Murine Models of Cryptococcus Infection.
Cryptococcus gattii
Cryptococus neoformans
bronchoalveolar lavage
flow cytometry
fungal infection
immune responses
intranasal inhalation
Journal
Current protocols
ISSN: 2691-1299
Titre abrégé: Curr Protoc
Pays: United States
ID NLM: 101773894
Informations de publication
Date de publication:
Mar 2024
Mar 2024
Historique:
medline:
8
3
2024
pubmed:
8
3
2024
entrez:
8
3
2024
Statut:
ppublish
Résumé
Cryptococcus is recognized as one of the emerging fungal pathogens that have major impact on diverse populations worldwide. Because of the high mortality rate and limited antifungal therapy options, there is an urgent need to understand the impact of dynamic processes between fungal pathogens and hosts that influence cryptococcal pathogenesis and disease outcomes. With known common limitations in human studies, experimental murine cryptococcosis models that can recapitulate human disease provide a valuable tool for studying fungal virulence and the host interaction, leading to development of better treatment strategies. Infection with Cryptococcus in mice via intranasal inhalation is mostly used because it is noninvasive and considered to be the most common mode of infection, strongly correlating with cryptococcal disease in humans. The protocols described in this article provide the procedures of establishing a murine model of Cryptococcus infection by intranasal inhalation and assessing the host immune response and disease progression during Cryptococcus infection. © 2024 Wiley Periodicals LLC. Basic Protocol 1: Murine model of pulmonary cryptococcal infection via intranasal inhalation Basic Protocol 2: Assessment of the pulmonary immune response during Cryptococcus infection Support Protocol: Evaluation of pulmonary gene expression by real-time PCR Basic Protocol 3: Enumeration of survival rate and organ fungal burden.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1001Informations de copyright
© 2024 Wiley Periodicals LLC.
Références
Anderson, D. A., & Sagha, H. M. (1988). Persistence of infection in mice inoculated intranasally with Cryptococcus neoformans. Mycopathologia, 104(3), 163-169. https://doi.org/10.1007/BF00437432
Angkasekwinai, P., Sringkarin, N., Supasorn, O., Fungkrajai, M., Wang, Y. H., Chayakulkeeree, M., Ngamskulrungroj, P., Angkasekwinai, N., & Pattanapanyasat, K. (2014). Cryptococcus gattii infection dampens Th1 and Th17 responses by attenuating dendritic cell function and pulmonary chemokine expression in the immunocompetent hosts. Infection and Immunity, 82(9), 3880-3890. https://doi.org/10.1128/iai.01773-14
Arora, S., Hernandez, Y., Erb-Downward, J. R., McDonald, R. A., Toews, G. B., & Huffnagle, G. B. (2005). Role of IFN-γ in regulating T2 immunity and the development of alternatively activated macrophages during allergic bronchopulmonary mycosis. The Journal of Immunology, 174(10), 6346-6356. https://doi.org/10.4049/jimmunol.174.10.6346
Bava, A. J., & Negroni, R. (1992). Comparative study of six antifungal treatments in an experimental model of murine cryptococcosis. European Journal of Epidemiology, 8(3), 422-426. https://doi.org/10.1007/BF00158577
Block, E. R., & Bennett, J. E. (1973). The combined effect of 5-fluorocytosine and amphotericin B in the therapy of murine cryptococcosis. Proceedings of the Society for Experimental Biology and Medicine, 142(2), 476-480. https://doi.org/10.3181/00379727-142-37049
Bockamp, E., Maringer, M., Spangenberg, C., Fees, S., Fraser, S., Eshkind, L., Oesch, F., & Zabel, B. (2002). Of mice and models: Improved animal models for biomedical research. Physiological Genomics, 11(3), 115-132. https://doi.org/10.1152/physiolgenomics.00067.2002
Burki, T. (2023). WHO publish fungal priority pathogens list. The Lancet Microbe, 4(2), e74. https://doi.org/10.1016/S2666-5247(23)00003-4
Capilla, J., Maffei, C. M., Clemons, K. V., Sobel, R. A., & Stevens, D. A. (2006). Experimental systemic infection with Cryptococcus neoformans var. grubii and Cryptococcus gattii in normal and immunodeficient mice. Medical Mycology, 44(7), 601-610. https://doi.org/10.1080/13693780600810040
Charlier, C., Nielsen, K., Daou, S., Brigitte, M., Chretien, F., & Dromer, F. (2009). Evidence of a role for monocytes in dissemination and brain invasion by Cryptococcus neoformans. Infection and Immunity, 77(1), 120-127. https://doi.org/10.1128/IAI.01065-08
Chen, G.-H., McNamara, D. A., Hernandez, Y., Huffnagle, G. B., Toews, G. B., & Olszewski, M. A. (2008). Inheritance of immune polarization patterns is linked to resistance versus susceptibility to Cryptococcus neoformans in a mouse model. Infection and Immunity, 76(6), 2379-2391. https://doi.org/10.1128/IAI.01143-07
Chen, S. C., Meyer, W., & Sorrell, T. C. (2014). Cryptococcus gattii infections. Clinical Microbiology Reviews, 27(4), 980-1024. https://doi.org/10.1128/CMR.00126-13
Chretien, F., Lortholary, O., Kansau, I., Neuville, S., Gray, F., & Dromer, F. (2002). Pathogenesis of cerebral Cryptococcus neoformans infection after fungemia. Journal of Infectious Diseases, 186(4), 522-530. https://doi.org/10.1086/341564
Coelho, C., Camacho, E., Salas, A., Alanio, A., & Casadevall, A. (2019). Intranasal Inoculation of Cryptococcus neoformans in mice produces nasal infection with rapid brain dissemination. mSphere, 4(4), e00483-19. https://doi.org/10.1128/mSphere.00483-19
Coelho, C., & Casadevall, A. (2016). Cryptococcal therapies and drug targets: The old, the new and the promising. Cellular Microbiology, 18(6), 792-799. https://doi.org/10.1111/cmi.12590
Davis, M. J., Tsang, T. M., Qiu, Y., Dayrit, J. K., Freij, J. B., Huffnagle, G. B., & Olszewski, M. A. (2013). Macrophage M1/M2 polarization dynamically adapts to changes in cytokine microenvironments in Cryptococcus neoformans infection. mBio, 4(3), e00264-00213. https://doi.org/10.1128/mBio.00264-13
Decken, K., Köhler, G., Palmer-Lehmann, K., Wunderlin, A., Mattner, F., Magram, J., Gately, M. K., & Alber, G. (1998). Interleukin-12 is essential for a protective Th1 response in mice infected with Cryptococcus neoformans. Infection and Immunity, 66(10), 4994-5000. https://doi.org/10.1128/IAI.66.10.4994-5000.1998
Ding, M., Smith, K. D., Wiesner, D. L., Nielsen, J. N., Jackson, K. M., & Nielsen, K. (2021). Use of clinical isolates to establish criteria for a mouse model of latent Cryptococcus neoformans Infection. Frontiers in Cellular and Infection Microbiology, 11, 804059. https://doi.org/10.3389/fcimb.2021.804059
Fisher, M. C., & Denning, D. W. (2023). The WHO fungal priority pathogens list as a game-changer. Nature Reviews Microbiology, 21(4), 211-212. https://doi.org/10.1038/s41579-023-00861-x
Flaczyk, A., Duerr, C. U., Shourian, M., Lafferty, E. I., Fritz, J. H., & Qureshi, S. T. (2013). IL-33 signaling regulates innate and adaptive immunity to Cryptococcus neoformans. The Journal of Immunology, 191(5), 2503-2513. https://doi.org/10.4049/jimmunol.1300426
Fukushima, A., Yamaguchi, T., Ishida, W., Fukata, K., Taniguchi, T., Liu, F.-T., & Ueno, H. (2006). Genetic background determines susceptibility to experimental immune-mediated blepharoconjunctivitis: Comparison of Balb/c and C57BL/6 mice. Experimental Eye Research, 82(2), 210-218. https://doi.org/10.1016/j.exer.2005.06.010
Gibson, J. F., & Johnston, S. A. (2015). Immunity to Cryptococcus neoformans and C. gattii during cryptococcosis. Fungal Genetics and Biology, 78, 76-86. https://doi.org/10.1016/j.fgb.2014.11.006
Goldman, D. L., Lee, S. C., Mednick, A. J., Montella, L., & Casadevall, A. (2000). Persistent Cryptococcus neoformans pulmonary infection in the rat is associated with intracellular parasitism, decreased inducible nitric oxide synthase expression, and altered antibody responsiveness to cryptococcal polysaccharide. Infection and Immunity, 68(2), 832-838. https://doi.org/10.1128/IAI.68.2.832-838.2000
Guess, T., Lai, H., Smith, S. E., Sircy, L., Cunningham, K., Nelson, D. E., & McClelland, E. E. (2018). Size matters: Measurement of capsule diameter in Cryptococcus neoformans. JoVE (Journal of Visualized Experiments), (132), e57171. https://doi.org/10.3791/57171
Hamed, M. F., Enriquez, V., Munzen, M. E., Charles-Niño, C. L., Mihu, M. R., Khoshbouei, H., Alviña, K., & Martinez, L. R. (2023). Clinical and pathological characterization of central nervous system cryptococcosis in an experimental mouse model of stereotaxic intracerebral infection. PLOS Neglected Tropical Diseases, 17(1), e0011068. https://doi.org/10.1371/journal.pntd.0011068
Hamilton, J. D., & Elliott, D. M. (1975). Combined activity of amphotericin B and 5-fluorocytosine against Cryptococcus neoformans in vitro and in vivo in mice. Journal of Infectious Diseases, 131(2), 129-137. https://doi.org/10.1093/infdis/131.2.129
Hansakon, A., Jeerawattanawart, S., Pattanapanyasat, K., & Angkasekwinai, P. (2020). IL-25 receptor signaling modulates host defense against Cryptococcus neoformans infection. The Journal of Immunology, 205(3), 674-685. https://doi.org/10.4049/jimmunol.2000073
Hansakon, A., Mutthakalin, P., Ngamskulrungroj, P., Chayakulkeeree, M., & Angkasekwinai, P. (2019). Cryptococcus neoformans and Cryptococcus gattii clinical isolates from Thailand display diverse phenotypic interactions with macrophages. Virulence, 10(1), 26-36. https://doi.org/10.1080/21505594.2018.1556150
Hansakon, A., Ngamphiw, C., Tongsima, S., & Angkasekwinai, P. (2023). Arginase 1 expression by macrophages promotes Cryptococcus neoformans proliferation and invasion into brain microvascular endothelial cells. Journal of Immunology, 210(4), 408-419. https://doi.org/10.4049/jimmunol.2200592
Hardison, S. E., Ravi, S., Wozniak, K. L., Young, M. L., Olszewski, M. A., & Wormley, F. L. Jr. (2010). Pulmonary infection with an interferon-gamma-producing Cryptococcus neoformans strain results in classical macrophage activation and protection. American Journal of Pathology, 176(2), 774-785. https://doi.org/10.2353/ajpath.2010.090634
Hoag, K. A., Lipscomb, M. F., Izzo, A. A., & Street, N. E. (1997). IL-12 and IFN-gamma are required for initiating the protective Th1 response to pulmonary cryptococcosis in resistant C.B-17 mice. American Journal of Respiratory Cell and Molecular Biology, 17(6), 733-739. https://doi.org/10.1165/ajrcmb.17.6.2879
Iyer, K. R., Revie, N. M., Fu, C., Robbins, N., & Cowen, L. E. (2021). Treatment strategies for cryptococcal infection: Challenges, advances and future outlook. Nature Reviews Microbiology, 19(7), 454-466. https://doi.org/10.1038/s41579-021-00511-0
Jackson, K. M., Ding, M., & Nielsen, K. (2023). Importance of clinical isolates in Cryptococcus neoformans research. Journal of Fungi, 9(3), 364. https://doi.org/10.3390/jof9030364
Jain, A. V., Zhang, Y., Fields, W. B., McNamara, D. A., Choe, M. Y., Chen, G. H., Erb-Downward, J., Osterholzer, J. J., Toews, G. B., Huffnagle, G. B., & Olszewski, M. A. (2009). Th2 but not Th1 immune bias results in altered lung functions in a murine model of pulmonary Cryptococcus neoformans infection. Infection and Immunity, 77(12), 5389-5399. https://doi.org/10.1128/IAI.00809-09
Kawakami, K., Kohno, S., Morikawa, N., Kadota, J., Saito, A., & Hara, K. (1994). Activation of macrophages and expansion of specific T lymphocytes in the lungs of mice intratracheally inoculated with Cryptococcus neoformans. Clinical and Experimental Immunology, 96(2), 230-237. https://doi.org/10.1111/j.1365-2249.1994.tb06547.x
Kwon-Chung, K. J., Fraser, J. A., Doering, T. L., Wang, Z., Janbon, G., Idnurm, A., & Bahn, Y. S. (2014). Cryptococcus neoformans and Cryptococcus gattii, the etiologic agents of cryptococcosis. Cold Spring Harbor Perspectives in Medicine, 4(7), a019760. https://doi.org/10.1101/cshperspect.a019760
Leopold Wager, C. M., Hole, C. R., Wozniak, K. L., Olszewski, M. A., Mueller, M., & Wormley, F. L. Jr. (2015). STAT1 signaling within macrophages is required for antifungal activity against Cryptococcus neoformans. Infection and Immunity, 83(12), 4513-4527. https://doi.org/10.1128/IAI.00935-15
Lim, T. S., Murphy, J. W., & Cauley, L. K. (1980). Host-etiological agent interactions in intranasally and intraperitoneally induced Cryptococcosis in mice. Infection and Immunity, 29(2), 633-641. https://doi.org/10.1128/iai.29.2.633-641.1980
Lortholary, O., Improvisi, L., Nicolas, M., Provost, F., Dupont, B., & Dromer, F. (1999). Fungemia during murine cryptococcosis sheds some light on pathophysiology. Medical Mycology, 37(3), 169-174. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/10421848
May, R. C., Stone, N. R., Wiesner, D. L., Bicanic, T., & Nielsen, K. (2016). Cryptococcus: From environmental saprophyte to global pathogen. Nature Reviews Microbiology, 14(2), 106-117. https://doi.org/10.1038/nrmicro.2015.6
Maziarz, E. K., & Perfect, J. R. (2016). Cryptococcosis. Infectious Disease Clinics of North America, 30(1), 179-206. https://doi.org/10.1016/j.idc.2015.10.006
Mourad, A., & Perfect, J. R. (2018). Present and future therapy of Cryptococcus infections. Journal of Fungi, 4(3), 79. https://doi.org/10.3390/jof4030079
Mpoza, E., Rhein, J., & Abassi, M. (2018). Emerging fluconazole resistance: Implications for the management of cryptococcal meningitis. Medical Mycology Case Reports, 19, 30-32. https://doi.org/10.1016/j.mmcr.2017.11.004
Mukaremera, L., McDonald, T. R., Nielsen, J. N., Molenaar, C. J., Akampurira, A., Schutz, C., Taseera, K., Muzoora, C., Meintjes, G., Meya, D. B., Boulware, D. R., & Nielsen, K. (2019). The mouse inhalation model of Cryptococcus neoformans infection recapitulates strain virulence in humans and shows that closely related strains can possess differential virulence. Infection and Immunity, 87(5), e00046-19. https://doi.org/10.1128/IAI.00046-19
Neal, L. M., Xing, E., Xu, J., Kolbe, J. L., Osterholzer, J. J., Segal, B. M., Williamson, P. R., & Olszewski, M. A. (2017). CD4(+) T cells orchestrate lethal immune pathology despite fungal clearance during Cryptococcus neoformans Meningoencephalitis. mBio, 8(6), e01415-17. https://doi.org/10.1128/mBio.01415-17
Ngamskulrungroj, P., Chang, Y., Sionov, E., & Kwon-Chung, K. J. (2012). The primary target organ of Cryptococcus gattii is different from that of Cryptococcus neoformans in a murine model. mBio, 3(3), e00103-12. https://doi.org/10.1128/mBio.00103-12
Normile, T. G., Bryan, A. M., & Del Poeta, M. (2020). Animal Models of Cryptococcus neoformans in identifying immune parameters associated with primary infection and reactivation of latent infection. Frontiers in Immunology, 11, 581750. https://doi.org/10.3389/fimmu.2020.581750
Rajasingham, R., Govender, N. P., Jordan, A., Loyse, A., Shroufi, A., Denning, D. W., Meya, D. B., Chiller, T. M., & Boulware, D. R. (2022). The global burden of HIV-associated cryptococcal infection in adults in 2020: A modelling analysis. The Lancet Infectious Diseases, 22(12), 1748-1755. https://doi.org/10.1016/S1473-3099(22)00499-6
Rajasingham, R., Smith, R. M., Park, B. J., Jarvis, J. N., Govender, N. P., Chiller, T. M., Denning, D. W., Loyse, A., & Boulware, D. R. (2017). Global burden of disease of HIV-associated cryptococcal meningitis: An updated analysis. The Lancet Infectious Diseases, 17(8), 873-881. https://doi.org/10.1016/S1473-3099(17)30243-8
Romani, L. (2011). Immunity to fungal infections. Nature Reviews Immunology, 11(4), 275-288. https://doi.org/10.1038/nri2939
Rosen, L. B., Freeman, A. F., Yang, L. M., Jutivorakool, K., Olivier, K. N., Angkasekwinai, N., Suputtamongkol, Y., Bennett, J. E., Pyrgos, V., Williamson, P. R., Ding, L., Holland, S. M., & Browne, S. K. (2013). Anti-GM-CSF autoantibodies in patients with cryptococcal meningitis. Journal of Immunology, 190(8), 3959-3966. https://doi.org/10.4049/jimmunol.1202526
Sabiiti, W., Robertson, E., Beale, M. A., Johnston, S. A., Brouwer, A. E., Loyse, A., Jarvis, J. N., Gilbert, A. S., Fisher, M. C., Harrison, T. S., May, R. C., & Bicanic, T. (2014). Efficient phagocytosis and laccase activity affect the outcome of HIV-associated cryptococcosis. Journal of Clinical Investigation, 124(5), 2000-2008. https://doi.org/10.1172/JCI72950
Saijo, T., Chen, J., Chen, S. C., Rosen, L. B., Yi, J., Sorrell, T. C., Bennett, J. E., Holland, S. M., Browne, S. K., & Kwon-Chung, K. J. (2014). Anti-granulocyte-macrophage colony-stimulating factor autoantibodies are a risk factor for central nervous system infection by Cryptococcus gattii in otherwise immunocompetent patients. mBio, 5(2), e00912-00914. https://doi.org/10.1128/mBio.00912-14
Spadari, C. C., Wirth, F., Lopes, L. B., & Ishida, K. (2020). New Approaches for Cryptococcosis Treatment. Microorganisms, 8(4), 613. https://doi.org/10.3390/microorganisms8040613
Spellberg, B., & Edwards, J. E. Jr. (2001). Type 1/Type 2 immunity in infectious diseases. Clinical Infectious Diseases, 32(1), 76-102. https://doi.org/10.1086/317537
Stenzel, W., Müller, U., Köhler, G., Heppner, F. L., Blessing, M., McKenzie, A. N., Brombacher, F., & Alber, G. (2009). IL-4/IL-13-dependent alternative activation of macrophages but not microglial cells is associated with uncontrolled cerebral cryptococcosis. The American Journal of Pathology, 174(2), 486-496. https://doi.org/10.2353/ajpath.2009.080598
Stone, N. R., Rhodes, J., Fisher, M. C., Mfinanga, S., Kivuyo, S., Rugemalila, J., Segal, E. S., Needleman, L., Molloy, S. F., Kwon-Chung, J., Harrison, T. S., Hope, W., Berman, J., & Bicanic, T. (2019). Dynamic ploidy changes drive fluconazole resistance in human cryptococcal meningitis. Journal of Clinical Investigation, 129(3), 999-1014. https://doi.org/10.1172/JCI124516
Strickland, A. B., Chen, Y., Sun, D., & Shi, M. (2023). Alternatively activated lung alveolar and interstitial macrophages promote fungal growth. Iscience, 26(5), 106717. https://doi.org/10.1016/j.isci.2023.106717
Sun, D., Sun, P., Li, H., Zhang, M., Liu, G., Strickland, A. B., Chen, Y., Fu, Y., Xu, J., Yosri, M., Nan, Y., Zhou, H., Zhang, X., & Shi, M. (2019). Fungal dissemination is limited by liver macrophage filtration of the blood. Nature Communications, 10(1), 4566. https://doi.org/10.1038/s41467-019-12381-5
Torda, A., Kumar, R. K., & Jones, P. D. (2001). The pathology of human and murine pulmonary infection with Cryptococcus neoformans var. gattii. Pathology, 33(4), 475-478. https://doi.org/10.1080/00313020120083197
Underwood, W., & Anthony, R. (2020). AVMA guidelines for the euthanasia of animals: 2020 edition. Retrieved on March, 2013(30), 2020-2021.
Upadhya, R., Lam, W. C., Maybruck, B., Specht, C. A., Levitz, S. M., & Lodge, J. K. (2016). Induction of protective immunity to cryptococcal infection in mice by a heat-killed, Chitosan-deficient strain of Cryptococcus neoformans. mBio, 7(3), e00547-16. https://doi.org/10.1128/mBio.00547-16
van der Weyden, L., Adams, D. J., & Bradley, A. (2002). Tools for targeted manipulation of the mouse genome. Physiological Genomics, 11(3), 133-164. https://doi.org/10.1152/physiolgenomics.00074.2002
Voelz, K., & May, R. C. (2010). Cryptococcal interactions with the host immune system. Eukaryotic Cell, 9(6), 835-846. https://doi.org/10.1128/EC.00039-10
Wager, C. L., & Wormley, F. Jr. (2014). Classical versus alternative macrophage activation: The Ying and the Yang in host defense against pulmonary fungal infections. Mucosal Immunology, 7(5), 1023-1035. https://doi.org/10.1038/mi.2014.65
Wang, P., Cutler, J., King, J., & Palmer, D. (2004). Mutation of the regulator of G protein signaling Crg1 increases virulence in Cryptococcus neoformans. Eukaryotic Cell, 3(4), 1028-1035. https://doi.org/10.1128/EC.3.4.1028-1035.2004
World Health Organization (2022). WHO fungal priority pathogens list to guide research, development and public health action Retrieved from https://www.who.int/publications/i/item/9789240060241
Zhang, Y., Wang, F., Tompkins, K. C., McNamara, A., Jain, A. V., Moore, B. B., Toews, G. B., Huffnagle, G. B., & Olszewski, M. A. (2009). Robust Th1 and Th17 immunity supports pulmonary clearance but cannot prevent systemic dissemination of highly virulent Cryptococcus neoformans H99. The American Journal of Pathology, 175(6), 2489-2500. https://doi.org/10.2353/ajpath.2009.090530
Zhao, Y., Ye, L., Zhao, F., Zhang, L., Lu, Z., Chu, T., Wang, S., Liu, Z., Sun, Y., Chen, M., Liao, G., Ding, C., Xu, Y., Liao, W., & Wang, L. (2023). Cryptococcus neoformans, a global threat to human health. Infectious Diseases of Poverty, 12(1), 20. https://doi.org/10.1186/s40249-023-01073-4