Activin signal promotes cancer progression and is involved in cachexia in a subset of pancreatic cancer

Cancer Letters

Volumn 356, Issue 2, 2015, Pages 819-827

  Togashi, Yosuke ^a   Kogita, Akihiro ^a   Sakamoto, Hiroki ^a   Hayashi, Hidetoshi ^a   Terashima, Masato ^a   de Velasco, Marco A ^a   Sakai, Kazuko ^a   Fujita, Yoshihiko ^a   Tomida, Shuta ^a   Kitano, Masayuki ^a   Okuno, Kiyotaka ^a   Kudo, Masatoshi ^a   Nishio, Kazuto ^a  

^a KINKI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Activin signal; Cachexia; INHBA; INHBB; Pancreatic cancer

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ACTIVIN A; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; ANTINEOPLASTIC AGENT; DOXORUBICIN; ERLOTINIB; FLUOROURACIL; GEMCITABINE; INHIBIN B; PACLITAXEL; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; ACTIVIN; MESSENGER RNA; TUMOR MARKER;

ADVANCED CANCER; AGED; ARTICLE; CACHEXIA; CANCER GROWTH; CANCER INHIBITION; CANCER STAGING; CANCER SURVIVAL; CELL GROWTH; CLINICAL ARTICLE; COLONY FORMATION; CONTROLLED STUDY; ENDOSCOPIC BIOPSY; FEMALE; HUMAN; MALE; MOUSE; NONHUMAN; PANCREAS CANCER; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; TREATMENT RESPONSE; TUMOR VOLUME; TUMOR XENOGRAFT; ANIMAL; APOPTOSIS; BAGG ALBINO MOUSE; BLOOD; CELL PROLIFERATION; COMPLICATION; DISEASE COURSE; DRUG SCREENING; ENZYME IMMUNOASSAY; GENETICS; LYMPH NODE METASTASIS; METABOLISM; MIDDLE AGED; MORTALITY; NUDE MOUSE; PANCREAS TUMOR; PATHOLOGY; PROGNOSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SURVIVAL RATE; TUMOR CELL CULTURE; VERY ELDERLY; WESTERN BLOTTING;

AGOUTI PACA; MUS;

ACTIVINS; AGED; AGED, 80 AND OVER; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CACHEXIA; CELL PROLIFERATION; DISEASE PROGRESSION; FEMALE; HUMANS; IMMUNOENZYME TECHNIQUES; LYMPHATIC METASTASIS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MIDDLE AGED; NEOPLASM STAGING; PANCREATIC NEOPLASMS; PROGNOSIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; SURVIVAL RATE; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL; TUMOR STEM CELL ASSAY; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84919459476     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.10.037     Document Type: Article

References (49)

1. Moore M.J., Goldstein D., Hamm J., Figer A., Hecht J.R., Gallinger S., et al. Erlotinib plus gemcitabine compared with gemcitabine alone in patients with advanced pancreatic cancer: a phase III trial of the National Cancer Institute of Canada Clinical Trials Group. J. Clin. Oncol 2007, 25:1960-1966.
2. Conroy T., Desseigne F., Ychou M., Bouché O., Guimbaud R., Bécouarn Y., et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N. Engl. J. Med 2011, 364:1817-1825.
3. Von Hoff D.D., Ervin T., Arena F.P., Chiorean E.G., Infante J., Moore M., et al. Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N. Engl. J. Med 2013, 369:1691-1703.
4. Siegel R., Naishadham D., Jemal A. Cancer statistics, 2013. CA Cancer J. Clin 2013, 63:11-30.
5. Macgregor-Das A.M., Iacobuzio-Donahue C.A. Molecular pathways in pancreatic carcinogenesis. J. Surg. Oncol 2013, 107:8-14.
6. Ikushima H., Miyazono K. TGFbeta signalling: a complex web in cancer progression. Nat. Rev. Cancer 2010, 10:415-424.
7. Akhurst R.J., Hata A. Targeting the TGFβ signalling pathway in disease. Nat. Rev. Drug Discov 2012, 11:790-811.
8. Birnbaum D.J., Mamessier E., Birnbaum D. The emerging role of the TGFβ tumor suppressor pathway in pancreatic cancer. Cell Cycle 2012, 11:683-686.
9. Ijichi H., Chytil A., Gorska A.E., Aakre M.E., Fujitani Y., Fujitani S., et al. Aggressive pancreatic ductal adenocarcinoma in mice caused by pancreas-specific blockade of transforming growth factor-beta signaling in cooperation with active Kras expression. Genes Dev 2006, 20:3147-3160.
10. Izeradjene K., Combs C., Best M., Gopinathan A., Wagner A., Grady W.M., et al. Kras(G12D) and Smad4/Dpc4 haploinsufficiency cooperate to induce mucinous cystic neoplasms and invasive adenocarcinoma of the pancreas. Cancer Cell 2007, 11:229-243.
11. Kleeff J., Ishiwata T., Friess H., Büchler M.W., Korc M. Concomitant over-expression of activin/inhibin beta subunits and their receptors in human pancreatic cancer. Int. J. Cancer 1998, 77:860-868.
12. Su G.H., Bansal R., Murphy K.M., Montgomery E., Yeo C.J., Hruban R.H., et al. ACVR1B (ALK4, activin receptor type 1B) gene mutations in pancreatic carcinoma. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:3254-3257.
13. Lonardo E., Hermann P.C., Mueller M.T., Huber S., Balic A., Miranda-Lorenzo I., et al. Nodal/Activin signaling drives self-renewal and tumorigenicity of pancreatic cancer stem cells and provides a target for combined drug therapy. Cell Stem Cell 2011, 9:433-446.
14. McPherson S.J., Mellor S.L., Wang H., Evans L.W., Groome N.P., Risbridger G.P. Expression of activin A and follistatin core proteins by human prostate tumor cell lines. Endocrinology 1999, 140:5303-5309.
15. Yokomuro S., Tsuji H., Lunz J.G., Sakamoto T., Ezure T., Murase N., et al. Growth control of human biliary epithelial cells by interleukin 6, hepatocyte growth factor, transforming growth factor beta1, and activin A: comparison of a cholangiocarcinoma cell line with primary cultures of non-neoplastic biliary epithelial cells. Hepatology 2000, 32:26-35.
16. Panopoulou E., Murphy C., Rasmussen H., Bagli E., Rofstad E.K., Fotsis T. Activin A suppresses neuroblastoma xenograft tumor growth via antimitotic and antiangiogenic mechanisms. Cancer Res 2005, 65:1877-1886.
17. Burdette J.E., Jeruss J.S., Kurley S.J., Lee E.J., Woodruff T.K. Activin A mediates growth inhibition and cell cycle arrest through Smads in human breast cancer cells. Cancer Res 2005, 65:7968-7975.
18. Ramachandran A., Marshall E.S., Love D.R., Baguley B.C., Shelling A.N. Activin is a potent growth suppressor of epithelial ovarian cancer cells. Cancer Lett 2009, 285:157-165.
19. Bauer J., Sporn J.C., Cabral J., Gomez J., Jung B. Effects of activin and TGFβ on p21 in colon cancer. PLoS ONE 2012, 7. e39381.
20. Togashi Y., Sakamoto H., Hayashi H., Terashima M., de Velasco M.A., Fujita Y., et al. Homozygous deletion of the activin A receptor, type IB gene is associated with an aggressive cancer phenotype in pancreatic cancer. Mol. Cancer 2014, 13:126.
21. Kaneda H., Arao T., Matsumoto K., De Velasco M.A., Tamura D., Aomatsu K., et al. Activin A inhibits vascular endothelial cell growth and suppresses tumour angiogenesis in gastric cancer. Br. J. Cancer 2011, 105:1210-1217.
22. Yanagihara K., Takigahira M., Tanaka H., Arao T., Aoyagi Y., Oda T., et al. Establishment and molecular profiling of a novel human pancreatic cancer panel for 5-FU. Cancer Sci 2008, 99:1859-1864.
23. Arao T., Fukumoto H., Takeda M., Tamura T., Saijo N., Nishio K. Small in-frame deletion in the epidermal growth factor receptor as a target for ZD6474. Cancer Res 2004, 64:9101-9104.
24. Mu Y., Gudey S.K., Landström M. Non-Smad signaling pathways. Cell Tissue Res 2012, 347:11-20.
25. Weiss R.H. p21Waf1/Cip1 as a therapeutic target in breast and other cancers. Cancer Cell 2003, 4:425-429.
26. Zhou X., Wang J.L., Lu J., Song Y., Kwak K.S., Jiao Q., et al. Reversal of cancer cachexia and muscle wasting by ActRIIB antagonism leads to prolonged survival. Cell 2010, 142:531-543.
27. Fearon K.C., Glass D.J., Guttridge D.C. Cancer cachexia: mediators, signaling, and metabolic pathways. Cell Metab 2012, 16:153-166.
28. Trendelenburg A.U., Meyer A., Jacobi C., Feige J.N., Glass D.J. TAK-1/p38/nNFκB signaling inhibits myoblast differentiation by increasing levels of Activin A. Skelet. Muscle 2012, 2:3.
29. Chen J.L., Walton K.L., Winbanks C.E., Murphy K.T., Thomson R.E., Makanji Y., et al. Elevated expression of activins promotes muscle wasting and cachexia. FASEB J. 2014, 28:1711-1723.
30. Stenvers K.L., Findlay J.K. Inhibins: from reproductive hormones to tumor suppressors. Trends Endocrinol. Metab 2010, 21:174-180.
31. Seder C.W., Hartojo W., Lin L., Silvers A.L., Wang Z., Thomas D.G., et al. Upregulated INHBA expression may promote cell proliferation and is associated with poor survival in lung adenocarcinoma. Neoplasia 2009, 11:388-396.
32. Seder C.W., Hartojo W., Lin L., Silvers A.L., Wang Z., Thomas D.G., et al. INHBA overexpression promotes cell proliferation and may be epigenetically regulated in esophageal adenocarcinoma. J. Thorac. Oncol 2009, 4:455-462.
33. Wang Q., Wen Y.G., Li D.P., Xia J., Zhou C.Z., Yan D.W., et al. Upregulated INHBA expression is associated with poor survival in gastric cancer. Med. Oncol 2012, 29:77-83.
34. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 2000, 103:239-252.
35. Weston C.R., Davis R.J. The JNK signal transduction pathway. Curr. Opin. Cell Biol 2007, 19:142-149.
36. Tessari G., Ferrara C., Poletti A., Dubrovich A., Corsini A., Del Favero G., et al. The expression of proto-oncogene c-jun in human pancreatic cancer. Anticancer Res 1999, 19:863-867.
37. Ennis B.W., Fultz K.E., Smith K.A., Westwick J.K., Zhu D., Boluro-Ajayi M., et al. Inhibition of tumor growth, angiogenesis, and tumor cell proliferation by a small molecule inhibitor of c-Jun N-terminal kinase. J. Pharmacol. Exp. Ther 2005, 313:325-332.
38. Takahashi R., Hirata Y., Sakitani K., Nakata W., Kinoshita H., Hayakawa Y., et al. Therapeutic effect of c-Jun N-terminal kinase inhibition on pancreatic cancer. Cancer Sci 2013, 104:337-344.
39. Okada M., Shibuya K., Sato A., Seino S., Suzuki S., Seino M., et al. Targeting the K-Ras-JNK axis eliminates cancer stem-like cells and prevents pancreatic tumor formation. Oncotarget 2014, 5:5100-5112.
40. Engelman J.A. Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat. Rev. Cancer 2009, 9:550-562.
41. Rodon J., Dienstmann R., Serra V., Tabernero J. Development of PI3K inhibitors: lessons learned from early clinical trials. Nat. Rev. Clin. Oncol 2013, 10:143-153.
42. Fruman D.A., Rommel C. PI3K and cancer: lessons, challenges and opportunities. Nat. Rev. Drug Discov 2014, 13:140-156.
43. Ruggeri B.A., Huang L., Wood M., Cheng J.Q., Testa J.R. Amplification and overexpression of the AKT2 oncogene in a subset of human pancreatic ductal adenocarcinomas. Mol. Carcinog 1998, 21:81-86.
44. Cheng J.Q., Ruggeri B., Klein W.M., Sonoda G., Altomare D.A., Watson D.K., et al. Amplification of AKT2 in human pancreatic cells and inhibition of AKT2 expression and tumorigenicity by antisense RNA. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:3636-3641.
45. Altomare D.A., Tanno S., De Rienzo A., Klein-Szanto A.J., Skele K.L., Hoffman J.P., et al. Frequent activation of AKT2 kinase in human pancreatic carcinomas. J. Cell. Biochem 2002, 87:470-476.
46. Trendelenburg A.U., Meyer A., Rohner D., Boyle J., Hatakeyama S., Glass D.J. Myostatin reduces Akt/TORC1/p70S6K signaling, inhibiting myoblast differentiation and myotube size. Am. J. Physiol. Cell Physiol 2009, 296:1258-1270.
47. Sartori R., Milan G., Patron M., Mammucari C., Blaauw B., Abraham R., et al. Smad2 and 3 transcription factors control muscle mass in adulthood. Am. J. Physiol. Cell Physiol 2009, 296:1248-1257.
48. Lokireddy S., Mouly V., Butler-Browne G., Gluckman P.D., Sharma M., Kambadur R., et al. Myostatin promotes the wasting of human myoblast cultures through promoting ubiquitin-proteasome pathway-mediated loss of sarcomeric proteins. Am. J. Physiol. Cell Physiol 2011, 301:1316-1324.
49. Leto G., Incorvaia L., Badalamenti G., Tumminello F.M., Gebbia N., Flandina C., et al. Activin A circulating levels in patients with bone metastasis from breast or prostate cancer. Clin. Exp. Metastasis 2006, 23:117-122.