Skip to main content

Advertisement

SpringerLink
Log in

Endocrine-Disrupting Chemical Exposure and the American Alligator: A Review of the Potential Role of Environmental Estrogens on the Immune System of a Top Trophic Carnivore

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Endocrine-disrupting chemicals (EDCs) alter cellular and organ system homeostasis by interfering with the body’s normal physiologic processes. Numerous studies have identified environmental estrogens as modulators of EDC-related processes in crocodilians, notably in sex determination. Other broader studies have shown that environmental estrogens dysregulate normal immune function in mammals, birds, turtles, lizards, fish, and invertebrates; however, the effects of such estrogenic exposures on alligator immune function have not been elucidated. Alligators occupy a top trophic status, which may give them untapped utility as indicators of environmental quality. Environmental estrogens are also prevalent in the waters they occupy. Understanding the effects of these EDCs on alligator immunity is critical for managing and assessing changes in their health and is thus the focus of this review.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Ahmed SA (2000) The immune system as a potential target for environmental estrogens (endocrine disrupters): a new emerging field. Toxicology 150:191–206

    CAS  Google Scholar 

  • Barua A, Furusawa S, Yoshimura Y (2000) Influence of aging and estrogen treatment on the IgY concentration in the egg yolk of chicken, Gallus domesticus. Jpn Poult Sci 37:280–288

    CAS  Google Scholar 

  • Bergeron JM, Crews D, McLachlan JA (1994) PCBs as environmental estrogens: turtle sex determination as a biomarker of environmental contamination. Environ Health Perspect 102:780–781

    CAS  Google Scholar 

  • Bohana-Kashtan O, Ziporen L, Donin N, Kraus S, Fishelson Z (2004) Cell signals transduced by complement. Mol Immunol 41:583–597

    CAS  Google Scholar 

  • Bouman A, Heineman MJ, Faas MM (2005) Sex hormones and the immune response in humans. Human Reprod Update 11:411–423

    CAS  Google Scholar 

  • Brochu CA (2003) Phylogenetic approaches toward crocodylian history. Annu Rev Earth Planet Sci 31:357–397

    CAS  Google Scholar 

  • Bull JJ, Gutzke WHN, Crews D (1988) Sex reversal by estradiol in three reptilian orders. Gen Comp Endocrinol 70:425–428

    CAS  Google Scholar 

  • Burnham DK, Lackey A, Manering M, Jaensson E, Pearson J, Tyler DO et al (2003) Effects of 17α-ethinylestradiol on immune parameters in the lizard Sceloporus occidentalis. Environ Toxicol 18:211–218

    CAS  Google Scholar 

  • Cabas I, Liarte S, García-Alcázar A, Meseguer J, Mulero V, García-Ayala A (2012) 17a-Ethynylestradiol alters the immune response of the teleost gilthead seabream (Sparus aurata L.) both in vivo and in vitro. Dev Comp Immunol 36:547–556

    CAS  Google Scholar 

  • Campbell TW, Ellis CK (2007) Avian and exotic animal hematology and cytology, 3rd edn. Blackwell, Ames

    Google Scholar 

  • Canesi L, Betti M, Lorusso LC, Ciacci C, Gallo G (2005) In vivo effects of bisphenol A in Mytilus hemocytes: Modulation of kinase mediated signaling pathways. Aquat Toxicol 71:73–84

    CAS  Google Scholar 

  • Canesi L, Ciacci C, Lorusso LC, Betti M, Guarnieri T, Tavolari S et al (2006) Immunomodulation of 17 beta-estradiol in bivalve hemocytes. Am J Physiol Regul Integr Comp Physiol 291:R664–R673

    CAS  Google Scholar 

  • Carlsten H, Nilsson N, Johnsson R, Bäckman K, Holmdahl R, Tarkowski A (1992) Estrogen accelerates immune-complex glomerulonephritis but ameliorates T-cell mediated vasculitis and sialadenitis in autoimmune MRL lpr/lpr mice. Cell Immunol 144:190–202

    CAS  Google Scholar 

  • Chao TC, Chao HH, Chen MF, Greager JA, Walter RJ (2000) Female sex hormones modulate the function of LPS-treated macrophages. Am J Reprod Immunol 44:310–318

    CAS  Google Scholar 

  • Craighead FC (1968) The role of the alligator in shaping plant communities and maintain wildlife in the southern Everglades. Fla Nat 41:2–7

    Google Scholar 

  • Crain DA, Guillette LJ Jr, Rooney AA, Pickford DB (1997) Alterations in steroidogenesis in alligators (Alligator mississippiensis) exposed naturally and experimentally to environmental contaminants. Environ Health Perspect 105:528–533

    CAS  Google Scholar 

  • Crews D (2003) Sex determination: where environment and genetics meet. Evol Dev 5:50–55

    Google Scholar 

  • Crews D, Bergeron JM, McLachlan JA (1995) The role of estrogen in turtle sex determination and the effect of PCBs. Environ Health Perspect 103:73–77

    CAS  Google Scholar 

  • Cuchens MA, Clem LW (1979) Phylogeny of lymphocyte heterogeneity. IV. Evidence for T-like and B-like cells in reptiles. Dev Comp Immunol 3:287–297

    CAS  Google Scholar 

  • Cutolo M, Capellino S, Montagna P, Ghiorzo P, Sulli A, Villaggio B (2005) Sex hormone modulation of cell growth and apoptosis of the human monocytic/macrophage cell line. Arthritis Res Ther 7:R1124–R1132

    CAS  Google Scholar 

  • Cutolo M, Capellino S, Sulli A, Serioli B, Secchi ME, Villaggio B et al (2006) Estrogens and autoimmune disease. Ann N Y Acad Sci 1089:538–547

    CAS  Google Scholar 

  • Dean JH, Lauer LD, Murray MJ, Luster MI, Neptun D, Adams DO (1986) Functions of mononuclear phagocytes in mice exposed to diethylstilbestrol: A model of aberrant macrophage development. Cell Immunol 102:315–322

    CAS  Google Scholar 

  • Dzik JM (2010) The ancestry and cumulative evolution of immune reactions. Acta Biochim Pol 57:443–466

    CAS  Google Scholar 

  • El Ridi R, Zada S, Afifi A, El Deed S, El Rouby S, Farag M et al (1988) Cyclic changes in the differentiation of lymphoid cells in reptiles. Cell Differ 24:1–8

    Google Scholar 

  • Elf PK (2003) Yolk steroid hormones and sex determination in reptiles with TSD. Gen Comp Endocr 132:349–355

    CAS  Google Scholar 

  • Elsey RM, Trosclair PL III, Linscombe JT (2004) The American alligator as a predator of mottled ducks. Southeast Nat 3:381–390

    Google Scholar 

  • Ewert MA, Nelson CE (2003) Metabolic heating of embryos and sex determination in the American alligator, alligator mississippiensis. J Therm Biol 28:159–165

    Google Scholar 

  • Fairbrother A, Smits J, Grasman KA (2004) Avian immunotoxicology. J Toxicol Environ Health B Crit Rev 7:105–137

    CAS  Google Scholar 

  • Fanti P, Nazareth M, Bucelli R, Mineo M, Gibbs K, Kumin M et al (2003) Estrogen decreases chemokine levels in murine mammary tissue: implications for the regulatory role of MIP-1 alpha and MCP-1/JE in mammary tumor formation. Endocrine 22:161–167

    CAS  Google Scholar 

  • Finger JW Jr, Isberg S (2012) A review of innate immune functions in crocodilians. Cab Rev 7 (67):1–11. http://www.cabi.org/cabreviews/?loadmodule=review&page=4051&reviewid=239841&Site=167

    Google Scholar 

  • Fossi CM, Marsili L, Neri G, Casini S, Bearzi G, Politi E et al (2000) Skin biopsy of Mediterranean cetaceans for the investigation of interspecies susceptibility to xenobiotic contaminants. Mar Environ Res 50:517–521

    CAS  Google Scholar 

  • Fossi CM, Casini S, Marsili L (2006) Endocrine disruptors in Mediterranean top marine predators. Environ Sci Pollut Res Int 13:204–207

    CAS  Google Scholar 

  • Gabrey SW (2010) Demographic and geographic variation in food habits of American alligators (Alligator mississippiensis) in Louisiana. Herpetol Conserv Biol 5:241–250

    Google Scholar 

  • Gabriel WN, Blumberg B, Sutton S, Place AR, Lance VA (2001) Alligator aromatase cDNA sequence and its expression in embryos at male and female incubation temperatures. J Exp Zool 290:439–448

    CAS  Google Scholar 

  • Gameiro CM, Romão F, Castelo-Branco C (2010) Menopause and aging: changes in the immune system—a review. Maturitas 67:316–320

    CAS  Google Scholar 

  • Gauthier-Clerc S, Pellerin J, Fournier M, Amiard JC (2006) Immunological and biochemical responses in Mya arenaria (Mollusca bivalvia) exposed in vivo to estradiol-17beta. Comp Biochem Physiol C Toxicol Pharmacol 144:228–234

    CAS  Google Scholar 

  • Grasman KA, Fox GA (2001) Associations between altered immune function and organochlorine contamination in young caspian terns (Sterna caspia) from Lake Huron, 1997–1999. Ecotoxicology 10:101–114

    CAS  Google Scholar 

  • Guillette LJ Jr, Gross TS, Masson GR, Matter JM, Percival HF, Woodward AR (1994) Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ Health Perspect 102(8):680–688

    CAS  Google Scholar 

  • Guillette LJ Jr, Crain DA, Gunderson MP, Kools SAE, Milnes MR, Orlando EF et al (2000) Alligators and endocrine disrupting contaminants: a current perspective. Am Zool 40:438–452

    CAS  Google Scholar 

  • Guillette LJ Jr, Vonier PM, McLachlan JA (2002) Affinity of the alligator estrogen receptor for serum pesticide contaminants. Toxicology 181–182:151–154

    Google Scholar 

  • Guzman-Rojas L, Sims-Mourtada JC, Rangel R, Martinez-Valdez H (2002) Life and death within germinal centres: a double edge sword. Immunology 107:167–175

    CAS  Google Scholar 

  • Hamlin HJ, Lowers RH, Albergotti LC, McCoy MW, Mutz J, Guillette LJ Jr (2010) Environmental influence on yolk steroids in American alligators (Alligator mississippiensis). Biol Reprod 83:736–741

    CAS  Google Scholar 

  • Hareramadas B, Rai U (2006) Cellular mechanism of estrogen-induced thymic involution in wall lizard: caspase-dependent action. J Exp Zool 305A:396–409

    CAS  Google Scholar 

  • Harmon BG (1998) Avian heterophils in inflammation and disease resistance. Poult Sci 77:972–977

    CAS  Google Scholar 

  • Heinz GH, Percival HF, Jennings ML (1991) Contaminants in American alligator eggs from Lake Apopka, Lake Griffin, and Lake Okeechobee, Florida. Environ Monit Asses 16:277–285

    CAS  Google Scholar 

  • Hewitt SC, Korach KS (2003) Oestrogen receptor knockout mice: roles for oestrogen receptors α and β in reproductive tissues. Reproduction 125:143–149

    CAS  Google Scholar 

  • Hince M, Sakkal S, Vlahos K, Dudakov J, Boyd R, Chidgey A (2008) The role of sex steroids and gonadectomy in the control of thymic involution. Cell Immunol 252:122–138

    CAS  Google Scholar 

  • Islander U, Erlandsson MC, Hasséus B, Jonsson CA, Ohlsson C, Gustafsson JA et al (2003) Influence of oestrogen receptor alpha and beta on the immune system in aged female mice. Immunology 110:149–157

    CAS  Google Scholar 

  • Janis K, Hoeltke J, Nazareth M, Fanti P, Poppenberg K, Aronica SM (2004) Estrogen decreases expression of chemokine receptors, and suppresses chemokine bioactivity in murine monocytes. Am J Reprod Immunol 51:22–31

    Google Scholar 

  • Jin Y, Chen R, Liu W, Fu Z (2010) Effect of endocrine disrupting chemicals on the transcription of genes related to the innate immune system in the early developmental stage of zebrafish (Danio rerio). Fish Shellfish Immunol 28:854–861

    CAS  Google Scholar 

  • Karpuzoglu E, Ahmed SA (2006) Estrogen regulation of nitric oxide and inducible nitric oxide synthase (iNOS) in immune cells: Implications for immunity, autoimmune diseases, and apoptosis. Nitric Oxide 15:177–186

    CAS  Google Scholar 

  • Karpuzoglu E, Phillips RA, Gogal RM Jr, Ahmed SA (2007) IFN-γ-inducing transcription factor, T-bet is upregulated by estrogen in murine splenocytes: role of IL-27 but not IL-12. Mol Immunol 44:1808–1814

    CAS  Google Scholar 

  • Katayama M, Fukuda T, Narabara K, Abe A, Kondo Y (2012) Localization of estrogen receptor in the central lymphoid organs of chickens during the late stage of embryogenesis. Biosci Biotechnol Biochem 76:2003–2007

    CAS  Google Scholar 

  • Katsu Y, Bermudez DS, Braun EL, Helbing C, Miyagawa S, Gunderson MP et al (2004) Molecular cloning of the estrogen and progesterone receptors of the American alligator. Gen Comp Endocrinol 136:122–133

    CAS  Google Scholar 

  • Keller JM, Kucklick JR, Stamper MA, Harms CA, McClellan-Green PD (2004) Associations between organochlorine contaminant concentrations and clinical health parameters in loggerhead sea turtles from North Carolina, USA. Environ Health Perspect 112:1074–1079

    CAS  Google Scholar 

  • Keller JM, McClellan-Green PD, Kucklick JR, Keil DE, Peden-Adams MM (2006) Effects of organochlorine contaminants on loggerhead sea turtle immunity: comparison of a correlative field study and in vitro exposure experiments. Environ Health Perspect 114:71–76

    Google Scholar 

  • Kohno S, Bermudez DS, Katsu Y, Iguchi T, Guillette LJ Jr (2008) Gene expression patterns in juvenile American alligators (Alligator mississippiensis) exposed to environmental contaminants. Aquat Toxicol 88:95–101

    CAS  Google Scholar 

  • Komi J, Möttönen M, Luukkainen R, Lassila O (2001) Nonsteroidal anti oestrogens inhibit the differentiation of synovial macrophages into dendritic cells. Rheumatology 40:185–191

    CAS  Google Scholar 

  • Kondo Y, Goto C, Abe A (2004) Effects of estrogen treatment during the embryogenic period on chick antibody production. J Poultry Sci 41:85–93

    CAS  Google Scholar 

  • Kovats S, Carreras E (2008) Regulation of dendritic cell differentiation and function by estrogen receptor ligands. Cell Immunol 252:81–90

    CAS  Google Scholar 

  • Kroese FG, Leceta J, Dopp EA, Herraez MP, Niewenhuis P, Zapata A (1985) Dendritic immune complex trapping cells in the spleen of the snake, Python reticulatus. Dev Comp Immunol 9:641–652

    CAS  Google Scholar 

  • Lance VA, Bogart MH (1994) Studies on sex determination in the American alligator Alligator mississippiensis. J Exp Zool 270:79–85

    Google Scholar 

  • Lang JW, Andrews HV (1994) Temperature-dependent sex determination in crocodilians. J Exp Zool 270:28–44

    Google Scholar 

  • Law WY, Chen WH, Song YL, Dufour S, Chang CF (2001) Differential in vitro suppressive effects of steroids on leukocyte phagocytosis in two teleosts, tilapia and common carp. Gen Comp Endocrinol 121:163–172

    CAS  Google Scholar 

  • Leceta J, Zapata A (1985) Seasonal changes in the thymus and spleen of the turtle, Mauremys caspcia. A morphometrical, light microscopical study. Dev Comp Immunol 9:653–688

    CAS  Google Scholar 

  • Lynch HE, Goldberg GL, Chidgey A, Van den Brink MRM, Boyd R, Sempowski GD (2009) Thymic involution and immune reconstitution. Trends Immunol 30:366–373

    CAS  Google Scholar 

  • Magadon-Mompo S, Sanchez-Espinel C, Gambon-Deza F (2013) IgH loci of American alligator and saltwater crocodile shed light on IgA evolution. Immunogenetics 65:531–541

    Google Scholar 

  • Markman S, Müller CT, Pascoe D, Dawson A, Buchanan KL (2011) Pollutants affect development in nesting starlings Sturnus vulgaris. J Appl Ecol 48:391–397

    Google Scholar 

  • Mateo MR, Roberts ED, Enright FM (1984) Morphologic, cytochemical, and functional studies of peripheral blood cells of young healthy American alligators (Alligator mississippiensis). Am J Vet Res 45:1046–1053

    CAS  Google Scholar 

  • Meethal SV, Atwood CS (2005) The role of hypothalamic-pituitary-gonadal hormones in the normal structure and functioning of the brain. Cell Mol Life Sci 62:257–270

    CAS  Google Scholar 

  • Merchant M, Roche C, Elsey RM, Prudhomme J (2003) Antibacterial properties of serum from the American alligator (Alligator mississippiensis). Comp Biochem Physiol B Biochem Mol Biol 136:505–513

    Google Scholar 

  • Merchant M, Thibodeaux D, Loubser K, Elsey RM (2004) Amoebacidal effects of serum from the American alligator (Alligator mississippiensis). J Parasitol 90:1480–1483

    Google Scholar 

  • Merchant M, Pallansch M, Paulman RL, Wells JB, Nalca A, Ptak R (2005) Antiviral activity of serum from the American alligator (Alligator mississippiensis). Antiviral Res 66:35–38

    CAS  Google Scholar 

  • Merchant M, Leger N, Jerkins E, Mills K, Pallansch MB, Paulman RL et al (2006) Broad spectrum antimicrobial activity of leukocyte extracts from the American alligator (Alligator mississippiensis). Vet Immunol Immunopathol 110:221–228

    Google Scholar 

  • Merchant M, Williams S, Trosclair PL 3rd, Elsey RM, Mills K (2007) Febrile response to infection in the American alligator (Alligator mississippiensis). Comp Biochem Physiol A Mol Integr Physiol 148:921–925

    Google Scholar 

  • Merchant M, Williams S, Hardy R (2009) Production of superoxide ions by leukocytes of the American alligator (Alligator mississippiensis). Comp Biochem Physiol B Biochem Mol Biol 152:67–71

    Google Scholar 

  • Messingham KA, Heinrich SA, Kovacs EJ (2001) Estrogen restores cellular immunity in injured male mice by way of suppression of interleukin-6 production. J Leukoc Biol 70:887–895

    CAS  Google Scholar 

  • Meyer A, Zardoya R (2003) Recent advances in the (molecular) phylogeny of vertebrates. Annu Rev Ecol Evol Syst 34:311–338

    Google Scholar 

  • Milnes MR, Guillette LJ Jr (2008) Alligator tales: new lessons about environmental contaminants from a sentinel species. Bioscience 58:1027–1036

    Google Scholar 

  • Milnes MR, Woodward AR, Rooney AA, Guillette LJ Jr (2002) Plasma steroid concentrations in relation to size and age in juvenile alligators from two Florida lakes. Comp Biochem Physiol A Mol Integr Physiol 131:923–930

    Google Scholar 

  • Milnes MR, Bryan TA, Katsu Y, Kohno S, Moore BC, Iguchi T et al (2008) Increased posthatching mortality and loss of sexually dimorphic gene expression in alligators (Alligator mississippiensis) from a contaminated environment. Biol Reprod 78:932–938

    CAS  Google Scholar 

  • Milston RH, Fitzpatrick MS, Vella AT, Clements S, Gundersen D, Fiest G et al (2003) Short-term exposure of chinook salmon (Oncoryhnchus tshawytscha) to o, p-DDE or DMSO during early life-history stages causes long-term humoral immunosuppression. Environ Health Perspect 111:1601–1607

    CAS  Google Scholar 

  • Molero L, Garcia-Duran M, Diaz-Recasens J, Rico L, Casado S, Lopez-Farre A (2002) Expression of estrogen receptor subtypes and neuronal nitric oxide synthase in neutrophils from women and men: regulation by estrogen. Cardiovasc Res 56:43–51

    CAS  Google Scholar 

  • Müller W, Groothuis TGG, Kasprzik A, Dijkstra C, Alatalo RV, Siitari H (2005) Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks. Proc Biol Sci 272:1971–1977

    Google Scholar 

  • Nadal A, Alonso-Magdalena P, Ripoll C, Fuentes E (2005) Disentangling the molecular mechanisms of action of endogenous and environmental estrogens. Pflugers Arch 449:335–343

    CAS  Google Scholar 

  • Nalbandian G, Kovats S (2005) Estrogen, immunity and autoimmune disease. Curr Med Chem Immunol Endocr Metab Agents 5:85–91

    CAS  Google Scholar 

  • Narita S, Goldblum RM, Watson CS, Brooks EG, Estes DM, Curran EM et al (2007) Environmental estrogens induce mast cell degranulation and enhance IgE-mediated release of allergic mediators. Environ Health Perspect 115:48–52

    CAS  Google Scholar 

  • Nilsson S, Koehler KF (2005) Oestrogen receptors and selective oestrogen receptor modulators: molecular and cellular pharmacology. Basic Clin Pharmacol Toxicol 96:15–25

    CAS  Google Scholar 

  • Nussinovitch U, Shoenfeld Y (2011) The role of sex and organ specific autoimmunity. Autoimmun Rev 11(6–7):A377–A385

    Google Scholar 

  • Pierdominici M, Maselli A, Colasanti T, Giammarioli AM, Delunardo F, Vacirca D et al (2010) Estrogen receptor profiles in human peripheral blood lymphocytes. Immunol Lett 132:79–85

    CAS  Google Scholar 

  • Platt SG, Brantley CG, Hastings RW (1990) Food habits of juvenile American alligators in the upper lake Ponchartrain estuary. Northeast Gulf Sci 11:123–130

    Google Scholar 

  • Prossnitz ER, Barton M (2009) Signaling, physiological functions and clinical relevance of the G protein-coupled estrogen receptor (GPER). Prostaglandins Other Lipid Mediat 89:89–97

    CAS  Google Scholar 

  • Pung OJ, Tucker AN, Vore SJ, Luster MI (1985) Influence of estrogen on host resistance: Increased susceptibility of mice to Listeria monocytogenes correlates with depressed production of interleukin 2. Infect Immunol 50:91–96

    CAS  Google Scholar 

  • Quinn MJ, McKeran M, Lavoie ET, Ottinger MA (2009) Effects of estradiol on the development of the bursa of fabricius in Japanese quail. J Exp Zool 311A:91–95

    Google Scholar 

  • Ramsey M, Crews D (2009) Steroid signaling and temperature-dependent sex determination-reviewing the evidence for early action of estrogen during ovarian determination in turtles. Semin Cell Dev Biol 20:283–292

    CAS  Google Scholar 

  • Rettew JA, Huet YM, Marriott I (2009) Estrogens augment cell surface TLR4 expression on murine macrophages and regulate sepsis susceptibility in vivo. Endocrinology 150:3877–3884

    CAS  Google Scholar 

  • Rider CV, Hartig PC, Cardon MC, Lambright CR, Bobseine KL, Guillette LJ Jr et al (2010) Differences in sensitivity but not selectivity of xenoestrogen binding to alligator versus human estrogen receptor alpha. Environ Toxicol Chem 29:2064–2071

    CAS  Google Scholar 

  • Roe JH, Hopkins WA, Baionno JA, Staub BP, Rowe CL, Jackson BP (2004) Maternal transfer of selenium in Alligator mississippiensis nesting downstream from a coal-burning power plant. Environ Toxicol Chem 23:1969–1972

    CAS  Google Scholar 

  • Rooney AA (1998) Variation in the endocrine and immune system of juvenile alligators: environmental influence on physiology. Dissertation, University of Florida, Gainesville

  • Rooney AA, Bermudez DS, Guillette LJ Jr (2003) Altered histology of the thymus and spleen in contaminant-exposed juvenile American alligators. J Morphol 256:349–359

    Google Scholar 

  • Seillet C, Laffont S, Trémollières F, Rouquié N, Ribot C, Arnal JF et al (2012) The TLR-mediated response of plasmacytoid dendritic cells is regulated by estradiol in vivo through cell-intrinsic estrogen receptor α signaling. Blood 119:454–464

    CAS  Google Scholar 

  • Shelley LK, Ross PS, Kennedy CJ (2012) The effects of an in vitro exposure to 17β-estradiol and nonylphenol on rainbow trout (Oncorhynchus mykiss) peripheral blood leukocytes. Comp Biochem Physiol C Toxicol Pharmacol 155:440–446

    CAS  Google Scholar 

  • Shin YH, Yonezawa Y, Abe A, Kondo Y (2008) Changes in estrogen receptor alpha expression in the bursa of fabricius during chick embryonic development. Anim Sci 79:97–103

    CAS  Google Scholar 

  • Shupnik MA (2002) Oestrogen receptors, receptor variants and oestrogen actions in the hypothalamic-pituitary axis. J Neuroendocrinol 14:85–94

    CAS  Google Scholar 

  • Simpson ER (2003) Sources of estrogen and their importance. J Steroid Biochem Mol Biol 86:225–230

    CAS  Google Scholar 

  • Smith EN (1975) Thermoregulation of the American alligator, Alligator mississippiensis. Phys Zool 48:177–194

    Google Scholar 

  • Soucy G, Boivin G, Labrie F, Rivest S (2005) Estradiol is required for a proper immune response to bacterial and viral pathogens in the female brain. J Immunol 174:6391–6398

    CAS  Google Scholar 

  • Straub RH (2007) The complex role of estrogens in inflammation. Endocrinol Rev 5:521–574

    Google Scholar 

  • Stygar D, Weslund P, Eriksson H, Sahlin L (2006) Identification of wild-type and variants of oestrogen receptors in polymorphonuclear and mononuclear leucocytes. Clin Endocrinol 64:74–81

    CAS  Google Scholar 

  • Sykes JM IV, Klaphake E (2008) Reptile hematology. Vet Clin North Am Exot Anim Pract 11:481–500

    Google Scholar 

  • Tanaka Y, Elsey RM (1997) Light microscopic study of the alligator (Alligator mississippiensis) spleen with special reference to vascular architecture. J Morphol 233:43–52

    Google Scholar 

  • Tanriverdi F, Silveira LF, MacColl GS, Bouloux PM (2003) The hypothalamic-pituitary-gonadal axis: Immune function and autoimmunity. J Endocrinol 176:293–304

    CAS  Google Scholar 

  • Thammasirirak S, Ponkham P, Preecharram S, Khanchanuan R, Phonyothee P, Daduang S et al (2006) Purification, characterization and comparison of reptile lysozymes. Comp Biochem Physiol C Toxicol Pharmacol 143:209–217

    Google Scholar 

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

    CAS  Google Scholar 

  • Turgeon JL, Carr MC, Maki PM, Mendelsohn ME, Wise PM (2006) Complex actions of sex steroids in adipose tissue, the cardiovascular system, and brain: Insights from basic science and clinical studies. Endocr Rev 27:575–605

    CAS  Google Scholar 

  • Urushitani H, Katsu Y, Miyagawa S, Kohno S, Ohta Y, Guillette LJ Jr et al (2011) Molecular cloning of anti-Mullerian hormone from the American alligator, Alligator mississippiensis. Mol Cell Endocrinol 333:190–199

    CAS  Google Scholar 

  • Vinuesa CG, Sanz I, Cook MC (2009) Dysregulation of germinal centres in autoimmune disease. Nat Rev Immunol 9:845–857

    CAS  Google Scholar 

  • Vonier PM, Crain DA, McLachlan JA, Guillette LJ Jr, Arnold SF (1996) Interaction of environmental chemicals with the estrogen and progesterone receptors from the oviduct of the American alligator. Environ Health Perspect 104:1318–1322

    CAS  Google Scholar 

  • Vonier PM, Guillette LJ Jr, McLachlan JA, Arnold SF (1997) Identification and characterization of estrogen and progesterone receptors from the oviduct of the American alligator (Alligator mississippiensis). Biochem Biophys Res Commun 232:308–312

    CAS  Google Scholar 

  • Watson CS, Jeng YJ, Guptarak J (2011) Endocrine disruption by way of estrogen receptors that participate in nongenomic signaling pathways. J Steroid Biochem Mol Biol 127:44–50

    CAS  Google Scholar 

  • Wibbels T, Bull JJ, Crews D (1991) Synergism between estradiol and temperature: a common pathway in turtle sex determination? J Exp Zool 260:130–134

    CAS  Google Scholar 

  • Woodward AR, Percival HF, Jennings MI, Moore CT (1993) Low clutch viability of American alligators on Lake Apopka. Fla Sci 56:52–63

    Google Scholar 

  • Wright RK, Cooper EL (1981) Temperature effects on ectotherm immune responses. Dev Comp Immunol 5:117–122

    Google Scholar 

  • Yellayi S, Zakrocyzminski MA, Selvaraj V, Valli VE, Ghanta V, Helferich WG et al (2003) The phytoestrogen genistein suppresses cell-mediated immunity in mice. J Endocrinol 176:267–274

    CAS  Google Scholar 

  • Yoshikane M, Kay WR, Shibata Y, Inoue M, Yanai T, Kamata R et al (2006) Very high concentrations of DDE and toxaphene residues in crocodiles from the Ord River, western Australia: an investigation into possible endocrine disruption. J Environ Monit 8:649–661

    CAS  Google Scholar 

  • Yoshino S, Yamaki K, Yanagisawa R, Takano H, Hayashi H, Mori Y (2003) Effects of bisphenol A on antigen-specific antibody production, proliferative responses of lymphoid cells, and TH1 and TH2 immune responses in mice. Br J Pharmacol 138:1271–1276

    CAS  Google Scholar 

  • Zapata AG, Vara A, Torroba M (1992) Seasonal variations in the immune system of lower vertebrates. Immunol Today 13:142–147

    CAS  Google Scholar 

  • Zheng W, Yoshimura Y (2001) Organ-specificity of estrogen effects on the induction of immunocompetent cells in the chicken. J Poultry Sci 38:41–49

    CAS  Google Scholar 

  • Zimmerman LM, Paitz RT, Vogel LA, Bowden RM (2010a) Variation in the seasonal patterns of innate and adaptive immunity in the red-eared slider (Trachemys scripta). J Exp Biol 213:1477–1483

    CAS  Google Scholar 

  • Zimmerman LM, Vogel LA, Bowden RM (2010b) Understanding the vertebrate immune system: insights from the reptilian perspective. J Exp Biol 213:661–671

    CAS  Google Scholar 

  • Zimmerman LM, Vogel LA, Edwards KA, Bowden RM (2010c) Phagocytic B cells in a reptile. Biol Lett 6:270–273

    Google Scholar 

Download references

Acknowledgments

The authors thank Steve Holladay and Joerg Mayer for critical review of this manuscript.

Author information

Authors and Affiliations

  1. Department of Environmental Health Science, College of Public Health, University of Georgia, Athens, GA, USA

    John W. Finger Jr.

  2. Porosus Pty Ltd, PO Box 86, Palmerston, NT, 0831, Australia

    John W. Finger Jr.

  3. Department of Biosciences and Diagnostic Imaging, College of Veterinary Medicine, University of Georgia, Athens, GA, USA

    Robert M. Gogal Jr.

Authors
  1. John W. Finger Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert M. Gogal Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Robert M. Gogal Jr..

Rights and permissions

Reprints and permissions

About this article

Cite this article

Finger, J.W., Gogal, R.M. Endocrine-Disrupting Chemical Exposure and the American Alligator: A Review of the Potential Role of Environmental Estrogens on the Immune System of a Top Trophic Carnivore. Arch Environ Contam Toxicol 65, 704–714 (2013). https://doi.org/10.1007/s00244-013-9953-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-013-9953-x

Keywords

Search

Navigation