Alterations in the expression and localization of protein kinase C isoforms during mammary gland differentiation

European Journal of Cell Biology

Volumn 78, Issue 7, 1999, Pages 497-510

  Masso Welch, Patricia A ^a   Verstovsek, Gordana ^a   Ip, Margot M ^a,b  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

Breast; Lactation; Mammary; PKC; Pregnancy

Indexed keywords

ISOENZYME; PROTEIN KINASE C;

ANIMAL TISSUE; ARTICLE; BREAST CARCINOGENESIS; BREAST DEVELOPMENT; BREAST DUCT; BREAST EPITHELIUM; CELL DIFFERENTIATION; CELL NUCLEUS; ENZYME LOCALIZATION; IMMUNOBLOTTING; INVOLUTION; LACTATION; MYOEPITHELIUM; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; RAT; SIGNAL TRANSDUCTION; STAINING;

ANIMALIA;

EID: 0032859859     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/s0171-9335(99)80076-4     Document Type: Article

References (70)

1. Assert, R., H. Schatz, A. Pfeiffer: Upregulation of PKC delta-and downregulation of PKC alpha-mRNA and protein by a phorbol ester in humanT84 cells. FEBS Lett. 388, 195-199 (1996).
2. Banerjee, R., B. K. Vonderhaar: Prolactin-induced protein kinase C activity in a mouse mammary cell line (NOG-8). Mol. Cell. Endocrinol. 90, 61-67 (1992).
3. Barry, S. T., D. R. Critchley: The RhoA-dependent assembly of focal adhesions in Swiss 3T3 cells is associated with increased tyrosine phosphorylation and the recruitment of both pp125FAK and protein kinase C-delta to focal adhesions. J. Cell Sci. 107, 2033-2045 (1994).
4. Birkenfeld, H. P., B. S. McIntyre, K. P. Briski, P. W. Sylvester: Protein kinase C isoenzyme expression in normal mouse mammary epithelial cells grown in primary culture. Proc. Soc. Exp. Biol. Med. 213, 65-70 (1996).
5. Borner, C., S. N. Guadagno, D. Fabbro, I. B. Weinstein: Expression of four protein kinase C isoforms in rat fibroblasts. Distinct subcellular distribution and regulation by calcium and phorbol esters. J. Biol. Chem. 267, 12892-12899 (1992).
6. Borner, C., S. N. Guadagno, L. Hsieh, W. Hsiao, I. B. Weinstein: Transformation by a ras oncogene causes increased expression of protein kinase C-alpha and decreased expression of protein kinase C-epsilon. Cell Growth Differ. 1, 653-660 (1990).
7. Cacace, A. M., S. N. Guadagno, R. S. Krauss, D. Fabbro, I. B. Weinstein: The epsilon isoform of protein kinase C is an oncogene when overexpressed in rat fibroblasts. Oncogene 8, 2095-2104 (1993).
8. Caulfield, J. J., F. F. Bolander, Jr.: Involvement of protein kinase C in mouse mammary gland development. J. Endocrinol. 109, 29-34 (1986).
9. Cho, Y. H., A. P. Tighe, D. A. Talmage: Retinoic acid induced growth arrest of human breast carcinoma cells requires protein kinase C alpha expression and activity. J. Cell. Physiol. 172, 306-313 (1997).
10. Chun, J., M. Ha, B. S. Jacobson: Differential translocation of protein kinase C epsilon during HeLa cell adhesion to a gelatin substratum. J. Biol. Chem. 271, 13008-13012 (1996).
11. Connor, K., R. A. Clegg: Isoenzymes of protein kinase C in rat mammary tissue: changes in properties and relative amounts during pregnancy and lactation. Biochem. J. 291, 817-824 (1993).
12. Darcy, K. M., J. D. Black, H. A. Hahm, M. M. Ip: Mammary organoids from immature virgin rats undergo ductal and alveolar morphogenesis when grown within a reconstituted basement membrane. Exp. Cell Res. 196, 49-65 (1991).
13. Deacon, E. M., J. Pongracz, G. Griffiths, J. M. Lord: Isoenzymes of protein kinase C: Differential involvement in apoptosis and pathogenesis. J. Clin. Pathol. Clin. Mol. Pathol. 50, 124-131 (1997).
14. Dekker, L. V., P. McIntyre, P. J. Parker: Mutagenesis of the regulatory domain of rat protein kinase C-eta: A molecular basis for restricted histone kinase activity. J. Biol. Chem. 268, 19498-19504 (1993).
15. Dlugosz, A. A., C. Cheng, E. K. Williams, A. G. Dharia, M. F. Denning, S. H. Yuspa: Alterations in murine keratinocyte differentiation induced by activated rasHa genes are mediated by protein kinase C-alpha. Cancer Res. 54, 6413-6420 (1994).
16. Dodane, V., B. Kachar: Identification of G proteins and PKC that colocalize with tight junctions. J. Membr. Biol. 149, 199-209 (1996).
17. Dong, L., J. L. Stevens, S. Jaken: Transformation-sensitive localization of alpha-protein kinase C at cell-cell contacts in rat renal proximal tubule epithelial cells. Cell Growth Differ. 4, 793-798 (1993).
18. Fabbro, D., R. Regazzi, S. D. Costa, C. Borner, U. Eppenberger: Protein kinase C desensitization by phorbol esters and its impact on growth of human breast cancer cells. Biochem. Biophys. Res. Commun. 135, 65-72 (1986).
19. Fasano, A., C. Fiorentini, G. Donelli, S. Uzzau, J. B. Kaper, K. Margaretten, X. Ding, S. Guandalini, L. Comstock, S. E. Goldblum: Zonula occludens toxin modulates tight junctions through protein kinase C-dependent actin reorganization, in vitro. J. Clin. Invest. 96, 710-720 (1995).
20. Foncea, R., S. Varela, M. Sapag-Hagar, S. Lavandero: Changes in protein kinase C activity, subcellular distribution and protein phosphorylation during the lactogenic cycle in rat mammary tissue. Res. Commun. Mol. Pathol. Pharmacol. 87, 253-268 (1995).
21. Garcia-Rocha, M., J. Avila, J. Lozano: The zeta isoform of protein kinase C binds to tubulin through the pseudosubstrate domain. Exp. Cell Res. 230, 1-8 (1997).
22. Glukhova, M., V. Koteliansky, X. Sastre, J. Thiery: Adhesion systems in normal breast and in invasive breast carcinoma. Am. J. Pathol. 146, 706-716 (1995).
23. Gomez, J., A. Martinez de Aragon, P. Bonay, C. Pitton, A. Garcia, A. Silva, M. Fresno, F. Alvarez, A. Rebollo: Physical association and functional relationship between protein kinase C zeta and the actin cytoskeleton. Eur. J. Immunol. 25, 2673-2678 (1995).
24. Gordge, P C., M. J. Hulme, R. A. Clegg, W. R. Miller: Elevation of protein kinase A and protein kinase C activities in malignant as compared with normal human breast tissue. Eur. J. Cancer 32A. 2120-2126 (1996).
25. Gruber, J. R., S. Desai, J. K. Blusztajn, R. M. Niles: Retinoic acid specifically increases nuclear PKC alpha and stimulates AP-1 transcriptional activity in B16 mouse melanoma cells. Exp. Cell Res. 221, 377-384 (1995).
26. Guelstein, V. I., T. A. Tchypysheva, V. D. Ermilova, A. V. Ljubimov: Myoepithelial and basement membrane antigens in benign and malignant human breast tumors. Int. J. Cancer 53, 269-277 (1993).
27. Hocevar, B. A., A. P. Fields: Selective translocation of beta II-protein kinase C to the nucleus of human promyelocytic (HL60) leukemia cells. J. Biol. Chem. 266, 28-33 (1991).
28. Hogervorst, F., L. G. Admiraal, C. Niessen, I. Kuikman, H. Janssen, H. Daams, A. Sonnenberg: Biochemical characterization and tissue distribution of the A and B variants of the integrin alpha 6 subunit. J. Cell Biol. 121, 179-191 (1993).
29. Hogervorst, F., I. Kuikman, E. Noteboom, A. Sonnenberg: The role of phosphorylation in activation of the alpha 6A beta 1 laminin receptor. J. Biol. Chem. 268, 18427-18430 (1993).
30. Holladay, C. S., F. F. J. Bolander: Hormonal regulation of protein kinase C in the mouse mammary gland. Proc. Soc. Exp. Biol. Med. 183, 343-347 (1986).
31. Hyatt, S. L., T. Klauck, S. Jaken: Protein kinase C is localized in focal contacts of normal but not transformed fibroblasts. Mol. Carcinog. 3, 45-53 (1990).
32. Hyatt, S. L., L. Liao, C. Chapline, S. Jaken: Identification and characterization of alpha-protein kinase C binding proteins in normal and transformed REF52 cells. Biochemistry 33, 1223-1228 (1994).
33. Jaken, S., K. Leach, T. Klauck: Association of type 3 protein kinase C with focal contacts in rat embryo fibroblasts. J. Cell Biol. 109, 697-704 (1989).
34. Kennedy, M. J., L. J. Prestigiacomo, G. Tyler, W.S. May, N.E. Davidson: Differential effects of bryostatin 1 and phorbol ester on human breast cancer cell lines. Cancer Res. 52, 1278-1283 (1992).
35. Kiley, S. C., J. Welsh, C. Narvaez, S. Jaken: Protein kinase C isozymes and substrates in mammary carcinogenesis. J. Mammary Gland Biol. Neoplasia 1, 177-187 (1996).
36. Knutson, K. L., M. Hoenig: Regulation of distinct pools of protein kinase C delta in beta cells. J. Cell. Biochem. 60, 130-138 (1996).
37. Lehel, C., Z. Olah, G. Jakab, Z. Szallasi, G. Petrovics, G. Harta, P. M. Blumberg, W. B. Anderson: Protein kinase C epsilon subcellular localization domains and proteolytic degradation sites. A model for protein kinase C conformational changes. J. Biol. Chem. 270, 19651-19658 (1995).
38. Lehrich, R. W., J. N. Forrest, Jr.: Protein kinase C zeta is associated with the mitotic apparatus in primary cell cultures of the shark rectal gland. J. Biol. Chem. 269, 32446-32450 (1994).
39. Manni, A., E. Buckwalter, R. Etindi, S. Kunselman, A. Rossini, D. Mauger, D. Dabbs, L. Demers: Induction of a less aggressive breast cancer phenotype by protein kinase C-alpha and -beta overexpression. Cell Growth Differ. 7, 1187-1198 (1996).
40. Marte, B. M., T. Meyer, S. Stabel, G. J. Standke, S. Jaken, D. Fabbro, N. E. Hynes: Protein kinase C and mammary cell differentiation: involvement of protein kinase C alpha in the induction of beta-casein expression. Cell Growth Differ. 5, 239-247 (1994).
41. Masso-Welch, P. A., G. Verstovsek, K. Darcy, C. Tagliarino, M. M. Ip: Protein kinase C eta upregulation and secretion during postnatal rat mammary gland differentiation. Eur. J. Cell Biol. 77, 48-59 (1998).
42. McGarrity, T. J., L. P. Peiffer, E. B. Neely, R. G. Palavarapu, W. A. Kolton, P. Parker, M. K. Howett: Localization of protein kinase C alpha isoform expression in the human gastrointestinal tract. Cell Growth Differ. 7, 953-959 (1996).
43. Mellor, H., P. J. Parker: The extended protein kinase C superfamily. Biochem. J. 332, 281-292 (1998).
44. Mills, K. J., S. B. Bocckino, D. J. Burns, C. R. Loomis, R. C. Smart: Alterations in protein kinase C isozymes alpha and beta 2 in activated Ha-ras containing papillomas in the absence of an increase in diacylglycerol. Carcinogenesis 13, 1113-1120 (1992).
45. Mischak, H., J. A. Goodnight, W. Kolch, G. Martiny-Baron, C. Schaechtle, M. G. Kazanietz, P. M. Blumberg, J. H. Pierce, J. F. Mushinski: Overexpression of protein kinase C-delta and -epsilon in NIH 3T3 cells induces opposite effects on growth, morphology, anchorage dependence, and tumorigenicity. J. Biol. Chem. 268, 6090-6096 (1993).
46. Mischak, H., W. Kolch, J. Goodnight, W. F. Davidson, U. Rapp, S. Rose-John, J. F. Mushinski: Expression of protein kinase C genes in hemopoietic cells is cell type-and B cell differentiation stage-specific. J. Immunol. 147, 3981-3987 (1991).
47. Moreton, K., R. Turner, N. Blake, A. Paton, N. Groome, M. Rumsby: Protein expression of the alpha, gamma, delta and epsilon subspecies of protein kinase C changes as C6 glioma cells become contact inhibited and quiescent in the presence of serum. FEBS Lett. 372, 33-38 (1995).
48. Nakaigawa, N., S.-I. Hirai, K. Mizuno, T. Shuin, M. Hosaka, S. Ohno: Differential effects of overexpression of PKC alpha and PKC delta/epsilon on cellular E2F activity in late G1 phase. Biochem. Biophys. Res. Commun. 222, 95-100 (1996).
49. Niles, R. M.: Interactions between retinoic acid and protein kinase C in induction of melanoma differentiation. Adv. Exp. Med. Biol. 354, 37-57 (1994).
50. O'Brian, C. A., V. G. Vogel, S. E. Singletary, N. E. Ward: Elevated protein kinase C expression in human breast tumor biopsies relative to normal breast tissue. Cancer Res. 49, 3215-3217 (1989).
51. Ogawara, M., N. Inagaki, K. Tsujimura, Y. Takai, M. Sekimata, M. H. Ha, S. Imajoh-Ohmi, S. Hirai, S. Ohno, H. Sugiura, et al.: Differential targeting of protein kinase C and CaM kinase II signalings to vimentin. J. Cell Biol. 131, 1055-1066 (1995).
52. Osborne, C. K., B. Hamilton, M. Nover, J. Ziegler: Antagonism between epidermal growth factor and phorbol ester tumor promoters in human breast cancer cells. J. Clin. Invest. 67, 943-951 (1981).
53. Owen, P. J., G. D. Johnson, J. M. Lord: Protein kinase C-delta associates with vimentin intermediate filaments in differentiated HL60 cells. Exp. Cell Res. 225, 366-373 (1996).
54. Palmantier, R., J. D. Roberts, W. C. Glasgow, T. E. Eling, K. Olden: Regulation of the adhesion of a human breast carcinoma cell line to type IV collagen and vitronectin: Roles for lipoxygenase and protein kinase C. Cancer Res. 56, 2206-2212 (1996).
55. Prekeris, R., M. W. Mayhew, J. B. Cooper, D. M. Terrian: Identification and localization of an actin-binding motif that is unique to the epsilon isoform of protein kinase C and participates in the regulation of synaptic function. J. Cell Biol. 132, 77-90 (1996).
56. Rillema, J. A., M. Sluyser: Increased sensitivity of mouse mammary gland for hormones and tumor promoter 12-O-tetradecanoyl-phorbol-13-acetate in tissues containing the Mtv-2 gene. Horm. Res. 19, 52-56 (1984).
57. Sappino, A. P., O. Skalli, B. Jackson, W. Schürch, G. Gabbiani: Smooth-muscle differentiation in stromal cells of malignant and non-malignant breast tissues. Int. J. Cancer 41, 707-712 (1988).
58. Saxon, M. L., X. Zhao, J. D. Black: 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).
59. Starzec, A., E. Spanakis, A. Nehme, V. Salle, N. Veber, C. Mainguene, P. Planchon, A. Valette, G. Prevost, L. Israel: Proliferative effects of epithelial cells to 8-bromo-cyclic AMP and to a phorbol ester change during breast pathogenesis. J. Cell. Physiol. 161, 31-38 (1994).
60. Stuart, R. O., S. K. Nigam: Regulated assembly of tight junctions by protein kinase C. Proc. Natl. Acad. Sci. USA 92, 6072-6076 (1995).
61. Taketani, Y., T. Oka: Tumor promoter 12-O-tetradecanoylphorbol 13-acetate, like epidermal growth factor, stimulates cell proliferation and inhibits differentiation of mouse mammary epithelial cells in culture. Proc. Natl. Acad. Sci. USA 80, 1646-1649 (1983).
62. Timar, J., B. Liu, R. Bazaz, K. V. Honn: Association of protein kinase-C-alpha with cytoplasmic vesicles in melanoma cells. J. Histochem. Cytochem. 44, 177-182 (1996).
63. Valette, A., N. Gas, S. Jozan, M. A. Roubinet, M. A. Dupont, F. Bayard: Influence of 12-O-tetradecanoylphorbol-13-acetate on proliferation and maturation of human breast carcinoma cells (MCF-7): relationship to cell cycle events. Cancer Res. 47, 1615-1620 (1987).
64. Wada, T., K. M. Darcy, X. Guan, M. M. Ip: Phorbol 12-myristate 13-acetate stimulates proliferation and ductal morphogenesis and inhibits functional differentiation of normal rat mammary epithelial cells in primary culture. J. Cell. Physiol. 158, 97-109 (1994).
65. Warburton, M. J., S. R. Dundas, B. A. Gusterson, M. J. O'Hare: Regulation of urokinase-type plasminogen activator production by rat mammary myoepithelial cells. Exp. Cell Res. 228, 76-83 (1996).
66. Warburton, M. J., D. Mitchell, E. J. Ormerod, P. Rudland: Distribution of myoepithelial cells and basement membrane proteins in the resting, pregnant, lactating, and involuting rat mammary gland. J. Histochem. Cytochem. 30, 667-676 (1982).
67. Waters, S. B., J. A. Rillema: Role of protein kinase C in the prolactin-induced responses in mouse mammary gland explants. Mol. Cell. Endocrinol. 63, 159-166 (1989).
68. Ways, D. K., C. A. Kukoly, J. de Vente, J. L. Hooker, W. O. Bryant, K. J. Posekany, D. J. Fletcher, P. P. Cook, P. J. Parker: MCF-7 breast cancer cells transfected with protein kinase C-alpha exhibit altered expression of other protein kinase C isoforms and display a more aggressive neoplastic phenotype. J. Clin. Invest. 95, 1906-1915 (1995).
69. Williams, J. M., C. W. Daniel: Mammary ductal elongation: Differentiation of myoepithelium and basal lamina during branching morphogenesis. Dev. Biol. 97, 274-290 (1983).
70. Zhou, Y., E. Dziak, M. Opas: Adhesiveness and proliferation of epithelial cells are differentially modulated by activation and inhibition of protein kinase C in a substratum-dependent manner. J. Cell. Physiol. 155, 14-26 (1993).