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PMID: 7560079 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Phorbol esters induce death in MCF-7 breast cancer cells with altered expression of protein kinase C isoforms. Role for p53-independent induction of gadd-45 in initiating death.

The Journal of clinical investigation ·Vol. 96 ·No. 4 ·1995-10-00 ·Pages 1874-86

de Vente JE, Kukoly CA, Bryant WO, Posekany KJ, Chen J, Fletcher DJ, Parker PJ, Pettit GJ, Lozano G, Cook PP

Abstract

Protein kinase C (PKC) modulates growth, differentiation and apoptosis in a cell-specific fashion. Overexpression of PKC-alpha in MCF-7 breast cancer cells (MCF-7-PKC-alpha cell) leads to expression of a more transformed phenotype. The response of MCF-7 and MCF-7-PKC-alpha cells to phorbol esters (TPA) was examined. TPA-treated MCF-7 cells demonstrated a modest cytostatic response associated with a G1 arrest that was accompanied by Cip1 expression and retinoblastoma hypophosphorylation. While p53 was detected in MCF-7 cells, evidence for TPA-induced stimulation of p53 transcriptional activity was not evident. In contrast, TPA treatment induced death of MCF-7-PKC-alpha cells. Bryostatin 1, another PKC activator, exerted modest cytostatic effects on MCF-7 cells while producing a cytotoxic response at low doses in MCF-7-PKC-alpha cells that waned at higher concentrations. TPA-treated MCF-7-PKC-alpha cells accumulated in G2/M, did not express p53, displayed decreased Cip1 expression, and demonstrated a reduction in retinoblastoma hypophosphorylation. TPA-treated MCF-7-PKC-alpha cells expressed gadd-45 which occurred before the onset of apoptosis. Thus, alterations in the PKC pathway can modulate the decision of a breast cancer cell to undergo death or differentiation. In addition, these data show that PKC activation can induce expression of gadd45 in a p53-independent fashion.

MeSH Terms
Apoptosis Breast Neoplasms/pathology Bryostatins Cell Cycle/drug effects Cyclin-Dependent Kinase Inhibitor p21 Cyclins/biosynthesis Dose-Response Relationship, Drug Female Genes, p53/physiology Humans Intracellular Signaling Peptides and Proteins Isoenzymes/analysis Lactones/pharmacology Macrolides Phosphorylation Protein Kinase C/analysis Proteins/physiology Retinoblastoma Protein/metabolism Tetradecanoylphorbol Acetate/pharmacology Tumor Cells, Cultured
Chemicals
Bryostatins CDKN1A protein, human Cyclin-Dependent Kinase Inhibitor p21 Cyclins GADD45 protein Intracellular Signaling Peptides and Proteins Isoenzymes Lactones Macrolides Proteins Retinoblastoma Protein bryostatin 1 Protein Kinase C Tetradecanoylphorbol Acetate
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
de Vente J E
Department of Medicine, East Carolina University School of Medicine, Greenville, North Carolina 27858, USA.
Kukoly C A
Bryant W O
Posekany K J
Chen J
Fletcher D J
Parker P J
Pettit G J
Lozano G
Cook P P
References (48)
48 references, click to expand
  1. Elevated protein kinase C expression in human breast tumor biopsies relative to normal breast tissue.
    Cancer Res. 1989 Jun 15;49(12):3215-7 PMID: 2720675
  2. Effects of chronic phorbol ester treatment on protein kinase C activity, content, and gene expression in the human monoblastoid U937 cell.
    Cell Growth Differ. 1994 Feb;5(2):161-9 PMID: 8180129
  3. Inhibition of DNA fragmentation in thymocytes and isolated thymocyte nuclei by agents that stimulate protein kinase C.
    J Biol Chem. 1989 Aug 15;264(23):13399-402 PMID: 2503500
  4. Cell cycle-dependent regulation of phosphorylation of the human retinoblastoma gene product.
    Science. 1989 Dec 8;246(4935):1300-3 PMID: 2588006
  5. Role of protein kinase C in the inhibition by fibroblast growth factor of apoptosis in serum-depleted endothelial cells.
    Biochem Biophys Res Commun. 1990 Nov 15;172(3):1081-5 PMID: 2244892
  6. Induction by ionizing radiation of the gadd45 gene in cultured human cells: lack of mediation by protein kinase C.
    Mol Cell Biol. 1991 Feb;11(2):1009-16 PMID: 1990262
  7. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry.
    J Immunol Methods. 1991 Jun 3;139(2):271-9 PMID: 1710634
  8. Participation of p53 protein in the cellular response to DNA damage.
    Cancer Res. 1991 Dec 1;51(23 Pt 1):6304-11 PMID: 1933891
  9. Induction of apoptosis in chronic lymphocytic leukemia cells and its prevention by phorbol ester.
    Exp Cell Res. 1992 Feb;198(2):367-72 PMID: 1729140
  10. Differential effects of bryostatin 1 and phorbol ester on human breast cancer cell lines.
    Cancer Res. 1992 Mar 1;52(5):1278-83 PMID: 1737390
  11. Acquisition of a growth-inhibitory response to phorbol ester involves DNA damage.
    Cancer Res. 1992 Apr 1;52(7):1907-15 PMID: 1372531
  12. Elevated level of nuclear protein kinase C in multidrug-resistant MCF-7 human breast carcinoma cells.
    Cancer Res. 1992 Jul 1;52(13):3750-9 PMID: 1617646
  13. A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia.
    Cell. 1992 Nov 13;71(4):587-97 PMID: 1423616
  14. Features of apoptotic cells measured by flow cytometry.
    Cytometry. 1992;13(8):795-808 PMID: 1333943
  15. Genotoxic-stress-response genes and growth-arrest genes. gadd, MyD, and other genes induced by treatments eliciting growth arrest.
    Ann N Y Acad Sci. 1992 Nov 21;663:139-53 PMID: 1482047
  16. Mammalian genes induced by radiation; activation of genes associated with growth control.
    Annu Rev Genet. 1992;26:507-26 PMID: 1482123
  17. Inhibition of phorbol ester-induced T cell proliferation by bryostatin is associated with rapid degradation of protein kinase C.
    J Immunol. 1993 Feb 15;150(4):1195-204 PMID: 8432975
  18. Molecular controls of apoptosis: differentiation/growth arrest primary response genes, proto-oncogenes, and tumor suppressor genes as positive & negative modulators.
    Oncogene. 1994 Jul;9(7):1807-12 PMID: 8208526
  19. Induction of WAF1/CIP1 by a p53-independent pathway.
    Cancer Res. 1994 Jul 1;54(13):3391-5 PMID: 8012956
  20. Tumor-promoting phorbol ester transiently down-modulates the p53 level and blocks the cell cycle.
    Cell Growth Differ. 1994 Mar;5(3):329-40 PMID: 8018565
  21. Induction of p21 (WAF-1/CIP1) during differentiation.
    Oncogene. 1994 Nov;9(11):3389-96 PMID: 7936667
  22. Induction of differentiation in human promyelocytic HL-60 leukemia cells activates p21, WAF1/CIP1, expression in the absence of p53.
    Oncogene. 1994 Nov;9(11):3397-406 PMID: 7936668
  23. Bryostatin 1 protects protein kinase C-delta from down-regulation in mouse keratinocytes in parallel with its inhibition of phorbol ester-induced differentiation.
    Mol Pharmacol. 1994 Nov;46(5):840-50 PMID: 7969070
  24. 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. 1995 Apr;95(4):1906-15 PMID: 7706498
  25. Phorbol ester treatment of U937 cells with altered protein kinase C content and distribution induces cell death rather than differentiation.
    Cell Growth Differ. 1995 Apr;6(4):371-82 PMID: 7794805
  26. Cell death: the significance of apoptosis.
    Int Rev Cytol. 1980;68:251-306 PMID: 7014501
  27. Protein kinase C desensitization by phorbol esters and its impact on growth of human breast cancer cells.
    Biochem Biophys Res Commun. 1986 Feb 26;135(1):65-73 PMID: 3513765
  28. 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. 1987 Mar 15;47(6):1615-20 PMID: 3102047
  29. Bryostatin 1, an activator of protein kinase C, inhibits tumor promotion by phorbol esters in SENCAR mouse skin.
    Carcinogenesis. 1987 Sep;8(9):1343-6 PMID: 3621472
  30. Immunological quantitation of phospholipid/Ca2+-dependent protein kinase of human mammary carcinoma cells: inverse relationship to estrogen receptors.
    Int J Cancer. 1987 Sep 15;40(3):344-8 PMID: 3623717
  31. Differing modulation of protein kinase C by bryostatin 1 and phorbol esters in JB6 mouse epidermal cells.
    J Biol Chem. 1988 Jun 15;263(17):8437-42 PMID: 3286649
  32. Inhibition of MCF-7 cell growth by 12-O-tetradecanoylphorbol-13-acetate and 1,2-dioctanoyl-sn-glycerol: distinct effects on protein kinase C activity.
    Cancer Res. 1988 Dec 1;48(23):6943-50 PMID: 3180102
  33. Effects of activators of protein kinase C, including bryostatins 1 and 2, on the growth of A549 human lung carcinoma cells.
    Int J Cancer. 1989 Jan 15;43(1):158-63 PMID: 2910827
  34. p53 is required for radiation-induced apoptosis in mouse thymocytes.
    Nature. 1993 Apr 29;362(6423):847-9 PMID: 8479522
  35. Thymocyte apoptosis induced by p53-dependent and independent pathways.
    Nature. 1993 Apr 29;362(6423):849-52 PMID: 8479523
  36. Cell cycle arrest and growth inhibition by the protein kinase antagonist UCN-01 in human breast carcinoma cells.
    Cancer Res. 1993 May 1;53(9):2081-6 PMID: 7683251
  37. Protein kinase C isoenzymes: divergence in signal transduction?
    Biochem J. 1993 Apr 15;291 ( Pt 2):329-43 PMID: 8484714
  38. Epstein-Barr virus infection is associated with increased apoptosis in untreated and phorbol ester-treated human Burkitt's lymphoma (AW-Ramos) cells.
    Biochem Biophys Res Commun. 1993 May 14;192(3):1415-23 PMID: 8389551
  39. A phase I study of intravenous bryostatin 1 in patients with advanced cancer.
    Br J Cancer. 1993 Aug;68(2):418-24 PMID: 8347500
  40. Analysis of the mammalian gadd45 gene and its response to DNA damage.
    J Biol Chem. 1993 Nov 15;268(32):24385-93 PMID: 8226988
  41. Phase I study of bryostatin 1: assessment of interleukin 6 and tumor necrosis factor alpha induction in vivo. The Cancer Research Campaign Phase I Committee.
    J Natl Cancer Inst. 1993 Nov 17;85(22):1812-8 PMID: 8230261
  42. WAF1, a potential mediator of p53 tumor suppression.
    Cell. 1993 Nov 19;75(4):817-25 PMID: 8242752
  43. Apoptotic death in epithelial cells: cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation.
    EMBO J. 1993 Sep;12(9):3679-84 PMID: 8253089
  44. Differential regulation of protein kinase C isozymes by bryostatin 1 and phorbol 12-myristate 13-acetate in NIH 3T3 fibroblasts.
    J Biol Chem. 1994 Jan 21;269(3):2118-24 PMID: 8294465
  45. WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis.
    Cancer Res. 1994 Mar 1;54(5):1169-74 PMID: 8118801
  46. The gadd and MyD genes define a novel set of mammalian genes encoding acidic proteins that synergistically suppress cell growth.
    Mol Cell Biol. 1994 Apr;14(4):2361-71 PMID: 8139541
  47. Protein kinase C--a question of specificity.
    Trends Biochem Sci. 1994 Feb;19(2):73-7 PMID: 8160269
  48. Hyperinducible gene expression from a metallothionein promoter containing additional metal-responsive elements.
    Gene. 1989 Mar 15;76(1):81-8 PMID: 2744482
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
1995-10-00
Pages
1874-86
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC185824
Subset
IM
Grants
NCI NIH HHS · CA-43823 · United States
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