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Effects of hypoxia and reoxygenation on the antioxidant defense system of the locomotor muscle of the crab Neohelice granulata (Decapoda, Varunidae)

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Abstract

Crustaceans often occur in areas with variations in oxygen and experience situations known as hypoxia and reoxygenation. Consequences of such situations are increased levels of reactive oxygen species. To avoid oxidative damage intertidal crabs appear to possess an efficient antioxidant defense system (ADS). However, to date, studies have not addressed the strategies that are adopted by the crabs when exposed to hypoxia/reoxygenation cycles. Towards this end we evaluated the ADS and the role of melatonin as an antioxidant in the locomotor muscle of the crab Neohelice granulata under conditions of severe hypoxia and reoxygenation. Total antioxidant capacity against peroxyl radicals and the enzymes superoxide dismutase, catalase, glutathione peroxidase (GPx), and glutathione-S-transferase as well as the key enzyme of glutathione synthesis, glutamate cysteine ligase (GCL), were evaluated. Furthermore, GSH, GSH/GSSG index as well as hemolymph and cellular melatonin levels were evaluated. During hypoxia, increased GPx and GCL activity and decreased GSH and mitochondrial melatonin levels were observed, but during reoxygenation catalase activity increased and cytosolic melatonin levels decreased. It appears that the ADS in the locomotor muscle of N. granulata exert a modulating effect when being confronted with hypoxia and reoxygenation to avoid oxidative stress. During hypoxia, the ADS appear to target GPX activity as well as GSH and mitochondrial melatonin. During reoxygenation, however, evidence suggests that catalase and cytosolic melatonin are involved in the recovery of the locomotor muscle from oxidative damage and the suppression of further damage.

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References

  • Abele D, Puntarulo S (2004) Formation of reactive species and induction of antioxidant defense systems in polar and temperate marine invertebrates and fish. Comp Biochem Physiol A 138:405–415

    Article  Google Scholar 

  • Acuna-Castroviejo D, Escames G, Len J, Carazo A, Khaldy H (2003) Mitochondrial regulation by melatonin and its metabolites. Adv Exp Med Biol 527:549–557

    Article  CAS  PubMed  Google Scholar 

  • Agapito MT, Herrero B, Pablos MI, Miguel JL, Recio JM (1995) Circadian rhythms of melatonin and serotonin-N-acetyltransferase activity in Procambarus clarkii. Comp Biochem Physiol A 112:179–185

    Article  Google Scholar 

  • Akerboon TP, Sies H (1981) Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples. Methods Enzymol 77:373–382

    Article  Google Scholar 

  • Amado LL, Garcia ML, Ramos PB, Freitas RF, Zafalon B, Ferreira JLR, Yunes JS, Monserrat JM (2009) A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: application to evaluate microcystins toxicity. Sci Total Environ 407:2115–2123

    Article  CAS  PubMed  Google Scholar 

  • Anisimov VN (2003) Effects of exogenous melatonin—a review. Toxicol Pathol 31:589–603

    CAS  PubMed  Google Scholar 

  • Arthur JR (2000) The glutathione peroxidases. Cell Mol Life Sci 57:1825–1835

    Article  CAS  PubMed  Google Scholar 

  • Arun S, Subramanian P (1998) Antioxidant enzymes activity in subcellular fraction of freshwater prawns Macrobrachium malcolmsonii and Macrobrachium lamarrei. Appl Biochem Biotechnol 75:187–192

    Article  CAS  Google Scholar 

  • Balzer I, Espínola IR, Fuentes-Pardo B (1997) Daily variations of immunoreactive melatonin in the visual system of crayfish. Biol Cell 89:539–543

    Article  CAS  Google Scholar 

  • Beutler E (1975) The preparation of red cells for assay. In: Beutler E (ed) Red cell metabolism: a manual of biochemical methods. Grune and Stratton, New York, pp 8–18

    Google Scholar 

  • Bickler PE, Buck LT (2007) Hypoxia tolerance in reptiles amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol 69:145–170

    Article  CAS  PubMed  Google Scholar 

  • Burggren WW, McMahon BR (1983) An analysis of scaphognathite pumping in the crayfish Orconectes virilis: compensatory changes to acute and chronic hypoxia. Physiol Zool 56:309–318

    Article  Google Scholar 

  • Cho CS, Lee S, Woo HA, Choi EJ, Rhee SG (2010) Irreversible inactivation of glutathione peroxidase 1 and reversible inactivation of peroxiredoxin II by H2O2 in red blood cells. Antioxid Redox Signal 12:1235–1246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clanton TL (2007) Hypoxia-induced reactive oxygen species formation in skeletal muscle. J Appl Physiol 102:2379–2388

    Article  CAS  PubMed  Google Scholar 

  • Dawson NJ, Katzenback BA, Storey KB (2015) Free-radical first responders: the characterization of CuZnSOD and MnSOD regulation during freezing of the freeze-tolerant North American wood frog. Rana sylvatica. Biochim Biophys Acta 1850:97–106

    Article  CAS  PubMed  Google Scholar 

  • de Oliveira UO, da Rosa Araujo AS, Belló-Klein A, da Silva RS, Kucharski LC (2005) Effects of environmental anoxia and different periods of reoxygenation on oxidative balance in gills of the estuarine crab Chasmagnathus granulata. Comp Biochem Physiol B 140:51–57

    Article  PubMed  Google Scholar 

  • Dupont-Prinet A, Pillet M, Chabot D, Hansen T, Tremblay R, Audet C (2013) Northern shrimp (Pandalus borealis) oxygen consumption and metabolic enzyme activities are severely constrained by hypoxia in the Estuary and Gulf of St. Lawrence. J Exp Mar Biol Ecol 448:298–307

    Article  CAS  Google Scholar 

  • Escobar JA, Rubio MA, Lissi EA (1996) SOD and catalase inactivation by singlet oxygen and peroxyl radical. Free Radic Biol Med 20:285–290

    Article  CAS  PubMed  Google Scholar 

  • Ferreira-Cravo M, Piedras FR, Moraes TM, Ferreira JLB, de Freitas DPS, Machado MD, Geracitano LA, Monserrat JM (2007) Antioxidant responses and reactive oxygen species induced in different body regions of the estuarine polychaeta Laeonereis acuta (Nereididae). Chemosphere 66:1367–1374

    Article  CAS  PubMed  Google Scholar 

  • Fridovich I (2004) Mitochondria: are they the seat of senescence? Aging Cell 3:13–16

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Tríana A, Zenteno-savín T, Peregrino-Uriarte AB, Yepiz-Plascencia G (2010) Hypoxia, reoxygenation and cytosolic manganese superoxide dismutase (cMnSOD) silencing in Litopenaeus vannamei: effects on cMnSOD transcripts, superoxide dismutase activity and superoxide anion production capacity. Dev Comp Immunol 34:1230–1235

    Article  PubMed  Google Scholar 

  • Gebicki JM, Nauser T, Domazou A, Steinmann D, Pounds PL, Koppenol WH (2010) Reduction of protein radicals by GSH and ascorbate: potential biological significance. Amino Acids 39:1131–1137

    Article  CAS  PubMed  Google Scholar 

  • Geihs MA, Vargas MA, Maciel FE, Caldas SS, Cruz BP, Primel EG, Monserrat JM, Nery LEM (2009) Effect of melatonin in the antioxidant defense system in the locomotor muscles of the estuarine crab Neohelice granulata (Decapoda, Brachyura). Gen Comp Endocr 166:72–82

    Article  PubMed  Google Scholar 

  • Geihs MA, Maciel FE, Vargas MA, Cruz BP, Nery LEM (2013) Effects of hypoxia and reoxygenation on the energetic metabolism of the crab Neohelice granulata (Decapoda, Varunidae). J Exp Mar Biol Ecol 445:69–78

    Article  Google Scholar 

  • Geihs MA, Vargas MA, Nery LEM (2014) Damages caused during hypoxia and reoxygenation in the locomotor muscle of the crab Neohelice granulata (Decapoda Varunidae). Comp Biochem Physiol A 172:1–9

    Article  CAS  Google Scholar 

  • Gorr TA, Wichmann D, Hu J, Hermes-Lima M, Welker AF, Terwilliger N, Wren JF, Viney M, Morris S, Nilsson GE, Deten A, Soliz J, Gassmann M (2010) Hypoxia tolerance in animals: biology and application. Physiol Biochem Zool 83:733–752

    Article  CAS  PubMed  Google Scholar 

  • Guerriero G, Di Finizio A, Ciarcia G (2002) Stress-induced changes of plasma antioxidants in aquaculture sea bass, Dicentrarchus labrax. Comp Biochem Physiol A 132:205–211

    Article  Google Scholar 

  • Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione S-transferases. Methods Enzymol 77:398–405

    Article  CAS  PubMed  Google Scholar 

  • Halestrap AP, Pasdois PP (2009) The role of the mitochondrial permeability transition pore in heart disease. Biochim Biophys Acta Bioenerg 1787:1402–1415

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JM (2001) Free radicals in biology and medicine, 3rd edn. Oxford, New York

    Google Scholar 

  • Hardeland R (2008) Melatonin, hormone of darkness and more—occurrence, control mechanisms, actions and bioactive metabolites. Cell Mol Life Sci 65:2001–2018

    Article  CAS  PubMed  Google Scholar 

  • Hardeland R, Poeggeler B (2003) Non-vertebrate melatonin. J Pineal Res 34:233–241

    Article  CAS  PubMed  Google Scholar 

  • Hermes-Lima M, Zenteno-Savín T (2002) Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comp Biochem Physiol C 133:537–556

    Article  Google Scholar 

  • Hermes-Lima M, Storey JM, Storey KB (2001) Antioxidant defenses and animal adaptation to oxygen availability during environmental stress. Protein adaptations and signal transduction. In: Storey KB, Storey JM (eds) Cell and mol. resp. to stress, vol 2. Elsevier, Amsterdam, pp 263–287

    Google Scholar 

  • Hermes-Lima M, Moreira DC, Rivera-Ingraham G, Giraud-Billoud M, Genaro-Mattos TC, Campos ÉG (2015) Preparation for oxidative stress under hypoxia and metabolic depression: revisiting the proposal two decades later Free Radic Biol Med 89:1122–1143

    CAS  PubMed  Google Scholar 

  • Herried CFL (1980) Hypoxia in invertebrates. Comp Biochem Physiol A 67:311–320

    Article  Google Scholar 

  • Hervant F, Mathieu J, Garin D, Freminet A (1995) Behavioral, ventilatory, and metabolic responses to severe hypoxia and subsequent recovery of the hypogean Niphargus rhenorhodanensis and epigean Gammarus fossarum (Crustacea, Amphipoda). Physiol Zool 68:223–244

    Article  Google Scholar 

  • Hill AD, Taylor AC, Strang RHC (1991) Physiological and metabolic responses of the shore crab Carcinus maenas (L.) during environmental anoxia and subsequent recovery. J Exp Mar Biol Ecol 150:31–50

    Article  CAS  Google Scholar 

  • Kaplovitz N, Tak YA, Ookhtens M (1985) The regulation of hepatic glutathione. Annu Rev Pharmacol Toxicol 25:715–744

    Article  Google Scholar 

  • Kim SC, Sprung R, Chen Y, Xu Y, Ball H, Pei J, Cheng T, Kho Y, Xiao H, Xiao L et al (2006) Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol Cell 23:607–618

    Article  CAS  PubMed  Google Scholar 

  • Lardone PJ, Alvarez-Garcia O, Varrillo-Vico A, Vega-Naredo I, Caballero B, Guerrero JM, Coto-Montes A (2006) A Inverse correlation between endogenous melatonin levels and oxidative damage in some tissues of SAM P8 mice. J Pineal Res 40:153–157

    Article  CAS  PubMed  Google Scholar 

  • Lawniczak M, Romestaing C, Roussel D, Maazouzi C, Renault D, Hervant F (2013) Preventive antioxidant responses to extreme oxygen level fluctuation in a subterranean crustacean. Comp Biochem Physiol A 165:299–303

    Article  CAS  Google Scholar 

  • Lesser MP (2006) Oxidative stress in marine environments. Biochem Physiol Ecol Ann Rev Physiol 68:253–278

    Article  CAS  Google Scholar 

  • Li CY, Jackson R (2002) Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol Cell Physiol 282:C227–C241

    Article  CAS  PubMed  Google Scholar 

  • Lushchak VI (2014) Classification of oxidative stress based of its intensity. EXCLI J 13:922–937

    PubMed  PubMed Central  Google Scholar 

  • Lushchak VI, Bagnyukova TV (2007) Hypoxia induces oxidative stress in tissues of a goby, the rotan Perccottus glenii. Comp Biochem Physiol B 148:390–397

    Article  PubMed  Google Scholar 

  • Lushchak VI, Lushchak LP, Mota AA, Hermes-Lima M (2001) Oxidative stress and antioxidant defenses in goldfish Carassius auratus during anoxia and reoxygenation. Am J Physiol 280:R100–R107

    CAS  Google Scholar 

  • Maciel FE, Geihs MA, Vargas MA, Cruz BP, Vakkuri O, Meyer-Rochow VB, Nery LEM, Allodi S (2008a) Daily variation of melatonin content in the optic lobes of the crab Neohelice granulata. Comp Biochem Physiol A 149:162–166

    Article  Google Scholar 

  • Maciel JES, Souza F, Valle S, Kucharski LC, da Silva RSM (2008b) Lactate metabolism in the muscle of the crab Chasmagnathus granulatus during hypoxia and post-hypoxia recovery. Comp Biochem Physiol 151:61–65

    Article  Google Scholar 

  • Manevich Y, Feinstein SI, Fisher AB (2004) Activation of the antioxidant enzyme 1-CYS peroxiredoxin requires glutathionylation mediated by heterodimerization with πGST. Proc Natl Acad Sci USA 101:3780–3785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martín MM, Macías G, Escames RJ, Reiter MT, Agapito GG, Acuna-Castroviejo D (2000) Melatonin-induced increased activity of the respiratory chain complexes I and IV can prevent mitochondrial damage induced by ruthenium red in vivo. J Pineal Res 28:242–248

    Article  PubMed  Google Scholar 

  • Martínez-álvarez RM, Morales AE, Sanz A (2005) Antioxidant defenses in fish: biotic and abiotic factors. Rev Fish Biol Fisher 15:75–88

    Article  Google Scholar 

  • Mayo JC, Sainz RM, Antolin I, Herrera F, Martin V, Rodriguez C (2002) Melatonin regulation of antioxidant enzyme expression. Cell Mol Life Sci 59:1706–1713

    Article  CAS  PubMed  Google Scholar 

  • McCord JM, Fridovich I (1969) Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055

    CAS  PubMed  Google Scholar 

  • Meyer-Rochow VB (2001) The crustacean eye: dark/light adaptation, polarization sensitivity, flicker fusion frequency, and photoreceptor damage. Zool Sci 18:1175–1197

    Article  CAS  PubMed  Google Scholar 

  • Pablos MI, Agapito MT, Gutierrez R (1995) Melatonin stimulates the activity of the detoxifying enzyme glutathione peroxidase in several tissues of chicks. J Pineal Res 19:111–115

    Article  CAS  PubMed  Google Scholar 

  • Pannunzio TM, Storey KB (1998) Antioxidant defenses and lipid peroxidation during anoxia stress and aerobic recovery in the marine gastropod Littorina littorea. J Exp Mar Biol Ecol 221:277–292

    Article  CAS  Google Scholar 

  • Pape C, Teschke M, Meyer B (2008) Melatonin and its possible role in mediating seasonal metabolic changes of Antarctic krill, Euphausia superba. Comp Biochem Physiol A 149:426–434

    Article  Google Scholar 

  • Parrilla-Taylor DP, Zenteno-Savín T (2011) Antioxidant enzyme activities in Pacific white shrimp (Litopenaeus vannamei) in response to environmental hypoxia and reoxygenation. Aquaculture 318:379–383

    Article  CAS  Google Scholar 

  • Paschke K, Cumillaf JP, Loyola S, Gebauer P, Urbina M, Chimal ME, Pascual C, Rosas C (2010) Effect of dissolved oxygen level on respiratory metabolism, nutritional physiology, and immune condition of southern king crab Lithodes santolla (Molina, 1782) (Decapoda, Lithodidae). Mar Biol 157:7–18

    Article  CAS  Google Scholar 

  • Reiter RJ (1996) Functional aspects of the pineal hormone melatonin in combating cell and tissue damage induced by free radicals. Eur J Endocr 134:412–420

    Article  CAS  Google Scholar 

  • Reiter RJ, Tan DX, Burkhardt S (2002) Reactive oxygen and nitrogen species and cellular and organismal decline: amelioration with melatonin. Mech Ageing Dev 123:1007–1019

    Article  CAS  PubMed  Google Scholar 

  • Richman PG, Meister A (1975) Regulation of Gamma glutamyl cysteine sintethase by nonallosteric feedback inhibition of glutathione. J Biol Chem 250:1422–1426

    CAS  PubMed  Google Scholar 

  • Russel WMS, Burch ML (1959) The principles of human experimental technique. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Sainath SB, Swetha CH, Reddy PS (2013) What do we need to know about melatonin in crustaceans? J Exp Zool A 319:365–377

    Article  CAS  Google Scholar 

  • Sies H (2014) Role of metabolic H2O2 generation: redox signalling and oxidative stress. J Biol Chem 289:8735–8741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith KJ, Able KW (2003) Dissolved oxygen dynamics in salt marsh pools and its potential impacts on fish assemblages. Mar Ecol Prog Ser 258:223–232

    Article  CAS  Google Scholar 

  • Tamarkin L, Baird CJ, Almeida OF (1985) Melatonin: a coordinating signal for mammalian reproduction? Science 227:714–720

    Article  CAS  PubMed  Google Scholar 

  • Tan DX, Manchester LC, Reiter RJ, Plummer BF, Hardies LJ, Weintraub ST, Vijayalaxmi Shepherd AMM (1998) A novel melatonin metabolite, cyclic 3-hydroxymelatonin: a biomarker of in vivo hydroxyl radical induced. Biochem Biophys Res Commun 253:614–620

    Article  CAS  PubMed  Google Scholar 

  • Tan DX, Manchester LC, Reiter RJ, Plummer BF, Limson J, Weintraub ST, Qi W (2000) Melatonin directly scavenges hydrogen peroxide: a potentially new metabolic pathway of melatonin biotransformation. Free Radic Biol Med 29:1177–1185

    Article  CAS  PubMed  Google Scholar 

  • Tilden AR, Rasmussen P, Awantang RM, Furlan S, Goldstein J, Palsgrove M, Sauer A (1997) Melatonin cycle in the fiddler crab Uca pugilator and influence of melatonin on limb reinduced. J Pineal Res 23:142–147

    Article  CAS  PubMed  Google Scholar 

  • Vakkuri O, Leppaluoto J, Vuolteenaho O (1984) Development and validation of a melatonin radioimmunoassay using radioiodinated melatonin as tracer. Acta Endocrinol 106:152–157

    CAS  PubMed  Google Scholar 

  • Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. PNAS 105:15452–15457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vargas MA, Geihs MA, Maciel FE, Cruz BP, Nery LEM, Allodi S (2011) The effects of UV radiation on the visual system of the crab Neohelice granulata: a protective role of melatonin. Comp Biochem Physiol C 154:427–434

    CAS  Google Scholar 

  • Vivien-Roels B, Pevet P (1986) Is melatonin an evolutionary conservative molecule involved in the transduction of photoperiodic information in all living organism? Adv Pineal Res 1:61–68

    CAS  Google Scholar 

  • Welker AF, Moreira DC, Campos EG, Hermes-Lima M (2013) Role of redox metabolism for adaptation of aquatic animals to drastic changes in oxygen availability. Comp Biochem Physiol A 165:384–404

    Article  CAS  Google Scholar 

  • White CC, Viernes H, Krejsa CM, Botta D, Kavanagh TJ (2003) Fluorescence-based microtiter plate assay for glutamate-cysteine ligase activity. Anal Biochem 318:175–180

    Article  CAS  PubMed  Google Scholar 

  • Withyachumnarnkul B, Buppaniroj K, Pongsa-Asawapaiboon A (1992) N-acetyltransferase and melatonin levels in the optic lobe of giant freshwaters prawns, Macrobrachium rosenbergii de Man. Comp Biochem Physiol A 102:703–707

    Article  Google Scholar 

  • Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice-Hall, Englewood Cliffs

    Google Scholar 

  • Zenteno-Savín T, Saldierna R, Ahuejote-Sandoval M (2006) Superoxide radical production in response to environmental hypoxia in cultured shrimp. Comp Biochem Physiol C 142:301–308

    Google Scholar 

Download references

Acknowledgments

The Brazilian agencies: Conselho Nacional de Pesquisa (CNPq), Coordenação de Pessoal de Nível Superior (CAPES) and Fundação de Pesquisa do Estado do Rio Grande do Sul (FAPERGS) supported this project. M. A. Geihs is a CAPES fellow.

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Authors and Affiliations

  1. Programa de Pós-Graduação em Ciências Fisiológicas, Fisiologia Animal Comparada, Instituto de Ciências Biológicas, Universidade Federal do Rio Grande, FURG, Av. Itália, Km 8, Rio Grande, RS, CEP 96203-900, Brazil

    Márcio Alberto Geihs, Marcelo Alves Vargas, Fábio Everton Maciel & Luiz Eduardo Maia Nery

  2. Department of Physiology, Oulu University, P.O. Box 3000, 50014, Oulu, Finland

    Olli Vakkuri

  3. Department of Biology, Oulu University, P.O. Box 3000, 50014, Oulu, Finland

    Victor Benno Meyer-Rochow

  4. Research Institute of Luminescent Organisms, Tokyo, Hachijojima, 100-1623, Japan

    Victor Benno Meyer-Rochow

  5. Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, UFRJ, Av. Carlos Chagas Filho 373 CCS, Bloco G2-001, Ilha do Fundão, Rio de Janeiro, RJ, 21449-902, Brazil

    Silvana Allodi

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  1. Márcio Alberto Geihs
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Geihs, M.A., Vargas, M.A., Maciel, F.E. et al. Effects of hypoxia and reoxygenation on the antioxidant defense system of the locomotor muscle of the crab Neohelice granulata (Decapoda, Varunidae). J Comp Physiol B 186, 569–579 (2016). https://doi.org/10.1007/s00360-016-0976-2

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