Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Journal of Neuroinflammation
Published in: Journal of Neuroinflammation 1/2024

Open Access 01-12-2024 | Cytokines | Research

Oxidative stress and inflammation cause auditory system damage via glial cell activation and dysregulated expression of gap junction proteins in an experimental model of styrene-induced oto/neurotoxicity

Authors: Fabiola Paciello, Anna Pisani, Rolando Rolesi, Raffaele Montuoro, Veronica Mohamed-Hizam, Giammarco Boni, Cristian Ripoli, Jacopo Galli, Renata Sisto, Anna Rita Fetoni, Claudio Grassi

Published in: Journal of Neuroinflammation | Issue 1/2024

Login to get access

Abstract

Background

Redox imbalance and inflammation have been proposed as the principal mechanisms of damage in the auditory system, resulting in functional alterations and hearing loss. Microglia and astrocytes play a crucial role in mediating oxidative/inflammatory injury in the central nervous system; however, the role of glial cells in the auditory damage is still elusive.

Objectives

Here we investigated glial-mediated responses to toxic injury in peripheral and central structures of the auditory pathway, i.e., the cochlea and the auditory cortex (ACx), in rats exposed to styrene, a volatile compound with well-known oto/neurotoxic properties.

Methods

Male adult Wistar rats were treated with styrene (400 mg/kg daily for 3 weeks, 5/days a week). Electrophysiological, morphological, immunofluorescence and molecular analyses were performed in both the cochlea and the ACx to evaluate the mechanisms underlying styrene-induced oto/neurotoxicity in the auditory system.

Results

We showed that the oto/neurotoxic insult induced by styrene increases oxidative stress in both cochlea and ACx. This was associated with macrophages and glial cell activation, increased expression of inflammatory markers (i.e., pro-inflammatory cytokines and chemokine receptors) and alterations in connexin (Cxs) and pannexin (Panx) expression, likely responsible for dysregulation of the microglia/astrocyte network. Specifically, we found downregulation of Cx26 and Cx30 in the cochlea, and high level of Cx43 and Panx1 in the ACx.

Conclusions

Collectively, our results provide novel evidence on the role of immune and glial cell activation in the oxidative/inflammatory damage induced by styrene in the auditory system at both peripheral and central levels, also involving alterations of gap junction networks. Our data suggest that targeting glial cells and connexin/pannexin expression might be useful to attenuate oxidative/inflammatory damage in the auditory system.
Appendix
Available only for authorised users
Literature
1.
2.
3.
Kujawa SG, Liberman MC. Synaptopathy in the noise-exposed and aging cochlea: primary neural degeneration in acquired sensorineural hearing loss. Hear Res. 2015;330:191–9.PubMedPubMedCentralCrossRef
4.
Muly S. Synaptophysin in the cochlear nucleus following acoustic trauma. Exp Neurol. 2002;177:202–21.PubMedCrossRef
5.
Kim JJ, Gross J, Potashner SJ, Morest DK. Fine structure of long-term changes in the cochlear nucleus after acoustic overstimulation: chronic degeneration and new growth of synaptic endings. J Neurosci Res. 2004;77:817–28.PubMedCrossRef
6.
Muly SM, Gross JS, Potashner SJ. Noise trauma altersD-[3H]aspartate release and AMPA binding in chinchilla cochlear nucleus. J Neurosci Res. 2004;75:585–96.PubMedCrossRef
7.
Fetoni AR, De Bartolo P, Eramo SLM, Rolesi R, Paciello F, Bergamini C, et al. 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. 2013;33:4011–23.PubMedPubMedCentralCrossRef
8.
Paciello F, Podda MV, Rolesi R, Cocco S, Petrosini L, Troiani D, et al. Anodal transcranial direct current stimulation affects auditory cortex plasticity in normal-hearing and noise-exposed rats. Brain Stimul. 2018;11:1008–23.PubMedCrossRef
9.
Paciello F, Rinaudo M, Longo V, Cocco S, Conforto G, Pisani A, et al. Auditory sensory deprivation induced by noise exposure exacerbates cognitive decline in a mouse model of Alzheimer’s disease. Elife. 2021;10:e70908.PubMedPubMedCentralCrossRef
10.
Paciello F, Pisani A, Rinaudo M, Cocco S, Paludetti G, Fetoni AR, et al. Noise-induced auditory damage affects hippocampus causing memory deficits in a model of early age-related hearing loss. Neurobiol Dis. 2023;178: 106024.PubMedCrossRef
11.
Wakabayashi K, Fujioka M, Kanzaki S, Okano HJ, Shibata S, Yamashita D, et al. Blockade of interleukin-6 signaling suppressed cochlear inflammatory response and improved hearing impairment in noise-damaged mice cochlea. Neurosci Res. 2010;66:345–52.PubMedCrossRef
12.
Tan WJT, Thorne PR, Vlajkovic SM. Characterisation of cochlear inflammation in mice following acute and chronic noise exposure. Histochem Cell Biol. 2016;146:219–30.PubMedCrossRef
13.
Benkafadar N, Menardo J, Bourien J, Nouvian R, François F, Decaudin D, et al. Reversible p53 inhibition prevents cisplatin ototoxicity without blocking chemotherapeutic efficacy. EMBO Mol Med. 2017;9:7–26.PubMedCrossRef
14.
Shen Y, Hu H, Fan C, Wang Q, Zou T, Ye B, et al. Sensorineural hearing loss may lead to dementia-related pathological changes in hippocampal neurons. Neurobiol Dis. 2021;156: 105408.PubMedCrossRef
15.
Block ML, Zecca L, Hong J-S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci. 2007;8:57–69.PubMedCrossRef
16.
Lin M, Yu H, Xie Q, Xu Z, Shang P. Role of microglia autophagy and mitophagy in age-related neurodegenerative diseases. Front Aging Neurosci. 2023;14:1100133.PubMedPubMedCentralCrossRef
17.
18.
19.
20.
Rasband MN. Glial contributions to neural function and disease. Mol Cell Proteomics. 2016;15:355–61.PubMedCrossRef
21.
22.
Valles SL, Singh SK, Campos-Campos J, Colmena C, Campo-Palacio I, Alvarez-Gamez K, et al. Functions of astrocytes under normal conditions and after a brain disease. IJMS. 2023;24:8434.PubMedPubMedCentralCrossRef
23.
Cuadros MA, Sepulveda MR, Martin-Oliva D, Marín-Teva JL, Neubrand VE. Microglia and microglia-like cells: similar but different. Front Cell Neurosci. 2022;16: 816439.PubMedPubMedCentralCrossRef
24.
Miron VE, Priller J. Investigating microglia in health and disease: challenges and opportunities. Trends Immunol. 2020;41:785–93.PubMedCrossRef
25.
Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, et al. Synaptic pruning by microglia is necessary for normal brain development. Science. 2011;333:1456–8.PubMedCrossRef
26.
27.
28.
Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, et al. The classical complement cascade mediates CNS synapse elimination. Cell. 2007;131:1164–78.PubMedCrossRef
29.
30.
Paolicelli RC, Sierra A, Stevens B, Tremblay M-E, Aguzzi A, Ajami B, et al. Microglia states and nomenclature: a field at its crossroads. Neuron. 2022;110:3458–83.PubMedPubMedCentralCrossRef
31.
Huang H, He W, Tang T, Qiu M. Immunological markers for central nervous system glia. Neurosci Bull. 2023;39:379–92.PubMedCrossRef
32.
33.
Li Q, Barres BA. Microglia and macrophages in brain homeostasis and disease. Nat Rev Immunol. 2018;18:225–42.PubMedCrossRef
34.
Borst K, Dumas AA, Prinz M. Microglia: immune and non-immune functions. Immunity. 2021;54:2194–208.PubMedCrossRef
35.
36.
37.
38.
Hough K, Verschuur CA, Cunningham C, Newman TA. Macrophages in the cochlea; an immunological link between risk factors and progressive hearing loss. Glia. 2022;70:219–38.PubMedCrossRef
39.
Alliot F, Godin I, Pessac B. Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain. Dev Brain Res. 1999;117:145–52.CrossRef
40.
Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science. 2010;330:841–5.PubMedPubMedCentralCrossRef
41.
Katsumoto A, Lu H, Miranda AS, Ransohoff RM. Ontogeny and functions of central nervous system macrophages. J Immunol. 2014;193:2615–21.PubMedCrossRef
42.
Hirose K, Discolo CM, Keasler JR, Ransohoff R. Mononuclear phagocytes migrate into the murine cochlea after acoustic trauma. J Comparative Neurol. 2005;489:180–94.CrossRef
43.
Parisi L, Gini E, Baci D, Tremolati M, Fanuli M, Bassani B, et al. Macrophage polarization in chronic inflammatory diseases: killers or builders? J Immunol Res. 2018;2018:1–25.CrossRef
44.
Spencer NG, Schilling T, Miralles F, Eder C. Mechanisms underlying interferon-γ-induced priming of microglial reactive oxygen species production. PLoS ONE. 2016;11:e0162497.PubMedPubMedCentralCrossRef
45.
Simpson DSA, Oliver PL. ROS generation in microglia: understanding oxidative stress and inflammation in neurodegenerative disease. Antioxidants. 2020;9:743.PubMedPubMedCentralCrossRef
46.
Smith AN, Shaughness M, Collier S, Hopkins D, Byrnes KR. Therapeutic targeting of microglia mediated oxidative stress after neurotrauma. Front Med. 2022;9:1034692.CrossRef
47.
Loane DJ, Kumar A. Microglia in the TBI brain: the good, the bad, and the dysregulated. Exp Neurol. 2016;275:316–27.PubMedCrossRef
48.
Członkowska A, Kurkowska-Jastrzębska I, Członkowski A, Peter D, Stefano GB. Immune processes in the pathogenesis of Parkinson’s disease – a potential role for microglia and nitric oxide. Med Sci Monit. 2002;8:165–77.
49.
Eugenín EA, Eckardt D, Theis M, Willecke K, Bennett MVL, Sáez JC. Microglia at brain stab wounds express connexin 43 and in vitro form functional gap junctions after treatment with interferon-γ and tumor necrosis factor-α. Proc Natl Acad Sci USA. 2001;98:4190–5.PubMedPubMedCentralCrossRef
50.
Retamal MA, Cortés CJ, Reuss L, Bennett MVL, Sáez JC. S-nitrosylation and permeation through connexin 43 hemichannels in astrocytes: induction by oxidant stress and reversal by reducing agents. Proc Natl Acad Sci USA. 2006;103:4475–80.PubMedPubMedCentralCrossRef
51.
Gajardo-Gómez R, Labra VC, Orellana JA. Connexins and pannexins: new insights into microglial functions and dysfunctions. Front Mol Neurosci. 2016;6:9.
52.
53.
Caruso G, Di Pietro L, Caraci F. Gap junctions and connexins in microglia-related oxidative stress and neuroinflammation: perspectives for drug discovery. Biomolecules. 2023;13:505.PubMedPubMedCentralCrossRef
54.
Suadicani SO, Brosnan CF, Scemes E. P2X 7 receptors mediate ATP release and amplification of astrocytic intercellular Ca 2+ signaling. J Neurosci. 2006;26:1378–85.PubMedPubMedCentralCrossRef
55.
56.
Rouach N, Calvo C-F, Glowinski J, Giaume C. Brain macrophages inhibit gap junctional communication and downregulate connexin 43 expression in cultured astrocytes: brain macrophages and gap junctions in astrocytes. Eur J Neurosci. 2002;15:403–7.PubMedCrossRef
57.
Faustmann PM, Haase CG, Romberg S, Hinkerohe D, Szlachta D, Smikalla D, et al. Microglia activation influences dye coupling and Cx43 expression of the astrocytic network. Glia. 2003;42:101–8.PubMedCrossRef
58.
Hinkerohe D, Smikalla D, Haghikia A, Heupel K, Haase CG, Dermietzel R, et al. Effects of cytokines on microglial phenotypes and astroglial coupling in an inflammatory coculture model. Glia. 2005;52:85–97.PubMedCrossRef
59.
Même W, Calvo C, Froger N, Ezan P, Amigou E, Koulakoff A, et al. Proinflammatory cytokines released from microglia inhibit gap junctions in astrocytes: potentiation by β-amyloid. FASEB j. 2006;20:494–6.PubMedCrossRef
60.
Retamal MA, Froger N, Palacios-Prado N, Ezan P, Sáez PJ, Sáez JC, et al. Cx43 hemichannels and gap junction channels in astrocytes are regulated oppositely by proinflammatory cytokines released from activated microglia. J Neurosci. 2007;27:13781–92.PubMedPubMedCentralCrossRef
61.
Orellana JA, Froger N, Ezan P, Jiang JX, Bennett MVL, Naus CC, et al. ATP and glutamate released via astroglial connexin 43 hemichannels mediate neuronal death through activation of pannexin 1 hemichannels: astroglial hemichannels induce neuronal death. J Neurochem. 2011;118:826–40.PubMedPubMedCentralCrossRef
62.
Fuentes-Santamaría V, Alvarado JC, Juiz JM. Long-term interaction between microglial cells and cochlear nucleus neurons after bilateral cochlear ablation. J Comp Neurol. 2012;520:2974–90.PubMedCrossRef
63.
Baizer JS, Wong KM, Manohar S, Hayes SH, Ding D, Dingman R, et al. Effects of acoustic trauma on the auditory system of the rat: the role of microglia. Neuroscience. 2015;303:299–311.PubMedCrossRef
64.
Campos Torres A, Vidal PP, de Waele C. Evidence for a microglial reaction within the vestibular and cochlear nuclei following inner ear lesion in the rat. Neuroscience. 1999;92:1475–90.PubMedCrossRef
65.
Noda M, Hatano M, Hattori T, Takarada-Iemata M, Shinozaki T, Sugimoto H, et al. Microglial activation in the cochlear nucleus after early hearing loss in rats. Auris Nasus Larynx. 2019;46:716–23.PubMedCrossRef
66.
Fetoni AR, Paciello F, Rolesi R, Pisani A, Moleti A, Sisto R, et al. Styrene targets sensory and neural cochlear function through the crossroad between oxidative stress and inflammation. Free Radical Biol Med. 2021;163:31–42.CrossRef
67.
Fetoni AR, Rolesi R, Paciello F, Eramo SLM, Grassi C, Troiani D, et al. Styrene enhances the noise induced oxidative stress in the cochlea and affects differently mechanosensory and supporting cells. Free Radical Biol Med. 2016;101:211–25.CrossRef
68.
Sisto R, Cerini L, Gatto MP, Gherardi M, Gordiani A, Sanjust F, et al. Otoacoustic emission sensitivity to exposure to styrene and noise. J Acoust Soc Am. 2013;134:3739–48.PubMedCrossRef
69.
Chen G-D, Henderson D. Cochlear injuries induced by the combined exposure to noise and styrene. Hear Res. 2009;254:25–33.PubMedCrossRef
70.
Alvarado JC, Fuentes-Santamaría V, Jareño-Flores T, Blanco JL, Juiz JM. Normal variations in the morphology of auditory brainstem response (ABR) waveforms: a study in wistar rats. Neurosci Res. 2012;73:302–11.PubMedCrossRef
71.
Paxinos G, Franklin KBJ. The mouse brain in stereotaxic coordinates, 2. San Diego: Academic; 2001.
72.
73.
Hol EM, Pekny M. Glial fibrillary acidic protein (GFAP) and the astrocyte intermediate filament system in diseases of the central nervous system. Curr Opin Cell Biol. 2015;32:121–30.PubMedCrossRef
74.
Korzhevskii DE, Kirik OV. Brain microglia and microglial markers. Neurosci Behav Physi. 2016;46:284–90.CrossRef
75.
Sholl DA. The measurable parameters of the cerebral cortex and their significance in its organization. Prog Neurobiol. 1956;2:324e33.
76.
Bisicchia E, Sasso V, Catanzaro G, Leuti A, Besharat ZM, Chiacchiarini M, et al. Resolvin D1 halts remote neuroinflammation and improves functional recovery after focal brain damage via ALX/FPR2 receptor-regulated MicroRNAs. Mol Neurobiol. 2018;55:6894–905.PubMedCrossRef
77.
Kongsui R, Beynon SB, Johnson SJ, Walker FR. Quantitative assessment of microglial morphology and density reveals remarkable consistency in the distribution and morphology of cells within the healthy prefrontal cortex of the rat. J Neuroinflammation. 2014;11:182.PubMedPubMedCentralCrossRef
78.
Catale C, Bisicchia E, Carola V, Viscomi MT. Early life stress exposure worsens adult remote microglia activation, neuronal death, and functional recovery after focal brain injury. Brain Behav Immun. 2021;94:89–103.PubMedCrossRef
79.
Fetoni AR, Pisani A, Rolesi R, Paciello F, Viziano A, Moleti A, et al. Early noise-induced hearing loss accelerates presbycusis altering aging processes in the cochlea. Front Aging Neurosci. 2022;14: 803973.PubMedPubMedCentralCrossRef
80.
Fetoni AR, Eramo SLM, Paciello F, Rolesi R, Samengo D, Paludetti G, et al. The redox protein p66shc mediates cochlear vascular dysfunction and transient noise-induced hearing loss. Sci Rep. 2016;6:25450.PubMedPubMedCentralCrossRef
81.
Havekes R, Timmer M, Van der Zee EA. Regional differences in hippocampal PKA immunoreactivity after training and reversal training in a spatial Y-maze task. Hippocampus. 2007;17:338–48.PubMedCrossRef
82.
Man H-Y, Sekine-Aizawa Y, Huganir RL. Regulation of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor trafficking through PKA phosphorylation of the Glu receptor 1 subunit. Proc Natl Acad Sci USA. 2007;104:3579–84.PubMedPubMedCentralCrossRef
83.
He K, Song L, Cummings LW, Goldman J, Huganir RL, Lee H-K. Stabilization of Ca 2+ -permeable AMPA receptors at perisynaptic sites by GluR1-S845 phosphorylation. Proc Natl Acad Sci USA. 2009;106:20033–8.PubMedPubMedCentralCrossRef
84.
Goel A, Xu LW, Snyder KP, Song L, Goenaga-Vazquez Y, Megill A, et al. Phosphorylation of AMPA receptors is required for sensory deprivation-induced homeostatic synaptic plasticity. PLoS ONE. 2011;6:e18264.PubMedPubMedCentralCrossRef
85.
Chen G-D, Chi L-H, Kostyniak PJ, Henderson D. Styrene induced alterations in biomarkers of exposure and effects in the cochlea: mechanisms of hearing loss. Toxicol Sci. 2007;98:167–77.PubMedCrossRef
86.
Vane JR, Bakhle YS, Botting R. Cyclooxygenases 1 and 2. Annu Rev Pharmacol Toxicol. 1998;38:97–120.PubMedCrossRef
87.
Jones SA, Wolf M, Qin S, Mackay CR, Baggiolini M. Different functions for the interleukin 8 receptors (IL-8R) of human neutrophil leukocytes: NADPH oxidase and phospholipase D are activated through IL-8R1 but not IL-8R2. Proc Natl Acad Sci USA. 1996;93:6682–6.PubMedPubMedCentralCrossRef
88.
Cambier S, Gouwy M, Proost P. The chemokines CXCL8 and CXCL12: molecular and functional properties, role in disease and efforts towards pharmacological intervention. Cell Mol Immunol. 2023;20:217–51.PubMedPubMedCentralCrossRef
89.
Rio C, Dikkes P, Liberman MC, Corfas G. Glial fibrillary acidic protein expression and promoter activity in the inner ear of developing and adult mice. J Comp Neurol. 2002;442:156–62.PubMedCrossRef
90.
Salter MW, Stevens B. Microglia emerge as central players in brain disease. Nat Med. 2017;23:1018–27.PubMedCrossRef
91.
92.
Paciello F, Zorzi V, Raspa M, Scavizzi F, Grassi C, Mammano F, et al. Connexin 30 deletion exacerbates cochlear senescence and age-related hearing loss. Front Cell Dev Biol. 2022;10: 950837.PubMedPubMedCentralCrossRef
93.
Kessels HW, Kopec CD, Klein ME, Malinow R. Roles of stargazin and phosphorylation in the control of AMPA receptor subcellular distribution. Nat Neurosci. 2009;12:888–96.PubMedPubMedCentralCrossRef
94.
Morgan MJ, Liu Z. Crosstalk of reactive oxygen species and NF-κB signaling. Cell Res. 2011;21:103–15.PubMedCrossRef
95.
Blaser H, Dostert C, Mak TW, Brenner D. TNF and ROS Crosstalk in Inflammation. Trends Cell Biol. 2016;26:249–61.PubMedCrossRef
96.
Kalinec GM, Lomberk G, Urrutia RA, Kalinec F. Resolution of cochlear inflammation: novel target for preventing or ameliorating drug-, noise- and age-related hearing loss. Front Cell Neurosci. 2017;11:192.PubMedPubMedCentralCrossRef
97.
Fetoni AR, Paciello F, Rolesi R, Paludetti G, Troiani D. Targeting dysregulation of redox homeostasis in noise-induced hearing loss: oxidative stress and ROS signaling. Free Radical Biol Med. 2019;135:46–59.CrossRef
98.
Daré E, Tofighi R, Nutt L, Vettori MV, Emgård M, Mutti A, et al. Styrene 7,8-oxide induces mitochondrial damage and oxidative stress in neurons. Toxicology. 2004;201:125–32.PubMedCrossRef
99.
Vettori MV, Caglieri A, Goldoni M, Castoldi AF, Darè E, Alinovi R, et al. Analysis of oxidative stress in SK-N-MC neurons exposed to styrene-7,8-oxide. Toxicol In Vitro. 2005;19:11–20.PubMedCrossRef
100.
Meszka-Jordan A, Mahlapuu R, Soomets U, Carlson GP. Oxidative stress due to (R)-styrene oxide exposure and the role of antioxidants in non-Swiss albino (NSA) mice. J Toxicol Environ Health A. 2009;72:642–50.PubMedCrossRef
101.
Sisto R, Botti T, Cerini L, Sanjust F, Tranfo G, Bonanni RC, et al. Oxidative stress biomarkers and otoacoustic emissions in humans exposed to styrene and noise. Int J Audiol. 2016;55:523–31.PubMedCrossRef
102.
Fuentes-Santamaría V, Alvarado JC, Melgar-Rojas P, Gabaldón-Ull MC, Miller JM, Juiz JM. The role of glia in the peripheral and central auditory system following noise overexposure: contribution of TNF-α and IL-1β to the pathogenesis of hearing loss. Front Neuroanat. 2017;11:9.PubMedPubMedCentralCrossRef
103.
Wang Z, Li H. Microglia-like cells in rat organ of corti following aminoglycoside ototoxicity. NeuroReport. 2000;11:1389–93.PubMedCrossRef
104.
Ladrech S, Wang J, Simonneau L, Puel J-L, Lenoir M. Macrophage contribution to the response of the rat organ of Corti to amikacin. J Neurosci Res. 2007;85:1970–9.PubMedCrossRef
105.
Noble K, Brown L, Elvis P, Lang H. Cochlear immune response in presbyacusis: a focus on dysregulation of macrophage activity. JARO. 2022;23:1–16.PubMedCrossRef
106.
Kaur T, Ohlemiller KK, Warchol ME. Genetic disruption of fractalkine signaling leads to enhanced loss of cochlear afferents following ototoxic or acoustic injury. J Comp Neurol. 2018;526:824–35.PubMedCrossRef
107.
108.
Garden GA, Möller T. Microglia biology in health and disease. Jrnl NeuroImmune Pharm. 2006;1:127–37.CrossRef
109.
Saijo K, Glass CK. Microglial cell origin and phenotypes in health and disease. Nat Rev Immunol. 2011;11:775–87.PubMedCrossRef
110.
Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev. 2007;87:315–424.PubMedCrossRef
111.
Brown GC, Neher JJ. Inflammatory neurodegeneration and mechanisms of microglial killing of neurons. Mol Neurobiol. 2010;41:242–7.PubMedCrossRef
112.
Saha RN, Pahan K. Regulation of inducible nitric oxide synthase gene in glial cells. Antioxid Redox Signal. 2006;8:929–47.PubMedCrossRef
113.
Minghetti L, Nicolini A, Polazzi E, Créminon C, Maclouf J, Levi G. Inducible nitric oxide synthase expression in activated rat microglial cultures is downregulated by exogenous prostaglandin E2 and by cyclooxygenase inhibitors. Glia. 1997;19:152–60.PubMedCrossRef
114.
115.
Graeber MB, Li W, Rodriguez ML. Role of microglia in CNS inflammation. FEBS Lett. 2011;585:3798–805.PubMedCrossRef
116.
117.
Mander P, Brown GC. Activation of microglial NADPH oxidase is synergistic with glial iNOS expression in inducing neuronal death: a dual-key mechanism of inflammatory neurodegeneration. J Neuroinflammation. 2005;2:20.PubMedPubMedCentralCrossRef
118.
Ogura T, Tatemichi M, Esumi H. TNF-a mediates inducible nitric oxide synthase expression in human neuroblastoma cell line by cisplatin. Biochem Biophys Res Commun. 1997;233:788–91.PubMedCrossRef
119.
Heneka MT, Löschmann P-A, Gleichmann M, Weller M, Schulz JB, Wüllner U, et al. Induction of nitric oxide synthase and nitric oxide-mediated apoptosis in neuronal PC12 cells after stimulation with tumor necrosis factor-α/lipopolysaccharide. J Neurochem. 2002;71:88–94.CrossRef
120.
Combs CK, Karlo JC, Kao S-C, Landreth GE. beta-Amyloid stimulation of microglia and monocytes results in TNFalpha-dependent expression of inducible nitric oxide synthase and neuronal apoptosis. J Neurosci. 2001;21:1179–88.PubMedPubMedCentralCrossRef
121.
Flynn G, Maru S, Loughlin J, Romero IA, Male D. Regulation of chemokine receptor expression in human microglia and astrocytes. J Neuroimmunol. 2003;136:84–93.PubMedCrossRef
122.
Madore C, Joffre C, Delpech JC, De Smedt-Peyrusse V, Aubert A, Coste L, et al. Early morphofunctional plasticity of microglia in response to acute lipopolysaccharide. Brain Behav Immun. 2013;34:151–8.PubMedCrossRef
123.
Sierra A, Abiega O, Shahraz A, Neumann H. Janus-faced microglia: beneficial and detrimental consequences of microglial phagocytosis. Front Cell Neurosci 2013;7.
124.
Waller R, Baxter L, Fillingham DJ, Coelho S, Pozo JM, Mozumder M, et al. Iba-1-/CD68+ microglia are a prominent feature of age-associated deep subcortical white matter lesions. PLoS ONE. 2019;14:e0210888.PubMedPubMedCentralCrossRef
125.
Yang Z, Wang KKW. Glial fibrillary acidic protein: from intermediate filament assembly and gliosis to neurobiomarker. Trends Neurosci. 2015;38:364–74.PubMedPubMedCentralCrossRef
126.
Wilhelmsson U, Bushong EA, Price DL, Smarr BL, Phung V, Terada M, et al. Redefining the concept of reactive astrocytes as cells that remain within their unique domains upon reaction to injury. Proc Natl Acad Sci USA. 2006;103:17513–8.PubMedPubMedCentralCrossRef
127.
Wilhelmsson U, Li L, Pekna M, Berthold C-H, Blom S, Eliasson C, et al. Absence of glial fibrillary acidic protein and vimentin prevents hypertrophy of astrocytic processes and improves post-traumatic regeneration. J Neurosci. 2004;24:5016–21.PubMedPubMedCentralCrossRef
128.
Garg S, Syed MM, Kielian T. Staphylococcus aureus-derived peptidoglycan induces Cx43 expression and functional gap junction intercellular communication in microglia. J Neurochem. 2005;95:475–83.PubMedPubMedCentralCrossRef
129.
Sáez PJ, Shoji KF, Retamal MA, Harcha PA, Ramírez G, Jiang JX, et al. ATP is required and advances cytokine-induced gap junction formation in microglia in vitro. Mediators Inflamm. 2013;2013:1–16.CrossRef
130.
Giaume C, Fromaget C, el Aoumari A, Cordier J, Glowinski J, Gros D. Gap junctions in cultured astrocytes: single-channel currents and characterization of channel-forming protein. Neuron. 1991;6:133–43.PubMedCrossRef
131.
Zhang J, Riquelme MA, Hua R, Acosta FM, Gu S, Jiang JX. Connexin 43 hemichannels regulate mitochondrial ATP generation, mobilization, and mitochondrial homeostasis against oxidative stress. Elife. 2022;11:e82206.PubMedPubMedCentralCrossRef
132.
Orellana JA, Shoji KF, Abudara V, Ezan P, Amigou E, Sáez PJ, et al. Amyloid β-induced death in neurons involves glial and neuronal hemichannels. J Neurosci. 2011;31:4962–77.PubMedPubMedCentralCrossRef
133.
134.
135.
Snoeckx RL, Huygen PLM, Feldmann D, Marlin S, Denoyelle F, Waligora J, et al. GJB2 mutations and degree of hearing loss: a multicenter study. Am J Human Genet. 2005;77:945–57.CrossRef
136.
Kenna MA, Feldman HA, Neault MW, Frangulov A, Wu B-L, Fligor B, et al. Audiologic phenotype and progression in GJB2 (Connexin 26) hearing loss. Arch Otolaryngol Head Neck Surg. 2010;136:81.PubMedPubMedCentralCrossRef
137.
del Castillo FJ, del Castillo I. DFNB1 non-syndromic hearing impairment: diversity of mutations and associated phenotypes. Front Mol Neurosci. 2017;10:428.PubMedPubMedCentralCrossRef
138.
Tajima S, Danzaki K, Ikeda K, Kamiya K. Degradation and modification of cochlear gap junction proteins in the early development of age-related hearing loss. Exp Mol Med. 2020;52:166–75.PubMedPubMedCentralCrossRef
139.
Ichimiya I, Suzuki M, Mogi G. Age-related changes in the murine cochlear lateral wall. Hear Res. 2000;139:116–22.PubMedCrossRef
140.
Fetoni AR, Zorzi V, Paciello F, Ziraldo G, Peres C, Raspa M, et al. Cx26 partial loss causes accelerated presbycusis by redox imbalance and dysregulation of Nfr2 pathway. Redox Biol. 2018;19:301–17.PubMedPubMedCentralCrossRef
141.
142.
143.
Abitbol JM, Kelly JJ, Barr K, Schormans AL, Laird DW, Allman BL. Differential effects of pannexins on noise-induced hearing loss. Biochem J. 2016;473:4665–80.PubMedCrossRef
144.
Zorzi V, Paciello F, Ziraldo G, Peres C, Mazzarda F, Nardin C, et al. Mouse Panx1 is dispensable for hearing acquisition and auditory function. Front Mol Neurosci. 2017;10:379.PubMedPubMedCentralCrossRef
Metadata
Title
Oxidative stress and inflammation cause auditory system damage via glial cell activation and dysregulated expression of gap junction proteins in an experimental model of styrene-induced oto/neurotoxicity
Authors
Fabiola Paciello
Anna Pisani
Rolando Rolesi
Raffaele Montuoro
Veronica Mohamed-Hizam
Giammarco Boni
Cristian Ripoli
Jacopo Galli
Renata Sisto
Anna Rita Fetoni
Claudio Grassi
Publication date
01-12-2024
Publisher
BioMed Central
Keyword
Cytokines
Published in
Journal of Neuroinflammation / Issue 1/2024
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/s12974-023-02996-3

Other articles of this Issue 1/2024

Journal of Neuroinflammation 1/2024 Go to the issue

Research

Th1 cells contribute to retinal ganglion cell loss in glaucoma in a VCAM-1-dependent manner

Research

Progranulin haploinsufficiency mediates cytoplasmic TDP-43 aggregation with lysosomal abnormalities in human microglia

Research

Autoimmune demyelination alters hypothalamic transcriptome and endocrine function

Research

Commonly disrupted pathways in brain and kidney in a pig model of systemic endotoxemia

Review

Border-associated macrophages in the central nervous system

Review

Peripheral blood amyloid-β involved in the pathogenesis of Alzheimer’s disease via impacting on peripheral innate immune cells