17β-estradiol and tamoxifen prevent gastric cancer by modulating leukocyte recruitment and oncogenic pathways in helicobacter Pylori-infected INS-GAS male mice

Cancer Prevention Research

Volumn 4, Issue 9, 2011, Pages 1426-1435

  Sheh, Alexander ^a,b   Ge, Zhongming ^a   Parry, Nicola M A ^a   Muthupalani, Sureshkumar ^a   Rager, Julia E ^c   Raczynski, Arkadiusz R ^b   Mobley, Melissa W ^a   McCabe, Amanda F ^a   Fry, Rebecca C ^c   Wang, Timothy C ^d   Fox, James G ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c University of North Carolina at Chapel Hill   (United States)

^d Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; ESTRADIOL; ESTROGEN; MESSENGER RNA; NE 121; NE 361; TAMOXIFEN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER RISK; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEREGULATION; DRUG MECHANISM; EXPERIMENTAL MODEL; FEMALE; GENE EXPRESSION REGULATION; HELICOBACTER INFECTION; HISTOPATHOLOGY; IMMUNOCOMPETENT CELL; LEUKOCYTE MIGRATION; MALE; MOUSE; MOUSE STRAIN; NEUTROPHIL CHEMOTAXIS; NEUTROPHIL COUNT; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SEX DIFFERENCE; SIGNAL TRANSDUCTION; STOMACH CANCER; STOMACH CARCINOGENESIS;

ANIMALS; ANTICARCINOGENIC AGENTS; CHEMOKINES; CYTOKINES; ESTRADIOL; FEMALE; HELICOBACTER PYLORI; HUMANS; IMMUNE SYSTEM; LEUKOCYTES; MALE; MICE; PLACEBOS; STOMACH NEOPLASMS; TAMOXIFEN; TIME FACTORS;

EID: 80052599040     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-11-0219     Document Type: Article

References (49)

1. Chandanos E., Lagergren J. Oestrogen and the enigmatic male predominance of gastric cancer. Eur J Cancer 2008;44:2397-2403
2. Fox J.G., Wang T.C. Inflammation, atrophy, and gastric cancer. J Clin Invest 2007;117:60-69 (Pubitemid 46048450)
3. Sipponen P., Correa P. Delayed rise in incidence of gastric cancer in females results in unique sex ratio (M/F) pattern: Etiologic hypothesis. Gastric Cancer 2002;5:213-219 (Pubitemid 36605884)
4. Chandanos E., Lindblad M., Jia C., Rubio C.A., Ye W., Lagergren J. Tamoxifen exposure and risk of oesophageal and gastric adenocarcinoma: A population-based cohort study of breast cancer patients in Sweden. Br J Cancer 2006;95:118-122 (Pubitemid 43980565)
5. Rutqvist L.E., Johansson H., Signomklao T., Johansson U., Fornander T., Wilking N. Adjuvant tamoxifen therapy for early stage breast cancer and second primary malignancies. Stockholm Breast Cancer Study Group. J Natl Cancer Inst 1995;87:645-651
6. Curtis R.E., Boice J.D. Jr, Shriner D.A., Hankey B.F., Fraumeni J.F. Jr. Second cancers after adjuvant tamoxifen therapy for breast cancer. J Natl Cancer Inst 1996;88:832-834 (Pubitemid 26187392)
7. Wang T.C., Dangler C.A., Chen D., Goldenring J.R., Koh T., Raychowdhury R., et al. Synergistic interaction between hypergastrinemia and Helicobacter infection in a mouse model of gastric cancer. Gastroenterology 2000;118:36-47. (Pubitemid 30020371)
8. Fox J.G., Rogers A.B., Ihrig M., Taylor N.S., Whary M.T., Dockray G., et al. Helicobacter pylori-associated gastric cancer in INS-GAS mice is gender specific. Cancer Res 2003;63:942-950 (Pubitemid 36278423)
9. Ohtani M., Garcia A., Rogers A.B., Ge Z., Taylor N.S., Xu S., et al. Protective role of 17{beta}-estradiol against the development of Helicobacter pylori-induced gastric cancer in INS-GAS mice. Carcinogenesis 2007;28:2597-2604 (Pubitemid 350238963)
10. Correa P. Human gastric carcinogenesis: A multistep and multifactorial process-first American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 1992;52:6735-6740 (Pubitemid 23006271)
11. Lee C.W., Rickman B., Rogers A.B., Ge Z., Wang T.C., Fox J.G. Helicobacter pylori eradication prevents progression of gastric cancer in hypergastrinemic INS-GAS mice. Cancer Res 2008;68:3540-3548
12. Ohtani M., Ge Z., Garcia A., Rogers A.B., Muthupalani S., Taylor N.S., et al. 17{beta}-estradiol suppresses Helicobacter pylori-induced gastric pathology in male hypergastrinemic INS-GAS mice. Carcinogenesis 2011; doi:10.1093/carcin/bgr072.
13. Rogers A.B., Taylor N.S., Whary M.T., Stefanich E.D., Wang T.C., Fox J.G. Helicobacter pylori but not high salt induces gastric intraepithelial neoplasia in B6129 mice. Cancer Res 2005;65:10709-10715 (Pubitemid 41713338)
14. Boivin G.P., Washington K., Yang K., Ward J.M., Pretlow T.P., Russell R., et al. Pathology of mouse models of intestinal cancer: Consensus report and recommendations. Gastroenterology 2003;124:762-777 (Pubitemid 36268493)
15. Rogers A.B., Cormier K.S., Fox J.G. Thiol-reactive compounds prevent nonspecific antibody binding in immunohistochemistry. Lab Invest 2006;86:526-533
16. Bergin I.L., Sheppard B.J., Fox J.G. Helicobacter pylori infection and high dietary salt independently induce atrophic gastritis and intestinal metaplasia in commercially available outbred Mongolian gerbils. Dig Dis Sci 2003;48:475-485 (Pubitemid 36324153)
17. Irizarry R.A., Bolstad B.M., Collin F., Cope L.M., Hobbs B., Speed T.P. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 2003;31:e15.
18. Storey J.D. The positive false discovery rate: A Bayesian interpretation and the q-value. Ann Stat 2003;31:23.
19. Theoharides T.C., Pang X., Letourneau R., Sant G.R. Interstitial cystitis: A neuroimmunoendocrine disorder. Ann N Y Acad Sci 1998;840: 619-634 (Pubitemid 28302088)
20. Straub R.H. The complex role of estrogens in inflammation. Endocr Rev 2007;28:521-574 (Pubitemid 47236336)
21. Saqui-Salces M., Rocha-Gutierrez B.L., Barrios-Payan J.A., Ruiz-Palacios G., Camacho-Arroyo I., Gamboa-Dominguez A. Effects of estradiol and progesterone on gastric mucosal response to early Helicobacter pylori infection in female gerbils. Helicobacter 2006; 11:123-130 (Pubitemid 43363311)
22. Jordan V.C., Gapstur S., Morrow M. Selective estrogen receptor modulation and reduction in risk of breast cancer, osteoporosis, and coronary heart disease. J Natl Cancer Inst 2001;93:1449-1457 (Pubitemid 32982673)
23. Gottardis M.M., Robinson S.P., Jordan V.C. Estradiol-stimulated growth of MCF-7 tumors implanted in athymic mice: A model to study the tumoristatic action of tamoxifen. J Steroid Biochem 1988;30: 311-314
24. Robinson S.P., Langan-Fahey S.M., Johnson D.A., Jordan V.C. Metabolites, pharmacodynamics, and pharmacokinetics of tamoxifen in rats and mice compared to the breast cancer patient. Drug Metab Dispos 1991;19:36-43.
25. Haghnegahdar H., Du J., Wang D., Strieter R.M., Burdick M.D., Nanney L.B., et al. The tumorigenic and angiogenic effects of MGSA/GRO proteins in melanoma. J Leukoc Biol 2000;67:53-62. (Pubitemid 30046818)
26. Boisvert W.A., Rose D.M., Johnson K.A., Fuentes M.E., Lira S.A., Curtiss L.K., et al. Up-regulated expression of the CXCR2 ligand KC/GROalpha in atherosclerotic lesions plays a central role in macrophage accumulation and lesion progression. Am J Pathol 2006;168: 1385-1395
27. Okumura T., Ericksen R.E., Takaishi S., Wang S.S., Dubeykovskiy Z., Shibata W., et al. K-ras mutation targeted to gastric tissue progenitor cells results in chronic inflammation, an altered microenvironment, and progression to intraepithelial neoplasia. Cancer Res 2010;70: 8435-8445
28. Lei Z.B., Fu X.J., Lu Z.T., Wang B.C., Liu X.L., You N.Z. Effect of estradiol on chemokine receptor CXCR2 expression in rats: Implications for atherosclerosis. Acta Pharmacol Sin 2003;24:670-674
29. Lei Z.B., Li X.Y., Wang B.C., Yang Y.F., You N.Z., Sun J. Regulation of growth-regulated oncogene alpha expression by estrogen in human endothelial cells. Acta Pharmacol Sin 2001;22:1003-1006 (Pubitemid 33593643)
30. Ghisletti S., Meda C., Maggi A., Vegeto E. 17{beta}-estradiol inhibits inflammatory gene expression by controlling NF-kappaB intracellular localization. Mol Cell Biol 2005;25:2957-2968 (Pubitemid 40464301)
31. Junnila S., Kokkola A., Mizuguchi T., Hirata K., Karjalainen-Lindsberg M.L., Puolakkainen P., et al. Gene expression analysis identifies overexpression of CXCL1, SPARC, SPP1, and SULF1 in gastric cancer. Genes Chromosomes Cancer 2010;49:28-39.
32. Jung J.J., Noh S., Jeung H.C., Jung M., Kim T.S., Noh S.H., et al. Chemokine growth-regulated oncogene 1 as a putative biomarker for gastric cancer progression. Cancer Sci 2010;101:2200-2206
33. Taguchi A., Ohmiya N., Shirai K., Mabuchi N., Itoh A., Hirooka Y., et al. Interleukin-8 promoter polymorphism increases the risk of atrophic gastritis and gastric cancer in Japan. Cancer Epidemiol Biomarkers Prev 2005;14:2487-2493 (Pubitemid 41752706)
34. Eck M., Schmausser B., Scheller K., Toksoy A., Kraus M., Menzel T., et al. CXC chemokines Gro(alpha)/IL-8 and IP-10/MIG in Helicobacter pylori gastritis. Clin Exp Immunol 2000;122:192-199
35. Dinarello C.A. Immunological and inflammatory functions of the interleukin- 1 family. Annu Rev Immunol 2009;27:519-550
36. Forster R., Davalos-Misslitz A.C., Rot A. CCR7 and its ligands: Balancing immunity and tolerance. Nat Rev Immunol 2008;8:362-371 (Pubitemid 351595218)
37. Serbina N.V., Jia T., Hohl T.M., Pamer E.G. Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol 2008;26:421-452 (Pubitemid 351600381)
38. Martinez F.O., Helming L., Gordon S. Alternative activation of macrophages: An immunologic functional perspective. Annu Rev Immunol 2009;27:451-483
39. Gilliver S.C. Sex steroids as inflammatory regulators. J Steroid Biochem Mol Biol 2010;120:105-115
40. Naugler W.E., Sakurai T., Kim S., Maeda S., Kim K., Elsharkawy A.M., et al. Gender disparity in liver cancer due to sex differences in MyD88- dependent IL-6 production. Science 2007;317:121-124 (Pubitemid 47056470)
41. Seruga B., Zhang H., Bernstein L.J., Tannock I.F. Cytokines and their relationship to the symptoms and outcome of cancer. Nat Rev Cancer 2008;8:887-899
42. Dano K., Behrendt N., Hoyer-Hansen G., Johnsen M., Lund L.R., Ploug M., et al. Plasminogen activation and cancer. Thromb Haemost 2005; 93:676-681 (Pubitemid 40485402)
43. Kenny S., Duval C., Sammut S.J., Steele I., Pritchard D.M., Atherton J.C., et al. Increased expression of the urokinase plasminogen activator system by Helicobacter pylori in gastric epithelial cells. Am J Physiol Gastrointest Liver Physiol 2008;295:G431-G441
44. Kaneko T., Konno H., Baba M., Tanaka T., Nakamura S. Urokinase-type plasminogen activator expression correlates with tumor angiogenesis and poor outcome in gastric cancer. Cancer Sci 2003;94:43-49 (Pubitemid 36575857)
45. Yang J., Duh E.J., Caldwell R.B., Behzadian M.A. Antipermeability function of PEDF involves blockade of the MAP kinase/GSK/beta-catenin signaling pathway and uPAR expression. Invest Ophthalmol Vis Sci 2010;51:3273-3280
46. Franco A.T., Israel D.A., Washington M.K., Krishna U., Fox J.G., Rogers A.B., et al. Activation of beta-catenin by carcinogenic Helicobacter pylori. Proc Natl Acad Sci U S A 2005;102:10646-10651 (Pubitemid 41061608)
47. Golan T., Yaniv A., Bafico A., Liu G., Gazit A. The human Frizzled 6 (HFz6) acts as a negative regulator of the canonical Wnt. beta-catenin signaling cascade. J Biol Chem 2004;279:14879-14888 (Pubitemid 38618878)
48. Nojima M., Suzuki H., Toyota M., Watanabe Y., Maruyama R., Sasaki S., et al. Frequent epigenetic inactivation of SFRP genes and constitutive activation of Wnt signaling in gastric cancer. Oncogene 2007;26: 4699-4713 (Pubitemid 47067406)
49. Hayashi K., Spencer T.E. WNT pathways in the neonatal ovine uterus: Potential specification of endometrial gland morphogenesis by SFRP2. Biol Reprod 2006;74:721-733