DNA repair modulates the vulnerability of the developing brain to alkylating agents

DNA Repair

Volumn 8, Issue 3, 2009, Pages 400-412

  Kisby, G E ^a   Olivas, A ^a   Park, T ^a   Churchwell, M ^b   Doerge, D ^b   Samson, L D ^c   Gerson, S L ^d   Turker, M S ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^c Massachusetts Institute of Technology Cambridge   (United States)

^d CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Alkyladenine DNA glycosylase (Aag); Cerebellum; Granule cell; Methylazoxymethanol (MAM); Nitrogen mustard (HN2); O6 Methylguanine methyltransferase (Mgmt)

Indexed keywords

2 CHLOROETHYLAMINE; ALKYLATING AGENT; CHLORMETHINE; DIMETHYL SULFATE; DNA GLYCOSYLTRANSFERASE; METHYLAZOXYMETHANOL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CEREBELLUM; DNA DAMAGE; DNA REPAIR; GRANULE CELL; IN VITRO STUDY; IN VIVO STUDY; MOTOR PERFORMANCE; MOUSE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE; WILD TYPE;

ALKYLATING AGENTS; ANIMALS; CATTLE; CELL SURVIVAL; CEREBELLUM; CHICKENS; DNA; DNA FRAGMENTATION; DNA GLYCOSYLASES; DNA MODIFICATION METHYLASES; DNA REPAIR; DNA REPAIR ENZYMES; ETHYLAMINES; HUMANS; MECHLORETHAMINE; METHYLAZOXYMETHANOL ACETATE; MICE; MOTOR ACTIVITY; NEURONS; SULFURIC ACID ESTERS; TUMOR SUPPRESSOR PROTEINS;

MUS;

EID: 59149098643     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2008.12.002     Document Type: Article

References (63)

1. Wu F.Y., Wu H.D., Yang H.L., Kuo H.W., Ying J.C., Lin C.J., Yang C.C., Lin L.Y., Chiu T.H., and Lai J.S. Associations among genetic susceptibility, DNA damage, and pregnancy outcomes of expectant mothers exposed to environmental tobacco smoke. Sci. Total Environ. 386 (2007) 124-133
2. Ahles T.A., and Saykin A.J. Candidate mechanisms for chemotherapy-induced cognitive changes. Nat. Rev. Cancer 7 (2007) 192-201
3. Butler R.W., and Haser J.K. Neurocognitive effects of treatment for childhood cancer. Ment. Retard. Dev. Disabil. Res. Rev. 12 (2006) 184-191
4. Everson R.B., Randerath E., Santella R.M., Avitts T.A., Weinstein I.B., and Randerath K. Quantitative associations between DNA damage in human placenta and maternal smoking and birth weight. J. Natl. Cancer Inst. 80 (1988) 567-576
5. Tang D., Li T.Y., Liu J.J., Chen Y.H., Qu L., and Perera F. PAH-DNA adducts in cord blood and fetal and child development in a Chinese cohort. Environ. Health Perspect. 114 (2006) 1297-1300
6. Perera F.P., Tang D., Tu Y.H., Cruz L.A., Borjas M., Bernert T., and Whyatt R.M. Biomarkers in maternal and newborn blood indicate heightened fetal susceptibility to procarcinogenic DNA damage. Environ. Health Perspect. 112 (2004) 1133-1136
7. Perera F.P., Rauh V., Whyatt R.M., Tsai W.Y., Tang D., Diaz D., Hoepner L., Barr D., Tu Y.H., Camann D., and Kinney P. Effect of prenatal exposure to airborne polycyclic aromatic hydrocarbons on neurodevelopment in the first 3 years of life among inner-city children. Environ. Health Perspect. 114 (2006) 1287-1292
8. Perera F.P., Tang D., Rauh V., Tu Y.H., Tsai W.Y., Becker M., Stein J.L., King J., Del Priore G., and Lederman S.A. Relationship between polycyclic aromatic hydrocarbon-DNA adducts, environmental tobacco smoke, and child development in the World Trade Center cohort. Environ. Health Perspect. 115 (2007) 1497-1502
9. Gleeson J.G. Neuronal migration disorders. Ment. Retard. Dev. Disabil. Res. Rev. 7 (2001) 167-171
10. Kisby G.E., Standley M., Lu X., O'Malley J., Lin B., Muniz J., Luo N.L., Back S.A., Pattee P., and Nagalla S.R. Molecular networks perturbed in a developmental animal model of brain injury. Neurobiol. Dis. 19 (2005) 108-118
11. Kisby G.E., Standley M., Park T., Fei S., Jacob T., Reddy A., Lu X., and Nagalla S.R. Proteomic analysis of the genotoxicant methylazoxymethanol (MAM) induced changes in the developing cerebellum. J. Proteome Res. 5 (2006) 2656-2665
12. Nishioka N., and Arnold S.E. Evidence for oxidative DNA damage in the hippocampus of elderly patients with chronic schizophrenia. Am. J. Geriatr. Psychiatry 12 (2004) 167-175
13. Lyras L., Cairns N.J., Jenner A., Jenner P., and Halliwell B. An assessment of oxidative damage to proteins, lipids, and DNA in brain from patients with Alzheimer's disease. J. Neurochem. 68 (1997) 2061-2069
14. Mecocci P., MacGarvey U., and Beal M.F. Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease. Ann. Neurol. 36 (1994) 747-751
15. Mecocci P., Beal M.F., Cecchetti R., Polidori M.C., Cherubini A., Chionne F., Avellini L., Romano G., and Senin U. Mitochondrial membrane fluidity and oxidative damage to mitochondrial DNA in aged and AD human brain. Mol. Chem. Neuropathol. 31 (1997) 53-64
16. 6-methylguanine in rat brain DNA. Nature 269 (1977) 625-626
17. 6-methylguanine-DNA methyltransferase deficiency in developing brain: implications for brain tumorigenesis. DNA Repair 6 (2007) 1127-1133
18. -/- mice. Oncogene 25 (2006) 2425-2432
19. Wong A.W., McCallum G.P., Jeng W., and Wells P.G. Oxoguanine glycosylase 1 protects against methamphetamine-enhanced fetal brain oxidative DNA damage and neurodevelopmental deficits. J. Neurosci. 28 (2008) 9047-9054
20. Gerson S.L. MGMT: its role in cancer aetiology and cancer therapeutics. Nat. Rev. Cancer 4 (2004) 296-307
21. Kaina B., Christmann M., Naumann S., and Roos W.P. MGMT: key node in the battle against genotoxicity, carcinogenicity and apoptosis induced by alkylating agents. DNA Repair 6 (2007) 1079-1099
22. Sedgwick B., Bates P.A., Paik J., Jacobs S.C., and Lindahl T. Repair of alkylated DNA: recent advances. DNA Repair 6 (2007) 429-442
23. 6-methylguanine-DNA methyltransferase in histologically normal brain adjacent to primary human brain tumors. Proc. Natl. Acad. Sci. 93 (1996) 6941-6946
24. Friedberg E.C., and Meira L.B. Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage Version 7. DNA Repair 5 (2006) 189-209
25. Engelward B.P., Weeda G., Wyatt M.D., Broekhof J.L., de Wit J., Donker I., Allan J.M., Gold B., Hoeijmakers J.H., and Samson L.D. Base excision repair deficient mice lacking the Aag alkyladenine DNA glycosylase. Proc. Natl. Acad. Sci. 94 (1997) 13087-13092
26. Glassner B.J., Weeda G., Allan J.M., Broekhof J.L., Carls N.H., Donker I., Engelward B.P., Hampson R.J., Hersmus R., Hickman M.J., Roth R.B., Warren H.B., Wu M.M., Hoeijmakers J.H., and Samson L.D. DNA repair methyltransferase (Mgmt) knockout mice are sensitive to the lethal effects of chemotherapeutic alkylating agents. Mutagenesis 14 (1999) 339-347
27. 6-alkylguanine-DNA alkyltransferase. Science 259 (1993) 219-222
28. Brewer G.J. Serum-free B27/neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, cerebellum, and dentate gyrus. J. Neurosci. Res. 42 (1995) 674-683
29. Kisby G.E., Olivas A., Standley M., Lu X., Pattee P., O'Malley P., Li J.X., Muniz J., and Nagalla S.R. Genotoxicants target distinct molecular networks in neonatal neurons. Environ. Health Perspect. 114 (2006) 1703-1712
30. Meira L.B., Devaraj S., Kisby G.E., Burns D.K., Daniel R.L., Hammer R.E., Grundy S., Jialal I., and Friedberg E.C. Heterozygosity for the mouse APEX gene results in phenotypes associated with oxidative stress. Cancer Res. 61 (2001) 5552-5557
31. White M.J., DiCapri M.J., and Greenberg D.A. Assessment of neuronal viability with Alamar blue in cortical and granule cell cultures. J. Neurosci. Methods 70 (1996) 195-200
32. Springer J.E., Azbill R.D., and Carlson S.L. A rapid and sensitive assay for measuring mitochondrial metabolic activity in isolated neural tissue. Brain. Res. Protoc. 2 (1998) 259-263
33. Kisby G.E., Lesselroth H., Olivas A., Samson L., Gold B., Tanaka K., and Turker M.S. Role of nucleotide- and base-excision repair in genotoxin-induced neuronal cell death. DNA Repair 3 (2004) 617-627
34. Matsumoto H., Spatz M., and Laqueur G.L. Quantitative changes with age in the DNA content of methylazoxymethanol-induced microencephalic rat brain. J. Neurochem. 19 (1972) 297-306
35. Lawley P.D., and Phillips D.H. DNA adducts from chemotherapeutic agents. Mutat. Res. 355 (1996) 13-40
36. Tokuda K., and Bodell W.J. Cytotoxicity and sister chromatid exchanges in 9L cells treated with monofunctional and bifunctional nitrogen mustards. Carcinogenesis 8 (1987) 1697-1701
37. Moller P., Wassermann K., Damgaard J., Nexo B.A., and Wallin H. Sensitivity to nitrogen mustard relates to the ability of processing DNA damage in Chinese hamster ovary cells. Pharmacol. Toxicol. 86 (2000) 169-177
38. Povirk L.F., and Shuker D.E. DNA damage and mutagenesis induced by nitrogen mustards. Mutat. Res. 318 (1994) 205-226
39. Kagami Y., and Furuichi T. Investigation of differentially expressed genes during the development of mouse cerebellum. Brain Res. Gene Expr. Patterns 1 (2001) 39-59
40. Eizirik D.L., and Kisby G.E. Cycad toxin-induced damage of rodent and human pancreatic beta-cells. Biochem. Pharmacol. 50 (1995) 355-365
41. +/- mice using LC/MS/MS. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 844 (2006) 60-66
42. Roth R.B., and Samson L.D. 3-Methyladenine DNA glycosylase-deficient Aag null mice display unexpected bone marrow alkylation resistance. Cancer Res. 62 (2002) 656-660
43. Rinne M.L., He Y., Pachkowski B.F., Nakamura J., and Kelley M.R. N-methylpurine DNA glycosylase overexpression increases alkylation sensitivity by rapidly removing non-toxic 7-methylguanine adducts. Nucleic Acids Res. 33 (2005) 2859-2867
44. Harrison J.F., Rinne M.L., Kelley M.R., Druzhyna N.M., Wilson G.L., and Ledoux S.P. Altering DNA base excision repair: use of nuclear and mitochondrial-targeted N-methylpurine DNA glycosylase to sensitize astroglia to chemotherapeutic agents. Glia 55 (2007) 1416-1425
45. Allan J.M., Engelward B.P., Dreslin A.J., Wyatt M.D., Tomasz M., and Samson L.D. Mammalian 3-methyladenine DNA glycosylase protects against the toxicity and clastogenicity of certain chemotherapeutic DNA cross-linking agents. Cancer Res. 58 (1998) 3965-3973
46. Matijasevic Z., and Volkert M.R. Base excision repair sensitizes cells to sulfur mustard and chloroethyl ethyl sulfide. DNA Repair 6 (2007) 733-741
47. Matsumoto H., and Higa H.H. Studies on methylazoxymethanol, the aglycone of cycasin: methylation of nucleic acids in vitro. Biochem. J. 98 (1966) 20C-22C
48. Mulhern R.K., Merchant T.E., Gajjar A., Reddick W.E., and Kun Late L.E. Neurocognitive sequelae in survivors of brain tumours in childhood. Lancet Oncol. 5 (2004) 399-408
49. Wijen J.P., Nivard M.J., and Vogel E.W. The in vivo genetic activity profile of the monofunctional nitrogen mustard 2-chloroethylamine differs drastically from its bifunctional counterpart mechlorethamine. Carcinogenesis 21 (2000) 1859-1867
50. McHugh P.J., Gill R.D., Waters R., and Hartley J.A. Excision repair of nitrogen mustard-DNA adducts in Saccharomyces cerevisiae. Nucleic Acids Res. 27 (1999) 3259-3266
51. De Alencar T.A., Leitao A.C., and Lage C. Nitrogen mustard- and half-mustard-induced damage in Escherichia coli requires different DNA repair pathways. Mutat. Res. 582 (2005) 105-115
52. Maor-Shoshani A., Meira L.B., Yang X., and Samson L.D. 3-Methyladenine DNA glycosylase is important for cellular resistance to psoralen interstrand cross-links. DNA Repair 7 (2008) 1399-1406
53. Wang X., Peterson C.A., Zheng H., Nairn R.S., Legerski R.J., and Li L. Involvement of nucleotide excision repair in a recombination-independent and error-prone pathway of DNA interstrand cross-link repair. Mol. Cell. Biol. 21 (2001) 713-720
54. McHugh P.J., Spanswick V.J., and Hartley J.A. Repair of DNA interstrand crosslinks: molecular mechanisms and clinical relevance. Lancet Oncol. 2 (2001) 483-490
55. Sarkar S., Davies A.A., Ulrich H.D., and McHugh P.J. DNA interstrand crosslink repair during G1 involves nucleotide excision repair and DNA polymerase zeta. EMBO J. 25 (2006) 1285-1294
56. Briegert M., Enk A.H., and Kaina B. Change in expression of MGMT during maturation of human monocytes into dendritic cells. DNA Repair 6 (2007) 1255-1263
57. 6-alkylguanine-DNA alkyltransferase. Carcinogenesis 7 (1986) 1203-1206
58. 6-benzylguanine on nitrogen mustard-induced toxicity, apoptosis, and mutagenicity in Chinese hamster ovary cells. Mol. Cancer Ther. 1 (2001) 21-28
59. Humphreys W.G., Kim D.H., Cmarik J.L., Shimada T., and Guengerich F.P. Comparison of the DNA-alkylating properties and mutagenic responses of a series of S-(2-haloethyl)-substituted cysteine and glutathione derivatives. Biochemistry 29 (1990) 10342-10350
60. 6-alkylguanine-DNA alkyltransferase. Chem. Res. Toxicol. 17 (2004) 972-982
61. 6-alkylguanine DNA alkyltransferase to DNA in the presence of antitumor nitrogen mustards. Chem. Res. Toxicol. 21 (2008) 787-795
62. 6-methylguanine DNA-methyltransferase (MGMT) overexpression in melanoma cells induces resistance to nitrosoureas and temozolomide but sensitizes to mitomycin C. Toxicol. Appl. Pharmacol. 211 (2006) 97-105
63. 6-methylguanine-DNA methyltransferase and chloroethylnitrosourea-treated DNA. Cancer Res. 52 (1992) 6052-6058