Redundant catalases detoxify phagocyte reactive oxygen and facilitate Histoplasma capsulatum pathogenesis

Infection and Immunity

Volumn 81, Issue 7, 2013, Pages 2334-2346

  Holbrook, Eric D ^a   Smolnycki, Katherine A ^a   Youseff, Brian H ^a,b   Rappleye, Chad A ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; CATALASE B; CATALASE P; PEROXIDE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; HISTOPLASMOSIS; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PHAGOCYTE; PRIORITY JOURNAL;

ANIMALS; CATALASE; ENZYME ACTIVATION; FUNGAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; HISTOPLASMA; HISTOPLASMOSIS; HUMANS; HYDROGEN PEROXIDE; MALE; MICE; MICE, INBRED C57BL; NEUTROPHILS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RNA, FUNGAL; SUPEROXIDE DISMUTASE; VIRULENCE;

EID: 84879438579     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00173-13     Document Type: Article

References (79)

1. DeLeo FR, Allen LA, Apicella M, Nauseef WM. 1999. NADPH oxidase activation and assembly during phagocytosis. J. Immunol. 163:6732-6740.
2. Fang FC. 2011. Antimicrobial actions of reactive oxygen species. mBio 2(5):00141-11.
3. Cohen MS, Isturiz RE, Malech HL, Root RK, Wilfert CM, Gutman L, Buckley RH. 1981. Fungal infection in chronic granulomatous disease. The importance of the phagocyte in defense against fungi. Am. J. Med. 71:59-66.
4. Soler-Palacin P, Margareto C, Llobet P, Asensio O, Hernandez M, Caragol I, Espanol T. 2007. Chronic granulomatous disease in pediatric patients: 25 years of experience. Allergol. Immunopathol. (Madr.) 35:83-89.
5. Fairfield AS, Abosch A, Ranz A, Eaton JW, Meshnick SR. 1988. Oxidant defense enzymes of Plasmodium falciparum. Mol. Biochem. Parasitol. 30: 77-82.
6. Cabiscol E, Tamarit J, Ros J. 2000. Oxidative stress in bacteria and protein damage by reactive oxygen species. Int. Microbiol. 3:3-8.
7. Hamilton AJ, Holdom MD. 1999. Antioxidant systems in the pathogenic fungi of man and their role in virulence. Med. Mycol. 37:375-389.
8. Liu L, Tewari RP, Williamson PR. 1999. Laccase protects Cryptococcus neoformans from antifungal activity of alveolar macrophages. Infect. Immun. 67:6034-6039.
9. Ruijter GJ, Bax M, Patel H, Flitter SJ, van de Vondervoort PJ, de Vries RP, vanKuyk PA, Visser J. 2003. Mannitol is required for stress tolerance in Aspergillus niger conidiospores. Eukaryot. Cell 2:690-698.
10. Alp S. 2010. Melanin and its role on the virulence of Cryptococcus neoformans. Mikrobiyol. Bul. 44:519-526. (In Turkish.)
11. Garre V, Tenberge KB, Eising R. 1998. Secretion of a fungal extracellular catalase by Claviceps purpurea during infection of rye: putative role in pathogenicity and suppression of host defense. Phytopathology 88:744-753.
12. Fang FC, DeGroote MA, Foster JW, Baumler AJ, Ochsner U, Testerman T, Bearson S, Giard JC, Xu Y, Campbell G, Laessig T. 1999. Virulent Salmonella typhimurium has two periplasmic Cu, Zn-superoxide dismutases. Proc. Natl. Acad. Sci. U. S. A. 96:7502-7507.
13. Zancope-Oliveira RM, Reiss E, Lott TJ, Mayer LW, Deepe GS, Jr. 1999. Molecular cloning, characterization, and expression of the M antigen of Histoplasma capsulatum. Infect. Immun. 67:1947-1953.
14. Zhu X, Gibbons J, Garcia-Rivera J, Casadevall A, Williamson PR. 2001. Laccase of Cryptococcus neoformans is a cell wall-associated virulence factor. Infect. Immun. 69:5589-5596.
15. Frohner IE, Bourgeois C, Yatsyk K, Majer O, Kuchler K. 2009. Candida albicans cell surface superoxide dismutases degrade host-derived reactive oxygen species to escape innate immune surveillance. Mol. Microbiol. 71:240-252.
16. Zhang N, Zhang S, Borchert S, Richardson K, Schmid J. 2011. High levels of a fungal superoxide dismutase and increased concentration of a PR-10 plant protein in associations between the endophytic fungus Neotyphodium lolii and ryegrass. Mol. Plant Microbe Interact. 24:984-992.
17. Youseff BH, Holbrook ED, Smolnycki KA, Rappleye CA. 2012. Extracellular superoxide dismutase protects Histoplasma yeast cells from hostderived oxidative stress. PLoS Pathog. 8:e1002713.
18. Zamocky M, Droghetti E, Bellei M, Gasselhuber B, Pabst M, Furtmuller PG, Battistuzzi G, Smulevich G, Obinger C. 2012. Eukaryotic extracellular catalase-peroxidase from Magnaporthe grisea-biophysical/ chemical characterization of the first representative from a novel phytopathogenic KatG group. Biochimie 94:673-683.
19. Edwards LB, Acquaviva FA, Livesay VT, Cross FW, Palmer CE. 1969. An atlas of sensitivity to tuberculin, PPD-B, and histoplasmin in the United States. Am. Rev. Respir. Dis. 99(Suppl):1-132.
20. Ajello L. 1971. The medical mycological iceberg. HSMHA Health Rep. 86:437-448.
21. Mukhopadhyay S, Katzenstein AL. 2010. Biopsy findings in acute pulmonary histoplasmosis: unusual histologic features in 4 cases mimicking lymphomatoid granulomatosis. Am. J. Surg. Pathol. 34:541-546.
22. Kroetz DN, Deepe GS. 2012. The role of cytokines and chemokines in Histoplasma capsulatum infection. Cytokine 58:112-117.
23. Eissenberg LG, Goldman WE. 1987. Histoplasma capsulatum fails to trigger release of superoxide from macrophages. Infect. Immun. 55:29-34.
24. Wolf JE, Kerchberger V, Kobayashi GS, Little JR. 1987. Modulation of the macrophage oxidative burst by Histoplasma capsulatum. J. Immunol. 138:582-586.
25. Schnur RA, Newman SL. 1990. The respiratory burst response to Histoplasma capsulatum by human neutrophils. Evidence for intracellular trapping of superoxide anion. J. Immunol. 144:4765-4772.
26. Kurita N, Brummer E, Yoshida S, Nishimura K, Miyaji M. 1991. Antifungal activity of murine polymorphonuclear neutrophils against Histoplasma capsulatum. J. Med. Vet. Mycol. 29:133-143.
27. Kurita N, Terao K, Brummer E, Ito E, Nishimura K, Miyaji M. 1991. Resistance of Histoplasma capsulatum to killing by human neutrophils. Evasion of oxidative burst and lysosomal-fusion products. Mycopathologia 115:207-213.
28. Johnson CH, Klotz MG, York JL, Kruft V, McEwen JE. 2002. Redundancy, phylogeny and differential expression of Histoplasma capsulatum catalases. Microbiology 148:1129-1142.
29. Pine L, Malcolm GB, Gross H, Gray SB. 1978. Evaluation of purified H and M antigens of histoplasmin as reagents in the complement fixation test. Sabouraudia 16:257-269.
30. Hamilton AJ, Bartholomew MA, Figueroa J, Fenelon LE, Hay RJ. 1990. Evidence that theMantigen of Histoplasma capsulatum var. capsulatum is a catalase which exhibits cross-reactivity with other dimorphic fungi. J. Med. Vet. Mycol. 28:479-485.
31. Kauffman CA. 2007. Histoplasmosis: a clinical and laboratory update. Clin. Microbiol. Rev. 20:115-132.
32. Guimaraes AJ, Hamilton AJ, de M Guedes HL, Nosanchuk JD, Zancope-Oliveira RM. 2008. Biological function and molecular mapping of M antigen in yeast phase of Histoplasma capsulatum. PLoS One 3:e3449.
33. Reiss E, Hutchinson H, Pine L, Ziegler DW, Kaufman L. 1977. Solidphase competitive-binding radioimmunoassay for detecting antibody to the M antigen of histoplasmin. J. Clin. Microbiol. 6:598-604.
34. Albuquerque PC, Nakayasu ES, Rodrigues ML, Frases S, Casadevall A, Zancope-Oliveira RM, Almeida IC, Nosanchuk JD. 2008. Vesicular transport in Histoplasma capsulatum: an effective mechanism for transcell wall transfer of proteins and lipids in ascomycetes. Cell. Microbiol. 10:1695-1710.
35. Worsham PL, Goldman WE. 1988. Quantitative plating of Histoplasma capsulatum without addition of conditioned medium or siderophores. J. Med. Vet. Mycol. 26:137-143.
36. Woods JP, Heinecke EL, Goldman WE. 1998. Electrotransformation and expression of bacterial genes encoding hygromycin phosphotransferase and beta-galactosidase in the pathogenic fungus Histoplasma capsulatum. Infect. Immun. 66:1697-1707.
37. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3:1101-1108.
38. Gavrilin MA, Bouakl IJ, Knatz NL, Duncan MD, Hall MW, Gunn JS, Wewers MD. 2006. Internalization and phagosome escape required for Francisella to induce human monocyte IL-1beta processing and release. Proc. Natl. Acad. Sci. U. S. A. 103:141-146.
39. Sebghati TS, Engle JT, Goldman WE. 2000. Intracellular parasitism by Histoplasma capsulatum: fungal virulence and calcium dependence. Science 290:1368-1372.
40. Kouoh F, Gressier B, Luyckx M, Brunet C, Dine T, Ballester L, Cazin M, Cazin JC. 2000. A simple method for isolating human and rabbit polymorphonuclear neutrophils (PMNs). Biol. Pharm. Bull. 23:1382-1383.
41. Nauseef WM. 2007. Isolation of human neutrophils from venous blood. Methods Mol. Biol. 412:15-20.
42. Schlesinger LS. 1993. Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors. J. Immunol. 150:2920-2930.
43. Holbrook ED, Edwards JA, Youseff BH, Rappleye CA. 2011. Definition of the extracellular proteome of pathogenic-phase Histoplasma capsulatum. J. Proteome Res. 10:1929-1943.
44. Howard DH. 1983. Studies on the catalase of Histoplasma capsulatum. Infect. Immun. 39:1161-1166.
45. Newman SL, Bullock WE. 1994. Interaction of Histoplasma capsulatum yeasts and conidia with human and animal macrophages. Immunol. Ser. 60:517-532.
46. Brummer E, Kurita N, Yoshida S, Nishimura K, Miyaji M. 1991. Killing of Histoplasma capsulatum by gamma-interferon-activated human monocyte-derived macrophages: evidence for a superoxide anion-dependent mechanism. J. Med. Microbiol. 35:29-34.
47. Fleischmann J, Wu-Hsieh B, Howard DH. 1990. The intracellular fate of Histoplasma capsulatum in human macrophages is unaffected by recombinant human interferon-gamma. J. Infect. Dis. 161:143-145.
48. Rappleye CA, Eissenberg LG, Goldman WE. 2007. Histoplasma capsulatum alpha-(1,3)-glucan blocks innate immune recognition by the betaglucan receptor. Proc. Natl. Acad. Sci. U. S. A. 104:1366-1370.
49. Kozel TR, Gotschlich EC. 1982. The capsule of Cryptococcus neoformans passively inhibits phagocytosis of the yeast by macrophages. J. Immunol. 129:1675-1680.
50. Vecchiarelli A, Retini C, Pietrella D, Monari C, Tascini C, Beccari T, Kozel TR. 1995. Downregulation by cryptococcal polysaccharide of tumor necrosis factor alpha and interleukin-1 beta secretion from human monocytes. Infect. Immun. 63:2919-2923.
51. Hohl TM, Feldmesser M, Perlin DS, Pamer EG. 2008. Caspofungin modulates inflammatory responses to Aspergillus fumigatus through stage-specific effects on fungal beta-glucan exposure. J. Infect. Dis. 198: 176-185.
52. Leal SM, Jr, Cowden S, Hsia YC, Ghannoum MA, Momany M, Pearlman E. 2010. Distinct roles for Dectin-1 and TLR4 in the pathogenesis of Aspergillus fumigatus keratitis. PLoS Pathog. 6:e1000976.
53. Wysong DR, Christin L, Sugar AM, Robbins PW, Diamond RD. 1998. Cloning and sequencing of a Candida albicans catalase gene and effects of disruption of this gene. Infect. Immun. 66:1953-1961.
54. Giles SS, Stajich JE, Nichols C, Gerrald QD, Alspaugh JA, Dietrich F, Perfect JR. 2006. The Cryptococcus neoformans catalase gene family and its role in antioxidant defense. Eukaryot. Cell 5:1447-1459.
55. Calera JA, Paris S, Monod M, Hamilton AJ, Debeaupuis JP, Diaquin M, Lopez-Medrano R, Leal F, Latge JP. 1997. Cloning and disruption of the antigenic catalase gene of Aspergillus fumigatus. Infect. Immun. 65:4718-4724.
56. Soler-Garcia AA, Jerse AE. 2007. Neisseria gonorrhoeae catalase is not required for experimental genital tract infection despite the induction of a localized neutrophil response. Infect. Immun. 75:2225-2233.
57. Buchmeier NA, Libby SJ, Xu Y, Loewen PC, Switala J, Guiney DG, Fang FC. 1995. DNA repair is more important than catalase for Salmonella virulence in mice. J. Clin. Invest. 95:1047-1053.
58. Vergauwen B, Herbert M, Van Beeumen JJ. 2006. Hydrogen peroxide scavenging is not a virulence determinant in the pathogenesis of Haemophilus influenzae type b strain Eagan. BMC Microbiol. 6:3.
59. Paris S, Wysong D, Debeaupuis JP, Shibuya K, Philippe B, Diamond RD, Latge JP. 2003. Catalases of Aspergillus fumigatus. Infect. Immun. 71:3551-3562.
60. Cuellar-Cruz M, Briones-Martin-del-Campo M, Canas-Villamar I, Montalvo-Arredondo J, Riego-Ruiz L, Castano I, De Las Penas A. 2008. High resistance to oxidative stress in the fungal pathogen Candida glabrata is mediated by a single catalase, Cta1p, and is controlled by the transcription factors Yap1p, Skn7p, Msn2p, and Msn4p. Eukaryot. Cell 7:814-825.
61. Tanabe S, Ishii-Minami N, Saitoh K, Otake Y, Kaku H, Shibuya N, Nishizawa Y, Minami E. 2011. The role of catalase-peroxidase secreted by Magnaporthe oryzae during early infection of rice cells. Mol. Plant Microbe Interact. 24:163-171.
62. Nakagawa Y. 2008. Catalase gene disruptant of the human pathogenic yeast Candida albicans is defective in hyphal growth, and a catalasespecific inhibitor can suppress hyphal growth of wild-type cells. Microbiol. Immunol. 52:16-24.
63. Missall TA, Pusateri ME, Lodge JK. 2004. Thiol peroxidase is critical for virulence and resistance to nitric oxide and peroxide in the fungal pathogen, Cryptococcus neoformans. Mol. Microbiol. 51:1447-1458.
64. Chaves GM, Bates S, Maccallum DM, Odds FC. 2007. Candida albicans GRX2, encoding a putative glutaredoxin, is required for virulence in a murine model. Genet. Mol. Res. 6:1051-1063.
65. Giles SS, Perfect JR, Cox GM. 2005. Cytochrome c peroxidase contributesto the antioxidant defense of Cryptococcus neoformans. Fungal Genet. Biol. 42:20-29.
66. Akhter S, McDade HC, Gorlach JM, Heinrich G, Cox GM, Perfect JR. 2003. Role of alternative oxidase gene in pathogenesis of Cryptococcus neoformans. Infect. Immun. 71:5794-5802.
67. Ruiz OH, Gonzalez A, Almeida AJ, Tamayo D, Garcia AM, Restrepo A, McEwen JG. 2011. Alternative oxidase mediates pathogen resistance in Paracoccidioides brasiliensis infection. PLoS Negl. Trop. Dis. 5:e1353.
68. Chaturvedi V, Wong B, Newman SL. 1996. Oxidative killing of Cryptococcus neoformans by human neutrophils. Evidence that fungal mannitol protects by scavenging reactive oxygen intermediates. J. Immunol. 156: 3836-3840.
69. Zaragoza O, Chrisman CJ, Castelli MV, Frases S, Cuenca-Estrella M, Rodriguez-Tudela JL, Casadevall A. 2008. Capsule enlargement in Cryptococcus neoformans confers resistance to oxidative stress suggesting a mechanism for intracellular survival. Cell. Microbiol. 10:2043-2057.
70. Alvarez-Peral FJ, Zaragoza O, Pedreno Y, Arguelles JC. 2002. Protective role of trehalose during severe oxidative stress caused by hydrogen peroxide and the adaptive oxidative stress response in Candida albicans. Microbiology 148:2599-2606.
71. Martinez-Esparza M, Aguinaga A, Gonzalez-Parraga P, Garcia-Penarrubia P, Jouault T, Arguelles JC. 2007. Role of trehalose in resistance to macrophage killing: study with a tps1/tps1 trehalose-deficient mutant of Candida albicans. Clin. Microbiol. Infect. 13:384-394.
72. Gonzalez-Parraga P, Hernandez JA, Arguelles JC. 2003. Role of antioxidant enzymatic defences against oxidative stress H(2)O(2) and the acquisition of oxidative tolerance in Candida albicans. Yeast 20:1161-1169.
73. Enjalbert B, MacCallum DM, Odds FC, Brown AJ. 2007. Niche-specific activation of the oxidative stress response by the pathogenic fungus Candida albicans. Infect. Immun. 75:2143-2151.
74. Kusch H, Engelmann S, Albrecht D, Morschhauser J, Hecker M. 2007. Proteomic analysis of the oxidative stress response in Candida albicans. Proteomics 7:686-697.
75. Alarco AM, Raymond M. 1999. The bZip transcription factor Cap1p is involved in multidrug resistance and oxidative stress response in Candida albicans. J. Bacteriol. 181:700-708.
76. Lessing F, Kniemeyer O, Wozniok I, Loeffler J, Kurzai O, Haertl A, Brakhage AA. 2007. The Aspergillus fumigatus transcriptional regulator AfYap1 represents the major regulator for defense against reactive oxygen intermediates but is dispensable for pathogenicity in an intranasal mouse infection model. Eukaryot. Cell 6:2290-2302.
77. Lin CH, Yang SL, Chung KR. 2009. The YAP1 homolog-mediated oxidative stress tolerance is crucial for pathogenicity of the necrotrophic fungus Alternaria alternata in citrus. Mol. Plant Microbe Interact. 22:942-952.
78. Hwang LH, Seth E, Gilmore SA, Sil A. 2012. SRE1 regulates irondependent and -independent pathways in the fungal pathogen Histoplasma capsulatum. Eukaryot. Cell 11:16-25.
79. Marion CL, Rappleye CA, Engle JT, Goldman WE. 2006. An alpha-(1,4)-amylase is essential for alpha-(1,3)-glucan production and virulence in Histoplasma capsulatum. Mol. Microbiol. 62:970-983.