Suppression of glymphatic fluid transport in a mouse model of Alzheimer's disease

Neurobiology of Disease

Volumn 93, Issue , 2016, Pages 215-225

  Peng, Weiguo ^a   Achariyar, Thiyagarajan M ^a   Li, Baoman ^a,c   Liao, Yonghong ^a,d   Mestre, Humberto ^a   Hitomi, Emi ^a   Regan, Sean ^a   Kasper, Tristan ^a   Peng, Sisi ^a   Ding, Fengfei ^a   Benveniste, Helene ^b   Nedergaard, Maiken ^a   Deane, Rashid ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c CHINA MEDICAL UNIVERSITY   (China)

^d THE AFFILIATED HOSPITAL OF SOUTHWEST MEDICAL UNIVERSITY   (China)

Author keywords

Alzheimer's disease; Amyloid ; AQP4; Astrocytes; Brain ISF clearance; Clearance; Convective ISF flow; CSF; Glymphatic pathways; Lymphatic system

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; BIOLOGICAL MARKER; OLIGOMER; AMYLOID BETA PROTEIN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CEREBROSPINAL FLUID; CONTROLLED STUDY; DISEASE COURSE; FEMALE; FLUID TRANSPORT; GLYMPHATIC FLUID TRANSPORT; INTERSTITIAL FLUID; MALE; MOUSE; NERVE CELL; NONHUMAN; OLIGOMERIZATION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; VASCULAR AMYLOIDOSIS; AMYLOID PLAQUE; ANIMAL; BRAIN; C57BL MOUSE; DISEASE EXACERBATION; DISEASE MODEL; METABOLISM; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BIOLOGICAL TRANSPORT; BRAIN; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; MICE, INBRED C57BL; NEURONS; PLAQUE, AMYLOID;

EID: 84973643437     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2016.05.015     Document Type: Article

References (76)

1. Abbott N.J., et al. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 2006, 7:41-53.
2. Banks W.A., et al. Efflux of human and mouse amyloid beta proteins 1-40 and 1-42 from brain: impairment in a mouse model of Alzheimer's disease. Neuroscience 2003, 121:487-492.
3. Bateman R.J., et al. Human amyloid-beta synthesis and clearance rates as measured in cerebrospinal fluid in vivo. Nat. Med. 2006, 12:856-861.
4. Bell R.D., et al. Transport pathways for clearance of human Alzheimer's amyloid beta-peptide and apolipoproteins E and J in the mouse central nervous system. J. Cereb. Blood Flow Metab. 2007, 27:909-918.
5. Blennow K. Cerebrospinal fluid protein biomarkers for Alzheimer's disease. NeuroRx 2004, 1:213-225.
6. Boulton M., et al. Drainage of CSF through lymphatic pathways and arachnoid villi in sheep: measurement of 125I-albumin clearance. Neuropathol. Appl. Neurobiol. 1996, 22:325-333.
7. Bradbury M.W. The blood-brain barrier. Transport across the cerebral endothelium. Circ. Res. 1985, 57:213-222.
8. Bradbury M.W., Westrop R.J. Factors influencing exit of substances from cerebrospinal fluid into deep cervical lymph of the rabbit. J. Physiol. 1983, 339:519-534.
9. Brinker T., et al. Dynamic properties of lymphatic pathways for the absorption of cerebrospinal fluid. Acta Neuropathol. 1997, 94:493-498.
10. Bruggink K.A., et al. Amyloid-beta oligomer detection by ELISA in cerebrospinal fluid and brain tissue. Anal. Biochem. 2013, 433:112-120.
11. Cirrito J.R., et al. P-glycoprotein deficiency at the blood-brain barrier increases amyloid-beta deposition in an Alzheimer disease mouse model. J. Clin. Invest. 2005, 115:3285-3290.
12. Cirrito J.R., et al. Synaptic activity regulates interstitial fluid amyloid-beta levels in vivo. Neuron 2005, 48:913-922.
13. Clifford P.M., et al. Alpha7 nicotinic acetylcholine receptor expression by vascular smooth muscle cells facilitates the deposition of Abeta peptides and promotes cerebrovascular amyloid angiopathy. Brain Res. 2008, 1234:158-171.
14. Deane R., et al. Clearance of amyloid-beta peptide across the blood-brain barrier: implication for therapies in Alzheimer's disease. CNS Neurol. Disord. Drug Targets 2009, 8:16-30.
15. Deane R., et al. RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat. Med. 2003, 9:907-913.
16. Deane R., et al. apoE isoform-specific disruption of amyloid beta peptide clearance from mouse brain. J. Clin. Invest. 2008, 118:4002-4013.
17. Deane R., et al. IgG-assisted age-dependent clearance of Alzheimer's amyloid beta peptide by the blood-brain barrier neonatal Fc receptor. J. Neurosci. 2005, 25:11495-11503.
18. Deane R., et al. A multimodal RAGE-specific inhibitor reduces amyloid beta-mediated brain disorder in a mouse model of Alzheimer disease. J. Clin. Invest. 2012, 122:1377-1392.
19. Deane R., et al. Sleep deprivation disrupts apoE isoform specific radial diffusion from the penetrating arteries into brain by the glymphatic system. Implications for CAA and Alzheimer's Disease Neuroscience 2015, Vol. 461. Chicago, 2015.
20. Deane R., et al. LRP/amyloid beta-peptide interaction mediates differential brain efflux of Abeta isoforms. Neuron 2004, 43:333-344.
21. Fagan A.M., Holtzman D.M. Cerebrospinal fluid biomarkers of Alzheimer's disease. Biomark. Med 2010, 4:51-63.
22. Fagan A.M., et al. Inverse relation between in vivo amyloid imaging load and cerebrospinal fluid Abeta42 in humans. Ann. Neurol. 2006, 59:512-519.
23. Fagan A.M., et al. Longitudinal change in CSF biomarkers in autosomal-dominant Alzheimer's disease. Sci. Transl. Med. 2014, 6.
24. Haj-Yasein N.N., et al. Glial-conditional deletion of aquaporin-4 (Aqp4) reduces blood-brain water uptake and confers barrier function on perivascular astrocyte endfeet. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:17815-17820.
25. Hawkes C.A., et al. Perivascular drainage of solutes is impaired in the ageing mouse brain and in the presence of cerebral amyloid angiopathy. Acta Neuropathol. 2011, 121:431-443.
26. Herrup K. The case for rejecting the amyloid cascade hypothesis. Nat. Neurosci. 2015, 18:794-799.
27. Herz J. Apolipoprotein E receptors in the nervous system. Curr. Opin. Lipidol. 2009, 20:190-196.
28. Holtzman D.M., et al. Apolipoprotein E and apolipoprotein E receptors: normal biology and roles in Alzheimer disease. Cold Spring Harb. Perspect. Med. 2012, 2:a006312.
29. Iliff J.J., et al. Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury. J. Neurosci. 2014, 34:16180-16193.
30. Iliff J.J., et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci. Transl. Med. 2012, 4.
31. Jaeger L.B., et al. Testing the neurovascular hypothesis of Alzheimer's disease: LRP-1 antisense reduces blood-brain barrier clearance, increases brain levels of amyloid-beta protein, and impairs cognition. J. Alzheimers Dis. 2009, 17:553-570.
32. Johanson C.E., et al. Multiplicity of cerebrospinal fluid functions: new challenges in health and disease. Cerebrospinal Fluid Res. 2008, 5:10.
33. Kanekiyo T., Bu G. The low-density lipoprotein receptor-related protein 1 and amyloid-beta clearance in Alzheimer's disease. Front. Aging Neurosci. 2014, 6:93.
34. Kanekiyo T., et al. Neuronal clearance of amyloid-beta by endocytic receptor LRP1. J. Neurosci. 2013, 33:19276-19283.
35. Kanekiyo T., et al. LRP1 in brain vascular smooth muscle cells mediates local clearance of Alzheimer's amyloid-beta. J. Neurosci. 2012, 32:16458-16465.
36. Kayed R., et al. Conformation dependent monoclonal antibodies distinguish different replicating strains or conformers of prefibrillar Abeta oligomers. Mol. Neurodegener. 2010, 5:57.
37. Kayed R., et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 2003, 300:486-489.
38. Kida S., et al. CSF drains directly from the subarachnoid space into nasal lymphatics in the rat. Anatomy, histology and immunological significance. Neuropathol. Appl. Neurobiol. 1993, 19:480-488.
39. Kress B.T., et al. Impairment of paravascular clearance pathways in the aging brain. Ann. Neurol. 2014.
40. Kumar-Singh S. Cerebral amyloid angiopathy: pathogenetic mechanisms and link to dense amyloid plaques. Genes Brain Behav. 2008, 7(Suppl. 1):67-82.
41. Lue L.F., et al. Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol. 1999, 155:853-862.
42. Mathiisen T.M., et al. The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction. Glia 2010, 58:1094-1103.
43. Mawuenyega K.G., et al. Decreased clearance of CNS beta-amyloid in Alzheimer's disease. Science 2010, 330:1774.
44. McLean C.A., et al. Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neurol. 1999, 46:860-866.
45. Michel C.C. Capillary permeability and how it may change. J. Physiol. 1988, 404:1-29.
46. Musiek E.S., Holtzman D.M. Three dimensions of the amyloid hypothesis: time, space and 'wingmen'. Nat. Neurosci. 2015, 18:800-806.
47. Nedergaard M. Neuroscience. Garbage truck of the brain. Science 2013, 340:1529-1530.
48. Niwa K., et al. A beta-peptides enhance vasoconstriction in cerebral circulation. Am. J. Physiol. Heart Circ. Physiol. 2001, 281:H2417-H2424.
49. Oe T., et al. Quantitative analysis of amyloid beta peptides in cerebrospinal fluid of Alzheimer's disease patients by immunoaffinity purification and stable isotope dilution liquid chromatography/negative electrospray ionization tandem mass spectrometry. Rapid Commun. Mass Spectrom. 2006, 20:3723-3735.
50. Paris D., et al. Soluble beta-amyloid peptides mediate vasoactivity via activation of a pro-inflammatory pathway. Neurobiol. Aging 2000, 21:183-197.
51. Plog B.A., et al. Biomarkers of traumatic injury are transported from brain to blood via the glymphatic system. J. Neurosci. 2015, 35:518-526.
52. Pollay M. The function and structure of the cerebrospinal fluid outflow system. Cerebrospinal Fluid Res. 2010, 7:9.
53. Rangroo Thrane V., et al. Paravascular microcirculation facilitates rapid lipid transport and astrocyte signaling in the brain. Sci. Rep. 2013, 3:2582.
54. Rangroo Thrane V., et al. Ammonia triggers neuronal disinhibition and seizures by impairing astrocyte potassium buffering. Nat. Med. 2013, 19:1643-1648.
55. Rennels M.L., et al. Evidence for a 'paravascular' fluid circulation in the mammalian central nervous system, provided by the rapid distribution of tracer protein throughout the brain from the subarachnoid space. Brain Res. 1985, 326:47-63.
56. Rolyan H., et al. Amyloid-beta protein modulates the perivascular clearance of neuronal apolipoprotein E in mouse models of Alzheimer's disease. J. Neural Transm. 2011, 118:699-712.
57. Schoonenboom N.S., et al. Amyloid beta 38, 40, and 42 species in cerebrospinal fluid: more of the same?. Ann. Neurol. 2005, 58:139-142.
58. Selkoe D.J. Clearing the brain's amyloid cobwebs. Neuron 2001, 32:177-180.
59. Shibata M., et al. Clearance of Alzheimer's amyloid-ss(1-40) peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier. J. Clin. Invest. 2000, 106:1489-1499.
60. Singh I., et al. Low levels of copper disrupt brain amyloid-beta homeostasis by altering its production and clearance. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:14771-14776.
61. Suo Z., et al. Soluble Alzheimers beta-amyloid constricts the cerebral vasculature in vivo. Neurosci. Lett. 1998, 257:77-80.
62. Thal D.R., et al. Occurrence and co-localization of amyloid beta-protein and apolipoprotein E in perivascular drainage channels of wild-type and APP-transgenic mice. Neurobiol. Aging 2007, 28:1221-1230.
63. Van Dorpe J., et al. Prominent cerebral amyloid angiopathy in transgenic mice overexpressing the London mutant of human APP in neurons. Am. J. Pathol. 2000, 157:1283-1298.
64. Walsh D.M., et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002, 416:535-539.
65. Wang M., et al. Cognitive deficits and delayed neuronal loss in a mouse model of multiple microinfarcts. J. Neurosci. 2012, 32:17948-17960.
66. Weller R.O., et al. Pathways of fluid drainage from the brain-morphological aspects and immunological significance in rat and man. Brain Pathol. 1992, 2:277-284.
67. Xie L., et al. Sleep drives metabolite clearance from the adult brain. Science 2013, 342:373-377.
68. Xu Z., et al. Deletion of aquaporin-4 in APP/PS1 mice exacerbates brain Abeta accumulation and memory deficits. Mol. Neurodegener. 2015, 10:58.
69. Yamada S., et al. Albumin outflow into deep cervical lymph from different regions of rabbit brain. Am. J. Phys. 1991, 261:H1197-H1204.
70. Yang J., et al. Loss of astrocyte polarization in the tg-ArcSwe mouse model of Alzheimer's disease. J. Alzheimers Dis. 2011, 27:711-722.
71. Yang L., et al. Evaluating glymphatic pathway function utilizing clinically relevant intrathecal infusion of CSF tracer. J. Transl. Med. 2013, 11:107.
72. Yang W., et al. Aquaporin-4 mediates astrocyte response to beta-amyloid. Mol. Cell. Neurosci. 2012, 49:406-414.
73. Zetterberg H., et al. Intra-individual stability of CSF biomarkers for Alzheimer's disease over two years. J. Alzheimers Dis. 2007, 12:255-260.
74. Zhu X., et al. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 2008, 135:145-157.
75. Zlokovic B.V. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008, 57:178-201.
76. Zlokovic B.V. New therapeutic targets in the neurovascular pathway in Alzheimer's disease. Neurotherapeutics 2008, 5:409-414.