In Vivo Mitochondrial p53 Translocation Triggers a Rapid First Wave of Cell Death in Response to DNA Damage That Can Precede p53 Target Gene Activation

REFERENCES

• Attardi, L. D., Reczek E. E., Cosmas C., Demicco E. G., McCurrach M. E., Lowe S. W., and Jacks T.. 2000. PERP, an apoptosis-associated target of p53, is a novel member of the PMP-22/gas3 family. Genes Dev. 14:704–718.
   PubMed Web of Science ®Google Scholar
• Baptiste, N., Friedlander P., Chen X., and Prives C.. 2002. The proline-rich domain of p53 is required for cooperation with anti-neoplastic agents to promote apoptosis of tumor cells. Oncogene 21:9–21.
   PubMedGoogle Scholar
• Bennett, M., Macdonald K., Chan S. W., Luzio J. P., Simari R., and Weissberg P.. 1998. Cell surface trafficking of Fas: a rapid mechanism of p53-mediated apoptosis. Science 282:290–293.
   PubMed Web of Science ®Google Scholar
• Caelles, C., Helmberg A., and Karin M.. 1994. p53-dependent apoptosis in the absence of transcriptional activation of p53-target genes. Nature 370:220–223.
   PubMed Web of Science ®Google Scholar
• Chao, C., Saito S., Kang J., Anderson C. W., Appella E., and Xu Y.. 2000. p53 transcriptional activity is essential for p53-dependent apoptosis following DNA damage. EMBO J. 19:4967–4975.
   PubMed Web of Science ®Google Scholar
• Chen, X., Ko L. J., Jayaraman L., and Prives C.. 1996. p53 levels, functional domains, and DNA damage determine the extent of the apoptotic response of tumor cells. Genes Dev. 10:2438–2451.
   PubMed Web of Science ®Google Scholar
• Chipuk, J. E., Kuwana T., Bouchier-Hayes L., Droin N. M., Newmeyer D. D., Schuler M., and Green D. R.. 2004. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303:1010–1014.
   PubMed Web of Science ®Google Scholar
• Clarke, A. R., Purdie C. A., Harrison D. J., Morris R. G., Bird C. C., Hooper M. L., and Wyllie A. H.. 1993. Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature 362:849–852.
   PubMed Web of Science ®Google Scholar
• Ding, H. F., Lin Y. L., McGill G., Juo P., Zhu H., Blenis J., Yuan J., and Fisher D. E.. 2000. Essential role for caspase-8 in transcription-independent apoptosis triggered by p53. J. Biol. Chem. 275:38905–38911.
   PubMed Web of Science ®Google Scholar
• el-Deiry, W. S., Tokino T., Velculescu V. E., Levy D. B., Parsons R., Trent J. M., Lin D., Mercer W. E., Kinzler K. W., and Vogelstein B.. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817–825.
   PubMed Web of Science ®Google Scholar
• Fei, P., Bernhard E. J., and el-Deiry W. S.. 2002. Tissue-specific induction of p53 targets in vivo. Cancer Res. 62:7316–7327.
   PubMed Web of Science ®Google Scholar
• Han, J., Flemington C., Houghton A. B., Gu Z., Zambetti G. P., Lutz R. J., Zhu L., and Chittenden T.. 2001. Expression of bbc3, a pro-apoptotic BH3-only gene, is regulated by diverse cell death and survival signals. Proc. Natl. Acad. Sci. USA 98:11318–11323.
   PubMed Web of Science ®Google Scholar
• Haupt, Y., Rowan S., Shaulian E., Vousden K. H., and Oren M.. 1995. Induction of apoptosis in HeLa cells by trans-activation-deficient p53. Genes Dev. 9:2170–2183.
   PubMed Web of Science ®Google Scholar
• Jeffers, J. R., Parganas E., Lee Y., Yang C., Wang J., Brennan J., MacLean K. H., Han J., Chittenden T., Ihle J. N., McKinnon P. J., Cleveland J. L., and Zambetti G. P.. 2003. Puma is an essential mediator of p53-dependent and -independent apoptotic pathways. Cancer Cell 4:321–328.
   PubMed Web of Science ®Google Scholar
• Jimenez, G. S., Nister M., Stommel J. M., Beeche M., Barcarse E. A., Zhang X. Q., O'Gorman S., and Wahl G. M.. 2000. A transactivation-deficient mouse model provides insights into Trp53 regulation and function. Nat. Genet. 26:37–43.
   PubMed Web of Science ®Google Scholar
• Knudson, C. M., Tung K. S., Tourtellotte W. G., Brown G. A., and Korsmeyer S. J.. 1995. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270:96–99.
   PubMed Web of Science ®Google Scholar
• Kokontis, J. M., Wagner A. J., O'Leary M., Liao S., and Hay N.. 2001. A transcriptional activation function of p53 is dispensable for and inhibitory of its apoptotic function. Oncogene 20:659–668.
   PubMed Web of Science ®Google Scholar
• Komarova, E. A., Chernov M. V., Franks R., Wang K., Armin G., Zelnick C. R., Chin D. M., Bacus S. S., Stark G. R., and Gudkov A. V.. 1997. Transgenic mice with p53-responsive lacZ: p53 activity varies dramatically during normal development and determines radiation and drug sensitivity in vivo. EMBO J. 16:1391–1400.
   PubMed Web of Science ®Google Scholar
• Lin, Y., Ma W., and Benchimol S.. 2000. Pidd, a new death-domain-containing protein, is induced by p53 and promotes apoptosis. Nat. Genet. 26:122–127.
   PubMed Web of Science ®Google Scholar
• Lowe, S. W., Schmitt E. M., Smith S. W., Osborne B. A., and Jacks T.. 1993. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature 362:847–849.
   PubMed Web of Science ®Google Scholar
• MacCallum, D. E., Hall P. A., and Wright E. G.. 2001. The Trp53 pathway is induced in vivo by low doses of gamma radiation. Radiat. Res. 156:324–327.
   PubMed Web of Science ®Google Scholar
• MacCallum, D. E., Hupp T. R., Midgley C. A., Stuart D., Campbell S. J., Harper A., Walsh F. S., Wright E. G., Balmain A., Lane D. P., and Hall P. A.. 1996. The p53 response to ionising radiation in adult and developing murine tissues. Oncogene 13:2575–2587.
   PubMed Web of Science ®Google Scholar
• Marchenko, N. D., Zaika A., and Moll U. M.. 2000. Death signal-induced localization of p53 protein to mitochondria. A potential role in apoptotic signaling. J. Biol. Chem. 275:16202–16212.
   PubMed Web of Science ®Google Scholar
• Matas, D., Sigal A., Stambolsky P., Milyavsky M., Weisz L., Schwartz D., Goldfinger N., and Rotter V.. 2001. Integrity of the N-terminal transcription domain of p53 is required for mutant p53 interference with drug-induced apoptosis. EMBO J. 20:4163–4172.
   PubMedGoogle Scholar
• Merritt, A. J., Allen T. D., Potten C. S., and Hickman J. A.. 1997. Apoptosis in small intestinal epithelia from p53-null mice: evidence for a delayed, p53-independent G2/M-associated cell death after gamma-irradiation. Oncogene 14:2759–2766.
   PubMed Web of Science ®Google Scholar
• Merritt, A. J., Potten C. S., Kemp C. J., Hickman J. A., Balmain A., Lane D. P., and Hall P. A.. 1994. The role of p53 in spontaneous and radiation-induced apoptosis in the gastrointestinal tract of normal and p53-deficient mice. Cancer Res. 54:614–617.
   PubMed Web of Science ®Google Scholar
• Mihara, M., Erster S., Zaika A., Petrenko O., Chittenden T., Pancoska P., and Moll U. M.. 2003. p53 has a direct apoptogenic role at the mitochondria. Mol. Cell 11:577–590.
   PubMed Web of Science ®Google Scholar
• Mihara, M., and Moll U. M.. 2003. Detection of mitochondrial localization of p53. Methods Mol. Biol. 234:203–209.
   PubMedGoogle Scholar
• Miyashita, T., Kitada S., Krajewski S., Horne W. A., Delia D., and Reed J. C.. 1995. Overexpression of the Bcl-2 protein increases the half-life of p21Bax. J. Biol. Chem. 270:26049–26052.
   PubMed Web of Science ®Google Scholar
• Muller, M., Wilder S., Bannasch D., Israeli D., Lehlbach K., Li-Weber M., Friedman S. L., Galle P. R., Stremmel W., Oren M., and Krammer P. H.. 1998. p53 activates the CD95 (APO-1/Fas) gene in response to DNA damage by anticancer drugs. J. Exp. Med. 188:2033–2045.
   PubMed Web of Science ®Google Scholar
• Nakano, K., and Vousden K. H.. 2001. PUMA, a novel proapoptotic gene, is induced by p53. Mol. Cell 7:683–694.
   PubMed Web of Science ®Google Scholar
• Oda, E., Ohki R., Murasawa H., Nemoto J., Shibue T., Yamashita T., Tokino T., Taniguchi T., and Tanaka N.. 2000. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 288:1053–1058.
   PubMed Web of Science ®Google Scholar
• Oda, K., Arakawa H., Tanaka T., Matsuda K., Tanikawa C., Mori T., Nishimori H., Tamai K., Tokino T., Nakamura Y., and Taya Y.. 2000. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 102:849–862.
   PubMed Web of Science ®Google Scholar
• Okamura, S., Arakawa H., Tanaka T., Nakanishi H., Ng C. C., Taya Y., Monden M., and Nakamura Y.. 2001. p53DINP1, a p53-inducible gene, regulates p53-dependent apoptosis. Mol. Cell 8:85–94.
   PubMed Web of Science ®Google Scholar
• Owen-Schaub, L. B., Angelo L. S., Radinsky R., Ware C. F., Gesner T. G., and Bartos D. P.. 1995. Soluble Fas/APO-1 in tumor cells: a potential regulator of apoptosis? Cancer Lett. 94:1–8.
   PubMed Web of Science ®Google Scholar
• Polyak, K., Xia Y., Zweier J. L., Kinzler K. W., and Vogelstein B.. 1997. A model for p53-induced apoptosis. Nature 389:300–305.
   PubMed Web of Science ®Google Scholar
• Qu, L., Huang S., Baltzis D., Rivas-Estilla A. M., Pluquet O., Hatzoglou M., Koumenis C., Taya Y., Yoshimura A., and Koromilas A. E.. 2004. Endoplasmic reticulum stress induces p53 cytoplasmic localization and prevents p53-dependent apoptosis by a pathway involving glycogen synthase kinase-3beta. Genes Dev. 18:261–277.
   PubMed Web of Science ®Google Scholar
• Regula, K. M., and Kirshenbaum L. A.. 2001. p53 activates the mitochondrial death pathway and apoptosis of ventricular myocytes independent of de novo gene transcription. J. Mol. Cell. Cardiol. 33:1435–1445.
   PubMedGoogle Scholar
• Sansome, C., Zaika A., Marchenko N. D., and Moll U. M.. 2001. Hypoxia death stimulus induces translocation of p53 protein to mitochondria. Detection by immunofluorescence on whole cells. FEBS Lett. 488:110–115.
   PubMed Web of Science ®Google Scholar
• Sax, J. K., Fei P., Murphy M. E., Bernhard E., Korsmeyer S. J., and el-Deiry W. S.. 2002. BID regulation by p53 contributes to chemosensitivity. Nat. Cell Biol. 4:842–849.
   PubMed Web of Science ®Google Scholar
• Schuler, M., Bossy-Wetzel E., Goldstein J. C., Fitzgerald P., and Green D. R.. 2000. p53 induces apoptosis by caspase activation through mitochondrial cytochrome c release. J. Biol. Chem. 275:7337–7342.
   PubMed Web of Science ®Google Scholar
• Schuler, M., and Green D. R.. 2001. Mechanisms of p53-dependent apoptosis. Biochem. Soc. Trans. 29:684–688.
   PubMed Web of Science ®Google Scholar
• Shibue, T., Takeda K., Oda E., Tanaka H., Murasawa H., Takaoka A., Morishita Y., Akira S., Taniguchi T., and Tanaka N.. 2003. Integral role of Noxa in p53-mediated apoptotic response. Genes Dev. 17:2233–2238.
   PubMed Web of Science ®Google Scholar
• Sugars, K. L., Budhram-Mahadeo V., Packham G., and Latchman D. S.. 2001. A minimal Bcl-x promoter is activated by Brn-3a and repressed by p53. Nucleic Acids Res. 29:4530–4540.
   PubMed Web of Science ®Google Scholar
• Villunger, A., Michalak E. M., Coultas L., Mullauer F., Bock G., Ausserlechner M. J., Adams J. M., and Strasser A.. 2003. p53- and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 302:1036–1038. [Online.]
   PubMed Web of Science ®Google Scholar
• Wagner, A. J., Kokontis J. M., and Hay N.. 1994. 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. 8:2817–2830.
   PubMed Web of Science ®Google Scholar
• Yu, J., Zhang L., Hwang P. M., Kinzler K. W., and Vogelstein B.. 2001. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol. Cell 7:673–682.
   PubMed Web of Science ®Google Scholar