Atypical mechanism of NF-κB activation by TRE17/ubiquitin-specific protease 6 (USP6) oncogene and its requirement in tumorigenesis

Oncogene

Volumn 31, Issue 30, 2012, Pages 3525-3535

  Pringle, L M ^a   Young, R ^a   Quick, L ^a   Riquelme, D N ^a   Oliveira, A M ^b   May, M J ^c   Chou, M M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b MAYO CLINIC   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

aneurysmal bone cyst; I B; NF B; TRE17; USP6

Indexed keywords

I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; I KAPPA B KINASE GAMMA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN TRE17; PROTEINASE; SERINE; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG;

ANEURYSMAL BONE CYST; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CELL NUCLEUS; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; ONCOGENE; ONCOGENE TRE 17; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; HELA CELLS; HUMANS; I-KAPPA B KINASE; MICE; MICE, NUDE; NF-KAPPA B; NIH 3T3 CELLS; PEPTIDE FRAGMENTS; PROTO-ONCOGENE PROTEINS; SERINE; TRANSCRIPTION FACTORS; UBIQUITIN THIOLESTERASE;

EID: 84864374400     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.520     Document Type: Article

References (48)

1. Brockman JA, Scherer DC, McKinsey TA, Hall SM, Qi X, Lee WY et al. (1995). Coupling of a signal response domain in I kappa B alpha to multiple pathways for NF-kappa B activation. Mol Cell Biol 15: 2809-2818.
2. Brummelkamp TR, Nijman SM, Dirac AM, Bernards R. (2003). Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-kappaB. comment. Nature 424: 797-801. (Pubitemid 37021711)
3. Buss H, Dorrie A, Schmitz ML, Hoffmann E, Resch K, Kracht M. (2004). Constitutive and interleuKin-1-inducible phosphorylation of p65 NF-{kappa}B at serine 536 is mediated by multiple protein Kinases including I{kappa}B Kinase (IKK)-{alpha}, IKK{beta}, IKK{epsilon}, TRAF family member-associated (TANK)-binding Kinase 1 (TBK1), and an unknown Kinase and couples p65 to TATA-binding protein-associated factor II31-mediated interleuKin-8 transcription. J Biol Chem 279: 55633-55643. (Pubitemid 40068850)
4. Calzado MA, Bacher S, Schmitz ML. (2007). NF-kappaB inhibitors for the treatment of inflammatory diseases and cancer. Curr Med Chem 14: 367-376.
5. Choudhary S, Lu M, Cui R, Brasier AR. (2007). Involvement of a novel Rac/RhoA guanosine triphosphatase-nuclear factor-kappaB inducing Kinase signaling pathway mediating angiotensin II-induced RelA transactivation. Mol Endocrinol 21: 2203-2217. (Pubitemid 47347382)
6. Cottalorda J, Bourelle S. (2007). Modern concepts of primary aneurysmal bone cyst. Arch Orthop Trauma Surg 127: 105-114. (Pubitemid 46165351)
7. Dobrovolskaia MA, Kozlov SV. (2005). Inflammation and cancer: when NF-kappaB amalgamates the perilous partnership. Curr Cancer Drug Targets 5: 325-344. (Pubitemid 41097757)
8. Douillette A, Bibeau-Poirier A, Gravel SP, Clement JF, Chenard V, Moreau P et al. (2006). The proinflammatory actions of angiotensin II are dependent on p65 phosphorylation by the IkappaB Kinase complex. J Biol Chem 281: 13275-13284. (Pubitemid 43855239)
9. Gilmore TD. (2006). Introduction to NF-kappaB: players, pathways, perspectives. Oncogene 25: 6680-6684. (Pubitemid 44657845)
10. Hacker H, Karin M. (2006). Regulation and function of IKK and IKK-related Kinases. Sci STKE 2006: re13.
11. Hansberger MW, Campbell JA, Danthi P, Arrate P, Pennington KN, Marcu KB et al. (2007). IkappaB Kinase subunits alpha and gamma are required for activation of NF-kappaB and induction of apoptosis by mammalian reovirus. J Virol 81: 1360-1371. (Pubitemid 46167857)
12. Harhaj EW, Dixit VM. (2011). Deubiquitinases in the regulation of NF-kappaB signaling. Cell Res 21: 22-39.
13. Hoberg JE, Popko AE, Ramsey CS, Mayo MW. (2006). IkappaB Kinase alpha-mediated derepression of SMRT potentiates acetylation of RelA/p65 by p300. Mol Cell Biol 26: 457-471. (Pubitemid 43090920)
14. Hu J, Nakano H, Sakurai H, Colburn NH. (2004). Insufficient p65 phosphorylation at S536 specifically contributes to the lack of NFkappaB activation and transformation in resistant JB6 cells. Carcinogenesis 25: 1991-2003. (Pubitemid 39405920)
15. Karin M. (2006). Nuclear factor-kappaB in cancer development and progression. Nature 441: 431-436. (Pubitemid 44050137)
16. Khandaker NA, Fazal F, Malik AB, Rahman A. (2004). RhoA/Rhoassociated Kinase pathway selectively regulates thrombin-induced intercellular adhesion molecule-1. Expression in endothelial cells via activation of IkB Kinase b and phosphorylation of RelA/p65. J Immunol 173: 6965-6972. (Pubitemid 39541085)
17. Kovalenko A, Chable-Bessia C, Cantarella G, Israel A, Wallach D, Courtois G. (2003). The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. comment. Nature 424: 801-805. (Pubitemid 37021712)
18. Lau AW, Pringle LM, Quick L, Riquelme DN, Ye Y, Oliveira AM et al. (2010). TRE17/Ubiquitin-specific protease 6 (USP6) oncogene translocated in aneurysmal bone cyst blocks osteoblastic maturation via an autocrine mechanism involving bone morphogenetic protein dysregulation. J Biol Chem 285: 37111-37120.
19. Lee DF, Hung MC. (2008). Advances in targeting IKK and IKKrelated Kinases for cancer therapy. Clin Cancer Res 14: 5656-5662.
20. Liu S, Chen ZJ. (2008). Expanding role of ubiquitination in NF-kappaB signaling. Cell Res 21: 6-21.
21. ManKin HJ, Hornicek FJ, Ortiz-Cruz E, Villafuerte J, Gebhardt MC. (2005). Aneurysmal bone cyst: a review of 150 patients. J Clin Oncol 23: 6756-6762. (Pubitemid 46190271)
22. Martinu L, Masuda-Robens JM, Robertson SE, Santy LC, Casanova JE, Chou MM. (2004). The TBC (TRE-2/Bub2/CDc16) domain protein TRE17 regulates plasma membrane-endosomal trafficKing through activation of Arf6. Mol Cell Biol 24: 9752-9762. (Pubitemid 39458804)
23. Masuda-Robens JM, Kutney SN, Qi H, Chou MM. (2003). The TRE17 oncogene encodes a component of a novel effector pathway for Rho GTPases CDc42 and Rac 1 and stimulates actin remodeling. Mol Cell Biol 23: 2151-2161. (Pubitemid 36278823)
24. Mattioli I, Sebald A, Bucher C, Charles RP, Nakano H, Doi T et al. (2004). Transient and selective NF-kappa B p65 serine 536 phosphorylation induced by T cell costimulation is mediated by I kappa B Kinase beta and controls the Kinetics of p65 nuclear import. J Immunol 172: 6336-6344. (Pubitemid 38621242)
25. Mendenhall WM, ZlotecKi RA, Gibbs CP, Reith JD, Scarborough MT, Mendenhall NP. (2006). Aneurysmal bone cyst. Am J Clin Oncol 29: 311-315. (Pubitemid 44270941)
26. Nakamura T, Hillova J, Mariage-Samson R, Onno M, Huebner K, Cannizzaro LA et al. (1992). A novel transcriptional unit of the TRE oncogene widely expressed in human cancer cells. Oncogene 7: 733-741.
27. Oliveira AM, Hsi BL, Weremowicz S, Rosenberg AE, Dal Cin P, Joseph N et al. (2004a). USP6 (TRE2) fusion oncogenes in aneurysmal bone cyst. Cancer Res 64: 1920-1923. (Pubitemid 38339434)
28. Oliveira AM, Perez-Atayde AR, Dal Cin P, Gebhardt MC, Chen CJ, Neff JR et al. (2005). Aneurysmal bone cyst variant translocations upregulate USP6 transcription by promoter swapping with the ZNF9, COL1A1, TRAP150, and OMD genes. Oncogene 24: 3419-3426. (Pubitemid 40756243)
29. Oliveira AM, Perez-Atayde AR, Inwards CY, Medeiros F, Derr V, Hsi BL et al. (2004b). USP6 and CDH11 oncogenes identify the neoplastic cell in primary aneurysmal bone cysts and are absent in so-called secondary aneurysmal bone cysts. Am J Pathol 165: 1773-1780. (Pubitemid 39435174)
30. OrlowsKi RZ, Baldwin Jr AS. (2002). NF-kappaB as a therapeutic target in cancer. TREnds Mol Med 8: 385-389.
31. Pahl HL. (1999). Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18: 6853-6866.
32. Rollins BJ. (2006). INFlammatory chemoKines in cancer growth and progression. Eur J Cancer 42: 760-767.
33. Saccomanni B. (2008). Aneurysmal bone cyst of spine: a review of literature. Arch Orthop Trauma Surg 128: 1145-1147.
34. Sakurai H, Chiba H, Miyoshi H, Sugita T, Toriumi W. (1999). IkappaB Kinases phosphorylate NF-kappaB p65 subunit on serine 536 in the transactivation domain. J Biol Chem 274: 30353-30356.
35. Sakurai H, SuzuKi S, KawasaKi N, Nakano H, OkazaKi T, Chino A et al. (2003). Tumor necrosis factor-alpha-induced IKK phosphorylation of NF-kappaB p65 on serine 536 is mediated through the TRAF2, TRAF5, and TAK1 signaling pathway. J Biol Chem 278: 36916-36923. (Pubitemid 37140026)
36. SasaKi CY, Barberi TJ, Ghosh P, Longo DL. (2005). Phosphorylation of RelA/p65 on serine 536 defines an I{kappa}B{alpha}-independent NF-{kappa}B pathway. J Biol Chem 280: 34538-34547. (Pubitemid 41504584)
37. Shen C, Ye Y, Robertson SE, Lau AW, Mak DO, Chou MM. (2005). Calcium/calmodulin regulates ubiquitination of the ubiquitinspecific protease TRE17/USP6. J Biol Chem 280: 35967-35973. (Pubitemid 41633865)
38. Shimada H, Rajagopalan LE. (2010). Rho Kinase-2 activation in human endothelial cells drives lysophosphatidic acid-mediated expression of cell adhesion molecules via NF-kappaB p65. J Biol Chem 285: 12536-12542.
39. Sitcheran R, Comb WC, Cogswell PC, Baldwin AS. (2008). Essential role for epidermal growth factor receptor in glutamate receptor signaling to NF-kappaB. Mol Cell Biol 28: 5061-5070.
40. Sizemore N, Lerner N, DombrowsKi N, Sakurai H, Stark GR. (2002). Distinct roles of the Ikappa B Kinase alpha and beta subunits in liberating nuclear factor kappa B (NF-kappa B) from Ikappa B and in phosphorylating the p65 subunit of NF-kappa B. J Biol Chem 277: 3863-3869. (Pubitemid 34968637)
41. Skaug B, Jiang X, Chen ZJ. (2009). The role of ubiquitin in NF-kappaB regulatory pathways. Annu Rev Biochem 78: 769-796.
42. Solt LA, Madge LA, Orange JS, May MJ. (2007). InterleuKin-1-induced NF-kappaB activation is NEMO-dependent but does not require IKKbeta. J Biol Chem 282: 8724-8733. (Pubitemid 47093521)
43. Sun W, Li H, Yu Y, Fan Y, Grabiner BC, Mao R et al. (2009). MEKK3 is required for lysophosphatidic acid-induced NF-kappaB activation. Cell Signal 21: 1488-1494.
44. TrompouKi E, Hatzivassiliou E, Tsichritzis T, Farmer H, Ashworth A, Mosialos G. (2003). CYLD is a deubiquitinating enzyme that negatively regulates NF-kappaB activation by TNFR family members. comment. Nature 424: 793-796. (Pubitemid 37021710)
45. Viatour P, Merville MP, Bours V, Chariot A. (2005). Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and iNFlammation. TREnds Biochem Sci 30: 43-52. (Pubitemid 40093740)
46. Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S et al. (2004). De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 430: 694-699. (Pubitemid 39061687)
47. Yang F, Tang E, Guan K, Wang CY. (2003). IKK beta plays an essential role in the phosphorylation of RelA/p65 on serine 536 induced by lipopolysaccharide. J Immunol 170: 5630-5635. (Pubitemid 36617854)
48. Ye Y, Pringle LM, Lau AW, Riquelme DN, Wang H, Jiang T et al. (2010). TRE17/USP6 oncogene translocated in aneurysmal bone cyst induces matrix metalloproteinase production via activation of NF-kappaB. Oncogene 29: 3619-3629.