HRC Is a Direct Transcriptional Target of MEF2 during Cardiac, Skeletal, and Arterial Smooth Muscle Development In Vivo

REFERENCES

• Andres, V., Cervera M., and Mahdavi V.. 1995. Determination of the consensus binding site for MEF2 expressed in muscle and brain reveals tissue-specific sequence constraints. J. Biol. Chem. 270:23246–23249.
   PubMed Web of Science ®Google Scholar
• Baker, D. L., Dave V., Reed T., Misra S., and Periasamy M.. 1998. A novel E box/AT-rich element is required for muscle-specific expression of the sarcoplasmic reticulum Ca2+-ATPase (SERCA2) gene. Nucleic Acids Res. 26:1092–1098.
   PubMed Web of Science ®Google Scholar
• Baker, D. L., Dave V., Reed T., and Periasamy M.. 1996. Multiple Sp1 binding sites in the cardiac/slow twitch muscle sarcoplasmic reticulum Ca2+-ATPase gene promoter are required for expression in Sol8 muscle cells. J. Biol. Chem. 271:5921–5928.
   PubMedGoogle Scholar
• Bi, W., Drake C. J., and Schwarz J. J.. 1999. The transcription factor MEF2C-null mouse exhibits complex vascular malformations and reduced cardiac expression of angiopoietin 1 and VEGF. Dev. Biol. 211:255–267.
   PubMedGoogle Scholar
• Black, B. L., Lu J., and Olson E. N.. 1997. The MEF2A 3′ untranslated region functions as a cis-acting translational repressor. Mol. Cell. Biol. 17:2756–2763.
   PubMedGoogle Scholar
• Black, B. L., Martin J. F., and Olson E. N.. 1995. The mouse MRF4 promoter is trans-activated directly and indirectly by muscle-specific transcription factors. J. Biol. Chem. 270:2889–2892.
   PubMedGoogle Scholar
• Black, B. L., Molkentin J. D., and Olson E. N.. 1998. Multiple roles for the MyoD basic region in transmission of transcriptional activation signals and interaction with MEF2. Mol. Cell. Biol. 18:69–77.
   PubMedGoogle Scholar
• Black, B. L., and Olson E. N.. 1998. Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu. Rev. Cell Dev. Biol. 14:167–196.
   PubMed Web of Science ®Google Scholar
• Bour, B. A., O'Brien M. A., Lockwood W. L., Goldstein E. S., Bodmer R., Taghert P. H., Abmayr S. M., and Nguyen H. T.. 1995. Drosophila MEF2, a transcription factor that is essential for myogenesis. Genes Dev. 9:730–741.
   PubMedGoogle Scholar
• Chang, D. F., Belaguli N. S., Iyer D., Roberts W. B., Wu S. P., Dong X. R., Marx J. G., Moore M. S., Beckerle M. C., Majesky M. W., and Schwartz R. J.. 2003. Cysteine-rich LIM-only proteins CRP1 and CRP2 are potent smooth muscle differentiation cofactors. Dev. Cell 4:107–118.
   PubMed Web of Science ®Google Scholar
• Chang, P. S., Li L., McAnally J., and Olson E. N.. 2001. Muscle specificity encoded by specific serum response factor-binding sites. J. Biol. Chem. 276:17206–17212.
   PubMedGoogle Scholar
• Chang, Y. F., Wei J., Liu X., Chen Y. H., Layne M. D., and Yet S. F.. 2003. Identification of a CArG-independent region of the cysteine-rich protein 2 promoter that directs expression in the developing vasculature. Am. J. Physiol. Heart Circ. Physiol. 285:H1675–H1683.
   PubMedGoogle Scholar
• Cheng, T. C., Wallace M. C., Merlie J. P., and Olson E. N.. 1993. Separable regulatory elements governing myogenin transcription in mouse embryogenesis. Science 261:215–218.
   PubMed Web of Science ®Google Scholar
• Cripps, R. M., Black B. L., Zhao B., Lien C. L., Schulz R. A., and Olson E. N.. 1998. The myogenic regulatory gene Mef2 is a direct target for transcriptional activation by Twist during Drosophila myogenesis. Genes Dev. 12:422–434.
   PubMedGoogle Scholar
• Damiani, E., and Margreth A.. 1991. Subcellular fractionation to junctional sarcoplasmic reticulum and biochemical characterization of 170 kDa Ca2+- and low-density-lipoprotein-binding protein in rabbit skeletal muscle. Biochem. J. 277:825–832.
   PubMedGoogle Scholar
• Dodou, E., Xu S. M., and Black B. L.. 2003. mef2c is activated directly by myogenic basic helix-loop-helix proteins during skeletal muscle development in vivo. Mech. Dev. 120:1021–1032.
   PubMedGoogle Scholar
• Edmondson, D. G., Cheng T. C., Cserjesi P., Chakraborty T., and Olson E. N.. 1992. Analysis of the myogenin promoter reveals an indirect pathway for positive autoregulation mediated by the muscle-specific enhancer factor MEF-2. Mol. Cell. Biol. 12:3665–3677.
   PubMedGoogle Scholar
• Firulli, A. B., Miano J. M., Bi W., Johnson A. D., Casscells W., Olson E. N., and Schwarz J. J.. 1996. Myocyte enhancer binding factor-2 expression and activity in vascular smooth muscle cells. Association with the activated phenotype. Circ. Res. 78:196–204.
   PubMed Web of Science ®Google Scholar
• Frank, K. F., Mesnard-Rouiller L., Chu G., Young K. B., Zhao W., Haghighi K., Sato Y., and Kranias E. G.. 2001. Structure and expression of the mouse cardiac calsequestrin gene. Basic Res. Cardiol. 96:636–644.
   PubMed Web of Science ®Google Scholar
• Hofmann, S. L., Brown M. S., Lee E., Pathak R. K., Anderson R. G., and Goldstein J. L.. 1989. Purification of a sarcoplasmic reticulum protein that binds Ca2+ and plasma lipoproteins. J. Biol. Chem. 264:8260–8270.
   PubMedGoogle Scholar
• Hofmann, S. L., Goldstein J. L., Orth K., Moomaw C. R., Slaughter C. A., and Brown M. S.. 1989. Molecular cloning of a histidine-rich Ca2+-binding protein of sarcoplasmic reticulum that contains highly conserved repeated elements. J. Biol. Chem. 264:18083–18090.
   PubMedGoogle Scholar
• Hofmann, S. L., Topham M., Hsieh C. L., and Francke U.. 1991. cDNA and genomic cloning of HRC, a human sarcoplasmic reticulum protein, and localization of the gene to human chromosome 19 and mouse chromosome 7. Genomics 9:656–669.
   PubMedGoogle Scholar
• Hogan, B., Beddington R., Costantini F., and Lacy E.. 1994. Manipulating the mouse embryo, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
   Google Scholar
• Horton, R. M. 1997. In vitro recombination and mutagenesis of DNA: SOEing together tailor-made genes, p. 141–149. In White B. A. (ed.), PCR cloning protocols, vol. 67. Humana Press, Totowa, N.J.
   Google Scholar
• Kim, E., Shin D. W., Hong C. S., Jeong D., Kim Do H., and Park W. J.. 2003. Increased Ca2+ storage capacity in the sarcoplasmic reticulum by overexpression of HRC (histidine-rich Ca2+ binding protein). Biochem. Biophys. Res. Commun. 300:192–196.
   PubMedGoogle Scholar
• Kim, S., Ip H. S., Lu M. M., Clendenin C., and Parmacek M. S.. 1997. A serum response factor-dependent transcriptional regulatory program identifies distinct smooth muscle cell sublineages. Mol. Cell. Biol. 17:2266–2278.
   PubMed Web of Science ®Google Scholar
• Kothary, R., Clapoff S., Darling S., Perry M. D., Moran L. A., and Rossant J.. 1989. Inducible expression of an hsp68-lacZ hybrid gene in transgenic mice. Development 105:707–714.
   PubMed Web of Science ®Google Scholar
• Layne, M. D., Yet S. F., Maemura K., Hsieh C. M., Liu X., Ith B., Lee M. E., and Perrella M. A.. 2002. Characterization of the mouse aortic carboxypeptidase-like protein promoter reveals activity in differentiated and dedifferentiated vascular smooth muscle cells. Circ. Res. 90:728–736.
   PubMedGoogle Scholar
• Lee, H. G., Kang H., Kim D. H., and Park W. J.. 2001. Interaction of HRC (histidine-rich Ca2+-binding protein) and triadin in the lumen of sarcoplasmic reticulum. J. Biol. Chem. 276:39533–39538.
   PubMedGoogle Scholar
• Li, L., Liu Z., Mercer B., Overbeek P., and Olson E. N.. 1997. Evidence for serum response factor-mediated regulatory networks governing SM22α transcription in smooth, skeletal, and cardiac muscle cells. Dev. Biol. 187:311–321.
   PubMedGoogle Scholar
• Li, L., Miano J. M., Mercer B., and Olson E. N.. 1996. Expression of the SM22α promoter in transgenic mice provides evidence for distinct transcriptional regulatory programs in vascular and visceral smooth muscle cells. J. Cell Biol. 132:849–859.
   PubMed Web of Science ®Google Scholar
• Lilly, B., Olson E. N., and Beckerle M. C.. 2001. Identification of a CArG box-dependent enhancer within the cysteine-rich protein 1 gene that directs expression in arterial but not venous or visceral smooth muscle cells. Dev. Biol. 240:531–547.
   PubMed Web of Science ®Google Scholar
• Lilly, B., Zhao B., Ranganayakulu G., Paterson B. M., Schulz R. A., and Olson E. N.. 1995. Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science 267:688–693.
   PubMed Web of Science ®Google Scholar
• Lin, Q., Lu J., Yanagisawa H., Webb R., Lyons G. E., Richardson J. A., and Olson E. N.. 1998. Requirement of the MADS-box transcription factor MEF2C for vascular development. Development 125:4565–4574.
   PubMedGoogle Scholar
• Lin, Q., Schwarz J., Bucana C., and Olson E. N.. 1997. Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276:1404–1407.
   PubMed Web of Science ®Google Scholar
• Lu, J., McKinsey T. A., Zhang C. L., and Olson E. N.. 2000. Regulation of skeletal myogenesis by association of the MEF2 transcription factor with class II histone deacetylases. Mol. Cell 6:233–244.
   PubMed Web of Science ®Google Scholar
• Mack, C. P., and Owens G. K.. 1999. Regulation of smooth muscle alpha-actin expression in vivo is dependent on CArG elements within the 5′ and first intron promoter regions. Circ. Res. 84:852–861.
   PubMed Web of Science ®Google Scholar
• Mack, C. P., Thompson M. M., Lawrenz-Smith S., and Owens G. K.. 2000. Smooth muscle alpha-actin CArG elements coordinate formation of a smooth muscle cell-selective, serum response factor-containing activation complex. Circ. Res. 86:221–232.
   PubMedGoogle Scholar
• Manabe, I., and Owens G. K.. 2001. CArG elements control smooth muscle subtype-specific expression of smooth muscle myosin in vivo. J. Clin. Investig. 107:823–834.
   PubMed Web of Science ®Google Scholar
• McFadden, D. G., Charite J., Richardson J. A., Srivastava D., Firulli A. B., and Olson E. N.. 2000. A GATA-dependent right ventricular enhancer controls dHAND transcription in the developing heart. Development 127:5331–5341.
   PubMedGoogle Scholar
• McKinsey, T. A., Zhang C. L., Lu J., and Olson E. N.. 2000. Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 408:106–111.
   PubMed Web of Science ®Google Scholar
• McKinsey, T. A., Zhang C. L., and Olson E. N.. 2001. Control of muscle development by dueling HATs and HDACs. Curr. Opin. Genet. Dev. 11:497–504.
   PubMed Web of Science ®Google Scholar
• McTiernan, C. F., Frye C. S., Lemster B. H., Kinder E. A., Ogletree-Hughes M. L., Moravec C. S., and Feldman A. M.. 1999. The human phospholamban gene: structure and expression. J. Mol. Cell. Cardiol. 31:679–692.
   PubMedGoogle Scholar
• Mericskay, M., Parlakian A., Porteu A., Dandre F., Bonnet J., Paulin D., and Li Z.. 2000. An overlapping CArG/octamer element is required for regulation of desmin gene transcription in arterial smooth muscle cells. Dev. Biol. 226:192–208.
   PubMedGoogle Scholar
• Molkentin, J. D., Black B. L., Martin J. F., and Olson E. N.. 1995. Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell 83:1125–1136.
   PubMedGoogle Scholar
• Morin, S., Charron F., Robitaille L., and Nemer M.. 2000. GATA-dependent recruitment of MEF2 proteins to target promoters. EMBO J. 19:2046–2055.
   PubMedGoogle Scholar
• Naya, F. J., Wu C., Richardson J. A., Overbeek P., and Olson E. N.. 1999. Transcriptional activity of MEF2 during mouse embryogenesis monitored with a MEF2-dependent transgene. Development 126:2045–2052.
   PubMedGoogle Scholar
• Nishida, K., Otsu K., Hori M., Kuzuya T., and Tada M.. 1996. Cloning and characterization of the 5′-upstream regulatory region of the Ca2+-release channel gene of cardiac sarcoplasmic reticulum. Eur. J. Biochem. 240:408–415.
   PubMedGoogle Scholar
• Ornatsky, O. I., Andreucci J. J., and McDermott J. C.. 1997. A dominant-negative form of transcription factor MEF2 inhibits myogenesis. J. Biol. Chem. 272:33271–33278.
   PubMedGoogle Scholar
• Parmacek, M. S. 2001. Transcriptional programs regulating vascular smooth muscle cell development and differentiation. Curr. Top. Dev. Biol. 51:69–89.
   PubMedGoogle Scholar
• Pathak, R. K., Anderson R. G., and Hofmann S. L.. 1992. Histidine-rich calcium binding protein, a sarcoplasmic reticulum protein of striated muscle, is also abundant in arteriolar smooth muscle cells. J. Muscle Res. Cell Motil. 13:366–376.
   PubMedGoogle Scholar
• Picello, E., Damiani E., and Margreth A.. 1992. Low-affinity Ca2+-binding sites versus Zn2+-binding sites in histidine-rich Ca2+-binding protein of skeletal muscle sarcoplasmic reticulum. Biochem. Biophys. Res. Commun. 186:659–667.
   PubMedGoogle Scholar
• Ranganayakulu, G., Zhao B., Dokidis A., Molkentin J. D., Olson E. N., and Schulz R. A.. 1995. A series of mutations in the D-MEF2 transcription factor reveal multiple functions in larval and adult myogenesis in Drosophila. Dev. Biol. 171:169–181.
   PubMedGoogle Scholar
• Schmoelzl, S., Leeb T., Brinkmeier H., Brem G., and Brenig B.. 1996. Regulation of tissue-specific expression of the skeletal muscle ryanodine receptor gene. J. Biol. Chem. 271:4763–4769.
   PubMedGoogle Scholar
• Suk, J. Y., Kim Y. S., and Park W. J.. 1999. HRC (histidine-rich Ca2+ binding protein) resides in the lumen of sarcoplasmic reticulum as a multimer. Biochem. Biophys. Res. Commun. 263:667–671.
   PubMed Web of Science ®Google Scholar
• Verzi, M. P., Anderson J. P., Dodou E., Kelly K. K., Greene S. B., North B. J., Cripps R. M., and Black B. L.. 2002. N-twist, an evolutionarily conserved bHLH protein expressed in the developing CNS, functions as a transcriptional inhibitor. Dev. Biol. 249:174–190.
   PubMedGoogle Scholar
• Wang, D. Z., Li S., Hockemeyer D., Sutherland L., Wang Z., Schratt G., Richardson J. A., Nordheim A., and Olson E. N.. 2002. Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc. Natl. Acad. Sci. USA 99:14855–14860.
   PubMed Web of Science ®Google Scholar
• Wang, Z., Wang D. Z., Pipes G. C., and Olson E. N.. 2003. Myocardin is a master regulator of smooth muscle gene expression. Proc. Natl. Acad. Sci. USA 100:7129–7134.
   PubMed Web of Science ®Google Scholar
• Yee, S. P., and Rigby P. W.. 1993. The regulation of myogenin gene expression during the embryonic development of the mouse. Genes Dev. 7:1277–1289.
   PubMed Web of Science ®Google Scholar
• Yoshida, T., Sinha S., Dandre F., Wamhoff B. R., Hoofnagle M. H., Kremer B. E., Wang D. Z., Olson E. N., and Owens G. K.. 2003. Myocardin is a key regulator of CArG-dependent transcription of multiple smooth muscle marker genes. Circ. Res. 92:856–864.
   PubMedGoogle Scholar