Discovery of a cholecystokinin-gastrin-like signaling system in nematodes

Endocrinology

Volumn 149, Issue 6, 2008, Pages 2826-2839

  Janssen, Tom ^a   Meelkop, Ellen ^a   Lindemans, Marleen ^a   Verstraelen, Karen ^a   Husson, Steven J ^a   Temmerman, Liesbet ^a   Nachman, Ronald J ^b   Schoofs, Liliane ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b SOUTHERN PLAINS AGRICULTURAL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLASE; ANTIBODY; CCK 8 ANTIBODY; CHOLECYSTOKININ; CHOLECYSTOKININ B RECEPTOR; CHOLECYSTOKININ RECEPTOR; GASTRIN; NEUROPEPTIDE RECEPTOR; SULFAKININ RECEPTOR;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DEFECATION; ENZYME ACTIVITY; ENZYME RELEASE; GENE IDENTIFICATION; GENE SEQUENCE; GENOME; LIPID STORAGE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SULFATION;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHOLECYSTOKININ; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CLONING, MOLECULAR; GASTRINS; OPEN READING FRAMES; RECEPTORS, CCR2; RECEPTORS, CHOLECYSTOKININ; SIGNAL TRANSDUCTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 44249103225     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2007-1772     Document Type: Article

References (106)

1. Johnsen AH 1998 Phylogeny of the cholecystokinin/gastrin family. Front Neuroendocrinol 19:73-99
2. Dufresne M, Seva C, Fourmy D 2006 Cholecystokinin and gastrin receptors. Physiol Rev 86:805-847
3. Konturek SJ, Pepera J, Zabielski K, Konturek PC, Pawlik T, Szlachcic A, Hahn EG 2003 Brain-gut axis in pancreatic secretion and appetite control. J Physiol Pharmacol 54:293-317
4. Clerc P, Coll Constans MG, Lulka H, Broussaud S, Guigne C, Leung-Theung-Long S, Perrin C, Knauf C, Carpene C, Penicaud L, Seva C, Burcelin R, Valet P, Fourmy D, Dufresne M 2007 Involvement of cholecystokinin 2 receptor in food intake regulation: hyperphagia and increased fat deposition in cholecystokinin 2 receptor-deficient mice. Endocrinology 148:1039-1049
5. Fourmy D, Escrieut C, Archer E, Gales C, Gigoux V, Maigret B, Moroder L, Silvente-Poirot S, Martinez J, Fehrentz JA, Pradayrol L 2002 Structure of cholecystokinin receptor binding sites and mechanism of activation/inactivation by agonists/antagonists. Pharmacol Toxicol 91:313-320
6. Silvente-Poirot S, Dufresne M, Vaysse N, Fourmy D 1993 The peripheral cholecystokinin receptors. Eur J Biochem 215:513-529
7. Wank SA 1998 G protein-coupled receptors in gastrointestinal physiology. I. CCK receptors: an exemplary family. Am J Physiol 274(4 Pt 1):G607-G613
8. Maestro JL, Aguilar R, Pascual N, Valero ML, Piulachs MD, Andreu D, Navarro I, Belles X 2001 Screening of antifeedant activity in brain extracts led to the identification of sulfakinin as a satiety promoter in the German cockroach. Are arthropod sulfakinins homologous to vertebrate gastrins-cholecystokinins? Eur J Biochem 268:5824-5830
9. Nachman RJ, Holman GM, Cook BJ, Haddon WF, Ling N 1986 Leucosulfakinin-II, a blocked sulfated insect neuropeptide with homology to cholecystokinin and gastrin. Biochem Biophys Res Commun 140:357-364
10. Nachman RJ, Holman GM, Haddon WF, Ling N 1986 Leucosulfakinin, a sulfated insect neuropeptide with homology to gastrin and cholecystokinin. Science 234:71-73
11. Predel R, Nachman RJ, Gade G 2001 Myostimulatory neuropeptides in cockroaches: structures, distribution, pharmacological activities, and mimetic analogs. J Insect Physiol 47:311-324
12. Schoofs L, Holman GM, Hayes TK, De Loof A 1990 Isolation and identification of a sulfakinin-like peptide with sequence homology to vertebrate gastrin and cholecystokinin, from the brain of Locusta migratoria. In: McCaffery A, Wilson I, eds. Chromatography and isolation of insect hormones and pheromones. New York: Plenum Press; 231-241
13. Veenstra JA 1989 Isolation and structure of two gastrin/CCK-like neuropeptides from the American cockroach homologous to the leucosulfakinins. Neuropeptides 14:145-149
14. Schoofs L, Clynen E, Cerstiaens A, Baggerman G, Wei Z, Vercammen T, Nachman R, De Loof A, Tanaka S 2001 Newly discovered functions for some myotropic neuropeptides in locusts. Peptides 22:219-227
15. Wei Z, Baggerman G, Nachman J, Goldsworthy G, Verhaert P, De Loof A, Schoofs L 2000 Sulfakinins reduce food intake in the desert locust, Schistocerca gregaria. J Insect Physiol 46:1259-1265
16. Meyering-Vos M, Muller A 2007 RNA interference suggests sulfakinins as satiety effectors in the cricket Gryllus bimaculatus. J Insect Physiol 53:840-848
17. Downer KE, Haselton AT, Nachman RJ, Stoffolano Jr JG 2007 Insect satiety: sulfakinin localization and the effect of drosulfakinin on protein and carbohydrate ingestion in the blow fly, Phormia regina (Diptera: Calliphoridae). J Insect Physiol 53:106-112
18. Downer KE, Nachman RJ, Stoffolano JG 2007 Effect of seasonality and perisulfakinin on engorgement by Tabanus nigrovittatus (Diptera: Tabanidae) in the laboratory. Ann Entomol Soc Am 100:251-256
19. Nachman RJ, Giard W, Favrel P, Suresh T, Streekumar S, Holman GM 1997 Insect myosuppressins and sulfakinins stimulate release of the digestive enzyme α-amylase in two invertebrates: the scallop Pecten maximus and insect Rhynchophorus ferrugineus. In: Beckwith BE, Saria A, Chronwall BM, Sandman CA, Strand FL (eds.) Neuropeptides in development and aging. Ann NY Acad Sci 814:335-338
20. Harshini S, Nachman RJ, Sreekumar S 2002 In vitro release of digestive enzymes by FMRF amide related neuropeptides and analogues in the lepidopteran insect Opisina arenosella (Walk.). Peptides 23:1759-1763
21. Duve H, Rehfeld JF, East P, Thorpe A 1994 Localisation of sulfakinin neuronal pathways in the blowfly Calliphora vomitoria. Cell Tissue Res 275:177-186
22. Johnsen AH, Duve H, Davey M, Hall M, Thorpe A 2000 Sulfakinin neuropeptides in a crustacean. Isolation, identification and tissue localization in the tiger prawn Penaeus monodon. Eur J Biochem 267:1153-1160
23. Nichols R, Lim IA 1996 Spatial and temporal immunocytochemical analysis of drosulfakinin (Dsk) gene products in the Drosophila melanogaster central nervous system. Cell Tissue Res 283:107-116
24. East PD, Hales DF, Cooper PD 1997 Distribution of sulfakinin-like peptides in the central and sympathetic nervous system of the American cockroach, Periplaneta americana (L.) and the field cricket, Teleogryllus commodus (Walker). Tissue Cell 29:347-354
25. Predel R, Brandt W, Kellner R, Rapus J, Nachman RJ, Gade G 1999 Post-translational modifications of the insect sulfakinins: sulfation, pyroglutamate-formation and O-methylation of glutamic acid. Eur J Biochem 263:552-560
26. Schoofs L, Nachman RJ 2006 Sulfakinins. In: Kastrin A, ed. Handbook of biologically active peptides. San Diego: Elsevier; 183-187
27. Torfs P, Baggerman G, Meeusen T, Nieto J, Nachman RJ, Calderon J, De Loof A, Schoofs L 2002 Isolation, identification, and synthesis of a disulfated sulfakinin from the central nervous system of an arthropods the white shrimp Litopenaeus vannamei. Biochem Biophys Res Commun 299:312-320
28. Nichols R, Schneuwly SA, Dixon JE 1988 Identification and characterization of a Drosophila homologue to the vertebrate neuropeptide cholecystokinin. J Biol Chem 263:12167-12170
29. Hewes RS, Taghert PH 2001 Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Res 11:1126-1142
30. Kubiak TM, Larsen MJ, Burton KJ, Bannow CA, Martin RA, Zantello MR, Lowery DE 2002 Cloning and functional expression of the first Drosophila melanogaster sulfakinin receptor DSK-R1. Biochem Biophys Res Commun 291:313-320
31. Smiri Y, Bulet P, Andries JC 1992 Molecular heterogeneity of gastrin cholecystokinin-like immunoreactive peptides in Nereis diversicolor (Annelida, Polychaeta). Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 101:71-73
32. McIntire SL, Horvitz HR 1985 Immunocytochemical reactivity of C. elegans neurons with antisera against known neurotransmitters. Cold Spring Harbor Abstracts (Abstract)
33. Cowden PC, Stretton AOW 1986 A CCK-like neuropeptide in Ascaris. Abstr Soc Neurosci 12:246 (Abstract)
34. Brownlee DJA, Fairweather I, Johnston CF, Smart D, Shaw C, Halton DW 1993 Immunocytochemical demonstration of neuropeptides in the central nervous system of the roundworm, Ascaris suum (Nematoda: Ascaroidea). Parasitology 106(Pt 3):305-316
35. Cowden C, Sithigorngul P, Brackley P, Guastella J, Stretton AOW 1993 Localization and differential expression of Fmrfamide-like immunoreactivity in the Nematode Ascaris suum. J Comp Neurol 333:455-468
36. Sithigorngul P, Cowden C, Guastella J, Stretton AOW 1989 Generation of monoclonal antibodies against a nematode peptide extract: another approach for identifying unknown neuropeptides. J Comp Neurol 284:389-397
37. Sithigorngul P, Cowden C, Stretton AOW 1996 Heterogeneity of cholecystokinin/ gastrin-like immunoreactivity in the nervous system of the nematode Ascaris suum. J Comp Neurol 370:427-442
38. McKay RM, McKay JP, Suh JM, Avery L, Graff JM 2007 Tripeptidyl peptidase II promotes fat formation in a conserved fashion. EMBO Rep 8:1183-1189
39. Meeusen T, Mertens I, De Loof A, Schoofs L 2003 G protein-coupled receptors in invertebrates: a state of the art. Int Rev Cytol 230:189-261
40. 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. Biochem Biophys Res Commun 330:967-974
41. Husson SJ, Clynen E, Baggerman G, De Loof A, Schoofs L 2005 Discovering neuropeptides in Caenorhabditis elegans by two dimensional liquid chromatography and mass spectrometry. Biochem Biophys Res Commun 335:76-86
42. Nachman RJ, Teal PE, Ujvary I 2001 Comparative topical pheromonotropic activity of insect pyrokinin/PBAN amphiphilic analogs incorporating different fatty and/or cholic acid components. Peptides 22:279-285
43. Nachman RJ, Holman GM, Haddon WF 1988 Structural aspects of gastrin/CCK-like insect leucosulfakinins and FMRF-amide. Peptides 9(Suppl 1):137-143
44. Wiechelman KJ, Braun RD, Fitzpatrick JD 1988 Investigation of the bicinchoninic acid protein assay: identification of the groups responsible for color formation. Anal Biochem 175:231-237
45. Kulkarni MM, Perrimon N 2005 Super-size flies. Cell Metab 1:288-290
46. Husson SJ, Clynen E, Baggerman G, Janssen T, Schoofs L 2006 Defective processing of neuropeptide precursors in Caenorhabditis elegans lacking proprotein convertase 2 (KPC-2/EGL-3): mutant analysis by mass spectrometry. J Neurochem 98:1999-2012
47. Hobert O 2002 PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32:728-730
48. White JG, Southgate E, Thomson JN, Brenner S 1986 The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314:1-340
49. Cook BJ, Holman GM 1978 Comparative pharmacological properties of muscle function in the foregut and the hindgut of the cockroach Leucophaea maderae. Comp Biochem Physiol C 61 C:291-295
50. Husson SJ, Mertens I, Janssen T, Lindemans M, Schoofs L 2007 Neuropeptidergic signaling in the nematode Caenorhabditis elegans. Prog Neurobiol 82:33-55
51. Li C 2005 The ever-expanding neuropeptide gene families in the nematode Caenorhabditis elegans. Parasitology 131(Suppl):S109-S127
52. Delsuc F, Brinkmann H, Chourrout D, Philippe H 2006 Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965-968
53. Jensen RT, Lemp GF, Gardner JD 1982 Interactions of COOH-terminal fragments of cholecystokinin with receptors on dispersed acini from guinea pig pancreas. J Biol Chem 257:5554-5559
54. Li C, Nelson LS, Kim K, Nathoo A, Hart AC 1999 Neuropeptide gene families in the nematode Caenorhabditis elegans. Ann NY Acad Sci 897:239-252
55. McVeigh P, Leech S, Marks NJ, Geary TG, Maule AG 2006 Gene expression and pharmacology of nematode NLP-12 neuropeptides. Int J Parasitol 36:633-640
56. Yew JY, Kutz KK, Dikler S, Messinger L, Li LJ, Stretton AO 2005 Mass spectrometric map of neuropeptide expression in Ascaris suum. J Comp Neurol 488:396-413
57. Meyering-Vos M, Muller A 2007 Structure of the sulfakinin cDNA and gene expression from the Mediterranean field cricket Gryllus bimaculatus. Insect Mol Biol 16:445-454
58. Thompson JD, Higgins DG, Gibson TJ 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680
59. Saitou N, Nei M 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425
60. Ruiz-Gayo M, Dauge V, Menant I, Begue D, Gacel G, Roques BP 1985 Synthesis and biological activity of Boc [Nle28, Nle31]CCK27-33, a highly potent CCK8 analogue. Peptides 6:415-420
61. Nathoo AN, Moeller RA, Westlund BA, Hart AC 2001 Identification of neuropeptide-like protein gene families in Caenorhabditis elegans and other species. Proc Natl Acad Sci USA 98:14000-14005
62. Arora S, Anubhuti 2006 Role of neuropeptides in appetite regulation and obesity-a review. Neuropeptides 40:375-401
63. Kopin AS, Mathes WF, McBride EW, Nguyen M, Al-Haider W, Schmitz F, Bonner-Weir S, Kanarek R, Beinborn M 1999 The cholecystokinin-A receptor mediates inhibition of food intake yet is not essential for the maintenance of body weight. J Clin Invest 103:383-391
64. Downer KE, Nachman RJ, Stoffolano JG 2007 Factors affecting engorgement behavior in the salt marsh horse fly, Tabanus nigrovittatus macquart (Diptera: Tabanidae). J Insect Behav 20:403-412
65. Ashrafi K, Chang FY, Watts JL, Fraser AG, Kamath RS, Ahringer J, Ruvkun G 2003 Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421:268-272
66. Ashrafi K 2007 Obesity and the regulation of fat metabolism. In: The C. elegans research community. WormBook; 1-20
67. Kimura KD, Tissenbaum HA, Liu Y, Ruvkun G 1997 daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277:942-946
68. Mak HY, Nelson LS, Basson M, Johnson CD, Ruvkun G 2006 Polygenic control of Caenorhabditis elegans fat storage. Nat Genet 38:363-368
69. McKay RM, McKay JP, Avery L, Graff JM 2003 C. elegans: a model for exploring the genetics of fat storage. Dev Cell 4:131-142
70. Mukhopadhyay A, Deplancke B, Walhout AJ, Tissenbaum HA 2005 C. elegans tubby regulates life span and fat storage by two independent mechanisms. Cell Metab 2:35-42
71. Sze JY, Victor M, Loer C, Shi Y, Ruvkun G 2000 Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403:560-564
72. Janssen T, Husson SJ, Lindemans M, Mertens I, Rademakers S, Ver Donck K, Geysen J, Jansen G, Schoofs L 2007 Modulation of locomotor activity through PDF receptor signaling in Caenorhabditis elegans. J Biol Chem 10.1074/jbc.M709060200
73. Kubiak TM, Larsen MJ, Zantello MR, Bowman JW, Nulf SC, Lowery DE 2003 Functional annotation of the putative orphan Caenorhabditis elegans G-protein-coupled receptor C10C6.2 as a FLP15 peptide receptor. J Biol Chem 278:42115-42120
74. Kubiak TM, Larsen MJ, Nulf SC, Zantello MR, Burton KJ, Bowman JW, Modric T, Lowery DE 2003 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 278:33724-33729
75. Mertens I, Vandingenen A, Meeusen T, Janssen T, Luyten W, Nachman RJ, De Loof A, Schoofs L 2004 Functional characterization of the putative orphan neuropeptide G-protein coupled receptor C26F1.6 in Caenorhabditis elegans. FEBS Lett 573:55-60
76. Mertens I, Clinckspoor I, Janssen T, Nachman R, Schoofs L 2006 FMRFamide related peptide ligands activate the Caenorhabditis elegans orphan GPCR Y59H11AL. 1. Peptides 27:1291-1296
77. 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. Nat Neurosci 6:1178-1185
78. Lee RW, Huttner WB 1983 Tyrosine-O-sulfated proteins of PC12 pheochromocytoma cells and their sulfation by a tyrosylprotein sulfotransferase. J Biol Chem 258:11326-11334
79. Nachman RJ, Vercammen T, Williams H, Kaczmarek K, Zabrocki J, Schoofs L 2005 Aliphatic amino diacid Asu functions as an effective mimic of Tyr(SO3H) in sulfakinins for myotropic and food intake-inhibition activity in insects. Peptides 26:115-120
80. Andersen BN 1985 Species variation in the tyrosine sulfation of mammalian gastrins. Gen Comp Endocrinol 58:44-50
81. Barbaz BS, Autry WL, Ambrose FG, Hall NR, Liebman JM 1986 Antinociceptive profile of sulfated CCK-8. Comparison with CCK-4, unsulfated CCK-8 and other neuropeptides. Neuropharmacology 25:823-829
82. Bonetto V, Jornvall H, Andersson M, Renlund S, Mutt V, Sillard R 1999 Isolation and characterization of sulphated and nonsulphated forms of cholecystokinin-58 and their action on gallbladder contraction. Eur J Biochem 264:336-340
83. Carrasco M, Del Rio M, Hernanz A, De la Fuente M 1997 Inhibition of human neutrophil functions by sulfated and nonsulfated cholecystokinin octapeptides. Peptides 18:415-422
84. Maeda A, Akimoto M, Goto Y, Ogihara Y, Debas HT, Yamashiata K 2000 Reciprocal effect of unsulfated and sulfated forms of cholecystokinin- octapeptide on gastric acid secretion in the rat. Pharmacol Res 42:333-336
85. Reeve Jr JR, Liddle RA, McVey DC, Vigna SR, Solomon TE, Keire DA, Rosenquist G, Shively JE, Lee TD, Chew P, Green GM, Coskun T 2004 Identification of nonsulfated cholecystokinin-58 in canine intestinal extracts and its biological properties. Am J Physiol Gastrointest Liver Physiol 287:G326-G333
86. Dockray GJ, Varro A, Dimaline R, Wang T 2001 The gastrins: their production and biological activities. Annu Rev Physiol 63:119-139
87. Gregory RA, Tracey HJ 1964 The constitution and properties of two gastrins extracted from hog antral mucosa. Gut 5:103-114
88. Gregory RA, Tracey HJ 1964Anote on the nature of the gastrin-like stimulant present in Zollinger-Ellison tumours. Gut 5:115-117
89. Rehfeld JF 1998 The new biology of gastrointestinal hormones. Physiol Rev 78:1087-1108
90. Nichols R 2007 The first nonsulfated sulfakinin activity reported suggests nsDSK acts in gut biology. Peptides 28:767-773
91. Meldal BH, Debenham NJ, De Ley P, De Ley IT, Vanfleteren JR, Vierstraete AR, Bert W, Borgonie G, Moens T, Tyler PA, Austen MC, Blaxter ML, Rogers AD, Lambshead PJ 2007 An improved molecular phylogeny of the Nematoda with special emphasis on marine taxa. Mol Phylogenet Evol 42:622-636
92. Philip GK, Creevey CJ, McInerney JO 2005 The Opisthokonta and the Ecdysozoa may not be clades: stronger support for the grouping of plant and animal than for animal and fungi and stronger support for the Coelomata than Ecdysozoa. Mol Biol Evol 22:1175-1184
93. Wolf YI, Rogozin IB, Koonin EV 2004 Coelomata and not Ecdysozoa: evidence from genome-wide phylogenetic analysis. Genome Res 14:29-36
94. Driscoll M, Tavernarakis N 1997 Molecules that mediate touch transduction in the nematode Caenorhabditis elegans. Gravit Space Biol Bull 10:33-42
95. Wicks SR, Roehrig CJ, Rankin CH 1996 A dynamic network simulation of the nematode tap withdrawal circuit: predictions concerning synaptic function using behavioral criteria. J Neurosci 16:4017-4031
96. Fares H, Grant B 2002 Deciphering endocytosis in Caenorhabditis elegans. Traffic 3:11-19
97. Fares H, Greenwald I 2001 Genetic analysis of endocytosis in Caenorhabditis elegans: coelomocyte uptake defective mutants. Genetics 159:133-145
98. Paupard MC, Miller A, Grant B, Hirsh D, Hall DH 2001 Immuno-EM localization of GFP-tagged yolk proteins in C. elegans using microwave fixation. J Histochem Cytochem 49:949-956
99. Haselton AT, Yin CM, Stoffolano JG 2006 The effects of Calliphora vomitoria Tachykinin-I and the FMRFamide-related peptide Perisulfakinin on female Phormia regina crop contractions, in vitro. J Insect Physiol 52:436-441
100. Nachman RJ, Holman GM, Haddon WF, Hayes TK 1989 Structure-activity relationships for myotropic activity of the gastrin/cholecystokinin-like insect sulfakinins. Pept Res 2:171-177
101. Reinitz CA, Herfel HG, Messinger LA, Stretton AOW 2000 Changes in locomotory behavior and cAMP produced in Ascaris suum by neuropeptides from Ascaris suum or Caenorhabditis elegans. Mol Biochem Parasitol 111:185-197
102. Maule AG, Geary TG, Bowman JW, Marks NJ, Blair KL, Halton DW, Shaw C, Thompson DP 1995 Inhibitory effects of nematode FMRFamide-related peptides (FaRPs) on muscle strips from Ascaris suum. Invert Neurosci 1:255-265
103. Sieburth D, Ch'ng Q, Dybbs M, Tavazoie M, Kennedy S, Wang D, Dupuy D, Rual JF, Hill DE, Vidal M, Ruvkun G, Kaplan JM 2005 Systematic analysis of genes required for synapse structure and function. Nature 436:510-517
104. Rose C, Vargas F, Facchinetti P, Bourgeat P, Bambal RB, Bishop PB, Chan SMT, Moore ANJ, Ganellin CR, Schwartz JC 1996 Characterization and Inhibition of a cholecystokinin-inactivating serine peptidase. Nature 380:403-409
105. Sawin ER, Ranganathan R, Horvitz HR 2000 C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26:619-631
106. Chiang SH, MacDougald OA 2003 Will fatty worms help cure human obesity? Trends Genet 19:523-525