Generation of membrane diversity by lysophospholipid acyltransferases

Journal of Biochemistry

Volumn 154, Issue 1, 2013, Pages 21-28

  Shindou, Hideo ^a,b   Hishikawa, Daisuke ^a   Harayama, Takeshi ^a   Eto, Miki ^a   Shimizu, Takao ^a  

^a NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Lands' cycle; LPCAT; LPLAT; lyso PAFAT; PAF

Indexed keywords

1 ACYLGLYCEROPHOSPHATE ACYLTRANSFERASE; ACYLTRANSFERASE; FAT DROPLET; LYSOPHOSPHOLIPID; LYSOPHOSPHOLIPID ACYLTRANSFERASE; PHOSPHOLIPASE A2; UNCLASSIFIED DRUG;

APOPTOSIS; CELL DIFFERENTIATION; CELL MATURATION; CELL MEMBRANE; CRYSTALLIZATION; ENDOPLASMIC RETICULUM; GENE OVEREXPRESSION; GERM CELL; GOLGI COMPLEX; HUMAN; LIPID COMPOSITION; MICROGLIA; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOLECULAR CLONING; NERVE FIBER GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; REVIEW; SITE DIRECTED MUTAGENESIS;

LANDS' CYCLE; LPCAT; LPLAT; LYSO-PAFAT; PAF;

1-ACYLGLYCEROPHOSPHOCHOLINE O-ACYLTRANSFERASE; AMINO ACID MOTIFS; ANIMALS; CELL MEMBRANE; HUMANS; MEMBRANE FLUIDITY; MEMBRANE LIPIDS; METABOLIC NETWORKS AND PATHWAYS; MICE; MODELS, BIOLOGICAL;

EID: 84879913749     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvt048     Document Type: Review

References (56)

1. Ishii, S. and Shimizu, T. (2000) Platelet-activating factor (PAF) receptor and genetically engineered PAF receptor mutant mice. Prog. Lipid Res. 39, 41-82 (Pubitemid 30145442)
2. Shimizu, T. (2009) Lipid mediators in health and disease: enzymes and receptors as therapeutic targets for the regulation of immunity and inflammation. Annu. Rev. Pharmacol. 49, 123-150
3. Yamashita, A., Sugiura, T., and Waku, K. (1997) Acyltransferases and transacylases involved in fatty acid remodeling ofphospholipids and metabolism ofbio-active lipids in mammalian cells. J. Biochem. 122, 1-16 (Pubitemid 27346216)
4. 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 (Pubitemid 351158912)
5. Schlame, M., Rua, D., and Greenberg, M.L. (2000) The biosynthesis and functional role of cardiolipin. Prog. Lipid Res. 39, 257-288 (Pubitemid 30224706)
6. Kennedy, E.P. and Weiss, S.B. (1956) The function of cytidine coenzymes in the biosynthesis of phospholipides. J. Biol. Chem. 222, 193-214
7. Lands, W.E. (1958) Metabolism ofglycerolipides; a com-parison of lecithin and triglyceride synthesis. J. Biol. Chem. 231, 883-888
8. Waku, K. and Nakazawa, Y. (1972) Acyltransferae activity to 1-acyl-, 1-O-alkenyl-, and 1-O-alkyl-glycero-3-phosphorylcholine in Ehrlich ascites tumor cells. J. Biochem. 72, 495-497
9. Lands, W.E. (2000) Stories about acyl chains. Biochim. Biophys. Acta 1483, 1-14
10. Shindou, H. and Shimizu, T. (2009) Acyl-Co A:lysophospholipid acyltransferases. J. Biol. Chem. 284, 1-5
11. Coleman, R.A. and Lee, D.P. (2004) Enzymes oftriacyl-glycerol synthesis and their regulation. Prog. Lipid Res. 43, 134-176 (Pubitemid 37492937)
12. Yuki, K., Shindou, H., Hishikawa, D., and Shimizu, T. (2009) Characterization of mouse lysophosphatidic acid acyltransferase 3: an enzyme with dual functions in the testis. J. Lipid Res. 50, 860-869
13. Koeberle, A., Shindou, H., Harayama, T., and Shimizu, T. (2010) Role oflysophosphatidic acid acyltransferase 3 for the supply of highly polyunsaturated fatty acids in TM4 Sertoli cells. FASEB J. 24, 4929-4938
14. Koeberle, A., Shindou, H., Harayama, T., Yuki, K., and Shimizu, T. (2012) Polyunsaturated fatty acids are incor-porated into maturating male mouse germ cells by lyso-phosphatidic acid acyltransferase 3. FASEB J. 26, 169-180
15. Cao, J., Liu, Y., Lockwood, J., Burn, P., and Shi, Y. (2004) A novel cardiolipin-remodeling pathway revealed by a gene encoding an endoplasmic reticulum-associated acyl-Co A:lysocardiolipin acyltransferase (ALCAT1) in mouse. J. Biol. Chem. 279, 31727-31734 (Pubitemid 39037844)
16. Zhao, Y., Chen, Y.Q., Li, S., Konrad, R.J., and Cao, G. (2009) The microsomal cardiolipin remodeling enzyme acyl-Co A lysocardiolipin acyltransferase is an acyltrans-ferase of multiple anionic lysophospholipids. J. Lipid Res. 50, 945-956
17. Li, J., Romestaing, C., Han, X., Li, Y., Hao, X., Wu, Y., Sun, C., Liu, X., Jefferson, L.S., Xiong, J., Lanoue, K.F., Chang, Z., Lynch, C.J., Wang, H., and Shi, Y. (2010) Cardiolipin remodeling by ALCAT1 links oxidative stress and mitochondrial dysfunction to obesity. Cell Metabol. 12, 154-165
18. Schlame, M., Kelley, R.I., Feigenbaum, A., Towbin, J.A., Heerdt, P.M., Schieble, T., Wanders, R.J., Di Mauro, S., and Blanck, T.J. (2003) Phospholipid abnormalities in children with Barth syndrome. J. Am. Coll. Cardiol. 42, 1994-1999 (Pubitemid 37485578)
19. Imae, R., Inoue, T., Nakasaki, Y., Uchida, Y., Ohba, Y., Kono, N., Nakanishi, H., Sasaki, T., Mitani, S., and Arai, H. (2012) LYCAT, a homologue of C. elegans acl-8, acl-9, and acl-10, determines the fatty acid com-position of phosphatidylinositol in mice. J. Lipid Res 53, 335-347
20. Yang, Y., Cao, J., and Shi, Y. (2004) Identification and characterization of a gene encoding human LPGAT1, an endoplasmic reticulum-associated lysophosphatidylgly-cerol acyltransferase. J. Biol. Chem. 279, 55866-55874 (Pubitemid 40066594)
21. Nakanishi, H., Shindou, H., Hishikawa, D., Harayama, T., Ogasawara, R., Suwabe, A., Taguchi, R., and Shimizu, T. (2006) Cloning and characterization of mouse lung-type acyl-Co A:lysophosphatidylcholine acyl-transferase 1 (LPCAT1): expression in alveolar type II cells and possible involvement in surfactant production. J. Biol. Chem. 281, 20140-20147 (Pubitemid 44065788)
22. Chen, X., Hyatt, B.A., Mucenski, M.L., Mason, R.J., and Shannon, J.M. (2006) Identification and character-ization of a lysophosphatidylcholine acyltransferase in alveolar type II cells. Proc. Natl Acad. Sci. U. S. A. 103, 11724-11729 (Pubitemid 44182518)
23. Stevens, T.P. and Sinkin, R.A. (2007) Surfactant replace-ment therapy. Chest 131, 1577-1582
24. Friedman, J.S., Chang, B., Krauth, D.S., Lopez, I., Waseem, N.H., Hurd, R.E., Feathers, K.L., Branham, K.E., Shaw, M., Thomas, G.E., Brooks, M.J., Liu, C., Bakeri, H.A., Campos, M.M., Maubaret, C., Webster, A.R., Rodriguez, I.R., Thompson, D.A., Bhattacharya, S.S., Koenekoop, R.K., Heckenlively, J.R., and Swaroop, A. (2010) Loss of lysophosphatidylcholine acyltransferase 1 leads to photoreceptor degeneration in rd11 mice. Proc. Natl Acad. Sci. U. S. A. 107, 15523-15528
25. Cheng, L., Han, X., and Shi, Y. (2009) A regulatory role of LPCAT1 in the synthesis ofinflammatory lipids, PAF and LPC, in the retina of diabetic mice. Am. J. Physiol. Endocrinol. Metab. 297, E1276-E1282
26. Bridges, J.P., Ikegami, M., Brilli, L.L., Chen, X., Mason, R.J., and Shannon, J.M. (2010) LPCAT1 regulates sur-factant phospholipid synthesis and is required for tran-sitioning to air breathing in mice. J. Clin. Invest. 120, 1736-1748
27. Harayama, T., Shindou, H., and Shimizu, T. (2009) Biosynthesis of phosphatidylcholine by human lysopho-sphatidylcholine acyltransferase 1. J. Lipid Res. 50, 1824-1831
28. Shindou, H., Hishikawa, D., Nakanishi, H., Harayama, T., Ishii, S., Taguchi, R., and Shimizu, T. (2007) A single enzyme catalyzes both platelet-activating factor produc-tion and membrane biogenesis of inflammatory cells. Cloning and characterization of acetyl-Co A:LYSO-PAF acetyltransferase. J. Biol. Chem. 282, 6532-6539 (Pubitemid 47100867)
29. Smith, W.L. and Langenbach, R. (2001) Why there are two cyclooxygenase isozymes. J. Clin. Invest. 107, 1491-1495 (Pubitemid 32574631)
30. Moessinger, C., Kuerschner, L., Spandl, J., Shevchenko, A., and Thiele, C. (2011) Human lysophosphatidylcho-line acyltransferases 1 and 2 are located in lipid droplets where they catalyze the formation of phosphatidylcho-line. J. Biol. Chem. 286, 21330-21339
31. Cao, J., Shan, D., Revett, T., Li, D., Wu, L., Liu, W., Tobin, J.F., and Gimeno, R.E. (2008) Molecular identi-fication of a novel mammalian brain isoform of acyl-Co A:lysophospholipid acyltransferase with prominent ethanolamine lysophospholipid acylating activity, LPEAT2. J. Biol. Chem. 283, 19049-19057
32. Lee, H.C., Inoue, T., Imae, R., Kono, N., Shirae, S., Matsuda, S., Gengyo-Ando, K., Mitani, S., and Arai, H. (2008) Caenorhabditis elegans mboa-7, a member of the MBOAT family, is required for selective incorpor-ation of polyunsaturated fatty acids into phosphatidyli-nositol. Mol. Biol. Cell 19, 1174-1184 (Pubitemid 351481829)
33. Hishikawa, D., Shindou, H., Kobayashi, S., Nakanishi, H., Taguchi, R., and Shimizu, T. (2008) Discovery of a lysophospholipid acyltransferase family essential for membrane asymmetry and diversity. Proc. Natl Acad. Sci. U. S. A. 105, 2830-2835 (Pubitemid 351723629)
34. Zhao, Y., Chen, Y.Q., Bonacci, T.M., Bredt, D.S., Li, S., Bensch, W.R., Moller, D.E., Kowala, M., Konrad, R.J., and Cao, G. (2008) Identification and characterization of a major liver lysophosphatidylcholine acyltransferase. J. Biol. Chem. 283, 8258-8265
35. Gijon, M., Riekhof, W., Zarini, S., Murphy, R., and Voelker, D. (2008) Lysophospholipid acyltransferases and arachidonate recycling in human neutrophils. J. Biol. Chem. 283, 30235-30245
36. Harayama, T., Shindou, H., Ogasawara, R., Suwabe, A., and Shimizu, T. (2008) Identification of a novel nonin-flammatory biosynthetic pathway of platelet-activating factor. J. Biol. Chem. 283, 11097-11106
37. Shindou, H., Eto, M., Morimoto, R., and Shimizu, T. (2009) Identification of membrane O-acyltransferase family motifs. Biochem. Biophys. Res. Commun. 383, 320-325
38. Schmidt, J. and Brown, W. (2009) Lysophosphatidic acid acyltransferase 3 regulates Golgi complex structure and function. J. Cell Biol 186, 211-218
39. Li, J., Liu, X., Wang, H., Zhang, W., Chan, D.C., and Shi, Y. (2012) Lysocardiolipin acyltransferase 1 (ALCAT1) controls mitochondrial DNA fidelity and biogenesis through modulation of MFN2 expression. Proc. Natl Acad. Sci. U. S. A. 109, 6975-6980
40. Liu, X., Ye, B., Miller, S., Yuan, H., Zhang, H., Tian, L., Nie, J., Imae, R., Arai, H., Li, Y., Cheng, Z., and Shi, Y. (2012) Ablation of ALCAT1 mitigates hypertrophic car-diomyopathy through effects on oxidative stress and mitophagy. Mol. Cell Biol. 32, 4493-4504
41. Lee, H.C., Inoue, T., Sasaki, J., Kubo, T., Matsuda, S., Nakasaki, Y., Hattori, M., Tanaka, F., Udagawa, O., Kono, N., Itoh, T., Ogiso, H., Taguchi, R., Arita, M., Sasaki, T., and Arai, H. (2012) LPIAT1 regulates arachi-donic acid content in phosphatidylinositol and is required for cortical lamination in mice. Mol. Biol. Cell 23, 4689-4700
42. Anderson, K.E., Kielkowska, A., Durrant, T.N., Juvin, V., Clark, J., Stephens, L.R., and Hawkins, P.T. (2013) Lysophosphatidylinositol- acyltransferase-1 (LPIAT1) is required to maintain physiological levels of Ptd Ins and Ptd Ins P2 in the mouse. Plo S One 8, e58425
43. Jain, S., Zhang, X., Khandelwal, P.J., Saunders, A.J., Cummings, B.S., and Oelkers, P. (2009) Characterization of human lysophospholipid acyltransferase 3. J. Lipid Res. 50, 1563-1570
44. Li, Z., Ding, T., Pan, X., Li, Y., Li, R., Sanders, P.E., Kuo, M.S., Hussain, M.M., Cao, G., and Jiang, X.C. (2012) Lysophosphatidylcholine acyltransferase 3 knock-down-mediated liver lysophosphatidylcholine accumula-tion promotes very low density lipoprotein production by enhancing microsomal triglyceride transfer protein expression. J. Biol. Chem. 287, 20122-20131
45. Mansilla, F., da Costa, K., Wang, S., Kruhøffer, M., Lewin, T.M., Orntoft, T.F., Coleman, R.A., and Birkenkamp-Demtroder, K. (2009) Lysophosphatidyl-choline acyltransferase 1 (LPCAT1) overexpression in human colorectal cancer. J. Mol. Med. 87, 85-97
46. Zhou, X., Lawrence, T.J., He, Z., Pound, C.R., Mao, J., and Bigler, S.A. (2012) The expression level oflysopho-sphatidylcholine acyltransferase 1 (LPCAT1) correlates to the progression of prostate cancer. Exp. Mol. Pathol. 92, 105-110
47. Shindou, H., Ishii, S., Yamamoto, M., Takeda, K., Akira, S., and Shimizu, T. (2005) Priming effect of lipo-polysaccharide on acetyl-coenzyme A:lyso-platelet-acti-vating factor acetyltransferase is My D88 and TRIF independent. J. Immunol. 175, 1177-1183 (Pubitemid 41095005)
48. Morimoto, R., Shindou, H., Oda, Y., and Shimizu, T. (2010) Phosphorylation oflysophosphatidylcholine acyl-transferase 2 at Ser34 enhances platelet-activating factor production in endotoxin-stimulated macrophages. J. Biol. Chem. 285, 29857-29862
49. Kihara, Y., Yanagida, K., Masago, K., Kita, Y., Hishikawa, D., Shindou, H., Ishii, S., and Shimizu, T. (2008) Platelet-activating factor production in the spinal cord of experimental allergic encephalomyelitis mice via the group IVA cytosolic phospholipase A2-lyso-PAFAT axis. J. Immunol. 181, 5008-5014
50. Okubo, M., Yamanaka, H., Kobayashi, K., Kanda, H., Dai, Y., and Noguchi, K. (2012) Up-regulation ofplate-let-activating factor synthases and its receptor in spinal cord contribute to development of neuropathic pain fol-lowing peripheral nerve injury. Mol. Pain 8, 1-11
51. Demeure, O., Lecerf, F., Duby, C., Desert, C., Ducheix, S., Guillou, H., and Lagarrigue, S. (2011) Regulation of LPCAT3 by LXR. Gene 470, 7-11
52. Eto, M., Shindou, H., Koeberle, A., Harayama, T., Yanagida, K., and Shimizu, T. (2012) Lysophosphatidyl-choline acyltransferase 3 is the key enzyme for incorpor-ating arachidonic acid into glycerophospholipids during adipocyte differentiation. Int. J. Mol. Sci. 13, 16267-16280
53. Yamazaki, T., Wakabayashi, M., Ikeda, E., Tanaka, S., Sakamoto, T., Mitsumoto, A., Kudo, N., and Kawashima, Y. (2012) Induction of 1-acylglyceropho-sphocholine acyltransferase genes by fibrates in the liver ofrats. Biol. Pharm. Bull. 35, 1509-1515
54. Tanaka, N., Matsubara, T., Krausz, K.W., Patterson, A.D., and Gonzalez, F.J. (2012) Disruption of phospholipid and bile acid homeostasis in mice with non-alcoholic steatohepatitis. Hepatology 56, 118-129
55. Matsubara, T., Tanaka, N., Sato, M., Kang, D.W., Krausz, K.W., Flanders, K.C., Ikeda, K., Luecke, H., Wakefield, L.M., and Gonzalez, F.J. (2012) TGF-beta-SMAD3 signaling mediates hepatic bile acid and phospholipid metabolism following lithocholic acid-induced liver injury. J. Lipid Res. 53, 2698-2707
56. Ostojic, O., O'Leary, M.F., Singh, K., Menzies, K.J., Vainshtein, A., and Hood, D.A. (2013) The ffects of chronic muscle use and disuse on cardiolipin metabolism. J. Appl. Physiol. 114, 444-452