Human mesenchymal stem cells in contact with their environment: Surface characteristics and the integrin system

Journal of Cellular and Molecular Medicine

Volumn 11, Issue 1, 2007, Pages 21-38

  Docheva, Denitsa ^a   Popov, Cvetan ^a   Mutschler, Wolf ^a   Schieker, Matthias ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

Differentiation; Focal adhesions; Integrins; Mesenchymal stem cells; Tissue engineering; Tumorigenesis

Indexed keywords

INTEGRIN;

ARTICLE; BIOLOGICAL MODEL; CELL ADHESION; CELL DIFFERENTIATION; CELL LINEAGE; CYTOLOGY; ENVIRONMENT; HUMAN; MESENCHYMAL STEM CELL; METHODOLOGY; PHYSIOLOGY; TISSUE ENGINEERING;

CELL ADHESION; CELL DIFFERENTIATION; CELL LINEAGE; ENVIRONMENT; HUMANS; INTEGRINS; MESENCHYMAL STEM CELLS; MODELS, BIOLOGICAL; TISSUE ENGINEERING;

EID: 33947312170     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2007.00001.x     Document Type: Article

References (101)

1. Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, Deans RJ, Krause DS, Keating A. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy. 2005; 7:393-5.
2. Friedenstein AJ. Osteogenetic activity of transplanted transitional epithelium. Acta Anat (Basel). 1961; 45:31-59.
3. Baksh D, Song L, Tuan RS. Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy. J Cell Mol Med. 2004; 8:301-16.
4. Robey PG, Bianco P. The use of adult stem cells in rebuilding the human face. J Am Dent Assoc. 2006; 137:961-72.
5. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006; 8:315-7.
6. Verfaillie CM. Adult stem cells: assessing the case for pluripotency. Trends Cell Biol. 2002; 12:502-8.
7. Phinney DG, Kopen G, Isaacson RL, Prockop DJ. Plastic adherent stromal cells from the bone marrow of commonly used strains of inbred mice: variations in yield, growth, and differentiation. J Cell Biochem. 1999; 72: 570-85.
8. Bianco P, Riminucci M, Gronthos S, Robey PG. Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells. 2001; 19:180-92.
9. Lakshmipathy U, Verfaillie C. Stem cell plasticity. Blood Rev. 2005; 19:29-38.
10. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature. 2002; 418:41-9.
11. Tuan RS, Boland G, Tuli R. Adult mesenchymal stem cells and cell-based tissue engineering. Arthritis Res Ther. 2003; 5:32-45.
12. Noth U, Osyczka AM, Tuli R, Hickok NJ, Danielson KG, Tuan RS. Multilineage mesenchymal differentiation potential of human trabecular bone-derived cells. J Orthop Res. 2002; 20:1060-9.
13. Romanov YA, Svintsitskaya VA, Smirnov VN. Searching for alternative sources of postnatal human mesenchymal stem cells: candidate MSC-like cells from umbilical cord. Stem Cells. 2003; 21:105-10.
14. Sabatini F, Petecchia L, Tavian M, Jodon dV, V, Rossi GA, Brouty-Boye D. Human bronchial fibroblasts lasts exhibit a mesenchymal stem cell phenotype and muitilineage differentiating potentialities. Lab Invest. 2005; 85: 962-71.
15. Shi S, Bartold PM, Miura M, Seo BM, Robey PG, Gronthos S. The efficacy of mesenchymal stem cells to regenerate and repair dental structures. Orthod Craniofac Res. 2005; 8:191-9.
16. Kern S, Eichler H, Stoeve J, Kluter H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells. 2006; 24:1294-301.
17. Minguell JJ, Ericas A, Conget P. Mesenchymal stem cells. Exp Biol Med. 2001 ; 226:507-20.
18. Roufbsse CA, Direkze NC, Otto WR, Wright NA. Circulating mesenchymal stem cells. Int J Biochem Cell Biol. 2004; 36:585-97.
19. He Q, Wan C, Li G. Multi-potent mesenchymal stromal cells in blood. Stem Cafe 2006; Sep 14: [Epub ahead of print].
20. Piersma AH, Ploemacher RE, Brockbank KG. Transplantation of bone marrow fibroblastoid stromal cells in mice via the intravenous route. Br J Haematol. 1983;54:285-90.
21. Kuznetsov SA, Mankani MH, Gronthos S, Satomura K, Bianco P, Robey PG. Circulating skeletal stem cells. J Cell Biol. 2001 ; 153:1133-40.
22. Lazarus HM, Haynesworth SE, Gerson SL, Caplan AI. Human bone marrow-derived mesenchymal (stromal) progenitor cells (MFCs) cannot be recovered from peripheral blood progenitor cell collections. J Hematother. 1997; 6:447-55.
23. Wexler SA, Donaldson C, Denning-Kendall P, Rice C, Bradley B, Hows JM. Adult bone marrow is a rich source of human mesenchymal 'stem' cells but umbilical cord and mobilized adult blood are not. Br J Haematol. 2003; 121:368-74.
24. Kassem M, Kristiansen M, Abdallah BM. Mesenchymal stem cells: cell biology and potential use in therapy. Basic Clin Pharmacol Toxicol. 2004; 95:209-14.
25. Pereira RF, O'Hara MD, Laptev AV, Halford KW, Pollard MD, Class R, Simon D, Livezey K, Prockop DJ. Marrow stromal cells as a source of progenitor cells for nonhematopoietic tissues in transgenic mice with a phenotype of osteogenesis imperfecta. Proc Natl Acad Sci USA. 1998; 95:1142-7.
26. Horwitz EM, Gordon PL, Koo WK, Marx JC, Neel MD, McNall RY, Muul L, Hofmann T. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone. Proc Nati Acad Sci USA. 2002; 99:8932-7.
27. Clark BR, Keating A. Biology of bone marrow stroma. Ann N Y Acad Sci. 1995; 770: 70-8.
28. Barry FP, Murphy JM. Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol. 2004; 36:568-84.
29. Zipori D. Mesenchymal stem cells: harnessing cell plasticity to tissue and organ repair. Blood Cells Mol Dis. 2004; 33:211-5.
30. Grove JE, Bruscia E, Krause DS. Plasticity of bone marrow-derived stem cells. Stem Cells. 2004; 22: 487-500.
31. Van Damme A, Vanden Driessche T, Collen D, Chuah MK. Bone marrow stromal cells as targets for gene therapy. Curr Gene Ther. 2002; 2:195-209.
32. Houghton J, Stoicov C, Nomura S, Rogers AB, Carison J, Li H, Cai X, Fox JG, Goldenring JR, Wang TC. Gastric cancer originating from bone marrow-derived cells. Science. 2004; 306:1568-71.
33. Nakamizo A, Marini F, Amano T, Khan A, Studeny M, Gumin J, Chen J, Hentschel S, Vecil G, Dembinski J, Andreeff M, Lang FF. Human bone marrow-derived mesenchymal stem cells in the treatment of gliomas. Cancer Res. 2005; 65: 3307-18.
34. Burns JS, Abdallah BM, Guldberg P, Rygaard J, Schroder HD, Kassem M. Tumorigenic heterogeneity in cancer stem cells evolved from long-term cultures of telomerase-immortalized human mesenchymal stem cells. Cancer Res. 2005; 65:3126-35.
35. Serakinci N, Guldberg P, Bums JS, Abdallah B, Schrodder H, Jensen T, Kassem M. Adult human mesenchymal stem cell as a target for neoplastic transformation. Oncogene. 2004; 23:5095-8.
36. Beachy PA, Karhadkar SS, Berman DM. Tissue repair and stem cell renewal in carcinogenesis. Nature. 2004;432:324-31.
37. Dittmar T, Seidel J, Zaenker KS, Niggemann B. Carcinogenesis driven by bone marrow-derived stem cells. Contrib Microbiol. 2006; 13:156-69.
38. Rubio D, Garcia-Castro J, Martin MC, de la FR, Cigudosa JC, Lloyd AC, Bemad A. Spontaneous human adult stem cell transformation. Cancer Res. 2005; 65: 3035-9.
39. Bianco P, Robey PG. Stem cells in tissue engineering. Nature. 2001;414:118-21.
40. Schieker M, Seitz H, Drosse I, Seitz S, Mutschler W. Biomaterials as scaffold for bone tissue engineering. Eur J Trauma. 2006; 32:114-24.
41. Kon E, Muraglia A, Corsi A, Bianco P, Marcacci M, Martin I, Boyde A, Ruspantini I, Chistolini P, Rocca M, Giardino R, Cancedda R, Quarto R. Autotogous bone marrow stromal cells loaded onto porous hydroxyapatite ceramic accelerate bone repair in critical-size defects of sheep tang bones. J Biomed Mater Res. 2000; 49:328-37.
42. Otto WR, Rao J. Tomorrow's skeleton staff: mesenchymal stem cells and the repair of bone and cartilage. Cell Prolif. 2004; 37:97-110.
43. Calderwood DA. Integrin activation. J Cell Sci. 2004; 117:657-66.
44. Reddy KV, Mangale SS. Integrin receptors: the dynamic modulators of endometrial function. Tissue Cell. 2003; 35:260-73.
45. Fisher LW.Torchia DA, Fohr B, Young MF, Fedarko NS. Flexible structures of SIBLING proteins, bone sialoprotein, and osteopontin. Biochem Biophys Res Commun. 2001; 280:460-5.
46. Ivaska J, Heino J. Adhesion receptors and cell invasion: mechanisms of integrin-guided degradation of extracellular matrix. Cell Mol Lite Sci. 2000; 57:16-24.
47. Brakebusch C, Fassler R. The integrin-actin connection, an eternal love affair. EMBOJ. 2003; 22:2324-33.
48. Zamir E, Geiger B. Molecular complexity and dynamics of cell-matrix adhesions. J Cell Sci. 2001 ; 114:3583-90.
49. Sakai T, Li S, Docheva D, Grashoff C, Sakai K, Kostka G, Braun A, Pfeifer A, Yurchenco PD, Fassler R. Integrin-linked kinase (ILK) is required for polarizing the epiblast, cell adhesion, and controlling actin accumulation. Genes Dev. 2003; 17:926-40.
50. Hall A. Rho GTPases and the actin cytoskeleton. Science. 1998; 279: 509-14.
51. Palecek SP, Loftus JC, Ginsberg MH, Lauffenburger DA, Horwitz AF. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature. 1997; 385:537-40.
52. Murphy-Ullrich JE. The de-adhesive activity of matricellular proteins: is intermediate cell adhesion an adaptive state? J Clin Invest. 2001; 107: 785-90.
53. Brakebusch C, Bouvard D, Stanchi F, Sakai T, Fassler R. Iniegrins in invasive growth. J Clin Invest. 2002;109:999-1006.
54. Danen EH, Sonnenberg A. Integrins in regulation of tissue development and function. J Pathol. 2003; 200: 471-80.
55. Vermeulen M, Le Pesteur F, Gagnerault MC, Mary JY, Sainteny F, Lepault F. Role of adhesion molecules in the homing and mobilization of murine hematopoietic stem and progenitor cells. Blood. 1998; 92:894-900.
56. Larsen M, Artym W, Green JA, Yamada KM. The matrix reorganized: extracellular matrix remodeing and integrin signaling. Curr Opin Cell Bid. 2006; 18:463-71.
57. De Arcangelis A, Georges-Labouesse E. Integrin and ECM functions: roles in vertebrate development. Trends Genet. 2000; 16:389-95.
58. Bouvard D, Brakebusch C, Gustafsson E, Aszodi A, Bengtsson T, Berna A, Fassler R. Functional consequences of integrin gene mutations in mice. Circ Res. 2001;89:211-23.
59. McHugh KP, Hodivala-Dilke K, Zheng MH, Namba N, Lam J, Novack D, Feng X, Ross FP, Hynes RO, TeJtelbaum SL, Mice lacking beta3 integrins are osteosclerotic because of dysfunctional osteoclasts. J Clin Invest 2000; 105:433-40.
60. Silletti S, Kessler T, Goldberg J, Boger DL, Cheresh DA. Disruption of matrix metalloproteinase 2 binding to integrin alpha vbeta 3 by an organic molecule inhibits angiogenesis and tumor growth in vivo. Proc Natl Acad Sci USA. 2001; 98:119-24.
61. Hood JD, Cheresh DA. Role of integrins in cell invasion and migration. Nat Rev Cancer. 2002; 2:91-100.
62. Guo W, Giancotti FG. Integrin signalling during tumour progression. Nat Rev Mol Cell Biol. 2004; 5: 816-26.
63. Wiesner S, Legate KR, Fassler R. Integrin-actin interactions. Cell Mol Life Sci. 2005; 62:1081-99.
64. Wozniak MA, Modzelewska K, Kwong L, Keely PJ. Focal adhesion regulation of cell behavior. Biochim Biophys Acta. 2004; 1692:103-19.
65. Cukierman E, Pankov R, Stevens DR, Yamada KM. Taking cell-matrix adhesions to the third dimension. Science. 2001; 294:1708-12.
66. Honczarenko M, Le Y, Swierkowski M, Ghiran I, Glodek AM, Silberstein LE. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem Cells. 2006; 24: 1030-41.
67. Honczarenko M, Glodek AM, Swierkowski M, Na IK, Silberstein LE. Developmental stage-specific shift in responsiveness to chemokines during human B-cell development. Exp Hematol. 2006; 34:1093-100.
68. Overstraeten-Schlogel N, Beguin Y, Gothot A. Role of stromal-derived factor-1 in the hematopoietic-supporting activity of human mesenchymal stem cells. Eur J Haematol. 2006; 76:488-93.
69. Son BR, Marquez-Curtis LA, Kucia M, Wysoczynski M, Turner AR, Ratajczak J, Ratajczak MZ, Janowska-Wieczorek A. Migration of bone marrow and cord blood mesenchymal stem cells in vitro is regulated by stromal-derived factor-1-CXCR4 and hepatocyte growth factor-c-met axes and involves matrix metalloproteinases. Stem Cells. 2006; 24:1254-64.
70. Kucia M, Reca R, Miekus K, Wanzeck J, Wojakowski W, Janowska-Wieczorek A, Ratajczak J, Ratajczak MZ. Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: pivotal role of the SDF-1-CXCR4 axis. Stem Cells. 2005; 23: 879-94.
71. Majumdar MK, Keane-Moore M, Buyaner D, Hardy WB, Moorman MA, McIntosh KR, Mosca JD. Characterization and functionality of cell surface molecules on human mesenchymal stem cells. J Biomed Sei. 2003;10:228-41.
72. Schieker M, Pautke C, Reitz K, Hemraj I, Neth P, Mutschler W, Milz S. The use of four-colour immunofluorescence techniques to identify mesenchymal stem cells. J Mat. 2004; 204:133-9.
73. Lisignoli G, Cristino S, Piacentini A, Cavallo C, Caplan AI, Facchini A. Hyaluronan-based polymer scaffold modulates the expression of inflammatory and degradative factors in mesenchymal stem cells: involvement of Cd44 and Cd54. J Cell Physiol. 2006; 207:364-73.
74. Zhu H, Mitsuhashi N, Klein A, Barsky LW, Weinberg K, Barr ML, Demetriou A, Wu GD. The role of the hyaluronan receptor CD44 in mesenchymal stem cell migration in the extracellular matrix. Stem Cells. 2006; 24: 928-35.
75. Asian H, Zilberman Y, Kandel L, Liebergall M, Oskouian RJ, Gazit D, Gazit Z. Osteogenic differentiation of noncultured immunoisolated bone marrow-derived CD105+ cells. Stem Cells. 2006; 24: 1728-37.
76. Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U, Blake J, Schwager C, Eckstein V, Ansorge W, Ho AD. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol. 2005; 33:1402-16.
77. Gronthos S, Simmons PJ, Graves SE, Robey PG. Integrin-mediated interactions between human bone marrow stromal precursor cells and the extracellular matrix. Bone. 2001; 28:174-81.
78. Foster LJ, Zeemann PA, Li C, Mann M, Jensen ON, Kassem M. Differential expression profiling of membrane proteins by quantitative proteomics in a human mesenchymal stem cell line undergoing osteoblast differentiation. Stem Cells. 2005; 23:1367-77.
79. Walsh S, Jordan GR, Jefferiss C, Stewart K, Beresford JN. High concentrations of dexarnethasone suppress the proliferation but not the differentiation or further maturation of human osteoblast precursors in vitro: relevance to glucocorticoid-induced osteoporosis. Rheumatology. 2001; 40:74-83.
80. Meyers VE, Zayzafbon M, Gonda SR, Gathings WE, McDonald JM. Modeled microgravity disrupts collagen l/integrin signaling during osteoblastic differentiation of human mesenchymal stem cells. J Cell Biochem. 2004; 93: 697-707.
81. Klees RF, Salasznyk RM, Kingsley K, Williams WA, Boskey A, Plopper GE. Laminin-5 induces osteogenic gene expression in human mesenchymal stem cells through an ERK-dependent pathway. Mol Biol Cell. 2005; 16:881-90.
82. Salasznyk RM, Klees RF, Boskey A, Plopper GE. Activation of FAK is necessary for the osteogenic differentiation of human mesenchymal stem cells on laminin5. J Cell Biochem. 2006; Aug 22: [Epub ahead of print].
83. Karadag A, Fisher LW. Bone sialoprotein enhances migration of bone marrow stromal cells through matrices by bridging MMP-2 to alpha(v)beta3- integrin. J Bone Miner Res. 2006; 21:1627-36.
84. Tuli R, Li WJ, Tuan RS. Current state of cartilage tissue engineering. Arthritis Res Ther. 2003; 5:235-8.
85. Goessler UR, Bieback K, Bugert P, HellerT, Sadick H, Hormann K, Riedel F. In vitro analysis of integrin expression during chondrogenic differentiation of mesenchymal stem cells and chondrocytes upon dedifferentiation in cell culture. Int J Mol Med. 2006; 17:301-7.
86. Pautke C, Schieker M, Tischer T, Kolk A, Neth P, Mutschler W, Milz S. Characterization of osteosarcoma cell lines MG-63, Saos-2 and U-2 OS in comparison to human osteoblasts. Anticancer Res, 2004; 24:3743-8.
87. Siebers MC, ter Brugge PJ, Walboomers XF, Jansen JA. Integrins as linker proteins between osteoblasts and bone replacing materials. A critical review. Biomaterials. 2005; 26:137-46.
88. Lange R, Luthen F, Beck U, Rychly J, Baumann A, Nebe B. Cell-extracellular matrix interaction and physico-chemical characteristics of titanium surfaces depend on the roughness of the material. Biomol Eng. 2002;19:255-61.
89. Webster TJ, Ergun C, Doremus RH, Siegel RW, Bizios R. Specific proteins mediate enhanced osteoblast adhesion on nanophase ceramics. J Biomed Mater Res. 2000; 51:475-83.
90. Heckmann L, Fiedler J, Mattes T, Brenner RE. Mesenchymal progenitor cells communicate via alpha and beta integrins with a three-dimensional collagen type I matrix. Cells Tissues Organs. 2006; 182:143-54.
91. Chang CF, Lee MW, Kuo PY, Wang YJ, Tu YH, Hung SC. Three-dimensional collagen fiber remodeling by mesenchymal stem cells requires the integrin-matrix interaction. J Biomed Mater Res A. 2006; Sep 29: [Epub ahead of print].
92. Grayson WL, Ma T, Bunnell B. Human mesenchymal stem cells tissue development in 3D PET matrices. Biotechnol Prog. 2004; 20:905-12.
93. Chastain SR, Kundu AK, Dhar S, Calvert JW, Putnam AJ. Adhesion of mesenchymal stem cells to polymer scaffolds occurs via distinct ECM ligands and controls their osteogenic differentiation. J Biomed Mater Res A. 2006; 78: 73-85.
94. Lee JW, Kim YH, Park KD, Jee KS, Shin JW, Hahn SB. Importance of integrin betal-mediated cell adhesion on biodegradable polymers under serum depletion in mesenchymal stem cells and chondrocytes. Biomaterials. 2004; 25:1901-9.
95. Van der Velde-Zimmermann D, Smits AJ, Verdaasdonk MA, Rademakers LH, Werner N, Spierings DC, De Weger R A, Van denTweel JG, Joling P. betal-Integrins dominate cell traffic of leukemic cells in human bone-marrow stroma. Int J Cancer. 1996; 66:225-33.
96. Van der Velde-Zimmermann D, Verdaasdonk MA, Rademakers LH, De Weger RA, Van den Tweel JG, Joling P. Rbronectin distribution in human bone marrow stroma: matrix assembly and tumor cell adhesion via alpha5 betal integrin. Exp Cell Res. 1997; 230:111-20.
97. Lang SH, Clarke NW, George NJ, Testa NG. Primary prostatic epithelial cell binding to human bone marrow stroma and the role of alpha2beta1 integrin. Clin Exp Metastasis. 1997; 15:218-27.
98. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell. 2002; 110:673-87.
99. Majumdar MK, Banks V, Peluso DP, Morris EA. Isolation, characterization, and chondrogenic potential of human bone marrow-derived multipotential stromal cells. J Cell Physiol. 2000; 185:98-106.
100. Neuss S, Becher E, Woltje M, Tietze L, Jahnen-Dechent W. Functional expression of HGF and HGF receptor/c-met in adult human mesenchymal stem cells suggests a role in cell mobilization, tissue repair, and wound healing. Stem Cells. 2004; 22:405-14.
101. Reyes M, Dudek A, Jahagirdar B, Koodie L, Marker PH, Verfaillie CM. Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest. 2002; 109:337-46.