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Endocrine Regulation of the Reproduction in Crustaceans: Identification of Potential Targets for Toxicants and Environmental Contaminants

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Endocrine Regulation of the Reproduction in Crustaceans: Identification of Potential Targets for Toxicants and Environmental Contaminants Biologia 63/2: 139—150, 2008 Section Zoology DOI: 10.2478/s11756-008-0027-x Review Endocrine regulation of the reproduction in crustaceans: Identification of potential targets for toxicants and environmental contaminants Edita Mazurová1,KláraHilscherová1,4,RitaTriebskorn2,3,Heinz-R.Kohler¨ 2, Blahoslav Maršálek1,4 & Luděk Bláha1,4* 1Research Centre for Environmental Chemistry and Ecotoxicology (RECETOX), Masaryk University, Kamenice 3, CZ-62500 Brno, Czech Republic; e-mail: [email protected] 2Animal Physiological Ecology Department, Eberhard-Karls University, T¨ubingen, Germany 3Steinbeis-Transferzentrum f¨ur Okotoxikologie¨ und Okophysiologie,¨ Rottenburg, Germany 4Academy of Sciences of the Czech Republic, Institute of Botany, Brno, Czech Republic Abstract: Progress in ecotoxicological research documents that crustaceans are highly vulnerable to diverse chemicals and toxicants in the environment. In particular, pollutants affecting endocrine homeostasis in crustaceans (i.e., endocrine disrup- tors) are intensively studied, and serious reproductive disorders have been documented. In this review, current knowledge about the endocrine regulation of the crustacean reproduction is put together with the published ecotoxicological data with an attempt to summarize the potential of xenobiotics to affect crustacean reproduction. Following gaps and trends were identified: (1) Studies are required in the field of neurohormone (serotonin and dopamine) regulation of the reproduction and possible modulations by environmental toxicants such as antidepressant drugs. (2) Molting-related parameters (regulated by ecdysteroid hormones) are closely coordinated with the development and reproduction cycles in crustaceans (cross-links with methyl farnesoate signalling), and their susceptibility to toxicants should be studied. (3) Other biochemical targets for xenobiotics were recently discovered in crustaceans and these should be explored by further ecotoxicological studies (e.g., new information about ecdysteroid receptor molecular biology). (4) Some sex steroid hormones known from verte- brates (testosterone, progesterone) have been reported in crustaceans but knowledge about their targets (crustacean steroid receptors) and signalling is still limited. (5) Determination of the sex in developing juveniles (affecting the sex ratio in population) is a sensitive parameter to various xenobiotics (including endocrine disruptors) but its modulation by general environmental stress and non-specific toxicity should be further studied. Key words: crustaceans; reproduction; endocrine disruption; sex determination; contaminant; ecotoxicology Introduction (1) Reproduction processes are generally sensitive to various endogenous and exogenous factors includ- Available data provide a clear evidence that crustaceans ing total energy pool (e.g., food supplies), seasonal are vulnerable to diverse chemicals and toxicants in variations and environmental conditions (including pol- the environment (James & Boyle 1998; Olmstead & lution), detoxification metabolism and also hormonal LeBlanc 2007; Verslycke et al. 2007), thus a range of regulations at various levels. Studies that examine re- crustacean species is often used in ecotoxicological re- sponses of wildlife to complex polluted environment search. In particular, compounds and pollutants affect- often discussed developmental and reproduction toxi- ing endocrine homeostasis (i.e., endocrine disruptors) city. However, it may be often difficult to find direct are intensively studied also in crustaceans (Hutchin- links between unspecific effects and endocrine disrup- son 2002; LeBlanc 2007, Rodriguez et al. 2007). Se- tion caused by chemical pollution (Brian 2005; Zou rious reproductive disorders in crustaceans have been 2005). documented after exposure to such chemicals as in- (2) Other studies with crustaceans focus on known sects hormones and their mimics (Peterson et al. 2001) or suspected endocrine disruptors with the aim to ex- or vertebrate-like (xeno)hormones (Zou & Fingerman plore alteration of biological functions on biochemical 1997). Current approaches to study endocrine toxicol- and molecular levels. Several of such studies in crus- ogy of crustaceans include (1) studies with complex en- taceans add new information to mechanisms and path- vironmental mixtures with expected endocrine toxicity, ways previously described only in traditional insect and (2) controlled laboratory experiments with individ- and/or vertebrate models (Verslycke et al. 2002; Wu ual chemicals (suspected endocrine disruptors). et al. 2004; Kim et al. 2005a). * Corresponding author c 2008 Institute of Zoology, Slovak Academy of Sciences 140 E. Mazurová et al. Sinus gland/X-organ MOIH, MIH, GIH/VIH GIH/VIH ? Gonads MOIH ? Males: AGH ? MIH ? Serotonin ? Steroids (T) Dopamine? ? Mandibular organ Androgenic gland AGH MF Cerebral and Thoracic ganglia Y-organ Serotonin, Dopamine 20-HE MF ? CRUSTACEAN MF ? ENDOCRINE SYSTEM ENDOCRINE Adults: MF ? Juveniles: MF ? Testosterone ? Physiological Molting Development/ effects Ontogeny/Maturation Adults: reproduction activity Male sex development, control male reproduction Reproduction Reproduction cycle control; Adults: reproduction potency ? effects ? males in brood Juveniles: delay in maturation ? Fig. 1. The diagram of endocrine system in crustaceans with specific regard to regulation of reproduction. The individual glands and their active substances are described in the upper part, physiological and reproduction endpoints are depicted below. The complex of sinus gland and X-organ downregulates gonads directly by GIH/VIH (Gonads/Vitellogenesis Inhibiting Hormone), and it also regulates Y-organ by MIH (Molt-Inhibiting Hormone) and mandibular organ by MOIH (Mandibular Organ Inhibiting Hormone). Also the products of cerebral and thoracic ganglia (biogenic amines serotonin and dopamine) were found to affect gonadal activity but the mechanisms are not known (dashed lines/arrows). Mandibular organ produces methyl farnesoate (MF) that regulates gonads directly (variable effects depending on the maturity status), and it also indirectly affects molting (probably via signaling of 20-hydroxyecdysone, 20-HE). Further, product of the androgenic gland (Androgenic Gland Hormone, AGH) affects gonads and promotes development of male sexual characteristics. Competition for receptor sites has been discovered also between testosterone (T) and 20-HE. This review combines current knowledge on crus- since they may also play a role in reproduction pro- tacean endocrinology (with special respect to reproduc- cesses. tion, see Fig. 1) with data from selected ecotoxicolog- ical studies. We have focused on reproduction related Neurohormones produced by X-organ effects, as it is one of the most important biological Sinus gland is a neurohemal organ located laterally on processes associated with species fitness and population optic ganglia in eyestalks and it is connected to X-organ survival. Rather than summarization of many ecotox- via a dense nervous tissue. Both organs are paired and icological case studies, we have aimed to identify gen- they serve as a key endocrine junction of central neu- eral physiological targets in crustaceans vulnerable to rosecretory signals (Withers 1992). exogenous xenobiotics including endocrine disruptors. The peptide hormones released from X-organ have The review covers following major areas related to re- diverse effects on growth and reproduction: molt- production physiology and toxicity in crustaceans: (i) inhibiting hormone (MIH) suppresses production of neuroendocrine control of reproduction, (ii) role of clas- ecdysteroids in Y-organ; mandibular-organ inhibiting sical endocrine glands in reproduction, and (iii) sex de- hormone (MOIH) down-regulates excretion of methyl termination in crustaceans. farnesoate (MF) from mandibular gland; and gonad in- hibiting hormone (GIH, or according to some authors Neuroendocrine control of reproduction vitellogenin inhibiting hormone – VIH) represses ovar- ian maturation and testes growth (Chang 1993; Ohira To the present knowledge, neuroendocrine regulation et al. 1999). However, precise actions of separate neu- axis shares similar structure inside a broad Coelomates ropeptides are not yet fully understood since most of clade. In crustacean taxa, known secretory active sites the studies used whole organ homogenates or eyestalk include neurosecretory cells in cerebral and thoracic ablated animals (in which whole complex of sinus gland ganglion, sinus gland/X-organ complex, postcomissural and X-organ was removed). organ and pericardial organ (Cooke & Sullivan 1982). For example, the biochemical character of GIH is This chapter focuses first on the complex of sinus gland still a matter of discussion (Rodriguez et al. 2002a), and X-organ that were extensively studied, and they are and its structure seems to vary among species (Chaves functionally well characterized. Secondly, we summa- 2000). Therefore, factors with MIH/CHH/GIH effects rize functions of various biogenic amines in crustaceans were grouped into a peptide family of X-organ neuro- Ecotoxicology of crustacean reproduction 141 hormones but their precise structural variability and growth. This stimulation was further promoted by ad- detailed physiological effects remain to be investigated ditions of methionine enkephaline (M-ENK; a ligand of (Chang 1993). opioid receptor known to stimulate serotonin synthesis). Molt-inhibiting hormone (MIH) inhibits the pro- Contrary, oocyte growth was inhibited by naxolone,
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