Purine utilization proteins in the Eurotiales: Cellular compartmentalization, phylogenetic conservation and divergence

Fungal Genetics and Biology

Volumn 69, Issue , 2014, Pages 96-108

  Galanopoulou, Katerina ^a   Scazzocchio, Claudio ^b,c   Galinou, Maria Eleftheria ^a   Liu, Weiwei ^b,d   Borbolis, Fivos ^a   Karachaliou, Mayia ^a   Oestreicher, Nathalie ^b,e   Hatzinikolaou, Dimitris G ^a   Diallinas, George ^a   Amillis, Sotiris ^a  

^a UNIVERSITY OF ATHENS   (Greece)

^b INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d Jubilant HollisterStier   (Canada)

^e UNIVERSITÉ DE CAEN   (France)

Author keywords

Aspergillus nidulans; Peroxisome; Transporter; Uric acid

Indexed keywords

2 OXO 4 HYDROXY 4 CARBOXYUREIDOIMIDAZOLINE DECARBOXYLASE; ALLANTOICASE; ALLANTOINASE; ALPHA KETOGLUTARATE IRON DEPENDENT DIOXYGENASE; FUNGAL ENZYME; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR UAY; UNCLASSIFIED DRUG; URATE OXIDASE; UREIDOGLYCOLATE LYASE; URIC ACID; XANTHINE DEHYDROGENASE; FUNGAL PROTEIN; PURINE DERIVATIVE;

ARTICLE; CELL COMPARTMENTALIZATION; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONIDIUM; CONTROLLED STUDY; CYTOSOL; EUROTIALES; EUROTIOMYCETES; NONHUMAN; OXIDATIVE STRESS; PEROXISOME; PEZIZOMYCOTINA; PRIORITY JOURNAL; PURINE METABOLISM; PURINE UTILIZATION; CHEMISTRY; CYTOPLASM; FUNGUS SPORE; GENETICS; METABOLISM;

CELL NUCLEUS; CYTOPLASM; EUROTIALES; FUNGAL PROTEINS; METABOLIC NETWORKS AND PATHWAYS; PEROXISOMES; PURINES; SPORES, FUNGAL;

EID: 84904247774     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2014.06.005     Document Type: Article

References (75)

1. Allam A.M., Elzainy T.A. Degradation of xanthine by Penicillium chrysogenum. J. Gen. Microbiol. 1969, 56:293-300.
2. Amrani L., Primus J., Glatigny A., Arcangeli L., Scazzocchio C., Finnerty V. Comparison of the sequences of the Aspergillus nidulans hxB and Drosophila melanogaster ma-l genes with nifS from Azotobacter vinelandii suggests a mechanism for the insertion of the terminal sulphur atom in the molybdopterin cofactor. Mol. Microbiol. 2000, 38:114-125.
3. Apostolaki A., Harispe L., Calcagno-Pizarelli A.M., Vangelatos I., Sophianopoulou V., Arst H.N., Peñalva M.A., Amillis S., Scazzocchio C. Aspergillus nidulans CkiA is an essential casein kinase I required for delivery of amino acid transporters to the plasma membrane. Mol. Microbiol. 2012, 84:530-549.
4. Berger H., Pachlinger R., Morozov I., Goller S., Narendja F., Caddick M., Strauss J. The GATA factor AreA regulates localization and in vivo binding site occupancy of the nitrate activator NirA. Mol. Microbiol. 2006, 59:433-446.
5. Bernreiter A., Ramon A., Fernández-Martínez J., Berger H., Araújo-Bazan L., Espeso E.A., Pachlinger R., Gallmetzer A., Anderl I., Scazzocchio C., Strauss J. Nuclear export of the transcription factor NirA is a regulatory checkpoint for nitrate induction in Aspergillus nidulans. Mol. Cell. Biol. 2007, 27:791-802.
6. Cecchetto G., Richero M., Oestreicher N., Muro-Pastor M.I., Pantano S., Scazzocchio C. Mutations in the basic loop of the Zn binuclear cluster of the UaY transcriptional activator suppress mutations in the dimerisation domain. Fungal Genet. Biol. 2012, 49:731-743.
7. Cove D.J. Evidence for a near limiting intracellular concentration of a regulator substance. Nature 1969, 224:272-273.
8. Cultrone A., Scazzocchio C., Rochet M., Montero-Morán G., Drevet C., Fernández-Martín R. Convergent evolution of hydroxylation mechanisms in the fungal kingdom: molybdenum cofactor-independent hydroxylation of xanthine via alpha-ketoglutarate-dependent dioxygenases. Mol. Microbiol. 2005, 57:276-290.
9. Cultrone A., Domínguez Y.R., Drevet C., Scazzocchio C., Fernández-Martín R. The tightly regulated promoter of the xanA gene of Aspergillus nidulans is included in a helitron. Mol. Microbiol. 2007, 63:1577-1587.
10. Darlington A.J., Scazzocchio C. Evidence for an alternative pathway of xanthine oxidation in Aspergillus nidulans. Biochim. Biophys. Acta 1968, 166:569-571.
11. Darlington A.J., Scazzocchio C., Pateman J.A. Biochemical and genetical studies of purine breakdown in Aspergillus. Nature 1965, 206:599-600.
12. De la Riva L., Badia J., Aguilar J., Bender R.A., Baldoma L. The hpx genetic system for hypoxanthine assimilation as a nitrogen source in Klebsiella pneumoniae: gene organization and transcriptional regulation. J. Bacteriol. 2008, 190:7892-7903.
13. Diallinas G. Aspergillus transporters. The Aspergilli. Genomics, Medical Applications, Biotechnology, and Research Methods 2008, 297-316. CRC Press. A. Osmani, G.H. Goldman (Eds.).
14. Enroth C., Eger B.T., Okamoto K., Nishino T., Nishino T., Pai E.F. Crystal structures of bovine milk xanthine dehydrogenase and xanthine oxidase: structure-based mechanism of conversion. Proc. Natl. Acad. Sci. USA 2000, 97:10723-10728.
15. Espeso E.A., Cobeño L., Arst H.N. Discrepancies between recombination frequencies and physical distances in Aspergillus nidulans: implications for gene identification. Genetics 2005, 171:835-838.
16. Etxebeste O., Markina-Iñarrairaegui A., Grazia A., Herrero-García E., Ugalde U., Espeso E.A. Kap1, a non-essential member of the Pse1p/lmp5 karyopherin family, controls colonial and asexual development in Aspergillus nidulans. Microbiology 2009, 155:3934-3945.
17. Gill G., Ptashne M. Negative effect of the transcriptional activator GAL4. Nature 1988, 334:721-724.
18. Glatigny A., Scazzocchio C. Cloning and molecular characterization of hxA, the gene coding for the xanthine dehydrogenase (purine hydroxylase I) of Aspergillus nidulans. J. Biol. Chem. 1995, 270:3534-3550.
19. Gómez D., Cubero B., Cecchetto G., Scazzocchio C. PrnA, a Zn2Cys6 activator with a unique DNA recognition mode, requires inducer for in vivo binding. Mol. Microbiol. 2002, 44:585-597.
20. Gómez D., García I., Scazzocchio C., Cubero B. Multiple GATA sites: protein binding and physiological relevance for the regulation of the proline transporter gene of Aspergillus nidulans. Mol. Microbiol. 2003, 50:277-289.
21. Gournas C., Amillis S., Vlanti A., Diallinas G. Transport-dependent endocytosis and turnover of a uric acid-xanthine permease. Mol. Microbiol. 2010, 75:246-260.
22. Gournas C., Oestreicher N., Amillis S., Diallinas G., Scazzocchio C. Completing the purine utilisation pathway of Aspergillus nidulans. Fungal Genet. Biol. 2011, 48:840-848.
23. Gründlinger M., Yasmin S., Lechner B.E., Geley S., Schrettl M., Hynes M., Haas H. Fungal siderophore biosynthesis is partially localized in peroxisomes. Mol. Microbiol. 2013, 88:862-875.
24. Hamari Z., Amillis S., Drevet C., Apostolaki A., Vágvölgyi C., Diallinas G., Scazzocchio C. Convergent evolution and orphan genes in the Fur4p-like family and characterization of a general nucleoside transporter in Aspergillus nidulans. Mol. Microbiol. 2009, 73:43-57.
25. Hayashi S., Fujiwara S., Noguchi T. Evolution of urate-degrading enzymes in animal peroxisomes. Cell Biochem. Biophys. 2000, 32:123-129.
26. Hilliker A.J., Duyf B., Evans D., Phillips J.P. Urate-null rosy mutants of Drosophila melanogaster are hypersensitive to oxygen stress. Proc. Natl. Acad. Sci. USA 1992, 89:4343-4347.
27. Hynes M.J., Murray S.L., Khew G.S., Davis M.A. Genetic analysis of the role of peroxisomes in the utilization of acetate and fatty acids in Aspergillus nidulans. Genetics 2008, 178:1355-1369.
28. Ito M., Nakamura M., Kato S., Ogawa H., Takagi Y. Structural analysis of the rat uricase gene and evidence that lysine 164 is involved in the substrate-binding site of the enzyme. Adv. Exp. Med. Biol. 1991, 309:377-381.
29. Karachaliou M., Amillis S., Evangelinos M., Kokotos A.C., Yalelis V., Diallinas G. The arrestin-like protein ArtA is essential for ubiquitination and endocytosis of the UapA transporter in response to both broad-range and specific signals. Mol. Microbiol. 2013, 88:301-317.
30. Kim K., Kim M.I., Chung J., Ahn J.H., Rhee S. Crystal structure of metal-dependent allantoinase from Escherichia coli. J. Mol. Biol. 2009, 387:1067-1074.
31. Koukaki M., Giannoutsou E., Karagouni A., Diallinas G. A novel improved method for Aspergillus nidulans transformation. J. Microbiol. Methods 2003, 55:687-695.
32. Kunze M., Hartig A. Permeability of the peroxisomal membrane: lessons from the glyoxylate cycle. Front. Physiol. 2013, 4:204.
33. Lehninger A.L. Biochemistry 1981, Worth, New York, pp. 729-747. second ed.
34. Lewis N.J., Scazzocchio C. The genetic control of molybdoflavoproteins in Aspergillus nidulans. A xanthine dehydrogenase I half-molecule in cnx-mutant strains of Aspergillus nidulans. Eur. J. Biochem. 1977, 76:441-446.
35. Lewis N.J., Hurt P., Sealy-Lewis H.M., Scazzocchio C. The genetic control of the molybdoflavoproteins in Aspergillus nidulans. IV. A comparison between purine hydroxylase I and II. Eur. J. Biochem. 1978, 91:311-316.
36. Li L., Hu X., Xia Y., Xiao G., Zheng P., Wang C. Linkage of oxidative stress and mitochondrial dysfunctions to spontaneous culture degeneration in Aspergillus nidulans. Mol. Cell. Proteomics 2014, 13:449-461.
37. Liu T.D., Marzluf G.A. Characterization of pco-1, a newly identified gene which regulates purine catabolism in Neurospora. Curr. Genet. 2004, 46:213-227.
38. Liu W., Mellado L., Espeso E.A., Heather M., Sealy-Lewis H.M. In Aspergillus nidulans the suppressors suaA and suaC code for release factors eRF1 and eRF3 and suaD codes for a glutamine tRNA. G3 (Bethesda) 2014, 4:1047-1057.
39. Mei D.A., Gross G.J., Nithipatikom K. Simultaneous determination of adenosine, inosine, hypoxanthine, xanthine, and uric acid in microdialysis samples using microbore column high-performance liquid chromatography with a diode array detector. Anal. Biochem. 1996, 238:34-39.
40. Montero-Morán G.M., Li M., Rendòn-Huerta E., Jourdan F., Lowe D.J., Stumpff-Kane A.W., Feig M., Scazzocchio C., Hausinger R.P. Purification and characterization of the FeII- and alpha-ketoglutarate-dependent xanthine hydroxylase from Aspergillus nidulans. Biochemistry 2007, 46:5293-5304.
41. Moriwaki Y., Yamamoto T., Higashino K. Enzymes involved in purine metabolism - a review of histochemical localization and functional implications. Histol. Histopathol. 1999, 14:1321-1340.
42. Müller M., Moller K.M. Urate oxidase and its association with peroxisomes in Acanthamoeba sp. Eur. J. Biochem. 1969, 9:424-430.
43. Nayak T., Szewczyk E., Oakley C.E., Osmani A., Ukil L., Murray S.L., Hynes M.J., Osmani S.A., Oakley B.R. A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 2006, 172:1557-1566.
44. Nikolaev I., Cochet M.F., Felenbok B. Nuclear import of zinc binuclear cluster proteins proceeds through multiple, overlapping transport pathways. Eukaryot. Cell 2003, 2:209-221.
45. Oestreicher N., Scazzocchio C. Sequence, regulation, and mutational analysis of the gene encoding urate oxidase in Aspergillus nidulans. J. Biol. Chem. 1993, 268:23382-23389.
46. Oestreicher N., Scazzocchio C. A single amino acid change in a pathway-specific transcription factor results in differing degrees of constitutivity, hyperinducibility and derepression of several structural genes. J. Mol. Biol. 1995, 249:693-699.
47. Oestreicher N., Scazzocchio C. Phenotypes of mutations in the 5'-UTR of a limiting transcription factor in Aspergillus nidulans can be accounted for by translational inhibition and leaky scanning. Genetics 2009, 181:1261-1272.
48. Oestreicher N., Sealy-Lewis H.M., Scazzocchio C. Characterisation, cloning and integrative properties of the gene encoding urate oxidase in Aspergillus nidulans. Gene 1993, 132:185-192.
49. Oestreicher N., Scazzocchio C., Suárez T. Mutations in a dispensable region of the UaY transcription factor of Aspergillus nidulans differentially affect the expression of structural genes. Mol. Microbiol. 1997, 24:1189-1199.
50. Pantazopoulou A., Lemuh N.D., Hatzinikolaou D.G., Drevet C., Cecchetto G., Scazzocchio C., Diallinas G. Differential physiological and developmental expression of the UapA and AzgA purine transporters in Aspergillus nidulans. Fungal Genet. Biol. 2007, 44:627-640.
51. Peñalva M.A. Tracing the endocytic pathway of Aspergillus nidulans with FM4-64. Fungal Genet. Biol. 2005, 42:963-975.
52. Percudani R., Carnevali D., Puggioni V. Ureidoglycolate hydrolase, amidohydrolase, lyase: how errors in biological databases are incorporated in scientific papers and vice versa. Database (Oxford) 2013, 2013:bat071.
53. Petriv O.I., Tang L., Titorenko V.I., Rachubinski R.A. A new definition for the consensus sequence of the peroxisome targeting signal type 2. J. Mol. Biol. 2004, 341:119-134.
54. Pokorska A., Drevet C., Scazzocchio C. The analysis of the transcriptional activator PrnA reveals a tripartite nuclear localisation sequence. J. Mol. Biol. 2000, 298:585-596.
55. Pope S.D., Chen L.L., Stewart V. Purine utilization by Klebsiella oxytoca M5al: genes for ring-oxidizing and -opening enzymes. J. Bacteriol. 2009, 191:1006-1017.
56. Puggioni V., Dondi A., Folli C., Shin I., Rhee S., Percudani R. Gene context analysis reveals functional divergence between hypothetically equivalent enzymes of the purine-ureide pathway. Biochemistry 2014, 53:735-745.
57. Ramazzina I., Folli C., Secchi A., Berni R., Percudani R. Completing the uric acid degradation pathway through phylogenetic comparison of whole genomes. Nat. Chem. Biol. 2006, 2:144-148.
58. Ramazzina I., Cendron L., Folli C., Berni R., Monteverdi D., Zanotti G., Percudani R. Logical identification of an allantoinase analog (puuE) recruited from polysaccharide deacetylases. J. Biol. Chem. 2008, 283:23295-23304.
59. Raymond S., Tocilj A., Ajamian E., Li Y., Hung M.N., Matte A., Cygler M. Crystal structure of ureidoglycolate hydrolase (AllA) from Escherichia coli O157:H7. Proteins 2005, 61:454-459.
60. Roberts T., Martinelli S., Scazzocchio C. Allele specific, gene unspecific suppressors in Aspergillus nidulans. Mol. Gen. Genet. 1979, 177:57-64.
61. Scazzocchio C. The genetics of the molybdenum-containing enzymes. Molybdenum and Molybdenum-containing Enzymes 1980, 487-515. Pergamon Press, Oxford, New York, Toronto, Sydney, Paris, Frankfurt. M. Coughlan (Ed.).
62. Scazzocchio C. The purine degradation pathway, genetics, biochemistry and regulation. Prog. Ind. Microbiol. 1994, 29:221-257.
63. Scazzocchio C., Darlington A.J. The induction and repression of the enzymes of purine breakdown in Aspergillus nidulans. Biochim. Biophys. Acta 1968, 166:557-568.
64. Scazzocchio C., Holl F.B., Foguelman A.I. The genetic control of molybdoflavoproteins in Aspergillus nidulans. Allopurinol-resistant mutants constitutive for xanthine-dehydrogenase. Eur. J. Biochem. 1973, 36:428-445.
65. Scazzocchio C., Sdrin N., Ong G. Positive regulation in a eukaryote, a study of the uaY gene of Aspergillus nidulans: I. Characterization of alleles, dominance and complementation studies, and a fine structure map of the uaY-oxpA cluster. Genetics 1982, 100:185-208.
66. Sealy-Lewis H.M., Scazzocchio C., Lee S. A mutation defective in the xanthine alternative pathway of Aspergillus nidulans: its use to investigate the specificity of uaY mediated induction. Mol. Gen. Genet. 1978, 164:303-308.
67. Suárez T., Oestreicher N., Peñalva M.A., Scazzocchio C. Molecular cloning of the uaY regulatory gene of Aspergillus nidulans reveals a favoured region for DNA insertions. Mol. Gen. Genet. 1991, 230:369-375.
68. Suárez T., de Queiroz M.V., Oestreicher N., Scazzocchio C. The sequence and binding specificity of UaY, the specific regulator of the purine utilization pathway in Aspergillus nidulans, suggest an evolutionary relationship with the PPR1 protein of Saccharomyces cerevisiae. EMBO J. 1995, 14:1453-1467.
69. Takada Y., Tsukiji N. Peroxisomal localization and activation by bivalent metal ions of ureidoglycolate lyase, the enzyme involved in urate degradation in Candida tropicalis. J. Bacteriol. 1987, 169:2284-2286.
70. Tavernarakis N., Thireos G. Transcriptional interference caused by GCN4 overexpression reveals multiple interactions mediating transcriptional activation. Mol. Gen. Genet. 1995, 247:571-578.
71. Tilburn J., Scazzocchio C., Taylor G.G., Zabicky-Zissman J.H., Lockington R.A., Davies R.W. Transformation by integration in Aspergillus nidulans. Gene 1983, 26:205-221.
72. Valdez-Taubas J., Harispe L., Scazzocchio C., Gorfinkiel L., Rosa A.L. Ammonium-induced internalisation of UapC, the general purine permease from Aspergillus nidulans. Fungal Genet. Biol. 2004, 41:42-51.
73. Vogels G.D., Van der Drift C. Degradation of purines and pyrimidines by microorganisms. Bacteriol. Rev. 1976, 40:403-468.
74. Yu R., Schellhorn H.E. Recent applications of engineered animal antioxidant deficiency models in human nutrition and chronic disease. J. Nutr. 2013, 143:1-11.
75. Zanotti G., Cendron L., Ramazzina I., Folli C., Percudani R., Berni R. Structure of zebra fish HIUase: insights into evolution of an enzyme to a hormone transporter. J. Mol. Biol. 2006, 363:1-9.