Mimotope-based vaccines of leishmania infantum antigens and their protective efficacy against visceral leishmaniasis

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Costa, Lourena Emanuele ^a   Goulart, Luiz Ricardo ^b,c   De Jesus Pereira, Nathália Cristina ^a   Lima, Mayara Ingrid Sousa ^b   Duarte, Mariana Costa ^a   Martins, Vivian Tamietti ^a   Lage, Paula Sousa ^a   Menezes Souza, Daniel ^a   Ribeiro, Tatiana Gomes ^a   Melo, Maria Norma ^a   Fernandes, Ana Paula ^a   Soto, Manuel ^d   Tavares, Carlos Alberto Pereira ^a   Cház Fumagalli, Miguel Angel ^a   Coelho, Eduardo Antonio Ferraz ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b FEDERAL UNIVERSITY OF UBERLÂNDIA   (Brazil)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; CYTOKINE; EPITOPE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN G2A ANTIBODY; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 4; LEISHMANIA INFANTUM ANTIGEN; LEISHMANIA VACCINE; PARASITE ANTIGEN; PEPTIDE; SAPONIN; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; ARTICLE; BONE MARROW; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOG; DRUG EFFICACY; FEMALE; IMMUNOSTIMULATION; IN VITRO STUDY; LEISHMANIA INFANTUM; LIVER; LYMPH NODE; MALE; MOLECULAR CLONING; MOUSE; NONHUMAN; PARASITE LOAD; PHAGE DISPLAY; SPLEEN; SPLEEN CELL; TH1 CELL; VISCERAL LEISHMANIASIS; WILD TYPE; ANIMAL; DISEASE MODEL; IMMUNOLOGY; LEISHMANIASIS, VISCERAL; PARASITOLOGY;

LEISHMANIA INFANTUM;

ANIMALS; ANTIGENS, PROTOZOAN; DISEASE MODELS, ANIMAL; DOGS; EPITOPES; LEISHMANIA INFANTUM; LEISHMANIASIS VACCINES; LEISHMANIASIS, VISCERAL; MICE;

EID: 84908030720     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110014     Document Type: Article

References (81)

1. Desjeux P (2004) Leishmaniasis: current situation and new perspectives.Comparative Immunology, Comp Immunol Microbiol Infect Dis 27: 305-318.
2. World Health Organization (2010) Control of the leishmaniases: report of a meeting of the 399 WHO Expert Committee on the Control of Leishmaniases. Available: http://whqlibdoc.who.int/trs/WHO-TRS-949-eng.pdf. Accessed 2014 September 28.
3. Alvar J, Ve'lez ID, Bern C, Herrero M, Desjeux P, et al. (2012) Leishmaniasis worldwide and global estimates of its incidence. PloS One 7: 1-12.
4. Baneth G, Koutinas AF, Solano-Gallego L, Bourdeau P, Ferrer L (2008) Canine leishmaniosis - new concepts and insights on an expanding zoonosis: part one. Trends Parasitol 24: 324-330.
5. Gramiccia M, Gradoni L (2005) The current status of zoonotic leishmaniases and approaches to disease control. Int J Parasitol 35: 1169-1180.
6. Cruz I, Acosta L, Gutiérrez MN, Nieto J, Cañavate C (2010) A canine leishmaniasis pilot survey in an emerging focus of visceral leishmaniasis: Posadas (Misiones, Argentina). BMC Infect Dis 10: 342.
7. Duprey ZH, Steurer FJ, Rooney JA, Kirchhoff L V, Jackson JE, et al. (2006) Canine Visceral Leishmaniasis in United States and Canada, 2000-2003. Emerg Infect Dis 12: 440-446.
8. Croft SL, Coombs GH (2003) Leishmaniasis-current chemotherapy and recent advances in the search for novel drugs. Trends Parasitol 19: 502-508.
9. Minodier P, Parola P (2010) Cutaneous leishmaniasis treatment. Travel Med Infect Dis 5: 150-158.
10. Costa CHN, Peters NC, Maruyama SR, Brito Jr EC, Santos IKFM (2011) Vaccines for the leishmaniases: proposals for a research agenda. The working group on research priorities for development of leishmaniasis vaccines. PLoS Negl Trop Dis 5: e943.
11. Coelho EAF, Tavares CA, Carvalho FA, Chaves KF, Teixeira KN, et al. (2003) Immune responses induced by the Leishmania (Leishmania) donovani A2 antigen, but not by the LACK antigen, are protective against experimental Leishmania (Leishmania) amazonensis infection. Infect Immun 71: 3988-3994.
12. Coelho EAF, Ram?rez L, Costa MA, Coelho VT, Martins VT, et al. (2009) Specific serodiagnosis of canine visceral leishmaniasis using Leishmania species ribosomal protein extracts. Clin Vaccine Immunol 16: 1774-1780.
13. Ram?rez L, Santos DM, Souza AP, Coelho EA, Barral A, et al. (2013) Evaluation of immune responses and analysis of the effect of vaccination of the Leishmania major recombinant ribosomal proteins L3 or L5 in two different murine models of cutaneous leishmaniasis. Vaccine 31: 1312-1319.
14. Ramirez L, Villen LC, Duarte MC, Chávez-Fumagalli MA, Valadares DG, et al. (2014) Cross-protective effect of a combined L5 plus L3 Leishmania major ribosomal protein based vaccine combined with a Th1 adjuvant in murine cutaneous and visceral leishmaniasis. Parasites & Vectors 2: 3-10.
15. Martins VT, Chávez-Fumagalli MA, Costa LE, Canavaci AMC, Martins AMCC, et al. (2013) Antigenicity and protective efficacy of a Leishmania amastigote-specific protein, member of the super-oxygenase family, against visceral leishmaniasis. PLoS Negl Trop Dis 7: e2148.
16. Coelho VT, Oliveira JS, Valadares DG, Chávez-Fumagalli MA, Duarte MC, et al. (2012) Identification of proteins in promastigote and amastigote-like leishmania using an immunoproteomic approach. PLoS Negl Trop Dis 6: e1430.
17. Vieira LQ, Goldschmidt M, Nashleanas M, Pfeffer K, Mak T, et al. (1996) Mice lacking the TNF receptor p55 fail to resolve lesions caused by infection with Leishmania major, but control parasite replication. J Immunol 157: 827-835.
18. Lima MM, Sarquis O, Oliveira TG, Gomes TF, Coutinho C, et al. (2012) Investigation of Chagas disease in four periurban areas in northeastern Brazil: epidemiologic survey in man, vectors, non-human hosts and reservoirs. Trans R Soc Trop Med Hyg 106: 143-149.
19. Roque AL, Xavier SC, Gerhardt M, Silva MF, Lima VS, et al. (2012) Trypanosoma cruzi among wild and domestic mammals in different areas of the Abaetetuba municipality (Para´State, Brazil), an endemic Chagas disease transmission area. Vet Parasitol 193: 71-77.
20. Zanin FH, Coelho EA, Tavares CA, Marques-da-Silva EA, Costa MMS, et al. (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.
21. Fernandes AP, Costa MMS, Coelho EAF, Michalick MSM, Freitas E, et al. (2008) Protective immunity against challenge with Leishmania (Leishmania)chagasi in beagle dogs vaccinated with recombinant A2 protein. Vaccine 26: 5888-5895.
22. Clark JR, March JB (2004) Bacteriophage-mediated nucleic acid immunisation. FEMS Immunol Med Microbiol 40: 21-26.
23. Smith PG, Petrenko VA (1997) Phage display. Chem Rev 97: 391-410.
24. Barbas CF, Burton DR, Scott JK, Silverman GJ (2001) Phage display: a laboratory manual. New York: Cold Spring Harbor Laboratory Press. 738 p.
25. Wang LF, Yu M (2004) Epitope identification and discovery using phage display libraries: applications in vaccine development and diagnostics. Curr Drug Targets 5: 1-15.
26. Germaschewski V, Murray K (1995) Screening a monoclonal antibody with a fusion-phage display library shows a discontinuity in a linear epitope within PreS1 of hepatitis B virus. J Med Virol 45: 300-305.
27. Greenwood J, Willis A, Perham R (1991) Multiple display of foreign peptides on a filamentous bacteriophage. Peptides from Plasmodium falciparum circumsporozoite protein as antigens. J Mol Biol 220: 821-827.
28. Monette M, Opella S, Greenwood J, Willis A, Perham R (2001) Structure of a malaria parasite antigenic determinant displayed on filamentous bacteriophage determined by NMR spectroscopy: implications for the structure of continuous pep- tide epitopes of proteins. Protein Sci 10: 1150-1159.
29. Demangel C, Lafaye P, Mazie J (1996) Reproducing the immune response against the Plasmodium vivax merozoite surface protein 1 with mimotopes selected from a phage-displayed peptide library. Mol Immunol 33: 909-916.
30. Costa LE, Lima MIS, Chávez-Fumagalli MA, Menezes-Souza D, Martins VT, et al. (2014) Subtractive phage display selection from canine visceral leishmaniasis identifies novel epitopes that mimic Leishmania infantum antigens with potential serodiagnosis applications. Clin Vaccine Immunol 21: 96-106.
31. Beghetto E, Spadoni A, Buffolano W, Pezzo M, Minenkova O, et al. (2003) Molecular dissection of the human B-cell response against Toxoplasma gondii infection by lambda display of cDNA libraries. Int J Parasitol 33: 163-173.
32. Cunha-Junior J, Silva D, Silva N, Souza M, Souza G, et al. (2010) A4D12 monoclonal antibody recognizes a new linear epitope from SAG2A Toxoplasma gondii tachyzoites, identified by phage display bioselection. Immunobiology 215: 26-37.
33. Pitcovsky TA, Mucci J, Alvarez P, Leguizamon MS, Burrone O, et al. (2001) Epitope mapping of trans-sialidase from Trypanosoma cruzi reveals the presence of several cross-reactive determinants. Infect Immun 69: 1869-1875.
34. Manoutcharian K, D?az-Orea A, Gevorkian G, Fragoso G, Acero G, et al. (2004) Recombinant bacteriophage-based multiepitope vaccine against Taenia solium pig cysticercosis. Vet Immunol Immunopathol 99: 11-24.
35. Gu Y, Li J, Zhu X, Yang J, Li Q, et al. (2008) Trichinella spiralis: characterization of phage-displayed specific epitopes and their protective immunity in balb/c mice. Exp Parasitol 118: 66-74.
36. Frenkel D, Katz O, Solomon B (2000) Immunization against Alzheimer's Bamyloid plaques via EFRH phage administration. Proc Natl Acad Sci USA 97: 11455-11459.
37. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
38. Shtatland T, Guettler D, Kossodo M, Pivovarov M, Weissleder R (2007) PepBank-a database of peptides based on sequence text mining and public peptide data sources. BMC Bioinformatics 8: 280.
39. Ru B, Huang J, Dai P, Li S, Xia Z, et al. (2010) MimoDB: a new repository for mimotope data derived from phage display technology. Molecules 15: 8279-8288.
40. Huang J, Ru B, Li S, Lin H, Guo FB (2010) SAROTUP: scanner and reporter of target-unrelated peptides. J Biomed Biotechnol 2010: 101932.
41. Jayanna PK, Bedi D, Deinnocentes P, Bird RC, Petrenko V (2010) Landscape phage ligands for PC3 prostate carcinoma cells. Protein Eng Des Sel 23: 423-430.
42. Coelho VTS, Oliveira JS, Valadares DG, Duarte MC, Cha'vez-Fumagalli MA, et al. (2012) Identification of proteins in promastigote and amastigote-like Leishmania using an immunoproteomic approach. PLoS Negl Trop Dis 6: e1430.
43. Carrión J, Nieto A, Iborra S, Iniesta V, Soto M, et al. (2006) Immunohistological features of visceral leishmaniasis in BALB/c mice. Parasite Immunol 28: 173-183.
44. Lehmann J, Enssle KH, Lehmann I, Emmendorfer A, Lohmann-Matthes ML (2000) The capacity to produce IFN-gamma rather than the presence of interleukin-4 determines the resistance and the degree of susceptibility to Leishmania donovani infection in mice. J Interferon Cytokine Res 20: 63-77.
45. Oliveira DM, Valadares DG, Duarte MC, Costa LE, Martins VT, et al. (2012)Evaluation of parasitological and immunological parameters of Leishmania chagasi infection in BALB/c mice using different doses and routes of inoculation of parasites. Parasitol Res 110: 1277-1285.
46. Afonso LC, Scott P (1993) Immune responses associated with susceptibility of C57BL/10 mice to Leishmania amazonensis . Infect Immun 61: 2952-2959.
47. Parmley SF, Smith GP (1988) Antibody-selectable filamentous fd phage vectors: affinity purification of target genes. Genes 73: 305-318.
48. Scott JK, Smith GP (1990) Searching for peptide ligands with an epitope library. Science 249: 386-390.
49. Hardy B, Raiter A (2005) A mimotope peptide-based anti-cancer vaccine selected by BAT monoclonal antibody. Vaccine 23: 4283-4291.
50. Wagner S, Hafner C, Allwardt D, Jasinska J, Ferrone S, et al. (2005) Vaccination with a human high molecular weight melanoma-associated antigen mimotope induces a humoral response inhibiting melanoma cell growth in vitro. J Immunol 174: 976-982.
51. Coomber DWJ, Ward RL, Coomber DWJ, Ward RL (2001) Isolation of human antibodies against the central DNA binding domain of p53 from an individual with colorectal cancer using antibody phage display isolation of human antibodies against the central DNA binding domain of p53 from an individual with colorect. Clin Cancer Res 7: 2802-2808.
52. Wan Y, Wu Y, Bian J, Wang XZ, Zhou W (2001) Induction of hepatitis B virusspecific cytotoxic T lymphocytes response in vivo by filamentous phage display vaccine. Vaccine 19: 2918-2923.
53. Van der Vaart JM, Pant N, Wolvers D, Bezemer S, Hermans PW, et al. (2006) Reduction in morbidity of rotavirus induced diarrhoea in mice by yeast produced monovalent llama-derived antibody fragments. Vaccine 24: 4130-4137.
54. Ledón T, Ferrán B, Pérez C, Suzarte E, Vichi J, et al. (2012) TLP01, an mshA mutant of Vibrio cholerae O139 as vaccine candidate against cholera. Microbes Infect 14: 968-978.
55. Yang Q, Wang L, Lu D, Gao R, Song J, et al. (2005) Prophylactic vaccination with phage-displayed epitope of C. albicans elicits protective immune responses against systemic candidiasis in C57BL/6 mice. Vaccine 23: 4088-4096.
56. Gnanasekar M, Rao KVN, He Y, Mishra PK, Nutman TB, et al. (2004) Novel phage display-based subtractive screening to identify vaccine candidates of Brugia malayi. Infect Immun 72: 4707-4715.
57. Wu HW, Hu XM, Wang Y, Kurtis JD, Zeng FJ, et al. (2006) Protective immunity induced by phage displayed mitochondrial related peptides of Schistosoma japonicum. Acta Tropica 99: 200-207.
58. Manoutcharian K, Terrazas LI, Gevorkian G, Acero G, Petrossian P, et al. (1999) Phage-displayed T-cell epitope grafted into immunoglobulin heavy-chain complementarity-determining regions: an effective vaccine design tested in murine cysticercosis. Infect Immun 67: 4764-4770.
59. Gaubin M, Fanutti C, Mishal Z, Durrbach A, Berardinis P, et al. (2003) Processing of filamentous bacteriophage virions in antigen-presenting cells targets both HLA class I and class II peptide loading compartments. DNA Cell Biol 22: 11-18.
60. Adhya S, Merril CR, Biswas B (2014) Therapeutic and prophylactic applications of bacteriophage components in modern medicine. Cold Spring Harb Perspect Med 4: a012518.
61. Gu Y, Li J, Zhu X, Yang J, Li Q, et al. (2008) Trichinella spiralis: characterization of phage-displayed specific epitopes and their protective immunity in BALB/c mice. Exp Parasitol 118: 66-74.
62. Mason KA, Ariga H, Neal R, Valdecanas D, Hunter N, et al. (2005) Targeting toll-like receptor 9 with CPG oligodeoxynucleotides enhances tumor response to fractionated radiotherapy targeting toll-like receptor 9 with CPG oligodeoxynucleotidesenhances tumor response to fractionated radiotherapy. Clin Cancer Res 11: 361-369.
63. Hashiguchi S, Yamaguchi Y, Takeuchi O, Akira S, Sugimura K (2010) Immunological basis of M13 phage vaccine: regulation under MyD88 and TLR9 signaling. Biochem Biophys Res Commun 402: 19-22.
64. Cui J, Ren HJ, Liu RD, Wang L, Zhang ZF (2013) Phage-displayed specific polypeptide antigens induce significant protective immunity against Trichinella spiralis infection in BALB/c mice. Vaccine 6: 1171-1177.
65. Pouyanfard S, Bamdad T, Hashemi H, Bandehpour M, Kazemi B (2012) Induction of protective anti-CTL epitope responses against HER-2-positive breast cancer based on multivalent T7 phage nanoparticles. PLoS One 7: e49539.
66. Prudencio CR, Rodrigues AAR, Cardoso R, Souza GR, SzabóMP (2011) Cutaneous hypersensitivity test to evaluate phage display anti-tick borne vaccine antigen candidates. Exp Parasitol 129: 388-392.
67. Ribeiro VS, Araújo TG, Gonzaga HT, Nascimento R, Goulart LR (2013) Development of specific scFv antibodies to detect neurocysticercosis antigens and potential applications in immunodiagnosis. Immunol Letters 156: 59-67.
68. Gumy A, Louis J, Launois P (2004) The murine model of infection with Leishmania major and its importance for the deciphering of mechanisms underlying differences in Th cell differentiation in mice from different genetic backgrounds. Int J Parasitol 34: 433-444.
69. Mizbani A, Taheri T, Zahedifard F, Taslimi Y, Azizi H, et al. (2009) Recombinant Leishmania tarentolae expressing the A2 virulence gene as a novel candidate vaccine against visceral leishmaniasis. Vaccine 28: 53-62.
70. Handman E (2001) Leishmaniasis: current status of vaccine development. Clin Microbiol Rev 14: 229-243.
71. Spitzer N, Jardim A, Lippert D, Olafson RW (1999) Long-term protection of mice against Leishmania major with a synthetic peptide vaccine. Vaccine 17: 1298-1300.
72. Wu W, Huang L, Mendez S (2010) A live Leishmania major vaccine containing CpG motifs induces the de novo generation of Th17 cells in C57BL/6 mice. Eur J Immunol 40: 2517-2527.
73. Bruhn KW, Birnbaum R, Haskell J, Vanchinathan V, Greger S, et al. (2012) Killed but metabolically active Leishmania infantum as a novel whole-cell vaccine for visceral leishmaniasis. Clin Vaccine Immunol 19: 490-498.
74. Awasthi A, Mathur RK, Saha B (2004) Immune response to Leishmania infection. Indian J Med Res 119: 238-258.
75. Murphy ML, Wille U, Villegas EN, Hunter CA, Farrell JP (2001) IL-10 mediates susceptibility to Leishmania donovani infection. Eur J Immunol 31: 2848-2856.
76. Murray HW, Lu CM, Mauze S, Freeman S, Moreira AL, et al. (2002) Interleukin-10 (IL-10) in experimental visceral leishmaniasis and IL-10 receptor blockade as immunotherapy. Infect Immun 70: 6284-6293.
77. Cha'vez-Fumagalli MA, Costa MA, Oliveira DM, Ram?rez L, Costa LE, et al (2010) Vaccination with the Leishmania infantum ribosomal proteins induces protection in BALB/c mice against Leishmania chagasi and Leishmania amazonensis challenge. Microbes Infect 12: 967-977.
78. Garg R, Dube A (2006) Animal models for vaccine studies for visceral leishmaniasis. Indian J Med Res 123: 439-454.
79. Dumas C, Muyombwe A, Roy G, Matte C, Ouellette M, et al. (2003) Recombinant Leishmania major secreting biologically active granulocytemacrophage colony-stimulating factor survives poorly in macrophages in vitro and delays disease development in mice. Infect Immun 71: 6499-6509.
80. Murray HW, Cervia JS, Hariprashad J, Taylor AP, Stoeckle MY, et al. (1995) Effect of granulocyte-macrophage colony-stimulating factor in experimental visceral leishmaniasis. J Clin Invest 95: 1183-1192.
81. Badaró R, Lobo I, Nakatani M, Muinos A, Netto EM, et al. (2001) Successful use of a defined antigen/GM-CSF adjuvant vaccine to treat mucosal leishmaniasis refractory to antimony: a case report. Braz J Infect Dis 5: 223-232.