Nuclear to cytoplasmic translocation of heterogeneous nuclear ribonucleoprotein U enhances TLR-induced proinflammatory cytokine production by stabilizing mRNAs in macrophages

Journal of Immunology

Volumn 188, Issue 7, 2012, Pages 3179-3187

  Zhao, Wei ^a   Wang, Lijuan ^a   Zhang, Meng ^a   Wang, Peng ^a   Qi, Jianni ^a   Zhang, Lei ^a   Gao, Chengjiang ^a  

^a SHANDONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROGENOUS NUCLEAR RIBONUCLEOPROTEIN U; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; RIBONUCLEOPROTEIN; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL STIMULATION; CELL TRANSPORT; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOPLASM; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; HALF LIFE TIME; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN TRANSPORT; RECEPTOR BINDING; REGULATORY MECHANISM; RNA STABILITY; SIGNAL TRANSDUCTION; TURNOVER TIME;

ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CELL LINE; CELL NUCLEUS; CYTOKINES; CYTOPLASM; FEMALE; GENE EXPRESSION REGULATION; GENES, REPORTER; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN U; INFLAMMATION; INTERLEUKINS; MACROPHAGES; MICE; MICE, INBRED C57BL; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; RNA STABILITY; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; TRANSFECTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84859396071     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101175     Document Type: Article

References (32)

1. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801. (Pubitemid 43261452)
2. Kawai, T., and S. Akira. 2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11: 373-384.
3. Beutler, B., Z. Jiang, P. Georgel, K. Crozat, B. Croker, S. Rutschmann, X. Du, and K. Hoebe. 2006. Genetic analysis of host resistance: Toll-like receptor signaling and immunity at large. Annu. Rev. Immunol. 24: 353-389.
4. Anderson, P. 2008. Post-transcriptional control of cytokine production. Nat. Immunol. 9: 353-359. (Pubitemid 351405104)
5. Stoecklin, G., and P. Anderson. 2006. Posttranscriptional mechanisms regulating the inflammatory response. Adv. Immunol. 89: 1-37.
6. Romig, H., F. O. Fackelmayer, A. Renz, U. Ramsperger, and A. Richter. 1992. Characterization of SAF-A, a novel nuclear DNA binding protein from HeLa cells with high affinity for nuclear matrix/scaffold attachment DNA elements. EMBO J. 11: 3431-3440.
7. Göhring, F., B. L. Schwab, P. Nicotera, M. Leist, and F. O. Fackelmayer. 1997. The novel SAR-binding domain of scaffold attachment factor A (SAF-A) is a target in apoptotic nuclear breakdown. EMBO J. 16: 7361-7371. (Pubitemid 28010496)
8. Kiledjian, M., and G. Dreyfuss. 1992. Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box. EMBO J. 11: 2655-2664.
9. Roshon, M. J., and H. E. Ruley. 2005. Hypomorphic mutation in hnRNP U results in post-implantation lethality. Transgenic Res. 14: 179-192. (Pubitemid 40747897)
10. Martens, J. H., M. Verlaan, E. Kalkhoven, J. C. Dorsman, and A. Zantema. 2002. Scaffold/matrix attachment region elements interact with a p300-scaffold attachment factor A complex and are bound by acetylated nucleosomes. Mol. Cell. Biol. 22: 2598-2606. (Pubitemid 34262982)
11. Eggert, M., J. Michel, S. Schneider, H. Bornfleth, A. Baniahmad, F. O. Fackelmayer, S. Schmidt, and R. Renkawitz. 1997. The glucocorticoid receptor is associated with the RNA-binding nuclear matrix protein hnRNP U. J. Biol. Chem. 272: 28471-28478. (Pubitemid 27517795)
12. Howell, M., C. Borchers, and S. L. Milgram. 2004. Heterogeneous nuclear ribonuclear protein U associates with YAP and regulates its co-activation of Bax transcription. J. Biol. Chem. 279: 26300-26306. (Pubitemid 38798779)
13. Ameyar-Zazoua, M., M. Souidi, L. Fritsch, P. Robin, A. Thomas, A. Hamiche, P. Percipalle, S. Ait-Si-Ali, and A. Harel-Bellan. 2009. Physical and functional interaction between heterochromatin protein 1alpha and the RNA-binding protein heterogeneous nuclear ribonucleoprotein U. J. Biol. Chem. 284: 27974-27979.
14. Kawano, S., M. Miyaji, S. Ichiyasu, K. M. Tsutsui, and K. Tsutsui. 2010. Regulation of DNA topoisomerase IIbeta through RNA-dependent association with heterogeneous nuclear ribonucleoprotein U (hnRNP U). J. Biol. Chem. 285: 26451-26460.
15. Obrdlik, A., A. Kukalev, E. Louvet, A. K. Farrants, L. Caputo, and P. Percipalle. 2008. The histone acetyltransferase PCAF associates with actin and hnRNP U for RNA polymerase II transcription. Mol. Cell. Biol. 28: 6342-6357.
16. Davis, M., A. Hatzubai, J. S. Andersen, E. Ben-Shushan, G. Z. Fisher, A. Yaron, A. Bauskin, F. Mercurio, M. Mann, and Y. Ben-Neriah. 2002. Pseudosubstrate regulation of the SCF(beta-TrCP) ubiquitin ligase by hnRNP-U. Genes Dev. 16: 439-451. (Pubitemid 34165101)
17. Tsuchiya, Y., T. Asano, K. Nakayama, T. Kato, Jr., M. Karin, and H. Kamata. 2010. Nuclear IKKbeta is an adaptor protein for IkappaBalpha ubiquitination and degradation in UV-induced NF-kappaB activation. Mol. Cell 39: 570-582.
18. Hasegawa, Y., N. Brockdorff, S. Kawano, K. Tsutui, K. Tsutui, and S. Nakagawa. 2010. The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev. Cell 19: 469-476.
19. Pullirsch, D., R. Härtel, H. Kishimoto, M. Leeb, G. Steiner, and A. Wutz. 2010. The Trithorax group protein Ash2l and Saf-A are recruited to the inactive X chromosome at the onset of stable X inactivation. Development 137: 935-943.
20. Gao, C., H. Guo, Z. Mi, P. Y.Wai, and P. C. Kuo. 2005. Transcriptional regulatory functions of heterogeneous nuclear ribonucleoprotein-U and -A/B in endotoxin-mediated macrophage expression of osteopontin. J. Immunol. 175: 523-530. (Pubitemid 40884358)
21. Zhao, W., L. Wang, L. Zhang, C. Yuan, P. C. Kuo, and C. Gao. 2010. Differential expression of intracellular and secreted osteopontin isoforms by murine macrophages in response to Toll-like receptor agonists. J. Biol. Chem. 285: 20452-20461.
22. Chen, C. Y., and A. B. Shyu. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20: 465-470.
23. Khabar, K. S. 2010. Post-transcriptional control during chronic inflammation and cancer: a focus on AU-rich elements. Cell. Mol. Life Sci. 67: 2937-2955.
24. Liew, F. Y., D. Xu, E. K. Brint, and L. A. O'Neill. 2005. Negative regulation of Toll-like receptor-mediated immune responses. Nat. Rev. Immunol. 5: 446-458. (Pubitemid 40835033)
25. Han, S. P., Y. H. Tang, and R. Smith. 2010. Functional diversity of the hnRNPs: past, present and perspectives. Biochem. J. 430: 379-392.
26. Lu, J. Y., N. Sadri, and R. J. Schneider. 2006. Endotoxic shock in AUF1 knockout mice mediated by failure to degrade proinflammatory cytokine mRNAs. Genes Dev. 20: 3174-3184. (Pubitemid 44790631)
27. Paschoud, S., A. M. Dogar, C. Kuntz, B. Grisoni-Neupert, L. Richman, and L. C. Kühn. 2006. Destabilization of interleukin-6 mRNA requires a putative RNA stem-loop structure, an AU-rich element, and the RNA-binding protein AUF1. Mol. Cell. Biol. 26: 8228-8241. (Pubitemid 44748560)
28. Sarkar, B., Q. Xi, C. He, and R. J. Schneider. 2003. Selective degradation of AU-rich mRNAs promoted by the p37 AUF1 protein isoform. Mol. Cell. Biol. 23: 6685-6693. (Pubitemid 37075777)
29. Woo, J. S., J. H. Imm, C. K. Min, K. J. Kim, S. S. Cha, and B. H. Oh. 2006. Structural and functional insights into the B30.2/SPRY domain. EMBO J. 25: 1353-1363.
30. Spraggon, L., T. Dudnakova, J. Slight, O. Lustig-Yariv, J. Cotterell, N. Hastie, and C. Miles. 2007. hnRNP-U directly interacts with WT1 and modulates WT1 transcriptional activation. Oncogene 26: 1484-1491. (Pubitemid 46340810)
31. Britton, S., C. Froment, P. Frit, B. Monsarrat, B. Salles, and P. Calsou. 2009. Cell nonhomologous end joining capacity controls SAF-A phosphorylation by DNAPK in response to DNA double-strand breaks inducers. Cell Cycle 8: 3717-3722.
32. Berglund, F. M., and P. R. Clarke. 2009. hnRNP-U is a specific DNA-dependent protein kinase substrate phosphorylated in response to DNA double-strand breaks. Biochem. Biophys. Res. Commun. 381: 59-64.