Stage-specific enhanced expression of mitochondrial fusion and fission factors during spermatogenesis in rat testis

Biochemical and Biophysical Research Communications

Volumn 311, Issue 2, 2003, Pages 424-432

  Honda, Shinji ^a   Hirose, Shigehisa ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

Dynamin related protein; Maternal inheritance; Mitochondria; Mitofusin; Sperm

Indexed keywords

DYNAMIN RELATED PROTEIN 1; DYNAMIN RELATED PROTEIN 1 ANTIBODY; MITOCHONDRIAL PROTEIN; MITOFUSIN 1; MITOFUSIN 2; MITOFUSIN 2 ANTIBODY; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONJUGATION; CONTROLLED STUDY; FERTILIZATION; IMMUNOHISTOCHEMISTRY; MALE; MITOCHONDRION; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; RAT; SEMINIFEROUS TUBULE; SPERMATID; SPERMATOGENESIS; TESTIS;

EID: 0242268107     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2003.10.008     Document Type: Article

References (66)

1. Saraste M. Oxidative phosphorylation at the finde siecle. Science. 283:1999;1488-1493.
2. Brenner C., Kroemer G. Mitochondria - the death signal integrators. Science. 289:2000;1150-1151.
3. Green D.R., Reed J.C. Mitochondria and apoptosis. Science. 281:1998;1309-1312.
4. Bakeeva L.E., Chentsov Y.S., Skulachev V.P. Ontogenesis of mitochondrial reticulum in rat diaphragm muscle. Eur. J. Cell Biol. 25:1981;175-181.
5. Bereiter-Hahn J., Voth M. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc. Res. Tech. 27:1994;198-219.
6. Kawano S., Takano H., Kuroiwa T. Sexuality of mitochondria: fusion, recombination, and plasmids. Int. Rev. Cytol. 161:1995;49-110.
7. Nunnari J., Marshall W.F., Straight A., Murray A., Sedat J.W., Walter P. Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. Mol. Biol. Cell. 8:1997;1233-1242.
8. Okamoto K., Perlman P.S., Butow R.A. The sorting of mitochondrial DNA and mitochondrial proteins in zygotes: preferential transmission of mitochondrial DNA to the medial bud. J. Cell Biol. 142:1998;613-623.
9. Nakada K., Inoue K., Ono T., Isobe K., Ogura A., Goto Y.I., Nonaka I., Hayashi J.I. Inter-mitochondrial complementation: mitochondria-specific system preventing mice from expression of disease phenotypes by mutant mtDNA. Nat. Med. 7:2001;934-940.
10. Ono T., Isobe K., Nakada K., Hayashi J.I. Human cells are protected from mitochondrial dysfunction by complementation of DNA products in fused mitochondria. Nat. Genet. 28:2001;272-275.
11. Yaffe M.P. The machinery of mitochondrial inheritance and behavior. Science. 283:1999;1493-1497.
12. Griparic L., van der Bliek A.M. The many shapes of mitochondrial membranes. Traffic. 2:2001;235-244.
13. Hermann G.J., Shaw J.M. Mitochondrial dynamics in yeast. Annu. Rev. Cell Dev. Biol. 14:1998;265-303.
14. Jensen R.E., Hobbs A.E., Cerveny K.L., Sesaki H. Yeast mitochondrial dynamics: fusion, division, segregation, and shape. Microsc. Res. Tech. 51:2000;573-583.
15. Yoon Y., McNiven M.A. Mitochondrial division: new partners in membrane pinching. Curr. Biol. 11:2001;R67-R70.
16. Mozdy A.D., Shaw J.M. A fuzzy mitochondrial fusion apparatus comes into focus. Nat. Rev. Mol. Cell. Biol. 4:2003;468-478.
17. Westermann B. Merging mitochondria matters: cellular role and molecular machinery of mitochondrial fusion. EMBO Rep. 3:2002;527-531.
18. Hales K.G., Fuller M.T. Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell. 90:1997;121-129.
19. Fritz S., Rapaport D., Klanner E., Neupert W., Westermann B. Connection of the mitochondrial outer and inner membranes by Fzo1 is critical for organellar fusion. J. Cell Biol. 152:2001;683-692.
20. Hermann G.J., Thatcher J.W., Mills J.P., Hales K.G., Fuller M.T., Nunnari J., Shaw J.M. Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J. Cell Biol. 143:1998;359-373.
21. Rapaport D., Brunner M., Neupert W., Westermann B. Fzo1p is a mitochondrial outer membrane protein essential for the biogenesis of functional mitochondria in Saccharomyces cerevisiae. J. Biol. Chem. 273:1998;20150-20155.
22. 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. 1:1999;298-304.
23. Sesaki H., Jensen R.E. Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J. Cell Biol. 147:1999;699-706.
24. 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. 14:2003;2342-2356.
25. Wong E.D., Wagner J.A., Scott S.V., Okreglak V., Holewinske T.J., Cassidy-Stone A., Nunnari J. The intramitochondrial dynamin-related GTPase, Mgm1p, is a component of a protein complex that mediates mitochondrial fusion. J. Cell Biol. 160:2003;303-311.
26. Santel A., Fuller M.T. Control of mitochondrial morphology by a human mitofusin. J. Cell Sci. 114:2001;867-874.
27. Legros F., Lombes A., Frachon P., Rojo M. Mitochondrial fusion in human cells is efficient, requires the inner membrane potential, and is mediated by mitofusins. Mol. Biol. Cell. 13:2002;4343-4354.
28. Rojo M., Legros F., Chateau D., Lombes A. Membrane topology and mitochondrial targeting of mitofusins, ubiquitous mammalian homologs of the transmembrane GTPase Fzo. J. Cell Sci. 115:2002;1663-1674.
29. Ishihara N., Jofuku A., Eura Y., Mihara K. Regulation of mitochondrial morphology by membrane potential, and DRP1-dependent division and FZO1-dependent fusion reaction in mammalian cells. Biochem. Biophys. Res. Commun. 301:2003;891-898.
30. Chen H., Detmer S.A., Ewald A.J., Griffin E.E., Fraser S.E., Chan D.C. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160:2003;189-200.
31. Bach D., Pich S., Soriano F.X., Vega N., Baumgartner B., Oriola J., Daugaard J.R., Lloberas J., Camps M., Zierath J.R., Rabasa-Lhoret R., Wallberg-Henriksson H., Laville M., Palacin M., Vidal H., Rivera F., Brand M., Zorzano A. Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism. J. Biol. Chem. 278:2003;17190-17197.
32. Santel A., Frank S., Gaume B., Herrler M., Youle R.J., Fuller M.T. Mitofusin-1 protein is a generally expressed mediator of mitochondrial fusion in mammalian cells. J. Cell Sci. 116:2003;2763-2774.
33. Fritz S., Weinbach N., Westermann B. Mdm30 is an F-box protein required for maintenance of fusion-competent mitochondria in yeast. Mol. Biol. Cell. 14:2003;2303-2313.
34. Fekkes P., Shepard K.A., Yaffe M.P. Gag3p, an outer membrane protein required for fission of mitochondrial tubules. J. Cell Biol. 151:2000;333-340.
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. 151:2000;367-380.
36. 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. 143:1998;333-349.
37. Tieu Q., Nunnari J. Mdv1p is a WD repeat protein that interacts with the dynamin-related GTPase, Dnm1p, to trigger mitochondrial division. J. Cell Biol. 151:2000;353-366.
38. Pitts K.R., Yoon Y., Krueger E.W., McNiven M.A. The dynamin-like protein DLP1 is essential for normal distribution and morphology of the endoplasmic reticulum and mitochondria in mammalian cells. Mol. Biol. Cell. 10:1999;4403-4417.
39. Smirnova E., Griparic L., Shurland D.L., van der Bliek A.M. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell. 12:2001;2245-2256.
40. Smirnova E., Shurland D.L., Ryazantsev S.N., van der Bliek A.M. A human dynamin-related protein controls the distribution of mitochondria. J. Cell Biol. 143:1998;351-358.
41. Karbowski M., Lee Y.J., Gaume B., Jeong S.Y., Frank S., Nechushtan A., Santel A., Fuller M., Smith C.L., Youle R.J. Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J. Cell Biol. 159:2002;931-938.
42. Breckenridge D.G., Stojanovic M., Marcellus R.C., Shore G.C. Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol. J. Cell Biol. 160:2003;1115-1127.
43. Kaneda H., Hayashi J., Takahama S., Taya C., Lindahl K.F., Yonekawa H. Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc. Natl. Acad. Sci. USA. 92:1995;4542-4546.
44. Shitara H., Kaneda H., Sato A., Inoue K., Ogura A., Yonekawa H., Hayashi J.I. Selective and continuous elimination of mitochondria microinjected into mouse eggs from spermatids, but not from liver cells, occurs throughout embryogenesis. Genetics. 156:2000;1277-1284.
45. Sutovsky P., Moreno R.D., Ramalho-Santos J., Dominko T., Simerly C., Schatten G. Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol. Reprod. 63:2000;582-590.
46. Sutovsky P., Moreno R.D., Ramalho-Santos J., Dominko T., Simerly C., Schatten G. Ubiquitin tag for sperm mitochondria. Nature. 402:1999;371-372.
47. Thompson W.E., Ramalho-Santos J., Sutovsky P. Ubiquitination of prohibitin in mammalian sperm mitochondria: possible roles in the regulation of mitochondrial inheritance and sperm quality control. Biol. Reprod. 69:2003;254-260.
48. Rajapurohitam V., Morales C.R., El Alfy M., Lefrancois S., Bedard N., Wing S.S. Activation of a UBC4-dependent pathway of ubiquitin conjugation during postnatal development of the rat testis. Dev. Biol. 212:1999;217-228.
49. Wing S.S., Bedard N., Morales C., Hingamp P., Trasler J. A novel rat homolog of the Saccharomyces cerevisiae ubiquitin-conjugating enzymes UBC4 and UBC5 with distinct biochemical features is induced during spermatogenesis. Mol. Cell. Biol. 16:1996;4064-4072.
50. Sesaki H., Jensen R.E. UGO1 encodes an outer membrane protein required for mitochondrial fusion. J. Cell Biol. 152:2001;1123-1134.
51. Wong E.D., Wagner J.A., Gorsich S.W., McCaffery J.M., Shaw J.M., Nunnari J. The dynamin-related GTPase, Mgm1p, is an intermembrane space protein required for maintenance of fusion competent mitochondria. J. Cell Biol. 151:2000;341-352.
52. 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., Hamel C.P. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat. Genet. 26:2000;207-210.
53. 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., Wissinger B. OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat. Genet. 26:2000;211-215.
54. Olichon A., Emorine L.J., Descoins E., Pelloquin L., Brichese L., Gas N., Guillou E., Delettre C., Valette A., Hamel C.P., Ducommun B., Lenaers G., Belenguer P. The human dynamin-related protein OPA1 is anchored to the mitochondrial inner membrane facing the inter-membrane space. FEBS Lett. 523:2002;171-176.
55. Olichon A., Baricault L., Gas N., Guillou E., Valette A., Belenguer P., Lenaers G. Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome. c release and apoptosis J. Biol. Chem. 278:2003;7743-7746.
56. Misaka T., Miyashita T., Kubo Y. Primary structure of a dynamin-related mouse mitochondrial GTPase and its distribution in brain, subcellular localization, and effect on mitochondrial morphology. J. Biol. Chem. 277:2002;15834-15842.
57. Imoto M., Tachibana I., Urrutia R. Identification and functional characterization of a novel human protein highly related to the yeast dynamin-like GTPase Vps1p. J. Cell Sci. 111:1998;1341-1349.
58. Kamimoto T., Nagai Y., Onogi H., Muro Y., Wakabayashi T., Hagiwara M. Dymple, a novel dynamin-like high molecular weight GTPase lacking a proline-rich carboxyl-terminal domain in mammalian cells. J. Biol. Chem. 273:1998;1044-1051.
59. Shin H.W., Shinotsuka C., Torii S., Murakami K., Nakayama K. Identification and subcellular localization of a novel mammalian dynamin-related protein homologous to yeast Vps1p and Dnm1p. J. Biochem. (Tokyo). 122:1997;525-530.
60. 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. 274:1999;2780-2785.
61. Yoon Y., Pitts K.R., McNiven M.A. Mammalian dynamin-like protein DLP1 tubulates membranes. Mol. Biol. Cell. 12:2001;2894-2905.
62. 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. 140:1998;779-793.
63. 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. 23:2003;5409-5420.
64. 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. 158:2002;445-452.
65. Inoue K., Nakada K., Ogura A., Isobe K., Goto Y., Nonaka I., Hayashi J.I. Generation of mice with mitochondrial dysfunction by introducing mouse mtDNA carrying a deletion into zygotes. Nat. Genet. 26:2000;176-181.
66. Hutchinson C.A., Newbold J.E., Poter S.S. Maternal inheritance of mammalian mitochondrial DNA. Nature. 251:1974;536-538.