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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
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essential physiological functions
ENDOCRINE SYSTEMS regulate essential physiological functions Reproduction - Growth & Repair - Metabolism Defense/Immune - Thyroid - Developmental Stress Responses - Neuroendocrine - others Homeostasis, Adaptation, Survival
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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
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. . . 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
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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
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Pacific Staghorn Sculpin Leptocottus armatus
Shiner Surfperch Cymatogaster aggregata Pacific Staghorn Sculpin Leptocottus armatus
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2006 Field Sites San Pablo Bay Berkeley Waterfront
Oakland Inner Harbor Redwood City far-field reference: Tomales Bay Bodega Bay
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Far Field Sites Bodega Bay Tomales Bay
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STRESS RESPONSE AXIS
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adaptational responses
Stress! Hypothalamo- Pituitary- Interrenal Axis (HPI Axis) BRAIN HYPOTHALAMUS CRH PITUITARY anterior posterior ACTH Interrenal tissues circulation ↑↑CORTISOL adaptational responses
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Plasma Cortisol Concentration (ng/ml)
Stress Response Shiner Surfperch a a 1200 b Plasma Cortisol Concentration (ng/ml) b 800 400 21 13 21 10 Oakland Inner Harbor Berkeley Waterfront San Pablo Bay Redwood City
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Plasma Cortisol Concentration (ng/ml)
Stress Response Pacific Staghorn Sculpin a a 1200 Plasma Cortisol Concentration (ng/ml) 800 b 400 c 17 16 13 19 Oakland Inner Harbor Berkeley Waterfront San Pablo Bay Redwood City
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REDUCED cortisol response
STRESSOR impaired HPI Axis BRAIN HYPOTHALAMUS CRH PITUITARY anterior posterior ACTH Interrenal tissues circulation EDCs ? REDUCED cortisol response
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(Quabius et al., 2005; Vijayan et al., 2006)
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)
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THYROID ENDOCRINE SYSTEM
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variety of physiological actions
Hypothalamo- Pituitary- Thyroid Axis (HPT Axis) BRAIN HYPOTHALAMUS TRH PITUITARY anterior posterior TSH Thyroid gland circulation T4 , T3 variety of physiological actions
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Thyroid Hormones T4 T3 broad physiological actions
3,5,3’,5’-tetraiodothyronine (thyroxine) 3,5,3’-triiodothyronine broad physiological actions essential for brain/neural development permissive to somatic growth important regulators of metabolism
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Thryoxine (T4) Levels in Shiner Surfperch
80 Shiner Surfperch Plasma Thyroxine (T4) Concentration, ng/ml 60 40 20 (11) (19) (19) (9) (14) San Pablo Bay Berkeley Waterfront Redwood City Oakland Inner Harbor Bodega Bay
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Thryoxine (T4) Levels in Pacific Staghorn Sculpin
80 Plasma Thyroxine (T4) Concentration, ng/ml 60 40 20 (8) (13) (17) (12) (5) San Pablo Bay Berkeley Waterfront Redwood City Oakland Inner Harbor Tomales Bay
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Thryoxine (T4) Levels in SF Bay Fish
100 80 Pacific Staghorn Sculpin Plasma Thyroxine (T4) Concentration, ng/ml 60 40 20 Shiner Surfperch (8) (11) (13) (19) (17) (19) (12) (9) (5) (14) San Pablo Bay Berkeley Waterfront Redwood City Oakland Inner Harbor Tomales/ Bodega Bay
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EDCs ? impaired HPT Axis altered physiology Altered T4 (T3) production
BRAIN HYPOTHALAMUS TRH PITUITARY anterior posterior TSH Thyroid Gland circulation EDCs ? Altered T4 (T3) production altered physiology
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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)
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Reproductive Steroids
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Plasma 17β-Estradiol Concentrations
Pacific Staghorn Sculpin 400 E2 (pg/ml) 300 200 N.D. for Testosterone (selected samples) 100 Female [winter] Female [summer] Male [winter] Female Male [immature] all SF Bay locations tested English Sole [Orange County] [n=13-29/bar]
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Shiner Surfperch ? August Oakland Inner Harbor
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Pacific Staghorn Sculpin
17α-Ethinylestradiol (EE2) in Fish Plasma 200 150 Plasma EE2 Concentration (pg/ml) 100 50 N.D. N.D. Turbot WWTP-affected site Shiner Surfperch Pacific Staghorn Sculpin (Tomales Bay, Redwood City, Oakland Inner Harbor, Berkeley, San Pablo Bay (Loch Lohmand)
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The Growth Endocrine Axis
PITUITARY The Growth Endocrine Axis Growth Hormone LIVER IGFBP-3 IGFBP-1 (IGFBPs 2,4-6) IGF-I IGFBP IGFBP “IGF Axis” IGF IGF IGF REC target cell GROWTH
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Stress Effects on Plasma IGFBP Levels
Jack Mackerel Trachurus symmetricus 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
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* * * ?! Endocrine Disruption—SF Bay Fish POTW, seasonal effects??
[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
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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
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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?)
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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?)
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?? QUESTIONS
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Liver Contaminant Analysis, GC/MS
Selected Contaminants* Shiner Surfperch Pacific Staghorn Sculpin Chlordane-gamma 1 – 4 2 – 5 Chlordane-alpha 3.5 – 15 6 – 10 trans-Nonachlor 3.5 – 12 5 – 20 cis-Nonachlor 1.5 – 5 4 – 13 4,4’-DDE 20 – 47 48 – 54 *range of ng/g wet weight values shown So-Calif would have 4, 4’-DDT Nov. 2006
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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: 28, 31, 44, 49, 52, 66, 70, 74, 87, 99,101, 105, 110, 118, , 141, 151, 156, 158, , 170, 177, 183, 187, 200 1 – 16 2 – 35 *range of ng/g wet weight values shown Nov. 2006
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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
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Russell Fairey et al. Moss Landing Marine Laboratories
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Southern California Sea Grant Program San Francisco Estuary Institute
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steroidogenic targets
cholesterol StAR, PBR mitochondria P450scc pregnenolone 17a-hydroxypregnenolone dehydroepiandrosterone progesterone 17a-hydroxyprogesterone androstenedione 11-deoxycorticosterone 11-deoxycortisol testosterone P45011b P450arom corticosterone cortisol estradiol-17b Cortisone (inactive) 11b-HSD-2 aldosterone
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Thyroxogenesis
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Stress!! Stress!! expensive processes Catabolic Pathways
handling crowding / captivity water quality Stimulate the HPI Axis elevated CORTISOL levels 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
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Elthusa californica . . . was commonly found in opercular chambers of shiner surfperch (staghorn sculpin, to lesser degree)
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