Skip to main content

Challenges of Endocrine Disruption and Cardiac Development

  • Chapter
  • First Online:
Development and Environment

Abstract

The endocrine system plays a crucial role in the survival of animals. It regulates many signaling processes that control the cardiovascular, immune, reproductive, and central nervous systems. In addition to its role in maintaining the functions of major organ systems, signaling by the endocrine system is critical for normal development. For example, estrogen signaling has been shown to regulate cellular physiology by influencing its proliferation rate. With the diverse array of pathways that the endocrine system regulates, disruption by exogenous agents can impair vital functions, not just at the cellular and organismal levels but also at the population level. The integrated role of various biological systems and the interaction between organs can make it difficult to assess the effects of endocrine-disrupting compounds (EDCs). Adding to the challenges of studying the effects of EDCs is the complex series of signaling events that occur in a precise spatiotemporal manner during embryogenesis. However, using model organisms with a well-characterized developmental pattern such as zebrafish can facilitate the study of EDCs on physiological endpoints with apical relevance, such as cardiovascular development. Consequently, this review will focus on the developmental challenge of EDC exposure on cardiac development in aquatic organisms.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abney TO (1999) The potential roles of estrogens in regulating Leydig cell development and function: a review. Steroids 64(9):610–617

    CAS  PubMed  Google Scholar 

  • Albanito L, Madeo A, Lappano R, Vivacqua A, Rago V, Carpino A, Oprea TI, Prossnitz ER, Musti AM, Andò S, Maggiolini M (2007) G protein-coupled receptor 30 (GPR30) mediates gene expression changes and growth response to 17beta-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Res 67(4):1859–1866

    CAS  PubMed  Google Scholar 

  • Andersson S, Geissler WM, Wu L, Davis DL, Grumbach MM, New MI, Schwarz HP, Blethen SL, Mendonca BB, Bloise W, Witchel SF, Cutler GB Jr, Griffin JE, Wilson JD, Russel DW (1996) Molecular genetics and pathophysiology of 17 beta-hydroxysteroid dehydrogenase 3 deficiency. J Clin Endocrinol Metab 81(1):130–136

    CAS  PubMed  Google Scholar 

  • Antkiewicz DS, Peterson RE, Heideman W (2006) Blocking expression of AHR2 and ARNT1 in zebrafish larvae protects against cardiac toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Sci 94(1):175–182

    CAS  PubMed  Google Scholar 

  • Aronica SM, Kraus WL, Katzenellenbogen BS (1994) Estrogen action via the cAMP signaling pathway: stimulation of adenylate cyclase and cAMP-regulated gene transcription. Proc Natl Acad Sci U S A 91(18):8517–8521

    CAS  PubMed  PubMed Central  Google Scholar 

  • Auman HJ, Coleman H, Riley HE, Olale F, Tsai HJ, Yelon D (2007) Functional modulation of cardiac form through regionally confined cell shape changes. PLoS Biol 5(3):e53

    PubMed  PubMed Central  Google Scholar 

  • Baird DT, Swanston IA, McNeilly AS (1981) Secretion of androgens and estrogens by the preovulatory follicle in the ewe. Biol Reprod 24:1013–1025

    CAS  PubMed  Google Scholar 

  • Bakkers J (2011) Zebrafish as a model to study cardiac development and human cardiac disease. Cardiovasc Res 91(2):279–288

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ball JS, Stedman DB, Hillegass JM, Zhang CX, Panzica-Kelly J, Coburn A, Enright BP, Tornesi B, Amouzadeh HR, Hetheridge M, Gustafson AL, Augustine-Rauch KA (2014) Fishing for teratogens: a consortium effort for a harmonized zebrafish developmental toxicology assay. Toxicol Sci 139(1):210–219

    CAS  PubMed  Google Scholar 

  • Beis D, Bartman T, Jin SW, Scott IC, D'Amico LA, Ober EA, Verkade H, Frantsve J, Field HA, Wehman A, Baier H, Tallafuss A, Bally-Cuif L, Chen JN, Stainier DY, Jungblut B (2005) Genetic and cellular analyses of zebrafish atrioventricular cushion and valve development. Development 132(18):4193–4204

    CAS  PubMed  Google Scholar 

  • Benten WP, Lieberherr M, Stamm O, Wrehlke C, Guo Z, Wunderlich F (1999) Testosterone signaling through internalizable surface receptors in androgen receptor-free macrophages. Mol Biol Cell 10(10):3113–3123

    CAS  PubMed  PubMed Central  Google Scholar 

  • Biondi B, Palmieri EA, Lombardi G, Fazio S (2002) Effects of thyroid hormone on cardiac function: the relative importance of heart rate, loading conditions, and myocardial contractility in the regulation of cardiac performance in human hyperthyroidism. J Clin Endocrinol Metab 87(3):968–974

    CAS  PubMed  Google Scholar 

  • Bopassa JC, Eghbali M, Toro L, Stefani E (2010) A novel estrogen receptor GPER inhibits mitochondria permeability transition pore opening and protects the heart against ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 298(1):16–23

    Google Scholar 

  • Breen JJ, Hickok NJ, Guff JA (1997) The rat TSH gene contains distinct response elements for regulation by retinoids and thyroid hormone. Mol Cell Endocrinol 131:137–146

    CAS  PubMed  Google Scholar 

  • Brent GA (1994) The molecular basis of thyroid hormone action. N Engl J Med 331(13):847–853

    CAS  PubMed  Google Scholar 

  • Brinkmann AO, Leemborg FG, Roodnat EM, De Jong FH, Van der Molen HJ (1980) A specific action of estradiol on enzymes involved in testicular steroidogenesis. Biol Reprod 23(4):801–809

    CAS  PubMed  Google Scholar 

  • Brix K, Herzog V (1994) Extrathyroidal release of thyroid hormones from thyroglobulin by J774 mouse macrophages. J Clin Invest 93(4):1388–1396

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bussmann J, Bakkers J, Schulte-Merker S (2007) Early endocardial morphogenesis requires Scl/Tal1. PLoS Genet 3(8):e140

    PubMed  PubMed Central  Google Scholar 

  • Cagnacci A, Soldani R, Puccini E, Fioretti P, Melis GB (1992) Lipid-independent therapeutic properties of transdermal 17 B-estradiol on cardiovascular diseases. Acta Obstet Gynecol Scand 71(8):639–641

    CAS  PubMed  Google Scholar 

  • Campbell BK, Baird DT, Webb R (1998) Effects of dose of LH on androgen production and luteinization of ovine theca cells cultured in a serum-free system. J Reprod Fertil 112(1):69–77

    CAS  PubMed  Google Scholar 

  • Carney SA, Chen J, Burns CG, Xiong KM, Peterson RE, Heideman W (2006) Aryl hydrocarbon receptor activation produces heart-specific transcriptional and toxic responses in developing zebrafish. Mol Pharmacol 70(2):549–561

    CAS  PubMed  Google Scholar 

  • Carney SA, Peterson RE, Heideman W (2004) 2,3,7,8-Tetrachlorodibenzo-p-dioxin activation of the aryl hydrocarbon receptor/aryl hydrocarbon receptor nuclear translocator pathway causes developmental toxicity through a CYP1A-independent mechanism in zebrafish. Mol Pharmacol 66(3):512–521

    CAS  PubMed  Google Scholar 

  • Carpenter G, Cohen S (1979) Epidermal growth factor. Annu Rev Biochem 48:193–216

    CAS  PubMed  Google Scholar 

  • Castro-Rivera E, Samudio I, Safe S (2001) Estrogen regulation of cyclin D1 gene expression in ZR-75 breast cancer cells involves multiple enhancer elements. J Biol Chem 276(33):30853–30861

    CAS  PubMed  Google Scholar 

  • Catterall WA (1991) Functional subunit structure of voltage-gated calcium channels. Science 253(5027):1499–1500

    CAS  PubMed  Google Scholar 

  • Ceballos G, Figueroa L, Rubio I, Gallo G, Garcia A, Martinez A, Yañez R, Perez J, Morato T, Chamorro G (1999) Acute and nongenomic effects of testosterone on isolated and perfused rat heart. J Cardiovasc Pharmacol 33(5):691–697

    CAS  PubMed  Google Scholar 

  • Chambliss KL, Shaul PW (2002) Estrogen modulation of endothelial nitric oxide synthase. Endocr Rev 23(5):665–686

    CAS  PubMed  Google Scholar 

  • Chandrasekar G, Archer A, Gustafsson JA, Andersson Lendahl M (2010) Levels of 17b-estradiol receptors expressed in embryonic and adult zebrafish following in vivo treatment of natural or synthetic ligands. PLoS One 5(3):e9678

    PubMed  PubMed Central  Google Scholar 

  • Chang C, Saltzman A, Yeh S, Young W, Keller E, Lee HJ, Wang C, Mizokami A (1995) Androgen receptor: an overview. Crit Rev Eukaryot Gene Expr 5(2):97–125

    CAS  PubMed  Google Scholar 

  • Chang CS, Kokontis J, Liao ST (1988a) Molecular cloning of human and rat complementary DNA encoding androgen receptors. Science 240(4850):324–326

    CAS  PubMed  Google Scholar 

  • Chang CS, Kokontis J, Liao ST (1988b) Structural analysis of complementary DNA and amino acid sequences of human and rat androgen receptors. Proc Natl Acad Sci U S A 85(19):7211–7215

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen JN, Fishman MC (1996) Zebrafish tinman homolog demarcates the heart field and initiates myocardial differentiation. Development 122(12):3809–3816

    CAS  PubMed  Google Scholar 

  • Chen JN, Haffter P, Odenthal J, Vogelsang E, Brand M, van Eeden FJ, Furutani-Seiki M, Granato M, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, Kelsh RN, Mullins MC, Nüsslein-Volhard C (1996) Mutations affecting the cardiovascular system and other internal organs in zebrafish. Development 123:293–302

    CAS  PubMed  Google Scholar 

  • Chen JN, van Eeden FJ, Warren KS, Chin A, Nüsslein-Volhard C, Haffter P, Fishman MC (1997) Left-right pattern of cardiac BMP4 may drive asymmetry of the heart in zebrafish. Development 124(21):4373–4382

    CAS  PubMed  Google Scholar 

  • Cheng SY, Leonard JL, Davis PJ (2010) Molecular aspects of thyroid hormone actions. Endocr Rev 31(2):139–170

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chow MS (1995) Benefit/risk of estrogen therapy in cardiovascular disease: current knowledge and future challenges. J Clin Pharmacol 35(9 Suppl):11S–17S

    CAS  PubMed  Google Scholar 

  • Crisp TM, Clegg ED, Cooper RL, Wood WP, Anderson DG, Baetcke KP, Hoffmann JL, Morrow MS, Rodier DJ, Schaeffer JE, Touart LW, Zeeman MG, Patel YM (1998) Environmental endocrine disruption: an effects assessment and analysis. Environ Health Perspect 106(Suppl 1):11–56

    CAS  PubMed  PubMed Central  Google Scholar 

  • Danzi S, Klein I (2002) Thyroid hormone-regulated cardiac gene expression and cardiovascular disease. Thyroid 12(6):467–472

    CAS  PubMed  Google Scholar 

  • Datta SR, Brunet A, Greenberg ME (1999) Cellular survival: a play in three Akts. Genes Dev 13(22):2905–2927

    CAS  PubMed  Google Scholar 

  • Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91(2):231–241

    CAS  PubMed  Google Scholar 

  • Daub H, Weiss FU, Wallasch C, Ullrich A (1996) Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 379(6565):557–560

    CAS  PubMed  Google Scholar 

  • Davis PJ, Davis FB (2002) Nongenomic actions of thyroid hormone on the heart. Thyroid 12(6):459–466

    CAS  PubMed  Google Scholar 

  • De Jong FH (1988) Inhibin. Physiol Rev 68(2):555–607

    PubMed  Google Scholar 

  • De Pater E, Clijsters L, Marques SR, Lin YF, Garavito-Aguilar ZV, Yelon D, Bakkers J (2009) Distinct phases of cardiomyocyte differentiation regulate growth of the zebrafish heart. Development 136(10):1633–1641

    PubMed  PubMed Central  Google Scholar 

  • De Waal PP, Wang DS, Nijenhuis WA, Schulz RW, Bogerd J (2008) Functional characterization and expression analysis of the androgen receptor in zebrafish (Danio rerio) testis. Reproduction 136(2):225–234

    PubMed  Google Scholar 

  • Denison MS, Fisher JM, Whitlock JP Jr (1988a) Inducible, receptor-dependent protein-DNA interactions at a dioxin-responsive transcriptional enhancer. Proc Natl Acad Sci U S A 85(8):2528–2532

    CAS  PubMed  PubMed Central  Google Scholar 

  • Denison MS, Fisher JM, Whitlock JP Jr (1988b) The DNA recognition site for the dioxin-Ah receptor complex. nucleotide sequence and functional analysis. J Biol Chem 263(33):17221–17224

    CAS  PubMed  Google Scholar 

  • DeRosa C, Richter P, Pohl H, Jones DE (1998) Environmental exposures that affect the endocrine system: public health implications. J Toxicol Environ Health B Crit Rev 1(1):3–26

    CAS  PubMed  Google Scholar 

  • Deschamps AM, Murphy E (2009) Activation of a novel estrogen receptor, GPER, is cardioprotective in male and female rats. Am J Physiol Heart Circ Physiol 297(5):1806–1813

    Google Scholar 

  • Diamante G, Menjivar-Cervantes N, Leung MS, Volz DC, Schlenk D (2017) Contribution of G protein-coupled estrogen receptor 1 (GPER) to 17β-estradiol-induced developmental toxicity in zebrafish. Aquat Toxicol 186:180–187

    CAS  PubMed  Google Scholar 

  • Ding Q, Gros R, Limbird LE, Chorazyczewski J, Feldman RD (2009) Estradiol-mediated ERK phosphorylation and apoptosis in vascular smooth muscle cells requires GPR 30. Am J Physiol Cell Physiol 297(5):C1178–C1187

    CAS  PubMed  Google Scholar 

  • Driever W, Solnica-Krezel L, Schier AF, Neuhauss SC, Malicki J, Stemple DL, Stainier DY, Zwartkruis F, Abdelilah S, Rangini Z, Belak J, Boggs C (1996) A genetic screen for mutations affecting embryogenesis in zebrafish. Development 123:37–46

    CAS  Google Scholar 

  • Duan R, Porter W, Safe S (1998) Estrogen-induced c-fos protooncogene expression in MCF-7 human breast cancer cells: role of estrogen receptor Sp1 complex formation. Endocrinology 139(4):1981–1990

    CAS  PubMed  Google Scholar 

  • Duan Z, Zhu L, Zhu L, Kun Y, Zhu X (2008) Individual and joint toxic effects of pentachlorophenol and bisphenol A on the development of zebrafish (Danio rerio) embryo. Ecotoxicol Environ Saf 71(3):774–780

    CAS  PubMed  Google Scholar 

  • Dunn AD, Crutchfield HE, Dunn JT (1991) Proteolytic processing of thyroglobulin by extracts of thyroid lysosomes. Endocrinology 128(6):3073–3080

    CAS  PubMed  Google Scholar 

  • Estrada M, Espinosa A, Müller M, Jaimovich E (2003) Testosterone stimulates intracellular calcium release and mitogen-activated protein kinases via a G protein-coupled receptor in skeletal muscle cells. Endocrinology 144(8):3586–3597

    CAS  PubMed  Google Scholar 

  • Estrada M, Uhlen P, Ehrlich BE (2006a) Ca2+ oscillations induced by testosterone enhance neurite outgrowth. J Cell Sci 119(Pt 4):733–743

    CAS  PubMed  Google Scholar 

  • Estrada M, Varshney A, Ehrlich BE (2006b) Elevated testosterone induces apoptosis in neuronal cells. J Biol Chem 281(35):25492–25501

    CAS  PubMed  Google Scholar 

  • Everts ME, Verhoeven FA, Bezstarosti K, Moerings EP, Hennemann G, Visser TJ, Lamers JM (1996) Uptake of thyroid hormones in neonatal rat cardiac myocytes. Endocrinology 137(10):4235–4242

    CAS  PubMed  Google Scholar 

  • Filardo EJ, Quinn JA, Bland KI, Frackelton AR Jr (2000) Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol Endocrinol 14(10):1649–1660

    CAS  PubMed  Google Scholar 

  • Foradori CD, Weiser MJ, Handa RJ (2008) Non-genomic actions of androgens. Front Neuroendocrinol 29(2):169–181

    CAS  PubMed  Google Scholar 

  • Frye CA, Bo E, Calamandrei G, Calzà L, Dessì-Fulgheri F, Fernández M, Fusani L, Kah O, Kajta M, Le Page Y, Patisaul HB, Venerosi A, Wojtowicz AK, Panzica GC (2012) Endocrine disrupters: a review of some sources, effects, and mechanisms of actions on behaviour and neuroendocrine systems. J Neuroendocrinol 24(1):144–159

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fujisawa-Sehara A, Sogawa K, Yamane M, Fujii-Kuriyama Y (1987) Characterization of xenobiotic responsive elements upstream from the drug-metabolizing cytochrome P-450c gene: a similarity to glucocorticoid regulatory elements. Nucleic Acids Res 15(10):4179–4191

    CAS  PubMed  PubMed Central  Google Scholar 

  • Funakoshi T, Yanai A, Shinoda K, Kawano MM, Mizukami Y (2006) G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem Biophys Res Commun 346(3):904–910

    CAS  PubMed  Google Scholar 

  • Gao X, Wang HS (2014) Impact of bisphenol a on the cardiovascular system – epidemiological and experimental evidence and molecular mechanisms. Int J Environ Res Public Health 11(8):8399–8413

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garavito-Aguilar ZV, Riley HE, Yelon D (2010) Hand2 ensures an appropriate environment for cardiac fusion by limiting Fibronectin function. Development 137(19):3215–3220

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gaub MP, Bellard M, Scheuer I, Chambon P, Sassone-Corsi P (1990) Activation of the ovalbumin gene by the estrogen receptor involves the fos-jun complex. Cell 63(6):1267–1276

    CAS  PubMed  Google Scholar 

  • Gobinet J, Poujol N, Sultan C (2002) Molecular action of androgens. Mol Cell Endocrinol 198:15–24

    CAS  PubMed  Google Scholar 

  • Gonzalez FJ, Fernandez-Salguero P (1998) The aryl hydrocarbon receptor: studies using the AHR-null mice. Drug Metab Dispos 26(12):1194–1198

    CAS  PubMed  Google Scholar 

  • Goodale BC, Tilton SC, Corvi MM, Wilson GR, Janszen DB, Anderson KA, Waters KM, Tanguay RL (2013) Structurally distinct polycyclic aromatic hydrocarbons induce differential transcriptional responses in developing zebrafish. Toxicol Appl Pharmacol 272(3):656–670

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gregory SJ, Kaiser UB (2004) Regulation of gonadotropins by inhibin and activin. Semin Reprod Med 22(3):253–267

    CAS  PubMed  Google Scholar 

  • Gustafsson J, Pousette K (1975) Demonstration and partial characterization of cytosol receptors for testosterone. Biochemistry 14(14):3094–3101

    CAS  Google Scholar 

  • Haffter P, Granato M, Brand M, Mullins MC, Hammerschmidt M, Kane DA, Odenthal J, van Eeden FJ, Jiang YJ, Heisenberg CP, Kelsh RN, Furutani-Seiki M, Vogelsang E, Beuchle D, Schach U, Fabian C, Nüsslein-Volhard C (1996) The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 123:1–36

    CAS  PubMed  Google Scholar 

  • Hall JM, Couse JF, Korach KS (2001) The multifaceted mechanisms of estradiol and estrogen receptor signaling. J Biol Chem 276(40):36869–36872

    CAS  PubMed  Google Scholar 

  • Handley-Goldstone HM, Grow MW, Stegeman JJ (2005) Cardiovascular gene expression profiles of dioxin exposure in zebrafish embryos. Toxicol Sci 85(1):683–693

    CAS  PubMed  Google Scholar 

  • Hansson V, Weddington SC, Petrusz P, Ritzen EM, Nayfeh SN (1975) French FS (1975) FSH stimulation of testicular androgen binding protein (ABP): comparison of ABP response and ovarian augmentation. Endocrinology 97(2):469–473

    CAS  PubMed  Google Scholar 

  • Hartong R, Wang N, Kurokawa R, Lazar MA, Glass CK, Apriletti JW, Dillmann WH (1994) Delineation of three different thyroid hormone-response elements in promoter of rat sarcoplasmic reticulum Ca2+ATPase gene. Demonstration that retinoid X receptor binds 5′ to thyroid hormone receptor in response element 1. J Biol Chem 269(17):13021–13029

    CAS  PubMed  Google Scholar 

  • Hausenloy DJ, Yellon DM (2003) The mitochondrial permeability transition pore: its fundamental role in mediating cell death during ischaemia and reperfusion. J Mol Cell Cardiol 35(4):339–341

    CAS  PubMed  Google Scholar 

  • Heintz RA, Short JW, Rice SD (1999) Sensitivity of fish embryos to weathered crude oil: II. Increased mortality of pink salmon (Oncorhynchus gorbuscha) embryos incubating downstream from weathered Exxon Valdez crude oil. Environ Toxicol Chem 18(3):494–503

    CAS  Google Scholar 

  • Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, Tujague M, Ström A, Treuter E, Warner M, Gustafsson JA (2007) Estrogen receptors: how do they signal and what are their targets. Physiol Rev 87(3):905–931

    CAS  PubMed  Google Scholar 

  • Henry TR, Spitsbergen JM, Hornung MW, Abnet CC, Peterson RE (1997) Early life stage toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in zebrafish (Danio rerio). Toxicol Appl Pharmacol 142(1):56–68

    CAS  PubMed  Google Scholar 

  • Herzog V (1983) Transcytosis in thyroid follicle cells. J Cell Biol 97(3):607–617

    CAS  PubMed  Google Scholar 

  • Hiroi H, Christenson LK, Strauss JF (2004) Regulation of transcription of the steroidogenic acute regulatory protein (StAR) gene: temporal and spatial changes in transcription factor binding and histone modification. Mol Cell Endocrinol 215(1–2):119–126

    CAS  PubMed  Google Scholar 

  • Hiroi Y, Kim HH, Ying H, Furuya F, Huang Z, Simoncini T, Noma K, Ueki K, Nguyen NH, Scanlan TS, Moskowitz MA, Cheng SY, Liao JK (2006) Rapid nongenomic actions of thyroid hormone. Proc Natl Acad Sci U S A 103(38):14104–14109

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hornung MW, Spitsbergen JM, Peterson RE (1999) 2,3,7,8-Tetrachlorodibenzo-p-dioxin alters cardiovascular and craniofacial development and function in sac fry of rainbow trout (Oncorhynchus mykiss). Toxicol Sci 47(1):40–51

    CAS  PubMed  Google Scholar 

  • Hossain MS, Larsson A, Scherbak N, Olsson PE, Orban L (2008) Zebrafish androgen receptor: isolation, molecular, and biochemical characterization. Biol Reprod 78(2):361–369

    CAS  PubMed  Google Scholar 

  • Hsieh KP, Martin TF (1992) Thyrotropin-releasing hormone and gonadotropin-releasing hormone receptors activate phospholipase C by coupling to the guanosine triphosphate-binding proteins Gq and G11. Mol Endocrinol 6(10):1673–1681

    CAS  PubMed  Google Scholar 

  • Hu J, Zhang Z, Shen WJ, Azhar S (2010) Cellular cholesterol delivery, intracellular processing and utilization for biosynthesis of steroid hormones. Nutr Metab (Lond) 7:47

    Google Scholar 

  • Huttner IG, Trivedi G, Jacoby A, Mann SA, Vandenberg JI, Fatkin D (2013) A transgenic zebrafish model of a human cardiac sodium channel mutation exhibits bradycardia, conduction-system abnormalities and early death. J Mol Cell Cardiol 61:123–132

    CAS  PubMed  Google Scholar 

  • Incardona JP, Carls MG, Holland L, Linbo TL, Baldwin DH, Myers MS, Peck KA, Tagal M, Rice SD, Scholz NL (2015) Very low embryonic crude oil exposures cause lasting cardiac defects in salmon and herring. Sci Rep 5:13499

    PubMed  PubMed Central  Google Scholar 

  • Incardona JP, Carls MG, Teraoka H, Sloan CA, Collier TK, Scholz NL (2005) Aryl hydrocarbon receptor-independent toxicity of weathered crude oil during fish development. Environ Health Perspect 113(12):1755–1762

    CAS  PubMed  PubMed Central  Google Scholar 

  • Incardona JP, Collier TK, Scholz NL (2004) Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons. Toxicol Appl Pharmacol 196(2):191–205

    CAS  PubMed  Google Scholar 

  • Incardona JP, Day HL, Collier TK, Scholz NL (2006) Developmental toxicity of 4-ring polycyclic aromatic hydrocarbons in zebrafish is differentially dependent on AH receptor isoforms and hepatic cytochrome P4501A metabolism. Toxicol Appl Pharmacol 217(3):308–321

    CAS  PubMed  Google Scholar 

  • Incardona JP, Gardner LD, Linbo TL, Brown TL, Esbaugh AJ, Mager EM, Stieglitz JD, French BL, Labenia JS, Laetz CA, Tagal M, Sloan CA, Elizur A, Benetti DD, Grosell M, Block BA, Scholz NL (2014) Deepwater horizon crude oil impacts the developing hearts of large predatory pelagic fish. Proc Natl Acad Sci U S A 111(15):E1510–E1518

    CAS  PubMed  PubMed Central  Google Scholar 

  • Incardona JP, Linbo TL, Scholz NL (2011) Cardiac toxicity of 5-ring polycyclic aromatic hydrocarbons is differentially dependent on the aryl hydrocarbon receptor 2 isoform during zebrafish development. Toxicol Appl Pharmacol 257(2):242–249

    CAS  PubMed  Google Scholar 

  • Incardona JP, Swarts TL, Edmunds RC, Linbo TL, Aquilina-Beck A, Sloan CA, Gardner LD, Block BA, Scholz NL (2013) Exxon Valdez to Deepwater horizon: comparable toxicity of both crude oils to fish early life stages. Aquat Toxicol 142-143:303–316

    CAS  PubMed  Google Scholar 

  • Ingenbleek Y, Young V (1994) Transthyretin (prealbumin) in health and disease: nutritional implications. Annu Rev Nutr 14:495–533

    CAS  PubMed  Google Scholar 

  • Jayasinghe BS, Volz DC (2012) Aberrant ligand-induced activation of G protein-coupled estrogen receptor 1 (GPER) results in developmental malformations during vertebrate embryogenesis. Toxicol Sci 125(1):262–273

    CAS  PubMed  Google Scholar 

  • Jayasundara N, Van Tiem Garner L, Meyer JN, Erwin KN, Di Giulio RT (2015) AHR2-mediated transcriptomic responses underlying the synergistic cardiac developmental toxicity of PAHs. Toxicol Sci 143(2):469–481

    CAS  PubMed  Google Scholar 

  • Jensen EV (1962) On the mechanism of estrogen action. Perspect Biol Med 6:47–54

    CAS  PubMed  Google Scholar 

  • Jensen EV, Desombre ER (1973) Estrogen-receptor interaction: estrogenic hormones effect transformation of specific receptor proteins to a biologically active form. Science 182:126–134

    CAS  PubMed  Google Scholar 

  • Jensen EV, Suzuki T, Kawashima T, Stumpf WE, Jungblut PW, DeSombre ER (1968) A two-step mechanism for the interaction of estradiol with rat uterus. Proc Natl Acad Sci U S A 59(2):632–638

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jenster G, van der Korput HA, van Vroonhoven C, van der Kwast TH, Trapman J, Brinkmann AO (1991) Domains of the human androgen receptor involved in steroid binding, transcriptional activation, and subcellular localization. Mol Endocrinol 5(10):1396–1404

    CAS  PubMed  Google Scholar 

  • Johnson BD, Zheng W, Korach KS, Scheuer T, Catterall WA, Rubanyi GM (1997) Increased expression of the cardiac L-type calcium channel in estrogen receptor-deficient mice. J Gen Physiol 110(2):135–140

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kahaly GJ, Dillmann WH (2005) Thyroid hormone action in the heart. Endocr Rev 26(5):704–728

    CAS  PubMed  Google Scholar 

  • Kalla NR, Nisula BC, Menard R, Loriaux DL (1980) The effect of estradiol on Leydig cell testosterone biosynthesis. Endocrinology 106:35–39

    CAS  PubMed  Google Scholar 

  • Kaushik M, Sontineni SP, Hunter C (2010) Cardiovascular disease and androgens: a review. Int J Cardiol 142(1):8–14

    PubMed  Google Scholar 

  • Kayes-Wandover KM, White PC (2000) Steroidogenic enzyme gene expression in the human heart. J Clin Endocrinol Metab 85(7):2519–2525

    CAS  PubMed  Google Scholar 

  • Khan SA, Ball RB, Hendry WJ (1998) Effects of neonatal administration of diethylstilbestrol in male hamsters: disruption of reproductive function in adults after apparently normal pubertal development. Biol Reprod 58(1):137–142

    CAS  PubMed  Google Scholar 

  • Kim J, Wu Q, Zhang Y, Wiens KM, Huang Y, Rubin N, Shimada H, Handin RI, Chao MY, Tuan TL, Starnes VA, Lien CL (2010) PDGF signaling is required for epicardial function and blood vessel formation in regenerating zebrafish hearts. Proc Natl Acad Sci U S A 107(40):17206–17210

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim K, Barhoumi R, Burghardt R, Safe S (2005) Analysis of estrogen receptor {α}-Sp1 interactions in breast cancer cells by fluorescence resonance energy transfer. Mol Endocrinol 19(4):843–854

    CAS  PubMed  Google Scholar 

  • Kim PS, Arvan P (1991) Folding and assembly of newly synthesized thyroglobulin occurs in a pre-Golgi compartment. J Biol Chem 266(19):12412–12418

    CAS  PubMed  Google Scholar 

  • Kim PS, Arvan P (1993) Hormonal regulation of thyroglobulin export from the endoplasmic reticulum of cultured thyrocytes. J Biol Chem 268(7):4873–4879

    CAS  PubMed  Google Scholar 

  • Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203(3):253–310

    CAS  PubMed  Google Scholar 

  • Kimura N, Mizokami A, Oonuma T, Sasano H, Nagura H (1993) Immunocytochemical localization of androgen receptor with polyclonal antibody in paraffin-embedded human tissues. J Histochem Cytochem 41(5):671–678

    CAS  PubMed  Google Scholar 

  • Kishimoto Y, Lee KH, Zon L, Hammerschmidt M, Schulte-Merker S (1997) The molecular nature of zebrafish swirl: BMP2 function is essential during early dorsoventral patterning. Development 124(22):4457–4466

    CAS  PubMed  Google Scholar 

  • Kiss E, Jakab G, Kranias EG, Edes I (1994) Thyroid hormone-induced alterations in phospholamban protein expression: regulatory effects on sarcoplasmic reticulum Ca2+ transport and myocardial relaxation. Circ Res 75(2):245–251

    CAS  PubMed  Google Scholar 

  • Klein I, Danzi S (2007) Thyroid disease and the heart. Circulation 116(15):1725–1735

    PubMed  Google Scholar 

  • Klingenberg M (1958) Pigments of rat liver microsomes. Arch Biochem Biophys 75(2):376–386

    CAS  PubMed  Google Scholar 

  • Kostrouch Z, Bernier-Valentin F, Munari-Silem Y, Rajas F, Rabilloud R, Rousset B (1993) Thyroglobulin molecules internalized by thyrocytes are sorted in early endosomes and partially recycled back to the follicular lumen. Endocrinology 132(6):2645–2653

    CAS  PubMed  Google Scholar 

  • Kostrouch Z, Munari-Silem Y, Rajas F, Bernier-Valentin F, Rousset B (1991) Thyroglobulin internalized by thyrocytes passes through early and late endosomes. Endocrinology 129(4):2202–2211

    CAS  PubMed  Google Scholar 

  • Kuiper GG, Carlsson B, Grandien K, Enmark E, Häggblad J, Nilsson S, Gustafsson JA (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138(3):863–870

    CAS  PubMed  Google Scholar 

  • Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA (1996) Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci U S A 93(12):5925–5930

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kupperman E, An S, Osborne N, Waldron S, Stainier DY (2000) A sphingosine-1-phosphate receptor regulates cell migration during vertebrate heart development. Nature 406:192–195

    CAS  PubMed  Google Scholar 

  • Lam SH, Winata CL, Tong Y, Korzh S, Lim WS, Korzh V, Spitsbergen J, Mathavan S, Miller LD, Liu ET, Gong Z (2006) Transcriptome kinetics of arsenic-induced adaptive response in zebrafish liver. Physiol Genomics 27(3):351–361

    CAS  PubMed  Google Scholar 

  • Lang IA, Galloway TS, Scarlett A, Henley WE, Depledge M, Wallace RB, Melzer D (2008) Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA 300(11):1303–1310

    CAS  PubMed  Google Scholar 

  • Larsson DGJ, Adolfsson-Erici M, Parkkonen J, Pettersson M, Berg AH, Olsson PE, Förlin L (1999) Ethinyloestradiol – an undesired fish contraceptive? Aquat Toxicol 45(2–3):91–97

    CAS  Google Scholar 

  • Lebbe M, Woodruff TK (2013) Involvement of androgens in ovarian health and disease. Mol Hum Reprod 19(12):828–837

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee HJ, Chattopadhyay S, Gong EY, Ahn RS, Lee K (2003) Antiandrogenic effects of bisphenol A and nonylphenol on the function of androgen receptor. Toxicol Sci 75(1):40–46

    CAS  PubMed  Google Scholar 

  • Lepilina A, Coon AN, Kikuchi K, Holdway JE, Roberts RW, Burns CG, Poss KD (2006) A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127(3):607–619

    CAS  PubMed  Google Scholar 

  • Ling N, Ying SY, Ueno N, Shimasaki S, Esch F, Hotta M, Guillemin R (1986) Pituitary FSH is released by a heterodimer of the beta-subunits from the two forms of inhibin. Nature 321(6072):779–782

    CAS  PubMed  Google Scholar 

  • Lints TJ, Parsons LM, Hartley L, Lyons I, Harvey RP (1993) Nkx-2. 5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development 119(3):419–431

    CAS  PubMed  Google Scholar 

  • Liu J, Stainier DY (2010) Tbx5 and Bmp signaling are essential for proepicardium specification in zebrafish. Circ Res 106(12):1818–1828

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu MM, Albanese C, Anderson CM, Hilty K, Webb P, Uht RM, Price RH Jr, Pestell RG, Kushner PJ (2002) Opposing action of estrogen receptors alpha and beta on cyclin D1 gene expression. J Biol Chem 277(27):24353–24360

    CAS  PubMed  Google Scholar 

  • Liu PY, Death AK, Handelsman DJ (2003) Androgens and cardiovascular disease. Endocr Rev 24(3):313–340

    CAS  PubMed  Google Scholar 

  • Long Q, Meng A, Wang H, Jessen JR, Farrell MJ, Lin S (1997) GATA-1 expression pattern can be recapitulated in living transgenic zebrafish using GFP reporter gene. Development 124(20):4105–4111

    CAS  PubMed  Google Scholar 

  • Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O (1993) Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci U S A 90(23):11162–11166

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lund AK, Goens MB, Kanagy NL, Walker MK (2003) Cardiac hypertrophy in aryl hydrocarbon receptor null mice is correlated with elevated angiotensin II, endothelin-1, and mean arterial blood pressure. Toxicol Appl Pharmacol 193(2):177–187

    CAS  PubMed  Google Scholar 

  • Martinez-Arguelles DB, Papadopoulos V (2010) Epigenetic regulation of the expression of genes involved in steroid hormone biosynthesis and action. Steroids 75(7):467–476

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mathew LK, Sengupta S, Kawakami A, Andreasen EA, Löhr CV, Loynes CA, Renshaw SA, Peterson RT, Tanguay RL (2007) Unraveling tissue regeneration pathways using chemical genetics. J Biol Chem 282(48):35202–35210

    CAS  PubMed  Google Scholar 

  • Matthews J, Gustafsson JA (2006) Estrogen receptor and aryl hydrocarbon receptor signaling pathways. Nucl Recept Signal 4:e016

    PubMed  PubMed Central  Google Scholar 

  • Matthews J, Wihlén B, Thomsen J, Gustafsson JA (2005) Aryl hydrocarbon receptor-mediated transcription: ligand-dependent recruitment of estrogen receptor alpha to 2,3,7,8-tetrachlorodibenzo-p-dioxin-responsive promoters. Mol Cell Biol 25(13):5317–5328

    CAS  PubMed  PubMed Central  Google Scholar 

  • McFadden DG, Charité J, Richardson JA, Srivastava D, Firulli AB, Olson EN (2000) A GATA-dependent right ventricular enhancer controls dHAND transcription in the developing heart. Development 127(24):5331–5341

    CAS  PubMed  Google Scholar 

  • McKenna NJ, O’Malley BW (2002) Combinatorial control of gene expression by nuclear receptors and coregulators. Cell 108(4):465–474

    CAS  PubMed  Google Scholar 

  • Meachem SJ, McLachlan RI, de Kretser DM, Robertson DM, Wreford NG (1996) Neonatal exposure of rats to recombinant follicle stimulating hormone increases adult Sertoli and spermatogenic cell numbers. Biol Reprod 54(1):36–44

    CAS  PubMed  Google Scholar 

  • Mellon SH, Griffin LD (2002) Neurosteroids: biochemistry and clinical significance. Trends Endocrinol Metab 13(1):35–43

    CAS  PubMed  Google Scholar 

  • Mellström B, Naranjo JR (2001) Mechanisms of Ca(2+)-dependent transcription. Curr Opin Neurobiol 11(3):312–319

    PubMed  Google Scholar 

  • Melner MH, Abney TO (1980a) The direct effect of 17β-estradiol on LH-stimulated testosterone production in hypophysectomized rats. J Steroid Biochem 13(2):203–210

    CAS  PubMed  Google Scholar 

  • Melner MH, Abney TO (1980b) Depletion of the cytoplasmic estrogen receptor in gonadotropin-desensitized testes. Endocrinology 107(5):1620–1626

    CAS  PubMed  Google Scholar 

  • Melzer D, Rice NE, Lewis C, Henley WE, Galloway TS (2010) Association of urinary bisphenol a concentration with heart disease: evidence from NHANES 2003/06. PLoS One 5(1):e8673

    PubMed  PubMed Central  Google Scholar 

  • Mendelsohn ME, Karas RH (1999) The protective effects of estrogen on the cardiovascular system. N Engl J Med 340(23):1801–1811

    CAS  PubMed  Google Scholar 

  • Meyer MR, Haas E, Prossnitz ER, Barton M (2009) Non-genomic regulation of vascular cell function and growth by estrogen. Mol Cell Endocrinol 308(1–2):9–16

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer MR, Prossnitz ER, Barton M (2011) The G protein-coupled estrogen receptor GPER/GPR30 as a regulator of cardiovascular function. Vasc Pharmacol 55(1–3):17–25

    CAS  Google Scholar 

  • Milan DJ, Giokas AC, Serluca FC, Peterson RT, MacRae CA (2006) Notch1b and neuregulin are required for specification of central cardiac conduction tissue. Development 133(6):1125–1132

    CAS  PubMed  Google Scholar 

  • Miller WL (2002) Androgen biosynthesis from cholesterol to DHEA. Mol Cell Endocrinol 198(1–2):7–14

    CAS  PubMed  Google Scholar 

  • Miller WL (2007) StAR search—what we know about how the steroidogenic acute regulatory protein mediates mitochondrial cholesterol import. Mol Endocrinol 21(3):589–601

    CAS  PubMed  Google Scholar 

  • Miller WL (2008) Steroidogenic enzymes. Endocr Dev 13:1–18

    CAS  PubMed  Google Scholar 

  • Miller WL, Strauss JF (1999) Molecular pathology and mechanism of action of the steroidogenic acute regulatory protein, StAR. J Steroid Biochem Mol Biol 69(1–6):131–141

    CAS  PubMed  Google Scholar 

  • Moriyama K, Tagami T, Akamizu T, Usui T, Saijo M, Kanamoto N, Hataya Y, Shimatsu A, Kuzuya H, Nakao K (2002) Thyroid hormone action is disrupted by bisphenol A as an antagonist. J Clin Endocrinol Metab 87(11):5185–5190

    CAS  PubMed  Google Scholar 

  • Mullur R, Liu YY, Brent GA (2014) Thyroid hormone regulation of metabolism. Physiol Rev 94(2):355–382

    CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy E (2011) Estrogen signaling and cardiovascular disease. Circ Res 109(6):687–696

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ni TT, Lu J, Zhu M, Maddison LA, Boyd KL, Huskey L, Ju B, Hesselson D, Zhong TP, Page-McCaw PS, Stainier DY, Chen W (2012) Conditional control of gene function by an invertible gene trap in zebrafish. Proc Natl Acad Sci U S A 109(38):15389–15394

    CAS  PubMed  PubMed Central  Google Scholar 

  • O’Shaughnessy PJ, Baker PJ, Heikkilä M, Vainio S, McMahon AP (2000) Localization of 17beta-hydroxysteroid dehydrogenase/17-ketosteroid reductase isoform expression in the developing mouse testis--androstenedione is the major androgen secreted by fetal/neonatal leydig cells. Endocrinology 141(7):2631–2637

    PubMed  Google Scholar 

  • Omiecinski CJ, Vanden Heuvel JP, Perdew GH, Peters JM (2011) Xenobiotic metabolism, disposition, and regulation by receptors: from biochemical phenomenon to predictors of major toxicities. Toxicol Sci 120(Suppl 1):S49–S75

    CAS  PubMed  Google Scholar 

  • Osborne N, Brand-Arzamendi K, Ober EA, Jin SW, Verkade H, Holtzman NG, Yelon D, Stainier DY (2008) The spinster homolog, two of hearts, is required for sphingosine 1-phosphate signaling in zebrafish. Curr Biol 18(23):1882–1888

    CAS  PubMed  PubMed Central  Google Scholar 

  • Padmanabhan V, Sairam MR, Hassing JM, Brown MB, Ridings JW, Beitins IZ (1991) Follicle-stimulating hormone signal transduction: role of carbohydrate in aromatase induction in immature rat sertoli cells. Mol Cell Endocrinol 79(1–3):119–128

    CAS  PubMed  Google Scholar 

  • Panzica GC, Viglietti-Panzica C, Mura E, Quinn MJ Jr, Lavoie E, Palanza P, Ottinger MA (2007) Effects of xenoestrogens on the differentiation of behaviorally-relevant neural circuits. Front Neuroendocrinol 28(4):179–200

    CAS  PubMed  Google Scholar 

  • Payne AH, Hales DB (2004) Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr Rev 25(6):947–970

    CAS  PubMed  Google Scholar 

  • Peterson RT, Link BA, Dowling JE, Schreiber SL (2000) Small molecule developmental screens reveal the logic and timing of vertebrate development. Proc Natl Acad Sci U S A 97(24):12965–12969

    CAS  PubMed  PubMed Central  Google Scholar 

  • Petz LN, Nardulli AM (2000) Sp1 binding sites and an estrogen response element half-site are involved in regulation of the human progesterone receptor A promoter. Mol Endocrinol 14(7):972–985

    CAS  PubMed  Google Scholar 

  • Pietras RJ, Szego CM (1975) Endometrial cell calcium and oestrogen action. Nature 253(5490):357–359

    CAS  PubMed  Google Scholar 

  • Pinzone JJ, Stevenson H, Strobl JS, Berg PE (2004) Molecular and cellular determinants of estrogen receptor alpha expression. Mol Cell Biol 24(11):4605–4612

    CAS  PubMed  PubMed Central  Google Scholar 

  • Prossnitz ER, Arterburn JB, Smith HO, Oprea TI, Sklar LA, Hathaway HJ (2008) Estrogen signaling through the transmembrane G protein-coupled receptor GPR30. Annu Rev Physiol 70:165–190

    CAS  PubMed  Google Scholar 

  • Purdom CE, Hardiman PA, Bye VVJ, Eno NC, Tyler CR, Sumpter JP (1994) Estrogenic effects of effluents from sewage treatment works. Chem Ecol 8:275–285

    CAS  Google Scholar 

  • Reiter JF, Alexander J, Rodaway A, Yelon D, Patient R, Holder N, Stainier DY (1999) Gata5 is required for the development of the heart and endoderm in zebrafish. Genes Dev 13(22):2983–2995

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reiter JF, Verkade H, Stainier DY (2001) Bmp2b and Oep promote early myocardial differentiation through their regulation of gata5. Dev Biol 234(2):330–338

    CAS  PubMed  Google Scholar 

  • Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER (2005) A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307(5715):1625–1630

    CAS  PubMed  Google Scholar 

  • Revelli A, Massobrio M, Tesarik J (1998) Nongenomic actions of steroid hormones in reproductive tissues. Endocr Rev 19(1):3–17

    CAS  PubMed  Google Scholar 

  • Rohr S, Otten C, Abdelilah-Seyfried S (2008) Asymmetric involution of the myocardial field drives heart tube formation in zebrafish. Circ Res 102(2):e12–e19

    CAS  PubMed  Google Scholar 

  • Rohr S, Bit-Avragim N, Abdelilah-Seyfried S (2006) Heart and soul/prkci and nagie oko/mpp5 regulate myocardial coherence and remodeling during cardiac morphogenesis. Development 133:107–115

    CAS  PubMed  Google Scholar 

  • Rowlands JC, Gustafsson JA (1997) Aryl hydrocarbon receptor-mediated signal transduction. Crit Rev Toxicol 27(2):109–134

    CAS  PubMed  Google Scholar 

  • Sahlin L, Norstedt G, Eriksson H (1994) Androgen regulation of the insulin-like growth factor-I and the estrogen receptor in rat uterus and liver. J Steroid Biochem Mol Biol 51(1–2):57–66

    CAS  PubMed  Google Scholar 

  • Schmidt JV, Bradfield CA (1996) Ah receptor signaling pathways. Annu Rev Cell Dev Biol 12:55–89

    CAS  PubMed  Google Scholar 

  • Scott IC, Masri B, D'Amico LA, Jin SW, Jungblut B, Wehman AM, Baier H, Audigier Y, Stainier DY (2007) The g protein-coupled receptor agtrl1b regulates early development of myocardial progenitors. Dev Cell 12(3):403–413

    CAS  PubMed  Google Scholar 

  • Seljelid R, Reith A, Nakken KF (1970) The early phase of endocytosis in rat thyroid follicle cells. Lab Investig 23:595–605

    CAS  PubMed  Google Scholar 

  • Serluca FC (2008) Development of the proepicardial organ in the zebrafish. Dev Biol 315(1):18–27

    CAS  PubMed  Google Scholar 

  • Shankar A, Teppala S, Sabanayagam C (2012) Urinary bisphenol a levels and measures of obesity: results from the national health and nutrition examination survey 2003–2008. ISRN Endocrinol 2012:965243

    PubMed  PubMed Central  Google Scholar 

  • Sohoni P, Sumpter JP (1998) Several environmental oestrogens are also anti-androgens. J Endocrinol 158(3):327–339

    CAS  PubMed  Google Scholar 

  • Stainier DY (2001) Zebrafish genetics and vertebrate heart formation. Nat Rev Genet 2(1):39–48

    CAS  PubMed  Google Scholar 

  • Stainier DY, Weinstein BM, Detrich HW, Zon LI, Fishman MC (1995) Cloche, an early acting zebrafish gene, is required by both the endothelial and hematopoietic lineages. Development 121(10):3141–3150

    CAS  PubMed  Google Scholar 

  • Staudt D, Stainier D (2012) Uncovering the molecular and cellular mechanisms of heart development using the zebrafish. Annu Rev Genet 46:397–418

    CAS  PubMed  Google Scholar 

  • Stein B, Yang MX (1995) Repression of the interleukin-6 promoter by estrogen receptor is mediated by NF-kappa B and C/EBP beta. Mol Cell Biol 15(9):4971–4979

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stumpf WE (1969) Nuclear concentration of 3H-estradiol in target tissues. Dry-mount autoradiography of vagina, oviduct, ovary, testis, mammary tumor, liver and adrenal. Endocrinology 85(1):31–37

    CAS  PubMed  Google Scholar 

  • Sumpter JP (1998) Xenoendorine disrupters--environmental impacts. Toxicol Lett 102-103:337–342

    CAS  PubMed  Google Scholar 

  • Szego CM, Davis JS (1967) Adenosine 3′,5′-monophosphate in rat uterus: acute elevation by estrogen. Proc Natl Acad Sci U S A 58(4):1711–1718

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takeda H, Chodak G, Mutchnik S, Nakamoto T, Chang C (1990) Immunohistochemical localization of androgen receptors with mono- and polyclonal antibodies to androgen receptor. J Endocrinol 126(1):17–25

    CAS  PubMed  Google Scholar 

  • Telakowski-Hopkins CA, King RG, Pickett CB (1988) Glutathione S-transferase Ya subunit gene: identification of regulatory elements required for basal level and inducible expression. Proc Natl Acad Sci U S A 85(4):1000–1004

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ternes TA, Stumpf M, Mueller J, Haberer K, Wilken RD, Servos M (1999) Behavior and occurrence of estrogens in municipal sewage treatment plants--I. Investigations in Germany, Canada and Brazil. Sci Total Environ 225(1–2):81–90

    CAS  PubMed  Google Scholar 

  • Tessadori F, van Weerd JH, Burkhard SB, Verkerk AO, de Pater E, Boukens BJ, Vink A, Christoffels VM, Bakkers J (2012) Identification and functional characterization of cardiac pacemaker cells in zebrafish. PLoS One 7(10):e47644

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thackaberry EA, Gabaldon DM, Walker MK, Smith SM (2002) Aryl hydrocarbon receptor null mice develop cardiac hypertrophy and increased hypoxia-inducible factor-1alpha in the absence of cardiac hypoxia. Cardiovasc Toxicol 2(4):263–274

    CAS  PubMed  Google Scholar 

  • Thackaberry EA, Jiang Z, Johnson CD, Ramos KS, Walker MK (2005) Toxicogenomic profile of 2,3,7,8-tetrachlorodibenzo-p-dioxin in the murine fetal heart: modulation of cell cycle and extracellular matrix genes. Toxicol Sci 88(1):231–241

    CAS  PubMed  Google Scholar 

  • Thomas P, Pang Y, Filardo EJ, Dong J (2005) Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 146(2):624–632

    CAS  PubMed  Google Scholar 

  • Timmerman LA, Grego-Bessa J, Raya A, Bertrán E, Pérez-Pomares JM, Díez J, Aranda S, Palomo S, McCormick F, Izpisúa-Belmonte JC, de la Pompa JL (2004) Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev 18(1):99–115

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tonissen KF, Drysdale TA, Lints TJ, Harvey RP, Krieg PA (1994) XNkx-2. 5, a Xenopus gene related to Nkx-2. 5 and tinman: evidence for a conserved role in cardiac development. Dev Biol 162(1):325–328

    CAS  PubMed  Google Scholar 

  • Trinh LA, Stainier DY (2004) Fibronectin regulates epithelial organization during myocardial migration in zebrafish. Dev Cell 6(3):371–382

    CAS  PubMed  Google Scholar 

  • Ubuka T, Son YL, Bentley GE, Millar RP, Tsutsui K (2013) Gonadotropin-inhibitory hormone (GnIH), GnIH receptor and cell signaling. Gen Comp Endocrinol 190:10–17

    CAS  PubMed  Google Scholar 

  • Umayahara Y, Kawamori R, Watada H, Imano E, Iwama N, Morishima T, Yamasaki Y, Kajimoto Y, Kamada T (1994) Estrogen regulation of the insulin-like growth factor I gene transcription involves an AP-1 enhancer. J Biol Chem 269(23):16433–16442

    CAS  PubMed  Google Scholar 

  • Veldman MB, Lin S (2008) Zebrafish as a developmental model organism for pediatric research. Pediatr Res 64(5):470–476

    PubMed  Google Scholar 

  • Verhoeven MC, Haase C, Christoffels VM, Weidinger G, Bakkers J (2011) Wnt signaling regulates atrioventricular canal formation upstream of BMP and Tbx2. Birth Defects Res A Clin Mol Teratol 91(6):435–440

    CAS  PubMed  Google Scholar 

  • Vermot J, Forouhar AS, Liebling M, Wu D, Plummer D, Gharib M, Fraser SE (2009) Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart. PLoS Biol 7(11):e1000246

    PubMed  PubMed Central  Google Scholar 

  • Vicencio JM, Ibarra C, Estrada M, Chiong M, Soto D, Parra V, Diaz-Araya G, Jaimovich E, Lavandero S (2006) Testosterone induces an intracellular calcium increase by a nongenomic mechanism in cultured rat cardiac myocytes. Endocrinology 147(3):1386–1395

    CAS  PubMed  Google Scholar 

  • Vivacqua A, Romeo E, De Marco P, De Francesco EM, Abonante S, Maggiolini M (2012) GPER mediates the Egr-1 expression induced by 17β-estradiol and 4-hydroxitamoxifen in breast and endometrial cancer cells. Breast Cancer Res Treat 133(3):1025–1035

    CAS  PubMed  Google Scholar 

  • Voutilainen R, Miller WL (1986) Developmental expression of genes for the steroidogenic enzymes P450scc (20,22-desmolase), P450c17 (17 alpha-hydroxylase/17,20-lyase), and P450c21 (21-hydroxylase) in the human fetus. J Clin Endocrinol Metab 63(5):1145–1150

    CAS  PubMed  Google Scholar 

  • Walisser JA, Bunger MK, Glover E, Bradfield CA (2004) Gestational exposure of Ahr and Arnt hypomorphs to dioxin rescues vascular development. Proc Natl Acad Sci U S A 101(47):16677–16682

    CAS  PubMed  PubMed Central  Google Scholar 

  • Walker MK, Catron TF (2000) Characterization of cardiotoxicity induced by 2,3,7, 8-tetrachlorodibenzo-p-dioxin and related chemicals during early chick embryo development. Toxicol Appl Pharmacol 167(3):210–221

    CAS  PubMed  Google Scholar 

  • Walsh EC, Stainier DY (2001) UDP-glucose dehydrogenase required for cardiac valve formation in zebrafish. Science 293(5535):1670–1673

    CAS  PubMed  Google Scholar 

  • Wang Q, Carroll JS, Brown M (2005) Spatial and temporal recruitment of androgen receptor and its coactivators involves chromosomal looping and polymerase tracking. Mol Cell 19(5):631–642

    CAS  PubMed  Google Scholar 

  • Waye A, Trudeau VL (2011) Neuroendocrine disruption: more than hormones are upset. J Toxicol Environ Health B Crit Rev 14(5–7):270–291

    CAS  PubMed  PubMed Central  Google Scholar 

  • Webb P, Nguyen P, Shinsako J, Anderson C, Feng W, Nguyen MP, Chen D, Huang SM, Subramanian S, McKinerney E, Katzenellenbogen BS, Stallcup MR, Kushner PJ (1998) Estrogen receptor activation function 1 works by binding p160 coactivator proteins. Mol Endocrinol 12(10):1605–1618

    CAS  PubMed  Google Scholar 

  • Webb P, Nguyen P, Valentine C, Lopez GN, Kwok GR, McInerney E, Katzenellenbogen BS, Enmark E, Gustafsson JA, Nilsson S, Kushner PJ (1999) The estrogen receptor enhances AP-1 activity by two distinct mechanisms with different requirements for receptor transactivation functions. Mol Endocrinol 13(10):1672–1685

    CAS  PubMed  Google Scholar 

  • Weisz A, Rosales R (1990) Identification of an estrogen response element upstream of the human c-fos gene that binds the estrogen receptor and the AP-1 transcription factor. Nucleic Acids Res 18(17):5097–5106

    CAS  PubMed  PubMed Central  Google Scholar 

  • Westin J, Lardelli M (1997) Three novel notch genes in zebrafish: implications for vertebrate notch gene evolution and function. Dev Genes Evol 207(1):51–63

    CAS  PubMed  Google Scholar 

  • Xiao FY, Nheu L, Komesaroff P, Ling S (2015) Testosterone protects cardiac myocytes from superoxide injury via NF-κB signalling pathways. Life Sci 133:45–52

    CAS  PubMed  Google Scholar 

  • Yan S, Chen Y, Dong M, Song W, Belcher SM, Wang HS (2011) Bisphenol A and 17β-estradiol promote arrhythmia in the female heart via alteration of calcium handling. PLoS One 6(9):e25455

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yelon D, Ticho B, Halpern ME, Ruvinsky I, Ho RK, Silver LM, Stainier DY (2000) The bHLH transcription factor hand2 plays parallel roles in zebrafish heart and pectoral fin development. Development 127(12):2573–2582

    CAS  PubMed  Google Scholar 

  • Yue P, Chatterjee K, Beale C, Poole-Wilson PA, Collins P (1995) Testosterone relaxes rabbit coronary arteries and aorta. Circulation 91(4):1154–1160

    CAS  PubMed  Google Scholar 

  • Zeng XX, Wilm TP, Sepich DS, Solnica-Krezel L (2007) Apelin and its receptor control heart field formation during zebrafish gastrulation. Dev Cell 12(3):391–402

    CAS  PubMed  Google Scholar 

  • Zoeller RT, Bansal R, Parris C (2005) Bisphenol-A, an environmental contaminant that acts as a thyroid hormone receptor antagonist in vitro, increases serum thyroxine, and alters RC3/neurogranin expression in the developing rat brain. Endocrinology 146(2):607–612

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Graciel Diamante .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Diamante, G., Schlenk, D. (2018). Challenges of Endocrine Disruption and Cardiac Development. In: Burggren, W., Dubansky, B. (eds) Development and Environment. Springer, Cham. https://doi.org/10.1007/978-3-319-75935-7_13

Download citation

Publish with us

Policies and ethics