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

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.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

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)

    Article  PubMed  Google 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)

    CAS  Article  PubMed  Google 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)

    Article  PubMed  PubMed Central  Google 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

    Article  Google Scholar 

  5. Halmagyi GM, Colebatch JG, Curthoys IS (1994) New tests of vestibular function. Baillieres Clin Neurol 3:485–500 (PMID: 7874404)

    CAS  PubMed  Google 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)

    Article  PubMed  Google 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)

    CAS  Article  Google 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)

    CAS  Article  PubMed  PubMed Central  Google 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)

    CAS  Article  PubMed  PubMed Central  Google 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)

    CAS  Article  PubMed  Google 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)

    CAS  Article  Google 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)

    Article  PubMed  Google 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)

    CAS  Article  PubMed  Google 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)

    CAS  Article  PubMed  PubMed Central  Google 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)

    CAS  Article  Google 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)

    CAS  Article  Google 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)

    CAS  Article  Google Scholar 

  18. Mohr GC, Cole JN, von Guild E, Gierke HE (1965) Effects of low frequency and infrasonic noises on man. Aero Med 36:817–827

    CAS  Google 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)

    Article  PubMed  Google 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)

    CAS  Article  PubMed  PubMed Central  Google 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)

    CAS  Article  PubMed  Google 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)

    CAS  Article  PubMed  Google 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

    Article  PubMed  Google 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

    CAS  Article  Google 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)

    CAS  Article  Google 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)

    CAS  Article  PubMed  PubMed Central  Google 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)

    Article  PubMed  PubMed Central  Google 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)

    CAS  Article  PubMed  Google 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)

    Article  Google 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)

    CAS  Article  PubMed  Google 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)

    Article  PubMed  PubMed Central  Google 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)

    CAS  Article  Google 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

    Article  PubMed  Google 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)

    CAS  Article  PubMed  Google 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)

    Article  Google 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)

    Article  Google 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)

    CAS  Article  PubMed  PubMed Central  Google 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)

    Article  PubMed  Google 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)

    CAS  Article  PubMed  Google 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)

    Article  PubMed  PubMed Central  Google 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)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Masashi Kato.

Ethics declarations

Conflict of interest

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

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 5729 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Negishi-Oshino, R., Ohgami, N., He, T. et al. Heat shock protein 70 is a key molecule to rescue imbalance caused by low-frequency noise. Arch Toxicol 93, 3219–3228 (2019). https://doi.org/10.1007/s00204-019-02587-3

Download citation

Keywords

  • HSP70
  • Low-frequency noise
  • Otoconial membrane
  • cVEMP
  • Balance