Advertisement

Molecular Neurobiology

, Volume 55, Issue 8, pp 6769–6787 | Cite as

Pacific Ciguatoxin Induces Excitotoxicity and Neurodegeneration in the Motor Cortex Via Caspase 3 Activation: Implication for Irreversible Motor Deficit

  • Pallavi Asthana
  • Ni Zhang
  • Gajendra Kumar
  • Virendra Bhagawan Chine
  • Kunal Kumar Singh
  • Yim Ling Mak
  • Leo Lai Chan
  • Paul Kwan Sing Lam
  • Chi Him Eddie Ma
Article

Abstract

Consumption of fish containing ciguatera toxins or ciguatoxins (CTXs) causes ciguatera fish poisoning (CFP). In some patients, CFP recurrence occurs even years after exposure related to CTXs accumulation. Pacific CTX-1 (P-CTX-1) is one of the most potent natural substances known that causes predominantly neurological symptoms in patients; however, the underlying pathogenies of CFP remain unknown. Using clinically relevant neurobehavioral tests and electromyography (EMG) to assess effects of P-CTX-1 during the 4 months after exposure, recurrent motor strength deficit occurred in mice exposed to P-CTX-1. We detected irreversible motor strength deficits accompanied by reduced EMG activity, demyelination, and slowing of motor nerve conduction, whereas control unexposed mice fully recovered in 1 month after peripheral nerve injury. Finally, to uncover the mechanism underlying CFP, we detected reduction of spontaneous firing rate of motor cortical neurons even 6 months after exposure and increased number of glial fibrillary acidic protein (GFAP)-immunoreactive astrocytes. Increased numbers of motor cortical neuron apoptosis were detected by dUTP-digoxigenin nick end labeling assay along with activation of caspase 3. Taken together, our study demonstrates that persistence of P-CTX-1 in the nervous system induces irreversible motor deficit that correlates well with excitotoxicity and neurodegeneration detected in the motor cortical neurons.

Keywords

Ciguatera fish poisoning Pacific ciguatoxin Excitotoxicity Neurodegeneration Apoptosis 

Notes

Acknowledgements

This work is supported in part by The Health and Medical Research Fund (HMRF), Food and Health Bureau, Hong Kong Special Administrative Region Government (Ref. No: 01122016 and 12134101), GRF grants from the Research Grant Council of the Hong Kong Special Administrative Region Government (CityU 11100015 and CityU 160813), SRG (7004587) and ARG (9667149) grants from the City University of Hong Kong award to Chi Ma, and the Collaborative Research Fund, the Research Grant Council of Hong Kong (C1012-15G) award to Paul Lam.

Authors’ Contributions

PA conducted in vivo electrophysiological study, NMJ and MBP quantification, performed sciatic nerve surgery and tissue harvest. NZ carried out the neurobehavioral assessments and data analysis with PA. GK performed single cell neuronal recording and GFAP staining. VBC and KKS performed experiments to confirm cell death. YLM performed P-CTX-1 extraction and tissue distribution analysis with expertise and resources provided by LLC and PKSL CHEM conceived the project and designed the study. PA, GK, and CHEM wrote the manuscript with inputs from all authors. All authors read and approved the final manuscript.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

12035_2018_875_MOESM1_ESM.pdf (701 kb)
ESM 1 (PDF 700 kb)

References

  1. 1.
    Dickey RW, Plakas SM (2010) Ciguatera: A public health perspective. Toxicon : Off J Int Soc Toxinology 56(2):123–136.  https://doi.org/10.1016/j.toxicon.2009.09.008 CrossRefGoogle Scholar
  2. 2.
    Bourdy G, Cabalion P, Amade P, Laurent D (1992) Traditional remedies used in the Western Pacific for the treatment of ciguatera poisoning. J Ethnopharmacol 36(2):163–174.  https://doi.org/10.1016/0378-8741(92)90017-L PubMedCrossRefGoogle Scholar
  3. 3.
    Banner AH (1976) Ciguatera: A disease from coral reef fish. Biol Geol Coral Reef 3:177–213CrossRefGoogle Scholar
  4. 4.
    Randall JE (1958) A review of ciguatera, tropical fish poisoning, with a tentative explanation of its cause. Bull Mar Sci 8(3):236–267Google Scholar
  5. 5.
    De Fouw J, Van Egmond H, Speijers GJA (2001) Ciguatera fish poisoning: A review.Google Scholar
  6. 6.
    Radke EG, Reich A, Morris JG, Jr. (2015) Epidemiology of Ciguatera in Florida. Am J Trop Med Hyg 93 (2):425–432. doi: https://doi.org/10.4269/ajtmh.14-0400
  7. 7.
    Lewis RJ (2000) Ciguatera management. SPC Live Reef Fish Information Bulletin 7:11–13Google Scholar
  8. 8.
    Barton ED, Tanner P, Turchen SG, Tunget CL, Manoguerra A, Clark RF (1995) Ciguatera fish poisoning. A southern California epidemic. West J Med 163(1):31–35PubMedPubMedCentralGoogle Scholar
  9. 9.
    Chan TY (1998) Lengthy persistence of ciguatoxin in the body. Trans R Soc Trop Med Hyg 92(6):662.  https://doi.org/10.1016/S0035-9203(98)90803-3 PubMedCrossRefGoogle Scholar
  10. 10.
    Hamilton B, Whittle N, Shaw G, Eaglesham G, Moore MR, Lewis RJ (2010) Human fatality associated with Pacific ciguatoxin contaminated fish. Toxicon 56(5):668–673.  https://doi.org/10.1016/j.toxicon.2009.06.007 PubMedCrossRefGoogle Scholar
  11. 11.
    Au NP, Kumar G, Asthana P, Tin C, Mak YL, Chan LL, Lam PK, Ma CH (2016) Ciguatoxin reduces regenerative capacity of axotomized peripheral neurons and delays functional recovery in pre-exposed mice after peripheral nerve injury. Sci Rep 6(1):26809.  https://doi.org/10.1038/srep26809 PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Kumar G, Au NP, Lei EN, Mak YL, Chan LL, Lam MH, Lam PK, Ma CH (2016) Acute exposure to Pacific ciguatoxin reduces electroencephalogram activity and disrupts neurotransmitter metabolic pathways in motor cortex. Mol Neurobiol 54(7):5590–5603.  https://doi.org/10.1007/s12035-016-0093-y PubMedCrossRefGoogle Scholar
  13. 13.
    Wang J, Cao B, Yang X, Wu J, Chan LL, Li Y (2017) Chronic ciguatoxin poisoning causes emotional and cognitive dysfunctions in rats. Toxicol Res 6(2):179–187.  https://doi.org/10.1039/C5TX00475F CrossRefGoogle Scholar
  14. 14.
    Bottein Dechraoui MY, Wang Z, Turquet J, Chinain M, Darius T, Cruchet P, Radwan FF, Dickey RW et al (2005) Biomonitoring of ciguatoxin exposure in mice using blood collection cards. Toxicon : Off J Int Soc Toxinology 46(3):243–251.  https://doi.org/10.1016/j.toxicon.2005.03.014 CrossRefGoogle Scholar
  15. 15.
    Benoit E, Juzans P, Legrand AM, Molgo J (1996) Nodal swelling produced by ciguatoxin-induced selective activation of sodium channels in myelinated nerve fibers. Neuroscience 71(4):1121–1131.  https://doi.org/10.1016/0306-4522(95)00506-4 PubMedCrossRefGoogle Scholar
  16. 16.
    Mattei C, Dechraoui MY, Molgo J, Meunier FA, Legrand AM, Benoit E (1999) Neurotoxins targetting receptor site 5 of voltage-dependent sodium channels increase the nodal volume of myelinated axons. J Neurosci Res 55(6):666–673.  https://doi.org/10.1002/(SICI)1097-4547(19990315)55:6<666::AID-JNR2>3.0.CO;2-H PubMedCrossRefGoogle Scholar
  17. 17.
    Hogg RC, Lewis RJ, Adams DJ (2002) Ciguatoxin-induced oscillations in membrane potential and action potential firing in rat parasympathetic neurons. Eur J Neurosci 16(2):242–248.  https://doi.org/10.1046/j.1460-9568.2002.02071.x PubMedCrossRefGoogle Scholar
  18. 18.
    Inserra MC, Israel MR, Caldwell A, Castro J, Deuis JR, Harrington AM, Keramidas A, Garcia-Caraballo S et al (2017) Multiple sodium channel isoforms mediate the pathological effects of Pacific ciguatoxin-1. Sci Rep 7:42810.  https://doi.org/10.1038/srep42810 PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Babiloni C, Lizio R, Marzano N, Capotosto P, Soricelli A, Triggiani AI, Cordone S, Gesualdo L et al (2016) Brain neural synchronization and functional coupling in Alzheimer's disease as revealed by resting state EEG rhythms. Int J Psychophysiol 103:88–102.  https://doi.org/10.1016/j.ijpsycho.2015.02.008 PubMedCrossRefGoogle Scholar
  20. 20.
    Foerster BR, Pomper MG, Callaghan BC, Petrou M, Edden RA, Mohamed MA, Welsh RC, Carlos RC et al (2013) An imbalance between excitatory and inhibitory neurotransmitters in amyotrophic lateral sclerosis revealed by use of 3-T proton magnetic resonance spectroscopy. JAMA Neurol 70(8):1009–1016.  https://doi.org/10.1001/jamaneurol.2013.234 PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Kehrer C, Maziashvili N, Dugladze T, Gloveli T (2008) Altered excitatory-inhibitory balance in the NMDA-hypofunction model of schizophrenia. Front Mol Neurosci 1:6.  https://doi.org/10.3389/neuro.02.006.2008 PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Ni Y, Su M, Lin J, Wang X, Qiu Y, Zhao A, Chen T, Jia W (2008) Metabolic profiling reveals disorder of amino acid metabolism in four brain regions from a rat model of chronic unpredictable mild stress. FEBS Lett 582(17):2627–2636.  https://doi.org/10.1016/j.febslet.2008.06.040 PubMedCrossRefGoogle Scholar
  23. 23.
    Rubenstein JL, Merzenich MM (2003) Model of autism: Increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2(5):255–267.  https://doi.org/10.1034/j.1601-183X.2003.00037.x PubMedCrossRefGoogle Scholar
  24. 24.
    Sun B, Halabisky B, Zhou Y, Palop JJ, Yu G, Mucke L, Gan L (2009) Imbalance between GABAergic and glutamatergic transmission impairs adult neurogenesis in an animal model of Alzheimer's disease. Cell Stem Cell 5(6):624–633.  https://doi.org/10.1016/j.stem.2009.10.003 PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Aosaki T, Miura M, Suzuki T, Nishimura K, Masuda M (2010) Acetylcholine-dopamine balance hypothesis in the striatum: An update. Geriatr Gerontol Int 10(Suppl 1):S148–S157.  https://doi.org/10.1111/j.1447-0594.2010.00588.x PubMedCrossRefGoogle Scholar
  26. 26.
    Dong XX, Wang Y, Qin ZH (2009) Molecular mechanisms of excitotoxicity and their relevance to pathogenesis of neurodegenerative diseases. Acta Pharmacol Sin 30(4):379–387.  https://doi.org/10.1038/aps.2009.24 PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Beal MF (1992) Mechanisms of excitotoxicity in neurologic diseases. FASEB J: Off Publ Fed Am Soc Exp Biol 6(15):3338–3344CrossRefGoogle Scholar
  28. 28.
    Shaw PJ (1994) Excitotoxicity and motor neurone disease: A review of the evidence. J Neurol Sci 124(Suppl):6–13.  https://doi.org/10.1016/0022-510X(94)90170-8 PubMedCrossRefGoogle Scholar
  29. 29.
    Beal MF (1998) Excitotoxicity and nitric oxide in Parkinson's disease pathogenesis. Ann Neurol 44(3 Suppl 1):S110–S114.  https://doi.org/10.1002/ana.410440716 PubMedCrossRefGoogle Scholar
  30. 30.
    Wu JJ, Mak YL, Murphy MB, Lam JC, Chan WH, Wang M, Chan LL, Lam PK (2011) Validation of an accelerated solvent extraction liquid chromatography-tandem mass spectrometry method for Pacific ciguatoxin-1 in fish flesh and comparison with the mouse neuroblastoma assay. Anal Bioanal Chem 400(9):3165–3175.  https://doi.org/10.1007/s00216-011-4977-4 PubMedCrossRefGoogle Scholar
  31. 31.
    Chan WH, Mak YL, JJ W, Jin L, Sit WH, Lam JC, Sadovy de Mitcheson Y, Chan LL et al (2011) Spatial distribution of ciguateric fish in the Republic of Kiribati. Chemosphere 84(1):117–123.  https://doi.org/10.1016/j.chemosphere.2011.02.036 PubMedCrossRefGoogle Scholar
  32. 32.
    Bottein MY, Wang Z, Ramsdell JS (2011) Toxicokinetics of the ciguatoxin P-CTX-1 in rats after intraperitoneal or oral administration. Toxicology 284(1–3):1–6.  https://doi.org/10.1016/j.tox.2011.02.005 PubMedCrossRefGoogle Scholar
  33. 33.
    Kumar G, Au NP, Lei EN, Mak YL, Chan LL, Lam MH, Chan LL, Lam PK et al (2016) Acute exposure to Pacific ciguatoxin reduces electroencephalogram activity and disrupts neurotransmitter metabolic pathways in motor cortex. Mol Neurobiol 54(7):5590–5603.  https://doi.org/10.1007/s12035-016-0093-y PubMedCrossRefGoogle Scholar
  34. 34.
    Ma CH, Brenner GJ, Omura T, Samad OA, Costigan M, Inquimbert P, Niederkofler V, Salie R et al (2011) The BMP coreceptor RGMb promotes while the endogenous BMP antagonist noggin reduces neurite outgrowth and peripheral nerve regeneration by modulating BMP signaling. J Neurosci 31(50):18391–18400.  https://doi.org/10.1523/JNEUROSCI.4550-11.2011 PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Ma CH, Omura T, Cobos EJ, Latremoliere A, Ghasemlou N, Brenner GJ, van Veen E, Barrett L et al (2011) Accelerating axonal growth promotes motor recovery after peripheral nerve injury in mice. J Clin Invest 121(11):4332–4347.  https://doi.org/10.1172/JCI58675 PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Inserra MM, Bloch DA, Terris DJ (1998) Functional indices for sciatic, peroneal, and posterior tibial nerve lesions in the mouse. Microsurgery 18(2):119–124.  https://doi.org/10.1002/(SICI)1098-2752(1998)18:2<119::AID-MICR10>3.0.CO;2-0 PubMedCrossRefGoogle Scholar
  37. 37.
    Painter MW, Brosius Lutz A, Cheng YC, Latremoliere A, Duong K, Miller CM, Posada S, Cobos EJ et al (2014) Diminished Schwann cell repair responses underlie age-associated impaired axonal regeneration. Neuron 83(2):331–343.  https://doi.org/10.1016/j.neuron.2014.06.016 PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Zhang X, Cao B, Wang J, Liu J, Tung VO, Lam PK, Chan LL, Li Y (2013) Neurotoxicity and reactive astrogliosis in the anterior cingulate cortex in acute ciguatera poisoning. NeuroMolecular Med 15(2):310–323.  https://doi.org/10.1007/s12017-013-8220-7 PubMedCrossRefGoogle Scholar
  39. 39.
    Pearn J (2001) Neurology of ciguatera. J Neurol Neurosurg Psychiatry 70(1):4–8.  https://doi.org/10.1136/jnnp.70.1.4 PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Bagnis R, Kuberski T, Laugier S (1979) Clinical observations on 3,009 cases of ciguatera (fish poisoning) in the South Pacific. Am J Trop Med Hyg 28(6):1067–1073.  https://doi.org/10.4269/ajtmh.1979.28.1067 PubMedCrossRefGoogle Scholar
  41. 41.
    Derouiche F, Cohen E, Rodier G, Boulay C, Courtois S (2000) Ciguatera and peripheral neuropathy: A case report. Rev Neurol (Paris) 156(5):514–516Google Scholar
  42. 42.
    Sozzi G, Marotta P, Aldeghi D, Tredici G, Calvi L (1988) Polyneuropathy secondary to ciguatoxin poisoning. Ital J Neurol Sci 9(5):491–495.  https://doi.org/10.1007/BF02337168 PubMedCrossRefGoogle Scholar
  43. 43.
    Deber CM, Reynolds SJ (1991) Central nervous system myelin: Structure, function, and pathology. Clin Biochem 24(2):113–134.  https://doi.org/10.1016/0009-9120(91)90421-A PubMedCrossRefGoogle Scholar
  44. 44.
    Weil MT, Mobius W, Winkler A, Ruhwedel T, Wrzos C, Romanelli E, Bennett JL, Enz L et al (2016) Loss of myelin basic protein function triggers myelin breakdown in models of demyelinating diseases. Cell Rep 16(2):314–322.  https://doi.org/10.1016/j.celrep.2016.06.008 PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Purves D, Augustine G, Fitzpatrick D, Katz L, LaMantia A, McNamara J, Williams S (2001) Increased conduction velocity as a result of myelination. NeuroscienceGoogle Scholar
  46. 46.
    Huxley C, Passage E, Robertson AM, Youl B, Huston S, Manson A, Saberan-Djoniedi D, Figarella-Branger D et al (1998) Correlation between varying levels of PMP22 expression and the degree of demyelination and reduction in nerve conduction velocity in transgenic mice. Hum Mol Genet 7(3):449–458.  https://doi.org/10.1093/hmg/7.3.449 PubMedCrossRefGoogle Scholar
  47. 47.
    Lim EF, Nakanishi ST, Hoghooghi V, Eaton SE, Palmer AL, Frederick A, Stratton JA, Stykel MG et al (2017) AlphaB-crystallin regulates remyelination after peripheral nerve injury. Proc Natl Acad Sci U S A 114(9):E1707–E1716.  https://doi.org/10.1073/pnas.1612136114 PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Tsodyks M, Kenet T, Grinvald A, Arieli A (1999) Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science 286(5446):1943–1946.  https://doi.org/10.1126/science.286.5446.1943 PubMedCrossRefGoogle Scholar
  49. 49.
    Philips T, Robberecht W (2011) Neuroinflammation in amyotrophic lateral sclerosis: Role of glial activation in motor neuron disease. Lancet Neurol 10(3):253–263.  https://doi.org/10.1016/S1474-4422(11)70015-1 PubMedCrossRefGoogle Scholar
  50. 50.
    O'Callaghan JP, Sriram K (2005) Glial fibrillary acidic protein and related glial proteins as biomarkers of neurotoxicity. Expert Opin Drug Saf 4(3):433–442.  https://doi.org/10.1517/14740338.4.3.433 PubMedCrossRefGoogle Scholar
  51. 51.
    Carron SF, Yan EB, Alwis DS, Rajan R (2016) Differential susceptibility of cortical and subcortical inhibitory neurons and astrocytes in the long term following diffuse traumatic brain injury. J Comp Neurol 524(17):3530–3560.  https://doi.org/10.1002/cne.24014 PubMedCrossRefGoogle Scholar
  52. 52.
    Faiz M, Sachewsky N, Gascon S, Bang KW, Morshead CM, Nagy A (2015) Adult neural stem cells from the subventricular zone give rise to reactive astrocytes in the cortex after stroke. Cell Stem Cell 17(5):624–634.  https://doi.org/10.1016/j.stem.2015.08.002 PubMedCrossRefGoogle Scholar
  53. 53.
    Jeong HK, Ji KM, Min KJ, Choi I, Choi DJ, Jou I, Joe EH (2014) Astrogliosis is a possible player in preventing delayed neuronal death. Mol Cells 37(4):345–355.  https://doi.org/10.14348/molcells.2014.0046 PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Buffo A, Rite I, Tripathi P, Lepier A, Colak D, Horn AP, Mori T, Gotz M (2008) Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain. Proc Natl Acad Sci U S A 105(9):3581–3586.  https://doi.org/10.1073/pnas.0709002105 PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    RAGELIS EP (1984) Ciguatera seafood poisoning: Overview. In. ACS Publications,Google Scholar
  56. 56.
    Skinner MP, Brewer TD, Johnstone R, Fleming LE, Lewis RJ (2011) Ciguatera fish poisoning in the Pacific Islands (1998 to 2008). PLoS Negl Trop Dis 5(12):e1416.  https://doi.org/10.1371/journal.pntd.0001416 PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Lehane L, Lewis RJ (2000) Ciguatera: Recent advances but the risk remains. Int J Food Microbiol 61(2–3):91–125.  https://doi.org/10.1016/S0168-1605(00)00382-2 PubMedCrossRefGoogle Scholar
  58. 58.
    Lewis RJ, Sellin M (1992) Multiple ciguatoxins in the flesh of fish. Toxicon : Off J Int Soc Toxinology 30(8):915–919.  https://doi.org/10.1016/0041-0101(92)90390-Q CrossRefGoogle Scholar
  59. 59.
    Katz AR, Terrell-Perica S, Sasaki DM (1993) Ciguatera on Kauai: Investigation of factors associated with severity of illness. Am J Trop Med Hyg 49(4):448–454.  https://doi.org/10.4269/ajtmh.1993.49.448 PubMedCrossRefGoogle Scholar
  60. 60.
    Bailey S (2014) Withers T (2014) ciguatera poisoning in the Cook Islands. BMJ Case Rep 2014(jun25 1):bcr2014204847.  https://doi.org/10.1136/bcr-2014-204847 PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Boada LD, Zumbado M, Luzardo OP, Almeida-Gonzalez M, Plakas SM, Granade HR, Abraham A, Jester EL et al (2010) Ciguatera fish poisoning on the West Africa Coast: An emerging risk in the Canary Islands (Spain). Toxicon : Off J Int Soc Toxinology 56(8):1516–1519.  https://doi.org/10.1016/j.toxicon.2010.07.021 CrossRefGoogle Scholar
  62. 62.
    Chateau-Degat ML, Beuter A, Vauterin G, Nguyen NL, Chinain M, Darius T, Legrand AM, Chansin R et al (2007) Neurologic signs of ciguatera disease: Evidence of their persistence. Am J Trop Med Hyg 77(6):1170–1175PubMedCrossRefGoogle Scholar
  63. 63.
    McKee DB, Fleming L, Tamer R, Weisman R, Blythe D (2001) Physician diagnosis and reporting of ciguatera fish poisoning in an endemic area. Harmful Algal Blooms 2000:451–453Google Scholar
  64. 64.
    Terao K, Ito E, Oarada M, Ishibashi Y, Legrand AM, Yasumoto T (1991) Light and electron microscopic studies of pathologic changes induced in mice by ciguatoxin poisoning. Toxicon : Off J Int Soc Toxinology 29(6):633–643.  https://doi.org/10.1016/0041-0101(91)90056-W CrossRefGoogle Scholar
  65. 65.
    Tunstall RJ, Mehan KA, Wadley GD, Collier GR, Bonen A, Hargreaves M, Cameron-Smith D (2002) Exercise training increases lipid metabolism gene expression in human skeletal muscle. Am J Physiol Endocrinol Metab 283(1):E66–E72.  https://doi.org/10.1152/ajpendo.00475.2001 PubMedCrossRefGoogle Scholar
  66. 66.
    Lange WR, Snyder FR, Fudala PJ (1992) Travel and ciguatera fish poisoning. Arch Intern Med 152(10):2049–2053.  https://doi.org/10.1001/archinte.1992.00400220075013 PubMedCrossRefGoogle Scholar
  67. 67.
    Nicholson GM, Lewis RJ (2006) Ciguatoxins: Cyclic polyether modulators of voltage-gated Iion channel function. Marine Drugs 4(3):82–118PubMedCentralCrossRefGoogle Scholar
  68. 68.
    Bagnis R (1993) Ciguatera fish poisoning.Google Scholar
  69. 69.
    Gillespie NC, Lewis RJ, Pearn JH, Bourke AT, Holmes MJ, Bourke JB, Shields WJ (1986) Ciguatera in Australia. Occurrence, clinical features, pathophysiology and management. Med J Aust 145(11–12):584–590PubMedGoogle Scholar
  70. 70.
    Glaziou P, Martin PM (1993) Study of factors that influence the clinical response to ciguatera fish poisoning. Toxicon 31(9):1151–1154.  https://doi.org/10.1016/0041-0101(93)90130-B PubMedCrossRefGoogle Scholar
  71. 71.
    Benoit E, Mattei C, Ouanounou G, Meunier FA, Suput D, Le Gall F, Marquais M, Dechraoui MY et al (2002) Ionic mechanisms involved in the nodal swelling of myelinated axons caused by marine toxins. Cell Mol Biol Lett 7(2):317–321PubMedGoogle Scholar
  72. 72.
    Allsop JL, Martini L, Lebris H, Pollard J, Walsh J, Hodgkinson S (1986) Neurologic manifestations of ciguatera. 3 cases with a neurophysiologic study and examination of one nerve biopsy. Rev Neurol (Paris) 142(6–7):590–597Google Scholar
  73. 73.
    Nawaz S, Kippert A, Saab AS, Werner HB, Lang T, Nave KA, Simons M (2009) Phosphatidylinositol 4,5-bisphosphate-dependent interaction of myelin basic protein with the plasma membrane in oligodendroglial cells and its rapid perturbation by elevated calcium. J Neurosci 29(15):4794–4807.  https://doi.org/10.1523/JNEUROSCI.3955-08.2009 PubMedCrossRefGoogle Scholar
  74. 74.
    Hidalgo J, Liberona JL, Molgo J, Jaimovich E (2002) Pacific ciguatoxin-1b effect over Na+ and K+ currents, inositol 1,4,5-triphosphate content and intracellular Ca2+ signals in cultured rat myotubes. Br J Pharmacol 137(7):1055–1062.  https://doi.org/10.1038/sj.bjp.0704980 PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Molgo J, Shimahara T, Legrand AM (1993) Ciguatoxin, extracted from poisonous morays eels, causes sodium-dependent calcium mobilization in NG108-15 neuroblastoma x glioma hybrid cells. Neurosci Lett 158(2):147–150.  https://doi.org/10.1016/0304-3940(93)90250-O PubMedCrossRefGoogle Scholar
  76. 76.
    Ryan JC, Morey JS, Bottein MY, Ramsdell JS, Van Dolah FM (2010) Gene expression profiling in brain of mice exposed to the marine neurotoxin ciguatoxin reveals an acute anti-inflammatory, neuroprotective response. BMC Neurosci 11(1):107.  https://doi.org/10.1186/1471-2202-11-107 PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Farooqui AA, Horrocks LA (1994) Involvement of glutamate receptors, lipases, and phospholipases in long-term potentiation and neurodegeneration. J Neurosci Res 38(1):6–11.  https://doi.org/10.1002/jnr.490380103 PubMedCrossRefGoogle Scholar
  78. 78.
    Ribeiro FM, Vieira LB, Pires RG, Olmo RP, Ferguson SS (2017) Metabotropic glutamate receptors and neurodegenerative diseases. Pharmacol Res 115:179–191.  https://doi.org/10.1016/j.phrs.2016.11.013 PubMedCrossRefGoogle Scholar
  79. 79.
    Butterfield DA, Pocernich CB (2003) The glutamatergic system and Alzheimer's disease: Therapeutic implications. CNS Drugs 17(9):641–652.  https://doi.org/10.2165/00023210-200317090-00004 PubMedCrossRefPubMedCentralGoogle Scholar
  80. 80.
    Litim N, Morissette M, Di Paolo T (2017) Metabotropic glutamate receptors as therapeutic targets in Parkinson's disease: An update from the last 5 years of research. Neuropharmacology 115:166–179.  https://doi.org/10.1016/j.neuropharm.2016.03.036 PubMedCrossRefGoogle Scholar
  81. 81.
    Rossi DJ, Oshima T, Attwell D (2000) Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403(6767):316–321.  https://doi.org/10.1038/35002090 PubMedCrossRefGoogle Scholar
  82. 82.
    Pitt D, Werner P, Raine CS (2000) Glutamate excitotoxicity in a model of multiple sclerosis. Nat Med 6(1):67–70.  https://doi.org/10.1038/71555 PubMedCrossRefGoogle Scholar
  83. 83.
    Barker-Haliski M, White HS (2015) Glutamatergic mechanisms associated with seizures and epilepsy. Cold Spring Harb Perspect Med 5(8):a022863.  https://doi.org/10.1101/cshperspect.a022863 PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Eulenburg V, Gomeza J (2010) Neurotransmitter transporters expressed in glial cells as regulators of synapse function. Brain Res Rev 63(1–2):103–112.  https://doi.org/10.1016/j.brainresrev.2010.01.003 PubMedCrossRefGoogle Scholar
  85. 85.
    Lenk K, Raisanen E, Hyttinen JA (2016) Understanding the role of astrocytic GABA in simulated neural networks. Conf Proc IEEE Eng Med Biol Soc 2016:6121–6124.  https://doi.org/10.1109/EMBC.2016.7592125 PubMedCrossRefGoogle Scholar
  86. 86.
    Barca-Mayo O, Pons-Espinal M, Follert P, Armirotti A, Berdondini L, De Pietri Tonelli D (2017) Astrocyte deletion of Bmal1 alters daily locomotor activity and cognitive functions via GABA signalling. Nat Commun 8:14336.  https://doi.org/10.1038/ncomms14336 PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Fattorini G, Melone M, Sanchez-Gomez MV, Arellano RO, Bassi S, Matute C, Conti F (2017) GAT-1 mediated GABA uptake in rat oligodendrocytes. Glia 65(3):514–522.  https://doi.org/10.1002/glia.23108 PubMedCrossRefGoogle Scholar
  88. 88.
    Jo S, Yarishkin O, Hwang YJ, Chun YE, Park M, Woo DH, Bae JY, Kim T et al (2014) GABA from reactive astrocytes impairs memory in mouse models of Alzheimer's disease. Nat Med 20(8):886–896.  https://doi.org/10.1038/nm.3639 PubMedCrossRefGoogle Scholar
  89. 89.
    Rothstein JD (2009) Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Ann Neurol 65 Suppl 1(S1):S3–S9.  https://doi.org/10.1002/ana.21543 PubMedCrossRefGoogle Scholar
  90. 90.
    Lewerenz J, Maher P (2015) Chronic glutamate toxicity in neurodegenerative diseases-what is the evidence? Front Neurosci 9:469.  https://doi.org/10.3389/fnins.2015.00469 PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Estrada Sanchez AM, Mejia-Toiber J, Massieu L (2008) Excitotoxic neuronal death and the pathogenesis of Huntington's disease. Arch Med Res 39(3):265–276.  https://doi.org/10.1016/j.arcmed.2007.11.011 PubMedCrossRefGoogle Scholar
  92. 92.
    Caudle WM, Zhang J (2009) Glutamate, excitotoxicity, and programmed cell death in Parkinson disease. Exp Neurol 220(2):230–233.  https://doi.org/10.1016/j.expneurol.2009.09.027 PubMedCrossRefGoogle Scholar
  93. 93.
    Hynd MR, Scott HL, Dodd PR (2004) Glutamate-mediated excitotoxicity and neurodegeneration in Alzheimer's disease. Neurochem Int 45(5):583–595.  https://doi.org/10.1016/j.neuint.2004.03.007 PubMedCrossRefGoogle Scholar
  94. 94.
    Rattray M, Bendotti C (2006) Does excitotoxic cell death of motor neurons in ALS arise from glutamate transporter and glutamate receptor abnormalities? Exp Neurol 201(1):15–23.  https://doi.org/10.1016/j.expneurol.2006.05.001 PubMedCrossRefGoogle Scholar
  95. 95.
    Tilleux S, Hermans E (2007) Neuroinflammation and regulation of glial glutamate uptake in neurological disorders. J Neurosci Res 85(10):2059–2070.  https://doi.org/10.1002/jnr.21325 PubMedCrossRefGoogle Scholar
  96. 96.
    Colangelo AM, Alberghina L, Papa M (2014) Astrogliosis as a therapeutic target for neurodegenerative diseases. Neurosci Lett 565:59–64.  https://doi.org/10.1016/j.neulet.2014.01.014 PubMedCrossRefGoogle Scholar
  97. 97.
    Eid T, Ghosh A, Wang Y, Beckstrom H, Zaveri HP, Lee TS, Lai JC, Malthankar-Phatak GH et al (2008) Recurrent seizures and brain pathology after inhibition of glutamine synthetase in the hippocampus in rats. Brain : a journal of neurology 131(Pt 8):2061–2070.  https://doi.org/10.1093/brain/awn133 CrossRefGoogle Scholar
  98. 98.
    van Landeghem FK, Weiss T, Oehmichen M, von Deimling A (2006) Decreased expression of glutamate transporters in astrocytes after human traumatic brain injury. J Neurotrauma 23(10):1518–1528.  https://doi.org/10.1089/neu.2006.23.1518 PubMedCrossRefGoogle Scholar
  99. 99.
    Knyazeva MG, Jalili M, Brioschi A, Bourquin I, Fornari E, Hasler M, Meuli R, Maeder P et al (2010) Topography of EEG multivariate phase synchronization in early Alzheimer's disease. Neurobiol Aging 31(7):1132–1144.  https://doi.org/10.1016/j.neurobiolaging.2008.07.019 PubMedCrossRefGoogle Scholar
  100. 100.
    Han CX, Wang J, Yi GS, Che YQ (2013) Investigation of EEG abnormalities in the early stage of Parkinson's disease. Cogn Neurodyn 7(4):351–359.  https://doi.org/10.1007/s11571-013-9247-z PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Vieregge P, Wauschkuhn B, Heberlein I, Hagenah J, Verleger R (1999) Selective attention is impaired in amyotrophic lateral sclerosis–a study of event-related EEG potentials. Brain research. Cogn Brain Res 8(1):27–35.  https://doi.org/10.1016/S0926-6410(99)00004-X CrossRefGoogle Scholar
  102. 102.
    Chaturvedi M, Hatz F, Gschwandtner U, Bogaarts JG, Meyer A, Fuhr P, Roth V (2017) Quantitative EEG (QEEG) measures differentiate Parkinson's disease (PD) patients from healthy controls (HC). Front Aging Neurosci 9:3.  https://doi.org/10.3389/fnagi.2017.00003 PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Schmidt MT, Kanda PA, Basile LF, da Silva Lopes HF, Baratho R, Demario JL, Jorge MS, Nardi AE et al (2013) Index of alpha/theta ratio of the electroencephalogram: A new marker for Alzheimer's disease. Front Aging Neurosci 5:60.  https://doi.org/10.3389/fnagi.2013.00060 PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Klassen BT, Hentz JG, Shill HA, Driver-Dunckley E, Evidente VG, Sabbagh MN, Adler CH, Caviness JN (2011) Quantitative EEG as a predictive biomarker for Parkinson disease dementia. Neurology 77(2):118–124.  https://doi.org/10.1212/WNL.0b013e318224af8d PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Westlake KP, Hinkley LB, Bucci M, Guggisberg AG, Byl N, Findlay AM, Henry RG, Nagarajan SS (2012) Resting state alpha-band functional connectivity and recovery after stroke. Exp Neurol 237(1):160–169.  https://doi.org/10.1016/j.expneurol.2012.06.020 PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Bertram L, Tanzi RE (2005) The genetic epidemiology of neurodegenerative disease. J Clin Invest 115(6):1449–1457.  https://doi.org/10.1172/JCI24761 PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Hatcher JM, Pennell KD, Miller GW (2008) Parkinson's disease and pesticides: A toxicological perspective. Trends Pharmacol Sci 29(6):322–329.  https://doi.org/10.1016/j.tips.2008.03.007 PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Pan-Montojo F, Reichmann H (2014) Considerations on the role of environmental toxins in idiopathic Parkinson's disease pathophysiology. Transl Neurodegener 3(1):10.  https://doi.org/10.1186/2047-9158-3-10 PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    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 PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Di Monte DA (2003) The environment and Parkinson's disease: Is the nigrostriatal system preferentially targeted by neurotoxins? Lancet Neurol 2(9):531–538.  https://doi.org/10.1016/S1474-4422(03)00501-5 PubMedCrossRefGoogle Scholar
  111. 111.
    Caller T, Henegan P, Stommel E (2017) The potential role of BMAA in neurodegeneration. Neurotox Res 33(1):222–226.  https://doi.org/10.1007/s12640-017-9752-7 PubMedCrossRefGoogle Scholar
  112. 112.
    Cox PA, Banack SA, Murch SJ (2003) Biomagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam. Proc Natl Acad Sci U S A 100(23):13380–13383.  https://doi.org/10.1073/pnas.2235808100 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Pallavi Asthana
    • 1
  • Ni Zhang
    • 1
  • Gajendra Kumar
    • 1
  • Virendra Bhagawan Chine
    • 1
  • Kunal Kumar Singh
    • 1
  • Yim Ling Mak
    • 2
    • 3
  • Leo Lai Chan
    • 1
    • 2
    • 3
  • Paul Kwan Sing Lam
    • 2
    • 3
    • 4
  • Chi Him Eddie Ma
    • 1
    • 2
    • 5
  1. 1.Department of Biomedical SciencesCity University of Hong KongHong KongHong Kong
  2. 2.State Key Laboratory in Marine PollutionCity University of Hong KongHong KongHong Kong
  3. 3.Shenzhen Key Laboratory for the Sustainable Use of Marine Biodiversity, Research Centre for the Oceans and Human HealthCity University of Hong Kong Shenzhen Research InstituteShenzhenChina
  4. 4.Department of Biology and ChemistryCity University of Hong KongHong KongHong Kong
  5. 5.Centre for Biosystems, Neuroscience, and NanotechnologyCity University of Hong KongHong KongHong Kong

Personalised recommendations