Therapeutic inducers of the HSP70/HSP110 protect mice against traumatic brain injury

Journal of Neurochemistry

Volumn 130, Issue 5, 2014, Pages 626-641

  Eroglu, Binnur ^a,b,c   Kimbler, Donald E ^c   Pang, Junfeng ^b,c   Choi, Justin ^c   Moskophidis, Demetrius ^b,c   Yanasak, Nathan ^c   Dhandapani, Krishnan M ^c   Mivechi, Nahid F ^a,b,c,d  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b AUGUSTA UNIVERSITY   (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

^d Georgia Regents University ^*  (United States)

Author keywords

BGP 15; celastrol; closed cortical impact; Hsp110; Hsp70; knockout mice

Indexed keywords

CELASTROL; HEAT SHOCK PROTEIN 110; HEAT SHOCK PROTEIN 70; LEUKEMIA INHIBITORY FACTOR; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; O (2 HYDROXY 3 PIPERIDINOPROPYL)NICOTINIC AMIDOXIME; PROTEIN P53; REACTIVE OXYGEN METABOLITE; TAU PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BEAM BALANCE TEST; BRAIN PROTECTION; BRAIN WATER; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFICACY; EXPERIMENTAL TEST; FEAR CONDITIONG TEST; GENE; GENE EXPRESSION; GENE TARGETING; HISTOPATHOLOGY; MALE; MOUSE; NONHUMAN; PIG1 GENE; PIG12 GENE; PIG8 GENE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TRAUMATIC BRAIN INJURY; WILD TYPE;

MUS; SUIDAE;

BGP-15; CELASTROL; CLOSED CORTICAL IMPACT; HSP110; HSP70; KNOCKOUT MICE;

ANIMALS; BRAIN; BRAIN INJURIES; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HSP110 HEAT-SHOCK PROTEINS; HSP72 HEAT-SHOCK PROTEINS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPLEX POLYMERASE CHAIN REACTION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIMES; PIPERIDINES; REACTIVE OXYGEN SPECIES; TRITERPENES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84907778046     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12781     Document Type: Article

References (52)

1. Abbas H. A., Maccio D. R., Coskun S., Jackson J. G., Hazen A. L., Sills T. M., You M. J., Hirschi K. K., and, Lozano G., (2010) Mdm2 is required for survival of hematopoietic stem cells/progenitors via dampening of ROS-induced p53 activity. Cell Stem Cell 7, 606-617.
2. Beck I. M., Drebert Z. J., Hoya-Arias R., et al,. (2013) Compound A, a selective glucocorticoid receptor modulator, enhances heat shock protein Hsp70 gene promoter activation. PLoS ONE 8, e69115.
3. Beere H. M., Wolf B. B., Cain K., Mosser D. D., Mahboubi A., Kuwana T., Tailor P., Morimoto R. I., Cohen G. M., and, Green D. R., (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. Bonner H. P., Concannon C. G., Bonner C., Woods I., Ward M. W., and, Prehn J. H., (2010) Differential expression patterns of Puma and Hsp70 following proteasomal stress in the hippocampus are key determinants of neuronal vulnerability. J. Neurochem. 114, 606-616.
5. Buschmann J. P., Berger K., Awad H., Clarner T., Beyer C., and, Kipp M., (2012) Inflammatory response and chemokine expression in the white matter corpus callosum and gray matter cortex region during cuprizone-induced demyelination. J. Mol. Neurosci. 48, 66-76.
6. Chen A. J., and, D'Esposito M., (2010) Traumatic brain injury: from bench to bedside [corrected] to society. Neuron 66, 11-14.
7. Covey M. V., and, Levison S. W., (2007) Leukemia inhibitory factor participates in the expansion of neural stem/progenitors after perinatal hypoxia/ischemia. Neuroscience 148, 501-509.
8. Devesa J., Reimunde P., Devesa P., Barbera M., and, Arce V., (2013) Growth hormone (GH) and brain trauma. Horm. Behav. 63, 331-344.
9. Engel T., Gomez-Villafuertes R., Tanaka K., Mesuret G., Sanz-Rodriguez A., Garcia-Huerta P., Miras-Portugal M. T., Henshall D. C., and, Diaz-Hernandez M., (2012) Seizure suppression and neuroprotection by targeting the purinergic P2X7 receptor during status epilepticus in mice. FASEB J. 26, 1616-1628.
10. Eroglu B., Moskophidis D., and, Mivechi N. F., (2010) Loss of Hsp110 leads to age-dependent tau hyperphosphorylation and early accumulation of insoluble amyloid beta. Mol. Cell. Biol. 30, 4626-4643.
11. Gabai V. L., Mabuchi K., Mosser D. D., and, Sherman M. Y., (2002) Hsp72 and stress kinase c-jun N-terminal kinase regulate the bid-dependent pathway in tumor necrosis factor-induced apoptosis. Mol. Cell. Biol. 22, 3415-3424.
12. Garcia-Aragon J., Lobie P. E., Muscat G. E., Gobius K. S., Norstedt G., and, Waters M. J., (1992) Prenatal expression of the growth hormone (GH) receptor/binding protein in the rat: a role for GH in embryonic and fetal development? Development 114, 869-876.
13. Gehrig S. M., van der Poel C., Sayer T. A., et al,. (2012) Hsp72 preserves muscle function and slows progression of severe muscular dystrophy. Nature 484, 394-398.
14. Gentleman R. C., Carey V. J., Bates D. M., et al,. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80.
15. Gombos I., Crul T., Piotto S., et al,. (2011) Membrane-lipid therapy in operation: the HSP co-inducer BGP-15 activates stress signal transduction pathways by remodeling plasma membrane rafts. PLoS ONE 6, e28818.
16. Haldimann P., Muriset M., Vigh L., and, Goloubinoff P., (2011) The novel hydroxylamine derivative NG-094 suppresses polyglutamine protein toxicity in Caenorhabditis elegans. J. Biol. Chem. 286, 18784-18794.
17. Hartl F. U., Bracher A., and, Hayer-Hartl M., (2011) Molecular chaperones in protein folding and proteostasis. Nature 475, 324-332.
18. Homma S., Jin X., Wang G., Tu N., Min J., Yanasak N., and, Mivechi N. F., (2007) Demyelination, astrogliosis, and accumulation of ubiquitinated proteins, hallmarks of CNS disease in hsf1-deficient mice. J. Neurosci. 27, 7974-7986.
19. Huang L., Mivechi N. F., and, Moskophidis D., (2001) Insights into regulation and function of the major stress-induced hsp70 molecular chaperone in vivo: analysis of mice with targeted gene disruption of the hsp70.1 or hsp70.3 gene. Mol. Cell. Biol. 21, 8575-8591.
20. da Huang W., Sherman B. T., and, Lempicki R. A., (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.
21. Humphreys I., Wood R. L., Phillips C. J., and, Macey S., (2013) The costs of traumatic brain injury: a literature review. Clinicoecon. Outcomes Res. 5, 281-287.
22. Hunt C. R., Dix D. J., Sharma G. G., Pandita R. K., Gupta A., Funk M., and, Pandita T. K., (2004) Genomic instability and enhanced radiosensitivity in Hsp70.1- and Hsp70.3-deficient mice. Mol. Cell. Biol. 24, 899-911.
23. Januchowski R., Zawierucha P., Andrzejewska M., Rucinski M., and, Zabel M., (2013) Microarray-based detection and expression analysis of ABC and SLC transporters in drug-resistant ovarian cancer cell lines. Biomed. Pharmacother. 67, 240-245.
24. Johnson V. E., Stewart W., and, Smith D. H., (2010) Traumatic brain injury and amyloid-beta pathology: a link to Alzheimer's disease? Nat. Rev. Neurosci. 11, 361-370.
25. Kim J. Y., Kim N., Zheng Z., Lee J. E., and, Yenari M. A., (2013) The 70 kDa heat shock protein protects against experimental traumatic brain injury. Neurobiol. Dis. 58C, 289-295.
26. Kim M. G., Jung Cho E., Won Lee J., Sook Ko Y., Young Lee H., Jo S. K., Cho W. Y., and, Kim H. K., (2014) The heat-shock protein-70-induced renoprotective effect is partially mediated by CD4CD25Foxp3 regulatory T cells in ischemia/reperfusion-induced acute kidney injury. Kidney Int. 85, 62-71.
27. Kimbler D. E., Shields J., Yanasak N., Vender J. R., and, Dhandapani K. M., (2012) Activation of P2X7 promotes cerebral edema and neurological injury after traumatic brain injury in mice. PLoS ONE 7, e41229.
28. Kumar A., and, Loane D. J., (2012) Neuroinflammation after traumatic brain injury: opportunities for therapeutic intervention. Brain Behav. Immun. 26, 1191-1201.
29. Laird M. D., Sukumari-Ramesh S., Swift A. E., Meiler S. E., Vender J. R., and, Dhandapani K. M., (2010) Curcumin attenuates cerebral edema following traumatic brain injury in mice: a possible role for aquaporin-4? J. Neurochem. 113, 637-648.
30. Lee S. H., and, DeJong J., (1999) Microsomal GST-I: genomic organization, expression, and alternative splicing of the human gene. Biochim. Biophys. Acta 1446, 389-396.
31. Lee H., Kang J. E., Lee J. K., Bae J. S., and, Jin H. K., (2013) Bone-marrow-derived mesenchymal stem cells promote proliferation and neuronal differentiation of Niemann-Pick type C mouse neural stem cells by upregulation and secretion of CCL2. Hum. Gene Ther. 24, 655-669.
32. Lehar S. M., Nacht M., Jacks T., Vater C. A., Chittenden T., and, Guild B. C., (1996) Identification and cloning of EI24, a gene induced by p53 in etoposide-treated cells. Oncogene 12, 1181-1187.
33. Li Y., He D., Zhang X., Liu Z., Dong L., Xing Y., Wang C., Qiao H., Zhu C., and, Chen Y., (2012) Protective effect of celastrol in rat cerebral ischemia model: Down-regulating p-JNK, p-c-Jun and NF-kappaB". Brain Res. 1464, 8-13.
34. Literati-Nagy B., Kulcsar E., Literati-Nagy Z., et al,. (2009) Improvement of insulin sensitivity by a novel drug, BGP-15, in insulin-resistant patients: a proof of concept randomized double-blind clinical trial. Horm. Metab. Res. 41, 374-380.
35. Liu F. T., Hsu D. K., Zuberi R. I., Kuwabara I., Chi E. Y., and, Henderson W. R., Jr, (1995) Expression and function of galectin-3, a beta-galactoside-binding lectin, in human monocytes and macrophages. Am. J. Pathol. 147, 1016-1028.
36. Maas A. I., Roozenbeek B., and, Manley G. T., (2010) Clinical trials in traumatic brain injury: past experience and current developments. Neurotherapeutics 7, 115-126.
37. Napieralski J. A., Raghupathi R., and, McIntosh T. K., (1999) The tumor-suppressor gene, p53, is induced in injured brain regions following experimental traumatic brain injury. Brain Res. Mol. Brain Res. 71, 78-86.
38. Narayan N., Lee I. H., Borenstein R., et al,. (2012) The NAD-dependent deacetylase SIRT2 is required for programmed necrosis. Nature 492, 199-204.
39. Plesnila N., von Baumgarten L., Retiounskaia M., Engel D., Ardeshiri A., Zimmermann R., Hoffmann F., Landshamer S., Wagner E., and, Culmsee C., (2007) Delayed neuronal death after brain trauma involves p53-dependent inhibition of NF-kappaB transcriptional activity. Cell Death Differ. 14, 1529-1541.
40. Polier S., Dragovic Z., Hartl F. U., and, Bracher A., (2008) Structural basis for the cooperation of Hsp70 and Hsp110 chaperones in protein folding. Cell 133, 1068-1079.
41. Qi D., Liu H., Niu J., et al,. (2012) Heat shock protein 72 inhibits c-Jun N-terminal kinase 3 signaling pathway via Akt1 during cerebral ischemia. J. Neurol. Sci. 317, 123-129.
42. Rola R., Mizumatsu S., Otsuka S., Morhardt D. R., Noble-Haeusslein L. J., Fishman K., Potts M. B., and, Fike J. R., (2006) Alterations in hippocampal neurogenesis following traumatic brain injury in mice. Exp. Neurol. 202, 189-199.
43. 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.
44. Sivanandam T. M., and, Thakur M. K., (2012) Traumatic brain injury: a risk factor for Alzheimer's disease. Neurosci. Biobehav. Rev. 36, 1376-1381.
45. Szabados E., Literati-Nagy P., Farkas B., and, Sumegi B., (2000) BGP-15, a nicotinic amidoxime derivate protecting heart from ischemia reperfusion injury through modulation of poly(ADP-ribose) polymerase. Biochem. Pharmacol. 59, 937-945.
46. Trott A., West J. D., Klaic L., Westerheide S. D., Silverman R. B., Morimoto R. I., and, Morano K. A., (2008) Activation of heat shock and antioxidant responses by the natural product celastrol: transcriptional signatures of a thiol-targeted molecule. Mol. Biol. Cell 19, 1104-1112.
47. Tupper D. E., and, Wallace R. B., (1980) Utility of the neurological examination in rats. Acta Neurobiol. Exp. (Wars) 40, 999-1003.
48. Westerheide S. D., Bosman J. D., Mbadugha B. N., Kawahara T. L., Matsumoto G., Kim S., Gu W., Devlin J. P., Silverman R. B., and, Morimoto R. I., (2004) Celastrols as inducers of the heat shock response and cytoprotection. J. Biol. Chem. 279, 56053-56060.
49. Wilson C. A., and, Terry A. V., Jr, (2013) Variable maternal stress in rats alters locomotor activity, social behavior, and recognition memory in the adult offspring. Pharmacol. Biochem. Behav. 104, 47-61.
50. Woodcock T., and, Morganti-Kossmann M. C., (2013) The role of markers of inflammation in traumatic brain injury. Front. Neurol. 4, 18.
51. Xu L., Xiong X., Ouyang Y., Barreto G., and, Giffard R., (2011) Heat shock protein 72 (Hsp72) improves long term recovery after focal cerebral ischemia in mice. Neurosci. Lett. 488, 279-282.
52. Zhao Z., Faden A. I., Loane D. J., Lipinski M. M., Sabirzhanov B., and, Stoica B. A., (2013) Neuroprotective effects of geranylgeranylacetone in experimental traumatic brain injury. J. Cereb. Blood Flow Metab. 33, 1897-1908.