Long chain polyunsaturated fatty acids are required for efficient neurotransmission in C. elegans

Journal of Cell Science

Volumn 116, Issue 24, 2003, Pages 4965-4975

  Lesa, Giovanni M ^a,f   Palfreyman, Mark ^b   Hall, David H ^c   Clandinin, M Thomas ^d   Rudolph, Claudia ^e   Jorgensen, Erik M ^b   Schiavo, Giampietro ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b UNIVERSITY OF UTAH   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF ALBERTA   (Canada)

^e EleGene AG   (Germany)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

C. elegans; Neuromuscular junction; Neurotransmitter release; Polyunsaturated fatty acids; Synapse

Indexed keywords

LINOLEOYL COENZYME A DESATURASE; LONG CHAIN FATTY ACID; NEUROTRANSMITTER; POLYUNSATURATED FATTY ACID;

ARTICLE; CAENORHABDITIS ELEGANS; CELL MEMBRANE; CELL TYPE; CONTROLLED STUDY; FATTY ACID METABOLISM; FATTY ACID SYNTHESIS; GENE EXPRESSION; GENETIC CODE; GENOME; LIPID COMPOSITION; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SYNAPSE VESICLE;

AMINO ACID SEQUENCE; ANIMALS; CADHERINS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; ELECTROPHYSIOLOGY; EPIDERMAL GROWTH FACTOR; FATTY ACIDS, UNSATURATED; MENTAL DISORDERS; MOLECULAR SEQUENCE DATA; NERVOUS SYSTEM PHYSIOLOGY; NEUROMUSCULAR JUNCTION; NEUROTRANSMITTER AGENTS; RECEPTORS, CHOLINERGIC; RECEPTORS, SEROTONIN, 5-HT1; SEQUENCE HOMOLOGY, AMINO ACID; SYNAPTIC VESICLES;

ANIMALIA; CAENORHABDITIS ELEGANS; EUKARYOTA; INVERTEBRATA; NEMATODA;

EID: 0346882605     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00918     Document Type: Article

References (43)

1. Anderson, J. W., Johnstone, B. M. and Remley, D. T. (1999). Breast-feeding and cognitive development: a meta-analysis. Am. J. Clin. Nutr. 70, 525-535.
2. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
3. Chomczynski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
4. Connor, W. E. and Neuringer, M. (1988). The effects of n-3 fatty acid deficiency and repletion upon the fatty acid composition and function of the brain and retina. Prog. Clin. Biol. Res. 282, 275-294.
5. Desai, C. and Horvitz, H. R. (1989). Caenorhabditis elegans mutants defective in the functioning of the motor neurons responsible for egg laying. Genetics 121, 703-721.
6. Frohnert, B. I. and Bernlohr, D. A. (2000). Regulation of fatty acid transporters in mammalian cells. Prog. Lipid Res. 39, 83-107.
7. Fukushige, T., Hawkins, M. G. and McGhee, J. D. (1998). The GATA-factor elt-2 is essential for formation of the Caenorhabditis elegans intestine. Dev. Biol. 198, 286-302.
8. Hall, D. H. (1995). Electron microscopy and three-dimensional image reconstruction. Methods Cell Biol. 48, 395-436.
9. Hargreaves, K. M. and Clandinin, M. T. (1988). Dietary control of diacylphosphatidylethanolamine species in brain. Biochim. Biophys. Acta 962, 98-104.
10. Harris, T. W., Hartwieg, E., Horvitz, H. R. and Jorgensen, E. M. (2000). Mutations in synaptojanin disrupt synaptic vesicle recycling. J. Cell Biol. 150, 589-600.
11. Helland, I. B., Smith, L., Saarem, K., Saugstad, O. D. and Drevon, C. A. (2003). Maternal supplementation with very-long-chain n-3 fatty acids during pregnancy and lactation augments children's IQ at 4 years of age. Pediatrics 111, e39-e44.
12. Hyttel, J. (1994). Pharmacological characterization of selective serotonin reuptake inhibitors (SSRIs). Int. Clin. Psychopharmacol. 9 Supplement 1, 19-26.
13. Jansen, G., Hazendonk, E., Thijssen, K. L. and Plasterk, R. H. (1997). Reverse genetics by chemical mutagenesis in Caenorhabditis elegans. Nature Genet. 17, 119-121.
14. Jorgensen, E. M., Hartwieg, E., Schuske, K., Nonet, M. L., Jin, Y. and Horvitz, H. R. (1995). Defective recycling of synaptic vesicles in synaptotagmin mutants of Caenorhabditis elegans. Nature 378, 196-199.
15. Lackner, M. R., Nurrish, S. J. and Kaplan, J. M. (1999). Facilitation of synaptic transmission by EGL-30 Gqα and EGL-8 PLCβ: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron 24, 335-346.
16. Lauritzen, L., Hansen, H. S., Jorgensen, M. H. and Michaelsen, K. F. (2001). The essentiality of long chain n-3 fatty acids in relation to development and function of the brain and retina. Prog. Lipid Res. 40, 1-94.
17. Los, D. A. and Murata, N. (1998). Structure and expression of fatty acid desaturases. Biochim. Biophys. Acta 1394, 3-15.
18. Maduro, M. and Pilgrim, D. (1995). Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 141, 977-988.
19. Martinez, M., Vazquez, E., Garcia-Silva, M. T., Manzanares, J., Bertran, J. M., Castello, F. and Mougan, I. (2000). Therapeutic effects of docosahexaenoic acid ethyl ester in patients with generalized peroxisomal disorders. Am. J. Clin. Nutr. 71, 376S-385S.
20. McDonald, K. (1999). High-pressure freezing for preservation of high resolution fine structure and antigenicity for immunolabeling. Methods Mol. Biol. 117, 77-97.
21. Mello, C. C., Kramer, J. M., Stinchcomb, D. and Ambros, V. (1991). Efficient gene transfer in C. elegans after microinjection of DNA into germline cytoplasm: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970.
22. Meloni, I., Muscettola, M., Raynaud, M., Longo, L, Bruttini, M., Moizard, M. P., Gomot, M., Chelly, J., des Portes, V., Fryns, J. P. et al. (2002). FACL4, encoding fatty acid-CoA ligase 4, is mutated in nonspecific X-linked mental retardation. Nature Genet. 30, 436-440.
23. Miller, K. G., Emerson, M. D. and Rand, J. B. (1999). Goα and diacylglycerol kinase negatively regulate the Gqα pathway in C. elegans. Neuron 24, 323-333.
24. Nakamura, M. T., Cho, H. P., Xu, J., Tang, Z. and Clarke, S. D. (2001). Metabolism and functions of highly unsaturated fatty acids: an update. Lipids 36, 961-964.
25. Napier, J. A., Hey, S. J., Lacey, D. J. and Shewry, P. R. (1998). Identification of a Coenorhabditis elegans Δ6-fatty-acid-desaturase by heterologous expression in Saccharomyces cerevisiae. Biochem. J. 330, 611-614.
26. Napier, J. A., Michaelson, L. V. and Stobart, A. K. (1999). Plant desaturases: harvesting the fat of the land. Curr. Opin. Plant Biol. 2, 123-127.
27. Nonet, M. L., Grundahl, K., Meyer, B. J. and Rand, J. B. (1993). Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73, 1291-1305.
28. Nonet, M. L., Saifee, O., Zhao, H., Rand, J. B. and Wei, L. (1998). Synaptic transmission deficits in Caenorhabditis elegans synaptobrevin mutants. J. Neurosci. 18, 70-80.
29. Nonet, M. L., Staunton, J. E., Kilgard, M. P., Fergestad, T., Hartwieg, E., Horvitz, H. R., Jorgensen, E. M. and Meyer, B. J. (1997). Caenorhabditis elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles. J. Neurosci. 17, 8061-8073.
30. Richmond, J. E., Davis, W. S. and Jorgensen, E. M. (1999). UNC-13 is required for synaptic vesicle fusion in C. elegans. Nat. Neurosci. 2, 959-964.
31. Richmond, J. E. and Jorgensen, E. M. (1999). One GABA and two acetylcholine receptors function at the C. elegans neuromuscular junction. Nat. Neurosci. 2, 791-797.
32. Sayanova, O., Shewry, P. R. and Napier, J. A. (1999). Histidine-41 of the cytochrome b5 domain of the borage delta6 fatty acid desaturase is essential for enzyme activity. Plant Physiol. 121, 641-646.
33. Sharon, R., Bar-Joseph, I., Frosch, M. P., Walsh, D. M., Hamilton, J. A. and Selkoe, D. J. (2003). The formation of highly soluble oligomers of alpha-synuclein is regulated by fatty acids and enhanced in Parkinson's disease. Neuron 37, 583-595.
34. Spychalla, J. P., Kinney, A. J. and Browse, J. (1997). Identification of an animal omega-3 fatty acid desaturase by heterologous expression in Arabidopsis. Proc. Natl Acad. Sci. USA 94, 1142-1147.
35. Sze, J. Y., Victor, M., Loer, C., Shi, Y. and Ruvkun, G. (2000). Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403, 560-564.
36. Trent, C., Tsung, N. and Horvitz, H. R. (1983). Egg-laying defective mutants of the nematode Caenorhabditis elegans. Genetics 104, 619-647.
37. Wallis, J. G., Watts, J. L. and Browse, J. (2002). Polyunsaturated fatty acid synthesis: what will they think of next? Trends Biochem. Sci. 27, 467-473.
38. Watts, J. L. and Browse, J. (2002). Genetic dissection of polyunsaturated fatty acid synthesis in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 99, 5854-5859.
39. Watts, J. L., Phillips, E., Griffing, K. R. and Browse, J. (2003). Deficiencies in C20 polyunsaturated fatty acids cause behavioral and developmental defects in Caenorhabditis elegansfat-3 mutants. Genetics 163, 581-589.
40. Weinshenker, D., Garriga, G. and Thomas, J. H. (1995). Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans. J. Neurosci. 15, 6975-6985.
41. Weisinger, H. S., Vingrys, A. J., Bui, B. V. and Sinclair, A. J. (1999). Effects of dietary n-3 fatty acid deficiency and repletion in the guinea pig retina. Invest. Ophthalmol. Vis. Sci. 40, 327-338.
42. Willatts, P., Forsyth, J. S., DiModugno, M. K., Varma, S. and Colvin, M. (1998). Effect of long-chain polyunsaturated fatty acids in infant formula on problem solving at 10 months of age. Lancet 352, 688-691.
43. Zhang, K., Kniazeva, M., Han, M., Li, W., Yu, Z., Yang, Z., Li, Y., Metzker, M. L., Allikmets, R., Zack, D. J. et al. (2001). A 5-bp deletion in ELOVL4 is associated with two related forms of autosomal dominant macular dystrophy. Nature Genet. 27, 89-93.