Ischemia-reperfusion injury of the cochlea: Pharmacological strategies for cochlear protection and implications of glutamate and reactive oxygen species

Current Neuropharmacology

Volumn 8, Issue 2, 2010, Pages 128-134

  Tabuchi, Keiji ^a   Nishimura, Bungo ^a   Tanaka, Shuho ^a   Hayashi, Kentaro ^a   Hirose, Yuki ^a   Hara, Akira ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Blood flow; Cochlea; Excitotoxicity; Ischemia reperfusion injury; Oxidative damage

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 2 CHLORO 6 N CYCLOPENTYLADENOSINE; 3 BROMO 7 NITROINDAZOLE; 6,7 DINITRO 2,3 QUINOXALINEDIONE; 7 NITROINDAZOLE; ADENOSINE RECEPTOR STIMULATING AGENT; AMINOGUANIDINE; DEFEROXAMINE; DIMETHYLTHIOUREA; DIZOCILPINE; DOPAMINE; EBSELEN; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR; GLUCOCORTICOID; GLUTAMATE RECEPTOR ANTAGONIST; GROWTH FACTOR; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; MANNITOL; METHYLPREDNISOLONE; MUSCIMOL; NITRIC OXIDE SYNTHASE INHIBITOR; NORPHENAZONE; PRASTERONE; PREDNISOLONE; RILUZOLE; SCAVENGER; SOMATOMEDIN C; TIRILAZAD; UNINDEXED DRUG;

ACOUSTIC NERVE FIBER; ARTICLE; CELL STRUCTURE; CLINICAL TRIAL; COCHLEA BLOOD FLOW; COCHLEA INJURY; COCHLEA POTENTIAL; DRUG MECHANISM; EXCITOTOXICITY; HAIR CELL; HUMAN; ISCHEMIA; NEUROPROTECTION; NONHUMAN; PATHOGENESIS; REPERFUSION INJURY; SENSORY NERVE; UNSPECIFIED SIDE EFFECT;

EID: 77953659872     PISSN: 1570159X     EISSN: None     Source Type: Journal    
DOI: 10.2174/157015910791233123     Document Type: Article

References (64)

1. Kim, J.S.; Lopes, I.; Dipatre, P.L.; Liu, F.; Ishiyama, A.; Baloh, R.W. Internal auditory artery infarction: clinicopathological correlation. Neurology, 1999,52, 40-44.
2. Thalmann, R.; Miyoshi, T.; Thalman, I. The influence of ischemia upon the energy reserves of inner ear tissues. Laryngoscope, 1972, 82, 2249-2272.
3. Perlman, H.B.; Kimura, R.; Fernandez, C. Experiments on temporary obstruction of the internal auditory artery. Laryngoscope, 1959, 69, 591-613.
4. Tabuchi, K.; Tsuji, S.; Fujihira, K.; Oikawa, K.; Hara, A.; Kusa-kari, J. Outer hair cells functionally and structurally deteriorate during reperfusion. Hear Res., 2002, 173, 153-163.
5. Olney, J.W.; Ho, O.L.; Rhee, V. Cytotoxic effects of acidic and sulphur containing amino acids on the infant mouse central nervous system. Exp. Brain Res., 1971, 14, 61-76.
6. Eybalin, M. Neurotransmitters and neuromodulators of the mammalian cochlea. Physiol. Rev., 1993, 73, 309-373.
7. Wenthold, R.J.; Hunter, C.; Petralia, R.S.; Niedzielski, A.S; Wang, Y.X.; Safieddine, S.; Zhao, H.M.; Rubio, M.E. Receptors in the auditory pathway. In: Neurotransmission and hearing loss. Basic sciences, diagnosis and management; Berlin, C.I., Ed.; Singular publishing group inc.: San Diego, CA., 1997, pp. 1-24.
8. Puel, J.L.; Pujol, R.; Tribillac, F.; Ladrech, S.; Eybalin, M. Excitatory amino acid antagonists protect cochlear auditory neurons from excitotoxicity. J. Comp. Neurol., 1994, 341, 241-256.
9. Hakuba, N.; Gyo, K.; Yanagihara, N.; Mitani, A.; Kataoka, K. Efflux of glutamate into the perilymph of the cochlea following transient ischemia in the gerbil. Neurosci. Lett., 1997, 230, 69-71.
10. Hakuba, N.; Koga, K.; Shudou, M.; Watanabe, F.; Mitani, A.; Gyo, K. Hearing loss and glutamate efflux in the perilymph following transient hindbrain ischemia in gerbils. J. Comp. Neurol., 2000, 418, 217-226.
11. Arriza, J.L.; Eliasof, S.; Kavanaugh, M.P.; Amara, S.G. Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc. Natl. Acad. Sci. USA., 1997, 94, 4155-4160.
12. Kanai, Y. Family of neutral and acidic amino acid transporters: molecular biology, physiology, and medical implications. Curr. Opin. Cell Biol., 1997, 9, 565-572.
13. Tanaka, K. Functions of glutamate transporters in the brain. Neuro-sci. Res., 2000, 37, 15-19.
14. Furness, D.N.; Lehre, K.P. Immunocytochemical localization of a high-affinity glutamate-aspartate transporter, GLAST, in the rat and guinea-pig cochlea. Eur. J. Neurosci., 1997, 9, 1961-1969.
15. Li, H.S.; Niedzielski, A.S.; Beisel, K.W.; Hiel, H.; Wenthold, R.J.; Morley, B.J. Identification of a glutamate/aspartate transporter in the rat cochlea. Hear Res., 1994, 78, 235-242.
16. Takumi, Y.; Matsubara, A.; Danbold, N.C.; Laake, J.H.; Storm-Mathisen, J.; Usami, S.I.; Shinkawa, H.; Ottersen, O.P. Discrete cellular and subcellular localization of glutamine synthetase and the glutamate transporter GLAST in the rat vestibular endorgan. Neu-roscience, 1997, 79, 1137-1144.
17. Usami, S.I.; Takumi, Y.; Matsubara, A.; Fujita, S.; Ottersen, O.P. Neurotransmission in the vestibular endorgans -glutamatergic transmission in the afferent synapse of hair cells. Biol. Sci. Space., 2001, 15, 367-370.
18. Hakuba, N.; Koga, K.; Gyo, K.; Usami, S.I.; Tanaka, K. Exacerbation of noise-induced hearing loss in mice lacking the glutamate transporter GLAST. J. Neurosci., 2000, 20, 8750-8753.
19. Aarts, M.M.; Tymianski, M. Novel treatment of excitotoxicity: targeted disruption of intracellular signaling from glutamate receptors. Biochem. Pharmacol., 2003, 66, 877-886.
20. Gerber, U.; Sin, J.A.; Gahwiler, B.H. Reduction of potassium conductances mediated by metabotropic glutamate receptors in rat CA3 pyramidal cells does not require protein kinase C or protein kinase A. Eur. J. Neurosci., 1992, 4, 792-797.
21. Hartmann, J.; Konnerth, A. Mechanisms of metabotropic glutamate receptor-medicated synaptic signaling in cerebellar Purkinje cells. Acta Physiol., 2009, 195, 79-90.
22. Shin, S.S.; Martino, J.J.; Chen, S. Metabotropic glutamate receptors (mGlus) and cellular transformation. Neuropharmacology, 2008, 55, 396-402.
23. Tabuchi, K.; Tsuji, S.; Wada, T.; Ito, Z.; Hara, A.; Kusakari, J. Effect of ketamine, dextromethorphan, and MK-801 on cochlear dysfunction induced by transient ischemia. Ann. Otol. Rhinol. Laryngol., 2002, 111, 44-49.
24. Sakai, S.; Tabuchi, K.; Murashita, H.; Hara, A. Activation of GABA(A) receptor ameliorates the cochlear excitotoxicity caused by kainic acid in the guinea pig. Tohoku J. Exp. Med., 2008, 215, 279-285.
25. Sun, H.; Salvi, R.J.; Ding, D.L.; Hashino, D.E.; Shero, M.; Zheng, X.Y. Excitotoxic effect of kainic acid on chicken otoacoustic emissions and cochlear potentials. J. Acoust. Soc. Am., 2000, 107, 2136-2142.
26. Mom, T.; Avan, P.; Romand, R.; Gilain, L. Monitoring of functional changes after transient ischemia in gerbil cochlea. Brain Res., 1997, 751, 20-30.
27. Morawski, K.; Telischi, F.F.; Niemczyk, K. A model of real time monitoring of the cochlear function during an induced local ischemia. Hear Res., 2006, 212, 117-127.
28. Tabuchi, K.; Ito, Z.; Wada, T.; Hara, A.; Kusakari, J. The effect of mannitol upon cochlear dysfunction induced by transient local anoxia. Hear Res., 1998, 126, 28-36.
29. Tsuji, S.; Tabuchi, K.; Hara, A.; Kusakari, J. Long-term observations on the reversibility of cochlear dysfunction after transient ischemia. Hear Res., 2003, 166, 72-81.
30. Samokyszyn, V.M.; Aust, S.D. Iron. In: Clinical ischemic syndromes; Zelenock, G.B., D'Alecy, L.G., Fantone III, J.C., Shlafer, M., Stanley, J.C., Eds.; Mosby Co: St. Louis, MO, USA, 1990, pp. 63-88.
31. Hara, A.; Komeno, M.; Senarita, M.; Serizawa, F.; Ishikawa, T.; Kusakari, J. Effect of asphyxia on the composition of cationic elements in the perilymph. Hear Res., 1995, 90, 228-231.
32. Hara, A.; Serizawa, F.; Tabuchi, K.; Senarita, M.; Kusakari, J. Hydroxyl radical formation in the perilymph of asphyxic guinea pig. Hear Res., 2000, 143, 110-114.
33. Tabuchi, K.; Tsuji, S.; Ito, Z.; Hara, A.; Kusakari, J. Does xanthine oxidase contribute to the hydroxyl radical generation in ischemia and reperfusion of the cochlea? Hear Res., 2001, 153, 1-6.
34. Morizane, I.; Hakuba, N.; Hyodo, J.; Shimizu, Y.; Fujita, K.; Yo-shida, T.; Gyo, K. Ischemic damage increase nitric oxide production via inducible nitric oxide synthase in the cochlea. Neurosci. Lett., 2005, 391, 62-67.
35. Franz, P.; Hauser-Kronberger, C.; Bock, P.; Quint, C.; Baumgartner, D. Localization of nitric oxide synthase I and III in the cochlea. Acta Otolaryngol., 1996, 116, 726-731.
36. Gosepath, K.; Gath, I.; Maurer, J.; Pollock, J.S.; Amedee, R.; Forstermann, U.; Mann, W. Characterization of nitric oxide synthase isoforms expressed in different structures of the guinea pig cochlea. Brain Res., 1997, 747, 26-33.
37. Tabuchi, K.; Ito, Z.; Wada, T.; Takahashi, K.; Hara, A.; Kusakari, J. Effect of 7-nitroindazole upon cochlear dysfunction induced by transient local anoxia. Ann. Otol. Rhinol. Laryngol., 2000, 109, 715-719.
38. Tabuchi, K.; Tsuji, S.; Asaka, Y.; Hara, A.; Kusakari, J. Ishcmeia-reperfusion injury of the cochlea: effects of iron chelator and nitric oxide synthase inhibitors. Hear Res., 2001, 160, 31-36.
39. Iadecola, C.; Zhang, F.; Xu, X. Induction of inducible nitric oxide synthase ameliorates cerebral ischemic damage. Am. J. Physiol., 1995, 268, R286-R292.
40. Iadecola, C.; Zhang, F.; Casey, R.; Clark, H.B.; Ross, E. Inducible nitric oxide synthase gene expression in vascular cells after transient focal cerebral ischemia. Stroke, 1996, 27, 1373-1380.
41. Zwolak, P.M.; Cronenwett, J.L. Hemodynamics and general patho-physiology of ischemic injury. In: Clinical ischemic syndromes; Zelenock, G.B., D'Alecy, L.G., Fantone III, J.C., Shlafer, M., Stanley, J.C., Eds.; Mosby Co.: St. Louis, MO, USA, 1990, pp. 63-88.
42. Gaborjan, A.; Lendvai, B.; Vizi, E.Z. Neurochemical evidence of dopamine release by lateral olivocochlear efferents and its presyn-aptic modulation in guinea-pig cochlea. Neuroscience, 1999, 90, 131-138.
43. Ruel, J.; Nouvian, R.; Gervais d'Aldin, C.; Pujol, R.; Eybalin, M.; Puel, J.L. Dopamine inhibition of auditory nerve activity in the adult mammalian cochlea. Eur. J. Neurosci., 2001, 14, 977-986.
44. Ruel, J.; Wang, J.; Pujol, R.; Hameq, A.; Dib, M.; Puel, J.L. Neuroprotective effect of riluzole in acute noise-induced hearing loss. Neuroreport, 2005, 16, 1087-1090.
45. Yamasoba, T.; Pourbakht, A.; Sakamot, T.; Suzuki, M. Ebselen prevents noise-induced excitotoxicity and temporary threshold shift. Neurosci. Lett., 2005, 380, 234-238.
46. Drescher, M.J.; Drescher, D.G.; Khan, K.M.; Hatfield, J.S.; Ramakrishnan, N.A.; Abu-Hamdan, M.D.; Lemonnier, L.A. Pituitary adenylyl cyclase-activating polypeptide (PACAP) and its receptor (PAC1-R) are positioned to modulate afferent signaling in the cochlea. Neuroscience, 2006, 142, 139-164.
47. Muir, K.W. Glutamate-based therapeutic approaches: clinical trials with NMDA antagonists. Curr. Opin. Pharmacol., 2006, 6, 53-60.
48. Seidman, M.D.; Quirk, W.S. The protective effects of tirilated mesylate (U74006F) on ischemic and reperfusion-induced cochlear damage. Otolaryngol. Head Neck Surg., 1991, 105, 511-516.
49. Maetani, T.; Hakuba, N.; Taniguchi, M.; Hyodo, J.; Shimizu, Y.; Gyo, K. Free radical scavenger protects against inner hair cell loss after cochlear ischemia. Neuroreport, 2003, 14, 1881-1884.
50. Tabuchi, K.; Okubo, H.; Fujihira, K.; Tsuji, S.; Hara, A.; Kusakari, J. Protection of outer hair cells from reperfusion injury by an iron chelator and a nitric oxide synthase inhibitor in the guinea pig cochlea. Neurosci. Lett., 2001, 307, 29-32.
51. Schubert, P.; Heinemann, U.; Kolb, R. Differential effect of adeno-sine on pre- and postsynaptic calcium influx. Brain Res., 1986, 376, 382-386.
52. Schubert, P. Physiological modulation by adenosine: selective blockade of A1-receptors with DPCPX enhances stimulus train-evoked neuronal Ca influx in rat hippocampal slices. Brain Res., 1988, 458, 162-165.
53. Simpson, P. Physiological modulation by adenosine: selective blockade of A1-receptors with DPCPX enhances stimulus train-evoked neuronal Ca influx in rat hippocampal slices. Brain Res., 1988, 458, 162-165.
54. Ford, M.S.; Maggirwar, S.B.; Rybak, L.P.; Whitworth, C.; Ram-kumar, V. Expression and function of adenosine receptors in the chinchilla cochlea. Hear Res., 1997, 105, 130-140.
55. Tabuchi, K.; Ito, Z.; Wada, T.; Takahashi, K.; Hara, A.; Kusakari, J. Effect of A1 adenosine receptor agonist upon cochlear dysfunction induced by transient ischemia. Hear Res., 1999, 136, 86-90.
56. Malgrange, B.; Rigo, J.M.; Coucke, P.; Thiry, M.; Hans, G.; Nguyen, L.; Van de Water, T.R.; Moonen, G.; Lefebvre, P.P. Identification of factors that maintain mammalian outer hair cells in adult organ of Corti explants. Hear Res., 2002, 170, 48-58.
57. Staecker, H.; Van de Water, T.R. Factors controlling hair-cell regeneration/repair in the inner ear. Curr. Opin. Neurobiol., 1998, 8, 480-487.
58. Andreeva, N.; Nyamaa, A.; Haupt, H.; Gross, J.; Mazurek, B. Recombinant human erythropoietin prevents ischemia-induced apoptosis and necrosis in explant cultures of the rat organ of Corti. Neurosci. Lett., 2006, 396, 86-90.
59. Fujiwara, T.; Hato, N.; Nakagawa, T.; Tabata, Y.; Yoshida, T.; Komobuchi, H.; Takeda, S.;, Hyodo, J.; Hakuba, N.; Gyo, K. Insulin-like growth factor 1 treatment via hydrogels rescues cochlear hair cells from ischemic injury. Neuroreport, 2008, 79, 1585-1588.
60. Lamm, K.; Arnold, W. The effect of predniolone and non-steroidal anti-inflammatory agents on the normal and noise-damaged guinea pig inner ear. Hear Res., 1998, 115, 149-161.
61. Lamm, K., Arnold, W. Successful treatment of noise-induced cochlear ischemia, hypoxia, and hearing loss. Ann. N. Y. Acad. Sci., 1999, 884, 233-248.
62. Tabuchi, K.; Oikawa, K.; Murashita, H.; Hoshino, T.; Tsuji, S.; Hara, A. Protective effects of glucocorticoids on ischemia-reperfusion injury of outer hair cells. Laryngoscope, 2006, 116, 627-629.
63. Tabuchi, K.; Oikawa, K.; Uemaetomari, I.; Tsuji, S.; Wada, T.; Hara, A. Glucocorticoids and dehydroepiandrosterone sulfate ameliorate ischemia-induced injury of the cochlea. Hear Res., 2003, 180, 51-56.
64. Tabuchi, K.; Murashita, H.; Tobita, T.; Oikawa, K.; Tsuji, S.; Uemaetomari, I.; Hara, A. Dehydroepiandrosterone sulfate reduces acoustic injury of the guinea-pig cochlea. J. Pharmacol. Sci., 2005, 99, 191-194.