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Published in: BMC Immunology 1/2010

Open Access 01-12-2010 | Research article

Rapid induction of IgE responses to a worm cysteine protease during murine pre-patent schistosome infection

Authors: Lucia A de Oliveira Fraga, Erika W Lamb, Elizabeth C Moreno, Mitali Chatterjee, Jan Dvořák, Melaine Delcroix, Mohammed Sajid, Conor R Caffrey, Stephen J Davies

Published in: BMC Immunology | Issue 1/2010

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Abstract

Background

During the pre-patent stage of infection, juvenile Schistosoma blood flukes co-opt signals from the adaptive immune system to facilitate parasite development, but the types of responses that are induced at this early stage of infection, and the parasite antigens they target, have not been characterized.

Results

Through analysis of experimental pre-patent infections, we show that the S. mansoni cysteine protease SmCB1 is rapidly targeted by an antigen-specific IgE response. The induction of this response is independent of schistosome eggs as infection with male or female worms alone also induced SmCB1-specific IgE. We also show that the SmCB1-specific IgE response is dependent on cognate CD4+ T cell help and IL-4, suggesting that pre-patent Th2 responses provide T cell help for the SmCB1-specific IgE response. Finally, exposed human subjects also produced IgE against SmCB1.

Conclusions

Our data demonstrate that, like eggs, schistosome worms also induce functional type 2 responses and that a parasite cysteine protease is an inducer of type 2 responses during the early stages of schistosome infection.
Appendix
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Literature
1.
go back to reference Pearce EJ, Sher A: Mechanisms of immune evasion in schistosomiasis. Contrib Microbiol Immunol. 1987, 8: 219-232.PubMed Pearce EJ, Sher A: Mechanisms of immune evasion in schistosomiasis. Contrib Microbiol Immunol. 1987, 8: 219-232.PubMed
3.
go back to reference Hewitson JP, Hamblin PA, Mountford AP: Immunity induced by the radiation-attenuated schistosome vaccine. Parasite Immunol. 2005, 27: 271-280. 10.1111/j.1365-3024.2005.00764.x.CrossRefPubMed Hewitson JP, Hamblin PA, Mountford AP: Immunity induced by the radiation-attenuated schistosome vaccine. Parasite Immunol. 2005, 27: 271-280. 10.1111/j.1365-3024.2005.00764.x.CrossRefPubMed
4.
go back to reference Davies SJ, Grogan JL, Blank RB, Lim KC, Locksley RM, McKerrow JH: Modulation of Blood Fluke Development in the Liver by Hepatic CD4+ Lymphocytes. Science. 2001, 294: 1358-1361. 10.1126/science.1064462.CrossRefPubMed Davies SJ, Grogan JL, Blank RB, Lim KC, Locksley RM, McKerrow JH: Modulation of Blood Fluke Development in the Liver by Hepatic CD4+ Lymphocytes. Science. 2001, 294: 1358-1361. 10.1126/science.1064462.CrossRefPubMed
5.
go back to reference Harrison RA, Doenhoff MJ: Retarded development of Schistosoma mansoni in immunosuppressed mice. Parasitology. 1983, 86: 429-438. 10.1017/S0031182000050629.CrossRefPubMed Harrison RA, Doenhoff MJ: Retarded development of Schistosoma mansoni in immunosuppressed mice. Parasitology. 1983, 86: 429-438. 10.1017/S0031182000050629.CrossRefPubMed
6.
go back to reference Pearce EJ: Priming of the immune response by schistosome eggs. Parasite Immunol. 2005, 27: 265-270. 10.1111/j.1365-3024.2005.00765.x.CrossRefPubMed Pearce EJ: Priming of the immune response by schistosome eggs. Parasite Immunol. 2005, 27: 265-270. 10.1111/j.1365-3024.2005.00765.x.CrossRefPubMed
7.
go back to reference Grzych JM, Pearce E, Cheever A, Caulada ZA, Caspar P, Heiny S, Lewis F, Sher A: Egg deposition is the major stimulus for the production of Th2 cytokines in murine schistosomiasis mansoni. J Immunol. 1991, 146: 1322-1327.PubMed Grzych JM, Pearce E, Cheever A, Caulada ZA, Caspar P, Heiny S, Lewis F, Sher A: Egg deposition is the major stimulus for the production of Th2 cytokines in murine schistosomiasis mansoni. J Immunol. 1991, 146: 1322-1327.PubMed
8.
go back to reference Stadecker MJ, Hernandez HJ, 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.PubMed Stadecker MJ, Hernandez HJ, 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.PubMed
9.
go back to reference Chen Y, Boros DL: Identification of the immunodominant T cell epitope of p38, a major egg antigen, and characterization of the epitope-specific Th responsiveness during murine schistosomiasis mansoni. J Immunol. 1998, 160: 5420-5427.PubMed Chen Y, Boros DL: Identification of the immunodominant T cell epitope of p38, a major egg antigen, and characterization of the epitope-specific Th responsiveness during murine schistosomiasis mansoni. J Immunol. 1998, 160: 5420-5427.PubMed
10.
go back to reference Hernandez HJ, Edson CM, Harn DA, Ianelli CJ, Stadecker MJ: Schistosoma mansoni: genetic restriction and cytokine profile of the CD4 + T helper cell response to dominant epitope peptide of major egg antigen Sm-p40. Exp Parasitol. 1998, 90: 122-130. 10.1006/expr.1998.4309.CrossRefPubMed Hernandez HJ, Edson CM, Harn DA, Ianelli CJ, Stadecker MJ: Schistosoma mansoni: genetic restriction and cytokine profile of the CD4 + T helper cell response to dominant epitope peptide of major egg antigen Sm-p40. Exp Parasitol. 1998, 90: 122-130. 10.1006/expr.1998.4309.CrossRefPubMed
11.
go back to reference Everts B, Perona-Wright G, Smits HH, Hokke CH, van der Ham AJ, Fitzsimmons CM, Doenhoff MJ, van der Bosch J, Mohrs K, Haas H, et al.,: Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. J Exp Med. 2009, 206: 1673-1680. 10.1084/jem.20082460.PubMedCentralCrossRefPubMed Everts B, Perona-Wright G, Smits HH, Hokke CH, van der Ham AJ, Fitzsimmons CM, Doenhoff MJ, van der Bosch J, Mohrs K, Haas H, et al.,: Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. J Exp Med. 2009, 206: 1673-1680. 10.1084/jem.20082460.PubMedCentralCrossRefPubMed
12.
go back to reference Steinfelder S, Andersen JF, Cannons JL, Feng CG, Joshi M, Dwyer D, Caspar P, Schwartzberg PL, Sher A, Jankovic D: The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1). J Exp Med. 2009, 206: 1681-1690. 10.1084/jem.20082462.PubMedCentralCrossRefPubMed Steinfelder S, Andersen JF, Cannons JL, Feng CG, Joshi M, Dwyer D, Caspar P, Schwartzberg PL, Sher A, Jankovic D: The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1). J Exp Med. 2009, 206: 1681-1690. 10.1084/jem.20082462.PubMedCentralCrossRefPubMed
13.
go back to reference Pearce EJ, Caspar P, Grzych JM, Lewis FA, 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. 10.1084/jem.173.1.159.CrossRefPubMed Pearce EJ, Caspar P, Grzych JM, Lewis FA, 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. 10.1084/jem.173.1.159.CrossRefPubMed
14.
go back to reference de Oliveira Fraga LA, Torrero MN, Tocheva AS, Mitre E, Davies SJ: Induction of type 2 responses by schistosome worms during prepatent infection. J Infect Dis. 2010, 201: 464-472. 10.1086/649841.PubMedCentralCrossRefPubMed de Oliveira Fraga LA, Torrero MN, Tocheva AS, Mitre E, Davies SJ: Induction of type 2 responses by schistosome worms during prepatent infection. J Infect Dis. 2010, 201: 464-472. 10.1086/649841.PubMedCentralCrossRefPubMed
15.
go back to reference Balloul JM, Sondermeyer P, Dreyer D, Capron M, Grzych JM, Pierce RJ, Carvallo D, Lecocq JP, Capron A: Molecular cloning of a protective antigen of schistosomes. Nature. 1987, 326: 149-153. 10.1038/326149a0.CrossRefPubMed Balloul JM, Sondermeyer P, Dreyer D, Capron M, Grzych JM, Pierce RJ, Carvallo D, Lecocq JP, Capron A: Molecular cloning of a protective antigen of schistosomes. Nature. 1987, 326: 149-153. 10.1038/326149a0.CrossRefPubMed
16.
go back to reference Pearce EJ, James SL, Dalton J, Barrall A, Ramos C, Strand M, Sher A: Immunochemical characterization and purification of Sm-97, a Schistosoma mansoni antigen monospecifically recognized by antibodies from mice protectively immunized with a nonliving vaccine. J Immunol. 1986, 137: 3593-3600.PubMed Pearce EJ, James SL, Dalton J, Barrall A, Ramos C, Strand M, Sher A: Immunochemical characterization and purification of Sm-97, a Schistosoma mansoni antigen monospecifically recognized by antibodies from mice protectively immunized with a nonliving vaccine. J Immunol. 1986, 137: 3593-3600.PubMed
17.
go back to reference Strand M, Dalton JP, Tom TD: Characterization and cloning of Schistosoma mansoni immunogens recognized by protective antibodies. Acta Trop Suppl. 1987, 12: 75-82.PubMed Strand M, Dalton JP, Tom TD: Characterization and cloning of Schistosoma mansoni immunogens recognized by protective antibodies. Acta Trop Suppl. 1987, 12: 75-82.PubMed
18.
go back to reference Correa-Oliveira R, Pearce EJ, Oliveira GC, Golgher DB, Katz N, Bahia LG, Carvalho OS, Gazzinelli G, Sher A: The human immune response to defined immunogens of Schistosoma mansoni: elevated antibody levels to paramyosin in stool-negative individuals from two endemic areas in Brazil. Trans R Soc Trop Med Hyg. 1989, 83: 798-804. 10.1016/0035-9203(89)90334-9.CrossRefPubMed Correa-Oliveira R, Pearce EJ, Oliveira GC, Golgher DB, Katz N, Bahia LG, Carvalho OS, Gazzinelli G, Sher A: The human immune response to defined immunogens of Schistosoma mansoni: elevated antibody levels to paramyosin in stool-negative individuals from two endemic areas in Brazil. Trans R Soc Trop Med Hyg. 1989, 83: 798-804. 10.1016/0035-9203(89)90334-9.CrossRefPubMed
19.
go back to reference El Ridi R, Farouk F, Sherif M, Al-Sherbiny M, Osman A, El Gengehi N, Shoemaker CB: T and B cell reactivity to a 42-kDa protein is associated with human resistance to both schistosomiasis mansoni and haematobium. J Infect Dis. 1998, 177: 1364-1372. 10.1086/515274.CrossRefPubMed El Ridi R, Farouk F, Sherif M, Al-Sherbiny M, Osman A, El Gengehi N, Shoemaker CB: T and B cell reactivity to a 42-kDa protein is associated with human resistance to both schistosomiasis mansoni and haematobium. J Infect Dis. 1998, 177: 1364-1372. 10.1086/515274.CrossRefPubMed
20.
go back to reference Goudot-Crozel V, Caillol D, Djabali M, Dessein AJ: The major parasite surface antigen associated with human resistance to schistosomiasis is a 37-kD glyceraldehyde-3P-dehydrogenase. J Exp Med. 1989, 170: 2065-2080. 10.1084/jem.170.6.2065.CrossRefPubMed Goudot-Crozel V, Caillol D, Djabali M, Dessein AJ: The major parasite surface antigen associated with human resistance to schistosomiasis is a 37-kD glyceraldehyde-3P-dehydrogenase. J Exp Med. 1989, 170: 2065-2080. 10.1084/jem.170.6.2065.CrossRefPubMed
21.
go back to reference Kearney ER, Pape KA, Loh DY, Jenkins MK: Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo. Immunity. 1994, 1: 327-339. 10.1016/1074-7613(94)90084-1.CrossRefPubMed Kearney ER, Pape KA, Loh DY, Jenkins MK: Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo. Immunity. 1994, 1: 327-339. 10.1016/1074-7613(94)90084-1.CrossRefPubMed
22.
go back to reference Kawabe T, Naka T, Yoshida K, Tanaka T, Fujiwara H, Suematsu S, Yoshida N, Kishimoto T, Kikutani H: The immune responses in CD40-deficient mice: impaired immunoglobulin class switching and germinal center formation. Immunity. 1994, 1: 167-178. 10.1016/1074-7613(94)90095-7.CrossRefPubMed Kawabe T, Naka T, Yoshida K, Tanaka T, Fujiwara H, Suematsu S, Yoshida N, Kishimoto T, Kikutani H: The immune responses in CD40-deficient mice: impaired immunoglobulin class switching and germinal center formation. Immunity. 1994, 1: 167-178. 10.1016/1074-7613(94)90095-7.CrossRefPubMed
23.
go back to reference Caffrey CR, McKerrow JH, Salter JP, Sajid M: Blood 'n' guts: an update on schistosome digestive peptidases. Trends Parasitol. 2004, 20: 241-248. 10.1016/j.pt.2004.03.004.CrossRefPubMed Caffrey CR, McKerrow JH, Salter JP, Sajid M: Blood 'n' guts: an update on schistosome digestive peptidases. Trends Parasitol. 2004, 20: 241-248. 10.1016/j.pt.2004.03.004.CrossRefPubMed
24.
go back to reference Chappell CL, Hackel J, Davis AH: Cloned Schistosoma mansoni proteinase (hemoglobinase) as a putative serodiagnostic reagent. J Clin Microbiol. 1989, 27: 196-198.PubMedCentralPubMed Chappell CL, Hackel J, Davis AH: Cloned Schistosoma mansoni proteinase (hemoglobinase) as a putative serodiagnostic reagent. J Clin Microbiol. 1989, 27: 196-198.PubMedCentralPubMed
25.
go back to reference Grogan J, Rotmans P, Ghoneim H, Deelder A, Yazdanbakhsh M, Klinkert MQ: Recognition of Schistosoma mansoni cathepsins B and L by human IgG1 and IgG4 antibodies. Parasite Immunol. 1997, 19: 215-220. 10.1046/j.1365-3024.1997.d01-199.x.CrossRefPubMed Grogan J, Rotmans P, Ghoneim H, Deelder A, Yazdanbakhsh M, Klinkert MQ: Recognition of Schistosoma mansoni cathepsins B and L by human IgG1 and IgG4 antibodies. Parasite Immunol. 1997, 19: 215-220. 10.1046/j.1365-3024.1997.d01-199.x.CrossRefPubMed
26.
go back to reference Klinkert MQ, Bommert K, Moser D, Felleisen R, Link G, Doumbo O, Beck E: Immunological analysis of cloned Schistosoma mansoni antigens Sm31 and Sm32 with sera of schistosomiasis patients. Trop Med Parasitol. 1991, 42: 319-324.PubMed Klinkert MQ, Bommert K, Moser D, Felleisen R, Link G, Doumbo O, Beck E: Immunological analysis of cloned Schistosoma mansoni antigens Sm31 and Sm32 with sera of schistosomiasis patients. Trop Med Parasitol. 1991, 42: 319-324.PubMed
27.
go back to reference Chappell CL, Dresden MH: Antibody response to a purified parasite proteinase (SMw32) in Schistosoma mansoni infected mice. Am J Trop Med Hyg. 1988, 39: 66-73.PubMed Chappell CL, Dresden MH: Antibody response to a purified parasite proteinase (SMw32) in Schistosoma mansoni infected mice. Am J Trop Med Hyg. 1988, 39: 66-73.PubMed
28.
go back to reference Vercelli D, Jabara HH, Arai K, Geha RS: Induction of human IgE synthesis requires interleukin 4 and T/B cell interactions involving the T cell receptor/CD3 complex and MHC class II antigens. J Exp Med. 1989, 169: 1295-1307. 10.1084/jem.169.4.1295.CrossRefPubMed Vercelli D, Jabara HH, Arai K, Geha RS: Induction of human IgE synthesis requires interleukin 4 and T/B cell interactions involving the T cell receptor/CD3 complex and MHC class II antigens. J Exp Med. 1989, 169: 1295-1307. 10.1084/jem.169.4.1295.CrossRefPubMed
29.
go back to reference LoVerde PT, Chen L: Schistosome female reproductive development. Parasitology Today. 1991, 7: 303-307. 10.1016/0169-4758(91)90263-N.CrossRefPubMed LoVerde PT, Chen L: Schistosome female reproductive development. Parasitology Today. 1991, 7: 303-307. 10.1016/0169-4758(91)90263-N.CrossRefPubMed
30.
go back to reference McCoy KD, Harris NL, Diener P, Hatak S, Odermatt B, Hangartner L, Senn BM, Marsland BJ, Geuking MB, Hengartner H, et al.,: Natural IgE production in the absence of MHC Class II cognate help. Immunity. 2006, 24: 329-339. 10.1016/j.immuni.2006.01.013.CrossRefPubMed McCoy KD, Harris NL, Diener P, Hatak S, Odermatt B, Hangartner L, Senn BM, Marsland BJ, Geuking MB, Hengartner H, et al.,: Natural IgE production in the absence of MHC Class II cognate help. Immunity. 2006, 24: 329-339. 10.1016/j.immuni.2006.01.013.CrossRefPubMed
31.
go back to reference Hagan P, Blumenthal UJ, Dunn D, Simpson AJ, Wilkins HA: Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature. 1991, 349: 243-245. 10.1038/349243a0.CrossRefPubMed Hagan P, Blumenthal UJ, Dunn D, Simpson AJ, Wilkins HA: Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature. 1991, 349: 243-245. 10.1038/349243a0.CrossRefPubMed
32.
go back to reference Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, Cerqueira GC, Mashiyama ST, Al-Lazikani B, Andrade LF, Ashton PD, et al.,: The genome of the blood fluke Schistosoma mansoni. Nature. 2009, 460: 352-358. 10.1038/nature08160.PubMedCentralCrossRefPubMed Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, Cerqueira GC, Mashiyama ST, Al-Lazikani B, Andrade LF, Ashton PD, et al.,: The genome of the blood fluke Schistosoma mansoni. Nature. 2009, 460: 352-358. 10.1038/nature08160.PubMedCentralCrossRefPubMed
33.
go back to reference Jolly ER, Chin CS, Miller S, Bahgat MM, Lim KC, DeRisi J, McKerrow JH: Gene expression patterns during adaptation of a helminth parasite to different environmental niches. Genome Biol. 2007, 8: R65-10.1186/gb-2007-8-4-r65.PubMedCentralCrossRefPubMed Jolly ER, Chin CS, Miller S, Bahgat MM, Lim KC, DeRisi J, McKerrow JH: Gene expression patterns during adaptation of a helminth parasite to different environmental niches. Genome Biol. 2007, 8: R65-10.1186/gb-2007-8-4-r65.PubMedCentralCrossRefPubMed
34.
go back to reference Mikhail MM, Mansour MM, Farid Z, Harrison R: Schistosoma mansoni antigens applicable to diagnosis of prepatent infections. J Egypt Soc Parasitol. 1997, 27: 1-20.PubMed Mikhail MM, Mansour MM, Farid Z, Harrison R: Schistosoma mansoni antigens applicable to diagnosis of prepatent infections. J Egypt Soc Parasitol. 1997, 27: 1-20.PubMed
35.
go back to reference Klinkert MQ, Felleisen R, Link G, Ruppel A, Beck E: Primary structures of Sm31/32 diagnostic proteins of Schistosoma mansoni and their identification as proteases. Mol Biochem Parasitol. 1989, 33: 113-122. 10.1016/0166-6851(89)90025-X.CrossRefPubMed Klinkert MQ, Felleisen R, Link G, Ruppel A, Beck E: Primary structures of Sm31/32 diagnostic proteins of Schistosoma mansoni and their identification as proteases. Mol Biochem Parasitol. 1989, 33: 113-122. 10.1016/0166-6851(89)90025-X.CrossRefPubMed
36.
go back to reference Skelly PJ, Shoemaker CB: Schistosoma mansoni proteases Sm31 (cathepsin B) and Sm32 (legumain) are expressed in the cecum and protonephridia of cercariae. J Parasitol. 2001, 87: 1218-1221.CrossRefPubMed Skelly PJ, Shoemaker CB: Schistosoma mansoni proteases Sm31 (cathepsin B) and Sm32 (legumain) are expressed in the cecum and protonephridia of cercariae. J Parasitol. 2001, 87: 1218-1221.CrossRefPubMed
37.
go back to reference Štefanić S, Dvořák J, Horn M, Braschi S, Sojka D, Ruelas D, Suzuki B, Lim KC, Hopkins SD, McKerrow JH, Caffrey CR: RNA interference in Schistosoma mansoni schistosomula: selectivity, sensitivity and operation for larger-scale screening. PLoS Negl Trop Dis. 2010, Štefanić S, Dvořák J, Horn M, Braschi S, Sojka D, Ruelas D, Suzuki B, Lim KC, Hopkins SD, McKerrow JH, Caffrey CR: RNA interference in Schistosoma mansoni schistosomula: selectivity, sensitivity and operation for larger-scale screening. PLoS Negl Trop Dis. 2010,
38.
go back to reference Correnti JM, Brindley PJ, Pearce EJ: Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth. Mol Biochem Parasitol. 2005, 143: 209-215. 10.1016/j.molbiopara.2005.06.007.CrossRefPubMed Correnti JM, Brindley PJ, Pearce EJ: Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth. Mol Biochem Parasitol. 2005, 143: 209-215. 10.1016/j.molbiopara.2005.06.007.CrossRefPubMed
39.
go back to reference Abdulla MH, Lim KC, Sajid M, McKerrow JH, Caffrey CR: Schistosomiasis mansoni: novel chemotherapy using a cysteine protease inhibitor. PLoS Med. 2007, 4: e14-10.1371/journal.pmed.0040014.PubMedCentralCrossRefPubMed Abdulla MH, Lim KC, Sajid M, McKerrow JH, Caffrey CR: Schistosomiasis mansoni: novel chemotherapy using a cysteine protease inhibitor. PLoS Med. 2007, 4: e14-10.1371/journal.pmed.0040014.PubMedCentralCrossRefPubMed
40.
go back to reference Medzhitov R: Origin and physiological roles of inflammation. Nature. 2008, 454: 428-435. 10.1038/nature07201.CrossRefPubMed Medzhitov R: Origin and physiological roles of inflammation. Nature. 2008, 454: 428-435. 10.1038/nature07201.CrossRefPubMed
41.
go back to reference Sokol CL, Barton GM, Farr AG, Medzhitov R: A mechanism for the initiation of allergen-induced T helper type 2 responses. Nat Immunol. 2008, 9: 310-318. 10.1038/ni1558.PubMedCentralCrossRefPubMed Sokol CL, Barton GM, Farr AG, Medzhitov R: A mechanism for the initiation of allergen-induced T helper type 2 responses. Nat Immunol. 2008, 9: 310-318. 10.1038/ni1558.PubMedCentralCrossRefPubMed
42.
go back to reference Lecaille F, Kaleta J, Bromme D: Human and parasitic papain-like cysteine proteases: their role in physiology and pathology and recent developments in inhibitor design. Chem Rev. 2002, 102: 4459-4488. 10.1021/cr0101656.CrossRefPubMed Lecaille F, Kaleta J, Bromme D: Human and parasitic papain-like cysteine proteases: their role in physiology and pathology and recent developments in inhibitor design. Chem Rev. 2002, 102: 4459-4488. 10.1021/cr0101656.CrossRefPubMed
43.
go back to reference McKerrow JH: Cysteine proteases of parasites: A remarkable diversity of function. Perspectives in Drug Discovery and Design. 1994, 2: 437-444. 10.1007/BF02172036.CrossRef McKerrow JH: Cysteine proteases of parasites: A remarkable diversity of function. Perspectives in Drug Discovery and Design. 1994, 2: 437-444. 10.1007/BF02172036.CrossRef
44.
go back to reference McMichael AJ, Phillips RE: Escape of human immunodeficiency virus from immune control. Annu Rev Immunol. 1997, 15: 271-296. 10.1146/annurev.immunol.15.1.271.CrossRefPubMed McMichael AJ, Phillips RE: Escape of human immunodeficiency virus from immune control. Annu Rev Immunol. 1997, 15: 271-296. 10.1146/annurev.immunol.15.1.271.CrossRefPubMed
45.
go back to reference Suzuki Y: Natural selection on the influenza virus genome. Mol Biol Evol. 2006, 23: 1902-1911. 10.1093/molbev/msl050.CrossRefPubMed Suzuki Y: Natural selection on the influenza virus genome. Mol Biol Evol. 2006, 23: 1902-1911. 10.1093/molbev/msl050.CrossRefPubMed
46.
go back to reference Cooreman MP, Leroux-Roels G, Paulij WP: Vaccine- and hepatitis B immune globulin-induced escape mutations of hepatitis B virus surface antigen. J Biomed Sci. 2001, 8: 237-247. 10.1007/BF02256597.CrossRefPubMed Cooreman MP, Leroux-Roels G, Paulij WP: Vaccine- and hepatitis B immune globulin-induced escape mutations of hepatitis B virus surface antigen. J Biomed Sci. 2001, 8: 237-247. 10.1007/BF02256597.CrossRefPubMed
47.
go back to reference Sternberg JM: Human African trypanosomiasis: clinical presentation and immune response. Parasite Immunol. 2004, 26: 469-476. 10.1111/j.0141-9838.2004.00731.x.CrossRefPubMed Sternberg JM: Human African trypanosomiasis: clinical presentation and immune response. Parasite Immunol. 2004, 26: 469-476. 10.1111/j.0141-9838.2004.00731.x.CrossRefPubMed
48.
go back to reference Martin DL, Weatherly DB, Laucella SA, Cabinian MA, Crim MT, Sullivan S, Heiges M, Craven SH, Rosenberg CS, Collins MH, et al.,: CD8+ T-Cell responses to Trypanosoma cruzi are highly focused on strain-variant trans-sialidase epitopes. PLoS Pathog. 2006, 2: e77-10.1371/journal.ppat.0020077.PubMedCentralCrossRefPubMed Martin DL, Weatherly DB, Laucella SA, Cabinian MA, Crim MT, Sullivan S, Heiges M, Craven SH, Rosenberg CS, Collins MH, et al.,: CD8+ T-Cell responses to Trypanosoma cruzi are highly focused on strain-variant trans-sialidase epitopes. PLoS Pathog. 2006, 2: e77-10.1371/journal.ppat.0020077.PubMedCentralCrossRefPubMed
49.
go back to reference Jung C, Lee CY, Grigg ME: The SRS superfamily of Toxoplasma surface proteins. Int J Parasitol. 2004, 34: 285-296. 10.1016/j.ijpara.2003.12.004.CrossRefPubMed Jung C, Lee CY, Grigg ME: The SRS superfamily of Toxoplasma surface proteins. Int J Parasitol. 2004, 34: 285-296. 10.1016/j.ijpara.2003.12.004.CrossRefPubMed
50.
go back to reference Lamb EW, Walls CD, Pesce JT, Riner DK, Maynard SK, Crow ET, Wynn TA, Schaefer BC, Davies SJ: Blood fluke exploitation of non-cognate CD4+ T cell help to facilitate parasite development. PLoS Pathog. 2010, 6: e1000892-10.1371/journal.ppat.1000892.PubMedCentralCrossRefPubMed Lamb EW, Walls CD, Pesce JT, Riner DK, Maynard SK, Crow ET, Wynn TA, Schaefer BC, Davies SJ: Blood fluke exploitation of non-cognate CD4+ T cell help to facilitate parasite development. PLoS Pathog. 2010, 6: e1000892-10.1371/journal.ppat.1000892.PubMedCentralCrossRefPubMed
51.
go back to reference Delcroix M, Medzihradsky K, Caffrey CR, Fetter RD, McKerrow JH: Proteomic analysis of adult S. mansoni gut contents. Mol Biochem Parasitol. 2007, 154: 95-97. 10.1016/j.molbiopara.2007.03.008.PubMedCentralCrossRefPubMed Delcroix M, Medzihradsky K, Caffrey CR, Fetter RD, McKerrow JH: Proteomic analysis of adult S. mansoni gut contents. Mol Biochem Parasitol. 2007, 154: 95-97. 10.1016/j.molbiopara.2007.03.008.PubMedCentralCrossRefPubMed
52.
go back to reference Merckelbach A, Hasse S, Dell R, Eschlbeck A, Ruppel A: cDNA sequences of Schistosoma japonicum coding for two cathepsin B-like proteins and Sj32. Trop Med Parasitol. 1994, 45: 193-198.PubMed Merckelbach A, Hasse S, Dell R, Eschlbeck A, Ruppel A: cDNA sequences of Schistosoma japonicum coding for two cathepsin B-like proteins and Sj32. Trop Med Parasitol. 1994, 45: 193-198.PubMed
53.
go back to reference Lichtenbergova L, Kolbekova P, Kourilova P, Kasny M, Mikes L, Haas H, Schramm G, Horak P, Kolarova L, Mountford AP: Antibody responses induced by Trichobilharzia regenti antigens in murine and human hosts exhibiting cercarial dermatitis. Parasite Immunol. 2008, 30: 585-595.PubMedCentralPubMed Lichtenbergova L, Kolbekova P, Kourilova P, Kasny M, Mikes L, Haas H, Schramm G, Horak P, Kolarova L, Mountford AP: Antibody responses induced by Trichobilharzia regenti antigens in murine and human hosts exhibiting cercarial dermatitis. Parasite Immunol. 2008, 30: 585-595.PubMedCentralPubMed
54.
go back to reference Leptak CL, McKerrow JH: Schistosome egg granulomas and hepatic expression of TNF-alpha are dependent on immune priming during parasite maturation. J Immunol. 1997, 158: 301-307.PubMed Leptak CL, McKerrow JH: Schistosome egg granulomas and hepatic expression of TNF-alpha are dependent on immune priming during parasite maturation. J Immunol. 1997, 158: 301-307.PubMed
55.
go back to reference Rihet P, Demeure CE, Bourgois A, Prata A, Dessein AJ: Evidence for an association between human resistance to Schistosoma mansoni and high anti-larval IgE levels. Eur J Immunol. 1991, 21: 2679-2686. 10.1002/eji.1830211106.CrossRefPubMed Rihet P, Demeure CE, Bourgois A, Prata A, Dessein AJ: Evidence for an association between human resistance to Schistosoma mansoni and high anti-larval IgE levels. Eur J Immunol. 1991, 21: 2679-2686. 10.1002/eji.1830211106.CrossRefPubMed
56.
go back to reference Ganley-Leal LM, Mwinzi PN, Cetre-Sossah CB, Andove J, Hightower AW, Karanja DM, Colley DG, Secor WE: Correlation between eosinophils and protection against reinfection with Schistosoma mansoni and the effect of human immunodeficiency virus type 1 coinfection in humans. Infect Immun. 2006, 74: 2169-2176. 10.1128/IAI.74.4.2169-2176.2006.PubMedCentralCrossRefPubMed Ganley-Leal LM, Mwinzi PN, Cetre-Sossah CB, Andove J, Hightower AW, Karanja DM, Colley DG, Secor WE: Correlation between eosinophils and protection against reinfection with Schistosoma mansoni and the effect of human immunodeficiency virus type 1 coinfection in humans. Infect Immun. 2006, 74: 2169-2176. 10.1128/IAI.74.4.2169-2176.2006.PubMedCentralCrossRefPubMed
57.
go back to reference Nyindo M, Kariuki TM, Mola PW, Farah IO, Elson L, Blanton RE, King CL: Role of adult worm antigen-specific immunoglobulin E in acquired immunity to Schistosoma mansoni infection in baboons. Infect Immun. 1999, 67: 636-642.PubMedCentralPubMed Nyindo M, Kariuki TM, Mola PW, Farah IO, Elson L, Blanton RE, King CL: Role of adult worm antigen-specific immunoglobulin E in acquired immunity to Schistosoma mansoni infection in baboons. Infect Immun. 1999, 67: 636-642.PubMedCentralPubMed
58.
go back to reference Correa-Oliveira R, Caldas IR, Gazzinelli G: Natural versus drug-induced resistance in Schistosoma mansoni infection. Parasitol Today. 2000, 16: 397-399. 10.1016/S0169-4758(00)01740-3.CrossRefPubMed Correa-Oliveira R, Caldas IR, Gazzinelli G: Natural versus drug-induced resistance in Schistosoma mansoni infection. Parasitol Today. 2000, 16: 397-399. 10.1016/S0169-4758(00)01740-3.CrossRefPubMed
59.
go back to reference Wynn TA, Hoffmann KF: Defining a schistosomiasis vaccination strategy - is it really Th1 versus Th2?. Parasitol Today. 2000, 16: 497-501. 10.1016/S0169-4758(00)01788-9.CrossRefPubMed Wynn TA, Hoffmann KF: Defining a schistosomiasis vaccination strategy - is it really Th1 versus Th2?. Parasitol Today. 2000, 16: 497-501. 10.1016/S0169-4758(00)01788-9.CrossRefPubMed
60.
go back to reference Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE: Helminth parasites--masters of regulation. Immunol Rev. 2004, 201: 89-116. 10.1111/j.0105-2896.2004.00191.x.CrossRefPubMed Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE: Helminth parasites--masters of regulation. Immunol Rev. 2004, 201: 89-116. 10.1111/j.0105-2896.2004.00191.x.CrossRefPubMed
61.
go back to reference Tran MH, Pearson MS, Bethony JM, Smyth DJ, Jones MK, Duke M, Don TA, McManus DP, Correa-Oliveira R, Loukas A: Tetraspanins on the surface of Schistosoma mansoni are protective antigens against schistosomiasis. Nat Med. 2006, 12: 835-840. 10.1038/nm1430.CrossRefPubMed Tran MH, Pearson MS, Bethony JM, Smyth DJ, Jones MK, Duke M, Don TA, McManus DP, Correa-Oliveira R, Loukas A: Tetraspanins on the surface of Schistosoma mansoni are protective antigens against schistosomiasis. Nat Med. 2006, 12: 835-840. 10.1038/nm1430.CrossRefPubMed
62.
go back to reference Jankovic D, Aslund L, Oswald IP, Caspar P, Champion C, Pearce E, Coligan JE, Strand M, Sher A, James SL: Calpain is the target antigen of a Th1 clone that transfers protective immunity against Schistosoma mansoni. J Immunol. 1996, 157: 806-814.PubMed Jankovic D, Aslund L, Oswald IP, Caspar P, Champion C, Pearce E, Coligan JE, Strand M, Sher A, James SL: Calpain is the target antigen of a Th1 clone that transfers protective immunity against Schistosoma mansoni. J Immunol. 1996, 157: 806-814.PubMed
63.
go back to reference Sajid M, McKerrow JH, Hansell E, Mathieu MA, Lucas KD, Hsieh I, Greenbaum D, Bogyo M, Salter JP, Lim KC, et al.,: Functional expression and characterization of Schistosoma mansoni cathepsin B and its trans-activation by an endogenous asparaginyl endopeptidase. Mol Biochem Parasitol. 2003, 131: 65-75. 10.1016/S0166-6851(03)00194-4.CrossRefPubMed Sajid M, McKerrow JH, Hansell E, Mathieu MA, Lucas KD, Hsieh I, Greenbaum D, Bogyo M, Salter JP, Lim KC, et al.,: Functional expression and characterization of Schistosoma mansoni cathepsin B and its trans-activation by an endogenous asparaginyl endopeptidase. Mol Biochem Parasitol. 2003, 131: 65-75. 10.1016/S0166-6851(03)00194-4.CrossRefPubMed
Metadata
Title
Rapid induction of IgE responses to a worm cysteine protease during murine pre-patent schistosome infection
Authors
Lucia A de Oliveira Fraga
Erika W Lamb
Elizabeth C Moreno
Mitali Chatterjee
Jan Dvořák
Melaine Delcroix
Mohammed Sajid
Conor R Caffrey
Stephen J Davies
Publication date
01-12-2010
Publisher
BioMed Central
Published in
BMC Immunology / Issue 1/2010
Electronic ISSN: 1471-2172
DOI
https://doi.org/10.1186/1471-2172-11-56

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