Subtle neurological and metabolic abnormalities in an Opa1 mouse model of autosomal dominant optic atrophy

Experimental Neurology

Volumn 220, Issue 2, 2009, Pages 404-409

  Alavi, Marcel V ^a   Fuhrmann, Nico ^a   Nguyen, Huu Phuc ^b   Yu Wai Man, Patrick ^c,d   Heiduschka, Peter ^b   Chinnery, Patrick F ^c   Wissinger, Bernd ^a  

^a Centre for Ophthalmology   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d ROYAL VICTORIA INFIRMARY   (United Kingdom)

Author keywords

Accelerod; ADOA; Life expectancy; Limb grasping; Mouse; mtDNA; Neuromuscular abnormalities; Opa1; Rotarod; SHIRPA; Subclinical; Tremor

Indexed keywords

CYTOCHROME C OXIDASE; MITOCHONDRIAL DNA; OPTIC ATROPHY 1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOSOMAL DOMINANT OPTIC ATROPHY; BODY WEIGHT; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; FOOD INTAKE; GENE MUTATION; GENETIC MODEL; LIFESPAN; MOUSE; NEUROMUSCULAR DISEASE; NONHUMAN; PRIORITY JOURNAL; RETINA GANGLION CELL; ROTAROD TEST; SKELETAL MUSCLE; TREMOR;

ADIPOSE TISSUE; ANIMALS; BODY WEIGHT; DNA, MITOCHONDRIAL; GENE DELETION; GTP PHOSPHOHYDROLASES; IMMUNOHISTOCHEMISTRY; LONGEVITY; MICE; MUTATION; OPTIC ATROPHY, AUTOSOMAL DOMINANT; PHENOTYPE; POSTURAL BALANCE; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES;

EID: 71549143796     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2009.09.026     Document Type: Article

References (44)

1. Alavi M.V., Bette S., Schimpf S., Schuettauf F., Schraermeyer U., Wehrl H.F., Ruttiger L., Beck S.C., Tonagel F., Pichler B.J., Knipper M., Peters T., Laufs J., and Wissinger B. A splice site mutation in the murine Opa1 gene features pathology of autosomal dominant optic atrophy. Brain 130 (2007) 1029-1042
2. 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., and 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
3. Amati-Bonneau P., Valentino M.L., Reynier P., Gallardo M.E., Bornstein B., Boissiere A., Campos Y., Rivera H., de la Aleja J.G., Carroccia R., Iommarini L., Labauge P., Figarella-Branger D., Marcorelles P., Furby A., Beauvais K., Letournel F., Liguori R., La Morgia C., Montagna P., Liguori M., Zanna C., Rugolo M., Cossarizza A., Wissinger B., Verny C., Schwarzenbacher R., Martin M.A., Arenas J., Ayuso C., Garesse R., Lenaers G., Bonneau D., and Carelli V. OPA1 mutations induce mitochondrial DNA instability and optic atrophy 'plus' phenotypes. Brain 131 (2008) 338-351
4. Barbet F., Hakiki S., Orssaud C., Gerber S., Perrault I., Hanein S., Ducroq D., Dufier J.L., Munnich A., Kaplan J., and Rozet J.M. A third locus for dominant optic atrophy on chromosome 22q. J. Med. Genet. 42 (2005) e1
5. Bette S., Schlaszus H., Wissinger B., Meyermann R., and Mittelbronn M. OPA1, associated with autosomal dominant optic atrophy, is widely expressed in the human brain. Acta Neuropathol. (Berl.) 109 (2005) 393-399
6. Caldwell J.B., Howard R.O., and Riggs L.A. Dominant juvenile optic atrophy. A study in two families and review of hereditary disease in childhood. Arch. Ophthalmol. 85 (1971) 133-147
7. Cipolat S., Martins de Brito O., Dal Zilio B., and Scorrano L. OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 15927-15932
8. Cipolat S., Rudka T., Hartmann D., Costa V., Serneels L., Craessaerts K., Metzger K., Frezza C., Annaert W., D'Adamio L., Derks C., Dejaegere T., Pellegrini L., D'Hooge R., Scorrano L., and De Strooper B. Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell 126 (2006) 163-175
9. Davies V.J., Hollins A.J., Piechota M.J., Yip W., Davies J.R., White K.E., Nicols P.P., Boulton M.E., and Votruba M. Opa1 deficiency in a mouse model of autosomal dominant optic atrophy impairs mitochondrial morphology, optic nerve structure and visual function. Hum. Mol. Genet. 16 (2007) 1307-1318
10. 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., and Hamel C.P. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat. Genet. 26 (2000) 207-210
11. Ferraris S., Clark S., Garelli E., Davidzon G., Moore S.A., Kardon R.H., Bienstock R.J., Longley M.J., Mancuso M., Gutierrez Rios P., Hirano M., Copeland W.C., and DiMauro S. Progressive external ophthalmoplegia and vision and hearing loss in a patient with mutations in POLG2 and OPA1. Arch. Neurol. 65 (2008) 125-131
12. Ferre M., Amati-Bonneau P., Tourmen Y., Malthiery Y., and Reynier P. eOPA1: an online database for OPA1 mutations. Hum. Mutat. 25 (2005) 423-428
13. Frezza C., Cipolat S., Martins de Brito O., Micaroni M., Beznoussenko G.V., Rudka T., Bartoli D., Polishuck R.S., Danial N.N., De Strooper B., and Scorrano L. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126 (2006) 177-189
14. Friedman M.J., Shah A.G., Fang Z.H., Ward E.G., Warren S.T., Li S., and Li X.J. Polyglutamine domain modulates the TBP-TFIIB interaction: implications for its normal function and neurodegeneration. Nat. Neurosci. 10 (2007) 1519-1528
15. Fuhrmann N., Alavi M.V., Bitoun P., Woernle S., Auburger G., Leo-Kottler B., Yu-Wai-Man P., Chinnery P., and Wissinger B. Genomic rearrangements in OPA1 are frequent in patients with autosomal dominant optic atrophy. J. Med. Genet. 46 (2009) 136-144
16. Hales K.G., and Fuller M.T. Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell 90 (1997) 121-129
17. Hayasaki H., Shimada M., Kanbara K., and Watanabe M. Regional difference in muscle fiber type and glucose uptake of mouse gastrocnemius at rest. Cell Mol. Biol. (2001) (Noisy-le-grand) 47 Online Pub, OL135-140
18. Heiduschka P., Schnichels S., Fuhrmann N., Hofmeister S., Schraermeyer U., Wissinger B., and Alavi M.V. Retinal ganglion cells are primarily affected in an animal model of OPA1 associated autosomal dominant optic atrophy. Invest. Ophthalmol. Vis. Sci. (2009) doi:10.1167/iovs.09-3606
19. Hudson G., Amati-Bonneau P., Blakely E.L., Stewart J.D., He L., Schaefer A.M., Griffiths P.G., Ahlqvist K., Suomalainen A., Reynier P., McFarland R., Turnbull D.M., Chinnery P.F., and Taylor R.W. Mutation of OPA1 causes dominant optic atrophy with external ophthalmoplegia, ataxia, deafness and multiple mitochondrial DNA deletions: a novel disorder of mtDNA maintenance. Brain 131 (2008) 329-337
20. Jaeger W. Hereditary optic atrophies in childhood. J. Genet. Hum. 15 (1966) 312-321
21. Johnson M.A., and Barron M.J. Muscle biopsy analysis. In: Lane R.J.M. (Ed). Handbook of Muscle Disease (1996), Marcel Dekker, New York, USA 61-79
22. Kerrison J.B., Arnould V.J., Ferraz Sallum J.M., Vagefi M.R., Barmada M.M., Li Y., Zhu D., and Maumenee I.H. Genetic heterogeneity of dominant optic atrophy, Kjer type: identification of a second locus on chromosome 18q12.2-12.3. Arch. Ophthalmol. 117 (1999) 805-810
23. Kivlin J.D., Lovrien E.W., Bishop D.T., and Maumenee I.H. Linkage analysis in dominant optic atrophy. Am. J. Hum. Genet. 35 (1983) 1190-1195
24. Kjer B., Eiberg H., Kjer P., and Rosenberg T. Dominant optic atrophy mapped to chromosome 3q region. II. Clinical and epidemiological aspects. Acta Ophthalmol. Scand. 74 (1996) 3-7
25. Klein R., Silos-Santiago I., Smeyne R.J., Lira S.A., Brambilla R., Bryant S., Zhang L., Snider W.D., and Barbacid M. Disruption of the neurotrophin-3 receptor gene trkC eliminates la muscle afferents and results in abnormal movements. Nature 368 (1994) 249-251
26. Kline L.B., and Glaser J.S. Dominant optic atrophy. The clinical profile. Arch. Ophthalmol. 97 (1979) 1680-1686
27. Lorenz B. Hereditary optic atrophy. Ophthalmologe 91 (1994) 831-850
28. Mangiarini L., Sathasivam K., Seller M., Cozens B., Harper A., Hetherington C., Lawton M., Trottier Y., Lehrach H., Davies S.W., and Bates G.P. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87 (1996) 493-506
29. Manttari S., and Jarvilehto M. Comparative analysis of mouse skeletal muscle fibre type composition and contractile responses to calcium channel blocker. BMC Physiol. 5 (2005) 4
30. Marchbank N.J., Craig J.E., Leek J.P., Toohey M., Churchill A.J., Markham A.F., Mackey D.A., Toomes C., and Inglehearn C.F. Deletion of the OPA1 gene in a dominant optic atrophy family: evidence that haploinsufficiency is the cause of disease. J. Med. Genet. e47 (2002) 39
31. Nguyen H.P., Kobbe P., Rahne H., Worpel T., Jager B., Stephan M., Pabst R., Holzmann C., Riess O., Korr H., Kantor O., Petrasch-Parwez E., Wetzel R., Osmand A., and von Horsten S. Behavioral abnormalities precede neuropathological markers in rats transgenic for Huntington's disease. Hum. Mol. Genet. 15 (2006) 3177-3194
32. 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., and 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
33. Olichon A., Baricault L., Gas N., Guillou E., Valette A., Belenguer P., and 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
34. Olichon A., Elachouri G., Baricault L., Delettre C., Belenguer P., and Lenaers G. OPA1 alternate splicing uncouples an evolutionary conserved function in mitochondrial fusion from a vertebrate restricted function in apoptosis. Cell Death Differ. 14 (2007) 682-692
35. Reynier P., Amati-Bonneau P., Verny C., Olichon A., Simard G., Guichet A., Bonnemains C., Malecaze F., Malinge M.C., Pelletier J.B., Calvas P., Dollfus H., Belenguer P., Malthiery Y., Lenaers G., and Bonneau D. OPA3 gene mutations responsible for autosomal dominant optic atrophy and cataract. J. Med. Genet. e110 (2004) 41
36. Roggeveen H.C., de Winter A.P., and Went L.N. Studies in dominant optic atrophy. Ophthalmic Paediatr. Genet. 5 (1985) 103-109
37. Rowlatt C., Chesterman F.C., and Sheriff M.U. Lifespan, age changes and tumour incidence in an ageing C57BL mouse colony. Lab. Anim. 10 (1976) 419-442
38. Spinazzi M., Cazzola S., Bortolozzi M., Baracca A., Loro E., Casarin A., Solaini G., Sgarbi G., Casalena G., Cenacchi G., Malena A., Frezza C., Carrara F., Angelini C., Scorrano L., Salviati L., and Vergani L. A novel deletion in the GTPase domain of OPA1 causes defects in mitochondrial morphology and distribution, but not in function. Hum. Mol. Genet. 17 21 (2008) 3291-3302
39. Taylor R.W., Schaefer A.M., Barron M.J., McFarland R., and Turnbull D.M. The diagnosis of mitochondrial muscle disease. Neuromuscu. Dis. 14 (2004) 237-245
40. Twig G., Elorza A., Molina A.J., Mohamed H., Wikstrom J.D., Walzer G., Stiles L., Haigh S.E., Katz S., Las G., Alroy J., Wu M., Py B.F., Yuan J., Deeney J.T., Corkey B.E., and Shirihai O.S. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27 (2008) 433-446
41. Tyynismaa H., Mjosund K.P., Wanrooij S., Lappalainen I., Ylikallio E., Jalanko A., Spelbrink J.N., Paetau A., and Suomalainen A. Mutant mitochondrial helicase Twinkle causes multiple mtDNA deletions and a late-onset mitochondrial disease in mice. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 17687-17692
42. Yu Wai Man C.Y., Chinnery P.F., and Griffiths P.G. Optic neuropathies-importance of spatial distribution of mitochondria as well as function. Med. Hypotheses 65 (2005) 1038-1042
43. Yu-Wai-Man P., Davies V.J., Piechota M.J., Cree L.M., Votruba M., and Chinnery P.F. Secondary mtDNA defects do not cause optic nerve dysfunction in a mouse model of dominant optic atrophy. Invest. Ophthalmol. Vis. Sci. 50 10 (2009) 4561-4566
44. Zeviani M. OPA1 mutations and mitochondrial DNA damage: keeping the magic circle in shape. Brain 131 (2008) 314-317