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Theory in Biosciences

, Volume 131, Issue 4, pp 253–264 | Cite as

A kinetic approach to assess oxidative metabolism related features in the bivalve Mya arenaria

  • Paula Mariela González
  • Doris Abele
  • Susana PuntaruloEmail author
Original Paper

Abstract

Electron paramagnetic resonance uses the resonant microwave radiation absorption of paramagnetic substances to detect highly reactive and, therefore, short-lived oxygen and nitrogen centered radicals. Previously, steady state concentrations of nitric oxide, ascorbyl radical (A·) and the labile iron pool (LIP) were determined in digestive gland of freshly collected animals from the North Sea bivalve Mya arenaria. The application of a simple kinetic analysis of these data based on elemental reactions allowed us to estimate the steady state concentrations of superoxide anion, the rate of A· disappearance and the content of unsaturated lipids. This analysis applied to a marine invertebrate opens the possibility of a mechanistic understanding of the complexity of free radical and LIP interactions in a metabolically slow, cold water organism under unstressed conditions. This data can be further used as a basis to assess the cellular response to stress in a simple system as the bivalve M. arenaria that can then be compared to cells of higher organisms.

Keywords

Kinetic approach Ascorbyl radical Labile iron pool Superoxide anion Unsaturated fatty acids 

Notes

Acknowledgments

This study was supported by grants from the University of Buenos Aires, National Council for Science and Technology (CONICET) (PIP 1171) and DAAD-CONICET collaborative visit. S.P. is career investigator from CONICET and P.M.G. is a postdoctoral fellow from CONICET.

References

  1. Abele D, Burlando B, Viarengo A, Pörtner HO (1998) Exposure to elevated temperatures and hydrogen peroxide elicits oxidative stress and antioxidant response in the Antarctic intertidal limpet Nacella concinna. Comp Biochem Physiol B 120:425–435CrossRefGoogle Scholar
  2. Abele D, Heise K, Pörtner HO, Puntarulo S (2002) Temperature-dependence of mitochondrial function and production of reactive oxygen species in the intertidal mud clam Mya arenaria. J Exp Biol 205:1831–1841PubMedGoogle Scholar
  3. Abele D, Philipp E, González PM, Puntarulo S (2007) Marine invertebrate mitochondria and oxidative stress. Front Biosci 12:933–946PubMedCrossRefGoogle Scholar
  4. Abele D, Kruppe M, Philipp EER, Brey T (2010) Mantle cavity water oxygen partial pressure (Po2) in marine molluscs aligns with lifestyle. Can J Fish Aquat Sci 53:1–11Google Scholar
  5. Abele-Oeschger D (1996) A comparative study of superoxide dismutase activity in marine benthic invertebrates with respect to environmental sulphide exposure. J Exp Mar Bio Ecol 197:39–49CrossRefGoogle Scholar
  6. Ahearn GA, Mandal PK, Mandal A (2004) Mechanisms of heavy-metal sequestration and detoxification in crustaceans: a review. J Comp Physiol 174(6):439–452Google Scholar
  7. Ahn I-Y, Lee SH, Kim KT, Shim JH, Kim DY (1996) Baseline heavy metal concentrations in the Antarctic clam, Laternula elliptica in Maxwell Bay, King George Island Antarctica. Mar Poll Bull 32:592–598CrossRefGoogle Scholar
  8. Aloísio Torres M, Pires Testa C, Gáspari C, Masutti MB, Neves Panitz CM, Curi-Pedrosa R, Alves de Almeida E, Di Mascio P, Wilhelm Filho D (2002) Oxidative stress in the mussel Mytella guyanensis from polluted mangroves on Santa Catarina Island. Braz Mar Pollut Bull 44(9):923–932CrossRefGoogle Scholar
  9. Alves de Almeida E, Dias Bainy AC, de Melo Loureiro AP, Martinez GR, Miyamoto S, Onuki J, Barbosa LF, Machado Garcia CC, Manso Prado F, Ronsein GE, Sigolo CA, Barbosa Brochini C, Gracioso Martins AM, Gennari de Medeirosa MH, Di Mascio P (2007) Oxidative stress in Perna perna and other bivalves as indicators of environmental stress in the Brazilian marine environment: antioxidants, lipid peroxidation and DNA damage. Comp Biochem Physiol A 146(4):588–600CrossRefGoogle Scholar
  10. Alyakrinskaya IO (2002) Physiological and biochemical adaptations to respiration of hemoglobin-containing hydrobionts. Biol Bull 29(3):268–283CrossRefGoogle Scholar
  11. Anderson G (1978) Metabolic rate, temperature acclimation and resistance to high temperature of soft-shell clams, Mya arenaria, as affected by shore level. Comp Biochem Physiol 61A:433–438CrossRefGoogle Scholar
  12. Antunes F, Boveris A, Cadenas E (2007) On the biologic role of the reaction of NO with oxidized cytochrome c oxidase. Antioxid Redox Signal 9(10):1569–1579PubMedCrossRefGoogle Scholar
  13. Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, pp 227–287Google Scholar
  14. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87:1620–1624PubMedCrossRefGoogle Scholar
  15. Beddig S, Brockmann U, Dannecker W, Körner D, Pohlmann T, Puls W, Radach G, Rebers A, Rickshort H-J, Schatzmann M, Schlünzen H, Schulz M (1997) Nitrogen fluxes in the German Bight. Mar Pollut Bull 34(6):382–394CrossRefGoogle Scholar
  16. Benjamin N, O’Driscoll F, Dougall H, Duncan C, Smith L, Golden M, McKenzie H (1994) Stomach NO synthesis. Nature 368:502PubMedCrossRefGoogle Scholar
  17. Bolaños JP, Heales SJR (2010) Persistent mitochondrial damage by nitric oxide and its derivatives: neuropathological implications. Front Neuroenerg 2:1–5Google Scholar
  18. Brand MD, Turner N, Ocloo A, Else PL, Hulbert AJ (2003) Proton conductance and fatty acyl composition of liver mitochondria correlates with body mass in birds. Biochem J 376:741–748PubMedCrossRefGoogle Scholar
  19. Breuer W, Epsztejn S, Cabantchik ZI (1995) Iron acquired from transferrin by K562 cells is delivered into a cytoplasmic pool of chelatable iron(II). J Biol Chem 270:24209–24215PubMedCrossRefGoogle Scholar
  20. Brousseau DJ (1978) Population dynamics of the soft-shell clam Mya arenaria. Mar Biol 50:63–71CrossRefGoogle Scholar
  21. Buettner GR, Jurkiewicz BA (1993) Ascorbate free radical as a marker of oxidative stress: an EPR study. Free Radic Biol Med 14:49–55PubMedCrossRefGoogle Scholar
  22. Buttemer WA, Abele D, Costantini D (2010) The ecology of antioxidants and oxidative stress in animals. From bivalves to birds: oxidative stress and longevity. Funct Ecol 24:971–983CrossRefGoogle Scholar
  23. Cadenas E, Davies KJ (2000) Mitochondrial free radical generation oxidative stress and aging. Free Radic Biol Med 29:222–230PubMedCrossRefGoogle Scholar
  24. Cairo G, Recalcati S, Pietrangelo A, Minotti G (2002) The iron regulatory proteins: targets and modulators of free radical reactions and oxidative damage. Free Radic Biol Med 32:1237–1243PubMedCrossRefGoogle Scholar
  25. Camus L, Birkely SR, Jones MB, Børseth JF, Grøsvike BE, Gulliksend B, Lønne OJ, Regoli F, Depledge MH (2003) Biomarker responses and PAH uptake in Mya truncata following exposure to oil-contaminated sediment in an Arctic fjord (Svalbard). Sci Total Environ 308(1–3):221–234PubMedCrossRefGoogle Scholar
  26. Castagna M, Chanley P (1973) Salinity tolerance of some marine bivalves from inshore and estuarine environments in Virginia waters on the western mid-Atlantic coast. Malacologia 12:47–96Google Scholar
  27. Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527–605PubMedGoogle Scholar
  28. Chang R (1999) Química. Sexta Edic. McGraw-Hill Interamericana, MéxicoGoogle Scholar
  29. Chapman VJ, Chapman DJ (1980) Sea vegetables (algae as food for man). In: Seaweeds and their uses, 3rd edn. Chapman and Hall, London, pp 62–97Google Scholar
  30. Chatterjee IB (1973a) Evolution and the biosynthesis of ascorbic acid. Science 182(118):1271–1272PubMedCrossRefGoogle Scholar
  31. Chatterjee IB (1973b) Vitamin C synthesis in animals: evolutionary trend. Sci Cult 39:210–212Google Scholar
  32. Czapski G, Goldstein S (1995) The role of the reactions of ·NO with superoxide and oxygen in biological systems: a kinetic approach. Free Radic Biol Med 19:785–794PubMedCrossRefGoogle Scholar
  33. de Beer D, Wenzhöfer F, Ferdelman TG, Boehme SE, Huettel M, van Beusekom JEE, Böttcher ME, Musat N, Dubilier N (2005) Transport and mineralization rates in North Sea sandy intertidal sediments, Sylt-Rømø Basin, Wadden Sea. Limnol Oceanogr 50(1):113–127CrossRefGoogle Scholar
  34. Estévez MS, Abele D, Puntarulo S (2002) Lipid radical generation in polar (Laternula elliptica) and temperate (Mya arenaria) bivalves. Comp Biochem Physiol B 132:729–737CrossRefGoogle Scholar
  35. Fowler BA, Wolte DA, Hettler WF (1975) Mercury and iron uptake by cytosomes in mantle epithelial cells of quahog clams (Mercenaria mercenaria) exposed to mercury. J Fish Res Bd Can 32:1767–1775CrossRefGoogle Scholar
  36. Funk F, Lenders JP, Crichton RR, Schneider W (1985) Reductive mobilization of ferritin iron. Eur J Biochem 152:167–172PubMedCrossRefGoogle Scholar
  37. Galatro A, Rousseau I, Puntarulo S (2006) Concentration analysis in steady state of ascorbate radical in soybean seedlings determined by electronic paramagnetic resonance. Phyton Intern J Exp Bot 75:7–20Google Scholar
  38. Galatro A, Rousseau I, Puntarulo S (2007) Ferritin role in iron toxicity in animals and plants. Res Trends Curr Topics Toxicol 4:65–76Google Scholar
  39. Galleano M, Aimo L, Borroni MV, Puntarulo S (2001) Nitric oxide and iron overload. Limitations of ESR detection by DETC. Toxicology 167:199–205PubMedCrossRefGoogle Scholar
  40. Galleano M, Aimo L, Puntarulo S (2002) Ascorbyl radical/ascorbate ratio in plasma from iron overloaded rats as oxidative stress indicator. Toxicol Lett 133:193–201PubMedCrossRefGoogle Scholar
  41. González PM, Abele D, Puntarulo S (2008) Iron and radical content in Mya arenaria. Possible sources of NO generation. Aquat Toxicol 89:122–128PubMedCrossRefGoogle Scholar
  42. González PM, Abele D, Puntarulo S (2010) Exposure to excess of iron in vivo affects oxidative status in the bivalve Mya arenaria. Comp Biochem Physiol C 152:167–174Google Scholar
  43. Graziano M, Lamattina L (2005) Nitric oxide and iron in plants: an emerging and converging story. Trends Plant Sci 10(1):4–8PubMedCrossRefGoogle Scholar
  44. Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL, Hediger MA (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388:482–488PubMedCrossRefGoogle Scholar
  45. Harrison PM, Arosio P (1996) The ferritins: molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta 1275:161–203PubMedCrossRefGoogle Scholar
  46. Horemans N, Asard H, Caubergs RJ (1994) The role of ascorbate free radical as an electron acceptor to cytochrome b-mediated trans-plasma membrane electron transport in higher plants. Plant Physiol 104:1455–1458PubMedGoogle Scholar
  47. Hubel CA, Kagan VE, Kosin ER, McLaughlin M, Roberts JM (1997) Increased ascorbate radical formation and ascorbate depletion in plasma from women with preeclampsia: implications for oxidative stress. Free Radic Biol Med 23:597–609PubMedCrossRefGoogle Scholar
  48. Huebers HA, Finch CA, Martin AW (1982) Characterization of an invertebrate transferring from the crab Cancer magister (Arthropoda). J Comp Physiol 148:101–109Google Scholar
  49. Huie RE, Padmaja S (1993) The reaction of NO with superoxide. Free Radic Res Commun 18(4):195–199PubMedCrossRefGoogle Scholar
  50. Jacklet JW (1997) Nitric oxide signaling in invertebrates. Invert Neurosci 3:1–14PubMedCrossRefGoogle Scholar
  51. Joseph JD (1982) Lipid composition of marine and estuarine invertebrates. Part II. Mollusca Prog Lipid Res 21:109–153CrossRefGoogle Scholar
  52. Kakhlon O, Cabantchik ZI (2002) The labile iron pool: characterization, measurement, and participation in cellular processes. Free Radic Biol Med 33:1037–1046PubMedCrossRefGoogle Scholar
  53. Keyer K, Imlay JA (1996) Superoxide accelerates DNA damage by elevating free-iron levels. Proc Natl Acad Sci USA 93:13635–13640PubMedCrossRefGoogle Scholar
  54. Knowles RG (1997) Nitric oxide biochemistry. Biochem Soc Trans 25:895–901PubMedGoogle Scholar
  55. Kruszewski M (2004) The role of labile iron pool in cardiovascular diseases. Acta Biochim Pol 51(2):471–480PubMedGoogle Scholar
  56. Lassig J (1965) The distribution of marine and brackishwater lamellibranchs in the northern Baltic area. Comment Biol 28:1–41Google Scholar
  57. Lesser MP (2006) Oxidative stress in marine environments. Biochem Physiol Ecol Annu Rev Physiol 68:253–278Google Scholar
  58. Lewis DE, Cerrato RM (1997) Growth uncoupling and the relationship between shell growth and metabolism in the soft shell clam Mya arenaria. Mar Ecol Prog Ser 158:177–189CrossRefGoogle Scholar
  59. Lizasoain I, Moro MA, Knowles RG, Darley-Usmar V, Moncada S (1996) Nitric oxide and peroxynitrite exert distinct effects on mitochondrial respiration which are differentially blocked by glutathione or glucose. Biochem J 314:887–898Google Scholar
  60. Mai K (1998) Comparative studies on the nutrition of two species of abalone, Haliotis tuberculata L. and Haliotis discus hannai Ino.: VII. Effects of dietary vitamin C on survival, growth and tissue concentration of ascorbic acid. Aquaculture 161(1–4):383–392CrossRefGoogle Scholar
  61. Martinez A (1995) Nitric oxide synthase in invertebrates. Histochem J 27:770–776PubMedGoogle Scholar
  62. Massabuau JC, Abele D (2012) Principles of oxygen uptake and tissue oxygenation in water-breathing animals. In: Abele D, Zenteno-Savin T, Vazquez-Medina J (eds) Oxidative stress in aquatic ecosystems. Blackwell Publishing Ltd, West SussexGoogle Scholar
  63. McKnight RC, Hunter FE Jr (1965) Effects of inorganic iron on the thiobarbituric acid method for determination of lipid peroxides. Biochim Biophys Acta 98:640–643CrossRefGoogle Scholar
  64. Moe YY, Koshioa S, Teshimaa S, Ishikawab M, Matsunagad Y, Panganiban A Jr (2004) Effect of vitamin C derivatives on the performance of larval kuruma shrimp, Marsupenaeus japonicas. Aquaculture 242:501–512CrossRefGoogle Scholar
  65. Moncada S, Bolaños JP (2006) Nitric oxide, cell bioenergetics and neurodegeneration. J Neurochem 97(6):1676–1689PubMedCrossRefGoogle Scholar
  66. Moncada S, Palmer RMJ, Higgs EA (1991) Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol Rev 43(2):109–142PubMedGoogle Scholar
  67. Moroz LL, Cheng D, Gillette MU, Gillette R (1996) Nitric oxide synthase activity in the molluscan CNS. J Neurochem 66:873–876PubMedCrossRefGoogle Scholar
  68. Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417:1–13PubMedCrossRefGoogle Scholar
  69. Newell CR, Hidu H (1986) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (North Atlantic)—softshell clam. US Fish Wildl Serv Biol Rep 82(11.53). US Army Corps of Engineers, TR EL-82-4Google Scholar
  70. Nilsson GE, Söderström V (1997) Comparative aspects on nitric oxide in brain and its role as a cerebral vasodilator. Comp Biochem Physiol A 118:949–958CrossRefGoogle Scholar
  71. Olsson C, Holmgren S (1997) Nitric oxide in the fish gut. Comp Biochem Physiol A 118(4):959–964CrossRefGoogle Scholar
  72. Petrat F, De Groot H, Sustmann R, Rauen U (2002) The chelatable iron pool in living cells: a methodically defined quantity. Biol Chem 383:489–502PubMedCrossRefGoogle Scholar
  73. Philipp EER, Lipinski S, Rast J, Rosenstiel P (2012) Immune defense of marine invertebrates: the role of reactive oxygen and nitrogen species. In: Abele D, Zenteno-Savin T, Vazquez-Medina J (eds) Oxidative stress in aquatic ecosystems. Blackwell Publishing Ltd, West SussexGoogle Scholar
  74. Pryor WA (1976) The role of free radical reactions in biological systems. In: Pryor WA (ed) Free radicals in biology. Academic Press, New York, pp 1–49Google Scholar
  75. Puls W, Heinrich H, Mayer B (1997) Suspended particulate matter budget for the German Bight. Mar Pollut Bull 34(6):398–409CrossRefGoogle Scholar
  76. Radach C, Lenhart HJ (1995) Nutrient dynamics in the North Sea: fluxes and budgets in the water column derived from ERSEM Neth. J Sea Rex 33:301–335CrossRefGoogle Scholar
  77. Randall D, Burggren W, French K (1997) Eckert animal physiology: mechanisms and adaptations, 4th edn. Freeman WH and Company, New YorkGoogle Scholar
  78. Regoli F, Nigro M, Bompadre S, Winston GW (2000) Total oxidant scavenging capacity (TOSC) of microsomal and cytosolic fractions from Antarctic, Arctic and Mediterranean scallops: differentiation between three potent oxidants. Aquat Toxicol 49:13–25PubMedCrossRefGoogle Scholar
  79. Robbins RA, Grisham MB (1997) Nitric oxide. Int J Biochem Cell Biol 29:857–860PubMedCrossRefGoogle Scholar
  80. Schneppensieper T, Finkler S, Czap A, van Eldik R, Heus M, Nieuwenhuizen P, Wreesmann C, Abma W (2001) Tuning the reversible binding of NO to iron(II) aminocarboxylate and related complexes in aqueous solution. Eur J Inorg Chem 2:491–501CrossRefGoogle Scholar
  81. Schreiber F (2009) Detecting and understanding nitric oxide formation during nitrogen cycling in microbial biofilms. In: International Max-Planck Research School for Marine Microbiology (IMPRS MarMic), University of Bremen, BremenGoogle Scholar
  82. Smirnoff N (2000) Ascorbic acid: metabolism and functions of a multi-facetted molecule. Curr Opin Plant Biol 3:229–235PubMedGoogle Scholar
  83. Srinivasa C, Liba A, Imlay JA, Valentine JS, Gralla FB (2000) Yeast lacking superoxide dismutase(s) show elevated levels of “free iron” as measured by whole cell electron paramagnetic resonance. J Biol Chem 275(38):29187–29192CrossRefGoogle Scholar
  84. St-Pierre J, Buckingham JA, Roebuck SJ, Brand MD (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 277(22):44784–44790PubMedCrossRefGoogle Scholar
  85. Taha Z, Kiechle F, Malinski T (1992) Oxidation of nitric oxide by oxygen in biological systems monitored by porphyrinic sensor. Biochem Biophys Res Commun 188:734–739PubMedCrossRefGoogle Scholar
  86. Tarpey MM, Wink DA, Grisham MB (2004) Methods for detection of reactive metabolites of oxygen and nitrogen: in vitro and in vivo considerations. Am J Physiol Regul Integr Comp Physiol 286:R431–R444PubMedCrossRefGoogle Scholar
  87. Terwilliger NB (1998) Functional adaptations of oxygen-transport proteins. J Exp Biol 201:1085–1098PubMedGoogle Scholar
  88. Terwilliger NB, Terwilliger RC, Meyhöfer E, Morse MP (1988) Bivalve hemocyanins—a comparison with other molluscan hemocyanins. Comp Biochem Physiol B 89:189–195PubMedCrossRefGoogle Scholar
  89. Vanin AF, Serezhenkov VA, Mikoyan VD, Genkin MV (1998) The 2.03 signal as an indicator of dinitrosyl-iron complexes with thiol-containing ligands. Nitric Oxide 2(4):224–234PubMedCrossRefGoogle Scholar
  90. Vanin AF, Papina AA, Serezhenkov VA, Koppenol WH (2004) The mechanisms of S-nitrosothiol decomposition catalyzed by iron. Nitric Oxide 10:60–73PubMedCrossRefGoogle Scholar
  91. Viarengo A, Canesi L, Garcia Martinez P, Peters LD, Livingstone DR (1995) Pro-oxidant processes and antioxidant defence systems in the tissues of the Antarctic scallop (Adamussium colbecki) compared with the Mediterranean scallop (Pecten jacobeus). Comp Biochem Physiol B 111:119–126CrossRefGoogle Scholar
  92. Viarengo A, Burlando B, Cavaletto M, Marchi B, Ponzano E, Blasco J (1999) Role of metallothionein against oxidative stress in the mussel Mytilus galloprovincialis. Am J Physiol Regul Integr Comp Physiol 277:1612–1619Google Scholar
  93. Walling C (1957) Free radicals in solution. In: Wiley, New York, p 631Google Scholar
  94. Wang J, Pantopoulos K (2011) Regulation of cellular iron metabolism. Biochem J 434:365–381PubMedCrossRefGoogle Scholar
  95. Williams RJ (1982) Free manganese (II) and iron (II) cations can act as intracellular cell controls. FEBS Lett 140(1):3–10PubMedCrossRefGoogle Scholar
  96. Winston GW, Moore MN, Kirchin MA, Soverchia C (1996) Production of reactive oxygen species by hemocytes from the marine mussel, Mytilus edulis: lysosomal localization and effect of xenobiotics. Comp Biochem Physiol C 113(2):221–229PubMedGoogle Scholar
  97. Winzerling JJ, Law JH (1997) Comparative nutrition of iron and copper. Annu Rev Nutr 17:501–526PubMedCrossRefGoogle Scholar
  98. Woodmansee AN, Imlay JA (2002) Quantification of intracellular free iron by electron paramagnetic resonance spectroscopy. Methods Enzymol 349:3–9PubMedCrossRefGoogle Scholar
  99. Zweier JL, Samouilov A, Kuppusamy P (1999) Non-enzymatic nitric oxide synthesis in biological systems. Biochim Biophys Acta Bioenerg 1411(2–3):250–262CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Paula Mariela González
    • 1
  • Doris Abele
    • 2
  • Susana Puntarulo
    • 1
    • 3
    Email author
  1. 1.Physical Chemistry-PRALIB, School of Pharmacy and BiochemistryUniversity of Buenos AiresBuenos AiresArgentina
  2. 2.Alfred Wegener Institute for Polar and Marine Research, Functional EcologyBremerhavenGermany
  3. 3.Fisicoquímica-PRALIB, Facultad de Farmacia y BioquímicaBuenos AiresArgentina

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