Post-transcriptional regulation of the human inducible nitric oxide synthase (iNOS) expression by the cytosolic poly(A)-binding protein (PABP)

Nitric Oxide - Biology and Chemistry

Volumn 33, Issue , 2013, Pages 6-17

  Casper, Ingrid ^a   Nowag, Sebastian ^a   Koch, Kathrin ^a   Hubrich, Thomas ^a   Bollmann, Franziska ^a   Henke, Jenny ^a   Schmitz, Katja ^a   Kleinert, Hartmut ^a   Pautz, Andrea ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

INOS; MRNA stability; PABP; SiRNA; UTR

Indexed keywords

BETA 2 MICROGLOBULIN; CYTOKINE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; POLYADENYLIC ACID BINDING PROTEIN; RNA; RNA POLYMERASE II; RNA POLYMERASE IIA; SMALL INTERFERING RNA; STAT1 PROTEIN; STAT1A PROTEIN; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; BINDING SITE; CONTROLLED STUDY; CYTOSOL; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; RECEPTOR DOWN REGULATION; REPORTER GENE; RNA INTERFERENCE; ULTRAVIOLET RADIATION;

3′-UNTRANSLATED REGION; 3′-UTR; 5′-UNTRANSLATED REGION; 5′-UTR; 6-DICHLORO-1-RIBOFURANOSYLBENZIMIDAZOLE; ARE; ARE BINDING PROTEIN; ARE-BP; AU-RICH ELEMENT; AU-RICH ELEMENT RNA BINDING PROTEIN 1; AUF1; CDS; CM; CO; CODING SEQUENCE; CONTROL CELLS; CYTOKINE MIXTURE; DRB; EGFP; ELAV; EMBRYONIC LETHAL ABNORMAL VISION; ENHANCED GREEN FLUORESCENCE PROTEIN; ERF3; EUKARYOTIC RELEASE FACTOR 3; FACS; FLUORESCENT ACTIVATED CELL SORTING; GAPDH; GLUTATHIONE S-TRANSFERASE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE; GST; HETERONUCLEAR RIBONUCLEOPROTEIN; HNRNP; HUMAN ANTIGEN R; HUR; IFN-Γ; IL-1Β; IMMUNOPRECIPITATION; INDUCIBLE NO-SYNTHASE; INOS; INTERFERON-Γ; INTERLEUKIN-1Β; IP; KH-TYPE SPLICING REGULATORY PROTEIN; KSRP; LUC; LUCIFERASE; MRNA STABILITY; NITRIC OXIDE; NO; PABP; POL 2A; POLY(A)BINDING PROTEIN; QRT-PCR; QUANTITATIVE REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA POLYMERASE II GREAT SUBUNIT; SHRNA; SIRNA; SMALL HAIRPIN RNA; SMALL INTERFERING RNA; TNF-Α; TRISTETRAPROLIN; TTP; TUMOR NECROSIS FACTOR-Α; UTR; WB; WESTERN BLOT; Y BOX FACTOR-1; YB-1; Β-TUB.; Β-TUBULIN; Β2-MICROGLOBULIN; Β2M;

3' UNTRANSLATED REGIONS; BINDING SITES; CELL LINE, TUMOR; CYTOKINES; DOWN-REGULATION; HUMANS; MUTATION; NITRIC OXIDE SYNTHASE TYPE II; POLY(A)-BINDING PROTEINS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER;

EID: 84885137979     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2013.05.002     Document Type: Article

References (58)

1. C. Bogdan, M. Rollinghoff, A. Diefenbach, Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity, Curr. Opin. Immunol. 12 (2000) 64-76. (Pubitemid 30093452)
2. K.D. Kroncke, K. Fehsel, V. Kolb-Bachofen, Inducible nitric oxide synthase in human diseases, Clin. Exp. Immunol. 113 (1998) 147-156. (Pubitemid 28352831)
3. A. Pautz, J. Art, S. Hahn, S. Nowag, C. Voss, H. Kleinert, Regulation of the expression of inducible nitric oxide synthase, Nitric Oxide 23 (2010) 75-93.
4. F. Rodriguez-Pascual, M. Hausding, I. Ihrig-Biedert, H. Furneaux, A.P. Levy, U. Förstermann, H. Kleinert, Complex contribution of the 30-untranslated region to the expressional regulation of the human inducible nitric-oxide synthase gene. Involvement of the RNA-binding protein HuR, J. Biol. Chem. 275 (2000) 26040-26049.
5. M. Fechir, K. Linker, A. Pautz, T. Hubrich, U. Forstermann, F. Rodriguez-Pascual, H. Kleinert, Tristetraprolin regulates the expression of the human inducible nitric-oxide synthase gene, Mol. Pharmacol. 67 (2005) 2148-2161. (Pubitemid 41007794)
6. W. Eberhardt, A. Doller, S. Akool el, J. Pfeilschifter, Modulation of mRNA stability as a novel therapeutic approach, Pharmacol. Ther. 114 (2007) 56-73. (Pubitemid 46498160)
7. Z. Guo, L. Shao, L. Zheng, Q. Du, P. Li, B. John, D.A. Geller, MiRNA-939 regulates human inducible nitric oxide synthase posttranscriptional gene expression in human hepatocytes, Proc. Natl. Acad. Sci. USA 109 (2012) 5826-5831.
8. K. Linker, A. Pautz, M. Fechir, T. Hubrich, J. Greeve, H. Kleinert, Involvement of KSRP in the post-transcriptional regulation of human iNOS expressioncomplex interplay of KSRP with TTP and HuR, Nucleic Acids Res. 33 (2005) 4813-4827. (Pubitemid 41418881)
9. A. Pautz, K. Linker, T. Hubrich, R. Korhonen, S. Altenhofer, H. Kleinert, The polypyrimidine tract-binding protein (PTB) is involved in the posttranscriptional regulation of human inducible nitric oxide synthase expression, J. Biol. Chem. 281 (2006) 32294-32302. (Pubitemid 46036783)
10. A. Pautz, K. Linker, S. Altenhofer, S. Heil, N. Schmidt, J. Art, S. Knauer, R. Stauber, N. Sadri, A. Pont, R.J. Schneider, H. Kleinert, Similar regulation of human inducible nitric-oxide synthase expression by different isoforms of the RNAbinding protein AUF1, J. Biol. Chem. 284 (2009) 2755-2766.
11. J. Bag, R.B. Bhattacharjee, Multiple levels of post-transcriptional control of expression of the poy (A)-binding protein, RNA Biol. 7 (2010) 5-12.
12. R.W. Smith, N.K. Gray, Poly(A)-binding protein (PABP): a common viral target, Biochem. J. 426 (2010) 1-12.
13. U. Kuhn, E. Wahle, Structure and function of poly(A) binding proteins, Biochim. Biophys. Acta 1678 (2004) 67-84. (Pubitemid 38626168)
14. B. Gorgoni, N.K. Gray, The roles of cytoplasmic poly(A)-binding proteins in regulating gene expression: a developmental perspective, Brief. Funct. Genomic. Proteomic. 3 (2004) 125-141.
15. S. Cheng, D.R. Gallie, EIF4G, eIFiso4G, and eIF4B bind the poly(A)-binding protein through overlapping sites within the RNA recognition motif domains, J. Biol. Chem. 282 (2007) 25247-25258. (Pubitemid 47372779)
16. S. Ma, R.B. Bhattacharjee, J. Bag, Expression of poly(A)-binding protein is upregulated during recovery from heat shock in HeLa cells, FEBS J. 276 (2009) 552-570.
17. R. Soto-Rifo, P.S. Rubilar, T. Limousin, S. de Breyne, D. Decimo, T. Ohlmann, DEAD-box protein DDX3 associates with eIF4F to promote translation of selected mRNAs, EMBO J. 31 (2012) 3745-3756.
18. D.A. Mangus, M.C. Evans, A. Jacobson, Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression, Genome Biol. 4 (2003) 223.
19. S. Hoshino, M. Imai, T. Kobayashi, N. Uchida, T. Katada, The eukaryotic polypeptide chain releasing factor (eRF3/GSPT) carrying the translation termination signal to the 30-poly(A) tail of mRNA. Direct association of erf3/ GSPT with polyadenylate-binding protein, J. Biol. Chem. 274 (1999) 16677-16680.
20. N. Uchida, S. Hoshino, H. Imataka, N. Sonenberg, T. Katada, A novel role of the mammalian GSPT/eRF3 associating with poly(A)-binding protein in Cap/ Poly(A)-dependent translation, J. Biol. Chem. 277 (2002) 50286-50292. (Pubitemid 36042176)
21. S. Hoshino, N. Hosoda, Y. Araki, T. Kobayashi, N. Uchida, Y. Funakoshi, T. Katada, Novel function of the eukaryotic polypeptide-chain releasing factor 3 (eRF3/GSPT) in the mRNA degradation pathway, Biochemistry. Biokhimiia 64 (1999) 1367-1372. (Pubitemid 129597021)
22. O.V. Skabkina, M.A. Skabkin, N.V. Popova, D.N. Lyabin, L.O. Penalva, L.P. Ovchinnikov, Poly(A)-binding protein positively affects YB-1 mRNA translation through specific interaction with YB-1 mRNA, J. Biol. Chem. 278 (2003) 18191-18198. (Pubitemid 36799435)
23. S.D. Kulkarni, B. Muralidharan, A.C. Panda, B. Bakthavachalu, A. Vindu, V. Seshadri, Glucose-stimulated translation regulation of insulin by the 50 UTRbinding proteins, J. Biol. Chem. 286 (2011) 14146-14156.
24. M.R. Fabian, G. Mathonnet, T. Sundermeier, H. Mathys, J.T. Zipprich, Y.V. Svitkin, F. Rivas, M. Jinek, J. Wohlschlegel, J.A. Doudna, C.Y. Chen, A.B. Shyu, J.R. Yates 3rd, G.J. Hannon, W. Filipowicz, T.F. Duchaine, N. Sonenberg, Mammalian miRNA RISC recruits CAF1 and PABP to affect PABP-dependent deadenylation, Mol. Cell 35 (2009) 868-880.
25. T.C. Chang, A. Yamashita, C.Y. Chen, Y. Yamashita, W. Zhu, S. Durdan, A. Kahvejian, N. Sonenberg, A.B. Shyu, UNR, a new partner of poly(A)-binding protein, plays a key role in translationally coupled mRNA turnover mediated by the c-fos major coding-region determinant, Genes Dev. 18 (2004) 2010-2023. (Pubitemid 39071582)
26. F. Tritschler, E. Huntzinger, E. Izaurralde, Role of GW182 proteins and PABPC1 in the miRNA pathway: a sense of deja vu, Nat. Rev. Mol. Cell Biol. 11 (2010) 379-384.
27. R.W. Walters, S.S. Bradrick, M. Gromeier, Poly(A)-binding protein modulates mRNA susceptibility to cap-dependent miRNA-mediated repression, RNA 16 (2010) 239-250.
28. E. Huntzinger, D. Kuzuoglu-Ozturk, J.E. Braun, A. Eulalio, L. Wohlbold, E. Izaurralde, The interactions of GW182 proteins with PABP and deadenylases are required for both translational repression and degradation of miRNA targets, Nucleic Acids Res. 41 (2012) 978-994.
29. R.T. Sladic, C.A. Lagnado, C.J. Bagley, G.J. Goodall, Human PABP binds AU-rich RNA via RNA-binding domains 3 and 4, Eur J. Biochem./FEBS 271 (2004) 450-457. (Pubitemid 38130472)
30. K. Nagaoka, T. Suzuki, T. Kawano, K. Imakawa, S. Sakai, Stability of casein mRNA is ensured by structural interactions between the 30-untranslated region and poly(A) tail via the HuR and poly(A)-binding protein complex, Biochim. Biophys. Acta 1759 (2006) 132-140. (Pubitemid 43816114)
31. F. Bollig, R. Winzen, M. Gaestel, S. Kostka, K. Resch, H. Holtmann, Affinity purification of ARE-binding proteins identifies polyA-binding protein 1 as a potential substrate in MK2-induced mRNA stabilization, Biochem. Biophys. Res. Commun. 301 (2003) 665-670. (Pubitemid 36268942)
32. S. Ma, T. Musa, J. Bag, Reduced stability of mitogen-activated protein kinase kinase-2 mRNA and phosphorylation of poly(A)-binding protein (PABP) in cells overexpressing PABP, J. Biol. Chem. 281 (2006) 3145-3156. (Pubitemid 43845924)
33. P. Vazquez-Pianzola, H. Urlaub, B. Suter, Pabp binds to the osk 30UTR and specifically contributes to osk mRNA stability and oocyte accumulation, Dev. Biol. 357 (2011) 404-418.
34. E. Hornstein, H. Harel, G. Levy, O. Meyuhas, Overexpression of poly(A)-binding protein down-regulates the translation or the abundance of its own mRNA, FEBS Lett. 457 (1999) 209-213. (Pubitemid 29401929)
35. H. Kleinert, C. Euchenhofer, G. Fritz, I. Ihrig-Biedert, U. Forstermann, Involvement of protein kinases in the induction of NO synthase II in human DLD-1 cells, Br. J. Pharmacol. 123 (1998) 1716-1722. (Pubitemid 28182056)
36. P. Chomczynski, N. Sacchi, Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction, Anal. Biochem. 162 (1987) 156-159. (Pubitemid 17064313)
37. H. Kleinert, C. Euchenhofer, I. Ihrig Biedert, U. Forstermann, Glucocorticoids inhibit the induction of nitric oxide synthase II by down-regulating cytokineinduced activity of transcription factor nuclear factor-kB, Mol. Pharmacol. 49 (1996) 15-21.
38. N. Schmidt, A. Pautz, J. Art, P. Rauschkolb, M. Jung, G. Erkel, M.B. Goldring, H. Kleinert, Transcriptional and post-transcriptional regulation of iNOS expression in human chondrocytes, Biochem. Pharmacol. 79 (2010) 722-732.
39. K.J. Livak, T.D. Schmittgen, Analysis of relative gene expression data using realtime quantitative PCR and the 2(-Delta Delta C(T)) method, Methods 25 (2001) 402-408. (Pubitemid 34164012)
40. G.M. Wilson, G. Brewer, Identification and characterization of proteins binding A + U-rich elements, Methods 17 (1999) 74-83. (Pubitemid 29440549)
41. R. Windoffer, A. Kolsch, S. Woll, R.E. Leube, Focal adhesions are hotspots for keratin filament precursor formation, J. Cell Biol. 173 (2006) 341-348.
42. M.E. de Vera, R.A. Shapiro, A.K. Nüssler, J.S. Mudgett, R.L. Simmons, S.M. Morris Jr., T.R. Billiar, D.A. Geller, Transcriptional regulation of human inducible nitric oxide synthase (NOS2) gene by cytokines: initial analysis of the human NOS2 promoter, Proc. Natl. Acad. Sci. USA 93 (1996) 1054-1059. (Pubitemid 26052841)
43. G. Singh, T.A. Cooper, Minigene reporter for identification and analysis of cis elements and trans factors affecting pre-mRNA splicing, Biotechniques 41 (2006) 177-181. (Pubitemid 46542601)
44. C. Grosset, C.Y. Chen, N. Xu, N. Sonenberg, H. Jacquemin-Sablon, A.B. Shyu, A mechanism for translationally coupled mRNA turnover: interaction between the poly(A) tail and a c-fos RNA coding determinant via a protein complex, Cell 103 (2000) 29-40.
45. C.Y. Chen, A.B. Shyu, AU-rich elements: characterization and importance in mRNA degradation, Trends Biochem. Sci. 20 (1995) 465-470.
46. T. Bakheet, M. Frevel, B.R. Williams, W. Greer, K.S. Khabar, ARED: human AUrich element-containing mRNA database reveals an unexpectedly diverse functional repertoire of encoded proteins, Nucleic Acids Res. 29 (2001) 246-254. (Pubitemid 32054460)
47. A.B. Shyu, J.G. Belasco, M.E. Greenberg, Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay, Genes Dev. 5 (1991) 221-231. (Pubitemid 21905947)
48. N. Xu, C.Y. Chen, A.B. Shyu, Modulation of the fate of cytoplasmic mRNA by AUrich elements: key sequence features controlling mRNA deadenylation and decay, Mol. Cell. Biol. 17 (1997) 4611-4621. (Pubitemid 27318137)
49. M. Gao, C.J. Wilusz, S.W. Peltz, J. Wilusz, A novel mRNA-decapping activity in HeLa cytoplasmic extracts is regulated by AU-rich elements, EMBO J. 20 (2001) 1134-1143. (Pubitemid 32186803)
50. E.M. Hollams, K.M. Giles, A.M. Thomson, P.J. Leedman, MRNA stability and the control of gene expression: implications for human disease, Neurochem. Res. 27 (2002) 957-980. (Pubitemid 35316096)
51. W. Zhang, B.J. Wagner, K. Ehrenman, A.W. Schaefer, C.T. DeMaria, D. Crater, K. DeHaven, L. Long, G. Brewer, Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1, Mol. Cell. Biol. 13 (1993) 7652-7665. (Pubitemid 23354290)
52. C.M. Brennan, J.A. Steitz, HuR and mRNA stability, Cell. Mol. Life Sci. 58 (2001) 266-277. (Pubitemid 32217358)
53. R. Gherzi, K.Y. Lee, P. Briata, D. Wegmuller, C. Moroni, M. Karin, C.Y. Chen, A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery, Mol. Cell 14 (2004) 571-583. (Pubitemid 38739081)
54. G. Stoecklin, X.F. Ming, R. Looser, C. Moroni, Somatic mRNA turnover mutants implicate tristetraprolin in the interleukin-3 mRNA degradation pathway, Mol. Cell. Biol. 20 (2000) 3753-3763. (Pubitemid 30314475)
55. H.A. Meijer, A.A. Thomas, Control of eukaryotic protein synthesis by upstream open reading frames in the 50-untranslated region of an mRNA, Biochem. J. 367 (2002) 1-11. (Pubitemid 35176885)
56. M. Schmid, T.H. Jensen, The exosome: a multipurpose RNA-decay machine, Trends Biochem. Sci. 33 (2008) 501-510.
57. T.M. Franks, J. Lykke-Andersen, The control of mRNA decapping and P-body formation, Mol. Cell 32 (2008) 605-615.
58. M. Brook, L. McCracken, J.P. Reddington, Z.L. Lu, N.A. Morrice, N.K. Gray, The multifunctional poly(A)-binding protein (PABP) 1 is subject to extensive dynamic post-translational modification, which molecular modelling suggests plays an important role in co-ordinating its activities, Biochem. J. 441 (2012) 803-812.