Increased proliferation reflects glial and vascular-associated changes, but not neurogenesis in the presenile Alzheimer hippocampus

Neurobiology of Disease

Volumn 24, Issue 1, 2006, Pages 1-14

  Boekhoorn, Karin ^a   Joels, Marian ^a   Lucassen, Paul J ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Alzheimer; Doublecortin; GFAP; Hippocampus; Ki 67; Neurogenesis; Postmortem delay; Presenile dementia; Vasculature

Indexed keywords

AGED; ALZHEIMER DISEASE; ARTICLE; CELL PROLIFERATION; COHORT ANALYSIS; DENTATE GYRUS; FEMALE; GLIA CELL; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; NERVOUS SYSTEM DEVELOPMENT; PRESENILE DEMENTIA; PRIORITY JOURNAL; VASCULARIZATION;

AGED; ALZHEIMER DISEASE; ANTIMETABOLITES; BLOOD VESSELS; BROMODEOXYURIDINE; CELL PROLIFERATION; CEREBROVASCULAR CIRCULATION; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; KI-67 ANTIGEN; MALE; MIDDLE AGED; NERVE FIBERS; NEUROGLIA; NEURONS; TISSUE BANKS;

EID: 33748790666     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2006.04.017     Document Type: Article

References (76)

1. Abraham H., Tornoczky T., Kosztolanyi G., and Seress L. Cell proliferation correlates with the postconceptual and not with the postnatal age in the hippocampal dentate gyrus, temporal neocortex and cerebellar cortex of preterm infants. Early Hum. Dev. 78 (2004) 29-43
2. Akiyama H., Barger S., Barnum S., Bradt B., Bauer J., Cole G.M., Cooper N.R., Eikelenboom P., Emmerling M., Fiebich B.L., Finch C.E., Frautschy S., Griffin W.S., Hampel H., Hull M., Landreth G., Lue L., Mrak R., Mackenzie I.R., McGeer P.L., O'Banion M.K., Pachter J., Pasinetti G., Plata-Salaman C., Rogers J., Rydel R., Shen Y., Streit W., Strohmeyer R., Tooyoma I., Van Muiswinkel F.L., Veerhuis R., Walker D., Webster S., Wegrzyniak B., Wenk G., and Wyss-Coray T. Inflammation and Alzheimer's disease. Neurobiol. Aging 21 (2000) 383-421
3. Arendt T., Rodel L., Gartner U., and Holzer M. Expression of the cyclin-dependent kinase inhibitor p16 in Alzheimer's disease. NeuroReport 7 (1996) 3047-3049
4. Blumcke I., Schewe J.C., Normann S., Brustle O., Schramm J., Elger C.E., and Wiestler O.D. Increase of nestin-immunoreactive neural precursor cells in the dentate gyrus of pediatric patients with early-onset temporal lobe epilepsy. Hippocampus 11 (2001) 311-321
5. Bobinski M., Wegiel J., Tarnawski M., Reisberg B., de Leon M.J., Miller D.C., and Wisniewski H.M. Relationships between regional neuronal loss and neurofibrillary changes in the hippocampal formation and duration and severity of Alzheimer disease. J. Neuropathol. Exp. Neurol. 56 (1997) 414-420
6. Boekhoorn K., Terwel D., Biemans B., Borghgraef P., Wiegert O., Ramakers G.J., de Vos K., Krugers H., Tomiyama T., Mori H., Joels M., van Leuven F., and Lucassen P.J. Improved long-term potentiation and memory in young tau-P301L transgenic mice before onset of hyperphosphorylation and tauopathy. J. Neurosci. 26 (2006) 3514-3523
7. Bondolfi L., Calhoun M., Ermini F., Kuhn H.G., Wiederhold K.H., Walker L., Staufenbiel M., Jucker M., et al. Amyloid-associated neuron loss and gliogenesis in the neocortex of amyloid precursor protein transgenic mice. J. Neurosci. 22 (2002) 515-522
8. Bowers D.C., Gargan L., Kapur P., Reisch J.S., Mulne A.F., Shapiro K.N., Elterman R.D., Winick N.J., and Margraf L.R. Study of the MIB-1 labeling index as a predictor of tumor progression in pilocytic astrocytomas in children and adolescents. J. Clin. Oncol. 21 (2003) 2968-2973
9. Braak H., and Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82 (1991) 239-259
10. Brown J.P., Couillard-Despres S., Cooper-Kuhn C.M., Winkler J., Aigner L., and Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 467 (2003) 1-10
11. Busser J., Geldmacher D.S., and Herrup K. Ectopic cell cycle proteins predict the sites of neuronal cell death in Alzheimer's disease brain. J. Neurosci. 18 (1998) 2801-2807
12. Cantara S., Donnini S., Morbidelli L., Giachetti A., Schulz R., Memo M., and Ziche M. Physiological levels of amyloid peptides stimulate the angiogenic response through FGF-2. FASEB J. 18 (2004) 1943-1945
13. Castellani R.J., Smith M.A., Perry G., and Friedland R.P. Cerebral amyloid angiopathy: major contributor or decorative response to Alzheimer's disease pathogenesis. Neurobiol. Aging 25 (2004) 599-602
14. Chevallier N.L., Soriano S., Kang D.E., Masliah E., Hu G., and Koo E.H. Perturbed neurogenesis in the adult hippocampus associated with presenilin-1 A246E mutation. Am. J. Pathol. 167 (2005) 151-159
15. Couillard-Despres S., Winner B., Schaubeck S., Aigner R., Vroemen M., Weidner N., Bogdahn U., Winkler J., Kuhn H.G., and Aigner L. Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci. 21 (2005) 1-14
16. Covolan L., Ribeiro L.T., Longo B.M., Mello L.E., et al. Cell damage and neurogenesis in the dentate granule cell layer of adult rats after pilocarpine- or kainate-induced status epilepticus. Hippocampus 10 (2000) 169-180
17. Del Bigio M.R. Proliferative status of cells in adult human dentate gyrus. Microsc. Res. Tech. 45 (1999) 353-358
18. Dong H., Goico B., Martin M., Csernansky C.A., Bertchume A., and Csernansky J.G. Modulation of hippocampal cell proliferation, memory, and amyloid plaque deposition in APPsw (Tg2576) mutant mice by isolation stress. Neuroscience 127 (2004) 601-609
19. Duchrow M., Schmidt M.H., Zingler M., Anemuller S., Bruch H.P., and Broll R. Suppression of cell division by pKi-67 antisense-RNA and recombinant protein. Cell. Physiol. Biochem. 11 (2001) 331-338
20. Endl E., and Gerdes J. The Ki-67 protein: fascinating forms and an unknown function. Exp. Cell Res. 257 (2000) 231-237
21. Eriksson P.S., Perfilieva E., Bjork-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., and Gage F.H. Neurogenesis in the adult human hippocampus. Nat. Med. 4 (1998) 1313-1317
22. Francis F., Koulakoff A., Boucher D., Chafey P., Schaar B., Vinet M.C., Friocourt G., McDonnell N., Reiner O., Kahn A., McConnell S.K., Berwald-Netter Y., Denoulet P., and Chelly J. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23 (1999) 247-256
23. Gartner U., Bruckner M.K., Krug S., Schmetsdorf S., Staufenbiel M., and Arendt T. Amyloid deposition in APP23 mice is associated with the expression of cyclins in astrocytes but not in neurons. Acta Neuropathol. (Berl.) 106 (2003) 535-544
24. Gerdes J., Li L., Schlueter C., Duchrow M., Wohlenberg C., Gerlach C., Stahmer I., Kloth S., Brandt E., and Flad H.D. Immunobiochemical and molecular biologic characterization of the cell proliferation-associated nuclear antigen that is defined by monoclonal antibody Ki-67. Am. J. Pathol. 138 (1991) 867-873
25. Gotz M., Hartfuss E., and Malatesta P. Radial glial cells as neuronal precursors: a new perspective on the correlation of morphology and lineage restriction in the developing cerebral cortex of mice. Brain Res. Bull. 57 (2002) 777-788
26. Haughey N.J., Nath A., Chan S.L., Borchard A.C., Rao M.S., and Mattson M.P. Disruption of neurogenesis by amyloid beta-peptide, and perturbed neural progenitor cell homeostasis, in models of Alzheimer's disease. J. Neurochem. 83 (2002) 1509-1524
27. Heine V.M., Maslam S., Joels M., and Lucassen P.J. Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation. Neurobiol. Aging 25 (2004) 361-375
28. Herrup K., Neve R., Ackerman S.L., and Copani A. Divide and die: cell cycle events as triggers of nerve cell death. J. Neurosci. 24 (2004) 9232-9239
29. Hoozemans J.J., Veerhuis R., Rozemuller J.M., and Eikelenboom P. Neuroinflammation and regeneration in the early stages of Alzheimer's disease pathology. Int. J. Dev. Neurosci. 24 2-3 (2006) 157-165
30. Jellinger K.A. Alzheimer disease and cerebrovascular pathology: an update. J. Neural Transm. 109 (2002) 813-836
31. Jin K., Peel A.L., Mao X.O., Xie L., Cottrell B.A., Henshall D.C., and Greenberg D.A. Increased hippocampal neurogenesis in Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 343-347
32. Jin K., Galvan V., Xie L., Mao X.O., Gorostiza O.F., Bredesen D.E., and Greenberg D.A. Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSw, Ind) mice. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 13363-13367
33. Kalaria R.N., Cohen D.L., Premkumar D.R., Nag S., LaManna J.C., and Lust W.D. Vascular endothelial growth factor in Alzheimer's disease and experimental cerebral ischemia. Brain Res. Mol. Brain Res. 62 (1998) 101-105
34. Kee N., Sivalingam S., Boonstra R., and Wojtowicz J.M. The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J. Neurosci. Methods 115 (2002) 97-105
35. Kondratick C.M., and Vandre D.D. Alzheimer's disease neurofibrillary tangles contain mitosis-specific phosphoepitopes. J. Neurochem. 67 (1996) 2405-2416
36. Kuhn H.G., Palmer T.D., and Fuchs E. Adult neurogenesis: a compensatory mechanism for neuronal damage. Eur. Arch. Psychiatry Clin. Neurosci. 251 (2001) 152-158
37. Letinic K., and Kostovic I. Transient fetal structure, the gangliothalamic body, connects telencephalic germinal zone with all thalamic regions in the developing human brain. J. Comp. Neurol. 384 (1997) 373-395
38. Lopez-Toledano M.A., and Shelanski M.L. Neurogenic effect of beta-amyloid peptide in the development of neural stem cells. J. Neurosci. 24 (2004) 5439-5444
39. Lucassen P.J., Chung W.C., Vermeulen J.P., Van Lookeren Campagne M., Van Dierendonck J.H., and Swaab D.F. Microwave-enhanced in situ end-labeling of fragmented DNA: parametric studies in relation to postmortem delay and fixation of rat and human brain. J. Histochem. Cytochem. 43 (1995) 1163-1171
40. Mandybur T.I. The incidence of cerebral amyloid angiopathy in Alzheimer's disease. Neurology 25 (1975) 120-126
41. McKhann G., Drachman D., Folstein M., Katzman R., Price D., and Stadlan E.M. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34 (1984) 939-944
42. McShea A., Harris P.L., Webster K.R., Wahl A.F., and Smith M.A. Abnormal expression of the cell cycle regulators P16 and CDK4 in Alzheimer's disease. Am. J. Pathol. 150 (1997) 1933-1939
43. Meda L., Baron P., and Scarlato G. Glial activation in Alzheimer's disease: the role of Abeta and its associated proteins. Neurobiol. Aging 22 (2001) 885-893
44. Munakata S., and Hendricks J.B. Effect of fixation time and microwave oven heating time on retrieval of the Ki-67 antigen from paraffin-embedded tissue. J. Histochem. Cytochem. 41 (1993) 1241-1246
45. Nagele R.G., Wegiel J., Venkataraman V., Imaki H., and Wang K.C. Contribution of glial cells to the development of amyloid plaques in Alzheimer's disease. Neurobiol. Aging 25 (2004) 663-674
46. Nagy Z., Esiri M.M., and Smith A.D. Expression of cell division markers in the hippocampus in Alzheimer's disease and other neurodegenerative conditions. Acta Neuropathol. (Berl.) 93 (1997) 294-300
47. Nicoll J.A., Yamada M., Frackowiak J., Mazur-Kolecka B., and Weller R.O. Cerebral amyloid angiopathy plays a direct role in the pathogenesis of Alzheimer's disease. Pro-CAA position statement. Neurobiol. Aging 25 (2004) 589-597
48. Noctor S.C., Flint A.C., Weissman T.A., Dammerman R.S., and Kriegstein A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409 (2001) 714-720
49. Ohsawa I., Takamura C., Morimoto T., Ishiguro M., and Kohsaka S. Amino-terminal region of secreted form of amyloid precursor protein stimulates proliferation of neural stem cells. Eur. J. Neurosci. 11 (1999) 1907-1913
50. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., and Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 17 (1997) 3727-3738
51. Radley J.J., and Jacobs B.L. Pilocarpine-induced status epilepticus increases cell proliferation in the dentate gyrus of adult rats via a 5-HT1A receptor-dependent mechanism. Brain Res. 966 (2003) 1-12
52. Raina A.K., Pardo P., Rottkamp C.A., Zhu X., Pereira-Smith O.M., and Smith M.A. Neurons in Alzheimer disease emerge from senescence. Mech. Ageing Dev. 123 (2001) 3-9
53. Rao M.S., and Shetty A.K. 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. 19 (2004) 234-246
54. Ravid R., and Swaab D.F. The Netherlands Brain Bank-a clinico-pathological link in aging and dementia research. J. Neural Transm., Suppl. 39 (1993) 143-153
55. Reisberg B., Ferris S.H., de Leon M.J., and Crook T. The Global Deterioration Scale for assessment of primary degenerative dementia. Am. J. Psychiatry 139 (1982) 1136-1139
56. Rensink A.A., Otte-Holler I., ten Donkelaar H.J., De Waal R.M., Kremer B., and Verbeek M.M. Differential gene expression in human brain pericytes induced by amyloid-beta protein. Neuropathol. Appl. Neurobiol. 30 (2004) 279-291
57. Rossler M., Zarski R., Bohl J., and Ohm T.G. Stage-dependent and sector-specific neuronal loss in hippocampus during Alzheimer's disease. Acta Neuropathol. (Berl.) 103 (2002) 363-369
58. Salhia B., Angelov L., Roncari L., Wu X., Shannon P., and Guha A. Expression of vascular endothelial growth factor by reactive astrocytes and associated neoangiogenesis. Brain Res. 883 (2000) 87-97
59. Scholzen T., and Gerdes J. The Ki-67 protein: from the known and the unknown. J. Cell. Physiol. 182 (2000) 311-322
60. Shi S.R., Imam S.A., Young L., Cote R.J., and Taylor C.R. Antigen retrieval immunohistochemistry under the influence of pH using monoclonal antibodies. J. Histochem. Cytochem. 43 (1995) 193-201
61. Simic G., Kostovic I., Winblad B., and Bogdanovic N. Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer's disease. J. Comp. Neurol. 379 (1997) 482-494
62. Smith T.W., and Lippa C.F. Ki-67 immunoreactivity in Alzheimer's disease and other neurodegenerative disorders. J. Neuropathol. Exp. Neurol. 54 (1995) 297-303
63. Suurmeijer A.J., and Boon M.E. Notes on the application of microwaves for antigen retrieval in paraffin and plastic tissue sections. Eur. J. Morphol. 31 (1993) 144-150
64. Swaab D.F., and Uylings H.B.M. Potentials and pitfalls in the use of human brain material in molecular neuroanatomy. In: van Leeuwen F.W., Pool C.W., and Pach O. (Eds). Molecular Neuroanatomy (1988), Elsevier Science Publisher, Amsterdam 403-416
65. Tarkowski E., Issa R., Sjogren M., Wallin A., Blennow K., Tarkowski A., and Kumar P. Increased intrathecal levels of the angiogenic factors VEGF and TGF-beta in Alzheimer's disease and vascular dementia. Neurobiol. Aging 23 (2002) 237-243
66. Taylor C.R., Shi S.R., Chaiwun B., Young L., Imam S.A., and Cote R.J. Strategies for improving the immunohistochemical staining of various intranuclear prognostic markers in formalin-paraffin sections: androgen receptor, estrogen receptor, progesterone receptor, p53 protein, proliferating cell nuclear antigen, and Ki-67 antigen revealed by antigen retrieval techniques. Hum. Pathol. 25 (1994) 263-270
67. Vagnucci Jr. A.H., Li W.W., et al. Alzheimer's disease and angiogenesis. Lancet 361 (2003) 605-608
68. Vincent I., Jicha G., Rosado M., and Dickson D.W. Aberrant expression of mitotic cdc2/cyclin B1 kinase in degenerating neurons of Alzheimer's disease brain. J. Neurosci. 17 (1997) 3588-3598
69. Wang R., Dineley K.T., Sweatt J.D., and Zheng H. Presenilin 1 familial Alzheimer's disease mutation leads to defective associative learning and impaired adult neurogenesis. Neuroscience 126 (2004) 305-312
70. Wen P.H., Hof P.R., Chen X., Gluck K., Austin G., Younkin S.G., Younkin L.H., DeGasperi R., Gama Sosa M.A., Robakis N.K., Haroutunian V., and Elder G.A. The presenilin-1 familial Alzheimer disease mutant P117L impairs neurogenesis in the hippocampus of adult mice. Exp. Neurol. 188 (2004) 224-237
71. Wharton S.B., Williams G.H., Stoeber K., Gelsthorpe C.H., Baxter L., Johnson A.L., and Ince P.G. Expression of Ki67, PCNA and the chromosome replication licensing protein Mcm2 in glial cells of the ageing human hippocampus increases with the burden of Alzheimer-type pathology. Neurosci. Lett. 383 (2005) 33-38
72. Wilhelmsson U., Li L., Pekna M., Berthold C.H., Blom S., Eliasson C., Renner O., Bushong E., Ellisman M., Morgan T.E., and Pekny M. Absence of glial fibrillary acidic protein and vimentin prevents hypertrophy of astrocytic processes and improves post-traumatic regeneration. J. Neurosci. 24 (2004) 5016-5021
73. Wu Z., Guo H., Chow N., Sallstrom J., Bell R.D., Deane R., Brooks A.I., Kanagala S., Rubio A., Sagare A., Liu D., Li F., Armstrong D., Gasiewicz T., Zidovetzki R., Song X., Hofman F., and Zlokovic B.V. Role of the MEOX2 homeobox gene in neurovascular dysfunction in Alzheimer disease. Nat. Med. 11 (2005) 959-965
74. Yang Y., Mufson E.J., and Herrup K. Neuronal cell death is preceded by cell cycle events at all stages of Alzheimer's disease. J. Neurosci. 23 (2003) 2557-2563
75. Zand L., Ryu J.K., and McLarnon J.G. Induction of angiogenesis in the beta-amyloid peptide-injected rat hippocampus. NeuroReport 16 (2005) 129-132
76. Zlokovic B.V. Neurovascular mechanisms of Alzheimer's neurodegeneration. Trends Neurosci. 28 (2005) 202-208