Antiproliferative effect of SOCS-1 through the suppression of STAT3 and p38 MAPK activation in gastric cancer cells

International Journal of Cancer

Volumn 131, Issue 6, 2012, Pages 1287-1296

  Souma, Yoshihito ^a   Nishida, Toshirou ^b   Serada, Satoshi ^c   Iwahori, Kota ^c   Takahashi, Tsuyoshi ^d   Fujimoto, Minoru ^c   Ripley, Barry ^a   Nakajima, Kiyokazu ^a   Miyazaki, Yasuaki ^a   Mori, Masaki ^a   Doki, Yuichiro ^a   Sawa, Yoshiki ^a   Naka, Tetsuji ^c  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA POLICE HOSPITAL   (Japan)

^c NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

^d OSAKA GENERAL MEDICAL CENTER   (Japan)

Author keywords

gastric cancer; Janus kinase; p38 mitogen activated protein kinase; signal transducer and activator of transcription; suppressor of cytokine signaling

Indexed keywords

ADENOVIRUS VECTOR; BETA GALACTOSIDASE; CYTOKINE; INTERLEUKIN 6; INTERLEUKIN 6 ANTIBODY; INTERLEUKIN 6 RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE P38; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER CELL CULTURE; CELL PROLIFERATION; CELL STRAIN; CELL STRAIN AGS; CELL STRAIN NUGC 3; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; SOCS 1 GENE; STOMACH CANCER; TUMOR SUPPRESSOR GENE; TUMOR XENOGRAFT; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; CPG ISLANDS; DNA METHYLATION; ENZYME ACTIVATION; GENETIC THERAPY; HUMANS; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED ICR; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTORS, INTERLEUKIN-6; STAT3 TRANSCRIPTION FACTOR; STOMACH NEOPLASMS; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84864136013     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.27350     Document Type: Article

References (48)

1. Pisani P, Parkin DM, Ferlay J,. Estimates of the worldwide mortality from eighteen major cancers in 1985. Implications for prevention and projections of future burden. Int J Cancer 1993; 55: 891-903.
2. Dicken BJ, Bigam DL, Cass C, Mackey JR, Joy AA, Hamilton SM,. Gastric adenocarcinoma: review and considerations for future directions. Ann Surg 2005; 241: 27-39.
3. Grivennikov SI, Greten FR, Karin M,. Immunity, inflammation, and cancer. Cell 2010; 140: 883-99.
4. Peek RM, Jr, Crabtree JE,. Helicobacter infection and gastric neoplasia. J Pathol 2006; 208: 233-48.
5. Lacronique V, Boureux A, Valle VD, Poirel H, Quang CT, Mauchauffe M, Berthou C, Lessard M, Berger R, Ghysdael J, Bernard OA,. A TEL-JAK2 fusion protein with constitutive kinase activity in human leukemia. Science 1997; 278: 1309-12.
6. Burke WM, Jin X, Lin HJ, Huang M, Liu R, Reynolds RK, Lin J,. Inhibition of constitutively active Stat3 suppresses growth of human ovarian and breast cancer cells. Oncogene 2001; 20: 7925-34.
7. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, Albanese C, Darnell JE, Jr,. Stat3 as an oncogene. Cell 1999; 98: 295-303.
8. Rahaman SO, Harbor PC, Chernova O, Barnett GH, Vogelbaum MA, Haque SJ,. Inhibition of constitutively active Stat3 suppresses proliferation and induces apoptosis in glioblastoma multiforme cells. Oncogene 2002; 21: 8404-13.
9. Zhang F, Li C, Halfter H, Liu J,. Delineating an oncostatin M-activated STAT3 signaling pathway that coordinates the expression of genes involved in cell cycle regulation and extracellular matrix deposition of MCF-7 cells. Oncogene 2003; 22: 894-905.
10. He B, You L, Uematsu K, Zang K, Xu Z, Lee AY, Costello JF, McCormick F, Jablons DM,. SOCS-3 is frequently silenced by hypermethylation and suppresses cell growth in human lung cancer. Proc Natl Acad Sci USA 2003; 100: 14133-8.
11. Yu H, Pardoll D, Jove R,. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 2009; 9: 798-809.
12. Kanda N, Seno H, Konda Y, Marusawa H, Kanai M, Nakajima T, Kawashima T, Nanakin A, Sawabu T, Uenoyama Y, Sekikawa A, Kawada M, et al. STAT3 is constitutively activated and supports cell survival in association with survivin expression in gastric cancer cells. Oncogene 2004; 23: 4921-9.
13. Howlett M, Menheniott TR, Judd LM, Giraud AS,. Cytokine signalling via gp130 in gastric cancer. Biochim Biophys Acta 2009; 1793: 1623-33.
14. Naka T, Narazaki M, Hirata M, Matsumoto T, Minamoto S, Aono A, Nishimoto N, Kajita T, Taga T, Yoshizaki K, Akira S, Kishimoto T,. Structure and function of a new STAT-induced STAT inhibitor. Nature 1997; 387: 924-9.
15. Starr R, Willson TA, Viney EM, Murray LJ, Rayner JR, Jenkins BJ, Gonda TJ, Alexander WS, Metcalf D, Nicola NA, Hilton DJ,. A family of cytokine-inducible inhibitors of signalling. Nature 1997; 387: 917-21.
16. Endo TA, Masuhara M, Yokouchi M, Suzuki R, Sakamoto H, Mitsui K, Matsumoto A, Tanimura S, Ohtsubo M, Misawa H, Miyazaki T, Leonor N, et al. A new protein containing an SH2 domain that inhibits JAK kinases. Nature 1997; 387: 921-4.
17. Yoshimura A, Naka T, Kubo M,. SOCS proteins, cytokine signalling and immune regulation. Nat Rev Immunol 2007; 7: 454-65.
18. Narazaki M, Fujimoto M, Matsumoto T, Morita Y, Saito H, Kajita T, Yoshizaki K, Naka T, Kishimoto T,. Three distinct domains of SSI-1/SOCS-1/JAB protein are required for its suppression of interleukin 6 signaling. Proc Natl Acad Sci USA 1998; 95: 13130-4.
19. Yasukawa H, Misawa H, Sakamoto H, Masuhara M, Sasaki A, Wakioka T, Ohtsuka S, Imaizumi T, Matsuda T, Ihle JN, Yoshimura A,. The JAK-binding protein JAB inhibits Janus tyrosine kinase activity through binding in the activation loop. EMBO J 1999; 18: 1309-20.
20. Krebs DL, Hilton DJ,. SOCS proteins: negative regulators of cytokine signaling. Stem Cells 2001; 19: 378-87.
21. Naka T, Fujimoto M, Tsutsui H, Yoshimura A,. Negative regulation of cytokine and TLR signalings by SOCS and others. Adv Immunol 2005; 87: 61-122.
22. Yoshikawa H, Matsubara K, Qian GS, Jackson P, Groopman JD, Manning JE, Harris CC, Herman JG,. SOCS-1, a negative regulator of the JAK/STAT pathway, is silenced by methylation in human hepatocellular carcinoma and shows growth-suppression activity. Nat Genet 2001; 28: 29-35.
23. Nagai H, Kim YS, Konishi N, Baba M, Kubota T, Yoshimura A, Emi M,. Combined hypermethylation and chromosome loss associated with inactivation of SSI-1/SOCS-1/JAB gene in human hepatocellular carcinomas. Cancer Lett 2002; 186: 59-65.
24. Fukushima N, Sato N, Sahin F, Su GH, Hruban RH, Goggins M,. Aberrant methylation of suppressor of cytokine signalling-1 (SOCS-1) gene in pancreatic ductal neoplasms. Br J Cancer 2003; 89: 338-43.
25. Galm O, Yoshikawa H, Esteller M, Osieka R, Herman JG,. SOCS-1, a negative regulator of cytokine signaling, is frequently silenced by methylation in multiple myeloma. Blood 2003; 101: 2784-8.
26. Yasui W, Oue N, Kuniyasu H, Ito R, Tahara E, Yokozaki H,. Molecular diagnosis of gastric cancer: present and future. Gastric Cancer 2001; 4: 113-21.
27. Yokozaki H, Yasui W, Tahara E,. Genetic and epigenetic changes in stomach cancer. Int Rev Cytol 2001; 204: 49-95.
28. Yasui W, Oue N, Aung PP, Matsumura S, Shutoh M, Nakayama H,. Molecular-pathological prognostic factors of gastric cancer: a review. Gastric Cancer 2005; 8: 86-94.
29. Yasui W, Yokozaki H, Fujimoto J, Naka K, Kuniyasu H, Tahara E,. Genetic and epigenetic alterations in multistep carcinogenesis of the stomach. J Gastroenterol 2000; 35 (Suppl 12): 111-5.
30. Yasui W, Oue N, Sentani K, Sakamoto N, Motoshita J,. Transcriptome dissection of gastric cancer: identification of novel diagnostic and therapeutic targets from pathology specimens. Pathol Int 2009; 59: 121-36.
31. To KF, Chan MW, Leung WK, Ng EK, Yu J, Bai AH, Lo AW, Chu SH, Tong JH, Lo KW, Sung JJ, Chan FK,. Constitutional activation of IL-6-mediated JAK/STAT pathway through hypermethylation of SOCS-1 in human gastric cancer cell line. Br J Cancer 2004; 91: 1335-41.
32. Aihara M, Tsuchimoto D, Takizawa H, Azuma A, Wakebe H, Ohmoto Y, Imagawa K, Kikuchi M, Mukaida N, Matsushima K,. Mechanisms involved in Helicobacter pylori-induced interleukin-8 production by a gastric cancer cell line, MKN45. Infect Immun 1997; 65: 3218-24.
33. Oshimo Y, Kuraoka K, Nakayama H, Kitadai Y, Yoshida K, Chayama K, Yasui W,. Epigenetic inactivation of SOCS-1 by CpG island hypermethylation in human gastric carcinoma. Int J Cancer 2004; 112: 1003-9.
34. Yamana J, Yamamura M, Okamoto A, Aita T, Iwahashi M, Sunahori K, Makino H,. Resistance to IL-10 inhibition of interferon gamma production and expression of suppressor of cytokine signaling 1 in CD4+ T cells from patients with rheumatoid arthritis. Arthritis Res Ther 2004; 6: R567-77.
35. Mizuguchi H, Kay MA,. A simple method for constructing E1- and E1/E4-deleted recombinant adenoviral vectors. Hum Gene Ther 1999; 10: 2013-7.
36. Sakurai H, Tashiro K, Kawabata K, Yamaguchi T, Sakurai F, Nakagawa S, Mizuguchi H,. Adenoviral expression of suppressor of cytokine signaling-1 reduces adenovirus vector-induced innate immune responses. J Immunol 2008; 180: 4931-8.
37. Maizel JV, Jr, White DO, Scharff MD,. The polypeptides of adenovirus. I. Evidence for multiple protein components in the virion and a comparison of types 2, 7A, and 12. Virology 1968; 36: 115-25.
38. Yamaoka Y, Kodama T, Kita M, Imanishi J, Kashima K, Graham DY,. Relation between cytokines and Helicobacter pylori in gastric cancer. Helicobacter 2001; 6: 116-24.
39. Wu CW, Wang SR, Chao MF, Wu TC, Lui WY, P'Eng F K, Chi CW,. Serum interleukin-6 levels reflect disease status of gastric cancer. Am J Gastroenterol 1996; 91: 1417-22.
40. Ashizawa T, Okada R, Suzuki Y, Takagi M, Yamazaki T, Sumi T, Aoki T, Ohnuma S,. Clinical significance of interleukin-6 (IL-6) in the spread of gastric cancer: role of IL-6 as a prognostic factor. Gastric Cancer 2005; 8: 124-31.
41. Iwahori K, Serada S, Fujimoto M, Nomura S, Osaki T, Lee CM, Mizuguchi H, Takahashi T, Ripley B, Okumura M, Kawase I, Kishimoto T, Naka T. Overexpression of SOCS3 exhibits preclinical antitumor activity against malignant pleural mesothelioma. Int J Cancer. 2011; 129: 1005-17.
42. Lin MT, Lin BR, Chang CC, Chu CY, Su HJ, Chen ST, Jeng YM, Kuo ML,. IL-6 induces AGS gastric cancer cell invasion via activation of the c-Src/RhoA/ROCK signaling pathway. Int J Cancer 2007; 120: 2600-8.
43. Kabir S, Daar GA,. Serum levels of interleukin-1, interleukin-6 and tumour necrosis factor-alpha in patients with gastric carcinoma. Cancer Lett 1995; 95: 207-12.
44. Howlett M, Giraud AS, Lescesen H, Jackson CB, Kalantzis A, van Driel IR, Robb L, van der Hoek M, Ernst M, Minamoto T, Boussioutas A, Oshima H, et al. The interleukin-6 family cytokine interleukin-11 regulates homeostatic epithelial cell turnover and promotes gastric tumor development. Gastroenterology 2009; 136: 967-77.
45. Cuadrado A, Nebreda AR,. Mechanisms and functions of p38 MAPK signalling. Biochem J 2010; 429: 403-17.
46. Li Q, Liu N, Shen B, Zhou L, Wang Y, Sun J, Fan Z, Liu RH,. Helicobacter pylori enhances cyclooxygenase 2 expression via p38MAPK/ATF-2 signaling pathway in MKN45 cells. Cancer Lett 2009; 278: 97-103.
47. He Y, Zhang W, Zhang R, Zhang H, Min W,. SOCS1 inhibits tumor necrosis factor-induced activation of ASK1-JNK inflammatory signaling by mediating ASK1 degradation. J Biol Chem 2006; 281: 5559-66.
48. Hayakawa Y, Hirata Y, Nakagawa H, Sakamoto K, Hikiba Y, Kinoshita H, Nakata W, Takahashi R, Tateishi K, Tada M, Akanuma M, Yoshida H, et al. Apoptosis signal-regulating kinase 1 and cyclin D1 compose a positive feedback loop contributing to tumor growth in gastric cancer. Proc Natl Acad Sci USA 2011; 108: 780-5.