Helicobacter pylori cytotoxin-associated gene A virulence and its association with the epithelial-mesenchymal transition in gastric cancer
DOI:
https://doi.org/10.12775/JEHS.2022.12.04.005Keywords
Helicobacter pylori, cytotoxin-associated gene A, epithelial-mesenchymal transition, gastric cancer, carcinogenesisAbstract
Gastric cancer is currently one of the most prevalent malignancies worldwide with a high mortality rate. Helicobacter pylori (H. pylori) infection significantly contributes to the onset and progression of gastric cancer mainly due to the induction of chronic inflammatory responses. The pathogenicity of H. pylori is associated with a vast number of virulence factors among which cytotoxin-associated gene A (CagA) plays a crucial role. We conducted a literature review of PubMed, Web of Science, and Scopus on September 1st, 2021. There were no limits regarding the year and the language of publication. Articles included in this review concerned human and animal studies. The following search string was applied during the search: (gastric cancer) AND (epithelial-mesenchymal transition) AND (Helicobacter pylori) AND (cytotoxin-associated gene A). The final analysis included 135 articles independently reviewed by the authors. H. pylori CagA-positive strains seem to be more virulent compared to the CagA-negative strains. CagA pathogenicity includes the increased secretion of pro-inflammatory cytokines, induction of cancer stem cell-like properties, apoptosis prevention, or overactivation of particular oncogenic pathways. H. pylori might induce epithelial-mesenchymal transition (EMT) via numerous pathways, among which CagA-related pathogenicity is considered to be of high significance. Mechanisms associated with CagA action are involved in the maintenance of chronic H. pylori infection, subsequent EMT induction, and further onset and progression of gastric cancer. Because of a huge number of H. pylori strains with different virulence mechanisms, the clinical outcome of patients is also associated with the particular type of strain that infected a patient.
References
Machlowska J, Baj J, Sitarz M. et al. Gastric Cancer: Epidemiology, Risk Factors, Classification, Genomic Characteristics and Treatment Strategies. Int J Mol Sci. 2020;21:4012. doi: 10.3390/ijms21114012.
Khazaei Z, MosaviJarrahi A, Momenabadi V, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide stomach cancers and their relationship with the human development index (HDI). World Cancer Res J. 2019;6:e1257.
Rawla P, Barsouk A. Epidemiology of gastric cancer: global trends, risk factors and prevention. Prz Gastroenterol. 2019;14(1):26-38. doi:10.5114/pg.2018.80001
Lauren P. The two histological main types of gastric carcinoma: Diffuse and so-called intestinal-type carcinoma. An attempt at a histo-clinical classification. Acta Pathol Microbiol Scand. 1965;64:31–49. doi: 10.1111/apm.1965.64.1.31.
Polkowski W, van Sandick J W, Offerhaus G J. et al. Prognostic value of Laurén classification and c-erbB-2 oncogene overexpression in adenocarcinoma of the esophagus and gastroesophageal junction. Ann Surg Oncol. 1999;6:290-297. doi: 10.1007/s10434-999-0290-2.
Sitarz R, Skierucha M, Mielko J. et al.Gastric cancer: epidemiology, prevention, classification, and treatment. Cancer Manag Res. 2018;10:239-248. doi: 10.2147/CMAR.S149619.
Choi J H, Choi Y W, Kang S Y. et al. Combination versus single-agent as palliative chemotherapy for gastric cancer. BMC Cancer. 2020;20:167. doi: 10.1186/s12885-020-6666-1.
Rawicz-Pruszyński K, van Sandick J W, Mielko J, et al. Current challenges in gastric cancer surgery: European perspective. Surg Oncol. 2018;27:650-656. doi: 10.1016/j.suronc.2018.08.004.
Yusefi A R, Lankarani K B, Bastani P. et al. Risk Factors for Gastric Cancer: A Systematic Review. Asian Pac J Cancer Prev. 2018;19:591–603. doi: 10.22034/APJCP.2018.19.3.591.
Berlth F, Bollschweiler E, Drebber U, Hoelscher A H, Moenig S. Pathohistological classification systems in gastric cancer: diagnostic relevance and prognostic value. World J Gastroenterol. 2014;20(19):5679-5684. doi:10.3748/wjg.v20.i19.5679
Jezerskyte E, van Berge Henegouwen M I, Cuesta M A. et al. Gastro-esophageal junction cancers: what is the best minimally invasive approach?. J Thorac Dis. 2017;9(Suppl 8):S751-S760. doi: 10.21037/jtd.2017.06.56.
Jezerskyte E, Saadeh L M, Hagens E R C. et al. Long-Term Quality of Life After Total Gastrectomy Versus Ivor Lewis Esophagectomy. World J Surg. 2020;44:838–848. doi: 10.1007/s00268-019-05281-8.
Siewert J R, Stein H J. Classification of adenocarcinoma of the esophagogastric junction. Br J Surg. 1998;85:1457–9. doi: 10.1046/j.1365-2168-1998.00940.x.
Zhang S, Orita H, Fukunaga T. Current surgical treatment of esophagogastric junction adenocarcinoma. World J Gastrointest Oncol. 2019;11:567-578. doi: 10.4251/wjgo.v11.i8.567.
Marano L, D'Ignazio A, Cammillini F. et al. Comparison between 7th and 8th edition of AJCC TNM staging system for gastric cancer: old problems and new perspectives. Transl Gastroenterol Hepatol. 2019;4:22. doi: 10.21037/tgh.2019.03.09.
Jung K, Park MI, Kim SE, et al. Borrmann Type 4 Advanced Gastric Cancer: Focus on the Development of Scirrhous Gastric Cancer. Clin Endosc. 2016;49(4):336-45. doi: 10.5946/ce.2016.057.
Berlth F, Bollschweiler E, Drebber U. et al. Pathohistological classification systems in gastric cancer: Diagnostic relevance and prognostic value. World J Gastroenterol. 2014;20:5679-5684. doi: 10.3748/wjg.v20.i19.5679.
Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2018 (5th edition). 2021;4:1-21 https://doi.org/10.1007/s10120-020-01042-y
Nagtegaal I D, Odze R D, Klimstra D. et al. The 2019 WHO classification of tumours of the digestive system. Histopathology. 2020;76:182-188. doi: 10.1111/his.13975. Epub 2019 Nov 13.
Yu Y. [Evaluation of traditional pathological classification at molecular classification era for gastric cancer]. Zhonghua Wei Chang Wai Ke Za Zhi = Chinese Journal of Gastrointestinal Surgery. 2014;17:18-20.
Daun T, Nienhold R, Paasinen-Sohns A, Frank A, Sachs M, Zlobec I, Cathomas G. Combined Simplified Molecular Classification of Gastric Adenocarcinoma, Enhanced by Lymph Node Status: An Integrative Approach. Cancers (Basel). 2021 Jul 24;13(15):3722. doi: 10.3390/cancers13153722.
Ventura L, Chiominto A, Discepoli S. et al. Lack of prognostic significance in Goseki grading of gastric carcinoma. J Exp Clin Cancer Res. 2002;21:225-227.
Moenig S, Baldus S E, Collet P H, et al. Histological grading in gastric cancer by Goseki classification: correlation with histopathological subtypes and prognosis. Anticancer Res. 2001;21:617-620.
Scilletta B, Lanteri R, Rapisarda C. et al. Gastric cancer: prognostic significance of the Goseki histological classification. Chir Ital. 2002;54:307-310.
Calik M, Calik I, Demirci E. et al. Goseki grade and tumour location influence survival of patients with gastric cancer. Asian Pac J Cancer Prev. 2014;15:1429-1434. doi: 10.7314/apjcp.2014.15.3.1429.
Songun I, van de Velde C J, Arends J W. et al. Classification of gastric carcinoma using the Goseki system provides prognostic information additional to TNM staging. Cancer. 1999;85:2114-8. doi: 10.1002/(sici)1097-0142(19990515)85:10<2114::aid-cncr3>3.0.co;2-u.
Sitarz R, Skierucha M, Mielko J, Offerhaus G J A, Maciejewski R, Polkowski W P. Gastric cancer: epidemiology, prevention, classification, and treatment. Cancer Manag Res. 2018;10:239-248
https://doi.org/10.2147/CMAR.S149619
Luebke T, Baldus S E, Grass G. et al. Histological grading in gastric cancer by Ming classification: correlation with histopathological subtypes, metastasis, and prognosis. World J Surg. 2005;29:1422-1428. doi: 10.1007/s00268-005-7795-z.
Cancer Genome Atlas Research Network. Comprehensive molecular characterization of gastric adenocarcinoma. Nature. 2014;513:202-9. doi: 10.1038/nature13480.
Cristescu R, Lee J, Nebozhyn M. et al. Molecular analysis of gastric cancer identifies subtypes associated with distinct clinical outcomes. Nat Med. 2015;21(5):449–456. doi: 10.1038/nm.3850.
Agnes A, Biondi A, Laurino A. et al. Global updates in the treatment of gastric cancer: a systematic review. Part 1: staging, classification and surgical treatment. Updates Surg. 2020;72:341-353. doi: 10.1007/s13304-020-00736-3.
Rawla P, Barsouk A. Epidemiology of gastric cancer: global trends, risk factors and prevention. Prz Gastroenterol. 2019;14:26-38. doi: 10.5114/pg.2018.80001.
Pucułek M, Machlowska J, Wierzbicki R. et al. Helicobacter pylori associated factors in the development of gastric cancer with special reference to the early-onset subtype. Oncotarget. 2018;9:31146-31162. doi: 10.18632/oncotarget.25757.
Zhao Y, Zhang J, Cheng A S L. et al. Gastric cancer: genome damaged by bugs. Oncogene. 2020;39:3427–3442. doi: 10.1038/s41388-020-1241-4.
Wang F, Meng W, Wang B. et al. Helicobacter pylori-induced gastric inflammation and gastric cancer. Cancer Lett. 2014;345:196–202. doi: 10.1016/j.canlet.2013.08.016.
Conteduca V, Sansonno D, Lauletta G. et al. H. pylori infection and gastric cancer: state of the art (review). Int J Oncol. 2013;42:5–18. doi: 10.3892/ijo.2012.1701.
Setia N, Clark J W, Duda D G. et al. Familial Gastric Cancers. Oncologist. 2015;20:1365-1377. doi: 10.1634/theoncologist.2015-0205.
Oliveira C, Pinheiro H, Figueiredo J. et al. Familial gastric cancer: genetic susceptibility, pathology, and implications for management. Lancet Oncol. 2015;16:e60-e70. doi: 10.1016/S1470-2045(14)71016-2.
Machlowska J, Kapusta P, Baj J. et al. High-Throughput Sequencing of Gastric Cancer Patients: Unravelling Genetic Predispositions Towards an Early-Onset Subtype. Cancers (Basel). 2020;12:1981. doi: 10.3390/cancers12071981.
Van der Post R S, Oliveira C, Guilford P. et al. Hereditary gastric cancer: what’s new? Update 2013–2018. Fam Cancer. 2019;18:363-367. doi: 10.1007/s10689-019-00127-7.
Boland C R, Yurgelun M B. Historical Perspective on Familial Gastric Cancer. Cell Mol Gastroenterol Hepatol. 2017;3:192-200. doi: 10.1016/j.jcmgh.2016.12.003.
Luo W, Fedda F, Lynch P, Tan D. CDH1 Gene and Hereditary Diffuse Gastric Cancer Syndrome: Molecular and Histological Alterations and Implications for Diagnosis And Treatment. Front Pharmacol. 2018 Dec 5;9:1421. doi: 10.3389/fphar.2018.01421.
Shenoy S. CDH1 (E-Cadherin) Mutation and Gastric Cancer: Genetics, Molecular Mechanisms and Guidelines for Management. Cancer Manag Res. 2019;11:10477-10486. doi: 10.2147/CMAR.S208818.
Di Ciaula A, Baj J, Garruti G, Celano G, De Angelis M, Wang H H, Di Palo D M, Bonfrate L, Wang D Q H, Portincasa P. Liver Steatosis, Gut-Liver Axis, Microbiome and Environmental Factors. A Never-Ending Bidirectional Cross-Talk. J. Clin Med. 2020;9(8):2648. https://doi.org/10.3390/jcm9082648
Poorolajal J, Moradi L, Mohammadi Y. et al. Risk factors for stomach cancer: a systematic review and meta-analysis. Epidemiol Health. 2020;42:e2020004. doi: 10.4178/epih.e2020004.
Ma K, Baloch Z, He T T. et al. Alcohol Consumption and Gastric Cancer Risk: A Meta-Analysis. Med Sci Monit. 2017;23:238-246. doi: 10.12659/msm.899423.
He Z, Zhao T T, Xu H M. et al. Association between alcohol consumption and the risk of gastric cancer: a meta-analysis of prospective cohort studies. Oncotarget. 2017;8:84459-84472. doi: 10.18632/oncotarget.20880.
Wang P L, Xiao F T, Gong B C, Liu F N. Alcohol drinking and gastric cancer risk: a meta-analysis of observational studies. Oncotarget. 2017;8(58):99013-99023. doi:10.18632/oncotarget.20918
Yoo J E, Shin D W, Han K. et al. Association of the Frequency and Quantity of Alcohol Consumption With Gastrointestinal Cancer. JAMA Netw Open. 2021;4(8):e2120382. doi:10.1001/jamanetworkopen.2021.20382
Jarl J, Heckley G, Brummer J. et al. Time characteristics of the effect of alcohol cessation on the risk of stomach cancer--a meta-analysis. BMC Public Health. 2013;13:600. doi: 10.1186/1471-2458-13-600.
Vahid F, Davoodi S H. Nutritional Factors Involved in the Etiology of Gastric Cancer: A Systematic Review. Nutr Cancer. 2021;73(3):376-390 doi:10.1080/01635581.2020.1756353
Baj J, Flieger W, Teresiński G. et al. Magnesium, Calcium, Potassium, Sodium, Phosphorus, Selenium, Zinc, and Chromium Levels in Alcohol Use Disorder: A Review. J. Clin. Med. 2020;9:1901. doi: 10.3390/jcm9061901.
Grochowski C, Blicharska E, Bogucki J. et al. Increased Aluminum Content in Certain Brain Structures is Correlated with Higher Silicon Concentration in Alcoholic Use Disorder. Molecules. 2019;24:1721. doi: 10.3390/molecules24091721.
Grochowski C, Blicharska E, Baj J. et al. Serum iron, Magnesium, Copper, and Manganese Levels in Alcoholism: A Systematic Review. Molecules. 2019;24:1361. doi: 10.3390/molecules24071361.
Lyons K, Le L C, Pham Y T,et al. Gastric cancer: epidemiology, biology, and prevention: a mini review. Eur J Cancer Prev. 2019;28:397-412. doi: 10.1097/CEJ.0000000000000480.
IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. IARC monographs on the evaluation of carcinogenic risks to humans Ingested nitrate and nitrite, and cyanobacterial peptide toxins. IARC Monogr Eval Carcinog Risks Hum. 2010;94:1–412.
Praud D, Rota M, Pelucchi C, Bertuccio P, Rosso T, Galeone C, Zhang Z F, Matsuo K, Ito H, Hu J, Johnson K C, Yu G P, Palli D, Ferraroni M, Muscat J, Lunet N, Peleteiro B, Malekzadeh R, Ye W, Song H, Zaridze D, Maximovitch D, Aragonés N, Castaño-Vinyals G, Vioque J, Navarrete-Muñoz E M, Pakseresht M, Pourfarzi F, Wolk A, Orsini N, Bellavia A, Håkansson N, Mu L, Pastorino R, Kurtz RC, Derakhshan M H, Lagiou A, Lagiou P, Boffetta P, Boccia S, Negri E, La Vecchia C. Cigarette smoking and gastric cancer in the Stomach Cancer Pooling (StoP) Project. Eur J Cancer Prev. 2018 Mar;27(2):124-133. doi: 10.1097/CEJ.0000000000000290.
Butt J, Varga M G, Wang T. et al. Smoking, Helicobacter pylori serology, and gastric cancer risk in prospective studies from China, Japan, and Korea. Cancer Prev Res. 2019;12:667-674. doi: 10.1158/1940-6207.CAPR-19-0238.
Zhang Y B, Pan X F, Chen J. et al. Combined lifestyle factors, incident cancer, and cancer mortality: a systematic review and meta-analysis of prospective cohort studies. Br J Cancer. 2020;22:1085-1093. doi: 10.1038/s41416-020-0741-x.
Schwingshackl L, Schwedhelm C, Galbete C. et al. Adherence to Mediterranean Diet and Risk of Cancer: An Updated Systematic Review and Meta-Analysis. Nutrients. 2017;9:1063. doi: 10.3390/nu9101063.
Phuoc L H, Sengngam K, Ogawa T, Ngatu N R, Ikeda S, Hoc T H, Phu P V, Minh D T, Ngoan L T. Fruit and Vegetable Intake and Stomach Cancer among Male Adults: A Case-Control Study in Northern Viet Nam. Asian Pac J Cancer Prev. 2020 Jul 1;21(7):2109-2115. doi: 10.31557/APJCP.2020.21.7.2109.
Bertuccio P, Rosato V, Andreano A, Ferraroni M, Decarli A, Edefonti V, La Vecchia C. Dietary patterns and gastric cancer risk: a systematic review and meta-analysis. Ann Oncol. 2013 Jun;24(6):1450-8. doi: 10.1093/annonc/mdt108.
Wang Q, Chen Y, Wang X. et al. Consumption of fruit, but not vegetables, may reduce risk of gastric cancer: results from a meta-analysis of cohort studies. Eur J Cancer. 2014;50:1498-1509. doi: 10.1016/j.ejca.2014.02.009.
Freedman N D, Subar A F, Hollenbeck A R. et al. Fruit and vegetable intake and gastric cancer risk in a large United States prospective cohort study. Cancer Causes Control. 2008;19:459-467. doi: 10.1007/s10552-007-9107-4.
Moss S F. The clinical evidence linking Helicobacter pylori to gastric cancer. Cell Mol Gastroenterol Hepatol. 2017;3:183-191. doi: 10.1016/j.jcmgh.2016.12.001.
Peng C, Li N S, Hu Y, Lu N H. Impact factors that modulate gastric cancer risk in Helicobacter pylori-infected rodent models. Helicobacter. 2019 Aug;24(4):e12580. doi: 10.1111/hel.12580.
Zamani M, Ebrahimtabar F, Zamani V. et al. Systematic review with meta‐analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther. 2018;47(7):868– 876. doi: 10.1111/apt.14561.
Alfarouk K O, Bashir A H H, Aljarbou A N. et al. The Possible Role of Helicobacter pylori in Gastric Cancer and Its Management. Front Oncol. 2019;9:75. doi: 10.3389/fonc.2019.00075.
Zhang X, Zhang P, Aboul-Soud MA. From inflammation to gastric cancer: Role of Helicobacter pylori (Review). Oncol Lett.2017;13:543-548. doi: 10.3892/ol.2016.5506.
Shafaie E, Saberi S, Esmaeili M. et al. Multiplex serology of Helicobacter pylori antigens in detection of current infection and atrophic gastritis-A simple and cost-efficient method. Microb Pathol. 2018;119:137-144. doi: 10.1016/j.micpath.2018.04.018.
Tang C L, Hao B, Zhang G X, Shi R H, Cheng W F. Helicobacter pylori tumor necrosis factor-α inducing protein promotes cytokine expression via nuclear factor-κB. World J Gastroenterol. 2013;19(3):399-403. doi:10.3748/wjg.v19.i3.399
Wessler S, Krisch L M, Elmer D P, Aberger F. From inflammation to gastric cancer - the importance of Hedgehog/GLI signaling in Helicobacter pylori-induced chronic inflammatory and neoplastic diseases. Cell Commun Signal. 2017;15(1):15. doi:10.1186/s12964-017-0171-4
Baj J, Forma A, Flieger W, Morawska I, Michalski A, Buszewicz G, Sitarz E, Portincasa P, Garruti G, Flieger M, Teresiński G. Helicobacter pylori Infection and Extragastric Diseases—A Focus on the Central Nervous System. Cells 2021;10:2191. https://doi.org/10.3390/cells10092191
Lee Y C, Chiang T H, Chou C K. et al. Association Between Helicobacter pylori Eradication and Gastric Cancer Incidence: A Systematic Review and Meta-analysis. Gastroenterology.b2016;150:113-1124 doi: 10.1053/j.gastro.2016.01.028.
Venerito M, Vasapolli R, Rokkas T. et al. Helicobacter pylori, gastric cancer and other gastrointestinal malignancies. Helicobacter. 2017;22(Suppl.1):e12413. doi: 10.1111/hel.12413.
Polyzos S A, Zeglinas C, Artemaki F. et al. Helicobacter pyloriinfection and esophageal adenocarcinoma: a review and a personal view. Ann Gastroenterol. 2018;31(1):8-13. doi:10.20524/aog.2017.0213
Baj J, Forma A, Sitarz M. et al. Helicobacter pylori Virulence Factors—Mechanisms of Bacterial Pathogenicity in the Gastric Microenvironment. Cells. 2021;10:27. doi: 10.3390/cells10010027.
Fiorentino M, Ding H, Blanchard T G, Czinn S J, Sztein M B, Fasano A. Helicobacter pylori-Induced Disruption of Monolayer Permeability and Proinflammatory Cytokine Secretion in Polarized Human Gastric Epithelial Cells. Infect Immun. 2013;81(3):876-883. doi:10.1128/iai.01406-12
Olivera-Severo D, Uberti A F, Marques M S. et al. A New Role for Helicobacter pylori Urease: Contributions to Angiogenesis. Front Microbiol. 2017;8:1883. doi:10.3389/fmicb.2017.01883.
Graham D Y, Miftahussurur M. Helicobacter pylori urease for diagnosis of Helicobacter pylori infection: A mini review. J Adv Res. 2018;13:51-57. doi: 10.1016/j.jare.2018.01.006.
Graham D Y, Miftahussurur. M. Helicobacter pylori urease for diagnosis of Helicobacter pylori infection: A mini review. J Adv Res. 2018;13:51-57. doi: 10.1016/j.jare.2018.01.006.
Pucułek M, Baj J, Portincasa P. et al. The morphology and application of stem cells in digestive system surgery. Folia Morphol (Warsz). 2020;80(1):13-19 doi:10.5603/FM.a2020.0024.
Minkara M S, Ucisik M N, Weaver M N. et al. Molecular Dynamics Study of Helicobacter pylori Urease. J Chem Theory Comput. 2014;10(5):1852–62. doi: 10.1021/ct5000023.
Hatakeyama M. Helicobacter pylori CagA and gastric cancer: a paradigm for hit-and-run carcinogenesis. Cell Host Microbe. 2014;12;15(3):306-16. doi: 10.1016/j.chom.2014.02.008.
Hatakeyama M. Structure and function of Helicobacter pylori CagA, the first-identified bacterial protein involved in human cancer. Proc Jpn Acad Ser B Phys Biol Sci. 2017;93:196-219. doi: 10.2183/pjab.93.013.
Tebbutt N C, Giraud AS, Inglese M. et al. Reciprocal regulation of gastrointestinal homeostasis by SHP2 and STAT-mediated trefoil gene activation in gp130 mutant mice. Nat Med. 2002;8:1089-97.
doi: 10.1038/nm763.
Lee I O, Kim J H, Choi Y J. et al. Helicobacter pylori CagA phosphorylation status determines the gp130-activated SHP2/ERK and JAK/STAT signal transduction pathways in gastric epithelial cells. J Biol Chem. 2010;285:16042-16050. doi: 10.1074/jbc.M110.111054.
Sierra J C, Piazuelo M B, Luis P B. et al. Spermine oxidase mediates Helicobacter pylori-induced gastric inflammation, DNA damage, and carcinogenic signaling. Oncogene. 2020;39(22):4465-4474. doi:10.1038/s41388-020-1304-6
Jeyamani L, Jayarajan J, Leelakrishnan V, Swaminathan M. CagA and VacA genes of Helicobacter pylori and their clinical relevance. Indian J Pathol Microbiol. 2018;61(1):66-69. doi: 10.4103/IJPM.IJPM_234_17.
Utsch C, Haas R. VacA’s Induction of VacA-Containing Vacuoles (VCVs) and Their Immunomodulatory Activities on Human T Cells. Toxins (Basel) 2016;8(6):190. https://doi.org/10.3390/toxins8060190
Yamasaki E, Wada A, Kumatori A. et al. Helicobacter pylori vacuolating cytotoxin induces activation of the proapoptotic proteins Bax and Bak, leading to cytochrome c release and cell death, independent of vacuolation. J Biol Chem. 2006;281:11250-9. doi: 10.1074/jbc.M509404200.
Luo J J, Li C Y, Liu S, Yu W, Tang S Y, Cai H L, Zhang Y. Overexpression of Helicobacter pylori VacA N-terminal fragment induces proinflammatory cytokine expression and apoptosis in human monocytic cell line through activation of NF-κB. Can J Microbiol. 2013 Aug;59(8):523-33. doi: 10.1139/cjm-2013-0021.
Hisatsune J, Yamasaki E, Nakayama M. et al. Helicobacter pylori VacA enhances prostaglandin E2 production through induction of cyclooxygenase 2 expression via a p38 mitogen-activated protein kinase/activating transcription factor 2 cascade in AZ-521 cells. Infect Immun. 2007;75:4472-81. doi: 10.1128/IAI.00500-07.
Nakayama M, Hisatsune J, Yamasaki E. et al. Helicobacter pylori VacA-induced inhibition of GSK3 through the PI3K/Akt signaling pathway. J Biol Chem. 2009;284:1612-9. doi: 10.1074/jbc.M806981200.
Foegeding N J, Caston R R, McClain M S. et al. An Overview of Helicobacter pylori VacA Toxin Biology. Toxins (Basel). 2016;8:173. doi: 10.3390/toxins8060173.
Matos R, Amorim I, Magalhães A, Haesebrouck F, Gärtner F, Reis C A. Adhesion of Helicobacter Species to the Human Gastric Mucosa: A Deep Look Into Glycans Role. Front MolBiosci. Front Mol Biosci. 2021;8:656439. doi: 10.3389/fmolb.2021.656439.
Oleastro M, Ménard A. The Role of Helicobacter pylori Outer Membrane Proteins in Adherence and Pathogenesis. Biology (Basel). 2013;2:1110–1134. doi: 10.3390/biology2031110.
Ramachandran M, Jin C, Yu D, Eriksson F, Essand M. Vector-encoded Helicobacter pylori neutrophil-activating protein promotes maturation of dendritic cells with Th1 polarization and improved migration. J Immunol. 2014;193(5):2287-96. doi: 10.4049/jimmunol.1400339.
Fu H W. Helicobacter pylori neutrophil-activating protein: From molecular pathogenesis to clinical applications. World J Gastroenterol. 2014;20:5294. doi: 10.3748/wjg.v20.i18.5294.
Lee K E, Khoi P N, Xia Y. et al. Helicobacter pylori and interleukin-8 in gastric cancer. World J Gastroenterol. 2013;19(45):8192-8202. doi:10.3748/wjg.v19.i45.8192
Mendoza J A, Weinberger K K, Swan M J. The Hsp60 protein of helicobacter pylori displays chaperone activity under acidic conditions. Biochem Biophys Rep. 2017;9:95–99. doi: 10.1016/j.bbrep.2016.11.011.
Bodoor K, Jalboush S A, Matalka I, Abu-Sheikha A, Waq R A, Ebwaini H, Abu-Awad A, Fayyad L, Al-Arjat J, Haddad Y. Heat Shock Protein Association with Clinico-Pathological Characteristics of Gastric Cancer in Jordan : HSP70 is Predictive of Poor Prognosis. Asian Pac J Cancer Prev. 2016;17(8):3929-37.
Tao L, Zou H, Huang Z. Effects of Helicobacter pylori and Heat Shock Protein 70 on the Proliferation of Human Gastric Epithelial Cells. Gastroenterol Res Pract. 2014:1–5. doi: 10.1155/2014/794342
Salton F, Volpe M C, Confalonieri M. Epithelial⁻Mesenchymal Transition in the Pathogenesis of Idiopathic Pulmonary Fibrosis. Medicina (Kaunas). 2019 Mar 28;55(4):83. doi: 10.3390/medicina55040083.
Singh M, Yelle N, Venugopal C, Singh S K. EMT: Mechanisms and therapeutic implications. Pharmacol Ther. 2018 Feb;182:80-94. doi: 10.1016/j.pharmthera.2017.08.009.
Heerboth S, Housman G, Leary M, et al. EMT and tumor metastasis. Clin Transl Med. 2015 Feb 26;4:6. doi: 10.1186/s40169-015-0048-3.
Xu Q, Sun Q, Zhang J. et al. Downregulation of miR-153 contributes to epithelial-mesenchymal transition and tumor metastasis in human epithelial cancer. Carcinogenesis. 2013;34:539-549. doi: 10.1093/carcin/bgs374.
Baj J, Brzozowska K, Forma A. et al. Immunological Aspects of the Tumor Microenvironment and Epithelial-Mesenchymal Transition in Gastric Carcinogenesis. Int J Mol Sci. 2020;21:2544. doi: 10.3390/ijms21072544.
Loh C Y, Chai J Y, Tang T F. et al. The E-Cadherin and N-Cadherin Switch in Epithelial-to-Mesenchymal Transition: Signaling, Therapeutic Implications, and Challenges. Cells. 2019;8:1118. doi: 10.3390/cells8101118.
Guo J, Wang B, Fu Z. et al. Hypoxic Microenvironment Induces EMT and Upgrades Stem-Like Properties of Gastric Cancer Cells. Technol Cancer Res Treat. 2016;15:60-8. doi: 10.1177/1533034614566413.
Kozak J, Forma A, Czeczelewski M. et al. Inhibition or Reversal of the Epithelial-Mesenchymal Transition in Gastric Cancer: Pharmacological Approaches. Int J Mol Sci. 2020;22:277. doi: 10.3390/ijms22010277.
Voon D C, Wang H, Koo J K. et al. Runx3 protects gastric epithelial cells against epithelial-mesenchymal transition-induced cellular plasticity and tumorigenicity. Stem Cells. 2012;30:2088-99. doi: 10.1002/stem.1183.
Nitta T, Mitsuhashi T, Hatanaka Y. et al. Prognostic significance of epithelial–mesenchymal transition-related markers in extrahepatic cholangiocarcinoma: comprehensive immunohistochemical study using a tissue microarray. Br J Cancer 2014;111(7):1363-72. https://doi.org/10.1038/bjc.2014.415
Stein M, Ruggiero P, Rappuoli R. et al. Helicobacter pylori CagA: From Pathogenic Mechanisms to Its Use as an Anti-Cancer Vaccine. Front Immunol. 2013;4:328. doi: 10.3389/fimmu.2013.00328.
Yu H, Zeng J, Liang X. et al. Helicobacter pylori promotes epithelial-mesenchymal transition in gastric cancer by downregulating programmed cell death protein 4 (PDCD4). PLoS One. 2014;9:e105306. doi: 10.1371/journal.pone.0105306.
Bessède E, Staedel C, Amador L A A. et al. Helicobacter pylori generates cells with cancer stem cell properties via epithelial–mesenchymal transition-like changes. Oncogene. 2013;33:4123–31. doi: 10.1038/onc.2013.380
Liu C, Zhang Y, Zhan J. et al. Interleukin-23A is associated with tumor growth in Helicobacter-pylori-related human gastric cancer. Cancer Cell Int. 2014;14:104. doi: 10.1186/s12935-014-0104-x.
Posselt G, Wiesauer M, Chichirau B E. et al. Helicobacter pylori-controlled c-Abl localization promotes cell migration and limits apoptosis. Cell Commun Signal. 2019;17:10. doi:10.1186/s12964-019-0323-9.
Baj J, Korona-Głowniak I, Forma A. et al. Mechanisms of the Epithelial–Mesenchymal Transition and Tumor Microenvironment in Helicobacter pylori-Induced Gastric Cancer. Cells. 2020;9:1055. doi: 10.3390/cells9041055.
Molina-Castro S E, Tiffon C, Giraud J. et al. The Hippo Kinase LATS2 Controls Helicobacter pylori-Induced Epithelial-Mesenchymal Transition and Intestinal Metaplasia in Gastric Mucosa. Cell Mol Gastroenterol Hepatol. 2020;9:257-276. doi: 10.1016/j.jcmgh.2019.10.007.
Li N, Feng Y, Hu Y. et al. Helicobacter pylori CagA promotes epithelial mesenchymal transition in gastric carcinogenesis via triggering oncogenic YAP pathway. J Exp Clin Cancer Res. 2018;37:280. doi: 10.1186/s13046-018-0962-5.
Shi Y, Yang Z, Zhang T. et al. SIRT1-targeted miR-543 autophagy inhibition and epithelial–mesenchymal transition promotion in Helicobacter pylori CagA-associated gastric cancer. Cell Death Dis. 2019;10:625. doi: 10.1038/s41419-019-1859-8.
Yoon J H, Seo H S, Choi S S. et al. Gastrokine 1 inhibits the carcinogenic potentials of Helicobacter pylori CagA. Carcinogenesis. 2014;35:2619–2629. doi: 10.1093/carcin/bgu199.
Choi S I, Yoon C, Park M R. et al. CDX1 Expression Induced by CagA-Expressing Helicobacter pylori Promotes Gastric Tumorigenesis. Mol Cancer Res. 2019;17:2169–83. doi: 10.1158/1541-7786.MCR-19-0181.
Park M J, Kim HY, Kim K. et al. Homeodomain transcription factor CDX1 is required for the transcriptional induction of PPARgamma in intestinal cell differentiation. FEBS letters. 2009;583:29-35. doi: 10.1016/j.febslet.2008.11.030.
Fujii Y, Yoshihashi K, Suzuki H. et al. CDX1 confers intestinal phenotype on gastric epithelial cells via induction of stemness-associated reprogramming factors SALL4 and KLF5. Proc Natl Acad Sci U S A. 2012;109:20584-9. doi: 10.1073/pnas.1208651109.
Krzysiek‐Maczka G, Targosz A, Szczyrk U. et al. Role of Helicobacter pylori infection in cancer‐associated fibroblast‐induced epithelial‐mesenchymal transition in vitro. Helicobacter. 2018;23:e12538. doi: 10.1111/hel.12538.
Krzysiek-Maczka G, Targosz A, Szczyrk U. et al. Involvement of epithelial-mesenchymal transition-inducing transcription factors in the mechanism of Helicobacter pylori-induced fibroblasts activation. J Physio Pharmacol. 2019;70:727-736. doi: 10.26402/jpp.2019.5.08.
Huang L, Wang Z Y, Pan D D. Penicillin‑binding protein 1A mutation‑positive Helicobacter pylori promotes epithelial‑mesenchymal transition in gastric cancer via the suppression of microRNA‑134. Int J Oncol. 2019;54:916–928. doi: 10.3892/ijo.2018.4665.
Jin H F, Dai J F, Meng L N. et al. Ling n-Butyl Alcohol Extract Inhibits AGS Cell Helicobacter pyloriCagA VacA Promoted Invasiveness by Down-Regulating Caudal Type Homeobox Transcription Factor and Claudin-2 Expression. Chin J Integr Med. 2020;26:122-129. doi: 10.1007/s11655-017-2958-y.
Lee DG, Kim HS, Lee YS. et al. Helicobacter pylori CagA promotes Snail-mediated epithelial–mesenchymal transition by reducing GSK-3 activity. Nature Communications.2014;5:4423.
Lin L, Wei H, Yi J. et al. Chronic CagA‐positive Helicobacter pylori infection with MNNG stimulation synergistically induces mesenchymal and cancer stem cell‐like properties in gastric mucosal epithelial cells. J Cell Biochem. 2019;120:17635–49. doi: 10.1002/jcb.29031.
Yu H, Zeng J, Liang X. et al. Helicobacter pylori Promotes Epithelial–Mesenchymal Transition in Gastric Cancer by Downregulating Programmed Cell Death Protein 4 (PDCD4). PLoS ONE. 2014;9:e105306. doi: 10.1371/journal.pone.0105306.
Sougleri I S, Papadakos K S, Zadik M P. et al. Helicobacter pyloriCagA protein induces factors involved in the epithelial to mesenchymal transition (EMT) in infected gastric epithelial cells in an EPIYA- phosphorylation-dependent manner. FEBS J. 2015;283:206–20. doi: 10.1111/febs.13592.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2022 Iga Dudek, Alicja Forma, Justyna Hamerska, Michał Flieger, Jacek Januszewski, Tomasz Cywka, Joanna Kozak, Jacek Baj
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
The periodical offers access to content in the Open Access system under the Creative Commons Attribution-NonCommercial-ShareAlike 4.0
Stats
Number of views and downloads: 471
Number of citations: 0