Adaptive immunity against leishmania nucleoside hydrolase maps its C-terminal domain as the target of the CD4+ T cell-driven protective response

PLoS Neglected Tropical Diseases

Volumn 4, Issue 11, 2010, Pages

  Nico, Dirlei ^a   Claser, Carla ^b,d   Borja Cabrera, Gulnara P ^a   Travassos, Luiz R ^b   Palatnik, Marcos ^a   Soares, Irene da Silva ^c   Rodrigues, Martins Mauricio ^b   de Palatnik Sousa, Clarisa B ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d AGENCY FOR SCIENCE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GAMMA INTERFERON; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN M ANTIBODY; INTERLEUKIN 10; LEISHMANIA VACCINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MONOCLONAL ANTIBODY; NH36 PROTEIN; NUCLEOSIDASE; PROTOZOAL PROTEIN; RECOMBINANT PROTEIN; SAPONIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; GLYCOSIDASE;

ADAPTIVE IMMUNITY; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; CARBOXY TERMINAL SEQUENCE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG TARGETING; FEMALE; FOOT PAD; GENE MAPPING; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; IN VIVO STUDY; LEISHMANIA CHAGASI; LEISHMANIA DONOVANI; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; LYMPHOCYTOPOIESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE VIRULENCE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN SECRETION; VACCINE PRODUCTION; VISCERAL LEISHMANIASIS; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; ENZYMOLOGY; EPITOPE MAPPING; GENETICS; HUMAN; IMMUNOLOGY; MOLECULAR GENETICS; PARASITOLOGY; PROTEIN TERTIARY STRUCTURE;

ADAPTIVE IMMUNITY; AMINO ACID SEQUENCE; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; EPITOPE MAPPING; FEMALE; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-10; LEISHMANIA DONOVANI; LEISHMANIASIS, VISCERAL; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; N-GLYCOSYL HYDROLASES; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS;

EID: 78649855837     PISSN: None     EISSN: None     Source Type: Journal    
DOI: 10.1371/journal.pntd.0000866     Document Type: Article

References (55)

1. Lukes J, Mauricio IL, Schönian G, Dujardin JC, Soteriadou K, et al. (2007) Evolutionary and geographical history of the Leishmania donovani complex with a revision of current taxonomy. Proc Natl Acad Sci U S A 104: 9375-9380. doi: 10.1073/pnas.0703678104.
2. Mauricio IL, Yeo M, Baghaei M, Doto D, Pratlong F (2006) Towards multilocus sequence typing of the Leishmania donovani complex: resolving genotypes and haplotypes for five polymorphic metabolic enzymes (ASAT, GPI, NH1, NH2, PGD). Int J Parasitol 36: 757-769. doi: 10.1016/j.ijpara.2006.03.006.
3. Gopaul DN, Meyer SL, Degano M, Sacchettini JC, Schramm VL (1996) Inosine-uridine nucleoside hydrolase from Crithidia fasciculata. Genetic characterization, crystallization, and identification of histidine 241 as a catalytic site residue. Biochemistry 35: 5963-5970. doi: 10.1021/bi952998u.
4. Pellé R, Schramm VL, Parkin DW (1998) Molecular cloning and expression of a purine-specific N-ribohydrolase from Trypanosoma brucei brucei. Sequence, expression and molecular analysis. J Biol Chem 273: 2118-2126. doi: 10.1074/jbc.273.4.2118.
5. Miller RL, Sabourin CLK, Krenitsky TA, Berens RL, Marr JJ (1984) Nucleoside Hydrolase from Trypanosoma cruzi. J Biol Chem 259: 5073-5077.
6. Shi W, Schramm VL, Almo SC (1999) Nucleoside hydrolase from Leishmania major. Cloning, expression, catalytic properties, transition state inhibitors, and the 2.5-A° crystal structure. J Biol Chem 274: 21114-21120. doi: 10.1074/jbc.274.30.21114.
7. Cui L, Rajasekariah GR, Martin SK (2001) A nonspecific nucleoside hydrolase from Leishmania donovani: implications for purine salvage by the parasite. Gene 280: 153-162. doi: 10.1016/S0378-1119(01)00768-5.
8. Santana DM, Borja-Cabrera GP, Paraguai de Souza E, Sturm NR, Palatnik de Sousa CB, et al. (2002) Nucleoside hydrolase from Leishmania (L.) donovani is an antigen diagnostic for visceral leishmaniasis. Mol Biochem Parasitol 120: 315-319. doi: 10.1016/S0166-6851(02)00010-5.
9. Iovane E, Giabbai B, Muzzolini L, Matafora V, Fornili A, et al. (2008) Structural basis for substrate specificity in group I nucleoside hydrolases. Biochemistry 47: 4418-4426. doi: 10.1021/bi702448s.
10. Todd SJ, Moir AJ, Johnson MJ, Moir A (2003) Genes of Bacillus cereus and Bacillus anthracis encoding proteins of the exosporium. J Bacteriol 185: 3373-3378. doi: 10.1128/JB.185.11.3373-3378.2003.
11. Mitterbauer R, Karl T, Adam G (2002) Saccharomyces cerevisiae URH1 (encoding uridine-cytidine N-ribohydrolase): functional complementation by a nucleoside hydrolase from a protozoan parasite and by a mammalian uridine phosphorylase. Appl Environ Microbiol 68: 1336-1343. doi: 10.1128/AEM.68.3.1336-1343.2002.
12. UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases (TDR) (1997) Guidelines for the evaluation of Plasmodium falciparum vaccines in populations exposed to natural infections. World Health Organization (ed.), Geneva, Switzerland. Available: http://www.who.int/vaccine_research/feuill_1_4-2.pdf. Accessed 9 April 2010.
13. BLAST-National Institutes of Health (NIH). Available: http://blast.ncbi.nlm.nih.gov/Blast.cgi. Accessed 2010 April, 9.
14. Aguilar-Be I, Zardo RS, Paraguai de Souza E, Borja-Cabrera GP, Rosado- Vallado M, et al. (2005) Cross-protective efficacy of a prophylactic Leishmania donovani DNA vaccine against visceral and cutaneous murine leishmaniasis. Infec Immun 73: 812-819. doi: 10.1128/IAI.73.2.812-819.2005.
15. Chalé-Balboa WG, Mut-Martin M, Ramirez-Sierra MJ, Garcia-Miss MR, Dumonteil E (2009) A combination DNA vaccine encoding nucleoside hydrolase 36 and glycoprotein 63 protects female but not male hamsters against Leishmania mexicana. Parasite 16: 227-230.
16. Souza LOP, Palatnik de Sousa CB (2009) The Nucleoside hydrolase DNA vaccine VR1012NH36 in prophylactic vaccination against mice tegumentar leishmaniasis. Proc Vaccinol 1: 120-123. doi: 10.1016/j.provac.2009.07.022.
17. Al-Wabel MA, Tonui WK, Cui L, Martin SK, Titus RG (2007) Protection of susceptible BALB/c mice from challenge with Leishmania major by nucleoside hydrolase, a soluble exo-antigen of Leishmania. Am J Trop Med Hyg 77:1060-1065.
18. da Silva VO, Borja-Cabrera GP, Correia Pontes NN, Paraguai de Souza E, Luz KG, et al. (2001) A Phase III trial of Efficacy of the FML- vaccine against canine kala-azar in an endemic area of Brazil (Sa ̃o Gonc ̧alo do Amarante, RN). Vaccine 19: 1068-1081. doi: 10.1016/S0264-410X(00)00339-X.
19. Borja-Cabrera GP, Santos FN, Bauer FS, Parra LE, Menz I, et al. (2008) Immunogenicity assay of the Leishmune vaccine against canine visceral leishmaniasis in Brazil. Vaccine 26: 4991-4997. doi: 10.1016/j.vaccine.2008.7.029.
20. Palatnik-de-Sousa CB, Barbosa AF, Oliveira SM, Nico D, Bernardo RR, et al. (2008) The FML-vaccine against canine visceral leishmaniasis: from the second generation to the synthetic vaccine. Exp Rev Vaccines 7: 833-851. doi: 10.1586/14760584.7.6.833.
21. Saraiva EM, Mendes-Aguiar CO, Paraguai de Souza E, Borja-Cabrera GP, Fampa P, et al. (2006) The FML-vaccine (Leishmune) against canine visceral leishmaniasis: a transmission blocking vaccine. Vaccine 24: 2423-2431. doi: 10.1016/j.vaccine.2005.11.061.
22. Palatnik-de-Sousa CB, Silva-Antunes I, Morgado AA, Menz I, Palatnik M, et al. (2009) Decrease of the incidence of human and canine visceral leishmaniasis after dog vaccination with Leishmune in Brazilian endemic areas. Vaccine 27: 3505-12. doi: 10.1016/j.vaccine.2009.03.045.
23. Palatnik-de-Sousa CB, Gomes EM, Paraguai de Souza E, Santos WR, Macedo SR, et al. (1996) The FML (Fucose Mannose Ligand) of Leishmania donovani. A new tool in diagnosis, prognosis, transfusional control and vaccination against human Kala-azar. Rev Soc Bras Med Trop 29: 153-163.
24. Palatnik de Sousa CB, Dutra HS, Borojevic R (1993) Leishmania donovani surface glycoproteins GP36, is the major immunogen component of the Fucose Mannose Ligand (FML). Acta Trop 53: 59-72. doi: 10.1016/0001-706X(93) 90006-W.
25. Paraguai de Souza E, Bernardo RR, Palatnik M, Palatnik de Sousa CB (2001) Vaccination of Balb/c mice against experimental visceral leishmaniasis with the GP36 glycoprotein antigen of Leishmania donovani. Vaccine 19: 3104-3115. doi: 10.1016/S0264-410X(01)00031-7.
26. Borja-Cabrera GP, Santos FB, Picillo E, Gravino E, Manna L, et al. (2009) Nucleoside hydrolase DNA vaccine against visceral leishmaniasis. Proc Vaccinol 1: 104-109. doi: 10.1016/j.provac.2009.07.019.
27. Gamboa-León R, Paraguai de Souza E, Borja Cabrera GP, Santos FN, Miyashiro LM, et al. (2006) Immunotherapy against visceral leishmaniasis with the nucleoside hydrolase-DNA vaccine of L. donovani. Vaccine 24: 4863-4873. doi: 10.1016/j.vaccine.2006.03.005.
28. Nico D, Claser C, Rodrigues MM, Soares IS, Palatnik-de-Sousa CB (2009) Cloning of the Nucleoside hydrolase of Leishmania donovani aiming at the development of a synthetic vaccine against visceral leishmaniasis. Proc Vaccinol 1: 115-119. doi: 10.1016/j.provac.2009.07.021.
29. Kao DJ, Hodges RS (2009) Advantages of a synthetic peptide immunogen over a protein immunogen in the Development of an anti-pilus vaccine for Pseudomonas aeruginosa. Biol Drug Res 74: 33-42. 10.1111/j.1747-0285.2009.00825.
30. Parra-López C, Calvo-Calle M, Cameron TO, Vargas LE, Salazar LM, et al. (2006) Major Histocompatibility Complex and T cell interactions of a universal T-cell epitope from Plasmodium falciparum circumsporozoite protein. J Biol Chem 281: 14907-14917. dói: 10.1074/jbc.M511571200.
31. Moreno A, Clavijo P, Edelman R, Davis J, Sztein M, et al. (1993) CD4+ T cell clones obtained from Plasmodium falciparum sporozoite-immunized volunteers recognize polymorphic sequences of the circumsporozoite protein. J Immunol 151: 489-499.
32. Oliveira-Freitas E, Casas CP, Borja-Cabrera GP, Santos FN, Nico D, et al. (2006) Acylated and deacylated saponins of Quillaja saponaria mixture as adjuvants for the FML-vaccine against visceral leishmaniasis. Vaccine 24: 3909-3920. doi: 10.1016/j.vaccine.2006.02.034.
33. Santos WR, de Lima VMF, Paraguai de Souza E, Bernardo RR, Palatnik M, et al. (2002) Saponins, IL12 and BCG adjuvant in the FML-vaccine formulation against murine visceral leishmaniasis. Vaccine 21: 30-43. doi: 10.1016/S0264-410X(02)00444-9.
34. Palatnik de Sousa CB, Bunn Moreno MM, Paraguai de Souza E, Borojevic R (1994) Vaccination with the FML antigen (Fucose Mannose Ligand) of Leishmania donovani protects hamsters from experimental Visceral Leishmaniasis. J Braz Soc Adv Sci Ciência Cultura 46: 290-296.
35. Manna L, Reale S, Viola E, Vitale F, Manzillo VF, et al. (2006) Leishmania DNA load and cytokine expression levels in asymptomatic naturally infected dogs. Vet Parasitol 142: 271-280. doi: 10.1016/j.vetpar.2006.06.028.
36. Murray HW, Hariprashad J (1995) Interleukin 12 is effective treatment for an established systemic intracellular infection: experimental visceral leishmaniasis. J Exp Med 181: 387-391.
37. Taylor AP, Murray HW (1997) Intracellular antimicrobial activity in the absence of interferon-gamma: effect of interleukin-12 in experimental visceral leishmaniasis in interferon-gamma gene-disrupted mice. J Exp Med 185: 1231-1239.
38. Selvapandiyan A, Dey R, Nylen S, Duncan R, Sacks D, et al. (2009) Intracellular replication-deficient Leishmania donovani induces long-lasting protective immunity against visceral leishmaniasis. J Immunol 183: 1813-1820. doi: 10.4049/jimmunol.0900276.
39. Manna PP, Chakrabarti G, Bandyopadhyaya S (2010) Innate immune defense in visceral leishmaniasis: cytokine mediates protective role by allogeneic effector cells. Vaccine 28: 803-810. doi: 10.1016/j.vaccine.2009.10.053.
40. Liew FY, Li Y, Millot S (1990) Tumor necrosis factor-a synergizes with IFN-c in mediating killing of Leishmania major through the induction of nitric oxide. J Immunol 145: 4306-4310.
41. Alves CF, de Amorim IF, Moura EP, Ribeiro RR, Alves CF, et al. (2009) Expression of IFNc, TNFa, IL-10 and TGFb in lymph nodes associates with parasite load and clinical form of disease in dogs naturally infected with Leishmania (Leishmania) chagasi. Vet Immunol Immunopathol 128: 349-358. doi:10.1016/j.vetimm.2008.11.020.
42. Sanchez-Robert E, Altet L, Alberola J, Rodriguez-Cortés A, Ojeda A, et al. (2008) Longitudinal analysis of cytokine gene expression and parasite load in PBMC in Leishmania infantum experimentally infected dogs. Vet Immunol Immunopathol 125: 168-175. doi: 10.1016/j.vetimm.2008.04.010.
43. De Leonardis F, Govoni M, Lo Monaco A, Trotta F (2009) Visceral leishmaniasis and anti TNFa therapy: case report and review of literature. Clin Exp Rheumatol 27: 502-506.
44. Melby PC, Yang J, Zhao W, Perez LE, Cheng J (2001) Leishmania donovani p36(LACK) DNA vaccine is highly immunogenic but not protective against experimental visceral leishmaniasis. Infect Immun 69: 4719-4725. doi: 10.1128/IAI.69.8.
45. Phillips R, Svensson M, Aziz N, Maroof A, Brown N, et al. (2010) Innate Killing of Leishmania donovani by Macrophages of the Splenic Marginal Zone Requires IRF-7. Plos Pathogens 6: 1-13. doi: 10.1371/journal.ppat.1000813.
46. Seder RA, Darrah PA, Roederer M (2008) T cell quality in memory and protection: implications for vaccine design. Nature Rev 8: 247-258. doi:10.1038/nri2274.
47. Darrah PA, Patel DT, De Luca PM, Lindsay RWB, Davey DF, et al. (2007) Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Medicine 13: 843-850. doi: 10.1038/nm1592.
48. Carvalho LO, Calabrese K da S, da Costa SC, Mendes VG, da Silva AP, et al. (2008) Leishmania (Leishmania) amazonensis: experimental cutaneous leishmaniasis associated with systemic amyloidosis in mice. Exp Parasitol 120(1): 123-5. doi: 10.1016/j.exppara.2008.06.004.
49. Scharfetsin J (2005) Parasite cysteine proteinase interactions with alpha 2- macroglobulin or kininogens: differential pathways modulating inflammation and innate immunity in infection by pathogenic typanosomatids. Immunobiology 211: 117-25. doi: 10.1016/j.imbio.2005.10.014.
50. Guerra CS, Macedo Silva RM, Carvalho LO, Calabrese KD, Bozza PT, et al. (2010) Histopathological analysis of initial cellular response in TLR-2 deficient mice experimentally infected by Leishmania (L.) amazonensis. nt J Exp Pathol 2010 Jun 25 I. Epub ahead of print. doi: 10.1111/j.1365-2613.2010.00717.
51. Coelho EA, 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. Inf Immun 71: 3988-94. doi:10.1128/IAI.71.7.3988-3994.2003.
52. Marciani DJ (2003) Vaccine adjuvants: role and mechanisms of action in vaccine immunogenicity. Drug Discov Today 8: 934-943. doi: 10.1016/S1359- 6446(03)02864-2.
53. Palatnik-de-Sousa CB (2008) Vaccines for leishmaniasis in the fore coming 25 years. Review. Vaccine 26: 1709-1724. doi: 10.1016/j.vaccine.2008.01.023.
54. Basu R, Roy S, Walden P (2007) HLA class I-restricted T cell epitopes of the kinetoplastid membrane protein-11 presented by Leishmania donovani-infected human macrophages. J Infect Dis 195: 1373-1380. doi: 10.1086/513439.
55. Bertholet S, Goto Y, Carter L, Bhatia A, Howard RF, et al. (2009) Optimized subunit vaccine protects against experimental leishmaniasis. Vaccine 27: 7036-7945. doi: 10.1016/j.vaccine.2009.09.066.