Is vasomotion in cerebral arteries impaired in Alzheimer's disease?

Journal of Alzheimer's Disease

Volumn 46, Issue 1, 2015, Pages 35-53

  Di Marco, Luigi Yuri ^a   Farkas, Eszter ^b   Martin, Chris ^a   Venneri, Annalena ^a,c   Frangi, Alejandro F ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF SZEGED   (Hungary)

^c IRCCS SAN CAMILLO HOSPITAL   (Italy)

Author keywords

Alzheimer's disease; cerebral amyloid angiopathy; cerebral autoregulation; endothelium; perivascular drainage; vascular smooth muscle cell; vasomotion

Indexed keywords

AMYLOID BETA PROTEIN;

ALZHEIMER DISEASE; ARTERIOLE; ARTERY DIAMETER; ARTICLE; BLOOD BRAIN BARRIER; BLOOD VESSEL REACTIVITY; BLOOD VESSEL TONE; BLOOD VESSEL WALL; BRAIN ARTERY; BRAIN BLOOD VESSEL; BRAIN CIRCULATION; BRAIN HEMORRHAGE; BRAIN HYPOXIA; BRAIN ISCHEMIA; BRAIN PERFUSION; CEREBROVASCULAR DISEASE; CHOLINERGIC SYSTEM; DISEASE PREDISPOSITION; HUMAN; NONHUMAN; OXIDATIVE STRESS; OXYGEN TRANSPORT; PATHOGENESIS; PRIORITY JOURNAL; VASCULAR AMYLOIDOSIS; WHITE MATTER INJURY; ADRENERGIC SYSTEM; CEREBRAL ARTERIAL DISEASES; COMPLICATION; PATHOLOGY; PATHOPHYSIOLOGY;

ALZHEIMER DISEASE; CEREBRAL ARTERIAL DISEASES; CEREBRAL ARTERIES; HUMANS; VASOMOTOR SYSTEM;

EID: 84929379204     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-142976     Document Type: Article

References (248)

1. Paulson OB, Strandgaard S, Edvinsson L (1990) Cerebral autoregulation. Cerebrovasc Brain Metab Rev 2, 161-192.
2. Johansson B, Mellander S (1975) Static and dynamic components in the vascular myogenic response to passive changes in length as revealed by electrical and mechanical recordings from the rat portal vein. Circ Res 36, 76-83.
3. Pradhan RK, Chakravarthy VS (2011) Informational dynamics of vasomotion in microvascular networks: A review. Acta Physiol (Oxf) 201, 193-218.
4. Intaglietta M (1991) Arteriolar vasomotion: Implications for tissue ischemia. Blood Vessels 28(Suppl 1), 1-7.
5. Aalkjær C, Boedtkjer D, Matchkov V (2011) Vasomo-tion-what is currently thought? Acta Physiol (Oxf) 202, 253-269.
6. Haddock RE, Hill CE (2005) Rhythmicity in arterial smooth muscle. J Physiol 566, 645-656.
7. Haddock RE, Hill CE (2002) Differential activation of ion channels by inositol 1, 4, 5-trisphosphate (IP3)-and ryanodine-sensitive calcium stores in rat basilar artery vaso-motion. J Physiol 545, 615-627.
8. Haddock RE, Grayson TH, Brackenbury TD, Meaney KR, Neylon CB, Sandow SL, Hill CE (2006) Endothelial coordination of cerebral vasomotion via myoendothelial gap junctions containing connexins 37 and 40. Am J Physiol Heart Circ Physiol 291, H2047-H2056.
9. Sakurai T, Terui N (2006) Effectsofsympathetically induced vasomotionontissue-capillary fluid exchange. Am JPhysiol Heart Circ Physiol 291, H1761-H1767.
10. Rücker M, Strobel O, Vollmar B, Roesken F, Menger MD (2000) Vasomotion in critically perfused muscle protects adjacent tissues from capillary perfusion failure. Am J Phys-iol Heart Circ Physiol 279, H550-H558.
11. Nilsson H, Aalkjaer C (2003) Vasomotion: Mechanisms and physiological importance. Mol Interv 3, 79-89.
12. Tsai AG, Intaglietta M (1993) Evidence of flowmotion induced changes in local tissue oxygenation. Int J Microcirc Clin Exp 12, 75-88.
13. Goldman D, Popel AS (2001) A computational study of the effect of vasomotion on oxygen transport from capillary networks. J Theor Biol 209, 189-199.
14. Pradhan RK, Chakravarthy VS (2007) A computational model that links non-periodic vasomotion to enhanced oxygenation in skeletal muscle. Math Biosci 209, 486-499.
15. Hapuarachchi T, Park CS, Payne S (2010) Quantification of the effects of vasomotion on mass transport to tissue from axisymmetric blood vessels. J Theor Biol 264, 553-559.
16. De Boer MP, Wijnstok NJ, Serné EH, Eringa EC, Stehouwer CDA, Flyvbjerg A, Hoekstra T, Heymans MW, Meijer RI, Twisk JW, Smulders YM (2014) Body mass index is related to microvascular vasomotion, this is partly explained by adiponectin. Eur J Clin Invest 44, 660-667.
17. Lacza Z, Hermán P, Görlach C, Hortobágyi T, Sándor P, Wahl M, Benyó Z (2001) NO synthase blockade induces chaotic cerebral vasomotion via activation of thromboxane receptors. Stroke 32, 2609-2614.
18. Plassman BL, Langa KM, Fisher GG, Heeringa SG, Weir DR, Ofstedal MB, Burke JR, Hurd MD, Potter GG, Rodgers WL, Steffens DC, Willis RJ, Wallace RB (2007) Prevalence of dementia in the United States: The aging, demographics, and memory study. Neuroepidemiology 29, 125-132.
19. Whitehouse PJ, Sciulli CG, Mason RM (1997) Dementia drug development: Useofinformation systemstoharmonize global drug development. Psychopharmacol Bull 33, 129-133.
20. Wilson RS, Weir DR, Leurgans SE, Evans DA, Hebert LE, Langa KM, Plassman BL, Small BJ, Bennett DA (2011) Sources of variability in estimates of the prevalence of Alzheimer's disease in the United States. Alzheimers Dement 7, 74-79.
21. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353-356.
22. Kelleher RJ, Soiza RL (2013) Evidence of endothelial dysfunction in the development of Alzheimer's disease: Is Alzheimer's a vascular disorder? Am J Cardiovasc Dis 3, 197-226.
23. Jellinger KA, Attems J (2005) Prevalence and pathogenic role of cerebrovascular lesions in Alzheimer disease. J Neu-rol Sci 229-230, 37-41.
24. delaTorre JC (2002) Alzheimer's disease: How does itstart? J Alzheimers Dis 4, 497-512.
25. Kalaria RN (2000) The role of cerebral ischemia in Alzheimer's disease. Neurobiol Aging 21, 321-330.
26. Zlokovic BV (2011) Neurovascular pathways to neurode-generation in Alzheimer's disease and other disorders. Nat Rev Neurosci 12, 723-738.
27. de la Torre JC (2004) Personal view: Is Alzheimer's disease a neurodegenerative or a vascular disorder? Data, dogma, and dialectics. Lancet Neurol 3, 184-190.
28. Cordonnier C, van der Flier WM (2011) Brain microb-leeds and Alzheimer's disease: Innocent observation or key player? Brain 134, 335-344.
29. Van Norden AGW, van Dijk EJ, de Laat KF, Scheltens P, Olderikkert MGM, de Leeuw FE (2012) Dementia: Alzheimer pathology and vascular factors: From mutually exclusive to interaction. Biochim Biophys Acta 1822, 340-349.
30. de la Torre JC, Mussivand T (1993) Can disturbed brain microcirculation cause Alzheimer's disease? Neurol Res 15, 146-153.
31. Stopa EG, Butala P, Salloway S, Johanson CE, Gonzalez L, Tavares R, Hovanesian V, Hulette CM, Vitek MP, Cohen RA (2008) Cerebral cortical arteriolar angiopathy, vascular beta-amyloid, smooth muscle actin, Braak stage, and APOE genotype. Stroke 39, 814-821.
32. Popa-Wagner A, Buga A-M, Popescu B, Muresanu D (2013) Vascular cognitive impairment, dementia, aging and energy demand. A vicious cycle. J Neural Transm. doi: 10.1007/s00702-013-1129-3
33. Brown WR, Thore CR (2011) Review: Cerebral microvascu-lar pathologyinageing and neurodegeneration. Neuropathol Appl Neurobiol 37, 56-74.
34. Van Beek AH, Claassen JA, Rikkert MGO, Jansen RW (2008) Cerebral autoregulation: An overview of current concepts and methodology with special focus on the elderly. J Cereb Blood Flow Metab 28, 1071-1085.
35. Iadecola C, Zhang F, Niwa K, Eckman C, Turner SK, Fischer E, Younkin S, Borchelt DR, Hsiao KK, Carlson GA (1999) SOD1 rescues cerebral endothelial dysfunction in mice overexpressing amyloid precursor protein. Nat Neu-rosci 2, 157-161.
36. Niwa K, Kazama K, Younkin L, Younkin SG, Carlson GA, Iadecola C (2002) Cerebrovascular autoregulation is profoundly impaired in mice overexpressing amyloid precursor protein. Am J Physiol Heart Circ Physiol 283, H315-H323.
37. Claassen JAHR, Zhang R (2011) Cerebral autoregulation in Alzheimer's disease. J Cereb Blood Flow Metab 31, 1572-1577.
38. Claassen JAHR, Diaz-Arrastia R, Martin-Cook K, Levine BD, Zhang R (2009) Altered cerebral hemodynamics in early Alzheimer disease: A pilot study using transcranial Doppler. J Alzheimers Dis 17, 621-629.
39. Tarumi T, Dunsky DI, Khan MA, Liu J, Hill C, Armstrong K, Martin-Cook K, Cullum CM, Zhang R (2014) Dynamic cerebral autoregulation and tissue oxygenation in amnestic mild cognitive impairment. J Alzheimers Dis 41, 765-778.
40. Gommer ED, Martens EGHJ, Aalten P, Shijaku E, Ver-hey FRJ, Mess WH, Ramakers IHGB, Reulen JPH (2012) Dynamic cerebral autoregulation in subjects with Alzheimer's disease, mild cognitive impairment, and controls: Evidence for increased peripheral vascular resistance with possible predictive value. J Alzheimers Dis 30, 805-813.
41. Habert MO, Spampinato U, Mas JL, Piketty ML, Bourdel MC, deRecondo J, Rondot P, Askienazy S (1991) Acompar-ative technetium 99m hexamethylpropylene amine oxime SPET study in different types of dementia. Eur J Nucl Med 18, 3-11.
42. Perani D, Di Piero V, Vallar G, Cappa S, Messa C, Bottini G, Berti A, Passafiume D, Scarlato G, Gerundini P (1988) Technetium-99m HM-PAO-SPECT study of regional cerebral perfusion in early Alzheimer's disease. J Nucl Med 29, 1507-1514.
43. Yoshikawa T, Murase K, Oku N, Imaizumi M, Takasawa M, Rishu P, Kimura Y, Ikejiri Y, Kitagawa K, Hori M, Hatazawa J (2003) Heterogeneity of cerebral blood flow in Alzheimer disease and vascular dementia. AJNR Am J Neuroradiol 24, 1341-1347.
44. Staffen W, Schönauer U, Zauner H, Spindler I, Mair A, Iglseder B, Bernroider G, Ladurner G (2006) Brain perfusion SPECT in patients with mild cognitive impairment and Alzheimer's disease: Comparison of a semiquantitative and a visual evaluation. J Neural Transm 113, 195-203.
45. Blaise R, Mateo V, Rouxel C, Zaccarini F, Glorian M, Béréziat G, Golubkov VS, Limon I (2012) Wild-type amyloid beta 1-40 peptide induces vascular smooth muscle cell death independently from matrix metalloprotease activity. Aging Cell 11, 384-393.
46. Maier FC, Wehrl HF, Schmid AM, Mannheim JG, Wiehr S, Lerdkrai C, Calaminus C, Stahlschmidt A, Ye L, Burnet M, Stiller D, Sabri O, Reischl G, Staufenbiel M, Garaschuk O, Jucker M, Pichler BJ (2014) Longitudinal PET-MRI reveals β-amyloid deposition and rCBF dynamics and connects vascular amyloidosis to quantitative loss of perfusion. Nat Med 20, 1485-1492.
47. Li H, Guo Q, Inoue T, Polito VA, Tabuchi K, Hammer RE, Pautler RG, Taffet GE, Zheng H (2014) Vascular and parenchymal amyloid pathology in an Alzheimer disease knock-in mouse model: Interplay with cerebral blood flow. Mol Neurodegener 9, 28.
48. Kara F, Dongen ES, van, Schliebs R, Buchem MA, van, Groot HJM, de, Alia A (2012) Monitoring blood flow alterations in the Tg2576 mouse model of Alzheimer's disease by in vivo magnetic resonance angiography at 17.6 T. Neuroimage 60, 958-966.
49. Park L, Koizumi K, El Jamal S, Zhou P, Previti M, Lou, Van Nostrand WE, Carlson G, Iadecola C (2014) Age-dependent neurovascular dysfunction and damage in a mouse model of cerebral amyloid angiopathy. Stroke 45, 1815-1821.
50. Thal DR, Griffin WST, de Vos RAI, Ghebremedhin E (2008) Cerebral amyloid angiopathy and its relationship to Alzheimer's disease. Acta Neuropathol 115, 599-609.
51. Maia LF, Mackenzie IRA, Feldman HH (2007) Clinical phe-notypes of cerebral amyloid angiopathy. J Neurol Sci 257, 23-30.
52. Chen H, Zhang JH (2011) Cerebral amyloid angiopathy-related microhemorrhages in Alzheimer's disease: A review of investigative animal models. Acta Neurochir Suppl 111, 15-17.
53. Kalaria RN (1999) The blood-brain barrier and cerebrovascular pathology in Alzheimer's disease. Ann N Y Acad Sci 893, 113-125.
54. Griffith TM, Edwards DH (1994) Fractal analysis of role of smooth muscle Ca2+ fluxes in genesis of chaotic arterial pressure oscillations. Am J Physiol 266, H1801-H1811.
55. Mayevsky A, Ziv I (1991) Oscillations of cortical oxidative metabolism and microcirculation in the ischaemic brain. Neurol Res 13, 39-47.
56. Gustafsson U, Wårdell K, Nilsson GE, Lewis DH (1991) Vasomotion in rat skeletal muscle induced by hemorrhage as recorded by laser-Doppler flowmetry. Microvasc Res 42, 224-228.
57. Vollmar B, Preissler G, Menger MD (1994) Hemorrhagic hypotension induces arteriolar vasomotion and intermittent capillary perfusion in rat pancreas. Am J Physiol 267, H1936-H1940.
58. Bek T, Jeppesen P, Kanters JK (2013) Spontaneous high frequency diameter oscillations of larger retinal arterioles are reduced in type 2 diabetes mellitus. Invest Ophthalmol Vis Sci 54, 636-640.
59. Benbow SJ, Pryce DW, Noblett K, MacFarlane IA, Friedmann PS, Williams G (1995) Flow motion in peripheral diabetic neuropathy. Clin Sci (Lond) 88, 191-196.
60. Stansberry KB, Shapiro SA, Hill MA, McNitt PM, Meyer MD, Vinik AI (1996) Impaired peripheral vasomotion in diabetes. Diabetes Care 19, 715-721.
61. Schmiedel O, Schroeter ML, Harvey JN (2007) Microalbu-minuria in Type 2 diabetes indicates impaired microvascular vasomotion and perfusion. Am J Physiol Heart Circ Physiol 293, H3424-H3431.
62. Osol G, Halpern W (1988) Spontaneous vasomotion in pressurized cerebral arteries from genetically hypertensive rats. Am J Physiol 254, H28-H33.
63. Lefer DJ, Lynch CD, Lapinski KC, Hutchins PM (1990) Enhanced vasomotion of cerebral arterioles in spontaneously hypertensive rats. Microvasc Res 39, 129-139.
64. Ahtiluoto S, Polvikoski T, Peltonen M, Solomon A, Tuomilehto J, Winblad B, Sulkava R, Kivipelto M (2010) Diabetes, Alzheimer disease, and vascular dementia: A population-based neuropathologic study. Neurology 75, 1195-1202.
65. Arvanitakis Z, Wilson RS, Bienias JL, Evans DA, Bennett DA (2004) Diabetes mellitus and risk of Alzheimer disease and decline in cognitive function. Arch Neurol 61, 661-666.
66. Ott A, Stolk RP, van Harskamp F, Pols HA, Hofman A, Breteler MM (1999) Diabetes mellitus and the risk of dementia: The Rotterdam Study. Neurology 53, 1937-1942.
67. Bermejo-Pareja F, Benito-León J, Louis ED, Trincado R, Carro E, Villarejo A, de la Cámara AG (2010) Risk of incident dementia in drug-untreated arterial hypertension: A population-based study. J Alzheimers Dis 22, 949-958.
68. Beydoun MA, Lhotsky A, Wang Y, Dal Forno G, An Y, Metter EJ, Ferrucci L, O'Brien R, Zonderman AB (2008) Association of adiposity status and changes in early to mid-adulthood with incidence of Alzheimer's disease. Am J Epidemiol 168, 1179-1189.
69. Fitzpatrick AL, Kuller LH, Lopez OL, Diehr P, O'Meara ES, Longstreth WT, Luchsinger JA (2009) Midlife and late-life obesity and the risk of dementia: Cardiovascular health study. Arch Neurol 66, 336-342.
70. Hassing LB, Dahl AK, Thorvaldsson V, Berg S, Gatz M, Pedersen NL, Johansson B (2009) Overweight in midlife and risk of dementia: A 40-year follow-up study. Int J Obes (Lond) 33, 893-898.
71. Morris MC, Scherr PA, Hebert LE, Glynn RJ, Bennett DA, Evans DA (2001) Association ofincident Alzheimer disease and blood pressure measured from 13 years before to 2 years after diagnosis in a large community study. Arch Neurol 58, 1640-1646.
72. Rönnemaa E, Zethelius B, Lannfelt L, Kilander L (2011) Vascular risk factors and dementia: 40-year follow-up of a population-based cohort. Dement Geriatr Cogn Disord 31, 460-466.
73. Atti AR, Palmer K, Volpato S, Winblad B, De Ronchi D, Fratiglioni L (2008) Late-life body mass index and dementia incidence: Nine-year follow-up data from the Kungsholmen Project. J Am Geriatr Soc 56, 111-116.
74. Hassing LB, Johansson B, Nilsson SE, Berg S, Pedersen NL, Gatz M, McClearn G (2002) Diabetes mellitusisarisk factor for vascular dementia, but not for Alzheimer's disease: A population-based study of the oldest old. Int Psychogeriatr 14, 239-248.
75. Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gunder-sen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med 4, 147ra111.
76. Iliff JJ, Wang M, Zeppenfeld DM, Venkataraman A, Plog BA, Liao Y, Deane R, Nedergaard M (2013) Cerebral arterial pulsation drives paravascular CSF-interstitial fluid exchange in the murine brain. J Neurosci 33, 18190-18199.
77. Hawkes CA, Jayakody N, Johnston DA, Bechmann I, Carare RO (2014) Failure of perivascular drainage of β-amyloid in cerebral amyloid angiopathy. Brain Pathol 24, 396-403.
78. Carare RO, Bernardes-Silva M, Newman TA, Page AM, Nicoll JAR, Perry VH, Weller RO (2008) Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: Significance for cerebral amyloid angiopathy and neuroimmunology. Neu-ropathol Appl Neurobiol 34, 131-144.
79. Weller RO, Subash M, Preston SD, Mazanti I, Carare RO (2008) Perivascular drainage of amyloid-beta peptides from the brain and its failure in cerebral amyloid angiopathy and Alzheimer's disease. Brain Pathol 18, 253-266.
80. Schley D, Carare-Nnadi R, Please CP, Perry VH, Weller RO (2006) Mechanisms to explain the reverse perivascular transport of solutes out of the brain. J Theor Biol 238, 962-974.
81. Diehl RR, Diehl B, Sitzer M, Hennerici M (1991) Spontaneous oscillations in cerebral blood flow velocity in normal humans and in patients with carotid artery disease. Neurosci Lett 127, 5-8.
82. Fujii K, Heistad DD, Faraci FM (1990) Vasomotion of basilar arteries in vivo. Am J Physiol 258, H1829-H1834.
83. Funk W, Endrich B, Messmer K, Intaglietta M (1983) Spontaneous arteriolar vasomotion as a determinant of peripheral vascular resistance. Int J Microcirc Clin Exp 2, 11-25.
84. Hartley CJ, Reddy AK, Madala S, Entman ML, Michael LH, Taffet GE (2004) Noninvasive ultrasonic measurement of arterial wall motion in mice. Am J Physiol Heart Circ Physiol 287, H1426-H1432.
85. Hartley CJ, Reddy AK, Madala S, Entman ML, Taffet GE (2010) Feasibility of dual Doppler velocity measurements to estimate volume pulsations of an arterial segment. Ultrasound Med Biol 36, 1169-1175.
86. Aalkjaer C, Nilsson H (2005) Vasomotion: Cellular background for the oscillator and for the synchronization of smooth muscle cells. Br J Pharmacol 144, 605-616.
87. Segal SS, Bény JL (1992) Intracellular recording and dye transfer in arterioles during blood flow control. Am J Physiol 263, H1-H7.
88. Gustafsson H (1993) Vasomotion and underlying mechanisms in small arteries. An in vitro study of rat blood vessels. Acta Physiol Scand Suppl 614, 1-44.
89. Gokina NI, Bevan RD, Walters CL, Bevan JA (1996) Electrical activity underlying rhythmic contraction in human pial arteries. Circ Res 78, 148-153.
90. Peng H, Matchkov V, Ivarsen A, Aalkjaer C, Nilsson H (2001) Hypothesis for the initiation of vasomotion. Circ Res 88, 810-815.
91. Oishi H, Schuster A, Lamboley M, Stergiopulos N, Meister J-J, Bény J-L (2002) Role of membrane potential in vasomotion of isolated pressurized rat arteries. Life Sci 71, 2239-2248.
92. Dirnagl U, Lindauer U, Villringer A (1993) Nitric oxide synthase blockade enhances vasomotion in the cerebral microcirculation of anesthetized rats. Microvasc Res 45, 318-323.
93. Yuill KH, McNeish AJ, Kansui Y, Garland CJ, Dora KA (2010) Nitric oxide suppresses cerebral vasomo-tion by sGC-independent effects on ryanodine receptors and voltage-gated calcium channels. J Vasc Res 47, 93-107.
94. Thomsen ABK, Kim S, Aalbaek F, Aalkjaer C, Boedtkjer E (2014) Intracellular acidification alters myogenic responsiveness and vasomotion of mouse middle cerebral arteries. J Cereb Blood Flow Metab 34, 161-168.
95. Hempelmann RG, Pradel RH, Mehdorn HM, Ziegler A (1998) Contractions induced by NO synthase inhibition in isolated rat basilar artery: Role of the endothelium and endogenous vasoconstrictors. Neurol Res 20, 63-72.
96. Jackson WF (1988) Oscillations in active tension in hamster aortas: Role of the endothelium. Blood Vessels 25, 144-156.
97. Okazaki K, Seki S, Kanaya N, Hattori J-I, Tohse N, Namiki A (2003) Role of endothelium-derived hyperpolarizing factor in phenylephrine-induced oscillatory vasomotion in rat small mesenteric artery. Anesthesiology 98, 1164-1171.
98. Omote M, Mizusawa H (1993) The role of sarcoplasmic reticulum in endothelium-dependent and endothelium-independent rhythmic contractions in the rabbit mesenteric artery. Acta Physiol Scand 149, 15-21.
99. Akata T, Kodama K, Takahashi S (1995) Role of endothe-lium in oscillatory contractile responses to various receptor agonistsinisolatedsmall mesenteric andepicardial coronary arteries. Jpn J Pharmacol 68, 331-343.
100. Kvandal P, Stefanovska A, Veber M, Kvernmo HD, Kver-mmo HD, Kirkebøen KA (2003) Regulation of human cutaneous circulation evaluated by laser Doppler flowme-try, iontophoresis, and spectral analysis: Importance of nitric oxide and prostaglandines. Microvasc Res 65, 160-171.
101. Bertuglia S, Colantuoni A, Intaglietta M (1995) Capillary reperfusion after L-arginine, L-NMMA, and L-NNA treatment in cheek pouch microvasculature. Microvasc Res 50, 162-174.
102. Sell M, Boldt W, Markwardt F (2002) Desynchronising effect of the endothelium on intracellular Ca2+ concentration dynamics in vascular smooth muscle cells of rat mesenteric arteries. Cell Calcium 32, 105-120.
103. Chemtob S, Inayatulla A, Varma DR (1992) Eicosanoid-dependent and endothelium-independent oscillations of rat aorta. J Vasc Res 29, 270-280.
104. Von der Weid PY, Bény JL (1993) Simultaneous oscillations in the membrane potential of pig coronary artery endothelial and smooth muscle cells. J Physiol 471, 13-24.
105. Filosa JA, Iddings JA (2013) Astrocyte regulationofcerebral vascular tone. Am J Physiol Heart Circ Physiol 305, H609-H619.
106. Filosa JA, Bonev AD, Nelson MT (2004) Calcium dynamics in cortical astrocytes and arterioles during neurovascular coupling. Circ Res 95, e73-e81.
107. Carmignoto G, Gómez-Gonzalo M (2010) The contribution of astrocyte signalling to neurovascular coupling. Brain Res Rev 63, 138-148.
108. Girouard H, Iadecola C (2006) Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol 100, 328-335.
109. Iadecola C (2004) Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev Neurosci 5, 347-360.
110. Brown EB, Shear JB, Adams SR, Tsien RY, Webb WW (1999) Photolysis of caged calcium in femtoliter volumes using two-photon excitation. Biophys J 76, 489-499.
111. Soeller C, Cannell MB (1999) Two-photon microscopy: Imaging in scattering samples and three-dimensionally resolved flash photolysis. Microsc Res Tech 47, 182-195.
112. Mulligan SJ, MacVicar BA (2004) Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431, 195-199.
113. Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann K-A, Pozzan T, Carmignoto G (2003) Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 6, 43-50.
114. Peng X, Carhuapoma JR, Bhardwaj A, Alkayed NJ, Falck JR, Harder DR, Traystman RJ, Koehler RC (2002) Suppression of cortical functional hyperemia to vibrissal stimulation in the rat by epoxygenase inhibitors. Am J Physiol Heart Circ Physiol 283, H2029-H2037.
115. Peng X, Zhang C, Alkayed NJ, Harder DR, Koehler RC (2004) Dependency of cortical functional hyperemia to forepaw stimulation on epoxygenase and nitric oxide synthase activities in rats. J Cereb Blood Flow Metab 24, 509-517.
116. Attwell D, Buchan AM, Charpak S, Lauritzen M, Macvicar BA, Newman EA (2010) Glial and neuronal control of brain blood flow. Nature 468, 232-243.
117. Blanco VM, Stern JE, Filosa JA (2008) Tone-dependent vascular responses to astrocyte-derived signals. Am J Physiol Heart Circ Physiol 294, H2855-H2863.
118. Gordon GRJ, Choi HB, Rungta RL, Ellis-Davies GCR, MacVicar BA (2008) Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 456, 745-749.
119. Metea MR, Newman EA (2006) Glial cells dilate and constrict blood vessels: A mechanism of neurovascular coupling. J Neurosci 26, 2862-2870.
120. Girouard H, Bonev AD, Hannah RM, Meredith A, Aldrich RW, Nelson MT (2010) Astrocytic endfoot Ca2+ and BK channels determine both arteriolar dilation and constriction. Proc Natl Acad Sci USA 107, 3811-3816.
121. Porter JT, McCarthy KD (1996) Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J Neurosci 16, 5073-5081.
122. Brown LA, Key BJ, Lovick TA (2002) Inhibition of vaso-motion in hippocampal cerebral arterioles during increases in neuronal activity. Auton Neurosci 95, 137-140.
123. Lovick TA, Brown LA, Key BJ (2005) Neuronal activity-related coupling in cortical arterioles: Involvement of astrocyte-derived factors. Exp Physiol 90, 131-140.
124. Ruzali WAW, Kehoe PG, Love S (2013) Influence of LRP-1 and apolipoprotein E on amyloid-β uptake and toxicity to cerebrovascular smooth muscle cells. J Alzheimers Dis 33, 95-110.
125. Stukas S, Robert J, Wellington CL (2014) High-density lipoproteins and cerebrovascular integrity in Alzheimer's disease. Cell Metab 19, 574-591.
126. Attems J, Jellinger K, Thal DR, Van Nostrand W (2011) Review: Sporadic cerebral amyloid angiopathy. Neu-ropathol Appl Neurobiol 37, 75-93.
127. Imaoka K, Kobayashi S, Fujihara S, Shimode K, Nagasaki M (1999) Leukoencephalopathy with cerebral amyloid angiopathy: A semiquantitative and morphometric study. J Neurol 246, 661-666.
128. Tian J, Shi J, Smallman R, Iwatsubo T, Mann DMA (2006) Relationships in Alzheimer's disease between the extent of Abeta deposition in cerebral blood vessel walls, as cerebral amyloid angiopathy, and the amount of cerebrovascular smooth muscle cells and collagen. Neuropathol Appl Neurobiol 32, 332-340.
129. Zekry D, Duyckaerts C, Belmin J, Geoffre C, Moulias R, Hauw J-J (2003) Cerebral amyloid angiopathy in the elderly: Vessel walls changes and relationship with dementia. Acta Neuropathol 106, 367-373.
130. Winkler DT, Bondolfi L, Herzig MC, Jann L, Calhoun ME, Wiederhold KH, Tolnay M, Staufenbiel M, Jucker M (2001) Spontaneous hemorrhagic stroke in a mouse model of cerebral amyloid angiopathy. J Neurosci 21, 1619-1627.
131. Christie R, Yamada M, Moskowitz M, Hyman B (2001) Structural and functional disruption of vascular smooth muscle cells in a transgenic mouse model of amyloid angiopathy. Am J Pathol 158, 1065-1071.
132. Zhang F, Eckman C, Younkin S, Hsiao KK, Iadecola C (1997) Increased susceptibility to ischemic brain damage in transgenic mice overexpressing the amyloid precursor protein. J Neurosci 17, 7655-7661.
133. Princz-Kranz FL, Mueggler T, Knobloch M, Nitsch RM, Rudin M (2010) Vascular response to acetazolamide decreases as a function of age in the arcA beta mouse model of cerebral amyloidosis. Neurobiol Dis 40, 284-292.
134. Vromman A, Trabelsi N, Rouxel C, Béréziat G, Limon I, Blaise R (2013) β-Amyloid context intensifies vascular smooth muscle cells induced inflammatory response and de-differentiation. Aging Cell 12, 358-369.
135. Grammas P (2011) Neurovascular dysfunction, inflammation and endothelial activation: Implications for the pathogenesis of Alzheimer's disease. J Neuroinflammation 8, 26.
136. Mark RJ, Hensley K, Butterfield DA, Mattson MP (1995) Amyloid beta-peptide impairs ion-motive ATPase activities: Evidence for a role in loss of neuronal Ca2+ homeostasis and cell death. J Neurosci 15, 6239-6249.
137. Hermes M, Eichhoff G, Garaschuk O (2010) Intracellular calcium signalling in Alzheimer's disease. J Cell Mol Med 14, 30-41.
138. Aliev G, Li Y, Palacios HH, Obrenovich ME (2011) Oxidative stress induced mitochondrial DNA deletion as a hallmark for the drug development in the context of the cerebrovascular diseases. Recent Pat Cardiovasc Drug Discov 6, 222-241.
139. Zhu X, Smith MA, Honda K, Aliev G, Moreira PI, Nuno-mura A, Casadesus G, Harris PLR, Siedlak SL, Perry G (2007) Vascular oxidative stress in Alzheimer disease. J Neurol Sci 257, 240-246.
140. Aliev G, Smith MA, Seyidov D, Neal ML, Lamb BT, Nuno-mura A, Gasimov EK, Vinters HV, Perry G, LaManna JC, Friedland RP (2002) The role of oxidative stress in the pathophysiology of cerebrovascular lesions in Alzheimer's disease. Brain Pathol 12, 21-35.
141. Müller WE, Eckert A, Kurz C, Eckert GP, Leuner K (2010) Mitochondrial dysfunction: Common final pathway in brain aging and Alzheimer's disease-therapeutic aspects. Mol Neurobiol 41, 159-171.
142. Aliev G, Priyadarshini M, Reddy VP, Grieg NH, Kamin-sky Y, Cacabelos R, Ashraf GM, Jabir NR, Kamal MA, Nikolenko VN, Zamyatnin AAJ, Benberin VV, Bachurin SO (2014) Oxidative stress mediated mitochondrial and vascular lesions as markers in the pathogenesis of Alzheimer disease. CurrMed Chem 21, 2208-2217.
143. Black S, Gao F, Bilbao J (2009) Understanding white matter disease: Imaging-pathological correlations in vascular cognitive impairment. Stroke 40, S48-S52.
144. Thore CR, Anstrom JA, Moody DM, Challa VR, Marion MC, Brown WR (2007) Morphometric analysis of arteriolar tortuosity in human cerebral white matter of preterm, young, and aged subjects. J Neuropathol Exp Neurol 66, 337-345.
145. Moody DM, Brown WR, Challa VR, Ghazi-Birry HS, Reboussin DM (1997) Cerebral microvascular alterations in aging, leukoaraiosis, and Alzheimer's disease. Ann N Y Acad Sci 826, 103-116.
146. Cuhlmann S, Van der Heiden K, Saliba D, Tremoleda JL, Khalil M, Zakkar M, Chaudhury H, Luong LA, Mason JC, Udalova I, Gsell W, Jones H, Haskard DO, Krams R, Evans PC (2011) Disturbed blood flow induces RelA expression via c-Jun N-terminal kinase 1: A novel mode of NF-κB regulation that promotes arterial inflammation. Circ Res 108, 950-959.
147. Heo K-S, Fujiwara K, Abe J-I (2014) Shear stress and atherosclerosis. Mol Cells 37, 435-440.
148. Chiu J-J, Chien S (2011) Effects of disturbed flow on vascular endothelium: Pathophysiological basis and clinical perspectives. Physiol Rev 91, 327-387.
149. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399, 601-605.
150. Mayhew JE, Askew S, Zheng Y, Porrill J, Westby GW, Redgrave P, Rector DM, Harper RM (1996) Cerebral vaso-motion: A 0.1-Hz oscillation in reflected light imaging of neural activity. Neuroimage 4, 183-193.
151. Griffith TM (1996) Temporal chaos in the microcirculation. Cardiovasc Res 31, 342-358.
152. Intaglietta M (1990) Vasomotion and flowmotion: Physiological mechanisms and clinical evidence. Vasc Med 1, 101-112.
153. Zhang Z, Khatami R (2014) Predominant endothelial vasomotor activity during human sleep: A near-infrared spectroscopy study. Eur J Neurosci 40, 3396-3404.
154. Glodzik L, Randall C, Rusinek H, de Leon MJ (2013) Cerebrovascular reactivity to carbon dioxide in Alzheimer's disease. J Alzheimers Dis 35, 427-440.
155. Balestrini S, Perozzi C, Altamura C, Vernieri F, Luzzi S, Bar-tolini M, Provinciali L, Silvestrini M (2013) Severe carotid stenosis and impaired cerebral hemodynamics can influence cognitive deterioration. Neurology 80, 2145-2150.
156. Ringelstein EB, Sievers C, Ecker S, Schneider PA, Otis SM (1988) Noninvasive assessment of CO2-induced cerebral vasomotor response in normal individuals and patients with internal carotid artery occlusions. Stroke 19, 963-969.
157. Ringelstein EB, Van Eyck S, Mertens I (1992) Evaluation of cerebral vasomotor reactivity by various vasodilating stimuli: Comparison of CO2 to acetazolamide. J Cereb Blood Flow Metab 12, 162-168.
158. Bär K-J, Boettger MK, Seidler N, Mentzel HJ, Terborg C, Sauer H (2007) Influence of galantamine on vasomotor reactivity in Alzheimer's disease and vascular dementia due to cerebral microangiopathy. Stroke 38, 3186-3192.
159. Bullock R, Mendelow AD, Bone I, Patterson J, Macleod WN, Allardice G (1985) Cerebral blood flow and CO2 responsiveness as an indicator of collateral reserve capacity in patients with carotid arterial disease. Br J Surg 72, 348-351.
160. Markus H, Cullinane M (2001) Severely impaired cere-brovascular reactivity predicts stroke and TIA risk in patients with carotid artery stenosis and occlusion. Brain 124, 457-467.
161. Vernieri F, Pasqualetti P, Passarelli F, Rossini PM, Silvestrini M (1999) Outcome of carotid artery occlusion is predicted by cerebrovascular reactivity. Stroke 30, 593-598.
162. Vernieri F, Pasqualetti P, Matteis M, Passarelli F, Troisi E, Rossini PM, Caltagirone C, Silvestrini M (2001) Effect of collateral blood flow and cerebral vasomotor reactivity on the outcome of carotid artery occlusion. Stroke 32, 1552-1558.
163. Vicenzini E, Ricciardi MC, Altieri M, Puccinelli F, Bonaffini N, Di Piero V, Lenzi GL (2007) Cerebrovascular reactivity in degenerative and vascular dementia: A transcranial Doppler study. Eur Neurol 58, 84-89.
164. Den Abeelen ASSM, Lagro J, van Beek AHEA, Claassen JAHR (2014) Impaired cerebral autoregulation and vasomotor reactivity in sporadic Alzheimer's disease. Curr Alzheimer Res 11, 11-17.
165. Silvestrini M, Pasqualetti P, Baruffaldi R, Bartolini M, Han-douk Y, Matteis M, Moffa F, Provinciali L, Vernieri F (2006) Cerebrovascular reactivity and cognitive decline in patients with Alzheimer disease. Stroke 37, 1010-1015.
166. de la Torre JC (2012) Cerebral hemodynamics and vascular risk factors: Setting the stage for Alzheimer's disease. J Alzheimers Dis 32, 553-567.
167. Han BH, Zhou M-L, Abousaleh F, Brendza RP, Dietrich HH, Koenigsknecht-Talboo J, Cirrito JR, Milner E, Holtz-man DM, Zipfel GJ (2008) Cerebrovascular dysfunction in amyloid precursor protein transgenic mice: Contribution of soluble and insoluble amyloid-beta peptide, partial restoration via gamma-secretase inhibition. J Neurosci 28, 13542-13550.
168. Dorr A, Sahota B, Chinta LV, Brown ME, Lai AY, Ma K, Hawkes CA, McLaurin J, Stefanovic B (2012) Amyloid-β-dependent compromise of microvascular structure and function in a model of Alzheimer's disease. Brain 135, 3039-3050.
169. Menendez-Gonzalez M, Garcia-Garcia J, Calleja S, Rojo J, Ribacoba R (2011) Vasomotor reactivity is similarly impaired in patients with Alzheimer's disease and patients with amyloid hemorrhage. J Neuroimaging 21, e83-e85.
170. Tsivgoulis G, Katsanos AH, Papageorgiou SG, Dardio-tis E, Voumvourakis K, Giannopoulos S (2014) The role of neurosonology in the diagnosis of vascular dementia. J Alzheimers Dis 42(Suppl 3), S251-S257.
171. Farkas E, Luiten PG (2001) Cerebral microvascular pathology in aging and Alzheimer's disease. Prog Neurobiol 64, 575-611.
172. Claassen JAHR, Jansen RWMM (2006) Cholinergically mediated augmentation of cerebral perfusion in Alzheimer's disease and related cognitive disorders: The cholinergic-vascular hypothesis. J Gerontol A Biol Sci Med Sci 61, 267-271.
173. Van Beek AHEA, Claassen JAHR (2011) The cerebrovascular role of the cholinergic neural system in Alzheimer's disease. Behav Brain Res 221, 537-542.
174. Silvestrini M, Viticchi G, Falsetti L, Balucani C, Vernieri F, Cerqua R, Luzzi S, Bartolini M, Provinciali L (2011) The role of carotid atherosclerosis in Alzheimer's disease progression. J Alzheimers Dis 25, 719-726.
175. Buratti L, Viticchi G, Falsetti L, Cagnetti C, Luzzi S, Bartolini M, Provinciali L, Silvestrini M (2014) Vascular impairment in Alzheimer's disease: The role of obstructive sleep apnea. J Alzheimers Dis 38, 445-453.
176. Zaknun JJ, Leblhuber F, Schücktanz H (2008) Value of cerebral blood flow quantification in the diagnosis of dementia. NuclMed Commun 29, 260-269.
177. Knapp WH, Dannenberg C, Marschall B, Zedlick D, Löschmann K, Bettin S, Barthel H, Seese A (1996) Changes in local cerebral blood flow by neuroactivation and vasoactivation in patients with impaired cognitive function. Eur J Nucl Med 23, 878-888.
178. Stoppe G, Schütze R, Kögler A, Staedt J, Munz DL, Emrich D, Rüther E. Cerebrovascular reactivity to acetazolamide in (senile) dementia of Alzheimer's type: Relationship to disease severity. Dementia 6, 73-82.
179. Bonte FJ, Devous MD, Reisch JS, Ajmani AK, Weiner MF, Hom J, Tintner R (1989) The effect of acetazolamide on regional cerebral blood flow in patients with Alzheimer's disease or stroke as measured by single-photon emission computed tomography. Invest Radiol 24, 99-103.
180. Pávics L, Grünwald F, Reichmann K, Sera T, Ambrus E, Horn R, Hartmann A, Menzel C, Csernay L, Biersack HJ (1998) rCBF SPECT and the acetazolamide test in the evaluation of dementia. Nucl Med Rev Cent East Eur 1, 13-19.
181. Martin C, Martindale J, Berwick J, Mayhew J (2006) Investigating neural-hemodynamic coupling and the hemodynamic response function in the awake rat. Neuroimage 32, 33-48.
182. Summers P, Taylor Z, Shih A (2014) Two-Photon imaging of cerebral vasodynamics in awake mice during health and disease. In Advances in Intravital Microscopy, Weigert R, ed. Springer, Netherlands, pp. 25-43.
183. Devor A, Sakadzic S, Srinivasan VJ, Yaseen MA, Nizar K, Saisan PA, Tian P, Dale AM, Vinogradov SA, Franceschini MA, Boas DA (2012) Frontiers in optical imaging of cerebral blood flow and metabolism. J Cereb Blood Flow Metab 32, 1259-1276.
184. Martin C (2014) Contributions and complexities from the use of in vivo animal models to improve understanding of human neuroimaging signals. Front Neurosci 8, 211.
185. Shih A, Drew P, Kleinfeld D (2014) Imaging vasodynamics in the awake mouse brain with two-photon microscopy. In Neurovascular Coupling Methods, Zhao M, Ma H, Schwartz TH, eds. Springer New York, pp. 55-73.
186. Palmer JC, Barker R, Kehoe PG, Love S (2012) Endothelin-1 is elevated in Alzheimer's disease and upregulated by amyloid-β. J Alzheimers Dis 29, 853-861.
187. Miners JS, Palmer JC, Tayler H, Palmer LE, Ashby E, Kehoe PG, Love S (2014) Aβ degradation or cerebral perfusion? Divergent effects of multifunctional enzymes. Front Aging Neurosci 6, 238.
188. Palmer JC, Kehoe PG, Love S (2010) Endothelin-converting enzyme-1 in Alzheimer's disease and vascular dementia. Neuropathol Appl Neurobiol 36, 487-497.
189. Maguire JJ (2002) Endothelin-converting enzyme activity in vascular smooth muscle preparations in vitro. Methods Mol Biol 206, 165-177.
190. Minami M, Kimura M, Iwamoto N, Arai H (1995) Endothelin-1-like immunoreactivity in cerebral cortex of Alzheimer-type dementia. Prog Neuropsychopharmacol Biol Psychiatry 19, 509-513.
191. Luo J, Grammas P (2010) Endothelin-1 is elevated in Alzheimer's disease brain microvessels and is neuroprotective. J Alzheimers Dis 21, 887-896.
192. Palmer JC, Tayler HM, Love S (2013) Endothelin-converting enzyme-1 activity, endothelin-1 production, and free radical-dependent vasoconstriction in Alzheimer's disease. J Alzheimers Dis 36, 577-587.
193. Palmer JC, Baig S, Kehoe PG, Love S (2009) Endothelin-converting enzyme-2 is increased in Alzheimer's disease and up-regulated by Abeta. Am J Pathol 175, 262-270.
194. Paris D, Humphrey J, Quadros A, Patel N, Crescentini R, Crawford F, Mullan M (2003) Vasoactive effects of A beta in isolated human cerebrovessels and in a transgenic mouse model of Alzheimer's disease: Role of inflammation. Neurol Res 25, 642-651.
195. Ivey ME, Osman N, Little PJ (2008) Endothelin-1 signalling in vascular smooth muscle: Pathways controlling cellular functions associated with atherosclerosis. Atherosclerosis 199, 237-247.
196. Delgado E, Marques-Neves C, Rocha I, Sales-Luis J, Silva-Carvalho L (2010) Endothelin-1 effects on spontaneous oscillations in choroidal arterioles. Acta Ophthalmol 88, 742-747.
197. Koenigsberger M, Sauser R, Bény J-L, Meister J-J (2005) Role of the endothelium on arterial vasomotion. Biophys J 88, 3845-3854.
198. Gentile MT, Vecchione C, Maffei A, Aretini A, Marino G, Poulet R, Capobianco L, Selvetella G, Lembo G (2004) Mechanisms of soluble beta-amyloid impairment of endothelial function. J Biol Chem 279, 48135-48142.
199. Toda N, Okamura T (2012) Cerebral blood flow regulation by nitric oxide in Alzheimer's disease. J Alzheimers Dis 32, 569-578.
200. Ciabattoni G, Porreca E, Di Febbo C, Di Iorio A, Paganelli R, Bucciarelli T, Pescara L, Del Re L, Giusti C, Falco A, Sau A, Patrono C, Davi G (2007) Determinants of platelet activation in Alzheimer's disease. Neurobiol Aging 28, 336-342.
201. Fonseca ACRG, Ferreiro E, Oliveira CR, Cardoso SM, Pereira CF (2013) Activation of the endoplasmic reticulum stress response by the amyloid-beta 1-40 peptide in brain endothelial cells. Biochim Biophys Acta 1832, 2191-2203.
202. Fonseca ACRG, Moreira PI, Oliveira CR, Cardoso SM, Pinton P, Pereira CF (2014) Amyloid-beta disrupts calcium and redox homeostasis inbrain endothelial cells.Mol Neurobiol. doi: 10.1007/s12035-014-8740-7
203. Aliev G, Palacios HH, Walrafen B, Lipsitt AE, Obrenovich ME, Morales L (2009) Brain mitochondria as a primary target in the development of treatment strategies for Alzheimer disease. Int J Biochem Cell Biol 41, 1989-2004.
204. Claudio L (1996) Ultrastructural features of the blood-brain barrier in biopsy tissue from Alzheimer's disease patients. Acta Neuropathol 91, 6-14.
205. Stewart PA, Hayakawa K, Akers MA, Vinters HV (1992) A morphometric study of the blood-brain barrier in Alzheimer's disease. Lab Invest 67, 734-742.
206. Aliev G, Seyidova D, Neal ML, Shi J, Lamb BT, Siedlak SL, Vinters HV, Head E, Perry G, Lamanna JC, Friedland RP, Cotman CW (2002) Atherosclerotic lesions and mitochondria DNA deletions in brain microvessels as a central target for the development of human AD and AD-like pathology in aged transgenic mice. Ann N Y Acad Sci 977, 45-64.
207. Aliev G, Smith MA, Obrenovich ME, de la Torre JC, Perry G (2003) Role of vascular hypoperfusion-induced oxida-tive stress and mitochondria failure in the pathogenesis of Azheimer disease. Neurotox Res 5, 491-504.
208. Grammas P, Martinez J, Miller B (2011) Cerebral microvascular endothelium and the pathogenesis of neu-rodegenerative diseases. Expert Rev Mol Med 13, e19.
209. De Bock M, Wang N, Decrock E, Bol M, Gadicherla AK, Culot M, Cecchelli R, Bultynck G, Leybaert L (2013) Endothelial calcium dynamics, connexin channels and blood-brain barrier function. Prog Neurobiol 108, 1-20.
210. ElAli A, Hermann DM (2011) ATP-binding cassette transporters and their roles in protecting the brain. Neuroscientist 17, 423-436.
211. Ueno M, Nakagawa T, Wu B, Onodera M, Huang C-L, Kusaka T, Araki N, Sakamoto H (2010) Transporters in the brain endothelial barrier. Curr Med Chem 17, 1125-1138.
212. Abuznait AH, Kaddoumi A (2012) Role of ABC transporters in the pathogenesis of Alzheimer's disease. ACS Chem Neu-rosci 3, 820-831.
213. Krohn M, Lange C, Hofrichter J, Scheffler K, Stenzel J, Steffen J, Schumacher T, Brüning T, Plath A-S, Alfen F, Schmidt A, Winter F, Rateitschak K, Wree A, Gsponer J, Walker LC, Pahnke J (2011) Cerebral amyloid-β proteosta-sis is regulated by the membrane transport protein ABCC1 in mice. J Clin Invest 121, 3924-3931.
214. Cirrito JR, Deane R, Fagan AM, Spinner ML, Parsada-nian M, Finn MB, Jiang H, Prior JL, Sagare A, Bales KR, Paul SM, Zlokovic BV, Piwnica-Worms D, Holtzman DM (2005) P-glycoprotein deficiency at the blood-brain barrier increases amyloid-beta deposition in an Alzheimer disease mouse model. J Clin Invest 115, 3285-3290.
215. Silverberg GD, Messier AA, Miller MC, Machan JT, Maj-mudar SS, Stopa EG, Donahue JE, Johanson CE (2010) Amyloid efflux transporter expression at the blood-brain barrier declines in normal aging. J Neuropathol Exp Neurol 69, 1034-1043.
216. Van Assema DME, Lubberink M, Bauer M, van der Flier WM, Schuit RC, Windhorst AD, Comans EFI, Hoetjes NJ, Tolboom N, Langer O, Müller M, Scheltens P, Lam-mertsma AA, van Berckel BNM (2012) Blood-brain barrier P-glycoprotein function in Alzheimer's disease. Brain 135, 181-189.
217. Suhara T, Magrané J, Rosen K, Christensen R, Kim H-S, Zheng B, McPhie DL, Walsh K, Querfurth H. Abeta42 generation is toxic to endothelial cells and inhibits eNOS function through an Akt/GSK-3beta signaling-dependent mechanism. Neurobiol Aging 24, 437-451.
218. Crouch PJ, Blake R, Duce JA, Ciccotosto GD, Li Q-X, Barnham KJ, Curtain CC, Cherny RA, Cappai R, Dyrks T, Masters CL, Trounce IA (2005) Copper-dependent inhibition of human cytochrome c oxidase by a dimeric conformer of amyloid-beta1-42. J Neurosci 25, 672-679.
219. Xu J, Chen S, Ku G, Ahmed SH, Chen H, Hsu CY (2001) Amyloid beta peptide-induced cerebral endothelial cell death involves mitochondrial dysfunction and caspase activation. J Cereb Blood Flow Metab 21, 702-710.
220. Manczak M, Anekonda TS, Henson E, Park BS, Quinn J, Reddy PH (2006) Mitochondria are a direct site of A beta accumulation in Alzheimer's disease neurons: Implications for free radical generation and oxidative damage in disease progression. HumMol Genet 15, 1437-1449.
221. Aliev G, Palacios HH, Lipsitt AE, Fischbach K, Lamb BT, Obrenovich ME, Morales L, Gasimov E, Bragin V (2009) Nitric oxide as an initiator of brain lesions during the development of Alzheimer disease. Neurotox Res 16, 293-305.
222. Busse R, Mülsch A (1990) Calcium-dependent nitric oxide synthesis in endothelial cytosol is mediated by calmodulin. FEBS Lett 265, 133-136.
223. Park WS, Han J, Earm YE (2008) Physiological role of inward rectifier K(+) channels in vascular smooth muscle cells. Pflugers Arch 457, 137-147.
224. Rodrigo GC, Standen NB (2005) ATP-sensitive potassium channels. Curr Pharm Des 11, 1915-1940.
225. Rosenblum WI, Wei EP, Kontos HA (2004) Vasodilation of brain surface arterioles by blockade of Na-H+ antiport and its inhibition by inhibitors of KATP channel openers. Brain Res 1005, 77-83.
226. Janigro D, Nguyen TS, Meno J, West GA, Winn HR (1997) Endothelium-dependent regulation of cerebrovascular tone by extracellular and intracellular ATP. Am J Physiol 273, H878-H885.
227. Brian JE, Faraci FM, Heistad DD (1996) Recent insights into the regulation of cerebral circulation. Clin Exp Pharmacol Physiol 23, 449-457.
228. Mayhan WG (1994) Effect of diabetes mellitus on response of the basilar artery to activation of ATP-sensitive potassium channels. Brain Res 636, 35-39.
229. Bari F, Louis TM, Meng W, Busija DW (1996) Global ischemia impairs ATP-sensitive K+ channel function in cerebral arterioles in piglets. Stroke 27, 1874-1880; discussion 1880-1881.
230. Liu Y, Gutterman DD (2002) Oxidative stress and potassium channel function. Clin Exp Pharmacol Physiol 29, 305-311.
231. Simpson JE, Ince PG, Shaw PJ, Heath PR, Raman R, Garwood CJ, Gelsthorpe C, Baxter L, Forster G, Matthews FE, Brayne C, Wharton SB (2011) Microarray analysis of the astrocyte transcriptome in the aging brain: Relationship to Alzheimer's pathology and APOE genotype. Neurobiol Aging 32, 1795-1807.
232. Casley CS, Lakics V, Lee H, Broad LM, Day TA, Cluett T, Smith MA, O'Neill MJ, Kingston AE (2009) Up-regulation of astrocyte metabotropic glutamate receptor 5 by amyloid-β peptide. Brain Res 1260, 65-75.
233. Alberdi E, Wyssenbach A, Alberdi M, Sánchez-Gomez MV, Cavaliere F, Rodriguez JJ, Verkhratsky A, Matute C (2013) Ca(2+)-dependent endoplasmic reticulum stress correlates with astrogliosis in oligomeric amyloid β-treated astrocytes and in a model of Alzheimer's disease. Aging Cell 12, 292-302.
234. Chow S-K, Yu D, Macdonald CL, Buibas M, Silva GA (2010) Amyloid β-peptide directly induces spontaneous calcium transients, delayed intercellular calcium waves and gliosis in rat cortical astrocytes. ASNNeuro 2, e00026.
235. Abramov AY, Canevari L, Duchen MR (2003) Changes in intracellular calcium and glutathione in astrocytes as the primary mechanism of amyloid neurotoxicity. J Neurosci 23, 5088-5095.
236. Abramov AY, Canevari L, Duchen MR (2004) Calcium signals induced by amyloid beta peptide and their consequences in neurons and astrocytes in culture. Biochim Biophys Acta 1742, 81-87.
237. Haughey NJ, Mattson MP (2003) Alzheimer's amyloid beta-peptide enhances ATP/gap junction-mediated calcium-wave propagation in astrocytes. Neuromolecular Med 3, 173-180.
238. Lim D, Iyer A, Ronco V, Grolla AA, Canonico PL, Aron-ica E, Genazzani AA (2013) Amyloid beta deregulates astroglial mGluR5-mediated calcium signaling via cal-cineurin and Nf-kB. Glia 61, 1134-1145.
239. Lim D, Ronco V, Grolla AA, Verkhratsky A, Genazzani AA (2014) Glial calcium signalling in Alzheimer's disease. Rev Physiol Biochem Pharmacol 167, 45-65.
240. Grolla AA, Fakhfouri G, Balzaretti G, Marcello E, Gardoni F, Canonico PL, DiLuca M, Genazzani AA, Lim D (2013) Aβ leads to Ca2+ signaling alterations and transcriptional changes in glial cells. Neurobiol Aging 34, 511-522.
241. Sarkar P, Narayanan J, Harder DR (2011) Differential effect of amyloid β on the cytochrome P450 epoxygenase activity in rat brain. Neuroscience 194, 241-249.
242. Yamamoto K, Ueta Y, Wang L, Yamamoto R, Inoue N, Inokuchi K, Aiba A, Yonekura H, Kato N (2011) Suppression of a neocortical potassium channel activity by intracellular amyloid-β and its rescue with Homer1a. J Neurosci 31, 11100-11109.
243. Bai J-Z, Lipski J (2014) Involvement of TRPV4 channels in Aβ(40)-induced hippocampal cell death and astrocytic Ca(2+) signalling. Neurotoxicology 41, 64-72.
244. Weller RO, Massey A, Newman TA, Hutchings M, Kuo YM, Roher AE (1998) Cerebral amyloid angiopathy: Amyloid beta accumulates in putative interstitial fluid drainage pathways in Alzheimer's disease. Am J Pathol 153, 725-733.
245. Weller RO, Nicoll JA (2003) Cerebral amyloid angiopathy: Pathogenesis and effects on the ageing and Alzheimer brain. Neurol Res 25, 611-616.
246. Colantuoni A, Bertuglia S, Intaglietta M (1985) Variations of rhythmic diameter changes at the arterial microvascular bifurcations. Pflugers Arch 403, 289-295.
247. Szabo T, Wu J (2000) A model for longitudinal and shear wave propagation in viscoelastic media. J Acoust Soc Am 107, 2437-2446.
248. Bamji-Mirza M, Callaghan D, Najem D, Shen S, Hasim MS, Yang Z, Zhang W (2014) Stimulation of insulin signaling and inhibition of JNK-AP1 activation protect cells from amyloid-β-induced signaling dysregulation and inflammatory response. J Alzheimers Dis 40, 105-122.