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Fish Physiology and Biochemistry

, Volume 45, Issue 6, pp 1829–1843 | Cite as

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

  • Yang XuEmail author
  • Yang Tian
  • Huan Zhao
  • Nan Zheng
  • Kaixia Ren
  • Qingwei LiEmail author
Article

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.

Keywords

CDK-2 Lamprey Evolution Apoptosis 

Notes

Author contributions

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.

Funding information

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).

Compliance with ethical standards

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.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Amemiya CT, Saha NR, Zapata A (2007) Evolution and development of immunological structures in the lamprey. Curr Opin Immunol 19(5):535–541PubMedPubMedCentralCrossRefGoogle Scholar
  2. Boehm T, McCurley N, Sutoh Y, Schorpp M, Kasahara M, Cooper MD (2012) VLR-based adaptive immunity. Annu Rev Immunol 30:203–220PubMedPubMedCentralCrossRefGoogle 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):711–714PubMedCrossRefGoogle 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 164:615–639PubMedCrossRefGoogle 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):237–263PubMedCrossRefGoogle Scholar
  6. Cicenas J, Valius M (2011) The CDK inhibitors in cancer research and therapy. J Cancer Res Clin Oncol 137(10):1409–1418PubMedCrossRefGoogle Scholar
  7. Cooper MD, Alder MN (2006) The evolution of adaptive immune systems. Cell 124(4):815–822PubMedCrossRefGoogle Scholar
  8. Fischer PM, Gianella-Borradori A (2003) CDK inhibitors in clinical development for the treatment of cancer. Expert Opin Investig Drugs 12(6):955–970PubMedCrossRefGoogle Scholar
  9. Fisher RP (2016) Getting to S: CDK functions and targets on the path to cell-cycle commitment. F1000Res 5:2374PubMedPubMedCentralCrossRefGoogle 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):15–23PubMedCrossRefGoogle Scholar
  11. Gladden AB, Diehl JA (2003) Cell cycle progression without cyclin E/CDK2: breaking down the walls of dogma. Cancer Cell 4(3):160–162PubMedCrossRefGoogle Scholar
  12. Golsteyn RM (2005) Cdk1 and Cdk2 complexes (cyclin dependent kinases) in apoptosis: a role beyond the cell cycle. Cancer Lett 217(2):129–138PubMedCrossRefGoogle Scholar
  13. Herrin BR, Cooper MD (2010) Alternative adaptive immunity in jawless vertebrates. J Immunol 185(3):1367–1374PubMedCrossRefGoogle Scholar
  14. Hinchcliffe EH, Sluder G (2002) Two for two: Cdk2 and its role in centrosome doubling. Oncogene 21(40):6154–6160PubMedCrossRefGoogle Scholar
  15. Hinds PW (2003) Cdk2 dethroned as master of S phase entry. Cancer Cell 3(4):305–307PubMedCrossRefGoogle Scholar
  16. Hinds PW (2006) A confederacy of kinases: Cdk2 and Cdk4 conspire to control embryonic cell proliferation. Mol Cell 22(4):432–433PubMedCrossRefGoogle 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):1384–1391PubMedPubMedCentralCrossRefGoogle Scholar
  18. Janvier P (2006) Paleontology: modern look for ancient lamprey. Nature 443(7114):921–924PubMedCrossRefGoogle Scholar
  19. Kaldis P, Aleem E (2005) Cell cycle sibling rivalry: Cdc2 vs. Cdk2. Cell Cycle 4(11):1491–1494PubMedCrossRefGoogle 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):175–183PubMedCrossRefGoogle 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 113CrossRefGoogle Scholar
  22. Obaya AJ, Sedivy JM (2002) Regulation of cyclin-Cdk activity in mammalian cells. Cell Mol Life Sci 59(1):126–142PubMedCrossRefGoogle Scholar
  23. Osório J, Rétaux S (2008) The lamprey in evolutionary studies. Dev Genes Evol 218(5):221–235PubMedCrossRefGoogle 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):174–180PubMedCrossRefGoogle 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):1–14PubMedCrossRefGoogle Scholar
  26. Shimeld SM, Donoghue PC (2012) Evolutionary crossroads in developmental biology: cyclostomes (lamprey and hagfish). Development 139(12):2091–2099PubMedCrossRefGoogle Scholar
  27. Wadler S (2001) Perspectives for cancer therapies with cdk2 inhibitors. Drug Resist Updat 4(6):347–367PubMedCrossRefGoogle Scholar
  28. Wood DJ, Endicott JA (2018) Structural insights into the functional diversity of the CDK-cyclin family. Open Biol 8(9):180112PubMedPubMedCentralCrossRefGoogle Scholar
  29. Xu Y, Zhu SW, Li QW (2016) Lamprey: a model for vertebrate evolutionary research. Zool Res 37(5):263–269PubMedPubMedCentralGoogle 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):337–345PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.College of Life ScienceLiaoning Normal UniversityDalianChina
  2. 2.Lamprey Research CenterLiaoning Normal UniversityDalianChina

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