The role of insulin in the vascular contributions to age-related dementia

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1862, Issue 5, 2016, Pages 983-991

  Hughes, Timothy M ^a   Craft, Suzanne ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Brain; Glucose; Insulin; Metabolism; Vascular

Indexed keywords

AMYLOID BETA PROTEIN; INSULIN;

AGING; ALZHEIMER DISEASE; ARTERIAL STIFFNESS; ARTERIOSCLEROSIS; ARTICLE; BLOOD BRAIN BARRIER; BLOOD VESSEL INJURY; BRAIN ATROPHY; BRAIN INJURY; BRAIN METABOLISM; COGNITIVE DEFECT; DEMENTIA; DISEASE COURSE; DYSLIPIDEMIA; ELEVATED BLOOD PRESSURE; ENDOTHELIAL DYSFUNCTION; FIBROSIS; GLUCOSE TRANSPORT; HUMAN; HYPERGLYCEMIA; HYPERINSULINEMIA; HYPERTENSION; INFLAMMATION; METABOLIC DISORDER; METABOLIC SYNDROME X; MICROANGIOPATHY; NONHUMAN; PRIORITY JOURNAL; VASCULAR DISEASE;

EID: 84950241835     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2015.11.013     Document Type: Article

References (151)

1. Jack C.R. Alzheimer disease: new concepts on its neurobiology and the clinical role imaging will play. Radiology 2012, 263:344-361.
2. Jack C.R., Holtzman D.M. Biomarker modeling of Alzheimer's disease. Neuron 2013, 80:1347-1358.
3. Schneider J.A., Wilson R.S., Bienias J.L., Evans D.A., Bennett D.A. Cerebral infarctions and the likelihood of dementia from Alzheimer disease pathology. Neurology 2004, 62:1148-1155.
4. Cullen K.M., Kocsi Z., Stone J. Microvascular pathology in the aging human brain: evidence that senile plaques are sites of microhaemorrhages. Neurobiol. Aging 2006, 27:1786-1796.
5. Iliff J.J., Wang M., Liao Y., Plogg B.A., Peng W., Gundersen G.A., Benveniste H., Vates G.E., Deane R., Goldman S.A., Nagelhus E.A., Nedergaard M. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci. Transl. Med. 2012, 4:147ra111.
6. Carare R.O., Bernardes-Silva M., Newman T.A., Page A.M., Nicoll J.A., Perry V.H., Weller R.O. Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: significance for cerebral amyloid angiopathy and neuroimmunology. Neuropathol. Appl. Neurobiol. 2008, 34:131-144.
7. Weller R.O., Djuanda E., Yow H.Y., Carare R.O. Lymphatic drainage of the brain and the pathophysiology of neurological disease. Acta Neuropathol. 2009, 117:1-14.
8. Bell R.D., Zlokovic B.V. Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease. Acta Neuropathol. 2009, 118:103-113.
9. Centers for Disease Control and Prevention National Diabetes Statistics Report: Estimates of Diabetes and Its Burden in the United States, GA: U.S. Department of Health and Human Services 2014.
10. Emerging Risk Factors, Sarwar N., Gao P., Seshasai S.R., Gobin R., Kaptoge S., Di Angelantonio E., Ingelsson E., Lawlor D.A., Selvin E., Stampfer M., Stehouwer C.D., Lewington S., Pennells L., Thompson A., Sattar N., White I.R., Ray K.K., Danesh J. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet 2010, 375:2215-2222.
11. Gorelick P.B., Scuteri A., Black S.E., Decarli C., Greenberg S.M., Iadecola C., Launer L.J., Laurent S., Lopez O.L., Nyenhuis D., Petersen R.C., Schneider J.A., Tzourio C., Arnett D.K., Bennett D.A., Chui H.C., Higashida R.T., Lindquist R., Nilsson P.M., Roman G.C., Sellke F.W., Seshadri S., C.o.E., American Heart Association Stroke Council, C.o.C.N.C.o.C.R.Prevention, Intervention, S.Council on Cardiovascular, 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.
12. Cheng G., Huang C., Deng H., Wang H. Diabetes as a risk factor for dementia and mild cognitive impairment: a meta-analysis of longitudinal studies. Intern. Med. J. 2012, 42:484-491.
13. Crescioni M., Gorina Y., Bilheimer L., Gillum R.F. Trends in health status and health care use among older men. Natl. Health Stat. Rep. 2010, 1-18.
14. H.K.H.c.o.a.a.y.a.o.U.S. Schoenborn CA, 2004-2007. National health statistics reports; no. 16 2009, National Center for Health Statistics, Hyattsville, MD.
15. Selby J.V., Peng T., Karter A.J., Alexander M., Sidney S., Lian J., Arnold A., Pettitt D. High rates of co-occurrence of hypertension, elevated low-density lipoprotein cholesterol, and diabetes mellitus in a large managed care population. Am. J. Manag. Care 2004, 10:163-170.
16. Qiu M., Shen W., Song X., Ju L., Tong W., Wang H., Zheng S., Jin Y., Wu Y., Wang W., Tian J. Effects of prediabetes mellitus alone or plus hypertension on subsequent occurrence of cardiovascular disease and diabetes mellitus: longitudinal study. Hypertension 2015, 65:525-530.
17. Cornier M.A., Dabelea D., Hernandez T.L., Lindstrom R.C., Steig A.J., Stob N.R., Van Pelt R.E., Wang H., Eckel R.H. The metabolic syndrome. Endocr. Rev. 2008, 29:777-822.
18. Rask-Madsen C., Kahn C.R. Tissue-specific insulin signaling, metabolic syndrome, and cardiovascular disease. Arterioscler. Thromb. Vasc. Biol. 2012, 32:2052-2059.
19. Tzourio C., Laurent S., Debette S. Is hypertension associated with an accelerated aging of the brain?. Hypertension 2014, 63:894-903.
20. Wiesmann M., Kiliaan A.J., Claassen J.A. Vascular aspects of cognitive impairment and dementia. J. Cereb. Blood Flow Metab. 2013, 33:1696-1706.
21. Rabkin S.W. Arterial stiffness: detection and consequences in cognitive impairment and dementia of the elderly. J. Alzheimers Dis. 2012, 32:541-549.
22. Gorelick P.B., Nyenhuis D., American Society of Hypertension Writing, Materson B.J., Calhoun D.A., Elliott W.J., Phillips R.A., Taler S.J., Townsend R.R. Blood pressure and treatment of persons with hypertension as it relates to cognitive outcomes including executive function. J. Am. Soc. Hypertens. 2012, 6:309-315.
23. Power M.C., Weuve J., Gagne J.J., McQueen M.B., Viswanathan A., Blacker D. The association between blood pressure and incident Alzheimer disease: a systematic review and meta-analysis. Epidemiology 2011, 22:646-659.
24. Pase M.P., Herbert A., Grima N.A., Pipingas A., O'Rourke M.F. Arterial stiffness as a cause of cognitive decline and dementia: a systematic review and meta-analysis. Intern. Med. J. 2012, 42:808-815.
25. Taylor C., Tillin T., Chaturvedi N., Dewey M., Ferri C.P., Hughes A., Prince M., Richards M., Shah A., Stewart R. Midlife hypertensive status and cognitive function 20 years later: the Southall and Brent revisited study. J. Am. Geriatr. Soc. 2013, 61:1489-1498.
26. Gottesman R.F., Schneider A.L., Albert M., Alonso A., Bandeen-Roche K., Coker L., Coresh J., Knopman D., Power M.C., Rawlings A., Sharrett A.R., Wruck L.M., Mosley T.H. Midlife hypertension and 20-year cognitive change: the atherosclerosis risk in communities neurocognitive study. JAMA Neurol. 2014.
27. Qiu C., Winblad B., Fratiglioni L. The age-dependent relation of blood pressure to cognitive function and dementia. Lancet Neurol. 2005, 4:487-499.
28. Birns J., Kalra L. Cognitive function and hypertension. J. Hum. Hypertens. 2009, 23:86-96.
29. Birns J., Morris R., Donaldson N., Kalra L. The effects of blood pressure reduction on cognitive function: a review of effects based on pooled data from clinical trials. J. Hypertens. 2006, 24:1907-1914.
30. Beauchet O., Celle S., Roche F., Bartha R., Montero-Odasso M., Allali G., Annweiler C. Blood pressure levels and brain volume reduction: a systematic review and meta-analysis. J. Hypertens. 2013, 31:1502-1516.
31. Muller M., Sigurdsson S., Kjartansson O., Aspelund T., Lopez O.L., Jonnson P.V., Harris T.B., van Buchem M., Gudnason V., Launer L.J., G.E.S.-R.S.I.Age Joint effect of mid- and late-life blood pressure on the brain: the AGES-Reykjavik study. Neurology 2014, 82:2187-2195.
32. Viswanathan A., Gray F., Bousser M.G., Baudrimont M., Chabriat H. Cortical neuronal apoptosis in CADASIL. Stroke 2006, 37:2690-2695.
33. Prabhakaran S., Wright C.B., Yoshita M., Delapaz R., Brown T., DeCarli C., Sacco R.L. Prevalence and determinants of subclinical brain infarction: the Northern Manhattan Study. Neurology 2008, 70:425-430.
34. Vlek A.L., Visseren F.L., Kappelle L.J., Geerlings M.I., Vincken K.L., Mali W.P., van der Graaf Y., Group S.S. Blood pressure and progression of cerebral atrophy in patients with vascular disease. Am. J. Hypertens. 2009, 22:1183-1189.
35. Vermeer S.E., Koudstaal P.J., Oudkerk M., Hofman A., Breteler M.M. Prevalence and risk factors of silent brain infarcts in the population-based Rotterdam Scan Study. Stroke 2002, 33:21-25.
36. Longstreth W.T., Bernick C., Manolio T.A., Bryan N., Jungreis C.A., Price T.R. Lacunar infarcts defined by magnetic resonance imaging of 3660 elderly people: the Cardiovascular Health Study. Arch. Neurol. 1998, 55:1217-1225.
37. Bezerra D.C., Sharrett A.R., Matsushita K., Gottesman R.F., Shibata D., Mosley T.H., Coresh J., Szklo M., Carvalho M.S., Selvin E. Risk factors for lacune subtypes in the Atherosclerosis Risk in Communities (ARIC) Study. Neurology 2012, 78:102-108.
38. Yates P.A., Villemagne V.L., Ellis K.A., Desmond P.M., Masters C.L., Rowe C.C. Cerebral microbleeds: a review of clinical, genetic, and neuroimaging associations. Front. Neurol. 2014, 4:205.
39. Vernooij M.W., van der Lugt A., Ikram M.A., Wielopolski P.A., Niessen W.J., Hofman A., Krestin G.P., Breteler M.M. Prevalence and risk factors of cerebral microbleeds: the Rotterdam Scan Study. Neurology 2008, 70:1208-1214.
40. Verhaaren B.F., Vernooij M.W., de Boer R., Hofman A., Niessen W.J., van der Lugt A., Ikram M.A. High blood pressure and cerebral white matter lesion progression in the general population. Hypertension 2013, 61:1354-1359.
41. Sparks D.L., Scheff S.W., Liu H., Landers T.M., Coyne C.M., Hunsaker J.C. Increased incidence of neurofibrillary tangles (NFT) in non-demented individuals with hypertension. J. Neurol. Sci. 1995, 131:162-169.
42. Petrovitch H., Ross G.W., Steinhorn S.C., Abbott R.D., Markesbery W., Davis D., Nelson J., Hardman J., Masaki K., Vogt M.R., Launer L., White L.R. AD lesions and infarcts in demented and non-demented Japanese-American men. Ann. Neurol. 2005, 57:98-103.
43. Petrovitch H., White L.R., Izmirilian G., Ross G.W., Havlik R.J., Markesbery W., Nelson J., Davis D.G., Hardman J., Foley D.J., Launer L.J. Midlife blood pressure and neuritic plaques, neurofibrillary tangles, and brain weight at death: the HAAS. Neurobiol. Aging 2000, 21:57-62.
44. Beach T.G., Wilson J.R., Sue L.I., Newell A., Poston M., Cisneros R., Pandya Y., Esh C., Connor D.J., Sabbagh M., Walker D.G., Roher A.E. Circle of Willis atherosclerosis: association with Alzheimer's disease, neuritic plaques and neurofibrillary tangles. Acta Neuropathol. 2007, 113:13-21.
45. Hoffman L.B., Schmeidler J., Lesser G.T., Beeri M.S., Purohit D.P., Grossman H.T., Haroutunian V. Less Alzheimer disease neuropathology in medicated hypertensive than nonhypertensive persons. Neurology 2009, 72:1720-1726.
46. Shah N.S., Vidal J.S., Masaki K., Petrovitch H., Ross G.W., Tilley C., DeMattos R.B., Tracy R.P., White L.R., Launer L.J. Midlife blood pressure, plasma beta-amyloid, and the risk for Alzheimer disease: the Honolulu Asia Aging Study. Hypertension 2012, 59:780-786.
47. Toledo J.B., Toledo E., Weiner M.W., Jack C.R., Jagust W., Lee V.M., Shaw L.M., Trojanowski J.Q., Alzheimer's disease Neuroimaging Cardiovascular risk factors, cortisol, and amyloid-beta deposition in Alzheimer's Disease Neuroimaging Initiative. Alzheimers Dement. 2012, 8:483-489.
48. Langbaum J.B., Chen K., Launer L.J., Fleisher A.S., Lee W., Liu X., Protas H.D., Reeder S.A., Bandy D., Yu M., Caselli R.J., Reiman E.M. Blood pressure is associated with higher brain amyloid burden and lower glucose metabolism in healthy late middle-age persons. Neurobiol. Aging 2012, 33:827.e11-827.e19.
49. Rodrigue K.M., Rieck J.R., Kennedy K.M., Devous M.D., Diaz-Arrastia R., Park D.C. Risk factors for beta-amyloid deposition in healthy aging: vascular and genetic effects. JAMA Neurol. 2013, 70:600-606.
50. Poels M.M., Zaccai K., Verwoert G.C., Vernooij M.W., Hofman A., van der Lugt A., Witteman J.C., Breteler M.M., Mattace-Raso F.U., Ikram M.A. Arterial stiffness and cerebral small vessel disease: the Rotterdam Scan Study. Stroke 2012, 43:2637-2642.
51. Jeerakathil T., Wolf P.A., Beiser A., Hald J.K., Au R., Kase C.S., Massaro J.M., DeCarli C. Cerebral microbleeds: prevalence and associations with cardiovascular risk factors in the Framingham Study. Stroke 2004, 35:1831-1835.
52. Henskens L.H., van Oostenbrugge R.J., Kroon A.A., de Leeuw P.W., Lodder J. Brain microbleeds are associated with ambulatory blood pressure levels in a hypertensive population. Hypertension 2008, 51:62-68.
53. Hughes T.M., Kuller L.H., Barinas-Mitchell E.J., McDade E.M., Klunk W.E., Cohen A.D., Mathis C.A., Dekosky S.T., Price J.C., Lopez O.L. Arterial stiffness and beta-amyloid progression in nondemented elderly adults. JAMA Neurol. 2014.
54. Hughes T.M., Kuller L.H., Barinas-Mitchell E.J.M., Mackey R.H., McDade E.M., Klunk W.E., Aizenstein H.J., Cohen A.D., Snitz B.E., Mathis C.A., DeKosky S.T., Lopez O.L. Pulse wave velocity is associated with β-amyloid deposition in the brains of very elderly adults. Neurology 2013.
55. Rizzoni D., Agabiti-Rosei E. Structural abnormalities of small resistance arteries in essential hypertension. Intern. Emerg. Med. 2012, 7:205-212.
56. O'Rourke M.F., Safar M.E. Relationship between aortic stiffening and microvascular disease in brain and kidney: cause and logic of therapy. Hypertension 2005, 46:200-204.
57. Mitchell G.F. Effects of central arterial aging on the structure and function of the peripheral vasculature: implications for end-organ damage. J. Appl. Physiol. 2008, 105:1652-1660.
58. AlGhatrif M., Strait J.B., Morrell C.H., Canepa M., Wright J., Elango P., Scuteri A., Najjar S.S., Ferrucci L., Lakatta E.G. Longitudinal trajectories of arterial stiffness and the role of blood pressure: the Baltimore longitudinal study of aging. Hypertension 2013, 62:934-941.
59. Lakatta E.G., Levy D. Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: part I: aging arteries: a "set up" for vascular disease. Circulation 2003, 107:139-146.
60. Scuteri A., Morrell C.H., Orru M., Strait J.B., Tarasov K.V., Ferreli L.A., Loi F., Pilia M.G., Delitala A., Spurgeon H., Najjar S.S., AlGhatrif M., Lakatta E.G. Longitudinal perspective on the conundrum of central arterial stiffness, blood pressure, and aging. Hypertension 2014, 64:1219-1227.
61. Safar M.E., Balkau B., Lange C., Protogerou A.D., Czernichow S., Blacher J., Levy B.I., Smulyan H. Hypertension and vascular dynamics in men and women with metabolic syndrome. J. Am. Coll. Cardiol. 2013, 61:12-19.
62. Serne E.H., Stehouwer C.D., ter Maaten J.C., ter Wee P.M., Rauwerda J.A., Donker A.J., Gans R.O. Microvascular function relates to insulin sensitivity and blood pressure in normal subjects. Circulation 1999, 99:896-902.
63. Mitchell G.F., Parise H., Benjamin E.J., Larson M.G., Keyes M.J., Vita J.A., Vasan R.S., Levy D. Changes in arterial stiffness and wave reflection with advancing age in healthy men and women: the Framingham Heart Study. Hypertension 2004, 43:1239-1245.
64. Safar M., O'Rourke M. Arterial Stiffness in Hypertension. Handbook of Hypertension 2006, Elsevier, London. W. Birkenhager, J. Reid (Eds.).
65. Liao D., Cooper L., Cai J., Toole J., Bryan N., Burke G., Shahar E., Nieto J., Mosley T., Heiss G. The prevalence and severity of white matter lesions, their relationship with age, ethnicity, gender, and cardiovascular disease risk factors: the ARIC Study. Neuroepidemiology 1997, 16:149-162.
66. Muller M., van der Graaf Y., Visseren F.L., Vlek A.L., Mali W.P., Geerlings M.I., Group S.S. Blood pressure, cerebral blood flow, and brain volumes. J. Hypertens. 2010, 28:1498-1505.
67. Xu T.Y., Staessen J.A., Wei F.F., Xu J., Li F.H., Fan W.X., Gao P.J., Wang J.G., Li Y. Blood flow pattern in the middle cerebral artery in relation to indices of arterial stiffness in the systemic circulation. Am. J. Hypertens. 2012, 25:319-324.
68. Webb A.J., Simoni M., Mazzucco S., Kuker W., Schulz U., Rothwell P.M. Increased cerebral arterial pulsatility in patients with leukoaraiosis: arterial stiffness enhances transmission of aortic pulsatility. Stroke 2012, 43:2631-2636.
69. Nation D.A., Edland S.D., Bondi M.W., Salmon D.P., Delano-Wood L., Peskind E.R., Quinn J.F., Galasko D.R. Pulse pressure is associated with Alzheimer biomarkers in cognitively normal older adults. Neurology 2013, 81:2024-2027.
70. Nation D.A., Delano-Wood L., Bangen K.J., Wierenga C.E., Jak A.J., Hansen L.A., Galasko D.R., Salmon D.P., Bondi M.W. Antemortem pulse pressure elevation predicts cerebrovascular disease in autopsy-confirmed Alzheimer's disease. J. Alzheimers Dis. 2012, 30:595-603.
71. Waldstein S.R., Rice S.C., Thayer J.F., Najjar S.S., Scuteri A., Zonderman A.B. Pulse pressure and pulse wave velocity are related to cognitive decline in the Baltimore Longitudinal Study of Aging. Hypertension 2008, 51:99-104.
72. Mitchell G.F., van Buchem M.A., Sigurdsson S., Gotal J.D., Jonsdottir M.K., Kjartansson O., Garcia M., Aspelund T., Harris T.B., Gudnason V., Launer L.J. Arterial stiffness, pressure and flow pulsatility and brain structure and function: the age, gene/environment susceptibility-Reykjavik study. Brain 2011, 134:3398-3407.
73. Laurent S., Cockcroft J., Van Bortel L., Boutouyrie P., Giannattasio C., Hayoz D., Pannier B., Vlachopoulos C., Wilkinson I., Struijker-Boudier H., European Network for Non-invasive Investigation of Large Expert consensus document on arterial stiffness: methodological issues and clinical applications. Eur. Heart J. 2006, 27:2588-2605.
74. Najjar S.S., Scuteri A., Shetty V., Wright J.G., Muller D.C., Fleg J.L., Spurgeon H.P., Ferrucci L., Lakatta E.G. Pulse wave velocity is an independent predictor of the longitudinal increase in systolic blood pressure and of incident hypertension in the Baltimore Longitudinal Study of Aging. J. Am. Coll. Cardiol. 2008, 51:1377-1383.
75. Pereira T., Maldonado J., Pereira L., Conde J. Aortic stiffness is an independent predictor of stroke in hypertensive patients. Arq. Bras. Cardiol. 2013, 100:437-443.
76. Rosano C., Watson N., Chang Y., Newman A.B., Aizenstein H.J., Du Y., Venkatraman V., Harris T.B., Barinas-Mitchell E., Sutton-Tyrrell K. Aortic pulse wave velocity predicts focal white matter hyperintensities in a biracial cohort of older adults. Hypertension 2013, 61:160-165.
77. Laugesen E., Hoyem P., Stausbol-Gron B., Mikkelsen A., Thrysoe S., Erlandsen M., Christiansen J.S., Knudsen S.T., Hansen K.W., Kim W.Y., Hansen T.K., Poulsen P.L. Carotid-femoral pulse wave velocity is associated with cerebral white matter lesions in type 2 diabetes. Diabetes Care 2013, 36:722-728.
78. Henskens L.H., Kroon A.A., van Oostenbrugge R.J., Gronenschild E.H., Fuss-Lejeune M.M., Hofman P.A., Lodder J., de Leeuw P.W. Increased aortic pulse wave velocity is associated with silent cerebral small-vessel disease in hypertensive patients. Hypertension 2008, 52:1120-1126.
79. Tsao C.W., Seshadri S., Beiser A.S., Westwood A.J., Decarli C., Au R., Himali J.J., Hamburg N.M., Vita J.A., Levy D., Larson M.G., Benjamin E.J., Wolf P.A., Vasan R.S., Mitchell G.F. Relations of arterial stiffness and endothelial function to brain aging in the community. Neurology 2013, 81:984-991.
80. Katulska K., Wykretowicz M., Minczykowski A., Krauze T., Milewska A., Piskorski J., Marciniak R., Stajgis M., Wysocki H., Guzik P., Wykretowicz A. Gray matter volume in relation to cardio-vascular stiffness. J. Neurol. Sci. 2014, 343:100-104.
81. Watson N.L., Sutton-Tyrrell K., Rosano C., Boudreau R.M., Hardy S.E., Simonsick E.M., Najjar S.S., Launer L.J., Yaffe K., Atkinson H.H., Satterfield S., Newman A.B. Arterial stiffness and cognitive decline in well-functioning older adults. J. Gerontol. A Biol. Sci. Med. Sci. 2011, 66:1336-1342.
82. King K.S., Chen K.X., Hulsey K.M., McColl R.W., Weiner M.F., Nakonezny P.A., Peshock R.M. White matter hyperintensities: use of aortic arch pulse wave velocity to predict volume independent of other cardiovascular risk factors. Radiology 2013, 267:709-717.
83. Provenzano F.A., Muraskin J., Tosto G., Muraskin J., Tosto G., Narkhede A., Wasserman B., Griffith E., Guzman V., Meier I., Zimmerman M., Brickman A. White matter hyperintensities and cerebral amyloidosis: necessary and sufficient for clinical expression of Alzheimer disease?. JAMA Neurol. 2013, 70:455-461.
84. Hughes T.M., Craft S., Lopez O.L. Review of 'the potential role of arterial stiffness in the pathogenesis of Alzheimer's disease'. Neurodegenerative Disease Management 2015, 5:121-135.
85. Woodward M., Zhang X., Barzi F., Pan W., Ueshima H., Rodgers A., MacMahon S., Asia Pacific Cohort Studies The effects of diabetes on the risks of major cardiovascular diseases and death in the Asia-Pacific region. Diabetes Care 2003, 26:360-366.
86. Ciulla T.A., Amador A.G., Zinman B. Diabetic retinopathy and diabetic macular edema: pathophysiology, screening, and novel therapies. Diabetes Care 2003, 26:2653-2664.
87. Jha V., Garcia-Garcia G., Iseki K., Li Z., Naicker S., Plattner B., Saran R., Wang A.Y., Yang C.W. Chronic kidney disease: global dimension and perspectives. Lancet 2013, 382:260-272.
88. Crane P.K., Walker R., Hubbard R.A., Li G., Nathan D.M., Zheng H., Haneuse S., Craft S., Montine T.J., Kahn S.E., McCormick W., McCurry S.M., Bowen J.D., Larson E.B. Glucose levels and risk of dementia. N. Engl. J. Med. 2013, 369:540-548.
89. Kerti L., Witte A.V., Winkler A., Grittner U., Rujescu D., Floel A. Higher glucose levels associated with lower memory and reduced hippocampal microstructure. Neurology 2013, 81:1746-1752.
90. Knopman D.S., Jack C.R., Wiste H.J., Lundt E.S., Weigand S.D., Vemuri P., Lowe V.J., Kantarci K., Gunter J.L., Senjem M.L., Mielke M.M., Roberts R.O., Boeve B.F., Petersen R.C. 18F-fluorodeoxyglucose positron emission tomography, aging, and apolipoprotein E genotype in cognitively normal persons. Neurobiol. Aging 2014, 35:2096-2106.
91. Willette A.A., Bendlin B.B., Starks E.J., Birdsill A.C., Johnson S.C., Christian B.T., Okonkwo O.C., La Rue A., Hermann B.P., Koscik R.L., Jonaitis E.M., Sager M.A., Asthana S. Association of insulin resistance with cerebral glucose uptake in late middle-aged adults at risk for Alzheimer disease. JAMA Neurol. 2015, 72:1013-1020.
92. Roberts R.O., Knopman D.S., Cha R.H., Mielke M.M., Pankratz V.S., Boeve B.F., Kantarci K., Geda Y.E., Jack C.R., Petersen R.C., Lowe V.J. Diabetes and elevated hemoglobin A1c levels are associated with brain hypometabolism but not amyloid accumulation. J. Nucl. Med. 2014, 55:759-764.
93. Craft S. Insulin resistance and Alzheimer's disease pathogenesis: potential mechanisms and implications for treatment. Curr. Alzheimer Res. 2007, 4:147-152.
94. Willette A.A., Johnson S.C., Birdsill A.C., Sager M.A., Christian B., Baker L.D., Craft S., Oh J., Statz E., Hermann B.P., Jonaitis E.M., Koscik R.L., La Rue A., Asthana S., Bendlin B.B. Insulin resistance predicts brain amyloid deposition in late middle-aged adults. Alzheimers Dement. 2014.
95. Willette A.A., Xu G., Johnson S.C., Birdsill A.C., Jonaitis E.M., Sager M.A., Hermann B.P., La Rue A., Asthana S., Bendlin B.B. Insulin resistance, brain atrophy, and cognitive performance in late middle-aged adults. Diabetes Care 2013, 36:443-449.
96. Tomita N., Furukawa K., Okamura N., Tashiro M., Une K., Furumoto S., Iwata R., Yanai K., Kudo Y., Arai H. Brain accumulation of amyloid beta protein visualized by positron emission tomography and BF-227 in Alzheimer's disease patients with or without diabetes mellitus. Geriatr. Gerontol. Int. 2013, 13:215-221.
97. Heitner J., Dickson D. Diabetics do not have increased Alzheimer-type pathology compared with age-matched control subjects. A retrospective postmortem immunocytochemical and histofluorescent study. Neurology 1997, 49:1306-1311.
98. Exalto L.G., Quesenberry C.P., Barnes D., Kivipelto M., Biessels G.J., Whitmer R.A. Midlife risk score for the prediction of dementia four decades later. Alzheimers Dement. 2013.
99. van Harten B., Oosterman J., Muslimovic D., van Loon B.J., Scheltens P., Weinstein H.C. Cognitive impairment and MRI correlates in the elderly patients with type 2 diabetes mellitus. Age Ageing 2007, 36:164-170.
100. Ramos-Rodriguez J.J., Jimenez-Palomares M., Murillo-Carretero M.I., Infante-Garcia C., Berrocoso E., Hernandez-Pacho F., Lechuga-Sancho A.M., Cozar-Castellano I., Garcia-Alloza M. Central vascular disease and exacerbated pathology in a mixed model of type 2 diabetes and Alzheimer's disease. Psychoneuroendocrinology 2015, 62:69-79.
101. Zheng C., Liu Z. Vascular function, insulin action, and exercise: an intricate interplay. Trends Endocrinol. Metab. 2015.
102. Westerbacka J., Seppala-Lindroos A., Yki-Jarvinen H. Resistance to acute insulin induced decreases in large artery stiffness accompanies the insulin resistance syndrome. J. Clin. Endocrinol. Metab. 2001, 86:5262-5268.
103. Lacy P.S., O'Brien D.G., Stanley A.G., Dewar M.M., Swales P.P., Williams B. Increased pulse wave velocity is not associated with elevated augmentation index in patients with diabetes. J. Hypertens. 2004, 22:1937-1944.
104. Hughes T.M., Althouse A.D., Niemczyk N.A., Hawkins M.S., Kuipers A.L., Sutton-Tyrrell K. Effects of weight loss and insulin reduction on arterial stiffness in the SAVE trial. Cardiovasc. Diabetol. 2012, 11:114.
105. Stone J., Johnstone D.M., Mitrofanis J., O'Rourke M. The mechanical cause of age-related dementia (Alzheimer's disease): the brain is destroyed by the pulse. J. Alzheimers Dis. 2015, 44:355-373.
106. Muniyappa R., Yavuz S. Metabolic actions of angiotensin II and insulin: a microvascular endothelial balancing act. Mol. Cell. Endocrinol. 2013, 378:59-69.
107. Katusic Z.S., Austin S.A. Endothelial nitric oxide: protector of a healthy mind. Eur. Heart J. 2014, 35:888-894.
108. Manrique C., Lastra G., Sowers J.R. New insights into insulin action and resistance in the vasculature. Ann. N. Y. Acad. Sci. 2014, 1311:138-150.
109. Gage M.C., Yuldasheva N.Y., Viswambharan H., Sukumar P., Cubbon R.M., Galloway S., Imrie H., Skromna A., Smith J., Jackson C.L., Kearney M.T., Wheatcroft S.B. Endothelium-specific insulin resistance leads to accelerated atherosclerosis in areas with disturbed flow patterns: a role for reactive oxygen species. Atherosclerosis 2013, 230:131-139.
110. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev. Neurosci. 2004, 5:347-360.
111. Zlokovic B.V. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat. Rev. Neurosci. 2011, 12:723-738.
112. Rusinek H., Ha J., Yau P.L., Storey P., Tirsi A., Tsui W.H., Frosch O., Azova S., Convit A. Cerebral perfusion in insulin resistance and type 2 diabetes. J. Cereb. Blood Flow Metab. 2015, 35:95-102.
113. Oldendorf W.H. Brain uptake of radiolabeled amino acids, amines, and hexoses after arterial injection. Am. J. Physiol. 1971, 221:1629-1639.
114. McEwen B.S., Reagan L.P. Glucose transporter expression in the central nervous system: relationship to synaptic function. Eur. J. Pharmacol. 2004, 490:13-24.
115. Grillo C.A., Piroli G.G., Hendry R.M., Reagan L.P. Insulin-stimulated translocation of GLUT4 to the plasma membrane in rat hippocampus is PI3-kinase dependent. Brain Res. 2009, 1296:35-45.
116. Piroli G.G., Grillo C.A., Reznikov L.R., Adams S., McEwen B.S., Charron M.J., Reagan L.P. Corticosterone impairs insulin-stimulated translocation of GLUT4 in the rat hippocampus. Neuroendocrinology 2007, 85:71-80.
117. Semba R.D., Nicklett E.J., Ferrucci L. Does accumulation of advanced glycation end products contribute to the aging phenotype?. J. Gerontol. A Biol. Sci. Med. Sci. 2010, 65:963-975.
118. Srikanth V., Maczurek A., Phan T., Steele M., Westcott B., Juskiw D., Munch G. Advanced glycation endproducts and their receptor RAGE in Alzheimer's disease. Neurobiol. Aging 2011, 32:763-777.
119. Basta G., Schmidt A.M., De Caterina R. Advanced glycation end products and vascular inflammation: implications for accelerated atherosclerosis in diabetes. Cardiovasc. Res. 2004, 63:582-592.
120. Mosconi L. Brain glucose metabolism in the early and specific diagnosis of Alzheimer's disease. FDG-PET studies in MCI and AD. Eur. J. Nucl. Med. Mol. Imaging 2005, 32:486-510.
121. Castellano C.A., Nugent S., Paquet N., Tremblay S., Bocti C., Lacombe G., Imbeault H., Turcotte E., Fulop T., Cunnane S.C. Lower brain 18F-fluorodeoxyglucose uptake but normal 11C-acetoacetate metabolism in mild Alzheimer's disease dementia. J. Alzheimers Dis. 2015, 43:1343-1353.
122. Banks W.A., Owen J.B., Erickson M.A. Insulin in the brain: there and back again. Pharmacol. Ther. 2012, 136:82-93.
123. Kondo T., Hafezi-Moghadam A., Thomas K., Wagner D.D., Kahn C.R. Mice lacking insulin or insulin-like growth factor 1 receptors in vascular endothelial cells maintain normal blood-brain barrier. Biochem. Biophys. Res. Commun. 2004, 317:315-320.
124. Kastin A.J., Akerstrom V. Glucose and insulin increase the transport of leptin through the blood-brain barrier in normal mice but not in streptozotocin-diabetic mice. Neuroendocrinology 2001, 73:237-242.
125. Bingham E.M., Hopkins D., Smith D., Pernet A., Hallett W., Reed L., Marsden P.K., Amiel S.A. The role of insulin in human brain glucose metabolism: an 18fluoro-deoxyglucose positron emission tomography study. Diabetes 2002, 51:3384-3390.
126. Cholerton B., Baker L.D., Craft S. Insulin resistance and pathological brain ageing. Diabet. Med. 2011, 28:1463-1475.
127. Reagan L.P., Gorovits N., Hoskin E.K., Alves S.E., Katz E.B., Grillo C.A., Piroli G.G., McEwen B.S., Charron M.J. Localization and regulation of GLUTx1 glucose transporter in the hippocampus of streptozotocin diabetic rats. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:2820-2825.
128. McNay E.C., Ong C.T., McCrimmon R.J., Cresswell J., Bogan J.S., Sherwin R.S. Hippocampal memory processes are modulated by insulin and high-fat-induced insulin resistance. Neurobiol. Learn. Mem. 2010, 93:546-553.
129. Fernandez A.M., Torres-Aleman I. The many faces of insulin-like peptide signalling in the brain. Nat. Rev. Neurosci. 2012, 13:225-239.
130. Nemoto T., Toyoshima-Aoyama F., Yanagita T., Maruta T., Fujita H., Koshida T., Yonaha T., Wada A., Sawaguchi A., Murakami M. New insights concerning insulin synthesis and its secretion in rat hippocampus and cerebral cortex: amyloid-beta1-42-induced reduction of proinsulin level via glycogen synthase kinase-3beta. Cell. Signal. 2014, 26:253-259.
131. Frank H.J., Pardridge W.M., Morris W.L., Rosenfeld R.G., Choi T.B. Binding and internalization of insulin and insulin-like growth factors by isolated brain microvessels. Diabetes 1986, 35:654-661.
132. Woods S.C., Porte D. Relationship between plasma and cerebrospinal fluid insulin levels of dogs. Am. J. Physiol. 1977, 233:E331-E334.
133. Greco A.V., Ghirlanda G., Fedeli G., Gambassi G. Insulin in the cerebro spinal fluid of man. Eur. Neurol. 1970, 3:303-307.
134. Gupta G., Azam M., Baquer N.Z. Modulation of rat brain insulin receptor kinase activity in diabetes. Neurochem. Int. 1992, 20:487-492.
135. Bose M., Olivan B., Laferrere B. Stress and obesity: the role of the hypothalamic-pituitary-adrenal axis in metabolic disease. Curr. Opin. Endocrinol. Diabetes Obes. 2009, 16:340-346.
136. Debons A.F., Krimsky I., From A. A direct action of insulin on the hypothalamic satiety center. Am. J. Physiol. 1970, 219:938-943.
137. Ho L., Qin W., Pompl P.N., Xiang Z., Wang J., Zhao Z., Peng Y., Cambareri G., Rocher A., Mobbs C.V., Hof P.R., Pasinetti G.M. Diet-induced insulin resistance promotes amyloidosis in a transgenic mouse model of Alzheimer's disease. FASEB J. 2004, 18:902-904.
138. Hanson A.J., Bayer-Carter J.L., Green P.S., Montine T.J., Wilkinson C.W., Baker L.D., Watson G.S., Bonner L.M., Callaghan M., Leverenz J.B., Tsai E., Postupna N., Zhang J., Lampe J., Craft S. Effect of apolipoprotein E genotype and diet on apolipoprotein E lipidation and amyloid peptides: randomized clinical trial. JAMA Neurol. 2013, 70:972-980.
139. Qiu W.Q., Walsh D.M., Ye Z., Vekrellis K., Zhang J., Podlisny M.B., Rosner M.R., Safavi A., Hersh L.B., Selkoe D.J. Insulin-degrading enzyme regulates extracellular levels of amyloid beta-protein by degradation. J. Biol. Chem. 1998, 273:32730-32738.
140. Xie L., Helmerhorst E., Taddei K., Plewright B., Van Bronswijk W., Martins R. Alzheimer's beta-amyloid peptides compete for insulin binding to the insulin receptor. J. Neurosci. 2002, 22:RC221.
141. Tamaki C., Ohtsuki S., Terasaki T. Insulin facilitates the hepatic clearance of plasma amyloid beta-peptide (1 40) by intracellular translocation of low-density lipoprotein receptor-related protein 1 (LRP-1) to the plasma membrane in hepatocytes. Mol. Pharmacol. 2007, 72:850-855.
142. Deane R., Sagare A., Zlokovic B.V. The role of the cell surface LRP and soluble LRP in blood-brain barrier Abeta clearance in Alzheimer's disease. Curr. Pharm. Des. 2008, 14:1601-1605.
143. Fuentealba R.A., Liu Q., Kanekiyo T., Zhang J., Bu G. Low density lipoprotein receptor-related protein 1 promotes anti-apoptotic signaling in neurons by activating Akt survival pathway. J. Biol. Chem. 2009, 284:34045-34053.
144. Reger M.A., Watson G.S., Green P.S., Wilkinson C.W., Baker L.D., Cholerton B., Fishel M.A., Plymate S.R., Breitner J.C., DeGroodt W., Mehta P., Craft S. Intranasal insulin improves cognition and modulates beta-amyloid in early AD. Neurology 2008, 70:440-448.
145. Craft S., Baker L.D., Montine T.J., Minoshima S., Watson G.S., Claxton A., Arbuckle M., Callaghan M., Tsai E., Plymate S.R., Green P.S., Leverenz J., Cross D., Gerton B. Intranasal insulin therapy for Alzheimer disease and amnestic mild cognitive impairment: a pilot clinical trial. Arch. Neurol. 2012, 69:29-38.
146. Claxton A., Baker L.D., Hanson A., Trittschuh E.H., Cholerton B., Morgan A., Callaghan M., Arbuckle M., Behl C., Craft S. Long-acting intranasal insulin detemir improves cognition for adults with mild cognitive impairment or early-stage Alzheimer's disease dementia. J. Alzheimers Dis. 2015, 44:897-906.
147. Liu Y., Tang G., Li Y., Wang Y., Chen X., Gu X., Zhang Z., Wang Y., Yang G.Y. Metformin attenuates blood-brain barrier disruption in mice following middle cerebral artery occlusion. J. Neuroinflammation 2014, 11:177.
148. Picone P., Nuzzo D., Caruana L., Messina E., Barera A., Vasto S., Di Carlo M. Metformin increases APP expression and processing via oxidative stress, mitochondrial dysfunction and NF-kappaB activation: use of insulin to attenuate metformin's effect. Biochim. Biophys. Acta 2015, 1853:1046-1059.
149. Risner M.E., Saunders A.M., Altman J.F., Ormandy G.C., Craft S., Foley I.M., Zvartau-Hind M.E., Hosford D.A., Roses A.D., Rosiglitazone in Alzheimer's disease Study Efficacy of rosiglitazone in a genetically defined population with mild-to-moderate Alzheimer's disease. Pharmacogenomics J. 2006, 6:246-254.
150. Watson G.S., Cholerton B.A., Reger M.A., Baker L.D., Plymate S.R., Asthana S., Fishel M.A., Kulstad J.J., Green P.S., Cook D.G., Kahn S.E., Keeling M.L., Craft S. Preserved cognition in patients with early Alzheimer disease and amnestic mild cognitive impairment during treatment with rosiglitazone: a preliminary study. Am. J. Geriatr. Psychiatr. 2005, 13:950-958.
151. de la Monte S.M. Relationships between diabetes and cognitive impairment. Endocrinol. Metab. Clin. N. Am. 2014, 43:245-267.