Immunotherapy with mutated onchocystatin fails to enhance the efficacy of a sub-lethal oxytetracycline regimen against Onchocerca ochengi

Veterinary Parasitology

Volumn 212, Issue 1-2, 2015, Pages 25-34

  Bah, Germanus S ^a,b   Tanya, Vincent N ^b,c   Makepeace, Benjamin L ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b Regional Centre of Wakwa   (Cameroon)

^c Cameroon Academy of Sciences   (Cameroon)

Author keywords

Cysteine proteinase inhibitor; Filariasis; Immunochemotherapy; Macrofilaricide; Symbiosis

Indexed keywords

CYSTEINE PROTEINASE INHIBITOR; IMMUNOGLOBULIN G ANTIBODY; OXYTETRACYCLINE; RECOMBINANT ONCHOCYSTATIN; UNCLASSIFIED DRUG; HELMINTH PROTEIN; IMMUNOGLOBULIN G; ONCHOCYSTATIN PROTEIN, ONCHOCERCA VOLVULUS; VACCINE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CAMEROONIAN; CATTLE DISEASE; CELL EXPANSION; CONTROLLED STUDY; CUTICLE; DRUG RESPONSE; DRUG TARGETING; EOSINOPHIL; EOSINOPHIL COUNT; FEMALE; HOST PARASITE INTERACTION; IMMUNOMODULATION; MALE; NEMATODE LIFE CYCLE STAGE; NONHUMAN; ONCHOCERCA; ONCHOCERCA OCHENGI; ONCHOCERCIASIS; PARASITE CONTROL; TREATMENT DURATION; ANIMAL; BLOOD; BOVINE; CAMEROON; CATTLE DISEASES; CHEMISTRY; DRUG COMBINATION; DRUG EFFECTS; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; MUTATION; PHYSIOLOGY; RANDOMIZATION; STANDARDS; TREATMENT OUTCOME; VETERINARY;

BOS; BOVINAE; LOA LOA; ONCHOCERCA OCHENGI; ONCHOCERCA VOLVULUS; WOLBACHIA;

ANIMALS; CAMEROON; CATTLE; CATTLE DISEASES; DRUG THERAPY, COMBINATION; FEMALE; HELMINTH PROTEINS; IMMUNOGLOBULIN G; IMMUNOTHERAPY; MALE; MUTATION; ONCHOCERCA; OXYTETRACYCLINE; RANDOM ALLOCATION; TREATMENT OUTCOME; VACCINES;

EID: 84938550090     PISSN: 03044017     EISSN: 18732550     Source Type: Journal    
DOI: 10.1016/j.vetpar.2015.06.005     Document Type: Article

References (72)

1. Abraham D., Leon O., Schnyder-Candrian S., Wang C.C., Galioto A.M., Kerepesi L.A., Lee J.J., Lustigman S. Immunoglobulin E and eosinophil-dependent protective immunity to larval Onchocerca volvulus in mice immunized with irradiated larvae. Infect. Immun. 2004, 72:810-817.
2. Anon The Merck Veterinary Manual 2005, Merck & Co., Inc., Whitehouse Station, NJ, USA.
3. Anon Working to Overcome the Global Impact of Neglected Tropical Diseases: First Who Report on Neglected Tropical Diseases 2010, World Health Organisation, Geneva. D.W.T. Crompton, P. Peters (Eds.).
4. Armstrong S.D., Babayan S.A., Lhermitte-Vallarino N., Gray N., Xia D., Martin C., Kumar S., Taylor D.W., Blaxter M.L., Wastling J.M., Makepeace B.L. Comparative analysis of the secretome from a model filarial nematode (Litomosoides sigmodontis) reveals maximal diversity in gravid female parasites. Mol. Cell. Proteomics 2014, 13:2527-2544.
5. Arumugam S., Wei J., Ward D., Abraham D., Lustigman S., Zhan B., Klei T.R. Vaccination with a genetically modified Brugia malayi cysteine protease inhibitor-2 reduces adult parasite numbers and affects the fertility of female worms following a subcutaneous challenge of Mongolian gerbils (Meriones unguiculatus) with B. malayi infective larvae. Int. J. Parasitol. 2014, 44:675-679.
6. Babayan S.A., Luo H., Gray N., Taylor D.W., Allen J.E. Deletion of parasite immune modulatory sequences combined with immune activating signals enhances vaccine mediated protection against filarial nematodes. PLoS Negl. Trop. Dis. 2012, 6:e1968.
7. Bah G.S., Ward E.L., Srivastava A., Trees A.J., Tanya V.N., Makepeace B.L. Efficacy of three-week oxytetracycline or rifampin monotherapy compared with a combination regimen against the filarial nematode Onchocerca ochengi. Antimicrob. Agents Chemother. 2014, 58:801-810.
8. Baldwin C.I., de M.F., Denham D.A. IgE responses in cats infected with Brugia pahangi. Parasite Immunol. 1993, 15:291-296.
9. Bandi C., McCall J.W., Genchi C., Corona S., Venco L., Sacchi L. Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia. Int. J. Parasitol. 1999, 29:357-364.
10. Blair L.S., Campbell W.C. Immunization of ferrets against Dirofilaria immitis by means of chemically abbreviated infections. Parasite Immunol. 1981, 3:143-147.
11. Botros S.S., Doughty B.L., Shaker Z.A., Akl M.M., Sharmy R., Diab T.M., Hassanein H.I. Efficacy of an antipathology vaccine in murine schistosomiasis administered with and without chemotherapy. Int. J. Immunopharmacol. 1996, 18:707-718.
12. Bourke C.D., Nausch N., Rujeni N., Appleby L.J., Trottein F., Midzi N., Mduluza T., Mutapi F. Cytokine responses to the anti-schistosome vaccine candidate antigen glutathione-S-transferase vary with host age and are boosted by praziquantel treatment. PLoS Negl. Trop. Dis. 2014, 8:e2846.
13. Brattig N.W. Pathogenesis and host responses in human onchocerciasis: impact of Onchocerca filariae and Wolbachia endobacteria. Microbes Infect. 2004, 6:113-128.
14. Bronsvoort B.M., Renz A., Tchakouté V., Tanya V.N., Ekale D.D., Trees A.J. Repeated high doses of avermectins cause prolonged sterilisation, but do not kill Onchocerca ochengi adult worms in African cattle. Filaria J. 2005, 4:8.
15. Chhabra S., Chang S.C., Nguyen H.M., Huq R., Tanner M.R., Londono L.M., Estrada R., Dhawan V., Chauhan S., Upadhyay S.K., Gindin M., Hotez P.J., Valenzuela J.G., Mohanty B., Swarbrick J.D., Wulff H., Iadonato S.P., Gutman G.A., Beeton C., Pennington M.W., Norton R.S., Chandy K.G. Kv1. 3 channel-blocking immunomodulatory peptides from parasitic worms: implications for autoimmune diseases. FASEB J. 2014, 28:3952-3964.
16. Cox F.E. Interactions between chemotherapy and immunity in bovine theileriosis. Parasitology 1992, 105(Suppl. S79-S84).
17. Crump A., Morel C.M., Omura S. The onchocerciasis chronicle: from the beginning to the end?. Trends Parasitol. 2012, 28:280-288.
18. Darby A.C., Christina G.A., Armstrong S.D., Hartley C.S., Xia D., Wastling J.M., Makepeace B.L. Integrated transcriptomic and proteomic analysis of the global response of Wolbachia to doxycycline-induced stress. ISME J 2014, 8:925-937.
19. Duffus W.P., Franks D. In vitro effect of immune serum and bovine granulocytes on juvenile Fasciola hepatica. Clin. Exp. Immunol. 1980, 41:430-440.
20. Duke B.O. Reinfections with Onchocerca volvulus in cured patients exposed to continuing transmission. Bull. World Health Organ. 1968, 39:307-309.
21. Dupré L., Hervé M., Schacht A.M., Capron A., Riveau G. Control of schistosomiasis pathology by combination of Sm28GST DNA immunization and praziquantel treatment. J. Infect. Dis. 1999, 180:454-463.
22. Ferri E., Bain O., Barbuto M., Martin C., Lo N., Uni S., Landmann F., Baccei S.G., Guerrero R., de Souza L.S., Bandi C., Wanji S., Diagne M., Casiraghi M. New insights into the evolution of Wolbachia infections in filarial nematodes inferred from a large range of screened species. PLoS One 2011, 6:e20843.
23. Gardon J., Gardon-Wendel N., Demanga N., Kamgno J., Chippaux J.P., Boussinesq M. Serious reactions after mass treatment of onchocerciasis with ivermectin in an area endemic for Loa loa infection. Lancet 1997, 350:18-22.
24. Gershwin L.J. Bovine immunoglobulin E. Vet. Immunol. Immunopathol. 2009, 132:2-6.
25. Ghedin E., Hailemariam T., DePasse J.V., Zhang X., Oksov Y., Unnasch T.R., Lustigman S. Brugia malayi gene expression in response to the targeting of the Wolbachia endosymbiont by tetracycline treatment. PLoS Negl. Trop. Dis. 2009, 3:e525.
26. Gilbert J., Nfon C.K., Makepeace B.L., Njongmeta L.M., Hastings I.M., Pfarr K.M., Renz A., Tanya V.N., Trees A.J. Antibiotic chemotherapy of onchocerciasis: in a bovine model, killing of adult parasites requires a sustained depletion of endosymbiotic bacteria (Wolbachia species). J. Infect. Dis. 2005, 192:1483-1493.
27. Gill A.C., Darby A.C., Makepeace B.L. Iron necessity: the secret of Wolbachia's success?. PLoS Negl. Trop. Dis. 2014, 8:e3224.
28. Grieve R.B., Abraham D., Mika-Grieve M., Seibert B.P. Induction of protective immunity in dogs to infection with Dirofilaria immitis using chemically-abbreviated infections. Am. J. Trop. Med. Hyg. 1988, 39:373-379.
29. Haben I., Hartmann W., Breloer M. Nematode-induced interference with vaccination efficacy targets follicular T helper cell induction and is preserved after termination of infection. PLoS Negl. Trop. Dis. 2014, 8:e3170.
30. Hansen R.D., Trees A.J., Bah G.S., Hetzel U., Martin C., Bain O., Tanya V.N., Makepeace B.L. A worm's best friend: recruitment of neutrophils by Wolbachia confounds eosinophil degranulation against the filarial nematode Onchocerca ochengi. Proc. R. Soc. B 2010, 278:2293-2302.
31. Hess J.A., Zhan B., Bonne-Annee S., Deckman J.M., Bottazzi M.E., Hotez P.J., Klei T.R., Lustigman S., Abraham D. Vaccines to combat river blindness: expression, selection and formulation of vaccines against infection with Onchocerca volvulus in a mouse model. Int. J. Parasitol. 2014, 44:637-646.
32. Hewitson J.P., Harcus Y.M., Curwen R.S., Dowle A.A., Atmadja A.K., Ashton P.D., Wilson A., Maizels R.M. The secretome of the filarial parasite, Brugia malayi: proteomic profile of adult excretory-secretory products. Mol. Biochem. Parasitol. 2008, 160:8-21.
33. Hoerauf A., Nissen-Pähle K., Schmetz C., Henkle-Dührsen K., Blaxter M.L., Büttner D.W., Gallin M.Y., Al-Qaoud K.M., Lucius R., Fleischer B. Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility. J. Clin. Invest. 1999, 103:11-18.
34. Hoerauf A., Volkmann L., Hamelmann C., Adjei O., Autenrieth I.B., Fleischer B., Büttner D.W. Endosymbiotic bacteria in worms as targets for a novel chemotherapy in filariasis. Lancet 2000, 355:1242-1243.
35. Hoerauf A., Marfo-Debrekyei Y., Buttner M., Debrah A.Y., Konadu P., Mand S., Adjei O., Buttner D.W. Effects of 6-week azithromycin treatment on the Wolbachia endobacteria of Onchocerca volvulus. Parasitol. Res. 2008, 103:279-286.
36. Hoerauf A., Specht S., Buttner M., Pfarr K., Mand S., Fimmers R., Marfo-Debrekyei Y., Konadu P., Debrah A.Y., Bandi C., Brattig N., Albers A., Larbi J., Batsa L., Taylor M.J., Adjei O., Buttner D.W. Wolbachia endobacteria depletion by doxycycline as antifilarial therapy has macrofilaricidal activity in onchocerciasis: a randomized placebo-controlled study. Med. Microbiol. Immunol. 2008, 197:295-311.
37. Hotez P.J., Alvarado M., Basanez M.G., Bolliger I., Bourne R., Boussinesq M., Brooker S.J., Brown A.S., Buckle G., Budke C.M., Carabin H., Coffeng L.E., Fevre E.M., Furst T., Halasa Y.A., Jasrasaria R., Johns N.E., Keiser J., King C.H., Lozano R., Murdoch M.E., O'Hanlon S., Pion S.D., Pullan R.L., Ramaiah K.D., Roberts T., Shepard D.S., Smith J.L., Stolk W.A., Undurraga E.A., Utzinger J., Wang M., Murray C.J., Naghavi M. The global burden of disease study 2010: interpretation and implications for the neglected tropical diseases. PLoS Negl. Trop. Dis. 2014, 8:e2865.
38. Jain-Gupta N., Contreras-Rodriguez A., Smith G.P., Garg V.K., Witonsky S.G., Isloor S., Vemulapalli R., Boyle S.M., Sriranganathan N. Immunotherapeutics to prevent the replication of Brucella in a treatment failure mouse model. Vaccine 2014, 32:918-923.
39. Johnston K.L., Ford L., Umareddy I., Townson S., Specht S., Pfarr K., Hoerauf A., Altmeyer R., Taylor M.J. Repurposing of approved drugs from the human pharmacopoeia to target Wolbachia endosymbionts of onchocerciasis and lymphatic filariasis. Int. J. Parasitol. Drugs Drug Resist. 2014, 4:278-286.
40. Katabarwa M.N., Lakwo T., Habomugisha P., Agunyo S., Byamukama E., Oguttu D., Tukesiga E., Unoba D., Dramuke P., Onapa A., Tukahebwa E.M., Lwamafa D., Walsh F., Unnasch T.R. Transmission of Onchocerca volvulus continues in Nyagak-Bondo focus of northwestern Uganda after 18 Years of a single dose of annual treatment with ivermectin. Am. J. Trop. Med. Hyg. 2013, 89:293-300.
41. Kurniawan A., Yazdanbakhsh M., van R.R., Aalberse R., Selkirk M.E., Partono F., Maizels R.M. Differential expression of IgE and IgG4 specific antibody responses in asymptomatic and chronic human filariasis. J. Immunol. 1993, 150:3941-3950.
42. Landmann F., Voronin D., Sullivan W., Taylor M.J. Anti-filarial activity of antibiotic therapy is due to extensive apoptosis after Wolbachia depletion from filarial nematodes. PLoS Pathog. 2011, 7:e1002351.
43. Langworthy N.G., Renz A., Mackenstedt U., Henkle-Dührsen K., de Bronsvoort M.B., Tanya V.N., Donnelly M.J., Trees A.J. Macrofilaricidal activity of tetracycline against the filarial nematode Onchocerca ochengi: elimination of Wolbachia precedes worm death and suggests a dependent relationship. Proc. R. Soc. B 2000, 267:1063-1069.
44. Lustigman S., Brotman B., Huima T., Prince A.M. Characterization of an Onchocerca volvulus cDNA clone encoding a genus specific antigen present in infective larvae and adult worms. Mol. Biochem. Parasitol. 1991, 45:65-75.
45. Makepeace B.L., Jensen S.A., Laney S.J., Nfon C.K., Njongmeta L.M., Tanya V.N., Williams S.A., Bianco A.E., Trees A.J. Immunisation with a multivalent, subunit vaccine reduces patent infection in a natural bovine model of onchocerciasis during intense field exposure. PLoS Negl. Trop. Dis. 2009, 3:e544.
46. Manoury B., Gregory W.F., Maizels R.M., Watts C. Bm-CPI-2, a cystatin homolog secreted by the filarial parasite Brugia malayi, inhibits class II MHC-restricted antigen processing. Curr. Biol. 2001, 11:447-451.
47. Morales-Hojas R., Cheke R.A., Post R.J. Molecular systematics of five Onchocerca species (Nematoda: Filarioidea) including the human parasite, O. volvulus, suggest sympatric speciation. J. Helminthol. 2006, 80:281-290.
48. Murray J., Manoury B., Balic A., Watts C., Maizels R.M. Bm-CPI-2, a cystatin from Brugia malayi nematode parasites, differs from Caenorhabditis elegans cystatins in a specific site mediating inhibition of the antigen-processing enzyme AEP. Mol. Biochem. Parasitol. 2005, 139:197-203.
49. Musa A.M., Khalil E.A., Mahgoub F.A., Elgawi S.H., Modabber F., Elkadaru A.E., Aboud M.H., Noazin S., Ghalib H.W., El-Hassan A.M. Immunochemotherapy of persistent post-kala-azar dermal leishmaniasis: a novel approach to treatment. Trans. R. Soc. Trop. Med. Hyg. 2008, 102:58-63.
50. Mutapi F., Ndhlovu P.D., Hagan P., Spicer J.T., Mduluza T., Turner C.M., Chandiwana S.K., Woolhouse M.E. Chemotherapy accelerates the development of acquired immune responses to Schistosoma haematobium infection. J. Infect. Dis. 1998, 178:289-293.
51. Naessens J., Newson J., Williams D.J., Lutje V. Identification of isotypes and allotypes of bovine immunoglobulin M with monoclonal antibodies. Immunology 1988, 63:569-574.
52. Nana-Djeunga H.C., Bourguinat C., Pion S.D., Bopda J., Kengne-Ouafo J.A., Njiokou F., Prichard R.K., Wanji S., Kamgno J., Boussinesq M. Reproductive status of Onchocerca volvulus after ivermectin treatment in an ivermectin-naive and a frequently treated population from Cameroon. PLoS Negl. Trop. Dis. 2014, 8:e2824.
53. Nfon C.K., Makepeace B.L., Njongmeta L.M., Tanya V.N., Bain O., Trees A.J. Eosinophils contribute to killing of adult Onchocerca ochengi within onchocercomata following elimination of Wolbachia. Microbes Infect. 2006, 8:2698-2705.
54. Nfon C.K., Makepeace B.L., Njongmeta L.M., Tanya V.N., Trees A.J. Lack of resistance after re-exposure of cattle cured of Onchocerca ochengi infection with oxytetracycline. Am. J. Trop. Med. Hyg. 2007, 76:67-72.
55. Njongmeta L.M., Nfon C.K., Gilbert J., Makepeace B.L., Tanya V.N., Trees A.J. Cattle protected from onchocerciasis by ivermectin are highly susceptible to infection after drug withdrawal. Int. J. Parasitol. 2004, 34:1069-1074.
56. Osei-Atweneboana M.Y., Eng J.K., Boakye D.A., Gyapong J.O., Prichard R.K. Prevalence and intensity of Onchocerca volvulus infection and efficacy of ivermectin in endemic communities in Ghana: a two-phase epidemiological study. Lancet 2007, 369:2021-2029.
57. Peng X., Keitany G.J., Vignali M., Chen L., Gibson C., Choi K., Huang F., Wang R. Artesunate versus chloroquine infection-treatment-vaccination defines stage-specific immune responses associated with prolonged sterile protection against both pre-erythrocytic and erythrocytic Plasmodium yoelii infection. J. Immunol. 2014, 193:1268-1277.
58. Renz A., Trees A.J., Achukwi D., Edwards G., Wahl G. Evaluation of suramin, ivermectin and CGP 20,376 in a new macrofilaricidal drug screen, Onchocerca ochengi in African cattle. Trop. Med. Parasitol. 1995, 46:31-37.
59. Richards F.O., Amann J., Arana B., Punkosdy G., Klein R., Blanco C., Lopez B., Mendoza C., Dominguez A., Guarner J., Maguire J.H., Eberhard M. No depletion of Wolbachia from Onchocerca volvulus after a short course of rifampin and/or azithromycin. Am. J. Trop. Med. Hyg. 2007, 77:878-882.
60. Rofatto H.K., Araujo-Montoya B.O., Miyasato P.A., Levano-Garcia J., Rodriguez D., Nakano E., Verjovski-Almeida S., Farias L.P., Leite L.C. Immunization with tegument nucleotidases associated with a subcurative praziquantel treatment reduces worm burden following Schistosoma mansoni challenge. PeerJ 2013, 1:e58.
61. Specht S., Mand S., Marfo-Debrekyei Y., Debrah A.Y., Konadu P., Adjei O., Buttner D.W., Hoerauf A. Efficacy of 2- and 4-week rifampicin treatment on the Wolbachia of Onchocerca volvulus. Parasitol. Res. 2008, 103:1303-1309.
62. Specht S., Taylor M.D., Hoeve M.A., Allen J.E., Lang R., Hoerauf A. Over expression of IL-10 by macrophages overcomes resistance to murine filariasis. Exp. Parasitol. 2012, 132:90-96.
63. Strubing U., Lucius R., Hoerauf A., Pfarr K.M. Mitochondrial genes for heme-dependent respiratory chain complexes are up-regulated after depletion of Wolbachia from filarial nematodes. Int. J. Parasitol. 2010, 40:1193-1202.
64. Taylor M.D., LeGoff L., Harris A., Malone E., Allen J.E., Maizels R.M. Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J. Immunol. 2005, 174:4924-4933.
65. Taylor M.J., Hoerauf A., Townson S., Slatko B.E., Ward S.A. Anti-Wolbachia drug discovery and development: safe macrofilaricides for onchocerciasis and lymphatic filariasis. Parasitology 2014, 141:119-127.
66. Tchakouté V.L., Graham S.P., Jensen S.A., Makepeace B.L., Nfon C.K., Njongmeta L.M., Lustigman S., Enyong P.A., Tanya V.N., Bianco A.E., Trees A.J. In a bovine model of onchocerciasis, protective immunity exists naturally, is absent in drug-cured hosts, and is induced by vaccination. Proc. Natl. Acad. Sci. USA 2006, 103:5971-5976.
67. Thylefors B., Alleman M. Towards the elimination of onchocerciasis. Ann. Trop. Med. Parasitol. 2006, 100:733-746.
68. Traore M.O., Sarr M.D., Badji A., Bissan Y., Diawara L., Doumbia K., Goita S.F., Konate L., Mounkoro K., Seck A.F., Toe L., Toure S., Remme J.H. Proof-of-principle of onchocerciasis elimination with ivermectin treatment in endemic foci in Africa: final results of a study in Mali and Senegal. PLoS Negl. Trop. Dis. 2012, 6:e1825.
69. van der Werf N., Redpath S.A., Azuma M., Yagita H., Taylor M.D. Th2 cell-intrinsic hypo-responsiveness determines susceptibility to helminth infection. PLoS Pathog. 2013, 9:e1003215.
70. Wanji S., Kengne-Ouafo J.A., Esum M.E., Chounna P.W., Tendongfor N., Adzemye B.F., Eyong J.E., Jato I., Datchoua-Poutcheu F.R., Kah E., Enyong P., Taylor D.W. Situation analysis of parasitological and entomological indices of onchocerciasis transmission in three drainage basins of the rain forest of South West Cameroon after a decade of ivermectin treatment. Parasit. Vectors 2015, 8:202.
71. Wilson M.S., Cheever A.W., White S.D., Thompson R.W., Wynn T.A. IL-10 blocks the development of resistance to re-infection with Schistosoma mansoni. PLoS Pathog. 2011, 7:e1002171.
72. Zhang Z., Xu H., Gan W., Zeng S., Hu X. Schistosoma japonicum calcium-binding tegumental protein SjTP22.4 immunization confers praziquantel schistosomulumicide and antifecundity effect in mice. Vaccine 2012, 30:5141-5150.