Delayed treatment with chondroitinase ABC promotes sensorimotor recovery and plasticity after stroke in aged rats

Brain

Volumn 135, Issue 4, 2012, Pages 1210-1223

  Soleman, Sara ^a   Yip, Ping K ^a,b   Duricki, Denise A ^a   Moon, Lawrence D F ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

ageing; chondroitin sulphate proteoglycans; perineuronal nets; plasticity; stroke

Indexed keywords

CHONDROITIN ABC LYASE; CHONDROITIN SULFATE;

AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATROPHY; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; CONVALESCENCE; DRUG EFFICACY; EXTRACELLULAR MATRIX; FEMALE; FOREFOOT; LEG MOVEMENT; MALE; MICROINJECTION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE SPROUTING; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PYRAMIDAL TRACT; RAT; SENSORIMOTOR FUNCTION; TACTILE DISCRIMINATION; TACTILE STIMULATION;

EID: 84860132066     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aws027     Document Type: Article

References (65)

1. Adkins DL, Voorhies AC, Jones TA. Behavioral and neuroplastic effects of focal endothelin-1 induced sensorimotor cortex lesions. Neuroscience 2004; 128: 473-86. (Pubitemid 39294571)
2. Alilain WJ, Horn KP, Hu H, Dick TE, Silver J. Functional regeneration of respiratory pathways after spinal cord injury. Nature 2011; 475: 196-200.
3. Badan I, Buchhold B, Hamm A, Gratz M, Walker LC, Platt D, et al. Accelerated glial reactivity to stroke in aged rats correlates with reduced functional recovery. J Cereb Blood Flow Metab 2003; 23: 845-54. (Pubitemid 36818692)
4. Barritt AW, Davies M, Marchand F, Hartley R, Grist J, Yip P, et al. Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury. J Neurosci 2006; 26: 10856-67.
5. Biernaskie J, Corbett D. Enriched rehabilitative training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury. J Neurosci 2001; 21: 5272-80. (Pubitemid 32622952)
6. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002; 416: 636-40. (Pubitemid 34406764)
7. Brott T, Marler JR, Olinger CP, Adams HP Jr, Tomsick T, Barsan WG, et al. Measurements of acute cerebral infarction: lesion size by computed tomography. Stroke 1989; 20: 871-5. (Pubitemid 19188241)
8. Buchan AM, Slivka A, Xue D. The effect of the NMDA receptor antagonist MK-801 on cerebral blood flow and infarct volume in experimental focal stroke. Brain Res 1992; 574: 171-7.
9. Cafferty WB, Bradbury EJ, Lidierth M, Jones M, Duffy PJ, Pezet S, et al. Chondroitinase ABC-mediated plasticity of spinal sensory function. J Neurosci 2008; 28: 11998-2009.
10. Carey LM, Matyas TA, Oke LE. Sensory loss in stroke patients: effective training of tactile and proprioceptive discrimination. Arch Phys Med Rehabil 1993; 74: 602-11. (Pubitemid 23172762)
11. Carmel JB, Berrol LJ, Brus-Ramer M, Martin JH. Chronic electrical stimulation of the intact corticospinal system after unilateral injury restores skilled locomotor control and promotes spinal axon outgrowth. J Neurosci 2010; 30: 10918-26.
12. Carmichael ST. Plasticity of cortical projections after stroke. Neuroscientist 2003; 9: 64-75. (Pubitemid 36139580)
13. Carmichael ST. Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx 2005; 2: 396-409. (Pubitemid 41444874)
14. Carmichael ST, Archibeque I, Luke L, Nolan T, Momiy J, Li S. Growth-associated gene expression after stroke: evidence for a growth-promoting region in peri-infarct cortex. Exp Neurol 2005; 193: 291-311. (Pubitemid 40616180)
15. Carter LM, Starkey ML, Akrimi SF, Davies M, McMahon SB, Bradbury EJ. The yellow fluorescent protein (YFP-H) mouse reveals neuroprotection as a novel mechanism underlying chondroitinase ABC-mediated repair after spinal cord injury. J Neurosci 2008; 28: 14107-20.
16. Carulli D, Pizzorusso T, Kwok JC, Putignano E, Poli A, Forostyak S, et al. Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 2010; 133: 2331-47.
17. Chen P, Goldberg DE, Kolb B, Lanser M, Benowitz LI. Inosine induces axonal rewiring and improves behavioral outcome after stroke. Proc Natl Acad Sci USA 2002; 99: 9031-6. (Pubitemid 34693678)
18. Clarkson AN, Huang BS, Macisaac SE, Mody I, Carmichael ST. Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature 2010; 468: 305-9.
19. Cramer SC. Repairing the human brain after stroke: I. Mechanisms of spontaneous recovery. Ann Neurol 2008; 63: 272-87. (Pubitemid 351499857)
20. Cramer SC, Nelles G, Schaechter JD, Kaplan JD, Finklestein SP. Computerized measurement of motor performance after stroke. Stroke 1997; 28: 2162-8. (Pubitemid 27497916)
21. Dancause N, Barbay S, Frost SB, Plautz EJ, Chen D, Zoubina EV, et al. Extensive cortical rewiring after brain injury. J Neurosci 2005; 25: 10167-79. (Pubitemid 41636213)
22. Di Carlo A. Human and economic burden of stroke. Age Ageing 2009; 38: 4-5.
23. Dijkhuizen RM, Singhal AB, Mandeville JB, Wu O, Halpern EF, Finklestein SP, et al. Correlation between brain reorganization, ischemic damage, and neurologic status after transient focal cerebral ischemia in rats: a functional magnetic resonance imaging study. J Neurosci 2003; 23: 510-7. (Pubitemid 36139550)
24. Dobkin BH. Strategies for stroke rehabilitation. Lancet Neurol 2004; 3: 528-36. (Pubitemid 39489836)
25. Enright LE, Zhang S, Murphy TH. Fine mapping of the spatial relationship between acute ischemia and dendritic structure indicates selective vulnerability of layer V neuron dendritic tufts within single neurons in vivo. J Cereb Blood Flow Metab 2007; 27: 1185-200. (Pubitemid 46808709)
26. Fisher M, Albers GW, Donnan GA, Furlan AJ, Grotta JC, Kidwell CS, et al. Enhancing the development and approval of acute stroke therapies: Stroke Therapy Academic Industry roundtable. Stroke 2005; 36: 1808-13. (Pubitemid 41098783)
27. Fisher M, Ratan R. New perspectives on developing acute stroke therapy. Ann Neurol 2003; 53: 10-20. (Pubitemid 36083824)
28. Galtrey CM, Asher RA, Nothias F, Fawcett JW. Promoting plasticity in the spinal cord with chondroitinase improves functional recovery after peripheral nerve repair. Brain 2007; 130: 926-39. (Pubitemid 47355587)
29. Garcia-Alias G, Barkhuysen S, Buckle M, Fawcett JW. Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat Neurosci 2009; 12: 1145-51.
30. Hsu JE, Jones TA. Time-sensitive enhancement of motor learning with the less-affected forelimb after unilateral sensorimotor cortex lesions in rats. Eur J Neurosci 2005; 22: 2069-80. (Pubitemid 41579395)
31. Hsu JE, Jones TA. Contralesional neural plasticity and functional changes in the less-affected forelimb after large and small cortical infarcts in rats. Exp Neurol 2006; 201: 479-94. (Pubitemid 44344241)
32. Hunanyan AS, Garcia-Alias G, Alessi V, Levine JM, Fawcett JW, Mendell LM, et al. Role of chondroitin sulfate proteoglycans in axonal conduction in Mammalian spinal cord. J Neurosci 2010; 30: 7761-9.
33. Jones TA, Schallert T. Overgrowth and pruning of dendrites in adult rats recovering from neocortical damage. Brain Res 1992; 581: 156-60.
34. Kelly-Hayes M, Beiser A, Kase CS, Scaramucci A, D'Agostino RB, Wolf PA. The influence of gender and age on disability following ischemic stroke: the Framingham study. J Stroke Cerebrovasc Dis 2003; 12: 119-26. (Pubitemid 36870484)
35. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. J Pharmacol Pharmacother 2010; 1: 94-9.
36. Lee JK, Geoffroy CG, Chan AF, Tolentino KE, Crawford MJ, Leal MA, et al. Assessing spinal axon regeneration and sprouting in Nogo-, MAG-, and OMgp-deficient mice. Neuron 2010; 66: 663-70.
37. Lee JK, Kim JE, Sivula M, Strittmatter SM. Nogo receptor antagonism promotes stroke recovery by enhancing axonal plasticity. J Neurosci 2004; 24: 6209-17. (Pubitemid 38891112)
38. Li S, Overman JJ, Katsman D, Kozlov SV, Donnelly CJ, Twiss JL, et al. An age-related sprouting transcriptome provides molecular control of axonal sprouting after stroke. Nat Neurosci 2010; 13: 1496-504.
39. Lindenberg R, Renga V, Zhu LL, Betzler F, Alsop D, Schlaug G. Structural integrity of corticospinal motor fibers predicts motor impairment in chronic stroke. Neurology 2010; 74: 280-7.
40. Macleod MR, Fisher M, O'Collins V, Sena ES, Dirnagl U, Bath PM, et al. Good laboratory practice: preventing introduction of bias at the bench. Stroke 2009; 40: e50-e52.
41. Markus TM, Tsai SY, Bollnow MR, Farrer RG, O'Brien TE, Kindler-Baumann DR, et al. Recovery and brain reorganization after stroke in adult and aged rats. Ann Neurol 2005; 58: 950-3. (Pubitemid 41746886)
42. Massey JM, Hubscher CH, Wagoner MR, Decker JA, Amps J, Silver J, et al. Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. J Neurosci 2006; 26: 4406-14. (Pubitemid 44315399)
43. Montoya CP, Campbell-Hope LJ, Pemberton KD, Dunnett SB. The "staircase test": a measure of independent forelimb reaching and grasping abilities in rats. J Neurosci Methods 1991; 36: 219-28.
44. Moon LD, Asher RA, Rhodes KE, Fawcett JW. Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat Neurosci 2001; 4: 465-6. (Pubitemid 32397182)
45. Papadopoulos CM, Tsai SY, Alsbiei T, O'Brien TE, Schwab ME, Kartje GL. Functional recovery and neuroanatomical plasticity following middle cerebral artery occlusion and IN-1 antibody treatment in the adult rat. Ann Neurol 2002; 51: 433-41. (Pubitemid 34260773)
46. Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 2002; 298: 1248-51. (Pubitemid 35285495)
47. Pizzorusso T, Medini P, Landi S, Baldini S, Berardi N, Maffei L. Structural and functional recovery from early monocular deprivation in adult rats. Proc Natl Acad Sci USA 2006; 103: 8517-22. (Pubitemid 43838487)
48. Rose L, Bakal DA, Fung TS, Farn P, Weaver LE. Tactile extinction and functional status after stroke. A preliminary investigation. Stroke 1994; 25: 1973-6. (Pubitemid 24291282)
49. Saver JL, Albers GW, Dunn B, Johnston KC, Fisher M. Stroke Therapy Academic Industry Roundtable (STAIR) recommendations for extended window acute stroke therapy trials. Stroke 2009; 40: 2594-600.
50. Schaechter JD, Perdue KL. Enhanced cortical activation in the contralesional hemisphere of chronic stroke patients in response to motor skill challenge. Cereb Cortex 2008; 18: 638-47. (Pubitemid 351264234)
51. Schallert T, Fleming SM, Leasure JL, Tillerson JL, Bland ST. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 2000; 39: 777-87. (Pubitemid 30103682)
52. Schallert T, Upchurch M, Lobaugh N, Farrar SB, Spirduso WW, Gilliam P, et al. Tactile extinction: distinguishing between sensorimotor and motor asymmetries in rats with unilateral nigrostriatal damage. Pharmacol Biochem Behav 1982; 16: 455-62. (Pubitemid 12147019)
53. Schallert T, Whishaw IQ. Bilateral cutaneous stimulation of the somatosensory system in hemidecorticate rats. Behav Neurosci 1984; 98: 518-40. (Pubitemid 14088521)
54. Soleman S, Yip P, Leasure JL, Moon L. Sustained sensorimotor impairments after endothelin-1 induced focal cerebral ischemia (stroke) in aged rats. Exp Neurol 2010; 222: 13-24.
55. Strong K, Mathers C, Bonita R. Preventing stroke: saving lives around the world. Lancet Neurol 2007; 6: 182-7. (Pubitemid 46097543)
56. Takahashi-Iwanaga H, Murakami T, Abe K. Three-dimensional microanatomy of perineuronal proteoglycan nets enveloping motor neurons in the rat spinal cord. J Neurocytol 1998; 27: 817-27. (Pubitemid 29441059)
57. Tang X, Davies JE, Davies SJ. Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J Neurosci Res 2003; 71: 427-44. (Pubitemid 36159501)
58. Truelsen T, Piechowski-Jozwiak B, Bonita R, Mathers C, Bogousslavsky J, Boysen G. Stroke incidence and prevalence in Europe: a review of available data. Eur J Neurol 2006; 13: 581-98. (Pubitemid 43873630)
59. Uryu K, MacKenzie L, Chesselet MF. Ultrastructural evidence for differential axonal sprouting in the striatum after thermocoagulatory and aspiration lesions of the cerebral cortex in adult rats. Neuroscience 2001; 105: 307-16. (Pubitemid 32728115)
60. Ward NS. Plasticity and the functional reorganization of the human brain. Int J Psychophysiol 2005; 58: 158-61. (Pubitemid 41539419)
61. Wiessner C, Bareyre FM, Allegrini PR, Mir AK, Frentzel S, Zurini M, et al. Anti-Nogo-A antibody infusion 24 hours after experimental stroke improved behavioral outcome and corticospinal plasticity in normotensive and spontaneously hypertensive rats. J Cereb Blood Flow Metab 2003; 23: 154-65. (Pubitemid 36188454)
62. Windle V, Szymanska A, Granter-Button S, White C, Buist R, Peeling J, et al. An analysis of four different methods of producing focal cerebral ischemia with endothelin-1 in the rat. Exp Neurol 2006; 201: 324-34. (Pubitemid 44344225)
63. Wong LF, Yip PK, Battaglia A, Grist J, Corcoran J, Maden M, et al. Retinoic acid receptor beta2 promotes functional regeneration of sensory axons in the spinal cord. Nat Neurosci 2006; 9: 243-50. (Pubitemid 43164548)
64. Zheng B, Atwal J, Ho C, Case L, He XL, Garcia KC, et al. Genetic deletion of the Nogo receptor does not reduce neurite inhibition in vitro or promote corticospinal tract regeneration in vivo. Proc Natl Acad Sci USA 2005; 102: 1205-10. (Pubitemid 40170750)
65. Zhu LL, Lindenberg R, Alexander MP, Schlaug G. Lesion load of the corticospinal tract predicts motor impairment in chronic stroke. Stroke 2010; 41: 910-5.