Mechanism of Action of Chemoprotective Ursodeoxycholate in the Azoxymethane Model of Rat Colonic Carcinogenesis: Potential Roles of Protein Kinase C-αβII, and -ζ1

Cancer Research

Volumn 55, Issue 22, 1995, Pages 5257-5264

  Wali, Ramesh K ^a   Frawley, Brendan P ^a   Hartmann, Susanne ^a   Roy, Hemant K ^a   Khare, Sharad ^a   Scaglione Sewell, Beth A ^a   Sitrin, Michael D ^a   Brasitus, Thomas A ^a   Bissonnette, Marc ^a   Earnest, David L ^b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLIC ACID; PROTEIN KINASE C; URSODEOXYCHOLIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL FRACTIONATION; COLON CARCINOMA; CONTROLLED STUDY; DIET SUPPLEMENTATION; IMMUNOBLOTTING; MALE; MALIGNANT TRANSFORMATION; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SECOND MESSENGER;

ANIMAL; ANTICARCINOGENIC AGENTS; AZOXYMETHANE; CHOLIC ACID; CHOLIC ACIDS; COLONIC NEOPLASMS; ISOENZYMES; MALE; PROTEIN KINASE C; RATS; RATS, INBRED F344; SUPPORT, NON-U.S. GOV'T; SUPPORT, U.S. GOV'T, P.H.S.; URSODEOXYCHOLIC ACID;

EID: 0028868935     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: None     Document Type: Article

References (61)

1. Zarling, E. G., and Rhodes, J. B. Colorectal cancer: its changing distribution and guidelines for early detection. Intern. Med. Spec, 3: 72–86, 1982.
2. Pretlow, T. P., Brasitus, T. A., Fulton, N. C., Cheyer, C., and Kaplan, E. L. K-ras mutations in putative preneoplastic lesions in human colon. J. Natl. Cancer Inst., 85: 2004–2007, 1993.
3. Vogelstein, B., and Kinzler, K. W. The multistep nature of cancer. Trends Genet., 9: 138–141, 1993.
4. Guillem, J. G., O'Brian, C. A., Fitzer, C. J., Forde, K. A., LoGerfo, P., Treat, M., and Weinstein, I. B. Altered levels of protein kinase C and Ca2+-dependent protein kinases in human colon carcinomas. Cancer Res., 47: 2036–2039, 1987.
5. Kopp, R., Noelke, B., Sauter, G., Schildberg, F. W., Paumgartner, G., and Pfeiffer, A. Altered protein kinase C activity in biopsies of human colonic adenomas and carcinomas. Cancer Res., 51: 205–210, 1991.
6. Kahl-Rainer, P., Karner-Hanusch, J., Weiss, W., and Marian, B. Five of six protein kinase C isoenzymes present in normal mucosa show reduced protein levels during tumor development in the human colon. Carcinogenesis (Lond.), 75: 779–782, 1994.
7. Craven, P. A., and DeRubertis, F. R. Alterations in protein kinase C in 1,2-dimeth-ylhydrazine induced colonic carcinogenesis. Cancer Res., 52: 2216–2221, 1992.
8. Weinstein, I. B. The roles of specific isoforms of protein kinase C in growth control and human colon cancer. Princess Takamatsu Symposia, 22: 277–283, 1991.
9. Weinstein, I. B. Growth factors, oncogenes, and multistage carcinogenesis. J. Cell. Biochem., 33: 213–224, 1987.
10. Nishizuka, Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science (Washington DC), 258: 607–614, 1992.
11. Dekker, L. V., and Parker, P. J. Protein kinase C: a question of specificity. Trends Biochem. Sci., 19: 73–77, 1994.
12. Bissonnette, M., Tien, X.-Y., Niedziela, S. M., Hartmann, S. C., Frawley, B. P., Jr., Roy, H. K., Sitrin, M. D., Perlman, R. L., and Brasitus, T. A. l,25(OH)2 vitamin D3 activates PKC-α in Caco-2 cells: a mechanism to limit secosteroid-induced rise in [Ca2+]i. Am. J. Physiol., 267: G465–G475, 1994.
13. Khare, S., Tien, X.-Y., Wilson, D., Wali, R. K., Bissonnette, B. M., Scaglione-Sewell, B., Sitrin, M. D., and Brasitus, T. A. The role of protein kinase-Ccr in the activation of particulate guanylate cyclase by la, 25-dihydroxyvitamin D3 in Caco-2 cells. Endocrinology, 135: 277–283, 1994.
14. Diaz-Meco, M. T., Berra, E., Municio, M. M., Sanz, L., Lozano, J., Dominguez, I., Diaz-Golpe, V., Lain de Lera, M. T., Alcami, J., Paya, C. V., Arenzana-Seisdedos, F., Virelizier, J.-L., and Moscat, J. A dominant negative protein kinase C ζ subspecies blocks NF-kB activation. Mol. Cell. Biol., 13: 4770–4775, 1993.
15. Mischak, H., Goodnight, J., Kolch, W., Martiny-Baron, G., Schaechtle, C., Kazanietz, M. G., Blumberg, P. M., Pierce, J. H., and Mushinski, J. F. Overex-pression of protein kinase C-δ and -ϵ in NIH 3T3 cells induces opposite effects on growth, morphology, anchorage dependence, and tumorigenicity. J. Biol. Chem., 268: 6090–6096, 1993.
16. Guillem, J. G., O'Brian, C. A., Fitzer, C. J., Johnson, M. D., Forde, K. A., LoGerfo, P., and Weinstein, I. B. Studies on protein kinase C and colon carcinogenesis. Arch. Surg., 722; 1475–1478, 1987.
17. Kusunoki, M., Sakanoue, Y., Hatada, T., Yanagi, H., Yamamura, T., and Utsunomiya, J. Protein kinase C activity in human colonic adenoma and colorectal carcinoma. Cancer (Phila.), 69: 24–30, 1992.
18. Sakanoue, Y., Hatada, T., Kusunoki, M., Yanagi, H., Yamamura, T., and Utsunomiya, J. Protein kinase C activity as marker for colorectal cancer. Int. J. Cancer, 48: 803–806, 1991.
19. DeRubertis, F. R., and Craven, P. A. Early alterations in rat colonic mucosal nucleotide metabolism and protein kinase activity induced by 1,2-dimethylhydrazine. Cancer Res., 40: 4589–4598, 1980.
20. Brasitus, T. A., Dudeja, P. K., and Dahiya, R. Premalignant alterations in the lipid composition and fluidity of colonic brush border membranes in rats administered 1,2-dimethylhydrazine. J. Clin. Invest., 77: 831–840, 1988.
21. Baum, C. L., Wali, R. K., Sitrin, M. D., Bolt, M. J. G., and Brasitus, T. A. 1,2-Dimethylhydrazine-induced alterations in protein kinase C activity in the rat preneoplastic colon. Cancer Res., 50: 3915–3920, 1990.
22. Wali, R. K., Baum, C. L., Bolt, M. J. G., Dudeja, P. K., Sitrin, M. D., and Brasitus, T. A. Down-regulation of protein kinase C activity in 1,2-dimethylhydrazine-induced rat colonic tumors. Biochim. Biophys. Acta, 7092: 119–123, 1991.
23. Reddy, B. S., and Wynder, E. L. Large bowel carcinogenesis: fecal constituents of populations with diverse incidence rates of colon cancer. J. Natl. Cancer Inst., 50: 1437–1442, 1973.
24. Draser, B. S., and Irving, D. Environmental factors and cancer of the colon and breast. Br. J. Cancer, 27: 167–172, 1973.
25. Wynder, E. L., and Reddy, B. S. Metabolic epidemiology of colorectal cancer. Cancer (Phila.), 34: 801–806, 1974.
26. McSherry, C. K., Cohen, B. I., Bokkenheuser, V. D., Mosbach, E. H., Winter, J., Matoba, N., and Scholes, J. Effects of calcium and bile acid feeding on colon tumors in the rat. Cancer Res., 49: 6039–6043, 1989.
27. Earnest, D. L., Holubec, H., Wali, R. K., Jolley, C. S., Bissonnette, M., Bhatta-charyya, A. K., Roy, H., Khare, S., and Brasitus, T. A. Chemoprevention of azoxymethane-induced colonic carcinogenesis by supplemental dietary ursodeoxycholic acid. Cancer Res., 54: 5071–5074, 1994.
28. Craven, P. A., Pfanstiel, J., and DeRubertis, F. R. Role of activation of protein kinase C in the stimulation of colonic epithelial proliferation and reactive oxygen formation by bile acids. J. Clin. Invest., 79: 532–541, 1987.
29. Fitzer, C. J., O'Brian, C. A., Guillem, J. G., and Weinstein, I. B. The regulation of protein kinase C by chenodeoxycholate, deoxycholate and several structurally related bile acids. Carcinogenesis (Lond.), 8: 217–220, 1987.
30. Pongracz, J., Clark, P., Neoptolemos, J. P., and Lord, J. M. Expression of protein kinase C isoenzymes in colorectal tissue and their differential activation by different bile acids. Int. J. Cancer, 61: 35–39, 1995.
31. Ward, A., Brogden, R. N., Heel, R. C., Speight, T. M., and Avery, G. S. Ursodeoxycholic acid: a review of its pharmacological properties and therapeutic efficacy. Drugs, 27: 95–131, 1984.
32. Rodrigues, C. M., Kren, B. T., Steer, C. J., and Setchell, K. D. Tauroursodeoxycholate increases rat liver ursodeoxycholate levels and limits lithocholate formation better than ursodeoxycholate. Gastroenterology, 709: 564–572, 1995.
33. Levy, M. F., Pocsidio, J., Guillem, J. G., Forde, K., LoGerfo, P., and Weinstein, I. B. Decreased levels of protein kinase C enzyme activity and protein kinase C mRNA in primary colon tumors. Dis. Colon Rectum, 36: 913–921, 1993.
34. Craven, P. A., and DeRubertis, F. R. Loss of protein kinase C δ isozyme immuno-reactivity in human adenocarcinomas. Dig. Dis. Sci., 39: 481–489, 1994.
35. Davidson, L. A., Jiang, Y. H., Derr, J. N., Aukema, H. M., Lupton, J. R., and Chapkin, R. S. Protein kinase C isoforms in human and rat colonic mucosa. Arch. Biochem. Biophys., 572: 547–553, 1994.
36. Bissonnette, M., Wali, R. K., Hartmann, S. C., Niedziela, S. M., Roy, H. K., Tien, X.-Y., Sitrin, M. D., and Brasitus, T. A. 1,25(OH)2 Vitamin D3 and TPA cause differential activation of Ca2+-dependent and Ca2+-independent isoforms of protein kinase C in rat colonocytes. J. Clin. Invest., 95: 2215–2221, 1995.
37. Schaffner, W., and Weissmann, C. A rapid, sensitive and specific method for the determination of protein in dilute solution. Anal. Biochem., 56: 502–514, 1973.
38. Batlle, E., Fabre, M., and Garcia de Herreros, A. Antipeptide antibodies directed against the C-terminus of protein kinase Cζ (PKCζ) react with a Ca2+- and TPA-sensitive PKC in HT-29 human intestinal epithelial cells. FEBS Lett., 344: 161–165, 1994.
39. Roy, H. K., Bissonnette, M., Wali, R. K., Frawley, B., Earnest, D. L., and Brasitus, T. A. Selective preservation of protein kinase C-ζ in the chemoprevention of azoxymethane-induced colonic tumors by piroxicam. FEBS Lett., 366: 143–145, 1995.
40. Snedecor, G. W., and Cochran, W. G. Analysis of Variances in “Statistical Methods,” pp. 215–233. Ames, IA: Iowa State University Press, 1980.
41. Wali, R. K., Bissonnette, M., Khare, S., Niedziela, S., Scaglione-Sewell, B., Earnest, D. L., and Brasitus, T. A. Chemoprotective ursodeoxycholic acid, but not chemopro-motional cholic acid, prevents the activation of PKC-β11,, and PKC-ζ in the azoxymeth-ane model of colon cancer. Gastroenterology (Abstract), 108: 550, 1995.
42. Kiley, S. C., Parker, P. J., Fabbro, D., and Jaken, S. Differential regulation of protein kinase C isozymes by thyrotropin-releasing hormone in GH4C, cells. J. Biol. Chem., 266: 23761–23768, 1991.
43. Saxon, M. L., Zhao, X., and Black, J. D. Activation of protein kinase C isozymes is associated with post-mitotic events in intestinal epithelial cells in situ. J. Cell Biol., 126: 747–763, 1994.
44. Sasaguri, T., Kosaka, C., Hirata, M., Masuda, J., Shimokado, K., Fujishima, M., and Ogata, J. Protein kinase C-mediated inhibition of vascular smooth muscle cell proliferation: the isoforms that may mediate G,/S inhibition. Exp. Cell. Res., 208: 311–320, 1993.
45. Mischak, H., Pierce, J. H., Goodnight, J., Kazanietz, M. G., Blumberg, P. M., and Mushinski, J. F. Phorbol ester-induced myeloid differentiation is mediated by protein kinase C-α and -δ and not by protein kinase C-βII, -ϼ;, -ζ, and -η. J. Biol. Chem., 268: 20110–20115, 1993.
46. Borner, C., Ueffing, M., Jaken, S., Parker, P. J., and Weinstein, I. B. Two closely related isoforms of protein kinase C produce reciprocal effects on the growth of rat fibroblasts. J. Biol. Chem., 270: 78–86, 1995.
47. Scaglione-Sewell, B. A., Abraham, C., Davidson, N. O., Davis, B., Bissonnette, M., and Brasitus, T. A. Alterations in expression of protein kinase C-a in Caco-2 cells result in changes in cellular proliferation. Gastroenterology (Abstract), 108: 534, 1995.
48. Watanabe, T., Ono, Y., Taniyama, Y., Hazama, K., Igarashi, K., Ogita, K., Kikkawa, U., and Nishizuka, Y. Cell division arrest induced by phorbol ester in CHO cells overexpressing protein kinase C-δ subspecies. Proc. Natl. Acad. Sci. USA, 89: 10159–10163, 1992.
49. Murray, N. R., Baumgardner, G. P., Burns, D. J., and Fields, A. P. Protein kinase C isotypes in human erythroleukemia (K562) cell proliferation and differentiation. Evidence that βII protein kinase C is required for proliferation. J. Biol. Chem., 268: 15847–15853, 1993.
50. Dominguez, I., Diaz-Meco, M. T., Municio, M. M., Berra, E., de Herreros, A. G., Cornet, M. E., Sanz, L., and Moscat, J. Evidence for a role of protein kinase C ζ subspecies in maturation of Xenopus laevis oocytes. Mol. Cell. Biol., 12: 3776–3783, 1992.
51. Khalil, R. A., Lajoie, C., Resnick, M. S., and Morgan, K. G. Ca2+-independent isoforms of protein kinase C differentially translocate in smooth muscle. Am. J. Physiol., 262: C714–C719, 1992.
52. Simboli-Campbell, M., Gagnon, A. M., Franks, D. J., and Welsh, J. E. 1,25-dihydroxyvitamin D3 translocates protein kinase C β to nucleus and enhances plasma membrane association of protein kinase C α in renal epithelial cells. J. Biol. Chem., 269: 3257–3264, 1994.
53. Dominguez, I., Sanz, L., Arenzana-Seisdedos, F., Diaz-Meco, M. T., Virelizier, J.-L., and Moscat, J. Inhibition of protein kinase C ζ subspecies blocks the activation of an NF-κB-like activity in Xenopus laevis oocytes. Mol. Cell. Biol., 13: 1290–1295, 1993.
54. Goss, V. L., Hocevar, B. A., Thompson, L. J., Stratton, C. A., Bums, D. J., and Fields, A. P. Identification of nuclear βII protein kinase C as a mitotic lamin kinase. J. Biol. Chem., 269: 19074–19080, 1994.
55. Cacace, A. M., Guadagno, S. N., Krauss, R. S., Fabbro, D., and Weinstein, I. B. The epsilon isoform of protein kinase C is an oncogene when overexpressed in rat fibroblasts. Oncogene, 8: 2095–2104, 1993.
56. Magnuson, B. A., Shirtliff, N., and Bird, R. P. Resistance of aberrant crypt foci to apoptosis induced by azoxymethane in rats chronically fed cholic acid. Carcinogenesis (Lond.), 75: 1459–1462, 1994.
57. Magnuson, B. A., Can, I., and Bird, R. P. Ability of aberrant crypt foci characteristics to predict colonic tumor incidence in rats fed cholic acid. Cancer Res., 53: 4499–4504, 1993.
58. Earnest, D., Batta, A., Holubec, H., Jolley, C. S., Brasitus, T., and Salen, G. Chemoprevention of colon cancer by ursodeoxycholic acid: a possible mechanism of action. Gastroenterology (Abstract), 108: 463, 1995.
59. Nakanishi, H., Brewer, K. A., and Exton, J. H. Activation of the ζ isoform of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem., 268: 13–16, 1993.
60. Diaz-Meco, M. T., Lozano, J., Municio, M. M., Berra, E., Frutos, S., Sanz, L., and Moscat, J. Evidence for the in vitro and in vivo interaction of Ras with protein kinase C ζ. J. Biol. Chem., 269: 31706–31710, 1994.
61. Bradshaw, D., Hill, C. H., Nixon, J. S., and Wilkinson, S. E. Therapeutic potential of protein kinase C inhibitors. Agents Actions, 38: 135–147, 1993.