Glio-vascular changes during ageing in wild-type and Alzheimer's disease-like APP/PS1 mice

Brain Research

Volumn 1620, Issue , 2015, Pages 153-168

  Janota, C S ^a   Brites, D ^a   Lemere, C A ^b   Brito, M A ^a  

^a RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Alzheimer'sdisease; Blood brain barrierdisruption; endproducts; Glial activation; Microvasculature; Pericytes; Receptor for advanced glycation

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; ALBUMIN; AMYLOID BETA PROTEIN; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; THROMBIN; AMYLOID PRECURSOR PROTEIN; APP PROTEIN, HUMAN; PRESENILIN 1; PSEN1 PROTEIN, HUMAN;

ADULT; AGING; ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BRAIN CORTEX; CONTROLLED STUDY; DISEASE COURSE; GLIA; GLIOSIS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MICROVASCULATURE; MIDDLE AGED; MOUSE; NONHUMAN; PARENCHYMA; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENILE PLAQUE; YOUNG ADULT; ANIMAL; BLOOD BRAIN BARRIER; C57BL MOUSE; CAPILLARY; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

AGING; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BLOOD-BRAIN BARRIER; CAPILLARIES; CEREBRAL CORTEX; GLIOSIS; HIPPOCAMPUS; HUMANS; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROGLIA; PERICYTES; PRESENILIN-1;

EID: 84940893928     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2015.04.056     Document Type: Article

References (61)

1. A. Abramsson, S. Kurup, M. Busse, S. Yamada, P. Lindblom, E. Schallmeiner, D. Stenzel, D. Sauvaget, J. Ledin, M. Ringvall, U. Landegren, L. Kjellen, G. Bondjers, J.P. Li, U. Lindahl, D. Spillmann, C. Betsholtz, and H. Gerhardt Defective N-sulfation of heparan sulfate proteoglycans limits PDGF-BB binding and pericyte recruitment in vascular development Genes. Dev. 21 2007 316 331
2. R.O. Akinyemi, E.B. Mukaetova-Ladinska, J. Attems, M. Ihara, and R.N. Kalaria Vascular risk factors and neurodegeneration in ageing related dementias: Alzheimer's disease and vascular dementia Curr. Alzheimer Res. 10 2013 642 653
3. R.A. Armstrong What causes alzheimer's disease? Folia Neuropathol. 51 2013 169 188
4. A. Armulik, G. Genove, M. Mae, M.H. Nisancioglu, E. Wallgard, C. Niaudet, L. He, J. Norlin, P. Lindblom, K. Strittmatter, B.R. Johansson, and C. Betsholtz Pericytes regulate the blood-brain barrier Nature 468 2010 557 561
5. T.L. Bailey, C.B. Rivara, A.B. Rocher, and P.R. Hof The nature and effects of cortical microvascular pathology in aging and Alzheimer's disease Neurol. Res. 26 2004 573 578
6. S.J. Baloyannis, and I.S. Baloyannis The vascular factor in Alzheimer's disease: a study in Golgi technique and electron microscopy J. Neurol. Sci. 322 2012 117 121
7. M.A. Bell, and M.J. Ball The correlation of vascular capacity with the parenchymal lesions of Alzheimer's disease Can. J. Neurol. Sci. 13 1986 456 461
8. M.A. Bell, and M.J. Ball Neuritic plaques and vessels of visual cortex in aging and Alzheimer's dementia Neurobiol. Aging 11 1990 359 370
9. R.D. Bell, E.A. Winkler, A.P. Sagare, I. Singh, B. LaRue, R. Deane, and B.V. Zlokovic Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging Neuron 68 2010 409 427
10. K.E. Biron, D.L. Dickstein, R. Gopaul, and W.A. Jefferies Amyloid triggers extensive cerebral angiogenesis causing blood brain barrier permeability and hypervascularity in Alzheimer's disease PLoS One 6 2011 e23789
11. D. Bonkowski, V. Katyshev, R.D. Balabanov, A. Borisov, and P. Dore-Duffy The CNS microvascular pericyte: pericyte-astrocyte crosstalk in the regulation of tissue survival Fluids Barriers CNS 8 2011 8
12. M.A. Brito, P. Pereira, C. Barroso, E. Aronica, and D. Brites New autopsy findings in different brain regions of a preterm neonate with kernicterus: neurovascular alterations and up-regulation of efflux transporters Pediatr. Neurol. 49 2013 431 438
13. W.R. Brown, and C.R. Thore Review: cerebral microvascular pathology in ageing and neurodegeneration Neuropathol. Appl. Neurobiol. 37 2011 56 74
14. H.J. Cho, S.M. Son, S.M. Jin, H.S. Hong, D.H. Shin, S.J. Kim, K. Huh, and I. Mook-Jung RAGE regulates BACE1 and Abeta generation via NFAT1 activation in Alzheimer's disease animal model FASEB J. 23 2009 2639 2649
15. R. Daneman, L. Zhou, A.A. Kebede, and B.A. Barres Pericytes are required for blood-brain barrier integrity during embryogenesis Nature 468 2010 562 566
16. R. Deane, Z. Wu, A. Sagare, J. Davis, S. Du Yan, K. Hamm, F. Xu, M. Parisi, B. LaRue, H.W. Hu, P. Spijkers, H. Guo, X. Song, P.J. Lenting, W.E. Van Nostrand, and B.V. Zlokovic LRP/amyloid beta-peptide interaction mediates differential brain efflux of Abeta isoforms Neuron 43 2004 333 344
17. R. Deane, Z. Wu, and B.V. Zlokovic RAGE (yin) versus LRP (yang) balance regulates alzheimer amyloid beta-peptide clearance through transport across the blood-brain barrier Stroke 35 2004 2628 2631
18. R. Deane, I. Singh, A.P. Sagare, R.D. Bell, N.T. Ross, B. LaRue, R. Love, S. Perry, N. Paquette, R.J. Deane, M. Thiyagarajan, T. Zarcone, G. Fritz, A.E. Friedman, B.L. Miller, and B.V. Zlokovic A multimodal RAGE-specific inhibitor reduces amyloid beta-mediated brain disorder in a mouse model of Alzheimer disease J. Clin. Invest. 122 2012 1377 1392
19. Y.S. Eisele, U. Obermuller, G. Heilbronner, F. Baumann, S.A. Kaeser, H. Wolburg, L.C. Walker, M. Staufenbiel, M. Heikenwalder, and M. Jucker Peripherally applied Abeta-containing inoculates induce cerebral beta-amyloidosis Science 330 2010 980 982
20. E. Farkas, and P.G. Luiten Cerebral microvascular pathology in aging and Alzheimer's disease Prog. Neurobiol. 64 2001 575 611
21. V.W. Fischer, A. Siddiqi, and Y. Yusufaly Altered angioarchitecture in selected areas of brains with Alzheimer's disease Acta Neuropathol. 79 1990 672 679
22. K. Gaengel, G. Genove, A. Armulik, and C. Betsholtz Endothelial-mural cell signaling in vascular development and angiogenesis Arterioscler. Thromb. Vasc. Biol. 29 2009 630 638
23. M. Garcia-Alloza, E.M. Robbins, S.X. Zhang-Nunes, S.M. Purcell, R.A. Betensky, S. Raju, C. Prada, S.M. Greenberg, B.J. Bacskai, and M.P. Frosch Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease Neurobiol. Dis. 24 2006 516 524
24. S. Gengler, A. Hamilton, and C. Holscher Synaptic plasticity in the hippocampus of a APP/PS1 mouse model of Alzheimer's disease is impaired in old but not young mice PLoS One 5 2010 e9764
25. D.A. Gimbel, H.B. Nygaard, E.E. Coffey, E.C. Gunther, J. Lauren, Z.A. Gimbel, and S.M. Strittmatter Memory impairment in transgenic Alzheimer mice requires cellular prion protein J. Neurosci. 30 2010 6367 6374
26. J.L. Jankowsky, D.J. Fadale, J. Anderson, G.M. Xu, V. Gonzales, N.A. Jenkins, N.G. Copeland, M.K. Lee, L.H. Younkin, S.L. Wagner, S.G. Younkin, and D.R. Borchelt Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase Hum. Mol. Genet. 13 2004 159 170
27. N.S. Jenny Inflammation in aging: cause, effect, or both? Discov. Med. 13 2012 451 460
28. B. Jeynes, and J. Provias Evidence for altered LRP/RAGE expression in Alzheimer lesion pathogenesis Curr. Alzheimer Res. 5 2008 432 437
29. M. Jucker, K. Battig, and W. Meier-Ruge Effects of aging and vincamine derivatives on pericapillary microenvironment: stereological characterization of the cerebral capillary network Neurobiol. Aging 11 1990 39 46
30. W. Kamphuis, C. Mamber, M. Moeton, L. Kooijman, J.A. Sluijs, A.H. Jansen, M. Verveer, L.R. de Groot, V.D. Smith, S. Rangarajan, J.J. Rodriguez, M. Orre, and E.M. Hol GFAP isoforms in adult mouse brain with a focus on neurogenic astrocytes and reactive astrogliosis in mouse models of Alzheimer disease PLoS One 7 2012 e42823
31. S. Kumar-Singh, D. Pirici, E. McGowan, S. Serneels, C. Ceuterick, J. Hardy, K. Duff, D. Dickson, and C. Van Broeckhoven Dense-core plaques in Tg2576 and PSAPP mouse models of Alzheimer's disease are centered on vessel walls Am. J. Pathol. 167 2005 527 543
32. R. Lalonde, H.D. Kim, J.A. Maxwell, and K. Fukuchi Exploratory activity and spatial learning in 12-month-old APP(695)SWE/co+PS1/DeltaE9 mice with amyloid plaques Neurosci. Lett. 390 2005 87 92
33. G.D. Lee, J.H. Aruna, P.M. Barrett, D.L. Lei, D.K. Ingram, and P.R. Mouton Stereological analysis of microvascular parameters in a double transgenic model of Alzheimer's disease Brain Res. Bull. 65 2005 317 322
34. C.A. Lemere, R. Maron, E.T. Spooner, T.J. Grenfell, C. Mori, R. Desai, W.W. Hancock, H.L. Weiner, and D.J. Selkoe Nasal A beta treatment induces anti-A beta antibody production and decreases cerebral amyloid burden in PD-APP mice Ann. N. Y. Acad. Sci. 920 2000 328 331
35. R. Liu, J.Z. Li, J.K. Song, D. Zhou, C. Huang, X.Y. Bai, T. Xie, X. Zhang, Y.J. Li, C.X. Wu, L. Zhang, L. Li, T.T. Zhang, and G.H. Du Pinocembrin improves cognition and protects the neurovascular unit in Alzheimer related deficits Neurobiol. Aging 35 2014 1275 1285
36. M. Maier, T.J. Seabrook, and C.A. Lemere Modulation of the humoral and cellular immune response in Abeta immunotherapy by the adjuvants monophosphoryl lipid A (MPL), cholera toxin B subunit (CTB) and E. coli enterotoxin LT(R192G) Vaccine 23 2005 5149 5159
37. N.L. Marchant, B.R. Reed, N. Sanossian, C.M. Madison, S. Kriger, R. Dhada, W.J. Mack, C. DeCarli, M.W. Weiner, D.M. Mungas, H.C. Chui, and W.J. Jagust The aging brain and cognition: contribution of vascular injury and abeta to mild cognitive dysfunction JAMA Neurol. 70 2013 488 495
38. F. Marques, J.C. Sousa, N. Sousa, and J.A. Palha Blood-brain-barriers in aging and in Alzheimer's disease Mol. Neurodegener. 8 2013 38
39. M.C. Miller, R. Tavares, C.E. Johanson, V. Hovanesian, J.E. Donahue, L. Gonzalez, G.D. Silverberg, and E.G. Stopa Hippocampal RAGE immunoreactivity in early and advanced Alzheimer's disease Brain Res. 1230 2008 273 280
40. A. Montagne, S.R. Barnes, M.D. Sweeney, M.R. Halliday, A.P. Sagare, Z. Zhao, A.W. Toga, R.E. Jacobs, C.Y. Liu, L. Amezcua, M.G. Harrington, H.C. Chui, M. Law, and B.V. Zlokovic Blood-brain barrier breakdown in the aging human hippocampus Neuron 85 2015 296 302
41. T. Nishioku, J. Matsumoto, S. Dohgu, N. Sumi, K. Miyao, F. Takata, H. Shuto, A. Yamauchi, and Y. Kataoka Tumor necrosis factor-alpha mediates the blood-brain barrier dysfunction induced by activated microglia in mouse brain microvascular endothelial cells J. Pharmacol. Sci. 112 2010 251 254
42. K. Niwa, K. Kazama, L. Younkin, S.G. Younkin, G.A. Carlson, and C. Iadecola Cerebrovascular autoregulation is profoundly impaired in mice overexpressing amyloid precursor protein Am. J. Physiol. Heart Circ. Physiol. 283 2002 H315 H323
43. D. Paris, N. Patel, A. DelleDonne, A. Quadros, R. Smeed, and M. Mullan Impaired angiogenesis in a transgenic mouse model of cerebral amyloidosis Neurosci. Lett. 366 2004 80 85
44. J.H. Park, G.A. Widi, D.A. Gimbel, N.Y. Harel, D.H. Lee, and S.M. Strittmatter Subcutaneous Nogo receptor removes brain amyloid-beta and improves spatial memory in Alzheimer's transgenic mice J. Neurosci. 26 2006 13279 13286
45. V.H. Perry, M.K. Matyszak, and S. Fearn Altered antigen expression of microglia in the aged rodent CNS Glia 7 1993 60 67
46. S.W. Pimplikar Neuroinflammation in Alzheimer's disease: from pathogenesis to a therapeutic target J. Clin. Immunol. 34 Suppl 1 2014 64 69
47. I. Sá-Pereira, D. Brites, and M.A. Brito Neurovascular unit: a focus on pericytes Mol. Neurobiol. 45 2012 327 347
48. A.P. Sagare, R.D. Bell, Z. Zhao, Q. Ma, E.A. Winkler, A. Ramanathan, and B.V. Zlokovic Pericyte loss influences Alzheimer-like neurodegeneration in mice Nat. Commun. 4 2013 2932
49. J.D. Sengillo, E.A. Winkler, C.T. Walker, J.S. Sullivan, M. Johnson, and B.V. Zlokovic Deficiency in mural vascular cells coincides with blood-brain barrier disruption in Alzheimer's disease Brain Pathol. 23 2013 303 310
50. A. Serrano-Pozo, M.P. Frosch, E. Masliah, and B.T. Hyman Neuropathological alterations in Alzheimer disease Cold Spring Harb. Perspect. Med. 1 2011 a006189
51. H.K. Shin, P.B. Jones, M. Garcia-Alloza, L. Borrelli, S.M. Greenberg, B.J. Bacskai, M.P. Frosch, B.T. Hyman, M.A. Moskowitz, and C. Ayata Age-dependent cerebrovascular dysfunction in a transgenic mouse model of cerebral amyloid angiopathy Brain 130 2007 2310 2319
52. A. Slowik, J. Merres, A. Elfgen, S. Jansen, F. Mohr, C.J. Wruck, T. Pufe, and L.O. Brandenburg Involvement of formyl peptide receptors in receptor for advanced glycation end products (RAGE) - and amyloid beta 1-42-induced signal transduction in glial cells Mol. Neurodegener. 7 2012 55
53. W.E. Sonntag, C.D. Lynch, P.T. Cooney, and P.M. Hutchins Decreases in cerebral microvasculature with age are associated with the decline in growth hormone and insulin-like growth factor 1 Endocrinology 138 1997 3515 3520
54. S. Takeda, N. Sato, K. Ikimura, H. Nishino, H. Rakugi, and R. Morishita Increased blood-brain barrier vulnerability to systemic inflammation in an Alzheimer disease mouse model Neurobiol. Aging 34 2013 2064 2070
55. A. Volianskis, R. Kostner, M. Molgaard, S. Hass, and M.S. Jensen Episodic memory deficits are not related to altered glutamatergic synaptic transmission and plasticity in the CA1 hippocampus of the APPswe/PS1deltaE9-deleted transgenic mice model of ss-amyloidosis Neurobiol. Aging 31 2010 1173 1187
56. Y.J. Wang, C.Y. Gao, M. Yang, X.H. Liu, Y. Sun, A. Pollard, X.Y. Dong, X.B. Wu, J.H. Zhong, H.D. Zhou, and X.F. Zhou Intramuscular delivery of a single chain antibody gene prevents brain Abeta deposition and cognitive impairment in a mouse model of Alzheimer's disease Brain Behav. Immun. 24 2010 1281 1293
57. R.O. Weller, M. Subash, S.D. Preston, I. Mazanti, and R.O. Carare Perivascular drainage of amyloid-beta peptides from the brain and its failure in cerebral amyloid angiopathy and Alzheimer's disease Brain Pathol. 18 2008 253 266
58. C.L. Willis Glia-induced reversible disruption of blood-brain barrier integrity and neuropathological response of the neurovascular unit Toxicol. Pathol. 39 2011 172 185
59. K.T. Wirz, K. Bossers, A. Stargardt, W. Kamphuis, D.F. Swaab, E.M. Hol, and J. Verhaagen Cortical beta amyloid protein triggers an immune response, but no synaptic changes in the APPswe/PS1dE9 Alzheimer's disease mouse model Neurobiol. Aging 34 2013 1328 1342
60. H. Xiong, D. Callaghan, J. Wodzinska, J. Xu, M. Premyslova, Q.Y. Liu, J. Connelly, and W. Zhang Biochemical and behavioral characterization of the double transgenic mouse model (APPswe/PS1dE9) of Alzheimer's disease Neurosci. Bull. 27 2011 221 232
61. B.V. Zlokovic Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders Nat. Rev. Neurosci. 12 2011 723 738