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American Journal of Pathology, Vol 145, 1323-1336, Copyright © 1994 by American Society for Investigative Pathology
REGULAR ARTICLES |
S Krajewski, M Krajewska, A Shabaik, T Miyashita, HG Wang and JC Reed
Oncogene and Tumor Suppressor Gene Program, La Jolla Cancer Research Foundation, California 92037.
The protein encoded by the bcl-2 gene is a regulator of programmed cell death and apoptosis. The cell survival-promoting activity of this protein is opposed by Bax, a homologous protein that forms heterodimers with Bcl-2 and accelerates rates of cell death. In this report, the in vivo patterns of bax gene expression were immunohistochemically assessed in the mouse, with a polyclonal antibody raised against a synthetic peptide corresponding to a unique region in the murine Bax protein. Direct comparisons were made with Bcl-2 by using anti-peptide antisera specific for the mouse Bcl-2 protein. The expression of bax was more widespread than bcl-2. For example, Bax immunoreactivity was present in the hepatocytes of the liver, the exocrine pancreas, and the renal tubule epithelial cells whereas Bcl-2 was absent from these tissues. Both the Bax and Bcl-2 proteins were present in several epithelia examined, including the small intestines, colon, breast, prostate, respiratory tract, and skin. The most intense Bax immunostaining was seen in cells located in the base of the crypts of the small intestinal mucosa, consistent with reports of high rates of spontaneous and inducible apoptosis in this region. Bcl-2 immunostaining was completely absent from these cells but was present in the absorptive epithelial cells of the small intestine. In contrast, Bax immunostaining in the colon tended to be stronger in the surface epithelial cells that had advanced up the crypts towards the lumen and that are destined for programmed cell death, whereas Bcl-2 immunoreactivity generally was stronger in the base of the colonic crypts. Similarly, bax expression in the gastric pits of the stomach occurred in a gradient such that higher levels of Bax immunostaining were found in the upper layers of gastric glands than in the lower regions. In addition, strong Bax immunostaining was detected in the androgen-dependent secretory epithelial cells of the prostate, whereas Bcl-2 was limited to the androgen-independent basal cells. Like Bcl-2, Bax was found in the thymic medulla but not the cortex, despite the propensity for immature cortical thymocytes to undergo apoptosis. Unlike Bcl-2, however, Bax immunostaining tended to be more intense in the germinal center lymphocytes of lymph nodes than in the interfollicular lymphocytes, consistent with the high rate of apoptotic cell death in the former.(ABSTRACT TRUNCATED AT 400 WORDS)
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F. A. White, C. R. Keller-Peck, C. M. Knudson, S. J. Korsmeyer, and W. D. Snider Widespread Elimination of Naturally Occurring Neuronal Death in Bax-Deficient Mice J. Neurosci., February 15, 1998; 18(4): 1428 - 1439. [Abstract] [Full Text] [PDF] |
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A. Sh. Parsadanian, Y. Cheng, C. R. Keller-Peck, D. M. Holtzman, and W. D. Snider Bcl-xL is an Antiapoptotic Regulator for Postnatal CNS Neurons J. Neurosci., February 1, 1998; 18(3): 1009 - 1019. [Abstract] [Full Text] [PDF] |
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B. A. Jones and G. J. Gores Physiology and pathophysiology of apoptosis in epithelial cells of the liver, pancreas, and intestine Am J Physiol Gastrointest Liver Physiol, December 1, 1997; 273(6): G1174 - G1188. [Abstract] [Full Text] [PDF] |
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R. D. Gascoyne, M. Krajewska, S. Krajewski, J. M. Connors, and J. C. Reed Prognostic Significance of Bax Protein Expression in Diffuse Aggressive Non-Hodgkin's Lymphoma Blood, October 15, 1997; 90(8): 3173 - 3178. [Abstract] [Full Text] [PDF] |
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X.-J. Tao, K. I. Tilly, D. V. Maravei, J. L. Shifren, S. Krajewski, J. C. Reed, J. L. Tilly, and K. B. Isaacson Differential Expression of Members of the bcl-2 Gene Family in Proliferative and Secretory Human Endometrium: Glandular Epithelial Cell Apoptosis Is Associated with Increased Expression of bax J. Clin. Endocrinol. Metab., August 1, 1997; 82(8): 2738 - 2746. [Abstract] [Full Text] [PDF] |
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N. K. Ossina, A. Cannas, V. C. Powers, P. A. Fitzpatrick, J. D. Knight, J. R. Gilbert, E. M. Shekhtman, L. D. Tomei, S. R. Umansky, and M. C. Kiefer Interferon-gamma Modulates a p53-independent Apoptotic Pathway and Apoptosis-related Gene Expression J. Biol. Chem., June 27, 1997; 272(26): 16351 - 16357. [Abstract] [Full Text] [PDF] |
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S. Krajewski, R. D. Gascoyne, J. M. Zapata, M. Krajewska, S. Kitada, M. Chhanabhai, D. Horsman, K. Berean, L. D. Piro, I. Fugier-Vivier, et al. Immunolocalization of the ICE/Ced-3-Family Protease, CPP32 (Caspase-3), in Non-Hodgkin's Lymphomas, Chronic Lymphocytic Leukemias, and Reactive Lymph Nodes Blood, May 15, 1997; 89(10): 3817 - 3825. [Abstract] [Full Text] [PDF] |
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K. S. Shindler, C. B. Latham, and K. A. Roth bax Deficiency Prevents the Increased Cell Death of Immature Neurons in bcl-x-Deficient Mice J. Neurosci., May 1, 1997; 17(9): 3112 - 3119. [Abstract] [Full Text] [PDF] |
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G. Olivetti, R. Abbi, F. Quaini, J. Kajstura, W. Cheng, J. A. Nitahara, E. Quaini, C. Di Loreto, C. A. Beltrami, S. Krajewski, et al. Apoptosis in the Failing Human Heart N. Engl. J. Med., April 17, 1997; 336(16): 1131 - 1141. [Abstract] [Full Text] [PDF] |
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J. Diez, A. Panizo, M. Hernandez, and J. Pardo Is the Regulation of Apoptosis Altered in Smooth Muscle Cells of Adult Spontaneously Hypertensive Rats? Hypertension, March 1, 1997; 29(3): 776 - 780. [Abstract] [Full Text] |
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H. Perlman, L. Maillard, K. Krasinski, and K. Walsh Evidence for the Rapid Onset of Apoptosis in Medial Smooth Muscle Cells After Balloon Injury Circulation, February 18, 1997; 95(4): 981 - 987. [Abstract] [Full Text] |
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K Vekrellis, M. McCarthy, A Watson, J Whitfield, L. Rubin, and J Ham Bax promotes neuronal cell death and is downregulated during the development of the nervous system Development, January 3, 1997; 124(6): 1239 - 1249. [Abstract] [PDF] |
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J. Misao, Y. Hayakawa, M. Ohno, S. Kato, T. Fujiwara, and H. Fujiwara Expression of bcl-2 Protein, an Inhibitor of Apoptosis, and Bax, an Accelerator of Apoptosis, in Ventricular Myocytes of Human Hearts With Myocardial Infarction Circulation, October 1, 1996; 94(7): 1506 - 1512. [Abstract] [Full Text] |
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C. Borner and C. Borner Diminished Cell Proliferation Associated with the Death-protective Activity of Bcl-2 J. Biol. Chem., May 31, 1996; 271(22): 12695 - 12698. [Abstract] [Full Text] [PDF] |
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R. Humphreys, M Krajewska, S Krnacik, R Jaeger, H Weiher, S Krajewski, J. Reed, and J. Rosen Apoptosis in the terminal endbud of the murine mammary gland: a mechanism of ductal morphogenesis Development, January 12, 1996; 122(12): 4013 - 4022. [Abstract] [PDF] |
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E White Life, death, and the pursuit of apoptosis. Genes & Dev., January 1, 1996; 10(1): 1 - 15. [PDF] |
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T. Miyashita, S. Kitada, S. Krajewski, W. A. Horne, D. Delia, and J. C. Reed Overexpression of the Bcl-2 Protein Increases the Half-life of p21[IMAGE] J. Biol. Chem., November 3, 1995; 270(44): 26049 - 26052. [Abstract] [Full Text] [PDF] |
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C. M. Knudson, K. S. K. Tung, W. G. Tourtellotte, G. A. J. Brown, and S. J. Korsmeyer Bax-Deficient Mice with Lymphoid Hyperplasia and Male Germ Cell Death Science, October 6, 1995; 270(5233): 96 - 99. [Abstract] [PDF] |
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D. A. Norris Differential Control of Cell Death in the Skin Arch Dermatol, August 1, 1995; 131(8): 945 - 948. [Abstract] [PDF] |
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M. R. Bennett, G. I. Evan, and S. M. Schwartz Apoptosis of Rat Vascular Smooth Muscle Cells Is Regulated by p53-Dependent and -Independent Pathways Circ. Res., August 1, 1995; 77(2): 266 - 273. [Abstract] [Full Text] |
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M. Hanada, C. Aimé-Sempé, T. Sato, and J. C. Reed Structure-Function Analysis of Bcl-2 Protein J. Biol. Chem., May 19, 1995; 270(20): 11962 - 11969. [Abstract] [Full Text] [PDF] |
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A. Merritt, C. Potten, A. Watson, D. Loh, K Nakayama, K Nakayama, and J. Hickman Differential expression of bcl-2 in intestinal epithelia. Correlation with attenuation of apoptosis in colonic crypts and the incidence of colonic neoplasia J. Cell Sci., January 6, 1995; 108(6): 2261 - 2271. [Abstract] [PDF] |
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A. J. Butt, S. M. Firth, M. A. King, and R. C. Baxter Insulin-like Growth Factor-binding Protein-3 Modulates Expression of Bax and Bcl-2 and Potentiates p53-independent Radiation-induced Apoptosis in Human Breast Cancer Cells J. Biol. Chem., December 8, 2000; 275(50): 39174 - 39181. [Abstract] [Full Text] [PDF] |
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B. Li and Q. P. Dou Bax degradation by the ubiquitin/proteasome-dependent pathway: Involvement in tumor survival and progression PNAS, April 11, 2000; 97(8): 3850 - 3855. [Abstract] [Full Text] [PDF] |
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