Expression and function analysis of metallothionein in the testis of stone crab Charybdis japonica exposed to cadmium

Aquatic Toxicology

Volumn 124-125, Issue , 2012, Pages 11-21

  Mao, Huan ^a,b   Tan, Fu Qing ^b   Wang, Da Hui ^a   Zhu, Jun Quan ^c   Zhou, Hong ^a   Yang, Wan Xi ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c NINGBO UNIVERSITY   (China)

Author keywords

Cadmium; Charybdis japonica; Metallothionein; Spermiogenesis; Testis

Indexed keywords

AMINO ACID; BIOLOGICAL MARKER; CADMIUM; COMPLEMENTARY DNA; CYSTEINE; MESSENGER RNA; METALLOTHIONEIN;

AMINO ACID; BIOMARKER; CADMIUM; CRAB; DNA; GENE EXPRESSION; METALLOTHIONEIN; POLLUTION EXPOSURE; PROTEIN; RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CHARYBDIS JAPONICA; CONTROLLED STUDY; CRAB; DNA SEQUENCE; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SPECIES DIFFERENTIATION; SPERMATOGENESIS; TESTIS; WATER POLLUTION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BRACHYURA; CADMIUM; DNA, MITOCHONDRIAL; GENE EXPRESSION REGULATION; MALE; METALLOTHIONEIN; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ALIGNMENT; TESTIS; WATER POLLUTANTS, CHEMICAL;

ANIMALIA; CHARYBDIS JAPONICA; DECAPODA (CRUSTACEA); INVERTEBRATA; VERTEBRATA;

EID: 84864809133     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.07.005     Document Type: Article

References (80)

1. + antiporter in invertebrates. Journal of Experimental Zoology 2001, 289(4):232-244.
2. Alsberg C.L., Schwartze E.W. Pharmacological action of cadmium. Journal of Pharmacology and Experimental Therapeutics 1919, 13:504-505.
3. Au D.W., Chiang M.W., Wu R.S. Effects of cadmium and phenol on motility and ultrastructure of sea urchin and mussel spermatozoa. Archives of Environmental Contamination and Toxicology 2000, 38(4):455-463.
4. Benoff S., Jacob A., Hurley I. Male infertility and environmental exposure to lead and cadmium. Human Reproduction 2000, 6(2):107-121.
5. Blindauer C.A., Leszczyszyn O.I. Metallothioneins: unparalleled diversity in structures and functions for metal ion homeostasis and more. Natural Products Reports 2010, 27:720-741.
6. Braissant O., Wahli W. A simplified in situ hybridization protocol using non-radioactively labeled probes to detect abundant and rare mRNAs on tissue sections. Biochemica 1998, 1:10-16.
7. Brouwer M., Enghild J., Hoexum-Brouwer T., Thogersen I., Truncali A. Primary structure and tissue-specific expression of blue crab (Callinectes sapidus) metallothionein isoforms. Biochemical Journal 1995, 311(2):617-622.
8. Brouwer M., Syring R., Hoexum B.T. Role of a copper-specific metallothionein of the blue crab, Callinectes sapidus, in copper metabolism associated with degradation and synthesis of hemocyanin. Journal of Inorganic Biochemistry 2002, 88(2):228-239.
9. Brown D.A., Parsons T.R. Relationship between cytoplasmic distribution of mercury and toxic effects to zooplancton and chum salmon (Oncorhynchus keta) exposed to mercury in a controlled ecosystem. Journal of the Fisheries Research Board of Canada 1978, 35:880-884.
10. Canli M., Stagg R.M., Rodger G. The induction of metallothionein in tissues of the Norway lobster Nephrops norvegicus following exposure to cadmium, copper and zinc: the relationships between metallothionein and the metals. Environmental Pollution 1997, 96(3):343-350.
11. Chabanon H., Nury D., Mickleburgh I., Burtle B., Hesketh J. Characterization of the cis-acting element directing perinuclear localization of the metallothionein-1 mRNA. Biochemical Society Transactions 2004, 32(5):702-704.
12. Chavez-Crooker P., Pozo P., Castro H., Dice M.S., Boutet I., Tanguy A., Moraga D., Ahearn G.A. Cellular localization of calcium, heavy metals, and metallothionein in lobster (Homarus americanus) hepatopancreas. Comparative Biochemistry and Physiology. Toxicology & Pharmacology: CBP 2003, 136(3):213-224.
13. Cheung L.A.P., Lam V.K.L., Chan K.M. Tilapia metallothionein genes: PCR-cloning and gene expression studies. Biochimica et Biophysica Acta 2005, 1731(3):191-201.
14. Cho Y.S., Choi B.N., Kim K.H., Kim S.K., Kim D.S., Bang I.C., Nam Y.K. Differential expression of Cu/Zn superoxide dismutase mRNA during exposures to heavy metals in rockbream (Oplegnathus fasciatus). Aquaculture 2006, 253(1-4):667-679.
15. Cho Y.S., Lee S.Y., Kim K.-Y., Nam Y.K. Two metallothionein genes from mud loach Misgurnus mizolepis (Teleostei; Cypriniformes): gene structure, genomic organization, and mRNA expression analysis. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 2009, 153(4):317-326.
16. Cody C.W., Huang P.C. Metallothionein detoxification function is impaired by replacement of both conserved lysines with glutamines in the hinge between the two domains. Biochemistry 1993, 32(19):5127-5131.
17. Cody C.W., Huang P.C. Replacement of all alpha-domain lysines with glutamates reduces metallothionein detoxification function. Biochemical and Biophysical Research Communications 1994, 202(2):954-959.
18. de Souza Predes F., Monteiro J.C., Matta S.L., Garcia M.C., Dolder H. Testicular histomorphometry and ultrastructure of rats treated with cadmium and Ginkgo biloba. Biological Trace Element Research 2011, 140(3):330-341.
19. De S.K., Enders G.C., Andrews G.K. High levels of metallothionein messenger RNAs in male germ cells of the adult mouse. Molecular Endocrinology 1991, 5(5):628-636.
20. De Ambrogi M., Spinaci M., Galeati G., Tamanini C. Viability and DNA fragmentation in differently sorted boar spermatozoa. Theriogenology 2006, 66(8):1994-2000.
21. Du N.S., Xue L.Z., Lai W. Studies on the sperm of Chinese mitten-handed crab, Eriocheir sinensis (Crustacea, Decapoda). II. Spermatogenesis. Oceanologia et Limnologia Sinica 1988, 19(1):71-75.
22. Dunn M.A. Metallothionein. Proceedings of the Society for Experimental Biology and Medicine 1987, 185:107-119.
23. Gao A.B., Wang L., Yuan H. Expression of metallothionein cDNA in a freshwater crab, Sinopotamon yangtsekiense, exposed to cadmium. Experimental and Toxicologic Pathology 2012, 64(3):253-258.
24. Gunnarsson D., Nordberg G., Lundgren P., Selstam G. Cadmium-induced decrement of the LH receptor expression and cAMP levels in the testis of rats. Toxicology 2003, 183(1-3):57-63.
25. Haffor A.S., Abou-Tarboush F.M. Testicular cellular toxicity of cadmium: transmission electron microscopy examination. Journal of Environment biology 2004, 25(3):251-258.
26. Hao Q., Hong S.-H., Maret W. Lipid raft-dependent endocytosis of metallothionein in HepG2 cells. Journal of Cellular Physiology 2007, 210(2):428-435.
27. He L., Girijashanker K., Dalton T.P., Reed J., Li H., Soleimani M., Nebert D.W. ZIP8, member of the solute-carrier-39 (SLC39) metal-transporter family: characterization of transporter properties. Molecular Pharmacology 2006, 70(1):171-180.
28. He Z., Kokkinaki M., Dym M. Signaling molecules and pathways regulating the fate of spermatogonial stem cells. Microscopy Research and Technique 2009, 72(8):586-595.
29. Hesketh J. 3'-Untranslated regions are important in mRNA localization and translation: lessons from selenium and metallothionein. Biochemical Society Transactions 2004, 32(6):990-993.
30. Hinsch G.W. Spermiogenesis in a hermit-crab, Coenobita clypeatus. II. Sertoli cells. Tissue and Cell 1980, 12(2):255-262.
31. Johnson M.R., Wang K., Smith J.B. Quantitation of dihydropyrimidine dehydrogenase expression by real-time reverse transcription polymerase chain reaction. Analytical Biochemistry 2000, 278(2):175-184.
32. Kagi J.H., Schaffer A. Biochemistry of metallothionein. Biochemistry 1988, 27(23):8509-8515.
33. Kojima Y. Definitions and nomenclature of metallothioneins. Methods in Enzymology 1991, 205:8-10.
34. Kusakabe T., Nakajima K., Suzuki K., Nakazato K., Takada H., Satoh T., Oikawa M., Kobayashi K., Koyama H., Arakawa K., Nagamine T. The changes of heavy metal and metallothionein distribution in testis induced by cadmium exposure. Biometals 2008, 21(1):71-81.
35. Laberge R.M., Boissonneault G. Chromatin remodeling in spermatids: a sensitive step for the genetic integrity of the male gamete. Archives of Andrology 2005, 51(2):125-133.
36. Leignel V., Marchand J., Moreau B., Chénais B. Metallothionein genes from hydrothermal crabs (Bythograeidae, Decapoda): characterization, sequence analysis, gene expression and comparison with coastal crabs. Comparative Biochemistry and Physiology. Toxicology & Pharmacology: CBP 2008, 148(1):6-13.
37. Li L.-H., Heindel J.J. Sertoli cell toxicants. Reproductive and Developmental Toxicology 1998, 655-691. Marcel Dekker, New York. K.S. Korach (Ed.).
38. Ma W.-L., Yan T., He Y., Wang L. Purification and cDNA cloning of a cadmium-binding metallothionein from the freshwater crab Sinopotamon henanense. Archives of Environment Contamination and Toxicology 2009, 56(4):747-753.
39. Mickleburgh I., Burtle B., Nury D., Chabanon H., Chrzanowska-Lightowlers Z., Hesketh J.E. Isolation and identification of a protein binding to the localization element ofmetallothionein-1mRNA. Biochemical Society Transactions 2004, 32(5):705-706.
40. Migliarini B., Campisi A.M., Maradonna F., Truzzi C., Annibaldi A., Scarponi G., Carnevali O. Effects of cadmium exposure on testis apoptosis in the marine teleost Gobius niger. General and Comparative Endocrinology 2005, 142(1-2):241-247.
41. Moltedo O., Verde C., Capasso A., Parisi E., Remondelli P., Bonatti S., Alvarez-Hernandez X., Glass J., Alvino C.G., Leone A. Zinc transport and metallothionein secretion in the intestinal human cell line Caco-2. Journal of Biological Chemistry 2000, 275(41):31819-31825.
42. Moltó E., Bonzón-Kulichenko E., Arco A.D., López-Alañón D.M., Carrillo O., Gallardo N., Andrés A. Cloning, tissue expression and metal inducibility of an ubiquitous metallothionein from Panulirus argus. Gene 2005, 361:140-148.
43. Monsefi M., Alaee S., Moradshahi A., Rohani L. Cadmium-induced infertility in male mice. Environmental Toxicology 2009, 25(1):94-102.
44. Mouneyrac C., Amiard-Triquet C., Amiard J.C., Rainbow P.S. Comparison of metallothionein concentrations and tissue distribution of trace metals in crabs (Pachygrapsus marmoratus) from a metal-rich estuary, in and out of the reproductive season. Comparative Biochemistry and Physiology. Toxicology & Pharmacology: CBP 2001, 129(3):193-209.
45. Mukhopadhyay D., Mitra A., Nandi P., Varghese A.C., Murmu N., Chowdhury R., Chaudhuri K., Bhattacharyya A.K. Expression of metallothionein-1 (MT-1) mRNA in the rat testes and liver after cadmium injection. Systems Biology in Reproductive Medicine 2009, 55(5-6):188-192.
46. Muñoz A., Forsterling F.H., Shaw C.F., Petering D.H. Structure of the (113)Cd(3)beta domains from Homarus americanus metallothionein-1: hydrogen bonding and solvent accessibility of sulfur atoms. Journal of Biological Inorganic Chemistry 2002, 7(7-8):713-724.
47. Narula S.S., Brouwer M., Hua Y., Armitage I.M. Three-dimensional solution structure of Callinectes sapidus metallothionein-1 determined by homonuclear and heteronuclear magnetic resonance spectroscopy. Biochemistry 1995, 34(2):620-631.
48. Ngu T.T., Easton A., Stillman M.J. Kinetic analysis of arsenic-metalation of human metallothionein: significance of the two-domain structure. Journal of the American Chemical Society 2008, 130(50):17016-17028.
49. Nishimura H., Nishimura N., Tohyama C. Localization of metallothionein in the genital organs of the male rat. Journal of Histochemistry and Cytochemistry 1990, 38(7):927-933.
50. Nury D., Chabanon H., Levadoux-Martin M., Hesketh J. An eleven nucleotide section of the 3'-untranslated region is required for perinuclear localization of rat metallothionein-1 mRNA. Biochemical Journal 2005, 387(2):419-428.
51. Oliveira H., Spanò M., Santos C., Pereira M.L. Adverse effects of cadmium exposure on mouse sperm. Reproductive Toxicology 2009, 28(4):550-555.
52. Otvos J.D., Engeseth H.R., Wehrli S. Preparation and 113Cd NMR studies of homogeneous reconstituted metallothionein: reaffirmation of the two-cluster arrangement of metals. Biochemistry 1985, 24(24):6735-6740.
53. Pan L., Zhang H. Metallothionein, antioxidant enzymes and DNA strand breaks as biomarkers of Cd exposure in a marine crab, Charybdis japonica. Comparative Biochemistry and Physiology. Toxicology & Pharmacology: CBP 2006, 144(1):67-75.
54. Pedersen K.L., Pedersen S.N., Hojrup P., Andersen J.S., Roepstorff P., Knudsen J., Depledge M.H. Purification and characterization of a cadmium-induced metallonthionein from the shore crab Carcinus maenas (L). Biochemical Journal 1994, 297(3):609-614.
55. Pedersen S.N., Lundebye A.K., Depledge M.H. Field application of metallothionein and stress protein biomarkers in the shore crab (Carcinus maenas) exposed to trace metals. Aquatic Toxicology 1997, 37(2-3):183-200.
56. Prozialeck W.C., Edwards J.R., Nebert D.W., Woods J.M., Barchowsky A., Atchison W.D. The vascular system as a target of metal toxicity. Toxicological Sciences 2008, 102(2):207-218.
57. Ren F., Jiang H., Sun J., He L., Li W., Wang Y., Wang Q. Cloning, characterization, expression, and copper sensitivity of the metallothionein-1 gene in the Chinese mitten crab, Eriocheir sinensis. Molecular Biology Reports 2011, 38(4):2383-2393.
58. Riek R., Precheur B., Wang Y., Mackay E.A., Wider G., Guntert P., Liu A., Kägi J.H., Wuthrich K. NMR structure of the sea urchin (Strongylocentrotus purpuratus) metallothionein MTA. Journal of Molecular Biology 1999, 291(2):417-428.
59. Roy, A., Kucukural, A., Zhang, Y., 2010. I-TASSER: a unified platform for automated protein structure and function prediction. Nature Protocols 5, 725-738.
60. Shimoda R., Nagamine T., Takagi H., Mori M., Waalkes M.P. Induction of apoptosis in cells by cadmium: quantitative negative correlation between basal or induced metallothionein concentration and apoptotic rate. Toxicological Sciences 2001, 64(2):208-215.
61. Siu E.R., Mruk D.D., Porto C.S., Cheng C.Y. Cadmium-induced testicular injury. Toxicology and Applied Pharmacology 2009, 238(3):240-249.
62. Soegianto A., Charmantier-Daures M., Trilles J.P. Impact of cadmium on the structure of gills and epipodites of the shrimp Penaeus japonicus (Crustacea: Decapoda). Aquatic Living Resources 1999, 12(1):57-70.
63. Suzuki M., Abe K., Yoshinaga K., Obinata M., Furusawa M., Abe K. Specific arrest of spermatogenesis caused by apoptotic cell death in transgenic mice. Genes to Cells 1996, 1(12):1077-1086.
64. Tohyama C., Nishimura N., Suzuki J.S., Karasawa M., Nishimura H. Metallothionein mRNA in the testis and prostate of the rat detected by digoxigenin-labeled riboprobe. Histochemistry 1994, 101(5):341-346.
65. Trifonov S., Houtani T., Hamada S., Kase M., Maruyama M., Sugimoto T. In situ hybridization study of the distribution of choline acetyltransferase mRNA and its splice variants in the mouse brain and spinal cord. Neuroscience 2009, 159(1):344-357.
66. Tsujikawa K., Imai K., Kakutani M., Kayamori Y., Mimura T., Otaki N., Kimura M., Fukuyama R., Shimuzu N. Localization of metallothionein in nuclei of growing primary cultured adult rat hepatocytes. FEBS Letters 1991, 283(2):239-242.
67. User Bulletin No. 2, 1997. ABI Prism 7700 Sequence Detection System Revision A.
68. Viarengo A., Nott J.A. Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comparative Biochemistry and Physiology. Toxicology & Pharmacology: CBP 1993, 104(3):355-372.
69. Wang B., Schneider S.N., Dragin N., Girijashanker K., Dalton T.P., He L., Miller M.L., Stringer K.F., Soleimani M., Richardson D.D., Nebert D.W. Enhanced cadmium-induced testicular necrosis and renal proximal tubule damage caused by gene-dose increase in a Slc39a8-transgenic mouse line. American Journal of Physiology. Cell Physiology 2007, 292(4):1523-1535.
70. Wang D.H., Yang W.X. Molecular cloning and characterization of KIFC1-like kinesin gene (es-KIFC1) in the testis of the Chinese mitten crab Eriocheir sinensis. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 2010, 157(2):123-131.
71. Wang L., Xu T., Lei W.W., Liu D.M., Li Y.J., Xuan R.J., Ma J.J. Cadmium-induced oxidative stress and apoptotic changes in the testis of freshwater crab, Sinopotamon henanense. PLoS ONE 2011, 6(11):e27853.
72. Webb M. Role of metallothionein in cadmium metabolism. Handbook of Experimental Pharmacology 1986, 281-337. Springer-Verlag, New York. E.C. Foulkes (Ed.).
73. Wolff N.A., Abouhamed M., Verroust P.J., Thévenod F. Megalin-dependent internalization of cadmium-metallothionein and cytotoxicity in cultured renal proximal tubule cells. Journal of Pharmacology and Experimental Therapeutics 2006, 318(2):782-791.
74. Xu X.H., Yan B.L., Zheng J.S., Xu J.T., Xu G.C., Wu J.X. Study on the development of sex gland and reproductive cycle of Charybdis japonica (A. Milne-Edwards). Transactions of Oceanology and Limnology 2010, 2:29-36.
75. Xu X.H., Yan B.L., Xu J.T., Xu G.C., Pu Y.F., Wu J.X. Spermatozoa morphology and influence of environmental factors on viability rates in crab Charybdis japonica. Acta Oceanologica Sinica 2010, 32(5):93-99.
76. Ye B., Maret W., Vallee B.L. Zinc metallothionein imported into liver mitochondria modulates respiration. Proceedings of the National Academy of Sciences of the United States of America 2001, 98(5):2317-2322.
77. Yin Y., DeWolf W.C., Morgentaler A. Experimental cryptorchidism induces testicular germ cell apoptosis by p53-dependent and -independent pathways in mice. Biology of Reproduction 1998, 58(2):492-496.
78. Yin Y., Stahl B.C., Dewolf W.C., Morgentaler A. P53 and Fas are sequential mechanisms of testicular germ cell apoptosis. Journal of Andrology 2002, 23(1):64-70.
79. Zhang Y. Template-based modeling and free modeling by I-TASSER in CASP7. Proteins 2007, 69(8):108-117.
80. Zhang Z., Cheng H., Wang Y., Wang S., Xie F., Li S. Acrosome reaction of sperm in the mud crab Scylla serrata as a sensitive toxicity test for metal exposures. Archives of Environment Contamination and Toxicology 2010, 58(1):96-104.