Neurobiology of Aging
Volume 31, Issue 10 , Pages 1774-1786 , October 2010

A role for p53 in the β-amyloid-mediated regulation of the lysosomal system

Received 31 July 2006 ,Revised 8 September 2008 ,Accepted 30 September 2008.

References 

  1. Adamec E, Mohan PS, Cataldo AM, Vonsattel JP, Nixon RA. Up-regulation of the lysosomal system in experimental models of neuronal injury: implications for Alzheimer's disease. Neuroscience. 2000;100:663–675
  2. Antunes F, Cadenas E, Brunk UT. Apoptosis induced by exposure to a low steady-state concentration of H2O2 is a consequence of lysosomal rupture. Biochem. J. 2001;356:549–555
  3. Boland B, Campbell V. β-Amyloid (1–40)-induced apoptosis of cultured cortical neurones involves calpain-mediated cleavage of poly-ADP-ribose polymerase. Neurobiol. Aging. 2003;24:179–186
  4. Boland B, Campbell V. Aβ-mediated activation of the apoptotic cascade in cultured cortical neurones: a role for cathepsin-L Neurobiol. Aging. 2004;25:83–91
  5. Boya P, Andreau K, Poncet D, Zamzami N, Perfettini JL, Metivier D, et al. Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion. J. Exp. Med. 2003;197:1323–1334
  6. Boya P, Gonzalez-Polo RA, Poncet D, Andreau K, Vieira HL, Roumier T, et al. Mitochondrial membrane permeabilization is a critical step of lysosome-initiated apoptosis induced by hydroxychloroquine. Oncogene. 2003;22:3927–3936
  7. Brunk UT, Svensson I. Oxidative stress, growth factor starvation and Fas activation may all cause apoptosis through lysosomal leak. Redox Rep. 1999;4:3–11
  8. Chen CS, Chen WN, Zhou M, Arttamangkul S, Haugland RP. Probing the cathepsins using a BODIPY FL-pepstatin A: applications in florescence polarization and microscopy. J. Biochem. Biophys. Meth. 2000;42:137–151
  9. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science. 2004;303:1010–1014
  10. Chua CC, Liu X, Gao J, Hamdy RC, Chua BHL. Multiple actions of pifithrin-α on doxorubicin-induced apoptosis in rat myoblastic H9c2 cells A. J. Physiol. Heart Circ. Physiol. 2006;290:H2606–H2613
  11. Culmsee C, Zhu X, Yu Q-S, Chan SL, Camandola S, Guo Z, et al. A synthetic inhibitor of p53 protects neurons against death induced by ischemic and excitotoxic insults, and amyloid β-peptide. J. Neurochem. 2001;77:220–228
  12. Finucane DM, Bossy-Wetzel E, Waterhouse NJ, Cotter TG, Green DR. Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xl. J. Biol. Chem. 1999;274:2225–2233
  13. Fogarty MP, Downer EJ, Campbell V. A role for c-jun N terminal kinase 1 (JNK1), but not JNK2, in the β-amyloid-mediated stabilization of protein p53 and induction of the apoptotic cascade in cultured cortical neuron. Biochem. J. 2003;371:789–798
  14. Giovanni A, Keramaris E, Morris EJ, Hou ST, O’Hare M, Dyson N, et al. E2F1 mediates death of β-amyloid-treated cortical neurons in a manner independent of p53 and dependent on Bax and caspase-3. J. Biol. Chem. 2000;275(16):11553–11560
  15. Glenner GG, Wong CW. Alzheimer's disease and Down's syndrome: sharing of a unique cerebrovascular amyloid fibril protein. Biochem. Biophys. Res. Comm. 1984;122:1131–1135
  16. Gowran A, Campbell VA. A role for p53 in the regulation of lysosomal permeability by Δ9-tetrahydrocannabinol in rat cortical neurones: implications for neurodegeneration. J. Neurochem. 2008;105:1513–1524
  17. Gudkov AV, Komarova EA. Prospective therapeutic applications of p53 inhibitors. Biochem. Biophys. Res. Commun. 2005;331:726–736
  18. Hitami J, Katayama T, Eguchi Y, Kudo T, Taniguchi M, Koyama Y, et al. Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Aβ-induced cell death. J. Cell Biol. 2004;165:347–356
  19. Ishisaka R, Utsumi T, Kanno T, Arita K, Katunuma N, Akiyama J, et al. Participation of a cathepsin-L-type protease in the activation of caspase-3. Cell Struct. Funct. 1999;24:465–470
  20. Iwatsubo T, Odaka A, Suzuki N, Mizusawa H, Nukina N, Ihara Y. Visualization of Aβ42 and Aβ40 in senile plaques with end-specific β monoclonals: evidence that an initially deposited species is Aβ42. Neuron. 1994;13:45–53
  21. Ji Z-S, Miranda RD, Newhouse YM, Weisgraber KH, Hunag Y, Mahley RW. Apolipoprotein E4 potentiates amyloid β peptide-induced lysosomal leakage and apoptosis in neuronal cells. J. Biol. Chem. 2002;277:21821–21828
  22. Ji ZS, Mullendorff K, Cheng IH, Miranda RD, Huang Y, Mahley RW. reactivity of apolipoprotein E4 and β-amyloid: lysosomal stability and neurodegeneration. J. Biol. Chem. 2006;281(5):2683–2692
  23. Kagedal K, Johansson AC, Johansson U, Heimlich G, Roberg K, Wang NS, et al. Lysosomal membrane permeabilization during apoptosis: involvement of Bax?. Int. J. Exp. Pathol. 2005;86(5):309–321
  24. Kitamura Y, Shimohama S, Kamoshima W, Matsuoka Y, Nomura Y, Taniguchi T. Changes of p53 in the brains of patients with Alzheimer's disease.. Biochem. Biophys. Res. Commun. 1997;232:418–421
  25. Komarov PG, Komarova EA, Kondratov RV, Christov-Tselkov K, Coon JS, Chernov MV, et al. A chemical inhibitor of p53 that protects mice from the side effects of cancer. Science. 1999;285:1733–1737
  26. Komarova EA, Neznanov N, Komarov PG, Gudkov A. p53 inhibior, PFT-alpha can suppress heat shock and glucocorticold signalling pathways. J. Biol. Chem. 2003;278:15465–15468
  27. Laferla FM, Hall CK, Ngo L, Jay G. Extracellular deposition of beta-amyloid upon p53-dependent neuronal cell death in transgenic mice. J. Clin. Invest. 1996;98:1232–1626
  28. Lin N, Zheng Y, Chen W, Wang C, Lui X, He W, et al. Adaptor protein LAPF recruits phosphorylated p53 to lysosomes and triggers lysosomal destabilization in apoptosis. Cancer Res. 2007;67:11176–11185
  29. MacGibbon GA, Lawlor PA, Sirimanne ES, Walton MR, Connor B, Young D, et al. Bax expression in mammalian neurons undergoing apoptosis, and in Alzheimer's disease hippocampus. Brain Res. 1997;750:223–234
  30. MacManus A, Ramsden M, Murray M, Pearson HA, Campbell V. Enhancement of 45Ca 2+ influx and voltage-dependent Ca2+ channel activity by β-amyloid(1–40) in rat cortical synaptosomes and cultured cortical neurones: modulation by the proinflammatory cytokine interleukin-1β. J. Biol. Chem. 2000;275(5):4713–4718
  31. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, et al. p53 has a direct apoptogenic role at the mitochondria. Mol. Cell. 2003;11:577–590
  32. Miyashita T, Reed JC. Tumour suppressor p53 is a direct transcriptional activator of the human bax gene. Cell. 1995;80:293–299
  33. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by β-amyloid. Nature. 2000;403:98–103
  34. Paradis E, Douillard H, Koutroumanis M, Goodyer C, LeBlanc A. Amyloid beta peptide of Alzheimer's disease downregulates Bcl-2 and upregulates Bax expression in human neurons. J. Neurosci. 1996;16:7533–7539
  35. Pompl PN, Yemul S, Xiang Z, Ho L, Haroutunian V, Purohit D, et al. Caspase gene expression in the brain as a function of the clinical progression in Alzheimer's disease. Arch. Neurol. 2003;60:369–376
  36. Schuler M, Green DR. Mechanisms of p53-dependent apoptosis. Biochem. Soc. Trans. 2001;29:684–688
  37. Sedarous M, Keramaris E, O’Hare M, Melloni E, Slack RS, Elce JS, et al. Calpains mediate p53 activation and neuronal death evoked by DNA damage. J. Biol. Chem. 2003;278(28):26031–26038
  38. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, et al. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J. Cell Biol. 1999;144:281–292
  39. Stoka V, Turk B, Schendel SL, Kim TH, Cirman T, Snipas SJ, et al. Lysosomal protease pathways to apoptosis. Cleavage of bid, not pre-caspases, most likely route. J. Biol. Chem. 2001;276:3149–3157
  40. Troy CM, Rabacchi SA, Friedman WJ, Frappier TF, Brown K, Shelanski ML. Caspase-2 mediates neuronal cell death induced by β-amyloid. J. Neurosci. 2000;20:1386–1392
  41. Uetsuki T, Takemoto K, Nishimura I, Okamoto M, Niinobe M, Momoi T, et al. Activation of neuronal caspase-3 by intracellular accumulation of wild-type Alzheimer amyloid precursor protein. J. Neurosci. 1999;19:6955–6964
  42. Wang SQ, Du QS, Zhao K, Li AX, Wei DQ, Chou KC. Virtual screening for finding natural inhibitor against cathepsin-L for SARS therapy. Amino Acids. 2007;33:129–135
  43. White AR, Guirguis R, Brazier MW, Jobling MF, Hill AF, Beyreuther K, et al. Sublethal concentration of prion peptide PrP106-126 or the amyloid peptide protein of Alzheimer's disease activates expression of proapoptotic markers in primary cortical neurons. Neurobiol. Dis. 2001;8:299–316
  44. Yamashima T, Tonchev AB, Tsukada T, Saido TC, Imajoh-Ohmi S, Momoi T, et al. Sustained capain activation associated with lysosomal rupture executes necrosis of the postischemic CAI neurons in primates. Hippocampus. 2003;13(7):791–800
  45. Yoshida T, Tomioka I, Nagahara T, Holyst T, Sawada M, Hayes P, et al. Bax-inhibiting peptide derived from mouse and rat Ku70. Biochem. Biophys. Res. Commun. 2004;321:961–966
  46. Yuan X-M, Li W, Dalen H, Lotem J, Kama R, Sachs L, et al. Lysosomal destabilization in p53-induced apoptosis. Proc. Natl. Acad. Sci. U.S.A. 2002;99:6286–6291
  47. Zhang Y, McLaughlin R, Goodyer C, LeBlanc A. Selective cytotoxicity of intracellular amyloid β-peptide1–42 through p53 and Bax in cultured primary human neurons. J. Cell Biol. 2002;156:519–529
  48. Zhao M, Eaton JW, Brunk UT. Bcl-2 phosphorylation is required for inhibition of oxidative stress-induced lysosomal leak and ensuing apoptosis. FEBS Lett. 2001;14:405–412

PII: S0197-4580(08)00360-6

doi: 10.1016/j.neurobiolaging.2008.09.018

Neurobiology of Aging
Volume 31, Issue 10 , Pages 1774-1786 , October 2010