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PMID: 17186946 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

A comprehensive proteomics and genomics analysis reveals novel transmembrane proteins in human platelets and mouse megakaryocytes including G6b-B, a novel immunoreceptor tyrosine-based inhibitory motif protein.

Molecular & cellular proteomics : MCP ·Vol. 6 ·No. 3 ·2007-03-00 ·Pages 548-64

Senis YA, Tomlinson MG, García A, Dumon S, Heath VL, Herbert J, Cobbold SP, Spalton JC, Ayman S, Antrobus R, Zitzmann N, Bicknell R, Frampton J, Authi KS, Martin A, Wakelam MJ, Watson SP

Abstract

The platelet surface is poorly characterized due to the low abundance of many membrane proteins and the lack of specialist tools for their investigation. In this study we identified novel human platelet and mouse megakaryocyte membrane proteins using specialist proteomics and genomics approaches. Three separate methods were used to enrich platelet surface proteins prior to identification by liquid chromatography and tandem mass spectrometry: lectin affinity chromatography, biotin/NeutrAvidin affinity chromatography, and free flow electrophoresis. Many known, abundant platelet surface transmembrane proteins and several novel proteins were identified using each receptor enrichment strategy. In total, two or more unique peptides were identified for 46, 68, and 22 surface membrane, intracellular membrane, and membrane proteins of unknown subcellular localization, respectively. The majority of these were single transmembrane proteins. To complement the proteomics studies, we analyzed the transcriptome of a highly purified preparation of mature primary mouse megakaryocytes using serial analysis of gene expression in view of the increasing importance of mutant mouse models in establishing protein function in platelets. This approach identified all of the major classes of platelet transmembrane receptors, including multitransmembrane proteins. Strikingly 17 of the 25 most megakaryocyte-specific genes (relative to 30 other serial analysis of gene expression libraries) were transmembrane proteins, illustrating the unique nature of the megakaryocyte/platelet surface. The list of novel plasma membrane proteins identified using proteomics includes the immunoglobulin superfamily member G6b, which undergoes extensive alternate splicing. Specific antibodies were used to demonstrate expression of the G6b-B isoform, which contains an immunoreceptor tyrosine-based inhibition motif. G6b-B undergoes tyrosine phosphorylation and association with the SH2 domain-containing phosphatase, SHP-1, in stimulated platelets suggesting that it may play a novel role in limiting platelet activation.

MeSH Terms
Animals Blood Platelets/chemistry Cell Membrane/chemistry Cells, Cultured Chromatography, Affinity Gene Expression Genomics Humans Megakaryocytes/chemistry Membrane Proteins/analysis,genetics,metabolism Mice Mice, Inbred C57BL Platelet Activation Proteomics RNA/metabolism Receptors, Immunologic/analysis,metabolism Tandem Mass Spectrometry
Chemicals
G6b-B receptor, mouse MPIG6B protein, human Membrane Proteins Receptors, Immunologic RNA
Authors & Affiliations
17 authors, click to expand affiliations / ORCID
Senis Yotis A
Centre for Cardiovascular Sciences, Institute of Biomedical Research, University of Birmingham, Wolfson Drive, Edgbaston, Birmingham B15 2TT, United Kingdom. [email protected]
Tomlinson Michael G
García Angel
Dumon Stephanie
Heath Victoria L
Herbert John
Cobbold Stephen P
Spalton Jennifer C
Ayman Sinem
Antrobus Robin
Zitzmann Nicole
Bicknell Roy
Frampton Jon
Authi Kalwant S
Martin Ashley
Wakelam Michael J O
Watson Stephen P
References (46)
46 references, click to expand
  1. Using the transcriptome to annotate the genome.
    Nat Biotechnol. 2002 May;20(5):508-12 PMID: 11981567
  2. Interactions between Eph kinases and ephrins provide a mechanism to support platelet aggregation once cell-to-cell contact has occurred.
    Proc Natl Acad Sci U S A. 2002 Jul 9;99(14):9219-24 PMID: 12084815
  3. Identification of the phosphotyrosine proteome from thrombin activated platelets.
    Proteomics. 2002 Jun;2(6):642-8 PMID: 12112843
  4. Gene expression profile of megakaryocytes from human cord blood CD34(+) cells ex vivo expanded by thrombopoietin.
    Stem Cells. 2002;20(5):402-16 PMID: 12351811
  5. Platelets in atherothrombosis.
    Nat Med. 2002 Nov;8(11):1227-34 PMID: 12411949
  6. Transcript profiling of human platelets using microarray and serial analysis of gene expression.
    Blood. 2003 Mar 15;101(6):2285-93 PMID: 12433680
  7. Expression of junctional proteins in human platelets.
    Platelets. 2003 Jun;14(4):247-51 PMID: 12850834
  8. Differential analysis of phosphorylated proteins in resting and thrombin-stimulated human platelets.
    Anal Bioanal Chem. 2003 Aug;376(7):973-93 PMID: 12904942
  9. GPVI levels in platelets: relationship to platelet function at high shear.
    Blood. 2003 Oct 15;102(8):2811-8 PMID: 12829582
  10. Regulatory T cells and dendritic cells in transplantation tolerance: molecular markers and mechanisms.
    Immunol Rev. 2003 Dec;196:109-24 PMID: 14617201
  11. Expression profiling of lymphocyte plasma membrane proteins.
    Mol Cell Proteomics. 2004 Jan;3(1):56-65 PMID: 14573526
  12. Extensive analysis of the human platelet proteome by two-dimensional gel electrophoresis and mass spectrometry.
    Proteomics. 2004 Mar;4(3):656-68 PMID: 14997489
  13. Characterization of the proteins released from activated platelets leads to localization of novel platelet proteins in human atherosclerotic lesions.
    Blood. 2004 Mar 15;103(6):2096-104 PMID: 14630798
  14. Differential proteome analysis of TRAP-activated platelets: involvement of DOK-2 and phosphorylation of RGS proteins.
    Blood. 2004 Mar 15;103(6):2088-95 PMID: 14645010
  15. GPIb-dependent platelet activation is dependent on Src kinases but not MAP kinase or cGMP-dependent kinase.
    Blood. 2004 Apr 1;103(7):2601-9 PMID: 14684423
  16. Cutting edge: TREM-like transcript-1, a platelet immunoreceptor tyrosine-based inhibition motif encoding costimulatory immunoreceptor that enhances, rather than inhibits, calcium signaling via SHP-2.
    J Immunol. 2004 May 15;172(10):5838-42 PMID: 15128762
  17. Platelet adhesion signalling and the regulation of thrombus formation.
    J Cell Sci. 2004 Jul 15;117(Pt 16):3415-25 PMID: 15252124
  18. A TREM family member, TLT-1, is found exclusively in the alpha-granules of megakaryocytes and platelets.
    Blood. 2004 Aug 15;104(4):1042-7 PMID: 15100151
  19. Platelet coagulation-protein interactions.
    Semin Thromb Hemost. 2004 Aug;30(4):461-71 PMID: 15354267
  20. Serial analysis of gene expression.
    Science. 1995 Oct 20;270(5235):484-7 PMID: 7570003
  21. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels.
    Anal Chem. 1996 Mar 1;68(5):850-8 PMID: 8779443
  22. Analysis of GPIIb/IIIa receptor number by quantification of 7E3 binding to human platelets.
    Blood. 1996 Aug 1;88(3):907-14 PMID: 8704248
  23. Thrombopoietin signal transduction in purified murine megakaryocytes.
    Blood. 1997 Jan 15;89(2):483-92 PMID: 9002950
  24. CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells.
    Nature. 1998 Feb 5;391(6667):591-4 PMID: 9468137
  25. A dual thrombin receptor system for platelet activation.
    Nature. 1998 Aug 13;394(6694):690-4 PMID: 9716134
  26. Role of the p110delta PI 3-kinase in integrin and ITAM receptor signalling in platelets.
    Platelets. 2005 May-Jun;16(3-4):191-202 PMID: 16011964
  27. Eph kinases and ephrins support thrombus growth and stability by regulating integrin outside-in signaling in platelets.
    Proc Natl Acad Sci U S A. 2005 Jul 12;102(28):9820-5 PMID: 15994237
  28. The human platelet proteome mapped by peptide-centric proteomics: a functional protein profile.
    Proteomics. 2005 Aug;5(12):3193-204 PMID: 16038019
  29. Comparative evaluation of mass spectrometry platforms used in large-scale proteomics investigations.
    Nat Methods. 2005 Sep;2(9):667-75 PMID: 16118637
  30. Platelets express functional Toll-like receptor-4.
    Blood. 2005 Oct 1;106(7):2417-23 PMID: 15961512
  31. C-type natriuretic peptide inhibits leukocyte recruitment and platelet-leukocyte interactions via suppression of P-selectin expression.
    Proc Natl Acad Sci U S A. 2005 Oct 4;102(40):14452-7 PMID: 16179391
  32. Platelet aggregation induces platelet aggregate stability via SLAM family receptor signaling.
    Blood. 2005 Nov 1;106(9):3028-34 PMID: 16037392
  33. The human platelet membrane proteome reveals several new potential membrane proteins.
    Mol Cell Proteomics. 2005 Nov;4(11):1754-61 PMID: 16081409
  34. PAR3 is a cofactor for PAR4 activation by thrombin.
    Nature. 2000 Apr 6;404(6778):609-13 PMID: 10766244
  35. Identification of platelet proteins separated by two-dimensional gel electrophoresis and analyzed by matrix assisted laser desorption/ionization-time of flight-mass spectrometry and detection of tyrosine-phosphorylated proteins.
    Electrophoresis. 2000 Jul;21(13):2622-36 PMID: 10949139
  36. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes.
    J Mol Biol. 2001 Jan 19;305(3):567-80 PMID: 11152613
  37. Inhibition of platelet function by administration of MRS2179, a P2Y1 receptor antagonist.
    Eur J Pharmacol. 2001 Feb 2;412(3):213-21 PMID: 11166284
  38. Platelet endothelial cell adhesion molecule-1 is a negative regulator of platelet-collagen interactions.
    Blood. 2001 Sep 1;98(5):1456-63 PMID: 11520795
  39. G6b, a novel immunoglobulin superfamily member encoded in the human major histocompatibility complex, interacts with SHP-1 and SHP-2.
    J Biol Chem. 2001 Nov 9;276(45):42070-6 PMID: 11544253
  40. Platelet endothelial cell adhesion molecule-1 signaling inhibits the activation of human platelets.
    Blood. 2002 Jan 1;99(1):137-44 PMID: 11756163
  41. A transmembrane tight junction protein selectively expressed on endothelial cells and platelets.
    J Biol Chem. 2002 May 3;277(18):16294-303 PMID: 11847224
  42. Platelet PECAM-1 inhibits thrombus formation in vivo.
    Blood. 2006 Jan 15;107(2):535-41 PMID: 16166583
  43. A novel Syk-dependent mechanism of platelet activation by the C-type lectin receptor CLEC-2.
    Blood. 2006 Jan 15;107(2):542-9 PMID: 16174766
  44. Platelet Toll-like receptor expression modulates lipopolysaccharide-induced thrombocytopenia and tumor necrosis factor-alpha production in vivo.
    Blood. 2006 Jan 15;107(2):637-41 PMID: 16179373
  45. Differentiation of murine committed megakaryocytic progenitors isolated by a novel strategy reveals the complexity of GATA and Ets factor involvement in megakaryocytopoiesis and an unexpected potential role for GATA-6.
    Exp Hematol. 2006 May;34(5):654-63 PMID: 16647571
  46. A global proteomics approach identifies novel phosphorylated signaling proteins in GPVI-activated platelets: involvement of G6f, a novel platelet Grb2-binding membrane adapter.
    Proteomics. 2006 Oct;6(19):5332-43 PMID: 16941570
Article Info
Journal
Molecular & cellular proteomics : MCP
Abbr.
Mol Cell Proteomics
ISSN
1535-9476
Published
2007-03-00
Epub
2006-00-23
Pages
548-64
Language
English
Region
United States
NLM ID
101125647
PMCID
PMC1860054
Subset
IM
Grants
Wellcome Trust · United Kingdom
British Heart Foundation · CH/03/003/15571 · United Kingdom
Medical Research Council · G0400247 · United Kingdom
Databases
GEO
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