The utility of rhesus monkey (Macaca mulatta) and other non-human primate models for preclinical testing of Leishmania candidate vaccines - A Review

Memorias do Instituto Oswaldo Cruz

Volumn 103, Issue 7, 2008, Pages 629-644

  Grimaldi Jr , Gabriel ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Experimental leishmaniasis; Leishmania vaccine development; Non human primates

Indexed keywords

ANIMALIA; CERCOPITHECIDAE; MACACA; MACACA MULATTA; PAPIO; PRIMATES;

DNA VACCINE; LEISHMANIA VACCINE;

ANIMAL; ANIMAL MODEL; DRUG SCREENING; HAPLORHINI; IMMUNOLOGY; LEISHMANIA; LEISHMANIASIS; MACACA MULATTA; REVIEW;

ANIMALS; DRUG EVALUATION, PRECLINICAL; HAPLORHINI; LEISHMANIA; LEISHMANIASIS; LEISHMANIASIS VACCINES; MACACA MULATTA; MODELS, ANIMAL; VACCINES, DNA;

EID: 56749091574     PISSN: 00740276     EISSN: 16788060     Source Type: Journal    
DOI: 10.1590/s0074-02762008000700002     Document Type: Review

References (142)

1. Amaral VF, Pirmez C, Ferreira AJS, Ferreira V, Grimaldi Jr G 2000. Cell populations in lesions of cutaneous leishmaniasis of Leishmania (L.) amazonensis-infected rhesus macaques, Macaca mulatta. Mem Inst Oswaldo Cruz 95: 209-216.
2. Amaral VF, Ransatto VAO, Conceição-Silva F, Molinaro E, Ferreira V, Coutinho SG, McMahon-Pratt D, Grimaldi G Jr 1996. Leishmania amazonensis: the Asian rhesus macaques (Macaca mulatta) as an experimental model for study of cutaneous leishmaniasis. Exp Parasitol 82: 34-44.
3. Amaral VF, Teva A, Oliveira-Neto MP, Silva AJ, Pereira MS, Cupolillo E, Porrozzi R, Coutinho SG, Pirmez C, Beverley SM, Grimaldi G Jr 2002. Study of the safety, immunogenicity and efficacy of attenuated and killed Leishmania (Leishmania) major vaccines in a rhesus monkey (Macaca mulatta) model of the human disease. Mem Inst Oswaldo Cruz 97: 1041-1048.
4. Amaral VF, Teva A, Porrozzi R, Silva AJ, Pereira MS, Grimaldi G Jr 2001. Leishmania (Leishmania) major-infected rhesus macaques (Macaca mulatta) develop varying levels of resistance against homologous reinfections. Mem Inst Oswaldo Cruz 96: 795-804.
5. Anuradha R, Pal R, Zehra K, Katiyar JC, Sethi N, Bhatia G, Singh RK 1992. The Indian langur: preliminary report of a new non-human primate host for visceral leishmaniasis. WHO Bulletin 70: 63-72.
6. Anuradha D, Sharma P, Skrivastava JK, Misra A, Naik S 1998. Vaccination of langur monkey (Presbytis entellus) against Leishmania donovani with autoclaved L. major plus BCG. Parasitology 116: 219-221.
7. + T cell efficacy in vaccination and disease. Nature Med 14: 623-628.
8. Badaró R, Lobo I, Munos A, Netto EM, Modabber F, Campos-Neto A, Coler RN, Reed SG 2006. Immunotherapy for drug-refractory mucosal leishmaniasis. J Infect Dis 194: 1151-1159.
9. Barouch DH, Letvin NL 2000. DNA Vaccination for HIV-1 and SIV. Intervirology 43: 282-287.
10. + regulatory T cells control Leishmania major persistence and immunity. Nature 420: 502-507.
11. Berman JD, Hanson WL, Chapman WL, Alving CR, Lopez-Berestein G 1986. Antileishmanial activity of liposome-encapsulated Amphotericin B in hamsters and monkeys. Antimicrob Agents Chemother 30: 847-851.
12. Bhowmick S, Ravindran R, Ali N 2007. Leishmanial antigens in liposomes promote protective immunity and provide immunotherapy against visceral leishmaniasis via polarized Th1 response. Vaccine 25: 6544-6556.
13. Binhazim AA, Githure JI, Muchemi GK, Reid GD 1987. Isolation of Leishmania major from a naturally infected vervet monkey (Cercopithecus aethiops) caught in Kiambu District, Kenya. Parasitology 73: 1278-1279.
14. Binhazim AA, Shin SS, Chapman WL Jr, Olobo J 1993. Comparative susceptibility of African green monkeys (Cercopithecus aethiops) to experimental infection with Leishmania leishmania donovani and Leishmania leishmania infantum. Lab Anim Sci 43: 37-47.
15. Broderson JR, Chapman WL Jr, Hanson WL 1986. Experimental visceral leishmaniasis in the owl monkey. Vet Pathol 23: 293-302.
16. Brodie TM, Smith MC, Morris RV, Titus RG 2007. Immunomodulatory effects of the Lutzomyia longipalpis salivary gland protein Maxadilan on mouse macrophages. Infect Immun 75: 2359-2365.
17. Campos-Neto A, Porrozzi R, Greeson K, Coler RN, Webb JR, Seiky YA, Reed SG, Grimaldi G Jr 2001. Protection against cutaneous leishmaniasis induced by recombinant antigens in murine and non-human primate models of the human disease. Infect Immun 69: 4103-4108.
18. Campos-Neto A, Webb JR, Greeson K, Coler RN, Skeiky YA, Reed SG 2002. Vaccination with plasmid DNA encoding TSA/LmSTI1 leishmanial fusion proteins confers protection against Leishmania major infection in susceptible BALB/c mice. Infect Immun 70: 2828-2836.
19. Chapman WL Jr, Hanson WL 1981. Visceral leishmaniasis in the squirrel monkey (Saimiri sciurea). J Parasitol 67: 740-741.
20. Chapman WL Jr, Hanson WL, Hendricks LD 1981. Leishmania donovani in the owl monkey (Aotus trivirgatus). Trans R Soc Trop Med Hyg 75: 124-125.
21. Christensen HA, de Vasquez AM 1981. Susceptibility of Aotus trivirgatus to Leishmania braziliensis and L. mexicana. Am J Trop Med Hyg 30: 54-56.
22. + T cells. Infect Immun 75: 4648-4654.
23. Coler RN, Reed SG 2005. Second-generation vaccines against leishmaniasis. Trends Parasitol 21: 244-248.
24. Cuba-Cuba CA, Ferreira V, Bampi M, Magalhães A, Marsden P, Vexenat A, Mello MT 1990. Experimental infection with Leishmania (Viannia) braziliensis and Leishmania (Leishmania) amazonensis in marmoset (Callithrix penicillata) (Primates, Callithricidae). Mem Inst Oswaldo Cruz 85: 459-467.
25. Cuba-Cuba CA, Marsden PD 1992. Failure to develop homologous immunity to a second challenge with Leishmania (Viannia) braziliensis in the black-plumed marmoset (Callithrix penicillata). Trans R Soc Trop Med Hyg 86: 37-45.
26. H1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nature Med 13: 843-850.
27. Davies CR, Kaye P, Croft SL, Sundar S 2003. Leishmaniasis: new approaches to disease control. BMJ 326: 377-382.
28. Delgado G, Parra-López C, Spinel C, Patarroyo ME 2005. Phenotypical and functional characterization of non-human primate Aotus spp. dendritic cells and their use as a tool for characterizing immune response to protein antigens. Vaccine 23: 3386-3395.
29. Dennis VA, Chapman WL Jr, Hanson WL, Lujan R 1985. Leishmania donovani: clinical, haematological and hepatic changes in squirrel monkeys (Saimiri sciureus). J Parasitol 71: 576-582.
30. Dennis VA, Lujan R, Chapman WL Jr, Hanson WL 1986. Leishmania donovani: Cellular and humoral immune responses after primary and challenge infections in squirrel monkeys, Saimiri sciureus. Exp Parasitol 61: 319-334.
31. Dietze R, Araújo RC, Lima MLR, Vexenat JA, Marsden PD, Barreto AC 1985. Ensaio terapêutico com glucantime em sagüis (Callithrix jacchus) infectados com uma cepa de Leishmania donovani aparentemente resistente ao tratamento. Rev Soc Bras Med Trop 18: 39-42.
32. Dondji B, Deak E, Goldsmith-Pestana K, Perez-Jimenez E, Esteban M, Miyake S, Yamamura T, McMahon-Pratt D 2008. Intradermal NKT cell activation during DNA priming in heterologous prime-boost vaccination enhances T cell responses and protection against Leishmania. Eur J Immunol 38: 706-719.
33. Dondji B, Pérez-Jimenez E, Goldsmith-Pestana K, Esteban M, McMahon-Pratt D 2005. Heterologous prime-boost vaccination with the LACK antigen protects against murine visceral leishmaniasis. Infect Immun 73: 5286-5289.
34. Doxiadis GGM, Otting NG, Natasja G, Bontrop RE 2001. Differential evolutionary MHC class II strategies in humans and rhesus macaques: relevance for biomedical studies. Non-human primate models for human disease and immunobiology. Immunol Rev 183: 76-85.
35. Dube A, Sharma P, Srivastava JK, Misra A, Naik S, Katiyar JC 1998. Vaccination of langur monkeys (Presbytis entellus) against Leishmania donovani with autoclaved L. major plus BCG. Parasitology 116: 219-221.
36. Dube A, Srivastava JK, Sharma P, Chaturvedi A, Katiyar JC, Naik S 1999. Leishmania donovani: cellular and humoral immune responses in Indian langur monkeys, Presbytis entellus. Acta Trop 73: 37-48.
37. Elias D, Akuffo H, Britton S 2005. PPD induced in vitro interferon gamma production is not a reliable correlate of protection against Mycobacterium tuberculosis. Trans R Soc Trop Med Hyg 99: 363-368.
38. Freidag BL, Mendez S, Cheever AW, Kenney RT, Flynn B, Sacks DL, Seder RA 2003. Immunological and pathological evaluation of rhesus macaques infected with Leishmania major. Exp Parasitol 103: 160-168.
39. Garcez LM, Silveira FT, El Harith A, Lainson R, Shaw JJ 2002. Experimental cutaneous leishmaniasis IV. The humoral response of Cebus apella (Primates: Cebidae) to infections of Leishmania (Leishmania) amazonensis, L. (Viannia) lainsoni and L. (V.) braziliensis using the direct agglutination test. Acta Trop 68: 65-76.
40. Giavedoni LD 2005. Simultaneous detection of multiple cytokines and chemokines from nonhuman primates using luminex technology. J Immunol Methods 301: 89-101.
41. Gibbs RA, Rogers J, Katze MG, Bumgarner R, Weinstock GM, Mardis ER, Remington KA, Strausberg RL, Venter JC, Wilson RK, Batzer MA, Bustamante CD, Eichler EE, Hahn MW, Hardison RC, Makova KD, Miller W, Milosavljevic A, Palermo RE, Siepel A, Sikela JM, Attaway T, Bell S, Bernard KE, Buhay CJ, Chandrabose MN, Clay Davis DM, Delehaunty KD, Ding Y, Dinh HH, Dugan-Rocha S, Fulton LA, Gabisi RA, Garner TT, Godfrey J, Hawes AC, Hernandez J, Hines S, Holder M, Hume J, Jhangiani SN, Joshi V, Khan ZM, Kirkness EF, Cree A, Fowler RG, Lee S, Lewis LR, Li Z, Liu Y, Moore SM, Muzny D, Nazareth LV, Ngo DN, Okwuonu GO, Pai G, Parker D, Paul HA, Pfannkoch C, Pohl CS, Rogers Y-H, Ruiz SJ, Sabo A, Santibanez J, Schneider BW, Smith SM, Sodergren E, Svatek AF, Utterback TR, Vattathil S, Warren W, White CS, Chinwalla AT, Feng Y, Halpern AL, Hillier LW, Huang X, Minx P, Nelson JO, Pepin KH, Qin X, Sutton GG, Venter E, Walenz BP, Wallis JW, Worley KC, Yang S-P, Jones SM, Marra MA, Rocchi M, Schein JE, Baertsch R, Clarke L, Csürös M, Glasscock J, Harris RA, Havlak P, Jackson AR, Jiang H, Liu Y, Messina DN, Shen Y, Xing-Zhi Song H, Wylie T, Zhang L, Birney E, Han K, Konkel MK, Lee J, Smit AFA, Ullmer B, Wang H, Xing J, Burhans R, Cheng Z, Karro JE, Ma J, Raney B, She X, Cox MJ, Demuth JP, Dumas LJ, Han S-G, Hopkins J, Karimpour-Fard A, Kim YH, Pollack JR, Vinar T, Addo-Quaye C, Degenhardt J, Denby A, Hubisz MJ, Indap A, Kosiol C, Lahn BT, Lawson HA, Marklein A, Nielsen R, Vallender EJ, Clark AG, Ferguson B, Hernandez RD, Hirani K, Kehrer-Sawatzki H, Kolb J, Patil S, Pu L-L, Ren Y, Smith DG, Wheeler DA, Schenck I, Ball EV, Chen R, Cooper DN, Giardine B, Hsu F, Kent FW, Lesk A, Nelson DL, O'Brien WE, Prüfer K, Stenson PD, Wallace JC, Ke H, Liu X-M, Wang P, Xiang AP, Yang F, Barber GP, Haussler D, Karolchik D, Kern AD, Kuhn RM, Smith KE, Zwieg AS 2007. Rhesus macaque genome sequencing and analysis consortium. Evolutionary and biomedical insights from the rhesus macaque genome. Science 316: 222-234.
42. Gicheru MM, Olobo JO, Anjili CO 1997. Heterologous protection by Leishmania donovani for Leishmania major infections in the vervet monkey model of the disease. Exp Parasitol 85: 109-116.
43. Gicheru MM, Olobo JO, Anjili CO, Orago AS, Modabber F, Scott P 2001. Vervet monkeys vaccinated with killed Leishmania major parasites and interleukin-12 develop a type 1 immune response but are not protected against challenge infection. Infect Immun 69: 245-251.
44. Gicheru MM, Olobo JO, Kariuki TM, Adhiambo C 1995. Visceral leishmaniasis in vervet monkeys: immunological responses during asymptomatic infections. Scand J Immunol 41: 202-208.
45. Githure JI, Reid GD, Binhazim AA, Anjili CO, Shatry AM, Hendricks LD 1987. Leishmania major: the suitability of East African non-human primates as animal models for cutaneous leishmaniasis. Exp Parasitol 64: 438-447.
46. Githure JI, Shatry AM, Tarara R, Chulay JD, Suleman MA, Chunge CN, Else JG 1986. The suitability of East African primates as animal models of visceral leishmaniasis. Trans R Soc Trop Med Hyg 80: 575-576.
47. Gonzalo RM, del Real G, Rodriguez JR, Rodriguez D, Heljasvaara R, Lucas P, Larraga V, Esteban M 2002. A heterologous prime-boost regime using DNA and recombinant vaccinia virus expressing the Leishmania infantum P36/LACK antigen protects BALB/c mice from cutaneous leishmaniasis. Vaccine 20: 1226-1231.
48. Grimaldi G Jr 1995. Meeting on vaccine studies towards the control of leishmaniasis. Mem Inst Oswaldo Cruz 90: 553-556.
49. Grimaldi G Jr, Tesh RB 1993. Leishmaniasis of the New World: Current concepts and implications for future research. Clin Microbiol Rev 6: 230-250.
50. Gunders AE 1987. Vaccination: past and future role in control. In W Peters, R Killick-Kendrick (eds.), The leishmaniasis in Biology and Medicine, Vol. 2, Academic Press, London, p. 928-941.
51. + T cells. J Immunol 165: 915-924.
52. Hanke T, Blanchard TJ, Schneider J, Hannan CM, Becker M, Gilbert SC, Hill AVS, Smith GL, McMichael A 1998. Enhancement of MHC class I-restricted peptide-specific T cell induction by a DNA prime/MVA boost vaccination regime. Vaccine 16: 439-445.
53. Hein WR, Griebel PJ 2003. A road less traveled: large animal models in immunological research. Nat Rev Immunol 3: 79-84.
54. Herrer A, Christensen HA, Beumer RJ 1973. Reservoir hosts of cutaneous leishmaniasis among Panamanian forest mammals. Am J Trop Med Hyg 22: 585-591.
55. Hu S-L 2005. Non-human primate models for AIDS vaccine research. Curr Drug Targets Infect Disord 5: 193-201.
56. Hu S-L, Klaniecki J, Dykers T, Sridhar P, Travis BM 1991. Neutralizing antibodies against HIV-1 BRU and SF2 isolates generated in mice immunized with recombinant vaccinia virus expressing HIV-1 (BRU) envelope glycoproteins and boosted with homologous gp160. AIDS Res Hum Retroviruses 7: 615-620.
57. Iborra S, Carrión J, Anderson C, Alonso C, Sacks D, Soto M 2005. Vaccination with the Leishmania infantum acidic ribosomal P0 protein plus CpG oligodeoxynucleotides induces protection against cutaneous leishmaniasis in C57BL/6 mice but does not prevent progressive disease in BALB/c mice. Infect Immun 73: 5842-5852.
58. Iborra S, Soto M, Carrión J, Alonso C, Requena JM 2004. Vaccination with a plasmid DNA cocktail encoding the nucleosomal histones of Leishmania confers protection against murine cutaneous leishmaniosis. Vaccine 22: 3865-3876.
59. Johnston MI 2000. The role of non-human primate models in AIDS vaccine development. Mol Med Today 6: 267-270.
60. Kedzierski L, Zhu Y, Handman E 2006. Leishmania vaccines: progress and problems. Parasitology 133 (Suppl.): 87-112.
61. Keeney TS, Nomura LE, Maecker HT, Sastry KJ 2003. Flow cytometric analysis of macaque whole blood for antigen-specific intracellular cytokine production by T lymphocytes. J Med Primatol 32: 23-30.
62. Kennedy RC, Shearer MH, Hildebrand WH 1997a. Nonhuman primate models to evaluate vaccine safety and immunogenicity. Vaccine 15: 903-908.
63. Kennedy RC, Shearer MH, Hildebrand WH, Simmonds RS 1997b. Non-human primates and their use in immunologically based investigations. The Immunologist 5/5: 150-156.
64. Kenney RT, Sacks DL, Sypek JP, Vilela L, Gam AA, Evans-Davis K 1999. Protective immunity using recombinant human IL-12 and alum as adjuvants in a primate model of cutaneous leishmaniasis. J Immunol 163: 4481-4488.
65. Killick-Kendrick R, Bryceson ADM, Peter W, Evans DA, Leaney AJ, Rioux JA 1985. Zoonotic cutaneous leishmaniasis in Saudi Arabia: Lesions healing naturally in man followed by a second infection with the same zymodeme of Leishmania major. Trans R Soc Trop Med Hyg 79: 363-365.
66. Klein J, Satta Y, O'Huigin C, Takahata N 1993. The molecular descent of the major histocompatibility complex. Immunol Reviews 11: 213-244.
67. + HIV-specific T cells during progression to AIDS. Blood 99: 2505-2511.
68. Lainson R, Braga RR, de Souza AAA, Povoa MM, Ishikawa EAY, Silveira FT 1989. Leishmania (Viannia) shawi sp. n., a parasite of monkeys, sloths and procyo nids in Amazonian Brazil. Ann Parasitol Hum Comp 64: 200-207.
69. Lainson R, Bray RS 1966. Studies on the immunology and serology of leishmaniasis. II. Cross-immunity experiments among different forms of American cutaneous leishmaniasis in monkeys. Trans R Soc Trop Med Hyg 60: 526-532.
70. Lainson R, Shaw JJ 1966. Studies on the immunology and serology of leishmaniasis. III. Cross-immunity between Panamenian cutaneous leishmaniasis and Leishmania mexicana infection in man. Trans R Soc Trop Med Hyg 60: 533-535.
71. Lainson R, Shaw JJ 1977. Leishmaniasis in Brazil: XII. Observations on cross-immunity in monkeys and man infected with Leishmania mexicana mexicana, L. m. amazonensis, L. braziliensis braziliensis, L. b. guyanensis and L. b. panamensis. J Trop Med 80: 29-35.
72. Lainson R, Shaw JJ, Braga RR, Sacawa EAY, Souza AA, Silveira FT 1988. Isolation of Leishmania from monkeys in the Amazon region of Brazil. Trans R Soc Trop Med Hyg 82: 132.
73. Lambert P-H, Liu M, Siegrist C-A 2005. Can successful vaccines teach us how to induce efficient protective immune responses? Nature Med 11 (Suppl.): 54-62.
74. Lawyer PG, Ghiture JI, Anjili CO, Olobo JO, Koech DK, Reid GDF 1990. Experimental transmission of Leishmania major to vervet monkeys (Cercopithecus aethiops) by bites of Phlebotomus duboscqi (Diptera: Psychodidae). Trans R Soc Trop Med Hyg 84: 229-232.
75. Levinson G, Hughes AL, Letvin NL 1992. Sequence and diversity of rhesus monkey T-cell receptor beta chain genes. Immunogenetics 35: 75-88.
76. Lima HC, Titus RG 1996. Effects of sand fly vector saliva on development of cutaneous lesions and the immune response to Leishmania braziliensis in BALB/c mice. Infect Immun 64: 5442-5445.
77. Lujan R, Chapman WL Jr, Hanson WL, Dennis VA 1986a. Leishmania braziliensis: development of primary and satellite lesions in the experimentally infected owl monkey, Aotus trivirgatus. Exp Parasitol 61: 348-358.
78. Lujan R, Chapman WL Jr, Hanson WL, Dennis VA 1990. Leishmania braziliensis in the squirrel monkeys: development of primary and satellite lesions and lack of cross-immunity with Leishmania donovani. J Parasitol 76: 594-597.
79. Lujan R, Dennis VA, Chapman WL Jr, Hanson WL 1986b. Blastogenic responses of peripheral blood leukocytes from owl monkeys experimentally infected with Leishmania braziliensis panamensis. Am J Trop Med Hyg 35: 1103-1109.
80. Lujan R, Hanson WL, Chapman WL Jr, Dennis VA 1987. Antibody responses, as measured by the enzyme-linked immunosorbent assay (ELISA), in owl monkeys experimentally infected with Leishmania braziliensis panamensis. J Parasitol 73: 430-432.
81. MacGregor RR, Boyer JD, Ugen KE, Lacy KE, Gluckman SJ, Bagarazzi ML, Chattergoon MA, Baine Y, Higgins TJ, Ciccarelli RB, Coney LR, Ginsberg RS, Weiner DB 1998. First human trial of a DNA-based vaccine for treatment of human immunodeficiency virus type 1 infection: safety and host response. J Infect Dis 178: 92-100.
82. Madindou TJ, Hanson WL, Chapman WL Jr 1985. Chemotherapy of visceral leishmaniasis (Leishmania donovani) in the squirrel monkey (Saimiri sciureus). Ann Trop Med Parasitol 79: 13-19.
83. Mäkitalo B, Andersson M, Areström I, Karlén K, Villinger F, Ansari A, Paulie S, Throstensson R, Ahlborg N 2002. ELISpot and ELISA analysis of spontaneous, mitogen-induced and antigen-specific cytokine production in cynomolgus and rhesus macaques. J Immunol Methods 270: 85-97.
84. Marques da Cunha A 1938. Infecções experimentais na leishmaniose visceral americana. Mem Inst Oswaldo Cruz 33: 581-598.
85. Marques da Cunha A 1944. Infecções experimentais na leishmaniose tegumentar americana. Mem Inst Oswaldo Cruz 41: 263-282.
86. Marsden PD, Cuba CC, Vexenat A, Costa e Silva M, Costa e Silva A, Barreto AC 1981. Experimental Leishmania chagasi infections in the marmoset Callithrix jacchus jacchus. Trans R Soc Trop Med Hyg 75: 314-315.
87. Massina S, Gicheru MM, Dempts SO, Fasel NJ 2003. Protection against cutaneous leishmaniasis in outbred vervet monkeys, using a recombinant histone H1 antigen. J Infect Dis 188: 1250-1257.
88. + cell depletion in Macaca nemestrina. J Med Primatol 29: 114-126.
89. Méndez S, Gurunathan S, Kamhawi S, Belkaid Y, Moga MA, Skeiky YA, Campos-Neto A, Reed S, Seder RA, Sacks D 2001. The potency and durability of DNA- and protein-based vaccines against Leishmania major evaluated using low-dose, intradermal challenge. J Immunol 166: 5122-5128.
90. Misra A, Dube A, Srivastava B, Sharma P, Srivastava JK, Katiyar JC, Naik S 2001. Successful vaccination against Leishmania donovani infection in Indian langur using alum-precipitated autoclaved Leishmania major with BCG. Vaccine 19: 3485-3492.
91. Moreno J, Nieto J, Masina S, Cañavate C, Cruz I, Chicharro C, Carrillo E, Napp S, Reymond C, Kaye PM, Smith DF, Fasel N, Alvar J 2007. Immunization with H1, HASPB1 and MML Leishmania proteins in a vaccine trial against experimental canine leishmaniasis. Vaccine 25: 5290-5300.
92. Nathansson N, Hirsch VM, Mathieson BJ 1999. The role of non-human primates in thedevelopment of an AIDS vaccine. AIDS 13 (Suppl. A): 113-120.
93. Nikolich-Žugich J 2007. Non-human primates models of T-cell reconstitution. Semin Immunol 19: 310-317.
94. Oliveira MR, Tafuri WL, Afonso LCC, Oliveira MAP, Nicoli JR, Vieira EC, Scott P, Melo MN, Vieira LQ 2005. Germ-free mice produce high levels of interferon-gamma in response to infection with Leishmania major but fail to heal lesions. Parasitology 131: 477-488.
95. Olobo JO, Anjili CO, Gicheru MM, Mbati PA, Kariuki TM, Githure JI, Koech DK, McMaster 1995. Vaccination of vervet monkeys against cutaneous leishmaniasis using recombinant Leishmania "major surface glycoporotein" (gp63). Vet Parasitol 60: 199-212.
96. Olobo JO, Reid GDF 1993. Delayed-type hypersensitivity responses in vervet monkeys self-cured from experimental cutaneous leishmaniasis. Acta Trop 52: 309-311.
97. Olobo JO, Reid GDF, Githure JI, Anjili CO 1992. IFN-gamma and delayed-type hypersensitivity are associated with cutaneous leishmaniasis in vervet monkeys following secondary rechallenge with Leishmania major. Scand J Immunol (Suppl.) 11: 48-52.
98. Pahar B, Li J, Rourke T, Miller CJ, McChesney MB 2003. Detection of antigen-specific T cell interferon-? expression by ELISPOT and cytokine flow cytometry assays in rhesus macaques. J Immunol Methods 282: 103-115.
99. Palatnik-de-Souza CB 2008. Vaccines for leishmaniasis in the fore coming 25 years. Vaccine 26: 1709-1724.
100. Parrot L, Donatien A, Lestoquard F 1927. Notes expérimentales sur le bouton d'Orient et sur la leishmaniose canine viscérale. Arch Inst Pasteur Alger 5: 120-130.
101. Pashine A, Valiente NM, Ulmer JB 2005. Targeting the innate immune response with improved vaccine adjuvants. Nature Med 11 (Suppl.): 63-68.
102. Pitcher CJ, Hagen SI, Walker JM, Lum R, Mitchell BL, Maino VC, Axthelm MK, Picker LJ 2002. Development and homeostasis of T cell memory in rhesus macaque. J Immunol 168: 29-43.
103. Porrozzi R, Pereira MS, Teva A, Volpini AC, Pinto MA, Marchevsky RS, Barbosa AA Jr, Grimaldi G Jr 2006. Leishmania infantum-induced primary and challenge infections in rhesus monkeys (Macaca mulatta): a primate model for visceral leishmaniasis. Trans R Soc Trop Med Hyg 100: 926-937.
104. Porrozzi R, Teva A, Amaral VF, Santos da Costa MV, Grimaldi G Jr 2004. Cross-immunity experiments between different species or strains of Leishmania in rhesus macaques (Macaca Mulatta). Am J Trop Med Hyg 71: 297-305.
105. Probst RJ, Wellde BT, Lawyer PG, Stiteler JS, Rowton ED 2001. Rhesus monkey model for Leishmania major transmitted by Phlebotomus papatasi sandfly bites. Med Vet Entomol 15: 12-21.
106. Pung OJ, Hulsebos LH, Kuhn RE 1988. Experimental American leishmaniasis and Chagas' disease in the Brazilian squirrel monkey: cross immunity and electrocardiographic studies of monkeys infected with Leishmania braziliensis and Trypanosoma cruzi. Internat J Parasitol 18: 1053-1059.
107. Pung OJ, Kuhn RE 1987. Experimental leishmaniasis in the Brazilian squirrel monkey (Saimiri sciureus): lesions, hematology, cellular and humoral immune responses. J Med Primatol 16: 165-174.
108. Ramiro MJ, Zárate JJ, Hanke T, Rodriguez D, Rodriguez JR, Esteban M, Lucientes J, Castillo JA, Larraga V 2003. Protection in dogs against visceral leishmaniasis caused by Leishmania infantum is achieved by immunization with a heterologous prime-boost regime using DNA and vaccinia recombinant vectors expressing LACK. Vaccine 21: 2474-2484.
109. Ramos I, Alonso A, Marcen JM, Peris A, Castillo JA, Colmenares M, Larraga V 2008. Heterologous prime-boost vaccination with a non-replicative vaccinia recombinant vector expressing LACK confers protection against canine visceral leishmaniasis with a predominant Th1-specific immune response. Vaccine 26: 333-344.
110. Ranque J, Depieds R, Nicole RM 1960. Les phénomènes d'immunité dans les leishmanioses. Path Biol 8: 99-107.
111. Reed SG, Scott P 2000. Immunologic mechanisms in Leishmania. MW Cunningham, RS Fujinami (eds.), Effects of microbes on the immune system. Lippincott Williams & Wilkins, Philadelphia, p. 537-554.
112. + T cell responses and protection against Leishmania major infection. J Exp Med 195: 1565-1573.
113. Robinson HL, Amara RR 2005. T cell vaccines for microbial infections. Nature Med 11 (Suppl.): 25-32.
114. Rodríguez-Cortés A, Ojeda A, López-Fuertes L, Timón M, Altet L, Solano-Gallego L, Sánchez-Robert E, Francino O, Alberola J 2007. Vaccination with plasmid DNA encoding KMPII, TRYP, LACK and GP63 does not protect dogs against Leishmania infantum experimental challenge. Vaccine 25: 7962-7971.
115. Saravia NG, Weigle K, Segura I, Giannini SH, Pacheco R, Labrada LA, Gonçalves A 1990. Recurrent lesions in humans Leishmania braziliensis infection - reactivation or reinfection? Lancet 336: 398-402.
116. + T cells using heterologous prime-boost immunisation strategies. Vaccines and vaccination - Part I. Immunol Rev 170: 29-38.
117. Sharma SK, Dube A, Nadeem A, Khan S, Saleem I, Garg R, Mohammad O 2006. Non PC liposome entrapped promastigote antigens elicit parasite specific CD8+ and CD4+ T-cell immune response and protect hamsters against visceral leishmaniasis. Vaccine 24: 1800-1810.
118. Shearer MH, Dark RD, Chodosh J, Kennedy RC 1999. Comparison and caracterization of immunoglobulin G subclasses among primate species. Clin Diagn Lab Immunol 6: 953-958.
119. Silveira FT, Lainson R, Shaw JJ, Garcez LM, Souza AA, Braga RR, Ishikawa EA 1989. Experimental cutaneous leishmaniasis: I - On the susceptibility of the primate Cebus apella (Cebidae) to the infection caused by Leishmania (Viannia) lainsoni Silveira, Shaw and Ishikawa, 1987. Rev Soc Bras Med Trop 22: 125-130.
120. Silveira FT, Lainson R, Shaw JJ, Garcez LM, Souza AA, Braga RR, Ishikawa EA 1990. Experimental skin leishmaniasis: I. Course of the infection in the Cebus apella primate (Cebidae) caused by Leishmania (V.) braziliensis and L. (L.) amazonensis. Rev Soc Bras Med Trop 23: 5-12.
121. Silvestre R, Cordeiro-da-Silva A, Quaissi A 2008. Live attenuated Leishmania vaccines: a potential strategic alternative. Arch Immunol Ther Exp 56: 123-126.
122. Skeiky YAW, Coler RN, Brannon M, Stromberg E, Greeson K, Crane RT, Campos-Neto A, Reed SG 2002. Protective efficacy of a tandemly linked, multi-subunit recombinant leishmanial vaccine (Leish-111f) formulated in MPL® adjuvant. Vaccine 20: 3292-3303.
123. Souza-Lemos C, de-Campos SN, Teva A, Côrte-Real S, Fonseca EC, Porrozzi R, Grimaldi G Jr 2008. Dynamics of immune granuloma formation in a Leishmania braziliensis-induced self-limiting cutaneous infection in the primate Macaca mulatta. J Pathol 216: 375-386.
124. Stäger S, Smith DF, Kaye PM 2000. Immunization with a recombinant stage-regulated surface protein from Leishmania donovani induces protection against visceral leishmaniasis. J Immunol 165: 7064-7071.
125. Stober CB, Lange UG, Roberts MT, Alcami A, Blackwell JM 2005. IL-10 from regulatory T cells determines vaccine efficacy in murine Leishmania major infection. J Immunol 175: 2517-2524.
126. Tabbara KS 2006. Progress towards a Leishmania vaccine. Saudi Med J 27: 942-950.
127. Tapia E, Pérez-Jiménez E, López-Fuertes L, Gonzalo R, Gherardi MM, Esteban M 2003. The combination of DNA vectors expressing IL-12 + IL-18 elicits high protective immune response against cutaneous leishmaniasis after priming with DNA-p36/LACK and the cytokines, followed by a booster with a vaccinia virus recombinant expressing p36/LACK. Microbes Infect 5: 73-84.
128. Teva A, Porrozzi R, Cupolillo E, Oliveira-Neto MP, Grimaldi G Jr 2005. Responses of Leishmania (Viannia) braziliensis cutaneous infection to N-methylglucamine antimoniate in the rhesus monkey (Macaca mulatta) model. J Parasitol 91: 976-978.
129. Teva A, Porrozzi R, Cupolillo E, Pirmes C, Oliveira-Neto MP, Grimaldi G Jr 2003. Leishmania (Viannia) braziliensis-induced chronic granulomatous cutaneous lesions affecting the nasal mucosa in the rhesus monkey (Macaca mulatta) model. Parasitology 127: 437-447.
130. Titus RG, Bishop JV, Mejia JS 2006. The immunomodulatory factors of arthropod saliva and the potential for these factors to serve as vaccine targets to prevent pathogen transmission. Parasite Immunol 28: 131-141.
131. Valenzuela JG, Belkaid Y, Garfield MK, Mendez S, Kamhawi S, Rowton ED, Sacks DL, Ribeiro JMC 2001. Toward a defined anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. J Exp Med 194: 331-342.
132. Vanloubbeeck Y, Jones DE 2004. The immunology of Leishmania infection and the implications for vaccine development. Ann N Y Acad Sci 1026: 267-272.
133. Verthelyi D, Kenney RT, Seder RA, Gam AA, Friedag B, Klinman DM 2002. CpG Oligodeoxynucleotides as vaccine adjuvants in primates. J Immunol 168: 1659-1663.
134. Von Stebut E 2007. Immunology of cutaneous leishmaniasis: the role of mast cells, phagocytes and dendritic cells for protective immunity. Eur J Dermatol 17: 115-122.
135. Vouldoukis I, Ogunkolade W, Strazielle L, Ploton I, Monjour L 1986. Susceptibility of Cebus nigrivittatus to Leishmania infantum. J Parasitol 72: 472-473.
136. Watkins DI, Kannagi M, Stone ME, Letvin NL 1988. Major histocompatibility complex class I molecules of nonhuman primates. Eur J Immunol 18: 1425-1432.
137. Webb JR, Campos-Neto, Ovendale PJ, Martin TI, Stromberg EJ, Badaro R, Reed SG 1998. Human and murine immune responses to a novel Leishmania major recombinant protein encoded by members of a multicopy gene family. Infec Immun 66: 3279-3289.
138. Webb JR, Kaufmann D, Campos-Neto, Reed SG 1996. Molecular cloning of a novel protein antigen of Leishmania major that elicits a potent immune response in experimental murine leishmaniasis. J Immunol 157: 5034-5041.
139. Wolf RE 1976. Immune response to Leishmania tropica in Macaca mulatta. J Parasitol 62: 209-214.
140. Zadeh-Vakili A, Taheri T, Taslimi Y, Doustdari F, Salmanian AH, Rafati S 2004. Immunization with the hybrid protein vaccine, consisting of Leishmania major cysteine proteinases Type I (CPB) and Type II (CPA), partially protects against leishmaniasis. Vaccine 22: 1930-1940.
141. Zanin FH, Coelho EA, Tavares CA, Marques-da-Silva EA, Silva Costa MM, Rezende SA, Gazzinelli RT, Fernandes AP 2007. Evaluation of immune responses and protection induced by A2 and nucleoside hydrolase (NH) DNA vaccines against Leishmania chagasi and Leishmania amazonensis experimental infections. Microbes Infect 9: 1070-1077.
142. Zaph C, Uzonna J, Beverley SM, Scott P 2004. Central memory T cells mediate long-term immunity to Leishmania major in the absence of persistent parasites. Nature Med 10: 1104 -1110.