Importance of mitochondria in survival of Cryptococcus neoformans under low oxygen conditions and tolerance to cobalt chloride

PLoS Pathogens

Volumn 4, Issue 9, 2008, Pages

  Ingavale, Susham S ^a   Chang, Yun C ^a   Lee, Hyeseung ^a   McClelland, Carol M ^a   Leong, Madeline L ^a   Kwon Chung, Kyung J ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COBALT CHLORIDE; DNA; IRON; REACTIVE OXYGEN METABOLITE; STEROL; COBALT;

ARTICLE; BREATHING RATE; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; DNA SCREENING; FUNGUS GROWTH; FUNGUS ISOLATION; GENE EXPRESSION; GENE MUTATION; HOMEOSTASIS; HYPOXIA; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; OXYGEN SENSING; RESPIRATORY SYSTEM; SURVIVAL; UBIQUITINATION; WILD TYPE; ADAPTATION; ANAEROBIC GROWTH; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; METABOLISM; MICROBIAL VIABILITY; PHYSIOLOGY;

FILOBASIDIELLA NEOFORMANS; FUNGI;

ADAPTATION, PHYSIOLOGICAL; ANAEROBIOSIS; COBALT; CRYPTOCOCCUS NEOFORMANS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; METABOLIC NETWORKS AND PATHWAYS; MICROBIAL VIABILITY; MITOCHONDRIA; REACTIVE OXYGEN SPECIES;

EID: 53049099032     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000155     Document Type: Article

References (69)

1. Kwon-Chung KJ, Bennett JE (1992) Medical Mycology. Philadelphia, PA: Lea & Febiger.
2. Lazera MS, Pires FD, Camillo-Coura L, Nishikawa MM, Bezerra CC, et al. (1996) Natural habitat of Cryptococcus neoformans var. neoformans in decaying wood forming hollows in living trees. J Med Vet Mycol 34: 127-131.
3. Nishikawa MM, Sant'Anna OD, Lazera MS, Wanke B (1996) Use of D-proline assimilation and CGB medium for screening Brazilian Cryptococcus neoformans isolates. J Med Vet Mycol 34: 365-366.
4. Odds FC, De Backer T, Dams G, Vranckx L, Woestenborghs F (1995) Oxygen as limiting nutrient for growth of Cryptococcus neoformans. J Clin Microbiol 33: 995-997.
5. Erecinska M, Silver IA (2001) Tissue oxygen tension and brain sensitivity to hypoxia. Respir Physiol 128: 263-276.
6. Goldberg MA, Dunning SP, Bunn HF (1988) Regulation of the erythropoietin gene: evidence that the oxygen sensor is a heme protein. Science 242: 1412-1415.
7. Semenza GL (2004) Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology (Bethesda) 19: 176-182.
8. Wang GL, Semenza GL (1993) Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia. J Biol Chem 268: 21513-21518.
9. Bruick RK, McKnight SL (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294: 1337-1340.
10. Goldberg MA, Glass GA, Cunningham JM, Bunn HF (1987) The regulated expression of erythropoietin by two human hepatoma cell lines. Proc Natl Acad Sci U S A 84: 7972-7976.
11. Wang G, Hazra TK, Mitra S, Lee HM, Englander EW (2000) Mitochondrial DNA damage and a hypoxic response are induced by CoCl(2) in rat neuronal PC12 cells. Nucleic Acids Res 28: 2135-2140.
12. Grasselli F, Basini G, Bussolati S, Bianco F (2005) Cobalt chloride, a hypoxia-mimicking agent, modulates redox status and functional parameters of cultured swine granulosa cells. Reprod Fertil Dev 17: 715-720.
13. Wang GL, Semenza GL (1993) General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci U S A 90: 4304-4308.
14. Semenza GL (2007) Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1. Biochem J 405: 1-9.
15. Healy WB, Cheng SC, Mc EW (1955) Metal toxicity and iron deficiency effects on enzymes in Neurospora. Arch Biochem 54: 206-214.
16. Padmanaban G, Sarma PS (1966) Cobalt toxicity and iron metabolism in Neurospora crassa. Biochem J 98: 330-334.
17. Lindegren CC, Nagai S, Nagai H (1958) Induction of respiratory deficiency in yeast by manganese, copper, cobalt and nickel. Nature 182: 446-448.
18. Lee H, Bien CM, Hughes AL, Espenshade PJ, Kwon-Chung KJ, et al. (2007) Cobalt chloride, a hypoxia-mimicking agent, targets sterol synthesis in the pathogenic fungus Cryptococcus neoformans. Mol Microbiol 65: 1018-1033.
19. Chang YC, Bien CM, Lee H, Espenshade PJ, Kwon-Chung KJ (2007) Sre1p, a regulator of oxygen sensing and sterol homeostasis, is required for virulence in Cryptococcus neoformans. Mol Microbiol 64: 614-629.
20. McClelland CM, Chang YC, Kwon-Chung KJ (2005) High frequency transformation of Cryptococcus neoformans and Cryptococcus gattii by Agrobacterium tumefaciens. Fungal Genet Biol 42: 904-913.
21. Chang YC, Kwon-Chung KJ (1994) Complementation of a capsule-deficient mutation of Cryptococcus neoformans restores its virulence. Mol Cell Biol 14: 4912-4919.
22. Toffaletti DL, Rude TH, Johnston SA, Durack DT, Perfect JR (1993) Gene transfer in Cryptococcus neoformans by use of biolistic delivery of DNA. J Bacteriol 175: 1405-1411.
23. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121.
24. Idnurm A, Reedy JL, Nussbaum JC, Heitman J (2004) Cryptococcus neoformans virulence gene discovery through insertional mutagenesis. Eukaryot Cell 3: 420-429.
25. Dingle JT, Heath JC, Webb M, Daniel M (1962) The biological action of cobalt and other metals. II. The mechanism of the respiratory inhibition produced by cobalt in mammalian tissues. Biochim Biophys Acta 65: 34-46.
26. Karovic O, Tonazzini I, Rebola N, Edstrom E, Lovdahl C, et al. (2007) Toxic effects of cobalt in primary cultures of mouse astrocytes: Similarities with hypoxia and role of HIF-1[alpha]. Biochemical Pharmacology 73: 694-708.
27. Hervouet E, Pecina P, Demont J, Vojtiskova A, Simonnet H, et al. (2006) Inhibition of cytochrome c oxidase subunit 4 precursor processing by the hypoxia mimic cobalt chloride. Biochem Biophys Res Commun 344: 1086-1093.
28. Lindegren CC, Miller PM (1969) Cobalt as a vital stain for yeast mitochondria in squash preparations. Can J Genet Cytol 11: 987-992.
29. Gakh O, Cavadini P, Isaya G (2002) Mitochondrial processing peptidases. Biochim Biophys Acta 1592: 63-77.
30. Ackerman SH, Tzagoloff A (2005) Function, structure, and biogenesis of mitochondrial ATP synthase. Prog Nucleic Acid Res Mol Biol 80: 95-133.
31. Lawson JE, Douglas MG (1988) Separate genes encode functionally equivalent ADP/ATP carrier proteins in Saccharomyces cerevisiae. Isolation and analysis of AAC2. J Biol Chem 263: 14812-14818.
32. Fiore C, Trezeguet V, Le Saux A, Roux P, Schwimmer C, et al. (1998) The mitochondrial ADP/ATP carrier: structural, physiological and pathological aspects. Biochimie 80: 137-150.
33. Entelis N, Brandina I, Kamenski P, Krasheninnikov IA, Martin RP, et al. (2006) A glycolytic enzyme, enolase, is recruited as a cofactor of tRNA targeting toward mitochondria in Saccharomyces cerevisiae. Genes Dev 20: 1609-1620.
34. Entelis NS, Krasheninnikov IA, Martin RP, Tarassov IA (1996) Mitochondrial import of a yeast cytoplasmic tRNA (Lys): possible roles of aminoacylation and modified nucleosides in subcellular partitioning. FEBS Lett 384: 38-42.
35. Sturley SL (2000) Conservation of eukaryotic sterol homeostasis: new insights from studies in budding yeast. Biochim Biophys Acta 1529: 155-163.
36. Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18: 321-336.
37. Leonard S, Gannett PM, Rojanasakul Y, Schwegler-Berry D, Castranova V, et al. (1998) Cobalt-mediated generation of reactive oxygen species and its possible mechanism. J Inorg Biochem 70: 239-244.
38. Jamieson DJ (1998) Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14: 1511-1527.
39. Berlett BS, Stadtman ER (1997) Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272: 20313-20316.
40. Harvey BH (2000) Acid-dependent dismutation of nitrogen oxides may be a critical source of nitric oxide in human macrophages. Medical Hypotheses 54: 829-831.
41. Jolly WL (1964) The inorganic chemistry of nitrogen. New York: W.A. Benjamin, Inc. pp 68-79.
42. De Groote MA, Fang FC (1995) NO inhibitions: antimicrobial properties of nitric oxide. Clin Infect Dis 21 Suppl 2: S162-165.
43. Drapier JC (1997) Interplay between NO and [Fe-S] clusters: relevance to biological systems. Methods 11: 319-329.
44. Joseph-Horne T, Hollomon DW, Wood PM (2001) Fungal respiration: a fusion of standard and alternative components. Biochim Biophys Acta 1504: 179-195.
45. Cocheme HM, Murphy MP (2008) Complex I is the major site of mitochondrial superoxide production by paraquat. J Biol Chem 283: 1786-1798.
46. Penninckx MJ, Elskens MT (1993) Metabolism and functions of glutathione in micro-organisms. Adv Microb Physiol 34: 239-301.
47. Freeman ML, Huntley SA, Meredith MJ, Senisterra GA, Lepock J (1997) Destabilization and denaturation of cellular protein by glutathione depletion. Cell Stress Chaperones 2: 191-198.
48. Moore AL, Siedow JN (1991) The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria. Biochim Biophys Acta 1059: 121-140.
49. Veiga A, Arrabaca JD, Loureiro-Dias MC (2003) Cyanide-resistant respiration, a very frequent metabolic pathway in yeasts. FEMS Yeast Res 3: 239-245.
50. Zitomer RS, Lowry CV (1992) Regulation of gene expression by oxygen in Saccharomyces cerevisiae. Microbiol Rev 56: 1-11.
51. Toledano MB, Delaunay A, Biteau B, Spector D, Azevedo D (2003) Oxidative stress responses in yeast. In: Hohmann S, Mager WH, eds. Topics in current genetics Springer. pp 242-303.
52. Hamilton AJ, Holdom MD (1999) Antioxidant systems in the pathogenic fungi of man and their role in virulence. Med Mycol 37: 375-389.
53. Grant CM, MacIver FH, Dawes IW (1997) Mitochondrial function is required for resistance to oxidative stress in the yeast Saccharomyces cerevisiae. FEBS Lett 410: 219-222.
54. St-Pierre J, Buckingham JA, Roebuck SJ, Brand MD (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 277: 44784-44790.
55. Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, et al. (2000) Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem 275: 25130-25138.
56. Guzy RD, Mack MM, Schumacker PT (2007) Mitochondrial complex III is required for hypoxia-induced ROS production and gene transcription in yeast. Antioxid Redox Signal 9: 1317-1328.
57. Cash TP, Pan Y, Simon MC (2007) Reactive oxygen species and cellular oxygen sensing. Free Radic Biol Med 43: 1219-1225.
58. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, et al. (1998) Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci U S A 95: 11715-11720.
59. Brandina I, Smirnov A, Kolesnikova O, Entelis N, Krasheninnikov IA, et al. (2007) tRNA import into yeast mitochondria is regulated by the ubiquitinproteasome system. FEBS Lett 581: 4248-4254.
60. Altmann K, Westermann B (2005) Role of essential genes in mitochondrial morphogenesis in Saccharomyces cerevisiae. Mol Biol Cell 16: 5410-5417.
61. Pearce DA, Sherman F (1997) Differential ubiquitin-dependent degradation of the yeast apo-cytochrome c isozymes. J Biol Chem 272: 31829-31836.
62. Martin CE, Oh CS, Kandasamy P, Chellapa R, Vemula M (2002) Yeast desaturases. Biochem Soc Trans 30: 1080-1082.
63. Sastry KS, Adiga PR, Venkatasubramanyam V, Sarma PS (1962) Interrelationships in trace-element metabolism in metal toxicities in Neurospora crassa. Biochem J 85: 486-491.
64. Padmanaban G, Sarma PS (1964) A New Iron-Binding Compound from Cobalt-Toxic Cultures of Neurospora Crassa. Arch Biochem Biophys 108: 362-363.
65. Stadler JA, Schweyen RJ (2002) The yeast iron regulon is induced upon cobalt stress and crucial for cobalt tolerance. J Biol Chem 277: 39649-39654.
66. Sinclair P, Gibbs AH, Sinclair JF, de Matteis F (1979) Formation of cobalt protoporphyrin in the liver of rats. A mechanism for the inhibition of liver haem biosynthesis by inorganic cobalt. Biochem J 178: 529-538.
67. Sinclair PR, Sinclair JF, Bonkowsky HL, Gibbs AH, De Matteis F (1982) Formation of cobalt protoporphyrin by chicken hepatocytes in culture. Relationship to decrease of 5-aminolaevulinate synthase caused by cobalt. Biochem Pharmacol 31: 993-999.
68. Kwast KE, Burke PV, Poyton RO (1998) Oxygen sensing and the transcriptional regulation of oxygen-responsive genes in yeast. J Exp Biol 201: 1177-1195.
69. Jung WH, Sham A, Lian T, Singh A, Kosman DJ, et al. (2008) Iron source preference and regulation of iron uptake in Cryptococcus neoformans. PLoS Pathog 4: e45. doi:10.1371/journal.ppat.1000045.