Putative endogenous mediators of preconditioning-induced ischemic tolerance in rat brain identified by genomic and proteomic analysis

Journal of Neurochemistry

Volumn 89, Issue 1, 2004, Pages 73-89

  Dhodda, Vinay K ^a   Sailor, Kurt A ^a   Bowen, Kellie K ^a   Vemuganti, Raghu ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b University of Wisconsin Cardiovascular Research Center   (United States)

Author keywords

GeneChip; Ischemic tolerance; Microarray; Neuroprotection; Proteomics; Stroke

Indexed keywords

BETA ACTIN; GUANYLATE CYCLASE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HEME OXYGENASE; ION CHANNEL; METALLOTHIONEIN; MUSKELIN; PROTEIN; THROMBOCYTE ACTIVATING FACTOR RECEPTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN INFARCTION SIZE; BRAIN INJURY; BRAIN ISCHEMIA; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; DNA MICROARRAY; GEL ELECTROPHORESIS; GENOMICS; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTEOMICS; PYRAMIDAL NERVE CELL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 1842614423     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02316.x     Document Type: Article

References (67)

1. Baines C. P., Liu G. S., Birincioglu M., Critz S. D., Cohen M. V. and Downey J. M. (1999) Ischemic preconditioning depends on interaction between mitochondrial KATP channels and actin cytoskeleton. Am. J. Physiol. 276, HI361-HI368.
2. Bergeron M., Gidday J. M. Yu A. Y., Semenza G. L., Ferriero D. M. and Sharp F. R. (2000) Role of hypoxia-inducible factor-1 in hypoxia-induced ischemic tolerance in neonatal rat brain. Ann. Neurol. 48, 285-296.
3. Bemaudin M., Bellail A., Marti H. H., Yvon A., Vivien D., Duchatelle I., Mackenzie E. T. and Petit E. (2000) Neurons and astrocytes express EPO mRNA: oxygen-sensing mechanisms that involve the redox-state of the brain. Glia 30, 271-278.
4. Bemaudin M., Nedelec A. S., Divoux D., MacKenzie E. T., Petit E. and Schumann-Bard P. (2002) Normobaric hypoxia induces tolerance to focal permanent cerebral ischemia in association with an increased expression of hypoxia-inducible factor-1 and its target genes, erythropoietin and VEGF, in the adult mouse brain. J. Cereb. Blood Flow Metab. 22, 393-403.
5. Boguski M. S. and McIntosh M. W. (2003) Biomedical informatics for proteomics. Nature 422, 233-237.
6. Cao Y. J., Shibata T. and Rainov N. G. (2002) Liposome-mediated transfer of the bcl-2 gene results in neuroprotection after in vivo transient focal cerebral ischemia in an animal model. Gene Ther. 9, 415-419.
7. Currie R. W., Ellision J. A., White R. F., Feuerstein G. Z., Wang X. and Barone F. C. (2000) Benign focal ischemic preconditioning induces neuronal Hsp70 and prolonged astrogliosis with expression of Hsp27. Brain Res. 863, 169-181.
8. Dogan A., Rao A. M., Hatcher J., Rao V. L., Baskaya M. K. and Dempsey R. J. (1999) Effects of MDL 72527, a specific inhibitor of polyamine oxidase, on brain edema, ischemic injury volume, and tissue polyamine levels in rats after temporary middle cerebral artery occlusion. J. Neurochem. 72, 765-770.
9. Dore S., Sampei K., Goto S., Alkayed N. J., Guastella D., Blackshaw S., Gallagher M., Traystman R. J., Hurn P. D., Koehler R. C. et al. (1999) Heme oxygenase-2 is neuroprotective in cerebral ischemia. Mol. Med. 5, 656-663.
10. Edwards R. J., Saurin A. T., Rakhit R. D. and Marber M. S. (2000) Therapeutic potential of ischaemic preconditioning. Br. J. Clin. Pharmacol. 50, 87-97.
11. Ferris C. D., Jaffrey S. R., Sawa A. et al. (1999) Heme oxygenase-1 prevents cell death by regulating cellular iron. Nat. Cell Biol. 1, 152-157.
12. Garrido C., Bruey J. M., Fromentin A., Hammann A., Arrigo A. P. and Solary E. (1999) HSP27 inhibits cytochrome c-dependent activation of procaspase-9. FASEB J. 13, 2061-2070.
13. Gharahdaghi F., Weinberg C. R., Meagher D. A., Imai B. S. and Mische S. M. (1999) Mass spectrometric identification of proteins from silver-stained polyacrylamide gel: a method for the removal of silver ions to enhance sensitivity. Electrophoresis 20, 601-605.
14. Gonzalez-Zulueta M., Feldman A. B., Klesse L. J., Kalb R. G., Dillman J. F., Parada L. F., Dawson T. M. and Dawson V. L. (2000) Requirement for nitric oxide activation of p21(ras)/extracellular regulated kinase in neuronal ischemic preconditioning. Proc. Natl Acad. Sci. USA 97, 436-441.
15. Gozal E., Gozal D., Pierce W. M., Thongboonkerd V., Scherzer J. A., Sachleben L. R. Jr, Brittian K. R., Guo S. Z., Cai J. and Klein J. B. (2002) Proteomic analysis of CA1 and CA3 regions of rat hippocampus and differential susceptibility to intermittent hypoxia. J. Neurochem. 83, 331-345.
16. Guay J., Lambert H., Gingras-Breton G., Lavoie J. N., Huot J. and Landry J. (1997) Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27. J. Cell Sci. 110, 357-368.
17. Hayashi H., Abdollah S., Qiu Y., Cai J., Xu Y. Y., Grinnell B. W., Richardson M. A., Topper J. N., Gimbrone M. A. Jr, Wrana J. L. et al. (1997) The MAD-related protein Smad7 associates with the TGF-β receptor and functions as an antagonist of TGF-β signaling. Cell 89, 1165-1173.
18. + channels in cerebral ischemic preconditioning. Proc. Natl Acad. Sci. USA 92, 4666-4670.
19. Horiguchi T., Kis B., Rajapakse N., Shimizu K. and Busija D. W. (2003) Opening of mitochondrial ATP-sensitive potassium channels is a trigger of 3-nitropropionic acid-induced tolerance to transient focal cerebral ischemia in rats. Stroke 34, 1015-1020.
20. Ideker T., Thorsson V., Ranish J. A., Christmas R., Buhler J., Eng J. K., Bumgamer R., Goodlett D. R., Aebersold R. and Hood L. (2001) Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 292, 929-934.
21. Irving E. A. and Bamford M. (2002) Role of mitogen- and stress-activated kinases in ischemic injury. J. Cereb. Blood Flow Metab. 22, 631-647.
22. Junier M. P. (2000) What role(s) for TGF-α in the central nervous system? Prog. Neurobiol. 62, 443-473.
23. Justicia C., Perez-Asensio F. J., Burguete M. C., Salom J. B. and Planas A. M. (2001) Administration of transforming growth factor-α reduces infarct volume after transient focal cerebral ischemia in the rat. J. Cereb. Blood Flow Metab. 21, 1097-1104.
24. Kelly E. J., Quaife C. J., Froelick G. J. and Palmiter R. D. (1996) Metallothionein I and II protect against zinc deficiency and zinc toxicity in mice. J. Nutr. 126, 1782-1790.
25. Kelty J. D., Noseworthy P. A., Feder M. E., Robertson R. M. and Ramirez J. M. (2002) Thermal preconditioning and heat-shock protein 72 preserve synaptic transmission during thermal stress. J. Neurosci. 22, RC193: 1-6.
26. Kirino T. (2002) Ischemic tolerance. J. Cereb. Blood Flow Metab. 22, 1283-1296.
27. Kobayashi S., Harris V. A. and Welsh F. A. (1995) Spreading depression induces tolerance of cortical neurons to ischemia in rat brain. J. Cereb. Blood Flow Metab. 15, 721-727.
28. Lee T. S. and Chau L. Y. (2002) Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat. Med. 8, 240-246.
29. Lee P. J., Jiang B.-H., Chin B. Y., Iyet N. V., Alam J., Semenza G. L. and Choi A. M. K. (1997) Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J. Biol. Chem. 272, 5375-5381.
30. Mardian J. K. and Isenberg I. (1978) Preparative gel electrophoresis: detection, excision, and elution of protein bands from unstained gels. Anal. Biochem. 91, 1-12.
31. Massague J. (1998) TGF-β signal transduction. Ann. Rev. Biochem. 67, 753-791.
32. McLaughlin B., Hartnett K. A., Erhardt J. A., Legos J. J., White R. F., Barone F. C. and Aizenman E. (2003) Caspase 3 activation is essential for neuroprotection in preconditioning. Proc. Natl Acad. Sci. USA 100, 715-720.
33. Mehlen P., Kretz-Remy C., Preville X. and Arrigo A. P. (1996) Human hsp27, Drosophila hsp27 and human αB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNFα-induced cell death. EMBO J. 15, 2695-2706.
34. Nandagopal K., Dawson T. M. and Dawson V. L. (2001) Critical role for nitric oxide signaling in cardiac and neuronal ischemic preconditioning and tolerance. J. Pharmacol. Exp. Ther 297, 474-478.
35. O'Farrell P. H. (1975) High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250, 4007-4021.
36. Ohtsuki T., Ruetzler C. A., Tasaki K. and Hallenbeck J. M. (1996) Interleukin-1 mediates induction of tolerance to global ischemia in gerbil hippocampal CA1 neurons. J. Cereb. Blood Flow Metab. 16, 1137-1142.
37. Osada S., Takano K., Nishihara T., Suzuki T., Muramatsu M. and Imagawa M. (1995) CCAAT/enhancer-binding proteins α and β interact with the silencer element in the promoter of glutathione S transferase P gene during hepatocarcinogenesis. J. Biol. Chem. 270, 31288-31293.
38. Panahian N., Yoshiura M. and Maines M. D. (1999) Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J. Neurochem. 72, 1187-1203.
39. Paxinos G. and Watson C. (1998) The Rat Brain in Stereotaxic Coordinates, 4th edn. Academic Press, New York.
40. Prass K., Wiegand F., Schumann P., Ahrens M., Kapinya K., Harms C., Liao W., Trendelenburg G., Gertz K., Moskowitz M. A. et al. (2000) Hyperbaric oxygenation induced tolerance against focal cerebral ischemia in mice is strain dependent. Brain Res. 871, 146-150.
41. Rajdev S., Hara K., Kokubo Y., Mestril R., Dillmann W., Weinstein P. R. and Sharp F. R. (2000) Mice overexpressing rat heat shock protein 70 are protected against cerebral infarction. Ann. Neurol. 47, 782-791.
42. Rao V. L., Dogan A., Todd K. G., Bowen K. K., Kim B.-T., Rothstein J. D. and Dempsey R. J. (2001a) Antisense knockdown of the glial glutamate transporter GLT-1, but not the neuronal glutamate transporter EAAC1, exacerbates transient focal cerebral ischemia-induced neuronal damage in rat brain. J. Neurosci. 21, 1876-1883.
43. Rao V. L., Dogan A., Bowen K. K. and Dempsey R. J. (2001b) Omithine decarboxylase knockdown exacerbates transient focal cerebral ischemia-induced neuronal damage in rat brain. J. Cereb. Blood Flow Metab. 21, 945-954.
44. Rao V. L., Bowen K. K., Dhodda V. K., Song G., Franklin J. L., Gavva N. R. and Dempsey R. J. (2002) Gene expression analysis of spontaneously hypertensive rat cerebral cortex following transient focal cerebral ischemia. J. Neurochem. 83, 1072-1086.
45. Rao V. L., Dhodda V. K., Song G., Bowen K. K. and Dempsey R. J. (2003) Traumatic brain injury-induced acute gene expression changes in rat cerebral cortex identified by GeneChip analysis. J. Neurosci. Res. 71, 208-219.
46. Rejdak R., Rejdak K., Sieklucka-Dziuba M., Stelmasiak Z. and Grieb P. (2001) Brain tolerance and preconditioning. Pol. J. Pharmacol. 53, 73-79.
47. Schmidt-Kastner R., Zhang B., Belayev L., Khoutorova L., Amin R., Busto R. and Ginsberg M. D. (2002) DNA microarray analysis of cortical gene expression during early recirculation after focal brain ischemia in rat. Mol. Brain Res. 108, 81-93.
48. Seki T. (2002) Expression patterns of immature neuronal markers PSA-NCAM, CRMP-4 and neuro-D in the hippocampus of young adult and aged rodents. J. Neurosci. Res. 70, 327-334.
49. Shamloo M., Rytter A. and Wieloch T. (1999) Activation of the extracellular signal-regulated protein kinase cascade in the hippocampal CA1 region in a rat model of global cerebral ischemic preconditioning. Neuroscience 93, 81-88.
50. Sheng H., Brady T. C., Pearlstein R. D., Crapo J. D. and Warner D. S. (1999) Extracellular superoxide dismutase deficiency worsens outcome from focal cerebral ischemia in the mouse. Neurosci. Lett. 267, 13-16.
51. Sheng H., Kudo M., Mackensen G. B., Pearlstein R. D., Crapo J. D. and Warner D. S. (2000) Mice overexpressing extracellular superoxide dismutase have increased resistance to global cerebral ischemia. Exp. Neurol. 163, 392-398.
52. Shimizu S., Nagayama T., Jin K. L., Zhu L., Loeffert J. E., Watkins S. C., Graham S. H. and Simon R. P. (2001) bcl-2 Antisense treatment prevents induction of tolerance to focal ischemia in the rat brain. J. Cereb. Blood Flow Metab. 21, 233-243.
53. Snyder S. H. and Baranano D. E. (2001) Heme oxygenase: a font of multiple messengers. Neuropsychopharmacology 25, 294-298.
54. Song G., Cechvala C., Resnick D. K., Dempsey R. J. and Rao V. L. (2001) GeneChip analysis after acute spinal cord injury in rat. J. Neurochem. 79, 804-815.
55. Song G., Dhodda V. K., Blei A. T., Dempsey R. J. and Rao V. L. (2002) GeneChip analysis shows altered mRNA expression of transcripts of neurotransmitter and signal transduction pathways in the cerebral cortex of portacaval shunted rats. J. Neurosci. Res. 68, 730-737.
56. Takagi K., Ginsberg M. D., Globus M. Y., Martinez E. and Busto R. (1994) Effect of hyperthermia on glutamate release in ischemic penumbra after middle cerebral artery occlusion in rats. Am. J. Physiol. 267, H1770-H1776.
57. Trendelenburg G., Prass K., Priller J. et al. (2002) Serial analysis of gene expression identifies metallothionein-II as major neuroprotective gene in mouse focal cerebral ischemia. J. Neurosci. 22, 5879-5888.
58. Truettner J., Busto R., Zhao W., Ginsberg M. D. and Perez-Pinzon M. A. (2002) Effect of ischemic preconditioning on the expression of putative neuroprotective genes in the rat brain. Mol. Brain Res. 103, 106-115.
59. Valentim L. M., Rodnight R., Geyer A. B., Horn A. P., Tavares A., Cimarosti H., Netto C. A. and Salbego C. G. (2003) Changes in heat shock protein 27 phosphorylation and immunocontent in response to preconditioning to oxygen and glucose deprivation in organotypic hippocampal cultures. Neuroscience 118, 379-386.
60. Van Lookeren Campagne M., Thibodeaux H., Van Bruggen N., Caims B., Gerlai R., Palmer J. T., Williams S. P. and Lowe D. G. (1999) Evidence for a protective role of metallothionein-1 in focal cerebral ischemia. Proc. Natl Acad. Sci. USA 96, 12870-12875.
61. Verrecchia F., Chu M. L. and Mauviel A. (2001) Identification of novel TGF-β/Smad gene targets in dermal fibroblasts using a combined cDNA microarray/promoter transactivation approach. J. Biol. Chem. 276, 17058-17062.
62. Widmann C., Gibson S., Jarpe M. B. and Johnson G. L. (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol. Rev. 79, 143-180.
63. Xu H., Aibiki M. and Nagoya J. (2002) Neuroprotective effects of hyperthermic preconditioning on infarcted volume after middle cerebral artery occlusion in rats: role of adenosine receptors. Crit. Care Med. 30, 1126-1130.
64. Yan J. X., Sanchez J. C., Binz P. A., Williams K. L. and Hochstrasser D. F. (1999) Method for identification and quantitative analysis of protein lysine methylation using matrix-assisted laser desorption/ionization - time-of-flight mass spectrometry and amino acid analysis. Electrophoresis 20, 749-754.
65. Yenari M. A., Fink S. L., Sun G. H., Chang L. K., Patel M. K., Kunis D. M., Onley D., Ho D. Y., Sapolsky R. M. and Steinberg G. K. (1998) Gene therapy with HSP72 is neuroprotective in rat models of stroke and epilepsy. Ann. Neurol. 44, 584-591.
66. Yunoki M., Nishio S., Ukita N., Anzivino M. J. and Lee K. S. (2003) Hypothermic preconditioning induces rapid tolerance to focal ischemic injury in the rat. Exp. Neurol. 181, 291-300.
67. Zhu Y., Yang G. Y., Ahlemeyer B., Pang L., Che X. M., Culmsee C., Klumpp S. and Krieglstein J. (2002) Transforming growth factor-β1 increases bad phosphorylation and protects neurons against damage. J. Neurosci. 22, 3898-3909.