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Current Genomics

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ISSN (Print): 1389-2029
ISSN (Online): 1875-5488

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Research Article

Long Noncoding RNA and mRNA Expression Profiles in Rats with LPS-induced Myocardial Dysfunction

Author(s): Ye-Chen Han, Zhu-Jun Shen, Ruo-Lan Xiang, Bo Lu, Hao Qian, Jing-Yi Li and Hong-Zhi Xie*

Volume 23, Issue 6, 2022

Published on: 27 January, 2023

Page: [412 - 423] Pages: 12

DOI: 10.2174/1389202924666230119160258

Price: $65

Abstract

Background: Sepsis is an uncontrolled systemic inflammatory response. Long noncoding RNAs (lncRNAs) are involved in the pathogenesis of sepsis. However, little is known about the roles of lncRNAs in sepsis-induced myocardial dysfunction.

Objective: We aimed to determine the regulatory mechanism of lncRNAs in sepsis-induced myocardial dysfunction.

Methods: In this study, we analysed the lncRNA and mRNA expression profiles using microarray analysis. Gene Ontology, Kyoto Encyclopedia of Genes and Genomes, protein-protein interaction network, and gene set enrichment analysis were used to evaluate the data. We also constructed coding and noncoding coexpression and competing endogenous RNA networks to investigate the mechanisms.

Results: In vivo lipopolysaccharide -induced sepsis rat model was established. A total of 387 lncRNAs and 1,952 mRNAs were identified as significantly changed in the left ventricle. Kyoto Encyclopedia of Genes and Genomes analysis of mRNAs showed that the upregulated genes were mainly enriched in the “complement and coagulation cascade pathway” and “immune-related biological processes” terms. Eight significantly changed lncRNAs detected by RT-qPCR may be responsible for these processes. A competing endogenous RNA network was generated, and the results indicated that eight lncRNAs were related to the “calcium ion binding” process.

Conclusion: These results demonstrate that crosstalk between lncRNAs and mRNAs may play important roles in the development of sepsis-induced myocardial dysfunction.

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[1]
Singer, M.; Deutschman, C.S.; Seymour, C.W.; Shankar-Hari, M.; Annane, D.; Bauer, M.; Bellomo, R.; Bernard, G.R.; Chiche, J.D.; Coopersmith, C.M.; Hotchkiss, R.S.; Levy, M.M.; Marshall, J.C.; Martin, G.S.; Opal, S.M.; Rubenfeld, G.D.; van der Poll, T.; Vincent, J.L.; Angus, D.C. The third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA, 2016, 315(8), 801-810.
[http://dx.doi.org/10.1001/jama.2016.0287] [PMID: 26903338]
[2]
Kalla, C.; Raveh, D.; Algur, N.; Rudensky, B.; Yinnon, A.M.; Balkin, J. Incidence and significance of a positive troponin test in bacteremic patients without acute coronary syndrome. Am. J. Med., 2008, 121(10), 909-915.
[http://dx.doi.org/10.1016/j.amjmed.2008.05.037] [PMID: 18823863]
[3]
Boyd, J.; Mathur, S.; Wang, Y.; Bateman, R.; Walley, K. Toll-like receptor stimulation in cardiomyoctes decreases contractility and initiates an NF-κB dependent inflammatory response. Cardiovasc. Res., 2006, 72(3), 384-393.
[http://dx.doi.org/10.1016/j.cardiores.2006.09.011] [PMID: 17054926]
[4]
Andersson, D.C.; Fauconnier, J.; Yamada, T.; Lacampagne, A.; Zhang, S.J.; Katz, A.; Westerblad, H. Mitochondrial production of reactive oxygen species contributes to the β-adrenergic stimulation of mouse cardiomycytes. J. Physiol., 2011, 589(7), 1791-1801.
[http://dx.doi.org/10.1113/jphysiol.2010.202838] [PMID: 21486840]
[5]
Yang, F.; Xue, X.; Bi, J.; Zheng, L.; Zhi, K.; Gu, Y.; Fang, G. Long noncoding RNA CCAT1, which could be activated by c-Myc, promotes the progression of gastric carcinoma. J. Cancer Res. Clin. Oncol., 2013, 139(3), 437-445.
[http://dx.doi.org/10.1007/s00432-012-1324-x] [PMID: 23143645]
[6]
Pearson, M.J.; Jones, S.W. Review: Long noncoding RNAs in the regulation of inflammatory pathways in rheumatoid arthritis and osteoarthritis. Arthritis Rheumatol., 2016, 68(11), 2575-2583.
[http://dx.doi.org/10.1002/art.39759] [PMID: 27214788]
[7]
Chen, Y.; Qiu, J.; Chen, B.; Lin, Y.; Chen, Y.; Xie, G.; Qiu, J.; Tong, H.; Jiang, D. RETRACTED: Long non-coding RNA NEAT1 plays an important role in sepsis-induced acute kidney injury by targeting miR-204 and modulating the NF-κB pathway. Int. Immunopharmacol., 2018, 59, 252-260.
[http://dx.doi.org/10.1016/j.intimp.2018.03.023] [PMID: 29669307]
[8]
Fang, Y.; Hu, J.; Wang, Z.; Zong, H.; Zhang, L.; Zhang, R.; Sun, L. LncRNA H19 functions as an Aquaporin 1 competitive endogenous RNA to regulate microRNA-874 expression in LPS sepsis. Biomed. Pharmacother., 2018, 105, 1183-1191.
[http://dx.doi.org/10.1016/j.biopha.2018.06.007] [PMID: 30021355]
[9]
Han, Y.; Cai, Y.; Lai, X.; Wang, Z.; Wei, S.; Tan, K.; Xu, M.; Xie, H. lncRNA RMRP prevents mitochondrial dysfunction and cardiomyocyte apoptosis via the miR-1-5p/hsp70 axis in LPS-Induced sepsis mice. Inflammation, 2020, 43(2), 605-618.
[http://dx.doi.org/10.1007/s10753-019-01141-8] [PMID: 31900829]
[10]
Wu, H.; Liu, J.; Li, W.; Liu, G.; Li, Z. LncRNA-HOTAIR promotes TNF-α production in cardiomyocytes of LPS-induced sepsis mice by activating NF-κB pathway. Biochem. Biophys. Res. Commun., 2016, 471(1), 240-246.
[http://dx.doi.org/10.1016/j.bbrc.2016.01.117] [PMID: 26806307]
[11]
Ramachandran, G. Gram-positive and gram-negative bacterial toxins in sepsis. Virulence, 2014, 5(1), 213-218.
[http://dx.doi.org/10.4161/viru.27024] [PMID: 24193365]
[12]
Nie, M.W.; Han, Y.C.; Shen, Z.J.; Xie, H.Z. Identification of circRNA and mRNA expression profiles and functional networks of vascular tissue in lipopolysaccharide‐induced sepsis. J. Cell. Mol. Med., 2020, 24(14), 7915-7927.
[http://dx.doi.org/10.1111/jcmm.15424] [PMID: 32452125]
[13]
Zhang, T.N.; Yang, N.; Goodwin, J.E.; Mahrer, K.; Li, D.; Xia, J.; Wen, R.; Zhou, H.; Zhang, T.; Song, W.L.; Liu, C.F. Characterization of circular RNA and microRNA Profiles in septic myocardial depression: A lipopolysaccharide-induced rat septic shock model. Inflammation, 2019, 42(6), 1990-2002.
[http://dx.doi.org/10.1007/s10753-019-01060-8] [PMID: 31332662]
[14]
Shi, Y.; Shang, J. Long noncoding RNA expression profiling using arraystar LncRNA microarrays. Methods Mol. Biol., 2016, 1402, 43-61.
[http://dx.doi.org/10.1007/978-1-4939-3378-5_6] [PMID: 26721483]
[15]
Faghihi, M.A.; Wahlestedt, C. Regulatory roles of natural antisense transcripts. Nat. Rev. Mol. Cell Biol., 2009, 10(9), 637-643.
[http://dx.doi.org/10.1038/nrm2738] [PMID: 19638999]
[16]
Shang, Z.; Yu, J.; Sun, L.; Tian, J.; Zhu, S.; Zhang, B.; Dong, Q.; Jiang, N.; Flores-Morales, A.; Chang, C.; Niu, Y. LncRNA PCAT1 activates AKT and NF-κB signaling in castration-resistant prostate cancer by regulating the PHLPP/FKBP51/IKKα complex. Nucleic Acids Res., 2019, 47(8), 4211-4225.
[http://dx.doi.org/10.1093/nar/gkz108] [PMID: 30773595]
[17]
Yan, S.; Wang, P.; Wang, J.; Yang, J.; Lu, H.; Jin, C.; Cheng, M.; Xu, D. Long non-coding RNA HIX003209 promotes inflammation by sponging miR-6089 via TLR4/NF-κB signaling pathway in rheumatoid arthritis. Front. Immunol., 2019, 10, 2218.
[http://dx.doi.org/10.3389/fimmu.2019.02218] [PMID: 31620132]
[18]
Subramanian, A.; Tamayo, P.; Mootha, V.K.; Mukherjee, S.; Ebert, B.L.; Gillette, M.A.; Paulovich, A.; Pomeroy, S.L.; Golub, T.R.; Lander, E.S.; Mesirov, J.P. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA, 2005, 102(43), 15545-15550.
[http://dx.doi.org/10.1073/pnas.0506580102] [PMID: 16199517]
[19]
Guo, L.L.; Song, C.H.; Wang, P.; Dai, L.P.; Zhang, J.Y.; Wang, K.J. Competing endogenous RNA networks and gastric cancer. World J. Gastroenterol., 2015, 21(41), 11680-11687.
[http://dx.doi.org/10.3748/wjg.v21.i41.11680] [PMID: 26556995]
[20]
Mo, M.; Liu, S.; Ma, X.; Tan, C.; Wei, L.; Sheng, Y.; Song, Y.; Zeng, X.; Huang, D.; Qiu, X. A liver-specific lncRNA, FAM99B, suppresses hepatocellular carcinoma progression through inhibition of cell proliferation, migration, and invasion. J. Cancer Res. Clin. Oncol., 2019, 145(8), 2027-2038.
[http://dx.doi.org/10.1007/s00432-019-02954-8] [PMID: 31243545]
[21]
Ma, X.; Mo, M.; Tan, H.J.J.; Tan, C.; Zeng, X.; Zhang, G.; Huang, D.; Liang, J.; Liu, S.; Qiu, X. LINC02499, a novel liver‐specific long non‐coding RNA with potential diagnostic and prognostic value, inhibits hepatocellular carcinoma cell proliferation, migration, and invasion. Hepatol. Res., 2020, 50(6), 726-740.
[http://dx.doi.org/10.1111/hepr.13491] [PMID: 32039538]
[22]
Kong, L.; Wu, Q.; Zhao, L.; Ye, J.; Li, N.; Yang, H. Identification of messenger and long noncoding RNAs associated with gallbladder cancer via gene expression profile analysis. J. Cell. Biochem., 2019, 120(12), 19377-19387.
[http://dx.doi.org/10.1002/jcb.28953] [PMID: 31498480]
[23]
Levi, M.; van der Poll, T. Coagulation and sepsis. Thromb. Res., 2017, 149, 38-44.
[http://dx.doi.org/10.1016/j.thromres.2016.11.007] [PMID: 27886531]
[24]
Fiusa, M.M.L.; Carvalho-Filho, M.A.; Annichino-Bizzacchi, J.M.; De Paula, E.V. Causes and consequences of coagulation activation in sepsis: An evolutionary medicine perspective. BMC Med., 2015, 13(1), 105.
[http://dx.doi.org/10.1186/s12916-015-0327-2] [PMID: 25943883]
[25]
Lupu, F.; Keshari, R.S.; Lambris, J.D.; Coggeshall, K.M. Crosstalk between the coagulation and complement systems in sepsis. Thromb. Res., 2014, 133(Suppl. 1), S28-S31.
[http://dx.doi.org/10.1016/j.thromres.2014.03.014]
[26]
Ribeiro Machado, F.; Santucci Cesar, M. Sepsis, coagulation and anticoagulants. Endocr. Metab. Immune Disord. Drug Targets, 2010, 10(3), 204-213.
[http://dx.doi.org/10.2174/187153010791936892] [PMID: 20509839]
[27]
Schultz, M.; van der Poll, T.; Levi, M. Sepsis and thrombosis. Semin. Thromb. Hemost., 2013, 39(5), 559-566.
[http://dx.doi.org/10.1055/s-0033-1343894] [PMID: 23625756]
[28]
Hotchkiss, R.S.; Monneret, G.; Payen, D. Sepsis-induced immunosuppression: from cellular dysfunctions to immunotherapy. Nat. Rev. Immunol., 2013, 13(12), 862-874.
[http://dx.doi.org/10.1038/nri3552] [PMID: 24232462]
[29]
Pei, F; Guan, X; Wu, J. Thymosin alpha 1 treatment for patients with sepsis. Expert Opin Biol Ther., 2018, 18(Suppl. 1), 71-76.
[http://dx.doi.org/10.1080/14712598.2018.1484104]
[30]
Hotchkiss, R.S.; Monneret, G.; Payen, D. Immunosuppression in sepsis: A novel understanding of the disorder and a new therapeutic approach. Lancet Infect. Dis., 2013, 13(3), 260-268.
[http://dx.doi.org/10.1016/S1473-3099(13)70001-X] [PMID: 23427891]
[31]
Patil, N.K.; Bohannon, J.K.; Sherwood, E.R. Immunotherapy: A promising approach to reverse sepsis-induced immunosuppression. Pharmacol. Res., 2016, 111, 688-702.
[http://dx.doi.org/10.1016/j.phrs.2016.07.019] [PMID: 27468649]
[32]
Obaid, M.; Udden, S.M.N.; Deb, P.; Shihabeddin, N.; Zaki, M.H.; Mandal, S.S. LncRNA HOTAIR regulates lipopolysaccharide-induced cytokine expression and inflammatory response in macrophages. Sci. Rep., 2018, 8(1), 15670.
[http://dx.doi.org/10.1038/s41598-018-33722-2] [PMID: 30353135]
[33]
Gomez, J.A.; Wapinski, O.L.; Yang, Y.W.; Bureau, J.F.; Gopinath, S.; Monack, D.M.; Chang, H.Y.; Brahic, M.; Kirkegaard, K. The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-γ locus. Cell, 2013, 152(4), 743-754.
[http://dx.doi.org/10.1016/j.cell.2013.01.015] [PMID: 23415224]
[34]
Imamura, K.; Imamachi, N.; Akizuki, G.; Kumakura, M.; Kawaguchi, A.; Nagata, K.; Kato, A.; Kawaguchi, Y.; Sato, H.; Yoneda, M.; Kai, C.; Yada, T.; Suzuki, Y.; Yamada, T.; Ozawa, T.; Kaneki, K.; Inoue, T.; Kobayashi, M.; Kodama, T.; Wada, Y.; Sekimizu, K.; Akimitsu, N. Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. Mol. Cell, 2014, 53(3), 393-406.
[http://dx.doi.org/10.1016/j.molcel.2014.01.009] [PMID: 24507715]
[35]
Gast, M.; Rauch, B.H.; Haghikia, A.; Nakagawa, S.; Haas, J.; Stroux, A.; Schmidt, D.; Schumann, P.; Weiss, S.; Jensen, L.; Kratzer, A.; Kraenkel, N.; Müller, C.; Börnigen, D.; Hirose, T.; Blankenberg, S.; Escher, F.; Kühl, A.A.; Kuss, A.W.; Meder, B.; Landmesser, U.; Zeller, T.; Poller, W. Long noncoding RNA NEAT1 modulates immune cell functions and is suppressed in early onset myocardial infarction patients. Cardiovasc. Res., 2019, 115(13), 1886-1906.
[http://dx.doi.org/10.1093/cvr/cvz085] [PMID: 30924864]
[36]
Liu, T.L.; Fan, X.C.; Li, Y.H.; Yuan, Y.J.; Yin, Y.L.; Wang, X.T.; Zhang, L.X.; Zhao, G.H. Expression profiles of mRNA and lncRNA in HCT-8 cells infected with Cryptosporidium parvum IId subtype. Front. Microbiol., 2018, 9, 1409.
[http://dx.doi.org/10.3389/fmicb.2018.01409] [PMID: 30013528]
[37]
Xiao, B.; Zhang, W.; Chen, L.; Hang, J.; Wang, L.; Zhang, R.; Liao, Y.; Chen, J.; Ma, Q.; Sun, Z.; Li, L. Analysis of the miRNA–mRNA–lncRNA network in human estrogen receptor-positive and estrogen receptor-negative breast cancer based on TCGA data. Gene, 2018, 658, 28-35.
[http://dx.doi.org/10.1016/j.gene.2018.03.011] [PMID: 29518546]
[38]
Wang, J.; Yin, J.; Wang, X.; Liu, H.; Hu, Y.; Yan, X.; Zhuang, B.; Yu, Z.; Han, S. Changing expression profiles of mRNA, lncRNA, circRNA, and miRNA in lung tissue reveal the pathophysiological of bronchopulmonary dysplasia (BPD) in mouse model. J. Cell. Biochem., 2019, 120(6), 9369-9380.
[http://dx.doi.org/10.1002/jcb.28212] [PMID: 30802330]
[39]
Hobai, I.A.; Edgecomb, J.; LaBarge, K.; Colucci, W.S. Dysregulation of intracellular calcium transporters in animal models of sepsis-induced cardiomyopathy. Shock, 2015, 43(1), 3-15.
[http://dx.doi.org/10.1097/SHK.0000000000000261] [PMID: 25186837]
[40]
Zhu, X.; Bernecker, O.Y.; Manohar, N.S.; Hajjar, R.J.; Hellman, J.; Ichinose, F.; Valdivia, H.H.; Schmidt, U. Increased leakage of sarcoplasmic reticulum Ca2+ contributes to abnormal myocyte Ca2+ handling and shortening in sepsis. Crit. Care Med., 2005, 33(3), 598-604.
[http://dx.doi.org/10.1097/01.CCM.0000152223.27176.A6] [PMID: 15753753]
[41]
Joseph, L.C.; Kokkinaki, D.; Valenti, M.C.; Kim, G.J.; Barca, E.; Tomar, D.; Hoffman, N.E.; Subramanyam, P.; Colecraft, H.M.; Hirano, M.; Ratner, A.J.; Madesh, M.; Drosatos, K.; Morrow, J.P. Inhibition of NADPH oxidase 2 (NOX2) prevents sepsis-induced cardiomyopathy by improving calcium handling and mitochondrial function. JCI Insight, 2017, 2(17), e94248.
[http://dx.doi.org/10.1172/jci.insight.94248] [PMID: 28878116]
[42]
Han, Y.C.; Xie, H.Z.; Lu, B.; Xiang, R.L.; Zhang, H.P.; Li, J.Y.; Zhang, S.Y. Lipopolysaccharide alters the m6A epitranscriptomic tagging of RNAs in cardiac tissue. Front. Mol. Biosci., 2021, 8, 670160.
[http://dx.doi.org/10.3389/fmolb.2021.670160] [PMID: 34395520]
[43]
Zhang, T.N.; Goodwin, J.E.; Liu, B.; Li, D.; Wen, R.; Yang, N.; Xia, J.; Zhou, H.; Zhang, T.; Song, W.L.; Liu, C.F. Characterization of long noncoding RNA and mRNA profiles in sepsis-induced myocardial depression. Mol. Ther. Nucleic Acids, 2019, 17, 852-866.
[http://dx.doi.org/10.1016/j.omtn.2019.07.020] [PMID: 31472370]

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