Spontaneous and Partial Repair of Ribbon Synapse in Cochlear Inner Hair Cells After Ototoxic Withdrawal

详细信息    查看全文

• 作者：Ke Liu ; DaiShi Chen ; WeiWei Guo ; Ning Yu ; XiaoYu Wang ; Fei Ji…
• 关键词：Sensorineural deafness ; Cochlea ; Ribbon synapse ; Ototoxic exposure ; RIBEYE/CtBP2
• 刊名：Molecular Neurobiology
• 出版年：2015
• 出版时间：December 2015
• 年：2015
• 卷：52
• 期：3
• 页码：1680-1689
• 全文大小：5,357 KB
• 参考文献：1.Komune S, Ide M, Nakano T, Morimitsu T (1987) Effects of kanamycin sulfate on cochlear potentials and potassium ion permeability through the cochlear partitions. ORL J Otorhinolaryngol Relat Spec 49(1):9鈥?6CrossRef PubMed
  2.Nakagawa T, Yamane H, Shibata S, Nakai Y (1997) Gentamicin ototoxicity induced apoptosis of the vestibular hair cells of guinea pigs. Eur Arch Otorhinolaryngol 254(1):9鈥?4CrossRef PubMed
  3.Wu WJ, Sha SH, McLaren JD, Kawamoto K, Raphael Y, Schacht J (2001) Aminoglycoside ototoxicity in adult CBA, C57BL and BALB mice and the Sprague-Dawley rat. Hear Res 158(1鈥?):165鈥?78CrossRef PubMed
  4.Gooi A, Hochman J, Wellman M, Blakley L, Blakley BW (2008) Ototoxic effects of single-dose versus 19-day daily-dose gentamicin. J Otolaryngol Head Neck Surg 37(5):664鈥?67PubMed
  5.Perletti G, Vral A, Patrosso MC, Marras E, Ceriani I, Willems P, Fasano M, Magri V (2008) Prevention and modulation of aminoglycoside ototoxicity (review). Mol Med Rep 1(1):3鈥?3PubMed
  6.Webster M, Webster DB (1981) Spiral ganglion neuron loss following organ of Corti loss: a quantitative study. Brain Res 212(1):17鈥?0CrossRef PubMed
  7.McFadden SL, Ding D, Jiang H, Salvi RJ (2004) Time course of efferent fiber and spiral ganglion cell degeneration following complete hair cell loss in the chinchilla. Brain Res 997(1):40鈥?1CrossRef PubMed
  8.Ding D, Jiang H, Salvi RJ (2010) Mechanisms of rapid sensory hair-cell death following co-administration of gentamicin and ethacrynic acid. Hear Res 259(1鈥?):16鈥?3. doi:10.鈥?016/鈥媕.鈥媓eares.鈥?009.鈥?8.鈥?08 PubMed Central CrossRef PubMed
  9.ShuNa L, Zhong R, Ke L (2009) A pattern of otoferlin expression interrupted by gentamicin exposure in ribbon synapse of inner hair cell in C57BL/6J mice. Acta Neurol Belg 109(3):221鈥?25PubMed
  10.Liu K, Jiang X, Shi C, Shi L, Yang B, Shi L, Xu Y, Yang W, Yang S (2013) Cochlear inner hair cell ribbon synapse is the primary target of ototoxic aminoglycoside stimuli. Mol Neurobiol 48(3):647鈥?54. doi:10.鈥?007/鈥媠12035-013-8454-2 CrossRef PubMed
  11.Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after 鈥渢emporary鈥?noise-induced hearing loss. J Neurosci 29(45):14077鈥?4085. doi:10.鈥?523/鈥婮NEUROSCI.鈥?2845-09.鈥?009 PubMed Central CrossRef PubMed
  12.Sidi S, Busch-Nentwich E, Friedrich R, Schoenberger U, Nicolson T (2004) Gemini encodes a zebrafish L-type calcium channel that localizes at sensory hair cell ribbon synapses. J Neurosci 24(17):4213鈥?223. doi:10.鈥?523/鈥婮NEUROSCI.鈥?0223-04.鈥?004 CrossRef PubMed
  13.Moser T, Neef A, Khimich D (2006) Mechanisms underlying the temporal precision of sound coding at the inner hair cell ribbon synapse. J Physiol 576(Pt 1):55鈥?2. doi:10.鈥?113/鈥媕physiol.鈥?006.鈥?14835 PubMed Central CrossRef PubMed
  14.Stamataki S, Francis HW, Lehar M, May BJ, Ryugo DK (2006) Synaptic alterations at inner hair cells precede spiral ganglion cell loss in aging C57BL/6J mice. Hear Res 221(1鈥?):104鈥?18. doi:10.鈥?016/鈥媕.鈥媓eares.鈥?006.鈥?7.鈥?14 CrossRef PubMed
  15.Lenzi D, Crum J, Ellisman MH, Roberts WM (2002) Depolarization redistributes synaptic membrane and creates a gradient of vesicles on the synaptic body at a ribbon synapse. Neuron 36(4):649鈥?59CrossRef PubMed
  16.Keen EC, Hudspeth AJ (2006) Transfer characteristics of the hair cell鈥檚 afferent synapse. Proc Natl Acad Sci U S A 103(14):5537鈥?542. doi:10.鈥?073/鈥媝nas.鈥?601103103 PubMed Central CrossRef PubMed
  17.Johnson SL, Forge A, Knipper M, Munkner S, Marcotti W (2008) Tonotopic variation in the calcium dependence of neurotransmitter release and vesicle pool replenishment at mammalian auditory ribbon synapses. J Neurosci 28(30):7670鈥?678. doi:10.鈥?523/鈥婮NEUROSCI.鈥?0785-08.鈥?008 PubMed Central CrossRef PubMed
  18.Ding D, Stracher A, Salvi RJ (2002) Leupeptin protects cochlear and vestibular hair cells from gentamicin ototoxicity. Hear Res 164(1鈥?):115鈥?26CrossRef PubMed
  19.Glowatzki E, Fuchs PA (2002) Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5(2):147鈥?54. doi:10.鈥?038/鈥媙n796 CrossRef PubMed
  20.Griesinger CB, Richards CD, Ashmore JF (2005) Fast vesicle replenishment allows indefatigable signalling at the first auditory synapse. Nature 435(7039):212鈥?15. doi:10.鈥?038/鈥媙ature03567 CrossRef PubMed
  21.Khimich D, Nouvian R, Pujol R, Tom Dieck S, Egner A, Gundelfinger ED, Moser T (2005) Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434(7035):889鈥?94. doi:10.鈥?038/鈥媙ature03418 CrossRef PubMed
  22.Nemzou NR, Bulankina AV, Khimich D, Giese A, Moser T (2006) Synaptic organization in cochlear inner hair cells deficient for the CaV1.3 (alpha1D) subunit of L-type Ca2+ channels. Neuroscience 141(4):1849鈥?860. doi:10.鈥?016/鈥媕.鈥媙euroscience.鈥?006.鈥?5.鈥?57 CrossRef
  23.Meyer AC, Frank T, Khimich D, Hoch G, Riedel D, Chapochnikov NM, Yarin YM, Harke B, Hell SW, Egner A, Moser T (2009) Tuning of synapse number, structure and function in the cochlea. Nat Neurosci 12(4):444鈥?53. doi:10.鈥?038/鈥媙n.鈥?293 CrossRef PubMed
  24.Liu K, Hu JY, Wang D, Schacher S (2003) Protein synthesis at synapse versus cell body: enhanced but transient expression of long-term facilitation at isolated synapses. J Neurobiol 56(3):275鈥?86. doi:10.鈥?002/鈥媙eu.鈥?0242 CrossRef PubMed
  25.Hu JY, Glickman L, Wu F, Schacher S (2004) Serotonin regulates the secretion and autocrine action of a neuropeptide to activate MAPK required for long-term facilitation in Aplysia. Neuron 43(3):373鈥?85. doi:10.鈥?016/鈥媕.鈥媙euron.鈥?004.鈥?7.鈥?11 CrossRef PubMed
  26.Hu JY, Baussi O, Levine A, Chen Y, Schacher S (2011) Persistent long-term synaptic plasticity requires activation of a new signaling pathway by additional stimuli. J Neurosci 31(24):8841鈥?850. doi:10.鈥?523/鈥婮NEUROSCI.鈥?1358-11.鈥?011 PubMed Central CrossRef PubMed
  27.Abrashkin KA, Izumikawa M, Miyazawa T, Wang CH, Crumling MA, Swiderski DL, Beyer LA, Gong TW, Raphael Y (2006) The fate of outer hair cells after acoustic or ototoxic insults. Hear Res 218(1鈥?):20鈥?9. doi:10.鈥?016/鈥媕.鈥媓eares.鈥?006.鈥?4.鈥?01 CrossRef PubMed
  28.Nouvian R, Beutner D, Parsons TD, Moser T (2006) Structure and function of the hair cell ribbon synapse. J Membr Biol 209(2鈥?):153鈥?65. doi:10.鈥?007/鈥媠00232-005-0854-4 PubMed Central CrossRef PubMed
  29.Neef A, Khimich D, Pirih P, Riedel D, Wolf F, Moser T (2007) Probing the mechanism of exocytosis at the hair cell ribbon synapse. J Neurosci 27(47):12933鈥?2944. doi:10.鈥?523/鈥婮NEUROSCI.鈥?1996-07.鈥?007 CrossRef PubMed
  30.Zanazzi G, Matthews G (2009) The molecular architecture of ribbon presynaptic terminals. Mol Neurobiol 39(2):130鈥?48. doi:10.鈥?007/鈥媠12035-009-8058-z PubMed Central CrossRef PubMed
  31.Roux I, Safieddine S, Nouvian R, Grati M, Simmler MC, Bahloul A, Perfettini I, Le Gall M, Rostaing P, Hamard G, Triller A, Avan P, Moser T, Petit C (2006) Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse. Cell 127(2):277鈥?89. doi:10.鈥?016/鈥媕.鈥媍ell.鈥?006.鈥?8.鈥?40 CrossRef PubMed
  32.Yu L, Jiang XH, Zhou Z, Tsang LL, Yu MK, Chung YW, Zhang XH, Wang AM, Tang H, Chan HC (2011) A protective mechanism against antibiotic-induced ototoxicity: role of prestin. PLoS ONE 6(2):e17322. doi:10.鈥?371/鈥媕ournal.鈥媝one.鈥?017322 PubMed Central CrossRef PubMed
  33.Schmitz F, Konigstorfer A, Sudhof TC (2000) RIBEYE, a component of synaptic ribbons: a protein鈥檚 journey through evolution provides insight into synaptic ribbon function. Neuron 28(3):857鈥?72CrossRef PubMed
  34.Wan L, Almers W, Chen W (2005) Two ribeye genes in teleosts: the role of Ribeye in ribbon formation and bipolar cell development. J Neurosci 25(4):941鈥?49. doi:10.鈥?523/鈥婮NEUROSCI.鈥?4657-04.鈥?005 CrossRef PubMed
  35.Magupalli VG, Schwarz K, Alpadi K, Natarajan S, Seigel GM, Schmitz F (2008) Multiple RIBEYE-RIBEYE interactions create a dynamic scaffold for the formation of synaptic ribbons. J Neurosci 28(32):7954鈥?967. doi:10.鈥?523/鈥婮NEUROSCI.鈥?1964-08.鈥?008 CrossRef PubMed
  36.Moser T, Brandt A, Lysakowski A (2006) Hair cell ribbon synapses. Cell Tissue Res 326(2):347鈥?59. doi:10.鈥?007/鈥媠00441-006-0276-3 PubMed Central CrossRef PubMed
  37.Hull C, Studholme K, Yazulla S, von Gersdorff H (2006) Diurnal changes in exocytosis and the number of synaptic ribbons at active zones of an ON-type bipolar cell terminal. J Neurophysiol 96(4):2025鈥?033. doi:10.鈥?152/鈥媕n.鈥?0364.鈥?006 PubMed Central CrossRef PubMed
  38.Frank T, Khimich D, Neef A, Moser T (2009) Mechanisms contributing to synaptic Ca2+ signals and their heterogeneity in hair cells. Proc Natl Acad Sci U S A 106(11):4483鈥?488. doi:10.鈥?073/鈥媝nas.鈥?813213106 PubMed Central CrossRef PubMed
  39.Jackman SL, Choi SY, Thoreson WB, Rabl K, Bartoletti TM, Kramer RH (2009) Role of the synaptic ribbon in transmitting the cone light response. Nat Neurosci 12(3):303鈥?10. doi:10.鈥?038/鈥媙n.鈥?267 PubMed Central CrossRef PubMed
  40.Lin HW, Furman AC, Kujawa SG, Liberman MC (2011) Primary neural degeneration in the guinea pig cochlea after reversible noise-induced threshold shift. J Assoc Res Otolaryngol 12(5):605鈥?16. doi:10.鈥?007/鈥媠10162-011-0277-0 PubMed Central CrossRef PubMed
  41.Shi L, Liu L, He T, Guo X, Yu Z, Yin S, Wang J (2013) Ribbon synapse plasticity in the cochleae of guinea pigs after noise-induced silent damage. PLoS ONE 8(12):e81566. doi:10.鈥?371/鈥媕ournal.鈥媝one.鈥?081566 PubMed Central CrossRef PubMed
  42.Forge A, Schacht J (2000) Aminoglycoside antibiotics. Audiol Neurootol 5(1):3鈥?2CrossRef PubMed
  43.Dehne N, Rauen U, de Groot H, Lautermann J (2002) Involvement of the mitochondrial permeability transition in gentamicin ototoxicity. Hear Res 169(1鈥?):47鈥?5CrossRef PubMed
  44.Hong SH, Park SK, Cho YS, Lee HS, Kim KR, Kim MG, Chung WH (2006) Gentamicin induced nitric oxide-related oxidative damages on vestibular afferents in the guinea pig. Hear Res 211(1鈥?):46鈥?3. doi:10.鈥?016/鈥媕.鈥媓eares.鈥?005.鈥?8.鈥?09 CrossRef PubMed
  45.Liu K, Shi C, Sun Y, Xu Y, Shi L, Shi L, Wang X, Ji F, Hou Z, Yang S (2014) Dynamic distribution of ototoxic gentamicin entry into inner hair cells of mice. Acta Otolaryngol 134(4):345鈥?51. doi:10.鈥?109/鈥?0016489.鈥?013.鈥?75219 CrossRef PubMed
  46.Starr A, Picton TW, Sininger Y, Hood LJ, Berlin CI (1996) Auditory neuropathy. Brain 119(Pt 3):741鈥?53CrossRef PubMed
  47.Ohashi T, Ochi K, Nishino H, Kenmochi M, Yoshida K (2005) Recovery of human compound action potential using a paired-click stimulation paradigm. Hear Res 203(1鈥?):192鈥?00. doi:10.鈥?016/鈥媕.鈥媓eares.鈥?004.鈥?2.鈥?01 CrossRef PubMed
  48.Seal RP, Akil O, Yi E, Weber CM, Grant L, Yoo J, Clause A, Kandler K, Noebels JL, Glowatzki E, Lustig LR, Edwards RH (2008) Sensorineural deafness and seizures in mice lacking vesicular glutamate transporter 3. Neuron 57(2):263鈥?75. doi:10.鈥?016/鈥媕.鈥媙euron.鈥?007.鈥?1.鈥?32 PubMed Central CrossRef PubMed
  
• 作者单位：Ke Liu (1)
  DaiShi Chen (1)
  WeiWei Guo (1)
  Ning Yu (1)
  XiaoYu Wang (1)
  Fei Ji (1)
  ZhaoHui Hou (1)
  Wei-Yan Yang (1)
  ShiMing Yang (1)
  
  1. Department of Otolaryngology-Head and Neck Surgery, the Institute of Otolaryngology, Chinese PLA General Hospital, 28 Fuxing Road, 100853, Beijing, China
  
• 刊物主题：Neurosciences; Neurobiology; Cell Biology; Neurology;
• 出版者：Springer US
• ISSN：1559-1182

文摘

Ototoxicity is one of the major causes of sensorineural deafness. However, it remains unclear whether sensorineural deafness is reversible after ototoxic withdrawal. Here, we report that the ribbon synapses between the inner hair cells (IHCs) and spiral ganglion nerve (SGN) fibers can be restored after ototoxic trauma. This corresponds with hearing restoration after ototoxic withdrawal. In this study, adult mice were injected daily with a low dose of gentamicin for 14 consecutive days. Immunostaining for RIBEYE/CtBP2 was used to estimate the number and size of synaptic ribbons in the cochlea. Hearing thresholds were assessed using auditory brainstem responses. Auditory temporal processing between IHCs and SGNs was evaluated by compound action potentials. We found automatic hearing restoration after ototoxicity withdrawal, which corresponded to the number and size recovery of synaptic ribbons, although both hearing and synaptic recovery were not complete. Thus, our study indicates that sensorineural deafness in mice can be reversible after ototoxic withdrawal due to an intrinsic repair of ribbon synapse in the cochlea. Keywords Sensorineural deafness Cochlea Ribbon synapse Ototoxic exposure RIBEYE/CtBP2