Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans

Molecular Microbiology

Volumn 50, Issue 4, 2003, Pages 1241-1255

  Lara Ortíz, Teresa ^a   Riveros Rosas, Héctor ^b   Aguirre, Jesús ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; MITOGEN ACTIVATED PROTEIN KINASE; NITROBLUE TETRAZOLIUM; PEROXIDASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

ARTICLE; ASPERGILLUS NIDULANS; CELL DIFFERENTIATION; CELL ULTRASTRUCTURE; CLEISTOTHECIA; ENZYME ACTIVITY; EUKARYOTE; FUNGUS HYPHAE; GENE DELETION; NONHUMAN; NUCLEOTIDE SEQUENCE; NULL ALLELE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEXUAL DEVELOPMENT; UNINDEXED SEQUENCE;

AMINO ACID SEQUENCE; ANIMALS; ASPERGILLUS NIDULANS; CELL DIFFERENTIATION; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE TARGETING; HUMANS; MOLECULAR SEQUENCE DATA; NADPH OXIDASE; PHYLOGENY; REACTIVE OXYGEN SPECIES; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

ANIMALIA; ASPERGILLUS; EMERICELLA NIDULANS; EUKARYOTA; FUNGI;

EID: 0345689448     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03800.x     Document Type: Article

References (60)

1. Adams, T.H., Wieser, J.K., and Yu, J.H. (1998) Asexual sporulation in Aspergillus nidulans. Microbiol Mol Biol Rev 62: 35-54.
2. Aguirre, J., Rodriguez, R., and Hansberg, W. (1989) Oxidation of Neurospora crassa NADP-specific glutamate dehydrogenase by activated oxygen species. J Bacteriol 171: 6243-6250.
3. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
4. Arnold, R.S., Shi, J., Murad, E., Whalen, A.M., Sun, C.Q., Polavarapu, R., et al. (2001) Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1. Proc Natl Acad Sci USA 98: 5550-5555.
5. Babior, B.M., Lambeth, J.D., and Nauseef, W. (2002) The neutrophil NADPH oxidase. Arch Biochem Biophys 397: 342-344.
6. Banfi, B., Molnar, G., Maturana, A., Steger, K., Hegedus, B., Demaurex, N., and Krause, K.H. (2001) A Ca(2+)-activated NADPH oxidase in testis, spleen, and lymph nodes. J Biol Chem 276: 37594-37601
7. Beckman, K.B., and Ames, B.N. (1998) The free radical theory of aging matures. Physiol Rev 78: 547-581.
8. Brody, H., Griffith, J., Cuticchia, A.J., Arnold, J., and Timberlake, W.E. (1991) Chromosome-specific recombinant DNA libraries from the fungus Aspergillus nidulans. Nucleic Acids Res 19: 3105-3109.
9. Champe, S.P., Nagle, D.L., and Yager, L.N. (1994) Sexual sporulation. In Aspergillus: 50 Years On, Vol. 29. Martinelli, S.D., and Kinghorn, J.R. (eds). Amsterdam: Elsevier, pp. 429-454.
10. Cheng, G., Cao, Z., Xu, X., van Meir, E.G., and Lambeth, J.D. (2001) Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 269: 131-140.
11. Clutterbuck, A.J. (1969) A mutational analysis of conidial development in Aspergillus nidulans. Genetics 63: 317-327.
12. Dehal, P., Satou, Y., Campbell, R.K., Chapman, J., Degnan, B., De Tomaso, A., et al. (2002) The draft genome of Ciona intestinales: insights into chordate and vertebrate origins. Science 298: 2157-2167.
13. Dinauer, M.C., Orkin, S.H., Brown, R., Jesaitis, A.J., and Parkos, C.A. (1987) The glycoprotein encoded by the X-linked chronic granulomatous disease locus is a component of the neutrophil cytochrome b complex. Nature 327: 717-720.
14. Dupuy, C., Ohayon, R., Valent, A., Noel-Hudson, M.S., Deme, D., and Virion, A. (1999) Purification of a novel flavoprotein involved in the thyroid NADPH oxidase. Cloning of the porcine and human cDNAs. J Biol Chem 274: 37265-37269.
15. Dutton, J.R., Johns, S., and Miller, B.L. (1997) StuAp is a sequence-specific transcription factor that regulates developmental complexity in Aspergillus nidulans. EMBO J 16: 5710-5721.
16. Edens, W.A., Sharling, L., Cheng, G., Shapira, R., Kinkade, J.M., Lee, T., et al. (2001) Tyrosine cross-linking of extracellular matrix is catalyzed by Duox, a multidomain oxidase/peroxidase with homology to the phagocyte oxidase subunit gp91phox. J Cell Biol 154: 879-891.
17. Foreman, J., Demidchik, V., Bothwell, J.H., Mylona, P., Miedema, H., Torres, M.A., et al. (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422: 442-446.
18. Galagan, J.E., Calvo, S.E., Borkovich, K.A., Selker, E.U., Read, N.D., Jaffe, D., et al. (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422: 859-868.
19. Geiszt, M., Kopp, J.B., Varnai, P., and Leto, T.L. (2000) Identification of renox, an NAD(P)H oxidase in kidney. Proc Natl Acad Sci USA 97: 8010-8014.
20. Geiszt, M., Lekstrom, K., Witta, J., and Leto, T.L. (2003) Proteins homologous to p47phox and p67phox support superoxide production by NAD(P)H oxidase 1 in colon epithelial cells. J Biol Chem 278: 20006-20012.
21. Greene, V., Cao, H., Schanne, F.A., and Bartelt, D.C. (2002) Oxidative stress-induced calcium signalling in Aspergillus nidulans. Cell Signal 14: 437-443.
22. Griendling, K.K., Sorescu, D., and Ushio-Fukai, M. (2000) NAD(P)H oxidase: role in cardiovascular biology and disease. Circulation Res 86: 494-501.
23. Halliwell, B., and Gutteridge, J.M.C. (1989) Free Radicals in Biology and Medicine. Oxford, UK: Clarendon Press and Oxford University Press.
24. Han, K.H., Han, K.Y., Yu, J.H., Chae, K.S., Jahng, K.Y., and Han, D.M. (2001) The nsdD gene encodes a putative GATA-type transcription factor necessary for sexual development of Aspergillus nidulans. Mol Microbiol 41: 299-309.
25. Hansberg, W., and Aguirre, J. (1990) Hyperoxidant states cause microbial cell differentiation by cell isolation from dioxygen. J Theor Biol 142: 201-221.
26. Hansberg, W., de Groot, H., and Sies, H. (1993) Reactive oxygen species associated with cell differentiation in Neurospora crassa. Free Radic Biol Med 14: 287-293.
27. Hermann, T.E., Kurtz, M.B., and Champe, S.P. (1983) Laccase localized in hulle cells and cleistothecial primordia of Aspergillus nidulans. J Bacteriol 154: 955-964.
28. Hill, T.W., and Käfer, E. (2001) Improved protocols for Aspergillus minimal medium: trace element and minimal medium stock solution. Fungal Genet Newslett 48: 20-21.
29. Hoffmann, B., Wanke, C., Lapaglia, S.K., and Braus, G.H. (2000) c-Jun and RACK1 homologues regulate a control point for sexual development in Aspergillus nidulans. Mol Microbiol 37: 28-41.
30. Irani, K., Xia, Y., Zweier, J.L., Der Sollott, S.J.C.J., Fearon, E.R., Sundaresan, M., et al. (1997) Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 275: 1649-1652.
31. Kawasaki, L., Sanchez, O., Shiozaki, K., and Aguirre, J. (2002) SakA MAP kinase is involved in stress signal transduction, sexual development and spore viability in Aspergillus nidulans. Mol Microbiol 45: 1153-1163.
32. Keller, T., Damude, H.G., Werner, D., Doerner, P., Dixon, R.A., and Lamb, C. (1998) A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. Plant Cell 10: 255-266.
33. Kim, D., Nakamura, A., Okamoto, T., Komatsu, N., Oda, T., lida, T., et al. (2000) Mechanism of superoxide anion generation in the toxic red tide phytoplankton Chattonella marina: possible involvement of NAD(P)H oxidase. Biochim Biophys Acta 1524: 220-227.
34. Kumar, S., Tamura, K., Jakobsen, I.B., and Nei, M. (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17: 1244-1245.
35. Kwak, J.M., Mori, I.C., Pei, Z.-M., Leonhardt, N., Torres, M.A., Dangl, J.L., et al. (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22: 2623-2633.
36. Lalucque, H., and Silar, P. (2003) NADPH oxidase: an enzyme for multicellularity? Trends Microbiol 11: 9-12.
37. Lambeth, J.D., Cheng, G., Arnold, R.S., and Edens, W.A. (2000) Novel homologs of gp91phox. Trends Biochem Sci 25: 459-461.
38. Law, D.J., and Timberlake, W.E. (1980) Developmental regulation of laccase levels in Aspergillus nidulans. J Bacteriol 144: 509-517.
39. McCord, J.M. (2000) The evolution of free radicals and oxidative stress. Am J Med 108: 652-659.
40. Martinelli, S.D., and Kinghorn, J.R. (eds) (1994) Aspergillus: 50 Years On. Amsterdam, The Netherlands: Elsevier.
41. Maturana, A., Arnaudeau, S., Ryser, S., Banfi, B., Hossle, J.P., Schlegel, W., et al. (2001) Heme histidine ligands within gp91 (phox) modulate proton conduction by the phagocyte NADPH oxidase. J Biol Chem 276: 30277-30284.
42. Moreno, J.C., Bikker, H., Kempers, M.J., van Trotsenburg, A.S., Baas, F., de Vijlder, J.J., et al. (2002) Inactivating mutations in the gene for thyroid oxidase 2 (THOX2) and congenital hypothyroidism. N Engl J Med 347: 95-102.
43. Navarro, R.E., and Aguirre, J. (1998) Posttranscriptional control mediates cell type-specific localization of catalase A during Aspergillus nidulans development. J Bacteriol 180: 5733-5738.
44. Osiewacz, H.D. (2002) Mitochondrial functions and aging. Gene 286: 65-71.
45. Riveros-Rosas, H., Julián-Sánchez, A., Villalobos-Molina, R., Pardo, J.P., and Piña, E. (2003) Diversity, taxonomy and evolution of medium-chain dehydrogenase/reductase superfamily. Eur J Biochem 270: 3309-3334.
46. Sagi, M., and Fluhr, R. (2001) Superoxide production by plant homologues of the gp91 (phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126: 1281-1290.
47. Satou, Y., Yamada, L., Mochizuki, Y., Takatori, N., Kawashima, T., Sasaki, A., et al. (2002) A cDNA resource from the basal chordate Ciona intestinalis. Genesis 33: 153-154.
48. Scherer, M., Wei, H., Liese, R., and Fischer, R. (2002) Aspergillus nidulans catalase-peroxidase gene (cpeA) is transcriptionally induced during sexual development through the transcription factor StuA. Eukaryot Cell 1: 725-735.
49. Shon, K.T., and Yoon, K.S. (2002) Ultrastructural study on the cleistothecium development in Aspergillus nidulans. Mycobiology 30: 117-127.
50. Skromne, I., Sanchez, O., and Aguirre, J. (1995) Starvation stress modulates the expression of the Aspergillus nidulans brlA regulatory gene. Microbiology 141: 21-28.
51. Suh, Y.A., Arnold, R.S., Lassegue, B., Shi, J., Xu, X., Sorescu, D., et al. (1999) Cell transformation by the superoxide-generating oxidase Mox1. Nature 401: 79-82.
52. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
53. Timberlake, W.E., and Clutterbuck, A.J. (1994) Genetic regulation of conidiation. In Aspergillus: 50 Years On, Vol. 29. Martinelli, S.D., and Kinghorn, J.R. (eds). Amsterdam: Elsevier, pp. 383-427.
54. Toledo, I., Noronha-Dutra, A.A., and Hansberg, W. (1991) Loss of NAD(P)-reducing power and glutathione disulfide excretion at the start of induction of aerial growth in Neurospora crassa. J Bacteriol 173: 3243-3249.
55. Toledo, I., Aguirre, J., and Hansberg, W. (1994) Enzyme inactivation related to a hyperoxidant state during conidiation of Neurospora crassa. Microbiology 140: 2391-2397.
56. Torres, M.A., Onouchi, H., Hamada, S., Machida, C., Hammond-Kosack, K.E., and Jones, J.D. (1998) Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). Plant J14: 365-370.
57. Torres, M.A., Dangl, J.L., and Jones, J.D. (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99: 517-522.
58. Vallim, M.A., Miller, K.Y., and Miller, B.L. (2000) Aspergillus SteA (sterile12-like) is a homeodomain-C2/H2-Zn+2 finger transcription factor required for sexual reproduction. Mol Microbiol 36: 290-301.
59. Wei, H., Requena, N., and Fischer, R. (2003) The MAPKK kinase SteC regulates conidiophore morphology and is essential for heterokaryon formation and sexual development in the homothallic fungus Aspergillus nidulans. Mol Microbiol 47: 1577-1588.
60. Yelton, M.M., Hamer, J.E., and Timberlake, W.E. (1984) Transformation of Aspergillus nidulans by using a trpC plasmid. Proc Natl Acad Sci USA 81: 1470-1474.