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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 - Metabolism Defense/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 established between 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 RESPONSE AXIS Stress! BRAIN HYPOTHALAMUS CRH PITUITARY anterior posterior circulation HypothalamoPituitaryInterrenal Axis (HPI Axis) ACTH Interrenal tissues ↑↑CORTISOL adaptational responses Stress Response Shiner Surfperch a Plasma Cortisol Concentration (ng/ml) a 1200 b b 800 400 21 13 21 10 Berkeley Waterfront San Pablo Bay 0 Redwood City Oakland Inner Harbor Plasma Cortisol Concentration (ng/ml) Stress Response a a 1200 Pacific Staghorn Sculpin 800 b 400 c 17 16 13 Redwood City Oakland Inner Harbor Berkeley Waterfront 19 0 San Pablo Bay STRESSOR impaired BRAIN HPI Axis HYPOTHALAMUS CRH PITUITARY anterior posterior circulation ACTH Interrenal tissues 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) THYROID ENDOCRINE SYSTEM BRAIN HYPOTHALAMUS TRH PITUITARY anterior posterior circulation HypothalamoPituitaryThyroid Axis (HPT Axis) TSH Thyroid gland T4 , T3 variety of physiological actions Thyroid Hormones T4 3,5,3’,5’-tetraiodothyronine (thyroxine) T3 3,5,3’-triiodothyronine • broad physiological actions • essential for brain/neural development • permissive to somatic growth • important regulators of metabolism Concentration, ng/ml Plasma Thyroxine (T4) Thryoxine (T4) Levels in Shiner Surfperch 80 Shiner Surfperch 60 40 20 0 (11) (19) (19) San Pablo Bay Berkeley Waterfront Redwood City (9) Oakland Inner Harbor (14) Bodega Bay Concentration, ng/ml Plasma Thyroxine (T4) Thryoxine (T4) Levels in Pacific Staghorn Sculpin Pacific Staghorn Sculpin 80 60 40 20 0 (8) San Pablo Bay (13) (17) Berkeley Waterfront Redwood City (12) Oakland Inner Harbor (5) Tomales Bay Thryoxine (T4) Levels in SF Bay Fish Concentration, ng/ml Plasma Thyroxine (T4) 100 80 Pacific Staghorn Sculpin 60 40 Shiner 20 0 (8) (11) San Pablo Bay (13) (19) Berkeley Waterfront (17) (19) Redwood City (12) (9) (5) (14) Oakland Tomales/ Bodega Inner Harbor Bay Surfperch BRAIN impaired HYPOTHALAMUS HPT Axis TRH PITUITARY anterior posterior circulation TSH Thyroid Gland 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) Reproductive Steroids Plasma 17β-Estradiol Concentrations E2 (pg/ml) 400 300 Pacific Staghorn Sculpin 200 N.D. for Testosterone (selected samples) 100 0 Female [winter] Female [summer] Male [winter] English Sole [Orange County] [n=13-29/bar] Male Female [immature] all SF Bay locations tested August 2006 Oakland Inner Harbor Shiner Surfperch ? 17α-Ethinylestradiol (EE2) in Fish Plasma Plasma EE2 Concentration (pg/ml) 200 150 100 50 N.D. N.D. 0 Turbot WWTP-affected site Shiner Surfperch Pacific Staghorn Sculpin (Tomales Bay, Redwood City, Oakland Inner Harbor, Berkeley, San Pablo Bay (Loch Lohmand) The Growth Endocrine Axis PITUITARY Growth Hormone LIVER IGFBP-3 IGFBP-1 IGF-I (IGFBPs 2,4-6) IGFBP “IGF Axis” IGF IGF IGF REC target cell GROWTH Jack Mackerel Trachurus symmetricus Stress Effects on Plasma IGFBP Levels 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 17β-Estradiol & 17α-Ethinylestradiol Testosterone & 11-ketotestosterone ?! POTW, seasonal effects?? IGF-I & IGFBPs (June 2007) Hepatic contaminants (chlorinated pesticides, PCB congeners, PAHs) =spatial differences detected Study Sites 2007 July-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?) ?? QUESTIONS Liver Contaminant Analysis, GC/MS Selected Contaminants* Shiner Surfperch Pacific Staghorn Sculpin Chlordane-gamma 1–4 Chlordane-alpha 3.5 – 15 2–5 6 – 10 trans-Nonachlor cis-Nonachlor 4,4’-DDE 3.5 – 12 1.5 – 5 20 – 47 5 – 20 4 – 13 48 – 54 *range of ng/g wet weight values shown So-Calif would have 4, 4’-DDT Nov. 2006 Liver Contaminant Analysis, GC/MS Selected Contaminants* Shiner Surfperch Pacific Staghorn Sculpin PCB 095 6 – 12 8 – 14 PCB 149 11 – 35 25 – 35 PCB 138 27 – 70 56 – 63 PCB 180 14 – 47 28 – 58 PCB 194 nd – 8 6 – 21 PCB 153 27 – 66 56 – 68 Other congeners measured: 1 – 16 28, 31, 44, 49, 52, 66, 70, 74, 87, 99,101, 105, 110, 118, 128+167, 141, 151, 156, 158, 168+132, 170, 177, 183, 187, 200 2 – 35 *range of ng/g wet weight values shown Nov. 2006 Liver Contaminant Analysis, GC/MS Selected Contaminants* Shiner Surfperch Pacific Staghorn Sculpin Naphthalene 13 – 19.5 15 – 20 2-methylnaphthalene 9 – 15 6 – 17 1-methylnaphthalene 5 – 13 6–8 Biphenyl 1 – 5.5 2–5 Fluorine 2.5 – 11 3.5 – 5 Phenanthrene 6.5 – 11 6.5 – 8 *range of ng/g wet weight values shown Nov. 2006 Russell Fairey et al. Moss Landing Marine Laboratories Southern California Sea Grant Program San Francisco Estuary Institute steroidogenic targets cholesterol mitochondria StAR, PBR P450scc pregnenolone progesterone 17a-hydroxypregnenolone dehydroepiandrosterone 17a-hydroxyprogesterone 11-deoxycorticosterone 11-deoxycortisol P45011b corticosterone aldosterone cortisol 11b-HSD-2 Cortisone (inactive) androstenedione testosterone P450arom estradiol-17b Thyroxogenesis Stress!! Stress!! handling water quality crowding / captivity Stimulate the HPI Axis elevated CORTISOL levels Catabolic Pathways ↑ Glucose, other fuels ↑ Hepatic glucose production ↑ AA release from muscle ↑ Lipid breakdown increased fuel mobilization & availability Overall: Anabolic Pathways ↓Growth & Repair ↓Reproduction ↓Immune function Overall: reduced energyexpensive processes Elthusa californica . . . was commonly found in opercular chambers of shiner surfperch (staghorn sculpin, to lesser degree)