Cryptococcus neoformans-induced macrophage lysosome damage crucially contributes to fungal virulence

Journal of Immunology

Volumn 194, Issue 5, 2015, Pages 2219-2231

  Davis, Michael J ^a,f   Eastman, Alison J ^a,b   Qiu, Yafeng ^a,c,g   Gregorka, Brian ^d   Kozel, Thomas R ^e   Osterholzer, John J ^a,c   Curtis, Jeffrey L ^a,b,c   Swanson, Joel A ^d   Olszewski, Michal A ^a,b,c  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

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

^g Key Lab of Grazing Animal Diseases MOA Key Lab of Veterinary Parasitology of Gansu Province   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CELL DAMAGE; CELL KILLING; CELL PROLIFERATION; CONTROLLED STUDY; CORRELATION ANALYSIS; CRYPTOCOCCUS NEOFORMANS; CYTOKINE RESPONSE; FLOW CYTOMETRY; FUNGAL REPRODUCTION; FUNGAL VIABILITY; FUNGAL VIRULENCE; FUNGUS GROWTH; IN VITRO STUDY; IN VIVO STUDY; LUNG ALVEOLUS CELL; LUNG ALVEOLUS MACROPHAGE; LYSOSOME; MACROPHAGE; MACROPHAGE ACTIVATION; MICROSCOPY; MOUSE; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; ANIMAL; BAGG ALBINO MOUSE; CRYPTOCOCCOSIS; DRUG EFFECTS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; LIGHT; LUNG; LUNG DISEASES, FUNGAL; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PHOTOCHEMISTRY; PRIMARY CELL CULTURE; RADIATION RESPONSE; VIRULENCE;

ANIMALS; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; HOST-PATHOGEN INTERACTIONS; INTERFERON-GAMMA; LIGHT; LUNG; LUNG DISEASES, FUNGAL; LYSOSOMES; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED BALB C; PHOTOCHEMICAL PROCESSES; PRIMARY CELL CULTURE; VIRULENCE;

EID: 84924370559     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402376     Document Type: Article

References (72)

1. Park, B. J., K. A. Wannemuehler, B. J. Marston, N. Govender, P. G. Pappas, and T. M. Chiller. 2009. Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 23: 525-530.
2. Chuck, S. L., and M. A. Sande. 1989. Infections with Cryptococcus neoformans in the acquired immunodeficiency syndrome. N. Engl. J. Med. 321: 794-799.
3. Olszewski, M. A., Y. Zhang, and G. B. Huffnagle. 2010. Mechanisms of cryptococcal virulence and persistence. Future Microbiol. 5: 1269-1288.
4. Baddley, J. W., J. R. Perfect, R. A. Oster, R. A. Larsen, G. A. Pankey, H. Henderson, D. W. Haas, C. A. Kauffman, R. Patel, A. K. Zaas, and P. G. Pappas. 2008. Pulmonary cryptococcosis in patients without HIV infection: factors associated with disseminated disease. Eur. J. Clin. Microbiol. Infect. Dis. 27: 937-943.
5. Feldmesser, M., Y. Kress, P. Novikoff, and A. Casadevall. 2000. Cryptococcus neoformans is a facultative intracellular pathogen in murine pulmonary infection. Infect. Immun. 68: 4225-4237.
6. Osterholzer, J. J., G. H. Chen, M. A. Olszewski, Y. M. Zhang, J. L. Curtis, G. B. Huffnagle, and G. B. Toews. 2011. Chemokine receptor 2-mediated accumulation of fungicidal exudate macrophages in mice that clear cryptococcal lung infection. Am. J. Pathol. 178: 198-211.
7. Osterholzer, J. J., R. Surana, J. E. Milam, G. T. Montano, G. H. Chen, J. Sonstein, J. L. Curtis, G. B. Huffnagle, G. B. Toews, and M. A. Olszewski. 2009. Cryptococcal urease promotes the accumulation of immature dendritic cells and a non-protective T2 immune response within the lung. Am. J. Pathol. 174: 932-943.
8. Arora, S., Y. Hernandez, J. R. Erb-Downward, R. A. McDonald, G. B. Toews, and G. B. Huffnagle. 2005. Role of IFN-gamma in regulating T2 immunity and the development of alternatively activated macrophages during allergic bronchopulmonary mycosis. J. Immunol. 174: 6346-6356.
9. Müller, U., W. Stenzel, G. Köhler, C. Werner, T. Polte, G. Hansen, N. Schütze, R. K. Straubinger, M. Blessing, A. N. McKenzie, et al. 2007. IL-13 induces disease-promoting type 2 cytokines, alternatively activated macrophages and allergic inflammation during pulmonary infection of mice with Cryptococcus neoformans. J. Immunol. 179: 5367-5377.
10. Voelz, K., D. A. Lammas, and R. C. May. 2009. Cytokine signaling regulates the outcome of intracellular macrophage parasitism by Cryptococcus neoformans. Infect. Immun. 77: 3450-3457.
11. Hardison, S. E., S. Ravi, K. L. Wozniak, M. L. Young, M. A. Olszewski, and F. L. Wormley, Jr. 2010. Pulmonary infection with an interferon-gamma-producing Cryptococcus neoformans strain results in classical macrophage activation and protection. Am. J. Pathol. 176: 774-785.
12. Zhang, Y., F. Wang, K. C. Tompkins, A. McNamara, A. V. Jain, B. B. Moore, G. B. Toews, G. B. Huffnagle, and M. A. Olszewski. 2009. Robust Th1 and Th17 immunity supports pulmonary clearance but cannot prevent systemic dissemination of highly virulent Cryptococcus neoformans H99. Am. J. Pathol. 175: 2489-2500.
13. Syme, R. M., T. F. Bruno, T. R. Kozel, and C. H. Mody. 1999. The capsule of Cryptococcus neoformans reduces T-lymphocyte proliferation by reducing phagocytosis, which can be restored with anticapsular antibody. Infect. Immun. 67: 4620-4627.
14. Syme, R. M., J. C. Spurrell, E. K. Amankwah, F. H. Green, and C. H. Mody. 2002. Primary dendritic cells phagocytose Cryptococcus neoformans via mannose receptors and Fcgamma receptor II for presentation to T lymphocytes. Infect. Immun. 70: 5972-5981.
15. Syme, R. M., J. C. Spurrell, L. L. Ma, F. H. Green, and C. H. Mody. 2000. Phagocytosis and protein processing are required for presentation of Cryptococcus neoformans mitogen to T lymphocytes. Infect. Immun. 68: 6147-6153.
16. Arora, S., R. A. McDonald, G. B. Toews, and G. B. Huffnagle. 2006. Effect of a CD4-depleting antibody on the development of Cryptococcus neoformans-induced allergic bronchopulmonary mycosis in mice. Infect. Immun. 74: 4339-4348.
17. Lindell, D. M., T. A. Moore, R. A. McDonald, G. B. Toews, and G. B. Huffnagle. 2005. Generation of antifungal effector CD8+ T cells in the absence of CD4+ T cells during Cryptococcus neoformans infection. J. Immunol. 174: 7920-7928.
18. Lindell, D. M., T. A. Moore, R. A. McDonald, G. B. Toews, and G. B. Huffnagle. 2006. Distinct compartmentalization of CD4+ T-cell effector function versus proliferative capacity during pulmonary cryptococcosis. Am. J. Pathol. 168: 847-855.
19. Huffnagle, G. B., M. F. Lipscomb, J. A. Lovchik, K. A. Hoag, and N. E. Street. 1994. The role of CD4+ and CD8+ T cells in the protective inflammatory response to a pulmonary cryptococcal infection. J. Leukoc. Biol. 55: 35-42.
20. Huffnagle, G. B., J. L. Yates, and M. F. Lipscomb. 1991. Immunity to a pulmonary Cryptococcus neoformans infection requires both CD4+ and CD8+ T cells. J. Exp. Med. 173: 793-800.
21. Artavanis-Tsakonas, K., P. V. Kasperkovitz, E. Papa, M. L. Cardenas, N. S. Khan, A. G. Van der Veen, H. L. Ploegh, and J. M. Vyas. 2011. The tetraspanin CD82 is specifically recruited to fungal and bacterial phagosomes prior to acidification. Infect. Immun. 79: 1098-1106.
22. Artavanis-Tsakonas, K., J. C. Love, H. L. Ploegh, and J. M. Vyas. 2006. Recruitment of CD63 to Cryptococcus neoformans phagosomes requires acidification. Proc. Natl. Acad. Sci. USA 103: 15945-15950.
23. Hole, C. R., H. Bui, F. L. Wormley, Jr., and K. L. Wozniak. 2012. Mechanisms of dendritic cell lysosomal killing of Cryptococcus. Sci Rep 2: 739.
24. Levitz, S. M., S. H. Nong, K. F. Seetoo, T. S. Harrison, R. A. Speizer, and E. R. Simons. 1999. Cryptococcus neoformans resides in an acidic phagolysosome of human macrophages. Infect. Immun. 67: 885-890.
25. Weber, S. M., and S. M. Levitz. 2001. Chloroquine antagonizes the proinflammatory cytokine response to opportunistic fungi by alkalizing the fungal phagolysosome. J. Infect. Dis. 183: 935-942.
26. Wozniak, K. L., and S. M. Levitz. 2008. Cryptococcus neoformans enters the endolysosomal pathway of dendritic cells and is killed by lysosomal components. Infect. Immun. 76: 4764-4771.
27. Christensen, K. A., J. T. Myers, and J. A. Swanson. 2002. pH-dependent regulation of lysosomal calcium in macrophages. J. Cell Sci. 115: 599-607.
28. Kinchen, J. M., and K. S. Ravichandran. 2008. Phagosome maturation: going through the acid test. Nat. Rev. Mol. Cell Biol. 9: 781-795.
29. El-Kirat-Chatel, S., and Y. F. Dufrêne. 2012. Nanoscale imaging of the Candidamacrophage interaction using correlated fluorescence-atomic force microscopy. ACS Nano 6: 10792-10799.
30. Tucker, S. C., and A. Casadevall. 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.
31. Johnston, S. A., and R. C. May. 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.
32. Davis, M. J., T. M. Tsang, Y. Qiu, J. K. Dayrit, J. B. Freij, G. B. Huffnagle, and M. A. Olszewski. 2013. Macrophage M1/M2 polarization dynamically adapts to changes in cytokine microenvironments in Cryptococcus neoformans infection. MBio 4: e00264-e13.
33. Nicola, A. M., E. J. Robertson, P. Albuquerque, Lda. S. Derengowski, and A. Casadevall. 2011. Nonlytic exocytosis of Cryptococcus neoformans from macrophages occurs in vivo and is influenced by phagosomal pH. MBio 2: 2.
34. Davis, M. J., B. Gregorka, J. E. Gestwicki, and J. A. Swanson. 2012. Inducible renitence limits Listeria monocytogenes escape from vacuoles in macrophages. J. Immunol. 189: 4488-4495.
35. Davis, M. J., and J. A. Swanson. 2010. Technical advance: Caspase-1 activation and IL-1β release correlate with the degree of lysosome damage, as illustrated by a novel imaging method to quantify phagolysosome damage. J. Leukoc. Biol. 88: 813-822.
36. Swanson, J. A. 1989. Phorbol esters stimulate macropinocytosis and solute flow through macrophages. J. Cell Sci. 94: 135-142.
37. Brandt, S., P. Thorkildson, and T. R. Kozel. 2003. Monoclonal antibodies reactive with immunorecessive epitopes of glucuronoxylomannan, the major capsular polysaccharide of Cryptococcus neoformans. Clin. Diagn. Lab. Immunol. 10: 903-909.
38. Kirkegaard, T., A. G. Roth, N. H. Petersen, A. K. Mahalka, O. D. Olsen, I. Moilanen, A. Zylicz, J. Knudsen, K. Sandhoff, C. Arenz, et al. 2010. Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature 463: 549-553.
39. Qiu, Y., M. J. Davis, J. K. Dayrit, Z. Hadd, D. L. Meister, J. J. Osterholzer, P. R. Williamson, and M. A. Olszewski. 2012. Immune modulation mediated by cryptococcal laccase promotes pulmonary growth and brain dissemination of virulent Cryptococcus neoformans in mice. PLoS ONE 7: e47853.
40. Chen, G. H., D. A. McNamara, Y. Hernandez, G. B. Huffnagle, G. B. Toews, and M. A. Olszewski. 2008. Inheritance of immune polarization patterns is linked to resistance versus susceptibility to Cryptococcus neoformans in a mouse model. Infect. Immun. 76: 2379-2391.
41. McCubbrey, A. L., J. Sonstein, T. M. Ames, C. M. Freeman, and J. L. Curtis. 2012. Glucocorticoids relieve collectin-driven suppression of apoptotic cell uptake in murine alveolar macrophages through downregulation of SIRPα. J. Immunol. 189: 112-119.
42. Huotari, J., and A. Helenius. 2011. Endosome maturation. EMBO J. 30: 3481-3500.
43. Osterholzer, J. J., J. E. Milam, G. H. Chen, G. B. Toews, G. B. Huffnagle, and M. A. Olszewski. 2009. Role of dendritic cells and alveolar macrophages in regulating early host defense against pulmonary infection with Cryptococcus neoformans. Infect. Immun. 77: 3749-3758.
44. Vermaelen, K., and R. Pauwels. 2004. Accurate and simple discrimination of mouse pulmonary dendritic cell and macrophage populations by flow cytometry: methodology and new insights. Cytometry A 61: 170-177.
45. Nicola, A. M., S. Frases, and A. Casadevall. 2009. Lipophilic dye staining of Cryptococcus neoformans extracellular vesicles and capsule. Eukaryot. Cell 8:1373-1380.
46. Alanio, A., M. Desnos-Ollivier, and F. Dromer. 2011. Dynamics of Cryptococcus neoformans-macrophage interactions reveal that fungal background influences outcome during cryptococcal meningoencephalitis in humans. MBio 2: 2.
47. Leenen, P. J., B. P. Canono, D. A. Drevets, J. S. Voerman, and P. A. Campbell. 1994. TNF-alpha and IFN-gamma stimulate a macrophage precursor cell line to kill Listeria monocytogenes in a nitric oxide-independent manner. J. Immunol. 153: 5141-5147.
48. Bermudez, L. E., and L. S. Young. 1988. Tumor necrosis factor, alone or in combination with IL-2, but not IFN-gamma, is associated with macrophage killing of Mycobacterium avium complex. J. Immunol. 140: 3006-3013.
49. Alvarez, M., and A. Casadevall. 2006. Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages. Curr. Biol. 16: 2161-2165.
50. Ma, H., J. E. Croudace, D. A. Lammas, and R. C. May. 2006. Expulsion of live pathogenic yeast by macrophages. Curr. Biol. 16: 2156-2160.
51. Stukes, S. A., H. W. Cohen, and A. Casadevall. 2014. Temporal kinetics and quantitative analysis of Cryptococcus neoformans nonlytic exocytosis. Infect. Immun. 82: 2059-2067.
52. Coelho, C., A. C. O. Souza, L. S. Derengowski, C. de Leon-Rodriguez, B. Wang, R. Leon-Rivera, A. L. Bocca, T. Gonçalves, and A. Casadevall. 2014. Macrophage mitochondrial and stress response to ingestion of Cryptococcus neoformans. J. Immunol. 194: 2345-2357.
53. Hornung, V., F. Bauernfeind, A. Halle, E. O. Samstad, H. Kono, K. L. Rock, K. A. Fitzgerald, and E. Latz. 2008. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9: 847-856.
54. Deepe, G. S., Jr., and W. R. Buesing. 2012. Deciphering the pathways of death of Histoplasma capsulatum-infected macrophages: implications for the immunopathogenesis of early infection. J. Immunol. 188: 334-344.
55. Gross, O., H. Poeck, M. Bscheider, C. Dostert, N. Hannesschläger, S. Endres, G. Hartmann, A. Tardivel, E. Schweighoffer, V. Tybulewicz, et al. 2009. Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence. Nature 459: 433-436.
56. Hise, A. G., J. Tomalka, S. Ganesan, K. Patel, B. A. Hall, G. D. Brown, and K. A. Fitzgerald. 2009. An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 5: 487-497.
57. Saïd-Sadier, N., E. Padilla, G. Langsley, and D. M. Ojcius. 2010. Aspergillus fumigatus stimulates the NLRP3 inflammasome through a pathway requiring ROS production and the Syk tyrosine kinase. PLoS ONE 5: e10008.
58. Zang, Y., R. L. Beard, R. A. Chandraratna, and J. X. Kang. 2001. Evidence of a lysosomal pathway for apoptosis induced by the synthetic retinoid CD437 in human leukemia HL-60 cells. Cell Death Differ. 8: 477-485.
59. Cirman, T., K. Oresić, G. D. Mazovec, V. Turk, J. C. Reed, R. M. Myers, G. S. Salvesen, and B. Turk. 2004. Selective disruption of lysosomes in HeLa cells triggers apoptosis mediated by cleavage of Bid by multiple papain-like lysosomal cathepsins. J. Biol. Chem. 279: 3578-3587.
60. Heinrich, M., J. Neumeyer, M. Jakob, C. Hallas, V. Tchikov, S. Winoto-Morbach, M. Wickel, W. Schneider-Brachert, A. Trauzold, A. Hethke, and S. Schütze. 2004. Cathepsin D links TNF-induced acid sphingomyelinase to Bid-mediated caspase-9 and -3 activation. Cell Death Differ. 11: 550-563.
61. Nagaraj, N. S., N. Vigneswaran, and W. Zacharias. 2006. Cathepsin B mediates TRAIL-induced apoptosis in oral cancer cells. J. Cancer Res. Clin. Oncol. 132: 171-183.
62. Sandes, E., C. Lodillinsky, R. Cwirenbaum, C. Argüelles, A. Casabé, and A. M. Eiján. 2007. Cathepsin B is involved in the apoptosis intrinsic pathway induced by Bacillus Calmette-Guérin in transitional cancer cell lines. Int. J. Mol. Med. 20: 823-828.
63. Yacoub, A., M. A. Park, P. Gupta, M. Rahmani, G. Zhang, H. Hamed, D. Hanna, D. Sarkar, I. V. Lebedeva, L. Emdad, et al. 2008. Caspase-, cathepsin-, and PERK-dependent regulation of MDA-7/IL-24-induced cell killing in primary human glioma cells. Mol. Cancer Ther. 7: 297-313.
64. Guicciardi, M. E., S. F. Bronk, N. W. Werneburg, X. M. Yin, and G. J. Gores. 2005. Bid is upstream of lysosome-mediated caspase 2 activation in tumor necrosis factor alpha-induced hepatocyte apoptosis. Gastroenterology 129: 269-284.
65. Hishita, T., S. Tada-Oikawa, K. Tohyama, Y. Miura, T. Nishihara, Y. Tohyama, Y. Yoshida, T. Uchiyama, and S. Kawanishi. 2001. Caspase-3 activation by lysosomal enzymes in cytochrome c-independent apoptosis in myelodysplastic syndrome-derived cell line P39. Cancer Res. 61: 2878-2884.
66. Chen, W., N. Li, T. Chen, Y. Han, C. Li, Y. Wang, W. He, L. Zhang, T. Wan, and X. Cao. 2005. The lysosome-associated apoptosis-inducing protein containing the pleckstrin homology (PH) and FYVE domains (LAPF), representative of a novel family of PH and FYVE domain-containing proteins, induces caspase-independent apoptosis via the lysosomal-mitochondrial pathway. J. Biol. Chem. 280: 40985-40995.
67. Boya, P., and G. Kroemer. 2008. Lysosomal membrane permeabilization in cell death. Oncogene 27: 6434-6451.
68. Kågedal, K., A. C. Johansson, U. Johansson, G. Heimlich, K. Roberg, N. S. Wang, J. M. Jürgensmeier, and K. Ollinger. 2005. Lysosomal membrane permeabilization during apoptosis-involvement of Bax? Int. J. Exp. Pathol. 86: 309-321.
69. Feldstein, A. E., N. W. Werneburg, A. Canbay, M. E. Guicciardi, S. F. Bronk, R. Rydzewski, L. J. Burgart, and G. J. Gores. 2004. Free fatty acids promote hepatic lipotoxicity by stimulating TNF-alpha expression via a lysosomal pathway. Hepatology 40: 185-194.
70. Feldstein, A. E., N.W. Werneburg, Z. Li, S. F. Bronk, and G. J. Gores. 2006. Bax inhibition protects against free fatty acid-induced lysosomal permeabilization. Am. J. Physiol. Gastrointest. Liver Physiol. 290: G1339-G1346.
71. Werneburg, N. W., M. E. Guicciardi, S. F. Bronk, S. H. Kaufmann, and G. J. Gores. 2007. Tumor necrosis factor-related apoptosis-inducing ligand activates a lysosomal pathway of apoptosis that is regulated by Bcl-2 proteins. J. Biol. Chem. 282: 28960-28970.
72. Sköld, M., and S. M. Behar. 2008. Tuberculosis triggers a tissue-dependent program of differentiation and acquisition of effector functions by circulating monocytes. J. Immunol. 181: 6349-6360.