Integrative and Comparative Biology

Integrative and Comparative Biology 2005 45(1):88-96; doi:10.1093/icb/45.1.88

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The Society for Integrative and Comparative Biology

Annelid Endocrine Disruptors and a Survey of Invertebrate FMRFamide-Related Peptides¹

Kevin G. Krajniak^2,1
1 Department of Biological Sciences, Southern Illinois University Edwardsville, Edwardsville, Illinois 62026-1651

	SYNOPSIS

TOP SYNOPSIS INTRODUCTION ANNELID ENDOCRINE DISRUPTORS FMRFAMIDE-RELATED PEPTIDES PEPTIDE SEQUENCES AND BIOLOGICAL... FARP GENES FARP RECEPTORS FARP CONCLUSIONS References

 
There is a growing body of literature describing the actions of endocrine disruptors on annelids. These pollutants cause decreases in growth and reproductive output, delay sexual maturation, and inhibit the immune system in annelids. More studies are needed to determine the mechanisms that underlie these responses. Most invertebrate endocrine disruptor research focuses on steroids. In recent years many new invertebrate peptide hormones including those related to the molluscan peptide FMRFamide have been identified. Since the storage of these peptides can be inhibited by steroids during insect metamorphosis, they may be affected by endocrine disruptors. Therefore, it is worthwhile to give a brief overview of this peptide family to those studying endocrine disruption in invertebrates with the hope that they may begin to consider these peptides in their future research. In 1977 Price and Greenberg isolated FMRFamide from the cerebral ganglia of the clam, Macrocallista nimbosa. Since then researchers have used bioassays and immunoassays to identify a large number of FMRFamide-related peptides (FaRPs) from many invertebrate phyla. Even more peptides are predicted by the FaRP genes that have been sequenced. FaRPs have a variety of functions and act as neurotransmitters, neuromodulators, or neurohormones. Each function is species and tissue specific. Most FaRP receptors are linked to a second messenger system. However, at least one is a ligand gated sodium channel. On going studies are examining FaRPs from the molecular to organismal level.

	INTRODUCTION

TOP SYNOPSIS INTRODUCTION ANNELID ENDOCRINE DISRUPTORS FMRFAMIDE-RELATED PEPTIDES PEPTIDE SEQUENCES AND BIOLOGICAL... FARP GENES FARP RECEPTORS FARP CONCLUSIONS References

 
This presentation will discuss two topics. The first part will review the effects of endocrine disruptors on annelids. The second part will consider the ever increasing family of invertebrate neuropeptides related to FMRFamide. Although there is currently no evidence that suggests these neuropeptides are targets of endocrine disruption in annelids or any other invertebrate, in insects the levels of these peptides can be regulated by steroid hormones during metamorphosis. Therefore, endocrine disruptors may have an effect on these peptides and this review can serve to bring them to the attention of researchers in the field of invertebrate endocrine disruption.

	ANNELID ENDOCRINE DISRUPTORS

TOP SYNOPSIS INTRODUCTION ANNELID ENDOCRINE DISRUPTORS FMRFAMIDE-RELATED PEPTIDES PEPTIDE SEQUENCES AND BIOLOGICAL... FARP GENES FARP RECEPTORS FARP CONCLUSIONS References

 
There are many chemicals which have been implicated in endocrine disruption in invertebrates. These include heavy metals, polychlorinated biphenyls (PCBs), alkylphenols, insectisides, synthetic and natural vertebrate steroids, and industrial effluents that contain chemical mixtures (Depledge and Billinghurst, 1999). Most studies have examined the uptake, accumulation, and toxicity of these materials in annelids; however, there are some studies that have examined the physiological impacts of these substances on the animals.

Heavy metals can affect the density, viability, cocoon production, growth and sexual development of terrestrial annelids (Spurgeon et al., 1994). Juvenile worms are more sensitive to these pollutants. When juvenile specimens of the earthworm Eisenia fetida are exposed to zinc they have a decreased growth rate, delayed sexual maturation, and a reduction in cocoon production (Spurgeon and Hopkin, 1996). Adult worms exposed to the same doses displayed none of these abnormalities. The researchers suggest that these responses may be due to the excess energy the animals must expend to void these metals, however they may also elicit other changes in physiology. Metals may also affect invertebrate immune systems. Copper has been shown to suppress immune system function in E. fetida by decreasing phagocytosis in the coelomocytes (Burch et al., 1999).

Tributyltin (TBT) is the active ingredient in marine antifouling paints. Hagger et al. (2002) exposed embryos and larvae of the polychaete Platynereis dumerilii to various TBT concentrations. The results showed that TBT had dose-dependent genotoxic, cytotoxic, and developmental effects on these worms. When juveniles of the polychaete Armandia brevis, a deposit feeder, were exposed to sediment-associated TBT growth was inhibited by twenty-five percent (Meador and Rice, 2001).

Herbicides and pesticides also can affect reproduction. When the earthworm Eisenia andrei was exposed to either the herbicide terbuthylazine or the pesticide carbofuran there was a concentration-dependent decrease in cocoon production and biomass (Viswantahan, 1997). Interestingly, the offspring of the terbuthylazine exposed worms exhibited enhancement of growth, development, and cocoon production when exposed to terbuthylazine. The offspring from parents exposed to carbofuran also had enhanced growth when treated with carbofuran; however cocoon production was below control values. When the larvae of the estuarine polychaete, Streblospio benedicti were treated with the pesticide disulfan there was a significant decrease in settlement and juvenile growth (Chandler and Scott, 1991).

Nonylphenol is an alkylphenol that mimics estrogen and disrupts sexual development in some invertebrates (Depledge and Billinghurst, 1999). Bettinetti and Provini (2002) exposed the benthic annelid Tubifex tubifex to 4-nonylphenol in the sediment. The production of cocoons and young worms decreased with increasing concentrations of nonylphenol. A histological examination of the clitellum revealed that damage occurred to both male and female gonads.

PCBs can affect annelid growth, reproduction, and immune system functions. When T. tubifex was exposed to soil contaminated with mixtures PCBs and other organic pollutants there was a decrease in reproduction and development (Bettinetti et al., 2003). In addition, the PCB aroclor suppressed phagocytosis in the coelomocytes of the earthworms Lumbricus terrestris and E. fetida (Burch et al., 1999).

These findings suggest that endocrine disruptors can affect the ability of annelids to develop, grow, sexually mature, reproduce, and fight off infections. The underlying mechanisms remain to be seen. Future studies need to examine the cellular and molecular mechanisms that are affected by these and other endocrine disruptors.

So far most of the invertebrate endocrine disruptor research has examined the effects of these toxins on steroid hormones. Over the last three decades a growing number of peptide hormones have been discovered in the invertebrate phyla. One family of peptides related to the molluscan peptide FMRFamide has been found in almost all invertebrates examined including annelids. In insects steroid hormones can regulate the levels of these peptides in cells during metamorphosis suggesting an interaction between these two types of messengers (Witten and Truman, 1996). Future research is needed to determine if there are any interactions between the peptides and endocrine disruptors. Therefore, the rest of this presentation will be a brief overview of this peptide family.

	FMRFAMIDE-RELATED PEPTIDES

TOP SYNOPSIS INTRODUCTION ANNELID ENDOCRINE DISRUPTORS FMRFAMIDE-RELATED PEPTIDES PEPTIDE SEQUENCES AND BIOLOGICAL... FARP GENES FARP RECEPTORS FARP CONCLUSIONS References

 
In 1977 Price and Greenberg reported the identification of FMRFamide, a cardioexctiatory neuropeptide isolated from cerebral ganglion of the Sunray Venus clam Macrocallista nimbosa. The name was derived from the single letter abbreviations of the four amino acids, phenylalanine, methionine, arginine, phenylalanine and the fact that it had a C-terminal amide. Shortly afterward similarly structured peptides were isolated from other molluscs and then from animals from other phyla. These were grouped into a family called the FMRFamide-related peptides or FaRPs (Price and Greenberg, 1989). Over the years the number of peptides identified by bioassay, immunoassay, or predicted by gene sequences has grown to over 200. In some of these peptides the only similarity to FMRFamide is the presence of an RFamide. This has led to several revisions of what exactly constitutes a FaRP. This discussion will be limited to those peptides which most closely resemble FMRFamide and contain the sequences of X₁X₂ RFamide where X₁ is F or Y and X₂ is M or L or I or T. A listing of all the RFamide peptides that have been isolated so far can be found in Espinoza et al. (2001).

	PEPTIDE SEQUENCES AND BIOLOGICAL ACTIVITY

TOP SYNOPSIS INTRODUCTION ANNELID ENDOCRINE DISRUPTORS FMRFAMIDE-RELATED PEPTIDES PEPTIDE SEQUENCES AND BIOLOGICAL... FARP GENES FARP RECEPTORS FARP CONCLUSIONS References

 
Molluscs
Seventeen FaRPs including FMRFamide have been isolated from molluscs (Table 1). FMRFamide and FLRFamide are found in every class that has been studied (Price et al., 1987). Cephalopods also have FIRFamide, AFLRFamide, TFLRFamide, YGGFMRFamide, and ALSGDAFLRFamide. However, gastropods have the largest number of FaRPs. So far ten N–terminally extended FLRFamide, YLRFamide, or FMRFamide sequences have been identified and another five including a YIRFamide have been predicted by gene sequences (see Espinoza et al., 2001).

View this table: [in this window] [in a new window]   TABLE 1. Molluscan and annelid FaRPs.

 
In molluscs FaRPs have many functions. In the nervous system they modulate synaptic transmission (Cottrell et al., 1992). FMRFamide which was isolated because it stimulates the heart of Mercenaria mercenaria not only excites molluscan hearts (Painter and Greenberg, 1982; Lesser and Greenberg, 1993), but also inhibits some bivalve hearts (Painter and Greenberg, 1982). FaRPs modulate molluscan visceral and somatic muscles (Lehman and Greenberg, 1987; Krajniak et al., 1989). In gastropods they control salivary glands (Bulloch et al., 1988) and inhibit both the feeding motor program (Cooke et al., 1985) and movement of the alimentary canal (Krajniak et al., 1989). They play a role in reproduction since FaRPs stimulate the gastropod penis and retractor muscles and regulate cephalopod egg laying (Lehman and Greenberg, 1987; Krajniak et al., 1989; Henry et al., 1999). FaRPs stimulate amylase secretion in the scallop Pectin maximus (Favrel et al., 1994; Nachman et al., 1999) and they are involved in osmoregulation (Madrid et al., 1994).

Annelids
Seven FaRPs have been isolated from annelids (Table 1). Two peptides, FMRFamide and FTRFamide, have been found in polychaetes, while all the FaRPs listed in Table 2, except FTRFamide, have been found in leeches. To date no FaRPs have been isolated from oligochaetes. In polychaetes FMRFamide controls heartbeat, body wall tone, and esophageal tone (Diaz-Miranda et al., 1992; Krajniak and Greenberg, 1992). In the leech, Hirudo medicinalis, FaRPs are cardioactive; they modulate neuronal circuitry (Kuhlman et al., 1985), and elicit contractions in the longitudinal muscle (Norris and Calabrese, 1990) and the pharynx (O'Gara et al., 1999). Furthermore, GDPFLRFamide acts as a diuretic hormone, while FMRFamide acts as an antidiuretic hormone in leeches (Salzet et al., 1994). In the oligochaete, E. foetida, FMRFamide inhibits the contractions of the crop-gizzard (Ukena et al., 1996), whereas in L. terrestris it causes a biphasic change in rate and a decrease in the contraction amplitude (Krajniak and Klohr, 1999).

View this table: [in this window] [in a new window]   TABLE 2. Crustacean FaRPs.

 
Crustaceans
Sixteen different FaRPs have been isolated from crustaceans (Table 2), all of which are N–terminally extended FLRFamides. Several FaRPs have been isolated from sites of neurohormone release, including pericardial organs and eyestalks. Their effects have been examined on the circulatory system, the digestive system, and exoskeletal muscles. FaRPs excite the isolated crustacean heart (Krajniak, 1991; Mercier et al., 1993); however in vivo they are cardioinhibitory (McGaw et al., 1995; McGaw and McMahon, 1995) and can change arterial hemolymph flow (McGaw and McMahon, 1995). The reason for the in vitro and in vivo differences is unclear. These peptides can stimulate movements in the somatograstic system (Tierney et al., 1997) and the hindgut (Mercier and Lee, 2002). They also enhance neuromuscular activity (Mercier et al., 1990).

Insects
So far 26 insect FaRPs have been isolated (Table 3). They include N–terminally extended FMRFamides, FIRFamides, and FLRFamides and more are predicted from insect genes (see Espinoza et al., 2001; Orchard et al., 2001). Those FLRFamides with the sequence XDVXHXFLRFamide are further grouped into the mysosuppressin subfamily. The FMRFamide containing peptides inhibit the heart, stimulate somatic muscle contractions, decrease contractions of the crop, and stimulate salivary gland output (Nichols et al., 1999a; Duttlinger et al., 2002; Hewes et al., 1988; Duve et al., 1992a). FLRFamide containing peptides inhibit movements of the crop, heart, midgut and oviducts, suppress the release of adipokinetic hormones, and reduce induced diuretic activity, while they increase the force of neurally evoked contractions in flight muscles, excite the ileum, and stimulate enzyme secretion in the midgut (Nachman et al., 1993; Holman, et al., 1986; Vullings et al., 1998; Kingan et al., 1996; Lange et al., 1994; Fuse et al., 1999). AFIRFamide and GQERNFLRFamide stimulate the contractions of the oviduct (Lange et al., 1994). Two peptides, VRDYPQLLDSGMKRQDVVHSFLRFamide (F24) and YAEAAGEQVPEYQALVRDYPQLLDSGMKRQDVVHSFLRFamide (F39), which contain the sequence of a smaller myosuppressin (pQDVVHSFLRFamide) have been found in the midguts of parasitized Manduca sexta larvae (Kingan et al., 1997). These peptides may be intermediates in the biosynthesis of the myosuppressin and may themselves be released locally from endocrine/paracrine cells in the midgut epithelium. In M. sexta, the steroid hormone, 20-hydroxyecdysone, appears to regulate the loss of FaRPs in motor neurons during metamorphosis (Witten and Truman, 1996).

View this table: [in this window] [in a new window]   TABLE 3. Insect FaRPs.

 
Nematodes
In nematodes sixteen FaRPs have been isolated and identified (Table 4) and more FLRFamides and FIRFamides are predicted from the genes of Caenorhabditis elegans (Li et al., 1999). Nematode FaRPs modulate somatic muscles (Maule et al., 1996), inhibit pharyngeal pumping (Brownlee and Walker, 1999), and reduce contractions of the female reproductive tract (Fellowes et al., 2000). In C. elegans, the FIRFamide peptides reduce locomotion and induce a linear body posture. KHEYLRFamide inhibits locomotion and causes occasional jerky movements, while SDIGISEPNFLRFamide prohibits movement (Davis and Stretton, 2001). Deletion of flp-1, the gene that codes for the FLRFamide peptides, causes several behavioral defects, including lack of coordination, hyperactivity, and a decreased response to high osmolarity; its overexpression results in reciprocal behaviors (Nelson et al., 1998).

View this table: [in this window] [in a new window]   TABLE 4. Nematode and Platyhelimenthes FaRPs.

 
Platyhelimenthes
Three FaRPs containing YIRFamide have been isolated from turbellarian flatworms (Table 4). These peptides and FMRFamide excite the muscle cells and fibers of tubellarians, digeneans, and monogeneans (Geary et al., 1996). In the turbellarian, Bdellura candida, native FaRPs are more potent and efficacious than FMRFamide (Johnston et al., 1996).

	FARP GENES

TOP SYNOPSIS INTRODUCTION ANNELID ENDOCRINE DISRUPTORS FMRFAMIDE-RELATED PEPTIDES PEPTIDE SEQUENCES AND BIOLOGICAL... FARP GENES FARP RECEPTORS FARP CONCLUSIONS References

 
FaRP genes from molluscs, insects, and nematodes have been sequenced (Price and Greenberg, 1994; Loi and Tublitz, 1997; Taghert et al., 1992; Li et al., 1999). The molluscan FMRFamide gene also codes for FLRFamide with the ratio of FMRFamide to FLRFamide being as high as 28:1 in Aplysia to as low as10:3 in Helix (Price and Greenberg, 1994). Other non-FaRP peptide sequences may also be present. In the snail Helix aspersa the N-terminally extended FaRP gene codes for two copies of the sequence QDPFLRIamide (Greenberg and Price, 1992). This sequence has a C-terminal isoleucine instead of the normal FaRP C-terminal phenylalanine. The corresponding peptide pQDPFLRIamide has been isolated and its biological activity is the exact opposite of the FaRPs on the snail heart. In the gastropod Lymnaea the FaRPs are encoded on two exons of the same gene. The first exon codes for the tetrapeptides and a second exon contains several copies of the different N-terminally extended FLRFamides and YLRFamides (Bright et al., 1993). Alternative splicing is used to express either the tetrapeptides or N-terminally extended peptides. In cephalopods the same gene codes for tetrapeptides and an N-terminally extended peptide (Loi and Tublitz, 1997).

Four FaRP genes have been identified in insects. In Drosophila multiple N–terminally extended FMRFamides are present in one gene (Taghert et al., 1992). Immunohistochemical data suggest that differential processing can occur in the N-terminally extended FMRFamide precursor protein to liberate the different FaRPs (Nichols et al., 1999b). This is also suggested by the biological activities of these peptides on different tissues (Duttlinger et al., 2002). A gene that codes for a single myosuppressin FLRFamide has been found in Drosophila (Nichols, 1992; Orchard et al., 2001), the cockroach Diploptera punctata (Donaly et al., 1996), and the true armyworm Pseudaletia unipuncta (Lee et al., 2002). There is no evidence for alternate splicing in expression of the gene in the cockroach gene. Interestingly, the myosuppressin sequence, pQDVVHSFLRFamide, in the army worm gene is part of a precursor that also codes for two larger peptides, F24 and F39, which have been found in the midguts of parasitized M. sexta larvae (Kingan et al., 1997).

In the nematode, C. elegans, many different FaRP genes have been identified (Li et al., 1999). The flp-1 gene codes for multiple copies of the different N-terminally extended FLRFamides, flp-2, flp-4, flp-8, flp-10, and flp-12 code for FIRFamide or YIRFamide containing peptides and flp-6 and flp-14 code for the YMRFamide or YLRFamide peptides. The flp-1 gene which codes for seven different FLRFamides has six exons, the last four encoding the FaRP sequences. Deletion flp-1, causes behavioral defects, including lack of coordination, hyperactivity, and a decreased response to high osmolarity, whereas its overexpression results in reciprocal activity (Nelson et al., 1998).

	FARP RECEPTORS

TOP SYNOPSIS INTRODUCTION ANNELID ENDOCRINE DISRUPTORS FMRFAMIDE-RELATED PEPTIDES PEPTIDE SEQUENCES AND BIOLOGICAL... FARP GENES FARP RECEPTORS FARP CONCLUSIONS References

 
The binding of ¹²⁵I-daYFnLRFamide, a radiolabelled analogue of FMRFamide, to its receptor in Helix neuron membranes is reversible, saturable, and specific, with a K_d of 14 nM and a B_max of 85 fmol/mg brain (Payza, 1987). A lower affinity receptor is also observed (K_d = 245 nM; B_max = 575 fmol/mg brain). Similarly, in locust oviduct membranes, the binding of ¹²⁵I-YDVDHFLRFamide, a radiolabelled analogue of PDVDHFLRFamide, to its receptor is reversible, saturable, and specific, with a K_d of 0.9 nM and a B_max of 14.5 fmol/mg protein (Wang et al., 1994). These membranes have a lower affinity receptor (K_d = 190 nM; B_max = 540 fmol/mg protein). A single high affinity FMRFamide receptor with K_d of 0.15 nM and a B_max of 237 fmol/mg protein is seen in optic lobe membranes of the squid Loligo pealei (Chin et al., 1994).

Most FaRP receptors are linked to G-proteins and stimulate the production of second messengers. FMRFamide increases intracellular levels of cyclic adenosine monophosphate (cAMP) (Higgins et al., 1978), 12-hydroperoxy-5,8,10,14-eicosatetraenoic acid (12-HPETE) (Piomelli et al., 1987), and inositol 1,4,5-trisphosphate (Falconer et al., 1993). Recently, two Gprotein coupled FaRP receptor were cloned; DrmFMRFamide-R from Drosphila (Cazzamali and Grimmelikhuijzen, 2002) and AngFMRFa-R from the mosquito Anopheles gambiae (Duttlinger et al., 2003). There is a high degree of sequence conservation between these two receptors. The Drosophila FaRP PDNFMRFamide has the highest affinity for DrmFMRFamide-R (Cazzamali and Grimmelikhuijzen, 2002; Meeusen et al., 2002). The native ligand of mosquito receptor is unknown, although, FMRFamide does excite the larval heart (Duttlinger et al., 2003).

A FMRFamide receptor cloned from the mollusc, Helix aspersa, is quite different from those linked to G-proteins. This receptor is the first peptide-gated sodium channel to be discovered (Lingueglia et al., 1995). Pharmacologically it is indistinguishable from the intact receptor in the Helix neuron C2 (Cottrell, 1997). It remains to be seen if FaRP receptors in animals from other phyla are also ligand gated ion channels.

Structure-activity relationship (SAR) studies using muscular tissues of molluscs (Payza, 1987), annelids (O'Gara et al., 1999), crustaceans (Krajniak, 1991), insects (Duve et al., 1992b), nematodes (Bowman et al., 2002), and platyhelimenths (Johnston et al., 1996) show that in each species and tissue the FaRP receptors have unique structural requirements for activation. Even when the native FaRP sequences are similar as in molluscs and annelids (Table 1) the receptors tolerate different amino acid substitutions in the peptide sequence (Payza, 1987; O'Gara et al., 1999).

SAR studies of the locust oviduct receptor show that are different binding and activation regions in native FaRP, PDVDHVFLRFamide (Wang et al., 1995c). HVFLRFamide is the minimum sequence for the normal inhibitory response, while VFLRFamide is weakly stimulatory. Sulfakinins, another group of insect peptides, which have a C-terminus sequence of Y(SO) GHMRFamide, cause an excitatory response in the oviduct (Nachman et al., 1993). It appears that these inhibitory and excitatory peptides use the same receptor, but are able to produce opposite responses because of differences in the activation sites. The receptor interacts with two different G-proteins; one transduces the inhibitory response, while the other couples the excitatory effect (Wang et al., 1995a, b).

	FARP CONCLUSIONS

TOP SYNOPSIS INTRODUCTION ANNELID ENDOCRINE DISRUPTORS FMRFAMIDE-RELATED PEPTIDES PEPTIDE SEQUENCES AND BIOLOGICAL... FARP GENES FARP RECEPTORS FARP CONCLUSIONS References

 
FaRPS are an ancient family of neuropeptides that go back to the beginning of bilaterally symmetric organisms. During evolution the structures of these peptides have varied mainly in the N–terminal with only small changes in the tetrapeptide core. Their functions also have been conserved. In most phyla FaRPs affect muscular tissues in the body, the digestive system, and the reproductive system. They also play a hormonal role in the annelids, arthropods, and molluscs.

Why are there so many different FaRPs in a single animal or on a single gene? Early on Greenberg and Price (1992) suggested that the action of a FaRP-containing neuron must be due to the overall sum of its secretory products or bouquet. If all the peptides present in a single propeptide are processed and released this would lead to a complex secretagogue. In D. melanogaster five different FMRFamides are present on a single gene. There appears to be cellspecific transcriptional regulation of the FMRFamide gene (Beneviste et al., 1998) and posttranslational processing of the proFMRFamide peptide (Nichols et al., 1999b; Merte and Nichols, 2002). Furthermore, the biological activities of the individual peptides do not appear to overlap on target tissues (Duttlinger et al., 2002). Thus it appears in some animals that even if many FaRPs are present in the whole animal; each one has a distinct pattern of expression and activity.

	FOOTNOTES

 
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: kkrajni{at}siue.edu

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