4,531
Views
9
CrossRef citations to date
0
Altmetric
Research Paper

Increased mitophagy protects cochlear hair cells from aminoglycoside-induced damage

, , , , , , , , , , ORCID Icon, , , , , , , ORCID Icon & ORCID Icon show all
Pages 75-91 | Received 08 Jul 2021, Accepted 01 Apr 2022, Published online: 26 Apr 2022

References

  • Wong AC, Ryan AF. Mechanisms of sensorineural cell damage, death and survival in the cochlea. Front Aging Neurosci. 2015;7:58.
  • Guthrie OW. Aminoglycoside induced ototoxicity. Toxicology. 2008;249:91–96.
  • Tablan OC, Reyes MP, Rintelmann WF, et al Renal and auditory toxicity of high-dose, prolonged therapy with gentamicin and tobramycin in pseudomonas endocarditis. J Infect Dis. 1984;149:257–263.
  • Kros CJ, Steyger PS. Aminoglycoside- and cisplatin-induced ototoxicity: mechanisms and otoprotective strategies. Cold Spring Harb Perspect Med. 2019;9:a033548.
  • Scheibinger M, Ellwanger DC, Corrales CE, et al Aminoglycoside damage and hair cell regeneration in the chicken utricle. Jaro-J Assoc Res Oto. 2018;19:17–29.
  • He Z, Sun S, Waqas M, et al Reduced TRMU expression increases the sensitivity of hair-cell-like HEI-OC-1 cells to neomycin damage in vitro. Sci Rep. 2016;6:29621.
  • Dunn JD, Alvarez LAJ, Zhang XZ, et al Reactive oxygen species and mitochondria: a nexus of cellular homeostasis. Redox Biol. 2015;6:472–485.
  • Lemasters JJ. Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res. 2005;8(1):3–5.
  • Goiran T, Duplan E, Rouland L, et al Nuclear p53-mediated repression of autophagy involves PINK1 transcriptional down-regulation. Cell Death Differ. 2018;25:873–884.
  • Narendra D, Tanaka A, Suen DF, et al. Parkin-induced mitophagy in the pathogenesis of Parkinson disease. Autophagy. 2009;5:706–708.
  • Vigie P, Camougrand N. Role of mitophagy in the mitochondrial quality control. Med Sci. 2017;33:231–237.
  • Lazarou M, Jin SM, Kane LA, et al. Role of PINK1 binding to the TOM complex and alternate intracellular membranes in recruitment and activation of the E3 ligase Parkin. Dev Cell. 2012;22:320–333.
  • Jin SM, Lazarou M, Wang C, et al. Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J Cell Biol. 2010;191:933–942.
  • Kim I, Rodriguez-Enriquez S, Lemasters JJ. Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys. 2007;462:245–253.
  • Chen Y, Dorn GW. PINK1-phosphorylated mitofusin 2 is a parkin receptor for culling damaged mitochondria. Science. 2013;340:471–475.
  • Narendra D, Tanaka A, Suen DF, et al. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol. 2008;183:795–803.
  • Kane LA, Lazarou M, Fogel AI, et al PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J Cell Biol. 2014;205:143–153.
  • Narendra DP, Jin SM, Tanaka A, et al PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. Plos Biol. 2010;8(1):e1000298.
  • Richter B, Sliter DA, Herhaus L, et al Phosphorylation of OPTN by TBK1 enhances its binding to Ub chains and promotes selective autophagy of damaged mitochondria. 2016;113(15):4039–4044.
  • Wong YC, Holzbaur EL. Temporal dynamics of PARK2/parkin and OPTN/optineurin recruitment during the mitophagy of damaged mitochondria. Autophagy. 2015;11:422–424.
  • Wong ACY, Ryan AF. Mechanisms of sensorineural cell damage, death and survival in the cochlea. Front Aging Neurosci. 2015;7:58.
  • Yu X, Liu W, Fan Z, et al c-Myb knockdown increases the neomycin-induced damage to hair-cell-like HEI-OC1 cells in vitro. Sci Rep. 2017;7:41094.
  • Nadal-Ferret M, Gelabert R, Moreno M, et al. How does the environment affect the absorption spectrum of the fluorescent protein mKeima? J Chem Theory Comput. 2013;9:1731–1742.
  • Henderson JN, Osborn MF, Koon N, et al. Excited state proton transfer in the red fluorescent protein mKeima. J Am Chem Soc. 2009;131:13212–13213.
  • Sun N, Yun J, Liu J, et al Measuring in vivo mitophagy. Mol Cell. 2015;60:685–696.
  • Kogure T, Kawano H, Abe Y, et al. Fluorescence imaging using a fluorescent protein with a large stokes shift. Methods. 2008;45:223–226.
  • Bueno M, Brands J, Voltz L, et al ATF3 represses PINK1 gene transcription in lung epithelial cells to control mitochondrial homeostasis. Aging Cell. 2018;17(2).
  • Checler F, Goiran T, Alves da Costa C. Presenilins at the crossroad of a functional interplay between PARK2/PARKIN and PINK1 to control mitophagy: implication for neurodegenerative diseases. Autophagy. 2017;13:2004–2005.
  • El Manaa W, Duplan E, Goiran T, et al Transcription- and phosphorylation-dependent control of a functional interplay between XBP1s and PINK1 governs mitophagy and potentially impacts Parkinson disease pathophysiology. Autophagy. 2021;17(12):1–23.
  • Landegger LD, Pan B, Askew C, et al A synthetic AAV vector enables safe and efficient gene transfer to the mammalian inner ear. Nat Biotechnol. 2017;35:280–284.
  • Gu X, Chai R, Guo L, et al Transduction of adeno-associated virus vectors targeting hair cells and supporting cells in the neonatal mouse cochlea. Front Cell Neurosci. 2019;13:8.
  • Allen GF, Toth R, James J, et al. Loss of iron triggers PINK1/Parkin-independent mitophagy. EMBO Rep. 2013;14:1127–1135.
  • Bingol B, Sheng M. Mechanisms of mitophagy: PINK1, Parkin, USP30 and beyond. Free Radical Bio Med. 2016;100:210–222.
  • Wang Y, Serricchio M, Jauregui M, et al Deubiquitinating enzymes regulate PARK2-mediated mitophagy. Autophagy. 2015;11:595–606.
  • Marcassa E, Kallinos A, Jardine J, et al. Dual role of USP30 in controlling basal pexophagy and mitophagy. EMBO Rep. 2018;19. DOI:10.15252/embr.201745595.
  • Kadlecova A, Makova B, Artal-Sanz M, et al. The plant hormone kinetin in disease therapy and healthy aging. Ageing Res Rev. 2019;55:100958.
  • Choi BH, Kim W, Wang QC, et al. Kinetin riboside preferentially induces apoptosis by modulating Bcl-2 family proteins and caspase-3 in cancer cells. Cancer Lett. 2008;261:37–45.
  • Hertz NT, Berthet A, Sos ML, et al. A neo-substrate that amplifies catalytic activity of Parkinson’s-disease-related kinase PINK1. Cell. 2013;154:737–747.
  • Lee SY, Han JJ, Lee SY, et al. Outcomes of peptide vaccine GV1001 treatment in a murine model of acute noise-induced hearing loss. Antioxidants (Basel). 2020;9(2):112.
  • Fettiplace R. Hair cell transduction, tuning, and synaptic transmission in the mammalian cochlea. Compr Physiol. 2017;7:1197–1227.
  • Yi W, MacDougall EJ, Tang MY, et al. The landscape of Parkin variants reveals pathogenic mechanisms and therapeutic targets in Parkinson’s disease. Hum Mol Genet. 2019;28:2811–2825.
  • Tang MY, Vranas M, Krahn AI, et al. Structure-guided mutagenesis reveals a hierarchical mechanism of Parkin activation. Nat Commun. 2017;8:14697.
  • Kliosnky D. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition) (vol 12, pg 1, 2015). Autophagy. 2016;12:443.
  • Cecconi F, Levine B. The role of autophagy in mammalian development: cell makeover rather than cell death. Dev Cell. 2008;15(3):344–357.
  • He Z, Guo L, Shu Y, et al. Autophagy protects auditory hair cells against neomycin-induced damage. Autophagy. 2017;13(11):1–21.
  • Yang Q, Zhou Y, Yin H, et al PINK1 protects against gentamicin-induced sensory hair cell damage: possible relation to induction of autophagy and inhibition of p53 signal pathway. Front Mol Neurosci. 2018;11:403.
  • Guan M, Fang Q, He Z, et al. Inhibition of ARC decreases the survival of HEI-OC-1 cells after neomycin damage in vitro. Oncotarget. 2016;7(41):66647–66659.
  • Youle RJ, Narendra DP. Mechanisms of mitophagy. Nat Rev Mol Cell Biol. 2011;12:9–14.
  • Pickrell AM, Youle RJ. The roles of PINK1, parkin, and mitochondrial fidelity in Parkinson’s disease. Neuron. 2015;85:257–273.
  • Shiba-Fukushima K, Imai Y, Yoshida S, et al PINK1-mediated phosphorylation of the Parkin ubiquitin-like domain primes mitochondrial translocation of Parkin and regulates mitophagy. Sci Rep. 2012;2:1002.
  • Goiran T, Duplan E, Chami M, et al Beta-amyloid precursor protein intracellular domain controls mitochondrial function by modulating phosphatase and tensin homolog-induced kinase 1 transcription in cells and in Alzheimer mice models. Biol Psychiatry. 2018;83:416–427.
  • Milon B, Shulman ED, So KS, et al A cell-type-specific atlas of the inner ear transcriptional response to acoustic trauma. Cell Rep. 2021;36:109758.
  • Kontoghiorghes GJ, Neocleous K, Kolnagou A. Benefits and risks of deferiprone in iron overload in Thalassaemia and other conditions: comparison of epidemiological and therapeutic aspects with deferoxamine. Drug Saf. 2003;26:553–584.
  • Georgakopoulos ND, Wells G, Campanella M. The pharmacological regulation of cellular mitophagy. Nat Chem Biol. 2017;13:136–146.
  • Zhang ZL, Wang NN, Ma QL, et al Somatic and germline mutations in the tumor suppressor gene PARK2 impair PINK1/Parkin-mediated mitophagy in lung cancer cells. Acta Pharmacol Sin. 2020;41:93–100.
  • Procaccio V, Bris C, Chao de la Barca JM, et al Perspectives of drug-based neuroprotection targeting mitochondria. Rev Neurol (Paris). 2014;170:390–400.
  • Ying Z, Wang HF, Fan HD, et al Gp78, an ER associated E3, promotes SOD1 and ataxin-3 degradation. Hum Mol Genet. 2009;18:4268–4281.
  • Tao ZT, Wang HF, Xia Q, et al Nucleolar stress and impaired stress granule formation contribute to C9orf72 RAN translation-induced cytotoxicity. Hum Mol Genet. 2015;24:2426–2441.
  • Xia Q, Wang GH, Wang HF, et al. Folliculin, a tumor suppressor associated with Birt-Hogg-Dube (BHD) syndrome, is a novel modifier of TDP-43 cytoplasmic translocation and aggregation. Hum Mol Genet. 2016;25:83–96.
  • Okatsu K, Oka T, Iguchi M, et al PINK1 autophosphorylation upon membrane potential dissipation is essential for Parkin recruitment to damaged mitochondria. Nat Commun. 2012;3:1016.
  • Tan F, Chu C, Qi J, et al AAV-ie enables safe and efficient gene transfer to inner ear cells. Nat Commun. 2019;10:3733.
  • Kalinec GM, Webster P, Lim DJ, et al. A cochlear cell line as an in vitro system for drug ototoxicity screening. Audiol Neuro-Otol. 2003;8:177–189.
  • Chen Y, Yu H, Zhang Y, et al Cotransfection of Pax2 and Math1 promote in situ cochlear hair cell regeneration after neomycin insult. Sci Rep. 2013;3:2996.
  • Makhdoumi P, Abnous K, Mehri S, et al. Oral deferiprone administration ameliorates cisplatin-induced nephrotoxicity in rats. J Pharm Pharmacol. 2018;70:1357–1368.
  • Fang Q, Zhang Y, Da P, et al Deletion of Limk1 and Limk2 in mice does not alter cochlear development or auditory function. Sci Rep. 2019;9:3357.
  • Wang J, Menchenton T, Yin S, et al Over-expression of X-linked inhibitor of apoptosis protein slows presbycusis in C57BL/6J mice. Neurobiol Aging. 2010;31:1238–1249.
  • Iguchi M, Kujuro Y, Okatsu K, et al Parkin-catalyzed ubiquitin-ester transfer is triggered by PINK1-dependent phosphorylation. J Biol Chem. 2013;288:22019–22032.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.