Abstract
Existing data indicate that YB-1, a gene member of the cold chock domain family, is regulated by cold stress in many species. However, information regarding YB-1 in fish is limited. To gain more insight into the potential biological function of YB-1 after cold stress, we have cloned YB-1 of the spotted sea bass (Lateolabrax maculatus) and studied the expression at transcriptional level of the LmYB-1 gene under low temperature. The cloned LmYB-1 cDNA (1454 bp) includes a 900-bp open-reading frame that encodes a 300-residue protein and contains C-terminal, CSD, and N-terminal domains. The results of real-time quantitative PCR showed that LmYB-1 was expressed in all tested tissues, with the highest expression in liver. Within liver, brain, and heart, LmYB-1 mRNA expression increased during cold stressed fish, compared to control fish. No significant induces in the expression of LmYB-1 were recorded in muscle, except at 10 °C during 24 h cold stress. Overexpression of LmYB-1 in CIK cells caused the upregulation of the expression of Hsc70, SOD1, and SOD2. Our results provided new insights into the LmYB-1 expression during cold stress and warranted further investigation into this potentially important protein in improving fish farming at low temperature.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Code availability
Not applicable.
Change history
14 June 2022
A Correction to this paper has been published: https://doi.org/10.1007/s10499-022-00914-7
References
Alemasova EE, Moor NA, Naumenko KN, Kutuzov MM, Sukhanova MV, Pestryakov PE, Lavrik OI (2016) Y-box-binding protein 1 as a non-canonical factor of base excision repair. Biochim Biophys Acta 1864:1631–1640. https://doi.org/10.1016/j.bbapap.2016.08.012
Alidousty C, Rauen T, Hanssen L, Wang Q, Alampour-Rajabi S, Mertens PR, Bernhagen J, Floege J, Ostendorf T, Raffetseder U (2014) Calcineurin-mediated YB-1 dephosphorylation regulates CCL5 expression during monocyte differentiation. J Biol Chem 289:21401–21412
Basaki Y, Taguchi K, Izumi H, Murakami Y, Kubo T, Hosoi F, Watari K, Nakano K, Kawaguchi H, Ohno S, Kohno K, Ono M, Kuwano M (2010) Y-box binding protein-1 (YB-1) promotes cell cycle progression through CDC6-dependent pathway in human cancer cells. Eur J Cancer 46:954–965. https://doi.org/10.1016/j.ejca.2009.12.024
Bates M, Boland A, McDermott N, Marignol L (2020) YB-1: The key to personalised prostate cancer management? Cancer Lett 490:66–75. https://doi.org/10.1016/j.canlet.2020.07.006
Bresciani G, da Cruz IB, Gonzalez-Gallego J (2015) Manganese superoxide dismutase and oxidative stress modulation. Adv Clin Chem 68:87–130. https://doi.org/10.1016/bs.acc.2014.11.001
Chu P, Wang T, Sun YR, Chu MX, Wang HY, Zheng X, Yin S (2021) Effect of cold stress on the MAPK pathway and lipidomics on muscle of Takifugu fasciatus. Aquaculture 540. https://doi.org/10.1016/j.aquaculture.2021.736691
Crawshaw GD, Wollmuth L, L S, (1985) Central nervous regulation of body temperature in vertebrates: comparative aspects. Pharmacol Ther 30:19–30
Cui J, Chu Q, Xu T (2016) miR-122 involved in the regulation of toll-like receptor signaling pathway after Vibrio anguillarum infection by targeting TLR14 in miiuy croaker. Fish Shellfish Immunol 58:67–72. https://doi.org/10.1016/j.fsi.2016.09.027
Dong S, Nie H, Li D, Cai Z, Sun X, Huo Z, Yan X (2020) Molecular cloning and characterization of Y-box gene (Rpybx) from Manila clam and its expression analysis in different strains under low-temperature stress. Anim Genet 51:430–438. https://doi.org/10.1111/age.12919
Dooley S, Said HM, Gressner AM, Floege J, En-Nia A, Mertens PR (2006) Y-box protein-1 is the crucial mediator of antifibrotic interferon-gamma effects. J Biol Chem 281:1784–1795. https://doi.org/10.1074/jbc.M510215200
Du J, Zeng Y, Wang H, Qian Y, Li H, Chen Q, Chen W, Cui J (2010) CuZnSOD gene expression and its relationship with anti-oxidative capacity and pork quality. South African Journal of Animal Science 40
El-Naggar AM, Veinotte CJ, Cheng H, Grunewald TGP, Negri LG (2015) Translational Activation of HIF1 alpha by YB-1 Promotes Sarcoma Metastasis. Cancer Cell 27:682–697
Evdokimova V, Ruzanov P, Imataka H, Raught B, Svitkin Y, Ovchinnikov LP, Sonenberg N (2001) The major mRNA-associated protein YB-1 is a potent 5’ cap-dependent mRNA stabilizer. EMBO J 20:5491–5502
Ewert L, Fischer A, Brandt S, Scurt FG, Philipsen L, Müller A, Girndt M, Zenclussen AC, Lindquist JA, Gorny X, Mentens R (2018) Cold shock Y-box binding protein-1 acetylation status in monocytes is associated with systemic inflammation and vascular damage. Atherosclerosis 278:156–165
Fishery Administration of the Ministry of Agriculture (2021) China fishery statistics yearbook. China Agriculture Press, Beijing, pp 22
Halliwell B, Gutteridge JJBj (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. 219 :1
He J, Xie TL, Li X, Yu Y, Zhan ZP, Weng SP, Guo CJ, He JG (2019) Molecular cloning of Y-Box binding protein-1 from mandarin fish and its roles in stress-response and antiviral immunity. Fish Shellfish Immunol 93:406–415. https://doi.org/10.1016/j.fsi.2019.07.069
Higashi K, Inagaki Y, Suzuki N, Mitsui S, Mauviel A, Kaneko H, Nakatsuka I (2003) Y-box-binding protein YB-1 mediates transcriptional repression of human alpha 2(I) collagen gene expression by interferon-gamma. J Biol Chem 278:5156–5162. https://doi.org/10.1074/jbc.M208724200
Homer C, Knight DA, Hananeia L, Sheard P, Risk J, Lasham A, Royds JA, Braithwaite AW (2005) Y-box factor YB1 controls p53 apoptotic function. Oncogene 24:8314–8325. https://doi.org/10.1038/sj.onc.1208998
Ivanova AA, Velichko AK, Kantidze OL, Razin SV (2015) Heat stress induces formation of cytoplasmic granules containing HSC70 protein. Dokl Biochem Biophys 463:213–215. https://doi.org/10.1134/S1607672915040043
Jia P, Jia KT, Yi MS (2015) Complete Genome Sequence of a Fish Nervous Necrosis Virus Isolated from Sea Perch (Lateolabrax japonicus) in China. Genome Announc 3. https://doi.org/10.1128/genomeA.00048-15
Jiao S, Nie M, Song H, Xu D, You F (2020) Physiological responses to cold and starvation stresses in the liver of yellow drum (Nibea albiflora) revealed by LC-MS metabolomics. Sci Total Environ 715:136940. https://doi.org/10.1016/j.scitotenv.2020.136940
Kim ER, Selyutina AA, Buldakov IA, Evdokimova V, Ovchinnikov LP, Sorokin AV (2013) The proteolytic YB-1 fragment interacts with DNA repair machinery and enhances survival during DNA damaging stress. Cell Cycle 12:3791–3803. https://doi.org/10.4161/cc.26670
Kloks CP, Spronk CA, Lasonder E, Hoffmann A, Vuister GW, Grzesiek S, Hilbers CW (2002) The solution structure and DNA-binding properties of the cold-shock domain of the human Y-box protein YB-1. J Mol Biol 316:317–326. https://doi.org/10.1006/jmbi.2001.5334
Kohno K, Izumi H, Uchiumi T, Ashizuka M, Kuwano M (2003) The pleiotropic functions of the Y-box-binding protein, YB-1. BioEssays 25:691–698. https://doi.org/10.1002/bies.10300
Koike K, Uchiumi T, Ohga T, Toh S, Wada M, Kohno K, Kuwano M (1997) Nuclear translocation of the Y-box binding protein by ultraviolet irradiation. FEBS Lett 417:390–394. https://doi.org/10.1016/s0014-5793(97)01296-9
Li G, Wang L, Wang Y, Li H, Liu Z, Wang H, Xu B, Guo X (2018) Developmental characterization and environmental stress responses of Y-box binding protein 1 gene (AccYB-1) from Apis cerana cerana. Gene 674:37–48. https://doi.org/10.1016/j.gene.2018.06.071
Liang XF, Hu L, Dong YC, Wu XF, Qin YC, Zheng YH, Shi DD, Xue M, Liang XF (2017) Substitution of fish meal by fermented soybean meal affects the growth performance and flesh quality of Japanese seabass ( Lateolabrax japonicus ). Anim Feed Sci Technol 229:1–12. https://doi.org/10.1016/j.anifeedsci.2017.03.006
Lindquist JA, Mertens PR (2018) Cold shock proteins: from cellular mechanisms to pathophysiology and disease. Cell Commun Signal 16:63. https://doi.org/10.1186/s12964-018-0274-6
Lindquist JA, Brandt S, Bernhardt A, Zhu C, Mertens PR (2014) The role of cold shock domain proteins in inflammatory diseases. J Mol Med (berl) 92:207–216. https://doi.org/10.1007/s00109-014-1136-3
Liu H, Xu D, Cui M, Hou T, Zhang Q (2018) The transcriptional factor YB-1 positively regulates Hsc70 transcription in Crassostrea hongkongensis. Biochem Biophys Res Commun 495:2404–2409. https://doi.org/10.1016/j.bbrc.2017.12.110
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Lu ZH, Books JT, Ley TJ (2006) Cold shock domain family members YB-1 and MSY4 share essential functions during murine embryogenesis. Mol Cell Biol 26:8410–8417. https://doi.org/10.1128/MCB.01196-06
Ma P, Yin X, Li D, Li L, Tang R (2021a) Acute temperature changes induce an oxidative stress response in kidney cells of grass carp Ctenopharyngodon idellus. Fish Sci 87:775–784. https://doi.org/10.1007/s12562-021-01545-2
Ma Z, Zhu Y, Wang Q, Deng M, Wang J, Li D, Gu L, Zhao R, Yan S (2021b) Y-box binding protein 1 regulates liver lipid metabolism by regulating the Wnt/beta-catenin signaling pathway. Ann Transl Med 9:1693. https://doi.org/10.21037/atm-21-5767
Makino Y, Ohga T, Toh S, Koike K, Okumura K, Wada M, Kuwano M, Kohno K (1996) Structural and Functional Analysis of the Human Y-Box Binding Protein (YB-1) Gene Promoter. Nucleic Acids Res 24:1873–1878
Matsumoto K, Wolffe AP (1998) Gene regulation by Y-box proteins: coupling control of transcription and translation. Trends Cell Biol 8:318
Nie H, Jiang L, Huo Z, Liu L, Yang F, Yan X (2016) Transcriptomic responses to low temperature stress in the Manila clam, Ruditapes philippinarum. Fish Shellfish Immunol 55:358–366. https://doi.org/10.1016/j.fsi.2016.06.008
Nie M, Hu J, Lu Y, Wu Z, Wang L, Xu D, Zhang P, You F (2019) Cold effect analysis and screening of SNPs associated with cold-tolerance in the olive flounder Paralichthys olivaceus. J Appl Ichthyol 35:924–932. https://doi.org/10.1111/jai.13908
Prakoso VA, Pouil S, Prabowo MNI, Sundari S, Arifin OZ, Subagja J, Affandi R, Kristanto AH, Slembrouck J (2019) Effects of temperature on the zootechnical performances and physiology of giant gourami (Osphronemus goramy) larvae. Aquaculture 510:160–168. https://doi.org/10.1016/j.aquaculture.2019.05.047
Prokešová M, Gebauer T, Matoušek J, Lundová K, Čejka J, Zusková E, Stejskal V (2020) Effect of temperature and oxygen regime on growth and physiology of juvenile Salvelinus fontinalis × Salvelinus alpinus hybrids. Aquaculture 522. doi:https://doi.org/10.1016/j.aquaculture.2020.735119
Przeslawski R, Ahyong S, Byrne M, WÖRheide G, Hutchings PAT, (2008) Beyond corals and fish: the effects of climate change on noncoral benthic invertebrates of tropical reefs. Glob Change Biol 14:2773–2795. https://doi.org/10.1111/j.1365-2486.2008.01693.x
Raffetseder U, Rauen T, Djudjaj S, Kretzler M, En-Nia A, Tacke F, Zimmermann HW, Nelson PJ, Frye BC, Floege J, Stefanidis I, Weber C, Mertens PR (2009) Differential regulation of chemokine CCL5 expression in monocytes/macrophages and renal cells by Y-box protein-1. Kidney Int 75:185–196. https://doi.org/10.1038/ki.2008.457
Raffetseder U, Liehn EA, Weber C, Mertens PR (2012) Role of cold shock Y-box protein-1 in inflammation, atherosclerosis and organ transplant rejection. Eur J Cell Biol 91:567–575. https://doi.org/10.1016/j.ejcb.2011.07.001
Rauen T, Frye BC, Wang J, Raffetseder U, Alidousty C, En-Nia A, Floege J, Mertens PR (2016) Cold shock protein YB-1 is involved in hypoxia-dependent gene transcription. Biochem Biophys Res Commun 478:982–987. https://doi.org/10.1016/j.bbrc.2016.08.064
Sangermano F, Delicato A, Calabro V (2020) Y box binding protein 1 (YB-1) oncoprotein at the hub of DNA proliferation, damage and cancer progression. Biochimie 179:205–216. https://doi.org/10.1016/j.biochi.2020.10.004
Skabkin MA, Evdokimova V, Thomas AA, Ovchinnikov LP (2001) The major messenger ribonucleoprotein particle protein p50 (YB-1) promotes nucleic acid strand annealing. J Biol Chem 276:44841–44847. https://doi.org/10.1074/jbc.M107581200
Song H, Xu D, Tian L, Chen R, Wang L, Tan P, You Q (2019) Overwinter mortality in yellow drum (Nibea albiflora): Insights from growth and immune responses to cold and starvation stress. Fish Shellfish Immunol 92:341–347. https://doi.org/10.1016/j.fsi.2019.06.030
Stickeler E, Fraser SD, Honig A, Chen AL, Cooper TA (2014) The RNA binding protein YB-1 binds A/C-rich exon enhancers and stimulates splicing of the CD44 alternative exon v4. EMBO J 20:3821–3830
Sun S, Fu H, Ge X, Zhu J, Zhang WJJoFoC (2017) Molecular cloning and expression analysis of cold shock protein Y-box gene from oriental river pawn(Macrobrachium nipponense). J Fish China 41
Sutherland BW, Kucab J, Wu J, Lee C, Cheang MC, Yorida E, Turbin D, Dedhar S, Nelson C, Pollak M, Leighton Grimes H, Miller K, Badve S, Huntsman D, Blake-Gilks C, Chen M, Pallen CJ, Dunn SE (2005) Akt phosphorylates the Y-box binding protein 1 at Ser102 located in the cold shock domain and affects the anchorage-independent growth of breast cancer cells. Oncogene 24:4281–4292. https://doi.org/10.1038/sj.onc.1208590
Takahashi M, Shimajiri S, Izumi H, Hirano G, Kashiwagi E, Yasuniwa Y, Wu Y, Han B, Akiyama M, Nishizawa S, Sasaguri Y, Kohno K (2010) Y-box binding protein-1 is a novel molecular target for tumor vessels. Cancer Sci 101:1367–1373. https://doi.org/10.1111/j.1349-7006.2010.01534.x
Takegaki T, Takeshita F (2020) Winter mortality of young mudskipper fish: Effects of size, temperature and energy depletion. J Exp Mar Biol Ecol 530-531. doi:https://doi.org/10.1016/j.jembe.2020.151436
Tanaka T, Ohashi S, Funakoshi T, Kobayashi S (2010) YB-1 binds to GluR2 mRNA and CaM1 mRNA in the brain and regulates their translational levels in an activity-dependent manner. Cell Mol Neurobiol 30:1089–1100. https://doi.org/10.1007/s10571-010-9541-9
Tanck M (2000) Cold shocks: a stressor for common carp. J Fish Biol 57:881–894. https://doi.org/10.1006/jfbi.2000.1355
Uramoto H, Izumi H, Ise T, Tada M, Uchiumi T, Kuwano M, Yasumoto K, Funa K, Kohno K (2002) p73 Interacts with c-Myc to Regulate Y-box-binding Protein-1 Expression. J Biol Chem 277:31694–31702. https://doi.org/10.1074/jbc.M200266200
Wang CY, Li ZB (2020) Growth performance, digestive enzyme activity and immune response of Japanese sea bass, Lateolabrax japonicus fed with fructooligosaccharide. Aquac Nutr 26:296–305. https://doi.org/10.1111/anu.12990
Wang M, Su X, Li Y, Jun Z, Li T (2010) Cloning and expression of the Mn-SOD gene from Phascolosoma esculenta. Fish Shellfish Immunol 29:759–764. https://doi.org/10.1016/j.fsi.2010.07.005
Wang XL, Zhang YX, Yang CG, Zhang B, Chen SL (2012) Cloning, characterization and expression analysis of a cold shock domain family member YB-1 in turbot Scophthalmus maximus. Fish Shellfish Immunol 33:1215–1221. https://doi.org/10.1016/j.fsi.2012.09.001
Wang Y, Wang F, Ji W-X, Han H, Li P (2015) Optimizing dietary protein sources for Japanese sea bass (Lateolabrax japonicus) with an emphasis on using poultry by-product meal to substitute fish meal. Aquac Res 46:874–883. https://doi.org/10.1111/are.12242
Wang Z, Dong Z, Yang Y, Wang J, Yang T, Chen X, Liang L, Mu W (2022) Histology, physiology, and glucose and lipid metabolism of Lateolabrax maculatus under low temperature stress. J Therm Biol 104:103161. https://doi.org/10.1016/j.jtherbio.2021.103161
Xie X, Xu K, Mao H, Lv Y, Weng P, Chang K, Lin G, Hu C (2020) Grass carp (Ctenopharyngodon idella) IRAK1 and STAT3 up-regulate synergistically the transcription of IL-10. Fish Shellfish Immunol 102:28–35. https://doi.org/10.1016/j.fsi.2020.04.014
Xu J-H, Qin J, Yan B-L, Zhu M, Luo G (2010) Effects of dietary lipid levels on growth performance, feed utilization and fatty acid composition of juvenile Japanese seabass (Lateolabrax japonicus) reared in seawater. Aquacult Int 19:79–89. https://doi.org/10.1007/s10499-010-9342-7
Xu D, You Q, Chi C, Luo S, Song H, Lou B, Takeuchi Y (2018) Transcriptional response to low temperature in the yellow drum (Nibea albiflora) and identification of genes related to cold stress. Comp Biochem Physiol Part D Genomics Proteomics 28:80–89. https://doi.org/10.1016/j.cbd.2018.07.003
Yang XJ, Zhu H, Mu SR, Wei WJ, Yuan X, Wang M, Liu Y, Hui J, Huang Y (2019) Crystal structure of a Y-box binding protein 1 (YB-1)-RNA complex reveals key features and residues interacting with RNA. J Biol Chem 294:10998–11010. https://doi.org/10.1074/jbc.RA119.007545
Yokoyama H, Harigae H, Takahashi S, Takahashi S, Furuyama K, Kaku M, Yamamoto M, Sasaki T (2003) Regulation of YB-1 gene expression by GATA transcription factors. Biochem Biophys Res Commun 303:140–145. https://doi.org/10.1016/s0006-291x(03)00296-1
Younes AF, Cerrato RM, Nye JA (2020) Overwintering survivorship and growth of young-of-the-year black sea bass Centropristis striata. PLoS One 15:e0236705. https://doi.org/10.1371/journal.pone.0236705
Zhang K, Liu X, Li X, Liu Y, Yu H, Liu J, Zhang Q (2020) Antibacterial functions of a novel fish-egg lectin from spotted knifejaw (Oplegnathus punctatus) during host defense immune responses. Dev Comp Immunol 111:103758. https://doi.org/10.1016/j.dci.2020.103758
Zhao Z, He R, Chu P, Cai H, Shen H, Zhao Z, Feng S, Cao D, Liao M, Gan G, Ye H, Chen Z, Qiu W, Deng J, Ming F, Ma M, Jia J, Wu J, Huang H, Sun C, Li J, Zhang L (2021) YBX has functional roles in CpG-ODN against cold stress and bacterial infection of Misgurnus anguillicaudatus. Fish Shellfish Immunol 118:72–84. https://doi.org/10.1016/j.fsi.2021.08.018
Funding
The research was supported by the the funding of “Blue granary” scientific and technological innovation of China (2019YFD0900405), and National Natural Science Foundation of China (32170523).
Author information
Authors and Affiliations
Contributions
Liqun Liang and Weijie Mu designed the experiments, analyzed data and wrote the manuscript together. The samples were obtained and the experiments were carried out by Zhen Wang and Jing Wang.
Corresponding authors
Ethics declarations
Ethics approval
The authors followed all applicable international, national, and/or institutional guidelines for animal care and use. However, this study was approved by the Ethics Committee of Heilongjiang River Fisheries Research Institute.
Consent to participate
All names in the author list have been involved in various stages of experimentation or writing.
Conflict of interest
The authors declare no competing interests.
Additional information
Handling Editor: Pierre Boudry
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
Wang, Z., Wang, J., Mu, W. et al. Molecular characterization, expression following cold stress, and functional characterization of YB-1 gene in the spotted sea bass (Lateolabrax maculatus). Aquacult Int 30, 1931–1950 (2022). https://doi.org/10.1007/s10499-022-00882-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-022-00882-y