Transcriptomic Analyses of Sexual Dimorphism of the Zebrafish Liver and the Effect of Sex Hormones

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Zheng, Weiling ^a   Xu, Hongyan ^a   Lam, Siew Hong ^a   Luo, Huaien ^b   Karuturi, R Krishna Murthy ^b   Gong, Zhiyuan ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b GENOME INSTITUTE OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

11 OXOTESTOSTERONE; ESTRADIOL; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; LIVER X RECEPTOR; MYC PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; RETINOID X RECEPTOR; STAT4 PROTEIN; VITELLOGENIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CHOLESTEROL METABOLISM; CONTROLLED STUDY; FEMALE; GENETIC ANALYSIS; GLUCOSE METABOLISM; HIGH THROUGHPUT SEQUENCING; HORMONE ACTION; HORMONE RESPONSE; HORMONE SENSITIVITY; LIPID TRANSPORT; LIVER PARENCHYMA; MALE; METABOLIC REGULATION; NONHUMAN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RNA SEQUENCE; RNA TRANSLATION; SERIAL ANALYSIS OF GENE EXPRESSION; SEX DIFFERENCE; SEX HORMONE DETERMINATION; SPAWNING; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; XENOBIOTIC METABOLISM; ZEBRA FISH;

ANIMALS; FEMALE; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; GONADAL STEROID HORMONES; HUMANS; LIVER; MALE; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; SEX CHARACTERISTICS; XENOBIOTICS; ZEBRAFISH;

ANIMALIA; DANIO RERIO;

EID: 84872594090     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053562     Document Type: Article

References (78)

1. Yang X, Schadt EE, Wang S, Wang H, Arnold AP, et al. (2006) Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res 16: 995-1004.
2. Cinaroglu A, Gao C, Imrie D, Sadler KC (2011) Activating transcription factor 6 plays protective and pathological roles in steatosis due to endoplasmic reticulum stress in zebrafish. Hepatology.
3. Howarth DL, Passeri M, Sadler KC, (2011) Drinks like a fish: using zebrafish to understand alcoholic liver disease. Alcohol Clin Exp Res 35: 826-829.
4. Gao H, Wang Y, Wegierski T, Skouloudaki K, Putz M, et al. (2010) PRKCSH/80K-H, the protein mutated in polycystic liver disease, protects polycystin-2/TRPP2 against HERP-mediated degradation. Hum Mol Genet 19: 16-24.
5. Ung CY, Lam SH, Gong ZY, (2009) Comparative Transcriptome Analyses Revealed Conserved Biological and Transcription Factor Target Modules Between the Zebrafish and Human Tumors. Zebrafish 6: 425-431.
6. Lam SH, Gong Z, (2006) Modeling liver cancer using zebrafish: a comparative oncogenomics approach. Cell Cycle 5: 573-577.
7. Lam SH, Wu YL, Vega VB, Miller LD, Spitsbergen J, et al. (2006) Conservation of gene expression signatures between zebrafish and human liver tumors and tumor progression. Nat Biotechnol 24: 73-75.
8. Li Z, Huang X, Zhan H, Zeng Z, Li C, et al. (2011) Inducible and repressable oncogene-addicted hepatocellular carcinoma in Tet-on xmrk transgenic zebrafish. J Hepatol 56: 419-425.
9. Nguyen AT, Emelyanov A, Koh CH, Spitsbergen JM, Lam SH, et al. (2011) A high level of liver-specific expression of oncogenic Kras(V12) drives robust liver tumorigenesis in transgenic zebrafish. Dis Model Mech 4: 801-813.
10. Nguyen AT, Emelyanov A, Koh CH, Spitsbergen JM, Parinov S, et al. (2012) An inducible kras(V12) transgenic zebrafish model for liver tumorigenesis and chemical drug screening. Dis Model Mech 5: 63-72.
11. Li Z, Zheng W, Wang Z, Zeng Z, Zhan H, et al. (2012) An inducible Myc zebrafish liver tumor model revealed conserved Myc signatures with mammalian liver tumors. Disease models & mechanisms.
12. Curado S, Stainier DY, (2010) deLiver'in regeneration: injury response and development. Semin Liver Dis 30: 288-295.
13. Curado S, Ober EA, Walsh S, Cortes-Hernandez P, Verkade H, et al. (2010) The mitochondrial import gene tomm22 is specifically required for hepatocyte survival and provides a liver regeneration model. Dis Model Mech 3: 486-495.
14. Ung CY, Lam SH, Hlaing MM, Winata CL, Korzh S, et al. (2010) Mercury-induced hepatotoxicity in zebrafish: in vivo mechanistic insights from transcriptome analysis, phenotype anchoring and targeted gene expression validation. BMC Genomics 11: 212.
15. Lam SH, Mathavan S, Tong Y, Li H, Karuturi RK, et al. (2008) Zebrafish whole-adult-organism chemogenomics for large-scale predictive and discovery chemical biology. PLoS Genet 4: e1000121.
16. Wen C, Zhang Z, Ma W, Xu M, Wen Z, et al. (2005) Genome-wide identification of female-enriched genes in zebrafish. Dev Dyn 232: 171-179.
17. Small CM, Carney GE, Mo Q, Vannucci M, Jones AG, (2009) A microarray analysis of sex- and gonad-biased gene expression in the zebrafish: evidence for masculinization of the transcriptome. BMC Genomics 10: 579.
18. Zeng S, Gong Z, (2002) Expressed sequence tag analysis of expression profiles of zebrafish testis and ovary. Gene 294: 45-53.
19. Li Y, Chia JM, Bartfai R, Christoffels A, Yue GH, et al. (2004) Comparative analysis of the testis and ovary transcriptomes in zebrafish by combining experimental and computational tools. Comp Funct Genomics 5: 403-418.
20. Sreenivasan R, Cai M, Bartfai R, Wang X, Christoffels A, et al. (2008) Transcriptomic analyses reveal novel genes with sexually dimorphic expression in the zebrafish gonad and brain. PLoS One 3: e1791.
21. Santos EM, Kille P, Workman VL, Paull GC, Tyler CR, (2008) Sexually dimorphic gene expression in the brains of mature zebrafish. Comp Biochem Physiol A Mol Integr Physiol 149: 314-324.
22. Davis LK, Pierce AL, Hiramatsu N, Sullivan CV, Hirano T, et al. (2008) Gender-specific expression of multiple estrogen receptors, growth hormone receptors, insulin-like growth factors and vitellogenins, and effects of 17 beta-estradiol in the male tilapia (Oreochromis mossambicus). Gen Comp Endocrinol 156: 544-551.
23. Taboada X, Robledo D, Del Palacio L, Rodeiro A, Felip A, et al. (2012) Comparative expression analysis in mature gonads, liver and brain of turbot (Scophthalmus maximus) by cDNA-AFLPS. Gene 492: 250-261.
24. Robison BD, Drew RE, Murdoch GK, Powell M, Rodnick KJ, et al. (2008) Sexual dimorphism in hepatic gene expression and the response to dietary carbohydrate manipulation in the zebrafish (Danio rerio). Comp Biochem Physiol Part D Genomics Proteomics 3: 141-154.
25. Kling P, Norman A, Andersson PL, Norrgren L, Forlin L, (2008) Gender-specific proteomic responses in zebrafish liver following exposure to a selected mixture of brominated flame retardants. Ecotoxicol Environ Saf 71: 319-327.
26. Zhang W, Zhang Y, Zhang H, Wang J, Cui R, et al. (2012) Sex differences in transcriptional expression of FABPs in zebrafish liver after chronic perfluorononanoic acid exposure. Environ Sci Technol 46: 5175-5182.
27. Roy AK, Chatterjee B, (1983) Sexual dimorphism in the liver. Annu Rev Physiol 45: 37-50.
28. Westerfield M (2000) The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio). University of Oregon Press, Eugene.
29. Hallare A, Nagel K, Kohler HR, Triebskorn R, (2006) Comparative embryotoxicity and proteotoxicity of three carrier solvents to zebrafish (Danio rerio) embryos. Ecotoxicology and environmental safety 63: 378-388.
30. Hashimoto S, Qu W, Ahsan B, Ogoshi K, Sasaki A, et al. (2009) High-resolution analysis of the 5′-end transcriptome using a next generation DNA sequencer. PLoS One 4: e4108.
31. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
32. Robinson MD, Smyth GK, (2007) Moderated statistical tests for assessing differences in tag abundance. Bioinformatics 23: 2881-2887.
33. Robinson MD, Smyth GK, (2008) Small-sample estimation of negative binomial dispersion, with applications to SAGE data. Biostatistics 9: 321-332.
34. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
35. Baker ME, (1988) Is vitellogenin an ancestor of apolipoprotein B-100 of human low-density lipoprotein and human lipoprotein lipase? Biochem J 255: 1057-1060.
36. Li ZJ, Zhang SC, Zhang J, Liu M, Liu ZH, (2009) Vitellogenin is a cidal factor capable of killing bacteria via interaction with lipopolysaccharide and lipoteichoic acid. Molecular Immunology 46: 3232-3239.
37. Liu X, Wang H, Gong Z, (2006) Tandem-repeated Zebrafish zp3 genes possess oocyte-specific promoters and are insensitive to estrogen induction. Biol Reprod 74: 1016-1025.
38. Cheng W, Guo L, Zhang Z, Soo HM, Wen C, et al. (2006) HNF factors form a network to regulate liver-enriched genes in zebrafish. Dev Biol 294: 482-496.
39. Groh KJ, Nesatyy VJ, Segner H, Eggen RI, Suter MJ, (2011) Global proteomics analysis of testis and ovary in adult zebrafish (Danio rerio). Fish Physiol Biochem 37: 619-647.
40. Levi L, Pekarski I, Gutman E, Fortina P, Hyslop T, et al. (2009) Revealing genes associated with vitellogenesis in the liver of the zebrafish (Danio rerio) by transcriptome profiling. BMC genomics 10: 141.
41. Holth TF, Nourizadeh-Lillabadi R, Blaesbjerg M, Grung M, Holbech H, et al. (2008) Differential gene expression and biomarkers in zebrafish (Danio rerio) following exposure to produced water components. Aquat Toxicol 90: 277-291.
42. Knoll-Gellida A, Andre M, Gattegno T, Forgue J, Admon A, et al. (2006) Molecular phenotype of zebrafish ovarian follicle by serial analysis of gene expression and proteomic profiling, and comparison with the transcriptomes of other animals. BMC Genomics 7: 46.
43. Correale J, Fiol M, (2011) Chitinase effects on immune cell response in neuromyelitis optica and multiple sclerosis. Mult Scler 17: 521-531.
44. Zhao C, Dahlman-Wright K, (2010) Liver X receptor in cholesterol metabolism. J Endocrinol 204: 233-240.
45. Zhao S, Li R, Li Y, Chen W, Zhang Y, et al. (2012) Roles of vitamin A status and retinoids in glucose and fatty acid metabolism. Biochem Cell Biol 90: 142-152.
46. Desvergne B, Michalik L, Wahli W, (2006) Transcriptional regulation of metabolism. Physiol Rev 86: 465-514.
47. Yafang L, Qiong W, Yue R, Xiaoming X, Lina Y, et al. (2011) Role of Estrogen Receptor-alpha in the Regulation of Claudin-6 Expression in Breast Cancer Cells. J Breast Cancer 14: 20-27.
48. Waxman DJ, Holloway MG, (2009) Sex differences in the expression of hepatic drug metabolizing enzymes. Mol Pharmacol 76: 215-228.
49. Mode A, Gustafsson JA, (2006) Sex and the liver- a journey through five decades. Drug Metab Rev 38: 197-207.
50. Wang-Buhler JL, Lee SJ, Chung WG, Stevens JF, Tseng HP, et al. (2005) CYP2K6 from zebrafish (Danio rerio): cloning, mapping, developmental/tissue expression, and aflatoxin B1 activation by baculovirus expressed enzyme. Comp Biochem Physiol C Toxicol Pharmacol 140: 207-219.
51. Troxel CM, Reddy AP, O'Neal PE, Hendricks JD, Bailey GS, (1997) In vivo aflatoxin B1 metabolism and hepatic DNA adduction in zebrafish (Danio rerio). Toxicol Appl Pharmacol 143: 213-220.
52. van Riggelen J, Yetil A, Felsher DW, (2010) MYC as a regulator of ribosome biogenesis and protein synthesis. Nat Rev Cancer 10: 301-309.
53. Shang Y, Hu X, DiRenzo J, Lazar MA, Brown M, (2000) Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103: 843-852.
54. Shang Y, Brown M, (2002) Molecular determinants for the tissue specificity of SERMs. Science 295: 2465-2468.
55. Wang C, Mayer JA, Mazumdar A, Fertuck K, Kim H, et al. (2011) Estrogen induces c-myc gene expression via an upstream enhancer activated by the estrogen receptor and the AP-1 transcription factor. Mol Endocrinol 25: 1527-1538.
56. Wolfrum C, Stoffel M, (2006) Coactivation of Foxa2 through Pgc-1beta promotes liver fatty acid oxidation and triglyceride/VLDL secretion. Cell Metab 3: 99-110.
57. Handschin C, Spiegelman BM, (2006) Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev 27: 728-735.
58. Gao M, Wang J, Lu N, Fang F, Liu J, et al. (2011) Mitogen-activated protein kinase kinases promote mitochondrial biogenesis in part through inducing peroxisome proliferator-activated receptor gamma coactivator-1beta expression. Biochim Biophys Acta 1813: 1239-1244.
59. Dell H, Hadzopoulou-Cladaras M, (1999) CREB-binding protein is a transcriptional coactivator for hepatocyte nuclear factor-4 and enhances apolipoprotein gene expression. J Biol Chem 274: 9013-9021.
60. Stoffel M, Duncan SA, (1997) The maturity-onset diabetes of the young (MODY1) transcription factor HNF4alpha regulates expression of genes required for glucose transport and metabolism. Proc Natl Acad Sci U S A 94: 13209-13214.
61. Wiwi CA, Gupte M, Waxman DJ, (2004) Sexually dimorphic P450 gene expression in liver-specific hepatocyte nuclear factor 4alpha-deficient mice. Mol Endocrinol 18: 1975-1987.
62. Gao B, (2005) Cytokines, STATs and liver disease. Cell Mol Immunol 2: 92-100.
63. Lam SH, Lee SG, Lin CY, Thomsen JS, Fu PY, et al. (2011) Molecular conservation of estrogen-response associated with cell cycle regulation, hormonal carcinogenesis and cancer in zebrafish and human cancer cell lines. BMC medical genomics 4: 41.
64. Goetz FW, Rise ML, Rise M, Goetz GW, Binkowski F, et al. (2009) Stimulation of growth and changes in the hepatic transcriptome by 17beta-estradiol in the yellow perch (Perca flavescens). Physiol Genomics 38: 261-280.
65. Pham CH, Park KS, Kim BC, Kim HN, Gu MB, (2011) Construction and characterization of Japanese medaka (Oryzias latipes) hepatic cDNA library and its implementation to biomarker screening in aquatic toxicology. Aquat Toxicol 105: 569-575.
66. Hoffmann JL, Thomason RG, Lee DM, Brill JL, Price BB, et al. (2008) Hepatic gene expression profiling using GeneChips in zebrafish exposed to 17alpha-methyldihydrotestosterone. Aquat Toxicol 87: 69-80.
67. Moens LN, van der Ven K, Van Remortel P, Del-Favero J, De Coen WM, (2007) Gene expression analysis of estrogenic compounds in the liver of common carp (Cyprinus carpio) using a custom cDNA microarray. J Biochem Mol Toxicol 21: 299-311.
68. Hook SE, Skillman AD, Small JA, Schultz IR, (2006) Gene expression patterns in rainbow trout, Oncorhynchus mykiss, exposed to a suite of model toxicants. Aquat Toxicol 77: 372-385.
69. Ruggeri B, Ubaldi M, Lourdusamy A, Soverchia L, Ciccocioppo R, et al. (2008) Variation of the genetic expression pattern after exposure to estradiol-17beta and 4-nonylphenol in male zebrafish (Danio rerio). General and comparative endocrinology 158: 138-144.
70. Kausch U, Alberti M, Haindl S, Budczies J, Hock B, (2008) Biomarkers for exposure to estrogenic compounds: gene expression analysis in zebrafish (Danio rerio). Environmental toxicology 23: 15-24.
71. Wang H, Tan JT, Emelyanov A, Korzh V, Gong Z, (2005) Hepatic and extrahepatic expression of vitellogenin genes in the zebrafish, Danio rerio. Gene 356: 91-100.
72. Tong Y, Shan T, Poh YK, Yan T, Wang H, et al. (2004) Molecular cloning of zebrafish and medaka vitellogenin genes and comparison of their expression in response to 17beta-estradiol. Gene 328: 25-36.
73. Rogers AB, Boutin SR, Whary MT, Sundina N, Ge Z, et al. (2004) Progression of chronic hepatitis and preneoplasia in Helicobacter hepaticus-infected A/JCr mice. Toxicol Pathol 32: 668-677.
74. Deaciuc IV, Doherty DE, Burikhanov R, Lee EY, Stromberg AJ, et al. (2004) Large-scale gene profiling of the liver in a mouse model of chronic, intragastric ethanol infusion. J Hepatol 40: 219-227.
75. Tan X, Behari J, Cieply B, Michalopoulos GK, Monga SP, (2006) Conditional deletion of beta-catenin reveals its role in liver growth and regeneration. Gastroenterology 131: 1561-1572.
76. Weng Y, DiRusso CC, Reilly AA, Black PN, Ding X, (2005) Hepatic gene expression changes in mouse models with liver-specific deletion or global suppression of the NADPH-cytochrome P450 reductase gene. Mechanistic implications for the regulation of microsomal cytochrome P450 and the fatty liver phenotype. J Biol Chem 280: 31686-31698.
77. Rogers AB, Theve EJ, Feng Y, Fry RC, Taghizadeh K, et al. (2007) Hepatocellular carcinoma associated with liver-gender disruption in male mice. Cancer Res 67: 11536-11546.
78. Sternberg EM, Chrousos GP, Wilder RL, Gold PW, (1992) The stress response and the regulation of inflammatory disease. Ann Intern Med 117: 854-866.