Inhibition of p53 sensitizes MCF-7 cells to ceramide treatment

International Journal of Oncology

Volumn 37, Issue 1, 2010, Pages 21-30

  Struckhoff, Amanda P ^a   Patel, Bhumi ^b   Beckman, Barbara S ^b  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE; CYCLIN D1; CYCLIN E; PIFITHRIN ALPHA; PROTEIN P21; PROTEIN P53; SMALL INTERFERING RNA; 2-OCTADECANOYLAMINO-1,3-DIHYDROXY-OCTADECENE-4; ANTINEOPLASTIC AGENT; BENZOTHIAZOLE DERIVATIVE; CYCLIN D; CYCLIN DEPENDENT KINASE INHIBITOR 1A; PIFITHRIN; TOLUENE;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL DEATH; CELL PROLIFERATION; CELL STRAIN MCF 7; CELL VIABILITY; CYTOTOXICITY; DNA CONTENT; DRUG EFFECT; DRUG INHIBITION; DRUG SENSITIVITY; HUMAN; HUMAN CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; CARCINOMA; CELL CYCLE; DRUG EFFECTS; DRUG POTENTIATION; DRUG SCREENING; FEMALE; GENE EXPRESSION REGULATION; GENETICS; PATHOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BENZOTHIAZOLES; BREAST NEOPLASMS; CARCINOMA; CELL CYCLE; CELL LINE, TUMOR; CERAMIDES; CYCLIN D; CYCLIN E; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DRUG EVALUATION, PRECLINICAL; DRUG SYNERGISM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; RNA, SMALL INTERFERING; TOLUENE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77953210135     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo_00000649     Document Type: Article

References (74)

1. Kolesnick RN and Clegg S: 1,2-Diacylglycerols, but not phorbol esters, activate a potential inhibitory pathway for protein kinase C in GH3 pituitary cells. Evidence for involvement of a sphingomyelinase. J Biol Chem 263: 6534-6537, 1988.
2. Chatterjee S: Neutral sphingomyelinase action stimulates signal transduction of tumor necrosis factor-alpha in the synthesis of cholesteryl esters in human fibroblasts. J Biol Chem 269: 879-882, 1994.
3. Okamoto Y, Obeid LM and Hannun YA: Bcl-xL interrupts oxidative activation of neutral sphingomyelinase. FEBS Lett 530: 104-108, 2002. (Pubitemid 35248194)
4. Schutze S, Potthoff K, Machleidt T, et al: TNF activates NF-kappa B by phosphatidylcholine-specific phospholipase C-induced 'acidic' sphingomyelin breakdown. Cell 71: 765-776, 1992.
5. Senchenkov A, Litvak DA and Cabot MC: Targeting ceramide metabolism - a strategy for overcoming drug resistance. J Natl Cancer Inst 93: 347-357, 2001.
6. Litvak DA, Bilchik AJ and Cabot MC: Modulators of ceramide metabolism sensitize colorectal cancer cells to chemotherapy: a novel treatment strategy. J Gastrointest Surg 7: 140-148, 2003.
7. Olshefski RS and Ladisch S: Glucosylceramide synthase inhibition enhances vincristine-induced cytotoxicity. Int J Cancer 93: 131-138, 2001.
8. Di Bartolomeo S and Spinedi A: Differential chemosensitizing effect of two glucosylceramide synthase inhibitors in hepatoma cells. Biochem Biophys Res Commun 288: 269-274, 2001.
9. Michael JM, Lavin MF and Watters DJ: Resistance to radiation-induced apoptosis in Burkitt's lymphoma cells is associated with defective ceramide signaling. Cancer Res 57: 3600-3605, 1997.
10. Chmura SJ, Nodzenski E, Beckett MA, et al: Loss of ceramide production confers resistance to radiation-induced apoptosis. Cancer Res 57: 1270-1275, 1997.
11. Ogretmen B and Hannun YA: Updates on functions of ceramide in chemotherapy-induced cell death and in multidrug resistance. Drug Resist Updat 4: 368-377, 2001. (Pubitemid 34746871)
12. Cai Z, Bettaieb A, Mahdani NE, et al: Alteration of the sphingomyelin/ceramide pathway is associated with resistance of human breast carcinoma MCF7 cells to tumor necrosis factor-alpha-mediated cytotoxicity. J Biol Chem 272: 6918-6926, 1997. (Pubitemid 27166390)
13. Wang XZ, Beebe JR, Pwiti L, et al: Aberrant sphingolipid signaling is involved in the resistance of prostate cancer cell lines to chemotherapy. Cancer Res 59: 5842-5848, 1999.
14. Itoh M, Kitano T, Watanabe M, et al: Possible role of ceramide as an indicator of chemoresistance: decrease of the ceramide content via activation of glucosylceramide synthase and sphingomyelin synthase in chemoresistant leukemia. Clin Cancer Res 9: 415-423, 2003. (Pubitemid 36109759)
15. Struckhoff AP, Bittman R, Burow ME, et al: Novel ceramide analogs as potential chemotherapeutic agents in breast cancer. J Pharmacol Exp Ther 309: 523-532, 2004. (Pubitemid 38542603)
16. Blagosklonny MV: Loss of function and p53 protein stabilization. Oncogene 15: 1889-1893, 1997.
17. Poluha W, Poluha DK, Chang B, et al: The cyclin-dependent kinase inhibitor p21 (WAF1) is required for survival of differentiating neuroblastoma cells. Mol Cell Biol 16: 1335-1341, 1996.
18. Harper JW, Adami GR, Wei N, et al: The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75: 805-816, 1993.
19. Formenti SC, Dunnington G, Uzieli B, et al: Original p53 status predicts for pathological response in locally advanced breast cancer patients treated preoperatively with continuous infusion 5-fluorouracil and radiation therapy. Int J Radiat Oncol Biol Phys 39: 1059-1068, 1997.
20. Aas T, Borresen AL, Geisler S, et al: Specific P53 mutations are associated with de novo resistance to doxorubicin in breast cancer patients. Nat Med 2: 811-814, 1996. (Pubitemid 26225099)
21. Brown JM and Wouters BG: Apoptosis, p53, and tumor cell sensitivity to anticancer agents. Cancer Res 59: 1391-1399, 1999.
22. Ghosh S, Mendoza T, Ortiz LA, et al: Bleomycin sensitivity of mice expressing dominant-negative p53 in the lung epithelium. Am J Respir Crit Care Med 166: 890-897, 2002.
23. Wahl AF, Donaldson KL, Fairchild C, et al: Loss of normal p53 function confers sensitization to Taxol by increasing G2/M arrest and apoptosis. Nat Med 2: 72-79, 1996. (Pubitemid 26029571)
24. Fan S, Smith ML, Rivet DJ II, et al: Disruption of p53 function sensitizes breast cancer MCF-7 cells to cisplatin and pentoxifylline. Cancer Res 55: 1649-1654, 1995.
25. Cassinelli G, Supino R, Perego P, et al: A role for loss of p53 function in sensitivity of ovarian carcinoma cells to taxanes. Int J Cancer 92: 738-747, 2001. (Pubitemid 32385719)
26. Taniguchi TEH, Chikstsu N, Uchimaru K and Matsuda T: Sodium butyrate induces growth arrest and senscence-like phenotypes in gynecological cancer cells. Blood 94: 257-267, 2001.
27. Scandurro AB and Beckman BS: Common proteins bind mRNAs encoding erythropoietin, tyrosine hydroxylase, and vascular endothelial growth factor. Biochem Biophys Res Commun 246: 436-440, 1998.
28. Liu YY, Han TY, Giuliano AE, et al: Expression of glucosylceramide synthase, converting ceramide to glucosylceramide, confers adriamycin resistance in human breast cancer cells. J Biol Chem 274: 1140-1146, 1999.
29. Crawford KW, Bittman R, Chun J, et al: Novel ceramide analogues display selective cytotoxicity in drug-resistant breast tumor cell lines compared to normal breast epithelial cells. Cell Mol Biol 49: 1017-1023, 2003.
30. Alesse E, Zazzeroni F, Angelucci A, et al: The growth arrest and downregulation of c-myc transcription induced by ceramide are related events dependent on p21 induction, Rb under-phosphorylation and E2F sequestering. Cell Death Differ 5: 381-389, 1998.
31. Bourbon NA, Sandirasegarane L and Kester M: Ceramide-induced inhibition of Akt is mediated through protein kinase Czeta: implications for growth arrest. J Biol Chem 277: 3286-3292, 2002. (Pubitemid 34953194)
32. Jayadev S, Liu B, Bielawska AE, et al: Role for ceramide in cell cycle arrest. J Biol Chem 270: 2047-2052, 1995.
33. Kuroki J, Hirokawa M, Kitabayashi A, et al: Cell-permeable ceramide inhibits the growth of B lymphoma Raji cells lacking TNF-alpha-receptors by inducing G0/G1 arrest but not apoptosis: a new model for dissecting cell-cycle arrest and apoptosis. Leukemia 10: 1950-1958, 1996.
34. Lee JY, Bielawska AE and Obeid LM: Regulation of cyclin-dependent kinase 2 activity by ceramide. Exp Cell Res 261: 303-311, 2000. (Pubitemid 32010227)
35. Komarov PG, Komarova EA, Kondratov RV, et al: A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 285: 1733-1737, 1999.
36. Culmsee C, Zhu X, Yu QS, et al: A synthetic inhibitor of p53 protects neurons against death induced by ischemic and excitotoxic insults, and amyloid beta-peptide. J Neurochem 77: 220-228, 2001.
37. Kang KH, Kim WH and Choi KH: p21 promotes ceramide-induced apoptosis and antagonizes the antideath effect of Bcl-2 in human hepatocarcinoma cells. Exp Cell Res 253: 403-412, 1999.
38. Oh WJ, Kim WH, Kang KH, et al: Induction of p21 during ceramide-mediated apoptosis in human hepatocarcinoma cells. Cancer Lett 129: 215-222, 1998.
39. 2 response of normal human fibroblasts. Biochem J 347: 543-551, 2000.
40. Gorospe M, Cirielli C, Wang X, et al: p21(Waf1/Cip1) protects against p53-mediated apoptosis of human melanoma cells. Oncogene 14: 929-935, 1997.
41. Waf1/Cip1 as a therapeutic target in breast and other cancers. Cancer Cell 4: 425-429, 2003.
42. Gorospe M, Wang X, Guyton KZ, et al: Protective role of p21(Waf1/Cip1) against prostaglandin A2-mediated apoptosis of human colorectal carcinoma cells. Mol Cell Biol 16: 6654-6660, 1996.
43. Hara S, Nakashima S, Kiyono T, et al: p53-independent ceramide formation in human glioma cells during gamma-radiation-induced apoptosis. Cell Death Differ 11: 853-861, 2004.
44. Sawada M, Kiyono T, Nakashima S, et al: Molecular mechanisms of TNF-alpha-induced ceramide formation in human glioma cells: P53-mediated oxidant stress-dependent and -independent pathways. Cell Death Differ 11: 997-1008, 2004.
45. Sawada M, Nakashima S, Kiyono T, et al: p53 regulates ceramide formation by neutral sphingomyelinase through reactive oxygen species in human glioma cells. Oncogene 20: 1368-1378, 2001.
46. Dbaibo GS, Pushkareva MY, Rachid RA, et al: p53-dependent ceramide response to genotoxic stress. J Clin Invest 102: 329-339, 1998.
47. Bras A, Albar JP, Leonardo E, et al: Ceramide-induced cell death is independent of the Fas/Fas ligand pathway and is prevented by Nur77 overexpression in A20 B cells. Cell Death Differ 7: 262-271, 2000.
48. Lopez-Marure R, Ventura JL, Sanchez L, et al: Ceramide mimics tumour necrosis factor-alpha in the induction of cell cycle arrest in endothelial cells. Induction of the tumour suppressor p53 with decrease in retinoblastoma/protein levels. Eur J Biochem 267: 4325-4333, 2000.
49. Willaime S, Vanhoutte P, Caboche J, et al: Ceramide-induced apoptosis in cortical neurons is mediated by an increase in p38 phosphorylation and not by the decrease in ERK phosphorylation. Eur J Neurosci 13: 2037-2046, 2001
50. Kim SS, Chae HS, Bach JH, et al: P53 mediates ceramide-induced apoptosis in SKN-SH cells. Oncogene 21: 2020-2028, 2002.
51. Yang J and Duerksen-Hughes PJ: Activation of a p53-independent, sphingolipid-mediated cytolytic pathway in p53-negative mouse fibroblast cells treated with N-methyl-N-nitro-N-nitrosoguanidine. J Biol Chem 276: 27129-27135, 2001.
52. Kim WH, Kang KH, Kim MY, et al: Induction of p53-independent p21 during ceramide-induced G1 arrest in human hepatocarcinoma cells. Biochem Cell Biol 78: 127-135, 2000.
53. Kirch HC, Flaswinkel S, Rumpf H, et al: Expression of human p53 requires synergistic activation of transcription from the p53 promoter by AP-1, NF-kappaB and Myc/Max. Oncogene 18: 2728-2738, 1999.
54. Cip1/Waf1 by tumor necrosis factor (alpha) induces growth arrest and cytoprotection in normal human keratinocytes. Mol Cancer Res 1: 262-270, 2003.
55. Hellin A-C, Bentires-Alj M, Verlaet M, et al: Roles of nuclear factor-kappa B, p53, and p21/WAF1 in Daunomycin-induced cell cycle arrest and apoptosis. J Pharmacol Exp Ther 295: 870-878, 2000.
56. Gooch JL, Herrera RE and Yee D: The role of p21 in interferon gamma-mediated growth inhibition of human breast cancer cells. Cell Growth Differ 11: 335-342, 2000.
57. WAF1/CIP1 mediated by STAT1. Science 272: 719-722, 1996.
58. De Siervi A, Marinissen M, Diggs J, et al: Transcriptional activation of p21(waf1/cip1) by alkylphospholipids: role of the mitogen-activated protein kinase pathway in the transactivation of the human p21(waf1/cip1) promoter by Sp1. Cancer Res 64: 743-750, 2004.
59. Chung YW, Jeong DW, Won JY, et al: H(2)O(2)-induced AP-1 activation and its effect on p21(WAF1/CIP1)-mediated G2/M arrest in a p53-deficient human lung cancer cell. Biochem Biophys Res Commun 293: 1248-1253, 2002.
60. Siddiqui RA, Jenski LJ, Harvey KA, et al: Cell-cycle arrest in Jurkat leukaemic cells: a possible role for docosahexaenoic acid. Biochem J 371: 621-629, 2003.
61. Spyridopoulos I, Mayer P, Shook KS, et al: Loss of cyclin A and G1-cell cycle arrest are a prerequisite of ceramide-induced toxicity in human arterial endothelial cells. Cardiovasc Res 50: 97-107, 2001.
62. Gewirtz DA: Growth arrest and cell death in the breast tumor cell in response to ionizing radiation and chemotherapeutic agents which induce DNA damage. Breast Cancer Res Treat 62: 223-235, 2000.
63. Garcia-Ruiz C, Colell A, Mari M, et al: Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. Role of mitochondrial glutathione. J Biol Chem 272: 11369-11377, 1997.
64. Gudz TI, Tserng K-Y and Hoppel CL: Direct inhibition of mitochondrial respiratory chain complex III by cell-permeable ceramide. J Biol Chem 272: 24154-24158, 1997.
65. Suematsu N, Tsutsui H, Wen J, et al: Oxidative stress mediates tumor necrosis factor-alpha-induced mitochondrial DNA damage and dysfunction in cardiac myocytes. Circulation 107: 1418-1423, 2003.
66. Guidarelli A, Clementi E, De Nadai C, et al: TNFalpha enhances the DNA single-strand breakage induced by the short-chain lipid hydroperoxide analogue tert-butylhydroperoxide via ceramide-dependent inhibition of complex III followed by enforced superoxide and hydrogen peroxide formation. Exp Cell Res 270: 56-65, 2001.
67. Galvano F, Campisi A, Russo A, et al: DNA damage in astrocytes exposed to fumonisin B1. Neurochem Res 27: 345-351, 2002.
68. Maurer BJ, Melton L, Billups C, et al: Synergistic cytotoxicity in solid tumor cell lines between N-(4-hydroxyphenyl)retinamide and modulators of ceramide metabolism. J Natl Cancer Inst 92: 1897-1909, 2000.
69. Santana P, Pena LA, Haimovitz-Friedman A, et al: Acid sphingomyelinase-deficient human lymphoblasts and mice are defective in radiation-induced apoptosis. Cell 86: 189-199, 1996.
70. WAF1/CIP1 sensitizes MCF-7 carcinoma cells to TNF-induced apoptosis. Biochem Biophys Res Commun 245: 691-697, 1998.
71. Drane P, Leblanc V, Miro-Mur F, et al: Accumulation of an inactive form of p53 protein in cells treated with TNF alpha. Cell Death Differ 9: 527-537, 2002.
72. Vancurova I, Wu R, Miskolci V, et al: Increased p50/p50 NF-kappaB activation in human papillomavirus type 6- or type 11-induced laryngeal papilloma tissue. J Virol 76: 1533-1536, 2002.
73. Elledge RM and Allred DC: The p53 tumor suppressor gene in breast cancer. Breast Cancer Res Treat 32: 39-47, 1994.
74. Ziyaie D, Hupp TR and Thompson AM: p53 and breast cancer. Breast 9: 239-246, 2000.