Modulation of dynamin-related protein 1 (DRP1) function by increased O-linked-β-N-acetylglucosamine modification (O-GlcNAc) in cardiac myocytes

Journal of Biological Chemistry

Volumn 287, Issue 35, 2012, Pages 30024-30034

  Gawlowski, Thomas ^a   Suarez, Jorge ^a   Scott, Brian ^a   Torres Gonzalez, Moises ^a   Wang, Hong ^a   Schwappacher, Raphaela ^a   Han, Xuemei ^c   Yates III, John R ^c   Hoshijima, Masahiko ^a,b   Dillmann, Wolfgang ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CYTOLOGY; MUSCLE; PHOSPHORYLATION; PROTEINS;

CHEMICAL INHIBITION; DIABETES-RELATED COMPLICATIONS; MITOCHONDRIAL DYSFUNCTION; MITOCHONDRIAL FRAGMENTATION; MITOCHONDRIAL FUNCTION; MITOCHONDRIAL MEMBRANE POTENTIAL; N-ACETYLGLUCOSAMINE; N-ACETYLGLUCOSAMINIDASE;

MITOCHONDRIA;

ADENOVIRUS VECTOR; DYNAMIN; DYNAMIN RELATED PROTEIN 1; N ACETYL BETA GLUCOSAMINIDASE; N ACETYLGLUCOSAMINE; O LINKED BETA N ACETYLGLUCOSAMINE; SERINE; THREONINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; CYTOPLASM; ENZYME INHIBITION; GLYCOSYLATION; HEART MUSCLE CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NEWBORN; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; WESTERN BLOTTING;

EID: 84865457924     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.390682     Document Type: Article

References (47)

1. Westermann, B. (2010) Mitochondrial fusion and fission in cell life and death. Nat. Rev. Mol. Cell Biol. 11, 872-884
2. Kane, L. A., and Youle, R. J. (2010) Mitochondrial fission and fusion and their roles in the heart. J. Mol. Med. 88, 971-979
3. Chang, C. R., and Blackstone, C. (2010) Dynamic regulation of mitochondrial fission through modification of the dynamin-related protein Drp1. Ann. N.Y. Acad. Sci. 1201, 34-39
4. 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
5. Chang, C. R., and Blackstone, C. (2007) Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology. J. Biol. Chem. 282, 21583-21587
6. 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
7. Cereghetti, G. M., Stangherlin, A., Martins de Brito, O., Chang, C. R., Blackstone, C., Bernardi, P., and Scorrano, L. (2008) Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc. Natl. Acad. Sci. U.S.A. 105, 15803-15808
8. Figueroa-Romero, C., Iñiguez-Lluhi, J. A., Stadler, J., Chang, C. R., Arnoult, D., Keller, P. J., Hong, Y., Blackstone, C., and Feldman, E. L. (2009) SUMOylation of the mitochondrial fission protein Drp1 occurs at multiple nonconsensus sites within the B domain and is linked to its activity cycle. FASEB J. 23, 3917-3927
9. Nakamura, N., Kimura, Y., Tokuda, M., Honda, S., and Hirose, S. (2006) MARCH-V is a novel mitofusin 2- and Drp1-binding protein able to change mitochondrial morphology. EMBO Rep. 7, 1019-1022
10. Cho, D. H., Nakamura, T., Fang, J., Cieplak, P., Godzik, A., Gu, Z., and Lipton, S. A. (2009) S-nitrosylation of Drp1 mediates β-amyloid-related mitochondrial fission and neuronal injury. Science 324, 102-105
11. Jahani-Asl, A., and Slack, R. S. (2007) The phosphorylation state of Drp1 determines cell fate. EMBO Rep. 8, 912-913
12. 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
13. Stojanovski, D., Koutsopoulos, O. S., Okamoto, K., and Ryan, M. T. (2004) Levels of human Fis1 at the mitochondrial outer membrane regulate mitochondrial morphology. J. Cell Sci. 117, 1201-1210
14. Otera, H., Wang, C., Cleland, M. M., Setoguchi, K., Yokota, S., Youle, R. J., and Mihara, K. (2010) Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J. Cell Biol. 191, 1141-1158
15. Yu, T., Fox, R. J., Burwell, L. S., and Yoon, Y. (2005) Regulation of mitochondrial fission and apoptosis by the mitochondrial outer membrane protein hFis1. J. Cell Sci. 118, 4141-4151
16. Hart, G. W., Housley, M. P., and Slawson, C. (2007) Cycling of O-linked β-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446, 1017-1022
17. Gewinner, C., Hart, G., Zachara, N., Cole, R., Beisenherz-Huss, C., and Groner, B. (2004) The coactivator of transcription CREB-binding protein interacts preferentially with the glycosylated form of Stat5. J. Biol. Chem. 279, 3563-3572
18. Hu, Y., Suarez, J., Fricovsky, E., Wang, H., Scott, B. T., Trauger, S. A., Han, W., Hu, Y., Oyeleye, M. O., and Dillmann, W. H. (2009) Increased enzymatic O-GlcNAcylation of mitochondrial proteins impairs mitochondrial function in cardiac myocytes exposed to high glucose. J. Biol. Chem. 284, 547-555
19. Cheng, X., and Hart, G. W. (2001) Alternative O-glycosylation/O- phosphorylation of serine-16 in murine estrogen receptor beta: post-translational regulation of turnover and transactivation activity. J. Biol. Chem. 276, 10570-10575
20. Love, D. C., Kochan, J., Cathey, R. L., Shin, S. H., and Hanover, J. A. (2003) Mitochondrial and nucleocytoplasmic targeting of O-linked GlcNAc transferase. J. Cell Sci. 116, 647-654
21. Clark, R. J., McDonough, P. M., Swanson, E., Trost, S. U., Suzuki, M., Fukuda, M., and Dillmann, W. H. (2003) Diabetes and the accompanying hyperglycemia impairs cardiomyocyte calcium cycling through increased nuclear O-GlcNAcylation. J. Biol. Chem. 278, 44230-44237
22. Hu, Y., Belke, D., Suarez, J., Swanson, E., Clark, R., Hoshijima, M., and Dillmann, W. H. (2005) Adenovirus-mediated overexpression of O-GlcNAcase improves contractile function in the diabetic heart. Circ. Res. 96, 1006-1013
23. Laczy, B., Hill, B. G., Wang, K., Paterson, A. J., White, C. R., Xing, D., Chen, Y. F., Darley-Usmar, V., Oparil, S., and Chatham, J. C. (2009) Protein O-GlcNAcylation. A new signaling paradigm for the cardiovascular system. Am. J. Physiol. Heart Circ. Physiol. 296, H13-28
24. Makino, A., Suarez, J., Gawlowski, T., Han, W., Wang, H., Scott, B. T., and Dillmann, W. H. (2011) Regulation of mitochondrial morphology and function by O-GlcNAcylation in neonatal cardiac myocytes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R1296-R1302
25. Gao, Y., Wells, L., Comer, F. I., Parker, G. J., and Hart, G. W. (2001) Dynamic O-glycosylation of nuclear and cytosolic proteins: cloning and characterization of a neutral, cytosolic β-N-acetylglucosaminidase from human brain. J. Biol. Chem. 276, 9838-9845
26. Gundemir, S., and Johnson, G. V. (2009) Intracellular localization and conformational state of transglutaminase 2. Implications for cell death. PLoS ONE 4, e6123
27. Zhao, J., Liu, T., Jin, S., Wang, X., Qu, M., Uhlen, P., Tomilin, N., Shupliakov, O., Lendahl, U., and Nister, M. (2011) Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission. EMBO J. 30, 2762-2778
28. Gandy, J. C., Rountree, A. E., and Bijur, G. N. (2006) Akt1 is dynamically modified with O-GlcNAc following treatments with PUGNAc and insulin- like growth factor-1. FEBS Lett. 580, 3051-3058
29. Schroeder, M. J., Webb, D. J., Shabanowitz, J., Horwitz, A. F., and Hunt, D. F. (2005) Methods for the detection of paxillin post-translational modifications and interacting proteins by mass spectrometry. J. Proteome Res. 4, 1832-1841
30. McDonald, W. H., Tabb, D. L., Sadygov, R. G., MacCoss, M. J., Venable, J., Graumann, J., Johnson, J. R., Cociorva, D., and Yates, J. R., 3rd. (2004) MS1, MS2, and SQT-three unified, compact, and easily parsed file formats for the storage of shotgun proteomic spectra and identifications. Rapid Commun. Mass Spectrom. 18, 2162-2168
31. Xu, T., Venable, J. D., Park, S. K., Cociorva, D., Lu, B., Liao, L., Wohlschlegel, J., Hewel, J., and Yates, J. R. (2006) ProLuCID, a fast and sensitive tandem mass spectra-based protein identification program. Mol. Cell. Proteomics 5, S174
32. Peng, J., Elias, J. E., Thoreen, C. C., Licklider, L. J., and Gygi, S. P. (2003) Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis. The yeast proteome. J. Proteome Res. 2, 43-50
33. Tabb, D. L., McDonald, W. H., and Yates, J. R., 3rd. (2002) DTASelect and Contrast. Tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 1, 21-26
34. Bimboese, P., Gibson, C. J., Schmidt, S., Xiang, W., and Ehrlich, B. E. (2011) Isoform-specific regulation of the inositol 1,4,5-trisphosphate receptor by O-linked glycosylation. J. Biol. Chem. 286, 15688-15697
35. Hoppins, S., Lackner, L., and Nunnari, J. (2007) The machines that divide and fuse mitochondria. Annu. Rev. Biochem. 76, 751-780
36. Yoon, Y., Krueger, E. W., Oswald, B. J., and McNiven, M. A. (2003) The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol. Cell. Biol. 23, 5409-5420
37. Hart, G. W., Slawson, C., Ramirez-Correa, G., and Lagerlof, O. (2011) Cross-talk between O-GlcNAcylation and phosphorylation. Roles in signaling, transcription, and chronic disease. Annu. Rev. Biochem. 80, 825-858
38. Wang, Z., Gucek, M., and Hart, G. W. (2008) Cross-talk between GlcNAcylation and phosphorylation. Site-specific phosphorylation dynamics in response to globally elevated O-GlcNAc. Proc. Natl. Acad. Sci. U.S.A. 105, 13793-13798
39. Hui, L., Hong, Y., Jingjing, Z., Yuan, H., Qi, C., and Nong, Z. (2010) HGF suppresses high glucose-mediated oxidative stress in mesangial cells by activation of PKG and inhibition of PKA. Free Radic. Biol. Med. 49, 467-473
40. Singh, L. P., and Crook, E. D. (2000) Hexosamine regulation of glucose-mediated laminin synthesis in mesangial cells involves protein kinases A and C. Am. J. Physiol. Renal Physiol. 279, F646-654
41. Hatakeyama, H., Kishimoto, T., Nemoto, T., Kasai, H., and Takahashi, N. (2006) Rapid glucose sensing by protein kinase A for insulin exocytosis in mouse pancreatic islets. J. Physiol. 570, 271-282
42. Chang, C. R., Manlandro, C. M., Arnoult, D., Stadler, J., Posey, A. E., Hill, R. B., and Blackstone, C. (2010) A lethal de novo mutation in the middle domain of the dynamin-related GTPase Drp1 impairs higher order assembly and mitochondrial division. J. Biol. Chem. 285, 32494-32503
43. 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 dynaminrelated protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 1, 515-525
44. Gu, Y., Ande, S. R., and Mishra, S. (2011) Altered O-GlcNAc modification and phosphorylation of mitochondrial proteins in myoblast cells exposed to high glucose. Arch. Biochem. Biophys. 505, 98-104
45. Buse, M. G. (2006) Hexosamines, insulin resistance, and the complications of diabetes. Current status. Am. J. Physiol. Endocrinol. Metab. 290, E1-E8
46. Karunakaran, U., and Jeoung, N. H. (2010) O-GlcNAc Modification. Friend or Foe in Diabetic Cardiovascular Disease. Korean Diabetes J. 34, 211-219
47. Tanaka, Y., Konno, N., and Kako, K. J. (1992) Mitochondrial dysfunction observed in situ in cardiomyocytes of rats in experimental diabetes. Cardiovasc. Res. 26, 409-414