Comprehensive regional and temporal gene expression profiling of the rat brain during the first 24 h after experimental stroke identifies dynamic ischemia-induced gene expression patterns, and reveals a biphasic activation of genes in surviving tissue

Journal of Neurochemistry

Volumn 96, Issue 1, 2006, Pages 14-29

  Rickhag, Mattias ^a   Wieloch, Tadeusz ^a   Gidö, Gunilla ^a   Elmér, Eskil ^a   Krogh, Morten ^c   Murray, Joseph ^b,d   Lohr, Scott ^b,d   Bitter, Hans ^b,d   Chin, Daniel J ^b,f   Von Schack, David ^b,e   Shamloo, Mehrdad ^b   Nikolich, Karoly ^b  

^a LUND UNIVERSITY   (Sweden)

^b AGY Therapeutics Inc   (United States)

^c LUND UNIVERSITY   (Sweden)

^d Predicant Biosciences   (United States)

^e PFIZER INC   (United States)

^f Roche   (United States)

Author keywords

Chaperone; Cluster analysis; G protein; Gene expression profiling; Ischemia; Myelin

Indexed keywords

APOLIPOPROTEIN D; BRAIN DERIVED NEUROTROPHIC FACTOR; CHLORIDE CHANNEL; CHOLINE KINASE; COMPLEMENTARY DNA; G PROTEIN COUPLED RECEPTOR; GLUCOSE 3 PHOSPHATE DEHYDROGENASE 1; MITOGEN ACTIVATED PROTEIN KINASE; NIEMANN PICK TYPE C1 PROTEIN; OXIDOREDUCTASE; PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION; BRAIN ISCHEMIA; CELL DEATH; CELL MOTILITY; CELL SURVIVAL; DNA MICROARRAY; GENE ACTIVATION; GENE CLUSTER; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE INDUCTION; IMMEDIATE EARLY GENE; IN SITU HYBRIDIZATION; LIPOGENESIS; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASTICITY; PRIORITY JOURNAL; RAT; REPERFUSION; SIGNAL TRANSDUCTION; STROKE; TRANSCRIPTION REGULATION; UNINDEXED SEQUENCE; ANIMAL; AUTORADIOGRAPHY; BIOSYNTHESIS; BRAIN; BRAIN LEVEL; CELL PROLIFERATION; CEREBRAL ARTERY DISEASE; CEREBROVASCULAR ACCIDENT; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MULTIGENE FAMILY; NERVE CELL PLASTICITY; NERVE REGENERATION; PATHOLOGY; PHYSIOLOGY; SYNAPSE; WISTAR RAT;

ANIMALIA;

ANIMALS; AUTORADIOGRAPHY; BRAIN; BRAIN CHEMISTRY; BRAIN ISCHEMIA; CELL PROLIFERATION; CELL SURVIVAL; CEREBROVASCULAR ACCIDENT; DNA, COMPLEMENTARY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IN SITU HYBRIDIZATION; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MULTIGENE FAMILY; NERVE REGENERATION; NEURONAL PLASTICITY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RATS, WISTAR; RNA; SYNAPSES;

EID: 33644834481     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03508.x     Document Type: Article

References (85)

1. Akins PT. Liu PK. Hsu CY. 1996 Immediate early gene expression in response to cerebral ischemia. Friend or foe? Stroke 27 1682 1687
2. Anelli T. Alessio M. Mezghrani A. Simmen T. Talamo F. Bachi A. Sitia R. 2002 ERp44, a novel endoplasmic reticulum folding assistant of the thioredoxin family EMBO J 21 835 844
3. Bando Y. Katayama T. Kasai K. Taniguchi M. Tamatani M. Tohyama M. 2003 GRP94 (94 kDa glucose-regulated protein) suppresses ischemic neuronal cell death against ischemia/reperfusion injury EurJNeurosci 18 829 840
4. Bederson JB. Pitts LH. Tsuji M. Nishimura MC. Davis RL. Bartkowski H. 1986a Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination Stroke 17 472 476
5. Bederson JB. Pitts LH. Germano SM. Nishimura MC. Davis RL. Bartkowski HM. 1986b Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats Stroke 17 1304 1308
6. Bengtsson L. Wilson K. L. 2004 Multiple and surprising new functions for emerin, a nuclear membrane protein CurrOpin. Cell Biol 16 73 79
7. Berditchevski F. Odintsova E. 1999 Characterization of integrin-tetraspanin adhesion complexes: role of tetraspanins in integrin signaling JCell Biol 146 477 492
8. Boris-Moller F. Kamme F. Wieloch T. 1998 The effect of hypothermia on the expression of neurotrophin mRNA in the hippocampus following transient cerebral ischemia in the rat Brain ResMolBrain Res 63 163 173
9. Bradbury A. Possenti R. Shooter EM. Tirone F. 1991 Molecular cloning of PC3, a putatively secreted protein whose mRNA is induced by nerve growth factor and depolarization ProcNatl AcadSciUSA 88 3353 3357
10. Brannvall K. Hjelm H. Korhonen L. Lahtinen U. Lehesjoki AE. Lindholm D. 2003 Cystatin-B is expressed by neural stem cells and by differentiated neurons and astrocytes BiochemBiophysResCommun 308 369 374
11. Chen Y. Ghosh A. 2005 Regulation of dendritic development by neuronal activity JNeurobiol 64 4 10
12. Diatchenko L. Lau YF. Campbell AP. et al. 1996 Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries ProcNatl AcadSciUSA 93 6025 6030
13. Dirnagl U. Iadecola C. Moskowitz MA. 1999 Pathobiology of ischaemic stroke: an integrated view Trends Neurosci 22 391 397
14. Eiraku M. Hirata Y. Takeshima H. Hirano T. Kengaku M. 2002 Delta/notch-like epidermal growth factor (EGF)-related receptor, a novel EGF-like repeat-containing protein targeted to dendrites of developing and adult central nervous system neurons JBiolChem 277 25 400 25 407
15. Espinosa de los Monteros A. Kumar S. Zhao P. Huang CJ. Nazarian R. Pan T. Scully S. Chang R. de Vellis J. 1999 Transferrin is an essential factor for myelination NeurochemRes 24 235 248
16. Feldman JD. Vician L. Crispino M. Tocco G. Marcheselli VL. Bazan NG. Baudry M. Herschman HR. 1998 KID-1, a protein kinase induced by depolarization in brain JBiolChem 273 16535 16543
17. Franz G. Reindl M. Patel SC. Beer R. Unterrichter I. Berger T. Schmutzhard E. Poewe W. Kampfl A. 1999 Increased expression of apolipoprotein D following experimental traumatic brain injury JNeurochem 73 1615 1625
18. Gilad GM. Gilad VH. 1981 Increased choline kinase activity in the rat superior cervical ganglion after axonal injury Brain Res 220 420 426
19. Gold SJ. Heifets BD. Pudiak CM. Potts BW. Nestler EJ. 2002 Regulation of regulators of G protein signaling mRNA expression in rat brain by acute and chronic electroconvulsive seizures JNeurochem 82 828 838
20. Griffin LD. Gong W. Verot L. Mellon SH. 2004 Niemann-Pick type C disease involves disrupted neurosteroidogenesis and responds to allopregnanolone NatMed 10 704 711
21. Hagen T. Lagace CJ. Modica-Napolitano JS. Aprille JR. 2003 Permeability transition in rat liver mitochondria is modulated by the ATP-Mg/Pi carrier AmJPhysiolGastrointestLiver Physiol 285 G274 G281
22. Hamann GF. Liebetrau M. Martens H. Burggraf D. Kloss CU. Bultemeier G. Wunderlich N. Jager G. Pfefferkorn T. 2002 Microvascular basal lamina injury after experimental focal cerebral ischemia and reperfusion in the rat JCerebBlood Flow Metab 22 526 533
23. Hartigan JA. Wong MA. 1979 A K-Means Clustering Algorithm ApplStat 28 100 108
24. Hartings JA. Rolli ML. Lu XC. Tortella FC. 2003 Delayed secondary phase of peri-infarct depolarizations after focal cerebral ischemia: relation to infarct growth and neuroprotection JNeurosci 23 11 602 11 610
25. Herdegen T. Leah JD. 1998 Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins Brain ResBrain ResRev 28 370 490
26. Kamme F. Campbell K. Wieloch T. 1995 Biphasic expression of the fos and jun families of transcription factors following transient forebrain ischaemia in the rat. Effect Hypothermia EurJNeurosci 7 2007 2016
27. Kato H. Liu Y. Kogure K. Kato K. 1994 Induction of 27-kDa heat shock protein following cerebral ischemia in a rat model of ischemic tolerance Brain Res 634 235 244
28. Kaufmann WE. Worley PF. Pegg J. Bremer M. Isakson P. 1996 COX-2, a synaptically induced enzyme, is expressed by excitatory neurons at postsynaptic sites in rat cerebral cortex ProcNatl AcadSciUSA 93 2317 2321
29. Kim H. Huh PW. Kim C. Kim YJ. Park EM. Park YM. 2001 Cerebral activation and distribution of inducible hsp110 and hsp70 mRNAs following focal ischemia in rat Toxicology 167 135 144
30. Kim YD. Sohn NW. Kang C. Soh Y. 2002 DNA array reveals altered gene expression in response to focal cerebral ischemia Brain ResBull 58 491 498
31. Kinouchi H. Sharp FR. Chan PH. Koistinaho J. Sagar SM. Yoshimoto T. 1994 Induction of NGFI-A mRNA following middle cerebral artery occlusion in rats: in situ hybridization study NeurosciLett 171 163 166
32. Kitano J. Kimura K. Yamazaki Y. Soda T. Shigemoto R. Nakajima Y. Nakanishi S. 2002 Tamalin, a PDZ domain-containing protein, links a protein complex formation of group 1 metabotropic glutamate receptors and the guanine nucleotide exchange factor cytohesins JNeurosci 22 1280 1289
33. Knoblach B. Keller BO. Groenendyk J. Aldred S. Zheng J. Lemire BD. Li L. Michalak M. 2003 ERp19 and ERp46, New Members of the Thioredoxin Family of Endoplasmic Reticulum Proteins MolCellProteomics 2 1104 1119
34. Kokaia Z. Zhao Q. Kokaia M. Elmer E. Metsis M. Smith ML. Siesjo BK. Lindvall O. 1995 Regulation of brain-derived neurotrophic factor gene expression after transient middle cerebral artery occlusion with and without brain damage ExpNeurol 136 73 88
35. Kunizuka H. Kinouchi H. Arai S. Izaki K. Mikawa S. Kamii H. Sugawara T. Suzuki A. Mizoi K. Yoshimoto T. 1999 Activation of Arc gene, a dendritic immediate early gene, by middle cerebral artery occlusion in rat brain Neuroreport 10 1717 1722
36. Kury P. Schroeter M. Jander S. 2004 Transcriptional response to circumscribed cortical brain ischemia: spatiotemporal patterns in ischemic vs. remote non-ischemic cortex EurJNeurosci 19 1708 1720
37. Lee SK. Kim YS. Lee SS. Lee YJ. Song IS. Park SC. Kozak C. Yamada Y. 2004 Molecular cloning, chromosomal mapping, and characteristic expression in tooth organ of rat and mouse Krox-25 Genomics 83 243 253
38. Lidman O. Olsson T. Piehl F. 1999 Expression of nonclassical MHC class I (RT1-U) in certain neuronal populations of the central nervous system EurJNeurosci 11 4468 4472
39. Liu Y. Han SS. Wu Y. Tuohy TM. Xue H. Cai J. Back SA. Sherman LS. Fischer I. Rao MS. 2004 CD44 expression identifies astrocyte-restricted precursor cells DevBiol 276 31 46
40. Lu A. Tang Y. Ran R. Clark JF. Aronow BJ. Sharp FR. 2003 Genomics of the periinfarction cortex after focal cerebral ischemia JCerebBlood Flow Metab 23 786 810
41. Lu XC. Williams AJ. Yao C. et al. 2004 Microarray analysis of acute and delayed gene expression profile in rats after focal ischemic brain injury and reperfusion JNeurosciRes 77 843 857
42. Memezawa H. Minamisawa H. Smith ML. Siesjo BK. 1992 Ischemic penumbra in a model of reversible middle cerebral artery occlusion in the rat ExpBrain Res 89 67 78
43. Milbrandt J. 1987 A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor Science 238 797 799
44. Moon C. Ahn M. Kim S. Jin JK. Sim KB. Kim HM. Lee MY. Shin T. 2004 Temporal patterns of the embryonic intermediate filaments nestin and vimentin expression in the cerebral cortex of adult rats after cryoinjury Brain Res 1028 238 242
45. Nakano H. 2004 Signaling crosstalk between NF-kappaB and JNK Trends Immunol 25 402 405
46. Namura S. Iihara K. Takami S. Nagata I. Kikuchi H. Matsushita K. Moskowitz MA. Bonventre JV. Alessandrini A. 2001 Intravenous administration of MEK inhibitor U0126 affords brain protection against forebrain ischemia and focal cerebral ischemia ProcNatl AcadSciUSA 98 11 569 11 574
47. Nguyen NH. Brathe A. Hassel B. 2003 Neuronal uptake and metabolism of glycerol and the neuronal expression of mitochondrial glycerol-3-phosphate dehydrogenase JNeurochem 85 831 842
48. Ozaki K. Kadomoto R. Asato K. Tanimura S. Itoh N. Kohno M. 2001 ERK pathway positively regulates the expression of Sprouty genes BiochemBiophysResCommun 285 1084 1088
49. Raghavendra Rao VL. Bowen KK. Dhodda VK. Song G. Franklin JL. Gavva NR. Dempsey RJ. 2002 Gene expression analysis of spontaneously hypertensive rat cerebral cortex following transient focal cerebral ischemia JNeurochem 83 1072 1086
50. Robbins M. J. Charles K. J. Harrison DC. Pangalos M. N. 2002 Localisation of the GPRC5B receptor in the rat brain and spinal cord Brain ResMol. Brain Res 106 136 144
51. Roth A. Gill R. Certa U. 2003 Temporal and spatial gene expression patterns after experimental stroke in a rat model and characterization of PC4, a potential regulator of transcription MolCellNeurosci 22 353 364
52. Rubin C. Zwang Y. Vaisman N. Ron D. Yarden Y. 2005 Phosphorylation of carboxyl-terminal tyrosines modulates the specificity of Sprouty-2 inhibition of different signaling pathways JBiolChem 280 9735 9744
53. Ryser S. Massiha A. Piuz I. Schlegel W. 2004 Stimulated initiation of mitogen-activated protein kinase phosphatase-1 (MKP-1) gene transcription involves the synergistic action of multiple cis-acting elements in the proximal promoter BiochemJ 378 473 484
54. Sakamoto K. Yamasaki Y. Kaneto H. Fujitani Y. Matsuoka T. Yoshioka R. Tagawa T. Matsuhisa M. Kajimoto Y. Hori M. 1999 Identification of oxidative stress-regulated genes in rat aortic smooth muscle cells by suppression subtractive hybridization FEBS Lett 461 47 51
55. Salin H. Maurin Y. Davis S. Laroche S. Mallet J. Dumas S. 2002 Spatio-temporal heterogeneity and cell-specificity of long-term potentiation-induced mRNA expression in the dentate gyrus in vivo Neuroscience 110 227 236
56. Schmidt-Kastner R. Zhang B. Belayev L. Khoutorova L. Amin R. Busto R. Ginsberg MD. 2002 DNA microarray analysis of cortical gene expression during early recirculation after focal brain ischemia in rat Brain ResMolBrain Res 108 81 93
57. Schneider A. Fischer A. Kruger C. Aronowski J. 2004 Identification of regulated genes during transient cortical ischemia in mice by restriction-mediated differential display (RMDD) Brain ResMolBrain Res 124 20 28
58. Schubert M. Brazil DP. Burks DJ. et al. 2003 Insulin receptor substrate-2 deficiency impairs brain growth and promotes tau phosphorylation JNeurosci 23 7084 7092
59. Selvaraju R. Bernasconi L. Losberger C. et al. 2004 Osteopontin is upregulated during in vivo demyelination and remyelination and enhances myelin formation in vitro MolCellNeurosci 25 707 721
60. Sharp FR. Lu A. Tang Y. Millhorn DE. 2000 Multiple molecular penumbras after focal cerebral ischemia JCerebBlood Flow Metab 20 1011 1032
61. Shimano H. 2001 Sterol regulatory element-binding proteins (SREBPs): transcriptional regulators of lipid synthetic genes ProgLipid Res 40 439 452
62. Siesjo BK. 1992 Pathophysiology and treatment of focal cerebral ischemia. Part I: Pathophysiology JNeurosurg 77 169 184
63. Sok J. Calfon M. Lu J. Lichtlen P. Clark SG. Ron D. 2001 Arsenite-inducible RNA-associated protein (AIRAP) protects cells from arsenite toxicity Cell Stress Chaperones 6 6 15
64. Soriano MA. Tessier M. Certa U. Gill R. 2000 Parallel gene expression monitoring using oligonucleotide probe arrays of multiple transcripts with an animal model of focal ischemia JCerebBlood Flow Metab 20 1045 1055
65. Suh KS. Mutoh M. Gerdes M. et al. 2005 Antisense suppression of the chloride intracellular channel family induces apoptosis, enhances tumor necrosis factor {alpha}-induced apoptosis, and inhibits tumor growth Cancer Res 65 562 571
66. Suzuki S. Tanaka K. Nogawa S. Dembo T. Kosakai A. Fukuuchi Y. 2001 Phosphorylation of signal transducer and activator of transcription-3 (Stat3) after focal cerebral ischemia in rats ExpNeurol 170 63 71
67. Takano S. Fukuyama H. Fukumoto M. Hirashimizu K. Higuchi T. Takenawa J. Nakayama H. Kimura J. Fujita J. 1995 Induction of CL100 protein tyrosine phosphatase following transient forebrain ischemia in the rat brain JCerebBlood Flow Metab 15 33 41
68. Takeda A. Onodera H. Sugimoto A. Itoyama Y. Kogure K. Shibahara S. 1994 Increased expression of heme oxygenase mRNA in rat brain following transient forebrain ischemia Brain Res 666 120 124
69. Thomas U. 2002 Modulation of synaptic signalling complexes by Homer proteins JNeurochem 81 407 413
70. Tohyama K. Kusuhara H. Sugiyama Y. 2004 Involvement of multispecific organic anion transporter, Oatp14 (Slc21a14), in the transport of thyroxine across the blood-brain barrier Endocrinology 145 4384 4391
71. Van Beek J. Chan P. Bernaudin M. Petit E. MacKenzie ET. Fontaine M. 2000 Glial responses, clusterin, and complement in permanent focal cerebral ischemia in the mouse Glia 31 39 50
72. Wada H. Kobayashi I. Yamaza H. Matsuo K. Kiyoshima T. Akhtar M. Sakai T. Koyano K. Sakai H. 2002 In situ expression of heat shock proteins, Hsc73, Hsj2 and Hsp86 in the developing tooth germ of mouse lower first molar HistochemJ 34 105 109
73. Wang S. Longo FM. Chen J. Butman M. Graham SH. Haglid KG. Sharp FR. 1993 Induction of glucose regulated protein (grp78) and inducible heat shock protein (hsp70) mRNAs in rat brain after kainic acid seizures and focal ischemia NeurochemInt 23 575 582
74. Wang K. Bekar LK. Furber K. Walz W. 2004 Vimentin-expressing proximal reactive astrocytes correlate with migration rather than proliferation following focal brain injury Brain Res 1024 193 202
75. Wieloch T. 2002 Molecular mechanisms of ischemic brain damage, In Cerebral Blood Flow and Metabolism Edvinsson L. Krause DN., eds), pp. 423 451 Lippincott Williams & Wilkins Philadelphia, USA
76. Wu X. Zhu D. Jiang X. Okagaki P. Mearow K. Zhu G. McCall S. Banaudha K. Lipsky RH. Marini AM. 2004 AMPA protects cultured neurons against glutamate excitotoxicity through a phosphatidylinositol 3-kinase-dependent activation in extracellular signal-regulated kinase to upregulate BDNF gene expression JNeurochem 90 807 818
77. Xu D. Hopf C. Reddy R. Cho RW. Guo L. Lanahan A. Petralia RS. Wenthold RJ. O'Brien RJ. Worley P. 2003 Narp and NP1 form heterocomplexes that function in developmental and activity-dependent synaptic plasticity Neuron 39 513 528
78. Yabe D. Nakamura T. Kanazawa N. Tashiro K. Honjo T. 1997 Calumenin, a Ca2+-binding protein retained in the endoplasmic reticulum with a novel carboxyl-terminal sequence, HDEF JBiolChem 272 18 232 18 239
79. Yamada M. Ohnishi H. Sano S. Nakatani A. Ikeuchi T. Hatanaka H. 1997 Insulin receptor substrate (IRS)-1 and IRS-2 are tyrosine-phosphorylated and associated with phosphatidylinositol 3-kinase in response to brain-derived neurotrophic factor in cultured cerebral cortical neurons JBiolChem 272 30 334 30 339
80. Yepes M. Brown SA. Moore EG. Smith EP. Lawrence DA. Winkles JA. 2005 A soluble fn14-fc decoy receptor reduces infarct Volume in a murine model of cerebral ischemia AmJPathol 166 511 520
81. Zafra F. Hengerer B. Leibrock J. Thoenen H. Lindholm D. 1990 Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors EMBO J 9 3545 3550
82. Zhan XL. Clemens JC. Neves G. Hattori D. Flanagan JJ. Hummel T. Vasconcelos ML. Chess A. Zipursky SL. 2004 Analysis of Dscam diversity in regulating axon guidance in Drosophila mushroom bodies Neuron 43 673 686
83. Zhang G. Ghosh S. 2002 Negative regulation of toll-like receptor-mediated signaling by Tollip JBiolChem 277 7059 7065
84. Zhao Q. Memezawa H. Smith ML. Siesjo BK. 1994 Hyperthermia complicates middle cerebral artery occlusion induced by an intraluminal filament Brain Res 649 253 259
85. Zhu D. Wu X. Strauss KI. Lipsky RH. Qureshi Z. Terhakopian A. Novelli A. Banaudha K. Marini AM. 2005 N-methyl- d -aspartate and TrkB receptors protect neurons against glutamate excitotoxicity through an extracellular signal-regulated kinase pathway JNeurosciRes 80 104 113