Immunization with the DNA-encoding N-terminal domain of proteophosphoglycan of Leishmania donovani generates Th1-type immunoprotective response against experimental visceral leishmaniasis

Journal of Immunology

Volumn 183, Issue 1, 2009, Pages 470-479

  Samant, Mukesh ^a   Gupta, Reema ^a   Kumari, Shraddha ^a   Misra, Pragya ^a   Khare, Prashant ^a   Kushawaha, Pramod Kumar ^a   Sahasrabuddhe, Amogh Anant ^a   Dube, Anuradha ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; DNA; DNA VACCINE; GAMMA INTERFERON; IMMUNOGLOBULIN G2; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 4; MESSENGER RNA; PCDNA3 VACCINE; PROTEOPHOSPHOGLYCAN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; LEISHMANIA VACCINE; MEMBRANE PROTEIN; PEPTIDE FRAGMENT; PPG1 PROTEIN, LEISHMANIA; PROTEOGLYCAN; PROTOZOAL DNA; PROTOZOAL PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; GENE FUNCTION; GENE STRUCTURE; IMMUNE RESPONSE; IMMUNIZATION; LEISHMANIA DONOVANI; MAMMAL CELL; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROKARYOTE; PROTEIN DOMAIN; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL RATE; SYRIAN HAMSTER; TH1 CELL; VISCERAL LEISHMANIASIS; ANIMAL; CELL LINE; CELL POLARITY; CHEMISTRY; ESCHERICHIA COLI; GENETICS; HAMSTER; HUMAN; IMMUNOLOGY; MALE; METABOLISM; PARASITOLOGY; PROTEIN TERTIARY STRUCTURE;

ANIMALS; CELL LINE; CELL POLARITY; CRICETINAE; DNA, PROTOZOAN; ESCHERICHIA COLI; HUMANS; LEISHMANIA DONOVANI; LEISHMANIASIS VACCINES; LEISHMANIASIS, VISCERAL; MALE; MEMBRANE PROTEINS; MESOCRICETUS; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, TERTIARY; PROTEOGLYCANS; PROTOZOAN PROTEINS; TH1 CELLS; VACCINES, DNA;

EID: 68949108180     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900265     Document Type: Article

References (75)

1. Foth, B., A. Piani, J. M. Curtis, T. Ilg, M. McConville, and E. Handman. 2002. Leishmania major proteophosphoglycans exist as membrane-bound and soluble forms and localise to the cell membrane, the flagellar pocket and the lysosome. Int. J. Parasitol. 32: 1701-1708.
2. Mengeling, B. J., D. Zilberstein, and S. J. Turco. 1997. Biosynthesis of Leishmania lipophosphoglycan: solubilization and partial characterization of the initiating mannosylphosphoryltransferase. Glycobiology 7: 847-853.
3. Ilg, T., E. Handman, and Y. D. Stierhof. 1999. Proteophosphoglycans from Leishmania promastigotes and amastigotes. Biochem. Soc. Trans. 27: 518-525.
4. Ilg, T., D. Craik, G. Currie, G. Multhaup, and A. Bacic. 1998. Stage-specific proteophosphoglycan from Leishmania mexicana amastigotes: structural characterization of novel mono-, di-, and triphosphorylated phosphodiester-linked oligosaccharides. J. Biol. Chem. 273: 13509-13523.
5. Piani, A., T. Ilg, A. G. Elefanty, J. Curtis, and E. Handman. 1999. Leishmania major proteophosphoglycan is expressed by amastigotes and has an immunomodulatory effect on macrophage function. Microbes Infect. 1: 589-599.
6. Stierhof, Y. D., M. Wiese, T. Ilg, P. Overath, M. Haner, and U. Aebi. 1998. Structure of a filamentous phosphoglycoprotein polymer: the secreted acid phosphatase of Leishmania mexicana. J. Mol. Biol. 282: 137-148.
7. Ilg, T., E. Handman, K. Ng, Y. D. Stierhof, and A. Bacic. 1999. Mucin-like proteophosphoglycans from the protozoan parasite Leishmania. Trends Glycosci. Glycotechnol. 11: 53-71. (Pubitemid 129634019)
8. Ilg, T., Y. D. Stierhof, M. J. McConville, and P. Overath. 1995. Purification, partial characterization and immunolocalization of a proteophosphoglycan secreted by Leishmania mexicana amastigotes. Eur. J. Cell Biol. 66: 205-215.
9. Gopfert, U., N. Goehring, C. Klein, and T. Ilg. 1999. Proteophosphoglycans of Leishmania mexicana: molecular cloning and characterization of the Leishmania mexicana ppg2 gene encoding the proteophosphoglycans aPPG and pPPG2 that are secreted by amastigotes and promastigotes. Biochem. J. 344: 787-795.
10. Klein, C., U. Gopfert, N. Goehring, Y. D. Stierhof, and T. Ilg. 1999. Proteophosphoglycans of Leishmania mexicana: identification, purification, structural and ultrastructural characterization of the secreted promastigote proteophosphoglycan pPPG2, a stage-specific glycoisoform of amastigote aPPG. Biochem. J. 344: 775-786.
11. Samant, M., A. A. Sahasrabuddhe, N. Singh, S. K. Gupta, S. Sundar, and A. Dube. 2007. Proteophosphoglycan is differentially expressed in sodium stibogluconate-sensitive and resistant Indian clinical isolates of Leishmania donovani. Parasitology 134: 1175-1184.
12. Turco, S. J., and A. Descoteaux. 1992. The lipophosphoglycan of Leishmania parasites. Annu. Rev. Microbiol. 46: 65-94.
13. Ng, K., E. Handman, and A. Bacic. 1994. Biosynthesis of lipophosphoglycan from Leishmania major: characterization of (β1-3)-galactosyltransferase(s) . Glycobiology 4: 845-853.
14. Ng, K., E. Handman, and A. Bacic. 1996. Biosynthesis of lipophosphoglycan from Leishmania major: solubilization and characterization of a (β1-3)-galactosyltransferase. Biochem. J. 317: 247-255. (Pubitemid 26238353)
15. Brown, G. M., A. R. Millar, C. Masterson, J. S. Brimacombe, A. V. Nikolaev, and M. A. Ferguson. 1996. Synthetic phospho-oligosaccharide fragments of lipophosphoglycan as acceptors for Leishmania major α-D- mannosylphosphate transferase. Eur. J. Biochem. 242: 410-416.
16. Ma, D., D. G. Russell, S. M. Beverley, and S. J. Turco. 1997. Golgi GDP-mannose uptake requires Leishmania LPG2: a member of a eukaryotic family of putative nucleotide-sugar transporters. J. Biol. Chem. 272: 3799-3805.
17. Ilg, T., J. Montgomery, Y. D. Stierhof, and E. Handman. 1999. Molecular cloning and characterization of a novel repeat-containing Leishmania major gene, ppg1, that encodes a membrane-associated form of proteophosphoglycan with a putative glycosylphosphatidylinositol anchor. J. Biol. Chem. 274: 31410-31420. (Pubitemid 129501595)
18. Montgomery, J., T. Ilg, J. K. Thompson, B. Kobe, and E. Handman. 2000. Identification and predicted structure of a leucine-rich repeat motif shared by Leishmania major proteophosphoglycan and parasite surface antigen 2. Mol. Biochem. Parasitol. 107: 289-295.
19. Ivens, A. C., C. S. Peacock, E. A. Worthey, L. Murphy, G. Aggarwal, M. Berriman, E. Sisk, M. A. Rajandream, E. Adlem, R. Aert, et al. 2005. The genome of the kinetoplastid parasite, Leishmania major. Science 309: 436-442.
20. Kolaskar, A. S., and P. C. Tongaonkar. 1990. A semi-empirical method for prediction of antigenic determinants on protein antigens. FEBS Lett. 276: 172-174.
21. Carvalho, E. M., R. S. Teixeira, and W. D. Johnson, Jr. 1981. Cell-mediated immunity in American visceral leishmaniasis: reversible immunosuppression during acute infection. Infect. Immun. 33: 498-500.
22. Carvalho, E. M., R. Badaro, S. G. Reed, T. C. Jones, and W. D. Johnson, Jr. 1985. Absence of γ interferon and interleukin 2 production during active visceral leishmaniasis. J. Clin. Invest. 76: 2066-2069.
23. Kaye, P. M., A. J. Curry, and J. M. Blackwell. 1991. 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. 146: 2763-2770.
24. Kemp, K., M. Kemp, A. Kharazmi, A. Ismail, J. A. Kurtzhals, L. Hviid, and T. G. Theander. 1999. Leishmania-specific T cells expressing interferon-γ (IFN-γ) and IL-10 upon activation are expanded in individuals cured of visceral leishmaniasis. Clin. Exp. Immunol. 116: 500-504.
25. Kemp, K. 2000. Cytokine-producing T cell subsets in human leishmaniasis. Arch. Immunol. Ther. Exp. 48: 173-176.
26. Kafetzis, D. A., and H. C. Maltezou. 2002. Visceral leishmaniasis in paediatrics. Curr. Opin. Infect. Dis. 15: 289-294.
27. Murray, H. W. 2001. Clinical and experimental advances in treatment of visceral leishmaniasis. Antimicrob. Agents Chemother. 45: 2185-2197.
28. Melby, P. C., V. V. Tryon, B. Chandrasekar, and G. L. Freeman. 1998. Cloning of Syrian hamster (Mesocricetus auratus) cytokine cDNAs and analysis of cytokine mRNA expression in experimental visceral leishmaniasis. Infect. Immun. 66: 2135-2142.
29. Garg, R., J. K. Srivastava, A. Pal, S. Naik, and A. Dube. 2005. Isolation of integral membrane proteins of Leishmania promastigotes and evaluation of their prophylactic potential in hamsters against experimental visceral leishmaniasis. Vaccine 23: 1189-1196.
30. Garg, R., S. K. Gupta, P. Tripathi, S. Naik, S. Sundar, and A. Dube. 2005. Immunostimulatory cellular responses of cured Leishmania-infected patients and hamsters against the integral membrane proteins and non-membranous soluble proteins of a recent clinical isolate of Leishmania donovani. Clin. Exp. Immunol. 140: 149-156.
31. Dube, A., P. Sharma, J. K. Srivastava, A. Misra, S. Naik, and J. C. Katiyar. 1998. Vaccination of langur monkeys (Presbytis entellus) against Leishmania donovani with autoclaved L. major plus BCG. Parasitology 116: 219-221.
32. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
33. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76: 4350-4354. (Pubitemid 9256559)
34. Tripp, C. A., W. A. Wisdom, P. J. Myler, and K. D. Stuart. 1992. A multicopy, extrachromosomal DNA in Leishmania infantum contains two inverted repeats of the 27.5-kilobase LD1 sequence and encodes numerous transcripts. Mol. Biochem. Parasitol. 55: 39-50.
35. Myler, P. J., G. M. Venkataraman, M. J. Lodes, and K. D. Stuart. 1994. A frequently amplified region in Leishmania contains a gene conserved in prokaryotes and eukaryotes. Gene 148: 187-193.
36. Scott, D. A., G. H. Coombs, and B. E. Sanderson. 1987. Effects of methotrexate and other antifolates on the growth and dihydrofolate reductase activity of Leishmania promastigotes. Biochem. Pharmacol. 36: 2043-2045.
37. Choudhry, A., P. Y. Guru, R. P. Saxena, A. Tandon, and K. C. Saxena. 1990. Enzyme-linked immunosorbent assay in the diagnosis of kala-azar in Bhadohi (Varanasi), India. Trans. R. Soc. Trop. Med. Hyg. 84: 363-366.
38. Bhowmick, S., R. Ravindran, and N. Ali. 2007. Leishmanial antigens in liposomes promote protective immunity and provide immunotherapy against visceral leishmaniasis via polarized Th1 response. Vaccine 25: 6544-6556.
39. Scharton-Kersten, T., and P. Scott. 1995. The role of the innate immune response in Th1 cell development following Leishmania major infection. J. Leukocyte Biol. 57: 515-522.
40. Ding, A. H., C. F. Nathan, and D. J. Stuehr. 1988. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages: comparison of activating cytokines and evidence for independent production. J. Immunol. 141: 2407-2412.
41. Voller, A., D. E. Bidwell, and A. Bartlett. 1979. The Enzyme Linked Immunosorbent Assay (ELISA): A Guide with Abstracts of Microplate Application. Guernsey Ci, U.K., Fileroline Press, pp. 1-25.
42. Melby, P. C., B. Chandrasekar, W. Zhao, and J. E. Coe. 2001. The hamster as a model of human visceral leishmaniasis: progressive disease and impaired generation of nitric oxide in the face of a prominent Th1-like cytokine response. J. Immunol. 166: 1912-1920.
43. Rama Iniguez, S., M. A. Dea-Ayuela, J. A. Sanchez-Brunete, J. J. Torrado, J. M. Alunda, and F. Bolas-Fernandez. 2006. Real-time reverse transcription-PCR quantification of cytokine mRNA expression in golden Syrian hamster infected with Leishmania infantum and treated with a new amphotericin B formulation. Antimicrob. Agents Chemother. 50: 1195-1201.
44. Haldar, J. P., S. Ghose, K. C. Saha, and A. C. Ghose. 1983. Cell-mediated immune response in Indian kala-azar and post-kala-azar dermal leishmaniasis. Infect. Immun. 42: 702-707.
45. Gifawesen, C., and J. P. Farrell. 1989. Comparison of T-cell responses in self-limiting versus progressive visceral Leishmania donovani infections in golden hamsters. Infect. Immun. 57: 3091-3096.
46. Xu, D., and F. Y. Liew. 1994. Genetic vaccination against leishmaniasis. Vaccine 12: 1534-1536.
47. Rodríguez-Cortés, A., A. Ojeda, L. López-Fuertes, M. Timón, L. Altet, L. Solano-Gallego, E. Sánchez-Robert, O. Francino, and J. Alberola. 2007. Vaccination with plasmid DNA encoding KMPII, TRYP, LACK and GP63 does not protect dogs against Leishmania infantum experimental challenge. Vaccine 25: 7962-7971.
48. Aguilar-Be, I., R. da Silva Zardo, E. Paraguai de Souza, G. P. Borja-Cabrera, M. Rosado-Vallado, M. Mut-Martin, R. Garcia-Miss Mdel, C. B. Palatnik de Sousa, and E. Dumonteil. 2005. Cross-protective efficacy of a prophylactic Leishmania donovani DNA vaccine against visceral and cutaneous murine leishmaniasis. Infect. Immun. 73: 812-819.
49. Palatnik-de-Sousa, C. B. 2008. Vaccines for leishmaniasis in the fore coming 25 years. Vaccine 26: 1709-1724.
50. Fragaki, K., I. Suffia, B. Ferrua, D. Rousseau, Y. Le Fichoux, and J. Kubar. 2001. Immunisation with DNA encoding Leishmania infantum protein papLe22 decreases the frequency of parasitemic episodes in infected hamsters. Vaccine 19: 1701-1709.
51. LACK DNA vaccine is highly immunogenic but not protective against experimental visceral leishmaniasis. Infect. Immun. 69: 4719-4725.
52. Sukumaran, B., P. Tewary, S. Saxena, and R. Madhubala. 2003. Vaccination with DNA encoding ORFF antigen confers protective immunity in mice infected with Leishmania donovani. Vaccine 21: 1292-1299.
53. Basu, R., S. Bhaumik, J. M. Basu, K. Naskar, T. De, and S. Roy. 2005. 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. 174: 7160-7171.
54. Rafati, S., A. Nakhaee, T. Taheri, Y. Taslimi, H. Darabi, D. Eravani, S. Sanos, P. Kaye, M. Taghikhani, S. Jamshidi, and M. A. Rad. 2005. Protective vaccination against experimental canine visceral leishmaniasis using a combination of DNA and protein immunization with cysteine proteinases type I and II of L. infantum. Vaccine 23: 3716-3725.
55. Ramiro, M. J., J. J. Zarate, T. Hanke, D. Rodriguez, J. R. Rodriguez, M. Esteban, J. Lucientes, J. A. Castillo, and V. Larraga. 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.
56. Gonzalo, R. M., G. del Real, J. R. Rodriguez, D. Rodriguez, R. Heljasvaara, P. Lucas, V. Larraga, and M. Esteban. 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.
57. Ghosh, A., S. Labrecque, and G. Matlashewski. 2001. Protection against Leishmania donovani infection by DNA vaccination: increased DNA vaccination efficiency through inhibiting the cellular p53 response. Vaccine 19: 3169-3178.
58. Ali, N., and F. Afrin. 1997. Protection of mice against visceral leishmaniasis by immunization with promastigote antigen incorporated in liposomes. J. Parasitol. 83: 70-75.
59. Afrin, F., R. Rajesh, K. Anam, M. Gopinath, S. Pal, and N. Ali. 2002. Characterization of Leishmania donovani antigens encapsulated in liposomes that induce protective immunity in BALB/c mice. Infect. Immun. 70: 6697-6706.
60. Melby, P. C., Y. Z. Yang, J. Cheng, and W. Zhao. 1998. Regional differences in the cellular immune response to experimental cutaneous or visceral infection with Leishmania donovani. Infect. Immun. 66: 18-27.
61. Armijos, R. X., M. M. Weigel, M. Calvopina, A. Hidalgo, W. Cevallos, and J. Correa. 2004. Safety, immunogenecity, and efficacy of an autoclaved Leishmania amazonensis vaccine plus BCG adjuvant against New World cutaneous leishmaniasis. Vaccine 22: 1320-1326.
62. Scott, P., E. Pearce, S. Heath, and A. Sher. 1987. Identification of T-cell-reactive antigens that protect BALB/c mice against Leishmania major. Ann. Inst. Pasteur Immunol. 138: 771-774. (Pubitemid 18002407)
63. Howard, J. G., and F. Y. Liew. 1984. Mechanisms of acquired immunity in leishmaniasis. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 307: 87-98.
64. Ghose, A. C., J. P. Haldar, S. C. Pal, B. P. Mishra, and K. K. Mishra. 1980. Serological investigations on Indian kala-azar. Clin. Exp. Immunol. 40: 318-326.
65. Kumari, S., M. Samant, P. Khare, P. Misra, S. Dutta, B. K. Kolli, S. Sharma, K. P. Chang, and A. Dube. 2009. Photodynamic vaccination of hamsters with inducible suicidal mutants of Leishmania amazonensis elicits immunity against visceral leishmaniasis. Eur. J. Immunol. 39: 178-191.
66. Bretscher, P. A., O. Ogunremi, and J. N. Menon. 1997. Distinct immunological states in murine cutaneous leishmaniasis by immunising with different amounts of antigen: the generation of beneficial, potentially harmful, harmful and potentially extremely harmful states. Behring Inst. Mitt. 98: 153-159.
67. Kemp, M., J. A. Kurtzhals, K. Bendtzen, L. K. Poulsen, M. B. Hansen, D. K. Koech, A. Kharazmi, and T. G. Theander. 1993. Leishmania donovani-reactive Th1- and Th2-like T-cell clones from individuals who have recovered from visceral leishmaniasis. Infect. Immun. 61: 1069-1073.
68. Liew, F. Y., Y. Li, and S. Millott. 1990. Tumor necrosis factor-α synergizes with IFN-γ in mediating killing of Leishmania major through the induction of nitric oxide. J. Immunol. 145: 4306-4310.
69. Liew, F. Y., Y. Li, and S. Millott. 1990. Tumour necrosis factor (TNF-α) in leishmaniasis: II. TNF-α-induced macrophage leishmanicidal activity is mediated by nitric oxide from L-arginine. Immunology 71: 556-559.
70. Ghalib, H. W., M. R. Piuvezam, Y. A. Skeiky, M. Siddig, F. A. Hashim, A. M. el-Hassan, D. M. Russo, and S. G. Reed. 1993. Interleukin 10 production correlates with pathology in human Leishmania donovani infections. J. Clin. Invest. 92: 324-329.
71. Noben-Trauth, N., R. Lira, H. Nagase, W. E. Paul, and D. L. Sacks. 2003. The relative contribution of IL-4 receptor signaling and IL-10 to susceptibility to Leishmania major. J. Immunol. 170: 5152-5158.
72. Karp, C. L., S. H. el-Safi, T. A. Wynn, M. M. Satti, A. M. Kordofani, F. A. Hashim, M. Hag-Ali, F. A. Neva, T. B. Nutman, and D. L. Sacks. 1993. In vivo cytokine profiles in patients with kala-azar: marked elevation of both interleukin-10 and interferon-γ. J. Clin. Invest. 91: 1644-1648.
73. Murray, H. W., C. Montelibano, R. Peterson, and J. P. Sypek. 2000. Interleukin-12 regulates the response to chemotherapy in experimental visceral leishmaniasis. J. Infect. Dis. 182: 1497-1502.
74. Rodrigues Junior, V., J. S. Da Silva, and A. Campos-Neto. 1992. Selective inability of spleen antigen presenting cells from Leishmania donovani infected hamsters to mediate specific T cell proliferation to parasite antigens. Parasite Immunol. 14: 49-58.
75. Montgomery, J., J. Curtis, and E. Handman. 2002. Genetic and structural heterogeneity of proteophosphoglycans in Leishmania. Mol. Biochem. Parasitol. 121: 75-85.