Endolymph; Organotypic culture; Potassium; Rat; Styrene; Vestibular explants; Animals; Animals, Newborn; Endolymph/drug effects; Endolymph/metabolism; Female; Potassium/metabolism; Rats, Long-Evans; Saccule and Utricle/drug effects; Saccule and Utricle/metabolism; Saccule and Utricle/pathology; Styrene/toxicity; Saccule and Utricle; Toxicology; General Medicine
Abstract :
[en] Despite well-documented neurotoxic and ototoxic properties, styrene remains commonly used in industry. Its effects on the cochlea have been extensively studied in animals, and epidemiological and animal evidence indicates an impact on balance. However, its influence on the peripheral vestibular receptor has yet to be investigated. Here, we assessed the vestibulotoxicity of styrene using an in vitro model, consisting of three-dimensional cultured newborn rat utricles filled with a high‑potassium (K+) endolymph-like fluid, called "cysts". K+ entry in the cyst ("influx") and its exit ("efflux") are controlled by secretory cells and hair cells, respectively. The vestibular epithelium's functionality is thus linked to K+ concentration, measured using a microelectrode. Known inhibitors of K+ efflux and influx validated the model. Cysts were subsequently exposed to styrene (0.25; 0.5; 0.75 and 1 mM) for 2 h or 72 h. The decrease in K+ concentration measured after both exposure durations was dose-dependent, and significant from 0.75 mM styrene. Vacuoles were visible in the cytoplasm of epithelial cells from 0.5 mM after 2 h and from 0.25 mM after 72 h. The results presented here are the first evidence that styrene may deregulate K+ homeostasis in the endolymphatic space, thereby altering the functionality of the vestibular receptor.
Tallandier, Valentin ; Université de Liège - ULiège > GIGA > GIGA Neurosciences ; Institut National de Recherche et de Sécurité, Rue du Morvan, CS 60027, F-54519 Vandœuvre, Cedex, France, DevAH EA 3450 - Développement, Adaptation et Handicap, Régulations cardio-respiratoires et de la motricité-Université de Lorraine, F-54500 Vandœuvre, France
Merlen, L; Institut National de Recherche et de Sécurité, Rue du Morvan, CS 60027, F-54519 Vandœuvre, Cedex, France
Boucard, S; Institut National de Recherche et de Sécurité, Rue du Morvan, CS 60027, F-54519 Vandœuvre, Cedex, France
Thomas, A; Institut National de Recherche et de Sécurité, Rue du Morvan, CS 60027, F-54519 Vandœuvre, Cedex, France
Venet, T; Institut National de Recherche et de Sécurité, Rue du Morvan, CS 60027, F-54519 Vandœuvre, Cedex, France, DevAH EA 3450 - Développement, Adaptation et Handicap, Régulations cardio-respiratoires et de la motricité-Université de Lorraine, F-54500 Vandœuvre, France
Chalansonnet, M; Institut National de Recherche et de Sécurité, Rue du Morvan, CS 60027, F-54519 Vandœuvre, Cedex, France. Electronic address: monique.chalansonnet@inrs.fr
Gauchard, G; DevAH EA 3450 - Développement, Adaptation et Handicap, Régulations cardio-respiratoires et de la motricité-Université de Lorraine, F-54500 Vandœuvre, France
Campo, P; Institut National de Recherche et de Sécurité, Rue du Morvan, CS 60027, F-54519 Vandœuvre, Cedex, France, DevAH EA 3450 - Développement, Adaptation et Handicap, Régulations cardio-respiratoires et de la motricité-Université de Lorraine, F-54500 Vandœuvre, France
Pouyatos, B; Institut National de Recherche et de Sécurité, Rue du Morvan, CS 60027, F-54519 Vandœuvre, Cedex, France
Language :
English
Title :
Styrene alters potassium endolymphatic concentration in a model of cultured utricle explants.
Publication date :
September 2020
Journal title :
Toxicology in Vitro: an International Journal Published in Association with BIBRA
Anniko, M., Embryologic development in vivo and in vitro of the dark cell region of the mammalian crista ampullaris. Acta Otolaryngol. 90 (1980), 106–114, 10.3109/00016488009131705.
Anniko, M., Nordemar, H., Embryogenesis of the inner ear. IV. Post-natal maturation of the secretory epithelia of the inner ear in correlation with the elemental composition in the endolymphatic space. Arch Otorhinolaryngol 229 (1980), 281–288.
Bakand, S., Winder, C., Khalil, C., Hayes, A., Toxicity assessment of industrial chemicals and airborne contaminants: transition from in vivo to in vitro test methods: a review. Inhal. Toxicol. 17 (2005), 775–787, 10.1080/08958370500225240.
Bale, A.S., Smothers, C.T., Woodward, J.J., Inhibition of neuronal nicotinic acetylcholine receptors by the abused solvent, toluene. Br. J. Pharmacol. 137 (2002), 375–383, 10.1038/sj.bjp.0704874.
Bale, A.S., Meacham, C.A., Benignus, V.A., Bushnell, P.J., Shafer, T.J., Volatile organic compounds inhibit human and rat neuronal nicotinic acetylcholine receptors expressed in Xenopus oocytes. Toxicol. Appl. Pharmacol. 205 (2005), 77–88, 10.1016/j.taap.2004.09.011.
Bartolami, S., Gaboyard, S., Quentin, J., Travo, C., Cavalier, M., Barhanin, J., Chabbert, C., Critical roles of transitional cells and Na/K-ATPase in the formation of vestibular Endolymph. J. Neurosci. 31 (2011), 16541–16549, 10.1523/JNEUROSCI.2430-11.2011.
Bergamaschi, E., Smargiassi, A., Mutti, A., Cavazzini, S., Vettori, M.V., Alinovi, R., Franchini, I., Mergler, D., Peripheral markers of catecholaminergic dysfunction and symptoms of neurotoxicity among styrene-exposed workers. Int. Arch. Occup. Environ. Health 69 (1997), 209–214.
Calabrese, G., Martini, A., Sessa, G., Cellini, M., Bartolucci, G.B., Marcuzzo, G., De Rosa, E., Otoneurological study in workers exposed to styrene in the fiberglass industry. Int. Arch. Occup. Environ. Health 68 (1996), 219–223.
Calderón-Guzmán, D., Espitia-Vázquez, I., López-Domínguez, A., Hernández-García, E., Huerta-Gertrudis, B., Coballase-Urritia, E., Juárez-Olguín, H., García-Fernández, B., Effect of toluene and nutritional status on serotonin, lipid peroxidation levels and NA+/K+-ATPase in adult rat brain. Neurochem. Res. 30 (2005), 619–624, 10.1007/s11064-005-2749-2.
Calderón-Guzmán, D., Hernández-Islas, J.L., Espítia Vázquez, I.R., Barragán-Mejía, G., Hernández-García, E., Del Angel, D.S., Juárez-Olguín, H., Effect of toluene and cresols on Na+,K+-ATPase, and serotonin in rat brain. Regul. Toxicol. Pharmacol. 41 (2005), 1–5, 10.1016/j.yrtph.2004.09.005.
Callejo, A., Durochat, A., Bressieux, S., Saleur, A., Chabbert, C., Domènech Juan, I., Llorens, J., Gaboyard-Niay, S., Dose-dependent cochlear and vestibular toxicity of trans-tympanic cisplatin in the rat. NeuroToxicology 60 (2017), 1–9, 10.1016/j.neuro.2017.02.007.
Campo, P., Loquet, G., Blachère, V., Roure, M., Toluene and styrene intoxication route in the rat cochlea. Neurotoxicol. Teratol. 21 (1999), 427–434.
Campo, P., Lataye, R., Loquet, G., Bonnet, P., Styrene-induced hearing loss: a membrane insult. Hear. Res. 154 (2001), 170–180.
Casimiro, M.C., Knollmann, B.C., Ebert, S.N., Vary, J.C., Greene, A.E., Franz, M.R., Grinberg, A., Huang, S.P., Pfeifer, K., Targeted disruption of the Kcnq1 gene produces a mouse model of Jervell and Lange-Nielsen syndrome. Proc. Natl. Acad. Sci. U. S. A. 98 (2001), 2526–2531, 10.1073/pnas.041398998.
Chen, G.-D., Chi, L.-H., Kostyniak, P.J., Henderson, D., Styrene induced alterations in biomarkers of exposure and effects in the cochlea: mechanisms of hearing loss. Toxicol. Sci. 98 (2007), 167–177, 10.1093/toxsci/kfm078.
Ciuman, R.R., Stria vascularis and vestibular dark cells: characterisation of main structures responsible for inner-ear homeostasis, and their pathophysiological relations. J. Laryngol. Otol., 123, 2009, 151, 10.1017/S0022215108002624.
Croute, F., Poinsot, J., Gaubin, Y., Beau, B., Simon, V., Murat, J.C., Soleilhavoup, J.P., Volatile organic compounds cytotoxicity and expression of HSP72, HSP90 and GRP78 stress proteins in cultured human cells. Biochim. Biophys. Acta 1591 (2002), 147–155, 10.1016/s0167-4889(02)00271-9.
Cruz, S.L., Mirshahi, T., Thomas, B., Balster, R.L., Woodward, J.J., Effects of the abused solvent toluene on recombinant N-methyl-D-aspartate and non-N-methyl-D-aspartate receptors expressed in Xenopus oocytes. J. Pharmacol. Exp. Ther. 286 (1998), 334–340.
Cruz, S.L., Balster, R.L., Woodward, J.J., Effects of volatile solvents on recombinant N-methyl-D-aspartate receptors expressed in Xenopus oocytes. Br. J. Pharmacol. 131 (2000), 1303–1308, 10.1038/sj.bjp.0703666.
Dechesne, C., Mbiene, J.P., Sans, A., Postnatal development of vestibular receptor surfaces in the rat. Acta Otolaryngol. 101 (1986), 11–18, 10.3109/00016488609108602.
Diodovich, C., Bianchi, M.G., Bowe, G., Acquati, F., Taramelli, R., Parent-Massin, D., Gribaldo, L., Response of human cord blood cells to styrene exposure: evaluation of its effects on apoptosis and gene expression by genomic technology. Toxicology 200 (2004), 145–157, 10.1016/j.tox.2004.03.021.
Farhood, Z., Lambert, P.R., The physiologic role of corticosteroids in Ménière's disease. Am. J. Otolaryngol. 37 (2016), 455–458, 10.1016/j.amjoto.2016.04.004.
Fetoni, A.R., Rolesi, R., Paciello, F., Eramo, S.L.M., Grassi, C., Troiani, D., Paludetti, G., Styrene enhances the noise induced oxidative stress in the cochlea and affects differently mechanosensory and supporting cells. Free Radic. Biol. Med. 101 (2016), 211–225, 10.1016/j.freeradbiomed.2016.10.014.
Gaboyard, S., Chabbert, C., Travo, C., Bancel, F., Lehouelleur, J., Yamauchi, D., Marcus, D.C., Sans, A., Three-dimensional culture of newborn rat utricle using an extracellular matrix promotes formation of a cyst. Neuroscience 133 (2005), 253–265, 10.1016/j.neuroscience.2005.02.011.
Géléoc, G.S.G., Holt, J.R., Developmental acquisition of sensory transduction in hair cells of the mouse inner ear. Nat. Neurosci. 6 (2003), 1019–1020, 10.1038/nn1120.
Gnedeva, K., Jacobo, A., Salvi, J.D., Petelski, A.A., Hudspeth, A.J., Elastic force restricts growth of the murine utricle. Elife, 6, 2017, 10.7554/eLife.25681.
Gu, R., Montcouquiol, M., Marchionni, M., Corwin, J.T., Proliferative responses to growth factors decline rapidly during postnatal maturation of mammalian hair cell epithelia. Eur. J. Neurosci. 25 (2007), 1363–1372, 10.1111/j.1460-9568.2007.05414.x.
Harvilchuck, J.A., Carlson, G.P., Comparison of styrene and its metabolites styrene oxide and 4-vinylphenol on cytotoxicity and glutathione depletion in Clara cells of mice and rats. Toxicology 227 (2006), 165–172, 10.1016/j.tox.2006.08.001.
Harvilchuck, J.A., Pu, X., Klaunig, J.E., Carlson, G.P., Indicators of oxidative stress and apoptosis in mouse whole lung and Clara cells following exposure to styrene and its metabolites. Toxicology 264 (2009), 171–178, 10.1016/j.tox.2009.08.001.
Hibino, H., Kurachi, Y., Molecular and physiological bases of the K + circulation in the mammalian inner ear. Physiology 21 (2006), 336–345, 10.1152/physiol.00023.2006.
Hibino, H., Nin, F., Tsuzuki, C., Kurachi, Y., How is the highly positive endocochlear potential formed? The specific architecture of the stria vascularis and the roles of the ion-transport apparatus. Pflugers Arch. 459 (2010), 521–533, 10.1007/s00424-009-0754-z.
Hoet, P., Lison, D., Ototoxicity of toluene and styrene: state of current knowledge. Crit. Rev. Toxicol. 38 (2008), 127–170, 10.1080/10408440701845443.
Johnson, A.-C., Relationship between styrene exposure and hearing loss: review of human studies. Int. J. Occup. Med. Environ. Health 20 (2007), 315–325, 10.2478/v10001-007-0040-2.
Kim, H.J., Lee, J.O., Koo, J.W., Kim, J.-S., Ban, J., Gentamicin-induced bilateral vestibulopathy in rabbits: vestibular dysfunction and histopathology. Laryngoscope 123 (2013), E51–E58, 10.1002/lary.24106.
Kimitsuki, T., Nakagawa, T., Hisashi, K., Komune, S., Komiyama, S., Gadolinium blocks mechano-electric transducer current in chick cochlear hair cells. Hear. Res. 101 (1996), 75–80, 10.1016/S0378-5955(96)00134-7.
Kishi, R., Tozaki, S., Gong, Y.Y., Impairment of neurobehavioral function and color vision loss among workers exposed to low concentration of styrene–a review of literatures. Ind. Health 38 (2000), 120–126.
Kohn, J., Minotti, S., Durham, H., Assessment of the neurotoxicity of styrene, styrene oxide, and styrene glycol in primary cultures of motor and sensory neurons. Toxicol. Lett. 75 (1995), 29–37, 10.1016/0378-4274(94)03153-x.
Kroese, A.B., Das, A., Hudspeth, A.J., Blockage of the transduction channels of hair cells in the bullfrog's sacculus by aminoglycoside antibiotics. Hear. Res. 37 (1989), 203–217.
Larsby, B., Tham, R., Odkvist, L.M., Hydén, D., Bunnfors, I., Aschan, G., Exposure of rabbits to styrene. Electronystagmographic findings correlated to the styrene level in blood and cerebrospinal fluid. Scand. J. Work Environ. Health 4 (1978), 60–65.
Lataye, R., Campo, P., Barthelemy, C., Loquet, G., Bonnet, P., Cochlear pathology induced by styrene. Neurotoxicol. Teratol. 23 (2001), 71–79.
Lataye, R., Campo, P., Pouyatos, B., Cossec, B., Blachère, V., Morel, G., Solvent ototoxicity in the rat and Guinea pig. Neurotoxicol. Teratol. 25 (2003), 39–50.
Lebel, C.P., Schatz, R.A., Altered synaptosomal phospholipid metabolism after toluene: possible relationship with membrane fluidity, Na+,K(+)-adenosine triphosphatase and phospholipid methylation. J. Pharmacol. Exp. Ther. 253 (1990), 1189–1197.
Lin, H.J., Shaffer, K.M., Chang, Y.H., Barker, J.L., Pancrazio, J.J., Stenger, D.A., Ma, W., Acute exposure of toluene transiently potentiates p42/44 mitogen-activated protein kinase (MAPK) activity in cultured rat cortical astrocytes. Neurosci. Lett. 332 (2002), 103–106, 10.1016/s0304-3940(02)00930-8.
Llorens, J., Demêmes, D., Sans, A., The behavioral syndrome caused by 3,3′-iminodipropionitrile and related nitriles in the rat is associated with degeneration of the vestibular sensory hair cells. Toxicol. Appl. Pharmacol. 123 (1993), 199–210, 10.1006/taap.1993.1238.
Loquet, G., Campo, P., Lataye, R., Comparison of toluene-induced and styrene-induced hearing losses. Neurotoxicol. Teratol. 21 (1999), 689–697.
Maguin, K., Campo, P., Parietti-Winkler, C., Toluene can perturb the neuronal voltage-dependent Ca2+ channels involved in the middle-ear reflex. Toxicol. Sci. 107 (2009), 473–481, 10.1093/toxsci/kfn242.
Masetto, S., Zucca, G., Bottà, L., Valli, P., Endolymphatic potassium of the chicken vestibule during embryonic development. Int. J. Dev. Neurosci. 23 (2005), 439–448, 10.1016/j.ijdevneu.2005.05.002.
Mbiene, J.P., Favre, D., Sans, A., The pattern of ciliary development in fetal mouse vestibular receptors. A qualitative and quantitative SEM study. Anat. Embryol. 170 (1984), 229–238, 10.1007/bf00318726.
Merchant, S.N., Adams, J.C., Nadol, J.B., Pathophysiology of Meniere's syndrome: are symptoms caused by endolymphatic hydrops?. Otol. Neurotol. 26 (2005), 74–81.
Miller, R.R., Newhook, R., Poole, A., Styrene production, use, and human exposure. Crit. Rev. Toxicol. 24 (1994), S1–S10, 10.3109/10408449409020137.
Möller, C., Odkvist, L., Larsby, B., Tham, R., Ledin, T., Bergholtz, L., Otoneurological findings in workers exposed to styrene. Scand. J. Work Environ. Health 16 (1990), 189–194.
Nicolas, M., Demêmes, D., Martin, A., Kupershmidt, S., Barhanin, J., KCNQ1/KCNE1 potassium channels in mammalian vestibular dark cells. Hear. Res. 153 (2001), 132–145, 10.1016/s0378-5955(00)00268-9.
Nicolas, M.-T., Lesage, F., Reyes, R., Barhanin, J., Demêmes, D., Localization of TREK-1, a two-pore-domain K+ channel in the peripheral vestibular system of mouse and rat. Brain Res. 1017 (2004), 46–52, 10.1016/j.brainres.2004.05.012.
Niklasson, M., Tham, R., Larsby, B., Eriksson, B., Effects of toluene, styrene, trichloroethylene, and trichloroethane on the vestibulo-and opto-oculo motor system in rats. Neurotoxicol. Teratol. 15 (1993), 327–334.
Pleban, F.T., Oketope, O., Shrestha, L., Occupational styrene exposure on auditory function among adults: a systematic review of selected workers. Saf. Health Work 8 (2017), 329–336, 10.1016/j.shaw.2017.01.002.
Popper, P., Winkler, J., Erbe, C.B., Lerch-Gaggl, A., Siebeneich, W., Wackym, P.A., Distribution of two-pore-domain potassium channels in the adult rat vestibular periphery. Hear. Res. 246 (2008), 1–8, 10.1016/j.heares.2008.09.004.
Rogers, J.V., Siegel, G.L., Pollard, D.L., Rooney, A.D., McDougal, J.N., The cytotoxicity of volatile JP-8 jet fuel components in keratinocytes. Toxicology 197 (2004), 113–121, 10.1016/j.tox.2003.12.011.
Sarangapani, R., Teeguarden, J.G., Cruzan, G., Clewell, H.J., Andersen, M.E., Physiologically based pharmacokinetic modeling of styrene and styrene oxide respiratory-tract dosimetry in rodents and humans. Inhal. Toxicol. 14 (2002), 789–834, 10.1080/08958370290084647.
Shubin, A.V., Demidyuk, I.V., Komissarov, A.A., Rafieva, L.M., Kostrov, S.V., Cytoplasmic vacuolization in cell death and survival. Oncotarget 7 (2016), 55863–55889, 10.18632/oncotarget.10150.
Spicer, S.S., Schulte, B.A., Evidence for a medial K+ recycling pathway from inner hair cells. Hear. Res. 118 (1998), 1–12.
Toppila, E., Forsman, P., Pyykkö, I., Starck, J., Tossavainen, T., Uitti, J., Oksa, P., Effect of styrene on postural stability among reinforced plastic boat plant workers in Finland. J. Occup. Environ. Med. 48 (2006), 175–180, 10.1097/01.jom.0000199510.80882.7b.
Vaalavirta, L., Tähti, H., Astrocyte membrane Na+, K(+)-ATPase and mg(2+)-ATPase as targets of organic solvent impact. Life Sci. 57 (1995), 2223–2230, 10.1016/0024-3205(95)02214-4.
Vaalavirta, L., Tähti, H., Effects of selected organic solvents on the astrocyte membrane ATPase in vitro. Clin. Exp. Pharmacol. Physiol. 22 (1995), 293–294, 10.1111/j.1440-1681.1995.tb01999.x.
Vouriot, A., Hannhart, B., Gauchard, G.C., Barot, A., Ledin, T., Mur, J.-M., Perrin, P.P., Long-term exposure to solvents impairs vigilance and postural control in serigraphy workers. Int. Arch. Occup. Environ. Health 78 (2005), 510–515, 10.1007/s00420-005-0609-7.
Winbo, A., Rydberg, A., Vestibular dysfunction is a clinical feature of the Jervell and Lange-Nielsen syndrome. Scand. Cardiovasc. J. 49 (2015), 7–13, 10.3109/14017431.2014.988172.
Wubbels, R.J., de Jong, H., van Marle, J., Morphometric analysis of the vestibular sensory epithelia of young adult rat. J. Vestib. Res. 12 (2002), 145–154.
Yang, W.P., Hu, B.H., Chen, G.D., Bielefeld, E.C., Henderson, D., Protective effect of N-acetyl-L-cysteine (L-NAC) against styrene-induced cochlear injuries. Acta Otolaryngol. 129 (2009), 1036–1043, 10.1080/00016480802566261.
Zheng, J.L., Helbig, C., Gao, W.Q., Induction of cell proliferation by fibroblast and insulin-like growth factors in pure rat inner ear epithelial cell cultures. J. Neurosci. 17 (1997), 216–226.