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Review Articles

Application of adverse outcome pathway networks to integrate mechanistic data informing the choice of a point of departure for hydrogen sulfide exposure limits

ORCID Icon & ORCID Icon
Pages 193-208 | Received 04 Oct 2020, Accepted 25 Feb 2021, Published online: 27 Apr 2021

References

  • ACGIH 2010. Hydrogen sulphide. Documentations of the threshold limit values and biological exposure indices, Seventh Edition – 2010. Cincinnati, Ohio: American Conference of Governmental Industrial Hygienists (ACGIH).
  • Albertine KH, Soulier MF, Wang Z, Ishizaka A, Hashimoto S, Zimmerman GA, Matthay MA, Ware LB. 2002. Fas and fas ligand are up-regulated in pulmonary edema fluid and lung tissue of patients with acute lung injury and the acute respiratory distress syndrome. Am J Pathol. 161(5):1783–1796.
  • Anantharam P, Whitley EM, Mahama B, Kim DS, Imerman PM, Shao D, Langley MR, Kanthasamy A, Rumbeiha WK. 2017. Characterizing a mouse model for evaluation of countermeasures against hydrogen sulfide-induced neurotoxicity and neurological sequelae. Ann NY Acad Sci. 1400(1):46–64.
  • Assaad S, Kratzert WB, Shelley B, Friedman MB, Perrino A. 2018. Assessment of pulmonary edema: principles and practice. J Cardiothorac Vasc Anesth. 32(2):901–914.
  • ATSDR. 2016. Toxicological profile for hydrogen sulfide/carbonyl sulfide. Atlanta (GA): US Department of Health and Human Services, Public Health Service.
  • Bailey LA, Nascarella MA, Kerper LE, Rhomberg LR. 2016. Hypothesis-based weight-of-evidence evaluation and risk assessment for naphthalene carcinogenesis. Crit Rev Toxicol. 46(1):1–42.
  • Bal-Price A, Leist M, Schildknecht S, Tschudi-Monnet F, Paini A, Terron A. 2018. Adverse outcome pathway on inhibition of the mitochondrial complex I of nigro-striatal neurons leading to parkinsonian motor deficits. OECD Series on Adverse Outcome Pathways, No. 7. Paris: OECD Publishing. DOI:https://doi.org/10.1787/b46c3c00-en.
  • Barazzone C, Horowitz S, Donati YR, Rodriguez I, Piguet P-F. 1998. Oxygen toxicity in mouse lung: pathways to cell death. Am J Respir Cell Mol Biol. 19(4):573–581.
  • Baumann A, Audibert G, McDonnell J, Mertes PM. 2007. Neurogenic pulmonary edema. Acta Anaesthesiol Scand. 51(4):447–455.
  • Beauchamp R, Bus JS, Popp JA, Boreiko CJ, Andjelkovich DA, Leber P. 1984. A critical review of the literature on hydrogen sulfide toxicity. Crit Rev Toxicol. 13(1):25–97.
  • Becker RA, Dellarco V, Seed J, Kronenberg JM, Meek B, Foreman J, Palermo C, Kirman C, Linkov I, Schoeny R, et al. 2017. Quantitative weight of evidence to assess confidence in potential modes of action. Regul Toxicol Pharmacol. 86:205–220.
  • Bergman O, Ben-Shachar D. 2016. Mitochondrial Oxidative Phosphorylation System (OXPHOS) deficits in schizophrenia: possible interactions with cellular processes. Can J Psychiatry. 61(8):457–469.
  • Bhambhani Y, Burnham R, Snydmiller G, MacLean I. 1997. Effects of 10-ppm hydrogen sulfide inhalation in exercising men and women. Cardiovascular, metabolic, and biochemical responses. J Occup Environ Med. 39(2):122–129.
  • Bhambhani Y, Burnham R, Snydmiller G, MacLean I, Lovlin R. 1996a. Effects of 10-ppm hydrogen sulfide inhalation on pulmonary function in healthy men and women. J Occup Environ Med. 38(10):1012–1017.
  • Bhambhani Y, Burnham R, Snydmiller G, MacLean I, Martin T. 1994. Comparative physiological responses of exercising men and women to 5 ppm hydrogen sulfide exposure. Am Ind Hyg Assoc J. 55(11):1030–1035.
  • Bhambhani Y, Burnham R, Snydmiller G, MacLean I, Martin T. 1996b. Effects of 5 ppm hydrogen sulfide inhalation on biochemical properties of skeletal muscle in exercising men and women. Am Ind Hyg Assoc J. 57(5):464–468.
  • Bhambhani Y, Singh M. 1991. Physiological effects of hydrogen sulfide inhalation during exercise in healthy men. J Appl Physiol (1985). 71(5):1872–1877.
  • Boesveldt S, Postma EM, Boak D, Welge-Luessen A, Schöpf V, Mainland JD, Martens J, Ngai J, Duffy VB. 2017. Anosmia – a clinical review. Chem Senses. 42(7):513–523.
  • Bogdanffy MS, VAN DER Meulen HCD, Beems RB, Feron VJ, Cascieri TC, Tyler TR, Vinegar MB, Rickard RW. 1994. Chronic toxicity and oncogenicity inhalation study with vinyl acetate in the rat and mouse1. Toxicol Sci. 23(2):215–229.
  • Bogen KT, Benson JM, Yost GS, Morris JB, Dahl AR, Clewell HJ, Krishnan K, Omiecinski CJ. 2008. Naphthalene metabolism in relation to target tissue anatomy, physiology, cytotoxicity and tumorigenic mechanism of action. Regul Toxicol Pharm. 51(2):27–36.
  • Brenneman KA, James RA, Gross EA, Dorman DC. 2000. Olfactory neuron loss in adult male CD rats following subchronic inhalation exposure to hydrogen sulfide. Toxicol Pathol. 28(2):326–333.
  • Brenneman KA, Meleason DF, Sar M, Marshall MW, James RA, Gross EA, Martin JT, Dorman DC. 2002. Olfactory mucosal necrosis in male CD rats following acute inhalation exposure to hydrogen sulfide: reversibility and the possible role of regional metabolism. Toxicol Pathol. 30(2):200–208.
  • Brown GC, Borutaite V-B. 2004. Inhibition of mitochondrial respiratory complex I by nitric oxide, peroxynitrite and S-nitrosothiols. Biochim Biophys Acta. 1658(1–2):44–49.
  • Burté F, Carelli V, Chinnery PF, Yu-Wai-Man P. 2015. Disturbed mitochondrial dynamics and neurodegenerative disorders. Nat Rev Neurol. 11(1):11–24.
  • Chamanza R, Wright J. 2015. A review of the comparative anatomy, histology, physiology and pathology of the nasal cavity of rats, mice, dogs and non-human primates. Relevance to inhalation toxicology and human health risk assessment. J Comp Pathol. 153(4):287–314.
  • Chi H, Chang H-Y, Sang T-K. 2018. Neuronal cell death mechanisms in major neurodegenerative diseases. IJMS. 19(10):3082.
  • Chin-Chan M, Navarro-Yepes J, Quintanilla-Vega B. 2015. Environmental pollutants as risk factors for neurodegenerative disorders: Alzheimer and Parkinson diseases [Review]. Environmental factors in neurodegeneration. Front Cell Neurosci. 9:124.
  • CIIT. 1983a. 90-Day vapor inhalation toxicity study of hydrogen sulfide in B6C3F1 mice. Research Triangle Park, NC. Chemical Industry Institute of Toxicology CIIT docket #42063.
  • CIIT. 1983b. 90-Day vapor inhalation toxicity study of hydrogen sulfide in Fischer 344 rats. Research Triangle Park, NC. Chemical Industry Institute of Toxicology CIIT docket #22063.
  • CIIT. 1983c. 90-Day vapor inhalation toxicity study of hydrogen sulfide in Sprague-Dawley rats. Research Triangle Park, NC. Chemical Industry Institute of Toxicology CIIT docket #32063.
  • Cogliati S, Lorenzi I, Rigoni G, Caicci F, Soriano ME. 2018. Regulation of mitochondrial electron transport chain assembly. J Mol Biol. 430(24):4849–4873.
  • Davison DL, Terek M, Chawla LS. 2012. Neurogenic pulmonary edema. Crit Care. 16(2):212.
  • de Vries RBM, Angrish M, Browne P, Brozek J, Rooney A, Wikoff DS, Whaley P, Edwards SW, Morgan RL, Druwe IL, et al. 2021. Applying evidence-based methods to the development and use of adverse outcome pathways. ALTEX – Alternatives to Animal Experimentation (In press). DOI:https://doi.org/10.14573/altex.2101211
  • Deveau M, Chen CP, Johanson G, Krewski D, Maier A, Niven KJ, Ripple S, Schulte PA, Silk J, Urbanus JH, et al. 2015. The global landscape of occupational exposure limits—implementation of harmonization principles to guide limit selection. J Occup Environ Hyg. 12(Sup1):S127–S144.
  • Dorman DC, Moulin FJM, McManus BE, Mahle KC, James RA, Struve MF. 2002. Cytochrome oxidase inhibition induced by acute hydrogen sulfide inhalation: correlation with tissue sulfide concentrations in the rat brain, liver, lung, and nasal epithelium. Toxicol Sci: Off J Soc Toxicol. 65(1):18–25.
  • Dorman DC, Struve MF, Gross EA, Brenneman KA. 2004. Respiratory tract toxicity of inhaled hydrogen sulfide in Fischer-344 rats, Sprague-Dawley rats, and B6C3F1 mice following subchronic (90-day) exposure. Toxicol Appl Pharmacol. 198(1):29–39.
  • Dorman DC, Struve MF, Wong BA, Gross EA, Parkinson C, Willson GA, Tan Y-M, Campbell JL, Teeguarden JG, Clewell HJ, et al. 2008. Derivation of an inhalation reference concentration based upon olfactory neuronal loss in male rats following subchronic acetaldehyde inhalation. Inhal Toxicol. 20(3):245–256.
  • Dourson ML, Felter SP, Robinson D. 1996. Evolution of science-based uncertainty factors in noncancer risk assessment. Regul Toxicol Pharmacol. 24(2 Pt 1):108–120.
  • Durham SK, Castleman WL. 1985. Pulmonary lesions induced by 3-methylindole in mice. Am J Pathol. 121(1):128–137.
  • EPA US. 2003. Toxicological review of hydrogen sulphide (CAS No. 7783-06-4). US Environmental Protection Agency. EPA/635/R-03/005.
  • Fahn S. 2003. Description of Parkinson's disease as a clinical syndrome. Ann N Y Acad Sci. 991(1):1–14.
  • Fink SL, Cookson BT. 2005. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immunity. 73(4):1907–1916.
  • Gandhirajan RK, Rödder K, Bodnar Y, Pasqual-Melo G, Emmert S, Griguer CE, Weltmann K-D, Bekeschus S. 2018. Cytochrome C oxidase inhibition and cold plasma-derived oxidants synergize in melanoma cell death induction. Sci Rep. 8(1):12734.
  • Glass DC. 1990. A review of the health effects of hydrogen sulphide exposure. Ann Occup Hyg. 34(3):323–327.
  • Godoy JA, Rios JA, Zolezzi JM, Braidy N, Inestrosa NC. 2014. Signaling pathway cross talk in Alzheimer's disease. Cell Commun Signal. 12(1):23.
  • Gorman AM. 2008. Neuronal cell death in neurodegenerative diseases: recurring themes around protein handling. J Cell Mol Med. 12(6A):2263–2280.
  • Green F, Schurch S, De Sanctis G, Wallace J, Cheng S, Prior M. 1991. Effects of hydrogen sulfide exposure on surface properties of lung surfactant. J Appl Physiol (1985). 70(5):1943–1949.
  • Guidotti TL. 2015. Hydrogen sulfide intoxication. Handbook of clinical neurology. New York, NY: Elsevier; p. 111–133.
  • Hannah RS, Hayden LJ, Roth SH. 1989. Hydrogen sulfide exposure alters the amino acid content in developing rat CNS. Neurosci Lett. 99(3):323–327.
  • Hardisty JF, Garman RH, Harkema JR, Lomax LG, Morgan KT. 1999. Histopathology of nasal olfactory mucosa from selected inhalation toxicity studies conducted with volatile chemicals. Toxicol Pathol. 27(6):618–627.
  • Harkema JR, Carey SA, Wagner JG. 2006. The nose revisited: a brief review of the comparative structure, function, and toxicologic pathology of the nasal epithelium. Toxicol Pathol. 34(3):252–269.
  • Hartwig A. 2013. Hydrogen sulfide [MAK Value Documentation, 2013]. The MAK-collection for occupational health and safety: Part I: MAK value documentations. New York, NY: John Wiley & Sons.
  • Health Council of the Netherlands. 2006. Hydrogen sulphide; Health-based recommended occupational exposure limit in the Netherlands; publication no. 2006/07OSH.
  • Holsapple MP, Pitot HC, Cohen SM, Cohen SH, Boobis AR, Klaunig JE, Pastoor T, Dellarco VL, Dragan YP. 2006. Mode of action in relevance of rodent liver tumors to human cancer risk. Toxicol Sci. 89(1):51–56.
  • Huart C, Rombaux P, Hummel T. 2013. Plasticity of the human olfactory system: the olfactory bulb. Molecules. 18(9):11586–11600.
  • Huh D, Leslie DC, Matthews BD, Fraser JP, Jurek S, Hamilton GA, Thorneloe KS, McAlexander MA, Ingber DE. 2012. A human disease model of drug toxicity-induced pulmonary edema in a lung-on-a-chip microdevice . Sci Transl Med. 4(159):159ra147.
  • Imaizumi N, Lee KK, Zhang C, Boelsterli UA. 2015. Mechanisms of cell death pathway activation following drug-induced inhibition of mitochondrial complex I. Redox Biol. 4:279–288.
  • Jia C, Roman C, Hegg CC. 2010. Nickel sulfate induces location-dependent atrophy of mouse olfactory epithelium: protective and proliferative role of purinergic receptor activation. Toxicol Sci. 115(2):547–556.
  • Kann O, Kovács R. 2007. Mitochondria and neuronal activity. Am J Physiol Cell Physiol. 292(2):C641–C657.
  • Khan A, Coppock R, Schuler M, Prior M. 1998. Biochemical effects of subchronic repeated exposures to low and moderate concentrations of hydrogen sulfide in Fischer 344 rats. Inhalation Toxicol. 10(11):1037–1044.
  • Khan AA, Schuler MM, Prior MG, Yong S, Coppock RW, Florence LZ, Lillie LE. 1990. Effects of hydrogen sulfide exposure on lung mitochondrial respiratory chain enzymes in rats. Toxicol Appl Pharmacol. 103(3):482–490.
  • Khan AA, Yong S, Prior MG, Lillie LE. 1991. Cytotoxic effects of hydrogen sulfide on pulmonary alveolar macrophages in rats. J Toxicol Environ Health. 33(1):57–64.
  • Kim J-W, Hong S-L, Lee CH, Jeon E-H, Choi A-R. 2010. Relationship between olfactory function and olfactory neuronal population in C57BL6 mice injected intraperitoneally with 3-methylindole. Otolaryngol Head Neck Surg. 143(6):837–842.
  • Kleinstreuer NC, Sullivan K, Allen D, Edwards S, Mendrick DL, Embry M, Matheson J, Rowlands JC, Munn S, Maull E, et al. 2016. Adverse outcome pathways: from research to regulation scientific workshop report. Regul Toxicol Pharmacol. 76:39–50.
  • Kohno M, Tanaka E, Nakamura T, Shimojo N, Misawa S. 1991. Influence of the short-term inhalation of hydrogen sulfide in rats. Eisei Kagaku. 37(2):103–106.
  • Kombian S, Warenycia M, Mele F, Reiffenstein R. 1988. Effects of acute intoxication with hydrogen sulfide on central amino acid transmitter systems. Neurotoxicology. 9(4):587–595.
  • Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke E, Blagosklonny M, El-Deiry W, Golstein P, Green DJCd, et al. Nomenclature Committee on Cell Death 2009. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 16(1):3–11.
  • Kühlbrandt W. 2015. Structure and function of mitochondrial membrane protein complexes. BMC Biol. 13(1):89.
  • Leist M, Ghallab A, Graepel R, Marchan R, Hassan R, Bennekou SH, Limonciel A, Vinken M, Schildknecht S, Waldmann T, et al. 2017. Adverse outcome pathways: opportunities, limitations and open questions. Arch Toxicol. 91(11):3477–3505.
  • Liang HL, Whelan HT, Eells JT, Meng H, Buchmann E, Lerch-Gaggl A, Wong-Riley M. 2006. Photobiomodulation partially rescues visual cortical neurons from cyanide-induced apoptosis. Neuroscience. 139(2):639–649.
  • Lopez A, Prior M, Lillie LE, Gulayets C, Atwal OS. 1988. Histologic and ultrastructural alterations in lungs of rats exposed to sub-lethal concentrations of hydrogen sulfide. Vet Pathol. 25(5):376–384.
  • Lopez A, Prior M, Yong S, Albassam M, Lillie LE. 1987. Biochemical and cytologic alterations in the respiratory tract of rats exposed for 4 hours to hydrogen sulfide. Fundam Appl Toxicol: Off J Soc Toxicol. 9(4):753–762.
  • Lund O, Wieland H. 1966. Pathologic-anatomic findings in experimental hydrogen sulfide poisoning (H2S). A study on rhesus monkeys. Internationales Archiv Fur Arbeitsmedizin. 22(1):46–54.
  • Mattson MP. 2004. Pathways towards and away from Alzheimer's disease. Nature. 430(7000):631–639.
  • McManus MJ, Murphy MP, Franklin JL. 2011. The mitochondria-targeted antioxidant MitoQ prevents loss of spatial memory retention and early neuropathology in a transgenic mouse model of Alzheimer's disease. J Neurosci. 31(44):15703–15715.
  • Meek M, Boobis A, Cote I, Dellarco V, Fotakis G, Munn S, Seed J, Vickers C. 2014. New developments in the evolution and application of the WHO/IPCS framework on mode of action/species concordance analysis. J Appl Toxicol. 34(1):1–18.
  • Milby TH, Baselt RC. 1999. Hydrogen sulfide poisoning: clarification of some controversial issues. Am J Ind Med. 35(2):192–195.
  • Monticello TM, Morgan KT, Uraih L. 1990. Nonneoplastic nasal lesions in rats and mice. Environ Health Perspect. 85:249–274.
  • Moon Y, Lee KH, Park J-H, Geum D, Kim K. 2005. Mitochondrial membrane depolarization and the selective death of dopaminergic neurons by rotenone: protective effect of coenzyme Q10. J Neurochem. 93(5):1199–1208.
  • Murray J. 2011. Pulmonary edema: pathophysiology and diagnosis. Int J Tuberc Lung Dis. 15(2):155–160.
  • Nicholson RA, Roth SH, Zhang A, Zheng J, Brookes J, Skrajny B, Bennington R. 1998. Inhibition of respiratory and bioenergetic mechanisms by hydrogen sulfide in mammalian brain. J Toxicol Environ Health, Part A. 54(6):491–507.
  • OECD. 2018. Users' handbook supplement to the guidance document for developing and assessing adverse outcome pathways. OECD Series on Adverse Outcome Pathways, No. 1. Paris: OECD Publishing. DOI:https://doi.org/10.1787/5jlv1m9d1g32-en.
  • Ohsawa I, Nishimaki K, Murakami Y, Suzuki Y, Ishikawa M, Ohta S. 2008. Age-dependent neurodegeneration accompanying memory loss in transgenic mice defective in mitochondrial aldehyde dehydrogenase 2 activity. J Neurosci. 28(24):6239–6249.
  • Ohta S, Ohsawa I. 2006. Dysfunction of mitochondria and oxidative stress in the pathogenesis of Alzheimer's disease: on defects in the cytochrome c oxidase complex and aldehyde detoxification. J Alzheimers Dis. 9(2):155–166. ].
  • O'Neill HC, Orlicky DJ, Hendry-Hofer TB, Loader JE, Day BJ, White CW. 2011. Role of reactive oxygen and nitrogen species in olfactory epithelial injury by the sulfur mustard analogue 2-chloroethyl ethyl sulfide. Am J Respir Cell Mol Biol. 45(2):323–331.
  • Partlo LA, Sainsbury RS, Roth SH. 2001. Effects of repeated hydrogen sulphide (H2S) exposure on learning and memory in the adult rat. Neurotoxicology. 22(2):177–189.
  • Patlewicz G, Kuseva C, Kesova A, Popova I, Zhechev T, Pavlov T, Roberts DW, Mekenyan O. 2014. Towards AOP application-implementation of an integrated approach to testing and assessment (IATA) into a pipeline tool for skin sensitization. Regul Toxicol Pharmacol. 69(3):529–545.
  • Piccirillo VJ, Bird MG, Lewis RJ, Bover WJ. 2012. Preliminary evaluation of the human relevance of respiratory tumors observed in rodents exposed to naphthalene. Regul Toxicol Pharmacol. 62(3):433–440.
  • Pistollato F, de Gyves EM, Carpi D, Bopp SK, Nunes C, Worth A, Bal-Price A. 2020. Assessment of developmental neurotoxicity induced by chemical mixtures using an adverse outcome pathway concept. Environ Health. 19(1):23.
  • Prior M, Green F, Lopez A, Balu A, De Sanctis GT, Fick G. 1990. Capsaicin pretreatment modifies hydrogen sulphide-induced pulmonary injury in rats. Toxicol Pathol. 18(2):279–288.
  • Proctor DM, Gatto NM, Hong SJ, Allamneni KP. 2007. Mode-of-action framework for evaluating the relevance of rodent forestomach tumors in cancer risk assessment. Toxicol Sci. 98(2):313–326.
  • Reiffenstein RJ, Hulbert WC, Roth SH. 1992. Toxicology of hydrogen sulfide. Annu Rev Pharmacol Toxicol. 32:109–134.
  • Rhomberg LR, Bailey LA, Goodman JE. 2010. Hypothesis-based weight of evidence: a tool for evaluating and communicating uncertainties and inconsistencies in the large body of evidence in proposing a carcinogenic mode of action-naphthalene as an example. Crit Rev Toxicol. 40(8):671–696.
  • Ricci JE, Waterhouse N, Green DR. 2003. Mitochondrial functions during cell death, a complex (I-V) dilemma. Cell Death Differ. 10(5):488–492.
  • Romashko J, Horowitz S, Franek WR, Palaia T, Miller EJ, Lin A, Birrer MJ, Scott W, Mantell LL. 2003. MAPK pathways mediate hyperoxia-induced oncotic cell death in lung epithelial cells. Free Radic Biol Med. 35(8):978–993.
  • Rugarli EI, Langer T. 2012. Mitochondrial quality control: a matter of life and death for neurons. Embo J. 31(6):1336–1349.
  • Rumbeiha W, Whitley E, Anantharam P, Kim DS, Kanthasamy A. 2016. Acute hydrogen sulfide-induced neuropathology and neurological sequelae: challenges for translational neuroprotective research. Ann N Y Acad Sci. 1378(1):5–16.
  • Sasajima H, Miyazono S, Noguchi T, Kashiwayanagi M. 2015. Intranasal administration of rotenone in mice attenuated olfactory functions through the lesion of dopaminergic neurons in the olfactory bulb. NeuroToxicology. 51:106–115.
  • Savolainen H, Tenhunen R, Elovaara E, Tossavainen A. 1980. Cumulative biochemical effects of repeated subclinical hydrogen sulfide intoxication in mouse brain. Int Arch Occup Environ Health. 46(1):87–92. ].
  • Schneider JS, Tobe EH, Mozley PD Jr, Barniskis L, Lidsky TI. 1998. Persistent cognitive and motor deficits following acute hydrogen sulphide poisoning. Occup Med (Lond). 48(4):255–260.
  • SCOEL. 2007. Recommendation from the Scientific Committee on Occupational Exposure Limits (SCOEL) for Hydrogen Sulphide. European Commission. SCOEL/SUM/124.
  • Selvatici R, Previati M, Marino S, Marani L, Falzarano S, Lanzoni I, Siniscalchi A. 2009. Sodium azide induced neuronal damage in vitro: evidence for non-apoptotic cell death. Neurochem Res. 34(5):909–916.
  • Skrajny B, Reiffenstein RJ, Sainsbury RS, Roth SH. 1996. Effects of repeated exposures of hydrogen sulphide on rat hippocampal EEG. Toxicol Lett. 84(1):43–53.
  • Stevenson RJ. 2010. An initial evaluation of the functions of human olfaction. Chem Senses. 35(1):3–20.
  • Struve MF, Brisbois JN, James RA, Marshall MW, Dorman DC. 2001. Neurotoxicological effects associated with short-term exposure of Sprague-Dawley rats to hydrogen sulfide. Neurotoxicology. 22(3):375–385.
  • Tawara T, Fukushima T, Hojo N, Isobe A, Shiwaku K, Setogawa T, Yamane Y. 1996. Effects of paraquat on mitochondrial electron transport system and catecholamine contents in rat brain. Arch Toxicol. 70(9):585–589. ].
  • Teeguarden JG. 2017. AOP136: intracellular acidification induced olfactory epithelial injury leading to site of contact nasal tumors (status as of 5 July 2019: "Open for citation & Comment"). Last modified 20 March 2017. https://aopwiki.org/aops/136.
  • Tvedt B, Edland A, Skyberg K, Forberg O. 1991. Delayed neuropsychiatric sequelae after acute hydrogen sulfide poisoning: affection of motor function, memory, vision and hearing. Acta Neurol Scand. 84(4):348–351.
  • van Aalst JA, Isakov R, Polk JD, Van Antwerp AD, Yang M, Fratianne RB. 2000. Hydrogen sulfide inhalation injury. J Burn Care Rehabil. 21(3):248–253.
  • Veereshwarayya V, Kumar P, Rosen KM, Mestril R, Querfurth HW. 2006. Differential effects of mitochondrial heat shock protein 60 and related molecular chaperones to prevent intracellular beta-amyloid-induced inhibition of complex IV and limit apoptosis. J Biol Chem. 281(40):29468–29478.
  • Villeneuve DL, Crump D, Garcia-Reyero N, Hecker M, Hutchinson TH, LaLone CA, Landesmann B, Lettieri T, Munn S, Nepelska M, et al. 2014a. Adverse Outcome Pathway (AOP) Development I: strategies and principles. Toxicol Sci. 142(2):312–320.
  • Villeneuve DL, Crump D, Garcia-Reyero N, Hecker M, Hutchinson TH, LaLone CA, Landesmann B, Lettieri T, Munn S, Nepelska M, et al. 2014b. Adverse outcome pathway development II: best practices. Toxicol Sci. 142(2):321–330.
  • Wallace DCJS. 1999. Mitochondrial diseases in man and mouse. Science. 283(5407):1482–1488.
  • Warenycia MW, Smith KA, Blashko CS, Kombian SB, Reiffenstein RJ. 1989. Monoamine oxidase inhibition as a sequel of hydrogen sulfide intoxication: increases in brain catecholamine and 5-hydroxytryptamine levels. Arch Toxicol. 63(2):131–136.
  • Wasch HH, Estrin WJ, Yip P, Bowler R, Cone JE. 1989. Prolongation of the P-300 latency associated with hydrogen sulfide exposure. Arch Neurol. 46(8):902–904.
  • Wei H, Leeds PR, Qian Y, Wei W, Chen R-w, Chuang D-M. 2000. β-Amyloid peptide-induced death of PC 12 cells and cerebellar granule cell neurons is inhibited by long-term lithium treatment. Eur J Pharmacol. 392(3):117–123.
  • Wolfe MS. 2018. Chapter 1 – Solving the puzzle of neurodegeneration. In: Wolfe MS, editor. The molecular and cellular basis of neurodegenerative diseases. London: Academic Press; p. 1–22.
  • Wu N, Du X, Wang D, Hao F. 2011. Myocardial and lung injuries induced by hydrogen sulfide and the effectiveness of oxygen therapy in rats. Clin Toxicol. 49(3):161–166.
  • Yee S, Choi BH. 1996. Oxidative stress in neurotoxic effects of methylmercury poisoning. Neurotoxicology. 17(1):17–26.
  • Youngentob SL, Schwob JE, Sheehe PR, Youngentob LM. 1997. Odorant threshold following methyl bromide-induced lesions of the olfactory epithelium. Physiol Behav. 62(6):1241–1252.
  • Zhang X, Bian J-S. 2014. Hydrogen sulfide: a neuromodulator and neuroprotectant in the central nervous system. ACS Chem Neurosci. 5(10):876–883.
  • Ziabreva I, Campbell G, Rist J, Zambonin J, Rorbach J, Wydro MM, Lassmann H, Franklin RJM, Mahad D. 2010. Injury and differentiation following inhibition of mitochondrial respiratory chain complex IV in rat oligodendrocytes. Glia. 58(15):1827–1837.