Regulation of cerebrospinal fluid (CSF) flow in neurodegenerative, neurovascular and neuroinflammatory disease

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1862, Issue 3, 2016, Pages 442-451

  Simon, Matthew J ^a,b   Iliff, Jeffrey J ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Cerebral ischemia; CSF; Diurnal variation; Glymphatic; Multiple sclerosis

Indexed keywords

EID: 84957844086     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2015.10.014     Document Type: Review

References (129)

1. Lehtinen M.K., Zappaterra M.W., Chen X., Yang Y.J., Hill A.D., Lun M., Maynard T., Gonzalez D., Kim S., Ye P., D'Ercole A.J., Wong E.T., LaMantia A.S., Walsh C.A. The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron 2011, 69:893-905.
2. Brinker T., Stopa E., Morrison J., Klinge P. A new look at cerebrospinal fluid circulation. Fluids Barriers CNS 2014, 11:10.
3. Hladky S.B., Barrand M.A. Mechanisms of fluid movement into, through and out of the brain: evaluation of the evidence. Fluids Barriers CNS 2014, 11:26.
4. Davson H. Physiology of the Cerebrospinal Fluid 1967, Churchill, London.
5. Iliff J.J., Chen M.J., Plog B.A., Zeppenfeld D.M., Soltero M., Yang L., Singh I., Deane R., Nedergaard M. Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury. J. Neurosci. 2014, 34:16180-16193.
6. Kress B.T., Iliff J.J., Xia M., Wang M., Wei H.S., Zeppenfeld D., Xie L., Kang H., Xu Q., Liew J.A., Plog B.A., Ding F., Deane R., Nedergaard M. Impairment of paravascular clearance pathways in the aging brain. Ann. Neurol. 2014, 76:845-861.
7. Iliff J.J., Wang M., Liao Y., Plogg B.A., Peng W., Gundersen G.A., Benveniste H., Vates G.E., Deane R., Goldman S.A., Nagelhus E.A., Nedergaard M. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Transl Med 2012, 4. 147ra111.
8. Engelhardt B., Ransohoff R.M. Capture, crawl, cross: the T cell code to breach the blood-brain barriers. Trends Immunol. 2012, 33:579-589.
9. Gaberel T., Gakuba C., Goulay R., Martinez De Lizarrondo S., Hanouz J.L., Emery E., Touze E., Vivien D., Gauberti M. Impaired glymphatic perfusion after strokes revealed by contrast-enhanced MRI: a new target for fibrinolysis?. Stroke 2014, 45:3092-3096.
10. Siler D.A., Gonzalez J.A., Wang R.K., Cetas J.S., Alkayed N.J. Intracisternal administration of tissue plasminogen activator improves cerebrospinal fluid flow and cortical perfusion after subarachnoid hemorrhage in mice. Transl. Stroke Res. 2014, 5:227-237.
11. Oi S. Classification of hydrocephalus: critical analysis of classification categories and advantages of "multi-categorical hydrocephalus classification" (Mc HC). Childs Nerv. Syst. 2011, 27:1523-1533.
12. Sheldon C.A., Kwon Y.J., Liu G.T., McCormack S.E. An integrated mechanism of pediatric pseudotumor cerebri syndrome: evidence of bioenergetic and hormonal regulation of cerebrospinal fluid dynamics. Pediatr. Res. 2015, 77:282-289.
13. Meyers S.P., Khademian Z.P., Chuang S.H., Pollack I.F., Korones D.N., Zimmerman R.A. Choroid plexus carcinomas in children: MRI features and patient outcomes. Neuroradiology 2004, 46:770-780.
14. Wolburg H., Paulus W. Choroid plexus: biology and pathology. Acta Neuropathol. 2010, 119:75-88.
15. Damkier H.H., Brown P.D., Praetorius J. Cerebrospinal fluid secretion by the choroid plexus. Physiol. Rev. 2013, 93:1847-1892.
16. Johanson C.E., Duncan J.A., Klinge P.M., Brinker T., Stopa E.G., Silverberg G.D. Multiplicity of cerebrospinal fluid functions: new challenges in health and disease. Cerebrospinal Fluid Res. 2008, 5:10.
17. Davson H., Segal M.B. Physiology of the CSF and Blood-Brain Barriers 1996, CRC Press, Boca Raton.
18. Dandy W.E. Extirpation of the choroid plexus of the lateral ventricles in communicating hydrocephalus. Ann. Surg. 1918, 68:569-579.
19. Pollay M., Curl F. Secretion of cerebrospinal fluid by the ventricular ependyma of the rabbit. Am. J. Physiol. 1967, 213:1031-1038.
20. Abbott N.J. Evidence for bulk flow of brain interstitial fluid: significance for physiology and pathology. Neurochem. Int. 2004, 45:545-552.
21. Cserr H.F. Role of secretion and bulk flow of brain interstitial fluid in brain volume regulation. Ann. N. Y. Acad. Sci. 1988, 529:9-20.
22. de R., Ames A., Nesbett F.B., Hofmann H.F. Fluid formed by choroid plexus; a technique for its collection and a comparison of its electrolyte composition with serum and cisternal fluids. J Neurophysiol 1960, 23:485-495.
23. Wolburg H., Wolburg-Buchholz K., Liebner S., Engelhardt B. Claudin-1, claudin-and claudin-11 are present in tight junctions of choroid plexus epithelium of the mouse. Neurosci. Lett. 2001, 307:77-80.
24. Millar I.D., Brown P.D. NBCe2 exhibits a 3 HCO3(-):1 Na+ stoichiometry in mouse choroid plexus epithelial cells. Biochem. Biophys. Res. Commun. 2008, 373:550-554.
25. Nielsen S., Smith B.L., Christensen E.I., Agre P. Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:7275-7279.
26. Kao L., Kurtz L.M., Shao X., Papadopoulos M.C., Liu L., Bok D., Nusinowitz S., Chen B., Stella S.L., Andre M., Weinreb J., Luong S.S., Piri N., Kwong J.M., Newman D., Kurtz I. Severe neurologic impairment in mice with targeted disruption of the electrogenic sodium bicarbonate cotransporter NBCe2 (Slc4a5 gene). J. Biol. Chem. 2011, 286:32563-32574.
27. Spector R. Micronutrient homeostasis in mammalian brain and cerebrospinal fluid. J. Neurochem. 1989, 53:1667-1674.
28. Spector R., Johanson C. Micronutrient and urate transport in choroid plexus and kidney: implications for drug therapy. Pharm. Res. 2006, 23:2515-2524.
29. Zhao R., Min S.H., Wang Y., Campanella E., Low P.S., Goldman I.D. A role for the proton-coupled folate transporter (PCFT-SLC46A1) in folate receptor-mediated endocytosis. J. Biol. Chem. 2009, 284:4267-4274.
30. Akanuma S., Sakurai T., Tachikawa M., Kubo Y., Hosoya K. Transporter-mediated L-glutamate elimination from cerebrospinal fluid: possible involvement of excitatory amino acid transporters expressed in ependymal cells and choroid plexus epithelial cells. Fluids Barriers CNS 2015, 12:11.
31. Oshio K., Watanabe H., Song Y., Verkman A.S., Manley G.T. Reduced cerebrospinal fluid production and intracranial pressure in mice lacking choroid plexus water channel Aquaporin-1. FASEB J. 2005, 19:76-78.
32. Dreha-Kulaczewski S., Joseph A.A., Merboldt K.D., Ludwig H.C., Gartner J., Frahm J. Inspiration is the major regulator of human CSF flow. J. Neurosci. 2015, 35:2485-2491.
33. Aspelund A., Antila S., Proulx S.T., Karlsen T.V., Karaman S., Detmar M., Wiig H., Alitalo K. A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J. Exp. Med. 2015, 212:991-999.
34. Louveau A., Smirnov I., Keyes T.J., Eccles J.D., Rouhani S.J., Peske J.D., Derecki N.C., Castle D., Mandell J.W., Lee K.S., Harris T.H., Kipnis J. Structural and functional features of central nervous system lymphatic vessels. Nature 2015, 523:337-341.
35. Feinberg D.A., Mark A.S. Human brain motion and cerebrospinal fluid circulation demonstrated with MR velocity imaging. Radiology 1987, 163:793-799.
36. Yamada S., Miyazaki M., Yamashita Y., Ouyang C., Yui M., Nakahashi M., Shimizu S., Aoki I., Morohoshi Y., McComb J.G. Influence of respiration on cerebrospinal fluid movement using magnetic resonance spin labeling. Fluids Barriers CNS 2013, 10:36.
37. Szentistvanyi I., Patlak C.S., Ellis R.A., Cserr H.F. Drainage of interstitial fluid from different regions of rat brain. Am. J. Physiol. 1984, 246:F835-F844.
38. Sykova E., Nicholson C. Diffusion in brain extracellular space. Physiol. Rev. 2008, 88:1277-1340.
39. Cserr H.F. Physiology of the choroid plexus. Physiol. Rev. 1971, 51:273-311.
40. Cserr H.F., Cooper D.N., Suri P.K., Patlak C.S. Efflux of radiolabeled polyethylene glycols and albumin from rat brain. Am. J. Physiol. 1981, 240:F319-F328.
41. Groothuis D.R., Vavra M.W., Schlageter K.E., Kang E.W., Itskovich A.C., Hertzler S., Allen C.V., Lipton H.L. Efflux of drugs and solutes from brain: the interactive roles of diffusional transcapillary transport, bulk flow and capillary transporters. J. Cereb. Blood Flow Metab. 2007, 27:43-56.
42. Rosenberg G.A., Kyner W.T., Estrada E. Bulk flow of brain interstitial fluid under normal and hyperosmolar conditions. Am. J. Physiol. 1980, 238:F42-F49.
43. Ichimura T., Fraser P.A., Cserr H.F. Distribution of extracellular tracers in perivascular spaces of the rat brain. Brain Res. 1991, 545:103-113.
44. Zhang E.T., Inman C.B., Weller R.O. Interrelationships of the pia mater and the perivascular (Virchow-Robin) spaces in the human cerebrum. J. Anat. 1990, 170:111-123.
45. Weller R.O., Djuanda E., Yow H.Y., Carare R.O. Lymphatic drainage of the brain and the pathophysiology of neurological disease. Acta Neuropathol. 2009, 117:1-14.
46. Hawkes C.A., Hartig W., Kacza J., Schliebs R., Weller R.O., Nicoll J.A., Carare R.O. 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.
47. Rennels M.L., Blaumanis O.R., Grady P.A. Rapid solute transport throughout the brain via paravascular fluid pathways. Adv. Neurol. 1990, 52:431-439.
48. Rennels M.L., Gregory T.F., Blaumanis O.R., Fujimoto K., Grady P.A. 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.
49. Pullen R.G., DePasquale M., Cserr H.F. Bulk flow of cerebrospinal fluid into brain in response to acute hyperosmolality. Am. J. Physiol. 1987, 253:F538-F545.
50. Iliff J.J., Wang M., Zeppenfeld D.M., Venkataraman A., Plog B.A., Liao Y., Deane R., Nedergaard M. Cerebral arterial pulsation drives paravascular CSF-interstitial fluid exchange in the murine brain. J. Neurosci. 2013, 33:18190-18199.
51. Xie L., Kang H., Xu Q., Chen M.J., Liao Y., Thiyagarajan M., O'Donnell J., Christensen D.J., Nicholson C., Iliff J.J., Takano T., Deane R., Nedergaard M. Sleep drives metabolite clearance from the adult brain. Science 2013, 342:373-377.
52. Iliff J.J., Lee H., Yu M., Feng T., Logan J., Nedergaard M., Benveniste H. Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J. Clin. Invest. 2013, 123:1299-1309.
53. Yang L., Kress B.T., Weber H.J., Thiyagarajan M., Wang B., Deane R., Benveniste H., Iliff J.J., Nedergaard M. Evaluating glymphatic pathway function utilizing clinically relevant intrathecal infusion of CSF tracer. J. Transl. Med. 2013, 11:107.
54. Lee H., Xie L., Yu M., Kang H., Feng T., Deane R., Logan J., Nedergaard M., Benveniste H. The effect of body posture on brain glymphatic transport. J. Neurosci. 2015, 35:11034-11044.
55. Lochhead J.J., Wolak D.J., Pizzo M.E., Thorne R.G. Rapid transport within cerebral perivascular spaces underlies widespread tracer distribution in the brain after intranasal administration. J. Cereb. Blood Flow Metab. 2015, 35:371-381.
56. Nedergaard M. Neuroscience. Garbage truck of the brain. Science 2013, 340:1529-1530.
57. Kervezee L., Hartman R., Van Den Berg D.J., Shimizu S., Emoto-Yamamoto Y., Meijer J.H., de Lange E.C. Diurnal variation in P-glycoprotein-mediated transport and cerebrospinal fluid turnover in the brain. AAPS J. 2014, 16:1029-1037.
58. Ohshiro K., Yaoita E., Yoshida Y., Fujinaka H., Matsuki A., Kamiie J., Kovalenko P., Yamamoto T. Expression and immunolocalization of AQP6 in intercalated cells of the rat kidney collecting duct. Arch. Histol. Cytol. 2001, 64:329-338.
59. Zeidel M.L., Ambudkar S.V., Smith B.L., Agre P. Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein. Biochemistry 1992, 31:7436-7440.
60. MacAulay N., Zeuthen T. Water transport between CNS compartments: contributions of aquaporins and cotransporters. Neuroscience 2010, 168:941-956.
61. Hasegawa H., Ma T., Skach W., Matthay M.A., Verkman A.S. Molecular cloning of a mercurial-insensitive water channel expressed in selected water-transporting tissues. J. Biol. Chem. 1994, 269:5497-5500.
62. Jung J.S., Bhat R.V., Preston G.M., Guggino W.B., Baraban J.M., Agre P. Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:13052-13056.
63. Verbavatz J.M., Ma T., Gobin R., Verkman A.S. Absence of orthogonal arrays in kidney, brain and muscle from transgenic knockout mice lacking water channel aquaporin-4. J. Cell Sci. 1997, 110(Pt 22):2855-2860.
64. Yang B., Brown D., Verkman A.S. The mercurial insensitive water channel (AQP-4) forms orthogonal arrays in stably transfected Chinese hamster ovary cells. J. Biol. Chem. 1996, 271:4577-4580.
65. Camassa L.M., Lunde L.K., Hoddevik E.H., Stensland M., Boldt H.B., De Souza G.A., Ottersen O.P., Amiry-Moghaddam M. Mechanisms underlying AQP4 accumulation in astrocyte endfeet. Glia 2015.
66. Papadopoulos M.C., Verkman A.S. Aquaporin water channels in the nervous system. Nat. Rev. Neurosci. 2013, 14:265-277.
67. Nagelhus E.A., Ottersen O.P. Physiological roles of aquaporin-in brain. Physiol. Rev. 2013, 93:1543-1562.
68. Eid T., Lee T.S., Thomas M.J., Amiry-Moghaddam M., Bjornsen L.P., Spencer D.D., Agre P., Ottersen O.P., de Lanerolle N.C. Loss of perivascular aquaporin 4 may underlie deficient water and K+ homeostasis in the human epileptogenic hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:1193-1198.
69. Yang J., Lunde L.K., Nuntagij P., Oguchi T., Camassa L.M., Nilsson L.N., Lannfelt L., Xu Y., Amiry-Moghaddam M., Ottersen O.P., Torp R. Loss of astrocyte polarization in the tg-ArcSwe mouse model of Alzheimer's disease. J. Alzheimers Dis. 2011, 27:711-722.
70. Ren Z., Iliff J.J., Yang L., Yang J., Chen X., Chen M.J., Giese R.N., Wang B., Shi X., Nedergaard M. 'Hit & run' model of closed-skull traumatic brain injury (TBI) reveals complex patterns of post-traumatic AQP4 dysregulation. J. Cereb. Blood Flow Metab. 2013, 33:834-845.
71. Crane J.M., Tajima M., Verkman A.S. Live-cell imaging of aquaporin-diffusion and interactions in orthogonal arrays of particles. Neuroscience 2010, 168:892-902.
72. Fenton R.A., Moeller H.B., Zelenina M., Snaebjornsson M.T., Holen T., MacAulay N. Differential water permeability and regulation of three aquaporin 4 isoforms. Cell. Mol. Life Sci. 2010, 67:829-840.
73. Furman C.S., Gorelick-Feldman D.A., Davidson K.G., Yasumura T., Neely J.D., Agre P., Rash J.E. Aquaporin-square array assembly: opposing actions of M1 and M23 isoforms. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:13609-13614.
74. Silberstein C., Bouley R., Huang Y., Fang P., Pastor-Soler N., Brown D., Van Hoek A.N. Membrane organization and function of M1 and M23 isoforms of aquaporin-in epithelial cells. Am. J. Physiol. Renal Physiol. 2004, 287:F501-F511.
75. Thrane A.S., Rangroo Thrane V., Nedergaard M. Drowning stars: reassessing the role of astrocytes in brain edema. Trends Neurosci. 2014, 37:620-628.
76. Smith A.J., Jin B.J., Verkman A.S. Muddying the water in brain edema?. Trends Neurosci. 2015, 38:331-332.
77. Thrane A.S., Rangroo Thrane V., Plog B.A., Nedergaard M. Filtering the muddied waters of brain edema. Trends Neurosci. 2015, 38:333-335.
78. Matsumae M., Hirayama A., Atsumi H., Yatsushiro S., Kuroda K. Velocity and pressure gradients of cerebrospinal fluid assessed with magnetic resonance imaging. J. Neurosurg. 2014, 120:218-227.
79. Nagelhus E.A., Veruki M.L., Torp R., Haug F.M., Laake J.H., Nielsen S., Agre P., Ottersen O.P. Aquaporin-water channel protein in the rat retina and optic nerve: polarized expression in Muller cells and fibrous astrocytes. J. Neurosci. 1998, 18:2506-2519.
80. Karran E., Mercken M., De Strooper B. The amyloid cascade hypothesis for Alzheimer's disease: an appraisal for the development of therapeutics. Nat. Rev. Drug Discov. 2011, 10:698-712.
81. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
82. Rogers J., Strohmeyer R., Kovelowski C.J., Li R. Microglia and inflammatory mechanisms in the clearance of amyloid beta peptide. Glia 2002, 40:260-269.
83. Pfefferbaum A., Mathalon D.H., Sullivan E.V., Rawles J.M., Zipursky R.B., Lim K.O. A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. Arch. Neurol. 1994, 51:874-887.
84. Albeck M.J., Skak C., Nielsen P.R., Olsen K.S., Borgesen S.E., Gjerris F. Age dependency of resistance to cerebrospinal fluid outflow. J. Neurosurg. 1998, 89:275-278.
85. Attems J., Jellinger K., Thal D.R., Van Nostrand W. Review: sporadic cerebral amyloid angiopathy. Neuropathol. Appl. Neurobiol. 2011, 37:75-93.
86. Cirrito J.R., Yamada K.A., Finn M.B., Sloviter R.S., Bales K.R., May P.C., Schoepp D.D., Paul S.M., Mennerick S., Holtzman D.M. Synaptic activity regulates interstitial fluid amyloid-beta levels in vivo. Neuron 2005, 48:913-922.
87. Paresce D.M., Ghosh R.N., Maxfield F.R. Microglial cells internalize aggregates of the Alzheimer's disease amyloid beta-protein via a scavenger receptor. Neuron 1996, 17:553-565.
88. Wyss-Coray T., Loike J.D., Brionne T.C., Lu E., Anankov R., Yan F., Silverstein S.C., Husemann J. Adult mouse astrocytes degrade amyloid-beta in vitro and in situ. Nat. Med. 2003, 9:453-457.
89. Kang J.E., Lim M.M., Bateman R.J., Lee J.J., Smyth L.P., Cirrito J.R., Fujiki N., Nishino S., Holtzman D.M. Amyloid-beta dynamics are regulated by orexin and the sleep-wake cycle. Science 2009, 326:1005-1007.
90. Deane R., Bell R.D., Sagare A., Zlokovic B.V. 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.
91. Pascale C.L., Miller M.C., Chiu C., Boylan M., Caralopoulos I.N., Gonzalez L., Johanson C.E., Silverberg G.D. Amyloid-beta transporter expression at the blood-CSF barrier is age-dependent. Fluids Barriers CNS 2011, 8:21.
92. Masseguin C., LePanse S., Corman B., Verbavatz J.M., Gabrion J. Aging affects choroidal proteins involved in CSF production in Sprague-Dawley rats. Neurobiol. Aging 2005, 26:917-927.
93. Silverberg G.D., Heit G., Huhn S., Jaffe R.A., Chang S.D., Bronte-Stewart H., Rubenstein E., Possin K., Saul T.A. The cerebrospinal fluid production rate is reduced in dementia of the Alzheimer's type. Neurology 2001, 57:1763-1766.
94. Plog B.A., Dashnaw M.L., Hitomi E., Peng W., Liao Y., Lou N., Deane R., Nedergaard M. Biomarkers of traumatic injury are transported from brain to blood via the glymphatic system. J. Neurosci. 2015, 35:518-526.
95. Billingsley M.L., Kincaid R.L. Regulated phosphorylation and dephosphorylation of tau protein: effects on microtubule interaction, intracellular trafficking and neurodegeneration. Biochem. J. 1997, 323(Pt 3):577-591.
96. Yamada K., Holth J.K., Liao F., Stewart F.R., Mahan T.E., Jiang H., Cirrito J.R., Patel T.K., Hochgrafe K., Mandelkow E.M., Holtzman D.M. Neuronal activity regulates extracellular tau in vivo. J. Exp. Med. 2014, 211:387-393.
97. Holmes B.B., Diamond M.I. Prion-like properties of tau protein: the importance of extracellular tau as a therapeutic target. J. Biol. Chem. 2014, 289:19855-19861.
98. Hawkes C.A., Sullivan P.M., Hands S., Weller R.O., Nicoll J.A., Carare R.O. Disruption of arterial perivascular drainage of amyloid-beta from the brains of mice expressing the human APOE epsilon4 allele. PLoS One 2012, 7.
99. Weller R.O., Subash M., Preston S.D., Mazanti I., Carare R.O. Perivascular drainage of amyloid-beta peptides from the brain and its failure in cerebral amyloid angiopathy and Alzheimer's disease. Brain Pathol. 2008, 18:253-266.
100. Rangroo Thrane V., Thrane A.S., Plog B.A., Thiyagarajan M., Iliff J.J., Deane R., Nagelhus E.A., Nedergaard M. Paravascular microcirculation facilitates rapid lipid transport and astrocyte signaling in the brain. Sci. Rep. 2013, 3:2582.
101. Ramanathan A., Nelson A.R., Sagare A.P., Zlokovic B.V. Impaired vascular-mediated clearance of brain amyloid beta in Alzheimer's disease: the role, regulation and restoration of LRP1. Front. Aging Neurosci. 2015, 7:136.
102. Johanson C., Stopa E., McMillan P., Roth D., Funk J., Krinke G. The distributional nexus of choroid plexus to cerebrospinal fluid, ependyma and brain: toxicologic/pathologic phenomena, periventricular destabilization, and lesion spread. Toxicol. Pathol. 2011, 39:186-212.
103. Sharma H.S., Duncan J.A., Johanson C.E. Whole-body hyperthermia in the rat disrupts the blood-cerebrospinal fluid barrier and induces brain edema. Acta Neurochir. Suppl. 2006, 96:426-431.
104. Carlos T.M., Clark R.S., Franicola-Higgins D., Schiding J.K., Kochanek P.M. Expression of endothelial adhesion molecules and recruitment of neutrophils after traumatic brain injury in rats. J. Leukoc. Biol. 1997, 61:279-285.
105. Vinters H.V., Ellis W.G., Zarow C., Zaias B.W., Jagust W.J., Mack W.J., Chui H.C. Neuropathologic substrates of ischemic vascular dementia. J. Neuropathol. Exp. Neurol. 2000, 59:931-945.
106. Smith D.H., Johnson V.E., Stewart W. Chronic neuropathologies of single and repetitive TBI: substrates of dementia?. Nat. Rev. Neurol. 2013, 9:211-221.
107. Haglund M., Passant U., Sjobeck M., Ghebremedhin E., Englund E. Cerebral amyloid angiopathy and cortical microinfarcts as putative substrates of vascular dementia. Int. J. Geriatr. Psychiatry 2006, 21:681-687.
108. Guo Z., Cupples L.A., Kurz A., Auerbach S.H., Volicer L., Chui H., Green R.C., Sadovnick A.D., Duara R., DeCarli C., Johnson K., Go R.C., Growdon J.H., Haines J.L., Kukull W.A., Farrer L.A. Head injury and the risk of AD in the MIRAGE study. Neurology 2000, 54:1316-1323.
109. Plassman B.L., Havlik R.J., Steffens D.C., Helms M.J., Newman T.N., Drosdick D., Phillips C., Gau B.A., Welsh-Bohmer K.A., Burke J.R., Guralnik J.M., Breitner J.C. Documented head injury in early adulthood and risk of Alzheimer's disease and other dementias. Neurology 2000, 55:1158-1166.
110. Nordstrom P., Michaelsson K., Gustafson Y., Nordstrom A. Traumatic brain injury and young onset dementia: a nationwide cohort study. Ann. Neurol. 2014, 75:374-381.
111. Ribeiro Mde C., Hirt L., Bogousslavsky J., Regli L., Badaut J. Time course of aquaporin expression after transient focal cerebral ischemia in mice. J. Neurosci. Res. 2006, 83:1231-1240.
112. Hirt L., Ternon B., Price M., Mastour N., Brunet J.F., Badaut J. Protective role of early aquaporin 4 induction against postischemic edema formation. J. Cereb. Blood Flow Metab. 2009, 29:423-433.
113. Wang M., Iliff J.J., Liao Y., Chen M.J., Shinseki M.S., Venkataraman A., Cheung J., Wang W., Nedergaard M. Cognitive deficits and delayed neuronal loss in a mouse model of multiple microinfarcts. J. Neurosci. 2012, 32:17948-17960.
114. Lu D.C., Zador Z., Yao J., Fazlollahi F., Manley G.T.M.D.P.D. Aquaporin-Reduces Post-Traumatic Seizure Susceptibility by Promoting Astrocytic Glial Scar Formation in Mice. J Neurotrauma 2011.
115. Fukuda A.M., Pop V., Spagnoli D., Ashwal S., Obenaus A., Badaut J. Delayed increase of astrocytic aquaporin 4 after juvenile traumatic brain injury: possible role in edema resolution?. Neuroscience 2012, 222:366-378.
116. Iliff J.J., Nedergaard M. Is there a cerebral lymphatic system?. Stroke 2013, 44:S93-S95.
117. Black P.M., Tzouras A., Foley L. Cerebrospinal fluid dynamics and hydrocephalus after experimental subarachnoid hemorrhage. Neurosurgery 1985, 17:57-62.
118. Blasberg R., Johnson D., Fenstermacher J. Absorption resistance of cerebrospinal fluid after subarachnoid hemorrhage in the monkey; effects of heparin. Neurosurgery 1981, 9:686-691.
119. Brinker T., Seifert V., Stolke D. Effect of intrathecal fibrinolysis on cerebrospinal fluid absorption after experimental subarachnoid hemorrhage. J. Neurosurg. 1991, 74:789-793.
120. Bartholomaus I., Kawakami N., Odoardi F., Schlager C., Miljkovic D., Ellwart J.W., Klinkert W.E., Flugel-Koch C., Issekutz T.B., Wekerle H., Flugel A. Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature 2009, 462:94-98.
121. Lucchinetti C.F., Popescu B.F., Bunyan R.F., Moll N.M., Roemer S.F., Lassmann H., Bruck W., Parisi J.E., Scheithauer B.W., Giannini C., Weigand S.D., Mandrekar J., Ransohoff R.M. Inflammatory cortical demyelination in early multiple sclerosis. N. Engl. J. Med. 2011, 365:2188-2197.
122. McCandless E.E., Piccio L., Woerner B.M., Schmidt R.E., Rubin J.B., Cross A.H., Klein R.S. Pathological expression of CXCL12 at the blood-brain barrier correlates with severity of multiple sclerosis. Am. J. Pathol. 2008, 172:799-808.
123. McCandless E.E., Wang Q., Woerner B.M., Harper J.M., Klein R.S. CXCL12 limits inflammation by localizing mononuclear infiltrates to the perivascular space during experimental autoimmune encephalomyelitis. J. Immunol. 2006, 177:8053-8064.
124. Reboldi A., Coisne C., Baumjohann D., Benvenuto F., Bottinelli D., Lira S., Uccelli A., Lanzavecchia A., Engelhardt B., Sallusto F. C-chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat. Immunol. 2009, 10:514-523.
125. Lennon V.A., Kryzer T.J., Pittock S.J., Verkman A.S., Hinson S.R. IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-water channel. J. Exp. Med. 2005, 202:473-477.
126. Lennon V.A., Wingerchuk D.M., Kryzer T.J., Pittock S.J., Lucchinetti C.F., Fujihara K., Nakashima I., Weinshenker B.G. A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 2004, 364:2106-2112.
127. Roemer S.F., Parisi J.E., Lennon V.A., Benarroch E.E., Lassmann H., Bruck W., Mandler R.N., Weinshenker B.G., Pittock S.J., Wingerchuk D.M., Lucchinetti C.F. Pattern-specific loss of aquaporin-immunoreactivity distinguishes neuromyelitis optica from multiple sclerosis. Brain 2007, 130:1194-1205.
128. Wolburg-Buchholz K., Mack A.F., Steiner E., Pfeiffer F., Engelhardt B., Wolburg H. Loss of astrocyte polarity marks blood-brain barrier impairment during experimental autoimmune encephalomyelitis. Acta Neuropathol. 2009, 118:219-233.
129. Iliff J.J., Goldman S.A., Nedergaard M. Implications of the discovery of brain lymphatic pathways. Lancet Neurol. 2015, 14:977-979.