Uncovering the proteome response of murine neuroblastoma cells against low-dose exposure to saxitoxin

References

• Abi-Khalil C, Finkelstein DS, Conejero G, Du Bois J, Destoumieux-Garzon D, Rolland JL. 2017. The paralytic shellfish toxin, saxitoxin, enters the cytoplasm and induces apoptosis of oyster immune cells through a caspase-dependent pathway. Aquat Toxicol. 190:133–141.
   PubMed Web of Science ®Google Scholar
• Agrawal PB, Joshi M, Savic T, Chen Z, Beggs AH. 2012. Normal myofibrillar development followed by progressive sarcomeric disruption with actin accumulations in a mouse CFL2 knockout demonstrates requirement of cofilin-2 for muscle maintenance. Hum Mol Genet. 21:2341–2356.
   PubMed Web of Science ®Google Scholar
• Alexander J, Benford D, Cockburn A, Cravedi JP, Dogliotti E, Di Domenico A, Fernández-Cruz M, Fink-Gremmels J, Fürst P, Galli C, et al. 2008. Scientific Opinion of the Panel on Contaminants in the Food chain on a request from the European Commission on marine biotoxins in shellfish – azaspiracids. EFSA J. 723:1–52.
   Google Scholar
• Alexander J, Benford D, Cockburn A, Cravedi JP, Dogliotti E, Di Domenico AD, Fernández-Cruz ML, Fink-Gremmels J, Fürst P, Galli C, et al. 2009. Scientific Opinion of the Panel on Contaminants in the Food Chain on a request from the European Commission on marine biotoxins in shellfish – saxitoxin group. EFSA J. 1019:1–76.
   Google Scholar
• Anitha A, Nakamura K, Thanseem I, Matsuzaki H, Miyachi T, Tsujii M, Iwata Y, Suzuki K, Sugiyama T, Mori N, et al. 2013. Downregulation of the expression of mitochondrial electron transport complex genes in autism brains. Brain Pathol. 23:294–302.
   PubMed Web of Science ®Google Scholar
• Astuya A, Carrera C, Ulloa V, Aballay A, Núñez-Acuña G, Hégaret H, Gallardo-Escárate C. 2015. Saxitoxin modulates immunological parameters and gene transcription in Mytilus chilensis hemocytes. Int J Mol Sci. 16:15235–15250.
   PubMed Web of Science ®Google Scholar
• Chen HK, Fernandez-Funez P, Acevedo SF, Lam YC, Kaytor MD, Fernandez MH, Aitken A, Skoulakis EM, Orr HT, Botas J, et al. 2003. Interaction of Akt-phosphorylated ataxin-1 with 14-3-3 mediates neurodegeneration in spinocerebellar ataxia type 1. Cell. 113:457–468.
   PubMed Web of Science ®Google Scholar
• Cliff R, Curran J, Hirota JA, Brauer M, Feldman H, Carlsten C. 2016. Effect of diesel exhaust inhalation on blood markers of inflammation and neurotoxicity: a controlled, blinded crossover study. Inhal Toxicol. 28:145–153.
   PubMed Web of Science ®Google Scholar
• da Silva CA, de Morais ECP, Costa MDM, Ribas JLC, Guiloski IC, Ramsdorf WA, Zanata SM, Cestari MM, Ribeiro CAO, Magalhães VF, et al. 2014. Saxitoxins induce cytotoxicity, genotoxicity and oxidative stress in teleost neurons in vitro. Toxicon. 86:8–15.
   PubMed Web of Science ®Google Scholar
• da Silva CA, Oba ET, Ramsdorf WA, Magalhães VF, Cestari MM, Oliveira Ribeiro CA, Silva de Assis HC. 2011. First report about saxitoxins in freshwater fish Hoplias malabaricus through trophic exposure. Toxicon. 57:141–147.
   PubMed Web of Science ®Google Scholar
• Davis CC. 1948. Gymnodinium breve: a cause of discolored water and animal mortality in the Gulf of Mexico. Bot Gaz. 109:358–360.
   Web of Science ®Google Scholar
• Fougerousse F, Edom-Vovard F, Merkulova T, Ott MO, Durand M, Butler-Browne G, Keller A. 2001. The muscle-specific enolase is an early marker of human myogenesis. J Muscle Res Cell Motil. 22:535–544.
   PubMed Web of Science ®Google Scholar
• Goehe RW, Shultz JC, Murudkar C, Usanovic S, Lamour NF, Massey DH, Zhang L, Camidge DR, Shay JW, Minna JD, et al. 2010. hnRNP L regulates the tumorigenic capacity of lung cancer xenografts in mice via caspase-9 pre-mRNA processing. J Clin Invest. 120:3923–3939.
   PubMed Web of Science ®Google Scholar
• Hong Y, Jang SW, Ye K. 2011. The N-terminal fragment from caspase-cleaved serine/arginine protein-specific kinase 2 (SRPK2) translocates into the nucleus and promotes apoptosis. J Biol Chem. 286:777–786.
   PubMed Web of Science ®Google Scholar
• Isgrò MA, Bottoni P, Scatena R. 2015. Neuron-specific enolase as a biomarker: biochemical and clinical aspects. Adv Exp Med Biol. 867:125–143.
   PubMed Web of Science ®Google Scholar
• Jovanovic K, Chetty CJ, Khumalo T, Da Costa Dias B, Ferreira E, Malindisa ST, Caveney R, Letsolo BT, Weiss SFT. 2015. Novel patented therapeutic approaches targeting the 37/67 kDa laminin receptor for treatment of cancer and Alzheimer’s disease. Expert Opin Ther Pat. 25:567–582.
   PubMed Web of Science ®Google Scholar
• Keller A, Peltzer J, Carpentier G, Horváth I, Oláh J, Duchesnay A, Orosz F, Ovádi J. 2007. Interactions of enolase isoforms with tubulin and microtubules during myogenesis. Biochim Biophys Acta. 1770: 919–926.
   PubMed Web of Science ®Google Scholar
• Liao Y, Hao Y, Chen H, He Q, Yuan Z, Cheng J. 2015. Mitochondrial calcium uniporter protein MCU is involved in oxidative stress-induced cell death. Protein Cell. 6:434–442.
   PubMed Web of Science ®Google Scholar
• Liu G, Lei L, Yu J, Kung S, Xie J. 2014. Refinement of the spectra of exon usage by combined effects of extracellular stimulus and intracellular factors. Biochim Biophys Acta. 1839:537–545.
   PubMedGoogle Scholar
• Llewellyn LE. 2006. Saxitoxin, a toxic marine natural product that targets a multitude of receptors. Nat Prod Rep. 23:200–222.
   PubMed Web of Science ®Google Scholar
• Manczak M, Reddy PH. 2012. Abnormal interaction of VDAC1 with amyloid beta and phosphorylated tau causes mitochondrial dysfunction in Alzheimer’s disease. Hum Mol Genet. 21:5131–5146.
   PubMed Web of Science ®Google Scholar
• Manczak M, Sheiko T, Craigen WJ, Reddy PH. 2013. Reduced VDAC1 protects against Alzheimer’s disease, mitochondria, and synaptic deficiencies. J Alzheimers Dis. 37:679–690.
   PubMed Web of Science ®Google Scholar
• Melegari SP, de Carvalho Pinto CRS, Moukha S, Creppy EE, Matias WG. 2015. Evaluation of cytotoxicity and cell death induced in vitro by saxitoxin in mammalian cells. J Toxicol Environ Health A. 78:1189–1200.
   PubMed Web of Science ®Google Scholar
• Melegari SP, Perreault F, Moukha S, Popovic R, Creppy EE, Matias WG. 2012. Induction to oxidative stress by saxitoxin investigated through lipid peroxidation in Neuro 2A cells and Chlamydomonas reinhardtii alga. Chemosphere. 89:38–43.
   PubMed Web of Science ®Google Scholar
• Mullins RD, Heuser JA, Pollard TD. 1998. The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc Natl Acad Sci USA. 95:6181–6186.
   PubMed Web of Science ®Google Scholar
• Ni R, Zheng D, Xiong S, Hill DJ, Sun T, Gardiner RB, Fan G-C, Lu Y, Abel ED, Greer PA, et al. 2016. Mitochondrial calpain-1 disrupts ATP synthase and induces superoxide generation in type 1 diabetic hearts: a novel mechanism contributing to diabetic cardiomyopathy. Diabetes. 65:255–268.
   PubMed Web of Science ®Google Scholar
• O’Mullane MJ, Baker MS. 1998. Loss of cell viability dramatically elevates cell surface plasminogen binding and activation. Exp Cell Res. 242:153–164.
   PubMed Web of Science ®Google Scholar
• O’Neill K, Musgrave IF, Humpage A. 2016. Low dose extended exposure to saxitoxin and its potential neurodevelopmental effects: a review. Environ Toxicol Pharmacol. 48:7–16.
   PubMed Web of Science ®Google Scholar
• O’Neill K, Musgrave IF, Humpage A. 2017. Extended low-dose exposure to saxitoxin inhibits neurite outgrowth in model neuronal cells. Basic Clin Pharmacol Toxicol. 120:390–397.
   PubMed Web of Science ®Google Scholar
• Oberemm A, Becker J, Codd GA, Steinberg C. 1999. Effects of cyanobacterial toxins and aqueous crude extracts of cyanobacteria on the development of fish and amphibians. Environ Toxicol. 14:77–88.
   Web of Science ®Google Scholar
• Pratheepa V, Vasconcelos V. 2017. Binding and pharmacokinetics of the sodium channel blocking toxins (saxitoxin and the tetrodotoxins). Mini Rev Med Chem. 17:320–327.
   PubMed Web of Science ®Google Scholar
• Savio-Galimberti E, Gollob MH, Darbar D. 2012. Voltage-gated sodium channels: biophysics, pharmacology, and related channelopathies. Front Pharmacol. 3:124.
   PubMed Web of Science ®Google Scholar
• Schütz R, Kuratli K, Richard N, Stoll C, Schwager J. 2016. Mitochondrial and glycolytic activity of UV-irradiated human keratinocytes and its stimulation by a Saccharomyces cerevisiae autolysate. J Photochem Photobiol B. 159:142–148.
   PubMed Web of Science ®Google Scholar
• Shinoda S, Skradski SL, Araki T, Schindler CK, Meller R, Lan J-Q, Taki W, Simon RP, Henshall DC. 2003. Formation of a tumour necrosis factor receptor 1 molecular scaffolding complex and activation of apoptosis signal-regulating kinase 1 during seizure-induced neuronal death. Eur J Neurosci. 17:2065–2076.
   PubMed Web of Science ®Google Scholar
• Smani D, Sarkar S, Raymick J, Kanungo J, Paule MG, Gu Q. 2017. Downregulation of 14-3-3 Proteins in a Kainic Acid-Induced Neurotoxicity Model. Mol Neurobiol. [accessed 2017 Aug 24]. DOI:10.1007/s12035-017-0724-y
   PubMed Web of Science ®Google Scholar
• Sommer H, Meyer KF. 1937. Paralytic shellfish poisoning. Arch Path. 24:560–598.
   Google Scholar
• Sun H, Varela D, Chartier D, Ruben PC, Nattel S, Zamponi GW, Leblanc N. 2008. Differential interactions of Na+ channel toxins with T-type Ca2+ channels. J Gen Physiol. 132:101–113.
   PubMed Web of Science ®Google Scholar
• Vartiainen MK, Mustonen T, Mattila PK, Ojala PJ, Thesleff I, Partanen J, Lappalainen P. 2002. The three mouse actin-depolymerizing factor/cofilins evolved to fulfill cell-type-specific requirements for actin dynamics. Mol Biol Cell. 13:183–194.
   PubMed Web of Science ®Google Scholar
• Wang J, Salata JJ, Bennett PB. 2003. Saxitoxin is a gating modifier of HERG K + channels. J Gen Physiol. 121:583–598.
   PubMed Web of Science ®Google Scholar
• Yu J, Hai Y, Liu G, Fang T, Kung SKP, Xie J. 2009. The heterogeneous nuclear ribonucleoprotein L is an essential component in the Ca2+/calmodulin-dependent protein kinase IV-regulated alternative splicing through cytidine-adenosine repeats. J Biol Chem. 284:1505–1513.
   PubMed Web of Science ®Google Scholar
• Zou L, Wu C, Wang Q, Zhou J, Su K, Li H, Hu N, Wang P. 2015. An improved sensitive assay for the detection of PSP toxins with neuroblastoma cell-based impedance biosensor. Biosens Bioelectron. 67:458–464.
   PubMed Web of Science ®Google Scholar
• Züngün C, Yilmaz FM, Tutkun E, Yilmaz H, Uysal S. 2013. Assessment of serum S100B and neuron specific enolase levels to evaluate the neurotoxıc effects of organıc solvent exposure. Clin Toxicol (Phila). 51:748–751.
   PubMed Web of Science ®Google Scholar