Speed and sensitivity of phototransduction in Drosophila depend on degree of saturation of membrane phospholipids

Journal of Neuroscience

Volumn 35, Issue 6, 2015, Pages 2731-2746

  Randall, Alex S ^a   Liu, Che Hsiung ^a   Brian, Chu ^a   Qifeng, Zhang ^b   Dongre, Sidharta A ^c   Juusola, Mikko ^c,d   Franze, Kristian ^a   Wakelam, Michael J O ^b   Hardie, Roger C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b BABRAHAM INSTITUTE   (United Kingdom)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

^d BEIJING NORMAL UNIVERSITY   (China)

Author keywords

Lipidomics; Mechanosensitivity; Phosphoinositide; Phospholipase C; Photoreceptors; PIP2

Indexed keywords

GLYCOSYLPHOSPHATIDYLINOSITOL DIACYLGLYCEROL LYASE; LINOLEIC ACID; LINOLENIC ACID; MEMBRANE PHOSPHOLIPID; PHOSPHATIDYLINOSITOL 4, 5 BISPHOSPHATE; POLYUNSATURATED FATTY ACID; RHODOPSIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL LIKE CHANNEL; UNCLASSIFIED DRUG; G PROTEIN COUPLED RECEPTOR; PHOSPHOLIPASE C; PHOSPHOLIPID; SODIUM CALCIUM EXCHANGE PROTEIN;

ADULT; ARTICLE; ATOMIC FORCE MICROSCOPY; BEHAVIOR ASSESSMENT; CONTROLLED STUDY; DIET; DROSOPHILA MELANOGASTER; ELECTROPHYSIOLOGY; FEEDBACK SYSTEM; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIGHT INTENSITY; LIGHT REFRACTION; LIGHT RELATED PHENOMENA; LIGHT SCATTERING; LIPID ANALYSIS; LIPID DIET; LIPID SATURATION; LIPIDOMICS; MASS SPECTROMETRY; MATHEMATICAL MODEL; MEMBRANE BIOLOGY; MICROFLUOROMETRY; MOVEMENT PERCEPTION; NONHUMAN; PHOTOMECHANICS; PHOTOREACTIVITY; PHOTORECEPTOR; PHOTOTRANSDUCTION; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SENSORY GATING; SIGNAL DETECTION; SIGNAL NOISE RATIO; SODIUM CALCIUM EXCHANGE; STIMULUS RESPONSE; ANIMAL; CELL MEMBRANE; CHANNEL GATING; LIGHT; LIPID METABOLISM; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL MEMBRANE; DIET; DROSOPHILA MELANOGASTER; ION CHANNEL GATING; LIGHT; LIGHT SIGNAL TRANSDUCTION; LIPID METABOLISM; PHOSPHOLIPIDS; RECEPTORS, G-PROTEIN-COUPLED; RHODOPSIN; SIGNAL-TO-NOISE RATIO; SODIUM-CALCIUM EXCHANGER; TYPE C PHOSPHOLIPASES;

EID: 84922567987     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1150-14.2015     Document Type: Article

References (73)

1. Acharya JK, Jalink K, Hardy RW, Hartenstein V, Zuker CS (1997) InsP3 receptor is essential for growth and differentiation but not for vision in Drosophila. Neuron 18: 881-887. CrossRef Medline.
2. Andersen OS, Koeppe RE 2nd (2007) Bilayer thickness and membrane protein function: an energetic perspective. Annu Rev Biophys Biomol Struct 36: 107-130. CrossRef Medline.
3. Andersen OS, Nielsen C, Maer AM, Lundbaek JA, Goulian M, Koeppe RE 2nd (1999) Ion channels as tools to monitor lipid bilayer-membrane protein interactions: gramicidin channels as molecular force transducers. Methods Enzymol 294: 208-224. CrossRef Medline.
4. Belusic G, Pirih P, StavengaDG (2010) Photoreceptor responses of fruitflies with normal and reduced arrestin content studied by simultaneous measurements of visual pigment fluorescence and ERG. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196: 23-35. CrossRef Medline.
5. Benolken RM, Anderson RE, Wheeler TG (1973) Membrane fatty acids associated with the electrical response in visual excitation. Science 182: 1253-1254. CrossRef Medline.
6. Brenner RR (1984) Effect of unsaturated acids on membrane structure and enzyme kinetics. Prog Lipid Res 23: 69-96. CrossRef Medline.
7. Carvalho M, Sampaio JL, Palm W, Brankatschk M, Eaton S, Shevchenko A (2012) Effects of diet and development on the Drosophila lipidome. Mol Syst Biol 8: 600. CrossRef Medline.
8. Chu B, Postma M, Hardie RC (2013a) Fractional Ca2+ Currents through TRP and TRPL Channels in Drosophila Photoreceptors. Biophys J 104: 1905-1916. CrossRef Medline.
9. Chu B, Liu CH, Sengupta S, Gupta A, Raghu P, Hardie RC (2013b) Common mechanisms regulating dark noise and quantum bump amplification in Drosophila photoreceptors. J Neurophysiol 109: 2044-2055. CrossRef Medline.
10. Chyb S, Raghu P, Hardie RC (1999) Polyunsaturated fatty acids activate the Drosophila light-sensitive channels TRP and TRPL. Nature 397: 255-259. CrossRef Medline.
11. Clark J, Anderson KE, Juvin V, Smith TS, Karpe F, Wakelam MJ, Stephens LR, Hawkins PT (2011) Quantification of PtdInsP3 molecular species in cells and tissues by mass spectrometry. Nat Methods 8: 267-272. CrossRef Medline.
12. Delgado R, Bacigalupo J (2009) Unitary recordings of TRP and TRPL channels from isolated Drosophila retinal photoreceptor rhabdomeres: activation by light and lipids. J Neurophysiol 101: 2372-2379. CrossRef Medline.
13. Delgado R, Muñoz Y, Peña-Cortés H, Giavalisco P, Bacigalupo J (2014) Diacylglycerol activates the light-dependent channel TRP in the photosensitive microvilli of Drosophila melanogaster photoreceptors. J Neurosci 34: 6679-6686. CrossRef Medline.
14. Ejsing CS, Sampaio JL, Surendranath V, Duchoslav E, Ekroos K, Klemm RW, Simons K, Shevchenko A (2009) Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry. Proc Natl Acad Sci U S A 106: 2136-2141. CrossRef Medline.
15. Elia N, Frechter S, Gedi Y, Minke B, Selinger Z (2005) Excess of G{beta}e over Gq{alpha} in vivo prevents dark, spontaneous activity of Drosophila photoreceptors. J Cell Biol 171: 517-526. CrossRef Medline.
16. Fain GL, Hardie R, Laughlin SB (2010) Phototransduction and the evolution of photoreceptors. Curr Biol 20: R114-R124. CrossRef Medline.
17. Feiler R, Bjornson R, Kirschfeld K, Mismer D, Rubin GM, Smith DP, Socolich M, Zuker CS (1992) Ectopic expression of ultraviolet-rhodopsins in the blue photoreceptor cells of Drosophila: visual physiology and photochemistry of transgenic animals. J Neurosci 12: 3862-3868. Medline.
18. Fougeron AS, Farine JP, Flaven-Pouchon J, Everaerts C, Ferveur JF (2011) Fatty-acid preference changes during development in Drosophila melanogaster. PLoS One 6: e26899. CrossRef Medline.
19. Franze K (2011) Atomic force microscopy and its contribution to under-standing the development of the nervous system. Curr Opin Genet Dev 21: 530-537. CrossRef Medline.
20. Gu Y, Oberwinkler J, Postma M, Hardie RC (2005) Mechanisms of light adaptation in Drosophila photoreceptors. Curr Biol 15: 1228-1234. CrossRef Medline.
21. Hardie RC (2011) A brief history of trp: commentary and personal perspective. Pflugers Arch 461: 493-498. CrossRef Medline.
22. Hardie RC (2012) Phototransduction mechanisms in Drosophila microvillar photoreceptors. WIREs Membr Transp Signal 1: 162-187. CrossRef.
23. Hardie RC, Franze K (2012) Photomechanical responses in Drosophila photoreceptors. Science 338: 260-263. CrossRef Medline.
24. Hardie RC, Minke B (1992) The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors. Neuron 8: 643-651. CrossRef Medline.
25. Hardie RC, Martin F, Cochrane GW, Juusola M, Georgiev P, Raghu P (2002) Molecular basis of amplification in Drosophila phototransduction. Roles for G protein, phospholipase C, and diacylglycerol kinase. Neuron 36: 689-701. CrossRef Medline.
26. Henderson SR, Reuss H, Hardie RC (2000) Single photon responses in Drosophila photoreceptors and their regulation by Ca2+. J Physiol 524: 179-194. CrossRef Medline.
27. Hilgemann DW, Ball R (1996) Regulation of cardiac Na+, Ca2+ exchange and KATP potassium channels by PIP2. Science 273: 956-959. CrossRef Medline.
28. Huang J, Liu CH, Hughes SA, Postma M, Schwiening CJ, Hardie RC (2010) Activation of TRP channels by protons and phosphoinositide depletion in Drosophila photoreceptors. Curr Biol 20: 189-197. CrossRef Medline.
29. Isono K, Tanimura T, Oda Y, Tsukahara Y (1988) Dependency on light and vitamin A derivatives of the biogenesis of 3-hydroxyretinal and visual pigment in the compound eyes of Drosophila melanogaster. J Gen Physiol 92: 587-600. CrossRef Medline.
30. Jump DB, Depner CM, Tripathy S (2012) Omega-3 fatty acid supplementation and cardiovascular disease. J Lipid Res 53: 2525-2545. CrossRef Medline.
31. Juusola M, de Polavieja GG (2003) The rate of information transfer of naturalistic stimulation by graded potentials. J Gen Physiol 122: 191-206. CrossRef Medline.
32. Juusola M, Hardie RC (2001) Light adaptation in Drosophila photoreceptors: I. Response dynamics and signaling efficiency at 25°C. J Gen Physiol 117: 3-25. CrossRef Medline.
33. Juusola M, Kouvalainen E, Järvilehto M, Weckström M (1994) Contrast gain, signal-to-noise ratio, and linearity in light-adapted blowfly photoreceptors. J Gen Physiol 104: 593-621. CrossRef Medline.
34. Katz B, Minke B (2009) Drosophila photoreceptors and signaling mechanisms. Front Cell Neurosci 3: 2. CrossRef Medline.
35. Katz B, Minke B (2012) Phospholipase C-mediated suppression of dark noise enables single-photon detection in Drosophila photoreceptors. J Neurosci 32: 2722-2733. CrossRef Medline.
36. Leung HT, Tseng-Crank J, Kim E, Mahapatra C, Shino S, Zhou Y, An L, Doerge RW, Pak WL (2008) DAG lipase activity is necessary for TRP channel regulation in Drosophila photoreceptors. Neuron 58: 884-896. CrossRef Medline.
37. Lev S, Katz B, Tzarfaty V, Minke B (2012) Signal-dependent hydrolysis of phosphatidylinositol 4, 5-bisphosphate without activation of phospholipase C: implications on gating of Drosophila TRPL (transient receptor potential-like) channel. J Biol Chem 287: 1436-1447. CrossRef Medline.
38. Matsumoto H, O'Tousa JE, Pak WL (1982) Light-induced modification of Drosophila retinal polypeptides in vivo. Science 217: 839-841. CrossRef Medline.
39. Minke B, Kirschfeld K (1979) The contribution of a sensitizing pigment to the photosensitivity spectra of fly rhodopsin and metarhodopsin. J Gen Physiol 73: 517-540. CrossRef Medline.
40. Montell C (2012) Drosophila visual transduction. Trends Neurosci 35: 356-363. CrossRef Medline.
41. Montell C, Rubin GM (1989) Molecular characterization of Drosophila trp locus, a putative integral membrane protein required for phototransduction. Neuron 2: 1313-1323. CrossRef Medline.
42. Muñoz Y, Fuenzalida K, Bronfman M, Gatica A, Sepúlveda M, JB, Bacigalupo J, Roth AD, Delgado R (2013) Fatty acid composition of Drosophila photoreceptor light-sensitive microvilli. Biol Res 46: 289-294. CrossRef Medline.
43. Niemeyer BA, Suzuki E, Scott K, Jalink K, Zuker CS (1996) The Drosophila light-activated conductance is composed of the two channels TRP and TRPL. Cell 85: 651-659. CrossRef Medline.
44. Norton LJ, Zhang Q, Saqib KM, Schrewe H, Macura K, Anderson KE, Lindsley CW, Brown HA, Rudge SA, Wakelam MJ (2011) PLD1 rather than PLD2 regulates phorbol-ester, adhesion-dependent and Fc{gamma}-receptor-stimulated ROS production in neutrophils. J Cell Sci 124: 1973-1983. CrossRef Medline.
45. Ollila S, Hyvönen MT, Vattulainen I (2007) Polyunsaturation in lipid membranes: dynamic properties and lateral pressure profiles. J Phys Chem B 111: 3139-3150. CrossRef Medline.
46. Organisciak DT, Vaughan DK (2010) Retinal light damage: mechanisms and protection. Prog Retin Eye Res 29: 113-134. CrossRef Medline.
47. Parnas M, Katz B, Lev S, Tzarfaty V, Dadon D, Gordon-Shaag A, Metzner H, Yaka R, Minke B (2009) Membrane lipid modulations remove divalent open channel block from TRP-Like and NMDA channels. J Neurosci 29: 2371-2383. CrossRef Medline.
48. Pettitt TR, Wakelam MJ (1999) Diacylglycerol kinase epsilon, but not zeta, selectively removes polyunsaturated diacylglycerol, inducing altered protein kinase C distribution in vivo. J Biol Chem 274: 36181-36186. CrossRef Medline.
49. Pettitt TR, Martin A, Horton T, Liossis C, Lord JM, Wakelam MJ (1997) Diacylglycerol and phosphatidate generated by phospholipases C and D, respectively, have distinct fatty acid compositions and functions. Phospholipase D-derived diacylglycerol does not activate protein kinase C in porcine aortic endothelial cells. J Biol Chem 272: 17354-17359. CrossRef Medline.
50. Phillips AM, Bull A, Kelly LE (1992) Identification of a Drosophila gene encoding a calmodulin-binding protein with homology to the trp phototransduction gene. Neuron 8: 631-642. CrossRef Medline.
51. Pinot M, Vanni S, Pagnotta S, Lacas-Gervais S, Payet LA, Ferreira T, Gautier R, Goud B, Antonny B, BarelliH (2014) Polyunsaturated phospholipids facilitate membrane deformation and fission by endocytic proteins. Science 345: 693-697. CrossRef Medline.
52. Postma M, Oberwinkler J, StavengaDG (1999) Does Ca2+ reach millimolar concentrations after single photon absorption in Drosophila photoreceptor microvilli? Biophys J 77: 1811-1823. CrossRef Medline.
53. Pumir A, Graves J, Ranganathan R, Shraiman BI (2008) Systems analysis of the single photon response in invertebrate photoreceptors. Proc Natl Acad Sci U S A 105: 10354-10359. CrossRef Medline.
54. Raghu P, Hardie RC (2009) Regulation of Drosophila TRPC channels by lipid messengers. Cell Calcium 45: 566-573. CrossRef Medline.
55. Raghu P, Colley NJ, Webel R, James T, Hasan G, Danin M, Selinger Z, Hardie RC (2000) Normal phototransduction in Drosophila photoreceptors lacking an InsP3 receptor gene. Mol Cell Neurosci 15: 429-445. CrossRef Medline.
56. Rawicz W, Olbrich KC, McIntosh T, Needham D, Evans E (2000) Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys J 79: 328-339. CrossRef Medline.
57. Reuss H, Mojet MH, Chyb S, Hardie RC (1997) In vivo analysis of the Drosophila light-sensitive channels, TRP and TRPL. Neuron 19: 1249-1259. CrossRef Medline.
58. Satoh AK, Xia H, Yan L, Liu CH, Hardie RC, Ready DF (2010) Arrestin translocation is stoichiometric to rhodopsin isomerization and accelerated by phototransduction in Drosophila photoreceptors. Neuron 67: 997-1008. CrossRef Medline.
59. Schwiening CJ, Willoughby D (2002) Depolarization-induced pH microdomains and their relationship to calcium transients in isolated snail neurones. J Physiol 538: 371-382. CrossRef Medline.
60. Scott K, Becker A, Sun Y, Hardy R, Zuker C (1995) Gq a protein function in vivo: genetic dissection of its role in photoreceptor cell physiology. Neuron 15: 919-927. CrossRef Medline.
61. Scott K, Sun Y, Beckingham K, Zuker CS (1997) Calmodulin regulation of Drosophila light-activated channels and receptor function mediates termination of the light response in vivo. Cell 91: 375-383. CrossRef Medline.
62. Shen LR, Lai CQ, Feng X, Parnell LD, Wan JB, Wang JD, Li D, Ordovas JM, Kang JX (2010) Drosophila lacks C20 and C22 PUFAs. J Lipid Res 51: 2985-2992. CrossRef Medline.
63. Song Z, Juusola M (2014) Refractory sampling links efficiency and costs of sensory encoding to stimulus statistics. J Neurosci 34: 7216-7237. CrossRef Medline.
64. Song Z, Postma M, Billings SA, Coca D, Hardie RC, Juusola M (2012) Sto-chastic, adaptive sampling of information by microvilli in fly photoreceptors. Curr Biol 22: 1371-1380. CrossRef Medline.
65. Stark WS, Lin TN, Brackhahn D, Christianson JS, Sun GY (1993) Phospholipids in Drosophila heads: effects of visual mutants and phototransduction manipulations. Lipids 28: 23-28. CrossRef Medline.
66. Tang S, Guo A (2001) Choice behavior of Drosophila facing contradictory visual cues. Science 294: 1543-1547. CrossRef Medline.
67. van Hateren JH (1997) Processing of natural time series of intensities by the visual system of the blowfly. Vision Res 37: 3407-3416. CrossRef Medline.
68. Vásquez V, Krieg M, Lockhead D, GoodmanMB (2014) Phospholipids that contain polyunsaturated fatty acids enhance neuronal cell mechanics and touch sensation. Cell Rep 6: 70-80. CrossRef Medline.
69. Wang T, Xu H, Oberwinkler J, Gu Y, Hardie RC, Montell C (2005) Light activation, adaptation, and cell survival Functions of the Na+/Ca 2+ exchanger CalX. Neuron 45: 367-378. CrossRef Medline.
70. Wardill TJ, List O, Li X, Dongre S, McCulloch M, Ting CY, O'Kane CJ, Tang S, Lee CH, Hardie RC, Juusola M (2012) Multiple spectral inputs improve motion discrimination in the Drosophila visual system. Science 336: 925-931. CrossRef Medline.
71. Weijers RN (2012) Lipid composition of cell membranes and its relevance in type 2 diabetes mellitus. Curr Diabetes Rev 8: 390-400. CrossRef Medline.
72. Yau KW, Hardie RC (2009) Phototransduction motifs and variations. Cell 139: 246-264. CrossRef Medline.
73. Zinkler D, Bentrop J, Paulsen R (1985) Phospholipids of fly photoreceptor membrane: fatty acid and phosphoinositide metabolism. Verh Dtsch Zool Ges 78: 303.