1. bookAHEAD OF PRINT
Dettagli della rivista
License
Formato
Rivista
eISSN
2300-8733
Prima pubblicazione
25 Nov 2011
Frequenza di pubblicazione
4 volte all'anno
Lingue
Inglese
access type Accesso libero

New long-non coding RNAs related to fat deposition based on pig model

Pubblicato online: 16 May 2022
Volume & Edizione: AHEAD OF PRINT
Pagine: -
Ricevuto: 17 Dec 2021
Accettato: 08 Mar 2022
Dettagli della rivista
License
Formato
Rivista
eISSN
2300-8733
Prima pubblicazione
25 Nov 2011
Frequenza di pubblicazione
4 volte all'anno
Lingue
Inglese
Abstract

Obesity is a problem in the last decades since the development of certain technologies has forced submission to a faster pace of life, resulting in nutritional changes. Domestic pigs are an excellent animal model in recognition of adiposity-related processes, corresponding to the size of individual organs, the distribution of body fat in the organism, and similar metabolism. The present study applied next-generation sequencing to identify adipose tissue (AT) transcriptomic signals related to increased fat content by identifying differentially expressed genes (DEGs), including long-non coding RNAs in Złotnicka White pigs (n=16). Moreover, besides commonly used functional analysis, we applied the Freiburg RNA tool to predict DE lncRNA targets based on calculation hybridisation energy. And in addition, DE lncRNAs were recognized based on information available in databases. The obtained results show that closely 230 gene expression was found to be dependent on fat content, included 8 lncRNAs. The most interesting was that among identified DE lncRNAs was transcript corresponding to human MALAT1, which was previously considered in the obesity-related context. Moreover, it was identified that in ENSSSCG00000048394, ENSSSCG00000047210, ENSSSCG00000047442 and ENSSSCG00000041577 lncRNAs are contained repeat insertion domains of LncRNAs (RIDLs) considered as important gene expression regulatory elements, and ENSSSCG00000041577 seems to be the host for mir1247(NR_031649.1). The analysis of energy hybridisation between DE lncRNAs and DEGs using the Freiburg IntaRNAv2 tool, including isoforms expressed in AT, showed that ENSSSCG00000047210 lncRNA interacted with the highest number of DEGs and ENSSSCG00000047210 expression was only correlated with positive fat-related DEGs. The functional analysis showed that down-regulated DEGs involved in ECM proteoglycan pathways could be under control of both positive and negative fat-related lncRNAs. The present study, using pigs as an animal model, expands our current knowledge of possible gene expression regulation by lncRNAs in fat tissue and indicates for MALAT1 role in the fat deposition determination, which function is still often questioned or doubtful.

Keywords

Amodio N., Raimondi L., Juli G., Stamato M.A., Caracciolo D., Tagliaferri P., Tassone P. (2018). MALAT1: A druggable long non-coding RNA for targeted anti-cancer approaches. J. Hematol. Oncol., 11: 1–19. Search in Google Scholar

Carter S., Miard S., Boivin L., Sallé-Lefort S., Picard F. (2018). Loss of Malat1 does not modify age- or diet-induced adipose tissue accretion and insulin resistance in mice. PLoS One, 13.10.1371/journal.pone.0196603594498729746487 Search in Google Scholar

Chen H., Mo D., Li M, Zhang Y., Chen L., Zhang X., Li M., Zhou X., Chen Y. (2014). MiR-709 inhibits 3T3-L1 cell differentiation by targeting GSK3β of Wnt/β-catenin signaling. Cell. Signal., 26: 2583–2589. Search in Google Scholar

Cheng L., Nan C., Kang L., Zhang N., Liu S., Chen H., Hong C., Chen Y., Liang Z., Liu X. (2020). Whole blood transcriptomic investigation identifies long non-coding RNAs as regulators in sepsis. J. Transl. Med., 18: 217. Search in Google Scholar

Chessler S.D., Fujimoto W.Y., Shofer J.B., Boyko E.J., Weigle D.S. (1998). Increased plasma leptin levels are associated with fat accumulation in Japanese Americans. Diabetes, 47: 239–243. Search in Google Scholar

Deming Y., Li Z., Kapoor M., Harari O., Del -Aguila J.L., Black K., Carrell D., Cai Y., Fernandez M.V., Budde J., Ma S., Saef B., Howells B., Huang K. lin, Bertelsen S., Fagan A.M., Holtzman D.M., Morris J.C., Kim S., Saykin A.J., De Jager P.L., Albert M., Moghekar A., O’Brien R., Riemenschneider M., Petersen R.C., Blennow K., Zetterberg H., Minthon L., Van Deerlin V.M., Lee V.M.Y., Shaw L.M., Trojanowski J.Q., Schellenberg G., Haines J.L., Mayeux R., Pericak-Vance M.A., Farrer L.A., Peskind E.R., Li G., Di Narzo A.F., Kauwe J.S.K., Goate A.M., Cruchaga C. (2017). Genome-wide association study identifies four novel loci associated with Alzheimer’s endophenotypes and disease modifiers. Acta Neuropathol., 133: 839–856. Search in Google Scholar

Du J., Xu Y., Zhang P., Zhao X., Gan M., Li Q., Ma J., Tang G., Jiang Y., Wang J., Li X., Zhang S., Zhu L. (2018). MicroRNA-125a-5p Affects Adipocytes Proliferation, Differentiation and Fatty Acid Composition of Porcine Intramuscular Fat. Int. J. Mol. Sci., 19: 501. Search in Google Scholar

Ebrahimi R., Toolabi K., Jannat Ali Pour N., Mohassel Azadi S., Bahiraee A., Zamani-Garmsiri F., Emamgholipour S. (2020). Adipose tissue gene expression of long non-coding RNAs; MALAT1, TUG1 in obesity: Is it associated with metabolic profile and lipid homeostasis-related genes expression? Diabetol. Metab. Syndr., 12: 36. Search in Google Scholar

Eißmann M., Gutschner T., Hämmerle M., Günther S., Caudron -Herger M., Groß M., Schirmacher P., Rippe K., Braun T., Zörnig M., Diederichs S. (2012). Loss of the abundant nuclear non-coding RNA MALAT1 is compatible with life and development. RNA Biol., 9: 1076–1087. Search in Google Scholar

Foote A.P., Hales K.E., Kuehn L.A., Keisler D.H., King D.A., Shackelford S.D., Wheeler T.L., Freetly H.C. (2015). Relationship of leptin concentrations with feed intake, growth, and efficiency in finishing beef steers. J. Anim. Sci., 93: 4401–4407. Search in Google Scholar

Goyenechea E., Crujeiras A.B., Abete I., Martínez J.A. (2009). Expression of two inflammation-related genes (RIPK3 and RNF216) in mononuclear cells is associated with weight-loss regain in obese subjects. J. Nutrigenet. Nutrigenomics, 2: 78–84. Search in Google Scholar

Gutschner T., Hämmerle M., Eißmann M., Hsu J., Kim Y., Hung G., Revenko, A., Arun G., Stentrup M., Groß M., Zörnig M., MacLeod A.R., Spector D.L., Diederichs S. (2013). The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Res., 73: 1180–1189. Search in Google Scholar

Hou L., Shi J., Cao L., Xu G., Hu C., Wang C. (2017). Pig has no uncoupling protein 1. Biochem. Biophys. Res. Commun., 487: 795–800. Search in Google Scholar

Iacomino G., Siani A. (2017). Role of microRNAs in obesity and obesity-related diseases. Genes Nutr., 12.10.1186/s12263-017-0577-z561346728974990 Search in Google Scholar

Ji P., Diederichs S., Wang W., Böing S., Metzger R., Schneider P.M., Tidow N., Brandt B., Buerger H., Bulk E., Thomas M., Berdel W.E., Serve H., Müller-Tidow C. (2003). MALAT-1, a novel noncoding RNA, and thymosin β4 predict metastasis and survival in early-stage non-small cell lung cancer. Oncogene, 22: 8031–8041. Search in Google Scholar

Jia P., Wu N., Jia D., Sun Y. (2019). Downregulation of MALAT1 alleviates saturated fatty acid-induced myocardial inflammatory injury via the miR-26a/HMGB1/TLR4/NF-κB axis. Diabetes, Metab. Syndr. Obes. Targets Ther., 12: 655–665. Search in Google Scholar

Johnson R., Guigó R. (2014). The RIDL hypothesis: Transposable elements as functional domains of long noncoding RNAs. RNA, 20: 959–976. Search in Google Scholar

Joshi H., Vastrad B.M., Joshi N. (2020). Distinct Molecular Mechanisms Analysis of Obesity Based on Gene Expression Proles. Res. Sq. Search in Google Scholar

Kim J., Piao H.L., Kim B.J., Yao F., Han Z., Wang Y., Xiao Z., Siverly A.N., Lawhon S.E., Ton B.N., Lee H., Zhou Z., Gan B., Nakagawa S., Ellis M.J., Liang H., Hung M.C., You M.J., Su, Y., Ma L. (2018). Long noncoding RNA MALAT1 suppresses breast cancer metastasis. Nat. Genet., 50: 1705–1715. Search in Google Scholar

Kurył J., Kapelański W., Pierzchała M., Bocian M., Grajewska S. (2003). A relationship between genotypes at the GH and LEP loci and carcass meat and fat deposition in pigs. Anim. Sci. Pap. Reports, 21: 15–26. Search in Google Scholar

Liu L., Tan L., Yao J., Yang L. (2020). Long non-coding RNA MALAT1 regulates cholesterol accumulation in ox-LDL-induced macrophages via the microRNA-17-5p/ABCA1 axis. Mol. Med. Rep., 21: 1761–1770. Search in Google Scholar

Liu X., Li D., Zhang D., Yin D., Zhao Y., Ji C., Zhao X., Li X., He Q., Chen R., Hu S., Zhu L. (2018). A novel antisense long noncoding RNA, TWISTED LEAF, maintains leaf blade flattening by regulating its associated sense R2R3-MYB gene in rice. New Phytol., 218: 774–788. Search in Google Scholar

Love M.I., Huber W., Anders S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol., 15.10.1186/s13059-014-0550-8430204925516281 Search in Google Scholar

Mann M., Wright P.R., Backofen R. (2017). IntaRNA 2.0: Enhanced and customizable prediction of RNA-RNA interactions. Nucleic Acids Res., 45: W435–W439. Search in Google Scholar

Perdomo G., Kim D.H., Zhang T., Qu S., Thomas E.A., Toledo F.G.S., Slusher S., Fan Y., Kelley D.E., Dong H.H. (2010). A role of apolipoprotein D in triglyceride metabolism. J. Lipid Res., 51: 1298–1311. Search in Google Scholar

Pfaffl M.W., Tichopad A., Prgomet C., Neuvians T.P. (2004). Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper - Excel-based tool using pair-wise correlations. Biotechnol. Lett., 26: 509–515. Search in Google Scholar

Piórkowska K., Ropka-Molik K., Eckert R., Rózycki M. (2013). The expression pattern of proteolytic enzymes of cathepsin family in two important porcine skeletal muscles. Livest. Sci., 157: 427–434. Search in Google Scholar

Ropka-Molik K., Pawlina-Tyszko K., Żukowski K., Tyra M., Derebecka N., Wesoły J., Szmatoła T., Piórkowska K., 2020. Identification of Molecular Mechanisms Related to Pig Fatness at the Transcriptome and miRNAome Levels. Genes (Basel)., 11: 600.10.3390/genes11060600734875632485856 Search in Google Scholar

Scoville D.W., Kang H.S., Jetten A.M. (2017). GLIS1-3: Emerging roles in reprogramming, stem and progenitor cell differentiation and maintenance. Stem Cell Investig., 4.10.21037/sci.2017.09.01563901129057252 Search in Google Scholar

Sindhu S., Akhter N., Kochumon S., Thomas R., Wilson A., Shenouda S., Tuomilehto J., Ahmad R. (2018). Increased Expression of the Innate Immune Receptor TLR10 in Obesity and Type-2 Diabetes: Association with ROS-Mediated Oxidative Stress. Cell. Physiol. Biochem., 45: 572–590. Search in Google Scholar

Singh D.K., Prasanth K. V. (2013). Functional insights into the role of nuclear-retained long noncoding RNAs in gene expression control in mammalian cells. Chromosom. Res., 21: 695–711. Search in Google Scholar

Singh U.P., Singh N.P., Murphy E.A., Singh S.K., Price R.L., Nagarkatti M., Nagarkatti P.S. (2018). Adipose T cell microRNAs influence the T cell expansion, microbiome and macrophage function during obesity. J. Immunol., 200. Search in Google Scholar

Skorobogatko Y., Dragan M., Cordon C., Reilly S.M., Hung C.W., Xia W., Zhao P., Wallace M., Lackey D.E., Chen X.W., Osborn O., Bogner -Strauss J.G., Theodorescu D., Metallo C.M., Olefsky J.M., Saltiel A.R., 2018. RalA controls glucose homeostasis by regulating glucose uptake in brown fat. Proc. Natl. Acad. Sci. U. S. A., 115: 7819–7824.10.1073/pnas.1801050115606503729915037 Search in Google Scholar

Song W., Chen Y.P., Huang R., Chen K., Pan P.L., Li J., Yang Y., Shang H.F. (2012). GLIS1 rs797906: An increased risk factor for late-onset Parkinson’s disease in the han Chinese population. Eur. Neurol., 68: 89–92. Search in Google Scholar

Song Z., Cooper D.K.C., Cai Z., Mou L. (2018). Expression and regulation profile of mature microRNA in the pig: Relevance to xenotransplantation. Biomed Res. Int. 2018.10.1155/2018/2983908588440329750148 Search in Google Scholar

Takahashi, K., Sakurai, N., Emura, N., Hashizume, T., Sawai, K., 2015. Effects of downregulating GLIS1 transcript on preimplantation development and gene expression of bovine embryos. J. Reprod. Dev., 61: 369–374.10.1262/jrd.2015-029462314126074126 Search in Google Scholar

Tosic M., Allen A., Willmann D., Lepper C., Kim J., Duteil D., Schüle R. (2018). Lsd1 regulates skeletal muscle regeneration and directs the fate of satellite cells. Nat. Commun., 9.10.1038/s41467-017-02740-5578554029371665 Search in Google Scholar

Tripathi V., Ellis J.D., Shen Z., Song D.Y., Pan Q., Watt A.T., Freier S.M., Bennett C.F., Sharma A., Bubulya P.A., Blencowe B.J., Prasanth S.G., Prasanth K. V. (2010). The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol. Cell, 39: 925–938. Search in Google Scholar

Xia S.F., Duan X.M., Cheng X.R., Chen L.M., Kang Y.J., Wang P., Tang X., Shi Y.H., Le G.W. (2017). Role of miR-383 and miR-146b in different propensities to obesity in male mice. J. Endocrinol., 234: 201–216. Search in Google Scholar

Xu Y., Du J., Zhang P., Zhao X., Li Q., Jiang A., Jiang D., Tang G., Jiang Y., Wang J., Li X., Zhang S., Zhu L. (2018). MicroRNA-125a-5p Mediates 3T3-L1 Preadipocyte Proliferation and Differentiation. Molecules, 23: 317. Search in Google Scholar

Yan C., Chen J., Chen N. (2016). Long noncoding RNA MALAT1 promotes hepatic steatosis and insulin resistance by increasing nuclear SREBP-1c protein stability. Sci. Rep., 6: 1–11. Search in Google Scholar

Zhang B., Arun G., Mao Y.S., Lazar Z., Hung G., Bhattacharjee G., Xiao X., Booth C.J., Wu J., Zhang C., Spector D.L. (2012). The lncRNA malat1 is dispensable for mouse development but its transcription plays a cis-regulatory role in the adult. Cell Rep., 2: 111–123. Search in Google Scholar

Zhang X., Wang W., Zhu W., Dong J., Cheng Y., Yin Z., Shen F. (2019). Mechanisms and functions of long non-coding RNAs at multiple regulatory levels. Int. J. Mol. Sci., 20.10.3390/ijms20225573688808331717266 Search in Google Scholar

Zhang X., Zhou Y., Chen S., Li W., Chen W., Gu W. (2019). LncRNA MACC1-AS1 sponges multiple miRNAs and RNA-binding protein PTBP1. Oncogenesis, 8: 1–13. Search in Google Scholar

Zhu Y.-L., Chen T., Xiong J.-L., Wu D., Xi Q.-Y., Luo J.-Y., Sun J.-J., Zhang Y.-L. (2018). miR-146b Inhibits Glucose Consumption by Targeting IRS1 Gene in Porcine Primary Adipocytes. Int. J. Mol. Sci., 19: 783. Search in Google Scholar

Articoli consigliati da Trend MD

Pianifica la tua conferenza remota con Sciendo