Helicobacter pylori dysregulates the expression of autophagy-related genes in human gastric adenocarcinoma cell line in vitro
-
Marzieh Esmaeilzadeh
,
Farshid Kafilzadeh
,
Mohammad Kargar
,
Hamid Asadzadeh Aghdaei
,
Abbas Yadegar
Abstract
Background and Objectives: Studies have indicated that Helicobacter pylori (H. pylori) infection could correlate with autophagy dysregulation. This research was undertaken to investigate whether H. pylori can dysregulate the expression of genes related to autophagy in human gastric adenocarcinoma (AGS) cells.
Materials and Methods: Ten H. pylori clinical isolates recovered from peptic ulcer disease (PUD) and chronic gastritis (CG) patients were used for cell infection assays. AGS cells infected with H. pylori strains at a multiplicity of infection (MOI) of 100 were incubated at 37°C for 12 h. The expression of autophagy-related genes (atg5, atg12, atg16L1, LC3B, and beclin-1) was determined in AGS cells by RT-qPCR. ELISA was applied to measure IL-8 production.
Results: The gene expression of atg5, atg12, atg16L1, LC3B was upregulated by both CG and PUD strains. The overexpression was more pronounced in PUD than CG strains. On the contrary, beclin-1 gene was downregulated in all H. pylori-infected AGS cells. In addition, H. pylori strains could significantly produce IL-8 in AGS cells.
Conclusion: Our in vitro study demonstrates that H. pylori could alter the expression of autophagy-related genes. Further investigation could precisely uncover the mechanism whereby H. pylori dysregulates host autophagy.
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12. Šterbenc A, Jarc E, Poljak M, Homan M. Helicobacter pylori virulence genes. World J Gastroenterol 2019; 25: 4870-4884.
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20. Farzi N, Yadegar A, Aghdaei HA, Yamaoka Y, Zali MR. Genetic diversity and functional analysis of oipA gene in association with other virulence factors among Helicobacter pylori isolates from Iranian patients with different gastric diseases. Infect Genet Evol 2018; 60: 26-34.
21. Azizimoghaddam Y, Kermanpour S, Mirzaei N, Houri H, Nabavi-Rad A, Asadzadeh Aghdaei H, et al. Genetic diversity of Helicobacter pylori type IV secretion system cagI and cagN genes and their association with clinical diseases. Sci Rep 2023; 13: 10264.
22. Tang B, Li N, Gu J, Zhuang Y, Li Q, Wang HG, et al. Compromised autophagy by MIR30B benefits the intracellular survival of Helicobacter pylori. Autophagy 2012; 8: 1045-1057.
23. Wu M, Chen B, Pan X, Su J. Prognostic value of autophagy-related proteins in human gastric cancer. Cancer Manag Res 2020; 12: 13527-13540.
24. Li J, Wang P, Xie Z, Yang R, Li Y, Wu X, et al. Elevated TRAF4 expression impaired LPS-induced autophagy in mesenchymal stem cells from ankylosing spondylitis patients. Exp Mol Med 2017; 49(6): e343.
25. Keulers TG, Koch A, van Gisbergen MW, Barbeau LMO, Zonneveld MI, de Jong MC, et al. ATG12 deficiency results in intracellular glutamine depletion, abrogation of tumor hypoxia and a favorable prognosis in cancer. Autophagy 2022; 18: 1898-1914.
26. Fu J, Bian L, Zhao L, Dong Z, Gao X, Luan H, et al. Identification of genes for normalization of quantitative real-time PCR data in ovarian tissues. Acta Biochim Biophys Sin (Shanghai) 2010; 42: 568-574.
27. Barber MF, Fitzgerald JR. Mechanisms of host adaptation by bacterial pathogens. FEMS Microbiol Rev 2024; 48: fuae019.
28. Li D, Wu M. Pattern recognition receptors in health and diseases. Signal Transduct Target Ther 2021; 6: 291.
29. Yuk J-M, Yoshimori T, Jo E-K. Autophagy and bacterial infectious diseases. Exp Mol Med 2012; 44: 99-108.
30. Huang J, Brumell JH. Bacteria–autophagy interplay: a battle for survival. Nat Rev Microbiol 2014; 12: 101-114.
31. Bah A, Vergne I. Macrophage autophagy and bacterial infections. Front Immunol 2017; 8: 1483.
32. Chong A, Wehrly TD, Child R, Hansen B, Hwang S, Virgin HW, et al. Cytosolic clearance of replication-deficient mutants reveals Francisella tularensis interactions with the autophagic pathway. Autophagy 2012; 8: 1342-1356.
33. Deuretzbacher A, Czymmeck N, Reimer R, Trulzsch K, Gaus K, Hohenberg H, et al. β1 integrin-dependent engulfment of Yersinia enterocolitica by macrophages is coupled to the activation of autophagy and suppressed by type III protein secretion. J Immunol 2009; 183: 5847-5860.
34. Choi J-H, Cheong T-C, Ha N-Y, Ko Y, Cho C-H, Jeon J-H, et al. Orientia tsutsugamushi subverts dendritic cell functions by escaping from autophagy and impairing their migration. PLoS Negl Trop Dis 2013; 7(1): e1981.
35. Wang Y, Du J, Wu X, Abdelrehem A, Ren Y, Liu C, et al. Crosstalk between autophagy and microbiota in cancer progression. Mol Cancer 2021; 20: 163.
36. Cho TJ, Wee SW, Woo VH, Choi JI, Kim SJ, Shin HI, et al. Porphyromonas gingivalis-induced autophagy suppresses cell proliferation through G1 arrest in oral cancer cells. Arch Oral Biol 2014; 59: 370-378.
37. Yu T, Guo F, Yu Y, Sun T, Ma D, Han J, et al. Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy. Cell 2017; 170: 548-563. e16.
38. Courtois S, Haykal M, Bodineau C, Sifré E, Azzi-Martin L, Ménard A, et al. Autophagy induced by Helicobacter pylori infection is necessary for gastric cancer stem cell emergence. Gastric Cancer 2021; 24: 133-144.
39. Zhang F, Chen C, Hu J, Su R, Zhang J, Han Z, et al. Molecular mechanism of Helicobacter pylori-induced autophagy in gastric cancer. Oncol Lett 2019; 18: 6221-6227.
40. Halder P, Datta C, Kumar R, Sharma AK, Basu J, Kundu M. The secreted antigen, HP0175, of Helicobacter pylori links the unfolded protein response (UPR) to autophagy in gastric epithelial cells. Cell Microbiol 2015; 17: 714-729.
41. Pareja ME, Colombo MI. Autophagic clearance of bacterial pathogens: molecular recognition of intracellular microorganisms. Front Cell Infect Microbiol 2013; 3: 54.
42. Tanaka S, Nagashima H, Uotani T, Graham DY, Yamaoka Y. Autophagy-related genes in Helicobacter pylori infection. Helicobacter 2017; 22: 10.1111/hel.12376.
43. Wang Y-h, Lv Z-f, Zhong Y, Liu D-s, Chen S-p, Xie Y. The internalization of Helicobacter pylori plays a role in the failure of H. pylori eradication. Helicobacter 2017; 22: 10.1111/hel.12324.
44. Capurro MI, Greenfield LK, Prashar A, Xia S, Abdullah M, Wong H, et al. VacA generates a protective intracellular reservoir for Helicobacter pylori that is eliminated by activation of the lysosomal calcium channel TRPML1. Nat Microbiol 2019; 4: 1411-1423.
45. Xie C, Li N, Wang H, He C, Hu Y, Peng C, et al. Inhibition of autophagy aggravates DNA damage response and gastric tumorigenesis via Rad51 ubiquitination in response to H. pylori infection. Gut Microbes 2020; 11: 1567-1589.
46. Yamaoka Y. Mechanisms of disease: Helicobacter pylori virulence factors. Nat Rev Gastroenterol Hepatol 2010; 7: 629-641.
47. Sadeghloo Z, Nabavi-Rad A, Zali MR, Klionsky DJ, Yadegar A. The interplay between probiotics and host autophagy: mechanisms of action and emerging insights. Autophagy 2025; 21: 260-282.
48. Yang Y, Shu X, Xie C. An overview of autophagy in Helicobacter pylori infection and related gastric cancer. Front Cell Infect Microbiol 2022; 12: 847716.
49. Puissant A, Fenouille N, Auberger P. When autophagy meets cancer through p62/SQSTM1. Am J Cancer Res 2012; 2: 397-413.
50. 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: 203.
51. Li N, Tang B, Jia YP, Zhu P, Zhuang Y, Fang Y, et al. Helicobacter pylori CagA protein negatively regulates autophagy and promotes inflammatory response via c-Met-PI3K/Akt-mTOR signaling pathway. Front Cell Infect Microbiol 2017; 7: 417.
52. Irving AT, Mimuro H, Kufer TA, Lo C, Wheeler R, Turner LJ, et al. The immune receptor NOD1 and kinase RIP2 interact with bacterial peptidoglycan on early endosomes to promote autophagy and inflammatory signaling. Cell Host Microbe 2014; 15: 623-635.
53. Huang X, Wang C, Sun J, Luo J, You J, Liao L, et al. Clinical value of CagA, c-Met, PI3K and Beclin-1 expressed in gastric cancer and their association with prognosis. Oncol Lett 2018; 15: 947-955.
54. Wang RC, Wei Y, An Z, Zou Z, Xiao G, Bhagat G, et al. Akt-mediated regulation of autophagy and tumorigenesis through Beclin 1 phosphorylation. Science 2012; 338: 956-959.
55. Zhu X, Wang Y, Xue W, Wang R, Wang L, Zhu ML, et al. The VEGFR-2 protein and the VEGFR-2 rs1870377 A>T genetic polymorphism are prognostic factors for gastric cancer. Cancer Biol Ther 2019; 20: 497-504.
2. Duan Y, Xu Y, Dou Y, Xu D. Helicobacter pylori and gastric cancer: mechanisms and new perspectives. J Hematol Oncol 2025; 18: 10.
3. Díaz P, Valenzuela Valderrama M, Bravo J, Quest AFG. Helicobacter pylori and gastric cancer: adaptive cellular mechanisms involved in disease progression. Front Microbiol 2018; 9: 5.
4. Tshibangu-Kabamba E, Yamaoka Y. Helicobacter pylori infection and antibiotic resistance - from biology to clinical implications. Nat Rev Gastroenterol Hepatol 2021; 18: 613-629.
5. Sonnenberg A. Epidemiology of Helicobacter pylori. Aliment Pharmacol Ther 2022; 55 Suppl 1: S1-S13.
6. Shirani M, Pakzad R, Haddadi MH, Akrami S, Asadi A, Kazemian H, et al. The global prevalence of gastric cancer in Helicobacter pylori-infected individuals: a systematic review and meta-analysis. BMC Infect Dis 2023; 23: 543.
7. Wroblewski LE, Peek RM Jr, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 2010; 23: 713-739.
8. Peek RM Jr, Crabtree JE. Helicobacter infection and gastric neoplasia. J Pathol 2006; 208: 233-248.
9. Mera R, Fontham ET, Bravo LE, Bravo JC, Piazuelo MB, Camargo MC, et al. Long term follow up of patients treated for Helicobacter pylori infection. Gut 2005; 54: 1536-1540.
10. Nabavi-Rad A, Sadeghi A, Asadzadeh Aghdaei H, Yadegar A, Smith SM, Zali MR. The double-edged sword of probiotic supplementation on gut microbiota structure in Helicobacter pylori management. Gut Microbes 2022; 14: 2108655.
11. Kao C-Y, Sheu B-S, Wu J-J. Helicobacter pylori infection: An overview of bacterial virulence factors and pathogenesis. Biomed J 2016; 39: 14-23.
12. Šterbenc A, Jarc E, Poljak M, Homan M. Helicobacter pylori virulence genes. World J Gastroenterol 2019; 25: 4870-4884.
13. Nabavi-Rad A, Yadegar A, Sadeghi A, Aghdaei HA, Zali MR, Klionsky DJ, et al. The interaction between autophagy, Helicobacter pylori, and gut microbiota in gastric carcinogenesis. Trends Microbiol 2023; 31: 1024-1043.
14. Li X, He S, Ma B. Autophagy and autophagy-related proteins in cancer. Mol Cancer 2020; 19: 12.
15. Sadeghloo Z, Saffarian P, Hakemi-Vala M, Sadeghi A, Yadegar A. The modulatory effect of Lactobacillus gasseri ATCC 33323 on autophagy induced by extracellular vesicles of Helicobacter pylori in gastric epithelial cells in vitro. Microb Pathog 2024; 188: 106559.
16. Ieni A, Cardia R, Giuffrè G, Rigoli L, Caruso RA, Tuccari G. Immunohistochemical expression of autophagy-related proteins in advanced tubular gastric adenocarcinomas and its implications. Cancers (Basel) 2019; 11: 389.
17. Takahashi-Kanemitsu A, Knight CT, Hatakeyama M. Molecular anatomy and pathogenic actions of Helicobacter pylori CagA that underpin gastric carcinogenesis. Cell Mol Immunol 2020; 17: 50-63.
18. Eslami M, Yousefi B, Kokhaei P, Arabkari V, Ghasemian A. Current information on the association of Helicobacter pylori with autophagy and gastric cancer. J Cell Physiol 2019; 234: 14800-14811.
19. Abdullah M, Greenfield LK, Bronte-Tinkew D, Capurro MI, Rizzuti D, Jones NL. VacA promotes CagA accumulation in gastric epithelial cells during Helicobacter pylori infection. Sci Rep 2019; 9: 38.
20. Farzi N, Yadegar A, Aghdaei HA, Yamaoka Y, Zali MR. Genetic diversity and functional analysis of oipA gene in association with other virulence factors among Helicobacter pylori isolates from Iranian patients with different gastric diseases. Infect Genet Evol 2018; 60: 26-34.
21. Azizimoghaddam Y, Kermanpour S, Mirzaei N, Houri H, Nabavi-Rad A, Asadzadeh Aghdaei H, et al. Genetic diversity of Helicobacter pylori type IV secretion system cagI and cagN genes and their association with clinical diseases. Sci Rep 2023; 13: 10264.
22. Tang B, Li N, Gu J, Zhuang Y, Li Q, Wang HG, et al. Compromised autophagy by MIR30B benefits the intracellular survival of Helicobacter pylori. Autophagy 2012; 8: 1045-1057.
23. Wu M, Chen B, Pan X, Su J. Prognostic value of autophagy-related proteins in human gastric cancer. Cancer Manag Res 2020; 12: 13527-13540.
24. Li J, Wang P, Xie Z, Yang R, Li Y, Wu X, et al. Elevated TRAF4 expression impaired LPS-induced autophagy in mesenchymal stem cells from ankylosing spondylitis patients. Exp Mol Med 2017; 49(6): e343.
25. Keulers TG, Koch A, van Gisbergen MW, Barbeau LMO, Zonneveld MI, de Jong MC, et al. ATG12 deficiency results in intracellular glutamine depletion, abrogation of tumor hypoxia and a favorable prognosis in cancer. Autophagy 2022; 18: 1898-1914.
26. Fu J, Bian L, Zhao L, Dong Z, Gao X, Luan H, et al. Identification of genes for normalization of quantitative real-time PCR data in ovarian tissues. Acta Biochim Biophys Sin (Shanghai) 2010; 42: 568-574.
27. Barber MF, Fitzgerald JR. Mechanisms of host adaptation by bacterial pathogens. FEMS Microbiol Rev 2024; 48: fuae019.
28. Li D, Wu M. Pattern recognition receptors in health and diseases. Signal Transduct Target Ther 2021; 6: 291.
29. Yuk J-M, Yoshimori T, Jo E-K. Autophagy and bacterial infectious diseases. Exp Mol Med 2012; 44: 99-108.
30. Huang J, Brumell JH. Bacteria–autophagy interplay: a battle for survival. Nat Rev Microbiol 2014; 12: 101-114.
31. Bah A, Vergne I. Macrophage autophagy and bacterial infections. Front Immunol 2017; 8: 1483.
32. Chong A, Wehrly TD, Child R, Hansen B, Hwang S, Virgin HW, et al. Cytosolic clearance of replication-deficient mutants reveals Francisella tularensis interactions with the autophagic pathway. Autophagy 2012; 8: 1342-1356.
33. Deuretzbacher A, Czymmeck N, Reimer R, Trulzsch K, Gaus K, Hohenberg H, et al. β1 integrin-dependent engulfment of Yersinia enterocolitica by macrophages is coupled to the activation of autophagy and suppressed by type III protein secretion. J Immunol 2009; 183: 5847-5860.
34. Choi J-H, Cheong T-C, Ha N-Y, Ko Y, Cho C-H, Jeon J-H, et al. Orientia tsutsugamushi subverts dendritic cell functions by escaping from autophagy and impairing their migration. PLoS Negl Trop Dis 2013; 7(1): e1981.
35. Wang Y, Du J, Wu X, Abdelrehem A, Ren Y, Liu C, et al. Crosstalk between autophagy and microbiota in cancer progression. Mol Cancer 2021; 20: 163.
36. Cho TJ, Wee SW, Woo VH, Choi JI, Kim SJ, Shin HI, et al. Porphyromonas gingivalis-induced autophagy suppresses cell proliferation through G1 arrest in oral cancer cells. Arch Oral Biol 2014; 59: 370-378.
37. Yu T, Guo F, Yu Y, Sun T, Ma D, Han J, et al. Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy. Cell 2017; 170: 548-563. e16.
38. Courtois S, Haykal M, Bodineau C, Sifré E, Azzi-Martin L, Ménard A, et al. Autophagy induced by Helicobacter pylori infection is necessary for gastric cancer stem cell emergence. Gastric Cancer 2021; 24: 133-144.
39. Zhang F, Chen C, Hu J, Su R, Zhang J, Han Z, et al. Molecular mechanism of Helicobacter pylori-induced autophagy in gastric cancer. Oncol Lett 2019; 18: 6221-6227.
40. Halder P, Datta C, Kumar R, Sharma AK, Basu J, Kundu M. The secreted antigen, HP0175, of Helicobacter pylori links the unfolded protein response (UPR) to autophagy in gastric epithelial cells. Cell Microbiol 2015; 17: 714-729.
41. Pareja ME, Colombo MI. Autophagic clearance of bacterial pathogens: molecular recognition of intracellular microorganisms. Front Cell Infect Microbiol 2013; 3: 54.
42. Tanaka S, Nagashima H, Uotani T, Graham DY, Yamaoka Y. Autophagy-related genes in Helicobacter pylori infection. Helicobacter 2017; 22: 10.1111/hel.12376.
43. Wang Y-h, Lv Z-f, Zhong Y, Liu D-s, Chen S-p, Xie Y. The internalization of Helicobacter pylori plays a role in the failure of H. pylori eradication. Helicobacter 2017; 22: 10.1111/hel.12324.
44. Capurro MI, Greenfield LK, Prashar A, Xia S, Abdullah M, Wong H, et al. VacA generates a protective intracellular reservoir for Helicobacter pylori that is eliminated by activation of the lysosomal calcium channel TRPML1. Nat Microbiol 2019; 4: 1411-1423.
45. Xie C, Li N, Wang H, He C, Hu Y, Peng C, et al. Inhibition of autophagy aggravates DNA damage response and gastric tumorigenesis via Rad51 ubiquitination in response to H. pylori infection. Gut Microbes 2020; 11: 1567-1589.
46. Yamaoka Y. Mechanisms of disease: Helicobacter pylori virulence factors. Nat Rev Gastroenterol Hepatol 2010; 7: 629-641.
47. Sadeghloo Z, Nabavi-Rad A, Zali MR, Klionsky DJ, Yadegar A. The interplay between probiotics and host autophagy: mechanisms of action and emerging insights. Autophagy 2025; 21: 260-282.
48. Yang Y, Shu X, Xie C. An overview of autophagy in Helicobacter pylori infection and related gastric cancer. Front Cell Infect Microbiol 2022; 12: 847716.
49. Puissant A, Fenouille N, Auberger P. When autophagy meets cancer through p62/SQSTM1. Am J Cancer Res 2012; 2: 397-413.
50. 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: 203.
51. Li N, Tang B, Jia YP, Zhu P, Zhuang Y, Fang Y, et al. Helicobacter pylori CagA protein negatively regulates autophagy and promotes inflammatory response via c-Met-PI3K/Akt-mTOR signaling pathway. Front Cell Infect Microbiol 2017; 7: 417.
52. Irving AT, Mimuro H, Kufer TA, Lo C, Wheeler R, Turner LJ, et al. The immune receptor NOD1 and kinase RIP2 interact with bacterial peptidoglycan on early endosomes to promote autophagy and inflammatory signaling. Cell Host Microbe 2014; 15: 623-635.
53. Huang X, Wang C, Sun J, Luo J, You J, Liao L, et al. Clinical value of CagA, c-Met, PI3K and Beclin-1 expressed in gastric cancer and their association with prognosis. Oncol Lett 2018; 15: 947-955.
54. Wang RC, Wei Y, An Z, Zou Z, Xiao G, Bhagat G, et al. Akt-mediated regulation of autophagy and tumorigenesis through Beclin 1 phosphorylation. Science 2012; 338: 956-959.
55. Zhu X, Wang Y, Xue W, Wang R, Wang L, Zhu ML, et al. The VEGFR-2 protein and the VEGFR-2 rs1870377 A>T genetic polymorphism are prognostic factors for gastric cancer. Cancer Biol Ther 2019; 20: 497-504.
| Files | ||
| Issue | Vol 17 No 5 (2025) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v17i5.19879 | |
| Keywords | ||
| Autophagy Helicobacter pylori Interleukin-8 Peptic ulcer Gene expression | ||
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How to Cite
1.
Esmaeilzadeh M, Kafilzadeh F, Kargar M, Asadzadeh Aghdaei H, Yadegar A. Helicobacter pylori dysregulates the expression of autophagy-related genes in human gastric adenocarcinoma cell line in vitro. Iran J Microbiol. 2025;17(5):708-717.
