RECQL1 and WRN DNA repair helicases: Potential 3 therapeutic targets and proliferative markers against cancers

Frontiers in Genetics

Volumn 5, Issue DEC, 2014, Pages

  Futami, Kazunobu ^a   Furuichi, Yasuhiro ^a  

^a GeneCare Research Institute Co Ltd   (Japan)

Author keywords

Anticancer drug candidates; Chemotherapy; DDS; Genome instability; Mitotic catastrophe; RecQ helicases; RECQL1 siRNA; WRN siRNA

Indexed keywords

ANTINEOPLASTIC AGENT; APHIDICOLIN; ATM PROTEIN; BLEOMYCIN; CAMPTOTHECIN; CYCLOPHOSPHAMIDE; DNA HELICASE; DNA TOPOISOMERASE INHIBITOR; DOXORUBICIN; ETOPOSIDE; FLUOROURACIL; KINESIN; MICRORNA; MITOMYCIN; NSC 19630; PLATINUM DERIVATIVE; RECQ HELICASE; SMALL INTERFERING RNA; SURVIVIN; TELOMERASE; TOLL LIKE RECEPTOR; TUMOR MARKER; UNCLASSIFIED DRUG; VASCULOTROPIN A; BLOOM SYNDROME HELICASE; RECQL1; WERNER SYNDROME PROTEIN;

ARTICLE; CANCER CELL; CANCER CHEMOTHERAPY; CARCINOGENESIS; CELL CYCLE REGULATION; DNA DAMAGE; DNA REPAIR; DOWN REGULATION; GENE SILENCING; GENOMIC INSTABILITY; HUMAN; IMMUNOHISTOCHEMISTRY; MOLECULARLY TARGETED THERAPY; NEOPLASM; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; RNA INTERFERENCE; WERNER SYNDROME; CANCER PROGNOSIS; CANCER RECURRENCE; CELL DIVISION; CELL PROLIFERATION; GENE EXPRESSION; GENE REPLICATION; GENETIC RECOMBINATION; GROWTH RATE; MITOSIS INHIBITION; REVIEW; SURVIVAL TIME; TUMOR CELL;

MUS;

EID: 84917686626     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2014.00441     Document Type: Article

References (83)

1. Aggarwal M, Banerjee T, Sommers JA, Brosh RM Jr. (2013) Targeting an Achilles' heel of cancer with a WRN helicase inhibitor. Cell Cycle. 2013 Oct 15;12(20):3329-35. doi: 10.4161/cc.26320. Epub 2013 Sep 12.
2. Aggarwal, M., Sommers, J.A., Shoemaker, R.H., Brosh, R.M. Jr. (2011) Inhibition of helicase activity by a small molecule impairs Werner syndrome helicase (WRN) function in the cellular response to DNA damage or replication stress. Proc Natl Acad Sci U S A. 108, 1525-1530. doi: 10.1073/pnas.1006423108.
3. Agrelo, R., Cheng, W.H., Setien, F., Ropero, S., Espada, J., Fraga, M.F., et al. (2006) Epigenetic inactivation of the premature aging Werner syndrome gene in human cancer. Proc Natl Acad Sci U S A. 103:8822-8827.
4. Arai, A., Chano, T., Futami, K., Furuichi, Y., Ikebuchi, K., Inui, T., et al. (2011). RECQL1 and WRN proteins are potential therapeutic targets in head and neck squamous cell carcinoma. Cancer Res. 71, 4598-4607. doi: 10.1158/0008-5472.
5. Banerjee, T., Aggarwal, M., Brosh, R.M. Jr. (2013) A new development in DNA repair modulation: discovery of a BLM helicase inhibitor. Cell Cycle. 12:713-4. doi: 10.4161/cc.23953.
6. Bernstein K.A., Gangloff, S., Rothstein, R. (2010). The RecQ DNA helicases in DNA repair. Annu. Rev. Genet. 44, 393-417. doi: 0.1146/annurev-genet-102209-163602.
7. Berti, M., Ray, Chaudhuri A., Thangavel, S., Gomathinayagam, S., Kenig, S., et al. (2013). Human RECQ1 promotes restart of replication forks reversed by DNA topoisomerase I inhibition. Nat. Struct. Mol. Biol. 20, 347-354. doi: 10.1038/nsmb.2501.
8. Bouwman, P. and Jonkers, J. (2012). The effects of deregulated DNA damage signaling on cancer chemotherapy response and resistance. Nat Rev. Cancer, 12, 9, 587-598. doi: 10.1038/nrc3342.
9. Brosh, R.M. Jr. (2013). DNA helicases involved in DNA repair and their roles in cancer. Nat. Rev. Cancer 13, 542-558.
10. Chan, T.A., Hermeking, H., Lengauer, C., Kinzler, K.W., Vogelstein, B. (1999). 14-3-3 Sigma is required to prevent mitotic catastrophe after DNA damage. Nature 401, 6753, 616-620. doi: 10.1038/nrc3560.
11. Cheng, W.H., Muftic, D., Muftuoglu, M., Dawut, L., Morris, C., Helleday, T. (2008) WRN is required for ATM activation and the S-phase checkpoint in response to interstrand cross-link-induced DNA double-strand breaks. Mol Biol Cell. 19:3923-33. doi: 10.1091/mbc.E07-07-0698. Epub 2008 Jul 2.
12. Croteau DL, Popuri V, Opresko PL, Bohr VA. (2014) Human RecQ helicases in DNA repair, recombination, and replication.Annu Rev Biochem. 2014;83:519-52. doi: 10.1146/annurev-biochem-060713-035428.
13. Cotton, R.T., Li, D., Scherer, S.E., Muzny, D.M., Hodges, S.E., Catania, R.L., et al. (2009). Single nucleotide polymorphism in RECQL and survival in resectable pancreatic adenocarcinoma. HPB (Oxford). 11:435-444. doi: 10.1111/j.1477-2574.
14. Cui, S., Arosio, D., Doherty, K.M., Brosh, R.M. Jr, Falaschi, A., Vindigni, A. (2004). Analysis of the unwinding activity of the dimeric RECQ1 helicase in the presence of human replication protein A. Nucleic Acids Res. 32, 7, 2158-2170.
15. Cui, S., Klima, R., Ochem, A., Arosio, D., Falaschi, A., Vindigni, A. (2003). Characterization of the DNA-unwinding activity of human RECQ1, a helicase specifically stimulated by human replication protein A. J Biol Chem. 278, 3, 1424-1432.
16. Daniel, R., Litwin, S., Katz, R.A., Skalka, A.M. (2001). Computational analysis of retrovirus-induced scid cell death. J Virol. 75, 7, 3121-3128.
17. Doherty, K.M., Sharma, S., Uzdilla, L.A., Wilson, T.M., Cui, S., Vindigni, A., et al. (2005). RECQ1 helicase interacts with human mismatch repair factors that regulate genetic recombination. J Biol Chem. 280, 30, 28085-28094.
18. Duxbury, M.S., Ito, H., Zinner, M.J., Ashley, S.W., Whang, E.E. (2004). RNA interference targeting the M2 subunit of ribonucleotide reductase enhances pancreatic adenocarcinoma chemosensitivity to gemcitabine. Oncogene 23, 1539-1548.
19. Ellis, N.A., Groden, J., Ye, T.Z., Straughen, J., Lennon, D.J., Ciocci, S., et al. (1995). The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 83, 655-666.
20. Erenpreisa, J. and Cragg, M.S. (2001). Mitotic death: a mechanism of survival? A review. Cancer cell international, 1, 1. Doi:10.1186/1475-2867-1-1.
21. Frei, C. and Gasser, S.M. (2000). RecQ-like helicases: the DNA replication checkpoint connection. J Cell Sci. 113, 2641-2546.
22. Fukuchi, K., Martin, G.M., Monnat, R.J. Jr. (1989). Mutator phenotype of Werner syndrome is characterized by extensive deletions. Proc Natl Acad Sci U S A. 86, 15, 5893-5897.
23. Furuichi, Y. (2001). Premature aging and predisposition to cancers caused by mutations in RecQ family helicases. Ann. N Y Acad. Sci. 928, 121-131.
24. Futami, K., Ishikawa, Y., Goto, M., Furuichi, Y., Sugimoto, M. (2008 b). The role of WRN helicase in carcinogenesis and in resistance by cancer cells to genotoxins. Cancer Sci. 99, 843-848. doi: 10.1111/j.1349-7006.2008.00778.x.
25. Futami, K., Kumagai, E., Makino, H., Goto, H., Takagi, M., Shimamoto, A., et al. (2008 a). Induction of mitotic cell death in cancer cells by small interference RNA suppressing the expression of RecQL1 helicase. Cancer Sci. 99, 71-80.
26. Futami, K., Kumagai, E., Makino, H., Sato, A., Takagi, M., Shimamoto, A., et al. (2008 c). Anticancer activity of RecQL1 helicase siRNA in mouse xenograft models. Cancer Sci. 99, 1227-1236. doi: 10.1111/j.1349-7006.2008.00794.
27. Futami, K., Ogasawara, S., Goto, H., Yano, H., Furuichi, Y. (2010). RecQL1 DNA repair helicase: A potential tumor marker and therapeutic target against hepatocellular carcinoma. Int. J. Mol. Med. 25, 537-545.
28. Futami, K., Takagi, M., Shimamoto, A., Sugimoto, M., Furuichi, Y. (2007). Increased chemotherapeutic activity of camptothecin in cancer cells by siRNA-induced silencing of WRN helicase. Biol. Pharm. Bull. 30, 1958-1961.
29. Goto, M., Miller, R.W., Ishikawa, Y., Sugano, H. (1996). Excess of rare cancers in Werner syndrome (adult progeria). Cancer Epidemiol Biomarkers Prev. 5, 239 -246 Gupta, R., Brosh, R.M. Jr. (2008). Helicases as prospective targets for anti-cancer therapy. Anticancer Agents Med. Chem. 8, 390-401.
30. Gupta, R., Brosh, R.M. Jr. (2008). Helicases as prospective targets for anti-cancer therapy. Anticancer Agents Med. Chem. 8, 390-401
31. Hamm, S., Latz, E., Hangel, D., Müller, T., Yu, P., Golenbock, D., et al. (2010) Alternating 2'-O-ribose methylation is a universal approach for generating non-stimulatory siRNA by acting as TLR7 antagonist. Immunobiology. 215:559-69. doi: 10.1016/j.imbio.2009.09.003.
32. Helleday, T., Petermann, E., Lundin, C., Hodgson, B., Sharma, R.A. (2008). DNA repair pathways as targets for cancer therapy. Nat. Rev. Cancer 8, 193-204. doi: 10.1038/nrc2342
33. Hickson, I.D. (2003). RecQ helicases: caretakers of the genome. Nat. Rev. Cancer 3, 169-178
34. Judge, A.D., Sood, V., Shaw, J.R., Fang, D., McClintock, K., MacLachlan, I. (2005) Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat Biotechnol. 23:457-62.
35. Kawabe, T., Tsuyama, N., Kitao, S., Nishikawa, K., Shimamoto, A., Shiratori, M., et al. (2000). Differential regulation of human RecQ family helicases in cell transformation and cell cycle. Oncogene 19, 4764-4772.
36. Kelly, M.R., Fishel, M.L. (2008). DNA repair proteins as molecular targets for cancer therapeutics. AnticancerAgents Med. Chem. 8, 417-425.
37. Kitao, S., Ohsugi, I.,Ichikawa, K.,Goto, M., Furuichi, Y. and Shimamoto A. (1998) Cloning of two New Human Helicase Genes of the RecQ Family:Biological Significance of Multiple Specie in Higher Eukaryote. Genomics 54, 443-452.
38. Kitao, S., Shimamoto, A., Furuichi, Y. (2002) Molecular Biology of Rothmund-Thomson syndrome (review article). In: Hisama, F.M., Weisman, S.M., Martin, G.M., (eds) Chromosomal instability and aging: basic science and clinical implication. Marcel Dekker, New York, pp 223-224.
39. Kitao S., Shimamoto, A., Goto, M., Miller, R.W., Smithson, W.A., Lindor, N.M., et al. (1999) Mutations in RECQL4 cause a subset of cases of Rothmund- Thomson syndrome. Nat Genet. 22:82-84.
40. LeRoy, G., Carroll, R., Kyin, S., Seki, M., Cole, M.D. (2005). Identification of RecQL1 as a holliday junction processing enzyme in human cell lines. Nucleic Acids Res. 33, 6251-6257. doi: 10.1093/nar/gki929
41. Li, D., Frazier M., Evans, D.B., Hess, K.R., Crane, C.H., Jia, L., et al.(2006a). Single nucleotide polymorphisms of RecQ1, RAD54L, and ATM genes are associated with reduced survival of pancreatic cancer. J Clin. Oncol. 24, 11, 1720-1728
42. Li, D., Liu, H., Jiao, L., Chang, D.Z., Beinart, G., Wolff, R.A., et al. (2006b) Significant effect of homologous recombination DNA repair gene polymorphisms on pancreatic cancer survival. Cancer Res., 66, 6, 3323-3330.
43. Lindor, N.M., Furuichi, Y., Kitao, S., Shimamoto, A., Arndt, C., Jalal, S. (2000) Rothmund-Thomson syndrome due to RECQ4 helicase mutations: report and clinical and molecular comparisons with Bloom syndrome and Werner syndrome. Am J Med Genet 90:223-8.
44. Mao, F.J., Sidorova, J.M., Lauper, J.M., Emond, M.J., Monnat, R.J. (2010) The human WRN and BLM RecQ helicases differentially regulate cell proliferation and survival after chemotherapeutic DNA damage. Cancer Res. 70:6548-55. doi: 10.1158/0008-5472.
45. Martin GM. (1985) Genetics and aging; the Werner syndrome as a segmental progeroid syndrome. Adv Exp Med Biol.;190:161-170.
46. Mendoza-Maldonado, R., Faoro, V., Bajpai, S., Berti, M., Odreman, F., Vindigni, et al. (2011). The human RECQ1 helicase is highly expressed in glioblastoma and plays an important role in tumor cell proliferation. Mol. Cancer 10, 83. doi: 10.1186/1476-4598-10-83.
47. Moser, R., Toyoshima, M., Robinson, K., Gurley, K.E., Howie, H.L., Davison, J., et al. (2012). MYC-driven tumorigenesis is inhibited by WRN syndrome gene deficiency. Mol Cancer Res. 10, 535-545. doi: 10.1158/1541-7786.MCR-11-0508.
48. Nguyen, G.H., Dexheimer, T.S., Rosenthal, A.S., Chu, W.K., Singh, D.K., Mosedale, G.et al. (2013) A small molecule inhibitor of the BLM helicase modulates chromosome stability in human cells. Chem Biol. 20:55-62. doi: 10.1016/j.chembiol.2012.10.016.
49. Nitta, M., Kobayashi, O., Honda, S., Hirota, T., Kuninaka, S., Marumoto, T., et al. H. (2004). Spindle checkpoint function is required for mitotic catastrophe induced by DNA-damaging agents. Oncogene 23, 39, 6548-6558.
50. Novina, C.D. and Sharp, P.A. (2004). The RNAi revolution. Nature, 430, 161-164.
51. Nyberg, K.A., Michelson, R.J., Putnam, C.W., Weinert, T.A. (2002). Toward maintaining the genome: DNA damage and replication checkpoints. Annu.Rev. Genet. 36, 617-656.
52. Opresko, P.L., Cheng, W.H., Bohr, V.A. (2004). Junction of RecQ helicase biochemistry and human disease. J Biol. Chem. 279, 18, 18099-18102.
53. Pichierri, P., Ammazzalorso, F., Bignami, M., Franchitto, A. (2011). The Werner syndrome protein: linking the replication checkpoint response to genome stability. Aging, 3,3, 311-318.
54. Popuri, V., Hsu, J., Khadka, P., Horvath, K., Liu, Y., Croteau, D. L., et al. (2014). Human RECQL1 participates in telomere maintenance. Nucleic Acids Res. 42, 5671-5688. doi: 10.1093/nar/gku200.
55. Popuri, V., Ramamoorthy, M., Tadokoro, T., Singh, D.K., Karmakar, P., Croteau, D.L., et al. (2012) Recruitment and retention dynamics of RECQL5 at DNA double strand break sites. DNA Repair.11:624-35. doi:10.1016/j.dnarep.2012.05.001.
56. Ramamoorthy, M., Tadokoro, T., Rybanska,.I, Ghosh, A.K., Wersto, R., May, A. (2012) RECQL5 cooperates with Topoisomerase II alpha in DNA decatenation and cell cycle progression. Nucleic Acids Res. 40:1621-35. doi: 10.1093/nar/gkr844. Epub 2011 Oct 19.
57. Roninson, I.B., Broude, E.V., Chang, B.D. (2001). If not apoptosis, then what? Treatment induced senscence and mitotic catastrophe in tumor cells. Drug Resist Update 4, 303-313.
58. Rosenthal A.S., Dexheimer T.S., Gileadi O., Nguyen G.H., Chu W.K., Hickson I.D., et al. (2013) Synthesis and SAR studies of 5-(pyridin-4-yl)-1,3,4-thiadiazol-2-amine derivatives as potent inhibitors of Bloom helicase. Bioorg Med Chem Lett. 23:5660-6. doi: 10.1016/j.bmcl.
59. Sakamoto, S., Nishikawa, K., Heo, S.J., Goto, M., Furuichi, Y., Shimamoto, A. (2001). Werner helicase relocates into nuclear foci in response to DNA damaging agents and co-localizes with RPA and Rad51. Genes Cells. 6, 5, 421-430.
60. Sanada, S., Futami,K., Terada,A., Yonemoto,K., Ogasawara, S., Akiba, J., et al. (2013). RECQL1 DNA repair helicase: a potential therapeutic target and a proliferative marker against ovarian cancer. PLoS ONE 8, e72820.doi:10.1371/journal.pone.0072820.
61. Seki, M., Miyazawa, H., Tada, S., Yanagisawa, J., Yamaoka, T., Hoshino, S., et al. (1994). Molecular cloning of cDNA encoding human DNA helicase Q1 which has homology to Escherichia coli Rec Q helicase and localization of the gene at chromosome 12p12. Nucleic Acids Res. 22, 4566-4573.
62. Shadrick W.R., Ndjomou J., Kolli R., Mukherjee S., Hanson A.M., Frick D.N. (2013) Discovering new medicines targetting helicases: challenges and recent progress. J Biomol Screen 18, 761-81.
63. Sharma, S., Brosh, R.M. Jr. (2007). Human RECQ1 is a DNA damage responsive protein required for genotoxic stress resistance and suppression of sister chromatid exchanges. PLoS One 2, e1297.
64. Sharma, S., Brosh, R.M. Jr. (2008). Unique and important consequences of RECQ1 deficiency in mammalian cells. Cell Cycle 7, 989-1000.
65. Sharma, S., Doherty, K.M., Brosh, R.M. Jr. (2006). Mechanisms of RecQ helicases in pathways of DNA metabolism and maintenance of genomic stability. Biochem. J. 398, 319-337.
66. Sharma, S., Stumpo, D.J., Balajee, A.S., Bock, C.B., Lansdorp, P.M., Brosh, R.M.Jr., Blackshear, P.J. (2007). RECQL, a member of the RecQ family of DNA helicases, suppresses chromosomal instability. Mol Cell Biol. 27, 1784-1794.
67. Shimamoto, A. Nishikawa, K., Kitao, S., Furuichi, Y. (2000) Human RecQ5beta, a large isomer of RecQ5 DNA helicase, localizes in the nucleoplasm and interacts with topoisomerases 3alpha and 3beta. Nucleic Acids Res. 28:1647-55
68. Shimamoto, A., Sugimoto, M., Furuichi, Y. (2004). Molecular biology of Werner syndrome. Int. J. Clin. Oncol. 9, 288-298.
69. Slupianek, A., Poplawski, T., Jozwiakowski, S.K., Cramer, K., Pytel, D., Stoczynska, E., et al. (2011). BCR/ABL stimulates WRN to promote survival and genomic instability. Cancer Res. 71, 842-851. doi: 10.1158/0008-5472.CAN-10-1066.
70. Su, Y., Meador, J.A., Calaf, G.M., Proietti, De-Santis. L., Zhao, Y. et al. (2010) Human RecQL4 helicase plays critical roles in prostate carcinogenesis. Cancer Res. 70:9207-17. doi: 10.1158/0008-5472.CAN-10-1743.
71. Sugimoto M. (2014) A cascade leading to premature aging phenotypes including abnormal tumor profiles in Werner syndrome (review). Int J Mol Med. 33:247-53. doi: 10.3892/ijmm.2013.1592. Epub 2013 Dec 17.
72. Tabernero, J., Shapiro, G.I., LoRusso, P.M., Cervantes, A., Schwartz, G.K., Weiss, G.J., et al. (2013). First-in-humans trial of an RNA interference therapeutic targeting VEGF and KSP in cancer patients with liver involvement. Cancer Discov. 4, 406-417. doi: 10.1158/2159-8290.
73. Tahara, H., Tokutake, Y., Maeda, S., Kataoka, H., Watanabe, T., Satoh, M., et al. (1997). Abnormal telomere dynamics of B-lymphoblastoid cell strains from Werner's syndrome patients transformed by Epstein-Barr virus. Oncogene. 15, 1911 -1920.
74. Tao, J., Tao, S., Han, J., Zhou, Z., Zhang, X., Wang, H., et al. (2014). RECQL1 plays an important role in the development of tongue squamous cell carcinoma. Cell Physiol Biochem. 33, 5, 1579-1590. doi: 10.1159/000358721.
75. Vaishnaw, A.K., Gollob, J., Gamba-Vitalo, C., Hutabarat, R., Sah, D., Meyers, R. et al. (2010) A status report on RNAi therapeutics. Silence. 8:1-14. doi:10.1186/1758-907X-1-14.
76. Vogel, C., Hager, C., Bastians, H. (2007). Mechanism of mitotic cell death induced by chemotherapy-mediated G2 checkpoint abrogation. Cancer Res. 67, 339-345.
77. Wu, Y., Brosh, R.M. Jr. (2010). Distinct roles of RECQ1 in the maintenance of genomic stability. DNA Repair 9, 315-324.
78. Yamabe, Y., Shimamoto, A., Goto, M., Yokota, J., Sugawara, M., Furuichi, Y. (1998). Sp1-mediated transcription of the Werner helicase gene is modulated by Rb and p53. Mol Cell Biol. 18, 6191-6200.
79. Yano J, Hirabayashi K, Nakagawa S, Yamaguchi T, Nogawa M, Kashimori I, et al. (2004) Antitumor activity of small interfering RNA/cationic liposome complex in mouse models of cancer. Clin Cancer Res. 10:7721-7726.
80. Yonesaka, K., Tamura, K., Kurata, T., Satoh, T., Ikeda, M., Fukuoka, M., et al. (2006). Small interfering RNA targeting survivin sensitizes lung cancer cell with mutant p53 to adriamycin. Int. J. Cancer 118, 812-820.
81. Yu, C.E., Oshima, J., Fu, Y.H., Wijsman, E.M., Hisama, F., Alisch, R., et al. (1996). Positional cloning of the Werner's syndrome gene. Science 272, 258-262.
82. Zhou, B.B. and Elledge, S.J. (2000). The DNA damage response: putting checkpoints in perspective. Nature 408, 433-439.
83. Zhou, D., He, Q.S., Wang, C., Zhang, J., Wong-Staal, F. (2006). RNA interference and potential applications. Curr.Topics Med Chem., 6, 901-911.