Brain proteomics identifies potential simvastatin targets in acute phase of stroke in a rat embolic model

Journal of Neurochemistry

Volumn 130, Issue 2, 2014, Pages 301-312

  Campos Martorell, Mireia ^a   Salvador, Nelida ^b   Monge, Marta ^c   Canals, Francesc ^c   García Bonilla, Lidia ^a   Hernández Guillamon, Mar ^a   Ayuso, María Irene ^b   Chacõn, Pilar ^a   Rosell, Anna ^a   Alcazar, Alberto ^b   Montaner, Joan ^a  

^a HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^b HOSPITAL RAMÓN Y CAJAL   (Spain)

^c UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

acute phase treatment; embolic cerebral ischemia; proteomics; rat; simvastatin; stroke

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; ALBUMIN; BETA TUBULIN; CHAPERONIN 60; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; DYNAMIN I; FODRIN; FRUCTOSE BISPHOSPHATE ALDOLASE; FUMARATE HYDRATASE; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 75; HEMOGLOBIN ALPHA CHAIN; HEMOGLOBIN BETA CHAIN; HEXOKINASE 1; MICROTUBULE ASSOCIATED PROTEIN 1; MYELIN BASIC PROTEIN; NEUROFILAMENT LIGHT POLYPEPTIDE; NEUROFILAMENT MEDIUM POLYPEPTIDE; NEUROMODULIN; PHOSPHOGLUCONATE DEHYDROGENASE; PHOSPHOGLYCERATE MUTASE; PLACEBO; POLYPEPTIDE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PYRUVATE CARBOXYLASE; SERINE PROTEINASE INHIBITOR; SIMVASTATIN; SYNAPSIN II; UNCLASSIFIED DRUG;

ACUTE DRUG ADMINISTRATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CORTEX; BRAIN EMBOLISM; BRAIN HOMOGENATE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; CORPUS STRIATUM; DRUG MECHANISM; DRUG TARGETING; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; RAT; RAT MODEL; STROKE PATIENT; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; WISTAR RAT;

ACUTE PHASE TREATMENT; EMBOLIC CEREBRAL ISCHEMIA; PROTEOMICS; RAT; SIMVASTATIN; STROKE;

ANIMALS; BLOTTING, WESTERN; BRAIN; BRAIN CHEMISTRY; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; INFARCTION, MIDDLE CEREBRAL ARTERY; INTRACRANIAL EMBOLISM; MALE; NEUROLOGIC EXAMINATION; PROTEOMICS; RATS; RATS, WISTAR; SIMVASTATIN; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STROKE;

EID: 84903989192     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12719     Document Type: Article

References (62)

1. Aikman J., O'steen B., Silver X., Torres R., Boslaugh S., Blackband S., Padgett K., Wang K. K., Hayes R., and, Pineda J., (2006) Alpha-II-spectrin after controlled cortical impact in the immature rat brain. Dev. Neurosci. 28, 457-465. (Pubitemid 44310511)
2. Alban A., David S. O., Bjorkesten L., Andersson C., Sloge E., Lewis S., and, Currie I., (2003) A novel experimental design for comparative two dimensional gel analysis: two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics 3, 36-44. (Pubitemid 36151066)
3. Amin-Hanjani S., Stagliano N. E., Yamada M., Huang P. L., Liao J. K., and, Moskowitz M. A., (2001) Mevastatin, an HMG-CoA reductase inhibitor, reduces stroke damage and upregulates endothelialnitric oxide synthase in mice. Stroke 32, 980-986.
4. Balduini W., De Angelis V., Mazzoni E., and, Cimino M., (2001) Simvastatin protects against long-lasting behavioral and morphological consequences of neonatal hypoxic/ischemic brain injury. Stroke 32, 2185-2191. (Pubitemid 32868120)
5. Belfiore F., Rabuazzo A. M., Napoli E., Borzi V., and, Lo Vecchio L., (1975) Enzymes of glucose metabolism and of the citrate cleavage pathway in adipose tissue of normal and diabetic subjects. Diabetes 24, 865-873.
6. Bellizzi D., Taverna D., D'Aquila P., De Blasi S., and, De Benedictis G., (2009) Mitochondrial DNA variability modulates mRNA and intramitochondrial protein levels of HSP60 and HSP75: experimentalevidence from cybrid lines. Cell Stress Chaperones 14, 265-271.
7. Brioschi M., Lento S., Tremoli E., and, Banfi C., (2013) Proteomic analysis of endothelial cell secretome: a means of studying the pleiotropic effects of Hmg-CoAreductase inhibitors. J. Proteomics 78, 346-361.
8. Carmichael S. T., (2005) Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx 2, 396-409. (Pubitemid 41444874)
9. Chen J., Zhang Z. G., Li Y., et al,. (2003) Statins induce angiogenesis, neurogenesis, and synaptogenesis after stroke. Ann. Neurol. 53, 743-751. (Pubitemid 36622511)
10. Chen A., Liao W. P., Lu Q., Wong W. S., and, Wong P. T., (2007) Upregulation of dihydropyrimidinase-related protein 2, spectrin alpha II chain, heat shock cognate protein 70 pseudogene 1 and tropomodulin 2 after focal cerebral ischemia in rats-a proteomics approach. Neurochem. Int. 50, 1078-1086. (Pubitemid 46962809)
11. Endres M., Laufs U., Huang Z., Nakamura T., Huang P., Moskowitz M. A., and, Liao J. K., (1998) Stroke protection by 3-hydroxy-3 methylglutaryl (HMG)-CoA reductasa inhibitors mediated by endothelial nitric oxide synthase. Proc. Natl Acad. Sci. USA 95, 8880-8885. (Pubitemid 28350583)
12. Esselens C. W., Malapeira J., Colomé N., Moss M., Canals F., and, Arribas J., (2008) Metastasis-associated C4.4A, a GPI-anchored protein cleaved by ADAM10 and ADAM17. Biol. Chem. 389, 1075-1084.
13. Essig M., Nguyen G., Prié D., Escoubet B., Sraer J. D., and, Friedlander G., (1998) 3-Hydroxy-3-methylglutaryl coenzyme A reductase inhibitors increase fibrinolytic activity in rat aortic endothelial cells. Role of geranylgeranylation and Rho proteins. Circ. Res. 83, 683-690. (Pubitemid 28462781)
14. Föcking M., Besselmann M., and, Trapp T., (2006) Proteomics of experimental stroke in mice. Acta Neurobiol. Exp. (Wars). 66, 273-278. (Pubitemid 46114711)
15. Fukata Y., Itoh T. J., Kimura T., et al,. (2002) CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat. Cell Biol. 4, 583-591.
16. García-Bonilla L., Campos M., Giralt D., Salat D., Chacõn P., Hernández-Guillamon M., Rosell A., and, Montaner J., (2012) Evidence for the efficacy of statins in animal stroke models: a meta-analysis. J. Neurochem. 122, 233-243.
17. Ghayour-Mobarhan M., Lamb D. J., Vaidya N., Livingstone C., Wang T., and, Ferns G. A., (2005) Heat shock protein antibody titers are reduced by statin therapy in dyslipidemic subjects: a pilot study. Angiology 56, 61-68. (Pubitemid 40175639)
18. Greisenegger S., Müllner M., Tentschert S., Lang W., and, Lalouschek W., (2004) Effect of pretreatment with statins on the severity of acute ischemic cerebrovascular events. J. Neurol. Sci. 221, 5-10. (Pubitemid 38721284)
19. Gu M. X., Fu Y., Sun X. L., Ding Y. Z., Li C. H., Pang W., Pan S., and, Zhu Y., (2012) Proteomic analysis of endothelial lipid rafts reveals a novel role of statins in antioxidation. J. Proteome Res. 11, 2365-2373.
20. Guisasola M. C., Dulin E., Almendral J., and, Garcia-Barreno P., (2009) Reduction of heat shock protein antibody levels by statin therapy. Lipids 44, 317-324.
21. Hernandez-Guillamon M., Garcia-Bonilla L., Solé M., et al,. (2010) Plasma VAP-1/SSAO activity predicts intracranial hemorrhages and adverse neurological outcome after tissue plasminogen activator treatment in stroke. Stroke 41, 1528-1535.
22. Hetrick B., Han M. S., Helgeson L. A., and, Nolen B. J., (2013) Small molecules CK-666 and CK-869 inhibit actin-related protein 2/3 complex by blocking an activating conformational change. Chem. Biol. 23 (20), 701-712.
23. Hori M., Nakamachi T., Rakwal R., Shibato J., Ogawa T., Aiuchi T., Tsuruyama T., Tamaki K., and, Shioda S., (2012) Transcriptomics and proteomics analyses of the PACAP38 influenced ischemic brain in permanent middle cerebral artery occlusion model mice. J. Neuroinflammation 9, 256.
24. Huff R. M., Axton J. M., and, Neer E. J., (1985) Physical and immunological characterization of a guanine nucleotide-binding protein purified from bovine cerebral cortex. J. Biol. Chem. 260, 10864-10871. (Pubitemid 16252274)
25. Jain M. K., and, Ridker P. M., (2005) Anti-inflammatory effects of statins: clinical evidence and basic mechanisms. Nat. Rev. Drug Discovery 4, 977-987.
26. Jonsson N., and, Asplund K., (2001) Does pre-treatment with statins improve clinical outcome after stroke? A pilot-case-referent study. Stroke 32, 1112-1115. (Pubitemid 32825793)
27. Julien F., and, Biebuyck M. B., (1990) The metabolic response to stress: an overview and update. Anesthesiology 73, 303-327.
28. Kahles T., Luedike P., Endres M., Galla H. J., Steinmetz H., Busse R., Neumann-Haefelin T., and, Brandes R. P., (2007) NADPH oxidase plays a central role in blood-brain barrier damage in experimental stroke. Stroke 38, 3000-3006. (Pubitemid 350035696)
29. Kiang J. G., and, Tsokos G. C., (1998) Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacol. Ther. 80, 183-201. (Pubitemid 28498227)
30. Koh P. O., (2010) Proteomics analysis of focal cerebral ischemic injury in male rats. J. Vet. Med. Sci. 72, 181-185.
31. Koh P. O., (2011) Identification of proteins differentially expressed in cerebral cortexes of Ginkgo biloba extract (EGb761)-tetraedrats in a middle cerebral artery occlusion model-a proteomics approach. Identification of proteins approach. Am. J. Chin. Med. 39, 315-324.
32. Kregel C., (2002) Invited review: heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J. Appl. Physiol. 92, 2177-2186.
33. Kureishi Y., Luo Z., Shiojima I., Bialik A., Fulton D., Lefer D. J., Sessa W. C., and, Walsh K., (2000) The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals. Nat. Med. 6, 1004-1010.
34. Lapergue B., Moreno J. A., Dang B. Q., et al,. (2010) Protective effect of high-density lipoprotein-based therapy in a model of embolic stroke. Stroke 41, 1536-1542.
35. Lashgari M. S., Devine-Beach K., Haas S., and, Khalili K., (1990) Nuclear proteins in mouse brain cells bind specifically to the myelin basic protein regulatory region. J. Clin. Invest. 86, 1671-1677. (Pubitemid 20372619)
36. Laufs U., La Fata V., Plutzky J., and, Liao J. K., (1998) Upregulation of endotelial nitric oxid syntase by HMG CoA reductasa inhibitors. Circulation 97, 1129-1135. (Pubitemid 28152885)
37. Laufs U., Gertz K., and, Huang P., (2000) Atorvastatin upregulates type III nitric oxide synthase in thrombocytes, decreases platelet activation, and protects from cerebral ischemia in normocholesterolemic mice. Stroke 31, 2442-2449.
38. Law R. H. P., Zhang Q., McGowan S., et al,. (2006) An overview of the serpin superfamily. Genome Biol. 7, 216.
39. Martí-Fàbregas J., Gomis M., Arboix A., et al,. (2004) Favorable outcome of ischemic stroke in patients pretreated with statins. Stroke 35, 1117-1121. (Pubitemid 38543528)
40. Montaner J., Chacõn P., Krupinski J., Rubio F., Millán M., Molina C. A., Hereu P., Quintana M., and, Alvarez-Sabín J., (2008) Simvastatin in the acute phase of ischemic stroke: a safety and efficacy pilot trial. Eur. J. Neurol. 15, 82-90. (Pubitemid 350265291)
41. Moohebati M., Bidmeshgi S., Azarpazhooh M. R., et al,. (2011) Simvastatin treatment reduces heat shock protein 60,65 and 70 antibody titers in dyslipidemic patients: a randomized, double-blind, placebo controlled, cross-over trial. Clin. Biochem. 44, 192-197.
42. Nagaraja T. N., Knight R. A., Croxen R. L., Konda K. P., and, Fenstermacher J. D., (2006) Acute neurovascular unit protection by simvastatin in transient cerebral ischemia. Neurol. Res. 28, 826-830. (Pubitemid 44904456)
43. Neves S. R., Ram P. T., and, Iyengar R., (2002) G protein pathways. Science 296, 1636-1639. (Pubitemid 34579147)
44. NINDS rt-PA Stroke Study Group (1995) Tissue plasminogen activator for acute ischemic stroke. N. Engl. J. Med. 333, 1581-1587.
45. NINDS rt-PA Stroke Study Group (1997) Intracerebral hemorrhage after intravenous t-pa therapy for ischemic stroke. Stroke 28, 2109-2118.
46. Palinski W., and, Tsimikas S., (2002) Immunomodulatory effects of statins: mechanisms and potential impact on arteriosclerosis. J. Am. Soc. Nephrol. 13, 1673-1681. (Pubitemid 34579257)
47. Perez-Asensio F. J., Hurtado O., Burguete M. C., et al,. (2005) Inhibition of iNOS activity by 1400 W decreases glutamate release and ameliorates stroke outcome after experimental ischemia. Neurobiol. Dis. 18, 375-384. (Pubitemid 40431121)
48. Pfaffinger P.J., Martin J. M., Hunter D. D., Nathanson N. M., and, Hille B., (1985) GTP-binding proteins couple cardiac muscarinic receptors to a K channel. Nature 317, 536-538. (Pubitemid 16224160)
49. Pienaar I. S., Schallert T., Hattingh S., and, Daniels W. M., (2009) Behavioral and quantitative mitochondrial proteome analyses of the effects of simvastatin: implications for models of neural degeneration. J. Neural Transm. 116, 791-806.
50. Pirzad Jahromi G., Seidi S., Sadr S. S., Shabanzadeh A. P., Keshavarz M., Kaka G. R., Hosseini S. K., Sohanaki H., and, Charish J., (2012) Therapeutic effects of a combinatorial treatment of simvastatin and bone marrow stromal cells on experimental embolic stroke. Basic Clin. Pharmacol. Toxicol. 110, 487-493.
51. Quinn C. C., Gray G. E., and, Hockfield S., (1999) A family of proteins implicated in axon guidance and outgrowth. J. Neurobiol. 41, 158-164. (Pubitemid 29467615)
52. Roger V. L., Go A. S., and, Lloyd-Jones D. M., et al,., American Heart Association Statistics Committee and Stroke Statistics Subcommittee. (2012) Heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation 125, e2-e220.
53. Rosenson R. S., (1999) Non-lipid-lowering effects of statins on atherosclerosis. Curr Cardiol Rep. 1, 225-232.
54. Shevchenko A., Wilm M., Vorm O., and, Mann M. l., (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858.
55. Tortosa E., Galjart N., Avila J., and, Sayas C. L., (2013) MAP1B regulates microtubule dynamics by sequestering EB1/3 in the cytosol of developing neuronal cells. EMBO J. 2 (32), 1293-1306.
56. Voloboueva L. A., Duan M., Ouyang Y., Emery J. F., Stoy C., and, Giffard R. G., (2008) Overexpression of mitochondrial Hsp70/Hsp75 protects astrocytes against ischemic injury in vitro. J. Cereb. Blood Flow Metab. 28, 1009-1016. (Pubitemid 351589637)
57. Wang C. X., Todd K. G., Yang Y., Gordon T., and, Shuaib A., (2001) Patency of cerebral microvessels after focal embolic stroke in the rat. J. Cereb. Blood Flow Metab. 21 (4), 413-421. (Pubitemid 32298888)
58. Worley P. F., Baraban J. M., Van Dops C., Neer E. J., and, Snyder S. H., (1986) Go, a guanine nucleotide-binding protein: Immunohistochemical localization in rat brain resembles distribution of second messenger systems. Proc. Natl Acad. Sci. USA 83, 4561-4565. (Pubitemid 16057089)
59. Yin W., Signore A. P., Iwai M., Cao G., and, Gao Y., (2008) Rapidly increased neuronal mitochondrial biogenesis after hypoxic-ischemic brain injury. Stroke 39, 3057-3063.
60. Yoon S. S., Dambrosia J., Chalela J., Ezzeddine M., Warach S., Haymore J., Davis L., and, Baird A. E., (2004) Rising statin use and effect on ischemic stroke outcome. BMC Med. 23, 2-4.
61. Zhang R. L., Chopp M., Zhang Z. G., Jiang Q., and, Ewing J. R., (1997) A rat model of focal embolic cerebral ischemia. Brain Res. 766, 83-92. (Pubitemid 27431437)
62. Zhou Y., Bhatia I., Cai Z., He Q. Y., Cheung P. T., and, Chiu J. F., (2008) Proteomic analysis of neonatal mouse brain: evidence for hypoxia- and ischemia-induced dephosphorylation of collapsin response mediator proteins. J. Proteome Res. 7, 2507-2515.