al.

Summary: Traditional drug discovery focuses on direct regulation of protein activity. However, the emerging targeted protein degradation (TPD) technologies, such as PROTAC, provide potential approaches to remove disease-associated proteins by utilizing cells' degradation machinery. These TPD strategies, including molecular glue, LYTAC, and AbTAC, expand the scope of TPD and offer fresh insights into drug discovery.

SIGNAL TRANSDUCTION AND TARGETED THERAPY (2022)

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Therapeutic peptides: current applications and future directions

Lei Wang et al.

Summary: Peptide drug development has achieved significant progress in the past decade, thanks to new production, modification, and analytic technologies. These advancements have addressed the inherent limitations of peptides and have resulted in achievements in various therapeutic areas.

SIGNAL TRANSDUCTION AND TARGETED THERAPY (2022)

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Article Biochemistry & Molecular Biology

Structural and functional characterization of ubiquitin variant inhibitors for the JAMM-family deubiquitinases STAMBP and STAMBPL1

Yusong Guo et al.

Summary: Ubiquitination is a crucial posttranslational protein modification involved in various biological pathways, and studies have focused on targeting deubiquitinases (DUBs) for drug discovery. This research utilized a phage display-based protein engineering strategy to develop UbV inhibitors targeting STAMBP, a member of the JAMM metalloprotease family. Two high-affinity UbVs were identified and the structure of the STAMBPL1-UbV(SP.1) complex was determined by X-ray crystallography, revealing the interaction hotspots. The UbV inhibitors were shown to be potent inhibitors of STAMBP isopeptidase activity, surpassing existing small-molecule inhibitors.

JOURNAL OF BIOLOGICAL CHEMISTRY (2021)

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Article Chemistry, Medicinal

Structure-Activity Relationship of USP5 Inhibitors

Mandeep K. Mann et al.

Summary: A chemical probe targeting USP5 has been developed and shown to competitively inhibit the enzyme's catalytic activity by occupying the C-terminal ubiquitin-binding site. Compound 64 has high binding affinity to USP5 and selectivity over other proteins, providing a potential tool for elucidating the function of USP5 in cells.

JOURNAL OF MEDICINAL CHEMISTRY (2021)

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Article Biochemistry & Molecular Biology

A Panel of Engineered Ubiquitin Variants Targeting the Family of Domains Found in Ubiquitin Specific Proteases (DUSPs)

Jason Q. Tang et al.

Summary: Domains found in ubiquitin specific proteases (DUSPs) occur in seven members of the ubiquitin specific protease (USP) family, which are defined by a distinct structural fold. By designing UbV libraries, protein-based tools can target DUSP family members with high affinity and specificity, potentially providing an alternative means of inhibiting USP activity.

JOURNAL OF MOLECULAR BIOLOGY (2021)

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Review Neurosciences

Exploration of Aberrant E3 Ligases Implicated in Alzheimer's Disease and Development of Chemical Tools to Modulate Their Function

Frances M. Potjewyd et al.

Summary: The Ubiquitin Proteasome System (UPS) is responsible for degrading misfolded or aggregated proteins through an ATP-dependent proteolytic mechanism. Dysfunction of the UPS is commonly observed in neurodegenerative diseases like Alzheimer's disease (AD), driving disease pathology and contributing to hallmarks of AD like amyloid-beta accumulation and tau hyperphosphorylation. E3 ligases, key members of the UPS machinery, play a crucial role in AD pathology, and their dysregulation can lead to aberrant processes that propagate the disease.

FRONTIERS IN CELLULAR NEUROSCIENCE (2021)

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Article Biochemistry & Molecular Biology

Identification of Ubiquitin Variants That Inhibit the E2 Ubiquitin Conjugating Enzyme, Ube2k

Adam J. Middleton et al.

Summary: This study identified protein-based reagents called UbVs that bind tightly to Ube2k, inhibiting its function. The unique binding site of UbVs suggests a potential target for inhibiting Ube2k and other E2 enzymes. Crystal structures revealed the mechanisms of UbVs blocking both ubiquitin charging of the E2 enzyme and E3-catalyzed ubiquitin transfer.

ACS CHEMICAL BIOLOGY (2021)

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Article Biochemical Research Methods

Engineering Single Pan-Specific Ubiquibodies for Targeted Degradation of All Forms of Endogenous ERK Protein Kinase

Erin A. Stephens et al.

Summary: Ubiquibodies are a customizable proteome editing technology that uses E3 ubiquitin ligases fused to synthetic binding proteins to degrade proteins of interest at the proteasome. Engineered uAbs can accelerate protein turnover, aiding in the study of cellular protein properties.

ACS SYNTHETIC BIOLOGY (2021)

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Review Biochemistry & Molecular Biology

E3 ubiquitin ligases: styles, structures and functions

Quan Yang et al.

Summary: E3 ubiquitin ligases are key enzymes in the ubiquitination process, playing a crucial role in transferring ubiquitin protein to the lysine site of targeted substrates. Their importance in regulating cellular activities and responding to cancer development is increasingly recognized.

MOLECULAR BIOMEDICINE (2021)

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Review Biochemistry & Molecular Biology

An E3 ligase guide to the galaxy of small-molecule-induced protein degradation

Predrag Jevtic et al.

Summary: Induced protein degradation involves elimination of pathological proteins by modifying them with ubiquitin chains through molecular glues or bivalent compounds that induce proximity to E3 ligases. The human genome encodes around 600 E3 ligases with diverse structures, catalytic mechanisms, and physiological roles. While some E3 ligases have been successfully targeted for drug discovery, there are still many new ubiquitylation enzymes that hold potential for therapeutic applications.

CELL CHEMICAL BIOLOGY (2021)

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Review Biochemistry & Molecular Biology

Viral vector platforms within the gene therapy landscape

Jote T. Bulcha et al.

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SIGNAL TRANSDUCTION AND TARGETED THERAPY (2021)

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Proteasome Inhibitor Drugs

Lloyd D. Fricker

ANNUAL REVIEW OF PHARMACOLOGY AND TOXICOLOGY, VOL 60 (2020)

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Structural and Functional Analysis of Ubiquitin-based Inhibitors That Target the Backsides of E2 Enzymes

Pankaj Garg et al.

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SEMINARS IN CANCER BIOLOGY (2020)

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Jing Xie et al.

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Relinde I. Y. Lieverse et al.

MOLECULAR ONCOLOGY (2020)

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Development of Ubiquitin Variants with Selectivity for Ubiquitin C-Terminal Hydrolase Deubiquitinases

Chad S. Hewitt et al.

BIOCHEMISTRY (2020)

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The role of ubiquitination in tumorigenesis and targeted drug discovery

Lu Deng et al.

SIGNAL TRANSDUCTION AND TARGETED THERAPY (2020)

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Resolving the Complexity of Ubiquitin Networks

Katarzyna Kliza et al.

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Yeast Two-Hybrid Analysis for Ubiquitin Variant Inhibitors of Human Deubiquitinases

Natasha Pascoe et al.

JOURNAL OF MOLECULAR BIOLOGY (2019)

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Dimerization of a ubiquitin variant leads to high affinity interactions with a ubiquitin interacting motif

Noah Manczyk et al.

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Structural and Functional Characterization of Ubiquitin Variant Inhibitors of USP15

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The deubiquitylating enzyme USP15 regulates homologous recombination repair and cancer cell response to PARP inhibitors

Yihan Peng et al.

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Protein engineering of a ubiquitin-variant inhibitor of APC/C identifies a cryptic K48 ubiquitin chain binding site

Edmond R. Watson et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2019)

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Inhibition of 53BP1 favors homology-dependent DNA repair and increases CRISPR-Cas9 genome-editing efficiency

Marella D. Canny et al.

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A Structure-Based Strategy for Engineering Selective Ubiquitin Variant Inhibitors of Skp1-Cul1-F-Box Ubiquitin Ligases

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Control of CCND1 ubiquitylation by the catalytic SAGA subunit USP22 is essential for cell cycle progression through G1 in cancer cells

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2018)

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Reduction of HIP2 expression causes motor function impairment and increased vulnerability to dopaminergic degeneration in Parkinson's disease models

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Generation and Validation of Intracellular Ubiquitin Variant Inhibitors for USP7 and USP10

Wei Zhang et al.

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A Highly Diverse and Functional Naive Ubiquitin Variant Library for Generation of Intracellular Affinity Reagents

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Mads Gabrielsen et al.

MOLECULAR CELL (2017)

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Targeting the deubiquitinase STAMBP inhibits NALP7 inflammasome activity

Joseph S. Bednash et al.

NATURE COMMUNICATIONS (2017)

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Potent and selective inhibition of pathogenic viruses by engineered ubiquitin variants

Wei Zhang et al.

PLOS PATHOGENS (2017)

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Mechanism and disease association of E2-conjugating enzymes: lessons from UBE2T and UBE2L3

Arno F. Alpi et al.

BIOCHEMICAL JOURNAL (2016)

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Divergence in Ubiquitin Interaction and Catalysis among the Ubiquitin-Specific Protease Family Deubiquitinating Enzymes

Adam H. Tencer et al.

BIOCHEMISTRY (2016)

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E2 enzymes: more than just middle men

Mikaela D. Stewart et al.

CELL RESEARCH (2016)

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Kirby N. Swatek et al.

CELL RESEARCH (2016)

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System-Wide Modulation of HECT E3 Ligases with Selective Ubiquitin Variant Probes

Wei Zhang et al.

MOLECULAR CELL (2016)

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Inhibition of SCF ubiquitin ligases by engineered ubiquitin variants that target the Cul1 binding site on the Skp1-F-box interface

Maryna Gorelik et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2016)

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Emerging Potential of Therapeutic Targeting of Ubiquitin-Specific Proteases in the Treatment of Cancer

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CANCER RESEARCH (2014)

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TRAF6 Stimulates the Tumor-Promoting Effects of TGFβ Type I Receptor Through Polyubiquitination and Activation of Presenilin 1

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UBE4B, a ubiquitin chain assembly factor, is required for MDM2-mediated p53 polyubiquitination and degradation

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TRAF6 ubiquitinates TGFβ type I receptor to promote its cleavage and nuclear translocation in cancer

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