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Cell Growth and Development

Extracellular Signal-Regulated Kinase Activates Topoisomerase IIα through a Mechanism Independent of Phosphorylation

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Pages 3551-3560 | Received 19 Oct 1998, Accepted 16 Feb 1999, Published online: 28 Mar 2023

REFERENCES

  • Ackerman, P., C. V. C. Glover, and J. Osheroff 1985. Phosphorylation of DNA topoisomerase II by casein kinase II: modulation of eukaryotic topoisomerase II activity in vitro. Proc. Natl. Acad. Sci. USA 82:3164–3168.
  • Andreassen, P., F. B. Lacroix, and J. Margolis 1997. Chromosomes with two intact axial cores are induced by G2 checkpoint override: evidence that DNA decatenation is not required to template the chromosome structure. J. Cell Biol. 136:29–43.
  • Beno, W. R., L. M. Brady, M. Bissonnette, and J. Davis 1995. Protein kinase C and mitogen-activated protein kinase are required for 1,25-dihydroxy vitamin D3-stimulated Egr induction. J. Biol. Chem. 270:3642–3647.
  • Bojanowski, K., O. Filhol, C. Cochet, E. M. Chambaz, and J. Larsen 1993. DNA topoisomerase II and casein kinase II associate in a molecular complex that is catalytically active. J. Biol. Chem. 268:22920–22926.
  • Brunet, A., G. Pagès, and J. Pouysségur 1994. Constitutively active mutants of MAP kinase kinase (MEK1) induce growth factor relaxation and oncogenicity when expressed in fibroblasts. Oncogene 9:3379–3387.
  • Burden, D. A., and J. Sullivan 1994. Phosphorylation of the α- and β-isoforms of DNA topoisomerase II is qualitatively different in interphase and mitosis in Chinese hamster ovary cells. Biochemistry 33:14651–14655.
  • Burden, D. A., and J. Osherhoff 1998. Mechanism of action of eukaryotic topoisomerase II and drugs targeted to the enzyme. Biochim. Biophys. Acta 1400:139–154.
  • Cardenas, M. E., Q. Dang, C. V. C. Glover, and J. Gasser 1992. Casein kinase II phosphorylates the eukaryote-specific C-terminal domain of topoisomerase II in vivo. EMBO J. 11:1785–1796.
  • Corbett, A. H., R. F. DeVore, and J. Osheroff 1992. Effect of casein kinase II-mediated phosphorylation on the catalytic cycle of topoisomerase II. J. Biol. Chem. 267:20513–20518.
  • Corbett, A. H., A. W. Fernald, and J. Osheroff 1993. Protein kinase C modulates the catalytic activity of topoisomerase II by enhancing the rate of ATP hydrolysis: evidence for a common mechanism of regulation by phosphorylation. Biochemistry 32:2090–2097.
  • Cowley, S., H. Paterson, P. Kemp, and J. Marshall 1994. Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 77:841–852.
  • Denko, N. C., A. J. Giaccia, J. R. Stringer, and J. Stambrook 1994. The human Ha-ras oncogene induces genomic instability in murine fibroblasts within one cell cycle. Proc. Natl. Acad. Sci. USA 91:5124–5128.
  • DeVore, R. F., A. H. Corbett, and J. Osheroff 1992. Phosphorylation of topoisomerase II by casein kinase II and protein kinase C: effects on enzyme-mediated DNA cleavage/religation and sensitivity to the antineoplastic drugs etoposide and 4′-(9′-acridinylamino)methane-sulfon- m -anisidide. Cancer Res. 52:2156–2161.
  • DiNardo, S., K. Voelkel, and J. Sternglanz 1984. DNA topoisomerase II mutant of Saccharomyces cerevisiae: topoisomerase II is required for segregation of daughter molecules at the termination of DNA replication. Proc. Natl. Acad. Sci. USA 81:2616–2620.
  • Downes, C. S., D. J. Clarke, A. M. Mullinger, J. F. Giménez-Ablán, A. M. Creighton, and J. Johnson 1994. A topoisomerase II-dependent G2 cycle checkpoint in mammalian cells. Nature 372:467–470.
  • Earnshaw, W. C., and J. MacKay 1994. Role of nonhistone proteins in the chromosomal events of mitosis. FASEB J. 8:947–956.
  • Englund, P. T. 1978. The replication of kinetoplast DNA networks in Crithidia fasciculata. Cell 14:157–168.
  • Froelich-Ammon, S. J., and J. Osheroff 1995. Topoisomerase poisons: harnessing the dark side of enzyme mechanism. J. Biol. Chem. 270:21429–21432.
  • Fukasawa, K., and J. Vande Woude 1997. Synergy between the Mos/mitogen-activated protein kinase pathway and loss of p53 function in transformation and chromosome instability. Mol. Cell. Biol. 17:506–518.
  • Heck, M. M. S., W. N. Hittelman, and J. Earnshaw 1989. In vivo phosphorylation of the 170-kDa form of eukaryotic DNA topoisomerase II. J. Biol. Chem. 264:15161–15164.
  • Isaacs, R. J., S. L. Davies, M. I. Sandri, C. Redwood, N. J. Wells, and J. Hickson 1998. Physiological regulation of eukaryotic topoisomerase II. Biochim. Biophys. Acta 1400:121–137.
  • Ishida, R., M. Hamatake, R. A. Wasserman, J. L. Nitiss, J. C. Wang, and J. Andoh 1995. DNA topoisomerase II is a molecular target of bisdioxopiperazine derivatives ICRF-159 and ICRF-193 in Saccharomyces cerevisiae. Cancer Res. 55:2299–2303.
  • Khokhlatchev, A. V., B. Canagarajah, J. Wilsbacher, M. Robinson, M. Atkinson, E. Goldsmith, and J. Cobb 1998. Phosphorylation of the MAP kinase ERK2 promotes its homodimerization and nuclear translocation. Cell 93:605–615.
  • Khosravi-Far, R., P. A. Solski, G. J. Clark, M. S. Kinch, and J. Der 1995. Activation of Rac1, RhoA, and mitogen-activated protein kinases is required for Ras transformation. Mol. Cell. Biol. 15:6443–6453.
  • Kimura, K., M. Saijo, M. Ui, and J. Enomoto 1994. Identification of the nature of modification that causes the shift of DNA topoisomerase IIβ to apparent higher molecular weight forms in the M phase. J. Biol. Chem. 269:24523–24526.
  • Kimura, K., M. Saijo, M. Tanaka, and J. Enomoto 1996. Phosphorylation-independent stimulation of DNA topoisomerase IIα activity. J. Biol. Chem. 271:10990–10995.
  • Kimura, K., N. Nozaki, T. Enomoto, M. Tanaka, and J. Kikuchi 1996. Analysis of M phase-specific phosphorylation of DNA topoisomerase II. J. Biol. Chem. 271:21439–21445.
  • Kingma, P. S., C. A. Greider, and J. Osheroff 1997. Spontaneous DNA lesions poison human topoisomerase IIα and stimulate cleavage proximal to leukemic 11q23 chromosomal breakpoints. Biochemistry 36:5934–5939.
  • Koo, H.-M., A. Monks, A. Mikheev, L. V. Rubinstein, M. Gray-Goodrich, M. J. McWilliams, W. G. Alvord, H. K. Oie, A. F. Gazdar, K. D. Paull, H. Zarbl, and J. Vande Woude 1996. Enhanced sensitivity to 1-β-d-arabinosfuranosylcytosine and topoisomerase II inhibitors in tumor cell lines harboring activated ras oncogenes. Cancer Res. 56:5211–5216.
  • Kortenjann, M., O. Thomae, and J. Shaw 1994. Inhibition of v-raf-dependent c-fos expression and transformation by a kinase-defective mutant of the mitogen-activated protein kinase Erk2. Mol. Cell. Biol. 14:4815–4824.
  • Lavoie, J. N., G. L’Allemain, A. Brunet, R. Muller, and J. Pouysségur 1996. Cyclin D1 expression is regulated positively by p42/p44mapk and negatively by the p38/HOGmapk pathway. J. Biol. Chem. 271:20608–20616.
  • Lenormand, P., J. M. Brondello, A. Brunet, and J. Pouyssegur 1998. Growth factor-induced p42/p44 MAPK nuclear translocation and retention requires both MAPK activation and neosynthesis of nuclear anchoring proteins. J. Cell Biol. 142:625–633.
  • Lewis, T. S., P. S. Shapiro, and J. Ahn 1998. Signal transduction through MAP kinase cascades. Adv. Cancer Res. 74:49–139.
  • Luke, M., and J. Bogenhagen 1989. Quantitation of type II topoisomerase in oocytes and eggs of Xenopus laevis. Dev. Biol. 136:459–468.
  • Mansour, S. J., J. M. Candia, J. E. Matsuura, M. C. Manning, and J. Ahn 1996. Interdependent domains controlling the enzymatic activity of mitogen-activated protein kinase kinase 1. Biochemistry 35:15529–15536.
  • Mansour, S. J., W. T. Matten, A. S. Hermann, J. M. Candia, S. Rong, K. Fukasawa, G. F. Vande Woude, and J. Ahn 1994. Transformation of mammalian cells by constitutively active MAP kinase kinase. Science 265:966–970.
  • Mansour, S. J., K. A. Resing, J. M. Candia, A. S. Hermann, J. W. Gloor, K. R. Herskind, M. Wartmann, R. J. Davis, and J. Ahn 1994. Mitogen-activated protein (MAP) kinase phosphorylation of MAP kinase kinase: determination of phosphorylation sites by mass spectrometry and site-directed mutagenesis. J. Biochem. 116:304–314.
  • Meyer, K. N., E. Kjelden, T. Straub, B. R. Knudsen, I. D. Hickson, A. Kikuchi, H. Kreipe, and J. Boege 1997. Cell cycle-coupled relocation of types I and II topoisomerases and modulation of catalytic enzyme activities. J. Cell Biol. 136:755–788.
  • Nitiss, J. L. 1998. Investigating the biological functions of DNA topoisomerases in eukaryotic cells. Biochim. Biophys. Acta 1400:63–81.
  • Osheroff, N., E. R. Shelton, and J. Brutlag 1983. DNA topoisomerase II from Drosophila melanogaster. J. Biol. Chem. 258:9536–9543.
  • Qiu, R. G., J. Chen, D. Kirn, F. McCormick, and J. Symons 1995. An essential role for Rac in Ras transformation. Nature 374:457–459.
  • Rattner, J. B., M. J. Hendzel, C. S. Furbee, M. T. Muller, and J. Bazett-Jones 1996. Topoisomerase IIα is associated with the mammalian centromere in a cell cycle- and species-specific manner and is required for proper centromere/kinetochore structure. J. Cell Biol. 134:1097–1107.
  • Redwood, C., S. L. Davies, N. J. Wells, A. M. Fry, and J. Hickson 1998. Casein kinase II stabilizes the activity of human topoisomerase IIα in a phosphorylation-independent manner. J. Biol. Chem. 273:3635–3642.
  • Rodriguez-Viciana, P., P. H. Warne, A. Khwaja, B. M. Marte, D. Pappin, P. Das, M. D. Waterfield, A. Ridley, and J. Downward 1997. Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytokeleton by ras. Cell 89:457–467.
  • Sahyoun, N., M. Wolf, J. Besterman, T.-S. Hsieh, M. Sander, H. LeVine III, K.-J. Chang, and J. Cuatrecasas 1986. Protein kinase C phosphorylates topoisomerase II: topoisomerase activation and its possible role in phorbol ester-induced differentiation of HL-60 cells. Proc. Natl. Acad. Sci. USA 83:1603–1607.
  • Saijo, M., M. Ui, and J. Enomoto 1992. Growth state and cell cycle dependent phosphorylation of DNA topoisomerase II in Swiss 3T3 cells. Biochemistry 31:359–363.
  • Saitoh, Y., and J. Laemmli 1994. Metaphase chromosome structure: bands arise from a differential folding path of the highly AT-rich scaffold. Cell 76:609–622.
  • Shapiro, P. S., E. Vaisberg, A. J. Hunt, N. S. Tolwinski, A. M. Whalen, J. R. McIntosh, and J. Ahn 1998. Activation of the MKK/ERK pathway during somatic cell mitosis. Direct interactions of active ERK with kinetochores and regulation of the mitotic 3F3/2 phosphoantigen. J. Cell Biol. 142:1533–1545.
  • Shelton, E. R., N. Osheroff, and J. Brutlag 1983. DNA topoisomerase II from Drosophila melanogaster. J. Biol. Chem. 258:9530–9535.
  • Sif, S., P. T. Stukenberg, M. W. Kirschner, and J. Kingston 1998. Mitotic inactivation of a human SWI/SNF chromatin remodeling complex. Genes Dev. 12:2842–2851.
  • Taagepera, S., P. N. Rao, F. H. Drake, and J. Gorbsky 1993. DNA topoisomerase IIα is the major chromosome protein recognized by the mitotic phosphoprotein antibody MPM-2. Proc. Natl. Acad. Sci. USA 90:8407–8411.
  • Traverse, S., N. Gomez, H. Paterson, C. Marshall, and J. Cohen 1992. Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Comparison of the effects of nerve growth factor and epidermal growth factor. Biochem. J. 288:351–355.
  • Vassetzky, Y. S., Q. Dang, P. Benedetti, and J. Gasser 1994. Topoisomerase II forms multimers in vitro: effects of metals, β-glycerophosphate, and phosphorylation of its C-terminal domain. Mol. Cell. Biol. 14:6962–6974.
  • Vouret-Craviari, V., E. Van Obberghen-Schilling, J. C. Scimeca, E. Van Obberghen, and J. Pouysségur 1993. Differential activation of p44mapk (ERK1) by alpha-thrombin and thrombin-receptor peptide agonist. Biochem. J. 289:209–214.
  • Wang, J. C. 1996. DNA topoisomerases. Annu. Rev. Biochem. 65:635–692.
  • Wells, N. J., C. M. Addison, A. M. Fry, R. Ganapathi, and J. Hickson 1994. Serine 1524 is a major site of phosphorylation on human topoisomerase IIα protein in vivo and is a substrate for casein kinase II in vitro. J. Biol. Chem. 269:29746–29751.
  • Wells, N. J., and J. Hickson 1995. Human topoisomerase IIα is phosphorylated in a cell-cycle phase-dependent manner by a proline-directed kinase. Eur. J. Biochem. 231:491–497.
  • Whalen, A. M., S. C. Galasinski, P. S. Shapiro, T. S. Nahreini, and J. Ahn 1997. Megakaryocytic differentiation induced by constitutive activation of mitogen-activated protein kinase kinase. Mol. Cell Biol. 17:1947–1958.
  • Wright, J. H., E. Munar, P. Andreassen, R. Margolis, R. Seger, and E. G. Krebs. Unpublished data.
  • Zecevic, M., A. D. Catling, S. T. Eblen, L. Renzi, J. C. Hittle, T. J. Yen, G. J. Gorbsky, and J. Weber 1998. Active MAP kinase in mitosis: localization at kinetochores and association with the motor protein CENP-E. J. Cell Biol. 142:1547–1558.

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