Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Research Article

Comprehensive Analysis of lncRNA and mRNA Expression Profile of Macrophage RAW264.7 Stimulated by Antimicrobial Peptide BSN-37

Author(s): Ting Qin, Mingcheng Liu, Yanhe Lv, Airong Zheng, Lei Wang, Yundi Wu, Oksana Kasianenko, Xiaobing Wei, Zhanwei Teng, Xiaojing Xia* and Jianhe Hu*

Volume 30, Issue 9, 2023

Published on: 14 September, 2023

Page: [783 - 793] Pages: 11

DOI: 10.2174/0929866530666230816110009

Price: $65

Abstract

Background: BSN-37, a novel antimicrobial peptide (AMP) containing 37 amino acid residues isolated from the bovine spleen, has not only antibacterial activity but also immunomodulatory activity. Recent evidence shows that long non-coding RNAs (lncRNAs) play an important role in regulating the activation and function of immune cells. The purpose of this experiment was to investigate the lncRNA and mRNA expression profile of mouse macrophages RAW264.7 stimulated by bovine antimicrobial peptide BSN-37.

Methods: The whole gene expression microarray was used to detect the differentially expressed lncRNA and mRNA between antimicrobial peptide BSN-37 activated RAW264.7 cells and normal RAW264.7 cells. KEGG pathway analysis and GO function annotation analysis of differentially expressed lncRNAs and mRNA were carried out. Eight kinds of lncRNAs and nine kinds of mRNA with large differences were selected for qRT-PCR verification, respectively.

Results: In the current study, we found that 1294 lncRNAs and 260 mRNAs were differentially expressed between antibacterial peptide BSN-37 treatment and control groups. Among them, Bcl2l12, Rab44, C1s, Cd101 and other genes were associated with immune responses and were all significantly up-regulated. Mest and Prkcz are related to cell growth, and other genes are related to glucose metabolism and lipid metabolism. In addition, some immune-related terms were also found in the GO and KEGG analyses. At the same time, real-time quantitative PCR was used to verify selected lncRNA and mRNA with differential expression. The results of qRT-PCR verification were consistent with the sequencing results, indicating that our data were reliable.

Conclusion: This study provides the lncRNA and mRNA expression profiles of RAW264.7 macrophages stimulated by antimicrobial peptide BSN-37 and helps to provide a reference value for subsequent studies on lncRNA regulation of antimicrobial peptide BSN-37 immune function.

« Previous
Graphical Abstract

[1]
Nayab, S.; Aslam, M.A.; Rahman, S.; Sindhu, Z.D.; Sajid, S.; Zafar, N.; Razaq, M.; Kanwar, R.; Amanullah, A. Review of antimicrobial peptides: its function, mode of action and therapeutic potential. Int. J. Pept. Res. Ther., 2022, 28(1), 46.
[http://dx.doi.org/10.1007/s10989-021-10325-6]
[2]
Li, X.; Zuo, S.; Wang, B.; Zhang, K.; Wang, Y. Antimicrobial mechanisms and clinical application prospects of antimicrobial peptides. Molecules, 2022, 27(9), 2675.
[http://dx.doi.org/10.3390/molecules27092675] [PMID: 35566025]
[3]
Hang, B.; Zhang, W.; Li, J.; Xu, J.; Zhang, H.; Hu, J. Bioinformatics analysis of antimicrobial peptide BSN-37. J. Hen. Inst. Sci. Tech., 2018, 46(1), 34-38.
[http://dx.doi.org/10.3969/j.issn.1008-7516.2018.01.007]
[4]
van Harten, R.; van Woudenbergh, E.; van Dijk, A.; Haagsman, H. Cathelicidins: Immunomodulatory antimicrobials. Vaccines, 2018, 6(3), 63.
[http://dx.doi.org/10.3390/vaccines6030063] [PMID: 30223448]
[5]
Scheenstra, M.R.; van Harten, R.M.; Veldhuizen, E.J.A.; Haagsman, H.P.; Coorens, M. Cathelicidins modulate TLR-activation and inflammation. Front. Immunol., 2020, 11, 1137.
[http://dx.doi.org/10.3389/fimmu.2020.01137] [PMID: 32582207]
[6]
Xie, F.; Zan, Y.; Zhang, X.; Zhang, H.; Jin, M.; Zhang, W.; Zhang, Y.; Liu, S.; Zhang, W.; Zhang, Y.; Liu, S. Differential abilities of mammalian cathelicidins to inhibit bacterial biofilm formation and promote multifaceted immune functions of neutrophils. Int. J. Mol. Sci., 2020, 21(5), 1871-1871.
[http://dx.doi.org/10.3390/ijms21051871] [PMID: 32182913]
[7]
Kurosaka, K.; Chen, Q.; Yarovinsky, F.; Oppenheim, J.J.; Yang, D. Mouse cathelin-related antimicrobial peptide chemoattracts leukocytes using formyl peptide receptor-like 1/mouse formyl peptide receptor-like 2 as the receptor and acts as an immune adjuvant. J. Immunol., 2005, 174(10), 6257-6265.
[http://dx.doi.org/10.4049/jimmunol.174.10.6257] [PMID: 15879124]
[8]
Young-Speirs, M.; Drouin, D.; Cavalcante, P.A.; Barkema, H.W.; Cobo, E.R. Host defense cathelicidins in cattle: Types, production, bioactive functions and potential therapeutic and diagnostic applications. Int. J. Antimicrob. Agents, 2018, 51(6), 813-821.
[http://dx.doi.org/10.1016/j.ijantimicag.2018.02.006] [PMID: 29476808]
[9]
Quinn, J.J.; Chang, H.Y. Unique features of long non-coding RNA biogenesis and function. Nat. Rev. Genet., 2016, 17(1), 47-62.
[http://dx.doi.org/10.1038/nrg.2015.10] [PMID: 26666209]
[10]
Jiang, N.; Zhang, X.; Gu, X.; Li, X.; Shang, L. Progress in understanding the role of lncRNA in programmed cell death. Cell Death Discov., 2021, 7(1), 30.
[http://dx.doi.org/10.1038/s41420-021-00407-1] [PMID: 33558499]
[11]
Zhao, D.; Wang, C.; Yan, S.; Chen, R. Advances in the identification of long non-coding RNA binding proteins. Anal. Biochem., 2022, 639, 114520.
[http://dx.doi.org/10.1016/j.ab.2021.114520] [PMID: 34896376]
[12]
Atianand, M.K.; Caffrey, D.R.; Fitzgerald, K.A. Immunobiology of long noncoding RNAs. Annu. Rev. Immunol., 2017, 35(1), 177-198.
[http://dx.doi.org/10.1146/annurev-immunol-041015-055459] [PMID: 28125358]
[13]
Zhou, H.; Li, S.; Pan, W.; Wu, S.; Ma, F.; Jin, P. Interaction of lncRNA-CR33942 with Dif/Dorsal facilitates antimicrobial peptide transcriptions and enhances Drosophila toll immune responses. J. Immunol., 2022, 208(8), 1978-1988.
[http://dx.doi.org/10.4049/jimmunol.2100658] [PMID: 35379744]
[14]
Zhou, H.; Ni, J.; Wu, S.; Ma, F.; Jin, P.; Li, S. lncRNA-CR46018 positively regulates the drosophila toll immune response by interacting with Dif/Dorsal. Dev. Comp. Immunol., 2021, 124, 104183.
[http://dx.doi.org/10.1016/j.dci.2021.104183] [PMID: 34174242]
[15]
Zhou, H.; Li, S.; Wu, S.; Jin, P.; Ma, F. LncRNA-CR11538 Decoys Dif/Dorsal to reduce antimicrobial peptide products for restoring drosophila toll immunity homeostasis. Int. J. Mol. Sci., 2021, 22(18), 10117.
[http://dx.doi.org/10.3390/ijms221810117] [PMID: 34576280]
[16]
Du, J.; Chen, X.; Ye, Y.; Sun, H. A comparative study on the mechanisms of innate immune responses in mice induced by Alum and Actinidia eriantha polysaccharide. Int. J. Biol. Macromol., 2020, 156, 1202-1216.
[http://dx.doi.org/10.1016/j.ijbiomac.2019.11.158] [PMID: 31758993]
[17]
Yang, L.; Sun, Y.; Xu, Y.; Hang, B.; Wang, L.; Zhen, K.; Hu, B.; Chen, Y.; Xia, X.; Hu, J. Antibacterial peptide BSN-37 kills extra-and intra-cellular Salmonella enterica Serovar Typhimurium by a nonlytic mode of action. Front. Microbiol., 2020, 11, 174.
[http://dx.doi.org/10.3389/fmicb.2020.00174] [PMID: 32117178]
[18]
Li, C.; Chen, J.; Zhang, K.; Feng, B.; Wang, R.; Chen, L. Progress and prospects of long noncoding RNAs (lncRNAs) in hepatocellular carcinoma. Cell. Physiol. Biochem., 2015, 36(2), 423-434.
[http://dx.doi.org/10.1159/000430109] [PMID: 25968300]
[19]
Mahlapuu, M.; Björn, C.; Ekblom, J. Antimicrobial peptides as therapeutic agents: Opportunities and challenges. Crit. Rev. Biotechnol., 2020, 40(7), 978-992.
[http://dx.doi.org/10.1080/07388551.2020.1796576] [PMID: 32781848]
[20]
He, B. Adjuvant activity and application of antimicrobial peptide BSN-37; Henan institute of science and technology: Xinxiang, 2022.
[21]
Li, H.; Yang, D.; Tang, Z. Bcl2 like protein-12 suppresses Foxp3+ regulatory T cells in patients with rheumatoid arthritis. Am. J. Transl. Res., 2019, 11(5), 3048-3055.
[PMID: 31217874]
[22]
Kadowaki, T.; Yamaguchi, Y.; Kido, M.A.; Abe, T.; Ogawa, K.; Tokuhisa, M.; Gao, W.; Okamoto, K.; Kiyonari, H.; Tsukuba, T. The large GTPase Rab44 regulates granule exocytosis in mast cells and IgE-mediated anaphylaxis. Cell. Mol. Immunol., 2020, 17(12), 1287-1289.
[http://dx.doi.org/10.1038/s41423-020-0413-z] [PMID: 32238914]
[23]
Ye, J.; Yang, P.; Yang, Y.; Xia, S. Complement C1s as a diagnostic marker and therapeutic target: Progress and propective. Front. Immunol., 2022, 13, 1015128.
[http://dx.doi.org/10.3389/fimmu.2022.1015128] [PMID: 36275687]
[24]
Richert-Spuhler, L.E.; Mar, C.M.; Shinde, P.; Wu, F.; Hong, T.; Greene, E.; Hou, S.; Thomas, K.; Gottardo, R.; Mugo, N.; de Bruyn, G.; Celum, C.; Baeten, J.M.; Lingappa, J.R.; Lund, J.M.; Celum, C.; Wald, A.; Lingappa, J.R.; Baeten, J.M.; Campbell, M.S.; Corey, L.; Coombs, R.W.; Hughes, J.P.; Magaret, A.; McElrath, M.J.; Morrow, R.; Mullins, J.I.; Coetzee, D.; Fife, K.; Were, E.; Essex, M.; Makhema, J.; Katabira, E.; Ronald, A.; Bukusi, E.; Cohen, C.; Kapiga, S.; Manongi, R.; Farquhar, C.; John-Stewart, G.; Kiarie, J.; Delany-Moretlwe, S.; Rees, H.; de Bruyn, G.; Gray, G.; McIntyre, J.; Mugo, N.R.; Celum, C.; Baeten, J.M.; Donnell, D.; Coombs, R.W.; Frenkel, L.; Hendrix, C.W.; Lingappa, J.R.; McElrath, M.J.; Fife, K.; Were, E.; Tumwesigye, E.; Ndase, P.; Katabira, E.; Ronald, A.; Bukusi, E.; Cohen, C.; Wangisi, J.; Campbell, J.; Tappero, J.; Kiarie, J.; Farquhar, C.; John-Stewart, G.; Mugo, N.R. CD101 genetic variants modify regulatory and conventional T cell phenotypes and functions. Cell Rep. Med., 2021, 2(6), 100322.
[http://dx.doi.org/10.1016/j.xcrm.2021.100322] [PMID: 34195685]
[25]
Yeini, E.; Ofek, P.; Pozzi, S.; Albeck, N.; Ben-Shushan, D.; Tiram, G.; Golan, S.; Kleiner, R.; Sheinin, R.; Israeli Dangoor, S.; Reich-Zeliger, S.; Grossman, R.; Ram, Z.; Brem, H.; Hyde, T.M.; Magod, P.; Friedmann-Morvinski, D.; Madi, A.; Satchi-Fainaro, R. P-selectin axis plays a key role in microglia immunophenotype and glioblastoma progression. Nat. Commun., 2021, 12(1), 1912.
[http://dx.doi.org/10.1038/s41467-021-22186-0] [PMID: 33771989]
[26]
Chen, L.; Wu, X.; Xie, H.; Yao, N.; Xia, Y.; Ma, G.; Qian, M.; Ge, H.; Cui, Y.; Huang, Y.; Wang, S.; Zheng, M. ZFP57 suppress proliferation of breast cancer cells through down-regulation of MEST-mediated Wnt/β-catenin signalling pathway. Cell Death Dis., 2019, 10(3), 169.
[http://dx.doi.org/10.1038/s41419-019-1335-5] [PMID: 30787268]
[27]
Chow, Y.P.; Tan, L.P.; Chai, S.J.; Abdul Aziz, N.; Choo, S.W.; Lim, P.V.H.; Pathmanathan, R.; Mohd Kornain, N.K.; Lum, C.L.; Pua, K.C.; Yap, Y.Y.; Tan, T.Y.; Teo, S.H.; Khoo, A.S.B.; Patel, V. Exome Sequencing identifies potentially druggable mutations in nasopharyngeal carcinoma. Sci. Sci. Rep., 2017, 7(1), 42980.
[http://dx.doi.org/10.1038/srep42980] [PMID: 28256603]
[28]
Hugosson, F.; Sjögren, C.; Birve, A.; Hedlund, L.; Eriksson, T.; Palmer, R.H. The Drosophila midkine/pleiotrophin homologues Miple1 and Miple2 affect adult lifespan but are dispensable for alk signaling during embryonic gut formation. PLoS One, 2014, 9(11), e112250.
[http://dx.doi.org/10.1371/journal.pone.0112250] [PMID: 25380037]
[29]
Chen, F.; Sun, G.; Peng, J. RNAi-mediated HOXD3 knockdown inhibits growth in human RKO cells. Oncol. Rep., 2016, 36(4), 1793-1798.
[http://dx.doi.org/10.3892/or.2016.4993] [PMID: 27499213]
[30]
Li, Y.; Bai, M.; Xu, Y.; Zhao, W.; Liu, N.; Yu, J. TPPP3 promotes cell proliferation, invasion and tumor metastasis via stat3/twist1 pathway in non-small-cell lung carcinoma. Cell. Physiol. Biochem., 2018, 50(5), 2004-2016.
[http://dx.doi.org/10.1159/000494892] [PMID: 30404076]
[31]
Fu, C.; Liu, J.; Ma, K.; Jia, S. The role of GPLD1 in chronic disease. Chemistry of Life, 2021, 41(09), 1967-1973.
[http://dx.doi.org/10.13488/j.smhx.20210345]
[32]
Li, M.; Chen, D.; Huang, H.; Wang, J.; Wan, X.; Xu, C.; Li, C.; Ma, H.; Yu, C.; Li, Y. Caveolin1 protects against diet induced hepatic lipid accumulation in mice. PLoS One, 2017, 12(6), e0178748.
[http://dx.doi.org/10.1371/journal.pone.0178748] [PMID: 28570612]
[33]
Kim, Y.S.; Cho, H.H.; Cho, D.I.; Jeong, H.; Lim, S.; Jun, J.H.; Kim, M.R.; Kang, B.G.; Cho, M.; Kang, H.; Kang, W.S.; Oh, G.T.; Ahn, Y. The adipokine Retnla deficiency increases responsiveness to cardiac repair through adiponectin-rich bone marrow cells. Cell Death Dis., 2021, 12(4), 307.
[http://dx.doi.org/10.1038/s41419-021-03593-z] [PMID: 33753732]
[34]
Rogg, M.; Yasuda-Yamahara, M.; Abed, A.; Dinse, P.; Helmstädter, M.; Conzelmann, A.C.; Frimmel, J.; Sellung, D.; Biniossek, M.L.; Kretz, O.; Grahammer, F.; Schilling, O.; Huber, T.B.; Schell, C. The WD40-domain containing protein CORO2B is specifically enriched in glomerular podocytes and regulates the ventral actin cytoskeleton. Sci. Rep., 2017, 7(1), 15910.
[http://dx.doi.org/10.1038/s41598-017-15844-1] [PMID: 29162887]
[35]
Sun, Y.; Zhang, X.; Wang, Y.; Day, R.; Yang, H.; Zhang, Z. Immunity-related genes and signaling pathways under hypoxic stresses in Haliotis diversicolor: A transcriptome analysis. Sci. Rep., 2019, 9(1), 19741.
[http://dx.doi.org/10.1038/s41598-019-56150-2] [PMID: 31874975]
[36]
Yang, Y.; Han, T.; Xiao, J.; Li, X.; Wang, J. Transcriptome analysis reveals carbohydrate-mediated liver immune responses in Epinephelus akaara. Sci. Rep., 2018, 8(1), 639.
[http://dx.doi.org/10.1038/s41598-017-18990-8] [PMID: 29330509]
[37]
Ahrén, B. Glucagon : Early breakthroughs and recent discoveries. Peptides, 2015, 67, 74-81.
[http://dx.doi.org/10.1016/j.peptides.2015.03.011] [PMID: 25814364]
[38]
Lu, H.; Zhang, J.; Jiang, Z.; Zhang, M.; Wang, T.; Zhao, H.; Zeng, P. Detection of genetic overlap between rheumatoid arthritis and systemic lupus erythematosus using gwas summary statistics. Front. Genet., 2021, 12, 656545.
[http://dx.doi.org/10.3389/fgene.2021.656545] [PMID: 33815486]
[39]
Chen, Q.; He, G.; Zhang, W.; Xu, T.; Qi, H.; Li, J.; Zhang, Y.; Gao, M.Q. Stromal fibroblasts derived from mammary gland of bovine with mastitis display inflammation-specific changes. Sci. Rep., 2016, 6(1), 27462.
[http://dx.doi.org/10.1038/srep27462] [PMID: 27272504]
[40]
Ma, X.H.; Ren, H.J.; Peng, R.Y.; Li, Y.; Ming, L. Comparative expression profiles of host circulating miRNAs in response to Trichinella spiralis infection. Vet. Res., 2020, 51(1), 39.
[http://dx.doi.org/10.1186/s13567-020-00758-0] [PMID: 32156309]
[41]
Sebők, C.; Walmsley, S.; Tráj, P.; Mackei, M.; Vörösházi, J.; Petrilla, J.; Kovács, L.; Kemény, Á.; Neogrády, Z.; Mátis, G. Immunomodulatory effects of chicken cathelicidin-2 on a primary hepatic cell co-culture model. PLoS One, 2022, 17(10), e0275847.
[http://dx.doi.org/10.1371/journal.pone.0275847] [PMID: 36215285]
[42]
Wang, C.; Du, J.; Chen, X.; Zhu, Y.; Sun, H. Activation of RAW264.7 macrophages by active fraction of Albizia julibrissin saponin via Ca2+–ERK1/2–CREB–lncRNA pathways. Int. Immunopharmacol., 2019, 77, 105955.
[http://dx.doi.org/10.1016/j.intimp.2019.105955] [PMID: 31678866]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy