• Users Online: 235
  • Home
  • Print this page
  • Email this page


 
 Table of Contents  
REVIEW
Year : 2019  |  Volume : 9  |  Issue : 2  |  Page : 88-92

The role of hydrogen sulfide in gastric mucosal damage


1 Department of Neurosurgery & Brain and Nerve Research Laboratory, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu Province, China
2 Department of Neurosurgery, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu Province, China

Date of Submission04-Dec-2018
Date of Acceptance15-Apr-2019
Date of Web Publication25-Jun-2019

Correspondence Address:
Mei-Fen Shen
Department of Neurosurgery, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu Province
China
Zhong Wang
Department of Neurosurgery & Brain and Nerve Research Laboratory, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu Province
China
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2045-9912.260650

Rights and Permissions
  Abstract 


Gastrointestinal disease is a major global threat to public health. In the past few decades, numerous studies have focuses on the application of small molecule gases in the disease treatment. Increasing evidence has shown that hydrogen sulfide (H2S) has anti-inflammatory and anti-oxidative effects, and can regulate gastric mucosal blood flow in the gastric mucosa. After gastric mucosa damage, the level of H2S in the stomach decreases. Administration of H2S can protect and repair the damaged gastric mucosa. Therefore, H2S is a new target for the repair and treatment of gastric mucosa damage. In this review, we introduce the roles of H2S in the treatment of gastric mucosa damage and provide the potential strategies for further clinical treatment.

Keywords: hydrogen sulfide; gastric mucosa; experimental study; anti-oxidation; anti-inflammation; gastric mucosal blood flow; protective effects; nitric oxide; carbon monoxide


How to cite this article:
Shen F, Zhao CS, Shen MF, Wang Z, Chen G. The role of hydrogen sulfide in gastric mucosal damage. Med Gas Res 2019;9:88-92

How to cite this URL:
Shen F, Zhao CS, Shen MF, Wang Z, Chen G. The role of hydrogen sulfide in gastric mucosal damage. Med Gas Res [serial online] 2019 [cited 2019 Jul 23];9:88-92. Available from: http://www.medgasres.com/text.asp?2019/9/2/88/260650




  Introduction Top


Gastric mucosal diseases, including gastric ulcers, affect 25–30% of the world’s population.[1],[2] An acute gastric mucosa damage is frequently initiated by alcohol consumption, prolonged use of non-steroidal anti-inflammatory drugs (NSAIDs) and stress-induced mucosal damage.[3],[4] Currently, the main clinic treatment for this disease is antisecretory drugs such as histamine type 2 receptor antagonists and irreversible proton pump inhibitors.[5],[6] Although effective, long-term use will bring more serious complications and aggravate the condition.[7] In a large number of previous studies, we have found that certain gaseous media are involved in the occurrence, development, and even treatment of diseases, and small molecule gas has been among the most studied biological mediators Hydrogen sulfide (H2S) is a small gaseous compound, forming the gasotransmitter family with nitric oxide (NO) and carbon monoxide (CO).[8] It influences physiological and pathological processes throughout the body.[9] However, increasing studies have shown that H2S has anti-inflammatory, anti-oxidative, and protective effects in neurological diseases, cardiovascular diseases, hematologic diseases, and urological diseases.[10],[11] The role of H2S in the gastrointestinal system has been lucubrated and received increasing attention. We retrieved studies and clinical trials related to H2S and gastric mucosal damage through literature databases and clinical laboratory platforms, and summarized the influence of H2S in gastric mucosa damage and the potential mechanisms to explore the feasibility of treatment.


  Hydrogen Sulfide Top


H2S was first detected in rat brain in 1989. It is metabolized from cysteine by enzymatic reaction in the presence of cystathionine-γ-lyase (CSE), cystathionine-β-synthetase (CBS) and 3-mercaptopyruvate sulfurtransferase. The distribution of the above enzymes is different in different tissues: CBS is mainly expressed in the nervous system, the cardiovascular system only expresses CSE, and the 3-mercaptopyruvate sulfurtransferase is active in erythrocytes and heart cells. Meanwhile, both CBS and CSE are expressed in digestive system. In some tissues, CSE and CBS are both required for H2S synthesis, whereas in others only one of these enzymes is necessary. H2S also has different expressions at different sites of action. According to reports, the level of H2S does not exceed 160 μM in brain, with serum levels of 30–100 μM.[12] H2S has been recognized as a toxic gas for a long time.[13] Recent studies have found that, similar to certain gases, such as NO, H2S is beneficial at physiological concentrations, but beyond a certain limit, it exhibits its toxicological effects. Because of the highly efficient systems for metabolizing, scavenging and sequestering, the concentration of H2S in plasma seldom exceeded the normal range after administration of H2S donors,[14] which lays the foundation for clinical research.


  Mechanisms of Gastric Mucosa Damage Top


The mechanisms underlying alcohol, NSAIDs and stress induced gastric injuries have not yet been fully elucidated. This pathology is complex and typically caused by an imbalance aggressive and protective factor in the gastric mucosa.[15] In some ways, they are independent of each other and closely related.

Ethanol is one of the aggressive factors that inhibits the proliferation of cells, promotes the infiltration of inflammatory cells,[16] and leads to the necrosis. It can increase the level of oxygen-derived free radicals (reactive oxygen species, ROS) in the stomach tissue and reducing the content of glutathione.[17],[18] While the mechanism of NSAIDs is through the ability to inhibit prostaglandins and cyclooxygenase-1 (an enzyme expressed by gastric epithelial cells), and the synthesis of prostaglandins is inseparable from cyclooxygenase.[19] In the stomach, prostaglandins play a vital protective role, stimulating the secretion of bicarbonate and mucus, maintaining mucosal blood flow, and regulating mucosal cell turnover and repair.[20] So the suppression of prostaglandins synthesis results in increased susceptibility to gastric mucosa damage. NSAIDs also can activate neutrophils to adhere to the vascular endothelium, which could lead to obstruction of capillaries, resulting in a reduction in gastric mucosal blood flow and thereby predisposing the mucosa to injury.[21]

However, whether it is ethanol or NSAIDs, its pathological process is inseparable from oxidative stress response.[18],[22],[23] Oxidative stress is believed to be closely related to the formation of gastric ulcers. A major factor in the development of stress ulcer is splanchnic hypoperfusion, which results from a number of stress-related effects that may include release of proinflammatory cytokines such as tumor necrosis factor-α (TNF-α). Then, overexposure to ROS and TNF-α can trigger caspase-dependent apoptosis, aggravating the damage of the gastric mucosa.[18] Beside the direct deleterious effect, oxidative stress also can induce inflammatory responses via activation of redox sensitive transcription factors such as nuclear factor-κB (NF-κB).[24]


  Experimental Studies of Hydrogen Sulfide in Gastric Mucosa Damage Top


As we all known, we have to test a large number of animal experiments before clinical application. As for animal tests, we have successfully established animal models of gastric mucosa damage. Due to the toxicity and high solubility of H2S, it is uncommon to inhale it directly. So we use other substances to simulate its effect. Sodium hydrosulfide (NaHS) is commonly used in experiments as a source of H2S to study the possible physiologic functions. NaHS immediately dissociates and forms the hydrosulfide anion HS-, which then reacts with H+ to form H2S.[25] Apply it to the model of gastric mucosa damage to explore the potential mechanisms of H2S. By summarizing the experiments, we found that the conclusions between the different experiments are inconsistent. According to some research,[26],[27],[28],[29],[30],[31],[32] NaHS played a protective effect in gastric mucosa damage. NaHS could decrease hemorrhagic damage, edema and epithelial cell loss induced by ethanol.[26] NaHS played a protective role through modulation of adenosine triphosphate-sensitive potassium channel opening and through the NF-κB dependent pathway.[27],[28] It could reduce the serum level of TNF-α and interleukin-1β to abrogate the inflammatory.[29],[30] It significantly decreased ulcer area[31] and increased gastric blood flow at ulcer margin.[30],[32] However, Chavez-Pina et al.[33] reported that H2S had no protective effect on the gastric mucosa, which finding was contrary to the former. This may be due to differences in experimental conditions and methods. We analyze several recent experiments related to this gas for gastric mucosa damage in this paper [Table 1], and summarize the outcomes and mechanisms.
Table 1: The effects of H2S in gastric mucosa damage

Click here to view



  Mechanisms of Hydrogen Sulfide in Gastric Mucosa Damage Anti-Oxidation Top


As mentioned above, oxidative stress is an important cause of gastric mucosa damage. ROS is the harmful specie known to cause the gastric ulcer development. ROS is indicated as an important cause of lipid oxidation, which leads to changes in membrane fluidity and permeability.[35],[36] Cells have different systems to remove ROS, and glutathione is one of the important substances.[37] Many studies have found that H2S can increase the level of glutathione and reduce the content of ROS in the gastric tissue.[38] As a result, H2S may play an anti-oxidation role in the digestive system.

Anti-inflammation

A large number of ROS produced by oxidative stress can activate the NF-κB signaling pathway within the cell, where NF-κB production results in increased levels of cytokines such as interleukin-6 and interleukin-1β.[36] Studies have confirmed that H2S is able to reduce inflammation by suppressing the NF-κB signaling pathway.[28],[39] It is reported that TNF-α was the major proinflammatory cytokine secreted by macrophages during gastric ulcer, which induces injury in a variety of tissues including the gastric mucosa by stimulating neutrophil infiltration into gastric mucosa.[40] H2S also exerts its anti-inflammatory action by inhibiting the level of TNF-α in the stomach.[41],[42] And in the present study, we find that H2S can reduce edema formation,[43] and the action appears to be mediated via adenosine triphosphate-sensitive potassium channels. These findings offer evidences for the powerful anti-inflammation role of H2S.

Regulate gastric mucosal blood flow

According to previous studies, a great deal of evidences described that H2S may regulate gastric microcirculation. H2S induced vasorelaxation in peripheral vessels may be mediated by various mechanisms, including opening of potassium channels,[27] blockade of voltage-gated Ca2+ channels, enhanced production or activity endothelial derived factors. It also can inhibit the expression of leukocyte adhesion molecules and adhesion of leukocytes to the vascular endothelium to increase the blood flow of the gastric mucosa.[44] H2S also activated the transient receptor potential ankyrin 1 receptor, releasing the vasoactive sensory neuropeptides calcitonin gene related peptide and substance P to regulate vasodilation.[45] The endogenous prostaglandin is also a major mediator of H2S-mediated increase in gastric microcirculation.[34]

Additional mechanisms

H2S also can reduce the gastric acid secretion along with pepsin activity and gastric mucosal carbonyl content level with concomitant increase in the gastric juice pH and mucin concentration.[27],[29],[46]

Interaction with carbon monoxide and nitric oxide

In addition to H2S, CO and NO are confirmed to play an important role in the mechanism of mucosal defense and gastroprotection. NO, created from L-arginine and oxygen by NO synthases, is also a pleiotropic neurotransmitter within both the central and peripheral nervous system.[47] Within the stomach, the NO can strengthen the defense function, help maintain the normal physiological state and integrity of the stomach. It can affect the secretion of mucus, increase the blood flow of the gastric mucosa.[48],[49] Like H2S, NO can also play a protective role by reducing oxidative stress. Unlike H2S and NO, CO is more stable. Most biologically relevant CO is produced by the action of heme oxygenase (HMOX). HMOX has been identified with three different phenotypes, of which HMOX-1 is usually expressed in the luminal gastrointestinal tract at a relatively low level.[25] HMOX-1 induction is usually associated with a protective response. New evidence suggests that HMOX-1 is not directly involved in anti-oxidative stress and other reactions, but by up-regulating CO to protect.[50] In terms of its role in gastric mucosa, CO exhibits its anti-inflammatory, anti-apoptotic and anti-oxidant responses in many ways.[51] A large number of studies have found that the three of them interact with each other.[52],[53] For example, H2Sn, generated by the rapid reaction of H2S and NO, could activate transient receptor potential ankyrin 1 channels to modify synaptic activity and cyclic guanosine monophosphate-dependent protein kinase-1α to induce vascular relaxation.[54] However, the way in which the three have previously interacted with each other has not been fully explained. Their protection of the stomach is interrelated and independent. At present, many studies have applied two or three of these gases to a model of gastric mucosal injury to explore whether their mutual effects can also protect the gastric mucosa and its mechanism.[30],[34],[48] We hope that there will be more and more discoveries about them in the future.


  Clinical Applications Top


Current research on H2S is still at the experimental stage and has not yet been applied to the clinic. The potential value for the clinical application of H2S needs to be further explored through translational research and clinical trials.


  Conclusion Top


Through the above introduction, it is believed that H2S may play a potential role in the physiology of the gastrointestinal tract including the gastroprotection of gastric mucosa and possibly exerts a protective effect in other parts of the digestive system. Although some studies have found that the role of H2S is somewhat inconsistent with those mentioned above, which may be caused by differences in dose, mode of action, and type of disease. After acting on the body, H2S does not simply cause the above mechanism. A larger regulatory network will be discovered and explored. Although we have not fully understood its mechanism, we will continue to do a lot of research in the future. H2S is expected to be used to the clinic, providing a more convenient and less side-effect treatment for gastric lesions.

Author contributions

Manuscript writing: FS; manuscript revision: CSZ; manuscript drafting and revision: MFS, ZW, GC. All the authors read and approved the final version of the manuscript for publication..

Conflicts of interest

The authors have no conflicts of interests to declare.

Financial support

None.

Copyright license agreement

The Copyright License Agreement has been signed by all authors before publication.

Plagiarism check

Checked twice by iThenticate.

Peer review

Externally peer reviewed.

Open access statement

This is an open access journal, and articles are distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as appropriate credit is given and the new creations are licensed under the identical terms.



 
  References Top

1.
Carneiro JG, Holanda TBL, Quindere ALG, et al. Gastroprotective effects of sulphated polysaccharides from the alga caulerpa mexicana reducing ethanol-induced gastric damage. Pharmaceuticals (Basel). 2018;11:E6.  Back to cited text no. 1
    
2.
Zhang Z, Zou YY, Li FJ, Hu CP. Asymmetric dimethylarginine: a novel biomarker of gastric mucosal injury? World J Gastroenterol. 2011;17:2178-2180.  Back to cited text no. 2
    
3.
Paulrayer A, Adithan A, Lee JH, et al. Aronia melanocarpa (Black Chokeberry) reduces ethanol-induced gastric damage via regulation of HSP-70, NF-κB, and MCP-1 signaling. Int J Mol Sci. 2017;18:E1195.  Back to cited text no. 3
    
4.
Zheng SQ, Hong XD, Chen TS, Luo PF, Xiao SC. Effects of caspase-1 inhibitor VX765 on cold-restraint stress-induced acute gastric ulcer in mice. Zhonghua Shao Shang Za Zhi. 2017;33:688-693.  Back to cited text no. 4
    
5.
Bi W, Hu L, Man MQ. Anti-ulcerogenic efficacy and mechanisms of edible and natural ingredients in nsaid-induced animal models. Afr J Tradit Complement Altern Med. 2017;14:221-238.  Back to cited text no. 5
    
6.
Goldstein JL, Cryer B. Gastrointestinal injury associated with NSAID use: a case study and review of risk factors and preventative strategies. Drug Healthc Patient Saf. 2015;7:31-41.  Back to cited text no. 6
    
7.
Kangwan N, Park JM, Hahm KB. Development of GI-safe NSAID; progression from the bark of willow tree to modern pharmacology. Curr Opin Pharmacol. 2014;19:17-23.  Back to cited text no. 7
    
8.
Bucci M, Papapetropoulos A, Vellecco V, et al. cGMP-dependent protein kinase contributes to hydrogen sulfide-stimulated vasorelaxation. PLoS One. 2012;7:e53319.  Back to cited text no. 8
    
9.
Wallace JL, Wang R. Hydrogen sulfide-based therapeutics: exploiting a unique but ubiquitous gasotransmitter. Nat Rev Drug Discov. 2015;14:329-345.  Back to cited text no. 9
    
10.
Citi V, Piragine E, Testai L, Breschi MC, Calderone V, Martelli A. The role of hydrogen sulfide and H2S-donors in myocardial protection against ischemia/reperfusion injury. Curr Med Chem. 2018;25:4380-4401.  Back to cited text no. 10
    
11.
Zheng J, Zhao T, Yuan Y, Hu N, Tang X. Hydrogen sulfide (H2S) attenuates uranium-induced acute nephrotoxicity through oxidative stress and inflammatory response via Nrf2-NF-κB pathways. Chem Biol Interact. 2015;242:353-362.  Back to cited text no. 11
    
12.
Fiorucci S, Distrutti E, Cirino G, Wallace JL. The emerging roles of hydrogen sulfide in the gastrointestinal tract and liver. Gastroenterology. 2006;131:259-271.  Back to cited text no. 12
    
13.
Warenycia MW, Goodwin LR, Benishin CG, et al. Acute hydrogen sulfide poisoning. Demonstration of selective uptake of sulfide by the brainstem by measurement of brain sulfide levels. Biochem Pharmacol. 1989;38:973-981.  Back to cited text no. 13
    
14.
Li L, Rossoni G, Sparatore A, Lee LC, Del Soldato P, Moore PK. Anti-inflammatory and gastrointestinal effects of a novel diclofenac derivative. Free Radic Biol Med. 2007;42:706-719.  Back to cited text no. 14
    
15.
Selmi S, Rtibi K, Grami D, Sebai H, Marzouki L. Protective effects of orange (Citrus sinensis L.) peel aqueous extract and hesperidin on oxidative stress and peptic ulcer induced by alcohol in rat. Lipids Health Dis. 2017;16:152.  Back to cited text no. 15
    
16.
Zhang Y, Wang H, Mei N, et al. Protective effects of polysaccharide from Dendrobium nobile against ethanol-induced gastric damage in rats. Int J Biol Macromol. 2018;107:230-235.  Back to cited text no. 16
    
17.
Silva RO, dos Santos GM, Nicolau LA, et al. Sulfated-polysaccharide fraction from red algae Gracilaria caudata protects mice gut against ethanol-induced damage. Mar Drugs. 2011;9:2188-2200.  Back to cited text no. 17
    
18.
Liang J, Dou Y, Wu X, et al. Prophylactic efficacy of patchoulene epoxide against ethanol-induced gastric ulcer in rats: Influence on oxidative stress, inflammation and apoptosis. Chem Biol Interact. 2018;283:30-37.  Back to cited text no. 18
    
19.
Fan DD, Lin S, Song YP, et al. Astragaloside IV protects rat gastric mucosa against aspirin-induced damage. Int Immunopharmacol. 2016;41:47-55.  Back to cited text no. 19
    
20.
Hu Z, Chang X, Pan Q, Gu K, Okechukwu PN. Gastroprotective and ulcer healing effects of camel milk and urine in HCl/EtOH, non-steroidal anti-inflammatory drugs (indomethacin), and water-restraint stress-induced ulcer in rats. Pharmacogn Mag. 2017;13:559-565.  Back to cited text no. 20
    
21.
Kim HK, Kim JI, Kim JK, et al. Preventive effects of rebamipide on NSAID-induced gastric mucosal injury and reduction of gastric mucosal blood flow in healthy volunteers. Dig Dis Sci. 2007;52:1776-1782.  Back to cited text no. 21
    
22.
Nagappan A, Jung DY, Kim JH, Lee H, Jung MH. Gomisin N alleviates ethanol-induced liver injury through ameliorating lipid metabolism and oxidative stress. Int J Mol Sci. 2018;19:E2601.  Back to cited text no. 22
    
23.
Alsarra IA, Ahmed MO, Alanazi FK, Eltahir KE, Alsheikh AM, Neau SH. Influence of cyclodextrin complexation with NSAIDs on NSAID/cold stress-induced gastric ulceration in rats. Int J Med Sci. 2010;7:232-239.  Back to cited text no. 23
    
24.
George MY, Esmat A, Tadros MG, El-Demerdash E. In vivo cellular and molecular gastroprotective mechanisms of chrysin; Emphasis on oxidative stress, inflammation and angiogenesis. Eur J Pharmacol. 2018;818:486-498.  Back to cited text no. 24
    
25.
Farrugia G, Szurszewski JH. Carbon monoxide, hydrogen sulfide, and nitric oxide as signaling molecules in the gastrointestinal tract. Gastroenterology. 2014;147:303-313.  Back to cited text no. 25
    
26.
Medeiros JV, Bezerra VH, Gomes AS, et al. Hydrogen sulfide prevents ethanol-induced gastric damage in mice: role of ATP-sensitive potassium channels and capsaicin-sensitive primary afferent neurons. J Pharmacol Exp Ther. 2009;330:764-770.  Back to cited text no. 26
    
27.
Sun HZ, Zheng S, Lu K, et al. Hydrogen sulfide attenuates gastric mucosal injury induced by restraint water-immersion stress via activation of KATP channel and NF-κB dependent pathway. World J Gastroenterol. 2017;23:87-92.  Back to cited text no. 27
    
28.
Guo C, Liang F, Shah Masood W, Yan X. Hydrogen sulfide protected gastric epithelial cell from ischemia/reperfusion injury by Keap1 s-sulfhydration, MAPK dependent anti-apoptosis and NF-κB dependent anti-inflammation pathway. Eur J Pharmacol. 2014;725:70-78.  Back to cited text no. 28
    
29.
Aboubakr EM, Taye A, El-Moselhy MA, Hassan MK. Protective effect of hydrogen sulfide against cold restraint stress-induced gastric mucosal injury in rats. Arch Pharm Res. 2013;36:1507-1515.  Back to cited text no. 29
    
30.
Magierowski M, Magierowska K, Hubalewska-Mazgaj M, et al. Interaction between endogenous carbon monoxide and hydrogen sulfide in the mechanism of gastroprotection against acute aspirin-induced gastric damage. Pharmacol Res. 2016;114:235-250.  Back to cited text no. 30
    
31.
Magierowski M, Magierowska K, Hubalewska-Mazgaj M, et al. Cross-talk between hydrogen sulfide and carbon monoxide in the mechanism of experimental gastric ulcers healing, regulation of gastric blood flow and accompanying inflammation. Biochem Pharmacol. 2018;149:131-142.  Back to cited text no. 31
    
32.
Magierowski M, Jasnos K, Kwiecien S, Brzozowski T. Role of hydrogen sulfide in the physiology of gastrointestinal tract and in the mechanism of gastroprotection. Postepy Hig Med Dosw (Online). 2013;67:150-156.  Back to cited text no. 32
    
33.
Chavez-Pina AE, Tapia-Alvarez GR, Navarrete A. Inhibition of endogenous hydrogen sulfide synthesis by PAG protects against ethanol-induced gastric damage in the rat. Eur J Pharmacol. 2010;630:131-136.  Back to cited text no. 33
    
34.
Magierowski M, Jasnos K, Kwiecien S, et al. Endogenous prostaglandins and afferent sensory nerves in gastroprotective effect of hydrogen sulfide against stress-induced gastric lesions. PLoS One. 2015;10:e0118972.  Back to cited text no. 34
    
35.
Liu J, Sun D, He J, et al. Gastroprotective effects of several H2RAs on ibuprofen-induced gastric ulcer in rats. Life Sci. 2016;149:65-71.  Back to cited text no. 35
    
36.
Yeo D, Hwang SJ, Kim WJ, Youn HJ, Lee HJ. The aqueous extract from Artemisia capillaris inhibits acute gastric mucosal injury by inhibition of ROS and NF-kB. Biomed Pharmacother. 2018;99:681-687.  Back to cited text no. 36
    
37.
Adefisayo MA, Akomolafe RO, Akinsomisoye OS, Alabi QK. Protective effects of methanol extract of Vernonia amygdalina (del.) leaf on aspirin-induced gastric ulceration and oxidative mucosal damage in a rat model of gastric injury. Dose Response. 2018;16:1559325818785087.  Back to cited text no. 37
    
38.
Nicolau LA, Silva RO, Damasceno SR, et al. The hydrogen sulfide donor, Lawesson’s reagent, prevents alendronate-induced gastric damage in rats. Braz J Med Biol Res. 2013;46:708-714.  Back to cited text no. 38
    
39.
Zhang GY, Lu D, Duan SF, et al. Hydrogen sulfide alleviates lipopolysaccharide-induced diaphragm dysfunction in rats by reducing apoptosis and inflammation through ROS/MAPK and TLR4/NF-κB signaling pathways. Oxid Med Cell Longev. 2018;2018:9647809.  Back to cited text no. 39
    
40.
Boutemine IM, Amri M, Amir ZC, et al. Gastro-protective, therapeutic and anti-inflammatory activities of Pistacia lentiscus L. fatty oil against ethanol-induced gastric ulcers in rats. J Ethnopharmacol. 2018;224:273-282.  Back to cited text no. 40
    
41.
Magierowski M, Magierowska K, Surmiak M, et al. The effect of hydrogen sulfide-releasing naproxen (ATB-346) versus naproxen on formation of stress-induced gastric lesions, the regulation of systemic inflammation, hypoxia and alterations in gastric microcirculation. J Physiol Pharmacol. 2017;68:749-756.  Back to cited text no. 41
    
42.
Yang CT, Lai ZZ, Zheng ZH, et al. A novel pH-controlled hydrogen sulfide donor protects gastric mucosa from aspirin-induced injury. J Cell Mol Med. 2017;21:2441-2451.  Back to cited text no. 42
    
43.
Zanardo RC, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, Wallace JL. Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J. 2006;20:2118-2120.  Back to cited text no. 43
    
44.
Fiorucci S, Antonelli E, Distrutti E, et al. Inhibition of hydrogen sulfide generation contributes to gastric injury caused by anti-inflammatory nonsteroidal drugs. Gastroenterology. 2005;129:1210-1224.  Back to cited text no. 44
    
45.
Hajna Z, Sághy É, Payrits M, et al. Capsaicin-sensitive sensory nerves mediate the cellular and microvascular effects of H2S via TRPA1 receptor activation and neuropeptide release. J Mol Neurosci. 2016;60:157-170.  Back to cited text no. 45
    
46.
Souza LK, Araujo TS, Sousa NA, et al. Evidence that d-cysteine protects mice from gastric damage via hydrogen sulfide produced by D-amino acid oxidase. Nitric Oxide. 2017;64:1-6.  Back to cited text no. 46
    
47.
Han T, Tang Y, Li J, et al. Nitric oxide donor protects against acetic acid-induced gastric ulcer in rats via S-nitrosylation of TRPV1 on vagus nerve. Sci Rep. 2017;7:2063.  Back to cited text no. 47
    
48.
Lucetti LT, Silva RO, Santana AP, et al. Nitric oxide and hydrogen sulfide interact when modulating gastric physiological functions in rodents. Dig Dis Sci. 2017;62:93-104.  Back to cited text no. 48
    
49.
Magierowski M, Magierowska K, Kwiecien S, Brzozowski T. Gaseous mediators nitric oxide and hydrogen sulfide in the mechanism of gastrointestinal integrity, protection and ulcer healing. Molecules. 2015;20:9099-9123.  Back to cited text no. 49
    
50.
Chang M, Xue J, Sharma V, Habtezion A. Protective role of hemeoxygenase-1 in gastrointestinal diseases. Cell Mol Life Sci. 2015;72:1161-1173.  Back to cited text no. 50
    
51.
Takagi T, Naito Y, Uchiyama K, et al. Carbon monoxide promotes gastric wound healing in mice via the protein kinase C pathway. Free Radic Res 2016;50:1098-1105.  Back to cited text no. 51
    
52.
de Araujo S, Oliveira AP, Sousa FBM, et al. AMPK activation promotes gastroprotection through mutual interaction with the gaseous mediators H2S, NO, and CO. Nitric Oxide. 2018;78:60-71.  Back to cited text no. 52
    
53.
Velazquez-Moyado JA, Navarrete A. The detection and quantification, in vivo and in real time, of hydrogen sulfide in ethanol-induced lesions in rat stomachs using an ion sensitive electrode. J Pharmacol Toxicol Methods. 2018;89:54-58.  Back to cited text no. 53
    
54.
Miyamoto R, Koike S, Takano Y, et al. Polysulfides (H2Sn) produced from the interaction of hydrogen sulfide (H2S) and nitric oxide (NO) activate TRPA1 channels. Sci Rep. 2017;7:45995.  Back to cited text no. 54
    



 
 
    Tables

  [Table 1]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

  Mechanisms of Ga...Experimental Stu...Mechanisms of Hy...Clinical Applica...
  In this article
Abstract
Introduction
Hydrogen Sulfide
Conclusion
References
Article Tables

 Article Access Statistics
    Viewed76    
    Printed6    
    Emailed0    
    PDF Downloaded24    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]