Leishmania major LACK Antigen Is Required for Efficient Vertebrate Parasitization

Journal of Experimental Medicine

Volumn 198, Issue 11, 2003, Pages 1689-1698

  Kelly, Ben L ^a   Stetson, Daniel B ^a   Locksley, Richard M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Gene targeting; LACK; Leishmania major; Protozoa; WD repeat proteins

Indexed keywords

ANTIGEN; EPITOPE; GENOMIC DNA; LACK ANTIGEN; UNCLASSIFIED DRUG;

AMASTIGOTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIPLOIDY; DRUG TARGETING; GENE LOCUS; GENE TARGETING; GENETIC COMPLEMENTATION; GENOME; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOLOCALIZATION; IN VITRO STUDY; LEISHMANIA MAJOR; LEISHMANIASIS; LIFE CYCLE; MACROPHAGE; MAMMAL; MOUSE; MOUSE STRAIN; MUTANT; NONHUMAN; PARASITE; PARASITE DEVELOPMENT; PARASITE MIGRATION; PARASITE PREVALENCE; PARASITE SURVIVAL; PARASITE VIRULENCE; PARASITISM; PRIORITY JOURNAL; PROMASTIGOTE; PROTOZOAL GENETICS; T LYMPHOCYTE; VERTEBRATE; WILD TYPE;

ANIMALS; ANTIGENS, PROTOZOAN; BLOTTING, SOUTHERN; BLOTTING, WESTERN; GENE TARGETING; GENES, PROTOZOAN; LEISHMANIA MAJOR; MACROPHAGES; MICE; MICE, INBRED BALB C; MICROSCOPY, FLUORESCENCE; PROTOZOAN PROTEINS; TEMPERATURE;

EID: 0344305409     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20031162     Document Type: Article

References (45)

1. Mougneau, E., F. Altare, A.E. Wakil, S. Zheng, T. Coppola, Z.E. Wang, R. Waldmann, R.M. Locksley, and N. Glaichenhaus. 1995. Expression cloning of a protective Leishmania antigen. Science. 268:563-566.
2. + T cells instructs Th2 development and susceptibility to Leishmania major in BALB/c mice. Immunity. 6:541-549.
3. Launois, P., K.G. Swihart, G. Milon, and J.A. Louis. 1997. Early production of IL-4 in susceptible mice infected with Leishmania major rapidly induces IL-12 unresponsiveness. J. Immunol. 158:3317-3324.
4. Pingel, S., P. Launois, D.J. Fowell, C.W. Turck, S. Southwood, A. Sette, N. Glaichenhaus, J.A. Louis, and R.M. Locksley. 1999. Altered ligands reveal limited plasticity in the T cell response to a pathogenic epitope. J. Exp. Med. 189:1111-1120.
5. Julia, V., M. Kassoulzadegan, and N. Glaichenhaus. 1996. Resistance to Leishmania induced by tolerance to a single antigen. Science. 274:421-423.
6. Stetson, D.B., M. Mohrs, V. Mallet-Designe, L. Teyton, and R.M. Locksley. 2002. Rapid expansion and IL-4 expression by Leishmania-specific naïve helper T cells in vivo. Immunity. 17:191-200.
7. Etges, R., J. Bouvier, and C. Bordier. 1986. The major surface protein of Leishmania promastigotes is a protease. J. Biol. Chem. 261:9098-9101.
8. Tapia, E., E. Perez-Jimenez, L. Lopez-Fuertes, R. Gonzalo, M.M. Gherardi, and M. Esteban. 2003. The combination of DNA vectors expressing IL-12 + IL-18 elicits high protective immune response against cutaneous leishmaniasis after priming with DNA-p36/LACK and the cytokines, followed by a booster with a vaccinia virus recombinant expressing p36/LACK. Microbes Infect. 5:73-84.
9. Gonzalo, R.M., J.R. Rodriguez, D. Rodriguez, G. Gonzalez-Aseguinolaza, V. Larraga, and M. Esteban. 2001. Protective immune response against cutaneous leishmaniasis by prime/booster immunization regimens with vaccinia virus recombinants expressing Leishmania infantum p36/LACK and IL-12 in combination with purified p36. Microbes Infect. 3:701-711.
10. Gurunathan, S., D.L. Sacks, D.L. Brown, S.L. Reiner, H. Charest, N. Glaichenhaus, and R.A. Seder. 1997. Vaccination with DNA encoding the immunodominant LACK parasite antigen confers protective immunity to mice infected with Leishmania major. J. Exp. Med. 186:1137-1147.
11. Neer, E.J., C.J. Schmidt, K. Nambudripad, and T.F. Smith. 1994. The ancient regulatory-protein family of WD-repeat proteins. Nature. 371:297-300.
12. Lambright, D.G., J. Sondek, A. Bohm, N.P. Skiba, H.E. Hamm, and P.B. Sigler. 1996. The 2.0 A crystal structure of a heterotrimeric G protein. Nature. 379:311-319.
13. Smith, T.F., C. Gaitatzes, K. Saxena, and E.J. Neer. 1999. The WD repeat: a common architecture for diverse functions. Trends Biochem. Sci. 24:181-185.
14. Ron, D., C.H. Chen, J. Caldwell, L. Jamieson, E. Orr, and D. Mochly-Rosen. 1994. Cloning of an intracellular receptor for protein kinase C: a homolog of the β subunit of G proteins. Proc. Natl. Acad. Sci. USA. 91:839-843.
15. Mochly-Rosen, D., and A.S. Gordon. 1998. Anchoring proteins for protein kinase C: a means for isozyme selectivity. FASEB J. 12:35-42.
16. Mochly-Rosen, D., B.L. Smith, C.H. Chen, M.H. Disatnik, and D. Ron. 1995. Interaction of protein kinase C with RACK1, a receptor for activated C kinase: a role in beta protein kinase C mediated signal transduction. Biochem. Soc. Trans. 23:596-600.
17. Dell, E.J., J. Connor, S. Chen, E.G. Stebbins, N.P. Skiba, D. Mochly-Rosen, and H.E. Hamm. 2002. The βγ subunit of heterotrimeric G proteins interacts with RACK1 and two other WD repeat proteins. J. Biol. Chem. 277:49888-49895.
18. Rodriguez, M.M., D. Ron, K. Touhara, C.H. Chen, and D. Mochly-Rosen. 1999. RACK1, a protein kinase C anchoring protein, coordinates the binding of activated protein kinase C and select pleckstrin homology domains in vitro. Biochemistry. 38:13787-13794.
19. Chang, B.Y., K.B. Conroy, E.M. Machleder, and C.A. Cartwright. 1998. RACK1 a receptor for activated C kinase and a homolog of the beta subunit of G proteins, inhibits activity of src tyrosine kinases and growth of NIH 3T3 cells. Mol. Cell. Biol. 18:3245-3256.
20. Chang, B.Y., M. Chiang, and C.A. Cartwright. 2001. The interaction of Src and RACKI is enhanced by activation of protein kinase C and tyrosine phosphorylation of RACK1. J. Biol. Chem. 276:20346-20356.
21. Lilient, J., and D.D. Chang. 1998. Rack1, a receptor for activated protein kinase C, interacts with integrin beta subunit. J. Biol. Chem. 273:2379-2383.
22. Welburn, S.C., and N.B. Murphy. 1998. Prohibitin and RACK homologues are up-regulated in trypanosomes induced to undergo apoptosis and in naturally occurring terminally differentiated forms. Cell Death Differ. 5:615-622.
23. Gonzalez-Aseguinolaza, G., S. Taladriz, A. Marquet, and V. Larraga. 1999. Molecular cloning, cell localization and binding affinity to DNA replication proteins of the p36/LACK protective antigen from Leishmania infantum. Eur. J. Biochem. 259:909-916.
24. Taladriz, S., G. Gonzalez-Aseguinolaza, A. Marquet, and V. Larraga. 1999. Cloning, molecular analysis and differential cell localization of the p36 RACK analogue antigen from the parasite protozoon Crithidia fasciculata. FEBS Lett. 443:375-380.
25. Korchak, H.M., and L.E. Kilpatrick. 2001. Roles for βII-protein kinase C and RACK1 in positive and negative signaling for superoxide anion generation in differentiated HL60 cells. J. Biol. Chem. 276:8910-8917.
26. Tardif, M., M. Savard, L. Flamand, and J. Gosselin. 2002. Impaired protein kinase C activation/translocation in Epstein-Barr virus-infected monocytes. J. Biol. Chem. 277:24148-24154.
27. Pingel, S., Z.E. Wang, and R.M. Locksley. 1998. Distribution of protein kinase C isoforms after infection of macrophages with Leishmania major. Infect. Immun. 66:1795-1799.
28. Joshi, P.B., D.L. Sacks, G. Modi, and W.R. McMaster. 1998. Targeted gene deletion of Leishmania major genes encoding developmental stage-specific leishmanolysin (GP63). Mol. Microbiol. 27:519-530.
29. Joshi, P.B., B.L. Kelly, S. Kamhawi, D.L. Sacks, and W.R. McMaster. 2002. Targeted gene deletion in Leishmania major identifies leishmanolysin (GP63) as a virulence factor. Mol. Biochem. Parasitol. 120:33-40.
30. Ha, D.S., J.K. Schwartz, S.J. Turco, and S.M. Beverley. 1996. Use of the green fluorescent protein as a marker in transfected Leishmania. Mol. Biochem. Parasitol. 77:57-64.
31. Medina-Acosta, E., and G.A.M. Cross. 1993. Rapid isolation of DNA from trypanosomatid protozoa using a simple 'mini-prep' procedure. Mol. Biochem. Parasitol. 59:327-329.
32. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 545 pp.
33. + T cells. Immunity. 11:399-409.
34. Philpott, K.L., J.L. Viney, G. Kay, S. Rastan, E.M. Gardiner, S. Chae, A.C. Hayday, and M.J. Owen. 1992. Lymphoid development in Mice congenitally lacking T cell receptor αβ-expressing cells. Science. 256:1448-1452.
35. Descoteaux, A., G. Matlashewski, and S.J. Turco. 1992. Inhibition of macrophage protein kinase C-mediated protein phosphorylation by Leishmania donovani lipophosphoglycan. J. Immunol. 149:3008-3015.
36. Miller, S.I., and D.F. Wirth. 1988. Trans-splicing in Leishmania enriettii and identification of ribonucleoprotein complexes containing the spliced leader and U2 equivalent RNAS. Mol. Cell. Biol. 8:2597-2603.
37. Sacks, D.L., T.N. Brodin, and S.L. Turco. 1990. Developmental modification of the lipophosphoglycan from Leishmania major promastigotes during metacyclogenesis. Mol. Biochem. Parasitol. 42:225-234.
38. + T cells in pathogenesis associated with Leishmania amazonensis infection. J. Immunol. 158:5374-5383.
39. Belkaid, Y., S. Mendez, R. Lira, N. Kadambi, G. Milon, and D. Sacks. 2000. A natural model of Leishmania major infection reveals a prolonged "silent" phase of parasite amplification in the skin before the onset of lesion formation and immunity. J. Immunol. 165:969-977.
40. Bourreau, E., G. Prevot, J. Gardon, R. Pradinaud, H. Hasagewa, G. Milon, and P. Launois. 2002. LACK-specific CD4(+) T cells that induce gamma interferon production in patients with localized cutaneous leishmaniasis during an early stage of infection. Infect. Immun. 70:3122-3129.
41. Kelly, B.L., S.D. Dyall, J.P. Warner, J. Tang, and D.F. Smith. 1995. Chromosomal organization of a repeated gene cluster expressed in mammalian stages of Leishmania. Gene. 163:145-149.
42. Voth, B.R., B.L. Kelly, P.B. Joshi, A.C. Ivens, and W.R. McMaster. 1998. Differentially expressed Leishmania major gp63 genes encode cell surface leishmanolysin with distinct signals for glycosylphosphatidylinositol attachment. Mol. Biochem. Parasitol. 93:31-41.
43. + T cells. J. Immunol. 165:915-924.
44. Späth, G.F., L. Lye, H. Segawa, D.L. Sacks, S.J. Turco, and S.M. Beverley. 2003. Persistence without pathology in phosphoglycan-deficient Leishmania major. Science. 301:1241-1243.
45. Bogdan, C., N. Donhauser, R. Döring, M. Röllinghoff, A. Diefenbach, and M.G. Rittig. 2000. Fibroblasts as host cells in latent leishmaniosis. J. Exp. Med. 191:2121-2129.