Fungal pathogens: Survival and replication within macrophages

Cold Spring Harbor Perspectives in Medicine

Volumn 5, Issue 7, 2015, Pages

  Gilbert, Andrew S ^a   Wheeler, Robert T ^b,c   May, Robin C ^a,c  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF MAINE   (United States)

^c QUEEN ELIZABETH HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

VIRULENCE FACTOR;

AJELLOMYCES CAPSULATUS; ARTICLE; ASPERGILLUS FUMIGATUS; CANDIDA; CANDIDA ALBICANS; CELL DIVISION; CELL SURVIVAL; COCCIDIODES POSADASII; COCCIDIOIDES; COCCIDIOIDES IMMITIS; CRYPTOCOCCUS GATTII; CRYPTOCOCCUS NEOFORMANS; HUMAN; MACROPHAGE; NONHUMAN; SACCHAROMYCES CEREVISIAE; YEAST CELL; GENETICS; HISTOPLASMA; MICROBIOLOGY;

AJELLOMYCES CAPSULATUS; ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; COCCIDIOIDES IMMITIS; FILOBASIDIELLA NEOFORMANS; FUNGI;

ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; CRYPTOCOCCUS NEOFORMANS; HISTOPLASMA; HUMANS; MACROPHAGES; VIRULENCE FACTORS;

EID: 84934782834     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a019661     Document Type: Article

References (95)

1. Aimanianda V, Bayry J, Bozza S, Kniemeyer O, Perruccio K, Elluru SR, Clavaud C, Paris S, Brakhage AA, Kaveri SV, et al. 2009. Surface hydrophobin prevents immune recog-nition of airborne fungal spores. Nature 460: 1117-1121.
2. Alvarez M, Casadevall A. 2006. Phagosome extrusion and host-cell survival after Cryptococcus neoformans phago-cytosis by macrophages. Curr Biol 16: 2161-2165.
3. Bain J, Lewis L, Okai B, Quinn J, Gow N, Erwig L. 2012. Non-lytic expulsion/exocytosis of Candida albicans from macrophages. Fungal Genet Biol 49: 677-678.
4. Beaman L, Holmberg C. 1980. In vitro response of alveolar macrophages to infection with Coccidioides immitis. In-fect Immun 28: 594-600.
5. Biswas S, Mantovani A. 2010. Macrophage plasticity and interaction with lymphocyte subsets: Cancer as a para-digm. Nat Immunol 11: 889-896.
6. Blanco J, Hontecillas R, Bouza E, Blanco I, Pelaez T, Munoz P, Molina J, García M. 2002. Correlation between the elastase activity index and invasiveness of clinical isolates of Aspergillus fumigatus. J Clin Microbiol 40: 1811-1813.
7. Borchers A, Gershwin M. 2010. The immune response in Coccidioidomycosis. Autoimmun Rev 10: 94-102.
8. Bose I, Reese A, Ory J, Janbon G, Doering T. 2003. A yeast under cover: The capsule of Cryptococcus neoformans. Eukaryot Cell 2: 655-663.
9. Brothers KM, Newman ZR, Wheeler RT. 2011. Live imaging of disseminated candidiasis in zebrafish reveals role of phagocyte oxidase in limiting filamentous growth. Eu-karyot Cell 10: 932-944.
10. Brothers KM, Gratacap RL, Barker SE, Newman ZR, Norum A, Wheeler RT. 2013. NADPH oxidase-driven phagocyte recruitment controls Candida albicans filamentous growth and prevents mortality. PLoS Pathog 9: e1003634.
11. Brown S, Campbell L, Lodge J. 2007. Cryptococcus neoformans, a fungus under stress. Curr Opin Microbiol 10: 320-325.
12. Brown GD, Denning DW, Gow NA, Levitz SM, Netea MG, White TC. 2012. Hidden killers: Human fungal infections. Sci Transl Med 4: 165rv113.
13. Calderone R, Sturtevant J. 1994. Macrophage interactions with Candida. Immunol Ser 60: 505-515.
14. Chaturvedi V, Chaturvedi S. 2011. Cryptococcus gattii: A resurgent fungal pathogen. Trends Microbiol 19: 564-571.
15. Chayakulkeeree M, Johnston S, Oei J, Lev S, Williamson P, Wilson C, Zuo X, Leal A, Vainstein M, Meyer W, et al. 2011. SEC14 is a specific requirement for secretion of phospholipase B1 and pathogenicity of Cryptococcus neo-formans. Mol Microbiol 80: 1088-1101.
16. Chen H, Langer R, Edwards D. 1997. A film tension theory of phagocytosis. J Colloid Interface Sci 190: 118-133.
17. Chu J, Feudtner C, Heydon K, Walsh T, Zaoutis T. 2006. Hospitalizations for endemic mycoses: A population-based national study. Clin Infect Dis 42: 822-825.
18. Derengowski L, Paes H, Albuquerque P, Tavares A, Fernandes L, Silva-Pereira I, Casadevall A. 2013. The tran-scriptional response of Cryptococcus neoformans to inges-tion by Acanthamoeba castellanii and macrophages provides insights into the evolutionary adaptation to the mammalian host. Eukaryot Cell 12: 761-774.
19. Diamond R, Bennett J. 1973. Growth of Cryptococcus neoformans within human macrophages in vitro. Infect Im-mun 7: 231-236.
20. Doering T. 2009. How sweet it is! Cell wall biogenesis and polysaccharide capsule formation in Cryptococcus neoformans. Annu Rev Microbiol 63: 223-247.
21. Edwards L, Acquaviv FA, Levesay V, Cross F, Palmer C. 1969. An atlas of sensitivity to tuberculin, PPD-B, and histoplasmin in the United States. Am Rev Respir Dis 99: 1-132.
22. Enjalbert B, Nantel A, Whiteway M. 2003. Stress-induced gene expression in Candida albicans: Absence of a general stress response. Mol Biol Cell 14: 1460-1467.
23. Fairn G, Grinstein S. 2012. How nascent phagosomes mature to become phagolysosomes. Trends Immunol 33: 397-405.
24. Fernandez-Arenas E, Bleck C, Nombela C, Gil C, Griffiths G, Diez-Orejas R. 2009. Candida albicans actively modulates intracellular membrane trafficking in mouse macrophage phagosomes. Cell Microbiol 11: 560-589.
25. Flannagan RS, Jaumouillé V, Grinstein S. 2012. The cell biology of phagocytosis. Annu Rev Pathol 7: 61-98.
26. Fradin C, De Groot P, MacCallum D, Schaller M, Klis F, Odds F, Hube B. 2005. Granulocytes govern the transcrip-tional response, morphology and proliferation of Candi-da albicans in human blood. Mol Microbiol 56: 397-415.
27. Frey CL, Drutz DJ. 1986. Influence of fungal surface components on the interaction of Coccidioides immitis with polymorphonuclear neutrophils. J Infect Dis 153: 933-943.
28. García-Rodas R, González-Camacho F, Rodríguez-Tudela JL, Cuenca-Estrella M, Zaragoza O. 2011. The interaction between Candida krusei and murine macrophages results in multiple outcomes, including intracellular survival and escape from killing. Infect Immun 79: 2136-2144.
29. Gonzalez A, Hung C, Cole G. 2011. Coccidioides releases a soluble factor that suppresses nitric oxide production by murine primary macrophages. Microb Pathog 50: 100-108.
30. Gordon S, Martinez F. 2010. Alternative activation of mac-rophages: Mechanism and functions. Immunity 32: 593-604.
31. Heinekamp T, Thywissen A, Macheleidt J, Keller S, Valiante V, Brakhage AA. 2013. Aspergillus fumigatus melanins: Interference with the host endocytosis pathway and im-pact on virulence. Front Microbiol 3: 440.
32. Helmbright A, Larsh H. 1952. Size of the spores of Histo-plasma capsulatum. Proc Soc Exp Biol Med 81: 550-551.
33. Hoang L, Maguire J, Doye P, Fyfe M, Roscoe D. 2004. Cryptococcus neoformans infections at Vancouver Hospital and Health Sciences Centre (1997-2002): Epidemiology, microbiology and histopathology. J Med Microbiol 53: 935-940.
34. Holbrook E, Smolnycki K, Youseff B, Rappleye C. 2013. Redundant catalases detoxify phagocyte reactive oxygen and facilitate Histoplasma capsulatum pathogenesis. In-fect Immun 81: 2334-2346.
35. Hung C, Ampel N, Christian L, Seshan K, Cole G. 2000. A major cell surface antigen of Coccidioides immitis which elicits both humoral and cellular immune responses. In-fect Immun 68: 584-593.
36. Hung C, Seshan K, Yu J, Schaller R, Xue J, Basrur V, Gardner M, Cole G. 2005. A metalloproteinase of Coccidioides posadasii contributes to evasion of host detection. Infect Immun 73: 6689-6703.
37. Hung C, Xue J, Cole G, Clemons K, LaniadoLaborin R, Stevens D. 2007. Virulence mechanisms of Coccidioides: Coccidioidomycosis: Sixth International Symposium. Ann NY Acad Sci 1111: 225-235.
38. Hwang C, Rhie G, Oh J, Huh W, Yim H, Kang S. 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: 3705-3713.
39. Inglis DO, Voorhies M, Hocking Murray DR, Sil A. 2013. Comparative transcriptomics of infectious spores from the fungal pathogen Histoplasma capsulatum reveals a core set of transcripts that specify infectious and patho-genic states. Eukaryot Cell 12: 828-852.
40. Jiménez-López C, Collette JR, Brothers KM, Shepardson KM, Cramer RA, Wheeler RT, Lorenz MC. 2013. Candida albicans induces arginine biosynthetic genes in response to host-derived reactive oxygen species. Eukaryot Cell 12: 91-100.
41. Johnston S, 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.
42. Johnston S, May RC. 2013. Cryptococcus interactions with macrophages: Evasion and manipulation of the phagosome by a fungal pathogen. Cell Microbiol 15: 403-411.
43. Kaur R, Ma B, Cormack B. 2007. A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc Natl Acad Sci 104: 7628-7633.
44. Kinchen J, Ravichandran K. 2008. Phagosome maturation: Going through the acid test. Nat Rev Mol Cell Biol 9: 781-795.
45. Klengel T, Liang W, Chaloupka J, Ruoff C, Schroppel K, Naglik J, Eckert S, Mogensen E, Haynes K, Tuite M, et al. 2005. Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence. Curr Biol 15: 2177-2177.
46. Kroetz D, Deepe G. 2012. The role of cytokines and chemo-kines in Histoplasma capsulatum infection. Cytokine 58: 112-117.
47. Krombach F, Munzing S, Allmeling AM, Gerlach JT, Behr J, Dörger M. 1997. Cell size of alveolar macrophages: An interspecies comparison. Environ Health Perspect 105: 1261-1263.
48. Latge J. 1999. Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 12: 310.
49. Levitz S, Nong S, Seetoo K, Harrison T, Speizer R, Simons E. 1999. Cryptococcus neoformans resides in an acidic phagolysosome of human macrophages. Infect Immun 67: 885-890.
50. Lionakis MS, Swamydas M, Fischer BG, Plantinga TS, John-son MD, Jaeger M, Green NM, Masedunskas A, Weigert R, Mikelis C, et al. 2013. CX3CR1-dependent renal mac-rophage survival promotes Candida control and host survival. J Clin Invest 123: 5035-5051.
51. Liu O, Chun C, Chow E, Chen C, Madhani H, Noble S. 2008. Systematic genetic analysis of virulence in the human fungal pathogen Cryptococcus neoformans. Cell 135: 174-188.
52. Lo HJ, Köhler JR, DiDomenico B, Loebenberg D, Caccia-puoti A, Fink GR. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939-949.
53. Lorenz M, Bender J, Fink G. 2004. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 3: 1076-1087.
54. Ma H, Croudace J, Lammas D, May RC. 2006. Expulsion of live pathogenic yeast by macrophages. Curr Biol 16: 2156-2160.
55. Mansour M, Tam J, Vyas J, Clemons K, Perlin D, Richardson M. 2012. The cell biology of the innate immune response to Aspergillus fumigatus. Ann NY Acad Sci 1273: 78-84.
56. Mayer F, Wilson D, Hube B. 2013. Candida albicans patho-genicity mechanisms. Virulence 4: 119-128.
57. McNeil M, Nash S, Hajjeh R, Phelan M, Conn L, Plikaytis B, Warnock D. 2001. Trends in mortality due to invasive mycotic diseases in the United States, 1980-1997. Clin Infect Dis 33: 641-647.
58. Meredith P, Riesz J. 2004. Radiative relaxation quantum yields for synthetic eumelanin. Photochem Photobiol 79: 211-216.
59. Miramón P, Dunker C, Windecker H, Bohovych IM, Brown AJ, Kurzai O, Hube B. 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: e52850.
60. Miramón P, Kasper L, Hube B. 2013. Thriving within the host: Candida spp. interactions with phagocytic cells. Med Microbiol Immunol 202: 183-195.
61. Mirbod-Donovan F, Schaller R, Hung C, Xue J, Reichard U, Cole G. 2006. Urease produced by Coccidioides posadasii contributes to the virulence of this respiratory pathogen. Infect Immun 74: 504-515.
62. Morton CO, Bouzani M, Loeffler J, Rogers TR. 2012. Direct interaction studies between Aspergillus fumigatus and human immune cells; what have we learned about pathoge-nicity and host immunity? Front Microbiol 3: 413.
63. Nierman W, Pain A, Anderson M, Wortman J, Kim H, Arroyo J, Berriman M, Abe K, Archer D, Bermejo C, et al. 2005. Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438: 1151-1156.
64. Okagaki L, Nielsen K. 2012. Titan cells confer protection from phagocytosis in Cryptococcus neoformans infections. Eukaryot Cell 11: 820-826.
65. Okagaki L, Strain A, Nielsen J, Charlier C, Baltes N, Chretien F, Heitman J, Dromer F, Nielsen K. 2010. Cryptococcal cell morphology affects host cell interactions and patho-genicity. PLoS Pathog 6: e1000953.
66. Pappas P, Alexander B, Andes D, Hadley S, Kauffman C, Freifeld A, Anaissie E, Brumble L, Herwaldt L, Ito J, et al. 2010. Invasive fungal infections among organ trans-plant recipients: Results of the Transplant-Associated In-fection Surveillance Network (TRANSNET). Clin Infect Dis 50: 1101-1111.
67. Park B, Wannemuehler K, Marston B, Govender N, Pappas P, Chiller T. 2009. Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. Aids 23: 525-530.
68. Patterson MJ, McKenzie CG, Smith DA, da Silva Dantas A, Sherston S, Veal EA, Morgan BA, Maccallum DM, Erwig LP, Quinn J. 2013. Ybp1 and Gpx3 signaling in Candida albicans govern hydrogen peroxide-induced oxidation of the Cap1 transcription factor and macrophage escape. Antioxid Redox Signal 19: 2244-2260.
69. Ramage G, Mowat E, Jones B, Williams C, Lopez-Ribot J. 2009. Our current understanding of fungal biofilms. Crit Rev Microbiol 35: 340-355.
70. Ramírez MA, Lorenz MC. 2009. The transcription factor homolog CTF1 regulates b-oxidation in Candida albi-cans. Eukaryot Cell 8: 1604-1614.
71. Rappleye C, Eissenberg L, Goldman W. 2007. Histoplasma capsulatum a-(1,3)-glucan blocks innate immune recognition by the b-glucan receptor. Proc Natl Acad Sci 104: 1366-1370.
72. Schrettl M, Haas H. 2011. Iron homeostasis-Achilles’ heel of Aspergillus fumigatus? Curr Opin Microbiol 14: 400-405.
73. Scully C, Elkabir M, Samaranayake L. 1994. Candida and oral candidosis: A review. Crit Rev Oral Biol Med 5: 125-157.
74. Seider K, Brunke S, Schild L, Jablonowski N, Wilson D, Majer O, Barz D, Haas A, Kuchler K, Schaller M, et al. 2011. The facultative intracellular pathogen Candida glabrata subverts macrophage cytokine production and phagolysosome maturation. J Immunol 187: 3072-3086.
75. Smith LM, May RC. 2013. Mechanisms of microbial escape from phagocyte killing. Biochem Soc Trans 41: 475-490.
76. Smith D, Nicholls S, Morgan B, Brown A, Quinn J. 2004. A conserved stress-activated protein kinase regulates a core stress response in the human pathogen Candida albicans. Mol Biol Cell 15: 4179-4190.
77. Stano P, Williams V, Villani M, Cymbalyuk E, Qureshi A, Huang Y, Morace G, Luberto C, Tomlinson S, Del Poeta M. 2009. App1: An antiphagocytic protein that binds to complement receptors 3 and 2. J Immunol 182: 84-91.
78. Steenbergen JN, Shuman HA, Casadevall A. 2001. Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc Natl Acad Sci 98: 15245-15250.
79. Strasser J, Newman S, Ciraolo G, Morris R, Howell M, Dean G. 1999. Regulation of the macrophage vacuolar ATPase and phagosome-lysosome fusion by Histoplasma capsu-latum. J Immunol 162: 6148-6154.
80. Thywissen A, Heinekamp T, Dahse HM, Schmaler-Ripcke J, Nietzsche S, Zipfel PF, Brakhage AA. 2011. Conidial dihydroxynaphthalene melanin of the human pathogenic fungus Aspergillus fumigatus interferes with the host en-docytosis pathway. Front Microbiol 2: 96.
81. Ullmann B, Myers H, Chiranand W, Lazzell A, Zhao Q, Vega L, Lopez-Ribot J, Gardner P, Gustin M. 2004. Inducible defense mechanism against nitric oxide in Candida albi-cans. Eukaryotic Cell 3: 715-723.
82. Uppuluri P, Chaturvedi A, Srinivasan A, Banerjee M, Ram-asubramaniam A, Kohler J, Kadosh D, Lopez-Ribot J. 2010. Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog 6: e1000828.
83. Vázquez-Torres A, Balish E. 1997. Macrophages in resistance to candidiasis. Microbiol Mol Biol Rev 61: 170-192.
84. Velagapudi R, Hsueh Y, Geunes-Boyer S, Wright J, Heitman J. 2009. Spores as infectious propagules of Cryptococcus neoformans. Infect Immun 77: 4345-4355.
85. Voelz K, Lammas D, May RC. 2009. Cytokine signaling reg-ulates the outcome of intracellular macrophage parasitism by Cryptococcus neoformans. Infect Immun 77: 3450-3457.
86. Vylkova S, Carman A, Danhof H, Collette J, Zhou H, Lorenz M. 2011. The fungal pathogen Candida albicans autoinduces hyphal morphogenesis by raising extracellular pH. MBio 2: e00055-11.
87. Wang Y, Cao Y, Jia X, Cao Y, Gao P, Fu X, Ying K, Chen W, Jiang Y. 2006. Cap1p is involved in multiple pathways of oxidative stress response in Candida albicans. Free Radic Biol Med 40: 1201-1209.
88. Wellington M, Koselny K, Krysan DJ. 2012. Candida albi-cans morphogenesis is not required for macrophage interleukin 1b production. MBio 4: e00433-00412.
89. Welsh O, Vera-Cabrera L, Rendon A, Gonzalez G, Bonifaz A. 2012. Coccidioidomycosis. Clin Dermatol 30: 573-591.
90. Wheeler R, Kombe D, Agarwala S, Fink G. 2008. Dynamic, morphotype-specific Candida albicans b-glucan expo-sure during infection and drug treatment. PLoS Pathog 4: e1000227.
91. Whiston E, Wise H, Sharpton T, Jui G, Cole G, Taylor J. 2012. Comparative transcriptomics of the Saprobic and parasitic growth phases in Coccidioides pp. PLoS ONE 7: e41034.
92. Youseff B, Holbrook E, Smolnycki K, Rappleye C. 2012. Extracellular superoxide dismutase protects histoplasma yeast cells from host-derived oxidative stress. PLoS Pathog 8: e1002713.
93. Zaragoza O, Nielsen K. 2013. Titan cells in Cryptococcus neoformans: Cells with a giant impact. Curr Opin Microbiol 16: 409-413.
94. Zaragoza O, Chrisman C, Castelli M, Frases S, Cuenca-Es-trella M, Rodriguez-Tudela J, Casadevall A. 2008. Capsule enlargement in Cryptococcus neoformans confers resis-tance to oxidative stress suggesting a mechanism for in-tracellular survival. Cell Microbiol 10: 2043-2057.
95. Zhu X, Gibbons J, García-Rivera J, Casadevall A, Williamson P. 2001. Laccase of Cryptococcus neoformans is a cell wall-associated virulence factor. Infect Immun 69: 5589-5596.