Abstract
Cold-inducible RNA-binding protein (CIRBP) responds to a wide array of cellular stresses such as cold shock, hypoxia, and inflammatory responses. However, functional studies of CIRBP in jawless vertebrates are limited. In this study, a CIRBP homolog from the jawless vertebrate lamprey (Lethenteron reissneri) was cloned and characterized (named Lr-CIRBP). The cDNA fragment of Lr-CIRBP has a 516 bp open reading frame (ORF) that encodes 171 amino acids, comprising a glycine-rich region at the C-terminal, similar to higher vertebrates but slightly shorter, and an RNA recognition motif (RRM) domain at the N-terminus. The predicted Lr-CIRBP sequence had 51.4 ~ 70.6% similarity with CIRBPs from other vertebrates. Further phylogenetic analysis revealed that Lr-CIRBP is located in the outgroup of vertebrates and is the ancestor of vertebrates. Based on real-time quantitative PCR experimental analysis, Lr-CIRBP expression was highest in leukocytes and increased significantly after multi-stimulation, peaking at 12 h. RNA interference showed that Lr-CIRBP knockdown can down-regulate the expression of inflammatory factors in Lethenteron reissneri. In conclusion, our study successfully clarifies the ancestral features and functions of CIRBP, while revealing valuable insight into how the protein is involved in the immune responses of a jawless vertebrate.
Data availability
All relevant data are available from the corresponding author upon reasonable request.
References
Aziz M, Brenner M, Wang P (2019) Extracellular CIRP (eCIRP) and inflammation. J Leukoc Biol 106(1):133–146. https://doi.org/10.1002/JLB.3MIR1118-443R
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208. https://doi.org/10.1093/nar/gkp335
Boehm T, McCurley N, Sutoh Y, Schorpp M, Kasahara M, Cooper MD (2012) VLR-based adaptive immunity. Annu Rev Immunol 30:203–220. https://doi.org/10.1146/annurev-immunol-020711-075038
Brochu C, Cabrita MA, Melanson BD, Hamill JD, Lau R, Pratt MA, McKay BC (2013) NF-κB-dependent role for cold-inducible RNA binding protein in regulating interleukin 1β. PLoS One 8(2):e57426. https://doi.org/10.1371/journal.pone.0057426
Chongsathidkiet P, Fecci PE (2021) Cold-inducible RNA-binding protein (CIRBP) as a biomarker to predict recurrence of brain metastases. Neuro Oncol 23(9):1419–1420. https://doi.org/10.1093/neuonc/noab122
Diao J, Yu X, Wang X, Fan Y, Wang S, Li L, Wang Y, Xu L, Gai C, Ye H, Liu H (2020) Full-length transcriptome sequencing combined with RNA-seq analysis revealed the immune response of fat greenling (Hexagrammos otakii) to Vibrio harveyi in early infection. Microb Pathog 149:104527. https://doi.org/10.1016/j.micpath.2020.104527
Horii Y, Shiina T, Uehara S, Nomura K, Shimaoka H, Horii K, Shimizu Y (2019) Hypothermia induces changes in the alternative splicing pattern of cold-inducible RNA-binding protein transcripts in a non-hibernator, the mouse. Biomed Res 40(4):153–161. https://doi.org/10.2220/biomedres.40.153
Hu J, You F, Wang Q, Wang L, Weng S, Xin M (2015) Cloning and expression analysis of cold-tolerance related genes CIRBP and HMGB1 in Paralichthys olivaceus. Mar Sci 39(01):29–38
Hunt SE, McLaren W, Gil L, Thormann A, Schuilenburg H, Sheppard D, Parton A, Armean IM, Trevanion SJ, Flicek P, Cunningham F (2018) Ensembl variation resources. Database 119. https://doi.org/10.1093/database/bay119
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096
Liu J, Xue J, Zhang H, Li S, Liu Y, Xu D, Zou M, Zhang Z, Diao J (2015) Cloning, expression, and purification of cold inducible RNA-binding protein and its neuroprotective mechanism of action. Brain Res 1597:189–195. https://doi.org/10.1016/j.brainres.2014.11.061
Letunic I, Bork P (2018) 20 years of the SMART protein domain annotation resource. Nucleic Acids Res 46(D1):D493–D496. https://doi.org/10.1093/nar/gkx922
Lopez MA, Meier D, Wong WW, Fontana A (2015) TNF induced inhibition of Cirbp expression depends on RelB NF-κB signalling pathway. Biochem Biophys Rep 5:22–26. https://doi.org/10.1016/j.bbrep.2015.11.007
Masuda T, Itoh K, Higashitsuji H, Higashitsuji H, Nakazawa N, Sakurai T, Liu Y, Tokuchi H, Fujita T, Zhao Y, Nishiyama H, Tanaka T, Fukumoto M, Ikawa M, Okabe M, Fujita J (2012) Cold-inducible RNA-binding protein (CIRP) interacts with Dyrk1b/Mirk and promotes proliferation of immature male germ cells in mice. Proc Natl Acad Sci USA 109(27):10885–10890. https://doi.org/10.1073/pnas.1121524109
Miao L, Li M, Chen Y, Hu M, Chen J (2017) Cloning of cold inducible RNA-binding protein (CIRP) gene in Larimichthys crocea and its expression analysis under cold treatments. J Fisheries China 41(04):481–489. https://doi.org/10.1016/S0065-3233(05)70008-5
Mitchell CD, Criscitiello MF (2020) Comparative study of cartilaginous fish divulges insights into the early evolution of primary, secondary and mucosal lymphoid tissue architecture. Fish Shellfish Immunol 107(Pt B):435–443. https://doi.org/10.1016/j.fsi.2020.11.006
Nguyen N, Vincens P, RoestCrollius H, Louis A (2018) Genomicus 2018: karyotype evolutionary trees and on-the-fly synteny computing. Nucleic Acids Res 46(D1):D816–D822. https://doi.org/10.1093/nar/gkx1003
Nikitina N, Bronner-Fraser M (2009) Sauka-Spengler T (2009) Microinjection of RNA and morpholino oligos into lamprey embryos. Cold Spring Harb Protoc 1:pdb.prot5123. https://doi.org/10.1101/pdb.prot5123
Nishiyama H, Itoh K, Kaneko Y, Kishishita M, Yoshida O, Fujita J (1997) A glycine-rich RNA-binding protein mediating cold-inducible suppression of mammalian cell growth. J Cell Biol 137(4):899–908. https://doi.org/10.1083/jcb.137.4.899
Pan F, Zarate J, Choudhury A, Rupprecht R, Bradley TM (2004) Osmotic stress of salmon stimulates upregulation of a cold inducible RNA binding protein (CIRP) similar to that of mammals and amphibians. Biochimie 86(7):451–461. https://doi.org/10.1016/j.biochi.2004.06.006
Saito T, Sugimoto K, Adachi Y, Wu Q, Mori KJ (2000) Cloning and characterization of amphibian cold inducible RNA-binding protein. Comparative biochemistry and physiology. Comp Biochem Physiol B Biochem Mol Biol 125(2):237–245
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Shiina T, Shimizu Y (2020) Temperature-dependent alternative splicing of precursor mRNAs and its biological significance: a review focused on post-transcriptional regulation of a cold shock protein gene in hibernating mammals. Int J Mol Sci 21(20):7599. https://doi.org/10.3390/ijms21207599
Smith JJ, Kuraku S, Holt C, Sauka-Spengler T, Jiang N, Campbell, M S, Yandell MD, Manousaki,T, Meyer A, Bloom OE, Morgan JR, Buxbaum JD, Sachidanandam R, Sims C, Garruss AS., Cook M, Krumlauf R, Wiedemann LM, Sower SA, Decatur WA, … Li, W (2013) Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat Genet 45(4):415–421e4212. https://doi.org/10.1038/ng.2568
Acknowledgements
The authors thank Jiao Tong of MEDx Co., Ltd for her help with this research.
Funding
This work was funded by the High-level Talent Innovation Support Program of Dalian (2017RQ046), the Young Star of Science and Technology of Dalian in 2020 (Grant No.2020RQ072), and the Youth Fund of Liaoning Provincial Department of Education (LQ2019025).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Ethics approval and consent to participate
All animal experiments were approved by the Animal Welfare and Research Ethics Committee of the Institute of Dalian Medical University and operated following the Guide for the Care and Use of Laboratory Animals 8th Edition Written by the National Research Council.
Competing interests
The authors declare no competing interests.
Additional information
Communicated by Matthias Hammerschmidt
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Duan, X., Pan, T., Wang, Z. et al. Molecular characterization and expression analysis of a novel cold-inducible RNA-binding protein (CIRBP) gene in lamprey (Lethenteron reissneri). Dev Genes Evol 233, 49–57 (2023). https://doi.org/10.1007/s00427-022-00700-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00427-022-00700-8