Control of pre-replicative complex during the division cycle in Chlamydomonas reinhardtii


Autoři: Amy E. Ikui aff001;  Noriko Ueki aff001;  Kresti Pecani aff002;  Frederick R. Cross aff002
Působiště autorů: Department of Biology, Brooklyn College, The City University of New York, New York City, New York, United States of America aff001;  Laboratory of Cell Cycle Genetics, The Rockefeller University, New York City, New York, United States of America aff002
Vyšlo v časopise: Control of pre-replicative complex during the division cycle in Chlamydomonas reinhardtii. PLoS Genet 17(4): e1009471. doi:10.1371/journal.pgen.1009471
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009471

Souhrn

DNA replication is fundamental to all living organisms. In yeast and animals, it is triggered by an assembly of pre-replicative complex including ORC, CDC6 and MCMs. Cyclin Dependent Kinase (CDK) regulates both assembly and firing of the pre-replicative complex. We tested temperature-sensitive mutants blocking Chlamydomonas DNA replication. The mutants were partially or completely defective in DNA replication and did not produce mitotic spindles. After a long G1, wild type Chlamydomonas cells enter a division phase when it undergoes multiple rapid synchronous divisions (‘multiple fission’). Using tagged transgenic strains, we found that MCM4 and MCM6 were localized to the nucleus throughout the entire multiple fission division cycle, except for transient cytoplasmic localization during each mitosis. Chlamydomonas CDC6 was transiently localized in nucleus in early division cycles. CDC6 protein levels were very low, probably due to proteasomal degradation. CDC6 levels were severely reduced by inactivation of CDKA1 (CDK1 ortholog) but not the plant-specific CDKB1. Proteasome inhibition did not detectably increase CDC6 levels in the cdka1 mutant, suggesting that CDKA1 might upregulate CDC6 at the transcriptional level. All of the DNA replication proteins tested were essentially undetectable until late G1. They accumulated specifically during multiple fission and then were degraded as cells completed their terminal divisions. We speculate that loading of origins with the MCM helicase may not occur until the end of the long G1, unlike in the budding yeast system. We also developed a simple assay for salt-resistant chromatin binding of MCM4, and found that tight MCM4 loading was dependent on ORC1, CDC6 and MCM6, but not on RNR1 or CDKB1. These results provide a microbial framework for approaching replication control in the plant kingdom.

Klíčová slova:

Cell cycle and cell division – DNA replication – Chromatin – Mitosis – Phosphorylation – Proteolysis – Saccharomyces cerevisiae – Yeast


Zdroje

1. Morgan DO. Principles of CDK regulation. Nature. 1995;374(6518):131–4. Epub 1995/03/09. doi: 10.1038/374131a0 7877684.

2. Cross FR, Umen JG. The Chlamydomonas cell cycle. Plant J. 2015;82(3):370–92. Epub 2015/02/19. doi: 10.1111/tpj.12795 25690512; PubMed Central PMCID: PMC4409525.

3. Vandepoele K, Raes J, De Veylder L, Rouze P, Rombauts S, Inze D. Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell. 2002;14(4):903–16. Epub 2002/04/24. doi: 10.1105/tpc.010445 11971144; PubMed Central PMCID: PMC150691.

4. Cizkova M, Pichova A, Vitova M, Hlavova M, Hendrychova J, Umysova D, et al. CDKA and CDKB kinases from Chlamydomonas reinhardtii are able to complement cdc28 temperature-sensitive mutants of Saccharomyces cerevisiae. Protoplasma. 2008;232(3–4):183–91. Epub 2008/04/19. doi: 10.1007/s00709-008-0285-z 18421551.

5. Tulin F, Cross FR. Cyclin-Dependent Kinase Regulation of Diurnal Transcription in Chlamydomonas. Plant Cell. 2015;27(10):2727–42. Epub 2015/10/18. doi: 10.1105/tpc.15.00400 26475866; PubMed Central PMCID: PMC4682320.

6. Zones JM, Blaby IK, Merchant SS, Umen JG. High-Resolution Profiling of a Synchronized Diurnal Transcriptome from Chlamydomonas reinhardtii Reveals Continuous Cell and Metabolic Differentiation. Plant Cell. 2015;27(10):2743–69. Epub 2015/10/04. doi: 10.1105/tpc.15.00498 26432862; PubMed Central PMCID: PMC4682324.

7. Bell SP, Stillman B. ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature. 1992;357(6374):128–34. Epub 1992/05/14. doi: 10.1038/357128a0 1579162.

8. Liang C, Weinreich M, Stillman B. ORC and Cdc6p interact and determine the frequency of initiation of DNA replication in the genome. Cell. 1995;81(5):667–76. Epub 1995/06/02. doi: 10.1016/0092-8674(95)90528-6 7774008.

9. Cocker JH, Piatti S, Santocanale C, Nasmyth K, Diffley JF. An essential role for the Cdc6 protein in forming the pre-replicative complexes of budding yeast. Nature. 1996;379(6561):180–2. Epub 1996/01/11. doi: 10.1038/379180a0 8538771.

10. Chen S, de Vries MA, Bell SP. Orc6 is required for dynamic recruitment of Cdt1 during repeated Mcm2-7 loading. Genes Dev. 2007;21(22):2897–907. Epub 2007/11/17. doi: 10.1101/gad.1596807 18006685; PubMed Central PMCID: PMC2049192.

11. Tanaka S, Araki H. Helicase activation and establishment of replication forks at chromosomal origins of replication. Cold Spring Harb Perspect Biol. 2013;5(12):a010371. Epub 2013/07/25. doi: 10.1101/cshperspect.a010371 23881938; PubMed Central PMCID: PMC3839609.

12. Remus D, Beuron F, Tolun G, Griffith JD, Morris EP, Diffley JF. Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell. 2009;139(4):719–30. Epub 2009/11/10. doi: 10.1016/j.cell.2009.10.015 19896182; PubMed Central PMCID: PMC2804858.

13. Diffley JF. Once and only once upon a time: specifying and regulating origins of DNA replication in eukaryotic cells. Genes Dev. 1996;10(22):2819–30. Epub 1996/11/15. doi: 10.1101/gad.10.22.2819 8918884.

14. Drury LS, Perkins G, Diffley JF. The cyclin-dependent kinase Cdc28p regulates distinct modes of Cdc6p proteolysis during the budding yeast cell cycle. Curr Biol. 2000;10(5):231–40. Epub 2000/03/14. doi: 10.1016/s0960-9822(00)00355-9 10712901.

15. Drury LS, Perkins G, Diffley JF. The Cdc4/34/53 pathway targets Cdc6p for proteolysis in budding yeast. EMBO J. 1997;16(19):5966–76. Epub 1997/10/06. doi: 10.1093/emboj/16.19.5966 9312054; PubMed Central PMCID: PMC1170227.

16. Perkins G, Drury LS, Diffley JF. Separate SCF(CDC4) recognition elements target Cdc6 for proteolysis in S phase and mitosis. EMBO J. 2001;20(17):4836–45. Epub 2001/09/05. doi: 10.1093/emboj/20.17.4836 11532947; PubMed Central PMCID: PMC125267.

17. Elsasser S, Lou F, Wang B, Campbell JL, Jong A. Interaction between yeast Cdc6 protein and B-type cyclin/Cdc28 kinases. Mol Biol Cell. 1996;7(11):1723–35. Epub 1996/11/01. doi: 10.1091/mbc.7.11.1723 8930895; PubMed Central PMCID: PMC276021.

18. Liku ME, Nguyen VQ, Rosales AW, Irie K, Li JJ. CDK phosphorylation of a novel NLS-NES module distributed between two subunits of the Mcm2-7 complex prevents chromosomal rereplication. Mol Biol Cell. 2005;16(10):5026–39. Epub 2005/08/12. doi: 10.1091/mbc.e05-05-0412 16093348; PubMed Central PMCID: PMC1237101.

19. DePamphilis ML. Cell cycle dependent regulation of the origin recognition complex. Cell Cycle. 2005;4(1):70–9. Epub 2004/12/22. doi: 10.4161/cc.4.1.1333 15611627.

20. Fujita M, Yamada C, Tsurumi T, Hanaoka F, Matsuzawa K, Inagaki M. Cell cycle- and chromatin binding state-dependent phosphorylation of human MCM heterohexameric complexes. A role for cdc2 kinase. J Biol Chem. 1998;273(27):17095–101. Epub 1998/06/27. doi: 10.1074/jbc.273.27.17095 9642275.

21. Moritani M, Ishimi Y. Inhibition of DNA binding of MCM2-7 complex by phosphorylation with cyclin-dependent kinases. J Biochem. 2013;154(4):363–72. Epub 2013/07/19. doi: 10.1093/jb/mvt062 23864661.

22. Fujita M, Yamada C, Goto H, Yokoyama N, Kuzushima K, Inagaki M, et al. Cell cycle regulation of human CDC6 protein. Intracellular localization, interaction with the human mcm complex, and CDC2 kinase-mediated hyperphosphorylation. J Biol Chem. 1999;274(36):25927–32. Epub 1999/08/28. doi: 10.1074/jbc.274.36.25927 10464337.

23. Walter D, Hoffmann S, Komseli ES, Rappsilber J, Gorgoulis V, Sorensen CS. SCF(Cyclin F)-dependent degradation of CDC6 suppresses DNA re-replication. Nat Commun. 2016;7:10530. Epub 2016/01/29. doi: 10.1038/ncomms10530 26818844; PubMed Central PMCID: PMC4738361.

24. Mailand N, Diffley JF. CDKs promote DNA replication origin licensing in human cells by protecting Cdc6 from APC/C-dependent proteolysis. Cell. 2005;122(6):915–26. Epub 2005/09/13. doi: 10.1016/j.cell.2005.08.013 16153703.

25. Duursma AM, Agami R. CDK-dependent stabilization of Cdc6: linking growth and stress signals to activation of DNA replication. Cell Cycle. 2005;4(12):1725–8. Epub 2005/11/01. doi: 10.4161/cc.4.12.2193 16258286.

26. Masuda HP, Ramos GB, de Almeida-Engler J, Cabral LM, Coqueiro VM, Macrini CM, et al. Genome based identification and analysis of the pre-replicative complex of Arabidopsis thaliana. FEBS Lett. 2004;574(1–3):192–202. Epub 2004/09/11. doi: 10.1016/j.febslet.2004.07.088 15358564.

27. de Jager SM, Menges M, Bauer UM, Murra JA. Arabidopsis E2F1 binds a sequence present in the promoter of S-phase-regulated gene AtCDC6 and is a member of a multigene family with differential activities. Plant Mol Biol. 2001;47(4):555–68. Epub 2001/10/24. doi: 10.1023/a:1011848528377 11669580.

28. Domenichini S, Benhamed M, De Jaeger G, Van De Slijke E, Blanchet S, Bourge M, et al. Evidence for a role of Arabidopsis CDT1 proteins in gametophyte development and maintenance of genome integrity. Plant Cell. 2012;24(7):2779–91. Epub 2012/07/10. doi: 10.1105/tpc.112.100156 22773747; PubMed Central PMCID: PMC3426114.

29. Castellano MM, del Pozo JC, Ramirez-Parra E, Brown S, Gutierrez C. Expression and stability of Arabidopsis CDC6 are associated with endoreplication. Plant Cell. 2001;13(12):2671–86. Epub 2001/12/26. doi: 10.1105/tpc.010329 11752380; PubMed Central PMCID: PMC139481.

30. Shultz RW, Lee TJ, Allen GC, Thompson WF, Hanley-Bowdoin L. Dynamic localization of the DNA replication proteins MCM5 and MCM7 in plants. Plant Physiol. 2009;150(2):658–69. Epub 2009/04/10. doi: 10.1104/pp.109.136614 19357199; PubMed Central PMCID: PMC2689970.

31. Honey S, Futcher B. Roles of the CDK phosphorylation sites of yeast Cdc6 in chromatin binding and rereplication. Mol Biol Cell. 2007;18(4):1324–36. Epub 2007/02/03. doi: 10.1091/mbc.e06-06-0544 17267692; PubMed Central PMCID: PMC1838967.

32. Springer PS, Holding DR, Groover A, Yordan C, Martienssen RA. 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. 2000;127(9):1815–22. Epub 2000/04/06. 10751170.

33. Dresselhaus T, Srilunchang KO, Leljak-Levanic D, Schreiber DN, Garg P. The fertilization-induced DNA replication factor MCM6 of maize shuttles between cytoplasm and nucleus, and is essential for plant growth and development. Plant Physiol. 2006;140(2):512–27. Epub 2006/01/13. doi: 10.1104/pp.105.074294 16407440; PubMed Central PMCID: PMC1361320.

34. Tuteja N, Tran NQ, Dang HQ, Tuteja R. Plant MCM proteins: role in DNA replication and beyond. Plant Mol Biol. 2011;77(6):537–45. Epub 2011/11/01. doi: 10.1007/s11103-011-9836-3 22038093.

35. Tulin F, Cross FR. A microbial avenue to cell cycle control in the plant superkingdom. Plant Cell. 2014;26(10):4019–38. Epub 2014/10/23. doi: 10.1105/tpc.114.129312 25336509; PubMed Central PMCID: PMC4247570.

36. Breker M, Lieberman K, Cross FR. Comprehensive Discovery of Cell-Cycle-Essential Pathways in Chlamydomonas reinhardtii. Plant Cell. 2018;30(6):1178–98. Epub 2018/05/11. doi: 10.1105/tpc.18.00071 29743196; PubMed Central PMCID: PMC6048789.

37. Kamimura Y, Tanaka H, Kobayashi Y, Shikanai T, Nishimura Y. Chloroplast nucleoids as a transformable network revealed by live imaging with a microfluidic device. Commun Biol. 2018;1:47. Epub 2018/10/03. doi: 10.1038/s42003-018-0055-1 30271930; PubMed Central PMCID: PMC6123815.

38. Hartwell LH, Weinert TA. Checkpoints: controls that ensure the order of cell cycle events. Science. 1989;246(4930):629–34. Epub 1989/11/03. doi: 10.1126/science.2683079 2683079.

39. Van Leene J, Hollunder J, Eeckhout D, Persiau G, Van De Slijke E, Stals H, et al. Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol Syst Biol. 2010;6:397. Epub 2010/08/14. doi: 10.1038/msb.2010.53 20706207; PubMed Central PMCID: PMC2950081.

40. Atkins KC, Cross FR. Interregulation of CDKA/CDK1 and the Plant-Specific Cyclin-Dependent Kinase CDKB in Control of the Chlamydomonas Cell Cycle. Plant Cell. 2018;30(2):429–46. Epub 2018/01/26. doi: 10.1105/tpc.17.00759 29367304; PubMed Central PMCID: PMC5868683.

41. King RW, Peters JM, Tugendreich S, Rolfe M, Hieter P, Kirschner MW. A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell. 1995;81(2):279–88. Epub 1995/04/21. doi: 10.1016/0092-8674(95)90338-0 7736580.

42. Nguyen VQ, Co C, Li JJ. Cyclin-dependent kinases prevent DNA re-replication through multiple mechanisms. Nature. 2001;411(6841):1068–73. Epub 2001/06/29. doi: 10.1038/35082600 11429609.

43. Nguyen VQ, Co C, Irie K, Li JJ. Clb/Cdc28 kinases promote nuclear export of the replication initiator proteins Mcm2-7. Curr Biol. 2000;10(4):195–205. Epub 2000/03/08. doi: 10.1016/s0960-9822(00)00337-7 10704410.

44. Di Talia S, Skotheim JM, Bean JM, Siggia ED, Cross FR. The effects of molecular noise and size control on variability in the budding yeast cell cycle. Nature. 2007;448(7156):947–51. Epub 2007/08/24. doi: 10.1038/nature06072 17713537.

45. Charvin G, Cross FR, Siggia ED. A microfluidic device for temporally controlled gene expression and long-term fluorescent imaging in unperturbed dividing yeast cells. PLoS One. 2008;3(1):e1468. Epub 2008/01/24. doi: 10.1371/journal.pone.0001468 18213377; PubMed Central PMCID: PMC2194624.

46. Fuhrmann M, Oertel W, Hegemann P. A synthetic gene coding for the green fluorescent protein (GFP) is a versatile reporter in Chlamydomonas reinhardtii. Plant J. 1999;19(3):353–61. Epub 1999/09/04. doi: 10.1046/j.1365-313x.1999.00526.x 10476082.

47. Calzada A, Sanchez M, Sanchez E, Bueno A. The stability of the Cdc6 protein is regulated by cyclin-dependent kinase/cyclin B complexes in Saccharomyces cerevisiae. J Biol Chem. 2000;275(13):9734–41. Epub 2000/03/29. doi: 10.1074/jbc.275.13.9734 10734126.

48. Sanchez M, Calzada A, Bueno A. The Cdc6 protein is ubiquitinated in vivo for proteolysis in Saccharomyces cerevisiae. J Biol Chem. 1999;274(13):9092–7. Epub 1999/03/20. doi: 10.1074/jbc.274.13.9092 10085159.

49. Elsasser S, Chi Y, Yang P, Campbell JL. Phosphorylation controls timing of Cdc6p destruction: A biochemical analysis. Mol Biol Cell. 1999;10(10):3263–77. Epub 1999/10/08. doi: 10.1091/mbc.10.10.3263 10512865; PubMed Central PMCID: PMC25589.

50. Bell SP, Dutta A. DNA replication in eukaryotic cells. Annu Rev Biochem. 2002;71:333–74. Epub 2002/06/05. doi: 10.1146/annurev.biochem.71.110601.135425 12045100.

51. Frigola J, Remus D, Mehanna A, Diffley JF. ATPase-dependent quality control of DNA replication origin licensing. Nature. 2013;495(7441):339–43. Epub 2013/03/12. doi: 10.1038/nature11920 23474987; PubMed Central PMCID: PMC4825857.

52. Adam SA, Marr RS, Gerace L. Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J Cell Biol. 1990;111(3):807–16. Epub 1990/09/01. doi: 10.1083/jcb.111.3.807 2391365; PubMed Central PMCID: PMC2116268.

53. Culligan K, Tissier A, Britt A. ATR regulates a G2-phase cell-cycle checkpoint in Arabidopsis thaliana. Plant Cell. 2004;16(5):1091–104. Epub 2004/04/13. doi: 10.1105/tpc.018903 15075397; PubMed Central PMCID: PMC423202.

54. Sazer S, Lynch M, Needleman D. Deciphering the evolutionary history of open and closed mitosis. Curr Biol. 2014;24(22):R1099–103. Epub 2014/12/03. doi: 10.1016/j.cub.2014.10.011 25458223; PubMed Central PMCID: PMC4278198.

55. Aoki K, Hayashi H, Furuya K, Sato M, Takagi T, Osumi M, et al. Breakage of the nuclear envelope by an extending mitotic nucleus occurs during anaphase in Schizosaccharomyces japonicus. Genes Cells. 2011;16(9):911–26. Epub 2011/07/08. doi: 10.1111/j.1365-2443.2011.01540.x 21733045.

56. Straube A, Weber I, Steinberg G. A novel mechanism of nuclear envelope break-down in a fungus: nuclear migration strips off the envelope. EMBO J. 2005;24(9):1674–85. Epub 2005/04/30. doi: 10.1038/sj.emboj.7600644 15861140; PubMed Central PMCID: PMC1142577.

57. De Souza CP, Osmani AH, Hashmi SB, Osmani SA. Partial nuclear pore complex disassembly during closed mitosis in Aspergillus nidulans. Curr Biol. 2004;14(22):1973–84. Epub 2004/11/24. doi: 10.1016/j.cub.2004.10.050 15556859.

58. De Souza CP, Osmani SA. Mitosis, not just open or closed. Eukaryot Cell. 2007;6(9):1521–7. Epub 2007/07/31. doi: 10.1128/EC.00178-07 17660363; PubMed Central PMCID: PMC2043359.

59. Johnson UG, Porter KR. Fine structure of cell division in Chlamydomonas reinhardi. Basal bodies and microtubules. J Cell Biol. 1968;38(2):403–25. Epub 1968/08/01. doi: 10.1083/jcb.38.2.403 5664210; PubMed Central PMCID: PMC2107492.

60. Blow JJ, Laskey RA. A role for the nuclear envelope in controlling DNA replication within the cell cycle. Nature. 1988;332(6164):546–8. Epub 1988/04/07. doi: 10.1038/332546a0 3357511.

61. Ikui AE, Archambault V, Drapkin BJ, Campbell V, Cross FR. Cyclin and cyclin-dependent kinase substrate requirements for preventing rereplication reveal the need for concomitant activation and inhibition. Genetics. 2007;175(3):1011–22. Epub 2006/12/30. doi: 10.1534/genetics.106.068213 17194775; PubMed Central PMCID: PMC1840059.

62. Dutcher SK. Mating and tetrad analysis in Chlamydomonas reinhardtii. Methods Cell Biol. 1995;47:531–40. Epub 1995/01/01. doi: 10.1016/s0091-679x(08)60857-2 7476541.


Článek vyšel v časopise

PLOS Genetics


2021 Číslo 4
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Hypertenze a hypercholesterolémie – synergický efekt léčby
nový kurz
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

Úloha kombinovaných preparátů v léčbě arteriální hypertenze
Autoři: prof. MUDr. Martin Haluzík, DrSc.

Halitóza
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Terapie roztroušené sklerózy v kostce
Autoři: MUDr. Dominika Šťastná, Ph.D.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se