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Environmental Endocrine Disruption Effects Assessment In San Francisco Bay Fishes

Environmental Endocrine Disruption Effects Assessment In San Francisco Bay Fishes Shiner Surfperch & Pacific Staghorn Sculpin. Kevin M. Kelley. Environmental Endocrinology Laboratory Inst. for Integrated Research on Materials, Environment & Society (IIRMES)

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Environmental Endocrine Disruption Effects Assessment In San Francisco Bay Fishes

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  1. Environmental Endocrine Disruption Effects Assessment In San Francisco Bay Fishes Shiner Surfperch & Pacific Staghorn Sculpin Kevin M. Kelley Environmental Endocrinology Laboratory Inst. for Integrated Research on Materials, Environment & Society (IIRMES) Center for Education in Proteomics Analysis (CEPA) Marine Biology Program, Dept of Biological Sciences, Calif. St. Univ. Long Beach

  2. ENDOCRINE SYSTEMS regulate essential physiological functions Reproduction - Growth & Repair - MetabolismDefense/Immune - Thyroid - Developmental Stress Responses - Neuroendocrine - others Homeostasis, Adaptation, Survival

  3. Because endocrine systems are . . . . . . highly sensitive, responsive . . . respond to presence of environmental stressors to a degree commensurate with the need to maintain homeostasis . . . reflective in their response to the specific type(s) of stressor present

  4. . . . measures of ‘endocrine disruption’ are increasingly being pursued as sensitive bioindicators for water/environmental quality and specific contaminant effects Endocrine-disrupting chemicals (EDCs) are present in marine and estuarine environments, particularly along highly populated coastal regions: SF Bay Estuary http://toxics.usgs.gov/photo_gallery/sanfran.html

  5. STUDY OBJECTIVES 1- determine incidence and magnitude of endocrine disruption in wild fishes, emphasizing assessment of endocrine systems regulating stress responses, growth & repair, thyroid & reproduction 2- determine whether spatial differences can be establishedbetween different SF Bay locations, with respect to endocrine disrupted condition(s) 3- determine liver contaminant concentrations in individuals, to identify correlations between specific contaminants and type(s) of endocrine disruption in fish sampled from different SF Bay locations

  6. Shiner Surfperch Cymatogaster aggregata Pacific Staghorn Sculpin Leptocottus armatus

  7. 2006 Field Sites San Pablo Bay Berkeley Waterfront Oakland Inner Harbor Redwood City far-field reference:Tomales Bay Bodega Bay

  8. Far Field Sites Bodega Bay Tomales Bay

  9. STRESS RESPONSE AXIS

  10. Stress! BRAIN HYPOTHALAMUS PITUITARY anterior posterior CRH circulation ACTH Interrenal tissues adaptational responses Hypothalamo- Pituitary- Interrenal Axis (HPI Axis) ↑↑CORTISOL

  11. Shiner Surfperch Stress Response a a 1200 b Plasma Cortisol Concentration (ng/ml) b 800 400 21 21 10 13 0 Oakland Inner Harbor Berkeley Waterfront San Pablo Bay Redwood City

  12. Pacific Staghorn Sculpin Stress Response a a 1200 Plasma Cortisol Concentration (ng/ml) 800 b 400 c 17 13 19 16 0 Oakland Inner Harbor Berkeley Waterfront San Pablo Bay Redwood City

  13. STRESSOR BRAIN HYPOTHALAMUS PITUITARY anterior posterior CRH circulation ACTH Interrenal tissues impairedHPI Axis EDCs ? REDUCED cortisol response

  14. Other wild fish species living in affected marine environments exhibit impairment of their neuroendocrine stress response system ...experimental studies have shown that contaminants, such as PCBs, impair stress responses in fish (Quabius et al., 2005; Vijayan et al., 2006)

  15. THYROID ENDOCRINE SYSTEM

  16. BRAIN HYPOTHALAMUS PITUITARY anterior posterior TRH circulation TSH Thyroid gland variety of physiological actions Hypothalamo- Pituitary- Thyroid Axis (HPT Axis) T4 , T3

  17. Thyroid Hormones T4 T3 • broad physiological actions • essential for brain/neural development • permissive to somatic growth • important regulators of metabolism 3,5,3’-triiodothyronine 3,5,3’,5’-tetraiodothyronine (thyroxine)

  18. Thryoxine (T4) Levels in Shiner Surfperch 80 Shiner Surfperch Plasma Thyroxine (T4) Concentration, ng/ml 60 40 20 (19) (19) (9) (14) (11) 0 San Pablo Bay Berkeley Waterfront Redwood City Oakland Inner Harbor Bodega Bay

  19. Thryoxine (T4) Levels in Pacific Staghorn Sculpin Pacific Staghorn Sculpin 80 Plasma Thyroxine (T4) Concentration, ng/ml 60 40 20 (8) (13) (17) (12) (5) 0 San Pablo Bay Berkeley Waterfront Redwood City Oakland Inner Harbor Tomales Bay

  20. Thryoxine (T4) Levels in SF Bay Fish 100 80 Pacific Staghorn Sculpin Plasma Thyroxine (T4) Concentration, ng/ml 60 40 Shiner Surfperch 20 (19) (8) (13) (19) (17) (12) (9) (5) (14) (11) 0 San Pablo Bay Berkeley Waterfront Redwood City Oakland Inner Harbor Tomales/ Bodega Bay

  21. BRAIN HYPOTHALAMUS PITUITARY anterior posterior TRH circulation TSH Thyroid Gland impairedHPT Axis EDCs ? Altered T4 (T3) production altered physiology

  22. PBDEs and PCBs are implicated in thyroid endocrine disruption: …in mammalian studies, PBDE exposure causes reduction of thyroid hormone level and production (e.g., Skarman et al., 2005; Boas et al., 2006) …in fish, PBDE exposure causes reduction in T4, but not T3 (Tomy et al., 2004 –lake trout; Lema et al., 2006 –fathead minnow) …in fish, PCB exposure alters T4 and T3 levels (LeRoy et al., 2006 –Atlantic croaker)

  23. Reproductive Steroids

  24. Pacific Staghorn Sculpin Plasma 17β-Estradiol Concentrations 400 E2 (pg/ml) 300 200 N.D. for Testosterone (selected samples) 100 0 Female [winter] Female [summer] Male Male [winter] Female [immature] all SF Bay locations tested English Sole [Orange County] [n=13-29/bar]

  25. Shiner Surfperch ? August 2006 Oakland Inner Harbor

  26. 17α-Ethinylestradiol (EE2) in Fish Plasma 200 150 Plasma EE2 Concentration (pg/ml) 100 50 N.D. N.D. 0 Pacific Staghorn Sculpin Shiner Surfperch Turbot WWTP-affected site (Tomales Bay, Redwood City, Oakland Inner Harbor, Berkeley, San Pablo Bay (Loch Lohmand)

  27. PITUITARY The Growth Endocrine Axis Growth Hormone LIVER IGFBP-3 IGFBP-1 (IGFBPs 2,4-6) IGF-I IGFBP IGFBP IGF IGF “IGF Axis” IGF REC target cell GROWTH

  28. Jack Mackerel Trachurus symmetricus Stress Effects on Plasma IGFBP Levels Controls Stressed Rat Plasma Control 45 kDa 30 kDa IGFBP-1 30 kDa 28 kDa increased IGFBP-1 >> growth inhibition cell culture work supports this

  29. Endocrine Disruption—SF Bay Fish [Yellow=Year-1 fish analyses] * Cortisol & Cortisone * Thyroxine & Triidothyronine POTW, seasonal effects?? 17β-Estradiol & 17α-Ethinylestradiol Testosterone & 11-ketotestosterone ?! IGF-I & IGFBPs (June 2007) Hepatic contaminants (chlorinated pesticides, PCB congeners, PAHs) * =spatial differences detected

  30. Study Sites 2007July-August San Pablo Bay (Loch Lohmand Marina) Richmond(Laurentian Channel, DDTs) Berkeley Waterfront Oakland Inner Harbor San Leandro Bay(PCBs) Redwood City South of Dunbarton(POTW) far-field reference:Tomales Bay Bodega Bay

  31. Stress (HPI) Axis –Continuing Analyses 2007 Field season July-Aug 2007 • a) interrenal histology • b) hepatic contaminants correlation • c) ACTH-challenge* • d) cortisone measurement*(11β-HSD-2) • e) ectoparasitic infestation assessment  • f) growth endocrine system (IGF-I, IGFBPs) • g) steroidogenic enzyme expression*(StAR, 11β-hydroxylase, 11β-HSD-2) With an emphasis on Oakland Inner Harbor (San Pablo Bay, San Leandro Bay??) vs. control sites *b-d = potential bioassays for disruption (EDC screening?)

  32. Thyroid (HPT) Axis –Continuing Analyses 2007 Field season July-Aug 2007 • a) T3 measurement* • b) hepatic contaminants correlation • c) thyroid histology [?] • d) TSH-challenge* [?] • e) peripheral deiodinases (D1-3)* [?] • f) thyroid hormone receptors (TRα & TRβ)* [?] • g) growth endocrine system (IGF-I, IGFBPs) *b-d = potential bioassays for disruption (EDC screening?)

  33. ?? QUESTIONS

  34. Liver Contaminant Analysis, GC/MS So-Calif would have 4, 4’-DDT Nov. 2006

  35. Liver Contaminant Analysis, GC/MS Nov. 2006

  36. Liver Contaminant Analysis, GC/MS Nov. 2006

  37. Russell Fairey et al. Moss Landing Marine Laboratories

  38. Southern California Sea Grant Program San Francisco Estuary Institute

  39. steroidogenictargets Cortisone (inactive) cholesterol StAR, PBR mitochondria P450scc pregnenolone 17a-hydroxypregnenolone dehydroepiandrosterone progesterone 17a-hydroxyprogesterone androstenedione 11-deoxycorticosterone 11-deoxycortisol testosterone P45011b P450arom corticosterone cortisol estradiol-17b 11b-HSD-2 aldosterone

  40. Thyroxogenesis

  41. Stress!! Stress!! water quality handling crowding / captivity Stimulate the HPI Axis elevatedCORTISOLlevels Catabolic Pathways Anabolic Pathways ↑ Glucose, other fuels ↑ Hepatic glucose production ↑ AA release from muscle ↑ Lipid breakdown Overall:increased fuel mobilization & availability ↓Growth & Repair ↓Reproduction ↓Immune function Overall:reduced energy- expensive processes

  42. Elthusa californica . . . was commonly found in opercular chambers of shiner surfperch (staghorn sculpin, to lesser degree)

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