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Study assessing endocrine disruption in San Francisco Bay fishes, focusing on stress responses, growth, thyroid, and reproduction regulations. Explore correlations between contaminants and disruption types.
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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
ENDOCRINE SYSTEMS regulate essential physiological functions Reproduction - Growth & Repair - MetabolismDefense/Immune - Thyroid - Developmental Stress Responses - Neuroendocrine - others Homeostasis, Adaptation, Survival
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
. . . 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
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
Shiner Surfperch Cymatogaster aggregata Pacific Staghorn Sculpin Leptocottus armatus
2006 Field Sites San Pablo Bay Berkeley Waterfront Oakland Inner Harbor Redwood City far-field reference:Tomales Bay Bodega Bay
Far Field Sites Bodega Bay Tomales Bay
Stress! BRAIN HYPOTHALAMUS PITUITARY anterior posterior CRH circulation ACTH Interrenal tissues adaptational responses Hypothalamo- Pituitary- Interrenal Axis (HPI Axis) ↑↑CORTISOL
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
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
STRESSOR BRAIN HYPOTHALAMUS PITUITARY anterior posterior CRH circulation ACTH Interrenal tissues impairedHPI Axis EDCs ? REDUCED cortisol response
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)
BRAIN HYPOTHALAMUS PITUITARY anterior posterior TRH circulation TSH Thyroid gland variety of physiological actions Hypothalamo- Pituitary- Thyroid Axis (HPT Axis) T4 , T3
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)
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
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
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
BRAIN HYPOTHALAMUS PITUITARY anterior posterior TRH circulation TSH Thyroid Gland impairedHPT Axis EDCs ? Altered T4 (T3) production altered physiology
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)
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]
Shiner Surfperch ? August 2006 Oakland Inner Harbor
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)
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
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
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
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
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?)
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?)
Liver Contaminant Analysis, GC/MS So-Calif would have 4, 4’-DDT Nov. 2006
Liver Contaminant Analysis, GC/MS Nov. 2006
Liver Contaminant Analysis, GC/MS Nov. 2006
Southern California Sea Grant Program San Francisco Estuary Institute
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
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
Elthusa californica . . . was commonly found in opercular chambers of shiner surfperch (staghorn sculpin, to lesser degree)