Transport assays in filamentous fungi: Kinetic characterization of the UapC purine transporter of Aspergillus nidulans

Fungal Genetics and Biology

Volumn 63, Issue , 2014, Pages 1-8

  Krypotou, Emilia ^a   Diallinas, George ^a  

^a UNIVERSITY OF ATHENS   (Greece)

Author keywords

Germinating conidiospores; NAT; Specificity; Uptake; Uric acid; Xanthine

Indexed keywords

CARRIER PROTEIN; UAPC PURINE TRANSPORTER; UNCLASSIFIED DRUG; URIC ACID; XANTHINE;

ARTICLE; BINDING AFFINITY; BIOASSAY; CONIDIUM; CONTROLLED STUDY; EMERICELLA NIDULANS; FUNGUS GROWTH; GENE SEQUENCE; GERMINATION; MYCELIUM; NONHUMAN; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; TRANSPORT ASSAY; TRANSPORT KINETICS;

ASCOMYCOTA; EMERICELLA NIDULANS; FUNGI;

GERMINATING CONIDIOSPORES; NAT; SPECIFICITY; UPTAKE; URIC ACID; XANTHINE;

AMINO ACID SEQUENCE; ASPERGILLUS NIDULANS; BIOLOGICAL TRANSPORT; FUNGAL PROTEINS; KINETICS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; OXYPURINOL; PURINES; URIC ACID; XANTHINE;

EID: 84892484643     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2013.12.004     Document Type: Article

References (58)

1. + symporter in Aspergillus nidulans. Fungal Genet. Biol. 2010, 47:1023-1033.
2. Ahmad M., Bussey H. Yeast arginine permease: nucleotide sequence of the CAN1 gene. Curr. Genet. 1986, 10:587-592.
3. Amillis S., Cecchetto G., Sophianopoulou V., Koukaki M., Scazzocchio C., Diallinas G. Transcription of purine transporter genes is activated during the isotropic growth phase of Aspergillus nidulans conidia. Mol. Microbiol. 2004, 52:205-216.
4. Amillis S., Hamari Z., Roumelioti K., Scazzocchio C., Diallinas G. Regulation of expression and kinetic modeling of substrate interactions of a uracil transporter in Aspergillus nidulans. Mol. Membr. Biol. 2007, 24:206-214.
5. Amillis S., Kosti V., Pantazopoulou A., Mikros E., Diallinas G. Mutational analysis and modeling reveal functionally critical residues in transmembrane segments 1 and 3 of the UapA transporter. J. Mol. Biol. 2011, 411:567-580.
6. Arst H.N., Scazzocchio C. Initiator constitutive mutation with an 'up-promoter' effect in Aspergillus nidulans. Nature 1975, 254:31-34.
7. Arst H.N., Scazzocchio C. A method for monitoring macromolecular synthesis and its use to study control of nuclear acid synthesis in Aspergillus nidulans. J. Gen. Microbiol. 1980, 118:443-454.
8. Barnett J.A. A history of research on yeasts 13. Active transport and the uptake of various metabolites. Yeast 2008, 25:689-731.
9. Darlington A.J., Scazzocchio C. Use of analogues and the substrate-sensitivity of mutants in analysis of purine uptake and breakdown in Aspergillus nidulans. J. Bacteriol. 1967, 93:937-940.
10. de Koning H.P., Bridges D.J., Burchmore R.J. Purine and pyrimidine transport in pathogenic protozoa: from biology to therapy. FEMS Microbiol. Rev. 2005, 29:987-1020.
11. Desai S.A. Ion and nutrient uptake by malaria parasite-infected erythrocytes. Cell Microbiol. 2012, 14:1003-1009.
12. Diallinas G. Allopurinol and xanthine use different translocation mechanisms and trajectories in the fungal UapA transporter. Biochimie 2013, 95:1755-1764.
13. Diallinas G., Gournas C. Structure-function relationships in the nucleobase-ascorbate transporter (NAT) family: lessons from model microbial genetic systems. Channels (Austin) 2008, 2:363-372.
14. Diallinas G., Scazzocchio C. A gene coding for the uric acid-xanthine permease of Aspergillus nidulans: inactivational cloning, characterization, and sequence of a cis-acting mutation. Genetics 1989, 122:341-350.
15. Diallinas G., Gorfinkiel L., Arst H.N., Cecchetto G., Scazzocchio C. Genetic and molecular characterization of a gene encoding a wide specificity purine permease of Aspergillus nidulans reveals a novel family of transporters conserved in prokaryotes and eukaryotes. J. Biol. Chem. 1995, 270:8610-8622.
16. Diallinas G., Valdez J., Sophianopoulou V., Rosa A., Scazzocchio C. Chimeric purine transporters of Aspergillus nidulans define a domain critical for function and specificity conserved in bacterial, plant and metazoan homologues. EMBO J. 1998, 17:3827-3837.
17. Elorza M.V., Arst H.N., Cove D.J., Scazzocchio C. Permeability properties of Aspergillus nidulans protoplasts. J. Bacteriol. 1969, 99:113-115.
18. Frillingos S. Insights to the evolution of Nucleobase-Ascorbate Transporters (NAT/NCS2 family) from the Cys-scanning analysis of xanthine permease XanQ. Int. J. Biochem. Mol. Biol. 2012, 3:250-272.
19. Gorfinkiel L., Diallinas G., Scazzocchio C. Sequence and regulation of the uapA gene encoding a uric acid-xanthine permease in the fungus Aspergillus nidulans. J. Biol. Chem. 1993, 268:23376-23381.
20. Goudela S., Karatza P., Koukaki M., Frillingos S., Diallinas G. Comparative substrate recognition by bacterial and fungal purine transporters of the NAT/NCS2 family. Mol. Membr. Biol. 2005, 22:263-275.
21. Goudela S., Tsilivi H., Diallinas G. Comparative kinetic analysis of AzgA and Fcy21p, prototypes of the two major fungal hypoxanthine-adenine-guanine transporter families. Mol. Membr. Biol. 2006, 23:291-303.
22. Goudela S., Reichard U., Amillis S., Diallinas G. Characterization and kinetics of the major purine transporters in Aspergillus fumigatus. Fungal Genet. Biol. 2008, 45:459-472.
23. Gournas C., Papageorgiou I., Diallinas G. The nucleobase-ascorbate transporter (NAT) family: genomics, evolution, structure-function relationships and physiological role. Mol. Biosyst. 2008, 4:404-416.
24. Grenson M., Hou C., Crabeel M. Multiplicity of the amino acid permeases in Saccharomyces cerevisiae. IV. Evidence for a general amino acid permease. J. Bacteriol. 1970, 103:770-777.
25. 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.
26. Jauniaux J.C., Grenson M. GAP1, the general amino acid permease gene of Saccharomyces cerevisiae. Nucleotide sequence, protein similarity with the other bakers yeast amino acid permeases, and nitrogen catabolite repression. Eur. J. Biochem. 1990, 190:39-44.
27. Kappy M.S., Metzenberg R.L. Multiple alterations in metabolite uptake in a mutant of Neurospora crassa. J. Bacteriol. 1967, 94:1629-1637.
28. Karatza P., Frillingos S. Cloning and functional characterization of two bacterial members of the NAT/NCS2 family in Escherichia coli. Mol. Membr. Biol. 2005, 22:251-261.
29. Kinghorn J.R., Pateman J.A. Mutations which affect amino acid transport in Aspergillus nidulans. J. Gen. Microbiol. 1975, 86:174-184.
30. Kosti V., Papageorgiou I., Diallinas G. Dynamic elements at both cytoplasmically and extracellularly facing sides of the UapA transporter selectively control the accessibility of substrates to their translocation pathway. J. Mol. Biol. 2010, 397:1132-1143.
31. Kosti V., Lambrinidis G., Myrianthopoulos V., Diallinas G., Mikros E. Identification of the substrate recognition and transport pathway in a eukaryotic member of the nucleobase-ascorbate transporter (NAT) family. PLoS ONE 2012, 7:e41939.
32. Lee T.J., Paulsen I., Karp P. Annotation-based inference of transporter function. Bioinformatics 2008, 24:259-267.
33. Leung J., Karachaliou M., Alves C., Diallinas G., Byrne B. Expression and purification of a functional uric acid-xanthine transporter (UapA). Protein Expr. Purif. 2010, 72:139-146.
34. Lu F., Li S., Jiang Y., Jiang J., Fan H., Lu G., Deng D., Dang S., Zhang X., Wang J., Yan N. Structure and mechanism of the uracil transporter UraA. Nature 2011, 472:243-246.
35. Pall M.L. Amino acid transport in Neurospora crassa. 3. Acidic amino acid transport. Biochim. Biophys. Acta 1970, 211:513-520.
36. Pall M.L. Amino acid transport in Neurospora crassa. IV. Properties and regulation of a methionine transport system. Biochim. Biophys. Acta 1971, 233:201-214.
37. 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.
38. Papageorgiou I., Gournas C., Vlanti A., Amillis S., Pantazopoulou A., Diallinas G. Specific interdomain synergy in the UapA transporter determines its unique specificity for uric acid among NAT carriers. J. Mol. Biol. 2008, 382:1121-1135.
39. Papakostas K., Frillingos S. Substrate selectivity of YgfU, a uric acid transporter from Escherichia coli. J. Biol. Chem. 2012, 287:15684-15695.
40. Pateman J.A., Dunn E., Kinghorn J.R., Forbes E.C. The transport of ammonium and methylammonium in wild type and mutant cells of Aspergillus nidulans. Mol. Gen. Genet. 1974, 133:225-236.
41. Pateman J.A., Kinghorn J.R., Dunn E. Regulatory aspects of L-glutamate transport in Aspergillus nidulans. J. Bacteriol. 1974, 119:534-542.
42. Polak A., Grenson M. Evidence for a common transport system for cytosine, adenine and hypoxanthine in Saccharomyces cerevisiae and Candida albicans. Eur. J. Biochem. 1973, 32:276-282.
43. Rubio-Texeira M., Van Zeebroeck G., Voordeckers K., Thevelein J.M. Saccharomyces cerevisiae plasma membrane nutrient sensors and their role in PKA signaling. FEMS Yeast Res. 2010, 10:134-149.
44. Scazzocchio, C., 1966. Studies on the Genetic Control of Purine Oxidation in Aspergillus nidulans. Ph.D. Thesis, University of Cambridge, Cambridge, UK.
45. Scazzocchio C., Arst H.N. The nature of an initiator constitutive mutation in Aspergillus nidulans. Nature 1978, 274:177-179.
46. Scazzocchio C., Gorton D.J. The regulation of purine breakdown. Genetics and Physiology of Aspergillus 1977, 255-265. Academic Press, New York, NY. J.E. Smith, J.A. Pateman (Eds.).
47. Sigel E. Use of Xenopus oocytes for the functional expression of plasma membrane proteins. J. Membr. Biol. 1990, 117:201-221.
48. Sophianopoulou V., Scazzocchio C. The proline transport protein of Aspergillus nidulans is very similar to amino acid transporters of Saccharomyces cerevisiae. Mol. Microbiol. 1989, 3:705-714.
49. Tazebay U.H., Sophianopoulou V., Cubero B., Scazzocchio C., Diallinas G. Post-transcriptional control and kinetic characterization of proline transport in germinating conidiospores of Aspergillus nidulans. FEMS Microbiol. Lett. 1995, 132:27-37.
50. Tazebay U.H., Sophianopoulou V., Scazzocchio C., Diallinas G. The gene encoding the major proline transporter of Aspergillus nidulans is upregulated during conidiospore germination and in response to proline induction and amino acid starvation. Mol. Microbiol. 1997, 24:105-117.
51. Thomas S.L., Bouyer G., Cueff A., Egée S., Glogowska E., Ollivaux C. Ion channels in human red blood cell membrane: actors or relicsα. Blood Cells Mol. Dis. 2011, 46:261-265.
52. Tsao T.F., Marzluf G.A. Genetic and metabolic regulation of purine base transport in Neurospora crassa. Mol. Gen. Genet. 1976, 149:347-355.
53. Unkles S.E., Hawker K.L., Grieve C., Campbell E.I., Montague P., Kinghorn J.R. CrnA encodes a nitrate transporter in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 1991, 88:204-208.
54. Vlanti A., Diallinas G. The Aspergillus nidulans FcyB cytosine-purine scavenger is highly expressed during germination and in reproductive compartments and is downregulated by endocytosis. Mol. Microbiol. 2008, 68:959-977.
55. Vlanti A., Amillis S., Koukaki M., Diallinas G. A novel-type substrate-selectivity filter and ER-exit determinants in the UapA purine transporter. J. Mol. Biol. 2006, 357:808-819.
56. Weiss J.N. The Hill equation revisited: uses and misuses. FASEB J. 1997, 11:835-841.
57. Wolfinbarger L., Kay W.W. Acidic amino acid transport in Neurospora crassa mycelia. Biochim. Biophys. Acta 1973, 330:335-343.
58. Yamamoto S., Inoue K., Murata T., Kamigaso S., Yasujima T., Maeda J.Y., Yoshida Y., Ohta K.Y., Yuasa H. Identification and functional characterization of the first nucleobase transporter in mammals: implication in the species difference in the intestinal absorption mechanism of nucleobases and their analogs between higher primates and other mammals. J. Biol. Chem. 2010, 285:6522-6531.