© 2001 by The Society for Integrative and Comparative Biology
Crustacean Pigmentary-Effector Hormones: Chemistry and Functions of RPCH, PDH, and Related Peptides1
1 Department of Biology, University of West Florida, 11000 University Parkway, Pensacola, Florida 32514-5751
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 SYNOPSIS INTRODUCTIONPIGMENT-CONCENTRATING HORMONESPIGMENT-DISPERSING HORMONESPERSPECTIVESReferences |
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Integumental color changes and eye pigment movements in crustaceans are regulated by pigmentary-effector hormones. The identified hormones include: an octapeptide RPCH (red pigment-concentrating hormone) and several forms of octadecapeptide PDH (pigment-dispersing hormone:
-PDH, ß-PDH). RPCH-related peptides (AKHs, adipokinetic hormones) and PDH-related peptides (PDFs, pigment-dispersing factors) occur in insects, and are recognized as members of AKH/RPCH and PDH/PDF peptide families. The domain for mature peptide is located between the signal peptide and precursor-related peptide in AKH/RPCH precursors, and at the C-terminal end in the PDH/PDF precursors. The precursor-related (associated) peptides in RPCH and PDH precursors in Crustacea show little or no similarity to corresponding domains of AKH and PDF precursors in insects. Although the functions of precursor-related peptides are unknown, the mature peptides are shown to serve diverse functions. RPCH's actions in crustaceans include: pigment concentration in one or more types of chromatophores, dark-adaptational screening pigment movement in distal eye pigment cells, increase of retinal sensitivity, and neuromodulation. The related AKHs largely influence metabolism in insects, although they serve additional functions. PDHs trigger pigment dispersion in chromatophores and induce light-adaptational screening pigment movements in extraretinular eye pigment cells. The related PDFs appear to serve as a transmitter of circadian signals in the regulation of biological rhythms in insects. Evolutionary relationships among the PDH/PDF peptides and directions for future research are discussed. |
INTRODUCTION |
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SYNOPSISINTRODUCTIONPIGMENT-CONCENTRATING HORMONESPIGMENT-DISPERSING HORMONESPERSPECTIVESReferences |
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Pigmentary effectors enable crustaceans to display rapidly reversible integumental color changes and retinal screening pigment movements. Color changes result from dispersion or concentration (aggregation) of pigment granules within epithelial chromatophores. Retinal screening pigment movements, occurring as part of light/dark-adaptive photomechanical changes in the compound eye, may be restricted to retinular cells (photoreceptor cells) or extended to involve other ommatidial pigment cells—reflecting pigment cells, distal pigment cells, or both, depending on the species (Fig. 1).
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The discovery of hormonal involvement in the control of pigment movements in crustacean chromatophores (Koller, 1927
; Perkins, 1928) and distal pigment cells in the eye (Kleinholz, 1934) triggered intensive studies on the regulation of pigmentary effectors. Starting with the work on rhythms of color change in the blue crab, Callinectes sapidus (Fingerman, 1955), Milton Fingerman made extensive contributions toward the elucidation of the regulation of crustacean pigmentary effectors, especially in areas such as the localization and differentiation of pigmentary-effector hormones, role of biogenic amines in hormone release, and cellular mechanisms of hormone action. These original contributions and his informative reviews (e.g., Fingerman, 1963, 1966, 1969, 1970, 1985, 1988; Fingerman et al., 1994) facilitated advancement of the field and promoted increased interest in crustacean endocrinology. In his honor, I will present here a progress report on the chemistry and actions of crustacean pigmentary-effector peptide hormones, including pertinent recent work on related peptides from insects.
Studies on decapod Crustacea indicate that, whereas screening pigment movements within retinular cells are triggered mainly by a direct action of light, the extra-retinular ommatidial cells and epithelial chromatophores are under hormonal control. The pigmentary-effector hormones are present in the eyestalks and in extra-eyestalk nervous tissues. Extracts of any of these tissues can elicit a complex set of responses, light- or dark-adaptational pigment translocation in extraretinular ommatidial cells, as well as dispersion or concentration of pigment granules in chromatophores. This is due to the widespread distribution of mutually antagonistic hormones in various parts of the nervous system. The total number of pigmentary-effector hormones present in any species remains unknown, but they can be differentiated into two sets. The hormones triggering chromatophoral pigment dispersion and ommatidial light adaptation belong to one set, and these are distinct from those responsible for chromatophoral pigment concentration and ommatidial dark adaptation (Kleinholz and Kimball, 1965; Fingerman and Bartell, 1969; Rao, 1985; Fingerman, 1988).
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PIGMENT-CONCENTRATING HORMONES |
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SYNOPSISINTRODUCTIONPIGMENT-CONCENTRATING HORMONESPIGMENT-DISPERSING HORMONESPERSPECTIVESReferences |
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Red pigment-concentrating hormone (RPCH)
In gel filtration chromatography (Sephadex G-25) of eyestalk extracts, two distinct zones of pigment-concentrating activity are evident (Skorkowski, 1971
; Fingerman, 1973). So far, however, only one of these hormones, red pigment-concentrating hormone (RPCH), has been characterized. RPCH is an octapeptide: pGlu-Leu-Asn-Phe-Ser-Pro-Gly-Trp-NH2 (Fernlund and Josefsson, 1972) and first identified from eyestalks of Pandalus borealis. Subsequently, RPCHs with an identical sequence have been characterized from Cancer magister, Carcinus maenas, Orconectes limosus (Gaus et al., 1990), Penaeus japonicus (Yang et al., 1999), Uca pugilator (K. R. Rao and J. P. Riehm, unpublished), and Callinectes sapidus (sequence identified by cDNA cloning; Klein et al., 1995a). Based on the amino-acid composition and chromatographic behavior, the RPCHs of several other crustaceans, Liocarcinus puber, Nephrops norvegica, Pacifastacus leniusculus, Procambarus clarkii, Palaemon squilla, Palaemonetes pugio, Homarus americanus, and Cardisoma carnifex, are thought to be identical to Pandalus RPCH (see Gaus et al., 1990; Rodriguez-Sosa et al., 1994). This indicates that the structure of RPCH is highly conserved among crustacean species.
AKH/RPCH family of peptides
A decapeptide adipokinetic hormone from locusts (Locusta migratoria AKH I: pGlu-Leu-Asn-Phe-Thr-Pro-Asn-Trp-Gly-Thr-NH2) is the first identified RPCH-related peptide in insects (Stone et al., 1976). Subsequently more than thirty structurally-related peptides have been characterized from diverse insect species, and are collectively recognized as the AKH/RPCH family of peptides (review: Gäde et al., 1997). Their common features are: N-terminal pGlu, an aromatic residue (Phe or Tyr) at position 4, Trp at position 8, and an amidated C-terminus. Whereas the primary structure of RPCH is conserved in Crustacea, the related peptides in insects show considerable heterogeneity—including variations in chain length (8, 9, or 10 residues) and intramolecular residue substitutions. In many species of insects two peptides of the AKH/RPCH family are found (Gäde et al., 1994), and in some species (e.g., Locusta migratoria) three different AKH peptides derived from distinct precursors (Bogerd et al., 1995) are identified.
Although RPCH itself has not been found in insects, several of the octapeptide AKHs from insects are very similar to RPCH—with some differing from RPCH at a single residue: Thr6 as in AKH II from Schistocerca gregaria, or Ala6 as in Locusta migratoria AKH II (Siegert et al., 1985). Residue substitutions at two positions are seen in several others: Thr3 and Asp7 (Phormia terraenovae HrTH; Gäde et al., 1990); Val2 and Thr6 (Gryllus bimaculatus AKH; Gäde and Rinehart, 1990); Val2 and Asn7 (Periplaneta americana CAH I; Scarborough et al., 1984); Thr5 and Trp7 (Locusta migratoria AKH III; Oudejans et al., 1991); Tyr2 and Thr6 (Onitis aygulus CC I: Gäde, 1997; Ona-CC: Gäde et al., 1997).
Attempts have been made to speculate evolutionary relationships among RPCH/AKH peptides by means of a computer program utilizing Protein Parsimony algorithm. Such an analysis pointed to the possibility that RPCH may have served as an ancestral peptide for the AKH family, and that an evolutionarily ancient step close to the time of origin of insects may have separated the octapeptides from the decapeptide/nonapeptide AKHs (see Gäde et al., 1994).
Precursors of RPCH and AKH
Molecular cloning studies indicate that the precursors of crustacean RPCH (Linck et al., 1993; Klein et al., 1995a) and insect AKHs (Bradfield and Keeley, 1989; Noyes and Schaffer, 1990; Schulz-Aellen et al., 1989; O'Shea and Rayne, 1992; Fischer-Lougheed et al.,1993; Noyes et al., 1995; Bogerd et al., 1995) share the following general organization and contain: a signal peptide, the peptide RPCH or AKH, a glycine residue, a dibasic cleavage site, and a precursor related peptide. Posttranslational processing is assumed to convert the N-terminal glutamine in RPCH and AKHs to pyroglutamate and the glycine (preceding the cleavage site) is used as an amide donor. The regions encoding RPCH and AKH show the expected high degree of similarity, but the signal peptide and the precursor-related peptide in RPCH precursors show little or no similarity to the corresponding components of AKH precursors. Whereas the precursor-related peptides (RPRPs) in RPCH precursors contain 73 (Callinectes sapidus) or 74 amino acids (Carcinus maenas), the corresponding peptides (APRPs) in AKH precursors are shorter—e.g., 28 residues occurring as dimers (AKH I and AKH II precursors in Schistocerca and Locusta); 44 residues (AKH III precursor in Locusta); or 46 residues (AKH precursor in Drosophila)—and show no similarity in sequence to crustacean RPRPs. The signal peptides in RPCH precursors contain 25 amino acids, whereas the corresponding peptides in insects contain 22 residues and show little similarity with the former.
There is, however, considerable similarity among the precursors within a taxonomic group. For example, among the RPCH precursors from the crabs Carcinus and Callinectes, there is 90% similarity in the RPRPs and 84% similarity in the signal peptides. The APRPs of the AKH II precursors from the locusts Schistocerca gregaria and Schistocerca nitans differ from each other at only one position. The AKH I and II precursors of Locusta migratoria are highly homologous to the Schistocerca AKH precursors, whereas the AKH III precursor is least homologous and is thought to be evolutionarily more related to the Manduca and Drosophila AKH precursors and to the crustacean RPCH precursors (Bogerd et al., 1995).
The functions of crustacean RPRPs and insect APRPs remain unknown. The APRPs isolated from the lubber grasshopper Romalea microptera failed to stimulate hyperlipemia, hypertrehalosemia, fat body glycogen activation, Malpighian tubule secretion, and hindgut myotropia, and did not enhance AKH activity when APRPs and AKH are delivered together (Hatle and Spring, 1999).
Functions of AKH/RPCH family of peptides
Because of their structural relationship, RPCH and AKHs are able to mimic each other in cross-tests and elicit hyperlipemia in locusts, hyperglycemia in cockroaches, and chromatophore pigment concentration in shrimp (reviews: Rao, 1985; Fingerman, 1988). Although these peptides show biological cross-reactivity, each of these hormones is generally more reactive in its own system than in the cross-test system. A comparison of the relative potency of RPCH and nine different AKHs in eliciting pigment concentration in erythrophores of the crayfish Cambarellus shufeldtii (Mohrherr et al., 1987; Rao and Riehm, 1991) revealed that RPCH is the most potent, followed by Schistocerca AKH II ([Thr6]-RPCH) with 81% potency relative to RPCH, and peptides with Val2 substitutions being the least potent: relative potencies of 0.06% (Gryllus AKH; [Val2, Thr6]-RPCH) and 0.05% (Periplaneta CAH I; [Val2, Asn7]-RPCH). In the crayfish erythrophore assays Periplaneta CAH I was 340-fold less potent than Periplaneta CAH II ([Thr2, Thr5, Asn7]-RPCH) (Mohrherr et al., 1987; Rao and Riehm, 1991), whereas these two peptides were equipotent in insect assay systems for cardioacceleration and hyperglycemia (Scarborough et al., 1984). Thus, while maintaining some critical degree of sequence homology, the AKH/RPCH family of peptides seemed to have evolved appropriate molecular modifications to serve unique functions in different species (reviews: Gäde et al., 1994; Rao and Riehm, 1991).
In insects, AKH peptides elicit one or more of the following: hyperlipemia, hyperglycemia, hyptertrehalosemia, cardioaccelaration, and myotropic activity, depending on the species (Gäde et al., 1994, 1997). Additional actions include hyperprolinemia in beetles (Gäde, 1997) and inhibition of vitellogenin synthesis in the locust fat body at the oviposition stage (Glinka et al., 1995).
Unlike the AKH's functions in insects, RPCH is not known to exert any metabolic actions in crustaceans although it is implicated in extrapigmentary roles such as the stimulation of methylfarnesoate secretion from mandibular glands (Laufer et al., 1987) and neuromodulation. RPCH has been shown to modulate the stomatogastric system of Cancer borealis and Panulirus interruptus, and modify the pyloric, gastric mill, and cardiac sac rhythms (Nusbaum and Marder, 1988; Dickinson et al., 1993, 1997), and also modulate the swimmeret rhythm of Pacifastacus leniusculus (Sherf and Mulloney, 1991).
The modulatory effects of RPCH also extend to crustacean photoreceptor cells. RPCH enhances the electroretinogram (ERG) amplitude in isolated eyes of Orconectes limosus (Gaus and Stieve, 1992). RPCH induces dark-adaptational movement of screening pigment in the distal eye pigment cells, enhances ERG amplitude in a dose-dependent manner, and potentiates ERG amplitude in both light-adapted and dark-adapted Procambarus clarkii (Garfias et al., 1995). RPCH's effects on ERG may result from both a direct action on photoreceptors, presumably at some stage of the phototransduction cascade, and an indirect effect resulting from dark-adaptational screening pigment translocation in distal pigment cells. RPCH does not cause positional changes of screening pigment (called proximal pigment) in photoreceptor cells of Procambarus clarkii (Garfias et al., 1995).
The action of RPCH on crustacean chromatophores varies with the species. As reviewed earlier (Rao and Riehm, 1988a, 1991; Fingerman, 1988), RPCH failed to act on the chromatophores of the stomatopod Squilla empusa and the isopod Ligia occidentalis, and showed differing effects on chromatophores of decapod species. Thus RPCH causes pigment concentration in erythrophores alone (e.g., Uca pugilator, Cambarellus shufeldtii); in leucophores as well as erythrophores (e.g., Palaemon squilla, Penaeus aztecus); or in melanophores, leucophores, and erythrophores (e.g., Crangon crangon). In Penaeus japonicus RPCH induces pigment concentration in all four types of chromatophores, including xanthophores, but is least effective on leucophores (Yang et al., 1999). These results, the finding of two zones of pigment-concentrating activity in gel filtration chromatography, and evidence from studies on the control of hormone release (Fingerman, 1988; Fingerman et al., 1994) point to the occurrence of additional pigment-concentrating hormones that remain to be characterized. Interestingly, in studies of RPCH precursor in Callinectes sapidus, Northern blots showed two hybridization products, one representing the RPCH-mRNA and the other of unknown origin (Klein et al., 1995a). In in situ hybridization studies, some cells in the eyestalk ganglia of Callinectes could be stained with an RPCH antiserum, but not with a specific RPCH c-RNA probe (Klein et al., 1995b), pointing to the presence of additional RPCH-like molecules. It is likely that pigment-concentrating hormones other than RPCH may be present in very low amounts, but it should be possible to characterize such molecules utilizing the current mass spectroscopy techniques.
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PIGMENT-DISPERSING HORMONES |
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SYNOPSISINTRODUCTIONPIGMENT-CONCENTRATING HORMONESPIGMENT-DISPERSING HORMONESPERSPECTIVESReferences |
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Pigment-dispersing hormones (PDHs) in crustaceans
Cation-exchange chromatography of eyestalk extracts reveals several zones of PDH activity, 3 to 5 depending on the species. The first of these hormones to be characterized is an octadecapeptide called light-adapting distal retinal pigment hormone (DRPH) from the eyestalks of Pandalus borealis (Ferlund, 1976
). This peptide triggers not only light-adaptational screening pigment movements in the eye, but also pigment dispersion in chromatophores (Kleinholz, 1975), and is referred to later as -PDH. The sequence of -PDH is: Asn-Ser-Gly-Met-Ile-Asn-Ser-Ile-Leu-Gly-Ile-Pro-Arg-Val-Met-Thr-Glu-Ala-NH2. Subsequently, an octadecapeptide differing from -PDH at six positions (Glu3, Leu4, Leu11, Lys13, Asn16, and Asp17), and designated as ß-PDH, has been identified as the major form of pigment-dispersing hormone in eyestalks of Uca pugilator (Rao et al., 1985). Since then, PDHs from 14 additional crustacean species have been characterized (Fig. 2).
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structure deduced from the sequencing of precursor cDNA, but not verified by amino acid sequencing of purified peptideß-PDH with an identical structure has been identified as the major form of PDH in the brachyuran crabs, Cancer magister (Kleinholz et al., 1986
), Callinectes sapidus (Mohrherr et al., 1990), and Carcinus maenas (Klein et al., 1992; Löhr et al., 1993). In crayfish the major form of PDH is either ß-PDH, as in Pacifastacus leniusculus (Rao and Riehm, 1993), or [Glu17]-ß-PDH as found in Procambarus clarkii (McCallum et al., 1991), Orconectes immunis (Rao and Riehm, 1993), and Orconectes limosus (DeKleijn et al., 1993). [Leu8, Ile11]-ß-PDH is the major PDH in the shrimp Penaeus aztecus (Phillips et al., 1988), and an identical peptide is found in Penaeus vannamei (identified by cDNA cloning; Desmoucelles-Carette et al., 1996).
The identification of multiple forms of PDH within an individual species has been accomplished by sequencing of purified peptides, as in Pandalus jordani (Rao et al., 1989) and Penaeus japonicus (Yang et al., 1999), or by molecular cloning as done in Callinectes sapidus (Klein et al., 1994) and Penaeus vannamei (Desmoucelles-Carette et al., 1996). In Penaeus vannamei, two of the sequenced clones (PDH I and II) coded for an identical peptide [Leu8, Ile11]-ß-PDH, whereas the third (partially sequenced clone) contained [Leu8]-ß-PDH. In Callinectes sapidus, besides the known ß-PDH, a related peptide with six residue substitutions (including unique Ser12 and Ala13 residues) has been identified by molecular cloning. In Penaeus japonicus two peptides related to ß-PDH, [Leu8, Ile11, Thr16]-ß-PDH and [Phe14, Ile16]-ß-PDH, have been isolated from sinus glands, and both peptides could be identified in extracts of sinus glands from a single animal. Whereas the multiple forms identified in the above species are all related to ß-PDH, the peptides isolated and characterized from Pandalus jordani (Rao et al., 1989) include: [Leu8, Thr16]-ß-PDH, -PDH, and [Lys13, Ala16, Asp17]--PDH. Recently, [Lys13, Ala16]--PDH has been identified from Macrobrachium rosenbergii by cDNA sequencing (U. Lechleitner, J. M. Klein, D. Böcking, R. Keller, and K. R. Rao, unpublished).
Thus ß-PDH or octadecapeptides very similar to ß-PDH are more widely distributed among crustaceans, than are -PDH and its analogues (found thus far in species of Pandalus and Macrobrachium). The PDH from the isopod Armadillidium vulgare (Fig. 1) has the same net charge as -PDH, but shows closer relationship to ß-PDH and insect PDFs, including the presence of Glu3 found in all peptides related to ß-PDH (Rao and Riehm, 1993).
PDH/PDF family of peptides
Insect head extracts can elicit pigment dispersion in crustacean chromatophores. Work in our laboratory led to the identification of primary structures of octadecapeptide pigment-dispersing factors (PDFs) from four insect species: Romalea microptera (Rao et al., 1987), Acheta domesticus (Rao and Riehm, 1988b, 1989), Periplaneta americana (Mohrherr et al., 1991), and Carausius morosus (Mohrherr et al., 1994). Recently the PDF of Drosophila melanogaster has been identified by means of molecular cloning (Park and Hall, 1998). As can be seen from Figure 2, the insect PDFs are closely related to crustacean ß-PDH.
The crustacean PDHs and insect PDFs are members of the PDH/PDF peptide family and share the following features: conserved chain length (18 residues); conserved termini (N-terminal Asn, C-terminal Ala-NH2); and other conserved residues (Ser2, Ile5, Asn6, Ser7, and Leu9). Residue substitutions at several positions are conservative: Met, Leu, or Ile at position 4; Ile or Leu at position 8; Met or Leu at position 15. Except for some unique substitutions such as Ala11 and Asn17 (Armadillidium), Ser10 and Asn14 (Drosophila), Phe14 and Ile16 (Penaeus japonicus PDH II), Ser12 and Ala13 (Callinectes PDH II), the ß-PDH and related peptides show a very high degree of sequence similarity (Fig. 2).
-PDHs of an identical structure occur in two species of Pandalus. Except for the unique Ala16 substitution in the two variants of -PDH, the peptides in this group also show substantial sequence similarity, accompanied by conservative substitutions at positions 13 (Arg or Lys) and 17 (Glu or Asp).
The amino acid substitutions observed at positions 4, 8, 10, 12, 15, and 17 in PDH/PDF peptides can arise from single point mutations in the relevant codons. Several other substitutions—Leu11 for Ile11; Arg13 for Lys13; Leu14 or Phe14 for Val14; Ala16 for Thr16; Thr16 or Ile16 for Asn16—also require only single point mutations. Although knowledge of the codon usage in PDH/PDF genes is derived from a few species, phylogenetic relationships among the peptides can be predicted by analyzing amino acid sequences using the parsimony principle (review: Felsenstein, 1988).
In applying the Protein Parsimony algorithm for PDH/PDF peptides, the sequence of ß-PDH is used to root the tree (Fig. 3). The computer program (PROTPARS) finds that there are 50 equally parsimonious trees that can explain the relationships of the PDH/PDF peptides. A total of 27 amino acid substitutions are required to construct each of the trees. Relatively minor differences are evident among the trees, but the basic outcomes are represented by the tree in Figure 3. The peptides emerge as two groups, one of which begins with the substitution of Glu17 for Asp17, and the other with the substitution of Leu8 for Ile8. The former substitution alone results in Procambarus PDH ([Glu17]-ß-PDH), with additional changes at other positions leading to the derivation of -PDH and -PDH analogues found in Pandalus and Macrobrachium—all of which are clustered in one group.
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The substitution of Leu8 for Ile8 generates Penaeus vannamei PDH-III. Additional amino acid substitutions at other positions lead to the formation of all other ß-PDH analogues, including insect PDFs. The interrelated insect PDFs appear in a subgroup, although Drosophila PDF (due to unique residues: Ser10, Asn14) follows a separate path. Owing to structural similarities (including the presence of Leu15), PDH of the isopod crustacean Armadillidium is included with the insect PDF group. Most of the other ß-PDH analogues from crustaceans are assembled as a separate subgroup. One of the peptides (Callinectes PDH II, which contains Glu17), however, appeared in the
-PDH group in some of the PROTPARS-generated phylogenetic trees (not shown here). Regardless of its placement in the tree, six substitutions (four in a single step) are needed to derive Callinectes PDH-II from ß-PDH. Additional structural intermediates are likely to be present along the pathways in the formation of peptides such as Callinectes PDH-II, -PDH, -PDH analogues, and Armadillidium PDH. It is necessary to identify additional PDH/PDF peptides from diverse arthropods.
A possible phyletic scheme for decapod crustaceans suggests that penaeids evolved as one of three independent stocks, apart from an ancestral stock represented by Palaeopalaemon that has characters of both astacidean and palinuran pleocyemates (Schram, 1982). The occurrence of ß-PDH and [Glu17]-ß-PDH in astacideans, the presence of highly homologous PDHs (83 to 94% residue identity with ß-PDH) in penaeid shrimp, and the identification of closely related PDFs (78 to 89% residue identity with ß-PDH) in representatives of evolutionarily divergent, phasmid, orthopteran, and dipteran insects suggest that ß-PDH is an ancient molecule from which the PDHs and PDFs evolved as a highly conserved family of neuropeptides.
Precursors of PDH and PDF
The PDH precursors have been identified by cDNA sequencing in several crustacean species: Carcinus maenas (Klein et al., 1992), Orconectes limosus (DeKleijn et al., 1993), Callinectes sapidus (Klein et al., 1994), and Penaeus vannamei (Desmoucelles-Carette et al., 1996). The structure of insect PDF precursors has been determined by cDNA sequencing in Romalea microptera (Davis et al., 1996) and by the sequencing of both the genomic DNA and cDNA in Drosophila melanogaster (Park and Hall, 1998). The PDF-encoding Drosophila gene (pdf) is intronless, present in a single copy of haploid genome, and located on the 97B region of the third chromosome (Park and Hall, 1998).
The PDH and PDF precursors share the following general organization and contain: a signal peptide, a precursor-related peptide, a cleavage site, the peptide PDH or PDF, and a glycine residue, followed by one or two basic amino acid residues. Except for the expected similarity in the PDH/PDF encoding region, the signal peptides and precursor-related peptides in crustacean PDH precursors are divergent from the corresponding components in the insect PDF precursors (Fig. 4). Whereas PDH signal peptides contain 20 to 23 amino acids, the PDF signal peptides contain 22 (Romalea) or 16 (Drosophila) residues and show little or no similarity to the former. The PDH precursor-related peptides (PPRP), which contain 33 or 34 amino acids, are shorter than the corresponding peptides in PDF precursors with 44 (Romalea) or 63 residues (Drosophila), and are distinct from the latter. The proteolytic processing site preceding the mature peptides (PDH or PDF) contains paired basic residues in the precursors in crustaceans and Romalea, but three basic residues occur at this site in Drosophila PDF precursor. The -amidation signal consists of glycine followed by two basic residues in the precursors in crustaceans and Romalea, but this region in Drosophila contains glycine followed by a single basic residue.
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Although the signal peptide and precursor-related peptides in crustacean PDH precursors are highly diverged from those of the insect PDF precursors, there is considerable similarity in these peptides among the crustacean species (Fig. 4). Interestingly, the PPRPs (also called PAP, precursor-associates peptides) in PDF precursors share little similarity among them (Drosophila and Romalea), the divergence presumably linked to their derivation from the distantly related dipteran and orthopteran species. The significance of these noted differences remains unclear, because the functions of PPRPs (PAPs) are unknown.
Functions of PDH in crustaceans
As reviewed earlier (Rao, 1985; Rao and Riehm, 1993), -PDH and ß-PDH are each able to induce light-adaptive movement of screening pigment in distal eye pigment cells and pigment dispersion in all types of chromatophores in crustaceans such as Palaemon, Uca, and Procambarus. In these tests, screening pigment migration in the eye has been determined by measuring the distance of movement of the distal eye pigment in live animals, and it remains unknown whether the PDHs effect movements of reflecting eye pigment in Palaemon and Uca. The reflecting pigment in the eye of Procambarus remains stationary during light- and dark-adaptation, and is not expected to be affected by hormones. In Palaemonetes pugio, histological examination shows that PDH induces light-adaptational movement of both distal and reflecting pigments (Rao et al., 1983). Further studies are needed, including ultrastructural examinations (as done in the housefly: Pyza and Meinertzhagen, 1998), to determine whether PDHs have any effect on the translocation of screening pigment granules (proximal pigment) in crustacean photoreceptor cells and terminals.
The significance of the presence of multiple forms of PDH in certain species and how such hormones (with apparently similar actions) are utilized to achieve complex pigmentary changes are not understood. In various cases, however, the identified multiple octadecapeptide PDHs differ in their relative potency. Among the two PDHs identified (and presumably released) from the sinus glands of Penaeus japonicus, PDH II is about 5, 7, and 10-fold more potent than PDH I in inducing dispersion in erythrophores, xanthophores, and melanophores, respectively. Both peptides are equipotent, but relatively weak in stimulating the leucophores (Yang et al., 1999). The higher potency of PDH II on the former chromatophores is thought to result from the substitution of a nonpolar residue (Ile) at position 16 in PDH II of Penaeus japonicus. The PDH II identified by molecular cloning in Callinectes sapidus is 400-fold less potent than PDH I (ß-PDH), due to interactive effects of multiple substitutions in the former peptide, especially Ser12 for Pro12 and Ala13 for Lys13, and also Glu17 for Asp17 (Klein et al., 1994). Although in situ hybridization studies show the expression of mRNAs of both peptides, either separately or colocalized, in a number of PDH-immunoreactive cells in the optic ganglia (Jaenecke et al., 1995), only ß-PDH could be purified from the sinus glands of Callinectes (Mohrherr et al., 1990). This indicates that Callinectes PDH II is unlikely to serve as a humoral regulator of pigmentary effectors, and the possibility that it may serve neuromodulatory or neurotransmitter functions merits exploration—as suggested by the earlier findings of extensive PDH-immunoreactive tracts in the crustacean eyestalk that do not project into the sinus glands (Mangerich et al., 1987). The three forms of PDH from Pandalus jordani have not been tested on this species to determine their relative potency, but in tests for melanophore pigment dispersion in Uca they show a 20-fold difference in potency—with [Leu8, Thr16 ]-ß-PDH being the most potent (as potent as ß-PDH) and -PDH being the least potent, the decreased potency of the latter being attributable to the presence of residues such as Gly3, Met4, and Glu17, and due to interactive effects of multiple substitutions (Rao and Riehm, 1993).
The cross-reactivity of PDHs among crustaceans has been affirmed by tests with synthetic peptides, and these studies also show that the structural requirements for PDH potency varies with the target cell type within a given species, as well as with the species tested. Thus, ß-PDH is 5, 6, and 8-fold more potent than [Glu17]-ß-PDH (Procambarus PDH) in causing pigment dispersion in Uca leucophores, erythrophores, and melanophores, respectively. [Glu17]-ß-PDH is 4-fold more potent than ß-PDH in causing erythrophore pigment dispersion in Procambarus, although these two peptides display less pronounced differences in potency in effecting leucophore pigment dispersion and light-adaptational distal eye pigment movement in Procambarus (McCallum et al., 1991).
Because of their structural relationship to ß-PDH, insect PDFs are able to trigger pigment dispersion in crustacean chromatophores. Among the four PDFs tested for melanophore pigment dispersion in Uca, Periplaneta PDF is twice as potent as ß-PDH (Rao and Riehm, 1993) whereas Carausius PDF is the least potent (4-fold less potent than ß-PDH; Mohrherr et al., 1994). Based on prior structure-activity studies with synthetic PDH analogues (see Rao and Riehm, 1988a, 1991, 1993), the higher potency of Periplaneta PDF is due to the substitution of Leu15 for Met15 which, along with Leu4, imparts full protection from oxidation. The low potency of Carausius PDF is attributable to the substitution of Ala10 for Gly10, as this is the only difference between the PDFs of Periplaneta and Carausius (Fig. 2). Drosophila PDF has not been tested on Uca, but it is likely to elicit melanophore pigment dispersion since Phormia PDF—with a deduced partial sequence of NSELINSLLSL (C. T. Lundquist, C. J. Mohrherr, D. R. Nässel, and K. R. Rao, unpublished), identical to residues 1–11 in Drosophila PDF—is active on Uca melanophores (Nässel et al., 1993).
Functions of PDF in insects
PDF has been shown to play an important role in the regulation of biological rhythms in insects. Immunocytochemical studies, using an antiserum against ß-PDH (Dircksen et al., 1987), revealed three groups of PDH-immunoreactive (PDH-ir) neurons in the optic lobe of orthopteran insects (Zahnow et al., 1987; Homberg et al., 1991), of which one group of cells (PDH Me) located at the anterior edge of the medulla fulfilled the morphological criteria predicted for pacemakers (Homberg et al., 1991). These PDH-ir neurons and their projections in the accessory medulla (AMe) are recognized as components of the optic lobe pacemaker of the insect circadian system (review: Helfrich-Förster et al., 1998). Lesion and transplantation studies have shown that the presence of AMe, with its associated PDH-ir neurons, is necessary and sufficient for the expression of the circadian locomotor activity rhythm in the cockroach Leucophaea maderae. Injection of synthetic PDF, an Arg13-substituted analogue of Acheta PDF, into the AMe region caused phase delays of locomotor activity (Petri and Stengl, 1997). These and other studies in Leucophaea suggest that the bilaterally symmetric accessory medulla receives photic input indirectly from the compound eyes and controls rhythmic activities through PDH-ir outputs to different areas: the contralateral clock, optic lobe neuropils, and other targets in the central brain (Helfrich-Förster et al., 1998).
In Drosophila melanogaster, PDH-ir neurons located at the anterior base of the medulla (Nässel et al., 1991) and showing colocalization of PDH- and PER-immunoreactivity (Helfrich-Förster, 1995) have been proposed to be the circadian pacemaker. PER is the protein product of the first well defined clock gene period in Drosophila (reviews: Hall, 1995; Young, 1998). The PDH-ir neurons (which comprise most of the LNv neurons, ventral lateral neurons located between the medulla and lateral cerebrum) also show colocalization of ß-PDH antigens with those detected by a new antibody to distinct sequences of precursor-associated peptide of Drosophila ProPDF (Renn et al., 1999; Park and Hall, 1998). The connection of these PDH/PDF-ir neurons to the circadian system is indicated by the absence of these cells in behaviorally arrhythmic disconnected (disco) mutants (Helfrich-Förster, 1998). In animals mutant for the pdf gene and in those subjected to selective ablation of PDF-ir neurons, the observed locomotor activity was largely arrhythmic although a minority of each pdf variant displayed weak to moderate free-running rhythmicity (Renn et al., 1999), confirming the principal pacemaker role for LNvs and implicating PDF as the principal transmitter of circadian signal in Drosophila. Misexpression of the pdf gene from Romalea in the central nervous system of Drosophila led to severe alterations in the activity and eclosion rhythms, especially when ectopic pdf expression is in neurons that projected into the dorsal central brain, indicating that PDF acts a neuromodulator in the rhythmic control of behavior (Helfrich-Förster et al., 2000).
It has been known that transcription factors dCLOCK and CYCLE are required for oscillations in the expression of Drosophila clock genes period and timeless (see Hall, 1995; Young, 1998). An additional clock control gene vrille (vri) is shown to be expressed in circadian pacemaker cells in larval and adult brains of Drosophila, with vri RNA levels oscillating with a circadian rhythm under the control of dCLOCK and CYCLE (Blau and Young, 1999). Cycling vri is required for a functional Drosophila clock, since continuous vri activity suppresses period and timeless expression and causes long-period behavioral rhythms and arrhythmia. Continuous expression of vri also suppresses PDF accumulation, indicating that vri additionally connects the clock to behavior. Other evidence from the transformed flies indicates that dCLOCK and VRI independently regulate levels of PDF—the former affecting accumulation of pdf RNA, and VRI affecting PDF accumulation presumably by specifying rhythmic expression of a factor involved in translation, maturation, transport, or release of PDF (Blau and Young, 1999).
PDF has also been implicated in the regulation of circadian structural changes in the visual system of the housefly Musca domestica (review: Meinertzhagen and Pyza, 1999). Immunoreactive varicosities of PDH-ir neurons exhibit size changes attributable to their cyclic release of PDF, or to its cyclical synthesis, transport, or both. Injections of Periplaneta PDF into Musca caused an increase in the girth of lamina axons of L1 and L2 (monopolar interneurons) and a decrease in the number of screening pigment granules in the terminals of R1–R6, presumably due to migration out of the terminals into the overlying photoreceptor cells (Pyza and Meinertzhagen, 1998), mimicking changes that are seen both during the day of a day/night cycle and the subjective day of constant darkness. These results suggest that PDF serves as a transmitter in the fly's circadian system.
Whereas PDF effected screening pigment migration in housefly photoreceptor terminals, PDH has not been shown to cause pigment movements in crustacean photoreceptor cells—the observed actions in the latter being limited to pigment cells in the eye and studied only at the light-microscopy level. In many insects ommatidial pigment cells also show screening pigment translocations (Stavenga, 1979), but the effect of PDF on these cells is unknown. Similarly, it remains to be determined whether PDF influences rapid color changes brought about by melanophores in Corethra and epidermal cells in Carausius (see Fingerman, 1963; Rao et al., 1991).
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PERSPECTIVES |
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SYNOPSISINTRODUCTIONPIGMENT-CONCENTRATING HORMONESPIGMENT-DISPERSING HORMONESPERSPECTIVESReferences |
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The fast and impressive progress in elucidating the function of PDF at molecular and genetic levels in insects should revitalize studies on the regulation of rhythmic phenomena in crustaceans. Persistent rhythms of integumental color change, eye pigment migration, and retinal sensitivity are displayed by many decapod Crustacea, and such rhythms are thought to be effected by pigmentary-effector hormones serving as clock output signals, although some of the effector cells (photoreceptor cells) may show hormone-independent oscillations. The cellular characteristics of the pacemakers and the clock control mechanisms are practically unknown in Crustacea, although it has been proposed that circadian rhythms of retinal sensitivity are controlled by a complex mechanism involving two pairs of entraining photoreceptors (retinal and extraretinal) and three pairs of oscillators (retinular cells in the two eyes; neurosecretory systems in the two eyestalks; and a pair of brain centers, located near the midline). The brain and its neuronal input to the optic lobe appear to be required for bilateral light-adaptation following unilateral retinal stimulation, as well as for synchronizing the rhythmic activities of the two eyes (reviews: Larimer and Smith, 1980
; Rao, 1985), akin to the required coupling for the synchronization of bilateral pacemakers in cockroaches (Helfrich-Förster et al., 1998).
Although much progress has been made in the characterization of crustacean pigmentary-effector hormones, the total number of hormones found in any given species and the mechanisms by which they bring about complex pigmentary changes require further study. Since RPCH and PDH act not only as hormones (released through neurohemal organs), but also as neuromodulators, their regulatory contributions would be diverse and integrative. The presence of RPCH- and PDH-ir fibers in the lamina region of the eyes (see Mangerich et al., 1987; Rodríguez-Sosa et al., 1994) point to their candidacy for influencing the visual system, and modulating visually-triggered neuronal and neuroendocrine processes.
The AKH/RPCH and PDH/PDF peptides are clearly members of peptide families common to crustaceans and insects, serving different functions in each group. Substances related to these peptide families may also occur in mollusks (Greenberg et al., 1985; Elekes and Nässel, 1999), and PDH-ir cells have also been found in the pituitary of dogfish (Vallarino et al., 1991). In addition to the available probes (e.g., antibodies to characterized peptides), knowledge of the receptors for AKH/RPCH and PDH/PDF peptides would facilitate further studies on the distribution, evolution, and functions of these molecules.
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ACKNOWLEDGMENTS |
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I thank Milton Fingerman for providing me a postdoctoral research opportunity during the early part of my career (1966–1972) and for his sustained encouragement and support of my endeavors. I am grateful to the many students, research associates, and senior colleagues for their contributions and collaboration over the years. I am especially thankful to John Riehm, a friend and colleague at UWF, for being a productive partner in pigmentary-effector research until his death in November 1999. My work has been supported by a University Research Professorship at UWF and by grants from the National Science Foundation. I thank Ms. Tanya Streeter for assistance in preparing the manuscript.
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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, at Atlanta, Georgia.
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