Bacillus thuringiensis-derived Cry5B Has Potent Anthelmintic Activity against Ascaris suum

PLoS Neglected Tropical Diseases

Volumn 7, Issue 6, 2013, Pages

  Urban, Joseph F ^a   Hu, Yan ^b   Miller, Melanie M ^b   Scheib, Ulrike ^b   Yiu, Ying Y ^b   Aroian, Raffi V ^b  

^a BELTSVILLE HUMAN NUTRITION RESEARCH CENTER   (United States)

^b SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; ANTHELMINTIC AGENT; CRY5B; GLYCOLIPID; GLYCOSPHINGOLIPID; MITOGEN ACTIVATED PROTEIN KINASE P38; PLACEBO; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTHELMINTIC ACTIVITY; ARTICLE; ASCARIASIS; ASCARIS LUMBRICOIDES; BACILLUS THURINGIENSIS; CHEMOTHERAPY; CHROMATOGRAPHY; CONTROLLED STUDY; DRUG EFFICACY; DRUG SENSITIVITY; ENZYME ACTIVATION; FEMALE; GASTROINTESTINAL TRACT; HELMINTHIASIS; HOOKWORM INFECTION; IN VIVO STUDY; INFECTION RESISTANCE; INTOXICATION; MALE; NONHUMAN; PARASITE CULTIVATION; PROTEIN PHOSPHORYLATION; RECEPTOR BINDING; SWINE; WESTERN BLOTTING; ANIMAL; ASCARIS SUUM; DRUG EFFECTS; ISOLATION AND PURIFICATION; LARVA; METABOLISM; PARASITOLOGY; PHYSIOLOGY; SWINE DISEASES; TREATMENT OUTCOME; VETERINARY;

ANIMALS; ANTHELMINTICS; ASCARIASIS; ASCARIS SUUM; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; ENDOTOXINS; FEMALE; HEMOLYSIN PROTEINS; LARVA; SWINE; SWINE DISEASES; TREATMENT OUTCOME;

EID: 84879523123     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002263     Document Type: Article

References (50)

1. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, et al. (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367: 1521-1532.
2. Cooper PJ, Chico ME, Sandoval C, Espinel I, Guevara A, et al. (2000) Human infection with Ascaris lumbricoides is associated with a polarized cytokine response. The Journal of infectious diseases 182: 1207-1213.
3. Cooper PJ, Chico ME, Losonsky G, Sandoval C, Espinel I, et al. (2000) Albendazole treatment of children with ascariasis enhances the vibriocidal antibody response to the live attenuated oral cholera vaccine CVD 103-HgR. The Journal of infectious diseases 182: 1199-1206.
4. Dold C, Holland CV, (2011) Ascaris and ascariasis. Microbes and infection/Institut Pasteur 13: 632-637.
5. Izumikawa K, Kohno Y, Hara K, Hayashi H, Maruyama H, et al. (2011) Eosinophilic pneumonia due to visceral larva migrans possibly caused by Ascaris suum: a case report and review of recent literatures. Japanese journal of infectious diseases 64: 428-432.
6. Wani I, Rather M, Naikoo G, Amin A, Mushtaq S, et al. (2010) Intestinal ascariasis in children. World journal of surgery 34: 963-968.
7. Adugna S, Kebede Y, Moges F, Tiruneh M, (2007) Efficacy of mebendazole and albendazole for Ascaris lumbricoides and hookworm infections in an area with long time exposure for antihelminthes, Northwest Ethiopia. Ethiopian medical journal 45: 301-306.
8. Stothard JR, Rollinson D, Imison E, Khamis IS, (2009) A spot-check of the efficacies of albendazole or levamisole, against soil-transmitted helminthiases in young Ungujan children, reveals low frequencies of cure. Annals of tropical medicine and parasitology 103: 357-360.
9. Vercruysse J, Behnke JM, Albonico M, Ame SM, Angebault C, et al. (2011) Assessment of the anthelmintic efficacy of albendazole in school children in seven countries where soil-transmitted helminths are endemic. PLoS neglected tropical diseases 5: e948.
10. Kaminsky R, Ducray P, Jung M, Clover R, Rufener L, et al. (2008) A new class of anthelmintics effective against drug-resistant nematodes. Nature 452: 176-180.
11. Roepstorff A, Mejer H, Nejsum P, Thamsborg SM, (2011) Helminth parasites in pigs: new challenges in pig production and current research highlights. Veterinary parasitology 180: 72-81.
12. Dawson HD, Beshah E, Nishi S, Solano-Aguilar G, Morimoto M, et al. (2005) Localized multigene expression patterns support an evolving Th1/Th2-like paradigm in response to infections with Toxoplasma gondii and Ascaris suum. Infection and immunity 73: 1116-1128.
13. Roneus O, (1966) Studies on the aetiology and pathogenesis of white spots in the liver of pigs. Acta veterinaria Scandinavica 7: Suppl 16: 11-112.
14. Steenhard NR, Jungersen G, Kokotovic B, Beshah E, Dawson HD, et al. (2009) Ascaris suum infection negatively affects the response to a Mycoplasma hyopneumoniae vaccination and subsequent challenge infection in pigs. Vaccine 27: 5161-5169.
15. Urban JF Jr, Steenhard NR, Solano-Aguilar GI, Dawson HD, Iweala OI, et al. (2007) Infection with parasitic nematodes confounds vaccination efficacy. Veterinary parasitology 148: 14-20.
16. Leles D, Gardner SL, Reinhard K, Iniguez A, Araujo A, (2012) Are Ascaris lumbricoides and Ascaris suum a single species? Parasites & vectors 5: 42.
17. Roh JY, Choi JY, Li MS, Jin BR, Je YH, (2007) Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control. Journal of microbiology and biotechnology 17: 547-559.
18. Betz FS, Hammond BG, Fuchs RL, (2000) Safety and advantages of Bacillus thuringiensis-protected plants to control insect pests. Regulatory toxicology and pharmacology: RTP 32: 156-173.
19. Sanahuja G, Banakar R, Twyman RM, Capell T, Christou P, (2011) Bacillus thuringiensis: a century of research, development and commercial applications. Plant biotechnology journal 9: 283-300.
20. Griffitts JS, Aroian RV, (2005) Many roads to resistance: how invertebrates adapt to Bt toxins. BioEssays: news and reviews in molecular, cellular and developmental biology 27: 614-624.
21. Cappello M, Bungiro RD, Harrison LM, Bischof LJ, Griffitts JS, et al. (2006) A purified Bacillus thuringiensis crystal protein with therapeutic activity against the hookworm parasite Ancylostoma ceylanicum. Proceedings of the National Academy of Sciences of the United States of America 103: 15154-15159.
22. Hu Y, Georghiou SB, Kelleher AJ, Aroian RV, (2010) Bacillus thuringiensis Cry5B protein is highly efficacious as a single-dose therapy against an intestinal roundworm infection in mice. PLoS neglected tropical diseases 4: e614.
23. Hu Y, Zhan B, Keegan B, Yiu YY, Miller MM, et al. (2012) Mechanistic and Single-Dose In Vivo Therapeutic Studies of Cry5B Anthelmintic Action against Hookworms. PLoS neglected tropical diseases 6: e1900.
24. Conlan JV, Khamlome B, Vongxay K, Elliot A, Pallant L, et al. (2012) Soil-transmitted helminthiasis in Laos: a community-wide cross-sectional study of humans and dogs in a mass drug administration environment. The American journal of tropical medicine and hygiene 86: 624-634.
25. Behnke JM, Menge DM, Noyes H, (2009) Heligmosomoides bakeri: a model for exploring the biology and genetics of resistance to chronic gastrointestinal nematode infections. Parasitology 136: 1565-1580.
26. Barrows BD, Haslam SM, Bischof LJ, Morris HR, Dell A, et al. (2007) Resistance to Bacillus thuringiensis toxin in Caenorhabditis elegans from loss of fucose. The Journal of biological chemistry 282: 3302-3311.
27. Griffitts JS, Haslam SM, Yang T, Garczynski SF, Mulloy B, et al. (2005) Glycolipids as receptors for Bacillus thuringiensis crystal toxin. Science 307: 922-925.
28. Griffitts JS, Huffman DL, Whitacre JL, Barrows BD, Marroquin LD, et al. (2003) Resistance to a bacterial toxin is mediated by removal of a conserved glycosylation pathway required for toxin-host interactions. The Journal of biological chemistry 278: 45594-45602.
29. Griffitts JS, Whitacre JL, Stevens DE, Aroian RV, (2001) Bt toxin resistance from loss of a putative carbohydrate-modifying enzyme. Science 293: 860-864.
30. Hui F, Scheib U, Hu Y, Sommer RJ, Aroian RV, et al. (2012) Structure and Glycolipid Binding Properties of the Nematicidal Protein Cry5B. Biochemistry.
31. Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, et al. (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392: 71-75.
32. Slotved HC, Barnes EH, Eriksen L, Roepstorff A, Nansen P, et al. (1997) Use of an agar-gel technique for large scale application to recover Ascaris suum larvae from intestinal contents of pigs. Acta veterinaria Scandinavica 38: 207-212.
33. Barrows BD, Griffitts JS, Aroian RV, (2006) Caenorhabditis elegans carbohydrates in bacterial toxin resistance. Methods in enzymology 417: 340-358.
34. Hu Y, Platzer EG, Bellier A, Aroian RV, (2010) Discovery of a highly synergistic anthelmintic combination that shows mutual hypersusceptibility. Proceedings of the National Academy of Sciences of the United States of America 107: 5955-5960.
35. Douvres FW, Tromba FG, Malakatis GM, (1969) Morphogenesis and migration of Ascaris suum larvae developing to fourth stage in swine. The Journal of parasitology 55: 689-712.
36. Bischof LJ, Kao CY, Los FC, Gonzalez MR, Shen Z, et al. (2008) Activation of the unfolded protein response is required for defenses against bacterial pore-forming toxin in vivo. PLoS pathogens 4: e1000176.
37. Kao CY, Los FC, Huffman DL, Wachi S, Kloft N, et al. (2011) Global functional analyses of cellular responses to pore-forming toxins. PLoS pathogens 7: e1001314.
38. Friedl CH, Lochnit G, Zahringer U, Bahr U, Geyer R, (2003) Structural elucidation of zwitterionic carbohydrates derived from glycosphingolipids of the porcine parasitic nematode Ascaris suum. The Biochemical journal 369: 89-102.
39. van Riet E, Wuhrer M, Wahyuni S, Retra K, Deelder AM, et al. (2006) Antibody responses to Ascaris-derived proteins and glycolipids: the role of phosphorylcholine. Parasite immunology 28: 363-371.
40. Jacela JY, DeRouchey JM, Tokach MD, Goodband RD, Nelssen JL, et al. (2009) Feed additives for swine: Fact sheets- carcass modifiers, carbohydrate-degrading enzymes and proteases, and anthelmintics. Journal of Swine Health and Production 17: 325-327.
41. Morimoto M, Zarlenga D, Beard H, Alkharouf N, Matthews BF, et al. (2003) Ascaris suum: cDNA microarray analysis of 4th stage larvae (L4) during self-cure from the intestine. Experimental parasitology 104: 113-121.
42. Roepstorff A, Eriksen L, Slotved HC, Nansen P, (1997) Experimental Ascaris suum infection in the pig: worm population kinetics following single inoculations with three doses of infective eggs. Parasitology 115 (Pt 4):: 443-452.
43. Domeneghini C, Di Giancamillo A, Arrighi S, Bosi G, (2006) Trophic feed additives and their effects upon the gut structure and intestinal metabolism. State of the art in the pig, and perspectives towards humans. Histology and Histopathology 21: 273-283.
44. Lamendella R, Domingo JW, Ghosh S, Martinson J, Oerther DB, (2011) Comparative fecal metagenomics unveils unique functional capacity of the swine gut. BMC microbiology 11: 103.
45. Tritten L, Silbereisen A, Keiser J, (2011) In vitro and in vivo efficacy of Monepantel (AAD 1566) against laboratory models of human intestinal nematode infections. PLoS neglected tropical diseases 5: e1457.
46. Li XQ, Tan A, Voegtline M, Bekele S, Chen CS, et al. (2008) Expression of Cry5B protein from Bacillus thuringiensis in plant roots confers resistance to root-knot nematode. Biological Control 47: 97-102.
47. Zhang F, Peng D, Ye X, Yu Z, Hu Z, et al. (2012) In vitro uptake of 140 kDa Bacillus thuringiensis nematicidal crystal proteins by the second stage juvenile of Meloidogyne hapla. PloS one 7: e38534.
48. Kotze AC, O'Grady J, Gough JM, Pearson R, Bagnall NH, et al. (2005) Toxicity of Bacillus thuringiensis to parasitic and free-living life-stages of nematode parasites of livestock. International journal for parasitology 35: 1013-1022.
49. Getachew T, Dorchies P, Jacquiet P, (2007) Trends and challenges in the effective and sustainable control of Haemonchus contortus infection in sheep. Review. Parasite 14: 3-14.
50. Reinemeyer CR, (2012) Anthelmintic resistance in non-strongylid parasites of horses. Veterinary parasitology 185: 9-15.