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The ever-expanding neuropeptide gene families in the nematode Caenorhabditis elegans

Published online by Cambridge University Press:  29 March 2006

C. LI
C. LI
Affiliation:
Department of Biology, City College of the City University of New York, Convent Avenue at 138th Street, New York, NY, 10031, USA
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Abstract

Neuropeptides act as chemical signals in the nervous system to modulate behaviour. With the ongoing EST projects and DNA sequence determination of different genomes, the identification of neuropeptide genes has been made easier. Despite the relatively ‘simple’ repertoire of behaviours in the nematode Caenorhabditis elegans, this worm contains a surprisingly large and diverse set of neuropeptide genes. At least 109 genes encoding over 250 potential neuropeptides have been identified in C. elegans; all genes are likely to be expressed and many, if not all, of the predicted peptides are produced. The predicted peptides include: 38 insulin-like peptides, several of which are involved in development and reproductive growth, and over 70 FMRFamide-related peptides, some of which are involved in locomotion, reproduction, and social behaviour. Many of the C. elegans peptides are identical or highly similar to those isolated or predicted in parasitic nematodes, such as Ascaris suum, Haemonchus contortus, Ancylostoma caninum, Heterodera glycines and Meloidogyne arenaria, suggesting that the function of these peptides is similar across species. The challenge for the future is to determine the function of all the genes and individual peptides and to identify the receptors through which the peptides signal.

Keywords

Neuropeptidesgene familiesinsulinFMRFamideflpnlp
Type
Research Article
Information
Parasitology , Volume 131 , Supplement S1: Parasite neuromusculature and its utility as a drug target , October 2005 , pp. S109 - S127
Copyright
2005 Cambridge University Press

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References

REFERENCES

BARGMANN, C. I. ( 1998). Neurobiology of the Caenorhabditis elegans genome. Science 282, 2028–2033.CrossRefGoogle Scholar
BARGMANN, C. I. & HORVITZ, H. R. ( 1991). Control of larval development by chemosensory neurons in Caenorhabditis elegans. Science 251, 1243–1246.CrossRefGoogle Scholar
BONINI, J. A., JONES, K. A., ADHAM, N., FORRAY, C., ARTYMYSHYN, R., DURKIN, M. M., SMITH, K. E., TAMM, J. A., BOTEJU, L. W., LAKHLANI, P. P., RADDATZ, R., YAO, W. J., OGOZALEK, K. L., BOYLE, N., KOURANOVA, E. V., QUAN, Y., VAYSSE, P. J., WETZEL, J. M., BRANCHEK, T. A., GERALD, C. & BOROWSKY, B. ( 2000). Identification and characterization of two G protein-coupled receptors for neuropeptide FF. Journal of Biological Chemistry 275, 39324–39331.CrossRefGoogle Scholar
BOWMAN, J. W., FRIEDMAN, A. R., THOMPSON, D. P., ICHHPURANI, A. K., KELLMAN, M. F., MARKS, N. J., MAULE, A. G. & GEARY, T. G. ( 1996). Structure-activity relationships of KNEFIRFamide (AF1), a nematode FMRFamide-related peptide, on Ascaris suum muscle. Peptides 17, 381–387.CrossRefGoogle Scholar
BOWMAN, J. W., FRIEDMAN, A. R., THOMPSON, D. P., MAULE, A. G., ALEXANDER-BOWMAN, S. J. & GEARY, T. G. ( 2002). Structure-activity relationships of an inhibitory nematode FMRFamide-related peptide, SDPNFLRFamide (PF1), on Ascaris suum muscle. International Journal for Parasitology 32, 1765–1771.CrossRefGoogle Scholar
BROWNLEE, D. J., FAIRWEATHER, I., HOLDEN-DYE, L. & WALKER, R. J. ( 1996). Nematode neuropeptides: Localization, isolation and functions. Parasitology Today 12, 343–351.CrossRefGoogle Scholar
BROWNLEE, D. J., HOLDEN-DYE, L., FAIRWEATHER, I. & WALKER, R. J. ( 1995). The action of serotonin and the nematode neuropeptide KSAYMRFamide on the pharyngeal muscle of the parasitic nematode, Ascaris suum. Parasitology 111, 379–384.CrossRefGoogle Scholar
BROWNLEE, D., HOLDEN-DYE, L. & WALKER, R. ( 2000). The range and biological activity of FMRFamide-related peptides and classical neurotransmitters in nematodes. Advances in Parasitology 45, 109–180.CrossRefGoogle Scholar
BROWNLEE, D. J. & WALKER, R. J. ( 1999). Actions of nematode FMRFamide-related peptides on the pharyngeal muscle of the parasitic nematode, Ascaris suum. Annals of the New York Academy of Sciences 897, 228–238.CrossRefGoogle Scholar
C. ELEGANS SEQUENCING CONSORTIUM ( 1998). Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282, 2012–2018.
CASSADA, R. C. & RUSSELL, R. L. ( 1975). The dauer larva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Developmental Biology 46, 326–342.CrossRefGoogle Scholar
CAZZAMALI, G. & GRIMMELIKHUIJZEN, C. J. ( 2002). Molecular cloning and functional expression of the first insect FMRFamide receptor. Proceedings of the National Academy of Sciences, USA 99, 12073–12078.CrossRefGoogle Scholar
CHEUNG, B. H. H., ARELLANO-carbajal, F., RYBICKI, I. & DE bono, M. ( 2004). Soluble guanylate cyclases act in neurons exposed to the body fluid to promote C. elegans aggregation behaviour. Current Biology 14, 1105–1111.Google Scholar
COUILLAULT, C., PUJOL, N., REBOUL, J., SABATIER, L., GUICHOU, J.-F., KOHARA, Y. & EWBANK, J. J. ( 2004). TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nature Immunology 5, 488–494.CrossRefGoogle Scholar
COWDEN, C. & STRETTON, A. O. ( 1993). AF2, an Ascaris neuropeptide: isolation, sequence, and bioactivity. Peptides 14, 423–430.CrossRefGoogle Scholar
COWDEN, C. & STRETTON, A. O. ( 1995). Eight novel FMRFamide-like neuropeptides isolated from the nematode Ascaris suum. Peptides 16, 491–500.CrossRefGoogle Scholar
COWDEN, C., STRETTON, A. O. & DAVIS, R. E. ( 1989). AF1, a sequenced bioactive neuropeptide isolated from the nematode Ascaris suum. Neuron 2, 1465–1473.CrossRefGoogle Scholar
DAVIES, A. G., BETTINGER, J. C., THIELE, T. R., JUDY, M. E. & MCINTIRE, S. L. ( 2004). Natural variation in the npr-1 gene modifies ethanol responses of wild strains of C. elegans. Neuron 42, 731–743.CrossRefGoogle Scholar
DAVIS, R. E. & STRETTON, A. O. ( 2001). Structure-activity relationships of 18 endogenous neuropeptides on the motor nervous system of the nematode Ascaris suum. Peptides 22, 7–23.CrossRefGoogle Scholar
DE BONO, M. & BARGMANN, C. I. ( 1998). Natural variation in a neuropeptide Y receptor homolog modifies social behaviour and food response in C. elegans. Cell 94, 679–689.CrossRefGoogle Scholar
DLAKIC, M. ( 2002). A new family of putative insulin receptor-like proteins in C. elegans. Current Biology 12, R155–R157.CrossRefGoogle Scholar
DOCKRAY, G. J. ( 2004). The expanding family of –RFamide peptides and their effects on feeding behaviour. Experimental Physiology 89, 229–235.CrossRefGoogle Scholar
DURET, L., GUEX, N., PEITSCH, M. C. & BAIROCH, A. ( 1998). New insulin-like proteins with atypical disulfide bond pattern characterized in Caenorhabditis elegans by comparative sequence analysis and homology modeling. Genome Research 8, 348–353.CrossRefGoogle Scholar
DUTTLINGER, A., MISPELON, M. & NICHOLS, R. ( 2003). The structure of the FMRFamide receptor and activity of the cardioexcitatory neuropeptide are conserved in mosquito. Neuropeptides 37, 120–126.CrossRefGoogle Scholar
EIPPER, B. A., MILGRAM, S. L., HUSTEN, E. J., YUN, H. Y. & MAINS, R. E. ( 1993). Peptidylglycine alpha-amidating monooxygenase: a multifunctional protein with catalytic, processing, and routing domains. Protein Science 2, 489–497.Google Scholar
FELLOWES, R. A., MAULE, A. G., MARKS, N. J., GEARY, T. G., THOMPSON, D. P., SHAW, C. & HALTON, D. W. ( 1998). Modulation of the motility of the vagina vera of Ascaris suum in vitro by FMRF amide-related peptides. Parasitology 116, 277–287.CrossRefGoogle Scholar
GEARY, T. G., PRICE, D. A., BOWMAN, J. W., WINTERROWD, C. A., MACKENZIE, C. D., GARRISON, R. D., WILLIAMS, J. F. & FRIEDMAN, A. R. ( 1992). Two FMRFamide-like peptides from the free-living nematode Panagrellus redivivus. Peptides 13, 209–214.CrossRefGoogle Scholar
GRAY, J. M., KAROW, D. S., LU, H., CHANG, A. J., CHANG, J. S., ELLIS, R. E., MARIETTA, M. A. & BARGMANN, C. I. ( 2004). Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430, 317–322.CrossRefGoogle Scholar
GREGOIRE, F. M., CHOMIKI, N., KACHINSKAS, D. & WARDEN, C. H. ( 1998). Cloning and developmental regulation of a novel member of the insulin-like gene family in Caenorhabditis elegans. Biochemical and Biophysical Research Communications 249, 385–390.CrossRefGoogle Scholar
HAN, M., PARK, D., VANDERZALM, P. J., MAINS, R. E., EIPPER, B. A. & TAGHERT, P. H. ( 2004). Drosophila uses two distinct neuropeptide amidating enzymes, dPAL1 and dPAL2. Journal of Neurochemistry 90, 129–141.CrossRefGoogle Scholar
HOLDEN-DYE, L., FRANKS, C. J., WILLIAMS, R. G. & WALKER, R. J. ( 1995). The effect of the nematode peptides SDPNFLRFamide (PF1) and SADPNFLRFamide (PF2) on synaptic transmission in the parasitic nematode Ascaris suum. Parasitology 110, 449–455.CrossRefGoogle Scholar
HUSSON, S. J., CLYNEN, E., BAGGERMAN, G., DE loof, A. & SCHOOFS, L. ( 2005) Discovering neuropeptides in Caenorhabditis elegans by two dimensional liquid chromatography and mass spectrometry. Biochemical and Biophysical Research Communications 335, 76–86.CrossRefGoogle Scholar
JACOB, T. C. & KAPLAN, J. M. ( 2003). The EGL-21 carboxypeptidase E facilitates acetylcholine release at Caenorhabditis elegans neuromuscular junctions. Journal of Neuroscience 23, 2122–2130.Google Scholar
KASS, J., JACOB, T. C., KIM, P. & KAPLAN, J. M. ( 2001). The EGL-3 proprotein convertase regulates mechanosensory responses of Caenorhabditis elegans. Journal of Neuroscience 21, 9265–9272.Google Scholar
KAWANO, T., ITO, Y., ISHIGURO, M., TAKUWA, K., NAKAJIMA, T. & KIMURA, Y. ( 2000). Molecular cloning and characterization of a new insulin/IGF-like peptide of the nematode Caenorhabditis elegans. Biochemical and Biophysical Research Communications 273, 431–436.CrossRefGoogle Scholar
KEATING, C. D., HOLDEN-dye, L., THORNDYKE, M. C., WILLIAMS, R. G., MALLETT, A. & WALKER, R. J. ( 1995). The FMRFamide-like neuropeptide AF2 is present in the parasitic nematode Haemonchus contortus. Parasitology 111, 515–521.CrossRefGoogle Scholar
KEATING, C. D., KRIEK, N., DANIELS, M., ASHCROFT, N. R., HOPPER, N. A., SINEY, EL. J., HOLDEN-DYE, L. & BURKE, J. F. ( 2003). Whole-genome analysis of 60 G protein-coupled receptors in Caenorhabditis elegans by gene knockout with RNAi. Current Biology 13, 1715–1720.CrossRefGoogle Scholar
KENYON, C., CHANG, J., GENSCH, E., RUDNER, A. & TABTIANG, R. ( 1993). A C. elegans mutant that lives twice as long as wild type. Nature 366, 461–464.Google Scholar
KIM, K. & LI, C. ( 2004). Expression and regulation of an FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. Journal of Comparative Neurology 475, 540–550.CrossRefGoogle Scholar
KIMURA, K. D., TISSENBAUM, H. A., LIU, Y. & RUVKUN, G. ( 1997). daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277, 942–946.CrossRefGoogle Scholar
KUBIAK, T. M., LARSEN, M. J., NULF, S. C., ZANTELLO, M. R., BURTON, K. J., BOWMAN, J. W., MODRIC, T. & LOWERY, D. E. ( 2003 a). Differential activation of “social” and “solitary” variants of the Caenorhabditis elegans G protein-coupled receptor NPR-1 by its cognate ligand AF9. Journal of Biological Chemistry 278, 33724–33729.Google Scholar
KUBIAK, T. M., LARSEN, M. J., ZANTELLO, M. R., BOWMAN, J. W., NULF, S. C. & LOWERY, D. E. ( 2003 b). Functional annotation of the putative orphan Caenorhabditis elegans G-protein-coupled receptor C10C6.2 as a FLP15 peptide receptor. Journal of Biological Chemistry 278, 42115–42120.Google Scholar
LI, W., KENNEDY, S. G. & RUVKUN, G. ( 2003). daf-28 encodes a C. elegans insulin superfamily member that is regulated by environmental cues and acts in the DAF-2 signaling pathway. Genes and Development 17, 844–858.Google Scholar
LI, C., KIM, K. & NELSON, L. S. ( 1998). FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. Brain Research 848, 26–34.Google Scholar
LI, C., NELSON, L. S., KIM, K., NATHOO, A. & HART, A. C. ( 1999). Neuropeptide gene families in the nematode Caenorhabditis elegans. Annals of the New York Academy of Sciences 897, 239–252.CrossRefGoogle Scholar
LINGUEGLIA, E., CHAMPIGNY, G., LAZDUNSKI, M. & BARBRY, P. ( 1995). Cloning of the amiloride-sensitive FMRFamide peptide-gated sodium channel. Nature 378, 730–733.CrossRefGoogle Scholar
LOWERY, D. E., GEARY, T. G., KUBIAK, T. M. & LARSEN, M. J. ( 2003). Pharmacia & Upjohn Company, G protein-coupled receptor-like receptors and modulators thereof, United States, Patent 6,632,621.
MALONE, E. A. & THOMAS, J. H. ( 1994). A screen for nonconditional dauer-constitutive mutations in Caenorhabditis elegans. Genetics 136, 879–886.Google Scholar
MARKS, N. J., MAULE, A. G., GEARY, T. G., THOMPSON, D. P., DAVIS, J. P., HALTON, D. W., VERHAERT, P. & SHAW, C. ( 1997). APEASPFIRFamide, a novel FMRFamide-related decapeptide from Caenorhabditis elegans: structure and myoactivity. Biochemical and Biophysical Research Communications 231, 591–595.CrossRefGoogle Scholar
MARKS, N. J., MAULE, A. G., GEARY, T. G., THOMPSON, D. P., LI, C., HALTON, D. W. & SHAW, C. ( 1998). KSAYMRFamide (PF3/AF8) is present in the free-living nematode, Caenorhabditis elegans. Biochemical and Biophysical Research Communications 248, 422–425.CrossRefGoogle Scholar
MARKS, N. J., MAULE, A. G., LI, C., NELSON, L. S., THOMPSON, D. P., ALEXANDER-BOWMAN, S., GEARY, T. G., HALTON, D. W., VERHAERT, P. & SHAW, C. ( 1999 a). Isolation, pharmacology and gene organization of KPSFVRFamide: a neuropeptide from Caenorhabditis elegans. Biochemical and Biophysical Research Communications 254, 222–230.Google Scholar
MARKS, N. J., SANGSTER, N. C., MAULE, A. G., HALTON, D. W., THOMPSON, D. P., GEARY, T. G. & SHAW, C. ( 1999 b). Structural characterisation and pharmacology of KHEYLRFamide (AF2) and KSAYMRFamide (PF3/AF8) from Haemonchus contortus. Molecular and Biochemical Parasitology 100, 185–194.Google Scholar
MARKS, N. J., SHAW, C., HALTON, D. W., THOMPSON, D. P., GEARY, T. G., LI, C. & MAULE, A. G. ( 2001). Isolation and preliminary biological assessment of AADGAPLIRFamide and SVPGVLRFamide from Caenorhabditis elegans. Biochemical and Biophysical Research Communications 286, 1170–1176.CrossRefGoogle Scholar
MARKS, N. J., SHAW, C., MAULE, A. G., DAVIS, J. P., HALTON, D. W., VERHAERT, P., GEARY, T. G. & THOMPSON, D. P. ( 1995). Isolation of AF2 (KHEYLRFamide) from Caenorhabditis elegans: evidence for the presence of more than one FMRFamide-related peptide-encoding gene. Biochemical and Biophysical Research Communications 217, 845–851.CrossRefGoogle Scholar
MAULE, A. G., BOWMAN, J. W., THOMPSON, D. P., MARKS, N. J., FRIEDMAN, A. R. & GEARY, T. G. ( 1996). FMRFamide-related peptides (FaRPs) in nematodes: occurrence and neuromuscular physiology. Parasitology 113, S119–S135.CrossRefGoogle Scholar
MAULE, A. G., GEARY, T. G., BOWMAN, J. W., MARKS, N. J., BLAIR, K. L., HALTON, D. W., SHAW, C. & THOMPSON, D. P. ( 1995). Inhibitory effects of nematode FMRFamide-related peptides (FaRPs) on muscle strips from Ascaris suum. Invertebrate Neuroscience 1, 255–265.CrossRefGoogle Scholar
MAULE, A. G., SHAW, C., BOWMAN, J. W., HALTON, D. W., THOMPSON, D. P., GEARY, T. G. & THIM, L. ( 1994 a). KSAYMRFamide: a novel FMRFamide-related heptapeptide from the free-living nematode, Panagrellus redivivus, which is myoactive in the parasitic nematode, Ascaris suum. Biochemical and Biophysical Research Communications 200, 973–980.Google Scholar
MAULE, A. G., SHAW, C., BOWMAN, J. W., HALTON, D. W., THOMPSON, D. P., GEARY, T. G. & THIM, L. ( 1994 b). The FMRFamide-like neuropeptide AF2 (Ascaris suum) is present in the free-living nematode, Panagrellus redivivus (Nematoda, Rhabditida). Parasitology 109, 351–356.Google Scholar
McCULLOCH, D. & GEMS, D. ( 2003). Body size, insulin/IGF signaling and aging in the nematode Caenorhabditis elegans. Experimental Gerontology 38, 129–136.CrossRefGoogle Scholar
McVEIGH, P., LEECH, S., MAIR, G. R., MARKS, N. J., GEARY, T. G. & MAULE, A. G. ( 2005). Analysis of FMRFamide-like peptide (FLP) diversity in phylum Nematoda. International Journal for Parasitology 35, 1043–1060.CrossRefGoogle Scholar
MEEUSEN, T., MERTENS, I., CLYNEN, E., BAGGERMAN, G., NICHOLS, R., NACHMAN, R. J., HUYBRECHTS, R., DE LOOF, A. & SCHOOFS, L. ( 2002). Identification in Drosophila melanogaster of the invertebrate G protein-coupled FMRFamide receptor. Proceedings of the National Academy of Sciences, USA 99, 15363–15368.CrossRefGoogle Scholar
MERTENS, I., MEEUSEN, T., JANSSEN, T., NACHMAN, R. & SCHOOFS, L. ( 2005). Molecular characterization of two G protein-coupled receptor splice variants as FLP2 receptors in Caenorhabditis elegans. Biochemical and Biophysical Research Communications 330, 967–974.CrossRefGoogle Scholar
MERTENS, I., VANDINGENEN, A., MEEURSEN, T., JANSSEN, T., LUYTEN, W., NACHMAN, R. J., DE LOOF, A. & SCHOOFS, L. ( 2004). Functional characterization of the putative orphan neuropeptide G-protein coupled receptor C26F1.6 in Caenorhabditis elegans. FEBS Letters 573, 55–60.Google Scholar
MOFFETT, C. L., BECKETT, A. M., MOUSLEY, A., GEARY, T. G., MARKS, N. J., HALTON, D. W., THOMPSON, D. P. & MAULE, A. G. ( 2003). The ovijector of Ascaris suum: multiple response types revealed by Caenorhabditis elegans FMRFamide-related peptides. International Journal for Parasitology 33, 859–876.CrossRefGoogle Scholar
MORTON, D. B., HUDSON, M. L., WATERS, E. & O'SHEA, M. ( 1999). Soluble guanylyl cyclases in Caenorhabditis elegans: NO is not the answer. Current Biology 9, R546–R547.CrossRefGoogle Scholar
NATHOO, A. N., MOELLER, R. A., WESTLUND, B. A. & HART, A. C. ( 2001). Identification of neuropeptide-like protein gene families in Caenorhabditis elegans and other species. Proceedings of the National Academy of Sciences, USA 98, 14000–14005.CrossRefGoogle Scholar
NELSON, L., KIM, K., MEMMOTT, J. & LI, C. ( 1998). FMRFamide-related gene family in the nematode Caenorhabditis elegans. Molecular Brain Research 58, 103–111.CrossRefGoogle Scholar
NELSON, L. S., ROSOFF, M. L. & LI, C. ( 1998). Disruption of a neuropeptide gene, flp-1, causes multiple behavioural defects in Caenorhabditis elegans. Science 281, 1686–1690.CrossRefGoogle Scholar
PIERCE, S. B., COSTA, M., WISOTZKEY, R., DEVADHAR, S., HOMBURGER, S. A., BUCHMAN, A. R., FERGUSON, K. C., HELLER, J., PLATT, D. M., PASQUINELLI, A. A., LIU, L. X., DOBERSTEIN, S. K. & RUVKUN, G. ( 2001). Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes and Development 15, 672–678.Google Scholar
PRICE, D. A. & GREENBERG, M. J. ( 1977). Structure of a molluscan cardioexcitatory neuropeptide. Science 197, 670–671.CrossRefGoogle Scholar
RIDDLE, D. L. & ALBERT, P. S. ( 1997). Genetic and environmental regulation of dauer larva development. In C. elegans II ( eds Riddle, D. L., Blumenthal, T., Meyer, B. J. and J. R. Priess), Cold Spring Harbor Laboratory Press, New York, pp. 739–768.
ROGERS, C. M., FRANKS, C. J., WALKER, R. J., BURKE, J. F. & HOLDEN-DYE, L. ( 2001). Regulation of the pharynx of Caenorhabditis elegans by 5-HT, octopamine, and FMRFamide-like neuropeptides. Journal of Neurobiology 15, 235–244.CrossRefGoogle Scholar
ROGERS, C., REALE, V., KIM, K., CHATWIN, H., LI, C., EVANS, P. & DE BONO, M. ( 2003). Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nature Neuroscience 6, 1178–1185.CrossRefGoogle Scholar
ROSOFF, M. L., BURGLIN, T. R. & LI, C. ( 1992). Alternatively spliced transcripts of the flp-1 gene encode distinct FMRFamide-like peptides in Caenorhabditis elegans. Journal of Neuroscience 12, 2356–2361.CrossRefGoogle Scholar
ROSOFF, M. L., DOBLE, K. E., PRICE, D. A. & LI, C. ( 1993). The flp-1 propeptide is processed into multiple, highly similar FMRFamide-like peptides in Caenorhabditis elegans. Peptides 14, 331–338.CrossRefGoogle Scholar
ROUMY, M. & ZAJAC, J. M. ( 1998). Neuropeptide FF, pain and analgesia. European Journal of Pharmacology 345, 1–11.CrossRefGoogle Scholar
RUSSO, V. C., GLUCKMAN, P., FELDMAN, E. L. & WERTHER, G. A. ( 2005). The insulin-like growth factor system and its pleiotropic functions in brain. Endocrine Reviews, (in press).CrossRefGoogle Scholar
SCHINKMANN, K. & LI, C. ( 1992). Localization of FMRFamide-like peptides in Caenorhabditis elegans. Journal of Comparative Neurolology 316, 251–260.CrossRefGoogle Scholar
SIMMER, F., TIJSTERMAN, M., PARRISH, S., KOUSHIKA, S. P., NONET, M. L., FIRE, A., AHRINGER, J. & PLASTERK, R. H. ( 2002). Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Currrent Biology 12, 1317–1319.Google Scholar
STEINER, D. F. ( 1998). The proprotein convertases. Current Opinion in Chemical Biology 2, 31–39.CrossRefGoogle Scholar
STRETTON, A. O., FISHPOOL, R. M., SOUTHGATE, E., DONMOYER, J. E., WALROND, J. P., MOSES, J. E. & KASS, I. S. ( 1978). Structure and physiological activity of the motoneurons of the nematode Ascaris. Proceedings of the National Academy of Sciences, USA 75, 3493–3497.CrossRefGoogle Scholar
SULSTON, J. E. & HORVITZ, H. R. ( 1977). Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Developmental Biology 56, 110–156.CrossRefGoogle Scholar
SULSTON, J. E., SCHIERENBERG, E., WHITE, J. G. & THOMSON, J. N. ( 1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Developmental Biology 100, 64–119.CrossRefGoogle Scholar
TANG, J., YANG, H.-Y. & COSTA, E. ( 1984). Inhibition of spontaneous and opiate mediated nociception by an endogenous neuropeptide with Phe-Met-Arg-Phe-NH2 immunoreactivity. Proceedings of the National Academy of Sciences, USA 81, 5002–5005.CrossRefGoogle Scholar
TENSEN, C. P., COX, K. J., SMIT, A. B., VAN DER SCHORS, R. C., MEYERHOF, W., RICHTER, D., PLANTA, R. J., HERMANN, P. M., VAN minnen, J., GERAERTS, W. P., KNOL, J. C., BURKE, J. F., VREUGDENHIL, E. & VAN heerikhuizen, H. ( 1998). The Lymnaea cardioexcitatory peptide (LyCEP) receptor: a G-protein-coupled receptor for a novel member of the RFamide neuropeptide family. Journal of Neuroscience 18, 9812–9821.Google Scholar
THACKER, C., PETERS, K., SRAYKO, M. & ROSE, A. M. ( 1995). The bli-4 locus of Caenorhabditis elegans encodes structurally distinct Kex2/Subtilisin-like endoproteases essential for early development and adult morphology. Genes and Development 9, 956–971.CrossRefGoogle Scholar
THACKER, C. & ROSE, A. M. ( 2000). A look at the Caenorhabditis elegans Kex2/Subtilisin-like proprotein convertase family. BioEssays 22, 545–553.3.0.CO;2-F>CrossRefGoogle Scholar
WAGGONER, L. E., HARDAKER, L. A., GOLIK, S. & SCHAFER, W. R. ( 2000). Effect of a neuropeptide gene on behavioural states in Caenorhabditis elegans egg-laying. Genetics 154, 1181–1192.Google Scholar
YEW, J. Y., KUTZ, K. K., DIKLER, S., MESSINGER, L., LI, L. & STRETTON, A. O. ( 2005). Mass spectrometric map of neuropeptide expression in Ascaris suum. Journal of Comparative Neurology 488, 396–413.CrossRefGoogle Scholar