Skip to main content

Advertisement

SpringerLink
Log in

Profiling and semiquantitative analysis of the cell surface proteome in human mesenchymal stem cells

  • Original Paper
  • Published:
Analytical and Bioanalytical Chemistry Aims and scope Submit manuscript

Abstract

Mulitpotent mesenchymal stem cells (MSCs) derived from human bone marrow are promising candidates for the development of cell therapeutic strategies. MSC surface protein profiles provide novel biological knowledge concerning the proliferation and differentiation of these cells, including the potential for identifying therapeutic targets. Basic fibroblast growth factor (bFGF) affects cell surface proteins, which are associated with increased growth rate, differentiation potential, as well as morphological changes of MSCs in vitro. Cell surface proteins were isolated using a biotinylation-mediated method and identified using a combination of one-dimensional sodium dodecyl sulfate–polyacrylamide gel electrophoresis and mass spectrometry. The resulting gel lines were cut into 20 bands and digested with trypsin. Each tryptic fragment was analyzed by liquid chromatography–electrospray ionization tandem mass spectrometry. Proteins were identified using the Mascot search program and the International Protein Index human database. Noble MSC surface proteins (n = 1,001) were identified from cells cultured either with (n = 857) or without (n = 667) bFGF-containing medium in three independent experiments. The proteins were classified using FatiGO to elucidate their function. We also confirmed the proteomics results using Western blotting and immunofluorescence microscopic analysis. The nature of the proteins identified makes it clear that MSCs express a wide variety of signaling molecules, including those related to cell differentiation. Among the latter proteins, four Ras-related Rab proteins, laminin-R, and three 14-3-3 proteins that were fractionated from MSCs cultured on bFGF-containing medium are implicated in bFGF-induced signal transduction of MSCs. Consequently, these finding provide insight into the understanding of the surface proteome of human MSCs.

ᅟ

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71–74

    Article  CAS  Google Scholar 

  2. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M et al (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41–49

    Article  CAS  Google Scholar 

  3. Krause DS (2002) Plasticity of marrow-derived stem cells. Gene Ther 9:754–758

    Article  CAS  Google Scholar 

  4. Phinney DG, Kopen G, Isaacson RL, Prockop DJ (1999) Plastic adherent stromal cells from the bone marrow of commonly used strains of inbred mice: variations in yield, growth, and differentiation. J Cell Biochem 72:570–585

    Article  CAS  Google Scholar 

  5. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147

    Article  CAS  Google Scholar 

  6. Brazelton TR, Rossi FM, Keshet GI, Blau HM (2000) From marrow to brain: expression of neuronal phenotypes in adult mice. Science 290:1775–1779

    Article  CAS  Google Scholar 

  7. Hermann A, Gastl R, Liebau S, Popa MO, Fiedler J, Boehm BO, Maisel M, Lerche H, Schwarz J, Brenner R, Storch A (2004) Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J Cell Sci 117:4411–4422

    Article  CAS  Google Scholar 

  8. Woodbury D, Schwarz EJ, Prockop DJ, Black IB (2000) Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 61:364–370

    Article  CAS  Google Scholar 

  9. Barry FP, Murphy JM (2004) Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 36:568–584

    Article  CAS  Google Scholar 

  10. Beyaert R, Fiers W (1994) Molecular mechanisms of tumor necrosis factor-induced cytotoxicity. What we do understand and what we do not. FEBS Lett 340:9–16

    Article  CAS  Google Scholar 

  11. Aggarwal S, Pittenger MF (2005) Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105:1815–1822

    Article  CAS  Google Scholar 

  12. Horwitz EM, Gordon PL, Koo WK, Marx JC, Neel MD, McNall RY, Muul L, Hofmann T (2002) Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone. Proc Natl Acad Sci USA 99:8932–8937

    Article  CAS  Google Scholar 

  13. Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, Neel M, Sussman M, Orchard P, Marx JC, Pyeritz RE, Brenner MK (1999) Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 5:309–313

    Article  CAS  Google Scholar 

  14. Koc ON, Day J, Nieder M, Gerson SL, Lazarus HM, Krivit W (2002) Allogeneic mesenchymal stem cell infusion for treatment of metachromatic leukodystrophy (MLD) and Hurler syndrome (MPS-IH). Bone Marrow Transplant 30:215–222

    Article  CAS  Google Scholar 

  15. Quarto R, Mastrogiacomo M, Cancedda R, Kutepov SM, Mukhachev V, Lavroukov A, Kon E, Marcacci M (2001) Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med 344:385–386

    Article  CAS  Google Scholar 

  16. Amos TA, Gordon MY (1995) Sources of human hematopoietic stem cells for transplantation – a review. Cell Transplant 4:547–569

    CAS  Google Scholar 

  17. Mueller SM, Glowacki J (2001) Age-related decline in the osteogenic potential of human bone marrow cells cultured in three-dimensional collagen sponges. J Cell Biochem 82:583–590

    Article  CAS  Google Scholar 

  18. Stenderup K, Justesen J, Clausen C, Kassem M (2003) Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33:919–926

    Article  Google Scholar 

  19. Sun HJ, Bahk YY, Choi YR, Shim JH, Han SH, Lee JW (2006) A proteomic analysis during serial subculture and osteogenic differentiation of human mesenchymal stem cell. J Orthop Res 24:2059–2071

    Article  CAS  Google Scholar 

  20. Akita S, Akino K, Tanaka K, Anraku K, Hirano A (2008) A basic fibroblast growth factor improves lower extremity wound healing with a porcine-derived skin substitute. J Trauma 64:809–815

    Article  CAS  Google Scholar 

  21. Douwes Dekker PB, Kuipers-Dijkshoorn NJ, Baelde HJ, van der Mey AG, Hogendoorn PC, Cornelisse CJ (2007) Basic fibroblast growth factor and fibroblastic growth factor receptor-1 may contribute to head and neck paraganglioma development by an autocrine or paracrine mechanism. Hum Pathol 38:79–85

    Article  CAS  Google Scholar 

  22. Kashiwakura I, Takahashi TA (2005) Fibroblast growth factor and ex vivo expansion of hematopoietic progenitor cells. Leuk Lymphoma 46:329–333

    Article  CAS  Google Scholar 

  23. Ornitz DM, Itoh N (2001) Fibroblast growth factors. Genome Biol 2:reviews3005.3001–reviews3005.3012

    Article  Google Scholar 

  24. Naski MC, Ornitz DM (1998) FGF signaling in skeletal development. Front Biosci 3:d781–d794

    CAS  Google Scholar 

  25. Eswarakumar VP, Lax I, Schlessinger J (2005) Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 16:139–149

    Article  CAS  Google Scholar 

  26. Akesson E, Piao JH, Samuelsson EB, Holmberg L, Kjaeldgaard A, Falci S, Sundstrom E, Seiger A (2007) Long-term culture and neuronal survival after intraspinal transplantation of human spinal cord-derived neurospheres. Physiol Behav 92:60–66

    Article  CAS  Google Scholar 

  27. Gronthos S, Franklin DM, Leddy HA, Robey PG, Storms RW, Gimble JM (2001) Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol 189:54–63

    Article  CAS  Google Scholar 

  28. Haynesworth SE, Baber MA, Caplan AI (1992) Cell surface antigens on human marrow-derived mesenchymal cells are detected by monoclonal antibodies. Bone 13:69–80

    Article  CAS  Google Scholar 

  29. Tocci A, Forte L (2003) Mesenchymal stem cell: use and perspectives. Hematol J 4:92–96

    Article  Google Scholar 

  30. Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U, Blake J, Schwager C, Eckstein V, Ansorge W, Ho AD (2005) Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 33:1402–1416

    Article  CAS  Google Scholar 

  31. Abdallah BM, Jensen CH, Gutierrez G, Leslie RG, Jensen TG, Kassem M (2004) Regulation of human skeletal stem cells differentiation by Dlk1/Pref-1. J Bone Miner Res 19:841–852

    Article  CAS  Google Scholar 

  32. Owen TA, Aronow M, Shalhoub V, Barone LM, Wilming L, Tassinari MS, Kennedy MB, Pockwinse S, Lian JB, Stein GS (1990) Progressive development of the rat osteoblast phenotype in vitro: reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. J Cell Physiol 143:420–430

    Article  CAS  Google Scholar 

  33. Paulsen IT, Sliwinski MK, Nelissen B, Goffeau A, Saier MH Jr (1998) Unified inventory of established and putative transporters encoded within the complete genome of Saccharomyces cerevisiae. FEBS Lett 430:116–125

    Article  CAS  Google Scholar 

  34. Wallin E, von Heijne G (1998) Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci 7:1029–1038

    Article  CAS  Google Scholar 

  35. Nunomura K, Nagano K, Itagaki C, Taoka M, Okamura N, Yamauchi Y, Sugano S, Takahashi N, Izumi T, Isobe T (2005) Cell surface labeling and mass spectrometry reveal diversity of cell surface markers and signaling molecules expressed in undifferentiated mouse embryonic stem cells. Mol Cell Proteomics 4:1968–1976

    Article  CAS  Google Scholar 

  36. Chen WN, Yu LR, Strittmatter EF, Thrall BD, Camp DG 2nd, Smith RD (2003) Detection of in situ labeled cell surface proteins by mass spectrometry: application to the membrane subproteome of human mammary epithelial cells. Proteomics 3:1647–1651

    Article  CAS  Google Scholar 

  37. Sabarth N, Lamer S, Zimny-Arndt U, Jungblut PR, Meyer TF, Bumann D (2002) Identification of surface proteins of Helicobacter pylori by selective biotinylation, affinity purification, and two-dimensional gel electrophoresis. J Biol Chem 277:27896–27902

    Article  CAS  Google Scholar 

  38. Zhang W, Zhou G, Zhao Y, White MA (2003) Affinity enrichment of plasma membrane for proteomics analysis. Electrophoresis 24:2855–2863

    Article  CAS  Google Scholar 

  39. Zhao Y, Zhang W, Kho Y (2004) Proteomic analysis of integral plasma membrane proteins. Anal Chem 76:1817–1823

    Article  CAS  Google Scholar 

  40. Al-Shahrour F, Diaz-Uriarte R, Dopazo J (2004) FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics 20:578–580

    Article  CAS  Google Scholar 

  41. Kim SS, Choi JM, Kim JW, Ham DS, Ghil SH, Kim MK, Kim-Kwon Y, Hong SY, Ahn SC, Kim SU et al (2005) cAMP induces neuronal differentiation of mesenchymal stem cells via activation of extracellular signal-regulated kinase/MAPK. Neuroreport 16:1357–1361

    Article  CAS  Google Scholar 

  42. Link AJ, Eng J, Schieltz DM, Carmack E, Mize GJ, Morris DR, Garvik BM, Yates JR 3rd (1999) Direct analysis of protein complexes using mass spectrometry. Nat Biotechnol 17:676–682

    Article  CAS  Google Scholar 

  43. Moore RE, Young MK, Lee TD (2002) Qscore: an algorithm for evaluating SEQUEST database search results. J Am Soc Mass Spectrom 13:378–386

    Article  CAS  Google Scholar 

  44. Wu SL, Choudhary G, Ramstrom M, Bergquist J, Hancock WS (2003) Evaluation of shotgun sequencing for proteomic analysis of human plasma using HPLC coupled with either ion trap or Fourier transform mass spectrometry. J Proteome Res 2:383–393

    Article  CAS  Google Scholar 

  45. Elschenbroich S, Kim Y, Medin JA, Kislinger T (2010) Isolation of cell surface proteins for mass spectrometry-based proteomics. Expert Rev Proteomics 7(1):141–154

    Article  CAS  Google Scholar 

  46. Kemper K, Sprick MR, de Bree M, Scopelliti A, Vermeulen L, Hoek M, Zeilstra J, Pals ST, Mehmet H, Stassi G, Medema JP (2010) The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res 70(2):719–729

    Article  CAS  Google Scholar 

  47. Mastroleo F, Leroy B, Van Houdt R, s’ Heeren C, Mergeay M, Hendrickx L, Wattiez R (2009) Shotgun proteome analysis of Rhodospirillum rubrum S1H: integrating data from gel-free and gel-based peptides fractionation methods. J Proteome Res 8(5):2530–2541

    Article  CAS  Google Scholar 

  48. Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, Rappsilber J, Mann M (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4:1265–1272

    Article  CAS  Google Scholar 

  49. Deans RJ, Moseley AB (2000) Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol 28:875–884

    Article  CAS  Google Scholar 

  50. Ohgushi H, Caplan AI (1999) Stem cell technology and bioceramics: from cell to gene engineering. J Biomed Mater Res 48:913–927

    Article  CAS  Google Scholar 

  51. Wang D, Park JS, Chu JS, Krakowski A, Luo K, Chen DJ, Li S (2004) Proteomic profiling of bone marrow mesenchymal stem cells upon transforming growth factor beta1 stimulation. J Biol Chem 279:43725–43734

    Article  CAS  Google Scholar 

  52. Lee SK, Kim Y, Kim SS, Lee JH, Cho K, Lee SS, Lee ZW, Kwon KH, Kim YH, Suh-Kim H et al (2009) Differential expression of cell surface proteins in human bone marrow mesenchymal stem cells cultured with or without basic fibroblast growth factor containing medium. Proteomics 9:4389–4405

    Article  CAS  Google Scholar 

  53. Jeong JA, Lee Y, Lee W, Jung S, Lee DS, Jeong N, Lee HS, Bae Y, Jeon CJ, Kim H (2006) Proteomic analysis of the hydrophobic fraction of mesenchymal stem cells derived from human umbilical cord blood. Mol Cells 22:36–43

    CAS  Google Scholar 

  54. Gautier V, Mouton-Barbosa E, Bouyssié D, Delcourt N, Beau M, Girard JP, Cayrol C, Burlet-Schiltz O, Monsarrat B, Gonzalez de Peredo A (2012) Label-free quantification and shotgun analysis of complex proteomes by one-dimensional SDS-PAGE/NanoLC-MS: evaluation for the large scale analysis of inflammatory human endothelial cells. Mol Cell Proteomics 11(8):527–539

    Article  CAS  Google Scholar 

  55. Gygi SP, Corthals GL, Zhang Y, Rochon Y, Aebersold R (2000) Evaluation of two-dimensional gel electrophoresis-based proteome analysis technology. Proc Natl Acad Sci USA 97(17):9390–9395

    Article  CAS  Google Scholar 

  56. Reuss B, von Bohlen und Halbach O (2003) Fibroblast growth factors and their receptors in the central nervous system. Cell Tissue Res 313:139–157

    Article  CAS  Google Scholar 

  57. Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2:107–117

    Article  CAS  Google Scholar 

  58. Ferro-Novick S, Novick P (1993) The role of GTP-binding proteins in transport along the exocytic pathway. Annu Rev Cell Biol 9:575–599

    Article  CAS  Google Scholar 

  59. Novick P, Brennwald P (1993) Friends and family: the role of the Rab GTPases in vesicular traffic. Cell 75:597–601

    Article  CAS  Google Scholar 

  60. Pfeffer SR (1994) Rab GTPases: master regulators of membrane trafficking. Curr Opin Cell Biol 6:522–526

    Article  CAS  Google Scholar 

  61. Zerial M, Stenmark H (1993) Rab GTPases in vesicular transport. Curr Opin Cell Biol 5:613–620

    Article  CAS  Google Scholar 

  62. Sonnichsen B, De Renzis S, Nielsen E, Rietdorf J, Zerial M (2000) Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol 149:901–914

    Article  CAS  Google Scholar 

  63. Bhattacharya M, Babwah AV, Ferguson SS (2004) Small GTP-binding protein-coupled receptors. Biochem Soc Trans 32:1040–1044

    Article  CAS  Google Scholar 

  64. Feng Y, Press B, Wandinger-Ness A (1995) Rab 7: an important regulator of late endocytic membrane traffic. J Cell Biol 131:1435–1452

    Article  CAS  Google Scholar 

  65. Garin J, Diez R, Kieffer S, Dermine JF, Duclos S, Gagnon E, Sadoul R, Rondeau C, Desjardins M (2001) The phagosome proteome: insight into phagosome functions. J Cell Biol 152:165–180

    Article  CAS  Google Scholar 

  66. Ang AL, Folsch H, Koivisto UM, Pypaert M, Mellman I (2003) The Rab8 GTPase selectively regulates AP-1B-dependent basolateral transport in polarized Madin-Darby canine kidney cells. J Cell Biol 163:339–350

    Article  CAS  Google Scholar 

  67. Chen W, Feng Y, Chen D, Wandinger-Ness A (1998) Rab11 is required for trans-golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor. Mol Biol Cell 9:3241–3257

    CAS  Google Scholar 

  68. Li Y, Luo L, Schubert M, Wagner RR, Kang CY (1993) Viral liposomes released from insect cells infected with recombinant baculovirus expressing the matrix protein of vesicular stomatitis virus. J Virol 67:4415–4420

    CAS  Google Scholar 

  69. Zhang W, Yang H, Kong X, Mohapatra S, San Juan-Vergara H, Hellermann G, Behera S, Singam R, Lockey RF, Mohapatra SS (2005) Inhibition of respiratory syncytial virus infection with intranasal siRNA nanoparticles targeting the viral NS1 gene. Nat Med 11:56–62

    Article  CAS  Google Scholar 

  70. Ang AL, Taguchi T, Francis S, Folsch H, Murrells LJ, Pypaert M, Warren G, Mellman I (2004) Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells. J Cell Biol 167:531–543

    Article  CAS  Google Scholar 

  71. Chen YA, Scales SJ, Patel SM, Doung YC, Scheller RH (1999) SNARE complex formation is triggered by Ca2+ and drives membrane fusion. Cell 97:165–174

    Article  CAS  Google Scholar 

  72. Harris E, Yoshida K, Cardelli J, Bush J (2001) Rab11-like GTPase associates with and regulates the structure and function of the contractile vacuole system in dictyostelium. J Cell Sci 114:3035–3045

    CAS  Google Scholar 

  73. Drubin DG, Nelson WJ (1996) Origins of cell polarity. Cell 84:335–344

    Article  CAS  Google Scholar 

  74. Peranen J, Auvinen P, Virta H, Wepf R, Simons K (1996) Rab8 promotes polarized membrane transport through reorganization of actin and microtubules in fibroblasts. J Cell Biol 135:153–167

    Article  CAS  Google Scholar 

  75. Peranen J, Furuhjelm J (2001) Expression, purification, and properties of Rab8 function in actin cortical skeleton organization and polarized transport. Methods Enzymol 329:188–196

    Article  CAS  Google Scholar 

  76. Ren M, Zeng J, De Lemos-Chiarandini C, Rosenfeld M, Adesnik M, Sabatini DD (1996) In its active form, the GTP-binding protein rab8 interacts with a stress-activated protein kinase. Proc Natl Acad Sci U S A 93:5151–5155

    Article  CAS  Google Scholar 

  77. Morrison DK (2009) The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development. Trends Cell Biol 19:16–23

    Article  CAS  Google Scholar 

  78. Aitken A (2006) 14-3-3 proteins: a historic overview. Semin Cancer Biol 16:162–172

    Article  CAS  Google Scholar 

  79. Mackintosh C (2004) Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem J 381:329–342

    Article  CAS  Google Scholar 

  80. Yaffe MB, Elia AE (2001) Phosphoserine/threonine-binding domains. Curr Opin Cell Biol 13:131–138

    Article  CAS  Google Scholar 

  81. Furdui CM, Lew ED, Schlessinger J, Anderson KS (2006) Autophosphorylation of FGFR1 kinase is mediated by a sequential and precisely ordered reaction. Mol Cell 21:711–717

    Article  CAS  Google Scholar 

  82. Hinsby AM, Olsen JV, Mann M (2004) Tyrosine phosphoproteomics of fibroblast growth factor signaling: a role for insulin receptor substrate-4. J Biol Chem 279:46438–46447

    Article  CAS  Google Scholar 

  83. Lundin L, Ronnstrand L, Cross M, Hellberg C, Lindahl U, Claesson-Welsh L (2003) Differential tyrosine phosphorylation of fibroblast growth factor (FGF) receptor-1 and receptor proximal signal transduction in response to FGF-2 and heparin. Exp Cell Res 287:190–198

    Article  CAS  Google Scholar 

  84. Mohammadi M, Dikic I, Sorokin A, Burgess WH, Jaye M, Schlessinger J (1996) Identification of six novel autophosphorylation sites on fibroblast growth factor receptor 1 and elucidation of their importance in receptor activation and signal transduction. Mol Cell Biol 16:977–989

    CAS  Google Scholar 

  85. Mohammadi M, Dionne CA, Li W, Li N, Spivak T, Honegger AM, Jaye M, Schlessinger J (1992) Point mutation in FGF receptor eliminates phosphatidylinositol hydrolysis without affecting mitogenesis. Nature 358:681–684

    Article  CAS  Google Scholar 

  86. Lonic A, Barry EF, Quach C, Kobe B, Saunders N, Guthridge MA (2008) Fibroblast growth factor receptor 2 phosphorylation on serine 779 couples to 14-3-3 and regulates cell survival and proliferation. Mol Cell Biol 28:3372–3385

    Article  CAS  Google Scholar 

  87. Fiegel HC, Kluth J, Lioznov MV, Holzhuter S, Fehse B, Zander AR, Kluth D (2003) Hepatic lineages isolated from developing rat liver show different ways of maturation. Biochem Biophys Res Commun 305:46–53

    Article  CAS  Google Scholar 

  88. Fiegel HC, Park JJ, Lioznov MV, Martin A, Jaeschke-Melli S, Kaufmann PM, Fehse B, Zander AR, Kluth D (2003) Characterization of cell types during rat liver development. Hepatology 37:148–154

    Article  Google Scholar 

  89. Petersen BE, Goff JP, Greenberger JS, Michalopoulos GK (1998) Hepatic oval cells express the hematopoietic stem cell marker Thy-1 in the rat. Hepatology 27:433–445

    Article  CAS  Google Scholar 

  90. Thorgeirsson SS (1996) Hepatic stem cells in liver regeneration. FASEB J 10:1249–1256

    CAS  Google Scholar 

  91. Javazon EH, Colter DC, Schwarz EJ, Prockop DJ (2001) Rat marrow stromal cells are more sensitive to plating density and expand more rapidly from single-cell-derived colonies than human marrow stromal cells. Stem Cells 19:219–225

    Article  CAS  Google Scholar 

  92. Anderson RG (1998) The caveolae membrane system. Annu Rev Biochem 67:199–225

    Article  CAS  Google Scholar 

  93. Brown DA, London E (1998) Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 14:111–136

    Article  CAS  Google Scholar 

  94. Galbiati F, Razani B, Lisanti MP (2001) Emerging themes in lipid rafts and caveolae. Cell 106:403–411

    Article  CAS  Google Scholar 

  95. Okamoto T, Schlegel A, Scherer PE, Lisanti MP (1998) Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J Biol Chem 273:5419–5422

    Article  CAS  Google Scholar 

  96. Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1:31–39

    Article  CAS  Google Scholar 

  97. Smart EJ, Graf GA, McNiven MA, Sessa WC, Engelman JA, Scherer PE, Okamoto T, Lisanti MP (1999) Caveolins, liquid-ordered domains, and signal transduction. Mol Cell Biol 19:7289–7304

    CAS  Google Scholar 

  98. Park WY, Park JS, Cho KA, Kim DI, Ko YG, Seo JS, Park SC (2000) Up-regulation of caveolin attenuates epidermal growth factor signaling in senescent cells. J Biol Chem 275:20847–20852

    Article  CAS  Google Scholar 

  99. Volonte D, Zhang K, Lisanti MP, Galbiati F (2002) Expression of caveolin-1 induces premature cellular senescence in primary cultures of murine fibroblasts. Mol Biol Cell 13:2502–2517

    Article  CAS  Google Scholar 

  100. Aumailley M, Bruckner-Tuderman L, Carter WG, Deutzmann R, Edgar D, Ekblom P, Engel J, Engvall E, Hohenester E, Jones JC et al (2005) A simplified laminin nomenclature. Matrix Biol 24:326–332

    Article  CAS  Google Scholar 

  101. Ekblom P, Lonai P, Talts JF (2003) Expression and biological role of laminin-1. Matrix Biol 22:35–47

    Article  CAS  Google Scholar 

  102. Kibbey MC, Grant DS, Kleinman HK (1992) Role of the SIKVAV site of laminin in promotion of angiogenesis and tumor growth: an in vivo Matrigel model. J Natl Cancer Inst 84:1633–1638

    Article  CAS  Google Scholar 

  103. Kleinman HK, Weeks BS, Schnaper HW, Kibbey MC, Yamamura K, Grant DS (1993) The laminins: a family of basement membrane glycoproteins important in cell differentiation and tumor metastases. Vitam Horm 47:161–186

    Article  CAS  Google Scholar 

  104. Nurcombe V (1992) Laminin in neural development. Pharmacol Ther 56:247–264

    Article  CAS  Google Scholar 

  105. Li X, Chen Y, Scheele S, Arman E, Haffner-Krausz R, Ekblom P, Lonai P (2001) Fibroblast growth factor signaling and basement membrane assembly are connected during epithelial morphogenesis of the embryoid body. J Cell Biol 153:811–822

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants to Y.M.P. from the Korea Institute of Science & Technology Evaluation and Planning (2006–2004605) and from the Korea Basic Science Institute (G30124).

Study approval

The Institutional Review Board of Ajou University Medical Center (Suwon, Republic of Korea) approved this study.

Competing interests

The authors claim no competing interests.

Authors' contributions

S.K.L. conducted preliminary experiments and wrote the final manuscript. J.H.K., T.W.K., K.H.K., N.H.P., S.Y.Y., H.J.A., and J.S.Y. conducted the proteomic analysis. S.S.K. and H.S. performed the cell culture and prepared the samples. S.S.L. and Z.W.L. conducted the confocal microscopy analysis. Y.M.P. conceived the study, obtained grant funding, and participated in experimental design and coordination. All authors read and approved the final manuscript.

Author information

Author notes

  1. Sang Kwang Lee

    Present address: Eulji Medical and Biological Research Institute (EMBRI), Daejeon, 302-799, Republic of Korea

  2. Sang Sook Lee

    Present address: Department of Biology, Chungnam National University, Daejeon, 305-764, Republic of Korea

Authors and Affiliations

  1. Mass Spectrometry Research Center, Korea Basic Science Institute, Ochang, 363-887, Republic of Korea

    Sang Kwang Lee, Jae Ho Kim, Taewook Kang, Nam Hyun Park, Kyung-Hoon Kwon, Kun Cho, Su Yeoung Yun, Ji Young Han, Jong Shin Yoo & Young Mok Park

  2. Department of Anatomy, Ajou University, School of Medicine, Suwon, 443-749, Republic of Korea

    Sung-Soo Kim & Hae young Suh-Kim

  3. Graduate Schools of Analytical Science and Technology, Chungnam National University, Daejeon, 305-764, Republic of Korea

    Taewook Kang, Nam Hyun Park, Su Yeoung Yun, Jong Shin Yoo & Hyun Joo An

  4. Biotechnology Fusion Research Team, Korea Basic Science Institute, Daejeon, 305-333, Republic of Korea

    Sang Sook Lee, Zee Won Lee & Young Mok Park

  5. Mass Spectrometry Research Center, Korea Basic Science Institute, Ochang, 363-883, Republic of Korea

    Young Mok Park

Authors
  1. Sang Kwang Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jae Ho Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sung-Soo Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Taewook Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nam Hyun Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kyung-Hoon Kwon
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sang Sook Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zee Won Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hae young Suh-Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Kun Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Su Yeoung Yun
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Ji Young Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Jong Shin Yoo
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Hyun Joo An
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Young Mok Park
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Young Mok Park.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 724 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lee, S.K., Kim, J.H., Kim, SS. et al. Profiling and semiquantitative analysis of the cell surface proteome in human mesenchymal stem cells. Anal Bioanal Chem 405, 5501–5517 (2013). https://doi.org/10.1007/s00216-013-6969-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00216-013-6969-z

Keywords

Search

Navigation