Pharmacologically-induced neurovascular uncoupling is associated with cognitive impairment in mice

Journal of Cerebral Blood Flow and Metabolism

Volumn 35, Issue 11, 2015, Pages 1871-1881

  Tarantini, Stefano ^a,b   Hertelendy, Peter ^a,c   Tucsek, Zsuzsanna ^a   Valcarcel Ares, M Noa ^a   Smith, Nataliya ^d   Menyhart, Akos ^c   Farkas, Eszter ^c   Hodges, Erik L ^a   Towner, Rheal ^d   Deak, Ferenc ^a,b   Sonntag, William E ^a,e   Csiszar, Anna ^a,b,e,f   Ungvari, Zoltan ^a,b,e,f   Toth, Peter ^a,f  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF SZEGED   (Hungary)

^d OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^e UNIVERSITY OF OKLAHOMA   (United States)

^f UNIVERSITY OF PÉCS   (Hungary)

Author keywords

behavior (rodent); cerebral hemodynamics; EET; HETE; microcirculation; neurovascular coupling; nitric oxide

Indexed keywords

INDOMETACIN; N (METHYLSULFONYL) 2 (2 PROPYNYLOXY) BENZENEHEXANAMIDE; N(G) NITROARGININE METHYL ESTER; OXYGENASE INHIBITOR; UNCLASSIFIED DRUG; VASODILATOR AGENT; ARACHIDONATE EPOXYGENASE; CYTOCHROME P450; ENZYME INHIBITOR; NEURONAL NITRIC OXIDE SYNTHASE; PROSTAGLANDIN SYNTHASE INHIBITOR;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE; BRAIN BLOOD FLOW; BRAIN PERFUSION; COGNITIVE DEFECT; CONTROLLED STUDY; DRUG MECHANISM; FEEDBACK SYSTEM; GAIT; LEARNING; MALE; MEMORY; MEMORY TEST; MOTOR COORDINATION; MOUSE; NEUROVASCULAR UNCOUPLING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RECOGNITION; SENSORIMOTOR FUNCTION; SPATIAL MEMORY; SYNAPTIC POTENTIAL; WORKING MEMORY; ANIMAL; ANTAGONISTS AND INHIBITORS; BODY EQUILIBRIUM; BRAIN CIRCULATION; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECTS; HAND STRENGTH; MAZE TEST; NEUROVASCULAR COUPLING; PSYCHOLOGY; SOMATOSENSORY EVOKED POTENTIAL;

ANIMALS; BLOOD PRESSURE; CEREBROVASCULAR CIRCULATION; COGNITION DISORDERS; CYCLOOXYGENASE INHIBITORS; CYTOCHROME P-450 ENZYME SYSTEM; ENZYME INHIBITORS; EVOKED POTENTIALS, SOMATOSENSORY; GAIT; HAND STRENGTH; INDOMETHACIN; MALE; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; NEUROVASCULAR COUPLING; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE TYPE I; POSTURAL BALANCE; RECOGNITION (PSYCHOLOGY);

EID: 84946076950     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2015.162     Document Type: Article

References (43)

1. Zlokovic BV. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat Rev Neurosci 2011; 12: 723-738.
2. Attwell D, Buchan AM, Charpak S, Lauritzen M, Macvicar BA, Newman EA. Glial and neuronal control of brain blood flow. Nature 2010; 468: 232-243.
3. Ma J, Ayata C, Huang PL, Fishman MC, Moskowitz MA. Regional cerebral blood flow response to vibrissal stimulation in mice lacking type I NOS gene expression. Am J Physiol 1996; 270: H1085-H1090.
4. Chen BR, Kozberg MG, Bouchard MB, Shaik MA, Hillman EM. A critical role for the vascular endothelium in functional neurovascular coupling in the brain. J Am Heart Assoc 2014; 3: e000787.
5. Stobart JL, Lu L, Anderson HD, Mori H, Anderson CM. Astrocyte-induced cortical vasodilation is mediated by D-serine and endothelial nitric oxide synthase. Proc Natl Acad Sci USA 2013; 110: 3149-3154.
6. Peng X, Carhuapoma JR, Bhardwaj A, Alkayed NJ, Falck JR, Harder DR, et al. Suppression of cortical functional hyperemia to vibrissal stimulation in the rat by epoxygenase inhibitors. Am J Physiol Heart Circ Physiol 2002; 283: H2029-H2037.
7. Takano T, Tian GF, Peng W, Lou N, Libionka W, Han X, et al. Astrocyte-mediated control of cerebral blood flow. Nat Neurosci 2006; 9: 260-267.
8. Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann KA, Pozzan T, et al. Neuron-To-Astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 2003; 6: 43-50.
9. Stefanova I, Stephan T, Becker-Bense S, Dera T, Brandt T, Dieterich M. Age-related changes of blood-oxygen-level-dependent signal dynamics during optokinetic stimulation. Neurobiol Aging 2013; 34: 2277-2286.
10. Topcuoglu MA, Aydin H, Saka E. Occipital cortex activation studied with simultaneous recordings of functional transcranial Doppler ultrasound (fTCD) and visual evoked potential (VEP) in cognitively normal human subjects: effect of healthy aging. Neurosci Lett 2009; 452: 17-22.
11. Toth P, Tarantini S, Tucsek Z, Ashpole NM, Sosnowska D, Gautam T, et al. Resveratrol treatment rescues neurovascular coupling in aged mice: role of improved cerebromicrovascular endothelial function and downregulation of NADPH oxidase. Am J Physiol Heart Circ Physiol 2014; 306: H299-H308.
12. Kazama K, Anrather J, Zhou P, Girouard H, Frys K, Milner TA, et al. Angiotensin II impairs neurovascular coupling in neocortex through NADPH oxidase-derived radicals. Circ Res 2004; 95: 1019-1026.
13. Tucsek Z, Toth P, Sosnowska D, Gautam T, Mitschelen M, Koller A, et al. Obesity in aging exacerbates blood-brain barrier disruption, neuroinflammation, and oxidative stress in the mouse hippocampus: effects on expression of genes involved in beta-Amyloid generation and Alzheimer's disease. J Gerontol A Biol Sci Med Sci 2013; 69: 1212-1226.
14. Girouard H, Iadecola C. Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol 2006; 100: 328-335.
15. Heinzel S, Liepelt-Scarfone I, Roeben B, Nasi-Kordhishti I, Suenkel U, Wurster I, et al. A neurodegenerative vascular burden index and the impact on cognition. Front Aging Neurosci 2014; 6: 161.
16. Brand-Schieber E, Falck JF, Schwartzman M. Selective inhibition of arachidonic acid epoxidation in vivo. J Physiol Pharmacol 2000; 51: 655-672.
17. Wakisaka Y, Chu Y, Miller JD, Rosenberg GA, Heistad DD. Spontaneous intracerebral hemorrhage during acute and chronic hypertension in mice. J Cereb Blood Flow Metab 2010; 30: 56-69.
18. Toth P, Tucsek Z, Sosnowska D, Gautam T, Mitschelen M, Tarantini S, et al. Agerelated autoregulatory dysfunction and cerebromicrovascular injury in mice with angiotensin II-induced hypertension. J Cereb Blood Flow Metab 2013; 33: 1732-1742.
19. Antunes M, Biala G. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process 2012; 13: 93-110.
20. MacLaren DA, Santini JA, Russell AL, Markovic T, Clark SD. Deficits in motor performance after pedunculopontine lesions in rats-impairment depends on demands of task. Eur J Neurosci 2014; 40: 3224-3236.
21. Bouet V, Boulouard M, Toutain J, Divoux D, Bernaudin M, Schumann-Bard P, et al. The adhesive removal test: a sensitive method to assess sensorimotor deficits in mice. Nat Protoc 2009; 4: 1560-1564.
22. Hamers FP, Koopmans GC, Joosten EA. CatWalk-Assisted gait analysis in the assessment of spinal cord injury. J Neurotrauma 2006; 23: 537-548.
23. Toth P, Tarantini S, Tucsek Z, Ashpole NM, Sosnowska D, Gautam T, et al. Resveratrol treatment rescues neurovascular coupling in aged mice: role of improved cerebromicrovascular endothelial function and down-regulation of NADPH oxidase. Am J Physiol Heart Circ Physiol 2014; 306: H299-H308.
24. Lind BL, Brazhe AR, Jessen SB, Tan FC, Lauritzen MJ. Rapid stimulus-evoked astrocyte Ca2+ elevations and hemodynamic responses in mouse somatosensory cortex in vivo. Proc Natl Acad Sci USA 2013; 110: E4678-E4687.
25. Nehlig A, Wittendorp-Rechenmann E, Lam CD. Selective uptake of [14C]2-deoxyglucose by neurons and astrocytes: high-resolution microautoradiographic imaging by cellular 14C-Trajectography combined with immunohistochemistry. J Cereb Blood Flow Metab 2004; 24: 1004-1014.
26. Frayling C, Britton R, Dale N. ATP-mediated glucosensing by hypothalamic tanycytes. J Physiol 2011; 589: 2275-2286.
27. Leithner C, Muller S, Fuchtemeier M, Lindauer U, Dirnagl U, Royl G. Determination of the brain-blood partition coefficient for water in mice using MRI. J Cereb Blood Flow Metab 2010; 30: 1821-1824.
28. Garteiser P, Doblas S, Watanabe Y, Saunders D, Hoyle J, Lerner M, et al. Multiparametric assessment of the anti-glioma properties of OKN007 by magnetic resonance imaging. J Magn Reson Imaging 2010; 31: 796-806.
29. Herscovitch P, Raichle ME. What is the correct value for the brain-blood partition coefficient for water? J Cereb Blood Flow Metab 1985; 5: 65-69.
30. Oka H, Shimono K, Ogawa R, Sugihara H, Taketani M. A new planar multielectrode array for extracellular recording: application to hippocampal acute slice. J Neurosci Methods 1999; 93: 61-67.
31. Park L, Anrather J, Girouard H, Zhou P, Iadecola C. Nox2-derived reactive oxygen species mediate neurovascular dysregulation in the aging mouse brain. J Cereb Blood Flow Metab 2007; 27: 1908-1918.
32. Keisker B, Hepp-Reymond MC, Blickenstorfer A, Kollias SS. Differential representation of dynamic and static power grip force in the sensorimotor network. Eur J Neurosci 2010; 31: 1483-1491.
33. Stenholm S, Sallinen J, Koster A, Rantanen T, Sainio P, Heliövaara M, et al. Association between obesity history and hand grip strength in older adults-exploring the roles of inflammation and insulin resistance as mediating factors. J Gerontol A Biol Sci Med Sci 2011; 66: 341-348.
34. Petzold GC, Albeanu DF, Sato TF, Murthy VN. Coupling of neural activity to blood flow in olfactory glomeruli is mediated by astrocytic pathways. Neuron 2008; 58: 897-910.
35. Sorond FA, Kiely DK, Galica A, Moscufo N, Serrador JM, Iloputaife I, et al. Neurovascular coupling is impaired in slow walkers: the MOBILIZE Boston Study. Ann Neurol 2011; 70: 213-220.
36. Gorelick PB, Scuteri A, Black SE, Decarli C, Greenberg SM, Iadecola C, et al. 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.
37. Leithner C, Royl G, Offenhauser N, Füchtemeier M, Kohl-Bareis M, Villringer A, et al. Pharmacological uncoupling of activation induced increases in CBF and CMRO2. J Cereb Blood Flow Metab 2010; 30: 311-322.
38. Bruhn H, Fransson P, Frahm J. Modulation of cerebral blood oxygenation by indomethacin: MRI at rest and functional brain activation. J Magn Reson Imaging 2001; 13: 325-334.
39. Mitschelen M, Garteiser P, Carnes BA, Farley JA, Doblas S, Demoe JH, et al. Basal and hypercapnia-Altered cerebrovascular perfusion predict mild cognitive impairment in aging rodents. Neuroscience 2009; 164: 918-928.
40. Miralbell J, Lopez-Cancio E, Lopez-Oloriz J, Arenillas JF, Barrios M, Soriano-Raya JJ, et al. Cognitive patterns in relation to biomarkers of cerebrovascular disease and vascular risk factors. Cerebrovasc Dis 2013; 36: 98-105.
41. Witte AV, Kerti L, Margulies DS, Floel A. Effects of resveratrol on memory performance, hippocampal functional connectivity, and glucose metabolism in healthy older adults. J Neurosci 2014; 34: 7862-7870.
42. Szabo K, Rosengarten B, Juhasz T, Lako E, Csiba L, Olah L. Effect of non-steroid anti-inflammatory drugs on neurovascular coupling in humans. J Neurol Sci 2014; 336: 227-231.
43. Waldstein SR, Wendell CR, Seliger SL, Ferrucci L, Metter EJ, Zonderman AB. Nonsteroidal anti-inflammatory drugs, aspirin, and cognitive function in the Baltimore longitudinal study of aging. J Am Geriatr Soc 2010; 58: 38-43.