A novel role for the proteasomal chaperone PSMD9 and hnRNPA1 in enhancing IκBα degradation and NF-κB activation - Functional relevance of predicted PDZ domain-motif interaction

FEBS Journal

Volumn 281, Issue 11, 2014, Pages 2688-2709

  Sahu, Indrajit ^a   Sangith, Nikhil ^a   Ramteke, Manoj ^a   Gadre, Rucha ^a   Venkatraman, Prasanna ^a  

^a TATA MEMORIAL HOSPITAL   (India)

Author keywords

hnRNPA1; I B degradation; NF B activity; PDZ domain; PSMD9

Indexed keywords

CHAPERONE; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEASOME; PROTEIN HNRNPA1; PROTEIN PSMD9; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; GENE DELETION; GENE OVEREXPRESSION; HEK293 CELL LINE; HUMAN; HUMAN CELL; PDZ DOMAIN; POINT MUTATION; PREDICTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UBIQUITINATION; UPREGULATION;

HNRNPA1; IΚBΑ DEGRADATION; NF-ΚB ACTIVITY; PDZ DOMAIN; PSMD9;

CELL LINE; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; HUMANS; I-KAPPA B PROTEINS; NF-KAPPA B; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING;

EID: 84901823461     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12814     Document Type: Article

References (56)

1. Kaneko T, Hamazaki J, Iemura S, Sasaki K, Furuyama K, Natsume T, Tanaka K, &, Murata S, (2009) Assembly pathway of the mammalian proteasome base subcomplex is mediated by multiple specific chaperones. Cell 137, 914-925.
2. da Fonseca PC, He J, &, Morris EP, (2012) Molecular model of the human 26S proteasome. Mol Cell 46, 54-66.
3. Thomas MK, Yao KM, Tenser MS, Wong GG, &, Habener JF, (1999) Bridge-1, a novel PDZ-domain coactivator of E2A-mediated regulation of insulin gene transcription. Mol Cell Biol 19, 8492-8504.
4. Jelen F, Oleksy A, Smietana K, &, Otlewski J, (2003) PDZ domains-common players in the cell signaling. Acta Biochim Pol 50, 985-1017.
5. Lee HJ, &, Zheng JJ, (2010) PDZ domains and their binding partners: structure, specificity, and modification. Cell Commun Signal 8, 8.
6. Lee JH, Volinic JL, Banz C, Yao KM, &, Thomas MK, (2005) Interactions with p300 enhance transcriptional activation by the PDZ-domain coactivator Bridge-1. J Endocrinol 187, 283-292.
7. Banz C, Munchow B, &, Diedrich K, (2010) Bridge-1 is expressed in human granulosa cells and is involved in the activin A signaling cascade. Fertil Steril 93, 1349-1352.
8. Volinic JL, Lee JH, Eto K, Kaur V, &, Thomas MK, (2006) Overexpression of the coactivator bridge-1 results in insulin deficiency and diabetes. Mol Endocrinol 20, 167-182.
9. Ren S, Uversky VN, Chen Z, Dunker AK, &, Obradovic Z, (2008) Short linear motifs recognized by SH2, SH3 and Ser/Thr kinase domains are conserved in disordered protein regions. BMC Genomics 9 (Suppl 2), S26.
10. Singh Gautam AK, Balakrishnan S, &, Venkatraman P, (2012) Direct ubiquitin independent recognition and degradation of a folded protein by the eukaryotic proteasomes-origin of intrinsic degradation signals. PLoS One 7, e34864.
11. Nanaware PP, Ramteke MP, Somavarapu AK, &, Venkatraman P, (2013) Discovery of multiple interacting partners of gankyrin, a proteasomal chaperone and an oncoprotein-evidence for a common hot spot site at the interface and its functional relevance. Proteins. doi: 10.1002/prot.24494.
12. Hay DC, Kemp GD, Dargemont C, &, Hay RT, (2001) Interaction between hnRNPA1 and IkappaBalpha is required for maximal activation of NF-kappaB-dependent transcription. Mol Cell Biol 21, 3482-3490.
13. Hayden MS, &, Ghosh S, (2008) Shared principles in NF-kappaB signaling. Cell 132, 344-362.
14. Li H, &, Lin X, (2008) Positive and negative signaling components involved in TNFalpha-induced NF-kappaB activation. Cytokine 41, 1-8.
15. Grilli M, Chiu JJ, &, Lenardo MJ, (1993) NF-kappa B and Rel: participants in a multiform transcriptional regulatory system. Int Rev Cytol 143, 1-62.
16. Ghosh S, May MJ, &, Kopp EB, (1998) NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 16, 225-260.
17. Baeuerle PA, &, Baltimore D, (1988) I kappa B: a specific inhibitor of the NF-kappa B transcription factor. Science 242, 540-546.
18. Beg AA, &, Baldwin AS Jr, (1993) The I kappa B proteins: multifunctional regulators of Rel/NF-kappa B transcription factors. Genes Dev 7, 2064-2070.
19. Chen Z, Hagler J, Palombella VJ, Melandri F, Scherer D, Ballard D, &, Maniatis T, (1995) Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev 9, 1586-1597.
20. Li N, &, Karin M, (1998) Ionizing radiation and short wavelength UV activate NF-kappaB through two distinct mechanisms. Proc Natl Acad Sci USA 95, 13012-13017.
21. Mukhopadhyay A, Manna SK, &, Aggarwal BB, (2000) Pervanadate-induced nuclear factor-kappaB activation requires tyrosine phosphorylation and degradation of IkappaBalpha. Comparison with tumor necrosis factor-alpha. J Biol Chem 275, 8549-8555.
22. Hayden MS, &, Ghosh S, (2004) Signaling to NF-kappaB. Genes Dev 18, 2195-2224.
23. Alkalay I, Yaron A, Hatzubai A, Orian A, Ciechanover A, &, Ben-Neriah Y, (1995) Stimulation-dependent I kappa B alpha phosphorylation marks the NF-kappa B inhibitor for degradation via the ubiquitin-proteasome pathway. Proc Natl Acad Sci USA 92, 10599-10603.
24. Tanaka K, Kawakami T, Tateishi K, Yashiroda H, &, Chiba T, (2001) Control of IkappaBalpha proteolysis by the ubiquitin-proteasome pathway. Biochimie 83, 351-356.
25. Miyamoto S, Seufzer BJ, &, Shumway SD, (1998) Novel IkappaB alpha proteolytic pathway in WEHI231 immature B cells. Mol Cell Biol 18, 19-29.
26. Shumway SD, Berchtold CM, Gould MN, &, Miyamoto S, (2002) Evidence for unique calmodulin-dependent nuclear factor-kappaB regulation in WEHI-231 B cells. Mol Pharmacol 61, 177-185.
27. Shumway SD, &, Miyamoto S, (2004) A mechanistic insight into a proteasome-independent constitutive inhibitor kappaBalpha (IkappaBalpha) degradation and nuclear factor kappaB (NF-kappaB) activation pathway in WEHI-231 B-cells. Biochem J 380, 173-180.
28. Ponnappan S, Cullen SJ, &, Ponnappan U, (2005) Constitutive degradation of IkappaBalpha in human T lymphocytes is mediated by calpain. Immun Ageing 2, 15.
29. Palombella VJ, Rando OJ, Goldberg AL, &, Maniatis T, (1994) The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell 78, 773-785.
30. Hoffmann A, Levchenko A, Scott ML, &, Baltimore D, (2002) The IkappaB-NF-kappaB signaling module: temporal control and selective gene activation. Science 298, 1241-1245.
31. Cohen S, Achbert-Weiner H, &, Ciechanover A, (2004) Dual effects of IkappaB kinase beta-mediated phosphorylation on p105 Fate: SCF(beta-TrCP)- dependent degradation and SCF(beta-TrCP)-independent processing. Mol Cell Biol 24, 475-486.
32. Liang C, Zhang M, &, Sun SC, (2006) beta-TrCP binding and processing of NF-kappaB2/p100 involve its phosphorylation at serines 866 and 870. Cell Signal 18, 1309-1317.
33. Moorthy AK, Savinova OV, Ho JQ, Wang VY, Vu D, &, Ghosh G, (2006) The 20S proteasome processes NF-kappaB1 p105 into p50 in a translation-independent manner. EMBO J 25, 1945-1956.
34. Dreyfuss G, Matunis MJ, Pinol-Roma S, &, Burd CG, (1993) hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem 62, 289-321.
35. Reigstad CS, Lunden GO, Felin J, &, Backhed F, (2009) Regulation of serum amyloid A3 (SAA3) in mouse colonic epithelium and adipose tissue by the intestinal microbiota. PLoS One 4, e5842.
36. Zhou A, Scoggin S, Gaynor RB, &, Williams NS, (2003) Identification of NF-kappa B-regulated genes induced by TNFalpha utilizing expression profiling and RNA interference. Oncogene 22, 2054-2064.
37. Miyamoto S, Maki M, Schmitt MJ, Hatanaka M, &, Verma IM, (1994) Tumor necrosis factor alpha-induced phosphorylation of I kappa B alpha is a signal for its degradation but not dissociation from NF-kappa B. Proc Natl Acad Sci USA 91, 12740-12744.
38. Shim SM, Lee WJ, Kim Y, Chang JW, Song S, &, Jung YK, (2012) Role of S5b/PSMD5 in proteasome inhibition caused by TNF-alpha/NFkappaB in higher eukaryotes. Cell Rep 2, 603-615.
39. DeMartino GN, Proske RJ, Moomaw CR, Strong AA, Song X, Hisamatsu H, Tanaka K, &, Slaughter CA, (1996) Identification, purification, and characterization of a PA700-dependent activator of the proteasome. J Biol Chem 271, 3112-3118.
40. Ferrell K, Wilkinson CR, Dubiel W, &, Gordon C, (2000) Regulatory subunit interactions of the 26S proteasome, a complex problem. Trends Biochem Sci 25, 83-88.
41. Chen C, Huang C, Chen S, Liang J, Lin W, Ke G, Zhang H, Wang B, Huang J, Han Z, et al,. (2008) Subunit-subunit interactions in the human 26S proteasome. Proteomics 8, 508-520.
42. Bohn S, Beck F, Sakata E, Walzthoeni T, Beck M, Aebersold R, Forster F, Baumeister W, &, Nickell S, (2010) Structure of the 26S proteasome from Schizosaccharomyces pombe at subnanometer resolution. Proc Natl Acad Sci USA 107, 20992-20997.
43. Lander GC, Estrin E, Matyskiela ME, Bashore C, Nogales E, &, Martin A, (2012) Complete subunit architecture of the proteasome regulatory particle. Nature 482, 186-191.
44. Lasker K, Forster F, Bohn S, Walzthoeni T, Villa E, Unverdorben P, Beck F, Aebersold R, Sali A, &, Baumeister W, (2012) Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc Natl Acad Sci USA 109, 1380-1387.
45. Deveraux Q, Ustrell V, Pickart C, &, Rechsteiner M, (1994) A 26S protease subunit that binds ubiquitin conjugates. J Biol Chem 269, 7059-7061.
46. Husnjak K, Elsasser S, Zhang N, Chen X, Randles L, Shi Y, Hofmann K, Walters KJ, Finley D, &, Dikic I, (2008) Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453, 481-488.
47. Su V, &, Lau AF, (2009) Ubiquitin-like and ubiquitin-associated domain proteins: significance in proteasomal degradation. Cell Mol Life Sci 66, 2819-2833.
48. Chen L, &, Madura K, (2002) Rad23 promotes the targeting of proteolytic substrates to the proteasome. Mol Cell Biol 22, 4902-4913.
49. Gomez TA, Kolawa N, Gee M, Sweredoski MJ, &, Deshaies RJ, (2011) Identification of a functional docking site in the Rpn1 LRR domain for the UBA-UBL domain protein Ddi1. BMC Biol 9, 33.
50. Babu JR, Geetha T, &, Wooten MW, (2005) Sequestosome 1/p62 shuttles polyubiquitinated tau for proteasomal degradation. J Neurochem 94, 192-203.
51. Parcellier A, Schmitt E, Gurbuxani S, Seigneurin-Berny D, Pance A, Chantome A, Plenchette S, Khochbin S, Solary E, &, Garrido C, (2003) HSP27 is a ubiquitin-binding protein involved in I-kappaBalpha proteasomal degradation. Mol Cell Biol 23, 5790-5802.
52. Watanabe TK, Saito A, Suzuki M, Fujiwara T, Takahashi E, Slaughter CA, DeMartino GN, Hendil KB, Chung CH, Tanahashi N, et al,. (1998) cDNA cloning and characterization of a human proteasomal modulator subunit, p27 (PSMD9). Genomics 50, 241-250.
53. Dolcet X, Llobet D, Pallares J, &, Matias-Guiu X, (2005) NF-kB in development and progression of human cancer. Virchows Arch 446, 475-482.
54. Ravi R, &, Bedi A, (2004) NF-kappaB in cancer-a friend turned foe. Drug Resist Updat 7, 53-67.
55. Lee SY, De la Mota-Peynado A, &, Roelofs J, (2011) Loss of Rpt5 protein interactions with the core particle and Nas2 protein causes the formation of faulty proteasomes that are inhibited by Ecm29 protein. J Biol Chem 286, 36641-36651.
56. Wu Y, Li Q, &, Chen XZ, (2007) Detecting protein-protein interactions by far western blotting. Nature protocol 2, 3278-3284.