Tyrosine phosphorylation allows integration of multiple signaling inputs by IKKβ

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Meyer, April N ^a   Drafahl, Kristine A ^a,d   McAndrew, Christopher W ^a,e   Gilda, Jennifer E ^a,f   Gallo, Leandro H ^a   Haas, Martin ^b   Brill, Laurence M ^c   Donoghue, Daniel J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c BURNHAM INSTITUTE   (United States)

^d MolecularMD   (United States)

^e Wilson Sonsini Goodrich Rosati   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FGFR2 PROTEIN, HUMAN; FIBROBLAST GROWTH FACTOR RECEPTOR 2; I KAPPA B KINASE; IKBKB PROTEIN, HUMAN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TYROSINE;

AMINO ACID SUBSTITUTION; ENZYME ACTIVATION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; MISSENSE MUTATION; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

AMINO ACID SUBSTITUTION; ENZYME ACTIVATION; HEK293 CELLS; HUMANS; I-KAPPA B KINASE; MUTATION, MISSENSE; NF-KAPPA B; PHOSPHORYLATION; PROTEIN STRUCTURE, SECONDARY; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; TYROSINE;

EID: 84893519408     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084497     Document Type: Article

References (58)

1. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S (2002) The protein kinase complement of the human genome. Science 298: 1912-1934. doi:10.1126/science.1075762. PubMed: 12471243. (Pubitemid 35425239)
2. Zhang Y, Gorry MC, Post JC, Ehrlich GD (1999) Genomic organization of the human fibroblast growth factor receptor 2 (FGFR2) gene and comparative analysis of the human FGFR gene family. Gene 230: 69-79. doi:10.1016/S0378-1119(99) 00047-5. PubMed: 10196476. (Pubitemid 29193197)
3. Eswarakumar VP, Lax I, Schlessinger J (2005) Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 16: 139-149. doi:10.1016/j.cytogfr.2005.01.001. PubMed: 15863030. (Pubitemid 40616112)
4. Naimi B, Latil A, Fournier G, Mangin P, Cussenot O et al. (2002) Down-regulation of (IIIb) and (IIIc) isoforms of fibroblast growth factor receptor 2 (FGFR2) is associated with malignant progression in human prostate. Prostate 52: 245-252. doi:10.1002/pros.10104. PubMed: 12111699. (Pubitemid 34791225)
5. Ricol D, Cappellen D, El Marjou A, Gil-Diez-de-Medina S, Girault JM, et al. (1999) Tumour suppressive properties of fibroblast growth factor receptor 2-IIIb in human bladder cancer. Oncogene 18: 7234-7243 (Pubitemid 30032102)
6. Jang JH, Shin KH, Park JG (2001) Mutations in fibroblast growth factor receptor 2 and fibroblast growth factor receptor 3 genes associated with human gastric and colorectal cancers. Cancer Res 61: 3541-3543. PubMed: 11325814.
7. Hunter DJ, Kraft P, Jacobs KB, Cox DG, Yeager M et al. (2007) A genome-wide association study identifies alleles in FGFR2 associated with risk of sporadic postmenopausal breast cancer. Nat Genet 39: 870-874. doi:10.1038/ng2075. PubMed: 17529973. (Pubitemid 47014500)
8. Gartside MG, Chen H, Ibrahimi OA, Byron SA, Curtis AV et al. (2009) Loss-of-function fibroblast growth factor receptor-2 mutations in melanoma. Mol Cancer Res 7: 41-54. doi: 10.1158/1541-7786.MCR-08-0021. PubMed: 19147536.
9. Courtois G, Gilmore TD (2006) Mutations in the NF-kappaB signaling pathway: implications for human disease. Oncogene 25: 6831-6843. doi:10.1038/sj.onc.1209939. PubMed: 17072331. (Pubitemid 44657855)
10. Gilmore TD (2007) Multiple myeloma: lusting for NF-kappaB. Cancer Cell 12: 95-97. doi:10.1016/j.ccr.2007.07.010. PubMed: 17692798.
11. Perkins ND (2012) The diverse and complex roles of NF-kappaB subunits in cancer. Nat Rev Cancer 12: 121-132. PubMed: 22257950.
12. Yamaoka S, Courtois G, Bessia C, Whiteside ST, Weil R et al. (1998) Complementation cloning of NEMO, a component of the IkappaB kinase complex essential for NF-kappaB activation. Cell 93: 1231-1240. doi:10.1016/S0092- 8674(00)81466-X. PubMed: 9657155. (Pubitemid 28307427)
13. Krappmann D, Hatada EN, Tegethoff S, Li J, Klippel A, et al. (2000) The I kappa B kinase (IKK) complex is tripartite and contains IKK gamma but not IKAP as a regular component. J Biol Chem 275: 29779-29787 (Pubitemid 32043862)
14. Rudolph D, Yeh WC, Wakeham A, Rudolph B, Nallainathan D et al. (2000) Severe liver degeneration and lack of NF-kappaB activation in NEMO/IKKgamma-deficient mice. Genes Dev 14: 854-862. PubMed: 10766741. (Pubitemid 30215004)
15. Ghosh S, Hayden MS (2012) Celebrating 25 years of NF-kappaB research. Immunol Rev 246: 5-13. doi:10.1111/j.1600-065X.2012.01111.x. PubMed: 22435544.
16. Hu MC, Lee DF, Xia W, Golfman LS, Ou-Yang F et al. (2004) IkappaB kinase promotes tumorigenesis through inhibition of forkhead FOXO3a. Cell 117: 225-237. doi:10.1016/S0092-8674(04)00302-2. PubMed: 15084260. (Pubitemid 38496242)
17. Annunziata CM, Davis RE, Demchenko Y, Bellamy W, Gabrea A et al. (2007) Frequent engagement of the classical and alternative NF-kappaB pathways by diverse genetic abnormalities in multiple myeloma. Cancer Cell 12: 115-130. doi:10.1016/j.ccr.2007.07.004. PubMed: 17692804. (Pubitemid 47199123)
18. Li ZW, Chen H, Campbell RA, Bonavida B, Berenson JR (2008) NF-kappaB in the pathogenesis and treatment of multiple myeloma. Curr Opin Hematol 15: 391-399. doi:10.1097/MOH.0b013e328302c7f4. PubMed: 18536579.
19. Cai D, Yuan M, Frantz DF, Melendez PA, Hansen L et al. (2005) Local and systemic insulin resistance resulting from hepatic activation of IKK-beta and NF-kappaB. Nat Med 11: 183-190. doi:10.1038/nm1166. PubMed: 15685173. (Pubitemid 40321354)
20. Andreakos E, Smith C, Kiriakidis S, Monaco C, de Martin R et al. (2003) Heterogeneous requirement of IkappaB kinase 2 for inflammatory cytokine and matrix metalloproteinase production in rheumatoid arthritis: implications for therapy. Arthritis Rheum 48: 1901-1912. doi:10.1002/art.11044. PubMed: 12847684. (Pubitemid 36828685)
21. Aupperle K, Bennett B, Han Z, Boyle D, Manning A et al. (2001) NF-kappa B regulation by I kappa B kinase-2 in rheumatoid arthritis synoviocytes. J Immunol 166: 2705-2711. PubMed: 11160335. (Pubitemid 32173511)
22. Mercurio F, Zhu H, Murray BW, Shevchenko A, Bennett BL et al. (1997) IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science 278: 860-866. doi:10.1126/science.278.5339.860. PubMed: 9346484. (Pubitemid 27467923)
23. Woronicz JD, Gao X, Cao Z, Rothe M, Goeddel DV (1997) IkappaB kinase-beta: NF-kappaB activation and complex formation with IkappaB kinase-alpha and NIK. Science 278: 866-869. doi:10.1126/science.278.5339.866. PubMed: 9346485. (Pubitemid 27467924)
24. Delhase M, Hayakawa M, Chen Y, Karin M (1999) Positive and negative regulation of IkappaB kinase activity through IKKbeta subunit phosphorylation. Science 284: 309-313. doi:10.1126/science.284.5412.309. PubMed: 10195894. (Pubitemid 129523447)
25. Ninomiya-Tsuji J, Kishimoto K, Hiyama A, Inoue J, Cao Z et al. (1999) The kinase TAK1 can activate the NIK-I kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 398: 252-256. doi:10.1038/18465. PubMed: 10094049.
26. Chen Z, Hagler J, Palombella VJ, Melandri F, Scherer D et al. (1995) Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev 9: 1586-1597. doi: 10.1101/gad.9.13. 1586. PubMed: 7628694.
27. Li X, Massa PE, Hanidu A, Peet GW, Aro P et al. (2002) IKKalpha, IKKbeta, and NEMO/IKKgamma are each required for the NF-kappa B-mediated inflammatory response program. J Biol Chem 277: 45129-45140. doi:10.1074/jbc.M205165200. PubMed: 12221085. (Pubitemid 36159115)
28. Pahl HL (1999) Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18: 6853-6866. doi:10.1038/sj.onc.1203239. PubMed: 10602461.
29. Tobe BT, Hou J, Crain AM, Singec I, Snyder EY et al. (2012) Phosphoproteomic analysis: an emerging role in deciphering cellular signaling in human embryonic stem cells and their differentiated derivatives. Stem. Cell Research 8: 16-31.
30. Ma L, Tao Y, Duran A, Llado V, Galvez A et al. (2013) Control of nutrient stress-induced metabolic reprogramming by PKCzeta in tumorigenesis. Cell 152: 599-611. doi:10.1016/j.cell.2012.12.028. PubMed: 23374352.
31. Drafahl KA, McAndrew CW, Meyer AN, Haas M, Donoghue DJ (2010) The receptor tyrosine kinase FGFR4 negatively regulates NFkappaB signaling. PLOS ONE 5: e14412. doi:10.1371/journal.pone.0014412. PubMed: 21203561.
32. Zandi E, Rothwarf DM, Delhase M, Hayakawa M, Karin M (1997) The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation. Cell 91: 243-252. doi:10.1016/S0092-8674(00)80406-7. PubMed: 9346241. (Pubitemid 27456391)
33. Polley S, Huang DB, Hauenstein AV, Fusco AJ, Zhong X, et al. (2013) A Structural Basis for IkappaB Kinase 2 Activation Via Oligomerization-Dependent Trans Auto-Phosphorylation. PLoS Biol 11: e1001581
34. Pati UK (1992) Novel vectors for expression of cDNA encoding epitope-tagged proteins in mammalian cells. Gene 114: 285-288. doi: 10.1016/0378-1119(92)90589-H. PubMed: 1376293.
35. Xu G, Lo YC, Li Q, Napolitano G, Wu X et al. (2011) Crystal structure of inhibitor of kappaB kinase beta. Nature 472: 325-330. doi:10.1038/nature09853. PubMed: 21423167.
36. Liu H, Sadygov RG, Yates JR 3rd (2004) A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 76: 4193-4201. doi:10.1021/ac0498563. PubMed: 15253663. (Pubitemid 38943698)
37. Huttlin EL, Jedrychowski MP, Elias JE, Goswami T, Rad R et al. (2010) A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143: 1174-1189. doi:10.1016/j.cell.2010.12.001. PubMed: 21183079.
38. Zhang Y, Otero JE, Abu-Amer Y (2013) Ubiquitin-Like Domain of IKKbeta Regulates Osteoclastogenesis and Osteolysis. Calcif Tissue Int 93: 78-85. doi:10.1007/s00223-013-9735-5. PubMed: 23686246.
39. Liu S, Misquitta YR, Olland A, Johnson MA, Kelleher KS et al. (2013) Crystal Structure of A Human IkappaB Kinase beta Asymmetric Dimer. J Biol Chem.
40. DiDonato JA, Hayakawa M, Rothwarf DM, Zandi E, Karin M (1997) A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB. Nature 388: 548-554. doi:10.1038/41493. PubMed: 9252186. (Pubitemid 27339997)
41. Hideshima T, Ikeda H, Chauhan D, Okawa Y, Raje N et al. (2009) Bortezomib induces canonical nuclear factor-kappaB activation in multiple myeloma cells. Blood 114: 1046-1052. doi:10.1182/blood-2009-01-199604. PubMed: 19436050.
42. Barisic S, Schmidt C, Walczak H, Kulms D (2010) Tyrosine phosphatase inhibition triggers sustained canonical serine-dependent NFkappaB activation via Src-dependent blockade of PP2A. Biochem Pharmacol 80: 439-447. doi:10.1016/j.bcp.2010.04.028. PubMed: 20450893.
43. Schomer-Miller B, Higashimoto T, Lee YK, Zandi E (2006) Regulation of IkappaB kinase (IKK) complex by IKKgamma-dependent phosphorylation of the T-loop and C terminus of IKKbeta. J Biol Chem 281: 15268-15276. doi:10.1074/jbc. M513793200. PubMed: 16597623. (Pubitemid 43855116)
44. Bártová I, Otyepka M, Kríz Z, Koca J (2005) The mechanism of inhibition of the cyclin-dependent kinase-2 as revealed by the molecular dynamics study on the complex CDK2 with the peptide substrate HHASPRK. Protein Sci 14: 445-451. doi:10.1110/ps.04959705. PubMed: 15632290.
45. Locascio LE, Donoghue DJ (2013) KIDs rule: regulatory phosphorylation of RTKs. Trends Biochem Sci 38: 75-84. doi:10.1016/j.tibs.2012.12.001. PubMed: 23312584.
46. Henson ES, Gibson EM, Villanueva J, Bristow NA, Haney N et al. (2003) Increased expression of Mcl-1 is responsible for the blockage of TRAIL-induced apoptosis mediated by EGF/ErbB1 signaling pathway. J Cell Biochem 89: 1177-1192. doi:10.1002/jcb.10597. PubMed: 12898516. (Pubitemid 36959385)
47. Ahmed KM, Cao N, Li JJ (2006) HER-2 and NF-kappaB as the targets for therapy-resistant breast cancer. Anticancer Res 26: 4235-4243. PubMed: 17201139. (Pubitemid 46039582)
48. Sethi G, Ahn KS, Chaturvedi MM, Aggarwal BB (2007) Epidermal growth factor (EGF) activates nuclear factor-kappaB through IkappaBalpha kinase-independent but EGF receptor-kinase dependent tyrosine 42 phosphorylation of IkappaBalpha. Oncogene 26: 7324-7332. doi:10.1038/sj.onc.1210544. PubMed: 17533369. (Pubitemid 350115978)
49. Kao DD, Oldebeken SR, Rai A, Lubos E, Leopold JA et al. (2013) Tumor necrosis factor-alpha-mediated suppression of dual-specificity phosphatase 4: crosstalk between NFkappaB and MAPK regulates endothelial cell survival. Mol Cell Biochem.
50. Yamaguchi H, Chang SS, Hsu JL, Hung MC (2013) Signaling cross-talk in the resistance to HER family receptor targeted therapy. Oncogene.
51. Wei W, Liu W, Cassol C, Zheng W, Asa SL et al. (2012) The Breast Cancer Susceptibility Gene FGFR2 Serves as a Scaffold for Regulation of NF-kappabeta Signaling. Mol Cell Biol.
52. Lee DF, Hung MC (2008) Advances in targeting IKK and IKK-related kinases for cancer therapy. Clin Cancer Res 14: 5656-5662. doi: 10.1158/1078-0432.CCR- 08-0123. PubMed: 18794072.
53. Lin Y, Bai L, Chen W, Xu S (2010) The NF-kappaB activation pathways, emerging molecular targets for cancer prevention and therapy. Expert Opin Ther Targets 14: 45-55. doi: 10.1517/14728220903431069. PubMed: 20001209.
54. Nogueira L, Ruiz-Ontañon P, Vazquez-Barquero A, Moris F, Fernandez-Luna JL (2011) The NFkappaB pathway: a therapeutic target in glioblastoma. Oncotarget 2: 646-653. PubMed: 21896960.
55. Liu F, Xia Y, Parker AS, Verma IM (2012) IKK biology. Immunol Rev 246: 239-253. doi:10.1111/j.1600-065X.2012.01107.x. PubMed: 22435559.
56. Hart KC, Robertson SC, Donoghue DJ (2001) Identification of tyrosine residues in constitutively activated fibroblast growth factor receptor 3 involved in mitogenesis, Stat activation, and phosphatidylinositol 3- kinase activation. Mol Biol Cell 12: 931-942. doi:10.1091/mbc.12.4.931. PubMed: 11294897. (Pubitemid 33051989)
57. Robertson SC, Meyer AN, Hart KC, Galvin BD, Webster MK et al. (1998) Activating mutations in the extracellular domain of the fibroblast growth factor receptor 2 function by disruption of the disulfide bond in the third immunoglobulin-like domain. Proc Natl Acad Sci U S A 95: 4567-4572. doi:10.1073/pnas.95.8.4567. PubMed: 9539778. (Pubitemid 28207953)
58. Meyer AN, McAndrew CW, Donoghue DJ (2008) Nordihydroguaiaretic acid inhibits an activated fibroblast growth factor receptor 3 mutant and blocks downstream signaling in multiple myeloma cells. Cancer Res 68: 7362-7370. doi:10.1158/0008-5472.CAN-08-0575. PubMed: 18794123.