Differentially localized acyl-CoA synthetase 4 isoenzymes mediate the metabolic channeling of fatty acids towards phosphatidylinositol

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1841, Issue 2, 2014, Pages 227-239

  Küch, Eva Maria ^a   Vellaramkalayil, Regina ^a   Zhang, Ingrid ^a   Lehnen, Daniela ^a   Brügger, Britta ^a   Stremmel, Wolfgang ^a   Ehehalt, Robert ^a   Poppelreuther, Margarete ^a   Füllekrug, Joachim ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

ACSL4; Acyl CoA synthetase; Fatty acid uptake; Localization; Phosphatidylinositol

Indexed keywords

LONG CHAIN FATTY ACID COENZYME A LIGASE; LONG CHAIN FATTY ACID COENZYME A LIGASE 4; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLINOSITOL; UNCLASSIFIED DRUG;

ARTICLE; CELL FRACTIONATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; FATTY ACID TRANSPORT; HUMAN; HUMAN CELL; HYDROPHOBICITY; LIPID METABOLISM; LIPOGENESIS; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL TARGETING SIGNAL; PHOSPHOLIPID METABOLISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; COENZYME A LIGASES; FATTY ACIDS; HUMANS; ISOENZYMES; PHOSPHATIDYLINOSITOLS;

EID: 84890381103     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2013.10.018     Document Type: Article

References (87)

1. P.A. Watkins, D. Maiguel, Z. Jia, and J. Pevsner Evidence for 26 distinct acyl-coenzyme A synthetase genes in the human genome J. Lipid Res. 48 2007 2736 2750
2. D.G. Mashek, K.E. Bornfeldt, R.A. Coleman, J. Berger, D.A. Bernlohr, P. Black, C.C. DiRusso, S.A. Farber, W. Guo, N. Hashimoto, V. Khodiyar, F.A. Kuypers, L.J. Maltais, D.W. Nebert, A. Renieri, J.E. Schaffer, A. Stahl, P.A. Watkins, V. Vasiliou, and T.T. Yamamoto Revised nomenclature for the mammalian long-chain acyl-CoA synthetase gene family J. Lipid Res. 45 2004 1958 1961
3. D.G. Mashek, L.O. Li, and R.A. Coleman Rat long-chain acyl-CoA synthetase mRNA, protein, and activity vary in tissue distribution and in response to diet J. Lipid Res. 47 2006 2004 2010
4. A. Sandoval, P. Fraisl, E. Arias-Barrau, C.C. DiRusso, D. Singer, W. Sealls, and P.N. Black Fatty acid transport and activation and the expression patterns of genes involved in fatty acid trafficking Arch. Biochem. Biophys. 477 2008 363 371
5. M.J. Kang, T. Fujino, H. Sasano, H. Minekura, N. Yabuki, H. Nagura, H. Iijima, and T.T. Yamamoto A novel arachidonate-preferring acyl-CoA synthetase is present in steroidogenic cells of the rat adrenal, ovary, and testis Proc. Natl. Acad. Sci. U. S. A. 94 1997 2880 2884
6. J.-H. Kim, T.M. Lewin, and R.A. Coleman Expression and characterization of recombinant rat acyl-CoA synthetases 1, 4, and 5. Selective inhibition by triacsin C and thiazolidinediones J. Biol. Chem. 276 2001 24667 24673
7. L. Stinnett, T.M. Lewin, and R.A. Coleman Mutagenesis of rat acyl-CoA synthetase 4 indicates amino acids that contribute to fatty acid binding Biochim. Biophys. Acta 1771 2007 119 125
8. M. Piccini, F. Vitelli, M. Bruttini, B.R. Pober, J.J. Jonsson, M. Villanova, M. Zollo, G. Borsani, A. Ballabio, and A. Renieri FACL4, a new gene encoding long-chain acyl-CoA synthetase 4, is deleted in a family with Alport syndrome, elliptocytosis, and mental retardation Genomics 47 1998 350 358
9. Y. Cao, K.J. Murphy, T.M. McIntyre, G.A. Zimmerman, and S.M. Prescott Expression of fatty acid-CoA ligase 4 during development and in brain FEBS Lett. 467 2000 263 267
10. M. Muscettola Meloni, M. Raynaud, I. Longo, M. Bruttini, M.-P. Moizard, M. Gomot, J. Chelly, V. des Portes, J.-P. Fryns, H.-H. Ropers, B. Magi, C. Bellan, N. Volpi, H.G. Yntema, S.E. Lewis, J.E. Schaffer, and A. Renieri FACL4, encoding fatty acid-CoA ligase 4, is mutated in nonspecific X-linked mental retardation Nat. Genet. 30 2002 436 440
11. H.H. Ropers, and B.C. Hamel X-linked mental retardation Nat. Rev. Genet. 6 2005 46 57
12. Y. Cao, A.T. Pearman, G.A. Zimmerman, T.M. McIntyre, and S.M. Prescott Intracellular unesterified arachidonic acid signals apoptosis Proc. Natl. Acad. Sci. U. S. A. 97 2000 11280 11285
13. L.O. Li, E.L. Klett, and R.A. Coleman Acyl-CoA synthesis, lipid metabolism and lipotoxicity Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1801 2009 246 251
14. P.A. Watkins, and J.M. Ellis Peroxisomal acyl-CoA synthetases Biochim. Biophys. Acta (BBA) - Mol. Basis Dis. 1822 2012 1411 1420
15. P. Maloberti, R. Castilla, F. Castillo, F.C. Maciel, C.F. Mendez, C. Paz, and E.J. Podestá Silencing the expression of mitochondrial acyl-CoA thioesterase I and acyl-CoA synthetase 4 inhibits hormone-induced steroidogenesis FEBS J. 272 2005 1804 1814
16. Y. Hisanaga, H. Ago, N. Nakagawa, K. Hamada, K. Ida, M. Yamamoto, T. Hori, Y. Arii, M. Sugahara, S. Kuramitsu, S. Yokoyama, and M. Miyano Structural basis of the substrate-specific two-step catalysis of long chain fatty acyl-CoA synthetase dimer J. Biol. Chem. 279 2004 31717 31726
17. F. Forneris, and A. Mattevi Enzymes without borders: mobilizing substrates, delivering products Science 321 2008 213 216
18. N.J. Faergeman, and J. Knudsen Role of long-chain fatty acyl-CoA esters in the regulation of metabolism and in cell signalling Biochem. J. 323 Pt 1 1997 1 12
19. R.A. Coleman, T.M. Lewin, C.G. Van Horn, and M.R. Gonzalez-Baro Do long-chain acyl-CoA synthetases regulate fatty acid entry into synthetic versus degradative pathways? J. Nutr. 132 2002 2123 2126
20. J.M. Ellis, J.L. Frahm, L.O. Li, and R.A. Coleman Acyl-coenzyme A synthetases in metabolic control Curr. Opin. Lipidol. 21 2010 212 217
21. M. Digel, R. Ehehalt, W. Stremmel, and J. Fullekrug Acyl-CoA synthetases: fatty acid uptake and metabolic channeling Mol. Cell. Biochem. 326 2009 23 28
22. K.H. Weiss, J.C. Lozoya, S. Tuma, D. Gotthardt, J. Reichert, R. Ehehalt, W. Stremmel, and J. Fullekrug Copper-induced translocation of the Wilson disease protein ATP7B independent of Murr1/COMMD1 and Rab7 Am. J. Pathol. 173 2008 1783 1794
23. K. Milger, T. Herrmann, C. Becker, D. Gotthardt, J. Zickwolf, R. Ehehalt, P.A. Watkins, W. Stremmel, and J. Fullekrug Cellular uptake of fatty acids driven by the ER-localized acyl-CoA synthetase FATP4 J. Cell Sci. 119 2006 4678 4688
24. M. Digel, S. Staffer, F. Ehehalt, W. Stremmel, R. Ehehalt, and J. Füllekrug FATP4 contributes as an enzyme to the basal and insulin-mediated fatty acid uptake of C2C12 muscle cells Am. J. Physiol. Endocrinol. Metab. 301 2011 E785 E796
25. D. Meder, A. Shevchenko, K. Simons, and J. Fullekrug Gp135/podocalyxin and NHERF-2 participate in the formation of a preapical domain during polarization of MDCK cells J. Cell Biol. 168 2005 303 313
26. R. Ehehalt, R. Sparla, H. Kulaksiz, T. Herrmann, J. Fullekrug, and W. Stremmel Uptake of long chain fatty acids is regulated by dynamic interaction of FAT/CD36 with cholesterol/sphingolipid enriched microdomains (lipid rafts) BMC Cell Biol. 9 2008 45
27. V. Dubreuil, A.-M. Marzesco, D. Corbeil, W.B. Huttner, and M. Wilsch-Brauninger Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1 J. Cell Biol. 176 2007 483 495
28. L. Kuerschner, C.S. Ejsing, K. Ekroos, A. Shevchenko, K.I. Anderson, and C. Thiele Polyene-lipids: a new tool to image lipids Nat. Methods 2 2004 39 45
29. Z. Harder, R. Zunino, and H. McBride Sumo1 conjugates mitochondrial substrates and participates in mitochondrial fission Curr. Biol. 14 2004 340 345
30. E.L. Snapp, R.S. Hegde, M. Francolini, F. Lombardo, S. Colombo, E. Pedrazzini, N. Borgese, and J. Lippincott-Schwartz Formation of stacked ER cisternae by low affinity protein interactions J. Cell Biol. 163 2003 257 269
31. J. Fullekrug, B. Sonnichsen, U. Wunsch, K. Arseven, P. Nguyen Van, H. Soling, and G. Mieskes CaBP1, a calcium binding protein of the thioredoxin family, is a resident KDEL protein of the ER and not of the intermediate compartment J. Cell Sci. 107 1994 2719 2727
32. L. Kuerschner, C. Moessinger, and C. Thiele Imaging of lipid biosynthesis: how a neutral lipid enters lipid droplets Traffic 9 2008 338 352
33. M. Poppelreuther, B. Rudolph, C. Du, R. Grossmann, M. Becker, C. Thiele, R. Ehehalt, and J. Fuellekrug The N-terminal region of acyl-CoA synthetase 3 is essential for both the localization on lipid droplets and the function in fatty acid uptake J. Lipid Res. 53 2012 888 900
34. J. Folch, M. Lees, and G.H. Sloane Stanley A simple method for the isolation and purification of total lipids from animal tissues J. Biol. Chem. 226 1957 497 509
35. J. Kasurinen A novel fluorescent fatty acid, 5-methyl-BDY-3-dodecanoic acid, is a potential probe in lipid transport studies by incorporating selectively to lipid classes of BHK cells Biochem. Biophys. Res. Commun. 187 1992 1594 1601
36. D. Allan, and S. Cockcroft A modified procedure for thin-layer chromatography of phospholipids J. Lipid Res. 23 1982 1373 1374
37. E.G. Bligh, and W.J. Dyer A rapid method of total lipid extraction and purification Can. J. Biochem. Physiol. 37 1959 911 917
38. G. Rouser, S. Fkeischer, and A. Yamamoto Two dimensional then layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots Lipids 5 1970 494 496
39. C. Özbalci, T. Sachsenheimer, and B. Brügger Quantitative analysis of cellular lipids by nano-electrospray ionization mass spectrometry D. Rapaport, J.M. Herrmann, Membrane Biogenesis vol. 1033 2013 Humana Press 3 20
40. S. Kanaji, J. Iwahashi, Y. Kida, M. Sakaguchi, and K. Mihara Characterization of the signal that directs tom20 to the mitochondrial outer membrane J. Cell Biol. 151 2000 277 288
41. D.G. Mashek, and R.A. Coleman Cellular fatty acid uptake: the contribution of metabolism Curr. Opin. Lipidol. 17 2006 274 278
42. J. Fuellekrug, R. Ehehalt, and M. Poppelreuther Outlook: membrane junctions enable the metabolic trapping of fatty acids by intracellular acyl-CoA synthetases Front. Physiol. 3 2012
43. T.M. Lewin, C.G. Van Horn, S.K. Krisans, and R.A. Coleman 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 2002 263 270
44. Y. Fujimoto, H. Itabe, J. Sakai, M. Makita, J. Noda, M. Mori, Y. Higashi, S. Kojima, and T. Takano Identification of major proteins in the lipid droplet-enriched fraction isolated from the human hepatocyte cell line HuH7 Biochim. Biophys. Acta 1644 2004 47 59
45. M.A. Welte Proteins under new management: lipid droplets deliver Trends Cell Biol. 17 2007 363 369
46. M. Digel, R. Ehehalt, and J. Füllekrug Lipid droplets lighting up: insights from live microscopy FEBS Lett. 584 2010 2168 2175
47. I. Meloni, V. Parri, R. De Filippis, F. Ariani, R. Artuso, M. Bruttini, E. Katzaki, I. Longo, F. Mari, C. Bellan, C.G. Dotti, and A. Renieri The XLMR gene ACSL4 plays a role in dendritic spine architecture Neuroscience 159 2009 657 669
48. T. Fujino, M.-J. Kang, H. Suzuki, H. Iijima, and T. Yamamoto Molecular characterization and expression of rat acyl-CoA synthetase 3 J. Biol. Chem. 271 1996 16748 16752
49. K. Takeuchi, K. Sakurada, H. Endou, M. Obinata, and M.P. Quinlan Differential effects of DNA tumor virus genes on the expression profiles, differentiation, and morphogenetic reprogramming potential of epithelial cells Virology 300 2002 8 19
50. J.R. Skinner, T.M. Shew, D.M. Schwartz, A. Tzekov, C.M. Lepus, N.A. Abumrad, and N.E. Wolins Diacylglycerol enrichment of endoplasmic reticulum or lipid droplets recruits perilipin 3/TIP47 during lipid storage and mobilization J. Biol. Chem. 284 2009 30941 30948
51. D.G. Mashek, M.A. McKenzie, C.G. Van Horn, and R.A. Coleman Rat long chain acyl-CoA synthetase 5 increases fatty acid uptake and partitioning to cellular triacylglycerol in McArdle-RH7777 cells J. Biol. Chem. 281 2006 945 950
52. P. Overath, G. Pauli, and H.U. Schairer Fatty acid degradation in Escherichia coli. An inducible acyl-CoA synthetase, the mapping of old-mutations, and the isolation of regulatory mutants Eur. J. Biochem. 7 1969 559 574
53. P.N. Black, and C.C. DiRusso Transmembrane movement of exogenous long-chain fatty acids: proteins, enzymes, and vectorial esterification Microbiol. Mol. Biol. Rev. 67 2003 454 472
54. J.F. Glatz, and J. Storch Unravelling the significance of cellular fatty acid-binding proteins Curr. Opin. Lipidol. 12 2001 267 274
55. A. Lykidis, P.D. Jackson, C.O. Rock, and S. Jackowski The role of CDP-diacylglycerol synthetase and phosphatidylinositol synthase activity levels in the regulation of cellular phosphatidylinositol content J. Biol. Chem. 272 1997 33402 33409
56. S. Saito, K. Goto, A. Tonosaki, and H. Kondo Gene cloning and characterization of CDP-diacylglycerol synthase from rat brain J. Biol. Chem. 272 1997 9503 9509
57. W.E.M. Lands Metabolism of glycerolipids: a comparison of lecithin and triglyceride synthesis J. Biol. Chem. 231 1958 883 888
58. F.H. Chilton, A.N. Fonteh, M.E. Surette, M. Triggiani, and J.D. Winkler Control of arachidonate levels within inflammatory cells Biochim. Biophys. Acta 1299 1996 1 15
59. A. Yamashita, T. Sugiura, and K. Waku Acyltransferases and transacylases involved in fatty acid remodeling of phospholipids and metabolism of bioactive lipids in mammalian cells J. Biochem. 122 1997 1 16
60. G. Pérez-Chacón, A.M. Astudillo, D. Balgoma, M.A. Balboa, and J. Balsinde Control of free arachidonic acid levels by phospholipases A2 and lysophospholipid acyltransferases Biochim. Biophys. Acta 1791 2009 1103 1113
61. H.-C. Lee, T. Inoue, J. Sasaki, T. Kubo, S. Matsuda, Y. Nakasaki, M. Hattori, F. Tanaka, O. Udagawa, N. Kono, T. Itoh, H. Ogiso, R. Taguchi, M. Arita, T. Sasaki, and H. Arai LPIAT1 regulates arachidonic acid content in phosphatidylinositol and is required for cortical lamination in mice Mol. Biol. Cell 23 2012 4689 4700
62. C. Eberhardt, P.W. Gray, and L.W. Tjoelker Human lysophosphatidic acid acyltransferase: cDNA cloning, expression, and localization to chromosome 9q34.3 J. Biol. Chem. 272 1997 20299 20305
63. D.L. Golej, B. Askari, F. Kramer, S. Barnhart, A. Vivekanandan-Giri, S. Pennathur, and K.E. Bornfeldt Long-chain acyl-CoA synthetase 4 modulates prostaglandin E2 release from human arterial smooth muscle cells J. Lipid Res. 52 2011 782 793
64. E. Soupene, and F.A. Kuypers Mammalian long-chain acyl-CoA synthetases Exp. Biol. Med. 233 2008 507 521
65. R.A. Igal, P. Wang, and R.A. Coleman Triacsin C blocks de novo synthesis of glycerolipids and cholesterol esters but not recycling of fatty acid into phospholipid: evidence for functionally separate pools of acyl-CoA Biochem. J. 324 Pt 2 1997 529 534
66. L.O. Li, D.G. Mashek, J. An, S.D. Doughman, C.B. Newgard, and R.A. Coleman Overexpression of rat long chain acyl-CoA synthetase 1 alters fatty acid metabolism in rat primary hepatocytes J. Biol. Chem. 281 2006 37246 37255
67. J.M. Ellis, L.O. Li, P.-C. Wu, T.R. Koves, O. Ilkayeva, R.D. Stevens, S.M. Watkins, D.M. Muoio, and R.A. Coleman Adipose acyl-CoA synthetase-1 directs fatty acids toward [beta]-oxidation and is required for cold thermogenesis Cell Metab. 12 2010 53 64
68. S.Y. Bu, and D.G. Mashek Hepatic long-chain acyl-CoA synthetase 5 (ACSL5) mediates fatty acid channeling between anabolic and catabolic pathways J. Lipid Res. 51 2010 3270 3280
69. X. Xu, P. Gopalacharyulu, T. Seppänen-Laakso, A.-L. Ruskeepää, C.C. Aye, B.P. Carson, S. Mora, M. Oresic, and A.A. Teleman Insulin signaling regulates fatty acid catabolism at the level of CoA activation PLoS Genet. 8 2012 e1002478
70. E.M. Melton, R.L. Cerny, P.A. Watkins, C.C. DiRusso, and P.N. Black Human fatty acid transport protein 2a/very long chain acyl-CoA synthetase 1 (FATP2a/Acsvl1) has a preference in mediating the channeling of exogenous n-3 fatty acids into phosphatidylinositol J. Biol. Chem. 286 2011 30670 30679
71. S. Lobo, B.M. Wiczer, and D.A. Bernlohr Functional analysis of long-chain acyl-CoA synthetase 1 in 3T3-L1 adipocytes J. Biol. Chem. 284 2009 18347 18356
72. B.B. Kragelund, J. Knudsen, and F.M. Poulsen Acyl-coenzyme A binding protein (ACBP) Biochim. Biophys. Acta 1441 1999 150 161
73. N.J. Faergeman, M. Wadum, S. Feddersen, M. Burton, B.B. Kragelund, and J. Knudsen Acyl-CoA binding proteins; structural and functional conservation over 2000 MYA Mol. Cell. Biochem. 299 2007 55 65
74. R.A. Coleman, T.M. Lewin, and D.M. Muoio Physiological and nutritional regulation of enzymes of triacylglycerol synthesis Annu. Rev. Nutr. 20 2000 77 103
75. H. Pownall Cellular transport of nonesterified fatty acids J. Mol. Neurosci. 16 2001 109 115
76. A. Cohen Simonsen, U. Bernchou Jensen, N.J. Færgeman, J. Knudsen, and O.G. Mouritsen Acyl-coenzyme A organizes laterally in membranes and is recognized specifically by acyl-coenzyme A binding protein FEBS Lett. 552 2003 253 258
77. Z. Liu, Y. Huang, Y. Zhang, D. Chen, and Y.Q. Zhang 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 2011 2052 2063
78. F. Cornejo Maciel, P. Maloberti, I. Neuman, F. Cano, R. Castilla, F. Castillo, C. Paz, and E.J. Podestá An arachidonic acid-preferring acyl-CoA synthetase is a hormone-dependent and obligatory protein in the signal transduction pathway of steroidogenic hormones J. Mol. Endocrinol. 34 2005 655 666
79. P.G. Mele, A. Duarte, C. Paz, A. Capponi, and E.J. Podesta Role of intramitochondrial arachidonic acid and acyl-CoA synthetase 4 in angiotensin ii-regulated aldosterone synthesis in NCI-H295R adrenocortical cell line Endocrinology 153 2012 3284 3294
80. M.E. Smith, E. Saraceno, F. Capani, and R. Castilla Long-chain acyl-CoA synthetase 4 is regulated by phosphorylation Biochem. Biophys. Res. Commun. 2012 2012
81. A. Duarte, A.F. Castillo, R. Castilla, P. Maloberti, C. Paz, E.J. Podestá, and F. Cornejo Maciel An arachidonic acid generation/export system involved in the regulation of cholesterol transport in mitochondria of steroidogenic cells FEBS Lett. 581 2007 4023 4028
82. D. Wang, and R.N. DuBois Eicosanoids and cancer Nat. Rev. Cancer 10 2010 181 193
83. Y.C. Liang, C.H. Wu, J.S. Chu, C.K. Wang, L.F. Hung, Y.J. Wang, Y.S. Ho, J.G. Chang, and S.Y. Lin Involvement of fatty acid-CoA ligase 4 in hepatocellular carcinoma growth: roles of cyclic AMP and p38 mitogen-activated protein kinase World J. Gastroenterol. 11 2005 2557 2563
84. Y. Cao, K.B. Dave, T.P. Doan, and S.M. Prescott Fatty acid CoA ligase 4 is up-regulated in colon adenocarcinoma Cancer Res. 61 2001 8429 8434
85. C. Hu, L. Chen, Y. Jiang, Y. Li, and S. Wang The effect of fatty acid-CoA ligase 4 on the growth of hepatic cancer cells Cancer Biol. Ther. 7 2008 131 134
86. P.M. Maloberti, A.B. Duarte, U.D. Orlando, M.E. Pasqualini, Á.R. Solano, C. López-Otín, and E.J. Podestá Functional interaction between acyl-CoA synthetase 4, lipooxygenases and cyclooxygenase-2 in the aggressive phenotype of breast cancer cells PLoS One 5 2010 e15540
87. V.A. Bankaitis, C.J. Mousley, and G. Schaaf The Sec14 superfamily and mechanisms for crosstalk between lipid metabolism and lipid signaling Trends Biochem. Sci. 35 2010 150 160