The fungal pathogen Cryptococcus neoformans manipulates macrophage phagosome maturation

Cellular Microbiology

Volumn 17, Issue 5, 2015, Pages 702-713

  Smith, Leanne M ^a   Dixon, Emily F ^a   May, Robin C ^a,b  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b QUEEN ELIZABETH HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RAB PROTEIN; RAB11 PROTEIN; RAB5 PROTEIN; RAB7 PROTEIN; RAB9 PROTEIN; UNCLASSIFIED DRUG; CALCIUM; PEPTIDE HYDROLASE;

ACIDIFICATION; ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL MATURATION; CELL PROLIFERATION; CRYPTOCOCCUS NEOFORMANS; ENZYME ACTIVITY; MACROPHAGE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; ANIMAL; CELL LINE; CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOUSE; PH; PHYSIOLOGY;

FILOBASIDIELLA NEOFORMANS;

ANIMALS; CALCIUM; CELL LINE; CRYPTOCOCCUS NEOFORMANS; HOST-PATHOGEN INTERACTIONS; HYDROGEN-ION CONCENTRATION; IMMUNE EVASION; MACROPHAGES; MICE; PEPTIDE HYDROLASES; PHAGOSOMES; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS;

EID: 84927784466     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12394     Document Type: Article

References (57)

1. Alanio, A., Desnos-Ollivier, M., and Dromer, F. (2011) Dynamics of Cryptococcus neoformans-macrophage interactions reveal that fungal background influences outcome during cryptococcal meningoencephalitis in humans. MBio 2: e00159-11.
2. Alvarez, M., and Casadevall, A. (2006) Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages. Curr Biol 16: 2161-2165.
3. Alvarez-Dominguez, C., Madrazo-Toca, F., Fernandez-Prieto, L., Vandekerckhove, J., Pareja, E., Tobes, R., etal. (2008) Characterization of a Listeria monocytogenes protein interfering with Rab5a. Traffic 9: 325-337.
4. Artavanis-Tsakonas, K., Love, J.C., Ploegh, H.L., and Vyas, J.M. (2006) Recruitment of CD63 to Cryptococcus neoformans phagosomes requires acidification. Proc Natl Acad Sci USA 103: 15945-15950.
5. Bain, J.M., Lewis, L.E., Okai, B., Quinn, J., Gow, N.A., and Erwig, L.P. (2012) Non-lytic expulsion/exocytosis of Candida albicans from macrophages. Fungal Genet Biol 49: 677-678.
6. Bakowski, M.A., Braun, V., Lam, G.Y., Yeung, T., Heo, W.D., Meyer, T., etal. (2010) The phosphoinositide phosphatase SopB manipulates membrane surface charge and trafficking of the Salmonella-containing vacuole. Cell Host Microbe 7: 453-462.
7. Barr, F.A. (2013) Review series: Rab GTPases and membrane identity: causal or inconsequential? J Cell Biol 202: 191-199.
8. Chayakulkeeree, M., Johnston, S.A., Oei, J.B., Lev, S., Williamson, P.R., Wilson, C.F., etal. (2011) SEC14 is a specific requirement for secretion of phospholipase B1 and pathogenicity of Cryptococcus neoformans. Mol Microbiol 80: 1088-1101.
9. Chen, C.S. (2002) Phorbol ester induces elevated oxidative activity and alkalization in a subset of lysosomes. BMC Cell Biol 3: 21.
10. Chen, Y., Toffaletti, D.L., Tenor, J.L., Litvintseva, A.P., Fang, C., Mitchell, T.G., etal. (2014) The Cryptococcus neoformans transcriptome at the site of human meningitis. MBio 5: e01087-13.
11. Claus, V., Jahraus, A., Tjelle, T., Berg, T., Kirschke, H., Faulstich, H., etal. (1998) Lysosomal enzyme trafficking between phagosomes, endosomes, and lysosomes in J774 macrophages. Enrichment of cathepsin H in early endosomes. J Biol Chem 273: 9842-9851.
12. Coers, J., Monahan, C., and Roy, C.R. (1999) Modulation of phagosome biogenesis by Legionella pneumophila creates an organelle permissive for intracellular growth. Nat Cell Biol 1: 451-453.
13. Cox, G.M., Mukherjee, J., Cole, G.T., Casadevall, A., and Perfect, J.R. (2000) Urease as a virulence factor in experimental cryptococcosis. Infect Immun 68: 443-448.
14. Cox, G.M., McDade, H.C., Chen, S.C., Tucker, S.C., Gottfredsson, M., Wright, L.C., etal. (2001) Extracellular phospholipase activity is a virulence factor for Cryptococcus neoformans. Mol Microbiol 39: 166-175.
15. Diamond, R.D., and Bennett, J.E. (1973) Growth of Cryptococcus neoformans within human macrophages in vitro. Infect Immun 7: 231-236.
16. Diamond, R.D., Root, R.K., and Bennett, J.E. (1972) Factors influencing killing of Cryptococcus neoformans by human leukocytes in vitro. J Infect Dis 125: 367-376.
17. Enjalbert, B., MacCallum, D.M., Odds, F.C., and Brown, A.J. (2007) Niche-specific activation of the oxidative stress response by the pathogenic fungus Candida albicans. Infect Immun 75: 2143-2151.
18. Feldmesser, M., Tucker, S., and Casadevall, A. (2001) Intracellular parasitism of macrophages by Cryptococcus neoformans. Trends Microbiol 9: 273-278.
19. Fernandez-Arenas, E., Bleck, C.K., Nombela, C., Gil, C., Griffiths, G., and Diez-Orejas, R. (2009) Candida albicans actively modulates intracellular membrane trafficking in mouse macrophage phagosomes. Cell Microbiol 11: 560-589.
20. Flannagan, R.S., Jaumouille, V., and Grinstein, S. (2012) The cell biology of phagocytosis. Annu Rev Pathol 7: 61-98.
21. Fratti, R.A., Backer, J.M., Gruenberg, J., Corvera, S., and Deretic, V. (2001) Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J Cell Biol 154: 631-644.
22. Garcia-Rodas, R., Gonzalez-Camacho, F., Rodriguez-Tudela, J.L., Cuenca-Estrella, M., and 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.
23. Hernandez, L.D., Hueffer, K., Wenk, M.R., and Galan, J.E. (2004) Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 304: 1805-1807.
24. Holm, A., Tejle, K., Magnusson, K.E., Descoteaux, A., and Rasmusson, B. (2001) Leishmania donovani lipophosphoglycan causes periphagosomal actin accumulation: correlation with impaired translocation of PKCalpha and defective phagosome maturation. Cell Microbiol 3: 439-447.
25. Horwitz, M.A. (1983) The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J Exp Med 158: 2108-2126.
26. Jacobson, E.S., Ayers, D.J., Harrell, A.C., and Nicholas, C.C. (1982) Genetic and phenotypic characterization of capsule mutants of Cryptococcus neoformans. J Bacteriol 150: 1292-1296.
27. Johnston, S.A., and May, R.C. (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.
28. Kasper, L., Seider, K., Gerwien, F., Allert, S., Brunke, S., Schwarzmuller, T., etal. (2014) Identification of Candida glabrata genes involved in pH modulation and modification of the phagosomal environment in macrophages. PLoS ONE 9: e96015.
29. Kechichian, T.B., Shea, J., and Del Poeta, M. (2007) Depletion of alveolar macrophages decreases the dissemination of a glucosylceramide-deficient mutant of Cryptococcus neoformans in immunodeficient mice. Infect Immun 75: 4792-4798.
30. Kinchen, J.M., and Ravichandran, K.S. (2008) Phagosome maturation: going through the acid test. Nat Rev Mol Cell Biol 9: 781-795.
31. Lennon-Dumenil, A.M., Bakker, A.H., Maehr, R., Fiebiger, E., Overkleeft, H.S., Rosemblatt, M., etal. (2002) Analysis of protease activity in live antigen-presenting cells shows regulation of the phagosomal proteolytic contents during dendritic cell activation. J Exp Med 196: 529-540.
32. Levitz, S.M., Nong, S.H., Seetoo, K.F., Harrison, T.S., Speizer, R.A., and Simons, E.R. (1999) Cryptococcus neoformans resides in an acidic phagolysosome of human macrophages. Infect Immun 67: 885-890.
33. Lorenz, M.C., Bender, J.A., and Fink, G.R. (2004) Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 3: 1076-1087.
34. Ma, H., Croudace, J.E., Lammas, D.A., and May, R.C. (2006) Expulsion of live pathogenic yeast by macrophages. Curr Biol 16: 2156-2160.
35. Malik, Z.A., Thompson, C.R., Hashimi, S., Porter, B., Iyer, S.S., and Kusner, D.J. (2003) Cutting edge: Mycobacterium tuberculosis blocks Ca2+ signaling and phagosome maturation in human macrophages via specific inhibition of sphingosine kinase. J Immunol 170: 2811-2815.
36. Mansour, M.K., Vyas, J.M., and Levitz, S.M. (2011) Dynamic virulence: real-time assessment of intracellular pathogenesis links Cryptococcus neoformans phenotype with clinical outcome. MBio 2: e00217-11.
37. Mottola, G., Boucherit, N., Trouplin, V., Oury Barry, A., Soubeyran, P., Mege, J.L., etal. (2014) Tropheryma whipplei, the agent of Whipple's disease, affects the early to late phagosome transition and survives in a Rab5- and Rab7-positive compartment. PLoS ONE 9: e89367.
38. Nunes, P., and Demaurex, N. (2010) The role of calcium signaling in phagocytosis. J Leukoc Biol 88: 57-68.
39. Orsi, C.F., Colombari, B., Ardizzoni, A., Peppoloni, S., Neglia, R., Posteraro, B., etal. (2009) The ABC transporter-encoding gene AFR1 affects the resistance of Cryptococcus neoformans to microglia-mediated antifungal activity by delaying phagosomal maturation. FEMS Yeast Res 9: 301-310.
40. Park, B.J., Wannemuehler, K.A., Marston, B.J., Govender, N., Pappas, P.G., and Chiller, T.M. (2009) Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 23: 525-530.
41. Purdy, G.E., Owens, R.M., Bennett, L., Russell, D.G., and Butcher, B.A. (2005) Kinetics of phosphatidylinositol-3-phosphate acquisition differ between IgG bead-containing phagosomes and Mycobacterium tuberculosis-containing phagosomes. Cell Microbiol 7: 1627-1634.
42. Qin, Q.M., Luo, J., Lin, X., Pei, J., Li, L., Ficht, T.A., etal. (2011) Functional analysis of host factors that mediate the intracellular lifestyle of Cryptococcus neoformans. PLoS Pathog 7: e1002078.
43. Rutherford, J.C. (2014) The emerging role of urease as a general microbial virulence factor. PLoS Pathog 10: e1004062.
44. Sabiiti, W., Robertson, E., Beale, M.A., Johnston, S.A., Brouwer, A.E., Loyse, A., etal. (2014) Efficient phagocytosis and laccase activity affect the outcome of HIV-associated cryptococcosis. J Clin Invest 124: 2000-2008.
45. Santangelo, R., Zoellner, H., Sorrell, T., Wilson, C., Donald, C., Djordjevic, J., etal. (2004) Role of extracellular phospholipases and mononuclear phagocytes in dissemination of cryptococcosis in a murine model. Infect Immun 72: 2229-2239.
46. Shao, X., Mednick, A., Alvarez, M., van Rooijen, N., Casadevall, A., and Goldman, D.L. (2005) An innate immune system cell is a major determinant of species-related susceptibility differences to fungal pneumonia. J Immunol 175: 3244-3251.
47. Singh, A., Panting, R.J., Varma, A., Saijo, T., Waldron, K.J., Jong, A., etal. (2013) Factors required for activation of urease as a virulence determinant in Cryptococcus neoformans. MBio 4: e00220-13.
48. Smith, L.M., and May, R.C. (2013) Mechanisms of microbial escape from phagocyte killing. Biochem Soc Trans 41: 475-490.
49. Strasser, J.E., Newman, S.L., Ciraolo, G.M., Morris, R.E., Howell, M.L., and Dean, G.E. (1999) Regulation of the macrophage vacuolar ATPase and phagosome-lysosome fusion by Histoplasma capsulatum. J Immunol 162: 6148-6154.
50. Sun, J., Wang, X., Lau, A., Liao, T.Y., Bucci, C., and Hmama, Z. (2010) Mycobacterial nucleoside diphosphate kinase blocks phagosome maturation in murine RAW 264.7 macrophages. PLoS ONE 5: e8769.
51. Tejle, K., Magnusson, K.E., and Rasmusson, B. (2002) Phagocytosis and phagosome maturation are regulated by calcium in J774 macrophages interacting with unopsonized prey. Biosci Rep 22: 529-540.
52. Tucker, S.C., and Casadevall, A. (2002) Replication of Cryptococcus neoformans in macrophages is accompanied by phagosomal permeabilization and accumulation of vesicles containing polysaccharide in the cytoplasm. Proc Natl Acad Sci USA 99: 3165-3170.
53. Vecchiarelli, A., Pietrella, D., Dottorini, M., Monari, C., Retini, C., Todisco, T., etal. (1994) Encapsulation of Cryptococcus neoformans regulates fungicidal activity and the antigen presentation process in human alveolar macrophages. Clin Exp Immunol 98: 217-223.
54. Vecchiarelli, A., Pericolini, E., Gabrielli, E., Kenno, S., Perito, S., Cenci, E., etal. (2013) Elucidating the immunological function of the Cryptococcus neoformans capsule. Future Microbiol 8: 1107-1116.
55. Vergne, I., Chua, J., and Deretic, V. (2003) Tuberculosis toxin blocking phagosome maturation inhibits a novel Ca2+/calmodulin-PI3K hVPS34 cascade. J Exp Med 198: 653-659.
56. Via, L.E., Deretic, D., Ulmer, R.J., Hibler, N.S., Huber, L.A., and Deretic, V. (1997) Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7. J Biol Chem 272: 13326-13331.
57. Vylkova, S., and Lorenz, M.C. (2014) Modulation of phagosomal pH by Candida albicans promotes hyphal morphogenesis and requires Stp2p, a regulator of amino acid transport. PLoS Pathog 10: e1003995.