Abstract
Three principal muscle types have evolved in essentially all vertebrate species to carry out functions related to cellular contraction. Traditionally, the three muscle types — cardiac, skeletal and smooth — have been distinguished by their unique structural and functional attributes. In recent years, great strides have been made with respect to the molecular characteristics of each muscle type and the regulatory pathways and factors governing muscle cell lineage determination and differentiation. This is especially true with skeletal and cardiac muscle where several transcription factors have been assigned critical roles in orchestrating developmental programmes unique to these two sarcomeric muscle types. The myogenic regulatory factors in skeletal muscle (myf5, MyoD, myogenin, and MRF4) have, indeed, formed the basis of a paradigm of cellular differentiation (Olson 1990). This paradigm has subsequently been extended to cardiac muscle where related transcription factors (e.g., dHAND) have been cloned and shown, through genetic means, to be essential for normal cardiogenesis (Olson and Srivastava 1996). The relative ease in which progress has been made with the two sarcomeric muscle types probably reflects their wellcircumscribed points of origin and their terminal differentiation.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Aikawa M, Sivam PN, Kuro M, Kimura K, Nakahara K, Takewaki S, Ueda M, Yamaguchi H, Yazaki Y, Periasamy M, Nagai R (1993) Human smooth muscle myosin heavy chain gene isoforms as molecular markers for vascular development and atherosclerosis. Circ Res 73: 1000–1012
Aikawa M, Sakomura Y, Ueda M, Kimura K, Manabe I, Ishiwata S, Komiyama N, Yamaguchi H, Yazaki Y, Nagai R (1997) Redifferentiation of smooth muscle cells after coronary angioplasty determined via myosin heavy chain expression. Circulation 96: 82–90
Almendral JM, Santaren JF, Perera J, Zerial M, Bravo R (1989) Expression, cloning and cDNA sequence of a fibroblast serum-regulated gene encoding a putative actin-associated protein (p27). Exp Cell Res 181: 518–530
Andrés V, Fisher S, Wearsch P, Walsh K (1995) Regulation of Gax homeobox gene transcription by a combination of positive factors including myocyte-specific enhancer factor 2. Mol Cell Biol 15: 4272–4281
Applegate D, Feng W, Green RS, Taubman MB (1994) Cloning and expression of a novel acidic calponin isoform from rat aortic vascular smooth muscle. J Biol Chem 269: 10683–10690
Arciniegas E, Sutton AB, Allen TD, Schor AM (1992) Transforming growth factor beta 1 promotes the differentiation of endothelial cells into smooth muscle cells in vitro. J Cell Sci 103: 521–529
Arciniegas E, Ponce L, Hartt Y, Graterol A, Carlini RG (2000) Intimal thickening involves trans-differentiation of embryonic endothelial cells. Anat Rec 258: 47–57
Babij P (1993) Tissue-specific and developmentally regulated alternative splicing of a visceral isoform of smooth muscle myosin heavy chain. Nucleic Acids Res 21: 1467–1471
Belaguli NS, Zhou W, Trinh T-HT, Majesky MW, Schwartz RJ (1999) Dominant negative murine serum response factor: alternative splicing within the activation domain inhibits transactivation of serum response factor binding targets. Mol Cell Biol 19: 4582–4591
Belknap JK, Grieshaber NA, Schwartz PE, Orton EC, Reidy MA, Majack RA (1996) Tropoelastin gene expression in individual vascular smooth muscle cells: relationship to DNA synthesis during vascular development and after arterial injury. Circ Res 78: 388–394
Bergwerff M, Verberne ME, DeRuiter MC, Poelmann RE, Gittenberger-de Groot AC (1998) Neural crest cell contribution to the developing circulatory system: implications for vascular morphology Circ Res 82: 221–231
Bevan JA (1979) Sites of transition between functional systemic and cerebral arteries of rabbits occur at embryological junctional sites. Science 204: 635–637
Black FM, Packer SE, Parker TG, Michael LH, Roberts R, Schwartz RJ, Schneider MD (1991) The vascular smooth muscle a-actin gene is reactivated during cardiac hypertrophy provoked by load. J Clin Invest 88: 1581–1588
Blank RS, Swartz EA, Thompson MM, Olson EN, Owens GK (1995) A retinoic acid-induced clonal cell line derived from multipotential P19 embryonal carcinoma cells expresses smooth muscle characteristics. Circ Res 76: 742–749
Borrione AC, Zanellato AMC, Giuriato L, Scannapieco G, Pauletto P, Sartore S (1990) Nonmuscle and smooth muscle myosin isoforms in bovine endothelial cells. Exp Cell Res 190: 1–10
Browning CL, Culberson DE, Aragon IV, Fillmore RA, Croissant JD, Schwartz RJ, Zimmer WE (1998) The developmentally regulated expression of serum response factor plays a key role in the control of smooth muscle-specific genes. Dev Biol 194: 18–37
Cal H, Levine M (1995) Modulation of enhancer-promoter interactions by insulators in the Drosophila embryo. Nature 376: 533–536
Camoretti-Mercado B, Liu H-W, Halayko AJ, Forsythe SM, Kyle JW, Li B, Fu Y, McConville J, Kogut P, Vieira JE, Patel NM, Hershenson MB, Fuchs E, Sinha S, Miano JM, Parmacek MS, Burkhardt JK, Solway J (2000) Physiological control of smooth muscle-specific gene expression through regulated nuclear translocation of serum response factor. J Biol Chem 275: 30387–30393
Carson JA, Fillmore RA, Schwartz RJ, Zimmer WE (2000) The smooth muscle y-actin gene promoter is a molecular target for the mouse bagpipe homologue, mNkx3–1, and serum response factor. J Biol Chem 275: 39061–39072
Chamley-Campbell J, Campbell GR, Ross R (1979) The smooth muscle cell in culture. Physiol Rev 59: 1–61
Chen J, Maltby KM, Miano JM (2001) A novel retinoid-response gene set in vascular smooth muscle cells. Biochem Biophys Res Comm 281: 475–482
Chen YH, Chen YL, Lin SJ, Chou CY, Mar GY, Chang MS, Wang SP (1997) Electron microscopic studies of phenotypic modulation of smooth muscle cells in coronary arteries of patients with unstable angina pectoris and postangioplasty restenosis. Circulation 95: 1169–1175
Chin MT, Maemura K, Fukumoto S, Jain MK, Layne MD, Watanabe M, Hsieh CM, Lee ME (2000) Cardiovascular basic helix loop helix factor 1, a novel transcriptional repressor expressed preferentially in the developing and adult cardiovascular system. J Biol Chem 275: 6381–6387
DeRuiter MC, Poelmann RE, Van Munsteren JC, Mironov V, Markwald RR, Gittenberger-de Groot AC (1997) Embryonic endothelial cells transdifferentiate into mesenchymal cells expressing smooth muscle actins in vivo and in vitro. Circ Res 80: 444–451
Desmoulière A, Rubbia-Brandt L, Abdiu A, Walz T, Macieira-Coelho A, Gabbiani G (1992) a-smooth muscle actin is expressed in a subpopulation of cultured and cloned fibroblasts and is modulated by y-interferon. Exp Cell Res 201: 64–73
Drab M, Haller H, Bychkov R, Erdmann B, Lindschau C, Haase H, Morano I, Luft FC, Wobus AM (1997) From totipotent embryonic stem cells to spontaneously contracting smooth muscle cells: a retinoic acid and db-cAMP in vitro differentiation model. FASEB J 11: 905–915
Mammalian Smooth Muscle Differentiation: Origins, Markers and Transcriptional Control 53
Duband JL, Gimona M, Scatena M, Sartore S, Small JV (1993) Calponin and SM 22 as differentiation markers of smooth muscle: spatiotemporal distribution during avian embryonic development. Differentiation 55: 1–11
Eddinger TJ, Wolf JA (1993) Expression of four myosin heavy chain isoforms with development in mouse uterus. Cell Motil Cytoskeleton 25: 358–368
Ellis PD, Chen Q, Barker PJ, Metcalfe JC, Kemp PR (2000) Nov gene encodes adhesion factor for vascular smooth muscle cells and is dynamically regulated in response to vascular injury. Arterioscler Thromb Vasc Biol 20: 1912–1919
Fazio MJ, Olsen DR, Kuivaniemi H, Chu ML, Davidson JM, Rosenbloom J, Uitto J (1988) Isolation and characterization of human elastin cDNAs, and age-associated variation in elastin gene expression in cultured skin fibroblasts. Lab Invest 58: 270–277
Ferhat L, Charton G, Represa A, Ben-Ari Y, der Terrossian E, Khrestchatisky M (1996) Acidic calponin cloned from neural cells is differentially expressed during rat brain development. Eur J Neurosci 8: 1501–1509
Firulli AB, Han D, Kelly-Roloff L, Koteliansky VE, Schwartz SM, Olson EN, Miano JM (1998) A comparative molecular analysis of four rat smooth muscle cell lines. In Vitro Cell Dev Biol 34: 217–226
Fukui Y, Masuda H, Takagi M, Takahashi K, Kiyokane K (1997) The presence of h2-calponin in human keratinocyte. J Dermatol Sci 14: 29–36
Gabbiani G, Kocher O, Bloom WS, Vandekerckhove J, Weber K (1984) Actin expression in smooth muscle cells of rat aortic intimal thickening, human artheromatous plaque, and cultured rat aortic media. J Clin Invest 73: 148–152
Gallagher PG, Herring BP (1991) The carboxyl terminus of the smooth muscle myosin light chainkinase is expressed as an independent protein, telokin. J Biol Chem 266: 23945–23952
Giangola G, Migaly J, Crawford B, Moskowitz P, Sebenick M (1995) Leiomyosarcoma of the subclavian artery. J Vasc Surg 22: 496–500
Gimona M, Herzog M, Vandekerchkhove J, Small JV (1990) Smooth muscle specific expression of calponin. FEBS Lett 274: 159–162
Glukhova M, Kabakov AE, Frid MG, Ornatsky OI, Belkin AM, Mukhin DN, Orekhov AN, Koteliansky VE, Smirnov VN (1988) Modulation of human aorta smooth muscle cell phenotype: a study of muscle-specific variants of vinculin, caldesmon, and actin expression. Proc Natl Acad Sci USA 85: 9542–9546
Goodson HV (1994) Molecular evolution of the myosin superfamily: application of phylogenetic techniques to cell biological questions. Society of General Physiologists Series 49. Rockefeller University Press, New York, pp 141–157
Goodson HV, Spudich JA (1993) Molecular evolution of the myosin family: relationships derived from comparisons of amino acid sequences. Proc Natl Acad Sci USA 90: 659–663
Gorski DH, LePage DF, Patel CV, Copeland NG, Jenkins NA, Walsh K (1993) Molecular cloning of a diverged homeobox gene that is rapidly down-regulated during the Go/G, transition in vascular smooth muscle cells. Mol Cell Biol 13: 3722–3733
Graves DC, Yablonka-Reuveni Z (2000) Vascular smooth muscle cells spontaneously adopt a skeletal muscle phenotype: a unique Myf5-/MyoD’ myogenic program. J Histochem Cytochem 48: 1173–1193
Hautmann MB, Thompson MM, Swartz EA, Olson EN, Owens GK (1997) Angiotensin II-induced stimulation of smooth muscle a -actin expression by serum response factor and the homeodomain transcription factor MHox. Circ Res 81: 600–610
Henderson JR, Macalma T, Brown D, Richardson JA, Olson EN, Beckerle MC (1999) The LIM protein, CRP1, is a smooth muscle marker. Dev Dyn 214: 229–238
Herring BP, Smith AF (1996) Telokin expression is mediated by a smooth muscle cell-specific promoter. Am J Physiol 270: C1656 - C1665
Herring BP, Smith AF (1997) Telokin expression in A10 smooth muscle cells requires serum response factor. Am J Physiol 272: C1394 - C1404
Herring BP, Lyons GE, Hoggatt AM, Gallagher PG (2001) Telokin expression is restricted to smooth muscle tissues during mouse development. Am J Physiol 280: C12 - C21
Horiuchi A, Nikaido T, Taniguchi S, Fujii S (1999) Possible role of calponin hl as a tumor suppressor in human uterine leiomyosarcoma. J Natl Cancer Inst 91: 790–796
Hsieh CM, Yoshizumi M, Endege WO, Kho CJ, Jain MK, Kashiki S, Santos R, Lee WS, Perrella MA, Lee ME (1996) APEG-1, a novel gene preferentially expressed in aortic smooth muscle cells, is down-regulated by vascular injury. J Biol Chem 271: 17354–17359
Hsu-Wong S, Katchman SD, Ledo I, Wu M, Khillan J, Bashir MM, Rosenbloom J, Uitto J (1994) Tissue-specific and developmentally regulated expression of human elastin promoter activity in transgenic mice. J Biol Chem 269: 18072–18075
Jain MK, Fujita KP, Hsieh CM, Endege WO, Sibinga NES, Yet SF, Kashiki S, Lee WS, Perrella MA, Haber E, Lee ME (1996) Molecular cloning and characterization of SmLIM, a developmentally regulated LIM protein preferentially expressed in aortic smooth muscle cells. J Biol Chem 271: 10194–10199
Jiang Z, Grange RW, Walsh MP, Kamm KE (1997) Adenovirus-mediated transfer of the smooth muscle cell calponin gene inhibits proliferation of smooth muscle cells and fibroblasts. FEBS Lett 413: 441–445
Jiang Z, Wallner M, Meera P, Toro L (1999) Human and rodent MaxiK channel (3-subunit genes: cloning and characterization. Genomics 55: 57–67
Johansen FE, Prywes R (1995) Serum response factor: transcriptional regulation of genes induced by growth factors and differentiation. Biochem Biophys Acta 1242: 1–10
Joutel A, Andreux F, Gaulis S, Domenga V, Cecillion M, Battail N, Piga N, Chapon F, Godfrain C, Tournier-Lasserve E (2000) The ectodomain of the Notch3 receptor accumulates within the cerebrovasculature of CADASIL patients. J Clin Invest 105: 597–605
Kahari VM, Fazio MJ, Chen YQ, Bashir MM, Rosenbloom J, Uitto J (1990) Deletion analysis of 5’flanking region of the human elastin gene: delineation of functional promoter and regulatory cis-elements. J Biol Chem 265: 9485–9490
Katoh Y, Loukianov E, Kopras E, Zilberman A, Periasamy M (1994) Identification of functional promoter elements in the rabbit smooth muscle myosin heavy chain gene. J Biol Chem 269: 30538–30545
Katoh Y, Molkentin JD, Dave V, Olson EN, Periasamy M (1998) MEF2B is a component of a smooth muscle-specific complex that binds an A/T-rich element important for smooth muscle myosin heavy chain gene expression. J Biol Chem 273: 1511–1518
Kelley CA, Takahashi M, Yu JH, Adelstein RS (1993) An insert of seven amino acids confers functional differences between smooth muscle myosins from the intestines and vasculature. J Biol Chem 268: 12848–12854
Kim S, Ip HS, Lu MM, Clendenin C, Parmacek MS (1997) A serum response factor-dependent transcriptional regulatory program identifies distinct smooth muscle cell sublineages. Mol Cell Biol 17: 2266–2278
Kirby ML, Gale TF, Stewart DE:1983. Neural crest cells contribute to normal aorticopulmonary septation. Science 220: 1059–1061
Kitami Y, Maguchi M, Nishida W, Okura T, Kohara K, Hiwada K (1999) The unique 5’-flanking region of the human basic calponin gene. Hypertens Res 22: 187–193
Kovacs A, Zimmer WE (1998) Cell-specific transcription of the smooth muscle gamma-actin gene requires both positive-and negative-acting cis elements. Gene Exp 7: 115–129
Krämer J, Quensel C, Meding J, Cardosa MC, Leonhardt H (2001) Identification and characteri- zation of novel smoothelin isoforms in vascular smooth muscle. J Vasc Res 38: 120–132
Kuisk IR, Li H, Tran D, Capetanaki Y (1996) A single MEF2 site governs desmin transcription in both heart and skeletal muscle during mouse embryogenesis. Dev Biol 174: 1–13
Landerholm TE, Dong X-R, Lu J, Belaguli NS, Schwartz RJ, Majesky MW (1999) A role for serum response factor in coronary smooth muscle differentiation from proepicardial cells. Development 126: 2053–2062
Layne MD, Endege WO, Jain MK, Yet SF, Hsieh CM, Chin MT, Perrella MA, Blanar MA, Haber E, Lee ME (1998) Aortic carboxypeptidase-like protein, a novel protein with discoidin and carboxypeptidase-like domains, is up-regulated during vascular smooth muscle cell differentiation. J Biol Chem 273: 15654–15660
Mammalian Smooth Muscle Differentiation: Origins, Markers and Transcriptional Control 55
Lazard D, Sastre X, Frid MG, Glukhova MA, Thiery JP, Koteliansky VE (1993) Expression of smooth muscle-specific proteins in myoepithelium and stromal myofibroblasts of normal and malignant human breast tissue. Proc Natl Acad Sci USA 90: 999–1003
Le Lievre CS, Le Douarin NM (1975) Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. J Embryol Exp Morph 34: 125–154
Lecain E, Alliot F, Laine MC, Calas B, Pessac B (1991) a isoform of smooth muscle actin is expressed in astrocytes in vitro and in vivo. J Neurosci Res 28: 601–606
Lees-Miller JP, Heeley DH, Smillie LB, Kay CM (1987a). Isolation and characterization of an abundant and novel 22-kDa protein (SM22) from chicken gizzard smooth muscle. J Biol Chem 262: 2988–2993
Lees-Miller JP, Heeley DH, Smillie LB (1987b) An abundant and novel protein of 22kDa (SM22) is widely distributed in smooth muscles. Biochem J 244: 705–709
Lemire JM, Covin CW, White S, Giachelli CM, Schwartz SM, (1994) Characterization of cloned aortic smooth muscle cells from young rats. Am J Pathol 144: 1068–1081
Leslie KO, Taatjes DJ, Schwarz J, von Turkovich M, Low RB (1991) Cardiac myofibroblasts express alpha smooth muscle actin during right ventricular pressure overload in the rabbit. Am J Pathol 139: 207–216
Li L, Miano JM, Cserjesi P, Olson EN (1996a) SM22a, a marker of adult smooth muscle, is expressed in multiple myogenic lineages during embryogenesis. Circ Res 78: 188–195
Li L, Miano JM, Mercer B, Olson EN (1996b) Expression of the SM22a promoter in transgenic mice provides evidence for distinct transcriptional regulatory programs in vascular and visceral smooth muscle cells. J Cell Biol 132: 849–859
Li L, Liu ZC, Mercer B, Overbeek P, Olson EN (1997) Evidence for serum response factor-mediated regulatory networks governing SM22a transcription in smooth, skeletal, and cardiac muscle cells. Dev Biol 187: 311–321
Li Z, Paulin D (1991) High level desmin expression depends on a muscle-specific enhancer. J Biol Chem 266: 6562–6570
Mack CP, Owens GK (1999) Regulation of smooth muscle a-actin expression in vivo is dependent on CArG elements within the 5’ and first intron promoter regions. Circ Res 84: 852–861
Madsen CS, Hershey JC, Hautmann MB, White SL, Owens GK (1997) Expression of the smooth muscle myosin heavy chain gene is regulated by a negative-acting GC-rich element located between two positive-acting serum response factor-binding elements. J Biol Chem 272: 6332–6340
Madsen CS, Regan CP, Hungerford JE, White SL, Manabe I, Owens GK (1998) Smooth muscle-specific expression of the smooth muscle myosin heavy chain gene in transgenic mice requires 5’-flanking and first intronic DNA sequence. Circ Res 82: 908–917
Majesky MW, Giachelli CM, Reidy MA, Schwartz SM (1992) Rat carotid neointimal smooth muscle cells reexpress a developmentally regulated mRNA phenotype during repair of arterial injury. Circ Res 71: 759–768
Manabe I, Owens GK (2001) CArG elements control smooth muscle subtype-specific expression of smooth muscle myosin in vivo. J Clin Invest 107: 823–834
Masuda H, Tanaka K, Takagi M, Ohgami K, Sakamaki T, Shibata N, Takahashi K (1996) Molecular cloning and characterization of human non-smooth muscle calponin. J Biochem 120: 415–424
McHugh KM (1995) Molecular analysis of smooth muscle development in the mouse. Dev Dyn 204: 278–290
McHugh KM, Lessard JL (1988) The developmental expression of the rat a-vascular and gamma-enteric smooth muscle isoactins; isolation and characterization of a rat gamma-enteric actin cDNA. J Biol Chem 8: 5224–5231
Miano JM, Olson EN (1996) Expression of the smooth muscle cell calponin gene marks the early cardiac and smooth muscle cell lineages during mouse embryogenesis. J Biol Chem 271: 7095–7103
Miano JM, Cserjesi P, Ligon KL, Periasamy M, Olson EN (1994) Smooth muscle myosin heavy chain exclusively marks the smooth muscle lineage during mouse embryogenesis. Circ Res 75: 803–812
Miano JM, Krahe R, Garcia E, Elliott JM, Olson EN (1997) Expression, genomic structure and high resolution mapping to 19p13.2 of the human smooth muscle cell calponin gene. Gene 197: 215–224
Miano JM, Kelly LA, Artacho CA, Nuckolls TA, Piantedosi R, Blaner WS (1998) all-trans-retinoic acid reduces neointimal formation and promotes favorable geometric remodeling of the rat carotid artery after balloon withdrawal injury. Circulation 98: 1219–1227
Miano JM, Carlson MJ, Spencer JA, Misra RP (2000) Serum response factor-dependent regulation of the smooth muscle calponin gene. J Biol Chem 275: 9814–9822
Miano JM, Thomas S, Disteche CM (2001) Expression and chromosomal mapping of the mouse smooth muscle calponin gene. Mamm Genome 12: 187–191
Miano JM, Kitchen CM, Chen J, Maltby KM, Kelly LA, Weiler H, Krahe R, Ashworth LK, Garcia E (2002) Human smooth muscle calponin expression in transgenic mice revealed with a bacterial artificial chromosome. In Press, Am J Physiol Heart & Circulatory
Minty A, Kedes L (1986) Upstream regions of the human cardiac actin gene that modulate its transcription in muscle cells: presence of an evolutionarily conserved repeated motif. Mol Cell Biol 6: 2125–2136
Moessler H, Mericskay M, Li Z, Nagl S, Paulin D, Small JV (1996) The SM 22 promoter directs tissue-specific expression in arterial but not in venous or visceral smooth muscle cells in transgenic mice. Development 122: 2415–2425
Moiseeva EP, Critchley DR (1997) Characterisation of the promoter which regulates expression of a phosphoglucomutase-related protein, a component of the dystrophin/utrophin cytoskeleton predominantly expressed in smooth muscle. Eur J Biochem 248: 634–643
Moiseeva EP, Belkin AM, Spurr NK, Koteliansky VE, Critchley DR (1996) A novel dystrophin/ utrophin-associated protein is an enzymatically inactive member of the phosphoglucomutase superfamily. Eur J Biochem 235: 103–113
Momiyama T, Hayashi K, Obata H, Chimori Y, Nishida T, Ito T, Kamiike W, Matsuda H, Sobue K (1998) Functional involvement of serum response factor in the transcriptional regulation of caldesmon gene. Biochem Biophys Res Comm 242: 429–435
Morano I, Chai G-X, Baltas LG, Lamounier-Zepter V, Lutsch G, Kott M, Haase H, Bader M (2000) Smooth-muscle contraction without smooth-muscle myosin. Nat Cell Biol 2: 371–375
Nakamura M, Nishida W, Mori S, Hiwada K, Hayashi K, Sobue K (2001) Transcriptional activation of 13-tropomyosin mediated by serum response factor and a novel Barx homologue, Barxlb, in smooth muscle cells. J Biol Chem 276: 18313–18320
Norman C, Runswick M, Pollock R, Treisman R (1988) Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell 55: 989–1003
North AJ, Gimona M, Cross RA, Small JV (1994) Calponin is localised in both the contractile apparatus and the cytoskeleton of smooth muscle cells. J Cell Sci 107: 437–444
Obata H, Hayashi K, Nishida W, Momiyama T, Uchida A, Ochi T, Sobue K (1997) Smooth muscle cell phenotype-dependent transcriptional regulation of the al integrin gene. J Biol Chem 272: 26643–26651
Olson EN (1990) MyoD family: a paradigm for development. Genes Dev 4: 1454–1461
Olson EN, Srivastava D (1996) Molecular pathways controlling heart development. Science 272: 671–676
Oosthuyse B, Moons L, Storkebaum E, Beck H, Nuyens D, Brusselmans K, Van Dorpe J, Hellings P, Gorselink M, Heymans S, Theilmeier G, Dewerchin M, Laudenbach V, Vermylen P, Raat H, Acker T, Vleminckx V, Van Den Bosch L, Cashman N, Fujisawa H, Drost MR, Sciot R, Bruyninckx F, Hicklin DJ, Ince C, Gressens P, Lupu F, Plate KH, Robberecht W, Herbert J-M, Collen D, Carmeliet P (2001) Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat Genet 28: 131–138
Mammalian Smooth Muscle Differentiation: Origins, Markers and Transcriptional Control 57
Osborn M, Caselitz J, Puschel K, Weber K (1987) Intermediate filament expression in human vascular smooth muscle and in arteriosclerotic plaques. Virchows Arch A Pathol Anat Histol 411: 449–458
Owens GK (1995) Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 75: 487–517
Parker CA, Takahashi K, Tang JX, Tao T, Morgan KG (1998) Cytoskeletal targeting of calponin in differentiated, contractile smooth muscle cells of the ferret. J Physiol 508: 187–198
Pascolini R, Di Rosa I, Fagotti A, Panara F, Gabbiani G (1992) The mammalian anti-a-smooth muscle actin monoclonal antibody recognizes an a-actin-like protein in planaria ( Dugesia lugubris s.l. ). Differentiation 51: 177–186
Prinjha RK, Shapland CE, Hsuan JJ, Totty NF, Mason IJ, Lawson D (1994) Cloning and sequencing of cDNAs encoding the actin cross-linking protein transgelin defines a new family of actin-associated proteins. Cell Motil Cytoskeleton 28: 243–255
Qian J, Kumar A, Szucsik JC, Lessard JL (1996) Tissue and developmental specific expression of murine smooth muscle gamma-actin fusion genes in transgenic mice. Dev Dyn 207: 135–144
Raguz S, Hobbs C, Yague E, Ioannou PA, Walsh FS, Antoniou M (1998) Muscle-specific locus control region activity associated with the human desmin gene. Dev Biol 201: 26–42
Regan CP, Adam PJ, Madsen CS, Owens GK (2000) Molecular mechanisms of decreased smooth muscle differentiation marker expression after vascular injury. J Clin Invest 106: 1139–1147
Roose J, Korver W, Oving E, Wilson A, Wagenaar G, Markman M, Lamers W, Clevers H (1998) High expression of the HMG box factor Sox-13 in arterial walls during embryonic development. Nucleic Acids Res 26: 469–476
Rothman A, Kulik TJ, Taubman MB, Berk BC, Smith CWJ, Nadal-Ginard B (1992) Development and characterization of a cloned rat pulmonary arterial smooth muscle cell line that maintains differentiated properties through multiple subcultures. Circulation 86: 1977–1986
Royuela M, Fraile B, Picazo L, Paniagua R (1997) Immunocytochemical electron microscopic study and Western blot analysis of caldesmon and calponin in striated muscle of the fruit fly Drosophila melanogaster and in several muscle cell types of the earthworm Eisenia foetida. Eur J Cell Biol 72: 90–94
Royuela M, Fraile B, Arenas MI, Paniagua R (2000) Characterization of several invertebrate muscle cell types: a comparison with vertebrate muscles. Microsc Res Tech 48: 107–115
Rudnicki MA, Sawtell NM, Reuhl KR, Berg R, Craig JC, Jardine K, Lessard JL, McBurney MW (1990) Smooth muscle actin expression during P19 embryonal carcinoma differentiation in cell culture. J Cell Physiol 142: 89–98
Ruzika DL, Schwartz RJ (1988) Sequential activation of a-actin genes during avian cardiogenesis: vascular smooth muscle a-actin gene transcripts mark the onset of cardiomyocyte differentiation. J Cell Biol 107: 2575–2586
Samaha FF, Ip HS, Morrisey EE, Seltzer J, Tang Z, Solway J, Parmacek MS (1996) Developmental pattern of expression and genomic organization of the calponin-hl gene: a contractile smooth muscle cell marker. J Biol Chem 271: 395–403
Sartorelli V, Webster KA, Kedes L (1990) Muscle-specific expression of the cardiac a-actin gene requires MyoD1, CArG-box binding factor, and Spl. Genes Dev 4: 1811–1822
Sawtell NM, Lessard JL (1989) Cellular distribution of smooth muscle actins during mammalian embryogenesis: expression of the a-vascular but not the y-enteric isoform in differentiating striated myocytes. J Cell Biol 109: 2929–2937
Schildmeyer LA, Braun R, Taffet G, Debiasi M, Burns AE, Bradley A, Schwartz RJ (2000) Impaired vascular contractility and blood pressure homeostasis in the smooth muscle a-actin null mouse. FASEB J 14: 2213–2220
Schnapp LM, Breuss JM, Ramos DM, Sheppard D, Pytela R (1995) Sequence and tissue distribution of the human integrin aR subunit: a R,-associated a subunit expressed in smooth muscle cells. J Cell Sci 108: 537–544
Schubert D, Harris AJ, Devine CE, Heinemann S (1974) Characterization of a unique muscle cell line. J Cell Biol 61: 398–413
Shah NM, Groves AK, Anderson DJ (1996) Alternative neural crest cell fates are instructively promoted by TGF13 superfamily members. Cell 85: 331–343
Shanahan CM, Cary NRB, Metcalfe JC, Weissberg PL (1994) High expression of genes for calcification-regulating proteins in human atherosclerotic plaques. J Clin Invest 93: 23932402
Shi Y, O’Brien JE, Fard A, Mannion JD, Wang D, Zalewski A (1996) Adventitial myofibroblasts contribute to neointimal formation in injured porcine coronary arteries. Circulation 94: 1655–1664
Shimizu RT, Blank RS, Jervis R, Lawrenz-Smith SC, Owens GK (1995) The smooth muscle a-actin gene promoter is differentially regulated in smooth muscle versus non-smooth muscle cells. J Biol Chem 270: 7631–7643
Solway J, Seltzer J, Samaha FF, Kim S, Alger LE, Niu Q, Morrisey EE, Ip HS, Parmacek MS (1995) Structure and expression of a smooth muscle cell-specific gene, SM22a. J Biol Chem 270: 13460–13469
Strasser P, Gimona M, Moessler H, Herzog M, Small JV (1993) Mammalian calponin: identification and expression of genetic variants. FEBS Lett 330: 13–18
Stull JT, Gallagher PG, Herring BP, Kamm KE (1991) Vascular smooth muscle contractile elements: cellular regulation. Hypertension 17: 723–732
Sugi Y, Lough J (1992) Onset of expression and regional deposition of alpha-smooth and sarcomeric actin during avian heart development. Dev Dyn 193: 116–124
Sugimoto T, Hosoi H, Horii Y, Ishida H, Mine H, Takahashi K, Abe T, Ohta S, Sawada T (1999) Malignant rhabdoid-tumor cell line showing neural and smooth-muscle-cell phenotypes. Int J Cancer 82: 678–686
Suzuki T, Kim HS, Kurabayashi M, Hamada H, Fujii H, Aikawa M, Watanabe M, Watanabe N, Sakomura Y, Yazaki Y, Nagai R (1996) 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 78: 395–404
Takahashi K, Hiwada K, Kokubu T (1986) Isolation and characterization of a 34,000-dalton calmodulin-and F-actin-binding protein from chicken gizzard smooth muscle. Biochem Biophys Res Comm 141: 20–26
Takahashi K, Hiwada K, Kokubu T (1988) Vascular smooth muscle calponin. A novel troponin T-like protein. Hypertension 11 (Pt 2): 620–626
Taubman MB, Smith CWJ, Izumo S, Grant JW, Endo T, Andreadis A, Nadal-Ginard B (1989) The expression of sarcomeric muscle-specific contractile protein genes in BC3H1 cells: BC3H1 cells resemble skeletal myoblasts that are defective for commitment to terminal differentiation. J Cell Biol 108: 1799–1806
Topouzis S, Majesky MW (1996) Smooth muscle lineage diversity in the chick embryo: two types of aortic smooth muscle cell differ in growth and receptor-mediated transcriptional responses to transforming growth factor-(3. Dev Biol 178: 430–445
Ueki N, Sobue K, Kanda K, Toshikazu H, Higashino K (1987) Expression of high and low molecular weight caldesmons during phenotypic modulation of smooth muscle cells. Proc Natl Acad Sci USA 84: 9049–9053
van der Loop FTL, Schaart G, Timmer EDJ, Ramaekers FCS, van Eys GJJM (1996) Smoothelin, a novel cytoskeletal protein specific for smooth muscle cells. J Cell Biol 134: 401–411
van der Loop FTL, Gabbiani G, Kohnen G, Ramaekers FCS, van Eys GJJM (1997) Differentiation of smooth muscle cells in human blood vessels as defined by smoothelin, a novel marker for the contractile phenotype. Arterioscler Thromb Vasc Biol 17: 665–671
van Groningen JJM, Bloemers HPJ, Swart GWM (1994) Rat desmin gene structure and expression. Biochim Biophys Acta 1217: 107–109
Vrancken Peeters M-PFM, Gittenberger-de Groot AC, Mentink MMT, Poelmann RE (1999) Smooth muscle cells and fibroblasts of the coronary arteries derive from epithelialmesenchymal transformation of the epicardium. Anat Embryol 199: 367–378
Waldo KL, Kumiski DH, Kirby ML (1994) Association of the cardiac neural crest with development of the coronary arteries in the chick embryo. Anat Rec 239: 315–331
Mammalian Smooth Muscle Differentiation: Origins, Markers and Transcriptional Control 59
Wang D-Z, Chang PS, Wang Z, Sutherland L, Richardson JA, Small E, Krieg PA, Olson EN (2001) Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell 105: 851–862
Wang J, Niu W, Nikiforov Y, Naito S, Chernausek S, Witte D, LeRoith D, Strauch A, Fagin JA (1997) Targeted overexpression of IGF-I evokes distinct patterns of organ remodeling in smooth muscle cell tissue beds of transgenic mice. J Clin Invest 100: 1425–1439
Weir L, Chen D, Pastore C, Isner JM, Walsh K (1995) Expression of gax, a growth arrest homeobox gene, is rapidly down-regulated in the rat carotid artery during the proliferative response to balloon injury. J Biol Chem 270: 5457–5461
White S, Martin AF, Periasamy M (1993) Identification of a novel smooth muscle myosin heavy chain cDNA: isoform diversity in the S1 head region. Am J Physiol 264: C1252 - C1258
Winder S, Walsh M (1990) Inhibition of the actomyosin MgATPase by chicken gizzard calponin. Prog Clin Biol Res 327: 141–148
Woodcock-Mitchell JL, Mitchell JJ, Low RB, Kieny M, Sengel P, Rubbia L, Skalli O, Jackson B, Gabbiani G (1988) a-smooth muscle actin is transiently expressed in embryonic rat cardiac and skeletal muscles. Differentiation 39: 161–166
Ya J, Markman MW, Wagenaar GT, Blommaart PJ, Moorman AF, Lamers WH (1997) Expression of the smooth-muscle proteins alpha-smooth-muscle actin and calponin, and of the intermediate filament protein desmin are parameters of cardiomyocyte maturation in the prenatal rat heart. Anat Rec 249: 495–505
Yamamura H, Masuda H, Ikeda W, Tokuyama T, Takagi M, Shibata N, Tatsuta M, Takahashi K (1997) Structure and expression of the human SM22a gene, assignment of the gene to chromosome 11, and repression of the promoter activity by cytosine DNA methylation. J Biochem 122: 157–167
Yamamura H, Yoshikawa H, Tatsuta M, Akedo H, Takahashi K (1998) Expression of the smooth muscle calponin gene in human osteosarcoma and its possible association with prognosis. Int J Cancer 79: 245–250
Yamashita J, Itoh H, Hirashima M, Ogawa M, Nishikawa S, Yurugi T, Naito M, Nakao K, Nishikawa S-I (2000) Flkl-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 408: 92–96
Yano H, Hayashi K, Momiyama T, Saga H, Haruna M, Sobue K (1995) Transcriptional regulation of the chicken caldesmon gene: activation of gizzard-type caldesmon promoter requires a CArG box-like motif. J Biol Chem 270: 23661–23666
Yet SF, Folta SC, Jain MK, Hsieh CM, Maemura K, Layne MD, Zhang D, Marria PB, Yoshizumi M, Chin MT, Perrella MA, Lee ME (1998) Molecular cloning, characterization, and promoter analysis of the mouse Crp2/SMLim gene: preferential expression of its promoter in the vascular smooth muscle cells of transgenic mice. J Biol Chem 273: 10530–10537
Yoshikawa H, Taniguchi S, Yamamura H, Mori S, Sugimoto M, Miyado K, Nakamura K, Nakao K, Katsuki M, Shibata N, Takahashi K (1998) Mice lacking smooth muscle calponin display increased bone formation that is associated with enhancement of bone morphogenetic protein responses. Genes Cells 3: 685–695
Zhang JCL, Kim S, Helmke BP, Yu WW, Du KL, Lu MM, Strobeck M, Yu Q-C, Parmacek MS (2001) Analysis of SM22a-deficient mice reveals unanticipated insights into smooth muscle cell differentiation and function. Mol Cell Biol 21: 1336–1344
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2002 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Miano, J.M. (2002). Mammalian Smooth Muscle Differentiation: Origins, Markers and Transcriptional Control. In: Brand-Saberi, B. (eds) Vertebrate Myogenesis. Results and Problems in Cell Differentiation, vol 38. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-45686-5_2
Download citation
DOI: https://doi.org/10.1007/978-3-540-45686-5_2
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-07735-7
Online ISBN: 978-3-540-45686-5
eBook Packages: Springer Book Archive