Gene expression analysis to identify molecular correlates of pre- and post-conditioning derived neuroprotection

Journal of Molecular Neuroscience

Volumn 47, Issue 2, 2012, Pages 322-339

  Prasad, Shiv S ^a   Russell, Marsha ^a   Nowakowska, Margeryta ^a   Williams, Andrew ^b   Yauk, Carole ^b  

^a HEALTH CANADA   (Canada)

^b Environmental Health Center   (Canada)

Author keywords

Ischaemia; Microarray; Neuroprotection; Postconditioning; Preconditioning

Indexed keywords

A DISINTEGRIN AND METALLOPROTEINASE WITH THROMBOSPONDIN1 MOTIF 9; BRAIN EXPRESSED, X LINKED 1; BRUNO LIKE 4, RNA BINDING PROTEIN; COPINE IV; GLUCOSE; METALLOPROTEINASE; NESTIN; NEUREXIN; NEUREXIN 3; OXYGEN; POLYMERASE I AND TRANSCRIPT RELEASE FACTOR; PROTEIN; TRANSGELIN; UNCLASSIFIED DRUG; VIMENTIN;

ANIMAL CELL; ARTICLE; BRAIN CELL; BRAIN ISCHEMIA; CLUSTER ANALYSIS; CONTROLLED STUDY; DOWN REGULATION; GENE CLUSTER; GENE EXPRESSION; GENE IDENTIFICATION; IN VITRO STUDY; ISCHEMIC POSTCONDITIONING; ISCHEMIC PRECONDITIONING; MICROARRAY ANALYSIS; NEUROPROTECTION; NONHUMAN; RAT; UPREGULATION;

ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; CYTOPROTECTION; FEMALE; GENE EXPRESSION REGULATION; ISCHEMIC PRECONDITIONING; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RATS, WISTAR; TRANSCRIPTOME;

NES; RATTUS;

EID: 84863872293     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-012-9751-3     Document Type: Article

References (68)

1. Banfic H, Tang X, Batty IH, Downes CP, Chen C, Rittenhouse SE (1998) A novel integrin-activated pathway forms PKB/Akt-stimulatory phosphatidylinositol 3,4-bisphosphate via phosphatidylinositol 3-phosphate in platelets. J Biol Chem 273:13-16 (Pubitemid 28042167)
2. Barone FC,White RF, Spera PA, Ellison J, Currie RW,Wang X, Feuerstein GZ (1998) Ischemic preconditioning and brain tolerance: temporal histological and functional outcomes, protein synthesis requirement, and interleukin- 1 receptor antagonist and early gene expression. Stroke 29:1937-1950 (Pubitemid 28399995)
3. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Series B Methodolog 57(1):289-300
4. Blondeau N, Widmann C, Lazdunski M, Heurteaux C (2002) Polyunsaturated fatty acids induce ischemic and epileptic tolerance. Neuroscience 109:231-241 (Pubitemid 34098964)
5. Bowen KK, Naylor M, Vemuganti R (2006) Prevention of inflammation is a mechanism of preconditioning-induced neuroprotection against focal cerebral ischemia. Neurochem Int 49:127-135 (Pubitemid 43867070)
6. Chen J, Graham SH, Zhu RL, Simon RP (1996) Stress proteins and tolerance to focal cerebral ischemia. J Cereb Blood Flow Metab 16:566-577 (Pubitemid 26227065)
7. Chen J, Jin K, Chen M, Pei W, Kawaguchi K, Greenberg DA, Simon RP (1997) Early detection of DNA strand breaks in the brain after transient focal ischemia: implications for the role of DNA damage in apoptosis and neuronal cell death. J Neurochem 69:232-245 (Pubitemid 27274177)
8. Cui X, Hwang JT, Qiu J, Blades NJ, Churchill GA (2005) Improved statistical tests for differential gene expression by shrinking variance components estimates. Biostatistics 6(1):59-75 (Pubitemid 41240370)
9. De Hoon MJL, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20(9):1453-1454 (Pubitemid 38931415)
10. R Development Core Team (2005) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
11. Ding YH, Li J, Yao WX, Rafols JA, Clark JC, Ding Y (2006) Exercise preconditioning upregulates cerebral integrins and enhances cerebrovascular integrity in ischemic rats. Acta Neuropathol 112 (1):74-84 (Pubitemid 43942164)
12. Ding K, Su Y, Pang L, Lu Q, Wang Z, Zhang S, Zheng S, Mao J, Zhu Y (2009) Inhibition of apoptosis by downregulation of hBex1, a novel mechanism, contributes to the chemoresistance of Bcr/Abl+leukemic cells. Carcinogenesis 30(1):35-42
13. Dirnagl U, Simon RP, Hallenbeck JM (2003) Ischemic tolerance and endogenous neuroprotection. Trends Neurosci 26(5):248-254 (Pubitemid 36556155)
14. Dirnagl U, Becker K, Meisel A (2009) Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol 8:398-412
15. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863-14868 (Pubitemid 29003722)
16. Emsley HC, Hopkins SJ (2008) Acute ischaemic stroke and infection: recent and emerging concepts. Lancet Neurol 7:341-353 (Pubitemid 351380535)
17. Frantseva MV, Carlen PL, Perez Velazquez JL (2001) Dynamics of intracellular calcium and free radical production during ischemia in pyramidal neurons. Free Radic Biol Med 31:1216-1227 (Pubitemid 33052497)
18. Gary DS, Mattson MP (2001) Integrin signaling via the PI3-kinase-Akt pathway increases neuronal resistance to glutamate-induced apoptosis. J Neurochem 76:1485-1496 (Pubitemid 32198253)
19. Gidday JM (2006) Cerebral preconditioning and ischaemic tolerance. Nat Rev Neurosci 7(6):437-448
20. Goodnight JH, Harvey WR (1978) Least-square means in the fixed-effects general linear models. Technical report no. R-103. SAS Institute Inc, Cary
21. Jiang X, Shi E, Nakajima Y, Sato S (2006) Postconditioning, a series of brief interruptions of early reperfusion, prevents neurologic injury after spinal cord ischemia. Ann Surg 244:148-153 (Pubitemid 44297459)
22. Kerr MK (2003) Design considerations for efficient and effective microarray studies. Biometrics 59:822-828
23. Kerr MK, Churchill GA (2001) Statistical design and the analysis of gene expression microarray data. Genet Res 77(2):123-128
24. King WG, Mattaliano MD, Chan TO, Tsichlis PN, Brugge JS (1997) Phosphatidylinositol-3-kinase is required for integrin-stimulated Akt and Raf-2/mitogen-activated protein kinase pathway activation. Mol Cell Biol 17:4406-4418 (Pubitemid 27318118)
25. Kirino T (2002) Ischemic tolerance. J Cereb Blood Flow Metab 22 (11):1283-1296
26. Kitagawa K, Matsumoto M, Tagaya M et al (1990) "Ischemic tolerance"phenomenon found in the brain. Brain Res 528:21-24
27. Koerner IP, Gatting M, Noppens R, Kempski O, Brambrink AM (2007) Induction of cerebral ischemic tolerance by erythromycin preconditioning reprograms the transcriptional response to ischemia and suppresses inflammation. Anesthesiology 106:538-547 (Pubitemid 46662220)
28. Kuroda S, Siesjö BK (1997) Reperfusion damage following focal ischemia: pathophysiology and therapeutic windows. Clin Neurosci 4(4):199-212 (Pubitemid 27250687)
29. Lee JW, Juliano RL (2000) Alpha5beta1 integrin protects intestinal epithelial cells from apoptosis through a phosphatidylinositol 3-kinase and protein kinase B-dependent pathway. Mol Biol Cell 11:1973-1987 (Pubitemid 30408058)
30. Liu PK, Hsu CY, Dizdaroglu M, Floyd RA, Kow YW, Karakaya A, Rabow LE, Cui J-K (1996) Damage, repair, and mutagenesis in nuclear genes after mouse forebrain ischemia-reperfusion. J Neurosci 16:6795-6806 (Pubitemid 26359363)
31. Lusardi TA, Farr CD, Faulkner CL et al (2010) Ischemic preconditioning regulates expression of microRNAs and a predicted target, MeCP2, in mouse cortex. J Cereb Blood Flow Metab 30:744-756
32. Marsh B, Stevens SL, Packard AE, Gopalan B, Hunter B, Leung PY, Harrington CA, Stenzel-Poore MP (2009) Systemic lipopolysaccharide protects the brain from ischemic injury by reprogramming the response of the brain to stroke: a critical role for IRF3. J Neurosci 29:9839-9849
33. Maulik N, Engelman RM, Rousou JA, Flack JE, III, Deaton D, Das DK (1999) Ischemic preconditioning reduces apoptosis by upregulating anti-death gene Bcl-2. Circulation 100:II369-II375 (Pubitemid 29523563)
34. Maulik N, Sasaki H, Addya S, Das DK (2000) Regulation of cardiomyocyte apoptosis by redoxsensitive transcription factors. FEBS Lett 485:7-12
35. McColl BW, Allan SM, Rothwell NJ (2009) Systemic infection, inflammation and acute ischemic stroke. Neuroscience 158:1049-1061
36. Meller R, Minami M, Cameron JA et al (2005) CREB-mediated Bcl-2 protein expression after ischemic preconditioning. J Cereb Blood Flow Metab 25(2):234-246 (Pubitemid 40171205)
37. Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124-1136 (Pubitemid 17174962)
38. 2+ concentration in the hippocampal CA1 area during global ischemia and reperfusion in the rat: a possible cause of delayed neuronal death. Neuroscience 88(1):57-67
39. Nakamura T, Xi G, Hua Y, Hoff JT, Keep RF (2003) Nestin expression after experimental intracerebral hemorrhage. Brain Res 981(1-2):108-117 (Pubitemid 37281225)
40. O'Duffy AE, Bordelon YM, McLaughlin B (2007) Killer proteases and little strokes: how the things that do not kill you make you stronger. J Cereb Blood Flow Metab 27:655-668 (Pubitemid 46474612)
41. Perez-Pinzon MA, Xu GP, Dietrich WD, Rosenthal M, Sick TJ (1997) Rapid preconditioning protects rats against ischemic neuronal damage after 3 but not 7days of reperfusion following global cerebral ischemia. J Cereb Blood Flow Metab 17:175-182 (Pubitemid 27085841)
42. Pignataro G, Meller R, Inoue K et al (2008) In vivo and in vitro characterization of a novel neuroprotective strategy for stroke: ischemic postconditioning. J Cereb Blood Flow Metab 28:232-241 (Pubitemid 351161298)
43. Pignataro G, Scorziello A, Di RG, Annunziato L (2009) Post-ischemic brain damage: effect of ischemic preconditioning and postconditioning and identification of potential candidates for stroke therapy. FEBS J 276:46-57
44. Prasad S, Kojic L, Wen YH, Chen Z, Xiong W, Jia W, Cynader MS (2010) Retinal gene expression after central retinal artery ligation: effects of ischemia and reperfusion. Invest Ophthalmol Vis Sci 51 (12):6207-6219
45. Prasad SS, Russell M, Nowakowska M (2011) Neuroprotection induced in vitro by ischemic preconditioning and postconditioning: modulation of apoptosis and pi3k-Akt pathways. J Mol Neurosci 43(3):428-442
46. Rosenzweig HL, Lessov NS, Henshall DC, Minami M, Simon RP, Stenzel-Poore MP (2004) Endotoxin preconditioning prevents cellular inflammatory response during ischemic neuroprotection in mice. Stroke 35:2576-2581 (Pubitemid 39458420)
47. Rosenzweig HL, Minami M, Lessov NS, Coste SC, Stevens SL, Henshall DC, Meller R, Simon RP, Stenzel-Poore MP (2007) Endotoxin preconditioning protects against the cytotoxic effects of TNFalpha after stroke: a novel role for TNFalpha in LPS-ischemic tolerance. J Cereb Blood Flow Metab 27:1663-1674 (Pubitemid 47476093)
48. Saldanha A (2004) Java treeview - extensible visualization of microarray data. Bioinformatics 20(17):3246-3248
49. Searle SR, Speed FM, Milliken GA (1980) Population marginal means in the linear model: an alternative to least squares means. Am Stat 34:216-221
50. Sethi T, Rintoul RC, Moore SM, MacKinnon AC, Salter D, Choo C, Chilvers ER, Dransfield I, Donnelly CS, Strieter R, Haslett C (1999) Extracellular matrix proteins protect small lung cancer cells against apoptosis: a mechanism from small cell lung cancer growth and drug resistance. Nat Med 5:662-668 (Pubitemid 29289430)
51. Shen J, Yang M, Ju D, Jiang H, Zheng JP, Xu Z, Li L (2010) Disruption of SM22 promotes inflammation after artery injury via nuclear factor kappaB activation. Circ Res 30;106(8):1351-1362
52. Simon RP, Niiro M, Gwinn R (1993) Prior ischemic stress protects against experimental stroke. Neurosci Lett 163:135-137 (Pubitemid 24005398)
53. Simonian NA, Coyle JT (1996) Oxidative stress in neurodegenerative diseases. Ann Rev Pharmacol Toxicol 36:83-106 (Pubitemid 26168695)
54. Singh DK, Karmakar P, Aamann M, Schurman SH, May A, Croteau DL et al (2010) The involvement of human RECQL4 in DNA double-strand break repair. Aging Cell 9(3):358-371
55. Stenzel-Poore MP, Stevens SL, Xiong Z et al (2003) Effect of ischaemic preconditioning on genomic response to cerebral ischaemia: similarity to neuroprotective strategies in hibernation and hypoxia-tolerant states. Lancet 362:1028-1037 (Pubitemid 37186880)
56. Stenzel-Poore MP, Stevens SL, Simon RP (2004) Genomics of preconditioning. Stroke 35:2683-2686 (Pubitemid 39458368)
57. Talaat AM, Howard ST, Hale W, Lyons R, Garner H, Johnston SA (2002) Genomic DNA standards for gene expression profiling in mycobacterium tuberculosis. Nucleic Acids Res 30:e104
58. Tobita M, Nagano I, Nakamura S, Itoyama Y, Kogure K (1995) DNA single-strand breaks in postischemic gerbil brain detected by in situ nick translation procedure. Neurosci Lett 200:129-132
59. Toker A (2000) Protein kinases as mediators of phosphoinositide 3- kinase signaling. Mol Pharmacol 57:652-658
60. Wang X, Barone FC, Aiyar NV, Feuerstein GZ (1997) Interleukin-1 receptor and receptor antagonist gene expression after focal stroke in rats. Stroke 28:155-161
61. Wang Z, Xue Y, Jiao H, Liu Y, Wang P (2012) Doxycycline-mediated protective effect against focal cerebral ischemia-reperfusion injury through the modulation of tight junctions and PKCδ signaling in rats. J Mol Neurosci. doi:10.1007/s12031-011-9689-x]
62. Watters O, Pickering M, O'Connor JJ (2011) Preconditioning effects of tumor necrosis factor-α and glutamate on calcium dynamics in rat organotypic hippocampal cultures. J Neuroimmunol 234(1):27-39
63. Weih M, Kallenberg K, Bergk A, Dirnagl U, Harms L, Wernecke KD, Einhaupl KM (1999) Attenuated stroke severity after prodromal TIA: a role for ischemic tolerance in the brain? Stroke 30:1851-1854 (Pubitemid 29411826)
64. Wu H, Kerr MK, Cui X, Churchill GA (2003) MAANOVA: a Software package for the analysis of spotted cDNA microarray experiments. In: Parmigiani GGE, Irizarry R, Zeger S (eds) In the analysis of gene expression data: an overview of methods and software. Springer, New York, pp 313-431
65. Yang YH, Dudoit S, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide variation. Nucleic Acids Res 30:1-e15
66. Zhao H (2009) Ischemic postconditioning as a novel avenue to protect against brain injury after stroke. J Cereb Blood Flow Metab 29:873-885
67. Zhao ZQ, Corvera JS, Halkos ME et al (2003) Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol 285:H579-H588 (Pubitemid 36885888)
68. Zhao H, Sapolsky Robert M, Steinberg GK (2006) Interrupting reperfusion as a stroke therapy: ischemic postconditioning reduces infarct size after focal ischemia in rats. J Cereb Blood Flow Metab 26:1114-1121 (Pubitemid 44268173)