Biosynthesis of anatoxin-a and analogues (anatoxins) in cyanobacteria

Toxicon

Volumn 91, Issue , 2014, Pages 15-22

  Méjean, Annick ^a   Paci, Guillaume ^a   Gautier, Valérie ^a   Ploux, Olivier ^a,b  

^a Bât Condorcet   (France)

^b PSL RESEARCH UNIVERSITY   (France)

Author keywords

Anatoxin a; Biosynthesis; Cyanobacteria; Dihydroanatoxin a; Homoanatoxin a; Polyketide synthase

Indexed keywords

ANATOXIN A; DIHYDROANATOXIN A; DIHYDROHOMOANATOXIN A; HOMOANATOXIN A; OXIDOREDUCTASE; UNCLASSIFIED DRUG; TROPANE DERIVATIVE;

ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATION; BIOSYNTHESIS; CYANOBACTERIUM; CYLINDROSPERMUM STAGNALE; ENZYME STRUCTURE; ENZYMOLOGY; GENE CLUSTER; IN VITRO STUDY; NONHUMAN; OSCILLATORIA; PREDICTION; SITE DIRECTED MUTAGENESIS; BACTERIAL GENE; GENETICS; METABOLISM; MULTIGENE FAMILY;

CYANOBACTERIA;

CYANOBACTERIA; GENES, BACTERIAL; MULTIGENE FAMILY; TROPANES;

EID: 84911879513     PISSN: 00410101     EISSN: 18793150     Source Type: Journal    
DOI: 10.1016/j.toxicon.2014.07.016     Document Type: Article

References (43)

1. R. Araoz, H.O. Nghiem, R. Rippka, N. Palibroda, N.T. de Marsac, and M. Herdman Neurotoxins in axenic oscillatorian cyanobacteria: coexistence of anatoxin-a and homoanatoxin-a determined by ligand-binding assay and GC/MS Microbiology 151 2005 1263 1273
2. A. Ballot, J. Fastner, M. Lentz, and C. Wiedner First report of anatoxin-a-producing cyanobacterium Aphanizomenon issatschenkoi in northeastern Germany Toxicon 56 2010 964 971
3. G. Bashiri, C.J. Squire, N.J. Moreland, and E.N. Baker Crystal structures of F420-dependent glucose-6-phosphate dehydrogenase FGD1 involved in the activation of the anti-tuberculosis drug candidate PA-824 reveal the basis of coenzyme and substrate binding J. Biol. Chem. 283 2008 17531 17541
4. H.A. Bates, and H. Rapoport Synthesis of anatoxin-a via intra-molecular cyclization of Iminium Salts J. Am. Chem. Soc. 101 1979 1259 1265
5. S. Cadel-Six, I. Iteman, C. Peyraud-Thomas, S. Mann, O. Ploux, and A. Mejean Identification of a polyketide synthase coding sequence specific for anatoxin-a-producing Oscillatoria cyanobacteria Appl. Environ. Microbiol. 75 2009 4909 4912
6. S. Cadel-Six, C. Peyraud-Thomas, L. Brient, N.T. de Marsac, R. Rippka, and A. Mejean Different genotypes of anatoxin-producing cyanobacteria coexist in the Tarn River, France Appl. Environ. Microbiol. 73 2007 7605 7614
7. H.F. Campbell, O.E. Edwards, and R. Kolt Synthesis of nor-anatoxin-a and anatoxin-A Can. J. Chem. 55 1977 1372 1379
8. W.W. Carmichael Cyanobacteria secondary metabolites - the cyanotoxins J. Appl. Bacteriol. 72 1992 445 459
9. W.W. Carmichael, D.F. Biggs, and P.R. Gorham Toxicology and pharmacological action of Anabaena flos-aquae toxin Science 187 1975 542 544
10. J.P. Devlin, O.E. Edwards, P.R. Gorham, N.R. Hunter, R.K. Pike, and B. Stavric Anatoxin-a, a toxic alkaloid from Anabaena-Flos-Aquae Nrc-44h Can. J. Chem. 55 1977 1367 1371
11. I.K. Dimitrakopoulos, T.S. Kaloudis, A.E. Hiskia, N.S. Thomaidis, and M.A. Koupparis Development of a fast and selective method for the sensitive determination of anatoxin-a in lake waters using liquid chromatography-tandem mass spectrometry and phenylalanine-d5 as internal standard Anal. Bioanal. Chem. 397 2010 2245 2252
12. C. Edwards, K.A. Beattie, C.M. Scrimgeour, and G.A. Codd Identification of anatoxin-A in benthic cyanobacteria (blue-green algae) and in associated dog poisonings at Loch Insh, Scotland Toxicon 30 1992 1165 1175
13. E.J. Faassen, L. Harkema, L. Begeman, and M. Lurling First report of (homo)anatoxin-a and dog neurotoxicosis after ingestion of benthic cyanobacteria in The Netherlands Toxicon 60 2012 378 384
14. M. Gugger, S. Lenoir, C. Berger, A. Ledreux, J.C. Druart, J.F. Humbert, C. Guette, and C. Bernard First report in a river in France of the benthic cyanobacterium Phormidium favosum producing anatoxin-a associated with dog neurotoxicosis Toxicon 45 2005 919 928
15. K.-i. Harada, H. Nagai, Y. Kimura, M. Suzuki, H.-D. Park, M.F. Watanabe, R. Luukkainen, K. Sivonen, and W.W. Carmichael Liquid chromatography/mass spectrometric detection of anatoxin-a, a neurotoxin from cyanobacteria Tetrahedron 49 1993 9251 9260
16. T. Hemscheidt, J. Rapala, K. Sivonen, and O.M. Skulberg Biosynthesis of anatoxin-a in Anabaena flos-aquae and homoanatoxin-a in Oscillatoria formosa J. Chem. Soc. Chem. Commun. 1995 1361 1362
17. K.J. James, J. Crowley, B. Hamilton, M. Lehane, O. Skulberg, and A. Furey Anatoxins and degradation products, determined using hybrid quadrupole time-of-flight and quadrupole ion-trap mass spectrometry: forensic investigations of cyanobacterial neurotoxin poisoning Rapid Commun. Mass Spectrom. 19 2005 1167 1175
18. K.J. James, A. Furey, I.R. Sherlock, M.A. Stack, M. Twohig, F.B. Caudwell, and O.M. Skulberg Sensitive determination of anatoxin-a, homoanatoxin-a and their degradation products by liquid chromatography with fluorimetric detection J. Chromatogr. A 798 1998 147 157
19. L. Krienitz, A. Ballot, K. Kotut, C. Wiegand, S. Putz, J.S. Metcalf, G.A. Codd, and S. Pflugmacher Contribution of hot spring cyanobacteria to the mysterious deaths of Lesser Flamingos at Lake Bogoria, Kenya FEMS Microbiol. Ecol. 43 2003 141 148
20. S. Mann, M. Cohen, F. Chapuis-Hugon, V. Pichon, R. Mazmouz, A. Mejean, and O. Ploux Synthesis, configuration assignment, and simultaneous quantification by liquid chromatography coupled to tandem mass spectrometry, of dihydroanatoxin-a and dihydrohomoanatoxin-a together with the parent toxins, in axenic cyanobacterial strains and in environmental samples Toxicon 60 2012 1404 1414
21. S. Mann, B. Lombard, D. Loew, A. Méjean, and O. Ploux Insights into the reaction mechanism of the prolyl-acyl carrier protein oxidase involved in anatoxin-a and homoanatoxin-a biosynthesis Biochemistry 50 2011 7184 7197
22. H.L. Mansell Synthetic approaches to anatoxin-a Tetrahedron 52 1996 6025 6061
23. A. Méjean, S. Mann, T. Maldiney, G. Vassiliadis, O. Lequin, and O. Ploux Evidence that biosynthesis of the neurotoxic alkaloids anatoxin-a and homoanatoxin-a in the cyanobacterium Oscillatoria PCC 6506 occurs on a modular polyketide synthase initiated by L-proline J. Am. Chem. Soc. 131 2009 7512 7513
24. A. Méjean, S. Mann, G. Vassiliadis, B. Lombard, D. Loew, and O. Ploux In vitro reconstitution of the first steps of anatoxin-a biosynthesis in Oscillatoria PCC 6506: from free L-proline to acyl carrier protein bound dehydroproline Biochemistry 49 2010 103 113
25. A. Méjean, R. Mazmouz, S. Mann, A. Calteau, C. Medigue, and O. Ploux The genome sequence of the cyanobacterium Oscillatoria sp. PCC 6506 reveals several gene clusters responsible for the biosynthesis of toxins and secondary metabolites J. Bacteriol. 192 2010 5264 5265
26. A. Méjean, C. Peyraud-Thomas, A.S. Kerbrat, S. Golubic, S. Pauillac, M. Chinain, and D. Laurent First identification of the neurotoxin homoanatoxin-a from mats of Hydrocoleum lyngbyaceum (marine cyanobacterium) possibly linked to giant clam poisoning in New Caledonia Toxicon 56 2010 829 835
27. A. Méjean, and O. Ploux A genomic view of secondary metabolite production in cyanobacteria Genomics Cyanobacteria 2013 189 234
28. M.C. Moffitt, and B.A. Neilan Evolutionary affiliations within the superfamily of ketosynthases reflect complex pathway associations J. Mol. Evol. 56 2003 446 457
29. K. Moncoq, L. Regad, S. Mann, A. Méjean, and O. Ploux Structure of the prolyl-acyl carrier protein oxidase involved in the biosynthesis of the cyanotoxin anatoxin-a Acta Crystallogr. D Biol. Crystallogr. 69 2013 2340 2352
30. M. Namikoshi, T. Murakami, T. Fujiwara, H. Nagai, T. Niki, E. Harigaya, M.F. Watanabe, T. Oda, J. Yamada, and S. Tsujimura Biosynthesis and transformation of homoanatoxin-a in the cyanobacterium Raphidiopsis mediterranea Skuja and structures of three new homologues Chem. Res. Toxicol. 17 2004 1692 1696
31. M. Namikoshi, T. Murakami, M.F. Watanabe, T. Oda, J. Yamada, S. Tsujimura, H. Nagai, and S. Oishi Simultaneous production of homoanatoxin-a, anatoxin-a, and a new non-toxic 4-hydroxyhomoanatoxin-a by the cyanobacterium Raphidiopsis mediterranea Skuja Toxicon 42 2003 533 538
32. P.J. Parsons, N.P. Camp, N. Edwards, and L. Ravi Sumoreeah Synthesis of (±)-Anatoxin-a and Analogues Tetrahedron 56 2000 309 315
33. A. Rantala-Ylinen, S. Kana, H. Wang, L. Rouhiainen, M. Wahlsten, E. Rizzi, K. Berg, M. Gugger, and K. Sivonen Anatoxin-a synthetase gene cluster of the cyanobacterium Anabaena sp. strain 37 and molecular methods to detect potential producers Appl. Environ. Microbiol. 77 2011 7271 7278
34. P.M. Shih, D. Wu, A. Latifi, S.D. Axen, D.P. Fewer, E. Talla, A. Calteau, F. Cai, N. Tandeau de Marsac, R. Rippka, M. Herdman, K. Sivonen, T. Coursin, T. Laurent, L. Goodwin, M. Nolan, K.W. Davenport, C.S. Han, E.M. Rubin, J.A. Eisen, T. Woyke, M. Gugger, and C.A. Kerfeld Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing Proc. Natl. Acad. Sci. U. S. A. 110 2013 1053 1058
35. K. Sivonen, K. Himberg, R. Luukkainen, S.I. Niemelä, G.K. Poon, and G.A. Codd Preliminary characterization of neurotoxic cyanobacteria blooms and strains from Finland Toxic. Assess. 4 1989 339 352
36. O.M. Skulberg, W.W. Carmichael, R.A. Andersen, S. Matsunaga, R.E. Moore, and R. Skulberg Investigations of a neurotoxic Oscillatorialean strain (Cyanophyceae) and its toxin - isolation and characterization of homoanatoxin-a Environ. Toxicol. Chem. 11 1992 321 329
37. M.E. van Apeldoorn, H.P. van Egmond, G.J.A. Speijers, and G.J.I. Bakker Toxins of cyanobacteria Mol. Nutr. Food Res. 51 2007 7 60
38. S. Wonnacott, and T. Gallagher The chemistry and pharmacology of anatoxin-a and related homotropanes with respect to nicotinic acetylcholine receptors Mar. Drugs 4 2006 228 254
39. S. Wonnacott, S. Jackman, K.L. Swanson, H. Rapoport, and E.X. Albuquerque Nicotinic pharmacology of anatoxin analogs. II. Side chain structure-activity relationships at neuronal nicotinic ligand binding sites J. Pharmacol. Exp. Ther. 259 1991 387 391
40. S. Wonnacott, K.L. Swanson, E.X. Albuquerque, N.J. Huby, P. Thompson, and T. Gallagher Homoanatoxin: a potent analogue of anatoxin-A Biochem. Pharmacol. 43 1992 419 423
41. S.A. Wood, M.W. Heath, J. Kuhajek, and K.G. Ryan Fine-scale spatial variability in anatoxin-a and homoanatoxin-a concentrations in benthic cyanobacterial mats: implication for monitoring and management J. Appl. Microbiol. 109 2010 2011 2018
42. S.A. Wood, A.I. Selwood, A. Rueckert, P.T. Holland, J.R. Milne, K.F. Smith, B. Smits, L.F. Watts, and C.S. Cary First report of homoanatoxin-a and associated dog neurotoxicosis in New Zealand Toxicon 50 2007 292 301
43. S.A. Wood, F.M. Smith, M.W. Heath, T. Palfroy, S. Gaw, R.G. Young, and K.G. Ryan Within-mat variability in anatoxin-a and homoanatoxin-a production among benthic Phormidium (cyanobacteria) strains Toxins (Basel) 4 2012 900 912