A mass spectrometric-derived cell surface protein atlas
Language English Country United States Media electronic-ecollection
Document type Journal Article, Research Support, N.I.H., Extramural, Research Support, Non-U.S. Gov't
Grant support
U01 CA152813
NCI NIH HHS - United States
U01CA152813
NCI NIH HHS - United States
PubMed
25894527
PubMed Central
PMC4404347
DOI
10.1371/journal.pone.0121314
PII: PONE-D-14-46273
Knihovny.cz E-resources
- MeSH
- Cell Line MeSH
- Databases, Protein MeSH
- Mass Spectrometry methods MeSH
- Humans MeSH
- Membrane Proteins chemistry MeSH
- Mice MeSH
- Proteomics methods MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Mice MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, N.I.H., Extramural MeSH
- Names of Substances
- Membrane Proteins MeSH
Cell surface proteins are major targets of biomedical research due to their utility as cellular markers and their extracellular accessibility for pharmacological intervention. However, information about the cell surface protein repertoire (the surfaceome) of individual cells is only sparsely available. Here, we applied the Cell Surface Capture (CSC) technology to 41 human and 31 mouse cell types to generate a mass-spectrometry derived Cell Surface Protein Atlas (CSPA) providing cellular surfaceome snapshots at high resolution. The CSPA is presented in form of an easy-to-navigate interactive database, a downloadable data matrix and with tools for targeted surfaceome rediscovery (http://wlab.ethz.ch/cspa). The cellular surfaceome snapshots of different cell types, including cancer cells, resulted in a combined dataset of 1492 human and 1296 mouse cell surface glycoproteins, providing experimental evidence for their cell surface expression on different cell types, including 136 G-protein coupled receptors and 75 membrane receptor tyrosine-protein kinases. Integrated analysis of the CSPA reveals that the concerted biological function of individual cell types is mainly guided by quantitative rather than qualitative surfaceome differences. The CSPA will be useful for the evaluation of drug targets, for the improved classification of cell types and for a better understanding of the surfaceome and its concerted biological functions in complex signaling microenvironments.
Department of Biochemistry Medical College of Wisconsin Wisconsin Milwaukee United States of America
Institute for Biomaterials and Biomedical Engineering University of Toronto Toronto Canada
Institute of Molecular Systems Biology ETH Zurich Zurich Switzerland
Oncology Research Laboratory University Children Hospital Zurich Zurich Switzerland
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Freitas RA Jr (2005) What is nanomedicine? Nanomedicine: nanotechnology, biology, and medicine 1: 2–9. PubMed
Schwartz SM (1999) The definition of cell type. Circ Res 84: 1234–1235. PubMed
Elschenbroich S, Kim Y, Medin JA, Kislinger T (2010) Isolation of cell surface proteins for mass spectrometry-based proteomics. Expert review of proteomics 7: 141–154. 10.1586/epr.09.97 PubMed DOI
Savas JN, Stein BD, Wu CC, Yates JR 3rd (2011) Mass spectrometry accelerates membrane protein analysis. Trends in biochemical sciences. PubMed PMC
da Cunha JP, Galante PA, de Souza JE, de Souza RF, Carvalho PM, et al. (2009) Bioinformatics construction of the human cell surfaceome. Proc Natl Acad Sci U S A 106: 16752–16757. 10.1073/pnas.0907939106 PubMed DOI PMC
Schwanhausser B, Busse D, Li N, Dittmar G, Schuchhardt J, et al. (2011) Global quantification of mammalian gene expression control. Nature 473: 337–342. 10.1038/nature10098 PubMed DOI
Siuti N, Kelleher NL (2007) Decoding protein modifications using top-down mass spectrometry. Nature methods 4: 817–821. PubMed PMC
Sun Y, Gallagher-Jones M, Barker C, Wright GJ (2012) A benchmarked protein microarray-based platform for the identification of novel low-affinity extracellular protein interactions. Analytical biochemistry 424: 45–53. 10.1016/j.ab.2012.01.034 PubMed DOI PMC
Zola H (2006) Medical applications of leukocyte surface molecules—the CD molecules. Mol Med 12: 312–316. PubMed PMC
Solter D, Knowles BB (1978) Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). Proceedings of the National Academy of Sciences of the United States of America 75: 5565–5569. PubMed PMC
Gundry RL, Boheler KR, Van Eyk JE, Wollscheid B (2008) A novel role for proteomics in the discovery of cell-surface markers on stem cells: Scratching the surface. Proteomics Clinical applications 2: 892–903. PubMed PMC
Ahn SM, Goode RJ, Simpson RJ (2008) Stem cell markers: insights from membrane proteomics? Proteomics 8: 4946–4957. 10.1002/pmic.200800312 PubMed DOI
Scott SD (1998) Rituximab: a new therapeutic monoclonal antibody for non-Hodgkin's lymphoma. Cancer practice 6: 195–197. PubMed
Baselga J, Tripathy D, Mendelsohn J, Baughman S, Benz CC, et al. (1999) Phase II study of weekly intravenous trastuzumab (Herceptin) in patients with HER2/neu-overexpressing metastatic breast cancer. Seminars in oncology 26: 78–83. PubMed
Belov L, de la Vega O, dos Remedios CG, Mulligan SP, Christopherson RI (2001) Immunophenotyping of leukemias using a cluster of differentiation antibody microarray. Cancer research 61: 4483–4489. PubMed
Bandura DR, Baranov VI, Ornatsky OI, Antonov A, Kinach R, et al. (2009) Mass cytometry: technique for real time single cell multitarget immunoassay based on inductively coupled plasma time-of-flight mass spectrometry. Analytical Chemistry 81: 6813–6822. 10.1021/ac901049w PubMed DOI
Uhlen M, Oksvold P, Fagerberg L, Lundberg E, Jonasson K, et al. (2010) Towards a knowledge-based Human Protein Atlas. Nat Biotechnol 28: 1248–1250. 10.1038/nbt1210-1248 PubMed DOI
Andersson O, Kozlowski M, Garachtchenko T, Nikoloff C, Lew N, et al. (2005) Determination of relative protein abundance by internally normalized ratio algorithm with antibody arrays. Journal of proteome research 4: 758–767. PubMed
Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, et al. (2004) UniProt: the Universal Protein knowledgebase. Nucleic acids research 32: D115–119. PubMed PMC
Kandasamy K, Keerthikumar S, Goel R, Mathivanan S, Patankar N, et al. (2009) Human Proteinpedia: a unified discovery resource for proteomics research. Nucleic Acids Res 37: D773–781. 10.1093/nar/gkn701 PubMed DOI PMC
Wilhelm M, Schlegl J, Hahne H, Moghaddas Gholami A, Lieberenz M, et al. (2014) Mass-spectrometry-based draft of the human proteome. Nature 509: 582–587. 10.1038/nature13319 PubMed DOI
Kim MS, Pinto SM, Getnet D, Nirujogi RS, Manda SS, et al. (2014) A draft map of the human proteome. Nature 509: 575–581. 10.1038/nature13302 PubMed DOI PMC
Beck M, Schmidt A, Malmstroem J, Claassen M, Ori A, et al. (2011) The quantitative proteome of a human cell line. Molecular systems biology 7: 549 10.1038/msb.2011.82 PubMed DOI PMC
Dormeyer W, van Hoof D, Braam SR, Heck AJ, Mummery CL, et al. (2008) Plasma membrane proteomics of human embryonic stem cells and human embryonal carcinoma cells. Journal of proteome research 7: 2936–2951. 10.1021/pr800056j PubMed DOI
Lewandrowski U, Wortelkamp S, Lohrig K, Zahedi RP, Wolters DA, et al. (2009) Platelet membrane proteomics: a novel repository for functional research. Blood 114: e10–19. 10.1182/blood-2009-02-203828 PubMed DOI
Deeb SJ, Cox J, Schmidt-Supprian M, Mann M (2014) N-linked glycosylation enrichment for in-depth cell surface proteomics of diffuse large B-cell lymphoma subtypes. Mol Cell Proteomics 13: 240–251. 10.1074/mcp.M113.033977 PubMed DOI PMC
Conn EM, Madsen MA, Cravatt BF, Ruf W, Deryugina EI, et al. (2008) Cell surface proteomics identifies molecules functionally linked to tumor cell intravasation. J Biol Chem 283: 26518–26527. 10.1074/jbc.M803337200 PubMed DOI PMC
Peirce MJ, Wait R, Begum S, Saklatvala J, Cope AP (2004) Expression profiling of lymphocyte plasma membrane proteins. Molecular & cellular proteomics: MCP 3: 56–65. PubMed
Autelitano F, Loyaux D, Roudieres S, Deon C, Guette F, et al. (2014) Identification of novel tumor-associated cell surface sialoglycoproteins in human glioblastoma tumors using quantitative proteomics. PLoS One 9: e110316 10.1371/journal.pone.0110316 PubMed DOI PMC
Rugg-Gunn PJ, Cox BJ, Lanner F, Sharma P, Ignatchenko V, et al. (2012) Cell-surface proteomics identifies lineage-specific markers of embryo-derived stem cells. Dev Cell 22: 887–901. 10.1016/j.devcel.2012.01.005 PubMed DOI PMC
Roesli C, Neri D, Rybak JN (2006) In vivo protein biotinylation and sample preparation for the proteomic identification of organ- and disease-specific antigens accessible from the vasculature. Nat Protoc 1: 192–199. PubMed
Prior MJ, Larance M, Lawrence RT, Soul J, Humphrey S, et al. (2011) Quantitative proteomic analysis of the adipocyte plasma membrane. J Proteome Res 10: 4970–4982. 10.1021/pr200446r PubMed DOI
Kim Y, Elschenbroich S, Sharma P, Sepiashvili L, Gramolini AO, et al. (2011) Use of colloidal silica-beads for the isolation of cell-surface proteins for mass spectrometry-based proteomics. Methods Mol Biol 748: 227–241. 10.1007/978-1-61779-139-0_16 PubMed DOI PMC
Josic D, Clifton JG (2007) Mammalian plasma membrane proteomics. Proteomics 7: 3010–3029. PubMed
Bock T, Bausch-Fluck D, Hofmann A, Wollscheid B (2011) CD proteome and beyond—technologies for targeting the immune cell surfaceome. Frontiers in Bioscience accepted. PubMed
Leth-Larsen R, Lund RR, Ditzel HJ (2010) Plasma membrane proteomics and its application in clinical cancer biomarker discovery. Molecular & cellular proteomics: MCP 9: 1369–1382. 10.1074/mcp.R900006-MCP200 PubMed DOI PMC
Wollscheid B, Bausch-Fluck D, Henderson C, O'Brien R, Bibel M, et al. (2009) Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins. Nat Biotechnol 27: 378–386. 10.1038/nbt.1532 PubMed DOI PMC
Hofmann A, Gerrits B, Schmidt A, Bock T, Bausch-Fluck D, et al. (2010) Proteomic cell surface phenotyping of differentiating acute myeloid leukemia cells. Blood 116: e26–34. 10.1182/blood-2010-02-271270 PubMed DOI
Gundry RL, Raginski K, Tarasova Y, Tchernyshyov I, Bausch-Fluck D, et al. (2009) The mouse C2C12 myoblast cell surface N-linked glycoproteome: identification, glycosite occupancy, and membrane orientation. Mol Cell Proteomics 8: 2555–2569. 10.1074/mcp.M900195-MCP200 PubMed DOI PMC
Ziegler A, Cerciello F, Bigosch C, Bausch-Fluck D, Felley-Bosco E, et al. (2011) Proteomic Surfaceome Analysis of Mesothelioma. Lung Cancer accepted. PubMed
Bock T, Moest H, Omasits U, Dolski S, Lundberg E, et al. (2012) Proteomic analysis reveals drug accessible cell surface N-glycoproteins of primary and established glioblastoma cell lines. Journal of proteome research 11: 4885–4893. 10.1021/pr300360a PubMed DOI
Mirkowska P, Hofmann A, Sedek L, Slamova L, Mejstrikova E, et al. (2013) Leukemia surfaceome analysis reveals new disease-associated features. Blood 121: e149–159. 10.1182/blood-2012-11-468702 PubMed DOI
Boysen G, Bausch-Fluck D, Thoma CR, Nowicka AM, Stiehl DP, et al. (2012) Identification and functional characterization of pVHL-dependent cell surface proteins in renal cell carcinoma. Neoplasia 14: 535–546. PubMed PMC
Eng JK, McCormack AL, Yates JR (1994) An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. Journal of the American Society for Mass Spectrometry 5: 976–989. 10.1016/1044-0305(94)80016-2 PubMed DOI
Deutsch EW, Mendoza L, Shteynberg D, Farrah T, Lam H, et al. (2010) A guided tour of the Trans-Proteomic Pipeline. Proteomics 10: 1150–1159. 10.1002/pmic.200900375 PubMed DOI PMC
Lam H, Deutsch EW, Eddes JS, Eng JK, Stein SE, et al. (2008) Building consensus spectral libraries for peptide identification in proteomics. Nat Methods 5: 873–875. 10.1038/nmeth.1254 PubMed DOI PMC
Omasits U, C HA, Muller S, Wollscheid B (2013) Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics. PubMed
Colonna M, Samaridis J (1995) Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. Science 268: 405–408. PubMed
Schwab U, Stein H, Gerdes J, Lemke H, Kirchner H, et al. (1982) Production of a monoclonal antibody specific for Hodgkin and Sternberg-Reed cells of Hodgkin's disease and a subset of normal lymphoid cells. Nature 299: 65–67. PubMed
Chuang W, Lagenaur CF (1990) Central nervous system antigen P84 can serve as a substrate for neurite outgrowth. Developmental biology 137: 219–232. PubMed
Dubois NC, Craft AM, Sharma P, Elliott DA, Stanley EG, et al. (2011) SIRPA is a specific cell-surface marker for isolating cardiomyocytes derived from human pluripotent stem cells. Nature biotechnology 29: 1011–1018. 10.1038/nbt.2005 PubMed DOI PMC
Kall L, Krogh A, Sonnhammer EL (2004) A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338: 1027–1036. PubMed
Ikeda M, Arai M, Lao DM, Shimizu T (2002) Transmembrane topology prediction methods: a re-assessment and improvement by a consensus method using a dataset of experimentally-characterized transmembrane topologies. In silico biology 2: 19–33. PubMed
Schmidt A, Gehlenborg N, Bodenmiller B, Mueller LN, Campbell D, et al. (2008) An integrated, directed mass spectrometric approach for in-depth characterization of complex peptide mixtures. Molecular & cellular proteomics: MCP 7: 2138–2150. PubMed PMC
Stahl-Zeng J, Lange V, Ossola R, Eckhardt K, Krek W, et al. (2007) High sensitivity detection of plasma proteins by multiple reaction monitoring of N-glycosites. Mol Cell Proteomics 6: 1809–1817. PubMed
Picotti P, Rinner O, Stallmach R, Dautel F, Farrah T, et al. (2010) High-throughput generation of selected reaction-monitoring assays for proteins and proteomes. Nature methods 7: 43–46. 10.1038/nmeth.1408 PubMed DOI
Gnad F, Ren S, Cox J, Olsen JV, Macek B, et al. (2007) PHOSIDA (phosphorylation site database): management, structural and evolutionary investigation, and prediction of phosphosites. Genome biology 8: R250 PubMed PMC
Bodenmiller B, Campbell D, Gerrits B, Lam H, Jovanovic M, et al. (2008) PhosphoPep—a database of protein phosphorylation sites in model organisms. Nature biotechnology 26: 1339–1340. 10.1038/nbt1208-1339 PubMed DOI PMC
Hornbeck PV, Chabra I, Kornhauser JM, Skrzypek E, Zhang B (2004) PhosphoSite: A bioinformatics resource dedicated to physiological protein phosphorylation. Proteomics 4: 1551–1561. PubMed
Boheler KR, Bhattacharya S, Kropp EM, Chuppa S, Riordon DR, et al. (2014) A Human Pluripotent Stem Cell Surface N-Glycoproteome Resource Reveals Markers, Extracellular Epitopes, and Drug Targets. Stem cell reports. PubMed PMC
Moest H, Frei AP, Bhattacharya I, Geiger M, Wollscheid B, et al. (2013) Malfunctioning of adipocytes in obesity is linked to quantitative surfaceome changes. Biochimica et biophysica acta 1831: 1208–1216. PubMed
Vom Berg J, Vrohlings M, Haller S, Haimovici A, Kulig P, et al. (2013) Intratumoral IL-12 combined with CTLA-4 blockade elicits T cell-mediated glioma rejection. J Exp Med 210: 2803–2811. 10.1084/jem.20130678 PubMed DOI PMC
Obermair FJ, Fiorelli R, Schroeter A, Beyeler S, Blatti C, et al. (2010) A novel classification of quiescent and transit amplifying adult neural stem cells by surface and metabolic markers permits a defined simultaneous isolation. Stem Cell Res 5: 131–143. 10.1016/j.scr.2010.05.001 PubMed DOI
Hartmann J, Tran TV, Kaudeer J, Oberle K, Herrmann J, et al. (2012) The stalk domain and the glycosylation status of the activating natural killer cell receptor NKp30 are important for ligand binding. J Biol Chem 287: 31527–31539. 10.1074/jbc.M111.304238 PubMed DOI PMC
Vizcaino JA, Cote RG, Csordas A, Dianes JA, Fabregat A, et al. (2013) The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic acids research 41: D1063–1069. 10.1093/nar/gks1262 PubMed DOI PMC
Zielinska DF, Gnad F, Wisniewski JR, Mann M (2010) Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 141: 897–907. 10.1016/j.cell.2010.04.012 PubMed DOI
Keller A, Eng J, Zhang N, Li XJ, Aebersold R (2005) A uniform proteomics MS/MS analysis platform utilizing open XML file formats. Molecular systems biology 1: 2005 0017. PubMed PMC
Clough T, Key M, Ott I, Ragg S, Schadow G, et al. (2009) Protein quantification in label-free LC-MS experiments. J Proteome Res 8: 5275–5284. 10.1021/pr900610q PubMed DOI
Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, et al. (2003) PANTHER: a library of protein families and subfamilies indexed by function. Genome research 13: 2129–2141. PubMed PMC
MacLean B, Tomazela DM, Shulman N, Chambers M, Finney GL, et al. (2010) Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26: 966–968. 10.1093/bioinformatics/btq054 PubMed DOI PMC
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