Isolation and Characterization of Human Mesenchymal Stromal Cell Subpopulations: Comparison of Bone Marrow and Adipose Tissue

Stem Cells and Development

Volumn 24, Issue 18, 2015, Pages 2142-2157

  Busser, Hélène ^a   Najar, Mehdi ^a   Raicevic, Gordana ^a   Pieters, Karlien ^a   Velez Pombo, Rafael ^b   Philippart, Pierre ^b   Meuleman, Nathalie ^a   Bron, Dominique ^a   Lagneaux, Laurence ^a  

^a JULES BORDET INSTITUTE   (Belgium)

^b IRIS   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CD271 ANTIGEN; CD34 ANTIGEN; CELL SURFACE MARKER; HERMES ANTIGEN; MEMBRANE PROTEIN; MSCA 1 PROTEIN; SUSD2 PROTEIN; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; MEMBRANE ANTIGEN; NERVE GROWTH FACTOR RECEPTOR; NERVE PROTEIN; NGFR PROTEIN, HUMAN; SUSD2 PROTEIN, HUMAN; W8B2 PROTEIN, HUMAN;

ABDOMINOPLASTY; ADIPOSE TISSUE; ARTICLE; BONE MARROW; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL GROWTH; CELL ISOLATION; CELL PROLIFERATION; CELL SUBPOPULATION; CLONOGENESIS; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOREGULATION; MESENCHYMAL STROMA CELL; PHENOTYPE; PRIMARY CULTURE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; ADIPOCYTE; ADOLESCENT; BONE MARROW CELL; COMPARATIVE STUDY; CYTOLOGY; FEMALE; FLOW CYTOMETRY; MALE; METABOLISM; PHYSIOLOGY; PROCEDURES;

ADIPOCYTES; ADIPOSE TISSUE; ADOLESCENT; ANTIGENS, SURFACE; BIOMARKERS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL PROLIFERATION; FEMALE; FLOW CYTOMETRY; HUMANS; MALE; MEMBRANE GLYCOPROTEINS; MESENCHYMAL STROMAL CELLS; NERVE TISSUE PROTEINS; PHENOTYPE; RECEPTORS, NERVE GROWTH FACTOR;

EID: 84940945829     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2015.0172     Document Type: Article

References (66)

1. Parekkadan B and JM Milwid. (2010). Mesenchymal stem cells as therapeutics. Annu Rev Biomed Eng 12:87-117.
2. Zuk PA, M Zhu, H Mizuno, J Huang, JW Futrell, AJ Katz, P Benhaim, HP Lorenz and MH Hedrick. (2001). Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7:211-228.
3. Lee OK, TK Kuo, WM Chen, KD Lee, SL Hsieh and TH Chen. (2004). Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 103:1669-1675.
4. De Bruyn C, M Najar, G Raicevic, N Meuleman, K Pieters, B Stamatopoulos, A Delforge, D Bron and L Lagneaux. (2011). A rapid, simple, and reproducible method for the isolation of mesenchymal stromal cells from Wharton's jelly without enzymatic treatment. Stem Cells Dev 20:547-557.
5. Vishnubalaji R, M Manikandan, M Al-Nbaheen, B Kadalmani, A Aldahmash and NM Alajez. (2012). In vitro differentiation of human skin-derived multipotent stromal cells into putative endothelial-like cells. BMC Dev Biol 12:7.
6. Moroni L and PM Fornasari. (2013). Human mesenchymal stem cells: a bank perspective on the isolation, characterization and potential of alternative sources for the regeneration of musculoskeletal tissues. J Cell Physiol 228:680-687.
7. Meirelles LdS, AM Fontes, DT Covas and AI Caplan. (2009). Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine Growth Factor Rev 20:419-427.
8. Caplan AI. (2009). Why are MSCs therapeutic? New data: new insight. J Pathol 217:318-324.
9. Dominici M, K Le Blanc, I Mueller, I Slaper-Cortenbach, F Marini, D Krause, R Deans, A Keating, D Prockop and E Horwitz. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315-317.
10. Horwitz EM. (2009). Culture conditions shape mesenchymal stromal cell phenotype and function. Cytotherapy 11:101-102.
11. Delorme B, J Ringe, N Gallay, Y Le Vern, D Kerboeuf, C Jorgensen, P Rosset, L Sensebe, P Layrolle, T Haupl, et al. (2008). Specific plasma membrane protein phenotype of culture-amplified and native human bone marrow mesenchymal stem cells. Blood 111:2631-2635.
12. Mosna F, L Sensebe and M Krampera. (2010). Human bone marrow and adipose tissue mesenchymal stem cells: a user's guide. Stem Cells Dev 19:1449-1470.
13. Jones E and R Schafer. (2015). Biological differences between native and cultured mesenchymal stem cells: implications for therapies. Methods Mol Biol 1235:105-120.
14. Qian H, K Le Blanc and M Sigvardsson. (2012). Primary mesenchymal stem and progenitor cells from bone marrow lack expression of CD44 protein. J Biol Chem 287:25795-25807.
15. Stewart K, P Monk, S Walsh, CM Jefferiss, J Letchford and JN Beresford. (2003). STRO-1, HOP-26 (CD63), CD49a and SB-10 (CD166) as markers of primitive human marrow stromal cells and their more differentiated progeny: a comparative investigation in vitro. Cell Tissue Res 313:281-290.
16. Tormin A, O Li, JC Brune, S Walsh, B Schutz, M Ehinger, N Ditzel, M Kassem and S Scheding. (2011). CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization. Blood 117:5067-5077.
17. Yoshimura K, T Shigeura, D Matsumoto, T Sato, Y Takaki, E Aiba-Kojima, K Sato, K Inoue, T Nagase, I Koshima, et al. (2006). Characterization of freshly isolated and cultured cells derived from the fatty and fluid portions of liposuction aspirates. J Cell Physiol 208:64-76.
18. Bourin P, BA Bunnell, L Casteilla, M Dominici, AJ Katz, KL March, H Redl, JP Rubin, K Yoshimura and JM Gimble. (2013). Stromal cells from the adipose tissuederived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT). Cytotherapy 15:641-648.
19. Suga H, D Matsumoto, H Eto, K Inoue, N Aoi, H Kato, J Araki and K Yoshimura. (2009). Functional implications of CD34 expression in human adipose-derived stem/progenitor cells. Stem Cells Dev 18:1201-1210.
20. Mitchell JB, K McIntosh, S Zvonic, S Garrett, ZE Floyd, A Kloster, Y Di Halvorsen, RW Storms, B Goh, G Kilroy, et al. (2006). Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cellassociated markers. Stem Cells 24:376-385.
21. Najar M, RM Rodrigues, K Buyl, S Branson, T Vanhaecke, L Lagneaux, V Rogiers and J De Kock. (2014). Proliferative and phenotypical characteristics of human adipose tissuederived stem cells: comparison of Ficoll gradient centrifugation and red blood cell lysis buffer treatment purification methods. Cytotherapy 16:1220-1228.
22. Tondreau T, L Lagneaux, M Dejeneffe, M Massy, C Mortier, A Delforge and D Bron. (2004). Bone marrow-derived mesenchymal stem cells already express specific neural proteins before any differentiation. Differentiation 72:319-326.
23. Lv FJ, RS Tuan, KMC Cheung and VYL Leung. (2014). Concise review: the surface markers and identity of human mesenchymal stem cells. Stem Cells 32:1408-1419.
24. Watson JT, T Foo, J Wu, BR Moed, M Thorpe, L Schon and Z Zhang. (2013). CD271 as a marker for mesenchymal stem cells in bone marrow versus umbilical cord blood. Cells Tissues Organs 197:496-504.
25. Nery AA, IC Nascimento, T Glaser, V Bassaneze, JE Krieger and H Ulrich. (2013). Human mesenchymal stem cells: from immunophenotyping by flow cytometry to clinical applications. Cytometry A 83:48-61.
26. Busser H, C De Bruyn, F Urbain, M Najar, K Pieters, G Raicevic, N Meuleman, D Bron and L Lagneaux. (2014). Isolation of adipose-derived stromal cells without enzymatic treatment: expansion, phenotypical, and functional characterization. Stem Cells Dev 23:2390-2400.
27. Fraser JK, M Zhu, I Wulur and Z Alfonso. (2008). Adiposederived stem cells. Methods Mol Biol 449:59-67.
28. Goodison S, V Urquidi and D Tarin. (1999). CD44 cell adhesion molecules. Mol Pathol 52:189-196.
29. Lin CS, H Ning, G Lin and TF Lue. (2012). Is CD34 truly a negative marker for mesenchymal stromal cells? Cytotherapy 14:1159-1163.
30. Baer PC. (2014). Adipose-derived mesenchymal stromal/ stem cells: An update on their phenotype in vivo and in vitro. World J Stem Cells 6:256-265.
31. Maumus M, JA Peyrafitte, R D'Angelo, C Fournier-Wirth, A Bouloumie, L Casteilla, C Sengenes and P Bourin. (2011). Native human adipose stromal cells: localization, morphology and phenotype. Int J Obes (Lond) 35:1141-1153.
32. Nielsen JS and KM McNagny. (2008). Novel functions of the CD34 family. J Cell Sci 121:3683-3692.
33. Sobiesiak M, K Sivasubramaniyan, C Hermann, C Tan, M Orgel, S Treml, F Cerabona, P de Zwart, U Ochs, CA Muller, et al. (2010). The mesenchymal stem cell antigen MSCA-1 is identical to tissue non-specific alkaline phosphatase. Stem Cells Dev 19:669-677.
34. Buhring HJ, VL Battula, S Treml, B Schewe, L Kanz and W Vogel. (2007). Novel markers for the prospective isolation of human MSC. Ann N Y Acad Sci 1106:262-271.
35. Sivasubramaniyan K, A Harichandan, S Schumann, M Sobiesiak, C Lengerke, AMaurer, H Kalbacher and HJ Buhring. (2013). Prospective isolation of mesenchymal stem cells from human bone marrow using novel antibodies directed against Sushi domain containing. Stem Cells Dev 22:1944-1954.
36. Quirici N, D Soligo, P Bossolasco, F Servida, C Lumini and GL Deliliers. (2002). Isolation of bone marrow mesenchymal stem cells by anti-nerve growth factor receptor antibodies. Exp Hematol 30:783-791.
37. Raicevic G, R Rouas, M Najar, P Stordeur, HI Boufker, D Bron, P Martiat, M Goldman, MT Nevessignsky and L Lagneaux. (2010). Inflammation modifies the pattern and the function of Toll-like receptors expressed by human mesenchymal stromal cells. Hum Immunol 71:235-244.
38. Raicevic G, M Najar, B Stamatopoulos, C De Bruyn, N Meuleman, D Bron, M Toungouz and L Lagneaux. (2011). The source of human mesenchymal stromal cells influences their TLR profile as well as their functional properties. Cell Immunol 270:207-216.
39. Tondreau T, N Meuleman, A Delforge, M Dejeneffe, R Leroy, M Massy, C Mortier, D Bron and L Lagneaux. (2005). Mesenchymal stem cells derived from CD133-positive cells in mobilized peripheral blood and cord blood: proliferation, Oct4 expression, and plasticity. Stem Cells 23:1105-1112.
40. Baer PC and H Geiger. (2012). Adipose-derived mesenchymal stromal/stem cells: tissue localization, char-acterization, and heterogeneity. Stem Cells Int 2012: 812693.
41. von Bahr L, B Sundberg, L Lonnies, B Sander, H Karbach, H Hagglund, P Ljungman,BGustafsson,HKarlsson,KLe Blanc, et al. (2012). Long-term complications, immunologic effects, and role of passage for outcome in mesenchymal stromal cell therapy. Biol Blood Marrow Transplant 18:557-564.
42. De Ugarte DA, Z Alfonso, PA Zuk, A Elbarbary, M Zhu, P Ashjian, P Benhaim, MH Hedrick and JK Fraser. (2003). Differential expression of stem cell mobilization-associated molecules on multi-lineage cells from adipose tissue and bone marrow. Immunol Lett 89:267-270.
43. Kern S, H Eichler, J Stoeve, H Kluter and K Bieback. (2006). Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24:1294-1301.
44. Wagner W, FWein, A Seckinger, M Frankhauser, U Wirkner, U Krause, J Blake, C Schwager, V Eckstein,WAnsorge, et al. (2005). Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 33:1402-1416.
45. Id Boufker H, L Lagneaux,M Najar,M Piccart, G Ghanem, JJ Body and F Journe. (2010). The Src inhibitor dasatinib accelerates the differentiation of human bone marrow-derived mesenchymal stromal cells into osteoblasts. BMC Cancer 10:298.
46. Xu J, W Wang, M Ludeman, K Cheng, T Hayami, JC Lotz and S Kapila. (2008). Chondrogenic differentiation of human mesenchymal stem cells in three-alginate gels. Tissue Eng Part A 14:667-680.
47. Ho AD, W Wagner and W Franke. (2008). Heterogeneity of mesenchymal stromal cell preparations. Cytotherapy 10:320-330.
48. De Francesco F, G Ricci, F D'Andrea, GF Nicoletti and GA Ferraro. (2015). Human Adipose Stem Cells (hASCs): from bench to bed-side. Tissue Eng Part B Rev [Epub ahead of print]; DOI:10. 1089/ten. TEB. 2014. 0608.
49. Samsonraj RM, B Rai, P Sathiyanathan, KJ Puan, O Rotzschke, JH Hui, M Raghunath, LW Stanton, V Nurcombe and SM Cool. (2015). Establishing criteria for human mesenchymal stem cell potency. Stem Cells 33:1878-1891.
50. Cuthbert RJ, PV Giannoudis, XN Wang, L Nicholson, D Pawson, A Lubenko, HB Tan, A Dickinson, D McGonagle and E Jones. (2015). Examining the feasibility of clinical grade CD271 + enrichment of mesenchymal stromal cells for bone regeneration. PLoS One 10:e0117855.
51. Jones E and D McGonagle. (2008). Human bone marrow mesenchymal stem cells in vivo. Rheumatology (Oxford) 47:126-131.
52. Battula VL, S Treml, H Abele and HJ Buhring. (2008). Prospective isolation and characterization of mesenchymal stem cells from human placenta using a frizzled-9-specific monoclonal antibody. Differentiation 76:326-336.
53. Jones EA, SE Kinsey, A English, RA Jones, L Straszynski, DM Meredith, AF Markham, A Jack, P Emery and D McGonagle. (2002). Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum 46:3349-3360.
54. Quirici N, C Scavullo, L de Girolamo, S Lopa, E Arrigoni, GL Deliliers and AT Brini. (2010). Anti-L-NGFR and-CD34 monoclonal antibodies identify multipotent mesenchymal stem cells in human adipose tissue. Stem Cells Dev 19:915-925.
55. Alvarez-Viejo M, Y Menendez-Menendez, MA Blanco-Gelaz, A Ferrero-Gutierrez, MA Fernandez-Rodriguez, J Gala and J Otero-Hernandez. (2013). Quantifying mesenchymal stem cells in the mononuclear cell fraction of bone marrow samples obtained for cell therapy. Transplant Proc 45:434-439.
56. Masuda H, SS Anwar, HJ Buhring, JR Rao and CE Gargett. (2012). A novel marker of human endometrial mesenchymal stem-like cells. Cell Transplant 21:2201-2214.
57. Cuevas-Diaz Duran R, MT Gonzalez-Garza, A Cardenas-Lopez, L Chavez-Castilla, DE Cruz-Vega and JE Moreno-Cuevas. (2013). Age-related yield of adipose-derived stem cells bearing the low-affinity nerve growth factor receptor. Stem Cells Int 2013:372164.
58. Corselli M, CW Chen, M Crisan, L Lazzari and B Peault. (2010). Perivascular ancestors of adult multipotent stem cells. Arterioscler Thromb Vasc Biol 30:1104-1109.
59. da Silva Meirelles L, AI Caplan and NB Nardi. (2008). In search of the in vivo identity of mesenchymal stem cells. Stem Cells 26:2287-2299.
60. Ong WK, CS Tan, KL Chan, GG Goesantoso, XHD Chan, E Chan, J Yin, CR Yeo, CM Khoo, JBY So, et al. (2014). Identification of specific cell-surface markers of adiposederived stem cells from subcutaneous and visceral fat depots. Stem Cell Rep 2:171-179.
61. Varma MJO, RGM Breuls, TE Schouten, WJFM Jurgens, HJ Bontkes, GJ Schuurhuis, SM van Ham and FJ van Milligen. (2007). Phenotypical and functional characterization of freshly isolated adipose tissue-derived stem cells. Stem Cells Dev 16:91-104.
62. Boquest AC, A Shahdadfar, K Fronsdal, O Sigurjonsson, SH Tunheim, P Collas and JE Brinchmann. (2005). Isolation and transcription profiling of purified uncultured human stromal stem cells: alteration of gene expression after in vitro cell culture. Mol Biol Cell 16:1131-1141.
63. Miranville A, C Heeschen, C Sengenes, CA Curat, R Busse and A Bouloumie. (2004). Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation 110:349-355.
64. Simmons PJ and B Torok-Storb. (1991). CD34 expression by stromal precursors in normal human adult bone marrow. Blood 78:2848-2853.
65. Simmons PJ and B Torok-Storb. (1991). Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood 78:55-62.
66. Kaiser S, B Hackanson, M Follo, A Mehlhorn, K Geiger, G Ihorst and U Kapp. (2007). BM cells giving rise to MSC in culture have a heterogeneous CD34 and CD45 phenotype. Cytotherapy 9:439-450.