A novel motif in the yeast mitochondrial dynamin Dnm1 is essential for adaptor binding and membrane recruitment

Journal of Cell Biology

Volumn 199, Issue 4, 2012, Pages 613-622

  Bui, Huyen T ^a   Karren, Mary A ^a   Bhar, Debjani ^a   Shaw, Janet M ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN I; GUANOSINE TRIPHOSPHATASE; MDV1 PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; FLUORESCENCE MICROSCOPY; GENE MUTATION; IN VIVO STUDY; MITOCHONDRION; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN MOTIF; YEAST;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; GTP PHOSPHOHYDROLASES; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT;

EID: 84872012439     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201207079     Document Type: Article

References (43)

1. Arimura, S., M. Fujimoto, Y. Doniwa, N. Kadoya, M. Nakazono, W. Sakamoto, and N. Tsutsumi. 2008. Arabidopsis ELONGATED MITOCHONDRIA1 is required for localization of DYNAMIN-RELATED PROTEIN3A to mitochondrial fission sites. Plant Cell. 20:1555-1566. http://dx.doi.org/10.1105/tpc.108.058578
2. Bhar, D., M.A. Karren, M. Babst, and J.M. Shaw. 2006. Dimeric Dnm1-G385D interacts with Mdv1 on mitochondria and can be stimulated to assemble into fission complexes containing Mdv1 and Fis1. J. Biol. Chem. 281:17312-17320. http://dx.doi.org/10.1074/jbc.M513530200
3. Bleazard, W., J.M. McCaffery, E.J. King, S. Bale, A. Mozdy, Q. Tieu, J. Nunnari, and J.M. Shaw. 1999. The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat. Cell Biol. 1:298-304. http://dx.doi.org/10.1038/13014
4. Cerveny, K.L., and R.E. Jensen. 2003. The WD-repeats of Net2p interact with Dnm1p and Fis1p to regulate division of mitochondria. Mol. Biol. Cell. 14:4126-4139. http://dx.doi.org/10.1091/mbc.E03-02-0092
5. Cerveny, K.L., J.M. McCaffery, and R.E. Jensen. 2001. Division of mitochondria requires a novel DMN1-interacting protein, Net2p. Mol. Biol. Cell. 12:309-321.
6. Chen, H., S.A. Detmer, A.J. Ewald, E.E. Griffin, S.E. Fraser, and D.C. Chan. 2003. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160:189-200. http://dx.doi.org/10.1083/jcb.200211046
7. Eura, Y., N. Ishihara, S. Yokota, and K. Mihara. 2003. Two mitofusin proteins, mammalian homologues of FZO, with distinct functions are both required for mitochondrial fusion. J. Biochem. 134:333-344. http://dx.doi.org/10.1093/jb/mvg150
8. Faelber, K., Y. Posor, S. Gao, M. Held, Y. Roske, D. Schulze, V. Haucke, F. Noé, and O. Daumke. 2011. Crystal structure of nucleotide-free dynamin. Nature. 477:556-560. http://dx.doi.org/10.1038/nature10369 Ford, M.G., S. Jenni, and J. Nunnari. 2011. The crystal structure of dynamin. Nature. 477:561-566. http://dx.doi.org/10.1038/nature10441
9. Ford, M.G., S. Jenni, and J. Nunnari. 2011. The crystal structure of dynamin. Nature. 477:561-566. http://dx.doi.org/10.1038/nature10441
10. Gandre-Babbe, S., and A.M. van der Bliek. 2008. The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells. Mol. Biol. Cell. 19:2402-2412. http://dx.doi.org/10.1091/mbc.E07-12-1287
11. Gao, H., D. Kadirjan-Kalbach, J.E. Froehlich, and K.W. Osteryoung. 2003. ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc. Natl. Acad. Sci. USA. 100:4328-4333. http://dx.doi.org/10.1073/pnas.0530206100
12. Griffin, E.E., J. Graumann, and D.C. Chan. 2005. The WD40 protein Caf4p is a component of the mitochondrial fission machinery and recruits Dnm1p to mitochondria. J. Cell Biol. 170:237-248. http://dx.doi.org/10.1083/jcb.200503148
13. Guthrie, C., and G. Fink. 2002. Guide to yeast genetics and molecular biology. Methods in enzymology series. Vol. 350. San Diego: Academic Press, Inc.
14. Hales, K.G., and M.T. Fuller. 1997. Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell. 90:121-129. http://dx.doi.org/10.1016/S0092-8674(00)80319-0
15. Hermann, G.J., J.W. Thatcher, J.P. Mills, K.G. Hales, M.T. Fuller, J. Nunnari, and J.M. Shaw. 1998. Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J. Cell Biol. 143:359-373. http://dx.doi.org/10.1083/jcb.143.2.359
16. Hu, J., Y. Shibata, P.P. Zhu, C. Voss, N. Rismanchi, W.A. Prinz, T.A. Rapoport, and C. Blackstone. 2009. A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell. 138:549-561. http://dx.doi.org/10.1016/j.cell.2009.05.025
17. Karren, M.A., E.M. Coonrod, T.K. Anderson, and J.M. Shaw. 2005. The role of Fis1p-Mdv1p interactions in mitochondrial fission complex assembly. J. Cell Biol. 171:291-301. http://dx.doi.org/10.1083/jcb.200506158
18. Kelley, L.A., and M.J. Sternberg. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4:363-371. http://dx.doi.org/10.1038/nprot.2009.2
19. Koch, A., M. Thiemann, M. Grabenbauer, Y. Yoon, M.A. McNiven, and M. Schrader. 2003. Dynamin-like protein 1 is involved in peroxisomal fission. J. Biol. Chem. 278:8597-8605. http://dx.doi.org/10.1074/jbc.M211761200
20. Koirala, S., H.T. Bui, H.L. Schubert, D.M. Eckert, C.P. Hill, M.S. Kay, and J.M. Shaw. 2010. Molecular architecture of a dynamin adaptor: implications for assembly of mitochondrial fission complexes. J. Cell Biol. 191:1127-1139. http://dx.doi.org/10.1083/jcb.201005046
21. Kuravi, K., S. Nagotu, A.M. Krikken, K. Sjollema, M. Deckers, R. Erdmann, M. Veenhuis, and I.J. van der Klei. 2006. Dynamin-related proteins Vps1p and Dnm1p control peroxisome abundance in Saccharomyces cerevisiae. J. Cell Sci. 119:3994-4001. http://dx.doi.org/10.1242/jcs.03166
22. Labrousse, A.M., M.D. Zappaterra, D.A. Rube, and A.M. van der Bliek. 1999. C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol. Cell. 4:815-826. http://dx.doi.org/10.1016/S1097-2765(00)80391-3
23. Lackner, L.L., J.S. Horner, and J. Nunnari. 2009. Mechanistic analysis of a dynamin effector. Science. 325:874-877. http://dx.doi.org/10.1126/science.1176921
24. Li, X., and S.J. Gould. 2003. The dynamin-like GTPase DLP1 is essential for peroxisome division and is recruited to peroxisomes in part by PEX11. J. Biol. Chem. 278:17012-17020. http://dx.doi.org/10.1074/jbc.M212031200
25. Mears, J.A., P. Ray, and J.E. Hinshaw. 2007. A corkscrew model for dynamin constriction. Structure. 15:1190-1202. http://dx.doi.org/10.1016/j.str.2007.08.012
26. Mears, J.A., L.L. Lackner, S. Fang, E. Ingerman, J. Nunnari, and J.E. Hinshaw. 2011. Conformational changes in Dnm1 support a contractile mechanism for mitochondrial fission. Nat. Struct. Mol. Biol. 18:20-26. http://dx.doi.org/10.1038/nsmb.1949
27. Moss, T.J., C. Andreazza, A. Verma, A. Daga, and J.A. McNew. 2011. Membrane fusion by the GTPase atlastin requires a conserved C-terminal cytoplasmic tail and dimerization through the middle domain. Proc. Natl. Acad. Sci. USA. 108:11133-11138. http://dx.doi.org/10.1073/pnas.1105056108
28. Mozdy, A.D., J.M. McCaffery, and J.M. Shaw. 2000. Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p. J. Cell Biol. 151:367-380. http://dx.doi.org/10.1083/jcb.151.2.367
29. Naylor, K., E. Ingerman, V. Okreglak, M. Marino, J.E. Hinshaw, and J. Nunnari. 2006. Mdv1 interacts with assembled dnm1 to promote mitochondrial division. J. Biol. Chem. 281:2177-2183. http://dx.doi.org/10.1074/jbc.M507943200
30. Nishida, K., F. Yagisawa, H. Kuroiwa, Y. Yoshida, and T. Kuroiwa. 2007. WD40 protein Mda1 is purified with Dnm1 and forms a dividing ring for mitochondria before Dnm1 in Cyanidioschyzon merolae. Proc. Natl. Acad.
31. Orr-Weaver, T.L., J.W. Szostak, and R.J. Rothstein. 1983. Genetic applications of yeast transformation with linear and gapped plasmids. Methods Enzymol. 101:228-245. http://dx.doi.org/10.1016/0076-6879(83)01017-4
32. Orso, G., D. Pendin, S. Liu, J. Tosetto, T.J. Moss, J.E. Faust, M. Micaroni, A. Egorova, A. Martinuzzi, J.A. McNew, and A. Daga. 2009. Homotypic fusion of ER membranes requires the dynamin-like GTPase atlastin. Nature. 460:978-983. http://dx.doi.org/10.1038/nature08280
33. Otera, H., C. Wang, M.M. Cleland, K. Setoguchi, S. Yokota, R.J. Youle, and K. Mihara. 2010. Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J. Cell Biol. 191:1141-1158. http://dx.doi.org/10.1083/jcb.201007152
34. Otsuga, D., B.R. Keegan, E. Brisch, J.W. Thatcher, G.J. Hermann, W. Bleazard, and J.M. Shaw. 1998. The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast. J. Cell Biol. 143:333-349. http://dx.doi.org/10.1083/jcb.143.2.333
35. Palmer, C.S., L.D. Osellame, D. Laine, O.S. Koutsopoulos, A.E. Frazier, and M.T. Ryan. 2011. MiD49 and MiD51, new components of the mitochondrial fission machinery. EMBO Rep. 12:565-573. http://dx.doi.org/10.1038/embor.2011.54
36. Praefcke, G.J., and H.T. McMahon. 2004. The dynamin superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell Biol. 5:133-147. http://dx.doi.org/10.1038/nrm1313
37. Rapaport, D., M. Brunner, W. Neupert, and B. Westermann. 1998. Fzo1p is a mitochondrial outer membrane protein essential for the biogenesis of functional mitochondria in Saccharomyces cerevisiae. J. Biol. Chem. 273:20150-20155. http://dx.doi.org/10.1074/jbc.273.32.20150
38. Sesaki, H., and R.E. Jensen. 1999. Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J. Cell Biol. 147:699-706. http://dx.doi.org/10.1083/jcb.147.4.699
39. Strack, S., and J.T. Cribbs. 2012. Allosteric modulation of Drp1 mechanoenzyme assembly and mitochondrial fission by the variable domain. J. Biol. Chem. 287:10990-11001. http://dx.doi.org/10.1074/jbc.M112.342105
40. Tieu, Q., and J. Nunnari. 2000. Mdv1p is a WD repeat protein that interacts with the dynamin-related GTPase, Dnm1p, to trigger mitochondrial division. J. Cell Biol. 151:353-366. http://dx.doi.org/10.1083/jcb.151.2.353
41. van der Bliek, A.M. 1999. Functional diversity in the dynamin family. Trends Cell Biol. 9:96-102. http://dx.doi.org/10.1016/S0962-8924(98)01490-1
42. Zhang, Y., N.C. Chan, H.B. Ngo, H. Gristick, and D.C. Chan. 2012. Crystal structure of mitochondrial fission complex reveals scaffolding function for mitochondrial division 1 (Mdv1) coiled coil. J. Biol. Chem. 287:9855-9861. http://dx.doi.org/10.1074/jbc.M111.329359
43. Zhao, J., T. Liu, S. Jin, X. Wang, M. Qu, P. Uhlén, N. Tomilin, O. Shupliakov, U. Lendahl, and M. Nistér. 2011. Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission. EMBO J. 30:2762-2778. http://dx.doi.org/10.1038/emboj.2011.198