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The Society for Integrative and Comparative Biology
Endocrine-like Signaling in Cnidarians: Current Understanding and Implications for Ecophysiology1
1 Department of Biology, Woods Hole Oceanographic Institution, 45 Water Street, MS-32, Woods Hole, Massachusetts 02543
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The vertebrate endocrine system is well-characterized, with many reports of disruption by environmental chemicals. In contrast, cnidarians are less compartmentalized, physiological regulation is poorly understood, and the potential for disruption is unknown. Endocrine-like activity has not been systematically studied in cnidarians, but several classical vertebrate hormones (e.g., steroids, iodinated organic compounds, neuropeptides, and indoleamines) have been identified in cnidarian tissues. Investigators have made progress in identifying putative bioregulatory molecules in cnidarians, and testing the effects of these individual compounds. Less progress has been made in elucidating signaling pathways. For example, putative gonadotropin-releasing hormone and sex steroids have been identified in cnidarian tissues, but it is unknown whether these compounds are components of a larger signal cascade comparable to the vertebrate hypothalamic-pituitary-gonadal axis. Further, while sex steroids and iodinated organic compounds may help to regulate cnidarian physiology, the mechanisms of action are unknown. Homologs to the vertebrate steroid and thyroid receptors have not been identified in cnidarians, so more research is needed to understand the mechanisms of endocrine-like signaling in cnidarians. Elucidation of cnidarian regulatory pathways will provide insight into evolution of hormonal signaling. These studies will also improve understanding of how cnidarians respond to environmental cues and will provide a basis to investigate disruption of physiological processes by physical and chemical stressors.
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INTRODUCTION |
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Metazoan animals include organisms with a rich diversity of body plans and a broad range in the degree of compartmentalization and intraorganismal communication. The vertebrate endocrine system is an exquisite example of compartmentalization and communication. Specialized cells and organs secrete tens to hundreds of distinct bioregulatory molecules, or hormones, that travel through the circulatory system and regulate physiological processes in target organs and tissues. Similarly, many invertebrates possess discrete endocrine organs that share some functions with corresponding organs in vertebrates. Among invertebrates, endocrine function has been most extensively studied in arthropods, particularly insects (Segal, 1993
; Karlson, 1996; Klowden, 2003; Swevers and Iatrou, 2003).
Comparatively little is known about endocrine-like bioregulation in cnidarians. In contrast to vertebrates, cnidarian cells are differentiated into tissues but are not generally organized into organs or systems. The cnidarian homolog of the nervous system is a nerve net that is largely ectodermal. Cnidarians contain chemical synapses and release neurotransmitters, including biogenic amines and peptides (reviewed by LeRoith et al., 1986; Grimmelikhuijzen et al., 1996; Grimmelikhuijzen and Westfall, 1995; Schmich et al., 1998). Because the nerve net can be identified as a distinct structure with associated signal molecules, bioregulation in cnidarians, and to some degree other invertebrates, has been considered to be primarily neurochemical (LeRoith et al., 1986); however, a diversity of potential signal molecules have been identified in cnidarians. The mechanism of action for many of these compounds in cnidarians is unknown. In contrast to the specialized endocrine organs and closed circulatory system found in vertebrates, cnidarians contain a variety of secretory cells (e.g., cnidocytes), and circulation occurs via diffusion. While these characteristics might imply limited or simple chemical signaling processes, the scope of neuroendocrine-like activity has not been investigated systematically in cnidarians.
Several compounds that have been described as vertebrate hormones either occur in cnidarians, are biologically active in cnidarians, or have cnidarian homologs. To illustrate this, Table 1 was adapted from a table entitled "Principal Hormones of Vertebrates" (Beaulieu, 1990). For each compound I have listed known occurrences of the hormones or related compounds and evidence of biological activity in cnidarians. In some cases, particularly when a compound has not been detected or has not been studied in cnidarians, I have listed occurrences in other invertebrates. Several compounds similar or identical to vertebrate hormones are present in cnidarians, but these compounds do not necessarily function in the same way. In addition, some cnidarian compounds (e.g., palytoxin, anthopleurin) are distinct from vertebrate hormones but can affect vertebrate hormone signaling pathways (Shibata et al., 1976; Lazzaro et al., 1987).
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A greater understanding of endocrine-like bioregulation in cnidarians is necessary to maximize the effectiveness of conservation programs, such as current efforts to protect and restore coral reefs. While a comparative approach can provide considerable insight into cnidarian physiology, it is potentially limiting because cnidarians and other invertebrates have evolved unique solutions to environmental demands. For example, specific terpenoids and unsaturated fatty alcohols have been identified as sperm attractants for an alcyonacean soft coral (Coll et al., 1995
) and a scleractinian coral (Coll et al., 1994).
Diversity of reproductive modes
In vertebrates, reproductive processes such as development of reproductive organs and gametes are controlled by a network of chemical signals within the endocrine system; these chemical signals may be mimicked or blocked, resulting in endocrine disruption (McLachlan, 2001). Chemical signals regulating cnidarian reproduction have not be elucidated, so the potential for disruption is currently unknown. Cnidarians exhibit a diversity of reproductive modes, so comparison of bioregulatory pathways among cnidarians will be of particular interest.
Cnidarians may reproduce asexually to form new individuals or colonies with varying degrees of integration; indeed for many species, asexual propagation is the primary mode of reproduction (Galliot and Schmid, 2002). The relative importance of sexual and asexual reproduction can vary greatly even between closely related taxa. Trade-offs between somatic tissue growth, skeletal growth, asexual reproduction and sexual reproduction have been described in many species, but the biochemical or molecular regulation of these processes has not been described. For example, fragmentation in scleractinian corals can reduce fecundity in polyps surrounding the damaged region or even entire coral colonies, by an unknown mechanism (Van Veghel and Bak, 1994; Rinkevich, 1996; but see also Ward, 1995).
Modes of sexual reproduction in cnidarians are diverse and include brooding larvae and broadcast spawning, simultaneous and sequential hermaphroditism, and gonochorism (Richmond and Hunter, 1990; Galliot and Schmid, 2002). One study has identified a gene in the hermaphroditic coral Acropora millepora (AmDM1) that is homologous to DM domain-containing proteins important to sex determination in other animals (Miller et al., 2003). It is yet unknown what role AmDM1 or other proteins play in the development of hermaphroditic versus gonochoric taxa.
Sexual reproduction of scleractinian corals has received considerable attention because some reef-building corals participate in dramatic multi-species mass-spawning events. Environmental signals for coral gametogenesis and spawning, such as water temperature, photoperiod, lunar illumination and tidal cycles have been described (Jokiel and Guinther, 1978; Richmond and Jokiel, 1984; Jokiel et al., 1985; Babcock et al., 1986; Hunter, 1988; Richmond and Hunter, 1990; Beauchamp, 1993), but it is not known how these environmental signals are biochemically transduced to create physiological responses, such as egg development or spawning.
Model organisms
Few bioregulatory molecules have been systematically studied across cnidarian classes. Studies of cnidarian biochemistry and physiology have generally used organisms that are easy to manipulate experimentally, lack a mineralized skeleton, and/or are available near temperate laboratories. Discussion of organisms commonly used in physiological experiments and some of the implications and consequences of those selections follows.
Hydrozoa
Hydras have historically been used as model organisms for studies of cellular differentiation, regeneration and morphogenesis (see Hassel et al., 1996; Martin et al., 1997; Plickert et al., 2003; Frank et al., 2001 and references therein). Existing inbred strains with varied reproductive characteristics (Martin et al., 1997) may provide insight into the biochemical and underlying molecular control of sexual and asexual reproduction. In addition, a suite of neuropeptides that can induce morphological changes, such as ectopic head or foot formation, have been identified and characterized in hydrozoans (Leitz et al., 1994). Hydras are comparable to other invertebrate model organisms, such as Drosophila melanogaster and Caenorhabditis elegans, in the sense that they grow rapidly, may be maintained relatively easily in the laboratory and are relatively well-characterized at cellular, biochemical and/or molecular levels. While there are considerable advantages to working with such organisms, one of the main disadvantages is that bioregulatory processes in hydras may not be representative of other cnidarians. In particular, D. melanogaster, C. elegans and hydras such as Hydra vulgaris are all considered highly derived organisms within their respective phyla (Bolker, 1995).
Scyphozoa and cubozoa
Jellyfish (medusae, which may be hydrozoan, scyphozoan or cubozoan) are important both as predators and prey in pelagic ecosystems. Jellyfish aggregations or blooms are common episodic events on local scales, and the global occurrence and severity of blooms may be increasing (Mills, 2001). Blooms are caused and maintained by a combination of physical and poorly understood behavioral and physiological processes (Lotan et al., 1994; Purcell et al., 2000; Graham et al., 2001; Lucas, 2001). In spite of their ecological importance, fewer studies of chemical signaling have been conducted in scyphozoans and cubozoans relative to other cnidarian taxa, which may reflect logistic limitations. Scyphozoans have been used in studies of chemical induction of metamorphosis (Walther and Fleck, 1998). Cubozoan jellyfish have also been studied in an evolutionary context some similarities in regulation of photoreceptor development have been observed between cubozoa and bilaterian animals (reviewed in Tomarev and Piatigorsky, 1996).
Anthozoa
Several modern studies indicate that this class is basal within the phylum Cnidaria (Bridge et al., 1992, 1995; Odorico and Miller, 1997), and several taxa are useful as models. It has been proposed that the most recent common ancestor between cnidarians and bilaterians would have been morphologically similar to a pennatulacean anthozoan (Dewel, 2000). Scleractinian corals, such as Acropora millepora, have been proposed as useful model organisms in part due to accessibility of their externally developing larvae released during mass-spawning events (Miller and Ball, 2000). An Acropora millepora EST database has been constructed (Ball et al., 2002). The starlet sea anemone, Nematostella vectensis is particularly useful as a model organism because it is readily available, it grows rapidly, and its reproductive cycle can be easily manipulated to obtain weekly spawning (Hand and Uhlinger, 1992; Fritzenwanker and Technau, 2002). As a result, N. vectensis is widely used to study developmental biology, neurobiology and physiology (Finnerty and Martindale, 1997; Anctil, 2000; Finnerty, 2001). A bacteria artificial chromosome (BAC) library has been constructed for N. vectensis (supported through the NSF BAC Library Initiative and currently available from the BACPAC Resource, Oakland, California, http://bacpac.chori.org/libraries.php), and the N. vectensis genome is currently being sequenced by the Joint Genome Institute (http://www.jgi.doe.gov/sequencing/seqplans.html).
In addition to their relevance as model organisms for understanding metazoan evolution, anthozoans are ecologically important. Scleractinian coral biology is of particular interest due to the importance of corals in maintaining tropical reefs and increasing human concerns about reef degradation (Richmond, 1993; Peters et al., 1997; Hughes et al., 2003). Few studies of chemical communication in cnidarians have focused directly on scleractinian corals, which probably reflects logistics of laboratory investigations. Diverse physiological processes in corals are almost certainly mediated by chemical signals, which are poorly understood. Examples include regulation of calcification, symbiosis and mass-spawning events. Structurally diverse compounds including diterpenes, prostaglandins and steroids have been described in octocorals (Weinheimer and Spraggins, 1969; Aceret et al., 1995; Slattery et al., 1995; Garrido et al., 2000; Valmsen et al., 2001). Some of these compounds are toxic and serve to deter potential predators, but the same or related compounds may act as hormones, including one example of a diterpene which acts as a sperm-attractant for the alcyonacean octocoral Lobophytum crassum (Coll et al., 1995).
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Hormonal control of mammalian reproduction is classically defined through the "hypothalamic-pituitary-gonadal axis," through which gonadotropin-releasing hormone (GnRH) is released by the hypothalamus to stimulate release of gonadotropins such as luteinizing hormone (LH) and follicle-stimulating hormone (FSH) from the pituitary (reviewed in Pierantoni et al., 2002
). These gonadotropins in turn stimulate synthesis of steroid hormones in target tissues. The sex steroids, which include progestins (e.g., progesterone) androgens (e.g., testosterone) and estrogens (e.g., estradiol), are essential to regulation of reproduction and development in vertebrates. Steroids classically act by binding to specific intracellular receptor proteins in the nuclear receptor superfamily that bind to response elements on DNA and regulate transcription of target genes (Evans, 1988). While comparable endocrine organs are not present in cnidarians and a similar cascade of signals has not been identified, several components of this pathway have been described in cnidarians.
Gonadotropin-releasing hormones and gonadotropins
Gonadotropin-releasing hormones (GnRHs) form a family of peptide hormones that are well-conserved among vertebrates and protochordates (Powell et al., 1996; Terakado, 2001; Dubois et al., 2002). Among vertebrates, GnRHs stimulate the release of gonadotropins; GnRHs also act throughout the body as neurotransmitters and circulating hormones (King and Millar, 1995). Compounds immunoreactive to antisera raised against vertebrate GnRHs have been detected in molluscs (Goldberg et al., 1993), and synthetic GnRHs can stimulate spawning and gametogenesis in molluscs (Pazos and Mathieu, 1999; Gorbman et al., 2003). GnRH immunoreactivity has also been identified in two anthozoan species: the sea pansy, Renilla koellikeri, and the sea anemone, Nematostella vectensis. GnRH-like compounds do not appear to act as spawning triggers in cnidarians. Both cnidarian GnRH-like compounds and vertebrate GnRHs inhibit rhythmic peristaltic contractions in Renilla koellikeri, and this effect can be blocked by the addition of a synthetic GnRH analog (Anctil, 2000).
The physiological role of GnRH-like compounds in cnidarians has not been described, and it is unknown whether cnidarian GnRH-like compounds stimulate the production or release of other peptides, which may be homologs or analogs to vertebrate gonadotropins. A receptor has also been identified in a sea anemone with a high degree of similarity to the vertebrate glycoprotein hormone receptor family, which includes gonadotropins and somatotropins (Nothacker and Grimmelikhuijzen, 1993). It is still a matter of speculation whether cnidarian gonadotropins exist and how their activity might be related to activity of GnRHs and/or steroid hormones.
Steroids
Diverse sterols have been identified in cnidarians (Ciereszko and Karns, 1973; Higgs and Faulkner, 1977; Popov et al., 1983); sterols are also produced by symbiotic dinoflagellates contained within the cells of many cnidarians (Ciereszko et al., 1968; Kokke et al., 1981). The functions of most cnidarian sterols have not been elucidated, although some of the compounds are cytotoxic in mammalian cell lines and may serve a defensive role (Garrido et al., 2000; Rueda et al., 2001).
Vertebrate-type sex steroids have been detected by immunoassay in several anthozoans, but the distribution of vertebrate-type sex steroids has not been documented in other cnidarian classes. In the hermaphroditic scleractinian coral, Montipora capitata, estradiol and estrone concentrations varied throughout the year with maximum values in February/March (estradiol) and April (estrone) prior to spawning in June and July (Tarrant et al., 1999). Female colonies of the coral Euphyllia ancora showed maximum values of estradiol, estradiol glucuronide and testosterone glucuronide during months of spawning (Twan et al., 2003). The pennatulacean octocoral Renilla koellikeri also showed elevated estradiol prior to spawning. In R. koellikeri, the peak estradiol concentration was greater in tissues from females than males. Estradiol, testosterone, and progesterone have also been detected in tissues from three species of alcyonacean soft corals (Slattery et al., 1997, 1999). Sinularia polydactyla showed sex-specific annual patterns in steroid concentration and a sharp decrease in testosterone concentration following spawning by both males and females (Slattery et al., 1999). Females also showed a drop in progesterone following spawning. Together these studies indicate the sex steroids are likely to play a role in regulating anthozoan gametogenesis and/or spawning.
Additional evidence for a role for estrogen in anthozoan reproduction comes from measurements of estrogen release into seawater prior to or during spawning events. Estradiol is released in association with spawning by scleractinians (Atkinson and Atkinson, 1992; Twan et al., 2003) and alcyonaceans (Slattery et al., 1999), with peak concentrations >10 ng L–1 reported in water adjacent to female Sinularia polydactyla colonies in Guam (pre-spawn concentrations were <200 pg L–1). In Taiwan, increases in estradiol, testosterone glucuronide, and especially estradiol glucuronide were detected in seawater surrounding spawning Euphyllia ancora colonies. Together these observations prompted speculation that free or conjugated estrogens might serve as chemical cues or pheromones to stimulate coral spawning. Polar steroid conjugates, such as estradiol glucuronide, are much more soluble in water than unconjugated steroids; thus, polar steroid conjugates are good candidates for water-borne pheromones. Polar steroid conjugates act as water-borne pheromones in a variety of vertebrates (Van den Hurk and Lambert, 1983; Sorensen et al., 1995).
The source of sex steroids in cnidarian tissues has not been demonstrated. In one study, coral homogenates metabolized estradiol into estrone and testosterone into androstenedione and androstanedione. Thus, corals contain a functional 17ß-hydroxysteroid dehydrogenase and 5
-reductase (Tarrant et al., 2003). The scleractinian coral Favia fragum converted radiolabeled progesterone into a variety of metabolites including a compound that co-migrated with testosterone during two-dimensional thin-layer chromatography (Gassman, 1992). Alcyonacean octocorals converted radiolabeled progesterone and androstenedione into several metabolites, but synthesis of androgens from progesterone was not observed (Slattery et al., 1997). Low levels of estrogen synthesis from androgen substrates by coral homogenates has been reported in one study (Twan et al., 2003), but other studies have not detected estrogen synthesis (Slattery et al., 1997; Tarrant et al., 2003). While it is still unclear whether corals can synthesize estrogens, there is evidence that steroidal estrogens are present in some coastal environments (Atkinson et al., 2003) and that corals can take up dissolved estrogens (Tarrant et al., 2001).
Investigation into the effects of endogenous or exogenous steroids on cnidarians is logistically complicated. Among vertebrates, precise doses of steroids may be injected into the bloodstream, and steroidogenic organs may be surgically removed. These approaches are not possible with cnidarians, and few studies have directly tested the effects of exogenous steroids on cnidarian physiology. Montipora capitata coral colonies treated with estradiol (nominally 2.3 µg L–1) for three weeks prior to spawning released fewer (29%) egg-sperm bundles than control colonies (Tarrant et al., 2004). Porites compressa coral fragments exposed continuously to 2 ng L–1 estrone for 2–8 weeks had lower (13–24%) skeletal growth rates than controls (Tarrant et al., 2004). Treatment with estrone or testosterone resulted in thicker tissue among the larger fragments. On the other hand, when Hydra vulgaris was exposed to ethinyl estradiol and bisphenol A, both of which are estrogenic in vertebrates, adverse physiological effects were only seen at high doses (<40 µg L–1) (Pascoe et al., 2002). In each of these studies, considerable natural variability was observed in the physiological endpoints measured, which resulted in limited statistical power.
If sex steroids do play a role in coral reproduction, then environmental sources of steroids may accumulate in tissues and either enhance or disrupt reproductive processes. Understanding steroid action in corals will also allow assessment of the potential for disruption of coral growth and reproduction by environmental contaminants. Steroidal estrogens and non-steroidal compounds with estrogenic activity have been identified globally in aquatic systems (Shore et al., 1993; Desbrow et al., 1998). Examples of endocrine disruption in vertebrates are numerous (McLachlan, 2001). Invertebrate examples include reproductive anomalies in the cladoceran Daphnia caused by nonylphenol (Shurin and Dodson, 1997; Gibble and Baer, 2003; Severin et al., 2003; Zhang et al., 2003) and imposex in gastropods associated with tributyl tin (Oberdorster and McClellan-Green, 2002; Santos et al., 2002).
Nuclear receptors and steroid action
In vertebrates, steroids diffuse freely through membranes of target cells, where they bind to specific receptor proteins in the nuclear receptor family. Nuclear receptors are transcription factors that occur throughout the animal kingdom, mediate the action of diverse hormonal ligands, and are essential to development, differentiation and homeostasis (Mangelsdorf et al., 1995; Laudet, 1997; Chawla et al., 2001). Nuclear receptors contain five domains, two of which are highly conserved: the ligand-binding domain (LBD) and the DNA-binding domain (DBD). Steroid hormone receptors, such as the estrogen receptor (ER), are activated by binding of a ligand (e.g., estradiol) to the LBD (Green et al., 1986; Beato et al., 1995). Two activated ER molecules form a homodimer and bind to response elements on the DNA through two zinc-finger regions of the DBD (Kumar and Chambon, 1988). Binding of receptors to DNA stimulates or represses transcription of target genes. Hundreds of nuclear receptors have been identified, primarily through use of the highly conserved DBD as a molecular probe. Among vertebrates, receptors have been described for steroid hormones, thyroid hormones, retinoic acid, and various dietary lipids; however, ligands have not yet been identified for most nuclear receptors (Laudet et al., 1992; Mangelsdorf and Evans, 1995; Chawla et al., 2001). Ligands may yet be found for some of these so-called "orphan receptors," but others are likely to be activated through different means or possess constitutive activity (Power et al., 1991; Marcus et al., 1996; Escriva et al., 1997).
Based on complete genome sequences, 21 nuclear receptor genes have been identified in the fruitfly Drosophila melanogaster and over two hundred in the nematode Caenorhabditis elegans (Chervitz et al., 1998; Sluder et al., 1999; Bertrand et al., 2004). Some of these invertebrate receptors have known mammalian homologs, particularly to various orphan receptors, but many, especially in C. elegans, are novel (Enmark and Gustafsson, 2001). Receptors to vertebrate sex steroids, such as the ER, have not been identified in C. elegans or D. melanogaster (Enmark and Gustafsson, 2001). An ER homolog has recently been reported in the mollusc, Aplysia californica (Thornton et al., 2003). Phylogenetic analyses indicate that ERs have been lost from the lineage containing insects and nematodes (Thornton et al., 2003; Bertrand et al., 2004) therefore, ER homologs may be present in other invertebrates. To date, an estrogen receptor has not been identifed in any cnidarian. Because a complete genomic sequence has not been determined for any cnidarian, it is possible that cnidarian steroid receptors will be identified in the future.
Several nuclear receptor genes, some of which have clear vertebrate homologues, have been identified in cnidarians. Homologs to COUP-TF (chicken ovalbumin upstream promoter transcription factor, an orphan receptor) are present in hydra (Escriva et al., 1997) and scleractinian corals (Grasso et al., 2001). RXR (retinoic acid "X" receptor, which binds 9-cis retinoic acid) has been identified in jellyfish (jRXR) and sea anemone (Kostrouch et al., 1998). Some nuclear receptors identified in sea anemones and scleractinian corals are sufficiently divergent from vertebrate sequences that they cannot easily be assigned to a nuclear receptor subfamily or a clear vertebrate homolog (Grasso et al., 2001).
Only one published study has attempted to characterize function of a cnidarian nuclear receptor. Kostrouch et al. (1998) demonstrated that the jRXR can bind 9-cis-retinoic acid and is expressed throughout development. They also identified binding sites for jRXR in promoter regions of crystallin genes, which are highly expressed in the jellyfish eye lens. The authors hypothesized that retinoid signaling through jRXR may regulate eye development in jellyfish and other invertebrates. In vertebrates, RXR is also required by many other nuclear receptors for dimerization and binding to DNA response elements (Glass, 1994; Mangelsdorf and Evans, 1995). If heterodimers do form in cnidarians, availability of RXR homologs may regulate activity of other nuclear receptors.
To characterize nuclear receptor action in cnidarians it will be necessary to describe patterns in gene expression during development, throughout the reproductive cycle, and in response to environmental signals. In vitro and cellular expression systems could be used to describe binding of putative ligands to coral nuclear receptors, binding of nuclear receptors to DNA response elements, transactivational activity, and dimerization patterns among receptors. Challenges still remain in developing cnidarian cell lines for functional assays, validating the use of cell lines from other organisms, or selecting appropriate noncellular assays. Characterizing expression and function of cnidarian nuclear receptors will improve current understanding of physiology. These studies will improve our understanding of how cnidarians respond to environmental cues and will provide a basis to investigate disruption of physiological processes by physical and chemical stressors.
Alternate mechanisms of steroid action
While classical estrogen receptors are not present in C. elegans and might not be present in cnidarians, nematodes and corals can both be affected by experimental exposure to estrogen. In C. elegans vitellogenin production increases in response to dosing with exogenous estrogen (Custodia et al., 2001). In corals, exogenous estrogens can decrease the number of eggs spawned, decrease skeletal growth rate and increase tissue thickness (Tarrant et al., 2004). Similarly, while some compounds that are estrogenic in mammals can inhibit reproduction and development in crustaceans, an estrogen receptor has not been identified in crustaceans (see Hutchinson et al., 1999 and references therein). Because a classical estrogen receptor has not been identified in any cnidarian or most other invertebrates, estrogens may act through a "functional estrogen receptor," that does not belong to the steroid receptor protein family described in vertebrates.
In vertebrates steroids can also act through various types of membrane-bound receptors to induce rapid, non-genomic effects. For example, steroids can bind to membrane-bound receptors for peptide hormones; specifically, progesterone can bind to a second site on the oxytocin receptor to maintain uterine quiescence during mammalian pregnancy (Grazzini et al., 1998). Other membrane-bound receptors appear to target steroid hormones more specifically. Some membrane-bound steroid receptors originate from the same transcripts as the corresponding nuclear receptors (Razandi et al., 1999). In contrast to these translocated "nuclear" receptors, a novel class of membrane-bound progestin receptors has recently been identified in fish and mammals; these receptors help to regulate oocyte maturation (Zhu et al., 2003a, b). Membrane-bound receptors for steroids can be coupled to different types of G-proteins (e.g., stimulatory or inhibitory) in different tissues. Alternatively, estrogen may work through non-receptor-mediated pathways in corals and other invertebrates.
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Melatonin and serotonin are indoleamines derived from tryptophan which are produced by the pineal gland in vertebrates. Melatonin synthesis rates are orders of magnitude higher during periods of darkness, and melatonin is rapidly degraded in light. As a result of these characteristics, melatonin has been used by vertebrates to regulate biological rhythmicity and acts as a "chemical messenger of darkness" (Reiter, 1991
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Exogenous melatonin can stimulate expansion of the oral disk and protrusion of the actinopharynx in sea anemones, and a derivative, 5-methoxytryptoamine (5-MT) can stimulate rhythmic muscular contraction of the body column (Tsang et al., 1997). In the sea pansy, Renilla koellikeri, serotonin can stimulate rhythmic muscular contraction (Anctil, 1989) and spawning (Tremblay et al., 2004), and melatonin can inhibit these contractions (Anctil et al., 1991). While daily peaks in melatonin were not identified in R. koellikeri, annual maxima coincided with the first stages of sexual maturation (Mechawar and Anctil, 1997).
Serotonin can also experimentally induce metomorphosis of hydrozoan larvae, and inhibition of serotonin synthesis can inhibit metamorphosis (McCauley, 1997; Walther and Fleck, 1998). McCauley (1997) proposed that external cues from specific bacteria induce the hydrozoan to release serotonin from intracellular stores to act on cell surface receptors leading to membrane depolarization, calcium influx, activation of protein kinase C and finally metamorphosis. This model provides an example of how an external environmental cue may be transduced through a series of biochemical messengers to create a biological response.
Melatonin is also synthesized by the dinoflagellate, Gonyaulax polyedra, where melatonin and 5-MT stimulate bioluminescence and, at high concentrations, encystment (Balzer and Hardeland, 1991; Burkhardt and Hardeland, 1996; Hardeland and Poeggeler, 2003). Because indoleamines appear to regulate behavior in both dinoflagellates and cnidarians, one might speculate that indoleamines may somehow affect the symbiosis between corals and zooxanthellae.
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IODINATED ORGANIC COMPOUNDS |
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The vertebrate thyroid gland produces two iodinated amino acids, thyroxine and triiodothyronine, which regulate diverse aspects of development, metabolic stimulation and metamorphosis (Johnson, 1997
). Iodinated organic compounds including thryoxine, monoiodotyrosine, and diiodotyrosine, have been reported in cnidarians since 1896 (reviewed by Spangenberg, [1984]); notably triiodothyronine has not been reported in cnidarians). Iodinated compounds have been shown to induce strobilation and metamorphosis in the jellyfish Aurelia sp. (Spangenberg, 1967; Spangenberg, 1971; Silverstone et al., 1977), and thyroxine concentration has been shown to increase sharply following changes in water temperature, the normal physical cue for strobilation (Gorbman, 1974).
Iodinated organic compounds are also important in mineralization and demineralization in vertebrates and help to form proteinaceous skeletons of gorgonians and other invertebrates (Szmant-Froelich, 1974). In Aurelia sp., exogenous thyroxine inhibits formation of statoliths and accelerates their resorption in starved individuals; these effects were greater than effects observed with an equimolar concentration of iodide (Spangenberg, 1984). Finally, iodinated organic compounds can be concentrated around testes of hydra (Gorbman, 1974), in plates of gorgonian skeleton (Szmant-Froelich, 1974), and within the scleroblasts (spicule-forming cells), polyp epithelium, and spicules of gorgoninans (Kingsley et al., 2001). No studies have reported on the effects or distribution of iodinated organic compounds in scleractinian corals. It would be particularly interesting to determine whether thyroxine can affect the metamorphosis from larval to adult forms or whether iodinated compounds play a role in coral skeletal formation.
Collectively, these studies indicate that iodinated organic compounds, such as thyroxine, can affect strobilation and mineralization in cnidarians. In vertebrates, thyroxine acts through binding to a specific thyroid hormone receptor, which can then bind to response elements on DNA and activate genes, a similar mechanism to that for steroid hormone action. Although there have been several attempts to identify a thyroid hormone receptor homolog in cnidarians using degenerate primers (Escriva et al., 1997; Kostrouch et al., 1998; Grasso et al., 2001) no putative thyroid receptor has been found, and the mechanism of action for iodinated organics in cnidarians is unknown. In an assessment of the evolution of iodinated hormones, Johnson (1997) reviewed biological activity of thyroxine in cnidarians, echinoderms and chordates and stated that because of the early divergence of cnidarians from other metazoa, it is likely that thryoxine activity in cnidarians arose separately from that in more complex animals. Without a documented lack of thyroxine activity in other invertebrates, this claim is not well-supported, and awaits further study.
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What can cnidarians tell us about endocrinology?
In recent years, much progress has been made in understanding of the evolution of metazoan developmental mechanisms. Highly conserved genes in the Hox, Wnt, and Pax gene families are instrumental in regulating embryonic development in cnidarians and higher animals (Hobmayer et al., 2000
; Miller et al., 2000; Finnerty et al., 2003). Similar progress will be made in the coming years toward understanding the evolution of endocrine-like bioregulation. Because cnidarians are basal metazoans, they can help to determine original or fundamental role of genes and signaling molecules and provide a context to study the evolution and diversification of regulatory genes in higher animals. Also by comparing bioregulatory processes across cnidarian classes, it will be possible to describe diversification of hormone action among animals with a relatively low level of cellular organization. Characterization of signaling processes in cnidarians may lead to new understanding of functions of signaling molecules in other organisms. Because cnidarians lack endocrine organs and a circulatory system, perhaps the greatest value in studying bioregulation is not what they can tell us directly about endocrinology, but what they can tell us about bioregulation in the absence of an endocrine system, about intracine, paracrine and exocrine regulation.
What can endocrinology tell us about cnidarians?
Research on cnidarians and most organisms can benefit from the tremendous effort that has been spent in understanding physiology of model organisms predominantly used for medical research. A comparative approach that utilizes existing data is perhaps the most efficient way to fill the gaps in our knowledge about other organisms. Similarly, comparison to annotated genomes of vertebrates, insects and nematodes will facilitate interpretation of results from currently available and proposed cnidarian DNA sequencing projects (Ryan and Finnerty, 2003). On the other hand, care must be taken not to assume processes will be identical in all organisms. For example, compounds that disrupt mammalian reproduction through interactions with the steroid receptors may affect physiology of invertebrates through an entirely different mechanism (Hutchinson, 2002). Characterization of endocrine-like signaling and other bioregulatory processes in cnidarians will provide a basis for future ecophysiological studies.
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ACKNOWLEDGMENTS |
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This manuscript was greatly improved by comments from two anonymous reviewers and from M. Atkinson, S. Atkinson, R. Kinzie and T. Verslycke. The author is also grateful for encouragement in development of this manuscript from J. McLachlan. Research by the author has been supported by an EPA STAR fellowship, the Seward Johnson Foundation and the Caribbean Marine Research Center. This publication was prepared by A. M. Tarrant pursuant (in part) to subcontract CMRC-03-NRAA-01-04A from the Perry Institute for Marine Science, Caribbean Marine Research Center, through support provided by the National Oceanic and Atmospheric Administration, US Department of Commerce Award No. NA06RU0228 and No. NA16RU1496. The statements, findings, conclusions, and recommendations are those of the author and do not necessarily reflect the views of U.S. Department of Commerce, National Oceanic and Atmospheric Administration or the Perry Institute for Marine Science/ Caribbean Marine Research Center. This is contribution number 11254 from the Woods Hole Oceanographic Institution.
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FOOTNOTES |
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1 From the Symposium EcoPhysiology and Conservation: The Contribution of Endocrinology and Immunology presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 5–9 January 2004, at New Orleans, Louisiana.
2 E-mail: atarrant{at}whoi.edu
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