Prior killing of intracellular bacteria Wolbachia reduces inflammatory reactions and improves antifilarial efficacy of diethylcarbamazine in rodent model of Brugia malayi

Parasitology Research

Volumn 102, Issue 5, 2008, Pages 963-972

  Shakya, Shilpy ^a   Bajpai, Preeti ^a   Sharma, Sharad ^a   Misra Bhattacharya, Shailja ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

DIETHYLCARBAMAZINE; TETRACYCLINE;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERICIDAL ACTIVITY; BRUGIA MALAYI; CONTROLLED STUDY; DRUG EFFICACY; FILARIASIS; FLUORESCENCE ACTIVATED CELL SORTING; HISTOPATHOLOGY; MALE; MASTOMYS; MICROFILARIASIS; MONOTHERAPY; NONHUMAN; PATHOGENESIS; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; RESPIRATORY BURST; RODENT; WOLBACHIA;

ANIMALS; ANTI-BACTERIAL AGENTS; BRUGIA MALAYI; DIETHYLCARBAMAZINE; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION SCHEDULE; DRUG THERAPY, COMBINATION; FEMALE; FILARIASIS; FILARICIDES; GERBILLINAE; HOST-PARASITE INTERACTIONS; HUMANS; INFLAMMATION; MALE; MURINAE; TETRACYCLINE; TREATMENT OUTCOME; WOLBACHIA;

BRUGIA MALAYI; MASTOMYS COUCHA; MERIONES UNGUICULATUS; NEMATODA; ONCHOCERCIDAE; RODENTIA; WOLBACHIA;

EID: 41549122901     PISSN: 09320113     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00436-007-0861-8     Document Type: Article

References (60)

1. Bajpai P, Vedi S, Owais M, Sharma SK, Misra-Bhattacharya S (2005) Use of liposomized tetracycline in elimination of Wolbachia endobacterium of human lymphatic filariid Brugia malayi in rodent model. J Drug Target 13(6):375-381
2. Bajpai P, Srivastava K, Shakya S, Saxena PN, Misra-Bhattacharya S (2007) Improvement in the efficacy of existing combination of antifilarials by inclusion of tetracycline in rodent model of brugian filariasis. Curr Sci 92(5):655-658
3. Bandi C, McCall JW, Genchi C, Corona S, Venco L, Sacchi L (1999) Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia. Int J Parasitol 29(2):357-364
4. Barza M, Scheife RT (1976) Antimicrobial spectrum, pharmacology, and therapeutic use of antibiotics.I. Tetracyclines. J Maine Med Assoc 67(12):368-376
5. Bonini MG, Rota C, Tomasi A, Mason RP (2006) The oxidation of 2′,7′-dichlorofluorescin to reactive oxygen species: a self-fulfilling prophesy? Free Radic Biol Med 40(6):968-975
6. Bosshardt SC, McCall JW, Coleman SH, Jones KL, Petit TA, Klei TL (1993) Prophylactic activity of tetracycline against Brugia pahangi infection in Jirds (Meriones uniguiculatus). J Parasitol 79:775-777
7. Brown CB, Wilson D, Turner D, Cameron JS, Ogg CS, Chantler C, Gill D (1974) Combined immunosuppression and anticoagulation in rapidly progressive glomerulonephritis. Lancet 2(7890):1166-1172
8. Casiraghi M, McCall JW, Simoncini L, Kramer LH, Sacchi L, Genchi C, Werren JH, Bandi C (2002) Tetracycline treatment and sex-ratio distortion: a role for Wolbachia in the moulting of filarial nematodes? Int J Parasitol 32:1457-1468
9. Chirgwin SR, Nowling JM, Coleman SU, Klei TR (2003a) Brugia pahangi and Wolbachia: the kinetics of bacteria elimination, worm viability, and host responses following tetracycline treatment. Exp Parasitol 103(1-2):16-26
10. Chirgwin SR, Coleman SU, Porthouse KH, Nowling JM, Punkosdy GA, Klei TR (2003b) Removal of Wolbachia from Brugia pahangi is closely linked to worm death and fecundity but does not result in altered lymphatic lesion formation in Mongolian gerbils (Meriones unguiculatus). Infect Immun 71(12):6986-6994
11. Cloud KA, Dillard JP (2002) A lytic transglycosylase of Neisseria gonorrhoeae is involved in peptidoglycan-derived cytotoxin production. Infect Immun 70(6):2752-2757
12. Cross HF, Haarbrink M, Egerton G, Yazdanbakhsh M, Taylor MJ (2001) Severe reactions to filarial chemotherapy and release of Wolbachia endosymbionts into blood. Lancet 358:1873-1875
13. Debrah AY, Mand S, Specht S, Marfo-Debrekyei Y, Batsa L, Pfarr K, Larbi J, Lawson B, Taylor M, Adjei O, Hoerauf A (2006) Doxycycline reduces plasma VEGF-C/sVEGFR-3 and improves pathology in lymphatic filariasis. PLoS Pathog 2(9):e92
14. Dreyer G, Addiss D, Williamson J, Norões J (2006) Efficacy of co-administered diethylcarbamazine and albendazole against adult Wuchereria bancrofti. Trans R Soc Trop Med Hyg 100(12):1118-1125
15. Foster J, Ganatra M, Kamal I, Ware J, Makarova K et al (2005) The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol 3(4):e121
16. Francis H, Awadzi K, Ottesen EA (1985) The Mazzotti reaction following treatment of onchocerciasis with diethylcarbamazine: clinical severity as a function of infection intensity. Am J Trop Med Hyg 34(3):529-536
17. Gilbert J, Nfon CK, Makepeace BL, Njongmeta LM, Hastings IM, Pfarr AR, Tanya VN, Trees AJ (2005) Antibiotic chemotherapy of onchocerciasis: in a bovine model, killing of adult parasites requires a sustained depletion of endosymbiotic bacteria (Wolbachia species). J Infect Dis 192(8):1483-1493
18. Haarbrink M, Terhell AJ, Abadi GK, Mitsui Y, Yazdanbakhsh M (1999) Inflammatory cytokines following diethylcarbamazine (DEC) treatment of different clinical groups in lymphatic filariasis. Trans R Soc Trop Med Hyg 93(6):665-672
19. Haarbrink M, Abadi GK, Buurman WA, Dentener MA, Terhell AJ, Yazdanbakhsh M (2000) Strong association of interleukin-6 and lipopolysaccharide-binding protein with severity of adverse reactions after diethylcarbamazine treatment of microfilaremic patients. J Infect Dis 182(2):564-569
20. Heider U, Blaxter M, Hoerauf A, Pfarr KM (2006) Differential display of genes expressed in the filarial nematode Litomosoides sigmodontis reveals a putative phosphate permease up-regulated after depletion of Wolbachia endobacteria. Int J Med Microbiol 296(4-5):287-299
21. Hoerauf A, Nissen-Paehle K, Schmetz C, Henkle-Durhsen K, Blaxter ML, Buttner TW, Gallin MY, Lucius R, Fleischer B (1999) Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility. J Clin Invest 103:11-18
22. Hoerauf A, Volkmann L, Hamelmann C, Adjei O, Autenreith I, Fleischer B, Buttner TW (2000) Endosymbiotic bacteria in worms as targets for a novel chemotherapy in filariasis. Lancet 355:1242-1243
23. Hoerauf A, Mand S, Fischer K, Kruppa T, Marfo-Debrekyei Y, Debrah AY, Pfarr KM, Adjei O, Buttner DW (2003a) Doxycycline as a novel strategy against bancroftian filariasis-depletion of Wolbachia endosymbionts from Wuchereria bancrofti and stop of microfilaria production. Med Microbiol Immunol 192(4):211-216
24. Hoerauf A, Mand S, Volkmann L, Büttner M, Marfo-Debrekyei Y, Taylor M, Adjei O, Büttner DW (2003b) Doxycycline in the treatment of human onchocerciasis: kinetics of Wolbachia endobacteria reduction and of inhibition of embryogenesis in female Onchocerca worms. Microbes Inf 5(4):261-273
25. Ismail MM, Jayakody RL, Weil GJ, Nirmalan N, Jayasinghe KSA, Abeyewickrema W, Rezvi Sheriff MH, Rajaratnam HN, Amarasekara N, de Silva DCL, Michalski ML, Dissanaike AL (1998) Efficacy of single dose combination of albendazole, ivermectin and diethylcarbamazine for the treatment of bancroftian filariasis. Trans Roy Soc Trop Med Hyg 92:94-97
26. Keiser PB, Reynolds SM, Awadzi K, Ottesen EA, Taylor MJ, Nutman TB (2002) Bacterial endosymbionts of Onchocerca volvulus in the pathogenesis of post-treatment reactions. J Infect Dis 185(6):805-811
27. Kirschning CJ, Schumann RR (2002) TLR2: cellular sensor for microbial and endogenous molecular patterns. Curr Top Microbiol Immunol 270:121-124
28. Langworthy NG, Renz A, Mackenstedt U, Henkle-Duhrsen K, de Bronsvoort MB, Tanya VN, Donnelly MJ, Trees AJ (2000) Macrofilaricidal activity of tetracycline against the filarial nematode Onchocerca ochengi: elimination of Wolbachia precedes worm death and suggests a dependent relationship. Proc Biol Sci 267(1448):1063-1069
29. Maizels RM, Denham DA (1992) Diethylcarbamazine (DEC): immunopharmacological interactions of an anti-filarial drug. Parasitology 105(Suppl):S49-S60
30. McGarry HF, Plant LD, Taylor MJ (2005) Diethylcarbamazine activity against Brugia malayi microfilariae is dependent on inducible nitric-oxide synthase and the cyclooxygenase pathway. Filaria J 4:4
31. Misra S, Chatterjee RK, Sen AB (1981) Antifilarial action of furazolidone. Indian J Med Res 73:725-728
32. Misra S, Mukherjee M, Dikshit M, Chatterjee RK (1998) Cellular immune response of gerbils and mastomys in experimental filariasis. Trop Med Int Health 3(2):124-129
33. Misra-Bhattacharya S, Katiyar D, Bajpai P, Tripathi RP, Saxena JK (2004) 4-Methyl-7-(tetradecanoyl)-2H-1-benzopyran-2-one: A novel DNA topoisomerase II inhibitor with adulticidal and embryostatic activity against sub-periodic Brugia malayi. Parasitol Res 92:177-182
34. Moulia-Pelat JP, Glazion P, Nguyen IN, Gaxotte P, Nicolas I (1995) Combination of ivermectin plus diethylcarbamazine, a new effective tool for control of lymphatic filariasis. Trop Med Parasitol 46:9-12
35. Ogawa T, Asai Y, Hashimoto M, Uchida H (2002) Bacterial fimbriae activate human peripheral blood monocytes utilizing TLR2, CD14 and CD11a/CD18 as cellular receptors. Eur J Immunol 32:2543-2550
36. Ottesen EA, Duke BOL, Karan M, Bebehani K (1997) Strategies and tools for control/elimination of lymphatic filariasis. Bull WHO 75:491-503
37. Owais M, Misra-Bhattacharya S, Haq W, Gupta CM (2003) Immunomodulator tuftsin augments antifilarial activity of diethylcarbamazine against experimental brugian filariasis. J Drug Target 11(4):247-251
38. Peixoto CA, Rocha A, Aguiar-Santos A, Florêncio MS (2004) The effects of diethylcarbamazine on the ultrastructure of microfilariae of Wuchereria bancrofti in vivo and in vitro. Parasitol Res 92(6):513-517
39. Pfarr KM, Hoerauf AM (2006) Antibiotics which target the Wolbachia endosymbionts of filarial parasites: a new strategy for control of filariasis and amelioration of pathology. Mini Rev Med Chem 6(2):203-210
40. Piessens WF, Beldekas M (1979) Diethylcarbamazine enhances antibody-mediated cellular adherence to Brugia malayi microfilariae. Nature 282(5741):845-847
41. Piessens WF, McGreevy PB, Piessens PW, McGreevy M, Koiman I, Saroso JS, Dennis DT (1980) Immune responses in human infections with Brugia malayi: specific cellular unresponsiveness to filarial antigens. J Clin Invest 65(1):172-179
42. Rajan TV (2004) Relationship of anti-microbial activity of tetracyclines to their ability to block the L3 to L4 molt of the human filarial parasite Brugia malayi. Am J Trop Med Hyg 71(1):24-28
43. Reuben R, Rajendran R, Sunish IP, Mani TR, Tewari SC, Hiriyan J, Gajanana A (2001) Annual single-dose diethylcarbamazine plus ivermectin for control of bancroftian filariasis: comparative efficacy with and without vector control. Ann Trop Med Parasitol 95(4):361-378
44. Sanger I, Lammler G, Kimming P (1981) Filarial infection in Mastomys natalensis and their relevance in experimental chemotherapy. Acta Trop 38:277-288
45. Segal AW, Allison AC (1978) Oxygen consumption by stimulated human neutrophils. Ciba Found Symp 65:205-223
46. Sharma DC (2002) New goals set for filariasis elimination in India. Lancet Infect Dis 2(7):389
47. Shenoy RK, George LM, John A, Suma TK, Kumaraswami V (1998) Treatment of microfilaraemia in asymptomatic brugian filariasis: the efficacy and safety of the combination of single doses of ivermectin and diethylcarbamazine. Ann Trop Med Parasitol 92:579-585
48. Simoncini L, Casiraghi M, Bazzocchi C, Sacchi L, Bandi C, Genchi C (2001) Real-time PCR for quantification of the bacterial endosymbionts (Wolbachia) of filarial nematodes. Parasitologia 43(4):173-178
49. Singh U, Misra S, Murthy PK, Katiyar JC, Agarwal A, Sircar AR (1997) Immunoreactive molecules of Brugia malayi and their diagnostic potential. Serodiagn Immunother Infect Dis 8:207-212
50. Smith HL, Rajan TV (2000) Tetracycline inhibits development of the infective-stage larvae of filarial nematodes in vitro. Exp Parasitol 95(4):265-270
51. Takeda K, Kaisho T, Akira S (2003) Toll-like receptors. Ann Rev Immunol 21:335-348
52. Taylor MJ (2003) Wolbachia in the inflammatory pathogenesis of human filariasis. Ann N Y Acad Sci 990:444-449
53. Taylor MJ, Hoerauf A (1999) Wolbachia bacteria of filarial nematodes. Parasitol Today 15(11):437-442
54. Taylor MJ, Cross HF, Bilo K (2000) Inflammatory responses induced by the filarial nematode Brugia malayi are mediated by lipopolysaccharide-like activity from endosymbiotic Wolbachia bacteria. J Exp Med 191(8):1429-1436
55. Taylor MJ, Makunde WH, McGarry HF, Turner JD, Mand S, Hoerauf A (2005) Macrofilaricidal activity after doxycycline treatment of Wuchereria bancrofti: a double-blind, randomised placebo-controlled trial. Lancet 365(9477):2116-2121
56. Townson S, Hutton D, Siemienska J, Hollick L, Scanlon T, Tagboto SK, Taylor MJ (2000) Antibiotics and Wolbachia in filarial nematodes: antifilarial activity of rifampicin, oxytetracycline and chloramphenicol against Onchocerca gutturosa, Onchocerca lienalis and Brugia pahangi. Ann Trop Med Parasitol 94(8):801-816
57. Turner JD, Langley RS, Johnston KL, Egerton G, Wanji S, Taylor MJ (2006) Wolbachia endosymbiotic bacteria of Brugia malayi mediate macrophage tolerance to TLR- and CD40-specific stimuli in a MyD88/TLR2-dependent manner. J Immunol 177(2):1240-1249
58. Tyagi K, Misra-Bhattacharya S (2003) Brugia malayi in Mastomys coucha: tetracycline a tool for transmission blocking. Curr Sci 85(5):588-589
59. Weller PF (1978) Cell-mediated immunity in experimental filariasis: lymphocyte reactivity to filarial stage-specific antigens and to B- and T-cell mitogens during acute and chronic infection. Cell Immunol 37(2):369-382
60. Zurgil N, Shafran Y, Afrimzon E, Fixler D, Shainberg A, Deutsch M (2006) Concomitant real-time monitoring of intracellular reactive oxygen species and mitochondrial membrane potential in individual living promonocytic cells. J Immunol Methods 316(1-2):27-41