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Review

Nucleoside analogs as a radiosensitizer modulating DNA repair, cell cycle checkpoints, and apoptosis

, , , , & ORCID Icon
Pages 439-452 | Received 31 Aug 2019, Accepted 16 Sep 2019, Published online: 27 Sep 2019

References

  • Lawrence, T. S.; Tepper, J. E.; Blackstock, A. W. Fluoropyrimidine-Radiation Interactions in Cells and Tumors. Semin. Radiat. Oncol. 1997, 7, 260–266. DOI: 10.1016/S1053-4296(97)80024-0.
  • Shewach, D. S.; Lawrence, T. S. Antimetabolite Radiosensitizers. J. Clin. Oncol. 2007, 25, 4043–4050.
  • Abdel-Aziz, W.; Jiang, H. Y.; Hickey, R. J.; Malkas, L. H. Ara-C Affects Formation of Cancer Cell DNA Synthesome Replication Intermediates. Cancer Chemother. Pharmacol. 2000, 45, 312–319. DOI: 10.1007/s002800050046.
  • Kufe, D. W.; Major, P. P.; Egan, E. M.; Beardsley, G. P. Correlation of Cytotoxicity with Incorporation of ara-C into DNA. J. Biol. Chem. 1980, 255, 8900–8997.
  • Carson, D. A.; Wasson, D. B.; Kaye, J.; Ullman, B.; Martin, D. W.; Jr.; Robins, R. K.; Montgomery, J. A. Deoxycytidine Kinase-Mediated Toxicity of Deoxyadenosine Analogs toward Malignant Human Lymphoblasts in Vitro and toward Murine L1210 Leukemia in Vivo. Proc. Natl. Acad. Sci. USA. 1980, 77, 6865–6869. DOI: 10.1073/pnas.77.11.6865.
  • Tanabe, K.; Hiraoka, W.; Kuwabara, M.; Sato, F.; Matsuda, A.; Ueda, T. Induction of DNA Double-Strand Breaks in Chinese Hamster V79 Cells by 2-Chlorodeoxyadenosine. Chem. Biol. Interact. 1989, 71, 167–175. DOI: 10.1016/0009-2797(89)90032-X.
  • Nomura, Y.; Inanami, O.; Takahashi, K.; Matsuda, A.; Kuwabara, M. 2-Chloro-2′-Deoxyadenosine Induces Apoptosis through the Fas/Fas Ligand Pathway in Human Leukemia Cell Line MOLT-4. Leukemia 2000, 14, 299–306. DOI: 10.1038/sj.leu.2401649.
  • Takahashi, E.; Inanami, O.; Ohta, T.; Matsuda, A.; Kuwabara, M. Lipid Raft Disruption Prevents Apoptosis Induced by 2-Chloro-2′-Deoxyadenosine (Cladribine) in Leukemia Cell Lines. Leuk. Res. 2006, 30, 1555–1561. DOI: 10.1016/j.leukres.2006.04.008.
  • Tanabe, K.; Hiraoka, W.; Kuwabara, M.; Matsuda, A.; Ueda, T.; Sato, F. Modification of the Repair of Potentially Lethal Damage in Plateau-Phase Chinese Hamster Cells by 2-Chlorodeoxyadenosine. JRR. 1988, 29, 172–181. DOI: 10.1269/jrr.29.172.
  • Shewach, D. S.; Hahn, T. M.; Chang, E.; Hertel, L. W.; Lawrence, T. S. Metabolism of 2′,2′-Difluoro-2′-Deoxycytidine and Radiation Sensitization of Human Colon Carcinoma Cells. Cancer Res. 1994, 54, 3218–3223.
  • Plunkett, W.; Huang, P.; Xu, Y. Z.; Heinemann, V.; Grunewald, R.; Gandhi, V. Gemcitabine: metabolism, Mechanisms of Action, and Self-Potentiation. Semin. Oncol. 1995, 22, 3–10.
  • Gregoire, V.; Rosier, J. F.; De Bast, M.; Bruniaux, M.; De Coster, B.; Octave-Prignot, M.; Scalliet, P. Role of Deoxycytidine Kinase (dCK) Activity in Gemcitabine's Radioenhancement in Mice and Human Cell Lines in Vitro. Radiother. Oncol. 2002, 63, 329–338. DOI: 10.1016/S0167-8140(02)00106-8.
  • Hayashi, M.; Kuwabara, M.; Yoshii, G.; Itoh, T. Sensitization of Escherichia coli B/r to X-Irradiation by 2′-Chloro-2′-Deoxythymidine. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 1984, 45, 185–192. DOI: 10.1080/09553008414550201.
  • Hayashi, M.; Kuwabara, M.; Sato, F.; Itoh, T. Radiation Sensitization of Escherichia coli B/r by 2′-Chloro-2′-Deoxythymidine under Various Irradiation Conditions. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 1985, 47, 523–529. DOI: 10.1080/09553008514550751.
  • Murai, T.; Kubo, K.; Kuwabara, M.; Itoh, T.; Yoshii, G.; Sato, F. Effects of 2′-Chlorothymidine on Chinese Hamster Cells Irradiated with X-Rays and Ultraviolet Light. JRR. 1985, 26, 233–237. DOI: 10.1269/jrr.26.233.
  • Hiraoka, W.; Tanabe, K.; Kuwabara, M.; Sato, F.; Matsuda, A.; Ueda, T. Sensitization of X-Irradiated Chinese Hamster V79 Cells by Derivatives of Pyrimidine Nucleosides. JRR. 1988, 29, 246–254. DOI: 10.1269/jrr.29.246.
  • Hiraoka, W.; Tanabe, K.; Kuwabara, M.; Sato, F.; Matsuda, A.; Ueda, T. Metabolic Effects of 3′-Deoxyadenosine (Cordycepin) and 2-Halo-3′-Deoxyadenosine on Repair of X-Ray-Induced Potentially Lethal Damage in Chinese Hamster V79 Cells. Radiat. Res. 1988, 114, 231–239. DOI: 10.2307/3577221.
  • Hiraoka, W.; Kuwabara, M.; Sato, F. Effects of 3′-Deoxyadenosine (Cordycepin) on the Repair of X-Ray-Induced DNA Single- and Double-Strand Breaks in Chinese Hamster V79 Cells. Jrr. 1990, 31, 156–161. DOI: 10.1269/jrr.31.156.
  • Komlodi-Pasztor, E.; Sackett, D. L.; Fojo, A. T. Inhibitors Targeting Mitosis: tales of How Great Drugs against a Promising Target Were Brought down by a Flawed Rationale. Clin. Cancer Res. 2012, 18, 51–63. DOI: 10.1158/1078-0432.CCR-11-0999.
  • Matsuda, A.; Sasaki, T. Antitumor Activity of Sugar-Modified Cytosine Nucleosides. Cancer Sci. 2004, 95, 105–111. DOI: 10.1111/j.1349-7006.2004.tb03189.x.
  • Ogawa, A.; Shuto, S.; Inanami, O.; Kuwabara, M.; Tanaka, M.; Sasaki, T.; Matsuda, A. Nucleosides and Nucleotides. 176. 2′-Deoxy-2′-Hydroxylaminocytidine: A New Antitumor Nucleoside That Inhibits DNA Synthesis Although It Has a Ribonucleoside Structure. Bioorg. Med. Chem. Lett. 1998, 8, 1913–1918. DOI: 10.1016/S0960-894X(98)00336-9.
  • Hattori, H.; Tanaka, M.; Fukushima, M.; Sasaki, T.; Matsuda, A. Nucleosides and Nucleotides. 158. 1-(3-C-Ethynyl-beta-D-Ribo-Pentofuranosyl)-Cytosine, 1-(3-C-Ethynyl-beta-D-Ribo-Pentofuranosyl)Uracil, and Their Nucleobase Analogues as New Potential Multifunctional Antitumor Nucleosides with a Broad Spectrum of Activity. J. Med. Chem. 1996, 39, 5005–5011. DOI: 10.1021/jm960537g.
  • Abdelrahim, M.; Matsuda, A.; Naing, A. TAS-106: preclinical, Clinical and beyond. Oncology 2013, 85, 356–363. DOI: 10.1159/000356571.
  • Inanami, O.; Iizuka, D.; Iwahara, A.; Yamamori, T.; Kon, Y.; Asanuma, T.; Matsuda, A.; Kashiwakura, I.; Kitazato, K.; Kuwabara, M. A Novel Anticancer Ribonucleoside, 1-(3-C-Ethynyl-beta-D-Ribo-Pentofuranosyl)Cytosine, Enhances Radiation-Induced Cell Death in Tumor Cells. Radiat. Res. 2004, 162, 635–645. DOI: 10.1667/RR3268.
  • Iizuka, D.; Inanami, O.; Matsuda, A.; Kashiwakura, I.; Asanuma, T.; Kuwabara, M. X Irradiation Induces the Proapoptotic State Independent of the Loss of Clonogenic Ability in Chinese Hamster V79 Cells. Radiat. Res. 2005, 164, 36–44. DOI: 10.1667/RR3393.
  • Yasui, H.; Inanami, O.; Asanuma, T.; Iizuka, D.; Nakajima, T.; Kon, Y.; Matsuda, A.; Kuwabara, M. Treatment Combining X-Irradiation and a Ribonucleoside Anticancer Drug, TAS106, Effectively Suppresses the Growth of Tumor Cells Transplanted in Mice. Int. J. Radiat. Oncol. Biol. Phys. 2007, 68, 218–228. DOI: 10.1016/j.ijrobp.2006.12.061.
  • Yasui, H.; Ogura, A.; Asanuma, T.; Matsuda, A.; Kashiwakura, I.; Kuwabara, M.; Inanami, O. Inhibition of HIF-1alpha by the Anticancer Drug TAS106 Enhances X-Ray-Induced Apoptosis in Vitro and in Vivo. Br. J. Cancer. 2008, 99, 1442–1452. DOI: 10.1038/sj.bjc.6604720.
  • Meike, S.; Yamamori, T.; Yasui, H.; Eitaki, M.; Matsuda, A.; Morimatsu, M.; Fukushima, M.; Yamasaki, Y.; Inanami, O. A Nucleoside Anticancer Drug, 1-(3-C-Ethynyl-beta-D-Ribo-Pentofuranosyl)Cytosine (TAS106), Sensitizes Cells to Radiation by Suppressing BRCA2 Expression. Mol. Cancer 2011, 10, 92. DOI: 10.1186/1476-4598-10-92.
  • Maeda, K.; Yasui, H.; Yamamori, T.; Matsuura, T.; Takao, S.; Suzuki, M.; Matsuda, A.; Inanami, O.; Shirato, H. A Nucleoside Anticancer Drug, 1-(3-C-Ethynyl-beta-D-Ribo-Pentofuranosyl)Cytosine, Induces Depth-Dependent Enhancement of Tumor Cell Death in Spread-Out Bragg Peak (SOBP) of Proton Beam. PLoS One 2016, 11, e0166848. DOI: 10.1371/journal.pone.0166848.
  • Azuma, A.; Matsuda, A.; Sasaki, T.; Fukushima, M. 1-(3-C-Ethynyl-beta-D-Ribo-Pentofuranosyl)Cytosine (ECyd, TAS-106)1: antitumor Effect and Mechanism of Action. Nucleos. Nucleot. Nucl. 2001, 20, 609–619. DOI: 10.1081/NCN-100002337.
  • Hattori, H.; Nozawa, E.; Iino, T.; Yoshimura, Y.; Shuto, S.; Shimamoto, Y.; Nomura, M.; Fukushima, M.; Tanaka, M.; Sasaki, T.; et al. Nucleosides and Nucleotides. 175. Structural Requirements of the Sugar Moiety for the Antitumor Activities of New Nucleoside Antimetabolites, 1-(3-C-Ethynyl-beta-D-Ribo-Pentofuranosyl)Cytosine and -uracil1. J. Med. Chem. 1998, 41, 2892–2902. DOI: 10.1021/jm9801814.
  • Matsuda, A.; Fukushima, M.; Wataya, Y.; Sasaki, T. A New Antitumor Nucleoside, 1-(3-C-Ethynyl-beta-D-Ribo-Pentofuranosyl)Cytosine (ECyd), Is a Potent Inhibitor of RNA Synthesis. Nucleos. Nucleot. 1999, 18, 811–814. DOI: 10.1080/15257779908041568.
  • Tabata, S.; Tanaka, M.; Endo, Y.; Obata, T.; Matsuda, A.; Sasaki, T. Anti-Tumor Mechanisms of 3′-Ethynyluridine and 3′-Ethynylcytidine as RNA Synthesis Inhibitors: Development and Characterization of 3′-Ethynyluridine-Resistant Cells. Cancer Lett. 1997, 116, 225–231. DOI: 10.1016/S0304-3835(97)00188-2.
  • Tabata, S.; Tanaka, M.; Matsuda, A.; Fukushima, M.; Sasaki, T. Antitumor Effect of a Novel Multifunctional Antitumor Nucleoside, 3′-Ethynylcytidine, on Human Cancers. Oncol. Rep. 1996, 3, 1029–1034.
  • Maehara, Y.; Nakamura, H.; Nakane, Y.; Kawai, K.; Okamoto, M.; Nagayama, S.; Shirasaka, T.; Fujii, S. Activities of Various Enzymes of Pyrimidine Nucleotide and DNA Syntheses in Normal and Neoplastic Human Tissues. GAN 1982, 73, 289–298.
  • Koizumi, K.; Shimamoto, Y.; Azuma, A.; Wataya, Y.; Matsuda, A.; Sasaki, T.; Fukushima, M. Cloning and Expression of Uridine/Cytidine Kinase cDNA from Human Fibrosarcoma Cells. Int. J. Mol. Med. 2001, 8, 273–278.
  • Hall, E. J.; Giaccia, A. J. In Radiobiology for the Radiologist, 7th ed.; Mitchell C. W., Ed.; Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia, 2012.
  • Franken, N. A.; Oei, A. L.; Kok, H. P.; Rodermond, H. M.; Sminia, P.; Crezee, J.; Stalpers, L. J.; Barendsen, G. W. Cell Survival and Radiosensitisation: modulation of the Linear and Quadratic Parameters of the LQ Model (Review). Int. J. Oncol. 2013, 42, 1501–1515. DOI: 10.3892/ijo.2013.1857.
  • Wilkins, D. E.; Ng, C. E.; Raaphorst, G. P. Cisplatin and Low Dose Rate Irradiation in Cisplatin Resistant and Sensitive Human Glioma Cells. Int. J. Radiat. Oncol. Biol. Phys. 1996, 36, 105–111. DOI: 10.1016/S0360-3016(96)00243-X.
  • Wilkins, D. E.; Heller, D. P.; Raaphorst, G. P. Inhibition of Potentially Lethal Damage Recovery by Cisplatin in a Brain Tumor Cell Line. Anticancer Res. 1993, 13, 2137–2142.
  • Rogakou, E. P.; Boon, C.; Redon, C.; Bonner, W. M. Megabase Chromatin Domains Involved in DNA Double-Strand Breaks in Vivo. J. Cell Biol. 1999, 146, 905–916. DOI: 10.1083/jcb.146.5.905.
  • Schultz, L. B.; Chehab, N. H.; Malikzay, A.; Halazonetis, T. D. p53 Binding Protein 1 (53BP1) Is an Early Participant in the Cellular Response to DNA Double-Strand Breaks. J. Cell Biol. 2000, 151, 1381–1390. DOI: 10.1083/jcb.151.7.1381.
  • Bracey, T. S.; Williams, A. C.; Paraskeva, C. Inhibition of Radiation-Induced G2 Delay Potentiates Cell Death by Apoptosis and/or the Induction of Giant Cells in Colorectal Tumor Cells with Disrupted p53 Function. Clin. Cancer Res. 1997, 3, 1371–1381.
  • Higuchi, K.; Mitsuhashi, N.; Saitoh, J.; Maebayashi, K.; Sakurai, H.; Akimoto, T.; Niibe, H. Caffeine Enhanced Radiosensitivity of Rat Tumor Cells with a Mutant-Type p53 by Inducing Apoptosis in a p53-Independent Manner. Cancer Lett. 2000, 152, 157–162. DOI: 10.1016/S0304-3835(99)00449-8.
  • Zhou, B. B.; 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 G(2)/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.
  • Yu, L.; Orlandi, L.; Wang, P.; Orr, M. S.; Senderowicz, A. M.; Sausville, E. A.; Silvestrini, R.; Watanabe, N.; Piwnica-Worms, H.; O'Connor, P. M. UCN-01 Abrogates G2 Arrest through a Cdc2-Dependent Pathway That Is Associated with Inactivation of the Wee1Hu Kinase and Activation of the Cdc25C Phosphatase. J. Biol. Chem. 1998, 273, 33455–33464. DOI: 10.1074/jbc.273.50.33455.
  • Yu, Q.; La Rose, J.; Zhang, H.; Takemura, H.; Kohn, K. W.; Pommier, Y. UCN-01 Inhibits p53 up-Regulation and Abrogates Gamma-Radiation-Induced G(2)-M Checkpoint Independently of p53 by Targeting Both of the Checkpoint Kinases, Chk2 and Chk1. Cancer Res. 2002, 62, 5743–5748.
  • Iizuka, D.; Inanami, O.; Kashiwakura, I.; Kuwabara, M. Purvalanol a Enhances Cell Killing by Inhibiting up-Regulation of CDC2 Kinase Activity in Tumor Cells Irradiated with High Doses of X Rays. Radiat. Res. 2007, 167, 563–571. DOI: 10.1667/RR0622.1.
  • Meike, S.; Yamamori, T.; Yasui, H.; Eitaki, M.; Matsuda, A.; Inanami, O. 8-Aminoadenosine Enhances Radiation-Induced Cell Death in Human Lung Carcinoma A549 Cells. JRR. 2011, 52, 456–463. DOI: 10.1269/jrr.10188.
  • Altieri, D. C. Survivin, Versatile Modulation of Cell Division and Apoptosis in Cancer. Oncogene 2003, 22, 8581–8589. DOI: 10.1038/sj.onc.1207113.
  • Schimmer, A. D. Inhibitor of Apoptosis Proteins: translating Basic Knowledge into Clinical Practice. Cancer Res. 2004, 64, 7183–7190. DOI: 10.1158/0008-5472.CAN-04-1918.
  • Shin, S.; Sung, B. J.; Cho, Y. S.; Kim, H. J.; Ha, N. C.; Hwang, J. I.; Chung, C. W.; Jung, Y. K.; Oh, B. H. An anti-Apoptotic Protein Human Survivin Is a Direct Inhibitor of Caspase-3 and -7. Biochemistry 2001, 40, 1117–1123. DOI: 10.1021/bi001603q.
  • Harada, H. How Can we Overcome Tumor Hypoxia in Radiation Therapy? J. Radiat. Res. 2011, 52, 545–556. DOI: 10.1269/jrr.11056.
  • Brown, J. M. Tumor Hypoxia in Cancer Therapy. Meth. Enzymol. 2007, 435, 297–321. DOI: 10.1016/S0076-6879(07)35015-5.
  • Naing, A.; Fu, S.; Zinner, R. G.; Wheler, J. J.; Hong, D. S.; Arakawa, K.; Falchook, G. S.; Kurzrock, R. Phase I Dose-Escalating Study of TAS-106 in Combination with Carboplatin in Patients with Solid Tumors. Invest. New Drugs 2014, 32, 154–159. DOI: 10.1007/s10637-013-9964-5.
  • Friday, B.; Lassere, Y.; Meyers, C. A.; Mita, A.; Abbruzzese, J. L.; Thomas, M. B. A Phase I Study to Determine the Safety and Pharmacokinetics of Intravenous Administration of TAS-106 Once per Week for Three Consecutive Weeks Every 28 Days in Patients with Solid Tumors. Anticancer Res. 2012, 32, 1689–1696.
  • Hammond-Thelin, L. A.; Thomas, M. B.; Iwasaki, M.; Abbruzzese, J. L.; Lassere, Y.; Meyers, C. A.; Hoff, P.; de Bono, J.; Norris, J.; Matsushita, H.; et al. Phase I and Pharmacokinetic Study of 3′-C-Ethynylcytidine (TAS-106), an Inhibitor of RNA Polymerase I, II and III, in Patients with Advanced Solid Malignancies. Invest. New Drugs 2012, 30, 316–326. DOI: 10.1007/s10637-010-9535-y.
  • Tsao, A.; Hui, E. P.; Juergens, R.; Marur, S.; Huat, T. E.; Cher, G. B.; Hong, R. L.; Hong, W. K.; Chan, A. T. Phase II Study of TAS-106 in Patients with Platinum-Failure Recurrent or Metastatic Head and Neck Cancer and Nasopharyngeal Cancer. Cancer Med. 2013, 2, 351–359. DOI: 10.1002/cam4.79.
  • Ishikawa, H.; Tsuji, H.; Murayama, S.; Sugimoto, M.; Shinohara, N.; Maruyama, S.; Murakami, M.; Shirato, H.; Sakurai, H. Particle Therapy for Prostate Cancer: The past, Present and Future. Int. J. Urol. in press. DOI: 10.1111/iju.14041.
  • Maeda, K.; Yasui, H.; Matsuura, T.; Yamamori, T.; Suzuki, M.; Nagane, M.; Nam, J. M.; Inanami, O.; Shirato, H. Evaluation of the Relative Biological Effectiveness of Spot-Scanning Proton Irradiation in Vitro. J. Radiat. Res. 2016, 57, 307–311. DOI: 10.1093/jrr/rrv101.
  • Matsumoto, Y.; Matsuura, T.; Wada, M.; Egashira, Y.; Nishio, T.; Furusawa, Y. Enhanced Radiobiological Effects at the Distal End of a Clinical Proton Beam: In Vitro Study. J. Radiat. Res 2014, 55, 816–822. DOI: 10.1093/jrr/rrt230.
  • Chaudhary, P.; Marshall, T. I.; Perozziello, F. M.; Manti, L.; Currell, F. J.; Hanton, F.; McMahon, S. J.; Kavanagh, J. N.; Cirrone, G. A.; Romano, F.; et al. Relative Biological Effectiveness Variation along Monoenergetic and Modulated Bragg Peaks of a 62-MeV Therapeutic Proton Beam: A Preclinical Assessment. Int. J. Radiat. Oncol. Biol. Phys. 2014, 90, 27–35. DOI: 10.1016/j.ijrobp.2014.05.010.

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