Molecular and functional effects of organismal ageing on smooth muscle cells derived from bone marrow mesenchymal stem cells

Cardiovascular Research

Volumn 87, Issue 1, 2010, Pages 147-155

  Han, Juhee ^a   Liu, Jin Yu ^a   Swartz, Daniel D ^b,c   Andreadis, Stelios T ^a,c  

^a the State University of New York   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

Author keywords

Ageing; Bone marrow; Cardiovascular tissue regeneration; Extracellular matrix profile; Mesenchymal stem cells; Smooth muscle; Vascular reactivity

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BASIC FIBROBLAST GROWTH FACTOR; CALVASCULIN; COLLAGEN TYPE 1; DESMIN; ELASTIN; ENDOTHELIN 1; FIBRIN; SMOOTHELIN; TRANSFORMING GROWTH FACTOR BETA1; TROPOELASTIN; ACTIN; ENHANCED GREEN FLUORESCENT PROTEIN; FIBROBLAST GROWTH FACTOR 2; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; VASOCONSTRICTOR AGENT;

AGING; ANIMAL CELL; ARTICLE; BLOOD VESSEL REACTIVITY; CELL PROLIFERATION; CLONOGENESIS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HYDROGEL; MESENCHYMAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SHEEP; SMOOTH MUSCLE FIBER; TENSILE STRENGTH; TISSUE REGENERATION; AGE; ANIMAL; BIOSYNTHESIS; BONE MARROW CELL; CELL AGING; COMPARATIVE STUDY; DOWN REGULATION; DRUG EFFECTS; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; NEWBORN; PHENOTYPE; PHYSIOLOGY; PROMOTER REGION; REPORTER GENE; TRANSGENIC ANIMAL; VASOCONSTRICTION;

ACTINS; AGE FACTORS; AGING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANIMALS, NEWBORN; BONE MARROW CELLS; CELL AGING; CELL PROLIFERATION; COLLAGEN TYPE I; DESMIN; DOWN-REGULATION; FIBRIN; FIBROBLAST GROWTH FACTOR 2; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; MESENCHYMAL STROMAL CELLS; MYOCYTES, SMOOTH MUSCLE; PHENOTYPE; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; SHEEP; TRANSFORMING GROWTH FACTOR BETA1; TROPOELASTIN; VASOCONSTRICTION; VASOCONSTRICTOR AGENTS;

EID: 77955138569     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvq024     Document Type: Article

References (48)

1. Roobrouck VD, Ulloa-Montoya F, Verfaillie CM. Self-renewal and differentiation capacity of young and aged stem cells. Exp Cell Res 2008;314:1937-1944.
2. Stenderup K, Justesen J, Clausen C, Kassem M. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 2003;33:919-926.
3. Baxter MA, Wynn RF, Jowitt SN, Wraith JE, Fairbairn LJ, Bellantuono I. Study of tel-omere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells 2004;22:675-682.
4. Hacia JG, Lee CC, Jimenez DF, Karaman MW, Ho VV, Siegmund KD et al. Age-related gene expression profiles of rhesus monkey bone marrow-derived mesenchymal stem cells. J Cell Biochem 2008;103:1198-1210.
5. Meirelles Lda S, Nardi NB. Murine marrow-derived mesenchymal stem cell: isolation, in vitro expansion, and characterization. Br J Haematol 2003;123:702-711.
6. Zhou S, Greenberger JS, Epperly MW, Goff JP, Adler C, Leboff MS et al. Age-related intrinsic changes in human bone-marrow-derived mesenchymal stem cells and their differentiation to osteoblasts. Aging Cell 2008;7:335-343.
7. D'Ippolito G, Schiller PC, Ricordi C, Roos BA, Howard GA. Age-related osteogenic potential of mesenchymal stromal stem cells from human vertebral bone marrow. J Bone Miner Res 1999;14:1115-1122.
8. Zheng H, Martin JA, Duwayri Y, Falcon G, Buckwalter JA. Impact of aging on rat bone marrow-derived stem cell chondrogenesis. J Gerontol A Biol Sci Med Sci 2007;62: 136-148.
9. Roura S, Farre J, Soler-Botija C, Llach A, Hove-Madsen L, Cairo JJ et al. Effect of aging on the pluripotential capacity of human CD105(\+) mesenchymal stem cells. Eur J Heart Fail 2006;8:555-563.
10. Dressler MR, Butler DL, Boivin GP. Effects of age on the repair ability of mesenchymal stem cells in rabbit tendon. J Orthop Res 2005;23:287-293.
11. Ruiz-Torres A, Gimeno A, Melon J, Mendez L, Munoz FJ, Macia M. Age-related loss of proliferative activity of human vascular smooth muscle cells in culture. Mech Ageing Dev 1999;110:49-55.
12. Solan A, Niklason L. Age effects on vascular smooth muscle: an engineered tissue approach. Cell Transplant 2005;14:481-488.
13. Gong Z, Niklason LE. Blood vessels engineered from human cells. Trends Cardiovasc Med 2006;16:153-156.
14. McKee JA, Banik SS, Boyer MJ, Hamad NM, Lawson JH, Niklason LE et al. Human arteries engineered in vitro. EMBO Rep 2003;4:633-638.
15. Poh M, Boyer M, Solan A, Dahl SL, Pedrotty D, Banik SS et al. Blood vessels engineered from human cells. Lancet 2005;365:2122-2124.
16. Klinger RY, Blum JL, Hearn B, Lebow B, Niklason LE. Relevance and safety of telomer-ase for human tissue engineering. Proc Natl Acad Sci USA 2006;103:2500-2505.
17. Liu JY, Peng HF, Andreadis ST. Contractile smooth muscle cells derived from hair-follicle stem cells. Cardiovasc Res 2008;79:24-33.
18. Liu JY, Swartz DD, Peng HF, Gugino SF, Russell JA, Andreadis ST. Functional tissue-engineered blood vessels from bone marrow progenitor cells. Cardiovasc Res 2007;75:618-628.
19. Swartz DD, Russell JA, Andreadis ST. Engineering of fibrin-based functional and implantable small-diameter blood vessels. Am J Physiol Heart Circ Physiol 2005;288: H1451-H1460.
20. Koria P, Brazeau D, Kirkwood K, Hayden P, Klausner M, Andreadis ST. Gene expression profile of tissue engineered skin subjected to acute barrier disruption. J Invest Dermatol 2003;121:368-382
21. An YH, Freidman RJ, eds. Animal Models in Orthopaedic Research. Boca Raton, FL: CRC Press; 1999.
22. Grainger DJ. Transforming growth factor beta and atherosclerosis: so far, so good for the protective cytokine hypothesis. Arterioscler Thromb Vasc Biol 2004;24:399-404.
23. Yao L, Swartz DD, Gugino SF, Russell JA, Andreadis ST. Fibrin-based tissue-engineered blood vessels: differential effects of biomaterial and culture parameters on mechanical strength and vascular reactivity. Tissue Eng 2005;11:991-1003.
24. Hinz B, Celetta G, Tomasek JJ, Gabbiani G, Chaponnier C. Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol Biol Cell 2001;12: 2730-2741.
25. Chen J, Li H, SundarRaj N, Wang JH. Alpha-smooth muscle actin expression enhances cell traction force. Cell Motil Cytoskeleton 2007;64:248-257.
26. Bar H, Wende P, Watson L, Denger S, van Eys G, Kreuzer J et al. Smoothelin is an indicator of reversible phenotype modulation of smooth muscle cells in balloon-injured rat carotid arteries. Basic Res Cardiol 2002;97:9-16.
27. van der Loop FT, Gabbiani G, Kohnen G, Ramaekers FC, van Eys GJ. Differentiation of smooth muscle cells in human blood vessels as defined by smoothelin, a novel marker for the contractile phenotype. Arterioscler Thromb Vasc Biol 1997;17:665-671.
28. Loufrani L, Matrougui K, Li Z, Levy BI, Lacolley P, Paulin D et al. Selective microvas-cular dysfunction in mice lacking the gene encoding for desmin. FASEB J 2002;16: 117-119.
29. Tsutsumi S, Shimazu A, Miyazaki K, Pan H, Koike C, Yoshida E et al. Retention of mul-tilineage differentiation potential of mesenchymal cells during proliferation in response to FGF. Biochem Biophys Res Commun 2001;288:413-419.
30. Solchaga LA, Penick K, Porter JD, Goldberg VM, Caplan AI, Welter JF. FGF-2 enhances the mitotic and chondrogenic potentials of human adult bone marrow-derived mesenchymal stem cells. J Cell Physiol 2005;203:398-409.
31. Vallier L, Alexander M, Pedersen RA. Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J Cell Sci 2005;118:4495-4509.
32. Bianchi G, Banfi A, Mastrogiacomo M, Notaro R, Luzzatto L, Cancedda R et al. Ex vivo enrichment of mesenchymal cell progenitors by fibroblast growth factor 2. Exp Cell Res 2003;287:98-105.
33. Mastrogiacomo M, Cancedda R, Quarto R. Effect of different growth factors on the chondrogenic potential of human bone marrow stromal cells. Osteoarthritis Cartilage 2001;9(Suppl. A):S36-S40.
34. Zaragosi LE, Ailhaud G, Dani C. Autocrine fibroblast growth factor 2 signaling is critical for self-renewal of human multipotent adipose-derived stem cells. Stem Cells 2006; 24:2412-2419.
35. Ito T, Sawada R, Fujiwara Y, Seyama Y, Tsuchiya T. FGF-2 suppresses cellular senescence of human mesenchymal stem cells by down-regulation of TGF-beta2. Biochem Biophys Res Commun 2007;359:108-114.
36. Sinha S, Hoofnagle MH, Kingston PA, McCanna ME, Owens GK. Transforming growth factor-beta1 signaling contributes to development of smooth muscle cells from embryonic stem cells. Am J Physiol Cell Physiol 2004;287:C1560-C1568.
37. 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;141:805-814.
38. Kinner B, Zaleskas JM, Spector M. Regulation of smooth muscle actin expression and contraction in adult human mesenchymal stem cells. Exp Cell Res 2002;278:72-83.
39. Wang D, Park JS, Chu JS, Krakowski A, Luo K, Chen DJ et al. Proteomic profiling of bone marrow mesenchymal stem cells upon transforming growth factor beta1 stimulation. J Biol Chem 2004;279:43725-43734.
40. Gong Z, Niklason LE. Small-diameter human vessel wall engineered from bone marrow-derived mesenchymal stem cells (hMSCs). FASEB J 2008;22:1635-1648.
41. Ross JJ, Hong Z, Willenbring B, Zeng L, Isenberg B, Lee EH et al. Cytokine-induced differentiation of multipotent adult progenitor cells into functional smooth muscle cells. J Clin Invest 2006;116:3139-3149.
42. Long JL, Tranquillo RT. Elastic fiber production in cardiovascular tissue-equivalents. Matrix Biol 2003;22:339-350.
43. Loufrani L, Li Z, Levy BI, Paulin D, Henrion D. Excessive microvascular adaptation to changes in blood flow in mice lacking gene encoding for desmin. Arterioscler Thromb Vasc Biol 2002;22:1579-1584.
44. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 2004;84:767-801.
45. Barocas VH, Girton TS, Tranquillo RT. Engineered alignment in media equivalents: magnetic prealignment and mandrel compaction. J Biomech Eng 1998;120:660-666.
46. Zhang H, Fazel S, Tian H, Mickle DA, Weisel RD, Fujii T et al. Increasing donor age adversely impacts beneficial effects of bone marrow but not smooth muscle myocar-dial cell therapy. Am J Physiol Heart Circ Physiol 2005;289:H2089-H2096.
47. Zhang ZY, Teoh SH, Chong MS, Schantz JT, Fisk NM, Choolani MA et al. Superior osteogenic capacity for bone tissue engineering of fetal compared to perinatal and adult mesenchymal stem cells. Stem Cells 2009;27:126-137.
48. Psaltis PJ, Zannettino AC, Worthley SG, Gronthos S. Concise review: mesenchymal stromal cells: potential for cardiovascular repair. Stem Cells 2008;26:2201-2210.