CD146 expression on mesenchymal stem cells is associated with their vascular smooth muscle commitment

Journal of Cellular and Molecular Medicine

Volumn 18, Issue 1, 2014, Pages 104-114

  Espagnolle, Nicolas ^a   Guilloton, Fabien ^a   Deschaseaux, Frédéric ^a   Gadelorge, Mélanie ^a   Sensébé, Luc ^a   Bourin, Philippe ^a,b  

^a ETABLISSEMENT FRANÇAIS DU SANG   (France)

^b CSA21 7 chemin des silos 31100 ^*  (France)

Author keywords

CD146; Differentiation; Mesenchymal stem cells; Proliferation; Vascular smooth muscle cell

Indexed keywords

CD146 ANTIGEN; FIBROBLAST GROWTH FACTOR 2; MCAM PROTEIN, HUMAN; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CD146; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SEPARATION; CYTOLOGY; DIFFERENTIATION; HUMAN; MESENCHYMAL STEM CELL; MESENCHYMAL STROMA CELL; METABOLISM; MOLECULAR GENETICS; PHENOTYPE; PHYSIOLOGY; PROLIFERATION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; VASCULAR SMOOTH MUSCLE CELL;

CD146; DIFFERENTIATION; MESENCHYMAL STEM CELLS; PROLIFERATION; VASCULAR SMOOTH MUSCLE CELL;

ANTIGENS, CD146; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SEPARATION; CELLS, CULTURED; FIBROBLAST GROWTH FACTOR 2; HUMANS; MESENCHYMAL STROMAL CELLS; MOLECULAR SEQUENCE DATA; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PHENOTYPE; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84891373062     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12168     Document Type: Article

References (45)

1. Friedenstein AJ, Chailakhyan RK, Latsinik NV, et al. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation. 1974; 17: 331-40.
2. Friedenstein AJ, Gorskaja JF, Kulagina NN. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol. 1976; 4: 267-74.
3. Pereira RF, Halford KW, O'Hara MD, et al. Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc Natl Acad Sci USA. 1995; 92: 4857-61.
4. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999; 284: 143-7.
5. Bianco P, Robey PG, Simmons PJ. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell. 2008; 2: 313-9.
6. Delorme B, Ringe J, Gallay N, et al. Specific plasma membrane protein phenotype of culture-amplified and native human bone marrow mesenchymal stem cells. Blood. 2008; 111: 2631-5.
7. Sacchetti B, Funari A, Michienzi S, et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell. 2007; 131: 324-36.
8. Sorrentino A, Ferracin M, Castelli G, et al. Isolation and characterization of CD146+ multipotent mesenchymal stromal cells. Exp Hematol. 2008; 36: 1035-46.
9. Russell KC, Phinney DG, Lacey MR, et al. 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. 2010; 28: 788-98.
10. Tormin A, Li O, Brune JC, et al. CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization. Blood. 2011; 117: 5067-77.
11. Corselli M, Chen CW, Sun B, et al. The tunica adventitia of human arteries and veins as a source of mesenchymal stem cells. Stem Cells Dev. 2012; 21: 1299-308.
12. Crisan M, Yap S, Casteilla L, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008; 3: 301-13.
13. Menard C, Pacelli L, Bassi G, et al. Clinical-grade mesenchymal stromal cells produced under various good manufacturing practice processes differ in their immunomodulatory properties: standardization of immune quality controls. Stem Cells Dev. 2013; 12: 1789-801.
14. Sensebe L, Bourin P, Tarte K. Good manufacturing practices production of mesenchymal stem/stromal cells. Hum Gene Ther. 2011; 22: 19-26.
15. 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.
16. Yang H, Zhang L, Weakley SM, et al. Transforming growth factor-beta increases the expression of vascular smooth muscle cell markers in human multi-lineage progenitor cells. Med Sci Monit. 2011; 17: BR55-61.
17. Kennard S, Liu H, Lilly B. Transforming growth factor-beta (TGF- 1) down-regulates Notch3 in fibroblasts to promote smooth muscle gene expression. J Biol Chem. 2008; 283: 1324-33.
18. Gregory CA, Gunn WG, Peister A, et al. An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Anal Biochem. 2004; 329: 77-84.
19. Greenspan P, Mayer EP, Fowler SD. Nile red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol. 1985; 100: 965-73.
20. Obata H, Hayashi K, Nishida W, et al. Smooth muscle cell phenotype-dependent transcriptional regulation of the alpha1 integrin gene. J Biol Chem. 1997; 272: 26643-51.
21. Belkin VM, Belkin AM, Koteliansky VE. Human smooth muscle VLA-1 integrin: purification, substrate specificity, localization in aorta, and expression during development. J Cell Biol. 1990; 111: 2159-70.
22. Bussone G, Tamby MC, Calzas C, et al. IgG from patients with pulmonary arterial hypertension and/or systemic sclerosis binds to vascular smooth muscle cells and induces cell contraction. Ann Rheum Dis. 2012; 71: 596-605.
23. Montesano R, Orci L. Transforming growth factor beta stimulates collagen-matrix contraction by fibroblasts: implications for wound healing. Proc Natl Acad Sci USA. 1988; 85: 4894-7.
24. Hautmann MB, Madsen CS, Owens GK. A transforming growth factor beta (TGFbeta) control element drives TGFbeta-induced stimulation of smooth muscle alpha-actin gene expression in concert with two CArG elements. J Biol Chem. 1997; 272: 10948-56.
25. Hirschi KK, Rohovsky SA, D'Amore PA. PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J Cell Biol. 1998; 141: 805-14.
26. Kurpinski K, Lam H, Chu J, et al. Transforming growth factor-beta and notch signaling mediate stem cell differentiation into smooth muscle cells. Stem Cells. 2010; 28: 734-42.
27. Wang D, Park JS, Chu JS, et al. Proteomic profiling of bone marrow mesenchymal stem cells upon transforming growth factor beta1 stimulation. J Biol Chem. 2004; 279: 43725-34.
28. Tsutsumi S, Shimazu A, Miyazaki K, et al. Retention of multilineage differentiation potential of mesenchymal cells during proliferation in response to FGF. Biochem Biophys Res Commun. 2001; 288: 413-9.
29. 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: 275-81.
30. Gregory CA, Ylostalo J, Prockop DJ. Adult bone marrow stem/progenitor cells (MSCs) are preconditioned by microenvironmental "niches" in culture: a two-stage hypothesis for regulation of MSC fate. Sci STKE. 2005; 2005: pe37.
31. Bardin N, Frances V, Lesaule G, et al. Identification of the S-Endo 1 endothelial-associated antigen. Biochem Biophys Res Commun. 1996; 218: 210-6.
32. Filshie RJ, Zannettino AC, Makrynikola V, et al. MUC18, a member of the immunoglobulin superfamily, is expressed on bone marrow fibroblasts and a subset of hematological malignancies. Leukemia. 1998; 12: 414-21.
33. Sers C, Kirsch K, Rothbacher U, et al. Genomic organization of the melanoma-associated glycoprotein MUC18: implications for the evolution of the immunoglobulin domains. Proc Natl Acad Sci USA. 1993; 90: 8514-8.
34. Stopp S, Bornhauser M, Ugarte F, et al. Expression of the melanoma cell adhesion molecule in human mesenchymal stromal cells regulates proliferation, differentiation, and maintenance of hematopoietic stem and progenitor cells. Haematologica. 2013; 4: 505-13
35. Sobue K, Hayashi K, Nishida W. Expressional regulation of smooth muscle cell-specific genes in association with phenotypic modulation. Mol Cell Biochem. 1999; 190: 105-18.
36. Johnson RC, Leopold JA, Loscalzo J. Vascular calcification: pathobiological mechanisms and clinical implications. Circ Res. 2006; 99: 1044-59.
37. Charbord P, Tamayo E, Deschaseaux F, et al. The hematopoietic microenvironment: phenotypic and functional characterization of human marrow vascular stromal cells. Hematology. 1999; 4: 257-82.
38. Charbord P, Gown AM, Keating A, et al. CGA-7 and HHF, two monoclonal antibodies that recognize muscle actin and react with adherent cells in human long-term bone marrow cultures. Blood. 1985; 66: 1138-42.
39. Dexter TM. Stromal cell associated haemopoiesis. J Cell Physiol Suppl. 1982; 1: 87-94.
40. Galmiche MC, Koteliansky VE, Briere J, et al. Stromal cells from human long-term marrow cultures are mesenchymal cells that differentiate following a vascular smooth muscle differentiation pathway. Blood. 1993; 82: 66-76.
41. Lo Celso C, Scadden DT. The haematopoietic stem cell niche at a glance. J Cell Sci. 2011; 124: 3529-35.
42. Lichtman MA. The relationship of stromal cells to hemopoietic cells in marrow. Kroc Found Ser. 1984; 18: 3-29.
43. Schmitt-Graff A, Skalli O, Gabbiani G. Alpha-smooth muscle actin is expressed in a subset of bone marrow stromal cells in normal and pathological conditions. Virchows Arch B Cell Pathol Incl Mol Pathol. 1989; 57: 291-302.
44. Charbord P, Tavian M, Humeau L, et al. Early ontogeny of the human marrow from long bones: an immunohistochemical study of hematopoiesis and its microenvironment. Blood. 1996; 87: 4109-19.
45. Corselli M, Chin CJ, Parekh C, et al. Perivascular support of human hematopoietic cells. Blood. 2013; 15: 2891-901