Polycyclic aromatic hydrocarbons with bay-like regions inhibited gap junctional intercellular communication and stimulated MAPK activity

Toxicological Sciences

Volumn 49, Issue 2, 1999, Pages 232-240

  Rummel, Alisa M ^a   Trosko, James E ^a   Wilson, Melinda R ^a   Upham, Brad L ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Chloroanthracene; Extracellular receptor kinase; Gap junctional intercellular communication; Methylanthracene; Mitogen activated phosphokinase; Polycyclic aromatic hydrocarbons

Indexed keywords

1 CHLOROANTHRACENE; 1 METHYLANTHRACENE; 2 CHLOROANTHRACENE; 2 METHYLANTHRACENE; 9 CHLOROANTHRACENE; 9 METHYLANTHRACENE; 9,10 DIMETHYLANTHRACENE; ANTHRACENE; MITOGEN ACTIVATED PROTEIN KINASE; POLYCYCLIC AROMATIC HYDROCARBON; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL COMMUNICATION; CHEMICAL STRUCTURE; CYTOTOXICITY; DOSE RESPONSE; ENZYME ACTIVATION; GAP JUNCTION; GROWTH INHIBITION; NONHUMAN; PROTEIN PHOSPHORYLATION; RAT; STRUCTURE ACTIVITY RELATION;

ANIMALS; BAY REGION (CHEMISTRY); BLOTTING, WESTERN; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CARCINOGENS; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIUM; GAP JUNCTIONS; LIVER; P-AMINOHIPPURIC ACID; RATS; RATS, INBRED F344; STRUCTURE-ACTIVITY RELATIONSHIP; TIME FACTORS;

ANIMALIA;

EID: 0033001404     PISSN: 10966080     EISSN: None     Source Type: Journal    
DOI: 10.1093/toxsci/49.2.232     Document Type: Article

References (76)

1. Archuleta, M. M., Schieven, G. L., Ledbetter, J. A., Deanin, G. G., and Burchiel, S. W. (1993). 7,12-Dimethylbenz(a)anthracene activates protein-tyrosine kinases Fyn and Lck in the HPB-ALL human T-cell line and increases tyrosine phosphorylation of phospholipases C-γ1, formation of inositol 1,4,5-triphophate, and mobilization of intracellular calcium. Proc. Natl. Acad. Sci. USA 90, 6105-6109.
2. Ashby, J., and Tennant, R. W. (1991). Definitive relationships among chemical structure, carcinogenicity, and mutagenicity for 301 chemicals tested by the U.S. NTP. Mutat. Res. 257, 229-306.
3. Beech, J. A. (1991). Cancer promotion in cells initiated by polycyclic aromatic hydrocarbons and other non-viral carcinogens. Med. Hypotheses 36, 4-5.
4. Birrer, M. J., Alani, R., Cuttitta, F., Preis, L. H., Sabich, A. L., Sanders, D. A., Siegfried, J. M., Szabo, E., and Brown, P. H. (1992). Early events in the neoplastic transformation of respiratory epithelium. J. Natl. Cancer Inst. Monogr. 13, 31-37.
5. Bock, F. G., Swain, A. P., and Stedman, R. L. (1969). Bioassay of major fractions of cigarette smoke condensates by an accelerated technic. Cancer Res. 29, 584-587.
6. Borenfreund, E., and Puerna, J. (1985). Toxicology determined in vitro by morphological alterations and neutral red absorption. Toxicol. Lett. 24, 119-124.
7. Boutwell, R. K. (1964). Some biological aspects of skin carcinogenesis. Prog. Exp. Tumor Res. 4, 207-290.
8. Boyd, J. A. and Barrett, J. C. (1990). Genetic and cellular basis of multistep carcinogenesis. Pharmacol. Ther. 46, 469-486.
9. Denhardt, D. T. (1996). Signal-transducing protein phosphorylation cascades mediated by Ras/Rho proteins in the mammalian cell: The potential for multiplex signalling. Biochem. J. 318, 729-747.
10. Dipple, A. (1976). Polynuclear aromatic carcinogens. In Chemical Carcinogens, ACS Monograph 173 (C. E. Searle, Ed.), pp. 245-314. Washington, DC.
11. Dipple, A., Moschel, R. C., and Bigger, C. A. H. (1984). Polynuclear aromatic carcinogens. In Chemical Carcinogens, ACS Monograph (C. E. Searle, Ed.), 2nd Ed., Vol.1, pp. 41-163. Washington, DC.
12. El-Fouly, M. H., Trosko, J. E., and Chang, C. C. (1987). Scrape-loading and dye transfer: A rapid and simple technique to study gap junctional intercellular communication. Exp. Cell Res. 168, 422-430.
13. Flesher, J. W., and Myers, S. R. (1991a). Bioakylation of benz(a)anthracene as a biochemical probe for carcinogenic activity: Lack of bioakylation in a series of six noncarcinogenic polynuclear aromatic hydrocarbons. Drug Metab. Dispos. 18, 163-167.
14. Flesher, J. W., and Myers, S. R. (1991b). Rules of molecular geometry for predicting carcinogenic activity of unsubstituted polynuclear aromatic hydrocarbons. Teratog. Carcinog. Mutagen. 11, 41-54.
15. Flesher, J. W., Myers, S. R., and Stansbury, K. H. (1990). The site of substitution of the methyl group in the bioalkylation of benzo(a)pyrene. Carcinogenesis 11, 493-496.
16. Goldberg, G. S., Martyn, K. D., and Lau, A. F. (1994). A connexin 43 antisense vector reduces the ability of normal cells to inhibit the foci formation of transformed cells. Mol. Carcinog. 11, 106-114.
17. Harris, C. C. (1991). Chemical and physical carcinogenesis: Advances and perspectives for the 1990s. Cancer Res. 51(suppl.), 5023s-5044s.
18. Hartman, T. G., and Rosen, J. D. (1983). Inhibition of metabolic cooperation by cigarette smoke condensate and its fractions in V-79 Chinese hamster lung fibroblasts. Proc. Natl. Acad. Sci. U S A 80, 5305-5309.
19. Hecht, S. S., Loy, M., and Hoffmann, D. (1977). On the structure and carcinogenicity of the methylchrysenes. In Carcinogenesis, Vol. 1, Polynuclear Aromatic Hydrocarbons: Chemistry, Metabolism and Carcinogenesis (R. I. Freudenthal and P. W. Jones, Eds.), pp. 325-340. Raven Press, New York.
20. Hill, C. S., Marais, R., John, S., Wynne, J., Dalton, S., and Treisman, R. (1993). Functional analysis of a growth factor-responsive transcription factor complex. Cell 73, 395-406.
21. Hoffman, D., Lavoie, E. J., and Hecht, S. S. (1982). Polynuclear aromatic hydrocarbons: Effects of chemical structure on tumorigenicity. In Polynuclear Aromatic Hydrocarbons: Physical and Biological Chemistry (M. Cooke, A. J. Dennis, and G. L. Fisher, Eds.), pp. 1-19. Battelle Press, Columbus, OH.
22. Holliday, R. (1987). DNA methylation and epigenetic defects in carcinogenesis. Mutat. Res. 181, 215-217.
23. Hossain, M. Z., Ao, P., and Boynton, A. L. (1998). Platelet-derived growth factor-induced disruption of gap junctional communication and phosphorylation of connexin43 involves protein kinase C and mitogen-activated protein kinase. J. Cell Physiol. 176, 332-341.
24. IARC. (1984). Polynuclear aromatic compounds: Industrial exposures in aluminum production, coal gasification, coke production, and iron and steel founding. In IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans, Vol. 34(3), pp. 107-108. Lyon, France.
25. IARC. (1983). Polynuclear aromatic compounds: Chemical, environmental and experimental data. In IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans, Vol. 32(1), pp. 95-447. Lyon, France.
26. Jerina, D. M., Yagi, H., Lehr, R. E., Thakker, D. R., Schaefer-Ridder, M., Karle, J. M., Levin, W., Wood, A. W., Chang, R. L., and Conney, A. H. (1978). The bay-region theory of carcinogenesis by polycyclic aromatic hydrocarbons. In Polycyclic Hydrocarbons and Cancer, Vol. 1, Environment, Chemistry, and Metabolism (H. Gelboin and P. O. P. Ts'o, Eds.), pp. 173-188. Academic Press, New York.
27. Kanemitsu, M. Y., and Lau, A. F. (1993). Epidermal growth factor stimulates the disruption of gap junctional communication and connexin43 phosphorylation independent of 12-0-tetradecanoylphorbol 13-acetate-sensitive protein kinase C: The possible involvement of mitogen-activated protein kinase. Mol. Cell. Biol. 4, 837-848.
28. Kurihara, T., Motohashi, N., Pang, G.-L., Higano, M., Kiguchi, K., and Molnar, J. (1996). Correlations between topological resonance energy of methyl-substituted benz(c)acridines, benzo(a)phenothiazines and chrysenes, and their carcinogenic or anti-tumor activities. Anticancer Res. 16, 2757-2765.
29. Kyriakis, J. M., Banerjee, P., Nikolakaki, E., Dai, T., Rubie, E. A., Ahmad, M. F., Avruch, J., and Woodgett, J. R. (1994). The stress-activated protein kinase subfamily of c-Jun kinases. Nature 369, 156-160.
30. Laemmli, N. K. (1970). Cleavage of structural proteins during the assembly head of bacteriophage T4. Nature 227, 680-685.
31. LaVoie, E. J., Coleman, D. T., Rice, J. E., Geddie, N. G., and Hoffman, D. (1985). Tumor-initiating activity, mutagenicity, and metabolism of methylated anthracenes. Carcinogenesis 6, 1483-1488.
32. LaVoie, E. J., Tulley-Freiler, L., Bedenko, V., and Hoffmann, D. (1981). Mutagenicity, tumor-initiating activity, and metabolism of methylphenanthrenes. Cancer Res. 41, 3441-3447.
33. 2-terminal kinase 1 by benzo(a)pyrene. Cancer Res. 58, 2102-2106.
34. Marais, R., Wynn, J., and Treisman, R. (1993). The SRF accessory protein Elk-1 contains a growth factor-regulated transcriptional activation domain. Cell 73, 381-393.
35. Markert, C. (1968). Neoplasia: A disease of differentiation. Cancer Res. 28, 1908-1914.
36. Myers, S. R., Blake, J. W., and Flesher, J. W. (1988). Bioalkylation and biooxidation of anthracene, in vitro and in vivo. Biochem. Biophys. Res. Commun. 151, 1441-1445.
37. Myers, S. R. and Flesher, J. W. (1991). Bioakylation of benz(a)anthracene, 7-methylbenz(a)anthracene and 12-methylbenz(a)anthracene in rat lung cytosol preparations. Biochem. Pharmacol. 41, 1683-1690.
38. Neff, J. M (1979). Polycyclic Aromatic Hydrocarbons in the Aquatic Environment: Sources, Fates, and Biological Effects, pp 1-259. Applied Science Publishers, London.
39. Nesnow, S., Triplett, L. L., and Slaga, T. J. (1985). Studies on the tumor initiating, tumor promoting, and tumor co-initiating properties of respiratory carcinogenesis. Carcinog. Compr. Surv. 8, 257-277.
40. Parrish, A. R., Fisher, R., Bral, C M., Burghardt, R. C., Gandolfi, A. J., Brendel, K., Ramos, K. S. (1998). Benzo(a)pyrene-induced alterations in growth-related gene expression and signaling in precision-cut adult rat liver and kidney slices. Toxicol. Appl. Pharmacol 152, 302-308.
41. Pulverer, B. J., Kyriakis, J. M., Avruch, J., Nikolakaki, E., and Woodgett, J. R. (1991). Phosphorylation of c-jun mediated MAP kinases. Nature 353, 670-674.
42. Rao, V. N., and Reddy, E. S. (1994). Elk-1 proteins interact with MAP kinases. Oncogene 9, 1855-1860.
43. Ruch, R. J., Guan, X., and Sigler, K. (1995). Inhibition of gap junctional intercellular communication and enhancement of growth in BALB/c 3T3 cells treated with connexin 43 antisense oligonucleotides. Mol. Carcinog 14, 269-274.
44. Rutten, A. A. J. J. L, Jongen, W. M. F., d'Haan, L. H. J., Hendriksen, E. G. J., and Koeman, J. H. (1988). Effect of retinol and cigarette-smoke condensate on dye-coupled intercellular communication between hamster tracheal epithelial cells. Carcinogenesis 9, 315-320.
45. Severson, R. F., Snook, M. E., Higman, H. C., Chortyk, O. T., and Akin. F. J. (1976). Isolation, identification, and quantification of the polynuclear aromatic hydrocarbons in tobacco smoke. In Polynuclear Aromatic Hydrocarbons: Physical and Biological Chemistry (R. I. Freudenthal and P. W. Jones, Eds.), pp. 253-270. Raven Press, New York.
46. Silverman, B. D., and Lowe, J. P. (1982). Diol-epoxide reactivity of methylated polycyclic aromatic hydrocarbons (PAH): Ranking the reactivity of the positional monomethyl isomers. In Chemistry, Metabolism, and Carcinogenesis (M. Cooke, A. J. Dennis, and G. L. Fisher, Eds.), pp. 743-753. Battelle Press, Columbus, OH.
47. Slaga, T.-J., Bowden, G. T., Scribner, J. D., and Boutwell, R. K. (1974). Dose-response studies on the ability of 7,12-dimethylbenz(α)anthracene and benz(α)anthracene to initiate skin tumors. J. Natl. Cancer Inst. 53, 1337-1340.
48. Slaga, T. J., Iyer, R. P., Lyga, W., Secrist A., Daub, G. H., and Harvey, R. G. (1980). Comparison of the skin tumor-initiating activities of dihydrodiols, dioleperoxides, and methylated derivatives of various polycyclic aromatic hydrocarbons. In Polynuclear Aromatic Hydrocarbons: Chemistry and Biological Effects (A. Bjerseth and A. J. Dennis, Eds.), pp. 753-769. Battelle Press, Columbus, OH.
49. Solomon, T. W. G. (1987). In Organic Chemistry, pp. 65, 118, 653, and 661. Wiley, New York.
50. 2+ and cell proliferation in primary human mammary epithelial cells. Carcinogenesis 18, 1177-1182.
51. Temme, A., Buchmann, A., Gabriel, H.-D., Nelles, E., Schwarz, M., and Willecke, K. (1997). High incidence of spontaneous and chemically induced liver tumors in mice deficient for connexin32. Curr. Biol. 7, 713-716.
52. Trosko, J. E. (1997). Challenge to the simple paradigm that "carcinogens" are "mutagens" and to the in vitro and in vivo assays used to test the paradigm. Mutat. Res. 373, 245-249.
53. Trosko, J. E. and Chang, C. C. (1988). Non-genotoxic mechanisms in carcinogenesis: Role of inhibited intercellular communication. In Banbury Report 31: New Directions in the Qualitative and Quantitative Aspects of Carcinogen Risk Assessment (R. W. Hart and F. D. Hoerger, Eds.), pp. 139-170. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
54. Trosko, J. E., Chang, C. C., and Madhukar, B. V. (1988). Modulation of gap junction intercellular communication by tumor promoting chemicals, oncogenes, and growth factors during carcinogenesis. In Modern Cell Biology, Vol. 7: Gap Junctions (E. L. Hertzberg, and R. G. Johnson, Eds.), pp. 435-448. Alan R. Liss, New York.
55. Trosko, J. E., Chang, C. C., and Madhukar, B. V. (1990a). In vitro analysis of modulators of intercellular communication: Implications for biologically based risk assessment models for chemical exposure. Toxicol In vitro 4, 635-643.
56. Trosko, J. E., Chang, C. C., Madhukar, B. V., and Oh, S. Y. (1990b). Modulators of gap junction function: The scientific basis of epigenetic toxicology. In vitro Toxicol. 3, 9-26.
57. Trosko, J. E., Chang, C. C., Madhukar, B. V., and Klaunig, J. E. (1990c). Chemical, oncogene and growth factor inhibition of gap junctional intercellular communication: An integrative hypothesis of carcinogenesis. Pathobiology 58, 265-278.
58. Trosko, J. E., Chang, C. C., and Madhukar, B. V. (1994). The role of modulated gap junctional intercellular communication in epigenetic toxicology. Risk Anal. 14, 303-312.
59. Trosko, J. E., Chang, C. C., Madhukar, B. V., and Dupont, E. (1996). Intercellular communication: A paradigm for the interpretation of the initiation/promotion/progression model of carcinogenesis. In Chemical Induction of Cancer: Modulation and Combination Effects (J. C. Arcos, M. F. Argus, and Y. T. Woo, Eds.), pp. 205-225. Birkhauser, Boston.
60. Trosko, J. E., Chang, C. C., and Medcalf, A. (1983). Mechanisms of tumor promotion: Potential role of intercellular communication. Cancer Invest. 1, 511-526.
61. Trosko, J. E., Madhukar, B. V., and Chang, C. C. (1993). Endogenous and exogenous modulation of gap junctional intercellular communication: Toxicological and pharmacological implications. Life Sci. 53, 1-19.
62. Trosko, J. E., and Ruch, R. J. (1998). Cell-cell communication in carcinogenesis. Frontiers in Biosci. 3, 208-236.
63. Tsao, M. S., Smith, J. D., Nelson, K. G., and Grisham, J. W. A. (1984). Diploid epithelial cell line from normal adult rat liver with phenotypic properties of oval cells. Experimental Cell Research 154, 38-52.
64. Upham, B. L., Masten, S. J., Lockwood, B. R., and Trosko, J. E. (1994). Non-genetoxic effects of polycyclic aromatic hydrocarbons and their ozonation by-products on the intercellular communication of rat liver epithelial cells. Fundam. Appl. Toxicol. 23, 470-475.
65. Upham, B. L., Weis, L. M., Rummel, A. M., Masten, S. J., and Trosko, J. E. (1996). The effects of anthracene and methylated anthracenes on gap junctional intercellular communication in rat liver epithelial cells. Fundam. Appl. Toxicol. 34, 260-264.
66. Upham, B. L., Weis, L. M., and Trosko, J. E. (1998). Modulated gap junctional intercellular communication as a biomarker of PAH epigenetic toxicity: Structure-function relationship. Environ. Health Perspect. 106, 975-981.
67. Upham, B. L., Yao, J.-J., Trosko, J. E., and Masten S. J. (1995). Determination of the efficacy of ozone treatment systems using a gap junction intercellular communiction bioassay. Environ. Sci. Technol. 29, 2923-2928.
68. Vang, O., Wallin, H., and Autrup, H. (1995). Inhibitions of intercellular communication by condensates of high and low tar cigarettes. Arch. Toxicol. 69, 415-420
69. Warn-Cramer, B. J., Cottrell, G. T., Burt, J. M., and Lau, A.F. (1998). Regulation of connexin-43 gap junctional intercellular communication by mitogen-activated protein kinase. J. Biol. Chem. 273, 9188-9196.
70. Warn-Cramer, B. J, Lampe, P. D., Kurata, W. E., Kanemitsu, M. Y., Loo, L. W., Eckhart, W., and Lau, A. F. (1996). Characterization of the mitogen-activated protein kinase phosphorylation sites on the connexin-43 gap junction protein. J. Biol. Chem. 271, 3779-3786.
71. Weis, L. M., Rummel, A. M., Masten, S. J., Trosko, J. E., and Upham, B. L. (1998). Bay or baylike regions of polycyclic aromatic hydrocarbons were potent inhibitors of gap junctional intercellular communication. Environ. Health Perspect. 106, 17-22.
72. Weisburger, J. H., and Wynder, E. L. (1984). The role of genotoxic carcinogens and of promoters in carcinogenesis and in human cancer causation. Acta Pharmacol. Toxicol. 55(suppl. 2), 53-68.
73. Wilson, M. R., Umeh, I., Kang, K.-S., and Trosko, J. E. (1998). A role for mitogen-activated protein kinase (MAPK) during ras-induced down-regulation of gap junctional intercellular communication. In Gap Junctions (R. Werner, Ed.), pp. 239-243. IOS Press, Amsterdam.
74. Yamasaki, H., and Naus, C. C. G. (1996). Role of connexin genes in growth control. Carcinogenesis 17, 1199-1213.
75. Zhang Y., and Ramos, K. S. (1997). The induction of proliferative vascular smooth muscle cell phenotypes by benzo(a)pyrene does not involve mutational activation of ras genes. Mutat. Res. 373, 285-292.
76. Zinck, R., Hipskind, R. A., Pingoud, V., and Nordheim, A. (1993). c-Fos transcriptional activation and repression correlate temporally with the phosphorylation status of TCF. EMBO J. 12, 2377-2387.