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Neuroplastic and neuropathological changes in the central nervous system of the Gray mussel Crenomytilus grayanus (Dunker) under environmental stress

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Invertebrate Neuroscience

Abstract

We studied here neuron ultrastructure, synaptic plasticity and subcellular localization of NADPH-diaphorase (NADPH-d), a cytochemical marker for nitric oxide syntase, in the pedal ganglia of the Gray mussel Crenomytilus grayanus sampled from the polluted and reference sites in Amursky Bay (Sea of Japan) at lower and higher water temperature (in the beginning and the end of August, respectively). At lower temperature, neuroplastic changes in mussel ganglia prevailed: a sharp increase in the number of cytosomes in NADPH-d-positive neurons and a sharp decrease in the number of mitochondria in both NADPH-d-positive and NADPH-d-negative neurons. At higher temperature, neurodegenerative changes prevailed: disruption of a part of NADPH-d-negative axons and interneuronal contacts, formation of concentric lamellar structures in the neuropils, and accumulation of autophagosomes in NADPH-d negative neurons. The results suggest that the stress-induced production of nitric oxide in cytosomes of mussel neurons and plasticity of gap junctions have a neuroprotective effect.

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References

  • Abele D, Philipp E, Gonzalez PM, Puntarulo S (2007) Marine invertebrate mitochondria and oxidative stress. Front Biosci 12:933–946

    Article  CAS  PubMed  Google Scholar 

  • Alderton WK, Cooper CE, Knowles RG (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357:593–615

    Article  CAS  PubMed  Google Scholar 

  • Annikova LV, Pimenova EA, Dyuizen IV, Varaksin AA (2000) Localization of NO-ergic elements in the central nervous system of the bivalve mollusk Crenomytilus grayanus. J Evol Biochem Physiol 36:588–594

    CAS  Google Scholar 

  • Blottner D, Grozdanovic Z, Gossrau R (1995) Histochemistry of nitric oxide synthase in the nervous system. Histochem J 27:785–811

    CAS  PubMed  Google Scholar 

  • Bogolepov NN (1983) Ultrastructure of the brain in hypoxia. Imported Publications, Chicago (Published in the USSR by Mir Publishers, Moscow)

  • Brazhe (Ulyanova) NA, Erokhova LA, Churin AA, Maksimov GV (2005) The relation of different-scale membrane processes under nitric oxide influence. J Biol Phys 31:533–546

    Google Scholar 

  • Bredt DS, Snyder SN (1992) Nitric oxide, a novel neuronal messenger. Neuron 8:3–11

    Article  CAS  PubMed  Google Scholar 

  • Brown GC (2001) Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase. Biochim Biophys Acta Bioenerg 1504:46–57

    Article  CAS  Google Scholar 

  • Brown GC, Borutaite V (2007) Nitric oxide and mitochondrial respiration in the heart. Cardiovasc Res 75:283–290

    Article  CAS  PubMed  Google Scholar 

  • Calabrese V, Bates TE, Stella AMG (2000) NO synthase and NO-dependent signal pathways in brain aging and neurodegenerative disorders: the role of oxidant/antioxidant balance. Neurochem Res 25:1315–1341

    Article  CAS  PubMed  Google Scholar 

  • Calabrese V, Mancuso C, Calvani M, Rizzarelli E, Butterfield DA, Stella AMG (2007) Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat Rev Neurosci 8:766–775

    Article  CAS  PubMed  Google Scholar 

  • Casares FM, Mantione KJ (2006) Pesticides may be altering constitutive nitric oxide release, thereby compromising. Med Sci Mon Int Med J Exp Clin Res 12:235–240

    Google Scholar 

  • Chu CT (2006) Autophagic stress in neuronal injury and disease. J Neuropathol Exp Neurol 65:423–432

    Article  PubMed  Google Scholar 

  • Colasanti M, Venturini G (1998) Nitric oxide in invertebrates. Mol Neurobiol 17:157–174

    Article  CAS  PubMed  Google Scholar 

  • Conley DJ, Carstensen J, Ærtebjerg G, Christensen PB, Dalsgaard T, Hansen JLS, Josefson AB (2007) Long-term changes and impacts of hypoxia in Danish coastal waters. Ecol Appl 17(5):165–184

    Article  Google Scholar 

  • Dawson TM, Bredt DS, Fotuhi MH, Wang PM, Snyder SH (1991) Nitric oxide synthase and neuronal NADPH-diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci USA 88:7797–7801

    Article  CAS  PubMed  Google Scholar 

  • Dermietzel R, Spray DC (1993) Gap junctions in the brain: where, what type, how many and why? Trends Neurosci 16:186–192

    Article  CAS  PubMed  Google Scholar 

  • Erokhova LA, Brazhe NA, Maksimov GV, Rubin AB (2005) Analysis of conformational changes in neuronal carotenoids under the influence of neuromediator. Doklady Biochem Biophys 402:233–235

    Article  CAS  Google Scholar 

  • Essawy AE, Abdelmeguied NE, Radwan MA, Hamed SS, Hegazy AE (2009) Neuropathological effect of carbamate molluscicides on the land snail, Eobania vermiculata. Cell Biol Toxicol 25:275–290

    Article  CAS  PubMed  Google Scholar 

  • Fiskum G (2001) Mitochondrial dysfunction in the pathogenesis of acute neural cell death. In: Lemasters JJ, Nieminen AL (eds) Mitochondria in pathogenesis. Kluwer Academic/Plenum Publishers, New York, pp 317–331

    Google Scholar 

  • Giovine M, Pozzolini M, Fayre A, Bavestrello G, Cerrano C, Ottaviani F, Chiarantini L, Cerasi A, Cangiotti M, Zocchi E, Scarfi S, Sara M, Benattitt U (2001) Heat stress-activated, calcium-dependent nitric oxide synthase in sponges. Nitric Oxide 5:427–431

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez PM, Abele D, Puntarulo S (2008) Iron and radical content in Mya arenaria: possible sources of NO generation. Aquat Toxicol 89:122–128

    Article  CAS  PubMed  Google Scholar 

  • Hope BT, Michael GJ, Knigge KM, Vincent SR (1991) Neuronal NADPH-diaphorase is a nitric oxide synthase. Proc Natl Acad Sci USA 88:2811–2814

    Article  CAS  PubMed  Google Scholar 

  • Huynh P, Boyd SK (2007) Nitric oxide synthase and NADPH diaphorase distribution in the bullfrog (Rana catesbeiana) CNS: pathways and functional implications. Brain Behav Evol 70:145–163

    Article  PubMed  Google Scholar 

  • Kakkar P, Singh BK (2007) Mitochondria: a hub of redox activities and cellular distress control. Mol Cell Biochem 305:235–253

    Article  CAS  PubMed  Google Scholar 

  • Karnaukhov VN (1971) Carotenoids in oxidative metabolism of molluscoid neurons. Exp Cell Res 64:301–306

    Article  CAS  PubMed  Google Scholar 

  • Keating DJ (2008) Mitochondrial dysfunction, oxidative stress, regulation of exocytosis and their relevance to neurodegenerative diseases. J Neurochem 104:298–305

    CAS  PubMed  Google Scholar 

  • Kiss JP, Vizi ES (2001) Nitric oxide: a novel link between synaptic and nonsynaptic transmission. Trends Neurosci 24:211–215

    Article  CAS  PubMed  Google Scholar 

  • Kotsyuba EP (2008) Effect of elevated temperature and of hypoxia on NO activity in the central nervous system of bivalve molluscs. J Evol Biochem Physiol 44:237–246

    Article  CAS  Google Scholar 

  • Kotsyuba EP, Kotsyuba AE (2003) NO-synthase in the central nervous system of freshwater bivalve mollusc Nodularia vladivostokensis in norm and in hypoxia. J Evol Biochem Physiol 39:235–240

    Article  CAS  Google Scholar 

  • Larade K, Storey KB (2002) A profile of the metabolic responses to anoxia in marine invertebrates. In: Storey KB, Storey JM (eds) Cell and molecular response to stress 3: sensing: signaling and cell adaptation. Elsevier, Amsterdam, pp 27–46

    Chapter  Google Scholar 

  • López-Costa JJ, Acuipil C, Tagliaferro P, Patel S, Ramos J, Brusco A, Saavedra JP (2002) Distribution of NADPH-diaphorase in rat mesencephalon: a light and electron microscopical study. Biocell 26:247–252

    PubMed  Google Scholar 

  • Mancuso C, Scapagnini G, Curro D, Stella AMG, De Marco C, Butterfield DA, Calabrese V (2007) Mitochondrial dysfunction, free radical generation and cellular stress response in neurodegenerative disorders. Front Biosci 12:1107–1123

    Article  CAS  PubMed  Google Scholar 

  • Manduzio H, Rocher B, Durand F, Galap C, Leboulenger F (2005) The point about oxidative stress in mollusks. Invert Survival J 2:91–104

    Google Scholar 

  • Matsumoto T, Nakane M, Pollock JS, Kuk JE, Förstermann U (1993) A correlation between soluble brain nitric oxide synthase and NADPH-diaphorase activity is only seen after exposure of the tissue to fixative. Neurosci Lett 155:61–64

    Article  CAS  PubMed  Google Scholar 

  • Mattson MP (2007) Mitochondrial regulation of neuronal plasticity. Neurochem Res 32:707–715

    Article  CAS  PubMed  Google Scholar 

  • Moore MN (2008) Autophagy as a second level protective process in conferring resistance to environmentally-induced oxidative stress. Autophagy 4:254–256

    CAS  PubMed  Google Scholar 

  • Moore MN, Viarengo A, Donkin P, Hawkins AJS (2007) Autophagic and lysosomal reactions to stress in the hepatopancreas of blue mussels. Aquat Toxicol 84:80–91

    Article  CAS  PubMed  Google Scholar 

  • Moroz L (2000) Giant identified NO-releasing neurons and comparative histochemistry of putative nitrergic systems in gastropod molluscs. Microsc Res Tech 49:557–569

    Article  CAS  PubMed  Google Scholar 

  • Motavkine PA, Varaksine AA (1989) Le reproduction chez lez mollusques bivalves role du systeme nervaux et regulation. Rapports Scientifiques et Techniques de l’IFREMER, 10. IFREMER, Brest, France

  • Zs.-Nagy I (1977) Cytosomes (yellow pigment granules) of mollusks as cell organelles of anoxic energy production. Int Rev Cytol 49:331–377

    Google Scholar 

  • Newcomb JM, Watson WH (2001) Identifiable nitrergic neurons in the central nervous system of the nudibranch Melibe leonina localized with NADPH-diaphorase histochemistry and nitric oxide synthase immunoreactivity. J Comp Neurol 437:70–78

    Article  CAS  PubMed  Google Scholar 

  • Palumbo A (2005) Nitric oxide in marine invertebrates: a comparative perspective. Comp Biochem Physiol A 142:241–248

    Article  Google Scholar 

  • Pedersen PL (1999) Mitochondrial events in the life and death of animal cells: a brief overview. J Bioenerg Biomembr 31:291–304

    Article  CAS  PubMed  Google Scholar 

  • Petrunyaka VV (1982) Localization and role of carotenoids in molluscan neurons. Cell Mol Neurobiol 1:11–20

    Article  Google Scholar 

  • Puka-Sundvall M, Gajkowska B, Cholewinski M, Blomgren K, Lazarewicz JW, Hagberg H (2000) Subcellular distribution of calcium and ultrastructural changes after cerebral hypoxia–ischemia in immature rats. Dev Brain Res 125:31–41

    Article  CAS  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  CAS  PubMed  Google Scholar 

  • Rothe F, Langnaese K, Wolf G (2005) New aspects of the location of neuronal nitric oxide synthase in the skeletal muscle: a light and electron microscopic study. Nitric Oxide 13:21–35

    Article  CAS  PubMed  Google Scholar 

  • Ruzhinskaya NN, Gdovskii PA (2002) NADPH-diaphorase in the olfactory system of the carp Cyprinus carpio. J Evol Biochem Physiol 38:114–120

    Article  CAS  Google Scholar 

  • Smith KL, Galloway TS, Depledge MH (2000) Neuro-endocrine biomarkers of population-induced stress in marine invertebrates. Sci Total Environ 262:185–190

    Article  CAS  PubMed  Google Scholar 

  • Talhouk RS, Zeinieh MP, Mikati MA, El-Sabban ME (2008) Gap junctional intercellular communication in hypoxia–ischemia-induced neuronal injury. Prog Neurobiol 84:57–76

    Article  CAS  PubMed  Google Scholar 

  • Tishchenko PYa, Sergeev AF, Lobanov VB, Zvalinsky VI, Koltunov AM, Mikhajlik TA, Tishchenko PP, Shevtsova MG (2008) Hypoxia of the bottom waters of Amursky Bay. Vestnik DVO RAN (Bulletin of the Far Eastern Branch of the Russian Academy of Sciences) 6:115–125 (in Russian with English summary)

  • Tseng C-Y, Lue J-H, Chang H-M, Wen C-Y, Shieh J-Y (2000) Ultrastructural localisation of NADPH-d/nNOS expression in the superior cervical ganglion of the hamster. J Anat 197:461–475

    Article  CAS  PubMed  Google Scholar 

  • Vaschenko MA (2000) Pollution in Peter the Great Bay, Sea of Japan, and its biological consequences. Rus J Mar Biol 26:155–166

    Article  Google Scholar 

  • Vaschenko MA, Kotsyuba EP (2008) NADPH-diaphorase activity in the central nervous system of the Gray mussel Crenomytilus grayanus (Dunker) under stress conditions: a histochemical study. Mar Environ Res 66:249–258

    Article  CAS  PubMed  Google Scholar 

  • Wiemann M, Wittkowski W, Altrup U, Speckmann E-J (1996) Alterations of neuronal fibers after epileptic activity induced by pentylenetetrazole: fine structure investigated by calcium cytochemistry and neurobiotin labeling (buccal ganglia, Helix pomatia). Cell Tissue Res 286:43–53

    Article  CAS  PubMed  Google Scholar 

  • Wolf G (1997) Nitric oxide and nitric oxide synthase: biology, pathology, localization. Histol Histopathol 12:251–261

    CAS  PubMed  Google Scholar 

  • Wolf G, Würdig S, Schünzel G (1992) Nitric oxide synthase in rat brain is predominantly located at neuronal endoplasmic reticulum: an electron microscopic demonstration of NADPH-diaphorase activity. Neurosci Lett 147:63–66

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Far Eastern Branch of the Russian Academy of Sciences (09-1-II 16-04, 09-III-A-06-194). We declare that the experiments comply with the current laws in Russian Federation, the country in which the experiments were performed.

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Correspondence to Marina A. Vaschenko.

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Kotsyuba, E.P., Vaschenko, M.A. Neuroplastic and neuropathological changes in the central nervous system of the Gray mussel Crenomytilus grayanus (Dunker) under environmental stress. Invert Neurosci 10, 35–46 (2010). https://doi.org/10.1007/s10158-010-0103-0

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