Neurotherapeutic activity of the recombinant heat shock protein Hsp70 in a model of focal cerebral ischemia in rats

Drug Design, Development and Therapy

Volumn 8, Issue , 2014, Pages 639-650

  Shevtsov, Maxim A ^a,b   Nikolaev, Boris P ^c   Yakovleva, Ludmila Y ^c   Dobrodumov, Anatolii V ^d   Dayneko, Anastasiy S ^e   Shmonin, Alexey A ^b,e   Vlasov, Timur D ^e   Melnikova, Elena V ^e   Vilisov, Alexander D ^d,e   Guzhova, Irina V ^a   Ischenko, Alexander M ^c   Mikhrina, Anastasiya L ^f   Galibin, Oleg V ^e   Yakovenko, Igor V ^b   Margulis, Boris A ^a  

^a INSTITUTE OF CYTOLOGY   (Russian Federation)

^b ALMAZOV NATIONAL MEDICAL RESEARCH CENTRE   (Russian Federation)

^c Institute for Highly Pure Biopreparations   (Russian Federation)

^d INSTITUTE OF MACROMOLECULAR COMPOUNDS   (Russian Federation)

^e PAVLOV FIRST SAINT PETERSBURG STATE MEDICAL UNIVERSITY   (Russian Federation)

^f SECHENOV INSTITUTE OF EVOLUTIONARY PHYSIOLOGY AND BIOCHEMISTRY   (Russian Federation)

Author keywords

Alginate granules; Focal ischemia; Neuroprotection; Neurotherapy; Stroke

Indexed keywords

ALGINIC ACID; HEAT SHOCK PROTEIN 70; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL PROTECTION; CONTROLLED STUDY; DRUG MECHANISM; DRUG RELEASE; DRUG RESPONSE; MALE; NEUROPROTECTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OPTIMAL DRUG DOSE; RAT; ANIMAL; DISEASE MODEL; INTRAVENOUS DRUG ADMINISTRATION; WISTAR RAT;

ADMINISTRATION, INTRAVENOUS; ANIMALS; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; HSP70 HEAT-SHOCK PROTEINS; MALE; RATS; RATS, WISTAR; RECOMBINANT PROTEINS;

EID: 84901673446     PISSN: 11778881     EISSN: None     Source Type: Journal    
DOI: 10.2147/DDDT.S62024     Document Type: Article

References (52)

1. Sharp FR, Zhan X, Liu DZ. Heat shock proteins in the brain: role of Hsp70, Hsp27, and HO-1 (Hsp32) and their therapeutic potential. Transl Stroke Res. 2013;4:685-692.
2. Fink SL, Chang LK, Ho DY, Sapolsky RM. Defective herpes simplex virus vectors expressing the rat brain stress-inducible heat shock protein 72 protect cultured neurons from severe heat shock. J Neurochem. 1997;68:961-969.
3. Rajdev S, Hara K, Kokubo Y, et al. Mice overexpressing rat heat shock protein 70 are protected against cerebral infarction. Ann Neurol. 2000;47:782-791.
4. Lu A, Ran R, Parmentier-Batteur S, Nee A, Sharp FR. Geldanamycin induces heat shock proteins in brain and protects against focal cerebral ischemia. J Neurochem. 2002;81(2):355-364.
5. Guzhova I, Kislyakova K, Moskaliova O, et al. In vitro studies show that Hsp70 can be released by glia and that exogenous Hsp70 can enhance neuronal stress tolerance. Brain Res. 2001;914:66-73.
6. Ekimova IV, Nitsinskaya LE, Romanova IV, Pastukhov YF, Margulis BA, Guzhova IV. Exogenous protein Hsp70/Hsc70 can penetrate into brain structures and attenuate the severity of chemically-induced seizures. J Neurochem. 2010;115:1035-1044.
7. Guzhova IV, Lazarev VF, Kaznacheeva AV, et al. Novel mechanism of Hsp70 chaperone-mediated prevention of polyglutamine aggregates in a cellular model of Huntington disease. Hum Mol Genet. 2011;20: 3953-3963.
8. Soriano MA, Ferrer I, Rodríguez-Farré E, Planas AM. Expression of c-fos and inducible hsp-70 mRNA following a transient episode of focal ischemia that had non-lethal effects on the rat brain. Brain Res. 1995;670:317-320.
9. Zhan X, Kim C, Sharp FR. Very brief focal ischemia simulating transient ischemic attacks (TIAs) can injure brain and induce Hsp70 protein. Brain Res. 2008;1234:183-197.
10. Sharp FR, Lu A, Tang Y, Millhorn DE. Multiple molecular penumbras after focal cerebral ischemia. J Cereb Blood Flow Metab. 2000;20: 1011-1032.
11. Nishi S, Taki W, Uemura Y, et al. Ischemic tolerance due to the induction of HSP70 in a rat ischemic recirculation model. Brain Res. 1993;615:281-288.
12. Nishino K, Nowak TS Jr. Time course and cellular distribution of hsp27 and hsp72 stress protein expression in a quantitative gerbil model of ischemic injury and tolerance: thresholds for hsp72 induction and hilar lesioning in the context of ischemic preconditioning. J Cereb Blood Flow Metab. 2004;24:167-178.
13. Currie RW, Ellison JA, White RF, Feuerstein GZ, Wang X, Barone FC. Benign focal ischemic preconditioning induces neuronal Hsp70 and prolonged astrogliosis with expression of Hsp27. Brain Res. 2000;863:169-181.
14. Liu Y, Kato H, Nakata N, Kogure K. Temporal profile of heat shock protein 70 synthesis in ischemic tolerance induced by preconditioning ischemia in rat hippocampus. Neuroscience. 1993;56:921-927.
15. Zhan X, Ander BP, Liao IH, et al. Recombinant Fv-Hsp70 protein mediates neuroprotection after focal cerebral ischemia in rats. Stroke. 2010;41:538-543.
16. Dai J, Chen L, Qiu YM, et al. Activations of GABAergic signaling, HSP70 and MAPK cascades are involved in baicalin's neuroprotection against gerbil global ischemia/reperfusion injury. Brain Res Bull. 2013;90:1-9.
17. Guo JF, Jourdian GW, MacCallum DK. Culture and growth characteristics of chondrocytes encapsulated in alginate beads. Connect Tissue Res. 1989;19:277-297.
18. Koizumi J, Yoshida Y, Nakazawa T, Ooneda G. Experimental studies of ischemic brain edema. I. A new experimental model of cerebral embolism in which recirculation can introduced into the ischemic area. Jpn J Stroke. 1986;8:1-8.
19. Longa EZ, Weinstein PR, Carlson S, Cummins R. Reversible muddle cerebral artery occlusion without craniectomy in rats. Stroke. 1989;20:84-91.
20. Belayev L, Alonso OF, Busto R, Zhao W, Ginsberg MD. Middle cerebral artery occlusion in the rat by intraluminal suture. Neurological and pathological evaluation of an improved model. Stroke. 1996;27: 1616-1622.
21. Shmonin A, Melnikova E, Galagudza M, Vlasov T. Characteristics of cerebral ischemia in major rat stroke models of middle cerebral artery ligation through craniectomy. Int J Stroke. Epub December 4, 2012.
22. Bivard A, Lin L, Parsonsb MW. Review of stroke thrombolytics. J Stroke. 2013;15:90-98.
23. Khatri R, McKinney AM, Swenson B, Janardhan V. Blood-brain barrier, reperfusion injury, and hemorrhagic transformation in acute ischemic stroke. Neurology. 2012;79(13 Suppl 1):S52-S57.
24. Shevtsov MA, Yakovleva LY, Nikolaev BP, et al. Tumor targeting using magnetic nanoparticle Hsp70 conjugate in a model of C6 glioma. Neuro Oncol. 2014;16:38-49.
25. Asea A, Kraeft SK, Kurt-Jones EA, et al. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med. 2000;6:435-442.
26. Peraçoli JC, Bannwart-Castro CF, Romao M, et al. High levels of heat shock protein 70 are associated with pro-inflammatory cytokines and may differentiate early-from late-onset preeclampsia. J Reprod Immunol. 2013;100:129-134.
27. Lambertsen KL, Biber K, Finsen B. Inflammatory cytokines in experimental and human stroke. J Cereb Blood Flow Metab. 2012;32: 1677-1698.
28. Karikó K, Weissman D, Welsh FA. Inhibition of toll-like receptor and cytokine signaling-a unifying theme in ischemic tolerance. J Cereb Blood Flow Metab. 2004;24:1288-1304.
29. Borges TJ, Wieten L, van Herwijnen MJ, et al. The anti-inflammatory mechanisms of Hsp70. Front Immunol. 2012;3:95.
30. Planas AM, Solé S, Justicia C. Expression and activation of matrix metalloproteinase-2 and-9 in rat brain after transient focal cerebral ischemia. Neurobiol Dis. 2001;8:834-846.
31. Rosell A, Ortega-Aznar A, Alvarez-Sabín J, et al. Increased brain expression of matrix metalloproteinase-9 after ischemic and hemorrhagic human stroke. Stroke. 2006;37:1399-1406.
32. Lee JE, Kim YJ, Kim JY, Lee WT, Yenari MA, Giffard RG. The 70 kDa heat shock protein suppresses matrix metalloproteinases in astrocytes. Neuroreport. 2004;15:499502.
33. Barber PA. Magnetic resonance imaging of ischemia viability thresholds and the neurovascular unit. Sensors (Basel). 2013;13: 6981-7003.
34. Macintosh BJ, Graham SJ. Magnetic resonance imaging to visualize stroke and characterize stroke recovery: a review. Front Neurol. 2013;4:60.
35. Luginbuehl V, Wenk E, Koch A, Gander B, Merkle HP, Meinel L. Insulin-like growth factor I-releasing alginate-tricalciumphosphate composites for bone regeneration. Pharm Res. 2005;22:940-950.
36. Abkin SV, Pankratova KM, Komarova EY, Guzhova IV, Margulis BA. Hsp70 chaperone-based gel composition as a novel immunotherapeutic anti-tumor tool. Cell Stress Chaperones. 2013;18:391-396.
37. Saibil H. Chaperone machines for protein folding, unfolding and disaggregation. Nat Rev Mol Cell Biol. 2013;14:630-642.
38. Kim YE, Hipp MS, Bracher A, Hayer-Hartl M, Hartl FU. Molecular chaperone functions in protein folding and proteostasis. Annu Rev Biochem. 2013;82:323-355.
39. Sharma SK, Christen P, Goloubinoff P. Disaggregating chaperones: an unfolding story. Curr Protein Pept Sci. 2009;10:432-446.
40. del Zoppo GJ, Sharp FR, Heiss WD, Albers GW. Heterogeneity in the penumbra. J Cereb Blood Flow Metab. 2011;31:1836-1851.
41. Saleh A, Srinivasula SM, Balkir L, Robbins PD, Alnemri ES. Negative regulation of the Apaf-1 apoptosome by Hsp 70. Nat Cell Biol. 2000;2: 476-483.
42. Stankiewicz AR, Lachapelle G, Foo CP, Radicioni SM, Mosser DD. Hsp70 inhibits heat-induced apoptosis upstream of mitochondria by preventing Bax translocation. J Biol Chem. 2005;280:38729-38739.
43. Ravagnan L, Gurbuxani S, Susin SA, et al. Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat Cell Biol. 2001;3:839-843.
44. Gabai VL, Meriin AB, Yaglom JA, Wei JY, Mosser DD, Sherman MY. Suppression of stress kinase JNK is involved in HSP72-mediated protection of myogenic cells from transient energy deprivation. HSP72 alleviates the stress-induced inhibition of JNK dephosphorylation. J Biol Chem. 2000;275:38088-38094.
45. Franklin TB, Krueger-Naug AM, Clarke DB, Arrigo AP, Currie RW. The role of heat shock proteins Hsp70 and Hsp27 in cellular protection of the central nervous system. Int J Hyperthermia. 2005;21(5): 379-392.
46. Latchman DS. HSP27 and cell survival in neurones. Int J Hyperthermia. 2005;21(5):393-402.
47. van der Weerd L, Tariq Akbar M, Aron Badin R, et al. Overexpression of heat shock protein 27 reduces cortical damage after cerebral ischemia. J Cereb Blood Flow Metab. 2010;30(4):849-856.
48. Teramoto S, Shimura H, Tanaka R, et al. Human-derived physiological heat shock protein 27 complex protects brain after focal cerebral ischemia in mice. PLoS One. 2013;8(6):e66001.
49. Hwang IK, Ahn HC, Yoo KY, et al. Changes in immunoreactivity of HSP60 and its neuroprotective effects in the gerbil hippocampal CA1 region induced by transient ischemia. Exp Neurol. 2007;208(2): 247-256.
50. Greenhalgh AD, Galea J, Dénes A, Tyrrell PJ, Rothwell NJ. Rapid brain penetration of interleukin-1 receptor antagonist in rat cerebral ischaemia: pharmacokinetics, distribution, protection. Br J Pharmacol. 2010;160:153-159.
51. Emsley HC, Smith CJ, Georgiou RF, et al; Acute Stroke Investigators. A randomised phase II study of interleukin-1 receptor antagonist in acute stroke patients. J Neurol Neurosurg Psychiatry. 2005;76: 1366-1372.
52. Singh N, Hopkins SJ, Hulme S, et al. The effect of intravenous interleukin-1 receptor antagonist on inflammatory mediators in cerebrospinal fluid after subarachnoid haemorrhage: a phase II randomised controlled trial. J Neuroinflammation. 2014;11:1.