Hyperlipidemia disrupts cerebrovascular reflexes and worsens ischemic perfusion defect

Journal of Cerebral Blood Flow and Metabolism

Volumn 33, Issue 6, 2013, Pages 954-962

  Ayata, Cenk ^a   Shin, Hwa Kyoung ^a,b   Dileköz, Ergin ^a,c   Atochin, Dmitriy N ^a   Kashiwagi, Satoshi ^a   Eikermann Haerter, Katharina ^a   Huang, Paul L ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b Pusan National University   (South Korea)

^c GAZI UNIVERSITY FACULTY OF MEDICINE   (Turkey)

Author keywords

Apolipoprotein E knockout mice; Autoregulation; Hypercapnia; Hypercholesterolemia; Middle cerebral artery occlusion; Neurovascular coupling

Indexed keywords

APOLIPOPROTEIN E; ENDOTHELIAL NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATTENUATION; BLOOD PRESSURE; BRAIN ATHEROSCLEROSIS; BRAIN BLOOD FLOW; BRAIN INFARCTION; BRAIN ISCHEMIA; BRAIN PERFUSION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HISTOPATHOLOGY; HYPERCAPNIA; HYPEREMIA; HYPERLIPIDEMIA; LIPID DIET; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; STENOSIS; VASOMOTOR REFLEX; WILD TYPE;

ANIMALS; APOLIPOPROTEINS E; BRAIN; BRAIN ISCHEMIA; CEREBROVASCULAR CIRCULATION; DIET, HIGH-FAT; HYPERLIPIDEMIAS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION;

EID: 84878563998     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2013.38     Document Type: Article

References (38)

1. Amarenco P. Hypercholesterolemia, lipid-lowering agents, and the risk for brain infarction. Neurology 2001; 57: S35-S44.
2. Demchuk AM, Hess DC, Brass LM, Yatsu FM. Is cholesterol a risk factor for stroke?: Yes. Arch Neurol 1999; 56: 1518-1520.
3. d'Uscio LV, Smith LA, Katusic ZS. Hypercholesterolemia impairs endotheliumdependent relaxations in common carotid arteries of apolipoprotein e-deficient mice. Stroke 2001; 32: 2658-2664.
4. d'Uscio LV, Baker TA, Mantilla CB, Smith L, Weiler D, Sieck GC et al. Mechanism of endothelial dysfunction in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2001; 21: 1017-1022.
5. Kitayama J, Faraci FM, Lentz SR, Heistad DD. Cerebral vascular dysfunction during hypercholesterolemia. Stroke 2007; 38: 2136-2141.
6. Bonthu S, Heistad DD, Chappell DA, Lamping KG, Faraci FM. Atherosclerosis, vascular remodeling, and impairment of endothelium-dependent relaxation in genetically altered hyperlipidemic mice. Arterioscler Thromb Vasc Biol 1997; 17: 2333-2340.
7. Rossitch Jr. E, Alexander 3rd E, Black PM, Cooke JP. L-arginine normalizes endothelial function in cerebral vessels from hypercholesterolemic rabbits. J Clin Invest 1991; 87: 1295-1299.
8. Ishikawa M, Stokes KY, Zhang JH, Nanda A, Granger DN. Cerebral microvascular responses to hypercholesterolemia: roles of NADPH oxidase and P-selectin. Circ Res 2004; 94: 239-244.
9. Galle J, Mameghani A, Bolz SS, Gambaryan S, Gorg M, Quaschning T et al. Oxidized LDL and its compound lysophosphatidylcholine potentiate AngII-induced vasoconstriction by stimulation of RhoA. J Am Soc Nephrol 2003; 14: 1471-1479.
10. Zhang SH, Reddick RL, Piedrahita JA, Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 1992; 258: 468-471.
11. Reddick RL, Zhang SH, Maeda N. Atherosclerosis in mice lacking apo E. Evaluation of lesional development and progression. Arterioscler Thromb 1994; 14: 141-147.
12. Nakashima Y, Plump AS, Raines EW, Breslow JL, Ross R. ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb 1994; 14: 133-140.
13. Fujii M, Hara H, Meng W, Vonsattel JP, Huang Z, Moskowitz MA. Strain-related differences in susceptibility to transient forebrain ischemia in SV-129 and C57black/6 mice. Stroke 1997; 28: 1805-1810.
14. Ayata C, Dunn AK, Gursoy OY, Huang Z, Boas DA, Moskowitz MA. Laser speckle flowmetry for the study of cerebrovascular physiology in normal and ischemic mouse cortex. J Cereb Blood Flow Metab 2004; 24: 744-755.
15. Shin HK, Jones PB, Garcia-Alloza M, Borrelli L, Greenberg SM, Bacskai BJ et al. Age-dependent cerebrovascular dysfunction in a transgenic mouse model of cerebral amyloid angiopathy. Brain 2007; 130: 2310-2319.
16. Eikermann-Haerter K, Hyun Lee J, Yuzawa I, Liu CH, Zhou Z, Kyoung Shin H et al. Migraine mutations increase stroke vulnerability by facilitating ischemic depolarizations. Circulation 2012; 125: 335-345.
17. Buttini M, Orth M, Bellosta S, Akeefe H, Pitas RE, Wyss-Coray T et al. Expression of human apolipoprotein E3 or E4 in the brains of Apoe-/- mice: isoform-specific effects on neurodegeneration. J Neurosci 1999; 19: 4867-4880.
18. McCalden TA, Nath RG, Coleman L, Meyer JS. Hypercholesterolemia and the baboon cerebral circulation. Life Sci 1987; 41: 447-451.
19. Lanza E, Dionigi R, Subissi A, Piccinini F. Effects of experimental atherosclerosis on cerebral blood flow in rabbits. Reversal by sorbinicate. Artery 1982; 11: 64-73.
20. Bart RD, Sheng H, Laskowitz DT, Pearlstein RD, Warner DS. Regional CBF in apolipoprotein E-deficient and wild type mice during focal cerebral ischemia. Neuroreport 1998; 9: 2615-2620.
21. Heistad DD, Marcus ML, Piegors DJ, Armstrong ML. Regulation of cerebral blood flow in atherosclerotic monkeys. Am J Physiol 1980; 239: H539-H544.
22. Rubba P, Faccenda F, Di Somma S, Gnasso A, Scarpato N, Iannuzzi A et al. Cerebral blood flow velocity and systemic vascular resistance after acute reduction of low-density lipoprotein in familial hypercholesterolemia. Stroke 1993; 24: 1154-1161.
23. Bakker SL, de Leeuw FE, Koudstaal PJ, Hofman A, Breteler MM. Cerebral CO2 reactivity, cholesterol, and high-density lipoprotein cholesterol in the elderly. Neurology 2000; 54: 987-989.
24. Pfefferkorn TK, Knuppel HP, Jaeger BR, Thiery J, Hamann GF. Increased cerebral CO(2) reactivity after heparin-mediated extracorporal LDL precipitation (HELP) in patients with coronary heart disease and hyperlipidemia. Stroke 1999; 30: 1802-1806.
25. van Laar PJ, van der Graaf Y, Mali WP, van der Grond J, Hendrikse J. Effect of cerebrovascular risk factors on regional cerebral blood flow. Radiology 2008; 246: 198-204.
26. Rodriguez G, Bertolini S, Nobili F, Arrigo A, Masturzo P, Elicio N et al. Regional cerebral blood flow in familial hypercholesterolemia. Stroke 1994; 25: 831-836.
27. Laskowitz DT, Sheng H, Bart RD, Joyner KA, Roses AD, Warner DS. Apolipoprotein E-deficient mice have increased susceptibility to focal cerebral ischemia. J Cereb Blood Flow Metab 1997; 17: 753-758.
28. Mogi M, Iwai M, Chen R, Iwanami J, Ide A, Tsukuda K et al. Amlodipine treatment reduces stroke size in apolipoprotein E-deficient mice. Am J Hypertens 2006; 19: 1144-1149.
29. Hatcher JP, Virley D, Hadingham SJ, Roberts J, Hunter AJ, Parsons AA. The behavioural effect of middle cerebral artery occlusion on apolipoprotein-E deficient mice. Behav Brain Res 2002; 131: 139-149.
30. Kim E, Tolhurst AT, Qin LY, Chen XY, Febbraio M, Cho S. CD36/fatty acid translocase, an inflammatory mediator, is involved in hyperlipidemia-induced exacerbation in ischemic brain injury. J Neurosci 2008; 28: 4661-4670.
31. Horsburgh K, Kelly S, McCulloch J, Higgins GA, Roses AD, Nicoll JA. Increased neuronal damage in apolipoprotein E-deficient mice following global ischaemia. Neuroreport 1999; 10: 837-841.
32. Sheng H, Laskowitz DT, Mackensen GB, Kudo M, Pearlstein RD, Warner DS. Apolipoprotein E deficiency worsens outcome from global cerebral ischemia in the mouse. Stroke 1999; 30: 1118-1124.
33. Plump AS, Smith JD, Hayek T, Aalto-Setala K, Walsh A, Verstuyft JG et al. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 1992; 71: 343-353.
34. Postiglione A, Nappi A, Brunetti A, Soricelli A, Rubba P, Gnasso A et al. Relative protection from cerebral atherosclerosis of young patients with homozygous familial hypercholesterolemia. Atherosclerosis 1991; 90: 23-30.
35. Puchowicz MA, Zechel JL, Valerio J, Emancipator DS, Xu K, Pundik S et al. Neuroprotection in diet-induced ketotic rat brain after focal ischemia. J Cereb Blood Flow Metab 2008; 28: 1907-1916.
36. Yamashiro K, Milsom AB, Duchene J, Panayiotou C, Urabe T, Hattori N et al. Alterations in nitric oxide and endothelin-1 bioactivity underlie cerebrovascular dysfunction in ApoE-deficient mice. J Cereb Blood Flow Metab 2010; 30: 1494-1503.
37. Atochin DN, Wang A, Liu VW, Critchlow JD, Dantas AP, Looft-Wilson R et al. The phosphorylation state of eNOS modulates vascular reactivity and outcome of cerebral ischemia in vivo. J Clin Invest 2007; 117: 1961-1967.
38. Shin HK, Salomone S, Potts EM, Lee SW, Millican E, Noma K et al. Rho-kinase inhibition acutely augments blood flow in focal cerebral ischemia via endothelial mechanisms. J Cereb Blood Flow Metab 2007; 27: 998-1009.