Vaccination against filarial nematodes with irradiated larvae provides long-term protection against the third larval stage but not against subsequent life cycle stages

International Journal for Parasitology

Volumn 36, Issue 8, 2006, Pages 903-914

  Babayan, Simon A ^a,b   Attout, Tarik ^a   Harris, Anjanette ^b   Taylor, Matthew D ^b   Le Goff, Laetitia ^b   Vuong, Phat N ^c   Rénia, Laurent ^d   Allen, Judith E ^b   Bain, Odile ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c Hopital Saint Michel   (France)

^d INSTITUT COCHIN   (France)

Author keywords

Antibody; Cytokine; Filariasis; Litomosoides sigmodontis; Nematode; Vaccines

Indexed keywords

FILARIA VACCINE; LIVE VACCINE;

ANTIBODY; FILARIASIS; IMMUNIZATION; LARVAL DEVELOPMENT; LIFE CYCLE; NEMATODE; RODENT; VACCINATION;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ARTICLE; CLINICAL PROTOCOL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEVELOPMENTAL STAGE; EOSINOPHIL; FEMALE; FILARIASIS; GROWTH RATE; INFECTION CONTROL; INFECTION PREVENTION; INOCULATION; IRRADIATION; LARVAL DEVELOPMENT; LIFE CYCLE; LITOMOSOIDES SIGMODONTIS; LONG TERM CARE; LYMPH NODE; NONHUMAN; PLEURA CAVITY; PROVOCATION TEST; SUBCUTANEOUS TISSUE; TH2 CELL;

ANIMALS; ANTIBODIES, HELMINTH; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; EOSINOPHILS; FEMALE; FILARIASIS; FILARIOIDEA; FLOW CYTOMETRY; HUMANS; LARVA; LYMPH NODES; MICE; MICE, INBRED BALB C; PLEURAL CAVITY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, HELMINTH; STATISTICS, NONPARAMETRIC; VACCINATION; VACCINES;

ANIMALIA; LITOMOSOIDES SIGMODONTIS; MURINAE; NEMATODA;

EID: 33845245864     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2006.04.013     Document Type: Article

References (63)

1. Abraham D., Grieve R.B., Mika-Grieve M., and Seibert B.P. Active and passive immunization of mice against larval Dirofilaria immitis. J. Parasitol. 74 (1988) 275-282
2. Abraham D., Eberhard M.L., Lange A.M., Yutanawiboonchai W., Perler F.B., and Lok J.B. Identification of surrogate rodent hosts for larval Onchocerca lienalis and induction of protective immunity in a model system. J. Parasitol. 78 (1992) 447-453
3. Allen J.E., Daub J., Guiliano D., McDonnell A., Lizotte-Waniewski M., Taylor D.W., and Blaxter M. Analysis of genes expressed at the infective larval stage validates utility of Litomosoides sigmodontis as a murine model for filarial vaccine development. Infect. Immun. 68 (2000) 5454-5458
4. Attout, T., Martin, C., Kozek, W.J., Babayan, S.A., Bazzocchi, C., Oudet, F., Gallagher, I.J., Specht, S., Bain, O. Filarial granulomas in vivo: relations with moults, worm alteration and pleural leukocytes.
5. Babayan S., Ungeheuer M.N., Martin C., Attout T., Belnoue E., Snounou G., Renia L., Korenaga M., and Bain O. Resistance and susceptibility to filarial infection with Litomosoides sigmodontis are associated with early differences in parasite development and in localized immune reactions. Infect. Immun. 71 (2003) 6820-6829
6. Babayan S., Attout T., Specht S., Hoerauf A., Snounou G., Renia L., Korenaga M., Bain O., and Martin C. Increased early local immune responses and altered worm development in high-dose infections of mice susceptible to the filaria Litomosoides sigmodontis. Med. Microbiol. Immunol. (Berl.) 194 (2005) 151-162
7. Bain O., and Babayan S. Behaviour of filariae: morphological and anatomical signatures of their life style within the arthropod and vertebrate hosts. Filaria J. 2 (2003) 16
8. Bain O., Wanji S., Vuong P.N., Marechal P., Le Goff L., and Petit G. Larval biology of six filariae of the sub-family Onchocercinae in a vertebrate host. Parasite 1 (1994) 241-254
9. Bancroft A.J., Grencis R.K., Else K.J., and Devaney E. Cytokine production in BALB/c mice immunized with radiation attenuated third stage larvae of the filarial nematode, Brugia pahangi. J. Immunol. 150 (1993) 1395-1402
10. Chakir H., Wang H., Lefebvre D.E., Webb J., and Scott F.W. T-bet/GATA-3 ratio as a measure of the Th1/Th2 cytokine profile in mixed cell populations: predominant role of GATA-3. J. Immunol. Methods 278 (2003) 157-169
11. Chandler, A.C., 1931. New genera and species of nematode worms. Proceedings of the United States National Museum 78, 1-11.
12. Chusattayanond W., and Denham D.A. Attempted vaccination of jirds (Meriones unguiculatus) against Brugia pahangi with radiation attenuated infective larvae. J. Helminthol. 60 (1986) 149-155
13. Cooper P.J., Mancero T., Espinel M., Sandoval C., Lovato R., Guderian R.H., and Nutman T.B. Early human infection with Onchocerca volvulus is associated with an enhanced parasite-specific cellular immune response. J. Infect. Dis. 183 (2001) 1662-1668
14. Crawley, M.J., 2002. Analysis of variance. In: Statistical computing: an introduction to data analysis using S-Plus. Wiley, Chichester, pp. 243-279.
15. Denham D.A., McGreevy P.B., Suswillo R.R., and Rogers R. The resistance to re-infection of cats repeatedly inoculated with infective larvae of Brugia pahangi. Parasitology 86 (1983) 11-18
16. Denham D.A., Suswillo R.R., and Chusattayanond W. Parasitological observations on Meriones unguiculatus singly or multiply infected with Brugia pahangi. Parasitology 88 (1984) 295-301
17. Devaney E., and Osborne J. The third-stage larva (L3) of Brugia: its role in immune modulation and protective immunity. Microbes Infect. 2 (2000) 1363-1371
18. Diagne M., Petit G., Liot P., Cabaret J., and Bain O. The filaria Litomosoides galizai in mites; microfilarial distribution in the host and regulation of the transmission. Ann Parasitol Hum Comp 65 (1990) 193-199
19. Fenton A., Paterson S., Viney M.E., and Gardner M.P. Determining the optimal developmental route of Strongyloides ratti: an evolutionarily stable strategy approach. Evolution 58 (2004) 989-1000
20. Fischer P., Djoha S., Buttner D.W., and Zipfel P.F. Isolation and characterization of the regulatory subunit of cAMP-dependent protein kinase from the filarial parasite Onchocerca volvulus. Mol. Biochem. Parasitol. 128 (2003) 33-42
21. Ganley-Leal L.M., Guarner J., Todd C.W., Da'Dara A.A., Freeman Jr. G.L., Boyer A.E., Harn D.A., and Secor W.E. Comparison of Schistosoma mansoni irradiated cercariae and Sm23 DNA vaccines. Parasite Immunol. 27 (2005) 341-349
22. Gardon J., Gardon-Wendel N., Demanga N., Kamgno J., Chippaux J.P., and Boussinesq M. Serious reactions after mass treatment of onchocerciasis with ivermectin in an area endemic for Loa loa infection. Lancet 350 (1997) 18-22
23. Goyal P.K., and Wakelin D. Vaccination against Trichinella spiralis in mice using antigens from different isolates. Parasitology 107 (1993) 311-317
24. Gregory W.F., Atmadja A.K., Allen J.E., and Maizels R.M. The abundant larval transcript-1 and -2 genes of Brugia malayi encode stage-specific candidate vaccine antigens for filariasis. Infect. Immun. 68 (2000) 4174-4179
25. Guinnee M.A., Gemmill A.W., Chan B.H., Viney M.E., and Read A.F. Host immune status affects maturation time in two nematode species-but not as predicted by a simple life-history model. Parasitology 127 (2003) 507-512
26. Hoerauf A. Control of filarial infections: not the beginning of the end, but more research is needed. Curr. Opin. Infect. Dis. 16 (2003) 403-410
27. Hoerauf A., and Brattig N. Resistance and susceptibility in human onchocerciasis-beyond Th1 vs. Th2. Trends Parasitol. 18 (2002) 25-31
28. Ihaka R., and Gentleman R. R: a language for data analysis and graphics. J. Comput. Graph. Stat. 5 (1996) 299-314
29. Lange A.M., Yutanawiboonchai W., Lok J.B., Trpis M., and Abraham D. Induction of protective immunity against larval Onchocerca volvulus in a mouse model. Am. J. Trop. Med. Hyg. 49 (1993) 783-788
30. Lange A.M., Yutanawiboonchai W., Scott P., and Abraham D. IL-4- and IL-5-dependent protective immunity to Onchocerca volvulus infective larvae in BALB/cBYJ mice. J. Immunol. 153 (1994) 205-211
31. Le Goff L., Maréchal P., Petit G., Taylor D.W., Hoffmann W., and Bain O. Early reduction of the challenge recovery rate following immunization with irradiated infective larvae in a filaria mouse system. Trop. Med. Int. Health 2 (1997) 1170-1174
32. Le Goff L., Loke P., Ali H.F., Taylor D.W., and Allen J.E. Interleukin-5 is essential for vaccine-mediated immunity but not innate resistance to a filarial parasite. Infect. Immun. 68 (2000) 2513-2517
33. Le Goff L., Martin C., Oswald I.P., Vuong P.N., Petit G., Ungeheuer M.N., and Bain O. Parasitology and immunology of mice vaccinated with irradiated Litomosoides sigmodontis larvae. Parasitology 120 (2000) 271-280
34. Le Goff L., Lamb T., Graham A., Harcus Y., and Allen J. IL-4 is required to prevent filarial nematode development in resistant but not susceptible strains of mice. Int. J. Parasitol. 32 (2002) 1277
35. Loke P., MacDonald A.S., Robb A., Maizels R.M., and Allen J.E. Alternatively activated macrophages induced by nematode infection inhibit proliferation via cell-to-cell contact. Eur. J. Immunol. 30 (2000) 2669-2678
36. Loukas A., Bethony J.M., Williamson A.L., Goud G.N., Mendez S., Zhan B., Hawdon J.M., Elena Bottazzi M., Brindley P.J., and Hotez P.J. Vaccination of dogs with a recombinant cysteine protease from the intestine of canine hookworms diminishes the fecundity and growth of worms. J. Infect. Dis. 189 (2004) 1952-1961
37. Lucius R., Textor G., Kern A., and Kirsten C. Acanthocheilonema viteae: vaccination of jirds with irradiation- attenuated stage-3 larvae and with exported larval antigens. Exp. Parasitol. 73 (1991) 184-196
38. Lüder C.G.K., Soboslay P.T., Prince A.M., Greene B.M., Lucius R., and Schulz-Key H. Experimental onchocerciasis in chimpanzees: cellular responses and antigen recognition after immunization and challenge with Onchocerca volvulus infective third-stage larvae. Parasitol. Parasite Immunol. 107 (1993) 87-97
39. Maizels R.M., and Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat. Rev. Immunol. 3 (2003) 733-744
40. Maizels R.M., Balic A., Gomez-Escobar N., Nair M., Taylor M.D., and Allen J.E. Helminth parasites-masters of regulation. Immunol. Rev. 201 (2004) 89-116
41. Maréchal P., Le Goff L., Petit G., Diagne M., Taylor D.W., and Bain O. The fate of the filaria Litomosoides sigmodontis in susceptible and naturally resistant mice. Parasite 3 (1996) 25-31
42. Maréchal P., Le Goff L., Hoffman W., Rapp J., Oswald I.P., Ombrouck C., Taylor D.W., Bain O., and Petit G. Immune response to the filaria Litomosoides sigmodontis in susceptible and resistant mice. Parasite Immunol. 19 (1997) 273-279
43. Martin C., Le Goff L., Ungeheuer M.N., Vuong P.N., and Bain O. Drastic reduction of a filarial infection in eosinophilic interleukin-5 transgenic mice. Infect. Immun. 68 (2000) 3651-3656
44. Martin C., Al-Qaoud K.M., Ungeheuer M.N., Paehle K., Vuong P.N., Bain O., Fleischer B., and Hoerauf A. IL-5 is essential for vaccine-induced protection and for resolution of primary infection in murine filariasis. Med. Microbiol. Immunol. (Berl.) 189 (2000) 67-74
45. Martin C., Saeftel M., Vuong P.N., Babayan S., Fischer K., Bain O., and Hoerauf A. B-cell deficiency suppresses vaccine-induced protection against murine filariasis but does not increase the recovery rate for primary infection. Infect. Immun. 69 (2001) 7067-7073
46. Molyneux D.H. Onchocerciasis control and elimination: coming of age in resource-constrained health systems. Trends Parasitol. 21 (2005) 525-529
47. Nutman T.B. Future directions for vaccine-related onchocerciasis research. Trends Parasitol. 18 (2002) 237-239
48. Osborne J., and Devaney E. The L3 of Brugia induces a Th2-polarized response following activation of an IL-4-producing CD4-CD8- alphabeta T cell population. Int. Immunol. 10 (1998) 1583-1590
49. Perbandt M., Hoppner J., Betzel C., Walter R.D., and Liebau E. Structure of the major cytosolic glutathione S-transferase from the parasitic nematode Onchocerca volvulus. J. Biol. Chem. 280 (2005) 12630-12636
50. Petit G., Diagne M., Marechal P., Owen D., Taylor D., and Bain O. Maturation of the filaria Litomosoides sigmodontis in BALB/c mice; comparative susceptibility of nine other inbred strains. Ann. Parasitol. Hum. Comp. 67 (1992) 144-150
51. Saeftel M., Arndt M., Specht S., Volkmann L., and Hoerauf A. Synergism of gamma interferon and interleukin-5 in the control of murine filariasis. Infect. Immun. 71 (2003) 6978-6985
52. Steel C., and Nutman T.B. CTLA-4 in filarial infections: implications for a role in diminished T cell reactivity. J. Immunol. 170 (2003) 1930-1938
53. Storey D.M., and Al-Mukhtar A.S. Vaccination of jirds, Meriones unguiculatus, against Litomosoides carinii and Brugia pahangi using irradiated larvae of L. carinii. Tropenmed. Parasitol. 33 (1982) 23-24
54. Taylor M.J. Onchocerca volvulus infections in chimpanzees: an assessment of the requirements for vaccination trials. J. Helminthol. 68 (1994) 3-6
55. Taylor M.J., van Es R.P., Shay K., Folkard S.G., Townson S., and Bianco A.E. Protective immunity against Onchocerca volvulus and O. lienalis infective larvae in mice. Trop. Med. Parasitol. 45 (1994) 17-23
56. Taylor M.D., LeGoff L., Harris A., Malone E., Allen J.E., and Maizels R.M. Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J. Immunol. 174 (2005) 4924-4933
57. Tisch D.J., Michael E., and Kazura J.W. Mass chemotherapy options to control lymphatic filariasis: a systematic review. Lancet Infect. Dis. 5 (2005) 514-523
58. Ungeheuer M., Elissa N., Morelli A., Georges A.J., Deloron P., Debre P., Bain O., and Millet P. Cellular responses to Loa loa experimental infection in mandrills (Mandrillus sphinx) vaccinated with irradiated infective larvae. Parasite Immunol. 22 (2000) 173-183
59. Volkmann L., Bain O., Saeftel M., Specht S., Fischer K., Brombacher F., Matthaei K.I., and Hoerauf A. Murine filariasis: interleukin 4 and interleukin 5 lead to containment of different worm developmental stages. Med. Microbiol. Immunol. (Berl.) 192 (2003) 23-31
60. Wanji S., Cabaret J., Gantier J.C., Bonnand N., and Bain O. The fate of the filaria Monanema martini in two rodent hosts: recovery rate, migration, and localization. Ann. Parasitol. Hum. Comp. 65 (1990) 80-88
61. Wanji S., Gantier J.C., Petit G., Rapp J., and Bain O. Monanema martini in its murid hosts: microfiladermia related to infective larvae and adult filariae. Trop. Med. Parasitol. 45 (1994) 107-111
62. Wenk P., and Wegerhof P.H. The effect of a subcutaneous injection of microfilariae given during the prepatent period upon the subsequent development of Litomosoides carinii in cotton rats. Z. Parasitenkd. 50 (1976) 180
63. Wu Y., Egerton G., Pappin D.J., Harrison R.A., Wilkinson M.C., Underwood A., and Bianco A.E. The secreted larval acidic proteins (SLAPs) of Onchocerca spp. are encoded by orthologues of the alt gene family of Brugia malayi and have host protective potential. Mol. Biochem. Parasitol. 134 (2004) 213-224