Immunization of Mastomys coucha with Brugia malayi Recombinant Trehalose-6-Phosphate Phosphatase Results in Significant Protection against Homologous Challenge Infection

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Kushwaha, Susheela ^a   Singh, Prashant Kumar ^a   Rana, Ajay Kumar ^a   Misra Bhattacharya, Shailja ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; IMMUNOMODULATING AGENT; INTERLEUKIN 2; INTERLEUKIN 4; RECOMBINANT TREHALOSE 6 PHOSPHATE PHOSPHATASE; RECOMBINANT VACCINE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ARTICLE; BRUGIAN FILARIASIS; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DISEASE MODEL; FEMALE; FEMALE STERILITY; IMMUNOPROPHYLAXIS; INFECTION SENSITIVITY; LYMPHATIC FILARIASIS; MALE; MASTOMYS; MASTOMYS COUCHA; MICROFILARIA (NEMATODE LARVA); NONHUMAN; PARASITE DEVELOPMENT; PARASITE LOAD; PARASITE VIABILITY; TH1 CELL; TH2 CELL;

ANIMALS; ANTIBODIES, HELMINTH; BRUGIA MALAYI; FILARIASIS; HELMINTH PROTEINS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; MURINAE; PHOSPHORIC MONOESTER HYDROLASES; RECOMBINANT PROTEINS; TH1 CELLS; TH2 CELLS;

EID: 84883148245     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072585     Document Type: Article

References (64)

1. WHO (2011) Global Programme to Eliminate Lymphatic Filariasis: progress report on mass drug administration, 2010. Weekly Epidemiological Record 86: 377-388.
2. Liu LX, Weller PF, (1996) Antiparasitic drugs. N Engl J Med 334: 1178-1184.
3. Rom WN, Vijayan VK, Cornelius MJ, Kumaraswami V, Prabhakar R, et al. (1990) Persistent lower respiratory tract inflammation associated with interstitial lung disease in patients with tropical pulmonary eosinophilia following conventional treatment with diethylcarbamazine. Am Rev Respir Dis 142: 1088-1092.
4. Richard-Lenoble D, Chandenier J, Gaxotte P, (2003) Ivermectin and filariasis. Fundam Clin Pharmacol 17: 199-203.
5. Molyneux DH, Zagaria N, (2002) Lymphatic filariasis elimination: progress in global programme development. Ann Trop Med Parasitol 96Suppl 2: S15-40.
6. Prichard RK, (2007) Ivermectin resistance and overview of the Consortium for Anthelmintic Resistance SNPs. Expert Opin Drug Discovery 2: S41-S52.
7. Townson S, Ramirez B, Fakorede F, Mouries M, Nwaka S (2007) Challenges in drug discovery for novel antifilarials. Expert Opin Drug Discovery. S63-S73.
8. Coles GC, Jackson F, Pomroy WE, Prichard RK, von Samson-Himmelstjerna G, et al. (2006) The detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol 136: 167-185.
9. Schwab AE, Churcher TS, Schwab AJ, Basanez MG, Prichard RK, (2007) An analysis of the population genetics of potential multi-drug resistance in Wuchereria bancrofti due to combination chemotherapy. Parasitology 134: 1025-1040.
10. Molyneux DH, (2009) Filaria control and elimination: diagnostic, monitoring and surveillance needs. Trans R Soc Trop Med Hyg 103: 338-341.
11. Schwab AE, Boakye DA, Kyelem D, Prichard RK, (2005) Detection of benzimidazole resistance-associated mutations in the filarial nematode Wuchereria bancrofti and evidence for selection by albendazole and ivermectin combination treatment. Am J Trop Med Hyg 73: 234-238.
12. Johnston KL, Taylor MJ, (2007) Wolbachia in filarial parasites: targets for filarial infection and disease control. Curr Infect Dis Rep 9: 55-59.
13. Hoerauf A, Specht S, Buttner M, Pfarr K, Mand S, et al. (2008) Wolbachia endobacteria depletion by doxycycline as antifilarial therapy has macrofilaricidal activity in onchocerciasis: a randomized placebo-controlled study. Med Microbiol Immunol 197: 295-311.
14. Hoerauf A, (2003) Control of filarial infections: not the beginning of the end, but more research is needed. Curr Opin Infect Dis 16: 403-410.
15. Bottazzi ME, Miles AP, Diemert D, Hotez PJ, (2006) An ounce of prevention on a budget: a nonprofit approach to developing vaccines against neglected diseases. Expert Rev Vaccines 5: 189-198.
16. Ottesen EA, (1984) Immunological aspects of lymphatic filariasis and onchocerciasis in man. Trans R Soc Trop Med Hyg 78Suppl: 9-18.
17. Yates JA, Higashi GI, (1985) Brugia malayi: vaccination of jirds with 60cobalt-attenuated infective stage larvae protects against homologous challenge. Am J Trop Med Hyg 34: 1132-1137.
18. Le Goff L, Marechal P, Petit G, Taylor DW, Hoffmann W, et al. (1997) Early reduction of the challenge recovery rate following immunization with irradiated infective larvae in a filaria mouse system. Trop Med Int Health 2: 1170-1174.
19. Diemert DJ, Bethony JM, Hotez PJ, (2008) Hookworm vaccines. Clin Infect Dis 46: 282-288.
20. Makepeace BL, Jensen SA, Laney SJ, Nfon CK, Njongmeta LM, et al. (2009) Immunisation with a multivalent, subunit vaccine reduces patent infection in a natural bovine model of onchocerciasis during intense field exposure. PLoS Negl Trop Dis 3: e544.
21. Vanam U, Pandey V, Prabhu PR, Dakshinamurthy G, Reddy MV, et al. (2009) Evaluation of immunoprophylactic efficacy of Brugia malayi transglutaminase (BmTGA) in single and multiple antigen vaccination with BmALT-2 and BmTPX for human lymphatic filariasis. Am J Trop Med Hyg 80: 319-324.
22. Vedi S, Dangi A, Hajela K, Misra-Bhattacharya S, (2008) Vaccination with 73 kDa recombinant heavy chain myosin generates high level of protection against Brugia malayi challenge in jird and mastomys models. Vaccine 26: 5997-6005.
23. Gregory WF, Atmadja AK, Allen JE, Maizels RM, (2000) The abundant larval transcript-1 and-2 genes of Brugia malayi encode stage-specific candidate vaccine antigens for filariasis. Infect Immun 68: 4174-4179.
24. Thirugnanam S, Pandiaraja P, Ramaswamy K, Murugan V, Gnanasekar M, et al. (2007) Brugia malayi: comparison of protective immune responses induced by Bm-alt-2 DNA, recombinant Bm-ALT-2 protein and prime-boost vaccine regimens in a jird model. Exp Parasitol 116: 483-491.
25. Dakshinamoorthy G, Samykutty AK, Munirathinam G, Shinde GB, Nutman T, et al. (2012) Biochemical characterization and evaluation of a Brugia malayi small heat shock protein as a vaccine against lymphatic filariasis. PLoS One 7: e34077.
26. Shakya S, Singh PK, Kushwaha S, Misra-Bhattacharya S, (2009) Adult Brugia malayi approximately 34 kDa (BMT-5) antigen offers Th1 mediated significant protection against infective larval challenge in Mastomys coucha. Parasitol Int 58: 346-353.
27. Pokharel DR, Rai R, Nandakumar Kodumudi K, Reddy MV, Rathaur S, (2006) Vaccination with Setaria cervi 175 kDa collagenase induces high level of protection against Brugia malayi infection in jirds. Vaccine 24: 6208-6215.
28. Babayan SA, Attout T, Harris A, Taylor MD, Le Goff L, et al. (2006) Vaccination against filarial nematodes with irradiated larvae provides long-term protection against the third larval stage but not against subsequent life cycle stages. Int J Parasitol 36: 903-914.
29. Kalyanasundaram R, Balumuri P, (2011) Multivalent vaccine formulation with BmVAL-1 and BmALT-2 confer significant protection against challenge infections with Brugia malayi in mice and jirds. Res Rep Trop Med 2011: 45-56.
30. Kushwaha S, Singh PK, Rana AK, Misra-Bhattacharya S, (2011) Cloning, expression, purification and kinetics of trehalose-6-phosphate phosphatase of filarial parasite Brugia malayi. Acta Trop 119: 151-159.
31. Kushwaha S, Singh PK, Gupta J, Soni VK, Misra-Bhattacharya S, (2012) Recombinant trehalose-6-phosphate phosphatase of Brugia malayi cross-reacts with human Wuchereria bancrofti immune sera and engenders a robust protective outcome in mice. Microbes Infect 14: 1330-1339.
32. Kushwaha S, Soni VK, Singh PK, Bano N, Kumar A, et al. (2011) Withania somnifera chemotypes NMITLI 101R, NMITLI 118R, NMITLI 128R and Withaferin A protect Mastomys coucha from Brugia malayi infection. Parasite Immunol.
33. Veerapathran A, Dakshinamoorthy G, Gnanasekar M, Reddy MV, Kalyanasundaram R, (2009) Evaluation of Wuchereria bancrofti GST as a vaccine candidate for lymphatic filariasis. PLoS Negl Trop Dis 3: e457.
34. Loke P, MacDonald AS, Allen JE, (2000) Antigen-presenting cells recruited by Brugia malayi induce Th2 differentiation of naive CD4(+) T cells. Eur J Immunol 30: 1127-1135.
35. Whelan M, Harnett MM, Houston KM, Patel V, Harnett W, et al. (2000) A filarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J Immunol 164: 6453-6460.
36. Semnani RT, Sabzevari H, Iyer R, Nutman TB, (2001) Filarial antigens impair the function of human dendritic cells during differentiation. Infect Immun 69: 5813-5822.
37. Jenson JS, O'Connor R, Osborne J, Devaney E, (2002) Infection with Brugia microfilariae induces apoptosis of CD4(+) T lymphocytes: a mechanism of immune unresponsiveness in filariasis. Eur J Immunol 32: 858-867.
38. Mabbott NA, Sutherland IA, Sternberg JM, (1995) Suppressor macrophages in Trypanosoma brucei infection: nitric oxide is related to both suppressive activity and lifespan in vivo. Parasite Immunol 17: 143-150.
39. Nanduri J, Kazura JW, (1989) Clinical and laboratory aspects of filariasis. Clinical Microbiology 2: 39-50.
40. Ottesen EA, (1992) The Wellcome Trust Lecture. Infection and disease in lymphatic filariasis: an immunological perspective. Parasitology 104Suppl: S71-79.
41. Solomon A, Salomon R, Paperna I, Glazer I, (2000) Desiccation stress of entomopathogenic nematodes induces the accumulation of a novel heat-stable protein. Parasitology 121 (Pt 4): 409-416.
42. Gal TZ, Solomon A, Glazer I, Koltai H, (2001) Alterations in the levels of glycogen and glycogen synthase transcripts during desiccation in the insect-killing nematode Steinernema feltiae IS-6. J Parasitol 87: 725-732.
43. Wharton DA, Goodall G, Marshall CJ, (2002) Freezing rate affects the survival of a short-term freezing stress in Panagrolaimus davidi, an Antarctic nematode that survives intracellular freezing. Cryo Letters 23: 5-10.
44. Benoita JB, Martineza GL, Elnitsky MA, Lee RE, Denlinger DL, (2009) Dehydration-induced cross tolerance of Belgica antarctica larvae to cold and heat is facilitated by trehalose accumulation. Comp Biochem Physiol A Mol Integr Physiol 152: 518-523.
45. Kushwaha S, Singh PK, Shahab M, Pathak M, Bhattacharya SM, (2011) In vitro silencing of Brugia malayi trehalose-6-phosphate phosphatase impairs embryogenesis and in vivo development of infective larvae in jirds. PLoS Negl Trop Dis 6: e1770.
46. Chandrashekar R, Rao UR, Parab PB, Subrahmanyam D, (1985) Brugia malayi: serum dependent cell-mediated reactions to microfilariae. Southeast Asian J Trop Med Public Health 16: 15-21.
47. Chandrashekar R, Rao UR, Subrahmanyam D, (1985) Serum dependent cell-mediated immune reactions to Brugia pahangi infective larvae. Parasite Immunol 7: 633-641.
48. Sim BK, Kwa BE, Mak JW, (1982) Immune responses in human Brugia malayi infections: Serum dependent cell mediated destruction of infective larvae in vitro. Trans R Soc Trop Med Hyg 76: 362-369.
49. Chenthamarakshan V, Cheirmaraj K, Reddy MVR, Harinath BC, (1997) Immunoprophylactic studies with a 43 kDa human circulating filarial antigen and a cross reactive 120 kDa Brugia malayi sodium dodecyl sulphate soluble antigen in filariasis. J Biosci 22: 91-98.
50. Sim BK, Kwa BH, Mak JW, (1982) Immune responses in human Brugia malayi infections: serum dependent cell-mediated destruction of infective larvae in vitro. Trans R Soc Trop Med Hyg 76: 362-370.
51. Lloyd S, Soulsby EJ, (1978) The role of IgA immunoglobulins in the passive transfer of protection to Taenia taeniaeformis in the mouse. Immunology 34: 939-945.
52. Almond NM, Parkhouse RM, (1986) Immunoglobulin class specific responses to biochemically defined antigens of Trichinella spiralis. Parasite Immunol 8: 391-406.
53. Grzych JM, Grezel D, Xu CB, Neyrinck JL, Capron M, et al. (1993) IgA antibodies to a protective antigen in human Schistosomiasis mansoni. J Immunol 150: 527-535.
54. Khalil HM, Abd el Baki MH, Abd el Mawla MM, Maklad KM, Sharaf SA, et al. (1999) Interleukin-4, immunoglobulin E and immunoglobulin A and resistance to re-infection with Schistosoma haematobium before and after chemotherapy. J Egypt Soc Parasitol 29: 395-408.
55. Sahu BR, Mohanty MC, Sahoo PK, Satapathy AK, Ravindran B, (2008) Protective immunity in human filariasis: a role for parasite-specific IgA responses. J Infect Dis 198: 434-443.
56. Saeftel M, Arndt M, Specht S, Volkmann L, Hoerauf A, (2003) Synergism of gamma interferon and interleukin-5 in the control of murine filariasis. Infect Immun 71: 6978-6985.
57. Volkmann L, Saeftel M, Bain O, Fischer K, Fleischer B, et al. (2001) Interleukin-4 is essential for the control of microfilariae in murine infection with the filaria Litomosoides sigmodontis. Infect Immun 69: 2950-2956.
58. Bancroft AJ, Artis D, Donaldson DD, Sypek JP, Grencis RK, (2000) Gastrointestinal nematode expulsion in IL-4 knockout mice is IL-13 dependent. Eur J Immunol 30: 2083-2091.
59. Elson LH, Calvopina M, Paredes W, Araujo E, Bradley JE, et al. (1995) Immunity to onchocerciasis: putative immune persons produce a Th1-like response to Onchocerca volvulus. J Infect Dis 171: 652-658.
60. Dimock KA, Eberhard ML, Lammie PJ, (1996) Th1-like antifilarial immune responses predominate in antigen-negative persons. Infect Immun 64: 2962-2967.
61. Diefenbach A, Schindler H, Donhauser N, Lorenz E, Laskay T, et al. (1998) Type 1 interferon (IFNalpha/beta) and type 2 nitric oxide synthase regulate the innate immune response to a protozoan parasite. Immunity 8: 77-87.
62. MacDonald AS, Maizels RM, Lawrence RA, Dransfield I, Allen JE, (1998) Requirement for in vivo production of IL-4, but not IL-10, in the induction of proliferative suppression by filarial parasites. J Immunol 160: 1304-1312.
63. Osborne J, Hunter SJ, Devaney E, (1996) Anti-interleukin-4 modulation of the Th2 polarized response to the parasitic nematode Brugia pahangi. Infect Immun 64: 3461-3466.
64. Vickery AC, Vincent AL, (1984) Immunity to Brugia pahangi in athymic nude and normal mice: eosinophilia, antibody and hypersensitivity responses. Parasite Immunol 6: 545-559.