Lack of dietary polyunsaturated fatty acids causes synapse dysfunction in the Drosophila visual system

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Ziegler, Anna B ^a   Ménagé, Cindy ^a   Grégoire, Stéphane ^a   Garcia, Thibault ^a   Ferveur, Jean François ^a   Bretillon, Lionel ^a   Grosjean, Yael ^a  

^a CENTRE DES SCIENCES DU GOÛT ET DE L ALIMENTATION   (France)

Author keywords

[No Author keywords available]

Indexed keywords

OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; POLYUNSATURATED FATTY ACID; FAT INTAKE; UNSATURATED FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; DROSOPHILA MELANOGASTER; ELECTRORETINOGRAM; ESSENTIAL FATTY ACID DEFICIENCY; FAT INTAKE; HEAD; LIPID COMPOSITION; MALE; NONHUMAN; PHOTORECEPTOR; PHOTOTAXIS; SYNAPSE; SYNAPTIC TRANSMISSION; VISUAL SYSTEM; ANIMAL; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; PHARMACOLOGY; PHYSIOLOGY; VISION;

ANIMALS; DIETARY FATS; DOSE-RESPONSE RELATIONSHIP, DRUG; DROSOPHILA MELANOGASTER; FATTY ACIDS, UNSATURATED; SYNAPSES; SYNAPTIC TRANSMISSION; VISUAL PERCEPTION;

EID: 84943196427     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0135353     Document Type: Article

References (72)

1. Yehuda S, Rabinovitz S, Mostofsky DI. Essential fatty acids are mediators of brain biochemistry and cognitive functions. J Neurosci Res. 1999;56:565-570. doi: 10.1002/(SICI) 1097-4547 (19990615) 56:6<565::AID-JNR2>3.0. CO;2-H PMID: 10374811
2. Ross BM. a-3 Fatty acid deficiency in major depressive disorder is caused by the interaction between diet and a genetically determined abnormality in phospholipid metabolism. Med Hypotheses. 2007;68:515-524. doi: 10.1016/j.mehy.2006.07.054 PMID: 17045757
3. Meloni I, Muscettola M, Raynaud M, Longo I, Bruttini M, Moizard M-P, et al. FACL4, encoding fatty acid-CoA ligase 4, is mutated in nonspecific X-linked mental retardation. Nat Genet. 2002;30:436-440. doi: 10.1038/ng857 PMID: 11889465
4. Covault J, Pettinati H, Moak D, Mueller T, Kranzler HR. Association of a long-chain fatty acid-CoA ligase 4 gene polymorphism with depression and with enhanced niacin-induced dermal erythema. Am J Med Genet B Neuropsychiatr Genet. 2004;127B:42-47. doi: 10.1002/ajmg.b.20156 PMID: 15108178
5. Tanaka K, Farooqui AA, Siddiqi NJ, Alhomida AS, Ong W-Y. Effects of docosahexaenoic Acid on neurotransmission. Biomol Ther (Seoul). 2012;20:152-7. doi: 10.4062/biomolther.2012.20.2.152
6. Marza E, Lesa GM. Polyunsaturated fatty acids and neurotransmission in Caenorhabditis elegans. Biochem Soc Trans. 2006;34:77-80. doi: 10.1042/BST0340077 PMID: 16417487
7. Mathieu G, Géraldine M, Denis S, Stéphanie D, Langelier B, Bénédicte L, et al. DHA enhances the noradrenaline release by SH-SY5Y cells. Neurochem Int. 2010;56:94-100. doi: 10.1016/j.neuint.2009. 09.006 PMID: 19770016
8. Bazinet RP, Layé S. Polyunsaturated fatty acids and their metabolites in brain function and disease. Nat Rev Neurosci. 2014;15:771-85. doi: 10.1038/nrn3820 PMID: 25387473
9. Dacks PA, Shineman DW, Fillit HM. Current evidence for the clinical use of long-chain polyunsaturated n-3 fatty acids to prevent age-related cognitive decline and Alzheimer's disease. J Nutr Health Aging. 2013;17:240-51. doi: 10.1007/s12603-012-0431-3 PMID: 23459977
10. Merle BMJ, Delyfer M-N, Korobelnik J-F, Rougier M-B, Malet F, Féart C, et al. High concentrations of plasma n3 fatty acids are associated with decreased risk for late age-related macular degeneration. J Nutr. 2013;143:505-11. doi: 10.3945/jn. 112.171033 PMID: 23406618
11. Galli C, Risé P. Origin of fatty acids in the body: endogenous synthesisversus dietary intakes. Eur J Lipid Sci Technol. 2006;108:521-525. doi: 10.1002/ejlt.200600056
12. Visioli F, Crawford MA, Cunnane S, Rise P, Galli C. Lipid transport, dietary fats, and endogenous lipid synthesis: hypotheses on saturation and competition processes. Nutr Health. 2006;18:127-32. doi: 10.1177/026010600601800204 PMID: 16859175
13. Hibbeln JR, Gow R V. The Potential for Military Diets to Reduce Depression, Suicide, and Impulsive Aggression: A Review of Current Evidence for Omega-3 and Omega-6 Fatty Acids. Mil Med. 2014;179:117-128. doi: 10.7205/MILMED-D-14-00153 PMID: 25373095
14. Hibbeln JR. Depression, suicide and deficiencies of omega-3 essential fatty acids in modern diets. World Rev Nutr Diet. 2009;99:17-30. doi: 10.1159/000192992 PMID: 19136836
15. Chong EW-T, Kreis AJ, Wong TY, Simpson JA, Guymer RH. Dietary omega-3 fatty acid and fish intake in the primary prevention of age-related macular degeneration: a systematic review and meta-analysis. Arch Ophthalmol (Chicago, Ill 1960). 2008;126:826-33. doi: 10.1001/archopht.126.6.826
16. Papadimitriou GN, Dikeos DG, Souery D, Del-Favero J, Massat I, Avramopoulos D, et al. Genetic association between the phospholipase A2 gene and unipolar affective disorder: a multicentre case-control study. Psychiatr Genet. 2003;13:211-20. doi: 10.1097/01.ypg.0000084945.07075.ec PMID: 14639048
17. Pae C-U, Yu H-S, Kim J-J, Lee C-U, Lee S-J, Lee K-U, et al. BanI polymorphism of the cytosolic phospholipase A2 gene and mood disorders in the Korean population. Neuropsychobiology. 2004;49:185-8. doi: 10.1159/000077364 PMID: 15118355
18. Parvy J-P, Napal L, Rubin T, Poidevin M, Perrin L, Wicker-Thomas C, et al. Drosophila melanogaster Acetyl-CoA-carboxylase sustains a fatty acid-dependent remote signal to waterproof the respiratory system. PLoS Genet. 2012;8:e1002925. doi: 10.1371/journal.pgen. 1002925 PMID: 22956916
19. Dallerac R, Labeur C, Jallon JM, Knipple DC, Roelofs WL, Wicker-Thomas C. A delta 9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster. Proc Natl Acad Sci U S A. 2000;97:9449-54. doi: 10.1073/pnas. 150243997 PMID: 10920187
20. Wicker-Thomas C, Henriet C, Dallerac R. Partial characterization of a fatty acid desaturase gene in Drosophila melanogaster. Insect Biochem Mol Biol. 1997;27:963-72. doi: 10.1016/S0965-1748 (97) 00077-5 PMID: 9501419
21. Vrablik TL, Watts JL. Polyunsaturated fatty acid derived signaling in reproduction and development: insights from Caenorhabditis elegans and Drosophila melanogaster. Mol Reprod Dev. 2013;80:244-59. doi: 10.1002/mrd.22167 PMID: 23440886
22. Stark WS, Lin TN, Brackhahn D, Christianson JS, Sun GY. Fatty acids in the lipids of Drosophila heads: effects of visual mutants, carotenoid deprivation and dietary fatty acids. Lipids. 1993;28:345-50. doi: 10.1007/BF02536321 PMID: 8487627
23. Shen LR, Lai CQ, Feng X, Parnell LD, Wan JB, Wang JD, et al. Drosophila lacks C20 and C22 PUFAs. J Lipid Res. 2010;51:2985-92. doi: 10.1194/jlr. M008524 PMID: 20656917
24. Fougeron A-S, Farine J-P, Flaven-Pouchon J, Everaerts C, Ferveur J-F. Fatty-acid preference changes during development in Drosophila melanogaster. PLoS One. 2011;6:e26899. doi: 10.1371/journal. pone.0026899 PMID: 22046401
25. Chang CL, Coudron TA, Goodman C, Stanley D, An S, Song Q. Wheat germ oil in larval diet influences gene expression in adult oriental fruit fly. J Insect Physiol. 2010;56:356-65. doi: 10.1016/j.jinsphys. 2009.11.014 PMID: 19932112
26. Wang T, Jiao Y, Montell C. Dissection of the pathway required for generation of vitamin A and for Drosophila phototransduction. J Cell Biol. 2007;177:305-16. doi: 10.1083/jcb.200610081 PMID: 17452532
27. Benzer S. Behaviolral Mutants Of Drosophila Isolated By Countercurrent Distribution. Proc Natl Acad Sci U S A. 1967;58:1112-9. doi: 10.1073/pnas.58.3.1112 PMID: 16578662
28. True JR, Yeh S-D, Hovemann BT, Kemme T, Meinertzhagen IA, Edwards TN, et al. Drosophila tan encodes a novel hydrolase required in pigmentation and vision. PLoS Genet. 2005;1:e63. doi: 10. 1371/journal.pgen. 0010063 PMID: 16299587
29. Ziegler AB, Brüsselbach F, Hovemann BT. Activity and coexpression of Drosophila black with ebony in fly optic lobes reveals putative cooperative tasks in vision that evade electroretinographic detection. J Comp Neurol. 2013;521:1207-24. doi: 10.1002/cne.23247 PMID: 23124681
30. Savarit F, Sureau G, Cobb M, Ferveur JF. Genetic elimination of known pheromones reveals the fundamental chemical bases of mating and isolation in Drosophila. Proc Natl Acad Sci U S A. 1999;96:9015-20. doi: 10.1073/pnas.96.16.9015 PMID: 10430887
31. Folch J, Lees M, Sloane, Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226:497-509. PMID: 13428781
32. Morrison WR, Smith LM. Preparation of Fatty Acid Methyl Esters and Dimethylacetals from Lipids With Boron Fluoride-Methanol. J Lipid Res. 1964;5:600-8. PMID: 14221106
33. Heisenberg M. Separation of receptor and lamina potentials in the electroretinogram of normal and mutant Drosophila. J Exp Biol. 1971;55:85-100. PMID: 5001616
34. Hotta Y, Benzer S. Abnormal electroretinograms in visual mutants of Drosophila. Nature. 1969;222:354-6. Available: http://www.ncbi.nlm.nih.gov/pubmed/5782111. PMID: 5782111
35. Bloomquist BT, Shortridge RD, Schneuwly S, Perdew M, Montell C, Steller H, et al. Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell. 1988;54:723-33. doi: 10.1016/S0092-8674 (88) 80017-5 PMID: 2457447
36. Montell C, Rubin GM. Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron. 1989;2:1313-23. doi: 10.1016/0896-6273 (89) 90069-X PMID: 2516726
37. Hardie RC, Minke B. The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors. Neuron. 1992;8:643-51. doi: 10.1016/0896-6273 (92) 90086-S PMID: 1314617
38. Niemeyer BA, Suzuki E, Scott K, Jalink K, Zuker CS. The Drosophila light-activated conductance is composed of the two channels TRP and TRPL. Cell. 1996;85:651-9. doi: 10.1016/S0092-8674 (00) 81232-5 PMID: 8646774
39. Phillips AM, Bull A, Kelly LE. Identification of a Drosophila gene encoding a calmodulin-binding protein with homology to the trp phototransduction gene. Neuron. 1992;8:631-42. doi: 10.1016/0896-6273 (92) 90085-R PMID: 1314616
40. Montell C, Jones K, Hafen E, Rubin G. Rescue of the Drosophila phototransduction mutation trp by germline transformation. Science. 1985;230:1040-3. PMID: 3933112
41. Huang J, Liu C-H, Hughes SA, Postma M, Schwiening CJ, Hardie RC. Activation of TRP channels by protons and phosphoinositide depletion in Drosophila photoreceptors. Curr Biol. 2010;20:189-97. doi: 10.1016/j.cub.2009.12.019 PMID: 20116246
42. Acharya JK, Jalink K, Hardy RW, Hartenstein V, Zuker CS. InsP3 receptor is essential for growth and differentiation but not for vision in Drosophila. Neuron. 1997;18:881-7. doi: 10.1016/S0896-6273 (00) 80328-1 PMID: 9208856
43. Raghu P, Colley NJ, Webel R, James T, Hasan G, Danin M, et al. Normal phototransduction in Drosophila photoreceptors lacking an InsP (3) receptor gene. Mol Cell Neurosci. 2000;15:429-45. doi: 10. 1006/mcne.2000.0846 PMID: 10833300
44. Hardie RC, Raghu P. Activation of heterologously expressed Drosophila TRPL channels: Ca2+ is not required and InsP3 is not sufficient. Cell Calcium. 1998;24:153-63. doi: 10.1016/S0143-4160 (98) 90125-7 PMID: 9883270
45. Chyb S, Raghu P, Hardie RC. Polyunsaturated fatty acids activate the Drosophila light-sensitive channels TRP and TRPL. Nature. 1999;397:255-9. doi: 10.1038/16703 PMID: 9930700
46. Delgado R, Muñoz Y, Peña-Cortés H, Giavalisco P, Bacigalupo J. Diacylglycerol activates the lightdependent channel TRP in the photosensitive microvilli of Drosophila melanogaster photoreceptors. J Neurosci. 2014;34:6679-86. doi: 10.1523/JNEUROSCI.0513-14.2014 PMID: 24806693
47. Delgado R, Bacigalupo J. Unitary recordings of TRP and TRPL channels from isolated Drosophila retinal photoreceptor rhabdomeres: activation by light and lipids. J Neurophysiol. 2009;101:2372-9. doi: 10.1152/jn. 90578.2008 PMID: 19261713
48. Leung H-T, Tseng-Crank J, Kim E, Mahapatra C, Shino S, Zhou Y, et al. DAG lipase activity is necessary for TRP channel regulation in Drosophila photoreceptors. Neuron. 2008;58:884-96. doi: 10.1016/j.neuron. 2008.05.001 PMID: 18579079
49. Estacion M, Sinkins WG, Schilling WP. Regulation of Drosophila transient receptor potential-like (TrpL) channels by phospholipase C-dependent mechanisms. J Physiol. 2001;530:1-19. doi: 10.1007/s00424-007-0275-6 PMID: 11136854
50. Borycz J, Borycz JA, Loubani M, Meinertzhagen IA. tan and ebony genes regulate a novel pathway for transmitter metabolism at fly photoreceptor terminals. J Neurosci. 2002;22:10549-57. PMID: 12486147
51. Burg MG, Sarthy P V, Koliantz G, Pak WL. Genetic and molecular identification of a Drosophila histidine decarboxylase gene required in photoreceptor transmitter synthesis. EMBO J. 1993;12:911-9. PMID: 8096176
52. Gisselmann G, Pusch H, Hovemann BT, Hatt H. Two cDNAs coding for histamine-gated ion channels in D. melanogaster. Nat Neurosci. 2002;5:11-2. doi: 10.1038/nn787 PMID: 11753412
53. Witte I, Kreienkamp H-J, Gewecke M, Roeder T. Putative histamine-gated chloride channel subunits of the insect visual system and thoracic ganglion. J Neurochem. 2002;83:504-14. doi: 10.1046/j.1471-4159.2002.01076.x PMID: 12390512
54. Gengs C, Leung H-T, Skingsley DR, Iovchev MI, Yin Z, Semenov EP, et al. The target of Drosophila photoreceptor synaptic transmission is a histamine-gated chloride channel encoded by ort (hclA). J Biol Chem. 2002;277:42113-20. doi: 10.1074/jbc. M207133200 PMID: 12196539
55. Richardt A, Kemme T, Wagner S, Schwarzer D, Marahiel MA, Hovemann BT. Ebony, a novel nonribosomal peptide synthetase for beta-alanine conjugation with biogenic amines in Drosophila. J Biol Chem. 2003;278:41160-6. doi: 10.1074/jbc. M304303200 PMID: 12900414
56. Richardt A, Rybak J, Störtkuhl KF, Meinertzhagen IA, Hovemann BT. Ebony protein in the Drosophila nervous system: optic neuropile expression in glial cells. J Comp Neurol. 2002;452:93-102. doi: 10. 1002/cne.10360 PMID: 12205712
57. Lesa GM, Palfreyman M, Hall DH, Clandinin MT, Rudolph C, Jorgensen EM, et al. Long chain polyunsaturated fatty acids are required for efficient neurotransmission in C. elegans. J Cell Sci. 2003;116:4965-75. doi: 10.1242/jcs.00918 PMID: 14625390
58. Marza E, Long T, Saiardi A, Sumakovic M, Eimer S, Hall DH, et al. Polyunsaturated fatty acids influence synaptojanin localization to regulate synaptic vesicle recycling. Mol Biol Cell. 2008;19:833-42. doi: 10. 1091/mbc. E07-07-0719 PMID: 18094048
59. Ben Gedalya T, Loeb V, Israeli E, Altschuler Y, Selkoe DJ, Sharon R. α-Synuclein and Polyunsaturated Fatty Acids Promote Clathrin-Mediated Endocytosis and Synaptic Vesicle Recycling. Traffic. 2009;10:218-234. doi: 10.1111/j.1600-0854.2008.00853.x PMID: 18980610
60. Puchkov D, Haucke V. Greasing the synaptic vesicle cycle by membrane lipids. Trends Cell Biol. 2013;23:493-503. doi: 10.1016/j.tcb.2013.05.002 PMID: 23756446
61. Connell E, Darios F, Broersen K, Gatsby N, Peak-Chew S-Y, Rickman C, et al. Mechanism of arachidonic acid action on syntaxin-Munc18. EMBO Rep. EMBO Press; 2007;8:414-9. doi: 10.1038/sj. embor.7400935 PMID: 17363971
62. Darios F, Davletov B. Omega-3 and omega-6 fatty acids stimulate cell membrane expansion by acting on syntaxin 3. Nature. 2006;440:813-7. doi: 10.1038/nature04598 PMID: 16598260
63. Rickman C, Davletov B. Arachidonic acid allows SNARE complex formation in the presence of Munc18. Chem Biol. 2005;12:545-53. doi: 10.1016/j.chembiol.2005.03.004 PMID: 15911375
64. Takamori S, Holt M, Stenius K, Lemke EA, Grønborg M, Riedel D, et al. Molecular anatomy of a trafficking organelle. Cell. 2006;127:831-46. doi: 10.1016/j.cell.2006.10.030 PMID: 17110340
65. Deutsch JW, Kelly RB. Lipids of synaptic vesicles: relevance to the mechanism of membrane fusion. Biochemistry. American Chemical Society; 1981;20:378-385. doi: 10.1021/bi00505a024 PMID: 7470487
66. Auestad N, Korsak RA, Morrow JW, Edmond J. Fatty acid oxidation and ketogenesis by astrocytes in primary culture. J Neurochem. 1991;56:1376-86. PMID: 2002348
67. Moore SA, Yoder E, Murphy S, Dutton GR, Spector AA. Astrocytes, not neurons, produce docosahexaenoic acid (22:6 omega-3) and arachidonic acid (20:4 omega-6). J Neurochem. 1991;56:518-24. PMID: 1824862
68. Schnebelen C, Pasquis B, Salinas-Navarro M, Joffre C, Creuzot-Garcher CP, Vidal-Sanz M, et al. A dietary combination of omega-3 and omega-6 polyunsaturated fatty acids is more efficient than single supplementations in the prevention of retinal damage induced by elevation of intraocular pressure in rats. Graefes Arch Clin Exp Ophthalmol. 2009;247:1191-203. doi: 10.1007/s00417-009-1094-6 PMID: 19437028
69. Grintal B, Champeil-Potokar G, Lavialle M, Vancassel S, Breton S, Denis I. Inhibition of astroglial glutamate transport by polyunsaturated fatty acids: evidence for a signalling role of docosahexaenoic acid. Neurochem Int. 2009;54:535-43. doi: 10.1016/j.neuint.2009.02.018 PMID: 19428799
70. Camargo N, Smit AB, Verheijen MHG. SREBPs: SREBP function in glia-neuron interactions. FEBS J. 2009;276:628-36. doi: 10.1111/j.1742-4658.2008.06808.x PMID: 19143832
71. Avet-Rochex A, Maierbrugger KT, Bateman JM. Glial enriched gene expression profiling identifies novel factors regulating the proliferation of specific glial subtypes in the Drosophila brain. Gene Expr Patterns. 2014;16:61-8. doi: 10.1016/j.gep. 2014.09.001 PMID: 25217886
72. Nichols Charles D., Jaime Becnel, Pandey Udai B.. Methods to assay Drosophila behavior. J Vis Exp. 2012(61:):3795. doi: 10.3791/3795 PMID: 22433384