β-Methylamino-L-alanine-induced protein aggregation in vitro and protection by L-serine.
Amino Acids, Diamino
/ adverse effects
Antioxidants
/ pharmacology
Cell Differentiation
Chaperone-Mediated Autophagy
Cyanobacteria Toxins
/ adverse effects
Excitatory Amino Acid Agonists
/ adverse effects
Humans
Lysosomal-Associated Membrane Protein 2
/ genetics
Neuroblastoma
/ drug therapy
Oxidative Stress
Proteasome Endopeptidase Complex
/ genetics
Protein Aggregates
/ drug effects
Serine
/ pharmacology
Tumor Cells, Cultured
Ubiquitin
/ metabolism
BMAA
L-serine
Lamp2a
Protein aggregation
Ubiquitin
Journal
Amino acids
ISSN: 1438-2199
Titre abrégé: Amino Acids
Pays: Austria
ID NLM: 9200312
Informations de publication
Date de publication:
Sep 2021
Sep 2021
Historique:
received:
13
03
2021
accepted:
12
07
2021
pubmed:
21
7
2021
medline:
18
1
2022
entrez:
20
7
2021
Statut:
ppublish
Résumé
The cyanobacterial non-protein amino acid α-amino-β-methylaminopropionic acid, more commonly known as BMAA, was first discovered in the seeds of the ancient gymnosperm Cycad circinalis (now Cycas micronesica Hill). BMAA was linked to the high incidence of neurological disorders on the island of Guam first reported in the 1950s. BMAA still attracts interest as a possible causative factor in amyotrophic lateral sclerosis (ALS) following the identification of ALS disease clusters associated with living in proximity to lakes with regular cyanobacterial blooms. Since its discovery, BMAA toxicity has been the subject of many in vivo and in vitro studies. A number of mechanisms of toxicity have been proposed including an agonist effect at glutamate receptors, competition with cysteine for transport system x
Identifiants
pubmed: 34283312
doi: 10.1007/s00726-021-03049-w
pii: 10.1007/s00726-021-03049-w
doi:
Substances chimiques
Amino Acids, Diamino
0
Antioxidants
0
Cyanobacteria Toxins
0
Excitatory Amino Acid Agonists
0
LAMP2 protein, human
0
Lysosomal-Associated Membrane Protein 2
0
Protein Aggregates
0
Ubiquitin
0
beta-N-methylamino-L-alanine
108SA6URTV
Serine
452VLY9402
Proteasome Endopeptidase Complex
EC 3.4.25.1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1351-1359Subventions
Organisme : Motor Neurone Disease Australia
ID : PRO-15-0352
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.
Références
Beri J, Nash T, Martin RM, Bereman MS (2017) Exposure to BMAA mirrors molecular processes linked to neurodegenerative disease. Proteomics. https://doi.org/10.1002/pmic.201700161
doi: 10.1002/pmic.201700161
pubmed: 28837265
pmcid: 5828681
Cai HY, Tian KW, Zhang YY, Jiang H, Han S (2018) Angiopoietin-1 and alphanubeta3 integrin peptide promote the therapeutic effects of L-serine in an amyotrophic lateral sclerosis/parkinsonism dementia complex model. Aging (Albany NY) 10(11):3507–3527. https://doi.org/10.18632/aging.101661
doi: 10.18632/aging.101661
Caller TA, Doolin JW, Haney JF, Murby AJ, West KG, Farrar HE, Ball A, Harris BT, Stommel EW (2009) A cluster of amyotrophic lateral sclerosis in New Hampshire: a possible role for toxic cyanobacteria blooms. Amyotroph Lateral Scler 10(Suppl 2):101–108. https://doi.org/10.3109/17482960903278485
doi: 10.3109/17482960903278485
pubmed: 19929741
Caller TA, Field NC, Chipman JW, Shi X, Harris BT, Stommel EW (2012) Spatial clustering of amyotrophic lateral sclerosis and the potential role of BMAA. Amyotroph Lateral Scler 13(1):25–32. https://doi.org/10.3109/17482968.2011.621436
doi: 10.3109/17482968.2011.621436
pubmed: 22214351
Cox PA, Banack SA, Murch SJ, Rasmussen U, Tien G, Bidigare RR, Metcalf JS, Morrison LF, Codd GA, Bergman B (2005) Diverse taxa of cyanobacteria produce beta-N-methylamino-L-alanine, a neurotoxic amino acid. Proc Natl Acad Sci USA 102(14):5074–5078. https://doi.org/10.1073/pnas.0501526102
doi: 10.1073/pnas.0501526102
pubmed: 15809446
pmcid: 555964
Cox PA, Davis DA, Mash DC, Metcalf JS, Banack SA (2016) Dietary exposure to an environmental toxin triggers neurofibrillary tangles and amyloid deposits in the brain. Proc Biol Sci 283(1823):20152397. https://doi.org/10.1098/rspb.2015.2397
doi: 10.1098/rspb.2015.2397
pubmed: 26791617
pmcid: 4795023
Cox PA, Kostrzewa RM, Guillemin GJ (2018) BMAA and neurodegenerative illness. Neurotox Res 33(1):178–183. https://doi.org/10.1007/s12640-017-9753-6
doi: 10.1007/s12640-017-9753-6
pubmed: 28540663
Dice JF (2007) Chaperone-mediated autophagy. Autophagy 3(4):295–299. https://doi.org/10.4161/auto.4144
doi: 10.4161/auto.4144
pubmed: 17404494
Dunlop RA, Brunk UT, Rodgers KJ (2011) Proteins containing oxidized amino acids induce apoptosis in human monocytes. Biochem J 435(1):207–216. https://doi.org/10.1042/BJ20100682
doi: 10.1042/BJ20100682
pubmed: 21210766
Dunlop RA, Cox PA, Banack SA, Rodgers KJ (2013) The non-protein amino acid BMAA is misincorporated into human proteins in place of l-serine causing protein misfolding and aggregation. PLoS ONE 8(9):e75376. https://doi.org/10.1371/journal.pone.0075376PONE-D-13-17380
doi: 10.1371/journal.pone.0075376PONE-D-13-17380
pubmed: 24086518
pmcid: 3783393
Esterhuizen-Londt M, Wiegand C, Downing TG (2015) Beta-N-methylamino-L-alanine (BMAA) uptake by the animal model, Daphnia magna and subsequent oxidative stress. Toxicon 100:20–26. https://doi.org/10.1016/j.toxicon.2015.03.021
doi: 10.1016/j.toxicon.2015.03.021
pubmed: 25841344
Garruto RM, Gajdusek C, Chen KM (1980) Amyotrophic lateral sclerosis among Chamorro migrants from Guam. Ann Neurol 8(6):612–619. https://doi.org/10.1002/ana.410080612
doi: 10.1002/ana.410080612
pubmed: 7212649
Glover WB, Mash DC, Murch SJ (2014) The natural non-protein amino acid N-beta-methylamino-L-alanine (BMAA) is incorporated into protein during synthesis. Amino Acids 46(11):2553–2559. https://doi.org/10.1007/s00726-014-1812-1
doi: 10.1007/s00726-014-1812-1
pubmed: 25096519
Halliwell B (2014) Cell culture, oxidative stress, and antioxidants: avoiding pitfalls. Biomed J 37(3):99–105. https://doi.org/10.4103/2319-4170.128725
doi: 10.4103/2319-4170.128725
pubmed: 24923566
Huang CC, Bose JK, Majumder P, Lee KH, Huang JT, Huang JK, Shen CK (2014) Metabolism and mis-metabolism of the neuropathological signature protein TDP-43. J Cell Sci 127(Pt 14):3024–3038. https://doi.org/10.1242/jcs.136150
doi: 10.1242/jcs.136150
pubmed: 24860144
Jiang L, Eriksson J, Lage S, Jonasson S, Shams S, Mehine M, Ilag LL, Rasmussen U (2014) Diatoms: a novel source for the neurotoxin BMAA in aquatic environments. PLoS ONE 9(1):e84578. https://doi.org/10.1371/journal.pone.0084578
doi: 10.1371/journal.pone.0084578
pubmed: 24392143
pmcid: 3879315
Karamyan VT, Speth RC (2008) Animal models of BMAA neurotoxicity: a critical review. Life Sci 82(5–6):233–246
doi: 10.1016/j.lfs.2007.11.020
Karlsson O, Berg AL, Lindstrom AK, Hanrieder J, Arnerup G, Roman E, Bergquist J, Lindquist NG, Brittebo EB, Andersson M (2012) Neonatal exposure to the cyanobacterial toxin BMAA induces changes in protein expression and neurodegeneration in adult hippocampus. Toxicol Sci 130(2):391–404. https://doi.org/10.1093/toxsci/kfs241
doi: 10.1093/toxsci/kfs241
pubmed: 22872059
pmcid: 3498744
Karlsson O, Berg AL, Hanrieder J, Arnerup G, Lindstrom AK, Brittebo EB (2015) Intracellular fibril formation, calcification, and enrichment of chaperones, cytoskeletal, and intermediate filament proteins in the adult hippocampus CA1 following neonatal exposure to the nonprotein amino acid BMAA. Arch Toxicol 89(3):423–436. https://doi.org/10.1007/s00204-014-1262-2
doi: 10.1007/s00204-014-1262-2
pubmed: 24798087
Kurland LT, Mulder DW (1954) Epidemiologic investigations of amyotrophic lateral sclerosis I preliminary report on geographic distribution and special reference to the Mariana Islands, including clinical and pathologic observations. Neurology 4(6):438–448
doi: 10.1212/WNL.4.6.438
Kurtishi A, Rosen B, Patil KS, Alves GW, Moller SG (2018) Cellular proteostasis in neurodegeneration. Mol Neurobiol. https://doi.org/10.1007/s12035-018-1334-z
doi: 10.1007/s12035-018-1334-z
pubmed: 30182337
Laugeray A, Oummadi A, Jourdain C, Feat J, Meyer-Dilhet G, Menuet A, Ple K, Gay M, Routier S, Mortaud S, Guillemin GJ (2018) Perinatal exposure to the cyanotoxin beta-N-methylamino-L-alanine (BMAA) results in long-lasting behavioral changes in offspring-potential involvement of DNA damage and oxidative stress. Neurotox Res 33(1):87–112. https://doi.org/10.1007/s12640-017-9802-1
doi: 10.1007/s12640-017-9802-1
pubmed: 28879461
Levine TD, Miller RG, Bradley WG, Moore DH, Saperstein DS, Flynn LE, Katz JS, Forshew DA, Metcalf JS, Banack SA, Cox PA (2017) Phase I clinical trial of safety of L-serine for ALS patients. Amyotroph Lateral Scler Frontotemporal Degener 18(1–2):107–111. https://doi.org/10.1080/21678421.2016.1221971
doi: 10.1080/21678421.2016.1221971
pubmed: 27589995
Liu X, Rush T, Zapata J, Lobner D (2009) Beta-N-methylamino-l-alanine induces oxidative stress and glutamate release through action on system Xc(-). Exp Neurol 217(2):429–433. https://doi.org/10.1016/j.expneurol.2009.04.002
doi: 10.1016/j.expneurol.2009.04.002
pubmed: 19374900
Lobner D (2009) Mechanisms of beta-N-methylamino-L-alanine induced neurotoxicity. Amyotroph Lateral Scler 10(Suppl 2):56–60. https://doi.org/10.3109/17482960903269062
doi: 10.3109/17482960903269062
pubmed: 19929733
Main BJ, Dunlop RA, Rodgers KJ (2016) The use of L-serine to prevent beta-methylamino-L-alanine (BMAA)-induced proteotoxic stress in vitro. Toxicon 109:7–12. https://doi.org/10.1016/j.toxicon.2015.11.003
doi: 10.1016/j.toxicon.2015.11.003
pubmed: 26559613
Main BJ, Bowling LC, Padula MP, Bishop DP, Mitrovic SM, Guillemin GJ, Rodgers KJ (2018a) Detection of the suspected neurotoxin beta-methylamino-l-alanine (BMAA) in cyanobacterial blooms from multiple water bodies in Eastern Australia. Harmful Algae 74:10–18. https://doi.org/10.1016/j.hal.2018.03.004
doi: 10.1016/j.hal.2018.03.004
pubmed: 29724339
Main BJ, Italiano CJ, Rodgers KJ (2018b) Investigation of the interaction of beta-methylamino-L-alanine with eukaryotic and prokaryotic proteins. Amino Acids 50(3–4):397–407. https://doi.org/10.1007/s00726-017-2525-z
doi: 10.1007/s00726-017-2525-z
pubmed: 29235019
Malkus KA, Ischiropoulos H (2012) Regional deficiencies in chaperone-mediated autophagy underlie alpha-synuclein aggregation and neurodegeneration. Neurobiol Dis 46(3):732–744. https://doi.org/10.1016/j.nbd.2012.03.017
doi: 10.1016/j.nbd.2012.03.017
pubmed: 22426402
pmcid: 3352979
Metcalf JS, Dunlop RA, Powell JT, Banack SA, Cox PA (2018) L-Serine: a naturally-occurring amino acid with therapeutic potential. Neurotox Res 33(1):213–221. https://doi.org/10.1007/s12640-017-9814-x
doi: 10.1007/s12640-017-9814-x
pubmed: 28929385
de Munck E, Munoz-Saez E, Antonio MT, Pineda J, Herrera A, Miguel BG, Arahuetes RM (2013) Effect of beta-N-methylamino-L-alanine on oxidative stress of liver and kidney in rat. Environ Toxicol Pharmacol 35(2):193–199. https://doi.org/10.1016/j.etap.2012.12.004
doi: 10.1016/j.etap.2012.12.004
pubmed: 23328118
Munoz-Saez E, de Munck E, Arahuetes RM, Solas MT, Martinez AM, Miguel BG (2013) Beta-N-methylamino-L-alanine induces changes in both GSK3 and TDP-43 in human neuroblastoma. J Toxicol Sci 38(3):425–430. https://doi.org/10.2131/jts.38.425
doi: 10.2131/jts.38.425
pubmed: 23665941
Munoz-Saez E, de Munck GE, ArahuetesPortero RM, Vicente F, Ortiz-Lopez FJ, Cantizani J, Gomez Miguel B (2015) Neuroprotective role of sphingosine-1-phosphate in L-BMAA treated neuroblastoma cells (SH-SY5Y). Neurosci Lett 593:83–89. https://doi.org/10.1016/j.neulet.2015.03.010
doi: 10.1016/j.neulet.2015.03.010
pubmed: 25769802
Nunn PB, Seelig M, Zagoren JC, Spencer PS (1987) Stereospecific acute neuronotoxicity of “uncommon” plant amino acids linked to human motor-system diseases. Brain Res 410(2):375–379
doi: 10.1016/0006-8993(87)90342-8
Nunn PB, Ponnusamy M (2009) Beta-N-methylaminoalanine (BMAA): metabolism and metabolic effects in model systems and in neural and other tissues of the rat in vitro. Toxicon 54(2):85–94. https://doi.org/10.1016/j.toxicon.2009.03.008
doi: 10.1016/j.toxicon.2009.03.008
pubmed: 19285998
Nunn PB (2017) 50 years of research on alpha-amino-beta-methylaminopropionic acid (beta-methylaminoalanine). Phytochemistry 144:271–281. https://doi.org/10.1016/j.phytochem.2017.10.002
doi: 10.1016/j.phytochem.2017.10.002
pubmed: 29102875
Okle O, Stemmer K, Deschl U, Dietrich DR (2013) L-BMAA induced ER stress and enhanced caspase 12 cleavage in human neuroblastoma SH-SY5Y cells at low nonexcitotoxic concentrations. Toxicol Sci 131(1):217–224. https://doi.org/10.1093/toxsci/kfs291
doi: 10.1093/toxsci/kfs291
pubmed: 23047912
Pablo J, Banack SA, Cox PA, Johnson TE, Papapetropoulos S, Bradley WG, Buck A, Mash DC (2009) Cyanobacterial neurotoxin BMAA in ALS and Alzheimer’s disease. Acta Neurol Scand 120(4):216–225. https://doi.org/10.1111/j.1600-0404.2008.01150.x
doi: 10.1111/j.1600-0404.2008.01150.x
pubmed: 19254284
Plato CC, Garruto RM, Gajdusek DC (1983) Further studies on the genetics of the Chamorros of Guam: dermatoglyphics. Hum Hered 33(6):329–343
doi: 10.1159/000153401
Plato CC, Garruto RM, Galasko D, Craig UK, Plato M, Gamst A, Torres JM, Wiederholt W (2003) Amyotrophic lateral sclerosis and parkinsonism-dementia complex of Guam: changing incidence rates during the past 60 years. Am J Epidemiol 157(2):149–157
doi: 10.1093/aje/kwf175
Rodgers KJ (2014) Non-protein amino acids and neurodegeneration: the enemy within. Exp Neurol 253:192–196. https://doi.org/10.1016/j.expneurol.2013.12.010
doi: 10.1016/j.expneurol.2013.12.010
pubmed: 24374297
Spencer PS, Hugon J, Ludolph A, Nunn PB, Ross SM, Roy DN, Schaumburg HH (1987a) Discovery and partial characterization of primate motor-system toxins. Ciba Found Symp 126:221–238
pubmed: 3107939
Spencer PS, Nunn PB, Hugon J, Ludolph AC, Ross SM, Roy DN, Robertson RC (1987b) Guam amyotrophic lateral sclerosis-parkinsonism-dementia linked to a plant excitant neurotoxin. Science 237(4814):517–522
doi: 10.1126/science.3603037
Violi JP, Facey JA, Mitrovic SM, Colville A, Rodgers KJ (2019a) Production of beta-methylamino-L-alanine (BMAA) and its isomers by freshwater diatoms. Toxins (basel) 11(9):512. https://doi.org/10.3390/toxins11090512
doi: 10.3390/toxins11090512
Violi JP, Mitrovic SM, Colville A, Main BJ, Rodgers KJ (2019b) Prevalence of beta-methylamino-L-alanine (BMAA) and its isomers in freshwater cyanobacteria isolated from eastern Australia. Ecotoxicol Environ Saf 172:72–81. https://doi.org/10.1016/j.ecoenv.2019.01.046
doi: 10.1016/j.ecoenv.2019.01.046
pubmed: 30682636
Weiss JH, Christine CW, Choi DW (1989) Bicarbonate dependence of glutamate receptor activation by beta-N-methylamino-L-alanine: channel recording and study with related compounds. Neuron 3(3):321–326. https://doi.org/10.1016/0896-6273(89)90256-0
doi: 10.1016/0896-6273(89)90256-0
pubmed: 2561969
Zeevalk GD, Nicklas WJ (1989) Acute excitotoxicity in chick retina caused by the unusual amino acids BOAA and BMAA: effects of MK-801 and kynurenate. Neurosci Lett 102(2–3):284–290
doi: 10.1016/0304-3940(89)90093-1
Zogovic N, Tovilovic-Kovacevic G, Misirkic-Marjanovic M, Vucicevic L, Janjetovic K, Harhaji-Trajkovic L, Trajkovic V (2015) Coordinated activation of AMP-activated protein kinase, extracellular signal-regulated kinase, and autophagy regulates phorbol myristate acetate-induced differentiation of SH-SY5Y neuroblastoma cells. J Neurochem 133(2):223–232. https://doi.org/10.1111/jnc.12980
doi: 10.1111/jnc.12980
pubmed: 25348263