Low dose Hsp90 inhibitor 17AAG protects neural progenitor cells from ischemia induced death

Journal of Cell Communication and Signaling

Volumn 8, Issue 4, 2014, Pages 353-362

  Bradley, Eric ^a   Zhao, Xiaying ^a   Wang, Rebecca ^a   Brann, Darrell ^a   Bieberich, Erhard ^a   Wang, Guanghu ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

17AAG; Hormesis; Hsp90; Ischemia; Regenerative and reparative medicine; Stress adaptation; Stroke

Indexed keywords

17 N ALLYLAMINO 17 DEMETHOXYGELDANAMYCIN; GLUCOSE; HEAT SHOCK PROTEIN 90 INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE; OXYGEN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ASSAY; BRAIN; CELL DEATH; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; ISCHEMIA; LOW DRUG DOSE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NECROSIS; NEURAL STEM CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REGENERATIVE MEDICINE;

EID: 84921937831     PISSN: 18739601     EISSN: 1873961X     Source Type: Journal    
DOI: 10.1007/s12079-014-0247-5     Document Type: Article

References (73)

1. Aimone JB, Wiles J, Gage FH (2006) Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci 9(6):723–727
2. Allen DM, van Praag H, Ray J, Weaver Z, Winrow CJ, Carter TA, Braquet R, Harrington E, Ried T, Brown KD, Gage FH, Barlow C (2001) Ataxia telangiectasia mutated is essential during adult neurogenesis. Genes Dev 15(5):554–566
3. Ansar S, Burlison JA, Hadden MK, Yu XM, Desino KE, Bean J, Neckers L, Audus KL, Michaelis ML, Blagg BS (2007) A non-toxic Hsp90 inhibitor protects neurons from Abeta-induced toxicity. Bioorg Med Chem Lett 17(7):1984–1990
4. Banerjee S, Bentley P, Hamady M, Marley S, Davis J, Shlebak A, Nicholls J, Williamson DA, Jensen SL, Gordon M, Habib N, Chataway J (2014) Intra-Arterial Immunoselected CD34+ Stem Cells for Acute Ischemic Stroke. Stem Cells Transl Med.
5. Bhat RV, Budd Haeberlein SL, Avila J (2004) Glycogen synthase kinase 3: a drug target for CNS therapies. J Neurochem 89(6):1313–1317
6. Bieberich E, MacKinnon S, Silva J, Noggle S, Condie BG (2003) Regulation of cell death in mitotic neural progenitor cells by asymmetric distribution of prostate apoptosis response 4 (PAR-4) and simultaneous elevation of endogenous ceramide. J Cell Biol 162(3):469–479
7. Bieberich E, Silva J, Wang G, Krishnamurthy K, Condie BG (2004) Selective apoptosis of pluripotent mouse and human stem cells by novel ceramide analogues prevents teratoma formation and enriches for neural precursors in ES cell-derived neural transplants. J Cell Biol 167(4):723–734
8. Bliss TM, Kelly S, Shah AK, Foo WC, Kohli P, Stokes C, Sun GH, Ma M, Masel J, Kleppner SR, Schallert T, Palmer T, Steinberg GK (2006) Transplantation of hNT neurons into the ischemic cortex: cell survival and effect on sensorimotor behavior. J Neurosci Res 83(6):1004–1014
9. Bradley E, Bieberich E, Mivechi NF, Tangpisuthipongsa D, Wang G (2012) Regulation of embryonic stem cell pluripotency by heat shock protein 90. Stem Cells 30(8):1624–1633
10. Brazel CY, Nunez JL, Yang Z, Levison SW (2005) Glutamate enhances survival and proliferation of neural progenitors derived from the subventricular zone. Neuroscience 131(1):55–65
11. Calabrese EJ (2013a) Biphasic dose responses in biology, toxicology and medicine: accounting for their generalizability and quantitative features. Environ Pollut 182:452–460
12. Calabrese EJ (2013b) Hormetic mechanisms. Crit Rev Toxicol 43(7):580–606
13. Camphausen K, Tofilon PJ (2007) Inhibition of Hsp90: a multitarget approach to radiosensitization. Clin Cancer Res 13(15 Pt 1):4326–4330
14. Chang YC, Shyu WC, Lin SZ, Li H (2007) Regenerative therapy for stroke. Cell Transplant 16(2):171–181
15. Chen ZH, Lam HC, Jin Y, Kim HP, Cao J, Lee SJ, Ifedigbo E, Parameswaran H, Ryter SW, Choi AM (2010) Autophagy protein microtubule-associated protein 1 light chain-3B (LC3B) activates extrinsic apoptosis during cigarette smoke-induced emphysema. Proc Natl Acad Sci U S A 107(44):18880–18885
16. Chopp M, Zhang ZG, Jiang Q (2007) Neurogenesis, angiogenesis, and MRI indices of functional recovery from stroke. Stroke 38(2 Suppl):827–831
17. Croslan DR, Schoell MC, Ford GD, Pulliam JV, Gates A, Clement CM, Harris AE, Ford BD (2008) Neuroprotective effects of neuregulin-1 on B35 neuronal cells following ischemia. Brain Res 1210:39–47
18. Davalos A, Castillo J, Serena J, Noya M (1997) Duration of glutamate release after acute ischemic stroke. Stroke 28(4):708–710
19. Della-Morte D, Dave KR, DeFazio RA, Bao YC, Raval AP, Perez-Pinzon MA (2009) Resveratrol pretreatment protects rat brain from cerebral ischemic damage via a sirtuin 1-uncoupling protein 2 pathway. Neuroscience 159(3):993–1002
20. Dezwaan DC, Freeman BC (2008) HSP90: the Rosetta stone for cellular protein dynamics? Cell Cycle 7(8):1006–1012
21. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4(11):1313–1317
22. Frederix K, Chauhan AK, Kisucka J, Zhao BQ, Hoff EI, Spronk HM, Ten Cate H, Wagner DD (2007) Platelet adhesion receptors do not modulate infarct volume after a photochemically induced stroke in mice. Brain Res 1185:239–245
23. Gallo KA (2006) Targeting HSP90 to halt neurodegeneration. Chem Biol 13(2):115–116
24. Haas S, Weidner N, Winkler J (2005) Adult stem cell therapy in stroke. Curr Opin Neurol 18(1):59–64
25. Hahn CD, Manlhiot C, Schmidt MR, Nielsen TT, Redington AN (2011) Remote ischemic per-conditioning: a novel therapy for acute stroke? Stroke 42(10):2960–2962
26. Hess DC, Hoda MN, Bhatia K (2013) Remote limb perconditioning [corrected] and postconditioning: will it translate into a promising treatment for acute stroke? Stroke 44(4):1191–1197
27. Hicks AU, Lappalainen RS, Narkilahti S, Suuronen R, Corbett D, Sivenius J, Hovatta O, Jolkkonen J (2009) Transplantation of human embryonic stem cell-derived neural precursor cells and enriched environment after cortical stroke in rats: cell survival and functional recovery. Eur J Neurosci 29(3):562–574
28. Horie N, Pereira MP, Niizuma K, Sun G, Keren-Gill H, Encarnacion A, Shamloo M, Hamilton SA, Jiang K, Huhn S, Palmer TD, Bliss TM, Steinberg GK (2011) Transplanted stem cell-secreted vascular endothelial growth factor effects poststroke recovery, inflammation, and vascular repair. Stem Cells 29(2):274–285
29. Hougaard KD, Hjort N, Zeidler D, Sorensen L, Norgaard A, Thomsen RB, Jonsdottir K, Mouridsen K, Hansen TM, Cho TH, Nielsen TT, Botker HE, Ostergaard L, Andersen G (2013) Remote ischemic perconditioning in thrombolysed stroke patients: randomized study of activating endogenous neuroprotection - design and MRI measurements. Int J Stroke 8(2):141–146
30. Jarosz DF, Lindquist S (2010) Hsp90 and environmental stress transform the adaptive value of natural genetic variation. Science 330(6012):1820–1824
31. Jin K, Wang X, Xie L, Mao XO, Zhu W, Wang Y, Shen J, Mao Y, Banwait S, Greenberg DA (2006) Evidence for stroke-induced neurogenesis in the human brain. Proc Natl Acad Sci U S A 103(35):13198–13202
32. Kaushal V, Schlichter LC (2008) Mechanisms of microglia-mediated neurotoxicity in a new model of the stroke penumbra. J Neurosci 28(9):2221–2230
33. Kelly S, Bliss TM, Shah AK, Sun GH, Ma M, Foo WC, Masel J, Yenari MA, Weissman IL, Uchida N, Palmer T, Steinberg GK (2004) Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc Natl Acad Sci U S A 101(32):11839–11844
34. Koch S, Katsnelson M, Dong C, Perez-Pinzon M (2011) Remote ischemic limb preconditioning after subarachnoid hemorrhage: a phase Ib study of safety and feasibility. Stroke 42(5):1387–1391
35. Koga F, Xu W, Karpova TS, McNally JG, Baron R, Neckers L (2006) Hsp90 inhibition transiently activates Src kinase and promotes Src-dependent Akt and Erk activation. Proc Natl Acad Sci U S A 103(30):11318–11322
36. Kostandy BB (2012) The role of glutamate in neuronal ischemic injury: the role of spark in fire. Neurol Sci 33(2):223–237
37. Kwon HM, Kim Y, Yang SI, Kim YJ, Lee SH, Yoon BW (2008) Geldanamycin protects rat brain through overexpression of HSP70 and reducing brain edema after cerebral focal ischemia. Neurol Res 30(7):740–745
38. Lee HJ, Kim KS, Kim EJ, Choi HB, Lee KH, Park IH, Ko Y, Jeong SW, Kim SU (2007) Brain transplantation of immortalized human neural stem cells promotes functional recovery in mouse intracerebral hemorrhage stroke model. Stem Cells 25(5):1204–1212
39. Lee JJ, Li L, Jung HH, Zuo Z (2008) Postconditioning with isoflurane reduced ischemia-induced brain injury in rats. Anesthesiology 108(6):1055–1062
40. Li J, Zeng Z, Viollet B, Ronnett GV, McCullough LD (2007) Neuroprotective effects of adenosine monophosphate-activated protein kinase inhibition and gene deletion in stroke. Stroke 38(11):2992–2999
41. Majid A (2014) Neuroprotection in stroke: past, present, and future. ISRN Neurol 2014:515716
42. Marini AM, Jiang H, Pan H, Wu X, Lipsky RH (2008) Hormesis: a promising strategy to sustain endogenous neuronal survival pathways against neurodegenerative disorders. Ageing Res Rev 7(1):21–33
43. Mitrecic D, Nicaise C, Klimaschewski L, Gajovic S, Bohl D, Pochet R (2012) Genetically modified stem cells for the treatment of neurological diseases. Front Biosci (Elite Ed) 4:1170–1181
44. Mitsios N, Gaffney J, Kumar P, Krupinski J, Kumar S, Slevin M (2006) Pathophysiology of acute ischaemic stroke: an analysis of common signalling mechanisms and identification of new molecular targets. Pathobiology 73(4):159–175
45. Moretti A, Ferrari F, Villa RF (2014) Neuroprotection for ischaemic stroke: Current status and challenges. Pharmacol Ther.
46. Nagy D, Kocsis K, Fuzik J, Marosi M, Kis Z, Teichberg VI, Toldi J, Farkas T (2011) Kainate postconditioning restores LTP in ischemic hippocampal CA1: onset-dependent second pathophysiological stress. Neuropharmacology 61(5–6):1026–1032
47. Norgaard R, Kassem M, Rattan SI (2006) Heat shock-induced enhancement of osteoblastic differentiation of hTERT-immortalized mesenchymal stem cells. Ann N Y Acad Sci 1067:443–447
48. Ohira K, Furuta T, Hioki H, Nakamura KC, Kuramoto E, Tanaka Y, Funatsu N, Shimizu K, Oishi T, Hayashi M, Miyakawa T, Kaneko T, Nakamura S (2009) Ischemia-induced neurogenesis of neocortical layer 1 progenitor cells. Nat Neurosci.
49. Pradeep H, Diya JB, Shashikumar S, Rajanikant GK (2012) Oxidative stress–assassin behind the ischemic stroke. Folia Neuropathol 50(3):219–230
50. Ratan RR, Siddiq A, Smirnova N, Karpisheva K, Haskew-Layton R, McConoughey S, Langley B, Estevez A, Huerta PT, Volpe B, Roy S, Sen CK, Gazaryan I, Cho S, Fink M, LaManna J (2007) Harnessing hypoxic adaptation to prevent, treat, and repair stroke. J Mol Med 85(12):1331–1338
51. Raval AP, Bramlett H, Perez-Pinzon MA (2006) Estrogen preconditioning protects the hippocampal CA1 against ischemia. Neuroscience 141(4):1721–1730
52. Roitberg BZ, Mangubat E, Chen EY, Sugaya K, Thulborn KR, Kordower JH, Pawar A, Konecny T, Emborg ME (2006) Survival and early differentiation of human neural stem cells transplanted in a nonhuman primate model of stroke. J Neurosurg 105(1):96–102
53. Rosova I, Dao M, Capoccia B, Link D, Nolta JA (2008) Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells 26(8):2173–2182
54. Sawe N, Steinberg G, Zhao H (2008) Dual roles of the MAPK/ERK1/2 cell signaling pathway after stroke. J Neurosci Res 86(8):1659–1669
55. Shaller CA, Jacques S, Shelden CH (1980) The pathophysiology of stroke: a review with molecular considerations. Surg Neurol 14(6):433–443
56. Steindler DA (2007) Stem cells, regenerative medicine, and animal models of disease. Ilar J 48(4):323–338
57. Terasawa K, Minami M, Minami Y (2005) Constantly updated knowledge of Hsp90. J Biochem (Tokyo) 137(4):443–447
58. Theus MH, Wei L, Cui L, Francis K, Hu X, Keogh C, Yu SP (2008) In vitro hypoxic preconditioning of embryonic stem cells as a strategy of promoting cell survival and functional benefits after transplantation into the ischemic rat brain. Exp Neurol 210(2):656–670
59. Wang G, Krishnamurthy K, Tangpisuthipongsa D (2011) Protection of murine neural progenitor cells by the Hsp90 inhibitor 17-allylamino-17-demethoxygeldanamycin in the low nanomolar concentration range. J Neurochem 117(4):703–711
60. Wang G, Silva J, Krishnamurthy K, Tran E, Condie BG, Bieberich E (2005) Direct binding to ceramide activates protein kinase Czeta before the formation of a pro-apoptotic complex with PAR-4 in differentiating stem cells. J Biol Chem 280(28):26415–26424
61. Wang X, Zhao T, Huang W, Wang T, Qian J, Xu M, Kranias EG, Wang Y, Fan GC (2009) Hsp20-engineered mesenchymal stem cells are resistant to oxidative stress via enhanced activation of Akt and increased secretion of growth factors. Stem Cells 27(12):3021–3031
62. Waza M, Adachi H, Katsuno M, Minamiyama M, Tanaka F, Doyu M, Sobue G (2006) Modulation of Hsp90 function in neurodegenerative disorders: a molecular-targeted therapy against disease-causing protein. J Mol Med 84(8):635–646
63. Wei L, Cui L, Snider BJ, Rivkin M, Yu SS, Lee CS, Adams LD, Gottlieb DI, Johnson EM Jr, Yu SP, Choi DW (2005) Transplantation of embryonic stem cells overexpressing Bcl-2 promotes functional recovery after transient cerebral ischemia. Neurobiol Dis 19(1–2):183–193
64. Wei S, Sun J, Li J, Wang L, Hall CL, Dix TA, Mohamad O, Wei L, Yu SP (2013) Acute and delayed protective effects of pharmacologically induced hypothermia in an intracerebral hemorrhage stroke model of mice. Neuroscience 252:489–500
65. Wen XR, Li C, Zong YY, Yu CZ, Xu J, Han D, Zhang GY (2008) Dual inhibitory roles of geldanamycin on the c-Jun NH2-terminal kinase 3 signal pathway through suppressing the expression of mixed-lineage kinase 3 and attenuating the activation of apoptosis signal-regulating kinase 1 via facilitating the activation of Akt in ischemic brain injury. Neuroscience 156(3):483–497
66. Wheeler DS, Wong HR (2007) Heat shock response and acute lung injury. Free Radic Biol Med 42(1):1–14
67. Wu X, Qian Z, Ke Y, Du F, Zhu L (2009) Ginkgolide B preconditioning protects neurons against ischaemia-induced apoptosis. J Cell Mol Med 13(11–12):4474–4483
68. Xie R, Wang P, Ji X, Zhao H (2013) Ischemic post-conditioning facilitates brain recovery after stroke by promoting Akt/mTOR activity in nude rats. J Neurochem 127(5):723–732
69. Yano A, Tsutsumi S, Soga S, Lee MJ, Trepel J, Osada H, Neckers L (2008) Inhibition of Hsp90 activates osteoclast c-Src signaling and promotes growth of prostate carcinoma cells in bone. Proc Natl Acad Sci U S A 105(40):15541–15546
70. Yu SP, Wei Z, Wei L (2013) Preconditioning strategy in stem cell transplantation therapy. Transl Stroke Res 4(1):76–88
71. Yuan J (2009) Neuroprotective strategies targeting apoptotic and necrotic cell death for stroke. Apoptosis 14(4):469–477
72. Zhang H, Burrows F (2004) Targeting multiple signal transduction pathways through inhibition of Hsp90. J Mol Med 82(8):488–499
73. Zhao H, Sapolsky RM, Steinberg GK (2006) Phosphoinositide-3-kinase/akt survival signal pathways are implicated in neuronal survival after stroke. Mol Neurobiol 34(3):249–270