Abstract
Three human RecQ DNA helicases, WRN, BLM and RTS, are involved in the genetic disorders associated with genomic instability and a high incidence of cancer. RecQL1 and RecQL5 also belong to the human RecQ helicase family, but their correlation with genetic disorders, if any, is unknown. We report here that in human B cells transformed by Epstein-Barr virus (EBV), human fibroblasts and umbilical endothelial cells transformed by simian virus 40, the expression of WRN, BLM, RTS and RecQL1 was sharply up-regulated. In B cells this expression was stimulated within 5–40 h by the tumor promoting agent phorbol myristic acetate (PMA). Interestingly, RecQL5β, an alternative splicing product of RecQL5 with a nuclear localization signal, is expressed in resting B cells without significant modulation of its synthesis by EBV or PMA, suggesting it has a role in resting cells. We also roughly determined the number of copies per cell for the five RecQ helicase in B cells. In addition, levels of the different RecQ helicases are modulated in different ways during the cell cycle of actively proliferating fibroblasts and umbilical endothelial cells. Our results support the view that the levels of WRN, BLM, RTS and RecQL1 are differentially up-regulated to guarantee genomic stability in cells that are transformed or actively proliferating.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 50 print issues and online access
$259.00 per year
only $5.18 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Abb J, Bayliss GJ and Deinhardt F. . 1979 J. Immunol. 122: 1639–1642.
Amanuma K and Mitsui Y. . 1991 Biochim. Biophys. Acta. 1092: 336–340.
Balajee AS, Machwe A, May A, Gray MD, Oshima J, Martin GM, Nehlin JO, Brosh R, Orren DK and Bohr VA. . 1999 Mol. Biol. Cell. 10: 2655–2668.
Bertoglio JH. . 1983 J. Immunol. 131: 2279–2281.
Brosh Jr. RM, Orren DK, Nehlin JO, Ravn PH, Kenny MK, Machwe A and Bohr VA. . 1999 J. Biol. Chem. 274: 18341–18350.
Brosh J, Li JL, Kenny MK, Karow JK, Cooper MP, Kureekattil RP, Hickson ID and Bohr VA. . 2000 J. Biol. Chem. 275: 23500–23508.
Castagna M, Takai Y, Kaibuchi K, Sano K, Kikkawa U and Nishizuka Y. . 1982 J. Biol. Chem. 257: 7847–7851.
Clevers HC, Versteegen JM, Logtenberg T, Gmelig-Meyling FH and Ballieux RE. . 1985 J. Immunol. 135: 3827–3830.
Cooper MP, Machwe A, Orren DK, Brosh RM, Ramsden D and Bohr VA. . 2000 Genes Dev. 14: 907–912.
Courcelle J and Hanawalt PC. . 1999 Mol. Gen. Genet. 262: 543–551.
Egeler RM, de Kraker J, Slater R and Purtilo DT. . 1992 Cancer 70: 683–687.
Ellis NA, Groden J, Ye TZ, Straughen J, Lennon DJ, Ciocci S, Proytcheva M and German J. . 1995 Cell 83: 655–666.
Ellis NA, Proytcheva M, Sanz MM, Ye TZ and German J. . 1999 Am. J. Hum. Genet. 65: 1368–1374.
German J. . 1993 Medicine (Baltimore) 72: 393–406.
Goto M, Miller RW, Ishikawa Y and Sugano H. . 1996 Cancer Epidemiol Biomarkers Prev 5: 239–246.
Goto M, Yamabe M, Shiratori M, Okada M, Kawabe T, Matsumoto T, Sugimoto M and Furuichi Y. . 1999 Human Genetics 105: 301–307.
Hanaoka F, Yamada M, Takeuchi F, Goto M, Miyamoto T and Hori T. . 1985 Adv. Exp. Med. Biol. 190: 439–457.
Huang RP, Fan Y, Ni Z, Mercola D and Adamson ED. . 1997 J. Cell. Biochem. 66: 489–499.
Ide T, Tsuji Y, Ishibashi S and Mitsui Y. . 1983 Exp. Cell. Res. 143: 343–349.
Ide T, Tsuji Y, Nakashima T and Ishibashi S. . 1984 Exp. Cell. Res. 321–328.
Kamath-Loeb AS, Johansson E, Burgers PM and Loeb LA. . 2000 Proc. Natl. Acad. Sci. USA 97: 4603–4608.
Kataoka H, Tahara H, Watanabe T, Sugawara M, Ide T, Goto M, Furuichi Y and Sugimoto M. . 1997 Differentiation 62: 203–211.
Kitao S, Lindor NM, Shiratori M, Furuichi Y and Shimamoto A. . 1999a Genomics 61: 268–276.
Kitao S, Ohsugi I, Ichikawa K, Goto M, Furuichi Y and Shimamoto A. . 1998 Genomics 54: 443–452.
Kitao S, Shimamoto A, Goto M, Miller RW, Smithson WA, Lindor NM and Furuichi Y. . 1999b Nat. Genet. 22: 82–84.
Kuchino T and Yamaguchi N. . 1975 J. Virol. 15: 1302–1307.
Lebel M, Spillare EA, Harris CC and Leder P. . 1999 J. Biol. Chem. 274: 37795–37799.
Lindor NM, Devries EM, Michels VV, Schad CR, Jalal SM, Donovan KM, Smithson WA, Kvols LK, Thibodeau SN and Dewald GW. . 1996 Clin. Genet. 49: 124–129.
Lohman TM. . 1993 J. Biol. Chem. 268: 2269–2272.
Marciniak RA, Lombard DB, Johnson FB and Guarente L. . 1998 Proc. Natl. Acad. Sci. USA 95: 6887–6892.
Matsumoto T, Imamura O, Yamabe Y, Kuromitsu J, Tokutake Y, Shimamoto A, Suzuki N, Satoh M, Kitao S, Ichikawa K, Kataoka H, Sugawara K, Thomas W, Mason B, Tsuchihashi Z, Drayna D, Sugawara M, Sugimoto M, Furuichi Y and Goto M. . 1997 Hum. Genet. 100: 123–130.
Matsuo M, Kaji K, Utakoji T and Hosoda K. . 1982 J. Gerontol. 37: 33–37.
Miller G. . 1990 Virology. Fields BN aK, KM (ed.) Raven Press: New York pp. 1921–1958.
Moser MJ, Kamath-Loeb AS, Jacob JE, Bennett SE, Oshima J and Monnat Jr. RJ. . 2000 Nucleic. Acids Res. 28: 648–654.
Nakayama H, Nakayama K, Nakayama R, Irino N, Nakayama Y and Hanawalt PC. . 1984 Mol. Gen. Genet. 195: 474–480.
Neff NF, Ellis NA, Ye TZ, Noonan J, Huang K, Sanz M and Proytcheva M. . 1999 Mol. Biol. Cell. 10: 665–676.
Puranam KL and Blackshear PJ. . 1994 J. Biol. Chem. 269: 29838–29845.
Salk D, Au K, Hoehn H and Martin GM. . 1985 Ad. Exp. Med. Biol. 190: 541–546.
Schulz VP, Zakian VA, Ogburn CE, McKay J, Jarzebowicz AA, Edland SD and Martin GM. . 1996 Hum. Genet. 97: 750–754.
Seki M, Miyazawa H, Tada S, Yanagisawa J, Yamaoka T, Hoshino S, Ozawa K, Eki T, Nogami M, Okumura K, Taguchi H, Hanaoka F and Enomoto T. . 1994 Nucleic. Acids Res. 22: 4566–4573.
Shimamoto A, Nishikawa K, Kitao S and Furuichi Y. . 2000 Nucleic. Acids Res. 28: 1647–1655.
Shiratori M, Sakamoto S, Suzuki N, Tokutake Y, Kawabe Y, Enomoto T, Sugimoto M, Goto M, Matsumoto T and Furuichi Y. . 1999 J. Cell. Biol. 144: 1–9.
Sinclair DA and Guarente L. . 1997 Cell 91: 1033–1042.
Sinclair DA, Millis K and Guarente L. . 1997 Science 277: 1313–1316.
Spender LC, Cannell EJ, Hollyoake M, Wensing B, Gawn JM, Brimmell M, Packham G and Farrell PJ. . 1999 J. Virol. 73: 4678–4688.
Spillare EA, Robles AI, Wang XW, Shen JC, Yu CE, Schellenberg GD and Harris CC. . 1999 Genes Dev. 13: 1355–1360.
Stewart E, Chapman CR, Al-Khodairy F, Carr AM and Enoch T. . 1997 Embo. J. 16: 2682–2692.
Suzuki N, Shimamoto A, Imamura O, Kuromitsu J, Kitao S, Goto M and Furuichi Y. . 1997 Nucleic. Acids Res. 25: 2973–2978.
Suzuki N, Shiratori M, Goto M and Furuichi Y. . 1999 Nucleic. Acids Res. 27: 2361–2368.
Tada S, Yanagisawa J, Sonoyama T, Miyajima A, Seki M, Ui M and Enomoto T. . 1996 Cell. Struct. Funct. 21: 123–132.
Tahara H, Sato E, Noda A and Ide T. . 1995 Oncogene 10: 835–840.
Tahara H, Tokutake Y, Maeda S, Kataoka H, Watanabe T, Satoh M, Matsumoto T, Sugawara M, Ide T, Goto M, Furuichi Y and Sugimoto M. . 1997 Oncogene 15: 1911–1920.
Tsuyama N, Miura M, Kitahira M, Ishibashi S and Ide T. . 1991 Cell. Struct. Funct. 16: 55–62.
Umezu K and Nakayama H. . 1993 J. Mol. Biol. 230: 1145–1150.
Umezu K, Nakayama K and Nakayama H. . 1990 Proc. Natl. Acad. Sci. USA 87: 5363–5367.
Wu L, Davies SL, North PS, Goulaouic H, Riou JF, Turley H, Gatter KC and Hickson ID. . 2000 J. Biol. Chem. 275: 9636–9644.
Yamabe Y, Shimamoto A, Goto M, Yokota J, Sugawara M and Furuichi Y. . 1998 Mol. Cell. Biol. 18: 6191–6200.
Yamagata K, Kato J, Shimamoto A, Goto M, Furuichi Y and Ikeda H. . 1998 Proc. Natl. Acad. Sci. USA 95: 8733–8738.
Yamaguchi N and Kuchino T. . 1975 J. Virol. 15: 1297–1301.
Yu CE, Oshima J, Fu YH, Wijsman EM, Hisama F, Alisch R, Matthews S, Nakura J, Miki T, Ouais S, Martin GM, Mulligan J and Schellenberg GD. . 1996 Science 272: 258–262.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Kawabe, T., Tsuyama, N., Kitao, S. et al. Differential regulation of human RecQ family helicases in cell transformation and cell cycle. Oncogene 19, 4764–4772 (2000). https://doi.org/10.1038/sj.onc.1203841
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/sj.onc.1203841
Keywords
This article is cited by
-
RecQL4-Aurora B kinase axis is essential for cellular proliferation, cell cycle progression, and mitotic integrity
Oncogenesis (2018)
-
The level of RECQL1 expression is a prognostic factor for epithelial ovarian cancer
Journal of Ovarian Research (2014)
-
Replication stress induces specific enrichment of RECQ1 at common fragile sites FRA3B and FRA16D
Molecular Cancer (2013)
-
DNA helicases involved in DNA repair and their roles in cancer
Nature Reviews Cancer (2013)
-
The human RECQ1 helicase is highly expressed in glioblastoma and plays an important role in tumor cell proliferation
Molecular Cancer (2011)