Increased permeability of the blood-brain barrier and Alzheimer's disease-like alterations in slit-2 transgenic Mice

Journal of Alzheimer's Disease

Volumn 43, Issue 2, 2015, Pages 535-548

  Li, Jiang Chao ^a   Han, Lu ^a   Wen, Yin Xin ^a   Yang, Yong Xia ^a   Li, Shuai ^a   Li, Xue Song ^b   Zhao, Chang Jiang ^b   Wang, Ting Yu ^c   Chen, Hui ^a   Liu, Ying ^a   Qi, Cui Ling ^a   He, Xiao Dong ^a   Gu, Qu Liang ^a   Ye, Yu Xiang ^a   Zhang, Yu ^d   Huang, Ren ^d   Wu, Yu E ^d   He, Rong Rong ^e   Kurihara, Hiroshi ^e   Song, Xiao Yu ^f   Cao, Liu ^f   Wang, Li Jing ^a   more..

^a GUANGDONG PHARMACEUTICAL UNIVERSITY   (China)

^b Third People's Hospital of Foshan   (China)

^c Dongguan Xinyong Hospital   (China)

^d Guangdong Laboratory Animals Monitoring Institute   (China)

^e JINAN UNIVERSITY   (China)

^f CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Alzheimer's disease; blood brain barrier; Slit homolog 2 protein; transgenic mice

Indexed keywords

AMYLOID BETA PROTEIN; GLUTAMIC ACID; SLIT2 PROTEIN; AMYLOID PRECURSOR PROTEIN; NERVE PROTEIN; SIGNAL PEPTIDE; SLIT HOMOLOG 2 PROTEIN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; HIPPOCAMPUS; HISTOPATHOLOGY; LATERAL BRAIN VENTRICLE; MALE; MOLECULAR DIAGNOSIS; MOUSE; NERVE CELL; NONHUMAN; PERMEABILITY; PROTEIN EXPRESSION; AGED; ANIMAL; BLOOD; BLOOD EYE BARRIER; C57BL MOUSE; CAPILLARY PERMEABILITY; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE; PATHOLOGY; PATHOPHYSIOLOGY; TRANSGENIC MOUSE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BLOOD-AQUEOUS BARRIER; CAPILLARY PERMEABILITY; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; MIDDLE AGED; NERVE TISSUE PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR;

EID: 84911885234     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-141215     Document Type: Article

References (39)

1. Keihaninejad S, Ryan NS, Malone IB, Modat M, Cash D, Ridgway GR, Zhang H, Fox NC, Ourselin S (2012) Theimportance of group-wise registration in tract based spatial statistics study of neurodegeneration: A simulation study inAlzheimer's disease. PLoS One 7, e45996.
2. Preti MG, Baglio F, Lagana MM, Griffanti L, Nemni R, Clerici M, Bozzali M, Baselli G (2012) Assessing corpus callosumchanges in Alzheimer's disease: Comparison between tractbasedspatial statistics and atlas-based tractography. PloS One 7, e35856.
3. Dubois B, Gauthier S, Cummings J (2013) The utility of thenew research diagnostic criteria for Alzheimer's disease. Int Psychogeriatr 25, 175-177.
4. Giacobini E, Gold G (2013) Alzheimer disease therapy movingfrom amyloid-beta to tau. Nat Rev Neurol 12, 223.
5. Rosenblum WI (2014) Why Alzheimer trials fail: Removingsoluble oligomeric beta amyloid is essential, inconsistent, anddifficult. Neurobiol Aging 35, 969-974.
6. Peng J, Liang G, Inan S, Wu Z, Joseph DJ, Meng Q, Peng Y, Eckenhoff MF, Wei H (2012) Dantrolene amelioratescognitive decline and neuropathology in Alzheimer tripletransgenic mice. Neurosci Lett 516, 274-279.
7. Akiyama H, Hosokawa M, Kametani F, Kondo H, Chiba M, Fukushima M, Tabira T (2012) Long-term oral intake of aluminiumor zinc does not accelerate Alzheimer pathology inAbetaPP and AbetaPP/tau transgenic mice. Neuropathology32, 390-397.
8. Hiltunen M, Khandelwal VK, Yaluri N, Tiilikainen T, Tusa M, Koivisto H, Krzisch M, Vepsalainen S, Makinen P, Kemppainen S, Miettinen P, Haapasalo A, Soininen H, Laakso M, Tanila H (2012) Contribution of genetic and dietary insulinresistance to Alzheimer phenotype in APP/PS1 transgenicmice. J Cell Mol Med 16, 1206-1222.
9. Deane R, Wu Z, Zlokovic BV (2004) RAGE (yin) versusLRP (yang) balance regulates alzheimer amyloid beta-peptideclearance through transport across the blood-brain barrier. Stroke 35, 2628-2631.
10. Chin J (2011) Selecting a mouse model of Alzheimer's disease. Methods Mol Biol 670, 169-189.
11. Abbott NJ (2013) Blood-brain barrier structure and functionand the challenges for CNS drug delivery. J Inherit Metab Dis36, 437-449.
12. Desai BS, Monahan AJ, Carvey PM, Hendey B (2007) Blood-brain barrier pathology in Alzheimer's and Parkinson'sdisease: Implications for drug therapy. Cell Transplant 16, 285-299.
13. Bell RD, Winkler EA, Sagare AP, Singh I, LaRue B, Deane R, Zlokovic BV (2010) Pericytes control key neurovascularfunctions and neuronal phenotype in the adult brain and duringbrain aging. Neuron 68, 409-427.
14. Winkler EA, Sengillo JD, Bell RD, Wang J, Zlokovic BV (2012) Blood-spinal cord barrier pericyte reductions contributeto increased capillary permeability. J Cereb BloodFlow Metab 32, 1841-1852.
15. Sagare AP, Bell RD, Zhao Z, Ma Q, Winkler EA, Ramanathan A, Zlokovic BV (2013) Pericyte loss influences Alzheimerlikeneurodegeneration in mice. Nat Commun 4, 2932.
16. Sengillo JD, Winkler EA, Walker CT, Sullivan JS, Johnson M, Zlokovic BV (2013) Deficiency in mural vascular cellscoincides with blood-brain barrier disruption in Alzheimer'sdisease. Brain Pathol 23, 303-310.
17. Brose K, Bland KS, Wang KH, Arnott D, Henzel W, Goodman CS, Tessier-Lavigne M, Kidd T (1999) Slit proteins bindRobo receptors and have an evolutionarily conserved role inrepulsive axon guidance. Cell 96, 795-806.
18. Fujiwara M, Ghazizadeh M, Kawanami O (2006) Potentialrole of the Slit/Robo signal pathway in angiogenesis. VascMed 11, 115-121.
19. Brown WR, Thore CR (2011) Review: Cerebral microvascularpathology in ageing and neurodegeneration. Neuropathol Appl Neurobiol 37, 56-74.
20. Han HX, Geng JG (2011) Over-expression of Slit2 inducesvessel formation and changes blood vessel permeability inmouse brain. Acta Pharmacol Sin 32, 1327-1336.
21. Emerich DF, Skinner SJ, Borlongan CV, Vasconcellos AV, Thanos CG (2005) The choroid plexus in the rise, fall andrepair of the brain. Bioessays 27, 262-274.
22. Wu Z, Guo H, Chow N, Sallstrom J, Bell RD, Deane R, Brooks AI, Kanagala S, Rubio A, Sagare A, Liu D, Li F, Armstrong D, Gasiewicz T, Zidovetzki R, Song X, Hofman F, Zlokovic BV (2005) Role of the MEOX2 homeobox gene in neurovasculardysfunction in Alzheimer disease. Nat Med 11, 959-965.
23. Bell RD, Deane R, Chow N, Long X, Sagare A, Singh I, Streb JW, Guo H, Rubio A, Van Nostrand W, Miano JM, Zlokovic BV (2009) SRF and myocardin regulate LRPmediatedamyloid-beta clearance in brain vascular cells. Nat Cell Biol 11, 143-153.
24. BradburyMW (1984) The structure and function of the bloodbrainbarrier. Fed Proc 43, 186-190.
25. Hawkins RA (2009) The blood-brain barrier and glutamate. Am J Clin Nutr 90, 867S-874S.
26. Cohen-Kashi-Malina K, Cooper I, Teichberg VI (2012) Mechanisms of glutamate efflux at the blood-brain barrier:Involvement of glial cells. J Cereb Blood Flow Metab 32, 177-189.
27. Kulijewicz-Nawrot M, Sykova E, Chvatal A, Verkhratsky A, Rodriguez JJ (2013) Astrocytes and glutamate homoeostasisin Alzheimer's disease: A decrease in glutamine synthetase, but not in glutamate transporter-1, in the prefrontal cortex. ASN Neuro 5, 273-282.
28. Matos M, Augusto E, Oliveira CR, Agostinho P (2008) Amyloid-beta peptide decreases glutamate uptake in culturedastrocytes: Involvement of oxidative stress andmitogen-activated protein kinase cascades. Neuroscience 156, 898-910.
29. Krezymon A, Richetin K, Halley H, Roybon L, Lassalle JM, Frances B, Verret L, Rampon C (2013) Modifications of hippocampalcircuits and early disruption of adult neurogenesisin the tg2576 mouse model of Alzheimer's disease. PLoS One8, e76497.
30. Yakel JL, Shao Z (2004) Functional and molecular characterizationof neuronal nicotinicACh receptors in rat hippocampalinterneurons. Prog Brain Res 145, 95-107.
31. Armstrong RA (2011) The pathogenesis of Alzheimer's disease:A reevaluation of the "amyloid cascade hypothesis". Int J Alzheimers Dis 2011, 630865.
32. Marques F, Sousa JC, Sousa N, Palha JA (2013) Blood-brain-barriers in aging and in Alzheimer's disease. Mol Neurodegener 8, 38.
33. Bell RD, Winkler EA, Singh I, Sagare AP, Deane R, Wu Z, Holtzman DM, Betsholtz C, Armulik A, Sallstrom J, Berk BC, Zlokovic BV (2012) Apolipoprotein E controls cerebrovascularintegrity via cyclophilin A. Nature 485, 512-516.
34. Acevedo LM, Weis SM, Cheresh DA (2008) Robo4 counteractsVEGF signaling. Nat Med 14, 372-373.
35. Yuen DA, Robinson LA (2013) Slit2-Robo signaling:Anovelregulator of vascular injury. Curr Opin Nephrol Hypertens 22, 445-451.
36. Jones CA, London NR, Chen H, Park KW, Sauvaget D, Stockton RA, Wythe JD, Suh W, Larrieu-Lahargue F, Mukouyama YS, Lindblom P, Seth P, Frias A, Nishiya N, Ginsberg MH, Gerhardt H, Zhang K, Li DY (2008) Robo4stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat Med 14, 448-453.
37. Guijarro-Munoz I, Cuesta AM, Alvarez-Cienfuegos A, Geng JG, Alvarez-Vallina L, Sanz L (2012) The axonal repellentSlit2 inhibits pericyte migration: Potential implications inangiogenesis. Exp Cell Res 318, 371-378.
38. Takechi R, Pallebage-Gamarallage MM, Lam V, Giles C, MamoJC (2013) Aging-related changes in blood-brain barrierintegrity and the effect of dietary fat. Neurodegener Dis 12, 125-135.
39. Bowman GL, Kaye JA, Quinn JF (2012) Dyslipidemia and blood-brain barrier integrity in Alzheimer's disease. Curr Gerontol Geriatr Res 2012, 184042.