Molecular and immunological tools for the evaluation of the cellular immune response in the neotropical monkey Saimiri sciureus, a non-human primate model for malaria research

Malaria Journal

Volumn 14, Issue 1, 2015, Pages 1-17

  Riccio, Evelyn KP ^a   Pratt Riccio, Lilian R ^a   Bianco Júnior, Cesare ^a   Sanchez, Violette ^a,b   Totino, Paulo RR ^a   Carvalho, Leonardo JM ^a   Daniel Ribeiro, Cláudio Tadeu ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b SANOFI PASTEUR   (France)

Author keywords

Cellular response; Cytokines; Immune response; Malaria; Saimiri sciureus

Indexed keywords

BETA INTERFERON; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; IONOMYCIN; PHORBOL 13 ACETATE 12 MYRISTATE; TUMOR NECROSIS FACTOR; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD SAMPLING; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS REACTION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; GENE EXPRESSION; GENE EXPRESSION ASSAY; HUMAN; IMMUNOLOGICAL PROCEDURES; IN VITRO STUDY; INTERMETHOD COMPARISON; LIMIT OF DETECTION; MALARIA; NEOTROPICS; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; REAL TIME POLYMERASE CHAIN REACTION; SAIMIRI SCIUREUS; SPLEEN CELL; SPLENECTOMY; ANIMAL; COMPARATIVE STUDY; DISEASE MODEL; IMMUNOLOGY; MONONUCLEAR CELL; PROCEDURES; SQUIRREL MONKEY;

ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; ENZYME-LINKED IMMUNOSPOT ASSAY; IMMUNITY, CELLULAR; LEUKOCYTES, MONONUCLEAR; MALARIA; REAL-TIME POLYMERASE CHAIN REACTION; SAIMIRI;

EID: 84928605842     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/s12936-015-0688-1     Document Type: Article

References (52)

1. MacDonald DM, Holmes EC, Lewis JCM, Simmonds PJ. Detection of hepatitis B virus infection in wild-born chimpanzees (Pan troglodytes verus): phylogenetic relationships with human and other primate genotypes. J Virol. 2000;74:4253-7.
2. Makuwa M, Souquiere S, Clifford SL, Mouinga-Ondeme A, Bawe-Johnson M, Wickings EJ. Identification of hepatitis B virus genome in faecal sample from wild living chimpanzee (Pan troglodytes troglodytes) in Gabon. J Clin Virol. 2005;34:83-8.
3. Carcamo WC, Nguyen CQ. Advancement in the development of models for hepatitis C research. J Biomed Biotechnol. 2012;2012:346761.
4. Dupinay T, Gheit T, Roques P, Cova L, Chevallier-Queyron P, Tasahsu SI, et al. Discovery of naturally occurring transmissible chronic hepatitis B virus infection among Macaca fascicularis from Mauritius Island. Hepatology. 2013;58:1610-20.
5. Li T, Zhu S, Shuai L, Xu Y, Yin S, Bian Y, et al. Infection of common marmosets with hepatitis C virus/GB virus-B chimeras. Hepatology. 2014;59:789-802.
6. Staprans SI, Feinberg MB. The roles of nonhuman primates in the preclinical evaluation of candidate AIDS vaccines. Expert Rev Vaccines. 2004;3:S5-32.
7. Morgan C, Marthas M, Miller C, Duerr A, Cheng-Mayer C, Desrosiers R, et al. The use of nonhuman primate models in HIV vaccine development. PLoS Med. 2008;5:e173.
8. Singh S, Nehete P, Hanley P, Nehete B, Yang G, He H, et al. Procedures for mucosal immunization and analyses of cellular immune response to candidate HIV vaccines in murine and nonhuman primate models. Methods Mol Biol. 2014;1184:417-55.
9. Gardner MB, Luciw PA. Macaque models of human infectious disease. ILAR J. 2008;49:220-55.
10. Good MF. The hope but challenge for developing a vaccine that might control malaria. Eur J Immunol. 2009;39:939-43.
11. Wykes MN, Good MF. What have we learnt from mouse models for the study of malaria? Eur J Immunol. 2009;39:2004-7.
12. Langhorne J, Buffet P, Galinski M, Good M, Harty J, Leroy D, et al. The relevance of non-human primate and rodent malaria models for humans. Malar J. 2011;10:23.
13. Teixeira C, Gomes R. Experimental models in vaccine research: malaria and leishmaniasis. Braz J Med Biol Res. 2013;46:109-16.
14. Krief S, Escalante AA, Pacheco MA, Mugisha L, André C, Halbwax M. On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from Bonobos. PLoS Pathog. 2010;6:e1000765.
15. Prugnolle F, Ollomo B, Durand P, Yalcindag E, Arnathau C, Elguero E. African monkeys are infected by Plasmodium falciparum nonhuman primate-specific strains. Proc Natl Acad Sci U S A. 2011;108:11948-53.
16. Sharp PM, Liu W, Learn GH, Rayner JC, Peeters M, Hahn BH. Source of the human malaria parasite Plasmodium falciparum. Proc Natl Acad Sci U S A. 2011;108:744-5.
17. WHO. Role of non-human primates in malaria vaccine development: memorandum from WHO meeting. Bull World Health Organ. 1988;66:719-28.
18. Kennedy RC, Shearer MH, Hildebrand WH, Simmonds RS. Non-human primates and their potential use in immunologically based investigations. The Immunologist. 1997;5:150-6.
19. Reynolds J. Report on the biomedical primate research center. Annual resource guide. Primate supply information clearinghouse. US: Washington Regional Primate Research Center; 2001.
20. Bailey J. Non-human primates in medical research and drug development: a critical review. Biog Amines. 2005;19:235-55.
21. Carvalho LJM, Oliveira SG, Alves FA, Brígido MCO, Muniz JAPC, Daniel-Ribeiro CT. Aotus infulatus monkey is susceptible to Plasmodium falciparum and may constitute an alternative experimental model for malaria. Mem Inst Oswaldo Cruz. 2000;95:363-5.
22. Herrera S, Perlaza BL, Bonelo A, Arévalo-Herrera M. Aotus monkeys: their great value for anti-malaria vaccines and drug testing. Int J Parasitol. 2002;32:1625-35.
23. Carvalho LJM, Alves FA, Oliveira SG, Valle RR, Fernandes AAM, Muniz JAPC. Severe anemia affects both splenectomized and non-splenectomized Plasmodium falciparum-infected Aotus infulatus monkeys. Mem Inst Oswaldo Cruz. 2003;98:679-86.
24. Carvalho LJ, Oliveira SG, Theisen M, Alves FA, Andrade MC, Zanini GM, et al. Immunization of Saimiri sciureus monkeys with Plasmodium falciparum merozoite surface protein-3 and glutamate-rich protein suggests that protection is related to antibody levels. Scand J Immunol. 2004;59:363-72.
25. Carvalho LJ, Alves FA, Bianco Jr C, Oliveira SG, Zanini GM, Soe S, et al. Immunization of Saimiri sciureus monkeys with a recombinant hybrid protein derived from the Plasmodium falciparum antigen glutamate-rich protein and merozoite surface protein 3 can induce partial protection with Freund and Montanide ISA720 adjuvants. Clin Diagn Lab Immunol. 2005;12:242-8.
26. Arévalo-Herrera M, Vera O, Castellanos A, Céspedes N, Soto L, Corradin G, et al. Preclinical vaccine study of Plasmodium vivax circumsporozoite protein derived-synthetic polypeptides formulated in montanide ISA 720 and montanide ISA 51 adjuvants. Am J Trop Med Hyg. 2011;84:21-7.
27. Craig AG, Grau GE, Janse C, Kazura JW, Milner D, Barnwell JW, et al. The role of animal models for research on severe malaria. PLoS Pathog. 2012;8:e1002401.
28. Villinger F, Brar SS, Mayne A, Chikkala N, Ansari AA. Comparative sequence analysis of cytokine genes from human and nonhuman primates. J Immunol. 1995;155:3946-54.
29. Delgado G, Parra-Lopez C, Spinel C, Patarroyo ML. 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. 2005;23:3386-95.
30. Heraud JM, Lavergne A, Kazanji M. Molecular cloning, characterization, and quantification of squirrel monkey (Saimiri sciureus) Th1 and Th2 cytokines. Immunogenetics. 2002;54:20-9.
31. Hernández EC, Suárez CF, Méndez JA, Echeverry SJ, Murillo LA, Patarroyo ME. Identification, cloning and sequencing of different cytokine genes in four species of owl monkey. Immunogenetics. 2002;54:645-53.
32. Mérien F, Lavergne A, Behr C, Contamin H. Sequencing and analysis of genomic DNA and cDNA encoding TNF in squirrel monkey (Saimiri sciureus). Vet Immunol Immunopathol. 2003;92:37-43.
33. Alves FA, Souza MT, Gonçalves EC, Schneider MP, Marinho AM, Muniz JA, et al. DNA sequencing of 13 cytokine gene fragments of Aotus infulatus and Saimiri sciureus, two non-human primate models for malaria. Cytokine. 2010;52:151-5.
34. Walsh DS, Pichyangkul S, Gettayacamin M, Tongtawe P, Siegrist CA, Hansukjariya P, et al. Safety and immunogenicity of RTS, S + TRAP malaria vaccine, formulated in the AS02A adjuvant system, in infant Rhesus monkeys. Am J Trop Med Hyg. 2004;70:499-509.
35. WHO: World Malaria report 2013. http://www.who.int/malaria/publications/world-malaria-report-2013/report/en/.
36. Miller LH, Baruch DI, Marsh K, Doumbo OK. The pathogenic basis of malaria. Nature. 2002;415:673-9.
37. Carvalho LJM, Daniel-Ribeiro CT, Goto H. Malaria vaccine: candidate antigens, mechanisms, constraints and prospects. Scand J Immunol. 2002;56:327-43.
38. Lorenz V, Karanis G, Karanis P. Malaria vaccine development and how external forces shape it: an overview. Int J Environ Res Public Health. 2014;11:6791-807.
39. Barry AE, Arnott A. Strategies for designing and monitoring malaria vaccines targeting diverse antigens. Front Immunol. 2014;5:1-16.
40. Huang DT, Hadian M. Bench-to-bedside review: human subjects research - are more standards needed? Crit Care. 2006;10:244.
41. Legrand N, Weijer K, Spits H. Experimental models to study development and fuction of the human immune system in vivo. J of Immunol. 2006;176:2053-8.
42. Baruch DI, Gamain B, Barnwell JW, Sullivan JS, Stowers A, Galland GG, et al. Immunization of Aotus monkeys with a functional domain of the Plasmodium falciparum variant antigen induces protection against a lethal parasite line. Proc Natl Acad Sci U S A. 2002;99:3860-5.
43. Egan AF, Fabucci ME, Saul A, Kaslow DC, Miller LH. Aotus New World monkeys: models for studying malaria-induced anemia. Blood. 2002;99:3863-6.
44. Jones TR, Gramzinski RA, Aguiar JC, Sim BK, Narum DL, Fuhrmann SR, et al. Absence of antigenic competition in monkeys immunized with Plasmodium falciparum DNA vaccines delivered as a mixture. Vaccine. 2002;20:1675-80.
45. Lyon JA, Angov E, Fay MP, Sullivan JS, Girourd AS, Robinson SI, et al. Protection induced by Plasmodium falciparum MSP1 (42) is strain-specific, antigen and adjuvant dependent, and correlates with antibody responses. PLoS One. 2008;3:e2830.
46. Iriemenam NC, Okafor CM, Balogun HA, Ayede I, Omosun Y, Persson JO, et al. Cytokine profiles and antibody responses to Plasmodium falciparum malaria infection in individuals living in Ibadan, southwest Nigeria. Afr Health Sci. 2009;9:66-74.
47. Diaz D, Daubenberger CA, Zalac T, Rodriguez R, Patarroyo ME. Sequence and expression of MHC-DPB1 molecules of the New World monkey Aotus nancymaae, a primate model for Plasmodium falciparum. Immunogenetics. 2002;54:251-9.
48. Kazanji M, Heraud JM, Merien F, Pique C, de Thé G, Gessain A, et al. Chimeric peptide vaccine composed of B- and T-cell epitopes of human T-cell leukemia virus type 1 induces humoral and cellular immune responses and reduces the proviral load in immunized squirrel monkeys (Saimiri sciureus). J Gen Virol. 2006;87:1331-7.
49. Villinger F, Hunt D, Mayne A, Vuchetich M, Findley H, Ansari AA. Qualitative and quantitative studies of cytokines synthesized and secreted by non-human primate peripheral blood mononuclear cells. Cytokine. 1993;5:469-79.
50. Contamin H, Loizon S, Bourreau E, Michel JC, Garraud O, Mercereau- Puijalon O, et al. Flow cytometry identification and characterization of mononuclear cell subsets in the neotropical primate Saimiri sciureus (squirrel monkey). J Immunol Methods. 2005;297:61-71.
51. Daubenberger CA, Spirig R, Patarroyo ME, Pluschke G. Flow cytometric analysis on cross-reactivity of human-specific CD monoclonal antibodies with splenocytes of Aotus nancymaae, a non-human primate model for biomedical research. Vet Immunol Immunopathol. 2007;119:14-20.
52. Alves FA, Pelajo-Machado M, Totino PRR, Souza MT, Gonçalves EC, Schneider MPC, et al. Splenic architecture disruption and parasite-induced splenocyte activation and anergy in Plasmodium falciparum -infected Saimiri sciureus monkeys. Malar J. 2015;14:128.