Manipulation of mtDNA heteroplasmy in all striated muscles of newborn mice by AAV9-mediated delivery of a mitochondria-targeted restriction endonuclease

Gene Therapy

Volumn 19, Issue 11, 2012, Pages 1101-1106

  Bacman, S R ^a   Williams, S L ^a   Duan, D ^b   Moraes, C T ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b University of Missouri   (United States)

Author keywords

AAV9; Heteroplasmy; Mouse model; mtDNA; Myopathy

Indexed keywords

ADENOASSOCIATED VIRUS 9 VECTOR; MITOCHONDRIAL DNA; PARVOVIRUS VECTOR; RESTRICTION ENDONUCLEASE; UNCLASSIFIED DRUG;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS 9; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE MUTATION; GENETIC MANIPULATION; HAPLOTYPE; HETEROPLASMY; MITOCHONDRIAL MYOPATHY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS PARTICLE; VIRUS RECOMBINANT;

ANIMALS; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; DNA RESTRICTION ENZYMES; DNA, MITOCHONDRIAL; FEMALE; GENE EXPRESSION; GENETIC THERAPY; GENETIC VECTORS; MICE; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL MYOPATHIES; MUSCLE, STRIATED; TRANSDUCTION, GENETIC;

MUS; VASCONCELLEA CANDICANS;

EID: 84869089115     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2011.196     Document Type: Article

References (37)

1. Kyriakouli DS, Boesch P, Taylor RW, Lightowlers RN. Progress and prospects: gene therapy for mitochondrial DNA disease. Gene Therapy 2008; 15: 1017-1023. (Pubitemid 351927692)
2. Cwerman-Thibault H, Sahel JA, Corral-Debrinski M. Mitochondrial medicine: to a new era of gene therapy for mitochondrial DNA mutations. J Inherit Metab Dis 2011; 34: 327-344.
3. Thorburn DR, Dahl HH. Mitochondrial disorders: genetics, counseling, prenatal diagnosis and reproductive options. Am J Med Genet 2001; 106: 102-114.
4. DiMauro S, Schon EA. Mitochondrial respiratory-chain diseases. N Engl J Med 2003; 348: 2656-2668. (Pubitemid 36741594)
5. Srivastava S, Moraes CT. Manipulating mitochondrial DNA heteroplasmy by a mitochondrially targeted restriction endonuclease. Hum Mol Genet 2001; 10: 3093-3099. (Pubitemid 34083495)
6. Bayona-Bafaluy MP, Blits B, Battersby BJ, Shoubridge EA, Moraes CT. Rapid directional shift of mitochondrial DNA heteroplasmy in animal tissues by a mitochondrially targeted restriction endonuclease. Proc Natl Acad Sci USA 2005; 102: 14392-14397. (Pubitemid 41429708)
7. Tanaka M, Borgeld HJ, Zhang J, Muramatsu S, Gong JS, Yoneda M et al. Gene therapy for mitochondrial disease by delivering restriction endonuclease SmaI into mitochondria. J Biomed Sci 2002; 9: 534-541. (Pubitemid 35316865)
8. Alexeyev MF, Venediktova N, Pastukh V, Shokolenko I, Bonilla G, Wilson GL. Selective elimination of mutant mitochondrial genomes as therapeutic strategy for the treatment of NARP and MILS syndromes. Gene Therapy 2008; 15: 516-523. (Pubitemid 351405091)
9. Bacman SR, Williams SL, Hernandez D, Moraes CT. Modulating mtDNA heteroplasmy by mitochondria-targeted restriction endonucleases in a 'differential multiple cleavage-site' model. Gene Therapy 2007; 14: 1309-1318.
10. Bacman SR, Williams SL, Garcia S, Moraes CT. Organ-specific shifts in mtDNA heteroplasmy following systemic delivery of a mitochondria-targeted restriction endonuclease. Gene Therapy 2010; 17: 713-720.
11. Uusimaa J, Remes AM, Rantala H, Vainionpaa L, Herva R, Vuopala K et al. Childhood encephalopathies and myopathies: a prospective study in a defined population to assess the frequency of mitochondrial disorders. Pediatrics 2000; 105: 598-603. (Pubitemid 30129677)
12. Jenuth JP, Peterson AC, Shoubridge EA. Tissue-specific selection for different mtDNA genotypes in heteroplasmic mice. Nat Genet 1997; 16: 93-95. (Pubitemid 27198163)
13. Battersby BJ, Shoubridge EA. Selection of a mtDNA sequence variant in hepatocytes of heteroplasmic mice is not due to differences in respiratory chain function or efficiency of replication. Hum Mol Genet 2001; 10: 2469-2479. (Pubitemid 33094997)
14. Battersby BJ, Loredo-Osti JC, Shoubridge EA. Nuclear genetic control of mitochondrial DNA segregation. Nat Genet 2003; 33: 183-186. (Pubitemid 36177071)
15. Moreno-Loshuertos R, Acin-Perez R, Fernandez-Silva P, Movilla N, Perez-Martos A, Rodriguez de Cordoba S et al. Differences in reactive oxygen species production explain the phenotypes associated with common mouse mitochondrial DNA variants. Nat Genet 2006; 38: 1261-1268. (Pubitemid 44646288)
16. Inagaki K, Fuess S, Storm TA, Gibson GA, McTiernan CF, Kay MA et al. Robust systemic transduction with AAV9 vectors in mice: efficient global cardiac gene transfer superior to that of AAV8. Mol Ther 2006; 14: 45-53. (Pubitemid 43899488)
17. Ghosh A, Yue Y, Long C, Bostick B, Duan D. Efficient whole-body transduction with trans-splicing adeno-associated viral vectors. Mol Ther 2007; 15: 750-755. (Pubitemid 46431995)
18. Wenz T, Williams SL, Bacman SR, Moraes CT. Emerging therapeutic approaches to mitochondrial diseases. Dev Disabil Res Rev 2010; 16: 219-229.
19. Lightowlers RN, Chinnery PF, Turnbull DM, Howell N. Mammalian mitochondrial genetics: heredity, heteroplasmy and disease. Trends Genet 1997; 13: 450-455. (Pubitemid 27479904)
20. Chiaratti MR, Meirelles FV, Wells D, Poulton J. Therapeutic treatments of mtDNA diseases at the earliest stages of human development. Mitochondrion 2011; 11: 820-828.
21. Poulton J, Turnbull DM. 74th ENMC international workshop: mitochondrial diseases 19-20 November 1999, Naarden, The Netherlands. Neuromuscul Disord 2000; 10: 460-462. (Pubitemid 30433819)
22. Tsao CY, Mendell JR, Bartholomew D. High mitochondrial DNA T8993G mutation (o90%) without typical features of Leigh's and NARP syndromes. J Child Neurol 2001; 16: 533-535. (Pubitemid 32725393)
23. Pacak CA, Mah CS, Thattaliyath BD, Conlon TJ, Lewis MA, Cloutier DE et al. Recombinant adeno-associated virus serotype 9 leads to preferential cardiac transduction in vivo. Circ Res 2006; 99: e3-e9. (Pubitemid 44255502)
24. Zincarelli C, Soltys S, Rengo G, Rabinowitz JE. Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 2008; 16: 1073-1080. (Pubitemid 351737072)
25. Bostick B, Ghosh A, Yue Y, Long C, Duan D. Systemic AAV-9 transduction in mice is influenced by animal age but not by the route of administration. Gene Therapy 2007; 14: 1605-1609. (Pubitemid 350056232)
26. Foust KD, Nurre E, Montgomery CL, Hernandez A, Chan CM, Kaspar BK. Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 2009; 27: 59-65.
27. Ogura T, Mizukami H, Mimuro J, Madoiwa S, Okada T, Matsushita T et al. Utility of intraperitoneal administration as a route of AAV serotype 5 vector-mediated neonatal gene transfer. J Gene Med 2006; 8: 990-997. (Pubitemid 44282995)
28. Pruchnic R, Cao B, Peterson ZQ, Xiao X, Li J, Samulski RJ et al. The use of adenoassociated virus to circumvent the maturation-dependent viral transduction of muscle fibers. Hum Gene Ther 2000; 11: 521-536. (Pubitemid 30134296)
29. Blankinship MJ, Gregorevic P, Allen JM, Harper SQ, Harper H, Halbert CL et al. Efficient transduction of skeletal muscle using vectors based on adeno-associated virus serotype 6. Mol Ther 2004; 10: 671-678. (Pubitemid 39272856)
30. Lai Y, Yue Y, Liu M, Ghosh A, Engelhardt JF, Chamberlain JS et al. Efficient in vivo gene expression by trans-splicing adeno-associated viral vectors. Nat Biotechnol 2005; 23: 1435-1439. (Pubitemid 41679397)
31. Pettman R, Hurley T, Addis J, Robinson B, Scott H, Kronick JB. Prenatal diagnosis by amniocentesis and chorionic villus biopsy of mtDNA mutation 8993 T4G. J Inherit Metab Dis 2007; 30: 404.
32. Tatuch Y, Christodoulou J, Feigenbaum A, Clarke JT, Wherret J, Smith C et al. Heteroplasmic mtDNA mutation (T-G) at 8993 can cause Leigh disease when the percentage of abnormal mtDNA is high. Am J Hum Genet 1992; 50: 852-858.
33. Rossignol R, Faustin B, Rocher C, Malgat M, Mazat JP, Letellier T. Mitochondrial threshold effects. Biochem J 2003; 370: 751-762. (Pubitemid 36399067)
34. Minczuk M. Engineered zinc finger proteins for manipulation of the human mitochondrial genome. Methods Mol Biol 2010; 649: 257-270.
35. Handel EM, Cathomen T. Zinc-finger nuclease based genome surgery: it's all about specificity. Curr Gene Ther 2011; 11: 28-37.
36. Bacman SR, Williams SL, Moraes CT. Intra- and inter-molecular recombination of mitochondrial DNA after in vivo induction of multiple double-strand breaks. Nucleic Acids Res 2009; 37: 4218-4226.
37. Moraes CT, Ricci E, Bonilla E, DiMauro S, Schon EA. The mitochondrial tRNA(Leu(UUR)) mutation in mitochondrial encephalomyopathy, lactic acidosis, and strokelike episodes (MELAS): genetic, biochemical, and morphological correlations in skeletal muscle. Am J Hum Genet 1992; 50: 934-949.