Advertisement

Archives of Toxicology

, Volume 93, Issue 11, pp 3219–3228 | Cite as

Heat shock protein 70 is a key molecule to rescue imbalance caused by low-frequency noise

  • Reina Negishi-Oshino
  • Nobutaka Ohgami
  • Tingchao He
  • Xiang Li
  • Masashi Kato
  • Masayoshi Kobayashi
  • Yishuo Gu
  • Kanako Komuro
  • Charalampos E. Angelidis
  • Masashi KatoEmail author
Molecular Toxicology

Abstract

A previous study showed that people living in urban areas are generally exposed to low-frequency noise (LFN) with frequencies below 100 Hz and sound levels of 60–110 dB in daily and occupational environments. Exposure to LFN has been shown to affect balance in humans and mice. However, there is no information about prevention of LFN-mediated imbalance because of a lack of information about the target region based on health risk assessment of LFN exposure. Here, we show that acute exposure to LFN at 100 Hz, 95 dB, but not at 85 dB or 90 dB, for only 1 h caused imbalance in mice. The exposed mice also had decreased cervical vestibular-evoked myogenic potential (cVEMP) with impaired activity of vestibular hair cells. Since imbalance in the exposed mice was irreversible, morphological damage in the vestibules of the exposed mice was further examined. The exposed mice had breakage of the otoconial membrane in the vestibule. LFN-mediated imbalance and breakage of the otoconial membrane in mice were rescued by overexpression of a stress-reactive molecular chaperone, heat shock protein 70 (Hsp70), which has been shown to be induced by exposure of mice to 12 h per day of LFN at 95 dB for 5 days. Taken together, the results of this study demonstrate that acute exposure to LFN at 100 Hz, 95 dB for only 1 h caused irreversible imbalance in mice with structural damage of the otoconial membrane as the target region for LFN-mediated imbalance, which can be rescued by Hsp70.

Keywords

HSP70 Low-frequency noise Otoconial membrane cVEMP Balance 

Notes

Acknowledgements

This study was supported in part by Grants-in-Aid for Scientific Research on Innovative Areas (16H01639 and 18H04975), Scientific Research (A) (15H01743, 15H02588, and 19H01147), (B) (17KT0033) and (C) (25460178, 16K08343, and 17K09156) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Mirai-Program Small Start Type from the Japan Science and Technology Agency (JST), DAIKO FOUNDATION, Kobayashi International Scholarship Foundation and AEON Environmental Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Compliance with ethical standards

Conflict of interest

All authors declare to have no actual or potential conflicts of interest.

Supplementary material

204_2019_2587_MOESM1_ESM.pdf (5.6 mb)
Supplementary material 1 (PDF 5729 kb)

References

  1. Agrawal Y, Carey JP, Della-Santina CC, Schubert MC, Minor LB (2009) Disorders of balance and vestibular function in US adults: data from the National Health and Nutrition Examination Survey, 2001–2004. Arch Intern Med 169(10):938–944.  https://doi.org/10.1001/archinternmed.2009.66 (PMID: 19468085)CrossRefPubMedGoogle Scholar
  2. Berglund B, Hassmén P (1996) Sources and effects of low-frequency noise. J Acoust Soc Am 99(5):2985–3002.  https://doi.org/10.1121/1.414863 (PMID: 8642114)CrossRefPubMedGoogle Scholar
  3. Bisdorff A, Bosser G, Gueguen R, Perrin P (2013) The epidemiology of vertigo, dizziness, and unsteadiness and its links to co-morbidities. Front Neurol 4:29.  https://doi.org/10.3389/fneur.2013.00029 (PMID: 23526567)CrossRefPubMedPubMedCentralGoogle Scholar
  4. Evans MJ, Tempest W (1972) Some effects of infrasonic noise in transportation. J Sound Vib 22(1):19–24.  https://doi.org/10.1016/0022-460X(72)90840-1 CrossRefGoogle Scholar
  5. Halmagyi GM, Colebatch JG, Curthoys IS (1994) New tests of vestibular function. Baillieres Clin Neurol 3:485–500 (PMID: 7874404)PubMedGoogle Scholar
  6. Harrison RV (2015) On the biological plausibility of Wind Turbine syndrome. Int J Environ Health Res 25(5):463–468.  https://doi.org/10.1080/09603123.2014.963034 (PMID: 25295915)CrossRefPubMedGoogle Scholar
  7. Hasson T, Gillespie PG, Garcia JA, MacDonald RB, Zhao Y, Yee AG, Mooseker MS, Corey DP (1997) Unconventional myosins in inner-ear sensory epithelia. J Cell Biol 137(6):1287–1307 (PMID: 9182663)CrossRefGoogle Scholar
  8. Huang M, Sage C, Li H, Xiang M, Heller S, Chen ZY (2008) Diverse expression patterns of LIM-homeodomain transcription factors (LIM-HDs) in mammalian inner ear development. Dev Dyn 237(11):3305–3312.  https://doi.org/10.1002/dvdy.21735 (PMID: 18942141)CrossRefPubMedPubMedCentralGoogle Scholar
  9. Kawashima Y, Géléoc GS, Kurima K, Labay V, Lelli A, Asai Y, Makishima T, Wu DK, Della Santina CC, Holt JR, Griffith AJ (2011) Mechanotransduction in mouse inner ear hair cells requires transmembrane channel-like genes. J Clin Invest 121(12):4796–4809.  https://doi.org/10.1172/JCI60405 (PMID: 22105175)CrossRefPubMedPubMedCentralGoogle Scholar
  10. Lambert FM, Bras H, Cardoit L, Vinay L, Coulon P, Glover JC (2016) Early postnatal maturation in vestibulospinal pathways involved in neck and forelimb motor control. Dev Neurobiol 76(10):1061–1077.  https://doi.org/10.1002/dneu.22375 (PMID: 26724676)CrossRefPubMedGoogle Scholar
  11. Lanneau D, Wettstein G, Bonniaud P, Garrido C (2010) Heat shock proteins: cell protection through protein triage. Sci World J 10:1543.  https://doi.org/10.1100/tsw.2010.152 (PMID: 20694452)CrossRefGoogle Scholar
  12. Lundberg YW, Xu Y, Thiessen KD, Kramer KL (2015) Mechanisms of otoconia and otolith development. Dev Dyn 244(3):239–253.  https://doi.org/10.1002/dvdy.24195 (PMID: 25255879)CrossRefPubMedGoogle Scholar
  13. Matsuda M, Hoshino T, Yamakawa N, Tahara K, Adachi H, Sobue G, Maji D, Ihn H, Mizushima T (2013) Suppression of UV-induced wrinkle formation by induction of HSP70 expression in mice. J Invest Dermatol 133(4):919–928.  https://doi.org/10.1038/jid.2012.383 (PMID: 23096703)CrossRefPubMedGoogle Scholar
  14. 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(8):3577–3587.  https://doi.org/10.1172/JCI68480 (PMID: 23863716)CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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):40–51 (PMID: 14715148)CrossRefGoogle Scholar
  16. Mimura K, Watanabe K, Okawa S, Kobayashi M, Miyakawa O (2004) Morphological and chemical characterizations of the interface of a hydroxyapatite-coated implant. Dent Mater J 23(3):353–360 (PMID: 15510865)CrossRefGoogle Scholar
  17. Miyakawa O, Okawa S, Kobayashi M (2006) Abrading increases oxygen and hardness of titanium surface. Dent Mater J 25(1):13–19 (PMID: 16706291)CrossRefGoogle Scholar
  18. Mohr GC, Cole JN, von Guild E, Gierke HE (1965) Effects of low frequency and infrasonic noises on man. Aero Med 36:817–827Google Scholar
  19. Murofushi T (2016) Clinical application of vestibular evoked myogenic potential (VEMP). Auris Nasus Larynx 43(4):367–376.  https://doi.org/10.1016/j.anl.2015.12.006 (PMID: 26791591)CrossRefPubMedGoogle Scholar
  20. Negishi-Oshino R, Ohgami N, He T, Ohgami K, Li X, Kato M (2019) cVEMP correlated with imbalance in a mouse model of vestibular disorder. Environ Health Prev Med 24(1):39.  https://doi.org/10.1186/s12199-019-0794-8 (PMID: 31153359)CrossRefPubMedPubMedCentralGoogle Scholar
  21. Neuhauser HK, von Brevern M, Radtke A, Lezius F, Feldmann M, Ziese T, Lempert T (2005) Epidemiology of vestibular vertigo: a neurotologic survey of the general population. Neurology 65(6):898–904.  https://doi.org/10.1212/01.wnl.0000175987.59991.3d (PMID: 16186531)CrossRefPubMedGoogle Scholar
  22. Ninomiya H, Ohgami N, Oshino R, Kato M, Ohgami K, Li X, Shen D, Iida M, Yajima I, Angelidis CE, Adachi H, Katsuno M, Sobue G, Kato M (2018) Increased expression level of Hsp70 in the inner ears of mice by exposure to low frequency noise. Hear Res 363:49–54.  https://doi.org/10.1016/j.heares.2018.02.006 (PMID: 16186531)CrossRefPubMedGoogle Scholar
  23. Ohgami N, Ida-Eto M, Shimotake T, Sakashita N, Sone M, Nakashima T, Tabuchi K, Hoshino T, Shimada A, Tsuzuki T, Yamamoto M, Sobue G, Jijiwa M, Asai N, Hara A, Takahashi M, Kato M (2010) c-Ret-mediated hearing loss in mice with Hirschsprung disease. Proc Natl Acad Sci USA 107(29):13051–13056.  https://doi.org/10.1073/pnas.1004520107 CrossRefPubMedGoogle Scholar
  24. Ohgami N, Ida-Eto M, Sakashita N, Sone M, Nakashima T, Tabuchi K, Hoshino T, Shimada A, Tsuzuki T, Yamamoto M, Sobue G, Jijiwa M, Asai N, Hara A, Takahashi M, Kato M (2012) Partial impairment of c-Ret at tyrosine 1062 accelerates age-related hearing loss in mice. Neurobiol Aging 33(3):626.e25–626.e34.  https://doi.org/10.1016/j.neurobiolaging.2011.04.002 CrossRefGoogle Scholar
  25. Ohgami N, Oshino R, Ninomiya H, Li X, Kato M, Yajima I, Kato M (2017) Risk Assessment of Neonatal Exposure to Low Frequency Noise Based on Balance in Mice. Front Behav Neurosci 22:11–30.  https://doi.org/10.3389/fnbeh.2017.00030 (PMID: 28275341)CrossRefGoogle Scholar
  26. Plumier JC, Ross BM, Currie RW, Angelidis CE, Kazlaris H, Kollias G, Pagoulatos GN (1995) Transgenic mice expressing the human heat shock protein 70 have improved post-ischemic myocardial recovery. J Clin Invest 95(4):1854–1860.  https://doi.org/10.1172/JCI117865 (PMID: 7706492)CrossRefPubMedPubMedCentralGoogle Scholar
  27. Pujol R, Pickett SB, Nguyen TB, Stone JS (2014) Large basolateral processes on type II hair cells comprise a novel processing unit in mammalian vestibular organs. J Comp Neurol 522(14):3141–3159.  https://doi.org/10.1002/cne.23625 (PMID: 24825750)CrossRefPubMedPubMedCentralGoogle Scholar
  28. Safiulina D, Peet N, Seppet E, Zharkovsky A, Kaasik A (2006) Dehydroepiandrosterone inhibits complex I of the mitochondrial respiratory chain and is neurotoxic in vitro and in vivo at high concentrations. Toxicol Sci 93(2):348–356.  https://doi.org/10.1093/toxsci/kfl064 (PMID: 16849397)CrossRefPubMedGoogle Scholar
  29. Sakakura K, Miyashita M, Chikamatsu K, Takahashi K, Furuya N (2003) Tone burst-evoked myogenic potentials in rat neck extensor and flexor muscles. Hear Res 185:57–64 (PMID: 14599693)CrossRefGoogle Scholar
  30. Salt AN, DeMott JE (1999) Longitudinal endolymph movements and endocochlear potential changes induced by stimulation at infrasonic frequencies. J Acoust Soc Am 106(2):847–856.  https://doi.org/10.1121/1.427101 (PMID: 10462790)CrossRefPubMedGoogle Scholar
  31. Sheykholeslami K, Megerian CA, Zheng QY (2009) Vestibular evoked myogenic potentials in normal mice and Phex mice with spontaneous endolymphatic hydrops. Otol Neurotol 30(4):535–544.  https://doi.org/10.1097/MAO.0b013e31819bda13 (PMID: 19300299)CrossRefPubMedPubMedCentralGoogle Scholar
  32. Shimizu K, Murofushi T, Sakurai M, Halmagyi M (2000) Vestibular evoked myogenic potentials in multiple sclerosis. J Neurol Neurosurg Psychiatr 69(2):276–277 (PMID: 10960289)CrossRefGoogle Scholar
  33. Shojaku H, Zang RL, Tsubota M, Fujisaka M, Hori E, Nishijo H, Watanabe Y (2007) Effects of selective cochlear toxicity and vestibular deafferentation on vestibular evoked myogenic potentials in guinea pigs. Acta Otolaryngol 127(4):430–435.  https://doi.org/10.1080/00016480600895136 CrossRefPubMedGoogle Scholar
  34. Simmler MC, Cohen-Salmon M, El-Amraoui A, Guillaud L, Benichou JC, Petit C, Panthier JJ (2000) Targeted disruption of otog results in deafness and severe imbalance. Nat Genet 24(2):139–143.  https://doi.org/10.1038/72793 (PMID: 10655058)CrossRefPubMedGoogle Scholar
  35. Sreenivasan A, Sivaraman G, Parida PK, Alexander A, Saxena SK, Suria G (2015) The clinical utility of vestibular evoked myogenic potentials in patients of benign paroxysmal positional vertigo. J Clin Diagn Res 9(6):1–3.  https://doi.org/10.7860/JCDR/2015/9953.6058 (PMID: 26266140)CrossRefGoogle Scholar
  36. Takigawa H, Hayashi F, Sugiura S, Sakamoto H (1988) Effects of infrasound on human body sway. J Low Freq Noise Vib 7:66–73 (PMID: 3726296)CrossRefGoogle Scholar
  37. Tamura H, Ohgami N, Yajima I, Iida M, Ohgami K, Fujii N, Itabe H, Kusudo T, Yamashita H, Kato M (2012) Chronic exposure to low frequency noise at moderate levels causes impaired balance in mice. PLoS One 7(6):e39807.  https://doi.org/10.1371/journal.pone.0039807 (PMID: 22768129)CrossRefPubMedPubMedCentralGoogle Scholar
  38. Yang TH, Young YH (2005) Click-evoked myogenic potentials recorded on alert guinea pigs. Hear Res 205:277–283.  https://doi.org/10.1016/j.heares.2005.03.029 (PMID: 15953537)CrossRefPubMedGoogle Scholar
  39. Yazawa I, Giasson BI, Sasaki R, Zhang B, Joyce S, Uryu K, Trojanowski JQ, Lee VM (2005) Mouse model of multiple system atrophy alpha-synuclein expression in oligodendrocytes causes glial and neuronal degeneration. Neuron 45(6):847–859.  https://doi.org/10.1016/j.neuron.2005.01.032 (PMID: 15797547)CrossRefPubMedGoogle Scholar
  40. Zhao X, Jones SM, Thoreson WB, Lundberg YW (2008a) Osteopontin is not critical for otoconia formation or balance function. J Assoc Res Otolaryngol 9(2):191–201.  https://doi.org/10.1007/s10162-008-0117-z( PMID: 18459000)CrossRefPubMedPubMedCentralGoogle Scholar
  41. Zhao X, Jones SM, Yamoah EN, Lundberg YW (2008b) Otoconin-90 deletion leads to imbalance but normal hearing: a comparison with other otoconia mutants. Neuroscience 153(1):289–299.  https://doi.org/10.1016/j.neuroscience.2008.01.055 (PMID: 18355969)CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Reina Negishi-Oshino
    • 1
  • Nobutaka Ohgami
    • 1
  • Tingchao He
    • 1
  • Xiang Li
    • 1
  • Masashi Kato
    • 2
  • Masayoshi Kobayashi
    • 3
  • Yishuo Gu
    • 1
  • Kanako Komuro
    • 1
  • Charalampos E. Angelidis
    • 4
  • Masashi Kato
    • 1
    Email author
  1. 1.Department of Occupational and Environmental HealthNagoya University Graduate School of MedicineNagoyaJapan
  2. 2.Department of Electrical and Mechanical EngineeringNagoya Institute of TechnologyNagoyaJapan
  3. 3.EPMA LaboratoryNiigata University Center for Instrumental AnalysisNiigataJapan
  4. 4.General Biology, Medical SchoolUniversity of IoanninaIoanninaGreece

Personalised recommendations