The molecular pathogenesis of STAT3-driven gastric tumourigenesis in mice is independent of IL-17

Journal of Pathology

Volumn 225, Issue 2, 2011, Pages 255-264

  Kennedy, Catherine L ^a   Najdovska, Meri ^a   Jones, Gareth W ^a,b   McLeod, Louise ^a   Hughes, Norman R ^c   Allison, Cody ^a   Huey Ooi, Chia ^d   Tan, Patrick ^d,e   Ferrero, Richard L ^a   Jones, Simon A ^b   Dev, Anouk ^a   Sievert, William ^a   Bhathal, Prithi S ^c   Jenkins, Brendan J ^a  

^a MONASH UNIVERSITY   (Australia)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d DUKE NUS MEDICAL SCHOOL   (Singapore)

^e GENOME INSTITUTE OF SINGAPORE   (Singapore)

Author keywords

gastric cancer; gastritis; gp130; IL 17A; IL 6; STAT3

Indexed keywords

GLYCOPROTEIN GP 130; INTERLEUKIN 11; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 6; STAT3 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; CANCER GROWTH; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; GASTRITIS; GENE EXPRESSION; HELICOBACTER PYLORI; HUMAN; HUMAN TISSUE; IMMUNOPATHOGENESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH BIOPSY; STOMACH CARCINOGENESIS; T LYMPHOCYTE; TH17 CELL; UPREGULATION; WILD TYPE;

ANIMALS; CELL DIFFERENTIATION; CELL SEPARATION; CELL TRANSFORMATION, NEOPLASTIC; FLOW CYTOMETRY; GASTRITIS; GENE KNOCK-IN TECHNIQUES; HUMANS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-17; INTERLEUKIN-6; MICE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STAT3 TRANSCRIPTION FACTOR; STOMACH NEOPLASMS; TH17 CELLS;

EID: 80052510422     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2933     Document Type: Article

References (51)

1. Hohenberger P, Gretschel S,. Gastric cancer. Lancet 2003; 362: 305-315. (Pubitemid 36936845)
2. Fox JG, Wang TC,. Inflammation, atrophy, and gastric cancer. J Clin Invest 2007; 117: 60-69. (Pubitemid 46048450)
3. Korn T, Bettelli E, Oukka M, et al., IL-17 and Th17 Cells. Annu Rev Immunol 2009; 27: 485-517.
4. Peck A, Mellins ED,. Precarious balance: Th17 cells in host defense. Infect Immun 2010; 78: 32-38.
5. Pappu R, Ramirez-Carrozzi V, Ota N, et al., The IL-17 family cytokines in immunity and disease. J Clin Immunol 2010; 30: 185-195.
6. Maniati E, Soper R, Hagemann T,. Up for mischief? IL-17/Th17 in the tumour microenvironment. Oncogene 2010; 29: 5653-5662.
7. Kimura A, Kishimoto T,. IL-6: regulator of Treg/Th17 balance. Eur J Immunol 2010; 40: 1830-1835.
8. McGeachy MJ, Chen Y, Tato CM, et al., The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat Immunol 2009; 10: 314-324.
9. Korn T, Bettelli E, Gao W, et al., IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 2007; 448: 484-487. (Pubitemid 47123515)
10. Coquet JM, Chakravarti S, Smyth MJ, et al., Cutting edge: IL-21 is not essential for Th17 differentiation or experimental autoimmune encephalomyelitis. J Immunol 2008; 180: 7097-7101.
11. Chen Z, Laurence A, O'Shea JJ,. Signal transduction pathways and transcriptional regulation in the control of Th17 differentiation. Semin Immunol 2007; 19: 400-408.
12. Luzza F, Parrello T, Monteleone G, et al., Up-regulation of IL-17 is associated with bioactive IL-8 expression in Helicobacter pylori-infected human gastric mucosa. J Immunol 2000; 165: 5332-5337.
13. Mizuno T, Ando T, Nobata K, et al., Interleukin-17 levels in Helicobacter pylori-infected gastric mucosa and pathologic sequelae of colonization. World J Gastroenterol 2005; 11: 6305-6311. (Pubitemid 43013998)
14. Shibata T, Tahara T, Hirata I, et al., Genetic polymorphism of interleukin-17A and -17F genes in gastric carcinogenesis. Hum Immunol 2009; 70: 547-551.
15. Zhang B, Rong G, Wei H, et al., The prevalence of Th17 cells in patients with gastric cancer. Biochem Biophys Res Commun 2008; 374: 533-537.
16. + regulatory T cells in tumor-infiltrating lymphocytes, tumor-draining lymph nodes and peripheral blood lymphocytes in patients with gastric cancer. Cancer Sci 2010; 101: 1947-1954.
17. Heinrich PC, Behrmann I, Muller-Newen G, et al., Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem J 1998; 334 (pt 2): 297-314. (Pubitemid 28448572)
18. Tebbutt NC, Giraud AS, Inglese M, et al., Reciprocal regulation of gastrointestinal homeostasis by SHP2 and STAT-mediated trefoil gene activation in gp130 mutant mice. Nat Med 2002; 8: 1089-1097. (Pubitemid 35175963)
19. Nicholson SE, De Souza D, Fabri LJ, et al., Suppressor of cytokine signaling-3 preferentially binds to the SHP-2-binding site on the shared cytokine receptor subunit gp130. Proc Natl Acad Sci USA 2000; 97: 6493-6498. (Pubitemid 30412741)
20. Jenkins BJ, Grail D, Nheu T, et al., Hyperactivation of Stat3 in gp130 mutant mice promotes gastric hyperproliferation and desensitizes TGF-β signaling. Nat Med 2005; 11: 845-852. (Pubitemid 41161116)
21. Ernst M, Najdovska M, Grail D, et al., STAT3 and STAT1 mediate IL-11-dependent and inflammation-associated gastric tumorigenesis in gp130 receptor mutant mice. J Clin Invest 2008; 118: 1727-1738. (Pubitemid 351632376)
22. Gong W, Wang L, Yao JC, et al., Expression of activated signal transducer and activator of transcription 3 predicts expression of vascular endothelial growth factor in and angiogenic phenotype of human gastric cancer. Clin Cancer Res 2005; 11: 1386-1393. (Pubitemid 40315217)
23. Ellmark P, Ingvarsson J, Carlsson A, et al., Identification of protein expression signatures associated with Helicobacter pylori infection and gastric adenocarcinoma using recombinant antibody microarrays. Mol Cell Proteom 2006; 5: 1638-1646. (Pubitemid 44480391)
24. Dixon MF, Genta RM, Yardley JH, et al., Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston, 1994. Am J Surg Pathol 1996; 20: 1161-1181.
25. Boonjakuakul JK, Canfield DR, Solnick JV,. Comparison of Helicobacter pylori virulence gene expression in vitro and in the Rhesus macaque. Infect Immun 2005; 73: 4895-4904. (Pubitemid 41105646)
26. Jenkins BJ, Roberts AW, Greenhill CJ, et al., Pathologic consequences of STAT3 hyperactivation by IL-6 and IL-11 during hematopoiesis and lymphopoiesis. Blood 2007; 109: 2380-2388. (Pubitemid 46425878)
27. Nakae S, Komiyama Y, Nambu A, et al., Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 2002; 17: 375-387. (Pubitemid 35279557)
28. Viala J, Chaput C, Boneca IG, et al., Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol 2004; 5: 1166-1174. (Pubitemid 39549631)
29. Bancroft JD, Stevens A,. Theory and Practice of Histological Techniques, 3rd edn. Churchill Livingstone: Edinburgh, New York, 1990.
30. Yang XO, Chang SH, Park H, et al., Regulation of inflammatory responses by IL-17F. J Exp Med 2008; 205: 1063-1075. (Pubitemid 351679682)
31. Park H, Li Z, Yang XO, et al., A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005; 6: 1133-1141. (Pubitemid 41541791)
32. Kryczek I, Wei S, Zou L, et al., Cutting edge: Th17 and regulatory T cell dynamics and the regulation by IL-2 in the tumor microenvironment. J Immunol 2007; 178: 6730-6733. (Pubitemid 46847396)
33. Ooi CH, Ivanova T, Wu J, et al., Oncogenic pathway combinations predict clinical prognosis in gastric cancer. PLoS Genet 2009; 5: e1000676.
34. Kido S, Kitadai Y, Hattori N, et al., Interleukin 8 and vascular endothelial growth factor-prognostic factors in human gastric carcinomas? Eur J Cancer 2001; 37: 1482-1487. (Pubitemid 32744677)
35. Meimarakis G, Winter H, Assmann I, et al., Helicobacter pylori as a prognostic indicator after curative resection of gastric carcinoma: a prospective study. Lancet Oncol 2006; 7: 211-222. (Pubitemid 43286451)
36. Lee WJ, Lin JT, Shun CT, et al., Comparison between resectable gastric adenocarcinomas seropositive and seronegative for Helicobacter pylori. Br J Surg 1995; 82: 802-805.
37. Algood HM, Allen SS, Washington MK, et al., Regulation of gastric B cell recruitment is dependent on IL-17 receptor A signaling in a model of chronic bacterial infection. J Immunol 2009; 183: 5837-5846.
38. Otani K, Watanabe T, Tanigawa T, et al., Anti-inflammatory effects of IL-17A on Helicobacter pylori-induced gastritis. Biochem Biophys Res Commun 2009; 382: 252-258.
39. Shiomi S, Toriie A, Imamura S, et al., IL-17 is involved in Helicobacter pylori-induced gastric inflammatory responses in a mouse model. Helicobacter 2008; 13: 518-524.
40. + Th with a minimum effect on that of Treg in the steady state. Int Immunol 2007; 19: 695-702. (Pubitemid 47078714)
41. Harris TJ, Grosso JF, Yen HR, et al., Cutting edge: An in vivo requirement for STAT3 signaling in TH17 development and TH17-dependent autoimmunity. J Immunol 2007; 179: 4313-4317.
42. Chen Z, Laurence A, Kanno Y, et al., Selective regulatory function of Socs3 in the formation of IL-17-secreting T cells. Proc Natl Acad Sci USA 2006; 103: 8137-8142. (Pubitemid 43801065)
43. Shi Y, Liu XF, Zhuang Y, et al., Helicobacter pylori-induced Th17 responses modulate Th1 cell responses, benefit bacterial growth, and contribute to pathology in mice. J Immunol 2010; 184: 5121-5129.
44. Kortylewski M, Xin H, Kujawski M, et al., Regulation of the IL-23 and IL-12 balance by Stat3 signaling in the tumor microenvironment. Cancer Cell 2009; 15: 114-123.
45. Wang L, Yi T, Kortylewski M, et al., IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway. J Exp Med 2009; 206: 1457-1464.
46. Wang L, Yi T, Zhang W, et al., IL-17 enhances tumor development in carcinogen-induced skin cancer. Cancer Res 2010; 70: 10112-10120.
47. Becker C, Fantini MC, Schramm C, et al., TGF-β suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling. Immunity 2004; 21: 491-501. (Pubitemid 39370505)
48. Wu S, Rhee KJ, Albesiano E, et al., A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 2009; 15: 1016-1022.
49. Kobayashi T, Okamoto S, Hisamatsu T, et al., IL23 differentially regulates the Th1/Th17 balance in ulcerative colitis and Crohn's disease. Gut 2008; 57: 1682-1689.
50. Hou L, El-Omar EM, Chen J, et al., Polymorphisms in Th1-type cell-mediated response genes and risk of gastric cancer. Carcinogenesis 2007; 28: 118-123. (Pubitemid 44942634)
51. Stoicov C, Fan X, Liu JH, et al., T-bet knockout prevents Helicobacter felis-induced gastric cancer. J Immunol 2009; 183: 642-649.