Insecticidal toxins from Photorhabdus bacteria and their potential use in agriculture

Toxicon

Volumn 49, Issue 4, 2007, Pages 436-451

  ffrench Constant, Richard H ^a   Dowling, Andrea ^b   Waterfield, Nicholas R ^b  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b University of Bath   (United Kingdom)

Author keywords

Photorhabdus; Photorhabdus virulence cassettes; Protein insecticides; Toxin complexes; Xenorhabdus

Indexed keywords

BACTERIAL TOXIN; INSECTICIDE; PROTEIN MCF1; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

AGRICULTURE; BACTERIAL GENE; BACTERIAL VIRULENCE; BIOLOGICAL PEST CONTROL; ENTOMOPATHOGENIC NEMATODE; GENE CASSETTE; NONHUMAN; PHOTORHABDUS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SYMBIONT; TOXICITY; XENORHABDUS;

AGRICULTURE; ANIMALS; BACTERIAL TOXINS; INSECTICIDES; PEST CONTROL, BIOLOGICAL; PHOTORHABDUS; PLANTS, GENETICALLY MODIFIED;

ARABIDOPSIS; BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS); HEXAPODA; LEPTINOTARSA DECEMLINEATA; MAMMALIA; NEMATODA; PHOTORHABDUS; XENORHABDUS;

EID: 33847348344     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2006.11.019     Document Type: Review

References (59)

1. Blackburn M., Golubeva E., Bowen D., and ffrench-Constant R.H. A novel insecticidal toxin from Photorhabdus luminescens: histopathological effects of Toxin complex A (Tca) on the midgut of Manduca sexta. Appl. Environ. Microbiol. 64 (1998) 3036-3041
2. Blanke S.R. Micro-managing the executioner: pathogen targeting of mitochondria. Trends Microbiol. 13 (2005) 64-71
3. Bouillet P., and Strasser A. BH3-only proteins-evolutionarily conserved proapoptotic Bcl-2 family members essential for initiating programmed cell death. J. Cell. Sci. 115 (2002) 1567-1574
4. Bowen D.J., and Ensign J.C. Purification and characterization of a high molecular weight insecticidal protein complex produced by the entomopathogenic bacterium Photorhabdus luminescens. Appl. Environ. Microbiol. 64 (1998) 3029-3035
5. Bowen D., Rocheleau T.A., Blackburn M., Andreev O., Golubeva E., Bhartia R., and ffrench-Constant R.H. Insecticidal toxins from the bacterium Photorhabdus luminescens. Science 280 (1998) 2129-2132
6. Cheng E.H., Wei M.C., Weiler S., Flavell R.A., Mak T.W., Lindsten T., and Korsmeyer S.J. BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol. Cell 8 (2001) 705-711
7. Ciche T.A., and Ensign J.C. For the insect pathogen Photorhabdus luminescens, which end of a nematode is out?. Appl. Environ. Microbiol. 69 (2003) 1890-1897
8. Crosland R.D., Hsiao T.H., and McClure W.O. Purification and characterization of beta-leptinotarsin-h, an activator of presynaptic calcium channels. Biochemistry 23 (1984) 734-741
9. Crosland R.D., Fitch R.W., and Hines H.B. Characterization of beta-leptinotarsin-h and the effects of calcium flux antagonists on its activity. Toxicon 45 (2005) 829-841
10. Daborn P.J., Waterfield N., Silva C.P., Au C.P., Sharma S., and ffrench-Constant R.H. A single Photorhabdus gene, makes caterpillars floppy (mcf), allows E. coli to persist within and kill insects. Proc. Nat. Acad. Sci. USA 99 (2002) 10742-10747
11. Daborn P.J., Waterfield N., Silva C.P., Au C.P.Y., Sharma S., and ffrench-Constant R.H. A single Photorhabdus gene makes caterpillars floppy (mcf) allows Esherichia coli to persist within and kill insects. Proc. Nat. Acad. Sci. USA 99 (2002) 10742-10747
12. 2+-induced permeability transition of isolated mitochondria. J. Biol. Chem.
13. Dove C.H., Wang S.-Z., Price S.B., Phelps C.J., Lyerly D.M., Wilkins T.D., and Johnson J.L. Molecular characterization of the Clostridium difficile toxin A gene. Infect. Immun. 58 (1990) 480-488
14. Dowling A.J., Daborn P.J., Waterfield N.R., Wang P., Streuli C.H., and ffrench-Constant R.H. The insecticidal toxin Makes caterpillars floppy (Mcf) promotes apoptosis in mammalian cells. Cell. Microbiol. 6 (2004) 345-353
15. Duchaud E., Rusniok C., Frangeul L., Buchrieser C., Givaudan A., Taourit S., Bocs S., Boursaux-Eude C., Chandler M., Charles J.F., Dassa E., Derose R., Derzelle S., Freyssinet G., Gaudriault S., Medigue C., Lanois A., Powell K., Siguier P., Vincent R., Wingate V., Zouine M., Glaser P., Boemare N., Danchin A., and Kunst F. The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nat. Biotechnol. 21 (2003) 1307-1313
16. Enright M.R., and Griffin C.T. Specificity of association between Paenibacillus spp. and the entomopathogenic nematodes, Heterorhabditis spp. Microb. Ecol. 48 (2004) 414-423
17. Enright M.R., and Griffin C.T. Effects of Paenibacillus nematophilus on the entomopathogenic nematode Heterorhabditis megidis. J. Invertebr. Pathol. 88 (2005) 40-48
18. ffrench-Constant R., Waterfield N., Daborn P., Joyce S., Bennett H., Au C., Dowling A., Boundy S., Reynolds S., and Clarke D. Photorhabdus: towards a functional genomic analysis of a symbiont and pathogen. FEMS Microbiol. Rev. 26 (2003) 433-456
19. ffrench-Constant R.H., Waterfield N., and Daborn P. Insecticidal toxins from Photorhabdus and Xenorhabdus. Compr. Mol. Insect Sci. 5 (2004) 239-253
20. Forst S., and Clarke D. Bacteria-nematode symbiosis. In: Gaugler R. (Ed). Entomopathogenic Nematology (2002), CAB International, London 57-77
21. Gerrard J., Waterfield N., Vohra R., and ffrench-Constant R. Human infection with Photorhabdus asymbiotica: an emerging bacterial pathogen. Microb. Infect. 6 (2004) 229-237
22. Gonzalez-Garcia M., Perez-Ballestero R., Ding L., Duan L., Boise L.H., Thompson C.B., and Nunez G. bcl-XL is the major bcl-x mRNA form expressed during murine development and its product localizes to mitochondria. Development 120 (1994) 3033-3042
23. Heimlich G., McKinnon A.D., Bernardo K., Brdiczka D., Reed J.C., Kain R., Kronke M., and Jurgensmeier J.M. Bax-induced cytochrome c release from mitochondria depends on alpha-helices-5 and -6. Biochem. J. 378 (2004) 247-255
24. Hey, T.D., Schleper, A.D., Bevan, S.A., Bintrim, S.B., Mitchell, J.C., Lize, S., Ni, W., Zhu, B., Merlo, D.J., Apel-Birkhold, P., 2004. Mixing and matching Tc proteins for pest control. World Intellectual Property Patent number WO2004067727.
25. Heyndrickx, M., Vandemeulebroecke, K., Hoste, B., Janssen, P., Kersters, K., De Vos, P., Logan, N.A., Ali, N., Berkeley, R.C., 1996. Reclassification of Paenibacillus (formerly Bacillus) pulvifaciens (Nakamura 1984) Ash et al. 1994, a later subjective synonym of Paenibacillus (formerly Bacillus) larvae (White 1906) Ash et al. 1994, as a subspecies of P. larvae, with emended descriptions of P. larvae as P. larvae subsp. larvae and P. larvae subsp. pulvifaciens. Int. J. Syst. Bacteriol. 46, 270-279.
26. Hockenbery D., Nunez G., Milliman C., Schreiber R.D., and Korsmeyer S.J. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348 (1990) 334-336
27. Hofmann F., Busch C., Prepens U., Just I., and Aktories K. Localization of the glucosyltransferase activity of Clostridium difficile toxin B to the N-terminal part of the holotoxin. J. Biol. Chem. 272 (1997) 11074-11078
28. Hurst M.R., Glare T.R., Jackson T.A., and Ronson C.W. Plasmid-located pathogenicity determinants of Serratia entomophila, the causal agent of amber disease of grass grub, show similarity to the insecticidal toxins of Photorhabdus luminescens. J. Bacteriol. 182 (2000) 5127-5138
29. Hurst M.R., Glare T.R., and Jackson T.A. Cloning Serratia entomophila antifeeding genes-a putative defective prophage active against the grass grub Costelytra zealandica. J. Bacteriol. 186 (2004) 5116-5128
30. Kramer S.J., and DeKort C.A. Age-dependent changes in juvenile hormone esterase and general carboxyesterase activity in the hemolymph of the colorado potato beetle, Leptinotarsa decemlineata. Mol. Cell. Endocrinol. 4 (1975) 43-53
31. Landraud L., Pulcini C., Gounon P., Flatau G., Boquet P., and Lemichez E. E. coli CNF1 toxin: a two-in-one system for host-cell invasion. Int. J. Med. Microbiol. 293 (2004) 513-518
32. Liu D., Burton S., Glancy T., Li Z.S., Hampton R., Meade T., and Merlo D.J. Insect resistance conferred by 283-kDa Photorhabdus luminescens protein TcdA in Arabidopsis thaliana. Nat. Biotechnol. 21 (2003) 1307-1313
33. Lutter M., Perkins G.A., and Wang X. The pro-apoptotic Bcl-2 family member tBid localizes to mitochondrial contact sites. BMC Cell Biol. 2 (2001) 22
34. Madeddu L., Pozzan T., Robello M., Rolandi R., Hsiao T.H., and Meldolesi J. Leptinotoxin-h action in synaptosomes, neurosecretory cells, and artificial membranes: stimulation of ion fluxes. J. Neurochem. 45 (1985) 1708-1718
35. Miljanich G.P., Yeager R.E., and Hsiao T.H. Leptinotarsin-D, a neurotoxic protein, evokes neurotransmitter release from, and calcium flux into, isolated electric organ nerve terminals. J. Neurobiol. 19 (1988) 373-386
36. Morgan J.A., Sergeant M., Ellis D., Ousley M., and Jarrett P. Sequence analysis of insecticidal genes from Xenorhabdus nematophilus PMFI296. Appl. Environ. Microbiol. 67 (2001) 2062-2069
37. Parkhill J., Wren B.W., Thomson N.R., Titball R.W., Holden M.T., Prentice M.B., Sebaihia M., James K.D., Churcher C., Mungall K.L., Baker S., Basham D., Bentley S.D., Brooks K., Cerdeno-Tarraga A.M., Chillingworth T., Cronin A., Davies R.M., Davis P., Dougan G., Feltwell T., Hamlin N., Holroyd S., Jagels K., Karlyshev A.V., Leather S., Moule S., Oyston P.C., Quail M., Rutherford K., Simmonds M., Skelton J., Stevens K., Whitehead S., and Barrell B.G. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413 (2001) 523-527
38. Perry R.D., and Fetherston J.D. Yersinia pestis-etiologic agent of plague. Clin. Microbiol. Rev. 10 (1997) 35-66
39. Sattler M., Liang H., Nettesheim D., Meadows R.P., Harlan J.E., Eberstadt M., Yoon H.S., Shuker S.B., Chang B.S., Minn A.J., Thompson C.B., and Fesik S.W. Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 275 (1997) 983-986
40. Schaller A., Kuhn R., Kuhnert P., Nicolet J., Anderson T.J., MacInnes J.I., Segers R.P., and Frey J. Characterization of apxIVA, a new RTX determinant of Actinobacillus pleuropneumoniae. Microbiology 145 (1999) 2105-2116
41. Sergeant M., Jarrett P., Ousley M., and Morgan J.A. Interactions of insecticidal toxin gene products from Xenorhabdus nematophilus PMFI296. Appl. Environ. Microbiol. 69 (2003) 3344-3349
42. Valentijn, A.J., Gilmore, A.P., 2004. Translocation of full-length bid to mitochondria during Anoikis. J. Biol. Chem.
43. Vermunt A.M., Koopmanschap A.B., Vlak J.M., and de Kort C.A. Cloning and sequence analysis of cDNA encoding a putative juvenile hormone esterase from the Colorado potato beetle. Insect Biochem. Mol. Biol. 27 (1997) 919-928
44. Vermunt A.M., Vermeesch A.M., and de Kort C.A. Purification and characterization of juvenile hormone esterase from hemolymph of the Colorado potato beetle. Arch. Insect Biochem. Physiol. 35 (1997) 261-277
45. von der Weid I., Alviano D.S., Santos A.L., Soares R.M., Alviano C.S., and Seldin L. Antimicrobial activity of Paenibacillus peoriae strain NRRL BD-62 against a broad spectrum of phytopathogenic bacteria and fungi. J. Appl. Microbiol. 95 (2003) 1143-1151
46. Waterfield N., Dowling A., Sharma S., Daborn P.J., Potter U., and ffrench-Constant R.H. Oral toxicity of Photorhabdus luminescens W14 toxin complexes in E. coli. Appl. Environ. Microbiol. 67 (2001) 5017-5024
47. Waterfield N.R., Bowen D.J., Fetherston J.D., Perry R.D., and ffrench-Constant R.H. The tc genes of Photorhabdus: a growing family. Trends Microbiol. 9 (2001) 185-191
48. Waterfield N., Daborn P.J., and ffrench-Constant R.H. Genomic islands in Photorhabdus. Trends Microbiol. 10 (2002) 541-545
49. Waterfield N.R., Daborn P.J., Dowling A.J., Yang G., Hares M., and ffrench-Constant R.H. The insecticidal toxin Makes caterpillars floppy 2 (Mcf2) shows similarity to HrmA, an avirulence protein from a plant pathogen. FEMS Microbiol. Lett. 229 (2003) 265-270
50. Waterfield N.R., Daborn P.J., and ffrench-Constant R.H. Insect pathogenicity islands in the insect pathogenic bacterium Photorhabdus. Physiol. Entomol. 29 (2004) 240-250
51. Waterfield N., Hares M., Dowling A., and ffrench-Constant R. Potentiation and cellular phenotypes of the insecticidal Toxin complexes of Photorhabdus bacteria. Cell. Microbiol. 7 (2005) 373-382
52. Waterfield N., Kamita S.G., Hammock B.D., and ffrench-Constant R. The Photorhabdus Pir toxins are similar to a developmentally regulated insect protein but show no juvenile hormone esterase activity. FEMS Microbiol. Lett. 245 (2005) 47-52
53. Wei M.C., Lindsten T., Mootha V.K., Weiler S., Gross A., Ashiya M., Thompson C.B., and Korsmeyer S.J. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 14 (2000) 2060-2071
54. Wei M.C., Zong W.X., Cheng E.H., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacGregor G.R., Thompson C.B., and Korsmeyer S.J. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292 (2001) 727-730
55. Weinrauch Y., and Zychlinsky A. The induction of apoptosis by bacterial pathogens. Annu. Rev. Microbiol. 53 (1999) 155-187
56. Wolter K.G., Hsu Y.T., Smith C.L., Nechushtan A., Xi X.G., and Youle R.J. Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell. Biol. 139 (1997) 1281-1292
57. Zamzami N., and Kroemer G. Apoptosis: mitochondrial membrane permeabilization-the (w)hole story?. Curr. Biol. 13 (2003) R71-R73
58. Zha H., Aime-Sempe C., Sato T., and Reed J.C. Proapoptotic protein Bax heterodimerizes with Bcl-2 and homodimerizes with Bax via a novel domain (BH3) distinct from BH1 and BH2. J. Biol. Chem. 271 (1996) 7440-7444
59. Zumbihl R., Aepfelbacher M., Andor A., Jacobi C.A., Ruckdeschel K., Rouot B., and Heesemann J. The cytotoxin YopT of Yersinia enterocolitica induces modification and cellular redistribution of the small GTP-binding protein RhoA. J. Biol. Chem. 274 (1999) 29289-29293