Regulation by bcl-2, c-myc, and p53 of susceptibility to induction of apoptosis by heat shock and cancer chemotherapy compounds in differentiation-competent and -defective myeloid leukemic cells

HOME

HELP

FEEDBACK

SUBSCRIPTIONS

Regulation by bcl-2, c-myc, and p53 of susceptibility to induction of apoptosis by heat shock and cancer chemotherapy compounds in differentiation-competent and -defective myeloid leukemic cells

J Lotem and L Sachs
Department of Molecular Genetics and Virology, Weizmann Institute of Science, Rehovot, Israel.

Myeloid leukemias that differ in their competence for induction of differentiation were analyzed for expression of bcl-2 and c-myc and for their sensitivity to induction of apoptosis by heat shock and cancer chemotherapy compounds. The M1 leukemia expressed a high level of bcl-2 and showed a much lower susceptibility to induction of apoptosis by heat shock, Adriamycin, 1-beta-D-arabinofuranosylcytosine, methotrexate, and cycloheximide, compared to five other leukemias which expressed a low level of bcl-2. There was no association between susceptibility to induction of apoptosis and competence for induction of differentiation. The difference in susceptibility to methotrexate, which is not regulated by the multidrug resistance (MDR) genes, and treatment with verapamil, which blocks MDR activity, have indicated that the higher resistance of the M1 leukemia to these agents was not due to MDR activity. The results indicate that the level of regulated bcl-2 expression in these myeloid leukemias was associated with cell susceptibility to induction of apoptosis by different apoptosis-inducing agents. Screening for expression of bcl-2 may thus be useful to characterize leukemias regarding susceptibility to induction of apoptosis by different agents. The level of regulated c-myc expressed in these leukemias was not associated with susceptibility to induction of apoptosis. Transfection with a deregulated mutant p53 into the M1 leukemia did not change susceptibility to apoptosis induction, but transfection with deregulated c-myc increased susceptibility to apoptosis.(ABSTRACT TRUNCATED AT 250 WORDS)

This article has been cited by other articles:

T.-T. Ou, C.-J. Wang, G.-U. Hung, C.-H. Wu, and H.-J. Lee
Aqueous Extract of Shi-Liu-Wei-Liu-Qi-Yin Induces G2/M Phase Arrest and Apoptosis in Human Bladder Carcinoma Cells via Fas and Mitochondrial Pathway
Evid. Based Complement. Altern. Med., May 25, 2009; (2009) nep016v2.
[Abstract] [Full Text] [PDF]

C. Shanmugam, V. R. Katkoori, N. C. Jhala, W. E. Grizzle, G. P. Siegal, and U. Manne
p53 Nuclear Accumulation and Bcl-2 Expression in Contiguous Adenomatous Components of Colorectal Adenocarcinomas Predict Aggressive Tumor Behavior
J. Histochem. Cytochem., March 1, 2008; 56(3): 305 - 312.
[Abstract] [Full Text] [PDF]

C. M. Rudin, R. Salgia, X. Wang, L. D. Hodgson, G. A. Masters, M. Green, and E. E. Vokes
Randomized Phase II Study of Carboplatin and Etoposide With or Without the bcl-2 Antisense Oligonucleotide Oblimersen for Extensive-Stage Small-Cell Lung Cancer: CALGB 30103
J. Clin. Oncol., February 20, 2008; 26(6): 870 - 876.
[Abstract] [Full Text] [PDF]

D Trere, L Montanaro, C Ceccarelli, S Barbieri, G Cavrini, D Santini, M Taffurelli, and M Derenzini
Prognostic relevance of a novel semiquantitative classification of Bcl2 immunohistochemical expression in human infiltrating ductal carcinomas of the breast
Ann. Onc., June 1, 2007; 18(6): 1004 - 1014.
[Abstract] [Full Text] [PDF]

H. Biliran Jr., S. Banerjee, A. Thakur, F. H. Sarkar, A. Bollig, F. Ahmed, J. Wu, Y. Sun, and J. D. Liao
c-Myc Induced Chemosensitization Is Mediated by Suppression of Cyclin D1 Expression and Nuclear Factor-{kappa}B Activity in Pancreatic Cancer Cells
Clin. Cancer Res., May 1, 2007; 13(9): 2811 - 2821.
[Abstract] [Full Text] [PDF]

R. Aneja, J. Zhou, B. Zhou, R. Chandra, and H. C. Joshi
Treatment of hormone-refractory breast cancer: apoptosis and regression of human tumors implanted in mice.
Mol. Cancer Ther., September 1, 2006; 5(9): 2366 - 2377.
[Abstract] [Full Text] [PDF]

F. Nagashima, N. Boku, A. Ohtsu, S. Yoshida, T. Hasebe, A. Ochiai, Y. Sakata, H. Saito, Y. Miyata, I. Hyodo, et al.
Biological Markers as a Predictor for Response and Prognosis of Unresectable Gastric Cancer Patients Treated with Irinotecan and Cisplatin
Jpn. J. Clin. Oncol., December 1, 2005; 35(12): 714 - 719.
[Abstract] [Full Text] [PDF]

C. M. Rudin, M. Kozloff, P. C. Hoffman, M. J. Edelman, R. Karnauskas, R. Tomek, L. Szeto, and E. E. Vokes
Phase I Study of G3139, a bcl-2 Antisense Oligonucleotide, Combined With Carboplatin and Etoposide in Patients With Small-Cell Lung Cancer
J. Clin. Oncol., March 15, 2004; 22(6): 1110 - 1117.
[Abstract] [Full Text] [PDF]

A. A. A. M. Danen-van Oorschot, Y.-H. Zhang, S. R. Leliveld, J. L. Rohn, M. C. M. J. Seelen, M. W. Bolk, A. van Zon, S. J. Erkeland, J.-P. Abrahams, D. Mumberg, et al.
Importance of Nuclear Localization of Apoptin for Tumor-specific Induction of Apoptosis
J. Biol. Chem., July 18, 2003; 278(30): 27729 - 27736.
[Abstract] [Full Text] [PDF]

C. M. Rudin, G. A. Otterson, A. M. Mauer, M. A. Villalona-Calero, R. Tomek, B. Prange, C. M. George, L. Szeto, and E. E. Vokes
A pilot trial of G3139, a bcl-2 antisense oligonucleotide, and paclitaxel in patients with chemorefractory small-cell lung cancer
Ann. Onc., April 1, 2002; 13(4): 539 - 545.
[Abstract] [Full Text] [PDF]

D. J. Bearss, R. J. Lee, D. A. Troyer, R. G. Pestell, and J. J. Windle
Differential Effects of p21WAF1/CIP1 Deficiency on MMTV-ras and MMTV-myc Mammary Tumor Properties
Cancer Res., April 1, 2002; 62(7): 2077 - 2084.
[Abstract] [Full Text] [PDF]

J. C. Cusack Jr., R. Liu, M. Houston, K. Abendroth, P. J. Elliott, J. Adams, and A. S. Baldwin Jr.
Enhanced Chemosensitivity to CPT-11 with Proteasome Inhibitor PS-341:: Implications for Systemic Nuclear Factor-{{kappa}}B Inhibition
Cancer Res., May 1, 2001; 61(9): 3535 - 3540.
[Abstract] [Full Text]

A. Sigal and V. Rotter
Oncogenic Mutations of the p53 Tumor Suppressor: The Demons of the Guardian of the Genome
Cancer Res., December 1, 2000; 60(24): 6788 - 6793.
[Abstract] [Full Text]

Y. Ohmura, M. Aoe, A. Andou, and N. Shimizu
Telomerase Activity and Bcl-2 Expression in Non-Small Cell Lung Cancer
Clin. Cancer Res., August 1, 2000; 6(8): 2980 - 2987.
[Abstract] [Full Text]

A. Bottini, A. Berruti, A. Bersiga, M. P. Brizzi, A. Brunelli, G. Gorzegno, B. DiMarco, S. Aguggini, G. Bolsi, F. Cirillo, et al.
p53 but not bcl-2 Immunostaining Is Predictive of Poor Clinical Complete Response to Primary Chemotherapy in Breast Cancer Patients
Clin. Cancer Res., July 1, 2000; 6(7): 2751 - 2758.
[Abstract] [Full Text]

T. Kondo, T. Matsuda, T. Kitano, A. Takahashi, M. Tashima, H. Ishikura, H. Umehara, N. Domae, T. Uchiyama, and T. Okazaki
Role of c-jun Expression Increased by Heat Shock- and Ceramide-activated Caspase-3 in HL-60 Cell Apoptosis. POSSIBLE INVOLVEMENT OF CERAMIDE IN HEAT SHOCK-INDUCED APOPTOSIS
J. Biol. Chem., March 10, 2000; 275(11): 7668 - 7676.
[Abstract] [Full Text] [PDF]

S. W. Lowe and A. W. Lin
Apoptosis in cancer
Carcinogenesis, March 1, 2000; 21(3): 485 - 495.
[Abstract] [Full Text] [PDF]

P. Sabbatini and F. McCormick
Phosphoinositide 3-OH Kinase (PI3K) and PKB/Akt Delay the Onset of p53-mediated, Transcriptionally Dependent Apoptosis
J. Biol. Chem., August 20, 1999; 274(34): 24263 - 24269.
[Abstract] [Full Text] [PDF]

S. Wesselborg, I. H. Engels, E. Rossmann, M. Los, and K. Schulze-Osthoff
Anticancer Drugs Induce Caspase-8/FLICE Activation and Apoptosis in the Absence of CD95 Receptor/Ligand Interaction
Blood, May 1, 1999; 93(9): 3053 - 3063.
[Abstract] [Full Text] [PDF]

C. Richardson, M. E. Moynahan, and M. Jasin
Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations
Genes & Dev., December 15, 1998; 12(24): 3831 - 3842.
[Abstract] [Full Text]

C. E. Nesbit, S. Fan, H. Zhang, and E. V. Prochownik
Distinct Apoptotic Responses Imparted by c-myc and max
Blood, August 1, 1998; 92(3): 1003 - 1010.
[Abstract] [Full Text] [PDF]

S. Moallem and B. Hales
The role of p53 and cell death by apoptosis and necrosis in 4-hydroperoxycyclophosphamide-induced limb malformations
Development, January 8, 1998; 125(16): 3225 - 3234.
[Abstract] [PDF]

J. M. Garland and A. Halestrap
Energy Metabolism during Apoptosis. bcl-2 PROMOTES SURVIVAL IN HEMATOPOIETIC CELLS INDUCED TO APOPTOSE BY GROWTH FACTOR WITHDRAWAL BY STABILIZING A FORM OF METABOLIC ARREST
J. Biol. Chem., February 21, 1997; 272(8): 4680 - 4688.
[Abstract] [Full Text] [PDF]

D. E. Banker, M. Groudine, T. Norwood, and F. R. Appelbaum
Measurement of Spontaneous and Therapeutic Agent-Induced Apoptosis With BCL-2 Protein Expression in Acute Myeloid Leukemia
Blood, January 1, 1997; 89(1): 243 - 255.
[Abstract] [Full Text] [PDF]

P. Robbins
p53 and Breast Cancer
International Journal of Surgical Pathology, October 1, 1996; 4(2): 93 - 110.
[Abstract] [PDF]

L. A. Robinson, L. J. Smith, M. P. Fontaine, H. D. Kay, C. P. Mountjoy, and S. J. Pirruccello
c-myc Antisense Oligodeoxyribonucleotides Inhibit Proliferation of Non-Small Cell Lung Cancer
Ann. Thorac. Surg., December 1, 1995; 60(6): 1583 - 1591.
[Abstract] [Full Text]

C. Thompson
Apoptosis in the pathogenesis and treatment of disease
Science, March 10, 1995; 267(5203): 1456 - 1462.
[Abstract] [PDF]

C. F. Shuler
Programmed Cell Death and Cell Transformation in Craniofacial Development
Critical Reviews in Oral Biology & Medicine, January 1, 1995; 6(3): 202 - 217.
[Abstract] [Full Text] [PDF]

A J Wagner, J M Kokontis, and N Hay
Myc-mediated apoptosis requires wild-type p53 in a manner independent of cell cycle arrest and the ability of p53 to induce p21waf1/cip1.
Genes & Dev., December 1, 1994; 8(23): 2817 - 2830.
[Abstract] [PDF]

S. Lowe, S Bodis, A McClatchey, L Remington, H. Ruley, D. Fisher, D. Housman, and T Jacks
p53 status and the efficacy of cancer therapy in vivo
Science, November 4, 1994; 266(5186): 807 - 810.
[Abstract] [PDF]

G. Asher, J. Lotem, B. Cohen, L. Sachs, and Y. Shaul
Regulation of p53 stability and p53-dependent apoptosis by NADH quinone oxidoreductase 1
PNAS, January 30, 2001; 98(3): 1188 - 1193.
[Abstract] [Full Text] [PDF]

Cancer Research	Clinical Cancer Research
Cancer Epidemiology Biomarkers & Prevention	Molecular Cancer Therapeutics
Molecular Cancer Research	Cell Growth & Differentiation

Cancer Research	Clinical Cancer Research
Cancer Epidemiology Biomarkers & Prevention	Molecular Cancer Therapeutics
Molecular Cancer Research	Cell Growth & Differentiation

				C. Shanmugam, V. R. Katkoori, N. C. Jhala, W. E. Grizzle, G. P. Siegal, and U. Manne p53 Nuclear Accumulation and Bcl-2 Expression in Contiguous Adenomatous Components of Colorectal Adenocarcinomas Predict Aggressive Tumor Behavior J. Histochem. Cytochem., March 1, 2008; 56(3): 305 - 312. [Abstract] [Full Text] [PDF]

				C. M. Rudin, R. Salgia, X. Wang, L. D. Hodgson, G. A. Masters, M. Green, and E. E. Vokes Randomized Phase II Study of Carboplatin and Etoposide With or Without the bcl-2 Antisense Oligonucleotide Oblimersen for Extensive-Stage Small-Cell Lung Cancer: CALGB 30103 J. Clin. Oncol., February 20, 2008; 26(6): 870 - 876. [Abstract] [Full Text] [PDF]

				D Trere, L Montanaro, C Ceccarelli, S Barbieri, G Cavrini, D Santini, M Taffurelli, and M Derenzini Prognostic relevance of a novel semiquantitative classification of Bcl2 immunohistochemical expression in human infiltrating ductal carcinomas of the breast Ann. Onc., June 1, 2007; 18(6): 1004 - 1014. [Abstract] [Full Text] [PDF]

				H. Biliran Jr., S. Banerjee, A. Thakur, F. H. Sarkar, A. Bollig, F. Ahmed, J. Wu, Y. Sun, and J. D. Liao c-Myc Induced Chemosensitization Is Mediated by Suppression of Cyclin D1 Expression and Nuclear Factor-{kappa}B Activity in Pancreatic Cancer Cells Clin. Cancer Res., May 1, 2007; 13(9): 2811 - 2821. [Abstract] [Full Text] [PDF]

				R. Aneja, J. Zhou, B. Zhou, R. Chandra, and H. C. Joshi Treatment of hormone-refractory breast cancer: apoptosis and regression of human tumors implanted in mice. Mol. Cancer Ther., September 1, 2006; 5(9): 2366 - 2377. [Abstract] [Full Text] [PDF]

				F. Nagashima, N. Boku, A. Ohtsu, S. Yoshida, T. Hasebe, A. Ochiai, Y. Sakata, H. Saito, Y. Miyata, I. Hyodo, et al. Biological Markers as a Predictor for Response and Prognosis of Unresectable Gastric Cancer Patients Treated with Irinotecan and Cisplatin Jpn. J. Clin. Oncol., December 1, 2005; 35(12): 714 - 719. [Abstract] [Full Text] [PDF]

				C. M. Rudin, M. Kozloff, P. C. Hoffman, M. J. Edelman, R. Karnauskas, R. Tomek, L. Szeto, and E. E. Vokes Phase I Study of G3139, a bcl-2 Antisense Oligonucleotide, Combined With Carboplatin and Etoposide in Patients With Small-Cell Lung Cancer J. Clin. Oncol., March 15, 2004; 22(6): 1110 - 1117. [Abstract] [Full Text] [PDF]

				A. A. A. M. Danen-van Oorschot, Y.-H. Zhang, S. R. Leliveld, J. L. Rohn, M. C. M. J. Seelen, M. W. Bolk, A. van Zon, S. J. Erkeland, J.-P. Abrahams, D. Mumberg, et al. Importance of Nuclear Localization of Apoptin for Tumor-specific Induction of Apoptosis J. Biol. Chem., July 18, 2003; 278(30): 27729 - 27736. [Abstract] [Full Text] [PDF]

				C. M. Rudin, G. A. Otterson, A. M. Mauer, M. A. Villalona-Calero, R. Tomek, B. Prange, C. M. George, L. Szeto, and E. E. Vokes A pilot trial of G3139, a bcl-2 antisense oligonucleotide, and paclitaxel in patients with chemorefractory small-cell lung cancer Ann. Onc., April 1, 2002; 13(4): 539 - 545. [Abstract] [Full Text] [PDF]

				D. J. Bearss, R. J. Lee, D. A. Troyer, R. G. Pestell, and J. J. Windle Differential Effects of p21WAF1/CIP1 Deficiency on MMTV-ras and MMTV-myc Mammary Tumor Properties Cancer Res., April 1, 2002; 62(7): 2077 - 2084. [Abstract] [Full Text] [PDF]

				J. C. Cusack Jr., R. Liu, M. Houston, K. Abendroth, P. J. Elliott, J. Adams, and A. S. Baldwin Jr. Enhanced Chemosensitivity to CPT-11 with Proteasome Inhibitor PS-341:: Implications for Systemic Nuclear Factor-{{kappa}}B Inhibition Cancer Res., May 1, 2001; 61(9): 3535 - 3540. [Abstract] [Full Text]

				A. Sigal and V. Rotter Oncogenic Mutations of the p53 Tumor Suppressor: The Demons of the Guardian of the Genome Cancer Res., December 1, 2000; 60(24): 6788 - 6793. [Abstract] [Full Text]

				Y. Ohmura, M. Aoe, A. Andou, and N. Shimizu Telomerase Activity and Bcl-2 Expression in Non-Small Cell Lung Cancer Clin. Cancer Res., August 1, 2000; 6(8): 2980 - 2987. [Abstract] [Full Text]

				A. Bottini, A. Berruti, A. Bersiga, M. P. Brizzi, A. Brunelli, G. Gorzegno, B. DiMarco, S. Aguggini, G. Bolsi, F. Cirillo, et al. p53 but not bcl-2 Immunostaining Is Predictive of Poor Clinical Complete Response to Primary Chemotherapy in Breast Cancer Patients Clin. Cancer Res., July 1, 2000; 6(7): 2751 - 2758. [Abstract] [Full Text]

				T. Kondo, T. Matsuda, T. Kitano, A. Takahashi, M. Tashima, H. Ishikura, H. Umehara, N. Domae, T. Uchiyama, and T. Okazaki Role of c-jun Expression Increased by Heat Shock- and Ceramide-activated Caspase-3 in HL-60 Cell Apoptosis. POSSIBLE INVOLVEMENT OF CERAMIDE IN HEAT SHOCK-INDUCED APOPTOSIS J. Biol. Chem., March 10, 2000; 275(11): 7668 - 7676. [Abstract] [Full Text] [PDF]

				S. W. Lowe and A. W. Lin Apoptosis in cancer Carcinogenesis, March 1, 2000; 21(3): 485 - 495. [Abstract] [Full Text] [PDF]

				P. Sabbatini and F. McCormick Phosphoinositide 3-OH Kinase (PI3K) and PKB/Akt Delay the Onset of p53-mediated, Transcriptionally Dependent Apoptosis J. Biol. Chem., August 20, 1999; 274(34): 24263 - 24269. [Abstract] [Full Text] [PDF]

				S. Wesselborg, I. H. Engels, E. Rossmann, M. Los, and K. Schulze-Osthoff Anticancer Drugs Induce Caspase-8/FLICE Activation and Apoptosis in the Absence of CD95 Receptor/Ligand Interaction Blood, May 1, 1999; 93(9): 3053 - 3063. [Abstract] [Full Text] [PDF]

				C. Richardson, M. E. Moynahan, and M. Jasin Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations Genes & Dev., December 15, 1998; 12(24): 3831 - 3842. [Abstract] [Full Text]

				C. E. Nesbit, S. Fan, H. Zhang, and E. V. Prochownik Distinct Apoptotic Responses Imparted by c-myc and max Blood, August 1, 1998; 92(3): 1003 - 1010. [Abstract] [Full Text] [PDF]

ARTICLES

Regulation by bcl-2, c-myc, and p53 of susceptibility to induction of apoptosis by heat shock and cancer chemotherapy compounds in differentiation-competent and -defective myeloid leukemic cells

				S. Moallem and B. Hales The role of p53 and cell death by apoptosis and necrosis in 4-hydroperoxycyclophosphamide-induced limb malformations Development, January 8, 1998; 125(16): 3225 - 3234. [Abstract] [PDF]

				J. M. Garland and A. Halestrap Energy Metabolism during Apoptosis. bcl-2 PROMOTES SURVIVAL IN HEMATOPOIETIC CELLS INDUCED TO APOPTOSE BY GROWTH FACTOR WITHDRAWAL BY STABILIZING A FORM OF METABOLIC ARREST J. Biol. Chem., February 21, 1997; 272(8): 4680 - 4688. [Abstract] [Full Text] [PDF]

				D. E. Banker, M. Groudine, T. Norwood, and F. R. Appelbaum Measurement of Spontaneous and Therapeutic Agent-Induced Apoptosis With BCL-2 Protein Expression in Acute Myeloid Leukemia Blood, January 1, 1997; 89(1): 243 - 255. [Abstract] [Full Text] [PDF]

				P. Robbins p53 and Breast Cancer International Journal of Surgical Pathology, October 1, 1996; 4(2): 93 - 110. [Abstract] [PDF]

				L. A. Robinson, L. J. Smith, M. P. Fontaine, H. D. Kay, C. P. Mountjoy, and S. J. Pirruccello c-myc Antisense Oligodeoxyribonucleotides Inhibit Proliferation of Non-Small Cell Lung Cancer Ann. Thorac. Surg., December 1, 1995; 60(6): 1583 - 1591. [Abstract] [Full Text]

				C. Thompson Apoptosis in the pathogenesis and treatment of disease Science, March 10, 1995; 267(5203): 1456 - 1462. [Abstract] [PDF]

				C. F. Shuler Programmed Cell Death and Cell Transformation in Craniofacial Development Critical Reviews in Oral Biology & Medicine, January 1, 1995; 6(3): 202 - 217. [Abstract] [Full Text] [PDF]

				A J Wagner, J M Kokontis, and N Hay Myc-mediated apoptosis requires wild-type p53 in a manner independent of cell cycle arrest and the ability of p53 to induce p21waf1/cip1. Genes & Dev., December 1, 1994; 8(23): 2817 - 2830. [Abstract] [PDF]

				S. Lowe, S Bodis, A McClatchey, L Remington, H. Ruley, D. Fisher, D. Housman, and T Jacks p53 status and the efficacy of cancer therapy in vivo Science, November 4, 1994; 266(5186): 807 - 810. [Abstract] [PDF]

				G. Asher, J. Lotem, B. Cohen, L. Sachs, and Y. Shaul Regulation of p53 stability and p53-dependent apoptosis by NADH quinone oxidoreductase 1 PNAS, January 30, 2001; 98(3): 1188 - 1193. [Abstract] [Full Text] [PDF]