Advertisement

Molecular Biology Reports

, Volume 39, Issue 11, pp 9911–9919 | Cite as

TNFAIP1 interacts with KCTD10 to promote the degradation of KCTD10 proteins and inhibit the transcriptional activities of NF-κB and AP-1

  • Xiang Hu
  • Feng Yan
  • Fangmei Wang
  • Zijian Yang
  • Ling Xiao
  • Li Li
  • Shuanglin Xiang
  • Jianlin Zhou
  • Xiaofeng Ding
  • Jian Zhang
Article

Abstract

The broad-complex, tramtrack, and bric-a-brac/poxvirus and zinc finger domain-containing protein tumor necrosis factor, alpha-induced protein 1 (TNFAIP1) was first identified as a gene whose expression can be induced by the tumor necrosis factor alpha. Some studies showed that TNFAIP1 may function in DNA replication, apoptosis and human diseases. However, the definite functions and the mechanisms of TNFAIP1 are poorly known. In this study, we performed a yeast two-hybrid assay and used TNFAIP1 as the bait to screen human brain cDNA library. Potassium channel tetramerisation domain containing 10 (KCTD10) was identified as TNFAIP1-interacting partner. The KCTD10–TNFAIP1 interaction was then confirmed by the in vitro GST pull-down assays and the in vivo co-immunoprecipitation and colocalization assays. In addition, protein degradation and ubiquitin assays revealed TNFAIP1 overexpression resulted in ubiquitin-mediated degradation of KCTD10 proteins, which was significantly alleviated with the proteasome inhibitor MG132 treatment. Furthermore, transient transfection assays with two reporters showed that TNFAIP1 and KCTD10 inhibited the transcriptional activities of nuclear factor kappa B (NF-κB) and activating protein-1 reporters. Taken together, our results indicated the novel interaction and function between KCTD10 and TNFAIP1 in human PDIP1 family.

Keywords

TNFAIP1 gene KCTD10 gene BTB domain Protein degradation Transcription inhibition 

Notes

Acknowledgments

We thank Dr. Yue Xiong (University of North Carolina at Chapel Hill), for providing Cul-3 and ubiquitin constructs. This work was supported in part by the 973 project of Ministry of Science and Technique of China (No. 2009ZX08010-024B), the Program for The National Natural Science Foundation of China (No. 30900827) and the Science & Technology Department of Hunan Province (No. 2011FJ3140, No. 2011TT2008).

References

  1. 1.
    He H, Tan CK, Downey KM, So AG (2001) A tumor necrosis factor alpha- and interleukin 6-inducible protein that interacts with the small subunit of DNA polymerase delta and proliferating cell nuclear antigen. Proc Natl Acad Sci USA 98:11979–11984PubMedCrossRefGoogle Scholar
  2. 2.
    Zhou J, Hu X, Xiong X, Liu X, Liu Y, Ren K, Jiang T, Hu X, Zhang J (2005) Cloning of two rat PDIP1 related genes and their interactions with proliferating cell nuclear antigen. J Exp Zool A Comp Exp Biol 303:227–240PubMedGoogle Scholar
  3. 3.
    Zhou J, Ren K, Liu X, Xiong X, Hu X, Zhang J (2005) A novel PDIP1-related protein, KCTD10, that interacts with proliferating cell nuclear antigen and DNA polymerase delta. Biochim Biophys Acta 1729:200–203PubMedCrossRefGoogle Scholar
  4. 4.
    Wang Y, Zheng Y, Luo F, Fan X, Chen J, Zhang C, Hui R (2009) KCTD10 interacts with proliferating cell nuclear antigen and its down-regulation could inhibit cell proliferation. J Cell Biochem 106:409–413PubMedCrossRefGoogle Scholar
  5. 5.
    Liu M, Sun Z, Zhou A, Li H, Yang L, Zhou C, Liu R, Hu X, Zhou J, Xiang S, Zhang J (2010) Functional characterization of the promoter region of human TNFAIP1 gene. Mol Biol Rep 37:1699–1705PubMedCrossRefGoogle Scholar
  6. 6.
    Yang L, Liu N, Hu X, Zhang W, Wang T, Li H, Zhang B, Xiang S, Zhou J, Zhang J (2010) CK2 phosphorylates TNFAIP1 to affect its subcellular localization and interaction with PCNA. Mol Biol Rep 37:2967–2973PubMedCrossRefGoogle Scholar
  7. 7.
    Locksley RM, Killeen N, Lenardo MJ (2001) The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104:487–501PubMedCrossRefGoogle Scholar
  8. 8.
    Mencoboni M, Lerza R, Bogliolo G (1992) Tumor necrosis factor: a cytokine with multiple actions. Recent Prog Med 83:15–17Google Scholar
  9. 9.
    Wolf FW, Marks RM, Sarma V, Byers MG, Katz RW, Shows TB, Dixit VM (1992) Characterization of a novel tumor necrosis factor-alpha-induced endothelial primary response gene. J Biol Chem 267:1317–1326PubMedGoogle Scholar
  10. 10.
    Yang L, Zhou A, Li H, Zhang W, Wu Y, Zhang J, Han M (2006) Expression profile in the cell lines of human TNFAIP1 gene. Hereditas 28:918–922PubMedGoogle Scholar
  11. 11.
    Xiong X, Liu X, Hu X, Jiang X, Liu Y, Zhang J (2004) Differential expression analysis of B12 gene after mouse partial hepatectomy. J Nat Sci Hunan Norm Univ 27:71–74Google Scholar
  12. 12.
    Liu XW, Lu FG, Zhang GS, Wu XP, You Y, Ouyang CH, Yang DY (2004) Proteomics to display tissue repair opposing injury response to LPS-induced liver injury. World J Gastroenterol 10:2701–2705PubMedGoogle Scholar
  13. 13.
    Lin MC, Lee NP, Zheng N, Yang PH, Wong OG, Kung HF, Hui CK, Luk JM, Lau GK (2005) Tumor necrosis factor-alpha-induced protein 1 and immunity to hepatitis B virus. World J Gastroenterol 11:7564–7568PubMedGoogle Scholar
  14. 14.
    Link CD, Taft A, Kapulkin V, Duke K, Kim S, Fei Q, Wood DE, Sahagan BG (2003) Gene expression analysis in a transgenic caenorhabditis elegans Alzheimer’s disease model. Neurobiol Aging 24:397–413PubMedCrossRefGoogle Scholar
  15. 15.
    Zhang W, Zhou A, Yang L, Li H, Zhang J (2006) Expression and preparation of antiserum of human KCTD10 and its expression profile in the cell lines. Acta Laser Biol Sinica 15:496–500Google Scholar
  16. 16.
    Ding X, Fan C, Zhou J, Zhong Y, Liu R, Ren K, Hu X, Luo C, Xiao S, Wang Y, Feng D, Zhang J (2006) GAS41 interacts with transcription factor AP-2beta and stimulates AP-2beta-mediated transactivation. Nucleic Acids Res 34:2570–2578PubMedCrossRefGoogle Scholar
  17. 17.
    Ding X, Luo C, Zhou J, Zhong Y, Hu X, Zhou F, Ren K, Gan L, He A, Zhu J, Gao X, Zhang J (2009) The interaction of KCTD1 with transcription factor AP-2alpha inhibits its transactivation. J Cell Biochem 106:285–295PubMedCrossRefGoogle Scholar
  18. 18.
    Kim DM, Chung KS, Choi SJ, Jung YJ, Park SK, Han GH, Ha JS, Song KB, Choi NS, Kim HM, Won M, Seo YS (2009) RhoB induces apoptosis via direct interaction with TNFAIP1 in HeLa cells. Int J Cancer 125:2520–2527PubMedCrossRefGoogle Scholar
  19. 19.
    Sun JK, Zhang B, Zhang J, Zhou JL (2007) Preparation of mouse KCTD10 antibody and expression analysis of KCTD10 in neuroepithelium of neural tube and dorsal root ganglion. Sheng Wu Gong Cheng Xue Bao 23:1011–1016PubMedGoogle Scholar
  20. 20.
    Ahmad KF, Engel CK, Prive GG (1998) Crystal structure of the BTB domain from PLZF. Proc Natl Acad Sci USA 95:12123–12128PubMedCrossRefGoogle Scholar
  21. 21.
    Cullinan SB, Gordan JD, Jin J, Harper JW, Diehl JA (2004) The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase. Mol Cell Biol 24:8477–8486PubMedCrossRefGoogle Scholar
  22. 22.
    Kwon JE, La M, Oh KH, Oh YM, Kim GR, Seol JH, Baek SH, Chiba T, Tanaka K, Bang OS, Joe CO, Chung CH (2006) BTB domain-containing speckle-type POZ protein (SPOP) serves as an adaptor of daxx for ubiquitination by Cul3-based ubiquitin ligase. J Biol Chem 281:12664–12672PubMedCrossRefGoogle Scholar
  23. 23.
    Furukawa M, Xiong Y (2005) BTB protein Keap1 targets antioxidant transcription factor Nrf2 for ubiquitination by the cullin 3-Roc1 ligase. Mol Cell Biol 25:162–171PubMedCrossRefGoogle Scholar
  24. 24.
    Bayon Y, Trinidad AG, de la Puerta ML, Del Carmen Rodriguez M, Bogetz J, Rojas A, De Pereda JM, Rahmouni S, Williams S, Matsuzawa S, Reed JC, Crespo MS, Mustelin T, Alonso A (2008) KCTD5, a putative substrate adaptor for cullin3 ubiquitin ligases. FEBS J 275:3900–3910PubMedCrossRefGoogle Scholar
  25. 25.
    Correale S, Pirone L, Di Marcotullio L, De Smaele E, Greco A, Mazza D, Moretti M, Alterio V, Vitagliano L, Di Gaetano S, Gulino A, Pedone EM (2011) Molecular organization of the cullin E3 ligase adaptor KCTD11. Biochimie 93:715–724PubMedCrossRefGoogle Scholar
  26. 26.
    Li X, Peng H, Schultz DC, Lopez-Guisa JM, Rauscher FJ 3rd, Marmorstein R (1999) Structure-function studies of the BTB/POZ transcriptional repression domain from the promyelocytic leukemia zinc finger oncoprotein. Cancer Res 59:5275–5282PubMedGoogle Scholar
  27. 27.
    Ding XF, Luo C, Ren KQ, Zhang J, Zhou JL, Hu X, Liu RS, Wang Y, Gao X, Zhang J (2008) Characterization and expression of a human KCTD1 gene containing the BTB domain, which mediates transcriptional repression and homomeric interactions. DNA Cell Biol 27:257–265PubMedCrossRefGoogle Scholar
  28. 28.
    Prajapati B, Singhal M, Yashwant, Sharma GN, Gupta V (2010) Role of NFkB in various immunological & inflammatory disorders. Int J Toxicol Pharmacol Res 2:35–39Google Scholar
  29. 29.
    Tian B, Brasier AR (2003) Identification of a nuclear factor kappa B-dependent gene network. Recent Prog Horm Res 58:95–130PubMedCrossRefGoogle Scholar
  30. 30.
    Td G (2006) Introduction to NF-κB players, pathways, perspectives. Oncogene 25:6680–6684CrossRefGoogle Scholar
  31. 31.
    Glover JNHS (1995) Crystal structure of the heterodimeric bZIP transcription factor c-Fos-c-Jun bound to DNA. Nature 373:257–261PubMedCrossRefGoogle Scholar
  32. 32.
    Ameyar MWM, Weitzman JB (2003) A role for AP-1 in apoptosis: the case for and against. Biochimie 85:747–752PubMedCrossRefGoogle Scholar
  33. 33.
    Li Q, Verma IM (2002) NF-kappaB regulation in the immune system. Nat Rev Immunol 2:725–734PubMedCrossRefGoogle Scholar
  34. 34.
    Shaulian E, Karin M (2002) AP-1 as a regulator of cell life and death. Nat Cell Biol 4:E131–E136PubMedCrossRefGoogle Scholar
  35. 35.
    Fujioka S, Niu J, Schmidt C, Sclabas GM, Peng B, Uwagawa T, Li Z, Evans DB, Abbruzzese JL, Chiao PJ (2004) NF-kappaB and AP-1 connection: mechanism of NF-kappaB-dependent regulation of AP-1 activity. Mol Cell Biol 24:7806–7819PubMedCrossRefGoogle Scholar
  36. 36.
    Wu HM, Wen HC, Lin WW (2002) Proteasome inhibitors stimulate interleukin-8 expression via ras and apoptosis signal-regulating kinase-dependent extracellular signal-related kinase and c-Jun N-terminal kinase activation. Am J Respir Cell Mol Biol 27:234–243PubMedGoogle Scholar
  37. 37.
    Ortiz-Lazareno PC, Hernandez-Flores G, Dominguez-Rodriguez JR, Lerma-Diaz JM, Jave-Suarez LF, Aguilar-Lemarroy A, Gomez-Contreras PC, Scott-Algara D, Bravo-Cuellar A (2008) MG132 proteasome inhibitor modulates proinflammatory cytokines production and expression of their receptors in U937 cells: involvement of nuclear factor-kappaB and activator protein-1. Immunology 124:534–541PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Xiang Hu
    • 1
  • Feng Yan
    • 1
  • Fangmei Wang
    • 1
  • Zijian Yang
    • 1
  • Ling Xiao
    • 1
  • Li Li
    • 1
  • Shuanglin Xiang
    • 1
  • Jianlin Zhou
    • 1
  • Xiaofeng Ding
    • 1
  • Jian Zhang
    • 1
  1. 1.Key Laboratory of Protein Chemistry and Developmental Biology of State Education Ministry of China, College of Life ScienceHunan Normal UniversityChangshaChina

Personalised recommendations