A novel CDK-2 homolog identified in lamprey, Lampetra japonica, with roles in apoptosis

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Abstract

CDK-2, a member of the cyclin-dependent kinase family, plays an important role in many cell processes, such as cell cycle regulation, cell growth and differentiation, and cell apoptosis. Lampreys belong to the most primitive vertebrates, and there is no report about the CDK-2 gene in lampreys at present. In this study, a CDK-2-like gene sequence and deduced amino acid sequence were identified in Japanese lamprey (Lampetra japonica, L. japonica). The CDK-2-like gene has about 80% similarity with its homologs in jaw vertebrates. The polyclonal antibody against CDK-2-like was well prepared, and the results showed that CDK-2-like was highly expressed in the gonad tissue of lampreys. Apoptosis could reduce the expression of CDK-2-like in lymphocytes of lamprey, while overexpression of CDK-2-like could inhibit apoptosis. In addition, inhibition of CDK-2-like activity was able to trigger out apoptosis and also helped apoptotic inducer actinomycin D (Act-D) to induce apoptosis. These results suggest that CDK-2-like identified from lamprey may play a crucial role in apoptosis of jawless vertebrates.

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  • 20 November 2020

    The original version of the article unfortunately contained an error

References

  1. Amemiya CT, Saha NR, Zapata A (2007) Evolution and development of immunological structures in the lamprey. Curr Opin Immunol 19(5):535–541

    CAS  Article  Google Scholar 

  2. Boehm T, McCurley N, Sutoh Y, Schorpp M, Kasahara M, Cooper MD (2012) VLR-based adaptive immunity. Annu Rev Immunol 30:203–220

    CAS  Article  Google Scholar 

  3. Burningham RA, Arimura GK, Yunis AA (1966) Effect of Monase and related compounds on uptake of 5-hydroxytryptamine by platelets. Proc Soc Exp Biol Med 122(3):711–714

    CAS  Article  Google Scholar 

  4. Cheng W, Yang Z, Wang S, Li Y, Wei H, Tian X, Kan Q (2019) Recent development of CDK inhibitors: an overview of CDK/inhibitor co-crystal structures. Eur J Med Chem 164:615–639

    CAS  Article  Google Scholar 

  5. Chohan TA, Qian H, Pan Y, Chen JZ (2015) Cyclin-dependent kinase-2 as a target for cancer therapy: progress in the development of CDK2 inhibitors as anti-cancer agents. Curr Med Chem 22(2):237–263

    CAS  Article  Google Scholar 

  6. Cicenas J, Valius M (2011) The CDK inhibitors in cancer research and therapy. J Cancer Res Clin Oncol 137(10):1409–1418

    CAS  Article  Google Scholar 

  7. Cooper MD, Alder MN (2006) The evolution of adaptive immune systems. Cell 124(4):815–822

    CAS  Article  Google Scholar 

  8. Fischer PM, Gianella-Borradori A (2003) CDK inhibitors in clinical development for the treatment of cancer. Expert Opin Investig Drugs 12(6):955–970

    CAS  Article  Google Scholar 

  9. Fisher RP (2016) Getting to S: CDK functions and targets on the path to cell-cycle commitment. F1000Res 5:2374

    Article  Google Scholar 

  10. Furet P (2003) X-ray crystallographic studies of CDK2, a basis for cyclin-dependent kinase inhibitor design in anti-cancer drug research. Curr Med Chem Anticancer Agents 3(1):15–23

    CAS  Article  Google Scholar 

  11. Gladden AB, Diehl JA (2003) Cell cycle progression without cyclin E/CDK2: breaking down the walls of dogma. Cancer Cell 4(3):160–162

    CAS  Article  Google Scholar 

  12. Golsteyn RM (2005) Cdk1 and Cdk2 complexes (cyclin dependent kinases) in apoptosis: a role beyond the cell cycle. Cancer Lett 217(2):129–138

    CAS  Article  Google Scholar 

  13. Herrin BR, Cooper MD (2010) Alternative adaptive immunity in jawless vertebrates. J Immunol 185(3):1367–1374

    CAS  Article  Google Scholar 

  14. Hinchcliffe EH, Sluder G (2002) Two for two: Cdk2 and its role in centrosome doubling. Oncogene 21(40):6154–6160

    CAS  Article  Google Scholar 

  15. Hinds PW (2003) Cdk2 dethroned as master of S phase entry. Cancer Cell 3(4):305–307

    CAS  Article  Google Scholar 

  16. Hinds PW (2006) A confederacy of kinases: Cdk2 and Cdk4 conspire to control embryonic cell proliferation. Mol Cell 22(4):432–433

    CAS  Article  Google Scholar 

  17. Ishidate T, Elewa A, Kim S, Mello CC, Shirayama M (2014) Divide and differentiate: CDK/cyclins and the art of development. Cell Cycle 13(9):1384–1391

    CAS  Article  Google Scholar 

  18. Janvier P (2006) Paleontology: modern look for ancient lamprey. Nature 443(7114):921–924

    CAS  Article  Google Scholar 

  19. Kaldis P, Aleem E (2005) Cell cycle sibling rivalry: Cdc2 vs. Cdk2. Cell Cycle 4(11):1491–1494

    CAS  Article  Google Scholar 

  20. Kuratani S, Kuraku S, Murakami Y (2002) Lamprey as an evo-devo model: lessons from comparative embryology and molecular phylogenetics. Genesis 34(3):175–183

    CAS  Article  Google Scholar 

  21. Nikitina N, Bronner-Fraser M, Sauka-Spengler T (2009) The sea lamprey Petromyzon marinus: a model for evolutionary and developmental biology. Cold Spring Harb Protoc 2009(1):pdb. Emo 113

    Article  Google Scholar 

  22. Obaya AJ, Sedivy JM (2002) Regulation of cyclin-Cdk activity in mammalian cells. Cell Mol Life Sci 59(1):126–142

    CAS  Article  Google Scholar 

  23. Osório J, Rétaux S (2008) The lamprey in evolutionary studies. Dev Genes Evol 218(5):221–235

    Article  Google Scholar 

  24. Pancer Z, Amemiya CT, Ehrhardt GR, Ceitlin J, Gartland GL, Cooper MD (2004) Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430(6996):174–180

    CAS  Article  Google Scholar 

  25. Ruetz S, Fabbro D, Zimmermann J, Meyer T, Gray N (2003) Chemical and biological profile of dual Cdk1 and Cdk2 inhibitors. Curr Med Chem Anticancer Agents 3(1):1–14

    CAS  Article  Google Scholar 

  26. Shimeld SM, Donoghue PC (2012) Evolutionary crossroads in developmental biology: cyclostomes (lamprey and hagfish). Development 139(12):2091–2099

    CAS  Article  Google Scholar 

  27. Wadler S (2001) Perspectives for cancer therapies with cdk2 inhibitors. Drug Resist Updat 4(6):347–367

    CAS  Article  Google Scholar 

  28. Wood DJ, Endicott JA (2018) Structural insights into the functional diversity of the CDK-cyclin family. Open Biol 8(9):180112

    Article  Google Scholar 

  29. Xu Y, Zhu SW, Li QW (2016) Lamprey: a model for vertebrate evolutionary research. Zool Res 37(5):263–269

    PubMed  PubMed Central  Google Scholar 

  30. Youson JH, Sower SA (2001) Theory on the evolutionary history of lamprey metamorphosis: role of reproductive and thyroid axes. Comp Biochem Physiol B Biochem Mol Biol 129(2–3):337–345

    CAS  Article  Google Scholar 

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Funding

This study was supported by the Project funded by China Postdoctoral Science Foundation (2017M611257), Teachers guide undergraduates scientific research training project of Liaoning Normal University (CX201902062), the National Natural Science Foundation of China (31501911), the General Scientific Research Foundation of Liaoning Educational Committee (L2015293), and the Youth Scientific Research Project of Liaoning Normal University (LS2014L008).

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Y. X. conceived the study, designed experiments, and wrote the paper. Y. X., Y. T., H. Z., N. Z., and K. R. performed the experiments. Q. L. reviewed the study results and revised the manuscript. All of the authors reviewed the manuscript.

Corresponding authors

Correspondence to Yang Xu or Qingwei Li.

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The work was confirmed by the animal welfare and Research Ethics Committee of Dalian Medical University (license number SYXK2004-0029), and the methods were carried out according to the approved guidelines.

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The authors declare that they have no conflict of interest.

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Xu, Y., Tian, Y., Zhao, H. et al. A novel CDK-2 homolog identified in lamprey, Lampetra japonica, with roles in apoptosis. Fish Physiol Biochem 45, 1829–1843 (2019). https://doi.org/10.1007/s10695-019-00683-w

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Keywords

  • CDK-2
  • Lamprey
  • Evolution
  • Apoptosis