The p38 Mitogen-Activated Protein Kinase Pathway Links the DNA Mismatch Repair System to the G₂ Checkpoint and to Resistance to Chemotherapeutic DNA-Methylating Agents

REFERENCES

• Adamson, A. W., W.-J. Kim, S. Shangary, R. Baskaran, and K. D. Brown. 2002. ATM is activated in response to N-methyl-N′-nitro-N-nitrosoguanidine-induced DNA alkylation. J. Biol. Chem. 277: 38222–38229.
   PubMed Web of Science ®Google Scholar
• Baudhuin, L. M., K. L. Christina, J. Lu, and Y. Xu. 2002. Akt activation induced by lysophosphatidic acid and sphingosine-1-phosphate requires both mitogen-activated protein kinase and p38 mitogen-activated protein kinase and is cell-line specific. Mol. Pharmacol. 62: 660–671.
   PubMedGoogle Scholar
• Bellacosa, A. 2001. Functional interactions and signaling properties of mammalian DNA mismatch repair proteins. Cell Death Differ. 8: 1076–1092.
   PubMed Web of Science ®Google Scholar
• Bignami, M., M. O'Driscoll, G. Aquilina, and P. Karan. 2000. Unmasking a killer: DNA O6-methylguanine and the cytotoxicity of methylating agents. Mutat. Res. 462: 71–82.
   PubMed Web of Science ®Google Scholar
• Bleehen, N. M., E. S. Newlands, S. M. Lee, N. Thatcher, P. Selby, A. H. Calvert, G. J. Rustin, M. Brampton, and M. F. Stevens. 1995. Cancer research campaign phase II trial of temozolomide in metastatic melanoma. J. Clin. Oncol. 13: 910–913.
   PubMed Web of Science ®Google Scholar
• Branch, P., R. Hampson, and P. Karran. 1995. DNA mismatch repair binding defects, DNA damage tolerance and mutator phenotypes on human colorectal carcinoma cell lines. Cancer Res. 55: 2304–2309.
   PubMed Web of Science ®Google Scholar
• Branch, P., G. Aquilina, M. Bignami, and P. Karran. 1993. Defective mismatch binding and a mutator phenotype in cells tolerant to DNA damage. Nature 362: 652–654.
   PubMed Web of Science ®Google Scholar
• Brown, K. D., A. Rathi, R. Kamath, D. I. Beardsley, Q. Zhan, J. Mannino, and R. Baskaran. 2003. The mismatch repair system is required for S-phase checkpoint activation. Nat. Genet. 33: 80–84.
   PubMedGoogle Scholar
• Bulavin, D. V., Y. Higashimoto, I. J. Popoff, W. A. Gaarde, V. Basrur, O. Potapova, E. Appella, and A. J. Fornace, Jr. 2001. Initiation of a G2/M checkpoint after ultraviolet radiation requires p38 kinase. Nature 411: 102–107.
   PubMed Web of Science ®Google Scholar
• Chan, T. A., H. Hermeking, C. Lengauer, K. W. Kinzler, and B. Vogelstein. 1999. 14-3-3 sigma is required to prevent mitotic catastrophe after DNA damage. Nature 401: 616–620.
   PubMed Web of Science ®Google Scholar
• Conejo, R., C. de Alvaro, M. Benito, A. Cuadrado, and M. Lorenzo. 2002. Insulin restores differentiation of Ras-transformed C2C12 myoblasts by inducing NF-kappaB through an AKT/P70S6K/p38-MAPK pathway. Oncogene 21: 3739–3753.
   PubMed Web of Science ®Google Scholar
• D'Atri, S., D. Piccioni, A. Castellano, V. Tuorto, A. Franchi, K. Lu, N. Christiansen, S. Frankel, Y. M. Rustum, G. Papa, F. Mandelli, and E. Bonmasser. 1995. Chemosensitivity to triazine compounds and O6-alkylguanine-DNA-alkyltransferase levels: studies with blasts of leukemic patients. Ann. Oncol. 6: 389–393.
   PubMed Web of Science ®Google Scholar
• D'Atri, S., L. Tentori, P. M. Lacal, G. Graziani, E. Pagani, E. Benincasa, G. Zambruno, E. Bonmassar, and J. Jiricny. 1998. Involvement of the mismatch repair system in temozolomide-induced apoptosis. Mol. Pharmacol. 54: 334–341.
   PubMed Web of Science ®Google Scholar
• Davies, S. P., H. Reddy, M. Caivano, and P. Cohen. 2000. Specificity and mechanism of actions of some commonly used protein kinase inhibitors. Biochem. J. 351: 95–105.
   PubMed Web of Science ®Google Scholar
• Denny, B. J., R. T. Wheelhouse, M. F. G. Stevens, L. H. Tsang, and J. A. Slack. 1994. NMR and molecular modeling investigation of the mechanism of activation of the antitumor drug temozolomide and its interaction with DNA. Biochemistry 33: 9045–9051.
   PubMed Web of Science ®Google Scholar
• Dimri, G. P., X. Lee, G. Basile, M. Acosta, G. Scott, C. Rocskelley, E. E. Medrano, M. Linskens, I. Rubelj, O. Pereira-Smith, M. Peacocke, and J. Campisi. 1995. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 92: 9363–9367.
   PubMed Web of Science ®Google Scholar
• Drummond, J. T., G. M. Li, M. J. Longley, and P. Modrich. 1995. Isolation of an hMSH2-p160 heterodimer that restores DNA mismatch repair to tumor cells. Science 268: 1909–1912.
   PubMed Web of Science ®Google Scholar
• Enslen, H., J. Raingeaud, and R. J. Davis. 1998. Selective activation of p38 mitogen-activated protein (MAP) kinase isoforms by the MAP kinase kinases MKK3 and MKK6. J. Biol. Chem. 273: 1741–1748.
   PubMed Web of Science ®Google Scholar
• Furnari, B., N. Rhind, and P. Russell. 1997. Cdc25 mitotic inducer targeted by chk1 DNA damage checkpoint kinase. Science 277: 1495–1497.
   PubMed Web of Science ®Google Scholar
• Goldmacher, V. S., R. A. Cuzick, and W. G. Thilly. 1986. Isolation and partial characterization of human cell mutants differing in sensitivity to killing and mutation by methylnitrosourea and N-methyl-N′-nitro-N-nitrosoguanidine. J. Biol. Chem. 261: 12462–12471.
   PubMedGoogle Scholar
• Hawn, M. T., A. Umar, J. M. Carethers, T. A. Kunkel, C. R. Boland, and M. Koi. 1995. Evidence for a connection between the mismatch repair system and the G2 cell cycle checkpoint. Cancer Res. 55: 3721–3725.
   PubMed Web of Science ®Google Scholar
• Heinen, C. D., C. Schmutte, and R. Fishel. 2002. DNA repair and tumorigenesis: lessons from hereditary cancer syndromes. Cancer Biol. Ther. 1: 477–485.
   PubMed Web of Science ®Google Scholar
• Hirose, Y., S. Berger, and R. O. Pieper. 2001. p53 affects both the duration of G2/M arrest and the fate of temozolomide-treated human glioblastoma cells. Cancer Res. 61: 1957–1963.
   PubMed Web of Science ®Google Scholar
• Hirose, Y., M. S. Berger, and R. O. Pieper. 2001. Abrogation of the Chk1-mediated G2 checkpoint pathway potentiates temozolomide-induced toxicity in a p53-independent manner in human glioblastoma cells. Cancer Res. 61: 5843–5849.
   PubMed Web of Science ®Google Scholar
• Hirose, Y., E. L. Kreklau, L. C. Erickson, M. S. Berger, and R. O. Pieper. 2003. Delayed repletion of O6-methylguanine-DNA methyltransferase resulting in failure to protect the human glioblastoma cell line SF767 from temozolomide-induced cytotoxicity. J. Neurosurg. 98: 591–598.
   PubMed Web of Science ®Google Scholar
• Ianzini, F., and M. A. Mackey. 1997. Spontaneous premature chromatin condensation and mitotic catastrophe following irradiation of HeLa S3 cells. Int. J. Radiat. Biol. 72: 409–421.
   PubMed Web of Science ®Google Scholar
• Jean-Claude, B. J., A. Mustafa, A. J. Watson, Z. Damian, D. Vasilescu, T. H. Chan, and B. Leyland-Jones. 1999. Tetrazepinones are equally cytotoxic to Mer+ and Mer− human tumor cell lines. J. Pharmacol. Exp. Ther. 288: 484–489.
   PubMedGoogle Scholar
• Kanamori, M., H. Kon, T. Nobukuni, S. Nomura, K. Sugano, S. Mashiyama, T. Kumabe, T. Yoshimoto, M. Meuth, T. Sekiya, and Y. Murakami. 2000. Microsatellite instability and PTEN 1 gene mutation in a subset of early onset gliomas carrying germline mutation or promoter methylation of the hMLH1 gene. Oncogene 19: 1564–1571.
   PubMed Web of Science ®Google Scholar
• Kandel, E. S., J. Skeen, N. Majewski, A. Di Cristofano, P. P. Pandolfi, C. S. Feliciano, A. Gartel, and N. Hay. 2002. Activation of Akt/protein kinase B overcomes a G2/M cell cycle checkpoint induced by DNA damage. Mol. Cell. Biol. 22: 7831–7841.
   PubMed Web of Science ®Google Scholar
• Karran, P., and M. G. Marinus. 1982. Mismatch correction at O6-methylguanine residues in E. coli DNA. Nature (London) 296: 868–869.
   PubMed Web of Science ®Google Scholar
• Karran, P., and M. Bignami. 1992. Self-destruction and tolerance in resistance of mammalian cells to alkylation damage. Nucleic Acids Res. 20: 2933–2940.
   PubMed Web of Science ®Google Scholar
• Kat, A., W. G. Thilly, W. H. Fang, M. J. Longley, G. M. Li, and P. Modrich. 1993. An alkylation-tolerant, mutator human cell line is deficient in strand-specific mismatch repair. Proc. Natl. Acad. Sci. USA 90: 6424–6428.
   PubMed Web of Science ®Google Scholar
• Koi, M., A. Umar, D. P. Chaudan, S. P. Cherian, J. M. Carethers, T. A. Kunkel, and C. R. Boland. 1994. Human chromosome 3 corrects mismatch repair deficiency and microsatellite instability and reduces N-methyl-N′-nitro-N-nitroguanidine tolerance in colon tumor cells with homozygous hMLH1 mutation. Cancer Res. 54: 4308–4312.
   PubMed Web of Science ®Google Scholar
• Lali, F. V., A. E. Hunt, S. J. Turner, and B. M. J. Foxwell. 2000. The pyridinyl imidazole inhibitor SB203580 blocks phosphoinositide-dependent protein kinase activity, protein kinase B phosphorylation, and retinoblastoma hyperphosphorylation in interleukin-2-stimulated T cells independently of p38 mitogen-activated protein kinase. J. Biol. Chem. 275: 7395–7402.
   PubMed Web of Science ®Google Scholar
• Lee, J. C., S. Kassis, S. Kumar, A. Badger, and J. L. Adams. 1999. p38 mitogen-activated protein kinase inhibitors—mechanisms and therapeutic potentials. Pharmacol. Ther. 82: 389–397.
   PubMed Web of Science ®Google Scholar
• Leung, S. Y., T. L. Chan, L. P. Chung, Y. W. Fan, K. N. Hung, Y. K. Kwok, J. W. Ho, and S. T. Yuen. 1998. Microsatellite instability and mutation of DNA mismatch repair genes in glioma. Am. J. Pathol. 153: 1181–1188.
   PubMedGoogle Scholar
• Liu, L., P. Taverna, C. M. Whitacre, S. Chaterjee, and S. L. Gerson. 1999. Pharmacologic disruption of base excision repair sensitizes mismatch repair-deficient and -proficient colon cancer cells to methylating agents. Clin. Cancer Res. 5: 2908–2917.
   PubMed Web of Science ®Google Scholar
• Liu, Q., S. Guntuku, X.-S. Cui, S. Matsuoka, D. Cortez, K. Tamai, G. Luo, S. Carattini-Rivera, F. DeMayo, A. Bradley, L. A. Donehower, and S. J. Elledge. 2000. Chk1 is an essential kinase that is regulated by Atr and required for the G2/M damage checkpoint. Genes Dev. 14: 1448–1459.
   PubMedGoogle Scholar
• McLaughlin, M. M., S. Kumar, P. C. McDonnell, S. Van Horn, J. C. Lee, G. P. Livi, and P. R. Young. 1996. Identification of mitogen-activated protein (MAP) kinase-activated protein kinase-3, a novel substrate of CSBP p38 MAP kinase. J. Biol. Chem. 271: 8488–8492.
   PubMed Web of Science ®Google Scholar
• Nilsson, I., and I. Hoffman. 2000. Cell cycle regulation by the cdc25 phosphatase family. Prog. Cell Cycle Res. 4: 107–114.
   PubMedGoogle Scholar
• Ono, K., and J. Han. 2000. The p38 signal transduction pathway: activation and function. Cell Signal. 12: 1–13.
   PubMed Web of Science ®Google Scholar
• Palombo, F., I. Iaccarino, E. Nakajima, M. Ikejima, T. Shimada, and J. Jiricny. 1996. hMutS beta, a heterodimer of hMSH2 and hMSH3, binds to insertion/deletion loops in DNA. Curr. Biol. 6: 1181–1184.
   PubMed Web of Science ®Google Scholar
• Pearson, R. G. 1973. Hard and soft acids and bases. Dowden, Hutchinson and Ross, Stroudsburg, Pa.
   Google Scholar
• Pegg, A. E., L. Wiest, R. S. Foote, S., Mitra, and W. Perry. 1983. Purification and properties of O-6-methylguanine-DNA transmethylase for rat liver. J. Biol. Chem. 258: 2327–2333.
   PubMed Web of Science ®Google Scholar
• Pegg, A. E. 1990. Mammalian O-6-alkylguanine-DNA alkyltransferase: regulation and importance in response to alkylating carcinogenic and therapeutic agents. Cancer Res. 50: 6119–6129.
   PubMed Web of Science ®Google Scholar
• Prados, M. D. 2000. Future directions in the treatment of malignant gliomas with temozolomide. Semin. Oncol. 27: 41–46.
   PubMedGoogle Scholar
• Sanchez, Y., C. Wong, R. S. Thoma, R. Richman, Z. Wu, H. Piwnica-Worms, and S. J. Elledge. 1997. Conservation of the chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through cdc25. Science 277: 1497–1501.
   PubMed Web of Science ®Google Scholar
• Silber, J. R., M. S. Bobola, S. Ghatan, A. Blank, D. D. Kolstoe, and M. S. Berger. 1998. O6-methylguanine-DNA-methyltransferase activity in adult gliomas: relation to patient and tumor characteristics. Cancer Res. 58: 1068–1073.
   PubMed Web of Science ®Google Scholar
• Sonoda, Y., T. Ozawa, Y. Hirose, K. D. Aldape, M. McMahon, M. S. Berger, and R. O. Pieper. 2001. Formation of intracranial tumors by genetically modified human astrocytes defines four pathways critical in the development of human anaplastic astrocytomas. Cancer Res. 61: 4956–4960.
   PubMed Web of Science ®Google Scholar
• Stevens, M. F. G., J. A. Hickman, S. P. Langdon, et al. 1987. Antitumor activity and pharmacokinetics in mice of 8-crbamoyl-3-methylimidazo [5,1-d]-1,2,3,5-tetrazin-4(3H)-one (CCRG 81045; M&B 39831), a novel drug with potential as an alternative to dacarbazine. Cancer Res. 47: 5846–5852.
   PubMed Web of Science ®Google Scholar
• Strupp, R., M. Gander, S. Leyvraz, and E. Newlands. 2001. Current and future developments in the use of temozolomide for the treatment of brain tumors. Lancet Oncol. 2: 552–560.
   PubMedGoogle Scholar
• Wang, X., C. H. McGowan, M. Zhao, L. He, J. S. Downey, C. Fearns, Y. Wang, S. Huang, and J. Han. 2000. Involvement of the MKK6-p38 gamma cascade in gamma-radiation-induced cell cycle arrest. Mol. Cell. Biol. 20: 4543–4552.
   PubMed Web of Science ®Google Scholar
• Wang, X. Z., and D. Ron. 1996. Stress-induced phosphorylation and activation of the transcription factor CHOP (GADD153) by p38 MAP kinase. Science 272: 1347–1349.
   PubMed Web of Science ®Google Scholar
• Wolfman, J. C., T. Palmby, C. J. Der, and A. Wolfman. 2002. Cellular N-Ras promotes cell survival by downregulation of Jun N-terminal protein kinase and p38. Mol. Cell. Biol. 22: 1589–1606.
   PubMedGoogle Scholar
• Yung, W. K. A. 2000. Temozolomide in malignant gliomas. Semin. Oncol. 3: 27–34.
   Google Scholar