Candida albicans isolates from the gut of critically ill patients respond to phosphate limitation by expressing filaments and a lethal phenotype

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Romanowski, Kathleen ^a   Zaborin, Alexander ^a   Valuckaite, Vesta ^a   Rolfes, Ronda J ^b   Babrowski, Trissa ^a   Bethel, Cindy ^a   Olivas, Andrea ^a   Zaborina, Olga ^a   Alverdy, John C ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATASE; PHOSPHATE; ACID PHOSPHATASE; FUNGAL PROTEIN;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOFILM; CANDIDA ALBICANS; CONTROLLED STUDY; CRITICALLY ILL PATIENT; ENZYME ACTIVITY; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS ISOLATION; GENETIC TRANSFORMATION; HUMAN; INTESTINE FLORA; LETHALITY; MORPHOTYPE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PSEUDOMONAS AERUGINOSA; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; C57BL MOUSE; CAENORHABDITIS ELEGANS; CRITICAL ILLNESS; CYTOLOGY; DNA SEQUENCE; DRUG EFFECT; FECES; GASTROINTESTINAL TRACT; GENETIC TRANSCRIPTION; GENETICS; INTESTINE; ISOLATION AND PURIFICATION; MALE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MUTATION; PATHOLOGY; PHYSIOLOGY; ULTRASTRUCTURE;

CAENORHABDITIS ELEGANS; CANDIDA ALBICANS; MUS; PSEUDOMONAS AERUGINOSA;

ACID PHOSPHATASE; ANIMALS; BIOFILMS; CAENORHABDITIS ELEGANS; CANDIDA ALBICANS; CRITICAL ILLNESS; FECES; FUNGAL PROTEINS; GASTROINTESTINAL TRACT; HUMANS; INTESTINES; MALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PHOSPHATES; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION, GENETIC;

EID: 84855826068     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030119     Document Type: Article

References (50)

1. Zollner-Schwetz I, Auner HW, Paulitsch A, Buzina W, Staber PB, et al. (2008) Oral and intestinal Candida colonization in patients undergoing hematopoietic stem-cell transplantation. J Infect Dis 198: 150-153.
2. Sacristan B, Blanco MT, Galan-Ladero MA, Blanco J, Perez-Giraldo C, et al. (2011) Aspartyl proteinase, phospholipase, hemolytic activities and biofilm production of Candida albicans isolated from bronchial aspirates of ICU patients. Med Mycol.
3. Slavin MA, Sorrell TC, Marriott D, Thursky KA, Nguyen Q, et al. (2010) Candidaemia in adult cancer patients: risks for fluconazole-resistant isolates and death. J Antimicrob Chemother 65: 1042-1051.
4. Struck MF, Stiller D, Corterier CC, Reichelt B, Steen M, (2009) Fulminant, undetected Candida sepsis after an apparently survivable burn injury. J Burn Care Res 30: 894-897.
5. Sonoyama K, Miki A, Sugita R, Goto H, Nakata M, et al. (2011) Gut colonization by Candida albicans aggravates inflammation in the gut and extra-gut tissues in mice. Med Mycol.
6. Pinheiro MR, Lacerda HR, Melo RG, Maciel MA, (2008) Pseudomonas aeruginosa infections: factors relating to mortality with emphasis on resistance pattern and antimicrobial treatment. Braz J Infect Dis 12: 509-515.
7. Montero M, Dominguez M, Orozco-Levi M, Salvado M, Knobel H, (2009) Mortality of COPD patients infected with multi-resistant Pseudomonas aeruginosa: a case and control study. Infection 37: 16-19.
8. Payne S, Gibson G, Wynne A, Hudspith B, Brostoff J, et al. (2003) In vitro studies on colonization resistance of the human gut microbiota to Candida albicans and the effects of tetracycline and Lactobacillus plantarum LPK. Curr Issues Intest Microbiol 4: 1-8.
9. Samonis G, Kofteridis DP, Maraki S, Alegakis D, Mantadakis E, et al. (2005) Levofloxacin and moxifloxacin increase human gut colonization by Candida species. Antimicrob Agents Chemother 49: 5189.
10. Samonis G, Mantadakis E, Barbounakis E, Kofteridis D, Papadakis G, et al. (2008) Effects of tigecycline and daptomycin on murine gut colonization by Candida albicans. Mycoses 51: 324-327.
11. Samonis G, Maraki S, Barbounakis E, Leventakos K, Lamaris G, et al. (2006) Effects of vancomycin, teicoplanin, linezolid, quinupristin-dalfopristin, and telithromycin on murine gut colonization by Candida albicans. Med Mycol 44: 193-196.
12. Furtado GH, Bergamasco MD, Menezes FG, Marques D, Silva A, et al. (2009) Imipenem-resistant Pseudomonas aeruginosa infection at a medical-surgical intensive care unit: risk factors and mortality. J Crit Care 24: 625 e629-614.
13. Zaborina O, Lepine F, Xiao G, Valuckaite V, Chen Y, et al. (2007) Dynorphin activates quorum sensing quinolone signaling in Pseudomonas aeruginosa. PLoS Pathog 3: e35.
14. Patel NJ, Zaborina O, Wu L, Wang Y, Wolfgeher DJ, et al. (2007) Recognition of intestinal epithelial HIF-1alpha activation by Pseudomonas aeruginosa. Am J Physiol Gastrointest Liver Physiol 292: G134-142.
15. Wu L, Estrada O, Zaborina O, Bains M, Shen L, et al. (2005) Recognition of host immune activation by Pseudomonas aeruginosa. Science 309: 774-777.
16. Maki DG, (2004) Microbiologic diagnosis of blood culture-negative sepsis by hemofiltration. Crit Care Med 32: 1075-1077.
17. Zaborin A, Romanowski K, Gerdes S, Holbrook C, Lepine F, et al. (2009) Red death in Caenorhabditis elegans caused by Pseudomonas aeruginosa PAO1. Proc Natl Acad Sci U S A 106: 6327-6332.
18. Lamarche MG, Wanner BL, Crepin S, Harel J, (2008) The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol Rev 32: 461-473.
19. Jacobsen SM, Lane MC, Harro JM, Shirtliff ME, Mobley HL, (2008) The high-affinity phosphate transporter Pst is a virulence factor for Proteus mirabilis during complicated urinary tract infection. FEMS Immunol Med Microbiol 52: 180-193.
20. von Kruger WM, Lery LM, Soares MR, de Neves-Manta FS, Batista e Silva CM, et al. (2006) The phosphate-starvation response in Vibrio cholerae O1 and phoB mutant under proteomic analysis: disclosing functions involved in adaptation, survival and virulence. Proteomics 6: 1495-1511.
21. Peirs P, Lefevre P, Boarbi S, Wang XM, Denis O, et al. (2005) Mycobacterium tuberculosis with disruption in genes encoding the phosphate binding proteins PstS1 and PstS2 is deficient in phosphate uptake and demonstrates reduced in vivo virulence. Infect Immun 73: 1898-1902.
22. Kim J, Sudbery P, (2011) Candida albicans, a major human fungal pathogen. J Microbiol 49: 171-177.
23. Lim CS, Rosli R, Seow HF, Chong PP, (2011) Candida and invasive candidiasis: back to basics. Eur J Clin Microbiol Infect Dis.
24. Wisplinghoff H, Seifert H, Wenzel RP, Edmond MB, (2006) Inflammatory response and clinical course of adult patients with nosocomial bloodstream infections caused by Candida spp. Clin Microbiol Infect 12: 170-177.
25. Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, et al. (2004) Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 39: 309-317.
26. Vincent JL, Rello J, Marshall J, Silva E, Anzueto A, et al. (2009) International study of the prevalence and outcomes of infection in intensive care units. Jama 302: 2323-2329.
27. Gillum AM, Tsay EY, Kirsch DR, (1984) Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol Gen Genet 198: 179-182.
28. Wilson RB, Davis D, Mitchell AP, (1999) Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J Bacteriol 181: 1868-1874.
29. Noble SM, Johnson AD, (2005) Strains and strategies for large-scale gene deletion studies of the diploid human fungal pathogen Candida albicans. Eukaryot Cell 4: 298-309.
30. Homann OR, Dea J, Noble SM, Johnson AD, (2009) A phenotypic profile of the Candida albicans regulatory network. PLoS Genet 5: e1000783.
31. Long J, Zaborina O, Holbrook C, Zaborin A, Alverdy J, (2008) Depletion of intestinal phosphate after operative injury activates the virulence of P aeruginosa causing lethal gut-derived sepsis. Surgery 144: 189-197.
32. Mouillon JM, Persson BL, (2006) New aspects on phosphate sensing and signalling in Saccharomyces cerevisiae. FEMS Yeast Res 6: 171-176.
33. Lee YS, Mulugu S, York JD, O'Shea EK, (2007) Regulation of a cyclin-CDK-CDK inhibitor complex by inositol pyrophosphates. Science 316: 109-112.
34. Kerwin CL, Wykoff DD, (2009) Candida glabrata PHO4 is necessary and sufficient for Pho2-independent transcription of phosphate starvation genes. Genetics 182: 471-479.
35. Manolakaki D, Velmahos G, Kourkoumpetis T, Chang Y, Alam HB, et al. (2010) Candida infection and colonization among trauma patients. Virulence 1: 367-375.
36. Rosenbach A, Dignard D, Pierce JV, Whiteway M, Kumamoto CA, (2010) Adaptations of Candida albicans for growth in the mammalian intestinal tract. Eukaryot Cell 9: 1075-1086.
37. White SJ, Rosenbach A, Lephart P, Nguyen D, Benjamin A, et al. (2007) Self-regulation of Candida albicans population size during GI colonization. PLoS Pathog 3: e184.
38. Zaborina O, Zaborin A, Romanowski K, Babrowski T, Alverdy J Host Stress and Virulence Expression in Intestinal Pathogens: Development of Therapeutic Strategies using Mice and C. elegans. (2011) Curr Pharm Des 17: 1254-1260.
39. Cassone A, Carpinelli G, Angiolella L, Maddaluno G, Podo F, (1983) 31P nuclear magnetic resonance study of growth and dimorphic transition in Candida albicans. J Gen Microbiol 129: 1569-1575.
40. Yang J, Wu J, Ao SZ, (1996) The Effect of Yeast Transcriptional Factor PHO2 on the Gene Expression of PHO5, HIS4 and HO. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai) 28: 516-522.
41. Smith RF, Blasi D, Dayton SL, (1973) Phosphatase activity among Candida species and other yeasts isolated from clinical material. Appl Microbiol 26: 364-367.
42. Zaborina O, Kohler JE, Wang Y, Bethel C, Shevchenko O, et al. (2006) Identification of multi-drug resistant Pseudomonas aeruginosa clinical isolates that are highly disruptive to the intestinal epithelial barrier. Ann Clin Microbiol Antimicrob 5: 14.
43. Zaborina O, Holbrook C, Chen Y, Long J, Zaborin A, et al. (2008) Structure-function aspects of PstS in multi-drug-resistant Pseudomonas aeruginosa. PLoS Pathog 4: e43.
44. Barbaric S, Munsterkotter M, Goding C, Horz W, (1998) Cooperative Pho2-Pho4 interactions at the PHO5 promoter are critical for binding of Pho4 to UASp1 and for efficient transactivation by Pho4 at UASp2. Mol Cell Biol 18: 2629-2639.
45. Kurtz MB, Cortelyou MW, Kirsch DR, (1986) Integrative transformation of Candida albicans, using a cloned Candida ADE2 gene. Mol Cell Biol 6: 142-149.
46. Laughlin RS, Musch MW, Hollbrook CJ, Rocha FM, Chang EB, et al. (2000) The key role of Pseudomonas aeruginosa PA-I lectin on experimental gut-derived sepsis. Ann Surg 232: 133-142.
47. Alverdy J, Holbrook C, Rocha F, Seiden L, Wu RL, et al. (2000) Gut-derived sepsis occurs when the right pathogen with the right virulence genes meets the right host: evidence for in vivo virulence expression in Pseudomonas aeruginosa. Ann Surg 232: 480-489.
48. Pierce CG, Thomas DP, Lopez-Ribot JL, (2009) Effect of tunicamycin on Candida albicans biofilm formation and maintenance. J Antimicrob Chemother 63: 473-479.
49. Calderon J, Zavrel M, Ragni E, Fonzi WA, Rupp S, et al. (2010) PHR1, a pH-regulated gene of Candida albicans encoding a glucan-remodelling enzyme, is required for adhesion and invasion. Microbiology 156: 2484-2494.
50. Blankenship JR, Fanning S, Hamaker JJ, Mitchell AP, (2010) An extensive circuitry for cell wall regulation in Candida albicans. PLoS Pathog 6: e1000752.