Activin and TGFβ use diverging mitogenic signaling in advanced colon cancer

Molecular Cancer

Volumn 14, Issue 1, 2015, Pages

  Bauer, Jessica ^a   Ozden, Ozkan ^a   Akagi, Naomi ^a   Carroll, Timothy ^a   Principe, Daniel R ^a   Staudacher, Jonas J ^a   Spehlmann, Martina E ^b   Eckmann, Lars ^c   Grippo, Paul J ^a   Jung, Barbara ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Activin; Colon cancer; Mitogenic signaling; P21; PI3K; TGF

Indexed keywords

ACTIVIN; PROTEIN P21; PROTEIN P85; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; ACTIVIN RECEPTOR 2; ACTIVIN RECEPTOR TYPE II-A; PHOSPHATIDYLINOSITOL 3 KINASE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CELL MIGRATION; COLON CANCER; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; EPITHELIAL MESENCHYMAL TRANSITION; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; UPREGULATION; ANIMAL; COLON TUMOR; GENETICS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN VITRO STUDY; KNOCKOUT MOUSE; METABOLISM; TUMOR CELL LINE; WESTERN BLOTTING;

ACTIVIN RECEPTORS, TYPE II; ACTIVINS; ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; COLONIC NEOPLASMS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN VITRO TECHNIQUES; MICE; MICE, KNOCKOUT; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS P21(RAS); RECEPTORS, TRANSFORMING GROWTH FACTOR BETA;

EID: 84945130735     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/s12943-015-0456-4     Document Type: Article

References (52)

1. SEER Stat Fact Sheets: Colon and Rectum Cancer 2014. Available from: (http://seer.cancer.gov/statfacts/html/colorect.html ).
2. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz Jr LA, Kinzler KW. Cancer genome landscapes. Science. 2013;339(6127):1546-58.
3. Massague J. TGFbeta signalling in context. Nat Rev Mol Cell Biol. 2012;13(10):616-30.
4. Loomans HA, Andl CD. Intertwining of activin a and TGFb signaling: dual roles in cancer progression and cancer cell invasion. Cancers. 2014;7:70-91.
5. Principe DR, Doll JA, Bauer J, Jung B, Munshi HG, Bartholin L, et al. TGF-beta: duality of function between tumor prevention and carcinogenesis. J Natl Cancer Inst. 2014;106(2):djt369.
6. Mathews LS, Vale WW. Expression cloning of an activin receptor, a predicted transmembrane serine kinase. Cell. 1991;65(6):973-82.
7. Gray PC, Greenwald J, Blount AL, Kunitake KS, Donaldson CJ, Choe S, et al. Identification of a binding site on the type II activin receptor for activin and inhibin. J Biol Chem. 2000;275(5):3206-12.
8. Chen YG, Wang Q, Lin SL, Chang CD, Chuang J, Ying SY. Activin signaling and its role in regulation of cell proliferation, apoptosis, and carcinogenesis. Exp Biol Med. 2006;231(5):534-44.
9. Bauer J, Sporn JC, Cabral J, Gomez J, Jung B. Effects of activin and TGFbeta on p21 in colon cancer. PLoS One. 2012;7(6), e39381.
10. Massague J. TGFbeta in Cancer. Cell. 2008;134(2):215-30.
11. Meulmeester E, Ten Dijke P. The dynamic roles of TGF-beta in cancer. J Pathol. 2011;223(2):205-18.
12. Chen YG, Lui HM, Lin SL, Lee JM, Ying SY. Regulation of cell proliferation, apoptosis, and carcinogenesis by activin. Exp Biol Med (Maywood). 2002;227(2):75-87.
13. Watanabe T, Wu TT, Catalano PJ, Ueki T, Satriano R, Haller DG, et al. Molecular predictors of survival after adjuvant chemotherapy for colon cancer. N Engl J Med. 2001;344(16):1196-206.
14. Calon A, Lonardo E, Berenguer-Llergo A, Espinet E, Hernando-Momblona X, Iglesias M, et al. Stromal gene expression defines poor-prognosis subtypes in colorectal cancer. Nat Genet. 2015;47(4):320-9.
15. Togashi Y, Kogita A, Sakamoto H, Hayashi H, Terashima M, de Velasco MA, et al. Activin signal promotes cancer progression and is involved in cachexia in a subset of pancreatic cancer. Cancer Lett. 2015;356(2 Pt B):819-27.
16. Fleming NI, Jorissen RN, Mouradov D, Christie M, Sakthianandeswaren A, Palmieri M, et al. SMAD2, SMAD3 and SMAD4 mutations in colorectal cancer. Cancer Res. 2013;73(2):725-35.
17. Valcourt U, Kowanetz M, Niimi H, Heldin CH, Moustakas A. TGF-beta and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition. Mol Biol Cell. 2005;16(4):1987-2002.
18. Piek E, Moustakas A, Kurisaki A, Heldin CH, ten Dijke P. TGF-(beta) type I receptor/ALK-5 and Smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells. J Cell Sci. 1999;112(Pt 24):4557-68.
19. Levy L, Hill CS. Alterations in components of the TGF-beta superfamily signaling pathways in human cancer. Cytokine Growth Factor Rev. 2006;17(1-2):41-58.
20. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139(5):871-90.
21. de Lima MD, Marques YM, Alves Sde Jr M, Freitas VM, Soares FA, de Araujo VC, et al. MDM2, P53, P21WAF1 and pAKT protein levels in genesis and behaviour of adenoid cystic carcinoma. Cancer Epidemiol. 2009;33(2):142-6.
22. Wang H, Wang HS, Zhou BH, Li CL, Zhang F, Wang XF, et al. Epithelial-mesenchymal transition (EMT) induced by TNF-alpha requires AKT/GSK-3beta-mediated stabilization of snail in colorectal cancer. PLoS One. 2013;8(2), e56664.
23. Liu P, Cheng H, Roberts TM, Zhao JJ. Targeting the phosphoinositide 3-kinase pathway in cancer. Nat Rev Drug Discov. 2009;8(8):627-44.
24. Vivanco I, Sawyers CL. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer. 2002;2(7):489-501.
25. Maurer G, Tarkowski B, Baccarini M. Raf kinases in cancer-roles and therapeutic opportunities. Oncogene. 2011;30(32):3477-88.
26. Saif MW, Chu E. Biology of colorectal cancer. Cancer J. 2010;16(3):196-201.
27. Yung HW, Charnock-Jones DS, Burton GJ. Regulation of AKT phosphorylation at Ser473 and Thr308 by endoplasmic reticulum stress modulates substrate specificity in a severity dependent manner. PLoS One. 2011;6(3), e17894.
28. Heldin CH, Vanlandewijck M, Moustakas A. Regulation of EMT by TGFbeta in cancer. FEBS Lett. 2012;586(14):1959-70.
29. Liu M, Casimiro MC, Wang C, Shirley LA, Jiao X, Katiyar S, et al. p21CIP1 attenuates Ras- and c-Myc-dependent breast tumor epithelial mesenchymal transition and cancer stem cell-like gene expression in vivo. Proc Natl Acad Sci U S A. 2009;106(45):19035-9.
30. Grady WM, Carethers JM. Genomic instability and molecular pathogenesis of colorectal cancer. Gastroenterology. 2008;4(135):1079-99.
31. Jung BH, Beck SE, Cabral J, Chau E, Cabrera BL, Fiorino A, et al. Activin type 2 receptor restoration in MSI-H colon cancer suppresses growth and enhances migration with activin. Gastroenterology. 2007;132(2):633-44.
32. Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2013;487:330-7.
33. Jung B, Gomez J, Chau E, Cabral J, Lee JK, Anselm A, et al. Activin signaling in microsatellite stable colon cancers is disrupted by a combination of genetic and epigenetic mechanisms. PLoS One. 2009;4(12), e8308.
34. Grady WM, Myeroff LL, Swinler SE, Rajput A, Thiagalingam S, Lutterbaugh JD, et al. Mutational inactivation of transforming growth factor beta receptor type II in microsatellite stable colon cancers. Cancer Res. 1999;59(2):320-4.
35. Jung B, Smith EJ, Doctolero RT, Gervaz P, Alonso JC, Miyai K, et al. Influence of target gene mutations on survival, stage and histology in sporadic microsatellite unstable colon cancers. Int J Cancer. 2006;118(10):2509-13.
36. Kang HY, Shyr CR. Activins and cell migration. Vitam Horm. 2011;85:129-48.
37. Tol J, Koopman M, Cats A, Rodenburg CJ, Creemers GJ, Schrama JG, et al. Chemotherapy, bevacizumab, and cetuximab in metastatic colorectal cancer. N Engl J Med. 2009;360(6):563-72.
38. Soares HP, Ming M, Mellon M, Young SH, Han L, Sinnet-Smith J, et al. Dual PI3K/mTOR inhibitors induce rapid overactivation of the MEK/ERK pathway in human pancreatic cancer cells through suppression of mTORC2. Mol Cancer Ther. 2015;14(4):1014-23.
39. Yi JY, Shin I, Arteaga CL. Type I transforming growth factor beta receptor binds to and activates phosphatidylinositol 3-kinase. J Biol Chem. 2005;280(11):10870-6.
40. Zhao L, Vogt PK. Class I PI3K in oncogenic cellular transformation. Oncogene. 2008;27(41):5486-96.
41. McCubrey JA, Steelman LS, Abrams SL, Lee JT, Chang F, Bertrand FE, et al. Roles of the RAF/MEK/ERK and PI3K/PTEN/AKT pathways in malignant transformation and drug resistance. Adv Enzyme Regul. 2006;46:249-79.
42. Xu J, Acharya S, Sahin O, Zhang Q, Saito Y, Yao J, et al. 14-3-3zeta turns TGF-beta's function from tumor suppressor to metastasis promoter in breast cancer by contextual changes of Smad partners from p53 to Gli2. Cancer Cell. 2015;27(2):177-92.
43. Abbas T, Dutta A. p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer. 2009;9(6):400-14.
44. Deng C, Zhang P, Harper JW, Elledge SJ, Leder P. Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell. 1995;82(4):675-84.
45. Brugarolas J, Chandrasekaran C, Gordon JI, Beach D, Jacks T, Hannon GJ. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature. 1995;377(6549):552-7.
46. Wang J, Yang L, Yang J, Kuropatwinski K, Wang W, Liu XQ, et al. Transforming growth factor beta induces apoptosis through repressing the phosphoinositide 3-kinase/AKT/survivin pathway in colon cancer cells. Cancer Res. 2008;68(9):3152-60.
47. Ansieau S, Bastid J, Doreau A, Morel AP, Bouchet BP, Thomas C, et al. Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell. 2008;14(1):79-89.
48. Barrallo-Gimeno A, Nieto MA. The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development. 2005;132(14):3151-61.
49. Piek E, Van Dinther M, Parks WT, Sallee JM, Bottinger EP, Roberts AB, et al. RLP, a novel Ras-like protein, is an immediate-early transforming growth factor-beta (TGF-beta) target gene that negatively regulates transcriptional activity induced by TGF-beta. Biochem J. 2004;383(Pt 1):187-99.
50. Chen Y, Lebrun JJ, Vale W. Regulation of transforming growth factor beta- and activin-induced transcription by mammalian Mad proteins. Proc Natl Acad Sci U S A. 1996;93(23):12992-7.
51. Chow JY, Cabral JA, Chang J, Carethers JM. TGFbeta modulates PTEN expression independently of SMAD signaling for growth proliferation in colon cancer cells. Cancer Biol Ther. 2008;7(10):1694-9.
52. Jung B, Doctolero RT, Tajima A, Nguyen AK, Keku T, Sandler RS, et al. Loss of activin receptor type 2 protein expression in microsatellite unstable colon cancers. Gastroenterology. 2004;126(3):654-9.