Expression and regulation of an FMRFamide-related neuropeptide gene family in Caenorhabditis elegans

Journal of Comparative Neurology

Volumn 475, Issue 4, 2004, Pages 540-550

  Kim, Kyuhyung ^a,c   Li, Chris ^a,b  

^a Boston University   (United States)

^b CITY COLLEGE OF NEW YORK   (United States)

^c BRANDEIS UNIVERSITY   (United States)

Author keywords

C. elegans; FaRPs; Flp; Mec 3

Indexed keywords

ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CELL SPECIFICITY; EMBRYO; EMBRYO DEVELOPMENT; FLP 20 GENE; FLP 23 GENE; FLP 4 GENE; FLP 8 GENE; FLP GENE; GENE; GENE CONTROL; GENE EXPRESSION; GENE MAPPING; MULTIGENE FAMILY; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CAENORHABDITIS ELEGANS; FEMALE; FMRFAMIDE; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HELMINTH; MALE; NEURONS; NEUROPEPTIDES; SEX FACTORS;

EID: 3042818433     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20189     Document Type: Article

References (85)

1. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, George RA, Lewis SE, Richards S, Ashburner M, Henderson SN, Sutton GG, Wortman JR, Yandell MD, Zhang Q, Chen LX, Brandon RC, Rogers YH, Blazej RG, Champe M, Pfeiffer BD, Wan KH, Doyle C, Baxter EG, Helt G, Nelson CR, Gabor GL, Abril JF, Agbayani A, An HJ, Andrews-Pfannkoch C, Baldwin D, Ballew RM, Basu A, Baxendale J, Bayraktaroglu L, Beasley EM, Beeson KY, Benos PV, Berman BP, Bhandari D, Bolshakov S, Borkova D, Botchan MR, Bouck J, Brokstein P, Brottier P, Burtis KC, Busam DA, Butler H, Cadieu E, Center A, Chandra I, Cherry JM, Cawley S, Dahlke C, Davenport LB, Davies P, de Pablos B, Delcher A, Deng Z, Mays AD, Dew I, Dietz SM, Dodson K, Doup LE, Downes M, Dugan-Rocha S, Dunkov BC, Dunn P, Durbin KJ, Evangelista CC, Ferraz C, Ferriera S, Fleischmann W, Fosler C, Gabrielian AE, Garg NS, Gelbart WM, Glasser K, Glodek A, Gong F, Gorrell JH, Gu Z, Guan P, Harris M, Harris NL, Harvey D, Heiman TJ, Hernandez JR, Houck J, Hostin D, Houston KA, Howland TJ, Wei MH, Ibegwam C, et al. 2000, The genome sequence of Drosophila melanogaster, Science 287: 2185-2195.
2. Albertson DG, Thomson JN. 1976. The pharynx of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 275:299-325.
3. Avery L, Horvitz HR. 1989. Pharyngeal pumping continues after laser killing of the pharyngeal nervous system of C. elegans. Neuron 3:473-485,
4. Bargmann CI, Horvitz HR, 1991. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 7:729-742.
5. Beck B, 2000. Neuropeptides and obesity. Nutrition 16:916-923.
6. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94.
7. Brownlee DJ, Fairweather I. 1999. Exploring the neurotransmitter labyrinth in nematodes. Trends Neurosci 22:16-24.
8. Cassada RC, Russell RL, 1975. The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Dev Biol 46: 326-342.
9. Chalfie M, Au M. 1989. Genetic control of differentiation of the Caenorhabditis elegans touch receptor neurons. Science 243:1027-1033.
10. Chalfie M, Sulston J. 1981. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev Biol 82:358-370.
11. Chalfie M, Sulston JE, White JG, Southgate E, Thomson JN, Brenner S. 1985. The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci 5:956-964.
12. Consortium C. elegans Sequencing. 1998. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282:2012-2018.
13. Cowden C, Stretton AO. 1993. AF2, an Ascaris neuropeptide: isolation, sequence, and bioactivity. Peptides 14:423-430.
14. Cowden C, Stretton AO. 1995. Eight novel FMRFamide-like neuropeptides isolated from the nematode Ascaris suum. Peptides 16:491-500.
15. Cowden C, Sithigorngul P, Brackley P, Guastella J, Stretton AO. 1993. Localization and differential expression of FMRFamide-like immunoreactivity in the nematode Ascaris suum. J Comp Neurol 333:455-468.
16. Davis R, Stretton A, 1996, The motornervous system of Ascaris: electrophysiology and anatomy of neurons and their control by neuromodulators. Parasitology 113:S97-S117.
17. Desai C, Garriga G, McIntire SL, Horvitz HR. 1988. A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature 336:638-646.
18. Duggan A, Ma C, Chalfie M. 1998. Regulation of touch receptor differentiation by the Caenorhabditis elegans mec-3 and unc-86 genes. Development 125:4107-4119.
19. Duret L, Guex N, Peitsch MC, Bairoch A. 1998, New insulin-like proteins with atypical disulfide bond pattern characterized in Caenorhabditis elegans by comparative sequence analysis and homology modeling. Genome Res 8:348-353.
20. Finney M, Ruvkun G. 1990. The unc86 gene product couples cell lineage and cell identity in C. elegans. Cell 63:895-905.
21. Geary, TG, Price DA, Bowman JW, Winterrowd, CA, Mackenzie CD, Garrison RD, Willliams JF, Friedman AR. 1992. Two FMRFamide-like peptides from the free-living nematode Panagrellus redivius. Peptides 13:209-214.
22. Gregoire FM, Chomiki N, Kachinskas D, Warden CH. 1998. Cloning and developmental regulation of a novel member of the insulin-like gene family in Caenorhabditis elegans. Biochem Biophys Res Commun 249; 385-390.
23. Hamelin M, Scott IM, Way JC, Culotti JG. 1992, The mec-7 beta-tubulin gene of Caenorhabditis elegans is expressed primarily in the touch receptor neurons. EMBO J 11:2885-2893.
24. Hinuma S, Shintani Y, Fukusumi S, Iijima N, Matsumoto Y, Hosoya M, Fujii R, Watanabe T, Kikuchi K, Terao Y, Yano T, Yamamoto T, Kawamata Y, Habata Y, Asada M, Kitada C, Kurokawa T, Onda H, Nishimura O, Tanaka M, Ibata Y, Fujino M. 2000. New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat Cell Biol 2:703-708.
25. Hobert O, Mori I, Yamashita Y, Honda H, Ohshima Y, Liu Y, Ruvkun G, 1997. Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron 19:345-357.
26. Hokfelt T, Broberger C, Xu ZQ, Sergeyev V, Ubink R, Diez M, 2000. Neuropeptides-an overview. Neuropharmacology 39:1337-1356.
27. Jansen G, Thijssen KL, Werner P, van der Horst M, Hazendonk E, Plasterk RH. 1999. The complete family of genes encoding G proteins of Caenorhabditis elegans. Nat Genet 21:414-419.
28. Jiang M, Ryu J, Kiraly M, Duke K, Reinke V, Kim SK. 2001. Genome-wide analysis of developmental and sex-regulated gene expression profiles in Caenorhabditis elegans. Proc Natl Acad Sci USA 98:218-223.
29. Jin Y, Hoskins R, Horvitz HR. 1994. Control of type-D GABAergic neuron differentiation by C. elegans UNC-30 homeodomain protein. Nature 372:780-783.
30. Joosten EA, Verhaagh S, Martin D, Robe P, Franzen R, Hooiveld M, Doornbos R, Bar PR, Moonen G. 1996, Alpha-MSH stimulates neurite outgrowth of neonatal rat corticospinal neurons in vitro. Brain Res 736:91-98.
31. Kavaliers M, Colwell DD. 1993. Neuropeptide FF (FLQPQRFamide) and IgG from neuropeptide FF antiserum affect spatial learning in mice, Neurosci Lett 157:75-78.
32. 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. Biochem Biophys Res Commun 273:431-436.
33. Kimber MJ, Fleming CC, Prior A, Jones JT, Halton DW, Maule AG. 2002. Localisation of Globodera pallida FMRFamide-related peptide encoding genes using in situ hybridisation. Int J Parasitol 32:1095-1105.
34. Klimaschewski L, Unsicker K, Heym C. 1995. Vasoactive intestinal peptide but not galanin promotes survival of neonatal rat sympathetic neurons and neurite outgrowth of PC12 cells. Neurosci Lett 195:133-136.
35. Kuhlman JR, Li C, Calabrese RL. 1985. FMRF-amide-like substances in the leech. II. Bioactivity on the heartbeat system. J Neurosci 5:2310-2317.
36. Lesser W, Greenberg MJ. 1993. Cardiac regulation by endogenous small cardioactive peptides and FMRFamide-related peptides in the snail Helix aspersa. J Exp Biol 178:205-230.
37. Li C, Kim K, Nelson LS. 1999a. FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. Brain Res 848:26-34.
38. Li C, Nelson LS, Kim K, Nathoo A, Hart AC. 1999b. Neuropeptide gene families in the nematode Caenorhabditis elegans. Ann NY Acad Sci 897:239-252.
39. Lickteig KM, Duerr JS, Fisby DL, Hall DH, Rand JB, Miller DM. 2001. Regulation of neurotransmitter vesicles by the homeodomain protein UNC-4 and its transcriptional corepressor UNC-37/Groucho in Caenorhabditis elegans cholinergic motor neurons. J Neurosci 21:2001-2014.
40. Liu KS, Sternberg PW. 1995. Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 14:79-89.
41. Liu Q, Guan XM, Martin WJ, McDonald TP, Clements MK, Jiang Q, Zeng Z, Jacobson M, Williams DL, Jr., Yu H, Bomford D, Figueroa D, Mallee J, Wang R, Evans J, Gould R, Austin CP. 2001. Identification and characterization of novel mammalian neuropeptide FF-like peptides that attenuate morphine-induced antinociception. J Biol Chem 276: 36961-36969.
42. Loer CM, Kenyon CJ. 1993. Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans. J Neurosci 13:5407-5417.
43. Mackey SL, Glanzman DL, Small SA, Dyke AM, Kandel ER, Hawkins RD. 1987. Tail shock produces inhibition as well as sensitization of the siphon-withdrawal reflex of Aplysia: possible behavioral role for presynaptic inhibition mediated by the peptide Phe-Met-Arg-Phe-NH2. Proc Natl Acad Sci USA 84:8730-8734.
44. Majane EA, Panula P, Yang HY. 1989. Rat brain regional distribution and spinal cord neuronal pathway of FLFQPQRF-NH2, a mammalian FMRF-NH2-like peptide. Brain Res 494:1-12.
45. Marks NJ, Shaw C, Maule AG, Davis JP, Halton DW, Verhaert P, Geary TG, Thompson DP. 1995. Isolation of AF2 (KHEYLRFamide) from Caenorhabditis elegans: evidence for the presence of more than one FMRFamide-related peptide-encoding gene. Biochem Biophys Res Commun 217:845-851.
46. Marks NJ, Maule AG, Geary TG, Thompson DP, Davis JP, Halton DW, Verhaert P, Shaw C. 1997. APEASPFIRFamide, a novel FMRFamide-related decapeptide from Caenorhabditis elegans: structure and myoactivity. Biochem Biophys Res Commun 231:591-595.
47. Marks NJ, Maule AG, Geary TG, Thompson DP, Li C, Halton DW, Shaw C. 1998. KSAYMRFamide (PF3/AF8) is present in the free-living nematode, Caenorhabditis elegans. Biochem Biophys Res Commun 248:422-425.
48. Marks NJ, Maule AG, Li C, Nelson LS, Thompson DP, Alexander-Bowman S, Geary TG, Halton DW, Verhaert P, Shaw C. 1999a. Isolation, pharmacology and gene organization of KPSFVRFamide: a neuropeptide from Caenorhabditis elegans. Biochem Biophys Res Commun 254:222-230.
49. Marks NJ, Sangster NC, Maule AG, D.W. Halton DW, D.P. Thompson DP, Shaw C. 1999b. Structural characterisation and pharmacology of KHEYLRFamide (AF2) and KSAYMRFamide (PF3/AF8) from Haemonchus contortus. Mol Biochem Parasitol 100:185-194.
50. Marks NJ, Shaw C, Halton DW, Thompson DP, Geary TG, Li C, Maule AG. 2001. Isolation and preliminary biological assessment of AADGAPLIRFamide and SVPGVLRFamide from Caenorhabditis elegans. Biochem Biophys Res Commun 286:1170-1176.
51. Maule AG, Shaw C, Bowman JW, Halton DW, Thompson DP, Geary TG, Thim L. 1994. The FMRFamide-like neuropeptide AF2 (Ascaris suum) is present in the free-living nematode, Panagrellus redivivus (Nematoda: Rhabditia). Parasitology 109:351-356.
52. 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.
53. McIntire SL, Jorgensen E, Kaplan J, Horvitz HR. 1993. The GABAergic nervous system of Caenorhabditis elegans. Nature 364:337-341.
54. Mello C, Fire A. 1995. DNA transformation. Methods Cell Biol 48:451-482.
55. Mitani S, Du H, Hall DH, Driscoll M, Chalfie M. 1993. Combinatorial control of touch receptor neuron expression in Caenorhabditis elegans. Development 119:773-783.
56. Nelson LS, Kim K, Memmott JE, Li C. 1998a. FMRFamide-related gene family in the nematode, Caenorhabditis elegans. Brain Res Mol Brain Res 58:103-111.
57. Nelson LS, Rosoff ML, Li C. 1998b. Disruption of a neuropeptide gene, flp-1, causes multiple behavioral defects in Caenorhabditis elegans. Science 281:1686-1690.
58. O'Brien MA, Schneider LE, Taghert PH. 1991. In situ hybridization analysis of the FMRFamide neuropeptide gene in Drosophila. II. Constancy in the cellular pattern of expression during metamorphosis. J Comp Neurol 304:623-638.
59. Panula P, Kalso E, Nieminen M, Kontinen VK, Brandt A, Pertovaara A. 1999. Neuropeptide FF and modulation of pain. Brain Res 848:191-196.
60. Perkins LA, Hedgecock EM, Thomson JN, Culotti JG. 1986. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol 117:456-487.
61. Price D, Greenberg M. 1977. The structure of a molluscan cardioexcitatory neuropeptide. Science 197:670-671.
62. 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.
63. Rosoff ML, Burglin TR, Li C. 1992. Alternatively spliced transcripts of the flp-1 gene encode distinct FMRFamide-like peptides in Caenorhabditis elegans. J Neurosci 12:2356-2361.
64. Rosoff ML, Doble KE, Price DA, Li C. 1993. The flp-1 propeptide is processed into multiple, highly similar FMRFamide-like peptides in Caenorhabditis elegans. Peptides 14:331-338.
65. Schinkmann K, Li C. 1992. Localization of FMRFamide-like peptides in Caenorhabditis elegans. J Comp Neurol 316:251-260.
66. Schneider LE, Roberts MS, Taghert PH. 1993a. Cell type-specific transcriptional regulation of the Drosophila FMRFamide neuropeptide gene. Neuron 10:279-291.
67. Schneider LE, Sun ET, Garland DJ, Taghert PH. 1993b. An immunocytochemical study of the FMRFamide neuropeptide gene products in Drosophila. J Comp Neurol 337:446-460.
68. Schwartz JP, Ji Z, Epelbaum J. 1998. Somatostatin as a neurotrophic factor. Which receptor/second messenger transduction system is involved? Perspect Dev Neurobiol 5:427-435.
69. Small SA, Kandel ER, Hawkins RD. 1989. Activity-dependent enhancement of presynaptic inhibition in Aplysia sensory neurons. Science 243:1603-1606.
70. Strand FL. 1999. Neuropeptides. Cambridge, MA: MIT Press.
71. Sulston JE, Albertson DG, Thomson JN. 1980. The Caenorhabditis elegans male: postembryonic development of nongonadal structures. Dev Biol 78:542-576.
72. 2 immunoreactivity. Proc Natl Acad Sci USA 81:5002-5005.
73. Trent C, Tsung N, Horvitz H. 1983. Egg-laying defective mutants of the nematode Caenorhabditis elegans. Genetics 104:619-647.
74. Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI. 1995. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83:207-218.
75. Vilim FS, Aarnisalo AA, Nieminen ML, Lintunen M, Karlstedt K, Kontinen VK, Kalso E, States B, Panula P, ZiffE. 1999. Gene for pain modulatory neuropeptide NPFF: induction in spinal cord by noxious stimuli. Mol Pharmacol 55:804-811.
76. Waggoner LE, Hardaker LA, Golik S, Schafer WR. 2000. Effect of a neuropeptide gene on behavioral states in Caenorhabditis elegans egglaying. Genetics 154:1181-1192.
77. Way JC, Chalfie M. 1988. mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans. Cell 54:5-16.
78. Weinshenker D, Garriga G, Thomas JH. 1995. Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans. J Neurosci 15:6975-6985.
79. White J, Southgate E, Thomson J, Brenner S. 1986. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond 314:1-340.
80. Wong TM, Greenberg MJ, Tse SY. 1985. Cardiovascular effects of intraventricular injection of FMRFamide, Met-enkephalin and their common analogues in the rat. Comp Biochem Physiol C 81:175-179.
81. Wood, WD, The nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1988.
82. Xue D, Tu Y, Chalfie M. 1993. Cooperative interactions between the Caenorhabditis elegans homeoproteins UNC-86 and MEC-3. Science 261: 1324-1328.
83. Yang, H-YT, Fratta W, Majane EA, Costa E. 1985. Isolation, sequencing, synthesis and pharmacological characterization of two brain neuropeptides that modulate the action of morphine. Proc Natl Acad Sci USA 82:7757-7761.
84. Yu S, Avery L, Baude E, Garbers DL. 1997. Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors. Proc Natl Acad Sci USA 94:3384-3387.
85. Zhang Y, Ma C, Delohery T, Nasipak B, Foat BC, Bounoutas A, Bussemaker HJ, Kim SK, Chalfie M. 2002. Identification of genes expressed in C. elegans touch receptor neurons. Nature 418:331-335.