Cellular vaccination with bone marrow-derived dendritic cells pulsed with a peptide of Leishmania infantum KMP-11 and CpG oligonucleotides induces protection in a murine model of visceral leishmaniasis

Vaccine

Volumn 29, Issue 31, 2011, Pages 5053-5064

  Agallou, Maria ^a   Margaroni, Maritsa ^a   Karagouni, Evdokia ^a  

^a HELLENIC PASTEUR INSTITUTE   (Greece)

Author keywords

CpG ODNs; DCs based vaccine; IFN ; IgG1; IgG2a; IL 10; IL 12; IL 17; KMP 11; Murine visceral leishmaniasis; TGF

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; GAMMA INTERFERON; GAMMA INTERFERON ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; INTERLEUKIN 10; INTERLEUKIN 10 ANTIBODY; INTERLEUKIN 12; INTERLEUKIN 17; KINETOPLASTID MEMBRANE PROTEIN 11 12 31AA; LEISHMANIA VACCINE; ODN 1826; UNCLASSIFIED DRUG;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ARTICLE; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; IMMUNE RESPONSE; IMMUNITY; LEISHMANIA INFANTUM; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; TH1 TH2 BALANCE; TH17 CELL; VACCINATION; VISCERAL LEISHMANIASIS;

ADJUVANTS, IMMUNOLOGIC; ADOPTIVE TRANSFER; ANIMALS; ANTIBODIES, PROTOZOAN; CYTOKINES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; IMMUNOGLOBULIN G; LEISHMANIA INFANTUM; LEISHMANIASIS, VISCERAL; LIVER; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; OLIGODEOXYRIBONUCLEOTIDES; PROTOZOAN PROTEINS; RODENT DISEASES; SPLEEN;

EID: 79959687681     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.04.089     Document Type: Article

References (88)

1. Steinman R.M. The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 1991, 9(April):271-296.
2. Palucka K., Ueno H., Roberts L., Fay J., Banchereau J. Dendritic cells: are they clinically relevant?. Cancer J 2010, 16(July-August (4)):318-324.
3. Sabado R.L., Bhardwaj N. Directing dendritic cell immunotherapy towards successful cancer treatment. Immunotherapy 2010, 2(January (1)):37-56.
4. Fajardo-Moser M., Berzel S., Moll H. Mechanisms of dendritic cell-based vaccination against infection. Int J Med Microbiol 2008, 298(January (1-2)):11-20.
5. Moll H., Berberich C. Dendritic cell-based vaccination strategies: induction of protective immunity against leishmaniasis. Immunobiology 2001, 204(December (5)):659-666.
6. Postigo J.A. Leishmaniasis in the World Health Organization Eastern Mediterranean Region. Int J Antimicrob Agents 2010, 36(suppl. 1 (November)):S62-S65.
7. Encke J., Findeklee J., Geib J., Pfaff E., Stremmel W. Prophylactic and therapeutic vaccination with dendritic cells against hepatitis C virus infection. Clin Exp Immunol 2005, 142(November (2)):362-369.
8. Su H., Messer R., Whitmire W., Fischer E., Portis J.C., Caldwell H.D. Vaccination against chlamydial genital tract infection after immunization with dendritic cells pulsed ex vivo with nonviable Chlamydiae. J Exp Med 1998, 188(September (5)):809-818.
9. Worgall S., Kikuchi T., Singh R., Martushova K., Lande L., Crystal R.G. Protection against pulmonary infection with Pseudomonas aeruginosa following immunization with P. aeruginosa-pulsed dendritic cells. Infect Immun 2001, 69(July (7)):4521-4527.
10. World Health Organization [Internet]. Geneva, Switzerland, c2011. Available from: http://www.who.int/leishmaniasis/en/index.html.
11. Desjeux P. Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis 2004, 27(September (5)):305-318.
12. Herwaldt B.L. Leishmaniasis. Lancet 1999, 354(October (9185)):1191-1199.
13. Murray H.W. Clinical experimental advances in treatment of visceral leishmaniasis. Antimicrob Agents Chemother 2001, 45(August (8)):2185-2197.
14. Sundar S., Murray H.W. Availability of miltefosine for the treatment of kala-azar in India. Bull World Health Organ 2005, 83(May (5)):394-395.
15. Sundar S., More D.K., Singh M.K., Singh V.P., Sharma S., Makharia A., et al. Failure of pentavalent antimony in visceral leishmaniasis in India: report from the center of the Indian epidemic. Clin Infect Dis 2000, 31(October (4)):1104-1107.
16. Bittar R.C., Nogueira R.S., Vieira-Goncalves R., Pinho-Ribeiro V., Mattos M.S., Oliveira-Neto M.P., et al. T-cell responses associated with resistance to Leishmania infection in individuals from endemic areas for Leishmania (Viannia) braziliensis. Mem Inst Oswaldo Cruz 2007, 102(August (5)):625-630.
17. Reed S.G., Scott P. T-cell and cytokine responses in leishmaniasis. Curr Opin Immunol 1993, 5(August (4)):524-531.
18. Rogers K.A., DeKrey G.K., Mbow M.L., Gillespie R.D., Brodskyn C.I., Titus R.G. Type 1 and type 2 responses to Leishmania major. FEMS Microbiol Lett 2002, 209(March (1)):1-7.
19. Sacks D., Noben-Trauth N. The immunology of susceptibility and resistance to Leishmania major in mice. Nat Rev Immunol 2002, 2(November (11)):845-858.
20. Goto H., Lindoso J.A. Immunity and immunosuppression in experimental visceral leishmaniasis. Braz J Med Biol Res 2004, 37(April (4)):615-623.
21. Kaye P.M., Curry A.J., Blackwell J.M. Differential production of Th1- and Th2-derived cytokines does not determine the genetically controlled or vaccine-induced rate of cure in murine visceral leishmaniasis. J Immunol 1991, 146(April (8)):2763-2770.
22. Berberich C., Requena J.M., Alonso C. Cloning of genes and expression and antigenicity analysis of the Leishmania infantum KMP-11 protein. Exp Parasitol 1997, 85(January (1)):105-108.
23. Jardim A., Tolson D.L., Turco S.J., Pearson T.W., Olafson R.W. The Leishmania donovani lipophosphoglycan T lymphocyte-reactive component is a tightly associated protein complex. J Immunol 1991, 147(Novenber (10)):3538-3544.
24. Kurtzhals J.A., Hey A.S., Jardim A., Kemp M., Schaefer K.U., Odera E.O., et al. Dichotomy of the human T cell response to Leishmania antigens. II. Absent or Th2-like response to gp63 and Th1-like response to lipophosphoglycan-associated protein in cells from cured visceral leishmaniasis patients. Clin Exp Immunol 1994, 96(June (3)):416-421.
25. Russo D.M., Turco S.J., Burns J.M., Reed S.G. Stimulation of human T lymphocytes by Leishmania lipophosphoglycan-associated proteins. J Immunol 1992, 148(January (1)):202-207.
26. Todoli F., Solano-Gallego L., de Juan R., Morell P., Nunez Mdel C., Lasa R., et al. Humoral and in vivo cellular immunity against the raw insect-derived recombinant Leishmania infantum antigens KMPII, TRYP, LACK, and papLe22 in dogs from an endemic area. Am J Trop Med Hyg 2010, 83(December (6)):1287-1294.
27. Tolson D.L., Jardim A., Schnur L.F., Stebeck C., Tuckey C., Beecroft R.P., et al. The kinetoplastid membrane protein 11 of Leishmania donovani and African trypanosomes is a potent stimulator of T-lymphocyte proliferation. Infect Immun 1994, 62(November (11)):4893-4899.
28. Stebeck C.E., Beecroft R.P., Singh B.N., Jardim A., Olafson R.W., Tuckey C., et al. Kinetoplastid membrane protein-11 (KMP-11) is differentially expressed during the life cycle of African trypanosomes and is found in a wide variety of kinetoplastid parasites. Mol Biochem Parasitol 1995, 71(April (1)):1-13.
29. Berberich C., Machado G., Morales G., Carrillo G., Jimenez-Ruiz A., Alonso C. The expression of the Leishmania infantum KMP-11 protein is developmentally regulated and stage specific. Biochim Biophys Acta 1998, 1442(November (2-3)):230-237.
30. Jardim A., Funk V., Caprioli R.M., Olafson R.W. Isolation and structural characterization of the Leishmania donovani kinetoplastid membrane protein-11, a major immunoreactive membrane glycoprotein. Biochem J 1995, 305(January (Pt 1)):307-313.
31. Jardim A., Hanson S., Ullman B., McCubbin W.D., Kay C.M., Olafson R.W. Cloning and structure-function analysis of the Leishmania donovani kinetoplastid membrane protein-11. Biochem J 1995, 305(January (Pt 1)):315-320.
32. Matos D.C., Faccioli L.A., Cysne-Finkelstein L., Luca P.M., Corte-Real S., Armoa G.R., et al. Kinetoplastid membrane protein-11 is present in promastigotes and amastigotes of Leishmania amazonensis and its surface expression increases during metacyclogenesis. Mem Inst Oswaldo Cruz 2010, 105(May (3)):341-347.
33. Basu R., Bhaumik S., Basu J.M., Naskar K., De T., Roy S. Kinetoplastid membrane protein-11 DNA vaccination induces complete protection against both pentavalent antimonial-sensitive and -resistant strains of Leishmania donovani that correlates with inducible nitric oxide synthase activity and IL-4 generation: evidence for mixed Th1- and Th2-like responses in visceral leishmaniasis. J Immunol 2005, 174(June (11)):7160-7171.
34. Basu R., Bhaumik S., Haldar A.K., Naskar K., De T., Dana S.K., et al. Hybrid cell vaccination resolves Leishmania donovani infection by eliciting a strong CD8+cytotoxic T-lymphocyte response with concomitant suppression of interleukin-10 (IL-10) but not IL-4 or IL-13. Infect Immun 2007, 75(December (12)):5956-5966.
35. Mukhopadhyay S., Sen P., Bhattacharyya S., Majumdar S., Roy S. Immunoprophylaxis and immunotherapy against experimental visceral leishmaniasis. Vaccine 1999, 17(January (3)):291-300.
36. Basu R., Roy S., Walden P. HLA class I-restricted T cell epitopes of the kinetoplastid membrane protein-11 presented by Leishmania donovani-infected human macrophages. J Infect Dis 2007, 195(May (9)):1373-1380.
37. Delgado G., Parra-Lopez C.A., Vargas L.E., Hoya R., Estupinan M., Guzman F., et al. Characterizing cellular immune response to kinetoplastid membrane protein-11 (KMP-11) during Leishmania (Viannia) panamensis infection using dendritic cells (DCs) as antigen presenting cells (APCs). Parasite Immunol 2003, 25(April (4)):199-209.
38. Jensen A.T., Gasim S., Ismail A., Gaafar A., Kurtzhals J.A., Kemp M., et al. Humoral and cellular immune responses to synthetic peptides of the Leishmania donovani kinetoplastid membrane protein-11. Scand J Immunol 1998, 48(July (1)):103-109.
39. Klinman D.M., Yi A.K., Beaucage S.L., Conover J., Krieg A.M. CpG motifs present in bacteria DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon gamma. Proc Natl Acad Sci USA 1996, 93(April (7)):2879-2883.
40. Roman M., Martin-Orozco E., Goodman J.S., Nguyen M.D., Sato Y., Ronaghy A., et al. Immunostimulatory DNA sequences function as T helper-1-promoting adjuvants. Nat Med 1997, 3(August (8)):849-854.
41. Sparwasser T., Vabulas R.M., Villmow B., Lipford G.B., Wagner H., Bacterial CpG-DNA activates dendritic cells in vivo: T helper cell-independent cytotoxic T cell responses to soluble proteins. Eur J Immunol 2000, 30(December (12)):3591-3597.
42. Hartmann G., Weiner G.J., Krieg A.M. CpG DNA: a potent signal for growth, activation, and maturation of human dendritic cells. Proc Natl Acad Sci USA 1999, 96(August (16)):9305-9310.
43. Stacey K.J., Blackwell J.M., Immunostimulatory DNA as an adjuvant in vaccination against Leishmania major. Infect Immun 1999, 67(August (8)):3719-3726.
44. Wu W., Huang L., Mendez S. A live Leishmania major vaccine containing CpG motifs induces the de novo generation of Th17 cells in C57BL/6 mice. Eur J Immunol 2010, 40(September (9)):2517-2527.
45. Wu W., Weigand L., Belkaid Y., Mendez S. Immunomodulatory effects associated with a live vaccine against Leishmania major containing CpG oligodeoxynucleotides. Eur J Immunol 2006, 36(December (12)):3238-3247.
46. Carrion J., Nieto A., Soto M., Alonso C. Adoptive transfer of dendritic cells pulsed with Leishmania infantum nucleosomal histones confers protection against cutaneous leishmaniosis in BALB/c mice. Microbes Infect 2007, 9(May (6)):735-743.
47. Ramirez-Pineda J.R., Frohlich A., Berberich C., Moll H. Dendritic cells (DC) activated by CpG DNA ex vivo are potent inducers of host resistance to an intracellular pathogen that is independent of IL-12 derived from the immunizing DC. J Immunol 2004, 172(May (10)):6281-6289.
48. Tsagozis P., Karagouni E., Dotsika E. Function of CD8+T lymphocytes in a self-curing mouse model of visceral leishmaniasis. Parasitol Int 2005, 54(June (2)):139-146.
49. Papadopoulou G., Karagouni E., Dotsika E. ISCOMs vaccine against experimental leishmaniasis. Vaccine 1998, 16(May-June (9-10)):885-892.
50. Lutz M.B., Kukutsch N., Ogilvie A.L., Rossner S., Koch F., Romani N., et al. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 1999, 223(February (1)):77-92.
51. Tsagozis P., Karagouni E., Dotsika E. Dendritic cells pulsed with peptides of gp63 induce differential protection against experimental cutaneous leishmaniasis. Int J Immunopathol Pharmacol 2004, 17(September-December (3)):343-352.
52. Carrion J., Nieto A., Iborra S., Iniesta V., Soto M., Folgueira C., et al. Immunohistological features of visceral leishmaniasis in BALB/c mice. Parasite Immunol 2006, 28(May (5)):173-183.
53. Santambrogio L., Sato A.K., Fischer F.R., Dorf M.E., Stern L.J. Abundant empty class II MHC molecules on the surface of immature dendritic cells. Proc Natl Acad Sci USA 1999, 96(December (26)):15050-15055.
54. Santambrogio L., Sato A.K., Carven G.J., Belyanskaya S.L., Strominger J.L., Stern L.J. Extracellular antigen processing and presentation by immature dendritic cells. Proc Natl Acad Sci USA 1999, 96(December (26)):15056-15061.
55. Seder R.A., Gazzinelli R., Sher A., Paul W.E. Interleukin 12 acts directly on CD4+ T cells to enhance priming for interferon gamma production and diminishes interleukin 4 inhibition of such priming. Proc Natl Acad Sci USA 1993, 90(November (21)):10188-10192.
56. Askew D., Chu R.S., Krieg A.M., Harding C.V. CpG DNA induces maturation of dendritic cells with distinct effects on nascent and recycling MHC-II antigen-processing mechanisms. J Immunol 2000, 165(December (12)):6889-6895.
57. Stober C.B., Lange U.G., Roberts M.T., Alcami A., Blackwell J.M. IL-10 from regulatory T cells determines vaccine efficacy in murine Leishmania major infection. J Immunol 2005, 175(August (4)):2517-2524.
58. Zhang X., Munegowda M.A., Yuan J., Wei Y., Xiang J. Optimal TLR9 signal converts tolerogenic CD4-8- DCs into immunogenic ones capable of stimulating antitumor immunity via activating CD4+ Th1/Th17 and NK cell responses. J Leukoc Biol 2010, 88(August (2)):393-403.
59. Korn T., Bettelli E., Oukka M., Kuchroo V.K. IL-17 and Th17 Cells. Annu Rev Immunol 2009, 27:485-517.
60. Ouyang W., Kolls J.K., Zheng Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 2008, 28(April (4)):454-467.
61. Smith K.M., Pottage L., Thomas E.R., Leishman A.J., Doig T.N., Xu D., et al. Th1 and Th2 CD4+ T cells provide help for B cell clonal expansion and antibody synthesis in a similar manner in vivo. J Immunol 2000, 165(September (6)):3136-3144.
62. Snapper C.M., Paul W.E., Interferon-gamma B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science 1987, 236(May (4804)):944-947.
63. Mitsdoerffer M., Lee Y., Jager A., Kim H.J., Korn T., Kolls J.K., et al. Proinflammatory T helper type 17 cells are effective B-cell helpers. Proc Natl Acad Sci USA 2010, 107(August(32)):14292-14297.
64. Ozaki K., Spolski R., Ettinger R., Kim H.P., Wang G., Qi C.F., et al. Regulation of B cell differentiation and plasma cell generation by IL-21, a novel inducer of Blimp-1 and Bcl-6. J Immunol 2004, 173(November (9)):5361-5371.
65. Ozaki K., Spolski R., Feng C.G., Qi C.F., Cheng J., Sher A., et al. A critical role for IL-21 in regulating immunoglobulin production. Science 2002, 298(November (5598)):1630-1634.
66. Kuchen S., Robbins R., Sims G.P., Sheng C., Phillips T.M., Lipsky P.E., et al. Essential role of IL-21 in B cell activation, expansion, and plasma cell generation during CD4+ T cell-B cell collaboration. J Immunol 2007, 179(November (9)):5886-5896.
67. Rolao N., Cortes S., Gomes-Pereira S., Campino L. Leishmania infantum: mixed T-helper-1/T-helper-2 immune response in experimentally infected BALB/c mice. Exp Parasitol 2007, 115(March (3)):270-276.
68. Heinzel F.P., Schoenhaut D.S., Rerko R.M., Rosser L.E., Gately M.K. Recombinant interleukin 12 cures mice infected with Leishmania major. J Exp Med 1993, 177(May (5)):1505-1509.
69. Rhalem A., Sahibi H., Guessous-Idrissi N., Lasri S., Natami A., Riyad M., et al. Immune response against Leishmania antigens in dogs naturally and experimentally infected with Leishmania infantum. Vet Parasitol 1999, 81(March (3)):173-184.
70. Saha S., Mondal S., Ravindran R., Bhowmick S., Modak D., Mallick S., et al. IL-10- and TGF-beta-mediated susceptibility in kala-azar and post-kala-azar dermal leishmaniasis: the significance of amphotericin B in the control of Leishmania donovani infection in India. J Immunol 2007, 179(October (8)):5592-5603.
71. Hailu A., van der Poll T., Berhe N., Kager P.A. Elevated plasma levels of interferon (IFN)-gamma, IFN-gamma inducing cytokines, and IFN-gamma inducible CXC chemokines in visceral leishmaniasis. Am J Trop Med Hyg 2004, 71(November (5)):561-567.
72. Kemp K., Kemp M., Kharazmi A., Ismail A., Kurtzhals J.A., Hviid L., et al. Leishmania-specific T cells expressing interferon-gamma (IFN-gamma) and IL-10 upon activation are expanded in individuals cured of visceral leishmaniasis. Clin Exp Immunol 1999, 116(June (3)):500-504.
73. Ding A.H., Nathan C.F., Stuehr D.J. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J Immunol 1988, 141(October (7)):2407-2412.
74. Murphy M.L., Cotterell S.E., Gorak P.M., Engwerda C.R., Kaye P.M. Blockade of CTLA-4 enhances host resistance to the intracellular pathogen. Leishmania donovani. J Immunol 1998, 161(October (8)):4153-4160.
75. Karp C.L., el-Safi S.H., Wynn T.A., Satti M.M., Kordofani A.M., Hashim F.A., et al. In vivo cytokine profiles in patients with kala-azar. Marked elevation of both interleukin-10 and interferon-gamma. J Clin Invest 1993, 91(April (4)):1644-1648.
76. Bodas M., Jain N., Awasthi A., Martin S., Penke Loka R.K., Dandekar D., et al. Inhibition of IL-2 induced IL-10 production as a principle of phase-specific immunotherapy. J Immunol 2006, 177(October (7)):4636-4643.
77. Nishikawa H., Kato T., Tawara I., Ikeda H., Kuribayashi K., Allen P.M., et al. IFN-gamma controls the generation/activation of CD4+ CD25+ regulatory T cells in antitumor immune response. J Immunol 2005, 175(October (7)):4433-4440.
78. Banerjee A., De M., Ali N. Combination therapy with Paromomycin associated Stearylamine-bearing liposomes cures experimental visceral leishmaniasis through Th1-biased immunomodulation. Antimicrob Agents Chemother 2011, 55(April (4)):1161-1170.
79. Murray H.W., Flanders K.C., Donaldson D.D., Sypek J.P., Gotwals P.J., Liu J., et al. Antagonizing deactivating cytokines to enhance host defense and chemotherapy in experimental visceral leishmaniasis. Infect Immun 2005, 73(July (7)):3903-3911.
80. Rodrigues O.R., Marques C., Soares-Clemente M., Ferronha M.H., Santos-Gomes G.M. Identification of regulatory T cells during experimental Leishmania infantum infection. Immunobiology 2009, 214(2):101-111.
81. Cua D.J., Tato C.M. Innate IL-17-producing cells: the sentinels of the immune system. Nat Rev Immunol 2010, 10(July(7)):479-489.
82. Lopez Kostka S., Dinges S., Griewank K., Iwakura Y., Udey M.C., von Stebut E. IL-17 promotes progression of cutaneous leishmaniasis in susceptible mice. J Immunol 2009, 182(March (5)):3039-3046.
83. Vargas-Inchaustegui D.A., Xin L., Soong L. Leishmania braziliensis infection induces dendritic cell activation, ISG15 transcription, and the generation of protective immune responses. J Immunol 2008, 180(June (11)):7537-7545.
84. Xin L., Li Y., Soong L. Role of interleukin-1beta in activating the CD11c(high) CD45RB- dendritic cell subset and priming Leishmania amazonensis-specific CD4+ T cells in vitro and in vivo. Infect Immun 2007, 75(October (10)):5018-5026.
85. Castilho T.M., Goldsmith-Pestana K., Lozano C., Valderrama L., Saravia N.G., McMahon-Pratt D. Murine model of chronic L. (Viannia) panamensis infection: role of IL-13 in disease. Eur J Immunol 2010, 40(October(10)):2816-2829.
86. Pitta M.G., Romano A., Cabantous S., Henri S., Hammad A., Kouriba B., et al. IL-17 and IL-22 are associated with protection against human kala azar caused by Leishmania donovani. J Clin Invest 2009, 119(August (8)):2379-2387.
87. Novoa R., Bacellar O., Nascimento M., Cardoso T.M., Ramasawmy R., Oliveira W.N., et al. IL-17 and Regulatory Cytokines (IL-10 and IL-27) in L. braziliensis Infection. Parasite Immunol 2011, 33(February(2)):132-136.
88. Boaventura V.S., Santos C.S., Cardoso C.R., de Andrade J., Dos Santos W.L., Clarencio J., et al. Human mucosal leishmaniasis: neutrophils infiltrate areas of tissue damage that express high levels of Th17-related cytokines. Eur J Immunol 2010, 40(October(10)):2830-2836.