The deafness gene DFNA5 induces programmed cell death through mitochondria and MAPK-related pathways

Frontiers in Cellular Neuroscience

Volumn 9, Issue JULY, 2015, Pages

  Van Rossom, Sofie ^a,b   de Beeck, Ken Op ^a   Hristovska, Vesna ^b   Winderickx, Joris ^b   Van Camp, Guy ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

DFNA5; Hearing loss; MAPK; Mitochondria; Oxidative stress; Programmed cell death

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; CYSTATHIONINE GAMMA LYASE; CYTOCHROME C OXIDASE; EARLY GROWTH RESPONSE FACTOR 1; GLUCOSE TRANSPORTER 4; HEAT SHOCK PROTEIN 70; MINICHROMOSOME MAINTENANCE PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE; MULTIENZYME COMPLEX; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; OLIGOSACCHARIDE; PHOSPHOGLYCERATE KINASE; PROTEIN BCL 2; PYRUVATE KINASE; RNA; TRANSCRIPTION FACTOR FOSB; TRANSCRIPTION FACTOR JUNB; TRIOSEPHOSPHATE ISOMERASE;

APOPTOSIS; ARTICLE; AUTOSOMAL DOMINANT DISORDER; CONTROLLED STUDY; DFNA5 GENE; DOWN REGULATION; ENERGY METABOLISM; GENE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC TRANSFORMATION; GLYCOLYSIS; HEARING IMPAIRMENT; HUMAN; HUMAN CELL; MAL12 GENE; MAL32 GENE; MICROARRAY ANALYSIS; MITOCHONDRION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PENTOSE PHOSPHATE CYCLE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SACCHAROMYCES CEREVISIAE; SUC2 GENE; TDH3 GENE; TUMOR SUPPRESSOR GENE; UPREGULATION; WESTERN BLOTTING;

EID: 84937425933     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00231     Document Type: Article

References (94)

1. Ahmed, Z. M., Yousaf, R., Lee, B. C., Khan, S. N., Lee, S., Lee, K., et al. (2011). Functional null mutations of MSRB3 encoding methionine sulfoxide reductase are associated with human deafness DFNB74. Am. J. Hum. Genet. 88, 19-29. doi: 10.1016/j.ajhg.2010.11.010
2. Akino, K., Toyota, M., Suzuki, H., Imai, T., Maruyama, R., Kusano, M., et al. (2007). Identification of DFNA5 as a target of epigenetic inactivation in gastric cancer. Cancer Sci. 98, 88-95. doi: 10.1111/j.1349-7006.2006.00351.x
3. Anastasiou, D., Poulogiannis, G., Asara, J. M., Boxer, M. B., Jiang, J. K., Shen, M., et al. (2011). Inhibition of pyruvate kinase M2 by reactive oxygen species contributes to cellular antioxidant responses. Science 334, 1278-1283. doi: 10.1126/science.1211485
4. Andrews, Z. B. (2010). Uncoupling protein-2 and the potential link between metabolism and longevity. Curr. Aging Sci. 3, 102-112. doi: 10.2174/1874609811003020102
5. Andrews, Z. B., and Horvath, T. L. (2009). Uncoupling protein-2 regulates lifespan in mice. Am. J. Physiol. Endocrinol. Metab. 296, E621-E627. doi: 10.1152/ajpendo.90903.2008
6. Antonicka, H., Leary, S. C., Guercin, G. H., Agar, J. N., Horvath, R., Kennaway, N. G., et al. (2003). Mutations in COX10 result in a defect in mitochondrial heme A biosynthesis and account for multiple, early-onset clinical phenotypes associated with isolated COX deficiency. Hum. Mol. Genet. 12, 2693-2702. doi: 10.1093/hmg/ddg284
7. Arnold, S., and Kadenbach, B. (1999). The intramitochondrial ATP/ADP-ratio controls cytochrome c oxidase activity allosterically. FEBS Lett. 443, 105-108. doi: 10.1016/S0014-5793(98)01694-9
8. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., et al. (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29. doi: 10.1038/75556
9. Basu Ball, W., Kar, S., Mukherjee, M., Chande, A. G., Mukhopadhyaya, R., and Das, P. K. (2011). Uncoupling protein 2 negatively regulates mitochondrial reactive oxygen species generation and induces phosphatase-mediated anti-inflammatory response in experimental visceral leishmaniasis. J. Immunol. 187, 1322-1332. doi: 10.4049/jimmunol.1004237
10. Bellezza, I., Roberti, R., Gatticchi, L., del Sordo, R., Rambotti, M. G., Marchetti, M. C., et al. (2013). A novel role for Tm7sf2 gene in regulating TNFalpha expression. PLoS ONE 8:e68017. doi: 10.1371/journal.pone.0068017
11. Bender, T., Leidhold, C., Ruppert, T., Franken, S., and Voos, W. (2010). The role of protein quality control in mitochondrial protein homeostasis under oxidative stress. Proteomics 10, 1426-1443. doi: 10.1002/pmic.200800619
12. Bender, T., Lewrenz, I., Franken, S., Baitzel, C., and Voos, W. (2011). Mitochondrial enzymes are protected from stress-induced aggregation by mitochondrial chaperones and the Pim1/LON protease. Mol. Biol. Cell 22, 541-554. doi: 10.1091/mbc.E10-08-0718
13. Bennati, A. M., Castelli, M., Della Fazia, M. A., Beccari, T., Caruso, D., Servillo, G., et al. (2006). Sterol dependent regulation of human TM7SF2 gene expression: role of the encoded 3beta-hydroxysterol Delta14-reductase in human cholesterol biosynthesis. Biochim. Biophys. Acta 1761, 677-685. doi: 10.1016/j.bbalip.2006.05.004
14. Bischoff, A. M., Luijendijk, M. W., Huygen, P. L., van Duijnhoven, G., De Leenheer, E. M., Oudesluijs, G. G., et al. (2004). A novel mutation identified in the DFNA5 gene in a Dutch family: a clinical and genetic evaluation. Audiol. Neurootol. 9, 34-46. doi: 10.1159/000074185
15. Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E., Li, J., Hieter, P., et al. (1998). Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132.
16. Buttner, S., Eisenberg, T., Carmona-Gutierrez, D., Ruli, D., Knauer, H., Ruckenstuhl, C., et al. (2007). Endonuclease G regulates budding yeast life and death. Mol. Cell 25, 233-246. doi: 10.1016/j.molcel.2006.12.021
17. Casano, R. A., Johnson, D. F., Bykhovskaya, Y., Torricelli, F., Bigozzi, M., and Fischel-Ghodsian, N. (1999). Inherited susceptibility to aminoglycoside ototoxicity: genetic heterogeneity and clinical implications. Am. J. Otolaryngol. 20, 151-156. doi: 10.1016/S0196-0709(99)90062-5
18. Chambers, J. W., and Lograsso, P. V. (2011). Mitochondrial c-Jun N-terminal kinase (JNK) signaling initiates physiological changes resulting in amplification of reactive oxygen species generation. J. Biol. Chem. 286, 16052-16062. doi: 10.1074/jbc.M111.223602
19. Chen, F. Q., Zheng, H. W., Hill, K., and Sha, S. H. (2012). Traumatic noise activates Rho-family GTPases through transient cellular energy depletion. J. Neurosci. 32, 12421-12430. doi: 10.1523/JNEUROSCI.6381-11.2012
20. Cheng, J., Han, D. Y., Dai, P., Sun, H. J., Tao, R., Sun, Q., et al. (2007). A novel DFNA5 mutation, IVS8+4 A>G, in the splice donor site of intron 8 causes late-onset non-syndromic hearing loss in a Chinese family. Clin. Genet. 72, 471-477. doi: 10.1111/j.1399-0004.2007.00889.x
21. Cheng, J., Zhu, Y., He, S., Lu, Y., Chen, J., Han, B., et al. (2011). Functional mutation of SMAC/DIABLO, encoding a mitochondrial proapoptotic protein, causes human progressive hearing loss DFNA64. Am. J. Hum. Genet. 89, 56-66. doi: 10.1016/j.ajhg.2011.05.027
22. Christofk, H. R., Vander Heiden, M. G., Harris, M. H., Ramanathan, A., Gerszten, R. E., Wei, R., et al. (2008). The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452, 230-233. doi: 10.1038/nature06734
23. Dando, I., Fiorini, C., Pozza, E. D., Padroni, C., Costanzo, C., Palmieri, M., et al. (2013). UCP2 inhibition triggers ROS-dependent nuclear translocation of GAPDH and autophagic cell death in pancreatic adenocarcinoma cells. Biochim. Biophys. Acta 1833, 672-679. doi: 10.1016/j.bbamcr.2012.10.028
24. Davies, K. J. (2001). Degradation of oxidized proteins by the 20S proteasome. Biochimie 83, 301-310. doi: 10.1016/S0300-9084(01)01250-0
25. De Brito, O. M., and Scorrano, L. (2010). An intimate liaison: spatial organization of the endoplasmic reticulum-mitochondria relationship. EMBO J. 29, 2715-2723. doi: 10.1038/emboj.2010.177
26. Deng, S., Yang, Y., Han, Y., Li, X., Wang, X., Li, X., et al. (2012). UCP2 inhibits ROS-mediated apoptosis in A549 under hypoxic conditions. PLoS ONE 7:e30714. doi: 10.1371/journal.pone.0030714
27. Ding, Y., Leng, J., Fan, F., Xia, B., and Xu, P. (2013). The role of mitochondrial DNA mutations in hearing loss. Biochem. Genet. 51, 588-602. doi: 10.1007/s10528-013-9589-6
28. Dowlati, M. A., Derakhshandeh-Peykar, P., Houshmand, M., Farhadi, M., Shojaei, A., Fallah, M., et al. (2013). Novel nucleotide changes in mutational analysis of mitochondrial 12SrRNA gene in patients with nonsyndromic and aminoglycoside-induced hearing loss. Mol. Biol. Rep. 40, 2689-2695. doi: 10.1007/s11033-012-2355-8
29. Dunning, M. J., Smith, M. L., Ritchie, M. E., and Tavare, S. (2007). beadarray: R classes and methods for Illumina bead-based data. Bioinformatics 23, 2183-2184. doi: 10.1093/bioinformatics/btm311
30. Emre, Y., Hurtaud, C., Nubel, T., Criscuolo, F., Ricquier, D., and Cassard-Doulcier, A. M. (2007). Mitochondria contribute to LPS-induced MAPK activation via uncoupling protein UCP2 in macrophages. Biochem. J. 402, 271-278. doi: 10.1042/BJ20061430
31. Estivill, X., Govea, N., Barcelo, E., Badenas, C., Romero, E., Moral, L., et al. (1998). Familial progressive sensorineural deafness is mainly due to the mtDNA A1555G mutation and is enhanced by treatment of aminoglycosides. Am. J. Hum. Genet. 62, 27-35. doi: 10.1086/301676
32. Fekete, D. M., Homburger, S. A., Waring, M. T., Riedl, A. E., and Garcia, L. F. (1997). Involvement of programmed cell death in morphogenesis of the vertebrate inner ear. Development 124, 2451-2461.
33. Fischel-Ghodsian, N. (1999). Genetic factors in aminoglycoside toxicity. Ann. N.Y. Acad. Sci. 884, 99-109. doi: 10.1111/j.1749-6632.1999.tb08639.x
34. Foury, F. (1997). Human genetic diseases: a cross-talk between man and yeast. Gene 195, 1-10. doi: 10.1016/S0378-1119(97)00140-6
35. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., et al. (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5:R80. doi: 10.1186/gb-2004-5-10-r80
36. Gietz, D., St Jean, A., Woods, R. A., and Schiestl, R. H. (1992). Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20:1425. doi: 10.1093/nar/20.6.1425
37. Gredilla, R., and Barja, G. (2005). Minireview: the role of oxidative stress in relation to caloric restriction and longevity. Endocrinology 146, 3713-3717. doi: 10.1210/en.2005-0378
38. Gredilla, R., Bohr, V. A., and Stevnsner, T. (2010). Mitochondrial DNA repair and association with aging—An update. Exp. Gerontol. 45, 478-488. doi: 10.1016/j.exger.2010.01.017
39. Gregan, J., Van Laer, L., Lieto, L. D., Van Camp, G., and Kearsey, S. E. (2003). A yeast model for the study of human DFNA5, a gene mutated in nonsyndromic hearing impairment. Biochim. Biophys. Acta 1638, 179-186. doi: 10.1016/S0925-4439(03)00083-8
40. Gruning, N. M., Du, D., Keller, M. A., Luisi, B. F., and Ralser, M. (2014). Inhibition of triosephosphate isomerase by phosphoenolpyruvate in the feedback-regulation of glycolysis. Open Biol. 4:130232. doi: 10.1098/rsob.130232
41. Gruning, N. M., Rinnerthaler, M., Bluemlein, K., Mulleder, M., Wamelink, M. M., Lehrach, H., et al. (2011). Pyruvate kinase triggers a metabolic feedback loop that controls redox metabolism in respiring cells. Cell Metab. 14, 415-427. doi: 10.1016/j.cmet.2011.06.017
42. Hochberg, Y., and Benjamini, Y. (1990). More powerful procedures for multiple significance testing. Stat. Med. 9, 811-818. doi: 10.1002/sim.4780090710
43. Holmer, L., Pezhman, A., and Worman, H. J. (1998). The human lamin B receptor/sterol reductase multigene family. Genomics 54, 469-476. doi: 10.1006/geno.1998.5615
44. Jacobs, H. T., Hutchin, T. P., Kappi, T., Gillies, G., Minkkinen, K., Walker, J., et al. (2005). Mitochondrial DNA mutations in patients with postlingual, nonsyndromic hearing impairment. Eur. J. Hum. Genet. 13, 26-33. doi: 10.1038/sj.ejhg.5201250
45. Jin, L., Yang, A., Zhu, Y., Zhao, J., Wang, X., Yang, L., et al. (2007). Mitochondrial tRNASer(UCN) gene is the hot spot for mutations associated with aminoglycoside-induced and non-syndromic hearing loss. Biochem. Biophys. Res. Commun. 361, 133-139. doi: 10.1016/j.bbrc.2007.06.171
46. Kalinec, G. M., Thein, P., Parsa, A., Yorgason, J., Luxford, W., Urrutia, R., et al. (2014). Acetaminophen and NAPQI are toxic to auditory cells via oxidative and endoplasmic reticulum stress-dependent pathways. Hear. Res. 313, 26-37. doi: 10.1016/j.heares.2014.04.007
47. Kim, M. S., Chang, X., Yamashita, K., Nagpal, J. K., Baek, J. H., Wu, G., et al. (2008a). Aberrant promoter methylation and tumor suppressive activity of the DFNA5 gene in colorectal carcinoma. Oncogene 27, 3624-3634. doi: 10.1038/sj.onc.1211021
48. Kim, M. S., Lebron, C., Nagpal, J. K., Chae, Y. K., Chang, X., Huang, Y., et al. (2008b). Methylation of the DFNA5 increases risk of lymph node metastasis in human breast cancer. Biochem. Biophys. Res. Commun. 370, 38-43. doi: 10.1016/j.bbrc.2008.03.026
49. Kruger, A., Gruning, N. M., Wamelink, M. M., Kerick, M., Kirpy, A., Parkhomchuk, D., et al. (2011). The pentose phosphate pathway is a metabolic redox sensor and regulates transcription during the antioxidant response. Antioxid. Redox Signal. 15, 311-324. doi: 10.1089/ars.2010.3797
50. Leon, Y., Sanchez-Galiano, S., and Gorospe, I. (2004). Programmed cell death in the development of the vertebrate inner ear. Apoptosis 9, 255-264. doi: 10.1023/B:APPT.0000025802.07676.a5
51. Liu, Y. M., Li, X. D., Guo, X., Liu, B., Lin, A. H., Ding, Y. L., et al. (2010). SOD2 V16A SNP in the mitochondrial targeting sequence is associated with noise induced hearing loss in Chinese workers. Dis. Markers 28, 137-147. doi: 10.1155/2010/753073
52. Lo, B., Li, L., Gissen, P., Christensen, H., Mckiernan, P. J., Ye, C., et al. (2005). Requirement of VPS33B, a member of the Sec1/Munc18 protein family, in megakaryocyte and platelet alpha-granule biogenesis. Blood 106, 4159-4166. doi: 10.1182/blood-2005-04-1356
53. Luo, L. F., Hou, C. C., and Yang, W. X. (2013). Nuclear factors: roles related to mitochondrial deafness. Gene 520, 79-89. doi: 10.1016/j.gene.2013.03.041
54. Madeo, F., Carmona-Gutierrez, D., Ring, J., Büttner, S., Eisenberg, T., and Kroemer, G. (2009). Caspase-dependent and caspase-independent cell death pathways in yeast. Biochem. Biophys. Res. Commun. 382, 227-231. doi: 10.1016/j.bbrc.2009.02.117
55. Marchi, S., Patergnani, S., and Pinton, P. (2014). The endoplasmic reticulum-mitochondria connection: one touch, multiple functions. Biochim. Biophys. Acta 1837, 461-469. doi: 10.1016/j.bbabio.2013.10.015
56. Maynard, S., Schurman, S. H., Harboe, C., de Souza-Pinto, N. C., and Bohr, V. A. (2009). Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis 30, 2-10. doi: 10.1093/carcin/bgn250
57. Meyer Zum Gottesberge, A. M., Massing, T., and Hansen, S. (2012). Missing mitochondrial Mpv17 gene function induces tissue-specific cell-death pathway in the degenerating inner ear. Cell Tissue Res. 347, 343-356. doi: 10.1007/s00441-012-1326-7
58. Mollet, J., Giurgea, I., Schlemmer, D., Dallner, G., Chretien, D., Delahodde, A., et al. (2007). Prenyldiphosphate synthase, subunit 1 (PDSS1) and OH-benzoate polyprenyltransferase (COQ2) mutations in ubiquinone deficiency and oxidative phosphorylation disorders. J. Clin. Invest. 117, 765-772. doi: 10.1172/JCI29089
59. Moran, J. V., Wernette, C. M., Mecklenburg, K. L., Butow, R. A., and Perlman, P. S. (1992). Intron 5 alpha of the COXI gene of yeast mitochondrial DNA is a mobile group I intron. Nucleic Acids Res. 20, 4069-4076. doi: 10.1093/nar/20.15.4069
60. Napiwotzki, J., and Kadenbach, B. (1998). Extramitochondrial ATP/ADP-ratios regulate cytochrome c oxidase activity via binding to the cytosolic domain of subunit IV. Biol. Chem. 379, 335-339. doi: 10.1515/bchm.1998.379.3.335
61. Nishikori, T., Hatta, T., Kawauchi, H., and Otani, H. (1999). Apoptosis during inner ear development in human and mouse embryos: an analysis by computer-assisted three-dimensional reconstruction. Anat. Embryol. 200, 19-26. doi: 10.1007/s004290050255
62. Nishio, A., Noguchi, Y., Sato, T., Naruse, T. K., Kimura, A., Takagi, A., et al. (2014). A DFNA5 mutation identified in Japanese families with autosomal dominant hereditary hearing loss. Ann. Hum. Genet. 78, 83-91. doi: 10.1111/ahg.12053
63. Op de Beeck, K., Van Camp, G., Thys, S., Cools, N., Callebaut, I., Vrijens, K., et al. (2011). The DFNA5 gene, responsible for hearing loss and involved in cancer, encodes a novel apoptosis-inducing protein. Eur. J. Hum. Genet. 19, 965-973. doi: 10.1038/ejhg.2011.63
64. Park, H. J., Cho, H. J., Baek, J. I., Ben-Yosef, T., Kwon, T. J., Griffith, A. J., et al. (2010). Evidence for a founder mutation causing DFNA5 hearing loss in East Asians. J. Hum. Genet. 55, 59-62. doi: 10.1038/jhg.2009.114
65. Payne, M., Yang, Z., Katz, B. J., Warner, J. E., Weight, C. J., Zhao, Y., et al. (2004). Dominant optic atrophy, sensorineural hearing loss, ptosis, and ophthalmoplegia: a syndrome caused by a missense mutation in OPA1. Am. J. Ophthalmol. 138, 749-755. doi: 10.1016/j.ajo.2004.06.011
66. Pevsner, J., Hsu, S. C., Hyde, P. S., and Scheller, R. H. (1996). Mammalian homologues of yeast vacuolar protein sorting (vps) genes implicated in Golgi-to-lysosome trafficking. Gene 183, 7-14. doi: 10.1016/S0378-1119(96)00367-8
67. Raha, S., and Robinson, B. H. (2000). Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem. Sci. 25, 502-508. doi: 10.1016/S0968-0004(00)01674-1
68. Ralser, M., Wamelink, M. M., Kowald, A., Gerisch, B., Heeren, G., Struys, E. A., et al. (2007). Dynamic rerouting of the carbohydrate flux is key to counteracting oxidative stress. J. Biol. 6, 10. doi: 10.1186/jbiol61
69. Roesch, K., Curran, S. P., Tranebjaerg, L., and Koehler, C. M. (2002). Human deafness dystonia syndrome is caused by a defect in assembly of the DDP1/TIMM8a-TIMM13 complex. Hum. Mol. Genet. 11, 477-486. doi: 10.1093/hmg/11.5.477
70. Sauner, M. T., and Levy, M. (1971). Study of the transfer of phospholipids from the endoplasmic reticulum to the outer and inner mitochondrial membranes. J. Lipid Res. 12, 71-75.
71. Schiavoni, G., Bennati, A. M., Castelli, M., Fazia, M. A., Beccari, T., Servillo, G., et al. (2010). Activation of TM7SF2 promoter by SREBP-2 depends on a new sterol regulatory element, a GC-box, and an inverted CCAAT-box. Biochim. Biophys. Acta 1801, 587-592. doi: 10.1016/j.bbalip.2010.01.013
72. Schroder, M. (2008). Endoplasmic reticulum stress responses. Cell. Mol. Life Sci. 65, 862-894. doi: 10.1007/s00018-007-7383-5
73. Selimovic, D., Hassan, M., Haikel, Y., and Hengge, U. R. (2008). Taxol-induced mitochondrial stress in melanoma cells is mediated by activation of c-Jun N-terminal kinase (JNK) and p38 pathways via uncoupling protein 2. Cell. Signal. 20, 311-322. doi: 10.1016/j.cellsig.2007.10.015
74. Seraphin, B., Faye, G., Hatat, D., and Jacq, C. (1992). The yeast mitochondrial intron aI5 alpha: associated endonuclease activity and in vivo mobility. Gene 113, 1-8. doi: 10.1016/0378-1119(92)90663-A
75. Sha, S. H., Chen, F. Q., and Schacht, J. (2009). Activation of cell death pathways in the inner ear of the aging CBA/J mouse. Hear. Res. 254, 92-99. doi: 10.1016/j.heares.2009.04.019
76. Sha, S. H., Taylor, R., Forge, A., and Schacht, J. (2001). Differential vulnerability of basal and apical hair cells is based on intrinsic susceptibility to free radicals. Hear. Res. 155, 1-8. doi: 10.1016/S0378-5955(01)00224-6
77. Shang, F., Nowell, T. R. Jr., and Taylor, A. (2001). Removal of oxidatively damaged proteins from lens cells by the ubiquitin-proteasome pathway. Exp. Eye Res. 73, 229-238. doi: 10.1006/exer.2001.1029
78. Shang, F., and Taylor, A. (2011). Ubiquitin-proteasome pathway and cellular responses to oxidative stress. Free Radic. Biol. Med. 51, 5-16. doi: 10.1016/j.freeradbiomed.2011.03.031
79. Singh, S., Misiak, M., Beyer, C., and Arnold, S. (2009). Cytochrome c oxidase isoform IV-2 is involved in 3-nitropropionic acid-induced toxicity in striatal astrocytes. Glia 57, 1480-1491. doi: 10.1002/glia.20864
80. Smyth, G. K. (2004). Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3:3. doi: 10.2202/1544-6115.1027
81. Someya, S., Xu, J., Kondo, K., Ding, D., Salvi, R. J., Yamasoba, T., et al. (2009). Age-related hearing loss in C57BL/6J mice is mediated by Bak-dependent mitochondrial apoptosis. Proc. Natl. Acad. Sci. U.S.A. 106, 19432-19437. doi: 10.1073/pnas.0908786106
82. Srinivasan, S., and Avadhani, N. G. (2012). Cytochrome c oxidase dysfunction in oxidative stress. Free Radic. Biol. Med. 53, 1252-1263. doi: 10.1016/j.freeradbiomed.2012.07.021
83. Stiban, J., Caputo, L., and Colombini, M. (2008). Ceramide synthesis in the endoplasmic reticulum can permeabilize mitochondria to proapoptotic proteins. J. Lipid Res. 49, 625-634. doi: 10.1194/jlr.M700480-JLR200
84. Tavazoie, S., Hughes, J. D., Campbell, M. J., Cho, R. J., and Church, G. M. (1999). Systematic determination of genetic network architecture. Nat. Genet. 22, 281-285. doi: 10.1038/10343
85. Van Laer, L., Huizing, E. H., Verstreken, M., van Zuijlen, D., Wauters, J. G., Bossuyt, P. J., et al. (1998). Nonsyndromic hearing impairment is associated with a mutation in DFNA5. Nat. Genet. 20, 194-197. doi: 10.1038/2503
86. Van Rossom, S., Op de Beeck, K., Franssens, V., Swinnen, E., Schepers, A., Ghillebert, R., et al. (2012). The splicing mutant of the human tumor suppressor protein DFNA5 induces programmed cell death when expressed in the yeast Saccharomyces cerevisiae. Front. Oncol. 2:77. doi: 10.3389/fonc.2012.00077
87. Walsh, T., Pierce, S. B., Lenz, D. R., Brownstein, Z., Dagan-Rosenfeld, O., Shahin, H., et al. (2010). Genomic duplication and overexpression of TJP2/ZO-2 leads to altered expression of apoptosis genes in progressive nonsyndromic hearing loss DFNA51. Am. J. Hum. Genet. 87, 101-109. doi: 10.1016/j.ajhg.2010.05.011
88. Wang, C. J., Tang, L., Shen, D. W., Wang, C., Yuan, Q. Y., Gao, W., et al. (2013). The expression and regulation of DFNA5 in human hepatocellular carcinoma DFNA5 in hepatocellular carcinoma. Mol. Biol. Rep. 40, 6525-6531. doi: 10.1007/s11033-013-2581-8
89. Westermann, B., and Neupert, W. (2000). Mitochondria-targeted green fluorescent proteins: convenient tools for the study of organelle biogenesis in Saccharomyces cerevisiae. Yeast 16, 1421-1427. doi: 10.1002/1097-0061(200011)16:15<1421::AID-YEA624>3.0.CO;2-U
90. Wiel, C., Lallet-Daher, H., Gitenay, D., Gras, B., Le Calve, B., Augert, A., et al. (2014). Endoplasmic reticulum calcium release through ITPR2 channels leads to mitochondrial calcium accumulation and senescence. Nat. Commun. 5, 3792. doi: 10.1038/ncomms4792
91. Winderickx, J., Delay, C., De Vos, A., Klinger, H., Pellens, K., Vanhelmont, T., et al. (2008). Protein folding diseases and neurodegeneration: lessons learned from yeast. Biochim. Biophys. Acta 1783, 1381-1395. doi: 10.1016/j.bbamcr.2008.01.020
92. Wissing, S., Ludovico, P., Herker, E., Buttner, S., Engelhardt, S. M., Decker, T., et al. (2004). An AIF orthologue regulates apoptosis in yeast. J. Cell Biol. 166, 969-974. doi: 10.1083/jcb.200404138
93. Yu, C., Meng, X., Zhang, S., Zhao, G., Hu, L., and Kong, X. (2003). A 3-nucleotide deletion in the polypyrimidine tract of intron 7 of the DFNA5 gene causes nonsyndromic hearing impairment in a Chinese family. Genomics 82, 575-579. doi: 10.1016/S0888-7543(03)00175-7
94. Zecchini, E., Siviero, R., Giorgi, C., Rizzuto, R., and Pinton, P. (2007). Mitochondrial calcium signalling: message of life and death. Ital. J. Biochem. 56, 235-242