Neurogenic effects of β-amyloid in the choroid plexus epithelial cells in Alzheimer's disease

Cellular and Molecular Life Sciences

Volumn 70, Issue 15, 2013, Pages 2787-2797

  Bolos, Marta ^a,b   Spuch, Carlos ^c   Ordoñez Gutierrez, Lara ^b,d   Wandosell, Francisco ^b,d   Ferrer, Isidro ^b,e   Carro, Eva ^a,b  

^a HOSPITAL UNIVERSITARIO 12 DE OCTUBRE   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^c UNIVERSITY HOSPITAL COMPLEX OF VIGO   (Spain)

^d UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^e HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

Author keywords

Alzheimer's disease patients; Amyloid; Choroid plexus; Neurogenesis; Transgenic mice

Indexed keywords

AMYLOID BETA PROTEIN; CALBINDIN; CASPASE 3; CASPASE 9;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CHOROID PLEXUS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROPATHOLOGY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CELLS, CULTURED; CHOROID PLEXUS; EPITHELIAL CELLS; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; NEURAL STEM CELLS; NEUROGENESIS; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

MUS; MUS MUSCULUS;

EID: 84880291842     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1300-x     Document Type: Article

References (57)

1. Kitada M, Chakrabortty S, Matsumoto N, Taketomi M, Ide C (2001) Differentiation of choroid plexus ependymal cells into astrocytes after grafting into the pre-lesioned spinal cord in mice. Glia 36:364-374
2. Li Y, Chen J, Chopp M (2002) Cell proliferation and differentiation from ependymal, subependymal and choroid plexus cells in response to stroke in rats. J Neurol Sci 193:137-146
3. Itokazu Y, Kitada M, Dezawa M, Mizoguchi A, Matsumoto N, Shimizu A, Ide C (2006) Choroid plexus ependymal cells host neural progenitor cells in the rat. Glia 53:32-42
4. Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173-189
5. Chiasson BJ, Tropepe V, Morshead CM, van der Kooy D (1999) Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J Neurosci 19:4462-4471
6. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716
7. Sahay A, Scobie KN, Hill AS, O'Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsky A, Hen R (2011) Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472:466-470
8. Stone SS, Teixeira CM, Devito LM, Zaslavsky K, Josselyn SA, Lozano AM, Frankland PW (2011) Stimulation of entorhinal cortex promotes adult neurogenesis and facilitates spatial memory. J Neurosci 31:13469-13484
9. Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ (2009) A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325:210-213
10. Lazarov O, Mattson MP, Peterson DA, Pimplikar SW, van Praag H (2010) When neurogenesis encounters aging and disease. Trends Neurosci 33:569-579
11. Winner B, Kohl Z, Gage FH (2011) Neurodegenerative disease and adult neurogenesis. Eur J Neurosci 33:1139-1151
12. Rensink AA, de Waal RM, Kremer B, Verbeek MM (2003) Pathogenesis of cerebral amyloid angiopathy. Brain Res Brain Res Rev 43:207-223
13. Selkoe DJ (2004) Cell biology of protein misfolding: the examples of Alzheimer's and Parkinson's diseases. Nat Cell Biol 6:1054-1061
14. Dietrich MO, Spuch C, Antequera D, Rodal I, De Yebenes JG, Molina JA, Bermejo F, Carro E (2008) Megalin mediates the transport of leptin across the blood-CSF barrier. Neurobiol Aging 29:902-912
15. Alvira-Botero X, Carro EM (2010) Clearance of amyloid-beta peptide across the choroid plexus in Alzheimer's disease. Curr Aging Sci 3:219-229
16. Carro E, Trejo JL, Gomez-Isla T, Leroith D, Torres-Aleman I (2002) Serum insulin-like growth factor I regulates brain amyloid-beta levels. Nat Med 8:1390-1397
17. Zlokovic BV (2004) Clearing amyloid through the blood-brain barrier. J Neurochem 89:807-811
18. Antequera D, Vargas T, Ugalde C, Spuch C, Molina JA, Ferrer I, Bermejo-Pareja F, Carro E (2009) Cytoplasmic gelsolin increases mitochondrial activity and reduces Abeta burden in a mouse model of Alzheimer's disease. Neurobiol Dis 36:42-50
19. Vargas T, Ugalde C, Spuch C, Antequera D, Moran MJ, Martin MA, Ferrer I, Bermejo-Pareja F, Carro E (2010) Abeta accumulation in choroid plexus is associated with mitochondrial-induced apoptosis. Neurobiol Aging 31:1569-1581
20. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416:535-539
21. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, Gallagher M, Ashe KH (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440:352-357
22. Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, Sabatini BL (2007) Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci 27:2866-2875
23. Koffie RM, Meyer-Luehmann M, Hashimoto T, Adams KW, Mielke ML, Garcia-Alloza M, Micheva KD, Smith SJ, Kim ML, Lee VM, Hyman BT, Spires-Jones TL (2009) Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc Natl Acad Sci USA 106:4012-4017
24. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297:353-356
25. López-Toledano MA, Shelanski ML (2004) Neurogenic effect of beta-amyloid peptide in the development of neural stem cells. J Neurosci 24:5439-5444
26. Calafiore M, Copani A, Deng W (2012) DNA polymerase-β mediates the neurogenic effect of β-amyloid protein in cultured subventricular zone neurospheres. J Neurosci Res 90:559-567
27. Antequera D, Portero A, Bolos M, Orive G, Hernández RM, Pedraz JL, Carro E (2012) Encapsulated VEGF-secreting cells enhance proliferation of neuronal progenitors in the hippocampus of AβPP/Ps1 mice. J Alzheimers Dis 29:187-200
28. Pérez-González R, Antequera D, Vargas T, Spuch C, Bolós M, Carro E (2011) Leptin induces proliferation of neuronal progenitors and neuroprotection in a mouse model of Alzheimer's disease. J Alzheimers Dis 24:17-25
29. Braak H, Braak E (1999) Temporal sequence of Alzheimer's disease-related pathology. In: Peters A, Morrison JH (eds) Cerebral cortex, vol 14., Neurodegenerative and age-related changes in structure and function of cerebral cortex. Kluwer Academic/Plenum Press, New York, pp 475-512
30. Yu Y, He J, Zhang Y, Luo H, Zhu S, Yang Y, Zhao T, Wu J, Huang Y, Kong J, Tan Q, Li XM (2009) Increased hippocampal neurogenesis in the progressive stage of Alzheimer's disease phenotype in an APP/Ps1 double transgenic mouse model. Hippocampus 19:1247-1253
31. Esteras N, Bartolomé F, Alquézar C, Antequera D, Muñoz U, Carro E, Martín-Requero A (2012) Altered cell cycle-related gene expression in brain and lymphocytes from a transgenic mouse model of Alzheimer's disease [amyloid precursor protein/presenilin 1 (PS1)]. Eur J Neurosci 36:2609-2618
32. Marques F, Sousa JC, Coppola G, Gao F, Puga R, Brentani H, Geschwind DH, Sousa N, Correia-Neves M, Palha JA (2011) Transcriptome signature of the adult mouse choroid plexus. Fluids Barriers CNS 8:1-11
33. Borchelt DR, Ratovitski T, van Lare J, Lee MK, Gonzales V, Jenkins NA, Copeland NG, Price DL, Sisodia SS (1997) Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 19:939-945
34. Emerich DF, Skinner SJ, Borlongan CV, Thanos CG (2005) A role of the choroid plexus in transplantation therapy. Cell Transplant 14:715-725
35. Kuhn HG, Palmer TD, Fuchs E (2001) Adult neurogenesis: a compensatory mechanism for neuronal damage. Eur Arch Psychiatry Clin Neurosci 251:152-158
36. Zhu W, Cheng S, Xu G, Ma M, Zhou Z, Liu D, Liu X (2011) Intranasal nerve growth factor enhances striatal neurogenesis in adult rats with focal cerebral ischemia. Drug Deliv 18:338-343
37. Lee J, Duan W, Mattson MP (2002) Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J Neurochem 82:1367-1375
38. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA (2002) Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA 99:11946-11950
39. Burbach GJ, Hellweg R, Haas CA, Del Turco D, Deicke U, Abramowski D, Jucker M, Staufenbiel M, Deller T (2004) Induction of brain-derived neurotrophic factor in plaque-associated glial cells of aged APP23 transgenic mice. J Neurosci 24:2421-2430
40. Tarkowski E, Issa R, Sjögren M, Wallin A, Blennow K, Tarkowski A, Kumar P (2002) Increased intrathecal levels of the angiogenic factors VEGF and TGF-beta in Alzheimer's disease and vascular dementia. Neurobiol Aging 23:237-243
41. Jin K, Peel AL, Mao XO, Xie L, Cottrell BA, Henshall DC, Greenberg DA (2004) Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci USA 101:343-347
42. Li L, Xu B, Zhu Y, Chen L, Sokabe M, Chen L (2010) DHEA prevents Aβ25-35-impaired survival of newborn neurons in the dentate gyrus through a modulation of PI3K-Akt-mTOR signaling. Neuropharmacology 59:323-333
43. Steen E, Terry BM, Rivera EJ, Cannon JL, Neely TR, Tavares R, Xu XJ, Wands JR, de la Monte SM (2005) Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease - is this type 3 diabetes? J Alzheimer Dis 7:63-80
44. Nagahara AH, Merrill DA, Coppola G, Tsukada S, Schroeder BE, Shaked GM, Wang L, Blesch A, Kim A, Conner JM, Rockenstein E, Chao MV, Koo EH, Geschwind D, Masliah E, Chiba AA, Tuszynski MH (2009) Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease. Nat Med 15:331-337
45. Moloney AM, Griffin RJ, Timmons S, O'Connor R, Ravid R, O'Neill C (2010) Defects in IGF-1 receptor, insulin receptor and IRS-1/2 in Alzheimer's disease indicate possible resistance to IGF-1 and insulin signalling. Neurobiol Aging 31:224-243
46. Spuch C, Antequera D, Portero A, Orive G, Hernández RM, Molina JA, Bermejo-Pareja F, Pedraz JL, Carro E (2010) The effect of encapsulated VEGF-secreting cells on brain amyloid load and behavioral impairment in a mouse model of Alzheimer's disease. Biomaterials 31:5608-5618
47. Dahlgren KN, Manelli AM, Stine WB Jr, Baker LK, Krafft GA, LaDu MJ (2002) Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J Biol Chem 277:32046-32053
48. Kim HJ, Chae SC, Lee DK, Chromy B, Lee SC, Park YC, Klein WL, Krafft GA, Hong ST (2003) Selective neuronal degeneration induced by soluble oligomeric amyloid beta protein. FASEB J 17:118-120
49. Zhang C, McNeil E, Dressler L, Siman R (2007) Long-lasting impairment in hippocampal neurogenesis associated with amyloid deposition in a knock-in mouse model of familial Alzheimer's disease. Exp Neurol 204:77-87
50. Boekhoorn K, Joels M, Lucassen PJ (2006) Increased proliferation reflects glial and vascular-associated changes, but not neurogenesis in the presenile Alzheimer hippocampus. Neurobiol Dis 24:1-14
51. Chao MV (2003) Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4:299-309
52. Spuch C, Carro E (2011) The p75 neurotrophin receptor localization in blood-CSF barrier: expression in choroid plexus epithelium. BMC Neurosci 12:39
53. Chang L, Karin M (2001) Mammalian MAP kinase signalling cascades. Nature 410:37-40
54. Rohe M, Carlo AS, Breyhan H, Sporbert A, Militz D, Schmidt V, Wozny C, Harmeier A, Erdmann B, Bales KR, Wolf S, Kempermann G, Paul SM, Schmitz D, Bayer TA, Willnow TE, Andersen OM (2008) Sortilin-related receptor with A-type repeats (SORLA) affects the amyloid precursor protein-dependent stimulation of ERK signaling and adult neurogenesis. J Biol Chem 283:14826-14834
55. Giovannini MG, Scal C, Prosperi C, Bellucci A, Vannucchi MG, Rosi S, Pepeu G, Casamenti F (2002) Beta-amyloid-induced inflammation and cholinergic hypofunction in the rat brain in vivo: involvement of the p38MAPK pathway. Neurobiol Dis 11:257-274
56. Franciosi S, Ryu JK, Choi HB, Radov L, Kim SU, McLarnon JG (2006) Broad-spectrum effects of 4-aminopyridine to modulate amyloid beta1-42-induced cell signaling and functional responses in human microglia. J Neurosci 26:11652-11664
57. Zhu X, Rottkamp CA, Hartzler A, Sun Z, Takeda A, Boux H, Shimohama S, Perry G, Smith MA (2001) Activation of MKK6, an upstream activator of p38, in Alzheimer's disease. J Neurochem 79:311-318