Clonal analysis of the proliferation potential of human bone marrow mesenchymal stem cells as a function of potency

Biotechnology and Bioengineering

Volumn 108, Issue 11, 2011, Pages 2716-2726

  Russell, Katie C ^a,b   Lacey, Michelle R ^a   Gilliam, Jennifer K ^a   Tucker, H Alan ^b   Phinney, Donald G ^c   O'Connor, Kim C ^a,b  

^a Tulane University   (United States)

^b TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Apoptosis; Mesenchymal stem cells; Osteogenesis; Potency; Proliferation; Senescence

Indexed keywords

MESENCHYMAL STEM CELL; OSTEOGENESIS; POTENCY; PROLIFERATION; SENESCENCE;

ANIMAL CELL CULTURE; BONE; CELL DEATH; EXPANSION; FLOWCHARTING; STEM CELLS;

CLONE CELLS;

ADIPOGENESIS; APOPTOSIS; ARTICLE; BONE DEVELOPMENT; CELL CLONE; CELL CULTURE; CELL FUNCTION; CELL LINEAGE; CELL PROLIFERATION; CHONDROGENESIS; COLONY FORMING CELL; EXTRACELLULAR MATRIX; GROWTH RATE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MINERALIZATION;

ADIPOGENESIS; APOPTOSIS; BONE MARROW; CELL PROLIFERATION; CELL SURVIVAL; CHONDROGENESIS; HUMANS; MESENCHYMAL STEM CELLS; OSTEOGENESIS;

EID: 80053054005     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.23193     Document Type: Article

References (45)

1. Bajada S, Marshall MJ, Wright KT, Richardson JB, Johnson WE. 2009. Decreased osteogenesis, increased cell senescence and elevated Dickkopf-1 secretion in human fracture non-union stromal cells. Bone 45: 726-735.
2. Banfi A, Muraglia A, Dozin B, Mastrogiacomo M, Cancedda R, Quarto R. 2000. Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: Implications for their use in cell therapy. Exp Hematol 28: 707-715.
3. Barbosa I, Garcia S, Barbier-Chassefière V, Caruelle J, Martelly I, Papy-García D. 2003. Improved and simple micro assay for sulfated glycosaminoglycans quantification in biological extracts and its use in skin and muscle tissue studies. Glycobiology 13: 647-653.
4. Barrilleaux BL, Phinney DG, Prockop DJ, O'Connor KC. 2006. Review: Ex vivo engineering of living tissues with adult stem cells. Tissue Eng 12: 3007-3019.
5. Barrilleaux BL, Phinney DG, Fischer-Valuck BW, Russell KC, Wang G, Prockop DJ, O'Connor KC. 2009. Small-molecule antagonist of macrophage migration inhibitory factor enhances migratory response of mesenchymal stem cells to bronchial epithelial cells. Tissue Eng A 15: 2335-2346.
6. Battula VL, Treml S, Bareiss PM, Gieseke F, Roelofs H, de Zwart P, Müller I, Schewe B, Skutella T, Fibbe WE, Kanz L, Bühring HJ. 2009. Isolation of functionally distinct mesenchymal stem cell subsets using antibodies against CD56, CD271, and mesenchymal stem cell antigen-1. Haematologica 94: 173-184.
7. Bianco P, Riminucci M, Gronthos S, Robey PG. 2001. Bone marrow stromal stem cells: Nature, biology, and potential applications. Stem Cells 19: 180-192.
8. Blanch HW, Clark DS. 1997. Biochemical engineering. New York: Marcel Dekker, p. 702.
9. Bruder SP, Jaiswal N, Haynesworth SE. 1997. Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J Cell Biochem 64: 278-294.
10. Caplan AI, Dennis JE. 2006. Mesenchymal stem cells as trophic mediators. J Cell Biochem 98: 1076-1084.
11. 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. Proc Natl Acad Sci USA 98: 7841-7845.
12. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, Norotte C, Teng PN, Traas J, Schugar R, Deasy BM, Badylak S, Buhring HJ, Giacobino JP, Lazzari L, Huard J, Péault B. 2008. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3: 301-313.
13. DiGirolamo CM, Stokes D, Colter D, Phinney DG, Class R, Prockop DJ. 1999. Propagation and senescence of human marrow stromal cells in culture: A simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate. Br J Haematol 107: 275-281.
14. D'Ippolito G, Diabira S, Howard GA, Menei P, Roos BA, Schiller PC. 2004. Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J Cell Sci 117: 2971-2981.
15. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini FC, Krause DS, Deans RJ, Keating A, Prockop DJ, Horwitz EM. 2006. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8: 315-317.
16. Fischer-Valuck BW, Barrilleaux BL, Phinney DG, Russell KC, Prockop DJ, O'Connor KC. 2010. Migratory response of mesenchymal stem cells to macrophage migration inhibitory factor and its antagonist as a function of colony-forming efficiency. Biotechnol Lett 32: 19-27.
17. Friedenstein AJ, Deriglasova UF, Kulagina NN, Panasuk AF, Rudakowa SF, Luria EA, Ruadkow IA. 1974. Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol 2: 83-92.
18. 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: 1827-1835.
19. Hachisuka H, Mochizuki Y, Yasunaga Y, Natsu K, Sharman P, Shinomiya R, Ochi M. 2007. Flow cytometric discrimination of mesenchymal progenitor cells from bone marrow-adherent cell populations using CD34/44/45(-) and Sca-1(+) markers. J Orthop Sci 12: 161-169.
20. 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.
21. Karystinou A, Dell'Accio F, Kurth TB, Wackerhage H, Khan IM, Archer CW, Jones EA, Mitsiadis TA, De Bari C. 2009. Distinct mesenchymal progenitor cell subsets in the adult human synovium. Rheumatology 48: 1057-1064.
22. Kretlow JD, Jin YQ, Liu W, Zhang WJ, Hong TH, Zhou G, Baggett LS, Mikos AG, Cao Y. 2008. Donor age and cell passage affects differentiation potential of murine bone marrow-derived stem cells. BMC Cell Biol 9: 60.
23. Lee CC, Christensen JE, Yoder MC, Tarantal AF. 2010. Clonal analysis and hierarchy of human bone marrow mesenchymal stem and progenitor cells. Exp Hematol 38: 46-54.
24. Lee RH, Hsu SC, Munoz J, Jung JS, Lee NR, Pochampally R, Prockop DJ. 2006. A subset of human rapidly self-renewing marrow stromal cells preferentially engraft in mice. Blood 107: 2153-2161.
25. Mareddy S, Crawford R, Brooke G, Xiao Y. 2007. Clonal isolation and characterization of bone marrow stromal cells from patients with osteoarthritis. Tissue Eng 13: 819-829.
26. Mets T, Verdonk G. 1981. In vitro aging of human bone marrow derived stromal cells. Mech Ageing Dev 16: 81-89.
27. Muraglia A, Cancedda R, Quarto R. 2000. Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci 113: 1161-1166.
28. Neuhuber B, Swanger SA, Howard L, Mackay A, Fischer I. 2008. Effects of plating density and culture time on bone marrow stromal cell characteristics. Exp Hematol 36: 1176-1185.
29. Ortiz LA, Gambelli F, McBride C, Gaupp D, Baddoo M, Kaminski N, Phinney DG. 2003. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci USA 100: 8407-8411.
30. Penick KJ, Solchaga LA, Welter JF. 2005. High-throughput aggregate culture system to assess the chondrogenic potential of mesenchymal stem cells. Biotechniques 39: 687-691.
31. Prockop DJ. 1997. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276: 71-74.
32. Ringdén O, Uzunel M, Rasmusson I, Remberger M, Sundberg B, Lönnies H, Marschall HU, Dlugosz A, Szakos A, Hassan Z, Omazic B, Aschan J, Barkholt L, Le Blanc K. 2006. Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation 81: 1390-1397.
33. Russell KC, Phinney DG, Lacey MR, Barrilleaux BL, Meyertholen KE, O'Connor KC. 2010. In vitro high-capacity assay to quantify the clonal heterogeneity in trilineage potential of mesenchymal stem cells reveals a complex hierarchy of lineage commitment. Stem Cells 28: 788-798.
34. Saldaña L, Sánchez-Salcedo S, Izquierdo-Barba I, Bensiamar F, Munuera L, Vallet-Regí M, Vilaboa N. 2009. Calcium phosphate-based particles influence osteogenic maturation of human mesenchymal stem cells. Acta Biomater 5: 1294-1305.
35. Salem HK, Thiemermann C. 2010. Mesenchymal stromal cells: Current understanding and clinical status. Stem Cells 28: 585-596.
36. Sekiya I, Larson BL, Smith JR, Pochampally R, Cui J, Prockop DJ. 2002. Expansion of human adult stem cells from bone marrow stroma: Conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells 20: 530-541.
37. Severino J, Allen RG, Balin S, Balin A, Cristofalo VJ. 2000. Is beta-galactosidase staining a marker of senescence in vitro and in vivo? Exp Cell Res 257: 162-171.
38. Smith JR, Pochampally R, Perry A, Hsu SC, Prockop DJ. 2004. Isolation of a highly clonogenic and multipotential subfraction of adult stem cells from bone marrow stroma. Stem Cells 22: 823-831.
39. Song H, David O, Clejan S, Giordano CL, Pappas-LeBeau H, Xu L, O'Connor KC. 2004. Spatial composition of prostate cancer spheroids in mixed and static cultures. Tissue Eng 10: 1266-1276.
40. Sotiropoulou PA, Perez SA, Salagianni M, Baxevanis CN, Papamichail M. 2006. Characterization of the optimal culture conditions for clinical scale production of human mesenchymal stem cells. Stem Cells 24: 462-471.
41. Tormin A, Brune JC, Olsson E, Valcich J, Neuman U, Olofsson T, Jacobsen SE, Scheding S. 2009. Characterization of bone marrow-derived mesenchymal stromal cells (MSC) based on gene expression profiling of functionally defined MSC subsets. Cytotherapy 11: 114-128.
42. Veyrat-Masson R, Boiret-Dupré N, Rapatel C, Descamps S, Guillouard L, Guérin JJ, Pigeon P, Boisgard S, Chassagne J, Berger MG. 2007. Mesenchymal content of fresh bone marrow: A proposed quality control method for cell therapy. Br J Haematol 139: 312-320.
43. Wagner W, Bork S, Horn P, Krunic D, Walenda T, Diehlmann A, Benes V, Blake J, Huber FX, Eckstein V, Boukamp P, Ho AD. 2009. Aging and replicative senescence have related effects on human stem and progenitor cells. PLoS One 4: e5846.
44. Zhang S, Ge J, Sun A, Xu D, Qian J, Lin J, Zhao Y, Hu H, Li Y, Wang K, Zou Y. 2006. Comparison of various kinds of bone marrow stem cells for the repair of infarcted myocardium: Single clonally purified non-hematopoietic mesenchymal stem cells serve as a superior source. J Cell Biochem 99: 1132-1147.
45. Zhou S, Greenberger JS, Epperly MW, Goff JP, Adler C, Leboff MS, Glowacki J. 2008. Age-related intrinsic changes in human bone-marrow-derived mesenchymal stem cells and their differentiation to osteoblasts. Aging Cell 7: 335-343.