Dopamine-induced toxicity is synergistically potentiated by simultaneous HSP-90 and Akt inhibition in oligodendrocyte progenitors

Journal of Neurochemistry

Volumn 105, Issue 4, 2008, Pages 1223-1234

  Hemdan, Sandy ^a   Almazan, Guillermina ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Apoptosis; Dopamine; Heat shock proteins; Oligodendrocyte progenitors; Oxidative stress; Periventricular leucomalacia

Indexed keywords

ALPHA CRYSTALLIN; CASPASE 3; DOPAMINE; HEAT SHOCK PROTEIN 10; HEAT SHOCK PROTEIN 25; HEAT SHOCK PROTEIN 72; HEAT SHOCK PROTEIN 90; PROTEIN KINASE B; PROTEIN KINASE B INHIBITOR; TANESPIMYCIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL LOSS; CELL MATURATION; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME INHIBITION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; STEM CELL; UPREGULATION;

ANIMALS; ANIMALS, NEWBORN; BENZOQUINONES; CELL DIFFERENTIATION; CELLS, CULTURED; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; HSP90 HEAT-SHOCK PROTEINS; LACTAMS, MACROCYCLIC; OLIGODENDROGLIA; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; STEM CELLS;

EID: 42549157506     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05227.x     Document Type: Article

References (71)

1. Ahagon A., Ishikawa M. Handa H. (1980) Histochemical changes of brain dopamine in an acute stage of cerebral ischemia in gerbils. Stroke J. Cerebral Circ. 11, 622 628.
2. Akiyama Y., Koshimura K., Ohue T., Lee K., Miwa S., Yamagata S. Kikuchi H. (1991) Effects of hypoxia on the activity of the dopaminergic neuron system in the rat striatum as studied by in vivo brain microdialysis. J. Neurochem. 57, 997 1002.
3. Almazan G., Afar D. E. Bell J. C. (1993) Phosphorylation and disruption of intermediate filament proteins in oligodendrocyte precursor cultures treated with calyculin A. J. Neurosci. Res. 36, 163 172.
4. Back S. A., Gan X., Li Y., Rosenberg P. A. Volpe J. J. (1998) Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J. Neurosci. 18, 6241 6253.
5. Back S. A., Han B. H., Luo N. L., Chricton C. A., Xanthoudakis S., Tam J., Arvin K. L. Holtzman D. M. (2002) Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J. Neurosci. 22, 455 463.
6. Barker C. R., McNamara A. V., Rackstraw S. A., Nelson D. E., White M. R., Watson A. J. Jenkins J. R. (2006) Inhibition of Hsp90 acts synergistically with topoisomerase II poisons to increase the apoptotic killing of cells due to an increase in topoisomerase II mediated DNA damage. Nucleic Acids Res. 34, 1148 1157.
7. Basso A. D., Solit D. B., Chiosis G., Giri B., Tsichlis P. Rosen N. (2002) Akt forms an intracellular complex with heat shock protein 90 (Hsp90) and Cdc37 and is destabilized by inhibitors of Hsp90 function. J. Biol. Chem. 277, 39858 39866.
8. Baud O., Li J., Zhang Y., Neve R. L., Volpe J. J. Rosenberg P. A. (2004) Nitric oxide-induced cell death in developing oligodendrocytes is associated with mitochondrial dysfunction and apoptosis-inducing factor translocation. Eur. J. Neurosci. 20, 1713 1726.
9. Beere H. M. (2005) Death versus survival: functional interaction between the apoptotic and stress-inducible heat shock protein pathways. J. Clin. Invest. 115, 2633 2639.
10. Brami-Cherrier K., Valijent E., Garcia M., Pages C., Hipskind R. A. Caboche J. (2002) Dopamine induces a PI3-Kinase-Independent Activation of Akt in Striatal Neurons: A New Route to cAMP Response Element-Binding Protein Phosphorylation. J. Neurosci. 22, 8911 8921.
11. Buisson A., Callebert J., Mathieu E., Plotkine M. Boulu R. G. (1992) Striatal protection induced by lesioning the substantia nigra of rats subjected to focal ischemia. J. Neurochem. 59, 1153 1157.
12. Cao Y., Gunn A. J., Bennet L., Wu D., George S., Gluckman P. D., Shao X. M. Guan J. (2003) Insulin-like growth factor (IGF)-1 suppresses oligodendrocyte caspase-3 activation and increases glial proliferation after ischemia in near-term fetal sheep. J. Cereb. Blood Flow Metab. 23, 739 747.
13. Casaccia-Bonnefil P. (2000) Cell death in the oligodendrocyte lineage: a molecular perspective of life/death decisions in development and disease. Glia 29, 124 135.
14. Cohen R. I. Almazan G. (1994) Rat oligodendrocytes express muscarinic receptors coupled to phosphoinositide hydrolysis and adenylyl cyclase. Eur. J. Neurosci. 6, 1213 1224.
15. Cragg S. J., Nicholson C., Kume-Kick J., Tao L. Rice M. E. (2001) Dopamine-mediated volume transmission in midbrain is regulated by distinct extracellular geometry and uptake. J. Neurophysiol. 85, 1761 1771.
16. Cui Q. L., Zheng W. H., Quirion R. Almazan G. (2005) Inhibition of Src-like kinases reveals Akt-dependent and -independent pathways in insulin-like growth factor I-mediated oligodendrocyte progenitor survival. J. Biol. Chem. 280, 8918 8928.
17. Datta S. R., Brunet A. Greenberg M. E. (1999) Cellular survival: a play in three Akts. Genes Dev. 13, 2905 2927.
18. De Louw A. J., Van De Berg W. D., De Vente J., Blanco C. E., Gavilanes A. W., Steinbusch H. P., Steinbusch H. W., Troost J. Vles J. S. (2002) Developmental apoptosis in the spinal cord white matter in neonatal rats. Glia 37, 89 91.
19. Dello Russo C., Polak P. E., Mercado P. R. et al. (2006) The heat-shock protein 90 inhibitor 17-allylamino-17-demethoxygeldanamycin suppresses glial inflammatory responses and ameliorates experimental autoimmune encephalomyelitis. J. Neurochem. 99, 1351 1362.
20. Dewar D., Underhill S. M. Goldberg M. P. (2003) Oligodendrocytes and ischemic brain injury. J. Cereb. Blood Flow Metab. 23, 263 274.
21. Fragoso G., Martinez-Bermudez A. K., Liu H. N., Khorchid A., Chemtob S., Mushynski W. E. Almazan G. (2004) Developmental differences in HO-induced oligodendrocyte cell death: role of glutathione, mitogen-activated protein kinases and caspase 3. J. Neurochem. 90, 392 404.
22. Georgakis G. V., Li Y. Younes A. (2006) The heat shock protein 90 inhibitor 17-AAG induces cell cycle arrest and apoptosis in mantle cell lymphoma cell lines by depleting cyclin D1, Akt, Bid and activating caspase 9. Br. J. Haematol. 135, 68 71.
23. George P., Bali P., Cohen P. et al. (2004) Cotreatment with 17-allylamino-demethoxygeldanamycin and FLT-3 kinase inhibitor PKC412 is highly effective against human acute myelogenous leukemia cells with mutant FLT-3. Cancer Res. 64, 3645 3652.
24. Goldbaum O. Richter-Landsberg C. (2001) Stress proteins in oligodendrocytes: differential effects of heat shock and oxidative stress. J. Neurochem. 78, 1233 1242.
25. Gordon N. (2003) Alexander disease. Eur J Paediatr Neurol. 7, 395 399.
26. Graham D. G. (1978) Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones. Mol. Pharmacol. 14, 633 643.
27. Hastings T. G. (1995) Enzymatic oxidation of dopamine: the role of prostaglandin H synthase. J. Neurochem. 64, 919 924.
28. Hayes R. L., Yang K., Raghupathi R. McIntosh T. K. (1995) Changes in gene expression following traumatic brain injury in the rat. J. Neurotrauma 12, 779 790.
29. Helmbrecht K., Zeise E. Rensing L. (2000) Chaperones in cell cycle regulation and mitogenic signal transduction: a review. Cell Prolif. 33, 341 365.
30. Hemdan S. Almazan G. (2006) Iron contributes to dopamine-induced toxicity in oligodendrocyte progenitors. Neuropathol. Appl. Neurobiol. 32, 428 440.
31. Hemdan S. Almazan G. (2007) Deficient peroxide detoxification underlies the susceptibility of oligodendrocyte progenitors to dopamine toxicity. Neuropharmacology 52, 1385 1395.
32. Hirai K., Hayashi T., Chan P. H., Zeng J., Yang G. Y., Basus V. J., James T. L. Litt L. (2004) PI3K inhibition in neonatal rat brain slices during and after hypoxia reduces phospho-Akt and increases cytosolic cytochrome c and apoptosis. Brain Res. Mol. Brain Res. 124, 51 61.
33. Hsu H. Y., Wu H. L., Tan S. K., Li V. P., Wang W. T., Hsu J. Cheng C. H. (2007) Geldanamycin interferes with the 90-kDa heat shock protein, affecting lipopolysaccharide-mediated interleukin-1 expression and apoptosis within macrophages. Mol. Pharmacol. 71, 344 356.
34. Jelinski S. E., Yager J. Y. Juurlink B. H. (1999) Preferential injury of oligodendroblasts by a short hypoxic-ischemic insult. Brain Res. 815, 150 153.
35. Kato H., Liu Y., Kogure K. Kato K. (1994) Induction of 27-kDa heat shock protein following cerebral ischemia in a rat model of ischemic tolerance. Brain Res. 634, 235 244.
36. Kau T. R., Schroeder F., Ramaswamy S., Wojciechowski C. L., Zhao J. J., Roberts T. M., Clardy J., Sellers W. R. Silver P. A. (2003) A chemical genetic screen identifies inhibitors of regulated nuclear export of a Forkhead transcription factor in PTEN-deficient tumor cells. Cancer cell 4, 463 476.
37. Kawagoe J., Abe K., Aoki M. Kogure K. (1993) Induction of HSP90 alpha heat shock mRNA after transient global ischemia in gerbil hippocampus. Brain Res. 621, 121 125.
38. Kennedy S. G., Kandel E. S., Cross T. K. Hay N. (1999) Akt/Protein kinase B inhibits cell death by preventing the release of cytochrome c from mitochondria. Mol. Cell. Biol. 19, 5800 5810.
39. Khorchid A., Fragoso G., Shore G. Almazan G. (2002) Catecholamine-induced oligodendrocyte cell death in culture is developmentally regulated and involves free radical generation and differential activation of caspase-3. Glia 40, 283 299.
40. Knoblach S. M., Huang X., VanGelderen J., Calva-Cerqueira D. Faden A. I. (2005) Selective caspase activation may contribute to neurological dysfunction after experimental spinal cord trauma. J. Neurosci. Res. 80, 369 380.
41. Koga F., Xu W., arpova T. S., McNally J. G., Baron R. Neckers L. (2006) HSP90 inhibition transiently activates Src kinase and promotes Src-dependent Akt and ER activation. PNAS 103, 11318 11322.
42. Leslie N. R., Bennett D., Lindsay Y. E., Stewart H., Gray A. Downes C. P. (2003) Redox regulation of PI3-kinase signalling via inactivation of PTEN. EMBO J. 22, 5501 5510.
43. Lin S., Fan L. W., Pang Y., Rhodes P. G., Mitchell H. J. Cai Z. (2005) IGF-1 protects oligodendrocyte progenitor cells and improves neurological functions following cerebral hypoxia-ischemia in the neonatal rat. Brain Res. 1063, 15 26.
44. Liu H. N., Giasson B. I., Mushynski W. E. Almazan G. (2002) AMPA receptor-mediated toxicity in oligodendrocyte progenitors involves free radical generation and activation of JNK, calpain and caspase 3. J. Neurochem. 82, 398 409.
45. Luo H. R., Hattori H., Hossain M. A., Hester L., Huang Y., Lee-Kwon W., Donowitz M., Nagata E. Snyder S. H. (2003) Akt as a mediator of cell death. Proc. Natl Acad. Sci. USA 100, 11712 11717.
46. Mariucci G., Tantucci M., Giuditta A. Ambrosini M. V. (2007) Permanent brain ischemia induces marked increments in hsp72 expression and local protein synthesis in synapses of the ischemic hemisphere. Neurosci. Lett. 415, 77 80.
47. McCarthy K. D. de Vellis J. (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85, 890 902.
48. McCollum A. K., TenEyck C. J., Sauer B. M., Toft D. O. Erlichman C. (2006) Up-regulation of Heat Shock Protein 27 induces Resistance to 17-Allylamino-Demethoxygeldanamycin through a Glutathione-Mediated Mechanism. Cancer Res. 66, 10967 10975.
49. Ness J. K., Scaduto Jr. R. C. Wood T. L. (2004) IGF-I prevents glutamate-mediated bax translocation and cytochrome C release in O4 + oligodendrocyte progenitors. Glia 46, 183 194.
50. Nimmanapalli R., O'Bryan E., Kuhn D., Yamaguchi H., Wang H. G. Bhalla K. N. (2003) Regulation of 17-AAG-induced apoptosis: role of Bcl-2, Bcl-XL, and Bax downstream of 17-AAG-mediated down-regulation of Akt, Raf-1, and Src kinases. Blood 102, 269 275.
51. Ouyang Y. B., Xu L. Giffard R. G. (2005) Geldanamycin treatment reduces delayed CA1 damage in mouse hippocampal organotypic cultures subjected to oxygen glucose deprivation. Neurosci. Lett. 380, 229 233.
52. Pandey P., Saleh A., Nakazawa A. et al. (2000) Negative regulation of cytochrome c-mediated oligomerization of Apaf-1 and activation of procaspase-9 by heat shock protein 90. EMBO J. 19, 4310 4322.
53. Premkumar D. R., Arnold B., Jane E. P. Pollack I. F. (2006) Synergistic interaction between 17-AAG and phosphatidylinositol 3-kinase inhibition in human malignant glioma cells. Mol. Carcinog. 45, 47 59.
54. Rahmani M., Yu C., Dai Y., Reese E., Ahmed W., Dent P. Grant S. (2003) Coadministration of the heat shock protein 90 antagonist 17-allylamino- 17-demethoxygeldanamycin with suberoylanilide hydroxamic acid or sodium butyrate synergistically induces apoptosis in human leukemia cells. Cancer Res. 63, 8420 8427.
55. Rezaie P. Dean A. (2002) Periventricular leukomalacia, inflammation and white matter lesions within the developing nervous system. Neuropathology 22, 106 132.
56. Richter-Landsberg C. Goldbaum O. (2003) Stress proteins in neural cells: functional roles in health and disease. Cell Mol Life Sci. 60, 337 349.
57. Richter-Landsberg C. Vollgraf U. (1998) Mode of cell injury and death after hydrogen peroxide exposure in cultured oligodendroglia cells. Exp. Cell Res. 244, 218 229.
58. Schulte T. W. Neckers L. M. (1998) The benzoquinone ansamycin 17-allylamino-17-demethoxygeldanamycin binds to HSP90 and shares important biologic activities with geldanamycin. Cancer Chemother. Pharmacol. 42, 273 279.
59. Shen H. Y., He J. C., Wang Y., Huang Q. Y. Chen J. F. (2005) Geldanamycin induces heat shock protein 70 and protects against MPTP-induced dopaminergic neurotoxicity in mice. J. Biol. Chem. 280, 39962 39969.
60. Sittler A., Lurz R., Lueder G., Priller J., Lehrach H., Hayer-Hartl M. K., Hartl F. U. Wanker E. E. (2001) Geldanamycin activates a heat shock response and inhibits huntingtin aggregation in a cell culture model of Huntington's disease. Hum. Mol. Genet. 10, 1307 1315.
61. Sun Y. MacRae T. H. (2005) Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci. 62, 2460 2476.
62. Sykova E. Chvatal A. (2000) Glial cells and volume transmission in the CNS. Neurochem. Int. 36, 397 409.
63. Terasawa K., Minami M. Minami Y. (2005) Constantly updated knowledge of Hsp90. J. Biochem. 137, 443 447.
64. Thorburne S. K. Juurlink B. H. (1996) Low glutathione and high iron govern the susceptibility of oligodendroglial precursors to oxidative stress. J. Neurochem. 67, 1014 1022.
65. Volpe J. J. (2001) Neurobiology of periventricular leukomalacia in the premature infant. Pediatr. Res. 50, 553 562.
66. Wang X., Venable J., LaPointe P. et al. (2006) Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis. Cell 127, 803 815.
67. Ye P., Kollias G. D'Ercole A. J. (2007) Insulin-like growth factor-I ameliorates demyelination induced by tumor necrosis factor-alpha in transgenic mice. J. Neurosci. Res. 85, 712 722.
68. Yenari M. A., Liu J., Zheng Z., Vexler Z. S., Lee J. E. Giffard R. G. (2005) Antiapoptotic and anti-inflammatory mechanisms of heat-shock protein protection. Ann. NY Acad. Sci. 1053, 74 83.
69. Yun B. Matts R. L. (2005) HSP90 functions to balance the phosphorylation state of Akt during C2C12 myoblast differentiation. Cell. Signal. 17, 1477 1485.
70. Zeger M., Popken G., Zhang J. et al. (2007) Insulin-like growth factor type 1 receptor signaling in the cells of oligodendrocyte lineage is required for normal in vivo oligodendrocyte development and myelination. Glia 55, 400 411.
71. Zhang R., Luo D., Miao R., Bai L., Ge Q., Sessa W. C. Min W. (2005) Hsp90-Akt phosphorylates ASK1 and inhibits ASK1-mediated apoptosis. Oncogene 24, 3954 3963.