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Proteomic Characterization of Mesenchymal Stem Cell-Like Populations Derived from Various Tissue Types

  • Krzysztof M. Mrozik
  • Jimin Xiong
  • Peter S. Zilm
  • Stan Gronthos
  • P. Mark Bartold
Chapter
Part of the Stem Cells and Cancer Stem Cells book series (STEM, volume 3)

Abstract

The evolution of proteomics has led to its application in identifying biomarkers of biological processes and pathways including signal transduction and cell development. Proteomic technologies are increasingly utilized to define the molecular mechanisms controlling mesenchymal stem/stromal cell (MSC) self-renewal, multipotency and fate. Bone marrow-derived MSCs are highly promising candidates in regenerative medicine based on their high proliferative capacity, multi-lineage differentiation potential and immunomodulatory properties. Recently, equivalent MSC-like populations have also been isolated from adipose, dental and various feto-maternal tissues. This chapter discusses the current technologies available for proteomic analysis and the studies performed on tissue-specific MSC-like populations to date.

Keywords

Adipose tissue Bone marrow Periodontal ligament Dental pulp Umbilical cord blood Mesenchymal stem cells (MSCs) Proteomics 

References

  1. Aebersold R, Cravatt BF (2002) Proteomics–advances, applications and the challenges that remain. Trends Biotechnol 20:S1–S2PubMedCrossRefGoogle Scholar
  2. Alldridge LC, Bryant CE (2003) Annexin 1 regulates cell proliferation by disruption of cell morphology and inhibition of cyclin D1 expression through sustained activation of the ERK1/2 MAPK signal. Exp Cell Res 290:93–107PubMedCrossRefGoogle Scholar
  3. Angelucci S, Marchisio M, Di Giuseppe F, Pierdomenico L, Sulpizio EE, Lanuti P, Sabatino G, Miscia S, Di Ilio C (2010) Proteome analysis of human Wharton’s jelly cells during in vitro expansion. Proteome Sci 8:18PubMedCrossRefGoogle Scholar
  4. Arthur A, Rychkov G, Shi S, Koblar SA, Gronthos S (2008) Adult human dental pulp stem cells differentiate toward functionally active neurons under appropriate environmental cues. Stem Cells 26:1787–1795PubMedCrossRefGoogle Scholar
  5. Bairoch A (2010) Bioinformatics for human proteomics: current state and future status. Nat Proc. http://precedings.nature.com/documents/5050/version/1
  6. Becker KF, Metzger V, Hipp S, Hofler H (2006) Clinical proteomics: new trends for protein microarrays. Curr Med Chem 13:1831–1837PubMedCrossRefGoogle Scholar
  7. Bennett KP, Bergeron C, Acar E, Klees RF, Vandenberg SL, Yener B, Plopper GE (2007) Proteomics reveals multiple routes to the osteogenic phenotype in mesenchymal stem cells. BMC Genomics 8:380PubMedCrossRefGoogle Scholar
  8. Bianco P, Riminucci M, Gronthos S, Robey PG (2001) Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19:180–192PubMedCrossRefGoogle Scholar
  9. Bieback K, Kern S, Kluter H, Eichler H (2004) Critical parameters for the isolation of mesenchymal stem cells from umbilical cord blood. Stem Cells 22:625–634PubMedCrossRefGoogle Scholar
  10. Chai Y, Jiang X, Ito Y, Bringas P Jr., Han J, Rowitch DH, Soriano P, McMahon AP, Sucov HM (2000) Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127:1671–1679PubMedGoogle Scholar
  11. Choi J, Levey AI, Weintraub ST, Rees HD, Gearing M, Chin LS, Li L (2004) Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson’s and Alzheimer’s diseases. J Biol Chem 279:13256–13264PubMedCrossRefGoogle Scholar
  12. Coates PJ, Nenutil R, McGregor A, Picksley SM, Crouch DH, Hall PA, Wright EG (2001) Mammalian prohibitin proteins respond to mitochondrial stress and decrease during cellular senescence. Exp Cell Res 265:262–273PubMedCrossRefGoogle Scholar
  13. Colter DC, Sekiya I, Prockop DJ (2001) Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. PNAS 98:7841–7845PubMedCrossRefGoogle Scholar
  14. Dechat T, Shimi T, Adam SA, Rusinol AE, Andres DA, Spielmann HP, Sinensky MS, Goldman RD (2007) Alterations in mitosis and cell cycle progression caused by a mutant lamin A known to accelerate human aging. PNAS 104:4955–4960PubMedCrossRefGoogle Scholar
  15. De Coppi P, Bartsch G Jr, Siddiqui MM, Xu T, Santos CC, Perin L, Mostoslavsky G, Serre AC, Snyder EY, Yoo JJ, Furth ME, Soker S, Atala A (2007) Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol 25:100–106PubMedCrossRefGoogle Scholar
  16. DeLany JP, Floyd ZE, Zvonic S, Smith A, Gravois A, Reiners E, Wu X, Kilroy G, Lefevre M, Gimble JM (2005) Proteomic analysis of primary cultures of human adipose-derived stem cells: modulation by adipogenesis. Mol Cell Proteomics 4:731–740PubMedCrossRefGoogle Scholar
  17. DeSouza L, Diehl G, Rodrigues MJ, Guo J, Romaschin AD, Colgan TJ, Siu KW (2005) Search for cancer markers from endometrial tissues using differentially labeled tags iTRAQ and cICAT with multidimensional liquid chromatography and tandem mass spectrometry. J Proteome Res 4:377–386PubMedCrossRefGoogle Scholar
  18. Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, Grisanti S, Gianni AM (2002) Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99:3838–3843PubMedCrossRefGoogle Scholar
  19. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop Dj, Horwitz E (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315–317PubMedCrossRefGoogle Scholar
  20. Eppinga RD, Li Y, Lin JL, Lin JJ (2006) Tropomyosin and caldesmon regulate cytokinesis speed and membrane stability during cell division. Arch Biochem Biophys 456:161–174PubMedCrossRefGoogle Scholar
  21. Erices A, Conget P, Minguell JJ (2000) Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol 109: 235–242PubMedCrossRefGoogle Scholar
  22. Eriksson JE, He T, Trejo-Skalli AV, Harmala-Brasken AS, Hellman J, Chou YH, Goldman RD (2004) Specific in vivo phosphorylation sites determine the assembly dynamics of vimentin intermediate filaments. J Cell Sci 117: 919–932PubMedCrossRefGoogle Scholar
  23. Evans CA, Tonge R, Blinco D, Pierce A, Shaw J, Lu Y, Hamzah HG, Gray A, Downes CP, Gaskell SJ, Spooncer E, Whetton AD (2004) Comparative proteomics of primitive hematopoietic cell populations reveals differences in expression of proteins regulating motility. Blood 103:3751–3759PubMedCrossRefGoogle Scholar
  24. Feldmann RE Jr., Bieback K, Maurer MH, Kalenka A, Bürgers HF, Gross B, Hunzinger C, Klüter H, Kuschinsky W, Eichler H (2005) Stem cell proteomes: a profile of human mesenchymal stem cells derived from umbilical cord blood. Electrophoresis 26:2749–2758PubMedCrossRefGoogle Scholar
  25. Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, Mavilio F (1998) Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279:1528–1530PubMedCrossRefGoogle Scholar
  26. Ferrell JE Jr. (1996) MAP kinases in mitogenesis and development. Curr Top Dev Biol 33:1–60PubMedCrossRefGoogle Scholar
  27. Fitter S, Dewar AL, Kostakis P, To LB, Hughes TP, Roberts MM, Lynch K, Vernon-Roberts B, Zannettino AC (2008) Long-term imatinib therapy promotes bone formation in CML patients. Blood 111:2538–2547PubMedCrossRefGoogle Scholar
  28. Foster LJ, Zeemann PA, Li C, Mann M, Jensen ON, Kassem M (2005) Differential expression profiling of membrane proteins by quantitative proteomics in a human mesenchymal stem cell line undergoing osteoblast differentiation. Stem Cells 23:1367–1377PubMedCrossRefGoogle Scholar
  29. Friedenstein AJ, Piatetzky SII, Petrakova KV (1966) Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol 16:381–390PubMedGoogle Scholar
  30. Gade D, Thiermann J, Markowsky D, Rabus R (2003) Evaluation of two-dimensional difference gel electrophoresis for protein profiling. Soluble proteins of the marine bacterium Pirellula sp. strain 1. J Mol Microbiol Biotechnol 5:240–251PubMedCrossRefGoogle Scholar
  31. Garcia-Gomez I, Elvira G, Zapata AG, Lamana ML, Ramirez M, Castro JG, Arranz MG, Vincente A, Bueren J, Garcia-Olmo D (2010) Mesenchymal stem cells: biological properties and clinical applications. Expert Opin Biol Ther 10:1453–1468PubMedCrossRefGoogle Scholar
  32. Gimble J, Guilak F (2003) Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy 5:362–369PubMedCrossRefGoogle Scholar
  33. Giusta MS, Andrade H, Santos AV, Castanheira P, Lamana L, Pimenta AMC, Goes AM (2010) Proteomic analysis of human mesenchymal stromal cells derived from adipose tissue undergoing osteoblast differentiation. Cytotherapy 12:478–490PubMedCrossRefGoogle Scholar
  34. Gorg A, Boguth G, Obermaier C, Weiss W (1998) Two-dimensional electrophoresis of proteins in an immobilized pH 4-12 gradient. Electrophoresis 19:1516–1519PubMedCrossRefGoogle Scholar
  35. Gronthos S, Graves SE, Ohta S, Simmons PJ (1994) The STRO-1+ fraction of adult human bone marrow contains the osteogenic precursors. Blood 84:4164–4173PubMedGoogle Scholar
  36. Gronthos S, Mankani M, Brahim J, Robey PG, Shi S (2000) Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. PNAS 97:13625–13630PubMedCrossRefGoogle Scholar
  37. Gronthos S, Zannettino AC, Hay SJ, Shi S, Graves SE, Kortesidis A, Simmons PJ (2003) Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 116:1827–1835PubMedCrossRefGoogle Scholar
  38. Gronthos S, Fitter S, Diamond P, Simmons PJ, Itescu S, Zannettino AC (2007) A novel monoclonal antibody (STRO-3) identifies an isoform of tissue nonspecific alkaline phosphatase expressed by multipotent bone marrow stromal stem cells. Stem Cells Dev 16:953–963PubMedCrossRefGoogle Scholar
  39. Gronthos S, McCarty R, Mrozik K, Fitter S, Paton S, Menicanin D, Itescu S, Bartold PM, Xian C, Zannettino ACW (2009) Heat shock protein-90 beta is expressed at the surface of multipotential mesenchymal precursor cells: generation of a novel monoclonal antibody, STRO-4, with specificity for mesenchymal precursor cells from human and ovine tissues. Stem Cells Dev 18:1253–1262PubMedCrossRefGoogle Scholar
  40. Gygi SP, Rochon Y, Franza BR, Aebersold R (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19:1720–1730PubMedGoogle Scholar
  41. Huang GP, Pan ZJ, Huang JP, Yang JF, Guo CJ, Wang YG, Zheng Q, Chen R, Xu YL, Wang GZ, Xi YM, Shen D, Jin J, Wang JF (2008a) Proteomic analysis of human bone marrow mesenchymal stem cells transduced with human telomerase reverse transcriptase gene during proliferation. Cell Prolif 41:625–644PubMedCrossRefGoogle Scholar
  42. Huang GT, Sonoyama W, Liu Y, Liu H, Wang S, Shi S (2008b) The hidden treasure in apical papilla: the potential role in pulp/dentin regeneration and bioroot engineering. J Endod 34:645–651PubMedCrossRefGoogle Scholar
  43. Jeong JA, Lee Y, Lee W, Jung S, Lee D, Jeong N, Lee HS, Bae Y, Jeon C, Kim H (2006) Proteomic analysis of the hydrophobic fraction of mesenchymal stem cells derived from human umbilical cord blood. Mol Cells 22:36–43PubMedGoogle Scholar
  44. Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU (1998) In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 238:265–272PubMedCrossRefGoogle Scholar
  45. Kadri T, Lataillade JJ, Doucet C, Marie A, Ernou I, Bourin P, Joubert-Caron R, Caron M, Lutomski D (2005) Proteomic study of Galectin-1 expression in human mesenchymal stem cells. Stem Cells Dev 14:204–212PubMedCrossRefGoogle Scholar
  46. Kaneki H, Takasugi I, Fujieda M, Kiriu M, Mizuochi S, Ide H (1999) Prostaglandin E2 stimulates the formation of mineralized bone nodules by a cAMP-independent mechanism in the culture of adult rat calvarial osteoblasts. J Cell Biochem 73:36–48PubMedCrossRefGoogle Scholar
  47. Karas M, Hillenkamp F (1988) Laser desorption ionization of proteins with molecular masses exceeding 10,000 daltons. Anal Chem 60:2299–2301PubMedCrossRefGoogle Scholar
  48. Kawano Y, Yoshimura T, Tsuboi D, Kawabata S, Kaneko-Kawano T, Shirataki H, Takenawa T, Kaibuchi K (2005) CRMP-2 is involved in kinesin-1-dependent transport of the Sra-1/WAVE1 complex and axon formation. Mol Cell Biol 25:9920–9935PubMedCrossRefGoogle Scholar
  49. Kim JS, Lee HK, Kim MR, Kim PK, Kim CW (2008) Differentially expressed proteins of mesenchymal stem cells derived from human cord blood (hUCB) during osteogenic differentiation. Biosci Biotechnol Biochem 72:2309–2317PubMedCrossRefGoogle Scholar
  50. Kim S, Min WK, Chun S, Lee W, Chung H, Choi SJ, Yang SE, Yang YS, Yoo J (2010) Protein expression profiles during osteogenic differentiation of mesenchymal stem cells derived from human umbilical cord blood. Tohoku J Exp Med 221:141–150PubMedCrossRefGoogle Scholar
  51. Kratchmarova I, Blagoev B, Haack-Sorensen M, Kassem M, Mann M (2005) Mechanism of divergent growth factor effects in mesenchymal stem cell differentiation. Science 308:1472–1477PubMedCrossRefGoogle Scholar
  52. Lahm HW, Langen H (2000) Mass spectrometry: a tool for the identification of proteins separated by gels. Electrophoresis 21:2105–2114PubMedCrossRefGoogle Scholar
  53. Le Blanc K, Tammik L, Sundberg B, Haynesworth SE, Ringden O (2003) Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol 57:11–20PubMedCrossRefGoogle Scholar
  54. Lee WC, Lee KH (2004) Applications of affinity chromatography in proteomics. Anal Biochem 324:1–10PubMedCrossRefGoogle Scholar
  55. Lee HK, Lee BH, Park SA, Kim CW (2006) The proteomic analysis of an adipocyte differentiated from human mesenchymal stem cells using two-dimensional gel electrophoresis. Proteomics 6:1223–1229PubMedCrossRefGoogle Scholar
  56. Lee MJ, Kim J, Kim MY, Bae YS, Ryu SH, Lee TG, Kim JH (2010) Proteomic analysis of tumor necrosis factor-alpha-induced secretome of human adipose tissue-derived mesenchymal stem cells. J Proteome Res 9:1754–1762PubMedCrossRefGoogle Scholar
  57. Li G, Zhang XA, Wang H, Wang X, Meng C, Chan C, Yew DTW, Tsang KS, Li K, Tsai S, Ngai S, Han ZC, Lin MC, He M, Kung H (2009) Comparative proteomic analysis of mesenchymal stem cells derived from human bone marrow, umbilical cord, and placenta: implication in the migration. Proteomics 9:20–30PubMedCrossRefGoogle Scholar
  58. Makridakis M, Vlahou A (2010) Secretome proteomics for discovery of cancer biomarkers. J Proteomics 73:2291–2305PubMedCrossRefGoogle Scholar
  59. Mareddy S, Broadbent J, Crawford R, Xiao Y (2009) Proteomic profiling of distinct clonal populations of bone marrow mesenchymal stem cells. J Cell Biochem 106:776–786PubMedCrossRefGoogle Scholar
  60. Martens TP, See F, Schuster MD, Sondermeijer HP, Hefti MM, Zannettino A, Gronthos S, Seki T, Itescu S (2006) Mesenchymal lineage precursor cells induce vascular network formation in ischemic myocardium. Nat Clin Pract Cardiovasc Med 3(Suppl 1):S18–22PubMedCrossRefGoogle Scholar
  61. Matlin AJ, Clark F, Smith CW (2005) Understanding alternative splicing: towards a cellular code. Nat Rev Mol Cell Biol 6:386–398PubMedCrossRefGoogle Scholar
  62. Menicanin D, Bartold PM, Zannettino AC, Gronthos S (2009) Genomic profiling of mesenchymal stem cells. Stem Cell Rev Rep 5:36–50CrossRefGoogle Scholar
  63. Menicanin D, Bartold PM, Zannettino AC, Gronthos S (2010) Identification of a common gene expression signature associated with immature clonal mesenchymal cell populations derived from bone marrow and dental tissues. Stem Cells Dev 19:1501–1510PubMedCrossRefGoogle Scholar
  64. Miao Z, Jin J, Chen L, Zhu J, Huang W, Zhao J, Qian H, Zhang X (2006) Isolation of mesenchymal stem cells from human placenta: comparison with human bone marrow mesenchymal stem cells. Cell Biol Int 30:681–687PubMedCrossRefGoogle Scholar
  65. Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey P, Shi S (2003) SHED: stem cells from human exfoliated deciduous teeth. PNAS 100:5807–5812PubMedCrossRefGoogle Scholar
  66. Monticone M, Liu Y, Tonachini L, Mastrogiacomo M, Parodi S, Quarto R, Cancedda R, Castagnola P (2004) Gene expression profile of human bone marrow stromal cells determined by restriction fragment differential display analysis. J Cell Biochem 92:733–744PubMedCrossRefGoogle Scholar
  67. Morsczeck C, Gotz W, Schierholz J, Zeilhofer F, Kühn U, Möhl C, Sippel C, Hoffmann KH (2005) Isolation of precursor cells (PCs) from human dental follicle of wisdom teeth. Matrix Biol 24:155–165PubMedCrossRefGoogle Scholar
  68. Morsczeck C, Petersen J, Vollner F, Driemel O, Reichert T, Beck HC (2009) Proteomic analysis of osteogenic differentiation of dental follicle precursor cells. Electrophoresis 30:1175–1184PubMedCrossRefGoogle Scholar
  69. Mrozik KM, Zilm PS, Bagley CJ, Hack S, Hoffmann P, Gronthos S, Bartold PM (2010) Proteomic characterization of mesenchymal stem cell-like populations derived from ovine periodontal ligament, dental pulp, and bone marrow: analysis of differentially expressed proteins. Stem Cells Dev 19:1485–1499PubMedCrossRefGoogle Scholar
  70. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, Mann M (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1(5):376–386PubMedCrossRefGoogle Scholar
  71. Ong SY, Dai H, Leong KW (2006) Hepatic differentiation potential of commercially available human mesenchymal stem cells. Tissue Eng 12:3477–3485PubMedCrossRefGoogle Scholar
  72. Panepucci RA, Siufi JL, Silva WA Jr., Proto-Siquiera R, Neder L, Orellana M, Rocha V, Covas DT, Zago MA (2004) Comparison of gene expression of umbilical cord vein and bone marrow-derived mesenchymal stem cells. Stem Cells 22:1263–1278PubMedCrossRefGoogle Scholar
  73. Park HW, Shin JS, Kim CW (2007) Proteome of mesenchymal stem cells. Proteomics 7:2881–2894PubMedCrossRefGoogle Scholar
  74. Petrak J, Ivanek R, Toman O, Cmejla R, Cmejlova J, Vyoral D, Zivny J, Vulpe CD (2008) Deja vu in proteomics. A hit parade of repeatedly identified differentially expressed proteins. Proteomics 8:1744–1749PubMedCrossRefGoogle Scholar
  75. 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 284:143–147PubMedCrossRefGoogle Scholar
  76. Pivoriuunas A, Surovas A, Borutinskaitė V, Matuzevičius D, Treigytė G, Savickienė J, Tunaitis V, Aldonytė R, Jarmalavičiuutė A, Suriakaitė K, Liutkevičius E, Venalis A, Navakauskas D, Navakauskienė R, Magnusson K (2010) Proteomic analysis of stromal cells derived from the dental pulp of human exfoliated deciduous teeth. Stem Cells Dev 19:1081–1093PubMedCrossRefGoogle Scholar
  77. Plavina T, Wakshull E, Hancock WS, Hincapie M (2007) Combination of abundant protein depletion and multi-lectin affinity chromatography (M-LAC) for plasma protein biomarker discovery. J Proteome Res 6:662–671PubMedCrossRefGoogle Scholar
  78. Quinn CC, Gray GE, Hockfield S (1999) A family of proteins implicated in axon guidance and outgrowth. J Neurobiol 41:158–164PubMedCrossRefGoogle Scholar
  79. Rajesh RV, Heo GN, Park MR, Nam J, Kim N, Yoon D, Kim T, Lee H (2010) Proteomic analysis of bovine omental, subcutaneous and intramuscular preadipocytes during in vitro adipogenic differentiation. Comp Biochem Physiol Part D 5:234–244Google Scholar
  80. Rane MJ, Pan Y, Singh S, Powell DW, Wu R, Cummins T, Chen O, McLeish KR, Klein JB (2003) Heat shock protein 27 controls apoptosis by regulating Akt activation. J Biol Chem 278:27828–27835PubMedCrossRefGoogle Scholar
  81. Reichenberg E, Redlich M, Cancemi P, Zaks B, Fontana S, Pucci-Minafra I, Palmon A (2005) Proteomic analysis of protein components in periodontal ligament fibroblasts. J Periodontol 76:1645–1653PubMedCrossRefGoogle Scholar
  82. Roche S, Delorme B, Oostendorp RA, Barbet R, Caton D, Noel D, Boumediene K, Papadaki HA, Cousin B, Crozet C, Milhavet O, Casteilla L, Hatzfeld J, Jorgensen C, Charbord P, Lehmann S (2009) Comparative proteomic analysis of human mesenchymal and embryonic stem cells: towards the definition of a mesenchymal stem cell proteomic signature. Proteomics 9:223–232PubMedCrossRefGoogle Scholar
  83. Roubelakis MG, Pappa KI, Bitsika V, Zagoura D, Vlahou A, Papadaki HA, Antsaklis A, Anagnou NP (2007) Molecular and proteomic characterization of human mesenchymal stem cells derived from amniotic fluid: comparison to bone marrow mesenchymal stem cells. Stem Cells Dev 16:931–952PubMedCrossRefGoogle Scholar
  84. Sakaguchi Y, Sekiya I, Yagishita K, Muneta T (2005) Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum 52:2521–2529PubMedCrossRefGoogle Scholar
  85. Salasznyk RM, Westcott AM, Klees RF, Ward DF, Xiang Z, Vandenberg S, Bennett K, Plopper GE (2005) Comparing the protein expression profiles of human mesenchymal stem cells and human osteoblasts using gene ontologies. Stem Cells Dev 14:354–366PubMedCrossRefGoogle Scholar
  86. Scadden DT (2006) The stem-cell niche as an entity of action. Nature 441:1075–1079PubMedCrossRefGoogle Scholar
  87. Seo BM, Miura M, Gronthos S, Bartold PM, Batouli S, Brahim J, Young M, Robey P, Wang C, Shi S (2004) Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 364:149–155PubMedCrossRefGoogle Scholar
  88. Shan YX, Yang TL, Mestril R, Wang PH (2003) Hsp10 and Hsp60 suppress ubiquitination of insulin-like growth factor-1 receptor and augment insulin-like growth factor-1 receptor signaling in cardiac muscle: implications on decreased myocardial protection in diabetic cardiomyopathy. J Biol Chem 278:45492–45498PubMedCrossRefGoogle Scholar
  89. Shi S, Gronthos S (2003) Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 18:696–704PubMedCrossRefGoogle Scholar
  90. Shi S, Gronthos S, Chen S, Reddi A, Counter CM, Robey PG, Wang CY (2002) Bone formation by human postnatal bone marrow stromal stem cells is enhanced by telomerase expression. Nat Biotechnol 20:587–591PubMedCrossRefGoogle Scholar
  91. Simonsen JL, Rosada C, Serakinci N, Justesen J, Stenderup K, Rattan SI, Jensen TG, Kassem M (2002) Telomerase expression extends the proliferative life-span and maintains the osteogenic potential of human bone marrow stromal cells. Nat Biotechnol 20:592–596PubMedCrossRefGoogle Scholar
  92. Skalnikova H, Motlik J, Gadher SJ, Kovarova H (2011) Mapping of the secretome of primary isolates of mammalian cells, stem cells and derived cell lines. Proteomics 11:691–708PubMedCrossRefGoogle Scholar
  93. Sonoyama W, Liu Y, Fang D, Yamaza T, Seo BM, Zhang C, Liu H, Gronthos S, Wang CY, Wang S, Shi S (2006) Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS One 1:e79PubMedCrossRefGoogle Scholar
  94. 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 24:2059–2071PubMedCrossRefGoogle Scholar
  95. Thesleff I, Aberg T (1999) Molecular regulation of tooth development. Bone 25:123–125PubMedCrossRefGoogle Scholar
  96. Thingholm TE, Jensen ON, Larsen MR (2009) Enrichment and separation of mono- and multiply phosphorylated peptides using sequential elution from IMAC prior to mass spectrometric analysis. Methods Mol Biol 527:67–78, xiPubMedGoogle Scholar
  97. Tokunaga A, Oya T, Ishii Y, Motomura H, Nakamura H, Ishizawa S, Fujimori T, Nabeshima Y, Umezawa A, Kanamori M, Kimura T, Sasahara M (2008) PDGF receptor beta is a potent regulator of mesenchymal stromal cell function. J Bone Miner Res 23:1519–1528PubMedCrossRefGoogle Scholar
  98. Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD (2002) Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 105:93–98PubMedCrossRefGoogle Scholar
  99. Trimpin S, Brizzard B (2009) Analysis of insoluble proteins. Biotechniques 46:409–419PubMedCrossRefGoogle Scholar
  100. Troyer DL, Weiss ML (2008) Wharton’s jelly-derived cells are a primitive stromal cell population. Stem Cells 26:591–599PubMedCrossRefGoogle Scholar
  101. Unwin RD, Gaskell SJ, Evans CA, Whetton AD (2003) The potential for proteomic definition of stem cell populations. Exp Hematol 31:1147–1159PubMedCrossRefGoogle Scholar
  102. Urbas L, Brne P, Gabor B, Barut M, Strlic M, Petric TC, Strancar A (2009) Depletion of high-abundance proteins from human plasma using a combination of an affinity and pseudo-affinity column. J Chromatogr A 1216:2689–2694PubMedCrossRefGoogle Scholar
  103. Wada N, Menicanin D, Shi S, Bartold PM, Gronthos S (2009) Immunomodulatory properties of human periodontal ligament stem cells. J Cell Physiol 219:667–676PubMedCrossRefGoogle Scholar
  104. Wang D, Park JS, Chu JS, Krakowski A, Luo K, Chen DJ, Li S (2004a) Proteomic profiling of bone marrow mesenchymal stem cells upon transforming growth factor beta1 stimulation. J Biol Chem 279:43725–43734PubMedCrossRefGoogle Scholar
  105. Wang HS, Hung SC, Peng ST, Huang CC, Wei HM, Guo YJ, Fu YS, Lai MC, Chen CC (2004b) Mesenchymal stem cells in the Wharton’s jelly of the human umbilical cord. Stem Cells 22:1330–1337PubMedCrossRefGoogle Scholar
  106. Wang P, Bouwman FG, Mariman EC (2009) Generally detected proteins in comparative proteomics–a matter of cellular stress response? Proteomics 9:2955–2966PubMedCrossRefGoogle Scholar
  107. Wei X, Wu L, Ling J, Liu L, Liu S, Liu W, Li M, Xiao Y (2008) Differentially expressed protein profile of human dental pulp cells in the early process of odontoblast-like differentiation in vitro. J Endod 34:1077–1084PubMedCrossRefGoogle Scholar
  108. Wiese S, Reidegeld KA, Meyer HE, Warscheid B (2007) Protein labeling by iTRAQ: a new tool for quantitative mass spectrometry in proteome research. Proteomics 7:340–350PubMedCrossRefGoogle Scholar
  109. Wu L, Wei X, Ling J, Liu L, Liu S, Li M, Xiao Y (2009) Early osteogenic differential protein profile detected by proteomic analysis in human periodontal ligament cells. J Periodontal Res 44:645–656PubMedCrossRefGoogle Scholar
  110. Yang SE, Ha CW, Jung M, Jin HJ, Lee M, Song H, Choi S, Oh W, Yang YS (2004) Mesenchymal stem/progenitor cells developed in cultures from UC blood. Cytotherapy 6:476–486PubMedCrossRefGoogle Scholar
  111. Ye NS, Zhang RL, Zhao YF, Feng X, Wang YM, Luo GA (2006a) Effect of 5-azacytidine on the protein expression of porcine bone marrow mesenchymal stem cells in vitro. Genomics Proteomics Bioinformatics 4:18–25PubMedCrossRefGoogle Scholar
  112. Ye NS, Chen J, Luo GA, Zhang RL, Zhao YF, Wang YM (2006b) Proteomic profiling of rat bone marrow mesenchymal stem cells induced by 5-azacytidine. Stem Cells Dev 15:665–676PubMedCrossRefGoogle Scholar
  113. Zannettino AC, Paton S, Arthur A, Khor F, Itescu S, Gimble JM, Gronthos S (2008) Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 214:413–421PubMedCrossRefGoogle Scholar
  114. Zhang AX, Yu WH, Ma BF, Yu X, Mao FF, Liu W, Zhang J, Zhang X, Li S, Li M, Lahn BT, Xiang AP (2007) Proteomic identification of differently expressed proteins responsible for osteoblast differentiation from human mesenchymal stem cells. Mol Cell Biochem 304:167–179PubMedCrossRefGoogle Scholar
  115. Zhang Q, Shi S, Liu Y, Uyanne J, Shi Y, Le AD (2009) Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. J Immunol 183:7787–7798PubMedCrossRefGoogle Scholar
  116. Zhao L, Jiang S, Hantash BM (2010) Transforming growth factor beta1 induces osteogenic differentiation of murine bone marrow stromal cells. Tissue Eng Part A 16:725–733PubMedCrossRefGoogle Scholar
  117. Zhuang H, Wang W, Tahernia AD, Levitz CL, Luchetti WT, Brighton CT (1996) Mechanical strain-induced proliferation of osteoblastic cells parallels increased TGF-beta 1 mRNA. Biochem Biophys Res Commun 229:449–453PubMedCrossRefGoogle Scholar
  118. Zolotarjova N, Mrozinski P, Chen H, Martosella J (2008) Combination of affinity depletion of abundant proteins and reversed-phase fractionation in proteomic analysis of human plasma/serum. J Chromatogr A 1189:332–338PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Krzysztof M. Mrozik
    • 1
  • Jimin Xiong
    • 1
  • Peter S. Zilm
    • 1
  • Stan Gronthos
    • 2
  • P. Mark Bartold
    • 1
  1. 1.Colgate Australian Clinical Dental Research Centre, Dental SchoolThe University of AdelaideAdelaideAustralia
  2. 2.Mesenchymal Stem Cell Group, Department of Haematology/Centre for Stem Cell ResearchRobinson Institute, Discipline of Medicine, SA Pathology/The University of AdelaideAdelaideAustralia

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