Over-expression of HSP70 attenuates caspase-dependent and caspase-independent pathways and inhibits neuronal apoptosis

Journal of Neurochemistry

Volumn 123, Issue 4, 2012, Pages 542-554

  Sabirzhanov, Boris ^a   Stoica, Bogdan A ^a   Hanscom, Marie ^a   Piao, Chun Shu ^a   Faden, Alan I ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

AIF; Apaf 1; apoptosis; HSP70; neurons; neuroprotection

Indexed keywords

ALLOGRAFT INFLAMMATORY FACTOR 1; AMYLOID BETA PROTEIN[25-35]; APOPTOSIS INDUCING FACTOR; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; C2 CERAMIDE; CASPASE 3; CASPASE 9; CERAMIDE; ETOPOSIDE; HEAT SHOCK PROTEIN 70; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; STAUROSPORINE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CELL; CELL DEATH; CELL LINE; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; NEUROPROTECTION; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION;

AMYLOID BETA-PEPTIDES; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CASPASES; CELLS, CULTURED; CEREBRAL CORTEX; EMBRYO, MAMMALIAN; ETOPOSIDE; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOPRECIPITATION; NEURAL INHIBITION; NEUROBLASTOMA; NEURONS; PEPTIDE FRAGMENTS; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN BINDING; RATS; SIGNAL TRANSDUCTION; SPHINGOSINE; STAUROSPORINE; TRANSFECTION;

EID: 84867581392     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07927.x     Document Type: Article

References (57)

1. Amin V., Cumming D. V., Coffin R. S., and, Latchman D. S., (1995) The degree of protection provided to neuronal cells by a pre-conditioning stress correlates with the amount of heat shock protein 70 it induces and not with the similarity of the subsequent stress. Neurosci. Lett. 200, 85-88.
2. Artus C., Boujrad H., Bouharrour A., et al,. (2010) AIF promotes chromatinolysis and caspase-independent programmed necrosis by interacting with histone H2AX. EMBO J. 29, 1585-1599.
3. Beere H. M., Wolf B. B., Cain K., et al,. (2000) Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat. Cell Biol. 2, 469-475.
4. Bellmann K., Jaattela M., Wissing D., Burkart V., and, Kolb H., (1996) Heat shock protein hsp70 overexpression confers resistance against nitric oxide. FEBS Lett. 391, 185-188.
5. Bhat R. V., Shanley J., Correll M. P., Fieles W. E., Keith R. A., Scott C. W., and, Lee C. M., (2000) Regulation and localization of tyrosine216 phosphorylation of glycogen synthase kinase-3beta in cellular and animal models of neuronal degeneration. Proc. Natl Acad. Sci. USA 97, 11074-11079.
6. Brana C., Benham C., and, Sundstrom L., (2002) A method for characterising cell death in vitro by combining propidium iodide staining with immunohistochemistry. Brain Res. Brain Res. Protoc. 10, 109-114.
7. Bukau B., Deuerling E., Pfund C., and, Craig E. A., (2000) Getting newly synthesized proteins into shape. Cell 101, 119-122.
8. Chow A. M., Steel R., and, Anderson R. L., (2009) Hsp72 chaperone function is dispensable for protection against stress-induced apoptosis. Cell Stress Chaperones 14, 253-263.
9. Clemons N. J., Buzzard K., Steel R., and, Anderson R. L., (2005) Hsp72 inhibits Fas-mediated apoptosis upstream of the mitochondria in type II cells. J. Biol. Chem. 280, 9005-9012.
10. Cordeiro M. F., Guo L., Coxon K. M., et al,. (2010) Imaging multiple phases of neurodegeneration: a novel approach to assessing cell death in vivo. Cell Death Dis. 1, e3.
11. Fink S. L., Chang L. K., Ho D. Y., and, Sapolsky R. M., (1997) Defective herpes simplex virus vectors expressing the rat brain stress-inducible heat shock protein 72 protect cultured neurons from severe heat shock. J. Neurochem. 68, 961-969.
12. Gribaldo S., Lumia V., Creti R., Conway de Macario E., Sanangelantoni A., and, Cammarano P., (1999) Discontinuous occurrence of the hsp70 (dnaK) gene among Archaea and sequence features of HSP70 suggest a novel outlook on phylogenies inferred from this protein. J. Bacteriol. 181, 434-443.
13. Hageman J., and, Kampinga H. H., (2009) Computational analysis of the human HSPH/HSPA/DNAJ family and cloning of a human HSPH/HSPA/DNAJ expression library. Cell Stress Chaperones 14, 1-21.
14. Harada J., and, Sugimoto M., (1999) Activation of caspase-3 in beta-amyloid-induced apoptosis of cultured rat cortical neurons. Brain Res. 842, 311-323.
15. Hartl F. U., and, Hayer-Hartl M., (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852-1858.
16. Hetman M., Cavanaugh J. E., Kimelman D., and, Xia Z., (2000) Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal. J. Neurosci. 20, 2567-2574.
17. Kelly S., Bieneman A., Horsburgh K., Hughes D., Sofroniew M. V., McCulloch J., and, Uney J. B., (2001) Targeting expression of hsp70i to discrete neuronal populations using the Lmo-1 promoter: assessment of the neuroprotective effects of hsp70i in vivo and in vitro. J. Cereb. Blood Flow Metab. 21, 972-981.
18. Koh J. Y., Wie M. B., Gwag B. J., Sensi S. L., Canzoniero L. M., Demaro J., Csernansky C., and, Choi D. W., (1995) Staurosporine-induced neuronal apoptosis. Exp. Neurol. 135, 153-159.
19. Lee J. E., Yenari M. A., Sun G. H., Xu L., Emond M. R., Cheng D., Steinberg G. K., and, Giffard R. G., (2001) Differential neuroprotection from human heat shock protein 70 overexpression in in vitro and in vivo models of ischemia and ischemia-like conditions. Exp. Neurol. 170, 129-139.
20. Li G. C., (1983) Induction of thermotolerance and enhanced heat shock protein synthesis in Chinese hamster fibroblasts by sodium arsenite and by ethanol. J. Cell. Physiol. 115, 116-122.
21. Li G. C., Li L., Liu R. Y., Rehman M., and, Lee W. M., (1992) Heat shock protein hsp70 protects cells from thermal stress even after deletion of its ATP-binding domain. Proc. Natl Acad. Sci. USA 89, 2036-2040.
22. Li P., Nijhawan D., Budihardjo I., Srinivasula S. M., Ahmad M., Alnemri E. S., and, Wang X., (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479-489.
23. Lowenstein D. H., Chan P. H., and, Miles M. F., (1991) The stress protein response in cultured neurons: characterization and evidence for a protective role in excitotoxicity. Neuron 7, 1053-1060.
24. Mailhos C., Howard M. K., and, Latchman D. S., (1993) Heat shock protects neuronal cells from programmed cell death by apoptosis. Neuroscience 55, 621-627.
25. Mailhos C., Howard M. K., and, Latchman D. S., (1994) Heat shock proteins hsp90 and hsp70 protect neuronal cells from thermal stress but not from programmed cell death. J. Neurochem. 63, 1787-1795.
26. Majdzadeh N., Wang L., Morrison B. E., Bassel-Duby R., Olson E. N., and, D'Mello S. R., (2008) HDAC4 inhibits cell-cycle progression and protects neurons from cell death. Dev. Neurobiol. 68, 1076-1092.
27. Matsumori Y., Hong S. M., Aoyama K., et al,. (2005) Hsp70 overexpression sequesters AIF and reduces neonatal hypoxic/ischemic brain injury. J. Cereb. Blood Flow Metab. 25, 899-910.
28. Mosser D. D., Caron A. W., Bourget L., Denis-Larose C., and, Massie B., (1997) Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol. Cell. Biol. 17, 5317-5327.
29. Movsesyan V. A., Yakovlev A. G., Dabaghyan E. A., Stoica B. A., and, Faden A. I., (2002) Ceramide induces neuronal apoptosis through the caspase-9/caspase-3 pathway. Biochem. Biophys. Res. Commun. 299, 201-207.
30. Movsesyan V. A., Stoica B. A., and, Faden A. I., (2004) MGLuR5 activation reduces beta-amyloid-induced cell death in primary neuronal cultures and attenuates translocation of cytochrome c and apoptosis-inducing factor. J. Neurochem. 89, 1528-1536.
31. Nakajima M., Kashiwagi K., Ohta J., Furukawa S., Hayashi K., Kawashima T., and, Hayashi Y., (1994) Etoposide induces programmed death in neurons cultured from the fetal rat central nervous system. Brain Res. 641, 350-352.
32. Nardi N., Avidan G., Daily D., Zilkha-Falb R., and, Barzilai A., (1997) Biochemical and temporal analysis of events associated with apoptosis induced by lowering the extracellular potassium concentration in mouse cerebellar granule neurons. J. Neurochem. 68, 750-759.
33. Neupert W., and, Brunner M., (2002) The protein import motor of mitochondria. Nat. Rev. Mol. Cell Biol. 3, 555-565.
34. Papadopoulos M. C., Sun X. Y., Cao J., Mivechi N. F., and, Giffard R. G., (1996) Over-expression of HSP-70 protects astrocytes from combined oxygen-glucose deprivation. NeuroReport 7, 429-432.
35. Patel Y. J., Payne Smith M. D., de Belleroche J., and, Latchman D. S., (2005) Hsp27 and Hsp70 administered in combination have a potent protective effect against FALS-associated SOD1-mutant-induced cell death in mammalian neuronal cells. Brain Res. Mol. Brain Res. 134, 256-274.
36. Pfister J. A., Ma C., Morrison B. E., and, D'Mello S. R., (2008) Opposing effects of sirtuins on neuronal survival: sIRT1-mediated neuroprotection is independent of its deacetylase activity. PLoS ONE 3, e4090.
37. Pratt W. B., and, Toft D. O., (2003) Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp. Biol. Med. (Maywood) 228, 111-133.
38. Ravagnan L., Gurbuxani S., Susin S. A., et al,. (2001) Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat. Cell Biol. 3, 839-843.
39. Le Rhun Y., Kirkland J. B., and, Shah G. M., (1998) Cellular responses to DNA damage in the absence of Poly(ADP-ribose) polymerase. Biochem. Biophys. Res. Commun. 245, 1-10.
40. Rordorf G., Koroshetz W. J., and, Bonventre J. V., (1991) Heat shock protects cultured neurons from glutamate toxicity. Neuron 7, 1043-1051.
41. Ryan M. T., and, Pfanner N., (2001) Hsp70 proteins in protein translocation. Adv. Protein Chem. 59, 223-242.
42. Saleh A., Srinivasula S. M., Balkir L., Robbins P. D., and, Alnemri E. S., (2000) Negative regulation of the Apaf-1 apoptosome by Hsp70. Nat. Cell Biol. 2, 476-483.
43. Sinn D. I., Chu K., Lee S. T., et al,. (2007) Pharmacological induction of heat shock protein exerts neuroprotective effects in experimental intracerebral hemorrhage. Brain Res. 1135, 167-176.
44. Srinivasula S. M., Ahmad M., Fernandes-Alnemri T., and, Alnemri E. S., (1998) Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol. Cell 1, 949-957.
45. Stankiewicz A. R., Lachapelle G., Foo C. P., Radicioni S. M., and, Mosser D. D., (2005) Hsp70 inhibits heat-induced apoptosis upstream of mitochondria by preventing Bax translocation. J. Biol. Chem. 280, 38729-38739.
46. Steel R., Doherty J. P., Buzzard K., Clemons N., Hawkins C. J., and, Anderson R. L., (2004) Hsp72 inhibits apoptosis upstream of the mitochondria and not through interactions with Apaf-1. J. Biol. Chem. 279, 51490-51499.
47. Stoica B. A., Movsesyan V. A., Knoblach S. M., and, Faden A. I., (2005) Ceramide induces neuronal apoptosis through mitogen-activated protein kinases and causes release of multiple mitochondrial proteins. Mol. Cell. Neurosci. 29, 355-371.
48. Susin S. A., Lorenzo H. K., Zamzami N., et al,. (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397, 441-446.
49. Turturici G., Sconzo G., and, Geraci F., (2011) Hsp70 and its molecular role in nervous system diseases. Biochem. Res. Int. 2011, 618127.
50. Volbracht C., Leist M., Kolb S. A., and, Nicotera P., (2001) Apoptosis in caspase-inhibited neurons. Mol. Med. 7, 36-48.
51. Wagstaff M. J., Collaco-Moraes Y., Smith J., de Belleroche J. S., Coffin R. S., and, Latchman D. S., (1999) Protection of neuronal cells from apoptosis by Hsp27 delivered with a herpes simplex virus-based vector. J. Biol. Chem. 274, 5061-5069.
52. van der Weerd L., Lythgoe M. F., Badin R. A., Valentim L. M., Akbar M. T., de Belleroche J. S., Latchman D. S., and, Gadian D. G., (2005) Neuroprotective effects of HSP70 overexpression after cerebral ischaemia-an MRI study. Exp. Neurol. 195, 257-266.
53. Wyatt S., Mailhos C., and, Latchman D. S., (1996) Trigeminal ganglion neurons are protected by the heat shock proteins hsp70 and hsp90 from thermal stress but not from programmed cell death following nerve growth factor withdrawal. Brain Res. Mol. Brain Res. 39, 52-56.
54. Xu L., and, Giffard R. G., (1997) HSP70 protects murine astrocytes from glucose deprivation injury. Neurosci. Lett. 224, 9-12.
55. Yakovlev A. G., Ota K., Wang G., Movsesyan V., Bao W. L., Yoshihara K., and, Faden A. I., (2001) Differential expression of apoptotic protease-activating factor-1 and caspase-3 genes and susceptibility to apoptosis during brain development and after traumatic brain injury. J. Neurosci. 21, 7439-7446.
56. Young J. C., Barral J. M., and, Ulrich Hartl F., (2003) More than folding: localized functions of cytosolic chaperones. Trends Biochem. Sci. 28, 541-547.
57. Zourlidou A., Payne Smith M. D., and, Latchman D. S., (2004) HSP27 but not HSP70 has a potent protective effect against alpha-synuclein-induced cell death in mammalian neuronal cells. J. Neurochem. 88, 1439-1448.