Aberrant methylation of suppressor of cytokine signalling-1 (SOCS-1) gene in pancreatic ductal neoplasms

British Journal of Cancer

Volumn 89, Issue 2, 2003, Pages 338-343

  Fukushima, N ^a   Sato, N ^a   Sahin, F ^a   Su, G H ^a   Hruban, R H ^a   Goggins, M ^a  

^a DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

CpG island methylation; IL 6; JAK STAT pathway; Pancreatic ductal adenocarcinoma; SOCS 1

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; JANUS KINASE; STAT PROTEIN;

ADENOCARCINOMA; ARTICLE; CANCER CELL CULTURE; CANCER INFILTRATION; CELL GROWTH; CELL PROLIFERATION; CPG ISLAND; DOSE TIME EFFECT RELATION; GENE EXPRESSION; GENE FUNCTION; GENE INACTIVATION; GENE REPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INTRADUCTAL CARCINOMA; METHYLATION; ONCOGENE; PANCREAS TUMOR; PAPILLARY CARCINOMA; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SOCS 1 GENE;

ADULT; AGED; AGED, 80 AND OVER; CARCINOMA, PANCREATIC DUCTAL; CARRIER PROTEINS; DNA METHYLATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MIDDLE AGED; PANCREATIC NEOPLASMS; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANS-ACTIVATION (GENETICS); TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL;

EID: 0042575343     PISSN: 00070920     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjc.6601039     Document Type: Article

References (37)

1. Barber MD, Fearon KC, Ross JA (1999) Relationship of serum levels of interleukin-6, soluble interleukin-6 receptor and tumour necrosis factor receptors to the acute-phase protein response in advanced pancreatic cancer. Clin Sci (Lond) 96: 83-87
2. Blay JY, Negrier S, Combaret V, Attali S, Goillot E, Merrouche Y, Mercatello A, Ravault A, Tourani JM, Moskovtchenko JF (1992) Serum level of interleukin 6 as a prognosis factor in metastatic renal cell carcinoma. Cancer Res 52: 3317-3322
3. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, Albanese C, Darnell Jr JE (1999) Stat3 as an oncogene. Cell 98: 295-303
4. Brysha M, Zhang JG, Bertolino P, Corbin JE, Alexander WS, Nicola NA, Hilton DJ, Starr R (2001) Suppressor of cytokine signaling-1 attenuates the duration of interferon gamma signal transduction in vitro and in vivo. J Biol Chem 276: 22086-22089
5. Endo TA, Masuhara M, Yokouchi M, Suzuki R, Sakamoto H, Mitsui K, Matsumoto A, Tanimura S, Ohtsubo M, Misawa H, Miyazaki T, Leonor N, Taniguchi T, Fujita T, Kanakura Y, Komiya S, Yoshimura A (1997) A new protein containing an SH2 domain that inhibits JAK kinases. Nature 387: 921-924
6. Fukushima N, Kimberly MW, Ueki T, Sato N, Matsubayashi H, Cameron JL, Hruban RH, Canto M, Yeo CJ, Goggins M (2003) Diagnosing pancreatic cancer using methylation specific PCR analysis of pancreatic juice. Cancer Biol Ther 2: 78-83
7. Fukushima N, Mukai K, Kanai Y, Hasebe T, Shimada K, Ozaki H, Kinoshita T, Kosuge T (1997) Intraductal papillary tumors and mucinous cystic tumors of the pancreas: clinicopathologic study of 38 cases. Hum Pathol 28: 1010-1017
8. Fukushima N, Sato N, Ueki T, Rosty C, Walter KM, Wilentz RE, Yeo CJ, Hruban RH, Goggins M (2002) Aberrant methylation of preproenkephalin and p16 genes in pancreatic intraepithelial neoplasia and pancreatic ductal adenocarcinoma. Am J Pathol 160: 1573-1581
9. Galm O, Yoshikawa H, Esteller M, Osieka R, Herman JG (2002) SOCS-1, a negative regulator of cytokine signaling, is frequently silenced by methylation in multiple myeloma. Blood 27: 27
10. Giri D, Ozen M, Ittmann M (2001) Interleukin-6 is an autocrine growth factor in human prostate cancer. Am J Pathol 159: 2159-2165
11. Goggins M, Hruban RH, Kern, SE (2000) BRCA2 is inactivated late in the development of pancreatic intraepithelial neoplasia: evidence and implications. Am J Pathol 156: 1767-1771
12. Goydos JS, Brumfield AM, Frezza E, Booth A, Lotze MT, Carty SE. (1998) Marked elevation of serum interleukin-6 in patients with cholangiocarcinoma: validation of utility as a clinical marker. Ann Surg 227: 398-404
13. Hruban RH, Adsay NV, Albores-Saavedra J, Compton C, Garrett ES, Goodman SN, Kern SE, Klimstra DS, Kloppel G, Longnecker DS, Luttges J, Offerhaus GJ (2001) Pancreatic intraepithelial neoplasia: a new nomenclature and classification system for pancreatic duct lesions. Am J Surg Pathol 25: 579-586
14. Hussein MA, Juturi JV, Lieberman I (2002) Multiple myeloma: present and future. Curr Opin Oncol 14: 31-35
15. Jansen M, Fukushima N, Rosty C, Walter K, Altink R, Heek TV, Hruban R, Offerhaus JG, Goggins M (2002) Aberrant methylation of the 5′ CpG island of TSLC1 is common in pancreatic ductal adenocarcinoma and is first manifest in high-grade PanlNs. Cancer Biol Ther 1: 293-296
16. Jones PA, Baylin SB (2002) The fundamental role of epigenetic events in cancer. Nat Rev Genet 3: 415-428
17. Kishimoto T, Kikutani H (2001) Knocking the SOCS off a tumor suppressor. Nat Genet 28: 4-5
18. Klöppel GHR, Longnecker DS, Adler G, Kern SE, Partanen TJ (2000) Ductal adenocarcinoma of the pancreas. In Pathology & Genetics, Tumours of the Digestive System, World Health Organization of Tumours, Hamilton SR and Aattonen LA (ed) pp 221-230. Lyon: IARC Press
19. Longnecker DS, HR, Adler G, Klöppel G (2000) Intraductal papillary-mucinous neoplasms of the pancreas. In Pathology & Genetics, Tumours of the Digestive System, World Health Organization of Tumours, Hamilton SR and Aattonen LA (ed) pp 237-240. Lyon: IARC Press
20. Matsubayashi H, Sato N, Fukushima N, Yeo C, Walter KM, Brune K, Sahin F, Hruban R, Goggins M (2003) High frequency of cyclin D2 methylation in pancreatic carcinoma. Clin Cancer Res 9: 1446-1452
21. Morita Y, Naka T, Kawazoe Y, Fujimoto M, Narazaki M, Nakagawa R, Fukuyama H, Nagata S, Kishimoto T (2000) Signals transducers and activators of transcription (STAT)-induced STAT inhibitor-1 (SSI-1)/suppressor of cytokine signaling-1 (SOCS-1) suppresses tumor necrosis factor alpha-induced cell death in fibroblasts. Proc Natl Acad Sci USA 97: 5405-5410
22. Moskaluk CA, Hruban RH, Kern SE (1997) p16 and K-ras gene mutations in the intraductal precursors of human pancreatic adenocarcinoma. Cancer Res 57: 2140-2143
23. Naka T, Narazaki M, Hirata M, Matsumoto T, Minamoto S, Aono A, Nishimoto N, Kajita T, Taga T, Yoshizaki K, Akira S, Kishimoto T (1997) Structure and function of a new STAT-induced STAT inhibitor. Nature 387: 924-929
24. Narazaki M, Fujimoto M, Matsumoto T, Morita Y, Saito H, Kajita T, Yoshizaki K, Naka T, Kishimoto T (1998) Three distinct domains of SSI-1/SOCS-1/JAB protein are required for its suppression of interleukin 6 signaling. Proc Natl Acad Sci USA 95: 13130-13134
25. Plante M, Rubin SC, Wong GY, Federici MG, Finstad CL, Gastl GA (1994) Interleukin-6 level in serum and ascites as a prognostic factor in patients with epithelial ovarian cancer. Cancer 73: 1882-1888
26. Rottapel R, Ilangumaran S, Neale C, La Rose J, Ho JM, Nguyen MH, Barber D, Dubreuil P, de Sepulveda P (2002) The tumor suppressor activity of SOCS-1. Oncogene 21: 4351-4362
27. Sato N, Ueki T, Fukushima N, Iacobuzio-Donahue CA, Yeo CJ, Cameron JL, Hruban RH, Goggins M (2002) Aberrant methylation of CpG islands in intraductal papillary mucinous neoplasms of the pancreas. Gastroenterology 123: 365-372
28. Schneider MR, Hoeflich A, Fischer JR, Wolf E, Sordat B, Lahm H (2000) Interleukin-6 stimulates clonogenic growth of primary and metastatic human colon carcinoma cells. Cancer Lett 151: 31-38
29. Sporri B, Kovanen PE, Sasaki A, Yoshimura A, Leonard WJ (2001) JAB/SOCS1/SSI-1 is an interleukin-2-induced inhibitor of IL-2 signaling. Blood 97: 221-226
30. Starr R, Willson TA, Viney EM, Murray LJ, Rayner JR, Jenkins BJ, Gonda TJ, Alexander WS, Metcalf D, Nicola NA, Hilton DJ (1997) A family of cytokine-inducible inhibitors of signalling. Nature 387: 917-921
31. Ueki T, Toyota M, Skinner H, Walter KM, Yeo CJ, Issa JP, Hruban RH, Goggins M (2001) Identification and characterization of differentially methylated CpG islands in pancreatic carcinoma. Cancer Res 61: 8540-8546
32. Ueki T, Toyota M, Sohn T, Yeo CJ, Issa JP, Hruban RH, Goggins M (2000) Hypermethylation of multiple genes in pancreatic adenocarcinoma. Cancer Res 60: 1835-1839
33. Wilentz RE, Geradts J, Maynard R, Offerhaus GJ, Kang M, Goggins, M, Yeo CJ, Kern SE, Hruban RH (1998) Inactivation of the p16 (INK4A) tumor-suppressor gene in pancreatic duct lesions: loss of intranuclear expression. Cancer Res 58: 4740-4744
34. Wilentz RE, Iacobuzio-Donahue CA, Argani P, McCarthy DM, Parsons JL, Yeo CJ, Kern SE, Hruban RH (2000) Loss of expression of Dpc4 in pancreatic intraepithelial neoplasia: evidence that DPC4 inactivation occurs late in neoplastic progression. Cancer Res 60: 2002-2006
35. Yasukawa H, Misawa H, Sakamoto H, Masuhara M, Sasaki A, Wakioka T, Ohtsuka S, Imaizumi T, Matsuda T, Ihle JN, Yoshimura A. (1999) The JAK-binding protein JAB inhibits Janus tyrosine kinase activity through binding in the activation loop. EMBO J 18: 1309-1320
36. Yoshikawa H, Matsubara K, Qian GS, Jackson P, Groopman JD, Manning JE, Harris CC, Herman JG (2001) 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 28: 29-35
37. Yu CL, Meyer DJ, Campbell GS, Larner AC, Carter-Su C, Schwartz J, Jove R (1995) Enhanced DNA-binding activity of a Stat3-related protein in cells transformed by the Src oncoprotein. Science 269: 81-83