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

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Translational Neurodegeneration
Published in: Translational Neurodegeneration 1/2018

Open Access 01-12-2018 | Review

Hydrogen sulfide, nitric oxide, and neurodegenerative disorders

Authors: Sandesh Panthi, Sumeet Manandhar, Kripa Gautam

Published in: Translational Neurodegeneration | Issue 1/2018

Login to get access

Abstract

Hydrogen Sulfide (H2S) and Nitric Oxide (NO) have become recognized as important gaseous signaling molecules with enormous pharmacological effects, therapeutic value, and central physiological roles. NO is one of the most important regulators of the pathophysiological condition in central nervous system (CNS). It is critical in the various functioning of the brain; however, beyond certain concentration/level, it is toxic. H2S was regarded as toxic gas with the smell like rotten egg. But, it is now regarded as emerging neuroprotectant and neuromodulator. Recently, the use of donors and inhibitors of these signaling molecules have helped us to identify their accurate and precise biological effects. The most abundant neurotransmitter of CNS (glutamate) is the initiator of the reaction that forms NO, and H2S is highly expressed in brain. These molecules are shedding light on the pathogenesis of various neurological disorders. This review is mainly focused on the importance of H2S and NO for normal functioning of CNS.
Literature
1.
Li L, Moore PK. An overview of the biological significance of endogenous gases: new roles for old molecules. Portland Press Limited. 2007;
2.
Fukuto JM, Carrington SJ, Tantillo DJ, Harrison JG, Ignarro LJ, Freeman BA, et al. Small molecule signaling agents: the integrated chemistry and biochemistry of nitrogen oxides, oxides of carbon, dioxygen, hydrogen sulfide, and their derived species. Chem Res Toxicol. 2012;25:769–93.PubMedPubMedCentralCrossRef
3.
Wang RUI. Two’s company, three’sa crowd: can H2S be the third endogenous gaseous transmitter? FASEB J. 2002;16:1792–8.PubMedCrossRef
4.
Wang R. Signal transduction and the Gasotransmitters: NO, CO, and H2S in biology and medicine. Springer Science & Business Media; 2004.CrossRef
5.
Rajfer J, Aronson WJ, Bush PA, Dorey FJ, Ignarro LJ. Nitric oxide as a mediator of relaxation of the corpus cavernosum in response to nonadrenergic, noncholinergic neurotransmission. N Engl J Med Mass Medical Soc. 1992;326:90–4.CrossRef
6.
Cech TR, Bennett D, Jasny B, Kelner KL, Miller LJ, Szuromi PD, et al. The molecule of the year. Science. 1992;258:1861.CrossRef
7.
Zhou L, Zhu D-Y. Neuronal nitric oxide synthase: structure, subcellular localization, regulation, and clinical implications. Nitric Oxide. 2009;20:223–30.PubMedCrossRef
8.
Tinajero-Trejo M, Jesse HE, Poole RK. Gasotransmitters, poisons, and antimicrobials: it’s a gas, gas, gas! F1000Prime Rep 2013;5.
9.
Motterlini R, Otterbein LE. The therapeutic potential of carbon monoxide. Nat Rev Drug Discov. 2010;9:728–43.PubMedCrossRef
10.
Carbon MBE. Monoxide: an essential signaling molecule. Med. Organomet Chem. 2010:247–85.
11.
Kashfi K, Olson KR. Biology and therapeutic potential of hydrogen sulfide and hydrogen sulfide-releasing chimeras. Biochem Pharmacol. 2013;85:689–703.PubMedCrossRef
12.
Kajimura M, Fukuda R, Bateman RM, Yamamoto T, Suematsu M. Interactions of multiple gas-transducing systems: hallmarks and uncertainties of CO, NO, and H2S gas biology. Antioxid Redox Signal. 2010;13:157–92.PubMedPubMedCentralCrossRef
13.
Furne J, Saeed A, Levitt MD. Whole tissue hydrogen sulfide concentrations are orders of magnitude lower than presently accepted values. Am J Phys. 2008;295:1479–85.
14.
Panthi S, Chung H-J, Jung J, Jeong NY. Physiological importance of hydrogen sulfide: emerging potent neuroprotector and neuromodulator. Oxidative Med Cell Longev. 2016;2016
15.
16.
Shefa U, Yeo SG, Kim M-S, Song IO, Jung J, Jeong NY, et al. Role of Gasotransmitters in oxidative stresses, Neuroinflammation, and neuronal repair. Biomed Res Int. 2017;2017
17.
Cirino G, Vellecco V, Bucci M. Nitric oxide and hydrogen sulfide: the gasotransmitter paradigm of the vascular system. Br J Pharmacol. 2017;
18.
Qian Y, Matson JB. Gasotransmitter delivery via self-assembling peptides: treating diseases with natural signaling gases. Adv Drug Deliv Rev. 2017;110:137–56.PubMedCrossRef
19.
Szabo C. Gasotransmitters in cancer: from pathophysiology to experimental therapy. Nat Rev Drug Discov. 2016;15:185–203.PubMedCrossRef
20.
Knowles RG, Palacios M, Palmer RM, Moncada S. Formation of nitric oxide from L-arginine in the central nervous system: a transduction mechanism for stimulation of the soluble guanylate cyclase. Proc Natl Acad Sci. 1989;86:5159–62.PubMedPubMedCentralCrossRef
21.
Garry PS, Ezra M, Rowland MJ, Westbrook J, Pattinson KTS. The role of the nitric oxide pathway in brain injury and its treatment—from bench to bedside. Exp Neurol. 2015;263:235–43.PubMedCrossRef
22.
Calabrese V, Mancuso C, Calvani M, Rizzarelli E, Butterfield DA, Stella AMG. Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat Rev Neurosci. 2007;8:766–75.PubMedCrossRef
23.
Boissel J-P, Schwarz PM, Förstermann U. Neuronal-type NO synthase: transcript diversity and expressional regulation. Nitric Oxide. 1998;2:337–49.PubMedCrossRef
24.
25.
Garthwaite J, Boulton CL. Nitric oxide signaling in the central nervous system. Annu Rev Physiol. 1995;57:683–706.PubMedCrossRef
26.
Tieu K, Ischiropoulos H, Przedborski S. Nitric oxide and reactive oxygen species in Parkinson’s disease. IUBMB Life. 2003;55:329–35.PubMedCrossRef
27.
Bredt DS, Glatt CE, Hwang PM, Fotuhi M, Dawson TM, Snyder SH. Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron. 1991;7:615–24.PubMedCrossRef
28.
Wang H-G, Lu F-M, Jin I, Udo H, Kandel ER, de Vente J, et al. Presynaptic and postsynaptic roles of NO, cGK, and RhoA in long-lasting potentiation and aggregation of synaptic proteins. Neuron. 2005;45:389–403.PubMedCrossRef
29.
Pautz A, Art J, Hahn S, Nowag S, Voss C, Kleinert H. Regulation of the expression of inducible nitric oxide synthase. Nitric Oxide. 2010;23:75–93.PubMedCrossRef
30.
Raju K, Ischiropoulos H. Gaseous Signaling in the Central Nervous System. Neurosci. 21st Century. 2016;1–16.
31.
Chachlaki K, Garthwaite J, Prevot V. The gentle art of saying NO: how nitric oxide gets things done in the hypothalamus. Nat Rev Endocrinol. 2017;13:521.PubMedCrossRef
32.
Yamamoto K, Takei H, Koyanagi Y, Koshikawa N, Kobayashi M. Presynaptic cell type-dependent regulation of GABAergic synaptic transmission by nitric oxide in rat insular cortex. Neuroscience. 2015;284:65–77.PubMedCrossRef
33.
Yassin L, Radtke-Schuller S, Asraf H, Grothe B, Hershfinkel M, Forsythe ID, et al. Nitric oxide signaling modulates synaptic inhibition in the superior paraolivary nucleus (SPN) via cGMP-dependent suppression of KCC2. Front Neural Circuits. 2014;8
34.
Puzzo D, Vitolo O, Trinchese F, Jacob JP, Palmeri A, Arancio O. Amyloid-β peptide inhibits activation of the nitric oxide/cGMP/cAMP-responsive element-binding protein pathway during hippocampal synaptic plasticity. J Neurosci. 2005;25:6887–97.PubMedCrossRef
35.
Su K, Lin S, Wei J, Lee K, Zhao J, Shyue S, et al. The essential role of transient receptor potential vanilloid 1 in simvastatin-induced activation of endothelial nitric oxide synthase and angiogenesis. Acta Physiol. 2014;212:191–204.CrossRef
36.
Greco R, Amantea D, Blandini F, Nappi G, Bagetta G, Corasaniti MT, et al. Neuroprotective effect of nitroglycerin in a rodent model of ischemic stroke: evaluation of Bcl-2 expression. Int Rev Neurobiol. 2007;82:423–35.PubMedCrossRef
37.
Khan M, Jatana M, Elango C, Paintlia AS, Singh AK, Singh I. Cerebrovascular protection by various nitric oxide donors in rats after experimental stroke. Nitric Oxide. 2006;15:114–24.PubMedCrossRef
38.
Iwanishi K, Watabe H, Hayashi T, Miyake Y, Minato K, Iida H. Influence of residual oxygen-15-labeled carbon monoxide radioactivity on cerebral blood flow and oxygen extraction fraction in a dual-tracer autoradiographic method. Ann Nucl Med. 2009;23:363–71.PubMedCrossRef
39.
Toda N, Ayajiki K, Okamura T. Cerebral blood flow regulation by nitric oxide: recent advances. Pharmacol Rev. 2009;61:62–97.PubMedCrossRef
40.
Kielstein JT, Donnerstag F, Gasper S, Menne J, Kielstein A, Martens-Lobenhoffer J, et al. ADMA increases arterial stiffness and decreases cerebral blood flow in humans. Stroke. 2006;37:2024–9.PubMedCrossRef
41.
Kawamoto EM, Vasconcelos AR, Degaspari S, Böhmer AE, Scavone C, Marcourakis T. Age-related changes in nitric oxide activity, cyclic GMP, and TBARS levels in platelets and erythrocytes reflect the oxidative status in central nervous system. Age. 2013;35:331–42.PubMedCrossRef
42.
Biojone C, Cabrera Casarotto P, Regiane Joca S, Castren E. Interplay between nitric oxide and brain-derived neurotrophic factor in neuronal plasticity. CNS Neurol Disord Targets. 2015;14:979–87.CrossRef
43.
Kakizawa S, Yamazawa T, Chen Y, Ito A, Murayama T, Oyamada H, et al. Nitric oxide-induced calcium release via ryanodine receptors regulates neuronal function. EMBO J. 2012;31:417–28.PubMedCrossRef
44.
Lev-Ram V, Jiang T, Wood J, Lawrence DS, Tsien RY. Synergies and coincidence requirements between NO, cGMP, and ca 2+ in the induction of cerebellar long-term depression. Neuron. 1997;18:1025–38.PubMedCrossRef
45.
Lev-Ram V, Wong ST, Storm DR, Tsien RY. A new form of cerebellar long-term potentiation is postsynaptic and depends on nitric oxide but not cAMP. Proc Natl Acad Sci. 2002;99:8389–93.PubMedPubMedCentralCrossRef
46.
Katoh A, Kitazawa H, Itohara S, Nagao S. Inhibition of nitric oxide synthesis and gene knockout of neuronal nitric oxide synthase impaired adaptation of mouse optokinetic response eye movements. Learn Mem. 2000;7:220–6.PubMedPubMedCentralCrossRef
47.
Gautier-Sauvigné S, Colas D, Parmantier P, Clement P, Gharib A, Sarda N, et al. Nitric oxide and sleep. Sleep Med Rev. 2005;9:101–13.PubMedCrossRef
48.
49.
Benarroch EE. Nitric oxide a pleiotropic signal in the nervous system. Neurology AAN Enterprises. 2011;77:1568–76.
50.
Nakamura T, Gu Z, Lipton SA. Contribution of glutamatergic signaling to nitrosative stress-induced protein misfolding in normal brain aging and neurodegenerative diseases. Aging Cell. 2007;6:351–9.PubMedCrossRef
51.
Edwards TM, Rickard NS. New perspectives on the mechanisms through which nitric oxide may affect learning and memory processes. Neurosci Biobehav Rev. 2007;31:413–25.PubMedCrossRef
52.
Lüth H-J, Münch G, Arendt T. Aberrant expression of NOS isoforms in Alzheimer’s disease is structurally related to nitrotyrosine formation. Brain Res. 2002;953:135–43.PubMedCrossRef
53.
Malinski T. Nitric oxide and nitroxidative stress in Alzheimer’s disease. J Alzheimers Dis. 2007;11:207–18.PubMedCrossRef
54.
Virarkar M, Alappat L, Bradford PG, Awad AB. L-arginine and nitric oxide in CNS function and neurodegenerative diseases. Crit Rev Food Sci Nutr. 2013;53:1157–67.PubMedCrossRef
55.
Huang Z, Huang PL, Ma J, Meng W, Ayata C, Fishman MC, et al. Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro-L-arginine. J Cereb Blood Flow Metab. 1996;16:981–7.PubMedCrossRef
56.
Lundblad C, Grände P-O, Bentzer P. Hemodynamic and histological effects of traumatic brain injury in eNOS-deficient mice. J Neurotrauma. 2009;26:1953–62.PubMedCrossRef
57.
Robertson CS, Gopinath SP, Valadka AB, Van M, Swank PR, Goodman JC. Variants of the endothelial nitric oxide gene and cerebral blood flow after severe traumatic brain injury. J Neurotrauma. 2011;28:727–37.PubMedPubMedCentralCrossRef
58.
Dezfulian C, Alekseyenko A, Dave KR, Raval AP, Do R, Kim F, et al. Nitrite therapy is neuroprotective and safe in cardiac arrest survivors. Nitric Oxide. 2012;26:241–50.PubMedPubMedCentralCrossRef
59.
60.
Terpolilli NA, Kim S-W, Thal SC, Kuebler WM, Plesnila N. Inhaled nitric oxide reduces secondary brain damage after traumatic brain injury in mice. J Cereb Blood Flow Metab. 2013;33:311–8.PubMedCrossRef
61.
Terpolilli NA, Kim S-W, Thal SC, Kataoka H, Zeisig V, Nitzsche B, et al. Inhalation of nitric oxide prevents ischemic brain damage in experimental stroke by selective dilatation of collateral arterioles. Circ Res. 2011; Circresaha-111
62.
Zhang F, White JG, Iadecola C. Nitric oxide donors increase blood flow and reduce brain damage in focal ischemia: evidence that nitric oxide is beneficial in the early stages of cerebral ischemia. J Cereb Blood Flow Metab. 1994;14:217–26.PubMedCrossRef
63.
Jung K-H, Chu K, Ko S-Y, Lee S-T, Sinn D-I, Park D-K, et al. Early intravenous infusion of sodium nitrite protects brain against in vivo ischemia-reperfusion injury. Stroke. 2006;37:2744–50.PubMedCrossRef
64.
Morikawa E, Moskowitz MA, Huang Z, Yoshida T, Irikura K, Dalkara T. L-arginine infusion promotes nitric oxide-dependent vasodilation, increases regional cerebral blood flow, and reduces infarction volume in the rat. Stroke. 1994;25:429–35.PubMedCrossRef
65.
Li Y-S, Shemmer B, Stone E, Nardi MA, Jonas S, Quartermain D. Neuroprotection by inhaled nitric oxide in a murine stroke model is concentration and duration dependent. Brain Res. 2013;1507:134–45.PubMedCrossRef
66.
Fathi AR, Pluta RM, Bakhtian KD, Qi M, Lonser RR. Reversal of cerebral vasospasm via intravenous sodium nitrite after subarachnoid hemorrhage in primates. J Neurosurg. 2011;115:1213–20.PubMedPubMedCentralCrossRef
67.
Pluta R, Dejam AA, Gladwin M, Oldfiled E. Nitrite infusions prevent delayed cerebral vasospasm in a primate model of subarachnoid hemorrhage. Free Radic Biol Med. 2004;37:S81.
68.
69.
Olivier P, Loron G, Fontaine RH, Pansiot J, Dalous J, Thi HP, et al. Nitric oxide plays a key role in myelination in the developing brain. J Neuropathol Exp Neurol. 2010;69:828–37.PubMedCrossRef
70.
71.
Huang Z, Huang PL, Panahian N, Dalkara T, Fishman MC, Moskowitz MA. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Sci. 1994:1883.
72.
Baruch K, Kertser A, Porat Z, Schwartz M. Cerebral nitric oxide represses choroid plexus NFκB-dependent gateway activity for leukocyte trafficking. EMBO J. 2015;34:1816–28.PubMedPubMedCentralCrossRef
73.
P Fernandez A, Pozo-Rodrigalvarez A, Serrano J, Martinez-Murillo R. Nitric oxide: target for therapeutic strategies in Alzheimer’s disease. Curr Pharm Des. 2010;16:2837–50.CrossRef
74.
de Souza KPR, Silva EG, de Oliveira Rocha ES, Figueiredo LB, de Almeida-Leite CM, Arantes RME, et al. Nitric oxide synthase expression correlates with death in an experimental mouse model of dengue with CNS involvement. Virol J. 2013;10:267.PubMedPubMedCentralCrossRef
75.
Yuste JE, Tarragon E, Campuzano CM, Ros-Bernal F. Implications of glial nitric oxide in neurodegenerative diseases. Front Cell Neurosci. 2015;9
76.
Kimura H, Nagai Y, Umemura K, Kimura Y. Physiological roles of hydrogen sulfide: synaptic modulation, neuroprotection, and smooth muscle relaxation. Antioxid Redox Signal. 2005;7:795–803.PubMedCrossRef
77.
78.
Qu K, Lee SW, Bian JS, Low C-M, Wong PT-H. Hydrogen sulfide: neurochemistry and neurobiology. Neurochem Int. 2008;52:155–65.PubMedCrossRef
79.
Chen X, Jhee KH, Kruger WD. Production of the neuromodulator H2S by cystathionine beta-synthase via the condensation of cysteine and homocysteine. J Biol Chem. 2004;279:52082–6.PubMedCrossRef
80.
Stipanuk MH, Beck PW. Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat. Biochem J. 1982;206:267–77.PubMedPubMedCentralCrossRef
81.
Li L, Moore PK. Putative biological roles of hydrogen sulfide in health and disease: a breath of not so fresh air? Trends Pharmacol Sci. 2008;29:84–90.PubMedCrossRef
82.
Mikami Y, Shibuya N, Kimura Y, Nagahara N, Ogasawara Y, Kimura H. Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide. Biochem J. 2011;439:479–85.PubMedCrossRef
83.
Tang S, Huang D, An N, Chen D, Zhao D. A novel pathway for the production of H 2 S by DAO in rat jejunum. Neurogastroenterol Motil. 2016;
84.
Shibuya N, Koike S, Tanaka M, Ishigami-Yuasa M, Kimura Y, Ogasawara Y, et al. A novel pathway for the production of hydrogen sulfide from D-cysteine in mammalian cells. Nat Commun. 2013;4:1366.PubMedCrossRef
85.
Polhemus DJ, Lefer DJ. Emergence of hydrogen sulfide as an endogenous gaseous signaling molecule in cardiovascular disease. Circ Res. 2014;114:730–7.PubMedPubMedCentralCrossRef
86.
87.
88.
Hermann A, Sitdikova GF, Weiger TM. Gasotransmitters: Physiology and Pathophysiology. 2012.
89.
Tan BH, Wong PT-H, Bian J-S. Hydrogen sulfide: a novel signaling molecule in the central nervous system. Neurochem Int. 2010;56:3–10.PubMedCrossRef
90.
Gong Q-H, Wang Q, Pan L-L, Liu X-H, Huang H, Zhu Y-Z. Hydrogen sulfide attenuates lipopolysaccharide-induced cognitive impairment: a pro-inflammatory pathway in rats. Pharmacol Biochem Behav. 2010;96:52–8.PubMedCrossRef
91.
Tang X, Yang C, Chen J, Yin W, Tian S, Hu B, et al. Effect of hydrogen sulphide on β-amyloid-induced damage in PC12 cells. Clin Exp Pharmacol Physiol. 2008;35:180–6.PubMed
92.
Fan H, Guo Y, Liang X, Yuan Y, Qi X, Wang M, et al. Hydrogen sulfide protects against amyloid beta-peptide induced neuronal injury via attenuating inflammatory responses in a rat model. J Biomed. 2013;27:296.
93.
Xuan A, Long D, Li J, Ji W, Zhang M, Hong L, et al. Hydrogen sulfide attenuates spatial memory impairment and hippocampal neuroinflammation in beta-amyloid rat model of Alzheimer’s disease. J Neuroinflammation. 2012;9:202.PubMedPubMedCentralCrossRef
94.
Eto K, Asada T, Arima K, Makifuchi T, Kimura H. Brain hydrogen sulfide is severely decreased in Alzheimer’s disease. Biochem Biophys Res Commun. 2002;293:1485–8.PubMedCrossRef
95.
Zhang L-M, Jiang C-X, Liu D-W. Hydrogen sulfide attenuates neuronal injury induced by vascular dementia via inhibiting apoptosis in rats. Neurochem Res. 2009;34:1984–92.PubMedCrossRef
96.
Giuliani D, Ottani A, Zaffe D, Galantucci M, Strinati F, Lodi R, et al. Hydrogen sulfide slows down progression of experimental Alzheimer’s disease by targeting multiple pathophysiological mechanisms. Neurobiol Learn Mem. 2013;104:82–91.PubMedCrossRef
97.
Schreier SM, Muellner MK, Steinkellner H, Hermann M, Esterbauer H, Exner M, et al. Hydrogen sulfide scavenges the cytotoxic lipid oxidation product 4-HNE. Neurotox Res. 2010;17:249–56.PubMedCrossRef
98.
Kida K, Ichinose F. Hydrogen sulfide and neuroinflammation. Chem Biochem Pharmacol Hydrog Sulfide. 2015:181–9.
99.
Kida K, Yamada M, Tokuda K, Marutani E, Kakinohana M, Kaneki M, et al. Inhaled hydrogen sulfide prevents neurodegeneration and movement disorder in a mouse model of Parkinson’s disease. Antioxid Redox Signal. 2011;15:343–52.PubMedPubMedCentralCrossRef
100.
Hu L, Lu M, Tiong CX, Dawe GS, Hu G, Bian J. Neuroprotective effects of hydrogen sulfide on Parkinson’s disease rat models. Aging Cell. 2010;9:135–46.PubMedCrossRef
101.
Xie L, Hu L-F, Teo XQ, Tiong CX, Tazzari V, Sparatore A, et al. Therapeutic effect of hydrogen sulfide-releasing L-Dopa derivative ACS84 on 6-OHDA-induced Parkinson’s disease rat model. PLoS One. 2013;8:e60200.PubMedPubMedCentralCrossRef
102.
Cao X, Cao L, Ding L, Bian J. A new hope for a devastating disease: hydrogen sulfide in Parkinson’s disease. Mol Neurobiol. 2017:1–11.
103.
Karimi SA, Hosseinmardi N, Janahmadi M, Sayyah M, Hajisoltani R. The protective effect of hydrogen sulfide (H2S) on traumatic brain injury (TBI) induced memory deficits in rats. Brain Res Bull. 2017;134:177–82.PubMedCrossRef
104.
Borgens R. Ben, Liu-Snyder P. Understanding secondary injury Q Rev Biol. 2012;87:89–127.PubMed
105.
Mustafa AG, Alshboul OA. Pathophysiology of traumatic brain injury. Neurosci. 2013;18:222–34.
106.
Homsi S, Federico F, Croci N, Palmier B, Plotkine M, Marchand-Leroux C, et al. Minocycline effects on cerebral edema: relations with inflammatory and oxidative stress markers following traumatic brain injury in mice. Brain Res. 2009;1291:122–32.PubMedCrossRef
107.
Zhang M, Shan H, Wang T, Liu W, Wang Y, Wang L, et al. Dynamic change of hydrogen sulfide after traumatic brain injury and its effect in mice. Neurochem Res. 2013;38:714–25.PubMedCrossRef
108.
Dai H-B, Xu M-M, Lv J, Ji X-J, Zhu S-H, Ma R-M, et al. Mild hypothermia combined with hydrogen sulfide treatment during resuscitation reduces hippocampal neuron apoptosis via NR2A, NR2B, and PI3K-Akt signaling in a rat model of cerebral ischemia-reperfusion injury. Mol Neurobiol. 2016;53:4865–73.PubMedCrossRef
109.
Li T, Liu H, Xue H, Zhang J, Han X, Yan S, et al. Neuroprotective effects of hydrogen sulfide against early brain injury and secondary cognitive deficits following subarachnoid hemorrhage. Brain Pathol. 2016;
110.
Yonezawa D, Sekiguchi F, Miyamoto M, Taniguchi E, Honjo M, Masuko T, et al. A protective role of hydrogen sulfide against oxidative stress in rat gastric mucosal epithelium. Toxicology. 2007;241:11–8.PubMedCrossRef
111.
Chu Q-J, He L, Zhang W, Liu C-L, Ai Y-Q, Zhang Q. Hydrogen sulfide attenuates surgical trauma-induced inflammatory response and cognitive deficits in mice. J Surg Res. 2013;183:330–6.PubMedCrossRef
112.
Zhang M, Shan H, Chang P, Wang T, Dong W, Chen X, et al. Hydrogen sulfide offers neuroprotection on traumatic brain injury in parallel with reduced apoptosis and autophagy in mice. PLoS One. 2014;9:e87241.PubMedPubMedCentralCrossRef
113.
Paul BD, Sbodio JI, Xu R, Vandiver MS, Cha JY, Snowman AM, et al. Cystathionine gamma-lyase deficiency mediates neurodegeneration in Huntington’s disease. Nature. 2014;509:96–100.PubMedPubMedCentralCrossRef
114.
Paul BD, Snyder SH. Role Of neuronal signaling effector hydrogen sulfide (H2S) and sulfhydration in Huntington’s disease. FASEB J. 2016;30:1271–6.CrossRef
115.
116.
Deng J, Lei C, Chen Y, Fang Z, Yang Q, Zhang H, et al. Neuroprotective gases–fantasy or reality for clinical use? Prog Neurobiol. 2014;115:210–45.PubMedCrossRef
117.
Mikami Y, Shibuya N, Kimura Y, Nagahara N, Yamada M, Kimura H. Hydrogen sulfide protects the retina from light-induced degeneration by the modulation of Ca2+ influx. J Biol Chem. 2011;286:39379–86.PubMedPubMedCentralCrossRef
118.
119.
Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci. 1996;16:1066–71.PubMed
120.
Lee SW, Hu Y-S, Hu L-F, Lu Q, Dawe GS, Moore PK, et al. Hydrogen sulphide regulates calcium homeostasis in microglial cells. Glia. 2006;54:116–24.PubMedCrossRef
121.
Geng B, Chang L, Pan C, Qi Y, Zhao J, Pang Y, et al. Endogenous hydrogen sulfide regulation of myocardial injury induced by isoproterenol. Biochem Biophys Res Commun. 2004;318:756–63.PubMedCrossRef
122.
White BJO. The vascular effects of hydrogen sulphide. 2012.
123.
124.
Coletta C, Papapetropoulos A, Erdelyi K, Olah G, Módis K, Panopoulos P, et al. Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc Natl Acad Sci. 2012;109:9161–6.PubMedPubMedCentralCrossRef
125.
126.
Nagpure BV, Interaction BJ-S. Of hydrogen sulfide with nitric oxide in the cardiovascular system. Oxidative Med Cell Longev. 2015;2016
127.
Furchgott RF, Jothianandan D. Endothelium-dependent and-independent vasodilation involving cyclic GMP: relaxation induced by nitric oxide, carbon monoxide and light. J Vasc Res. 1991;28:52–61.CrossRef
128.
Taoka S, Banerjee R. Characterization of NO binding to human cystathionine β-synthase:: Possible implications of the effects of CO and NO binding to the human enzyme. J Inorg Biochem. 2001;87:245–51.PubMedCrossRef
129.
130.
Beltowski J, Jamroz-Wiśnniewska A. Hydrogen sulfide and endothelium-dependent vasorelaxation. Molecules. 2014;19:21506–28.CrossRef
131.
Broos K, Feys HB, De Meyer SF, Vanhoorelbeke K, Deckmyn H. Platelets at work in primary hemostasis. Blood Rev. 2011;25:155–67.PubMedCrossRef
Metadata
Title
Hydrogen sulfide, nitric oxide, and neurodegenerative disorders
Authors
Sandesh Panthi
Sumeet Manandhar
Kripa Gautam
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Translational Neurodegeneration / Issue 1/2018
Electronic ISSN: 2047-9158
DOI
https://doi.org/10.1186/s40035-018-0108-x

Other articles of this Issue 1/2018

Translational Neurodegeneration 1/2018 Go to the issue

Research

Efficacy and safety of rasagiline in Chinese patients with early Parkinson’s disease: a randomized, double-blind, parallel, placebo-controlled, fixed-dose study

Research

Bis(9)-(−)-Meptazinol, a novel dual-binding AChE inhibitor, rescues cognitive deficits and pathological changes in APP/PS1 transgenic mice

Research

Cerebrospinal fluid phosphorylated tau, visinin-like protein-1, and chitinase-3-like protein 1 in mild cognitive impairment and Alzheimer’s disease

Review

Exercise-induced increase in brain-derived neurotrophic factor in human Parkinson's disease: a systematic review and meta-analysis

Research

Ultra-High Field Diffusion MRI Reveals Early Axonal Pathology in Spinal Cord of ALS mice

Research

Divergent topological networks in Alzheimer’s disease: a diffusion kurtosis imaging analysis