Nerve growth factor blocks thapsigargin-induced apoptosis at the level of the mitochondrion viaregulation of Bim

Journal of Cellular and Molecular Medicine

Volumn 12, Issue 6A, 2008, Pages 2482-2496

  Szegezdi, E ^a   Reed Herbert, K ^a   Kavanagh, E T ^a   Samali, A ^a   Gorman, A M ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Bimel; Endoplasmic reticulum (ER); Mitochondria; Nerve growth factor (NGF); Thapsigargin (TG)

Indexed keywords

APOPTOSIS REGULATORY PROTEIN; BAX PROTEIN, RAT; BCL 2 LIKE PROTEIN 11; BCL-2-LIKE PROTEIN 11; CASP12 PROTEIN, RAT; CASPASE 12; MEMBRANE PROTEIN; MESSENGER RNA; NERVE GROWTH FACTOR; ONCOPROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PRIMER DNA; PROTEIN BAX; SMALL INTERFERING RNA; THAPSIGARGIN;

ACTIVE TRANSPORT; ANIMAL; APOPTOSIS; ARTICLE; BIOLOGICAL MODEL; CELL STRAIN; DRUG ANTAGONISM; DRUG EFFECT; ENDOPLASMIC RETICULUM; GENETICS; METABOLISM; MITOCHONDRION; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROTEIN FOLDING; RAT; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BASE SEQUENCE; BCL-2-ASSOCIATED X PROTEIN; BIOLOGICAL TRANSPORT, ACTIVE; CASPASE 12; DNA PRIMERS; ENDOPLASMIC RETICULUM; MEMBRANE PROTEINS; MITOCHONDRIA; MODELS, BIOLOGICAL; NERVE GROWTH FACTOR; PC12 CELLS; PROTEIN FOLDING; PROTO-ONCOGENE PROTEINS; RATS; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; THAPSIGARGIN;

EID: 54949142920     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2008.00268.x     Document Type: Article

References (56)

1. Lindholm D, Wootz H, Korhonen L. ER stress and neurodegenerative diseases. Cell Death Differ. 2006 13 : 385 92.
2. Szegezdi E, Logue SE, Gorman AM, Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 2006 7 : 880 5.
3. Morishima N, Nakanishi K, Takenouchi H, Shibata T, Yasuhiko Y. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J Biol Chem. 2002 277 : 34287 94.
4. Rao RV, Castro-Obregon S, Frankowski H, Schuler M, Stoka V, del Rio G, Bredesen DE, Ellerby HM. Coupling endoplasmic reticulum stress to the cell death program. An Apaf-1-independent intrinsic pathway. J Biol Chem. 2002 277 : 21836 42.
5. Hitomi J, Katayama T, Taniguchi M, Honda A, Imaizumi K, Tohyama M. Apoptosis induced by endoplasmic reticulum stress depends on activation of caspase-3 via caspase-12. Neurosci Lett. 2004 357 : 127 30.
6. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 1997 91 : 479 89.
7. Zou H, Li Y, Liu X, Wang X. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates pro-caspase-9. J Biol Chem. 1999 274 : 11549 56.
8. Cory S, Adams JM. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer. 2002 2 : 647 56.
9. Willis SN, Adams JM. Life in the balance: how BH3-only proteins induce apoptosis. Curr Opin Cell Biol. 2005 17 : 617 25.
10. Galonek HL, Hardwick JM. Upgrading the BCL-2 Network. Nat Cell Biol. 2006 8 : 1317 9.
11. Kaplan DR, Miller FD. Signal transduction by the neurotrophin receptors. Curr Opin Cell Biol. 1997 9 : 213 21.
12. Deckwerth TL, Johnson EM, Jr. Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor. J Cell Biol. 1993 123 : 1207 22.
13. Mesner PW, Winters TR, Green SH. Nerve growth factor withdrawal-induced cell death in neuronal PC12 cells resembles that in sympathetic neurons. J Cell Biol. 1992 119 : 1669 80.
14. Salinas M, Diaz R, Abraham NG, Ruiz de Galarreta CM, Cuadrado A. Nerve growth factor protects against 6-hydroxy-dopamine-induced oxidative stress by increasing expression of heme oxygenase-1 in a phosphatidylinositol 3-kinase-depend-ent manner. J Biol Chem. 2003 278 : 13898 904.
15. Shimoke K, Kishi S, Utsumi T, Shimamura Y, Sasaya H, Oikawa T, Uesato S, Ikeuchi T. NGF-induced phos-phatidylinositol 3-kinase signaling pathway prevents thapsigargin-triggered ER stress-mediated apoptosis in PC12 cells. Neurosci Lett. 2005 389 : 124 8.
16. Shimoke K, Utsumi T, Kishi S, Nishimura M, Sasaya H, Kudo M, Ikeuchi T. Prevention of endoplasmic reticulum stress-induced cell death by brain-derived neurotrophic factor in cultured cerebral cortical neurons. Brain Res. 2004 1028 : 105 11.
17. Takadera T, Ohyashiki T. Apoptotic cell death and CPP32-like activation induced by thapsigargin and their prevention by nerve growth factor in PC12 cells. Biochim Biophys Acta. 1998 1401 : 63 71.
18. Kavanagh ET, Loughlin JP, Herbert KR, Dockery P, Samali A, Doyle KM, Gorman AM. Functionality of NGF-protected PC12 cells following exposure to 6-hydroxy-dopamine. Biochem Biophys Res Commun. 2006 351 : 890 5.
19. Yao R, Cooper GM. Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science. 1995 267 : 2003 6.
20. Crowder RJ, Freeman RS. Phosphatidylinositol 3-kinase and Akt protein kinase are necessary and sufficient for the survival of nerve growth factor-dependent sympathetic neurons. J Neurosci. 1998 18 : 2933 43.
21. Kaplan DR, Martin-Zanca D, Parada LF. Tyrosine phosphorylation and tyrosine kinase activity of the trk proto-oncogene product induced by NGF. Nature. 1991 350 : 158 60.
22. 2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci USA. 1990 87 : 2466 70.
23. Gorman AM, Szegezdi E, Quigney DJ, Samali A. Hsp27 inhibits 6-hydroxy-dopamine-induced cytochrome c release and apoptosis in PC12 cells. Biochem Biophys Res Commun. 2005 327 : 801 10.
24. 2+ pump levels in PC12 cells. Neuroreport. 2000 11 : 65 8.
25. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell. 2001 107 : 881 91.
26. Smith MI, Deshmukh M. Endoplasmic reticulum stress-induced apoptosis requires bax for commitment and Apaf-1 for execution in primary neurons. Cell Death Differ. 2007 14 : 1011 1019.
27. Zhang D, Armstrong JS. Bax and the mito-chondrial permeability transition cooperate in the release of cytochrome c during endoplasmic reticulum-stress-induced apoptosis. Cell Death Differ. 2007 14 : 703 715.
28. Boya P, Cohen I, Zamzami N, Vieira HL, Kroemer G. Endoplasmic reticulum stress-induced cell death requires mitochondrial membrane permeabilization. Cell Death Differ. 2002 9 : 465 7.
29. Wright KM, Linhoff MW, Potts PR, Deshmukh M. Decreased apoptosome activity with neuronal differentiation sets the threshold for strict IAP regulation of apoptosis. J Cell Biol. 2004 167 : 303 13.
30. Annis MG, Soucie EL, Dlugosz PJ, Cruz-Aguado JA, Penn LZ, Leber B, Andrews DW. Bax forms multispanning monomers that oligomerize to permeabilize membranes during apoptosis. EMBO J. 2005 24 : 2096 103.
31. Katoh S, Mitsui Y, Kitani K, Suzuki T. The rescuing effect of nerve growth factor is the result of up-regulation of bcl-2 in hyperoxia-induced apoptosis of a subclone of pheochromocytoma cells, PC12h. Neurosci Lett. 1997 232 : 71 4.
32. Bui NT, Livolsi A, Peyron JF, Prehn JH. Activation of nuclear factor kappaB and Bcl-x survival gene expression by nerve growth factor requires tyrosine phospho-rylation of IkappaBalpha. J Cell Biol. 2001 152 : 753 64.
33. Morishima N, Nakanishi K, Tsuchiya K, Shibata T, Seiwa E. Translocation of Bim to the Endoplasmic Reticulum (ER) Mediates ER Stress Signaling for Activation of Caspase-12 during ER Stress-induced Apoptosis. J Biol Chem. 2004 279 : 50375 81.
34. Patapoutian A, Reichardt LF. Trk receptors: mediators of neurotrophin action. Curr Opin Neurobiol. 2001 11 : 272 80.
35. Stahl M, Dijkers PF, Kops GJ, Lens SM, Coffer PJ, Burgering BM, Medema RH. The forkhead transcription factor FoxO regulates transcription of p27Kip1 and Bim in response to IL-2. J Immunol. 2002 168 : 5024 31.
36. Dijkers PF, Medema RH, Lammers JW, Koenderman L, Coffer PJ. Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr Biol. 2000 10 : 1201 4.
37. Walker EH, Pacold ME, Perisic O, Stephens L, Hawkins PT, Wymann MP, Williams RL. Structural determinants of phosphoinositide 3-kinase inhibition by wortmannin, LY294002, quercetin, myricetin, and staurosporine. Mol Cell. 2000 6 : 909 19.
38. Shimoke K, Amano H, Kishi S, Uchida H, Kudo M, Ikeuchi T. Nerve growth factor attenuates endoplasmic reticulum stress-mediated apoptosis via suppression of caspase-12 activity. J Biochem (Tokyo). 2004 135 : 439 46.
39. Elyaman W, Terro F, Suen KC, Yardin C, Chang RC, Hugon J. BAD and Bcl-2 regulation are early events linking neuronal endoplasmic reticulum stress to mitochondria-mediated apoptosis. Brain Res Mol Brain Res. 2002 109 : 233 8.
40. Mao W, Iwai C, Keng PC, Vulapalli R, Liang CS. Norepinephrine-induced oxidative stress causes PC-12 cell apoptosis by both endoplasmic reticulum stress and mitochondrial intrinsic pathway: inhibition of phosphatidylinositol 3-kinase survival pathway. Am J Physiol Cell Physiol. 2006 290 : C1373 84.
41. Puthalakath H, O'Reilly LA, Gunn P, Lee L, Kelly PN, Huntington ND, Hughes PD, Michalak EM, McKimm-Breschkin J, Motoyama N, Gotoh T, Akira S, Bouillet P, Strasser A. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell. 2007 129 : 1337 49.
42. Reimertz C, Kogel D, Rami A, Chittenden T, Prehn JH. Gene expression during ER stress-induced apoptosis in neurons: induction of the BH3-only protein Bbc3/PUMA and activation of the mitochondrial apoptosis pathway. J Cell Biol. 2003 162 : 587 97.
43. Biswas SC, Greene LA. Nerve growth factor (NGF) down-regulates the Bcl-2 homology 3 (BH3) domain-only protein Bim and suppresses its proapoptotic activity by phosphorylation. J Biol Chem. 2002 277 : 49511 6.
44. Biswas SC, Shi Y, Sproul A, Greene LA. Pro-apoptotic bim induction in response to NGF deprivation requires simultaneous activation of three different death signaling pathways. J Biol Chem. 2007 282 : 29368 74.
45. Wang GL, Iakova P, Wilde M, Awad S, Timchenko NA. Liver tumors escape negative control of proliferation via PI3K/Akt-mediated block of C/EBP alpha growth inhibitory activity. Genes Dev. 2004 18 : 912 25.
46. Datta J, Majumder S, Kutay H, Motiwala T, Frankel W, Costa R, Cha HC, MacDougald OA, Jacob ST, Ghoshal K. Metallothionein expression is suppressed in primary human hepatocellular carcinomas and is mediated through inactivation of CCAAT/enhancer binding protein alpha by phosphatidylinositol 3-kinase signaling cascade. Cancer Res. 2007 67 : 2736 46.
47. Ley R, Ewings KE, Hadfield K, Cook SJ. Regulatory phosphorylation of Bim: sorting out the ERK from the JNK. Cell Death Differ. 2005 12 : 1008 14.
48. el apoptotic function. J Biol Chem. 2006 281 : 813 23.
49. Zhou H, Li XM, Meinkoth J, Pittman RN. Akt regulates cell survival and apoptosis at a postmitochondrial level. J Cell Biol. 2000 151 : 483 94.
50. Eves EM, Xiong W, Bellacosa A, Kennedy SG, Tsichlis PN, Rosner MR, Hay N. Akt, a target of phosphatidylinositol 3-kinase, inhibits apoptosis in a differentiating neu-ronal cell line. Mol Cell Biol. 1998 18 : 2143 52.
51. Kim H, Rafiuddin-Shah M, Tu HC, Jeffers JR, Zambetti G P, Hsieh JJ, Cheng EH. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol. 2006 8 : 1348 58.
52. 2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science. 1999 284 : 339 43.
53. Kennedy SG, Kandel ES, Cross TK, Hay N. Akt/Protein kinase B inhibits cell death by preventing the release of cytochrome c from mitochondria. Mol Cell Biol. 1999 19 : 5800 10.
54. Hoozemans JJ, van Haastert ES, Eikelenboom P, de Vos RA, Rozemuller JM, Scheper W. Activation of the unfolded protein response in Parkinson's disease. Biochem Biophys Res Commun. 2007 354 : 707 11.
55. Hoozemans JJ, Veerhuis R, Van Haastert ES, Rozemuller JM, Baas F, Eikelenboom P, Scheper W. The unfolded protein response is activated in Alzheimer's disease. Acta Neuropathol. 2005 110 : 165 72.
56. Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, Inoue K, Hori S, Kakizuka A, Ichijo H. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev. 2002 16 : 1345 55.