Long chain polyunsaturated fatty acid synthesis in a marine vertebrate: Ontogenetic and nutritional regulation of a fatty acyl desaturase with Δ4 activity

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1821, Issue 4, 2012, Pages 660-671

  Morais, Sofia ^a   Castanheira, Filipa ^b   Martinez Rubio, Laura ^c   Conceição, Luis E C ^b   Tocher, Douglas R ^c  

^a IRTA   (Spain)

^b UNIVERSITY OF ALGARVE   (Portugal)

^c UNIVERSITY OF STIRLING   (United Kingdom)

Author keywords

4 desaturase; Marine teleost; Ontogenesis; Polyunsaturated fatty acid synthesis; Solea senegalensis; Transcriptional regulation

Indexed keywords

ACYL COENZYME A DESATURASE; DOCOSAHEXAENOIC ACID; ICOSAPENTAENOIC ACID; POLYUNSATURATED FATTY ACID;

ARTICLE; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME REGULATION; FATTY ACID SYNTHESIS; LARVAL DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; ONTOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOLEA SENEGALENSIS; TELEOST; TRANSCRIPTION REGULATION;

ACETYLTRANSFERASES; AMINO ACID SEQUENCE; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; FATTY ACID DESATURASES; FATTY ACIDS; FATTY ACIDS, UNSATURATED; FISH PROTEINS; FLATFISHES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LARVA; LIPIDS; MOLECULAR SEQUENCE DATA; PHYLOGENY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; TIME FACTORS;

SOLEA SENEGALENSIS; TELEOSTEI; VERTEBRATA;

EID: 84857679091     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2011.12.011     Document Type: Article

References (54)

1. M.V. Bell, R.S. Batty, J.R. Dick, K. Fretwell, J.C. Navarro, and J.R. Sargent Dietary deficiency of docosahexaenoic acid impairs vision at low light intensities in juvenile herring (Clupea harengus L.) Lipids 30 1995 443 449
2. M.V. Bell, and D.R. Tocher Molecular species composition of the major phospholipids in brain and retina from rainbow trout (Salmo gairdneri). Occurrence of high levels of di-(n - 3)polyunsaturated fatty acid species Biochem. J. 264 1989 909 915 (Pubitemid 20023467)
3. A. Gil, M. Ramirez, and M. Gil Role of long-chain polyunsaturated fatty acids in infant nutrition Eur. J. Clin. Nutr. 57 Suppl. 1 2003 S31 S34
4. B. Koletzko, E. Lien, C. Agostoni, H. Böhles, C. Campoy, I. Cetin, T. Decsi, J.W. Dudenhausen, C. Dupont, S. Forsyth, I. Hoesli, W. Holzgreve, A. Lapillonne, G. Putet, N.J. Secher, M. Symonds, H. Szajewska, P. Willatts, R. Uauy World Association of Perinatal Medicine Dietary Guidelines Working Group The roles of long-chain polyunsaturated fatty acids in pregnancy, lactation and infancy: review of current knowledge and consensus recommendations J. Perinat. Med. 36 2008 5 14
5. D.B. Jump, S.D. Clarke, A. Thelen, M. Liimatta, B. Ren, and M. Badin Dietary polyunsaturated fatty acid regulation of gene transcription Prog. Lipid Res. 35 1996 227 241 (Pubitemid 27092443)
6. P.C. Calder Dietary modification of inflammation with lipids Proc. Nutr. Soc. 61 2002 345 358 (Pubitemid 34982924)
7. N.D. Riediger, R.A. Othman, M. Suh, and M.H. Moghadasian A systemic review of the roles of n - 3 fatty acids in health and disease J. Am. Diet. Assoc. 109 2009 668 679
8. D.R. Tocher Fatty acid requirements in ontogeny of marine and freshwater fish Aquacult. Res. 41 2010 717 732
9. X. Zheng, I. Seiliez, N. Hastings, D.R. Tocher, S. Panserat, C.A. Dickson, P. Bergot, and A.J. Teale Characterisation and comparison of fatty acyl Δ6 desaturase cDNAs from freshwater and marine teleost fish species Comp. Biochem. Physiol. 139B 2004 269 279 (Pubitemid 39304177)
10. X. Zheng, D.R. Tocher, C.A. Dickson, J.R. Dick, J.G. Bell, and A.J. Teale Highly unsaturated fatty acid synthesis in vertebrates: new insights with the cloning and characterisation of a Δ6 desaturase of Atlantic salmon Lipids 40 2005 13 24
11. N. Hastings, M. Agaba, D.R. Tocher, M.J. Leaver, J.R. Dick, J.R. Sargent, and A.J. Teale A vertebrate fatty acid desaturase with Δ5 and Δ6 activities Proc. Natl. Acad. Sci. U. S. A. 98 2001 14304 14309 (Pubitemid 33121387)
12. N. Hastings, M.K. Agaba, D.R. Tocher, X. Zheng, C.A. Dickson, J.R. Dick, and A.J. Teale Molecular cloning and functional characterization of fatty acyl desaturase and elongase cDNAs involved in the production of eicosapentaenoic and docosahexaenoic acids from α-linolenic acid in Atlantic salmon (Salmo salar) Mar. Biotechnol. 6 2005 463 474 (Pubitemid 40580413)
13. Y. Li, O. Monroig, L. Zhang, S. Wang, X. Zheng, J.R. Dick, C. You, and D.R. Tocher Vertebrate fatty acyl desaturase with Δ4 activity Proc. Natl. Acad. Sci. U. S. A. 107 2010 16840 16845
14. A. Voss, M. Reinhart, S. Sankarappa, and H. Sprecher The metabolism of 7, 10, 13, 16, 19-docosapentaenoic acid to 4, 7, 10, 13, 16, 19-docosahexaenoic acid in rat liver is independent of a 4-desaturase J. Biol. Chem. 266 1991 19995 20000 (Pubitemid 21908418)
15. FAO The State of World Fisheries and Aquaculture 2008 2009 Food and Agriculture Organization of the United Nations Rome
16. B.E. Torstensen, and D.R. Tocher The Effects of fish oil replacement on lipid metabolism of fish G.M. Turchini, W.-K. Ng, D.R. Tocher, Fish Oil Replacement and Alternative Lipid Sources in Aquaculture Feeds 2010 Taylor & Francis, CRC Press Boca Raton 405 437
17. M.T. Dinis Aspects of the potential of Solea senegalensis Kaup for aquaculture: larval rearing and weaning to artificial diets Aquacult. Fish. Manage. 23 1992 515 520
18. M.T. Dinis, L. Ribeiro, F. Soares, and C. Sarasquete A review on the cultivation potential of Solea senegalensis in Spain and in Portugal Aquaculture 176 1999 27 38 (Pubitemid 29247499)
19. P. Borges, B. Oliveira, S. Casal, J. Dias, L. Conceição, and L.M. Valente Dietary lipid level affects growth performance and nutrient utilisation of Senegalese sole (Solea senegalensis) juveniles Br. J. Nutr. 102 2009 1007 1014
20. J.M.G. Silva, M. Espe, L.E.C. Conceição, J. Dias, and L.M.P. Valente Senegalese sole juveniles (Solea senegalensis Kaup, 1858) grow equally well on diets devoid of fish meal provided the dietary amino acids are balanced Aquaculture 296 2009 309 317
21. J.R. Sargent, L.A. McEvoy, and J.G. Bell Requirements, presentation and sources of polyunsaturated fatty acids in marine fish larval feeds Aquaculture 155 1997 117 128
22. S. Morais, L. Narciso, E. Dores, and P. Pousão-Ferreira Lipid enrichment for Senegalese sole (Solea senegalensis) larvae: effect on larval growth, survival and fatty acid profile Aquacult. Int. 12 2004 281 298 (Pubitemid 39073699)
23. M. Villalta, A. Estévez, M.P. Bransden, and J.G. Bell The effect of graded concentrations of dietary DHA on growth, survival and tissue fatty acid profile of Senegal sole (Solea senegalensis) larvae during the Artemia feeding period Aquaculture 249 2005 353 365 (Pubitemid 41187887)
24. S. Morais, G. Mourente, A. Ortega, J.A. Tocher, and D.R. Tocher Expression of fatty acyl desaturase and elongase genes, and evolution of DHA:EPA ratio during development of unfed larvae of Atlantic bluefin tuna (Thunnus thynnus L.) Aquaculture 313 2010 129 139
25. N. Saitou, and M. Nei The neighbor-joining method. A new method for reconstructing phylogenetic trees Mol. Biol. Evol. 4 1987 406 425
26. K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods Mol. Biol. Evol. 2011 10.1093/molbev/msr121
27. L.E.C. Conceição, L. Ribeiro, S. Engrola, C. Aragão, S. Morais, M. Lacuisse, F. Soares, and M.T. Dinis Nutritional physiology during development of Senegalese sole (Solea senegalensis) Aquaculture 268 2007 64 81 (Pubitemid 47017385)
28. S. Engrola, L. Figueira, L.E.C. Conceição, P.J. Gavaia, L. Ribeiro, and M.T. Dinis Co-feeding in Senegalese sole larvae with inert diet from mouth opening promotes growth at weaning Aquaculture 288 2009 264 272
29. C. Infante, M.P. Matsuoka, E. Asensio, J.P. Cañavate, M. Reith, and M. Manchado Selection of housekeeping genes for gene expression studies in larvae from flatfish using real-time PCR BMC Mol. Biol. 9 2008 28
30. J. Vandesompele, K. De Preter, F. Pattyn, B. Poppe, N. Van Roy, A. De Paepe, and F. Speleman Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes Genome Biol. 3 2002 34.1 34.11
31. J. Folch, M. Lees, and G.H. Sloane-Stanley A simple method for the isolation and purification of total lipides from animal tissues J. Biol. Chem. 226 1957 497 509
32. W.W. Christie Lipid Analysis 3rd Edition 2003 The Oily Press Bridgewater, UK
33. H. Sprecher, D.L. Luthria, B.S. Mohammed, and S.P. Baykousheva Reevaluation of the pathways for the biosynthesis of polyunsaturated fatty acids J. Lipid Res. 36 1995 2471 2477 (Pubitemid 26028787)
34. X. Qiu, H. Hong, and S.L. MacKenzie Identification of a Delta 4 fatty acid desaturase from Thraustochytrium sp. involved in the biosynthesis of docosahexanoic acid by heterologous expression in Saccharomyces cerevisiae and Brassica juncea J. Biol. Chem. 276 2001 31561 31566
35. T. Tonon, D. Harvey, T.R. Larson, and I.A. Graham Identification of a very long chain polyunsaturated fatty acid delta4-desaturase from the microalga Pavlova lutheri FEBS Lett. 553 2003 440 444 (Pubitemid 37315646)
36. T. Tonon, O. Sayanova, L.V. Michaelson, R. Qing, D. Harvey, T.R. Larson, Y. Li, J.A. Napier, and I.A. Graham Fatty acid desaturases from the microalga Thalassiosira pseudonana FEBS J. 272 2005 3401 3412 (Pubitemid 40979310)
37. S.L. Pereira, A.E. Leonard, Y.S. Huang, L.T. Chuang, and P. Mukerji Identification of two novel microalgal enzymes involved in the conversion of the omega3-fatty acid, eicosapentaenoic acid, into docosahexaenoic acid Biochem. J. 384 2004 357 366 (Pubitemid 39656248)
38. A. Meyer, P. Cirpus, C. Ott, R. Schlecker, U. Zähringer, and E. Heinz Biosynthesis of docosahexaenoic acid in Euglena gracilis: biochemical and molecular evidence for the involvement of a delta4-fatty acyl group desaturase Biochemistry 42 2003 9779 9788 (Pubitemid 36993151)
39. K.E. Tripodi, L.V. Buttigliero, S.G. Altabe, and A.D. Uttaro Functional characterization of front-end desaturases from trypanosomatids depicts the first polyunsaturated fatty acid biosynthetic pathway from a parasitic protozoan FEBS J. 273 2006 271 280
40. J.G. Metz, P. Roessler, D. Facciotti, C. Levering, F. Dittrich, M. Lassner, R. Valentine, K. Lardizabal, F. Domergue, A. Yamada, K. Yazawa, V. Knauf, and J. Browse Production of polyunsaturated fatty acids by polyketide synthases in both prokaryotes and eukaryotes Science 293 2001 290 293 (Pubitemid 32694743)
41. E. Garcia-Franquesa, A. Molinero, J. Valero, and R. Flos Influence of sex, age and season on the feeding habits of the flatfish Solea senegalensis Environ. Biol. Fish. 47 1996 289 298
42. H.N. Cabral Comparative feeding ecology of sympatric Solea solea and S. senegalensis, within the nursery areas of the Tagus estuary, Portugal J. Fish Biol. 57 2000 1550 1562 (Pubitemid 32013183)
43. M. Graeve, G. Kattner, and D. Piepenburg Lipids in Arctic benthos: does the fatty acid and alcohol composition reflect feeding and trophic interactions? Polar Biol. 18 1997 53 61
44. V.I. Kharlamenko, S.I. Kiyashko, S.A. Rodkina, and A.B. Imbs Determination of food sources of marine invertebrates from a subtidal sand community using analyses of fatty acids and stable isotopes Russ. J. Mar. Biol. 34 2008 101 109 (Pubitemid 351757045)
45. O.J. Luis, and A.M. Passos Seasonal changes in lipid content and composition of the polychaete Nereis (Hediste) diversicolor Comp. Biochem. Physiol. 111B 1995 579 586
46. R.G. Ackman, and D.M. Nash Lipids and fatty acids of Corophium volutator from Minas basin Proc. N.S. Inst. Sci. 29 1979 501 516
47. S.A. Bradshaw, S.C.M. O'Hara, E.D.S. Corner, and G. Eglinton Effects on dietary lipids of the marine bivalve Scrobicularia plana feeding in different modes J. Mar. Biol. Assoc. U. K. 71 1991 635 653
48. K. Hashimoto, A.C. Yoshizawa, S. Okuda, K. Kuma, S. Goto, and M. Kanehisa The repertoire of desaturases and elongases reveals fatty acid variations in 56 eukaryotic genomes J. Lipid Res. 49 2008 183 191
49. K. Hashimoto, A.C. Yoshizawa, K. Saito, T. Yamada, and M. Kanehisa The repertoire of desaturases for unsaturated fatty acid synthesis in 397 genomes Genome Inform. 17 2006 173 183
50. S. Morais, O. Monroig, X. Zheng, M.J. Leaver, and D.R. Tocher Highly unsaturated fatty acid synthesis in Atlantic salmon: characterization of ELOVL5- and ELOVL2-like elongases Mar. Biotechnol. 1 2009 627 639
51. O. Monroig, J. Rotllant, E. Sánchez, J.M. Cerdá-Reverter, and D.R. Tocher Expression of long-chain polyunsaturated fatty acid (LC-PUFA) biosynthesis genes during zebrafish Danio rerio early embryogenesis Biochim. Biophys. Acta 1791 2009 1093 1101
52. C. Fernández-Díaz, M. Yúfera, J.P. Cañavate, F.J. Moyano, F.J. Alarcón, and M. Díaz Growth and physiological changes during metamorphosis of Senegal sole reared in the laboratory J. Fish Biol. 58 2001 1 13
53. M. Naz The changes in the biochemical compositions and enzymatic activities of rotifer (Brachionus plicatilis, Müller) and Artemia during the enrichment and starvation periods Fish Physiol. Biochem. 34 2008 391 404
54. V.C. Nhu, K. Dierckens, T.H. Nguyen, M.T. Tran, and P. Sorgeloos Can umbrella-stage Artemia franciscana substitute enriched rotifers for Cobia (Rachycentron canadum) fish larvae? Aquaculture 289 2009 64 69