Patrón de expresión tisular de los genes elovl4 en Sparus aurata y Solea senegalensis: de larva a adulto
DOI:
https://doi.org/10.33936/at.v3i1.3476Keywords:
Very long-chain fatty acids, Marine fish, Special-distributionAbstract
Very long-chain (˃ C24) fatty acids (VLC-FA) play critical roles during early development of vertebrates, since these compounds are accumulated in the rapidly forming neural tissues, ensuring their normal function. The functionality of VLC-FA has aroused scientific interest, focusing on the study of elongases protein 4 of very long chain fatty acid (Elovl4), which are responsible for their biosynthesis from shorter fatty acids (precursors). For a better understanding of the metabolism and the potential tissue-specific requirements of VLC-FA in marine teleosts, the present study aimed to determine the tissue-expression pattern of the genes that encode for Elovl4 isoforms, i.e. elovl4a and elovl4b, in different windows of development (larval and adult stages) of Gilthead seabream Sparus aurata and Senegalese sole Solea senegalensis. The results indicated that in S. aurata larvae, elovl4a is widely expressed in the head, while elovl4b is strongly focused in the eyes. Interestingly, in S. senegalensis larvae an opposite tissue-expression pattern was observed for both elovl4 isoforms. In adults of both fish, although elovl4 transcripts were detected in most tissues analyzed, elovl4a and elovl4b genes were strongly expressed in brain and eyes, respectively. Importantly, the differential tissue-expression pattern of both elovl4 isoforms associated to the pre- and post-metamorphic stage of S. senegalensis could be indicative of the VLC-FA particular needs linked to neural tissues functionality in each development stage. These findings can contribute to a better understanding of the species-specific VLC-FA metabolism in marine teleosts.
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References
Agbaga, M.P., Mandal, M.N.A, Anderson, R.E. (2010). Retinal very long-chain PUFAs: new insights from studies on ELOVL4 protein. Journal of Lipid Research 51(7): 1624-1642.
Aldahmesh, M.A., Mohamed, J.Y., Alkuraya, H.S., Verma, I.C., Puri, R.D., Alaiya, A.A., Rizzo, W.B., Alkuraya, F.S. (2011). Recessive mutations in ELOVL4 cause ichthyosis, intellectual disability, and spastic quadriplegia. The American Journal of Human Genetics 89(6): 745-750.
Bazan, N.G. (2018). Docosanoids and elovanoids from omega-3 fatty acids are pro-homeostatic modulators of inflammatory responses, cell damage and neuroprotection. Molecular Aspects of Medicine 64: 18-33.
Betancor, M.B., Oboh, A., Ortega, A., Mourente, G., Navarro, J.C., de la Gandara, F., Tocher D.R., Monroig, O. (2020). Molecular and functional characterisation of a putative elovl4 gene and its expression in response to dietary fatty acid profile in Atlantic bluefin tuna (Thunnus thynnus). Comparative Biochemistry and Physiology Part B Biochemical and Molecular Biology 240, 110372.
Cameron, D.J., Tong, Z., Yang, Z., Kaminoh, J., Kamiyah, S., Chen, H., Zeng, J., Chen, Y., Luo, L., Zhang, K. (2007). Essential role of Elovl4 in very long chain fatty acid synthesis, skin permeability barrier function, and neonatal survival. International Journal of Biological Sciences 3(2): 111-119.
Carmona-Antoñanzas, G., Monroig, Ó., Dick, J.R., Davie, A., Tocher, D.R. (2011). Biosynthesis of very long-chain fatty acids (C>24) in Atlantic salmon: Cloning, functional characterisation, and tissue distribution of an Elovl4 elongase. Comparative Biochemistry and Physiology Part B Biochemical and Molecular Biology 159(2): 122-129.
Castro, L.F.C., Tocher, D.R., Monroig, Ó. (2016). Long-chain polyunsaturated fatty acid biosynthesis in chordates: insights into the evolution of Fads and Elovl gene repertoire. Progress in Lipid Research 62: 25-40.
Deák, F.; Anderson, R.E.; Fessler, J.L.; Sherry, D.M. (2019). Novel cellular functions of very long chain-fatty acids: Insight from ELOVL4 mutations. Frontiers in Cellular Neuroscience 13, 428.
Dyall, S.C. (2015). Long-chain omega-3 fatty acids and the brain: A review of the independent and shared effects of EPA, DPA and DHA. Frontiers in Aging Neuroscience 7: 1-15.
Hopiavuori, B.R., Deak, F., Wilkerson, J.L., Brush, R.S., Rocha-Hopiavuori, N.A., Hopiavuori, A.R., Ozan, K.G., Sullivan, M.T., Wren, J.D., Georgescu, C., Szweda, L., Awasthi, V., Towner, R., Sherry, D.M., Anderson, R.E., Agbaga, M.P. (2018). Homozygous expression of mutant ELOVL4 leads to seizures and death in a novel animal model of very long-chain fatty acid deficiency. Molecular Neurobiology 55 (2): 1795-1813.
Hopiavuori, B.R., Anderson, R.E., Agbaga, M.P. (2019). ELOVL4: very long chain fatty acids serve an eclectic role in mammalian health and function. Progress in Retinal and Eye Research 69: 137-158.
Jin, M., Monroig, Ó., Navarro, J.C., Tocher, D.R., Zhou, Q.C. (2017). Molecular and functional characterisation of two elovl4 elongases involved in the biosynthesis of very long-chain (>C24) polyunsaturated fatty acids in black seabream Acanthopagrus schlegelii. Comparative Biochemistry and Physiology Part B Biochemical and Molecular Biology 212: 41-50.
Monroig, Ó., Rotllant, J., Cerdá-Reverter, J.M., Dick, J.R., Figueras, A., Tocher, D.R. (2010). Expression and role of Elovl4 elongases in biosynthesis of very long-chain fatty acids during zebrafish Danio rerio early embryonic development. Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids 1801(10): 1145-1154.
Monroig, Ó., Webb, K., Ibarra-Castro, L., Holt, G.J., Tocher, D.R. (2011). Biosynthesis of long-chain polyunsaturated fatty acids in marine fish: Characterization of an Elovl4-like elongase from cobia Rachycentron canadum and activation of the pathway during early life stages. Aquaculture 312(1-4): 145-153.
Monroig, Ó., Tocher, D.R., Castro, L.F.C. (2018). Polyunsaturated Fatty Acid Biosynthesis and Metabolism in Fish, in: Burdge G. C. (Ed.), Polyunsaturated Fatty Acid Metabolism. Elsevier, Amsterdam, pp. 31-60.
Morais, S., Castanheira, F., Martinez-Rubio, L., Conceição, L.E.C., Tocher, D.R. (2012). 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 1821 (4): 660-671.
Morais, S., Torres, M., Hontoria, F., Monroig, Ó., Varó, I., Agulleiro, M. J., Navarro, J. C. (2020). Molecular and Functional Characterization of elovl4 Genes in Sparus aurata and Solea senegalensis Pointing to a Critical Role in Very Long-Chain (> C24) Fatty Acid Synthesis during Early Neural Development of Fish. International Journal of Molecular Science 21(10): 3514.
Mourente, G. (2003). Accumulation of DHA (docosahexaenoic acid; 22:6n-3) in larval and juvenile fish brain, in: Howard I. B. (Ed), The Big Fish Bang. Norwegian Institute of Marine Research, Bergen, pp. 239-248.
Oboh, A., Navarro, J.C., Tocher, D.R., Monroig, Ó. (2017). Elongation of very long-chain (>C24) fatty acids in Clarias gariepinus: cloning, functional characterization and tissue expression of elovl4 elongases. Lipids 52(10): 837-848.
Rotllant, J., Liu, D., Yan, Y.L., Postlethwait, J.H., Westerfield, M., Du, S.J. (2008). Sparc (Osteonectin) functions in morphogenesis of the pharyngeal skeleton and inner ear. Matrix Biology 27(6): 561-572.
Sarasquete, C., Gisbert, E., Ortiz-Delgado, J.B. (2019). Embryonic and larval ontogeny of the Senegalese sole, Solea senegalensis, in: Muñoz-Cueto, J.A., Mañanos, E., Sánchez, F.J. (Eds.), The Biology of Sole. CRC Press, Boca Ratón, 216-252 pp.
Seiliez, I., Panserat, S., Corraze, G., Kaushik, S., Bergot, P. (2003). Cloning and nutritional regulation of a Δ6-desaturase-like enzyme in the marine teleost gilthead seabream (Sparus aurata). Comparative Biochemistry and Physiology Part B Biochemical and Molecular Biology 135 (3): 449-460.
Thisse, C., Thisse, B. (2008). High-resolution in situ hybridization to whole-mount zebrafish embryos. Nature Protocols 3: 59-69.
Torres, M.; Navarro, J.C.; Varó, I.; Agulleiro, M.J.; Morais, S.; Monroig, Ó.; Hontoria, F. (2020a). Expression of genes related to long-chain (C18-22) and very long-chain (>C24) fatty acid biosynthesis in gilthead seabream (Sparus aurata) and Senegalese sole (Solea senegalensis) larvae: Investigating early ontogeny and nutritional regulation. Aquaculture 520: 734949.
Torres, M.; Navarro, J.C.; Varó, I.; Monroig, Ó.; Hontoria, F. (2020b). Nutritional regulation of genes responsible for long-chain (C20-24) and very long-chain (>C24) polyunsaturated fatty acid biosynthesis in post-larvae of gilthead seabream (Sparus aurata) and Senegalese sole (Solea senegalensis). Aquaculture 525: 735314.
Xie, D., Chen, F., Lin, S., You, C., Wang, S., Zhang, Q., Monroig, Ó., Tocher, D.R., Li, Y. (2016). Long-chain polyunsaturated fatty acid biosynthesis in the euryhaline herbivorous teleost Scatophagus argus: Functional characterization, tissue expression and nutritional regulation of two fatty acyl elongases. Comparative Biochemistry and Physiology Part B Biochemical and Molecular Biology 198: 37-45.
Yan, J., Liang, X., Cui, Y., Cao, X., Gao, J. (2018). Elovl4 can effectively elongate C18 polyunsaturated fatty acids in loach Misgurnus anguillicaudatus. Biochemical and Biophysical Research Communications 495(4): 2637-2642.
Zheng, X., Seiliez, I., Hastings, N., Tocher, D.R., Panserat, S., Dickson, C.A., Bergot, P., Teale, A.J. (2004). Characterization and comparison of fatty acyl Δ6 desaturase cDNAs from freshwater and marine teleost fish species. Comparative Biochemistry and Physiology Part B Biochemical and Molecular Biology 139 (2): 269-279.
Aldahmesh, M.A., Mohamed, J.Y., Alkuraya, H.S., Verma, I.C., Puri, R.D., Alaiya, A.A., Rizzo, W.B., Alkuraya, F.S. (2011). Recessive mutations in ELOVL4 cause ichthyosis, intellectual disability, and spastic quadriplegia. The American Journal of Human Genetics 89(6): 745-750.
Bazan, N.G. (2018). Docosanoids and elovanoids from omega-3 fatty acids are pro-homeostatic modulators of inflammatory responses, cell damage and neuroprotection. Molecular Aspects of Medicine 64: 18-33.
Betancor, M.B., Oboh, A., Ortega, A., Mourente, G., Navarro, J.C., de la Gandara, F., Tocher D.R., Monroig, O. (2020). Molecular and functional characterisation of a putative elovl4 gene and its expression in response to dietary fatty acid profile in Atlantic bluefin tuna (Thunnus thynnus). Comparative Biochemistry and Physiology Part B Biochemical and Molecular Biology 240, 110372.
Cameron, D.J., Tong, Z., Yang, Z., Kaminoh, J., Kamiyah, S., Chen, H., Zeng, J., Chen, Y., Luo, L., Zhang, K. (2007). Essential role of Elovl4 in very long chain fatty acid synthesis, skin permeability barrier function, and neonatal survival. International Journal of Biological Sciences 3(2): 111-119.
Carmona-Antoñanzas, G., Monroig, Ó., Dick, J.R., Davie, A., Tocher, D.R. (2011). Biosynthesis of very long-chain fatty acids (C>24) in Atlantic salmon: Cloning, functional characterisation, and tissue distribution of an Elovl4 elongase. Comparative Biochemistry and Physiology Part B Biochemical and Molecular Biology 159(2): 122-129.
Castro, L.F.C., Tocher, D.R., Monroig, Ó. (2016). Long-chain polyunsaturated fatty acid biosynthesis in chordates: insights into the evolution of Fads and Elovl gene repertoire. Progress in Lipid Research 62: 25-40.
Deák, F.; Anderson, R.E.; Fessler, J.L.; Sherry, D.M. (2019). Novel cellular functions of very long chain-fatty acids: Insight from ELOVL4 mutations. Frontiers in Cellular Neuroscience 13, 428.
Dyall, S.C. (2015). Long-chain omega-3 fatty acids and the brain: A review of the independent and shared effects of EPA, DPA and DHA. Frontiers in Aging Neuroscience 7: 1-15.
Hopiavuori, B.R., Deak, F., Wilkerson, J.L., Brush, R.S., Rocha-Hopiavuori, N.A., Hopiavuori, A.R., Ozan, K.G., Sullivan, M.T., Wren, J.D., Georgescu, C., Szweda, L., Awasthi, V., Towner, R., Sherry, D.M., Anderson, R.E., Agbaga, M.P. (2018). Homozygous expression of mutant ELOVL4 leads to seizures and death in a novel animal model of very long-chain fatty acid deficiency. Molecular Neurobiology 55 (2): 1795-1813.
Hopiavuori, B.R., Anderson, R.E., Agbaga, M.P. (2019). ELOVL4: very long chain fatty acids serve an eclectic role in mammalian health and function. Progress in Retinal and Eye Research 69: 137-158.
Jin, M., Monroig, Ó., Navarro, J.C., Tocher, D.R., Zhou, Q.C. (2017). Molecular and functional characterisation of two elovl4 elongases involved in the biosynthesis of very long-chain (>C24) polyunsaturated fatty acids in black seabream Acanthopagrus schlegelii. Comparative Biochemistry and Physiology Part B Biochemical and Molecular Biology 212: 41-50.
Monroig, Ó., Rotllant, J., Cerdá-Reverter, J.M., Dick, J.R., Figueras, A., Tocher, D.R. (2010). Expression and role of Elovl4 elongases in biosynthesis of very long-chain fatty acids during zebrafish Danio rerio early embryonic development. Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids 1801(10): 1145-1154.
Monroig, Ó., Webb, K., Ibarra-Castro, L., Holt, G.J., Tocher, D.R. (2011). Biosynthesis of long-chain polyunsaturated fatty acids in marine fish: Characterization of an Elovl4-like elongase from cobia Rachycentron canadum and activation of the pathway during early life stages. Aquaculture 312(1-4): 145-153.
Monroig, Ó., Tocher, D.R., Castro, L.F.C. (2018). Polyunsaturated Fatty Acid Biosynthesis and Metabolism in Fish, in: Burdge G. C. (Ed.), Polyunsaturated Fatty Acid Metabolism. Elsevier, Amsterdam, pp. 31-60.
Morais, S., Castanheira, F., Martinez-Rubio, L., Conceição, L.E.C., Tocher, D.R. (2012). 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 1821 (4): 660-671.
Morais, S., Torres, M., Hontoria, F., Monroig, Ó., Varó, I., Agulleiro, M. J., Navarro, J. C. (2020). Molecular and Functional Characterization of elovl4 Genes in Sparus aurata and Solea senegalensis Pointing to a Critical Role in Very Long-Chain (> C24) Fatty Acid Synthesis during Early Neural Development of Fish. International Journal of Molecular Science 21(10): 3514.
Mourente, G. (2003). Accumulation of DHA (docosahexaenoic acid; 22:6n-3) in larval and juvenile fish brain, in: Howard I. B. (Ed), The Big Fish Bang. Norwegian Institute of Marine Research, Bergen, pp. 239-248.
Oboh, A., Navarro, J.C., Tocher, D.R., Monroig, Ó. (2017). Elongation of very long-chain (>C24) fatty acids in Clarias gariepinus: cloning, functional characterization and tissue expression of elovl4 elongases. Lipids 52(10): 837-848.
Rotllant, J., Liu, D., Yan, Y.L., Postlethwait, J.H., Westerfield, M., Du, S.J. (2008). Sparc (Osteonectin) functions in morphogenesis of the pharyngeal skeleton and inner ear. Matrix Biology 27(6): 561-572.
Sarasquete, C., Gisbert, E., Ortiz-Delgado, J.B. (2019). Embryonic and larval ontogeny of the Senegalese sole, Solea senegalensis, in: Muñoz-Cueto, J.A., Mañanos, E., Sánchez, F.J. (Eds.), The Biology of Sole. CRC Press, Boca Ratón, 216-252 pp.
Seiliez, I., Panserat, S., Corraze, G., Kaushik, S., Bergot, P. (2003). Cloning and nutritional regulation of a Δ6-desaturase-like enzyme in the marine teleost gilthead seabream (Sparus aurata). Comparative Biochemistry and Physiology Part B Biochemical and Molecular Biology 135 (3): 449-460.
Thisse, C., Thisse, B. (2008). High-resolution in situ hybridization to whole-mount zebrafish embryos. Nature Protocols 3: 59-69.
Torres, M.; Navarro, J.C.; Varó, I.; Agulleiro, M.J.; Morais, S.; Monroig, Ó.; Hontoria, F. (2020a). Expression of genes related to long-chain (C18-22) and very long-chain (>C24) fatty acid biosynthesis in gilthead seabream (Sparus aurata) and Senegalese sole (Solea senegalensis) larvae: Investigating early ontogeny and nutritional regulation. Aquaculture 520: 734949.
Torres, M.; Navarro, J.C.; Varó, I.; Monroig, Ó.; Hontoria, F. (2020b). Nutritional regulation of genes responsible for long-chain (C20-24) and very long-chain (>C24) polyunsaturated fatty acid biosynthesis in post-larvae of gilthead seabream (Sparus aurata) and Senegalese sole (Solea senegalensis). Aquaculture 525: 735314.
Xie, D., Chen, F., Lin, S., You, C., Wang, S., Zhang, Q., Monroig, Ó., Tocher, D.R., Li, Y. (2016). Long-chain polyunsaturated fatty acid biosynthesis in the euryhaline herbivorous teleost Scatophagus argus: Functional characterization, tissue expression and nutritional regulation of two fatty acyl elongases. Comparative Biochemistry and Physiology Part B Biochemical and Molecular Biology 198: 37-45.
Yan, J., Liang, X., Cui, Y., Cao, X., Gao, J. (2018). Elovl4 can effectively elongate C18 polyunsaturated fatty acids in loach Misgurnus anguillicaudatus. Biochemical and Biophysical Research Communications 495(4): 2637-2642.
Zheng, X., Seiliez, I., Hastings, N., Tocher, D.R., Panserat, S., Dickson, C.A., Bergot, P., Teale, A.J. (2004). Characterization and comparison of fatty acyl Δ6 desaturase cDNAs from freshwater and marine teleost fish species. Comparative Biochemistry and Physiology Part B Biochemical and Molecular Biology 139 (2): 269-279.
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2021-04-30
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