Cadmium induces liver cell apoptosis through caspase-3A activation in purse red common carp (Cyprinus carpio)

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Gao, Dian ^a   Xu, Zhen'e ^a   Qiao, Panpan ^a   Liu, Shen ^a   Zhang, Li ^a   He, Penghui ^a   Zhang, Xiaoyan ^a   Wang, Yannan ^a   Min, Weiping ^a,b  

^a NANCHANG UNIVERSITY   (China)

^b Hematology Department Jiangxi Academy of Medical Science   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CADMIUM; CASPASE; CASPASE 3A; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARP; CASPASE 3A GENE; CONTROLLED STUDY; CYTOPLASM; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE; GENE ISOLATION; GENE SEQUENCE; LIVER CELL; LIVER TOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE;

ANIMALS; APOPTOSIS; CADMIUM; CARPS; CASPASE 3; ENZYME ACTIVATION; FISH PROTEINS; HEPATOCYTES; HUMANS; LIVER;

EID: 84892599306     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083423     Document Type: Article

References (69)

1. Portt L, Norman G, Clapp C, Greenwood M, Greenwood MT (2011) Antiapoptosis and cell survival: A review. BBA - Mol Cell Res 1813: 238-259.
2. Ulukaya E, Acilan C, Yilmaz Y (2011) Apoptosis: why and how does it occur in biology? Cell Biochem Funct 29: 468-480.
3. Walsh JG, Cullen SP, Sheridan C, Luethi AU, Gerner C, et al. (2008) Executioner caspase-3 and caspase-7 are functionally distinct proteases. Proc Natl Acad Sci U S A 105: 12815-12819.
4. Gonzalez D, Espino J, Bejarano I, Lopez JJ, Rodriguez AB, et al. (2010) Caspase-3 and-9 are activated in human myeloid HL-60 cells by calcium signal. Mol Cell Biochem 333: 151-157.
5. Kuranaga E (2011) Caspase signaling in animal development. Dev Growth Differ 53: 137-148.
6. Kumar S (2007) Caspase function in programmed cell death. Cell Death Differ 14: 32-43.
7. Martinez MM, Reif RD, Pappas D (2010) Detection of apoptosis: A review of conventional and novel techniques. Analytical Methods 2: 996-1004.
8. Wong RSY (2011) Apoptosis in cancer: from pathogenesis to treatment. J Exp Clin Cancer Res 30.
9. Jin Z, El-Deiry WS (2005) Overview of cell death signaling pathways. Cancer Biol Ther 4: 139-163.
10. Bivik C, Rosdahl I, Ollinger K (2007) Hsp70 protects against UVB induced apoptosis by preventing release of cathepsins and cytochrome c in human melanocytes. Carcinogenesis 28: 537-544.
11. Seitz SJ, Schleithoff ES, Koch A, Schuster A, Teufel A, et al. (2010) Chemotherapy-induced apoptosis in hepatocellular carcinoma involves the p53 family and is mediated via the extrinsic and the intrinsic pathway. Int J Cancer 126: 2049-2066.
12. Zhang L, Li L, Zhang G (2011) Gene discovery, comparative analysis and expression profile reveal the complexity of the Crassostrea gigas apoptosis system. Dev Comp Immunol 35: 603-610.
13. Wu H-C, Wu J-L, Chu H-L, Su Y-C, Hong J-R (2010) RGNNV induces mitochondria-mediated cell death via newly synthesized protein dependent pathway in fish cells. Fish Shellfish Immunol 29: 451-463.
14. Zhang JY, Zhang HJ, Ni WM (2009) Oxidative stress and apoptosis of Carassius auratus lymphocytes induced by nonplanar (PCB153) and coplanar (PCB169) polychlorinated biphenyl congeners in vitro. J Environ Sci (China) 21: 1284-1289.
15. Solhaug A, Refsnes M, Lag M, Schwarze PE, Husoy T, et al. (2004) Polycyclic aromatic hydrocarbons induce both apoptotic and anti-apoptotic signals in Hepa1c1c7 cells. Carcinogenesis 25: 809-819.
16. Jin Y, Pan X, Cao L, Ma B, Fu Z (2013) Embryonic exposure to cis-bifenthrin enantioselectively induces the transcription of genes related to oxidative stress, apoptosis and immunotoxicity in zebrafish (Danio rerio). Fish Shellfish Immunol 34: 717-723.
17. Pathak N, Mitra S, Khandelwal S (2013) Cadmium Induces Thymocyte Apoptosis via Caspase-Dependent and Caspase-Independent Pathways. J Biochem Mol Toxicol.
18. Luzio A, Monteiro SM, Fontaínhas-Fernandes AA, Pinto-Carnide O, Matos M, et al. (2013) Copper induced upregulation of apoptosis related genes in zebrafish (Danio rerio) gill. Aquat Toxicol 128-129: 183-189.
19. Sokolova IM, Evans S, Hughes FM (2004) Cadmium-induced apoptosis in oyster hemocytes involves disturbance of cellular energy balance but no mitochondrial permeability transition. J Exp Biol 207: 3369-3380.
20. Petanidis S, Hadzopoulou-Cladaras M, Salifoglou A (2013) Cadmium modulates H-ras expression and caspase-3 apoptotic cell death in breast cancer epithelial MCF-7 cells. J Inorg Biochem 121: 100-107.
21. Song NH, Koh JW (2012) Effects of cadmium chloride on the cultured human lens epithelial cells. Mol Vis 18: 983-988.
22. Zhang H, Cai C, Shi C, Cao H, Han Z, et al. (2012) Cadmium-induced oxidative stress and apoptosis in the testes of frog Rana limnocharis. Aquat Toxicol 122: 67-74.
23. Wang L, Xu T, Lei WW, Liu DM, Li YJ, et al. (2011) Cadmium-induced oxidative stress and apoptotic changes in the testis of freshwater crab, Sinopotamon henanense. PLoS One 6: e27853.
24. Mao WP, Ye JL, Guan ZB, Zhao JM, Zhang C, et al. (2007) Cadmium induces apoptosis in human embryonic kidney (HEK) 293 cells by caspase-dependent and -independent pathways acting on mitochondria. Toxicol In Vitro 21: 343-354.
25. Lee WK, Abouhamed M, Thevenod F (2006) Caspase-dependent and - independent pathways for cadmium-induced apoptosis in cultured kidney proximal tubule cells. Am J Physiol Renal Physiol 291: F823-F832.
26. Coutant A, Lebeau J, Bidon-Wagner N, Levalois C, Lectard B, et al. (2006) Cadmium-induced apoptosis in lymphoblastoid cell line: involvement of caspase-dependent and -independent pathways. Biochimie 88: 1815-1822.
27. Krumschnabel G, Ebner HL, Hess MW, Villunger A (2010) Apoptosis and necroptosis are induced in rainbow trout cell lines exposed to cadmium. Aquat Toxicol 99: 73-85.
28. Rose WL, Nisbet RM, Green PG, Norris S, Fan T, et al. (2006) Using an integrated approach to link biomarker responses and physiological stress to growth impairment of cadmium-exposed larval topsmelt. Aquat Toxicol 80: 298-308.
29. Gonzalez P, Baudrimont M, Boudou A, Bourdineaud JP (2006) Comparative effects of direct cadmium contamination on gene expression in gills, liver, skeletal muscles and brain of the zebrafish (Danio rerio). Biometals 19: 225-235.
30. Porter AG, Janicke RU (1999) Emerging roles of caspase-3 in apoptosis. Cell Death Differ 6: 99-104.
31. Kim NN, Lee J, Habibi HR, Choi CY (2012) Molecular cloning and expression of caspase-3 in the protandrous cinnamon clownfish, Amphiprion melanopus, during sex change. Fish Physiol Biochem 39: 417-429.
32. Elvitigala DAS, Whang I, Premachandra HKA, Umasuthan N, Oh M-J, et al. (2012) Caspase 3 from rock bream (Oplegnathus fasciatus): Genomic characterization and transcriptional profiling upon bacterial and viral inductions. Fish Shellfish Immunol 33: 99-110.
33. Reis MI, Nascimento DS, do Vale A, Silva MT, dos Santos NM (2007) Molecular cloning and characterisation of sea bass (Dicentrarchus labrax L.) caspase-3 gene. Mol Immunol 44: 774-783.
34. Yabu T, Kishi S, Okazaki T, Yamashita M (2001) Characterization of zebrafish caspase-3 and induction of apoptosis through ceramide generation in fish fathead minnow tailbud cells and zebrafish embryo. Biochem J 360: 39-47.
35. Li M, Ding Y, Mu Y, Ao J, Chen X (2011) Molecular cloning and characterization of caspase-3 in large yellow croaker (Pseudosciaena crocea). Fish Shellfish Immunol 30: 910-916.
36. Takle H, McLeod A, Andersen O (2006) Cloning and characterization of the executioner caspases 3, 6, 7 and Hsp70 in hyperthermic Atlantic salmon (Salmo salar) embryos. Comp Biochem Physiol B Biochem Mol Biol 144: 188-198.
37. Monteiro SM, dos Santos NMS, Calejo M, Fontainhas-Fernandes A, Sousa M (2009) Copper toxicity in gills of the teleost fish, Oreochromis niloticus: Effects in apoptosis induction and cell proliferation. Aquat Toxicol 94: 219-228.
38. Naruse K, Fukamachi S, Mitani H, Kondo M, Matsuoka T, et al. (2000) A detailed linkage map of medaka, Oryzias latipes: comparative genomics and genome evolution. Genetics 154: 1773-1784.
39. Xu J, Ji P, Zhao Z, Zhang Y, Feng J, et al. (2012) Genome-wide SNP discovery from transcriptome of four common carp strains. PLoS One 7: e48140.
40. Williams DR, Li W, Hughes MA, Gonzalez SF, Vernon C, et al. (2008) Genomic resources and microarrays for the common carp Cyprinus carpio L. J Fish Biol 72: 2095-2117.
41. Zhao X, Duan D, Feng X, Chen Y, Sun Z, et al. (2012) Molecular cloning and expression analysis of common carp Cyprinus carpio tumor necrosis factor-a. Fish Sci 78: 1229-1236.
42. Kono T, Sakai T, Sakai M (2003) Molecular cloning and expression analysis of a novel caspase recruitment domain protein (CARD) in common carp Cyprinus carpio L. Gene 309: 57-64.
43. Campanella JJ, Bitincka L, Smalley J (2003) MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinformatics 4: 29.
44. Wang GL, Li JH, Zou PF, Xie HX, Huang B, et al. (2012) Expression pattern, promoter activity and bactericidal property of beta-defensin from the mandarin fish Siniperca chuatsi. Fish Shellfish Immunol 33: 522-531.
45. Gao D, Xu Z, Zhang X, Zhu C, Wang Y, et al. (2013) Cadmium triggers kidney cell apoptosis of purse red common carp (Cyprinus carpio) without caspase-8 activation. Dev Comp Immunol 41: 728-737.
46. Bin Q, Rao H, Hu JN, Liu R, Fan YW, et al. (2013) The caspase pathway of linoelaidic acid (9t, 12t-c18:2)-induced apoptosis in human umbilical vein endothelial cells. Lipids 48: 115-126.
47. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
48. Gao D, Xu Z, Zhang X, Wang H, Wang Y, et al. (2013) Molecular cloning, immunohistochemical localization, characterization and expression analysis of caspase-9 from the purse red common carp (Cyprinus carpio) exposed to cadmium. Aquat Toxicol 142-143: 53-62.
49. Hossain S, Liu HN, Nguyen M, Shore G, Almazan G (2009) Cadmium exposure induces mitochondria-dependent apoptosis in oligodendrocytes. Neurotoxicology 30: 544-554.
50. Lavrik IN (2010) Systems biology of apoptosis signaling networks. Curr Opin Biotechnol 21: 551-555.
51. Eimon PM, Ashkenazi A (2010) The zebrafish as a model organism for the study of apoptosis. Apoptosis 15: 331-349.
52. Sakamaki K, Satou Y (2009) Caspases: evolutionary aspects of their functions in vertebrates. J Fish Biol 74: 727-753.
53. Boatright KM, Salvesen GS (2003) Mechanisms of caspase activation. Curr Opin Cell Biol 15: 725-731.
54. Kim S, Cheon HS, Kim SY, Juhnn YS, Kim YY (2013) Cadmium induces neuronal cell death through reactive oxygen species activated by GADD153. BMC Cell Biol 14: 4.
55. Li Y, Lim SC (2007) Cadmium-induced apoptosis of hepatocytes is not associated with death receptor-related caspase-dependent pathways in the rat. Environ Toxicol Pharmacol 24: 231-238.
56. Kim J, Sharma RP (2006) Cadmium-induced apoptosis in murine macrophages is antagonized by antioxidants and caspase inhibitors. J Toxicol Environ Health A 69: 1181-1201.
57. Kondera E, Lugowska K, Sarnowski P (2013) High affinity of cadmium and copper to head kidney of common carp (Cyprinus carpio L.). Fish Physiol Biochem: DOI: 10.1007/s10695-013-9819-1.
58. Razo-Estrada AC, García-Medina S, Madrigal-Bujaidar E, Gómez-Oliván LM, Galar-Martínez M (2013) Aluminum-Induced Oxidative Stress and Apoptosis in Liver of the Common Carp, Cyprinus carpio. Water, Air, Soil Pollut 224: 1-9.
59. García-Medina S, Angélica Núñez-Betancourt J, Lucero García-Medina A, Galar-Martínez M, Neri-Cruz N, et al. (2013) The relationship of cytotoxic and genotoxic damage with blood aluminum levels and oxidative stress induced by this metal in common carp (Cyprinus carpio) erythrocytes. Ecotoxicol Environ Saf 96: 191-197.
60. Cao J, Chen J, Wang J, Jia R, Xue W, et al. (2013) Effects of fluoride on liver apoptosis and Bcl-2, Bax protein expression in freshwater teleost, Cyprinus carpio. Chemosphere 91: 1203-1212.
61. Bownik A, Rymuszka A, Sieroslawska A, Skowronski T (2012) Anatoxin-a induces apoptosis of leukocytes and decreases the proliferative ability of lymphocytes of common carp (Cyprinus carpio L.) in vitro. Pol J Vet Sci 15: 531-535.
62. Poon WL, Hung CY, Nakano K, Randall DJ (2007) An in vivo study of common carp (Cyprinus carpio L.) liver during prolonged hypoxia. Comp Biochem Physiol Part D Genomics Proteomics 2: 295-302.
63. Fujiwara Y, Lee J-Y, Tokumoto M, Satoh M (2012) Cadmium Renal Toxicity via Apoptotic Pathways. Biol Pharm Bull 35: 1892-1897.
64. Vaculova A, Zhivotovsky B (2008) Caspases: Determination of their activities in apoptotic cells. In: KhosraviFar R, Zakeri Z, Lockshin RA, Piacentini M, editors. Programmed Cell Death, General Principles for Studying Cell Death, Pt A. San Diego: Elsevier Academic Press Inc. pp. 157-181.
65. Peluffo MC, Young KA, Stouffer RL (2005) Dynamic expression of caspase-2, - 3, -8, and -9 proteins and enzyme activity, but not messenger ribonucleic acid, in the monkey corpus luteum during the menstrual cycle. J Clin Endocrinol Metab 90: 2327-2335.
66. Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35: 495-516.
67. Kondera E, Witeska M (2013) Cadmium and copper reduce hematopoietic potential in common carp (Cyprinus carpio L.) head kidney. Fish Physiol Biochem 39: 755-764.
68. Herranz L, Teba F, Martin R, Ingelmo I, Gomez V, et al. (2010) Quantitative changes in rat seminiferous epithelium after chronic administration of low doses of cadmium and zinc: A stereological study. Open Androl J 2: 27-36.
69. Mazumder S, Plesca D, Almasan A (2008) Caspase-3 activation is a critical determinant of genotoxic stress-induced apoptosis. In: Mor G, Alvero AB, editors. Methods Mol Biol. pp. 13-21.