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

Volumn 28, Issue 4, 2010, Pages 788-798

  Russell, Katie C ^a,b   Phinney, Donald G ^b   Lacey, Michelle R ^a   Barrilleaux, Bonnie L ^a,b   Meyertholen, Kristin E ^a   O'Connor, Kim C ^a,b  

^a Tulane University   (United States)

^b TULANE UNIVERSITY   (United States)

Author keywords

Assay; Clone; Differentiation; Heterogeneity; Hierarchy; Mesenchymal stem cells

Indexed keywords

5' NUCLEOTIDASE; ADAPALENE; CD146 ANTIGEN; HERMES ANTIGEN;

ADIPOGENESIS; ADULT; ANTIGEN EXPRESSION; ARTICLE; BONE DEVELOPMENT; CELL ASSAY; CELL CLONE; CELL CULTURE; CELL HETEROGENEITY; CELL LINEAGE; CELL PROLIFERATION; CHONDROGENESIS; COLONY FORMING UNIT; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; IN VITRO STUDY; MESENCHYMAL STEM CELL; MULTIPOTENT STEM CELL; NORMAL HUMAN; PHENOTYPE; PROTEIN EXPRESSION; STEM CELL EXPANSION;

ANTIGENS, CD146; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; HUMANS; MESENCHYMAL STEM CELLS;

EID: 77950991204     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.312     Document Type: Article

References (53)

1. Barrilleaux B, Phinney DG, Prockop DJ et al. Review: Ex vivo engineering of living tissues with adult stem cells. Tissue Eng 2006;12: 3007-3019. (Pubitemid 44846407)
2. Phinney DG. Biochemical heterogeneity of mesenchymal stem cell populations: Clues to their therapeutic efficacy. Cell Cycle 2007;6:2884-2889.
3. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society For Cellular Therapy Position Statement. Cytotherapy 2006;8:315-317.
4. Wang CC, Chen CH, Lin WW et al. Direct intramyocardial injection of mesenchymal stem cell sheet fragments improves cardiac functions after infarction. Cardiovasc Res 2008;77:515-524.
5. Choi S, Park M, Kim J et al. The role of mesenchymal stem cells in the functional improvement of the chronic renal failure. Stem Cells Dev 2009;18:521-529.
6. Wang Y, Kim UJ, Blasioli DJ et al. In vitro cartilage tissue engineering with 3D porous aqueous-derived silk scaffolds and mesenchymal stem cells. Biomaterials 2005;26:7082-7094.
7. Muraglia A, Cancedda R, Quarto R. Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci 2000;113(Pt 7):1161-1166. (Pubitemid 30229533)
8. Kuznetsov SA, Krebsbach PH, Satomura K et al. Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J Bone Miner Res 1997;12:1335-1347. (Pubitemid 27375376)
9. Digirolamo CM, Stokes D, Colter D et al. 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 1999;107:275-281. (Pubitemid 29530211)
10. Banfi A, Muraglia A, Dozin B et al. Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: Implications for their use in cell therapy. Exp Hematol 2000;28: 707-715. (Pubitemid 30398528)
11. Suva D, Garavaglia G, Menetrey J et al. Non-hematopoietic human bone marrow contains long-lasting, pluripotential mesenchymal stem cells. J Cell Physiol 2004;198:110-118. (Pubitemid 38120971)
12. Chen FG, Zhang WJ, Bi D et al. Clonal analysis of nestin(-) vimentin(+) multipotent fibroblasts isolated from human dermis. J Cell Sci 2007;120:2875-2883. (Pubitemid 47394261)
13. D'Ippolito G, Diabira S, Howard GA et al. Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of post-natal young and old human cells with extensive expansion and differentiation potential. J Cell Sci 2004;117:2971-2981. (Pubitemid 39117672)
14. Colter DC, Sekiya I, Prockop DJ. Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc Natl Acad Sci U S A 2001;98: 7841-7845. (Pubitemid 32642648)
15. Wagner W, Feldmann RE, Jr., Seckinger A et al. The heterogeneity of human mesenchymal stem cell preparations - Evidence from simultaneous analysis of proteomes and transcriptomes. Exp Hematol 2006; 34:536-548.
16. Smith JR, Pochampally R, Perry A et al. Isolation of a highly clonogenic and multipotential subfraction of adult stem cells from bone marrow stroma. Stem Cells 2004;22:823-831. (Pubitemid 39166939)
17. Penick KJ, Solchaga LA, Welter JF. High-throughput aggregate culture system to assess the chondrogenic potential of mesenchymal stem cells. Biotechniques 2005;39:687-691.
18. Sekiya I, Larson BL, Smith JR et al. Expansion of human adult stem cells from bone marrow stroma: conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells 2002;20: 530-541. (Pubitemid 35463066)
19. Pittenger MF, Mackay AM, Beck SC et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-147. (Pubitemid 29282067)
20. Hung SC, Pochampally RR, Hsu SC et al. Short-term exposure of multipotent stromal cells to low oxygen increases their expression of CX3CR1 and CXCR4 and their engraftment in vivo. PLoS One 2007; 2:e416.
21. Stanford CM, Jacobson PA, Eanes ED et al. Rapidly forming apatitic mineral in an osteoblastic cell line (UMR 106-01 BSP). J Biol Chem 1995;270:9420-9428.
22. Mbalaviele G, Abu-Amer Y, Meng A et al. Activation of peroxisome proliferator-activated receptor-gamma pathway inhibits osteoclast differentiation. J Biol Chem 2000;275:14388-14393. (Pubitemid 30339723)
23. Sekiya I, Larson BL, Vuoristo JT et al. Comparison of effect of BMP-2, -4, and -6 on in vitro cartilage formation of human adult stem cells from bone marrow stroma. Cell Tissue Res 2005;320: 269-276.
24. Johnstone B, Hering TM, Caplan AI et al. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 1998;238:265-272.
25. Denker AE, Haas AR, Nicoll SB et al. Chondrogenic differentiation of murine C3H10T1/2 multipotential mesenchymal cells: I. Stimulation by bone morphogenetic protein-2 in high-density micromass cultures. Differentiation 1999;64:67-76.
26. Lunstrum GP, Keene DR, Weksler NB et al. Chondrocyte differentiation in a rat mesenchymal cell line. J Histochem Cytochem 1999;47: 1-6. (Pubitemid 29044283)
27. Farndale RW, Sayers CA, Barrett AJ. A direct spectrophotometric microassay for sulfated glycosaminoglycans in cartilage cultures. Connect Tissue Res 1982;9:247-248.
28. Barbosa I, Garcia S, Barbier-Chassefiere V et al. Improved and simple micro assay for sulfated glycosaminoglycans quantification in biological extracts and its use in skin and muscle tissue studies. Glycobiology 2003;13:647-653. (Pubitemid 37220443)
29. O'Connor KC, Enmon RM, Dotson RS et al. Characterization of autocrine growth factors, their receptors and extracellular matrix present in three-dimensional cultures of Du 145 human prostate carcinoma cells grown in simulated microgravity. Tissue Eng 1997;3:161-171.
30. Song H, David O, Clejan S et al. Spatial composition of prostate cancer spheroids in mixed and static cultures. Tissue Eng 2004;10: 1266-1276. (Pubitemid 39223803)
31. Sorrentino A, Ferracin M, Castelli G et al. Isolation and characterization of CD146+ multipotent mesenchymal stromal cells. Exp Hematol 2008;36:1035-1046.
32. Majore I, Moretti P, Hass R et al. Identification of subpopulations in mesenchymal stem cell-like cultures from human umbilical cord. Cell Commun Signal 2009;7:6.
33. Bühring HJ, Battula VL, Treml S et al. Novel markers for the prospective isolation of human MSC. Ann NY Acad Sci 2007;1106: 262-271. (Pubitemid 47443036)
34. Markov V, Kusumi K, Tadesse MG et al. Identification of cord blood-derived mesenchymal stem/stromal cell populations with distinct growth kinetics, differentiation potentials, and gene expression profiles. Stem Cells Dev 2007;16:53-73. (Pubitemid 46362592)
35. Halleux C, Sottile V, Gasser JA et al. Multi-lineage potential of human mesenchymal stem cells following clonal expansion. J Musculoskelet Neuronal Interact 2001;2:71-76.
36. Okamoto T, Aoyama T, Nakayama T et al. Clonal heterogeneity in differentiation potential of immortalized human mesenchymal stem cells. Biochem Biophys Res Commun 2002;295:354-361. (Pubitemid 34785842)
37. Ortiz LA, Dutreil M, Fattman C et al. Interleukin 1 receptor antagonist mediates the antiinflammatory and antifibrotic effect of mesenchymal stem cells during lung injury. Proc Natl Acad Sci U S A 2007; 104:11002-11007. (Pubitemid 47175216)
38. Bianchi G, Banfi A, Mastrogiacomo M et al. Ex vivo enrichment of mesenchymal cell progenitors by fibroblast growth factor 2. Exp Cell Res 2003;287:98-105. (Pubitemid 36683205)
39. Geiger H, True JM, de Haan G et al. Age- and stage-specific regulation patterns in the hematopoietic stem cell hierarchy. Blood 2001;98: 2966-2972.
40. Ogawa M. Differentiation and proliferation of hematopoietic stem cells. Blood 1993;81:2844-2853. (Pubitemid 23162099)
41. Prudhomme WA, Duggar KH, Lauffenburger DA. Cell population dynamics model for deconvolution of murine embryonic stem cell self-renewal and differentiation responses to cytokines and extracellular matrix. Biotechnol Bioeng 2004;88:264-272.
42. Viswanathan S, Davey RE, Cheng D et al. Clonal evolution of stem and differentiated cells can be predicted by integrating cell-intrinsic and -extrinsic parameters. Biotechnol Appl Biochem 2005;42: 119-131. (Pubitemid 41445233)
43. Phinney DG, Prockop DJ. Concise review: Mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair - Current views. Stem Cells 2007;25:2896-2902.
44. Pera MF. Stem cells: Low-risk reprogramming. Nature 2009;458: 715-716.
45. Song H, O'Connor KC, Papadopoulos KD et al. Differentiation kinetics of in vitro 3T3-L1 preadipocyte cultures. Tissue Eng 2002;8: 1071-1081. (Pubitemid 35397252)
46. Hong JH, Hwang ES, McManus MT et al. TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 2005; 309:1074-1078. (Pubitemid 41134465)
47. Gronthos S, Zannettino AC, Hay SJ et al. Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 2003;116:1827-1835. (Pubitemid 36582169)
48. Mareddy S, Crawford R, Brooke G et al. Clonal isolation and characterization of bone marrow stromal cells from patients with osteoarthritis. Tissue Eng 2007;13:819-829. (Pubitemid 46651512)
49. Shih IM. The role of CD146 (Mel-CAM) in biology and pathology. J Pathol 1999;189:4-11.
50. Baksh D, Yao R, Tuan RS. Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow. Stem Cells 2007;25:1384-1392. (Pubitemid 47106005)
51. Covas DT, Panepucci RA, Fontes AM et al. Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts. Exp Hematol 2008;36:642-654.
52. Shi S, Gronthos S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 2003; 18:696-704. (Pubitemid 36899319)
53. Xie S, Luca M, Huang S et al. Expression of MCAM/MUC18 by human melanoma cells leads to increased tumor growth and metastasis. Cancer Res 1997;57:2295-2303. (Pubitemid 27247052)