Endothelial nitric oxide: Protector of a healthy mind

European Heart Journal

Volumn 35, Issue 14, 2014, Pages 888-894

  Katusic, Zvonimir S ^a   Austin, Susan A ^a  

^a MAYO CLINIC   (United States)

Author keywords

Alzheimer's disease; Amyloid precursor protein; BACE1; Cognitive impairment; Endothelium; Exercise; Hippocampus; Microglia; Mitochondria; Neuronal progenitors; Nitric oxide; Vascular dementia

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BETA SECRETASE 1; ENDOTHELIAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; APLP1 PROTEIN, HUMAN;

ALZHEIMER DISEASE; COGNITION; HUMAN; MICROGLIA; MITOCHONDRION; NERVE CELL PLASTICITY; NEURAL STEM CELL; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN SECRETION; REVIEW; VASCULAR ENDOTHELIUM; ANIMAL; BIOSYNTHESIS; BRAIN; BRAIN CIRCULATION; METABOLISM; MICROVASCULATURE; MOUSE; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; VASCULARIZATION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; CEREBROVASCULAR CIRCULATION; ENDOTHELIUM, VASCULAR; HUMANS; MICE; MICROGLIA; MICROVESSELS; NEURONAL PLASTICITY; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; OXIDATIVE STRESS;

EID: 84898849858     PISSN: 0195668X     EISSN: 15229645     Source Type: Journal    
DOI: 10.1093/eurheartj/eht544     Document Type: Review

References (50)

1. Muqtadar H, Testai FD, Gorelick PB. The dementia of cardiac disease. Curr Cardiol Rep 2012;14:732-740.
2. Atochin DN, Huang PL. Endothelialnitric oxide synthase transgenic modelsofendo-thelial dysfunction. Pflugers Arch 2010;460:965-974.
3. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, Technau-Ihling K, Leiher AM, Dimmeler S.Essential roleof endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 2003;9:1370-1376.
4. Guo S, Kim WJ, Lok J, Lee SR, Besancon E, Luo BH, Stins MF, Wang X, Dedhar S, Lo EH. Neuroprotection via matric-trophic coupling between cerebral endothelial cells and neurons. Proc Natl Acad Sci USA 2008;105:7582-7587.
5. Rubanyi GM, Vanhoutte PM. Superoxide anions and hyperoxia inactivate endothelium-derived relaxing factor. Am J Physiol 1986;250:H822-H827.
6. Katusic ZS. Superoxide anion and endothelial regulation of arterial tone. Free Radic Biol Med 1996;20:443-448.
7. Beckman JS. Understanding peroxynitrite biochemistry and its potential for treating human diseases. Arch Biochem Biophys 2009;484:114-116.
8. Katusic ZS, d'Uscio LV, Nath KA. Vascular protection by tetrahydrobiopterin: progress and therapeutic prospects. Trends Pharmacol Sci 2009;30:48-54.
9. Niwa K, Carlson GA, Iadecola C. Exogenous A beta1-40 reproduces cerebrovascu-lar alterations resulting from amyloid precursor protein overexpression in mice. J Cereb Blood Flow Metab 2000;20:1659-1668.
10. Iadecola C, Zhang F, Niew K, Eckman C, Turner SK, Fischer E, Younkin S, Borchelt DR, Hsiao KK, Carlson GA. SOD1 rescues cerebral endothelial dysfunction in mice overexpressing amyloid precursor protein. Nat Neurosci 1999;2: 157-161.
11. Selkoe DJ. The molecular pathology of Alzheimer's disease. Neuron 1991;6: 487-498.
12. Hardy JA, Higgins GA. Alzheimer's disease: the amyloid cascade hypothesis. Science; 256:184-185.
13. Iadecola C. Neurovascular regulationin the normal brain and inAlzheimer's disease. Nat Rev Neurosci 2004;5:347-360.
14. Iadecola C, Park L, Capone C. Threatsto the mind: aging, amyloid, and hypertension. Stroke 2009;40:S40-S44.
15. Park L, Zhou P, Pitstick R, Capone C, Anrather J, Norris EH, Younkin L, Younkin S, Carlson G, McEwen BS, Iadecola C. Nox2-derived radicals contribute to neurovas-cular and behavioral dysfunction in mice overexpressing the amyloid precursor protein. Proc Natl Acad Sci USA 2008;105:1347-1352.
16. Park L, Zhou J, Zhou P, Pistick R, El Jamal S, Younkin L, Pierce J, Arreguin A, Anrather J, Younkin SG, Carlson GA, McEwen BS, Iadecola C. Innate immunity receptor CD36 promotes cerebral amyloid angiopathy. Proc Natl Acad Sci USA 2013;110: 3089-3094.
17. Park L, Zhou P, Koizumi K, El Jamal S, Previti ML, van Nostrand WE, Carlson G, Iadecola C. Brain and circulating levels of Ab1-40 differentially contribute to vaso-motor dysfunction in the mouse brain. Stroke 2013;44:198-204.
18. d'Uscio LV, Das P, Santhanam AV, He T, Younkin SG, Katusic ZS. Activation of PPARd prevents endothelial dysfunction induced by overexpression of amyloid-b precursor protein. Cardiovasc Res 2012;96:504-512.
19. Nicolakakis N, Hamel E. Neurovascular function in Alzheimer's disease patients and experimental models. J Cereb Blood Flow Metab 2011;31:1354-1370.
20. Weller RO, Preston SD, Subash M, Carare RO. Cerebral amyloid angiopathy in the aetiology and immunotherapy of Alzheimer disease. Alzheimers Res Ther 2009;1: 6-18.
21. Weller RO, Subash M, Preston SD, Mazanti I, Carare RO. Perivascular drainage of amyloid-b peptides from the brain and its failure in cerebral amyloid angiopathy and Alzheimer's disease. Brain Pathol 2008;18:253-266.
22. Jung SM, Jandu S, Steppan J, Belkin A, An SS, Pak A, Choi EY, Nyhan D, Butlin M, Viegas K, Avolio A, Berkowitz DE, Santhanam L. Increased tissue transglutaminase activity contributes to central vascular stiffness in eNOS knockout mice. Am J Physiol Heart Circ Physiol 2013;305:H803-H810.
23. Sagare AP, Bell RD, Zlokovic BV. Neurovascular dysfunction and faulty amyloid b-peptide clearance in Alzheimer disease. Cold Spring Harb Perspect Med 2012;2: 1-18.
24. Jeynes B, Provias J. Significant negative correlations between capillary expressed eNOS and Alzheimer lesion burden. Neurosci Lett 2009;463:244-248.
25. Haul S, Godecke A, Schrader J, Haas HL, Luhmann HJ. Impairment of neocortical long-term potentiation in mice deficient of endothelial nitric oxide synthase. J Neurophysiol 1999;81:494-497.
26. Doreulee N, Sergeeva OA, Yanovsky Y, Chepkova AN, Selbach O, Godecke A, Schrader J, Haas HL. Cortico-striatal synaptic plasticity in endothelial nitric oxide synthase deficient mice. Brain Res 2003;964:159-163.
27. Hyman BT, Van Hoesen GW, Damasio AR, Barnes CL. Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science 1984;225: 1168-1170.
28. Hopper RA, Garthwaite J. Tonic and phasic nitric oxide signals in hippocampal long-term potentiation. J Neurosci 2006;26:11513-11521.
29. Bon CLM, Garthwaite J. On the role of nitric oxide in hippocampal long-term po-tentiation. J Neurosci 2003;23:1941-1948.
30. Blackshaw S, Eliasson MJ, Sawa A, Watkins CC, Krug D, Gupta A, Arai T, Ferrante RJ, Snyder SH. Species, strain and developmental variations in hippocampal neuronal and endothelial nitric oxide synthase clarify discrepancies in nitric oxide-dependent synaptic plasticity. Neuroscience 2003;119:979-990.
31. Seidel B, Stanarius A, Wolf G. Differential expression of neuronal and endothelial nitric oxide synthase in blood vessels of the rat brain. Neurosci Lett 1997;239: 109-112.
32. Stanarius A, Topel I, Schulz S, Noack H, Wolf G. Immunocytochemistry of endothe-lial nitric oxide synthaseinthe rat brain:alight and electron microscopical study using the tyramide signal amplification technique. Acta Histochem 1997;99:411-429.
33. Pawlik G, Rackl A, Bing RJ. Quantitative capillary topography and blood flow in the cerebral cortex of cats: an in vivo microscopic study. Brain Res 1981;208:35-58.
34. Launer LJ, Masaki K, Petrovitch H, Foley D, Havlik RJ. The association betweenmidlife blood pressure levels and late-life cognitive function. The Honolulu-Asia Aging Study. JAMA 1995;274:1846-1851.
35. Faraco G, Iadecola C. Hypertension: a harbinger of stroke and dementia. Hypertension 2013. [Epub ahead of print].
36. Atochin DN, Demchenko IT, Astern J, Boso AE, Piantadosi CA, Huang PL. Contributions of endothelial and neuronal nitric oxide synthases to cerebrovascular responses to hyperoxia. J Cereb Blood Flow Metab 2003;23:1219-1226.
37. Huang PL. Mouse models of nitric oxide synthase deficiency. J Am Soc Nephrol 2000; 11:S120-S123.
38. Austin SA, Santhanam AV, Katusic ZS. Endothelial nitric oxide modulates expression and processing of amyloid precursor protein. Circ Res 2010;107:1498-1502.
39. Austin SA, d'Uscio LV, Katusic ZS. Supplementation of nitric oxide attenuates AbPP and BACE1 protein in cerebral microcirculation of eNOS-deficient mice. J Alzheimers Dis 2013;33:29-33.
40. Austin SA, Santhanam AV, Hinton DJ, Choi DS, Katusic ZS. Endothelial nitric oxide deficiency promotes Alzheimer's disease pathology. J Neurochem 2013. [Epub ahead of print].
41. Aguzzi A, Barres BA, Bennett ML. Microglia: scapegoat, saboteur, orsomething else? Science 2013;339:156-161.
42. Gandy S, Heppner FL. Microgliaas dynamic and essential components ofthe amyloid hypothesis. Neuron 2013;78:575-577.
43. Nisoli E, Clementi E, Paolucci C, Cozzi V, Tonello C, Sciorati C, Bracale R, Valerio A, Francolini M, Moncada S, Carruba MO. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 2003;299:896-899.
44. Nisoli E, Falcone S, Tonello C, Cozzi V, Palomba L, Fiorani M, Pisconti A, Brunelli S, Cardile A, Francolini M, Cantoni O, Carruba MO, Moncada S, Clementi E.Mitochon-drial biogenesis by NO yields functionally active mitochondria inmammals. Proc Natl Acad Sci USA 2004;101:16507-16512.
45. Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, Moncada S, Carruba MO. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 2005;310: 314-317.
46. Huang PL. eNOS, metabolic syndrome and cardiovascular disease. Trends Endocrinol Metab 2009;20:295-302.
47. Hall CN, Attwell D. Assessing the physiological concentration and targets of nitric oxide in brain tissue. J Physiol 2008;586:3597-3615.
48. Chen J, Zacharek A, Zhang C, Jiang H, Li Y, Roberts C, Lu M, Kapke A, Chopp M. Endothelial nitric oxide synthase regulates brain-derived neurotrophic factor expression and neurogenesis after stroke in mice. J Neurosci 2005;25:2366-2375.
49. Nagahara AH, Merrill DA, Coppola G, Tsukada S, Schroeder BE, Shaked GM, Wang L, Blesch A, Kim A, Conner JM, Rockenstein E, Chao MV, Koo EH, Geschwind D, Masliah E, Chiba AA, Tuszynski MH. Neuroprotective effectsofbrain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease. Nat Med 2009;15:331-337.
50. De Strooper B, Vassar R, Golde T. The secretases: enzymes with therapeutic potential in Alzheimer disease. Nat Rev Neurol. 2010;6:99-107.