In vivo functions of Drp1: Lessons learned from yeast genetics and mouse knockouts

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 8, 2014, Pages 1179-1185

  Sesaki, Hiromi ^a   Adachi, Yoshihiro ^a   Kageyama, Yusuke ^a   Itoh, Kie ^a   Iijima, Miho ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Dynamin related GTPase; Membrane fission; Mitochondrion; Mouse; Neurodegeneration; Yeast

Indexed keywords

DYNAMIN; DYNAMIN RELATED PROTEIN 1; MITOCHONDRIAL DNA; UNCLASSIFIED DRUG; DYNAMIN I; FUNGAL DNA; FUNGAL PROTEIN; ISOPROTEIN;

ACTIN FILAMENT; AGING; BRAIN DEVELOPMENT; DEGENERATIVE DISEASE; EMBRYO DEVELOPMENT; GENETIC MODEL; GENETICS; IN VIVO STUDY; KNOCKOUT MOUSE; MITOCHONDRION; MITOPHAGY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; YEAST; CELL AGING; CELL STRUCTURE; CELL SURVIVAL; ENDOPLASMIC RETICULUM; FUNGAL GENETICS; HUMAN; MAMMALIAN GENETICS; MOUSE MODEL;

DYNAMIN-RELATED GTPASE; MEMBRANE FISSION; MITOCHONDRION; MOUSE; NEURODEGENERATION; YEAST;

ANIMALS; DYNAMINS; GENE KNOCKOUT TECHNIQUES; HUMANS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; SACCHAROMYCES CEREVISIAE;

EID: 84903268566     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.11.024     Document Type: Review

References (100)

1. Nunnari J., Suomalainen A. Mitochondria: in sickness and in health. Cell 2012, 148:1145-1159.
2. Wallace D.C. Bioenergetic origins of complexity and disease. Cold Spring Harb. Symp. Quant. Biol. 2011, 76:1-16.
3. Youle R.J., van der Bliek A.M. Mitochondrial fission, fusion, and stress. Science 2012, 337:1062-1065.
4. Tamura Y., Itoh K., Sesaki H. SnapShot: mitochondrial dynamics. Cell 2011, 145:1158. (1158 e1151).
5. Shutt T.E., McBride H.M. Staying cool in difficult times: mitochondrial dynamics, quality control and the stress response. Biochim. Biophys. Acta 2013, 1833:417-424.
6. Chan D.C. Fusion and fission: interlinked processes critical for mitochondrial health. Annu. Rev. Genet. 2012, 46:265-287.
7. Itoh K., Nakamura K., Iijima M., Sesaki H. Mitochondrial dynamics in neurodegeneration. Trends Cell Biol. 2013, 23:64-71.
8. Reddy P.H., Reddy T.P. Mitochondria as a therapeutic target for aging and neurodegenerative diseases. Curr. Alzheimer Res. 2011, 8:393-409.
9. Cho D.H., Nakamura T., Lipton S.A. Mitochondrial dynamics in cell death and neurodegeneration. Cell. Mol. Life Sci. 2010, 67:3435-3447.
10. Knott A.B., Perkins G., Schwarzenbacher R., Bossy-Wetzel E. Mitochondrial fragmentation in neurodegeneration. Nat. Rev. Neurosci. 2008, 9:505-518.
11. Waterham H.R., Koster J., van Roermund C.W., Mooyer P.A., Wanders R.J., Leonard J.V. A lethal defect of mitochondrial and peroxisomal fission. N. Engl. J. Med. 2007, 356:1736-1741.
12. Otera H., Ishihara N., Mihara K. New insights into the function and regulation of mitochondrial fission. Biochim. Biophys. Acta 2013, 1833:1256-1268.
13. Elgass K., Pakay J., Ryan M.T., Palmer C.S. Recent advances into the understanding of mitochondrial fission. Biochim. Biophys. Acta 2013, 1833:150-161.
14. Schmid S.L., Frolov V.A. Dynamin: functional design of a membrane fission catalyst. Annu. Rev. Cell Dev. Biol. 2011, 27:79-105.
15. Ferguson S.M., De Camilli P. Dynamin, a membrane-remodelling GTPase. Nat. Rev. Mol. Cell Biol. 2012, 13:75-88.
16. Kageyama Y., Zhang Z., Sesaki H. Mitochondrial division: molecular machinery and physiological functions. Curr. Opin. Cell Biol. 2011, 23:427-434.
17. Westermann B. Mitochondrial dynamics in model organisms: what yeasts, worms and flies have taught us about fusion and fission of mitochondria. Semin. Cell Dev. Biol. 2010, 21:542-549.
18. Okamoto K., Shaw J.M. Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu. Rev. Genet. 2005, 39:503-536.
19. Mears J.A., Lackner L.L., Fang S., Ingerman E., Nunnari J., Hinshaw J.E. Conformational changes in Dnm1 support a contractile mechanism for mitochondrial fission. Nat. Struct. Mol. Biol. 2011, 18:20-26.
20. Zhang P., Hinshaw J.E. Three-dimensional reconstruction of dynamin in the constricted state. Nat. Cell Biol. 2001, 3:922-926.
21. Yoon Y., Pitts K.R., McNiven M.A. Mammalian dynamin-like protein DLP1 tubulates membranes. Mol. Biol. Cell 2001, 12:2894-2905.
22. Ingerman E., Perkins E.M., Marino M., Mears J.A., McCaffery J.M., Hinshaw J.E., Nunnari J. Dnm1 forms spirals that are structurally tailored to fit mitochondria. J.Cell Biol. 2005, 170:1021-1027.
23. Ford M.G., Jenni S., Nunnari J. The crystal structure of dynamin. Nature 2011, 477:561-566.
24. Frohlich C., Grabiger S., Schwefel D., Faelber K., Rosenbaum E., Mears J., Rocks O., Daumke O. Structural insights into oligomerization and mitochondrial remodelling of dynamin 1-like protein. EMBO J. 2013, 32:1280-1292.
25. Faelber K., Posor Y., Gao S., Held M., Roske Y., Schulze D., Haucke V., Noe F., Daumke O. Crystal structure of nucleotide-free dynamin. Nature 2011, 477:556-560.
26. Chang C.R., Manlandro C.M., Arnoult D., Stadler J., Posey A.E., Hill R.B., Blackstone C. 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. 2010, 285:32494-32503.
27. Strack S., Cribbs J.T. Allosteric modulation of Drp1 mechanoenzyme assembly and mitochondrial fission by the variable domain. J. Biol. Chem. 2012, 287:10990-11001.
28. Montessuit S., Somasekharan S.P., Terrones O., Lucken-Ardjomande S., Herzig S., Schwarzenbacher R., Manstein D.J., Bossy-Wetzel E., Basanez G., Meda P., Martinou J.C. Membrane remodeling induced by the dynamin-related protein Drp1 stimulates Bax oligomerization. Cell 2010, 142:889-901.
29. Zhu P.P., Patterson A., Stadler J., Seeburg D.P., Sheng M., Blackstone C. Intra- and intermolecular domain interactions of the C-terminal GTPase effector domain of the multimeric dynamin-like GTPase Drp1. J. Biol. Chem. 2004, 279:35967-35974.
30. Fukushima N.H., Brisch E., Keegan B.R., Bleazard W., Shaw J.M. The GTPase effector domain sequence of the Dnm1p GTPase regulates self-assembly and controls a rate-limiting step in mitochondrial fission. Mol. Biol. Cell 2001, 12:2756-2766.
31. Yoon Y., Pitts K.R., Dahan S., McNiven M.A. A novel dynamin-like protein associates with cytoplasmic vesicles and tubules of the endoplasmic reticulum in mammalian cells. J. Cell Biol. 1998, 140:779-793.
32. Howng S.L., Sy W.D., Cheng T.S., Lieu A.S., Wang C., Tzou W.S., Cho C.L., Hong Y.R. Genomic organization, alternative splicing, and promoter analysis of human dynamin-like protein gene. Biochem. Biophys. Res. Commun. 2004, 314:766-772.
33. Uo T., Dworzak J., Kinoshita C., Inman D.M., Kinoshita Y., Horner P.J., Morrison R.S. Drp1 levels constitutively regulate mitochondrial dynamics and cell survival in cortical neurons. Exp. Neurol. 2009, 218:274-285.
34. Strack S., Wilson T.J., Cribbs J.T. Cyclin-dependent kinases regulate splice-specific targeting of dynamin-related protein 1 to microtubules. J. Cell Biol. 2013, 201:1037-1051.
35. Mozdy A.D., McCaffery J.M., Shaw J.M. Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p. J. Cell Biol. 2000, 151:367-380.
36. Cerveny K.L., Jensen R.E. The WD-repeats of Net2p interact with Dnm1p and Fis1p to regulate division of mitochondria. Mol. Biol. Cell 2003, 14:4126-4139.
37. Tieu Q., Okreglak V., Naylor K., Nunnari J. The WD repeat protein, Mdv1p, functions as a molecular adaptor by interacting with Dnm1p and Fis1p during mitochondrial fission. J. Cell Biol. 2002, 158:445-452.
38. Griffin E.E., Graumann J., Chan D.C. The WD40 protein Caf4p is a component of the mitochondrial fission machinery and recruits Dnm1p to mitochondria. J. Cell Biol. 2005, 170:237-248.
39. Lackner L.L., Horner J.S., Nunnari J. Mechanistic analysis of a dynamin effector. Science 2009, 325:874-877.
40. Koirala S., Guo Q., Kalia R., Bui H.T., Eckert D.M., Frost A., Shaw J.M. Interchangeable adaptors regulate mitochondrial dynamin assembly for membrane scission. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E1342-E1351.
41. Cerveny K.L., Studer S.L., Jensen R.E., Sesaki H. Yeast mitochondrial division and distribution require the cortical num1 protein. Dev. Cell 2007, 12:363-375.
42. Hammermeister M., Schodel K., Westermann B. Mdm36 is a mitochondrial fission-promoting protein in Saccharomyces cerevisiae. Mol. Biol. Cell 2010, 21:2443-2452.
43. Michelot A., Drubin D.G. Building distinct actin filament networks in a common cytoplasm. Curr. Biol. 2011, 21:R560-R569.
44. Boldogh I.R., Yang H.C., Pon L.A. Mitochondrial inheritance in budding yeast. Traffic 2001, 2:368-374.
45. Klecker T., Scholz D., Fortsch J., Westermann B. The yeast cell cortical protein Num1 integrates mitochondrial dynamics into cellular architecture. J. Cell Sci. 2013, 126:2924-2930.
46. Loson O.C., Song Z., Chen H., Chan D.C. Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol. Biol. Cell 2013, 24:659-667.
47. Otera H., Wang C., Cleland M.M., Setoguchi K., Yokota S., Youle R.J., Mihara K. Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J. Cell Biol. 2010, 191:1141-1158.
48. Gandre-Babbe S., van der Bliek A.M. The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells. Mol. Biol. Cell 2008, 19:2402-2412.
49. Friedman J.R., Lackner L.L., West M., DiBenedetto J.R., Nunnari J., Voeltz G.K. ER tubules mark sites of mitochondrial division. Science 2011, 334:358-362.
50. Palmer C.S., Osellame L.D., Laine D., Koutsopoulos O.S., Frazier A.E., Ryan M.T. MiD49 and MiD51, new components of the mitochondrial fission machinery. EMBO Rep. 2011, 12:565-573.
51. Zhao J., Liu T., Jin S., Wang X., Qu M., Uhlen P., Tomilin N., Shupliakov O., Lendahl U., Nister M. Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission. EMBO J. 2011, 30:2762-2778.
52. Liu T., Yu R., Jin S.B., Han L., Lendahl U., Zhao J., Nister M. The mitochondrial elongation factors MIEF1 and MIEF2 exert partially distinct functions in mitochondrial dynamics. Exp. Cell Res. 2013, 319:2893-2904.
53. Yoon Y., Krueger E.W., Oswald B.J., McNiven M.A. The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol. Cell. Biol. 2003, 23:5409-5420.
54. James D.I., Parone P.A., Mattenberger Y., Martinou J.C. hFis1, a novel component ofthe mammalian mitochondrial fission machinery. J. Biol. Chem. 2003, 278:36373-36379.
55. Jofuku A., Ishihara N., Mihara K. Analysis of functional domains of rat mitochondrial Fis1, the mitochondrial fission-stimulating protein. Biochem. Biophys. Res. Commun. 2005, 333:650-659.
56. Han X.J., Lu Y.F., Li S.A., Kaitsuka T., Sato Y., Tomizawa K., Nairn A.C., Takei K., Matsui H., Matsushita M. CaM kinase Ialpha-induced phosphorylation of Drp1 regulates mitochondrial morphology. J. Cell Biol. 2008, 182:573-585.
57. Wang W., Wang Y., Long J., Wang J., Haudek S.B., Overbeek P., Chang B.H., Schumacker P.T., Danesh F.R. Mitochondrial fission triggered by hyperglycemia is mediated by ROCK1 activation in podocytes and endothelial cells. Cell Metab. 2012, 15:186-200.
58. Helle S.C., Kanfer G., Kolar K., Lang A., Michel A.H., Kornmann B. Organization andfunction of membrane contact sites. Biochim. Biophys. Acta 2013, 1833:2526-2541.
59. Korobova F., Ramabhadran V., Higgs H.N. An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2. Science 2013, 339:464-467.
60. 2+ entry. Neurobiol. Dis. 2013, 55:140-151.
61. de Brito O.M., Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 2008, 456:605-610.
62. Quintanilla R.A., Dolan P.J., Jin Y.N., Johnson G.V. Truncated tau and Abeta cooperatively impair mitochondria in primary neurons. Neurobiol. Aging 2012, 33(619):e625-e635.
63. Xie H., Guan J., Borrelli L.A., Xu J., Serrano-Pozo A., Bacskai B.J. Mitochondrial alterations near amyloid plaques in an Alzheimer's disease mouse model. J. Neurosci. Off. J. Soc. Neurosci. 2013, 33:17042-17051.
64. DuBoff B., Gotz J., Feany M.B. Tau promotes neurodegeneration via DRP1 mislocalization invivo. Neuron 2012, 75:618-632.
65. DuBoff B., Feany M., Gotz J. Why size matters-balancing mitochondrial dynamics in Alzheimer's disease. Trends Neurosci. 2013, 36:325-335.
66. Manczak M., Reddy P.H. Abnormal interaction between the mitochondrial fission protein Drp1 and hyperphosphorylated tau in Alzheimer's disease neurons: implications for mitochondrial dysfunction and neuronal damage. Hum. Mol. Genet. 2012, 21:2538-2547.
67. Sesaki H., Jensen R.E. Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J. Cell Biol. 1999, 147:699-706.
68. Bleazard W., McCaffery J.M., King E.J., Bale S., Mozdy A., Tieu Q., Nunnari J., Shaw J.M. The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat. Cell Biol. 1999, 1:298-304.
69. Otsuga D., Keegan B.R., Brisch E., Thatcher J.W., Hermann G.J., Bleazard W., Shaw J.M. The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast. J. Cell Biol. 1998, 143:333-349.
70. Gorsich S.W., Shaw J.M. Importance of mitochondrial dynamics during meiosis and sporulation. Mol. Biol. Cell 2004, 15:4369-4381.
71. Sesaki H., Jensen R.E. UGO1 encodes an outer membrane protein required for mitochondrial fusion. J. Cell Biol. 2001, 152:1123-1134.
72. Sesaki H., Southard S.M., Yaffe M.P., Jensen R.E. Mgm1p, a dynamin-related GTPase, is essential for fusion of the mitochondrial outer membrane. Mol. Biol. Cell 2003, 14:2342-2356.
73. Germain M., Mathai J.P., McBride H.M., Shore G.C. Endoplasmic reticulum BIK initiates DRP1-regulated remodelling of mitochondrial cristae during apoptosis. EMBO J. 2005, 24:1546-1556.
74. Rabl R., Soubannier V., Scholz R., Vogel F., Mendl N., Vasiljev-Neumeyer A., Korner C., Jagasia R., Keil T., Baumeister W., Cyrklaff M., Neupert W., Reichert A.S. Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj1 and Su e/g. J. Cell Biol. 2009, 185:1047-1063.
75. Hoppins S., Collins S.R., Cassidy-Stone A., Hummel E., Devay R.M., Lackner L.L., Westermann B., Schuldiner M., Weissman J.S., Nunnari J. A mitochondrial-focusedgenetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria. J. Cell Biol. 2011, 195:323-340.
76. von der Malsburg K., Muller J.M., Bohnert M., Oeljeklaus S., Kwiatkowska P., Becker T., Loniewska-Lwowska A., Wiese S., Rao S., Milenkovic D., Hutu D.P., Zerbes R.M., Schulze-Specking A., Meyer H.E., Martinou J.C., Rospert S., Rehling P., Meisinger C., Veenhuis M., Warscheid B., van der Klei I.J., Pfanner N., Chacinska A., van der Laan M. Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev. Cell 2011, 21:694-707.
77. Harner M., Korner C., Walther D., Mokranjac D., Kaesmacher J., Welsch U., Griffith J., Mann M., Reggiori F., Neupert W. The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J. 2011, 30:4356-4370.
78. Itoh K., Tamura Y., Iijima M., Sesaki H. Effects of Fcj1-Mos1 and mitochondrial division on aggregation of mitochondrial DNA nucleoids and organelle morphology. Mol. Biol. Cell 2013, 24:1842-1851.
79. Murley A., Lackner L.L., Osman C., West M., Voeltz G.K., Walter P., Nunnari J. ER-associated mitochondrial division links the distribution of mitochondria and mitochondrial DNA in yeast. Elife 2013, 2:e00422.
80. Ban-Ishihara R., Ishihara T., Sasaki N., Mihara K., Ishihara N. Dynamics of nucleoid structure regulated by mitochondrial fission contributes to cristae reformation and release of cytochrome c. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:11863-11868.
81. Parone P.A., Da Cruz S., Tondera D., Mattenberger Y., James D.I., Maechler P., Barja F., Martinou J.C. Preventing mitochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. PLoS One 2008, 3:e3257.
82. Kanki T., Wang K., Baba M., Bartholomew C.R., Lynch-Day M.A., Du Z., Geng J., Mao K., Yang Z., Yen W.L., Klionsky D.J. A genomic screen for yeast mutants defective in selective mitochondria autophagy. Mol. Biol. Cell 2009, 20:4730-4738.
83. Mao K., Wang K., Liu X., Klionsky D.J. The scaffold protein atg11 recruits fission machinery to drive selective mitochondria degradation by autophagy. Dev. Cell 2013, 26:9-18.
84. Okamoto K., Kondo-Okamoto N., Ohsumi Y. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev. Cell 2009, 17:87-97.
85. Kanki T., Wang K., Cao Y., Baba M., Klionsky D.J. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev. Cell 2009, 17:98-109.
86. Scheckhuber C.Q., Erjavec N., Tinazli A., Hamann A., Nystrom T., Osiewacz H.D. Reducing mitochondrial fission results in increased life span and fitness of two fungal ageing models. Nat. Cell Biol. 2007, 9:99-105.
87. Yang C.C., Chen D., Lee S.S., Walter L. The dynamin-related protein DRP-1 and the insulin signaling pathway cooperate to modulate Caenorhabditis elegans longevity. Aging Cell 2011, 10:724-728.
88. Kageyama Y., Zhang Z., Roda R., Fukaya M., Wakabayashi J., Wakabayashi N., Kensler T.W., Reddy P.H., Iijima M., Sesaki H. Mitochondrial division ensures the survival of postmitotic neurons by suppressing oxidative damage. J. Cell Biol. 2012, 197:535-551.
89. Zhang Z., Kageyama Y., Sesaki H. Mitochondrial division prevents neurodegeneration. Autophagy 2012, 8:1531-1533.
90. Shin H.W., Takatsu H., Mukai H., Munekata E., Murakami K., Nakayama K. Intermolecular and interdomain interactions of a dynamin-related GTP-binding protein, Dnm1p/Vps1p-like protein. J. Biol. Chem. 1999, 274:2780-2785.
91. Wakabayashi J., Zhang Z., Wakabayashi N., Tamura Y., Fukaya M., Kensler T.W., Iijima M., Sesaki H. The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice. J. Cell Biol. 2009, 186:805-816.
92. Ishihara N., Nomura M., Jofuku A., Kato H., Suzuki S.O., Masuda K., Otera H., Nakanishi Y., Nonaka I., Goto Y., Taguchi N., Morinaga H., Maeda M., Takayanagi R., Yokota S., Mihara K. Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat. Cell Biol. 2009, 11:958-966.
93. Manczak M., Sesaki H., Kageyama Y., Reddy P.H. Dynamin-related protein 1 heterozygote knockout mice do not have synaptic and mitochondrial deficiencies. Biochim. Biophys. Acta 2012, 1822:862-874.
94. Verstreken P., Ly C.V., Venken K.J., Koh T.W., Zhou Y., Bellen H.J. Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 2005, 47:365-378.
95. Li H., Alavian K.N., Lazrove E., Mehta N., Jones A., Zhang P., Licznerski P., Graham M., Uo T., Guo J., Rahner C., Duman R.S., Morrison R.S., Jonas E.A. A Bcl-xL-Drp1 complex regulates synaptic vesicle membrane dynamics during endocytosis. Nat. Cell Biol. 2013, 15:773-785.
96. Youle R.J., Narendra D.P. Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 2011, 12:9-14.
97. Sterky F.H., Lee S., Wibom R., Olson L., Larsson N.G. Impaired mitochondrial transport and Parkin-independent degeneration of respiratory chain-deficient dopamine neurons invivo. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:12937-12942.
98. Schrader M. Shared components of mitochondrial and peroxisomal division. Biochim. Biophys. Acta 2006, 1763:531-541.
99. Kaur N., Hu J. Dynamics of peroxisome abundance: a tale of division and proliferation. Curr. Opin. Plant Biol. 2009, 12:781-788.
100. Opalinski L., Veenhuis M., van der Klei I.J. Peroxisomes: membrane events accompanying peroxisome proliferation. Int. J. Biochem. Cell Biol. 2011, 43:847-851.