DOI QR코드

DOI QR Code

Identification and characterization of a rice MCM2 homologue required for DNA replycation

  • Cho, Jae-Han (Department of Biological Sciences, Myongji University) ;
  • Kim, Ho-Bang (Department of Biological Sciences, Myongji University) ;
  • Kim, Hyung-Sae (Department of Biological Sciences, Myongji University) ;
  • Choi, Sang-Bong (Department of Biological Sciences, Myongji University)
  • Published : 2008.08.31

Abstract

The pre-replication complex (pre-RC), including the core hexameric MCM2-7 complex, ensures that the eukaryotic genome is replicated only once per cell division cycle. In this study, we identified a rice $\underline{m}ini\underline{c}hromosome$ $\underline{m}aintenance$ (MCM) homologue (OsMCM2) that functionally complemented fission yeast MCM2 (CDC19) mutants. We found OsMCM2 transcript expression in roots, leaves, and seeds, although expression levels differed slightly among the organs. Likewise, the OsMCM2 protein was ubiquitously expressed, but it was downregulated when nutritients were limiting, indicating that MCM2 expression (and therefore cell cycle progression) requires adequate nutrition. Yeast two-hybrid and GST pull-down assays demonstrated that OsMCM2 interacted with the COP9 signalosome 5 (CSN5). Taken as a whole, our results indicated that OsMCM2 functions as a subunit of the rice MCM complex and interacts with CSN5 during developmental regulation.

Keywords

References

  1. Tye, B. K. (1999) MCM proteins in DNA replication. Annu. Rev. Biochem. 68, 649-686. https://doi.org/10.1146/annurev.biochem.68.1.649
  2. Blow, J. J. and Dutta, A. (2005) Preventing re-replication of chromosomal DNA. Nat. Rev. Mol. Cell Biol. 6, 476-486. https://doi.org/10.1038/nrm1663
  3. Forsburg, S. L. (2004) Eukaryotic MCM proteins: beyond replication initiation. Microbiol. Mol. Biol. Rev. 68, 109- 131. https://doi.org/10.1128/MMBR.68.1.109-131.2004
  4. Forsburg, S. L. (2008) The MCM helicase: linking checkpoints to the replication fork. Biochem. Soc. Trans. 36, 114-119. https://doi.org/10.1042/BST0360114
  5. Tye, B. K. and Sawyer, S. (2000) The hexameric eukaryotic MCM helicase: building symmetry from nonidentical parts. J. Biol. Chem. 275, 34833-34836. https://doi.org/10.1074/jbc.R000018200
  6. Ishimi, Y. (1997) A DNA helicase activity is associated with an MCM4, -6, and -7 protein complex. J. Biol. Chem. 272, 24508-24513. https://doi.org/10.1074/jbc.272.39.24508
  7. Dresselhaus, T., Srilunchang, K. O., Leljak-Levanic, D., Schreiber, D. N. and Garg, P. (2006) The fertilization- induced DNA replication factor MCM6 of maize shuttles betweencytoplasm and nucleus, and is essential for plant growth and development. Plant Physiol. 140, 512-527. https://doi.org/10.1104/pp.105.074294
  8. Sabelli, P. A., Burgess, S. R., Kush, A. K., Young, M. R. and Shewry, P. R. (1996) cDNA cloning and characterisation of a maize homologue of the MCM proteins required for the initiation of DNA replication. Mol. Gen. Genet. 252, 125- 136. https://doi.org/10.1007/BF02173212
  9. Springer, P. S., Holding, D. R., Groover, A., Yordan, C. and Martienssen, R. A. (2000) The essential Mcm7 protein PROLIFERA is localized to the nucleus of dividing cells during the G(1) phase and is required maternally for early Arabidopsis development. Development 127, 1815-1822.
  10. Springer, P. S., McCombie, W. R., Sundaresan, V. and Martienssen, R. A. (1995) Gene trap tagging of PROLIFERA, an essential MCM2-3-5-like gene in Arabidopsis. Science 268, 877-880. https://doi.org/10.1126/science.7754372
  11. Lei, M. and Tye, B. K. (2001) Initiating DNA synthesis: from recruiting to activating the MCM complex. J. Cell Sci. 114, 1447-1454.
  12. Komamura-Kohno, Y., Tanaka, R., Omori, A., Kohno, T. and Ishimi, Y. (2008) Biochemical characterization of fragmented human MCM2. FEBS J. 275, 727-738. https://doi.org/10.1111/j.1742-4658.2007.06239.x
  13. Crevel, G., Ivetic, A., Ohno, K., Yamaguchi, M. and Cotterill, S. (2001) Nearest neighbour analysis of MCM protein complexes in Drosophila melanogaster. Nucleic Acids Res. 29, 4834-4842. https://doi.org/10.1093/nar/29.23.4834
  14. Schwacha, A. and Bell, S. P. (2001) Interactions between two catalytically distinct MCM subgroups are essential for coordinated ATP hydrolysis and DNA replication. Mol. Cell. 8, 1093-1104. https://doi.org/10.1016/S1097-2765(01)00389-6
  15. Ishimi, Y., Ichinose, S., Omori, A., Sato, K. and Kimura, H. (1996) Binding of human minichromosome maintenance proteins with histone H3. J. Biol. Chem. 271, 24115-24122. https://doi.org/10.1074/jbc.271.39.24115
  16. Ishimi, Y., Komamura, Y., You, Z. and Kimura, H. (1998) Biochemical function of mouse minichromosome maintenance 2 protein. J. Biol. Chem. 273, 8369-8375. https://doi.org/10.1074/jbc.273.14.8369
  17. Burke, T. W., Cook, J. G., Asano, M. and Nevins, J. R. (2001) Replication factors MCM2 and ORC1 interact with the histone acetyltransferase HBO1. J. Biol. Chem. 276, 15397-15408. https://doi.org/10.1074/jbc.M011556200
  18. Holland, L., Gauthier, L., Bell-Rogers, P. and Yankulov, K. (2002) Distinct parts of minichromosome maintenance protein 2 associate with histone H3/H4 and RNA polymerase II holoenzyme. Eur. J. Biochem. 269, 5192-5202. https://doi.org/10.1046/j.1432-1033.2002.03224.x
  19. Ishimi, Y., Komamura-Kohno, Y., Arai, K. and Masai, H. (2001) Biochemical activities associated with mouse Mcm2 protein. J. Biol. Chem. 276, 42744-42752. https://doi.org/10.1074/jbc.M106861200
  20. Holding, D. R. and Springer, P. S. (2002) The Arabidopsis gene PROLIFERA is required for proper cytokinesis during seed development. Planta 214, 373-382. https://doi.org/10.1007/s00425-001-0686-0
  21. Bastida, M. and Puigdomenech, P. (2002) Specific expression of ZmPRL, the maize homolog of MCM7, during early embryogenesis. Plant Sci. 162, 97-106. https://doi.org/10.1016/S0168-9452(01)00537-4
  22. Sabelli, P. A., Parker, J. and Barlow, P. (1999) cDNA and promoter sequences for MCM3 homologues from maize, and protein localization in cycling cells. J. Exp. Bot. 50, 1315-1322. https://doi.org/10.1093/jexbot/50.337.1315
  23. Stevens, R., Mariconti, L., Rossignol, P., Perennes, C., Cella, R. and Bergounioux, C. (2002) Two E2F sites in the Arabidopsis MCM3 promoter have different roles in cell cycle activation and meristematic expression. J. Biol. Chem. 277, 32978-32984. https://doi.org/10.1074/jbc.M205125200
  24. Postma-Haarsma, A. D., Verwoert, I. I., Stronk, O. P., Koster, J., Lamers, G. E., Hoge, J. H. and Meijer, A. H. (1999) Characterization of the KNOX class homeobox genes Oskn2 and Oskn3 identified in a collection of cDNA libraries covering the early stages of rice embryogenesis. Plant Mol. Biol. 39, 257-271. https://doi.org/10.1023/A:1006153506868
  25. Forsburg, S. L. and Nurse, P. (1994) The fission yeast cdc19+ gene encodes a member of the MCM family of replication proteins. J. Cell Sci. 107, 2779-2788.
  26. Fowler, M. R., Eyre, S., Scott, N. W., Slater, A. and Elliott, M. C. (1998) The plant cell cycle in context. Mol. Biotechnol. 10, 123-153. https://doi.org/10.1007/BF02760861
  27. Menges, M., Samland, A. K., Planchais, S. and Murray, J. A. (2006) The D-type cyclin CYCD3;1 is limiting for the G1-to-S-phase transition in Arabidopsis. Plant Cell 18, 893-906. https://doi.org/10.1105/tpc.105.039636
  28. Hartig, K. and Beck, E. (2006) Crosstalk between auxin, cytokinins, and sugars in the plant cell cycle. Plant Biol. 8, 389-396. https://doi.org/10.1055/s-2006-923797
  29. Riou-Khamlichi, C., Menges, M., Healy, J. M. and Murray, J. A. (2000) Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Mol. Cell Biol. 20, 513-521.
  30. Chamovitz, D. A. and Segal, D. (2001) JAB1/CSN5 and the COP9 signalosome. A complex situation. EMBO Rep. 2, 96-101. https://doi.org/10.1093/embo-reports/kve028
  31. Yamamoto, T., Kimura, S., Mori, Y., Uchiyama, Y., Ishibashi, T., Hashimoto, J. and Sakaguchi, K. (2003) Interaction between proliferating cell nuclear antigen and JUN-activation-domain-binding protein 1 in the meristem of rice, Oryza sativa L. Planta 217, 175-183
  32. Tomoda, K., Kubota, Y. and Kato, J. (1999) Degradation of the cyclin-dependent-kinase inhibitor p27Kip1 is instigated by Jab1. Nature 398, 160-165. https://doi.org/10.1038/18230
  33. Rosel, D. and Kimmel, A. R. (2006) The COP9 signalosome regulates cell proliferation of Dictyostelium discoideum. Eur. J. Cell Biol. 85, 1023-1034. https://doi.org/10.1016/j.ejcb.2006.04.006
  34. Pawlowski, K., Kunze, R., de Vries, S. and Bisseling, T. (1994) Isolation of total, Poly(A) and polysomal RNA from plant tissues; in Plant Molecular Biology Manual, 2nd ed., Gelvin, S. B. and Schilperoof, R. A. (eds), pp. D5: 1-13. Kluwer Academic Publishers, Dordrecht, Holland
  35. Martinez-Garcia, J. F., Monte, E. and Quail, P. H. (1999) A simple, rapid and quantitative method for preparing Arabidopsis protein extracts for immunoblot analysis. Plant J. 20, 251-257. https://doi.org/10.1046/j.1365-313x.1999.00579.x
  36. Choi, S. B., Kim, K. H., Kavakli, I. H., Lee, S. K. and Okita, T. W. (2001) Transcriptional expression characteristics and subcellular localization of ADP-glucose pyrophosphorylase in the oil plant Perilla frutescens. Plant Cell Physiol. 42, 146-153. https://doi.org/10.1093/pcp/pce019
  37. Forsburg, S. L. and Sherman, D. A. (1997) General purpose tagging vectors for fission yeast. Gene 191, 191-195. https://doi.org/10.1016/S0378-1119(97)00058-9
  38. Gietz, R. D., Schiestl, R. H., Willems, A. R. and Woods, R. A. (1995) Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11, 355- 360. https://doi.org/10.1002/yea.320110408
  39. Moreno, S., Klar, A. and Nurse, P. (1991) Molecular genetic analysis of the fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823. https://doi.org/10.1016/0076-6879(91)94059-L

Cited by

  1. Transcriptomes of isolatedOryza sativagametes characterized by deep sequencing: evidence for distinct sex-dependent chromatin and epigenetic states before fertilization vol.76, pp.5, 2013, https://doi.org/10.1111/tpj.12336
  2. The ArabidopsisMCM2gene is essential to embryo development and its over-expression alters root meristem function vol.184, pp.2, 2009, https://doi.org/10.1111/j.1469-8137.2009.02961.x
  3. Plant MCM proteins: role in DNA replication and beyond vol.77, pp.6, 2011, https://doi.org/10.1007/s11103-011-9836-3
  4. Arabidopsis MCM2 is responsible for reduction in cell division induced by loss of function of the alpha subunit of GTP-binding protein vol.37, pp.11, 2015, https://doi.org/10.1007/s11738-015-1976-7
  5. Arabidopsis thaliana MCM2 plays role(s) in mungbean yellow mosaic India virus (MYMIV) DNA replication vol.158, pp.5, 2013, https://doi.org/10.1007/s00705-012-1563-9
  6. The plant cell cycle: Pre-Replication complex formation and controls vol.40, pp.1 suppl 1, 2017, https://doi.org/10.1590/1678-4685-gmb-2016-0118
  7. Co-infection of Sweet Orange with Severe and Mild Strains of Citrus tristeza virus Is Overwhelmingly Dominated by the Severe Strain on Both the Transcriptional and Biological Levels vol.8, 2017, https://doi.org/10.3389/fpls.2017.01419
  8. Knockdown of ZNF403 inhibits cell proliferation and induces G2/M arrest by modulating cell-cycle mediators vol.365, pp.1-2, 2012, https://doi.org/10.1007/s11010-012-1262-6