RrmA regulates the stability of specific transcripts in response to both nitrogen source and oxidative stress

Molecular Microbiology

Volumn 89, Issue 5, 2013, Pages 975-988

  Krol, Kinga ^a,e   Morozov, Igor Y ^b,e   Jones, Meriel G ^b   Wyszomirski, Tomasz ^d   Weglenski, Piotr ^a,c   Dzikowska, Agnieszka ^a,c   Caddick, Mark X ^b  

^a UNIVERSITY OF WARSAW   (Poland)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^d UNIVERSITY OF WARSAW   (Poland)

^e Faculty of Engineering and Computing   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AREA MRNA BINDING PROTEIN; ARGININE; DEOXYHYPUSINE SYNTHASE; GLUTAMINE; HYPUSINE; LYSINE; MESSENGER RNA; NITROGEN; RNA BINDING PROTEIN; RRMA PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; ASPERGILLUS NIDULANS; CELLULAR DISTRIBUTION; DHSA GENE; EIF5A GENE; EIFE GENE; FUNGAL GENE; GENE EXPRESSION; GENETIC CODE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN MODIFICATION; REGULATORY RNA SEQUENCE; RNA ISOLATION; RNA STABILITY; RNA TRANSCRIPTION; RNA TRANSLATION; RRMA GENE; SIGNAL TRANSDUCTION;

EMERICELLA NIDULANS;

ARGININE; ASPERGILLUS NIDULANS; GENE DELETION; GENE EXPRESSION REGULATION; GLUTAMINE; NITROGEN; OXIDATIVE STRESS; RNA STABILITY; RNA-BINDING PROTEINS;

EID: 84883189658     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12324     Document Type: Article

References (58)

1. Asano, Y., Hagiwara, D., Yamashino, T., and Mizuno, T. (2007) Characterization of the bZip-type transcription factor NapA with reference to oxidative stress response in Aspergillus nidulans. Biosci Biotechnol Biochem 71: 1800-1803.
2. Baker, C.S., Morozov, I., Suzuki, K., Romeo, T., and Babitzke, P. (2002) CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli. Mol Microbiol 44: 1599-1610.
3. Beelman, C.A., and Parker, R. (1994) Differential effects of translational inhibition in cis and in trans on the decay of the unstable yeast MFA2 mRNA. J Biol Chem 269: 9687-9692.
4. Bevilacqua, A., Ceriani, M.C., Capaccioli, S., and Nicolin, A. (2003) Post-transcriptional regulation of gene expression by degradation of messenger RNAs. J Cell Physiol 195: 356-372.
5. Borsuk, P., Przykorska, A., Blachnio, K., Koper, M., Pawlowicz, J.M., Pekala, M., and Weglenski, P. (2007) L-arginine influences the structure and function of arginase mRNA in Aspergillus nidulans. Biol Chem 388: 135-144.
6. Caddick, M.X., Dobson, C., Morozov, I.Y., and Jones, M.G. (2006a) Gene regulation in Aspergillus: from genetics to genomics. Med Mycol 44: S13-S16.
7. Caddick, M.X., Jones, M.G., van Tonder, J.M., Le Cordier, H., Narendja, F., Strauss, J., and Morozov, I.Y. (2006b) Opposing signals differentially regulate transcript stability in Aspergillus nidulans. Mol Microbiol 62: 509-519.
8. Castello, A., Fischer, B., Eichelbaum, K., Horos, R., Beckmann, B.M., Strein, C., etal. (2012) Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 149: 1393-1406.
9. Clutterbuck, A.J. (1974) Aspergillus Nidulans. New York: Plenum Press.
10. Clutterbuck, A.J. (1993) Aspergillus Nidulans. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
11. Conlon, H., Zadra, I., Haas, H., Arst, H.N., Jr, Jones, M.G., and Caddick, M.X. (2001) The Aspergillus nidulans GATA transcription factor gene areB encodes at least three proteins and features three classes of mutation. Mol Microbiol 40: 361-375.
12. Cove, D.J. (1966) The induction and repression of nitrate reductase in the fungus Aspergillus nidulans. Biochim Biophys Acta 113: 51-56.
13. Empel, J., Sitkiewicz, I., Andrukiewicz, A., Lasocki, K., Borsuk, P., and Weglenski, P. (2001) arcA, the regulatory gene for the arginine catabolic pathway in Aspergillus nidulans. Mol Genet Genomics 266: 591-597.
14. Goldstrohm, A.C., Hook, B.A., Seay, D.J., and Wickens, M. (2006) PUF proteins bind Pop2p to regulate messenger RNAs. Nat Struct Mol Biol 13: 533-539.
15. Ha, H.C., Sirisoma, N.S., Kuppusamy, P., Zweier, J.L., Woster, P.M., and Casero, R.A., Jr. (1998) The natural polyamine spermine functions directly as a free radical scavenger. Proc Natl Acad Sci USA 95: 11140-11145.
16. Hagiwara, D., Asano, Y., Marui, J., Furukawa, K., Kanamaru, K., Kato, M., etal. (2007) The SskA and SrrA response regulators are implicated in oxidative stress responses of hyphae and asexual spores in the phosphorelay signaling network of Aspergillus nidulans. Biosci Biotechnol Biochem 71: 1003-1014.
17. Hagiwara, D., Asano, Y., Yamashino, T., and Mizuno, T. (2008) Characterization of bZip-type transcription factor AtfA with reference to stress responses of conidia of Aspergillus nidulans. Biosci Biotechnol Biochem 72: 2756-2760.
18. Henderson, A., and Hershey, J.W. (2011) The role of eIF5A in protein synthesis. Cell Cycle 10: 3617-3618.
19. Heukeshoven, J., and Dernick, R. (1988) Improved silver staining procedure for fast staining in PhastSystem Development Unit. I. Staining of sodium dodecyl sulfate gels. Electrophoresis 9: 28-32.
20. Hook, B.A., Goldstrohm, A.C., Seay, D.J., and Wickens, M. (2007) Two yeast PUF proteins negatively regulate a single mRNA. J Biol Chem 282: 15430-15438.
21. Hoshino, S. (2012) Mechanism of the initiation of mRNA decay: role of eRF3 family G proteins. Wiley Interdiscip Rev RNA 3: 743-757.
22. Igarashi, K., and Kashiwagi, K. (2000) Polyamines: mysterious modulators of cellular functions. Biochem Biophys Res Commun 271: 559-564.
23. Iwai, Y., Akahane, K., Pluznik, D.H., and Cohen, R.B. (1993) Ca2+ ionophore A23187-dependent stabilization of granulocyte-macrophage colony-stimulating factor messenger RNA in murine thymoma EL-4 cells is mediated through two distinct regions in the 3′-untranslated region. J Immunol 150: 4386-4394.
24. Kadyrova, L.Y., Habara, Y., Lee, T.H., and Wharton, R.P. (2007) Translational control of maternal Cyclin B mRNA by Nanos in the Drosophila germline. Development 134: 1519-1527.
25. Kaiser, A. (2012) Translational control of eIF5A in various diseases. Amino Acids 42: 679-684.
26. Kang, H.A., and Hershey, J.W. (1994) Effect of initiation factor eIF-5A depletion on protein synthesis and proliferation of Saccharomyces cerevisiae. J Biol Chem 269: 3934-3940.
27. Li, C.H., Ohn, T., Ivanov, P., Tisdale, S., and Anderson, P. (2010) eIF5A promotes translation elongation, polysome disassembly and stress granule assembly. PLoS ONE 5: e9942.
28. Macios, M., Caddick, M.X., Weglenski, P., Scazzocchio, C., and Dzikowska, A. (2012) The GATA factors AREA and AREB together with the co-repressor NMRA, negatively regulate arginine catabolism in Aspergillus nidulans in response to nitrogen and carbon source. Fungal Genet Biol 49: 189-198.
29. Martin, V., Rodriguez-Gabriel, M.A., McDonald, W.H., Watt, S., Yates, J.R. , Bahler, J., and Russell, P. (2006) Cip1 and Cip2 are novel RNA-recognition-motif proteins that counteract Csx1 function during oxidative stress. Mol Cell Biol 17: 1176-1183.
30. Matia-Gonzalez, A.M., Sotelo, J., and Rodriguez-Gabriel, M.A. (2012) The RNA binding protein Csx1 promotes sexual differentiation in Schizosaccharomyces pombe. PLoS ONE 7: e30067.
31. May, G.S., and Morris, N.R. (1988) Developmental regulation of a conidiation specific beta-tubulin in Aspergillus nidulans. Dev Biol 128: 406-414.
32. Morozov, I.Y., Martinez, M.G., Jones, M.G., and Caddick, M.X. (2000) A defined sequence within the 3′ UTR of the areA transcript is sufficient to mediate nitrogen metabolite signalling via accelerated deadenylation. Mol Microbiol 37: 1248-1257.
33. Morozov, I.Y., Galbis-Martinez, M., Jones, M.G., and Caddick, M.X. (2001) Characterization of nitrogen metabolite signalling in Aspergillus via the regulated degradation of areA mRNA. Mol Microbiol 42: 269-277.
34. Morozov, I.Y., Jones, M.G., Razak, A.A., Rigden, D.J., and Caddick, M.X. (2010a) CUCU modification of mRNA promotes decapping and transcript degradation in Aspergillus nidulans. Mol Cell Biol 30: 460-469.
35. Morozov, I.Y., Jones, M.G., Spiller, D.G., Rigden, D.J., Dattenbock, C., Novotny, R., etal. (2010b) Distinct roles for Caf1, Ccr4, Edc3 and CutA in the co-ordination of transcript deadenylation, decapping and P-body formation in Aspergillus nidulans. Mol Microbiol 76: 503-516.
36. Morozov, I.Y., Jones, M.G., Gould, P.D., Crome, V., Wilson, J.B., Hall, A.J., etal. (2012) mRNA 3′ tagging is induced by nonsense-mediated decay and promotes ribosome dissociation. Mol Cell Biol 32: 2585-2595.
37. Nishimura, A., Kotani, T., Sasano, Y., and Takagi, H. (2010) An antioxidative mechanism mediated by the yeast N-acetyltransferase Mpr1: oxidative stress-induced arginine synthesis and its physiological role. FEMS Yeast Res 10: 687-698.
38. Ohn, T., and Anderson, P. (2010) The role of posttranslational modifications in the assembly of stress granules. Wiley Interdiscip Rev RNA 1: 486-493.
39. Olszewska, A., Krol, K., Weglenski, P., and Dzikowska, A. (2007) Arginine catabolism in Aspergillus nidulans is regulated by the rrmA gene coding for the RNA-binding protein. Fungal Genet Biol 44: 1285-1297.
40. Park, M.H. (2006) The post-translational synthesis of a polyamine-derived amino acid, hypusine, in the eukaryotic translation initiation factor 5A (eIF5A). J Biochem 139: 161-169.
41. Parker, R., and Song, H. (2004) The enzymes and control of eukaryotic mRNA turnover. Nat Struct Mol Biol 11: 121-127.
42. Platt, A., Langdon, T., Arst, H.N., Jr, Kirk, D., Tollervey, D., Sanchez, J.M., and Caddick, M.X. (1996) Nitrogen metabolite signalling involves the C-terminus and the GATA domain of the Aspergillus transcription factor AREA and the 3′ untranslated region of its mRNA. EMBO J 15: 2791-2801.
43. Puig, S., Askeland, E., and Thiele, D.J. (2005) Coordinated remodeling of cellular metabolism during iron deficiency through targeted mRNA degradation. Cell 120: 99-110.
44. Rider, J.E., Hacker, A., Mackintosh, C.A., Pegg, A.E., Woster, P.M., and Casero, R.A., Jr. (2007) Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide. Amino Acids 33: 231-240.
45. Rodriguez-Gabriel, M.A., Burns, G., McDonald, W.H., Martin, V., Bahler, J.R., Yates, , J., and Russell, P. (2003) RNA-binding protein Csx1 mediates global control of gene expression in response to oxidative stress. EMBO J 22: 6256-6266.
46. Sachs, A.B., Sarnow, P., and Hentze, M.W. (1997) Starting at the beginning, middle, and end: translation initiation in eukaryotes. Cell 89: 831-838.
47. Saini, P., Eyler, D.E., Green, R., and Dever, T.E. (2009) Hypusine-containing protein eIF5A promotes translation elongation. Nature 459: 118-121.
48. SAS Institute Inc. (2010) SAS/STAT® 9.22 User's Guide. Cary, NC: SAS Institute Inc.
49. Schrader, R., Young, C., Kozian, D., Hoffmann, R., and Lottspeich, F. (2006) Temperature-sensitive eIF5A mutant accumulates transcripts targeted to the nonsense-mediated decay pathway. J Biol Chem 281: 35336-35346.
50. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858.
51. Shi, H., Ye, T., Chen, F., Cheng, Z., Wang, Y., Yang, P., etal. (2013) Manipulation of arginase expression modulates abiotic stress tolerance in Arabidopsis: effect on arginine metabolism and ROS accumulation. J Exp Bot 64: 1367-1379.
52. Shim, J., and Karin, M. (2002) The control of mRNA stability in response to extracellular stimuli. Mol Cells 14: 323-331.
53. Stoecklin, G., Hahn, S., and Moroni, C. (1994) Functional hierarchy of AUUUA motifs in mediating rapid interleukin-3 mRNA decay. J Biol Chem 269: 28591-28597.
54. Szewczyk, E., Nayak, T., Oakley, C.E., Edgerton, H., Xiong, Y., Taheri-Talesh, N., etal. (2006) Fusion PCR and gene targeting in Aspergillus nidulans. Nat Protoc 1: 3111-3120.
55. Tucker, M., Valencia-Sanchez, M.A., Staples, R.R., Chen, J., Denis, C.L., and Parker, R. (2001) The transcription factor associated Ccr4 and Caf1 proteins are components of the major cytoplasmic mRNA deadenylase in Saccharomyces cerevisiae. Cell 104: 377-386.
56. Wang, L., Xu, C., Wang, C., and Wang, Y. (2012) Characterization of a eukaryotic translation initiation factor 5A homolog from Tamarix androssowii involved in plant abiotic stress tolerance. BMC Plant Biol 12: 118.
57. Wang, Y., Liu, C.L., Storey, J.D., Tibshirani, R.J., Herschlag, D., and Brown, P.O. (2002) Precision and functional specificity in mRNA decay. Proc Natl Acad Sci USA 99: 5860-5865.
58. Yang, E., van Nimwegen, E., Zavolan, M., Rajewsky, N., Schroeder, M., Magnasco, M., and Darnell, J.E., Jr. (2003) Decay rates of human mRNAs: correlation with functional characteristics and sequence attributes. Genome Res 13: 1863-1872.