Mature astrocytes in the adult human neocortex express the early neuronal marker doublecortin

Brain

Volumn 130, Issue 12, 2007, Pages 3321-3335

  Verwer, R W H ^a   Sluiter, A A ^a   Balesar, R A ^a   Baayen, J C ^b   Noske, D P ^b   Dirven, C M F ^b   Wouda, J ^c   Van Dam, A M ^b   Lucassen, P J ^c   Swaab, D F ^a  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Alzheimer pathology; Epilepsy; Microglia; Neurodegenerative disease; Neurons

Indexed keywords

BIOLOGICAL MARKER; DOUBLECORTIN; GLIAL FIBRILLARY ACIDIC PROTEIN;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; ASTROCYTE; ASTROCYTIC SOMATA; AUTOPSY; BRAIN; BRAIN SURGERY; CELL COMPARTMENTALIZATION; CHILD; CORRELATION ANALYSIS; CYTOARCHITECTURE; DEGENERATIVE DISEASE; DISEASE MARKER; FEMALE; GLIA CELL; HLA SYSTEM; HUMAN; HUMAN TISSUE; IMMUNOREACTIVITY; MAJOR CLINICAL STUDY; MALE; MATURITY; NEOCORTEX; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEUROLOGIC DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADOLESCENT; ADULT; AGE DISTRIBUTION; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ASTROCYTES; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; MALE; MICROTUBULE-ASSOCIATED PROTEINS; MIDDLE AGED; NEOCORTEX; NEURODEGENERATIVE DISEASES; NEUROPEPTIDES;

EID: 36749010157     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awm264     Document Type: Article

References (60)

1. Alvarez-Buylla A, García-Verdugo JM, Tramontin AD. A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2001; 2: 287-93.
2. Arsenijevic Y, Villemure JG, Brunet JF, Bloch JJ, Deglon N, Kostic C, et al. Isolation of multipotent neural precursors residing in the cortex of the adult human brain. Exp Neurol 2001; 170: 48-62.
3. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 2002; 8: 963-70.
4. Björklund A, Lindvall O. Self-repair in the brain. Nature 2000; 405: 892-5.
5. Boekhoorn K, Joels M, Lucassen PJ. Increased proliferation reflects glial and vascular-associated changes, but not neurogenesis in the presenile Alzheimer hippocampus. Neurobiol Dis 2006; 24: 1-14.
6. Bothwell S, Meredith GE, Phillips J, Staunton H, Doherty C, Grigorenko E, et al. Neuronal hypertrophy in the neocortex of patients with temporal lobe epilepsy. J Neurosci 2001; 21: 4789-800.
7. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991; 82: 239-59.
8. Briellmann RS, Kalnins RM, Berkovic SF, Jackson GD. Hippocampal pathology in refractory temporal lobe epilepsy. T2-weighted signal change reflects dentate gliosis. Neurology 2002; 58: 265-71.
9. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 2003; 467: 1-10.
10. Burgess HA, Reiner O. Doublecortin-like kinase is associated with microtubules in neuronal growth cones. Mol Cell Neurosci 2000; 16: 529-41.
11. Choi Y-L, Park S-H, Chung C-K, Suh YL, Chi JG. Cortical laminar disorganization is correlated with severity of the cortical dysplasia and surgical outcome - experience with 150 cases. Epilepsy Res 2004; 62: 171-8.
12. Colombo JA, Quinn B, Puissant V. Disruption of astroglial interlaminar processes in Alzheimer's disease. Brain Res Bull 2002; 58: 235-42.
13. Conover WJ. Practical nonparametric statistics. 2nd edn., New York: Wiley; 1980. p. 229-39.
14. Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, et al. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 2005; 21: 1-14.
15. Crespel A, Coubes P, Rousset MC, Brana C, Rougier A, Rondouin G, et al. Inflammatory reactions in human medial temporal lobe epilepsy with hippocampal sclerosis. Brain Res 2002; 18: 159-69.
16. Crespel A, Rigau V, Coubes P, Rousset MC, de Bock F, Okano H, et al. Increased number of neural progenitors in human temporal lobe epilepsy. Neurobiol Dis 2005; 19: 436-50.
17. Curtis MA, Penney EB, Pearson AG, van Roon-Mom WMC, Butterworth NJ, Dragunow M, et al. Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc Natl Acad Sci USA 2003; 100: 9023-7.
18. Curtis MA, Kam M, NannMark U, Anderson MF, Zetterstrom Axell M, Wikkelso C, et al. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 2007; 315: 1243-9.
19. Darsalia V, Heldmann U, Lindvall O, Kokaia Z. Stroke-induced neurogenesis in aged brain. Stroke 2005; 36: 1790-5.
20. Daou MC, Smith TW, Litofsky NS, Hsieh CC, Ross AH. Doublecortin is preferentially expressed in invasive human brain tumors. Acta Neuropathol 2005; 110: 472-80.
21. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn A, Nordborg C, Peterson DA, et al. Neurogenesis in the adult human hippocampus. Nat Med 1998; 4: 1-5.
22. Fahrner A, Kann G, Flubacher A, Heinrich C, Freiman TM, Zentne J, et al. Granule cell dispersion is not accompanied by enhanced neurogenesis in temporal lobe epilepsy patients. Exp Neurol 2007; 203: 320-32.
23. Francis F, Koulakoff A, Boucher D, Chafey P, Schaar B, Vinet MC, et al. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiated neurons. Neuron 1999; 23: 247-56.
24. Friocourt G, Koulakoff A, Chafey P, Boucher D, Fauchereau F, Chelly J, et al. Doublecortin functions at the extremities of growing neuronal processes. Cereb Cortex 2003; 13: 620-6.
25. Gleeson JG, Lin PT, Flanagan LA, Walsh CA. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 1999; 23: 257-71.
26. Goldman S. Glia as neural progenitor cells. Trends Neurosci 2003; 26: 590-6.
27. Gould E, Tanapat P. Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. Neuroscience 1997; 80: 427-36.
28. Hardy JA, Wester P, Winblad B, Gezelius C, Bring G, Erikson A. The patients dying after long terminal phase have acidotic brains: implications for biochemical measurements on autopsy tissue. J Neural Transm 1985; 61: 253-64.
29. Jessberger S, Römer B, Babu H, Kempermann G. Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells. Exp Neurol 2005; 196: 342-51.
30. Jiang W, Gu W, Brännström T, Rosqvist R, Wester P. Cortical neurogenesis in adult rats after transient middle cerebral artery occlusion. Stroke 2001; 32: 1201-7.
31. Jin K, Sun Y, Xie L, Peel A, Mao XO, Batteur S, et al. Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum. Mol Cell Neurosci 2003; 24: 171-89.
32. Jin K, Peel AL, Mao XO, Xie L, Cottrell BA, Henshall DC, et al. Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci USA 2004; 101: 343-7.
33. Kendall C, Everall I, Polkey C, Al-Sarraj S. Glial cell changes in the white matter in temporal lobe epilepsy. Epilepsy Res 1999; 36: 43-51.
34. Koizumi H, Higginbotham H, Poon T, Tanaka T, Brinkman BC, Gleeson JG. Doublecortin maintains bipolar shape and nuclear translocation during migration in the adult forebrain. Nat Neurosci 2006; 9: 779-86.
35. Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 1996; 16: 2027-33.
36. Kukekov VG, Laywell ED, Suslov O, Davies K, Scheffler B, Thomas LB, et al. Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of the adult human brain. Exp Neurol 1999; 156: 333-44.
37. Leavitt BR, Hernit-Grant CS, Macklis JD. Mature astrocytes transform into transitional radial glia within adult mouse neocortex that supports directed migration of transplanted immature neurons. Exp Neurol 1999; 157: 43-57.
38. Lee A, Maldonado M, Baybis M, Walsh CA, Scheithauer B, Yeung R, et al. Markers of cellular proliferation are expressed in cortical tubers. Ann Neurol 2003; 53: 668-73.
39. Lois C, Alvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci USA 1993; 90: 2074-77.
40. Magavi SS, Leavitt BR, Macklis JD. Induction of neurogenesis in the neocortex of adult mice. Nature 2000; 405: 951-5.
41. Nacher J, Crespo C, McEwen BS. Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 2001; 14: 629-44.
42. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, et al. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 2002; 110: 429-41.
43. Oberheim NA, Wang X, Goldman S, Nedergaard M. Astrocytic complexity distinguishes the human brain. Trends Neurosci 2006; 29: 547-53.
44. Omori Y, Suzuki M, Ozaki K, Harada Y, Nakamura Y, Takahashi E, et al. Expression and chromosomal localization of KIAA0369, a putative kinase structurally related to doublecortin. J Hum Gen 1998; 43: 169-77.
45. Palmer TD, Willhoit AR, Gage FR. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 2000; 425: 479-94.
46. Palmer TD, Schwartz PH, Taupin P, Kaspar B, Stein SA, Gage F. Progenitor cells from human brain after death. Nature 2001; 411: 42-3.
47. Parent JM. The role of seizure-induced neurogenesis in epileptogenesis and brain repair. Epilepsy Res 2002; 50: 179-89.
48. Pincus DW, Harrison-Restelli C, Barry J, Goodman RR, Fraser RAR, Nedergaard M, et al. In vitro neurogenesis by adult human epileptic temporal neocortex. Clin Neurosurg 1997; 44: 17-25.
49. Prayson RA, Estes ML. Cortical dysplasia; a histopathologic study of 52 cases of partial lobectomy in patients with epilepsy. Hum Pathol 1995; 25: 493-500.
50. Rakic P. Neuroscience: immigration denied. Nature 2004; 427: 685-6.
51. Rao MS, Shetty AK. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 2004; 19: 234-46.
52. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004; 427: 740-4.
53. Spreafico R, Pasquier B, Minotti L, Garbelli R, Kahane P, Grand S, et al. Immunocytochemical investigation on dysplastic human tissue from epileptic patients. Epilepsy Res 1998; 32: 34-48.
54. Steindler DA, Laywell ED. Astrocytes as stem cells: nomenclature, phenotype, and translation. Glia 2003; 43: 62-9.
55. Sundholm-Peters NL, Yang HKC, Goings GE, Walker AS, Szele FG. Subventricular zone neuroblasts emigrate toward cortical lesions. J Neuropathol Exp Neurol 2005; 64: 1089-100.
56. Unal-Cevik I, Kilinc M, Gursoy-Ozdemir Y, Gurer G, Dalkara T. Loss of NeuN immunoreactivity after cerebral ischemia does not indicate neuronal cell loss: a cautionary note. Brain Res 2004; 1015: 169-74.
57. Verwer RWH, Hermens WTJMC, Dijkhuizen PA, ter Brake O, Baker RE, Salehi A, et al. Cells in human postmortem brain tissue slices remain alive for several weeks in culture. FASEB J 2002; 16: 54-60.
58. Verwer RWH, Baker RE, Boiten EFJ, Dubelaar EJG, van Ginkel CJM, Sluiter AA, et al. Postmortem brain tissue cultures from elderly control subjects and patients with a neurodegenerative disease. Exp Gerontol 2003; 38: 167-72.
59. Yanamoto H, Miyamoto S, Tohnia N, Nagata I, Xue JH, Nakano Y, et al. Induced spreading depression activates persistent neurogenesis in the subventricular zone, generating cells with markers for divided and early committed neurons in the caudate putamen and cortex. Stroke 2005; 36: 1544-50.
60. Zhou L, Del Villar K, Dong Z, Miller CA. Neurogenesis response to hypoxia-induced cell death: map kinase signal transduction mechanisms. Brain Res 2004; 1021: 8-19.