The RFX protein RfxA is an essential regulator of growth and morphogenesis in penicillium marneffei

Eukaryotic Cell

Volumn 9, Issue 4, 2010, Pages 578-591

  Bugeja, Hayley E ^a   Hynes, Michael J ^a   Andrianopoulos, Alex ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; DNA BINDING PROTEIN; FUNGAL PROTEIN; REGULATORY FACTOR X TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CELL DIFFERENTIATION; CELL DIVISION; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MOLECULAR GENETICS; MORPHOGENESIS; PENICILLIUM; PHYSIOLOGY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL DIVISION; DNA-BINDING PROTEINS; FUNGAL PROTEINS; HUMANS; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; PENICILLIUM; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); EUKARYOTA; FUNGI; PENICILLIUM MARNEFFEI;

EID: 77950537445     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00226-09     Document Type: Article

References (71)

1. Adams, T. H., M. T. Boylan, and W. E. Timberlake. 1988. BrlA is necessary and sufficient to direct conidiophore development in Aspergillus nidulans. Cell 54:353-362.
2. Anderson, M., S. S. Ng, V. Marchesi, F. H. MacIver, F. E. Stevens, T. Riddell, D. M. Glover, I. M. Hagan, and C. J. McInerny. 2002. Plo1(+) regulates gene transcription at the M-G(1) interval during the fission yeast mitotic cell cycle. EMBO J. 21:5745-5755.
3. Andrianopoulos, A., and W. E. Timberlake. 1994. The Aspergillus nidulans abaA gene encodes a transcriptional activator that acts as a genetic switch to control development. Mol. Cell. Biol. 14:2503-2515.
4. Ashburner, M., C. A. Ball, J. A. Blake, D. Botstein, H. Butler, J. M. Cherry, A. P. Davis, K. Dolinski, S. S. Dwight, J. T. Eppig, M. A. Harris, D. P. Hill, L. Issel-Tarver, A. Kasarskis, S. Lewis, J. C. Matese, J. E. Richardson, M. Ringwald, G. M. Rubin, and G. Sherlock. 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25:25-29.
5. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, and J. A. Smith. 1994. Current protocols in molecular biology. John Wiley & Sons, Inc., New York, NY.
6. Borneman, A. R., M. J. Hynes, and A. Andrianopoulos. 2000. The abaA homologue of Penicillium marneffei participates in two developmental programmes: conidiation and dimorphic growth. Mol. Microbiol. 38:1034-1047.
7. Borneman, A. R., M. J. Hynes, and A. Andrianopoulos. 2001. An STE12 homolog from the asexual, dimorphic fungus Penicillium marneffei complements the defect in sexual development of an Aspergillus nidulans steA mutant. Genetics 157:1003-1014.
8. Borneman, A. R., M. J. Hynes, and A. Andrianopoulos. 2002. A basic helixloop-helix protein with similarity to the fungal morphological regulators, Phd1p, Efg1p and StuA, controls conidiation but not dimorphic growth in Penicillium marneffei. Mol. Microbiol. 44:621-631.
9. Buck, V., S. S. Ng, A. B. Ruiz-Garcia, K. Papadopoulou, S. Bhatti, J. M. Samuel, M. Anderson, J. B. Millar, and C. J. McInerny. 2004. Fkh2p and Sep1p regulate mitotic gene transcription in fission yeast. J. Cell Sci. 117: 5623-5632.
10. Chan, Y. F., and T. C. Chow. 1990. Ultrastructural observations on Penicillium marneffei in natural human infection. Ultrastruct. Pathol. 14:439-452.
11. Chang, Y. C., and W. E. Timberlake. 1993. Identification of Aspergillus brlA response elements (BREs) by genetic selection in yeast. Genetics 133:29-38.
12. Clutterbuck, A. J. 1969. Cell volume per nucleus in haploid and diploid strains of Aspergillus nidulans. J. Gen. Microbiol. 55:291-299.
13. Clutterbuck, A. J. 1970. Synchronous nuclear division and septation in Aspergillus nidulans. J. Gen. Microbiol. 60:133-135.
14. Cove, D. J. 1966. The induction and repression of nitrate reductase in the fungus Aspergillus nidulans. Biochim. Biophys. Acta 113:51-56.
15. Denison, S. H., E. Kafer, and G. S. May. 1993. Mutation in the bimD gene of Aspergillus nidulans confers a conditional mitotic block and sensitivity to DNA damaging agents. Genetics 134:1085-1096.
16. Desany, B. A., A. A. Alcasabas, J. B. Bachant, and S. J. Elledge. 1998. Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes Dev. 12:2956-2970.
17. Dubruille, R., A. Laurencon, C. Vandaele, E. Shishido, M. Coulon-Bublex, P. Swoboda, P. Couble, M. Kernan, and B. Durand. 2002. Drosophila regulatory factor X is necessary for ciliated sensory neuron differentiation. Development 129:5487-5498.
18. Dutton, J. R., S. Johns, and B. L. Miller. 1997. StuAp is a sequence-specific transcription factor that regulates developmental complexity in Aspergillus nidulans. EMBO J. 16:5710-5721.
19. Efimenko, E., K. Bubb, H. Y. Mak, T. Holzman, M. R. Leroux, G. Ruvkun, J. H. Thomas, and P. Swoboda. 2005. Analysis of xbx genes in C. elegans. Development 132:1923-1934.
20. Efimov, V. P., and N. R. Morris. 1998. A screen for dynein synthetic lethals in Aspergillus nidulans identifies spindle assembly checkpoint genes and other genes involved in mitosis. Genetics 149:101-116.
21. Emery, P., B. Durand, B. Mach, and W. Reith. 1996. RFX proteins, a novel family of DNA binding proteins conserved in the eukaryotic kingdom. Nucleic Acids Res. 24:803-807.
22. Enos, A. P., and N. R. Morris. 1990. Mutation of a gene that encodes a kinesin-like protein blocks nuclear division in A. nidulans. Cell 60:1019-1027.
23. Fagundes, M. R., J. F. Lima, M. Savoldi, I. Malavazi, R. E. Larson, M. H. Goldman, and G. H. Goldman. 2004. The Aspergillus nidulans npkA gene encodes a Cdc2-related kinase that genetically interacts with the UvsBATR kinase. Genetics 167:1629-1641.
24. Gajiwala, K. S., H. Chen, F. Cornille, B. P. Roques, W. Reith, B. Mach, and S. K. Burley. 2000. Structure of the winged-helix protein hRFX1 reveals a new mode of DNA binding. Nature 403:916-921.
25. Garrison, R., and K. Boyd. 1973. Dimorphism of Penicillium marneffei as observed by electron microscopy. Can. J. Microbiol. 19:1305-1309.
26. Goldman, G. H., and E. Kafer. 2004. Aspergillus nidulans as a model system to characterize the DNA damage response in eukaryotes. Fungal Genet. Biol. 41:428-442.
27. Hao, B., C. J. Clancy, S. Cheng, S. B. Raman, K. A. Iczkowski, and M. H. Nguyen. 2009. Candida albicans RFX2 encodes a DNA binding protein involved in DNA damage responses, morphogenesis, and virulence. Eukaryot. Cell 8:627-639.
28. Harris, S. D., and J. E. Hamer. 1995. sepB: an Aspergillus nidulans gene involved in chromosome segregation and the initiation of cytokinesis. EMBO J. 14:5244-5257.
29. Harris, S. D., and P. R. Kraus. 1998. Regulation of septum formation in Aspergillus nidulans by a DNA damage checkpoint pathway. Genetics 148: 1055-1067.
30. Hastie, A. C. 1970. Benlate-induced inst ability of Aspergillus diploids. Nature 226:771.
31. Hoff, B., E. K. Schmitt, and U. Kuck. 2005. CPCR1, but not its interacting transcription factor AcFKH1, controls fungal arthrospore formation in Acremonium chrysogenum. Mol. Microbiol. 56:1220-1233.
32. Huang, M., Z. Zhou, and S. J. Elledge. 1998. The DNA replication and damage checkpoint pathways induce transcription by inhibition of the Crt1 repressor. Cell 94:595-605.
33. Iwama, A., J. Pan, P. Zhang, W. Reith, B. Mach, D. G. Tenen, and Z. Sun. 1999. Dimeric RFX proteins contribute to the activity and lineage specificity of the interleukin-5 receptor promoter through activation and repression domains. Mol. Cell. Biol. 19:3940-3950.
34. Katan, Y., R. Agami, and Y. Shaul. 1997. The transcriptional activation and repression domains of RFX1, a context-dependent regulator, can mutually neutralize their activities. Nucleic Acids Res. 25:3621-3628.
35. Katan-Khaykovich, Y., I. Spiegel, and Y. Shaul. 1999. The dimerization/ repression domain of RFX1 is related to a conserved region of its yeast homologues Crt1 and Sak1: a new function for an ancient motif. J. Mol. Biol. 294:121-137.
36. Liu, M., B. H. Lee, and M. B. Mathews. 1999. Involvement of RFX1 protein in the regulation of the human proliferating cell nuclear antigen promoter. J. Biol. Chem. 274:15433-15439.
37. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408.
38. Lubelsky, Y., N. Reuven, and Y. Shaul. 2005. Autorepression of rfx1 gene expression: functional conservation from yeast to humans in response to DNA replication arrest. Mol. Cell. Biol. 25:10665-10673.
39. Matsumura, T., T. Yuasa, T. Hayashi, T. Obara, Y. Kimata, and M. Yanagida. 2003. A brute force postgenome approach to identify temperature-sensitive mutations that negatively interact with separase and securin plasmids. Genes Cells 8:341-355.
40. May, G. S., C. A. McGoldrick, C. L. Holt, and S. H. Denison. 1992. The bimB3 mutation of Aspergillus nidulans uncouples DNA replication from the completion of mitosis. J. Biol. Chem. 267:15737-15743.
41. Mirabito, P. M., T. H. Adams, and W. E. Timberlake. 1989. Interactions of three sequentially expressed genes control temporal and spatial specificity in Aspergillus development. Cell 57:859-868.
42. Nakayama, A., H. Murakami, N. Maeyama, N. Yamashiro, A. Sakakibara, N. Mori, and M. Takahashi. 2003. Role for RFX transcription factors in nonneuronal cell-specific inactivation of the microtubule-associated protein MAP1A promoter. J. Biol. Chem. 278:233-240.
43. cdc25 in Aspergillus nidulans. EMBO J. 11:2139-2149.
44. Oliva, A., A. Rosebrock, F. Ferrezuelo, S. Pyne, H. Chen, S. Skiena, B. Futcher, and J. Leatherwood. 2005. The cell cycle-regulated genes of Schizosaccharomyces pombe. PLoS Biol. 3:e225.
45. Osmani, A. H., B. R. Oakley, and S. A. Osmani. 2006. Identification and analysis of essential Aspergillus nidulans genes using the heterokaryon rescue technique. Nat. Protoc. 1:2517-2526.
46. Osmani, S. A., D. B. Engle, J. H. Doonan, and N. R. Morris. 1988. Spindle formation and chromatin condensation in cells blocked at interphase by mutation of a negative cell cycle control gene. Cell 52:241-251.
47. Otsuki, K., Y. Hayashi, M. Kato, H. Yoshida, and M. Yamaguchi. 2004. Characterization of dRFX2, a novel RFX family protein in Drosophila. Nucleic Acids Res. 32:5636-5648.
48. Papadopoulou, K., S. S. Ng, H. Ohkura, M. Geymonat, S. G. Sedgwick, and C. J. McInerny. 2008. Regulation of gene expression during M-G1-phase in fission yeast through Plo1p and forkhead transcription factors. J. Cell Sci. 121:38-47.
49. Pinsky, B. A., and S. Biggins. 2005. The spindle checkpoint: tension versus attachment. Trends Cell Biol. 15:486-493.
50. Pitt, C. W., E. Moreau, P. A. Lunness, and J. H. Doonan. 2004. The pot1 homologue in Aspergillus nidulans is required for ordering mitotic events. J. Cell Sci. 117:199-209.
51. Pongsunk, S., A. Andrianopoulos, and S. C. Chaiyaroj. 2005. Conditional lethal disruption of TATA-binding protein gene in Penicillium marneffei. Fungal Genet. Biol. 42:893-903.
52. Reith, W., C. Herrero-Sanchez, M. Kobr, P. Silacci, C. Berte, E. Barras, S. Fey, and B. Mach. 1990. MHC class II regulatory factor RFX has a novel DNA-binding domain and a functionally independent dimerization domain. Genes Dev. 4:1528-1540.
53. Reith, W., C. Ucla, E. Barras, A. Gaud, B. Durand, C. Herrero-Sanchez, M. Kobr, and B. Mach. 1994. RFX1, a transactivator of hepatitis B virus enhancer I, belongs to a novel family of homodimeric and heterodimeric DNA-binding proteins. Mol. Cell. Biol. 14:1230-1244.
54. Salimova, E., M. Sohrmann, N. Fournier, and V. Simanis. 2000. The S. pombe orthologue of the S. cerevisiae mob1 gene is essential and functions in signalling the onset of septum formation. J. Cell Sci. 113:1695-1704.
55. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
56. Schmitt, E. K., A. Bunse, D. Janus, B. Hoff, E. Friedlin, H. Kurnsteiner, and U. Kuck. 2004. Winged helix transcription factor CPCR1 is involved in regulation of -lactam biosynthesis in the fungus Acremonium chrysogenum. Eukaryot. Cell 3:121-134.
57. Schmitt, E. K. and U. Kuck. 2000. The fungal CPCR1 protein, which binds specifically to -lactam biosynthesis genes, is related to human regulatory factor X transcription factors. J. Biol. Chem. 275:9348-9357.
58. Siegrist, C. A., B. Durand, P. Emery, E. David, P. Hearing, B. Mach, and W. Reith. 1993. RFX1 is identical to enhancer factor C and functions as a transactivator of the hepatitis B virus enhancer. Mol. Cell. Biol. 13:6375-6384.
59. Steimle, V., B. Durand, E. Barras, M. Zufferey, M. R. Hadam, B. Mach, and W. Reith. 1995. A novel DNA-binding regulatory factor is mutated in primary MHC class II deficiency (bare lymphocyte syndrome). Genes Dev. 9:1021-1032.
60. Swoboda, P., H. T. Adler, and J. H. Thomas. 2000. The RFX-type transcription factor DAF-19 regulates sensory neuron cilium formation in C. elegans. Mol. Cell 5:411-421.
61. Thompson, J. D., F. Plewniak, J. Thierry, and O. Poch. 2000. DbClustal: rapid and reliable global multiple alignments of protein sequences detected by database searches. Nucleic Acids Res. 28:2919-2926.
62. Uhlmann, F., D. Wernic, M. A. Poupart, E. V. Koonin, and K. Nasmyth. 2000. Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 103:375-386.
63. Upshall, A., and I. D. Mortimore. 1984. Isolation of aneuploid-generating mutants of Aspergillus nidulans, one of which is defective in interphase of the cell cycle. Genetics 108:107-121.
64. van Helden, J. 2003. Regulatory sequence analysis tools. Nucleic Acids Res. 31:3593-3596.
65. Wolkow, T. D., P. M. Mirabito, S. Venkatram, and J. E. Hamer. 2000. Hypomorphic bimA (APC3) alleles cause errors in chromosome metabolism that activate the DNA damage checkpoint blocking cytokinesis in Aspergillus nidulans. Genetics 154:167-179.
66. Wu, S. Y., and M. McLeod. 1995. The sak1 gene of Schizosaccharomyces pombe encodes an RFX family DNA-binding protein that positively regulates cyclic AMP-dependent protein kinase-mediated exit from the mitotic cell cycle. Mol. Cell. Biol. 15:1479-1488.
67. Ye, X. S., S. L. Lee, T. D. Wolkow, S. L. McGuire, J. E. Hamer, G. C. Wood, and S. A. Osmani. 1999. Interaction between developmental and cell cycle regulators is required for morphogenesis in Aspergillus nidulans. EMBO J. 18:6994-7001.
68. Yuasa, T., T. Hayashi, N. Ikai, T. Katayama, K. Aoki, T. Obara, Y. Toyoda, T. Maruyama, D. Kitagawa, K. Takahashi, K. Nagao, Y. Nakaseko, and M. Yanagida. 2004. An interactive gene network for securin-separase, condensin, cohesin, Dis1/Mtc1 and histones constructed by mass transformation. Genes Cells 9:1069-1082.
69. Zadra, I., B. Abt, W. Parson, and H. Haas. 2000. xylP promoter-based expression system and its use for antisense downregulation of the Penicillium chrysogenum nitrogen regulator NRE. Appl. Environ. Microbiol. 66:4810-4816.
70. Zaim, J., E. Speina, and A. M. Kierzek. 2005. Identification of new genes regulated by the Crt1 transcription factor, an effector of the DNA damage checkpoint pathway in Saccharomyces cerevisiae. J. Biol. Chem. 280:28-37.
71. Zajac-Kaye, M., N. Ben-Baruch, E. Kastanos, F. J. Kaye, and C. Allegra. 2000. Induction of Myc-intron-binding polypeptides MIBP1 and RFX1 during retinoic acid-mediated differentiation of haemopoietic cells. Biochem. J. 345:535-541.