TGF-β and NF-κB signal pathway cross-talk is mediated through TAK1 and SMAD7 in a subset of head and neck cancers

Oncogene

Volumn 32, Issue 12, 2013, Pages 1549-1559

  Freudlsperger, C ^a,b   Bian, Y ^a   Contag Wise, S ^a,c   Burnett, J ^a   Coupar, J ^a   Yang, X ^a   Chen, Z ^a   Van Waes, C ^a  

^a NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c PFIZER INC   (United States)

Author keywords

celastrol; head and neck cancer; NF kB; SMAD7; TGF b TAK1

Indexed keywords

CELASTROL; DNA; I KAPPA B ALPHA; I KAPPA B KINASE; LIPOCORTIN 5; SMAD7 PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RELA; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TRANSFORMING GROWTH FACTOR BETA2;

APOPTOSIS; ARTICLE; CELL NUCLEUS; CELL PROLIFERATION; DNA FRAGMENTATION; ENZYME PHOSPHORYLATION; GENE SILENCING; HEAD AND NECK CANCER; MIGRATION INHIBITION; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN TRANSPORT;

CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; HEAD AND NECK NEOPLASMS; HUMANS; MAP KINASE KINASE KINASES; NEOPLASM INVASIVENESS; NF-KAPPA B; SIGNAL TRANSDUCTION; SMAD7 PROTEIN; TRANSCRIPTION FACTOR RELA; TRANSFORMING GROWTH FACTOR BETA;

EID: 84884211557     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.171     Document Type: Article

References (61)

1. Siegel P, Massagué J. Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 2003; 3: 807-821.
2. Cui W, Fowlis D, Bryson S, Duffie E, Ireland H, Balmain A et al. TGFbeta1 inhibits the formation of benign skin tumors, but enhances progression to invasive spindle carcinomas in transgenic mice. Cell 1996; 86: 531-542.
3. Attisano L, Lee-Hoeflich S. The Smads. Genome Biol 2001; 2: REVIEWS3010 (e-pub ahead of print 2 August 2001).
4. Massagué J. TGFbeta in Cancer. Cell 2008; 134: 215-230.
5. White RA, Malkoski SP, Wang XJ. TGFb signaling in head and neck squamous cell carcinoma. Oncogene 2010; 29: 5437-5446.
6. Bian Y, Terse A, Du J, Hall B, Molinolo A, Zhang P et al. Progressive tumor formation in mice with conditional deletion of TGF-beta signaling in head and neck epithelia is associated with activation of the PI3K/Akt pathway. Cancer Res 2009; 69: 5918-5926.
7. Bornstein S, White R, Malkoski S, Oka M, Han G, Cleaver T et al. Smad4 loss in mice causes spontaneous head and neck cancer with increased genomic instability and inflammation. J Clin Invest 2009; 119: 3408-3419.
8. Lu SL, Herrington H, Reh D, Weber S, Bornstein S, Wang D et al. Loss of transforming growth factor-beta type II receptor promotes metastatic head-and-neck squamous cell carcinoma. Genes Dev 2006; 20: 1331-1342.
9. Cohen J, Chen Z, Lu S, Yang X, Arun P, Ehsanian R et al. Attenuated transforming growth factor beta signaling promotes nuclear factor-kappaB activation in head and neck cancer. Cancer Res 2009; 69: 3415-3424.
10. Van Waes C. Nuclear factor-kB in development, prevention, and therapy of cancer. Clin Cancer Res 2007; 13: 1076-1082.
11. Wolf JS, Chen Z, Dong G, Sunwoo JB, Bancroft CC, Capo DE et al. Interleukin-1a promotes nuclear factor kappaB and AP-1-induced IL-8 expression, cell survival and proliferation in head and neck squamous cell carcinoma. Clin Cancer Res 2001; 7: 1812-1820.
12. Jackson-Bernitsas DG, Ichikawa H, Takada Y, Myers JN, Lin XL, Darnay BG et al. Evidence that TNF-TNFR1-TRADD-TRAF2-RIP-TAK1-IKK pathway mediates constitutive NF-kB activation and proliferation in human head and neck squamous cell carcinoma. Oncogene 2007; 26: 1385-1397.
13. Sakurai H, Miyoshi H, Toriumi W, Sugita T. Functional interactions of transforming growth factor beta-activated kinase 1 with IkappaB kinases to stimulate NFkappaB activation. J Biol Chem 1999; 274: 10641-10648.
14. Takaesu G, Kishida S, Hiyama A, Yamaguchi K, Shibuya H, Irie K et al. TAB2, a novel adaptor protein, mediates activation of TAK1 MAPKKK by linking TAK1 to TRAF6 in the IL-1 signal transduction pathway. Mol Cell 2000; 5: 649-658.
15. Hong S, Lim S, Li A, Lee C, Lee Y, Lee E et al. Smad7 binds to the adaptors TAB2 and TAB3 to block recruitment of the kinase TAK1 to the adaptor TRAF2. Nat Immunol 2007; 8: 504-513.
16. Zhang Y. Non-Smad pathways in TGF-beta signaling. Cell Res 2009; 19: 128-139.
17. Solt LA, May MJ. The IkappaB kinase complex: master regulator of NF-kappaB signaling. Immunol Res 2008; 42: 3-18.
18. Baldwin AJ. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu Rev Immunol 1996; 14: 649-683.
19. Perkins ND. The diverse and complex roles of NF-kB subunits in cancer. Nat Rev Cancer 2012; 12: 121-132.
20. Bitzer M, von Gersdorff G, Liang D, Dominguez-Rosales A, Beg A, Rojkind M et al. A mechanism of suppression of TGF-beta/SMAD signaling by NF-kappa B/RelA. Genes Dev 2000; 14: 187-197.
21. Derynck R, Smad-dependent Zhang Y. and Smad-independent pathways in TGFbeta family signalling. Nature 2003; 425: 577-584.
22. Hong S, Lee C, Kim S. Smad7 sensitizes tumor necrosis factor induced apoptosis through the inhibition of antiapoptotic gene expression by suppressing activation of the nuclear factor-kappaB pathway. Cancer Res 2007; 67: 9577-9583.
23. Sethi G, Ahn K, Pandey M, Aggarwal B. Celastrol a novel triterpene, potentiates TNF-induced apoptosis and suppresses invasion of tumor cells by inhibiting NFkappaB-regulated gene products and TAK1-mediated NF-kappaB activation. Blood 2007; 109: 2727-2735.
24. Brenner JC, Graham MP, Kumar B, Saunders LM, Kupfer R, Lyons RH et al. Genotyping of 73 UM-SCC head and neck squamous cell carcinoma cell lines. Head Neck 2010; 32: 1195-1201.
25. Reiss M, Stash E. High frequency of resistance of human squamous carcinoma cells to the anti-proliferative action of transforming growth factor beta. Cancer Commun 1990; 2: 363-369.
26. Zhang PL, Pellitteri PK, Law A, Gilroy PA, Wood GC, Kennedy TL et al. Overexpression of phosphorylated nuclear factor-kappa B in tonsillar squamous cell carcinoma and high-grade dysplasia is associated with poor prognosis. Mod Pathol 2005; 18: 924-932.
27. Yamaguchi K, Shirakabe K, Shibuya H, Irie K, Oishi I, Ueno N et al. Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction. Science 1995; 270: 2008-2011.
28. Yamashita M, Fatyol K, Jin C, Wang X, Liu Z, Zhang YE. TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-beta. Mol Cell 2008; 31: 918-924.
29. Sorrentino A, Thakur N, Grimsby S, Marcusson A, von Bulow V, Schuster N et al. The type I TGF-beta receptor engages E3ligase TRAF6 to turn on the kinase TAK1 to kill prostate cancer cells. Nat Cell Biol 2008; 10: 1199-1207.
30. Mu Y, Gudey SK, Landstrom M. Non-Smad signaling pathways. Cell Tissue Res 2012; 347: 11-20.
31. Lam LT, Davis RE, Pierce J, Hepperle M, Xu Y, Hottelet M et al. Small molecule inhibitors of IkB kinase are selectively toxic for subgroups of diffuse large B-cell lymphoma defined by gene expression profiling. Clin Cancer Res 2005; 11: 28-40.
32. Setty A, Sigal L. Herbal medications commonly used in the practice of rheumatology: mechanisms of action, efficacy, and side effects. Semin Arthritis Rheum 2005; 34: 773-784.
33. Hayashi H, Abdollah S, Qiu Y, Cai J, Xu YY, Grinnell BW et al. The MAD-related protein Smad7 associates with the TGFbeta receptor and functions as an antagonist of TGFbeta signaling. Cell 1997; 89: 1165-1173.
34. Arsura M, Panta GR, Bilyeu JD, Cavin LG, Sovak MA et al. Transient activation of TAK1/IKK kianse pathway by TGF-beta1 inhibits AP-1/SMAD signaling and apoptosis: implications in liver tumor formation. Hepatology 2003; 38: 1540-1551.
35. Dowdy SC, Mariani A, Janknect R. HER2/Neu-and TAK1-mediated up-regulation of the transforming growth factor beta inhibitor Smad7 via the ETS protein ER81. J Biol Chem 2003; 278: 44377-44384.
36. Edlund S, Bu S, Schuster N, Aspenstrom P, Heuchel R, Heldin NE et al. Transforming growth factor-beta1 (TGF-beta)-induced apoptosis of prostate cancer cells involves Smad-7 dependent activation of p38 by TGF-beta-activated kinase-1 and mitogen-activated protein kinase kinase 3. Mol Biol Cell 2003; 14: 529-524.
37. Yasui T, Kadono Y, Nakamura M, Oshima Y, Matsumoto T, Masuda H et al. Regulation of RANKL-induced osteoclatogenesis by TGF-b through molecular interaction between Smad3 and Traf6. J Bone Miner Res 2011; 26: 1447-1456.
38. Hahn S, Schutte M, Hoque A, Moskaluk C, da Costa L, Rozenblum E et al. DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 1996; 271: 350-353.
39. Xie W, Bharathy S, Kim D, Haffty B, Rimm D, Reiss M. Frequent alterations of Smad signaling in human head and neck squamous cell carcinomas: a tissue microarray analysis. Oncol Res 2003; 14: 61-73.
40. Jadrich JL, O'Conner MB, Coucouvanis E. Expression of TAK1, a mediator of TGF-b and BMP signaling, during mouse embryonic development. Gene Expr Patterns 2003; 3: 131-134.
41. Chatterjee A, Chang X, Sen T, Ravi R, Bedi A, Sidransky D. Regulation of p53 family member isoform deltaNp63alpha by the nuclear factor-kappaB targeting kinase IkappaBbeta. Cancer Res 2010; 70: 1419-1429.
42. Irie T, Muta T, Takeshige K. TAK1 mediates an activation signal from toll-like receptor(s) to nuclear factor-kappaB in lipopolysaccharide-stimulated macrophages. FEBS Lett 2000; 467: 160-164.
43. Ninomiya-Tsuji J, Kishimoto K, Hiyama A, Inoue J, Cao Z, Matsumoto K. The kinase TAK1 can activate the NIK-I kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 1999; 398: 252-256.
44. Calixto J, Campos M, Otuki M, Santos A. Anti-inflammatory compounds of plant origin. Part II. modulation of pro-inflammatory cytokines, chemokines and adhesion molecules. Planta Med 2004; 70: 93-103.
45. Li H, Zhang Y, Huang X, Sun Y, Jia Y, Li D. Beneficial effect of tripterine on systemic lupus erythematosus induced by active chromatin in BALB/c mice. Eur J Pharmacol 2005; 512: 231-237.
46. Tao X, Younger J, Fan F, Wang B, Lipsky P. Benefit of an extract of Tripterygium Wilfordii Hook F in patients with rheumatoid arthritis: a double-blind, placebocontrolled study. Arthritis Rheum 2002; 46: 1735-1743.
47. Yang H, Chen D, Cui Q, Yuan X, Dou Q. Celastrol, a triterpene extracted from the Chinese 'Thunder of God Vine,' is a potent proteasome inhibitor and suppresses human prostate cancer growth in nude mice. Cancer Res 2006; 66: 4758-4765.
48. Azuma M, Motegi K, Aota K, Yamashita T, Yoshida H, Sato M. TGF-beta1 inhibits NF-kappaB activity through induction of IkappaB-alpha expression in human salivary gland cells: a possible mechanism of growth suppression by TGF-beta1. Exp Cell Res 1999; 250: 213-222.
49. Sovak M, Arsura M, Zanieski G, Kavanagh K, Sonenshein G. The inhibitory effects of transforming growth factor beta1 on breast cancer cell proliferation are mediated through regulation of aberrant nuclear factor-kappaB/Rel expression. Cell Growth Differ 1999; 10: 537-544.
50. Arsura M, Wu M, Sonenshein G. TGF beta 1 inhibits NF-kappa B/Rel activity inducing apoptosis of B cells: transcriptional activation of I kappa B alpha. Immunity 1996; 5: 31-40.
51. Arsura M, FitzGerald M, Fausto N, Sonenshein G. Nuclear factor-kappaB/Rel blocks transforming growth factor beta1-induced apoptosis of murine hepatocyte cell lines. Cell Growth Differ 1997; 8: 1049-1059.
52. Sheng H, Shao J, O'Mahony C, Lamps L, Albo D, Isakson P et al. Transformation of intestinal epithelial cells by chronic TGF-beta1 treatment results in downregulation of the type II TGF-beta receptor and induction of cyclooxygenase-2. Oncogene 1999; 18: 855-867.
53. Lu T, Burdelya L, Swiatkowski S, Boiko A, Howe P, Stark G et al. Secreted transforming growth factor beta2 activates NF-kappaB, blocks apoptosis, and is essential for the survival of some tumor cells. Proc Natl Acad Sci USA 2004; 101: 7112-7117.
54. Bhowmick N, Ghiassi M, Bakin A, Aakre M, Lundquist C, Engel M et al. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol Biol Cell 2001; 12: 27-36.
55. Wang W, Huang XR, Li AG, Liu F, Li JH, Truong LD et al. Signaling mechanism of TGF-b1 in prevention of renal inflammation: Role of Smad7. J Am Soc Nephrol 2005; 16: 1371-1383.
56. Yan B, Yang X, Lee TL, Friedman J, Tang J, Van Waes C et al. Genome-wide identification of novel expression signatures reveal distinct patterns and prevalence of binding motifs for p53, nuclear factor-kappaB and other signal transcription factors in head and neck squamous cell carcinoma. Genome Biol 2007; 8: R78.
57. Friedman J, Nottingham L, Duggal P, Pernas FG, Yan B, Yang XP et al. Deficient TP53 expression, function, and cisplatin sensitivity are restored by quinacrine in head and neck cancer. Clin Cancer Res 2007; 13: 6568-6578.
58. Lee TL, Yeh J, Friedman J, Yan B, Yang X, Yeh NT et al. A signal network involving coactivated NF-kappaB and STAT3 and altered p53 modulates BAX/BCL-XL expression and promotes cell survival of head and neck squamous cell carcinomas. Int J Cancer 2008; 122: 1987-1998.
59. Bancroft CC, Chen Z, Yeh J, Sunwoo JB, Yeh NT, Jackson S et al. Effects of pharmacologic antagonists of epidermal growth factor receptor, PI3K and MEK signal kinases on NF-kappaB and AP-1 activation and IL-8 and VEGF expression in human head and neck squamous cell carcinoma lines. Int J Cancer 2002; 99: 538-548.
60. Wrana JL, Attisano L, Carcamo J, Zentella A, Doody J, Laiho M et al. TGF beta signals through a heteromeric protein kinase receptor complex. Cell 1992; 71: 1003-1014.
61. Dennler S, Itoh S, Vivien D, ten Dijke P, Huet S, Gauthier JM. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J 1998; 17: 3091-3100.