Expansion of CD4 T cells expressing a highly restricted TCR structure specific for a single parasite epitope correlates with high pathology in murine schistosomiasis

European Journal of Immunology

Volumn 35, Issue 9, 2005, Pages 2659-2669

  Finger, Eduardo ^a   Brodeur, Peter H ^a,b   Hernandez, Hector J ^b   Stadecker, Miguel J ^a,b  

^a TUFTS UNIVERSITY   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antigenic peptides epitopes; Parasite helminth; T cells; TCR; Th1 Th2 cells

Indexed keywords

CD4 ANTIGEN; EPITOPE; PROTEIN P40; PROTEIN SM; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; HYBRIDOMA CELL CULTURE; IMMUNOPATHOLOGY; IMMUNOSTIMULATION; LIVER DISEASE; MOLECULAR RECOGNITION; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; STRAIN DIFFERENCE; T LYMPHOCYTE;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, HELMINTH; CD4-POSITIVE T-LYMPHOCYTES; CLONING, MOLECULAR; FEMALE; HELMINTH PROTEINS; HYBRIDOMAS; IMMUNODOMINANT EPITOPES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED CBA; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RNA, HELMINTH; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SEQUENCE ANALYSIS, DNA;

EID: 26044476619     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200526344     Document Type: Article

References (71)

1. Bica, I., Hamer, D. H. and Stadecker, M. J., Hepatic schistosomiasis. Infect. Dis. Clin. North. Am. 2000. 14: 583-604, viii.
2. Gause, W. C., Urban, J. F., Jr. and Stadecker, M. J., The immune response to parasitic helminths: insights from murine models. Trends Immunol. 2003. 24: 269-277.
3. Pearce, E., Caspar, P., Grzych, J., Lewis, F. and Sher, A., Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J. Exp. Med. 1991. 173: 159-166.
4. Pearce, E. J. and MacDonald, A. S., The immunobiology of schistosomiasis. Nat. Rev. Immunol. 2002. 2: 499-511.
5. Hernandez, H. J., Sharpe, A. H. and Stadecker, M. J., Experimental murine schistosomiasis in the absence of B7 costimulatory molecules: reversal of elicited T cell cytokine profile and partial inhibition of egg granuloma formation. J. Immunol. 1999. 162: 2884-2889.
6. MacDonald, A. S., Patton, E. A., La Flamme, A. C., Araujo, M. I., Huxtable, C. R., Bauman, B. and Pearce, E. J., Impaired Th2 development and increased mortality during Schistosoma mansoni infection in the absence of CD40/CD154 interaction. J. Immunol. 2002. 168: 4643-4649.
7. Brunet, L. R., Finkelman, F. D., Cheever, A. W., Kopf, M. A. and Pearce, E. J., IL-4 protects against TNF-alpha-mediated cachexia and death during acute schistosomiasis. J. Immunol. 1997. 159: 777-785.
8. Chiaramonte, M. G., Donaldson, D. D., Cheever, A. W. and Wynn, T. A., An IL-13 inhibitor blocks the development of hepatic fibrosis during a T-helper type 2-dominated inflammatory response. J. Clin. Invest. 1999. 104: 777-785.
9. Fallon, P. G., Richardson, E. J., McKenzie, G. J. and McKenzie, A. N., Schistosome infection of transgenic mice defines distinct and contrasting pathogenic roles for IL-4 and IL-13: IL-13 is a profibrotic agent. J. Immunol. 2000. 164: 2585-2591.
10. Fanning, M., Peters, P., Davis, R., Kazura, J. and Mahmoud, A., Immunopathology of murine infection with Schistosoma mansoni: Relationship of genetic background to hepatosplenic disease and modulation. J. Infect. Dis. 1981. 144: 148-153.
11. Cheever, A., Duvall, R., Hallack Jr, T., Minker, R., Malley, J. and Malley, K., Variation of hepatic fibrosis and granuloma size among mouse strains infected with Schistosoma mansoni. Am. J. Trop. Med. Hyg. 1987. 37: 85-97.
12. Henderson, G. S., Nix, N. A., Montesano, M. A., Gold, D., Freeman, G. L., Jr., McCurley, T. L. and Colley, D. G., Two distinct pathological syndromes in male CBA/J inbred mice with chronic Schistosoma mansoni infections. Am. J. Pathol. 1993. 142: 703-714.
13. + T helper cell response to dominant epitope peptide of major egg antigen Sm-p40. Exp. Parasitol. 1998. 90: 122-130.
14. Cai, Y., Langley, J., Smith, D. and Boros, D., A cloned major Schistosoma mansoni egg antigen with homologies to small heat shock proteins elicits Th1 responsiveness. Infect. Immun. 1996. 64: 1750-1755.
15. Nene, V., Dunne, D. W., Johnson, K. S., Taylor, D. W. and Cordingley, J. S., Sequence and expression of a major egg antigen from Schistosoma mansoni. Homologies to heat shock proteins and alpha-crystallins. Mol. Biochem. Parasitol. 1986. 21: 179-188.
16. Cao, M., Chao, H. and Doughty, B., Cloning of a cDNA encoding an egg antigen homologue from Schistosoma mansoni. Mol. Biochem. Parasitol. 1993. 58: 169-171.
17. Chikunguwo, S. M., Quinn, J. J., Harn, D. A. and Stadecker, M. J., The cell-mediated response to schistosomal antigens at the clonal level. III. Identification of soluble egg antigens recognized by cloned specific granulomagenic murine CD4+ Th1-type lymphocytes. J. Immunol. 1993. 150: 1413-1421.
18. Hernandez, H. J., Trzyna, W. C., Cordingley, J. S., Brodeur, P. H. and Stadecker, M. J., Differential antigen recognition by T cell populations from strains of mice developing polar forms of granulomatous inflammation in response to eggs of Schistosoma mansoni. Eur. J. Immunol. 1997. 27: 666-670.
19. Hernandez, H. J. and Stadecker, M. J., Elucidation and role of critical residues of immunodominant peptide associated with T cell-mediated parasitic disease. J. Immunol 1999. 163: 3877-3882.
20. Asahi, H., Hernandez, H. J. and Stadecker, M. J., A novel 62-kilodalton egg antigen from Schistosoma mansoni induces a potent CD4(+) T helper cell response in the C57BL/6 mouse. Infect. Immun. 1999. 67: 1729-1735.
21. Asahi, H., Osman, A., Cook, R. M., LoVerde, P. T. and Stadecker, M. J., Schistosoma mansoni phosphoenolpyruvate carboxykinase, a novel egg antigen: immunological properties of the recombinant protein and identification of a T-cell epitope. Infect. Immun. 2000. 68: 3385-3393.
22. Williams, D. L., Asahi, H., Botkin, D. J. and Stadecker, M. J., Schistosome infection stimulates host CD4(+) T helper cell and B-cell responses against a novel egg antigen, thioredoxin peroxidase. Infect. Immun. 2001. 69: 1134-1141.
23. Uematsu, Y., A novel and rapid cloning method for the T-cell receptor variable region sequences. Immunogenetics 1991. 34: 174-178.
24. Chowers, Y., Holtmeier, W., Morzycka-Wroblewska, E. and Kagnoff, M. F., Inverse PCR amplification of rare T cell receptor delta messages from mucosal biopsy specimens. J. Immunol. Methods 1995. 179: 261-263.
25. Bill, J., Appel, V. B. and Palmer, E., An analysis of T-cell receptor variable region gene expression in major histocompatibility complex disparate mice. Proc. Natl. Acad. Sci. USA 1988. 85: 9184-9188.
26. Sant'Angelo, D. B., Cresswell, P., Janeway, C. A., Jr. and Denzin, L. K., Maintenance of TCR clonality in T cells expressing genes for two TCR heterodimers. Proc. Natl. Acad. Sci. USA 2001. 98: 6824-6829.
27. Franco, G. R., Valadao, A. F., Azevedo, V. and Rabelo, E. M., The Schistosoma gene discovery program: state of the art. Int. J. Parasitol. 2000. 30: 453-463.
28. Secor, W. E. and Freeman, G. L., Jr., Differential Vbeta T-cell receptor usage during chronic experimental schistosomiasis corresponds with distinct pathological presentations. Infect. Immun. 2001. 69: 4177-4179.
29. + T-cell receptor V beta usage during the immune response to Schistosoma mansoni. Infect. Immun. 1993. 61: 5381-5383.
30. + TCR repertoire heterogeneity in Schistosoma mansoni-induced granulomas. J. Immunol. 2002. 169: 6386-6393.
31. Cohen, S., McCluskey, R. T. and Benacerraf, B., Studies on the specificity of the cellular infiltrate of delayed hypersensitivity reactions. J. Immunol. 1967. 98: 269-273.
32. Deng, H., Apple, R., Clare-Salzler, M., Trembleau, S., Mathis, D., Adorini, L. and Sercarz, E., Determinant capture as a possible mechanism of protection afforded by major histocompatibility complex class II molecules in autoimmune disease. J. Exp. Med. 1993. 178: 1675-1680.
33. Berzofsky, J. A., Immunodominance in T lymphocyte recognition. Immunol. Lett. 1988. 18: 83-92.
34. Waldner, H., Whitters, M. J., Sobel, R. A., Collins, M. and Kuchroo, V. K., Fulminant spontaneous autoimmunity of the central nervous system in mice transgenic for the myelin proteolipid protein-specific T cell receptor. Proc. Natl. Acad. Sci. USA 2000. 97: 3412-3417.
35. Cole, G. A., Hogg, T. L. and Woodland, D. L., The MHC class I-restricted T cell response to Sendai virus infection in C57BL/6 mice: a single immunodominant epitope elicits an extremely diverse repertoire of T cells. Int. Immunol. 1994. 6: 1767-1775.
36. + T-cell recognition is directed predominantly to the hemagglutinin-neuraminidase glycoprotein. J. Virol. 1994. 68: 6863-6870.
37. Deckhut, A. M., Allan, W., McMickle, A., Eichelberger, M., Blackman, M. A., Doherty, P. C. and Woodland, D. L., Prominent usage of V beta 8.3 T cells in the H-2Db-restricted response to an influenza A virus nucleoprotein epitope. J. Immunol. 1993. 151: 2658-2666.
38. Holtappels, R., Podlech, J., Geginat, G., Steffens, H. P., Thomas, D. and Reddehase, M. J., Control of murine cytomegalovirus in the lungs: relative but not absolute immunodominance of the immediate-early 1 nonapeptide during the antiviral cytolytic T-lymphocyte response in pulmonary infiltrates. J. Virol. 1998. 72: 7201-7212.
39. Pewe, L. and Perlman, S., Immune response to the immunodominant epitope of mouse hepatitis virus is polyclonal, but functionally monospecific in C57Bl/6 mice. Virology 1999. 255: 106-116.
40. Rawle, F. C., Knowles, B. B., Ricciardi, R. P., Brahmacheri, V., Duerksen-Hughes, P., Wold, W. S. and Gooding, L. R., Specificity of the mouse cytotoxic T lymphocyte response to adenovirus 5. E1A is immunodominant in H-2b, but not in H-2d or H-2k mice. J. Immunol. 1991. 146: 3977-3984.
41. van der Most, R. G., Sette, A., Oseroff, C., Alexander, J., Murali-Krishna, K., Lau, L. L., Southwood, S. et al., Analysis of cytotoxic T cell responses to dominant and subdominant epitopes during acute and chronic lymphocytic choriomeningitis virus infection. J. Immunol. 1996. 157: 5543-5554.
42. Varga, S. M., Wang, X., Welsh, R. M. and Braciale, T. J., Immunopathology in RSV infection is mediated by a discrete oligoclonal subset of antigen-specific CD4(+) T cells. Immunity 2001. 15: 637-646.
43. Busch, D. H., Pilip, I. and Pamer, E. G., Evolution of a complex T cell receptor repertoire during primary and recall bacterial infection. J. Exp. Med. 1998. 188: 61-70.
44. Scheckelhoff, M. and Deepe, G. S., Jr., The protective immune response to heat shock protein 60 of Histoplasma capsulatum is mediated by a subset of V beta 8.1/8.2+ T cells. J. Immunol. 2002. 169: 5818-5826.
45. Myler, P. J., Sisk, E., McDonagh, P. D., Martinez-Calvillo, S., Schnaufer, A., Sunkin, S. M., Yan, S. et al., Genomic organization and gene function in Leishmania. Biochem. Soc. Trans. 2000. 28: 527-531.
46. Locksley, R. M., Heinzel, F. P., Sadick, M. D., Holaday, B. J. and Gardner, K. D., Jr., Murine cutaneous leishmaniasis: susceptibility correlates with differential expansion of helper T-cell subsets. Ann. Inst. Pasteur Immunol. 1987. 138: 744-749.
47. Sacks, D. and Noben-Trauth, N., The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2002. 2: 845-858.
48. Gumy, A., Louis, J. A. and Launois, P., The murine model of infection with Leishmania major and its importance for the deciphering of mechanisms underlying differences in Th cell differentiation in mice from different genetic backgrounds. Int. J. Parasitol. 2004. 34: 433-444.
49. + T cells instructs Th2 development and susceptibility to Leishmania major in BALB/c mice. Immunity 1997. 6: 541-549.
50. Kuchroo, V. K., Sobel, R. A., Laning, J. C., Martin, C. A., Greenfield, E., Dorf, M. E. and Lees, M. B., Experimental allergic encephalomyelitis mediated by cloned T cells specific for a synthetic peptide of myelin proteolipid protein. Fine specificity and T cell receptor V beta usage. J. Immunol. 1992. 148: 3776-3782.
51. Deng, H., Fosdick, L. and Sercarz, E., The involvement of antigen processing in determinant selection by class II MHC and its relationship to immunodominance. Apmis 1993. 101: 655-662.
52. Li, W. F., Fan, M. D., Pan, C. B. and Lai, M. Z., T cell epitope selection: dominance maybe determined by both affinity for major histocompatibility complex and stoichiometry of epitope. Eur. J. Immunol. 1992. 22: 943-949.
53. Rudensky, A., Preston-Hurlburt, P., Hong, S. C., Barlow, A. and Janeway, C. A., Jr., Sequence analysis of peptides bound to MHC class II molecules. Nature 1991. 353: 622-627.
54. Stadecker, M. J., Hernandez, H. J. and Asahi, H., The identification and characterization of new immunogenic egg components: implications for evaluation and control of the immunopathogenic T cell response in schistosomiasis. Mem. Inst. Oswaldo Cruz 2001. 96 Suppl: 29-33.
55. Reche, P. A., Glutting, J. P. and Reinherz, E. L., Prediction of MHC class I binding peptides using profile motifs. Hum. Immunol. 2002. 63: 701-709.
56. Rammensee, H., Bachmann, J., Emmerich, N. P., Bachor, O. A. and Stevanovic, S., SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 1999. 50: 213-219.
57. Nelson, C. A., Viner, N. J., Young, S. P., Petzold, S. J. and Unanue, E. R., A negatively charged anchor residue promotes high affinity binding to the MHC class II molecule I-Ak. J. Immunol. 1996. 157: 755-762.
58. Murray, J. S., Madri, J., Pasqualini, T. and Bottomly, K., Functional CD4 T cell subset interplay in an intact immune system. J. Immunol. 1993. 150: 4270-4276.
59. Murray, J. S., Pfeiffer, C., Madri, J. and Bottomly, K., Major histocompatibility complex (MHC) control of CD4 T cell subset activation. II. A single peptide induces either humoral or cell-mediated responses in mice of distinct MHC genotype. Eur. J. Immunol. 1992. 22: 559-565.
60. Pfeiffer, C., Murray, J., Madri, J. and Bottomly, K., Selective activation of Th1- and Th2-like cells in vivo-response to human collagen IV. Immunol. Rev. 1991. 123: 65-84.
61. + T cell subset activation. J. Exp. Med. 1989. 170: 2135-2140.
62. Bhardwaj, V., Kumar, V., Geysen, H. M. and Sercarz, E. E., Subjugation of dominant immunogenic determinants within a chimeric peptide. Eur. J. Immunol. 1992. 22: 2009-2016.
63. Adewusi, O. I., Nix, N. A., Lu, X., Colley, D. G. and Secor, W. E., Schistosoma mansoni: relationship of tumor necrosis factor-alpha to morbidity and collagen deposition in chronic experimental infection. Exp. Parasitol. 1996. 84: 115-123.
64. Bosshardt, S. C., Freeman, G. L., Jr., Secor, W. E. and Colley, D. G., IL-10 deficit correlates with chronic, hypersplenomegaly syndrome in male CBA/J mice infected with Schistosoma mansoni. Parasite Immunol. 1997. 19: 347-353.
65. Reiner, S. L., Fowell, D. J., Moskowitz, N. H., Swier, K., Brown, D. R., Brown, C. R., Turck, C. W. et al., Control of Leishmania major by a monoclonal alpha beta T cell repertoire. J. Immunol. 1998. 160: 884-889.
66. Sun, J. B., Stadecker, M. J., Mielcarek, N., Lakew, M., Li, B. L., Hernandez, H. J., Czerkinsky, C. and Holmgren, J., Nasal administration of Schistosoma mansoni egg antigen-cholera B subunit conjugate suppresses hepatic granuloma formation and reduces mortality in S. mansoni-infected mice. Scand. J. Immunol. 2001. 54: 440-447.
67. Hernandez, H. J., Rutitzky, L. I., Lebens, M., Holmgren, J. and Stadecker, M. J., Diminished immunopathology in Schistosoma mansoni infection following intranasal administration of cholera toxin B-immunodominant peptide conjugate correlates with enhanced transforming growth factor-beta production by CD4 T cells. Parasite Immunol. 2002. 24: 423-427.
68. Brown, C. R. and Reiner, S. L., Genes outside the major histocompatibility complex control resistance and susceptibility to experimental Lyme arthritis. Med. Microbiol. Immunol. (Berl) 2000. 189: 85-90.
69. Trischmann, T. M. and Bloom, B. R., Genetics of murine resistance to Trypanosoma cruzi. Infect. Immun. 1982. 35: 546-551.
70. Boros, D. L. and Warren, K. S., Delayed hypersensitivity-type granuloma formation and dermal reaction induced and elicited by a soluble factor isolated from Schistosoma mansoni eggs. J. Exp. Med. 1970. 132: 488-507.
71. Rutitzky, L. I., Hernandez, H. J. and Stadecker, M. J., Th1-polarizing immunization with egg antigens correlates with severe exacerbation of immunopathology and death in schistosome infection. Proc. Natl. Acad. Sci. USA 2001. 98: 13243-13248.