Smooth muscle cell differentiation in vitro: Models and underlying molecular mechanisms

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 7, 2011, Pages 1485-1494

  Xie, Changqing ^a   Ritchie, Raquel P ^a   Huang, Huarong ^a   Zhang, Jifeng ^a   Chen, Y Eugene ^a,b  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b NONE   (United States)

Author keywords

vascular biology; vascular muscle

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CALPONIN; HISTONE DEACETYLASE; MESSENGER RNA; MICRORNA; MYOCARDIN; MYOSIN HEAVY CHAIN; RETINOIC ACID; RETINOIC ACID RECEPTOR;

ANIMAL CELL CULTURE; CELL ADHESION; CELL PROLIFERATION; CELL SELECTION; CELL STRAIN; CELL STRAIN A404; CELL STRAIN C3H 10T1 2; CELL STRAIN JOMA1; CELL STRAIN MONC 1; CELL STRAIN P19; CULTURE MEDIUM; EMBRYOID BODY; EMBRYONAL CARCINOMA STEM CELL; EMBRYONIC STEM CELL; EPIGENETICS; EXTRACELLULAR MATRIX; HUMAN; IN VITRO STUDY; INTRACELLULAR SIGNALING; MOLECULAR MODEL; MONOLAYER CULTURE; NEURAL CREST CELL; NEURAL STEM CELL; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; RECEPTOR BINDING; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PHENOTYPE; SIGNAL TRANSDUCTION;

EID: 79959698368     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.110.221101     Document Type: Review

References (102)

1. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev. 2004;84:767-801. (Pubitemid 38823766)
2. Majesky MW. Developmental basis of vascular smooth muscle diversity. Arterioscler Thromb Vasc Biol. 2007;27:1248-1258. (Pubitemid 46809412)
3. Yoshida T, Owens GK. Molecular determinants of vascular smooth muscle cell diversity. Circ Res. 2005;96:280-291. (Pubitemid 40279902)
4. Hirschi KK, Rohovsky SA, D'Amore PA. PDGF, TGF-β, 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. (Pubitemid 28217923)
5. Jain MK, Layne MD, Watanabe M, Chin MT, Feinberg MW, Sibinga NE, Hsieh CM, Yet SF, Stemple DL, Lee ME. In vitro system for differentiating pluripotent neural crest cells into smooth muscle cells. J Biol Chem. 1998;273:5993-5996. (Pubitemid 28144672)
6. Manabe I, Owens GK. Recruitment of serum response factor and hyperacetylation of histones at smooth muscle-specific regulatory regions during differentiation of a novel P19-derived in vitro smooth muscle differentiation system. Circ Res. 2001;88:1127-1134. (Pubitemid 34132512)
7. Adams B, Xiao Q, Xu Q. Stem cell therapy for vascular disease. Trends Cardiovasc Med. 2007;17:246-251. (Pubitemid 47532730)
8. McBurney MWP. 19 embryonal carcinoma cells. Int J Dev Biol. 1993; 37:135-140.
9. McBurney MW, Rogers BJ. Isolation of male embryonal carcinoma cells and their chromosome replication patterns. Dev Biol. 1982;89: 503-508. (Pubitemid 12154110)
10. Rudnicki MA, Sawtell NM, Reuhl KR, Berg R, Craig JC, Jardine K, Lessard JL, McBurney MW. Smooth muscle actin expression during P19 embryonal carcinoma differentiation in cell culture. J Cell Physiol. 1990;142:89-98.
11. Blank RS, Swartz EA, Thompson MM, Olson EN, Owens GK. A retinoic acid-induced clonal cell line derived from multipotential P19 embryonal carcinoma cells expresses smooth muscle characteristics. Circ Res. 1995;76:742-749.
12. Spin JM, Nallamshetty S, Tabibiazar R, Ashley EA, King JY, Chen M, Tsao PS, Quertermous T. Transcriptional profiling of in vitro smooth muscle cell differentiation identifies specific patterns of gene and pathway activation. Physiol Genomics. 2004;19:292-302. (Pubitemid 40039935)
13. Chen J, Kitchen CM, Streb JW, Miano JM. Myocardin: a component of a molecular switch for smooth muscle differentiation. J Mol Cell Cardiol. 2002;34:1345-1356. (Pubitemid 35244412)
14. Yoshida T, Sinha S, Dandre F, Wamhoff BR, Hoofnagle MH, Kremer BE, Wang DZ, Olson EN, Owens GK. Myocardin is a key regulator of CArG-dependent transcription of multiple smooth muscle marker genes. Circ Res. 2003;92:856-864. (Pubitemid 36542526)
15. Miano JM, Cserjesi P, Ligon KL, Periasamy M, Olson EN. Smooth muscle myosin heavy chain exclusively marks the smooth muscle lineage during mouse embryogenesis. Circ Res. 1994;75:803-812. (Pubitemid 24323513)
16. Owens GK. Regulation of differentiation of vascular smooth muscle cells. Physiol Rev. 1995;75:487-517.
17. Martin GR, Evans MJ. Differentiation of clonal lines of teratocarcinoma cells: formation of embryoid bodies in vitro. Proc Natl Acad Sci USA. 1975;72:1441-1445.
18. Bratt-Leal AM, Carpenedo RL, McDevitt TC. Engineering the embryoid body microenvironment to direct embryonic stem cell differentiation. Biotechnology Progress. 2009;25:43-51.
19. Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol. 1985;87:27-45. (Pubitemid 15029925)
20. Drab M, Haller H, Bychkov R, Erdmann B, Lindschau C, Haase H, Morano I, Luft FC, Wobus AM. From totipotent embryonic stem cells to spontaneously contracting smooth muscle cells: a retinoic acid and db-cAMP in vitro differentiation model. FASEB J. 1997;11:905-915. (Pubitemid 27371900)
21. Sinha S, Hoofnagle MH, Kingston PA, McCanna ME, Owens GK. Transforming growth factor-β1 signaling contributes to development of smooth muscle cells from embryonic stem cells. Am J Physiol Cell Physiol. 2004;287:C1560- C1568. (Pubitemid 39507673)
22. Sinha S, Wamhoff BR, Hoofnagle MH, Thomas J, Neppl RL, Deering T, Helmke BP, Bowles DK, Somlyo AV, Owens GK. Assessment of contractility of purified smooth muscle cells derived from embryonic stem cells. Stem Cells. 2006;24:1678-1688. (Pubitemid 44474181)
23. Ferreira LS, Gerecht S, Shieh HF, Watson N, Rupnick MA, Dallabrida SM, Vunjak-Novakovic G, Langer R. Vascular progenitor cells isolated from human embryonic stem cells give rise to endothelial and smooth muscle like cells and form vascular networks in vivo. Circ Res. 2007; 101:286-294. (Pubitemid 47344078)
24. Xie CQ, Zhang J, Villacorta L, Cui T, Huang H, Chen YE. A highly efficient method to differentiate smooth muscle cells from human embryonic stem cells. Arterioscler Thromb Vasc Biol. 2007;27:e311-e312. (Pubitemid 350158939)
25. Nishikawa S, Jakt LM, Era T. Embryonic stem-cell culture as a tool for developmental cell biology. Nat Rev Mol Cell Biol. 2007;8:502-507. (Pubitemid 46809158)
26. Rathjen J, Rathjen PD. Mouse ES cells: experimental exploitation of pluripotent differentiation potential. Curr Opin Genet Dev. 2001;11: 587-594. (Pubitemid 32800735)
27. Huang H, Zhao X, Chen L, Xu C, Yao X, Lu Y, Dai L, Zhang M. Differentiation of human embryonic stem cells into smooth muscle cells in adherent monolayer culture. Biochem Biophys Res Commun. 2006; 351:321-327. (Pubitemid 44666692)
28. Xie CQ, Huang H, Wei S, Song LS, Zhang J, Ritchie RP, Chen L, Zhang M, Chen YE. A comparison of murine smooth muscle cells generated from embryonic versus induced pluripotent stem cells. Stem Cells Dev. 2009;18:741-748.
29. Xiao Q, Zeng L, Zhang Z, Hu Y, Xu Q. Stem cell-derived Sca-1+ progenitors differentiate into smooth muscle cells, which is mediated by collagen IV-integrinα1/β1/αv and PDGF receptor pathways. Am J Physiol Cell Physiol. 2007;292:C342-C352. (Pubitemid 46127310)
30. Xiao Q, Zeng L, Zhang Z, Margariti A, Ali ZA, Channon KM, Xu Q, Hu Y. Sca-1+ progenitors derived from embryonic stem cells differentiate into endothelial cells capable of vascular repair after arterial injury. Arterioscler Thromb Vasc Biol. 2006;26:2244-2251. (Pubitemid 44465718)
31. Reznikoff CA, Brankow DW, Heidelberger C. Establishment and characterization of a cloned line of C3H mouse embryo cells sensitive to postconfluence inhibition of division. Cancer Res. 1973;33: 3231-3238.
32. Brunelli S, Tagliafico E, De Angelis FG, Tonlorenzi R, Baesso S, Ferrari S, Niinobe M, Yoshikawa K, Schwartz RJ, Bozzoni I, Cossu G. Msx2 and necdin combined activities are required for smooth muscle differentiation in mesoangioblast stem cells. Circ Res. 2004;94:1571-1578. (Pubitemid 38856964)
33. Rao MS, Anderson DJ. Immortalization and controlled in vitro differentiation of murine multipotent neural crest stem cells. J Neurobiol. 1997;32:722-746. (Pubitemid 27250904)
34. Chen S, Lechleider RJ. Transforming growth factor-β-induced differentiation of smooth muscle from a neural crest stem cell line. Circ Res. 2004;94:1195-1202. (Pubitemid 38656406)
35. van der Loop FT, Schaart G, Timmer ED, Ramaekers FC, van Eys GJ. Smoothelin, a novel cytoskeletal protein specific for smooth muscle cells. J Cell Biol. 1996;134:401-411. (Pubitemid 26250708)
36. van Eys GJ, Voller MC, Timmer ED, Wehrens XH, Small JV, Schalken JA, Ramaekers FC, van der Loop FT. Smoothelin expression characteristics: development of a smooth muscle cell in vitro system and identification of a vascular variant. Cell Struct Funct. 1997;22:65-72. (Pubitemid 27223247)
37. Stemple DL, Anderson DJ. Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell. 1992;71:973-985.
38. Maurer J, Fuchs S, Jager R, Kurz B, Sommer L, Schorle H. Establishment and controlled differentiation of neural crest stem cell lines using conditional transgenesis. Differentiation. 2007;75:580-591. (Pubitemid 47301600)
39. Suzuki S, Narita Y, Yamawaki A, Murase Y, Satake M, Mutsuga M, Okamoto H, Kagami H, Ueda M, Ueda Y. Effects of extracellular matrix on differentiation of human bone marrow-derived mesenchymal stem cells into smooth muscle cell lineage: utility for cardiovascular tissue engineering. Cells Tissues Organs. 2010;191:269-280.
40. Qiu P, Ritchie RP, Fu Z, Cao D, Cumming J, Miano JM, Wang DZ, Li HJ, Li L. Myocardin enhances Smad3-mediated transforming growth factor-β1 signaling in a CArG box-independent manner: Smad-binding element is an important cis element for SM22α transcription in vivo. Circ Res. 2005;97:983-991. (Pubitemid 41668911)
41. Kurpinski K, Lam H, Chu J, Wang A, Kim A, Tsay E, Agrawal S, Schaffer DV, Li S. Transforming growth factor-β and notch signaling mediate stem cell differentiation into smooth muscle cells. Stem Cells. 2010;28:734-742.
42. Xiao Q, Luo Z, Pepe AE, Margariti A, Zeng L, Xu Q. Embryonic stem cell differentiation into smooth muscle cells is mediated by Nox4-produced H2O2. Am J Physiol Cell Physiol. 2009;296:C711-C723.
43. Pepe AE, Xiao Q, Zampetaki A, Zhang Z, Kobayashi A, Hu Y, Xu Q. Crucial role of nrf3 in smooth muscle cell differentiation from stem cells. Circ Res. 2010;106:870-879.
44. Shang Y, Yoshida T, Amendt BA, Martin JF, Owens GK. Pitx2 is functionally important in the early stages of vascular smooth muscle cell differentiation. J Cell Biol. 2008;181:461-473. (Pubitemid 351645036)
45. Kawai-Kowase K, Kumar MS, Hoofnagle MH, Yoshida T, Owens GK. PIAS1 activates the expression of smooth muscle cell differentiation marker genes by interacting with serum response factor and class I basic helix-loop-helix proteins. Mol Cell Biol. 2005;25:8009-8023. (Pubitemid 41262995)
46. Colbert MC. Retinoids and cardiovascular developmental defects. Cardiovasc Toxicol. 2002;2:25-39. (Pubitemid 37070570)
47. Gudas LJ, Wagner JA. Retinoids regulate stem cell differentiation. J Cell Physiol. 2011;226:322-330.
48. Li G, Margueron R, Hu G, Stokes D, Wang YH, Reinberg D. Highly compacted chromatin formed in vitro reflects the dynamics of transcription activation in vivo. Mol Cell. 2010;38:41-53.
49. Schoenfelder S, Sexton T, Chakalova L, Cope NF, Horton A, Andrews S, Kurukuti S, Mitchell JA, Umlauf D, Dimitrova DS, Eskiw CH, Luo Y, Wei CL, Ruan Y, Bieker JJ, Fraser P. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet. 2010;42:53-61.
50. Mongan NP, Gudas LJ. Diverse actions of retinoid receptors in cancer prevention and treatment. Differentiation. 2007;75:853-870. (Pubitemid 350086170)
51. Colbert MC, Kirby ML, Robbins J. Endogenous retinoic acid signaling colocalizes with advanced expression of the adult smooth muscle myosin heavy chain isoform during development of the ductus arteriosus. Circ Res. 1996;78:790-798. (Pubitemid 26131362)
52. Kastner P, Grondona JM, Mark M, Gansmuller A, LeMeur M, Decimo D, Vonesch JL, Dolle P, Chambon P. Genetic analysis of RXRα developmental function: convergence of RXR and RAR signaling pathways in heart and eye morphogenesis. Cell. 1994;78:987-1003.
53. Sucov HM, Dyson E, Gumeringer CL, Price J, Chien KR, Evans RM. RXRα mutant mice establish a genetic basis for vitamin A signaling in heart morphogenesis. Genes Dev. 1994;8:1007-1018.
54. Krezel W, Dupe V, Mark M, Dierich A, Kastner P, Chambon P. RXRα null mice are apparently normal and compound RXRα+/-/RXRβ-/-/ RXRγ-/-mutant mice are viable. Proc Natl Acad Sci USA. 1996;93: 9010-9014.
55. Suzuki T, Kim HS, Kurabayashi M, Hamada H, Fujii H, Aikawa M, Watanabe M, Watanabe N, Sakomura Y, Yazaki Y, Nagai R. Preferential differentiation of P19 mouse embryonal carcinoma cells into smooth muscle cells: use of retinoic acid and antisense against the central nervous system-specific POU transcription factor Brn-2. Circ Res. 1996;78:395-404.
56. Yao CC, Breuss J, Pytela R, Kramer RH. Functional expression of the α7 integrin receptor in differentiated smooth muscle cells. J Cell Sci. 1997;110:1477-1487. (Pubitemid 27326666)
57. Huang H, Xie C, Sun X, Ritchie RP, Zhang J, Chen YE. miR-10a contributes to retinoid acid-induced smooth muscle cell differentiation. J Biol Chem. 2010;285:9383-9389.
58. Xie C, Huang H, Sun X, Guo Y, Hamblin M, Ritchie RP, Garcia-Barrio MT, Zhang J, Chen YE. MicroRNA-1 regulates smooth muscle cell differentiation by repressing Kruppel-like factor 4. Stem Cells Dev. 2011;20:205-210.
59. Wiblin AE, Cui W, Clark AJ, Bickmore WA. Distinctive nuclear organisation of centromeres and regions involved in pluripotency in human embryonic stem cells. J Cell Sci. 2005;118:3861-3868. (Pubitemid 41410270)
60. Schones DE, Zhao K. Genome-wide approaches to studying chromatin modifications. Nat Rev Genet. 2008;9:179-191. (Pubitemid 351271798)
61. Duncan EM, Muratore-Schroeder TL, Cook RG, Garcia BA, Shabanowitz J, Hunt DF, Allis CD. Cathepsin L proteolytically processes histone H3 during mouse embryonic stem cell differentiation. Cell. 2008;135:284-294.
62. Jackson M, Krassowska A, Gilbert N, Chevassut T, Forrester L, Ansell J, Ramsahoye B. Severe global DNA hypomethylation blocks differentiation and induces histone hyperacetylation in embryonic stem cells. Mol Cell Biol. 2004;24:8862-8871. (Pubitemid 39313892)
63. Agger K, Cloos PA, Christensen J, Pasini D, Rose S, Rappsilber J, Issaeva I, Canaani E, Salcini AE, Helin K. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature. 2007;449:731-734. (Pubitemid 47552088)
64. Gillespie RF, Gudas LJ. Retinoid regulated association of transcriptional co-regulators and the polycomb group protein SUZ12 with the retinoic acid response elements of Hoxa1, RARβ(2), and Cyp26A1 in F9 embryonal carcinoma cells. J Mol Biol. 2007;372:298-316. (Pubitemid 47267961)
65. Kashyap V, Gudas LJ. Epigenetic regulatory mechanisms distinguish retinoic acid-mediated transcriptional responses in stem cells and fibroblasts. J Biol Chem. 2010;285:14534-14548.
66. Azuara V, Perry P, Sauer S, Spivakov M, Jorgensen HF, John RM, Gouti M, Casanova M, Warnes G, Merkenschlager M, Fisher AG. Chromatin signatures of pluripotent cell lines. Nat Cell Biol. 2006;8: 532-538.
67. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006;125:315-326.
68. McDonald OG, Wamhoff BR, Hoofnagle MH, Owens GK. Control of SRF binding to CArG box chromatin regulates smooth muscle gene expression in vivo. J Clin Invest. 2006;116:36-48. (Pubitemid 43121789)
69. Wang Z, Wang DZ, Pipes GC, Olson EN. Myocardin is a master regulator of smooth muscle gene expression. Proc Natl Acad Sci USA. 2003;100:7129-7134. (Pubitemid 36706404)
70. Illi B, Scopece A, Nanni S, Farsetti A, Morgante L, Biglioli P, Capogrossi MC, Gaetano C. Epigenetic histone modification and cardiovascular lineage programming in mouse embryonic stem cells exposed to laminar shear stress. Circ Res. 2005;96:501-508. (Pubitemid 40463458)
71. Spin JM, Quertermous T, Tsao PS. Chromatin remodeling pathways in smooth muscle cell differentiation, and evidence for an integral role for p300. PLoS One. 2010;5:e14301.
72. Zampetaki A, Zeng L, Xiao Q, Margariti A, Hu Y, Xu Q. Lacking cytokine production in ES cells and ES-cell-derived vascular cells stimulated by TNF-α is rescued by HDAC inhibitor trichostatin A. Am J Physiol Cell Physiol. 2007;293:C1226-C1238. (Pubitemid 47556736)
73. Margariti A, Xiao Q, Zampetaki A, Zhang Z, Li H, Martin D, Hu Y, Zeng L, Xu Q. Splicing of HDAC7 modulates the SRF-myocardin complex during stem-cell differentiation towards smooth muscle cells. J Cell Sci. 2009;122:460-470.
74. Yoshida T, Gan Q, Owens GK. Kruppel-like factor 4, Elk-1, and histone deacetylases cooperatively suppress smooth muscle cell differentiation markers in response to oxidized phospholipids. Am J Physiol Cell Physiol. 2008;295:C1175-C1182. (Pubitemid 352790337)
75. Cao D, Wang Z, Zhang CL, Oh J, Xing W, Li S, Richardson JA, Wang DZ, Olson EN. Modulation of smooth muscle gene expression by association of histone acetyltransferases and deacetylases with myocardin. Mol Cell Biol. 2005;25:364-376. (Pubitemid 40039826)
76. Dressel U, Bailey PJ, Wang SC, Downes M, Evans RM, Muscat GE. A dynamic role for HDAC7 in MEF2-mediated muscle differentiation. J Biol Chem. 2001;276:17007-17013.
77. Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: stem cells and their niche. Cell. 2004;116:769-778. (Pubitemid 38410723)
78. Walker MR, Patel KK, Stappenbeck TS. The stem cell niche. J Pathol. 2009;217:169-180.
79. Poschl E, Schlotzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, Mayer U. Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development. 2004;131:1619-1628. (Pubitemid 38559288)
80. Behonick DJ, Werb Z. A bit of give and take: the relationship between the extracellular matrix and the developing chondrocyte. Mech Dev. 2003;120:1327-1336. (Pubitemid 37421166)
81. Chen SS, Revoltella RP, Papini S, Michelini M, Fitzgerald W, Zimmerberg J, Margolis L. Multilineage differentiation of rhesus monkey embryonic stem cells in three-dimensional culture systems. Stem Cells. 2003;21:281-295. (Pubitemid 36623170)
82. Hu J, Sun X, Ma H, Xie C, Chen YE, Ma PX. Porous nanofibrous PLLA scaffolds for vascular tissue engineering. Biomaterials. 2010;31: 7971-7977.
83. Sone M, Itoh H, Yamahara K, Yamashita JK, Yurugi-Kobayashi T, Nonoguchi A, Suzuki Y, Chao TH, Sawada N, Fukunaga Y, Miyashita K, Park K, Oyamada N, Taura D, Tamura N, Kondo Y, Nito S, Suemori H, Nakatsuji N, Nishikawa S, Nakao K. Pathway for differentiation of human embryonic stem cells to vascular cell components and their potential for vascular regeneration. Arterioscler Thromb Vasc Biol. 2007;27:2127-2134. (Pubitemid 350287240)
84. Rana TM. Illuminating the silence: understanding the structure and function of small RNAs. Nat Rev Mol Cell Biol. 2007;8:23-36. (Pubitemid 46012012)
85. Schickel R, Boyerinas B, Park SM, Peter ME. MicroRNAs: key players in the immune system, differentiation, tumorigenesis and cell death. Oncogene. 2008;27:5959-5974.
86. Guo H, Ingolia NT, Weissman JS, Bartel DP. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature. 2010;466: 835-840.
87. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature. 2005;433:769-773. (Pubitemid 40292988)
88. Hutvagner G, Zamore PD. A microRNA in a multiple-turnover RNAi enzyme complex. Science. 2002;297:2056-2060.
89. Cheng Y, Liu X, Yang J, Lin Y, Xu DZ, Lu Q, Deitch EA, Huo Y, Delphin ES, Zhang C. MicroRNA-145, a novel smooth muscle cell phenotypic marker and modulator, controls vascular neointimal lesion formation. Circ Res. 2009;105:158-166.
90. Cordes KR, Sheehy NT, White MP, Berry EC, Morton SU, Muth AN, Lee TH, Miano JM, Ivey KN, Srivastava D. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature. 2009;460:705-710.
91. Boettger T, Beetz N, Kostin S, Schneider J, Kruger M, Hein L, Braun T. Acquisition of the contractile phenotype by murine arterial smooth muscle cells depends on the Mir143/145 gene cluster. J Clin Invest. 2009;119:2634-2647.
92. Elia L, Quintavalle M, Zhang J, Contu R, Cossu L, Latronico MV, Peterson KL, Indolfi C, Catalucci D, Chen J, Courtneidge SA, Condorelli G. The knockout of miR-143 and-145 alters smooth muscle cell maintenance and vascular homeostasis in mice: correlates with human disease. Cell Death Differ. 2009;16:1590-1598.
93. Xin M, Small EM, Sutherland LB, Qi X, McAnally J, Plato CF, Richardson JA, Bassel-Duby R, Olson EN. MicroRNAs miR-143 and miR-145 modulate cytoskeletal dynamics and responsiveness of smooth muscle cells to injury. Genes Dev. 2009;23:2166-2178.
94. Albinsson S, Suarez Y, Skoura A, Offermanns S, Miano JM, Sessa WC. MicroRNAs are necessary for vascular smooth muscle growth, differentiation, and function. Arterioscler Thromb Vasc Biol. 2010;30:1118-1126.
95. Jiang X, Rowitch DH, Soriano P, McMahon AP, Sucov HM. Fate of the mammalian cardiac neural crest. Development. 2000;127:1607-1616. (Pubitemid 30234918)
96. Nakamura T, Colbert MC, Robbins J. Neural crest cells retain multipotential characteristics in the developing valves and label the cardiac conduction system. Circ Res. 2006;98:1547-1554. (Pubitemid 44297078)
97. Mikawa T, Fischman DA. Retroviral analysis of cardiac morphogenesis: discontinuous formation of coronary vessels. Proc Natl Acad Sci USA. 1992;89:9504-9508.
98. Wilm B, Ipenberg A, Hastie ND, Burch JB, Bader DM. The serosal mesothelium is a major source of smooth muscle cells of the gut vasculature. Development. 2005;132:5317-5328. (Pubitemid 43020185)
99. Maeda J, Yamagishi H, McAnally J, Yamagishi C, Srivastava D. Tbx1 is regulated by forkhead proteins in the secondary heart field. Dev Dyn. 2006;235:701-710.
100. Waldo KL, Hutson MR, Ward CC, Zdanowicz M, Stadt HA, Kumiski D, Abu-Issa R, Kirby ML. Secondary heart field contributes myocardium and smooth muscle to the arterial pole of the developing heart. Dev Biol. 2005;281:78-90. (Pubitemid 40558724)
101. Esner M, Meilhac SM, Relaix F, Nicolas JF, Cossu G, Buckingham ME. Smooth muscle of the dorsal aorta shares a common clonal origin with skeletal muscle of the myotome. Development. 2006;133: 737-749.
102. Pouget C, Gautier R, Teillet MA, Jaffredo T. Somite-derived cells replace ventral aortic hemangioblasts and provide aortic smooth muscle cells of the trunk. Development. 2006;133:1013-1022.