© 2001 by The Society for Integrative and Comparative Biology
Regulation of the Crustacean Mandibular Organ1
1 Department of Biological Sciences, Illinois State University, Normal, Illinois 61790-4120
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The crustacean mandibular organ (MO) produces methyl farnesoate (MF), a juvenile hormone-related compound thought to have roles in crustacean reproduction and development. Therefore, the control of MF production by the MO has been of considerable interest. Current evidence indicates that the MO is negatively regulated by peptides present in the eyestalk (MO inhibiting factor, MO-IH). Several eyestalk neuropeptides have been identified that inhibit MF synthesis by MO incubated in vitro. The amino acid sequences of these MO-IH peptides are similar to peptides in the crustacean hyperglycemic hormone (CHH) family of neuropeptides. In addition, there appears to be a compound in the eyestalk that lowers hemolymph levels of MF in vivo but does not directly affect the MO in vitro. The inhibition of MF synthesis by eyestalk peptides involves the inhibition of farnesoic acid O-methyl transferase, the last enzyme in the MF biosynthetic pathway. The activity of this enzyme is affected by cyclic nucleotides, suggesting that these compounds may be involved in the signal transduction pathway mediating the effects of MO-IH.
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The crustacean mandibular organ (MO) was first identified by Le Roux (1968)
and has since been identified in a large number of crustaceans. In decapods, this glandular tissue is located at the base of the tendon associated with the posterior abductor muscle of the mandibles. Initial studies by several authors suggested that the MO might be involved in regulating reproduction (Le Roux, 1968; Hinsch, 1981), and molting (Aoto et al., 1974; Byard et al., 1975; Yudin et al., 1980). This view was strengthened by ultrastructural studies of this tissue, which showed cells with extensive smooth endoplasmic reticulum and abundant mitochondria, features typical of steroid-secreting cells. Variations in MO structure during reproduction and molting suggested that its activity changed during these processes (Le Roux, 1968; Hinsch, 1981).
Such conclusions were supported by the identification of methyl farnesoate (MF) as a secretory product of the MO (Borst et al., 1987; Laufer et al., 1987a). MF is a member of the juvenile hormone family of compounds, and its structure is nearly identical to that of JH III, the most ubiquitous of the juvenile hormones (Fig. 1). This chemical similarity suggested that MF might have roles in crustaceans similar to those of JH in insects (e.g., the regulation of metamorphosis, growth, reproduction and behavior; see Riddiford, 1994; Wyatt and Davey, 1996; Homola and Chang, 1997). In the past few years, evidence has accumulated that supports roles for MF in reproduction (Laufer et al., 1998; Reddy and Ramamurthi, 1998), molting (Tamone and Chang, 1993; Chang et al., 1993), metamorphosis (Borst et al., 1987; Abdu et al., 1998), behavior (Sagi et al., 1994; Borst et al., 1995a) and possibly stress (Lovett et al., 1997, 2001).
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A major difficulty in investigating the roles of MF has been the anatomical location of the MO, which has made its surgical removal difficult. Thus, it has not been possible to do ‘classical’ ablation-replacement studies to investigate MF function. As a result, most investigators have sought to demonstrate a correlation between a physiological event and either the synthetic rate of MF by the MO or the hemolymph level of MF. However, the episodic nature of MF production (Borst and Tsukimura, 1992
) has made even this approach difficult. To address these experimental difficulties, several laboratories have studied the molecular mechanisms involved in regulating MF production, since such information might be useful in regulating levels of MF in vivo. In this paper, we will review the current research on this topic. |
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Neuroendocrine peptides are important regulators of the insect corpus allatum, and both stimulatory (allatotropins) and inhibitory (allatostatins) peptides have been identified (Tobe and Stay, 1985
; Goodman, 1990; Stay et al., 1994). Thus, it was not surprising that peptides also have a role in the regulation of the MO, though to date only peptides that inhibit this gland (MO-inhibiting hormone or MO-IH) have been identified. Interestingly, none of the MO-IHs are structurally related to the family of allatostatins though variants of allatostatins have been isolated in crustaceans (Duve et al., 1997).
One particularly important source of MO-IHs in decapod crustaceans is the sinus gland (SG), a neurohemal organ found in the eyestalk. This tissue produces numerous neuroendocrine compounds that affect a variety of physiological functions, in some cases through modulation of other endocrine glands. Several observations indicate that that the SG produces a compound(s) that affects the function of the MO. Studies by LeRoux and others showed that removal of the SG by eyestalk ablation (ESA) causes hypertrophy and ultrastructural changes in the MO of adults (LeRoux, 1968; Bazin, 1976; Hinsch, 1977) and larvae (Le Roux, 1983).
These observations were followed by the discovery that ESA elevates hemolymph levels of MF in several species (e.g., Laufer et al., 1987a; Tsukimura and Borst, 1992; Borst et al., 1995b). For example, MF levels in the lobster Homarus americanus increase over several days after ESA, often rising from undetectable levels to more than 30 ng/ml (Fig. 2). The elevation in hemolymph levels of MF by ESA reflects at least partly an increase in MF synthesis by the MO (Laufer et al., 1987b; Borst and Laufer, 1990; Wainwright et al., 1996a, b). In addition, incubating MO in vitro with extracts of the entire eyestalk or the SG can inhibit MF synthesis. This has been demonstrated in several species, including the spider crab Libinia emarginata (Laufer et al., 1987b), the edible crab Cancer pagurus (Wainwright et al., 1996b) and H. americanus (Borst, unpublished results). Consistent with this in vitro effect is the observation that the injection of ESA animals with SG extract causes a rapid and reversible decrease in hemolymph levels of MF (Tsukimura and Borst, 1992; Fig. 3).
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= 0.05). Similar levels of inhibition were observed with as little as 0.1 SGEyestalk compounds that inhibit MO synthesis of MF
Several approaches have been used to identify MO-IHs in SG extracts. One approach is to incubate MOs in vitro with potential inhibiting compounds. The level of MF synthesis by the treated MO is then compared to the MF synthesis measured in the untreated contralateral gland (Laufer et al., 1987b
). Using this in vitro approach, Landau et al. (1989) incubated MO from the crayfish Procambarus clarkii with known eyestalk peptides. Pigment dispersing hormone (PDH) and red pigment concentrating hormone (RPCH) were found to inhibit and stimulate, respectively, MF synthesis. However, these results have not been confirmed in other species (Wainwright et al., 1996b; Liu and Laufer, 1996).
A similar in vitro bioassay was also used to isolate and characterize MO-IH from the SG of C. pagurus. Fractionation of SG extracts by reversed phase HPLC identified two peptides (MO-IH-1 and MO-IH-2) that inhibit MF synthesis by MO. Other eyestalk peptides, such as CHH had no activity. Both MO-IH-1 and MO-IH-2 contain 78 amino acids and differ in sequence by a single residue (Wainwright et al., 1996b). The amino acids sequences of MO-IH-1 and MO-IH-2 are similar to molt inhibiting hormone (MIH) and vitellogenesis inhibiting hormone (VIH), two other SG peptides that also contain 78 amino acids. For example, the amino acid sequence of MO-IH-1 is 59% similar to the sequence of its own MIH (Chung et al., 1996), 55% similar to MIH from C. maenas (Webster, 1991) and 42% similarity to VIH from H. americanus (De Kleijn et al., 1994). The MIH/VIH peptides form a subgroup in the crustacean hyperglycemic hormone (CHH) family of neuropeptides (Keller, 1992; Van Herp, 1998; Wainwright et al., 1998). Hence, MO-IH-1 has modest similarity (20% and 23%) to its own CHH (Chung et al., 1998) and to CHH from C. maenas (Kegel et al., 1989), respectively. This degree of similarity is comparable to that of MIH to CHH. MIH from C. pagurus also has a low degree of similarity (28% and 27%) to its own CHH and to CHH from C. maenas, respectively.
The relationship of MO-IH-1 and MO-IH-2 from C. pagurus to other MIH/VIH peptides was confirmed by an analysis of their cDNAs (Tang et al., 1999). The cDNAs for MO-IH-1 and MO-IH-2 encode a 34-residue signal sequence and the 78-residue mature peptide sequence. Member of the MIH/VIH peptides have a similar structure, lacking the additional precursor peptides found in other members of the CHH family (see below).
MO-IH peptides have also been identified in L. emarginata with an in vitro bioassay using dissociated cells (Liu and Laufer, 1996). Three peptide fractions were detected that inhibited MF synthesis, one of which (P22) has been sequenced (Liu et al., 1997a). The sequence of this 72 amino acid peptide was 81% and 72% similar to the sequences of CHH from C. pagurus (Chung et al., 1998) and C. maenas (Kegel et al., 1989), respectively. Indeed, the MOIH from L. emarginata had CHH activity, causing a transient increase in glucose levels when injected into the fiddler crab Uca pugilator (Liu et al., 1997a). The similarity of the MO-IH (P22) from L. emarginata to other CHH peptides was confirmed by comparing its cDNA to that for other CHH peptides. Besides the 72-residue mature peptide, the cDNA for MO-IH (P22) also encodes a 26-residue signal sequence, a 34-residue precursor related peptide, a dipeptide N-terminal fragment and a tripeptide C-terminal fragment, all of which are removed post-translationally (Liu et al., 1997b). Similar peptide fragments are produced during the maturation of CHH in other species.
In parallel with the above studies, we developed an in vivo bioassay to identify MO-IH peptides. This approach uses a sensitive (<0.5 ng/ml) HPLC method to measure hemolymph levels of MF. As demonstrated in Figure 3, the injection of SG extracts into ESA animal (which have high levels of MF) causes a rapid but transient decrease in MF levels. For the in vivo bioassay, ESA animals are injected with potential MO-IHs and their hemolymph levels of MF determined immediately before and 3–4 hr after treatment. The change in MF levels (expressed either as % initial MF level or the MF inhibition index) is then calculated.
We have used the in vivo bioassay to study MO-IH in H. americanus (Tsukimura and Borst, 1990) and C. pagurus (Borst et al., 1998). SG extracts from each of these species were fractionated by reversed phase HPLC. The fractions were tested with the bioassay to identify those that lowered hemolymph levels of MF. In C. pagurus these fractions were distinct from those that contained MO-IH-1 and MO-IH-2, determined either by an RIA for these peptides (see Fig. 4) or using the in vitro bioassay (Wainwright et al., 1996b). Likewise, injection of ESA C. pagurus with purified MO-IH-1 or MO-IH-2 had no effect on hemolymph levels of MF, even at high doses (20 pmol/animal) of these peptides (Borst et al., 1998). Since a single SG contains approximately 10 pmol of MO-IH-1 and 5 pmol MO-IH-2, this treatment must be near the physiologically relevant maximum (the total amount of MO-IH found in two SG) (Wainwright et al., 1996b). The SG compounds responsible for lowering MF levels in vivo from both C. pagurus and H. americanus are heat and acid stable and sensitive to protease digestion, indicating that they are peptides. We are currently continuing efforts to identify the peptides responsible for the in vivo inhibition of the MO.
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These observations indicate that SG contains peptides that can inhibit the gland directly and others that affect the gland indirectly. The inability of this latter group of compounds to inhibit MO function in vitro indicates that there must be an intermediate compound(s) involved. One possible group of intermediate compounds is the biogenic amines. Serotonin has been reported to inhibit MO function in vitro (Homola and Laufer, 1989
), although its role in MO function has not been clarified. Biogenic amines (e.g., octopamine and dopamine) have been shown to affect corpora allata activity in many insects (Thompson et al., 1990; Pastor et al., 1991; Rachinsky, 1994), though the response (inhibitory or stimulatory) varies with the stage of the animal (Granger et al., 1996). Whether such variations in responsiveness to biogenic amines occur in crustacean MOs has not yet been investigated.
In view of the discovery that the SG contains multiple peptides that inhibit MF synthesis by the MO, the true physiological roles of these peptides remain uncertain. This is certainly the case for the MO-IH-1 and MO-IH-2 from C. pagurus, since neither affected hemolymph levels of MF when injected in vivo. Similar concerns can be raised regarding the MO-IH (P22) isolated from L. emarginata. While the effect of the L. emarginata MO-IH (P22) in vitro suggests that it is a regulator of the MO, there is no report that this peptide affects MF levels in vivo, though it does affect hemolymph levels of glucose. When coupled with its amino acid sequence, these data suggest that the L. emarginata MO-IH (P22) is a CHH. If so, the regulation of MF synthesis would have to be added as yet another one of the functions (including glucose metabolism, vitellogenesis, molting, and osmoregulation) apparently regulated by CHH (Van Herp, 1998; Webster, 1998).
However, the ED50 for the in vitro inhibition of MF synthesis in L. emarginata using MO-IH (P22) is 1 nM (Liu et al., 1997a). In those species in which CHH has been measured (C. pagurus, Webster, 1996 and H. americanus, Chang et al., 1998), the hemolymph levels of this peptide are generally very low (<10 pM) in unstressed animals. Stress causes a striking increase in CHH levels (to about 50 pM) in both species and appears to have a similar effect in C. maenas (Santos and Keller, 1993). However, these stress levels are still much lower than the ED50 value (1 nM) for the inhibition of MF synthesis in vitro (Liu et al., 1997a). In addition, it should be noted that stress causes a substantial rise in the hemolymph levels of MF in C. maenas and L. emarginata (Lovett et al., 1997, 2001; Ogan et al., 1997). It is not clear how a CHH can be the inhibitor of MF synthesis (MO-IH) if MF levels rise during conditions known to elevate CHH levels.
In summary, a number of peptides that regulate the MO have been identified, but their physiological roles in regulating the MO in vivo are not clear. Until these issues have been clarified it will be difficult to evaluate the relative importance of these SG peptides. Sorting out the roles of these peptides will provide a closer view of how this endocrine system is regulated and may illuminate further the importance of MF in crustaceans.
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THE BIOSYNTHETIC PATHWAY OF METHYL FARNESOATE |
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The biosynthetic pathway of MF (see Fig. 5) appears to be similar to the general mevalonate pathway for acyclic isoprenoids (Goldstein and Brown, 1990
). Indeed, many of these steps have been demonstrated for the synthesis of juvenile hormone (Schooley and Baker, 1985; Goodman, 1990). The initial steps of this pathway involve the synthesis of mevalonate from acetate via HMG-CoA synthase and HMG-CoA reductase, followed by its conversion to isopentyl pyrophosphate. Three units of isopentyl pyrophosphate (one of which isomerizes to 3,3'-dimethylallyl pyrophosphate) are condensed to form farnesyl pyrophosphate, which is hydrolyzed to farnesol and oxidized in two steps to form farnesoic acid. The farnesoic acid is then converted to MF by farnesoic acid O-methyl transferase (MeT),
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The applicability of this general pathway to MF biosynthesis is supported by studies using radiolabeled precursors. Thus, the time course of incorporation of radiolabeled acetate into MF as well as biosynthetic intermediates (e.g., farnesol and farnesoic acid) is consistent with this pathway (Tobe et al., 1989
; Wainwright et al., 1998). Similarly, the decrease in hemolymph levels of MF observed after treatment of ESA crabs with mevinolin, a potent inhibitor of HMG-CoA reductase, indicates the importance of this enzyme in MF production (Henry et al., 1999).
The only enzyme in the MF biosynthetic pathway that has been studied to date is MeT, which has been characterized in H. americanus (Claerhout et al., 1996), L. emarginata, (Ogan et al., 1997) and C. pagurus (Wainwright et al., 1998). MeT catalyzes the final step in the pathway, the transfer of a methyl group from S-adenosylmethionine to farnesoic acid. Similar to the O-methyl transferase in the insect corpus allatum, MeT in the MO is a cytosolic enzyme. In H. americanus, MeT has a MW of about 36,000 and a Km of 4–5 µM (Table 1). ESA animals have substantially higher levels of MeT activity, which results from an increase in the Vmax of the enzyme. The treatment of ESA lobsters in vivo with SG extract caused a reduction (up to 99%) in the Vmax of the enzyme (Claerhout et al., 1996; Table 1). Similarly, MO-IH-1 has been shown to affect MeT activity of MO treated in vitro (Wainwright et al., 1998).
These data indicate that MeT is a key regulatory step in the MF biosynthetic pathway. Indeed, there is a close correlation between MeT activity and hemolymph levels of MF in L. emarginata (Ogan et al., 1997). Consistent with this conclusion is an increase in farnesoic acid levels in MO treated in vitro with SG extract (Wainwright et al., 1998). The regulation of MF synthesis at its terminal step suggests that the MO may switch from MF production to farnesoic acid production. Indeed, it has been previously suggested that farnesoic acid may be another important product of the MO (Tobe et al., 1989). While these authors were unable to detect farnesoic acid in hemolymph, there may be some physiological conditions during which it does occur.
The regulation of MeT in the MF biosynthetic pathway is in contrast to the regulation of the JH biosynthetic pathway in insects. In the cockroach Diplotera punctata, inhibition of JH synthesis by corpora allata incubated with allatostatin did not reflect a change in methyl transferase activity (Feyereisen and Farnsworth, 1987). Rather, this inhibitory peptide appears to affect JH synthesis by regulating the transport of acetate from the mitochondria (Sutherland and Feyereisen, 1996). Likewise, the increase in JH synthesis observed after treating corpora allata from the tobacco hornworm, Manduca sexta with allatotropin does not appear to be due to an increase in methyl transferase activity (Unni et al., 1991). Nevertheless, at some developmental stages the activity of MeT in the corpora allata does appear to be regulated. For example, the corpora allata of M. sexta switch from JH production to JH acid production during the fifth instar (Bhaskaran et al., 1986). Whether this regulation of the corpus allatum is analogous to the regulation of MeT in the MO is not yet clear.
The identification and characterization of MeT in the MO provides an important link between SG peptides and their regulation of MF synthesis. In indicated above, MeT has been characterized in three species to date. In all three species, the activity of MeT is decreased when the MO is treated with SG peptides in vitro or in vivo. It would be useful to examine other steps in the MF biosynthetic pathway, to see if these are also regulated by SG peptides. A better understanding of other enzymes of the pathway would also be useful in comparing the process of MF synthesis to that of JH synthesis in the insect corpus allatum.
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SIGNAL TRANSDUCTION MECHANISMS |
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Several investigators have studied the intracellular events that mediate the effects of SG peptides on MO function. Landau et al. (1989)
showed that the Ca2+ ionophore A23187
[GenBank]
decreased MF synthesis by MO from P. clarkii, leading to the suggestion that intracellular Ca2+ levels are involved in the signal transduction pathway. Tsukimura et al. (1993) showed that analogues of both cGMP and cAMP could inhibit the in vitro synthesis of MF by MO from H. americanus. However, the tissue was approximately 100-fold more sensitive to 8-bromo-cGMP (I50 = 10–7 M) than to 8-bromo-cAMP (I50 = 10–5 M). In addition, incubation of MO with SG extracts (0.02 SG/ml) increase cGMP levels two-fold (to 0.2 x 10–7 M) but had no effect on cAMP levels (which remained unchanged at 
1.7 x 10–7 M). This latter result is not particularly surprising, given that CHH (which would have been present in the SG extract) has been shown to elevate cGMP levels in every lobster tissue tested (Goy et al., 1987). In contrast, only analogues of cAMP can inhibit MF synthesis in the MO from C. pagurus. Both 8-bromo-cAMP (I50 = 50 µM) and compounds (e.g., forskolin) that elevate intracellular levels of cAMP were inhibitory (Wainwright et al., 1999). Other compounds, including those known to affect the Ca2+, cGMP, and protein kinase C pathways had no effect on MF synthesis. Furthermore, treatment of MO membranes to MO-IH-1 caused a dose-dependent increase in cAMP production, with 100 nM (10 SG equivalents/ml) causing a 2-fold increase (Wainwright et al., 1999).
Additional research is needed to clarify these intracellular mechanisms. Nevertheless, it does appear that cyclic nucleotides have a central role in the regulation of the MO, although cGMP appears to be more important in H. americanus and cAMP appears to be more important in C. pagurus. Such differences may reflect the existence of multiple parallel signaling pathways for regulating MF synthesis. The prominence of each pathway may differ between species. An analogous situation appears to exist in the insect corpus allatum, where multiple factors (including cyclic nucleotides, Ca2+ and phosphatidyinositol) have all been shown to affect the synthesis of JH (Stay et al., 1994).
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SUMMARY |
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During the past decade considerable progress has been made in understanding the regulation of MF synthesis by the crustacean MO. Not surprisingly, the overall regulation of MF synthesis is similar to the regulation of JH synthesis by the corpus allatum. As in the corpora allata of many insects, the MO is negatively regulated by neuropeptides (MO-IH). Putative MO-IHs have been isolated from the sinus glands of two species, and have been sequenced and their cDNAs cloned. Another class of inhibitory peptide, one that acts indirectly on the gland, has also been identified, although not completely characterized. This last class indicates that there must be additional, intermediary compounds that regulate the MO. The physiological roles of these peptides in the regulation of MF levels are not clear. However, the development of antisera to these compounds should allow their roles to be determined.
The inhibitory peptides from the sinus gland act at least partly by inhibiting the activity of the final enzyme involved in MF synthesis, O-methyl transferase. In this way, the regulation of the MO appears to differ from that of the corpus allatum, in which JH synthesis appears to be regulated at the very initial stages of the pathway. The importance of this difference is unclear. Compounds regulating the MO may affect multiple enzymes in the MF synthesis pathway. Alternately, inhibition of MeT may allow the MO to produce and release farnesoic acid at certain stages or in response to particular situations.
The signal transduction pathway involved in regulating both the MO and the corpus allatum appears to be complex, and may involve several different second messenger pathways acting in parallel. Understanding the importance of these pathways in the synthesis of MF may provide rewarding insights into the regulation of this compound.
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ACKNOWLEDGMENTS |
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The authors gratefully acknowledge Dr. Ernie Chang (Bodega Marine Lab, University of California, Davis) who provided HPLC fractions of SG from H. americanus and Drs. Geoff Wainwright and Huw Rees (University of Liverpool) for help in experiments with C. pagurus. We express our appreciation to Dr. John Hatle for comments on the manuscript. Parts of this research were supported by the NSF (IBN 93-19206), NIH (R15-HD37953-01), and a Fogarty International Fellowship (1 FO6 TW02253-01).
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FOOTNOTES |
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1 From the Symposium Recent Progress in Crustacean Endocrinology: A Symposium in Honor of Milton Fingerman presented at the Annual Meeting of the Society for Comparative and Integrative Biology, 4–8 January 2000, Atlanta, Georgia.
2 E-mail: dwborst{at}ilstu.edu
3 Current address: Department of Biology, California State University, Fresno, CA 93740.
4 Current address: Department of Biology, Purdue University, North Central, Westville, IN 46391.
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