Activin upregulation by NF-κB is required to maintain mesenchymal features of cancer stem-like cells in non-small cell lung cancer

Cancer Research

Volumn 75, Issue 2, 2015, Pages 426-435

  Wamsley, J Jacob ^a   Kumar, Manish ^a   Allison, David F ^a   Clift, Sheena H ^a   Holzknecht, Caitlyn M ^a   Szymura, Szymon J ^a   Hoang, Stephen A ^a   Xu, Xiaojiang ^a   Moskaluk, Christopher A ^a   Jones, David R ^a,b   Bekiranov, Stefan ^a   Mayo, Marty W ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ACTIVIN; INHIBIN; INHIBIN BETA A SUBUNIT; RNA;

ACTIVIN A GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER STEM CELL; CONTROLLED STUDY; DISEASE ASSOCIATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; LUNG METASTASIS; MOLECULAR PATHOLOGY; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; BIOSYNTHESIS; GENETICS; LUNG TUMOR; MESODERM; METABOLISM; MULTICELLULAR SPHEROID; PATHOLOGY; TUMOR CELL LINE; UPREGULATION;

ACTIVINS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; INHIBIN-BETA SUBUNITS; LUNG NEOPLASMS; MESODERM; NEOPLASTIC STEM CELLS; NF-KAPPA B; RNA, NEOPLASM; SPHEROIDS, CELLULAR; UP-REGULATION;

EID: 84920982352     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-2702     Document Type: Article

References (49)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013;63:11-30.
2. Scheel C, Weinberg RA. Cancer stem cells and epithelial-mesenchymal transition: concepts and molecular links. Semin Cancer Biol 2012;22: 396-403.
3. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 2008;14: 818-29.
4. Heldin C-H, Vanlandewijck M, Moustakas A. Regulation ofEMTby TGFb in cancer. FEBS Lett 2012;586:1959-70.
5. Wendt MK, Tian M, Schiemann WP. Deconstructing the mechanisms and consequences of TGF-b-induced EMT during cancer progression. Cell Tissue Res 2012;347:85-101.
6. Wakefield LM, Hill CS. Beyond TGFb: roles of other TGFb superfamily members in cancer. Nat Rev Cancer 2013;13:328-41.
7. Asiedu MK, Ingle JN, Behrens MD, Radisky DC, Knutson KL. TGFb/TNFa-mediated epithelial-mesenchymal transition generates breast cancer stem cells with a claudin-low phenotype. Cancer Res 2011;71: 4707-19.
8. Kawata M, Koinuma D, Ogami T, Umezawa K, Iwata C, Watabe T, et al. TGF-b-induced epithelial-mesenchymal transition of A549 lung adenocarcinoma cells is enhanced by pro-inflammatory cytokines derived from RAW 264. 7 macrophage cells. J Biochem 2012;151:205-16.
9. KumarM, AllisonDF, Baranova NN, Wamsley JJ, Katz AJ, Bekiranov S, et al. NF-kB regulates mesenchymal transition for the induction of non-small cell lung cancer initiating cells. PLoS ONE 2013;8:e68597.
10. Baldwin AS. Regulation of cell death and autophagy by IKK and NF-kB: critical mechanisms in immune function and cancer. Immunol Rev 2012;246:327-45.
11. Basseres DS, Baldwin AS. Nuclear factor-kB and inhibitor of kB kinase pathways in oncogenic initiation and progression. Oncogene 2006;25: 6817-30.
12. Allison DF, Wamsley JJ, Kumar M, Li D, Gray LG, Hart GW, et al. Modification of RelA by O-linked N-acetylglucosamine links glucose metabolism to NF-kB acetylation and transcription. Proc Natl Acad Sci U S A 2012;109:16888-93.
13. Chen L, Mu Y, Greene WC. Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kB. EMBO J 2002;21:6539-48.
14. Duran A, Diaz-Meco MT, Moscat J. Essential role of RelA Ser311 phosphorylation by zetaPKC in NF-kB transcriptional activation. EMBO J 2003;22:3910-8.
15. Hoberg JE, Popko AE, Ramsey CS, Mayo MW. IkB kinase a-mediated derepression of SMRT potentiates acetylation of RelA/p65 by p300. Mol Cell Biol 2006;26:457-71.
16. Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR, Frye RA, et al. Modulation of NF-kB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J 2004;23:2369-80.
17. Zhong H, May MJ, Jimi E, Ghosh S. The phosphorylation status of nuclear NF-kB determines its association with CBP/p300 or HDAC-1. Mol Cell 2002;9:625-36.
18. ChenW, Li Z, Bai L, Lin Y. NF-kB in lung cancer, a carcinogenesismediator and a prevention and therapy target. Front Biosci 2011;16:1172-85.
19. Cao Y, Luo J-L, Karin M. IkB kinase a kinase activity is required for selfrenewal of ErbB2/Her2-transformedmammary tumor-initiating cells. Proc Natl Acad Sci U S A 2007;104:15852-7.
20. Liu M, Sakamaki T, Casimiro MC, Willmarth NE, Quong AA, Ju X, et al. The canonical NF-kB pathway governs mammary tumorigenesis in transgenic mice and tumor stem cell expansion. Cancer Res 2010;70:10464-73.
21. Kendellen MF, Bradford JW, Lawrence CL, Clark KS, Baldwin AS. Canonical and non-canonical NF-kB signaling promotes breast cancer tumor-initiating cells. Oncogene 2014;33:1297-305.
22. Wu Z, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F. A modelbased background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 2004;99:909-17.
23. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004;3:Article3. Epub 2004 Feb 12.
24. Jones DR, Moskaluk CA, Gillenwater HH, Petroni GR, Burks SG, Philips J, et al. Phase I trial of induction histone deacetylase and proteasome inhibition followed by surgery in non-small cell lung cancer. J Thorac Oncol 2012;7:1683-90.
25. Facoetti A, Pasi F, Nano R. Some considerations for the study of TGFb in medium of irradiated T98G cells: activation, release and consumption. Anticancer Res 2010;30:3341-4.
26. Cieslik M, Hoang SA, Baranova N, Chodaparambil S, Kumar M, Allison D, et al. Epigenetic coordination of signaling pathways during the epithelialmesenchymal transition. Epigenetics Chromatin 2013;6:28.
27. Chen Y, Zhang Y, Yin Y, Gao G, Li S, Jiang Y, et al. SPD-aweb-based secreted protein database. Nucleic Acids Res 2005;33:D169-73.
28. Antsiferova M, Werner S. The bright and the dark sides of activin in wound healing and cancer. J Cell Sci 2012;125:3929-37.
29. Vallier L, Alexander M, Pedersen RA. Activin/Nodal and FGF pathways cooperate tomaintain pluripotency of human embryonic stem cells. J Cell Sci 2005;118:4495-509.
30. Xiao L, Yuan X, Sharkis SJ. Activin A maintains self-renewal and regulates fibroblast growth factor, Wnt, and bone morphogenic protein pathways in human embryonic stem cells. Stem Cells 2006;24:1476-86.
31. Cerdan C, McIntyre BAS, Mechael R, Levadoux-Martin M, Yang J, Lee JB, et al. Activin A promotes hematopoietic fated mesoderm development through upregulation of brachyury in human embryonic stem cells. Stem Cells Dev 2012;21:2866-77.
32. D'Amour KA, Agulnick AD, Eliazer S, Kelly OG, Kroon E, Baetge EE. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol 2005;23:1534-41.
33. Green JB, Smith JC. Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature 1990;347:391-4.
34. Lonardo E, Hermann PC, 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;9:433-46.
35. Topczewska JM, Postovit L-M, Margaryan NV, Sam A, Hess AR, Wheaton WW, et al. Embryonic and tumorigenic pathways converge via Nodal signaling: role in melanoma aggressiveness. Nat Med 2006;12: 925-32.
36. HuberMA, Azoitei N, Baumann B, Grunert S, Sommer A, Pehamberger H, et al. NF-kB is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression. J Clin Invest 2004;114: 569-81.
37. Inman GJ, Nicolas FJ, Callahan JF, Harling JD, Gaster LM, Reith AD, et al. SB-431542 is a potent and specific inhibitor of TGFb superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol Pharmacol 2002;62:65-74.
38. Floor S, van Staveren WCG, LarsimontD, Dumont JE, Maenhaut C. Cancer cells in epithelial-to-mesenchymal transition and tumor-propagating-cancer stem cells: distinct, overlapping or same populations. Oncogene 2011;30:4609-21.
39. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008;133:704-15.
40. Morel A-P, Lievre M, Thomas C, Hinkal G, Ansieau S, Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS ONE 2008;3:e2888.
41. Scheel C, Eaton EN, Li SH-J, Chaffer CL, Reinhardt F, Kah K-J, et al. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 2011;145:926-40.
42. Cai KX, Tse LY, Leung C, Tam PKH, Xu R, Sham MH. Suppression of lung tumor growth and metastasis in mice by adeno-associated virus-mediated expression of vasostatin. Clin Cancer Res 2008;14:939-49.
43. Meuwissen R, Berns A. Mouse models for human lung cancer. Genes Dev 2005;19:643-64.
44. Seder CW, Hartojo W, Lin L, Silvers AL, Wang Z, Thomas DG, et al. Upregulated INHBA expression may promote cell proliferation and is associated with poor survival in lung adenocarcinoma. Neoplasia 2009;11:388-96.
45. Kimlin LC, Casagrande G, Virador VM. In vitro three-dimensional (3D) models in cancer research: an update. Mol Carcinog 2013;52:167-82.
46. Nurwidya F, Murakami A, Takahashi F, Takahashi K. Lung cancer stem cells: tumor biology and clinical implications. Asia Pac J Clin Oncol 2012;8:217-22.
47. Yi S-Y,Hao Y-B, Nan K-J, Fan T-L. Cancer stem cells niche: a target for novel cancer therapeutics. Cancer Treat Rev 2013;39:290-6.
48. Yoshinaga K, Yamashita K, Mimori K, Tanaka F, Inoue H, Mori M. Activin A causes cancer cell aggressiveness in esophageal squamous cell carcinoma cells. Ann Surg Oncol 2008;15:96-103.
49. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, et al. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 2004;6:1-6.