Study advances of microorganisms and pathogenic mechanism of pancreatic cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

ZHAO Suyue ¹ ,  ZHU Kexiang ^1,2 , LI Wenjun ¹

1. The First Clinical Medical College, Lanzhou University, Lanzhou 730000, P. R. China;
2. Department of General Surgery, The First Hospital of Lanzhou University, Lanzhou 730000, P. R. China;

Corresponding author：

ZHU Kexiang, Email: flexzhu6910@163.com

Keywords：

pancreatic cancer; oral microorganism; intestinal microbiota; Helicobacter pylori

DOI：

10.7507/1007-9424.201912045

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the recent advances in the pathogenic mechanism of microorganisms and pancreatic cancer.Method Through the retrieval of relevant literatures, the recent progresses in the study of microorganism and pathogenesis of pancreatic cancer were reviewed.Results In recent years, the potential role of intestinal microbiota in the pathogenic mechanism of pancreatic cancer had been studied. The studies found that the microbiome played an important role in the development of pancreatic cancer. Among them, the infections of Helicobacter pylori, oral pathogenic bacteria such as the Porphyromonas ginggivalis, Aggregatibacter actinomycetemcomitans and Phylum fusobacteria, and the changes of composition and diversity of intestinal microflora were closely related to the pancreatic cancer. The microorganisms induced the chronic inflammation and immune response through multiple pathways. The bacterial lipopolysaccharide stimulated the mutations in the KARS gene and mediated the inflammatory response by activating the nuclear factor-κB signaling pathway through Toll like receptor. The oral pathogenic microorganisms and Helicobacter pylori could also promote the cancer progression by secreting toxins that activated cancer-related signaling pathways.Conclusions Bacteria might be important carcinogens. These microorganisms promote development of cancer by causing chronic inflammation, activating cancer-related pathways, activating immune response, oxidative stress, and damaging DNA double strands.

Citation： ZHAO Suyue, ZHU Kexiang, LI Wenjun. Study advances of microorganisms and pathogenic mechanism of pancreatic cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2020, 27(8): 1044-1048. doi: 10.7507/1007-9424.201912045 Copy

1.	吴万龙, 彭兵. 胰腺癌流行病学及危险因素. 中国普外基础与临床杂志, 2019, 26(12): 1500-1503.
2.	Maisonneuve P. Epidemiology and burden of pancreatic cancer. Presse Med, 2019, 48(3 Pt 2): e113-e123.
3.	Zhao CF, Gao F, Li QW, et al. The distributional characteristic and growing trend of pancreatic cancer in China. Pancreas, 2019, 48(3): 309-314.
4.	Rahib L, Smith BD, Aizenberg R, et al. Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res, 2014, 74(11): 2913-2921.
5.	Pang YJ, Holmes MV, Chen ZM, et al. A review of lifestyle, metabolic risk factors, and blood-based biomarkers for early diagnosis of pancreatic ductal adenocarcinoma. J Gastroenterol Hepatol, 2019, 34(2): 330-345.
6.	Wei MY, Shi S, Liang C, et al. The microbiota and microbiome in pancreatic cancer: more influential than expected. Mol Cancer, 2019, 18(1): 97.
7.	Gordon-Dseagu VL, Devesa SS, Goggins M, et al. Pancreatic cancer incidence trends: evidence from the Surveillance, Epidemiology and End Results (SEER) population-based data. Int J Epidemiol, 2018, 47(2): 427-439.
8.	Nagano T, Otoshi T, Hazama D, et al. Novel cancer therapy targeting microbiome. Onco Targets Ther, 2019, 12: 3619-3624.
9.	Cani PD, Jordan BF. Gut microbiota-mediated inflammation in obesity: a link with gastrointestinal cancer. Nat Rev Gastroenterol Hepatol, 2018, 15(11): 671-682.
10.	Meng C, Bai C, Brown TD, et al. Human gut microbiota and gastrointestinal cancer. Genomics Proteomics Bioinformatics, 2018, 16(1): 33-49.
11.	Karpiński TM. The microbiota and pancreatic cancer. Gastroenterol Clin North Am, 2019, 48(3): 447-464.
12.	Miller DP, Wang Q, Weinberg A, et al. Transcriptome analysis of Porphyromonas gingivalis and Acinetobacter baumannii in polymicrobial communities. Mol Oral Microbiol, 2018, 33(5): 364-377.
13.	Karpinski TM. Role of oral microbiota in cancer development. Microorganisms, 2019, 7(1): 1-14.
14.	Fan X, Alekseyenko AV, Wu J, et al. Human oral microbiome and prospective risk for pancreatic cancer: a population-based nested case-control study. Gut, 2018, 67(1): 120-127.
15.	Damgaard C, Danielsen AK, Enevold C2, et al. Porphyromonas gingivalis in saliva associates with chronic and aggressive periodontitis. J Oral Microbiol, 2019, 11(1): 1653123.
16.	Lee J, Roberts JS, Atanasova KR, et al. A novel kinase function of a nucleoside-diphosphate-kinase homologue in Porphyromonas gingivalis is critical in subversion of host cell apoptosis by targeting heat-shock protein 27. Cell Microbiol, 2018, 20(5): e12825.
17.	Olsen I, Yilmaz Ö. Possible role of Porphyromonas gingivalis in orodigestive cancers. J Oral Microbiol, 2019, 11(1): 1563410.
18.	Binder Gallimidi A, Fischman S, Revach B, et al. Periodontal pathogens Porphyromonas gingivalis and Fusobacterium nucleatum promote tumor progression in an oral-specific chemical carcinogenesis model. Oncotarget, 2015, 6(26): 22613-22623.
19.	Carmi Y, Dotan S, Rider P, et al. The role of IL-1β in the early tumor cell-induced angiogenic response. J Immunol, 2013, 190(7): 3500-3509.
20.	Mao S, Park Y, Hasegawa Y, et al. Intrinsic apoptotic pathways of gingival epithelial cells modulated by Porphyromonas gingivalis. Cell Microbiol, 2007, 9(8): 1997-2007.
21.	Yao L, Jermanus C, Barbetta B, et al. Porphyromonas gingivalis infection sequesters pro-apoptotic Bad through Akt in primary gingival epithelial cells. Mol Oral Microbiol, 2010, 25(2): 89-101.
22.	Inaba H, Sugita H, Kuboniwa M, et al. Porphyromonas gingivalis promotes invasion of oral squamous cell carcinoma through induction of proMMP9 and its activation. Cell Microbiol, 2014, 16(1): 131-145.
23.	Obradović D, Gašperšič R, Caserman S, et al. A cytolethal distending toxin variant from Aggregatibacter actinomycetemcomitans with an aberrant CdtB that lacks the conserved catalytic histidine 160. PLoS One, 2016, 11(7): e0159231.
24.	Teng YT, Zhang X. Apoptotic activity and sub-cellular localization of a T4SS-associated CagE-homologue in Actinobacillus actinomycetemcomitans. Microb Pathog, 2005, 38(2-3): 125-132.
25.	Rubinstein MR, Wang X, Liu W, et al. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe, 2013, 14(2): 195-206.
26.	Fardini Y, Wang X, Témoin S, et al. Fusobacterium nucleatum adhesin FadA binds vascular endothelial cadherin and alters endothelial integrity. Mol Microbiol, 2011, 82(6): 1468-1480.
27.	Manson McGuire A, Cochrane K, Griggs AD, et al. Evolution of invasion in a diverse set of Fusobacterium species. mBio, 2014, 5(6): e01864.
28.	Park SR, Kim DJ, Han SH, et al. Diverse Toll-like receptors mediate cytokine production by Fusobacterium nucleatum and Aggregatibacter actinomycetemcomitans in macrophages. Infect Immun, 2014, 82(5): 1914-1920.
29.	Yang Y, Weng W, Peng J, et al. Fusobacterium nucleatum increases proliferation of colorectal cancer cells and tumor development in mice by activating Toll-like receptor 4 signaling to nuclear factor-κB, and up-regulating expression of microRNA-21. Gastroenterology, 2017, 152(4): 851-866.
30.	Uitto VJ, Baillie D, Wu Q, et al. Fusobacterium nucleatum increases collagenase 3 production and migration of epithelial cells. Infect Immun, 2005, 73(2): 1171-1179.
31.	Mitsuhashi K, Nosho K, Sukawa Y, et al. Association of Fusobacterium species in pancreatic cancer tissues with molecular features and prognosis. Oncotarget, 2015, 6(9): 7209-7220.
32.	Grimmig T, Moench R, Kreckel J, et al. Toll like receptor 2, 4, and 9 signaling promotes autoregulative tumor cell growth and VEGF/PDGF expression in human pancreatic cancer. Int J Mol Sci, 2016, 17(12). pii: E2060. PMID: 27941651.
33.	Jiaqi H, Ulrika Z, Göran H, et al. Helicobacter pylori infection, chronic corpus atrophic gastritis and pancreatic cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort: A nested case-control study. Int J Cancer, 2017, 140(8): 1727-1735.
34.	Lin SH, He YT, Lan TT. Su2010 the association between peptic ulcer with or without Helicobacter pylori infection and colorectal cancer—A population-based matched case-control study in Taiwan. Gastroenterology, 2015, 148(4): S-574.
35.	Chen XZ, Wang R, Chen HN, et al. Cytotoxin-associated gene A-negative strains of Helicobacter pylori as a potential risk factor of pancreatic cancer: A meta-analysis based on nested case-control studies. Pancreas, 2015, 44(8): 1340-13444.
36.	Hirabayashi M, Inoue M, Sawada N, et al. Helicobacter pylori infection, atrophic gastritis, and risk of pancreatic cancer: A population-based cohort study in a large Japanese population: the JPHC Study. Sci Rep, 2019, 9(1): 6099.
37.	Mei QX, Huang CL, Luo SZ, et al. Characterization of the duodenal bacterial microbiota in patients with pancreatic head cancer vs. healthy controls. Pancreatology, 2018, 18(4): 438-445.
38.	Knorr J, Ricci V, Hatakeyama M, et al. Classification of Helicobacter pylori virulence factors: Is CagA a toxin or not? Trends Microbiol, 2019, 27(9): 731-738.
39.	Stein M, Bagnoli F, Halenbeck R, et al. c-Src/Lyn kinases activate Helicobacter pylori CagA through tyrosine phosphorylation of the EPIYA motifs. Mol Microbiol, 2002, 43(4): 971-980.
40.	Rabelo-Gonçalves EM, Roesler BM, Zeitune JM. Extragastric manifestations of Helicobacter pylori infection: Possible role of bacterium in liver and pancreas diseases. World J Hepatol, 2015, 7(30): 2968-2979.
41.	Ramos-Alvarez I, Lee L, Jensen RT. Cyclic AMP-dependent protein kinase A and EPAC mediate VIP and secretin stimulation of PAK4 and activation of Na⁺, K⁺-ATPase in pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol, 2019, 316(2): G263-G277.
42.	Nagy TA, Frey MR, Yan F, et al. Helicobacter pylori regulates cellular migration and apoptosis by activation of phosphatidylinositol 3-kinase signaling. J Infect Dis, 2009, 199(5): 641-651.
43.	Smith MF Jr, Novotny J, Carl VS, et al. Helicobacter pylori and toll-like receptor agonists induce syndecan-4 expression in an NF-kappaB-dependent manner. Glycobiology, 2006, 16(3): 221-229.
44.	Lesina M, Kurkowski MU, Ludes K, et al. Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer. Cancer Cell, 2011, 19(4): 456-469.
45.	Pushalkar S, Hundeyin M, Daley D, et al. The pancreatic cancer microbiome promotes oncogenesis by induction of innate and adaptive immune suppression. Cancer Discov, 2018, 8(4): 403-416.
46.	Mendez R, Kesh K, Arora N, et al. Microbial dysbiosis and polyamine metabolism as predictive markers for early detection of pancreatic cancer. Carcinogenesis, 2019 Aug 1. pii: bgz116.
47.	Ren Z, Jiang J, Xie H, et al. Gut microbial profile analysis by MiSeq sequencing of pancreatic carcinoma patients in China. Oncotarget, 2017, 8(56): 95176-95191.
48.	Pagliari D, Saviano A, Newton EE, et al. Gut microbiota—immune system crosstalk and pancreatic disorders. Mediators Inflamm, 2018, 2018: 7946431.
49.	Francescone R, Hou V, Grivennikov SI. Microbiome, inflammation, and cancer. Cancer J, 2014, 20(3): 181-189.
50.	Ahuja M, Schwartz DM, Tandon M, et al. Orai1-mediated antimicrobial secretion from pancreatic acini shapes the gut microbiome and regulates gut innate immunity. Cell Metab, 2017, 25(3): 635-646.
51.	Capurso G, Signoretti M, Archibugi L, et al. Systematic review and meta-analysis: Small intestinal bacterial overgrowth in chronic pancreatitis. United European Gastroenterol J, 2016, 4(5): 697-705.
52.	Huang H, Daniluk J, Liu Y, et al. Oncogenic K-Ras requires activation for enhanced activity. Oncogene, 2014, 33(4): 532-535.
53.	Han JL, Lin HL. Intestinal microbiota and type 2 diabetes: from mechanism insights to therapeutic perspective. World J Gastroenterol, 2014, 20(47): 17737-17745.
54.	Riquelme E, Zhang Y, Zhang L, et al. Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell, 2019, 178(4): 795-806.
55.	Sivan A, Corrales L, Hubert N, et al. Commensal bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science, 2015, 350(6264): 1084-1089.
56.	Serna-Thomé G, Castro-Eguiluz D, Fuchs-Tarlovsky V, et al. Use of functional foods and oral supplements as adjuvants in cancer treatment. Rev Invest Clin, 2018, 70(3): 136-146.

1. 吴万龙, 彭兵. 胰腺癌流行病学及危险因素. 中国普外基础与临床杂志, 2019, 26(12): 1500-1503.
2. Maisonneuve P. Epidemiology and burden of pancreatic cancer. Presse Med, 2019, 48(3 Pt 2): e113-e123.
3. Zhao CF, Gao F, Li QW, et al. The distributional characteristic and growing trend of pancreatic cancer in China. Pancreas, 2019, 48(3): 309-314.
4. Rahib L, Smith BD, Aizenberg R, et al. Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res, 2014, 74(11): 2913-2921.
5. Pang YJ, Holmes MV, Chen ZM, et al. A review of lifestyle, metabolic risk factors, and blood-based biomarkers for early diagnosis of pancreatic ductal adenocarcinoma. J Gastroenterol Hepatol, 2019, 34(2): 330-345.
6. Wei MY, Shi S, Liang C, et al. The microbiota and microbiome in pancreatic cancer: more influential than expected. Mol Cancer, 2019, 18(1): 97.
7. Gordon-Dseagu VL, Devesa SS, Goggins M, et al. Pancreatic cancer incidence trends: evidence from the Surveillance, Epidemiology and End Results (SEER) population-based data. Int J Epidemiol, 2018, 47(2): 427-439.
8. Nagano T, Otoshi T, Hazama D, et al. Novel cancer therapy targeting microbiome. Onco Targets Ther, 2019, 12: 3619-3624.
9. Cani PD, Jordan BF. Gut microbiota-mediated inflammation in obesity: a link with gastrointestinal cancer. Nat Rev Gastroenterol Hepatol, 2018, 15(11): 671-682.
10. Meng C, Bai C, Brown TD, et al. Human gut microbiota and gastrointestinal cancer. Genomics Proteomics Bioinformatics, 2018, 16(1): 33-49.
11. Karpiński TM. The microbiota and pancreatic cancer. Gastroenterol Clin North Am, 2019, 48(3): 447-464.
12. Miller DP, Wang Q, Weinberg A, et al. Transcriptome analysis of Porphyromonas gingivalis and Acinetobacter baumannii in polymicrobial communities. Mol Oral Microbiol, 2018, 33(5): 364-377.
13. Karpinski TM. Role of oral microbiota in cancer development. Microorganisms, 2019, 7(1): 1-14.
14. Fan X, Alekseyenko AV, Wu J, et al. Human oral microbiome and prospective risk for pancreatic cancer: a population-based nested case-control study. Gut, 2018, 67(1): 120-127.
15. Damgaard C, Danielsen AK, Enevold C2, et al. Porphyromonas gingivalis in saliva associates with chronic and aggressive periodontitis. J Oral Microbiol, 2019, 11(1): 1653123.
16. Lee J, Roberts JS, Atanasova KR, et al. A novel kinase function of a nucleoside-diphosphate-kinase homologue in Porphyromonas gingivalis is critical in subversion of host cell apoptosis by targeting heat-shock protein 27. Cell Microbiol, 2018, 20(5): e12825.
17. Olsen I, Yilmaz Ö. Possible role of Porphyromonas gingivalis in orodigestive cancers. J Oral Microbiol, 2019, 11(1): 1563410.
18. Binder Gallimidi A, Fischman S, Revach B, et al. Periodontal pathogens Porphyromonas gingivalis and Fusobacterium nucleatum promote tumor progression in an oral-specific chemical carcinogenesis model. Oncotarget, 2015, 6(26): 22613-22623.
19. Carmi Y, Dotan S, Rider P, et al. The role of IL-1β in the early tumor cell-induced angiogenic response. J Immunol, 2013, 190(7): 3500-3509.
20. Mao S, Park Y, Hasegawa Y, et al. Intrinsic apoptotic pathways of gingival epithelial cells modulated by Porphyromonas gingivalis. Cell Microbiol, 2007, 9(8): 1997-2007.
21. Yao L, Jermanus C, Barbetta B, et al. Porphyromonas gingivalis infection sequesters pro-apoptotic Bad through Akt in primary gingival epithelial cells. Mol Oral Microbiol, 2010, 25(2): 89-101.
22. Inaba H, Sugita H, Kuboniwa M, et al. Porphyromonas gingivalis promotes invasion of oral squamous cell carcinoma through induction of proMMP9 and its activation. Cell Microbiol, 2014, 16(1): 131-145.
23. Obradović D, Gašperšič R, Caserman S, et al. A cytolethal distending toxin variant from Aggregatibacter actinomycetemcomitans with an aberrant CdtB that lacks the conserved catalytic histidine 160. PLoS One, 2016, 11(7): e0159231.
24. Teng YT, Zhang X. Apoptotic activity and sub-cellular localization of a T4SS-associated CagE-homologue in Actinobacillus actinomycetemcomitans. Microb Pathog, 2005, 38(2-3): 125-132.
25. Rubinstein MR, Wang X, Liu W, et al. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe, 2013, 14(2): 195-206.
26. Fardini Y, Wang X, Témoin S, et al. Fusobacterium nucleatum adhesin FadA binds vascular endothelial cadherin and alters endothelial integrity. Mol Microbiol, 2011, 82(6): 1468-1480.
27. Manson McGuire A, Cochrane K, Griggs AD, et al. Evolution of invasion in a diverse set of Fusobacterium species. mBio, 2014, 5(6): e01864.
28. Park SR, Kim DJ, Han SH, et al. Diverse Toll-like receptors mediate cytokine production by Fusobacterium nucleatum and Aggregatibacter actinomycetemcomitans in macrophages. Infect Immun, 2014, 82(5): 1914-1920.
29. Yang Y, Weng W, Peng J, et al. Fusobacterium nucleatum increases proliferation of colorectal cancer cells and tumor development in mice by activating Toll-like receptor 4 signaling to nuclear factor-κB, and up-regulating expression of microRNA-21. Gastroenterology, 2017, 152(4): 851-866.
30. Uitto VJ, Baillie D, Wu Q, et al. Fusobacterium nucleatum increases collagenase 3 production and migration of epithelial cells. Infect Immun, 2005, 73(2): 1171-1179.
31. Mitsuhashi K, Nosho K, Sukawa Y, et al. Association of Fusobacterium species in pancreatic cancer tissues with molecular features and prognosis. Oncotarget, 2015, 6(9): 7209-7220.
32. Grimmig T, Moench R, Kreckel J, et al. Toll like receptor 2, 4, and 9 signaling promotes autoregulative tumor cell growth and VEGF/PDGF expression in human pancreatic cancer. Int J Mol Sci, 2016, 17(12). pii: E2060. PMID: 27941651.
33. Jiaqi H, Ulrika Z, Göran H, et al. Helicobacter pylori infection, chronic corpus atrophic gastritis and pancreatic cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort: A nested case-control study. Int J Cancer, 2017, 140(8): 1727-1735.
34. Lin SH, He YT, Lan TT. Su2010 the association between peptic ulcer with or without Helicobacter pylori infection and colorectal cancer—A population-based matched case-control study in Taiwan. Gastroenterology, 2015, 148(4): S-574.
35. Chen XZ, Wang R, Chen HN, et al. Cytotoxin-associated gene A-negative strains of Helicobacter pylori as a potential risk factor of pancreatic cancer: A meta-analysis based on nested case-control studies. Pancreas, 2015, 44(8): 1340-13444.
36. Hirabayashi M, Inoue M, Sawada N, et al. Helicobacter pylori infection, atrophic gastritis, and risk of pancreatic cancer: A population-based cohort study in a large Japanese population: the JPHC Study. Sci Rep, 2019, 9(1): 6099.
37. Mei QX, Huang CL, Luo SZ, et al. Characterization of the duodenal bacterial microbiota in patients with pancreatic head cancer vs. healthy controls. Pancreatology, 2018, 18(4): 438-445.
38. Knorr J, Ricci V, Hatakeyama M, et al. Classification of Helicobacter pylori virulence factors: Is CagA a toxin or not? Trends Microbiol, 2019, 27(9): 731-738.
39. Stein M, Bagnoli F, Halenbeck R, et al. c-Src/Lyn kinases activate Helicobacter pylori CagA through tyrosine phosphorylation of the EPIYA motifs. Mol Microbiol, 2002, 43(4): 971-980.
40. Rabelo-Gonçalves EM, Roesler BM, Zeitune JM. Extragastric manifestations of Helicobacter pylori infection: Possible role of bacterium in liver and pancreas diseases. World J Hepatol, 2015, 7(30): 2968-2979.
41. Ramos-Alvarez I, Lee L, Jensen RT. Cyclic AMP-dependent protein kinase A and EPAC mediate VIP and secretin stimulation of PAK4 and activation of Na⁺, K⁺-ATPase in pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol, 2019, 316(2): G263-G277.
42. Nagy TA, Frey MR, Yan F, et al. Helicobacter pylori regulates cellular migration and apoptosis by activation of phosphatidylinositol 3-kinase signaling. J Infect Dis, 2009, 199(5): 641-651.
43. Smith MF Jr, Novotny J, Carl VS, et al. Helicobacter pylori and toll-like receptor agonists induce syndecan-4 expression in an NF-kappaB-dependent manner. Glycobiology, 2006, 16(3): 221-229.
44. Lesina M, Kurkowski MU, Ludes K, et al. Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer. Cancer Cell, 2011, 19(4): 456-469.
45. Pushalkar S, Hundeyin M, Daley D, et al. The pancreatic cancer microbiome promotes oncogenesis by induction of innate and adaptive immune suppression. Cancer Discov, 2018, 8(4): 403-416.
46. Mendez R, Kesh K, Arora N, et al. Microbial dysbiosis and polyamine metabolism as predictive markers for early detection of pancreatic cancer. Carcinogenesis, 2019 Aug 1. pii: bgz116.
47. Ren Z, Jiang J, Xie H, et al. Gut microbial profile analysis by MiSeq sequencing of pancreatic carcinoma patients in China. Oncotarget, 2017, 8(56): 95176-95191.
48. Pagliari D, Saviano A, Newton EE, et al. Gut microbiota—immune system crosstalk and pancreatic disorders. Mediators Inflamm, 2018, 2018: 7946431.
49. Francescone R, Hou V, Grivennikov SI. Microbiome, inflammation, and cancer. Cancer J, 2014, 20(3): 181-189.
50. Ahuja M, Schwartz DM, Tandon M, et al. Orai1-mediated antimicrobial secretion from pancreatic acini shapes the gut microbiome and regulates gut innate immunity. Cell Metab, 2017, 25(3): 635-646.
51. Capurso G, Signoretti M, Archibugi L, et al. Systematic review and meta-analysis: Small intestinal bacterial overgrowth in chronic pancreatitis. United European Gastroenterol J, 2016, 4(5): 697-705.
52. Huang H, Daniluk J, Liu Y, et al. Oncogenic K-Ras requires activation for enhanced activity. Oncogene, 2014, 33(4): 532-535.
53. Han JL, Lin HL. Intestinal microbiota and type 2 diabetes: from mechanism insights to therapeutic perspective. World J Gastroenterol, 2014, 20(47): 17737-17745.
54. Riquelme E, Zhang Y, Zhang L, et al. Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell, 2019, 178(4): 795-806.
55. Sivan A, Corrales L, Hubert N, et al. Commensal bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science, 2015, 350(6264): 1084-1089.
56. Serna-Thomé G, Castro-Eguiluz D, Fuchs-Tarlovsky V, et al. Use of functional foods and oral supplements as adjuvants in cancer treatment. Rev Invest Clin, 2018, 70(3): 136-146.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Study advances of microorganisms and pathogenic mechanism of pancreatic cancer

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