Cited by 4Cancer Immunotherapy and BiomarkersImmune Cell Function and Interactionvaccines and immunoinformatics approaches

The DOI matches its Crossref record; 3 of the 3 references it cites were found in a registry or an index.

A novel bioinformatics pipeline for the identification of immune inhibitory receptors as potential therapeutic targets

Open access
Singh, Akashdip, Miranda Bedate, Alberto, von Richthofen, Helen J, Vijver, Saskia V, van der Vlist, Michiel, Kuhn, Raphael, Yermanos, Alexander, Kuball, Jürgen J, Kesmir, Can, Pascoal Ramos, M Ines, Meyaard, Linde·2024·eLife

Published version of a preprint

Abstract

Despite major successes with inhibitory receptor blockade in cancer, the identification of novel inhibitory receptors as putative drug targets is needed due to lack of durable responses, therapy resistance, and side effects. Most inhibitory receptors signal via immunoreceptor tyrosine-based inhibitory motifs (ITIMs) and previous studies estimated that our genome contains over 1600 ITIM-bearing transmembrane proteins. However, testing and development of these candidates requires increased understanding of their expression patterns and likelihood to function as inhibitory receptor. Therefore, we designed a novel bioinformatics pipeline integrating machine learning-guided structural predictions and sequence-based likelihood models to identify putative inhibitory receptors. Using transcriptomics data of immune cells, we determined the expression of these novel inhibitory receptors, and classified them into previously proposed functional categories. Known and putative inhibitory receptors were expressed across different immune cell subsets with cell type-specific expression patterns. Furthermore, putative immune inhibitory receptors were differentially expressed in subsets of tumour infiltrating T cells. In conclusion, we present an inhibitory receptor pipeline that identifies 51 known and 390 novel human inhibitory receptors. This pipeline will support future drug target selection across diseases where therapeutic targeting of immune inhibitory receptors is warranted.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.7554/elife.92870

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 50

  1. AkashdipSingh. 2023. IIR_pipeline. Software Heritage. swh:1:rev:989cfba460c3672f133fcbb1d800bd45bd02dae3. https://archive.softwareheritage.org/swh:1:dir:e73c060824474aaef3203dcc379d51fcc4fa11e2;origin=https://github.com/AkashdipSingh/IIR_pipeline;visit=swh:1:snp:e53fbf602826766bc73b479a6befe8439ef9e260;anchor=swh:1:rev:989cfba460c3672f133fcbb1d800bd45bd02dae3.
  2. Andrews, 2019, Inhibitory receptors and ligands beyond PD-1, PD-L1 and CTLA-4: breakthroughs or backups, Nature Immunology, 20, 1425, 10.1038/s41590-019-0512-0 · DOI
  3. Barrow, 2006, You say ITAM and I say ITIM, let’s call the whole thing off: the ambiguity of immunoreceptor signalling, European Journal of Immunology, 36, 1646, 10.1002/eji.200636195 · DOI
  4. Békés, 2022, PROTAC targeted protein degraders: the past is prologue, Nature Reviews. Drug Discovery, 21, 181, 10.1038/s41573-021-00371-6 · DOI · Paper page
  5. Calderon, 2019, Landscape of stimulation-responsive chromatin across diverse human immune cells, Nature Genetics, 51, 1494, 10.1038/s41588-019-0505-9 · DOI
  6. Chemnitz, 2004, SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation, Journal of Immunology, 173, 945, 10.4049/jimmunol.173.2.945 · DOI · Paper page
  7. Chocarro, 2022, Cutting-edge: Preclinical and clinical development of the first approved lag-3 inhibitor, Cells, 11, 10.3390/cells11152351 · DOI
  8. Cunningham, 2022, Ensembl 2022, Nucleic Acids Research, 50, D988, 10.1093/nar/gkab1049 · DOI · Paper page
  9. Daëron, 2008, Immunoreceptor tyrosine-based inhibition motifs: a quest in the past and future, Immunological Reviews, 224, 11, 10.1111/j.1600-065X.2008.00666.x · DOI
  10. de Vet, 2001, G6b, a novel immunoglobulin superfamily member encoded in the human major histocompatibility complex, interacts with SHP-1 and SHP-2, Journal of Biological Chemistry, 276, 42070, 10.1074/jbc.M103214200 · DOI
  11. Dietrich, 2001, Ig-like transcript 2 (ILT2)/leukocyte Ig-like receptor 1 (LIR1) inhibits TCR signaling and actin cytoskeleton reorganization, Journal of Immunology, 166, 2514, 10.4049/jimmunol.166.4.2514 · DOI
  12. Durinck, 2009, Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt, Nature Protocols, 4, 1184, 10.1038/nprot.2009.97 · DOI
  13. Ferjoux, 2003, Critical role of Src and SHP-2 in sst2 somatostatin receptor-mediated activation of SHP-1 and inhibition of cell proliferation, Molecular Biology of the Cell, 14, 3911, 10.1091/mbc.e03-02-0069 · DOI
  14. Gagolewski, 2022, stringi: Fast and portable character string processing in R, Journal of Statistical Software, 103, 1, 10.18637/jss.v103.i02 · DOI
  15. Gaur, 2008, Altered splicing of CEACAM1 in breast cancer: identification of regulatory sequences that control splicing of CEACAM1 into long or short cytoplasmic domain isoforms, Molecular Cancer, 7, 10.1186/1476-4598-7-46 · DOI
  16. Geerdink, 2018, LAIR-1 limits neutrophil extracellular trap formation in viral bronchiolitis, The Journal of Allergy and Clinical Immunology, 141, 811, 10.1016/j.jaci.2017.08.031 · DOI
  17. Grant, 2021, The Bio3D packages for structural bioinformatics, Protein Science, 30, 20, 10.1002/pro.3923 · DOI
  18. Grebinoski, 2020, Inhibitory receptor agonists: the future of autoimmune disease therapeutics?, Current Opinion in Immunology, 67, 1, 10.1016/j.coi.2020.06.001 · DOI · Paper page
  19. Helfrich, 2019, Size matters: The functional role of the CEACAM1 isoform signature and its impact for NK cell-mediated killing in melanoma, Cancers, 11, 10.3390/cancers11030356 · DOI
  20. Jakob, 2014, Conditionally and transiently disordered proteins: awakening cryptic disorder to regulate protein function, Chemical Reviews, 114, 6779, 10.1021/cr400459c · DOI
  21. Karpisheh, 2022, The role of Th17 cells in the pathogenesis and treatment of breast cancer, Cancer Cell International, 22, 10.1186/s12935-022-02528-8 · DOI
  22. Kiefhaber, 2012, Dynamics and mechanisms of coupled protein folding and binding reactions, Current Opinion in Structural Biology, 22, 21, 10.1016/j.sbi.2011.09.010 · DOI
  23. Long, 1999, Regulation of immune responses through inhibitory receptors, Annual Review of Immunology, 17, 875, 10.1146/annurev.immunol.17.1.875 · DOI
  24. Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biology, 15, 10.1186/s13059-014-0550-8 · DOI · Paper page
  25. Mirdita, 2022, ColabFold: making protein folding accessible to all, Nature Methods, 19, 679, 10.1038/s41592-022-01488-1 · DOI · Paper page
  26. Möller, 2001, Evaluation of methods for the prediction of membrane spanning regions, Bioinformatics, 17, 646, 10.1093/bioinformatics/17.7.646 · DOI
  27. Ostrakhovitch, 2006, The role of SLAM family receptors in immune cell signaling, Biochemistry and Cell Biology = Biochimie et Biologie Cellulaire, 84, 832, 10.1139/o06-191 · DOI
  28. Reynolds, 2008, Transmembrane topology and signal peptide prediction using dynamic bayesian networks, PLOS Computational Biology, 4, 10.1371/journal.pcbi.1000213 · DOI
  29. Rives, 2021, Biological structure and function emerge from scaling unsupervised learning to 250 million protein sequences, PNAS, 118, 10.1073/pnas.2016239118 · DOI · Paper page
  30. Rumpret, 2020, Functional categories of immune inhibitory receptors, Nature Reviews. Immunology, 20, 771, 10.1038/s41577-020-0352-z · DOI
  31. Schnell, 2020, The yin and yang of co-inhibitory receptors: toward anti-tumor immunity without autoimmunity, Cell Research, 30, 285, 10.1038/s41422-020-0277-x · DOI
  32. Seal, 2023, Genenames.org: the HGNC resources in 2023, Nucleic Acids Research, 51, D1003, 10.1093/nar/gkac888 · DOI
  33. Sharma, 2017, Primary, adaptive, and acquired resistance to cancer immunotherapy, Cell, 168, 707, 10.1016/j.cell.2017.01.017 · DOI · Paper page
  34. Staub, 2004, Systematic identification of immunoreceptor tyrosine-based inhibitory motifs in the human proteome, Cellular Signalling, 16, 435, 10.1016/j.cellsig.2003.08.013 · DOI
  35. Tay, 2021, Revisiting the role of CD4+ T cells in cancer immunotherapy-new insights into old paradigms, Cancer Gene Therapy, 28, 5, 10.1038/s41417-020-0183-x · DOI
  36. Timmerman, 2021, Identification of a novel conserved signaling motif in CD200 receptor required for its inhibitory function, PLOS ONE, 16, 10.1371/journal.pone.0244770 · DOI
  37. Tompa, 2014, A million peptide motifs for the molecular biologist, Molecular Cell, 55, 161, 10.1016/j.molcel.2014.05.032 · DOI
  38. Tsirigos, 2015, The TOPCONS web server for consensus prediction of membrane protein topology and signal peptides, Nucleic Acids Research, 43, W401, 10.1093/nar/gkv485 · DOI
  39. Tsirigos, 2018, Topology of membrane proteins-predictions, limitations and variations, Current Opinion in Structural Biology, 50, 9, 10.1016/j.sbi.2017.10.003 · DOI
  40. Varadi, 2022, AlphaFold Protein Structure Database: massively expanding the structural coverage of protein-sequence space with high-accuracy models, Nucleic Acids Research, 50, D439, 10.1093/nar/gkab1061 · DOI · Paper page
  41. Voisin, 2008, A hallmark of immunoreceptor, the tyrosine-based inhibitory motif ITIM, is present in the G protein-coupled receptor OX1R for orexins and drives apoptosis: A novel mechanism, FASEB Journal, 22, 1993, 10.1096/fj.07-098723 · DOI
  42. Voisinne, 2018, CD5, an Undercover Regulator of TCR Signaling, Frontiers in Immunology, 9, 10.3389/fimmu.2018.02900 · DOI
  43. von Richthofen, 2023, Sensing context: Inhibitory receptors on non-hematopoietic cells, European Journal of Immunology, 53, 10.1002/eji.202250306 · DOI
  44. West, 2016, A TSLP-complement axis mediates neutrophil killing of methicillin-resistant Staphylococcus aureus, Science Immunology, 1, 10.1126/sciimmunol.aaf8471 · DOI
  45. Wolchok, 2013, Nivolumab plus ipilimumab in advanced melanoma, The New England Journal of Medicine, 369, 122, 10.1056/NEJMoa1302369 · DOI · Paper page
  46. Zhai, 2021, Immune checkpoints, a novel class of therapeutic targets for autoimmune diseases, Frontiers in Immunology, 12, 10.3389/fimmu.2021.645699 · DOI
  47. Zheng, 2021, Pan-cancer single-cell landscape of tumor-infiltrating T cells, Science, 374, 10.1126/science.abe6474 · DOI · Paper page
  48. Zheng L, Qin S, Si W, Wang A, Xing B, Gao R, Ren X, Wang L, Wu X, Zhang J, Wu N, Zhang N, Zheng H, Ouyang H, Chen K, Bu Z, Hu X, Ji J, Zhang Z. 2021. Pan-Cancer Single Cell Landscape of Tumor-Infiltrating T Cells. NCBI Gene Expression Omnibus. https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE156728. GSE156728.
  49. West EE, Spolski R, Kazemian M, Zx Yu, Kemper C, Leonard WJ. 2016. TSLP acts on neutrophils to drive complement-mediated killing of methicillin-resistant Staphylococcus aureus. NCBI Gene Expression Omnibus. https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE73313. GSE73313.
  50. Calderon D, Nguyen ML, Mezger A. 2019. RNA-seq data. NCBI Gene Expression Omnibus. https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE118165. GSE118165.

Metadata

Authors
Singh, A., Miranda Bedate, A., von Richthofen, H. J., Vijver, S. V., van der Vlist, M., Kuhn, R., Yermanos, A., Kuball, J. J., Kesmir, C., Pascoal Ramos, M. I., & Meyaard, L.
Affiliations
  • Utrecht University (NL)
  • Center for Translational Immunology, University Medical Centre Utrecht, Utrecht University
  • ETH Zurich (CH)
  • Theoretical Biology and Bioinformatics, Department of Biology, Utrecht University
Corresponding author
Meyaard, Linde
Venue
eLife
Published
2024-10-08
Volume
13
ISSN
2050-084X (ISSN-L)
OpenAlex
W4392748029
Cited by
4
References
3
Citations by year
2025: 4
Type
posted content
Language
en
Open access
Locations
  • eLife (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Oncode Institute
  • KWF Kankerbestrijding (2021-14339)
Topics
  • Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
  • Life Sciences › Immunology and Microbiology › Immunology › Immune Cell Function and Interaction
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › vaccines and immunoinformatics approaches
Keywords
immune inhibitory receptors, ITIM, drug target identification, machine learning prediction, structure prediction, transcriptomics, tumor-infiltrating T cells, cancer immunotherapy, treatment resistance
MeSH terms
Machine Learning, Humans, Neoplasms, Receptors, Immunologic, Computational Biology

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review