Strengths and Weaknesses of Cell Synchronization Protocols Based on Inhibition of DNA Synthesis

. 2021 Oct 05 ; 22 (19) : . [epub] 20211005

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid34639098

Grantová podpora
TN01000013 Technology Agency of the Czech Republic
project EATRIS-CZ, grant number LM2015064 Ministry of Education Youth and Sports
project ENOCH, grant number CZ.02.1.01/0.0/0.0/16_019/0000868 European Regional Development Fund

Synchronous cell populations are commonly used for the analysis of various aspects of cellular metabolism at specific stages of the cell cycle. Cell synchronization at a chosen cell cycle stage is most frequently achieved by inhibition of specific metabolic pathway(s). In this respect, various protocols have been developed to synchronize cells in particular cell cycle stages. In this review, we provide an overview of the protocols for cell synchronization of mammalian cells based on the inhibition of synthesis of DNA building blocks-deoxynucleotides and/or inhibition of DNA synthesis. The mechanism of action, examples of their use, and advantages and disadvantages are described with the aim of providing a guide for the selection of suitable protocol for different studied situations.

Zobrazit více v PubMed

Cooper G.M. The Cell: A Molecular Approach. 2nd ed. Sinauer Associates; Sunderland, MA, USA: 2000. The Eukaryotic Cell Cycle.

Alberts B., Johnson A., Lewis J., Raff M., Roberts K., Walter P. Molecular Biology of the Cell. 6th ed. Garland Science; New York, NY, USA: 2002. The Mechanics of Cell Division; pp. 1027–1062.

Malumbres M., Barbacid M. Cell Cycle, CDKs and Cancer: A Changing Paradigm. Nat. Rev. Cancer. 2009;9:153–166. doi: 10.1038/nrc2602. PubMed DOI

Bower J.J., Vance L.D., Psioda M., Smith-Roe S.L., Simpson D.A., Ibrahim J.G., Hoadley K.A., Perou C.M., Kaufmann W.K. Patterns of Cell Cycle Checkpoint Deregulation Associated with Intrinsic Molecular Subtypes of Human Breast Cancer Cells. NPJ Breast Cancer. 2017;3:9. doi: 10.1038/s41523-017-0009-7. PubMed DOI PMC

Pardee A.B. G1 Events and Regulation of Cell Proliferation. Science. 1989;246:603–608. doi: 10.1126/science.2683075. PubMed DOI

Harashima H., Dissmeyer N., Schnittger A. Cell Cycle Control Across the Eukaryotic Kingdom. Trends Cell Biol. 2013;23:345–356. doi: 10.1016/j.tcb.2013.03.002. PubMed DOI

Lane A.N., Fan T.W. Regulation of Mammalian Nucleotide Metabolism and Biosynthesis. Nucleic Acids Res. 2015;43:2466–2485. doi: 10.1093/nar/gkv047. PubMed DOI PMC

Reichard P. Ribonucleotide Reductases: The Evolution of Allosteric Regulation. Arch. Biochem. Biophys. 2002;397:149–155. doi: 10.1006/abbi.2001.2637. PubMed DOI

Jordan A., Reichard P. Ribonucleotide Reductases. Annu. Rev. Biochem. 1998;67:71–98. doi: 10.1146/annurev.biochem.67.1.71. PubMed DOI

Nordlund P., Reichard P. Ribonucleotide Reductases. Annu. Rev. Biochem. 2006;75:681–706. doi: 10.1146/annurev.biochem.75.103004.142443. PubMed DOI

DeGregori J., Kowalik T., Nevins J.R. Cellular Targets for Activation by the E2F1 Transcription Factor Include DNA Synthesis- and G1/S-Regulatory Genes. Mol. Cell. Biol. 1995;15:4215–4224. doi: 10.1128/MCB.15.8.4215. PubMed DOI PMC

Chabes A.L., Pfleger C.M., Kirschner M.W., Thelander L. Mouse Ribonucleotide Reductase R2 Protein: A New Target for Anaphase-Promoting Complex-Cdh1-Mediated Proteolysis. Proc. Natl. Acad. Sci. USA. 2003;100:3925–3929. doi: 10.1073/pnas.0330774100. PubMed DOI PMC

Chabes A., Thelander L. Controlled Protein Degradation Regulates Ribonucleotide Reductase Activity in Proliferating Mammalian Cells during the Normal Cell Cycle and in Response to DNA Damage and Replication Blocks. J. Biol. Chem. 2000;275:17747–17753. doi: 10.1074/jbc.M000799200. PubMed DOI

Pontarin G., Ferraro P., Bee L., Reichard P., Bianchi V. Mammalian Ribonucleotide Reductase Subunit p53R2 is Required for Mitochondrial DNA Replication and DNA Repair in Quiescent Cells. Proc. Natl. Acad. Sci. USA. 2012;109:13302–13307. doi: 10.1073/pnas.1211289109. PubMed DOI PMC

Tanaka H., Arakawa H., Yamaguchi T., Shiraishi K., Fukuda S., Matsui K., Takei Y., Nakamura Y. A Ribonucleotide Reductase Gene Involved in a p53-Dependent Cell-Cycle Checkpoint for DNA Damage. Nature. 2000;404:42–49. doi: 10.1038/35003506. PubMed DOI

Guittet O., Hakansson P., Voevodskaya N., Fridd S., Graslund A., Arakawa H., Nakamura Y., Thelander L. Mammalian p53R2 Protein Forms an Active Ribonucleotide Reductase In Vitro with the R1 Protein, Which is Expressed Both in Resting Cells in Response to DNA Damage and in Proliferating Cells. J. Biol. Chem. 2001;276:40647–40651. doi: 10.1074/jbc.M106088200. PubMed DOI

Bourdon A., Minai L., Serre V., Jais J.P., Sarzi E., Aubert S., Chretien D., de Lonlay P., Paquis-Flucklinger V., Arakawa H., et al. Mutation of RRM2B, Encoding p53-Controlled Ribonucleotide Reductase (p53R2), Causes Severe Mitochondrial DNA Depletion. Nat. Genet. 2007;39:776–780. doi: 10.1038/ng2040. PubMed DOI

Lim A.Z., McFarland R., Taylor R.W., Gorman G.S. RRM2B Mitochondrial DNA Maintenance Defects. In: Adam M.P., Ardinger H.H., Pagon R.A., Wallace S.E., Bean L.J.H., Mirzaa G., Amemiya A., editors. GeneReviews ((R)) University of Washington; Seattle, WA, USA: 1993–2021. PubMed

Thelander L., Reichard P. Reduction of Ribonucleotides. Annu. Rev. Biochem. 1979;48:133–158. doi: 10.1146/annurev.bi.48.070179.001025. PubMed DOI

Ahmad M.F., Dealwis C.G. The Structural Basis for the Allosteric Regulation of Ribonucleotide Reductase. Prog. Mol. Biol. Transl. Sci. 2013;117:389–410. doi: 10.1016/B978-0-12-386931-9.00014-3. PubMed DOI PMC

Hofer A., Crona M., Logan D.T., Sjoberg B.M. DNA Building Blocks: Keeping Control of Manufacture. Crit. Rev. Biochem. Mol. Biol. 2012;47:50–63. doi: 10.3109/10409238.2011.630372. PubMed DOI PMC

Brown N.C., Canellakis Z.N., Lundin B., Reichard P., Thelander L. Ribonucleoside Diphosphate Reductase. Purification of the Two Subunits, Proteins B1 and B2. Eur. J. Biochem. 1969;9:561–573. doi: 10.1111/j.1432-1033.1969.tb00646.x. PubMed DOI

Brown N.C., Reichard P. Role of Effector Binding in Allosteric Control of Ribonucleoside Diphosphate Reductase. J. Mol. Biol. 1969;46:39–55. doi: 10.1016/0022-2836(69)90056-4. PubMed DOI

Reichard P., Eliasson R., Ingemarson R., Thelander L. Cross-Talk between the Allosteric Effector-Binding Sites in Mouse Ribonucleotide Reductase. J. Biol. Chem. 2000;275:33021–33026. doi: 10.1074/jbc.M005337200. PubMed DOI

Xu H., Faber C., Uchiki T., Fairman J.W., Racca J., Dealwis C. Structures of Eukaryotic Ribonucleotide Reductase I Provide Insights into dNTP Regulation. Proc. Natl. Acad. Sci. USA. 2006;103:4022–4027. doi: 10.1073/pnas.0600443103. PubMed DOI PMC

Chimploy K., Mathews C.K. Mouse Ribonucleotide Reductase Control: Influence of Substrate Binding upon Interactions with Allosteric Effectors. J. Biol. Chem. 2001;276:7093–7100. doi: 10.1074/jbc.M006232200. PubMed DOI

Ray N.B., Mathews C.K. Nucleoside Diphosphokinase: A Functional Link between Intermediary Metabolism and Nucleic Acid Synthesis. Curr. Top. Cell. Regul. 1992;33:343–357. doi: 10.1016/b978-0-12-152833-1.50025-3. PubMed DOI

Nyiri K., Mertens H.D.T., Tihanyi B., Nagy G.N., Kohegyi B., Matejka J., Harris M.J., Szabo J.E., Papp-Kadar V., Nemeth-Pongracz V., et al. Structural Model of Human dUTPase in Complex with a Novel Proteinaceous Inhibitor. Sci. Rep. 2018;8:4326. doi: 10.1038/s41598-018-22145-8. PubMed DOI PMC

Rose M.G., Farrell M.P., Schmitz J.C. Thymidylate Synthase: A Critical Target for Cancer Chemotherapy. Clin. Colorectal Cancer. 2002;1:220–229. doi: 10.3816/CCC.2002.n.003. PubMed DOI

Anderson D.D., Stover P.J. SHMT1 and SHMT2 are Functionally Redundant in Nuclear de Novo Thymidylate Biosynthesis. PLoS ONE. 2009;4:e5839. doi: 10.1371/journal.pone.0005839. PubMed DOI PMC

Okesli A., Khosla C., Bassik M.C. Human Pyrimidine Nucleotide Biosynthesis as a Target for Antiviral Chemotherapy. Curr. Opin. Biotech. 2017;48:127–134. doi: 10.1016/j.copbio.2017.03.010. PubMed DOI PMC

Matsuda S., Kasahara T. Simultaneous and Absolute Quantification of Nucleoside Triphosphates Using Liquid Chromatography-Triple Quadrupole Tandem Mass Spectrometry. Genes Environ. 2018;40:13. doi: 10.1186/s41021-018-0101-8. PubMed DOI PMC

Engstrom J.U., Kmiec E.B. DNA Replication, Cell Cycle Progression and the Targeted Gene Repair Reaction. Cell Cycle. 2008;7:1402–1414. doi: 10.4161/cc.7.10.5826. PubMed DOI

Chen G., Deng X. Cell Synchronization by Double Thymidine Block. Bio Protoc. 2018;8 doi: 10.21769/BioProtoc.2994. PubMed DOI PMC

Bjursell G., Reichard P. Effects of Thymidine on Deoxyribonucleoside Triphosphate Pools and Deoxyribonucleic Acid Synthesis in Chinese Hamster Ovary Cells. J. Biol. Chem. 1973;248:3904–3909. doi: 10.1016/S0021-9258(19)43819-2. PubMed DOI

Morris N.R., Fischer G.A. Studies Concerning Inhibition of the Synthesis of Deoxycytidine by Phosphorylated Derivatives of Thymidine. Biochim. Biophys. Acta. 1960;42:183–184. doi: 10.1016/0006-3002(60)90777-0. PubMed DOI

Skoog L., Bjursell G. Nuclear and Cytoplasmic Pools of Deoxyribonucleoside Triphosphates in Chinese Hamster Ovary Cells. J. Biol. Chem. 1974;249:6434–6438. doi: 10.1016/S0021-9258(19)42175-3. PubMed DOI

Adams R.L.P., Berryman S., Thomson A. Deoxyribonucleoside Triphosphate Pools in Synchronized and Drug-Inhibited L929 Cells. Biochim. Biophys. Acta. 1971;240:455–462. doi: 10.1016/0005-2787(71)90702-7. PubMed DOI

Ligasova A., Raska I., Koberna K. Organization of Human Replicon: Singles or Zipping Couples? J. Struct. Biol. 2009;165:204–213. doi: 10.1016/j.jsb.2008.11.004. PubMed DOI PMC

Ma H.T., Poon R.Y. Synchronization of HeLa Cells. Methods Mol. Biol. 2011;761:151–161. doi: 10.1007/978-1-61779-182-6_10. PubMed DOI

Dresler W.F.C., Stein R. Ueber den Hydroxylharnstoff. Justus Liebigs Annalen der Chemie. 1869;150:242–252. doi: 10.1002/jlac.18691500212. DOI

Singh A., Xu Y.J. The Cell Killing Mechanisms of Hydroxyurea. Genes. 2016;7:99. doi: 10.3390/genes7110099. PubMed DOI PMC

Skoog L., Nordenskjold B. Effects of Hydroxyurea and 1-Beta-D-Arabinofuranosyl-Cytosine on Deoxyribonucleotide Pools in Mouse Embryo Cells. Eur. J. Biochem. 1971;19:81–89. doi: 10.1111/j.1432-1033.1971.tb01290.x. PubMed DOI

Tyrsted G. Effect of Hydroxyurea and 5-Fluorodeoxy-Uridine on Deoxyribonucleoside Triphosphate Pools Early in Phytohemagglutinin-Stimulated Human-Lymphocytes. Biochem. Pharmacol. 1982;31:3107–3113. doi: 10.1016/0006-2952(82)90087-9. PubMed DOI

Koc A., Wheeler L.J., Mathews C.K., Merrill G.F. Hydroxyurea Arrests DNA Replication by a Mechanism that Preserves Basal dNTP Pools. J. Biol. Chem. 2004;279:223–230. doi: 10.1074/jbc.M303952200. PubMed DOI

Tobey R.A., Crissman H.A. Preparation of Large Quantities of Synchronized Mammalian Cells in Late G1 in the Pre-DNA Replicative Phase of the Cell Cycle. Exp. Cell Res. 1972;75:460–464. doi: 10.1016/0014-4827(72)90453-3. PubMed DOI

Enger M.D., Tobey R.A. Effects of Isoleucine Deficiency on Nucleic Acid and Protein Metabolism in Cultured Chinese Hamster Cells. Continued Ribonucleic Acid and Protein Synthesis in the Absence of Deoxyribonucleic Acid Synthesis. Biochemistry. 1972;11:269–277. doi: 10.1021/bi00752a019. PubMed DOI

Raska I., Koberna K., Jarnik M., Petrasovicova V., Bednar J., Raska K., Jr., Bravo R. Ultrastructural Immunolocalization of Cyclin/PCNA in Synchronized 3T3 Cells. Exp. Cell. Res. 1989;184:81–89. doi: 10.1016/0014-4827(89)90366-2. PubMed DOI

Walker M.M., Wanda P.E. Immunochemical Detection of Cell Cycle Synchronization in a Human Erythroleukemia Cell Line, K562. J. Histochem. Cytochem. 1987;35:1143–1148. doi: 10.1177/35.10.3476671. PubMed DOI

Cronstein B.N., Aune T.M. Methotrexate and its Mechanisms of Action in Inflammatory Arthritis. Nat. Rev. Rheumatol. 2020;16:145–154. doi: 10.1038/s41584-020-0373-9. PubMed DOI

Raimondi M.V., Randazzo O., La Franca M., Barone G., Vignoni E., Rossi D., Collina S. DHFR Inhibitors: Reading the Past for Discovering Novel Anticancer Agents. Molecules. 2019;24:1140. doi: 10.3390/molecules24061140. PubMed DOI PMC

Avendano C., Menendez J.C. Antimetabolites That Interfere with Nucleic Acid Biosynthesis. In: Avendano C., Menendez J.C., editors. Medicinal Chemistry of Anticancer Drugs. 2nd ed. Elsevier; Amsterdam, The Netherlands: 2015. pp. 23–79. DOI

Liew S.C. Folic Acid and Diseases—Supplement It or Not? Rev. Assoc. Med. Bras. 2016;62:90–100. doi: 10.1590/1806-9282.62.01.90. PubMed DOI

Cylwik B., Chrostek L. Interactions between Alcohol and Folate. In: Patel V.B., editor. Molecular Aspects of Alcohol and Nutrition. Academic Press; San Diego, CA, USA: 2016. pp. 157–169. Chapter 13. DOI

Ducker G.S., Rabinowitz J.D. One-Carbon Metabolism in Health and Disease. Cell Metab. 2017;25:27–42. doi: 10.1016/j.cmet.2016.08.009. PubMed DOI PMC

Adams R.L.P. Cell Synchronisation. In: Work T.S., Burdon R.H., editors. Laboratory Techniques in Biochemistry and Molecular Biology. Volume 8. Elsevier; Amsterdam, The Netherlands: 1980. pp. 211–238.

McBurney M.W., Whitmore G.F. Mechanism of Growth Inhibition by Methotrexate. Cancer Res. 1975;35:586–590. PubMed

Adams R.L. The Effect of Endogenous Pools of Thymidylate on the Apparent Rate of DNA Synthesis. Exp. Cell Res. 1969;56:55–58. doi: 10.1016/0014-4827(69)90393-0. PubMed DOI

Lindsay J.G., Berryman S., Adams R.L. Characteristics of Deoxyribonucleic acid Polymerase Activity in Nuclear and Supernatant Fractions of Cultured Mouse Cells. Biochem. J. 1970;119:839–848. doi: 10.1042/bj1190839. PubMed DOI PMC

Yunis J.J. High Resolution of Human Chromosomes. Science. 1976;191:1268–1270. doi: 10.1126/science.1257746. PubMed DOI

Rueckert R.R., Mueller G.C. Studies on Unbalanced Growth in Tissue Culture. I. induction and Consequences of Thymidine Deficiency. Cancer Res. 1960;20:1584–1591. PubMed

Kozminski P., Halik P.K., Chesori R., Gniazdowska E. Overview of Dual-Acting Drug Methotrexate in Different Neurological Diseases, Autoimmune Pathologies and Cancers. Int. J. Mol. Sci. 2020;21:3483. doi: 10.3390/ijms21103483. PubMed DOI PMC

Rossana C., Gollakota Rao L., Johnson L.F. Thymidylate Synthetase Overproduction in 5-Fluorodeoxyuridine-Resistant Mouse Fibroblasts. Mol. Cell. Biol. 1982;2:1118–1125. doi: 10.1128/MCB.2.9.1118. PubMed DOI PMC

Grogan B.C., Parker J.B., Guminski A.F., Stivers J.T. Effect of the Thymidylate Synthase Inhibitors on dUTP and TTP Pool Levels and the Activities of DNA Repair Glycosylases on Uracil and 5-Fluorouracil in DNA. Biochemistry. 2011;50:618–627. doi: 10.1021/bi102046h. PubMed DOI PMC

Yan Y., Han X.Z., Qing Y.L., Condie A.G., Gorityala S., Yang S.M., Xu Y., Zhang Y.W., Gerson S.L. Inhibition of Uracil DNA Glycosylase Sensitizes Cancer Cells to 5-Fluorodeoxyuridine through Replication Fork Collapse-Induced DNA Damage. Oncotarget. 2016;7:59299–59313. doi: 10.18632/oncotarget.11151. PubMed DOI PMC

Webber L.M., Garson O.M. Fluorodeoxyuridine Synchronization of Bone Marrow Cultures. Cancer Genet. Cytogenet. 1983;8:123–132. doi: 10.1016/0165-4608(83)90044-4. PubMed DOI

Longley D.B., Harkin D.P., Johnston P.G. 5-Fluorouracil: Mechanisms of Action and Clinical Strategies. Nat. Rev. Cancer. 2003;3:330–338. doi: 10.1038/nrc1074. PubMed DOI

Malet-Martino M., Martino R. Clinical Studies of Three Oral Prodrugs of 5-Fluorouracil (Capecitabine, UFT, S-1): A Review. Oncologist. 2002;7:288–323. doi: 10.1634/theoncologist.7-4-288. PubMed DOI

Power D.G., Kemeny N.E. The Role of Floxuridine in Metastatic Liver Disease. Mol. Cancer Ther. 2009;8:1015–1025. doi: 10.1158/1535-7163.MCT-08-0709. PubMed DOI

Brundret K.M., Dalziel W., Hesp B., Jarvis J.A.J., Neidle S. X-Ray Crystallographic Determination of the Structure of the Antibiotic Aphidicolin: A Tetracyclic Diterpenoid Containing a New Ring System. J. Chem. Soc. Chem. Commun. 1972;18:1027–1028. doi: 10.1039/c39720001027. DOI

Ikegami S., Taguchi T., Ohashi M., Oguro M., Nagano H., Mano Y. Aphidicolin Prevents Mitotic Cell Division by Interfering with the Activity of DNA Polymerase-Alpha. Nature. 1978;275:458–460. doi: 10.1038/275458a0. PubMed DOI

Pedrali-Noy G., Spadari S., Miller-Faures A., Miller A.O., Kruppa J., Koch G. Synchronization of HeLa Cell Cultures by Inhibition of DNA Polymerase Alpha with Aphidicolin. Nucleic Acids Res. 1980;8:377–387. doi: 10.1093/nar/8.2.377. PubMed DOI PMC

Matherly L.H., Schuetz J.D., Westin E., Goldman I.D. A Method for the Synchronization of Cultured-Cells with Aphidicolin -Application to the Large-Scale Synchronization of L1210 Cells and the Study of the Cell-Cycle Regulation of Thymidylate Synthase and Dihydrofolate-Reductase. Anal. Biochem. 1989;182:338–345. doi: 10.1016/0003-2697(89)90605-2. PubMed DOI

Fox M.H., Read R.A., Bedford J.S. Comparison of Synchronized Chinese-Hamster Ovary Cells Obtained by Mitotic Shake-Off, Hydroxyurea, Aphidicolin, or Methotrexate. Cytometry. 1987;8:315–320. doi: 10.1002/cyto.990080312. PubMed DOI

Kim J.K., Esteve P.O., Jacobsen S.E., Pradhan S. UHRF1 Binds G9a and Participates in p21 Transcriptional Regulation in Mammalian Cells. Nucleic Acids Res. 2009;37:493–505. doi: 10.1093/nar/gkn961. PubMed DOI PMC

Gilbert D.M., Neilson A., Miyazawa H., Depamphilis M.L., Burhans W.C. Mimosine Arrests DNA-Synthesis at Replication Forks by Inhibiting Deoxyribonucleotide Metabolism. J. Biol. Chem. 1995;270:9597–9606. doi: 10.1074/jbc.270.16.9597. PubMed DOI

Dai Y.M., Gold B., Vishwanatha J.K., Rhode S.L. Mimosine Inhibits Viral-DNA Synthesis through Ribonucleotide Reductase. Virology. 1994;205:210–216. doi: 10.1006/viro.1994.1636. PubMed DOI

Mosca P.J., Dijkwel P.A., Hamlin J.L. The Plant Amino-Acid Mimosine May Inhibit Initiation at Origins of Replication in Chinese-Hamster Cells. Mol. Cell Biol. 1992;12:4375–4383. doi: 10.1128/MCB.12.10.4375. PubMed DOI PMC

Perry C., Sastry R., Nasrallah I.M., Stover P.J. Mimosine Attenuates Serine Hydroxymethyltransferase Transcription by Chelating Zinc. Implications for Inhibition of DNA Replication. J. Biol. Chem. 2005;280:396–400. doi: 10.1074/jbc.M410467200. PubMed DOI

Wang G., Miskimins R., Miskimins W.K. Mimosine Arrests Cells in G1 by Enhancing the Levels of p27(Kip1) Exp. Cell Res. 2000;254:64–71. doi: 10.1006/excr.1999.4743. PubMed DOI

Nguyen B.C., Tawata S. The Chemistry and Biological Activities of Mimosine: A Review. Phytother. Res. 2016;30:1230–1242. doi: 10.1002/ptr.5636. PubMed DOI

Galgano P.J., Schildkraut C.L. G1/S Phase Synchronization Using Mimosine Arrest. CSH Protoc. 2006;2006 doi: 10.1101/pdb.prot4488. PubMed DOI

Park S.Y., Im J.S., Park S.R., Kim S.E., Wang H.J., Lee J.K. Mimosine Arrests the Cell Cycle Prior to the Onset of DNA Replication by Preventing the Binding of Human Ctf4/and-1 to Chromatin via Hif-1 Alpha Activation in HeLa Cells. Cell Cycle. 2012;11:761–766. doi: 10.4161/cc.11.4.19209. PubMed DOI

Zeman M.K., Cimprich K.A. Causes and Consequences of Replication Stress. Nat. Cell Biol. 2014;16:2–9. doi: 10.1038/ncb2897. PubMed DOI PMC

Byun T.S., Pacek M., Yee M.C., Walter J.C., Cimprich K.A. Functional Uncoupling of MCM Helicase and DNA Polymerase Activities the ATR-Dependent Checkpoint. Gene Dev. 2005;19:1040–1052. doi: 10.1101/gad.1301205. PubMed DOI PMC

MacDougall C.A., Byun T.S., Van C., Yee M.C., Cimprich K.A. The Structural Determinants of Checkpoint Activation. Gene Dev. 2007;21:898–903. doi: 10.1101/gad.1522607. PubMed DOI PMC

Marechal A., Zou L. DNA Damage Sensing by the ATM and ATR Kinases. Cold Spring Harb. Perspect. Biol. 2013;5:a012716. doi: 10.1101/cshperspect.a012716. PubMed DOI PMC

Nam E.A., Cortez D. AIR Signalling: More than Meeting at the Fork. Biochem. J. 2011;436:527–536. doi: 10.1042/BJ20102162. PubMed DOI PMC

Zou L., Elledge S.J. Sensing DNA Damage through ATRIP Recognition of RPA-ssDNA Complexes. Science. 2003;300:1542–1548. doi: 10.1126/science.1083430. PubMed DOI

Darzynkiewicz Z., Halicka H.D., Zhao H., Podhorecka M. Cell Synchronization by Inhibitors of DNA Replication Induces Replication Stress and DNA Damage Response: Analysis by Flow Cytometry. Methods Mol. Biol. 2011;761:85–96. doi: 10.1007/978-1-61779-182-6_6. PubMed DOI PMC

Halicka D., Zhao H., Li J.W., Garcia J., Podhorecka M., Darzynkiewicz Z. DNA Damage Response Resulting from Replication Stress Induced by Synchronization of Cells by Inhibitors of DNA Replication: Analysis by Flow Cytometry. Methods Mol. Biol. 2017;1524:107–119. doi: 10.1007/978-1-4939-6603-5_7. PubMed DOI

Kurose A., Tanaka T., Huang X., Traganos F., Darzynkiewicz Z. Synchronization in the Cell Cycle by Inhibitors of DNA Replication Induces Histone H2AX Phosphorylation: An Indication of DNA Damage. Cell Prolif. 2006;39:231–240. doi: 10.1111/j.1365-2184.2006.00380.x. PubMed DOI PMC

Hammond E.M., Green S.L., Giaccia A.J. Comparison of Hypoxia-Induced Replication Arrest with Hydroxyurea and Aphidicolin-Induced Arrest. Mutat. Res. Mol. Mech. Mutagen. 2003;532:205–213. doi: 10.1016/j.mrfmmm.2003.08.017. PubMed DOI

Yang S.J., Hahn G.M., Bagshaw M.A. Chromosome Aberrations Induced by Thymidine. Exp. Cell Res. 1966;42:130–135. doi: 10.1016/0014-4827(66)90326-0. PubMed DOI

Gong J.P., Traganos F., Darzynkiewicz Z. Growth Imbalance and Altered Expression of Cyclin-B1, Cyclin-a, Cyclin-E, and Cyclin-D3 in Molt-4 Cells Synchronized in the Cell-Cycle by Inhibitors of DNA-Replication. Cell Growth Differ. 1995;6:1485–1493. PubMed

Kuriyama R., Terada Y., Lee K.S., Wang C.L.C. Centrosome Replication in Hydroxyurea-Arrested CHO Cells Expressing GFP-Tagged Centrin2. J. Cell Sci. 2007;120:2444–2453. doi: 10.1242/jcs.008938. PubMed DOI

MacFarlane A.J., Anderson D.D., Flodby P., Perry C.A., Allen R.H., Stabler S.P., Stover P.J. Nuclear Localization of de Novo Thymidylate Biosynthesis Pathway Is Required to Prevent Uracil Accumulation in DNA. J. Biol. Chem. 2011;286:44015–44022. doi: 10.1074/jbc.M111.307629. PubMed DOI PMC

MacFarlane A.J., Perry C.A., McEntee M.F., Lin D.M., Stover P.J. Shmt1 Heterozygosity Impairs Folate-Dependent Thymidylate Synthesis Capacity and Modifies Risk of Apc(min)-Mediated Intestinal Cancer Risk. Cancer Res. 2011;71:2098–2107. doi: 10.1158/0008-5472.CAN-10-1886. PubMed DOI PMC

Schormann N., Ricciardi R., Chattopadhyay D. Uracil-DNA Glycosylases-Structural and Functional Perspectives on An Essential Family of DNA Repair Enzymes. Protein Sci. 2014;23:1667–1685. doi: 10.1002/pro.2554. PubMed DOI PMC

Schrader C.E., Guikema J.E.J., Wu X.M., Stavnezer J. The roles of APE1, APE2, DNA Polymerase Beta and Mismatch Repair in Creating S Region DNA Breaks during Antibody Class Switch. Philos. Trans. R. Soc. B Biol. Sci. 2009;364:645–652. doi: 10.1098/rstb.2008.0200. PubMed DOI PMC

Chon J., Stover P.J., Field M.S. Targeting Nuclear Thymidylate Biosynthesis. Mol. Asp. Med. 2017;53:48–56. doi: 10.1016/j.mam.2016.11.005. PubMed DOI PMC

Wyatt M.D., Wilson D.M. Participation of DNA Repair in the Response to 5-Fluorouracil. Cell. Mol. Life Sci. 2009;66:788–799. doi: 10.1007/s00018-008-8557-5. PubMed DOI PMC

Berger S.H., Jenh C.H., Johnson L.F., Berger F.G. Thymidylate Synthase Overproduction and Gene Amplification in Fluorodeoxyuridine-Resistant Human-Cells. Mol. Pharmacol. 1985;28:461–467. PubMed

Banerjee D., Mayer-Kuckuk P., Capiaux G., Budak-Alpdogan T., Gorlick R., Bertino J.R. Novel Aspects of Resistance to Drugs Targeted to Dihydrofolate Reductase and Thymidylate Synthase. BBA Acta Mol. Basis Dis. 2002;1587:164–173. doi: 10.1016/S0925-4439(02)00079-0. PubMed DOI

Feher Z., Mishra N.C. Aphidicolin-Resistant Chinese-Hamster Ovary Cells Possess Altered DNA-Polymerases of the Alpha-Family. BBA Gene Struct. Expr. 1994;1218:35–47. doi: 10.1016/0167-4781(94)90098-1. PubMed DOI

Zwanenburg T.S.B. Standardized Shake-Off to Synchronize Cultured Cho Cells. Mutat. Res. 1983;120:151–159. doi: 10.1016/0165-7992(83)90157-4. PubMed DOI

Liu Y., Nan B., Niu J., Kapler G.M., Gao S. An Optimized and Versatile Counter-Flow Centrifugal Elutriation Workflow to Obtain Synchronized Eukaryotic Cells. Front. Cell Dev. Biol. 2021;9:664418. doi: 10.3389/fcell.2021.664418. PubMed DOI PMC

Juan G., Hernando E., Cordon-Cardo C. Separation of Live Cells in Different Phases of the Cell Cycle for Gene Expression Analysis. Cytometry. 2002;49:170–175. doi: 10.1002/cyto.10173. PubMed DOI

Vecsler M., Lazar I., Tzur A. Using Standard Optical Flow Cytometry for Synchronizing Proliferating Cells in the G1 Phase. PLoS ONE. 2013;8:e83935. doi: 10.1371/journal.pone.0083935. PubMed DOI PMC

De Brabander M.J., Van de Veire R.M., Aerts F.E., Borgers M., Janssen P.A. The Effects of Methyl (5-(2-thienylcarbonyl)-1H-benzimidazol-2-yl) Carbamate, (R 17934; NSC 238159), a New Synthetic Antitumoral Drug Interfering with Microtubules, on Mammalian Cells Cultured In Vitro. Cancer Res. 1976;36:905–916. PubMed

Salmon E.D., McKeel M., Hays T. Rapid Rate of Tubulin Dissociation from Microtubules in the Mitotic Spindle In Vivo Measured by Blocking Polymerization with Colchicine. J. Cell Biol. 1984;99:1066–1075. doi: 10.1083/jcb.99.3.1066. PubMed DOI PMC

Blagosklonny M.V. Mitotic Arrest and Cell-Fate Why and How Mitotic Inhibition of Transcription Drives Mutually Exclusive Events. Cell Cycle. 2007;6:70–74. doi: 10.4161/cc.6.1.3682. PubMed DOI

Zieve G.W., Turnbull D., Mullins J.M., Mcintosh J.R. Production of Large Numbers of Mitotic Mammalian-Cells by Use of the Reversible Microtubule Inhibitor Nocodazole-Nocodazole Accumulated Mitotic Cells. Exp. Cell Res. 1980;126:397–405. doi: 10.1016/0014-4827(80)90279-7. PubMed DOI

Yao Y.Z., Zhang Y.Y., Liu W.S., Deng X.M. Highly Efficient Synchronization of Sheep Skin Fibroblasts at G2/M Phase and Isolation of Sheep Y Chromosomes by Flow Cytometric Sorting. Sci. Rep. 2020;10:9933. doi: 10.1038/s41598-020-66905-x. PubMed DOI PMC

Romsdahl M.M. Synchronization of Human Cell Lines with Colcemid. Exp. Cell Res. 1968;50:463–467. doi: 10.1016/0014-4827(68)90465-5. PubMed DOI

Vassilev L.T., Tovar C., Chen S., Knezevic D., Zhao X., Sun H., Heimbrook D.C., Chen L. Selective Small-Molecule Inhibitor Reveals Critical Mitotic Functions of Human CDK1. Proc. Natl. Acad. Sci. USA. 2006;103:10660–10665. doi: 10.1073/pnas.0600447103. PubMed DOI PMC

Ma H.T., Tsang Y.H., Marxer M., Poon R.Y. Cyclin A2-Cyclin-Dependent Kinase 2 Cooperates with the PLK1-SCFbeta-TrCP1-EMI1-Anaphase-Promoting Complex/Cyclosome Axis to Promote Genome Reduplication in the Absence of Mitosis. Mol. Cell Biol. 2009;29:6500–6514. doi: 10.1128/MCB.00669-09. PubMed DOI PMC

Vassilev L.T. Cell Cycle Synchronization at the G2/M Phase Border by Reversible Inhibition of CDK1. Cell Cycle. 2006;5:2555–2556. doi: 10.4161/cc.5.22.3463. PubMed DOI

Rao S., Lowe M., Herliczek T.W., Keyomarsi K. Lovastatin Mediated G1 Arrest in Normal and Tumor Breast Cells is through Inhibition of CDK2 Activity and Redistribution of p21 and p27, Independent of p53. Oncogene. 1998;17:2393–2402. doi: 10.1038/sj.onc.1202322. PubMed DOI

JavanMoghadam-Kamrani S., Keyomarsi K. Synchronization of the Cell Cycle Using Lovastatin. Cell Cycle. 2008;7:2434–2440. doi: 10.4161/cc.6364. PubMed DOI

Davis P.K., Ho A., Dowdy S.F. Biological Methods for Cell-Cycle Synchronization of Mammalian Cells. Biotechniques. 2001;30:1322–1326. doi: 10.2144/01306rv01. PubMed DOI

Kues W.A., Anger M., Carnwath J.W., Paul D., Motlik J., Niemann H. Cell Cycle Synchronization of Porcine Fetal Fibroblasts: Effects of Serum Deprivation and Reversible Cell Cycle Inhibitors. Biol. Reprod. 2000;62:412–419. doi: 10.1095/biolreprod62.2.412. PubMed DOI

Khammanit R., Chantakru S., Kitiyanant Y., Saikhun J. Effect of Serum Starvation and Chemical Inhibitors on Cell Cycle Synchronization of Canine Dermal Fibroblasts. Theriogenology. 2008;70:27–34. doi: 10.1016/j.theriogenology.2008.02.015. PubMed DOI

Nilausen K., Green H. Reversible Arrest of Growth in G1 of an Established Fibroblast Line (3T3) Exp. Cell Res. 1965;40:166–168. doi: 10.1016/0014-4827(65)90306-X. PubMed DOI

Holley R.W., Kiernan J.A. Contact Inhibition of Cell Division in 3t3 Cells. Proc. Natl. Acad. Sci. USA. 1968;60:300–304. doi: 10.1073/pnas.60.1.300. PubMed DOI PMC

Forsberg F., Mooser R., Arnold M., Hack E., Wyss P. 3D Micro-Scale Deformations of Wood in Bending: Synchrotron Radiation μCT data Analyzed with Digital Volume Correlation. J. Struct. Biol. 2008;164:255–262. doi: 10.1016/j.jsb.2008.08.004. PubMed DOI

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