Role of mitochondrial carrier protein Mrs3/4 in iron acquisition and oxidative stress resistance of Cryptococcus neoformans

Medical Mycology

Volumn 40, Issue 6, 2002, Pages 581-591

  Nyhus, Karin J ^a   Ozaki, Luiz S ^c   Jacobson, Eric S ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Ferric reductase; Iron uptake; Mitochondrial iron uptake; Mitochondrial transporter; Oxidative stress

Indexed keywords

CARRIER PROTEIN; GLUTAMIC ACID; HYDROGEN PEROXIDE; IRON; IRON REDUCTASE; LYSINE; OXIDIZING AGENT; PROTEIN MRS3/4; UNCLASSIFIED DRUG;

ALLELE; ANTIBIOTIC RESISTANCE; ARTICLE; CRYPTOCOCCUS NEOFORMANS; EUKARYOTE; FUNGUS MUTANT; FUNGUS MUTATION; GENE DISRUPTION; GENE ISOLATION; GENE LIBRARY; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC STRAIN; IRON INTAKE; IRON METABOLISM; IRON RESTRICTION; IRON TRANSPORT; MIOSIS; MITOCHONDRIAL MEMBRANE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PROTEIN TRANSPORT; SENSITIVITY ANALYSIS; STOP CODON; WILD TYPE;

CRYPTOCOCCUS NEOFORMANS; EUKARYOTA; FILOBASIDIELLA NEOFORMANS; FUNGI; MYXOGASTRIA;

EID: 0036930220     PISSN: 13693786     EISSN: None     Source Type: Journal    
DOI: 10.1080/mmy.40.6.581.591     Document Type: Article

References (55)

1. Piot P, Bartos M, Ghys PD, Walker N, Schwartlander B. The global impact of AIDS. Nature 2001; 410: 968-973.
2. Buchanan KL, Murphy JW. What makes Cryptococcus neoformans a pathogen? Emerg. Infect. Dis. 1998; 4: 71-83.
3. Monari C, Casadevall A, Baldelli F, Francisci D, Piertrella D, Bistoni F, Vecchiarelli A. Normalization of anti-cryptococcal activity and interleukin-12 production after highly active antiretroviral therapy. AIDS 2000; 14: 2699-2708.
4. Hakim JG, Gangaidzo IT, Heyderman RS, Mielke J, Mushangi E, Taziwa A, Robertson VJ, Musvaire P, Mason PR. Impact of HIV infection on meningitis in Harare, Zimbabwe: A prospective study of 406 predominantly adult patients. AIDS 2000; 14: 1401-1407.
5. Boelaert JR, Weinberg GA, Weinberg ED. Altered iron metabolism in HIV infection: Mechanisms, possible consequences, and proposals for management. Infect. Agents. Dis. 1996; 5: 36-46.
6. Vartivarian SE, Anaissie EJ, Cowart RE, Sprigg HA, Tingler MJ, Jacobson ES. Regulation of cryptococcal capsular polysaccharide by iron. J. Infect. Diseases 1993; 167: 186-190.
7. Nyhus KJ, Wilborn AT, Jacobson ES. Ferric iron reduction by Cryptococcus neoformans. Infect. Immun. 1997; 65: 434-438.
8. Jacobson ES, Goodner AP, Nyhus KJ. Ferrous iron uptake in Cryptococcus neoformans. Infect. Immun. 1998; 66: 4169-4175.
9. Eide DJ. Metal ion transport in eukaryotic microorganisms: Insights from Saccharomyces cerevisiae. Adv. Microb. Physiol. 2000; 43: 1-38.
10. Jacobson ES, Petro MJ. Extracellular iron chelation in Cryptococcus neoformans. J. Med Veterin. Mycol. 1987; 25: 415-418.
11. Jacobson ES, Milhausen SM. 3-Hydroxyanthranilate in Cryptococcus neoformans: A secreted reductant which does not enable wood rot. Med. Mycol. (In press).
12. Ramanan N, Wang Y. A high-affinity iron permease essential for Candida albicans virulence. Science 2000; 288: 1062-1064.
13. Levitz SM. Macrophage-cryptococcus interactions. In: Zwilling, BS, Eisenstein, TK eds. Macrophage-Pathogen Interactions. New York: Marcel Dekker, 1994: 533-543.
14. Hamilton AJ, Holdom MD. Antioxidant systems in the pathogenic fungi of man and their role in virulence. Med. Mycol. 1999; 37: 375-389.
15. Rhodes JC, Polacheck I, Kwon-Chung KJ. Phenoloxidase activity and virulence in isogenic strains of Cryptococcus neoformans. Infect. Immun. 1982; 36: 1175-1184.
16. Chaturvedi V, Wong B, Newman SL. Oxidative killing of Cryptococcus neoformans by human neutrophils. J. Immunol. 1996; 156: 3836-3840.
17. Jacobson ES, Emery HS. Catecholamine uptake, melanization, and oxygen toxicity in Cryptococcus neoformans. J. Bacteriol. 1991; 173: 401-403.
18. Emery HS, Shelburne CP, Bowman JP, Fallon PG, Schulz CA, Jacobson ES. Genetic study of oxygen resistance and melanization in Cryptococcus neoformans. Infect. Immun. 1994; 62: 5694-5697.
19. Jacobson ES, Jenkins ND, Todd JM. Relationship between superoxide dismutase and melanin in a pathogenic fungus. Infect. Immun. 1994; 62: 4085-4086.
20. Stohs SJ, Bagchi D. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 1995; 18: 321-336.
21. Babcock M, De Silva D, Oaks R, Davis-Kaplan S, Jiralspong S, Montermini L, Pandolfo M, Kaplan J. Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science 1997; 276: 1709-1712.
22. Schilke B, Voisine C, Beinert H, Craig E. Evidence for a conserved system for iron metabolism in the mitochondria of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 1999; 96: 10206-10211.
23. Kispal G, Csere P, Guiard B, Lill R. The ABC transporter Atm1p is required for mitochondrial iron homeostasis. FEBS Lett 1997; 418: 346-350.
24. Nyhus KK, Jacobson ES. Genetic and physiologic characterization of ferric/cupric reductase constitutive mutants of Cryptococcus neoformans. Infect. Immun. 1999; 67: 2357-2365.
25. Moore TDE, Edman JC. The α-mating type locus of Cryptococcus neoformans contains a peptide pheromone gene. Mol. Cell Biol. 1993; 13: 1962-1970.
26. Fish WW. Rapid colorimetric micromethod for the quantitation of complexed iron in biological samples. Methods Enzymol. 1988; 158: 357-364.
27. Jacobson ES, Ayers DJ, Harrell AC, Nicholas CC. Genetic and phenotypic characterization of capsule mutants of Cryptococcus neoformans. J. Bacteriol. 1982; 25: 415-418.
28. Cruz MC, Fox DS, Heitman J. Calcineurin is required for hyphal elongation during mating and haploid fruiting in Cryptococcus neoformans. EMBO J 2001; 20: 1020-1032.
29. Wickes BL, Edman JC. Development of a transformation system for Cryptococcus neoformans. In: Maresca, B, Kobayashi, GS, eds. Molecular Biology of Pathogenic Fungi, New York: Telos Press, 1994: 309-311.
30. Casadevall A, Perfect J. Cryptococcus neoformans. Washington, DC: ASM Press, 1998: 394.
31. Thomson JD, Higgins DG, Gibson TJ. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994; 22: 4673-4680.
32. Sudarshan S, Davison RC, Heitman J, Alspaugh JA. Molecular analysis of the Cryptococcus neoformans ADE2 gene, a selectable marker for transformation and gene disruption. Fung. Genet. Biol. 1999;27:36-48.
33. Davidson RC, Cruz MC, Sia RAL, Allen B, Alspaugh JA, Heitman J, Gene disruption by biolistic transformation in serotype D strains of Cryptococcus neoformans. Fungal Genetics Biology 2000; 29: 38-48.
34. Wickes BL, Edman JC, The Cryptococcus neoformans GAL7 gene and its use as an inducible promoter. Mol. Microbiol. 1995; 16: 1099-1109.
35. Weisenberger G, Link TA, Von Ahsen U, Waldherr M, Schweyen RJ. MRS3 and MRS4, two suppressors of mtRNA splicing defects in yeast, are new members of the mitochondrial carrier family. J. Mol. Biol. 1991; 217: 23-27.
36. Catmull J, Miller DJ. cDNAs from Onchocerca sp encoding members of the MRS3/MRS4 class of mitochondrial solute carriers. Biochim. Biophys. Acta. 1996; 1282: 179-181.
37. Li F-Y, Nikali K, Gregan J, Leibiger I, Leibiger B, Schweyen R, Larsson C, Suomalainen A. Characterization of a novel human putative mitochondrial transporter homologous to the yeast mitochondrial RNA splicing proteins 3 and 4. FEBS Lett 2001; 494: 79-84.
38. Gimeno RE, Dembski M, Weng X, Deng N, Shyjan AW, Gimeno CJ, Iris F, Ellis SJ, Woolf EA, Tartaglia LA. Cloning and characterization of an uncoupling protein homolog: A potential molecular mediator of human thermogenesis. Diabetes (1997) 46: 900-906.
39. Jensen LT, Culotta VC. Role of Saccharomyces cerevisiae ISA1 and ISA2 in iron homeostasis. Mol. Cell Biol. 2000; 20: 3918-3927.
40. Fincham JRS, Day PR, Radford A. Fungal Genetics. Berkeley: University of California Press, 1979.
41. Schmidt C, Sollner T, Schweyen RJ. Nuclear suppression of a mitochondrial RNA splice defect: Nucleotide sequence and disruption of the MRS3 gene. Mol. Gen. Genet. 1987; 210: 145-152.
42. Walker JE, Runswick MJ. The mitochondrial transport protein superfamily. J. Bioenerg. Biomembr. 1993; 25: 435-446.
43. Stearman R, Yuan DS, Yamaguchi-Iwai Y, Klausner RD, Dancis A. A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science 1996; 271: 1552-1557.
44. Rogers EE, Eide, DJ, Guerinot ML. Altered selectivity in an Arabidopsis metal transporter. Proc Natl Acad Sci USA 2000; 97: 12356-12360.
45. Li, L, Kaplan, J. Characterization of two homologous yeast genes that encode mitochondrial iron transporters. J Biol Chem 1997; 272: 28485-28493.
46. Mühlenhoff, U, Lill, R. Biogenesis of iron-sulfur proteins in eukaryotes: A novel task of mitochondria that is inherited from bacteria. Biochim Biophys Acta 2000; 1459: 370-382.
47. Li, J, Saxena, S, Pain, D, Dancis, A. Adrenodoxin reductase homolog (Arh1p) of yeast mitochondria required for iron homeostasis. J Biol Chem 2001; 276: 1503-1509.
48. Adamec, J, Rusnak, F, Owen, W G, Naylor, S, Benson, LM, Gacy, AM, Isaya, G. Iron-dependent self-assembly of recombinant yeast frataxin: Implications for Friedreich ataxia. Am J Hum Genet 2000; 67: 549-562.
49. Radisky, DC, Babcock, MC, Kaplan, J. The yeast frataxin homologue mediates mitochondrial iron efflux. J Biol Chem 1999; 274: 4497-4499.
50. Sluse, FE, Jarmuszkiewicz, W. Alternative oxidase in the branched mitochondrial respiratory network: An overview on structure, function, regulation, and role. Braz J Med Biol Res 1998; 31: 733-747.
51. Maxwell, DP, Wang, Y, McIntosh, L. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 1999; 96: 8271-8276.
52. Nyhus, KJ, Jacobson, ES. Oxy2 is a master control gene for copper uptake and melanin synthesis in Cryptococcus neoformans. Manuscript submitted.
53. Dancis, A, Yuan, DS, Haile, D, Askwith, C, Eide, D, Moehle, C, Kaplan, J, Klausner, RD. Molecular characterization of a copper transport protein in S. cerevisiae: An unexpected role for copper in iron transport. Cell 1994; 76: 3934-3402.
54. Liu, L, Tewari, RP, Williamson, PR. Laccase protects Cryptococcus neoformans from antifungal activity of alveolar macrophages. Infect Immun 1999; 67: 6034-6039.
55. Polacheck, I, Hearing, VJ, Kwon-Chung, KJ. Biochemical studies of phenoloxidase and utilization of catecholamines in Cryptococcus neoformans. J Bacteriol 1982; 150: 1212-1220.