N-glycoprotein Surfaceomes of Four Developmentally Distinct Mouse Cell Types

Overview

Journal Proteomics Clin Appl

Specialty Biochemistry

Date 2014 Jun 13

PMID 24920426

Citations 9

Authors

Erin M Kropp

Subarna Bhattacharya

Matthew Waas

Sandra L Chuppa

Anna-Katerina Hadjantonakis

Kenneth R Boheler

Rebekah L Gundry

Affiliations

Soon will be listed here.

Abstract

Purpose: Detailed knowledge of cell surface proteins present during early embryonic development remains limited for most cell lineages. Due to the relevance of cell surface proteins in their functional roles controlling cell signaling and their utility as accessible, nongenetic markers for cell identification and sorting, the goal of this study was to provide new information regarding the cell surface proteins present during early mouse embryonic development.

Experimental Design: Using the cell surface capture technology, the cell surface N-glycoproteomes of three cell lines and one in vitro differentiated cell type representing distinct cell fates and stages in mouse embryogenesis were assessed.

Results: Altogether, more than 600 cell surface N-glycoproteins were identified represented by >5500 N-glycopeptides.

Conclusions And Clinical Relevance: The development of new, informative cell surface markers for the reliable identification and isolation of functionally defined subsets of cells from early developmental stages will advance the use of stem cell technologies for mechanistic developmental studies, including disease modeling and drug discovery.

Citing Articles

Cell surface markers for immunophenotyping human pluripotent stem cell-derived cardiomyocytes.

Boheler K, Poon E Pflugers Arch. 2021; 473(7):1023-1039.

PMID: 33928456 DOI: 10.1007/s00424-021-02549-8.

The quest of cell surface markers for stem cell therapy.

Meyfour A, Pahlavan S, Mirzaei M, Krijgsveld J, Baharvand H, Hosseini Salekdeh G Cell Mol Life Sci. 2020; 78(2):469-495.

PMID: 32710154 PMC: 11073434. DOI: 10.1007/s00018-020-03602-y.

The in silico human surfaceome.

Bausch-Fluck D, Goldmann U, Muller S, van Oostrum M, Muller M, Schubert O Proc Natl Acad Sci U S A. 2018; 115(46):E10988-E10997.

PMID: 30373828 PMC: 6243280. DOI: 10.1073/pnas.1808790115.

Biophysical subsets of embryonic stem cells display distinct phenotypic and morphological signatures.

Bongiorno T, Gura J, Talwar P, Chambers D, Young K, Arafat D PLoS One. 2018; 13(3):e0192631.

PMID: 29518080 PMC: 5843178. DOI: 10.1371/journal.pone.0192631.

Mass Spectrometry-Based Identification of Extracellular Domains of Cell Surface N-Glycoproteins: Defining the Accessible Surfaceome for Immunophenotyping Stem Cells and Their Derivatives.

Fujinaka C, Waas M, Gundry R Methods Mol Biol. 2017; 1722:57-78.

PMID: 29264798 PMC: 5791894. DOI: 10.1007/978-1-4939-7553-2_4.

References

Artus J, Douvaras P, Piliszek A, Isern J, Baron M, Hadjantonakis A . BMP4 signaling directs primitive endoderm-derived XEN cells to an extraembryonic visceral endoderm identity. Dev Biol. 2011; 361(2):245-62. PMC: 3246571. DOI: 10.1016/j.ydbio.2011.10.015. View

Boheler K, Bhattacharya S, Kropp E, Chuppa S, Riordon D, Bausch-Fluck D . A human pluripotent stem cell surface N-glycoproteome resource reveals markers, extracellular epitopes, and drug targets. Stem Cell Reports. 2014; 3(1):185-203. PMC: 4110789. DOI: 10.1016/j.stemcr.2014.05.002. View

Parker B, Palmisano G, Edwards A, White M, Engholm-Keller K, Lee A . Quantitative N-linked glycoproteomics of myocardial ischemia and reperfusion injury reveals early remodeling in the extracellular environment. Mol Cell Proteomics. 2011; 10(8):M110.006833. PMC: 3149091. DOI: 10.1074/mcp.M110.006833. View

Ong S, Blagoev B, Kratchmarova I, Kristensen D, Steen H, Pandey A . Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics. 2002; 1(5):376-86. DOI: 10.1074/mcp.m200025-mcp200. View

Palmisano G, Parker B, Engholm-Keller K, Lendal S, Kulej K, Schulz M . A novel method for the simultaneous enrichment, identification, and quantification of phosphopeptides and sialylated glycopeptides applied to a temporal profile of mouse brain development. Mol Cell Proteomics. 2012; 11(11):1191-202. PMC: 3494194. DOI: 10.1074/mcp.M112.017509. View

Apweiler R, Hermjakob H, Sharon N . On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim Biophys Acta. 1999; 1473(1):4-8. DOI: 10.1016/s0304-4165(99)00165-8. View

Gundry R, Raginski K, Tarasova Y, Tchernyshyov I, Bausch-Fluck D, Elliott S . The mouse C2C12 myoblast cell surface N-linked glycoproteome: identification, glycosite occupancy, and membrane orientation. Mol Cell Proteomics. 2009; 8(11):2555-69. PMC: 2773721. DOI: 10.1074/mcp.M900195-MCP200. View

Brown K, Legros S, Artus J, Doss M, Khanin R, Hadjantonakis A . A comparative analysis of extra-embryonic endoderm cell lines. PLoS One. 2010; 5(8):e12016. PMC: 2919048. DOI: 10.1371/journal.pone.0012016. View

Franco D, Lamers W, Moorman A . Patterns of expression in the developing myocardium: towards a morphologically integrated transcriptional model. Cardiovasc Res. 1998; 38(1):25-53. DOI: 10.1016/s0008-6363(97)00321-0. View

10.

Boheler K, Joodi R, Qiao H, Juhasz O, Urick A, Chuppa S . Embryonic stem cell-derived cardiomyocyte heterogeneity and the isolation of immature and committed cells for cardiac remodeling and regeneration. Stem Cells Int. 2011; 2011:214203. PMC: 3168772. DOI: 10.4061/2011/214203. View

11.

Rugg-Gunn P, Cox B, Lanner F, Sharma P, Ignatchenko V, McDonald A . Cell-surface proteomics identifies lineage-specific markers of embryo-derived stem cells. Dev Cell. 2012; 22(4):887-901. PMC: 3405530. DOI: 10.1016/j.devcel.2012.01.005. View

12.

Nagy A, Rossant J, Nagy R, Abramow-Newerly W, Roder J . Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc Natl Acad Sci U S A. 1993; 90(18):8424-8. PMC: 47369. DOI: 10.1073/pnas.90.18.8424. View

13.

Wollscheid B, Bausch-Fluck D, Henderson C, OBrien R, Bibel M, Schiess R . Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins. Nat Biotechnol. 2009; 27(4):378-86. PMC: 2829300. DOI: 10.1038/nbt.1532. View

14.

Gundry R, Riordon D, Tarasova Y, Chuppa S, Bhattacharya S, Juhasz O . A cell surfaceome map for immunophenotyping and sorting pluripotent stem cells. Mol Cell Proteomics. 2012; 11(8):303-16. PMC: 3412963. DOI: 10.1074/mcp.M112.018135. View

15.

Yen T, Haste N, Timpe L, Litsakos-Cheung C, Yen R, Macher B . Using a cell line breast cancer progression system to identify biomarker candidates. J Proteomics. 2013; 96:173-83. PMC: 3920745. DOI: 10.1016/j.jprot.2013.11.006. View

16.

Elliott D, Braam S, Koutsis K, Ng E, Jenny R, Lagerqvist E . NKX2-5(eGFP/w) hESCs for isolation of human cardiac progenitors and cardiomyocytes. Nat Methods. 2011; 8(12):1037-40. DOI: 10.1038/nmeth.1740. View

17.

Deeb S, Cox J, Schmidt-Supprian M, Mann M . N-linked glycosylation enrichment for in-depth cell surface proteomics of diffuse large B-cell lymphoma subtypes. Mol Cell Proteomics. 2013; 13(1):240-51. PMC: 3879617. DOI: 10.1074/mcp.M113.033977. View

18.

Shizuru J, Negrin R, Weissman I . Hematopoietic stem and progenitor cells: clinical and preclinical regeneration of the hematolymphoid system. Annu Rev Med. 2005; 56:509-38. DOI: 10.1146/annurev.med.54.101601.152334. View

19.

Hofmann A, Gerrits B, Schmidt A, Bock T, Bausch-Fluck D, Aebersold R . Proteomic cell surface phenotyping of differentiating acute myeloid leukemia cells. Blood. 2010; 116(13):e26-34. DOI: 10.1182/blood-2010-02-271270. View

20.

Kunath T, Arnaud D, Uy G, Okamoto I, Chureau C, Yamanaka Y . Imprinted X-inactivation in extra-embryonic endoderm cell lines from mouse blastocysts. Development. 2005; 132(7):1649-61. DOI: 10.1242/dev.01715. View