Regulation of mammalian desaturases by myristic acid: N-terminal myristoylation and other modulations

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1811, Issue 1, 2011, Pages 1-8

  Rioux, Vincent ^a   Pédrono, Frédérique ^a   Legrand, Philippe ^a  

^a Agrocampus French National Institute of Health and Medical Research   (France)

Author keywords

Dihydroceramide desaturase; Fatty acid desaturase; Myristic acid; N myristoylation; Protein acylation

Indexed keywords

CERAMIDE; COENZYME A; DIHYDROCERAMIDE DELTA4 DESATURASE 1; DIHYDROCERAMIDE DELTA4 DESATURASE 2; FATTY ACID DESATURASE 2; LONG CHAIN FATTY ACID COENZYME A LIGASE; MYRISTIC ACID; MYRISTOYL COENZYME A; OXYGENASE; POLYUNSATURATED FATTY ACID; PROTEIN N MYRISTOYLTRANSFERASE; SPHINGOLIPID; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; BIOAVAILABILITY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; FATTY ACID DESATURATION; FATTY ACID SYNTHESIS; HUMAN; MYRISTYLATION; NONHUMAN; PHOSPHOLIPID BILAYER; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; RNA TRANSLATION; SEQUENCE ALIGNMENT;

ACYL COENZYME A; ANIMALS; CARDIOVASCULAR DISEASES; CHOLESTEROL; CYTOCHROME-B(5) REDUCTASE; FATTY ACID DESATURASES; FATTY ACIDS, UNSATURATED; HUMANS; MYRISTIC ACID; PROTEIN PROCESSING, POST-TRANSLATIONAL;

ANIMALIA; EUKARYOTA; MAMMALIA;

EID: 78649763329     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2010.09.005     Document Type: Review

References (65)

1. V. Rioux, D. Catheline, M. Bouriel, and P. Legrand Dietary myristic acid at physiologically relevant levels increases the tissue content of C20:5 n-3 and C20:3 n-6 in the rat Reprod. Nutr. Dev. 45 2005 599 612
2. T.A. Hughes, M. Heimberg, X. Wang, H. Wilcox, S.M. Hughes, E.A. Tolley, D.M. Desiderio, and J.T. Dalton Comparative lipoprotein metabolism of myristate, palmitate, and stearate in normolipidemic men Metabolism 45 1996 1108 1118
3. V. Rioux, P. Lemarchal, and P. Legrand Myristic acid, unlike palmitic acid, is rapidly metabolized in cultured rat hepatocytes J. Nutr. Biochem. 11 2000 198 207
4. V. Rioux, and P. Legrand Saturated fatty acids: simple molecular structures with complex cellular functions Curr. Opin. Clin. Nutr. Metab. Care 10 2007 752 758
5. D.A. Towler, J.I. Gordon, S.P. Adams, and L. Glaser The biology and enzymology of eukaryotic protein acylation Annu. Rev. Biochem. 57 1988 69 99
6. D.R. Johnson, R.S. Bhatnagar, L.J. Knoll, and J.I. Gordon Genetic and biochemical studies of protein N-myristoylation Annu. Rev. Biochem. 63 1994 869 914
7. R.A. McIlhinney, K. Young, M. Egerton, R. Camble, A. White, and M. Soloviev Characterization of human and rat brain myristoyl-CoA:protein N-myristoyltransferase: evidence for an alternative splice variant of the enzyme Biochem. J. 333 Pt 3 1998 491 495
8. D.K. Giang, and B.F. Cravatt A second mammalian N-myristoyltransferase J. Biol. Chem. 273 1998 6595 6598
9. D.R. Rundle, R.V. Rajala, and R.E. Anderson Characterization of Type I and Type II myristoyl-CoA:protein N-myristoyltransferases with the Acyl-CoAs found on heterogeneously acylated retinal proteins Exp. Eye Res. 75 2002 87 97
10. V. Rioux, E. Beauchamp, F. Pedrono, S. Daval, D. Molle, D. Catheline, and P. Legrand Identification and characterization of recombinant and native rat myristoyl-CoA: protein N-myristoyltransferases Mol. Cell. Biochem. 286 2006 161 170
11. S.H. Yang, A. Shrivastav, C. Kosinski, R.K. Sharma, M.H. Chen, L.G. Berthiaume, L.L. Peters, P.T. Chuang, S.G. Young, and M.O. Bergo N-myristoyltransferase 1 is essential in early mouse development J. Biol. Chem. 280 2005 18990 18995
12. E. Beauchamp, V. Rioux, and P. Legrand New regulatory and signal functions for myristic acid Med. Sci. (Paris) 25 2009 57 63
13. J. Shanklin, J.E. Guy, G. Mishra, and Y. Lindqvist Desaturases: emerging models for understanding functional diversification of diiron-containing enzymes J. Biol. Chem. 284 2009 18559 18563
14. T. Aki, Y. Shimada, K. Inagaki, H. Higashimoto, S. Kawamoto, S. Shigeta, K. Ono, and O. Suzuki Molecular cloning and functional characterization of rat delta-6 fatty acid desaturase Biochem. Biophys. Res. Commun. 255 1999 575 579
15. H.P. Cho, M.T. Nakamura, and S.D. Clarke Cloning, expression, and nutritional regulation of the mammalian Delta-6 desaturase J. Biol. Chem. 274 1999 471 477
16. S. D'Andrea, H. Guillou, S. Jan, D. Catheline, J.N. Thibault, M. Bouriel, V. Rioux, and P. Legrand The same rat Delta6-desaturase not only acts on 18- but also on 24-carbon fatty acids in very-long-chain polyunsaturated fatty acid biosynthesis Biochem. J. 364 2002 49 55
17. A. Marquardt, H. Stohr, K. White, and B.H. Weber cDNA cloning, genomic structure, and chromosomal localization of three members of the human fatty acid desaturase family Genomics 66 2000 175 183
18. W.J. Park, K.S. Kothapalli, H.T. Reardon, L.Y. Kim, and J.T. Brenna Novel fatty acid desaturase 3 (FADS3) transcripts generated by alternative splicing Gene 446 2009 28 34
19. F. Pedrono, H. Blanchard, M. Kloereg, S. D'Andrea, S. Daval, V. Rioux, and P. Legrand The fatty acid desaturase 3 gene encodes for different FADS3 protein isoforms in mammalian tissues J. Lipid Res. 2009
20. P. Ternes, S. Franke, U. Zahringer, P. Sperling, and E. Heinz Identification and characterization of a sphingolipid delta 4-desaturase family J. Biol. Chem. 277 2002 25512 25518
21. Y. Mizutani, A. Kihara, and Y. Igarashi Identification of the human sphingolipid C4-hydroxylase, hDES2, and its up-regulation during keratinocyte differentiation FEBS Lett. 563 2004 93 97
22. E. Beauchamp, D. Goenaga, J. Le Bloc'h, D. Catheline, P. Legrand, and V. Rioux Myristic acid increases the activity of dihydroceramide Delta4-desaturase 1 through its N-terminal myristoylation Biochimie 89 2007 1553 1561
23. S. Maurer-Stroh, M. Gouda, M. Novatchkova, A. Schleiffer, G. Schneider, F.L. Sirota, M. Wildpaner, N. Hayashi, and F. Eisenhaber MYRbase: analysis of genome-wide glycine myristoylation enlarges the functional spectrum of eukaryotic myristoylated proteins Genome Biol. 5 2004 R21
24. A. Enomoto, F. Omae, M. Miyazaki, Y. Kozutsumi, T. Yubisui, and A. Suzuki Dihydroceramide:sphinganine C-4-hydroxylation requires Des2 hydroxylase and the membrane form of cytochrome b5 Biochem. J. 397 2006 289 295
25. H. Guillou, S. D'Andrea, V. Rioux, R. Barnouin, S. Dalaine, F. Pedrono, S. Jan, and P. Legrand Distinct roles of endoplasmic reticulum cytochrome b5 and fused cytochrome b5-like domain for rat Delta6-desaturase activity J. Lipid Res. 45 2004 32 40
26. R. Jeffcoat, P.R. Brawn, R. Safford, and A.T. James Properties of rat liver microsomal stearoyl-coenzyme A desaturase Biochem. J. 161 1977 431 437
27. F.S. Heinemann, and J. Ozols Stearoyl-CoA desaturase, a short-lived protein of endoplasmic reticulum with multiple control mechanisms Prostaglandins Leukot. Essent. Fatty Acids 68 2003 123 133
28. S. Colombo, R. Longhi, S. Alcaro, F. Ortuso, T. Sprocati, A. Flora, and N. Borgese N-myristoylation determines dual targeting of mammalian NADH-cytochrome b5 reductase to ER and mitochondrial outer membranes by a mechanism of kinetic partitioning J. Cell Biol. 168 2005 735 745
29. N. Borgese, D. Aggujaro, P. Carrera, G. Pietrini, and M. Bassetti A role for N-myristoylation in protein targeting: NADH-cytochrome b5 reductase requires myristic acid for association with outer mitochondrial but not ER membranes J. Cell Biol. 135 1996 1501 1513
30. J. Ozols, S.A. Carr, and P. Strittmatter Identification of the NH2-terminal blocking group of NADH-cytochrome b5 reductase as myristic acid and the complete amino acid sequence of the membrane-binding domain J. Biol. Chem. 259 1984 13349 13354
31. F. Omae, M. Miyazaki, A. Enomoto, M. Suzuki, Y. Suzuki, and A. Suzuki DES2 protein is responsible for phytoceramide biosynthesis in the mouse small intestine Biochem. J. 379 2004 687 695
32. A. Bielawska, H.M. Crane, D. Liotta, L.M. Obeid, and Y.A. Hannun Selectivity of ceramide-mediated biology. Lack of activity erythro- dihydroceramide J. Biol. Chem. 268 1993 26226 26232
33. T.I. Gudz, K.Y. Tserng, and C.L. Hoppel Direct inhibition of mitochondrial respiratory chain complex III by cell-permeable ceramide J. Biol. Chem. 272 1997 24154 24158
34. C. Garcia-Ruiz, A. Colell, M. Mari, A. Morales, and J.C. Fernandez-Checa Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. Role of mitochondrial glutathione J. Biol. Chem. 272 1997 11369 11377
35. L.J. Siskind, R.N. Kolesnick, and M. Colombini Ceramide channels increase the permeability of the mitochondrial outer membrane to small proteins J. Biol. Chem. 277 2002 26796 26803
36. E. Beauchamp, X. Tekpli, G. Marteil, D. Lagadic-Gossmann, P. Legrand, and V. Rioux N-Myristoylation targets dihydroceramide Delta4-desaturase 1 to mitochondria: partial involvement in the apoptotic effect of myristic acid Biochimie 91 2009 1411 1419
37. D. Ardail, I. Popa, K. Alcantara, A. Pons, J.P. Zanetta, P. Louisot, L. Thomas, and J. Portoukalian Occurrence of ceramides and neutral glycolipids with unusual long-chain base composition in purified rat liver mitochondria FEBS Lett. 488 2001 160 164
38. C. Michel, and G. van Echten-Deckert Conversion of dihydroceramide to ceramide occurs at the cytosolic face of the endoplasmic reticulum FEBS Lett. 416 1997 153 155
39. C. Bionda, J. Portoukalian, D. Schmitt, C. Rodriguez-Lafrasse, and D. Ardail Subcellular compartmentalization of ceramide metabolism: MAM (mitochondria-associated membrane) and/or mitochondria? Biochem. J. 382 2004 527 533
40. H. Shimeno, S. Soeda, M. Sakamoto, T. Kouchi, T. Kowakame, and T. Kihara Partial purification and characterization of sphingosine N-acyltransferase (ceramide synthase) from bovine liver mitochondrion-rich fraction Lipids 33 1998 601 605
41. S. El Bawab, P. Roddy, T. Qian, A. Bielawska, J.J. Lemasters, and Y.A. Hannun Molecular cloning and characterization of a human mitochondrial ceramidase J. Biol. Chem. 275 2000 21508 21513
42. H. Van Overloop, S. Gijsbers, and P.P. Van Veldhoven Further characterization of mammalian ceramide kinase: substrate delivery and (stereo)specificity, tissue distribution, and subcellular localization studies J. Lipid Res. 47 2006 268 283
43. J. Stiban, L. Caputo, and M. Colombini Ceramide synthesis in the endoplasmic reticulum can permeabilize mitochondria to proapoptotic proteins J. Lipid Res. 49 2008 625 634
44. S. Jan, H. Guillou, S. D'Andrea, S. Daval, M. Bouriel, V. Rioux, and P. Legrand Myristic acid increases delta6-desaturase activity in cultured rat hepatocytes Reprod. Nutr. Dev. 44 2004 131 140
45. P. Strittmatter, J.M. Kittler, J.E. Coghill, and J. Ozols Interaction of non-myristoylated NADH-cytochrome b5 reductase with cytochrome b5-dimyristoylphosphatidylcholine vesicles J. Biol. Chem. 268 1993 23168 23171
46. V. Rioux, D. Catheline, E. Beauchamp, J. Le Bloc'h, F. Pédrono, and P. Legrand Substitution of dietary oleic for myristic acid increases the tissue storage of alfa-linolenic acid and the concentration of docosahexaenoic acid in brain, red blood cells and plasma in the rat Animal 2 2008 636 644
47. H. Dabadie, E. Peuchant, M. Bernard, P. LeRuyet, and F. Mendy Moderate intake of myristic acid in sn-2 position has beneficial lipidic effects and enhances DHA of cholesteryl esters in an interventional study J. Nutr. Biochem. 16 2005 375 382
48. L. Xie, and S.M. Innis Genetic variants of the FADS1 FADS2 gene cluster are associated with altered (n-6) and (n-3) essential fatty acids in plasma and erythrocyte phospholipids in women during pregnancy and in breast milk during lactation J. Nutr. 138 2008 2222 2228
49. M. Miyazaki, and J.M. Ntambi Role of stearoyl-coenzyme A desaturase in lipid metabolism Prostaglandins Leukot. Essent. Fatty Acids 68 2003 113 121
50. P.A. Schenck, H. Rakoff, and E.A. Emken Delta 8 desaturation in vivo of deuterated eicosatrienoic acid by mouse liver Lipids 31 1996 593 600
51. M. Hamosh, and J. Bitman Human milk in disease: lipid composition Lipids 27 1992 848 857
52. L.X. Wang, T.L. Kaduce, and A.A. Spector Myristic acid utilization and processing in BC3H1 muscle cells J. Biol. Chem. 266 1991 13883 13890
53. E.E. Mosley, and M.A. McGuire Methodology for the in vivo measurement of the delta9-desaturation of myristic, palmitic, and stearic acids in lactating dairy cattle Lipids 42 2007 939 945
54. A.C. Awad, H.S. Shin, D.R. Romsos, and J.I. Gray Direct desaturation of free myristic acid by hen liver microsomal Delta9-desaturase without prior activation to myristoyl-CoA derivative J. Agric. Food Chem. 52 2004 3194 3201
55. P. Legrand, D. Catheline, V. Rioux, and G. Durand Lauric acid is desaturated to 12:1n-3 by hepatocytes and rat liver homogenates Lipids 37 2002 569 572
56. H. Guillou, V. Rioux, D. Catheline, J.N. Thibault, M. Bouriel, S. Jan, S. D'Andrea, and P. Legrand Conversion of hexadecanoic acid to hexadecenoic acid by rat Delta 6-desaturase J. Lipid Res. 44 2003 450 454
57. T.A. Neubert, R.S. Johnson, J.B. Hurley, and K.A. Walsh The rod transducin alpha subunit amino terminus is heterogeneously fatty acylated J. Biol. Chem. 267 1992 18274 18277
58. K. Kokame, Y. Fukada, T. Yoshizawa, T. Takao, and Y. Shimonishi Lipid modification at the N terminus of photoreceptor G-protein alpha-subunit Nature 359 1992 749 752
59. J.C. DeMar Jr., T.G. Wensel, and R.E. Anderson Biosynthesis of the unsaturated 14-carbon fatty acids found on the N termini of photoreceptor- specific proteins J. Biol. Chem. 271 1996 5007 5016
60. J.C. DeMar Jr., and R.E. Anderson Identification and quantitation of the fatty acids composing the CoA ester pool of bovine retina, heart, and liver J. Biol. Chem. 272 1997 31362 31368
61. A. Pinilla, F. Camps, and G. Fabrias Cryptoregiochemistry of the delta11-myristoyl-CoA desaturase involved in the biosynthesis of Spodoptera littoralis sex pheromone Biochemistry 38 1999 15272 15277
62. O. Tsfadia, A. Azrielli, L. Falach, A. Zada, W. Roelofs, and A. Rafaeli Pheromone biosynthetic pathways: PBAN-regulated rate-limiting steps and differential expression of desaturase genes in moth species Insect Biochem. Mol. Biol. 38 2008 552 567
63. V. Rioux, D. Catheline, and P. Legrand In rat hepatocytes, myristic acid occurs through lipogenesis, palmitic shortening and lauric acid elongation Animal 1 2007 820 826
64. A. Wolk, M. Furuheim, and B. Vessby Fatty acid composition of adipose tissue and serum lipids are valid biological markers of dairy fat intake in men J. Nutr. 131 2001 828 833
65. D.D. Martin, G.L. Vilas, J.A. Prescher, G. Rajaiah, J.R. Falck, C.R. Bertozzi, and L.G. Berthiaume Rapid detection, discovery, and identification of post-translationally myristoylated proteins during apoptosis using a bio-orthogonal azidomyristate analog FASEB J. 22 2008 797 806