Cochlear hair cells of echolocating bats are immune to intense noise

Zhen Liu; Peng Chen; Yuan-Yuan Li; Meng-Wen Li; Qi Liu; Wen-Lu Pan; Dong-Ming Xu; Jing Bai; Li-Biao Zhang; Jie Tang; Peng Shi

doi:10.1016/j.jgg.2021.06.007

Volume 48 Issue 11

Nov. 2021

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Article Navigation > Journal of Genetics and Genomics > 2021 > 48(11): 984-993

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Cochlear hair cells of echolocating bats are immune to intense noise

doi: 10.1016/j.jgg.2021.06.007

a State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650223, China;
b Kunming College of Life Science, University of Chinese Academy of Sciences, Beijing 100049, China;
c Key Laboratory of Mental Health of the Ministry of Education, Southern Medical University, Guangzhou, Guangdong 510515, China;
d Guangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of Sciences, Guangzhou, Guangdong 510260, China;
e Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, Yunnan 650223, China

Funds:

the China National Center for Biotechnology Development (2020YFC0847000)

We thank Hui Yang for his valuable comments. This work was supported by grants from the National Natural Science Foundation of China (31930011, 31922010, 31871270), China

the Key Research Program of the Chinese Academy of Sciences (KJZD-SW-L11)

and the Yunnan Fundamental Research Project (No. 2019FI008), China. J.T. was supported by the Program for Changjiang Scholars and Innovative Research Team in University (IRT_16R37). L.B.Z. was supported by the GDAS Special Project of Science and Technology Development (2018GDASCX-0107).

Received Date: 2021-01-08
Accepted Date: 2021-06-06
Rev Recd Date: 2021-05-15
Publish Date: 2021-11-20

Abstract

Abstract

Exposure to intense noise can damage cochlear hair cells, leading to hearing loss in mammals. To avoid this constraint, most mammals have evolved in relatively quiet environments. Echolocating bats, however, are naturally exposed to continuous intense sounds from their own and neighboring sonar emissions for maintaining sonar directionality and range. Here, we propose the presence of intense noise resistance in cochlear hair cells of echolocating bats against noise-induced hearing loss (NIHL). To test this hypothesis, we performed noise exposure experiments for laboratory mice, one nonecholocating bat species, and five echolocating bat species. Contrary to nonecholocating fruit bats and mice, the hearing and the cochlear hair cells of echolocating bats remained unimpaired after continuous intense noise exposure. The comparative analyses of cochleae transcriptomic data showed that several genes protecting cochlear hair cells from intense sounds were overexpressed in echolocating bats. Particularly, the experimental examinations revealed that ISL1 overexpression significantly improved the survival of cochlear hair cells. Our findings support the existence of protective effects in cochlear hair cells of echolocating bats against intense noises, which provides new insight into understanding the relationship between cochlear hair cells and intense noises, and preventing or ameliorating NIHL in mammals.
- Echolocation,
- ISL1,
- Noise protection,
- Bats,
- Hair cells

These authors contributed equally to this work.

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References(68)

References

Amichai, E., Blumrosen, G., Yovel, Y., 2015. Calling louder and longer:how bats use biosonar under severe acoustic interference from other bats. Proc. Biol. Sci. 282, 20152064.

Barabasi, A.L., Oltvai, Z.N., 2004. Network biology:understanding the cell's functional organization. Nat. Rev. Genet. 5, 101-113.

Bermingham, N.A., Hassan, B.A., Price, S.D., Vollrath, M.A., Ben-Arie, N., Eatock, R.A., Bellen, H.J., Lysakowski, A., Zoghbi, H.Y., 1999. Math1:an essential gene for the generation of inner ear hair cells. Science 284, 1837-1841.

Davies, K.T., Cotton, J.A., Kirwan, J.D., Teeling, E.C., Rossiter, S.J., 2011. Parallel signatures of sequence evolution among hearing genes in echolocating mammals:an emerging model of genetic convergence. Heredity (Edinb) 108, 480-489.

Dechmann, D.K., Kranstauber, B., Gibbs, D., Wikelski, M., 2010. Group hunting-a reason for sociality in molossid bats? PLoS One 5, e9012.

Dong, C., Davis, R.J., Flavell, R.A., 2002. Map kinases in the immune response. Annu. Rev. Immunol. 20, 55-72.

Esterberg, R., Hailey, D.W., Rubel, E.W., Raible, D.W., 2014. ER-mitochondrial calcium flow underlies vulnerability of mechanosensory hair cells to damage. J. Neurosci. 34, 9703-9719.

Fay, R.R., 1988. Hearing in Vertebrates:A Psychophysics Databook. Ear and Hearing, 9, 359.

Fetoni, A.R., De Bartolo, P., Eramo, S.L., 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.

Fujioka, M., Okano, H., Edge, A.S., 2015. Manipulating cell fate in the cochlea:a feasible therapy for hearing loss. Trends Neurosci. 38, 139-144.

Haas, B.J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P.D., Bowden, J., Couger, M.B., Eccles, D., Li, B., Lieber, M., et al., 2013. De novo transcript sequence reconstruction from RNA-seq using the trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494-1512.

Han, F., Yu, H., Zheng, T., Ma, X., Zhao, X., Li, P., Le, L., Su, Y., Zheng, Q.Y., 2013. Otoprotective effects of erythropoietin on Cdh23^erl/erl mice. Neuroscience 237, 1-6.

Harding, G.W., Bohne, B.A., 2004. Noise-induced hair-cell loss and total exposure energy:analysis of a large data set. J. Acoust. Soc. Am. 115, 2207-2220.

Harding, G.W., Bohne, B.A., Ahmad, M., 2002. DPOAE level shifts and ABR threshold shifts compared to detailed analysis of histopathological damage from noise. Hear. Res. 174, 158-171.

Holderied, M.W., Korine, C., Fenton, M.B., Parsons, S., Robson, S., Jones, G., 2005. Echolocation call intensity in the aerial hawking bat Eptesicus bottae (Vespertilionidae) studied using stereo videogrammetry. J. Exp. Biol. 208, 1321-1327.

Huang, M., Kantardzhieva, A., Scheffer, D., Liberman, M.C., Chen, Z.Y., 2013. Hair cell overexpression of Islet1 reduces age-related and noise-induced hearing loss. J. Neurosci. 33, 15086-15094.

Huang, T., Santarelli, R., Starr, A., 2009. Mutation of OPA1 gene causes deafness by affecting function of auditory nerve terminals. Brain Res. 1300, 97-104.

Huth, M.E., Ricci, A.J., Cheng, A.G., 2011. Mechanisms of aminoglycoside ototoxicity and targets of hair cell protection. Int. J. Otolaryngol. 2011, 937861.

Jakobsen, L., Brinklov, S., Surlykke, A., 2013. Intensity and directionality of bat echolocation signals. Front. Physiol. 4, 89.

Jamesdaniel, S., Hu, B., Kermany, M.H., Jiang, H., Ding, D., Coling, D., Salvi, R., 2011. Noise induced changes in the expression of p38/MAPK signaling proteins in the sensory epithelium of the inner ear. J. Proteomics 75, 410-424.

Jen, P.H., Suga, N., 1976. Coordinated activities of middle-ear and laryngeal muscles in echolocating bats. Science 191, 950-952.

Jones, G., Teeling, E.C., 2006. The evolution of echolocation in bats. Trends Ecol. Evol. 21, 149-156.

Keithley, E.M., Wang, X., Barkdull, G.C., 2008. Tumor necrosis factor a can induce recruitment of inflammatory cells to the cochlea. Otol. Neurotol. 29, 854-859.

Kopke, R.D., Coleman, J.K., Liu, J., Campbell, K.C., Riffenburgh, R.H., 2002. Candidate's thesis:enhancing intrinsic cochlear stress defenses to reduce noiseinduced hearing loss. Laryngoscope 112, 1515-1532.

Kozel, P.J., Davis, R.R., Krieg, E.F., Shull, G.E., Erway, L.C., 2002. Deficiency in plasma membrane calcium ATPase isoform 2 increases susceptibility to noiseinduced hearing loss in mice. Hear. Res. 164, 231-239.

Kuperman, W.A., Roux, P., 2007. Underwater acoustics. In:Rossing, T.D. (Ed.), Springer Handbook of Acoustics. Springer, New York, pp. 149-204.

Kurabi, A., Keithley, E.M., Housley, G.D., Ryan, A.F., Wong, A.C., 2017. Cellular mechanisms of noise-induced hearing loss. Hear. Res. 349, 129-137.

Li, B., Dewey, C.N., 2011. RSEM:accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinf. 12, 323.

Li, Y., Liu, H., Giffen, K.P., Chen, L., Beisel, K.W., He, D.Z.Z., 2018. Transcriptomes of cochlear inner and outer hair cells from adult mice. Sci. Data 5, 180199.

Li, Y., Liu, Z., Shi, P., Zhang, J., 2010. The hearing gene prestin unites echolocating bats and whales. Curr. Biol. 20, R55-R56.

Li, S., Price, S.M., Cahill, H., Ryugo, D.K., Shen, M.M., Xiang, M., 2002. Hearing loss caused by progressive degeneration of cochlear hair cells in mice deficient for the Barhl1 homeobox gene. Development 129, 3523-3532.

Liu, H., Chen, L., Giffen, K.P., Stringham, S.T., Li, Y., Judge, P.D., Beisel, K.W., He, D.Z.Z., 2018a. Cell-specific transcriptome analysis shows that adult pillar and deiters' cells express genes encoding machinery for specializations of cochlear hair cells. Front. Mol. Neurosci. 11, 356.

Liu, Y., Cotton, J.A., Shen, B., Han, X., Rossiter, S.J., Zhang, S., 2010. Convergent sequence evolution between echolocating bats and dolphins. Curr. Biol. 20, R53-R54.

Liu, Z., Li, S., Wang, W., Xu, D., Murphy, R.W., Shi, P., 2011. Parallel evolution of KCNQ4 in echolocating bats. PLoS One 6, e26618.

Liu, Z., Qi, F.Y., Xu, D.M., Zhou, X., Shi, P., 2018b. Genomic and functional evidence reveals molecular insights into the origin of echolocation in whales. Sci. Adv. 4, eaat8821.

Liu, Z., Qi, F.Y., Zhou, X., Ren, H.Q., Shi, P., 2014. Parallel sites implicate functional convergence of the hearing gene prestin among echolocating mammals. Mol. Biol. Evol. 31, 2415-2424.

Lowenheim, H., Furness, D.N., Kil, J., Zinn, C., Gultig, K., Fero, M.L., Frost, D., Gummer, A.W., Roberts, J.M., Rubel, E.W., et al., 1999. Gene disruption of p27_Kip1 allows cell proliferation in the postnatal and adult organ of corti. Proc. Natl. Acad. Sci. U. S. A. 96, 4084-4088.

Maeda, Y., Fukushima, K., Omichi, R., Kariya, S., Nishizaki, K., 2013. Time courses of changes in phospho- and total- MAP kinases in the cochlea after intense noise exposure. PLoS One 8, e58775.

Mariappan, S., Bogdanowicz, W., Marimuthu, G., Rajan, K.E., 2013. Distress calls of the greater short-nosed fruit bat cynopterus sphinx activate hypothalamic-pituitary-adrenal (HPA) axis in conspecifics. J. Comp. Physiol. 199, 775-783.

Mizutari, K., Fujioka, M., Hosoya, M., Bramhall, N., Okano, H.J., Okano, H., Edge, A.S., 2013. Notch inhibition induces cochlear hair cell regeneration and recovery of hearing after acoustic trauma. Neuron 77, 58-69.

Montojo, J., Zuberi, K., Rodriguez, H., Kazi, F., Wright, G., Donaldson, S.L., Morris, Q., Bader, G.D., 2010. Genemania cytoscape plugin:fast gene function predictions on the desktop. Bioinformatics 26, 2927-2928.

Nachtigall, P.E., Schuller, G., 2014. Hearing during echolocation in whales and bats. In:Surlykke, A., Nachtigall, P.E., Fay, R.R., Popper, A.N. (Eds.), Biosonar, 51, pp. 143-168.

Nelson, J.E., 2000. Vocal communication in Australian Flying foxes (Pteropodidae; Megachiroptera). Ethology 21, 857-870.

Nordmann, A.S., Bohne, B.A., Harding, G.W., 2000. Histopathological differences between temporary and permanent threshold shift. Hear. Res. 139, 13-30.

Noren, D.P., Holt, M.M., Dunkin, R.C., Williams, T.M., 2017. Echolocation is cheap for some mammals:dolphins conserve oxygen while producing high-intensity clicks. J. Exp. Mar. Biol. Ecol. 495, 103-109.

Nouvian, R., Ruel, J., Wang, J., Guitton, M.J., Pujol, R., Puel, J.L., 2003. Degeneration of sensory outer hair cells following pharmacological blockade of cochlear KCNQ channels in the adult Guinea pig. Eur. J. Neurosci. 17, 2553-2562.

Ohinata, Y., Miller, J.M., Altschuler, R.A., Schacht, J., 2000. Intense noise induces formation of vasoactive lipid peroxidation products in the cochlea. Brain Res. 878, 163-173.

Ollivier, F.J., Samuelson, D.A., Brooks, D.E., Lewis, P.A., Kallberg, M.E., Komaromy, A.M., 2004. Comparative morphology of the tapetum lucidum (among selected species). Vet. Ophthalmol. 7, 11-22.

Omotehara, Y., Hakuba, N., Hato, N., Okada, M., Gyo, K., 2011. Protection against ischemic cochlear damage by intratympanic administration of AM-111. Otol. Neurotol. 32, 1422-1427.

Parker, J., Tsagkogeorga, G., Cotton, J.A., Liu, Y., Provero, P., Stupka, E., Rossiter, S.J., 2013. Genome-wide signatures of convergent evolution in echolocating mammals. Nature 502, 228-231.

Patel, M., Hu, Z., Bard, J., Jamison, J., Cai, Q., Hu, B.H., 2013. Transcriptome characterization by RNA-seq reveals the involvement of the complement components in noise-traumatized rat cochleae. Neuroscience 248, 1-16.

Ponnath, A., Depreux, F.F., Jodelka, F.M., Rigo, F., Farris, H.E., Hastings, M.L., Lentz, J.J., 2018. Rescue of outer hair cells with antisense oligonucleotides in usher mice is dependent on age of treatment. J. Assoc. Res. Otolaryngol. 19, 1-16.

Rubel, E.W., Furrer, S.A., Stone, J.S., 2013. A brief history of hair cell regeneration research and speculations on the future. Hear. Res. 297, 42-51.

Shen, Y.Y., Liang, L., Li, G.S., Murphy, R.W., Zhang, Y.P., 2012. Parallel evolution of auditory genes for echolocation in bats and toothed whales. PLoS Genet. 8, e1002788.

Simmons, A.M., Boku, S., Riquimaroux, H., Simmons, J.A., 2015. Auditory brainstem responses of Japanese house bats (Pipistrellus abramus) after exposure to broadband ultrasonic noise. J. Acoust. Soc. Am. 138, 2430-2437.

Simmons, A.M., Hom, K.N., Warnecke, M., Simmons, J.A., 2016. Broadband noise exposure does not affect hearing sensitivity in big brown bats (Eptesicus fuscus). J. Exp. Biol. 219, 1031-1040.

Suga, N., Jen, P.H., 1975. Peripheral control of acoustic signals in the auditory system of echolocating bats. J. Exp. Biol. 62, 277-311.

Tamura, A., Matsunobu, T., Tamura, R., Kawauchi, S., Sato, S., Shiotani, A., 2016. Photobiomodulation rescues the cochlea from noise-induced hearing loss via upregulating nuclear factor kappab expression in rats. Brain Res. 1646, 467-474.

Thomas, D.W., 1984. Fruit intake and energy budgets of frugivorous bats. Physiol. Zool. 57, 457-467.

Tornabene, S.V., Sato, K., Pham, L., Billings, P., Keithley, E.M., 2006. Immune cell recruitment following acoustic trauma. Hear. Res. 222, 115-124.

Van Campen, L.E., Murphy, W.J., Franks, J.R., Mathias, P.I., Toraason, M.A., 2002. Oxidative DNA damage is associated with intense noise exposure in the rat. Hear. Res. 164, 29-38.

Vital-Lopez, F.G., Memisevic, V., Dutta, B., 2012. Tutorial on biological networks. Wires. Data Min. Knowl. 2, 298-325.

Wagner, E.L., Shin, J.B., 2019. Mechanisms of hair cell damage and repair. Trends Neurosci. 42, 414-424.

Waldhaus, J., Durruthy-Durruthy, R., Heller, S., 2015. Quantitative high-resolution cellular map of the organ of corti. Cell Rep. 11, 1385-1399.

Wang, J., Ruel, J., Ladrech, S., Bonny, C., van de Water, T.R., Puel, J.L., 2007. Inhibition of the c-Jun N-terminal kinase-mediated mitochondrial cell death pathway restores auditory function in sound-exposed animals. Mol. Pharmacol. 71, 654-666.

Wang, J., Tymczyszyn, N., Yu, Z., Yin, S., Bance, M., Robertson, G.S., 2011. Overexpression of X-linked inhibitor of apoptosis protein protects against noiseinduced hearing loss in mice. Gene Ther. 18, 560-568.

Yamashita, T., Zheng, F., Finkelstein, D., Kellard, Z., Carter, R., Rosencrance, C.D., Sugino, K., Easton, J., Gawad, C., Zuo, J., 2018. High-resolution transcriptional dissection of in vivo Atoh1-mediated hair cell conversion in mature cochleae identifies Isl1 as a co-reprogramming factor. PLoS Genet. 14, e1007552.

Yang, S., Cai, Q., Bard, J., Jamison, J., Wang, J., Yang, W., Hu, B.H., 2015. Variation analysis of transcriptome changes reveals cochlear genes and their associated functions in cochlear susceptibility to acoustic overstimulation. Hear. Res. 330, 78-89.

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