Developmentally Specific Effects of the DNA Cross-Linking Agent Mitomycin C on Phosphoenolpyruvate Carboxykinase Gene Expression in Vivo: Correlation with Changes in Chromatin Structure within the Promoter Region of the Gene

Journal of Biochemical and Molecular Toxicology

Volumn 12, Issue 6, 1998, Pages 325-337

  Caron, Rosemary M ^a   Hamilton, Joshua W ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Carcinogenesis; Chicken Embryo; DNA Damage; Gene Regulation; Liver

Indexed keywords

GALLUS GALLUS;

ALKYLATING AGENT; MESSENGER RNA; MITOMYCIN; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP);

ANIMAL; ARTICLE; CHEMISTRY; CHICK EMBRYO; CHROMATIN; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; PROMOTER REGION; PROTEIN CONFORMATION;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; CHICK EMBRYO; CHROMATIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MITOMYCIN; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); PROMOTER REGIONS (GENETICS); PROTEIN CONFORMATION; RNA, MESSENGER;

EID: 0031615815     PISSN: 10956670     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1099-0461(1998)12:6<325::aid-jbt2>3.0.co;2-2     Document Type: Article

References (81)

1. V. A. Bohr, D. H. Phillips, and P. C. Hanawalt (1987). Heterogeneous DNA damage and repair in the mammalian genome. Cancer Res., 47, 6426-6436.
2. M. C. MacLeod (1995). Interaction of bulky chemical carcinogens with DNA in chromatin. Carcinogenesis, 16, 2009-2014.
3. M. F. Denissenko, A. Pao, M.-S. Tang, and G. P. Pfeifer (1996). Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in P53. Science, 274, 430-432.
4. J. W. Hamilton and K. E. Wetterhahn (1989). Differential effects of chromium(VI) on constitutive and inducible gene expression in chick embryo liver in vivo and correlation with chromium(VI)-induced DNA damage. Mol. Carcinogen., 2, 274-286.
5. J. W. Hamilton, C. A. Louis, K. A. Doherty, S. R. Hunt, M. J. Reed, and M. D. Treadwell (1993). Preferential alteration of inducible gene expression in vivo by carcinogens that induce bulky DNA lesions. Mol. Carcinogen., 8, 34-43.
6. J. McCaffrey and J. W. Hamilton (1994). Comparison of effects of direct-acting DNA methylating and ethylating agents on inducible gene expression in vivo. Environ. Mol. Mutagen., 23, 164-170.
7. J. W. Hamilton, J. McCaffrey, R. M. Caron, C. A. Louis, M. D. Treadwell, S. R. Hunt, M. J. Reed, and K. A. Doherty (1994). Genotoxic chemical carcinogens target inducible genes in vivo. Ann. N. Y. Acad. Sci., 726, 343-345.
8. R. M. Caron and J. W. Hamilton (1995). Preferential effects of the chemotherapeutic DNA crosslinking agent mitomycin C on inducible gene expression in vivo. Environ. Mol. Mutagen., 25, 4-11.
9. D. K. Granner and E. G. Beale (1985). Regulation of the synthesis of tyrosine aminotransferase and phosphoenolpyruvate carboxykinase by glucocorticoid hormones. In Biochemical Actions of Hormones, vol. XII, pp. 89-138, Academic, New York.
10. P. C. Lucas and D. K. Granner (1992). Hormone response domains in gene transcription. Annu. Rev. Biochem., 61, 1131-1173.
11. R. W. Hanson and Y. M. Patel (1994). Phosphoenolpyruvate carboxykinase (GTP): the gene and the enzyme. Adv. Enzymol. Rel. Areas Mol. Biol., 69, 203-281.
12. J. McCaffrey and J. W. Hamilton (1994). Developmental regulation of basal and hormone-inducible phoshoenol-pyruvate carboxykinase gene expression in chick embryo liver in vivo. Arch. Biochem. Biophys., 309, 10-17.
13. A. Sato, T. Suzuki, and H. Kochi (1990). Regulation of hormonal induction of chick liver cytosol-specific phosphoenolpyruvate carboxykinase. J. Biochem., 108, 720-725.
14. S. Savon, P. Hakimi, and R. W. Hanson (1993). Expression of the genes for the mitochondrial and cytosolic forms of PEPCK in avian liver during development. Biol. Neonate, 64, 62-68.
15. Y. Hod, H. Yoo-Warren, and R. W. Hanson (1984). The gene encoding the cytosolic form of phosphoenolpyruvate carboxykinase (GTP) from the chicken. J. Biol. Chem., 259, 15609-15614.
16. R. F. Cook, S. J. Cook, S. Savon, M. McGrane, M. Hartitz, R. W. Hanson, and C. P. Hodgson (1993). Liver-specific expression of a phosphoenolpyruvate carboxykinase-neo gene in genetically modified chickens. Poultry Sci., 72, 554-567.
17. M. Watford (1989). Hormonal and nutritional regulation of phosphoenolpyruvate carboxykinase mRNA levels in chicken kidney. J. Nutr., 119, 319-322.
18. J. McCaffrey, C. M. Wolf, and J. W. Hamilton (1994). Effects of the genotoxic carcinogen chromium(VI) on basal and hormone-inducible phosphoenolpyruvate carboxykinase gene expression in vivo: correlation with glucocorticoid- and developmentally-regulated expression. Mol. Carcinogen., 10, 189-198.
19. D. C. Doll, R. B. Weiss, and B. F. Issell (1984). Mitomycin: ten years after approval for marketing. J. Clin. Oncol., 3, 276-286.
20. J. W. Hamilton, M. S. Denison, and S. E. Bloom (1983). Development of basal and induced aryl hydrocarbon (benzo[a]pyrene) hydroxylase activity in the chicken embryo in ovo. Proc. Natl. Acad. Sci. USA, 80, 3372-3376.
21. J. W. Hamilton, W. J. Bement, P. R. Sinclair, J. F. Sinclair, and K. E. Wetterhahn (1988). Expression of 5-aminolaevulinate synthase and cytochrome P-450 mRNAs in chicken embryo hepatocytes in vivo and in cell culture: effect of porphyrinogenic drugs and haem. Biochem. J., 255, 267-275.
22. W. C. Forrester, E. Epner, M. C. Driscoll, T. Enver, M. Brice, T. Papayannopoulou, and M. Groudine (1990). A deletion of the human b-globin locus activation region causes a major alteration in chromatin structure and replication across the entire b-globin locus. Genes and Development, 4, 1637-1649.
23. S. P. Savon, P. Hakimi, D. R. Crawford, D. J. Klemm, A. L. Gurney, and R. W. Hanson (1997). The promoter regulatory regions of the genes for the cytosolic form of phosphoenolpyruvate carboxykinase (GTP) from the chicken and the rat have different species-specific roles in gluconeogenesis. J. Nutr., 127, 276-285.
24. 2G interstrand crosslink in a model synthetic 23 base pair oligonucleotide DNA duplex. Chem. Res. Toxicol., 9, 1063-1071.
25. 32P-postlabeling: time course for formation and removal of adducts and biochemical modulation. Cancer Res., 58, 453-461.
26. P. C. Hanawalt (1991). Heterogeneity of DNA repair at the gene level. Mutat. Res., 247, 203-211.
27. R. J. Wilkins (1985). Site-specific analysis of drug interactions and damage in DNA using sequencing techniques. Anal. Biochem., 147, 267-279.
28. R. J. Wilkins (1984). Sequence specificities in the interactions of chemicals and radiations with DNA. Mol. Cell. Biochem., 64, 111-126.
29. K. Hemminki (1983). Nucleic acid adducts of chemical carcinogens and mutagens. Arch. Toxicol., 52, 249-285.
30. 1 with guanines in different DNA sequences. Biochemistry, 27, 472-481.
31. A. Kootstra, L. K. Lew, R. S. Nairn, and M. C. MacLeod (1989). Preferential modification of GC boxes by benzo[a]pyrene-7,8-diol-9,10-epoxide. Mol. Carcinogen., 1, 239-244.
32. P. Kurian, A. M. Jeffrey, and G. E. Milo (1985). Preferential binding of benzo[a]pyrene-diol epoxide to the linker DNA of human foreskin fibroblasts in S phase in the presence of benzamide. Proc. Natl. Acad. Sci. USA, 82, 2769-2773.
33. P. L. Jack and P. Brookes (1982). Mechanism for the loss of preferential benzo[a]pyrene binding to the linker DNA of chromatin. Carcinogenesis, 3, 341-344.
34. 1 adduction of sequence-positioned nucleosome core particles. J. Biol. Chem., 264, 12226-12231.
35. L. Marrot, E. Hebert, G. Saint-Ruf, and M. Leng (1987). Comparison of the reactivity of B-DNA and Z-DNA with two isosteric chemical carcinogens: 2-N,N-acetoxyacetylaminofluorene and 3-N,N-acetoxyacetylamino-4,6-dimethyldipyrido[1,2-a:3′,2′-d]imida zole. Nucl. Acid Res., 15, 5629-5642.
36. R. S. Paules, M. Cordeiro-Stone, M. J. Mass, M. C. Poirier, S. H. Yuspa, and D. G. Kaufman (1988). Benzo[a]pyrene diol epoxide I binds to DNA at replication forks. Proc. Natl. Acad. Sci. USA, 85, 2176-2180.
37. Y. Kohwi (1989). Non-B DNA structure: preferential target for the chemical carcinogen glycidaldehyde. Carcinogenesis, 10, 2035-2042.
38. T. Kohwi-Shigematsu, N. Scribner, and Y. Kohwi (1988). An ultimate chemical carcinogen, N-acetoxy-2-acetylaminofluorene, detects non-B DNA structures that are reactive with chloroacetaldehyde in supercoiled plasmid DNA. Carcinogenesis, 9, 457-461.
39. 1 adduction of chicken erythrocyte chromatin. Cancer Res., 48, 7146-7149.
40. J. E. Arrand and A. M. Murray (1982). Benzpyrene groups bind preferentially to the DNA of active chromatin in human lung cells. Nucl. Acid Res., 10, 1547-1555.
41. 1 to the transcriptionally active regions of rat liver nucleolar chromatin in vivo and in vitro. Carcinogenesis, 4, 889-893.
42. F.-L. Yu (1983). Actinomycin D-binding in vivo: active chromatin preferred. FEBS Lett., 156, 83-87.
43. R. C. Gupta (1984). Nonrandom binding of the carcinogen N-hydroxy-2-acetylaminofluorene to repetitive sequences of rat liver DNA in vivo. Proc. Natl. Acad. Sci. USA, 81, 6943-6947.
44. 1 adducts formed in vivo within the ribosomal RNA genes of rat liver DNA. Cancer Res., 45, 3497-3502.
45. F. O. Obi, A. J. Ryan, and M. A. Billett (1986). Preferential binding of the carcinogen benzo[a]pyrene to DNA in active chromatin and the nuclear matrix. Carcinogenesis, 7, 907-913.
46. J. J. Yunis, A. L. Soreng, and A. E. Bowe (1987). Fragile sites are targets of diverse mutagens and carcinogens. Oncogene, 1, 59-69.
47. P. D. Kurth and M. Bustin (1985). Site-specific carcinogen binding to DNA in polytene chromosomes. Proc. Natl. Acad. Sci. USA, 82, 7076-7080.
48. O. A. Olivero, H. Huitfeldt, and M. C. Poirier (1990). Chromosome site-specific immunohistochemical detection of DNA adducts in N-acetoxy-2-acetylaminofluorene-exposed Chinese hamster ovary cells. Mol. Carcinogen., 3, 37-43.
49. C. T. McMurray, W. D. Wilson, and J. O. Douglass (1991). Hairpin formation within the enhancer region of the hu-man enkaphalin gene. Proc. Natl. Acad. Sci. USA, 88, 666-670.
50. P. M. Lieberman and A. J. Berk (1991). The Zta trans-activator protein stabilizes TFIID association with promoter DNA by direct protein-protein interaction. Genes Dev., 5, 2441-2454.
51. L. J. Maher III, P. B. Dervan, and B. Wold (1992). Analysis of promoter-specific repression by triple-helical DNA complexes in a eukaryotic cell-free transcription system. Biochemistry, 31, 70-81.
52. A. R. Rahmouni and R. D. Wells (1992). Direct evidence for the effect of transcription on local DNA supercoiling in vivo. J. Mol. Biol., 223, 131-144.
53. A. Jimenez-Ruiz, J. M. Requena, M. C. Lopez, and C. Alonso (1991). A potential Z-DNA-forming sequence is located between two transcription units alternatively expressed during development of Drosophila hydei. Proc. Natl. Acad. Sci. USA, 88, 31-35.
54. B. Wittig, T. Dorbic, and A. Rich (1991). Transcription is associated with Z-DNA formation in metabolically active permeabilized mammalian cell nuclei. Proc. Natl. Acad. Sci. USA, 88, 2259-2263.
55. M. W. Leonard and R. K. Patient (1991). Evidence for torsional stress in transcriptionally activated chromatin. Mol. Cell. Biol., 11, 6128-6138.
56. J. Delic, R. Onclercq, and M. Moisan-Coppey (1991). Inhibition and enhancement of eukaryotic gene expression by potential non-B DNA sequences. Biochem. Biophys. Res. Commun., 180, 1273-1283.
57. S. Spadari, B. M. Sutherland, G. Pedrali-Noy, F. Focher, M. T. Chiesa, and G. Ciarrocchi (1987). Alteration of DNA tertiary structure by physical and chemical carcinogens: involvement in DNA repair processes. Toxicol. Pathol., 15, 82-87.
58. P. A. Jones (1986). DNA methylation and cancer. Cancer Res., 46, 461-466.
59. V. L. Wilson, R. A. Smith, J. Longoria, M. A. Liotta, C. M. Harper, and C. C. Harris (1987). Chemical carcinogen-induced decreases in genomic 5-methyldeoxycytidine content of normal human bronchial epithelial cells. Proc. Natl. Acad. Sci. USA, 84, 3298-3301.
60. 5CpG dinucleotide sequence in DNA by mitomycin C for alkylation and cross-linking. Bioorg. Med. Chem., 3, 851-860.
61. R. H. Getzenberg, K. J. Pienta, W. S. Ward, and D. S. Coffey (1991). Nuclear structure and the three-dimensional organization of DNA. J. Cell. Biochem., 47, 289-299.
62. C. Bonifer, A. Hecht, H. Saueressig, D. M. Winter, and A. E. Sippel (1991). Dynamic chromatin: the regulatory domain organization of eukaryotic gene loci. J. Cell. Biochem., 47, 99-108.
63. A. J. Courey, S. E. Plon, and J. C. Wang (1986). The use of psoralen-modified DNA to probe the mechanism of enhancer action. Cell, 45, 567-574.
64. K. E. Wetterhahn and J. W. Hamilton (1989). Molecular basis of hexavalent chromium carcinogenicity: effect on gene expression. Sci. Total Environ., 86, 113-129.
65. J. A. Alcedo, M. Misra, J. W. Hamilton, and K. E. Wetterhahn (1994). The genotoxic carcinogen chromium(VI) alters the metal-inducible expression but not the basal expression of the metallothionein gene in vivo. Carcinogenesis, 15, 1089-1092.
66. M. A. Ihnat, J. P. Lariviere, A. J. Warren, N. La Ronde, J. R. N. Blaxall, K. M. Pierre, B. W. Turpie, and J. W. Hamilton (1997). Suppression of p-glycoprotein expression and multidrug resistance by DNA crosslinking agents. Clin. Cancer Res., 3, 1339-1346.
67. I. Stammberger, W. Schmahl, and K. Tempel (1989). Scheduled and unscheduled DNA synthesis in chick embryo liver following X-irradiation and treatment with DNA repair inhibitors in vivo. Int. J. Radiat. Biol., 56, 325-333.
68. J. W. Hamilton and M. A. Ihnat (1994). The preferential effects of carcinogens on inducible gene expression are not mediated by the "UV response" pathway. Proc. Am. Assoc. Cancer Res., 35, 143.
69. J. W. Hamilton, R. C. Kaltreider, O. V. Bajenova, M. A. Ihnat, J. McCaffrey, B. W. Turpie, E. E. Rowell, J. Oh, M. J. Nemeth, C. A. Pesce, and J. P. Lariviere (1998). Molecular basis for effects of carcinogenic heavy metals on inducible gene expression. Environ. Hlth. Perspect., 106 (suppl. 4), 1005-1015.
70. D. Granner, R. O'Brien, E. Imai, C. Forest, J. Mitchell, and P. Lucas (1991). Complex hormone response unit regulating transcription of the phosphoenolpyruvate carboxykinase gene: from metabolic pathways to molecular biology. Rec. Prog. Horm. Res., 47, 319-346.
71. S. Faber, T. Ip, D. Granner, and R. Chalkley (1991). The interplay of ubiquitous DNA-binding factors, availability of binding sites in the chromatin, and DNA methylation in the differential regulation of phosphoenolpyruvate carboxykinase gene expression. Nucl. Acid Res., 19, 4681-4688.
72. J. Liu and R. W. Hanson (1991). Regulation of phosphoenolpyruvate carboxykinase (GTP) gene transcription. Mol. Cell. Biochem., 104, 89-100.
73. E. Imai, P.-E. Stromstedt, P. G. Quinn, J. Carlstedt-Duke, J.-A. Gustafsson, and D. K. Granner (1990). Characterization of a complex glucocorticoid response unit in the phosphoenolpyruvate carboxykinase gene. Mol. Cell. Biol., 10, 4712-4719.
74. W. J. Roesler, J. G. Graham, R. Kolen, D. J. Klemm, and P. J. McFie (1995). The cAMP response element binding protein synergizes with other transcription factors to mediate cAMP responsiveness. J. Biol. Chem., 270, 8225-8232.
75. P.-O. Angrand, C. Coffinier, and M. C. Weiss (1994). Response of the phosphoenolpyruvate carboxykinase gene to glucocorticoids depends on the integrity of the cAMP pathway. Cell Growth Differ., 5, 957-966.
76. Y. T. Ip, D. K. Granner, and R. Chalkley (1989). Hormonal regulation of phosphoenolpyravate carboxykinase gene expression is mediated through modulation of an already disrupted chromatin structure. Mol. Cell. Biol., 9, 1289-1297.
77. Y. T. Ip, D. Poon, D. Stone, D. K. Granner, and R. Chalkley (1990). Interaction of a liver-specific factor with an enchancer 4.8 kilobases upstream of the phosphoenolpyruvate carboxykinase gene. Mol. Cell. Biol., 10, 3770-3781.
78. M. Trus, N. Benvenisty, H. Cohen, and L. Reshef (1990). Developmentally regulated interactions of liver nuclear factors with the rat phosphoenolpyruvate carboxykinase promoter. Mol. Cell. Biol., 10, 2418-2422.
79. M. K. Short, D. E. Clouthier, I. M. Schaefer, R. E. Hammer, M. A. Magnuson, and E. G. Beale (1992). Tissue-specific, developmental, hormonal, and dietary regulation of rat phosphoenolpyruvate carboxykinase-human growth hormone fusion genes in transgenic mice. Mol. Cell. Biol., 12, 1007-1020.
80. W. J. Roesler, G. R. Vandenbark, and R. W. Hanson (1989). Identification of multiple protein binding domains in the promoter-regulatory region of the phosphoenolpyruvate carboxykinase (GTP) gene. J. Biol. Chem., 264, 9657-9664.
81. C. D. Forest, R. M. O'Brien, P. C. Lucas, M. A. Magnuson, and D. K. Granner (1990). Regulation of phosphoenolpyruvate carboxykinase gene expression by insulin. Use of the stable transfection approach to locate an insulin responsive sequence. Mol. Endocrinol., 4, 1302-1310.