Molecular cloning of manganese superoxide dismutase gene in the cladoceran Daphnia magna: Effects of microcystin, nitrite, and cadmium on gene expression profiles

Aquatic Toxicology

Volumn 148, Issue , 2014, Pages 55-64

  Lyu, Kai ^a   Zhu, Xuexia ^a   Chen, Rui ^a   Chen, Yafen ^b   Yang, Zhou ^a  

^a NANJING NORMAL UNIVERSITY   (China)

^b NANJING INSTITUTE OF GEOGRAPHY AND LIMNOLOGY   (China)

Author keywords

Antioxidation; Biomarker; Cladoceran; Enzyme activity; Oxidative stress

Indexed keywords

CADMIUM; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; MICROCYSTIN LR; NITRITE;

ANTIOXIDANT; BIOMARKER; CADMIUM; CRUSTACEAN; ENZYME ACTIVITY; GENE EXPRESSION; NITRITE; POLLUTION EXPOSURE;

ADULT; AMINO ACID SEQUENCE; ARTICLE; BYTHOGRAEA THERMYDRON; CANCER PAGURUS; CONTROLLED STUDY; CRUSTACEA; DAPHNIA MAGNA; DROMIA PERSONATA; GENE EXPRESSION PROFILING; JUVENILE ANIMAL; METAL BINDING; MOLECULAR CLONING; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; SCYLLA PARAMAMOSAIN; UPREGULATION; WATER POLLUTANT;

ANTIOXIDATION; BIOMARKER; CLADOCERAN; ENZYME ACTIVITY; OXIDATIVE STRESS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BIOLOGICAL MARKERS; CADMIUM; DAPHNIA; GENE EXPRESSION REGULATION; MICROCYSTINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NITRITES; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SUPEROXIDE DISMUTASE; WATER POLLUTANTS, CHEMICAL;

EID: 84892849418     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2013.12.031     Document Type: Article

References (81)

1. Alberto A., Rocío O.B., Fernando M.J. Age effect on the antioxidant activity of Daphnia magna (Anomopoda: Daphniidae): does younger mean more sensitivity?. J. Environ. Biol. 2011, 32:481-487.
2. Alonso E., Santos A., Callejón M., Jiménez J. Speciation as a screening tool for the determination of heavy metal surface water pollution in the Guadiamar river basin. Chemosphere 2004, 56:561-570.
3. Amado L.L., Monserrat J.M. Oxidative stress generation by microcystins in aquatic animals: why and how. Environ. Int. 2010, 36:226-235.
4. Arzate-Cárdenas M.A., Martínez-Jerónimo F. Age-altered susceptibility in hexavalent chromium-exposed Daphnia schodler (Anomopoda, Daphniidae): integrated biomarker response implementation. Aquat. Toxicol. 2011, 105:528-534.
5. Bandara J., Senevirathna D., Dasanayake D., Herath V., Bandara J., Abeysekara T., et al. Chronic renal failure among farm families in cascade irrigation systems in Sri Lanka associated with elevated dietary cadmium levels in rice and freshwater fish (Tilapia). Environ. Geochem. Health 2008, 30:465-478.
6. Barata C., Carlos Navarro J., Varo I., Carmen Riva M., Arun S., Porte C. Changes in antioxidant enzyme activities, fatty acid composition and lipid peroxidation in Daphnia magna during the aging process. Comp. Biochem. Physiol. B-Biochem. Mol. Biol. 2005, 140:81-90.
7. Becker D., Brinkmann B.F., Zeis B., Paul R.J. Acute changes in temperature or oxygen availability induce ROS fluctuations in Daphnia magna linked with fluctuations of reduced and oxidized glutathione, catalase activity and gene (haemoglobin) expression. Biol. Cell 2011, 103:351-363.
8. Bervoets L., Blust R. Metal concentrations in water, sediment and gudgeon (Gobio gobio) from a pollution gradient: relationship with fish condition factor. Environ. Pollut. 2003, 126:9-19.
9. Bohrer R., Lampert W. Simultaneous measurement of the effect of food concentration on assimilation and respiration in Daphnia magna Straus. Funct. Ecol. 1988, 2:463-471.
10. Borgstahl G.E., Parge H.E., Hickey M.J., Beyer W.F., Hallewell R.A., Tainer J.A. The structure of human mitochondrial manganese superoxide dismutase reveals a novel tetrameric interface of two 4-helix bundles. Cell 1992, 71:107-118.
11. Brouwer M., Brouwer T.H., Grater W., Brown-Peterson N. Replacement of a cytosolic copper/zinc superoxide dismutase by a novel cytosolic manganese superoxide dismutase in crustaceans that use copper (haemocyanin) for oxygen transport. Biochem. J. 2003, 374:219.
12. Cadenas E., Davies K. Mitochondrial free radical generation, oxidative stress, and aging. Free Radical Biol. Med. 2000, 29:222.
13. Chen W., Song L., Ou D., Gan N. Chronic toxicity and responses of several important enzymes in Daphnia magna on exposure to sublethal microcystin-LR. Environ. Toxicol. 2005, 20:323-330.
14. Cheng W., Tung Y.H., Liu C.H., Chen J.C. Molecular cloning and characterisation of cytosolic manganese superoxide dismutase (cytMn-SOD) from the giant freshwater prawn Macrobrachium rosenbergii. Fish Shellfish Immunol. 2006, 20:438-449.
15. Cho Y.S., Lee S.Y., Bang I.C., Kim D.S., Nam Y.K. Genomic organization and mRNA expression of manganese superoxide dismutase (Mn-SOD) from Hemibarbus mylodon (Teleostei, Cypriniformes). Fish Shellfish Immunol. 2009, 27:571-576.
16. Choi J., Roche H., Caquet T. Characterization of superoxide dismutase activity in Chironomus riparius Mg. (Diptera, Chironomidae) larvae-a potential biomarker. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 1999, 124:73-81.
17. Choi Y.S., Lee K.S., Yoon H.J., Kim I., Sohn H.D., Jin B.R. Bombus ignitus Cu, Zn superoxide dismutase (SOD1): cDNA cloning, gene structure, and up-regulation in response to paraquat, temperature stress, or lipopolysaccharide stimulation. Comp. Biochem. Physiol. B-Biochem. Mol. Biol. 2006, 144:365-371.
18. Connon R., Hooper H.L., Sibly R.M., Lim F.L., Heckmann L.H., Moore D.J., et al. Linking molecular and population stress responses in Daphnia magna exposed to cadmium. Environ. Sci. Technol. 2008, 42:2181-2188.
19. Cook C.E., Yue Q., Akam M. Mitochondrial genomes suggest that hexapods and crustaceans are mutually paraphyletic. Proc. R. Soc. B-Biol. Sci. 2005, 272:1295-1304.
20. den Hartog G.J., Haenen G.R., Vegt E., van der Vijgh W.J., Bast A. Superoxide dismutase: the balance between prevention and induction of oxidative damage. Chem.-Biol. Interact. 2003, 145:33-39.
21. Dhar A.K., Bowers R.M., Licon K.S., Veazey G., Read B. Validation of reference genes for quantitative measurement of immune gene expression in shrimp. Mol. Immunol. 2009, 46:1688-1695.
22. Duttaroy A., Meidinger R., Kirby K., Carmichael S., Hilliker A., Phillips J. A manganese superoxide dismutase-encoding cDNA from Drosophila melanogaster. Gene 1994, 143:223-225.
23. Elendt B.P., Bias W.R. Trace nutrient deficiency in Daphnia magna cultured in standard medium for toxicity testing. Effects of the optimization of culture conditions on life history parameters of D. magna. Water Res. 1990, 24:1157-1167.
24. Gómez-Anduro G.A., Barillas-Mury C.V., Peregrino-Uriarte A.B., Gupta L., Gollas-Galván T., Hernández-López J., et al. The cytosolic manganese superoxide dismutase from the shrimp Litopenaeus vannamei: Molecular cloning and expression. Dev. Comp. Immunol. 2006, 30:893-900.
25. García-Machado E., Pempera M., Dennebouy N., Oliva-Suarez M., Mounolou J.-C., Monnerot M. Mitochondrial genes collectively suggest the paraphyly of Crustacea with respect to Insecta. J. Mol. Evol. 1999, 49:142-149.
26. Glazier D.S. Separating the respiration rates of embryos and brooding females of Daphnia magna: Implications for the cost of brooding and the allometry of metabolic rate. Limnol. Oceanogr. 1991, 36:354-362.
27. Hannas B.R., Das P.C., Li H., LeBlanc G.A. Intracellular conversion of environmental nitrate and nitrite to nitric oxide with resulting developmental toxicity to the crustacean Daphnia magna. PLoS One 2010, 5:e12453.
28. Heckmann L.H., Connon R., Hutchinson T.H., Maund S.J., Sibly R.M., Callaghan A. Expression of target and reference genes in Daphnia magna exposed to ibuprofen. BMC Genomics 2006, 7:175.
29. Hunter T., Bannister W.H., Hunter G.J. Cloning, expression, and characterization of two manganese superoxide dismutases from Caenorhabditis elegans. J. Biol. Chem. 1997, 272:28652-28659.
30. Jensen F.B. Nitrite disrupts multiple physiological functions in aquatic animals. Comp. Biochem. Physiol. A-Mol. Integr. Physiol. 2003, 135:9-24.
31. Jones G.J., Orr P.T. Release and degradation of microcystin following algicide treatment of a Microcystis aeruginosa bloom in a recreational lake, as determined by HPLC and protein phosphatase inhibition assay. Water Res. 1994, 28:871-876.
32. Kamstra A., Span J., Weerd J.H. The acute toxicity and sublethal effects of nitrite on growth and feed utilization of European eel, Anguilla anguilla (L.). Aquacult. Res. 1996, 27:903-911.
33. Karnati S., Luers G., Pfreimer S., Baumgart-Vogt E. Mammalian SOD2 is exclusively located in mitochondria and not present in peroxisomes. Histochem. Cell Biol. 2013, 140:105-117.
34. Kasahara T., Miyazaki T., Nitta H., Ono A., Miyagishima T., Nagao T., et al. Evaluation of methods for duration of preservation of RNA quality in rat liver used for transcriptome analysis. J. Toxicol. Sci. 2006, 31:509-519.
35. Kim B.M., Rhee J.S., Park G.S., Lee J., Lee Y.M., Lee J.S. Cu/Zn- and Mn-superoxide dismutase (SOD) from the copepod Tigriopus japonicus: Molecular cloning and expression in response to environmental pollutants. Chemosphere 2011, 84:1467-1475.
36. Kim J.H., Rhee J.S., Lee J.S., Dahms H.U., Lee J., Han K.N., et al. Effect of cadmium exposure on expression of antioxidant gene transcripts in the river pufferfish, Takifugu obscurus (Tetraodontiformes). Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 2010, 152:473-479.
37. Kim J., Kim S., An K.W., Choi C.Y., Lee S., Choi K. Molecular cloning of Daphnia magna catalase and its biomarker potential against oxidative stresses. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 2010, 152:263-269.
38. Kong B.W., Kim H., Foster D.N. Expression analysis and mitochondrial targeting properties of the chicken manganese-containing superoxide dismutase. Biochim. Biophys. Acta 2003, 1625:98-108.
39. Legg D.A., Sutton M.D., Edgecombe G.D. Arthropod fossil data increase congruence of morphological and molecular phylogenies. Nat. commun. 2013, 4. 10.1038/ncomms3485.
40. Li X., Liu Y., Song L., Liu J. Responses of antioxidant systems in the hepatocytes of common carp (Cyprinus carpio L.) to the toxicity of microcystin-LR. Toxicon 2003, 42:85-89.
41. -δδCT method. Methods 2001, 25:402-408.
42. Lushchak V.I. Environmentally induced oxidative stress in aquatic animals. Aquat. Toxicol. 2011, 101:13-30.
43. Lyu K., Wang Q., Chen R., Lu Q., Yang Z. Inter-specific differences in survival and reproduction of cladocerans to nitrite gradient and the ecological implications. Biochem. Syst. Ecol. 2013, 48:151-156.
44. Lyu K., Zhu X., Wang Q., Chen Y., Yang Z. Copper/zinc superoxide dismutase from the cladoceran Daphnia magna: molecular cloning and expression in response to different acute environmental stressors. Environ. Sci. Technol. 2013, 47:8887-8893.
45. Malek R.L., Sajadi H., Abraham J., Grundy M.A., Gerhard G.S. The effects of temperature reduction on gene expression and oxidative stress in skeletal muscle from adult zebrafish. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 2004, 138:363-373.
46. Marinković M., de Leeuw W.C., Ensink W.A., de Jong M., Breit T.M., Admiraal W., Kraak M.H., Jonker M.J. Gene expression patterns and life cycle responses of toxicant-exposed chironomids. Environ. Sci. Technol. 2012, 46:12679-12686.
47. Miccadei S., Floridi A. Sites of inhibition of mitochondrial electron transport by cadmium. Chem.-Biol. Interact. 1993, 89:159-167.
48. Mikhailov A., Härmälä-Braskén A.S., Hellman J., Meriluoto J., Eriksson J.E. Identification of ATP-synthase as a novel intracellular target for microcystin-LR. Chem.-Biol. Interact. 2003, 142:223-237.
49. Mruk D.D., Silvestrini B., Mo M.Y., Cheng C.Y. Antioxidant superoxide dismutase-a review: its function, regulation in the testis, and role in male fertility. Contraception 2002, 65:305-311.
50. Ortiz-Rodríguez R., Wiegand C. Age related acute effects of microcystin-LR on Daphnia magna biotransformation and oxidative stress. Toxicon 2010, 56:1342-1349.
51. Paerl H.W., Huisman J. Climate. Blooms like it hot. Science 2008, 320:57-58.
52. Pan L., Zhang H. Metallothionein, antioxidant enzymes and DNA strand breaks as biomarkers of Cd exposure in a marine crab, Charybdis japonica. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 2006, 144:67-75.
53. Parker M.W., Blake C.C. Crystal structure of manganese superoxide dismutase from Bacillus stearothermophilus at 2, 4Å resolution. J. Mol. Biol. 1988, 199:649-661.
54. Porta J., Vahedi-Faridi A., Borgstahl G.E. Structural analysis of peroxide-soaked MnSOD crystals reveals side-on binding of peroxide to active-site manganese. J. Mol. Biol. 2010, 399:377-384.
55. Rahman M.S., Thomas P. Effects of hypoxia exposure on hepatic cytochrome p450 1a (CYP1a) expression in Atlantic croaker: molecular mechanisms of CYP1a down-regulation. PLoS One 2012, 7:e40825.
56. Ray P.D., Huang B.W., Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell. Signal 2012, 24:981-990.
57. Romano N., Zeng C. Toxic effects of ammonia, nitrite, and nitrate to decapod crustaceans: a review on factors influencing their toxicity, physiological consequences, and coping mechanisms. Rev. Fish. Sci. 2013, 21:1-21.
58. Sarma S., Nandini S. Review of recent ecotoxicological studies on cladocerans. J. Environ. Sci. Health Part B-Pestic. Contam. Agric. Wastes 2006, 41:1417-1430.
59. Satarug S., Baker J.R., Urbenjapol S., Haswell-Elkins M., Reilly P.E., Williams D.J., et al. A global perspective on cadmium pollution and toxicity in non-occupationally exposed population. Toxicol. Lett. 2003, 137:65-83.
60. Semedo M., Reis-Henriques M.A., Rey-Salgueiro L., Oliveira M., Delerue-Matos C., Morais S., et al. Metal accumulation and oxidative stress biomarkers in octopus (Octopus vulgaris) from Northwest Atlantic. Sci. Total Environ. 2012, 433:230-237.
61. Sharma V.K. Reactive oxygen species. Oxidation of Amino Acids, Peptides, and Proteins: Kinetics and Mechanism 2013, 122-204. John Wiley & Sons, Inc.
62. Shi H., Sui Y., Wang X., Luo Y., Ji L. Hydroxyl radical production and oxidative damage induced by cadmium and naphthalene in liver of Carassius auratus. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 2005, 140:115-121.
63. Svrcek C., Smith D.W. Cyanobacteria toxins and the current state of knowledge on water treatment options: a review. J. Environ. Eng. Sci. 2004, 3:155-185.
64. Tang B., Zhu L., Zhou Q. Joint effects of Penta-BDE and heavy metals on Daphnia magna survival, its antioxidant enzyme activities and lipid peroxidation. Front. Environ. Sci. Eng. China 2011, 5:99-110.
65. Umasuthan N., Bathige S.D.N.K., Revathy K.S., Lee Y., Whang I., Choi C.Y., et al. A manganese superoxide dismutase (MnSOD) from Ruditapes philippinarum: Comparative structural- and expressional-analysis with copper/zinc superoxide dismutase (Cu/ZnSOD) and biochemical analysis of its antioxidant activities. Fish Shellfish Immunol. 2012, 33:753-765.
66. Umasuthan N., Revathy K.S., Bathige S.D., Lim B.S., Park M.A., Whang I., et al. A manganese superoxide dismutase with potent antioxidant activity identified from Oplegnathus fasciatus: genomic structure and transcriptional characterization. Fish Shellfish Immunol. 2013, 34:23-37.
67. Valavanidis A., Vlahogianni T., Dassenakis M., Scoullos M. Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol. Environ. Saf. 2006, 64:178-189.
68. Vega M.P., Pizarro R.A. Oxidative stress and defence mechanisms of the freshwater cladoceran Daphnia longispina exposed to UV radiation. J. Photochem. Photobiol., B 2000, 54:121-125.
69. Wang M., Su X., Li Y., Jun Z., Li T. Cloning and expression of the Mn-SOD gene from Phascolosoma esculenta. Fish Shellfish Immunol. 2010, 29:759-764.
70. Wang W., Wang A., Zhang Y. Effect of dietary higher level of selenium and nitrite concentration on the cellular defense response of Penaeus vannamei. Aquaculture 2006, 256:558-563.
71. Wang Y., Fang J., Leonard S.S., Krishna Rao K.M. Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radical Biol. Med. 2004, 36:1434-1443.
72. Wang Z.C., Cai F., Chen X.Y., Luo M.H., Hu L.L., Lu Y. The role of mitochondria-derived reactive oxygen species in hyperthermia-induced platelet apoptosis. PLoS One 2013, 8:e75044.
73. White J.D., Kaul R.B., Knoll L.B., Wilson A.E., Sarnelle O. Large variation in vulnerability to grazing within a population of the colonial phytoplankter, Microcystis aeruginosa. Limnol. Oceanogr. 2011, 56:1714-1724.
74. Wilson A.E., Sarnelle O., Tillmanns A.R. Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: meta-analyses of laboratory experiments. Limnol. Oceanogr. 2006, 51:1915-1924.
75. Xiang F.H., Yang W., Chen Y.F., Yang Z. Acute toxicity of nitrite and ammonia to Daphnia similoides of different developmental stages: using the modified gaussian model to describe. Bull. Environ. Contam. Toxicol. 2010, 84:708-711.
76. Yang Z., Lü K., Chen Y., Montagnes D.J. The interactive effects of ammonia and microcystin on life-history traits of the cladoceran Daphnia magna: synergistic or antagonistic?. PLoS One 2012, 7:e32285.
77. Yang Z., Xiang F., Minter E.J., Lü K., Chen Y., Montagnes D.J. The interactive effects of microcystin and nitrite on life-history parameters of the cladoceran Daphnia obtusa. J. Hazard. Mater. 2011, 190:113-118.
78. Zelko I.N., Mariani T.J., Folz R.J. Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radical Biol. Med. 2002, 33:337-349.
79. Zhang Q., Li F., Wang B., Zhang J., Liu Y., Zhou Q., et al. The mitochondrial manganese superoxide dismutase gene in Chinese shrimp Fenneropenaeus chinensis: Cloning, distribution and expression. Dev. Comp. Immunol. 2007, 31:429-440.
80. Zhang X., Chen C., Ding J., Hou A., Li Y., Niu Z., et al. The 2007 water crisis in Wuxi, China: analysis of the origin. J. Hazard. Mater. 2010, 182:130-135.
81. Zhang X., Xie P., Wang W., Li D., Li L., Tang R., et al. Dose-dependent effects of extracted microcystins on embryonic development, larval growth and histopathological changes of southern catfish (Silurus meridionalis). Toxicon 2008, 51:449-456.