Response of the Green Alga Chlamydomonas reinhardtii to the DNA Damaging Agent Zeocin

. 2019 Jul 17 ; 8 (7) : . [epub] 20190717

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31319624

DNA damage is a ubiquitous threat endangering DNA integrity in all living organisms. Responses to DNA damage include, among others, induction of DNA repair and blocking of cell cycle progression in order to prevent transmission of damaged DNA to daughter cells. Here, we tested the effect of the antibiotic zeocin, inducing double stranded DNA breaks, on the cell cycle of synchronized cultures of the green alga Chlamydomonas reinhardtii. After zeocin application, DNA replication partially occurred but nuclear and cellular divisions were completely blocked. Application of zeocin combined with caffeine, known to alleviate DNA checkpoints, decreased cell viability significantly. This was probably caused by a partial overcoming of the cell cycle progression block in such cells, leading to aberrant cell divisions. The cell cycle block was accompanied by high steady state levels of mitotic cyclin-dependent kinase activity. The data indicate that DNA damage response in C. reinhardtii is connected to the cell cycle block, accompanied by increased and stabilized mitotic cyclin-dependent kinase activity.

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Kastan M.B., Bartek J. Cell-cycle checkpoints and cancer. Nature. 2004;432:316–323. doi: 10.1038/nature03097. PubMed DOI

Harper J.W., Elledge S.J. The DNA damage response: Ten years after. Mol. Cell. 2007;28:739–745. doi: 10.1016/j.molcel.2007.11.015. PubMed DOI

Yoshiyama K.O., Sakaguchi K., Kimura S. DNA damage response in plants: Conserved and variable response compared to animals. Biology. 2013;2:1338–1356. doi: 10.3390/biology2041338. PubMed DOI PMC

Recolin B., van der Laan S., Tsanov N., Maiorano D. Molecular mechanisms of DNA replication checkpoint activation. Genes. 2014;5:147–175. doi: 10.3390/genes5010147. PubMed DOI PMC

Zhou B.-B.S., Elledge S.J. The DNA damage response: Putting checkpoints in perspective. Nature. 2000;408:433–439. doi: 10.1038/35044005. PubMed DOI

Culligan K.M., Robertson C.E., Foreman J., Doerner P., Britt A.B. ATR and ATM play both distinct and additive roles in response to ionizing radiation. Plant J. 2006;48:947–961. doi: 10.1111/j.1365-313X.2006.02931.x. PubMed DOI

Bartek J., Lukas C., Lukas J. Checking on DNA damage in S phase. Nat. Rev. Mol. Cell Biol. 2004;5:792–804. doi: 10.1038/nrm1493. PubMed DOI

Kastan M.B., Lim D.-S. The many substrates and functions of ATM. Nat. Rev. Mol. Cell Biol. 2000;1:179–186. doi: 10.1038/35043058. PubMed DOI

Yoshiyama K.O., Kimura S., Maki H., Britt A.B., Umeda M. The role of SOG1, a plant-specific transcriptional regulator, in the DNA damage response. Plant Signal. Behav. 2014;9:e28889. doi: 10.4161/psb.28889. PubMed DOI PMC

Yoshiyama K.O., Kobayashi J., Ogita N., Ueda M., Kimura S., Maki H., Umeda M. ATM-mediated phosphorylation of SOG1 is essential for the DNA damage response in Arabidopsis. EMBO Rep. 2013;14:817–822. doi: 10.1038/embor.2013.112. PubMed DOI PMC

Ogita N., Okushima Y., Tokizawa M., Yamamoto Y.Y., Tanaka M., Seki M., Makita Y., Matsui M., Yoshiyama K.O., Sakamoto T., et al. Identifying the target genes of SUPPRESSOR OF GAMMA RESPONSE 1, a master transcription factor controlling DNA damage response in Arabidopsis. Plant J. 2018;94:439–453. doi: 10.1111/tpj.13866. PubMed DOI

Bourbousse C., Vegesna N., Law J.A. SOG1 activator and MYB3R repressors regulate a complex DNA damage network in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2018;115:E12453–E12462. doi: 10.1073/pnas.1810582115. PubMed DOI PMC

Cools T., De Veylder L. DNA stress checkpoint control and plant development. Curr. Opin. Plant Biol. 2009;12:23–28. doi: 10.1016/j.pbi.2008.09.012. PubMed DOI

Yi D., Kamei C.L.A., Cools T., Vanderauwera S., Takahashi N., Okushima Y., Eekhout T., Yoshiyama K.O., Larkin J., Van den Daele H., et al. The Arabidopsis SIAMESE-RELATED cyclin-dependent kinase inhibitors SMR5 and SMR7 regulate the DNA damage checkpoint in response to reactive oxygen species. Plant Cell. 2014;26:296–309. doi: 10.1105/tpc.113.118943. PubMed DOI PMC

Nisa M.-U., Huang Y., Benhamed M., Raynaud C. The plant DNA damage response: Signaling pathways leading to growth inhibition and putative role in response to stress conditions. Front. Plant Sci. 2019;10:653. doi: 10.3389/fpls.2019.00653. PubMed DOI PMC

Adachi S., Minamisawa K., Okushima Y., Inagaki S., Yoshiyama K., Kondou Y., Kaminuma E., Kawashima M., Toyoda T., Matsui M., et al. Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2011;108:10004–10009. doi: 10.1073/pnas.1103584108. PubMed DOI PMC

Takahashi N., Ogita N., Takahashi T., Taniguchi S., Tanaka M., Seki M., Umeda M. A regulatory module controlling stress-induced cell cycle arrest in Arabidopsis. Elife. 2019;8:e43944. doi: 10.7554/eLife.43944. PubMed DOI PMC

Chen P., Takatsuka H., Takahashi N., Kurata R., Fukao Y., Kobayashi K., Ito M., Umeda M. Arabidopsis R1R2R3-Myb proteins are essential for inhibiting cell division in response to DNA damage. Nat. Commun. 2017;8:635. doi: 10.1038/s41467-017-00676-4. PubMed DOI PMC

Coleman A.W. The nuclear-cell cycle in Chlamydomonas (Chlorophyceae) J. Phycol. 1982;18:192–195. doi: 10.1111/j.1529-8817.1982.tb03172.x. DOI

Craigie R.A., Cavalier-Smith T. Cell volume and the control of the Chlamydomonas cell cycle. J. Cell Sci. 1982;54:173–191.

Lien T., Knutsen G. Synchronized cultures of a cell wall-less mutant of Chlamydomonas reinhardii. Arch. Microbiol. 1976;108:189–194. doi: 10.1007/BF00428950. PubMed DOI

Donnan L., John P.C.L. CeII cycle control by timer and sizer in Chlamydomonas. Nature. 1983;304:630–633. doi: 10.1038/304630a0. PubMed DOI

Lien T., Knutsen G. Synchronous growth of Chlamydomonas reinhardtii (Chlorophyceae): A review of optimal conditions. J. Phycol. 1979;15:191–200. doi: 10.1111/j.0022-3646.1979.00191.x. DOI

Donnan L., John P.C.L. Timer and sizer controls in the cell cycles of Chlamydomonas and Chlorella. In: Nurse P., Streiblová E., editors. The Microbial Cell Cycle. CRC Press; Boca Raton, FL, USA: 1984. pp. 231–251.

Spudich J.L., Sager R. Regulation of the Chlamydomonas cell cycle by light and dark. J. Cell Biol. 1980;85:136–145. doi: 10.1083/jcb.85.1.136. PubMed DOI PMC

Umen J.G., Goodenough U.W. Control of cell division by a retinoblastoma protein homolog in Chlamydomonas. Genes Dev. 2001;15:1652–1661. doi: 10.1101/gad.892101. PubMed DOI PMC

John P.C.L. Control of the cell division cycle in Chlamydomonas. Microbiol. Sci. 1984;1:96–101. PubMed

John P.C.L. Control points in the Chlamydomonas cell cycle. In: Wiesnar W., Robinson D.G., Starr R.C., editors. Algal Development. Springer; Berlin/Heidelberg, Germany: New York, NY, USA: London, UK: Paris, France: Tokyo, Japan: 1987. pp. 9–16.

Bisova K., Krylov D.M., Umen J.G. Genome-wide annotation and expression profiling of cell cycle regulatory genes in Chlamydomonas reinhardtii. Plant Physiol. 2005;137:1–17. doi: 10.1104/pp.104.054155. PubMed DOI PMC

Sueoka N. Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA. 1960;46:83–91. doi: 10.1073/pnas.46.1.83. PubMed DOI PMC

Zachleder V., Šetlík I. Effect of irradiance on the course of RNA synthesis in the cell cycle of Scenedesmus quadricauda. Biol. Plant. 1982;24:341–353. doi: 10.1007/BF02909100. DOI

Hlavová M., Viítová M., Bišová K. Synchronization of green algae by light and dark regimes for cell cycle and cell division studies. Methods Mol. Biol. 2016;1370:3–16. PubMed

Wanka F. Die Bestimmung der Nucleinsäuren in Chlorella pyrenoidosa. Planta. 1962;58:594–619. doi: 10.1007/BF01914751. DOI

Lukavský J., Tetík K., Vendlová J. Extraction of nucleic acid from the alga Scenedesmus quadricauda. Algol. Stud. 1973;9:416–426.

Decallonne J.R., Weyns C.J. A shortened procedure of the diphenylamine reaction for measurement of deoxyribonucleic acid by using light activation. Anal. Biochem. 1976;74:448–456. doi: 10.1016/0003-2697(76)90225-6. PubMed DOI

Zachleder V. Optimization of nucleic acids assay in green and blue-green algae: Extraction procedures and the light-activated reaction for DNA. Algol. Stud. 1984;36:313–328. doi: 10.1127/algol_stud/67/1984/313. DOI

Zachleder V. Regulation of growth processes during the cell cycle of the chlorococcal alga Scenedesmus quadricauda under a DNA replication block. J. Phycol. 1995;30:941–947. doi: 10.1111/j.0022-3646.1995.00941.x. DOI

Langan T.A., Gautier J., Lohka M., Hollingsworth R., Moreno S., Nurse P., Maller J., Sclafani R.A. Mammalian growth-associated H1 histone kinase: A homologue of cdc2+/CDC28 protein kinases controlling mitotic entry in yeast and frog cells. Mol. Cell. Biol. 1989;9:3860–3868. doi: 10.1128/MCB.9.9.3860. PubMed DOI PMC

Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–685. doi: 10.1038/227680a0. PubMed DOI

Zachleder V., Ivanov I., Vítová M., Bišová K. Effects of cyclin-dependent kinase activity on the coordination of growth and the cell cycle in green algae at different temperatures. J. Exp. Bot. 2019;70:845–858. doi: 10.1093/jxb/ery391. PubMed DOI

Gatignol A., Durand H., Tiraby G. Bleomycin resistance conferred by a drug-binding protein. FEBS Lett. 1988;230:171–175. doi: 10.1016/0014-5793(88)80665-3. PubMed DOI

Ehrenfeld G.M., Shipley J.B., Heimbrook D.C., Sugiyama H., Long E.C., van Boom J.H., van der Marel G.A., Oppenheimer N.J., Hecht S.M. Copper-dependent cleavage of DNA by bleomycin. Biochemistry. 1987;26:931–942. doi: 10.1021/bi00377a038. PubMed DOI

Kostrub C.F., al-Khodairy F., Ghazizadeh H., Carr A.M., Enoch T. Molecular analysis of hus1+, a fission yeast gene required for S/M and DNA damage checkpoints. Mol. Gen. Genet. 1997;254:389–399. doi: 10.1007/PL00008606. PubMed DOI

Lau C.C., Pardee A.B. Mechanism by which caffeine potentiates lethality of nitrogen-mustard. Proc. Natl. Acad. Sci. USA. 1982;79:2942–2946. doi: 10.1073/pnas.79.9.2942. PubMed DOI PMC

Moser B.A., Brondello J.M., Baber-Furnari B., Russell P. Mechanism of caffeine-induced checkpoint override in fission yeast. Mol. Cell. Biol. 2000;20:4288–4294. doi: 10.1128/MCB.20.12.4288-4294.2000. PubMed DOI PMC

Sarkaria J.N., Busby E.C., Tibbetts R.S., Roos P., Taya Y., Karnitz L.M., Abraham R.T. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res. 1999;59:4375–4382. PubMed

Zhou B.-B.S., Chaturvedi P., Spring K., Scott S.P., Johanson R.A., Mishra R., Mattern M.R., Winkler J.D., Khanna K.K. Caffeine abolishes the mammalian G2/M DNA damage checkpoint by inhibiting ataxia-telangiectasia-mutated kinase activity. J. Biol. Chem. 2000;275:10342–10348. doi: 10.1074/jbc.275.14.10342. PubMed DOI

Tulin F., Cross F.R. A microbial avenue to cell cycle control in the plant superkingdom. Plant Cell. 2014;26:4019–4038. doi: 10.1105/tpc.114.129312. PubMed DOI PMC

Slaninová M., Nagyová B., Gálová E., Hendrychová J., Bišová K., Zachleder V., Vlček D. The alga Chlamydomonas reinhardtii UVS11 gene is responsible for cell division delay and temporal decrease in histone H1 kinase activity caused by UV irradiation. DNA Repair. 2003;2:737–750. doi: 10.1016/S1568-7864(03)00047-8. PubMed DOI

Schlegel R., Pardee A.B. Caffeine-induced uncoupling of mitosis from the completion of DNA replication in mammalian cells. Science. 1986;232:1264–1266. doi: 10.1126/science.2422760. PubMed DOI

Amino S., Nagata T. Caffeine-induced uncoupling of mitosis from DNA replication in tobacco BY2-cells. J. Plant Res. 1996;109

Kumagai A., Yakowec P.S., Dunphy W.G. 14-3-3 proteins act as negative regulators of the inducer Cdc25 in Xenopus egg extracts. Mol. Biol. Cell. 1998;9:345–354. doi: 10.1091/mbc.9.2.345. PubMed DOI PMC

Kumagai A., Guo Z., Emami K.H., Wang S.X., Dunphy W.G. The Xenopus Chk1 protein kinase mediates a caffeine-sensitive pathway of checkpoint control in cell-free extracts. J. Cell Biol. 1998;142:1559–1569. doi: 10.1083/jcb.142.6.1559. PubMed DOI PMC

Dasso M., Newport J.W. Completion of DNA replication is monitored by a feedback system that controls the initiation of mitosis in vitro: Studies in Xenopus. Cell. 1990;61:811–823. doi: 10.1016/0092-8674(90)90191-G. PubMed DOI

Pelayo H., Lastres P., de la Torre C. Replication and G2 checkpoints: Their response to caffeine. Planta. 2001;212:444–453. doi: 10.1007/s004250000415. PubMed DOI

Weingartner M., Pelayo H.R., Binarova P., Zwerger K., Melikant B., de la Torre C., Heberle-Bors E., Bogre L. A plant cyclin B2 is degraded early in mitosis and its ectopic expression shortens G2-phase and alleviates the DNA-damage checkpoint. J. Cell Sci. 2003;116:487–498. doi: 10.1242/jcs.00250. PubMed DOI

Kumagai A., Dunphy W.G. Control of the Cdc2/cyclin-B complex in Xenopus egg extracts arrested at a G2/M checkpoint with DNA synthesis inhibitors. Mol. Biol. Cell. 1995;6:199–213. doi: 10.1091/mbc.6.2.199. PubMed DOI PMC

Poon R.Y.C., Chau M.S., Yamashita K., Hunter T. The role of Cdc2 feedback loop control in the DNA damage checkpoint in mammalian cells. Cancer Res. 1997;57:5168–5178. PubMed

Rosen H., Rehn M.M., Johnson B.A. The effect of caffeine on repair in Chlamydomonas reinhardtii: I. Enhancement of recombination repair. Mutat. Res. 1980;70:301–309. doi: 10.1016/0027-5107(80)90020-2. PubMed DOI

Vlcek D., Sevcovicova A., Sviezena B., Galova E., Miadokova E. Chlamydomonas reinhardtii: A convenient model system for the study of DNA repair in photoautotrophic eukaryotes. Curr. Genet. 2008;53:1–22. doi: 10.1007/s00294-007-0163-9. PubMed DOI

Hlavová M., Čížková M., Vítová M., Bišová K., Zachleder V. DNA damage during G2 phase does not affect cell cycle progression of the green alga Scenedesmus quadricauda. PLoS ONE. 2011;6:e19626. doi: 10.1371/journal.pone.0019626. PubMed DOI PMC

Jazayeri A., Falck J., Lukas C., Bartek J., Smith G.C., Lukas J., Jackson S.P. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 2006;8:37–45. doi: 10.1038/ncb1337. PubMed DOI

Alvarez-Fernandez M., Halim V.A., Krenning L., Aprelia M., Mohammed S., Heck A.J., Medema R.H. Recovery from a DNA-damage-induced G2 arrest requires Cdk-dependent activation of FoxM1. EMBO Rep. 2010;11:452–458. doi: 10.1038/embor.2010.46. PubMed DOI PMC

Ira G., Pellicioli A., Balijja A., Wang X., Fiorani S., Carotenuto W., Liberi G., Bressan D., Wan L., Hollingsworth N.M., et al. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature. 2004;431:1011–1017. doi: 10.1038/nature02964. PubMed DOI PMC

Biedermann S., Harashima H., Chen P., Heese M., Bouyer D., Sofroni K., Schnittger A. The retinoblastoma homolog RBR1 mediates localization of the repair protein RAD51 to DNA lesions in Arabidopsis. EMBO J. 2017;36:1279–1297. doi: 10.15252/embj.201694571. PubMed DOI PMC

Weimer A.K., Biedermann S., Harashima H., Roodbarkelari F., Takahashi N., Foreman J., Guan Y., Pochon G., Heese M., Van Damme D., et al. The plant-specific CDKB1-CYCB1 complex mediates homologous recombination repair in Arabidopsis. EMBO J. 2016;35:2068–2086. doi: 10.15252/embj.201593083. PubMed DOI PMC

Atkins K.C., Cross F. Inter-regulation of CDKA/CDK1 and the plant-specific cyclin-dependent kinase CDKB in control of the Chlamydomonas cell cycle. Plant Cell. 2018;30:429–446. doi: 10.1105/tpc.17.00759. PubMed DOI PMC

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