Mesenchymal stem cells and the artery wall

Circulation Research

Volumn 95, Issue 7, 2004, Pages 671-676

  Abedin, Moeen ^a   Tintut, Yin ^a   Demer, Linda L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Atherosclerosis; Bone; Calcification; Mesenchymal stem cell; Vascular

Indexed keywords

ADIPOSE TISSUE; ARTERY WALL; ARTIFACT; BONE MARROW; BONE TISSUE; CARDIOVASCULAR DISEASE; CARTILAGE; CELL DIFFERENTIATION; CELL LINEAGE; CELL REGENERATION; CIRCULATION; ECTOPIC TISSUE; HUMAN; HUMAN CELL; HUMAN TISSUE; MESENCHYMAL STEM CELL; MESENCHYME CELL; MICROVASCULATURE; MULTIPOTENT STEM CELL; MUSCLE TISSUE; PRIORITY JOURNAL; REVIEW; STEM CELL; VASCULAR TISSUE;

ANIMALS; ARTERIES; ARTERIOSCLEROSIS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; CHONDROGENESIS; CHORISTOMA; ENDOTHELIUM, VASCULAR; GRAFT SURVIVAL; HEART TRANSPLANTATION; HUMANS; INFLAMMATION; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; METAPLASIA; MICE; OSTEOGENESIS; REGENERATION; SHEEP; TRANSPLANTATION, HETEROLOGOUS; TUNICA MEDIA;

EID: 4944232950     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000143421.27684.12     Document Type: Review

References (100)

1. Hull G. Caleb Hillier Parry 1755-1822: a notable provincial physician. J R Soc Med. 1998;91:335-338.
2. Virchow R. Cellular Pathology. New York, NY: Dover; 1863.
3. Jeziorska M, McCollum C, Wooley DE. Observations on bone formation and remodeling in advanced atherosclerotic lesions of human carotid arteries. Virchows Arch. 1998;433:559-565.
4. Seemayer TA, Thelmo WL, Morin J. Cartilaginous transformation of the aortic valve. Am J Clin Pathol. 1973;60:616-620.
5. Bunting CH. The formation of true bone with cellular (red) marrow in a sclerotic aorta. Journal of Experimental Medicine. 1906;8:365-376.
6. Buerger L, Oppenheimer A. Bone formation in sclerotic arteries. J Exp Med. 1908;10:354-367.
7. Hunt JL, Fairman R, Mitchell ME, Carpenter JP, Golden M, Khalapyan T, Wolfe M, Neschis D, Milner R, Scoll B, Cusack A, Mohler ER III. Bone formation in carotid plaques: a clinicopathological study. Stroke. 2002;33:1214-1219.
8. Christian RC, Fitzpatrick LA. Vascular calcification. Curr Opin Nephrol Hypertens. 1999;8:443-448.
9. Qiao JH, Mertens RB, Fishbein MC, Geller SA. Cartilaginous metaplasia in calcified diabetic peripheral vascular disease: morphologic evidence of enchondral ossification. Hum Pathol. 2003;34:402-407.
10. Stehbens WE. Chronic vascular changes in the walls of experimental berry aneurysms of the aortic bifurcation in rabbits. Stroke. 1981;12:643-647.
11. Haust D, More RH. Spontaneous Lesions of the Aorta in the Rabbit. New York, NY: Harper and Row; 1965.
12. Hadjiisky P, Donev S, Renais J, Scebat L. Cartilage and bone formation in arterial wall. 1. Morphological and histochemical aspects. Basic Res Cardiol. 1979;74:649-662.
13. Hadjiisky P, Donev S, Renais J, Scebat L. Cartilage and bone formation in arterial wall. 2. Ultrastructural patterns. Basic Res Cardiol. 1980;75:365-367.
14. Rosenfeld ME, Polinsky P, Virmani R, Kauser K, Rubanyi G, Schwartz SM. Advanced atherosclerotic lesions in the innominate artery of the ApoE knockout mouse. Arterioscler Thromb Vasc Biol. 2000;20:2587-2592.
15. Tse J, Martin-McNaulty B, Halks-Miller M, Kauser K, DelVecchio V, Vergona R, Sullivan ME, Rubanyi GM. Accelerated atherosclerosis and premature calcified cartilaginous metaplasia in the aorta of diabetic male Apo E knockout mice can be prevented by chronic treatment with 17 beta-estradiol. Atherosclerosis. 1999;144:303-313.
16. Wayhs R, Zelinger A, Raggi P. High coronary artery calcium scores pose an extremely elevated risk for hard events. J Am Coll Cardiol. 2002;39:225-230.
17. Arad Y, Spadaro LA, Goodman K, Newstein D, Guerci AD. Prediction of coronary events with electron beam computed tomography. J Am Coll Cardiol. 2000;36:1253-1260.
18. Keelan PC, Bielak LF, Ashai K, Jamjoum LS, Denktas AE, Rumberger JA, Sheedy IP, Peyser PA, Schwartz RS. Long-term prognostic value of coronary calcification detected by electron-beam computed tomography in patients undergoing coronary angiography. Circulation. 2001;104:412-417.
19. Wong ND, Detrano RC, Diamond G, Rezayat C, Mahmoudi R, Chong EC, Tang W, Puentes G, Kang X, Abrahamson D. Does coronary artery screening by electron beam computed tomography motivate potentially beneficial lifestyle behaviors? Am J Cardiol. 1996;78:1220-1223.
20. Kelly RP, Tunin R, Kass DA. Effect of reduced aortic compliance on cardiac efficiency and contractile function of in situ canine left ventricle. Circ Res. 1992;71:490-502.
21. Ohtsuka S, Kakihana M, Watanabe H, Sugishita Y. Chronically decreased aortic distensibility causes deterioration of coronary perfusion during increased left ventricular contraction. J Am Coll Cardiol. 1994;24:1406-1414.
22. Watanabe H, Ohtsuka S, Kakihana M, Sugishita Y. Decreased aortic compliance aggravates subendocardial ischaemia in dogs with stenosed coronary artery. Cardiovasc Res. 1992;26:1212-1218.
23. Richardson PD, Davies MJ, Born GV. Influence of plaque configuration and stress distribution on fissuring of coronary atherosclerotic plaques. Lancet. 1989;2:941-944.
24. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276:71-74.
25. Prockop DJ. Marrow stromal cells as stem cells for continual renewal of nonhematopoietic tissues and as potential vectors for gene therapy. J Cell Biochem Suppl. 1998;30-31:284-285.
26. Liechty KW, MacKenzie TC, Shaaban AF, Radu A, Moseley AM, Deans R, Marshak DR, Flake AW. Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med. 2000;6:1282-1286.
27. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7:211-228.
28. Mizuno H, Zuk PA, Zhu M, Lorenz HP, Benhaim P, Hedrick MH. Myogenic differentiation by human processed lipoaspirate cells. Plast Reconstr Surg. 2002;109:199-209.
29. Arai Y, Hirose N, Yamamura K, Kimura M, Murayama A, Fujii I, Tsushima M. Long-term effect of lipid-lowering therapy on atherosclerosis of abdominal aorta in patients with hypercholesterolemia: noninvasive evaluation by a new image analysis program. Angiology. 2002;53:57-68.
30. Wakitani S, Yamamoto T. Response of the donor and recipient cells in mesenchymal cell transplantation to cartilage defect. Microsc Res Tech. 2002;58:14-18.
31. Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood. 2001;98:2396-2402.
32. Erices A, Conget P, Minguell JJ. Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol. 2000;109:235-242.
33. Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, Mavilio F. Muscle regeneration by bone marrow-derived myogenic progenitors. Science. 1998;279:1528-1530.
34. Hirschi KK, Goodell MA. Hematopoietic, vascular and cardiac fates of bone marrow-derived stem cells. Gene Ther. 2002;9:648-652.
35. Caplan AI. Mesenchymal stem cells. J Orthop Res. 1991;9:641-650.
36. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143-147.
37. Schwartz RE, Reyes M, Koodie L, Jiang Y, Blackstad M, Lund T, Lenvik T, Johnson S, Hu WS, Verfaillie CM. Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. J Clin Invest. 2002;109:1291-1302.
38. Hirschi K, Goodell M. Common origins of blood and blood vessels in adults? Differentiation. 2001;68:186-192.
39. Majumdar MK, Banks V, Peluso DP, Morris EA. Isolation, characterization, and chondrogenic potential of human bone marrow-derived multipotential stromal cells. J Cell Physiol. 2000;185:98-106.
40. Song L, Tuan RS. Transdifferentiation potential of human mesenchymal stem cells derived from bone marrow. FASEB J. 2004;18:980-982.
41. Ying QL, Nichols J, Evans EP, Smith AG. Changing potency by spontaneous fusion. Nature. 2002;416:545-548.
42. Terada N, Hamazaki T, Oka M, Hoki M, Mastalerz DM, Nakano Y, Meyer EM, Morel L, Petersen BE, Scott EW. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature. 2002;416:542-545.
43. Kashiwakura Y, Katoh Y, Tamayose K, Konishi H, Takaya N, Yuhara S, Yamada M, Sugimoto K, Daida H. Isolation of bone marrow stromal cell-derived smooth muscle cells by a human SM22alpha promoter: in vitro differentiation of putative smooth muscle progenitor cells of bone marrow. Circulation. 2003;107:2078-2081.
44. Matsumura G, Miyagawa-Tomita S, Shin'oka T, Ikada Y, Kurosawa H. First evidence that bone marrow cells contribute to the construction of tissue-engineered vascular autografts in vivo. Circulation. 2003;108:1729-1734.
45. Babaev VR, Bobryshev YV, Stenina OV, Tararak EM, Gabbiani G. Heterogeneity of smooth muscle cells in atheromatous plaque of human aorta. Am J Pathol. 1990;136:1031-1042.
46. Martin GM, Ogburn CE, Wight TN. Comparative rates of decline in the primary cloning efficiencies of smooth muscle cells from the aging thoracic aorta of two murine species of contrasting maximum life span potentials. Am J Pathol. 1983;110:236-245.
47. Chamley JH, Campbell GR, Burnstock G. Dedifferentiation, redifferentiation and bundle formation of smooth muscle cells in tissue culture: the influence of cell number and nerve fibres. J Embryol Exp Morphol. 1974;32:297-323.
48. Kasai T, Pollak OJ. Smooth muscle cells in aortic cultures of untreated and cholesterol-fed rabbits. Z Zellforsch Mikrosk Anat. 1964;62:743-752.
49. Fritz KE, Jarmolych J, Daoud AS. Association of DNA synthesis and apparent dedifferentiation of aortic smooth muscle cells in vitro. Exp Mol Pathol. 1970;12:354-362.
50. Wissler RW, Vesselinovitch D. Comparative pathogenetic patterns in atherosclerosis. Adv Lipid Res. 1968;6:181-206.
51. Schor AM, Allen TD, Canfield AE, Sloan P, Schor SL. Pericytes derived from the retinal microvasculature undergo calcification in vitro. J Cell Sci. 1990;97:449-461.
52. Watson KE, Bostrom K, Ravindranath R, Lam T, Norton B, Demer LL. TGF-beta 1 and 25-hydroxycholesterol stimulate osteoblast-like vascular cells to calcify. J Clin Invest. 1994;93:2106-2113.
53. Canfield AE, Sutton AB, Hoyland JA, Schor AM. Association of thrombospondin-1 with osteogenic differentiation of retinal pericytes in vitro. J Cell Sci. 1996;109:343-353.
54. Tintut Y, Parhami F, Bostrom K, Jackson SM, Demer LL. cAMP stimulates osteoblast-like differentiation of calcifying vascular cells. Potential signaling pathway for vascular calcification. J Biol Chem. 1998;273:7547-7553.
55. Wada T, McKee MD, Steitz S, Giachelli CM. Calcification of vascular smooth muscle cell cultures: inhibition by osteopontin. Circ Res. 1999;84:166-178.
56. Jono S, Nishizawa Y, Shioi A, Morii H. Parathyroid hormone-related peptide as a local regulator of vascular calcification. Its inhibitory action on in vitro calcification by bovine vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 1997;17:1135-1142.
57. Proudfoot D, Skepper JN, Shanahan CM, Weissberg PL. Calcification of human vascular cells in vitro is correlated with high levels of matrix G1a protein and low levels of osteopontin expression. Arterioscler Thromb Vasc Biol. 1998;18:379-388.
58. Shioi A, Nishizawa Y, Jono S, Koyama H, Hosoi M, Morii H. Beta-glycerophosphate accelerates calcification in cultured bovine vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 1995;15:2003-2009.
59. Lian JB, Stein GS. Concepts of osteoblast growth and differentiation: basis for modulation of bone cell development and tissue formation. Crit Rev Oral Biol Med. 1992;3:269-305.
60. Mohler ER III, Chawla MK, Chang AW, Vyavahare N, Levy RJ, Graham L, Gannon FH. Identification and characterization of calcifying valve cells from human and canine aortic valves. J Heart Valve Dis. 1999;8:254-260.
61. Rajamannan NM, Subramaniam M, Rickard D, Stock SR, Donovan J, Springett M, Orszulak T, Fullerton DA, Tajik AJ, Bonow RO, Spelsberg T. Human aortic valve calcification is associated with an osteoblast phenotype. Circulation. 2003;107:2181-2184.
62. Jarvelainen HT, Kinsella MG, Wight TN, Sandell LJ. Differential expression of small chondroitin/dermatan sulfate proteoglycans, PG-I/biglycan and PG-II/decorin, by vascular smooth muscle and endothelial cells in culture. J Biol Chem. 1991;266:23274-23281.
63. Shanahan CM, Cary NR, Metcalfe JC, Weissberg PL. High expression of genes for calcification-regulating proteins in human atherosclerotic plaques. J Clin Invest. 1994;93:2393-2402.
64. Doherty MJ, Ashton BA, Walsh S, Beresford JN, Grant ME, Canfield AE. Vascular pericytes express osteogenic potential in vitro and in vivo. J Bone Miner Res. 1998;13:828-838.
65. Farrington-Rock C, Crofts NJ, Doherty MJ, Ashton BA, Griffin-Jones C, Canfield AE. Chondrogenc and adipogenic potential of microvascular pericytes. Circulation. In press.
66. Bostrom K, Watson KE, Horn S, Wortham C, Herman IM, Demer LL. Bone morphogenetic protein expression in human atherosclerotic lesions. J Clin Invest. 1993;91:1800-1809.
67. Romanov YA, Svintsitskaya VA, Smirnov VN. Searching for alternative sources of postnatal human mesenchymal stem cells: candidate MSC-like cells from umbilical cord. Stem Cells. 2003;21:105-110.
68. Andreeva ER, Pugach IM, Gordon D, Orekhov AN. Continuous subendothelial network formed by pericyte-like cells in human vascular bed. Tissue Cell. 1998;30:127-135.
69. Ahrens M, Ankenbauer T, Schroder D, Hollnagel A, Mayer H, Gross G. Expression of human bone morphogenetic proteins-2 or -4 in murine mesenchymal progenitor C3H10T1/2 cells induces differentiation into distinct mesenchymal cell lineages. DNA Cell Biol. 1993;12:871-880.
70. Ghosh-Choudhury N, Choudhury GG, Harris MA, Wozney J, Mundy GR, Abboud SL, Harris SE. Autoregulation of mouse BMP-2 gene transcription is directed by the proximal promoter element. Biochem Biophys Res Commun. 2001;286:101-108.
71. Garfinkel A, Tintut Y, Petrasek D, Bostrom K, Demer LL. Pattern formation by vascular mesenchymal cells. Proc Natl Acad Sci USA. 2004;101:9247-9250.
72. Garcia-Castro MI, Marcelle C, Bronner-Fraser M. Ectodermal Wnt function as a neural crest inducer. Science. 2002;297:848-851.
73. Roskelley CD, Bissell MJ. Dynamic reciprocity revisited: a continuous, bidirectional flow of information between cells and the extracellular matrix regulates mammary epithelial cell function. Biochem Cell Biol. 1995;73:391-397.
74. Keren G, Douek P, Oblon C, Bonner RF, Pichard AD, Leon MB. Atherosclerotic saphenous vein grafts treated with different interventional procedures assessed by intravascular ultrasound. Am Heart J. 1992;124:198-206.
75. Lardenoye JH, de Vries MR, Lowik CW, Xu Q, Dhore CR, Cleutjens JP, van Hinsbergh VW, van Bockel JH, Quax PH. Accelerated atherosclerosis and calcification in vein grafts: a study in APOE*3 Leiden transgenic mice. Circ Res. 2002;91:577-584.
76. Caplice NM, Bunch TJ, Stalboerger PG, Wang S, Simper D, Miller DV, Russell SJ, Litzow MR, Edwards WD. Smooth muscle cells in human coronary atherosclerosis can originate from cells administered at marrow transplantation. Proc Natl Acad Sci USA. 2003;100:4754-4759.
77. Rauscher FM, Goldschmidt-Clermont PJ, Davis BH, Wang T, Gregg D, Ramaswami P, Pippen AM, Annex BH, Dong C, Taylor DA. Aging, progenitor cell exhaustion, and atherosclerosis. Circulation. 2003;108:457-463.
78. Han CI, Campbell GR, Campbell JH. Circulating bone marrow cells can contribute to neointimal formation. J Vasc Res. 2001;38:113-119.
79. Shimizu K, Sugiyama S, Aikawa M, Fukumoto Y, Rabkin E, Libby P, Mitchell RN. Host bone-marrow cells are a source of donor intimal smooth-muscle-like cells in murine aortic transplant arteriopathy. Nat Med. 2001;7:738-741.
80. Xu Q, Zhang Z, Davison F, Hu Y. Circulating progenitor cells regenerate endothelium of vein graft atherosclerosis, which is diminished in ApoE-deficient mice. Circ Res. 2003;93:e76-86.
81. Atkinson C, Horsley J, Rhind-Tutt S, Charman S, Phillpotts CJ, Wallwork J, Goddard MJ. Neointimal smooth muscle cells in human cardiac allograft coronary artery vasculopathy are of donor origin. J Heart Lung Transplant. 2004;23:427-435.
82. Ziegelhoeffer T, Fernandez B, Kostin S, Heil M, Voswinckel R, Helisch A, Schaper W. Bone marrow-derived cells do not incorporate into the adult growing vasculature. Circ Res. 2004;94:230-238.
83. Voswinckel R, Ziegelhoeffer T, Heil M, Kostin S, Breier G, Mehling T, Haberberger R, Clauss M, Gaumann A, Schaper W, Seeger W. Circulating vascular progenitor cells do not contribute to compensatory lung growth. Circ Res. 2003;93:372-379.
84. Tanaka K, Sata M, Hirata Y, Nagai R. Diverse contribution of bone marrow cells to neointimal hyperplasia after mechanical vascular injuries. Circ Res. 2003;93:783-790.
85. Campbell JH, Efendy JL, Campbell GR. Novel vascular graft grown within recipient's own peritoneal cavity. Circ Res. 1999;85:1173-1178.
86. Kouchi Y, Onuki Y, Wu MH, Shi Q, Ghali R, Wechezak AR, Kaplan S, Walker M, Sauvage LR. Apparent blood stream origin of endothelial and smooth muscle cells in the neointima of long, impervious carotid-femoral grafts in the dog. Ann Vasc Surg. 1998;12:46-54.
87. Montfort MJ, Olivares CR, Mulcahy JM, Fleming WH. Adult blood vessels restore host hematopoiesis following lethal irradiation. Exp Hematol. 2002;30:950-956.
88. Simper D, Stalboerger PG, Panetta CJ, Wang S, Caplice NM. Smooth muscle progenitor cells in human blood. Circulation. 2002;106:1199-1204.
89. Gulati R, Jevremovic D, Peterson TE, Witt TA, Kleppe LS, Mueske CS, Lerman A, Vile RG, Simari RD. Autologous culture-modified mononuclear cells confer vascular protection after arterial injury. Circulation. 2003;108:1520-1526.
90. Kawamoto A, Gwon HC, Iwaguro H, Yamaguchi JI, Uchida S, Masuda H, Silver M, Ma H, Kearney M, Isner JM, Asahara T. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation. 2001;103:634-637.
91. Griese DP, Ehsan A, Melo LG, Kong D, Zhang L, Mann MJ, Pratt RE, Mulligan RC, Dzau VJ. Isolation and transplantation of autologous circulating endothelial cells into denuded vessels and prosthetic grafts: implications for cell-based vascular therapy. Circulation. 2003;108:2710-2715.
92. Majka SM, Jackson KA, Kienstra KA, Majesky MW, Goodell MA, Hirschi KK. Distinct progenitor populations in skeletal muscle are bone marrow derived and exhibit different cell fates during vascular regeneration. J Clin Invest. 2003;111:71-79.
93. Werner N, Priller J, Laufs U, Endres M, Bohm M, Dimagl U, Nickenig G. Bone marrow-derived progenitor cells modulate vascular reendothelialization and neointimal formation: effect of 3-hydroxy-3-methylglutaryl coenzyme a reductase inhibition. Arterioscler Thromb Vasc Biol. 2002;22:1567-1572.
94. Strehlow K, Werner N, Berweiler J, Link A, Dirnagl U, Priller J, Laufs K, Ghaeni L, Milosevic M, Bohm M, Nickenig G. Estrogen increases bone marrow-derived endothelial progenitor cell production and diminishes neointima formation. Circulation. 2003;107:3059-3065.
95. Bahlmann FH, De Groot K, Spandau JM, Landry AL, Hertel B, Duckert T, Boehm SM, Menne J, Haller H, Fliser D. Erythropoietin regulates endothelial progenitor cells. Blood. 2004;103:921-926.
96. Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, Finkel T. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med. 2003;348:593-600.
97. Laufs U, Werner N, Link A, Endres M, Wassmann S, Jurgens K, Miche E, Bohm M, Nickenig G. Physical training increases endothelial progenitor cells, inhibits neointima formation, and enhances angiogenesis. Circulation. 2004;109:220-226.
98. Beerepoot LV, Mehra N, Vermaat JS, Zonnenberg BA, Gebbink MF, Voest EE. Increased levels of viable circulating endothelial cells are an indicator of progressive disease in cancer patients. Ann Oncol. 2004;15:139-145.
99. Ramasesh N, Adams LB, Franzblau SG, Krahenbuhl JL. Effects of activated macrophages on Mycobacterium leprae. Infect Immun. 1991;59:2864-2869.
100. Darrah PA, Hondalus MK, Chen Q, Ischiropoulos H, Mosser DM. Cooperation between reactive oxygen and nitrogen intermediates in killing of Rhodococcus equi by activated macrophages. Infect Immun. 2000;68:3587-3593.