Noise-induced loss of hair cells and cochlear synaptopathy are mediated by the activation of AMPK

Journal of Neuroscience

Volumn 36, Issue 28, 2016, Pages 7497-7510

  Hill, Kayla ^a   Yuan, Hu ^a   Wang, Xianren ^a   Sha, Su Hua ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Activation of AMPK; Cochlear synaptopathy; Noise induced hearing loss; Protection of noise induced hearing loss; Sensory hair cells

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ACTIVATOR; PROTEIN KINASE LKB1; (6-(4-(2-PIPERIDIN-1-YLETHOXY)PHENYL))-3-PYRIDIN-4-YLPYRAZOLO(1,5-A)PYRIMIDINE; AMPA RECEPTOR; CTBP2 PROTEIN, MOUSE; DNA BINDING PROTEIN; ENZYME INHIBITOR; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 2; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PHOSPHOPROTEIN; PROTEIN SERINE THREONINE KINASE; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE; SMALL INTERFERING RNA; STK11 PROTEIN, MOUSE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ANTIBODY SPECIFICITY; ARTICLE; CELL COUNT; CELL DEATH; COCHLEA INJURY; COCHLEAR HAIR CELL; COCHLEAR NERVE; COCHLEAR SYNAPTOPATHY; CONTROLLED STUDY; CORNEAL ENDOTHELIAL CELL LOSS; ELECTROPHORESIS; EVOKED BRAIN STEM AUDITORY RESPONSE; HEARING IMPAIRMENT; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NEUROEPITHELIUM; NOISE; NONHUMAN; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SOUND INTENSITY; WESTERN BLOTTING; ADVERSE EFFECTS; ANIMAL; AUDITORY STIMULATION; CBA MOUSE; COCHLEA; DOSE RESPONSE; DRUG ADMINISTRATION ROUTE; DRUG EFFECTS; GENE EXPRESSION REGULATION; HEARING LOSS, NOISE-INDUCED; METABOLISM; PATHOLOGY; PHYSIOLOGY; SYNAPSE;

ACOUSTIC STIMULATION; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELL DEATH; COCHLEA; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION ROUTES; ENZYME INHIBITORS; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; GENE EXPRESSION REGULATION; HAIR CELLS, AUDITORY; HEARING LOSS, NOISE-INDUCED; MALE; MICE; MICE, INBRED CBA; NOISE; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; PYRAZOLES; PYRIMIDINES; RECEPTORS, AMPA; RNA, SMALL INTERFERING; SYNAPSES;

EID: 84978805732     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0782-16.2016     Document Type: Article

References (46)

1. Anselmi F, Hernandez VH, Crispino G, Seydel A, Ortolano S, Roper SD, Kessaris N, Richardson W, Rickheit G, Filippov MA, Monyer H, Mammano F (2008) ATP release through connexin hemichannels and gap junction transfer of second messengers propagate Ca2signals across the inner ear. Proc Natl Acad Sci U S A 105:18770-18775. CrossRef Medline
2. Chen FQ, Zheng HW, Hill K, Sha SH (2012) Traumatic noise activates rhofamily GTPases through transient cellular energy depletion. J Neurosci 32:12421–12430. CrossRef Medline
3. Chen FQ, Zheng HW, Schacht J, Sha SH (2013) Mitochondrial peroxiredoxin 3 regulates sensory cell survival in the cochlea. PLoS One 8:e61999. CrossRef Medline
4. Chen GD, Fechter LD (2003) The relationship between noise-induced hearing loss and hair cell loss in rats. Hear Res 177:81–90. CrossRef Medline
5. Denoyelle F, Lina-Granade G, Plauchu H, Bruzzone R, Chaïb H, Lévi-Acobas F, Weil D, Petit C (1998) Connexin 26 gene linked to a dominant deafness. Nature 393:319-320. CrossRef Medline
6. Fetoni AR, De Bartolo P, Eramo SL, Rolesi R, Paciello F, Bergamini C, Fato R, Paludetti G, Petrosini L, Troiani D (2013) Noise-induced hearing loss (NIHL) as a target of oxidative stress-mediated damage: cochlear and cortical responses after an increase in antioxidant defense. J Neurosci 33:4011–4023. CrossRef Medline
7. Föller M, Jaumann M, Dettling J, Saxena A, Pakladok T, Munoz C, Ruth P, Sopjani M, Seebohm G, Rüttiger L, Knipper M, Lang F (2012) AMPactivated protein kinase in BK-channel regulation and protection against hearing loss following acoustic overstimulation. FASEB J 26:4243–4253. CrossRef Medline
8. Han Y, Wang X, Chen J, Sha SH (2015) Noise-induced cochlear F-actin depolymerization is mediated via ROCK2/p-ERM signaling. J Neurochem 133:617–628. CrossRef Medline
9. Hardie DG (2003) Minireview: the AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology 144:5179-5183. CrossRef Medline
10. Hardie DG, Salt IP, Hawley SA, Davies SP (1999) AMP-activated protein kinase: an ultrasensitive system for monitoring cellular energy charge. Biochem J 338:717–722. CrossRef Medline
11. Hardie DG, Scott JW, Pan DA, Hudson ER (2003) Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett 546: 113–120. CrossRef Medline
12. Hu BH, Henderson D, Nicotera TM (2002) F-actin cleavage in apoptotic outer hair cells in chinchilla cochleas exposed to intense noise. Hear Res 172:1–9. CrossRef Medline
13. Jansen M, Ten Klooster JP, Offerhaus GJ, Clevers H (2009) LKB1 and AMPKfamily signaling: the intimate link between cell polarity and energy metabolism. Physiol Rev 89:777–798. CrossRef Medline
14. Jensen-Smith HC, Hallworth R, Nichols MG (2012) Gentamicin rapidly inhibits mitochondrial metabolism in high-frequency cochlear outer hair cells. PLoS One 7:e38471. CrossRef Medline
15. Kefas BA, Cai Y, Kerckhofs K, Ling Z, Martens G, Heimberg H, Pipeleers D, Van de Casteele M (2004) Metformin-induced stimulation of AMPactivated protein kinase in beta-cells impairs their glucose responsiveness and can lead to apoptosis. Biochem Pharmacol 68:409–416. CrossRef Medline
16. Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J Neurosci 29:14077–14085. CrossRef Medline
17. Lahne M, Gale JE (2010) Damage-induced cell-cell communication in different cochlear cell types via two distinct ATP-dependent Ca waves. Purinergic Signal 6:189–200. CrossRef Medline
18. Le Prell CG, Hughes LF, Miller JM (2007) Free radical scavengers vitamins A, C, and E plus magnesium reduce noise trauma. Free Radic Biol Med 42:1454-1463. CrossRef Medline
19. Liberman LD, Suzuki J, Liberman MC (2015) Dynamics of cochlear synaptopathy after acoustic overexposure. J Assoc Res Otolaryngol 16:205–219. CrossRef Medline
20. Lizcano JM, Göransson O, Toth R, Deak M, Morrice NA, Boudeau J, Hawley SA, Udd L, Mäkelä TP, Hardie DG, Alessi DR (2004) LKB1 is a master kinase that activates 13 kinases of theAMPKsubfamily, including MARK/ PAR-1. EMBO J 23:833–843. CrossRef Medline
21. May LA, Kramarenko II, Brandon CS, Voelkel-Johnson C, Roy S, Truong K, Francis SP, Monzack EL, Lee FS, Cunningham LL (2013) Inner ear supporting cells protect hair cells by secreting HSP70. J Clin Invest 123: 3577–3587. CrossRef Medline
22. McKay SE, Yan W, Nouws J, Thormann MJ, Raimundo N, Khan A, Santos- Sacchi J, Song L, Shadel GS (2015) Auditory pathology in a transgenic mtTFB1 mouse model of mitochondrial deafness. Am J Pathol 185: 3132–3140. CrossRef Medline
23. Müller M, von Hünerbein K, Hoidis S, Smolders JW (2005) A physiological place-frequency map of the cochlea in the CBA/J mouse. Hear Res 202: 63–73. CrossRef Medline
24. Nagashima R, Yamaguchi T, Kuramoto N, Ogita K (2011) Acoustic overstimulation activates 5’-AMP-activated protein kinase through a temporary decrease in ATP level in the cochlear spiral ligament prior to permanent hearing loss in mice. Neurochem Int 59:812–820. CrossRef Medline
25. Ohinata Y, Miller JM, Altschuler RA, Schacht J (2000) Intense noise induces formation of vasoactive lipid peroxidation products in the cochlea. Brain Res 878:163–173. CrossRef Medline
26. Ohlemiller KK, Wright JS, Dugan LL (1999) Early elevation of cochlear reactive oxygen species following noise exposure. Audiol Neurootol 4: 229–236. CrossRef Medline
27. Oishi N, Chen FQ, Zheng HW, Sha SH (2013) Intra-tympanic delivery of short interfering RNA into the adult mouse cochlea. Hear Res 296:36–41. CrossRef Medline
28. Schulz E, Dopheide J, Schuhmacher S, Thomas SR, Chen K, Daiber A, Wenzel P, Münzel T, Keaney JF Jr (2008) Suppression of the JNK pathway by induction of a metabolic stress response prevents vascular injury and dysfunction. Circulation 118:1347–1357. CrossRef Medline
29. Shen QW, Gerrard DE, Du M (2008) Compound C, an inhibitor of AMPactivated protein kinase, inhibits glycolysis in mouse longissimus dorsi postmortem. Meat Sci 78:323–330. CrossRef Medline
30. Song P, Xie Z, Wu Y, Xu J, Dong Y, Zou MH (2008) Protein kinase Czetadependent LKB1 serine 428 phosphorylation increases LKB1 nucleus export and apoptosis in endothelial cells. J Biol Chem 283:12446-12455. CrossRef Medline
31. Suter M, Riek U, Tuerk R, Schlattner U, Wallimann T, Neumann D (2006) Dissecting the role of 5’-AMP for allosteric stimulation, activation, and deactivation of AMP-activated protein kinase. J Biol Chem 281:32207–32216. CrossRef Medline
32. Tiede L, Steyger PS, Nichols MG, Hallworth R (2009) Metabolic imaging of the organ of corti—a window on cochlea bioenergetics. Brain Res 1277: 37–41. CrossRef Medline
33. Vicente-Torres MA, Schacht J (2006) A BAD link to mitochondrial cell death in the cochlea of mice with noise-induced hearing loss. J Neurosci Res 83:1564-1572. CrossRef Medline
34. Viollet B, Horman S, Leclerc J, Lantier L, Foretz M, Billaud M, Giri S, Andreelli F (2010) AMPK inhibition in health and disease. Crit Rev Biochem Mol Biol 45:276-295. CrossRef Medline
35. Wan G, Gomez-Casati ME, Gigliello AR, Liberman MC, Corfas G (2014) Neurotrophin-3 regulates ribbon synapse density in the cochlea and induces synapse regeneration after acoustic trauma. Elife 3:e03564. CrossRef Medline
36. Wang Y, Hirose K, Liberman MC (2002) Dynamics of noise-induced cellular injury and repair in the mouse cochlea. J Assoc Res Otolaryngol 3: 248–268. CrossRef Medline
37. Weisová P, Dávila D, Tuffy LP, Ward MW, Concannon CG, Prehn JH (2011) Role of 5’-adenosine monophosphate-activated protein kinase in cell survival and death responses in neurons. Antioxid Redox Signal 14:1863–1876. CrossRef Medline
38. Winder WW, Thomson DM (2007) Cellular energy sensing and signaling by AMP-activated protein kinase. Cell Biochem Biophys 47:332–347. CrossRef Medline
39. Xia JH, Liu CY, Tang BS, Pan Q, Huang L, Dai HP, Zhang BR, Xie W, Hu DX, Zheng D, Shi XL, Wang DA, Xia K, Yu KP, Liao XD, Feng Y, Yang YF, Xiao JY, Xie DH, Huang JZ (1998) Mutations in the gene encoding gap junction protein beta-3 associated with autosomal dominant hearing impairment. Nat Genet 20:370-373. CrossRef Medline
40. Yamane H, Nakai Y, Takayama M, Iguchi H, Nakagawa T, Kojima A (1995) Appearance of free radicals in the guinea pig inner ear after noise-induced acoustic trauma. Eur Arch Otorhinolaryngol 252:504-508. CrossRef Medline
41. Yamasoba T, Nuttall AL, Harris C, Raphael Y, Miller JM (1998) Role of glutathione in protection against noise-induced hearing loss. Brain Res 784:82–90. CrossRef Medline
42. Yuan H, Wang X, Hill K, Chen J, Lemasters J, Yang SM, Sha SH (2015) Autophagy attenuates noise-induced hearing loss by reducing oxidative stress. Antioxid Redox Signal 22:1308-1324. CrossRef Medline
43. Yun H, Lee M, Kim SS, Ha J (2005) Glucose deprivation increases mRNA stability of vascular endothelial growth factor through activation of AMPactivated protein kinase in DU145 prostate carcinoma. J Biol Chem 280: 9963–9972. CrossRef Medline
44. Yun H, Kim HS, Lee S, Kang I, Kim SS, Choe W, Ha J (2009) AMP kinase signaling determines whether c-Jun N-terminal kinase promotes survival or apoptosis during glucose deprivation. Carcinogenesis 30:529–537. CrossRef Medline
45. Zhang Y, Tang W, Ahmad S, Sipp JA, Chen P, Lin X (2005) Gap junctionmediated intercellular biochemical coupling in cochlear supporting cells is required for normal cochlear functions. Proc Natl Acad Sci U S A 102: 15201–15206. CrossRef Medline
46. Zheng HW, Chen J, Sha SH (2014) Receptor-interacting protein kinases modulate noise-induced sensory hair cell death. Cell Death Dis 5:e1262. CrossRef Medline