Animal models for the analysis of immune responses to leishmaniasis

Current Protocols in Immunology

Volumn 2015, Issue , 2015, Pages 19.2.1-19.2.24

  Sacks, David L ^a   Melby, Peter C ^b  

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

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Animal models; Leishmaniasis; Liver; Sand fly; Skin; Spleen

Indexed keywords

PEANUT AGGLUTININ;

AMASTIGOTE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CRYOPRESERVATION; DENSITY GRADIENT CENTRIFUGATION; DISEASE MODEL; HAMSTER; HAMSTER MODEL; IMMUNE RESPONSE; INOCULATION; LEISHMANIASIS; MOUSE; MOUSE MODEL; NONHUMAN; PARASITE LOAD; PRIORITY JOURNAL; PROMASTIGOTE; REAL TIME POLYMERASE CHAIN REACTION; SKIN LEISHMANIASIS; THAWING; VISCERAL LEISHMANIASIS; ANIMAL; CLASSIFICATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; ISOLATION AND PURIFICATION; LEISHMANIA; LIFE CYCLE STAGE; PARASITOLOGY; PATHOLOGY; PROCEDURES;

ANIMALS; CRICETINAE; CRYOPRESERVATION; DISEASE MODELS, ANIMAL; LEISHMANIA; LEISHMANIASIS; LEISHMANIASIS, CUTANEOUS; LEISHMANIASIS, VISCERAL; LIFE CYCLE STAGES; MICE; PARASITE LOAD;

EID: 84949217522     PISSN: 19343671     EISSN: 1934368X     Source Type: Journal    
DOI: 10.1002/0471142735.im1902s108     Document Type: Article

References (70)

1. Abbasi, I., Aramin, S., Hailu, A., Shiferaw, W., Kassahun, A., Belay, S., Jaffe, C., and Warburg, A. 2013. Evaluation of PCR procedures for detecting and quantifying Leishmania donovani DNA in large numbers of dried human blood samples from a visceral leishmaniasis focus in Northern Ethiopia. BMC Infect. Dis.13:153-160.
2. Adler, J.H. 1989. The origin of the golden hamster as a laboratory animal. Isr. J. Med. Sci. 25:206-209.
3. Ahmed, S., Colmenares, M., Soong, L., Goldsmith- Pestana, K., Munstermann, L., Molina, R., and McMahon-Pratt, D. 2003. Intradermal infection model for pathogenesis and vaccine studies of murine visceral leishmaniasis. Infect. Immun. 71:401-410.
4. Alexander, J. and Kaye, P.M. 1985. Immunoregulatory pathways in murine leishmaniasis: Different regulatory control during Leishmania mexicana mexicana and Leishmania major infections. Clin. Exp. Immunol. 61:674-682.
5. Anderson, C.F., Mendez, S., and Sacks, D.L. 2005. Nonhealing infection despite Th1 polarization produced by a strain of Leishmania major in C57BL/6 mice. J. Immunol. 174:2934-2941.
6. Aslan, H., Dey, R., Meneses, C., Castrovinci, P., Jeronimo, S.M., Oliva, G., Fischer, L., Duncan, R.C., Nakhasi, H.L., Valenzuela, J.G., and Kamhawi, S. 2013. A new model of progressive visceral leishmaniasis in hamsters by natural transmission via bites of vector sand flies. J. Infect. Dis. 207:1328-1338.
7. Barral, A., Peterson, E., Sacks, D.L., and Neva, F.A. 1983. Late metastatic disease in the mouse. A model for mucocutaneous leishmaniasis. Am. J. Trop. Med. Hyg. 32:277-284.
8. Belkaid, Y., Mendez, S., Lira, R., Kadambi, N., Milon, G., and Sacks, D. 2000. A natural model of Leishmania major infection reveals a prolonged "silent" phase of parasite amplification in the skin before the onset of lesion formation and immunity. J. Immunol. 165:969-977.
9. Blackwell, J.M. 1996. Genetic susceptibility to leishmanial infections: Studies in mice and man. Parasitology 112:S67-S74.
10. Blackwell, J.M., Freeman, J., and Bradley, D. 1980. Influence of H-2 complex on acquired resistance to Leishmania donovani infection in mice. Nature 283:72-74.
11. Bradley, D.J. 1977. Regulation of Leishmania populations within the host. II. Genetic control of acute susceptibility of mice to Leishmania donovani infection. Clin. Exp. Immunol. 30:130-140.
12. Bretscher, P.A., Wei, G., Menon, J.N., and Bielefeldt-Ohmann, H. 1992. Establishment of stable, cell-mediated immunity that makes susceptible mice resistant to Leishmaniamajor. Science 257:539-542.
13. Castilho, T.M., Goldsmith-Pestana, K., Lozano, C., Valderrama, L., Saravia, N.G., and McMahon- Pratt, D. 2010. Murine model of chronic L. (Viannia) panamensis infection: Role of IL-13 in disease. Eur. J. Immunol. 40:2816-2829.
14. Courret, N., Prina, E., Mougneau, E., Saraiva, E.M., Sacks, D.L., Glaichenhaus, N., andAntoine, J.C. 1999. Presentation of the Leishmania antigen LACK by infected macrophages is dependent upon the virulence of the phagocytosed parasites. Eur. J. Immunol. 29:762-773.
15. Donovan, J. and Brown, P. 1998. Anesthesia. Curr. Protoc. Immunol. 27:1.4.1-1.4.5.
16. Donovan, J. and Brown, P. 2006a. Handling and restraint. Curr. Protoc. Immunol. 73:1.3.1-1.3.6.
17. Donovan, J. and Brown, P. 2006b. Parenteral injections. Curr. Protoc. Immunol. 73:1.6.1-1.6.10.
18. Donovan, J. and Brown, P. 2006c. Blood collection. Curr. Protoc. Immunol. 73:1.7.1-1.7.9.
19. Doyle, P.S., Engel, J.C., Pimenta, P.F., da Silva, P.P., and Dwyer, D.M. 1991. Leishmania donovani: Long-term culture of axenic amastigotes at 37 degrees C. Exp. Parasitol. 73:326-334.
20. Eperon, S. and McMahon-Pratt, D. 1989. I. Extracellular cultivation and morphological characterization of amastigote-like forms of Leishmania panamensis and L. braziliensis. J. Protozool. 36:502-510.
21. Giannini, M.S. 1974. Effects of promastigote growth phase, frequency of subculture, and host age on promastigote-initiated infections with Leishmania donovani in the golden hamster. J. Protozool. 21:521-527.
22. Glaser, T.A., Wells, S.J., Spithill, T.W., Pettitt, J.M., Humphris, D.C., and Mukada, A.J. 1990. Leishmania major and Leishmania donovani: A method for rapid purification of amastigotes. Exp. Parasitol. 71:343-345.
23. Gomes, R., Teixeira, C., Teixeira, M.J., Oliveira, F., Menezes, M.J., Silva, C., de Oliveira, C.I., Miranda, J.C., Elnaiem, D.E., Kamhawi, S., Valenzuela, J.G., and Brodskyn, C.I. 2008. Immunity to a salivary protein of a sand fly vector protects against the fatal outcome of visceral leishmaniasis in a hamster model. Proc. Natl. Acad. Sci. U.S.A. 105:7845-7850.
24. Hill, J.O. and Fahety, J.R. 1987. Leishmania spp.: Agar plating as an alternative approach to limiting dilution and impression smears for the enumeration of viable parasites in tissue. Exp. Parasitol. 63:108-111.
25. Hill, J.O., North, R.J., and Collins, F.M. 1983. Advantages of measuring changes in the number of viable parasites in murine models of experimental cutaneous leishmaniasis. Infect. Immun. 39:1087-1094.
26. Hommel, M., Jaffe, C.L., Travi, B., and Milon, G. 1995. Experimental models for leishmaniasis and for testing anti-leishmanial vaccines. Ann. Trop. Med. Parasitol. 89:55-73.
27. Howard, J.G., Hale, C., and Chan-Liew, W.L. 1980. Immunological regulation of experimental cutaneous leishmaniasis. I. Immunological aspects of susceptibility to Leishmania tropica (major) in mice. Parasite Immunol. 2:303-314.
28. Jara, M., Adaui, V., Valencia, B.M., Martinez, D., Alba, M., Castrillon, C., Cruz, M., Cruz, I., Van der Auwera, G., Llanos-Cuentas, A., Dujardin, J.C., and Arevalo, J. 2013. Real-time PCR assay for detection and quantification of Leishmania (Viannia) organisms in skin and mucosal lesions: exploratory study of parasite load and clinical parameters. J. Clin. Microbiol. 51:1826-1833.
29. Jones, K.H. and Senft, J.A. 1985. An improved method to determine cell viability by simultaneous staining with fluorescein diacetatepropidium iodide. J. Histochem. Cytochem. 33:77-79.
30. Joshi, P.B., Sacks, D.L., Modi, G., and McMaster, W.R. 1998. Targeted gene deletion of Leishmania major genes encoding developmental stagespecific leishmanolysin (GP63). Mol. Microbiol. 27:519-530.
31. Kellina, O.I. 1965. A comparative study of the virulence of L. tropica major strains. Med. Parazitol. Parazit. Bolezni. 34:309-316.
32. Kruisbeek, A.M. 2000. Isolation of mouse mononuclear cells. Curr. Protoc. Immunol. 39:3.1.1-3.1.5.
33. Lira, R., Mendez, S., Carrera, L., Jaffe, C., Neva, F., and Sacks, D. 1998. Leishmania tropica: The identification and purification of metacyclic promastigotes and use in establishing mouse and hamster models of cutaneous and visceral disease. Exp. Parasitol. 89:331-342.
34. Lira, R., Doherty, M., Modi, G., and Sacks, D. 2000. Evolution of lesion formation, parasitic load, immune response, and reservoir potential in C57BL/6 mice following high- and low-dose challenge with Leishmania major. Infect. Immun. 68:5176-5182.
35. Mahoney, A.B., Sacks, D.L., Saraiva, E., Modi, G., and Turco, S.J. 1999. Intra-species and stagespecific polymorphisms in lipophosphoglycan structure control Leishmania donovani-sand fly interactions. Biochemistry 38:9813-9823.
36. McConville, M., Turco, S., Ferguson, M., and Sacks, D. 1992. Developmental modification of lipophosphoglycan: During the differentiation of Leishmania major promastigotes to an infectious stage. EMBO J. 11:3593-3600.
37. McConville, M.J., Schnur, L.F., Jaffe, C., and Schneider, P. 1995. Structure of Leishmania lipophosphoglycan Inter- and intra-specific polymorphism in Old World species. Biochem. J. 310:807-818.
38. Melby, P.C., Tryon, V.V., Chandrasekar, B., and Freeman, G.L. 1998a. Cloning of Syrian hamster (Mesocricetus auratus) cytokine cDNAs and analysis of cytokine mRNA expression in experimental visceral leishmaniasis. Infect. Immun. 66:2135-2142.
39. Melby, P.C., Yang, Y.-Z., Cheng, J., and Zhao, W. 1998b. Regional differences in the cellular immune response to experimental cutaneous or visceral infection with Leishmania donovani. Infect. Immun. 66:18-27.
40. Mitchell, G.F., Handman, E., and Spithill, T.W. 1984. Vaccination against cutaneous leishmaniasis in mice using nonpathogenic cloned promastigotes of Leishmaniamajor and importance of route of injection. Aust. J. Exp. Biol. Med. Sci. 62:145-153.
41. Nabors, G.S. and Farell, J.P. 1994. Site-specific immunity to Leishmania major in SWR mice: The site of infection influences susceptibility and the expression of the antileishmanial immune response. Infect. Immun. 62:3655-3662.
42. Nicolas, L., Prina, E., Lang, T., and Milon, G. 2002. Real-time PCR for detection and quantitation of leishmania in mouse tissues. J. Clin Microbiol. 40:1666-1669.
43. Pan, A. 1984. Leishmania mexicana: Serial cultivation of intracellular stages in a cell-free medium. Exp. Parasitol. 58:72-80.
44. Pearson, R.D., Cox, G., Evans, T., Smith, D.L., Weidel, D., and Castracane, J. 1990. Wasting and macrophage production of tumor necrosis factor/cachectin and interleukin 1 in experimental visceral leishmaniasis. Am. J. Trop. Med. Hyg. 43:640-649.
45. Perez, H., Labrador, F., and Torealba, J.W. 1979. Variations in the response of five strains of mice to Leishmania mexicana. Int. J. Parasitol. 9:27-32.
46. Pinto-da-Silva, L.H., Camurate, M., Costa, K.A., Oliveira, S.M., da Cunha-e-Silva, N.L., and Saraiva, E.M. 2002. Leishmania (Viannia) braziliensis metacyclic promastigotes purified using Bauhinia purpurea lectin are complement resistant and highly infective for macrophages in vitro and hamsters in vivo. Int. J. Parasitol. 32:1371-1377.
47. Preston, P.M. and Dumonde, D.C. 1976. Experimental cutaneous leishmaniasis. V. Protective immunity in subclinical and self-healing infections in the mouse. Clin. Exp. Immunol. 23:126-138.
48. Prina, E., Roux, E., Mattei, D., and Milon, G. 2007. Leishmania DNA is rapidly degraded following parasite death: An analysis by microscopy and real-time PCR. Microbes Infect. 9:1307-1315.
49. Rey, J.A., Travi, B., Valencia, A.Z., and Saravia, N.G. 1990. Infectivity of the subspecies of the Leishmania braziliensis complex in vivo and in vitro. Am. J. Trop. Med. Hyg. 43:89-193.
50. Ribeiro-Gomes, F.L., Roma, E.H., Carneiro, M.B.H., Sacks, D.L., and Peters, N.C. 2014. Site dependent recruitment of inflammatory cells determines the effective dose of Leishmaniamajor. Infect. Immun. In press.
51. Romero, I., Tellez, J., Suarez, Y., Cardona, M., Figueroa, R., Zelazny, A., and Saravia, N. 2010. Viability and burden of Leishmania in extralesional sites during human dermal leishmaniasis. PLoS Negl. Trop. Dis. 4-12.
52. Sacks, D.L. 1989. Metacyclogenesis in Leishmania promastigotes. Exp. Parasitol. 69:100-103.
53. Sacks, D. and Kamhawi, S. 2001. Molecular aspects of parasite-vector and vector-host interactions in leishmaniasis. Annu. Rev. Microbiol. 55:453-483.
54. Sacks, D.L. and Perkins, P.V. 1984. Identification of an infective stage of Leishmania promastigotes. Science 223:1417-1419.
55. Sacks, D.L., Hieny, S., and Sher, A. 1985. Identification of cell surface carbohydrate and antigenic changes between noninfective and infective developmental stages of Leishmania major promastigotes. J. Immunol. 135:564-569.
56. Sacks, D.L., Pimenta, P.F., McConville, M.J., Schneider, P., and Turco, S.J. 1995. Stagespecific adhesion of Leishmania donovani to the sand fly vector midgut is regulated by conformational changes in the abundant surface lipophosphoglycan. J. Exp. Med. 181:685-697.
57. Saraiva, E.M.B., Pimenta, P., Pereira, M., and DeSouza, W. 1983. Isolation and purification of amastigotes of Leishmania mexicana amazonensis by a gradient of metrizamide. J. Parasitol. 69:627-629.
58. Scott, P.A. and Farrell, J.P. 1982. Experimental cutaneous leishmaniasis: Disseminated leishmaniasis in genetically susceptible and resistant mice. Am. J. Trop. Med. Hyg. 31:230-238.
59. Serafim, T.D., Figueiredo, A.B., Costa, P.A., Marques-da-Silva, E.A., Goncalves, R., de Moura, S.A., Gontijo, N.F., da Silva, S.M., Michalick, M.S., Meyer-Fernandes, J.R., de Carvalho, R.P., Uliana, S.R., Fietto, J.L., and Afonso, L.C. 2012. Leishmania metacyclogenesis is promoted in the absence of purines. PLoS Negl. Trop. Dis. 6:e1833.
60. Soares, R.P., Macedo, M.E., Ropert, C., Gontijo, N.F., Almeida, I.C., Gazzinelli, R.T., Pimenta, P.F., and Turco, S.J. 2002. Leishmania chagasi: Lipophosphoglycan characterization and binding to the midgut of the sand fly vector Lutzomyia longipalpis. Mol. Biochem. Parasitol. 121:213-224.
61. Spath, G.F. and Beverley, S.M. 2001. A lipophosphoglycan-independent method for isolation of infective Leishmania metacyclic promastigotes by density gradient centrifugation. Exp. Parasitol. 99:97-103.
62. Stauber, L.A. 1966. The origin and significance of the distribution of parasites in visceral leishmaniasis. Trans. N.Y. Acad. Sci. 28:635-643.
63. Strober, W. 1997. Monitoring cell growth. Curr. Protoc. Immunol. 21:3A.1-A.3A.2.
64. Taswell, C. 1981. Limiting dilution assays for the determination of immunocompetent cell frequencies. I. Data analysis. J. Immunol. 126:1614-1619.
65. Titus, R.G., Marchand, M., Boon, T., and Louis, J.A. 1985. A limiting dilution assay for quantifying Leishmania major in tissues of infected mice. Parasite Immunol. 7:545-555.
66. van den Bogaart, E., Schoone, G.J., Adams, E.R., and Schallig, H.D. 2014. Duplex quantitative Reverse-Transcriptase PCR for simultaneous assessment of drug activity against Leishmania intracellular amastigotes and their host cells. Int. J. Parasitol. Drugs Drug Resist. 4:14-9.
67. van der Meide, W., Guerra, J., Schoone, G., Farenhorst, M., Coelho, L., Faber, W., Peekel, I., and Schallig, H. 2008. Comparison between quantitative nucleic acid sequence-based amplification, real-time reverse transcriptase PCR, and real-time PCR for quantification of Leishmania parasites. J. Clin. Microbiol. 46:73-8.
68. Vidal, S.M., Malo, D., Vogan, K., Skamene, E., and Gros, P. 1993. Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg. Cell 73:469-485.
69. Yokoyama, W.M., Thompson, M.L. and Ehrhardt, R.O. 2012. Cryopreservation and thawing of cells. Curr. Protoc. Immunol. 99:A.3G.1-A.3G.5.
70. Zakai, H.A., Chance, M.L., and Bates, P.A. 1998. In vitro stimulation of metacyclogenesis in Leishmania braziliensis, L. donovani, L. major, and L. mexicana. Parasitology 116:305-309.