Growth-associated gene expression after stroke: Evidence for a growth-promoting region in peri-infarct cortex

Experimental Neurology

Volumn 193, Issue 2, 2005, Pages 291-311

  Carmichael, S Thomas ^a   Archibeque, Ivonne ^a   Luke, Linslee ^a   Nolan, Tim ^a   Momiy, Janneth ^a   Li, Songlin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Barrel cortex; GAP43; Plasticity; Repair; Sprouting

Indexed keywords

AGGRECAN; BRAIN PROTEIN; BREVICAN; CALMODULIN BINDING PROTEIN; CALMODULIN BINDING PROTEIN 23; EPHRIN A5; EPHRIN B1; GROWTH ASSOCIATED PROTEIN; GROWTH INHIBITOR; GROWTH PROMOTOR; L1 PROTEIN; MARCKS PROTEIN; MEMBRANE PROTEIN; NEUROMODULIN; NEUROPILIN 1; PHOSPHACAN; PROTEIN C JUN; PROTEIN P21; PROTEOCHONDROITIN SULFATE; SCG10 PROTEIN; SCLIP PROTEIN; SEMAPHORIN 3A; SMALL PROLINE REPEAT RICH 1 PROTEIN; TUBULIN ALPHA 1 PROTEIN; UNCLASSIFIED DRUG; VERSICAN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN INFARCTION; BRAIN REGION; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION PROFILING; MALE; NERVE CELL PLASTICITY; NERVE FIBER REGENERATION; NERVE SPROUTING; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SOMATOSENSORY CORTEX; STROKE;

EID: 18144416945     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2005.01.004     Document Type: Article

References (91)

1. American Heart Association Heart disease and stroke statistics update 2004 http://www.americanheart.org/presenter.jhtml?identifier=3000090
2. R.A. Asher, D.A. Morgenstern, M.C. Shearer, K.H. Adcock, P. Pesheva, and J.W. Fawcett Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells J. Neurosci. 22 2002 2225 2236
3. A.J. Bean, and T. Hökfelt Production of labeled cRNA probes useful for in situ hybridization histochemistry without vector cloning Z. Hendersen In situ hybridization 1996 Wiley and Sons West Sussex, England 133 140
4. T. Becker, R.R. Bernhardt, F. Reinhard, M.F. Wulliman, E. Tongiorgi, and M. Schachner Readiness of zebrafish brain neurons to regenerate a spinal axon correlates with differential expression of specific cell recognition molecules J. Neurosci. 18 1998 5789 5803
5. L.I. Benowitz, and A. Routtenberg GAP-43: an intrinsic determinant of neuronal development and plasticity Trends Neurosci. 20 1997 84 91
6. L.I. Benowitz, D.E. Goldberg, and N. Irwin Inosine stimulates axon growth in vitro and in the adult CNS Prog. Brain Res. 137 2002 389 399
7. C. Biervert, E. Horvath, and T. Fahrig Semiquantitative expression analysis of ephrine-receptor tyrosine kinase mRNA's in a rat model of traumatic brain injury Neurosci. Lett. 315 2001 25 28
8. J. Bolz, D. Uziel, S. Muhlfriedel, A. Gullmar, C. Peuckert, K. Zarbalis, W. Wurst, M. Toril, and P. Levitt Multiple roles of ephrins during the formation of thalamocortical projections: maps and more J. Neurobiol. 59 2004 82 94
9. H.M. Bomze, K.R. Bulsara, B.J. Iskander, P. Caroni, and J.H. Skene Spinal axon regeneration evoked by replacing two growth cone proteins in adult neurons Nat. Neurosci. 4 2001 38 43
10. I.E. Bonilla, K. Tanabe, and S.M. Strittmatter Small proline-rich repeat protein 1A is expressed by axotomized neurons and promotes axonal outgrowth J. Neurosci. 22 2002 1303 1315
11. E.J. Bradbury, L.D. Moon, R.J. Popat, V.R. King, G.S. Bennett, P.N. Patel, J.W. Fawcett, and S.B. McMahon Chondroitinase ABC promotes functional recovery after spinal cord injury Nature 416 2002 636 640
12. K.R. Bulsara, B.J. Iskandar, A.T. Villavicencio, and J.H. Skene A new millenium for spinal cord regeneration: growth-associated genes Spine 27 2002 1946 1949
13. L.Q. Bundesen, T.A. Scheel, B.S. Bregman, and L.F. Kromer Ephrin-B2 and EphB2 regulation of astrocyte-meningeal fibroblast interactions in response to spinal cord lesions in adult rats J. Neurosci. 23 2003 7789 7800
14. C. Calautti, and J.C. Baron Functional neuroimaging studies of motor recovery after stroke in adults: a review Stroke 34 2003 1553 1566
15. S.T. Carmichael Plasticity of cortical projections after stroke Neuroscientist 9 2003 64 75
16. S.T. Carmichael Gene expression changes after focal stroke, traumatic brain and spinal cord injuries Curr. Opin. Neurol. 16 2003 699 704
17. S.T. Carmichael, and M.F. Chesselet Synchronous neuronal activity is a signal for axonal sprouting after cortical lesions in the adult J. Neurosci. 22 2001 6062 6070
18. S.T. Carmichael, L. Wei, C.M. Rovainen, and T.A. Woolsey New patterns of intra-cortical projections after focal cortical stroke Neurobiol. Dis. 2001 910 922
19. S.T. Carmichael, K. Tatsukawa, D. Katsman, N. Tsuyuguchi, and H.I. Kornblum Evolution of diaschisis in a focal stroke model Stroke 35 2004 758 763
20. P. Caroni Intrinsic neuronal determinants that promote axonal sprouting and elongation BioEssays 19 1997 767 775
21. P. Caroni New EMBO members' review: actin cytoskeleton regulation through modulation of PI(4,5)P(2) rafts EMBO J. 20 2001 4332 4336
22. D. Carulli, A. Buffo, and P. Strata Reparative mechanisms in the cerebellar cortex Prog. Neurobiol. 72 2004 373 398
23. V. Castellani, E. De Angelis, S. Kenwrick, and G. Rougon Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3a EMBO J. 21 2000 6348 6357
24. J.E. Cavazos, G. Golarai, and T.P. Sutula Mossy fiber synaptic reorganization induced by kindling: time course of development, progression, and permanence J. Neurosci. 11 1991 2795 2803
25. M.R. Celio, R. Spreafico, S. De Biasi, and L. Vitellaro-Zuccarello Perineuronal nets: past and present Trends Neurosci. 21 1998 510 515
26. B.D. Chang, K. Watanabe, E.V. Broude, J. Fang, J.C. Poole, T.V. Kalinichenko, and I.B. Roninson Effects of p21 on cellular gene expression: implications for carcinogenesis, senescence, and age-related diseases Proc. Natl. Acad. Sci. U. S. A. 97 2000 4291 4296
27. M.F. Chesselet Quantitative analysis and interpretation of data for in situ hybridization at the cellular level Z. Hendersen In Situ hybridization techniques for the brain 1996 Wiley and Sons West Sussex, England 141 149
28. 35S- and digoxigenin labeled RNA probes Z. Hendersen In situ hybridization techniques for the brain 1996 Wiley and Sons West Sussex, England 70 100
29. M. Costigan, K. Befort, L. Karchewski, R.S. Griffin, D. D'Urso, A. Allchorne, J. Sitarski, J.W. Mannion, R.E. Pratt, and C.J. Woolf Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury BMC Neurosci. 3 2002 16
30. F. De Winter, M. Oudega, A.J. Lankhorst, F.P. Hamers, B. Blits, M.J. Ruitenberg, R.J. Pasterkamp, W.H. Gispen, and J. Verhaagen Injury-induced class 3 semaphorin expression in the rat spinal cord Exp. Neurol. 175 2002 61 175
31. R.M. Dijkhuizen, A.B. Singhal, J.B. Mandeville, O. Wu, E.F. Halpern, S.P. Finklestein, B.R. Rosen, and E.H. Lo Correlation between brain reorganization, ischemic damage, and neurologic status after transient focal cerebral ischemia in rats: a functional magnetic resonance imaging study J. Neurosci. 23 2003 510 517
32. A. Dobbertin, K.E. Rhodes, J. Garwood, F. Properzi, N. Heck, J.H. Rogers, J.W. Fawcett, and A. Faissner Regulation of RPTPbeta/phosphacan expression and glycosaminoglycan epitopes in injured brain and cytokine-treated glia Mol. Cell. Neurosci. 24 2002 951 971
33. R.S. Erzurumlu, S. Jhaveri, and L.I. Benowitz Transient patterns of GAP-43 expression during the formation of barrels in the rat somatosensory cortex J. Comp. Neurol. 292 1990 443 456
34. J.W. Fawcett, and R.A. Asher The glial scar and central nervous system repair Brain Res. Bull. 49 1999 377 391
35. K.J. Fernandes, D.P. Fan, B.J. Tsui, S.L. Cassar, and W. Tetzlaff Influence of the axotomy to cell body distance in rat rubrospinal and spinal motoneurons: differential regulation of GAP-43, tubulins, and neurofilament-M J. Comp. Neurol. 414 1999 495 510
36. Freeman, W.M., Walker, S.J., Vrana, K.E. 1999, Quantitative RT-PCR: pitfalls and potential. Biotechniques 26, 112-122, 124-125.
37. D. Frey, T. Laux, L. Xu, C. Schneider, and P. Caroni Shared and unique roles of CAP23 and GAP43 in actin regulation, neurite outgrowth, and anatomical plasticity J. Cell Biol. 149 2000 1443 1454
38. H. Fujita, B. Zhang, K. Sato, J. Tanaka, and M. Sakanaka Expressions of neuropilin-1, neuropilin-2 and semaphorin 3A mRNA in the rat brain after middle cerebral artery occlusion Brain Res. 914 2001 1 14
39. R. Gregersen, T. Christensen, E. Lehrmann, N.H. Diemer, and B. Finsen Focal cerebral ischemia induces increased myelin basic protein and growth-associated protein-43 gene transcription in peri-infarct areas in the rat brain Exp. Brain Res. 138 2001 384 392
40. G. Grenningloh, S. Soehrman, P. Bondallaz, E. Ruchti, and H. Cadas Role of the microtubule destabilizing proteins SCG10 and stathmin in neuronal growth J. Neurobiol. 58 2004 60 69
41. D.C. Harrison, A.D. Medhurst, B.C. Bond, C.A. Campbell, R.P. Davis, and K.L. Philpott The use of quantitative RT-PCR to measure mRNA expression in a rat model of focal ischemia-caspase-3 as a case study Brain Res., Mol. Brain Res. 75 2000 143 149
42. T. Herdegen, P. Skene, and M. Bahr The c-Jun transcription factor-bipotential mediator of neuronal death, survival and regeneration Trends Neurosci. 20 1997 227 231
43. T. Iwata, K. Namikawa, M. Honma, N. Mori, S. Yachiku, and H. Kiyama Increased expression of mRNAs for microtubule disassembly molecules during nerve regeneration Brain Res., Mol. Brain Res. 102 2002 105 109
44. L.L. Jones, R.U. Margolis, and M.H. Tuszynski The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury Exp. Neurol. 182 2002 399 411
45. M. Jung, B. Petrausch, and C.A. Stuermer Axon-regenerating retinal ganglion cells in adult rats synthesize the cell adhesion molecule L1 but not TAG-1 or SC-1 Mol. Cell. Neurosci. 9 1997 116 131
46. D. Katsman, K. Spinelli, J. Zhang, and S.T. Carmichael Tissue microenvironments within functional cortical subdivisions adjacent to focal stroke J. Cereb. Blood Flow Metab. 23 2003 997 1009
47. T. Kawamata, W.D. Dietrich, T. Schallert, J.E. Gotts, R.R. Cocke, L.I. Benowitz, and S.P. Finklestein Intracisternal basic fibroblast growth factor enhances functional recovery and up-regulates the expression of a molecular marker of neuronal sprouting following focal cerebral infarction Proc. Natl. Acad. Sci. U. S. A. 94 1997 8179 8184
48. T. Laux, K. Fukami, M. Thelen, T. Golub, D. Frey, and P. Caroni GAP43, MARCKS, and CAP23 modulate PI(4,5)P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism J. Cell Biol. 149 2000 1455 1472
49. D.H. Lee, S.M. Strittmatter, and D.W. Sah Targeting the Nogo receptor to treat central nervous system injuries Nat. Rev., Drug Discov. 2 2004 872 878
50. J.K. Lee, J.E. Kim, M. Sivula, and S.M. Strittmatter Nogo receptor antagonism promotes stroke recovery by enhancing axonal plasticity J. Neurosci. 24 2004 6209 6217
51. Li, S., Zheng, J., Carmichel, S.T., in press. Differences in ischemic injury after stroke between aged and young adults. Neurobiol. Dis.
52. D.J. Liebl, C.J. Morris, M. Henkemeyer, and L.F. Parada mRNA expression of ephrins and Eph receptor tyrosine kinases in the neonatal and adult mouse central nervous system J. Neurosci. Res. 71 2003 7 22
53. R.Y. Liu, and W.D. Snider Different signaling pathways mediate regenerative versus developmental sensory axon growth J. Neurosci. 21 2001 RC164
54. A. Lu, Y. Tang, R. Ran, J.F. Clark, B.J. Aronow, and F.R. Sharp Genomics of the periinfarction cortex after focal cerebral ischemia J. Cereb. Blood Flow Metab. 23 2003 786 810
55. M.R. Mason, A.R. Lieberman, G. Grenningloh, and P.N. Anderson Transcriptional upregulation of SCG10 and CAP-23 is correlated with regeneration of the axons of peripheral and central neurons in vivo Mol. Cell. Neurosci. 20 2002 595 615
56. R.T. Matthews, G.M. Kelly, C.A. Zerillo, G. Gray, M. Tiemeyer, and S. Hockfield Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets J. Neurosci. 22 2002 7536 7547
57. R.J. McKeon, M.J. Jurynec, and C.R. Buck The chondroitin sulfate proteoglycans neurocan and phosphacan are expressed by reactive astrocytes in the chronic CNS glial scar J. Neurosci. 19 1999 10778 10788
58. F.D. Miller, and J.W. Geddes Increased expression of the major embryonic alpha-tubulin mRNA, T alpha 1, during neuronal regeneration, sprouting, and in Alzheimer's disease Prog. Brain Res. 86 1990 321 330
59. F.D. Miller, C.C. Naus, M. Durand, F.E. Bloom, and R.J. Milner Isotypes of alpha-tubulin are differentially regulated during neuronal maturation J. Cell Biol. 105 1987 3065 3373
60. L.D. Moon, R.A. Asher, K.E. Rhodes, and J.W. Fawcett Relationship between sprouting axons, proteoglycans and glial cells following unilateral nigostriatal axotomy in the adult rat Neuroscience 109 2002 101 117
61. D.A. Morgenstern, R.A. Asher, and J.W. Fawcett Chondroitin sulphate proteoglycans in the CNS injury response Prog. Brain Res. 137 2002 313 332
62. N. Mori, and H. Morii SCG10-related neuronal growth-associated proteins in neural development, plasticity, degeneration, and aging J. Neurosci. Res. 70 2002 264 273
63. L. Naudon, J.M. Delfs, N. Clavel, J.F. Lorden, and M.F. Chesselet Differential expression of glutamate decarboxylase messenger RNA in cerebellar Purkinje cells and deep cerebellar nuclei of the genetically dystonic rat Neuroscience 82 1998 1087 1094
64. N. Ohba, M. Maeda, S. Nakagomi, M. Muraoka, and H. Kiyama Biphasic expression of activating transcription factor-3 in neurons after cerebral infarction Brain Res., Mol. Brain Res. 115 2003 147 156
65. C.M. Papadopoulos, S.Y. Tsai, T. Alsbiei, T.E. O'Brien, M.E. Schwab, and G.L. Kartje Functional recovery and neuroanatomical plasticity following middle cerebral artery occlusion and IN-1 antibody treatment in the adult rat Ann. Neurol. 51 2002 433 441
66. R.J. Pasterkamp, R.J. Giger, M.J. Ruitenberg, A.J. Holtmaat, J. De Wit, F. De Winter, and J. Verhaagen Expression of the gene encoding the chemorepellent semaphorin III is induced in the fibroblast component of neural scar tissue formed following injuries of adult but not neonatal CNS Mol. Cell. Neurosci. 13 1999 143 166
67. M.W. Pfaffl A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Res. 29 2001 E45 E50
68. M.W. Pfaffl, G.W. Horgan, and L. Dempfle Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR Nucleic Acids Res. 30 2002 e36
69. T. Pizzorusso, P. Medini, N. Berardi, S. Chierzi, J.W. Fawcett, and L. Maffei Reactivation of ocular dominance plasticity in the adult visual cortex Science 298 2002 1248 1251
70. A.M. Planas, S. Sole, and C. Justicia Expression and activation of matrix metalloproteinase-2 and -9 in rat brain after transient focal cerebral ischemia Neurobiol. Dis. 8 1998 834 846
71. W. Plunet, B.K. Kwon, and W. Tetzlaff Promoting axonal regeneration in the central nervous system by enhancing the cell body response to axotomy J. Neurosci. Res. 68 2002 1 6
72. G. Raivich, M. Bohatschek, C. Da Costa, O. Iwata, M. Galiano, M. Hristova, A.S. Nateri, M. Makwana, L. Riera-Sans, D.P. Wolfer, H.P. Lipp, A. Aguzzi, E.F. Wagner, and A. Behrens The AP-1 transcription factor c-Jun is required for efficient axonal regeneration Neuron 43 2004 57 67
73. I.B. Roninson Oncogenic functions of tumour suppressor p21: association with cell senescence and tumour-promoting activities of stromal fibroblasts Cancer Lett. 170 2002 1 14
74. G.A. Rosenberg Matrix metalloproteinases in neuroinflammation Glia 39 2002 279 291
75. A. Sandvig, M. Berry, L.B. Barrett, A. Butt, and A. Logan Myelin-, reactive glia-, and scar-derived CNS axon growth inhibitors: expression, receptor signaling, and correlation with axon regeneration Glia 46 2004 225 251
76. R. Schmidt-Kastner, J. Truettner, W. Zhao, L. Belayev, C. Krieger, R. Busto, and M.D. Ginsberg Differential changes of bax, caspase-3 and p21 mRNA expression after transient focal brain ischemia in the rat Brain Res., Mol. Brain Res. 79 2000 88 101
77. A.B. Schmitt, S. Breuer, J. Liman, A. Buss, C. Schlangen, K. Pech, E.M. Hol, G.A. Brook, J. Noth, and F.W. Schwaiger Identification of regeneration-associated genes after central and peripheral nerve injury in the adult rat BMC Neurosci. 4 2003 8
78. J. Silver, and J.H. Miller Regeneration beyond the glial scar Nat. Rev., Neurosci. 5 2004 146 156
79. J.M. Sorrell, D.A. Carrino, and A.I. Caplan Structural domains in chondroitin sulfate identified by anti-chondroitin sulfate monoclonal antibodies. Immunosequencing of chondroitin sulfates Matrix 13 1993 351 361
80. O. Steward, S.L. Vinsant, and L. Davis The process of reinnervation in the dentate gyrus of adult rats: an ultrastructural study of changes in presynaptic terminals as a result of sprouting J. Comp. Neurol. 267 1988 203 210
81. R.P. Stroemer, T.A. Kent, and C.E. Hulsebosch Neocortical neural sprouting, synaptogenesis, and behavioral recovery after neocortical infarction in rats Stroke 26 1995 2135 2144
82. K. Tanabe, I. Bonilla, J.A. Winkles, and S.M. Strittmatter Fibroblast growth factor-inducible-14 is induced in axotomized neurons and promotes neurite outgrowth J. Neurosci. 23 2003 9675 9686
83. W. Tetzlaff, N.R. Kobayashi, K.M. Giehl, B.J. Tsui, S.L. Cassar, and A.M. Bedard Response of rubrospinal and corticospinal neurons to injury and neurotrophins Prog. Brain Res. 103 1994 271 286
84. N. Thon, C.A. Haas, U. Rauch, T. Merten, R. Fassler, M. Frotscher, and T. Deller The chondroitin sulphate proteoglycan brevican is upregulated by astrocytes after entorhinal cortex lesions in adult rats Eur. J. Neurosci. 12 2000 2547 2558
85. P. Vanderhaeghen, Q. Lu, N. Prakash, J. Frisen, C.A. Walsh, R.D. Frostig, and J.G. Flanagan A mapping label required for normal scale of body representation in the cortex Nat. Neurosci. 3 2000 358 365
86. M. van Lookeren Campagne, and R. Gill Tumor-suppressor p53 is expressed in proliferating and newly formed neurons of the embryonic and postnatal rat brain: comparison with expression of the cell cycle regulators p21Waf1/Cip1, p27Kip1, p57Kip2, p16Ink4a, cyclin G1, and the proto-oncogene Bax J. Comp. Neurol. 397 1998 181 198
87. F.S. Walsh, and P. Dougherty Neural cell adhesion molecules of the immunoglobulin superfamily: role in axon growth and guidance Annu. Rev. Cell Dev. Biol. 13 1999 425 456
88. F. Wegner, W. Hartig, A. Bringmann, J. Groshe, K. Wohlfarth, W. Zuschratter, and G. Brcukner Diffuse perineuronal nets and modified pyramidal cells immunoreactive for glutamate and the GABA(A) receptor alpha1 subunit form a unique entity in rat cerebral cortex Exp. Neurol. 184 2003 705 714
89. J. Wilhelm, and A. Pingoud Real-time polymerase chain reaction ChemBioChem 4 2003 1120 1128
90. C.A. Willson, J.D. Miranda, R.D. Foster, S.M. Onifer, and S.R. Whittemore Transection of the adult rat spinal cord upregulates EphB3 receptor and ligand expression Cell Transplant. 12 2003 279 290
91. M. Zagrebelsky, A. Buffo, A. Skerra, M.E. Schwab, P. Strata, and F. Rossi Retrograde regulation of growth-associated gene expression in adult rat Purkinje cells by myelin-associated neurite growth inhibitory proteins J. Neurosci. 18 1998 7912 7929