Methionine Sulfoxide Reductase B3-Targeted in Utero Gene Therapy Rescues Hearing Function in a Mouse Model of Congenital Sensorineural Hearing Loss

Antioxidants and Redox Signaling

Volumn 24, Issue 11, 2016, Pages 590-602

  Kim, Min A ^a   Cho, Hyun Ju ^a   Bae, Seung Hyun ^a   Lee, Byeonghyeon ^a   Oh, Se Kyung ^a,b   Kwon, Tae Jun ^c   Ryoo, Zae Young ^a   Kim, Hwa Young ^d   Cho, Jin Ho ^a   Kim, Un Kyung ^a   Lee, Kyu Yup ^e  

^a Kyungpook National University   (South Korea)

^b Korea Polar Research Institute (KOPRI)   (South Korea)

^c New Drug Development Center   (South Korea)

^d Yeungnam University College of Medicine   (South Korea)

^e Kyungpook National University School of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; METHIONINE SULFOXIDE REDUCTASE B3; RECOMBINANT ENZYME; UNCLASSIFIED DRUG; METHIONINE SULFOXIDE REDUCTASE; METHIONINE SULFOXIDE REDUCTASE B3, MOUSE;

ADENO ASSOCIATED VIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ULTRASTRUCTURE; COCHLEAR HAIR CELL; CORTI ORGAN; HEARING; INNER EAR; MOUSE; NONHUMAN; PERCEPTION DEAFNESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRAL GENE THERAPY; ANIMAL; DEFICIENCY; DISEASE MODEL; FEMALE; GENE THERAPY; GENETICS; HEARING LOSS, SENSORINEURAL; KNOCKOUT MOUSE; METABOLISM; UTERUS;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; GENETIC THERAPY; HEARING LOSS, SENSORINEURAL; METHIONINE SULFOXIDE REDUCTASES; MICE; MICE, KNOCKOUT; UTERUS;

EID: 84964818142     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2015.6442     Document Type: Article

References (54)

1. Ahmed ZM, Yousaf R, Lee BC, Khan SN, Lee S, Lee K, Husnain T, Rehman AU, Bonneux S, Ansar M, Ahmad W, Leal SM, Gladyshev VN, Belyantseva IA, Van Camp G, Riazuddin S, Friedman TB, and Riazuddin S. Functional null mutations of MSRB3 encoding methionine sulfoxide reductase are associated with human deafness DFNB74. Am J Hum Genet 88: 19-29, 2011.
2. Akil O, Seal RP, Burke K, Wang C, Alemi A, During M, Edwards RH, and Lustig LR. Restoration of hearing in the VGLUT3 knockout mouse using virally mediated gene therapy. Neuron 75: 283-293, 2012.
3. Atkinson PJ, Wise AK, Flynn BO, Nayagam BA, and Richardson RT. Hair cell regeneration after ATOH1 gene therapy in the cochlea of profoundly deaf adult guinea pigs. PLoS One 9: el02077, 2014.
4. Bedrosian JC, Gratton MA, Brigande JV, Tang W, Landau J, and Bennett J. In vivo delivery of recombinant viruses to the fetal murine cochlea: transduction characteristics and long-term effects on auditory function. Mol Ther 14: 328-335, 2006.
5. Berlett BS and Stadtman ER. Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272: 20313-20316, 1997.
6. Cao G, Lee KP, van der Wij st J, de Graaf M, van der Kemp A, Bindels RJ, and Hoenderop JG. Methionine sulfoxide reductase Bl (MsrBl) recovers TRPM6 channel activity during oxidative stress. J Biol Chem 285: 26081-26087, 2010.
7. Ciorba MA, Heinemann SH, Weissbach H, Brot N, and Hoshi T. Modulation of potassium channel function by methionine oxidation and reduction. Proc Natl Acad Sci USA94: 9932-9937, 1997.
8. Gabbita SP, Aksenov MY, Lovell MA, and Markesbery WR. Decrease in peptide methionine sulfoxide reductase in Alz-heimer's disease brain. JNeurochem 73: 1660-1666, 1999.
9. Gillespie LN, Richardson RT, Nayagam BA, and Wise AK. Treating hearing disorders with cell and gene therapy. J Neural Eng 11: 065001, 2014.
10. Groves AK. The challenge of hair cell regeneration. Exp Biol Med (Maywood) 235: 434-446, 2010.
11. Heffer LF, Sly DJ, Fallon JB, White MW, Shepherd RK, and O'Leary SJ. Examining the auditory nerve fiber response to high rate cochlear implant stimulation: chronic sensorineural hearing loss and facilitation. J Neurophysiol 104: 3124-3135, 2010.
12. Henderson LB, Doshi VK, Blackman SM, Naughton KM, Pace RG, Moskovitz J, Knowles MR, Durie PR, Dramm ML, and Cutting GR. Variation in MSRA modifies risk of neonatal intestinal obstruction in cystic fibrosis. PLoS Genet 8: el002580, 2012.
13. Hildebrand MS, Newton SS, Gubbels SP, Sheffield AM, Kochhar A, de Silva MG, Dahl HH, Rose SD, Behlke MA, and Smith RJ. Advances in molecular and cellular therapies for hearing loss. Mol Ther 16: 224-236, 2007.
14. Hoshi T and Heinemann S. Regulation of cell function by methionine oxidation and reduction. J Physiol 531:1-11, 2001.
15. Hung RJ, Pak CW, and Terman JR. Direct redox regulation of F-actin assembly and disassembly by Mical. Science 334: 1710-1713, 2011.
16. Hung RJ, Yazdani U, Yoon J, Wu H, Yang T, Gupta N, Huang Z, van Berkel WJ, and Terman JR. Mical links semaphorins to F-actin disassembly. Nature 463: 823-827, 2010.
17. Hunter-Duvar IM. A technique for preparation of cochlear specimens for assessment with the scanning electron microscope. Acta Otolaryngol Suppl 351: 3-23, 1978.
18. Imlay JA. Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77: 755-776, 2008.
19. Jecmenica J, Bajec-Opancina A, and Jecmenica D. Genetic hearing impairment. Childs Nerv Syst 31: 515-519, 2015.
20. Jero J, Mhatre AN, Tseng CJ, Stern RE, Coling DE, Goldstein JA, Hong K, Zheng WW, Hoque AT, and Lalwani AK. Cochlear gene delivery through an intact round window membrane in mouse. Hum Gene Ther 12: 539-548, 2001.
21. Konishi M, Kawamoto K, Izumikawa M, Kuriyama H, and Yamashita T. Gene transfer into guinea pig cochlea using adeno-associated virus vectors. J Gene Med 10:610-618, 2008.
22. Krause KH. Aging: a revisited theory based on free radicals generated by NOX family NADPH oxidases. Exp Gerontol 42: 256-262, 2007.
23. Kryukov GV, Kumar RA, Koc A, Sun Z, and Gladyshev VN. Selenoprotein R is a zinc-containing stereo-specific methionine sulfoxide reductase. Proc Natl Acad Sci USA 99: 4245-4250, 2002.
24. Kwon TJ, Cho HJ, Kim UK, Lee E, Oh SK, Bok J, Bae YC, Yi JK, Lee JW, Ryoo ZY, Lee SH, Lee KY, and Kim HY. Methionine sulfoxide reductase B3 deficiency causes hearing loss due to stereocilia degeneration and apoptotic cell death in cochlear hair cells. Hum Mol Genet 23: 1591-1601, 2014.
25. Lee BC, Dikiy A, Kim HY, and Gladyshev VN. Functions and evolution of selenoprotein methionine sulfoxide reductases. Biochim Biophys Acta 1790: 1471-1477, 2009.
26. Lee BC, Peterfi Z, Hoffmann FW, Moore RE, Kaya A, Avanesov A, Tarrago L, Zhou Y, Weerapana E, Fomenko DE, Hoffmann PR, and Gladyshev VN. MsrBl and MI-CALs regulate actin assembly and macrophage function via reversible stereoselective methionine oxidation. Mol Cell 51: 397-404, 2013.
27. Lee HJ, Jung J, Shin JW, Song MH, Kim SH, Lee JH, Lee KA, Shin S, Kim UK, Bok J, Lee KY, Choi JY, and Park HJ. Correlation between genotype and phenotype in patients with bi-allelic SLC26A4 mutations. Clin Genet 86: 270-275, 2014.
28. Lee HJ, Yoo SJ, Lee S, Song HJ, Huh MI, Jin SU, Lee KY, Lee J, Cho JH, and Chang Y. Functional activity mapping of rat auditory pathway after intratympanic manganese administration. Neuroimage 60: 1046-1054, 2012.
29. Minoda R, Miwa T, Ise M, and Takeda H. Potential treatments for genetic hearing loss in humans: current conundrums. Gene Ther 22: 603-609, 2015.
30. Miwa T, Minoda R, Ise M, Yamada T, and Yumoto E. Mouse otocyst transuterine gene transfer restores hearing in mice with connexin 30 deletion-associated hearing loss. Mol Ther 21: 1142-1150, 2013.
31. Moskovitz J. Methionine sulfoxide reductases: ubiquitous enzymes involved in antioxidant defense, protein regulation, and prevention of aging-associated diseases. Biochim Biophys Acta 1703: 213-219, 2005.
32. Moskovitz J, Berlett BS, Poston JM, and Stadtman ER. The yeast peptide-methionine sulfoxide reductase functions as an antioxidant in vivo. Proc Natl Acad Sci USA 94: 9585-9589, 1997.
33. Moskovitz J, Rahman MA, Strassman J, Yancey SO, Kushner SR, Brot N, and Weissbach H. Escherichia coli peptide methionine sulfoxide reductase gene: regulation of expression and role in protecting against oxidative damage. J Bacteriol 177: 502-507, 1995.
34. Oien DB, Ortiz AN, Rittel AG, Dobrowsky RT, Johnson MA, Levant B, Fowler SC, and Moskovitz J. Dopamine D(2) receptor function is compromised in the brain of the methionine sulfoxide reductase A knockout mouse. J Neurochem 114: 51-61, 2010.
35. Oien DB, Osterhaus GL, Latif SA, Pinkston JW, Fulks J, Johnson M, Fowler SC, and Moskovitz J. MsrA knockout mouse exhibits abnormal behavior and brain dopamine levels. Free Radic Biol Med 45: 193-200, 2008.
36. Pal R, Oien DB, Ersen FY, and Moskovitz J. Elevated levels of brain-pathologies associated with neurodegenerative diseases in the methionine sulfoxide reductase A knockout mouse. Exp Brain Res 180: 765-774, 2007.
37. Pang JJ, Boye SL, Kumar A, Dinculescu A, Deng W, Li J, Li Q, Rani A, Foster TC, Chang B, Hawes NL, Boatright JH, and Hauswirth WW. AAV-mediated gene therapy for retinal degeneration in the rdlO mouse containing a recessive PDEbeta mutation. Invest Ophthalmol Vis Sci 49: 4278-4283, 2008.
38. Patuzzi RB, Yates GK, and Johnstone BM. Outer hair cell receptor current and sensorineural hearing loss. Hear Res 42: 47-72, 1989.
39. Rivolta MN. New strategies for the restoration of hearing loss: challenges and opportunities. Br Med Bull 105: 69-84, 2012.
40. Rodrigo MJ, Moskovitz J, Salamini F, and Bartels D. Reverse genetic approaches in plants and yeast suggest a role for novel, evolutionarily conserved, selenoprotein-related genes in oxidative stress defense. Mol Genet Genomics 267: 613-621, 2002.
41. Santarelli LC, Wassef R, Heinemann SH, and Hoshi T. Three methionine residues located within the regulator of conductance for K+ (RCK) domains confer oxidative sensitivity to large-conductance Ca2+-activated K+ channels. J Physiol 571: 329-348, 2006.
42. Shepherd RK and Hardie NA. Deafness-induced changes in the auditory pathway: implications for cochlear implants. Audiol Neurootol 6: 305-318, 2001.
43. Singh VK and Moskovitz J. Multiple methionine sulfoxide reductase genes in Staphylococcus aureus: expression of activity and roles in tolerance of oxidative stress. Microbiology 149: 2739-2747, 2003.
44. Sinha K, Das J, Pal PB, and Sil PC. Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch Toxicol 87: 1157-1180, 2013.
45. Skaar EP, Tobiason DM, Quick J, Judd RC, Weissbach H, Etienne F, Brot N, and Seifert HS. The outer membrane localization of the Neisseria gonorrhoeae MsrA/B is involved in survival against reactive oxygen species. Proc Natl Acad Sci USA 99: 10108-10113, 2002.
46. Stadtman ER. Protein oxidation and aging. Free Radic Res 40: 1250-1258, 2006.
47. Stadtman ER and Levine RL. Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 25: 207-218, 2003.
48. Stadtman ER, Moskovitz J, Berlett BS, and Levine RL. Cyclic oxidation and reduction of protein methionine residues is an important antioxidant mechanism. Mol Cell Biochem 234-235: 3-9, 2002.
49. Stadtman ER, Moskovitz J, and Levine RL. Oxidation of methionine residues of proteins: biological consequences. Antioxid Redox Signal 5: 577-582, 2003.
50. Stone IM, Lurie DI, Kelley MW, and Poulsen DJ. Adeno-associated virus-mediated gene transfer to hair cells and support cells of the murine cochlea. Mol Ther 11: 843-848, 2005.
51. Stone JS, Oesterle EC, and Rubel EW. Recent insights into regeneration of auditory and vestibular hair cells. Curr Opin Neurol 11: 17-24, 1998.
52. Ugarte N, Petropoulos I, and Friguet B. Oxidized mitochondrial protein degradation and repair in aging and oxidative stress. Antioxid Redox Signal 13: 539-549, 2010.
53. Wilson C and Gonzalez-Billault C. Regulation of cyto-skeletal dynamics by redox signaling and oxidative stress: implications for neuronal development and trafficking. Front CellNeurosci 9: 381, 2015.
54. Yagi M, Kanzaki S, Kawamoto K, Shin B, Shah PP, Magal E, Sheng J, and Raphael Y. Spiral ganglion neurons are protected from degeneration by GDNF gene therapy. J Assoc Res Otolaryngol 1: 315-325, 2000.