Mouse mtDNA mutant model of Leber hereditary optic neuropathy

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

Volumn 109, Issue 49, 2012, Pages 20065-20070

  Lin, Chun Shi ^a,b   Sharpley, Mark S ^a,b   Fan, Weiwei ^b   Waymire, Katrina G ^b,c   Sadun, Alfredo A ^d   Carelli, Valerio ^d,e,f   Ross Cisneros, Fred N ^d   Baciu, Peter ^g   Sung, Eric ^g   McManus, Meagan J ^a   Pan, Billy X ^d   Gil, Daniel W ^g   MacGregor, Grant R ^b,c   Wallace, Douglas C ^a,b,h  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^e IRCCS ISTITUTO DELLE SCIENZE NEUROLOGICHE DI BOLOGNA   (Italy)

^f UNIVERSITY OF BOLOGNA   (Italy)

^g ALLERGAN INC   (United States)

^h UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Maternal inheritance; Neurodegenerative disease; Ophthalmology; Oxidative phosphorylation

Indexed keywords

MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DEMYELINATION; ELECTRORETINOGRAM; FEMALE; LEBER HEREDITARY OPTIC NEUROPATHY; MALE; MOUSE; NERVE FIBER DEGENERATION; NONHUMAN; OPTIC NERVE FIBER; PRIORITY JOURNAL; SYNAPTOSOME;

ADENOSINE TRIPHOSPHATE; AGE FACTORS; ANIMALS; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; DNA, MITOCHONDRIAL; ELECTRORETINOGRAPHY; HUMANS; IMMUNOBLOTTING; MICE; MUTATION, MISSENSE; NADH DEHYDROGENASE; OPTIC ATROPHY, HEREDITARY, LEBER; OPTIC NERVE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RETINA; SYNAPTOSOMES;

ANIMALIA; MUS;

EID: 84870623870     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1217113109     Document Type: Article

References (48)

1. Wallace DC, et al. (1988) Mitochondrial DNA mutation associated with Leber's hereditary optic neuropathy. Science 242(4884):1427-1430. (Pubitemid 19008070)
2. Sadun AA, La Morgia C, Carelli V (2011) Leber's hereditary optic neuropathy. Curr Treat Options Neurol 13(1):109-117.
3. Huoponen K, Vilkki J, Aula P, Nikoskelainen EK, Savontaus ML (1991) A new mtDNA mutation associated with Leber hereditary optic neuroretinopathy. Am J Hum Genet 48(6):1147-1153.
4. Johns DR, Neufeld MJ, Park RD (1992) An ND-6 mitochondrial DNA mutation associated with Leber hereditary optic neuropathy. Biochem Biophys Res Commun 187(3):1551-1557.
5. Jun AS, Brown MD, Wallace DC (1994) A mitochondrial DNA mutation at np 14459 of the ND6 gene associated with maternally inherited Leber's hereditary optic neuropathy and dystonia. Proc Natl Acad Sci USA 91(13):6206-6210. (Pubitemid 24188312)
6. Malfatti E, et al. (2007) Novel mutations of ND genes in complex I deficiency associated with mitochondrial encephalopathy. Brain 130(Pt 7):1894-1904. (Pubitemid 47343808)
7. Savini G, et al. (2005) Retinal nerve fiber layer evaluation by optical coherence tomography in unaffected carriers with Leber's hereditary optic neuropathy mutations. Ophthalmology 112(1):127-131. (Pubitemid 40075331)
8. Ventura DF, et al. (2007) Male prevalence of acquired color vision defects in asymptomatic carriers of Leber's hereditary optic neuropathy. Invest Ophthalmol Vis Sci 48 (5):2362-2370. (Pubitemid 351261318)
9. Hirst J (2010) Towards the molecular mechanism of respiratory complex I. Biochem J 425(2):327-339.
10. Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417(1):1-13.
11. Trounce IA, Kim YL, Jun AS, Wallace DC (1996) Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol 264:484-509.
12. Jun AS, Trounce IA, Brown MD, Shoffner JM, Wallace DC (1996) Use of transmitochondrial cybrids to assign a complex I defect to the mitochondrial DNA-encoded NADH dehydrogenase subunit 6 gene mutation at nucleotide pair 14459 that causes Leber hereditary optic neuropathy and dystonia. Mol Cell Biol 16(3):771-777.
13. Jun AS, Trounce IA, Brown MD, Shoffner JM, Wallace DC (1996) Use of transmitochondrial cybrids to assign a complex I defect to the mitochondrial DNA-encoded NADH dehydrogenase subunit 6 gene mutation at nucleotide pair 14459 that causes Leber hereditary optic neuropathy and dystonia. Mole Cell Biol 16(3):771-777.
14. Brown MD, Allen JC, Van Stavern GP, Newman NJ, Wallace DC (2001) Clinical, genetic, and biochemical characterization of a Leber hereditary optic neuropathy family containing both the 11778 and 14484 primary mutations. Am J Med Genet 104(4):331-338. (Pubitemid 33131652)
15. Brown MD, Trounce IA, Jun AS, Allen JC, Wallace DC (2000) Functional analysis of lymphoblast and cybrid mitochondria containing the 3460, 11778, or 14484 Leber's hereditary optic neuropathy mitochondrial DNA mutation. J Biol Chem 275(51):39831-39836. (Pubitemid 32064602)
16. Carelli V, et al. (1999) Biochemical features of mtDNA 14484 (ND6/M64V) point mutation associated with Leber's hereditary optic neuropathy. Ann Neurol 45(3):320-328. (Pubitemid 29120036)
17. Carelli V, et al. (1997) Leber's hereditary optic neuropathy: Biochemical effect of 11778/ND4 and 3460/ND1 mutations and correlation with the mitochondrial genotype. Neurology 48(6):1623-1632.
18. Baracca A, et al. (2005) Severe impairment of complex I-driven adenosine triphosphate synthesis in leber hereditary optic neuropathy cybrids. Arch Neurol 62(5):730-736. (Pubitemid 40656087)
19. Beretta S, et al. (2006) Partial mitochondrial complex I inhibition induces oxidative damage and perturbs glutamate transport in primary retinal cultures. Relevance to Leber Hereditary Optic Neuropathy (LHON). Neurobiol Dis 24(2):308-317. (Pubitemid 44572749)
20. Floreani M, et al. (2005) Antioxidant defences in cybrids harboring mtDNA mutations associated with Leber's hereditary optic neuropathy. FEBS J 272(5):1124-1135. (Pubitemid 40314932)
21. Ghelli A, et al. (2008) Protection against oxidant-induced apoptosis by exogenous glutathione in Leber hereditary optic neuropathy cybrids. Invest Ophthalmol Vis Sci 49(2):671-676.
22. Sala G, et al. (2008) Antioxidants partially restore glutamate transport defect in leber hereditary optic neuropathy cybrids. J Neurosci Res 86(15):3331-3337.
23. Giordano C, et al. (2011) Oestrogens ameliorate mitochondrial dysfunction in Leber's hereditary optic neuropathy. Brain 134(Pt 1):220-234.
24. Acín-Pérez R, et al. (2004) Respiratory complex III is required to maintain complex I in mammalian mitochondria. Mol Cell 13(6):805-815. (Pubitemid 38438476)
25. Fan W, et al. (2008) A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations. Science 319(5865):958-962. (Pubitemid 351263767)
26. Sligh JE, et al. (2000) Maternal germ-line transmission of mutant mtDNAs from embryonic stem cell-derived chimeric mice. Proc Natl Acad Sci USA 97(26):14461-14466. (Pubitemid 32016598)
27. MacGregor GR, Fan WW, Waymire KG, Wallace DC (2006) Generating animal models of human mitochondrial genetic disease using mouse ES cells. Embryonic Stem Cells, Practical Approach Series, eds Notarianni E, Evans MJ (Oxford University Press, New York, NY), pp 72-104.
28. Marella M, Seo BB, Thomas BB, Matsuno-Yagi A, Yagi T (2010) Successful amelioration of mitochondrial optic neuropathy using the yeast NDI1 gene in a rat animal model. PLoS ONE 5(7):e11472.
29. Cock HR, Cooper JM, Schapira AH (1999) Functional consequences of the 3460-bp mitochondrial DNA mutation associated with Leber's hereditary optic neuropathy. J Neurol Sci 165(1):10-17. (Pubitemid 29298074)
30. Silva JM, Wong A, Carelli V, Cortopassi GA (2009) Inhibition of mitochondrial function induces an integrated stress response in oligodendroglia. Neurobiol Dis 34(2):357-365.
31. Earle WR (1943) Production of malignancy in vitro. IV The mouse fibroblast cultures and changes seen in living cells. J Natl Cancer Inst 4:165-212.
32. Ishikawa K, et al. (2008) ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science 320(5876):661-664. (Pubitemid 351928347)
33. Hashizume O, et al. (2012) Specific mitochondrial DNA mutation in mice regulates diabetes and lymphoma development. Proc Natl Acad Sci USA 109(26):10528-10533.
34. Fan W, Lin CS, Potluri P, Procaccio V, Wallace DC (2012) mtDNA lineage analysis of mouse L-cell lines reveals the accumulation of multiple mtDNA mutants and intermolecular recombination. Genes Dev 26(4):384-394.
35. Salomão SR, et al. (2004) Visual electrophysiologic findings in patients from an extensive Brazilian family with Leber's hereditary optic neuropathy. Doc Ophthalmol 108(2):147-155.
36. Shibata K, Shibagaki Y, Nagai C, Iwata M (1999) Visual evoked potentials and electroretinograms in an early stage of Leber's hereditary optic neuropathy. J Neurol 246(9):847-849. (Pubitemid 29467166)
37. Carelli V, Ross-Cisneros FN, Sadun AA (2004) Mitochondrial dysfunction as a cause of optic neuropathies. Prog Retin Eye Res 23(1):53-89. (Pubitemid 38177172)
38. Sadun AA, Win PH, Ross-Cisneros FN, Walker SO, Carelli V (2000) Leber's hereditary optic neuropathy differentially affects smaller axons in the optic nerve. Trans Am Ophthalmol Soc 98:223-232, discussion 232-235.
39. Brand MD (2010) The sites and topology of mitochondrial superoxide production. Exp Gerontol 45(7-8):466-472.
40. Pryde KR, Hirst J (2011) Superoxide is produced by the reduced flavin in mitochondrial complex I: A single, unified mechanism that applies during both forward and reverse electron transfer. J Biol Chem 286(20):18056-18065.
41. Wong A, Cortopassi G (1997) mtDNA mutations confer cellular sensitivity to oxidant stress that is partially rescued by calcium depletion and cyclosporin A. Biochem Biophys Res Commun 239(1):139-145. (Pubitemid 27480330)
42. Porcelli AM, et al. (2009) Respiratory complex I dysfunction due to mitochondrial DNA mutations shifts the voltage threshold for opening of the permeability transition pore toward resting levels. J Biol Chem 284(4):2045-2052.
43. Schriner SE, et al. (2005) Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 308(5730):1909-1911. (Pubitemid 40941874)
44. Melov S, et al. (1998) A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat Genet 18(2):159-163. (Pubitemid 28082464)
45. Melov S, et al. (2001) Lifespan extension and rescue of spongiform encephalopathy in superoxide dismutase 2 nullizygous mice treated with superoxide dismutase-catalase mimetics. J Neurosci 21(21):8348-8353. (Pubitemid 33051432)
46. Bayona-Bafaluy MP, Manfredi G, Moraes CT (2003) A chemical enucleation method for the transfer of mitochondrial DNA to rho(o) cells. Nucleic Acids Res 31(16):e98.
47. Trounce I, Wallace DC (1996) Production of transmitochondrial mouse cell lines by cybrid rescue of rhodamine-6G pre-treated L-cells. Somat Cell Mol Genet 22(1):81-85. (Pubitemid 26177599)
48. Nagy A, Gertsenstein M, Vinterson K, Behringer R (2003) Manipulating the Mouse Embryo, a Laboratory Manual (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY), 3rd Ed.