Interleukin-6 Mediates Epithelial-Stromal Interactions and Promotes Gastric Tumorigenesis

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Kinoshita, Hiroto ^a   Hirata, Yoshihiro ^a   Nakagawa, Hayato ^a   Sakamoto, Kei ^b   Hayakawa, Yoku ^a   Takahashi, Ryota ^a   Nakata, Wachiko ^a   Sakitani, Kosuke ^a   Serizawa, Takako ^a   Hikiba, Yohko ^b   Akanuma, Masao ^b   Shibata, Wataru ^c   Maeda, Shin ^c   Koike, Kazuhiko ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b INSTITUTE FOR ADULT DISEASES   (Japan)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

1,3 DIMETHYLNITROSOUREA; ALPHA SMOOTH MUSCLE ACTIN; CYCLOOXYGENASE 2; INOSITOL; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; INTERLEUKIN 6 ANTIBODY; MESSENGER RNA; NEUTRALIZING ANTIBODY; SMALL INTERFERING RNA; STAT3 PROTEIN;

ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL INTERACTION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EPITHELIUM CELL; FIBROBLAST; GASTRITIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STOMACH CANCER; STOMACH CARCINOGENESIS; STROMA CELL;

ANIMALS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CULTURE MEDIA, CONDITIONED; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; FIBROBLASTS; HUMANS; INTERLEUKIN-6; METHYLNITROSOUREA; MICE; MODELS, BIOLOGICAL; NEOPLASTIC STEM CELLS; STAT3 TRANSCRIPTION FACTOR; STOMACH NEOPLASMS; STROMAL CELLS;

MUS;

EID: 84876094509     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060914     Document Type: Article

References (47)

1. Parkin DM, Bray F, Ferlay J, Pisani P, (2005) Global cancer statistics, 2002. CA Cancer J Clin 55: 74-108.
2. Inoue M, Tsugane S, (2005) Epidemiology of gastric cancer in Japan. Postgrad Med J 81: 419-424.
3. Koizumi W, Narahara H, Hara T, Takagane A, Akiya T, et al. (2008) S-1 plus cisplatin versus S-1 alone for first-line treatment of advanced gastric cancer (SPIRITS trial): a phase III trial. Lancet Oncol 9: 215-221.
4. Lin W, Kao HW, Robinson D, Kung HJ, Wu CW, et al. (2000) Tyrosine kinases and gastric cancer. Oncogene 19: 5680-5689.
5. Bang YJ, Van Cutsem E, Feyereislova A, Chung HC, Shen L, et al. (2010) Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet 376: 687-697.
6. Hong DS, Angelo LS, Kurzrock R, (2007) Interleukin-6 and its receptor in cancer: implications for translational therapeutics. Cancer 110: 1911-1928.
7. Ancrile B, Lim KH, Counter CM, (2007) Oncogenic Ras-induced secretion of IL6 is required for tumorigenesis. Genes Dev 21: 1714-1719.
8. Iliopoulos D, Hirsch HA, Struhl K, (2009) An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation. Cell 139: 693-706.
9. Grivennikov S, Karin E, Terzic J, Mucida D, Yu GY, et al. (2009) IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 15: 103-113.
10. Bollrath J, Phesse TJ, von Burstin VA, Putoczki T, Bennecke M, et al. (2009) gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis. Cancer Cell 15: 91-102.
11. Tang CH, Chen CF, Chen WM, Fong YC, (2011) IL-6 increases MMP-13 expression and motility in human chondrosarcoma cells. J Biol Chem 286: 11056-11066.
12. Lin MT, Lin BR, Chang CC, Chu CY, Su HJ, et al. (2007) IL-6 induces AGS gastric cancer cell invasion via activation of the c-Src/RhoA/ROCK signaling pathway. Int J Cancer 120: 2600-2608.
13. Walter M, Liang S, Ghosh S, Hornsby PJ, Li R, (2009) Interleukin 6 secreted from adipose stromal cells promotes migration and invasion of breast cancer cells. Oncogene 28: 2745-2755.
14. Yadav A, Kumar B, Datta J, Teknos TN, Kumar P, (2011) IL-6 promotes head and neck tumor metastasis by inducing epithelial-mesenchymal transition via the JAK-STAT3-SNAIL signaling pathway. Mol Cancer Res 9(12): 1658-1667.
15. Maeda S, Hikiba Y, Sakamoto K, Nakagawa H, Hirata Y, et al. (2009) Ikappa B kinasebeta/nuclear factor-kappaB activation controls the development of liver metastasis by way of interleukin-6 expression. Hepatology 50: 1851-1860.
16. Lee SA, Choi SR, Jang JS, Lee JH, Roh MH, et al. (2010) Expression of VEGF, EGFR, and IL-6 in Gastric Adenomas and Adenocarcinomas by Endoscopic Submucosal Dissection. Dig Dis Sci 55(7): 1955-1963.
17. Huang SP, Wu MS, Shun CT, Wang HP, Lin MT, et al. (2004) Interleukin-6 increases vascular endothelial growth factor and angiogenesis in gastric carcinoma. J Biomed Sci 11: 517-527.
18. Liao WC, Lin JT, Wu CY, Huang SP, Lin MT, et al. (2008) Serum interleukin-6 level but not genotype predicts survival after resection in stages II and III gastric carcinoma. Clin Cancer Res 14: 428-434.
19. Ashizawa T, Okada R, Suzuki Y, Takagi M, Yamazaki T, et al. (2005) Clinical significance of interleukin-6 (IL-6) in the spread of gastric cancer: role of IL-6 as a prognostic factor. Gastric Cancer 8: 124-131.
20. Kalluri R, Zeisberg M, (2006) Fibroblasts in cancer. Nat Rev Cancer 6: 392-401.
21. Erez N, Truitt M, Olson P, Arron ST, Hanahan D, (2010) Cancer-Associated Fibroblasts Are Activated in Incipient Neoplasia to Orchestrate Tumor-Promoting Inflammation in an NF-kappaB-Dependent Manner. Cancer Cell 17: 135-147.
22. Paland N, Kamer I, Kogan-Sakin I, Madar S, Goldfinger N, et al. (2009) Differential influence of normal and cancer-associated fibroblasts on the growth of human epithelial cells in an in vitro cocultivation model of prostate cancer. Mol Cancer Res 7: 1212-1223.
23. Quante M, Tu SP, Tomita H, Gonda T, Wang SS, et al. (2011) Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 19: 257-272.
24. Nishiyama M, Saeki S, Aogi K, Hirabayashi N, Toge T, (1993) Relevance of DT-diaphorase activity to mitomycin C (MMC) efficacy on human cancer cells: differences in in vitro and in vivo systems. Int J Cancer 53: 1013-1016.
25. Ochiai A, Yasui W, Tahara E, (1985) Growth-promoting effect of gastrin on human gastric carcinoma cell line TMK-1. Jpn J Cancer Res 76: 1064-1071.
26. Takahashi M, Kawabe T, Ogura K, Maeda S, Mikami Y, et al. (1997) Expression of vascular endothelial growth factor at the human gastric ulcer margin and in cultured gastric fibroblasts: a new angiogenic factor for gastric ulcer healing. Biochem Biophys Res Commun 234: 493-498.
27. Hayakawa Y, Hirata Y, Nakagawa H, Sakamoto K, Hikiba Y, et al. (2011) Apoptosis signal-regulating kinase 1 and cyclin D1 compose a positive feedback loop contributing to tumor growth in gastric cancer. Proc Natl Acad Sci U S A 108: 780-785.
28. Montero AJ, Diaz-Montero CM, Kyriakopoulos CE, Bronte V, Mandruzzato S, (2012) Myeloid-derived suppressor cells in cancer patients: a clinical perspective. J Immunother 35: 107-115.
29. Pedranzini L, Dechow T, Berishaj M, Comenzo R, Zhou P, et al. (2006) Pyridone 6, a pan-Janus-activated kinase inhibitor, induces growth inhibition of multiple myeloma cells. Cancer Res 66: 9714-9721.
30. Chen CN, Hsieh FJ, Cheng YM, Chang KJ, Lee PH, (2006) Expression of inducible nitric oxide synthase and cyclooxygenase-2 in angiogenesis and clinical outcome of human gastric cancer. J Surg Oncol 94: 226-233.
31. Takaishi S, Okumura T, Tu S, Wang SS, Shibata W, et al. (2009) Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells 27: 1006-1020.
32. Dinarello CA, (1996) Biologic basis for interleukin-1 in disease. Blood 87: 2095-2147.
33. Orjalo AV, Bhaumik D, Gengler BK, Scott GK, Campisi J, (2009) Cell surface-bound IL-1alpha is an upstream regulator of the senescence-associated IL-6/IL-8 cytokine network. Proc Natl Acad Sci U S A 106: 17031-17036.
34. Sakamoto K, Hikiba Y, Nakagawa H, Hayakawa Y, Yanai A, et al. (2010) Inhibitor of kappaB kinase beta regulates gastric carcinogenesis via interleukin-1alpha expression. Gastroenterology 139: 226-238 e226.
35. Sebba A, (2008) Tocilizumab: the first interleukin-6-receptor inhibitor. Am J Health Syst Pharm 65: 1413-1418.
36. Fleischmann RM, Tesser J, Schiff MH, Schechtman J, Burmester GR, et al. (2006) Safety of extended treatment with anakinra in patients with rheumatoid arthritis. Ann Rheum Dis 65: 1006-1012.
37. Nishimoto N, Kanakura Y, Aozasa K, Johkoh T, Nakamura M, et al. (2005) Humanized anti-interleukin-6 receptor antibody treatment of multicentric Castleman disease. Blood 106: 2627-2632.
38. Kanda N, Seno H, Konda Y, Marusawa H, Kanai M, et al. (2004) STAT3 is constitutively activated and supports cell survival in association with survivin expression in gastric cancer cells. Oncogene 23: 4921-4929.
39. Okamoto W, Okamoto I, Arao T, Yanagihara K, Nishio K, et al. (2011) Differential roles of STAT3 depending on the mechanism of STAT3 activation in gastric cancer cells. Br J Cancer 105: 407-412.
40. Gong W, Wang L, Yao JC, Ajani JA, Wei D, et al. (2005) 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 11: 1386-1393.
41. Ernst M, Najdovska M, Grail D, Lundgren-May T, Buchert M, et al. (2008) STAT3 and STAT1 mediate IL-11-dependent and inflammation-associated gastric tumorigenesis in gp130 receptor mutant mice. J Clin Invest 118: 1727-1738.
42. Howlett M, Judd LM, Jenkins B, La Gruta NL, Grail D, et al. (2005) Differential regulation of gastric tumor growth by cytokines that signal exclusively through the coreceptor gp130. Gastroenterology 129: 1005-1018.
43. Howlett M, Giraud AS, Lescesen H, Jackson CB, Kalantzis A, et al. (2009) The interleukin-6 family cytokine interleukin-11 regulates homeostatic epithelial cell turnover and promotes gastric tumor development. Gastroenterology 136: 967-977.
44. Shibata W, Maeda S, Hikiba Y, Yanai A, Sakamoto K, et al. (2008) c-Jun NH2-terminal kinase 1 is a critical regulator for the development of gastric cancer in mice. Cancer Res 68: 5031-5039.
45. Iliopoulos D, Hirsch HA, Wang G, Struhl K, (2011) Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proc Natl Acad Sci U S A 108: 1397-1402.
46. Guo X, Oshima H, Kitmura T, Taketo MM, Oshima M, (2008) Stromal fibroblasts activated by tumor cells promote angiogenesis in mouse gastric cancer. J Biol Chem 283: 19864-19871.
47. Mahara K, Kato J, Terui T, Takimoto R, Horimoto M, et al. (1994) Transforming growth factor beta 1 secreted from scirrhous gastric cancer cells is associated with excess collagen deposition in the tissue. Br J Cancer 69: 777-783.