Progress of <i>Helicobacter pylori</i>-related cell apoptosis in mechanisms of gastric carcinogenesis_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

WU Ziyao ^1,2 , MA Jichun ^1,2 , LI Xingliang ^1,2 , PAN Zhiang ³ , ZHU Ciba ⁴ ,  DA Mingxu ^1,2,3

1. The First Clinical Medical College of Lanzhou University, Lanzhou 730000, P. R. China;
2. Lanzhou University, Lanzhou 730000, P. R. China;
3. Department of Oncology Surgery, Gansu Provincial People’s Hospital, Lanzhou 730000, P. R. China;
4. The First Clinical Medical College of Gansu University of Chinese Medicine, Lanzhou 730000, P. R. China;

Corresponding author：

DA Mingxu, Email: hxdamingxu@hotmail.com

Keywords：

gastric cancer; Helicobacter pylori; cell apoptosis

DOI：

10.7507/1007-9424.202309015

Video：

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Objective To understand the mechanisms of gastric carcinogenesis relevant to Helicobacter pylori (H. pylori)-related cell apoptosis and explore potential causes of gastric cancer development through cell apoptosis. Method The literature of recently domestic and international research on the mechanisms of H. pylori-related cell apoptosis in the gastric carcinogenesis was searched and reviewed. Results The H. pylori infection was one of the important risk factors in the occurrence and development of gastric cancer, which was characterized by the imbalance of the interaction between gastric epithelial cells and various cell components in the gastric microenvironment, and which promoted or inhibited the process of apoptosis, and thus interfered with the process of gastric cancer. Conclusions H. pylori, through the regulation of various cellular components and molecular pathways, increases the sensitivity of gastric epithelial cells to apoptosis, actively participates in the progression of gastric cancer. With the advent of the era of precision medicine, research on the mechanisms of H. pylori-related cell apoptosis in gastric carcinogenesis is transitioning to clinical applications, offering promising new treatment strategies for gastric cancer patients.

Citation： WU Ziyao, MA Jichun, LI Xingliang, PAN Zhiang, ZHU Ciba, DA Mingxu. Progress of Helicobacter pylori-related cell apoptosis in mechanisms of gastric carcinogenesis. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2024, 31(1): 98-102. doi: 10.7507/1007-9424.202309015 Copy

1.	Thrift AP, Wenker TN, El-Serag HB. Global burden of gastric cancer: epidemiological trends, risk factors, screening and prevention. Nat Rev Clin Oncol, 2023, 20(5): 338-349.
2.	Allemani C, Matsuda T, Di Carlo V, et al. Global surveillance of trends in cancer survival 2000-14 (CONCORD-3): analysis of individual records for 37 513 025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet, 2018, 391(10125): 1023-1075.
3.	Krzysiek-Maczka G, Brzozowski T, Ptak-Belowska A. Helicobacter pylori-activated fibroblasts as a silent partner in gastric cancer development. Cancer Metastasis Rev, 2023, 42(4): 1219-1256.
4.	Marozzi M, Parnigoni A, Negri A, et al. Inflammation, extracellular matrix remodeling, and proteostasis in tumor microenvironment. Int J Mol Sci, 2021, 22(15): 8102.
5.	Häcker G. The morphology of apoptosis. Cell Tissue Res, 2000, 301(1): 5-17.
6.	Sharma A, Boise LH, Shanmugam M. Cancer metabolism and the evasion of apoptotic cell death. Cancers (Basel), 2019, 11(8): 1144.
7.	Zhong HH, Wang HY, Li J, et al. TRAIL-based gene delivery and therapeutic strategies. Acta Pharmacol Sin, 2019, 40(11): 1373-1385.
8.	Pfeffer CM, Singh ATK. Apoptosis: a target for anticancer therapy. Int J Mol Sci, 2018, 19(2): 448.
9.	Thornberry NA, Lazebnik Y. Caspases: enemies within. Science, 1998, 281(5381): 1312-1316.
10.	Nie S, Yuan Y. The role of gastric mucosal immunity in gastric diseases. J Immunol Res, 2020, 2020: 7927054. doi: 10.1155/2020/7927054.
11.	Liu JF, Guo D, Kang EM, et al. Acute and chronic infection of H. pylori caused the difference in apoptosis of gastric epithelial cells. Microb Pathog, 2021, 150: 104717.
12.	Zuo W, Yang H, Li N, et al. Helicobacter pylori infection activates Wnt/β-catenin pathway to promote the occurrence of gastritis by upregulating ASCL1 and AQP5. Cell Death Discov, 2022, 8(11): 257.
13.	Chaithongyot S, Naumann M. Helicobacter pylori-induced reactive oxygen species direct turnover of CSN-associated STAMBPL1 and augment apoptotic cell death. Cell Mol Life Sci, 2022, 79(2): 86. doi: 10.1007/s00018-022-04135-2.
14.	Palrasu M, Zaika E, El-Rifai W, et al. Role of bacterial and viral pathogens in gastric carcinogenesis. Cancers (Basel), 2021, 13(8): 1878.
15.	Palrasu M, Zaika E, Paulrasu K, et al. Helicobacter pylori pathogen inhibits cellular responses to oncogenic stress and apoptosis. PLoS Pathog, 2022, 18(6): e1010628.
16.	Yao X, Liu D, Zhou L, et al. FAM60A, increased by Helicobacter pylori, promotes proliferation and suppresses apoptosis of gastric cancer cells by targeting the PI3K/AKT pathway. Biochem Biophys Res Commun, 2020, 521(4): 1003-1009.
17.	Dang Y, Zhang Y, Xu L, et al. PUMA-mediated epithelial cell apoptosis promotes Helicobacter pylori infection-mediated gastritis. Cell Death Dis, 2020, 11(2): 139. doi: 10.1038/s41419-020-2339-x.
18.	Maubach G, Lim MCC, Sokolova O, et al. TIFA has dual functions in Helicobacter pylori-induced classical and alternative NF-κB pathways. EMBO Rep, 2021, 22(9): e52878.
19.	Lim MCC, Maubach G, Birkl-Toeglhofer AM, et al. A20 undermines alternative NF-κB activity and expression of anti-apoptotic genes in Helicobacter pylori infection. Cell Mol Life Sci, 2022, 79(2): 102. doi: 10.1007/s00018-022-04139-y.
20.	Park D, Lim JW, Kim H. α-lipoic acid inhibits apoptosis by suppressing the loss of Ku proteins in Helicobacter pylori-infected human gastric epithelial cells. Nutrients, 2022, 14(15): 3206.
21.	Zhao S, Wan D, Zhong Y, et al. 1α, 25-dihydroxyvitamin D3 protects gastric mucosa epithelial cells against Helicobacter pylori-infected apoptosis through a vitamin D receptor-dependent c-Raf/MEK/ERK pathway. Pharm Biol, 2022, 60(1): 801-809.
22.	Zhang J, Ning J, Fu W, et al. CMTM3 protects the gastric epithelial cells from apoptosis and promotes IL-8 by stabilizing NEMO during Helicobacter pylori infection. Gut Pathog, 2023, 15(1): 6. doi: 10.1186/s13099-023-00533-4.
23.	Boccellato F, Woelffling S, Imai-Matsushima A, et al. Polarised epithelial monolayers of the gastric mucosa reveal insights into mucosal homeostasis and defence against infection. Gut, 2019, 68(3): 400-413.
24.	Chen X, Chen W, Zhao Y, et al. Interplay of Helicobacter pylori, fibroblasts, and cancer cells induces fibroblast activation and serpin E1 expression by cancer cells to promote gastric tumorigenesis. J Transl Med, 2022, 20(1): 322. doi:10.1186/s12967-022-03537-x.
25.	Gonciarz W, Krupa A, Hinc K, et al. The effect of Helicobacter pylori infection and different H. pylori components on the proliferation and apoptosis of gastric epithelial cells and fibroblasts. PLoS One, 2019, 14(8): e0220636.
26.	Jantaree P, Bakhchova L, Steinmann U, et al. From 3D back to 2D monolayer stomach organoids-on-a-chip. Trends Biotechnol, 2021, 39(8): 745-748.
27.	Zhang Y, Sun H, Zhao H, et al. Early apoptosis of monocytes induced by Helicobacter pylori infection through multiple pathways. Dev Comp Immunol, 2017, 73: 46-51.
28.	Zhang Y, Sun H, Li J, et al. The leukocyte-associated immunoglobulin (Ig)-like receptor-1 modulating cell apoptosis and inflammatory cytokines secretion in THP-1 cells after Helicobacter pylori infection. Microb Pathog, 2017, 109: 292-299.
29.	张亚辉, 蔡东, 龚建平. 肿瘤相关巨噬细胞与T细胞相互作用对肝细胞性肝癌影响的研究进展. 中国普外基础与临床杂志, 2020, 27(10): 1325-1328.
30.	Tavares R, Pathak SK. Helicobacter pylori secreted protein HP1286 triggers apoptosis in macrophages via TNF-independent and ERK MAPK-dependent pathways. Front Cell Infect Microbiol, 2017, 7: 58. doi: 10.3389/fcimb.2017.00058.
31.	Gerlach BD, Ampomah PB, Yurdagul A, et al. Efferocytosis induces macrophage proliferation to help resolve tissue injury. Cell Metab, 2021, 33(12): 2445-2463.
32.	Oh DY, Fong L, Newell EW, et al. Toward a better understanding of T cells in cancer. Cancer Cell, 2021, 39(12): 1549-1552.
33.	Yi M, Zheng X, Niu M, et al. Combination strategies with PD-1/PD-L1 blockade: current advances and future directions. Mol Cancer, 2022, 21(1): 28. doi: 10.1186/s12943-021-01489-2.
34.	Chiu YM, Tsai CL, Kao JT, et al. PD-1 and PD-L1 up-regulation promotes T-cell apoptosis in gastric adenocarcinoma. Anticancer Res, 2018, 38(4): 2069-2078.
35.	Holokai L, Chakrabarti J, Broda T, et al. Increased programmed death-ligand 1 is an early epithelial cell response to Helicobacter pylori infection. PLoS Pathog, 2019, 15(1): e1007468.
36.	Ferreira DA, Tayyar Y, Idris A, et al. A “hit-and-run” affair—A possible link for cancer progression in virally driven cancers. Biochim Biophys Acta Rev Cancer, 2021, 1875(1): 188476.
37.	Imai S, Ooki T, Murata-Kamiya N, et al. Helicobacter pylori CagA elicits BRCAness to induce genome instability that may underlie bacterial gastric carcinogenesis. Cell Host Microbe, 2021, 29(6): 941-958.
38.	Richardson RB. p53 mutations associated with aging-related rise in cancer incidence rates. Cell Cycle, 2013, 12(15): 2468-2478.
39.	Wroblewski LE, Peek RM. Helicobacter pylori: a stealth assassin. Trends Cancer, 2021, 7(9): 807-808.
40.	Diepstraten ST, Anderson MA, Czabotar PE, et al. The manipulation of apoptosis for cancer therapy using BH3-mimetic drugs. Nat Rev Cancer, 2022, 22(1): 45-64.

1. Thrift AP, Wenker TN, El-Serag HB. Global burden of gastric cancer: epidemiological trends, risk factors, screening and prevention. Nat Rev Clin Oncol, 2023, 20(5): 338-349.
2. Allemani C, Matsuda T, Di Carlo V, et al. Global surveillance of trends in cancer survival 2000-14 (CONCORD-3): analysis of individual records for 37 513 025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet, 2018, 391(10125): 1023-1075.
3. Krzysiek-Maczka G, Brzozowski T, Ptak-Belowska A. Helicobacter pylori-activated fibroblasts as a silent partner in gastric cancer development. Cancer Metastasis Rev, 2023, 42(4): 1219-1256.
4. Marozzi M, Parnigoni A, Negri A, et al. Inflammation, extracellular matrix remodeling, and proteostasis in tumor microenvironment. Int J Mol Sci, 2021, 22(15): 8102.
5. Häcker G. The morphology of apoptosis. Cell Tissue Res, 2000, 301(1): 5-17.
6. Sharma A, Boise LH, Shanmugam M. Cancer metabolism and the evasion of apoptotic cell death. Cancers (Basel), 2019, 11(8): 1144.
7. Zhong HH, Wang HY, Li J, et al. TRAIL-based gene delivery and therapeutic strategies. Acta Pharmacol Sin, 2019, 40(11): 1373-1385.
8. Pfeffer CM, Singh ATK. Apoptosis: a target for anticancer therapy. Int J Mol Sci, 2018, 19(2): 448.
9. Thornberry NA, Lazebnik Y. Caspases: enemies within. Science, 1998, 281(5381): 1312-1316.
10. Nie S, Yuan Y. The role of gastric mucosal immunity in gastric diseases. J Immunol Res, 2020, 2020: 7927054. doi: 10.1155/2020/7927054.
11. Liu JF, Guo D, Kang EM, et al. Acute and chronic infection of H. pylori caused the difference in apoptosis of gastric epithelial cells. Microb Pathog, 2021, 150: 104717.
12. Zuo W, Yang H, Li N, et al. Helicobacter pylori infection activates Wnt/β-catenin pathway to promote the occurrence of gastritis by upregulating ASCL1 and AQP5. Cell Death Discov, 2022, 8(11): 257.
13. Chaithongyot S, Naumann M. Helicobacter pylori-induced reactive oxygen species direct turnover of CSN-associated STAMBPL1 and augment apoptotic cell death. Cell Mol Life Sci, 2022, 79(2): 86. doi: 10.1007/s00018-022-04135-2.
14. Palrasu M, Zaika E, El-Rifai W, et al. Role of bacterial and viral pathogens in gastric carcinogenesis. Cancers (Basel), 2021, 13(8): 1878.
15. Palrasu M, Zaika E, Paulrasu K, et al. Helicobacter pylori pathogen inhibits cellular responses to oncogenic stress and apoptosis. PLoS Pathog, 2022, 18(6): e1010628.
16. Yao X, Liu D, Zhou L, et al. FAM60A, increased by Helicobacter pylori, promotes proliferation and suppresses apoptosis of gastric cancer cells by targeting the PI3K/AKT pathway. Biochem Biophys Res Commun, 2020, 521(4): 1003-1009.
17. Dang Y, Zhang Y, Xu L, et al. PUMA-mediated epithelial cell apoptosis promotes Helicobacter pylori infection-mediated gastritis. Cell Death Dis, 2020, 11(2): 139. doi: 10.1038/s41419-020-2339-x.
18. Maubach G, Lim MCC, Sokolova O, et al. TIFA has dual functions in Helicobacter pylori-induced classical and alternative NF-κB pathways. EMBO Rep, 2021, 22(9): e52878.
19. Lim MCC, Maubach G, Birkl-Toeglhofer AM, et al. A20 undermines alternative NF-κB activity and expression of anti-apoptotic genes in Helicobacter pylori infection. Cell Mol Life Sci, 2022, 79(2): 102. doi: 10.1007/s00018-022-04139-y.
20. Park D, Lim JW, Kim H. α-lipoic acid inhibits apoptosis by suppressing the loss of Ku proteins in Helicobacter pylori-infected human gastric epithelial cells. Nutrients, 2022, 14(15): 3206.
21. Zhao S, Wan D, Zhong Y, et al. 1α, 25-dihydroxyvitamin D3 protects gastric mucosa epithelial cells against Helicobacter pylori-infected apoptosis through a vitamin D receptor-dependent c-Raf/MEK/ERK pathway. Pharm Biol, 2022, 60(1): 801-809.
22. Zhang J, Ning J, Fu W, et al. CMTM3 protects the gastric epithelial cells from apoptosis and promotes IL-8 by stabilizing NEMO during Helicobacter pylori infection. Gut Pathog, 2023, 15(1): 6. doi: 10.1186/s13099-023-00533-4.
23. Boccellato F, Woelffling S, Imai-Matsushima A, et al. Polarised epithelial monolayers of the gastric mucosa reveal insights into mucosal homeostasis and defence against infection. Gut, 2019, 68(3): 400-413.
24. Chen X, Chen W, Zhao Y, et al. Interplay of Helicobacter pylori, fibroblasts, and cancer cells induces fibroblast activation and serpin E1 expression by cancer cells to promote gastric tumorigenesis. J Transl Med, 2022, 20(1): 322. doi:10.1186/s12967-022-03537-x.
25. Gonciarz W, Krupa A, Hinc K, et al. The effect of Helicobacter pylori infection and different H. pylori components on the proliferation and apoptosis of gastric epithelial cells and fibroblasts. PLoS One, 2019, 14(8): e0220636.
26. Jantaree P, Bakhchova L, Steinmann U, et al. From 3D back to 2D monolayer stomach organoids-on-a-chip. Trends Biotechnol, 2021, 39(8): 745-748.
27. Zhang Y, Sun H, Zhao H, et al. Early apoptosis of monocytes induced by Helicobacter pylori infection through multiple pathways. Dev Comp Immunol, 2017, 73: 46-51.
28. Zhang Y, Sun H, Li J, et al. The leukocyte-associated immunoglobulin (Ig)-like receptor-1 modulating cell apoptosis and inflammatory cytokines secretion in THP-1 cells after Helicobacter pylori infection. Microb Pathog, 2017, 109: 292-299.
29. 张亚辉, 蔡东, 龚建平. 肿瘤相关巨噬细胞与T细胞相互作用对肝细胞性肝癌影响的研究进展. 中国普外基础与临床杂志, 2020, 27(10): 1325-1328.
30. Tavares R, Pathak SK. Helicobacter pylori secreted protein HP1286 triggers apoptosis in macrophages via TNF-independent and ERK MAPK-dependent pathways. Front Cell Infect Microbiol, 2017, 7: 58. doi: 10.3389/fcimb.2017.00058.
31. Gerlach BD, Ampomah PB, Yurdagul A, et al. Efferocytosis induces macrophage proliferation to help resolve tissue injury. Cell Metab, 2021, 33(12): 2445-2463.
32. Oh DY, Fong L, Newell EW, et al. Toward a better understanding of T cells in cancer. Cancer Cell, 2021, 39(12): 1549-1552.
33. Yi M, Zheng X, Niu M, et al. Combination strategies with PD-1/PD-L1 blockade: current advances and future directions. Mol Cancer, 2022, 21(1): 28. doi: 10.1186/s12943-021-01489-2.
34. Chiu YM, Tsai CL, Kao JT, et al. PD-1 and PD-L1 up-regulation promotes T-cell apoptosis in gastric adenocarcinoma. Anticancer Res, 2018, 38(4): 2069-2078.
35. Holokai L, Chakrabarti J, Broda T, et al. Increased programmed death-ligand 1 is an early epithelial cell response to Helicobacter pylori infection. PLoS Pathog, 2019, 15(1): e1007468.
36. Ferreira DA, Tayyar Y, Idris A, et al. A “hit-and-run” affair—A possible link for cancer progression in virally driven cancers. Biochim Biophys Acta Rev Cancer, 2021, 1875(1): 188476.
37. Imai S, Ooki T, Murata-Kamiya N, et al. Helicobacter pylori CagA elicits BRCAness to induce genome instability that may underlie bacterial gastric carcinogenesis. Cell Host Microbe, 2021, 29(6): 941-958.
38. Richardson RB. p53 mutations associated with aging-related rise in cancer incidence rates. Cell Cycle, 2013, 12(15): 2468-2478.
39. Wroblewski LE, Peek RM. Helicobacter pylori: a stealth assassin. Trends Cancer, 2021, 7(9): 807-808.
40. Diepstraten ST, Anderson MA, Czabotar PE, et al. The manipulation of apoptosis for cancer therapy using BH3-mimetic drugs. Nat Rev Cancer, 2022, 22(1): 45-64.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Progress of Helicobacter pylori-related cell apoptosis in mechanisms of gastric carcinogenesis

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