Acsl, the Drosophila ortholog of intellectual-disability-related ACSL4, inhibits synaptic growth by altered lipids

Journal of Cell Science

Volumn 129, Issue 21, 2016, Pages 4034-4045

  Huang, Yan ^a   Huang, Sheng ^a,b   Lam, Sin Man ^a   Liu, Zhihua ^a,c   Shui, Guanghou ^a   Zhang, Yong Q ^a,d  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

ACSL; Fatty acid; Lipid; Long chain acyl CoA synthetase; Neuromuscular junction; Synaptic growth

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CERAMIDE; DROSOPHILA PROTEIN; ERGOSTEROL; FATTY ACID; GLUCOSYLCERAMIDE; LIPID; LONG CHAIN ACYL COA SYNTHETASE 4; LONG CHAIN FATTY ACID COENZYME A LIGASE; MEMBRANE LIPID; PHOSPHOETHANOLAMINE; UNCLASSIFIED DRUG; ACYL COENZYME A DESATURASE; COENZYME A LIGASE; DESAT1 PROTEIN, DROSOPHILA; LONG-CHAIN-FATTY-ACID-COA LIGASE; STEROL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; DROSOPHILA; GROWTH INHIBITION; LIPID COMPOSITION; LIPIDOMICS; NEUROMUSCULAR JUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; CHEMISTRY; DROSOPHILA MELANOGASTER; ENDOPLASMIC RETICULUM; GENETICS; INTELLECTUAL IMPAIRMENT; MEMBRANE MICRODOMAIN; METABOLISM; MUTATION; NERVE CELL; PEROXISOME; SEQUENCE HOMOLOGY; SYNAPSE;

ANIMALS; BRAIN; CERAMIDES; COENZYME A LIGASES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOPLASMIC RETICULUM; FATTY ACID DESATURASES; FATTY ACIDS; INTELLECTUAL DISABILITY; LIPIDS; MEMBRANE MICRODOMAINS; MUTATION; NEUROMUSCULAR JUNCTION; NEURONS; PEROXISOMES; SEQUENCE HOMOLOGY, AMINO ACID; STEROLS; SYNAPSES;

EID: 84995407015     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.195032     Document Type: Article

References (59)

1. Allen, J. A., Halverson-Tamboli, R. A. and Rasenick, M. M. (2007). Lipid raft microdomains and neurotransmitter signalling. Nat. Rev. Neurosci. 8, 128-140.
2. Bazinet, R. P. and Layé, S. (2014). Polyunsaturated fatty acids and their metabolites in brain function and disease. Nat. Rev. Neurosci. 15, 771-785.
3. Bu, S. Y., Mashek, M. T. and Mashek, D. G. (2009). Suppression of long chain acyl-CoA synthetase 3 decreases hepatic de novo fatty acid synthesis through decreased transcriptional activity. J. Biol. Chem. 284, 30474-30483.
4. Carvalho, M., Schwudke, D., Sampaio, J. L., Palm, W., Riezman, I., Dey, G., Gupta, G. D., Mayor, S., Riezman, H., Shevchenko, A. et al. (2010). Survival strategies of a sterol auxotroph. Development 137, 3675-3685.
5. Carvalho, M., Sampaio, J. L., Palm, W., Brankatschk, M., Eaton, S. and Shevchenko, A. (2012). Effects of diet and development on the Drosophila lipidome. Mol. Syst. Biol. 8, 600.
6. Chen, Y.-W., Pedersen, J.W., Wandall, H. H., Levery, S. B., Pizette, S., Clausen, H. and Cohen, S. M. (2007). Glycosphingolipids with extended sugar chain have specialized functions in development and behavior of Drosophila. Dev. Biol. 306, 736-749.
7. Chen, H., Liu, Z. and Huang, X. (2010). Drosophila models of peroxisomal biogenesis disorder: peroxins are required for spermatogenesis and very-longchain fatty acid metabolism. Hum. Mol. Genet. 19, 494-505.
8. Christie, W. W. (1989). Gas Chromatography and Lipids: a Practical Guide. Ayr, Scotland: The Oily Press.
9. Coleman, R. A., Lewin, T. M. and Muoio, D. M. P. (2000). Physiological and nutritional regulation of enzymes of triacylglycerol synthesis. Annu. Rev. Nutr. 20, 77-103.
10. Collins, C. A. and DiAntonio, A. (2007). Synaptic development: insights from Drosophila. Curr. Opin. Neurobiol. 17, 35-42.
11. Davletov, B. and Montecucco, C. (2010). Lipid function at synapses. Curr. Opin. Neurobiol. 20, 543-549.
12. Deshpande, M. and Rodal, A. A. (2016). The crossroads of synaptic growth signaling, membrane traffic and neurological disease: insights from Drosophila. Traffic 17, 87-101.
13. Di Paolo, G. and De Camilli, P. (2006). Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657.
14. Ellis, J. M., Frahm, J. L., Li, L. O. and Coleman, R. A. (2010). Acyl-coenzyme A synthetases in metabolic control. Curr. Opin. Lipidol. 21, 212-217.
15. Faust, J. E., Manisundaram, A., Ivanova, P. T., Milne, S. B., Summerville, J. B., Brown, H. A., Wangler, M., Stern, M. and McNew, J. A. (2014). Peroxisomes are required for lipid metabolism and muscle function in Drosophila melanogaster. PLoS ONE 9, e100213.
16. Golej, D. L., Askari, B., Kramer, F., Barnhart, S., Vivekanandan-Giri, A., Pennathur, S. and Bornfeldt, K. E. (2011). Long-chain acyl-CoA synthetase 4 modulates prostaglandin E2 release from human arterial smooth muscle cells. J. Lipid. Res. 52, 782-793.
17. Hammad, L. A., Cooper, B. S., Fisher, N. P., Montooth, K. L. and Karty, J. A. (2011). Profiling and quantification of Drosophila melanogaster lipids using liquid chromatography/mass spectrometry. Rapid Commun. Mass Spectrom. 25, 2959-2968.
18. Hebbar, S., Lee, E., Manna, M., Steinert, S., Kumar, G. S., Wenk, M., Wohland, T. and Kraut, R. (2008). A fluorescent sphingolipid binding domain peptide probe interacts with sphingolipids and cholesterol-dependent raft domains. J. Lipid Res. 49, 1077-1089.
19. Hering, H., Lin, C. C. and Sheng, M. (2003). Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J. Neurosci. 23, 3262-3271.
20. Hryniewicz-Jankowska, A., Augoff, K., Biernatowska, A., Podkalicka, J. and Sikorski, A. F. (2014). Membrane rafts as a novel target in cancer therapy. Biochim. Biophys. Acta 1845, 155-165.
21. Kang, M.-J., Fujino, T., Sasano, H., Minekura, H., Yabuki, N., Nagura, H., Iijima, H. and Yamamoto, T. T. (1997). A novel arachidonate-preferring acyl-CoA synthetase is present in steroidogenic cells of the rat adrenal, ovary, and testis. Proc. Natl. Acad. Sci. USA 94, 2880-2884.
22. Kelley, C. F., Messelaar, E. M., Eskin, T. L., Wang, S., Song, K., Vishnia, K., Becalska, A. N., Shupliakov, O., Hagan, M. F., Danino, D. et al. (2015). Membrane charge directs the outcome of F-BAR domain lipid binding and autoregulation. Cell Rep. 13, 2597-2609.
23. Kim, J. H., Lewin, T. M. and Coleman, R. A. (2001). Expression and characterization of recombinant rat Acyl-CoA synthetases 1, 4, and 5. Selective inhibition by triacsin C and thiazolidinediones. J. Biol. Chem. 276, 24667-24673.
24. Kniazeva, M., Shen, H. L., Euler, T., Wang, C. and Han, M. (2012). Regulation of maternal phospholipid composition and IP3-dependent embryonic membrane dynamics by a specific fatty acid metabolic event in C. elegans. Gene Dev. 26, 554-566.
25. Köhler, K., Brunner, E., Guan, X. L., Boucke, K., Greber, U. F., Mohanty, S., Barth, J. M. I., Wenk, M. R. and Hafen, E. (2009). A combined proteomic and genetic analysis identifies a role for the lipid desaturase Desat1 in starvationinduced autophagy in Drosophila. Autophagy 5, 980-990.
26. Küch, E.-M., Vellaramkalayil, R., Zhang, I., Lehnen, D., Brügger, B., Sreemmel, W., Ehehalt, R., Poppelreuther, M. and Füllekrug, J. (2014). Differentially localized acyl-CoA synthetase 4 isoenzymes mediate the metabolic channeling of fatty acids towards phosphatidylinositol. Biochim. Biophys. Acta Mol. Cell Biol. 1841, 227-239.
27. Lam, S. M., Wang, Y., Duan, X., Wenk, M. R., Kalaria, R. N., Chen, C. P., Lai, M. K. P. and Shui, G. (2014). The brain lipidomes of subcortical ischemic vascular dementia and mixed dementia. Neurobiol. Aging 35, 2369-2381.
28. Lauwers, E., Goodchild, R. and Verstreken, P. (2016). Membrane lipids in presynaptic function and disease. Neuron 90, 11-25.
29. Lewin, T. M., Van Horn, C. G., Krisans, S. K. and Coleman, R. A. (2002). Rat liver acyl-CoA synthetase 4 is a peripheral-membrane protein located in two distinct subcellular organelles, peroxisomes, and mitochondrial-associated membrane. Arch. Biochem. Biophys. 404, 263-270.
30. Lingwood, D. and Simons, K. (2010). Lipid rafts as a membrane-organizing principle. Science 327, 46-50.
31. Liu, Z., Huang, Y., Zhang, Y., Chen, D. and Zhang, Y. Q. (2011). Drosophila acyl-CoA synthetase long-chain family member 4 regulates axonal transport of synaptic vesicles and is required for synaptic development and transmission. J. Neurosci. 31, 2052-2063.
32. Liu, Z., Huang, Y., Hu, W., Huang, S., Wang, Q., Han, J. and Zhang, Y. Q. (2014). dAcsl, the Drosophila ortholog of acyl-CoA synthetase long-chain family member 3 and 4, inhibits synapse growth by attenuating bone morphogenetic protein signaling via endocytic recycling. J. Neurosci. 34, 2785-2796.
33. Longo, I., Frints, S. G., Fryns, J. P., Meloni, I., Pescucci, C., Ariani, F., Borghgraef, M., Raynaud, M., Marynen, P., Schwartz, C. et al. (2003). A third MRX family (MRX68) is the result of mutation in the long chain fatty acid-CoA ligase 4 (FACL4) gene: proposal of a rapid enzymatic assay for screening mentally retarded patients. J. Med. Genet. 40, 11-17.
34. Mashek, D. G., Li, L. O. and Coleman, R. A. (2007). Long-chain acyl-CoA synthetases and fatty acid channeling. Future Lipidol. 2, 465-476.
35. Meloni, I., Muscettola, M., Raynaud, M., Longo, I., 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. Nat. Genet. 30, 436-440.
36. Meloni, I., Parri, V., De Filippis, R., Ariani, F., Artuso, R., Bruttini, M., Katzaki, E., Longo, I., Mari, F., Bellan, C. et al. (2009). The XLMR gene ACSL4 plays a role in dendritic spine architecture. Neuroscience 159, 657-669.
37. Mauch, D. H., Nägler, K., Schumacher, S., Göritz, C., Müller, E.-C., Otto, A. and Pfrieger, F. W. (2001). CNS synaptogenesis promoted by glia-derived cholesterol. Science 294, 1354-1357.
38. Najmabadi, H., Hu, H., Garshasbi, M., Zemojtel, T., Abedini, S. S., Chen, W., Hosseini, M., Behjati, F., Haas, S., Jamali, P. et al. (2011). Deep sequencing reveals 50 novel genes for recessive cognitive disorders. Nature 478, 57-63.
39. O'Connor-Giles, K. M., Ho, L. L. and Ganetzky, B. (2008). Nervous wreck interacts with thickveins and the endocytic machinery to attenuate retrograde BMP signaling during synaptic growth. Neuron 58, 507-518.
40. O'Sullivan, N. C., Jahn, T. R., Reid, E. and O'Kane, C. J. (2012). Reticulon-like-1, the Drosophila orthologue of the Hereditary Spastic Paraplegia gene reticulon 2, is required for organization of endoplasmic reticulum and of distal motor axons. Hum. Mol. Genet. 21, 3356-3365.
41. Packard, M., Koo, E. S., Gorczyca, M., Sharpe, J., Cumberledge, S. and Budnik, V. (2002). The drosophila wnt, wingless, provides an essential signal for pre-and postsynaptic differentiation. Cell 111, 319-330.
42. Persson, U., Izumi, H., Souchelnytskyi, S., Itoh, S., Grimsby, S., Engstrom, U., Heldin, C. H., Funa, K. and ten Dijke, P. (1998). The L45 loop in type I receptors for TGF-beta family members is a critical determinant in specifying Smad isoform activation. FEBS Lett. 434, 83-87.
43. Rietveld, A., Neutz, S., Simons, K. and Eaton, S. (1999). Association of sterol-and glycosylphosphatidylinositol-linked proteins with Drosophila raft lipid microdomains. J. Biol. Chem. 274, 12049-12054.
44. Schroeder, F., Petrescu, A. D., Huang, H., Atshaves, B. P., McIntosh, A. L., Martin, G. G., Hostetler, H. A., Vespa, A., Landrock, D., Landrock, K. K. et al. (2008). Role of fatty acid binding proteins and long chain fatty acids in modulating nuclear receptors and gene transcription. Lipids 43, 1-17.
45. Sharma, P., Varma, R., Sarasij, R. C., Ira, Gousset, K., Krishnamoorthy, G., Rao, M. and Mayor, S. (2004). Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116, 577-589.
46. Shen, L. R., Lai, C. Q., Feng, X., Parnell, L. D., Wan, J. B., Wang, J. D., Li, D., Ordovas, J. M. and Kang, J. X. (2010). Drosophila lacks C20 and C22 PUFAs. J. Lipid. Res. 51, 2985-2992.
47. Sivachenko, A., Gordon, H. B., Kimball, S. S., Gavin, E. J., Bonkowsky, J. L. and Letsou, A. (2016). Neurodegeneration in a Drosophila model of Adrenoleukodystrophy: the roles of the bubblegum and double bubble acyl-CoA synthetases. Dis. Model. Mech. 9, 377-387.
48. Van Horn, C. G., Caviglia, J. M., Li, L. O., Wang, S., Granger, D. A. and Coleman, R. A. (2005). Characterization of recombinant long-chain rat acyl-CoA synthetase isoforms 3 and 6: identification of a novel variant of isoform 6. Biochemistry 44, 1635-1642.
49. van Meer, G., Voelker, D. R. and Feigenson, G.W. (2008). Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell. Biol. 9, 112-124.
50. Wandall, H. H., Pedersen, J.W., Park, C., Levery, S. B., Pizette, S., Cohen, S. M., Schwientek, T. and Clausen, H. (2003). Drosophila egghead encodes a beta 1, 4-mannosyltransferase predicted to form the immediate precursor glycosphingolipid substrate for brainiac. J. Biol. Chem. 278, 1411-1414.
51. Wandall, H. H., Pizette, S., Pedersen, J.W., Eichert, H., Levery, S. B., Mandel, U., Cohen, S. M. and Clausen, H. (2005). Egghead and brainiac are essential for glycosphingolipid biosynthesis in vivo. J. Biol. Chem. 280, 4858-4863.
52. Wanders, R. J. A. and Waterham, H. R. (2006). Biochemistry of mammalian peroxisomes revisited. Annu. Rev. Biochem. 75, 295-332.
53. Watkins, P. A., Maiguel, D., Jia, Z. and Pevsner, J. (2007). Evidence for 26 distinct acyl-coenzyme A synthetase genes in the human genome. J. Lipid Res. 48, 2736-2750.
54. Xu, Y.-H., Barnes, S., Sun, Y. and Grabowski, G. A. (2010). Multi-system disorders of glycosphingolipid and ganglioside metabolism. J. Lipid Res. 51, 1643-1675.
55. Zhai, L., Chaturvedi, D. and Cumberledge, S. (2004). Drosophila Wnt-1 undergoes a hydrophobic modification and is targeted to lipid rafts, a process that requires porcupine. J. Biol. Chem. 279, 33220-33227.
56. Zhang, Y., Chen, D. and Wang, Z. (2009). Analyses of mental dysfunction-related ACSl4 in Drosophila reveal its requirement for Dpp/BMP production and visual wiring in the brain. Hum. Mol. Genet. 18, 3894-3905.
57. Zhang, H. J., Abraham, N., Khan, L. A., Hall, D. H., Fleming, J. T. and Gobel, V. (2011). Apicobasal domain identities of expanding tubular membranes depend on glycosphingolipid biosynthesis. Nat. Cell. Biol. 13, 1189-1201.
58. Zhu, H. H., Shen, H. L., Sewell, A. K., Kniazeva, M. and Han, M. (2013). A novel sphingolipid-TORC1 pathway critically promotes postembryonic development in Caenorhabditis elegans. Elife 2, e00429.
59. Zoghbi, H. Y. and Bear, M. F. (2012). Synaptic dysfunction in neurodevelopmental disorders associated with autism and intellectual disabilities. Cold Spring Harb. Perspect. Biol. 4, a009886.