The transitional endoplasmic reticulum ATPase p97 regulates the alternative nuclear factor NF-κB signaling via partial degradation of the NF-κB subunit p100

Journal of Biological Chemistry

Volumn 290, Issue 32, 2015, Pages 19558-19568

  Zhang, Zhao ^a   Wang, Yanyan ^a   Li, Chuanchuan ^a   Shi, Zhubing ^a,b   Hao, Qian ^a   Wang, Wenjia ^a   Song, Xiaomin ^a   Zhao, Yun ^a   Jiao, Shi ^a,c   Zhou, Zhaocai ^a,c  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b TONGJI UNIVERSITY   (China)

^c SHANGHAITECH UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; DISEASES; GENES; MAMMALS; ONCOLOGY; TRANSCRIPTION;

ATP-ASE ACTIVITY; DOWNSTREAM TARGET; ENDOPLASMIC RETICULUM; FRONTOTEMPORAL DEMENTIAS; INCLUSION BODIES; NUCLEAR FACTORS; PARTIAL DEGRADATION; SPECIFIC INHIBITORS;

GENE EXPRESSION;

ADAPTOR PROTEIN; ADAPTOR PROTEIN NPL4; ADAPTOR PROTEIN UFD1; ADENOSINE TRIPHOSPHATASE; F BOX PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P100; PROTEIN P52; PROTEIN P97; UNCLASSIFIED DRUG; KARYOPHERIN BETA; KPNB1 PROTEIN, HUMAN; LIPOPOLYSACCHARIDE; N2,N4-DIBENZYLQUINAZOLINE-2,4-DIAMINE; NPLOC4 PROTEIN, HUMAN; NUCLEAR PROTEIN; PROTEASOME; PROTEIN; QUINAZOLINE DERIVATIVE; UBIQUITIN PROTEIN LIGASE; UFD1L PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SUBSTRATE COMPLEX; FRONTOTEMPORAL DEMENTIA; GENE TARGETING; HUMAN; INCLUSION BODY MYOSITIS; LUNG INJURY; LYMPHOMA CELL; MALE; MOLECULARLY TARGETED THERAPY; MOUSE; NONHUMAN; PAGET BONE DISEASE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UBIQUITINATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; CYTOLOGY; DRUG EFFECTS; ENDOPLASMIC RETICULUM; FIBROBLAST; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HEK293 CELL LINE; KNOCKOUT MOUSE; LUNG; LYMPHOCYTE; METABOLISM; PATHOLOGY; PNEUMONIA; TUMOR CELL LINE;

MUS;

ANIMALS; BETA KARYOPHERINS; CELL LINE, TUMOR; ENDOPLASMIC RETICULUM; FIBROBLASTS; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; LIPOPOLYSACCHARIDES; LUNG; LYMPHOCYTES; MALE; MICE; MICE, KNOCKOUT; NF-KAPPA B P52 SUBUNIT; NUCLEAR PROTEINS; PNEUMONIA; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEINS; PROTEOLYSIS; QUINAZOLINES; SIGNAL TRANSDUCTION; SKP CULLIN F-BOX PROTEIN LIGASES; TRANSCRIPTION, GENETIC; UBIQUITINATION;

EID: 84939170347     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.630061     Document Type: Article

References (49)

1. Erzurumlu, Y., Kose, F. A., Gozen, O., Gozuacik, D., Toth, E. A., and Ballar, P. (2013) A unique IBMPFD-related P97/VCP mutation with differential binding pattern and subcellular localization. Int. J. Biochem. Cell Biol. 45, 773-782
2. Meyer, H. (2012) p97 complexes as signal integration hubs. BMC Biol. 10, 48-52
3. Lilley, B. N., and Ploegh, H. L. (2005) Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. U.S.A. 102, 14296-14301
4. Woodman, P. G. (2003) p97, a protein coping with multiple identities. J. Cell Sci. 116, 4283-4290
5. Rabinovich, E., Kerem, A., Fröhlich, K. U., Diamant, N., and Bar-Nun, S. (2002) AAA-ATPase p97/Cdc48p, a Cytosolic Chaperone Required for Endoplasmic Reticulum-Associated Protein Degradation. Mol. Cell. Biol. 22, 626-634
6. Kumar, K. R., Needham, M., Mina, K., Davis, M., Brewer, J., Staples, C., Ng, K., Sue, C. M., and Mastaglia, F. L. (2010) Two Australian families with inclusion-body myopathy, Paget's disease of bone and frontotemporal dementia: novel clinical and genetic findings. Neuromuscul. Disord. 20, 330-334
7. Ju, J. S., and Weihl, C. C. (2010) Inclusion body myopathy, Paget's disease of the bone and fronto-temporal dementia: a disorder of autophagy. Hum. Mol. Genet. 19, R38-45
8. Stojkovic, T., Hammouda el, H., Richard, P., López de Munain, A., Ruiz-Martinez, J., Camaño, P., Gonzalez, P. C., Laforêt, P., Pénisson-Besnier, I., Ferrer, X., Lacour, A., Lacomblez, L., Claeys, K. G., Maurage, C. A., Fardeau, M., and Eymard, B. (2009) Clinical outcome in 19 French and Spanish patients with valosin-containing protein myopathy associated with Paget's disease of bone and frontotemporal dementia. Neuromuscul. Disord. 19, 316-323
9. Watts, G. D., Wymer, J., Kovach, M. J., Mehta, S. G., Mumm, S., Darvish, D., Pestronk, A., Whyte, M. P., and Kimonis, V. E. (2004) Inclusion body myopathy associated with Paget disease of bone and frontotemporal dementia is caused by mutant valosin-containing protein. Nat. Genet. 36, 377-381
10. Mizuno, Y., Hori, S., Kakizuka, A., and Okamoto, K. (2003) Vacuole-creating protein in neurodegenerative diseases in humans. Neurosci. Lett. 343, 77-80
11. Yamamoto, S., Tomita, Y., Hoshida, Y., Iizuka, N., Kidogami, S., Miyata, H., Takiguchi, S., Fujiwara, Y., Yasuda, T., Yano, M., Nakamori, S., Sakon, M., Monden, M., and Aozasa, K. (2004) Expression level of valosin-containing protein (p97) is associated with prognosis of esophageal carcinoma. Clin. Cancer Res. 10, 5558-5565
12. Asaka, S., Fujimoto, T., Akaishi, J., Ogawa, K., and Onda, M. (2006) Genetic prognostic index influences patient outcome for node-positive breast cancer. Surg. Today 36, 793-801
13. Yamamoto, S., Tomita, Y., Hoshida, Y., Iizuka, N., Monden, M., Yamamoto, S., Iuchi, K., and Aozasa, K. (2004) Expression level of valosin-containing protein (p97) is correlated with progression and prognosis of non-small-cell lung carcinoma. Ann. Surg. Oncol. 11, 697-704
14. Zhao, C. H., and Li, Q. F. (2005) Altered profiles of nuclear matrix proteins during the differentiation of human gastric mucous adenocarcinoma MGc80-3 cells. World J. Gastroenterol. 11, 4628-4633
15. Asai, T., Tomita, Y., Nakatsuka, S., Hoshida, Y., Myoui, A., Yoshikawa, H., and Aozasa, K. (2002) VCP (p97) regulates NFκB signaling pathway, which is important for metastasis of osteosarcoma cell line. Jpn J Cancer Res. 93, 296-304
16. Ye, Y. (2006) Diverse functions with a common regulator: Ubiquitin takes command of an AAA ATPase. J. Struct. Biol. 156, 29-40
17. Wójcik, C., Rowicka, M., Kudlicki, A., Nowis, D., McConnell, E., Kujawa, M., and DeMartino, G. N. (2006) Valosin-containing protein (p97) is a regulator of endoplasmic reticulum stress and of the degradation of N-end rule and ubiquitin-fusion degradation pathway substrates in mammalian cells. Mol. Biol. Cell 17, 4606-4618
18. Alexandru, G., Graumann, J., Smith, G. T., Kolawa, N. J., Fang, R., and Deshaies, R. J. (2008) UBXD7 binds multiple ubiquitin ligases and implicates p97 in HIF1α turnover. Cell 134, 804-816
19. Magadán, J. G., Pérez-Victoria, F. J., Sougrat, R., Ye, Y., Strebel, K., and Bonifacino, J. S. (2010) Multilayered mechanism of CD4 downregulation by HIV-1 Vpu involving distinct ER retention and ERAD targeting steps. PLoS Pathog. 6, e1000869
20. Acs, K., Luijsterburg, M. S., Ackermann, L., Salomons, F. A., Hoppe, T., and Dantuma, N. P. (2011) The AAA-ATPase VCP/p97 promotes 53BP1 recruitment by removing L3MBTL1 from DNA double-strand breaks. Nat. Struct. Mol. Biol. 18, 1345-1350
21. Franz, A., Orth, M., Pirson, P. A., Sonneville, R., Blow, J. J., Gartner, A., Stemmann, O., and Hoppe, T. (2011) CDC-48/p97 coordinates CDT-1 degradation with GINS chromatin dissociation to ensure faithful DNA replication. Mol. Cell 44, 85-96
22. Verma, R., Oania, R., Fang, R., Smith, G. T., and Deshaies, R. J. (2011) Cdc48/p97 mediates UV-dependent turnover of RNA Pol II. Mol. Cell 41, 82-92
23. Kahn, M., Sugawara, H., McGowan, P., Okuno, K., Nagoya, S., Hellström, K. E., Hellström, I., and Greenberg, P. (1991) CD4+ T cell clones specific for the human p97 melanoma-associated antigen can eradicate pulmonary metastases from a murine tumor expressing the p97 antigen. J. Immunol. 146, 3235-3241
24. Li, J. M., Wu, H., Zhang, W., Blackburn, M. R., and Jin, J. (2014) The p97-UFD1L-NPL4 protein complex mediates cytokine-induced IκBα proteolysis. Mol. Cell. Biol. 34, 335-347
25. Silverman, N., and Maniatis, T. (2001) NF-κB signaling pathways in mammalian and insect innate immunity. Genes Dev. 15, 2321-2342
26. Fan, C. M., and Maniatis, T. (1991) Generation of p50 subunit of NF-κB by processing of p105 through an ATP-dependent pathway. Nature 354, 395-398
27. Fukushima, H., Matsumoto, A., Inuzuka, H., Zhai, B., Lau, A. W., Wan, L., Gao, D., Shaik, S., Yuan, M., Gygi, S. P., Jimi, E., Asara, J. M., Nakayama, K., Nakayama, K. I., and Wei, W. (2012) SCF(Fbw7) modulates the NFκB signaling pathway by targeting NFkB2 for ubiquitination and destruction. Cell Rep 1, 434-443
28. Dejardin, E., Droin, N. M., Delhase, M., Haas, E., Cao, Y., Makris, C., Li, Z.-W., Karin, M., Ware, C. F., and Green, D. R. (2002) The Lymphotoxin-κReceptor Induces Different Patterns of Gene Expression via Two NF-κB Pathways. Immunity 17, 525-535
29. Claudio, E., Brown, K., Park, S., Wang, H., and Siebenlist, U. (2002) BAFF-induced NEMO-independent processing of NF-κB2 in maturing B cells. Nat. Immunol. 3, 958-965
30. Liang, C., Zhang, M., and Sun, S. C. (2006) κ-TrCP binding and processing of NF-κB2/p100 involve its phosphorylation at serines 866 and 870. Cell. Signal. 18, 1309-1317
31. Giardino Torchia, M. L., Conze, D. B., Jankovic, D., and Ashwell, J. D. (2013) Balance between NF-κB p100 and p52 regulates T cell costimulation dependence. J. Immunol. 190, 549-555
32. Coope, H. J., Atkinson, P. G., Huhse, B., Belich, M., Janzen, J., Holman, M. J., Klaus, G. G., Johnston, L. H., and Ley, S. C. (2002) CD40 regulates the processing of NF-κB2 p100 to p52. EMBO J. 21, 5375-5385
33. Thakur, S., Lin, H. C., Tseng, W. T., Kumar, S., Bravo, R., Foss, F., Gélinas, C., and Rabson, A. B. (1994) Rearrangement and altered expression of the NFKB-2 gene in human cutaneous T-lymphoma cells. Oncogene 9, 2335-2344
34. Fracchiolla, N. S., Lombardi, L., Salina, M., Migliazza, A., Baldini, L., Berti, E., Cro, L., Polli, E., Maiolo, A. T., and Neri, A. (1993) Structural alterations of the NF-κB transcription factor lyt-10 in lymphoid malignancies. Oncogene 8, 2839-2845
35. Cogswell, P. C., Guttridge, D. C., Funkhouser, W. K., and Baldwin, A. S., Jr. (2000) Selective activation of NF-κB subunits in human breast cancer: potential roles for NF-κB2/p52 and for Bcl-3. Oncogene 19, 1123-1131
36. Rayet, B., and Gélinas, C. (1999) Aberrant rel/nfkb genes and activity in human cancer. Oncogene 18, 6938-6947
37. Zhang, Z., Lv, X., Yin, W.-C., Zhang, X., Feng, J., Wu, W., Hui, C.-C., Zhang, L., and Zhao, Y. (2013) Ter94 ATPase complex targets K11-linked ubiquitinated Ci to proteasomes for partial degradation. Dev. Cell 25, 636-644
38. Jiao, S., Zhang, Z., Li, C., Huang, M., Shi, Z., Wang, Y., Song, X., Liu, H., Li, C., Chen, M., Wang, W., Zhao, Y., Jiang, Z., Wang, H., Wong, C. C., Wang, C., and Zhou, Z. (2015) The kinase MST4 limits inflammatory responses through direct phosphorylation of the adaptor TRAF6. Nat. Immunol. 16, 246-257
39. Chen, C., Shi, Z., Zhang, W., Chen, M., He, F., Zhang, Z., Wang, Y., Feng, M., Wang, W., Zhao, Y., Brown, J. H., Jiao, S., and Zhou, Z. (2014) Striatins contain a noncanonical coiled coil that binds protein phosphatase 2A A subunit to form a 2:2 heterotetrameric core of striatin-interacting phosphatase and kinase (STRIPAK) complex. J. Biol. Chem. 289, 9651-9661
40. Piccaluga, P. P., Agostinelli, C., Califano, A., Rossi, M., Basso, K., Zupo, S., Went, P., Klein, U., Zinzani, P. L., Baccarani, M., Dalla Favera, R., and Pileri, S. A. (2007) Gene expression analysis of peripheral T cell lymphoma, unspecified, reveals distinct profiles and new potential therapeutic targets. J. Clin. Invest. 117, 823-834
41. Tang, W. K., and Xia, D. (2013) Altered intersubunit communication is the molecular basis for functional defects of pathogenic p97 mutants. J. Biol. Chem. 288, 36624-36635
42. Pye, V. E., Beuron, F., Keetch, C. A., McKeown, C., Robinson, C. V., Meyer, H. H., Zhang, X., and Freemont, P. S. (2007) Structural insights into the p97-Ufd1-Npl4 complex. Proc. Natl. Acad. Sci. U.S.A. 104, 467-472
43. Maruyama, T., Fukushima, H., Nakao, K., Shin, M., Yasuda, H., Weih, F., Doi, T., Aoki, K., Alles, N., Ohya, K., Hosokawa, R., and Jimi, E. (2010) Processing of the NF-κB2 precursor p100 to p52 is critical for RANKL-induced osteoclast differentiation. J. Bone Miner. Res. 25, 1058-1067
44. Solan, N. J., Miyoshi, H., Carmona, E. M., Bren, G. D., and Paya, C. V. (2002) RelB cellular regulation and transcriptional activity are regulated by p100. J. Biol. Chem. 277, 1405-1418
45. Xiao, G., Fong, A., and Sun, S. C. (2004) Induction of p100 processing by NF-κB-inducing kinase involves docking IκB kinase α (IKKα) to p100 and IKKα-mediated phosphorylation. J. Biol. Chem. 279, 30099-30105
46. Qu, Z., Qing, G., Rabson, A., and Xiao, G. (2004) Tax deregulation of NF-κB2 p100 processing involves both β-TrCP-dependent and -independent mechanisms. J. Biol. Chem. 279, 44563-44572
47. Meyer, H. J., and Rape, M. (2014) Enhanced protein degradation by branched ubiquitin chains. Cell 157, 910-921
48. Zhang, J., Chang, C. C., Lombardi, L., and Dalla-Favera, R. (1994) Rearranged NFKB2 gene in the HUT78 T-lymphoma cell line codes for a constitutively nuclear factor lacking transcriptional repressor functions. Oncogene 9, 1931-1937
49. Yilmaz, Z. B., Kofahl, B., Beaudette, P., Baum, K., Ipenberg, I., Weih, F., Wolf, J., Dittmar, G., and Scheidereit, C. (2014) Quantitative dissection and modeling of the NF-κB p100-p105 module reveals interdependent precursor proteolysis. Cell Rep 9, 1756-1769