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PMID: 22302811 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Contrast-enhanced magnetic resonance microangiography reveals remodeling of the cerebral microvasculature in transgenic ArcAβ mice.

Klohs J, Baltes C, Princz-Kranz F, Ratering D, Nitsch RM, Knuesel I, Rudin M

Abstract

Amyloid-β (Aβ) deposition in the cerebral vasculature is accompanied by remodeling which has a profound influence on vascular integrity and function. In the current study we have quantitatively assessed the age-dependent changes of the cortical vasculature in the arcAβ model of cerebral amyloidosis. To estimate the density of the cortical microvasculature in vivo, we used contrast-enhanced magnetic resonance microangiography (CE-μMRA). Three-dimensional gradient echo datasets with 60 μm isotropic resolution were acquired in 4- and 24-month-old arcAβ mice and compared with wild-type (wt) control mice of the same age before and after administration of superparamagnetic iron oxide nanoparticles. After segmentation of the cortical vasculature from difference images, an automated algorithm was applied for assessing the number and size distribution of intracortical vessels. With CE-μMRA, cerebral arteries and veins with a diameter of less than the nominal pixel resolution (60 μm) can be visualized. A significant age-dependent reduction in the number of functional intracortical microvessels (radii of 20-80 μm) has been observed in 24-month-old arcAβ mice compared with age-matched wt mice, whereas there was no difference between transgenic and wt mice of 4 months of age. Immunohistochemistry demonstrated strong fibrinogen and Aβ deposition in small- and medium-sized vessels, but not in large cerebral arteries, of 24-month-old arcAβ mice. The reduced density of transcortical vessels may thus be attributed to impaired perfusion and vascular occlusion caused by deposition of Aβ and fibrin. The study demonstrated that remodeling of the cerebrovasculature can be monitored noninvasively with CE-μMRA in mice.

MeSH Terms
Amyloid beta-Peptides/genetics,metabolism Animals Cerebral Amyloid Angiopathy/genetics,metabolism,physiopathology Cerebrovascular Circulation/genetics Contrast Media Cytoskeletal Proteins/genetics,metabolism Female Fibrinogen/genetics,metabolism Humans Magnetic Resonance Angiography/methods Male Mice Mice, Transgenic Microvessels/diagnostic imaging,physiology Nerve Tissue Proteins/genetics,metabolism Radiography
Chemicals
Amyloid beta-Peptides Contrast Media Cytoskeletal Proteins Nerve Tissue Proteins activity regulated cytoskeletal-associated protein Fibrinogen
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Klohs Jan
Institute for Biomedical Engineering, Swiss Federal Institute of Technology and University of Zurich, CH-8093 Zurich, Switzerland.
Baltes Christof
Princz-Kranz Felicitas
Ratering David
Nitsch Roger M
Knuesel Irene
Rudin Markus
References (47)
47 references, click to expand
  1. Perivascular drainage of amyloid-beta peptides from the brain and its failure in cerebral amyloid angiopathy and Alzheimer's disease.
    Brain Pathol. 2008 Apr;18(2):253-66 PMID: 18363936
  2. MR contrast due to intravascular magnetic susceptibility perturbations.
    Magn Reson Med. 1995 Oct;34(4):555-66 PMID: 8524024
  3. Vascular response to acetazolamide decreases as a function of age in the arcA beta mouse model of cerebral amyloidosis.
    Neurobiol Dis. 2010 Oct;40(1):284-92 PMID: 20600914
  4. Cerebral amyloid angiopathy and cortical microinfarcts as putative substrates of vascular dementia.
    Int J Geriatr Psychiatry. 2006 Jul;21(7):681-7 PMID: 16802283
  5. Capillary cerebral amyloid angiopathy is associated with vessel occlusion and cerebral blood flow disturbances.
    Neurobiol Aging. 2009 Dec;30(12):1936-48 PMID: 18359131
  6. Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields.
    Magn Reson Med. 1990 Apr;14(1):68-78 PMID: 2161986
  7. Congophilic angiopathy in the pathogenesis of Alzheimer's degeneration.
    Ann Pathol. 1981;1(2):120-9 PMID: 6169353
  8. Accurate assessment of carotid artery stenosis in atherosclerotic mice using accelerated high-resolution 3D magnetic resonance angiography.
    MAGMA. 2011 Feb;24(1):9-18 PMID: 20862514
  9. Magnetic resonance angiography of the rat cerebrovascular system without the use of contrast agents.
    NMR Biomed. 1999 Jun;12(4):189-96 PMID: 10421910
  10. Detection of vascular alterations by in vivo magnetic resonance angiography and histology in APP/PS1 mouse model of Alzheimer's disease.
    MAGMA. 2010 Feb;23(1):53-64 PMID: 20066469
  11. Transcranial pulsed Doppler measurements of blood velocity in the middle cerebral artery: reference values at rest and during hyperventilation in healthy volunteers in relation to age and sex.
    Ultrasound Med Biol. 1989;15(1):1-8 PMID: 2646803
  12. Altered angioarchitecture in selected areas of brains with Alzheimer's disease.
    Acta Neuropathol. 1990;79(6):672-9 PMID: 2360411
  13. Cerebral microvascular amyloid beta protein deposition induces vascular degeneration and neuroinflammation in transgenic mice expressing human vasculotropic mutant amyloid beta precursor protein.
    Am J Pathol. 2005 Aug;167(2):505-15 PMID: 16049335
  14. Magnetic resonance imaging of atherosclerotic vascular disease.
    Am J Hypertens. 1993 Nov;6(11 Pt 2):335S-339S PMID: 8297541
  15. Hemodynamic consequences of deformed microvessels in the brain in Alzheimer's disease.
    Ann N Y Acad Sci. 1997 Sep 26;826:75-91 PMID: 9329682
  16. Developmental and amyloid plaque-related changes in cerebral cortical capillaries in transgenic Tg2576 Alzheimer mice.
    Int J Dev Neurosci. 2006 Apr-May;24(2-3):187-93 PMID: 16423498
  17. A leaky blood-brain barrier, fibrinogen infiltration and microglial reactivity in inflamed Alzheimer's disease brain.
    J Cell Mol Med. 2009 Sep;13(9A):2911-25 PMID: 18657226
  18. Alzheimer's dementia begins as a disease of small blood vessels, damaged by oxidative-induced inflammation and dysregulated amyloid metabolism: implications for early detection and therapy.
    FASEB J. 2011 Jan;25(1):5-13 PMID: 21205781
  19. Micro MRI of the mouse brain using a novel 400 MHz cryogenic quadrature RF probe.
    NMR Biomed. 2009 Oct;22(8):834-42 PMID: 19536757
  20. Pharmacokinetics of superparamagnetic iron-oxide MR contrast agents in the rat.
    Invest Radiol. 1990 Jul;25(7):771-7 PMID: 2391194
  21. Intravascular contrast agent improves magnetic resonance angiography of carotid arteries in minipigs.
    J Magn Reson Imaging. 1997 Nov-Dec;7(6):963-71 PMID: 9400838
  22. Neuronal overexpression of mutant amyloid precursor protein results in prominent deposition of cerebrovascular amyloid.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):14088-93 PMID: 10570203
  23. Vessel size imaging.
    Magn Reson Med. 2001 Mar;45(3):397-408 PMID: 11241696
  24. The role of von Willebrand factor in thrombus formation.
    Thromb Res. 2007;120 Suppl 1:S5-9 PMID: 17493665
  25. Pathological alterations of the cerebral microvasculature in Alzheimer's disease and related dementing disorders.
    Acta Neuropathol. 1994;87(5):469-80 PMID: 8059599
  26. Stereologic analysis of microvascular morphology in the elderly: Alzheimer disease pathology and cognitive status.
    J Neuropathol Exp Neurol. 2006 Mar;65(3):235-44 PMID: 16651885
  27. Microvasculature changes and cerebral amyloid angiopathy in Alzheimer's disease and their potential impact on therapy.
    Acta Neuropathol. 2009 Jul;118(1):87-102 PMID: 19234858
  28. Detection of cerebral microbleeds with quantitative susceptibility mapping in the ArcAbeta mouse model of cerebral amyloidosis.
    J Cereb Blood Flow Metab. 2011 Dec;31(12):2282-92 PMID: 21847134
  29. Age-dependent cerebrovascular abnormalities and blood flow disturbances in APP23 mice modeling Alzheimer's disease.
    J Neurosci. 2003 Sep 17;23(24):8453-9 PMID: 13679413
  30. Small vessels in the human brain: MR venography with deoxyhemoglobin as an intrinsic contrast agent.
    Radiology. 1997 Jul;204(1):272-7 PMID: 9205259
  31. Cerebral microvascular alterations in aging, leukoaraiosis, and Alzheimer's disease.
    Ann N Y Acad Sci. 1997 Sep 26;826:103-16 PMID: 9329684
  32. Detection of neuritic plaques in Alzheimer's disease by magnetic resonance microscopy.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):14079-84 PMID: 10570201
  33. Physiologic alterations in cranial blood flow demonstrated by magnetic resonance angiography.
    Invest Radiol. 1992 Mar;27(3):240-4 PMID: 1551776
  34. Correlations between cognitive impairment, middle cerebral artery flow velocity and cortical glucose metabolism in the early phase of Alzheimer's disease.
    Dementia. 1995 Jan-Feb;6(1):32-8 PMID: 7728217
  35. In vivo micro-MRI of intracortical neurovasculature.
    Neuroimage. 2006 Aug 1;32(1):62-9 PMID: 16675271
  36. 2D and 3D high resolution gradient echo functional imaging of the brain: venous contributions to signal in motor cortex studies.
    NMR Biomed. 1994 Mar;7(1-2):54-62 PMID: 8068526
  37. Intracellular Abeta and cognitive deficits precede beta-amyloid deposition in transgenic arcAbeta mice.
    Neurobiol Aging. 2007 Sep;28(9):1297-306 PMID: 16876915
  38. Cerebral beta amyloid angiopathy is a risk factor for cerebral ischemic infarction. A case control study in human brain biopsies.
    J Neuropathol Exp Neurol. 2000 Sep;59(9):768-73 PMID: 11005257
  39. Cerebral amyloid angiopathy: incidence and complications in the aging brain. I. Cerebral hemorrhage.
    Stroke. 1983 Nov-Dec;14(6):915-23 PMID: 6658995
  40. Stereological analysis of microvascular parameters in a double transgenic model of Alzheimer's disease.
    Brain Res Bull. 2005 Apr 30;65(4):317-22 PMID: 15811597
  41. Vascular β-amyloid and early astrocyte alterations impair cerebrovascular function and cerebral metabolism in transgenic arcAβ mice.
    Acta Neuropathol. 2011 Sep;122(3):293-311 PMID: 21688176
  42. Abeta is targeted to the vasculature in a mouse model of hereditary cerebral hemorrhage with amyloidosis.
    Nat Neurosci. 2004 Sep;7(9):954-60 PMID: 15311281
  43. Fibrinogen and beta-amyloid association alters thrombosis and fibrinolysis: a possible contributing factor to Alzheimer's disease.
    Neuron. 2010 Jun 10;66(5):695-709 PMID: 20547128
  44. Magnetic resonance angiography and vascular corrosion casting as tools in biomedical research: application to transgenic mice modeling Alzheimer's disease.
    Neurol Res. 2004 Jul;26(5):507-16 PMID: 15265268
  45. Magnetic resonance imaging of blood vessels at high fields: in vivo and in vitro measurements and image simulation.
    Magn Reson Med. 1990 Oct;16(1):9-18 PMID: 2255240
  46. Quantitative studies of the autofluorescence derived from neuronal lipofuscin.
    J Microsc. 1981 Sep;123(Pt 3):249-58 PMID: 7299812
  47. Fibrin deposition accelerates neurovascular damage and neuroinflammation in mouse models of Alzheimer's disease.
    J Exp Med. 2007 Aug 6;204(8):1999-2008 PMID: 17664291
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2012-02-01
Pages
1705-13
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6703349
Subset
IM
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