Age-dependent neurovascular dysfunction and damage in a mouse model of cerebral amyloid angiopathy

Stroke

Volumn 45, Issue 6, 2014, Pages 1815-1821

  Park, Laibaik ^a   Koizumi, Kenzo ^a   El Jamal, Sleiman ^a   Zhou, Ping ^a   Previti, Mary Lou ^b   Van Nostrand, William E ^b   Carlson, George ^c   Iadecola, Costantino ^a  

^a FEIL FAMILY BRAIN AND MIND RESEARCH INSTITUTE   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c MCLAUGHLIN RESEARCH INSTITUTE   (United States)

Author keywords

amyloid ; cerebral blood flow; cerebrovascular disorder

Indexed keywords

ADENOSINE; AMYLOID PRECURSOR PROTEIN; REACTIVE OXYGEN METABOLITE;

AGE; ANIMAL EXPERIMENT; ARTICLE; BRAIN BLOOD FLOW; CEREBROVASCULAR DISEASE; CONTROLLED STUDY; DRUG RESPONSE; HYPERCAPNIA; HYPEREMIA; LASER DOPPLER FLOWMETRY; MOUSE; MOUSE MODEL; NEOCORTEX; NONHUMAN; OXIDATIVE STRESS; PERICYTE; PRIORITY JOURNAL; SMOOTH MUSCLE; SOMATOSENSORY CORTEX; TRANSGENIC MOUSE; VASCULAR AMYLOIDOSIS; WILD TYPE;

AMYLOID-Β; CEREBRAL BLOOD FLOW; CEREBROVASCULAR DISORDER;

AMYLOID BETA-PEPTIDES; ANIMALS; BLOOD FLOW VELOCITY; CEREBRAL AMYLOID ANGIOPATHY; CEREBROVASCULAR CIRCULATION; DISEASE MODELS, ANIMAL; MALE; MICE; MICE, TRANSGENIC; SOMATOSENSORY CORTEX; TIME FACTORS;

EID: 84901846788     PISSN: 00392499     EISSN: 15244628     Source Type: Journal    
DOI: 10.1161/STROKEAHA.114.005179     Document Type: Article

References (35)

1. Iadecola C. The pathobiology of vascular dementia. Neuron. 2013;80:844-866.
2. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991;82:239-259.
3. Weller RO, Boche D, Nicoll JA. Microvasculature changes and cerebral amyloid angiopathy in Alzheimer's disease and their potential impact on therapy. Acta Neuropathol. 2009;118:87-102.
4. Kimberly WT, Gilson A, Rost NS, Rosand J, Viswanathan A, Smith EE, et al. Silent ischemic infarcts are associated with hemorrhage burden in cerebral amyloid angiopathy. Neurology. 2009;72:1230-1235.
5. Gorelick PB, Scuteri A, Black SE, Decarli C, Greenberg SM, Iadecola C, et al; American Heart Association Stroke Council, Council on Epidemiology and Prevention, Council on Cardiovascular Nursing, Council on Cardiovascular Radiology and Intervention, and Council on Cardiovascular Surgery and Anesthesia. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2011;42:2672-2713.
6. Attems J, Jellinger K, Thal DR, Van Nostrand W. Review: sporadic cerebral amyloid angiopathy. Neuropathol Appl Neurobiol. 2011;37:75-93.
7. Charidimou A, Gang Q, Werring DJ. Sporadic cerebral amyloid angiopathy revisited: recent insights into pathophysiology and clinical spectrum. J Neurol Neurosurg Psychiatry. 2012;83:124-137.
8. Peca S, McCreary CR, Donaldson E, Kumarpillai G, Shobha N, Sanchez K, et al. Neurovascular decoupling is associated with severity of cerebral amyloid angiopathy. Neurology. 2013;81:1659-1665.
9. Viswanathan A, Greenberg SM. Cerebral amyloid angiopathy in the elderly. Ann Neurol. 2011;70:871-880.
10. Dumas A, Dierksen GA, Gurol ME, Halpin A, Martinez-Ramirez S, Schwab K, et al. Functional magnetic resonance imaging detection of vascular reactivity in cerebral amyloid angiopathy. Ann Neurol. 2012;72:76-81.
11. Davis J, Xu F, Deane R, Romanov G, Previti ML, Zeigler K, et al. Early-onset and robust cerebral microvascular accumulation of amyloid beta-protein in transgenic mice expressing low levels of a vasculotropic Dutch/Iowa mutant form of amyloid beta-protein precursor. J Biol Chem. 2004;279:20296-20306.
12. Fan R, Xu F, Previti ML, Davis J, Grande AM, Robinson JK, et al. Minocycline reduces microglial activation and improves behavioral def-cits in a transgenic model of cerebral microvascular amyloid. J Neurosci. 2007;27:3057-3063.
13. Xu F, Grande AM, Robinson JK, Previti ML, Vasek M, Davis J, et al. Early-onset subicular microvascular amyloid and neuroinfammation correlate with behavioral defcits in vasculotropic mutant amyloid beta-protein precursor transgenic mice. Neuroscience. 2007;146:98-107.
14. Park L, Zhou P, Koizumi K, El Jamal S, Previti ML, Van Nostrand WE, et al. Brain and circulating levels of Aβ1-40 differentially contribute to vasomotor dysfunction in the mouse brain. Stroke. 2013;44:198-204.
15. Iadecola C, Zhang F, Niwa K, Eckman C, Turner SK, Fischer E, et al. SOD1 rescues cerebral endothelial dysfunction in mice overexpressing amyloid precursor protein. Nat Neurosci. 1999;2:157-161.
16. Park L, Anrather J, Forster C, Kazama K, Carlson GA, Iadecola C. Abeta-induced vascular oxidative stress and attenuation of functional hyperemia in mouse somatosensory cortex. J Cereb Blood Flow Metab. 2004;24:334-342.
17. Park L, Anrather J, Zhou P, Frys K, Pitstick R, Younkin S, et al. NADPH-oxidase-derived reactive oxygen species mediate the cerebro-vascular dysfunction induced by the amyloid beta peptide. J Neurosci. 2005;25:1769-1777.
18. Park L, Zhou P, Pitstick R, Capone C, Anrather J, Norris EH, et al. Nox2-derived radicals contribute to neurovascular and behavioral dysfunction in mice overexpressing the amyloid precursor protein. Proc Natl Acad Sci USA. 2008;105:1347-1352.
19. Tong XK, Nicolakakis N, Kocharyan A, Hamel E. Vascular remodeling versus amyloid beta-induced oxidative stress in the cerebrovas-cular dysfunctions associated with Alzheimer's disease. J Neurosci. 2005;25:11165-11174.
20. Park L, Zhou J, Zhou P, Pistick R, El Jamal S, Younkin L, et al. Innate immunity receptor CD36 promotes cerebral amyloid angiopathy. Proc Natl Acad Sci USA. 2013;110:3089-3094.
21. Park L, Anrather J, Girouard H, Zhou P, Iadecola C. Nox2-derived reactive oxygen species mediate neurovascular dysregulation in the aging mouse brain. J Cereb Blood Flow Metab. 2007;27:1908-1918.
22. Niwa K, Araki E, Morham SG, Ross ME, Iadecola C. Cyclooxygenase-2 contributes to functional hyperemia in whisker-barrel cortex. J Neurosci. 2000;20:763-770.
23. Miao J, Xu F, Davis J, Otte-Höller I, Verbeek MM, Van Nostrand WE. Cerebral microvascular amyloid beta protein deposition induces vascular degeneration and neuroinfammation in transgenic mice expressing human vasculotropic mutant amyloid beta precursor protein. Am J Pathol. 2005;167:505-515.
24. Sagare AP, Bell RD, Zhao Z, Ma Q, Winkler EA, Ramanathan A, et al. Pericyte loss infuences Alzheimer-like neurodegeneration in mice. Nat Commun. 2013;4:2932.
25. Niwa K, Porter VA, Kazama K, Cornfeld D, Carlson GA, Iadecola C. A beta-peptides enhance vasoconstriction in cerebral circulation. Am J Physiol Heart Circ Physiol. 2001;281:H2417-H2424.
26. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev Neurosci. 2004;5:347-360.
27. Niwa K, Haensel C, Ross ME, Iadecola C. Cyclooxygenase-1 participates in selected vasodilator responses of the cerebral circulation. Circ Res. 2001;88:600-608.
28. Rosenblum WI. Hydroxyl radical mediates the endothelium-dependent relaxation produced by bradykinin in mouse cerebral arterioles. Circ Res. 1987;61:601-603.
29. Rosenblum WI, Nelson GH. Endothelium dependence of dilation of pial arterioles in mouse brain by calcium ionophore. Stroke. 1988;19:1379-1382.
30. Bell RD, Winkler EA, Sagare AP, Singh I, LaRue B, Deane R, et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron. 2010;68:409-427.
31. Wilhelmus MM, Otte-Höller I, van Triel JJ, Veerhuis R, Maat-Schieman ML, Bu G, et al. Lipoprotein receptor-related protein-1 mediates amyloid-beta-mediated cell death of cerebrovascular cells. Am J Pathol. 2007;171:1989-1999.
32. Capone C, Anrather J, Milner TA, Iadecola C. Estrous cycle-dependent neurovascular dysfunction induced by angiotensin II in the mouse neo-cortex. Hypertension. 2009;54:302-307.
33. Girouard H, Lessard A, Capone C, Milner TA, Iadecola C. The neu-rovascular dysfunction induced by angiotensin II in the mouse neo-cortex is sexually dimorphic. Am J Physiol Heart Circ Physiol. 2008;294:H156-H163.
34. Charidimou A, Jaunmuktane Z, Baron JC, Burnell M, Varlet P, Peeters A, et al. White matter perivascular spaces: an MRI marker in pathology-proven cerebral amyloid angiopathy? Neurology. 2014;82:57-62.
35. Yates PA, Villemagne VL, Ellis KA, Desmond PM, Masters CL, Rowe CC. Cerebral microbleeds: a review of clinical, genetic, and neuroimag-ing associations. Front Neurol. 2014;4:205.