From microbiota toward gastro-enteropancreatic neuroendocrine neoplasms: Are we on the highway to hell?

Cytokines Inflammation Microbiota Neuroendocrine tumors Tumor microenvironment

Journal

Reviews in endocrine & metabolic disorders
ISSN: 1573-2606
Titre abrégé: Rev Endocr Metab Disord
Pays: Germany
ID NLM: 100940588

Informations de publication

Date de publication:
09 2021
Historique:
accepted: 04 09 2020
pubmed: 17 9 2020
medline: 15 12 2021
entrez: 16 9 2020
Statut: ppublish

Résumé

Gut microbiota is represented by different microorganisms that colonize the intestinal tract, mostly the large intestine, such as bacteria, fungi, archaea and viruses. The gut microbial balance has a key role in several functions. It modulates the host's metabolism, maintains the gut barrier integrity, participates in the xenobiotics and drug metabolism, and acts as protection against gastro-intestinal pathogens through the host's immune system modulation. The impaired gut microbiota, called dysbiosis, may be the result of an imbalance in this equilibrium and is linked with different diseases, including cancer. While most of the studies have focused on the association between microbiota and gastrointestinal adenocarcinomas, very little is known about gastroenteropancreatic (GEP) neuroendocrine neoplasms (NENs). In this review, we provide an overview concerning the complex interplay between gut microbiota and GEP NENs, focusing on the potential role in tumorigenesis and progression in these tumors.

Identifiants

pubmed: 32935263
doi: 10.1007/s11154-020-09589-y
pii: 10.1007/s11154-020-09589-y
pmc: PMC8346435
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

511-525

Informations de copyright

© 2020. The Author(s).

Références

Muscogiuri G, Balercia G, Barrea L, Cignarelli A, Giorgino F, Holst JJ, et al. Gut: a key player in the pathogenesis of type 2 diabetes? Crit Rev Food Sci Nutr. 2018;24:1294–309.
Barrea L, Muscogiuri G, Annunziata G, Laudisio D, Pugliese G, Salzano C, et al. From gut microbiota dysfunction to obesity: could short-chain fatty acids stop this dangerous course? Hormones (Athens). 2019;18:245–50.
Zhang YL, Li S, Gan RY, Zhou T, Xu DP, Li HB. Impacts of gut bacteria on human health and diseases. Int J Mol Sci. 2015;4:7493–519.
doi: 10.3390/ijms16047493
Feng Q, Chen WD, Wang YD. Gut microbiota: an integral moderator in health and disease. Front Microbiol. 2018;9:151.
pubmed: 29515527 pmcid: 5826318 doi: 10.3389/fmicb.2018.00151
Kong F, Cai Y. Study insights into gastrointestinal cancer through the gut microbiota. Biomed Res Int. 2019;3:1–8.
Lynch SV, Pedersen O. The human intestinal microbiome in health and disease. N Engl J Med. 2016;375:2369–79.
pubmed: 27974040 doi: 10.1056/NEJMra1600266
Greenhalgh K, Meyer KM, Aagaard KM, Wilmes P. The human gut microbiome in health: establishment and resilience of microbiota over a lifetime. Environ Microbiol. 2016;18:2103–16.
pubmed: 27059297 pmcid: 7387106 doi: 10.1111/1462-2920.13318
Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M, Strauss J, et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 2012;22:299–306.
Raza MH, Gul K, Arshad A, Riaz N, Waheed U, Rauf A, et al. Microbiota in cancer development and treatment. J Cancer Res Clin Oncol. 2019;145:49–63.
pubmed: 30542789 doi: 10.1007/s00432-018-2816-0
Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science. 2015;350:1084–9.
pubmed: 26541606 pmcid: 4873287 doi: 10.1126/science.aac4255
Schmidt TSB, Raes J, Bork P. The human gut microbiome: from association to modulation. Cell. 2018;172:1198–215.
pubmed: 29522742 doi: 10.1016/j.cell.2018.02.044
Cani PD. Human gut microbiome: hopes, threats and promises. Gut. 2018;67:1716–25.
pubmed: 29934437 doi: 10.1136/gutjnl-2018-316723
Vivarelli S, Salemi R, Candido S, Falzone L, Santagati M, Stefani S, et al. Gut microbiota and cancer: from pathogenesis to therapy. Cancers (Basel). 2019;11:38.
doi: 10.3390/cancers11010038
Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ. Dysbiosis of the gut microbiota in disease. Microb Ecol Health Dis. 2015;26:26191.
pubmed: 25651997
Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science. 2015;348:69–74.
pubmed: 25838375 doi: 10.1126/science.aaa4971
Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell. 2012;21:309–22.
pubmed: 22439926 doi: 10.1016/j.ccr.2012.02.022
Joyce JA, Fearon DT. T cell exclusion, immune privilege, and the tumor microenvironment. Science. 2015;348:74–80.
pubmed: 25838376 doi: 10.1126/science.aaa6204
Guerra L, Guidi R, Frisan T. Do bacterial genotoxins contribute to chronic inflammation, genomic instability and tumor progression? FEBS J. 2011;278:4577–88.
pubmed: 21585655 doi: 10.1111/j.1742-4658.2011.08125.x
Hekmatshoar Y, Rahbar Saadat Y, Hosseiniyan Khatibi SM, Ozkan T, Zununi Vahed F, Nariman-Saleh-Fam Z, et al. The impact of tumor and gut microbiotas on cancer therapy: beneficial or detrimental? Life Sci. 2019;233:116680.
pubmed: 31344431 doi: 10.1016/j.lfs.2019.116680
Nougayrède JP, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, et al. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science. 2006;313:848–51.
pubmed: 16902142 doi: 10.1126/science.1127059
Putze J, Hennequin C, Nougayrède JP, Zhang W, Homburg S, Karch H, et al. Genetic structure and distribution of the colibactin genomic island among members of the family Enterobacteriaceae. Infect Immun. 2009;77:4696–703.
pubmed: 19720753 pmcid: 2772509 doi: 10.1128/IAI.00522-09
Arthur JC, Gharaibeh RZ, Mühlbauer M, Perez-Chanona E, Uronis JM, McCafferty J, et al. Microbial genomic analysis reveals the essential role of inflammation in bacteria-induced colorectal cancer. Nat Commun. 2014;5:4724.
pubmed: 25182170 doi: 10.1038/ncomms5724
Arthur JC, Perez-Chanona E, Mühlbauer M, Tomkovich S, Uronis JM, Fan TJ, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science. 2012;338:120–3.
pubmed: 22903521 pmcid: 3645302 doi: 10.1126/science.1224820
Goodwin AC, Destefano Shields CE, Wu S, Huso DL, Wu X, Murray-Stewart TR, et al. Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci U S A. 2011;108:15354–9.
pubmed: 21876161 pmcid: 3174648 doi: 10.1073/pnas.1010203108
Clevers H, Nusse R. Wnt/β-catenin signaling and disease. Cell. 2012;149:1192–205.
pubmed: 22682243 doi: 10.1016/j.cell.2012.05.012
Nusse R, Clevers H. Wnt/β-catenin signaling, disease, and emerging therapeutic modalities. Cell. 2017;169:985–99.
pubmed: 28575679 doi: 10.1016/j.cell.2017.05.016
Loh KM, van Amerongen R, Nusse R. Generating cellular diversity and spatial form: Wnt signaling and the evolution of multicellular animals. Dev Cell. 2016;38:643–55.
pubmed: 27676437 doi: 10.1016/j.devcel.2016.08.011
Holstein TW. The evolution of the Wnt pathway. Cold Spring Harb Perspect Biol. 2012;4:a007922.
pubmed: 22751150 pmcid: 3385961 doi: 10.1101/cshperspect.a007922
Kretzschmar K, Clevers H. Wnt/β-catenin signaling in adult mammalian epithelial stem cells. Dev Biol. 2017;428:273–82.
pubmed: 28526587 doi: 10.1016/j.ydbio.2017.05.015
Majidinia M, Aghazadeh J, Jahanban-Esfahlani R, Yousefi B. The roles of Wnt/β-catenin pathway in tissue development and regenerative medicine. J Cell Physiol. 2018;233:5598–612.
pubmed: 29150936 doi: 10.1002/jcp.26265
Krausova M, Korinek V. Wnt signaling in adult intestinal stem cells and cancer. Cell Signal. 2014;26:570–9.
pubmed: 24308963 doi: 10.1016/j.cellsig.2013.11.032
Lu R, Liu X, Wu S, Xia Y, Zhang YG, Petrof EO, et al. Consistent activation of the β-catenin pathway by Salmonella type-three secretion effector protein AvrA in chronically infected intestine. Am J Physiol Gastrointest Liver Physiol. 2012;303:G1113–25.
pubmed: 22982337 pmcid: 3517655 doi: 10.1152/ajpgi.00453.2011
Panebianco C, Andriulli A, Pazienza V. Pharmacomicrobiomics: exploiting the drug-microbiota interactions in anticancer therapies. Microbiome. 2018;6:92.
pubmed: 29789015 pmcid: 5964925 doi: 10.1186/s40168-018-0483-7
Zitvogel L, Galluzzi L, Viaud S, Vétizou M, Daillère R, Merad M, et al. Cancer and the gut microbiota: an unexpected link. Sci Transl Med. 2015;7(271):271ps1.
Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science. 2012;336:1268–73.
pubmed: 22674334 pmcid: 4420145 doi: 10.1126/science.1223490
Liu Y, Baba Y, Ishimoto T, Iwatsuki M, Hiyoshi Y, Miyamoto Y, et al. Progress in characterizing the linkage between Fusobacterium nucleatum and gastrointestinal cancer. J Gastroenterol. 2019;54:33–41.
Panebianco C, Potenza A, Andriulli A, Pazienza V. Exploring the microbiota to better understand gastrointestinal cancers physiology. Clin Chem Lab Med. 2018;56(9):1400–12.
pubmed: 29630505 doi: 10.1515/cclm-2017-1163
Rea D, Coppola G, Palma G, Barbieri A, Luciano A, Del Prete P, et al. Microbiota effects on cancer: from risks to therapies. Oncotarget. 2018;9:17915–27.
Wong SH, Kwong TNY, Wu CY, Yu J. Clinical applications of gut microbiota in cancer biology. Semin Cancer Biol. 2019;55:28–36.
pubmed: 29782923 doi: 10.1016/j.semcancer.2018.05.003
Panebianco C, Adamberg K, Jaagura M, Copetti M, Fontana A, Adamberg S, et al. Influence of gemcitabine chemotherapy on the microbiota of pancreatic cancer xenografted mice. Cancer Chemother Pharmacol. 2018;81:773–82.
pubmed: 29473096 doi: 10.1007/s00280-018-3549-0
DiDonato JA, Mercurio F, Karin M. NF-κB and the link between inflammation and cancer. Immunol Rev. 2012;246:379–400.
pubmed: 22435567 doi: 10.1111/j.1600-065X.2012.01099.x
Grivennikov SI, Wang K, Mucida D, Stewart CA, Schnabl B, Jauch D, et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature. 2012;491:254–8.
pubmed: 23034650 pmcid: 3601659 doi: 10.1038/nature11465
Schwabe RF, Jobin C. The microbiome and cancer. Nat Rev Cancer. 2013;13:800–12.
pubmed: 24132111 pmcid: 3986062 doi: 10.1038/nrc3610
Elinav E, Nowarski R, Thaiss CA, Hu B, Jin C, Flavell RA. Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms. Nat Rev Cancer. 2013;13:759–71.
pubmed: 24154716 doi: 10.1038/nrc3611
Grivennikov SI, Karin M. Inflammatory cytokines in cancer: tumour necrosis factor and interleukin 6 take the stage. Ann Rheum Dis. 2011;70:i104–8.
pubmed: 21339211 doi: 10.1136/ard.2010.140145
Grivennikov SI. IL-11: a prominent pro-tumorigenic member of the IL-6 family. Cancer Cell. 2013;24:145–7.
pubmed: 23948295 doi: 10.1016/j.ccr.2013.07.018
Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer. 2009;9:798–809.
pubmed: 19851315 pmcid: 4856025 doi: 10.1038/nrc2734
Li N, Grivennikov SI, Karin M. The unholy trinity: inflammation, cytokines, and STAT3 shape the cancer microenvironment. Cancer Cell. 2011;19:429–31.
pubmed: 21481782 pmcid: 3111086 doi: 10.1016/j.ccr.2011.03.018
Valenzano M, Bisio A, Grassi G. Helicobacter pylori and diabetes mellitus: a controversial relationship. Minerva Endocrinol. 2019;44:301–9.
pubmed: 31304727 doi: 10.23736/S0391-1977.19.03021-9
Warren JR, Marshall B. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet. 1983;1:1273–5.
pubmed: 6134060
Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, et al. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med. 1991;325:1127–31.
pubmed: 1891020 doi: 10.1056/NEJM199110173251603
Nomura A, Stemmermann GN, Chyou PH, Kato I, Perez-Perez GI, Blaser MJ. Helicobacter pylori infection and gastric carcinoma among Japanese Americans in Hawaii. N Engl J Med. 1991;325:1132–6.
pubmed: 1891021 doi: 10.1056/NEJM199110173251604
Forman D, Newell DG, Fullerton F, Yarnell JW, Stacey AR, Wald N, et al. Association between infection with helicobacter pylori and risk of gastric cancer: evidence from a prospective investigation. BMJ. 1991;302:1302–5.
pubmed: 2059685 pmcid: 1670011 doi: 10.1136/bmj.302.6788.1302
Correa P, Fox J, Fontham E, Ruiz B, Lin YP, Zavala D, et al. Helicobacter pylori and gastric carcinoma. Serum antibody prevalence in populations with contrasting cancer risks. Cancer. 1990;66:2569–74.
pubmed: 2249197 doi: 10.1002/1097-0142(19901215)66:12<2569::AID-CNCR2820661220>3.0.CO;2-I
Sipponen P, Hyvarinen H. Role of helicobacter pylori in the pathogenesis of gastritis, peptic ulcer and gastric cancer. Scand J Gastroenterol Suppl. 1993;196:3–6.
pubmed: 8341988 doi: 10.3109/00365529309098333
Oberg K, Astrup L, Eriksson B, Falkmer SE, Falkmer UG, Gustafsen J, et al. Guidelines for the management of gastroenteropancreatic neuroendocrine tumours (including bronchopulmonary and thymic neoplasms). Part II-specific NE tumour types. Acta Oncol. 2004;43:626–36.
pubmed: 15545183 doi: 10.1080/02841860410018502
Grozinsky-Glasberg S, Alexandraki KI, Angelousi A, Chatzellis E, Sougioultzis S, Kaltsas G. Gastric carcinoids. Endocrinol Metab Clin N Am. 2018;47:645–60.
doi: 10.1016/j.ecl.2018.04.013
Antonodimitrakis P, Tsolakis A, Welin S, Kozlovacki G, Oberg K, Granberg D. Gastric carcinoid in a patient infected with helicobacter pylori: a new entity? World J Gastroenterol. 2011;17:3066–8.
pubmed: 21799655 pmcid: 3132260 doi: 10.3748/wjg.v17.i25.3066
Takahashi S. Long-term helicobacter pylori infection and the development of atrophic gastritis and gastric cancer in Japan. J Gastroenterol. 2002;37:24–7.
pubmed: 12109661 doi: 10.1007/BF02990095
Hirayama F, Takagi S, Iwao E, Yokoyama Y, Haga K, Hanada S. Development of poorly differentiated adenocarcinoma and carcinoid due to long-term helicobacter pylori colonization in Mongolian gerbils. J Gastroenterol. 1999;34:450–4.
pubmed: 10452676 doi: 10.1007/s005350050295
Sato Y, Iwafuchi M, Ueki J, Yoshimura A, Mochizuki T, Motoyama H, et al. Gastric carcinoid tumors without autoimmune gastritis in Japan: a relationship with helicobacter pylori infection. Dig Dis Sci. 2002;47:579–85.
pubmed: 11911346 doi: 10.1023/A:1017972204219
Kagawa J, Honda S, Kodama M, Sato R, Murakami K, Fujioka T. Enterocromaffin-like cell tumor induced by helicobacter pylori infection in Mongolian gerbils. Helicobacter. 2002;7:390–7.
pubmed: 12485127 doi: 10.1046/j.1523-5378.2002.00115.x
Cao L, Mizoshita T, Tsukamoto T, Takenaka Y, Toyoda T, Cao X, et al. Development of carcinoid tumors of the glandular stomach and effects of eradication in helicobacter pylori-infected Mongolian gerbils. Asian Pac J Cancer Prev. 2008;9:25–30.
pubmed: 18439067
Murphy G, Dawsey SM, Engels EA, Ricker W, Parsons R, Etemadi A, et al. Cancer risk after pernicious anemia in the US elderly population. Clin Gastroenterol Hepatol. 2015;13:2282–9.
pubmed: 26079040 pmcid: 4655146 doi: 10.1016/j.cgh.2015.05.040
Solcia E, Rindi G, Fiocca R, Villani L, Buffa R, Ambrosiani L, et al. Distinct patterns of chronic gastritis associated with carcinoid and cancer and their role in tumorigenesis. Yale J Biol Med. 1992;65:793–804.
pubmed: 1341079 pmcid: 2589778
Karnes WE Jr, Samloff IM, Siurala M, Kekki M, Sipponen P, Kim SW, et al. Positive serum antibody and negative tissue staining for helicobacter pylori in subjects with atrophic body gastritis. Gastroenterology. 1991;101:167–74.
pubmed: 2044906 doi: 10.1016/0016-5085(91)90474-Y
Ananthamurthy A, Correa M, Patil M. Type 1 gastric carcinoid in the indian population and its association with multifocal gastric atrophy. Euroasian J Hepatogastroenterol. 2016;6:106–10.
pubmed: 29201740 pmcid: 5578576 doi: 10.5005/jp-journals-10018-1180
Modlin M, Tang LH. The gastric enterochromaffin-like cell: an enigmatic cellular lesion. Gastroenterology. 1996;111:783–810.
pubmed: 8780586 doi: 10.1053/gast.1996.v111.agast961110783
Sue S, Shibata W, Maeda S. Helicobacter pylori-induced signaling pathways contribute to intestinal metaplasia and gastric carcinogenesis. Biomed Res Int. 2015;2015:737621.
pubmed: 26064948 pmcid: 4441984 doi: 10.1155/2015/737621
Kidd M, Miu K, Tang LH, Perez-Perez GI, Blaser MJ, Sandor A, et al. Helicobacter pylori lipopolysaccharide stimulates histamine release and DNA synthesis in rat enterochromaffin-like cells. Gastroenterology. 1997;113:1110–7.
Modlin M, Kidd M, Miu K, Tang LH. The effect of Helicobacter pylori on enterochromaffin-like (ECL) cell function. Helicobacter pylori pp 176–187.
Kinoshita Y, Ishihara S, Kadowaki Y, Fukui H, Chiba T. Reg protein is a unique growth factor of gastric mucosal cells. J Gastroenterol. 2004;39:507–13.
pubmed: 15235866 doi: 10.1007/s00535-004-1354-5
Chang WL, Yeh YC, Sheu BS. The impacts of H pylori virulence factors on the development of gastroduodenal diseases. J Biomed Sci. 2018;25:68.
pubmed: 30205817 pmcid: 6131906 doi: 10.1186/s12929-018-0466-9
Bowen KA, Silva SR, Johnson JN, Doan HQ, Jackson LN, Gulhati P, et al. An analysis of trends and growth factor receptor expression of GI carcinoid tumors. Gastrointest Surg. 2009;13:1773–80.
doi: 10.1007/s11605-009-0958-8
Besig S, Voland P, Baur DM, Perren A, Prinz C. Vascular endothelial growth factors, angiogenesis, and survival in human ileal enterochromaffin cell carcinoids. Neuroendocrinology. 2009;90:402–15.
pubmed: 19816005 doi: 10.1159/000245900
Shah T, Hochhauser D, Frow R, Quaglia A, Dhillon AP, Caplin ME. Epidermal growth factor receptor expression and activation in neuroendocrine tumours. J Neuroendocrinol. 2006;18:355–60.
pubmed: 16629834 doi: 10.1111/j.1365-2826.2006.01425.x
Azzoni C, Bottarelli L, Cecchini S, Lagrasta C, Pizzi S, D'Adda T, et al. Involvement of HER-2/neu and metastasis-related proteins in the development of ileal neuroendocrine tumors. Virchows Arch. 2011;458:525–36.
pubmed: 21445634 doi: 10.1007/s00428-011-1069-y
Grillo F, Florio T, Ferraù F, Kara E, Fanciulli G, Faggiano A, et al. Emerging multitarget tyrosine kinase inhibitors in the treatment of neuroendocrine neoplasms. Endocr Relat Cancer. 2018;25:R453–66.
pubmed: 29769293 doi: 10.1530/ERC-17-0531
de Jesus SM, de Moraes JA, Da Silva VN, Helal-Neto E, Uberti AF, Scopel-Guerra A, et al. Helicobacter pylori urease induces pro-inflammatory effects and differentiation of human endothelial cells: cellular and molecular mechanism. Helicobacter. 2019 Jun;24:e12573.
doi: 10.1111/hel.12573
Keates S, Keates AC, Katchar K, Peek RM Jr, Kelly CP. Helicobacter pylori induces up-regulation of the epidermal growth factor receptor in AGS gastric epithelial cells. J Infect Dis. 2007;196:95–103.
pubmed: 17538889 doi: 10.1086/518440
Gunawardhana N, Jang S, Choi YH, Hong YA, Jeon YE, Kim A, et al. Helicobacter pylori-induced HB-EGF upregulates gastrin expression via the EGF receptor, C-Raf, Mek1, and Erk2 in the MAPK pathway. Front Cell Infect Microbiol. 2018;7:541.
pubmed: 29379775 pmcid: 5775237 doi: 10.3389/fcimb.2017.00541
Kwok T, Zabler D, Urman S, Rohde M, Hartig R, Wessler S, et al. Helicobacter exploits integrin for type IV secretion and kinase activation. Nature. 2007;449:862–6.
pubmed: 17943123 doi: 10.1038/nature06187
Tegtmeyer N, Zabler D, Schmidt D, Hartig R, Brandt S, Backert S. Importance of EGF receptor, HER2/Neu and Erk1/2 kinase signalling for host cell elongation and scattering induced by the helicobacter pylori CagA protein: antagonistic effects of the vacuolating cytotoxin VacA. Cell Microbiol. 2009;11:488–505.
pubmed: 19046339 doi: 10.1111/j.1462-5822.2008.01269.x
Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, et al. Mutations of the BRAF gene in human cancer. Nature. 2002;417:949–54.
pubmed: 12068308 doi: 10.1038/nature00766
Jiao Y, Shi C, Edil BH, de Wilde RF, Klimstra DS, Maitra A, et al. DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumours. Science. 2011;331:1199–203.
pubmed: 21252315 pmcid: 3144496 doi: 10.1126/science.1200609
Gilbert JA, Adhikari LJ, Lloyd RV, Halfdanarson TR, Muders MH, Ames MM. Molecular markers for novel therapeutic strategies in pancreatic endocrine tumours. Pancreas. 2013;42:411–21.
pubmed: 23211371 pmcid: 3594087 doi: 10.1097/MPA.0b013e31826cb243
Astsaturov IA, Cohen SJ, Engstrom PF, Gatalica Z, Bender RP, Basu GD, et al. Profiling of a global cohort of 1250 neuroendocrine tumours to identify multiple potential drug targets. J Clin Oncol. 2014;32:214–4. https://doi.org/10.1200/jco.2014.32.3_suppl.214 .
Tannapfel A, Vomschloss S, Karhoff D, Markwarth A, Hengge UR, Wittekind C, et al. BRAF gene mutations are rare events in gastroenteropancreatic neuroendocrine tumors. Am J Clin Pathol. 2005;123:256–60.
pubmed: 15842051 doi: 10.1309/YQBR9C05RU4DD3RN
Karhoff D, Sauer S, Schrader J, Arnold R, Fendrich V, Bartsch DK, et al. Rap1/B-Raf signaling is activated in neuroendocrine tumors of the digestive tract and Raf kinase inhibition constitutes a putative therapeutic target. Neuroendocrinology. 2007;851:45–53.
doi: 10.1159/000100508
Sippel RS, Carpenter JE, Kunnimalaiyaan M, Lagerholm S, Chen H. Raf-1 activation suppresses neuroendocrine marker and hormone levels in human gastrointestinal carcinoid cells. Am J Physiol Gastrointest Liver Physiol. 2003;285:G245–54.
pubmed: 12851216 doi: 10.1152/ajpgi.00420.2002
Ning L, Chen H, Kunnimalaiyaan M. Focal adhesion kinase, a downstream mediator of Raf-1 signaling, suppresses cellular adhesion, migration, and neuroendocrine markers in BON carcinoid cells. Mol Cancer Res. 2010;8:775–82.
pubmed: 20407018 pmcid: 2872724 doi: 10.1158/1541-7786.MCR-09-0525
Rozengurt E, Walsh JH. Gastrin, CCK, signaling, and cancer. Annu Rev Physiol. 2001;63:49–76.
pubmed: 11181948 doi: 10.1146/annurev.physiol.63.1.49
Chalmers CJ, Gilley R, March HN, Balmanno K, Cook SJ. The duration of ERK1/2 activity determines the activation of c-Fos and Fra-1 and the composition and quantitative transcriptional output of AP-1. Cell Signal. 2007;19:695–704.
pubmed: 17052890 doi: 10.1016/j.cellsig.2006.09.001
Treinies I, Paterson HF, Hooper S, Wilson R, Marshall CJ. Activated MEK stimulates expression of AP-1 components independently of phosphatidylinositol 3-kinase (PI3-kinase) but requires a PI3-kinase signal to stimulate DNA synthesis. Mol Cell Biol. 1999;19:321–9.
pubmed: 9858556 pmcid: 83890 doi: 10.1128/MCB.19.1.321
Kinoshita Y, Nakata H, Kishi K, Kawanami C, Sawada M, Chiba T. Comparison of the signal transduction pathways activated by gastrin in enterochromaffin-like and parietal cells. Gastroenterology. 1998;115:93–100.
pubmed: 9649463 doi: 10.1016/S0016-5085(98)70369-5
Naumann M, Crabtree JE. Helicobacter pylori-induced epithelial cell signalling in gastric carcinogenesis. Trends Microbiol. 2004;12:29–36.
pubmed: 14700549 doi: 10.1016/j.tim.2003.11.005
Hisatsune J, Nakayama M, Isomoto H, Kurazono H, Mukaida N, Mukhopadhyay AK, et al. Molecular characterization of helicobacter pylori VacA induction of IL-8 in U937 cells reveals a prominent role for p38MAPK in activating transcription Factor-2, cAMP response element binding protein, and NF-κB activation. J Immunol. 2008;180:5017–27.
pubmed: 18354227 doi: 10.4049/jimmunol.180.7.5017
Nakayama M, Kimura M, Wada A, Yahiro K, Ogushi K, Niidome T, et al. Helicobacter pylori VacA activates the p38/activating transcription factor 2-mediated signal pathway in AZ-521 cells. J Biol Chem. 2004;279:7024–8.
pubmed: 14630932 doi: 10.1074/jbc.M308898200
Lee IO, Kim JH, Choi YJ, Pillinger MH, Kim SY, Blaser MJ, et al. Helicobacter pylori CagA phosphorylation status determines the gp130-activated SHP2/ERK and JAK/STAT signal transduction pathways in gastric epithelial cells. Biol Chem. 2010;285:16042–50.
doi: 10.1074/jbc.M110.111054
Keates S, Keates AC, Warny M, Peek RM Jr, Murray PG, Kelly CP. Differential activation of mitogen-activated protein kinases in AGS gastric epithelial cells by cagand cag helicobacter pylori. J Immunol. 1999;163:5552–9.
pubmed: 10553083
Berardi R, Morgese F, Torniai M, Savini A, Partelli S, Rinaldi S, et al. Medical treatment for gastro-entero-pancreatic neuroendocrine tumours. World J Gastrointest Oncol. 2016;8:389–401.
pubmed: 27096034 pmcid: 4824717 doi: 10.4251/wjgo.v8.i4.389
Svejda B, Kidd M, Kazberouk A, Lawrence B, Pfragner R, Modlin IM. Limitations in small intestinal neuroendocrine tumor therapy by mTor kinase inhibition reflect growth factor-mediated PI3K feedback loop activation via ERK1/2 and AKT. Cancer. 2011;117:4141–54.
pubmed: 21387274 doi: 10.1002/cncr.26011
Yang Z, Xie C, Xu W, Liu G, Cao X, Li W, et al. Phosphorylation and inactivation of PTEN at residues Ser380/Thr382/383 induced by helicobacter pylori promotes gastric epithelial cell survival through PI3K/Akt pathway. Oncotarget. 2015;6:31916–26.
pubmed: 26376616 pmcid: 4741650 doi: 10.18632/oncotarget.5577
Tabassam FH, Graham DY, Yamaoka Y. Helicobacter pylori-associated regulation of forkhead transcription factors FoxO1/3a in human gastric cells. Helicobacter. 2012;17:193–202.
pubmed: 22515357 pmcid: 3335761 doi: 10.1111/j.1523-5378.2012.00939.x
Valenzuela-Valderrama M, Cerda-Opazo P, Backert S, González MF, Carrasco-Véliz N, Jorquera-Cordero C, et al. The helicobacter pylori urease virulence factor is required for the induction of hypoxia-induced factor-1α in gastric cells. Cancers. 2019;11:799.
pmcid: 6627347 doi: 10.3390/cancers11060799
Wang H, Chen Y, Fernandez-Del Castillo C, Yilmaz O, Deshpande V. Heterogeneity in signalling pathways of gastroenteropancreatic neuroendocrine tumors: a critical look at notch signaling pathway. Mod Pathol. 2013;26:139–47.
pubmed: 22918166 doi: 10.1038/modpathol.2012.143
Liu T, He W, Li Y. Helicobacter pylori infection of gastric epithelial cells affects NOTCH pathway in vitro. Dig Dis Sci. 2016;61:2516–21.
pubmed: 27073072 doi: 10.1007/s10620-016-4161-y
Kim JT, Li J, Jang ER, Gulhati P, Rychahou PG, Napier DL, et al. Deregulation of Wnt/β-catenin signaling through genetic or epigenetic alterations in human neuroendocrine tumors. Carcinogenesis. 2013;34:953–61.
pubmed: 23354304 pmcid: 3643417 doi: 10.1093/carcin/bgt018
Su MC, Wang CC, Chen CC, Hu RH, Wang TH, Kao HL, et al. Nuclear translocation of beta-catenin protein but absence of beta-catenin and APC mutation in gastrointestinal carcinoid tumor. Ann Surg Oncol. 2006;13:1604–9.
pubmed: 17009161 doi: 10.1245/s10434-006-9072-2
Fujimori M, Ikeda S, Shimizu Y, Okajima M, Asahara T. Accumulation of beta-catenin protein and mutations in exon 3 of beta-catenin gene in gastrointestinal carcinoid tumor. Cancer Res. 2001;61:6656–9.
pubmed: 11559529
Bottarelli L, Azzoni C, Pizzi S, D'Adda T, Silini EM, Bordi C, et al. Adenomatous polyposis coli gene involvement in ileal enterochromaffin cell neuroendocrine neoplasms. Hum Pathol. 2013;44:2736–42.
pubmed: 24139208 doi: 10.1016/j.humpath.2013.06.019
Franco AT, Israel DA, Washington MK, Krishna U, Fox JG, Rogers AB, et al. Activation of beta-catenin by carcinogenic helicobacter pylori. Proc Natl Acad Sci U S A. 2005;102:10646–51.
pubmed: 16027366 pmcid: 1180811 doi: 10.1073/pnas.0504927102
Nagy TA, Wroblewski LE, Wang D, Piazuelo MB, Delgado A, Romero-Gallo J, et al. β-Catenin and p120 mediate PPARδ-dependent proliferation induced by Helicobacter pylori in human and rodent epithelia. Gastroenterology. 2011;141:553–64.
pubmed: 21704622 doi: 10.1053/j.gastro.2011.05.004
Ito K, Chuang LS, Ito T, Chang TL, Fukamachi H, Salto-Tellez M, et al. Loss of Runx3 is a key event in inducing precancerous state of the stomach. Gastroenterology. 2011;140:1536–46e8.
pubmed: 21277301 doi: 10.1053/j.gastro.2011.01.043
Nakayama M, Hisatsune J, Yamasaki E, Isomoto H, Kurazono H, Hatakeyama M, et al. Helicobacter pylori VacA-induced inhibition of GSK3 through the PI3K/Akt signaling pathway. J Biol Chem. 2009;284:1612–9.
pubmed: 18996844 pmcid: 2615499 doi: 10.1074/jbc.M806981200
Schumacher MA, Donnelly JM, Engevik AC, Xiao C, Yang L, Kenny S, et al. Gastric Sonic Hedgehog acts as a macrophage chemoattractant during the immune response to Helicobacter pylori. Gastroenterology. 2012;142:1150–59.e6.
pubmed: 22285806 doi: 10.1053/j.gastro.2012.01.029
Liu N, Zhou N, Chai N, Liu X, Jiang H, Wu Q, et al. Helicobacter pylori promotes angiogenesis depending on Wnt/beta-catenin-mediated vascular endothelial growth factor via the cyclooxygenase-2 pathway in gastric cancer. BMC Cancer. 2016;16:321.
pubmed: 27198692 pmcid: 4873996 doi: 10.1186/s12885-016-2351-9
Papageorgis P. TGFbeta signaling in tumor initiation, epithelial to mesenchymal transition and metastasis. J.Oncol. 2015;2015:587193.
pubmed: 25883652 pmcid: 4389829 doi: 10.1155/2015/587193
Samanta D, Datta PK. Alterations in the Smad pathway in human cancers. Front Biosci (Landmark Ed). 2012;17:1281–93.
pmcid: 4281477 doi: 10.2741/3986
Akhurst RJ, Hata A. Targeting the TGFbeta signalling pathway in disease. Nat Rev Drug Discov. 2012;11:790–811.
pubmed: 23000686 pmcid: 3520610 doi: 10.1038/nrd3810
Xu X, Zhu L. MiR-124 promotes proliferation and differentiation of osteoblasts via BMP/TGF-β signaling pathway. Minerva Endocrinol. 2019.
Gilbert JA, Adhikari LJ, Lloyd RV, Rubin J, Haluska P, Carboni JM, et al. Molecular markers for novel therapies in neuroendocrine (carcinoid) tumors. Endocr Relat Cancer. 2010;17:623–36.
pubmed: 20385747 doi: 10.1677/ERC-09-0318
Roland CL, Starker LF, Kang Y, Chatterjee D, Estrella J, Rashid A, et al. Surgery. Loss of DPC4/SMAD4 expression in primary gastrointestinal neuroendocrine tumors is associated with cancer-related death after resection. 2017;161:753–9.
Banck MS, Kanwar R, Kulkarni AA, Boora GK, Metge F, Kipp BR, et al. The genomic landscape of small intestine neuroendocrine tumors. J Clin Invest. 2013;123:2502–8.
pubmed: 23676460 pmcid: 3668835 doi: 10.1172/JCI67963
Kidd M, Modlin IM, Pfragner R, Eick GN, Champaneria MC, Chan AK, et al. Small bowel carcinoid (enterochromaffin cell) neoplasia exhibits transforming growth factor-b1-mediated regulatory abnormalities including up-regulation of C-Myc and MTA1. Cancer. 2007;109:2420–31.
pubmed: 17469181 doi: 10.1002/cncr.22725
Rahimian G, Sanei MH, Shirzad H, Azadegan-Dehkordi F, Taghikhani A, et al. Virulence factors of helicobacter pylori vacA increase markedly gastric mucosal TGF-β1 mRNA expression in gastritis patients. Microb Pathog. 2014;67-68:1–7.
pubmed: 24462401 doi: 10.1016/j.micpath.2013.12.006
Inoue K, Fry EA, Frazier DP. Transcription factors that interact with p53 and Mdm2. Int J Cancer. 2016;138:1577–85.
pubmed: 26132471 doi: 10.1002/ijc.29663
Zhao Y, Aguilar A, Bernard D, Wang S. Small-molecule inhibitors of the MDM2-p53 protein-protein interaction (MDM2 inhibitors) in clinical trials for cancer treatment. J Med Chem. 2015;58:1038–52.
pubmed: 25396320 doi: 10.1021/jm501092z
Brazina J, Svadlenka J, Macurek L, Andera L, Hodny Z, Bartek J, et al. DNA damage-induced regulatory interplay between DAXX, p53, ATM kinase and Wip1 phosphatase. Cell Cycle. 2015;14:375–87.
pubmed: 25659035 pmcid: 4353233 doi: 10.4161/15384101.2014.988019
Makuuchi R, Terashima M, Kusuhara M, Nakajima T, Serizawa M, Hatakeyama K, et al. Comprehensive analysis of gene mutation and expression profiles in neuroendocrine carcinomas of the stomach. Biomed Res. 2017;38:19–27.
pubmed: 28239029 doi: 10.2220/biomedres.38.19
Vijayvergia N, Boland PM, Handorf E, Gustafson KS, Gong Y, Cooper HS, et al. Molecular profiling of neuroendocrine malignancies to identify prognostic and therapeutic markers: a Fox Chase Cancer Center pilot study. Br J Cancer. 2016;115:564–70.
pubmed: 27482646 pmcid: 4997552 doi: 10.1038/bjc.2016.229
Hu W, Feng Z, Modica I, Klimstra DS, Song L, Allen PJ, et al. Gene amplifications in well-differentiated pancreatic neuroendocrine tumors inactivate the p53 pathway. Genes Cancer. 2010;1:360–8.
pubmed: 20871795 pmcid: 2943645 doi: 10.1177/1947601910371979
Shin JU, Lee CH, Lee KT, Lee JK, Lee KH, Kim KM, et al. Prognostic significance of ATM and cyclin B1 in pancreatic neuroendocrine tumor. Tumour Biol. 2012;33:1645–51.
pubmed: 22707287 doi: 10.1007/s13277-012-0420-5
Lee J, Sung CO, Lee EJ, Do IG, Kim HC, Yoon SH, et al. Metastasis of neuroendocrine tumors are characterized by increased cell proliferation and reduced expression of the ATM gene. PLoS One. 2012:7–e34456.
Luque EA, Tang LH, Bortecen KH, Kidd M, Miu K, Efstathiou JA, et al. Gastrin-regulated expression of p53 in transformed enterochromaffin-like cells in the african rodent mastomys. J Clin Gastroenterol. 1998;27(Suppl 1):S116–24.
pubmed: 9872508 doi: 10.1097/00004836-199800001-00019
Wei J, Nagy TA, Vilgelm A, Zaika E, Ogden SR, Romero-Gallo J, et al. Regulation of p53 tumor suppressor by helicobacter pylori in gastric epithelial cells. Gastroenterology. 2010;139:1333–43.
pubmed: 20547161 doi: 10.1053/j.gastro.2010.06.018
Toller IM, Neelsen KJ, Steger M, Hartung ML, Hottiger MO, Stucki M, et al. Carcinogenic bacterial pathogen helicobacter pylori triggers DNA double-strand breaks and a DNA damage response in its host cells. Proc Natl Acad Sci U S A. 2011;108:14944–9.
pubmed: 21896770 pmcid: 3169107 doi: 10.1073/pnas.1100959108
Casimiro MC, Crosariol M, Loro E, Li Z, Pestell RG. Cyclins and cell cycle control in cancer and disease. Genes Cancer. 2012;3:649–57.
pubmed: 23634253 pmcid: 3636749 doi: 10.1177/1947601913479022
Cicenas J, Valius M. The CDK inhibitors in cancer research and therapy. J Cancer Res Clin Oncol. 2011;137:1409–18.
pubmed: 21877198 doi: 10.1007/s00432-011-1039-4
Cicenas J, Kalyan K, Sorokinas A, Jatulyte A, Valiunas D, Kaupinis A, et al. Highlights of the latest advances in research on CDK inhibitors. Cancers (Basel). 2014;6:2224–42.
doi: 10.3390/cancers6042224
Malumbres M. Perez de Castro I. Aurora kinase a inhibitors: promising agents in antitumoural therapy. Expert Opin Ther Targets. 2014;18:1377–93.
pubmed: 25200357
Law ME, Corsino PE, Narayan S, Law BK. Cyclin-dependent kinase inhibitors as anticancer therapeutics. Mol Pharmacol. 2015;88:846–52.
pubmed: 26018905 pmcid: 4613943 doi: 10.1124/mol.115.099325
Malinkova V, Vylicil J, Krystof V. Cyclin-dependent kinase inhibitors for cancer therapy: a patent review (2009–2014). Expert Opin Ther Pat. 2015;25:953–70.
pubmed: 26161698 doi: 10.1517/13543776.2015.1045414
Tang LH, Contractor T, Clausen R, Klimstra DS, Du YC, Allen PJ, et al. Attenuation of the retinoblastoma pathway in pancreatic neuroendocrine tumours because of increased cdk4/cdk6. Clin Cancer Res. 2012;18:4612–20.
pubmed: 22761470 doi: 10.1158/1078-0432.CCR-11-3264
Francis JM, Kiezun A, Ramos AH, Serra S, Pedamallu CS, Qian ZR, et al. Somatic mutation of CDKN1B in small intestine neuroendocrine tumors. Nat Genet. 2013;45:1483–6.
pubmed: 24185511 pmcid: 4239432 doi: 10.1038/ng.2821
Karpathakis A, Dibra H, Pipinikas C, Feber A, Morris T, Francis J, et al. Prognostic impact of novel molecular subtypes of small intestinal neuroendocrine tumour. Clin Cancer Res. 2016;22:250–8.
pubmed: 26169971 doi: 10.1158/1078-0432.CCR-15-0373
Grabowski P, Schrader J, Wagner J, Horsch D, Arnold R, Arnold CN, et al. Loss of nuclear p27 expression and its prognostic role in relation to cyclin E and p53 mutation in gastroenteropancreatic neuroendocrine tumours. Clin Cancer Res. 2008;14:7378–84. https://doi.org/10.1158/1078-0432.CCR-08-0698 .
Yachida S, Vakiani E, White CM, Zhong Y, Saunders T, Morgan R, et al. Small cell and large cell neuroendocrine carcinomas of the pancreas are genetically similar and distinct from well-differentiated pancreatic neuroendocrine tumors. Am J Surg Pathol. 2012;36:173–84.
pubmed: 22251937 pmcid: 3261427 doi: 10.1097/PAS.0b013e3182417d36
Zhang T, Tang L, Kidd M, Lauffer J, Modlin I. Gastric enterochromaffin-like (ECL) transformation is associated with increased expression of the G1 cell cycle regulators cyclin D1 and cdk4. Gastroenterology. 1998;114:G2932.
Kidd M, Hinoue T, Eick G, Lye KD, Mane SM, Wen Y, et al. Global expression analysis of ECL cells in Mastomys natalensis gastric mucosa identifies alterations in the AP-1 pathway induced by gastrin-mediated transformation. Physiol Genomics. 2004;20:131–42.
pubmed: 15602048 doi: 10.1152/physiolgenomics.00216.2003
Hönig A, Witte F, Mirecka J, Binder C, Schauer A. Helicobacter pylori-induced hyperproliferation: relevance for gastric cancer development in connection with mutagenic factors. Anticancer Res. 2000;20:1641–8.
pubmed: 10928084
Suzuki N, Wakasugi M, Nakaya S, Okada K, Mochida R, Sato M, et al. Production and application of new monoclonal antibodies specific for a fecal helicobacter pylori antigen. Clin Diagn Lab Immunol. 2002;9:75–8.
pubmed: 11777832 pmcid: 119870
Byun SW, Chang YJ, Chung IS, Moss SF, Kim SS. Helicobacter pylori decreases p27 expression through the delta opioid receptor-mediated inhibition of histone acetylation within the p27 promoter. Cancer Lett. 2012;326:96–104.
pubmed: 22867947 pmcid: 3444678 doi: 10.1016/j.canlet.2012.07.032
Bahnassy AA, Helal TE, El-Ghazawy IM, Samaan GF, Galal El-Din MM, et al. The role of E-cadherin and Runx3 in helicobacter pylori - associated gastric carcinoma is achieved through regulating P21waf and P27 expression. Cancer Gene Ther. 2018;228-229:64–72.
doi: 10.1016/j.cancergen.2018.08.006
Eguchi H, Carpentier S, Kim SS, Moss SF. P27kip1 regulates the apoptotic response of gastric epithelial cells to helicobacter pylori. Gut. 2004;53:797–804.
pubmed: 15138205 pmcid: 1774067 doi: 10.1136/gut.2003.032144
La Rosa S, Rigoli E, Uccella S, Chiaravalli AM, Capella C. CDX2 as a marker of intestinal EC-cells and related well-differentiated endocrine tumors. Virchows Arch. 2004;445:248–54.
pubmed: 15517368 doi: 10.1007/s00428-004-1080-7
Srivastava A, Hornick JL. Immunohistochemical staining for CDX-2, PDX-1, NESP-55 and TTF-1 can help distinguish gastrointestinal carcinoid tumors from pancreatic endocrine and pulmonary carcinoid tumors. Am J Surg Pathol. 2009;33:626–32.
pubmed: 19065104 doi: 10.1097/PAS.0b013e31818d7d8b
Herman Mahečić D, Cigrovski Berković M, Zjačić-Rotkvić V, Čačev T, Kapitanović S, Ulamec M. Inflammation-related cytokines and their roles in gastroenteropancreatic neuroendocrine neoplasms. Bosn J Basic Med Sci. 2020.
Kinoshita H, Hirata Y, Nakagawa H, Sakamoto K, Hayakawa Y, Takahashi R, et al. Interleukin-6 mediates epithelial-stromal interactions and promotes gastric tumorigenesis. PLoS One. 2013;8:e60914.
pubmed: 23593346 pmcid: 3625204 doi: 10.1371/journal.pone.0060914
Hatakeyama M. Helicobacter pylori CagA and gastric cancer: a paradigm for hit-and-run carcinogenesis. Cell Host Microbe. 2014;15:306–16.
pubmed: 24629337 doi: 10.1016/j.chom.2014.02.008
Wang TC, Goldenring JR. Inflammation intersection: gp130 balances gut irritation and stomach cancer. Nat Med. 2002;8:1080–2.
pubmed: 12357240 doi: 10.1038/nm1002-1080
Tebbutt NC, Giraud AS, Inglese M, Jenkins B, Waring P, Clay FJ, 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.
pubmed: 12219085 doi: 10.1038/nm763
Satoh K, Mutoh H, Eda A, Yanaka I, Osawa H, Honda S, et al. Aberrant expression of CDX2 in the gastric mucosa with and without intestinal metaplasia: effect of eradication of helicobacter pylori. Helicobacter. 2002;7:192–8.
pubmed: 12047325 doi: 10.1046/j.1523-5378.2002.00080.x
Kim HS, Lee HS, Kim WH. Clinical significance of protein expression of cyclooxygenase-2 and somatostatin receptors in gastroenteropancreatic neuroendocrine tumors. Cancer Res Treat. 2011;43:181–8.
pubmed: 22022296 pmcid: 3192880 doi: 10.4143/crt.2011.43.3.181
Liu B, Qu L, Yan S. Cyclooxygenase-2 promotes tumor growth and suppresses tumor immunity. Cancer Cell Int. 2015;15:106.
pubmed: 26549987 pmcid: 4635545 doi: 10.1186/s12935-015-0260-7
Fu S, Ramanujam KS, Wong A, Fantry GT, Drachenberg CB, James SP, et al. Increased expression and cellular localization of inducible nitric oxide synthase and cyclooxygenase 2 in helicobacter pylori gastritis. Gastroenterology. 1999;116:1319–29.
pubmed: 10348815 doi: 10.1016/S0016-5085(99)70496-8
Pero R, Peluso S, Angrisano T, Tuccillo C, Sacchetti S, Keller S, et al. Chromatin and DNA methylation dynamics of helicobacter pylori-induced COX-2 activation. Int J Med Microbiol. 2011;301:140–9.
pubmed: 20934379 doi: 10.1016/j.ijmm.2010.06.009
Zhang H, Ding C, Suo Z, Kang Y. Effect of helicobacter pylori on cyclooxygenase-2 and inducible nitric oxide synthase in patients with gastric precancerous lesions and its clinical significance. Exp Ther Med. 2015;9:2364–8.
pubmed: 26136988 pmcid: 4473662 doi: 10.3892/etm.2015.2387
Bojesen RD, Riis LB, Hogdall E, Nielsen OH, Jess T. Inflammatory bowel disease and small bowel cancer risk, clinical characteristics, and histopathology: a population-based study. Clin Gastroenterol Hepatol. 2017;15:1900–7.
pubmed: 28694132 doi: 10.1016/j.cgh.2017.06.051
Algaba A, Guerra I, Castano A, de la Poza G, Castellano VM, Lopez M, et al. Risk of cancer, with special reference to extra-intestinal malignancies, in patients with inflammatory bowel disease. World J Gastroenterol. 2013;19:9359–65.
pubmed: 24409063 pmcid: 3882409 doi: 10.3748/wjg.v19.i48.9359
Lal P, Saleh MA, Khoudari G, Gad MM, Mansoor E, Isenberg G, et al. Epidemiology of large bowel carcinoid tumors in the USA: a population-based national study. Dig Dis Sci. 2020;65:269–75.
pubmed: 31300994 doi: 10.1007/s10620-019-05725-0
Sciola V, Massironi S, Conte D, Caprioli F, Ferrero S, Ciafardini C, et al. Plasma chromogranin a in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2009;15:867–71.
pubmed: 19090560 doi: 10.1002/ibd.20851
Derikx LA, Vierdag WM, Kievit W, Bosch S, Hoentjen F, Nagtegaal ID. Is the prevalence of colonic neuroendocrine tumors increased in patients with inflammatory bowel disease? Int J Cancer. 2016;139:535–42.
pubmed: 26992110 doi: 10.1002/ijc.30096
Praticò C, Rizzello F, Fornarini GS, Calafiore A, Calabrese C, Campieri M, et al. Four cases of carcinoid tumour in Crohn's disease: coincidence or correlation? Int J Color Dis. 2013;28:1743–5.
doi: 10.1007/s00384-013-1732-7
Wong M, Larson BK, Dhall D. Neuroendocrine proliferations in inflammatory bowel disease: differentiating neuroendocrine tumours from neuroendocrine cell micronests. Histopathology. 2019;74:415–23.
pubmed: 30303561 doi: 10.1111/his.13769
Prosberg M, Bendtsen F, Vind I, Petersen AM, Gluud LL. The association between the gut microbiota and the inflammatory bowel disease activity: a systematic review and meta-analysis. Scand J Gastroenterol. 2016;51:1407–15.
pubmed: 27687331 doi: 10.1080/00365521.2016.1216587
Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012;491:119–24.
pubmed: 23128233 pmcid: 3491803 doi: 10.1038/nature11582
Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A. 2007;104:13780–5.
pubmed: 17699621 pmcid: 1959459 doi: 10.1073/pnas.0706625104
Nell S, Suerbaum S, Josenhans C. The impact of the microbiota on the pathogenesis of IBD: lessons from mouse infection models. Nat Rev Microbiol. 2010;8:564–77.
pubmed: 20622892 doi: 10.1038/nrmicro2403
Ni J, Wu JD, Albenberg L, Tomov VT. Gut microbiota and IBD: causation or correlation? Nat Rev Gastroenterol Hepatol. 2017;14:573–84.
pubmed: 28743984 pmcid: 5880536 doi: 10.1038/nrgastro.2017.88
Machiels K, Joossens M, Sabino J, De Preter V, Arijs I, Eeckhaut V, et al. A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut. 2014;63:1275–83.
pubmed: 24021287 doi: 10.1136/gutjnl-2013-304833
Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, et al. Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut. 2006;55:205–11.
pubmed: 16188921 pmcid: 1856500 doi: 10.1136/gut.2005.073817
Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux JJ, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A. 2008;105:16731–6.
pubmed: 18936492 pmcid: 2575488 doi: 10.1073/pnas.0804812105
Döerffel Y, Pavel M, Loening-Baucke V, Swidsinski A. Common biostructure of the fecal flora in celiac disease, Crohn's disease, and carcinoid tumors. Inflamm Bowel Dis. 2008;14:1613–4.
pubmed: 18521905 doi: 10.1002/ibd.20507
Varela E, Manichanh C, Gallart M, Torrejón A, Borruel N, Casellas F, et al. Colonization by Faecabalibacterium prausnitzii and maintenance of clinical remission in patients with ulcerative colitis. Aliment Pharmacol Ther. 2013;38:151–61.
pubmed: 23725320 doi: 10.1111/apt.12365
Ferreira-Halder CV, Faria AVS, Andrade SS. Action and function of Faecalibacterium prausnitzii in health and disease. Best Pract Res Clin Gastroenterol. 2017;31:643–8.
pubmed: 29566907 doi: 10.1016/j.bpg.2017.09.011
Ma J, Sun L, Liu Y, Ren H, Shen Y, Bi F, et al. Alter between gut bacteria and blood metabolites and the anti-tumor effects of Faecalibacterium prausnitzii in breast cancer. BMC Microbiol. 2020;20:82.
Chaput N, Lepage P, Coutzac C, Soularue E, Le Roux K, Monot C, et al. Baseline gut microbiota predicts clinical response and colitis in metastatic melanoma patients treated with ipilimumab. Ann Oncol. 2017;28:1368–79.
pubmed: 28368458 doi: 10.1093/annonc/mdx108
Zuo T, Ng SC. The gut microbiota in the pathogenesis and therapeutics of inflammatory bowel disease. Front Microbiol. 2018;9:2247.
pubmed: 30319571 pmcid: 6167487 doi: 10.3389/fmicb.2018.02247
Sokol H, Leducq V, Aschard H, Pham HP, Jegou S, Landman C, et al. Fungal microbiota dysbiosis in IBD. Gut. 2017;66:1039–48.
pubmed: 26843508 doi: 10.1136/gutjnl-2015-310746
Tamagno G, Bennett A, Ivanovski I. Lights and darks of neuroendocrine tumors of the appendix. Minerva Endocrinol. 2020 Jul 23. Online ahead of print. https://doi.org/10.23736/S0391-1977.20.03206-X .

Auteurs

Giovanni Vitale (G)

Istituto Auxologico Italiano IRCCS, Laboratory of Geriatric and Oncologic Neuroendocrinology Research, Cusano Milanino, MI, Italy. giovanni.vitale@unimi.it.
Department of Clinical Sciences and Community Health (DISCCO), University of Milan, Milan, Italy. giovanni.vitale@unimi.it.

Alessandra Dicitore (A)

Department of Clinical Sciences and Community Health (DISCCO), University of Milan, Milan, Italy.

Luigi Barrea (L)

Department of Clinical Medicine and Surgery, University of Naples Federico II, Naples, Italy.

Emilia Sbardella (E)

Department of Experimental Medicine, Sapienza University of Rome, Rome, Italy.

Paola Razzore (P)

Endocrinology Unit, A.O. Ordine Mauriziano, Turin, Italy.

Severo Campione (S)

Pathology Department, Cardarelli Hospital, Naples, Italy.

Antongiulio Faggiano (A)

Department of Experimental Medicine, Sapienza University of Rome, Rome, Italy.

Annamaria Colao (A)

Department of Clinical Medicine and Surgery, University of Naples Federico II, Naples, Italy.

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Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
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Humans Yoga Low Back Pain Female Male

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