Urea Amidolyase (DUR1,2) Contributes to Virulence and Kidney Pathogenesis of Candida albicans

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Navarathna, Dhammika H M L P ^a   Lionakis, Michail S ^b   Lizak, Martin J ^c   Munasinghe, Jeeva ^c   Nickerson, Kenneth W ^d   Roberts, David D ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

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

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^d UNIVERSITY OF NEBRASKA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; INTERLEUKIN 1; INTERLEUKIN 15; MITOGEN ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; UREA AMIDOLYASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; CANDIDA ALBICANS; COMPLEMENT ALTERNATIVE PATHWAY; CONTROLLED STUDY; CYTOKINE RESPONSE; DISEASE ASSOCIATION; DUR1,2 GENE; FEMALE; FLOW CYTOMETRY; FUNGAL COLONIZATION; FUNGAL GENE; FUNGAL STRAIN; FUNGAL VIRULENCE; GENE DELETION; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; INVASIVE CANDIDIASIS; KIDNEY; KIDNEY FUNCTION; KIDNEY INFECTION; MOUSE; NEPHRITIS; NEUTROPHIL CHEMOTAXIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOGENESIS; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION; SURVIVAL RATE; WILD TYPE;

ANIMALS; CANDIDA ALBICANS; CANDIDIASIS; CARBON-NITROGEN LIGASES; FEMALE; FUNGAL PROTEINS; GENE EXPRESSION; INFLAMMATION MEDIATORS; INTERLEUKIN-1; INTERLEUKIN-15; KIDNEY; MICE; MICE, INBRED BALB C; MUTATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UREA; VIRULENCE;

CANDIDA; CANDIDA ALBICANS; MURINAE; MUS;

EID: 84868089509     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048475     Document Type: Article

References (69)

1. Vincent JL, Norrenberg M, (2009) Intensive care unit-acquired weakness: framing the topic. Crit Care Med 37: S296-298.
2. Trick WE, Fridkin SK, Edwards JR, Hajjeh RA, Gaynes RP, (2002) Secular trend of hospital-acquired candidemia among intensive care unit patients in the United States during 1989-1999. Clin Infect Dis 35: 627-630.
3. Calderone AR, Clancy JC, editors (2012) Candida and candidiasis. 2 ed: Amer Society for Microbiology. 534 p.
4. Odds FC (1988) Candida and candidiasis. London: Bailliere Tindall.
5. Navarathna DH, Hornby JM, Krishnan N, Parkhurst A, Duhamel GE, et al. (2007) Effect of farnesol on a mouse model of systemic candidiasis, determined by use of a DPP3 knockout mutant of Candida albicans. Infect Immun 75: 1609-1618.
6. Navarathna DH, Roberts DD (2010) Candida albicans heme oxygenase and its product CO contribute to pathogenesis of candidemia and alter systemic chemokine and cytokine expression. Free Radic Biol Med.
7. Navarathna DHMLP, Das A, Morschhaeuser J, Nickerson KW, Roberts DD (2010) Dur3 is the major urea transporter in Candida albicans and is co-regulated with the urea amidolyase Dur1,2. Microbiology: In Press.
8. Eaton KA, Brooks CL, Morgan DR, Krakowka S, (1991) Essential role of urease in pathogenesis of gastritis induced by Helicobacter pylori in gnotobiotic piglets. Infect Immun 59: 2470-2475.
9. Jones BD, Lockatell CV, Johnson DE, Warren JW, Mobley HL, (1990) Construction of a urease-negative mutant of Proteus mirabilis: analysis of virulence in a mouse model of ascending urinary tract infection. Infect Immun 58: 1120-1123.
10. Cox GM, Mukherjee J, Cole GT, Casadevall A, Perfect JR, (2000) Urease as a virulence factor in experimental cryptococcosis. Infect Immun 68: 443-448.
11. Cole GT (1997) Ammonia production by Coccidiodes immitis and its posible significance to the host fungus interplay. In: Stevens DO, F., editor. Host-Fungus interplay. Bethesda: National foundation for infectious diseases. 247-263.
12. Olszewski MA, Noverr MC, Chen GH, Toews GB, Cox GM, et al. (2004) Urease expression by Cryptococcus neoformans promotes microvascular sequestration, thereby enhancing central nervous system invasion. Am J Pathol 164: 1761-1771.
13. Navarathna DH, Harris SD, Roberts DD, Nickerson KW, (2010) Evolutionary aspects of urea utilization by fungi. FEMS Yeast Res 10: 209-213.
14. Roon RJ, Levenberg B, (1972) Urea amidolyase. I. Properties of the enzyme from Candida utilis. J Biol Chem 247: 4107-4113.
15. Ghosh S, Navarathna DH, Roberts DD, Cooper JT, Atkin AL, et al. (2009) Arginine-induced germ tube formation in Candida albicans is essential for escape from murine macrophage line RAW 264.7. Infect Immun 77: 1596-1605.
16. Strope PK, Nickerson KW, Harris SD, Moriyama EN, (2011) Molecular evolution of urea amidolyase and urea carboxylase in fungi. BMC Evol Biol 11: 80.
17. Navarathna DH, Hornby JM, Hoerrmann N, Parkhurst AM, Duhamel GE, et al. (2005) Enhanced pathogenicity of Candida albicans pre-treated with subinhibitory concentrations of fluconazole in a mouse model of disseminated candidiasis. J Antimicrob Chemother 56: 1156-1159.
18. Nickerson WJ, (1953) Reduction of inorganic substances by yeasts. I. Extracellular reduction of sulfite by species of Candida. J Infect Dis 93: 43-56.
19. Raab SS, Cheville JC, Bottles K, Cohen MB, (1994) Utility of Gomori methenamine silver stains in bronchoalveolar lavage specimens. Mod Pathol 7: 599-604.
20. Lionakis MS, Lim JK, Lee CC, Murphy PM, (2011) Organ-specific innate immune responses in a mouse model of invasive candidiasis. J Innate Immun 3: 180-199.
21. Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, et al. (2008) Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol 26: 317-325.
22. Kohrer K, Domdey H, (1991) Preparation of high molecular weight RNA. Methods Enzymol 194: 398-405.
23. Rozen S, Skaletsky H, (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.
24. SAS (1999) SAS/STAT User's Guide. 8 ed. Cary, NC: SAS Institute Inc.
25. Navarathna DH, Nickerson KW, Duhamel GE, Jerrels TR, Petro TM, (2007) Exogenous farnesol interferes with the normal progression of cytokine expression during candidiasis in a mouse model. Infect Immun 75: 4006-4011.
26. ElBerry HM, Majumdar ML, Cunningham TS, Sumrada RA, Cooper TG, (1993) Regulation of the urea active transporter gene (DUR3) in Saccharomyces cerevisiae. J Bacteriol 175: 4688-4698.
27. Espondaburu OR, Fernandez SB, Bassols GB, (1996) Normal values of serum urea levels in adults using the automated enzyme kinetic method. Acta Bioquimica Clinica Latinoamericana 30: 287-288.
28. Ashman RB, Papadimitriou JM, (1995) Production and function of cytokines in natural and acquired immunity to Candida albicans infection. Microbiol Rev 59: 646-672.
29. Zotta E, Ochoa F, Yeyati NL, Ibarra C, (2009) Urea handling by the kidney and its adaptive mechanism during renal disease. Revista De Nefrologia Dialisis Y Trasplante 29: 35-40.
30. Rasmussen LE, (1971) Organ Distribution of Exogenous C-14-Urea in Elasmobranchs, with Special Regard to Nervous System. Comparative Biochemistry and Physiology 40: 145-154.
31. Brieland J, Essig D, Jackson C, Frank D, Loebenberg D, et al. (2001) Comparison of pathogenesis and host immune responses to Candida glabrata and Candida albicans in systemically infected immunocompetent mice. Infect Immun 69: 5046-5055.
32. Ghosh S, Howe N, Volk K, Tati S, Nickerson KW, et al. (2010) Candida albicans cell wall components and farnesol stimulate the expression of both inflammatory and regulatory cytokines in the murine RAW264.7 macrophage cell line. FEMS Immunol Med Microbiol 60: 63-73.
33. Moyes DL, Runglall M, Murciano C, Shen C, Nayar D, et al. (2010) A biphasic innate immune MAPK response discriminates between the yeast and hyphal forms of Candida albicans in epithelial cells. Cell Host Microbe 8: 225-235.
34. Maurer M, von Stebut E, (2004) Macrophage inflammatory protein-1. Int J Biochem Cell Biol 36: 1882-1886.
35. Peitsch MC, Tschopp J, (1991) Assembly of macromolecular pores by immune defense systems. Curr Opin Cell Biol 3: 710-716.
36. Scheurer B, Rittner C, Schneider PM, (1997) Expression of the human complement C8 subunits is independently regulated by interleukin 1 beta, interleukin 6, and interferon gamma. Immunopharmacology 38: 167-175.
37. Ashman RB, (2008) Protective and pathologic immune responses against Candida albicans infection. Front Biosci 13: 3334-3351.
38. Pereno R, Giron-Michel J, Gaggero A, Cazes E, Meazza R, et al. (2000) IL-15/IL-15Ralpha intracellular trafficking in human melanoma cells and signal transduction through the IL-15Ralpha. Oncogene 19: 5153-5162.
39. Budagian V, Bulanova E, Paus R, Bulfone-Paus S, (2006) IL-15/IL-15 receptor biology: a guided tour through an expanding universe. Cytokine Growth Factor Rev 17: 259-280.
40. Kim HR, Hwang KA, Park SH, Kang I, (2008) IL-7 and IL-15: biology and roles in T-Cell immunity in health and disease. Crit Rev Immunol 28: 325-339.
41. Subramaniam S, Stansberg C, Cunningham C, (2004) The interleukin 1 receptor family. Dev Comp Immunol 28: 415-428.
42. Massrieh W, Derjuga A, Doualla-Bell F, Ku CY, Sanborn BM, et al. (2006) Regulation of the MAFF transcription factor by proinflammatory cytokines in myometrial cells. Biol Reprod 74: 699-705.
43. Wang CH, Lin HC, Liu CY, Huang KH, Huang TT, et al. (2001) Upregulation of inducible nitric oxide synthase and cytokine secretion in peripheral blood monocytes from pulmonary tuberculosis patients. Int J Tuberc Lung Dis 5: 283-291.
44. Wang CH, Kuo HP, (2001) Nitric oxide modulates interleukin-1beta and tumour necrosis factor-alpha synthesis, and disease regression by alveolar macrophages in pulmonary tuberculosis. Respirology 6: 79-84.
45. Hromatka BS, Noble SM, Johnson AD, (2005) Transcriptional response of Candida albicans to nitric oxide and the role of the YHB1 gene in nitrosative stress and virulence. Mol Biol Cell 16: 4814-4826.
46. Corot C, Petry KG, Trivedi R, Saleh A, Jonkmanns C, et al. (2004) Macrophage imaging in central nervous system and in carotid atherosclerotic plaque using ultrasmall superparamagnetic iron oxide in magnetic resonance imaging. Invest Radiol 39: 619-625.
47. Sawada T, Falk LA, Rao P, Murphy WJ, Pluznik DH, (1997) IL-6 induction of protein-DNA complexes via a novel regulatory region of the inducible nitric oxide synthase gene promoter: role of octamer binding proteins. J Immunol 158: 5267-5276.
48. Spellberg B, Ibrahim AS, Edwards JE Jr, Filler SG, (2005) Mice with disseminated candidiasis die of progressive sepsis. J Infect Dis 192: 336-343.
49. Papadimitriou JM, Ashman RB, (1986) The pathogenesis of acute systemic candidiasis in a susceptible inbred mouse strain. J Pathol 150: 257-265.
50. Iranzo M, Canizares JV, Sainz-Pardo I, Aguado C, Ponton J, et al. (2003) Isolation and characterization of an avirulent Candida albicans yeast monomorphic mutant. Med Mycol 41: 43-52.
51. Robert R, Nail S, Marot-Leblond A, Cottin J, Miegeville M, et al. (2000) Adherence of platelets to Candida species in vivo. Infect Immun 68: 570-576.
52. Netea MG, van Tits LJ, Curfs JH, Amiot F, Meis JF, et al. (1999) Increased susceptibility of TNF-alpha lymphotoxin-alpha double knockout mice to systemic candidiasis through impaired recruitment of neutrophils and phagocytosis of Candida albicans. J Immunol 163: 1498-1505.
53. van de Veerdonk FL, Kullberg BJ, Netea MG, (2010) Pathogenesis of invasive candidiasis. Curr Opin Crit Care 16: 453-459.
54. Netea MG, Sutmuller R, Hermann C, Van der Graaf CA, Van der Meer JW, et al. (2004) Toll-like receptor 2 suppresses immunity against Candida albicans through induction of IL-10 and regulatory T cells. J Immunol 172: 3712-3718.
55. Overland G, Stuestol JF, Dahle MK, Myhre AE, Netea MG, et al. (2005) Cytokine responses to fungal pathogens in Kupffer Cells are Toll-like receptor 4 independent and mediated by tyrosine kinases. Scand J Immunol 62: 148-154.
56. Romani L, (1999) Immunity to Candida albicans: Th1, Th2 cells and beyond. Curr Opin Microbiol 2: 363-367.
57. Cook DN, (1996) The role of MIP-1 alpha in inflammation and hematopoiesis. J Leukoc Biol 59: 61-66.
58. MacCallum DM, (2009) Massive induction of innate immune response to Candida albicans in the kidney in a murine intravenous challenge model. FEMS Yeast Res 9: 1111-1122.
59. MacCallum DM, Castillo L, Brown AJ, Gow NA, Odds FC, (2009) Early-expressed chemokines predict kidney immunopathology in experimental disseminated Candida albicans infections. PLoS One 4: e6420.
60. Vylkova S, Carman AJ, Danhof HA, Collette JR, Zhou H, et al. (2011) The fungal pathogen Candida albicans autoinduces hyphal morphogenesis by raising extracellular pH. MBio 2: e00055-00011.
61. Celli JP, Turner BS, Afdhal NH, Keates S, Ghiran I, et al. (2009) Helicobacter pylori moves through mucus by reducing mucin viscoelasticity. Proc Natl Acad Sci U S A 106: 14321-14326.
62. Leduc D, Gallaud J, Stingl K, de Reuse H, (2010) Coupled amino acid deamidase-transport systems essential for Helicobacter pylori colonization. Infect Immun 78: 2782-2792.
63. Chiozzi V, Mazzini G, Oldani A, Sciullo A, Ventura U, et al. (2009) Relationship between Vac A toxin and ammonia in Helicobacter pylori-induced apoptosis in human gastric epithelial cells. J Physiol Pharmacol 60: 23-30.
64. Eng CH, Yu K, Lucas J, White E, Abraham RT (2010) Ammonia Derived from Glutaminolysis Is a Diffusible Regulator of Autophagy. Sci Signal 3: ra31-.
65. Marino G, Kroemer G (2010) Ammonia: A Diffusible Factor Released by Proliferating Cells That Induces Autophagy. Sci Signal 3: pe19-.
66. Coppi M, Niederman R, (1989) Effects of ammonia on human neutrophil N-formyl chemotactic peptide receptor-ligand interaction and cytoskeletal association. Biochem Biophys Res Commun 165: 377-383.
67. Mayo K, Held M, Wadstrom T, Megraud F, (1997) Helicobacter pylori-human polymorphonuclear leucocyte interaction in the presence of ammonia. Eur J Gastroenterol Hepatol 9: 457-461.
68. Shawcross DL, Wright GA, Stadlbauer V, Hodges SJ, Davies NA, et al. (2008) Ammonia impairs neutrophil phagocytic function in liver disease. Hepatology 48: 1202-1212.
69. Lionakis MS, Fischer BG, Lim JK, Swamydas M, Wan W, et al. (2012) Chemokine receptor ccr1 drives neutrophil-mediated kidney immunopathology and mortality in invasive candidiasis. PLoS Pathog 8: e1002865.