Paenibacillus larvae enolase as a virulence factor in honeybee larvae infection

Veterinary Microbiology

Volumn 147, Issue 1-2, 2011, Pages 83-89

  Antúnez, Karina ^a   Anido, Matilde ^a   Arredondo, Daniela ^a   Evans, Jay D ^b   Zunino, Pablo ^a  

^a INSTITUTO DE INVESTIGACIONES BIOLÓGICAS CLEMENTE ESTABLE   (Uruguay)

^b USDA ARS Bee Research Laboratory   (United States)

Author keywords

American foulbrood; Enolase; Paenibacillus larvae

Indexed keywords

ENOLASE; MILK PROTEIN; PLASMINOGEN; PROTEIN; RECOMBINANT ENOLASE; RECOMBINANT ENZYME; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

AMERICAN FOULBROOD; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL SPORE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME SYNTHESIS; FEMALE; HONEYBEE; IMMUNITY; IMMUNIZATION; IMMUNOGENICITY; IN VIVO STUDY; MICROBIAL DEGRADATION; MOUSE; NONHUMAN; PAENIBACILLUS; PAENIBACILLUS LARVAE; PROTEIN HYDROLYSIS; VEGETATIVE STAGE;

ANIMALS; BEES; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNE SERA; IN SITU HYBRIDIZATION, FLUORESCENCE; LARVA; MILK PROTEINS; PAENIBACILLUS; PHOSPHOPYRUVATE HYDRATASE; SPORES, BACTERIAL; VIRULENCE FACTORS;

APIS MELLIFERA; HEXAPODA; PAENIBACILLUS LARVAE; POSIBACTERIA;

EID: 78649498398     PISSN: 03781135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetmic.2010.06.004     Document Type: Article

References (39)

1. Andrews B.A., Asenjo A.J. Synthesis and regulation of extracellular beta (1-3) glucanase and protease by cytophaga sp. In batch and continuous culture. Biotechnology Bioengineering 1986, 28:1366-1375.
2. Antúnez K., Anido M., Evans J.D., Zunino P. Secreted and immunogenic proteins produced by the honeybee bacterial pathogen, Paenibacillus larvae. Veterinary Microbiology 2010, 141:385-389.
3. Antúnez K., Anido M., Schlapp G., Evans J.D., Zunino P. Characterization of secreted proteases of Paenibacillus larvae, potential virulence factors involved in honeybee larval infection. Journal of Invertebrate Pathology 2009, 102:129-132.
4. Antunez K, D'Alessandro B., Piccini C., Corbella E., Zunino P. Paenibacillus larvae larvae spores in honey samples from Uruguay: a nationwide survey. Journal of Invertebrate Pathology 2004, 86:56-58.
5. Antunez K., Piccini C., Castro-Sowinski S., Rosado A.S., Seldin L., Zunino P. Phenotypic and genotypic characterization of Paenibacillus larvae isolates. Veterinary Microbiology 2007, 124:178-183.
6. Bastian E.D., Brown R.J. Plasmin in milk and dairy products: an update. International Dairy Journal 1996, 6:435-457.
7. Bergmann S., Rohde M., Chhatwal G.S., Hammerschmidt S. alpha-Enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Molecular Microbiology 2001, 40:1273-1287.
8. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976, 72:248-254.
9. Bullock W.O., Fernandes J.M., Short J.M. XL1-Blue: a high efficiency plasmid transforming recA Escherichia coli strain with beta-galactosidase selection. Biotechniques 1987, 5:376.
10. Castro-Sowinski S., Cantera A.M. A rapid and inexpensive procedure for the determination of protelytic activity. Biochemical Education 1995, 23:41-43.
11. Corona M., Velarde R.A., Remolina S., Moran-Lauter A., Wang Y., Hughes K.A., Robinson G.E. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:7128-7133.
12. Chitlaru T., Gat O., Grosfeld H., Inbar I., Gozlan Y., Shafferman A. Identification of in vivo-expressed immunogenic proteins by serological proteome analysis of the Bacillus anthracis secretome. Infection and Immunity 2007, 75:2841-2852.
13. D'Alessandro B., Antunez K., Piccini C., Zunino P. DNA extraction and PCR detection of Paenibacillus larvae spores from naturally contaminated honey and bees using spore-decoating and freeze-thawing techniques. World Journal of Microbiology and Biotechnology 2007, 23:593-597.
14. Decanini L.I., Collins A.M., Evans J.D. Variation and heritability in immune gene expression by diseased honeybees. Journal of Heredity 2007, 98:195-201.
15. Delvecchio V.G., Connolly J.P., Alefantis T.G., Walz A., Quan M.A., Patra G., Ashton J.M., Whittington J.T., Chafin R.D., Liang X., Grewal P., Khan A.S., Mujer C.V. Proteomic profiling and identification of immunodominant spore antigens of Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis. Applied and Environmental Microbiology 2006, 72:6355-6363.
16. Evans J.D. Transcriptional immune responses by honey bee larvae during invasion by the bacterial pathogen, Paenibacillus larvae. Journal of Invertebrate Pathology 2004, 85:105-111.
17. Evans J.D., Lopez D.L. Bacterial probiotics induce an immune response in the honey bee (Hymenoptera: Apidae). Journal of Economic Entomology 2004, 97:752-756.
18. Genersch E., Forsgren E., Pentikainen J., Ashiralieva A., Rauch S., Kilwinski J., Fries I. Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation. International Journal of Systematic and Evolutionary Microbiology 2006, 56:501-511.
19. Hahn B.S., Cho S.Y., Ahn M.Y., Kim Y.S. Purification and characterization of a plasmin-like protease from Tenodera sinensis (Chinese mantis). Insect Biochemistry and Molecular Biology 2001, 31:573-581.
20. Hansen H., Brødsgaard C.J. American foulbrood: a review of its biology, diagnosis and control. Bee World 1999, 80:5-23.
21. Holst E.C., Sturtevant A.P. Relation of proteolytic enzymes to phase of life cycle of Bacillus larvae, and two new culture media for this organism. Journal of Bacteriology 1940, 40:723-731.
22. Hornitzky M.A.Z, Nicholls P.J. J medium is superior to sheep blood agar and brain heart infusion for the isolation of Bacillus larvae from honey samples. Journal of Apicultural Research 1993, 32:51-52.
23. Hurmalainen V., Edelman S., Antikainen J., Baumann M., Lahteenmaki K., Korhonen T.K. Extracellular proteins of Lactobacillus crispatus enhance activation of human plasminogen. Microbiology 2007, 153:1112-1122.
24. Kokabiyic S., Özdemir I. Purification and characterization of an intracellular chymotrypsin-like serine protease from Thermoplasma volcanium. Bioscience, Biotechnology, and Biochemistry 2006, 70:126-134.
25. Lamonica J.M., Wagner M., Eschenbrenner M., Williams L.E., Miller T.L., Patra G., DelVecchio V.G. Comparative secretome analyses of three Bacillus anthracis strains with variant plasmid contents. Infection and Immunity 2005, 73:3646-3658.
26. Moore B. Biofunctional and moonlighting enzymes: lighting the way to regulatory control. Trends in Plant Science 2004, 9:221-228.
27. Murphy G., Stanton H., Cowell S., Butler G., Knauper V., Atkinson S., Gavrilovic J. Mechanisms for pro matrix metalloproteinase activation. APMIS: acta pathologica. Microbiologica et Immunologica Scandinavica 1999, 107:38-44.
28. Pancholi V., Fischetti V.A. alpha-Enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci. Journal of Biological Chemistry 1998, 273:14503-14515.
29. Piccini C, D'Alessandro B., Antunez K., Zunino P. Detection of Paenibacillus larvae subspecies larvae spores in naturally infected bee larvae and artificially contaminated honey by PCR. World Journal of Microbiology and Biotechnology 2002, 18:761-765.
30. Plow E.F., Herren T., Redlitz A., Miles L.A., Hoover-Plow J.L. The cell biology of the plasminogen system. The FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 1995, 9:939-945.
31. Qin X., Evans J.D., Aronstein K.A., Murray K.D., Weinstock G.M. Genome sequences of the honey bee pathogens Paenibacillus larvae and Ascosphaera apis. Insect Molecular Biology 2006, 15:715-718.
32. Sha J., Erova T.E., Alyea R.A., Wang S., Olano J.P., Pancholi V., Chopra A.K. Surface-expressed enolase contributes to the pathogenesis of clinical isolate SSU of Aeromonas hydrophila. Journal of Bacteriology 2009, 191:3095-3107.
33. Sha J., Galindo C.L., Pancholi V., Popov V.L., Zhao Y., Houston C.W., Chopra A.K. Differential expression of the enolase gene under in vivo versus in vitro growth conditions of Aeromonas hydrophila. Microbial Pathogenesis 2003, 34:195-204.
34. Studier F.W., Moffatt B.A. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. Journal of Molecular Biology 1986, 189:113-130.
35. Whiting G.C., Evans J.T., Patel S., Gillespie S.H. Purification of native alpha-enolase from Streptococcus pneumoniae that binds plasminogen and is immunogenic. Journal of Medical Microbiology 2002, 51:837-843.
36. Whiting G.C., Rijpkema S., Adams T., Corbel M.J. Characterisation of adsorbed anthrax vaccine by two-dimensional gel electrophoresis. Vaccine 2004, 22:4245-4251.
37. Woodrow A.W. Susceptibility of honeybee larvae to individual inoculations with spores of Bacillus larvae. Journal of Economic Entomology 1942, 35.
38. Woodrow A.W., Holst E.C. The mechanism of colony resistance to American fouldbrood. Journal of Economic Entomology 1942, 35:327-330.
39. Yue D., Nordhoff M., Wieler L.H., Genersch E. Fluorescence in situ hybridization (FISH) analysis of the interactions between honeybee larvae and Paenibacillus larvae, the causative agent of American foulbrood of honeybees (Apis mellifera). Environmental Microbiology 2008, 10:1612-1620.