Cdc42 is an antihypertrophic molecular switch in the mouse heart

Journal of Clinical Investigation

Volumn 119, Issue 10, 2009, Pages 3079-3088

  Maillet, Marjorie ^a   Lynch, Jeffrey M ^a   Sanna, Bastiano ^a   York, Allen J ^a   Zheng, Yi ^a   Molkentin, Jeffery D ^a,b  

^a UNIVERSITY OF CINCINNATI   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; PROTEIN CDC42; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR NFAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ECHOCARDIOGRAPHY; EXERCISE; GENE DELETION; HEART FAILURE; HEART FUNCTION; HEART MUSCLE CELL; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE OVERLOAD; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SUDDEN DEATH; TRANSGENE;

ANIMALS; CALCINEURIN; CARDIOMEGALY; CDC42 GTP-BINDING PROTEIN; ECHOCARDIOGRAPHY; ENZYME ACTIVATION; HEART; HEART FAILURE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE 7; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR ACTIVITY; MYOCARDIUM; MYOCYTES, CARDIAC; NEUROPEPTIDES; NFATC TRANSCRIPTION FACTORS; RAC GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; SURVIVAL RATE;

EID: 70349678681     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI37694     Document Type: Article

References (56)

1. Claycomb, W.C. 1983. Cardiac muscle cell proliferation and cell differentiation in vivo and in vitro. Adv. Exp. Med. Biol. 161:249-265.
2. Levy, D., Garrison, R.J., Savage, D.D., Kannel, W.B., and Castelli, W.P. 1990. Prognostic implications of echocardiographically determined left ventricular mass in the Framingham Heart Study. N. Engl. J. Med. 322:1561-1566. (Pubitemid 20176696)
3. Ho, K.K., Pinsky, J.L., Kannel, W.B., and Levy, D. 1993. The epidemiology of heart failure: the Framingham Study. J. Am. Coll. Cardiol. 22:6A-13A. (Pubitemid 23285789)
4. Molkentin, J.D., et al. 1998. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell. 93:215-228. (Pubitemid 28180855)
5. Heineke, J., and Molkentin, J.D. 2006. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat. Rev. Mol. Cell Biol. 7:589-600. (Pubitemid 44325350)
6. Liang, Q., and Molkentin, J.D. 2003. Redefining the roles of p38 and JNK signaling in cardiac hypertrophy: dichotomy between cultured myocytes and animal models. J. Mol. Cell. Cardiol. 35:1385-1394. (Pubitemid 37491181)
7. Bueno, O.F., and Molkentin, J.D. 2002. Involvement of extracellular signal-regulated kinases 1/2 in cardiac hypertrophy and cell death. Circ. Res. 91:776-781.
8. Brown, J.H., Del Re, D.P., and Sussman, M.A. 2006. The Rac and Rho hall of fame: a decade of hypertrophic signaling hits. Circ. Res. 98:730-742.
9. Lezoualc'h, F., Metrich, M., Hmitou, I., Duquesnes, N., and Morel, E. 2008. Small GTP-binding proteins and their regulators in cardiac hypertrophy. J. Mol. Cell. Cardiol. 44:623-632.
10. Adams, A.E., Johnson, D.I., Longnecker, R.M., Sloat, B.F., and Pringle, J.R. 1990. CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae. J. Cell Biol. 111:131-142. (Pubitemid 20202623)
11. Jaffe, A.B., and Hall, A. 2005. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21:247-269.
12. Olofsson, B. 1999. Rho guanine dissociation inhibitors: pivotal molecules in cellular signalling. Cell Signal. 11:545-554. (Pubitemid 29255886)
13. Schmidt, A., and Hall, A. 2002. Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev. 16:1587-1609. (Pubitemid 34743321)
14. Bernards, A. 2003. GAPs galore! A survey of putative Ras superfamily GTPase activating proteins in man and Drosophila. Biochim. Biophys. Acta. 1603:47-82.
15. Etienne-Manneville, S., and Hall, A. 2002. Rho GTPases in cell biology. Nature. 420:629-635.
16. Wu, X., et al. 2006. Cdc42 controls progenitor cell differentiation and beta-catenin turnover in skin. Genes Dev. 20:571-585. (Pubitemid 43345323)
17. Chen, L., et al. 2006. Cdc42 deficiency causes Sonic hedgehog-independent holoprosencephaly. Proc. Natl. Acad. Sci. U. S. A. 103:16520-16525. (Pubitemid 44715228)
18. Cappello, S., et al. 2006. The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat. Neurosci. 9:1099-1107. (Pubitemid 44306302)
19. Yang, L., et al. 2007. Rho GTPase Cdc42 coordinates hematopoietic stem cell quiescence and niche interaction in the bone marrow. Proc. Natl. Acad. Sci. U. S. A. 104:5091-5096. (Pubitemid 47186181)
20. Yang, L., et al. 2007. Cdc42 critically regulates the balance between myelopoiesis and erythropoiesis. Blood. 110:3853-3861. (Pubitemid 350248440)
21. Wang, L., Yang, L., Debidda, M., Witte, D., and Zheng, Y. 2007. Cdc42 GTPase-activating protein deficiency promotes genomic instability and premature aging-like phenotypes. Proc. Natl. Acad. Sci. U. S. A. 104:1248-1253. (Pubitemid 46183990)
22. Yang, L., Wang, L., and Zheng, Y. 2006. Gene targeting of Cdc42 and Cdc42GAP affirms the critical involvement of Cdc42 in filopodia induction, directed migration, and proliferation in primary mouse embryonic fibroblasts. Mol. Biol. Cell. 17:4675-4685. (Pubitemid 44665738)
23. Nagai, T., et al. 2003. Cdc42 plays a critical role in assembly of sarcomere units in series of cardiac myocytes. Biochem. Biophys. Res. Commun. 305:806-810. (Pubitemid 36597834)
24. Chen, F., et al. 2000. Cdc42 is required for PIP(2)-induced actin polymerization and early development but not for cell viability. Curr. Biol. 10:758-765. (Pubitemid 30466938)
25. Bishop, A.L., and Hall, A. 2000. Rho GTPases and their effector proteins. Biochem. J. 348:241-255. (Pubitemid 30345195)
26. Sadoshima, J., et al. 2002. The MEKK1-JNK pathway plays a protective role in pressure overload but does not mediate cardiac hypertrophy. J. Clin. Invest. 110:271-279. (Pubitemid 34787364)
27. Liang, Q., et al. 2003. c-Jun N-terminal kinases (JNK) antagonize cardiac growth through cross-talk with calcineurin-NFAT signaling. EMBO J. 22:5079-5089. (Pubitemid 37222028)
28. Kaiser, R.A., et al. 2005. Genetic inhibition or activation of JNK1/2 protects the myocardium from ischemia-reperfusion-induced cell death in vivo. J. Biol. Chem. 280:32602-32608.
29. Chow, C.W., Rincon, M., Cavanagh, J., Dickens, M., and Davis, R.J. 1997. Nuclear accumulation of NFAT4 opposed by the JNK signal transduction pathway. Science. 278:1638-1641. (Pubitemid 27516286)
30. Porter, C.M., Havens, M.A., and Clipstone, N.A. 2000. Identification of amino acid residues and protein kinases involved in the regulation of NFATc subcellular localization. J. Biol. Chem. 275:3543-3551.
31. Zheng, M., et al. 2004. Sarcoplasmic reticulum calcium defect in Ras-induced hypertrophic cardiomyopathy heart. Am. J. Physiol. Heart Circ. Physiol. 286:H424-H433. (Pubitemid 38049509)
32. Sussman, M.A., et al. 2000. Altered focal adhesion regulation correlates with cardiomyopathy in mice expressing constitutively active rac1. J. Clin. Invest. 105:875-886.
33. Satoh, M., et al. 2006. Requirement of Rac1 in the development of cardiac hypertrophy. Proc. Natl. Acad. Sci. U. S. A. 103:7432-7437. (Pubitemid 43727850)
34. Sah, V.P., et al. 1999. Cardiac-specific overexpression of RhoA results in sinus and atrioventricular nodal dysfunction and contractile failure. J. Clin. Invest. 103:1627-1634.
35. Fiedler, B., et al. 2002. Inhibition of calcineurin-NFAT hypertrophy signaling by cGMP-dependent protein kinase type I in cardiac myocytes. Proc. Natl. Acad. Sci. U. S. A. 99:11363-11368. (Pubitemid 34920931)
36. Kass, D.A., Champion, H.C., and Beavo, J.A. 2007. Phosphodiesterase type 5: expanding roles in cardiovascular regulation. Circ. Res. 101:1084-1095.
37. Braz, J.C., et al. 2003. Targeted inhibition of p38 MAPK promotes hypertrophic cardiomyopathy through upregulation of calcineurin-NFAT signaling. J. Clin. Invest. 111:1475-1486.
38. Taniike, M., et al. 2008. Apoptosis signal-regulating kinase 1/p38 signaling pathway negatively regulates physiological hypertrophy. Circulation. 117:545-552.
39. Liao, P., et al. 2001. The in vivo role of p38 MAP kinases in cardiac remodeling and restrictive cardiomyopathy. Proc. Natl. Acad. Sci. U. S. A. 98:12283-12288. (Pubitemid 32959865)
40. Petrich, B.G., et al. 2004. Targeted activation of c-Jun N-terminal kinase in vivo induces restrictive cardiomyopathy and conduction defects. J. Biol. Chem. 279:15330-15338.
41. Choukroun, G., et al. 1999. Regulation of cardiac hypertrophy in vivo by the stress-activated protein kinases/c-Jun NH(2)-terminal kinases. J. Clin. Invest. 104:391-398. (Pubitemid 29534323)
42. Minamino, T., et al. 2002. MEKK1 is essential for cardiac hypertrophy and dysfunction induced by Gq. Proc. Natl. Acad. Sci. U. S. A. 99:3866-3871. (Pubitemid 34252197)
43. Fanger, G.R., Johnson, N.L., and Johnson, G.L. 1997. MEK kinases are regulated by EGF and selectively interact with Rac/Cdc42. EMBO J. 16:4961-4972.
44. Coso, O.A., et al. 1995. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell. 81:1137-1146.
45. Minden, A., Lin, A., Claret, F.X., Abo, A., and Karin, M. 1995. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell. 81:1147-1157.
46. Yeh, Y.C., Wang, C.Z., and Tang, M.J. 2009. Discoidin domain receptor 1 activation suppresses alpha(2)beta(1) integrin-dependent cell spreading through inhibition of Cdc42 activity. J. Cell. Physiol. 218:146-156.
47. Shiojima, I., and Walsh, K. 2006. Regulation of cardiac growth and coronary angiogenesis by the Akt/PKB signaling pathway. Genes Dev. 20:3347-3365. (Pubitemid 44969154)
48. Matsui, T., et al. 2002. Phenotypic spectrum caused by transgenic overexpression of activated Akt in the heart. J. Biol. Chem. 277:22896-22901. (Pubitemid 34967272)
49. Shioi, T., et al. 2002. Akt/protein kinase B promotes organ growth in transgenic mice. Mol. Cell. Biol. 22:2799-2809. (Pubitemid 34263000)
50. Oka, T., et al. 2006. Cardiac-specific deletion of Gata4 reveals its requirement for hypertrophy, compensation, and myocyte viability. Circ. Res. 98:837-845. (Pubitemid 43755268)
51. Wilkins, B.J., et al. 2004. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ. Res. 94:110-118. (Pubitemid 38064105)
52. Wilkins, B.J., et al. 2002. Targeted disruption of NFATc3, but not NFATc4, reveals an intrinsic defect in calcineurin-mediated cardiac hypertrophic growth. Mol. Cell. Biol. 22:7603-7613.
53. Shai, S.Y., et al. 2002. Cardiac myocyte-specific excision of the beta1 integrin gene results in myocardial fibrosis and cardiac failure. Circ. Res. 90:458-464.
54. Parsons, S.A., et al. 2004. Genetic loss of calcineurin blocks mechanical overload-induced skeletal muscle fiber type switching but not hypertrophy. J. Biol. Chem. 279:26192-26200.
55. De Windt, L.J., Lim, H.W., Haq, S., Force, T., and Molkentin, J.D. 2000. Calcineurin promotes protein kinase C and c-Jun NH2-terminal kinase activation in the heart. Cross-talk between cardiac hypertrophic signaling pathways. J. Biol. Chem. 275:13571-13579. (Pubitemid 30257424)
56. Maillet, M., et al. 2003. Crosstalk between Rap1 and Rac regulates secretion of sAPPalpha. Nat. Cell Biol. 5:633-639. (Pubitemid 36818085)