Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

Poly(ADP-ribosyl)ation of p53 Contributes to TPEN-Induced Neuronal Apoptosis

  • Kim, Hyun-Lim (Department of Molecular Biology, Sejong University) ;
  • Ra, Hana (Department of Molecular Biology, Sejong University) ;
  • Kim, Ki-Ryeong (Department of Molecular Biology, Sejong University) ;
  • Lee, Jeong-Min (Department of Molecular Biology, Sejong University) ;
  • Im, Hana (Department of Molecular Biology, Sejong University) ;
  • Kim, Yang-Hee (Department of Molecular Biology, Sejong University)
  • Received : 2014.06.02
  • Accepted : 2015.01.19
  • Published : 2015.04.30
Download PDF
⟨ Previous Next ⟩

Abstract

Depletion of intracellular zinc by N,N,N,N-tetrakis(2-pyridylmethyl) ethylenediamine (TPEN) induces p53-mediated protein synthesis-dependent apoptosis of mouse cortical neurons. Here, we examined the requirement for poly(ADP-ribose) polymerase (PARP)-1 as an upstream regulator of p53 in zinc depletion-induced neuronal apoptosis. First, we found that chemical inhibition or genetic deletion of PARP-1 markedly attenuated TPEN-induced apoptosis of cultured mouse cortical neurons. Poly(ADP-ribosyl)ation of p53 occurred starting 1 h after TPEN treatment. Suggesting the critical role of PARP-1, the TPEN-induced increase of stability and activity of p53 as well as poly(ADP-ribosyl)ation of p53 was almost completely blocked by PARP inhibition. Consistent with this, the induction of downstream pro-apoptotic proteins PUMA and NOXA was noticeably reduced by chemical inhibitors or genetic deletion of PARP-1. TPEN-induced cytochrome C release into the cytosol and caspase-3 activation were also blocked by inhibition of PARP-1. Taken together, these findings indicate that PARP-1 is essential for TPEN-induced neuronal apoptosis.

Keywords

References

  1. Ahn, Y.H., Kim, Y.H., Hong, S.H., and Koh, J.Y. (1998). Depletion of intracellular zinc induces protein synthesis-dependent neuronal apoptosis in mouse cortical culture. Exp. Neurol. 154, 47-56. https://doi.org/10.1006/exnr.1998.6931
  2. Appella, E., and Anderson, C.W. (2001). Post-translational modifications and activation of p53 by genotoxic stresses. Eur. J. Biochem. 268, 2764-2772. https://doi.org/10.1046/j.1432-1327.2001.02225.x
  3. Berger, N.A. (1985). Poly(ADP-ribose) in the cellular response to DNA damage. Radiat. Res. 101, 4-15. https://doi.org/10.2307/3576299
  4. Berger, N.A., and Petzold, S.J. (1985). Identification of minimal size requirements of DNA for activation of poly(ADP-ribose) polymerase. Biochemistry 24, 4352-4355. https://doi.org/10.1021/bi00337a015
  5. Blagosklonny, M.V. (1997). Loss of function and p53 protein stabilization. Oncogene 15, 1889-1893. https://doi.org/10.1038/sj.onc.1201374
  6. Boulares, A.H., Yakovlev, A.G., Ivanova, V., Stoica, B.A., Wang, G., Iyer, S., and Smulson, M. (1999). Role of poly(ADP-ribose) polymerase (PARP) cleavage in apoptosis. Caspase 3-resistant PARP mutant increases rates of apoptosis in transfected cells. J. Biol. Chem. 274, 22932-22940. https://doi.org/10.1074/jbc.274.33.22932
  7. Bozym, R.A., Thompson, R.B., Stoddard, A.K., and Fierke, C.A. (2006). Measuring picomolar intracellular exchangeable zinc in PC-12 cells using a ratiometric fluorescence biosensor. ACS Chem. Biol. 1, 103-111. https://doi.org/10.1021/cb500043a
  8. Choi, D.W., and Koh, J.Y. (1998). Zinc and brain injury. Annu. Rev. Neurosci. 21, 347-375. https://doi.org/10.1146/annurev.neuro.21.1.347
  9. Coleman, J.E. (1992). Zinc proteins: enzymes, storage proteins, transcription factors, and replication proteins. Annu. Rev. Biochem. 61, 897-946. https://doi.org/10.1146/annurev.bi.61.070192.004341
  10. Frederickson, C.J., and Bush, A.I. (2001). Synaptically released zinc: physiological functions and pathological effects. Biometals 14, 353-366. https://doi.org/10.1023/A:1012934207456
  11. Freeman, J.A., and Espinosa, J.M. (2013). The impact of post-transcriptional regulation in the p53 network. Brief. Funct. Genomics 12, 46-57. https://doi.org/10.1093/bfgp/els058
  12. Gangopadhyay, N.N., Luketich, J.D., Opest, A., Visus, C., Meyer, E.M., Landreneau, R., and Schuchert, M.J. (2011). Inhibition of poly(ADP-ribose) polymerase (PARP) induces apoptosis in lung cancer cell lines. Cancer Invest. 29, 608-616. https://doi.org/10.3109/07357907.2011.621916
  13. Gorospe, M., Wang, X., and Holbrook, N.J. (1998). p53-dependent elevation of p21Waf1 expression by UV light is mediated through mRNA stabilization and involves a vanadate-sensitive regulatory system. Mol. Cell. Biol. 18, 1400-1407. https://doi.org/10.1128/MCB.18.3.1400
  14. Hock, A.K., and Vousden, K.H. (2014). The role of ubiquitin modification in the regulation of p53. Biochim. Biophys. Acta 1843, 137-149. https://doi.org/10.1016/j.bbamcr.2013.05.022
  15. Jenkins, J.R., Rudge, K., Chumakov, P., and Currie, G.A. (1985). The cellular oncogene p53 can be activated by mutagenesis. Nature 317, 816-818. https://doi.org/10.1038/317816a0
  16. Johansson, M. (1999). A human poly(ADP-ribose) polymerase gene family (ADPRTL): cDNA cloning of two novel poly(ADP-ribose) polymerase homologues. Genomics 57, 442-445. https://doi.org/10.1006/geno.1999.5799
  17. Kim, Y.H., and Koh, J.Y. (2002). The role of NADPH oxidase and neuronal nitric oxide synthase in zinc-induced poly(ADP-ribose) polymerase activation and cell death in cortical culture. Exp. Neurol. 177, 407-418. https://doi.org/10.1006/exnr.2002.7990
  18. Kroncke, K.D. (2003). Nitrosative stress and transcription. Biol. Chem. 384, 1365-1377.
  19. Lavin, M.F., and Gueven, N. (2006). The complexity of p53 stabilization and activation. Cell Death Differ. 13, 941-950. https://doi.org/10.1038/sj.cdd.4401925
  20. Lee, J.M., Kim, Y.J., Ra, H., Kang, S.J., Han, S., Koh, J.Y., and Kim, Y.H. (2008a). The involvement of caspase-11 in TPEN-induced apoptosis. FEBS Lett. 582, 1871-1876. https://doi.org/10.1016/j.febslet.2008.04.056
  21. Lee, J.Y., Kim, Y.J., Kim, T.Y., Koh, J.Y., and Kim, Y.H. (2008b). Essential role for zinc-triggered p75NTR activation in preconditioning neuroprotection. J. Neurosci. 28, 10919-10927. https://doi.org/10.1523/JNEUROSCI.3421-08.2008
  22. Li, N., and Chen, J. (2014). ADP-ribosylation: activation, recognition, and removal. Mol. Cells 37, 9-16. https://doi.org/10.14348/molcells.2014.2245
  23. Makhov, P., Golovine, K., Uzzo, R.G., Rothman, J., Crispen, P.L., Shaw, T., Scoll, B.J., and Kolenko, V.M. (2008). Zinc chelation induces rapid depletion of the X-linked inhibitor of apoptosis and sensitizes prostate cancer cells to TRAIL-mediated apoptosis. Cell Death Differ. 15, 1745-1751. https://doi.org/10.1038/cdd.2008.106
  24. Marini, M., and Musiani, D. (1998). Micromolar zinc affects endonucleolytic activity in hydrogen peroxide-mediated apoptosis. Exp. Cell Res. 239, 393-398. https://doi.org/10.1006/excr.1997.3909
  25. McCabe, M.J., Jr., Jiang, S.A., and Orrenius, S. (1993). Chelation of intracellular zinc triggers apoptosis in mature thymocytes. Lab. Invest. 69, 101-110.
  26. Mendes, F., Groessl, M., Nazarov, A.A., Tsybin, Y.O., Sava, G., Santos, I., Dyson, P.J., and Casini, A. (2011). Metal-based inhibition of poly(ADP-ribose) polymerase--the guardian angel of DNA. J. Med. Chem. 54, 2196-2206. https://doi.org/10.1021/jm2000135
  27. Nargi-Aizenman, J.L., Simbulan-Rosenthal, C.M., Kelly, T.A., Smulson, M.E., and Griffin, D.E. (2002). Rapid activation of poly(ADP-ribose) polymerase contributes to Sindbis virus and staurosporine-induced apoptotic cell death. Virology 293, 164-171. https://doi.org/10.1006/viro.2001.1253
  28. Nguyen, D., Zajac-Kaye, M., Rubinstein, L., Voeller, D., Tomaszewski, J.E., Kummar, S., Chen, A.P., Pommier, Y., Doroshow, J.H., and Yang, S.X. (2011). Poly(ADP-ribose) polymerase inhibition enhances p53-dependent and -independent DNA damage responses induced by DNA damaging agent. Cell Cycle 10, 4074-4082. https://doi.org/10.4161/cc.10.23.18170
  29. Ra, H., Kim, H.L., Lee, H.W., and Kim, Y.H. (2009). Essential role of p53 in TPEN-induced neuronal apoptosis. FEBS Lett. 583, 1516-1520. https://doi.org/10.1016/j.febslet.2009.04.008
  30. Simbulan-Rosenthal, C.M., Rosenthal, D.S., Iyer, S., Boulares, A.H., and Smulson, M.E. (1998). Transient poly(ADP-ribosyl)ation of nuclear proteins and role of poly(ADP-ribose) polymerase in the early stages of apoptosis. J. Biol. Chem. 273, 13703-13712. https://doi.org/10.1074/jbc.273.22.13703
  31. Simbulan-Rosenthal, C.M., Rosenthal, D.S., Luo, R., and Smulson, M.E. (1999). Poly(ADP-ribosyl)ation of p53 during apoptosis in human osteosarcoma cells. Cancer Res. 59, 2190-2194.
  32. Villalba, M., Ferrari, D., Bozza, A., Del Senno, L., and Di Virgilio, F. (1995). Ionic regulation of endonuclease activity in PC12 cells. Biochem. J. 311 (Pt 3), 1033-1038. https://doi.org/10.1042/bj3111033
  33. Wang, X., Ohnishi, K., Takahashi, A., and Ohnishi, T. (1998). Poly(ADP-ribosyl)ation is required for p53-dependent signal transduction induced by radiation. Oncogene 17, 2819-2825. https://doi.org/10.1038/sj.onc.1202216
  34. Widlak, P., and Garrard, W.T. (2001). Ionic and cofactor requirements for the activity of the apoptotic endonuclease DFF40/CAD. Mol. Cell. Biochem. 218, 125-130. https://doi.org/10.1023/A:1007231822086
  35. Wilson, D., Varigos, G., and Ackland, M.L. (2006). Apoptosis may underlie the pathology of zinc-deficient skin. Immunol. Cell Biol. 84, 28-37. https://doi.org/10.1111/j.1440-1711.2005.01391.x
  36. Won, J., Chung, S.Y., Kim, S.B., Byun, B.H., Yoon, Y.S., and Joe, C.O. (2006). Dose-dependent UV stabilization of p53 in cultured human cells undergoing apoptosis is mediated by poly(ADP-ribosyl) ation. Mol. Cells 21, 218-223.
  37. Zhao, J., Chen, J., Lu, B., Dong, L., Wang, H., Bi, C., Wu, G., Guo, H., Wu, M., and Guo, Y. (2008). TIP30 induces apoptosis under oxidative stress through stabilization of p53 messenger RNA in human hepatocellular carcinoma. Cancer Res. 68, 4133-4141. https://doi.org/10.1158/0008-5472.CAN-08-0432

Cited by

  1. Hydroquinone induces TK6 cell growth arrest and apoptosis through PARP-1/p53 regulatory pathway vol.32, pp.9, 2017, https://doi.org/10.1002/tox.22429
  2. Upregulated Expression of Karyopherin α2 is Involved in Neuronal Apoptosis Following Intracerebral Hemorrhage in Adult Rats vol.36, pp.5, 2016, https://doi.org/10.1007/s10571-015-0258-7
  3. Nickel(II)-induced nasal epithelial toxicity and oxidative mitochondrial damage vol.42, 2016, https://doi.org/10.1016/j.etap.2016.01.005
  4. Tricyclic Antidepressants Amitriptyline and Desipramine Induced Neurotoxicity Associated with Parkinson’s Disease vol.38, pp.8, 2015, https://doi.org/10.14348/molcells.2015.0131
  5. Bcl-2 protects TK6 cells against hydroquinone-induced apoptosis through PARP-1 cytoplasm translocation and stabilizing mitochondrial membrane potential 2017, https://doi.org/10.1002/em.22126
  6. Myricitrin decreases traumatic injury of the spinal cord and exhibits antioxidant and anti-inflammatory activities in a rat model via inhibition of COX-2, TGF-β1, p53 and elevation of Bcl-2/Bax signaling pathway vol.16, pp.5, 2017, https://doi.org/10.3892/mmr.2017.7567
  7. Effects of Myricitrin and Relevant Molecular Mechanisms vol.14, pp.None, 2015, https://doi.org/10.2174/1574888x14666181126103338
  8. Identifying New AMP-Activated Protein Kinase Inhibitors That Protect against Ischemic Brain Injury vol.10, pp.5, 2019, https://doi.org/10.1021/acschemneuro.8b00654
  9. Kaempferol attenuates spinal cord injury by interfering inflammatory and oxidative stress by targeting the p53 protein: a molecular docking analysis vol.17, pp.3, 2021, https://doi.org/10.1007/s13273-021-00132-x
  10. Autophagy and apoptosis cascade: which is more prominent in neuronal death? vol.78, pp.24, 2015, https://doi.org/10.1007/s00018-021-04004-4