Distinguishing the cyanobacterial neurotoxin β-N-methylamino-l-alanine (BMAA) from its structural isomer 2,4-diaminobutyric acid (2,4-DAB)

Toxicon

Volumn 56, Issue 6, 2010, Pages 868-879

  Banack, S A ^a   Downing, T G ^b   Spacil Z ^c,e   Purdie, E L ^d   Metcalf, J S ^a   Downing, S ^b   Esterhuizen, M ^b   Codd, G A ^d   Cox, P A ^a  

^a Institute for Ethnomedicine   (United States)

^b NELSON MANDELA METROPOLITAN UNIVERSITY   (South Africa)

^c Charles University in Prague Faculty of Pharmacy   (Czech Republic)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

^e UNIVERSITY OF WASHINGTON   (United States)

Author keywords

2,4 DAB; Amyotrophic lateral sclerosis; BMAA; Cyanobacteria; Diaminobutyric acid; Excitotoxicity; Neurotoxicity; Non protein amino acids

Indexed keywords

2 AMINO 3 METHYLAMINOPROPIONIC ACID; 2,4 DIAMINOBUTYRIC ACID; CHLOROFORMATE; FORMIC ACID DERIVATIVE; ION; NEUROTOXIN; NINHYDRIN; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL STRUCTURE; CYANOBACTERIUM; DERIVATIZATION; GAS CHROMATOGRAPHY; ISOMER; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; REACTION ANALYSIS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY;

AMINO ACIDS, DIAMINO; AMINOBUTYRIC ACIDS; BACTERIAL TOXINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYANOBACTERIA; ISOMERISM; NEUROTOXINS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY;

CYANOBACTERIA;

EID: 77956064359     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2010.06.006     Document Type: Article

References (87)

1. Ackermann D., Menßen H.G. Niedrigmolekulare, N-haltige inhaltsstoffe der roten wegschnecke, arion empiricorum, II: hydroxylysin, α.γ-diamino-buttersäure, herzynin, homarin, trigonellin, glykokollbetain, putrescin, imidazolyl-essigsäure, -propionsäure, -milchsäure, -acrylsäure, und cholin. Hoppe-seylers Z. Physiol. Chem. 1960, 318:212-218.
2. Aráoz R., Molgó J., Tandeau de Marsac N. Neurotoxic cyanobacterial toxins. Toxicon 2010, 56:813-828.
3. Arment A.R., Carmichael W.W. Evidence that microcystin is a thiotemplate product. J. Phycol. 1996, 32:591-597.
4. Banack S.A., Cox P.A. Biomagnification of cycad neurotoxins in flying foxes: implications for ALS-PDC in Guam. Neurology 2003, 61:387-389.
5. Banack S.A., Cox P.A. Distribution of the neurotoxic nonprotein amino acid BMAA in Cycas micronesica. Bot. J. Linn. Soc. 2003, 143:165-168.
6. Banack S.A., Murch S.J., Cox P.A. Neurotoxic flying foxes as dietary items for the Chamorro people, Marianas Islands. J. Ethnopharmacol. 2006, 106(1):97-104.
7. Banack S.A., Johnson H.E., Cheng R., Cox P.A. Production of the Neurotoxin BMAA by a marine cyanobacterium. Mar. Drugs 2007, 5:180-196.
8. Bell E.A., Tirimanna S.L. Associations of amino acids and related compounds in the seeds of forty-seven species of Vicia: their taxonomic and nutritional significance. Biochem. J. 1965, 97:104-111.
9. Bidigare R.R., Christensen S.J., Wilde S.B., Banack S.A. Cyanobacteria and BMAA: possible linkage with avian vacuolar myelinopathy (AVM) in the south-eastern United States. Amyotroph. Lateral Scler. 2009, 10(S2):71-73.
10. Bradley W.G., Mash D.C. Beyond Guam: the cyanobacteria/BMAA hypothesis of the cause of ALS and other neurodegenerative diseases. Amyotroph. Lateral Scler. 2009, 10(S2):7-20.
11. Catch J.R., Jones T.S.G. The chemical nature of 'aerosporin'. Part II. Isolation of a new natural amino-acid. Biochem. J. 1948, 42:lii.
12. Cheng R., Banack S.A. Previous studies underestimate BMAA concentrations in cycad flour. Amyotroph. Lateral Scler. 2009, 10(S2):41-43.
13. Chen C.H., Flory W., Koeppe R.E. Variation of neurotoxicity of l- and d-2,4-diaminobutyric acid with route of administration. Toxicol. Appl. Pharmacol. 1972, 23:334-338.
14. Cohen S.A., Michaud D.P. Synthesis of a fluorescent derivatizing reagent, 6-aminoquinolyl-N-hydroxysuccinimidyl carbamate, and its application for the analysis of hydrolysate amino acids via high-performance liquid chromatography. Anal. Biochem. 1993, 211:279-287.
15. Cox P.A., Banack S.A., Murch S.J. Biomagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:13380-13383.
16. Cox P.A., Banack S.A., Murch S.J., Rasmussen U., Tien G., Bidigare R.R., Metcalf J.S., Morrison L.F., Codd G.A., Bergman B. Diverse taxa of cyanobacteria produce β-N-methylamino-l-alanine, a neurotoxic amino acid. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:5074-5078.
17. Cox P.A., Richer R., Metcalf J.S., Banack S.A., Codd G.A., Bradley W.G. Cyanobacteria and BMAA exposure from desert dust-a possible link to sporadic ALS among Gulf War veterans. Amyotroph. Lateral Scler. 2009, 10(S2):109-113.
18. Craighead D., Metcalf J.S., Banack S.A., Amgalan L., Reynolds H.V., Batmunkh M. Presence of the neurotoxic amino acids β-N-methylamino-l-alanine (BMAA) and 2,4-diamino-butyric acid (DAB) in shallow springs from the Gobi Desert. Amyotroph. Lateral Scler. 2009, 10(S2):96-100.
19. Dick F., Kelly J.S. l-2,4-diaminobutyric acid (l-DABA) as selective marker for inhibitory nerve terminals in rat brain. Br. J. Pharmacol. 1975, 53:439.
20. Dittmann E., Börner T. Genetic contributions to the risk assessment of microcystin in the environment. Toxicol. Appl. Pharmacol. 2005, 203:192-200.
21. Duncan M.W., Kopin I.J., Lavine L., Garruto R., Markey S.P. The putative neurotoxin BMAA in cycad-derived foods is an unlikely cause of ALS-PD. Lancet 1988, 2:631-632.
22. Duncan M.W., Steele J.C., Kopin I.J., Markey S.P. 2-amino-3-(methylamino)-propionic acid (BMAA) in cycad flour: an unlikely cause of amyotrophic lateral sclerosis and parkinsonism-dementia of Guam. Neurology 1990, 40:767-772.
23. Einarsson S., Josefsson B., Lagerkvist S. Determination of amino acids with 9-fluorenylmethyl chloroformate and reversed-phase high performance liquid chromatography. J. Chromatogr. A 1983, 282:609-618.
24. Eriksson J., Jonasson S., Papaefthimiou D., Rasmussen U., Bergman B. Improving derivatization efficiency of BMAA utilizing AccQ-Tag in a complex cyanobacterial matrix. Amino Acids 2009, 36:43-48.
25. Erecińska M., Troeger M.B., Alston T.A. Amino acid neurotransmitters in the CNS: properties of diaminobutyric acid transport. J. Neurochem. 1986, 46:1452-1457.
26. Esterhuizen M., Downing T. β-N-methylamino-l-alanine (BMAA) in novel South African cyanobacterial isolates. Ecotoxicol. Environ. Saf. 2008, 71:309-313.
27. Evans C.S., Clardy J., Hughes F., Bell E.A. 2-amino-4-acetylaminobutyric acid, 2,4-diaminobutyric acid and 2-amino-6N-oxalylureidopropionic acid (oxalylalbizziine) in seeds of Acacia angustissima. Phytochemistry 1985, 24:2273-2275.
28. Faassen E.J., Gillissen F., Zweers J., Lürling M. Determination of the neurotoxins BMAA (β-N-methylamino-l-alanine) and DAB (α-,γ-diaminobutyric acid) by LC-MSMS in Dutch urban waters with cyanobacterial blooms. Amyotroph. Lateral Scler. 2009, 10(S2):79-84.
29. Fowden L., Bryant M. Nitrogenous compounds and nitrogen metabolism in the Liliaceae 4. Isolation of azetidine-2-carboxylic acid and evidence for the occurrence of αγ-diaminobutyric acid in Polygonatum. Biochem. J. 1958, 70:626-629.
30. Groth I., Schumann P., Weiss N., Martin K., Rainey F.A. Agrococcus jenesis gen. nov., sp. nov., a new genus of actinomycetes with diaminobutyric acid in the cell wall. Int. J. Syst. Bacteriol. 1996, 46:234-239.
31. 2-methylamino-l-alanine. J. Am. Soc. Mass. Spectrom. 2007, 18:817-825.
32. Hoffmann E., de Strobant V. Mass Spectrometry: Principles and Applications 2007, J. Wiley, Chichester, UK, 489 pp.
33. Horton R.W., Collins J.F., Anlezark G.M., Meldrum B.S. Convulsant and anticonvulsant actions of DBA/2 mice of compounds blocking the reuptake of GABA. Eur. J. Pharmacol. 1979, 59:75-83.
34. Ikegami T., Tomomatsu K., Takubo H., Horie K., Tanaka N. Separation efficiencies in hydrophilic interaction chromatography. J. Chromatogr. A 2008, 1184:474-503.
35. Ince P.G., Codd G.A. Return of the cycad hypothesis - does the amyotrophic lateral sclerosis/parkinsonism dementia complex (ALS/PDC) of Guam have new implications for global health?. Neuropathol. Appl. Neurobiol. 2005, 31:345-353.
36. Johnson H., King S.R., Banack S.A., Webster C., Callanaupa W.J., Cox P.A. Cyanobacteria (Nostoc commune) used as a dietary item in Peruvian highlands produce the neurotoxic amino acid BMAA. J. Ethnopharmacol. 2008, 118:159-165.
37. Johnston G.A.R., Twitchin B. Stereospecificity of 2,4-diaminobutyric acid with respect to inhibition of 4-aminobutyric acid uptake and binding. Br. J. Pharmacol. 1977, 59:218-219.
38. Jonasson S., Eriksson J., Berntzon L., Spáčil Z., Ilag L.L., Ronnevi L.-O., Rasmussen U., Bergman B. Transfer of a cyanobacterial neurotoxin within a temperate aquatic ecosystem suggests pathways for human exposure. Proc. Natl. Acad. Sci. U.S.A. 2010, online, early edition:. http://www.pnas.org/cgi/doi/10.1073/pnas.0914417107.
39. Karamyan V., Speth R. Animal models of BMAA neurotoxicity: a critical review. Life Sci. 2008, 82:233-246.
40. Komura S., Kurahashi K. Partial purification and properties of l-2,4-diaminobutyric acid activating enzyme from a polymyxin E producing organism. J. Biochem. 1979, 86:1013-1021.
41. Krüger T., Mönch B., Oppenhäuser S., Luckas B. LC-MS/MS determination of the isomeric neurotoxins BMAA (β-N-methylamino-l-alanine) and DAB (2,4-diaminobutyric acid) in cyanobacteria and seeds of Cycas revoluta and Lathyrus latifolius. Toxicon 2010, 55:547-557.
42. Kubo T., Kato N., Hosoya K., Kaya K. Effective determination method for a cyanobacterial neurotoxin, β-N-methylamino-l-alanine. Toxicon 2008, 51:1264-1268.
43. Leal S.M., Kumar N., Neckameyer W.S. GABAergic modulation of motor-driven behaviors in juvenile Drosophila and evidence for a nonbehavioral role for GABA transport. J. Neurobiol. 2004, 61:189-208.
44. Li A., Tian Z., Li J., Yu R., Banack S.A., Wang Z. Detection of the neurotoxin BMAA within cyanobacteria isolated from freshwater in China. Toxicon 2010, 55:947-953.
45. Liu X., Rush T., Zapataa J., Lobner D. β-N-methylamino-l-alanine induces oxidative stress and glutamate release through action on system Xc-Exp. Neurol. 2009, 217:429-433.
46. Lobner D., Piana P.M., Salous A.K., Peoples R.W. Beta-N-methylamino-l-alanine enhances neurotoxicity through multiple mechanisms. Neurobiol. Dis. 2007, 25:360-366.
47. Lurling M., Beekman W., Zweers H. Methylamino-l-Alanine (BMAA), Een Neuro-Toxisch Aminozuur. Report No. M344 2008, Leerstoelgroep Aquatische Ecologie & Waterkwaliteitsbeheer, Wageningen, Netherlands.
48. Malizia L.A., Tunnicliff G. Uptake of gamma-aminobutyric acid by catfish brain. Comp. Biochem. Physiol. C 1987, 87:37-40.
49. Metcalf J.S., Banack S.A., Lindsay J., Morrison L.F., Cox P.A., Codd G.A. Co-occurrence of β-N-methylamino-l-alanine, a neurotoxic amino acid with other cyanobacterial toxins in British waterbodies, 1990-2004. Environ. Microbiol. 2008, 10:702-708.
50. Moura S., de Almeida Ultramari M., de Paula D.M.L., Yonamine M., Pinto E. 1H NMR determination of β-N-methylamino-l-alanine (L-BMAA) in environmental and biological samples. Toxicon 2009, 53:578-583.
51. Murch S.J., Cox P.A., Banack S.A. A mechanism for slow release of biomagnified cyanobacterial neurotoxins and neurodegenerative disease in Guam. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:12228-12231.
52. Murch S.J., Cox P.A., Banack S.A., Steele J.C., Sacks O.W. Occurrence of beta-methylamino-l-alanine (BMAA) in ALS/PDC patients from Guam. Acta Neurol. Scand. 2004, 110(4):267-269.
53. Nakajima T., Wolfgram F., Clark W.G. Identification of 1,4-methylhistamine, 1,3-diaminopropane, and 2,4-diaminobutyric acid in bovine brain. J. Neurochem. 1967, 14:1113-1118.
54. Neal M.J., Bowery N.G. Cis-3-aminocyclohexanecarboxlyic acid: a substrate for the neuronal GABA transport system. Brain Res. 1977, 138:169-174.
55. Nozal M.J., Bernal J.L., Toribio M.L., Diego J.C., Ruiz A. Rapid and sensitive method for determining free amino acids in honey by gas chromatography with flame ionization or mass spectrometric detection. J. Chromatog. A 2004, 1047:137-146.
56. Nunn P.B., Ponnusamy M. β-N-methylaminoalanine (BMAA): metabolism and metabolic effects in model systems and in neural and other tissues of the rat in vitro. Toxicon 2009, 54:85-94.
57. Oda T., Ueda F. Studies on colistin II. Leucine, threonine, α,γ-diaminobutyric acid, and fatty acid isolated from colistin hydrolysate. J. Pharm. Soc. Japan 1954, 74:1246-1248.
58. O'Neal R.M., Chen C.-H., Reynolds C.S., Meghal S.K., Koeppe R.E. The 'neurotoxicity' of l-2,4-diaminobutyric acid. Biochem. J. 1968, 106:699-706.
59. Pablo J., Banack S.A., Cox P.A., Johnson T.E., Papapetropoulos S., Bradley W.G., Buck A., Mash D.C. Cyanobacterial neurotoxin BMAA in ALS and Alzheimer's disease. Acta Neurol. Scand. 2009, 120:216-225.
60. Pan M., Mabry T.J., Cao P., Moini M. Identification of nonprotein amino acids from cycad seeds as N-ethoxycarbonyl ethyl ester derivatives by positive chemical-ionization gas chromatography-mass spectrometry. J. Chromatog. A 1997, 787:288-294.
61. Papapetropoulos S. Is there a role for naturally occurring cyanobacterial toxins in neurodegeneration? The beta-N-methylamino-l-alanine (BMAA) paradigm. Neurochem. Int. 2007, 50:998-1003.
62. Perkins H.R., Cummins C.S. Chemical structure of bacterial cell walls; ornithine and 2,4-diaminobutyric acid as components of the cell walls of plant pathogenic corynebacteria. Nature 1964, 14:1105-1107.
63. Peterson D.H., Reineke L.M. The chemistry of circulin, chromatographic isolation of the amino acid constituents with powdered cellulose. J. Biol. Chem. 1949, 181:95-108.
64. Polsky F.I., Nunn P.B., Bell E.A. Distribution and toxicity of α-amino-β-methlyaminopropionic acid. Fed. Proc. 1972, 31:1473-1475.
65. Purdie E.L., Samsudin S., Eddy F.B., Codd G.A. Effects of the cyanobacterial neurotoxin β-N-methylamino-l-alanine, on the early-life stage development of zebrafish (Danio rerio). Aquat. Toxicol. 2009, 95:279-284.
66. Purdie E.L., Metcalf J.S., Kashmiri S., Codd G.A. Toxicity of the cyanobacterial neurotoxin β-N-methylamino-l-alanine to three aquatic animal species. Amyotroph. Lateral Scler. 2009, 10(S2):67-70.
67. Rao S.L.N., Adiga P.R., Sarma P.S. The isolation of β-N-oxalyl-α,β-diaminopropionic acid: a neurotoxin from the seeds of Lathyrus sativus. Biochemistry 1964, 3:432-436.
68. Rao S.D., Banack S.A., Cox P.A., Weiss J.H. BMAA selectively injures motor neurons via AMPA/kainate receptor activation. Exp. Neurol. 2006, 201:244-252.
69. Rasmussen M.A., Allison M.J., Foster J.G. Flatpea intoxication in sheep and indications of ruminal adaptation. Vet. Hum. Toxicol. 1993, 35:123-127.
70. Ressler C., Redstone P.A., Erenberg R.H. Isolation and identification of a neuroactive factor from Lathyrus latifolius. Science 1961, 134:188-190.
71. Riggs T.R., Coyne B.A., Christensen H.A. Amino acid concentration by a free cell neoplasm. Structural influences. J. Biol. Chem. 1954, 209:395-411.
72. Rosén J., Hellenäs K.-E. Determination of the neurotoxin BMAA (β-N-methylamino-l-alanine) in cycad seed and cyanobacteria by LC-MS/MS (liquid chromatography tandem mass spectrometry). Analyst 2008, 133:1785-1789.
73. Ross S.M., Spencer P.S. Specific antagonism of behavioral action of " uncommon" amino acids linked to motor-system diseases. Synapse 2004, 1:248-253.
74. Schleifer K.H., Kandler O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 1972, 36:407-477.
75. Shuter E.R., Robins E. Elevation of brain gamma-aminobutyric acid in the mouse by l-2,4-diaminobutyric acid. Trans. Am. Neurol. Assoc. 1974, 99:49-51.
76. Snyder L.R., Cruz-Aguado R., Sadilek M., Galasko D., Shaw C.A., Montine T. Parkinson-dementia complex and development of a new stable isotope dilution assay for BMAA detection in tissue. Toxicol. Appl. Pharmacol. 2009, 240:180-188.
77. Spáčil Z., Eriksson J., Jonasson S., Rasmussen U., Ilag L.L., Bergman B. Analytical protocol for identification of BMAA and DAB in biological samples. Analyst 2010, 135:127-132.
78. Spencer P.S., Nunn P.B., Hugon J., Ludolph A.C., Ross S.M., Roy D.N., Robertson R.C. Guam amyotrophic lateral sclerosis-parkinsonism-dementia linked to a plant excitant neurotoxin. Science 1987, 237:517-522.
79. Stoll J., Wadhwani K.C., Smith Q.R. Identification of the cationic amino acid transporter (system y+) of the rat blood-brain barrier. J. Neurochem. 1993, 60:1956-1959.
80. Strain G.M., Flory W., Tucker T.A. Inhibition of synaptosomal uptake of amino acid transmitters by diamines. Neruopharmacology 1984, 23:971-975.
81. Taberner P.V., Roberts F. The anticonvulsant action of l-2,4-diaminobutyric acid. Eur. J. Pharmacol. 1978, 52:281-286.
82. VanEtten C.H., Miller R.W. The neuroactive factor alpha-gamma diaminobutyric acid in angiospermous seeds. Econ. Bot. 1963, 17:107-109.
83. Vega A., Bell E.A. α-amino-ß-methyl-aminopropionic acid, a new amino acid from seeds of Cycas circinalis. Phytochemistry 1967, 6:759-762.
84. Vega A., Bell E.A., Nunn P.B. The preparation of l- and d-α-amino-β-methylaminopropionic acids and the identification of the compound isolated from Cycas circinalis as the l-isomer. Phytochemistry 1968, 7:1885-1887.
85. Weiss J.H., Choi D.W. Beta-N-methylamino-l-alanine neurotoxicity: requirement for bicarbonate as a cofactor. Science 1988, 241:973-975.
86. Weiss J.H., Chadwick W.C., Choi D.W. Bicarbonate dependence of glutamate receptor activation by β-N-methylamino-l-alanine: channel recording and study with related compounds. Neuron 1989, 3:321-326.
87. Weitsch-Dick F., Jessel T.M., Kelly J.S. The selective neuronal uptake and release of [3H]DL-2,4-diaminobutyric acid by rat cerebral cortex. J. Neurochem. 1978, 30:799-806.