Adult hippocampal neurogenesis in Parkinson's disease: Impact on neuronal survival and plasticity

Neural Plasticity

Volumn 2014, Issue , 2014, Pages

  Regensburger, Martin ^a   Prots, Iryna ^a   Winner, Beate ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; LEUCINE RICH REPEAT KINASE 2;

ADULT; ADULT DISEASE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; DISEASE COURSE; HIPPOCAMPUS; NERVE CELL; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PARKINSON DISEASE; REVIEW; ANIMAL; DISEASE MODEL; FEMALE; GENETICS; HUMAN; LATERAL BRAIN VENTRICLE; MALE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC ANIMAL;

ADULT; ALPHA-SYNUCLEIN; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL SURVIVAL; DISEASE MODELS, ANIMAL; FEMALE; HIPPOCAMPUS; HUMANS; LATERAL VENTRICLES; MALE; NEUROGENESIS; NEURONAL PLASTICITY; NEURONS; PARKINSON DISEASE;

EID: 84904689167     PISSN: 20905904     EISSN: 16875443     Source Type: Journal    
DOI: 10.1155/2014/454696     Document Type: Review

References (182)

1. von Campenhausen S., Bornschein B., Wick R., Bötzel K., Sampaio C., Poewe W., Oertel W., Siebert U., Berger K., Dodel R., Prevalence and incidence of Parkinson's disease in Europe. European Neuropsychopharmacology 2005 15 4 473 490 10.1016/j.euroneuro.2005.04.007 2-s2.0-21744443838 (Pubitemid 40949553)
2. Trenkwalder C., Schwarz J., Gebhard J., Ruland D., Trenkwalder P., Hence-H. W., Oertel W. H., Starnberg trial on epidemiology of parkinsonism and hypertension in the elderly: prevalence of Parkinson's disease and related disorders assessed by a door-to-door survey of inhabitants older than 65 years. Archives of Neurology 1995 52 10 1017 1022 10.1001/archneur.1995.00540340109020 2-s2.0-0029165806
3. Fahn S., Description of Parkinson's disease as a clinical syndrome. Annals of the New York Academy of Sciences 2003 991 1 14 2-s2.0-0038727936 (Pubitemid 36793796)
4. Hughes A. J., Daniel S. E., Kilford L., Lees A. J., Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. Journal of Neurology, Neurosurgery & Psychiatry 1992 55 3 181 184 10.1136/jnnp.55.3.181 2-s2.0-0026514953
5. Henchcliffe C., Severt W. L., Disease modification in Parkinson's disease. Drugs & Aging 2011 28 8 605 615 10.2165/11591320-000000000-00000 2-s2.0-79961220833
6. Kordower J. H., Freeman T. B., Snow B. J., Vingerhoets F. J. G., Mufson E. J., Sanberg P. R., Hauser R. A., Smith D. A., Nauert G. M., Perl D. P., Olanow C. W., Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson's disease. The New England Journal of Medicine 1995 332 17 1118 1124 10.1056/NEJM199504273321702 2-s2.0-0028911848
7. 18F]6-L-fluorodopa studies in two patients with putaminal implants. Annals of Neurology 1992 31 2 166 173 10.1002/ana.410310207 2-s2.0-0026533881
8. Kordower J. H., Freeman T. B., Chen E.-Y., Mufson E. J., Sanberg P. R., Hauser R. A., Snow B., Olanow C. W., Fetal nigral grafts survive and mediate clinical benefit in a patient with Parkinson's disease. Movement Disorders 1998 13 3 383 393 10.1002/mds.870130303 2-s2.0-0031922226 (Pubitemid 28221487)
9. Kordower J. H., Rosenstein J. M., Collier T. J., Functional fetal nigral grafts in a patient with Parkinson's disease: chemoanatomic, ultrastructural, and metabolic studies. The Journal of Comparative Neurology 1996 370 2 203 230 (Pubitemid 26227146)
10. Kordower J. H., Chu Y., Hauser R. A., Freeman T. B., Olanow C. W., Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nature Medicine 2008 14 5 504 506 10.1038/nm1747 2-s2.0-43249114934 (Pubitemid 351655212)
11. Kordower J. H., Chu Y., Hauser R. A., Olanow C. W., Freeman T. B., Transplanted dopaminergic neurons develop PD pathologic changes: a second case report. Movement Disorders 2008 23 16 2303 2306 10.1002/mds.22369 2-s2.0-61449216234
12. Li J.-Y., Englund E., Holton J. L., Soulet D., Hagell P., Lees A. J., Lashley T., Quinn N. P., Rehncrona S., Björklund A., Widner H., Revesz T., Lindvall O., Brundin P., Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nature Medicine 2008 14 5 501 503 10.1038/nm1746 2-s2.0-43249110200 (Pubitemid 351655211)
13. Mendez I., Viñuela A., Astradsson A., Mukhida K., Hallett P., Robertson H., Tierney T., Holness R., Dagher A., Trojanowski J. Q., Isacson O., Dopamine neurons implanted into people with Parkinson's disease survive without pathology for 14 years. Nature Medicine 2008 14 5 507 509 10.1038/nm1752 2-s2.0-43249085326 (Pubitemid 351655215)
14. Freed C. R., Greene P. E., Breeze R. E., Tsai W., DuMouchel W., Kao R., Dillon S., Winfield H., Culver S., Trojanowski J. Q., Eidelberg D., Fahn S., Transplantation of embryonic dopamine neurons for severe Parkinson's disease. The New England Journal of Medicine 2001 344 10 710 719 10.1056/ NEJM200103083441002 2-s2.0-0035826089 (Pubitemid 32204988)
15. Olanow C. W., Goetz C. G., Kordower J. H., Stoessl A. J., Sossi V., Brin M. F., Shannon K. M., Nauert G. M., Perl D. P., Godbold J., Freeman T. B., A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease. Annals of Neurology 2003 54 3 403 414 10.1002/ana.10720 2-s2.0-0042837887 (Pubitemid 37072046)
16. Petit G. H., Olsson T. T., Brundin P., The future of cell therapies and brain repair: Parkinson's disease leads the way. Neuropathology and Applied Neurobiology 2014 40 1 60 70
17. Chaudhuri K. R., Healy D. G., Schapira A. H. V., Non-motor symptoms of Parkinson's disease: diagnosis and management. The Lancet Neurology 2006 5 3 235 245 10.1016/S1474-4422(06)70373-8 2-s2.0-32544432029 (Pubitemid 43238347)
18. Global Parkinson's Disease Survey Steering Committee, Factors impacting on quality of life in Parkinson's disease: results from an international survey. Movement Disorders 2002 17 1 60 67 10.1002/mds.10010 2-s2.0-0036460864 (Pubitemid 36041261)
19. Schrag A., Jahanshahi M., Quinn N., What contributes to quality of life in patients with Parkinson's disease? Journal of Neurology Neurosurgery & Psychiatry 2000 69 3 308 312 10.1136/jnnp.69.3.308 2-s2.0-0033875826 (Pubitemid 30636233)
20. Braak H., del Tredici K., Rüb U., de Vos R. A. I., Jansen Steur E. N. H., Braak E., Staging of brain pathology related to sporadic Parkinson's disease. Neurobiology of Aging 2003 24 2 197 211 10.1016/S0197-4580(02)00065-9 2-s2.0-0037333666 (Pubitemid 36007810)
21. Spillantini M. G., Schmidt M. L., Lee V.-M., Trojanowski J. Q., Jakes R., Goedert M., α -Synuclein in Lewy bodies. Nature 1997 388 6645 839 840 10.1038/42166 2-s2.0-0030882856 (Pubitemid 27377048)
22. Abbott R. D., Petrovitch H., White L. R., Masaki K. H., Tanner C. M., Curb J. D., Grandinetti A., Blanchette P. L., Popper J. S., Ross G. W., Frequency of bowel movements and the future risk of Parkinson's disease. Neurology 2001 57 3 456 462 10.1212/WNL.57.3.456 2-s2.0-0035859865 (Pubitemid 32757593)
23. Hawkes C. H., The prodromal phase of sporadic Parkinson's disease: does it exist and if so how long is it? Movement Disorders 2008 23 13 1799 1807 10.1002/mds.22242 2-s2.0-57049123693
24. Ross G. W., Petrovitch H., Abbott R. D., Tanner C. M., Popper J., Masaki K., Launer L., White L. R., Association of olfactory dysfunction with risk for future Parkinson's disease. Annals of Neurology 2008 63 2 167 173 10.1002/ana.21291 2-s2.0-40449083312 (Pubitemid 351355295)
25. Savica R., Carlin J. M., Grossardt B. R., Bower J. H., Ahlskog J. E., Maraganore D. M., Bharucha A. E., Rocca W. A., Medical records documentation of constipation preceding Parkinson disease: a case-control study. Neurology 2009 73 21 1752 1758 10.1212/WNL.0b013e3181c34af5 2-s2.0-73349092154
26. Gagnon J.-F., Postuma R. B., Mazza S., Doyon J., Montplaisir J., Rapid-eye-movement sleep behaviour disorder and neurodegenerative diseases. The Lancet Neurology 2006 5 5 424 432 10.1016/S1474-4422(06)70441-0 2-s2.0-33646025535
27. Iranzo A., Molinuevo J. L., Santamaría J., Serradell M., Martí M. J., Valldeoriola F., Tolosa E., Rapid-eye-movement sleep behaviour disorder as an early marker for a neurodegenerative disorder: a descriptive study. The Lancet Neurology 2006 5 7 572 577 10.1016/S1474-4422(06) 70476-8 2-s2.0-33744991945 (Pubitemid 43867426)
28. Barone P., Antonini A., Colosimo C., Marconi R., Morgante L., Avarello T. P., Bottacchi E., Cannas A., Ceravolo G., Ceravolo R., Cicarelli G., Gaglio R. M., Giglia R. M., Iemolo F., Manfredi M., Meco G., Nicoletti A., Pederzoli M., Petrone A., Pisani A., Pontieri F. E., Quatrale R., Ramat S., Scala R., Volpe G., Zappulla S., Bentivoglio A. R., Stocchi F., Trianni G., Del Dotto P., The PRIAMO study: a multicenter assessment of nonmotor symptoms and their impact on quality of life in Parkinson's disease. Movement Disorders 2009 24 11 1641 1649 10.1002/mds.22643 2-s2.0-69949153066
29. Leentjens A. F. G., van den Akker M., Metsemakers J. F. M., Lousberg R., Verhey F. R. J., Higher incidence of depression preceding the onset of Parkinson's disease: a register study. Movement Disorders 2003 18 4 414 418 10.1002/mds.10387 2-s2.0-0038747039 (Pubitemid 36527282)
30. Tolosa E., Gaig C., Santamaría J., Compta Y., Diagnosis and the premotor phase of Parkinson disease. Neurology 2009 72 7 S12 S20 10.1212/WNL.0b013e318198db11 2-s2.0-61949235512
31. Winkler J., Ehret R., Büttner T., Dillmann U., Fogel W., Sabolek M., Winkelmann J., Kassubek J., Parkinson's disease risk score: moving to a premotor diagnosis. Journal of Neurology 2011 258 2 S311 S315 10.1007/s00415-011-5952-x 2-s2.0-79959933179
32. Halliday G. M., Holton J. L., Revesz T., Dickson D. W., Neuropathology underlying clinical variability in patients with synucleinopathies. Acta Neuropathologica 2011 122 2 187 204 10.1007/s00401-011-0852-9 2-s2.0-79960842310
33. Irwin D. J., Lee V. M., Trojanowski J. Q., Parkinson's disease dementia: convergence of α -Synuclein, tau and amyloid- β Pathologies. Nature Reviews. Neuroscience 2013 14 9 626 636 10.1038/nrn3549
34. McKeith IG., Dickson DW., Lowe J., Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 2005 65 1863 1872 10.1212/01.wnl.0000187889.17253.b1 (Pubitemid 43970103)
35. Curtis M. A., Kam M., Nannmark U., Anderson M. F., Axell M. Z., Wikkelso C., Holtås S., Van Roon-Mom W. M. C., Björk-Eriksson T., Nordborg C., Frisén J., Dragunow M., Faull R. L. M., Eriksson P. S., Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 2007 315 5816 1243 1249 10.1126/science.1136281 2-s2.0-33847629581 (Pubitemid 46364256)
36. Eriksson P. S., Perfilieva E., Björk-Eriksson T., Alborn A., Nordborg C., Peterson D. A., Gage F. H., Neurogenesis in the adult human hippocampus. Nature Medicine 1998 4 11 1313 1317 10.1038/3305 2-s2.0-0031789814 (Pubitemid 28512114)
37. Sanai N., Nguyen T., Ihrie R. A., Mirzadeh Z., Tsai H., Wong M., Gupta N., Berger M. S., Huang E., Garcia-Verdugo J., Rowitch D. H., Alvarez-Buylla A., Corridors of migrating neurons in the human brain and their decline during infancy. Nature 2011 478 7369 382 386 10.1038/nature10487 2-s2.0-80054998431
38. Spalding K. L., Bergmann O., Alkass K., Bernard S., Salehpour M., Huttner H. B., Boström E., Westerlund I., Vial C., Buchholz B. A., Possnert G., Mash D. C., Druid H., Frisén J., Dynamics of hippocampal neurogenesis in adult humans. Cell 2013 153 6 1219 1227 10.1016/j.cell.2013.05.002 2-s2.0-84878831768
39. Höglinger G. U., Rizk P., Muriel M. P., Duyckaerts C., Oertel W. H., Caille I., Hirsch E. C., Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nature Neuroscience 2004 7 7 726 735 10.1038/nn1265 2-s2.0-3042822087 (Pubitemid 38859057)
40. Baker S. A., Baker K. A., Hagg T., Dopaminergic nigrostriatal projections regulate neural precursor proliferation in the adult mouse subventricular zone. European Journal of Neuroscience 2004 20 2 575 579 10.1111/j.1460-9568.2004. 03486.x 2-s2.0-3242757365 (Pubitemid 38969643)
41. Freundlieb N., François C., Tandé D., Oertel W. H., Hirsch E. C., Höglinger G. U., Dopaminergic substantia nigra neurons project topographically organized to the subventricular zone and stimulate precursor cell proliferation in aged primates. Journal of Neuroscience 2006 26 8 2321 2325 10.1523/JNEUROSCI.4859-05.2006 2-s2.0-33645646860 (Pubitemid 44699041)
42. Winner B., Geyer M., Couillard-Despres S., Aigner R., Bogdahn U., Aigner L., Kuhn G., Winkler J., Striatal deafferentation increases dopaminergic neurogenesis in the adult olfactory bulb. Experimental Neurology 2006 197 1 113 121 10.1016/j.expneurol.2005.08.028 2-s2.0-29144431605 (Pubitemid 41817225)
43. O'Keeffe G. C., Tyers P., Aarsland D., Dalley J. W., Barker R. A., Caldwellf M. A., Dopamine-induced proliferation of adult neural precursor cells in the mammalian subventricular zone is mediated through EGF. Proceedings of the National Academy of Sciences of the United States of America 2009 106 21 8754 8759 10.1073/pnas.0803955106 2-s2.0-66649120006
44. O'Sullivan S. S., Johnson M., Williams D. R., Revesz T., Holton J. L., Lees A. J., Perry E. K., The effect of drug treatment on neurogenesis in Parkinson's disease. Movement Disorders 2011 26 1 45 50 10.1002/mds.23340 2-s2.0-79951473139
45. Ziabreva I., Ballard C., Johnson M., Larsen J. P., McKeith I., Perry R., Aarsland D., Perry E., Loss of Musashi1 in Lewy body dementia associated with cholinergic deficit. Neuropathology and Applied Neurobiology 2007 33 5 586 590 10.1111/j.1365-2990.2007.00848.x 2-s2.0-34548567189 (Pubitemid 47390082)
46. van den Berge S. A., van Strien M. E., Korecka J. A., Dijkstra A. A., Sluijs J. A., Kooijman L., Eggers R., de Filippis L., Vescovi A. L., Verhaagen J., van de Berg W. D. J., Hol E. M., The proliferative capacity of the subventricular zone is maintained in the parkinsonian brain. Brain 2011 134 11 3249 3263 10.1093/brain/awr256 2-s2.0-81055147229
47. van den Berge S. A., Middeldorp J., Zhang C. E., Curtis M. A., Leonard B. W., Mastroeni D., Voorn P., van de Berg W. D. J., Huitinga I., Hol E. M., Longterm quiescent cells in the aged human subventricular neurogenic system specifically express GFAP- δ Aging Cell 2010 9 3 313 326 10.1111/j.1474-9726.2010.00556.x 2-s2.0-77955271817
48. Wang S., Okun M. S., Suslov O., Zheng T., McFarland N. R., Vedam-Mai V., Foote K. D., Roper S. N., Yachnis A. T., Siebzehnrubl F. A., Steindler D. A., Neurogenic potential of progenitor cells isolated from postmortem human Parkinsonian brains. Brain Research 2012 1464 61 72 10.1016/j.brainres.2012.04. 039 2-s2.0-84862015595
49. Höglinger G. U., Barker R. A., Hagg T., Arias-Carrión O., Caldwell M. A., Hirsch E. C., Quantitative evaluation of the human subventricular zone. Brain 2012 135 e221 1-4, author reply e222-1-6 10.1093/brain/aws087
50. van den Berge S. A., van Strien M. E., Korecka J. A., Dijkstra A. A., Sluijs J. A., Kooijman L., Eggers R., De Filippis L., Vescovi A. L., Verhaagen J., Van De Berg W. D. J., Hol E. M., Reply: quantitative evaluation of the human subventricular zone. Brain 2012 135 8 e222 10.1093/brain/aws088 2-s2.0-84864706142
51. Bohnen N. I., Gedela S., Kuwabara H., Constantine G. M., Mathis C. A., Studenski S. A., Moore R. Y., Selective hyposmia and nigrostriatal dopaminergic denervation in Parkinson's disease. Journal of Neurology 2007 254 1 84 90 10.1007/s00415-006-0284-y 2-s2.0-33847145330 (Pubitemid 46295073)
52. Bohnen N. I., Müller M. L. T. M., Kotagal V., Koeppe R. A., Kilbourn M. A., Albin R. L., Frey K. A., Olfactory dysfunction, central cholinergic integrity and cognitive impairment in Parkinson's disease. Brain 2010 133 6 1747 1754 10.1093/brain/awq079 2-s2.0-77952998970
53. Kareken D. A., Mosnik D. M., Doty R. L., Dzemidzic M., Hutchins G. D., Functional anatomy of human odor sensation, discrimination, and identification in health and aging. Neuropsychology 2003 17 3 482 495 10.1037/0894-4105.17.3. 482 2-s2.0-0041467554 (Pubitemid 37013159)
54. Bohnen N. I., Gedela S., Herath P., Constantine G. M., Moore R. Y., Selective hyposmia in Parkinson disease: association with hippocampal dopamine activity. Neuroscience Letters 2008 447 1 12 16 10.1016/j.neulet.2008.09.070 2-s2.0-54249119573
55. Pearce R. K. B., Hawkes C. H., Daniel S. E., The anterior olfactory nucleus in Parkinson's disease. Movement Disorders 1995 10 3 283 287 10.1002/mds.870100309 2-s2.0-0029031709
56. Mueller A., Abolmaali N. D., Hakimi A. R., Gloeckler T., Herting B., Reichmann H., Hummel T., Olfactory bulb volumes in patients with idiopathic Parkinson's disease a pilot study. Journal of Neural Transmission 2005 112 10 1363 1370 10.1007/s00702-005-0280-x 2-s2.0-16444386525 (Pubitemid 41355964)
57. Mundiñano I., Caballero M., Ordóñez C., Hernandez M., DiCaudo C., Marcilla I., Erro M., Tuñon M., Luquin M., Increased dopaminergic cells and protein aggregates in the olfactory bulb of patients with neurodegenerative disorders. Acta Neuropathologica 2011 122 1 61 74 10.1007/s00401-011-0830-2 2-s2.0-79959588593
58. Huisman E., Uylings H. B. M., Hoogland P. V., A 100% increase of dopaminergic cells in the olfactory bulb may explain hyposmia in parkinson's disease. Movement Disorders 2004 19 6 687 692 10.1002/mds.10713 2-s2.0-3843079040 (Pubitemid 39173024)
59. Winner B., Regensburger M., Schreglmann S., Boyer L., Prots I., Rockenstein E., Mante M., Zhao C., Winkler J., Masliah E., Gage F. H., Role of α -Synuclein in adult neurogenesis and neuronal maturation in the dentate gyrus. Journal of Neuroscience 2012 32 47 16906 16916 10.1523/JNEUROSCI.2723-12. 2012 2-s2.0-84870015777
60. Ballanger B., Klinger H., Eche J., Lerond J., Vallet A., Le Bars D., Tremblay L., Sgambato-Faure V., Broussolle E., Thobois S., Role of serotonergic 1A receptor dysfunction in depression associated with Parkinson's disease. Movement Disorders 2012 27 1 84 89 10.1002/mds.23895 2-s2.0-84855920924
61. Pavese N., Metta V., Bose S. K., Chaudhuri K. R., Brooks D. J., Fatigue in Parkinson's disease is linked to striatal and limbic serotonergic dysfunction. Brain 2010 133 11 3434 3443 10.1093/brain/awq268 2-s2.0-78049460075
62. Goto Y., Grace A. A., Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nature Neuroscience 2005 8 6 805 812 10.1038/nn1471 2-s2.0-22544464049 (Pubitemid 43085848)
63. Kehagia A. A., Barker R. A., Robbins T. W., Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson's disease. The Lancet Neurology 2010 9 12 1200 1213 10.1016/S1474-4422(10)70212-X 2-s2.0-78349310514
64. Churchyard A., Lees A. J., The relationship between dementia and direct involvement of the hippocampus and amygdala in Parkinson's disease. Neurology 1997 49 6 1570 1576 10.1212/WNL.49.6.1570 2-s2.0-0031454241 (Pubitemid 28015119)
65. Calabresi P., Castrioto A., di Filippo M., Picconi B., New experimental and clinical links between the hippocampus and the dopaminergic system in Parkinson's disease. The Lancet Neurology 2013 12 8 811 821 10.1016/S1474- 4422(13)70118-2 2-s2.0-84880383782
66. Carlesimo G. A., Piras F., Assogna F., Pontieri F. E., Caltagirone C., Spalletta G., Hippocampal abnormalities and memory deficits in Parkinson disease: a multimodal imaging study. Neurology 2012 78 24 1939 1945 10.1212/WNL.0b013e318259e1c5 2-s2.0-84863593338
67. Schober A., Classic toxin-induced animal models of Parkinson's disease: 6-OHDA and MPTP. Cell and Tissue Research 2004 318 1 215 224 10.1007/s00441-004-0938-y 2-s2.0-5544229693 (Pubitemid 39366054)
68. Sui Y., Horne M. K., Stanić D., Reduced proliferation in the adult mouse subventricular zone increases survival of olfactory bulb interneurons. PLoS ONE 2012 7 2 e31549 10.1371/journal.pone.0031549 2-s2.0-84857406555
69. Winner B., Desplats P., Hagl C., Klucken J., Aigner R., Ploetz S., Laemke J., Karl A., Aigner L., Masliah E., Buerger E., Winkler J., Dopamine receptor activation promotes adult neurogenesis in an acute Parkinson model. Experimental Neurology 2009 219 2 543 552 10.1016/j.expneurol.2009.07.013 2-s2.0-69749092694
70. Iwakura Y., Piao Y., Mizuno M., Takei N., Kakita A., Takahashi H., Nawa H., Influences of dopaminergic lesion on epidermal growth factor-ErbB signals in Parkinson's disease and its model: neurotrophic implication in nigrostriatal neurons. Journal of Neurochemistry 2005 93 4 974 983 10.1111/j.1471-4159.2005. 03073.x 2-s2.0-18844406976 (Pubitemid 40695756)
71. Kuhn H. G., Winkler J., Kempermann G., Thal L. J., Gage F. H., Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. Journal of Neuroscience 1997 17 15 5820 5829 2-s2.0-0030809453 (Pubitemid 27310497)
72. Winner B., Couillard-Despres S., Geyer M., Aigner R., Bogdahn U., Aigner L., Kuhn H. G., Winkler J., Dopaminergic lesion enhances growth factor-induced striatal neuroblast migration. Journal of Neuropathology and Experimental Neurology 2008 67 2 105 116 10.1097/nen.0b013e3181630cff 2-s2.0-42949136458
73. Aponso P. M., Faull R. L. M., Connor B., Increased progenitor cell proliferation and astrogenesis in the partial progressive 6-hydroxydopamine model of Parkinson's disease. Neuroscience 2008 151 4 1142 1153 10.1016/j.neuroscience.2007.11.036 2-s2.0-39149132799
74. Liu B. F., Gao E. J., Zeng X. Z., Ji M., Cai Q., Lu Q., Yang H., Xu Q. Y., Proliferation of neural precursors in the subventricular zone after chemical lesions of the nigrostriatal pathway in rat brain. Brain Research 2006 1106 1 30 39 10.1016/j.brainres.2006.05.111 2-s2.0-33746771344 (Pubitemid 44163313)
75. Xi J. H., Nakayama H., Dong M., Yamauchi H., Ueno M., Uetsuka K., Doi K., Evidence of apoptosis in the subventricular zone and rostral migratory stream in the MPTP mouse model of Parkinson disease. Journal of Neuropathology and Experimental Neurology 2006 65 9 873 882 10.1097/01.jnen.0000235115.29440.ce 2-s2.0-33748552016 (Pubitemid 44371233)
76. He X. J., Yamauchi H., Uetsuka K., Nakayama H., Neurotoxicity of MPTP to migrating neuroblasts: Studies in acute and subacute mouse models of Parkinson's disease. NeuroToxicology 2008 29 3 413 420 10.1016/j.neuro.2008.02.007 2-s2.0-44649154416
77. Yamada M., Onodera M., Mizuno Y., Mochizuki H., Neurogenesis in olfactory bulb identified by retroviral labeling in normal and 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine-treated adult mice. Neuroscience 2004 124 1 173 181 10.1016/j.neuroscience.2003.10.040 2-s2.0-0442323568 (Pubitemid 38186627)
78. Peng J., Xie L., Jin K., Greenberg D. A., Andersen J. K., 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 3 664 670 10.1016/j.neuroscience.2008.02.063 2-s2.0-43049113827
79. Peng J., Andersen J. K., Mutant α -Synuclein and aging reduce neurogenesis in the acute 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. Aging Cell 2011 10 2 255 262 10.1111/j.1474-9726.2010. 00656.x 2-s2.0-79952584387
80. Dawson T. M., Ko H. S., Dawson V. L., Genetic animal models of Parkinson's disease. Neuron 2010 66 5 646 661 10.1016/j.neuron.2010.04.034 2-s2.0-77953666105
81. Kahle P. J., α -Synucleinopathy models and human neuropathology: similarities and differences. Acta Neuropathologica 2008 115 1 87 95 10.1007/s00401-007-0302-x 2-s2.0-36949031267 (Pubitemid 350238669)
82. Melrose H. L., Lincoln S. J., Tyndall G. M., Farrer M. J., Parkinson's disease: a rethink of rodent models. Experimental Brain Research 2006 173 2 196 204 10.1007/s00221-006-0461-3 2-s2.0-33747591029 (Pubitemid 44264883)
83. Rockenstein E., Crews L., Masliah E., Transgenic animal models of neurodegenerative diseases and their application to treatment development. Advanced Drug Delivery Reviews 2007 59 11 1093 1102 10.1016/j.addr.2007.08.013 2-s2.0-35348932113 (Pubitemid 47615209)
84. Campbell B. C. V., Li Q., Culvenor J. G., Jäkälä P., Cappai R., Beyreuther K., Masters C. L., McLean C. A., Accumulation of insoluble α -Synuclein in dementia with Lewy bodies. Neurobiology of Disease 2000 7 3 192 200 10.1006/nbdi.2000.0286 2-s2.0-0034210668 (Pubitemid 30451033)
85. Iwai A., Yoshimoto M., Masliah E., Saitoh T., Non-A β component of Alzheimer's disease amyloid (NAC) is amyloidogenic. Biochemistry 1995 34 32 10139 10145 10.1021/bi00032a006 2-s2.0-0028984925
86. Chartier-Harlin M., Kachergus J., Roumier C., Mouroux V., Douay X., Lincoln S., Levecque C., Larvor L., Andrieux J., Hulihan M., Waucquier N., Defebvre L., Amouyel P., Farrer M., Destée A., α -Synuclein locus duplication as a cause of familial Parkinson's disease. The Lancet 2004 364 9440 1167 1169 10.1016/S0140-6736(04)17103-1 2-s2.0-4644290985 (Pubitemid 39296604)
87. Kiely A. P., Asi Y. T., Kara E., Limousin P., Ling H., Lewis P., Proukakis C., Quinn N., Lees A. J., Hardy J., Revesz T., Houlden H., Holton J. L., α -Synucleinopathy associated with G51D SNCA mutation: a link between Parkinson's disease and multiple system atrophy? Acta Neuropathologica 2013 125 5 753 769 10.1007/s00401-013-1096-7 2-s2.0-84873493462
88. Krüger R., Kuhn W., Müller T., Woitalla D., Graeber M., Kösel S., Przuntek H., Epplen J. T., Schöls L., Riess O., AlaSOPro mutation in the gene encoding α -Synuclein in Parkinson's disease. Nature Genetics 1998 18 2 106 108 10.1038/ng0298-106 2-s2.0-0031990490
89. Polymeropoulos M. H., Lavedan C., Leroy E., Ide S. E., Dehejia A., Dutra A., Pike B., Root H., Rubenstein J., Boyer R., Stenroos E. S., Chandrasekharappa S., Athanassiadou A., Papapetropoulos T., Johnson W. G., Lazzarini A. M., Duvoisin R. C., Di Iorio G., Golbe L. I., Nussbaum R. L., Mutation in the α -Synuclein gene identified in families with Parkinson's disease. Science 1997 276 5321 2045 2047 10.1126/science.276.5321.2045 2-s2.0-0030744876 (Pubitemid 27443610)
90. Proukakis C., Dudzik C. G., Brier T., MacKay D. S., Cooper J. M., Millhauser G. L., Houlden H., Schapira A. H., A novel α -Synuclein missense mutation in Parkinson disease. Neurology 2013 80 11 1062 1064 10.1212/WNL.0b013e31828727ba 2-s2.0-84876226920
91. Singleton A. B., Farrer M., Johnson J., Hague S., Kachergus J., Hulihan M., Peuralinna T., Dutra A., Nussbaum R., Lincoln S., Crawley A., Hanson M., Maraganore D., Adler C., Cookson M. R., Muenter M., Baptista M., Miller D., Blancato J., Hardy J., Gwinn-Hardy K., α -Synuclein locus triplication causes Parkinson's disease. Science 2003 302 5646 841 10.1126/science.1090278 2-s2.0-0242300619 (Pubitemid 37339619)
92. Zarranz J. J., Alegre J., Gómez-Esteban J. C., Lezcano E., Ros R., Ampuero I., Vidal L., Hoenicka J., Rodriguez O., Atarés B., Llorens V., Gomez Tortosa E., Del Ser T., Muñoz D. G., De Yebenes J. G., The New Mutation, E46K, of α -Synuclein Causes Parkinson and Lewy Body Dementia. Annals of Neurology 2004 55 2 164 173 10.1002/ana.10795 2-s2.0-10744230149 (Pubitemid 38166992)
93. Satake W., Nakabayashi Y., Mizuta I., Hirota Y., Ito C., Kubo M., Kawaguchi T., Tsunoda T., Watanabe M., Takeda A., Tomiyama H., Nakashima K., Hasegawa K., Obata F., Yoshikawa T., Kawakami H., Sakoda S., Yamamoto M., Hattori N., Murata M., Nakamura Y., Toda T., Genome-wide association study identifies common variants at four loci as genetic risk factors for Parkinson's disease. Nature Genetics 2009 41 12 1303 1307 10.1038/ng.485 2-s2.0-70549084415
94. Simón-Sánchez J., Schulte C., Bras J. M., Genome-wide association study reveals genetic risk underlying Parkinson's disease. Nature Genetics 2009 41 12 1308 1312 10.1038/ng.487
95. Masliah E., Rockenstein E., Veinbergs I., Mallory M., Hashimoto M., Takeda A., Sagara Y., Sisk A., Mucke L., Dopaminergic loss and inclusion body formation in α -Synuclein mice: implications for neurodegenerative disorders. Science 2000 287 5456 1265 1269 10.1126/science.287.5456.1265 2-s2.0-0034681471 (Pubitemid 30112148)
96. Masliah E., Rockenstein E., Mante M., Crews L., Spencer B., Adame A., Patrick C., Trejo M., Ubhi K., Rohn T. T., Mueller-Steiner S., Seubert P., Barbour R., McConlogue L., Buttini M., Games D., Schenk D., Passive immunization reduces behavioral and neuropathological deficits in an alpha-synuclein transgenic model of lewy body disease. PLoS ONE 2011 6 4 e19338 10.1371/journal.pone.0019338 2-s2.0-79955757052
97. Winner B., Lie D. C., Rockenstein E., Aigner R., Aigner L., Masliah E., Kuhn H. G., Winkler J., Human wild-type α -Synuclein impairs neurogenesis. Journal of Neuropathology and Experimental Neurology 2004 63 11 1155 1166 2-s2.0-8544232135 (Pubitemid 39492021)
98. Winner B., Rockenstein E., Lie D. C., Aigner R., Mante M., Bogdahn U., Couillard-Despres S., Masliah E., Winkler J., Mutant α -Synuclein exacerbates age-related decrease of neurogenesis. Neurobiology of Aging 2008 29 6 913 925 10.1016/j.neurobiolaging.2006.12.016 2-s2.0-42649103331 (Pubitemid 351601896)
99. Kohl Z., Winner B., Ubhi K., Rockenstein E., Mante M., Münch M., Barlow C., Carter T., Masliah E., Winkler J., Fluoxetine rescues impaired hippocampal neurogenesis in a transgenic A53T synuclein mouse model. European Journal of Neuroscience 2012 35 1 10 19 10.1111/j.1460-9568.2011.07933.x 2-s2.0-84855278236
100. Nuber S., Petrasch-Parwez E., Winner B., Winkler J., Von Hörsten S., Schmidt T., Boy J., Kuhn M., Nguyen H. P., Teismann P., Schulz J. B., Neumann M., Pichler B. J., Reischl G., Holzmann C., Schmitt I., Bornemann A., Kuhn W., Zimmermann F., Servadio A., Riess O., Neurodegeneration and motor dysfunction in a conditional model of Parkinson's disease. Journal of Neuroscience 2008 28 10 2471 2484 10.1523/JNEUROSCI.3040-07.2008 2-s2.0-40449139321 (Pubitemid 351348209)
101. Marxreiter F., Nuber S., Kandasamy M., Klucken J., Aigner R., Burgmayer R., Couillard-Despres S., Riess O., Winkler J., Winner B., Changes in adult olfactory bulb neurogenesis in mice expressing the A30P mutant form of alpha-synuclein. European Journal of Neuroscience 2009 29 5 879 890 10.1111/j.1460-9568.2009.06641.x 2-s2.0-61449087466
102. Marxreiter F., Ettle B., May V. E. L., Esmer H., Patrick C., Kragh C. L., Klucken J., Winner B., Riess O., Winkler J., Masliah E., Nuber S., Glial A30P α -Synuclein pathology segregates neurogenesis from anxiety-related behavior in conditional transgenic mice. Neurobiology of Disease 2013 59 38 51 10.1016/j.nbd.2013.07.004 2-s2.0-84881113966
103. May V. E. L., Nuber S., Marxreiter F., Riess O., Winner B., Winkler J., Impaired olfactory bulb neurogenesis depends on the presence of human wild-type alpha-synuclein. Neuroscience 2012 222 343 355 10.1016/j.neuroscience.2012.07. 001 2-s2.0-84865623919
104. Conway K. A., Rochet J. S., Ding T. T., Harper J. D., Williamson R. E., Lansbury P. T. Jr., Accelerated oligomerization by Parkinson's disease linked α -Synuclein mutants. Annals of the New York Academy of Sciences 2000 920 42 45 2-s2.0-0034528027 (Pubitemid 32056550)
105. Danzer K. M., Krebs S. K., Wolff M., Birk G., Hengerer B., Seeding induced by α -Synuclein oligomers provides evidence for spreading of α -Synuclein pathology. Journal of Neurochemistry 2009 111 1 192 203 10.1111/j.1471-4159.2009.06324.x 2-s2.0-70349223775
106. Desplats P. J., Lee H. J., Bae E., Patrick C., Rockenstein E., Crews L., Spencer B., Masliah E., Lee S., Inclusion formation and neuronal cell death through neuron-to-neuron transmission of α -Synuclein. Proceedings of the National Academy of Sciences of the United States of America 2009 106 31 13010 13015 10.1073/pnas.0903691106 2-s2.0-69149089854
107. Lee H.-J., Suk J.-E., Patrick C., Bae E.-J., Cho J.-H., Rho S., Hwang D., Masliah E., Lee S.-J., Direct transfer of α -Synuclein from neuron to astroglia causes inflammatory responses in synucleinopathies. The Journal of Biological Chemistry 2010 285 12 9262 9272 10.1074/jbc.M109.081125 2-s2.0-77950571596
108. Winner B., Vogt-Weisenhorn D. M., Lie C. D., Blümcke I., Winkler J., Cellular repair strategies in Parkinson's disease. Therapeutic Advances in Neurological Disorders 2009 2 1 51 60 10.1177/1756285608100324 2-s2.0-70449645446
109. Brundin P., Melki R., Kopito R., Prion-like transmission of protein aggregates in neurodegenerative diseases. Nature Reviews Molecular Cell Biology 2010 11 4 301 307 10.1038/nrm2873 2-s2.0-77949848854
110. Nuber S., Harmuth F., Kohl Z., Adame A., Trejo M., Schönig K., Zimmermann F., Bauer C., Casadei N., Giel C., Calaminus C., Pichler B. J., Jensen P. H., Müller C. P., Amato D., Kornhuber J., Teismann P., Yamakado H., Takahashi R., Winkler J., Masliah E., Riess O., A progressive dopaminergic phenotype associated with neurotoxic conversion of α -Synuclein in BAC-transgenic rats. Brain 2013 136 2 412 432 10.1093/brain/aws358 2-s2.0-84874335392
111. Crews L., Mizuno H., Desplats P., Rockenstein E., Adame A., Patrick C., Winner B., Winkler J., Masliah E., α -Synuclein alters Notch-1 expression and neurogenesis in mouse embryonic stem cells and in the hippocampus of transgenic mice. The Journal of Neuroscience 2008 28 16 4250 4260 10.1523/JNEUROSCI.0066-08.2008 2-s2.0-42949133399
112. Desplats P., Spencer B., Crews L., Pathel P., Morvinski-Friedmann D., Kosberg K., Roberts S., Patrick C., Winner B., Winkler J., Masliah E., α -Synuclein induces alterations in adult neurogenesis in Parkinson disease models via p53-mediated repression of notch. The Journal of Biological Chemistry 2012 287 38 31691 31702 10.1074/jbc.M112.354522 2-s2.0-84866405384
113. Danzer K. M., Haasen D., Karow A. R., Moussaud S., Habeck M., Giese A., Kretzschmar H., Hengerer B., Kostka M., Different species of α -Synuclein oligomers induce calcium influx and seeding. Journal of Neuroscience 2007 27 34 9220 9232 10.1523/JNEUROSCI.2617-07.2007 2-s2.0-34548172773 (Pubitemid 47312071)
114. Winner B., Jappelli R., Maji S. K., Desplats P. A., Boyer L., Aigner S., Hetzer C., Loher T., Vilar M., Campioni S., Tzitzilonis C., Soragni A., Jessberger S., Mira H., Consiglio A., Pham E., Masliah E., Gage F. H., Riek R., In vivo demonstration that α -Synuclein oligomers are toxic. Proceedings of the National Academy of Sciences of the United States of America 2011 108 10 4194 4199 10.1073/pnas.1100976108 2-s2.0-79952742454
115. Rockenstein E., Nuber S., Overk C. R., Accumulation of oligomer-prone α -Synuclein exacerbates synaptic and neuronal degeneration in vivo. Brain 2014 10.1093/brain/awu057
116. Zhao C., Deng W., Gage F. H., Mechanisms and functional implications of adult neurogenesis. Cell 2008 132 4 645 660 10.1016/j.cell.2008.01.033 2-s2.0-39149107803 (Pubitemid 351253687)
117. Toni N., Sultan S., Synapse formation on adult-born hippocampal neurons. European Journal of Neuroscience 2011 33 6 1062 1068 10.1111/j.1460-9568.2011. 07604.x 2-s2.0-79952585214
118. Prots I., Veber V., Brey S., Campioni S., Buder K., Riek R., Böhm K. J., Winner B., α -Synuclein oligomers impair neuronal microtubule-kinesin interplay. Journal of Biological Chemistry 2013 288 30 21742 21754 10.1074/jbc.M113.451815 2-s2.0-84881259462
119. McNeill T. H., Brown S. A., Rafols J. A., Shoulson I., Atrophy of medium spiny I striatal dendrites in advanced Parkinson's disease. Brain Research 1988 455 1 148 152 10.1016/0006-8993(88)90124-2 2-s2.0-0023943663
120. Games D., Seubert P., Rockenstein E., Patrick C., Trejo M., Ubhi K., Ettle B., Ghassemiam M., Barbour R., Schenk D., Nuber S., Masliah E., Axonopathy in an α -Synuclein transgenic model of Lewy body disease is associated with extensive accumulation of c-terminal-truncated α -Synuclein. The American Journal of Pathology 2013 182 3 940 953 10.1016/j.ajpath.2012.11.018 2-s2.0-84874510614
121. Kramer M. L., Schulz-Schaeffer W. J., Presynaptic α -Synuclein aggregates, not Lewy bodies, cause neurodegeneration in dementia with lewy bodies. Journal of Neuroscience 2007 27 6 1405 1410 10.1523/JNEUROSCI.4564-06. 2007 2-s2.0-33846997878
122. Schulz-Schaeffer W. J., The synaptic pathology of α -Synuclein aggregation in dementia with Lewy bodies, Parkinson's disease and Parkinson's disease dementia. Acta Neuropathologica 2010 120 2 131 143 10.1007/s00401-010- 0711-0 2-s2.0-77957264418
123. Scott D. A., Tabarean I., Tang Y., Cartier A., Masliah E., Roy S., A pathologic cascade leading to synaptic dysfunction in α -Synuclein-induced neurodegeneration. Journal of Neuroscience 2010 30 24 8083 8095 10.1523/JNEUROSCI.1091-10.2010 2-s2.0-77953796839
124. Lashuel H. A., Overk C. R., Oueslati A., Masliah E., The many faces of α -Synuclein: from structure and toxicity to therapeutic target. Nature Reviews Neuroscience 2013 14 1 38 48 10.1038/nrn3406 2-s2.0-84871414210
125. Clayton D. F., George J. M., The synucleins: a family of proteins involved in synaptic function, plasticity, neurodegeneration and disease. Trends in Neurosciences 1998 21 6 249 254 10.1016/S0166-2236(97)01213-7 2-s2.0-0032102455 (Pubitemid 28239982)
126. Abeliovich A., Schmitz Y., Fariñas I., Choi-Lundberg D., Ho W., Castillo P. E., Shinsky N., Garcia Verdugo J. M., Armanini M., Ryan A., Hynes M., Phillips H., Sulzer D., Rosenthal A., Mice lacking α -Synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 2000 25 1 239 252 10.1016/S0896-6273(00)80886-7 2-s2.0-0034077041 (Pubitemid 30316525)
127. Chandra S., Fornai F., Kwon H., Yazdani U., Atasoy D., Liu X., Hammer R. E., Battaglia G., German D. C., Castillo P. E., Südhof T. C., Double-knockout mice for α-and β -synucleins: effect on synaptic functions. Proceedings of the National Academy of Sciences of the United States of America 2004 101 41 14966 14971 10.1073/pnas.0406283101 2-s2.0-6944227811 (Pubitemid 39410782)
128. Murphy D. D., Rueter S. M., Trojanowski J. Q., Lee V. M., Synucleins are developmentally expressed, and α -Synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. Journal of Neuroscience 2000 20 9 3214 3220 2-s2.0-0034193399 (Pubitemid 30263139)
129. Chandra S., Gallardo G., Fernández-Chacón R., Schlüter O. M., Südhof T. C., α -Synuclein cooperates with CSP α in preventing neurodegeneration. Cell 2005 123 3 123 383 10.1016/j.cell.2005.09.028 (Pubitemid 41546670)
130. Gorbatyuk O. S., Li S., Nash K., Gorbatyuk M., Lewin A. S., Sullivan L. F., Mandel R. J., Chen W., Meyers C., Manfredsson F. P., Muzyczka N., In vivo RNAi-mediated alpha-synuclein silencing induces nigrostriatal degeneration. Molecular Therapy 2010 18 8 1450 1457 10.1038/mt.2010.115 2-s2.0-77955176216
131. Mu Y., Zhao C., Gage F. H., Dopaminergic modulation of cortical inputs during maturation of adult-born dentate granule cells. Journal of Neuroscience 2011 31 11 4113 4123 10.1523/JNEUROSCI.4913-10.2011 2-s2.0-79952767355
132. Zimprich A., Biskup S., Leitner P., Lichtner P., Farrer M., Lincoln S., Kachergus J., Hulihan M., Uitti R. J., Calne D. B., Stoessl A. J., Pfeiffer R. F., Patenge N., Carbajal I. C., Vieregge P., Asmus F., Müller-Myhsok B., Dickson D. W., Meitinger T., Strom T. M., Wszolek Z. K., Gasser T., Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron 2004 44 4 601 607 10.1016/j.neuron.2004.11.005 2-s2.0-8844233579 (Pubitemid 39531225)
133. Mata I. F., Ross O. A., Kachergus J., Huerta C., Ribacoba R., Moris G., Blazquez M., Guisasola L. M., Salvador C., Martinez C., Farrer M., Alvarez V., LRRK2 mutations are a common cause of Parkinson's disease in Spain. The European Journal of Neurology 2006 13 4 391 394 10.1111/j.1468-1331.2006.01256.x 2-s2.0-33646048034
134. Ross O. A., Toft M., Whittle A. J., Johnson J. L., Papapetropoulos S., Mash D. C., Litvan I., Gordon M. F., Wszolek Z. K., Farrer M. J., Dickson D. W., Lrrk2 and Lewy body disease. Annals of Neurology 2006 59 2 388 393 10.1002/ana.20731 2-s2.0-32044466285 (Pubitemid 43202496)
135. Healy D. G., Falchi M., O'Sullivan S. S., Bonifati V., Durr A., Bressman S., Brice A., Aasly J., Zabetian C. P., Goldwurm S., Ferreira J. J., Tolosa E., Kay D. M., Klein C., Williams D. R., Marras C., Lang A. E., Wszolek Z. K., Berciano J., Schapira A. H., Lynch T., Bhatia K. P., Gasser T., Lees A. J., Wood N. W., Phenotype, genotype, and worldwide genetic penetrance of LRRK2-associated Parkinson's disease: a case-control study. The Lancet Neurology 2008 7 7 583 590 10.1016/S1474-4422(08)70117-0 2-s2.0-50049104725
136. Melrose H. L., Dächsel J. C., Behrouz B., Lincoln S. J., Yue M., Hinkle K. M., Kent C. B., Korvatska E., Taylor J. P., Witten L., Liang Y.-., Beevers J. E., Boules M., Dugger B. N., Serna V. A., Gaukhman A., Yu X., Castanedes-Casey M., Braithwaite A. T., Ogholikhan S., Yu N., Bass D., Tyndall G., Schellenberg G. D., Dickson D. W., Janus C., Farrer M. J., Impaired dopaminergic neurotransmission and microtubule-associated protein tau alterations in human LRRK2 transgenic mice. Neurobiology of Disease 2010 40 3 503 517 10.1016/j.nbd.2010.07.010 2-s2.0-77957794336
137. Winner B., Melrose H. L., Zhao C., Hinkle K. M., Yue M., Kent C., Braithwaite A. T., Ogholikhan S., Aigner R., Winkler J., Farrer M. J., Gage F. H., Adult neurogenesis and neurite outgrowth are impaired in LRRK2 G2019S mice. Neurobiology of Disease 2011 41 3 706 716 10.1016/j.nbd.2010.12.008 2-s2.0-79151473945
138. Sakaguchi-Nakashima A., Meir J. Y., Jin Y., Matsumoto K., Hisamoto N., LRK-1, a C. elegans PARK8-Related Kinase, Regulates Axonal-Dendritic Polarity of SV Proteins. Current Biology 2007 17 7 592 598 10.1016/j.cub.2007.01.074 2-s2.0-33947663512 (Pubitemid 46497793)
139. Cherra S. J. III, Steer E., Gusdon A. M., Kiselyov K., Chu C. T., Mutant LRRK2 elicits calcium imbalance and depletion of dendritic mitochondria in neurons. The American Journal of Pathology 2013 182 2 474 484 10.1016/j.ajpath.2012.10.027 2-s2.0-84872691988
140. Paus M., Kohl Z., Ben Abdallah N. M.-B., Galter D., Gillardon F., Winkler J., Enhanced dendritogenesis and axogenesis in hippocampal neuroblasts of LRRK2 knockout mice. Brain Research 2013 1497 85 100 10.1016/j.brainres.2012.12.024 2-s2.0-84873095084
141. Gallagher D. A., Lees A. J., Schrag A., What are the most important nonmotor symptoms in patients with Parkinson's disease and are we missing them? Movement Disorders 2010 25 15 2493 2500 10.1002/mds.23394 2-s2.0-78349236177
142. Czéh B., Michaelis T., Watanabe T., Frahm J., De Biurrun G., Van Kampen M., Bartolomucci A., Fuchs E., Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proceedings of the National Academy of Sciences of the United States of America 2001 98 22 12796 12801 10.1073/pnas.211427898 2-s2.0-0035940496 (Pubitemid 33020024)
143. Malberg J. E., Eisch A. J., Nestler E. J., Duman R. S., Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. Journal of Neuroscience 2000 20 24 9104 9110 2-s2.0-0034671366 (Pubitemid 32042912)
144. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., Weisstaub N., Lee J., Duman R., Arancio O., Belzung C., Hen R., Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003 301 5634 805 809 10.1126/science.1083328 2-s2.0-0042528720 (Pubitemid 36962615)
145. Eisch A. J., Petrik D., Depression and hippocampal neurogenesis: a road to remission? Science 2012 338 6103 72 75 10.1126/science.1222941 2-s2.0-84867213664
146. Lee M. M., Reif A., Schmitt A. G., Major Depression: A Role for Hippocampal Neurogenesis? Current Topics in Behavioral Neurosciences 2013 14 153 179 10.1007/7854-2012-226 2-s2.0-84880056448
147. Lucassen P. J., Pruessner J., Sousa N., Neuropathology of stress. Acta Neuropathologica 2014 127 109 135 10.1007/s00401-013-1223-5
148. Tang S. W., Helmeste D., Leonard B., Is neurogenesis relevant in depression and in the mechanism of antidepressant drug action? A critical review. World Journal of Biological Psychiatry 2012 13 6 402 412 10.3109/15622975.2011.639800 2-s2.0-84865208083
149. Huang Y., Coupland N. J., Lebel R. M., Carter R., Seres P., Wilman A. H., Malykhin N. V., Structural changes in hippocampal subfields in major depressive disorder: A high-field magnetic resonance imaging study. Biological Psychiatry 2013 74 1 62 68 10.1016/j.biopsych.2013.01.005 2-s2.0-84879290334
150. Boldrini M., Santiago A. N., Hen R., Dwork A. J., Rosoklija G. B., Tamir H., Arango V., John Mann J., Hippocampal granule neuron number and dentate gyrus volume in antidepressant-treated and untreated major depression. Neuropsychopharmacology 2013 38 6 1068 1077 10.1038/npp.2013.5 2-s2.0-84878614671
151. Reichmann H., Schneider C., Löhle M., Non-motor features of Parkinson's disease: depression and dementia. Parkinsonism & Related Disorders 2009 15 supplement 3 S87 S92 10.1016/S1353-8020(09)70789-8 2-s2.0-71849116135
152. Clelland C. D., Choi M., Romberg C., Clemenson G. D. Jr., Fragniere A., Tyers P., Jessberger S., Saksida L. M., Barker R. A., Gage F. H., Bussey T. J., A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 2009 325 5937 210 213 10.1126/science.1173215 2-s2.0-67650450542
153. Rangel L. M., Alexander A. S., Aimone J. B., Temporally selective contextual encoding in the dentate gyrus of the hippocampus. Nature Communications 2014 5, article 3181 10.1038/ncomms4181
154. Winner B., Kohl Z., Gage F. H., Neurodegenerative disease and adult neurogenesis. European Journal of Neuroscience 2011 33 6 1139 1151 10.1111/j.1460-9568.2011.07613.x 2-s2.0-79952579942
155. Frim D. M., Uhler T. A., Galpern W. R., Beal M. F., Breakefield X. O., Isacson O., Implanted fibroblasts genetically engineered to produce brain-derived neurotrophic factor prevent 1-methyl-4-phenylpyridinium toxicity to dopaminergic neurons in the rat. Proceedings of the National Academy of Sciences of the United States of America 1994 91 11 5104 5108 10.1073/pnas.91.11.5104 2-s2.0-0028276809 (Pubitemid 24177801)
156. Lang A. E., Gill S., Patel N. K., Lozano A., Nutt J. G., Penn R., Brooks D. J., Hotton G., Moro E., Heywood P., Brodsky M. A., Burchiel K., Kelly P., Dalvi A., Scott B., Stacy M., Turner D., Wooten V. G. F., Elias W. J., Laws E. R., Dhawan V., Stoessl A. J., Matcham J., Coffey R. J., Traub M., Randomized controlled trial of intraputamenal glial cell line-derived neurotrophic factor infusion in Parkinson disease. Annals of Neurology 2006 59 3 459 466 10.1002/ana.20737 2-s2.0-33644833272 (Pubitemid 43358066)
157. Levivier M., Przedborski S., Bencsics C., Kang U. J., Intrastriatal implantation of fibroblasts genetically engineered to produce brain-derived neurotrophic factor prevents degeneration of dopaminergic neurons in a rat model of Parkinson's disease. The Journal of Neuroscience 1995 15 12 7810 7820 2-s2.0-0029610630 (Pubitemid 26006890)
158. Ubhi K., Inglis C., Mante M., Patrick C., Adame A., Spencer B., Rockenstein E., May V., Winkler J., Masliah E., Fluoxetine ameliorates behavioral and neuropathological deficits in a transgenic model mouse of α -Synucleinopathy. Experimental Neurology 2012 234 2 405 416 10.1016/j.expneurol.2012.01.008 2-s2.0-84858157780
159. Wang S. H., Zhang Z. J., Guo Y. J., Sui Y. X., Sun Y., Notch1 signaling related hippocampal neurogenesis in adult poststroke depression rats: a valid index for an efficient combined citalopram and WAY100635 pharmacotherapy. Behavioural Pharmacology 2010 21 1 47 57 10.1097/FBP.0b013e328334b677 2-s2.0-74549158287
160. Pieper A. A., Xie S., Capota E., Estill S. J., Zhong J., Long J. M., Becker G. L., Huntington P., Goldman S. E., Shen C., Capota M., Britt J. K., Kotti T., Ure K., Brat D. J., Williams N. S., MacMillan K. S., Naidoo J., Melito L., Hsieh J., De Brabander J., Ready J. M., McKnight S. L., Discovery of a proneurogenic, neuroprotective chemical. Cell 2010 142 1 39 51 10.1016/j.cell.2010.06.018 2-s2.0-77954266958
161. Klempin F., Beis D., Mosienko V., Kempermann G., Bader M., Alenina N., Serotonin is required for exercise-induced adult hippocampal neurogenesis. Journal of Neuroscience 2013 33 19 8270 8275 10.1523/JNEUROSCI.5855-12.2013 2-s2.0-84877267860
162. Murray D. K., Sacheli M. A., Eng J. J., Stoessl A. J., The effects of exercise on cognition in Parkinson's disease: a systematic review. Translational Neurodegeneration 2014 3, article 5 10.1186/2047-9158-3-5
163. Kohl Z., Kandasamy M., Winner B., Aigner R., Gross C., Couillard-Despres S., Bogdahn U., Aigner L., Winkler J., Physical activity fails to rescue hippocampal neurogenesis deficits in the R6/2 mouse model of Huntington's disease. Brain Research 2007 1155 1 24 33 10.1016/j.brainres.2007.04.039 2-s2.0-34249986143 (Pubitemid 46891433)
164. Rugbjerg K., Friis S., Ritz B., Schernhammer E. S., Korbo L., Olsen J. H., Autoimmune disease and risk for Parkinson disease: a population-based case-control study. Neurology 2009 73 18 1462 1468 10.1212/WNL.0b013e3181c06635 2-s2.0-70449345919
165. Driver J. A., Logroscino G., Lu L., Gaziano J. M., Kurth T., Use of non-steroidal anti-inflammatory drugs and risk of Parkinson's disease: nested case-control study. British Medical Journal 2011 342 7791, article d198 10.1136/bmj.d198 2-s2.0-79251536194
166. Glass C. K., Saijo K., Winner B., Marchetto M. C., Gage F. H., Mechanisms underlying inflammation in neurodegeneration. Cell 2010 140 6 918 934 10.1016/j.cell.2010.02.016 2-s2.0-77950363010
167. Doorn K. J., Lucassen P. J., Boddeke H. W., Prins M., Berendse H. W., Drukarch B., van Dam A., Emerging roles of microglial activation and non-motor symptoms in Parkinson's disease. Progress in Neurobiology 2012 98 2 222 238 10.1016/j.pneurobio.2012.06.005 2-s2.0-84863487503
168. Doorn K. J., Goudriaan A., Blits-Huizinga C., Increased amoeboid microglial density in the olfactory bulb of Parkinson's and Alzheimer's patients. Brain Pathology 2014 24 2 152 165 10.1111/bpa.12088
169. Vroon A., Drukarch B., Bol J. G. J. M., Cras P., Brevé J. J. P., Allan S. M., Relton J. K., Hoogland P. V. J. M., Van Dam A., Neuroinflammation in Parkinson's patients and MPTP-treated mice is not restricted to the nigrostriatal system: microgliosis and differential expression of interleukin-1 receptors in the olfactory bulb. Experimental Gerontology 2007 42 8 762 771 10.1016/j.exger.2007.04.010 2-s2.0-34447328426 (Pubitemid 47058861)
170. Imamura K., Hishikawa N., Sawada M., Nagatsu T., Yoshida M., Hashizume Y., Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson's disease brains. Acta Neuropathologica 2003 106 6 518 526 10.1007/s00401-003-0766-2 2-s2.0-0344444234 (Pubitemid 37441607)
171. Monje M. L., Toda H., Palmer T. D., Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003 302 5651 1760 1765 10.1126/science. 1088417 2-s2.0-0345189366 (Pubitemid 37505739)
172. Ekdahl C. T., Claasen J.-H., Bonde S., Kokaia Z., Lindvall O., Inflammation is detrimental for neurogenesis in adult brain. Proceedings of the National Academy of Sciences of the United States of America 2003 100 23 13632 13637 10.1073/pnas.2234031100 2-s2.0-0344742225 (Pubitemid 37444791)
173. Ben-Hur T., Ben-Menachem O., Furer V., Einstein O., Mizrachi-Kol R., Grigoriadis N., Effects of proinflammatory cytokines on the growth, fate, and motility of multipotential neural precursor cells. Molecular and Cellular Neuroscience 2003 24 3 623 631 10.1016/S1044-7431(03)00218-5 2-s2.0-0344737625 (Pubitemid 37506007)
174. Reale M., Iarlori C., Thomas A., Gambi D., Perfetti B., Di Nicola M., Onofrj M., Peripheral cytokines profile in Parkinson's disease. Brain, Behavior, and Immunity 2009 23 1 55 63 10.1016/j.bbi.2008.07.003 2-s2.0-56849086964
175. Lindqvist D., Kaufman E., Brundin L., Hall S., Surova Y., Hansson O., Non-motor symptoms in patients with Parkinson's disease-correlations with inflammatory cytokines in serum. PLoS ONE 2012 7 10 e47387 10.1371/journal.pone. 0047387 2-s2.0-84867629199
176. Ekdahl C. T., Kokaia Z., Lindvall O., Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 2009 158 3 1021 1029 10.1016/j.neuroscience.2008.06.052 2-s2.0-59349110661
177. Kohman R. A., Rhodes J. S., Neurogenesis, inflammation and behavior. Brain, Behavior, and Immunity 2013 27 1 22 32 10.1016/j.bbi.2012.09.003 2-s2.0-84870740056
178. Sierra A., Beccari S., Diaz-Aparicio I., Encinas J. M., Comeau S., Tremblay M.-È., Surveillance, phagocytosis, and inflammation: how never-resting microglia influence adult hippocampal neurogenesis. Neural Plasticity 2014 2014 15 610343 10.1155/2014/610343
179. Ziv Y., Ron N., Butovsky O., Landa G., Sudai E., Greenberg N., Cohen H., Kipnis J., Schwartz M., Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nature Neuroscience 2006 9 2 268 275 10.1038/nn1629 2-s2.0-31544460682 (Pubitemid 43164551)
180. Vukovic J., Colditz M. J., Blackmore D. G., Ruitenberg M. J., Bartlett P. F., Microglia modulate hippocampal neural precursor activity in response to exercise and aging. Journal of Neuroscience 2012 32 19 6435 6443 10.1523/JNEUROSCI.5925-11.2012 2-s2.0-84860666072
181. Couillard-Despres S., Aigner L., In vivo imaging of adult neurogenesis. European Journal of Neuroscience 2011 33 6 1037 1044 10.1111/j.1460-9568.2011. 07601.x 2-s2.0-79952587418
182. Ho N. F., Hooker J. M., Sahay A., Holt D. J., Roffman J. L., In vivo imaging of adult human hippocampal neurogenesis: progress, pitfalls and promise. Molecular Psychiatry 2013 18 4 404 416 10.1038/mp.2013.8 2-s2.0-84874136726