8
Views
56
CrossRef citations to date
0
Altmetric
Cell Growth and Development

A Ras-Dependent Pathway Regulates RNA Polymerase II Phosphorylation in Cardiac Myocytes: Implications for Cardiac Hypertrophy

, , , , &
Pages 6729-6736 | Received 23 Apr 1998, Accepted 04 Aug 1998, Published online: 28 Mar 2023

REFERENCES

  • Abdellatif, M., W. R. MacLellan, and M. D. Schneider 1994. p21 Ras as a governer of global gene expression. J. Biol. Chem. 269: 15423–15426.
  • Abdellatif, M., and M. D. Schneider 1997. An effector-like function of Ras GTPase-activating protein predominates in cardiac muscle cells. J. Biol. Chem. 272: 525–533.
  • Allo, S. N., L. L. Carl, and H. E. Morgan 1992. Acceleration of growth of cultured cardiomyocytes and translocation of protein kinase C. Am. J. Physiol. 263: C319–C325.
  • Bader, D., T. Masaki, and D. A. Fischman 1982. Immunocytochemical analysis of myosin heavy chain during avian myogenesis in vivo. J. Cell Biol. 95: 763–770.
  • Bishopric, N. H., P. C. Simpson, and C. Ordahl 1987. Induction of the skeletal α-actin gene in α1-adrenoreceptor-mediated hypertrophy of rat cardiac myocytes. J. Clin. Investig. 80: 1194–1199.
  • Bregman, D. B., L. Du, Y. Li, S. Ribisi, and S. L. Warren 1994. Cytostellin distributes to nuclear regions enriched with splicing factors. J. Cell Sci. 107: 387–396.
  • Bregman, D. B., L. Du, S. van der Zee, and S. L. Warren 1995. Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains. J. Cell Biol. 129: 287–298.
  • Brill, S., S. Li, C. W. Lyman, D. M. Church, J. J. Wasmuth, L. Weissbach, A. Bernards, and A. J. Snijders 1996. The Ras GTPase-activating-protein-related human protein IQGAP2 harbors a potential actin binding domain and interacts with calmodulin and Rho family GTPases. Mol. Cell. Biol. 16: 4869–4878.
  • Cadena, D. L., and M. E. Dahmus 1987. Messenger RNA synthesis in mammalian cells is catalyzed by the phosphorylated form of RNA polymerase II. J. Biol. Chem. 262: 12468–12474.
  • Cutilletta, A. F., M. Rudnik, and R. Zak 1978. Muscle and non-muscle cell RNA polymerase activity during the development of myocardial hypertrophy. J. Mol. Cell. Cardiol. 10: 677–687.
  • DeClue, J. E., W. C. Vass, M. R. Johnson, D. W. Stacey, and D. R. Lowy 1993. Functional role of GTPase-activating protein in cell transformation by pp60v-src. Mol. Cell. Biol. 13: 6799–6809.
  • DePaolo, D., J. E.-B. Beusch, K. Carel, P. Bhuripanyo, J. W. Leitner, and B. Draznin 1996. Functional interaction of phosphatidylinositol 3-kinase with GTPase-activating protein in 3T3-L1 adipocytes. Mol. Cell. Biol. 16: 1450–1457.
  • Du, L., and S. L. Warren 1997. A functional interaction between the carboxy-terminal domain of RNA polymerase II and pre-mRNA splicing. J. Cell Biol. 136: 5–18.
  • Dubois, M.-F., V. T. Nguyen, M. E. Dahmus, G. Pages, J. Poussegur, and O. Bensaude 1994. Enhanced phosphorylation of the C-terminal domain of RNA polymerase II upon serum stimulation of quiescent cells: possible involvement of MAP kinases. EMBO J. 13: 4787–4797.
  • Duchesne, M., F. Schweighoffer, F. Parker, F. Clerc, Y. Frobert, M. N. Thang, and B. Tocqué 1993. Identification of the SH3 domain of GAP as an essential sequence for GAP-mediated signaling. Science 259: 525–528.
  • Feaver, W. J., J. Q. Svejstrup, N. L. Henry, and R. D. Kornberg 1994. Relationship of CDK-activating kinase and RNA polymerase II CTD kinase TFIIH/TFIIK. Cell 79: 1103–1109.
  • Gerber, H.-P., M. Hagmann, K. Seipel, O. Georgiev, M. A. L. West, Y. Litingtung, W. Schaffner, and J. Corden 1995. RNA polymerase II C-terminal domain required for enhancer-driven transcription. Nature 374: 660–662.
  • Gideon, P., J. John, M. Frech, A. Lautwein, R. Clark, J. E. Scheffler, and A. Wittinghofer 1992. Mutational and kinetic analyses of the GTPase-activating protein (GAP)–p21 interaction: the C-terminal domain of GAP is not sufficient for full activity. Mol. Cell. Biol. 12: 2050–2056.
  • Glennon, P. E., S. Kaddoura, E. M. Sale, G. J. Sale, S. J. Fuller, and P. H. Sugden 1996. Depletion of mitogen-activated protein kinase using an antisense oligodeoxynucleotide approach downregulates the phenylephrine-induced hypertrophic response in rat cardiac myocytes. Circ. Res. 78: 954–961.
  • Graham, F. L., and L. Prevec 1991. Methods in molecular biology 7 The Humana Press Inc., Clifton, N.J.
  • Hines, W. A., and A. Thorburn 1998. Ras and rho are required for α-induced hypertrophic gene expression in neonatal rat cardiac myocytes. J. Mol. Cell. Cardiol. 30: 485–494.
  • Hoshijima, M., V. P. Sah, Y. Wang, K. R. Chien, and J. H. Brown 1998. The low molecular weight GTPase rho regulates myofibril formation and organization in neonatal rat ventricular myocytes. Involvement of rho kinase. J. Biol. Chem. 273: 7725–7730.
  • Hunter, J. J., H. A. Rockman, and K. R. Chien 1994. Left ventricular hypertrophy produced by tissue-targeted expression of activated Ras in transgenic mice. Circulation 90: I-197 (Abstract.)
  • Hunter, J. J., N. Tanaka, H. A. Rockman, J. Ross, and K. R. Chien 1995. Ventricular expression of a MLC-2v-ras fusion gene induces cardiac hypertrophy and selective diastolic dysfunction in transgenic mice. J. Biol. Chem. 270: 23173–23178.
  • Kako, K. J., K. Varnai, and M. Beznak 1972. RNA synthesis and RNA content of nuclei prepared from hearts during hypertrophy. Cardiovasc. Res. 6: 56–66.
  • Kariya, K., L. R. Karns, and P. C. Simpson 1994. An enhancer core element mediates stimulation of the rat beta-myosin heavy chain promoter by an alpha 1-adrenergic agonist and activated beta-protein kinase C in hypertrophy of cardiac myocytes. J. Biol. Chem. 269: 3775–3782.
  • Kim, W.-Y., and M. E. Dahmus 1986. Immunochemical analysis of mammalian RNA polymerase II subspecies. J. Biol. Chem. 261: 14219–14225.
  • Kirshenbaum, L. A., W. R. MacLellan, W. Mazur, B. A. French, and M. D. Schneider 1993. Highly efficient gene transfer to adult rat ventricular myocytes by recombinant adenovirus. J. Clin. Investig. 92: 381–387.
  • Kirshenbaum, L. A., and M. D. Schneider 1995. Adenovirus E1A represses cardiac gene transcription and reactivates DNA synthesis in ventricular myocytes, via alternative pocket protein- and p300-binding domains. J. Biol. Chem. 270: 7791–7794.
  • Kirshenbaum, L., A. Abdellatif, M. Chakraborty, and M. D. Schneider. Human E2F-1 reactivates cell cycle progression in ventricular myocytes and represses cardiac gene transcription. Dev. Biol. 179:402–411.
  • Koide, T., and M. Rabinowitz 1969. Biochemical correlates of cardiac hypertrophy. II. Increased rate of RNA synthesis in experimental cardiac hypertrophy in the rat. Circ. Res. 24: 9–18.
  • LaMorte, V. J., J. Thorburn, D. Absher, A. Spiegel, J. H. Brown, K. R. Chien, J. R. Feramisco, and K. Knowlton 1994. Gq- and Ras-dependent pathways mediate hypertrophy of neonatal rat ventricular myocytes following α1-adrenergic stimulation. J. Biol. Chem. 269: 13490–13496.
  • Laybourn, P. J., and M. E. Dahmus 1990. Phosphorylation of RNA polymerase IIA occurs subsequent to interaction with the promoter and before initiation of transcription. J. Biol. Chem. 265: 13165–13173.
  • Lu, H., O. Flores, R. Weinmann, and D. Reinberg 1991. The nonphosphorylated form of RNA polymerase II preferentially associates with the preinitiation complex. Proc. Natl. Acad. Sci. USA 88: 10004–10008.
  • MacLellan, W. R., T. C. Lee, R. J. Schwartz, and M. D. Schneider 1994. Transforming growth factor-beta response elements of the skeletal alpha-actin gene. Combinatorial action of serum response factor, YY1, and the SV40 enhancer-binding protein, TEF-1. J. Biol. Chem. 269: 16754–16760.
  • Mäkelä, T. P., J. D. Parvin, J. Kim, L. J. Huber, P. A. Sharp, and R. A. Weinberg 1995. A kinase-deficient transcription factor TFIIH is functional in basal and activated transcription. Proc. Natl. Acad. Sci. USA 92: 5174–5178.
  • Martin, G. A., A. Yatani, R. Clark, L. Conroy, P. Polakis, A. M. Brown, and F. McCormick 1992. GAP domains responsible for Ras p21-dependent inhibition of muscarinic atrial K channel currents. Science 255: 192–194.
  • McDermott, P. J., L. L. Carl, K. J. Conner, and S. N. Allo 1991. Transcriptional regulation of ribosomal RNA synthesis during growth of cardiac myocytes in culture. J. Biol. Chem. 266: 4409–4416.
  • McDermott, P. J., L. I. Rothblum, S. D. Smith, and H. E. Morgan 1989. Accelerated rates of ribosomal RNA synthesis during growth of contracting heart cells in culture. J. Biol. Chem. 264: 18220–18227.
  • McGlade, J., B. Brunkhorst, D. Anderson, G. Mbamalu, J. Settleman, S. Dedhar, M. Rozakis-Adcock, L. B. Chen, and T. Pawson 1993. The N-terminal region of GAP regulates cytoskeletal structure and cell adhesion. EMBO J. 12: 3073–3081.
  • Medema, R., W. L. D. Laat, G. A. Martin, F. McCormick, and J. L. Bos 1992. GTPase-activating protein SH2-SH3 domains induce gene expression in a ras-dependent fashion. Mol. Cell. Biol. 12: 3425–3430.
  • Miao, W., L. Eichelberger, L. Baker, and M. S. Marshall 1996. p120 Ras GTPase-activating protein interacts with Ras-GTP through specific conserved residues. J. Biol. Chem. 271: 15322–15329.
  • Nair, K. G., A. F. Cutilletta, R. Zak, T. Koide, and M. Rabinowitz 1968. Biochemical correlates of cardiac hypertrophy. I. Experimental model; changes in heart weight, RNA content, and nuclear RNA polymerase activity. Circ. Res. 23: 451–462.
  • O’Brien, T., S. Hardin, A. Greenleaf, and J. T. Lis 1994. Phosphorylation of RNA polymerase II C-terminal domain and transcriptional elongation. Nature 370: 75–77.
  • Paradis, P., W. R. MacLellan, N. S. Belaguli, R. J. Schwartz, and M. D. Schneider 1996. Serum response factor mediates AP-1-dependent induction of the skeletal alpha-actin promoter in ventricular myocytes. J. Biol. Chem. 271: 10827–10833.
  • Parker, A., F. Maurier, I. Delumeau, M. Duchesne, D. Faucher, L. Debussche, A. Dugue, F. Schweighoffer, and B. Tocque 1996. A Ras-GTPase-activating protein SH3-domain-binding protein. Mol. Cell. Biol. 16: 2561–2569.
  • Parker, T. G., K. L. Chow, R. J. Schwartz, and M. D. Schneider 1992. Positive and negative control of the skeletal alpha-actin promoter in cardiac muscle. A proximal serum response element is sufficient for induction by basic fibroblast growth factor (FGF) but not for inhibition by acidic FGF. J. Biol. Chem. 267: 3343–3350.
  • Ramirez, M. T., G. R. Post, P. V. Sulakhe, and J. H. Brown 1995. M1 muscarinic receptors heterologously expressed in cardiac myocytes mediate Ras-dependent changes in gene expression. J. Biol. Chem. 270: 8446–8451.
  • Sadoshima, J., and S. Izumo 1995. Rapamycin selectively inhibits angiotensin II-induced increase in protein synthesis in cardiac myocytes in vitro. Circ. Res. 77: 1040–1052.
  • Sadoshima, J.-I., and S. Izumo 1993. Signal transduction pathways of angiotensin II induced c-fos gene expression in cardiac myocytes in vitro. Circ. Res. 73: 424–438.
  • Serizawa, H., T. P. Makela, J. W. Conaway, R. A. Weinberg, and R. A. Young 1995. Association of Cdk-activating kinase subunits with transcription factor TFIIH. Nature 374: 270–282.
  • Settleman, J., V. Narasimhan, L. C. Foster, and R. Weinberg 1992. Molecular cloning of cDNAs encoding the GAP-associated protein p190: implications for a signaling pathway from Ras to the nucleus. Cell 69: 539–549.
  • Settleman, J., V. Narasimhan, L. C. Foster, and R. Weinberg 1992. Molecular cloning of cDNAs encoding the GAP-associated protein p190: implications for a signaling pathway from Ras to the nucleus. Cell 69: 539–549.
  • Shiekhattar, R., F. Mermeistein, R. P. Fisher, R. Drapkin, B. Dynlacht, H. Wessling, D. Morgan, and D. Reinberg 1995. Cdk-activating kinase complex is a component of human transcription factor TFIIH. Nature 374: 283–287.
  • Swynghedauw, B., J. M. Moalic, P. Bouveret, J. Bercovici, D. D. L. Bastie, and K. Schwartz 1984. Messenger RNA content and complexity in normal and overloaded rat heart: a preliminary report. Eur. Heart J. 5: 211–217.
  • Thorburn, A. 1994. Ras activity is required for phenylephrine-induced activation of mitogen-activated protein kinase in cardiac muscle cells. Biochem. Biophys. Res. Commun. 205: 1417–1422.
  • Thorburn, A., J. Thorburn, S. Y. Chen, S. Powers, H. E. Shubeita, J. R. Feramisco, and K. R. Chien 1993. HRas-dependent pathways can activate morphological and genetic markers of cardiac muscle cell hypertrophy. J. Biol. Chem. 268: 2244–2249 (Erratum, 268:16082.)
  • Thorburn, J., J. A. Frost, and A. Thorburn 1994. Mitogen-activated protein kinases mediate changes in gene expression, but not cytoskeletal organization associated with cardiac muscle cell hypertrophy. J. Cell Biol. 126: 1565–1572.
  • Thorburn, J., M. McMahon, and A. Thorburn 1994. Raf-1 kinase activity is necessary and sufficient for gene expression changes but not sufficient for cellular morphology changes associated with cardiac myocyte hypertrophy. J. Biol. Chem. 269: 30580–30586.
  • Thorburn, J., S. Xu, and A. Thorburn 1997. MAP kinase- and Rho-dependent signals interact to regulate gene expression but not actin morphology in cardiac muscle cells. EMBO J. 16: 1888–1900.
  • Wada, H., C. T. Ivester, B. A. Carabello, G. T. Cooper, and P. J. McDermott 1996. Translational initiation factor eIF-4E: a link between cardiac load and protein synthesis. J. Biol. Chem. 271: 8359–8364.
  • Wang, Y., S. Huang, V. P. Sah, Ross J., Jr., J. H. Brown, J. Han, and K. R. Chien 1998. Cardiac muscle cell hypertrophy and apoptosis induced by distinct members of the p38 mitogen-activated protein kinase family. J. Biol. Chem. 273: 2161–2168.
  • Wang, Y., B. Su, V. P. Sah, J. H. Brown, J. Han, and K. R. Chien 1998. Cardiac hypertrophy induced by mitogen-activated protein kinase kinase 7, a specific activator for c-Jun NH2-terminal kinase in ventricular muscle cells. J. Biol. Chem. 273: 5423–5426.
  • Wong, G., O. Müller, R. Clark, L. Conroy, M. F. Moran, P. Polakis, and F. McCormick 1992. Molecular cloning and nucleic acid binding properties of the GAP-associated tyrosine phosphoprotein p62. Cell 69: 551–558.
  • Yatani, A., K. Okabe, P. Polakis, R. Halenbeck, F. McCormick, and A. M. Brown 1990. Ras p21 and Gap inhibit coupling of muscarinic receptors of atrial K channels. Cell 61: 769–776.
  • Yuryev, A., M. Patturajan, Y. Litingtung, R. V. Joshi, C. Gentile, M. Gebara, and J. Corden 1996. The C-terminal domain of the largest subunit of RNA polymerase II interact with a novel set of serine/threonine-rich proteins. Proc. Natl. Acad. Sci. USA 93: 6975–6980.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.