Molecular and cellular response to short-term oxygen variations in the Pacific oyster Crassostrea gigas

Journal of Experimental Marine Biology and Ecology

Volumn 412, Issue , 2012, Pages 87-95

  Sussarellu, Rossana ^a   Fabioux, Caroline ^a   Camacho Sanchez, Miguel ^a   Le Goïc, Nelly ^a   Lambert, Christophe ^a   Soudant, Philippe ^a   Moraga, Dario ^a  

^a UNIVERSITÉ DE BRETAGNE OCCIDENTALE   (France)

Author keywords

Gene expression; Hemocytes; Hypoxia; Oxidative stress; Oyster; Re oxygenation

Indexed keywords

ANTIOXIDANT; BIVALVE; ENZYME ACTIVITY; GENE EXPRESSION; INTERTIDAL COMMUNITY; INTERTIDAL ENVIRONMENT; METABOLISM; MOLECULAR ANALYSIS; OXIC CONDITIONS; OXYGEN; PHYSIOLOGICAL RESPONSE;

CRASSOSTREA GIGAS; MOLLUSCA; OSTREIDAE;

EID: 84155160715     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2011.11.007     Document Type: Article

References (56)

1. Abele D., Puntarulo S. Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2004, 138:405-415.
2. Adema C., Vanderknaap W., Sminia T. Molluscan hemocyte-mediated cytotoxicity - the role of reactive oxygen intermediates. Dev. Comp. Immunol. 1991, 4:201-223.
3. Almeida E.A., Bainy A.C.D., Dafre A.L., Gomes O.F., Medeiros M.H.G., Di Mascio P. Oxidative stress in digestive gland and gill of the brown mussel (Perna perna) exposed to air and re-submersed. J. Exp. Mar. Biol. Ecol. 2005, 318:21-30.
4. Anderson R. Interactions of Perkinsus marinus with humoral factors and hemocytes of Crassostrea virginica. J. Shellfish Res. 1996, 15:127-134.
5. Bartosz G. Reactive oxygen species: destroyers or messengers?. Biochem. Pharmacol. 2009, 77:1303-1315.
6. Boveris A., Chance B. The mitochondrial generation of hydrogen peroxide, general properties and effect of hyperbaric oxygen. Biochem. J. 1973, 134:707-716.
7. Boyd J., Burnett L. Reactive oxygen intermediate production by oyster hemocytes exposed to hypoxia. J. Exp. Biol. 1999, 202:3135-3143.
8. Bridges C.R., Taylor A.C., Morris S.J., Grieshaber M.K. Ecophysiological adaptations in Blennius pholis (L.) blood to intertidal rockpool environments. J. Exp. Mar. Biol. Ecol. 1984, 77:151-167.
9. Buttemer W.A., Abele D., Costantini D. From bivalves to birds: oxidative stress and longevity. Funct. Ecol. 2010, 24:971-983.
10. Cloern J.E. Our evolving conceptual model of the coastal eutrophication problem. Mar. Ecol. Prog. Ser. 2001, 210:223-253.
11. Conners D.E., Ringwood A.H. Effects of glutathione depletion on copper cytotoxicity in oysters (Crassostrea virginica). Aquat. Toxicol. 2000, 50:341-349.
12. David E., Tanguy A., Pichavant K., Moraga D. Response of the Pacific oyster Crassostrea gigas to hypoxia exposure under experimental conditions. FEBS J. 2005, 272:5635-5652.
13. Donaghy L., Lambert C., Choi K.-S., Soudant P. Hemocytes of the carpet shell clam (Ruditapes decussatus) and the Manila clam (Ruditapes philippinarum): current knowledge and future prospects. Aquaculture 2009, 297:10-24.
14. Fabioux C., Huvet A., Lelong C., Robert R., Pouvreau S., Daniel J.Y., Minguant C., Le Pennec M. Oyster vasa-like gene as a marker of the germline cell development in Crassostrea gigas. Biochem. Biophys. Res. Commun. 2004, 320:592-598.
15. Fried W., Johnson C., Heller P. Observations on regulation of erythropoiesis during prolonged periods of hypoxia. Blood 1970, 36:607-616.
16. Gorr T.A., Gassmann M., Wappner P. Sensing and responding to hypoxia via HIF in model invertebrates. J. Insect Physiol. 2006, 52:349-364.
17. Gray J.S., Wu R.S., Or Y.Y. Effects of hypoxia and organic enrichment on the coastal marine environment. Mar. Ecol. Prog. Ser. 2002, 238:249-279.
18. Greco L., Pellerin J., Capri E., Garnerot F., Louis S., Fournier M., Sacchi A., Fusi M., Lapointe D., Couture P. Physiological effects of temperature and a herbicide mixture on the soft-shell clam Mya arenaria (Mollusca, Bivalvia). Env. Toxicol. Chem. 2011, 30:132-141.
19. Greenway S.C., Storey K.B. The effect of prolonged anoxia on enzyme activities in oysters (Crassostrea virginica) at different seasons. J. Exp. Mar. Biol. Ecol. 1999, 242:259-272.
20. Grieshaber M.K., Hardewig I., Kreutzer U., Pörtner H.O. Physiological and metabolic responses to hypoxia in invertebrates. Reviews of Physiology, Biochemistry and Pharmacology 1994, 125:43-147. Springer Berlin Heidelberg.
21. Hellemans J., Mortier G., De Paepe A., Speleman F., Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 2007, 8:R19.
22. Hermes-Lima M. Oxygen in biology and biochemistry. Role of Free Radicals 2004, 319-368. K.B. Storey (Ed.).
23. Ivanina A.V., Sokolov E.P., Sokolova I.M. Effects of cadmium on anaerobic energy metabolism and mRNA expression during air exposure and recovery of an intertidal mollusk Crassostrea virginica. Aquat. Toxicol. 2010, 99:330-342.
24. Joyner-Matos J., Downs C.A., Julian D. Increased expression of stress proteins in the surf clam Donax variabilis following hydrogen sulfide exposure. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2006, 145:245-257.
25. Lambert C., Soudant P., Choquet G., Paillard C. Measurement of Crassostrea gigas hemocyte oxidative metabolism by flow cytometry and the inhibiting capacity of pathogenic vibrios. Fish Shellfish Immunol. 2003, 15:225-240.
26. Larade K., Storey K.B. Chapter 3 A profile of the metabolic responses to anoxia in marine invertebrates. Sensing, Signaling and Cell Adaptation 2002, 27-46. Elsevier.
27. Le Moullac G., Bacca H., Huvet A., Moal J., Pouvreau S., Van Wormhoudt A. Transcriptional regulation of pyruvate kinase and phosphoenolpyruvate carboxykinase in the adductor muscle of the oyster Crassostrea gigas during prolonged hypoxia. J. Exp. Zool. A Ecol. Genet. Physiol. 2007, 307A:371-382.
28. Li T., Brouwer M. Hypoxia-inducible factor, gsHIF, of the grass shrimp Palaemonetes pugio: molecular characterization and response to hypoxia. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2007, 147:11-19.
29. Marigómez I., Soto M., Cajaraville M.P., Angulo E., Giamberini L. Cellular and subcellular distribution of metals in molluscs. Microsc. Res. Tech. 2002, 56:358-392.
30. Massabuau J.-C. From low arterial- to low tissue-oxygenation strategy. An evolutionary theory. Respir. Physiol. 2001, 128:249-261.
31. McDonald A.E., Vanlerberghe G.C. Branched mitochondrial electron transport in the Animalia: presence of alternative oxidase in several animal phyla. IUBMB Life 2004, 56:333-341.
32. McDonald A.E., Vanlerberghe G.C., Staples J.F. Alternative oxidase in animals: unique characteristics and taxonomic distribution. J. Exp. Biol. 2009, 212:2627-2634.
33. McMahon R.F. Respiratory response to periodic emergence in intertidal molluscs. Am. Zool. 1988, 28:97-114.
34. Michaelidis B., Haas D., Grieshaber M.K. Extracellular and intracellular acid-base status with regard to the energy metabolism in the oyster Crassostrea gigas during exposure to air. Physiol. Biochem. Zool. 2005, 78:373-383.
35. Pannunzio T.M., Storey K.B. Antioxidant defenses and lipid peroxidation during anoxia stress and aerobic recovery in the marine gastropod Littorina littorea. J. Exp. Mar. Biol. Ecol. 1998, 221:277-292.
36. Pichavant K., Person-Le-Ruyet J., Le Bayon N., Sévère A., Le Roux A., Quéméner L., Maxime V., Nonnotte G., Boeuf G. Effects of hypoxia on growth and metabolism of juvenile turbot. Aquaculture 2000, 188:103-114.
37. Ringwood A.H., Conners D.E. The effects of glutathione depletion on reproductive success in oysters, Crassostrea virginica. Mar. Environ. Res. 2000, 50:207-211.
38. Romero M.C., Ansaldo M., Lovrich G.A. Effect of aerial exposure on the antioxidant status in the subantarctic stone crab Paralomis granulosa (Decapoda: Anomura). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2007, 146:54-59.
39. Sanchis D., Fleury C., Chomiki N., Goubern M., Huang Q., Neverova M., Grégoire F., Easlick J., Raimbault S., Lévi-Meyrueis C., Miroux B., Collins S., Seldin M., Richard D., Warden C., Bouillaud F., Ricquier D. BMCP1, a novel mitochondrial carrier with high expression in the central nervous system of humans and rodents, and respiration uncoupling activity in recombinant yeast. J. Biol. Chem. 1998, 273:34611-34615.
40. Semenza G.L. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J. Appl. Physiol. 2000, 88:1474-1480.
41. Shumway S.E. Effect of salinity fluctuation on the osmotic pressure and Na+, Ca2+ and Mg2+ ion concentrations in the hemolymph of bivalve molluscs. Mar. Biol. 1977, 41:153-177.
42. Sluse F.E., Jarmuszkiewicz W. Uncoupling proteins outside the animal and plant kingdoms: functional and evolutionary aspects. FEBS Lett. 2002, 510:117-120.
43. Sonanez-Organis J.G., Peregrino-Uriarte A.B., Gomez-Jimenez S., Lopez-Zavala A., Forman H.J., Yepiz-Plascencia G. Molecular characterization of hypoxia inducible factor-1 (HIF-1) from the white shrimp Litopenaeus vannamei and tissue-specific expression under hypoxia. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2009, 150:395-405.
44. Stahlberg A., Aman P., Ridell B., Mostad P., Kubista M. Quantitative Real-Time PCR method for detection of B-lymphocyte monoclonality by comparison of κ and λ immunoglobulin light chain expression. Clin. Chem. 2003, 49:51-59.
45. Staniek K., Nohl H. Are mitochondria a permanent source of reactive oxygen species? BBA. Bioenergetics 2000, 1460:268-275.
46. Storey K.B. Oxidative stress: animal adaptations in nature. Braz. J. Med. Biol. Res. 1996, 29:1715-1733.
47. Sussarellu R., Fabioux C., Le Moullac G., Fleury E., Moraga D. Transcriptomic response of the Pacific oyster Crassostrea gigas to hypoxia. Mar. Genomics 2010, 3:133-143.
48. Tran D., Boudou A., Massabuau J.-C. Mechanism for maintaining oxygen consumption under varying oxygenation levels in the freshwater clam Corbicula fluminea. Can. J. Zool. 2000, 78:2027-2036.
49. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 2003, 552:335-344.
50. Turrens J.F., Freeman B.A., Levitt J.G., Crapo J.D. The effect of hyperoxia on superoxide production by lung submitochondrial particles. Arch. Biochem. Biophys. 1982, 217:401-410.
51. Vanlerberghe G.C., McIntosh L. Alternative oxidase: from gene to function. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 1997, 48:703-734.
52. Viarengo A., Canesi L., Garcia Martinez P., Peters L.D., Livingstone D.R. Pro-oxidant processes and antioxidant defence systems in the tissues of the Antarctic scallop (Adamussium colbecki) compared with the Mediterranean scallop (Pecten jacobaeus). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 1995, 111:119-126.
53. Vidal M.-L., Bassères A., Narbonne J.-F. Influence of temperature, pH, oxygenation, water-type and substrate on biomarker responses in the freshwater clam Corbicula fluminea (Müller). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2002, 132:93-104.
54. Weihe E., Kriews M., Abele D. Differences in heavy metal concentrations and in the response of the antioxidant system to hypoxia and air exposure in the Antarctic limpet Nacella concinna. Mar. Environ. Res. 2010, 69:127-135.
55. Wu R.S.S. Hypoxia: from molecular responses to ecosystem responses. Mar. Pollut. Bull. 2002, 45:35-45.
56. Yu X.X., Mao W., Zhong A., Schow P., Brush J., Sherwood S.W., Adams S.H., Pan G. Characterization of novel UCP5/BMCP1 isoforms and differential regulation of UCP4 and UCP5 expression through dietary or temperature manipulation. FASEB J. 2000, 14:1611-1618.