Neuroendocrine Disruption: More Than Hormones are Upset

Figures & data

TABLE 1 In Vivo Neuroendocrine Disruption Observed in Vertebrates by Pharmaceuticals and Personal Care Products Released in Municipal Effluents and Detected in the Environment

Disruptor	Species	Effect	Treatment
Ethynylestradiol	Xenopus tropicalis	Decreased ER-α expression in brain, skewed female sex ratio with females lacking oviduct	1–100 nM waterborne (Pettersson et al. 2006)
	Danio rerio	Differential expression changes in liver and tel measured by microarray	10 ng/L waterborne, males (Martiniuk et al. 2007)
	Carassius auratus	Increased CYP19B expression in hyp and tel	10 ng/L waterborne, males (Martiniuk et al. 2006)
	Oryzias latipes	Decreased GnRH-R in brain	5000 ng/L waterborne, males (Zhang et al. 2008a)
		Decreased AR-α in brain, impaired sexual behavior	5 ng/L waterborne, males (Zhang et al. 2008a)
	Oreochromis niloticus	Decreased IGF-1 expression in female brain	125 μg/g b.w. dietary (Shved et al. 2007)
		Normal IGF-1 expression patterns disrupted in males and females, normal ER-α expression patterns disrupted in males and suppressed in females	5 and 25 ng/L waterborne (Shved et al. 2008)
Fadrozole	C. auratus	Differential gene expression in hyp and tel measured by microarray. Downregulation of CYP19B in hyp and tel	50 μg/L waterborne, females (Zhang et al. 2009)
Clotrimazole	X. tropicalis	Decreased CYP19 activity in brain of developing tadpoles	375 nM waterborne (Gyllenhammar et al. 2009)
Ketoconazole	O. latipes	Decreased GnRH-R expression in brain	3–300 μg/L females (Zhang et al. 2008b)
SSRIs	vertebrates	Neuroendocrine disruption	(Mennigen et al. 2011)
Note. Hyp, hypothalamus, Tel, telencephalon, GnRH-R, GnRH receptor, IGF-1, insulin-like growth factor 1, ER-α, estrogen receptor alpha, AR-α, androgen receptor alpha, CYP19B, aromatase B, and SSRI, selective serotonin reuptake inhibitor.

TABLE 2 In Vivo Neuroendocrine Disruption Observed in Vertebrates by Chlorinated Pesticides

Disruptor	Species	Effect	Treatment
Atrazine	Rattus norvegicus	Loss of brain-stimulated release of prolactin, inhibition of LH and FSH	200 mg/kg/d dietary, females (Goldman et al. 1999)
	Coturnix japonica	Increased GnRH, nonsignificant positive trend with increased exposure	0.5, 5, 50 μg injections to eggs (Ottinger et al. 2009)
Methoxychlor	R. norvegicus	Disrupted prolactin secretory patterns via inhibition of DA in hyp, decreased circulating LH	25 mg/kg/d dietary, females (Lafuente et al. 2000)
		Increased NA and disrupted 5-HT levels in different parts of hyp	25 mg/kg/d dietary, females (Lafuente et al. 2008)
	C. japonica	Increased GnRH in 5 ppm treated males, 0.5 ppm treated females	0.5 and 5 ppm dietary (Ottinger et al. 2005)
		Reduced NA and adrenalin in affected individuals	0.5 and 5 ppm dietary, females (Ottinger et al. 2009)
	Mus domesticus	Female offspring displayed typical male exploratory behavior, decreased D1-like receptor density in nucleus accumbens and olfactory tubercle.	20 μg/kg/d dietary to mothers (Panzica et al. 2007
Vinclozolin	Oryctolagus cuniculus	Fewer GnRH neurons and increased calbindin neurons in reproductive brain centres of offspring	10 mg/kg/d dietary to mothers (Bisenius et al. 2006)
		Decreased FSH and impaired sexual behavior and loss of pituitary GnRH sensitivity in male pups	7.2 and 72 mg/kg/d dietary to mothers (Veeramachaneni et al. 2006)
	C. japonica	Disruption to GnRH levels	25, 50, amd100 ppm injection to eggs (McGary et al. 2001)
Prochloraz	Oryzias latipes	Decreased GnRH, GnRH-R, and CYP19 in brain, reduced fecundity	3–300 μg/L waterborne to females (Zhang et al. 2008b)
Dieldrin	Micropterus salmoides	Transcriptomic and proteomic changes in hyp	10 mg/kg injections (Martyniuk et al. 2010a)
		Decreased ER-β expression in hyp	2.95 ppm dietary (Martyniuk et al. 2010b)
Note. GnRH, gonadotropin-releasing hormone, Hyp, hypothalamus, Tel, telencephalon, GnRH-R, GnRH receptor, DA, dopamine, 5-HT, serotonin, LH, luteinizing hormone, FSH, follicle-stimulating hormone, NA, noradrenaline, and ER-β, estrogen receptor beta.

TABLE 3 In Vivo Neuroendocrine Disruption Observed in Vertebrates by Industrial Contaminants

Disruptor	Species	Effect	Treatment
Cadmium	R. norvegicus	Disruption of DA, 5-HT, and NA in different brain regions, and disruption of FSH, LH, ACTH, prolactin, and TSH, depending on route, dose, and time of exposure	(Lafuente et al. 2000a; Lafuente et al. 2000b; Lafuente et al. 2001a; Lafuente et al. 2001b; Lafuente et al. 2003)
	M. salmoides	Increased GnRH in whole brain	67 ng/kg Injection, males (Martiniuk et al. 2009)
Cadmium and lead	R. norvegicus	Decreased DA and 5-HT from cadmium recovered when treated with both lead and cadmium at the same time. NA decreased by lead, cadmium, and lead and cadmium. Decreased LH and FSH from cadmium and cadmium and lead exposures.	0.05 mg/kg injection, females (Pillai et al. 2003)
Methylmercury	Neovison vison	Disruption of GABA levels
	fish	Neuroendocrine control of reproduction, neurotransmitter systems	0.1–2 ppm dietary, males (Basu et al. 2010) (Castoldi et al. 2001; Johansson et al. 2007; Crump and Trudeau 2009)
PCBs	R. norvegicus	Disruption to DA, glutamate, GABA, 5-HT and others.	(Fonnum and Mariussen 2009)
Pulp and paper mill effuents	C. auratus	Disruption of DA, GABA, glutamate systems	In vitro (Basu et al. 2009)
	Pimephales promelas	Differential gene expression in hypothalamus measured by microarray	100% effluent exposure, females (Popesku et al. 2010)
Note. DA, dopamine, 5-HT, serotonin, NA, noradrenaline, FSH, follicle-stimulating hormone, LH, luteinizing hormone, ACTH, adrenocorticotropic hormone, TSH, thyroid-stimulating hormone, GABA, gamma-aminobutyric acid.

TABLE 4 Evidence of Neuroendocrine Disruption in Invertebrates

Disruptor	Species	Effect	Treatment
Cadmium	Lymnaea palustris	Disrupted calcium currents in nerve collar neurons	1 mg/L waterborne (Szucs et al. 1994)
	L. stagnalis	Inhibition GABA-activated chloride currents via increased calcium levels in nerve collar cells	In vitro, 50 μM cell perfusion (Molnár et al. 2004)
	Uca pugilator	Blocking of NA-stimulated release of light-adapting hormone	10 mg/L waterborne (Reddy et al. 1997a)
		Inhibition of PDH synthesis	8.5 mg/kg injection (Reddy and Fingerman 1995)
	Procambarus clarkii	Increased release of GIH	1 mg/L waterborne (Rodríguez et al. 2000)
		Acetylcholinesterase inhibition	5 ppm waterborne (Devi and Fingerman 1995)
	Chasmagnathus granulata	Inhibited GIH release	0.5 mg/L waterborne (Medesani et al., 2004)
Municipal effluents	Elliptio complanata	Decreased 5-HT and DA, increased MAO activity in nerve ganglia	Injections and exposure to plume (Gagné and Blais, 2003)
		Decreased MAO and 5-HT transporter activity, increased DAT activity in nerve ganglia	Exposure to plume (Gagné and Blais, 2007)
		Increased DA, 5-HT, increased DAT, MAO, and COX activity, decreased 5-HT transporter activity	Direct exposure to aeration lagoon (Gagné and Blais, 2007)
		Decreased GABA, decreased GAD and MAO activity, increased 5-HT, DA, increased 5-HT transporter, DAT, and acetylcholinesterase activity; effects not mitigated by ozone treatment	Direct exposure to primary and ozone-treated effluents (Gagné et al., 2007)
PCBs	U. pugilator	Suppressed NA release from neural tissue, inhibiting PDH release from sinus gland	Injection of Aroclor 1242 (Hanumante et al. 1981)
Naphthalene	U. pugilator	Suppressed NA release from neural tissue, inhibiting PDH release from sinus gland	Injection (Staub and Fingerman 1984)
	P. clarkii	Suppression of GSH release	10 mg/L waterborne (Sarojini et al. 1994)
Copper	Palaemon elegans	CHH release and hyperglycemia, triggered by 5-HT stimulation	5 mg/L waterborne (Lorenzon et al., 2004; Lorenzon et al., 2005)
	C. granulata	Inhibited GIH release	0.1 mg/L waterborne (Medesani et al., 2004)
Mercury	P. elegans	CHH release and hyperglycemia	5 mg/L waterborne (Lorenzon et al., 2004)
	P. clarkii	Inhibition of 5-HT stimulated release of GSH	0.5 mg/kg injection (Reddy et al. 1997b)
		Acetylcholinesterase inhibition	0.2 ppm waterborne (Devi and Fingerman 1995)
Lead	P. clarkii	Acetylcholinesterase inhibition	100 ppm waterborne (Devi and Fingerman 1995)
Organophosphates and organocarbamates	crustaceans	Acetylcholinesterase inhibition	(Rapetto et al. 1988; Surendranath et al. 1990; Reddy et al. 1990)
Azadirachtin	insects	Blocked release of neurosecretory material, disruption of acetylcholine, GABA, and increased 5-HT	(Mordue and Blackwell 1993)
	Labidura riparia	Disruption of allatostatins, which inhibit JH synthesis	0.5, 1, 2, and 3 μg injection (Sayah et al. 1998)
Note. DA, dopamine, 5-HT, serotonin, NA, noradrenaline, FSH, follicle-stimulating hormone, LH, luteinizing hormone, ACTH, adrenocorticotropic hormone, TSH, thyroid-stimulating hormone, GABA, gamma-aminobutyric acid, PDH, pigment-dispersing hormone, GIH, gonad-inhibiting hormone, GSH, gonad-stimulating hormone, MAO, monoamine oxidase, DAT, dopamine transporter, COX, cyclooxygenase, CHH, crustacean hyperglycemic hormone, and JH, juvenile hormone.

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