Candida albicans SOD5 represents the prototype of an unprecedented class of Cu-only superoxide dismutases required for pathogen defense

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 16, 2014, Pages 5866-5871

  Gleason, Julie E ^a   Galaleldeen, Ahmad ^b   Peterson, Ryan L ^a   Taylor, Alexander B ^c   Holloway, Stephen P ^c   Waninger Saroni, Jessica ^b   Cormack, Brendan P ^d   Cabelli, Diane E ^e   John Hart, P ^c,f   Culotta, Valeria Cizewski ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b ST MARY'S UNIVERSITY   (United States)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e BROOKHAVEN NATIONAL LABORATORY   (United States)

^f SOUTH TEXAS VETERANS HEALTH CARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SOD5 ENZYME; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CANDIDA ALBICANS; ENZYME ACTIVITY; ESCHERICHIA COLI; HOST PATHOGEN INTERACTION; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; IONIC STRENGTH; NONHUMAN; OXIDATIVE STRESS; PH; PRIORITY JOURNAL; PROTEIN SECRETION; SACCHAROMYCES CEREVISIAE; SECRETORY PATHWAY; SEDIMENTATION RATE; X RAY DIFFRACTION;

AMINO ACID SEQUENCE; CANDIDA ALBICANS; COPPER; EXTRACELLULAR SPACE; FUNGAL PROTEINS; HUMANS; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PULSE RADIOLYSIS; SEQUENCE ANALYSIS, PROTEIN; STRUCTURAL HOMOLOGY, PROTEIN; SUPEROXIDE DISMUTASE;

EID: 84899070220     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1400137111     Document Type: Article

References (48)

1. McCord JM, Fridovich I (1969) Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244(22):6049-6055.
2. Antonyuk SV, Strange RW, Marklund SL, Hasnain SS (2009) The structure of human extracellular copper-zinc superoxide dismutase at 1.7 A resolution: Insights into heparin and collagen binding. J Mol Biol 388(2):310-326.
3. Roberts BR, et al. (2007) Structural characterization of zinc-deficient human superoxide dismutase and implications for ALS. J Mol Biol 373(4):877-890. (Pubitemid 47505245)
4. Banci L, et al. (1991) A characterization of copper/zinc superoxide dismutase mutants at position 124. Zinc-deficient proteins. Eur J Biochem 196(1):123-128.
5. Forman HJ, Fridovich I (1973) On the stability of bovine superoxide dismutase. The effects of metals. J Biol Chem 248(8):2645-2649.
6. Potter SZ, et al. (2007) Binding of a single zinc ion to one subunit of copper-zinc superoxide dismutase apoprotein substantially influences the structure and stability of the entire homodimeric protein. J Am Chem Soc 129(15):4575-4583. (Pubitemid 46648756)
7. Pantoliano MW, Valentine JS, Burger AR, Lippard SJ (1982) A pH-dependent superoxide dismutase activity for zinc-free bovine erythrocuprein. Reexamination of the role of zinc in the holoprotein. J Inorg Biochem 17(4):325-341.
8. Ellerby L, et al. (1996) Copper-zinc superoxide dismutase: Why not pH-dependent? J Am Chem Soc 118:6556-6561. (Pubitemid 26248149)
9. Getzoff ED, et al. (1992) Faster superoxide dismutase mutants designed by enhancing electrostatic guidance. Nature 358(6384):347-351.
10. Cudd A, Fridovich I (1982) Electrostatic interactions in the reaction mechanism of bovine erythrocyte superoxide dismutase. J Biol Chem 257(19):11443-11447. (Pubitemid 13203376)
11. Desideri A, et al. (1992) Evolutionary conservativeness of electric field in the Cu,Zn superoxide dismutase active site. Evidence for co-ordinated mutation of charged amino acid residues. J Mol Biol 223(1):337-342.
12. Fisher CL, Cabelli DE, Tainer JA, Hallewell RA, Getzoff ED (1994) The role of arginine 143 in the electrostatics and mechanism of Cu,Zn superoxide dismutase: Computational and experimental evaluation by mutational analysis. Proteins 19(1):24-34. (Pubitemid 24151481)
13. Cheng SC, Joosten LA, Kullberg BJ, Netea MG (2012) Interplay between Candida albicans and the mammalian innate host defense. Infect Immun 80(4):1304-1313.
14. Hwang CS, et al. (2002) Copper- and zinc-containing superoxide dismutase (Cu/ZnSOD) is required for the protection of Candida albicans against oxidative stresses and the expression of its full virulence. Microbiology 148(Pt 11):3705-3713.
15. Martchenko M, Alarco AM, Harcus D, Whiteway M (2004) Superoxide dismutases in Candida albicans: Transcriptional regulation and functional characterization of the hyphal-induced SOD5 gene. Mol Biol Cell 15(2):456-467. (Pubitemid 38146465)
16. Fradin C, et al. (2005) Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol Microbiol 56(2):397-415. (Pubitemid 40516780)
17. de Groot PW, et al. (2004) Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryot Cell 3(4):955-965.
18. 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(1):240-252.
19. Miramón P, et al. (2012) Cellular responses of Candida albicans to phagocytosis and the extracellular activities of neutrophils are critical to counteract carbohydrate starvation, oxidative and nitrosative stress. PLoS ONE 7(12):e52850.
20. Youseff BH, Holbrook ED, Smolnycki KA, Rappleye CA (2012) Extracellular superoxide dismutase protects Histoplasma yeast cells from host-derived oxidative stress. PLoS Pathog 8(5):e1002713.
21. Seetharaman SV, et al. (2010) Disrupted zinc-binding sites in structures of pathogenic SOD1 variants D124V and H80R. Biochemistry 49(27):5714-5725.
22. Hart PJ, et al. (1999) A structure-based mechanism for copper-zinc superoxide dismutase. Biochemistry 38(7):2167-2178.
23. Ogihara NL, et al. (1996) Unusual trigonal-planar copper configuration revealed in the atomic structure of yeast copper-zinc superoxide dismutase. Biochemistry 35(7):2316-2321. (Pubitemid 26071664)
24. Rypniewski WR, et al. (1995) Crystal structure of reduced bovine erythrocyte superoxide dismutase at 1.9 A resolution. J Mol Biol 251(2):282-296.
25. Vylkova S, et al. (2011) The fungal pathogen Candida albicans autoinduces hyphal morphogenesis by raising extracellular pH. MBio 2(3):e00055-e11.
26. Knight SA, Dancis A (2006) Reduction of 2,3-bis(2-methoxy-4-nitro-5- sulfophenyl)-2H-tetrazolium-5-carboxanilide inner salt (XTT) is dependent on CaFRE10 ferric reductase for Candida albicans grown in unbuffered media. Microbiology 152(Pt 8):2301-2308. (Pubitemid 44219639)
27. Leitch JM, et al. (2009) Activation of Cu,Zn-superoxide dismutase in the absence of oxygen and the copper chaperone CCS. J Biol Chem 284(33):21863-21871.
28. Furukawa Y, Torres AS, O'Halloran TV (2004) Oxygen-induced maturation of SOD1: A key role for disulfide formation by the copper chaperone CCS. EMBO J 23(14):2872- 2881.
29. Culotta VC, et al. (1997) The copper chaperone for superoxide dismutase. J Biol Chem 272(38):23469-23472. (Pubitemid 27410910)
30. Banci L, et al. (2012) Human superoxide dismutase 1 (hSOD1) maturation through interaction with human copper chaperone for SOD1 (hCCS). Proc Natl Acad Sci USA 109(34):13555-13560.
31. Petersen SV, et al. (2008) The folding of human active and inactive extracellular superoxide dismutases is an intracellular event. J Biol Chem 283(22):15031-15036.
32. Qin Z, Itoh S, Jeney V, Ushio-Fukai M, Fukai T (2006) Essential role for the Menkes ATPase in activation of extracellular superoxide dismutase: Implication for vascular oxidative stress. FASEB J 20(2):334-336. (Pubitemid 46671162)
33. Gleason JE, et al. (2013) Species-specific activation of Cu/Zn SOD by its CCS copper chaperone in the pathogenic yeast Candida albicans. J Biol Inorg Chem, 10.1007/s00775-013-1045-x.
34. Weissman Z, Shemer R, Kornitzer D (2002) Deletion of the copper transporter CaCCC2 reveals two distinct pathways for iron acquisition in Candida albicans. Mol Microbiol 44(6):1551-1560. (Pubitemid 34639432)
35. Festa RA, Thiele DJ (2012) Copper at the front line of the host-pathogen battle. PLoS Pathog 8(9):e1002887.
36. Wagner D, et al. (2005) Elemental analysis of Mycobacterium avium-, Mycobacterium tuberculosis-, and Mycobacterium smegmatis-containing phagosomes indicates pathogen-induced microenvironments within the host cell ' s endosomal system. J Immunol 174(3):1491 - 1500.
37. White C, Lee J, Kambe T, Fritsche K, Petris MJ (2009) A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J Biol Chem 284(49):33949-33956.
38. Osman D, et al. (2010) Copper homeostasis in Salmonella is atypical and copper-CueP is a major periplasmic metal complex. J Biol Chem 285(33):25259-25268.
39. Douglas LM, et al. (2012) Sur7 promotes plasma membrane organization and is needed for resistance to stressful conditions and to the invasive growth and virulence of Candida albicans. MBio 3(1):1-12.
40. Ding C, et al. (2013) Cryptococcus neoformans copper detoxification machinery is critical for fungal virulence. Cell Host Microbe 13(3):265-276.
41. Chaturvedi KS, et al. (2014) Cupric yersiniabactin is a virulence-associated superoxide dismutase mimic. ACS Chem Biol 9(2):551-561.
42. Botella H, et al. (2011) Mycobacterial p(1)-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe 10(3):248-259.
43. Kehl-Fie TE, Skaar EP (2010) Nutritional immunity beyond iron: A role for manganese and zinc. Curr Opin Chem Biol 14(2):218-224.
44. Spagnolo L, et al. (2004) Unique features of the sodC-encoded superoxide dismutase from Mycobacterium tuberculosis, a fully functional copper-containing enzyme lacking zinc in the active site. J Biol Chem 279(32):33447-33455. (Pubitemid 39062994)
45. Polticelli F, et al. (1998) Role of the electrostatic loop charged residues in Cu,Zn superoxide dismutase. Protein Sci 7(11):2354-2358. (Pubitemid 28506951)
46. McCoy AJ, et al. (2007) Pushing the boundaries of molecular replacement with maximum likelihood. J Appl Cryst 40(4):658-674.
47. Adams PD, et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66(Pt 2):213- 221.
48. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D, Biol Crystallogr 60(Pt 12 Pt 1):2126-2132.