Inflammation, oxidative stress, DNA damage response and epigenetic modifications interact behind the beneficial actions of melatonin on H. pylori-mediated gastric disorders
Melatonin in H. pylori-related gastric disorders
Keywords:
H. pylori, gastric mucosa, gastrointestinal disorder, gastric cancer, inflammation, reactive oxygen and nitrogen species (ROS/RNS), DNA damage response, epigenetic regulation, melatonin
Abstract
Helicobacter pylori (H. pylori) infection is associated with several disorders of the gastrointestinal tract, including gastric cancer. Studies of ours and others suggest that H. pylori infection may affect melatonin synthesis in the gastric epithelial cells. On the other hand, melatonin ameliorates gastric disorders as shown in clinical trials and experimental studies. Moreover, melatonin not only suppresses the DNA-damaging reaction of diet-related mutagens that can initiate carcinogenesis in gastric mucosa, but also the oxidative DNA damage evoked by reactive oxygen and nitrogen species produced during H. pylori-related gastric inflammation. H. pylori infection is associated with several functional and organic gastric disorders, including gastritis, peptic ulcer disease and gastric cancer, but the precise mechanism behind this association is not known and many pathways can be involved. Some of beneficial effects of melatonin in the gastrointestinal tract are underlined by mechanisms that likely play a role in detrimental effects of H. pylori in the stomach. Therefore, melatonin may modulate these mechanisms resulting in ameliorating H. pylori-related symptoms. In this narrative review the role of inflammation, oxidative stress, DNA damage response and epigenetic modifications in H. pylori-associated gastric disorders will be discussed with an emphasis on gastric cancer. We also suggest that melatonin may have potential to inhibit H. pylori-mediated pathologies through its interaction with essential pathways as described herein. Overlapping mechanisms of H. pylori-associated pathogenesis and beneficial effects of melatonin justify further studies on the action of melatonin on gastric disorders associated with H. pylori infection, including clinical trials.
References
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2. Brown LM (2000) Helicobacter pylori: epidemiology and routes of transmission. Epidemiol. Rev. 22: 283-297.
3. Hooi JKY et al. (2017) Global Prevalence of Helicobacter pylori Infection: systematic review and meta-analysis. Gastroenterology 153: 420-429.
4. Wroblewski L E, Peek R M, Jr., Wilson K T (2010) Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin. Microbiol. Rev. 23: 713-739.
5. Eusebi L H, Telese A, Marasco G, Bazzoli F, Zagari R M (2020) Gastric cancer prevention strategies: A global perspective. J. Gastroenterol. Hepatol. 35: 1495-1502.
6. Mehrzadi S, Pourhanifeh M H, Mirzaei A, Moradian F, Hosseinzadeh A (2021) An updated review of mechanistic potentials of melatonin against cancer: pivotal roles in angiogenesis, apoptosis, autophagy, endoplasmic reticulum stress and oxidative stress. Cancer Cell Int. 21: 188.
7. Targhazeh N et al. (2022) Oncostatic activities of melatonin: Roles in cell cycle, apoptosis, and autophagy. Biochimie 202: 34-48.
8. Chojnacki C, Mędrek-Socha M, Konrad P, Chojnacki J, Błońska A (2020) The value of melatonin supplementation in postmenopausal women with Helicobacter pylori-associated dyspepsia. BMC Womens Health 20: 262.
9. Chojnacki C, Poplawski T, Blasiak J, Chojnacki J, Klupinska G, (2013) Does melatonin homeostasis play a role in continuous epigastric pain syndrome? Int. J. Mol. Sci. 14: 12550-12562.
10. Chojnacki C et al. (2013) Expression of melatonin synthesizing enzymes in Helicobacter pylori infected gastric mucosa. Biomed. Res. Int. 2013: 845032.
11. Chojnacki C et al., (2019) Expression of tryptophan hydroxylase in gastric mucosa in symptomatic and asymptomatic Helicobacter pylori infection. Arch. Med. Sci. 15: 416-423.
12. Bouvard V et al. (2009) A review of human carcinogens--Part B: biological agents. Lancet Oncol. 10: 321-322.
13. Chiba T, Marusawa H, Seno H, Watanabe N (2008) Mechanism for gastric cancer development by Helicobacter pylori infection. J. Gastroenterol. Hepatol. 23: 1175-1181.
14. Yamaoka Y (2010) Mechanisms of disease: Helicobacter pylori virulence factors. Nat. Rev. Gastroenterol. Hepatol. 7: 629-641.
15. Hatakeyama M (2006) Helicobacter pylori CagA—a bacterial intruder conspiring gastric carcinogenesis. Int. J. Cancer 119: 1217-1223.
16. Ekström AM, Held M, Hansson LE, Engstrand L, Nyrén O (2001) Helicobacter pylori in gastric cancer established by CagA immunoblot as a marker of past infection. Gastroenterology 121: 784-791.
17. Kitajima Y et al. (2008) Helicobacter pylori infection is an independent risk factor for Runx3 methylation in gastric cancer. Oncol. Rep. 19: 197-202.
18. Tsang YH, Lamb A, Chen LF, (2011) New insights into the inactivation of gastric tumor suppressor RUNX3: the role of H. pylori infection. J. Cell. Biochem. 112: 381-386.
19. Buti L et al. (2011) Helicobacter pylori cytotoxin-associated gene A (CagA) subverts the apoptosis-stimulating protein of p53 (ASPP2) tumor suppressor pathway of the host. Proc. Nat. Acad. Sci. USA 108: 9238-9243.
20. Blaser M J et al. (1995) Infection with Helicobacter pylori strains possessing caga is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res. 55: 2111-2115.
21. Abdullah M et al. (2019) VacA promotes CagA accumulation in gastric epithelial cells during Helicobacter pylori infection. Sci. Rep. 9: 38.
22. Lamb A, Chen LF (2013) Role of the Helicobacter pylori-induced inflammatory response in the development of gastric cancer. J. Cell. Biochem. 114: 491-497.
23. Correa P (1988) A human model of gastric carcinogenesis. Cancer Res. 48: 3554-3560.
24. Raza Y et al. (2020) Helicobacter pylori severely reduces expression of DNA repair proteins PMS2 and ERCC1 in gastritis and gastric cancer. DNA Repair 89: 102836.
25. Yin H, Chu A, Liu S, Yuan Y, Gong Y (2020) Identification of DEGs and transcription factors involved in H. pylori-associated inflammation and their relevance with gastric cancer. PeerJ 8: e9223.
26. Butcher LD, den Hartog G, Ernst PB, Crowe SE (2017) oxidative stress resulting from Helicobacter pylori infection contributes to gastric carcinogenesis. Cell. Mol. Gastroenterol. Hepatol. 3: 316-322.
27. Chang T et al. (2020) Melatonin exerts immunoregulatory effects by balancing peripheral effector and regulatory T helper cells in myasthenia gravis. Aging 12: 21147-21160.
28. Jianhua L et al. (2018) Immunoregulatory role of melatonin in Helicobacter pylori-induced gastric diseases. FASEB J. 32: 805.803-805.803.
29. Bagheri N et al. (2015) Mucosal interleukin-21 mRNA expression level is high in patients with Helicobacter pylori and is associated with the severity of gastritis. Cent. Eur. J. Immunol. 40: 61-67.
30. McGee DJ, Mobley HL (2000) Pathogenesis of Helicobacter pylori infection. Curr. Opin. Gastroenterol. 16: 24-31.
31. Navaglia F et al. (2005) Interleukin 12 gene polymorphisms enhance gastric cancer risk in H pylori infected individuals. J. Med. Genet. 42: 503-510.
32. Sakitani K et al. (2012) Role of interleukin-32 in Helicobacter pylori-induced gastric inflammation. Infect. Immun. 80: 3795-3803.
33. Lee M H et al. (2019) Inhibitory Effects of Menadione on Helicobacter pylori Growth and Helicobacter pylori-Induced Inflammation via NF-κB Inhibition. Int. J. Mol. Sci. 20.
34. Liu T, Zhang L, Joo D, Sun SC (2017) NF-κB signaling in inflammation. Signal Transduct. Target. Ther. 2: 17023-.
35. Eaton K A, Mefford M, Thevenot T (2001) The role of T cell subsets and cytokines in the pathogenesis of Helicobacter pylori gastritis in mice. J. Immunol. 166: 7456-7461.
36. Chakraborty C, Sharma AR, Sharma G, Lee SS (2020) The interplay among mirnas, major cytokines, and cancer-related inflammation. Mol. Ther. 20: 606-620.
37. Kalisperati P et al. (2017) Inflammation, DNA damage, helicobacter pylori and gastric tumorigenesis. Front. Genet. 8: 20.
38. Favero G, Franceschetti L, Bonomini F, Rodella L F, Rezzani R (2017) Melatonin as an anti-inflammatory agent modulating inflammasome activation. Int. J. Endocrinol. 2017: 1835195.
39. Celinski K et al. (2011) Effects of melatonin and tryptophan on healing of gastric and duodenal ulcers with Helicobacter pylori infection in humans. J. Physiol. Pharmacol. 62: 521-526.
40. Li J H et al. (2005) Melatonin reduces inflammatory injury through inhibiting NF-kappaB activation in rats with colitis. Mediators Inflamm. 2005: 185-193.
41. Tamura EK, Fernandes PA, Marçola M, da Silveira Cruz-Machado S, Markus RP (2010) Long-lasting priming of endothelial cells by plasma melatonin levels. PloS One 5: e13958.
42. Tarakcioglu E, Tastan B, Arioz BI, Tufekci KU, Genc S (2022) Melatonin alters the mirna transcriptome of inflammasome activation in murine microglial cells. Neurochem. Res. 47: 3202-3211.
43. Yu GM, Kubota H, Okita M, Maeda T (2017) The anti-inflammatory and antioxidant effects of melatonin on LPS-stimulated bovine mammary epithelial cells. PloS One 12: e0178525.
44. Pachathundikandi SK, Backert S (2018) Helicobacter pylori controls NLRP3 expression by regulating hsa-miR-223-3p and IL-10 in cultured and primary human immune cells. Innate Immun. 24: 11-23.
45. Naito Y, Yoshikawa T (2002) Molecular and cellular mechanisms involved in Helicobacter pylori-induced inflammation and oxidative stress. Free Radical Biol. Med. 33: 323-336.
46. Lambeth JD, (2004) NOX enzymes and the biology of reactive oxygen. Nature Rev Immun. 4: 181-189.
47. Fu S et al. (1999) Increased expression and cellular localization of inducible nitric oxide synthase and cyclooxygenase 2 in Helicobacter pylori gastritis. Gastroenterology 116: 1319-1329.
48. Reiter RJ et al. (2016) Melatonin as an antioxidant: under promises but over delivers. J. Pineal Res. 61: 253-278.
49. Majidinia M et al. (2017) Melatonin: A pleiotropic molecule that modulates DNA damage response and repair pathways. J. Pineal Res. 63: e12416.
50. Jackson SP, Bartek J (2009) The DNA-damage response in human biology and disease. Nature 461: 1071-1078.
51. Machado AMD et al. (2009) Helicobacter pylori infection induces genetic instability of nuclear and mitochondrial DNA in gastric cells. Clin. Cancer Res. 15: 2995-3002.
52. Chaturvedi R et al.,(2011) Spermine oxidase mediates the gastric cancer risk associated with Helicobacter pylori CagA. Gastroenterology 141: 1696-1708.e1692.
53. Arabski M et al. (2005) DNA damage and repair in Helicobacter pylori-infected gastric mucosa cells. Mutat. Res. 570: 129-135.
54. Poplawski T et al. (2013) Helicobacter pylori infection and antioxidants can modulate the genotoxic effects of heterocyclic amines in gastric mucosa cells. Mol. Biol. Rep. 40: 5205-5212.
55. Bulanda S, Janoszka B (2022) Consumption of thermally processed meat containing carcinogenic compounds (polycyclic aromatic hydrocarbons and heterocyclic aromatic amines) versus a risk of some cancers in humans and the possibility of reducing their formation by natural food additives-a literature review. Int. J. Env. Res. Publ. Health 19.
56. Arabski M et al. (2006) Helicobacter pylori infection can modulate the susceptibility of gastric mucosa cells to MNNG. Cell. Mol. Biol. Lett. 11: 570-578.
57. Kidane D, Murphy DL, Sweasy JB (2014) Accumulation of abasic sites induces genomic instability in normal human gastric epithelial cells during Helicobacter pylori infection. Oncogenesis 3: e128-e128.
58. Liu H et al. (2022) The effect and mechanisms of melatonin on the proliferation and apoptosis of lung cancer cells. Bioengineered 13: 3462-3469.
59. Sánchez-Hidalgo M, Guerrero J M, Villegas I, Packham G, de la Lastra CA (2012) Melatonin, a natural programmed cell death inducer in cancer. Curr. Med. Chem. 19: 3805-3821.
60. Xie Y et al. (2022) Melatonin enhances osteoblastogenesis of senescent bone marrow stromal cells through NSD2-mediated chromatin remodelling. Clin. Transl. Med. 12: e746.
61. Mir S M et al. (2022) Melatonin: A smart molecule in the DNA repair system. Cell. Biochem. Funct. 40: 4-16.
62. Galano A, Reiter R J (2018) Melatonin and its metabolites vs oxidative stress: From individual actions to collective protection. J. Pineal Res. 65: e12514.
63. Pérez-González A, Castañeda-Arriaga R, Álvarez-Idaboy JR, Reiter R J, Galano A (2019) Melatonin and its metabolites as chemical agents capable of directly repairing oxidized DNA. J. Pineal Res. 66: e12539.
64. Cheung HH, Lee TL, Rennert OM, Chan WY (2009) DNA methylation of cancer genome. Birth Defects Res. C Embryo Today 87: 335-350.
65. Maekita T et al. (2006) High levels of aberrant DNA methylation in Helicobacter pylori-infected gastric mucosae and its possible association with gastric cancer risk. Clin. Cancer Res. 12: 989-995.
66. Nakajima T et al. (2009) The presence of a methylation fingerprint of Helicobacter pylori infection in human gastric mucosae. Int. J. Cancer 124: 905-910.
67. Ushijima T, Nakajima T, Maekita T (2006) DNA methylation as a marker for the past and future. J. Gastroenterol. 41: 401-407.
68. O'Brien J, Hayder H, Zayed Y, Peng C (2018) Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front. Endocrinol. 9: 402.
69. Shao T, Pan Y H, Xiong XD (2021) Circular RNA: an important player with multiple facets to regulate its parental gene expression. Mol. Ther. 23: 369-376.
70. Statello L, Guo C J, Chen L L, Huarte M (2021) Gene regulation by long non-coding RNAs and its biological functions. Nature Rev. 22: 96-118.
71. Santos JC, Ribeiro ML (2015) Epigenetic regulation of DNA repair machinery in Helicobacter pylori-induced gastric carcinogenesis. World J. Gastroenterol. 21: 9021-9037.
72. Ding SZ et al. (2010) Helicobacter pylori-induced histone modification, associated gene expression in gastric epithelial cells, and its implication in pathogenesis. PloS One 5: e9875.
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Published
2023-06-30
How to Cite
[1]
Blasiak, J., Chojnacki, J. and Chojnacki, C. 2023. Inflammation, oxidative stress, DNA damage response and epigenetic modifications interact behind the beneficial actions of melatonin on H. pylori-mediated gastric disorders. Melatonin Research. 6, 2 (Jun. 2023), 135-147. DOI:https://doi.org/https://doi.org/10.32794/mr112500145.
Section
Reviews
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