Immunization of mice with a TolA-like surface protein of Trypanosoma cruzi generates CD4+ T-cell-dependent parasiticidal activity

Infection and Immunity

Volumn 67, Issue 9, 1999, Pages 4603-4612

  Quanquin, Natalie M ^a,b   Galaviz, Charles ^a,c   Fouts, David L ^a   Wrightsman, Ruth A ^a   Manning, Jerry E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 2; NITRIC OXIDE; PROTEIN TOLT; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CYTOKINE PRODUCTION; FEMALE; GENE EXPRESSION; GENE SEQUENCE; HELPER CELL; MACROPHAGE ACTIVATION; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; T LYMPHOCYTE ACTIVATION; TRYPANOSOMA CRUZI;

EID: 0032774770     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.67.9.4603-4612.1999     Document Type: Article

References (46)

1. Beard, C. A., J. L. Saborio, D. Tewari, K. G. Krieglstein, A. H. Henschen, and J. E. Manning. 1992. Evidence for two distinct major protein components, PAR 1 and PAR 2, in the paraflagellar rod of Trypanosoma cruzi. J. Biol. Chem. 267:21656-21662.
2. Beard, C. A., R. A, Wrightsman, and J. E. Manning. 1988. Stage and strain specific expression of the tandemly repeated 90 kDa surface antigen gene family in Trypanosoma cruzi. Mol. Biochem. Parasitol. 28:227-234.
3. Brendel, V., P. Bucher, I. R. Nourbakhsh, B. E. Blaisdell, and S. Karlin. 1992. Methods and algorithms for statistical analysis of protein sequences. Proc. Natl. Acad. Sci. USA 89:2002-2006.
4. Chou, K. C. 1995. A novel approach to predicting protein structural classes in a (20-1)-D amino acid composition space. Proteins 21:319-344.
5. Deleage, G., and B. Roux. 1989. Use of class prediction to improve protein secondary structure prediction: joint prediction with methods based on sequence homology, p. 147-196. In G. D. Fasman (ed.), Prediction of protein structure and the principles of protein conformation. Plenum Press, New York, N. Y.
6. Dennis, J. J., E. R. Lafontaine, and P. A. Sokol. 1996. Identification and characterization of the tolQRA genes of Pseudomonas aeruginosa. J. Bacteriol. 178:7059-7068.
7. Fouts, D. L., J. E. Manning, G. M. Fox, and C. W. Schmid. 1981. A complex repeated DNA sequence within the Drosophila transposable element copia. Nucleic Acids Res. 9:7053-7064.
8. Fouts, D. L., B. J. Ruef, P. T. Ridley, R. A. Wrightsman, D. S. Peterson, and J. E. Manning. 1991. Nucleotide sequence and transcription of a trypomastigote surface antigen gene of Trypanosoma cruzi. Mol. Biochem. Parasitol. 46:189-200.
9. Julius, M. H., E. Simpson, and L. A. Herzenberg. 1973. A rapid method for the isolation of functional thymus-derived lymphocytes. Eur. J. Immunol. 3: 645-649.
10. Kierszenbaum, F., and J. G. Howard. 1976. Mechanisms of resistance against experimental Trypanosoma cruzi infection: the importance of antibodies and antibody-forming capacity in the Biozzi high and low responder mice. J. Immunol. 116:1208-1211.
11. King, R. D., and J. E. Sternberg. 1990. Machine learning approach for the prediction of protein secondary structure. J. Mol. Biol. 216:441-457.
12. Krettli, A. U., and Z. Brener. 1976. Protective effects of specific antibodies in Trypanosoma cruzi infections. J. Immunol. 116:755-761.
13. Lanar, D. 1979. Growth and isolation of Trypanosoma cruzi cultivated with Triatoma infestans embryo cell line. J. Protozool. 26:457-462.
14. Lebowitz, J. H., H. Q. Smith, L. Rusche, and S. M. Beverley. 1993. Coupling of poly(A) site selection and transsplicing in Leishmania. Genes Dev. 7: 996-1007.
15. Levengood, S. K., W. F. J. Beyer, and R. E. Webster. 1991. To1A: a membrane protein involved in colicin uptake contains an extended helical region. Proc. Natl. Acad. Sci. USA 88:5939-5943.
16. Levengood-Freyermuth, S. K., E. M. Click, and R. E. Webster. 1993. Role of the carboxyl-terminal domain of To1A in protein import and integrity of the outer membrane. J. Bacteriol. 175:222-228.
17. Levin, J. M., and J. Garnier. 1988. Improvements in a secondary structure prediction method based on a search for local sequence homologies and its use as a model building tool. Biochim. Biophys. Acta 95:283-295.
18. + CTL. J. Immunol. 160:1817-1823.
19. Mao, B., K. C. Chou, and C. T. Zhang. 1994. Protein folding classes: a geometric interpretation of the amino acid composition of globular proteins. Protein Eng. 7:319-330.
20. Miller, M. J., R. A. Wrightsman, and J. E. Manning. 1996. Trypanosoma cruzi: protective immunity in mice immunized with paraflagellar rod proteins is associated with a T-helper type 1 response. Exp. Parasitol. 84:156-167.
21. Miller, M. J., R. A. Wrightsman, G. A. Stryker, and J. E. Manning. 1997. Protection of mice against Trypanosoma cruzi by immunization with paraflagellar rod proteins requires T cell, but not B cell, function. J. Immunol. 158:5330-5337.
22. Munoz-Fernandez, M. A., M. A. Fernandez, and M. Fresno. 1992. Synergism between tumor necrosis factor-α and interferon-γ on macrophage activation for the killing of intracellular Trypanosoma cruzi through a nitric oxide-dependent mechanism. Eur. J. Immunol. 22:301-307.
23. Neesen, J., S. Padmanabhan, and H. Bunemann. 1994. Tandemly arranged repeats of a novel highly charged 16-amino-acid motif representing the major component of the sperm-tail-specific axoneme-associated protein family Dhmst101 form extended alpha-helical rods within the extremely elongated spermatozoa of Drosophila hydei. Eur. J. Biochem. 225:1089-1095.
24. Neesen, J., H. Bunemann, and U. A. Heilein. 1994. The Drosophila hydei gene Dhmst101(1) encodes a testis-specific, repetitive, axoneme-associated protein with differential abundance in Y chromosomal deletion mutant flies. Dev. Biol. 162:414-425.
25. Nickell, S. P., A. Gebremichael, R. Hoff, and M. H. Boyer. 1987. Isolation and functional characterization of murine T cell lines and clones specific for the protozoan parasite Trypanosoma cruzi. J. Immunol. 138:914-921.
26. + T-cell clones: T helper type 1-like phenotype and reactivity with shed trypomastigote antigens. Infect. Immun. 61:3250-3258.
27. Peterson, D. S., R. A. Wrightsman, and J. E. Manning. 1985. Cloning of a major surface-antigen gene of Trypanosoma cruzi and identification of a nonapeptide repeat. Nature 322:566-568.
28. Rodriguez, A. M., F. Santor, D. Afchain, H. Bazin, and A. Capron. 1981. Trypanosoma cruzi infection in B-cell-deficient rats. Infect. Immun. 31:524-529.
29. Rottenberg, M. E., M. Bakhiet, T. Olsson, K. Kristensson, T. Mak, H. Wigzell, and A. Orn. 1993. Differential susceptibilities of mice genomically deleted of CD4 and CD8 to infections with Trypanosoma cruzi or Trypanosoma brucei. Infect. Immun. 61:5129-5133.
30. Rottenberg, M. E., A. Riarte, L. Sporrong, J. Altcheh, P. Petray, A. M. Ruiz, H. Wigzell, and A. Orn. 1994. Outcome of infection with different strains of Trypanosoma cruzi in mice lacking CD4 and/or CD8. Immunol. Lett. 45: 53-60.
31. Rozed, C. E., and N. Davidson. 1983. Drosophila has one myosin heavy-chain gene with three developmentally regulated transcripts. Cell 32:23-34.
32. Saborio, J. L., J. M. Hernandez, S. Narayanswami, R. A. Wrightsman, E. Palmer, and J. E, Manning. 1989. Isolation and characterization of paraflagellar proteins from Trypanosoma cruzi. J. Biol. Chem. 264:4071-4075.
33. Saborio, J. L., R. A. Wrightsman, S. G. Kazuko, B. S. Granger, and J. E. Manning. 1990. Trypanosoma cruzi: identification of a surface antigen restricted to the flagellar region of the infective form of the parasite. Exp. Parasitol. 70:411-418.
34. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N. Y.
35. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
36. Schendel, S. L., E. M. Click, R. E. Webster, and W. A. Cramer. 1997. The To1A protein interacts with colicin E1 differently than with other group A colicins. J. Bacteriol. 179:3683-3690.
37. Takehara, H. A., A. Perini, M. H. Da Silva, and I. Mota. 1981. Trypanosoma cruzi: role of different antibody classes in protection against infection in the mouse. Exp. Parasitol. 52:137-146.
38. Tarleton, R. L. 1997. Immunity to Trypanosoma cruzi, p. 227-247. In S. H. E. Kaufman (ed.), Host response to intracellular pathogens. R. G. Landes Co., Austin, Tex.
39. 2-microglobulin-deficient mice to Trypanosoma cruzi infection. Nature 356:338-340.
40. Tibayrenc, M. 1995. Population genetics of parasitic protozoa and other microorganisms. Adv, Parasitol. 36:47-115.
41. Wiche, G., B. Becker, K. Luber, G. Weitzer, M. J. Castanon, R. Hauptmann, C. Stratowa, and M. Stewart. 1991. Cloning and sequencing of rat plectin indicates a 466-kD polypeptide chain with a three-domain structure based on a central alpha-helical coiled coil. J. Cell Biol. 114:83-99.
42. + Tc1 responses. J. Immunol. 159:6120-6130.
43. Wizel, B., N. Garg, and R. L. Tarleton. 1998. Vaccination with trypomastigote surface antigen 1-encoding plasmid DNA confers protection against lethal Trypanosoma cruzi infection. Infect. Immun. 66:5073-5081.
44. Wrightsman, R. A., B. D. Dawson, D. L. Fouts, and J. E. Manning. 1994 Identification of immunodominant epitopes in Trypanosoma cruzi trypomastigote surface antigen-1 protein that mask protective epitopes. J. Immunol. 153:3148-3154.
45. Wrightsman, R. A., and J. E. Manning. Unpublished data.
46. Wrightsman, R. A., M. J. Miller, J. L. Saborio, and J. E. Manning. 1995 Pure paraflagellar rod protein protects mice against Trypanosoma cruzi infection. Infect. Immun. 63:122-125.