The molecular mechanisms of OPA1-mediated optic atrophy in Drosophila model and prospects for antioxidant treatment

PLoS Genetics

Volumn 4, Issue 1, 2008, Pages 0062-0071

  Yarosh, Will ^a,b   Monserrate, Jessica ^b   Tong, James Jiayuan ^a,b   Tse, Stephanie ^a   Le, Phung Khanh ^a   Nguyen, Kimberly ^a   Brachmann, Carrie B ^b   Wallace, Douglas C ^a,b   Huang, Taosheng ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; COPPER ZINC SUPEROXIDE DISMUTASE; MITOCHONDRIAL PROTEIN; PROTEIN OPA1; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; OPA1 PROTEIN, DROSOPHILA; OPA1 PROTEIN, HUMAN; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOSOMAL DOMINANT DISORDER; CELL LOSS; CONTROLLED STUDY; DROSOPHILA; EYE DEVELOPMENT; GENE; GENE INSERTION; GENE MUTATION; GENE OVEREXPRESSION; HETEROZYGOSITY; HOMOZYGOSITY; LETHALITY; NONHUMAN; OPA1 GENE; OPTIC NERVE ATROPHY; PATHOGENESIS; PHENOTYPE; RETINA CONE; TRANSPOSON; VISUAL FIELD DEFECT; VISUAL IMPAIRMENT; AMINO ACID SEQUENCE; ANIMAL; AUTOSOMAL DOMINANT OPTIC ATROPHY; CHEMISTRY; DISEASE MODEL; DOMINANT GENE; EYE; GENE DOSAGE; GENE EXPRESSION REGULATION; GENETIC PROCEDURES; GENETICS; HOMOZYGOTE; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; PATHOLOGY; PENETRANCE; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; ANTIOXIDANTS; DISEASE MODELS, ANIMAL; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA; DROSOPHILA PROTEINS; EYE; GENE DOSAGE; GENES, DOMINANT; GENES, INSECT; GENETIC TECHNIQUES; GTP PHOSPHOHYDROLASES; HOMOZYGOTE; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MUTATION; OPTIC ATROPHY, AUTOSOMAL DOMINANT; PENETRANCE; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SUPEROXIDE DISMUTASE; VITAMIN E;

EID: 38949208881     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.0040006     Document Type: Article

References (48)

1. Bette S, Schlaszus H, Wissinger B, Meyermann R, Mittelbronn M (2005) OPA1, associated with autosomal dominant optic atrophy, is widely expressed in the human brain. Acta Neuropathol (Berl) 109: 393-399.
2. Kjer B, Eiberg H, Kjer P, Rosenberg T (1996) Dominant optic atrophy mapped to chromosome 3q region. II. Clinical and epidemiological aspects. Acta Ophthalmol Scand 74: 3-7.
3. Votruba M, Aijaz S, Moore AT (2003) A review of primary hereditary optic neuropathies. J Inherit Metab Dis 26: 209-227.
4. Carelli V, Ross-Cisneros FN, Sadun AA (2004) Mitochondrial dysfunction as a cause of optic neuropathies. Prog Retin Eye Res 23: 53-89.
5. Votruba M, Moore AT, Bhattacharya SS (1998) Clinical features, molecular genetics, and pathophysiology of dominant optic atrophy. J Med Genet 35: 793-800.
6. Kjer P, Jensen OA, Klinken L (1983) Histopathology of eye, optic nerve and brain in a case of dominant optic atrophy. Acta Ophthalmol (Copenh) 61: 300-312.
7. Toomes C, Marchbank NJ, Mackey DA, Craig JE, Newbury-Ecob RA, et al. (2001) Spectrum, frequency and penetrance of OPA1 mutations in dominant optic atrophy. Hum Mol Genet 10: 1369-1378.
8. Ozden S, Duzcan F, Wollnik B, Cetin OG, Sahiner T, et al. (2002) Progressive autosomal dominant optic atrophy and sensorineural hearing loss in a Turkish family. Ophthalmic Genet 23: 29-36.
9. Chen AS, Kovach MJ, Herman K, Avakian A, Frank W, et al. (2000) Clinical heterogeneity in autosomal dominant optic atrophy in two 3q28-qter linked central Illinois families. Genet Med 2: 283-289.
10. Gorgone G, Li Volti S, Cavallaro N, Conti L, Profeta GM, et al. (1986) Familial optic atrophy with sex-influenced severity. A new variety of autosomal-dominant optic atrophy? Ophthalmologica 192: 28-33.
11. Huang T, Whang JD, Kimonis V (2006) Sex-influenced autosomal dominant optic atrophy is caused by mutations of IVS9 +2A>G in the OPA1 gene. Genet Med 8: 59.
12. Delettre C, Lenaers G, Griffoin JM, Gigarel N, Lorenzo C, et al. (2000) Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 26: 207-210.
13. Alexander C, Votruba M, Pesch UE, Thiselton DL, Mayer S, et al. (2000) OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat Genet 26: 211-215.
14. Pesch UE, Leo-Kottler B, Mayer S, Jurklies B, Kellner U, et al. (2001) OPA1 mutations in patients with autosomal dominant optic atrophy and evidence for semi-dominant inheritance. Hum Mol Genet 10: 1359-1368.
15. Misaka T, Miyashita T, Kubo Y (2002) 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: 15834-15842.
16. Frezza C, Cipolat S, Martins de Brito O, Micaroni M, Beznoussenko GV, et al. (2006) OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126: 177-189.
17. Chan DC (2006) Dissecting mitochondrial fusion. Dev Cell 11: 592-594.
18. Duvezin-Caubet S, Jagasia R, Wagener J, Hofmann S, Trifunovic A, et al. (2006) Proteolytic processing of OPA1 links mitochondrial dysfunction to alterations in mitochondrial morphology. J Biol Chem 281: 37972-37979.
19. Cipolat S, Rudka T, Hartmann D, Costa V, Serneels L, et al. (2006) Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell 126: 163-175.
20. Cipolat S, Martins de Brito O, Dal Zilio B, Scorrano L (2004) OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc Natl Acad Sci U S A 101: 15927-15932.
21. Lee YJ, Jeong SY, Karbowski M, Smith CL, Youle RJ (2004) Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol Biol Cell 15: 5001-5011.
22. Zhang Y, Chan DC (2007) New insights into mitochondrial fusion. FEBS Lett 581: 2168-2173.
23. Lodi R, Tonon C, Valentino ML, Iotti S, Clementi V, et al. (2004) Deficit of in vivo mitochondrial ATP production in OPA1-related dominant optic atrophy. Ann Neurol 56: 719-723.
24. Arnoult D, Grodet A, Lee YJ, Estaquier J, 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.
25. Alavi MV, Bette S, Schimpf S, Schuettauf F, Schraermeyer U, et al. (2007) A splice site mutation in the murine Opa1 gene features pathology of autosomal dominant optic atrophy. Brain 130: 1029-1042.
26. Davies VJ, Hollins AJ, Piechota MJ, Yip W, Davies JR, et al. (2007) Opa1 deficiency in a mouse model of Autosomal Dominant Optic Atrophy impairs mitochondrial morphology, optic nerve structure and visual function. Hum Mol Genet 16: 1307-1318.
27. Brachmann CB, Cagan RL (2003) Patterning the fly eye: the role of apoptosis. Trends Genet 19: 91-96.
28. McQuibban GA, Lee JR, Zheng L, Juusola M, Freeman M (2006) Normal mitochondrial dynamics requires rhomboid-7 and affects Drosophila lifespan and neuronal function. Curr Biol 16: 982-989.
29. Liao TS, Call GB, Guptan P, Cespedes A, Marshall J, et al. (2006) An efficient genetic screen in Drosophila to identify nuclear-encoded genes with mitochondrial function. Genetics 174: 525-533.
30. Chen J, Call GB, Beyer E, Bui C, Cespedes A, et al. (2005) Discovery-based science education: functional genomic dissection in Drosophila by undergraduate researchers. PLoS Biol 3: e59. doi: 10.1371/journal.pbio. 0030059
31. Gottlieb E (2006) OPA1 and PARL keep a lid on apoptosis. Cell 126: 27-29.
32. Kamei S, Chen-Kuo-Chang M, Cazevieille C, Lenaers G, Olichon A, et al. (2005) Expression of the Opa1 mitochondrial protein in retinal ganglion cells: its downregulation causes aggregation of the mitochondrial network. Invest Ophthalmol Vis Sci 46: 4288-4294.
33. Misaka T, Murate M, Fujimoto K, Kubo Y (2006) The dynamin-related mouse mitochondrial GTPase OPA1 alters the structure of the mitochondrial inner membrane when exogenously introduced into COS-7 cells. Neurosci Res 55: 123-133.
34. Olichon A, Elachouri G, Baricault L, Delettre C, Belenguer P, et al. (2006) OPA1 alternate splicing uncouples an evolutionary conserved function in mitochondrial fusion from a vertebrate restricted function in apoptosis. Cell Death Differ 14: 682-692.
35. Ali SS, Xiong C, Lucero J, Behrens MM, Dugan LL, et al. (2006) Gender differences in free radical homeostasis during aging: shorter-lived female C57BL6 mice have increased oxidative stress. Aging Cell 5: 565-574.
36. Flores GV, Daga A, Kalhor HR, Banerjee U (1998) Lozenge is expressed in pluripotent precursor cells and patterns multiple cell types in the Drosophila eye through the control of cell-specific transcription factors. Development 125: 3681-3687.
37. Mandal S, Guptan P, Owusu-Ansah E, Banerjee U (2005) Mitochondrial regulation of cell cycle progression during development as revealed by the tenured mutation in Drosophila. Dev Cell 9: 843-854.
38. Tong JJ, Schriner SE, McCleary D, Day BJ, Wallace DC (2007) Life extension through neurofibromin mitochondrial regulation and antioxidant therapy for neurofibromatosis-1 in Drosophila melanogaster. Nat Genet 39: 476-485.
39. Wang D, Qian L, Xiong H, Liu J, Neckameyer WS, et al. (2006) Antioxidants protect PINK1-dependent dopaminergic neurons in Drosophila. Proc Natl Acad Sci U S A 103: 13520-13525.
40. Ready DF, Hanson TE, Benzer S (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53: 217-240.
41. Wolff T, Ready DF (1991) The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave. Development 113: 841-850.
42. Monserrate JP, Baker Brachmann C (2007) Identification of the death zone: a spatially restricted region for programmed cell death that sculpts the fly eye. Cell Death Differ 14: 209-217.
43. Miller DT, Cagan RL (1998) Local induction of patterning and programmed cell death in the developing Drosophila retina. Development 125: 2327-2335.
44. Mendes CS, Arama E, Brown S, Scherr H, Srivastava M, et al. (2006) Cytochrome c-d regulates developmental apoptosis in the Drosophila retina. EMBO J Rep 7: 933-939.
45. Morey M, Corominas M, Serras F (2003) DIAP1 suppresses ROS-induced apoptosis caused by impairment of the selD/sps1 homolog in Drosophila. J Cell Sci 116: 4597-4604.
46. Simon HU, Haj-Yehia A, Levi-Schaffer F (2000) Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5: 415-418.
47. Curtin JF, Donovan M, Cotter TG (2002) Regulation and measurement of oxidative stress in apoptosis. J Immunol Methods 265: 49-72.
48. Zhu QW, Pearson-White S, Luo KX (2005) Requirement for the SnoN oncoprotein in transforming growth factor beta-induced oncogenic transformation of fibroblast cells. Mol Cell Biol 25: 10731-10744.