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Division of Gastroenterology, Department of Internal Medicine, University of Michigan Medical School, Ann Arbor, Michigan 48109-0586 [M. T. H., J. M. C., G. M., C. R. B., M. K.]; Gastroenterology Section, Veteran's Affairs Medical Center, Ann Arbor, MI 48105-2399 [M. T. H., J. M. C., G. M., C. R. B., M. K.]; and Laboratories of Molecular Carcinogenesis [M. K.] and Molecular Genetics [A. U., T. A. K.], National Institute of Environmental Health Sciences, Research Triangle Park, NC 27709
The human colon tumor cell line HCT116 is deficient in wild-type hMLH1, is defective in mismatch repair (MMR), exhibits microsatellite instability, and is tolerant to N-methyl-N'-nitro-N-nitrosoguanidine (MNNG). Transferring a normal copy of hMLH1 on chromosome 3 into the cell line restores MMR activity, stabilizes microsatellite loci, and increases the sensitivity of the cell to MNNG. Previous studies in other cell lines tolerant to alkylating agents such as MNNG or N-methylnitrosourea have shown cross-tolerance to 6-thioguanine (6TG), leading to a hypothesis that tolerance to MNNG or 6TG may be the result of MMR deficiency. To test this hypothesis, we studied the effects of 6TG on the MNNG-tolerant, MMR-deficient HCT116 cell line and its MNNG-sensitive, MMR-proficient, MNNG-tolerant, and MMR-deficient derivatives. Continuous exposure to low doses of 6TG (0.31–1.25 µg/ml) had no apparent effect on colony-forming ability (CFA) in MNNG-tolerant, MMR-deficient cells, whereas MNNG-sensitive, MMR-proficient cells exhibited a dose-dependent decrease in CFA. Growth kinetics and cell cycle analysis revealed that the growth of 6TG-treated HCT116+chr3 cells was arrested at G2 after exposure to low dose of 6TG. In contrast, the same exposure to 6TG did not induce G2 arrest but rather a G1 delay in HCT116 and HCT116+chr2. To obtain further evidence for the role of MMR on 6TG and MNNG toxicity, we isolated an MNNG-resistant revertant clone, M2, from the MNNG-sensitive, MMR-proficient HCT116+chr3 cell line and characterized the MMR activity, hMLH1 status, and 6TG response. The results showed that M2 cells lost MMR activity as well as the previously introduced normal hMLH1 gene. Restoration of the CFA of M2 and an absence of G2 arrest were observed after treatment with low doses of 6TG. These results suggest that the mismatch repair system interacts with the G2 checkpoint in response to 6TG or MNNG-induced DNA lesions. The results further suggest that any agent that induces DNA mispairs will cause G2 arrest in MMR-proficient cells but not in MMR-deficient cells.
1 This work was partly supported by NIH Grant CA39233, the University of Michigan Cancer Center Grant CA46592, the Johnson Family Fund for Familial Colorectal Cancer, National Cancer Institute Grant R25 CA57716, the James Lind Scholarship, and the National Institute of Environmental Health Sciences.
2 To whom requests for reprints should be addressed, at University of Michigan Medical Center, Department of Internal Medicine, 4410 Keesge III, 200 Zina Pitcher Place, Ann Arbor, MI 48109-0586.
Received 5/31/95. Accepted 7/21/95.
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M. J. Longley, A. J. Pierce, and P. Modrich DNA Polymerase delta Is Required for Human Mismatch Repair in Vitro J. Biol. Chem., April 18, 1997; 272(16): 10917 - 10921. [Abstract] [Full Text] [PDF]
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L. Narayanan, J. A. Fritzell, S. M. Baker, R. M. Liskay, and P. M. Glazer Elevated levels of mutation in multiple tissues of mice deficient in the DNA mismatch repair gene Pms2 PNAS, April 1, 1997; 94(7): 3122 - 3127. [Abstract] [Full Text] [PDF]
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J. T. Drummond, A. Anthoney, R. Brown, and P. Modrich Cisplatin and Adriamycin Resistance Are Associated with MutLalpha and Mismatch Repair Deficiency in an Ovarian Tumor Cell Line J. Biol. Chem., August 16, 1996; 271(33): 19645 - 19648. [Abstract] [Full Text] [PDF]
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R Kolodner Biochemistry and genetics of eukaryotic mismatch repair. Genes & Dev., June 15, 1996; 10(12): 1433 - 1442. [PDF]
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M. Berardini, A. Mazurek, and R. Fishel The Effect of O6-Methylguanine DNA Adducts on the Adenosine Nucleotide Switch Functions of hMSH2-hMSH6 and hMSH2-hMSH3 J. Biol. Chem., September 1, 2000; 275(36): 27851 - 27857. [Abstract] [Full Text] [PDF]
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