Doublecortin-expressing cells in the ischemic penumbra of a small-vessel stroke

Journal of Neuroscience Research

Volumn 86, Issue 4, 2008, Pages 883-893

  Hua, Rui ^a   Doucette, Ron ^a   Walz, Wolfgang ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

5 (and 6 ) carboxyfluorescein diacetate succinimidyl ester; Focal ischemia; Migration; Neuroblasts; Neurogenesis

Indexed keywords

CARBOXYFLUORESCEIN DIACETATE SUCCINIMIDYL ESTER; DOUBLECORTIN; TUBULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CELL MIGRATION; COMPARATIVE STUDY; CONTROLLED STUDY; CORPUS CALLOSUM; GLIA CELL; IMMUNOREACTIVITY; MALE; NEOCORTEX; NEUROBLAST; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEM CELL; STROKE; SUBVENTRICULAR ZONE;

ANIMALS; BRAIN INFARCTION; CELL DIFFERENTIATION; CELL MOVEMENT; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, CONFOCAL; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; NEUROPEPTIDES; PIA MATER; RATS; RATS, WISTAR; STEM CELLS; STROKE;

EID: 40549105123     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21546     Document Type: Article

References (58)

1. Alvarez-Buylla A, Lim DA. 2004. For the long run: maintaining germinal niches in the adult brain. Neuron 41:683-686.
2. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. 2002. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963-970.
3. Bar T. 1980. The vascular system of the cerebral cortex. Adv Anat Embryol Cell Biol 59:I-VI, 1-62.
4. Belachew S, Chittajallu R, Aguirre AA, Yuan X, Kirby M, Anderson S, Gallo V. 2003. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J Cell Biol 161:169-186.
5. Bhardwaj RD, Curtis MA, Spalding KL, Buchholz BA, Fink D, Bjork-Eriksson T, Nordborg C, Gage FH, Druid H, Eriksson PS, Frisen J. 2006. Neocortical neurogenesis in humans is restricted to development. Proc Natl Acad Sci U S A 103:12564-12568.
6. Boenisch T. 2001. Formalin-fixed and heat-retrieved tissue antigens: a comparison of their imrnunoreactivity in experimental antibody diluents. Appl Immunohistochem Mol Morphol 9:176-179.
7. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. 2003. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
8. Carmichael ST. 2005. Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx 2:396-409.
9. Chester EM, Agamanolis DP, Banker BQ, Victor M. 1978. Hypertensive encephalopathy: a clinicopathologic study of 20 cases. Neurology 28:928-939.
10. Cogle CR, Yachnis AT, Laywell ED, Zander DS, Wingard JR, Steindler DA, Scott EW. 2004. Bone marrow transdifferentiation in brain after transplantation: a retrospective study. Lancet 363:1432-1437.
11. Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, Bogdahn U, Winkler J, Kuhn HG, Aigner L. 2005. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21:1-14.
12. Farr TD, Whishaw IQ. 2002. Quantitative and qualitative impairments in skilled reaching in the mouse (Mus musculus) after a focal motor cortex stroke. Stroke 33:1869-1875.
13. Gaughwin PM, Caldwell MA, Anderson JM, Schwiening CJ, Fawcett JW, Compston DA, Chandran S. 2006. Astrocytes promote neurogenesis from oligodendrocyte precursor cells. Eur J Neurosci 23:945-956.
14. Gleeson JG, Lin PT, Flanagan LA, Walsh CA. 1999. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23:257-271.
15. Gonzalez CL, Kolb B. 2003. A comparison of different models of stroke on behaviour and brain morphology. Eur J Neurosci 18:1950-1962.
16. Greenberg SM. 2006. Small vessels, big problems. N Engl J Med 354:1451-1453.
17. Gu W, Brannstrom T, Wester P. 2000. Cortical neurogenesis in adult rats after reversible photothrombotic stroke. J Cereb Blood Flow Metab 20:1166-1173.
18. Hallbergson AF, Gnatenco C, Peterson DA. 2003. Neurogenesis and brain injury: managing a renewable resource for repair. J Clin Invest 112:1128-1133.
19. Hess DC, Hill WD, Martin-Studdard A, Carothers J, Brailer J, Carroll J. 2002. Blood into brain after stroke. Trends Mol Med 8:452-453.
20. Hess DC, Abe T, Hill WD, Studdard AM, Carothers J, Masuya M, Fleming PA, Drake CJ, Ogawa M. 2004. Hematopoietic origin of microglial and perivascular cells in brain. Exp Neurol 186:134-144.
21. Hu H, Dong Y, Feng P, Fechner J, Hamawy M, Knechtle SJ. 2003. Effect of immunosuppressants on T-cell subsets observed in vivo using carboxy-fluorescein diacetate succinimidyl ester labeling. Transplantation 75:1075-1077.
22. Hua R, Walz W. 2006a. Minocycline treatment prevents cavitation in rats after a cortical devascularizing lesion. Brain Res 1090:172-181.
23. Hua R, Walz W. 2006b. The need for animal models in small-vessel brain disease. Crit Rev Neurobiol (in press).
24. Jepsen K, Hermanson O, Onami TM, Gleiberman AS, Lunyak V, McEvilly RJ, Kurokawa R, Kumar V, Liu F, Seto E, Hedrick SM, Mandel G, Glass CK, Rose DW, Rosenfeld MG. 2000. Combinatorial roles of the nuclear receptor corepressor in transcription and development. Cell 102:753-763.
25. Jiang W, Gu W, Brannstrom T, Rosqvist R, Wester P. 2001. Cortical neurogenesis in adult rats after transient middle cerebral artery occlusion. Stroke 32:1201-1207.
26. Jin K, Sun Y, Xie L, Peel A, Mao XO, Batteur S, Greenberg DA. 2003. Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum. Mol Cell Neurosci 24:171.
27. Key G, Becker MH, Baron B, Duchrow M, Schluter C, Flad HD, Gerdes J. 1993. New Ki-67-equivalent murine monoclonal antibodies (MIB 1-3) generated against bacterially expressed parts of the Ki-67 cDNA containing three 62 base pair repetitive elements encoding for the Ki-67 epitope. Lab Invest 68:629-636.
28. Koizumi H, Higginbotham H, Poon T, Tanaka T, Brinkman BC, Gleeson JG. 2006. Doublecortin maintains bipolar shape and nuclear translocation during migration in the adult forebrain. Nat Neurosci 9:779-786.
29. Komitova M, Zhao LR, Gido G, Johansson BB, Eriksson P. 2005. Post-ischemic exercise attenuates whereas enriched environment has certain enhancing effects on lesion-induced subventricular zone activation in the adult rat. Eur J Neurosci 21:2397-2405.
30. Kondo T, Raff M. 2000. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science 289:1754-1757.
31. Lee EJ, Kim IB, Lee E, Kwon SO, Oh SJ, Chun MH. 2003. Differential expression and cellular localization of doublecortin in the developing rat retina. Eur J Neurosci 17:1542-1548.
32. Li X, Dancausse H, Grijalva I, Oliveira M, Levi AD. 2003. Labeling Schwann cells with CFSE - an in vitro and in vivo study. J Neurosci Methods 125:83-91.
33. Lichtenwalner RJ, Parent JM. 2006. Adult neurogenesis and the ischemic forebrain. J Cereb Blood Flow Metab 26:1-20.
34. Lindsey BW, Tropepe V. 2006. A comparative framework for understanding the biological principles of adult neurogenesis. Prog Neurobiol 80:281-307.
35. Lindvall O, Kokaia Z. 2006. Stem cells for the treatment of neurological disorders. Nature 441:1094-1096.
36. Lledo PM, Alonso M, Grubb MS. 2006. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7:179-193.
37. Lu G, Wai SM, Poon WS, Yew DT. 2005. Ki67 and doublecortin positive cells in the human prefrontal cortices of normal aging and vascular dementia. Microsc Res Techniq 68:255-257.
38. Nacher J, Crespo C, McEwen BS. 2001. Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 14:629.
39. Nunes MC, Roy NS, Keyoung HM, Goodman RR, McKhann G 2nd, Jiang L, Kang J, Nedergaard M, Goldman SA. 2003. Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med 9:439-447.
40. Nygren J, Wieloch T, Pesic J, Brundin P, Deierborg T. 2006. Enriched environment attenuates cell genesis in subventricular zone after focal ischemia in mice and decreases migration of newborn cells to the striatum. Stroke 37:2824-2829.
41. Ocbina PJ, Dizon ML, Shin L, Szele FG. 2006. Doublecortin is necessary for the migration of adult subventricular zone cells from neurospheres. Mol Cell Neurosci 33:126-135.
42. Ohab JJ, Fleming S, Blesch A, Carmichael ST. 2006. A neurovascular niche for neurogenesis after stroke. J Neurosci 26:13007-13016.
43. Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM. 2002. Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol 52:802-813.
44. Peretto P, Merighi A, Fasolo A, Bonfanti L. 1999. The subependymal layer in rodents: a site of structural plasticity and cell migration in the adult mammalian brain. Brain Res Bull 49:221-243.
45. Petreanu L, Alvarez-Buylla A. 2002. Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22:6106-6113.
46. Plumpe T, Ehninger D, Steiner B, Klempin F, Jessberger S, Brandt M, Romer B, Rodriguez GR, Kronenberg G, Kempermann G. 2006. Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci 7:77.
47. Rafii S, Lyden D. 2003. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 9:702-712.
48. Ramaswamy S, Goings GE, Soderstrom KE, Szele FG, Kozlowski DA. 2005. Cellular proliferation and migration following a controlled cortical impact in the mouse. Brain Res 1053:38-53.
49. Taupin P. 2006. Stroke-induced neurogenesis: physiopathology and mechanisms. Curr Neurovasc Res 3:67-72.
50. Thored P, Arvidsson A, Cacci E, Ahlenius H, Kallur T, Darsalia V, Ekdahl CT, Kokaia Z, Lindvall O. 2006. Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24:739-747.
51. Ughrin YM, Chen ZJ, Levine JM. 2003. Multiple regions of the NG2 proteoglycan inhibit neurite growth and induce growth cone collapse. J Neurosci 23:175-186.
52. Wang K, Walz W. 2003. Unusual topographical pattern of proximal astrogliosis around a cortical devascularizing lesion. J Neurosci Res 73:497-506.
53. 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.
54. Wardlaw J. 2004. ACCESS: the acute cerebral CT evaluation stroke study. Emerg Med J 21:666.
55. Yamashita T, Ninomiya M, Hernandez Acosta P, Garcia-Verdugo JM, Sunabori T, Sakaguchi M, Adachi K, Kojima T, Hirota Y, Kawase T, Araki N, Abe K, Okano H, Sawamoto K. 2006. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J Neurosci 26:6627-6636.
56. Zhang RL, Zhang ZG, Zhang L, Chopp M. 2001. Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia. Neuroscience 105:33-41.
57. Zhang R, Zhang Z, Wang L, Wang Y, Gousev A, Zhang L, Ho KL, Morshead C, Chopp M. 2004. Activated neural stem cells contribute to stroke-induced neurogenesis and neuroblast migration toward the infarct boundary in adult rats. J Cereb Blood Flow Metab 24:441-448.
58. Zhang RL, Zhang ZG, Chopp M. 2005. Neurogenesis in the adult ischemic brain: generation, migration, survival, and restorative therapy. Neuroscientist 11:408-416.