Analysis of nitric oxide-stabilized mRNAs in human fibroblasts reveals HuR-dependent heme oxygenase 1 upregulation

Molecular and Cellular Biology

Volumn 29, Issue 10, 2009, Pages 2622-2635

  Kuwano, Yuki ^a   Rabinovic, Ariel ^b   Srikantan, Subramanya ^a   Gorospe, Myriam ^a   Demple, Bruce ^b  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DACTINOMYCIN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; HEME OXYGENASE 1; HUR PROTEIN; INHIBITOR OF DIFFERENTIATION 3; MESSENGER RNA; NITRIC OXIDE; RGS2 PROTEIN; ELAV-LIKE PROTEIN 1; MEMBRANE ANTIGEN; RNA BINDING PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL STRAIN 3T3; CHIC2 GENE; CONTROLLED STUDY; CYTOPLASM; FIBROBLAST; GENE; GENETIC STABILITY; HO 1 GENE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; LUNG FIBROBLAST; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PTGS2 GENE; RNA TRANSLATION; TIEG GENE; UPREGULATION; WESTERN BLOTTING; ANIMAL; CELL LINE; CYTOLOGY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; RNA STABILITY;

ANIMALS; ANTIGENS, SURFACE; BASE SEQUENCE; CELL LINE; FIBROBLASTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEME OXYGENASE-1; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NITRIC OXIDE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS; UP-REGULATION;

EID: 66349115397     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01495-08     Document Type: Article

References (60)

1. Abdelmohsen, K., Y. Kuwano, H. H. Kim, and M. Gorospe. 2008. Posttranscriptional gene regulation by RNA-binding proteins during oxidative stress: implications for cellular senescence. Biol. Chem. 389:243-255.
2. Abdelmohsen, K., R. Pullmann, Jr., A. Lal, H. H. Kim, S. Galban, X. Yang, J. D. Blethrow, M. Walker, J. Shubert, D. A. Gillespie, H. Furneaux, and M. Gorospe. 2007. Phosphorylation of HuR by Chk2 regulates SIRT1 expression. Mol. Cell 25:543-557.
3. Abler, M. L., and P. J. Green. 1996. Control of mRNA stability in higher plants. Plant Mol. Biol. 32:63-78.
4. Arenillas, A., F. Rubiera, and J. J. Pis. 2002. Nitric oxide reduction in coal combustion: role of char surface complexes in heterogeneous reactions. Environ. Sci. Technol. 36:5498-5503.
5. Beelman, C. A., and R. Parker. 1995. Degradation of mRNA in eukaryotes. Cell 81:179-183.
6. Bentz, B. G., R. L. Simmons, G. K. Haines III, and J. A. Radosevich. 2000. The yin and yang of nitric oxide: reflections on the physiology and pathophysiology of NO. Head Neck 22:71-83.
7. Boje, K. M. 2004. Nitric oxide neurotoxicity in neurodegenerative diseases. Front. Biosci. 9:763-776.
8. Bouton, C., and B. Demple. 2000. Nitric oxide-inducible expression of heme oxygenase-1 in human cells. Translation-independent stabilization of the mRNA and evidence for direct action of nitric oxide. J. Biol. Chem. 275: 32688-32693.
9. Brennan, C. M., and J. A. Steitz. 2001. HuR and mRNA stability. Cell. Mol. Life Sci. 58:266-277.
10. Chen, K., and M. D. Maines. 2000. Nitric oxide induces heme oxygenase-1 via mitogen-activated protein kinases ERK and p38. Cell. Mol. Biol. (Noisy-le-Grand) 46:609-617.
11. Chen, C. Y., and A. B. Shyu. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20:465-470.
12. Davis, K. L., E. Martin, I. V. Turko, and F. Murad. 2001. Novel effects of nitric oxide. Annu. Rev. Pharmacol. Toxicol. 41:203-236.
13. Dixon, D. A., N. D. Tolley, P. H. King, L. B. Nabors, T. M. McIntyre, G. A. Zimmerman, and S. M. Prescott. 2001. Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J. Clin. Investig. 108:1657-1665.
14. Doller, A., A. Huwiler, R. Müller, H. H. Radeke, J. Pfeilschifter, and W. Eberhardt. 2007. Protein kinase C alpha-dependent phosphorylation of the mRNA-stabilizing factor HuR: implications for posttranscriptional regulation of cyclooxygenase-2. Mol. Biol. Cell 18:2137-2148.
15. Ehretsmann, C. P., A. J. Carpousis, and H. M. Krisch. 1992. mRNA degradation in procaryotes. FASEB J. 6:3186-3192.
16. Faour, W. H., A. Mancini, Q. W. He, and J. A. Di Battista. 2003. T-cell-derived interleukin-17 regulates the level and stability of cyclooxygenase-2 (COX-2) mRNA through restricted activation of the p38 mitogen-activated protein kinase cascade: role of distal sequences in the 3′-untranslated region of COX-2 mRNA. J. Biol. Chem. 278:26897- 26907.
17. Galbán, S., Y. Kuwano, R. Pullmann, Jr., J. L. Martindale, H. H. Kim, A. Lal, K. Abdelmohsen, X. Yang, Y. Dang, J. O. Liu, S. M. Lewis, M. Holcik, and M. Gorospe. 2008. RNA-binding proteins HuR and PTB promote the translation of hypoxia-inducible factor 1α. Mol. Cell. Biol. 28:93-107.
18. Guhaniyogi, J., and G. Brewer. 2001. Regulation of mRNA stability in mammalian cells. Gene 265:11-23.
19. Ignarro, L. J. 1996. Physiology and pathophysiology of nitric oxide. Kidney Int. Suppl. 55:S2-S5.
20. Ignarro, L. J., G. Cirino, A. Casini, and C. Napoli. 1999. Nitric oxide as a signaling molecule in the vascular system: an overview. J. Cardiovasc. Pharmacol. 34:879-886.
21. Im, H., F. Rasouli, and M. Hajaligol. 2003. Formation of nitric oxide during tobacco oxidation. J. Agric. Food Chem. 51:7366-7372.
22. Jackman, J., I. Alamo, Jr., and A. J. Fornace, Jr. 1994. Genotoxic stress confers preferential and coordinate messenger RNA stability on the five gadd genes. Cancer Res. 54:5656-5662.
23. Keene, J. D. 2007. RNA regulons: coordination of post-transcriptional events. Nat. Rev. Genet. 8:533-543.
24. Kim, H. H., K. Abdelmohsen, A. Lal, R. Pullmann, Jr., X. Yang, S. Galban, S. Srikantan, J. L. Martindale, J. Blethrow, K. M. Shokat, and M. Gorospe. 2008. Nuclear HuR accumulation through phosphorylation by Cdk1. Genes Dev. 22:1804-1815.
25. Kimura, H., A. Weisz, Y. Kurashima, K. Hashimoto, T. Ogura, F. D'Acquisto, R. Addeo, M. Makuuchi, and H. Esumi. 2000. Hypoxia response element of the human vascular endothelial growth factor gene mediates transcriptional regulation by nitric oxide: control of hypoxia-inducible factor-1 activity by nitric oxide. Blood 95:189-197.
26. Kuwano, Y., H. H. Kim, K. Abdelmohsen, R. Pullmann, Jr., J. L. Martindale, X. Yang, and Gorospe, M. 2008. MKP-1 mRNA stabilization and translational control by RNA-binding proteins HuR and NF90. Mol. Cell. Biol. 28:4562-4575.
27. Lal, A., K. Mazan-Mamczarz, T. Kawai, X. Yang, J. L. Martindale, and M. Gorospe. 2004. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J. 23:3092-3102.
28. Lal, A., T. Kawai, X. Yang, K. Mazan-Mamczarz, and M. Gorospe. 2005. Antiapoptotic function of RNA-binding protein HuR effected through prothymosin alpha. EMBO J. 24:1852-1862.
29. Lal, A., K. Abdelmohsen, R. Pullmann, Jr., T. Kawai, S. Galban, X. Yang, G. Brewer, and M. Gorospe. 2006. Posttranscriptional derepression of GADD45alpha by genotoxic stress. Mol. Cell 22:117-128.
30. Lander, H. M., J. M. Tauras, J. S. Ogiste, O. Hori, R. A. Moss, and A. M. Schmidt. 1997. Activation of the receptor for advanced glycation end products triggers a p21(ras)-dependent mitogen-activated protein kinase pathway regulated by oxidant stress. J. Biol. Chem. 272:17810-17814.
31. Lander, H. M., D. P. Hajjar, B. L. Hempstead, U. A. Mirza, B. T. Chait, S. Campbell, and L. A. Quilliam. 1997. A molecular redox switch on p21(ras). Structural basis for the nitric oxide-p21(ras) interaction. J. Biol. Chem. 272:4323-4326.
32. Leautaud, V., and B. Demple. 2007. Regulation of heme oxygenase-1 mRNA deadenylation and turnover in NIH3T3 cells by nitrosative or alkylation stress. BMC Mol. Biol. 8:116.
33. López de Silanes, I., M. Zhan, A. Lal, X. Yang, and M. Gorospe. 2004. Identification of a target RNA motif for RNA-binding protein HuR. Proc. Natl. Acad. Sci. USA 101:2987-2992.
34. Marquis, J. C., and B. Demple. 1998. Complex genetic response of human cells to sublethal levels of pure nitric oxide. Cancer Res. 58:3435-3440.
35. Mazan-Mamczarz, K., S. Galbán, I. López de Silanes, J. L. Martindale, U. Atasoy, J. D. Keene, and M. Gorospe. 2003. RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc. Natl. Acad. Sci. USA 100:8354-8359.
36. McMahon, T. J., R. E. Moon, B. P. Luschinger, M. S. Carraway, A. E. Stone, B. W. Stolp, A. J. Gow, J. R. Pawloski, P. Watke, D. J. Singel, C. A. Piantadosi, and J. S. Stamler. 2002. Nitric oxide in the human respiratory cycle. Nat. Med. 8:711-717.
37. Mitchell, P., and D. Tollervey. 2000. mRNA stability in eukaryotes. Curr. Opin. Genet. Dev. 10:193-198.
38. Mitsumoto, M., A. Mitsumoto, and B. Demple. 2003. Nitric oxide-mediated upregulation of the TGF-beta-inducible early response gene-1 (TIEG1) in human fibroblasts by mRNA stabilization independent of TGF-beta. Free Radic. Biol. Med. 34:1607-1613.
39. Moncada, S. 2000. Nitric oxide and cell respiration: physiology and pathology. Verh. K. Acad. Geneeskd. Belg. 62:171-179, 179-181.
40. Pilz, R. B., M. Suhasini, S. Idriss, J. L. Meinkoth, and G. R. Boss. 1995. Nitric oxide and cGMP analogs activate transcription from AP-1-responsive promoters in mammalian cells. FASEB J. 9:552-558.
41. Ptasinska, A., S. Wang, J. Zhang, R. A. Wesley, and R. L. Danner. 2007. Nitric oxide activation of peroxisome proliferator-activated receptor through a p38 MAPK signaling pathway. FASEB J. 21:950-961.
42. Ross, J. 1995. mRNA stability in mammalian cells. Microbiol. Rev. 59:423-450.
43. Schuman, E. M., and D. V. Madison. 1991. A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 254:1503-1506.
44. Schwarzbach, E. 1971. Formation of ozone and nitric oxide caused by welding. Zentralbl. Arbeitsmed. 21:290-292.
45. Spiecker, M., H. B. Peng, and J. K. Liao. 1997. Inhibition of endothelial vascular cell adhesion molecule-1 expression by nitric oxide involves the induction and nuclear translocation of I B. J. Biol. Chem. 272:30969-30974.
46. Theil, E. C. 1993. The IRE (iron regulatory element) family: structures which regulate mRNA translation or stability. Biofactors 4:87-93.
47. Thomson, A. M., J. T. Rogers, and P. J. Leedman. 1999. Iron-regulatory proteins, iron-responsive elements and ferritin mRNA translation. Int. J. Biochem. Cell Biol. 31:1139-1152.
48. Tieu, K., H. Ischiropoulos, and S. Przedborski. 2003. Nitric oxide and reactive oxygen species in Parkinson's disease. IUBMB Life 55:329-335.
49. Tourriere, H., K. Chebli, and J. Tazi. 2002. mRNA degradation machines in eukaryotic cells. Biochimie 84:821-837.
50. Valencia-Sanchez, M. A., J. Liu, G. J. Hannon, and R. Parker. 2006. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 20:515-524.
51. Vlasova, I. A., N. M. Tahoe, D. Fan, O. Larsson, B. Rattenbacher, J. R. Sternjohn, J. Vasdewani, G. Karypis, C. S. Reilly, P. B. Bitterman, and P. R. Bohjanen. 2008. Conserved GU-rich elements mediate mRNA decay by binding to CUG-binding protein 1. Mol. Cell 29:263-270.
52. Wang, S., J. Zhang, Y. Zhang, S. Kern, and R. L. Danner. 2008. AU-rich element-dependent and -independent mechanisms. Nitric oxide-p38 MAPK signaling stabilizes mRNA through AU-rich element-dependent and -independent mechanisms. J. Leukoc. Biol. 83:982-990.
53. Wang, S., W. Wang, R. A. Wesley, and R. L. Danner. 1999. A Sp1 binding site of the tumor necrosis factor promoter functions as a nitric oxide response element. J. Biol. Chem. 274:33190-33193.
54. Wang, W., H. Furneaux, H. Cheng, M. C. Caldwell, D. Hutter, Y. Liu, N. J. Holbrook, and M. Gorospe. 2000. HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol. 20:760-769.
55. Wilks, A. 2002. Heme oxygenase: evolution, structure, and mechanism. Antioxid. Redox Signal. 4:603-614.
56. Wilusz, C. J., M. Wormington, and S. W. Peltz. 2001. The cap-to-tail guide to mRNA turnover. Nat. Rev. Mol. Cell Biol. 2:237-246.
57. Wink, D. A., Y. Vodovotz, J. Laval, F. Laval, M. W. Dewhirst, and J. B. Mitchell. 1998. The multifaceted roles of nitric oxide in cancer. Carcinogenesis 19:711-721.
58. Xu, W., L. Z. Liu, M. Loizidou, M. Ahmed, and I. G. Charles. 2002. The role of nitric oxide in cancer. Cell Res. 12:311-320.
59. Yang, E., E. van Nimwegen, M. Zavolan, N. Rajewsky, M. Schroeder, M. Magnasco, and J. E. Darnell, Jr. 2003. Decay rates of human mRNAs: correlation with functional characteristics and sequence attributes. Genome Res. 13:1863-1872.
60. Zhang, J., S. Wang, R. A. Wesley, R. L. Danner. 2003. Adjacent sequence controls the response polarity of nitric oxide-sensitive Sp factor binding sites. J. Biol. Chem. 278:29192-29200.