The capacity for long-chain polyunsaturated fatty acid synthesis in a carnivorous vertebrate: Functional characterisation and nutritional regulation of a Fads2 fatty acyl desaturase with Δ4 activity and an Elovl5 elongase in striped snakehead (Channa striata)

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1851, Issue 3, 2015, Pages 248-260

  Kuah, Meng Kiat ^a   Jaya Ram, Annette ^b   Shu Chien, Alexander Chong ^b  

^a Kemeneterian Sains Teknologi dan Inovasi   (Malaysia)

^b SCHOOL OF PHYSICS   (Malaysia)

Author keywords

Biosynthesis; Channa striata; Elongase; Long chain polyunsaturated fatty acids; Nutritional regulation; 4 desaturase

Indexed keywords

ACYL COENZYME A DESATURASE; CARBOXYMETHYLCELLULOSE; CASEIN; CELLULOSE; COMPLEMENTARY DNA; CORN OIL; DOCOSAHEXAENOIC ACID; ELOVL5 ELONGASE; FADS2 DESATURASE; FISH OIL; FRESH WATER; ICOSAPENTAENOIC ACID; LINSEED OIL; LIPID; LONG CHAIN FATTY ACID; LONG CHAIN POLYUNSATURATED FATTY ACID; MINERAL; POLYUNSATURATED FATTY ACID; PROTEIN; STARCH; UNCLASSIFIED DRUG; VEGETABLE OIL; VERY LONG CHAIN FATTY ACID; VITAMIN; ACYLTRANSFERASE; FATTY ACID ELONGASES; FISH PROTEIN; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN TISSUE; CARNIVORE; CHANNA STRIATUS; CONTROLLED STUDY; DIET; DIETARY INTAKE; DRUG FORMULATION; DRUG UPTAKE; ENZYME ACTIVITY; FATTY ACID DESATURATION; FATTY ACID SYNTHESIS; GENE EXPRESSION; GENETIC RESOURCE; IN VITRO STUDY; IN VIVO STUDY; LIVER; MOLECULAR CLONING; MUSCLE; NONHUMAN; PISCIVORE; PRIORITY JOURNAL; RECEPTOR UPREGULATION; VERTEBRATE; AMINO ACID SEQUENCE; ANIMAL; ANTIBODY SPECIFICITY; BIOSYNTHESIS; CARNIVORY; CLASSIFICATION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PERCIFORMES; PHYLOGENY; SEQUENCE ALIGNMENT;

CHANNA STRIATA; TELEOSTEI; VERTEBRATA;

ACETYLTRANSFERASES; AMINO ACID SEQUENCE; ANIMALS; BRAIN; CARNIVORY; CLONING, MOLECULAR; DIET; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; ESCHERICHIA COLI; FATTY ACID DESATURASES; FISH OILS; FISH PROTEINS; GENE EXPRESSION REGULATION; LIVER; MOLECULAR SEQUENCE DATA; MUSCLES; ORGAN SPECIFICITY; PERCIFORMES; PHYLOGENY; PLANT OILS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

EID: 84920842146     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2014.12.012     Document Type: Article

References (59)

1. C.H.S. Ruxton, S.C. Reed, M.J.A. Simpson, K.J. Millington, The health bene fits of omega-3 polyunsaturated fatty acids: a review of the evidence, J. Hum. Nutr. Diet. 17 (2004) 449-459.
2. GISSI, Dietary supplementation with n-3 polyunsaturated fatty acids and vitamin E aftermyocardial infarction: results of the GISSI-Prevenzione trial, Lancet 354 (1999) 447-455.
3. G. Amminger, M.R. Schäfer, K. Papageorgiou, et al., Long-chain ω-3 fatty acids for indicated prevention of psychotic disorders: a randomized, placebo-controlled trial, Arch. Gen. Psychiatry 67 (2010) 146-154.
4. P.C. Calder, Immunomodulatory and anti-inflammatory effects of n-3 polyunsaturated fatty acids, Proc. Nutr. Soc. 55 (1996) 737-774.
5. M. Fleith, M.T. Clandinin, Dietary PUFA for preterm and term infants: review of clinical studies, Crit. Rev. Food Sci. Nutr. 45 (2005) 205-229.
6. M. Neuringer, G.J. Anderson, W.E. Connor, The essentiality of n-3 fatty acids for the development and function of the retina and brain, Annu. Rev. Nutr. 8 (1988) 517-541.
7. R.L. Naylor, R.J. Goldburg, J.H. Primavera, N. Kautsky, M.C.M. Beveridge, J. Clay, C. Folke, J. Lubchenco, H. Mooney, M. Troell, Effect of aquaculture on world fish supplies, Nature 405 (2000) 1017-1024.
8. G. Mourente, J.E. Good, J.G. Bell, Partial substitution of fish oil with rapeseed, linseed and olive oils in diets for European sea bass (Dicentrarchus labrax L.): effects on flesh fatty acid composition, plasma prostaglandins E2 and F2α, immune function and effectiveness of a fish oil finishing diet, Aquacult. Nutr. 11 (2005) 25-40.
9. J.G. Bell, R.J. Henderson, D.R. Tocher, F. McGhee, J.R. Dick, A. Porter, R.P. Smullen, J.R. Sargent, Substituting fish oil with crude palm oil in the diet of Atlantic salmon (Salmo salar) affects muscle fatty acid composition and hepatic fatty acid metabolism, J. Nutr. 132 (2002) 222-230.
10. A. Jakobsson, R. Westerberg, A. Jacobsson, Fatty acid elongases in mammals: their regulation and roles in metabolism, Prog. Lipid Res. 45 (2006) 237-249.
11. M. Agaba, D.R. Tocher, C.A.Dickson, J.R.Dick, A.J. Teale, Zebrafish cDNA encoding multifunctional fatty acid elongase involved in production of eicosapentaenoic (20:5n-3) and docosahexaenoic (22:6n-3) acids, Mar. Biotechnol. 6 (2004) 251-261.
12. M.K. Agaba, D.R. Tocher, X. Zheng, C.A. Dickson, J.R. Dick, A.J. Teale, Cloning and functional characterisation of polyunsaturated fatty acid elongases of marine and freshwater teleost fish, Comp. Biochem. Physiol. B 142 (2005) 342-352.
13. S. Morais, O. Monroig, X. Zheng, M. Leaver, D. Tocher, Highly unsaturated fatty acid synthesis in Atlantic salmon: characterization of ELOVL5- and ELOVL2-like elongases, Mar. Biotechnol. 11 (2009) 627-639.
14. X. Zheng, Z. Ding, Y. Xu, O. Monroig, S. Morais, D.R. Tocher, Physiological roles of fatty acyl desaturases and elongases in marine fish: characterisation of cDNAs of fatty acyl Δ6 desaturase and elovl5 elongase of cobia (Rachycentron canadum), Aquaculture 290 (2009) 122-131.
15. M.K. Gregory, V.H.L. See, R.A. Gibson, K.A. Schuller, Cloning and functional characterisation of a fatty acyl elongase from southern bluefi n tuna (Thunnus maccoyii), Comp. Biochem. Physiol. B 155 (2010) 178-185.
16. G. Carmona-Antonanzas, D.R. Tocher, J.B. Taggart, M.J. Leaver, An evolutionary perspective on Elovl5 fatty acid elongase: comparison of northern pike and duplicated paralogs from Atlantic salmon, BMC Evol. Biol. 13 (2013) 1-13.
17. S. Morais, F. Castanheira, L.Martinez-Rubio, L.E.C. Conceic¸ão, D.R. Tocher, Long chain polyunsaturated fatty acid synthesis in a marine vertebrate: ontogenetic and nutritional regulation of a fatty acyl desaturase with Δ14 activity, BBA-Mol. Cell Biol. Lipids 1821 (2012) 660-671.
18. Ó. Monroig, D.R. Tocher, F. Hontoria, J.C. Navarro, Functional characterisation of a Fads2 fatty acyl desaturase with Δ6/Δ8 activity and an Elovl5 with C16, C18 and C20 elongase activity in the anadromous teleost meagre ( Argyrosomus regius), Aquaculture 412-413 (2013) 14-22.
19. O. Monroig, J. Rotllant, E. Sanchez, J.M. Cerda-Reverter, D.R. Tocher, Expression of long-chain polyunsaturated fatty acid (LC-PUFA) biosynthesis genes during zebrafish Danio rerio early embryogenesis, BBA-Mol. Cell Biol. Lipids 1791 (2009) 1093-1101.
20. M.K. Gregory, M.J. James, Rainbow trout (Oncorhynchus mykiss) Elovl5 and Elovl2 differ in selectivity for elongation of omega-3 docosapentaenoic acid, BBA-Mol. Cell Biol. Lipids 1841 (2014) 1656-1660.
21. D. Tocher, X. Zheng, C. Schlechtriem, N. Hastings, J. Dick, A. Teale, Highly unsaturated fatty acid synthesis in marine fish: cloning, functional characterization, and nutritional regulation of fatty acyl Ä6 desaturase of Atlantic cod (Gadus morhua L.), Lipids 41 (2006) 1003-1016.
22. N. Hastings, M.K. Agaba, D.R. Tocher, X. Zheng, C.A. Dickson, J.R. Dick, 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.
23. N. Hastings,M. Agaba, D.R. Tocher, M.J. Leaver, J.R. Dick, J.R. Sargent, A.J. Teale, A vertebrate fatty acid desaturase with Δ5 and Δ6 activities, Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 14304-14309.
24. Y. Li, O. Monroig, L. Zhang, S. Wang, X. Zheng, J.R. Dick, C. You, D.R. Tocher, Vertebrate fatty acyl desaturase with Δ 4 activity, Proc. Natl. Acad. Sci. U. S. A. 107 (2010) 16840-16845.
25. J. Fonseca-Madrigal, J.C. Navarro, F. Hontoria, D.R. Tocher, C.A. Martínez-Palacios, Ó. Monroig, Diversification of substrate specificities in teleostei Fads2: characterization of Δ4 and Δ6Δ5 desaturases of Chirostoma estor, J. Lipid Res. 55 (2014) 1408-1419.
26. O. Monroig, Y. Li, D.R. Tocher, Delta-8 desaturation activity varies among fatty acyl desaturases of teleost fish: high activity in delta-6 desaturases of marine species, Comp. Biochem. Physiol. B 159 (2011) 206-213.
27. M.J. Leaver, J.M. Bautista, B.T. Björnsson, E. Jönsson, G. Krey, D.R. Tocher, B.E. Torstensen, Towards fi sh lipid nutrigenomics: current state and prospects for fin-fish aquaculture, Rev. Fish. Sci. 16 (2008) 73-94.
28. Ó. Monroig, S. Wang, L. Zhang, C. You, D.R. Tocher, Y. Li, Elongation of long-chain fatty acids in rabbitfish Siganus canaliculatus: cloning, functional characterisation and tissue distribution of Elovl5- and Elovl4-like elongases, Aquaculture 350-353 (2012) 63-70.
29. R.J. Henderson, M.T. Park, J.R. Sargent, The desaturation and elongation of 14C-labelled polyunsaturated fatty acids by pike ( Esox lucius L.) in vivo, Fish Physiol. Biochem. 14 (1995) 223-235.
30. M. Buzzi, R.J. Henderson, J.R. Sargent, The biosynthesis of docosahexaenoic acid [22:6(n-3)] from linolenic acid in primary hepatocytes isolated from wild northern pike, J. Fish Biol. 51 (1997) 1197-1208.
31. D.S. Francis, G.M. Turchini, P.L. Jones, S.S. DeSilva, Dietary lipid source modulates in vivo fatty acid metabolism in the freshwater fish, Murray cod (Maccullochella peelii peelii), J. Agric. Food Chem. 55 (2007) 1582-1591.
32. D.S. Francis, D.J. Peters, G.M. Turchini, Apparent in vivo d6 desaturase activity, efficiency, and affinity are affected by total dietary C18 PUFA in the freshwater fish Murray cod, J. Agric. Food Chem. 57 (2009) 4381-4390.
33. E. Henrotte, D. Kpogue, S.N.M. Mandiki, N. Wang, J. Douxfils, J. Dick, D. Tocher, P. Kestemont, n-3 and n-6 fatty acid bioconversion abilities in Eurasian perch (Perca fluviatilis) at two developmental stages, Aquac. Nutr. 17 (2011) e216-e225.
34. K.Wee, The biology and culture of snakeheads, in: J. Muir, R. Roberts (Eds.), Recent Advances in Aquaculture, Westview Press, Boulder, Co, 1982, pp. 180-211.
35. A. Zuraini, M.N. Somchit, M.H. Solihah, Y.M. Goh, A.K. Arifah, M.S. Zakaria, N. Somchit, M.A. Rajion, Z.A. Zakaria, A.M. Mat Jais, Fatty acid and amino acid composition of three local Malaysian Channa spp. fish, Food Chem. 97 (2006) 674-678.
36. A. Jaya-Ram, S.D. Ishak, Y.-L. Enyu, M.-K. Kuah, K.-L. Wong, A.C. Shu-Chien, Molecular cloning and ontogenic mRNA expression of fatty acid desaturase in the carnivorous striped snakehead fish (Channa striata ), Comp. Biochem. Physiol. A 158 (2011) 415-422.
37. S. Ling, M.-K. Kuah, T.S. Tengku Muhammad, S. Kolkovski, A.C. Shu-Chien, Effect of dietary HUFA on reproductive performance, tissue fatty acid profile and desaturase and elongase mRNAs in female swordtail Xiphophorus helleri, Aquaculture 261 (2006) 204-214.
38. N. Saitou, M. Nei, The neighbor-joining method: a new method for reconstructing phylogenetic trees, Mol. Biol. Evol. 4 (1987) 406-425.
39. K. Tamura, J. Dudley, M. Nei, S. Kumar, MEGA4: Molecular Evolutionary Genetic Analysis (MEGA) software version 4.0, Mol. Biol. Evol. 24 (2007) 1596-1599.
40. AOAC, Official methods of analysis of AOAC International, in: P. Cunniff (Ed.), AOAC International, Arlington VA, 1997.
41. Z. Lim, T. Senger, P. Vrinten, Four amino acid residues influence the substrate chain-length and regioselectivity of Siganus canaliculatus Δ4 and Δ5/6 desaturases, Lipids 49 (2014) 357-367.
42. S. Tanomman,M. Ketudat-Cairns, A. Jangprai, S. Boonanuntanasarn, Characterization of fatty acid delta-6 desaturase gene in Nile tilapia and heterogenous expression in Saccharomyces cerevisiae, Comp. Biochem. Physiol. B 166 (2013) 148-156.
43. L.F.C. Castro, Ó. Monroig, M.J. Leaver, J. Wilson, I. Cunha, D.R. Tocher, Functional desaturase Fads1 Δ5 and Fads2 Δ6 orthologues evolved before the origin of jawed vertebrates, PLoS ONE 7 (2012) e31950.
44. K. Hashimoto, A.C. Yoshizawa, S. Okuda, K. Kuma, S. Goto, M. Kanehisa, The repertoire of desaturases and elongases reveals fatty acid variations in 56 eukaryotic genomes, J. Lipid Res. 49 (2008) 183-191.
45. H. Sprecher, D.L. Luthria, B.S. Mohammed, S.P. Baykousheva, Reevaluation of the pathways for the biosynthesis of polyunsaturated fatty acids, J. Lipid Res. 36 (1995) 2471-2477.
46. C. Desvilettes, G. Bourdier, J.-C. Breton, Lipid class and fatty acid composition of planktivorous larval pike Esox lucius living in a natural pond, Aquat. Living Resour. 7 (1994) 67-77.
47. P.G. Lee, P.K.L. Ng, The snakehead fishes of the Indo-Malayan region, Nat. Malays. 16 (1991) 113-129.
48. J. Qin, A.W. Fast, Food selection and growth of young snakehead Channa striatus, J. Appl. Ichthyol. 13 (1997) 21-25.
49. G. Ahigren, L. Sonesten, M. Boberg, L.B. Gustafsson, Fatty acid content of some freshwater fish in lakes of different trophic levels - a bottom-up effect? Ecol. Freshw. Fish 5 (1996) 15-27.
50. D.C. Muller-Navarra, M.T. Brett, S. Park, S. Chandra, A.P. Ballantyne, E. Zorita, C.R. Goldman, Unsaturated fatty acid content in seston and tropho-dynamic coupling in lakes, Nature 427 (2004) 69-72.
51. G. Ahlgren, T. Vrede, W. Goedkoop, Fatty acid ratios in freshwater fish, zooplankton and zoobenthos-are there specific optima? in:M. Kainz, M.T. Brett,M.T. Arts (Eds.), Lipids in Aquatic Ecosystems, Springer, New York, 2009, pp. 211-236.
52. J.R. Sargent, D.R. Tocher, J.G. Bell, The lipids, in: J.E. Halver, R.W. Hardy (Eds.), Fish Nutrition, Academic Press, San Diego, 2002, pp. 181-257.
53. G. Mourente, Accumulation of DHA (docosahexaenoic acid; 22:6n-3) in larval and juvenile fish brain, in: H.I. Brownan, A.B. Skiftesvik (Eds.),The Big Fish Bang: Proceedings of the 26th Annual Larval Fish Conference, Institute of Marine Research, Postboks 1870, Nordnes, Bergen, Norway, 2003, pp. 239-248.
54. B.L. Scott, N.G. Bazan, Membrane docosahexaenoate is supplied to the developing brain and retina by the liver, Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 2903-2907.
55. H.-T. Ren, G.-Q. Zhang, J.-L. Li, Y.-K. Tang, H.-X. Li, J.-H. Yu, P. Xu, Two Δ6- desaturase-like genes in common carp ( Cyprinus carpio var. Jian): structure characterization, mRNA expression, temperature and nutritional regulation, Gene 525 (2013) 11-17.
56. G.M. Turchini, D.S. Francis, S.P.S.D. Senadheera, T. Thanuthong, S.S. De Silva, Fish oil replacement with different vegetable oils in Murray cod: evidence of an "omega-3 sparing effect" by other dietary fatty acids, Aquaculture 315 (2011) 250-259.
57. D.R. Tocher, G. Mourente, J.R. Sargent, Metabolism of [1-14C]docosahexaenoate (22 : 6n-3), [1-14C]eicosapentaenoate (20 : 5n-3) and [1-14C]linolenate (18 : 3n-3) in brain cells from juvenile turbot Scophthalmus maximus, Lipids 27 (1992) 494-499.
58. M.R. Miller, P.D. Nichols, C.G. Carter, Replacement of dietary fish oil for Atlantic salmon parr (Salmo salar L.) with a stearidonic acid containing oil has no effect on omega-3 long-chain polyunsaturated fatty acid concentrations, Comp. Biochem. Physiol. B 146 (2007) 197-206.
59. B.J. Cleveland, D.S. Francis, G.M. Turchini, Echium oil provides no benefit over linseed oil for (n-3) long-chain PUFA biosynthesis in rainbow trout, J. Nutr. 142 (2012) 1449-1455.