Non-coding RNAs: Uncovering their Potential Relevance in Fish Nutrition
Keywords:
ncRNAs, miRNAs, nutrigenomics, transcriptomics, NGSAbstract
The optimization of industrial production would only be possible with the discovery, identification and
characterization of biological processes in which a nutrient or any other factor acts, as well as when their
genes and genetic networks revealed. With the advent of Next Generation-Sequencing technologies, the
discovery of non-coding RNAs having a key role on the control of a diverse set of biological functions in
multicellular organism will allow a deeper knowledge on genes and genetic networks control such processes
in farmed fish species. Here, the basics of non-coding RNAs regarding their features, biogenesis and mode of
action will be briefly reviewed, while the research works specifically conducted until now on the
identification of non-coding RNAs in different farmed fish species, developmental stages and tissues using
high throughput technologies will be described and compared. Several non-coding RNAs have been
associated with early developmental events, immune response to pathogen infections, sexual differentiation
and maturation, and nutrition. While the research on miRNAs is the most abundant, new efforts on the
characterization of long non-coding RNAs and PIWI-interacting RNAs profiles provided new insights on how
these non-coding RNAs are also involved in fish nutrition. Finally, the future perspectives and considerations
on the potential use of non-coding RNAs (mainly those found in circulation) in relevant cultured fish species
as new reliable biomarkers of physiological condition will be pointed out.
Downloads
References
Agarwal, S. et al., 2017. In silico mining of conserved miRNAs of Indian catfish Clarias batrachus
(Linnaeus, 1758 ) from the contigs, ESTs, and BAC end sequences. Applied Biochemistry and
Biotechnology, 182, pp.956–966.
Allegra, A. et al., 2012. Circulating microRNAs: New biomarkers in diagnosis, prognosis and treatment
of cancer (Review). International Journal of Oncology, 41, pp.1897–1912.
Andreassen, R., Worren, M.M. & Høyheim, B., 2013. Discovery and characterization of miRNA genes in
Atlantic salmon (Salmo salar) by use of a deep sequencing approach. BMC Genomics, 14, p.482.
Barozai, K., 2012. The microRNAs and their targets in the channel catfish (Ictalurus punctatus).
Molecular Biology Reports, 39, pp.8867–8872.
Basu, S., Müller, F. & Sanges, R., 2013. Examples of sequence conservation analyses capture a subset of
mouse long non-coding RNAs sharing homology with fish conserved genomic elements. BMC
Genomics, 14(Suppl 7), p.S14.
Bekaert, M. et al., 2013. Sequencing and characterisation of an extensive Atlantic ssalmon (Salmo salar
L.) microRNA repertoire. PLoS ONE, 8(7), p.e70136.
Berthelot, C. et al., 2014. The rainbow trout genome provides novel insights into evolution after wholegenome
duplication in vertebrates. Nature, 5, pp.1–10.
Bizuayehu, T.T. et al., 2013. Characterization of novel precursor miRNAs using next generation
sequencing and prediction of miRNA targets in Atlantic halibut. PLoS ONE, 8(4), p.e61378.
Bizuayehu, T.T. et al., 2012. Differential expression patterns of conserved miRNAs and isomiRs during
Atlantic halibut development. BMC Genomics, 13, p.11.
Bizuayehu, T.T. et al., 2016. First feed affects the expressions of microRNA and their targets in Atlantic
cod. British Journal of Nutrition, 115, pp.1145–1154.
Bizuayehu, T.T. et al., 2015. Temperature during early development has long-term effects on microRNA
expression in Atlantic cod. BMC Genomics, 16, p.305.
Bizuayehu, T.T. & Babiak, I., 2014. MicroRNA in teleost fish. Genome Biology and Evolution, 6(8),
pp.1911–1937.
Boltaña, S. et al., 2016. Long noncoding RNAs (lncRNAs) dynamics evidence immunomodulation during
ISAV- Infected Atlantic salmon (Salmo salar). Scientific Reports, 6, p.22698.
Campos, C. et al., 2014. Thermal plasticity of the miRNA transcriptome during Senegalese sole
development. BMC Genomics, 15, p.525.
Castel, S.E. & Martienssen, R.A., 2013. RNA interference in the nucleus: roles for small RNAs in
Fernández-Monzón, I. et al., 2017. Non-coding RNAs: uncovering their potential relevance in fish nutrition. En: Cruz-Suárez, L.E., Ricque-Marie, D., Tapia-Salazar, M., Nieto-
López, M.G., Villarreal-Cavazos, D. A., Gamboa-Delgado, J., López Acuña, L.M. y Galaviz-Espinoza, M. . (Eds), Investigación y Desarrollo en Nutrición Acuícola
Universidad Autónoma de Nuevo León, San Nicolás de los Garza, Nuevo León, México, pp. 363-389. ISBN 978-607-27-0822-8.
transcription, epigenetics and beyond. Nature Reviews, 14, pp.100–112.
Chi, W. et al., 2011. Characterization and comparative profiling of miRNA transcriptomes in bighead
carp and silver carp. PLoS ONE, 6(8), p.e23549.
Chiba, H. et al., 2008. Weak correlation between sequence conservation in promoter regions and in
protein-coding regions of human-mouse orthologous gene pairs. BMC genomics, 15, pp.1–15.
Craig, P.M., Trudeau, V.L. & Moon, T.W., 2014. Profiling hepatic microRNAs in zebrafish: Fluoxetine
exposure mimics a fasting response that targets AMP-Activated protein kinase (AMPK). PLoS
ONE, 9(4), p.e95351.
Crick, F., 1970. Central dogma of molecular biology. Nature, 227, pp.561–563.
Cui, J. et al., 2017. Nutrition, microRNAs, and human health. Advance in Nutrition, 8, pp.105–112.
Ebbesen, K.K., Kjems, J. & Hansen, T.B., 2016. Circular RNAs: Identification, biogenesis and function.
Biochimica et Biophysica Acta, 1859, pp.163–168.
The ENCODE Project Consortium, 2004. The ENCODE (Encyclopedia of DNA Elements) Project.
Science, 306, pp.636–640.
FAO, 2016. State of world fisheries and aquaculture 2016. Food and Agriculture Organization of the
United Nations, Rome.
Fatica, A. & Bozzoni, I., 2014. Long non-coding RNAs: new players in cell differentiation and
development. Nature Reviews, 15, pp.7–21.
Feng, J., Bi, C., Clark, B.S., Mady, R., Shah, P., Kohtz, J.D., 2006. The Evf-2 noncoding RNA is
transcribed from the Dlx-5/6 ultraconserved region and functions as a Dlx-2 transcriptional
coactivator. Genes and Development, 20, pp.1470–1484.
Figueras, A. et al., 2016. Whole genome sequencing of turbot (Scophthalmus maximus ;
Pleuronectiformes): a fish adapted to demersal life. DNA research, 23(3), pp.181–192.
Fritz, J.V., Heintz-Buschart, A., Ghosal, A., Wampach, L., Etheridge, A., Galas, D., Wilmes, P., 2016.
Sources and functions of extracellular small RNAs in human circulation. Annual Reviews in
Nutrition, 36, pp.301–336.
Fu, Y. et al., 2011. Identification and differential expression of microRNAs during metamorphosis of the
Japanese flounder (Paralichthys olivaceus). PLoS ONE, 6(7), p.e22957.
Ghildiyal, M. & Zamore, P.D., 2009. Small silencing RNAs: an expanding universe. Nature Reviews
Genetics, 10, pp.94–108.
Gomes, F. et al., 2017. Identification and characterizatio of the expression profile of the microRNAs in
the Amazon species Colossoma macropomum by next generation sequencing. Genomics, 109(2),
pp.67–74.
Ha, M. & Kim, V.N., 2014. Regulation of microRNA biogenesis. Nature Reviews, 15, pp.509–524.
Henry, V.J. et al., 2014. OMICtools: an informative directory for multi-omic data analysis. Database : the
journal of biological databases and curation, 2014(13), pp.1–5.
Huang, Y. et al., 2016. Genome-wide identification and characterization of microRNA genes and their
targets in large yellow croaker (Larimichthys crocea). Gene, 576(1), pp.261–267.
Iwasaki, Y.W., Siomi, M.C. & Siomi, H., 2015. PIWI-Interacting RNA: Its biogenesis and functions.
Annual Reviews in Biochemistry, 84, pp.405–433.
Fernández-Monzón, I. et al., 2017. Non-coding RNAs: uncovering their potential relevance in fish nutrition. En: Cruz-Suárez, L.E., Ricque-Marie, D., Tapia-Salazar, M., Nieto-
López, M.G., Villarreal-Cavazos, D. A., Gamboa-Delgado, J., López Acuña, L.M. y Galaviz-Espinoza, M. . (Eds), Investigación y Desarrollo en Nutrición Acuícola
Universidad Autónoma de Nuevo León, San Nicolás de los Garza, Nuevo León, México, pp. 363-389. ISBN 978-607-27-0822-8.
John, B., Enright, A.J., Aravin, A., Tuschl, T., Sander, C., Marks, D.S., 2004. Human microRNA targets.
PLoS Biology, 2, 11, p.e363.
Johnsson, P. et al., 2014. Evolutionary conservation of long non-coding RNAs; sequence, structure,
function. Biochimica et Biophysica Acta, 1840(3), pp.1063–1071.
Kaikkonen, M.U., Lam, M.T.Y. & Glass, C.K., 2011. Non-coding RNAs as regulators of gene expression
and epigenetics. Cardiovascular Research, 90, pp.430–440.
Kaitetzidou, E. et al., 2015. Dynamics of gene expression patterns during early development of the
European seabass (Dicentrarchus labrax). Physiological Genomics, 47, pp.158–169.
Kim, N.V., Han, J. & Siomi M.C., 2009. Biogenesis of small RNAs in animals. Nature Reviews in.
Molecular and Cell Biology, 10, pp.126–139.
Kozomara, A. & Griffiths-Jones, S., 2014. miRBase: annotating high confidence microRNAs using deep
sequencing data. Nucleic Acids Research, 42, pp.68–73.
Lam, M.T.Y. et al., 2014. Enhancer RNAs and regulated transcriptional programs. Trends in Biochemical
Sciences, 39(4), pp.170–182.
Li, E., & Li, C., 2014. Use of RNA-seq in Aquaculture Research. Poultry, Fisheries and Wildlife
Sciences, 2, p.e108.
Liang, L. et al., 2015. Long noncoding RNA expression profiles in gut tissues constitute molecular
signatures that reflect the types of microbes. Scientific Reports, 5, p.11763.
Lien, S. et al., 2016. The Atlantic salmon genome provides insights into rediploidization. Nature,
(7602), pp.200–205.
Loche, E. & Ozanne, S.E., 2016. Early nutrition, epigenetics, and cardiovascular disease. Current
Opinion in Lipidology, 27, pp.449–458.
Lozada-Chávez, I., Stadler, P.F. & Prohaska, S.J., 2011. Hypothesis for the modern RNA world: a
pervasive non-coding RNA-based genetic regulation is a prerequisite for the emergence of
multicellular complexity. Origins of Life and Evolution of Biospheres, 41, pp.587–607.
Ma, H. et al., 2012. Characterization of the rainbow trout egg microRNA transcriptome. PLoS ONE, 7(6),
p.e39649.
Malone, C.D. & Hannon, G.J., 2009. Small RNAs as guardians of the genome. Cell, 136, pp.656–668.
Martianov, I., et al., 2007. Repression of the human dihydrofolate reductase gene by a non-coding
interfering transcript. Nature, 445, pp.666–670.
McDonald, J.S., et al., 2011. Analysis of circulating microRNA: preanalytical and analytical challenges.
Clinical Chemistry, 57, 833–840.
Mennigen, J.A., et al., 2012. Postprandial regulation of hepatic microRNAs predicted to target the insulin
pathway in rainbow trout. PLoS ONE, 7, p.e38604.
Mennigen, J.A., Martyniuk, C.J., Seiliez, I., Panserat, S., Skiba-Cassy, S., 2014a. Metabolic consequences
of microRNA-122 inhibition in rainbow trout, Oncorhynchus mykiss. BMC Genomics, 15, p.70.
Mennigen, J.A., 2015. Micromanaging metabolism — a role for miRNAs in teleost energy metabolism.
Comparative Biochemistry and Physiology, Part B, 199, pp.115–125.
Nolan, T., Huggett, J. & Sanchez, E., 2013. Good practice guide for the application of quantitative PCR
(qPCR). LGC.
Fernández-Monzón, I. et al., 2017. Non-coding RNAs: uncovering their potential relevance in fish nutrition. En: Cruz-Suárez, L.E., Ricque-Marie, D., Tapia-Salazar, M., Nieto-
López, M.G., Villarreal-Cavazos, D. A., Gamboa-Delgado, J., López Acuña, L.M. y Galaviz-Espinoza, M. . (Eds), Investigación y Desarrollo en Nutrición Acuícola
Universidad Autónoma de Nuevo León, San Nicolás de los Garza, Nuevo León, México, pp. 363-389. ISBN 978-607-27-0822-8.
Núñez-Acuña, G. et al., 2017. Functional Diets Modulate lncRNA-Coding RNAs and Gene Interactions
in the Intestine of Rainbow Trout Oncorhynchus mykiss. Marine Biotechnology, 19, pp.287–
Orom, U.A., et al., 2010. Long noncoding RNAs with enhancer-like function in human cells. Cell, 143,
pp.46–58.
Paneru, B. et al., 2016. Differential expression of long non-coding RNAs in three genetic lines of rainbow
trout in response to infection with Flavobacterium psychrophilum. Scientific Reports, 6, p.36032.
Panzica-Kelly, J.M., Zhang, C.X. & Augustine-Rauch, K.A., 2015. Optimization and Performance
Assessment of the Chorion-Off [Dechorinated] Zebrafish Developmental Toxicity Assay.
Toxicological Sciences, 146(1), pp.127–34.
Papić, L., García, K. & Romero, J., 2015. Avances y limitaciones en el uso de los dsRNA como
estrategias de control y prevención de enfermedades virales en sistemas acuícolas diseases in
aquaculture. Latin American Journal of Aquatic Research, 43(3), pp.388–401.
Pauli, A. et al., 2012. Systematic identification of long noncoding RNAs expressed during zebrafish
embryogenesis. Genome Research, 22, pp.577–591.
Qiang, J. et al., 2017. Effects of exposure to Streptococcus iniae on microRNA expression in the head
kidney of genetically improved farmed tilapia (Oreochromis niloticus). BMC Genomics, 18,
p.190.
Quek, X.C. et al., 2015. lncRNAdb v2.0 : expanding the reference database for functional long noncoding
RNAs. Nucleic Acids Research, 43, pp.168–173.
Riffo-Campos, Á.L., Riquelme, I. & Brebi-Mieville, P., 2016. Tools for sequence-based miRNA target
prediction: What to choose? International Journal of Molecular Sciences, 17, p.1987.
Rosani, U., Pallavicini, A. & Venier, P., 2016. The miRNA biogenesis in marine bivalves. PeerJ, 4,
p.e1763.
Salem, M. et al., 2010. A microRNA repertoire for functional genome research in rainbow trout
(Oncorhynchus mykiss). Marine Biotechnology, 12, pp.410–429.
Sand, M. et al., 2012. The miRNA machinery in primary cutaneous malignant melanoma, cutaneous
malignant melanoma metastases and benign melanocytic nevi. Cell and Tissue Research, 350(1),
pp.119–126.
Sarkar, A., Volff, J. & Vaury, C., 2016. piRNAs and their diverse roles: a transposable element-driven
tactic for gene regulation? The FASEB Journal, 31, pp.1–12.
Shen, Y., Guo, X. & Wang, W., 2016. Identification and characterization of circular RNAs in zebrafish.
FEBS Letters, 591(1), pp.213–220.
Shinya, M. et al., 2013. Properties of gene knockdown system by vector-based siRNA in zebrafish.
Development, Growth and Differentiation, 55, pp.755–765.
Silva, M. & Melo, S.A., 2015. Non-coding RNAs in exosomes: new players in cancer biology. Current
Genomics, 5, pp.295–303.
Siomi, M.C. et al., 2011. PIWI-interacting small RNAs: the vanguard of genome defence. Nature Reviews
in Molecular and Cell Biology, 12, pp.246–258.
Smith, E. & Shilatifard, A., 2014. Enhancer biology and enhanceropathies. Nature Structural and
Fernández-Monzón, I. et al., 2017. Non-coding RNAs: uncovering their potential relevance in fish nutrition. En: Cruz-Suárez, L.E., Ricque-Marie, D., Tapia-Salazar, M., Nieto-
López, M.G., Villarreal-Cavazos, D. A., Gamboa-Delgado, J., López Acuña, L.M. y Galaviz-Espinoza, M. . (Eds), Investigación y Desarrollo en Nutrición Acuícola
Universidad Autónoma de Nuevo León, San Nicolás de los Garza, Nuevo León, México, pp. 363-389. ISBN 978-607-27-0822-8.
Molecular Biology, 21(3), pp.210–219.
Sokolova, O.A., et al., The interplay of transposon silencing genes in the Drosophila melanogaster
germline. Molekuliarnaia Biologiia, 45(4), pp.633–641.
Sun, Z., Hao, T. & Tian, J., 2017. Identification of exosomes and its signature miRNAs of male and
female Cynoglossus semilaevis. Scientific Reports, 7, p.860.
Tam, S., Tsao, M. & Mcpherson, J.D., 2015. Optimization of miRNA-seq data preprocessing. Briefings in
Bioinformatics, pp.1–14.
Taminato, T. et al., 2016. Enhancer activity-based identification of functional enhancers using zebrafish
embryos. Genomics, 108, pp.102–107.
Trinh, L.A. et al., 2017. Biotagging of specific cell populations in zebrafish reveals gene regulatory logic
encoded in the nuclear transcriptome. Cell Reports, 19, pp.425–440.
Ulitsky, I., et al., 2011. Conserved function of lincRNAs in vertebrate embryonic development despite
rapid sequence evolution. Cell, 147, pp.1537–1550.
Valenzuela-Miranda, D. & Gallardo-Escárate, C., 2016. Novel insights into the response of Atlantic
salmon (Salmo salar) to Piscirickettsia salmonis: Interplay of coding genes and lncRNAs during
bacterial infection. Fish and Shellfish Immunology, 59, pp.427–438.
van der Vlag, J. & Otte, A.P., 1999. Transcriptional repression mediated by the human polycomb-group
protein EED involves histone deacetylation. Nature Genetics, 23, pp.474–478.
Viereck, J. & Thum, T., 2017. Circulating noncoding RNAs as biomarkers of cardiovascular disease and
injury. Circulation Research, 120, pp.381–399.
Viereck, J., Bang, C., Foinquinos, A. & Thum, T., 2014. Regulatory RNAs and paracrine networks in the
heart. Cardiovascular Research, 102, pp.290–301.
Viré, E., et al., 2006. The Polycomb group protein EZH2 directly controls DNA methylation. Nature,
, pp.871–874.
Wang, X. et al., 2015. MicroRNA-sequence profiling reveals novel osmoregulatory microRNA
expression patterns in catadromous eel Anguilla marmorata. PLoS ONE, 10(8), p.e0136383.
Wang, F. et al., 2017. Identification and profiling of Cyprinus carpio microRNAs during ovary
differentiation by deep sequencing. BMC Genomics, 18, p.333.
Watanabe, T. & Lin, H., 2014. Posttranscriptional regulation of gene expression by Piwi proteins and
piRNAs. Molecular Cell, 56, pp.18–27.
Wilczynska, A. & Bushell, M., 2014. The complexity of miRNA-mediated repression. Cell Death and
Differentiation, 22(1), pp.22–33.
Wittrup, A. & Lieberman, J., 2015. Knocking down disease: a progress report on siRNA therapeutics.
Nature Reviews Genetics, 16, pp.543–552.
Wongwarangkana, C. et al., 2015. Deep sequencing, profiling and detailed annotation of microRNAs in
Takifugu rubripes. BMC Genomics, 16, p.457.
Wu, S. et al., 2015. MicroRNA profile analysis of Epithelioma papulosum cyprini cell line before and
after SVCV infection. Developmental and Comparative Immunology, 48, pp.124–128.
Xia, J.H. et al., 2011. Identification and characterization of 63 microRNAs in the Asian seabass Lates
calcarifer. PLoS ONE, 6(3), p.e17537.
Fernández-Monzón, I. et al., 2017. Non-coding RNAs: uncovering their potential relevance in fish nutrition. En: Cruz-Suárez, L.E., Ricque-Marie, D., Tapia-Salazar, M., Nieto-
López, M.G., Villarreal-Cavazos, D. A., Gamboa-Delgado, J., López Acuña, L.M. y Galaviz-Espinoza, M. . (Eds), Investigación y Desarrollo en Nutrición Acuícola
Universidad Autónoma de Nuevo León, San Nicolás de los Garza, Nuevo León, México, pp. 363-389. ISBN 978-607-27-0822-8.
Xu, S. et al., 2017. Transcriptome-wide identification and functional investigation of circular RNA in the
teleost large yellow croaker (Larimichthys crocea). Marine Genomics, 32, pp.71–78.
Xu, Z. et al., 2013. Identification and characterization of microRNAs in channel catfish (Ictalurus
punctatus) by using Solexa sequencing technology. PLoS ONE, 8(1), p.e54174.
Yan, B. et al., 2013. MicroRNA regulation of skin pigmentation in fish. Journal of Cell Science, 126,
pp.3401–3408.
Yan, X. et al., 2012. Identification and profiling of microRNAs from skeletal muscle of the common carp.
PLoS ONE, 7(1), p.e30925.
Yartseva, V. et al., 2016. RESA identifies mRNA-regulatory sequences at high resolution. Nature
Methods, 14, pp.201–207.
Yi, M. et al., 2014. GBE rapid evolution of piRNA pathway in the Teleost fish: Implication for an
adaptation to transposon diversity. Genome and Biology Evolution, 6(6), pp.1393–1407.
Zhang, D. et al., 2014a. The effect of exposure to a High-fat diet on microRNA expression in the Liver of
blunt snout bream (Megalobrama amblycephala). PLoS ONE, 9(5), p.e96132.
Zhang, Q. et al., 2014b. miR-17 is involved in the regulation of LC-PUFA biosynthesis in vertebrates:
effects on liver expression of a fatty acyl desaturase in the marine teleost Siganus canaliculatus.
Biochimica et Biophysica Acta, 1841, pp.934–943.
Zhang, P. et al., 2014c. piRBase: a web resource assisting piRNA functional study. Database, pp.1–7.
Zhou, Y. et al., 2016. Identification and comparative analysis of piRNAs in ovary and testis of Nile tilapia
(Oreochromis niloticus). Genes and Genomes, 38, pp.519–527.
Zhu, Y. et al., 2012. Identification of common carp (Cyprinus carpio) microRNAs and microRNA-related
SNPs. BMC Genomics, 13, p.413.