This Article
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Parmacek, M S
Right arrow Articles by Leiden, J M
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Parmacek, M S
Right arrow Articles by Leiden, J M

 Previous Article  |  Next Article 

Mol Cell Biol. 1994 March; 14(3): 1870-1885

A novel myogenic regulatory circuit controls slow/cardiac troponin C gene transcription in skeletal muscle.

M S Parmacek, H S Ip, F Jung, T Shen, J F Martin, A J Vora, E N Olson and J M Leiden

Department of Medicine, University of Chicago, Illinois 60637.

ABSTRACT

The slow/cardiac troponin C (cTnC) gene is expressed in three distinct striated muscle lineages: cardiac myocytes, embryonic fast skeletal myotubes, and adult slow skeletal myocytes. We have reported previously that cTnC gene expression in cardiac muscle is regulated by a cardiac-specific promoter/enhancer located in the 5' flanking region of the gene (bp -124 to +1). In this report, we demonstrate that the cTnC gene contains a second distinct and independent transcriptional enhancer which is located in the first intron. This second enhancer is skeletal myotube specific and is developmentally up-regulated during the differentiation of myoblasts to myotubes. This enhancer contains three functionally important nuclear protein binding sites: a CACCC box, a MEF-2 binding site, and a previously undescribed nuclear protein binding site, designated MEF-3, which is also present in a large number of skeletal muscle-specific transcriptional enhancers. Unlike most skeletal muscle-specific transcriptional regulatory elements, the cTnC enhancer does not contain a consensus binding site (CANNTG) for the basic helix-loop-helix (bHLH) family of transcription factors and does not directly bind MyoD-E12 protein complexes. Despite these findings, the cTnC enhancer can be transactivated by overexpression of the myogenic bHLH proteins, MyoD and myogenin, in C3H10T1/2 (10T1/2) cells. Electrophoretic mobility shift assays demonstrated changes in the patterns of MEF-2, CACCC, and MEF-3 DNA binding activities following the conversion of 10T1/2 cells into myoblasts and myotubes by stable transfection with a MyoD expression vector. In particular, MEF-2 binding activity was up-regulated in 10T1/2 cells stably transfected with a MyoD expression vector only after these cells fused and differentiated into skeletal myotubes. Taken together, these results demonstrated that distinct lineage-specific transcriptional regulatory elements control the expression of a single myofibrillar protein gene in fast skeletal and cardiac muscle. In addition, they show that bHLH transcription factors can indirectly transactivate the expression of some muscle-specific genes.

Mol Cell Biol. 1994 March; 14(3): 1870-1885




This article has been cited by other articles:

  • Pennacchio, L. A., Loots, G. G., Nobrega, M. A., Ovcharenko, I. (2007). Predicting tissue-specific enhancers in the human genome. Genome Res 17: 201-211 [Abstract] [Full Text]  
  • Azakie, A., LaMont, L., Fineman, J. R., He, Y. (2005). Divergent transcriptional enhancer factor-1 regulates the cardiac troponin T promoter. Am. J. Physiol. Cell Physiol. 289: C1522-C1534 [Abstract] [Full Text]  
  • Kislinger, T., Gramolini, A. O., Pan, Y., Rahman, K., MacLennan, D. H., Emili, A. (2005). Proteome Dynamics during C2C12 Myoblast Differentiation. Mol. Cell. Proteomics 4: 887-901 [Abstract] [Full Text]  
  • Allen, D. L., Weber, J. N., Sycuro, L. K., Leinwand, L. A. (2005). Myocyte Enhancer Factor-2 and Serum Response Factor Binding Elements Regulate Fast Myosin Heavy Chain Transcription in Vivo. J. Biol. Chem. 280: 17126-17134 [Abstract] [Full Text]  
  • Feriotto, G., Finotti, A., Volpe, P., Treves, S., Ferrari, S., Angelelli, C., Zorzato, F., Gambari, R. (2005). Myocyte Enhancer Factor 2 Activates Promoter Sequences of the Human A{beta}H-J-J Locus, Encoding Aspartyl-{beta}-Hydroxylase, Junctin, and Junctate. Mol. Cell. Biol. 25: 3261-3275 [Abstract] [Full Text]  
  • Viger, R. S., Taniguchi, H., Robert, N. M., Tremblay, J. J. (2004). The 25th Volume: Role of the GATA Family of Transcription Factors in Andrology. J Androl 25: 441-452 [Full Text]  
  • Himeda, C. L., Ranish, J. A., Angello, J. C., Maire, P., Aebersold, R., Hauschka, S. D. (2004). Quantitative Proteomic Identification of Six4 as the Trex-Binding Factor in the Muscle Creatine Kinase Enhancer. Mol. Cell. Biol. 24: 2132-2143 [Abstract] [Full Text]  
  • Brady, M., Koban, M. U, Dellow, K. A, Yacoub, M., Boheler, K. R, Fuller, S. J (2003). Sp1 and Sp3 transcription factors are required for trans-activation of the human SERCA2 promoter in cardiomyocytes. Cardiovasc Res 60: 347-354 [Abstract] [Full Text]  
  • Karasseva, N., Tsika, G., Ji, J., Zhang, A., Mao, X., Tsika, R. (2003). Transcription Enhancer Factor 1 Binds Multiple Muscle MEF2 and A/T-Rich Elements during Fast-to-Slow Skeletal Muscle Fiber Type Transitions. Mol. Cell. Biol. 23: 5143-5164 [Abstract] [Full Text]  
  • Swamynathan, S. K., Piatigorsky, J. (2002). Orientation-dependent Influence of an Intergenic Enhancer on the Promoter Activity of the Divergently Transcribed Mouse Shsp/alpha B-crystallin and Mkbp/HspB2 Genes. J. Biol. Chem. 277: 49700-49706 [Abstract] [Full Text]  
  • Sato, S., Nakamura, M., Cho, D. H., Tapscott, S. J., Ozaki, H., Kawakami, K. (2002). Identification of transcriptional targets for Six5: implication for the pathogenesis of myotonic dystrophy type 1. Hum Mol Genet 11: 1045-1058 [Abstract] [Full Text]  
  • Calvo, S., Vullhorst, D., Venepally, P., Cheng, J., Karavanova, I., Buonanno, A. (2001). Molecular Dissection of DNA Sequences and Factors Involved in Slow Muscle-Specific Transcription. Mol. Cell. Biol. 21: 8490-8503 [Abstract] [Full Text]  
  • Dellow, K. A., Bhavsar, P. K., Brand, N. J., Barton, P. J.R. (2001). Identification of novel, cardiac-restricted transcription factors binding to a CACC-box within the human cardiac troponin I promoter. Cardiovasc Res 50: 24-33 [Abstract] [Full Text]  
  • Harris, S. E., Winchester, C. L., Johnson, K. J. (2000). Functional analysis of the homeodomain protein SIX5. Nucleic Acids Res 28: 1871-1878 [Abstract] [Full Text]  
  • Mitchell-Felton, H., Kandarian, S. C. (1999). Normalization of muscle plasmid uptake by Southern blot: application to SERCA1 promoter analysis. Am. J. Physiol. Cell Physiol. 277: C1269-C1276 [Abstract] [Full Text]  
  • Rao, S., Garrett-Sinha, L. A., Yoon, J., Simon, M. C. (1999). The Ets Factors PU.1 and Spi-B Regulate the Transcription in Vivo of P2Y10, a Lymphoid Restricted Heptahelical Receptor. J. Biol. Chem. 274: 34245-34252 [Abstract] [Full Text]  
  • Vyas, D. R., McCarthy, J. J., Tsika, R. W. (1999). Nuclear Protein Binding at the beta -Myosin Heavy Chain A/T-rich Element Is Enriched following Increased Skeletal Muscle Activity. J. Biol. Chem. 274: 30832-30842 [Abstract] [Full Text]  
  • Peters, D. G., Mitchell-Felton, H., Kandarian, S. C. (1999). Unloading induces transcriptional activation of the sarco(endo)plasmic reticulum Ca2+-ATPase 1 gene in muscle. Am. J. Physiol. Cell Physiol. 276: C1218-C1225 [Abstract] [Full Text]  
  • Esser, K., Nelson, T., Lupa-Kimball, V., Blough, E. (1999). The CACC Box and Myocyte Enhancer Factor-2 Sites within the Myosin Light Chain 2 Slow Promoter Cooperate in Regulating Nerve-specific Transcription in Skeletal Muscle. J. Biol. Chem. 274: 12095-12102 [Abstract] [Full Text]  
  • Rao, S., Matsumura, A., Yoon, J., Simon, M. C. (1999). SPI-B Activates Transcription via a Unique Proline, Serine, and Threonine Domain and Exhibits DNA Binding Affinity Differences from PU.1. J. Biol. Chem. 274: 11115-11124 [Abstract] [Full Text]  
  • Calvo, S., Venepally, P., Cheng, J., Buonanno, A. (1999). Fiber-Type-Specific Transcription of the Troponin I Slow Gene Is Regulated by Multiple Elements. Mol. Cell. Biol. 19: 515-525 [Abstract] [Full Text]  
  • Spitz, F., Demignon, J., Porteu, A., Kahn, A., Concordet, J.-P., Daegelen, D., Maire, P. (1998). Expression of myogenin during embryogenesis is controlled by Six/sine oculis homeoproteins through a conserved MEF3 binding site. Proc. Natl. Acad. Sci. USA 95: 14220-14225 [Abstract] [Full Text]  
  • O'Mahoney, J. V., Guven, K. L., Lin, J., Joya, J. E., Robinson, C. S., Wade, R. P., Hardeman, E. C. (1998). Identification of a Novel Slow-Muscle-Fiber Enhancer Binding Protein, MusTRD1. Mol. Cell. Biol. 18: 6641-6652 [Abstract] [Full Text]  
  • Gao, J., Li, Z., Paulin, D. (1998). A Novel Site, Mt, in the Human Desmin Enhancer Is Necessary for Maximal Expression in Skeletal Muscle. J. Biol. Chem. 273: 6402-6409 [Abstract] [Full Text]  
  • Lupa-Kimball, V. A., Esser, K. A. (1998). Use of DNA injection for identification of slow nerve-dependent regions of the MLC2s gene. Am. J. Physiol. Cell Physiol. 274: C229-C235 [Abstract] [Full Text]  
  • Qin, W., Khuchua, Z., Klein, S. C., Strauss, A. W. (1997). Elements Regulating Cardiomyocyte Expression of the Human Sarcomeric Mitochondrial Creatine Kinase Gene in Transgenic Mice. J. Biol. Chem. 272: 25210-25216 [Abstract] [Full Text]  
  • Morrisey, E. E., Ip, H. S., Tang, Z., Parmacek, M. S. (1997). GATA-4 Activates Transcription Via Two Novel Domains That Are Conserved within the GATA-4/5/6 Subfamily. J. Biol. Chem. 272: 8515-8524 [Abstract] [Full Text]  
  • Lin, S., Lin, M., Horvath, P, Reddy, K., Storti, R. (1997). PDP1, a novel Drosophila PAR domain bZIP transcription factor expressed in developing mesoderm, endoderm and ectoderm, is a transcriptional regulator of somatic muscle genes. Development 124: 4685-4696 [Abstract]  
  • Ritchie, M. E., Ritchie, M. E. (1996). Characterization of Human B Creatine Kinase Gene Regulation in the Heart in Vitro and in Vivo. J. Biol. Chem. 271: 25485-25491 [Abstract] [Full Text]  
  • Ornatsky, O. I., McDermott, J. C. (1996). MEF2 Protein Expression, DNA Binding Specificity and Complex Composition, and Transcriptional Activity in Muscle and Non-muscle Cells. J. Biol. Chem. 271: 24927-24933 [Abstract] [Full Text]  
  • Ziober, B. L., Kramer, R. H. (1996). Identification and Characterization of the Cell Type-specific and Developmentally Regulated alpha 7 Integrin Gene Promoter. J. Biol. Chem. 271: 22915-22922 [Abstract] [Full Text]  
  • Wang, G. F., Nikovits, W. Jr., Schleinitz, M., Stockdale, F. E. (1996). Atrial Chamber-specific Expression of the Slow Myosin Heavy Chain 3Gene in the Embryonic Heart. J. Biol. Chem. 271: 19836-19845 [Abstract] [Full Text]  
  • Nikovits, W. Jr., Wang, G. F., Feldman, J. L., Miller, J. B., Wade, R., Nelson, L., Stockdale, F. E. (1996). Isolation and Characterization of an Avian Slow Myosin Heavy Chain Gene Expressed during Embryonic Skeletal Muscle Fiber Formation. J. Biol. Chem. 271: 17047-17056 [Abstract] [Full Text]  
  • Watanabe, M., Sakomura, Y., Kurabayashi, M., Manabe, I., Aikawa, M., Kuro-o, M., Suzuki, T., Yazaki, Y., Nagai, R. (1996). Structure and Characterization of the 5'-Flanking Region of the Mouse Smooth Muscle Myosin Heavy Chain (SM1/2) Gene. Circ. Res. 78: 978-989 [Abstract] [Full Text]  
  • Fabre-Suver, C., Hauschka, S. D. (1996). A Novel Site in the Muscle Creatine Kinase Enhancer Is Required for Expression in Skeletal but Not Cardiac Muscle. J. Biol. Chem. 271: 4646-4652 [Abstract] [Full Text]  
  • Schmoelzl, S., Leeb, T., Brinkmeier, H., Brem, G., Brenig, B. (1996). Regulation of Tissue-specific Expression of the Skeletal Muscle Ryanodine Receptor Gene. J. Biol. Chem. 271: 4763-4769 [Abstract] [Full Text]  
  • Wan, B., Moreadith, R. W. (1995). Structural Characterization and Regulatory Element Analysis of the Heart Isoform of Cytochrome c Oxidase VIa. J. Biol. Chem. 270: 26433-26440 [Abstract] [Full Text]  
  • Solway, J., Seltzer, J., Samaha, F. F., Kim, S., Alger, L. E., Niu, Q., Morrisey, E. E., Ip, H. S., Parmacek, M. S. (1995). Structure and Expression of a Smooth Muscle Cell-specific Gene, SM22[IMAGE]. J. Biol. Chem. 270: 13460-13469 [Abstract] [Full Text]  
  • Mitchell-Felton, H., Hunter, R. B., Stevenson, E. J., Kandarian, S. C. (2000). Identification of Weight-bearing-responsive Elements in the Skeletal Muscle Sarco(endo)plasmic Reticulum Ca2+ ATPase (SERCA1) Gene. J. Biol. Chem. 275: 23005-23011 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»