SUMOylation of the mitochondrial fission protein Drpl occurs at multiple nonconsensus sites within the B domain and is linked to its activity cycle
dc.contributor.author | Figueroa-Romero, Claudia | |
dc.contributor.author | Iñiguez-Lluhí, Jorge A. | |
dc.contributor.author | Stadler, Julia | |
dc.contributor.author | Chang, Chuang-Rung | |
dc.contributor.author | Arnoult, Damien | |
dc.contributor.author | Keller, Peter J. | |
dc.contributor.author | Hong, Yu | |
dc.contributor.author | Blackstone, Craig | |
dc.contributor.author | Feldman, Eva L. | |
dc.date.accessioned | 2020-03-17T18:27:34Z | |
dc.date.available | 2020-03-17T18:27:34Z | |
dc.date.issued | 2009-11 | |
dc.identifier.citation | Figueroa-Romero, Claudia; Iñiguez-Lluhí, Jorge A. ; Stadler, Julia; Chang, Chuang-Rung; Arnoult, Damien; Keller, Peter J.; Hong, Yu; Blackstone, Craig; Feldman, Eva L. (2009). "SUMOylation of the mitochondrial fission protein Drpl occurs at multiple nonconsensus sites within the B domain and is linked to its activity cycle." The FASEB Journal 23(11): 3917-3927. | |
dc.identifier.issn | 0892-6638 | |
dc.identifier.issn | 1530-6860 | |
dc.identifier.uri | https://hdl.handle.net/2027.42/154272 | |
dc.description.abstract | Dynamin‐related protein (Drp) 1 is a key regulator of mitochondrial fission and is composed of GTP‐binding, Middle, insert B, and C‐terminal GTPase effector (GED) domains. Drpl associates with mitochondrial fission sites and promotes membrane constriction through its intrinsic GTPase activity. The mechanisms that regulate Drpl activity remain poorly understood but are likely to involve reversible post‐translational modifications, such as conjugation of small ubiquitin‐like modifier (SUMO) proteins. Through a detailed analysis, we find that Drpl interacts with the SUMO‐conjugating enzyme Ubc9 via multiple regions and demonstrate that Drpl is a direct target of SUMO modification by all three SUMO isoforms. While Drpl does not harbor consensus SUMOylation sequences, our analysis identified2 clusters of lysine residues within the B domain that serve as noncanonical conjugation sites. Although initial analysis indicates that mitochondrial recruitment of ectopically expressed Drpl in response to staurosporine is unaffected by loss of SUMOylation, we find that Drpl SUMOylation is enhanced in the context of the K38A mutation. This dominant‐negative mutant, which is deficient in GTP binding and hydrolysis, does not associate with mitochondria and prevents normal mitochondrial fission. This finding suggests that SUMOylation of Drpl is linked to its activity cycle and is influenced by Drpl localization.—Figueroa‐Romero, C., Iniguez‐Lluhi, J. A., Stadler, J., Chang, C.‐R., Arnoult, D., Keller, P. J., Hong, Y., Blackstone, C., Feldman, E. L. SUMOylation of the mitochondrial fission protein Drpl occurs at multiple nonconsensus sites within the B domain and is linked to its activity cycle. FASEB J. 23, 3917–3927 (2009). www.fasebj.org | |
dc.publisher | Wiley Periodicals, Inc. | |
dc.subject.other | small ubiquitin-like modifier | |
dc.subject.other | Ubc9 | |
dc.subject.other | post-translational modification | |
dc.title | SUMOylation of the mitochondrial fission protein Drpl occurs at multiple nonconsensus sites within the B domain and is linked to its activity cycle | |
dc.type | Article | |
dc.rights.robots | IndexNoFollow | |
dc.subject.hlbsecondlevel | Biology | |
dc.subject.hlbtoplevel | Science | |
dc.description.peerreviewed | Peer Reviewed | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/154272/1/fsb2fj09136630.pdf | |
dc.identifier.doi | 10.1096/fj.09-136630 | |
dc.identifier.source | The FASEB Journal | |
dc.identifier.citedreference | Tatham, M. H., Jaffray, E., Vaughan, O. A., Desterro, J. M., Botting, C. H., Naismith, J. H., and Hay, R. T. 2001 Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J. Biol. Chem. 276, 35368 – 35374 | |
dc.identifier.citedreference | Li, M., Guo, D., Isales, C. M., Eizirik, D. L., Atkinson, M., She, J. X., and Wang, C. Y. 2005 SUMO wrestling with type 1 diabetes. J. Mol. Med. 83, 504 – 513 | |
dc.identifier.citedreference | Dorval, V., and Fraser, P. E. 2007 SUMO on the road to neurodegeneration. Biochim. Biophys. Acta 1773, 694 – 706 | |
dc.identifier.citedreference | Matic, I., van Hagen, M., Schimmel, J., Macek, B., Ogg, S. C., Tatham, M. H., Hay, R. T., Lamond, A. I., Mann, M., and Vertegaal, A. C. 2008 In vivo identification of human small ubiquitin-like modifier polymerization sites by high accuracy mass spectrometry and an in vitro to in vivo strategy. Mol. Cell. Proteomics 7, 132 – 144 | |
dc.identifier.citedreference | Zhang, F. P., Mikkonen, L., Toppari, J., Palvimo, J. J., Thesleff, I., and Janne, O. A. 2008 Sumo-1 function is dispensable in normal mouse development. Mol. Cell. Biol. 28, 5381 – 5390 | |
dc.identifier.citedreference | Ulrich, H. D. 2008 The fast-growing business of SUMO chains. Mol. Cell. 32, 301 – 305 | |
dc.identifier.citedreference | Lin, D. Y., Huang, Y. S., Jeng, J. C., Kuo, H. Y., Chang, C. C., Chao, T. T., Ho, C. C., Chen, Y. C., Lin, T. P., Fang, H. I., Hung, C. C., Suen, C. S., Hwang, M. J., Chang, K. S., Maul, G. G., and Shih, H. M. 2006 Role of SUMO-interacting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors. Mol. Cell. 24, 341 – 354 | |
dc.identifier.citedreference | Ivanov, A. V., Peng, H., Yurchenko, V., Yap, K. L., Negorev, D. G., Schultz, D. C., Psulkowski, E., Fredericks, W. J., White, D. E., Maul, G. G., Sadofsky, M. J., Zhou, M. M., and Rauscher, F. J., 3rd 2007 PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol. Cell. 28, 823 – 837 | |
dc.identifier.citedreference | Zunino, R., Braschi, E., Xu, L., and McBride, H. M. 2009 Translocation of SenP5 from the nucleoli to the mitochondria modulates DRP1-dependent fission during mitosis. J. Biol. Chem. 284, 17783 – 17795 | |
dc.identifier.citedreference | Braschi, E., Zunino, R., and McBride, H. M. 2009 MAPL is a new mitochondrial SUMO E3 ligase that regulates mitochondrial fission. EMBO Rep. 10, 748 – 754 | |
dc.identifier.citedreference | van der Bliek, A. M., Redelmeier, T. E., Damke, H., Tisdale, E. J., Meyerowitz, E. M., and Schmid, S. L. 1993 Mutations in human dynamin block an intermediate stage in coated vesicle formation. J. Cell Biol. 122, 553 – 563 | |
dc.identifier.citedreference | Vater, C. A., Raymond, C. K., Ekena, K., Howald-Stevenson, I., and Stevens, T. H. 1992 The VPS1 protein, a homolog of dynamin required for vacuolar protein sorting in Saccharomyces cerevisiae, is a GTPase with two functionally separable domains. J. Cell Biol. 119, 773 – 786 | |
dc.identifier.citedreference | Damke, H., Baba, T., Warnock, D. E., and Schmid, S. L. 1994 Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915 – 934 | |
dc.identifier.citedreference | Bleazard, W., McCaffery, J. M., King, E. J., Bale, S., Mozdy, A., Tieu, Q., Nunnari, J., and Shaw, J. M. 1999 The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat. Cell Biol. 1, 298 – 304 | |
dc.identifier.citedreference | Labrousse, A. M., Zappaterra, M. D., Rube, D. A., and van der Bliek, A. M. 1999 C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol. Cell. 4, 815 – 826 | |
dc.identifier.citedreference | 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 | |
dc.identifier.citedreference | Yoon, Y., Pitts, K. R., and McNiven, M. A. 2001 Mammalian dynamin-like protein DLP1 tubulates membranes. Mol. Biol. Cell. 12, 2894 – 2905 | |
dc.identifier.citedreference | Yu, T., Sheu, S. S., Robotham, J. L., and Yoon, Y. 2008 Mitochondrial fission mediates high glucose-induced cell death through elevated production of reactive oxygen species. Cardiovasc. Res. 79, 341 – 351 | |
dc.identifier.citedreference | Johnson, E. S., and Blobel, G. 1999 Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins. J. Cell Biol. 147, 981 – 994 | |
dc.identifier.citedreference | Pountney, D. L., Raftery, M. J., Chegini, F., Blumbergs, P. C., and Gai, W. P. 2008 NSF, Unc-18-1, dynamin-1 and HSP90 are inclusion body components in neuronal intranuclear inclusion disease identified by anti-SUMO-1-immunocapture. Acta Neuropathol. 116, 603 – 614 | |
dc.identifier.citedreference | Mishra, R. K., Jatiani, S. S., Kumar, A., Simhadri, V. R., Hosur, R. V., and Mittal, R. 2004 Dynamin interacts with members of the sumoylation machinery. J. Biol. Chem. 279, 31445 – 31454 | |
dc.identifier.citedreference | Leinninger, G. M., Backus, C., Sastry, A. M., Yi, Y. B., Wang, C. W., and Feldman, E. L. 2006 Mitochondria in DRG neurons undergo hyperglycemic mediated injury through Bim, Bax and the fission protein Drp1. Neurobiol. Dis. 23, 11 – 22 | |
dc.identifier.citedreference | Wang, X., Su, B., Fujioka, H., and Zhu, X. 2008 Dynamin-like protein 1 reduction underlies mitochondrial morphology and distribution abnormalities in fibroblasts from sporadic Alzheimer’s disease patients. Am. J. Pathol. 173, 470 – 482 | |
dc.identifier.citedreference | Yang, Y., Ouyang, Y., Yang, L., Beal, M. F., McQuibban, A., Vogel, H., and Lu, B. 2008 Pink1 regulates mitochondrial dynamics through interaction with the fission/fusion machinery. Proc. Natl. Acad. Sci. U. S. A. 105, 7070 – 7075 | |
dc.identifier.citedreference | Men, X., Wang, H., Li, M., Cai, H., Xu, S., Zhang, W., Xu, Y., Ye, L., Yang, W., Wollheim, C. B., and Lou, J. 2009 Dynamin-related protein 1 mediates high glucose induced pancreatic beta cell apoptosis. Int. J. Biochem. Cell Biol. 41, 879 – 890 | |
dc.identifier.citedreference | Mukherjee, S., Thomas, M., Dadgar, N., Lieberman, A. P., and Iniguez-Lluhl, J. A. 2009 SUMO modification of the androgen receptor attenuates polyglutamine-mediated aggregation. J. Biol. Chem., M109.011494 | |
dc.identifier.citedreference | Subramaniam, S., Sixt, K. M., Barrow, R., and Snyder, S. H. 2009 Rhes, a striatal specific protein, mediates mutant-huntingtin cytotoxicity. Science 324, 1327 – 1330 | |
dc.identifier.citedreference | Cerveny, K. L., Tamura, Y., Zhang, Z., Jensen, R. E., and Sesaki, H. 2007 Regulation of mitochondrial fusion and division. Trends Cell Biol. 17, 563 – 569 | |
dc.identifier.citedreference | Griparic, L., van der Wel, N. N., Orozco, I. J., Peters, P. J., and van der Bliek, A. M. 2004 Loss of the intermembrane space protein Mgm1/OPA1 induces swelling and localized constrictions along the lengths of mitochondria. J. Biol. Chem. 279, 18792 – 18798 | |
dc.identifier.citedreference | Santel, A., Frank, S., Gaume, B., Herrler, M., Youle, R. J., and Fuller, M. T. 2003 Mitofusin-1 protein is a generally expressed mediator of mitochondrial fusion in mammalian cells. J. CellSci. 116, 2763 – 2774 | |
dc.identifier.citedreference | Wells, R. C., Picton, L. K., Williams, S. C., Tan, F. J., and Hill, R. B. 2007 Direct binding of the dynamin-like GTPase, Dnm1, to mitochondrial dynamics protein Fis1 is negatively regulated by the Fis1 N-terminal arm. J. Biol. Chem. 282, 33769 – 33775 | |
dc.identifier.citedreference | 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 | |
dc.identifier.citedreference | Mozdy, A. D., McCaffery, J. M., and Shaw, J. M. 2000 Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p. J. Cell Biol. 151, 367 – 380 | |
dc.identifier.citedreference | Chen, H., and Chan, D. C. 2006 Critical dependence of neurons on mitochondrial dynamics. Curr. Opin. Cell Biol. 18, 453 – 459 | |
dc.identifier.citedreference | Baloh, R. H. 2008 Mitochondrial dynamics and peripheral neuropathy. Neuroscientist 14, 12 – 18 | |
dc.identifier.citedreference | Chan, D. C. 2007 Mitochondrial dynamics in disease. N. Engl. J. Med. 356, 1707 – 1709 | |
dc.identifier.citedreference | Ghafourifar, P., Mousavizadeh, K., Parihar, M. S., Nazarewicz, R. R., Parihar, A., and Zenebe, W. J. 2008 Mitochondria in multiple sclerosis. Front. Biosci. 13, 3116 – 3126 | |
dc.identifier.citedreference | Zeviani, M., and Carelli, V. 2007 Mitochondrial disorders. Curr. Opin. Neurol. 20, 564 – 571 | |
dc.identifier.citedreference | Alexander, C., Votruba, M., Pesch, U. E., Thiselton, D. L., Mayer, S., Moore, A., Rodriguez, M., Kellner, U., Leo-Kottler, B., Auburger, G., Bhattacharya, S. S., and Wissinger, B. 2000 OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat. Genet. 26, 211 – 215 | |
dc.identifier.citedreference | Delettre, C., Lenaers, G., Griffoin, J. M., Gigarel, N., Lorenzo, C., Belenguer, P., Pelloquin, L., Grosgeorge, J., Turc-Carel, C., Perret, E., Astarie-Dequeker, C., Lasquellec, L., Arnaud, B., Ducommun, B., Kaplan, J., and Hamel, C. P. 2000 Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat. Genet. 26, 207 – 210 | |
dc.identifier.citedreference | Sampson, D. A., Wang, M., and Matunis, M. J. 2001 The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification. J. Biol. Chem. 276, 21664 – 21669 | |
dc.identifier.citedreference | Zuchner, S., Mersiyanova, I. V., Muglia, M., Bissar-Tadmouri, N., Rochelle, J., Dadali, E. L., Zappia, M., Nelis, E., Patitucci, A., Senderek, J., Parman, Y., Evgrafov, O., Jonghe, P. D., Takahashi, Y., Tsuji, S., Pericak-Vance, M. A., Quattrone, A., Battaloglu, E., Polyakov, A. V., Timmerman, V., Schroder, J. M., and Vance, J. M. 2004 Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat. Genet. 36, 449 – 451 | |
dc.identifier.citedreference | Waterham, H. R., Koster, J., van Roermund, C. W., Mooyer, P. A., Wanders, R. J., and Leonard, J. V. 2007 A lethal defect of mitochondrial and peroxisomal fission. N. Engl. J. Med. 356, 1736 – 1741 | |
dc.identifier.citedreference | Zhu, P. P., Patterson, A., Stadler, J., Seeburg, D. P., Sheng, M., and Blackstone, C. 2004 Intra- and intermolecular domain interactions of the C-terminal GTPase effector domain of the multimeric dynamin-like GTPase Drp1. J. Biol. Chem. 279, 35967 – 35974 | |
dc.identifier.citedreference | Ingerman, E., Perkins, E. M., Marino, M., Mears, J. A., McCaffery, J. M., Hinshaw, J. E., and Nunnari, J. 2005 Dnm1 forms spirals that are structurally tailored to fit mitochondria. J. Cell Biol. 170, 1021 – 1027 | |
dc.identifier.citedreference | 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 | |
dc.identifier.citedreference | Smirnova, E., Shurland, D. L., Ryazantsev, S. N., and van der Bliek, A. M. 1998 A human dynamin-related protein controls the distribution of mitochondria. J. Cell Biol. 143, 351 – 358 | |
dc.identifier.citedreference | 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 | |
dc.identifier.citedreference | Etxebarria, A., Terrones, O., Yamaguchi, H., Landajuela, A., Landeta, O., Antonsson, B., Wang, H. G., and Basanez, G. 2009 Endophilin B1/Bif-1 stimulates BAX activation independently from its capacity to produce large-scale membrane morphological rearrangements. J. Biol. Chem. 284, 4200 – 4212 | |
dc.identifier.citedreference | 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 | |
dc.identifier.citedreference | 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 | |
dc.identifier.citedreference | 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 | |
dc.identifier.citedreference | 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 | |
dc.identifier.citedreference | 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 | |
dc.identifier.citedreference | 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 | |
dc.identifier.citedreference | Harder, Z., Zunino, R., and McBride, H. 2004 Sumo1 conjugates mitochondrial substrates and participates in mitochondrial fission. Curr. Biol. 14, 340 – 345 | |
dc.identifier.citedreference | 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 | |
dc.identifier.citedreference | 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 | |
dc.identifier.citedreference | Wasiak, S., Zunino, R., and McBride, H. M. 2007 Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J. Cell Biol. 177, 439 – 450 | |
dc.identifier.citedreference | Zunino, R., Schauss, A., Rippstein, P., Andrade-Navarro, M., and McBride, H. M. 2007 The SUMO protease SENP5 is required to maintain mitochondrial morphology and function. J. Cell Sci. 120, 1178 – 1188 | |
dc.identifier.citedreference | Ulrich, H. D. 2005 Mutual interactions between the SUMO and ubiquitin systems: a plea of no contest. Trends Cell Biol. 15, 525 – 532 | |
dc.identifier.citedreference | Saitoh, H., and Hinchey, J. 2000 Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 275, 6252 – 6258 | |
dc.identifier.citedreference | Su, H. L., and Li, S. S. 2002 Molecular features of human ubiquitin-like SUMO genes and their encoded proteins. Gene 296, 65 – 73 | |
dc.identifier.citedreference | Bohren, K. M., Nadkarni, V., Song, J. H., Gabbay, K. H., and Owerbach, D. 2004 A M55V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus. J. Biol. Chem. 279, 27233 – 27238 | |
dc.identifier.citedreference | Owerbach, D., McKay, E. M., Yeh, E. T., Gabbay, K. H., and Bohren, K. M. 2005 A proline-90 residue unique to SUMO-4 prevents maturation and sumoylation. Biochem. Biophys. Res. Commun. 337, 517 – 520 | |
dc.identifier.citedreference | Chun, T. H., Itoh, H., Subramanian, L., Iniguez-Lluhi, J. A., and Nakao, K. 2003 Modification of GATA-2 transcriptional activity in endothelial cells by the SUMO E3 ligase PIASy. Circ. Res. 92, 1201 – 1208 | |
dc.identifier.citedreference | Pichler, A., Gast, A., Seeler, J. S., Dejean, A., and Melchior, F. 2002 The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108, 109 – 120 | |
dc.identifier.citedreference | Sachdev, S., Bruhn, L., Sieber, H., Pichler, A., Melchior, F., and Grosschedl, R. 2001 PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev. 15, 3088 – 3103 | |
dc.identifier.citedreference | Yeh, E. T., Gong, L., and Kamitani, T. 2000 Ubiquitin-like proteins: new wines in new bottles. Gene 248, 1 – 14 | |
dc.identifier.citedreference | Chupreta, S., Holmstrom, S., Subramanian, L., and Iniguez-Lluhi, J. A. 2005 A small conserved surface in SUMO is the critical structural determinant of its transcriptional inhibitory properties. Mol. Cell. Biol. 25, 4272 – 4282 | |
dc.identifier.citedreference | Song, J., Durrin, L. K., Wilkinson, T. A., Krontiris, T. G., and Chen, Y. 2004 Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc. Natl. Acad. Sci. U. S. A. 101, 14373 – 14378 | |
dc.identifier.citedreference | Benson, M. D., Li, Q. J., Kieckhafer, K., Dudek, D., Whorton, M. R., Sunahara, R. K., Iniguez-Lluhi, J. A., and Martens, J. R. 2007 SUMO modification regulates inactivation of the voltage-gated potassium channel Kv1.5. Proc. Natl. Acad. Sci. U. S. A. 104, 1805 – 1810 | |
dc.identifier.citedreference | Vojtek, A. B., Hollenberg, S. M., and Cooper, J. A. 1993 Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 74, 205 – 214 | |
dc.identifier.citedreference | Arnoult, D., Grodet, A., Lee, Y. J., Estaquier, J., and Blackstone, C. 2005 Release of OPA1 during apoptosis participates in the rapid and complete release of cytochrome c and subsequent mitochondrial fragmentation. J. Biol. Chem. 280, 35742 – 35750 | |
dc.identifier.citedreference | Arnoult, D., Rismanchi, N., Grodet, A., Roberts, R. G., Seeburg, D. P., Estaquier, J., Sheng, M., and Blackstone, C. 2005 Bax/Bak-dependent release of DDP/TIMM8a promotes Drp1-mediated mitochondrial fission and mitoptosis during programmed cell death. Curr. Biol. 15, 2112 – 2118 | |
dc.identifier.citedreference | Santel, A., and Frank, S. 2008 Shaping mitochondria: The complex posttranslational regulation of the mitochondrial fission protein DRP1. IUBMB Life 60, 448 – 455 | |
dc.identifier.citedreference | Bernier-Villamor, V., Sampson, D. A., Matunis, M. J., and Lima, C. D. 2002 Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108, 345 – 356 | |
dc.identifier.citedreference | Rodriguez, M. S., Dargemont, C., and Hay, R. T. 2001 SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276, 12654 – 12659 | |
dc.identifier.citedreference | Kamimoto, T., Nagai, Y., Onogi, H., Muro, Y., Wakabayashi, T., and Hagiwara, M. 1998 Dymple, a novel dynamin-like high molecular weight GTPase lacking a proline-rich carboxylterminal domain in mammalian cells. J. Biol. Chem. 273, 1044 – 1051 | |
dc.identifier.citedreference | Niemann, H. H., Knetsch, M. L., Scherer, A., Manstein, D. J., and Kull, F. J. 2001 Crystal structure of a dynamin GTPase domain in both nucleotide-free and GDP-bound forms. EMBO J. 20, 5813 – 5821 | |
dc.identifier.citedreference | Germain, M., Mathai, J. P., McBride, H. M., and Shore, G. C. 2005 Endoplasmic reticulum BIK initiates DRP1-regulated remodelling of mitochondrial cristae during apoptosis. EMBO J. 24, 1546 – 1556 | |
dc.identifier.citedreference | Schrader, M. 2006 Shared components of mitochondrial and peroxisomal division. Biochim. Biophys. Acta 1763, 531 – 541 | |
dc.identifier.citedreference | Shin, H. W., Shinotsuka, C., Torii, S., Murakami, K., and Nakayama, K. 1997 Identification and subcellular localization of a novel mammalian dynamin-related protein homologous to yeast Vps1p and Dnm1p. J. Biochem. 122, 525 – 530 | |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
Files in this item
Remediation of Harmful Language
The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.
Accessibility
If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.