The FMRFamide-like peptide family in nematodes

Frontiers in Endocrinology

Volumn 5, Issue JUN, 2014, Pages

  Peymen, Katleen ^a   Watteyne, Jan ^a   Frooninckx, Lotte ^a   Schoofs, Liliane ^a   Beets, Isabel ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

C. elegans; Feeding behavior; FMRFamide like peptides; G protein coupled receptor; Nematodes; Neuropeptide; Reproduction

Indexed keywords

G PROTEIN COUPLED RECEPTOR; NEUROPEPTIDE RECEPTOR; PHENYLALANYLMETHIONYLARGINYLPHENYLALANINAMIDE;

CAENORHABDITIS ELEGANS; EGG LAYING; ELECTROPHYSIOLOGY; FLP GENE; FORAGING; GENE; GENE EXPRESSION; GENETIC POLYMORPHISM; IMMUNOCHEMISTRY; LOCOMOTION; NEMATODE; NOCICEPTION; NONHUMAN; PHARYNGEAL MUSCLE; PHYSIOLOGY; REVIEW; SEXUAL BEHAVIOR;

EID: 84905399568     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2014.00090     Document Type: Review

References (174)

1. Maule AG, Mousley A, Marks NJ, Day TA, Thompson DP, Geary TG, et al. Neuropeptide signaling systems - potential drug targets for parasite and pest control. Curr Top Med Chem (2002) 2:733-58. doi: 10.2174/1568026023393697
2. McVeigh P, Geary TG, Marks NJ, Maule AG. The FLP-side of nematodes. Trends Parasitol (2006) 22:385-96. doi:10.1016/j.pt.2006.06.010
3. Price DA, Greenberg MJ. Structure of a molluscan cardioexcitatory neuropeptide. Science (1977) 197:670-1. doi:10.1126/science.877582
4. Dockray GJ. The expanding family of RFamide peptides and their effects on feeding behaviour. Exp Physiol (2004) 89:229-35. doi:10.1113/expphysiol.2004.027169
5. Walker R, Papaioannou S, Holden-Dye L. A review of FMRFamide- and RFamide-like peptides in metazoa. Invertebr Neurosci (2009) 9:111-53. doi:10.1007/s10158-010-0097-7
6. Krajniak KG. Invertebrate FMRFamide related peptides. Protein Pept Lett (2013) 20:647-70. doi:10.2174/0929866511320060005
7. Espinoza E, Carrigan M, Thomas S, Shaw G, Edison A. A statistical view of FMRFamide neuropeptide diversity. Mol Neurobiol (2000) 21:35-56. doi:10.1385/MN:21:1-2:035
8. Jékely G. Global view of the evolution and diversity of metazoan neuropeptide signaling. Proc Natl Acad Sci U S A (2013) 110:8702-7. doi:10.1073/pnas.1221833110
9. Salzet M, Bulet P, Wattez C, Malecha J. FMRFamide-related peptides in the sex segmental ganglia of the Pharyngobdellid leech Erpobdella octoculata. Eur J Biochem (1994) 221:269-75. doi:10.1111/j.1432-1033.1994.tb18738.x
10. Kriegsfeld LJ. Driving reproduction: RFamide peptides behind the wheel. Horm Behav (2006) 50:655-66. doi:10.1016/j.yhbeh.2006.06.004
11. Bechtold DA, Luckman SM. The role of RFamide peptides in feeding. J Endocrinol (2007) 192:3-15. doi:10.1677/JOE-06-0069
12. Stretton AOW, Cowden C, Sithigorngul P, Davis RE. Neuropeptides in the nematode Ascaris suum. Parasitology (1991) 102:S107-16. doi:10.1017/S0031182000073339
13. McVeigh P, Leech S, Mair GR, Marks NJ, Geary TG, Maule AG. Analysis of FMRFamide-like peptide (FLP) diversity in phylum Nematoda. Int J Parasitol (2005) 35:1043-60. doi:10.1016/j.ijpara.2005.05.010
14. Larsen MJ, Lancheros ER, Williams T, Lowery DE, Geary TG, Kubiak TM. Functional expression and characterization of the C. elegans G-protein-coupled FLP-2 Receptor (T19F4.1) in mammalian cells and yeast. Int J Parasitol Drugs drug Resist (2013) 3:1-7. doi:10.1016/j.ijpddr.2012.10.002
15. Rosoff ML, Burglin TR, Li C. Alternatively spliced transcripts of the flp-1 gene encode distinct FMRFamide-like peptides in Caenorhabditis elegans. J Neurosci (1992) 12:2356-61.
16. Edison AS, Messinger LA, Stretton AO. afp-1: a gene encoding multiple transcripts of a new class of FMRFamide-like neuropeptides in the nematode Ascaris suum. Peptides (1997) 18:929-35. doi:10.1016/S0196-9781(97)00047-8
17. Maule A, Geary T, Bowman J, Shaw C, Falton D, Thompson D. The pharmacology of nematode FMRFamide-related peptides. Parasitol Today (1996) 12:351-7. doi:10.1016/0169-4758(96)10051-X
18. Day TA, Maule AG. Parasitic peptides! The structure and function of neuropeptides in parasitic worms. Peptides (1999) 20:999-1019. doi:10.1016/S0196-9781(99)00093-5
19. Cowden C, Stretton AO, Davis RE. AF1, a sequenced bioactive neuropeptide isolated from the nematode Ascaris suum. Neuron (1989) 2:1465-73. doi:10.1016/0896-6273(89)90192-X
20. The C. elegans Sequencing Consortium. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science (1998) 282:2012-8. doi:10.1126/science.282.5396.2012
21. Nelson LS, Kim K, Memmott JE, Li C. FMRFamide-related gene family in the nematode, Caenorhabditis elegans. Mol Brain Res (1998) 58:103-11. doi:10.1016/S0169-328X(98)00106-5
22. Li C, Kim K, Nelson LS. FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. Brain Res (1999) 848:26-34. doi:10.1016/S0006-8993(99)01972-1
23. Kim K, Li C. Expression and regulation of an FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. J Comp Neurol (2004) 475:540-50. doi:10.1002/cne.20189
24. McCoy CJ, Atkinson LE, Zamanian M, McVeigh P, Day TA, Kimber MJ, et al. New insights into the FLPergic complements of parasitic nematodes: informing deorphanisation approaches. EuPA Open Proteomics (2014) 3:262-72. doi:10.1016/j.euprot.2014.04.002
25. Husson SJ, Clynen E, Baggerman G, De Loof A, Schoofs L. Discovering neuropeptides in Caenorhabditis elegans by two dimensional liquid chromatography and mass spectrometry. Biochem Biophys Res Commun (2005) 335:76-86. doi:10.1016/j.bbrc.2005.07.044
26. Husson SJ, Clynen E, Baggerman G, Janssen T, Schoofs L. Defective processing of neuropeptide precursors in Caenorhabditis elegans lacking proprotein convertase 2 (KPC-2/EGL-3): mutant analysis by mass spectrometry. J Neurochem (2006) 98:1999-2012. doi:10.1111/j.1471-4159.2006.04014.x
27. Husson SJ, Janssen T, Baggerman G, Bogert B, Kahn-Kirby AH, Ashrafi K, et al. Impaired processing of FLP and NLP peptides in carboxypeptidase E (EGL-21)-deficient Caenorhabditis elegans as analyzed by mass spectrometry. J Neurochem (2007) 102:246-60. doi:10.1111/j.1471-4159.2007.04474.x
28. Yew JY, Dikler S, Stretton AO. De novo sequencing of novel neuropeptides directly from Ascaris suum tissue using matrix-assisted laser desorption/ionization time-of-flight/time-of-flight. Rapid Commun Mass Spectrom (2003) 17:2693-8. doi:10.1002/rcm.1240
29. Yew JY, Kutz KK, Dikler S, Messinger L, Li L, Stretton AO. Mass spectrometric map of neuropeptide expression in Ascaris suum. J Comp Neurol (2005) 488:396-413. doi:10.1002/cne.20587
30. Husson SJ, Landuyt B, Nys T, Baggerman G, Boonen K, Clynen E, et al. Comparative peptidomics of Caenorhabditis elegans versus C. briggsae by LC-MALDI-TOF MS. Peptides (2009) 30:449-57. doi:10.1016/j.peptides.2008.07.021
31. Jarecki JL, Andersen K, Konop CJ, Knickelbine JJ, Vestling MM, Stretton AO. Mapping neuropeptide expression by mass spectrometry in single dissected identified neurons from the dorsal ganglion of the nematode Ascaris suum. ACS Chem Neurosci (2010) 1:505-19. doi:10.1021/cn1000217
32. Jarecki JL, Frey BL, Smith LM, Stretton AO. Discovery of neuropeptides in the nematode Ascaris suum by database mining and tandem mass spectrometry. J Proteome Res (2011) 10:3098-106. doi:10.1021/pr2001176
33. Rosoff ML, Doble KE, Price DA, Li C. The flp-1 propeptide is processed into multiple, highly similar FMRFamide-like peptides in Caenorhabditis elegans. Peptides (1993) 14:331-8. doi:10.1016/0196-9781(93)90049-M
34. Rogers CM, Franks CJ, Walker RJ, Burke JF, Holden-Dye L. Regulation of the pharynx of Caenorhabditis elegans by 5-HT, octopamine, and FMRFamide-like neuropeptides. J Neurobiol (2001) 49:235-44. doi:10.1002/neu.1078
35. Mertens I, Clinckspoor I, Janssen T, Nachman R, Schoofs L. FMRFamide related peptide ligands activate the Caenorhabditis elegans orphan GPCR Y59H11AL.1. Peptides (2006) 27:1291-6. doi:10.1016/j.peptides.2005.11.017
36. Schinkmann K, Li C. Comparison of two Caenorhabditis genes encoding FMRFamide(Phe-Met-Arg-Phe-NH2)-like peptides. Mol Brain Res (1994) 24:238-46. doi:10.1016/0169-328X(94)90137-6
37. Kimber MJ, Fleming CC, Bjourson AJ, Halton DW, Maule AG. FMRFamide-related peptides in potato cyst nematodes. Mol Biochem Parasitol (2001) 116:199-208. doi:10.1016/S0166-6851(01)00323-1
38. Kimber MJ, Fleming CC, Prior A, Jones JT, Halton DW, Maule AG. Localisation of Globodera pallida FMRFamide-related peptide encoding genes using in situ hybridisation. Int J Parasitol (2002) 32:1095-105. doi:10.1016/S0020-7519(02)00084-X
39. Kimber MJ, Fleming CC. Neuromuscular function in plant parasitic nematodes: a target for novel control strategies? Parasitology (2005) 131:S129-42. doi:10.1017/S0031182005009157
40. Lowery DE, Geary TG, Kubiak TM, Larsen MJ. G Protein-Coupled Receptor-like Receptors and Modulators Thereof United States, Patent 6,632,621. (2003). Available at: http://www.google.com/patents/EP1238076A2?cl=nl
41. Geary TG, Price DA, Bowman JW, Winterrowd CA, Mackenzie CD, Garrison RD, et al. Two FMRFamide-like peptides from the free-living nematode Panagrellus redivivus. Peptides (1992) 13:209-14. doi:10.1016/0196-9781(92)90098-N
42. Jarecki JL, Viola IR, Andersen KM, Miller AH, Ramaker MA, Vestling MM, et al. Three independent techniques localize expression of transcript afp-11 and its bioactive peptide products to the paired AVK neurons in Ascaris suum: in situ hybridization, immunocytochemistry, and single cell mass spectrometry. ACS Chem Neurosci (2013) 4:418-34. doi:10.1021/cn3001334
43. Kikuchi T, Cotton JA, Dalzell JJ, Hasegawa K, Kanzaki N, McVeigh P, et al. Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus. PLoS Pathog (2011) 7:e1002219. doi:10.1371/journal.ppat.1002219
44. Abad P, Gouzy J, Aury J-M, Castagnone-Sereno P, Danchin EGJ, Deleury E, et al. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol (2008) 26:909-15. doi:10.1038/nbt.1482
45. Mertens I, Meeusen T, Janssen T, Nachman R, Schoofs L. Molecular characterization of two G protein-coupled receptor splice variants as FLP2 receptors in Caenorhabditis elegans. Biochem Biophys Res Commun (2005) 330:967-74. doi:10.1016/j.bbrc.2005.03.071
46. Li C, Kim K. Neuropeptide gene families in Caenorhabditis elegans. Adv Exp Med Biol (2010) 692:98-137. doi:10.1007/978-1-4419-6902-6_6
47. Greenwood K, Williams T, Geary T. Nematode neuropeptide receptors and their development as anthelmintic screens. Parasitology (2005) 131:S169-77. doi:10.1017/S003118200500819X
48. Marks NJ, Maule AG, Geary TG, Thompson DP, Li C, Halton DW, et al. KSAYMRFamide (PF3/AF8) is present in the free-living nematode, Caenorhabditis elegans. Biochem Biophys Res Commun (1998) 248:422-5. doi:10.1006/bbrc.1998.8982
49. Maule AG, Shaw C, Bowman JW, Halton DW, Thompson DP, Geary TG, et al. KSAYMRFamide: a novel FMRamide-related heptapeptide from the free-living nematode, Panagrellus redivivus, which is myoactive in the parasitic nematode, Ascaris suum. Biochem Biophys Res Commun (1994) 200:973-80. doi:10.1006/bbrc.1994.1545
50. Mertens I, Vandingenen A, Meeusen T, Janssen T, Luyten W, Nachman RJ, et al. Functional characterization of the putative orphan neuropeptide G-protein coupled receptor C26F1.6 in Caenorhabditis elegans. FEBS Lett (2004) 573:55-60. doi:10.1016/j.febslet.2004.07.058
51. Davis RE, Stretton AOW. The motornervous system of Ascaris: electrophysiology and anatomy of the neurons and their control by neuromodulators. Parasitology (1996) 113:S97-117. doi:10.1017/S0031182000077921
52. Marks NJ, Maule AG, Li C, Nelson LS, Thompson DP, Alexander-Bowman S, et al. Isolation, pharmacology and gene organization of KPSFVRFamide: a neuropeptide from Caenorhabditis elegans. Biochem Biophys Res Commun (1999) 254:222-30. doi:10.1006/bbrc.1998.9920
53. Ringstad N, Horvitz HR. FMRFamide neuropeptides and acetylcholine synergistically inhibit egg-laying by C. elegans. Nat Neurosci (2008) 11:1168-76. doi:10.1038/nn.2186
54. Yew JY, Davis R, Dikler S, Nanda J, Reinders B, Stretton AO. Peptide products of the afp-6 gene of the nematode Ascaris suum have different biological actions. J Comp Neurol (2007) 502:872-82. doi:10.1002/cne.21357
55. Johnston MJG, McVeigh P, McMaster S, Fleming CC, Maule AG. FMRFamide-like peptides in root knot nematodes and their potential role in nematode physiology. J Helminthol (2010) 84:253-65. doi:10.1017/S0022149X09990630
56. Marks NJ, Maule AG, Geary TG, Thompson DP, Davis JP, Halton DW, et al. APEASPFIRFamide, a novel FMRFamide-related decapeptide from Caenorhabditis elegans: structure and myoactivity. Biochem Biophys Res Commun (1997) 231:591-5. doi:10.1006/bbrc.1997.6155
57. Marks NJ, Shaw C, Halton DW, Thompson DP, Geary TG, Li C, et al. Isolation and preliminary biological assessment of AADGAPLIRFamide and SVPGVLRFamide from Caenorhabditis elegans. Biochem Biophys Res Commun (2001) 286:1170-6. doi:10.1006/bbrc.2001.5524
58. Cowden C, Stretton AO. AF2, an Ascaris neuropeptide: isolation, sequence, and bioactivity. Peptides (1993) 14:423-30. doi:10.1016/0196-9781(93)90127-3
59. Maule AG, Shaw C, Bowman JW, Halton DW, Thompson DP, Geary TG, et al. The FMRFamide-like neuropeptide AF2 (Ascaris suum) is present in the free-living nematode, Panagrellus redivivus (Nematoda, Rhabditida). Parasitology (1994) 109:351-6. doi:10.1017/S0031182000078380
60. Kubiak TM, Larsen MJ, Zantello MR, Bowman JW, Nulf SC, Lowery DE. Functional annotation of the putative orphan Caenorhabditis elegans G-protein-coupled receptor C10C6.2 as a FLP15 peptide receptor. J Biol Chem (2003) 278:42115-20. doi:10.1074/jbc.M304056200
61. Rogers C, Reale V, Kim K, Chatwin H, Li C, Evans P, et al. Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nat Neurosci (2003) 6:1178-85. doi:10.1038/nn1140
62. Cohen M, Reale V, Olofsson B, Knights A, Evans P, de Bono M. Coordinated regulation of foraging and metabolism in C. elegans by RFamide neuropeptide signaling. Cell Metab (2009) 9:375-85. doi:10.1016/j.cmet.2009.02.003
63. Kubiak TM, Larsen MJ, Nulf SC, Zantello MR, Burton KJ, Bowman JW, et al. Differential activation of "social" and "solitary" variants of the Caenorhabditis elegans G protein-coupled receptor NPR-1 by its cognate ligand AF9. J Biol Chem (2003) 278:33724-9. doi:10.1074/jbc.M304861200
64. Etchberger JF, Lorch A, Sleumer MC, Zapf R, Jones SJ, Marra MA, et al. The molecular signature and cis-regulatory architecture of a C. elegans gustatory neuron. Genes Dev (2007) 21:1653-74. doi:10.1101/gad.1560107
65. Husson SJ, Mertens I, Janssen T, Lindemans M, Schoofs L. Neuropeptidergic signaling in the nematode Caenorhabditis elegans. Prog Neurobiol (2007) 82:33-55. doi:10.1016/j.pneurobio.2007.01.006
66. Elsworth B, Wasmuth J, Blaxter M. NEMBASE4: the nematode transcriptome resource. Int J Parasitol (2011) 41:881-94. doi:10.1016/j.ijpara.2011.03.009
67. Kumar S, Koutsovoulos G, Kaur G, Blaxter M. Toward 959 nematode genomes. Worm (2012) 1:42-50. doi:10.4161/worm.19046
68. Maule A, Curtis R. Parallels between plant and animal parasitic nematodes. In: Jones J, Gheysen G, Fenoll C, editors. Genomics and Molecular Genetics of Plant-Nematode Interactions SE - 11. Dordrecht: Springer (2011). p. 221-51.
69. Nässel DR, Wegener C. A comparative review of short and long neuropeptide F signaling in invertebrates: any similarities to vertebrate neuropeptide Y signaling? Peptides (2011) 32:1335-55. doi:10.1016/j.peptides.2011.03.013
70. Clynen E, Husson SJ, Schoofs L. Identification of new members of the (short) neuropeptide F family in Locusts and Caenorhabditis elegans. Ann N Y Acad Sci (2009) 1163:60-74. doi:10.1111/j.1749-6632.2008.03624.x
71. Bargmann CI, Kaplan JM. Signal transduction in the Caenorhabditis elegans nervous system. Annu Rev Neurosci (1998) 21:279-308. doi:10.1146/annurev.neuro.21.1.279
72. Atkinson HJ, Isaac RE, Harris PD, Sharpe CM. FMRFamide-like immunoreactivity within the nervous system of the nematodes Panagrellus redivius, Caenorhabditis elegans and Heterodera glycines. J Zool (1988) 216:663-71. doi:10.1111/j.1469-7998.1988.tb02464.x
73. Masler EP, Kovaleva ES, Sardanelli S. Comparison of FaRP immunoreactivity in free-living nematodes and in the plant-parasitic nematode Heterodera glycines. Ann N Y Acad Sci (1999) 897:253-63. doi:10.1111/j.1749-6632.1999.tb07896.x
74. Schinkmann K, Li C. Localization of FMRF amide-like peptides in Caenorhabditis elegans. J Comp Neurol (1992) 316:251-60. doi:10.1002/cne.903160209
75. Nanda JC, Stretton AOW. In situ hybridization of neuropeptide-encoding transcripts afp-1, afp-3, and afp-4 in neurons of the nematode Ascaris suum. J Comp Neurol (2010) 518:896-910. doi:10.1002/cne.22251
76. Sithigorngul P, Jarecki JL, Stretton AOW. A specific antibody to neuropeptide AF1 (KNEFIRFamide) recognizes a small subset of neurons in Ascaris suum: differences from Caenorhabditis elegans. J Comp Neurol (2011) 519:1546-61. doi:10.1002/cne.22584
77. Stretton AOW, Davis RE, Angstadt JD, Donmoyer JE, Johnson CD. Neural control of behaviour in Ascaris. Trends Neurosci (1985) 8:294-300. doi:10.1016/0166-2236(85)90105-5
78. Angstadt JD, Donmoyer JE, Stretton AO. Retrovesicular ganglion of the nematode Ascaris. J Comp Neurol (1989) 284:374-88. doi:10.1002/cne.902840305
79. Gilchrist A. Modulating G-protein-coupled receptors: from traditional pharmacology to allosterics. Trends Pharmacol Sci (2007) 28:431-7. doi:10.1016/j.tips.2007.06.012
80. Bridges TM, Lindsley CW. G-protein coupled receptors: from classical modes of modulation to allosteric mechanisms. ACS Chem Biol (2008) 3:530-41. doi:10.1021/cb800116f
81. Frooninckx L, Van Rompay L, Temmerman L, Van Sinay E, Beets I, Janssen T, et al. Neuropeptide GPCRs in C. elegans. Front Endocrinol (2012) 3:167. doi:10.3389/fendo.2012.00167
82. Hobert O. The Neuronal Genome of Caenorhabditis elegans. In: WormBook. The C. elegans Research Community editor. WormBook (2013). doi:10.1895/wormbook.1.75.1
83. de Bono M, Bargmann CI. Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell (1998) 94:679-89. doi:10.1016/S0092-8674(00)81609-8
84. Mirabeau O, Joly J-S. Molecular evolution of peptidergic signaling systems in bilaterians. Proc Natl Acad Sci U S A (2013) 110:E2028-37. doi:10.1073/pnas.1219956110
85. Mertens I, Vandingenen A, Meeusen T, De Loof A, Schoofs L. Postgenomic characterization of G-protein-coupled receptors. Pharmacogenomics (2004) 5:657-72. doi:10.1517/14622416.5.6.657
86. Dalzell JJ, McMaster S, Fleming CC, Maule AG. Short interfering RNA-mediated gene silencing in Globodera pallida and Meloidogyne incognita infective stage juveniles. Int J Parasitol (2010) 40:91-100. doi:10.1016/j.ijpara.2009.07.003
87. Atkinson LE, Stevenson M, McCoy CJ, Marks NJ, Fleming C, Zamanian M, et al. flp-32 ligand/receptor silencing phenocopy faster plant pathogenic nematodes. PLoS Pathog (2013) 9:e1003169. doi:10.1371/journal.ppat.1003169
88. Kubiak TM, Larsen MJ, Bowman JW, Geary TG, Lowery DE. FMRFamide-like peptides encoded on the flp-18 precursor gene activate two isoforms of the orphan Caenorhabditis elegans G-protein-coupled receptor Y58G8A.4 heterologously expressed in mammalian cells. Biopolymers (2008) 90:339-48. doi:10.1002/bip.20850
89. Lingueglia E, Champigny G, Lazdunski M, Barbry P. Cloning of the amiloride-sensitive FMRFamide peptide-gated sodium channel. Nature (1995) 378:730-3. doi:10.1038/378730a0
90. Purcell J, Robertson AP, Thompson DP, Martin RJ. PF4, a FMRFamide-related peptide, gates low-conductance Cl- channels in Ascaris suum. Eur J Pharmacol (2002) 456:11-7. doi:10.1016/S0014-2999(02)02622-5
91. Bowman JW, Friedman AR, Thompson DP, Maule AG, Alexander-Bowman SJ, Geary TG. Structure-activity relationships of an inhibitory nematode FMRFamide-related peptide, SDPNFLRFamide (PF1), on Ascaris suum muscle. Int J Parasitol (2002) 32:1765-71. doi:10.1016/S0020-7519(02)00213-8
92. Maule AG, Geary TG, Bowman JW, Marks NJ, Blair KL, Halton DW, et al. Inhibitory effects of nematode FMRFamide-related peptides (FaRPs) on muscle strips from Ascaris suum. Invert Neurosci (1995) 1:255-65. doi:10.1007/BF02211027
93. Bowman JW, Friedman AR, Thompson DP, Ichhpurani AK, Kellman MF, Marks N, et al. Structure-activity relationships of KNEFIRFamide (AF1), a nematode FMRFamide-related peptide, on Ascaris suum muscle. Peptides (1996) 17:381-7. doi:10.1016/0196-9781(96)00007-1
94. Holden-Dye L, Brownlee DJ, Walker RJ. The effects of the peptide KPNFIRFamide (PF4) on the somatic muscle cells of the parasitic nematode Ascaris suum. Br J Pharmacol (1997) 120:379-86. doi:10.1038/sj.bjp.0700906
95. de Bono M, Maricq AV. Neuronal substrates of complex behaviors in C. elegans. Annu Rev Neurosci (2005) 28:451-501. doi:10.1146/annurev.neuro.27.070203.144259
96. Reinitz CA, Pleva AE, Stretton AOW. Changes in cyclic nucleotides, locomotory behavior, and body length produced by novel endogenous neuropeptides in the parasitic nematode Ascaris suum. Mol Biochem Parasitol (2011) 180:27-34. doi:10.1016/j.molbiopara.2011.08.001
97. Bendena WG, Campbell J, Zara L, Tobe SS, Chin-Sang ID. Select neuropeptides and their G-protein coupled receptors in Caenorhabditis elegans and Drosophila melanogaster. Front Endocrinol (2012) 3:93. doi:10.3389/fendo.2012.00093
98. de Bono M, Tobin DM, Davis MW, Avery L, Bargmann C. Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli. Nature (2002) 419:899-903. doi:10.1038/nature01169
99. Coates JC, de Bono M. Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Caenorhabditis elegans. Nature (2002) 419:925-9. doi:10.1038/nature01170
100. Macosko EZ, Pokala N, Feinberg EH, Chalasani SH, Butcher RA, Clardy J, et al. A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature (2009) 458:1171-5. doi:10.1038/nature07886
101. White JG, Southgate E, Thomson JN, Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc B Biol Sci (1986) 314:1-340. doi:10.1098/rstb.1986.0056
102. Gray JM, Karow DS, Lu H, Chang AJ, Chang JS, Ellis RE, et al. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature (2004) 430:317-22. doi:10.1038/nature02714
103. Cheung BHH, Cohen M, Rogers C, Albayram O, de Bono M. Experience-dependent modulation of C. elegans behavior by ambient oxygen. Curr Biol (2005) 15:905-17. doi:10.1016/j.cub.2005.04.017
104. Chang AJ, Chronis N, Karow DS, Marletta MA, Bargmann CI. A distributed chemosensory circuit for oxygen preference in C. elegans. PLoS Biol (2006) 4:e274. doi:10.1371/journal.pbio.0040274
105. Rogers C, Persson A, Cheung B, de Bono M. Behavioral motifs and neural pathways coordinating O2 responses and aggregation in C. elegans. Curr Biol (2006) 16:649-59. doi:10.1016/j.cub.2006.03.023
106. Chang AJ, Bargmann CI. Hypoxia and the HIF-1 transcriptional pathway reorganize a neuronal circuit for oxygen-dependent behavior in Caenorhabditis elegans. Proc Natl Acad Sci U S A (2008) 105:7321-6. doi:10.1073/pnas.0802164105
107. Davies AG, Bettinger JC, Thiele TR, Judy ME, McIntire SL. Natural variation in the npr-1 gene modifies ethanol responses of wild strains of C. elegans. Neuron (2004) 42:731-43. doi:10.1016/j.neuron.2004.05.004
108. Hallem EA, Sternberg PW. Acute carbon dioxide avoidance in Caenorhabditis elegans. Proc Natl Acad Sci U S A (2008) 105:8038-43. doi:10.1073/pnas.0707469105
109. Styer KL, Singh V, Macosko E, Steele SE, Bargmann CI, Aballay A. Innate immunity in Caenorhabditis elegans is regulated by neurons expressing NPR-1/GPCR. Science (2008) 322:460-4. doi:10.1126/science.1163673
110. Reddy KC, Andersen EC, Kruglyak L, Kim DH. A polymorphism in npr-1 is a behavioral determinant of pathogen susceptibility in C. elegans. Science (2009) 323:382-4. doi:10.1126/science.1166527
111. Pocock R, Hobert O. Hypoxia activates a latent circuit for processing gustatory information in C. elegans. Nat Neurosci (2010) 13:610-4. doi:10.1038/nn.2537
112. Glauser DA, Chen WC, Agin R, Macinnis BL, Hellman AB, Garrity PA, et al. Heat avoidance is regulated by transient receptor potential (TRP) channels and a neuropeptide signaling pathway in Caenorhabditis elegans. Genetics (2011) 188:91-103. doi:10.1534/genetics.111.127100
113. Carrillo MA, Guillermin ML, Rengarajan S, Okubo RP, Hallem EA. O2-sensing neurons control CO2 response in C. elegans. J Neurosci (2013) 33:9675-83. doi:10.1523/JNEUROSCI.4541-12.2013
114. Jang H, Kim K, Neal SJ, Macosko E, Kim D, Butcher RA, et al. Neuromodulatory state and sex specify alternative behaviors through antagonistic synaptic pathways in C. elegans. Neuron (2012) 75:585-92. doi:10.1016/j.neuron.2012.06.034
115. Choi S, Chatzigeorgiou M, Taylor KP, Schafer WR, Kaplan JM. Analysis of NPR-1 reveals a circuit mechanism for behavioral quiescence in C. elegans. Neuron (2013) 78:869-80. doi:10.1016/j.neuron.2013.04.002
116. Bargmann CI, Horvitz HR. Control of larval development by chemosensory neurons in Caenorhabditis elegans. Science (1991) 251:1243-6. doi:10.1126/science.2006412
117. Gray JM, Hill JJ, Bargmann C. A circuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci U S A (2005) 102:3184-91. doi:10.1073/pnas.0409009101
118. Tomioka M, Adachi T, Suzuki H, Kunitomo H, Schafer WR, Iino Y. The insulin/PI 3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron (2006) 51:613-25. doi:10.1016/j.neuron.2006.07.024
119. Chalasani SH, Chronis N, Tsunozaki M, Gray JM, Ramot D, Goodman M, et al. Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans. Nature (2007) 450:63-70. doi:10.1038/nature06292
120. Chalasani SH, Kato S, Albrecht DR, Nakagawa T, Abbott LF, Bargmann C. Neuropeptide feedback modifies odor-evoked dynamics in Caenorhabditis elegans olfactory neurons. Nat Neurosci (2010) 13:615-21. doi:10.1038/nn.2526
121. Hart A, Chao MY. From Odors to Behaviors in Caenorhabditis elegans. The Neurobiology of Olfaction. Boca Raton, FL: CRC Press (2010).
122. Chalfie M, Sulston J, White JG, Southgate E, Thomson JN, Brenner S. The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci (1985) 5:956-64.
123. Horoszok L, Raymond V, Sattelle DB, Wolstenholme AJ. GLC-3: a novel fipronil and BIDN-sensitive, but picrotoxinin-insensitive, L-glutamate-gated chloride channel subunit from Caenorhabditis elegans. Br J Pharmacol (2001) 132:1247-54. doi:10.1038/sj.bjp.0703937
124. Kaufman A, Keinan A, Meilijson I, Kupiec M, Ruppin E. Quantitative analysis of genetic and neuronal multi-perturbation experiments. PLoS Comput Biol (2005) 1:e64. doi:10.1371/journal.pcbi.0010064
125. Avery L. The genetics of feeding in Caenorhabditis elegans. Genetics (1993) 133:897-917.
126. Albertson DG, Thomson JN. The pharynx of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci (1976) 275:299-325. doi:10.1098/rstb.1976.0085
127. Nass R, Merchant KM, Ryan T. Caenohabditis elegans in Parkinson's disease drug discovery: addressing an unmet medical need. Mol Interv (2008) 8:284-93. doi:10.1124/mi.8.6.6
128. Papaioannou S, Marsden D, Franks CJ, Walker RJ, Holden-Dye L. Role of a FMRFamide-like family of neuropeptides in the pharyngeal nervous system of Caenorhabditis elegans. J Neurobiol (2005) 65:304-19. doi:10.1002/neu.20201
129. Papaioannou S, Holden-Dye L, Walker RJ. Evidence for a role for cyclic AMP in modulating the action of 5-HT and an excitatory neuropeptide, FLP17A, in the pharyngeal muscle of Caenorhabditis elegans. Invert Neurosci (2008) 8:91-100. doi:10.1007/s10158-008-0072-8
130. Brownlee DJA, Holden-Dye L, Fairweather I, Walker RJ. The action of serotonin and the nematode neuropeptide KSAYMRFamide on the pharyngeal muscle of the parasitic nematode, Ascaris suum. Parasitology (1995) 111:379-84. doi:10.1017/S0031182000081932
131. Brownlee DJ, Holden-Dye L, Walker RJ, Fairweather I. The pharynx of the nematode Ascaris suum: structure and function. Acta Biol Hung (1995) 46:195-204.
132. Brownlee DJ, Walker RJ. Actions of nematode FMRFamide-related peptides on the pharyngeal muscle of the parasitic nematode, Ascaris suum. Ann N Y Acad Sci (1999) 897:228-38. doi:10.1111/j.1749-6632.1999.tb07894.x
133. Fellowes RA, Maule AG, Marks NJ, Geary TG, Thompson DP, Shaw C, et al. Modulation of the motility of the vagina vera of Ascaris suum in vitro by FMRF amide-related peptides. Parasitology (1998) 116(Pt 3):277-87. doi:10.1017/S0031182097002229
134. Moffett CL, Beckett AM, Mousley A, Geary TG, Marks NJ, Halton DW, et al. The ovijector of Ascaris suum: multiple response types revealed by Caenorhabditis elegans FMRFamide-related peptides. Int J Parasitol (2003) 33:859-76. doi:10.1016/S0020-7519(03)00109-7
135. Trailovic SM, Clark CL, Robertson AP, Martin RJ. Brief application of AF2 produces long lasting potentiation of nAChR responses in Ascaris suum. Mol Biochem Parasitol (2005) 139:51-64. doi:10.1016/j.molbiopara.2004.10.001
136. Verma S, Robertson AP, Martin RJ. The nematode neuropeptide, AF2 (KHEYLRF-NH2), increases voltage-activated calcium currents in Ascaris suum muscle. Br J Pharmacol (2007) 151:888-99. doi:10.1038/sj.bjp.0707296
137. Thompson DP, Davis JP, Larsen MJ, Coscarelli EM, Zinser EW, Bowman JW, et al. Effects of KHEYLRFamide and KNEFIRFamide on cyclic adenosine monophosphate levels in Ascaris suum somatic muscle. Int J Parasitol (2003) 33:199-208. doi:10.1016/S0020-7519(02)00259-X
138. Davis RE, Stretton AO. Structure-activity relationships of 18 endogenous neuropeptides on the motor nervous system of the nematode Ascaris suum. Peptides (2001) 22:7-23. doi:10.1016/S0196-9781(00)00351-X
139. Reinitz CA, Herfel HG, Messinger LA, Stretton AOW. Changes in locomotory behavior and cAMP produced in Ascaris suum by neuropeptides from Ascaris suum or Caenorhabditis elegans. Mol Biochem Parasitol (2000) 111:185-97. doi:10.1016/S0166-6851(00)00317-0
140. Kimber MJ, McKinney S, McMaster S, Day TA, Fleming CC, Maule AG. flp gene disruption in a parasitic nematode reveals motor dysfunction and unusual neuronal sensitivity to RNA interference. FASEB J (2007) 21:1233-43. doi:10.1096/fj.06-7343com
141. Dalzell JJ, McMaster S, Johnston MJ, Kerr R, Fleming CC, Maule AG. Non-nematode-derived double-stranded RNAs induce profound phenotypic changes in Meloidogyne incognita and Globodera pallida infective juveniles. Int J Parasitol (2009) 39:1503-16. doi:10.1016/j.ijpara.2009.05.006
142. Papolu PK, Gantasala NP, Kamaraju D, Banakar P, Sreevathsa R, Rao U. Utility of host delivered RNAi of two FMRF amide like peptides, flp-14 and flp-18, for the management of root knot nematode, Meloidogyne incognita. PLoS One (2013) 8:e80603. doi:10.1371/journal.pone.0080603
143. Brenner S. The genetics of Caenorhabditis elegans. Genetics (1974) 77:71-94.
144. Alfonso A, Grundahl K, Duerr JS, Han HP, Rand JB. The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter. Science (1993) 261:617-9. doi:10.1126/science.8342028
145. McIntire SL, Jorgensen E, Kaplan J, Horvitz HR. The GABAergic nervous system of Caenorhabditis elegans. Nature (1993) 364:337-41. doi:10.1038/364337a0
146. Nelson LS, Rosoff ML, Li C. Disruption of a neuropeptide gene, flp-1, causes multiple behavioral defects in Caenorhabditis elegans. Science (1998) 281:1686-90. doi:10.1126/science.281.5383.1686
147. Sieburth D, Ch'ng Q, Dybbs M, Tavazoie M, Kennedy S, Wang D, et al. Systematic analysis of genes required for synapse structure and function. Nature (2005) 436:510-7. doi:10.1038/nature03809
148. Stawicki TM, Takayanagi-Kiya S, Zhou K, Jin Y. Neuropeptides function in a homeostatic manner to modulate excitation-inhibition imbalance in C. elegans. PLoS Genet (2013) 9:e1003472. doi:10.1371/journal.pgen.1003472
149. Wani KA, Catanese M, Normantowicz R, Herd M, Maher KN, Chase DL. D1 dopamine receptor signaling is modulated by the R7 RGS protein EAT-16 and the R7 binding protein RSBP-1 in Caenorhabditis elegans motor neurons. PLoS One (2012) 7:e37831. doi:10.1371/journal.pone.0037831
150. Taghert PH, Nitabach MN. Peptide neuromodulation in invertebrate model systems. Neuron (2012) 76:82-97. doi:10.1016/j.neuron.2012.08.035
151. Bargmann CI. Beyond the connectome: how neuromodulators shape neural circuits. Bioessays (2012) 34:458-65. doi:10.1002/bies.201100185
152. Yang H-YT, Tao T, Iadarola MJ. Modulatory role of neuropeptide FF system in nociception and opiate analgesia. Neuropeptides (2008) 42:1-18. doi:10.1016/j.npep.2007.06.004
153. Feng Y, He X, Yang Y, Chao D, Lazarus LH, Xia Y. Current research on opioid receptor function. Curr Drug Targets (2012) 13:230-46. doi:10.2174/138945012799201612
154. Greenberg MJ, Painter SD, Doble KE, Nagle GT, Price DA, Lehman HK. The molluscan neurosecretory peptide FMRFamide: comparative pharmacology and relationship to the enkephalins. Fed Proc (1983) 42:82-6.
155. Hart A, Sims S, Kaplan JM. Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature (1995) 378:82-5. doi:10.1038/378082a0
156. Chao MY, Komatsu H, Fukuto HS, Dionne HM, Hart A. Feeding status and serotonin rapidly and reversibly modulate a Caenorhabditis elegans chemosensory circuit. Proc Natl Acad Sci U S A (2004) 101:15512-7. doi:10.1073/pnas.0403369101
157. Akil H, Watson SJ, Young E, Lewis ME, Khachaturian H, Walker JM. Endogenous opioids: biology and function. Annu Rev Neurosci (1984) 7:223-55. doi:10.1146/annurev.ne.07.030184.001255
158. Fields H. State-dependent opioid control of pain. Nat Rev Neurosci (2004) 5:565-75. doi:10.1038/nrn1431
159. Waggoner LE, Hardaker LA, Golik S, Schafer WR. Effect of a neuropeptide gene on behavioral states in Caenorhabditis elegans egg-laying. Genetics (2000) 154:1181-92.
160. Keating CD, Kriek N, Daniels M, Ashcroft NR, Hopper NA, Siney EJ, et al. Whole-genome analysis of 60 G protein-coupled receptors in Caenorhabditis elegans by gene knockout with RNAi. Curr Biol (2003) 13:1715-20. doi:10.1016/j.cub.2003.09.003
161. Marks NJ, Maule AG. Neuropeptides in helminths: occurrence and distribution. Adv Exp Med Biol (2010) 692:49-77. doi:10.1007/978-1-4419-6902-6_4
162. Trent C, Tsuing N, Horvitz HR. Egg-laying defective mutants of the nematode Caenorhabditis elegans. Genetics (1983) 104:619-47.
163. Liu T, Kim K, Li C, Barr MM. FMRFamide-like neuropeptides and mechanosensory touch receptor neurons regulate male sexual turning behavior in Caenorhabditis elegans. J Neurosci (2007) 27:7174-82. doi:10.1523/JNEUROSCI.1405-07.2007
164. Guan Z, Giustetto M, Lomvardas S, Kim J-H, Miniaci MC, Schwartz JH, et al. Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell (2002) 111:483-93. doi:10.1016/S0092-8674(02)01074-7
165. Guan Z, Kim J-H, Lomvardas S, Holick K, Xu S, Kandel ER, et al. p38 MAP kinase mediates both short-term and long-term synaptic depression in aplysia. J Neurosci (2003) 23:7317-25.
166. Krashes MJ, DasGupta S, Vreede A, White B, Armstrong JD, Waddell S. A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell (2009) 139:416-27. doi:10.1016/j.cell.2009.08.035
167. Ardiel EL, Rankin CH. An elegant mind: learning and memory in Caenorhabditis elegans. Learn Mem (2010) 17:191-201. doi:10.1101/lm.960510
168. Beets I, Janssen T, Meelkop E, Temmerman L, Suetens N, Rademakers S, et al. Vasopressin/oxytocin-related signaling regulates gustatory associative learning in C. elegans. Science (2012) 338:543-5. doi:10.1126/science.1226860
169. Giles AC, Rankin CH. Behavioral and genetic characterization of habituation using Caenorhabditis elegans. Neurobiol Learn Mem (2009) 92:139-46. doi:10.1016/j.nlm.2008.08.004
170. Li C, Timbers TA, Rose JK, Bozorgmehr T, McEwan A, Rankin CH. The FMRFamide-related neuropeptide FLP-20 is required in the mechanosensory neurons during memory for massed training in C. elegans. Learn Mem (2013) 20:103-8. doi:10.1101/lm.028993.112
171. Rankin CH, Beck CD, Chiba CM. Caenorhabditis elegans: a new model system for the study of learning and memory. Behav Brain Res (1990) 37:89-92. doi:10.1016/0166-4328(90)90074-O
172. Rose JK, Rankin CH. Blocking memory reconsolidation reverses memory-associated changes in glutamate receptor expression. J Neurosci (2006) 26:11582-7. doi:10.1523/JNEUROSCI.2049-06.2006
173. Li C, Kim K. Neuropeptides. In WormBook. The C. elegans Research Community, editor. WormBook (2008). Available at: http://www.wormbook.org
174. Leinwand SG, Chalasani SH. Neuropeptide signaling remodels chemosensory circuit composition in Caenorhabditis elegans. Nat Neurosci (2013) 16:1461-7. doi:10.1038/nn.3511