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Performance of DNA Methylation on the Molecular Pathogenesis of Helicobacter pylori in Gastric Cancer; targeted therapy approach

  • Vahidi, Sogand (Medical Biology Research Center, Kermanshah University of Medical Sciences) ;
  • Mirzajani, Ebrahim (Department of Biochemistry, School of Medicine, Guilan University of Medical Sciences) ;
  • Norollahi, Seyedeh Elham (Cancer Research Center and Department of Immunology, Semnan University of Medical Sciences) ;
  • Aziminezhad, Mohsen (Non-Communicable Disease Research Center, Neyshabur University of Medical Sciences) ;
  • Samadani, Ali Akbar (Guilan Road Trauma Research Center, Guilan University of Medical Sciences)
  • Received : 2021.07.29
  • Accepted : 2022.04.11
  • Published : 2022.06.30

Abstract

Gastric cancer (GC) is a significant cause of cancer mortality which has led to focused exploration of the pathology of GC. The advent of genome-wide analysis methods has made it possible to uncover genetic and epigenetic fluctuation such as abnormal DNA methylation in gene promoter regions that is expected to play a key role in GC. The study of gastric malignancies requires an etiological perspective, and Helicobacter pylori (H. pylori) was identified to play a role in GC. H. pylori infection causes chronic inflammation of the gastric epithelium causing abnormal polyclonal methylation, which might raise the risk of GC. In the last two decades, various pathogenic factors by which H. pylori infection causes GC have been discovered. Abnormal DNA methylation is triggered in several genes, rendering them inactive. In GC, methylation patterns are linked to certain subtypes including microsatellite instability. Multiple cancer-related processes are more usually changed by abnormal DNA methylation than through mutations, according to current general and combined investigations. Furthermore, the amount of acquired abnormal DNA methylation is heavily linked to the chances of developing GC. Therefore, we investigated abnormal DNA methylation in GC and the link between methylation and H. pylori infection.

Keywords

Acknowledgement

Authors express their appreciation to all people who contributed to this manuscript.

References

  1. Rawla P, Barsouk A. Epidemiology of gastric cancer: global trends, risk factors and prevention. Prz Gastroenterol. 2019;14(1):26-38.
  2. Puculek M, Machlowska J, Wierzbicki R, Baj J, Maciejewski R, Sitarz R. Helicobacter pylori associated factors in the development of gastric cancer with special reference to the early-onset subtype. Oncotarget. 2018;9(57):31146-62. https://doi.org/10.18632/oncotarget.25757
  3. Nicolescu F. Trends in Helicobacter pylori infection. 1st ed. London (United Kingdom): IntechOpen; c2014. Chapter 6, Particulars of the Helicobacter pylori infection in children; p. 177.
  4. Huang Y, Wang QL, Cheng DD, Xu WT, Lu NH. Adhesion and invasion of gastric mucosa epithelial cells by Helicobacter pylori. Front Cell Infect Microbiol. 2016;6:159. https://doi.org/10.3389/fcimb.2016.00159
  5. Tilahun M, Gedefie A, Belayhun C, Sahle Z, Abera A. Helicobacter pylori pathogenicity islands and Giardia lamblia cysteine proteases in role of coinfection and pathogenesis. Infect Drug Resist. 2022;15:21-34. https://doi.org/10.2147/IDR.S346705
  6. Conteduca V, Sansonno D, Lauletta G, Russi S, Ingravallo G, Dammacco F. H. pylori infection and gastric cancer: state of the art (review). Int J Oncol. 2013;42(1):5-18. https://doi.org/10.3892/ijo.2012.1701
  7. Baj J, Forma A, Sitarz M, Portincasa P, Garruti G, Krasowska D, et al. Helicobacter pylori virulence factors-mechanisms of bacterial pathogenicity in the gastric microenvironment. Cells. 2020;10(1):27. https://doi.org/10.3390/cells10010027
  8. Toh JWT, Wilson RB. Pathways of gastric carcinogenesis, Helicobacter pylori virulence and interactions with antioxidant systems, vitamin C and phytochemicals. Int J Mol Sci. 2020;21(17):6451. https://doi.org/10.3390/ijms21176451
  9. White JR, Winter JA, Robinson K. Differential inflammatory response to Helicobacter pylori infection: etiology and clinical outcomes. J Inflamm Res. 2015;8:137-47. https://doi.org/10.2147/JIR.S64888
  10. Zhang Y, Zhang PS, Rong ZY, Huang C. One stomach, two subtypes of carcinoma-the differences between distal and proximal gastric cancer. Gastroenterol Rep (Oxf). 2021;9(6):489-504. https://doi.org/10.1093/gastro/goab050
  11. Pourzardosht N, Hashemi ZS, Mard-Soltani M, Jahangiri A, Rahbar MR, Zakeri A, et al. Liothyronine could block the programmed death-ligand 1 (PDL1) activity: an e-Pharmacophore modeling and virtual screening study. J Recept Signal Transduct Res. 2022;42(1):34-42. https://doi.org/10.1080/10799893.2020.1839765
  12. Graham DY. Helicobacter pylori update: gastric cancer, reliable therapy, and possible benefits. Gastroenterology. 2015;148(4):719-31.e3. https://doi.org/10.1053/j.gastro.2015.01.040
  13. Matsuo Y, Kido Y, Yamaoka Y. Helicobacter pylori outer membrane protein-related pathogenesis. Toxins (Basel). 2017;9(3):101. https://doi.org/10.3390/toxins9030101
  14. Yamaoka Y, Graham DY. Helicobacter pylori virulence and cancer pathogenesis. Future Oncol. 2014;10(8):1487-500. https://doi.org/10.2217/fon.14.29
  15. Tegtmeyer N, Ghete TD, Schmitt V, Remmerbach T, Cortes MCC, Bondoc EM, et al. Type IV secretion of Helicobacter pylori CagA into oral epithelial cells is prevented by the absence of CEACAM receptor expression. Gut Pathog. 2020;12:25. https://doi.org/10.1186/s13099-020-00363-8
  16. Matos JI, de Sousa HA, Marcos-Pinto R, Dinis-Ribeiro M. Helicobacter pylori CagA and VacA genotypes and gastric phenotype: a meta-analysis. Eur J Gastroenterol Hepatol. 2013;25(12):1431-41. https://doi.org/10.1097/MEG.0b013e328364b53e
  17. Amin M, Shayesteh AA, Serajian A. Concurrent detection of cagA, vacA, sodB and hsp60 virulence genes and their relationship with clinical outcomes of disease in Helicobacter pylori isolated strains of southwest of Iran. Iran J Microbiol. 2019;11(3):198-205.
  18. Queiroz DM, Silva CI, Goncalves MH, Braga-Neto MB, Fialho AB, Fialho AM, et al. Higher frequency of cagA EPIYA-C phosphorylation sites in H. pylori strains from first-degree relatives of gastric cancer patients. BMC Gastroenterol. 2012;12(1):107. https://doi.org/10.1186/1471-230X-12-107
  19. Oluwasola A, Otegbayo J, Ola S, Ebili H, Afolabi A, Odaibo G. Correlation of serum anti-Helicobacter pylori immunoglobulin a (IgA) with histological parameters of chronic gastritis in ibadan, Nigeria. Ann Ib Postgrad Med. 2012;10(1):18-24.
  20. Foegeding NJ, Caston RR, McClain MS, Ohi MD, Cover TL. An overview of Helicobacter pylori VacA toxin biology. Toxins (Basel). 2016;8(6):173. https://doi.org/10.3390/toxins8060173
  21. Abbasi O, Mashayekhi F, Mirzajani E, Fakhriyeh Asl S, Mahmoudi T, Saeedi Saedi H. Soluble VEGFR1 concentration in the serum of patients with colorectal cancer. Surg Today. 2015;45(2):215-20. https://doi.org/10.1007/s00595-014-0886-4
  22. Baj J, Korona-Glowniak I, Forma A, Maani A, Sitarz E, Rahnama-Hezavah M, et al. Mechanisms of the epithelial-mesenchymal transition and tumor microenvironment in Helicobacter pylori-induced gastric cancer. Cells. 2020;9(4):1055. https://doi.org/10.3390/cells9041055
  23. Dewayani A, Fauzia KA, Alfaray RI, Waskito LA, Doohan D, Rezkitha YAA, et al. The roles of IL-17, IL-21, and IL-23 in the Helicobacter pylori infection and gastrointestinal inflammation: a review. Toxins (Basel). 2021;13(5):315. https://doi.org/10.3390/toxins13050315
  24. Melit LE, Marginean CO, Marginean CD, Marginean MO. The relationship between toll-like receptors and Helicobacter pylorirelated gastropathies: still a controversial topic. J Immunol Res. 2019;2019:8197048. https://doi.org/10.1155/2019/8197048
  25. Shimomura H, Wanibuchi K, Hosoda K, Amgalanbaatar A, Masui H, Takahashi T, et al. Unique responses of Helicobacter pylori to exogenous hydrophobic compounds. Chem Phys Lipids. 2020;229:104908. https://doi.org/10.1016/j.chemphyslip.2020.104908
  26. Mirzaei R, Sabokroo N, Ahmadyousefi Y, Motamedi H, Karampoor S. Immunometabolism in biofilm infection: lessons from cancer. Mol Med. 2022;28(1):10.
  27. Hernandez-Rubio A, Sanvisens A, Bolao F, Perez-Mana C, Garcia-Marchena N, Fernandez-Prendes C, et al. Association of hyperuricemia and gamma glutamyl transferase as a marker of metabolic risk in alcohol use disorder. Sci Rep. 2020;10(1):20060. https://doi.org/10.1038/s41598-020-77013-1
  28. Vahidi S, Samadani AA. TERRA gene expression in gastric cancer: role of hTERT. J Gastrointest Cancer. 2021;52(2):431-47. https://doi.org/10.1007/s12029-020-00565-y
  29. Vahidi S, Norollahi SE, Agah S, Samadani AA. DNA methylation profiling of hTERT gene alongside with the telomere performance in gastric adenocarcinoma. J Gastrointest Cancer. 2020;51(3):788-99. https://doi.org/10.1007/s12029-020-00427-7
  30. Muhammad JS, Eladl MA, Khoder G. Helicobacter pyloriinduced DNA methylation as an epigenetic modulator of gastric cancer: recent outcomes and future direction. Pathogens. 2019;8(1):23. https://doi.org/10.3390/pathogens8010023
  31. Huang FY, Chan AO, Lo RC, Rashid A, Wong DK, Cho CH, et al. Characterization of interleukin-1β in Helicobacter pyloriinduced gastric inflammation and DNA methylation in interleukin-1 receptor type 1 knockout (IL-1R1(-/-)) mice. Eur J Cancer. 2013;49(12):2760-70. https://doi.org/10.1016/j.ejca.2013.03.031
  32. Na HK, Woo JH. Helicobacter pylori induces hypermethylation of CpG islands through upregulation of DNA methyltransferase: possible involvement of reactive oxygen/nitrogen species. J Cancer Prev. 2014;19(4):259-64. https://doi.org/10.15430/JCP.2014.19.4.259
  33. Polakovicova I, Jerez S, Wichmann IA, Sandoval-Borquez A, Carrasco-Veliz N, Corvalan AH. Role of microRNAs and exosomes in Helicobacter pylori and Epstein-Barr virus associated gastric cancers. Front Microbiol. 2018;9:636. https://doi.org/10.3389/fmicb.2018.00636
  34. Rizzato C, Torres J, Obazee O, Camorlinga-Ponce M, Trujillo E, Stein A, et al. Variations in cag pathogenicity island genes of Helicobacter pylori from Latin American groups may influence neoplastic progression to gastric cancer. Sci Rep. 2020;10(1):6570. https://doi.org/10.1038/s41598-020-63463-0
  35. Hayashi Y, Tsujii M, Wang J, Kondo J, Akasaka T, Jin Y, et al. CagA mediates epigenetic regulation to attenuate let-7 expression in Helicobacter pylori-related carcinogenesis. Gut. 2013;62(11):1536-46. https://doi.org/10.1136/gutjnl-2011-301625
  36. Ricci V. Relationship between VacA toxin and host cell autophagy in Helicobacter pylori infection of the human stomach: a few answers, many questions. Toxins (Basel). 2016;8(7):203. https://doi.org/10.3390/toxins8070203
  37. Norollahi SE, Alipour M, Rashidy-Pour A, Samadani AA, Larijani LV. Regulatory fluctuation of WNT16 gene expression is associated with human gastric adenocarcinoma. J Gastrointest Cancer. 2019;50(1):42-7. https://doi.org/10.1007/s12029-017-0022-y
  38. Whyte JM, Ellis JJ, Brown MA, Kenna TJ. Best practices in DNA methylation: lessons from inflammatory bowel disease, psoriasis and ankylosing spondylitis. Arthritis Res Ther. 2019;21(1):133. https://doi.org/10.1186/s13075-019-1922-y
  39. Zhang B, Zhang X, Jin M, Hu L, Zang M, Qiu W, et al. CagA increases DNA methylation and decreases PTEN expression in human gastric cancer. Mol Med Rep. 2019;19(1):309-19.
  40. Pizarro-Cerda J, Chorev DS, Geiger B, Cossart P. The diverse family of Arp2/3 complexes. Trends Cell Biol. 2017;27(2):93-100. https://doi.org/10.1016/j.tcb.2016.08.001
  41. Demidchik V, Shabala S, Isayenkov S, Cuin TA, Pottosin I. Calcium transport across plant membranes: mechanisms and functions. New Phytol. 2018;220(1):49-69. https://doi.org/10.1111/nph.15266
  42. Costa L, Corre S, Michel V, Le Luel K, Fernandes J, Ziveri J, et al. USF1 defect drives p53 degradation during Helicobacter pylori infection and accelerates gastric carcinogenesis. Gut. 2020;69(9):1582-91. https://doi.org/10.1136/gutjnl-2019-318640
  43. Wang Y, Huang LH, Xu CX, Xiao J, Zhou L, Cao D, et al. Connexin 32 and 43 promoter methylation in Helicobacter pyloriassociated gastric tumorigenesis. World J Gastroenterol. 2014;20(33):11770-9. https://doi.org/10.3748/wjg.v20.i33.11770
  44. Hoffmann W. Trefoil factor family (TFF) peptides and their diverse molecular functions in mucus barrier protection and more: changing the paradigm. Int J Mol Sci. 2020;21(12):4535. https://doi.org/10.3390/ijms21124535
  45. Funato N, Taga Y, Laurie LE, Tometsuka C, Kusubata M, Ogawa-Goto K. The transcription factor HAND1 is involved in cortical bone mass through the regulation of collagen expression. Int J Mol Sci. 2020;21(22):8638. https://doi.org/10.3390/ijms21228638
  46. Lu XX, Yu JL, Ying LS, Han J, Wang S, Yu QM, et al. Stepwise cumulation of RUNX3 methylation mediated by Helicobacter pylori infection contributes to gastric carcinoma progression. Cancer. 2012;118(22):5507-17. https://doi.org/10.1002/cncr.27604
  47. Uehara S, Udagawa N, Kobayashi Y. Non-canonical Wnt signals regulate cytoskeletal remodeling in osteoclasts. Cell Mol Life Sci. 2018;75(20):3683-92. https://doi.org/10.1007/s00018-018-2881-1
  48. Zhu ZJ, Teng M, Li HZ, Zheng LP, Liu JL, Yao Y, et al. Virusencoded miR-155 ortholog in Marek's disease virus promotes cell proliferation via suppressing apoptosis by targeting tumor suppressor WWOX. Vet Microbiol. 2021;252:108919. https://doi.org/10.1016/j.vetmic.2020.108919
  49. Hatzistergos KE, Williams AR, Dykxhoorn D, Bellio MA, Yu W, Hare JM. Tumor suppressors RB1 and CDKN2a cooperatively regulate cell-cycle progression and differentiation during cardiomyocyte development and repair. Circ Res. 2019;124(8):1184-97. https://doi.org/10.1161/circresaha.118.314063
  50. Murakami M, Sato H, Taketomi Y. Updating phospholipase A2 biology. Biomolecules. 2020;10(10):1457. https://doi.org/10.3390/biom10101457
  51. Lork M, Verhelst K, Beyaert R. CYLD, A20 and OTULIN deubiquitinases in NF-κB signaling and cell death: so similar, yet so different. Cell Death Differ. 2017;24(7):1172-83. https://doi.org/10.1038/cdd.2017.46
  52. Ye M, Song Y, Pan S, Chu M, Wang ZW, Zhu X. Evolving roles of lysyl oxidase family in tumorigenesis and cancer therapy. Pharmacol Ther. 2020;215:107633. https://doi.org/10.1016/j.pharmthera.2020.107633
  53. Alvarez MC, Santos JC, Maniezzo N, Ladeira MS, da Silva AL, Scaletsky IC, et al. MGMT and MLH1 methylation in Helicobacter pylori-infected children and adults. World J Gastroenterol. 2013;19(20):3043-51. https://doi.org/10.3748/wjg.v19.i20.3043
  54. Ye Y, Wang X, Jeschke U, von Schonfeldt V. COX-2-PGE2-EPs in gynecological cancers. Arch Gynecol Obstet. 2020;301(6):1365-75. https://doi.org/10.1007/s00404-020-05559-6
  55. Alvarez MC, Fernandes J, Michel V, Touati E, Ribeiro ML. Effect of Helicobacter pylori infection on GATA-5 and TFF1 regulation, comparison between pediatric and adult patients. Dig Dis Sci. 2018;63(11):2889-97. https://doi.org/10.1007/s10620-018-5223-0
  56. Cheng AS, Li MS, Kang W, Cheng VY, Chou JL, Lau SS, et al. Helicobacter pylori causes epigenetic dysregulation of FOXD3 to promote gastric carcinogenesis. Gastroenterology. 2013;144(1):122-33.e9. https://doi.org/10.1053/j.gastro.2012.10.002
  57. Tanaka S, Nagashima H, Uotani T, Graham DY, Yamaoka Y. Autophagy-related genes in Helicobacter pylori infection. Helicobacter. 2017;22(3):e12376. https://doi.org/10.1111/hel.12376
  58. Miao R, Guo X, Zhi Q, Shi Y, Li L, Mao X, et al. VEZT, a novel putative tumor suppressor, suppresses the growth and tumorigenicity of gastric cancer. PLoS One. 2013;8(9):e74409. https://doi.org/10.1371/journal.pone.0074409
  59. Mashayekhi S, Saeidi Saedi H, Salehi Z, Soltanipour S, Mirzajani E. Effects of miR-27a, miR-196a2 and miR-146a polymorphisms on the risk of breast cancer. Br J Biomed Sci. 2018;75(2):76-81. https://doi.org/10.1080/09674845.2017.1399572
  60. Prinz C, Weber D. MicroRNA (miR) dysregulation during Helicobacter pylori-induced gastric inflammation and cancer development: critical importance of miR-155. Oncotarget. 2020;11(10):894-904. https://doi.org/10.18632/oncotarget.27520
  61. Yang Y, Huang Y, Lin W, Liu J, Chen X, Chen C, et al. Host miRNAs-microbiota interactions in gastric cancer. J Transl Med. 2022;20(1):52. https://doi.org/10.1186/s12967-022-03264-3
  62. Xie WQ, Tan SY, Wang XF. MiR-146a rs2910164 polymorphism increases risk of gastric cancer: a meta-analysis. World J Gastroenterol. 2014;20(41):15440-7. https://doi.org/10.3748/wjg.v20.i41.15440
  63. Ebrahimi Ghahnavieh L, Tabatabaeian H, Ebrahimi Ghahnavieh Z, Honardoost MA, Azadeh M, Moazeni Bistgani M, et al. Fluctuating expression of miR-584 in primary and high-grade gastric cancer. BMC Cancer. 2020;20(1):621. https://doi.org/10.1186/s12885-020-07116-5
  64. Chu DT, Nguyen TT, Tien NLB, Tran DK, Jeong JH, Anh PG, et al. Recent progress of stem cell therapy in cancer treatment: molecular mechanisms and potential applications. Cells. 2020;9(3):563. https://doi.org/10.3390/cells9030563
  65. Peek RM Jr, Fiske C, Wilson KT. Role of innate immunity in Helicobacter pylori-induced gastric malignancy. Physiol Rev. 2010;90(3):831-58. https://doi.org/10.1152/physrev.00039.2009
  66. van Putten JPM, Strijbis K. Transmembrane mucins: signaling receptors at the intersection of inflammation and cancer. J Innate Immun. 2017;9(3):281-99. https://doi.org/10.1159/000453594
  67. He Y, Wang C, Zhang X, Lu X, Xing J, Lv J, et al. Sustained exposure to Helicobacter pylori lysate inhibits apoptosis and autophagy of gastric epithelial cells. Front Oncol. 2020;10:581364. https://doi.org/10.3389/fonc.2020.581364
  68. Yamamoto H, Watanabe Y, Oikawa R, Morita R, Yoshida Y, Maehata T, et al. BARHL2 methylation using gastric wash DNA or gastric juice exosomal DNA is a useful marker for early detection of gastric cancer in an H. pylori-independent manner. Clin Transl Gastroenterol. 2016;7(7):e184. https://doi.org/10.1038/ctg.2016.40
  69. Schneider BG, Mera R, Piazuelo MB, Bravo JC, Zabaleta J, Delgado AG, et al. DNA methylation predicts progression of human gastric lesions. Cancer Epidemiol Biomarkers Prev. 2015;24(10):1607-13. https://doi.org/10.1158/1055-9965.EPI-15-0388
  70. Asada K, Nakajima T, Shimazu T, Yamamichi N, Maekita T, Yokoi C, et al. Demonstration of the usefulness of epigenetic cancer risk prediction by a multicentre prospective cohort study. Gut. 2015;64(3):388-96. https://doi.org/10.1136/gutjnl-2014-307094
  71. Zhao R, Liu Z, Xu W, Song L, Ren H, Ou Y, et al. Helicobacter pylori infection leads to KLF4 inactivation in gastric cancer through a TET1-mediated DNA methylation mechanism. Cancer Med. 2020;9(7):2551-63. https://doi.org/10.1002/cam4.2892
  72. Tahara T, Tahara S, Horiguchi N, Kato T, Shinkai Y, Okubo M, et al. Prostate stem cell antigen gene polymorphism is associated with H. pylori-related promoter DNA methylation in nonneoplastic gastric epithelium. Cancer Prev Res (Phila). 2019;12(9):579-84. https://doi.org/10.1158/1940-6207.capr-19-0035