Smooth Muscle Stem Cells

Anatomical Record - Part A Discoveries in Molecular, Cellular, and Evolutionary Biology

Volumn 276, Issue 1, 2004, Pages 22-33

  Hirschi, Karen K ^a,b   Majesky, Mark W ^c,d  

^a CENTER FOR CELL AND GENE THERAPY   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Bone marrrow derived SP cells; Neural crest; Proepicardial cells

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CYANOCOBALAMIN; ENDOTHELIN 1; FIBROBLAST GROWTH FACTOR 8; INTRINSIC FACTOR; PROTEIN TBX1; TRANSCRIPTION FACTOR FOXC1; TRANSCRIPTION FACTOR PAX3; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ARTERY INJURY; BONE MARROW CELL; CELL DIFFERENTIATION; CELL FATE; EMBRYO; ENDOTHELIUM CELL; MOUSE; MULTIPOTENT STEM CELL; NEURAL CREST CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SMOOTH MUSCLE FIBER; STEM CELL; VASCULAR SMOOTH MUSCLE; VASCULAR SURGERY;

EID: 0347320857     PISSN: 0003276X     EISSN: None     Source Type: Journal    
DOI: 10.1002/ar.a.10128     Document Type: Review

References (93)

1. Abu-Issa R, Smyth G, Smoak I, Yamamura K, Meyers E. 2002. Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development 129:4613-4625.
2. Anderson D, Groves A, Lo L, Ma Q, Rao M, Shah N, Sommer L. 1997. Cell lineage determination and the control of neuronal identity in the neural crest. Cold Spring Harbor Symp Quant Biol 62:493-504.
3. Arciniegas E, Graterol A, Sanchez F. 2000. Characterization of non-muscle cells present in the intima of normal adult bovine pulmonary artery. Anat Rec 258:262-268.
4. Asakura A, Seale P, Girgis-Gabardo A, Rudnicki M. 2002. Myogenic specification of side population cells in skeletal muscle. J Cell Biol 159:123-134.
5. Ballard V, Mikawa T. 2002. Constitutive expression of preproendothelin in the cardiac neural crest selectively promotes expansion of the adventitia of the great vessels in vivo. Dev Biol 251:167-177.
6. Bannerman P, Nichols W, Puhalla S, Oliver T, Berman M, Pleasure D. 2000. Early migratory rat neural crest cells express functional gap junctions: evidence that neural crest cell survival requires gap junction function. J Neurosci Res 61:605-615.
7. Betsholtz C, Karlsson L, Lindahl P. 2001. Developmental roles of platelet-derived growth factors. Bioessays 23:494-507.
8. Bockman D, Redmond M, Waldo K, Davis H, Kirby M. 1987. Effect of neural crest ablation on development of the heart and arch arteries in the chick. Am J Anat 180:332-341.
9. Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch D, McMahon A, Sommer L, Boussadia O, Kemler R. 2001. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128:1253-1264.
10. Carmeliet P. 2000. One cell, two fates. Nature 408:43-45.
11. Chang C, Hemmati-Brivanlou A. 1998. Neural crest induction by Xwnt7B in Xenopus. Dev Biol 194:129-134.
12. Chen S, Kulik M, Lechleider R. 2003. Smad proteins regulate transcriptional induction of the SM22α gene by TGF-β. Nucleic Acids Res 31:1302-1310.
13. Clouthier D, Hosoda K, Richardson J, Williams S, Yanagisawa H, Kuwaki T, Kumada M, Hammer R, Yanagisawa M. 1998. Cranial and cardiac neural crest defects in endothelin-A receptor-deficient mice. Development 125:813-824.
14. Conway S, Bundy J, Chen J, Dickman E, Rogers R, Will B. 2000. Decreased neural crest stem cell expansion is responsible for the conotruncal heart defects within the splotch (Sp(2H))/Pax3 mouse mutant. Cardiovasc Res 47:314-328.
15. DeRuiter M, Poelmann R, VanMunsteren J, Mironov V, Markwald R, Gittenberger-de Groot A. 1997. Embryonic endothelial cells transdifferentiate into mesenchymal cells expressing smooth muscle actins in vivo and in vitro. Circ Res 80:444-451.
16. Ema M, Faloon P, Zhang W, Hirashima M, Reid T, Stanford W, Orkin S, Choi K, Rossant J. 2003. Combinatorial effects of Flk1 and Tal1 on vascular and hematopoietic development in the mouse. Genes Dev 17:380-393.
17. Epstein J, Li J, Lang D, Chen F, Brown C, Jin F, Lu M, Thomas M, Liu E, Wessels A, Lo C. 2000. Migration of cardiac neural crest cells in Splotch embryos. Development 127:1869-1878.
18. Franz T. 1989. Persistent truncus arteriosus in the Splotch mutant mouse. Anat Embryol 180:457-464.
19. Franz T, Kothary R, Surani M, Halata Z, Grim M. 1993. The splotch mutation inferferes with muscle development in the limbs. Anat Embryol (Berl) 187:153-160.
20. Frid M, Kale V, Stenmark K. 2002. Mature vascular endothelium can give rise to smooth muscle cells via endothelial-mesenchymal transdifferentiation: in vitro analysis. Circ Res 90:1189-1196.
21. Ghyselinck N, Wendling O, Messaddeq N, Dierich A, Lampron C, Decimo D, Viville S, Chambon P, Mark M. 1998. Contribution of retinoic acid receptor beta isoforms to the formation of the conotruncal septum of the embryonic heart. Dev Biol 196:303-318.
22. Gittenberger-de Groot A, Vrancken Peeters M, Mentink M, Gourdie R, Poelmann R. 1998. Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions. Circ Res 82:1043-1052.
23. Goodell M, Brose K, Paradis G, Conner A, Mulligan R. 1996. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183:1797-1806.
24. Gruneberg H, Truslove G. 1960. Two closely linked genes in the mouse. Genet Res (Camb) 1:69-90.
25. Guillemot F, Lo L, Johnson J, Auerbach A, Anderson D, Joyner A. 1993. Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75:463-476.
26. Han C, Campbell G, Campbell J. 2001. Circulating bone marrow cells can contribute to neointimal formation. J Vasc Res 38:113-119.
27. Hillebrands J, Klatter F, van den Hurk B, Popa E, Nieuwenhuis P, Rozing J. 2001. Origin of neointimal endothelium and alpha-actin-positive smooth muscle cells in transplant arteriosclerosis. J Clin Invest 107:1411-1422.
28. Hirschi K, Rohovsky S, D'Amore P. 1998. 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 141:805-814.
29. Hirschi K, Rohovsky S, Beck L, Smith S, D'Amore, P. 1999. Endothelial cells modulate the proliferation of mural cell precursors via platelet-derived growth factor-BB and heterotypic cell contact. Circ Res 84:298-305.
30. Hu Y, Davison F, Ludewig B, Erdel M, Mayr M, Url M, Dietrich H, Xu Q. 2002. Smooth muscle cells in transplant atherosclerotic lesions are originated from recipients, but not bone marrow progenitor cells. Circulation 106:1834-1839.
31. Huang G, Wessels A, Smith B, Linask K, Ewart J, Lo C. 1998. Alteration in connexin 43 gap junction gene dosage impairs conotruncal heart development. Dev Biol 198:32-44.
32. Ikeya M, Lee S, Johnson J, McMahon A, Takada S. 1997. Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389:966-970.
33. Ishisaki A, Hayashi H, Li A, Imamura T. 2003. Human umbilical vein endothelium -derived cells retain potential to differentiate into smooth muscle-like cells. J Biol Chem 278:1303-1309.
34. Jackson K, Majka S, Wang H, Pocius J, Hartley C, Majesky M, Entman M, Michael L, Hirschi K, Goodell M. 2001. Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 107:1395-1402.
35. Jiang X, Rowitch D, Soriano P, McMahon A, Sucov H. 2000. Fate of the mammalian cardiac neural crest. Development 127:1607-1616.
36. Kelly R, Brown N, Buckingham M. 2001. The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev Cell 1:435-440.
37. Kirby M. 1989. Plasticity and predetermination of mesencephalic and trunk neural crest transplanted into the region of the cardiac neural crest. Dev Biol 134:402-412.
38. Kirby M, Waldo K. 1995. Neural crest and cardiovascular patterning. Circ Res 77:211-215.
39. Kubu C, Orimoto K, Morrison S, Weinmaster G, Anderson D, Verdi J. 2002. Developmental changes in Notch1 and numb expression mediated by local cell-cell interactions underlie progressively increasing delta sensitivity in neural crest stem cells. Dev Biol 244:199-214.
40. Kurihara Y, Kurihara H, Oda H, Maemura K, Nagai R, Ishikawa T, Yazaki Y. 1995. Aortic arch malformations and ventricular septal defect in mice deficient in endothelin-1. J Clin Invest 96:293-300.
41. Kwang S, Brugger S, Lazik A, Merrill A, Wu L, Liu Y, Ishi M, Sangiorgi F, Rauchman M, Sucov H, Maas R, Maxon RJ. 2002. Msx2 is an immediate downstream effector of Pax3 in the development of the murine cardiac neural crest. Development 129:527-538.
42. LaBonne C, Bronner-Fraser M. 1998. Neural crest induction in Xenopus: evidence for a two-signal model. Development 125:2403-2414.
43. Lee R, Luo J, Evans R, Giguere V, Sucov H. 1997. Compartment-selective sensitivity of cardiovascular morphogenesis to combinations of retinoic acid receptor gene mutations. Circ Res 80:757-764.
44. LeLievre C, Le Douarin N. 1975. Mesenchymal derivatives of the neural crest: analysis of chimeric quail and chick embryos. J Embryol Exp Morphol 134:125-154.
45. Li J, Liu K, Jin F, Lu M, Epstein J. 1999. Transgenic rescue of congenital heart disease and spina bifida in Splotch mice. Development 126:2495-2503.
46. Li J, Han X, Jiang J, Zhong R, Williams G, Pickering J, Chow L. 2001. Vascular smooth muscle cells of recipient origin mediate intimal expansion after aortic allotransplantation in mice. Am J Pathol 158:1943-1947.
47. Lindahl P, Johansson B, Leveen P, Betsholtz C. 1997. Pericyte loss and microanerysm formation in PDGF-B-deficient mice. Science 277:242-245.
48. Lindahl P, Hellstrom M, Kalen M, Betsholtz C. 1998. Endothelial-perivascular cell signaling in vascular development: lessons from knockout mice. Curr Opin Lipidol 9:407-411.
49. Lindsay E, Vitelli F, Su H, Morishima M, Huynh T, Pramparo T, Jurecic V, Orgurinu G, Sutherland H, Scambler P, Bradley A, Baldini A. 2001. Tbx1 haploinsufficiency in the DiGeorge syndrome region causes aortic arch defects in mice. Nature 410:97-101.
50. Liu C, Liu W, Palie J, Lu M, Brown N, Martin J. 2002. Pitx2c patterns anterior myocardium and aortic arch vessels and is required for local cell movement into atrioventricular cushions. Development 129:5081-5091.
51. Majesky M, Schwartz S. 1997. An origin for smooth muscle from endothelium? Circ Res 80:601-603.
52. Majka S, Jackson K, Kienstra K, Majesky M, Goodell M, Hirschi K. 2003. Distinct progenitor populations in skeletal muscle are bone marrow derived and exhibit different cell fates during vascular regeneration. J Clin Invest 111:71-79.
53. Manasek F. 1969. Embryonic development of the heart II. Formation of the epicardium. J Embryol Exp Morphol 22:333-348.
54. Mendelsohn C, Lohnes D, Decimo D, Lufkin T, LeMeur M, Chambon P, Mark M. 1994. Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120:2749-2771.
55. Mikawa T, Fischman D. 1992. Retroviral analysis of cardiac morphogenesis: discontinuous formation of coronary vessels. Proc Natl Acad Sci USA 89:9504-9508.
56. Mikawa T, Gourdie R. 1996. Pericardial mesoderm generates a population of coronary smooth muscle cells migrating into the heart along with ingrowth of the epicardial organ. Dev Biol 174:221-232.
57. Millino C, Sarinella F, Tiveron C, Villa A, Sartore S, Ausoni S. 2000. Cardiac and smooth muscle cell contribution to the formation of the murine pulmonary veins. Dev Dyn 218:414-425.
58. Morrison S, Perez S, Qiao Z, Verdi J, Hicks C, Weinmaster G, Anderson D. 2000. Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101:499-510.
59. Morrison-Graham K, Schatteman G, Bork T, Bowen-Pope D, Weston J. 1992. A PDGF receptor mutation in the mouse (Patch) perturbs the development of a non-neuronal subset of neural crest-derived cells. Development 115:133-142.
60. Motoike T, Markham D, Rossant J, Sato T. 2003. Evidence for novel fate of Flk1+ progenitor: contribution to muscle lineage. Genesis 35:153-159.
61. Munoz-Chapuli R, Perez-Pomares J, Macias D, Garcia-Garrido L, Carmona R, Gonzalez M. 1999. Differentiation of hemangioblasts from embryonic mesothelial cells? A model of the origin of the vertebrate cardiovascular system. Differentiation 64:133-141.
62. Niederreither K, Vermot J, Messaddeq N, Schuhbaur B, Chambon P, Dolle P. 2001. Embryonic retinoic acid synthesis is essential for heart morphogenesis in the mouse. Development 128:1019-1031.
63. Orr-Urtreger A, Lonai P. 1992. Platelet-derived growth factor-A and its receptor are expressed in separate, but adjacent cell layers of the mouse embryo. Development 115:1045-1058.
64. Paranya G, Vineberg S, Dvorin E, Kaushal S, Roth S, Rabkin E, Schoen F, Bischoff J. 2001. Aortic valve endothelial cells undergo transforming growth factor-beta-mediated and non-transforming growth factor-beta-mediated transdifferentiation in vitro. Am J Pathol 159:1335-1343.
65. Petersen P, Zou K, Hwang J, Jan Y, Zhong W. 2002. Progenitor cell maintenance requires numb and numblike during mouse neurogenesis. Nature 419:929-934.
66. Phillips M, Waldo K, Kirby M. 1989. Neural crest ablation does not alter pulmonary vein development in the chick embryo. Anat Rec 223:292-298.
67. Rhyu M, Jan L, Jan Y. 1994. Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 76:477-491.
68. Rosenquist T, Kirby M, van Mierop L. 1989. Solitary aortic arch artery. A result of surgical ablation of cardiac neural crest and nodose placode in the avian embryo. Circulation 80:1469-1475.
69. Rosenquist T, Beall A. 1990. Elastogenic cells in the developing cardiovascular system: smooth muscle, nonmuscle and cardiac neural crest. Ann NY Acad Sci 588:106-119.
70. Saiura A, Sata M, Hirata Y, Nagai R, Makuuchi M. 2001. Circulating smooth muscle progenitor cells contribute to atherosclerosis. Nat Med 7:382-383.
71. Sasai Y, De Robertis E. 1997. Ectodermal patterning in vertebrate embryos. Dev Biol 182:5-20.
72. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R. 2002. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med 8:403-409.
73. Schatteman G, Motley S, Effmann E, Bowen-Pope D. 1995. Platelet-derived growth factor receptor alpha subunit deleted Patch mouse exhibits severe cardiovascular dysmorphogenesis. Teratology 51:351-366.
74. Schwartz S, Benditt E. 1973. Cell replication in the aortic endothelium: a new method for study of the problem. Lab Invest 28:699-707.
75. Shah N, Groves A, Anderson D. 1996. Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell 85:331-343.
76. Shah N, Anderson D. 1997. Integration of multiple instructive cues by neural crest stem cells reveals cell-intrinsic biases in relative growth factor responsiveness. Proc Natl Acad Sci USA 94:11369-11374.
77. Shimizu K, Sugiyama S, Aikawa M, Fukumoto Y, Rabkin E, Libby P, Mitchell R. 2001. Host bone-marrow cells are a source of donor intimal smooth muscle-like cells in murine aortic transplant arteriopathy. Nat Med 7:738-741.
78. Simper D, Stalboerger P, Panetta C, Wang S, Caplice N. 2002. Smooth muscle progenitor cells in human blood. Circulation 106:1199-1204.
79. Soriano P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21:70-71.
80. Spana E, Kopczynski C, Goodman C, Doe C. 1995. Asymmetric localization of numb autonomously determines sibling neuron identity in the Drosophila CNS. Development 121:3489-3494.
81. Svensson E, Huggins G, Lin H, Clendenin C, Jiang F, Tufts R, Dardik F, Leiden J. 2000. A syndrome of tricuspid atresia in mice with a targeted mutation of the gene encoding Fog-2. Nat Genet 25:353-356.
82. Tallquist M, Soriano P. 2003. Cell autonomous requirement for PDGFRα in population of cranial and cardiac neural crest cells. Development 130:507-518.
83. Tevosian S, Deconinck A, Tanaka M, Schinke M, Litvosky S, Izumo S, Fujiwara Y, Orkin S. 2000. FOG-2, a cofactor for GATA transcription factors, is essential for heart morphogenesis and development of coronary vessels from epicardium. Cell 101:729-739.
84. Thomas T, Kurihara H, Yamagishi H, Kurihara Y, Yazaki Y, Olson E, Srivastava D. 1998. A signaling cascade involving endothelin-1, dHAND and msx1 regulates development of neural-crest-derived branchial arch mesenchyme. Development 125:3005-3014.
85. Vitelli F, Morishima M, Taddei I, Lindsay E, Baldini A. 2002a. Tbx1 mutation causes multiple cardiovascular defects and disrupts neural crest and cranial nerve migratory pathways. Hum Mol Genet 11:915-922.
86. Vitelli F, Taddei I, Morishima M, Meyers E, Lindsay E, Baldini A. 2002b. A genetic link between Tbx1 and fibroblast growth factor signaling. Development 129:4605-4611.
87. White P, Morrison S, Orimoto K, Kubu C, Verdi J, Anderson D. 2001. Neural crest stem cells undergo cell-intrinsic developmental changes in sensitivity to instructive differentiation signals. Neuron 29:57-71.
88. Wu J, Saint-Jeannet J, Klein P. 2003. Wnt-frizzled signaling in neural crest formation. Trends Neurosci 26:40-45.
89. Xu X, Li W, Huang G, Meyer R, Chen T, Luo Y, Thomas M, Radice G, Lo C. 2001. Modulation of mouse neural crest cell motility by N-cadherin and connexin 43 gap junctions. J Cell Biol 154:217-230.
90. Yamagishi H, Maeda J, Hu T, McAnally J, Conway S, Kume T, Meyers E, Yamagishi C, Srivastava D. 2003. Tbx1 is regulated by tissue-specific forkhead proteins through a common Sonic hedge-hog-responsive enhancer. Genes Dev 17:269-281.
91. Yamashita J, Itoh H, Hirashima M, Ogawa M, Nishikawa S, Yurugi T, Naito M, Nakao K, Nishikawa S. 2000. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 408:92-96.
92. Yanagisawa H, Hammer R, Richardson J, Williams S, Clouthier D, Yanagisawa M. 1998. Role of endothelin-1/endothelin-A receptor-mediated signaling pathway in the aortic arch patterning in mice. J Clin Invest 102:22-33.
93. Yanagisawa H, Hammer R, Richardson J, Emoto N, Williams S, Takeda S, Clouthier D, Yanagisawa M. 2000. Disruption of ECE-1 and ECE-2 reveals a role for endothelin-converting enzyme-2 in murine cardiac development. J Clin Invest 105:1373-1382.