Modulation of Phagosomal pH by Candida albicans Promotes Hyphal Morphogenesis and Requires Stp2p, a Regulator of Amino Acid Transport

PLoS Pathogens

Volumn 10, Issue 3, 2014, Pages

  Vylkova, Slavena ^a   Lorenz, Michael C ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; FUNGAL PROTEIN; LACTATE DEHYDROGENASE; PERMEASE; STP2P PROTEIN; UNCLASSIFIED DRUG;

ALKALINIZATION; AMINO ACID TRANSPORT; ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; CYTOTOXICITY ASSAY; FUNGAL VIRULENCE; FUNGUS HYPHAE; FUNGUS MUTANT; HOST PATHOGEN INTERACTION; INNATE IMMUNITY; MACROPHAGE; MORPHOGENESIS; NONHUMAN; PH; PHAGOCYTOSIS; PHAGOSOME; SURVIVAL;

AMINO ACIDS; ANIMALS; BIOLOGICAL TRANSPORT; CANDIDA ALBICANS; CANDIDIASIS; CELL LINE; FEMALE; FUNGAL PROTEINS; HYDROGEN-ION CONCENTRATION; HYPHAE; MACROPHAGES; MICE; MICE, INBRED ICR; MORPHOGENESIS; PHAGOSOMES; VIRULENCE;

EID: 84897442496     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003995     Document Type: Article

References (68)

1. Kwon-Chung KJ, Bennett JE (1992) Medical Mycology. Philadelphia: Lea & Febiger.
2. Odds FC (1988) Candida and candidosis. Philadelphia: Bailliere Tindall.
3. 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.
4. Diekema D, Arbefeville S, Boyken L, Kroeger J, Pfaller M, (2012) The changing epidemiology of healthcare-associated candidemia over three decades. Diagn Microbiol Infect Dis 73: 45-48.
5. Hajjeh RA, Sofair AN, Harrison LH, Lyon GM, Arthington-Skaggs BA, et al. (2004) Incidence of bloodstream infections due to Candida species and n vitro susceptibilities of isolates collected from 1998 to 2000 in a population-based active surveillance program. J Clin Microbiol 42: 1519-1527.
6. Garrity-Ryan L, Kazmierczak B, Kowal R, Comolli J, Hauser A, et al. (2000) The arginine finger domain of ExoT contributes to actin cytoskeleton disruption and inhibition of internalization of Pseudomonas aeruginosa by epithelial cells and macrophages. Infect Immun 68: 7100-7113.
7. Grosdent N, Maridonneau-Parini I, Sory MP, Cornelis GR, (2002) Role of Yops and adhesins in resistance of Yersinia enterocolitica to phagocytosis. Infect Immun 70: 4165-4176.
8. Huang B, Hubber A, McDonough JA, Roy CR, Scidmore MA, et al. (2010) The Anaplasma phagocytophilum-occupied vacuole selectively recruits Rab-GTPases that are predominantly associated with recycling endosomes. Cell Microbiol 12: 1292-1307.
9. Mott J, Rikihisa Y, Tsunawaki S, (2002) Effects of Anaplasma phagocytophila on NADPH oxidase components in human neutrophils and HL-60 cells. Infect Immun 70: 1359-1366.
10. Park YK, Bearson B, Bang SH, Bang IS, Foster JW, (1996) Internal pH crisis, lysine decarboxylase and the acid tolerance response of Salmonella typhimurium. Mol Microbiol 20: 605-611.
11. Shaughnessy LM, Hoppe AD, Christensen KA, Swanson JA, (2006) Membrane perforations inhibit lysosome fusion by altering pH and calcium in Listeria monocytogenes vacuoles. Cell Microbiol 8: 781-792.
12. Vandal OH, Pierini LM, Schnappinger D, Nathan CF, Ehrt S, (2008) A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat Med 14: 849-854.
13. Lo HJ, Kohler JR, DiDomenico B, Loebenberg D, Cacciapuoti A, et al. (1997) Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939-949.
14. Saville SP, Lazzell AL, Monteagudo C, Lopez-Ribot JL, (2003) Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot Cell 2: 1053-1060.
15. Brown AJ (2002) Morphogenetic signaling pathways in Candida albicans. In: Calderone R, editor. Candida and candidiasis. Washington: ASM Press.
16. Fernandez-Arenas E, Bleck CK, Nombela C, Gil C, Griffiths G, et al. (2009) Candida albicans actively modulates intracellular membrane trafficking in mouse macrophage phagosomes. Cell Microbiol 11: 560-589.
17. Fradin C, De Groot P, MacCallum D, Schaller M, Klis F, et al. (2005) Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol Microbiol 56: 397-415.
18. Lorenz MC, Bender JA, Fink GR, (2004) Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 3: 1076-1087.
19. Lorenz MC, Fink GR, (2001) The glyoxylate cycle is required for fungal virulence. Nature 412: 83-86.
20. Rubin-Bejerano I, Fraser I, Grisafi P, Fink GR, (2003) Phagocytosis by neutrophils induces an amino acid deprivation response in Saccharomyces cerevisiae and Candida albicans. Proc Natl Acad Sci U S A 100: 11007-11012.
21. Fernandez-Arenas E, Cabezon V, Bermejo C, Arroyo J, Nombela C, et al. (2007) Integrated proteomics and genomics strategies bring new insight into Candida albicans response upon macrophage interaction. Mol Cell Proteomics 6: 460-478.
22. Barelle CJ, Priest CL, Maccallum DM, Gow NA, Odds FC, et al. (2006) Niche-specific regulation of central metabolic pathways in a fungal pathogen. Cell Microbiol 8: 961-971.
23. Ramirez MA, Lorenz MC, (2007) Mutations in Alternative Carbon Utilization Pathways in Candida albicans Attenuate Virulence and Confer Pleiotropic Phenotypes. Eukaryot Cell 6: 280-290.
24. Vieira N, Casal M, Johansson B, MacCallum DM, Brown AJ, et al. (2010) Functional specialization and differential regulation of short-chain carboxylic acid transporters in the pathogen Candida albicans. Mol Microbiol 75: 1337-1354.
25. Ene IV, Adya AK, Wehmeier S, Brand AC, MacCallum DM, et al. (2012) Host carbon sources modulate cell wall architecture, drug resistance and virulence in a fungal pathogen. Cell Microbiol 14: 1319-1335.
26. Ene IV, Cheng SC, Netea MG, Brown AJ, (2013) Growth of Candida albicans cells on the physiologically relevant carbon source lactate affects their recognition and phagocytosis by immune cells. Infect Immun 81: 238-248.
27. 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: e00055-11.
28. Martinez P, Ljungdahl PO, (2005) Divergence of Stp1 and Stp2 transcription factors in Candida albicans places virulence factors required for proper nutrient acquisition under amino acid control. Mol Cell Biol 25: 9435-9446.
29. Lay J, Henry LK, Clifford J, Koltin Y, Bulawa CE, et al. (1998) Altered expression of selectable marker URA3 in gene-disrupted Candida albicans strains complicates interpretation of virulence studies. Infect Immun 66: 5301-5306.
30. Brand A, MacCallum DM, Brown AJ, Gow NA, Odds FC, (2004) Ectopic Expression of URA3 can influence the virulence phenotypes and proteome of Candida albicans but can be overcome by targeted reintegration of URA3 at the RPS10 locus. Eukaryot Cell 3: 900-909.
31. Reuss O, Vik A, Kolter R, Morschhauser J, (2004) The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341: 119-127.
32. Huynh KK, Grinstein S, (2007) Regulation of vacuolar pH and its modulation by some microbial species. Microbiol Mol Biol Rev 71: 452-462.
33. McKenzie CG, Koser U, Lewis LE, Bain JM, Mora-Montes HM, et al. (2010) Contribution of Candida albicans cell wall components to recognition by and escape from murine macrophages. Infect Immun 78: 1650-1658.
34. She X, Zhang L, Chen H, Calderone R, Li D, (2013) Cell surface changes in the Candida albicans mitochondrial mutant goa1Delta are associated with reduced recognition by innate immune cells. Cell Microbiol 15: 1572-1584.
35. Wheeler RT, Fink GR, (2006) A drug-sensitive genetic network masks fungi from the immune system. PLoS Pathog 2: e35.
36. Rocha CR, Schroppel K, Harcus D, Marcil A, Dignard D, et al. (2001) Signaling through adenylyl cyclase is essential for hyphal growth and virulence in the pathogenic fungus Candida albicans. Mol Biol Cell 12: 3631-3643.
37. Balestrieri B, Maekawa A, Xing W, Gelb MH, Katz HR, et al. (2009) Group V secretory phospholipase A2 modulates phagosome maturation and regulates the innate immune response against Candida albicans. J Immunol 182: 4891-4898.
38. Kaposzta R, Marodi L, Hollinshead M, Gordon S, da Silva RP, (1999) Rapid recruitment of late endosomes and lysosomes in mouse macrophages ingesting Candida albicans. J Cell Sci 112 (Pt 19) (): 3237-3248.
39. Marcil A, Gadoury C, Ash J, Zhang J, Nantel A, et al. (2008) Analysis of PRA1 and its relationship to Candida albicans- macrophage interactions. Infect Immun 76: 4345-4358.
40. Mor N, Goren MB, (1987) Discrepancy in assessment of phagosome-lysosome fusion with two lysosomal markers in murine macrophages infected with Candida albicans. Infect Immun 55: 1663-1667.
41. Newman SL, Holly A, (2001) Candida albicans is phagocytosed, killed, and processed for antigen presentation by human dendritic cells. Infect Immun 69: 6813-6822.
42. Bidani A, Reisner BS, Haque AK, Wen J, Helmer RE, et al. (2000) Bactericidal activity of alveolar macrophages is suppressed by V-ATPase inhibition. Lung 178: 91-104.
43. Gordon AH, Hart PD, Young MR, (1980) Ammonia inhibits phagosome-lysosome fusion in macrophages. Nature 286: 79-80.
44. Ibrahim-Granet O, Philippe B, Boleti H, Boisvieux-Ulrich E, Grenet D, et al. (2003) Phagocytosis and intracellular fate of Aspergillus fumigatus conidia in alveolar macrophages. Infect Immun 71: 891-903.
45. Schneider B, Gross R, Haas A, (2000) Phagosome acidification has opposite effects on intracellular survival of Bordetella pertussis and B. bronchiseptica. Infect Immun 68: 7039-7048.
46. Schwartz JT, Allen LA, (2006) Role of urease in megasome formation and Helicobacter pylori survival in macrophages. J Leukoc Biol 79: 1214-1225.
47. Seider K, Brunke S, Schild L, Jablonowski N, Wilson D, et al. (2011) The facultative intracellular pathogen Candida glabrata subverts macrophage cytokine production and phagolysosome maturation. J Immunol 187: 3072-3086.
48. Eissenberg LG, Goldman WE, Schlesinger PH, (1993) Histoplasma capsulatum modulates the acidification of phagolysosomes. J Exp Med 177: 1605-1611.
49. Newman SL, Gootee L, Hilty J, Morris RE, (2006) Human macrophages do not require phagosome acidification to mediate fungistatic/fungicidal activity against Histoplasma capsulatum. J Immunol 176: 1806-1813.
50. Beck MR, Dekoster GT, Cistola DP, Goldman WE, (2009) NMR structure of a fungal virulence factor reveals structural homology with mammalian saposin B. Mol Microbiol 72: 344-353.
51. Johnston SA, May RC, (2010) The human fungal pathogen Cryptococcus neoformans escapes macrophages by a phagosome emptying mechanism that is inhibited by Arp2/3 complex-mediated actin polymerisation. PLoS Pathog 6: e1001041 doi: 10.1371/journal.ppat.1001041.
52. Hart PD, Young MR, (1991) Ammonium chloride, an inhibitor of phagosome-lysosome fusion in macrophages, concurrently induces phagosome-endosome fusion, and opens a novel pathway: studies of a pathogenic mycobacterium and a nonpathogenic yeast. J Exp Med 174: 881-889.
53. Opperdoes FR, Szikora JP, (2006) In silico prediction of the glycosomal enzymes of Leishmania major and trypanosomes. Mol Biochem Parasitol 147: 193-206.
54. Pelosi A, Smith D, Brammananth R, Topolska A, Billman-Jacobe H, et al. (2012) Identification of a novel gene product that promotes survival of Mycobacterium smegmatis in macrophages. PLoS One 7: e31788.
55. Isaac DT, Coady A, Van Prooyen N, Sil A, (2013) The 3-hydroxy-methylglutaryl coenzyme A lyase HCL1 is required for macrophage colonization by human fungal pathogen Histoplasma capsulatum. Infect Immun 81: 411-420.
56. 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.
57. Alonso-Monge R, Navarro-Garcia F, Molero G, Diez-Orejas R, Gustin M, et al. (1999) Role of the mitogen-activated protein kinase Hog1p in morphogenesis and virulence of Candida albicans. J Bacteriol 181: 3058-3068.
58. Jacobsen ID, Brunke S, Seider K, Schwarzmuller T, Firon A, et al. (2009) "Candida glabrata persistence in mice does not depend on host immunosuppression and is unaffected by fungal amino acid auxotrophy". Infect Immun 78: 1066-1077.
59. Kingsbury JM, McCusker JH, (2009) Cytocidal amino acid starvation of Saccharomyces cerevisiae and Candida albicans acetolactate synthase (ilv2{Delta}) mutants is influenced by the carbon source and rapamycin. Microbiology 156: 929-939.
60. Kirsch DR, Whitney RR, (1991) Pathogenicity of Candida albicans auxotrophic mutants in experimental infections. Infect Immun 59: 3297-3300.
61. 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.
62. Donovan M, Schumuke JJ, Fonzi WA, Bonar SL, Gheesling-Mullis K, et al. (2001) Virulence of a phosphoribosylaminoimidazole carboxylase-deficient Candida albicans strain in an immunosuppressed murine model of systemic candidiasis. Infect Immun 69: 2542-2548.
63. Jimenez-Lopez C, Collette JR, Brothers KM, Shepardson KM, Cramer RA, et al. (2013) Candida albicans induces arginine biosynthetic genes in response to host-derived reactive oxygen species. Eukaryot Cell 12: 91-100.
64. Martinez P, Ljungdahl PO, (2004) An ER packaging chaperone determines the amino acid uptake capacity and virulence of Candida albicans. Mol Microbiol 51: 371-384.
65. Palkova Z, Janderova B, Gabriel J, Zikanova B, Pospisek M, et al. (1997) Ammonia mediates communication between yeast colonies. Nature 390: 532-536.
66. Wong L, Sissons C, (2001) A comparison of human dental plaque microcosm biofilms grown in an undefined medium and a chemically defined artificial saliva. Arch Oral Biol 46: 477-486.
67. Tomás MS, Nader-Macías ME (2007) Effect of a medium simulating vaginal fluid on the growth and expression of beneficial characteristics of potentially probiotic lactobacilli. In: Méndez-Vilas A, editor. Communicating Current Research and Educational Topics and Trends in Applied Microbiology. Badajoz, Spain: Formatex. pp. 732-739.
68. Murad AM, Lee PR, Broadbent ID, Barelle CJ, Brown AJ, (2000) CIp10, an efficient and convenient integrating vector for Candida albicans. Yeast 16: 325-327.