Nuclear export of the transcription factor NirA is a regulatory checkpoint for nitrate induction in Aspergillus nidulans

Molecular and Cellular Biology

Volumn 27, Issue 3, 2007, Pages 791-802

  Bernreiter, Andreas ^a   Ramon, Ana ^b,e   Fernández Martínez, Javier ^c   Berger, Harald ^a   Araújo Bazan, Lidia ^c   Espeso, Eduardo A ^c   Pachlinger, Robert ^a   Gallmetzer, Andreas ^a   Anderl, Ingund ^a,f   Scazzocchio, Claudio ^b,d   Strauss, Joseph ^a  

^a AIT AUSTRIAN INSTITUTE OF TECHNOLOGY   (Austria)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^d INSTITUT UNIVERSITAIRE DE FRANCE   (France)

^e UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^f GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; KARYOPHERIN; LEPTOMYCIN; LEUCINE; NITRATE; NUCLEOPORIN; PROTEIN KAPK; PROTEIN NPLA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AREA; TRANSCRIPTION FACTOR NIRA; UNCLASSIFIED DRUG;

ARTICLE; ASPERGILLUS NIDULANS; CELL NUCLEUS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DNA BINDING; GENE ACTIVITY; GENE EXPRESSION; GENE MUTATION; IN VIVO STUDY; NIRA GENE; NITRATE METABOLISM; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEOCYTOPLASMIC TRANSPORT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; TRANSCRIPTION INITIATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ASPERGILLUS NIDULANS; BINDING SITES; CELL NUCLEUS; FATTY ACIDS, UNSATURATED; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; KARYOPHERINS; MUTATION; NITRATES; NUCLEAR EXPORT SIGNALS; NUCLEAR PORE COMPLEX PROTEINS; PHENOTYPE; PROTEIN BINDING; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; SEQUENCE HOMOLOGY; TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES;

EMERICELLA NIDULANS;

EID: 33846606876     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00761-06     Document Type: Article

References (68)

1. Adachi, Y., and M. Yanagida. 1989. Higher order chromosome structure is affected by cold-sensitive mutations in a Schizosaccharomyces pombe gene crm1+ which encodes a 115-kDa protein preferentially localized in the nucleus and its periphery. J. Cell Biol. 108:1195-1207.
2. Andrianopoulos, A., S. Kourambas, J. A. Sharp, M. A. Davis, and M. J. Hynes. 1998. Characterization of the Aspergillus nidulans nmrA gene involved in nitrogen metabolite repression. J. Bacteriol. 180:1973-1977.
3. Arst, H. N., Jr., and D. J. Cove. 1973. Nitrogen metabolite repression in Aspergillus nidulans. Mol. Gen. Genet. 126:111-141.
4. Axelrod, J. D., J. Majors, and M. C. Brandriss. 1991. Proline-independent binding of PUT3 transcriptional activator protein detected by footprinting in vivo. Mol. Cell. Biol. 11:564-567.
5. Berger, H., R. Pachlinger, I. Morozov, S. Goller, F. Narendja, M. Caddick, and J. Strauss. 2006. The GATA factor AreA regulates localization and in vivo binding site occupancy of the nitrate activator NirA. Mol. Microbiol. 59:433-446.
6. Bogerd, H. P., R. A. Fridell, S. Madore, and B. R. Cullen. 1995. Identification of a novel cellular cofactor for the Rev/Rex class of retroviral regulatory proteins. Cell 82:485-494.
7. Brisco, P. R., and G. B. Kohlhaw. 1990. Regulation of yeast LEU2: total deletion of regulatory gene LEU3 unmasks GCN4-dependent basal level expression of LEU2. J. Biol. Chem. 265:11667-11675.
8. Burger, G., J. Strauss, C. Scazzocchio, and B. F. Lang. 1991. nirA, the pathway-specific regulatory gene of nitrate assimilation in Aspergillus nidulans, encodes a putative GAL4-type zinc finger protein and contains four introns in highly conserved regions. Mol. Cell. Biol. 11:5746-5755.
9. Clutterbuck, A. J., and H. Arst. 1995. Genetic nomenclature guide. Aspergillus nidulans. Trends Genet.:13-14.
10. Cove, D. J. 1979. Genetic studies of nitrate assimilation in Aspergillus nidulans. Biol. Rev. Camb. Philos. Soc. 54:291-327.
11. Daboussi, M. J., T. Langin, F. Deschamps, Y. Brygoo, C. Scazzocchio, and G. Burger. 1991. Heterologous expression of the Aspergillus nidulans regulatory gene nirA in Fusarium oxysporum. Gene 109:155-160.
12. Delaunay. A., A. D. Isnard, and M. B. Toledano. 2000. H2O2 sensing through oxidation of the Yap1 transcription factor. EMBO J. 19:5157-5166.
13. De Souza, C. P., A. H. Osmani, S. B. Hashmi, and S. A. Osmani. 2004. Partial nuclear pore complex disassembly during closed mitosis in Aspergillus nidulans. Curr. Biol. 14:1973-1984.
14. Dominguez, D., B. Montserrat-Sentis, A. Virgos-Soler, S. Guaita, J. Grueso, M. Porta, I. Puig, J. Baulida, C. Franci, and A. Garcia de Herreros. 2003. Phosphorylation regulates the subcellular location and activity of the snail transcriptional repressor. Mol. Cell. Biol. 23:5078-5089.
15. Farjot, G., A. Sergeant, and I. Mikaelian. 1999. A new nucleoporin-like protein interacts with both HIV-1 Rev nuclear export signal and CRM-1. J. Biol. Chem. 274:17309-17317.
16. Feng, B., and G. A. Marzluf. 1998. Interaction between major nitrogen regulatory protein N1T2 and pathway-specific regulatory factor NIT4 is required for their synergistic activation of gene expression in Neurospora crassa. Mol. Cell. Biol. 18:3983-3990.
17. Floer, M., and G. Blobel. 1999. Putative reaction intermediates in Crm1-mediated nuclear protein export. J. Biol. Chem. 274:16279-16286.
18. Fornerod, M., M. Ohno, M. Yoshida, and I. W. Mattaj. 1997. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90:1051-1060.
19. Fritz, C. C., M. L. Zapp, and M. R. Green. 1995. A human nucleoporin-like protein that specifically interacts with HIV Rev. Nature 376:530-533.
20. Gietz, R. D., B. Triggs-Raine, A. Robbins, K. C. Graham, and R. A. Woods. 1997. Identification of proteins that interact with a protein of interest: applications of the yeast two-hybrid system. Mol. Cell. Biochem. 172:67-79.
21. Gomez, D., B. Cubero, G. Cecchetto, and C. Scazzocchio. 2002. PrnA, a Zn2Cys6 activator with a unique DNA recognition mode, requires inducer for in vivo binding. Mol. Microbiol. 44:585-597.
22. Guan, T., R. H. Kehlenbach, E. C. Schirmer, A. Kehlenbach, F. Fan, B. E. Clurman, N. Arnheim, and L. Gerace. 2000. Nup50, a nucleoplasmically oriented nucleoporin with a role in nuclear protein export. Mol. Cell. Biol. 20:5619-5630.
23. Hon, T., A. Hach, H. C. Lee, T. Cheng, and L. Zhang. 2000. Functional analysis of heme regulatory elements of the transcriptional activator Hap1. Biochem. Biophys. Res. Commun. 273:584-591.
24. Hon, T., H. C. Lee, A. Hach, J. L. Johnson, E. A. Craig, H. Erdjument-Bromage, P. Tempst, and L. Zhang. 2001. The Hsp70-Ydj1 molecular chaperone represses the activity of the heme activator protein Hap1 in the absence of heme. Mol. Cell. Biol. 21:7923-7932.
25. Kip1 on serine 10 is required for its binding to CRM1 and nuclear export. J. Biol. Chem. 277:14355-14358.
26. Kudo, N., N. Matsumori, H. Taoka, D. Fujiwara, E. P. Schreiner, B. Wolff, M. Yoshida, and S. Horinouchi. 1999. Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc. Natl. Acad. Sci. USA 96:9112-9117.
27. Lee, H. C., T. Hon, and L. Zhang. 2002. The molecular chaperone Hsp90 mediates heme activation of the yeast transcriptional activator Hap1. J. Biol. Chem. 277:7430-7437.
28. Leuther, K. K., and S. A. Johnston. 1992. Nondissociation of GAL4 and GAL80 in vivo after galactose induction. Science 256:1333-1335.
29. Leuther, K. K., J. M. Salmeron, and S. A. Johnston. 1993. Genetic evidence that an activation domain of GAL4 does not require acidity and may form a beta sheet. Cell 72:575-585.
30. Malardier, L., M. J. Daboussi, J. Julien, F. Roussel, C. Scazzocchio, and Y. Brygoo. 1989. Cloning of the nitrate reductase gene (niaD) of Aspergillus nidulans and its use for transformation of Fusarium oxysporum. Gene 78:147-156.
31. Marzluf, G. A. 1997. Genetic regulation of nitrogen metabolism in the fungi. Microbiol. Mol. Biol. Rev. 61:17-32.
32. Morozov, I. Y., M. Galbis-Martinez, M. G. Jones, and M. X. Caddick. 2001. Characterization of nitrogen metabolite signalling in Aspergillus via the regulated degradation of areA mRNA. Mol. Microbiol. 42:269-277.
33. Muro-Pastor, M. I., R. Gonzalez, J. Strauss, F. Narendja, and C. Scazzocchio. 1999. The GATA factor AreA is essential for chromatin remodeling in a eukaryotic bidirectional promoter. EMBO J. 18:1584-1597. (Erratum, 18:2670.)
34. Muro-Pastor, M. I., J. Strauss, A. Ramon, and C. Scazzocchio. 2004. A paradoxical mutant GATA factor. Eukaryot. Cell 3:393-405.
35. Narendja, F., S. P. Goller, M. Wolschek, and J. Strauss. 2002. Nitrate and the GATA factor AreA are necessary for in vivo binding of NirA, the pathway-specific transcriptional activator of Aspergillus nidulans. Mol. Microbiol. 44:573-583.
36. Nayak, T., E. Szewczyk, C. E. Oakley, A. Osmani, L. Ukil, S. L. Murray, M. J. Hynes, S. A. Osmani, and B. R. Oakley. 2006. A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 172:1557-1566.
37. Neville, M., and M. Rosbash. 1999. The NES-Crm1p export pathway is not a major mRNA export route in Saccharomyces cerevisiae. EMBO J. 18:3746-3756.
38. Neville, M., F. Stutz, L. Lee, L. I. Davis, and M. Rosbash. 1997. The importin-beta family member Crm1p bridges the interaction between Rev. and the nuclear pore complex during nuclear export. Curr. Biol. 7:767-775.
39. Okamura, H., J. Aramburu, C. Garcia-Rodriguez, J. P. Viola, A. Raghavan, M. Tahiliani, X. Zhang, J. Qin, P. G. Hogan, and A. Rao. 2000. Concerted dephosphorylation of the transcription factor NFAT1 induces a conformational switch that regulates transcriptional activity. Mol. Cell 6:539-550.
40. Orlando, V., H. Strutt, and R. Paro. 1997. Analysis of chromatin structure by in vivo formaldehyde cross-linking. Methods 11:205-214.
41. Pachlinger, R., R. Mitterbauer, G. Adam, and J. Strauss. 2005. Metabolically independent and accurately adjustable Aspergillus sp. expression system. Appl. Environ. Microbiol. 71:672-678.
42. Pateman, J. A., and D. J. Cove. 1967. Regulation of nitrate reduction in Aspergillus nidulans. Nature 215:1234-1237.
43. Pemberton, L. F., and B. M. Paschal. 2005. Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 6:187-198.
44. Pokorska, A., C. Drevet, and C. Scazzocchio. 2000. The analysis of the transcriptional activator PrnA reveals a tripartite nuclear localization sequence. J. Mol. Biol. 298:585-596.
45. Punt, P. J., M. A. Dingemanse, A. Kuyvenhoven, R. D. Soede, P. H. Pouwels, and C. A. van den Hondel. 1990. Functional elements in the promoter region of the Aspergillus nidulans gpdA gene encoding glyceraldehyde-3-phosphate dehydrogenase. Gene 93:101-109.
46. Punt, P. J., J. Strauss, R. Smit, J. R. Kinghorn, C. A. van den Hondel, and C. Scazzocchio. 1995. The intergenic region between the divergently transcribed niiA and niaD genes of Aspergillus nidulans contains multiple NirA binding sites which act bidirectionally. Mol. Cell. Biol. 15:5688-5699.
47. Rand, K. N., and H. N. Arst, Jr. 1978. Mutations in nirA gene of Aspergillus nidulans and nitrogen metabolism. Nature 272:732-734.
48. Rose, M. D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
49. Ryan, K. J., and S. R. Wente. 2000. The nuclear pore complex: a protein machine bridging the nucleus and cytoplasm. Curr. Opin. Cell Biol. 12:361-371.
50. Scazzocchio, C. 2000. The fungal GATA factors. Curr. Opin. Microbiol. 3:126-131.
51. Selleck, S. B., and J. E. Majors. 1987. In vivo DNA-binding properties of a yeast transcription activator protein. Mol. Cell. Biol. 7:3260-3267.
52. Serebriiskii, I. G., and E. A. Golemis. 2001. Two-hybrid system and false positives: approaches to detection and elimination. Methods Mol. Biol. 177:123-134.
53. Stade, K., C. S. Ford, C. Guthrie, and K. Weis. 1997. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 90:1041-1050.
54. Stoffler, D., B. Fahrenkrog, and U. Aebi. 1999. The nuclear pore complex: from molecular architecture to functional dynamics. Curr. Opin. Cell Biol. 11:391-401.
55. Strauss, J., M. I. Muro-Pastor, and C. Scazzocchio. 1998. The regulator of nitrate assimilation in ascomycetes is a dimer which binds a nonrepeated, asymmetrical sequence. Mol. Cell. Biol. 18:1339-1348.
56. Tilburn, J., C. Scazzocchio, G. G. Taylor, J. H. Zabicky-Zissman, R. A. Lockington, and R. W. Davies. 1983. Transformation by integration in Aspergillus nidulans. Gene 26:205-221.
57. Todd, R. B., J. A. Fraser, K. H. Wong, M. A. Davis, and M. J. Hynes. 2005. Nuclear accumulation of the GATA factor AreA in response to complete nitrogen starvation by regulation of nuclear export. Eukaryot. Cell 4:1646-1653.
58. Tollervey, D., and H. N. Arst, Jr. 1981. Mutations to constitutivity and derepression are separate and separable in a regulatory gene of Aspergillus nidulans. Curr. Genet. 4:63-68.
59. Unkles, S. E., K. L. Hawker, C. Grieve, E. I. Campbell, P. Montague, and J. R. Kinghorn. 1991. crnA encodes a nitrate transporter in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 88:204-208. (Errata, 88:4564,1991, and 92:3076, 1995.)
60. Unkles, S. E., D. Zhou, M. Y. Siddiqi, J. R. Kinghorn, and A. D. Glass. 2001. Apparent genetic redundancy facilitates ecological plasticity for nitrate transport. EMBO J. 20:6246-6255.
61. Wang, R., M. Okamoto, X. Xing, and N. M. Crawford. 2003. Microarray analysis of the nitrate response in Arabidopsis Roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol. 132:556-567.
62. Whitehead, M. P., S. J. Gurr, C. Grieve, S. E. Unkles, D. Spence, M. Ramsden, and J. R. Kinghorn. 1990. Homologous transformation of Cephalosporium acremonium with the nitrate reductase-encoding gene (niaD). Gene 90:193-198.
63. Wolschek, M. F., F. Narendja, J. Karlseder, C. P. Kubicek, C. Scazzocchio, and J. Strauss. 1998. In situ detection of protein-DNA interactions in filamentous fungi by in vivo footprinting. Nucleic Acids Res. 26:3862-3864.
64. Wood, M. J., G. Storz, and N. Tjandra. 2004. Structural basis for redox regulation of Yap1 transcription factor localization. Nature 430:917-921.
65. Yagita, K., S. Yamaguchi, F. Tamanini, G. T. van Der Horst, J. H. Hoeijmakers, A. Yasui, J. J. Loros, J. C. Dunlap, and H. Okamura. 2000. Dimerization and nuclear entry of mPER proteins in mammalian cells. Genes Dev. 14:1353-1363.
66. Yang, L., L. Ukil, A. Osmani, F. Nahm, J. Davies, C. P. De Souza, X. Dou, A. Perez-Balaguer, and S. A. Osmani. 2004. Rapid production of gene replacement constructs and generation of a green fluorescent protein-tagged centromeric marker in Aspergillus nidulans. Eukaryot. Cell 3:1359-1362.
67. Zhang, Y., and Y. Xiong. 2001. A p53 amino-terminal nuclear export signal inhibited by DNA damage-induced phosphorylation. Science 292:1910-1915.
68. Zhu, J., R. J. Hill, P. J. Heid, M. Fukuyama, A. Sugimoto, J. R. Priess, and J. H. Rothman. 1997. end-1 encodes an apparent GATA factor that specifies the endoderm precursor in Caenorhabditis elegans embryos. Genes Dev. 11:2883-2896.