The proliferative capacity of the subventricular zone is maintained in the parkinsonian brain

Brain

Volumn 134, Issue 11, 2011, Pages 3249-3263

  Van Den Berge, Simone A ^a   Van Strien, Miriam E ^a   Korecka, Joanna A ^a   Dijkstra, Anke A ^b   Sluijs, Jacqueline A ^a   Kooijman, Lieneke ^a   Eggers, Ruben ^a   De Filippis, Lidia ^c   Vescovi, Angelo L ^d   Verhaagen, Joost ^a   Van De Berg, Wilma D J ^b   Hol, Elly M ^a,e  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

^d CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

^e UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

adult neurogenesis; neural stem cells; Parkinson's disease

Indexed keywords

DOPAMINE; DOPAMINE RECEPTOR BLOCKING AGENT; DOPAMINE RECEPTOR STIMULATING AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPSY; BRAIN; CELL COUNT; CELL PROLIFERATION; CLINICAL ARTICLE; DIFFUSE LEWY BODY DISEASE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MOUSE; NEURAL STEM CELL; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; SUBVENTRICULAR ZONE; SYMPTOM;

EID: 81055147229     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awr256     Document Type: Article

References (73)

1. Ahlenius H, Visan V, Kokaia M, Lindvall O, Kokaia Z. Neural stem and progenitor cells retain their potential for proliferation and differentiation into functional neurons despite lower number in aged brain. J Neurosci 2009; 29: 4408-19.
2. Alafuzoff I, Ince PG, Arzberger T, Al-Sarraj S, Bell J, Bodi I, et al. Staging/typing of Lewy body related alpha-synuclein pathology: a study of the BrainNet Europe Consortium. Acta Neuropathol 2009; 117: 635-52.
3. Aponso PM, Faull RL, Connor B. Increased progenitor cell proliferation and astrogenesis in the partial progressive 6-hydroxydopamine model of Parkinson's disease. Neuroscience 2008; 151: 1142-53.
4. Arias-Carrion O, Freundlieb N, Oertel WH, Höglinger GU. Adult neuro-genesis and Parkinson's disease. CNS Neurol Disord Drug Targets 2007; 6: 326-35.
5. Arias-Carrion O, Hernandez-Lopez S, Ibanez-Sandoval O, Bargas J, Hernandez-Cruz A, Drucker-Colin R. Neuronal precursors within the adult rat subventricular zone differentiate into dopaminergic neurons after substantia nigra lesion and chromaffin cell transplant. J Neurosci Res 2006; 84: 1425-37. (Pubitemid 44683137)
6. Arias-Carrion O, Verdugo-Diaz L, Feria-Velasco A, Millan-Aldaco D, Gutierrez AA, Hernandez-Cruz A, et al. Neurogenesis in the subventricular zone following transcranial magnetic field stimulation and nigrostriatal lesions. J Neurosci Res 2004; 78: 16-28. (Pubitemid 39305150)
7. Baker SA, Baker KA, Hagg T. Dopaminergic nigrostriatal projections regulate neural precursor proliferation in the adult mouse subventricu-lar zone. Eur J Neurosci 2004; 20: 575-9. (Pubitemid 38969643)
8. Belluardo N, Mudo G, Bonomo A, Di Liberto V, Frinchi M, Fuxe K. Nicotine-induced fibroblast growth factor-2 restores the age-related decline of precursor cell proliferation in the subventricular zone of rat brain. Brain Res 2008; 1193: 12-24.
9. Berendse HW, Booij J, Francot CM, Bergmans PL, Hijman R, Stoof JC, et al. Subclinical dopaminergic dysfunction in asymptomatic Parkinson's disease patients' relatives with a decreased sense of smell. Ann Neurol 2001; 50: 34-41. (Pubitemid 32591460)
10. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991; 82: 239-59.
11. Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 2003; 24: 197-211. (Pubitemid 36007810)
12. Cooper O, Isacson O. Intrastriatal transforming growth factor-a delivery to a model of Parkinson's disease induces proliferation and migration of endogenous adult neural progenitor cells without differentiation into dopaminergic neurons. J Neurosci 2004; 24: 8924-31. (Pubitemid 39372237)
13. Coronas V, Bantubungi K, Fombonne J, Krantic S, Schiffmann SN, Roger M. Dopamine D3 receptor stimulation promotes the proliferation of cells derived from the post-natal subventricular zone. J Neurochem 2004; 91: 1292-301. (Pubitemid 39658556)
14. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, et al. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 2007; 315: 1243-9. (Pubitemid 46364256)
15. de Chevigny A, Cooper O, Vinuela A, Reske-Nielsen C, Lagace DC, Eisch AJ, et al. Fate mapping and lineage analyses demonstrate the production of a large number of striatal neuroblasts after transforming growth factor a and noggin striatal infusions into the dopamine-depleted striatum. Stem Cells 2008; 26: 2349-60.
16. De Filippis L, Lamorte G, Snyder EY, Malgaroli A, Vescovi AL. A novel, immortal, and multipotent human neural stem cell line generating functional neurons and oligodendrocytes. Stem Cells 2007; 25: 2312-21. (Pubitemid 47480490)
17. Diaz D, Valero J, Airado C, Baltanas FC, Weruaga E, Alonso JR. Sexual dimorphic stages affect both proliferation and serotonergic innervation in the adult rostral migratory stream. Exp Neurol 2009; 216: 357-64.
18. Dickson DW, Fujishiro H, DelleDonne A, Menke J, Ahmed Z, Klos KJ, et al. Evidence that incidental Lewy body disease is pre-symptomatic Parkinson's disease. Acta Neuropathol 2008; 115: 437-44.
19. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 1997; 17: 5046-61. (Pubitemid 27263818)
20. Eisch AJ, Mandyam CD. Adult neurogenesis: can analysis of cell cycle proteins move us "Beyond BrdU"? Curr Pharm Biotechnol 2007; 8: 147-65. (Pubitemid 47009482)
21. Fallon J, Reid S, Kinyamu R, Opole I, Opole R, Baratta J, et al. In vivo induction of massive proliferation, directed migration, and differentiation of neural cells in the adult mammalian brain. Proc Natl Acad Sci USA 2000; 97: 14686-691. (Pubitemid 32016636)
22. Freundlieb N, Francois C, Tande D, Oertel WH, Hirsch EC, Höglinger GU. Dopaminergic substantia nigra neurons project topographically organized to the subventricular zone and stimulate precursor cell proliferation in aged primates. J Neurosci 2006; 26: 2321-5. (Pubitemid 44699041)
23. Gaig C, Tolosa E. When does Parkinson's disease begin? Mov Disord 2009; 24: S656-64.
24. Geraerts M, Krylyshkina O, Debyser Z, Baekelandt V. Concise review: therapeutic strategies for Parkinson disease based on the modulation of adult neurogenesis. Stem Cells 2007; 25: 263-70. (Pubitemid 46232779)
25. Gonzalo-Gobernado R, Reimers D, Herranz AS, Diaz-Gil JJ, Osuna C, Asensio MJ, et al. Mobilization of neural stem cells and generation of new neurons in 6-OHDA-lesioned rats by intracerebroventricular infusion of liver growth factor. J Histochem Cytochem 2009; 57: 491-502.
26. Green W, Patil P, Marsden CA, Bennett GW, Wigmore PM. Treatment with olanzapine increases cell proliferation in the subventricular zone and prefrontal cortex. Brain Res 2006; 1070: 242-5. (Pubitemid 43247763)
27. Hawkes CH, Shephard BC, Daniel SE. Olfactory dysfunction in Parkinson's disease. J Neurol Neurosurg Psychiatry 1997; 62: 436-46. (Pubitemid 27237050)
28. Hitoshi S, Maruta N, Higashi M, Kumar A, Kato N, Ikenaka K. Antidepressant drugs reverse the loss of adult neural stem cells following chronic stress. J Neurosci Res 2007; 85: 3574-85. (Pubitemid 350228703)
29. Höglinger GU, Rizk P, Muriel MP, Duyckaerts C, Oertel WH, Caille I, et al. Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci 2004, 7, 726-35.
30. Huisman E, Uylings HB, Hoogland PV. A 100% increase of dopaminergic cells in the olfactory bulb may explain hyposmia in Parkinson's disease. Mov Disord 2004; 19: 687-92. (Pubitemid 39173024)
31. Huisman E, Uylings HBM, Hoogland PV. Gender-related changes in increase of dopaminergic neurons in the olfactory bulb of Parkinson's disease patients. Mov Disord 2008; 23: 1407-13.
32. Huitinga I, Rademaker M, Klioueva N. The art of brain banking in Europe: ethical, legal and practical guidelines for donor recruitment, tissue handling and tissue distribution. J Neural Transm 2008; 115: 1715.
33. Juan G, Traganos F, James WM, Ray JM, Roberge M, Sauve DM, et al. Histone H3 phosphorylation and expression of cyclins A and B1 measured in individual cells during their progression through G2 and mitosis. Cytometry 1998; 32: 71-7. (Pubitemid 28246753)
34. Karssen AM, Meijer OC, van der Sandt IC, Lucassen PJ, de Lange EC, de Boer AG, et al. Multidrug resistance P-glycoprotein hampers the access of cortisol but not of corticosterone to mouse and human brain. Endocrinology 2001; 142: 2686-94. (Pubitemid 32473126)
35. Kempermann G, Chesler EJ, Lu L, Williams RW, Gage FH. Natural variation and genetic covariance in adult hippocampal neurogenesis. Proc Natl Acad Sci USA 2006; 103: 780-5. (Pubitemid 43153102)
36. Kernie SG, Parent JM. Forebrain neurogenesis after focal Ischemic and traumatic brain injury. Neurobiol Dis 2010; 37: 267-74.
37. Kippin TE, Kapur S, van der Kooy D. Dopamine specifically inhibits fore-brain neural stem cell proliferation, suggesting a novel effect of anti-psychotic drugs. J Neurosci 2005; 25: 5815-23. (Pubitemid 40847894)
38. Korecka JA, Verhaagen J, Hol EM. Cell-replacement and gene-therapy strategies for Parkinson's and Alzheimer's disease. Regen Med 2007; 2: 425-46. (Pubitemid 47307222)
39. Lau W-M, Qiu G, Helmeste DM, Lee TMC, Tang S-W, So K-F, et al. Corticosteroid decreases subventricular zone cell proliferation, which could be reversed by paroxetine. Restor Neurol Neurosci 2007; 25: 17-23. (Pubitemid 46631010)
40. Leonard BW, Mastroeni D, Grover A, Liu Q, Yang K, Gao M, et al. Subventricular zone neural progenitors from rapid brain autopsies of elderly subjects with and without neurodegenerative disease. J Comp Neurol 2009; 515: 269-94.
41. Liu Bf, Gao Ej, Zeng Xz, Ji M, Cai Q, Lu Q, et al. Proliferation of neural precursors in the subventricular zone after chemical lesions of the nigrostriatal pathway in rat brain. Brain Res 2006; 1106: 30-9. (Pubitemid 44163313)
42. Lois C, Garcia-Verdugo J-M, Alvarez-Buylla A. Chain migration of neur-onal precursors. Science 1996; 271: 978-81.
43. Lucassen PJ, Meerlo P, Naylor AS, van Dam AM, Dayer AG, Fuchs E, et al. Regulation of adult neurogenesis by stress, sleep disruption, exercise and inflammation: implications for depression and antidepres-sant action. Eur Neuropsychopharmacol 2010; 20: 1-17.
44. Marti-Fabregas J, Romaguera-Ros M, Gomez-Pinedo U, Martinez-Ramirez S, Jimenez-Xarrie E, Marin R, et al. Proliferation in the human ipsilateral subventricular zone after ischemic stroke. Neurology 2010; 74: 357-65.
45. Marxreiter F, Nuber S, Kandasamy M, Klucken J, Aigner R, Burgmayer R, et al. Changes in adult olfactory bulb neurogenesis in mice expressing the A30P mutant form of alpha-synuclein. Eur J Neurosci 2009; 29: 879-90.
46. Meredith G, Sonsalla P, Chesselet M-F. Animal models of Parkinson's disease progression. Acta Neuropathol 2008; 115: 385-98.
47. Meredith GE, Totterdell S, Petroske E, Santa Cruz K, Callison RC Jr, Lau YS. Lysosomal malfunction accompanies alpha-synuclein aggregation in a progressive mouse model of Parkinson's disease. Brain Res 2002; 956: 156-65. (Pubitemid 35335568)
48. Meyer AK, Maisel M, Hermann A, Stirl K, Storch A. Restorative approaches in Parkinson's disease: Which cell type wins the race? J Neurol Sci 2010; 289: 93-103.
49. Middeldorp J, Kamphuis W, Sluijs JA, Achoui D, Leenaars CH, Feenstra MG, et al. Intermediate filament transcription in astrocytes is repressed by proteasome inhibition. FASEB J 2009; 23: 2710-26.
50. Mirescu C, Peters JD, Gould E. Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 2004; 7: 841-6. (Pubitemid 38989507)
51. Mohapel P, Frielingsdorf H, Haggblad J, Zachrisson O, Brundin P. Platelet-derived growth factor (PDGF-BB) and brain-derived neuro-trophic factor (BDNF) induce striatal neurogenesis in adult rats with 6-hydroxydopamine lesions. Neuroscience 2005; 132: 767-76.
52. Mokry J, Karbanova J, Osterreicher J. Experimental brain injury induces activation of neural stem cells in the forebrain subependyma. Appl Immunohistochem Mol Morphol 2003; 11: 161-7. (Pubitemid 36749571)
53. Mueller A, Abolmaali ND, Hakimi AR, Gloeckler T, Herting B, Reichmann H, et al. Olfactory bulb volumes in patients with idiopathic Parkinson's disease-a pilot study. J Neural Transm 2005; V112: 1363-70. (Pubitemid 41355964)
54. O'Keeffe GC, Tyers P, Aarsland D, Dalley JW, Barker RA, Caldwell MA. Dopamine-induced proliferation of adult neural precursor cells in the mammalian subventricular zone is mediated through EGF. Proc Natl Acad Sci USA 2009; 106: 8754-9.
55. Pearce RK, Hawkes CH, Daniel SE. The anterior olfactory nucleus in Parkinson's disease. Mov Disord 1995; 10: 283-7.
56. Peng J, Xie L, Jin K, Greenberg DA, Andersen JK. Fibroblast growth factor 2 enhances striatal and nigral neurogenesis in the acute 1-methyl-4-phenyl-1,2, 3,6-tetrahydropyridine model of Parkinson's disease. Neuroscience 2008; 153: 664-70.
57. Petroske E, Meredith GE, Callen S, Totterdell S, Lau YS. Mouse model of Parkinsonism: a comparison between subacute MPTP and chronic MPTP/probenecid treatment. Neuroscience 2001; 106: 589-601. (Pubitemid 32925247)
58. Poon A, Li Z, Wolfe GW, Lu L, Williams RW, Hayes NL, et al. Identification of a Chr 11 quantitative trait locus that modulates proliferation in the rostral migratory stream of the adult mouse brain. Eur J Neurosci 2010; 32: 523-37.
59. Quinones-Hinojosa A, Sanai N, Soriano-Navarro M, Gonzalez-Perez O, Mirzadeh Z, Gil-Perotin S, et al. Cellular composition and cytoarchi-tecture of the adult human subventricular zone: a niche of neural stem cells. J Comp Neurol 2006; 494: 415-34. (Pubitemid 41794059)
60. Ravid R, Van Zwieten EJ, Swaab DF. Brain banking and the human hypothalamus-factors to match for, pitfalls and potentials. Prog Brain Res 1992; 93: 83-95. (Pubitemid 23008658)
61. Roelofs RF, Fischer DF, Houtman SH, Sluijs JA, van Haren W, van Leeuwen FW, Hol EM. The adult human subventricular, subgranular and subpial zones contain astrocytes with a specialized intermediate filament cytoskeleton. Glia 2005; 52: 289-300. (Pubitemid 43076221)
62. 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. (Pubitemid 38294593)
63. Seiji H, Noriko M, Mikito H, Akhilesh K, Nobumasa K, Kazuhiro I. Antidepressant drugs reverse the loss of adult neural stem cells following chronic stress. J Neurosci Res 2007; 85: 3574-85.
64. Sun Y, Pollard S, Conti L, Toselli M, Biella G, Parkin G, et al. Long-term tripotent differentiation capacity of human neural stem (NS) cells in adherent culture. Mol Cell Neurosci 2008; 38: 245-58.
65. Thal DR, Rub U, Schultz C, Sassin I, Ghebremedhin E, Del Tredici K, et al. Sequence of Ab-protein deposition in the human medial temporal lobe. J Neuropathol Exp Neurol 2000; 59: 733-48. (Pubitemid 30626743)
66. van den Berge SA, Middeldorp J, Eleana Zhang C, Curtis MA, Leonard BW, Mastroeni D, et al. Longterm quiescent cells in the aged human subventricular neurogenic system specifically express GFAP-delta. Aging Cell 2010; 9: 313-26.
67. Wang DD, Krueger DD, Bordey A. GABA depolarizes neuronal progenitors of the postnatal subventricular zone via GABAA receptor activation. J Physiol 2003; 550: 785-800. (Pubitemid 37010063)
68. Winner B, Couillard-Despres S, Geyer M, Aigner R, Bogdahn U, Aigner L, et al. Dopaminergic lesion enhances growth factor-induced striatal neuroblast migration. J Neuropathol Exp Neurol 2008a; 67: 105-16.
69. Winner B, Desplats P, Hagl C, Klucken J, Aigner R, Ploetz S, et al. Dopamine receptor activation promotes adult neurogenesis in an acute Parkinson model. Exp Neurol 2009; 219: 543-52.
70. Winner B, Geyer M, Couillard-Despres S, Aigner R, Bogdahn U, Aigner L, et al. Striatal deafferentation increases dopaminergic neurogenesis in the adult olfactory bulb. Exp Neurol 2006; 197: 113-21. (Pubitemid 41817225)
71. Winner B, Lie DC, Rockenstein E, Aigner R, Aigner L, Masliah E, et al. Human wild-type a-synuclein impairs neurogenesis. J Neuropathol Exp Neurol 2004; 63: 1155-66. (Pubitemid 39492021)
72. Winner B, Rockenstein E, Lie DC, Aigner R, Mante M, Bogdahn U, et al. Mutant a-synuclein exacerbates age-related decrease of neurogenesis. Neurobiol Aging 2008b; 29: 913-25. (Pubitemid 351601896)
73. Zhao C, Deng W, Gage FH. Mechanisms and functional implications of adult neurogenesis. Cell 2008; 132: 645-60. (Pubitemid 351253687)