Interchangeable adaptors regulate mitochondrial dynamin assembly for membrane scission

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 15, 2013, Pages

  Koirala, Sajjan ^a   Guo, Qian ^a   Kalia, Raghav ^a   Bui, Huyen T ^a   Eckert, Debra M ^a   Frost, Adam ^a   Shaw, Janet M ^a  

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

Author keywords

Drp1 dnm1; Fis1 mdv1; Mff MiD49 MiD51; Mitochondrial fission dynamin

Indexed keywords

ADAPTOR PROTEIN; DRP1 PROTEIN; DYNAMIN; FIS1 PROTEIN; GUANOSINE TRIPHOSPHATASE; MDV1 PROTEIN; MEMBRANE PROTEIN; MFF PROTEIN; MID PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CELLULAR PARAMETERS; CONTROLLED STUDY; FUNGAL STRAIN; HUMAN; HYDROLYSIS; MITOCHONDRIAL MEMBRANE SCISSION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN STRUCTURE;

CELL DIVISION; DYNAMIN I; DYNAMINS; GREEN FLUORESCENT PROTEINS; GTP PHOSPHOHYDROLASES; GUANOSINE TRIPHOSPHATE; HUMANS; HYDROLYSIS; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; POLYMERS; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84876066609     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1300855110     Document Type: Article

References (64)

1. Praefcke GJ, McMahon HT (2004) The dynamin superfamily: Universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5(2):133-147.
2. Gorsich SW, Shaw JM (2004) Importance of mitochondrial dynamics during meiosis and sporulation. Mol Biol Cell 15(10):4369-4381.
3. Taguchi N, Ishihara N, Jofuku A, Oka T, Mihara K (2007) Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J Biol Chem 282(15):11521-11529.
4. Parone PA, et al. (2008) Preventing mitochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. PLoS ONE 3(9):e3257.
5. Twig G, et al. (2008) Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27(2):433-446.
6. Gomes LC, Di Benedetto G, Scorrano L (2011) During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol 13(5):589-598.
7. Rambold AS, Kostelecky B, Elia N, Lippincott-Schwartz J (2011) Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc Natl Acad Sci USA 108(25):10190-10195.
8. Ishihara N, et al. (2009) Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol 11(8):958-966.
9. Wakabayashi J, et al. (2009) The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice. J Cell Biol 186(6):805-816.
10. Bleazard W, et al. (1999) The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol 1(5):298-304.
11. Labrousse AM, Zappaterra MD, Rube DA, van der Bliek AM (1999) C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol Cell 4(5):815-826.
12. Otsuga D, et al. (1998) The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast. J Cell Biol 143(2):333-349.
13. Sesaki H, Jensen RE (1999) Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J Cell Biol 147(4):699-706.
14. Ingerman E, et al. (2005) Dnm1 forms spirals that are structurally tailored to fit mitochondria. J Cell Biol 170(7):1021-1027.
15. Mears JA, et al. (2011) Conformational changes in Dnm1 support a contractile mechanism for mitochondrial fission. Nat Struct Mol Biol 18(1):20-26.
16. Friedman JR, et al. (2011) ER tubules mark sites of mitochondrial division. Science 334(6054):358-362.
17. Cerveny KL, McCaffery JM, Jensen RE (2001) Division of mitochondria requires a novel DMN1-interacting protein, Net2p. Mol Biol Cell 12(2):309-321.
18. Tieu Q, Nunnari J (2000) Mdv1p is a WD repeat protein that interacts with the dynamin-related GTPase, Dnm1p, to trigger mitochondrial division. J Cell Biol 151(2):353-366.
19. Mozdy AD, McCaffery JM, Shaw JM (2000) Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p. J Cell Biol 151(2):367-380.
20. Naylor K, et al. (2006) Mdv1 interacts with assembled dnm1 to promote mitochondrial division. J Biol Chem 281(4):2177-2183.
21. Lackner LL, Horner JS, Nunnari J (2009) Mechanistic analysis of a dynamin effector. Science 325(5942):874-877.
22. Gandre-Babbe S, van der Bliek AM (2008) The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells. Mol Biol Cell 19(6):2402-2412.
23. Otera H, et al. (2010) Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J Cell Biol 191(6):1141-1158.
24. Palmer CS, et al. (2011) MiD49 and MiD51, new components of the mitochondrial fission machinery. EMBO Rep 12(6):565-573.
25. Zhao J, et al. (2011) Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission. EMBO J 30(14):2762-2778.
26. Griffin EE, Graumann J, Chan DC (2005) The WD40 protein Caf4p is a component of the mitochondrial fission machinery and recruits Dnm1p to mitochondria. J Cell Biol 170(2):237-248.
27. Tieu Q, Okreglak V, Naylor K, Nunnari J (2002) The WD repeat protein, Mdv1p, functions as a molecular adaptor by interacting with Dnm1p and Fis1p during mitochondrial fission. J Cell Biol 158(3):445-452.
28. Koirala S, et al. (2010) Molecular architecture of a dynamin adaptor: Implications for assembly of mitochondrial fission complexes. J Cell Biol 191(6):1127-1139.
29. Cerveny KL, Jensen RE (2003) The WD-repeats of Net2p interact with Dnm1p and Fis1p to regulate division of mitochondria. Mol Biol Cell 14(10):4126-4139.
30. Nunnari J, et al. (1997) Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. Mol Biol Cell 8(7):1233-1242.
31. Twig G, Shirihai OS (2011) The interplay between mitochondrial dynamics and mitophagy. Antioxid Redox Signal 14(10):1939-1951.
32. Chang CR, et al. (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(42):32494-32503.
33. Koch A, et al. (2003) Dynamin-like protein 1 is involved in peroxisomal fission. J Biol Chem 278(10):8597-8605.
34. Kuravi K, et al. (2006) Dynamin-related proteins Vps1p and Dnm1p control peroxisome abundance in Saccharomyces cerevisiae. J Cell Sci 119(Pt 19):3994-4001.
35. Li X, Gould SJ (2003) The dynamin-like GTPase DLP1 is essential for peroxisome division and is recruited to peroxisomes in part by PEX11. J Biol Chem 278(19):17012-17020.
36. Mendl N, et al. (2011) Mitophagy in yeast is independent of mitochondrial fission and requires the stress response gene WHI2. J Cell Sci 124(Pt 8):1339-1350.
37. Okamoto K, Kondo-Okamoto N, Ohsumi Y (2009) Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell 17(1):87-97.
38. Cereghetti GM, et al. (2008) Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc Natl Acad Sci USA 105(41):15803-15808.
39. Chang CR, Blackstone C (2007) Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology. J Biol Chem 282(30):21583-21587.
40. Cribbs JT, Strack S (2007) Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep 8(10):939-944.
41. Han XJ, et al. (2008) CaM kinase I alpha-induced phosphorylation of Drp1 regulates mitochondrial morphology. J Cell Biol 182(3):573-585.
42. Kim H, et al. (2011) Fine-tuning of Drp1/Fis1 availability by AKAP121/Siah2 regulates mitochondrial adaptation to hypoxia. Mol Cell 44(4):532-544.
43. Braschi E, Zunino R, McBride HM (2009) MAPL is a new mitochondrial SUMO E3 ligase that regulates mitochondrial fission. EMBO Rep 10(7):748-754.
44. Figueroa-Romero C, et al. (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(11):3917-3927.
45. Wasiak S, Zunino R, McBride HM (2007) Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J Cell Biol 177(3):439-450.
46. Zunino R, Braschi E, Xu L, McBride HM (2009) Translocation of SenP5 from the nucleoli to the mitochondria modulates DRP1-dependent fission during mitosis. J Biol Chem 284(26):17783-17795.
47. Cho DH, et al. (2009) S-nitrosylation of Drp1 mediates beta-amyloid-related mitochondrial fission and neuronal injury. Science 324(5923):102-105.
48. Horn SR, et al. (2011) Regulation of mitochondrial morphology by APC/CCdh1-mediated control of Drp1 stability. Mol Biol Cell 22(8):1207-1216.
49. Karbowski M, Neutzner A, Youle RJ (2007) The mitochondrial E3 ubiquitin ligase MARCH5 is required for Drp1 dependent mitochondrial division. J Cell Biol 178(1):71-84.
50. Nakamura N, Kimura Y, Tokuda M, Honda S, Hirose S (2006) MARCH-V is a novel mitofusin 2-and Drp1-binding protein able to change mitochondrial morphology. EMBO Rep 7(10):1019-1022.
51. Wang H, et al. (2011) Parkin ubiquitinates Drp1 for proteasome-dependent degradation: Implication of dysregulated mitochondrial dynamics in Parkinson disease. J Biol Chem 286(13):11649-11658.
52. Yonashiro R, et al. (2006) A novel mitochondrial ubiquitin ligase plays a critical role in mitochondrial dynamics. EMBO J 25(15):3618-3626.
53. Guo Q, Koirala S, Perkins EM, McCaffery JM, Shaw JM (2012) The mitochondrial fission adaptors Caf4 and Mdv1 are not functionally equivalent. PLoS ONE 7(12):e53523.
54. Bashkirov PV, et al. (2008) GTPase cycle of dynamin is coupled to membrane squeeze and release, leading to spontaneous fission. Cell 135(7):1276-1286.
55. Hernandez JM, et al. (2012) Membrane fusion intermediates via directional and full assembly of the SNARE complex. Science 336(6088):1581-1584.
56. Wang L, Bose PS, Sigworth FJ (2006) Using cryo-EM to measure the dipole potential of a lipid membrane. Proc Natl Acad Sci USA 103(49):18528-18533.
57. Leforestier A, Lemercier N, Livolant F (2012) Contribution of cryoelectron microscopy of vitreous sections to the understanding of biological membrane structure. Proc Natl Acad Sci USA 109(23):8959-8964.
58. Sundborger A, et al. (2011) An endophilin-dynamin complex promotes budding of clathrin-coated vesicles during synaptic vesicle recycling. J Cell Sci 124(Pt 1):133-143.
59. Takei K, Slepnev VI, Haucke V, De Camilli P (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol 1(1):33-39.
60. Green M, Sambrook J (2012) Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY), 4th Ed.
61. Guthrie C, Fink G (2002) Guide to Yeast Genetics and Molecular Biology. Methods in Enzymology (Academic, Inc., San Diego), Vol 350.
62. Amiott EA, Cohen MM, Saint-Georges Y, Weissman AM, Shaw JM (2009) A mutation associated with CMT2A neuropathy causes defects in Fzo1 GTP hydrolysis, ubiquitylation, and protein turnover. Mol Biol Cell 20(23):5026-5035.
63. Bui HT, Karren MA, Bhar D, Shaw JM (2012) A novel motif in the yeast mitochondrial dynamin Dnm1 is essential for adaptor binding and membrane recruitment. J Cell Biol 199(4):613-622.
64. Leonard M, Song BD, Ramachandran R, Schmid SL (2005) Robust colorimetric assays for dynamin' s basal and stimulated GTPase activities. Methods Enzymol 404:490-503.