This Article
Right arrow Full Text
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 Chang, S.
Right arrow Articles by Olson, E. N.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Chang, S.
Right arrow Articles by Olson, E. N.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, October 2004, p. 8467-8476, Vol. 24, No. 19
0270-7306/04/$08.00+0     DOI: 10.1128/MCB.24.19.8467-8476.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Histone Deacetylases 5 and 9 Govern Responsiveness of the Heart to a Subset of Stress Signals and Play Redundant Roles in Heart Development

Shurong Chang,1,{dagger} Timothy A. McKinsey,2,{dagger} Chun Li Zhang,1 James A. Richardson,1,3 Joseph A. Hill,1,4 and Eric N. Olson1*

Departments of Molecular Biology,1 Pathology,3 Cardiology, University of Texas Southwestern Medical Center, Dallas, Texas,4 Myogen, Inc., Westminster, Colorado2

Received 26 May 2004/ Returned for modification 17 June 2004/ Accepted 10 July 2004

The adult heart responds to stress signals by hypertrophic growth, which is often accompanied by activation of a fetal cardiac gene program and eventual cardiac demise. We showed previously that histone deacetylase 9 (HDAC9) acts as a suppressor of cardiac hypertrophy and that mice lacking HDAC9 are sensitized to cardiac stress signals. Here we report that mice lacking HDAC5 display a similar cardiac phenotype and develop profoundly enlarged hearts in response to pressure overload resulting from aortic constriction or constitutive cardiac activation of calcineurin, a transducer of cardiac stress signals. In contrast, mice lacking either HDAC5 or HDAC9 show a hypertrophic response to chronic ß-adrenergic stimulation identical to that of wild-type littermates, suggesting that these HDACs modulate a specific subset of cardiac stress response pathways. We also show that compound mutant mice lacking both HDAC5 and HDAC9 show a propensity for lethal ventricular septal defects and thin-walled myocardium. These findings reveal central roles for HDACs 5 and 9 in the suppression of a subset of cardiac stress signals as well as redundant functions in the control of cardiac development.

* Corresponding author. Mailing address: Department of Molecular Biology, University of Texas Southwestern Medical Center, 6000 Harry Hines Blvd., Dallas, TX 75390-9148. Phone: (214) 648-1187. Fax: (214) 648-1187. E-mail: eolson{at}hamon.swmed.edu.

{dagger} S.C. and T.A.M. contributed equally.

Molecular and Cellular Biology, October 2004, p. 8467-8476, Vol. 24, No. 19
0022-538X/04/$08.00+0     DOI: 10.1128/MCB.24.19.8467-8476.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Chandrasekaran, S., Peterson, R. E., Mani, S. K., Addy, B., Buchholz, A. L., Xu, L., Thiyagarajan, T., Kasiganesan, H., Kern, C. B., Menick, D. R. (2009). Histone deacetylases facilitate sodium/calcium exchanger up-regulation in adult cardiomyocytes. FASEB J. 23: 3851-3864 [Abstract] [Full Text]  
  • Cadot, B., Brunetti, M., Coppari, S., Fedeli, S., de Rinaldis, E., Russo, C. D., Gallinari, P., De Francesco, R., Steinkuhler, C., Filocamo, G. (2009). Loss of Histone Deacetylase 4 Causes Segregation Defects during Mitosis of p53-Deficient Human Tumor Cells. Cancer Res. 69: 6074-6082 [Abstract] [Full Text]  
  • Marchion, D. C., Bicaku, E., Turner, J. G., Schmitt, M. L., Morelli, D. R., Munster, P. N. (2009). HDAC2 regulates chromatin plasticity and enhances DNA vulnerability. Molecular Cancer Therapeutics 8: 794-801 [Abstract] [Full Text]  
  • Glenn, D. J., Wang, F., Chen, S., Nishimoto, M., Gardner, D. G. (2009). Endothelin-Stimulated Human B-Type Natriuretic Peptide Gene Expression Is Mediated by Yin Yang 1 in Association With Histone Deacetylase 2. Hypertension 53: 549-555 [Abstract] [Full Text]  
  • Jensen, E. D., Gopalakrishnan, R., Westendorf, J. J. (2009). Bone Morphogenic Protein 2 Activates Protein Kinase D to Regulate Histone Deacetylase 7 Localization and Repression of Runx2. J. Biol. Chem. 284: 2225-2234 [Abstract] [Full Text]  
  • Duong, V., Bret, C., Altucci, L., Mai, A., Duraffourd, C., Loubersac, J., Harmand, P.-O., Bonnet, S., Valente, S., Maudelonde, T., Cavailles, V., Boulle, N. (2008). Specific Activity of Class II Histone Deacetylases in Human Breast Cancer Cells. Mol Cancer Res 6: 1908-1919 [Abstract] [Full Text]  
  • Gallo, P., Latronico, M. V.G., Gallo, P., Grimaldi, S., Borgia, F., Todaro, M., Jones, P., Gallinari, P., De Francesco, R., Ciliberto, G., Steinkuhler, C., Esposito, G., Condorelli, G. (2008). Inhibition of class I histone deacetylase with an apicidin derivative prevents cardiac hypertrophy and failure. Cardiovasc Res 80: 416-424 [Abstract] [Full Text]  
  • Haumaitre, C., Lenoir, O., Scharfmann, R. (2008). Histone Deacetylase Inhibitors Modify Pancreatic Cell Fate Determination and Amplify Endocrine Progenitors. Mol. Cell. Biol. 28: 6373-6383 [Abstract] [Full Text]  
  • Granger, A., Abdullah, I., Huebner, F., Stout, A., Wang, T., Huebner, T., Epstein, J. A., Gruber, P. J. (2008). Histone deacetylase inhibition reduces myocardial ischemia-reperfusion injury in mice. FASEB J. 22: 3549-3560 [Abstract] [Full Text]  
  • Trivedi, C. M., Lu, M. M., Wang, Q., Epstein, J. A. (2008). Transgenic Overexpression of Hdac3 in the Heart Produces Increased Postnatal Cardiac Myocyte Proliferation but Does Not Induce Hypertrophy. J. Biol. Chem. 283: 26484-26489 [Abstract] [Full Text]  
  • Martini, J. S., Raake, P., Vinge, L. E., DeGeorge, B. R. Jr., Chuprun, J. K., Harris, D. M., Gao, E., Eckhart, A. D., Pitcher, J. A., Koch, W. J. (2008). Uncovering G protein-coupled receptor kinase-5 as a histone deacetylase kinase in the nucleus of cardiomyocytes. Proc. Natl. Acad. Sci. USA 105: 12457-12462 [Abstract] [Full Text]  
  • Wei, J. Q., Shehadeh, L. A., Mitrani, J. M., Pessanha, M., Slepak, T. I., Webster, K. A., Bishopric, N. H. (2008). Quantitative Control of Adaptive Cardiac Hypertrophy by Acetyltransferase p300. Circulation 118: 934-946 [Abstract] [Full Text]  
  • Marumo, T., Hishikawa, K., Yoshikawa, M., Fujita, T. (2008). Epigenetic Regulation of BMP7 in the Regenerative Response to Ischemia. J. Am. Soc. Nephrol. 19: 1311-1320 [Abstract] [Full Text]  
  • Wang, S., Li, X., Parra, M., Verdin, E., Bassel-Duby, R., Olson, E. N. (2008). Control of endothelial cell proliferation and migration by VEGF signaling to histone deacetylase 7. Proc. Natl. Acad. Sci. USA 105: 7738-7743 [Abstract] [Full Text]  
  • Feng, B., Chen, S., Chiu, J., George, B., Chakrabarti, S. (2008). Regulation of cardiomyocyte hypertrophy in diabetes at the transcriptional level. Am. J. Physiol. Endocrinol. Metab. 294: E1119-E1126 [Abstract] [Full Text]  
  • Ha, C. H., Wang, W., Jhun, B. S., Wong, C., Hausser, A., Pfizenmaier, K., McKinsey, T. A., Olson, E. N., Jin, Z.-G. (2008). Protein Kinase D-dependent Phosphorylation and Nuclear Export of Histone Deacetylase 5 Mediates Vascular Endothelial Growth Factor-induced Gene Expression and Angiogenesis. J. Biol. Chem. 283: 14590-14599 [Abstract] [Full Text]  
  • Backs, J., Backs, T., Bezprozvannaya, S., McKinsey, T. A., Olson, E. N. (2008). Histone Deacetylase 5 Acquires Calcium/Calmodulin-Dependent Kinase II Responsiveness by Oligomerization with Histone Deacetylase 4. Mol. Cell. Biol. 28: 3437-3445 [Abstract] [Full Text]  
  • Pang, J., Yan, C., Natarajan, K., Cavet, M. E., Massett, M. P., Yin, G., Berk, B. C. (2008). GIT1 Mediates HDAC5 Activation by Angiotensin II in Vascular Smooth Muscle Cells. Arterioscler. Thromb. Vasc. Bio. 28: 892-898 [Abstract] [Full Text]  
  • Schuetz, A., Min, J., Allali-Hassani, A., Schapira, M., Shuen, M., Loppnau, P., Mazitschek, R., Kwiatkowski, N. P., Lewis, T. A., Maglathin, R. L., McLean, T. H., Bochkarev, A., Plotnikov, A. N., Vedadi, M., Arrowsmith, C. H. (2008). Human HDAC7 Harbors a Class IIa Histone Deacetylase-specific Zinc Binding Motif and Cryptic Deacetylase Activity. J. Biol. Chem. 283: 11355-11363 [Abstract] [Full Text]  
  • Bossuyt, J., Helmstadter, K., Wu, X., Clements-Jewery, H., Haworth, R. S., Avkiran, M., Martin, J. L., Pogwizd, S. M., Bers, D. M. (2008). Ca2+/Calmodulin-Dependent Protein Kinase II{delta} and Protein Kinase D Overexpression Reinforce the Histone Deacetylase 5 Redistribution in Heart Failure. Circ. Res. 102: 695-702 [Abstract] [Full Text]  
  • Martin, M., Potente, M., Janssens, V., Vertommen, D., Twizere, J.-C., Rider, M. H., Goris, J., Dimmeler, S., Kettmann, R., Dequiedt, F. (2008). Protein phosphatase 2A controls the activity of histone deacetylase 7 during T cell apoptosis and angiogenesis. Proc. Natl. Acad. Sci. USA 105: 4727-4732 [Abstract] [Full Text]  
  • Fielitz, J., Kim, M.-S., Shelton, J. M., Qi, X., Hill, J. A., Richardson, J. A., Bassel-Duby, R., Olson, E. N. (2008). Requirement of protein kinase D1 for pathological cardiac remodeling. Proc. Natl. Acad. Sci. USA 105: 3059-3063 [Abstract] [Full Text]  
  • Colella, M., Grisan, F., Robert, V., Turner, J. D., Thomas, A. P., Pozzan, T. (2008). Ca2+ oscillation frequency decoding in cardiac cell hypertrophy: Role of calcineurin/NFAT as Ca2+ signal integrators. Proc. Natl. Acad. Sci. USA 105: 2859-2864 [Abstract] [Full Text]  
  • Potthoff, M. J., Olson, E. N. (2007). MEF2: a central regulator of diverse developmental programs. Development 134: 4131-4140 [Abstract] [Full Text]  
  • Zhao, T. C., Cheng, G., Zhang, L. X., Tseng, Y. T., Padbury, J. F. (2007). Inhibition of histone deacetylases triggers pharmacologic preconditioning effects against myocardial ischemic injury. Cardiovasc Res 76: 473-481 [Abstract] [Full Text]  
  • Zhang, T., Kohlhaas, M., Backs, J., Mishra, S., Phillips, W., Dybkova, N., Chang, S., Ling, H., Bers, D. M., Maier, L. S., Olson, E. N., Brown, J. H. (2007). CaMKII{delta} Isoforms Differentially Affect Calcium Handling but Similarly Regulate HDAC/MEF2 Transcriptional Responses. J. Biol. Chem. 282: 35078-35087 [Abstract] [Full Text]  
  • Xu, X., Ha, C.-H., Wong, C., Wang, W., Hausser, A., Pfizenmaier, K., Olson, E. N., McKinsey, T. A., Jin, Z.-G. (2007). Angiotensin II Stimulates Protein Kinase D-Dependent Histone Deacetylase 5 Phosphorylation and Nuclear Export Leading to Vascular Smooth Muscle Cell Hypertrophy. Arterioscler. Thromb. Vasc. Bio. 27: 2355-2362 [Abstract] [Full Text]  
  • Lahm, A., Paolini, C., Pallaoro, M., Nardi, M. C., Jones, P., Neddermann, P., Sambucini, S., Bottomley, M. J., Lo Surdo, P., Carfi, A., Koch, U., De Francesco, R., Steinkuhler, C., Gallinari, P. (2007). Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases. Proc. Natl. Acad. Sci. USA 104: 17335-17340 [Abstract] [Full Text]  
  • Zimmermann, S., Kiefer, F., Prudenziati, M., Spiller, C., Hansen, J., Floss, T., Wurst, W., Minucci, S., Gottlicher, M. (2007). Reduced Body Size and Decreased Intestinal Tumor Rates in HDAC2-Mutant Mice. Cancer Res. 67: 9047-9054 [Abstract] [Full Text]  
  • Paroni, G., Fontanini, A., Cernotta, N., Foti, C., Gupta, M. P., Yang, X.-J., Fasino, D., Brancolini, C. (2007). Dephosphorylation and Caspase Processing Generate Distinct Nuclear Pools of Histone Deacetylase 4. Mol. Cell. Biol. 27: 6718-6732 [Abstract] [Full Text]  
  • Dokmanovic, M., Perez, G., Xu, W., Ngo, L., Clarke, C., Parmigiani, R. B., Marks, P. A. (2007). Histone deacetylase inhibitors selectively suppress expression of HDAC7. Molecular Cancer Therapeutics 6: 2525-2534 [Abstract] [Full Text]  
  • Kasler, H. G., Verdin, E. (2007). Histone Deacetylase 7 Functions as a Key Regulator of Genes Involved in both Positive and Negative Selection of Thymocytes. Mol. Cell. Biol. 27: 5184-5200 [Abstract] [Full Text]  
  • Pagan, J. K., Arnold, J., Hanchard, K. J., Kumar, R., Bruno, T., Jones, M. J. K., Richard, D. J., Forrest, A., Spurdle, A., Verdin, E., Crossley, M., Fanciulli, M., Chenevix-Trench, G., Young, D. B., Khanna, K. K. (2007). A Novel Corepressor, BCoR-L1, Represses Transcription through an Interaction with CtBP. J. Biol. Chem. 282: 15248-15257 [Abstract] [Full Text]  
  • Little, G. H., Bai, Y., Williams, T., Poizat, C. (2007). Nuclear Calcium/Calmodulin-dependent Protein Kinase II{delta} Preferentially Transmits Signals to Histone Deacetylase 4 in Cardiac Cells. J. Biol. Chem. 282: 7219-7231 [Abstract] [Full Text]  
  • McKinsey, T. A. (2007). Derepression of pathological cardiac genes by members of the CaM kinase superfamily. Cardiovasc Res 73: 667-677 [Abstract] [Full Text]  
  • Haberland, M., Arnold, M. A., McAnally, J., Phan, D., Kim, Y., Olson, E. N. (2007). Regulation of HDAC9 Gene Expression by MEF2 Establishes a Negative-Feedback Loop in the Transcriptional Circuitry of Muscle Differentiation. Mol. Cell. Biol. 27: 518-525 [Abstract] [Full Text]  
  • Jaehnig, E. J., Heidt, A. B., Greene, S. B., Cornelissen, I., Black, B. L. (2006). Increased Susceptibility to Isoproterenol-Induced Cardiac Hypertrophy and Impaired Weight Gain in Mice Lacking the Histidine-Rich Calcium-Binding Protein. Mol. Cell. Biol. 26: 9315-9326 [Abstract] [Full Text]  
  • Karamboulas, C., Swedani, A., Ward, C., Al-Madhoun, A. S., Wilton, S., Boisvenue, S., Ridgeway, A. G., Skerjanc, I. S. (2006). HDAC activity regulates entry of mesoderm cells into the cardiac muscle lineage. J. Cell Sci. 119: 4305-4314 [Abstract] [Full Text]  
  • Dequiedt, F., Martin, M., Von Blume, J., Vertommen, D., Lecomte, E., Mari, N., Heinen, M.-F., Bachmann, M., Twizere, J.-C., Huang, M. C., Rider, M. H., Piwnica-Worms, H., Seufferlein, T., Kettmann, R. (2006). New Role for hPar-1 Kinases EMK and C-TAK1 in Regulating Localization and Activity of Class IIa Histone Deacetylases.. Mol. Cell. Biol. 26: 7086-7102 [Abstract] [Full Text]  
  • van Oort, R. J., van Rooij, E., Bourajjaj, M., Schimmel, J., Jansen, M. A., van der Nagel, R., Doevendans, P. A., Schneider, M. D., van Echteld, C. J.A., De Windt, L. J. (2006). MEF2 Activates a Genetic Program Promoting Chamber Dilation and Contractile Dysfunction in Calcineurin-Induced Heart Failure. Circulation 114: 298-308 [Abstract] [Full Text]  
  • Iguchi, N., Tobias, J. W., Hecht, N. B. (2006). Expression profiling reveals meiotic male germ cell mRNAs that are translationally up- and down-regulated. Proc. Natl. Acad. Sci. USA 103: 7712-7717 [Abstract] [Full Text]  
  • Harrison, B. C., Kim, M.-S., van Rooij, E., Plato, C. F., Papst, P. J., Vega, R. B., McAnally, J. A., Richardson, J. A., Bassel-Duby, R., Olson, E. N., McKinsey, T. A. (2006). Regulation of Cardiac Stress Signaling by Protein Kinase D1. Mol. Cell. Biol. 26: 3875-3888 [Abstract] [Full Text]  
  • Kim, I. A., Shin, J. H., Kim, I. H., Kim, J. H., Kim, J. S., Wu, H. G., Chie, E. K., Ha, S. W., Park, C. I., Kao, G. D. (2006). Histone Deacetylase Inhibitor-Mediated Radiosensitization of Human Cancer Cells: Class Differences and the Potential Influence of p53. Clin. Cancer Res. 12: 940-949 [Abstract] [Full Text]  
  • Backs, J., Olson, E. N. (2006). Control of Cardiac Growth by Histone Acetylation/Deacetylation. Circ. Res. 98: 15-24 [Abstract] [Full Text]  
  • McKinsey, T. A., Kuwahara, K., Bezprozvannaya, S., Olson, E. N. (2006). Class II Histone Deacetylases Confer Signal Responsiveness to the Ankyrin-Repeat Proteins ANKRA2 and RFXANK. Mol. Biol. Cell 17: 438-447 [Abstract] [Full Text]  
  • Bolger, T. A., Yao, T.-P. (2005). Intracellular Trafficking of Histone Deacetylase 4 Regulates Neuronal Cell Death. J. Neurosci. 25: 9544-9553 [Abstract] [Full Text]  
  • Zhao, X., Sternsdorf, T., Bolger, T. A., Evans, R. M., Yao, T.-P. (2005). Regulation of MEF2 by Histone Deacetylase 4- and SIRT1 Deacetylase-Mediated Lysine Modifications. Mol. Cell. Biol. 25: 8456-8464 [Abstract] [Full Text]  
  • Chang, S., Bezprozvannaya, S., Li, S., Olson, E. N. (2005). An expression screen reveals modulators of class II histone deacetylase phosphorylation. Proc. Natl. Acad. Sci. USA 102: 8120-8125 [Abstract] [Full Text]  
  • Yang, X.-J., Gregoire, S. (2005). Class II Histone Deacetylases: from Sequence to Function, Regulation, and Clinical Implication. Mol. Cell. Biol. 25: 2873-2884 [Full Text]  
  • Cao, D., Wang, Z., Zhang, C.-L., Oh, J., Xing, W., Li, S., Richardson, J. A., Wang, D.-Z., Olson, E. N. (2005). Modulation of Smooth Muscle Gene Expression by Association of Histone Acetyltransferases and Deacetylases with Myocardin. Mol. Cell. Biol. 25: 364-376 [Abstract] [Full Text]  
  • Harrison, B. C., Roberts, C. R., Hood, D. B., Sweeney, M., Gould, J. M., Bush, E. W., McKinsey, T. A. (2004). The CRM1 Nuclear Export Receptor Controls Pathological Cardiac Gene Expression. Mol. Cell. Biol. 24: 10636-10649 [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»