Quantitative phosphoproteomic study of pressure-overloaded mouse heart reveals dynamin-related protein 1 as a modulator of cardiac hypertrophy

Molecular and Cellular Proteomics

Volumn 12, Issue 11, 2013, Pages 3094-3107

  Chang, Yu Wang ^a,b   Chang, Ya Ting ^a,b   Wang, Qinchuan ^c   Lin, Jim Jung Ching ^c   Chen, Yu Ju ^d   Chen, Chien Chang ^a  

^a INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c UNIVERSITY OF IOWA   (United States)

^d INSTITUTE OF CHEMISTRY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN RELATED PROTEIN 1; MITOCHONDRIAL PROTEIN; OXYGEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HEART MUSCLE CELL; HEART MUSCLE OXYGEN CONSUMPTION; HEART STRESS; HEART VENTRICLE HYPERTROPHY; MALE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEOMICS; QUANTITATIVE ASSAY; QUANTITATIVE PHOSPHOPROTEOMICS; RAT; SENSOR;

ANIMALS; CARDIOMEGALY; CELLS, CULTURED; DYNAMINS; HYPERTROPHY, LEFT VENTRICULAR; MALE; MICE; MICE, INBRED C57BL; MYOCYTES, CARDIAC; OXYGEN CONSUMPTION; PHENYLEPHRINE; PHOSPHORYLATION; PROTEOMICS; RATS; SIGNAL TRANSDUCTION;

EID: 84887049813     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M113.027649     Document Type: Article

References (72)

1. Hill, J. A., and Olson, E. N. (2008) Cardiac plasticity. N. Engl. J. Med. 358, 1370-1380.
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. Koren, M. J., Devereux, R. B., Casale, P. N., Savage, D. D., and Laragh, J. H. (1991) Relation of left ventricular mass and geometry to morbidity and mortality in uncomplicated essential hypertension. Ann. Intern. Med. 114, 345-352.
4. Gardin, J. M., and Lauer, M. S. (2004) Left ventricular hypertrophy: The next treatable, silent killer? JAMA 292, 2396-2398. (Pubitemid 39491925)
5. Lindsey, M. L., Goshorn, D. K., Comte-Walters, S., Hendrick, J. W., Hapke, E., Zile, M. R., and Schey, K. (2006) A multidimensional proteomic approach to identify hypertrophy-associated proteins. Proteomics 6, 2225-2235.
6. Friehs, I., Cowan, D. B., Choi, Y. H., Black, K. M., Barnett, R., Bhasin, M. K., Daly, C., Dillon, S. J., Libermann, T. A., McGowan, F. X., Del Nido, P. J., Levitsky, S., and McCully, J. D. (2013) Pressure-overload hypertrophy of the developing heart reveals activation of divergent gene and protein pathways in the left and right ventricular myocardium. Am. J. Physiol. Heart Circ. Physiol. 304, H697-708.
7. Yang, K. C., Ku, Y. C., Lovett, M., and Nerbonne, J. M. (2012) Combined deep microRNA and mRNA sequencing identifies protective transcriptomal signature of enhanced PI3Kalpha signaling in cardiac hypertrophy. J. Mol. Cell. Cardiol. 53, 101-112.
8. Neely, J. R., Liebermeister, H., Battersby, E. J., and Morgan, H. E. (1967) Effect of pressure development on oxygen consumption by isolated rat heart. Am. J. Physiol. 212, 804-814.
9. Schwartz, G. G., Steinman, S., Garcia, J., Greyson, C., Massie, B., and Weiner, M. W. (1992) Energetics of acute pressure overload of the porcine right ventricle. In vivo 31P nuclear magnetic resonance. J. Clin. Invest. 89, 909-918.
10. Massie, B. M., Schwartz, G. G., Garcia, J., Wisneski, J. A., Weiner, M. W., and Owens, T. (1994) Myocardial metabolism during increased work states in the porcine left ventricle in vivo. Circ. Res. 74, 64-73.
11. Chazov, E. I., Pomoinetsky, V. D., Geling, N. G., Orlova, T. R., Nekrasova, A. A., and Smirnov, V. N. (1979) Heart adaptation to acute pressure overload: An involvement of endogenous prostaglandins. Circ. Res. 45, 205-211. (Pubitemid 9240491)
12. Dowell, R. T., Cutilletta, A. F., Rudnik, M. A., and Sodt, P. C. (1976) Heart functional responses to pressure overload in exercised and sedentary rats. Am. J. Physiol. 230, 199-204.
13. White, F. M. (2008) Quantitative phosphoproteomic analysis of signaling network dynamics. Curr. Opin. Biotechnol. 19, 404-409.
14. Van Eyk, J. E. (2011) Overview: The maturing of proteomics in cardiovascular research. Circ. Res. 108, 490-498.
15. Marx, S. O., Reiken, S., Hisamatsu, Y., Jayaraman, T., Burkhoff, D., Rosemblit, N., and Marks, A. R. (2000) PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101, 365-376.
16. Chiang, C. S., Huang, C. H., Chieng, H., Chang, Y. T., Chang, D., Chen, J. J., Chen, Y. C., Chen, Y. H., Shin, H. S., Campbell, K. P., and Chen, C. C. (2009) The Ca(v)3.2 T-type Ca(2+) channel is required for pressure overload-induced cardiac hypertrophy in mice. Circ. Res. 104, 522-530.
17. Han, C. L., Chien, C. W., Chen, W. C., Chen, Y. R., Wu, C. P., Li, H., and Chen, Y. J. (2008) A multiplexed quantitative strategy for membrane proteomics: opportunities for mining therapeutic targets for autosomal dominant polycystic kidney disease. Mol. Cell. Proteomics 7, 1983-1997.
18. Wang, Y. T., Tsai, C. F., Hong, T. C., Tsou, C. C., Lin, P. Y., Pan, S. H., Hong, T. M., Yang, P. C., Sung, T. Y., Hsu, W. L., and Chen, Y. J. (2010) An informatics-assisted label-free quantitation strategy that depicts phosphoproteomic profiles in lung cancer cell invasion. J. Proteome Res. 9, 5582-5597.
19. Ross, P. L., Huang, Y. N., Marchese, J. N., Williamson, B., Parker, K., Hattan, S., Khainovski, N., Pillai, S., Dey, S., Daniels, S., Purkayastha, S., Juhasz, P., Martin, S., Bartlet-Jones, M., He, F., Jacobson, A., and Pappin, D. J. (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell. Proteomics 3, 1154-1169.
20. Savitski, M. M., Lemeer, S., Boesche, M., Lang, M., Mathieson, T., Bantscheff, M., and Kuster, B. (2011) Confident phosphorylation site localization using the Mascot Delta Score. Mol. Cell. Proteomics 10, M110.003830.
21. Lin, W. T., Hung, W. N., Yian, Y. H., Wu, K. P., Han, C. L., Chen, Y. R., Chen, Y. J., Sung, T. Y., and Hsu, W. L. (2006) Multi-Q: A fully automated tool for multiplexed protein quantitation. J. Proteome Res. 5, 2328-2338.
22. Zeeberg, B. R., Qin, H., Narasimhan, S., Sunshine, M., Cao, H., Kane, D. W., Reimers, M., Stephens, R. M., Bryant, D., Burt, S. K., Elnekave, E., Hari, D. M., Wynn, T. A., Cunningham-Rundles, C., Stewart, D. M., Nelson, D., and Weinstein, J. N. (2005) High-Throughput GoMiner, an 'industrialstrength' integrative gene ontology tool for interpretation of multiplemicroarray experiments, with application to studies of Common Variable Immune Deficiency (CVID). BMC Bioinformatics 6, 168.
23. Villén, J., Beausoleil, S. A., Gerber, S. A., and Gygi, S. P. (2007) Large-scale phosphorylation analysis of mouse liver. Proc. Natl. Acad. Sci. U.S.A. 104, 1488-1493. (Pubitemid 46214617)
24. Gustafson-Wagner, E. A., Sinn, H. W., Chen, Y. L., Wang, D. Z., Reiter, R. S., Lin, J. L., Yang, B., Williamson, R. A., Chen, J., Lin, C. I., and Lin, J. J. (2007) Loss of mXinalpha, an intercalated disk protein, results in cardiac hypertrophy and cardiomyopathy with conduction defects. Am. J. Physiol. Heart Circ. Physiol. 293, H2680-2692. (Pubitemid 350106491)
25. Shioi, T., McMullen, J. R., Tarnavski, O., Converso, K., Sherwood, M. C., Manning, W. J., and Izumo, S. (2003) Rapamycin attenuates load-induced cardiac hypertrophy in mice. Circuelation 107, 1664-1670. (Pubitemid 36397337)
26. Purcell, N. H., Wilkins, B. J., York, A., Saba-El-Leil, M. K., Meloche, S., Robbins, J., and Molkentin, J. D. (2007) Genetic inhibition of cardiac ERK1/2 promotes stress-induced apoptosis and heart failure but has no effect on hypertrophy in vivo. Proc. Natl. Acad. Sci. U.S.A. 104, 14074-14079. (Pubitemid 350003337)
27. Trinidad, J. C., Thalhammer, A., Specht, C. G., Lynn, A. J., Baker, P. R., Schoepfer, R., and Burlingame, A. L. (2008) Quantitative analysis of synaptic phosphorylation and protein expression. Mol. Cell. Proteomics 7, 684-696. (Pubitemid 351597480)
28. Koss, K. L., and Kranias, E. G. (1996) Phospholamban: A prominent regulator of myocardial contractility. Circ. Res. 79, 1059-1063. (Pubitemid 26404138)
29. Dostanic, I., Schultz Jel, J., Lorenz, J. N., and Lingrel, J. B. (2004) The alpha 1 isoform of Na, K-ATPase regulates cardiac contractility and functionally interacts and co-localizes with the Na/Ca exchanger in heart. J. Biol. Chem. 279, 54053-54061. (Pubitemid 40053139)
30. Morrison, L. E., Hoover, H. E., Thuerauf, D. J., and Glembotski, C. C. (2003) Mimicking phosphorylation of alphaB-crystallin on serine-59 is necessary and sufficient to provide maximal protection of cardiac myocytes from apoptosis. Circ. Res. 92, 203-211. (Pubitemid 36254276)
31. Charette, S. J., Lavoie, J. N., Lambert, H., and Landry, J. (2000) Inhibition of Daxx-mediated apoptosis by heat shock protein 27. Mol. Cell. Biol. 20, 7602-7612.
32. Huang, C. H., Wang, J. S., Chiang, S. C., Wang, Y. Y., Lai, S. T., and Weng, Z. C. (2004) Brief pressure overload of the left ventricle preconditions rabbit myocardium against infarction. Ann. Thorac. Surg. 78, 628-633.
33. Walker, C. A., and Spinale, F. G. (1999) The structure and function of the cardiac myocyte: A review of fundamental concepts. J. Thorac. Cardiovasc. Surg. 118, 375-382. (Pubitemid 29360345)
34. Kranias, E. G., and Hajjar, R. J. (2012) Modulation of cardiac contractility by the phospholamban/SERCA2a regulatome. Circ. Res. 110, 1646-1660.
35. Toyofuku, T., Curotto Kurzydlowski, K., Narayanan, N., and MacLennan, D. H. (1994) Identification of Ser38 as the site in cardiac sarcoplasmic reticulum Ca(2+)-ATPase that is phosphorylated by Ca2+/calmodulindependent protein kinase. J. Biol. Chem. 269, 26492-26496.
36. Hoshijima, M. (2006) Mechanical stress-strain sensors embedded in cardiac cytoskeleton: Z disk, titin, and associated structures. Am. J. Physiol. Heart Circ. Physiol. 290, H1313-1325.
37. Wang, Q., Lin, J. L., Wu, K. H., Wang, D. Z., Reiter, R. S., Sinn, H. W., Lin, C. I., and Lin, C. J. (2012) Xin proteins and intercalated disc maturation, signaling and diseases. Front. Biosci. 17, 2566-2593.
38. Kvakan, H., Kleinewietfeld, M., Qadri, F., Park, J. K., Fischer, R., Schwarz, I., Rahn, H. P., Plehm, R., Wellner, M., Elitok, S., Gratze, P., Dechend, R., Luft, F. C., and Muller, D. N. (2009) Regulatory T cells ameliorate angiotensin II-induced cardiac damage. Circulation 119, 2904-2912.
39. Kimura, K., Ieda, M., Kanazawa, H., Yagi, T., Tsunoda, M., Ninomiya, S., Kurosawa, H., Yoshimi, K., Mochizuki, H., Yamazaki, K., Ogawa, S., and Fukuda, K. (2007) Cardiac sympathetic rejuvenation: A link between nerve function and cardiac hypertrophy. Circ. Res. 100, 1755-1764. (Pubitemid 46987868)
40. Gupta, S., Purcell, N. H., Lin, A., and Sen, S. (2002) Activation of nuclear factor-kappaB is necessary for myotrophin-induced cardiac hypertrophy. J. Cell Biol. 159, 1019-1028. (Pubitemid 36055756)
41. Chen, L., Hahn, H., Wu, G., Chen, C. H., Liron, T., Schechtman, D., Cavallaro, G., Banci, L., Guo, Y., Bolli, R., Dorn, G. W. 2nd, and Mochly-Rosen, D. (2001) Opposing cardioprotective actions and parallel hypertrophic effects of delta PKC and epsilon PKC. Proc. Natl. Acad. Sci. U.S.A. 98, 11114-11119. (Pubitemid 32928691)
42. Qi, X., Disatnik, M. H., Shen, N., Sobel, R. A., and Mochly-Rosen, D. (2011) Aberrant mitochondrial fission in neurons induced by protein kinase C{delta} under oxidative stress conditions in vivo. Mol. Biol. Cell 22, 256-265.
43. Pitts, K. R., Yoon, Y., Krueger, E. W., and McNiven, M. A. (1999) The dynamin-like protein DLP1 is essential for normal distribution and morphology of the endoplasmic reticulum and mitochondria in mammalian cells. Mol. Biol. Cell 10, 4403-4417.
44. Smirnova, E., Griparic, L., Shurland, D. L., and van der Bliek, A. M. (2001) Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12, 2245-2256. (Pubitemid 33051954)
45. Liesa, M., Palacin, M., and Zorzano, A. (2009) Mitochondrial dynamics in mammalian health and disease. Physiol. Rev. 89, 799-845.
46. Taguchi, N., Ishihara, N., Jofuku, A., Oka, T., and Mihara, K. (2007) Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J. Biol. Chem. 282, 11521-11529. (Pubitemid 47100787)
47. Cui, M., Tang, X., Christian, W. V., Yoon, Y., and Tieu, K. (2010) Perturbations in mitochondrial dynamics induced by human mutant PINK1 can be rescued by the mitochondrial division inhibitor mdivi-1. J. Biol. Chem. 285, 11740-11752.
48. Wang, X., Su, B., Lee, H. G., Li, X., Perry, G., Smith, M. A., and Zhu, X. (2009) Impaired balance of mitochondrial fission and fusion in Alzheimer's disease. J. Neurosci. 29, 9090-9103.
49. Cho, D. H., Nakamura, T., Fang, J., Cieplak, P., Godzik, A., Gu, Z., and Lipton, S. A. (2009) S-nitrosylation of Drp1 mediates beta-amyloid-related mitochondrial fission and neuronal injury. Science 324, 102-105.
50. Song, W., Chen, J., Petrilli, A., Liot, G., Klinglmayr, E., Zhou, Y., Poquiz, P., Tjong, J., Pouladi, M. A., Hayden, M. R., Masliah, E., Ellisman, M., Rouiller, I., Schwarzenbacher, R., Bossy, B., Perkins, G., and Bossy- Wetzel, E. (2011) Mutant huntingtin binds the mitochondrial fission GTPase dynamin-related protein-1 and increases its enzymatic activity. Nat. Med. 17, 377-382.
51. Ong, S. B., Subrayan, S., Lim, S. Y., Yellon, D. M., Davidson, S. M., and Hausenloy, D. J. (2010) Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion injury. Circulation 121, 2012-2022.
52. Cassidy-Stone, A., Chipuk, J. E., Ingerman, E., Song, C., Yoo, C., Kuwana, T., Kurth, M. J., Shaw, J. T., Hinshaw, J. E., Green, D. R., and Nunnari, J. (2008) Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev. Cell 14, 193-204. (Pubitemid 351189177)
53. Nakagawa, O., Ogawa, Y., Itoh, H., Suga, S., Komatsu, Y., Kishimoto, I., Nishino, K., Yoshimasa, T., and Nakao, K. (1995) Rapid transcriptional activation and early mRNA turnover of brain natriuretic peptide in cardiocyte hypertrophy. Evidence for brain natriuretic peptide as an "emergency" cardiac hormone against ventricular overload. J. Clin. Invest. 96, 1280-1287.
54. Frank, S., Gaume, B., Bergmann-Leitner, E. S., Leitner, W. W., Robert, E. G., Catez, F., Smith, C. L., and Youle, R. J. (2001) The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 1, 515-525. (Pubitemid 33586103)
55. Sansbury, B. E., Riggs, D. W., Brainard, R. E., Salabei, J. K., Jones, S. P., and Hill, B. G. (2011) Responses of hypertrophied myocytes to reactive species: implications for glycolysis and electrophile metabolism. Biochem. J. 435, 519-528.
56. Vahebi, S., Ota, A., Li, M., Warren, C. M., de Tombe, P. P., Wang, Y., and Solaro, R. J. (2007) p38-MAPK induced dephosphorylation of alphatropomyosin is associated with depression of myocardial sarcomeric tension and ATPase activity. Circ. Res. 100, 408-415.
57. Kumarapeli, A. R., Su, H., Huang, W., Tang, M., Zheng, H., Horak, K. M., Li, M., and Wang, X. (2008) Alpha B-crystallin suppresses pressure overload cardiac hypertrophy. Circ. Res. 103, 1473-1482.
58. Clerk, A., Bogoyevitch, M. A., Anderson, M. B., and Sugden, P. H. (1994) Differential activation of protein kinase C isoforms by endothelin-1 and phenylephrine and subsequent stimulation of p42 and p44 mitogenactivated protein kinases in ventricular myocytes cultured from neonatal rat hearts. J. Biol. Chem. 269, 32848-32857.
59. Li, J. M., and Brooks, G. (1999) Cell cycle regulatory molecules (cyclins, cyclin-dependent kinases and cyclin-dependent kinase inhibitors) and the cardiovascular system; potential targets for therapy? Eur. Heart J. 20, 406-420. (Pubitemid 29116537)
60. Han, X. J., Lu, Y. F., Li, S. A., Kaitsuka, T., Sato, Y., Tomizawa, K., Nairn, A. C., Takei, K., Matsui, H., and Matsushita, M. (2008) CaM kinase I alpha-induced phosphorylation of Drp1 regulates mitochondrial morphology. J. Cell Biol. 182, 573-585.
61. Wang, W., Wang, Y., Long, J., Wang, J., Haudek, S. B., Overbeek, P., Chang, B. H., Schumacker, P. T., and Danesh, F. R. (2012) Mitochondrial fission triggered by hyperglycemia is mediated by ROCK1 activation in podocytes and endothelial cells. Cell Metab. 15, 186-200.
62. Cribbs, J. T., and Strack, S. (2007) Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 8, 939-944. (Pubitemid 47500477)
63. Passier, R., Zeng, H., Frey, N., Naya, F. J., Nicol, R. L., McKinsey, T. A., Overbeek, P., Richardson, J. A., Grant, S. R., and Olson, E. N. (2000) CaM kinase signaling induces cardiac hypertrophy and activates the MEF2 transcription factor in vivo. J. Clin. Invest. 105, 1395-1406. (Pubitemid 30322405)
64. Higashi, M., Shimokawa, H., Hattori, T., Hiroki, J., Mukai, Y., Morikawa, K., Ichiki, T., Takahashi, S., and Takeshita, A. (2003) Long-term inhibition of Rho-kinase suppresses angiotensin II-induced cardiovascular hypertrophy in rats in vivo: effect on endothelial NAD(P)H oxidase system. Circ. Res. 93, 767-775. (Pubitemid 37288672)
65. Molkentin, J. D., Lu, J. R., Antos, C. L., Markham, B., Richardson, J., Robbins, J., Grant, S. R., and Olson, E. N. (1998) A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93, 215-228. (Pubitemid 28180855)
66. Hong, Z., Kutty, S., Toth, P. T., Marsboom, G., Hammel, J. M., Chamberlain, C., Ryan, J. J., Zhang, H. J., Sharp, W. W., Morrow, E., Trivedi, K., Weir, E. K., and Archer, S. L. (2013) Role of dynamin-related protein 1 (drp1)-mediated mitochondrial fission in oxygen sensing and constriction of the ductus arteriosus. Circ. Res. 112, 802-815.
67. Tsujimoto, I., Hikoso, S., Yamaguchi, O., Kashiwase, K., Nakai, A., Takeda, T., Watanabe, T., Taniike, M., Matsumura, Y., Nishida, K., Hori, M., Kogo, M., and Otsu, K. (2005) The antioxidant edaravone attenuates pressure overload-induced left ventricular hypertrophy. Hypertension 45, 921-926. (Pubitemid 40628938)
68. Tanaka, K., Honda, M., and Takabatake, T. (2001) Redox regulation of MAPK pathways and cardiac hypertrophy in adult rat cardiac myocyte. J. Am. Coll. Cardiol. 37, 676-685.
69. Berridge, M. J. (2006) Remodelling Ca2+ signalling systems and cardiac hypertrophy. Biochem. Soc. Trans. 34, 228-231.
70. Piquereau, J., Caffin, F., Novotova, M., Prola, A., Garnier, A., Mateo, P., Fortin, D., Huynh le, H., Nicolas, V., Alavi, M. V., Brenner, C., Ventura- Clapier, R., Veksler, V., and Joubert, F. (2012) Down-regulation of OPA1 alters mouse mitochondrial morphology, PTP function, and cardiac adaptation to pressure overload. Cardiovasc. Res. 94, 408-417.
71. Ashrafian, H., Docherty, L., Leo, V., Towlson, C., Neilan, M., Steeples, V., Lygate, C. A., Hough, T., Townsend, S., Williams, D., Wells, S., Norris, D., Glyn-Jones, S., Land, J., Barbaric, I., Lalanne, Z., Denny, P., Szumska, D., Bhattacharya, S., Griffin, J. L., Hargreaves, I., Fernandez-Fuentes, N., Cheeseman, M., Watkins, H., and Dear, T. N. (2010) A mutation in the mitochondrial fission gene Dnm1l leads to cardiomyopathy. PLoS Genet. 6, e1001000.
72. McKinsey, T. A., and Kass, D. A. (2007) Small-molecule therapies for cardiac hypertrophy: moving beneath the cell surface. Nat. Rev. Drug Discov. 6, 617-635. (Pubitemid 47207749)