The CCAAT-binding complex coordinates the oxidative stress response in eukaryotes

Nucleic Acids Research

Volumn 38, Issue 4, 2009, Pages 1098-1113

  Thön, Marcel ^a,b   Abdallah, Qusai Al ^a,b   Hortschansky, Peter ^a,b   Scharf, Daniel H ^a,b   Eisendle, Martin ^c   Haas, Hubertus ^c   Brakhage, Axel A ^a,b  

^a HANS KNÖLL INSTITUTE   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CATALASE; CCAAT BINDING FACTOR; GLUTATHIONE; HISTONE; PEROXIREDOXIN; PROTEIN HAPC; PROTEIN HAPE; THIOL GROUP; THIOREDOXIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ANCF; UNCLASSIFIED DRUG; AAB 1 PROTEIN, NEUROSPORA; AAB-1 PROTEIN, NEUROSPORA; ANCF PROTEIN, ASPERGILLUS NIDULANS; CYSTEINE; DNA; FUNGAL PROTEIN; PROTEOME; THIOREDOXIN REDUCTASE;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CYTOPLASM; EUKARYOTE; GENE MUTATION; HOMEOSTASIS; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DNA BINDING; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TRANSCRIPTION REGULATION; ACTIVE TRANSPORT; ASPERGILLUS NIDULANS; CELL NUCLEUS; CHEMISTRY; DIMERIZATION; ENZYMOLOGY; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROMOTER REGION;

EMERICELLA NIDULANS; EUKARYOTA;

ACTIVE TRANSPORT, CELL NUCLEUS; ASPERGILLUS NIDULANS; CCAAT-BINDING FACTOR; CELL NUCLEUS; CYSTEINE; DIMERIZATION; DNA; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROMOTER REGIONS, GENETIC; PROTEOME; THIOREDOXIN-DISULFIDE REDUCTASE; THIOREDOXINS;

EID: 77950353370     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp1091     Document Type: Article

References (80)

1. Bucher, P. (1990) Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J. Mol. Biol., 212, 563-578.
2. Barberis, A., Superti-Furga, G. and Busslinger, M. (1987) Mutually exclusive interaction of the CCAAT-binding factor and of a displacement protein with overlapping sequences of a histone gene promoter. Cell, 50, 347-359.
3. Johnson, P.F. and McKnight, S.L. (1989) Eukaryotic transcriptional regulatory proteins. Annu. Rev. Biochem., 58, 799-839.
4. Mitchell, P.J. and Tjian, R. (1989) Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science, 245, 371-378.
5. Morgan, W.D., Williams, G.T., Morimoto, R.I., Greene, J., Kingston, R.E. and Tjian, R. (1987) Two transcriptional activators, CCAAT-box-binding transcription factor and heat shock transcription factor, interact with a human hsp70 gene promoter. Mol. Cell. Biol., 7, 1129-1138.
6. Pinkham, J.L. and Guarente, L. (1985) Cloning and molecular analysis of the HAP2 locus: a global regulator of respiratory genes in Saccharomyces cerevisiae. Mol. Cell. Biol., 5, 3410-3416.
7. Raymondjean, M., Cereghini, S. and Yaniv, M. (1988) Several distinct "CCAAT" box binding proteins coexist in eukaryotic cells. Proc. Natl Acad. Sci. USA, 85, 757-761.
8. Santoro, C., Mermod, N., Andrews, P.C. and Tjian, R. (1988) A family of human CCAAT-box-binding proteins active in transcription and DNA replication: cloning and expression of multiple cDNAs. Nature, 334, 218-224.
9. Forsburg, S.L. and Guarente, L. (1989) Identification and characterization of HAP4: a third component of the CCAAT-bound HAP2/HAP3 heteromer. Genes Dev., 3, 1166-1178.
10. McNabb, D.S., Tseng, K.A. and Guarente, L. (1997) The Saccharomyces cerevisiae Hap5p homolog from fission yeast reveals two conserved domains that are essential for assembly of heterotetrameric CCAAT-binding factor. Mol. Cell. Biol., 17, 7008-7018.
11. McNabb, D.S., Xing, Y. and Guarente, L. (1995) Cloning of yeast HAP5: a novel subunit of a heterotrimeric complex required for CCAAT binding. Genes Dev., 9, 47-58.
12. Olesen, J.T., Fikes, J.D. and Guarente, L. (1991) The Schizosaccharomyces pombe homolog of Saccharomyces cerevisiae HAP2 reveals selective and stringent conservation of the small essential core protein domain. Mol. Cell. Biol., 11, 611-619.
13. Mulder, W., Scholten, I.H., de Boer, R.W. and Grivell, L.A. (1994) Sequence of the HAP3 transcription factor of Kluyveromyces lactis predicts the presence of a novel 4-cysteine zinc-finger motif. Mol. Gen. Genet., 245, 96-106.
14. Edwards, D., Murray, J.A. and Smith, A.G. (1998) Multiple genes encoding the conserved CCAAT-box transcription factor complex are expressed in Arabidopsis. Plant Physiol., 117, 1015-1022.
15. Brakhage, A.A., Andrianopoulos, A., Kato, M., Steidl, S., Davis, M.A., Tsukagoshi, N. and Hynes, M.J. (1999) HAP-Like CCAAT-binding complexes in filamentous fungi: implications for biotechnology. Fungal Genet. Biol., 27, 243-252.
16. Li, Q., Herrler, M., Landsberger, N., Kaludov, N., Ogryzko, V.V., Nakatani, Y. and Wolffe, A.P. (1998) Xenopus NF-Y pre-sets chromatin to potentiate p300 and acetylation-responsive transcription from the Xenopus hsp70 promoter in vivo. EMBO J., 17, 6300-6315.
17. Hooft van Huijsduijnen, R., Li, X.Y., Black, D., Matthes, H., Benoist, C. and Mathis, D. (1990) Co-evolution from yeast to mouse: cDNA cloning of the two NF-Y (CP-1/CBF) subunits. EMBO J., 9, 3119-3127.
18. Maity, S.N., Vuorio, T. and de Crombrugghe, B. (1990) The B subunit of a rat heteromeric CCAAT-binding transcription factor shows a striking sequence identity with the yeast Hap2 transcription factor. Proc. Natl Acad. Sci. USA, 87, 5378-5382.
19. Becker, D.M., Fikes, J.D. and Guarente, L. (1991) A cDNA encoding a human CCAAT-binding protein cloned by functional complementation in yeast. Proc. Natl Acad. Sci. USA, 88, 1968-1972.
20. Tüncher, A., Spröte, P., Gehrke, A. and Brakhage, A.A. (2005) The CCAAT-binding complex of eukaryotes: evolution of a second NLS in the HapB subunit of the filamentous fungus Aspergillus nidulans despite functional conservation at the molecular level between yeast, A.nidulans and human. J. Mol. Biol., 352, 517-533.
21. Sinha, S., Maity, S.N., Lu, J. and de Crombrugghe, B. (1995) Recombinant rat CBF-C, the third subunit of CBF/NFY, allows formation of a protein-DNA complex with CBF-A and CBF-B and with yeast HAP2 and HAP3. Proc. Natl Acad. Sci. USA, 92, 1624-1628.
22. Litzka, O., Then Bergh, K. and Brakhage, A.A. (1996) The Aspergillus nidulans penicillin-biosynthesis gene aat (penDE)is controlled by a CCAAT-containing DNA element. Eur. J. Biochem., 238, 675-682.
23. Then Bergh, K., Litzka, O. and Brakhage, A.A. (1996) Identification of a major cis-acting DNA element controlling the bidirectionally transcribed penicillin biosynthesis genes acvA (pcbAB) and ipnA (pcbC)ofAspergillus nidulans. J. Bacteriol., 178, 3908-3916.
24. Littlejohn, T.G. and Hynes, M.J. (1992) Analysis of the site of action of the amdR product for regulation of the amdS gene of Aspergillus nidulans. Mol. Genet. Genom., 235, 81-88.
25. Steidl, S., Hynes, M.J. and Brakhage, A.A. (2001) The Aspergillus nidulans multimeric CCAAT binding complex AnCF is negatively autoregulated via its hapB subunit gene. J. Mol. Biol., 306, 643-653.
26. Weidner, G., Steidl, S. and Brakhage, A.A. (2001) The Aspergillus nidulans homoaconitase gene lysF is negatively regulated by the multimeric CCAAT-binding complex AnCF and positively regulated by GATA sites. Arch. Microbiol., 175, 122-132.
27. Kato, M., Tateyama, Y., Hayashi, K., Naruse, F., Oonishi, R., Tanoue, S., Tanaka, A., Kobayashi, T. and Tsukagoshi, N. (2002) A quantity control mechanism regulating levels of the HapE subunit of the Hap complex in Aspergillus nidulans:no accumulation of HapE in hapC deletion mutants. FEBS Lett., 512, 227-229.
28. Hortschansky, P., Eisendle, M., Al-Abdallah, Q., Schmidt, A.D., Bergmann, S., Thön, M., Kniemeyer, O., Abt, B., Seeber, B., Werner, E.R. et al. (2007) Interaction of HapX with the CCAAT -binding complex-a novel mechanism of gene regulation by iron. EMBO J., 26, 3157-3168.
29. McNabb, D.S. and Pinto, I. (2005) Assembly of the Hap2p/Hap3p/Hap4p/Hap5p-DNA complex in Saccharomyces cerevisiae. Eukaryot. Cell, 4, 1829-1839.
30. Nakshatri, H., Bhat-Nakshatri, P. and Currie, R.A. (1996) Subunit association and DNA binding activity of the heterotrimeric transcription factor NF-Y is regulated by cellular redox. J. Biol. Chem., 271, 28784-28791.
31. Yoshioka, J., Schreiter, E.R. and Lee, R.T. (2006) Role of thioredoxin in cell growth through interactions with signaling molecules. Antioxid. Redox Signal., 8, 2143-2151.
32. Maity, S.N. and de Crombrugghe, B. (1998) Role of the CCAAT-binding protein CBF/NF-Y in transcription. Trends Biochem. Sci., 23, 174-178.
33. Mantovani, R. (1999) The molecular biology of the CCAAT-binding factor NF-Y. Gene, 239, 15-27.
34. Pontecorvo, G., Roper, J.A., Hemmons, L.M., Macdonald, K.D. and Bufton, A.W. (1953) The genetics of Aspergillus nidulans. Adv. Genet., 5, 141-238.
35. Ballance, D.J., Buxton, F.P. and Turner, G. (1983) Transformation of Aspergillus nidulans by the orotidine-5′-phosphate decarboxylase gene of Neurospora crassa. Biochem. Biophys. Res. Commun., 112, 284-289.
36. Thön, M., Al-Abdallah, Q., Hortschansky, P. and Brakhage, A.A. (2007) The thioredoxin system of the filamentous fungus Aspergillus nidulans: impact on development and oxidative stress response. J. Biol. Chem., 282, 27259-27269.
37. Litzka, O., Then Bergh, K. and Brakhage, A.A. (1995) Analysis of the regulation of the Aspergillus nidulans penicillin biosynthesis gene aat (penDE), which encodes acyl coenzyme A:6-aminopenicillanic acid acyltransferase. Mol. Gen. Genet., 249, 557-569.
38. Lessing, F., Kniemeyer, O., Wozniok, I., Loeffler, J., Kurzai, O., Haertl, A. and Brakhage, A.A. (2007) The Aspergillus fumigatus transcriptional regulator AfYap1 represents the major regulator for defense against reactive oxygen intermediates but is dispensable for pathogenicity in an intranasal mouse infection model. Eukaryot. Cell, 6, 2290-2302.
39. Tietze, F. (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem., 27, 502-522.
40. Kniemeyer, O., Lessing, F., Scheibner, O., Hertweck, C. and Brakhage, A.A. (2006) Optimisation of a 2-D gel electrophoresis protocol for the human-pathogenic fungus Aspergillus fumigatus. Curr. Genet., 49, 178-189.
41. Kim, I.S., Sinha, S., de Crombrugghe, B. and Maity, S.N. (1996) Determination of functional domains in the C subunit of the CCAAT-binding factor (CBF) necessary for formation of a CBF-DNA complex: CBF-B interacts simultaneously with both the CBF-A and CBF-C subunits to form a heterotrimeric CBF molecule. Mol. Cell. Biol., 16, 4003-4013.
42. Sinha, S., Kim, I.S., Sohn, K.Y., de Crombrugghe, B. and Maity, S.N. (1996) Three classes of mutations in the A subunit of the CCAAT-binding factor CBF delineate functional domains involved in the three-step assembly of the CBF-DNA complex. Mol. Cell. Biol., 16, 328-337.
43. Romier, C., Cocchiarella, F., Mantovani, R. and Moras, D. (2003) The NF-YB/NF-YC structure gives insight into DNA binding and transcription regulation by CCAAT factor NF-Y. J. Biol. Chem., 278, 1336-1345.
44. Bordoli, L., Kiefer, F., Arnold, K., Benkert, P., Battey, J. and Schwede, T. (2009) Protein structure homology modeling using SWISS-MODEL workspace. Nature protocols, 4, 1-13.
45. Hisabori, T., Hara, S., Fujii, T., Yamazaki, D., Hosoya-Matsuda, N. and Motohashi, K. (2005) Thioredoxin affinity chromatography: a useful method for further understanding the thioredoxin network. J. Exp. Bot., 56, 1463-1468.
46. Messens, J., Van Molle, I., Vanhaesebrouck, P., Limbourg, M., Van Belle, K., Wahni, K., Martins, J.C., Loris, R. and Wyns, L. (2004) How thioredoxin can reduce a buried disulphide bond. J. Biol. Chem., 339, 527-537.
47. Hink, M.A., Bisselin, T. and Visser, A.J. (2002) Imaging protein-protein interactions in living cells. Plant Mol. Biol., 50, 871-883.
48. Hoff, B. and Kück, U. (2005) Use of bimolecular fluorescence complementation to demonstrate transcription factor interaction in nuclei of living cells from the filamentous fungus Acremonium chrysogenum. Curr. Genet., 47, 132-138.
49. Hu, C.D., Chinenov, Y. and Kerppola, T.K. (2002) Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell, 9, 789-798.
50. Hu, C.D. and Kerppola, T.K. (2003) Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis. Nat. Biotechnol., 21, 539-545.
51. Magliery, T.J., Wilson, C.G., Pan, W., Mishler, D., Ghosh, I., Hamilton, A.D. and Regan, L. (2005) Detecting protein-protein interactions with a green fluorescent protein fragment reassembly trap: scope and mechanism. J. Am. Chem. Soc., 127, 146-157.
52. Toone, W.M., Morgan, B.A. and Jones, N. (2001) Redox control of AP-1-like factors in yeast and beyond. Oncogene, 20, 2336-2346.
53. 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.
54. Kawasaki, L., Wysong, D., Diamond, R. and Aguirre, J. (1997) Two divergent catalase genes are differentially regulated during Aspergillus nidulans development and oxidative stress. J. Bacteriol., 179, 3284-3292.
55. Penninckx, M.J. (2002) An overview on glutathione in Saccharomyces versus non-conventional yeasts. FEMS Yeast Res., 2, 295-305.
56. Pocsi, I., Prade, R.A. and Penninckx, M.J. (2004) Glutathione, altruistic metabolite in fungi. Adv. Microb. Physiol., 49, 1-76.
57. Kato, M. (2005) An overview of the CCAAT-box binding factor in filamentous fungi: assembly, nuclear translocation, and transcriptional enhancement. Biosci., Biotechnol., Biochem., 69, 663-672.
58. Biteau, B., Labarre, J. and Toledano, M.B. (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature, 425, 980-984.
59. Woo, H.A., Chae, H.Z., Hwang, S.C., Yang, K.S., Kang, S.W., Kim, K. and Rhee, S.G. (2003) Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation. Science, 300, 653-656.
60. Ikuta, S., Imamura, S., Misaki, H. and Horiuti, Y. (1977) Purification and characterization of choline oxidase from Arthrobacter globiformis. J. Biochem., Tokyo, 82, 1741-1749.
61. Douglas, K.T. (1987) Mechanisms of action of glutathione-dependent enzymes. In Meister, A. (ed.), Advances in Enzymology and Related Areas of Molecular Biology, Vol. 59. John Wiley and Sons, Inc., New York, pp. 103-167.
62. Steidl, S., Tüncher, A., Goda, H., Guder, C., Papadopoulou, N., Kobayashi, T., Tsukagoshi, N., Kato, M. and Brakhage, A.A. (2004) A single subunit of a heterotrimeric CCAAT-binding complex carries a nuclear localization signal: piggy back transport of the pre-assembled complex to the nucleus. J. Mol. Biol., 342, 515-524.
63. 2 sensing through oxidation of the Yap1 transcription factor. EMBO J., 19, 5157-5166.
64. 2 receptor and redox-transducer in gene activation. Cell, 111, 471-481.
65. Kuge, S., Jones, N. and Nomoto, A. (1997) Regulation of yAP-1 nuclear localization in response to oxidative stress. EMBO J., 16, 1710-1720.
66. Tachibana, T., Okazaki, S., Murayama, A., Naganuma, A., Nomoto, A. and Kuge, S. (2009) A major peroxiredoxin-induced activation of Yap1 transcription factor is mediated by reduction-sensitive disulfide bonds and reveals a low level of transcriptional activation. J. Biol. Chem., 284, 4464-4472.
67. 2 and diamide. J. Biol. Chem., 272, 7908-7914.
68. Kuge, S. and Jones, N. (1994) YAP1 dependent activation of TRX2 is essential for the response of Saccharomyces cerevisiae to oxidative stress by hydroperoxides. EMBO J., 13, 655-664.
69. Lee, J., Godon, C., Lagniel, G., Spector, D., Garin, J., Labarre, J. and Toledano, M.B. (1999) Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J. Biol. Chem., 274, 16040-16046.
70. Izawa, S., Maeda, K., Sugiyama, K., Mano, J., Inoue, Y. and Kimura, A. (1999) Thioredoxin deficiency causes the constitutive activation of Yap1, an AP-1-like transcription factor in Saccharomyces cerevisiae. J. Biol. Chem., 274, 28459-28465.
71. Grant, C.M., Maciver, F.H. and Dawes, I.W. (1996) Stationary-phase induction of GLR1 expression is mediated by the yAP-1 transcriptional regulatory protein in the yeast Saccharomyces cerevisiae. Mol. Microbiol., 22, 739-746.
72. Lee, J., Dawes, I.W. and Roe, J.H. (1997) Isolation, expression, and regulation of the pgr1
73. Takeuchi, T., Miyahara, K., Hirata, D. and Miyakawa, T. (1997) Mutational analysis of Yap1 protein, an AP-1-like transcriptional activator of Saccharomyces cerevisiae. FEBS Lett., 416, 339-343.
74. Wu, A.L. and Moye-Rowley, W.S. (1994) GSH1, which encodes gamma-glutamylcysteine synthetase, is a target gene for yAP-1 transcriptional regulation. Mol. Cell. Biol., 14, 5832-5839.
75. Sato, I., Shimizu, M., Hoshino, T. and Takaya, N. (2009) The glutathione system of Aspergillus nidulans involves a fungus-specific glutathione S-transferase. J. Biol. Chem., 284, 8042-8053.
76. Lim, J.C., Choi, H.I., Park, Y.S., Nam, H.W., Woo, H.A., Kwon, K.S., Kim, Y.S., Rhee, S.G., Kim, K. and Chae, H.Z. (2008) Irreversible oxidation of the active-site cysteine of peroxiredoxin to cysteine sulfonic acid for enhanced molecular chaperone activity. J. Biol. Chem., 283, 28873-28880.
77. Nayak, T., Szewczyk, E., Oakley, C.E., Osmani, A., Ukil, L., Murray, S.L., Hynes, M.J., Osmani, S.A. and Oakley, B.R. (2006) A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics, 172, 1557-1566.
78. Papagiannopoulos, P., Andrianopoulos, A., Sharp, J.A., Davis, M.A. and Hynes, M.J. (1996) The hapC gene of Aspergillus nidulans is involved in the expression of CCAAT-containing promoters. Mol. Gen. Genet., 251, 412-421.
79. Weidner, G., d'Enfert, C., Koch, A., Mol, P.C. and Brakhage, A.A. (1998) Development of a homologous transformation system for the human pathogenic fungus Aspergillus fumigatus based on the pyrG gene encoding orotidine 5′-monophosphate decarboxylase. Curr. Genet., 33, 378-385.
80. Mabey Gilsenan, J.E., Atherton, G., Bartholomew, J., Giles, P.F., Attwood, T.K., Denning, D.W. and Bowyer, P. (2009) Aspergillus genomes and the Aspergillus cloud. Nucleic Acids Res., 37, D509-D514.