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Published in: Gut Pathogens 1/2012

Open Access 01-12-2012 | Review

Helicobacter pylori infection induced gastric cancer; advance in gastric stem cell research and the remaining challenges

Authors: Song-Ze Ding, Peng-Yuan Zheng

Published in: Gut Pathogens | Issue 1/2012

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Abstract

Helicobacter pylori infection is the major cause of gastric cancer, which remains an important health care challenge. Recent investigation in gastric stem cell or progenitor cell biology has uncovered valuable information in understanding the gastric gland renewal and maintenance of homeostasis, they also provide clues for further defining the mechanisms by which gastric cancer may originate and progress. Lgr5, Villin-promoter, TFF2-mRNA and Mist have recently been identified as gastric stem/progenitor cell markers; their identification enriched our understanding on the gastric stem cell pathobiology during chronic inflammation and metaplasia. In addition, advance in gastric cancer stem cell markers such as CD44, CD90, CD133, Musashi-1 reveal novel information on tumor cell behavior and disease progression implicated for therapeutics. However, two critical questions remain to be of considerable challenges for future exploration; one is how H. pylori or chronic inflammation affects gastric stem cell or their progenitors, which give rise to mucus-, acid-, pepsinogen-, and hormone-secreting cell lineages. Another one is how bacterial infection or inflammation induces oncogenic transformation and propagates into tumors. Focus on the interactions of H. pylori with gastric stem/progenitor cells and their microenvironment will be instrumental to decipher the initiation and origin of gastric cancer. Future studies in these areas will be critical to uncover molecular mechanisms of chronic inflammation-mediated oncogenic transformation and provide options for cancer prevention and intervention. We review recent progress and discuss future research directions in these important research fields.
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Literature
1.
go back to reference Peek RM, Crabtree JE: Helicobacter infection and gastric neoplasia. J Pathol. 2006, 208: 233-248. 10.1002/path.1868.CrossRefPubMed Peek RM, Crabtree JE: Helicobacter infection and gastric neoplasia. J Pathol. 2006, 208: 233-248. 10.1002/path.1868.CrossRefPubMed
2.
go back to reference Ernst PB, Peura DA, Crowe SE: The translation of Helicobacter pylori basic research to patient care. Gastroenterology. 2006, 130: 188-206. 10.1053/j.gastro.2005.06.032. quiz 212–3.CrossRefPubMed Ernst PB, Peura DA, Crowe SE: The translation of Helicobacter pylori basic research to patient care. Gastroenterology. 2006, 130: 188-206. 10.1053/j.gastro.2005.06.032. quiz 212–3.CrossRefPubMed
3.
go back to reference Houghton J, Stoicov C, Nomura S, Rogers AB, Carlson J, Li H, Cai X, Fox JG, Goldenring JR, Wang TC: Gastric cancer originating from bone marrow-derived cells. Science. 2004, 306: 1568-1571. 10.1126/science.1099513.CrossRefPubMed Houghton J, Stoicov C, Nomura S, Rogers AB, Carlson J, Li H, Cai X, Fox JG, Goldenring JR, Wang TC: Gastric cancer originating from bone marrow-derived cells. Science. 2004, 306: 1568-1571. 10.1126/science.1099513.CrossRefPubMed
4.
go back to reference Segal ED, Cha J, Lo J, Falkow S, Tompkins LS: Altered states: involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc Natl Acad Sci U S A. 1999, 96: 14559-14564. 10.1073/pnas.96.25.14559.PubMedCentralCrossRefPubMed Segal ED, Cha J, Lo J, Falkow S, Tompkins LS: Altered states: involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc Natl Acad Sci U S A. 1999, 96: 14559-14564. 10.1073/pnas.96.25.14559.PubMedCentralCrossRefPubMed
5.
go back to reference Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, Moran AP, Athman R, Memet S, Huerre MR, Coyle AJ, DiStefano PS, Sansonetti PJ, Labigne A, Bertin J, Philpott DJ, Ferrero RL: Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol. 2004, 5: 1166-1174. 10.1038/ni1131.CrossRefPubMed Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, Moran AP, Athman R, Memet S, Huerre MR, Coyle AJ, DiStefano PS, Sansonetti PJ, Labigne A, Bertin J, Philpott DJ, Ferrero RL: Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol. 2004, 5: 1166-1174. 10.1038/ni1131.CrossRefPubMed
6.
go back to reference Hatakeyama M: Linking epithelial polarity and carcinogenesis by multitasking Helicobacter pylori virulence factor CagA. Oncogene. 2008, 27: 7047-7054. 10.1038/onc.2008.353.CrossRefPubMed Hatakeyama M: Linking epithelial polarity and carcinogenesis by multitasking Helicobacter pylori virulence factor CagA. Oncogene. 2008, 27: 7047-7054. 10.1038/onc.2008.353.CrossRefPubMed
7.
go back to reference Radin JN, Gonzalez-Rivera C, Ivie SE, McClain MS, Cover TL: Helicobacter pylori VacA induces programmed necrosis in gastric epithelial cells. Infect Immun. 2011, 79: 2535-2543. 10.1128/IAI.01370-10.PubMedCentralCrossRefPubMed Radin JN, Gonzalez-Rivera C, Ivie SE, McClain MS, Cover TL: Helicobacter pylori VacA induces programmed necrosis in gastric epithelial cells. Infect Immun. 2011, 79: 2535-2543. 10.1128/IAI.01370-10.PubMedCentralCrossRefPubMed
8.
go back to reference Odenbreit S, Swoboda K, Barwig I, Ruhl S, Boren T, Koletzko S, Haas R: Outer membrane protein expression profile in Helicobacter pylori clinical isolates. Infect Immun. 2009, 77: 3782-3790. 10.1128/IAI.00364-09.PubMedCentralCrossRefPubMed Odenbreit S, Swoboda K, Barwig I, Ruhl S, Boren T, Koletzko S, Haas R: Outer membrane protein expression profile in Helicobacter pylori clinical isolates. Infect Immun. 2009, 77: 3782-3790. 10.1128/IAI.00364-09.PubMedCentralCrossRefPubMed
9.
go back to reference Ding SZ, Goldberg JB, Hatakeyama M: Helicobacter pylori infection, oncogenic pathways and epigenetic mechanisms in gastric carcinogenesis. Future Oncol. 2010, 6: 851-862. 10.2217/fon.10.37.PubMedCentralCrossRefPubMed Ding SZ, Goldberg JB, Hatakeyama M: Helicobacter pylori infection, oncogenic pathways and epigenetic mechanisms in gastric carcinogenesis. Future Oncol. 2010, 6: 851-862. 10.2217/fon.10.37.PubMedCentralCrossRefPubMed
10.
go back to reference Murata-Kamiya N, Kurashima Y, Teishikata Y, Yamahashi Y, Saito Y, Higashi H, Aburatani H, Akiyama T, Peek RM, Azuma T, Hatakeyama M: Helicobacter pylori CagA interacts with E-cadherin and deregulates the beta-catenin signal that promotes intestinal transdifferentiation in gastric epithelial cells. Oncogene. 2007, 26: 4617-4626. 10.1038/sj.onc.1210251.CrossRefPubMed Murata-Kamiya N, Kurashima Y, Teishikata Y, Yamahashi Y, Saito Y, Higashi H, Aburatani H, Akiyama T, Peek RM, Azuma T, Hatakeyama M: Helicobacter pylori CagA interacts with E-cadherin and deregulates the beta-catenin signal that promotes intestinal transdifferentiation in gastric epithelial cells. Oncogene. 2007, 26: 4617-4626. 10.1038/sj.onc.1210251.CrossRefPubMed
11.
go back to reference Franco AT, Israel DA, Washington MK, Krishna U, Fox JG, Rogers AB, Neish AS, Collier-Hyams L, Perez-Perez GI, Hatakeyama M, Whitehead R, Gaus K, O’Brien DP, Romero-Gallo J, Peek RM: Activation of beta-catenin by carcinogenic Helicobacter pylori. Proc Natl Acad Sci U S A. 2005, 102: 10646-10651. 10.1073/pnas.0504927102.PubMedCentralCrossRefPubMed Franco AT, Israel DA, Washington MK, Krishna U, Fox JG, Rogers AB, Neish AS, Collier-Hyams L, Perez-Perez GI, Hatakeyama M, Whitehead R, Gaus K, O’Brien DP, Romero-Gallo J, Peek RM: Activation of beta-catenin by carcinogenic Helicobacter pylori. Proc Natl Acad Sci U S A. 2005, 102: 10646-10651. 10.1073/pnas.0504927102.PubMedCentralCrossRefPubMed
12.
go back to reference Wang TC, Dangler CA, Chen D, Goldenring JR, Koh T, Raychowdhury R, Coffey RJ, Ito S, Varro A, Dockray GJ, Fox JG: Synergistic interaction between hypergastrinemia and Helicobacter infection in a mouse model of gastric cancer. Gastroenterology. 2000, 118: 36-47. 10.1016/S0016-5085(00)70412-4.CrossRefPubMed Wang TC, Dangler CA, Chen D, Goldenring JR, Koh T, Raychowdhury R, Coffey RJ, Ito S, Varro A, Dockray GJ, Fox JG: Synergistic interaction between hypergastrinemia and Helicobacter infection in a mouse model of gastric cancer. Gastroenterology. 2000, 118: 36-47. 10.1016/S0016-5085(00)70412-4.CrossRefPubMed
13.
go back to reference Oshima H, Matsunaga A, Fujimura T, Tsukamoto T, Taketo MM, Oshima M: Carcinogenesis in mouse stomach by simultaneous activation of the Wnt signaling and prostaglandin E2 pathway. Gastroenterology. 2006, 131: 1086-1095. 10.1053/j.gastro.2006.07.014.CrossRefPubMed Oshima H, Matsunaga A, Fujimura T, Tsukamoto T, Taketo MM, Oshima M: Carcinogenesis in mouse stomach by simultaneous activation of the Wnt signaling and prostaglandin E2 pathway. Gastroenterology. 2006, 131: 1086-1095. 10.1053/j.gastro.2006.07.014.CrossRefPubMed
14.
go back to reference Ohnishi N, Yuasa H, Tanaka S, Sawa H, Miura M, Matsui A, Higashi H, Musashi M, Iwabuchi K, Suzuki M, Yamada G, Azuma T, Hatakeyama M: Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse. Proc Natl Acad Sci U S A. 2008, 105: 1003-1008. 10.1073/pnas.0711183105.PubMedCentralCrossRefPubMed Ohnishi N, Yuasa H, Tanaka S, Sawa H, Miura M, Matsui A, Higashi H, Musashi M, Iwabuchi K, Suzuki M, Yamada G, Azuma T, Hatakeyama M: Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse. Proc Natl Acad Sci U S A. 2008, 105: 1003-1008. 10.1073/pnas.0711183105.PubMedCentralCrossRefPubMed
15.
go back to reference Nagy TA, Wroblewski LE, Wang D, Piazuelo MB, Delgado A, Romero-Gallo J, Noto J, Israel DA, Ogden SR, Correa P, Cover TL, Peek RM: beta-Catenin and p120 mediate PPARdelta-dependent proliferation induced by Helicobacter pylori in human and rodent epithelia. Gastroenterology. 2011, 141: 553-564. 10.1053/j.gastro.2011.05.004.PubMedCentralCrossRefPubMed Nagy TA, Wroblewski LE, Wang D, Piazuelo MB, Delgado A, Romero-Gallo J, Noto J, Israel DA, Ogden SR, Correa P, Cover TL, Peek RM: beta-Catenin and p120 mediate PPARdelta-dependent proliferation induced by Helicobacter pylori in human and rodent epithelia. Gastroenterology. 2011, 141: 553-564. 10.1053/j.gastro.2011.05.004.PubMedCentralCrossRefPubMed
16.
go back to reference Oguma K, Oshima H, Aoki M, Uchio R, Naka K, Nakamura S, Hirao A, Saya H, Taketo MM, Oshima M: Activated macrophages promote Wnt signalling through tumour necrosis factor-alpha in gastric tumour cells. EMBO J. 2008, 27: 1671-1681. 10.1038/emboj.2008.105.PubMedCentralCrossRefPubMed Oguma K, Oshima H, Aoki M, Uchio R, Naka K, Nakamura S, Hirao A, Saya H, Taketo MM, Oshima M: Activated macrophages promote Wnt signalling through tumour necrosis factor-alpha in gastric tumour cells. EMBO J. 2008, 27: 1671-1681. 10.1038/emboj.2008.105.PubMedCentralCrossRefPubMed
17.
go back to reference Tu S, Bhagat G, Cui G, Takaishi S, Kurt-Jones EA, Rickman B, Betz KS, Penz-Oesterreicher M, Bjorkdahl O, Fox JG, Wang TC: Overexpression of interleukin-1beta induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell. 2008, 14: 408-419. 10.1016/j.ccr.2008.10.011.PubMedCentralCrossRefPubMed Tu S, Bhagat G, Cui G, Takaishi S, Kurt-Jones EA, Rickman B, Betz KS, Penz-Oesterreicher M, Bjorkdahl O, Fox JG, Wang TC: Overexpression of interleukin-1beta induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell. 2008, 14: 408-419. 10.1016/j.ccr.2008.10.011.PubMedCentralCrossRefPubMed
18.
go back to reference Tu SP, Quante M, Bhagat G, Takaishi S, Cui G, Yang XD, Muthuplani S, Shibata W, Fox JG, Pritchard DM, Wang TC: IFN-gamma inhibits gastric carcinogenesis by inducing epithelial cell autophagy and T-cell apoptosis. Cancer Res. 2011, 71: 4247-4259. 10.1158/0008-5472.CAN-10-4009.PubMedCentralCrossRefPubMed Tu SP, Quante M, Bhagat G, Takaishi S, Cui G, Yang XD, Muthuplani S, Shibata W, Fox JG, Pritchard DM, Wang TC: IFN-gamma inhibits gastric carcinogenesis by inducing epithelial cell autophagy and T-cell apoptosis. Cancer Res. 2011, 71: 4247-4259. 10.1158/0008-5472.CAN-10-4009.PubMedCentralCrossRefPubMed
19.
go back to reference El-Omar EM, Carrington M, Chow WH, McColl KE, Bream JH, Young HA, Herrera J, Lissowska J, Yuan CC, Rothman N, Lanyon G, Martin M, Fraumeni JF, Rabkin CS: Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature. 2000, 404: 398-402. 10.1038/35006081.CrossRefPubMed El-Omar EM, Carrington M, Chow WH, McColl KE, Bream JH, Young HA, Herrera J, Lissowska J, Yuan CC, Rothman N, Lanyon G, Martin M, Fraumeni JF, Rabkin CS: Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature. 2000, 404: 398-402. 10.1038/35006081.CrossRefPubMed
20.
go back to reference Peterson AJ, Menheniott TR, O’Connor L, Walduck AK, Fox JG, Kawakami K, Minamoto T, Ong EK, Wang TC, Judd LM, Giraud AS: Helicobacter pylori infection promotes methylation and silencing of trefoil factor 2, leading to gastric tumor development in mice and humans. Gastroenterology. 2010, 139: 2005-2017. 10.1053/j.gastro.2010.08.043.PubMedCentralCrossRefPubMed Peterson AJ, Menheniott TR, O’Connor L, Walduck AK, Fox JG, Kawakami K, Minamoto T, Ong EK, Wang TC, Judd LM, Giraud AS: Helicobacter pylori infection promotes methylation and silencing of trefoil factor 2, leading to gastric tumor development in mice and humans. Gastroenterology. 2010, 139: 2005-2017. 10.1053/j.gastro.2010.08.043.PubMedCentralCrossRefPubMed
21.
go back to reference Tomita H, Takaishi S, Menheniott TR, Yang X, Shibata W, Jin G, Betz KS, Kawakami K, Minamoto T, Tomasetto C, Rio MC, Lerkowit N, Varro A, Giraud AS, Wang TC: Inhibition of gastric carcinogenesis by the hormone gastrin is mediated by suppression of TFF1 epigenetic silencing. Gastroenterology. 2011, 140: 879-891. 10.1053/j.gastro.2010.11.037.PubMedCentralCrossRefPubMed Tomita H, Takaishi S, Menheniott TR, Yang X, Shibata W, Jin G, Betz KS, Kawakami K, Minamoto T, Tomasetto C, Rio MC, Lerkowit N, Varro A, Giraud AS, Wang TC: Inhibition of gastric carcinogenesis by the hormone gastrin is mediated by suppression of TFF1 epigenetic silencing. Gastroenterology. 2011, 140: 879-891. 10.1053/j.gastro.2010.11.037.PubMedCentralCrossRefPubMed
22.
go back to reference Karam SM: Cellular origin of gastric cancer. Ann N Y Acad Sci. 2008, 1138: 162-168. 10.1196/annals.1414.023.CrossRefPubMed Karam SM: Cellular origin of gastric cancer. Ann N Y Acad Sci. 2008, 1138: 162-168. 10.1196/annals.1414.023.CrossRefPubMed
23.
go back to reference Barker N, Huch M, Kujala P, van de Wetering M, Snippert HJ, van Es JH, Sato T, Stange DE, Begthel H, van den Born M, Danenberg E, van den Brink S, Korving J, Abo A, Peters PJ, Wright N, Poulsom R, Clevers H: Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell. 2010, 6: 25-36. 10.1016/j.stem.2009.11.013.CrossRefPubMed Barker N, Huch M, Kujala P, van de Wetering M, Snippert HJ, van Es JH, Sato T, Stange DE, Begthel H, van den Born M, Danenberg E, van den Brink S, Korving J, Abo A, Peters PJ, Wright N, Poulsom R, Clevers H: Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell. 2010, 6: 25-36. 10.1016/j.stem.2009.11.013.CrossRefPubMed
24.
go back to reference Qiao XT, Ziel JW, McKimpson W, Madison BB, Todisco A, Merchant JL, Samuelson LC, Gumucio DL: Prospective identification of a multilineage progenitor in murine stomach epithelium. Gastroenterology. 2007, 133: 1989-1998. 10.1053/j.gastro.2007.09.031.PubMedCentralCrossRefPubMed Qiao XT, Ziel JW, McKimpson W, Madison BB, Todisco A, Merchant JL, Samuelson LC, Gumucio DL: Prospective identification of a multilineage progenitor in murine stomach epithelium. Gastroenterology. 2007, 133: 1989-1998. 10.1053/j.gastro.2007.09.031.PubMedCentralCrossRefPubMed
25.
go back to reference Simon E, Petke D, Boger C, Behrens HM, Warneke V, Ebert M, Rocken C: The Spatial Distribution of LGR5(+) Cells Correlates With Gastric Cancer Progression. PLoS One. 2012, 7: e35486-10.1371/journal.pone.0035486.PubMedCentralCrossRefPubMed Simon E, Petke D, Boger C, Behrens HM, Warneke V, Ebert M, Rocken C: The Spatial Distribution of LGR5(+) Cells Correlates With Gastric Cancer Progression. PLoS One. 2012, 7: e35486-10.1371/journal.pone.0035486.PubMedCentralCrossRefPubMed
26.
go back to reference Uehara T, Ma D, Yao Y, Lynch JP, Morales K, Ziober A, Feldman M, Ota H, Sepulveda AR: H. pylori infection is associated with DNA damage of Lgr5-positive epithelial stem cells in the stomach of patients with gastric cancer. Dig Dis Sci. 2012, Sept Epub ahead of print. Uehara T, Ma D, Yao Y, Lynch JP, Morales K, Ziober A, Feldman M, Ota H, Sepulveda AR: H. pylori infection is associated with DNA damage of Lgr5-positive epithelial stem cells in the stomach of patients with gastric cancer. Dig Dis Sci. 2012, Sept Epub ahead of print.
27.
go back to reference Quante M, Marrache F, Goldenring JR, Wang TC: TFF2 mRNA transcript expression marks a gland progenitor cell of the gastric oxyntic mucosa. Gastroenterology. 2010, 139: 2018-2027. 10.1053/j.gastro.2010.08.003. e2.PubMedCentralCrossRefPubMed Quante M, Marrache F, Goldenring JR, Wang TC: TFF2 mRNA transcript expression marks a gland progenitor cell of the gastric oxyntic mucosa. Gastroenterology. 2010, 139: 2018-2027. 10.1053/j.gastro.2010.08.003. e2.PubMedCentralCrossRefPubMed
28.
go back to reference Goldenring JR, Nam KT, Mills JC: The origin of pre-neoplastic metaplasia in the stomach: chief cells emerge from the Mist. Exp Cell Res. 2011, 317: 2759-2764. 10.1016/j.yexcr.2011.08.017.PubMedCentralCrossRefPubMed Goldenring JR, Nam KT, Mills JC: The origin of pre-neoplastic metaplasia in the stomach: chief cells emerge from the Mist. Exp Cell Res. 2011, 317: 2759-2764. 10.1016/j.yexcr.2011.08.017.PubMedCentralCrossRefPubMed
29.
go back to reference Nam KT, Lee HJ, Sousa JF, Weis VG, O’Neal RL, Finke PE, Romero-Gallo J, Shi G, Mills JC, Peek RM, Konieczny SF, Goldenring JR: Mature chief cells are cryptic progenitors for metaplasia in the stomach. Gastroenterology. 2010, 139: 2028-2037. 10.1053/j.gastro.2010.09.005. e9.PubMedCentralCrossRefPubMed Nam KT, Lee HJ, Sousa JF, Weis VG, O’Neal RL, Finke PE, Romero-Gallo J, Shi G, Mills JC, Peek RM, Konieczny SF, Goldenring JR: Mature chief cells are cryptic progenitors for metaplasia in the stomach. Gastroenterology. 2010, 139: 2028-2037. 10.1053/j.gastro.2010.09.005. e9.PubMedCentralCrossRefPubMed
30.
go back to reference Jang BI, Li Y, Graham DY, Cen P: The role of CD44 in the pathogenesis, diagnosis, and therapy of gastric cancer. Gut Liver. 2011, 5: 397-405. 10.5009/gnl.2011.5.4.397.PubMedCentralCrossRefPubMed Jang BI, Li Y, Graham DY, Cen P: The role of CD44 in the pathogenesis, diagnosis, and therapy of gastric cancer. Gut Liver. 2011, 5: 397-405. 10.5009/gnl.2011.5.4.397.PubMedCentralCrossRefPubMed
31.
go back to reference Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF: Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003, 100: 3983-3988. 10.1073/pnas.0530291100.PubMedCentralCrossRefPubMed Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF: Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003, 100: 3983-3988. 10.1073/pnas.0530291100.PubMedCentralCrossRefPubMed
32.
go back to reference Takaishi S, Okumura T, Tu S, Wang SS, Shibata W, Vigneshwaran R, Gordon SA, Shimada Y, Wang TC: Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells. 2009, 27: 1006-1020. 10.1002/stem.30.PubMedCentralCrossRefPubMed Takaishi S, Okumura T, Tu S, Wang SS, Shibata W, Vigneshwaran R, Gordon SA, Shimada Y, Wang TC: Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells. 2009, 27: 1006-1020. 10.1002/stem.30.PubMedCentralCrossRefPubMed
33.
go back to reference Rocco A, Liguori E, Pirozzi G, Tirino V, Compare D, Franco R, Tatangelo F, Palaia R, D’Armiento FP, Pollastrone G, Affuso A, Bottazzi EC, Masone S, Persico G, Nardone G: CD133 and CD44 cell surface markers do not identify cancer stem cells in primary human gastric tumors. J Cell Physiol. 2012, 227: 2686-2693. 10.1002/jcp.23013.CrossRefPubMed Rocco A, Liguori E, Pirozzi G, Tirino V, Compare D, Franco R, Tatangelo F, Palaia R, D’Armiento FP, Pollastrone G, Affuso A, Bottazzi EC, Masone S, Persico G, Nardone G: CD133 and CD44 cell surface markers do not identify cancer stem cells in primary human gastric tumors. J Cell Physiol. 2012, 227: 2686-2693. 10.1002/jcp.23013.CrossRefPubMed
34.
go back to reference Liu YJ, Yan PS, Li J, Jia JF: Expression and significance of CD44s, CD44v6, and nm23 mRNA in human cancer. World J Gastroenterol. 2005, 11: 6601-6606.PubMedCentralPubMed Liu YJ, Yan PS, Li J, Jia JF: Expression and significance of CD44s, CD44v6, and nm23 mRNA in human cancer. World J Gastroenterol. 2005, 11: 6601-6606.PubMedCentralPubMed
35.
go back to reference Jiang J, Zhang Y, Chuai S, Wang Z, Zheng D, Xu F, Zhang Y, Li C, Liang Y, Chen Z: Trastuzumab (herceptin) targets gastric cancer stem cells characterized by CD90 phenotype. Oncogene. 2012, 31: 671-682. 10.1038/onc.2011.282.CrossRefPubMed Jiang J, Zhang Y, Chuai S, Wang Z, Zheng D, Xu F, Zhang Y, Li C, Liang Y, Chen Z: Trastuzumab (herceptin) targets gastric cancer stem cells characterized by CD90 phenotype. Oncogene. 2012, 31: 671-682. 10.1038/onc.2011.282.CrossRefPubMed
36.
go back to reference Yang ZF, Ho DW, Ng MN, Lau CK, Yu WC, Ngai P, Chu PW, Lam CT, Poon RT, Fan ST: Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell. 2008, 13: 153-166. 10.1016/j.ccr.2008.01.013.CrossRefPubMed Yang ZF, Ho DW, Ng MN, Lau CK, Yu WC, Ngai P, Chu PW, Lam CT, Poon RT, Fan ST: Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell. 2008, 13: 153-166. 10.1016/j.ccr.2008.01.013.CrossRefPubMed
37.
go back to reference Oikonomou D, Hassan K, Kaifi JT, Fiegel HC, Schurr PG, Reichelt U, Aridome K, Yekebas EF, Mann O, Kluth D, Strate T, Izbicki JR: Thy-1 as a potential novel diagnostic marker for gastrointestinal stromal tumors. J Cancer Res Clin Oncol. 2007, 133: 951-955. 10.1007/s00432-007-0238-5.CrossRefPubMed Oikonomou D, Hassan K, Kaifi JT, Fiegel HC, Schurr PG, Reichelt U, Aridome K, Yekebas EF, Mann O, Kluth D, Strate T, Izbicki JR: Thy-1 as a potential novel diagnostic marker for gastrointestinal stromal tumors. J Cancer Res Clin Oncol. 2007, 133: 951-955. 10.1007/s00432-007-0238-5.CrossRefPubMed
38.
go back to reference Fukamachi H, Shimada S, Ito K, Ito Y, Yuasa Y: CD133 is a marker of gland-forming cells in gastric tumors and Sox17 is involved in its regulation. Cancer Sci. 2011, 102: 1313-1321. 10.1111/j.1349-7006.2011.01947.x.CrossRefPubMed Fukamachi H, Shimada S, Ito K, Ito Y, Yuasa Y: CD133 is a marker of gland-forming cells in gastric tumors and Sox17 is involved in its regulation. Cancer Sci. 2011, 102: 1313-1321. 10.1111/j.1349-7006.2011.01947.x.CrossRefPubMed
39.
go back to reference Snippert HJ, van Es JH, van den Born M, Begthel H, Stange DE, Barker N, Clevers H: Prominin-1/CD133 marks stem cells and early progenitors in mouse small intestine. Gastroenterology. 2009, 136: 2187-2194. 10.1053/j.gastro.2009.03.002. e1.CrossRefPubMed Snippert HJ, van Es JH, van den Born M, Begthel H, Stange DE, Barker N, Clevers H: Prominin-1/CD133 marks stem cells and early progenitors in mouse small intestine. Gastroenterology. 2009, 136: 2187-2194. 10.1053/j.gastro.2009.03.002. e1.CrossRefPubMed
40.
go back to reference Wang T, Ong CW, Shi J, Srivastava S, Yan B, Cheng CL, Yong WP, Chan SL, Yeoh KG, Iacopetta B, Salto-Tellez M: Sequential expression of putative stem cell markers in gastric carcinogenesis. Br J Cancer. 2011, 105: 658-665. 10.1038/bjc.2011.287.PubMedCentralCrossRefPubMed Wang T, Ong CW, Shi J, Srivastava S, Yan B, Cheng CL, Yong WP, Chan SL, Yeoh KG, Iacopetta B, Salto-Tellez M: Sequential expression of putative stem cell markers in gastric carcinogenesis. Br J Cancer. 2011, 105: 658-665. 10.1038/bjc.2011.287.PubMedCentralCrossRefPubMed
41.
go back to reference Akasaka Y, Saikawa Y, Fujita K, Kubota T, Ishikawa Y, Fujimoto A, Ishii T, Okano H, Kitajima M: Expression of a candidate marker for progenitor cells, Musashi-1, in the proliferative regions of human antrum and its decreased expression in intestinal metaplasia. Histopathology. 2005, 47: 348-356. 10.1111/j.1365-2559.2005.02223.x.CrossRefPubMed Akasaka Y, Saikawa Y, Fujita K, Kubota T, Ishikawa Y, Fujimoto A, Ishii T, Okano H, Kitajima M: Expression of a candidate marker for progenitor cells, Musashi-1, in the proliferative regions of human antrum and its decreased expression in intestinal metaplasia. Histopathology. 2005, 47: 348-356. 10.1111/j.1365-2559.2005.02223.x.CrossRefPubMed
42.
go back to reference Murata H, Tsuji S, Tsujii M, Nakamura T, Fu HY, Eguchi H, Asahi K, Okano H, Kawano S, Hayashi N: Helicobacter pylori infection induces candidate stem cell marker Musashi-1 in the human gastric epithelium. Dig Dis Sci. 2008, 53: 363-369. 10.1007/s10620-007-9858-5.CrossRefPubMed Murata H, Tsuji S, Tsujii M, Nakamura T, Fu HY, Eguchi H, Asahi K, Okano H, Kawano S, Hayashi N: Helicobacter pylori infection induces candidate stem cell marker Musashi-1 in the human gastric epithelium. Dig Dis Sci. 2008, 53: 363-369. 10.1007/s10620-007-9858-5.CrossRefPubMed
43.
go back to reference Fukui T, Kishimoto M, Nakajima A, Yamashina M, Nakayama S, Kusuda T, Sakaguchi Y, Yoshida K, Uchida K, Nishio A, Matsuzaki K, Okazaki K: The specific linker phosphorylation of Smad2/3 indicates epithelial stem cells in stomach; particularly increasing in mucosae of Helicobacter-associated gastritis. J Gastroenterol. 2011, 46: 456-468. 10.1007/s00535-010-0364-8.CrossRefPubMed Fukui T, Kishimoto M, Nakajima A, Yamashina M, Nakayama S, Kusuda T, Sakaguchi Y, Yoshida K, Uchida K, Nishio A, Matsuzaki K, Okazaki K: The specific linker phosphorylation of Smad2/3 indicates epithelial stem cells in stomach; particularly increasing in mucosae of Helicobacter-associated gastritis. J Gastroenterol. 2011, 46: 456-468. 10.1007/s00535-010-0364-8.CrossRefPubMed
44.
go back to reference Gerbe F, Brulin B, Makrini L, Legraverend C, Jay P: DCAMKL-1 expression identifies Tuft cells rather than stem cells in the adult mouse intestinal epithelium. Gastroenterology. 2009, 137: 2179-2180. 10.1053/j.gastro.2009.06.072. author reply 2180–1.CrossRefPubMed Gerbe F, Brulin B, Makrini L, Legraverend C, Jay P: DCAMKL-1 expression identifies Tuft cells rather than stem cells in the adult mouse intestinal epithelium. Gastroenterology. 2009, 137: 2179-2180. 10.1053/j.gastro.2009.06.072. author reply 2180–1.CrossRefPubMed
45.
go back to reference Schmuck R, Warneke V, Behrens HM, Simon E, Weichert W, Rocken C: Genotypic and phenotypic characterization of side population of gastric cancer cell lines. Am J Pathol. 2011, 178: 1792-1804. 10.1016/j.ajpath.2010.12.043.PubMedCentralCrossRefPubMed Schmuck R, Warneke V, Behrens HM, Simon E, Weichert W, Rocken C: Genotypic and phenotypic characterization of side population of gastric cancer cell lines. Am J Pathol. 2011, 178: 1792-1804. 10.1016/j.ajpath.2010.12.043.PubMedCentralCrossRefPubMed
46.
go back to reference Fraga MF, Agrelo R, Esteller M: Cross-talk between aging and cancer: the epigenetic language. Ann N Y Acad Sci. 2007, 1100: 60-74. 10.1196/annals.1395.005.CrossRefPubMed Fraga MF, Agrelo R, Esteller M: Cross-talk between aging and cancer: the epigenetic language. Ann N Y Acad Sci. 2007, 1100: 60-74. 10.1196/annals.1395.005.CrossRefPubMed
47.
go back to reference Necchi V, Candusso ME, Tava F, Luinetti O, Ventura U, Fiocca R, Ricci V, Solcia E: Intracellular, intercellular, and stromal invasion of gastric mucosa, preneoplastic lesions, and cancer by Helicobacter pylori. Gastroenterology. 2007, 132: 1009-1023. 10.1053/j.gastro.2007.01.049.CrossRefPubMed Necchi V, Candusso ME, Tava F, Luinetti O, Ventura U, Fiocca R, Ricci V, Solcia E: Intracellular, intercellular, and stromal invasion of gastric mucosa, preneoplastic lesions, and cancer by Helicobacter pylori. Gastroenterology. 2007, 132: 1009-1023. 10.1053/j.gastro.2007.01.049.CrossRefPubMed
48.
go back to reference Oh JD, Karam SM, Gordon JI: Intracellular Helicobacter pylori in gastric epithelial progenitors. Proc Natl Acad Sci U S A. 2005, 102: 5186-5191. 10.1073/pnas.0407657102.PubMedCentralCrossRefPubMed Oh JD, Karam SM, Gordon JI: Intracellular Helicobacter pylori in gastric epithelial progenitors. Proc Natl Acad Sci U S A. 2005, 102: 5186-5191. 10.1073/pnas.0407657102.PubMedCentralCrossRefPubMed
49.
go back to reference Giannakis M, Chen SL, Karam SM, Engstrand L, Gordon JI: Helicobacter pylori evolution during progression from chronic atrophic gastritis to gastric cancer and its impact on gastric stem cells. Proc Natl Acad Sci U S A. 2008, 105: 4358-4363. 10.1073/pnas.0800668105.PubMedCentralCrossRefPubMed Giannakis M, Chen SL, Karam SM, Engstrand L, Gordon JI: Helicobacter pylori evolution during progression from chronic atrophic gastritis to gastric cancer and its impact on gastric stem cells. Proc Natl Acad Sci U S A. 2008, 105: 4358-4363. 10.1073/pnas.0800668105.PubMedCentralCrossRefPubMed
50.
go back to reference Varon C, Dubus P, Mazurier F, Asencio C, Chambonnier L, Ferrand J, Giese A, Senant-Dugot N, Carlotti M, Megraud F: Helicobacter pylori infection recruits bone marrow-derived cells that participate in gastric preneoplasia in mice. Gastroenterology. 2012, 142: 281-291. 10.1053/j.gastro.2011.10.036.CrossRefPubMed Varon C, Dubus P, Mazurier F, Asencio C, Chambonnier L, Ferrand J, Giese A, Senant-Dugot N, Carlotti M, Megraud F: Helicobacter pylori infection recruits bone marrow-derived cells that participate in gastric preneoplasia in mice. Gastroenterology. 2012, 142: 281-291. 10.1053/j.gastro.2011.10.036.CrossRefPubMed
51.
go back to reference Niwa T, Tsukamoto T, Toyoda T, Mori A, Tanaka H, Maekita T, Ichinose M, Tatematsu M, Ushijima T: Inflammatory processes triggered by Helicobacter pylori infection cause aberrant DNA methylation in gastric epithelial cells. Cancer Res. 2010, 70: 1430-1440. 10.1158/0008-5472.CAN-09-2755.CrossRefPubMed Niwa T, Tsukamoto T, Toyoda T, Mori A, Tanaka H, Maekita T, Ichinose M, Tatematsu M, Ushijima T: Inflammatory processes triggered by Helicobacter pylori infection cause aberrant DNA methylation in gastric epithelial cells. Cancer Res. 2010, 70: 1430-1440. 10.1158/0008-5472.CAN-09-2755.CrossRefPubMed
53.
go back to reference Cabarcas SM, Mathews LA, Farrar WL: The cancer stem cell niche–there goes the neighborhood?. Int J Cancer. 2011, 129: 2315-2327. 10.1002/ijc.26312.CrossRefPubMed Cabarcas SM, Mathews LA, Farrar WL: The cancer stem cell niche–there goes the neighborhood?. Int J Cancer. 2011, 129: 2315-2327. 10.1002/ijc.26312.CrossRefPubMed
54.
go back to reference Korkaya H, Paulson A, Charafe-Jauffret E, Ginestier C, Brown M, Dutcher J, Clouthier SG, Wicha MS: Regulation of mammary stem/progenitor cells by PTEN/Akt/beta-catenin signaling. PLoS Biol. 2009, 7: e1000121-10.1371/journal.pbio.1000121.PubMedCentralCrossRefPubMed Korkaya H, Paulson A, Charafe-Jauffret E, Ginestier C, Brown M, Dutcher J, Clouthier SG, Wicha MS: Regulation of mammary stem/progenitor cells by PTEN/Akt/beta-catenin signaling. PLoS Biol. 2009, 7: e1000121-10.1371/journal.pbio.1000121.PubMedCentralCrossRefPubMed
55.
go back to reference Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, Suri P, Wicha MS: Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 2006, 66: 6063-6071. 10.1158/0008-5472.CAN-06-0054.PubMedCentralCrossRefPubMed Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, Suri P, Wicha MS: Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 2006, 66: 6063-6071. 10.1158/0008-5472.CAN-06-0054.PubMedCentralCrossRefPubMed
56.
go back to reference Iliopoulos D, Hirsch HA, Struhl K: An epigenetic switch involving NF-kappaB, Lin28, Let-7 Micro RNA, and IL6 links inflammation to cell transformation. Cell. 2009, 139: 693-706. 10.1016/j.cell.2009.10.014.PubMedCentralCrossRefPubMed Iliopoulos D, Hirsch HA, Struhl K: An epigenetic switch involving NF-kappaB, Lin28, Let-7 Micro RNA, and IL6 links inflammation to cell transformation. Cell. 2009, 139: 693-706. 10.1016/j.cell.2009.10.014.PubMedCentralCrossRefPubMed
57.
go back to reference Okumura T, Wang SS, Takaishi S, Tu SP, Ng V, Ericksen RE, Rustgi AK, Wang TC: Identification of a bone marrow-derived mesenchymal progenitor cell subset that can contribute to the gastric epithelium. Lab Invest. 2009, 89 (12): 1410-1422. 10.1038/labinvest.2009.88.PubMedCentralCrossRefPubMed Okumura T, Wang SS, Takaishi S, Tu SP, Ng V, Ericksen RE, Rustgi AK, Wang TC: Identification of a bone marrow-derived mesenchymal progenitor cell subset that can contribute to the gastric epithelium. Lab Invest. 2009, 89 (12): 1410-1422. 10.1038/labinvest.2009.88.PubMedCentralCrossRefPubMed
58.
go back to reference Gonda TA, Tu S, Wang TC: Chronic inflammation, the tumor microenvironment and carcinogenesis. Cell Cycle. 2009, 8: 2005-2013. 10.4161/cc.8.13.8985.CrossRefPubMed Gonda TA, Tu S, Wang TC: Chronic inflammation, the tumor microenvironment and carcinogenesis. Cell Cycle. 2009, 8: 2005-2013. 10.4161/cc.8.13.8985.CrossRefPubMed
59.
go back to reference Ferrand J, Lehours P, Schmid-Alliana A, Megraud F, Varon C: Helicobacter pylori infection of gastrointestinal epithelial cells in vitro induces mesenchymal stem cell migration through an NF-kappaB-dependent pathway. PLoS One. 2011, 6: e29007-10.1371/journal.pone.0029007.PubMedCentralCrossRefPubMed Ferrand J, Lehours P, Schmid-Alliana A, Megraud F, Varon C: Helicobacter pylori infection of gastrointestinal epithelial cells in vitro induces mesenchymal stem cell migration through an NF-kappaB-dependent pathway. PLoS One. 2011, 6: e29007-10.1371/journal.pone.0029007.PubMedCentralCrossRefPubMed
60.
go back to reference Grivennikov SI, Karin M: Dangerous liaisons: STAT3 and NF-kappaB collaboration and crosstalk in cancer. Cytokine Growth Factor Rev. 2010, 21: 11-19. 10.1016/j.cytogfr.2009.11.005.PubMedCentralCrossRefPubMed Grivennikov SI, Karin M: Dangerous liaisons: STAT3 and NF-kappaB collaboration and crosstalk in cancer. Cytokine Growth Factor Rev. 2010, 21: 11-19. 10.1016/j.cytogfr.2009.11.005.PubMedCentralCrossRefPubMed
Metadata
Title
Helicobacter pylori infection induced gastric cancer; advance in gastric stem cell research and the remaining challenges
Authors
Song-Ze Ding
Peng-Yuan Zheng
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2012
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/1757-4749-4-18

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