Rapid transport of CCL11 across the blood-brain barrier: Regional variation and importance of blood cells

Journal of Pharmacology and Experimental Therapeutics

Volumn 349, Issue 3, 2014, Pages 497-507

  Erickson, Michelle A ^a,b,c   Morofuji, Yoichi ^b,c,e   Owen, Joshua B ^b,c,d   Banks, William A ^b,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

^e NAGASAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; CHEMOKINE RECEPTOR CCR3; EOTAXIN; IODINE 125;

ANATOMICAL VARIATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN PERFUSION; CELL SEPARATION; CONTROLLED STUDY; EFFUSION; ELECTRIC RESISTANCE; ENZYME LINKED IMMUNOSORBENT ASSAY; EX VIVO STUDY; IN VITRO STUDY; INHIBITION KINETICS; IODINATION; MALE; MEMBRANE BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TRANSPORT; TRANSENDOTHELIAL ELECTRICAL RESISTANCE;

ANIMALS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN; CELLS, CULTURED; CHEMOKINE CCL11; ENDOTHELIAL CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; INJECTIONS, INTRAVENOUS; IODINE RADIOISOTOPES; MALE; MICE; PRIMARY CELL CULTURE; REGRESSION ANALYSIS; TISSUE DISTRIBUTION;

EID: 84901199939     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.114.213074     Document Type: Article

References (42)

1. Adzemovic MZ, Öckinger J, Zeitelhofer M, Hochmeister S, Beyeen AD, Paulson A, Gillett A, Thessen Hedreul M, Covacu R, and Lassmann H, et al. (2012) Expression of Ccl11 associates with immune response modulation and protection against neuroinflammation in rats. PLoS ONE 7:e39794.
2. Akanuma S, Hosoya K, Ito S, Tachikawa M, Terasaki T, and Ohtsuki S (2010) Involvement of multidrug resistance-Associated protein 4 in efflux transport of prostaglandin E(2) across mouse blood-brain barrier and its inhibition by intravenous administration of cephalosporins. J Pharmacol Exp Ther 333:912-919.
3. Banks WA (2005) Blood-brain barrier transport of cytokines: a mechanism for neu-ropathology. Curr Pharm Des 11:973-984.
4. Banks WA, Clever CM, and Farrell CL (2000) Partial saturation and regional variation in the blood-to-brain transport of leptin in normal weight mice. Am J Physiol Endocrinol Metab 278:E1158-E1165.
5. Banks WA, Farr SA, and Morley JE (2002-2003) Entry of blood-borne cytokines into the central nervous system: effects on cognitive processes. Neuroimmunomodulation 10:319-327.
6. Banks WA and Kastin AJ (1989) Quantifying carrier-mediated transport of peptides from the brain to the blood. Methods Enzymol 168:652-660.
7. Banks WA, Niehoff ML, and Zalcman SS (2004) Permeability of the mouse blood-brain barrier to murine interleukin-2: predominance of a saturable efflux system. Brain Behav Immun 18:434-442.
8. Blasberg RG, Fenstermacher JD, and Patlak CS (1983) Transport of alpha-Aminoisobutyric acid across brain capillary and cellular membranes. J Cereb Blood Flow Metab 3:8-32.
9. Broman T, Radner S, and Svanberg L (1950) Supravital analysis of disorders in the cerebrovascular permeability. Acta Psychiatr Neurol 25:121-135.
10. Coisne C, Dehouck L, Faveeuw C, Delplace Y, Miller F, Landry C, Morissette C, Fenart L, Cecchelli R, Tremblay P, and Dehouck B (2005) Mouse syngenic in vitro blood-brain barrier model: a new tool to examine inflammatory events in cerebral endothelium. Lab Invest 85:734-746.
11. Culver JC, Vadakkan TJ, and Dickinson ME (2013) A specialized microvascular domain in the mouse neural stem cell niche. PLoS ONE 8:e53546.
12. Drewes LR, Conway WP, and Gilboe DD (1977) Net amino acid transport between plasma and erythrocytes and perfused dog brain. Am J Physiol 233:E320-E325.
13. Edinger AL, Mankowski JL, Doranz BJ, Margulies BJ, Lee B, Rucker J, Sharron M, Hoffman TL, Berson JF, and Zink MC, et al. (1997) CD4-independent, CCR5-dependent infection of brain capillary endothelial cells by a neurovirulent simian immunodeficiency virus strain. Proc Natl Acad Sci USA 94:14742-14747.
14. Elias MF, Elias PK, Sullivan LM, Wolf PA, and D'Agostino RB (2003) Lower cognitive function in the presence of obesity and hypertension: the Framingham heart study. Int J Obes Relat Metab Disord 27:260-268.
15. Ellyard JI, Simson L, Bezos A, Johnston K, Freeman C, and Parish CR (2007) Eotaxin selectively binds heparin. An interaction that protects eotaxin from pro-teolysis and potentiates chemotactic activity in vivo. J Biol Chem 282: 15238-15247.
16. Fernandez-Egea E, Scoriels L, Theegala S, Giro M, Ozanne SE, Burling K, and Jones PB (2013) Cannabis use is associated with increased CCL11 plasma levels in young healthy volunteers. Prog Neuropsychopharmacol Biol Psychiatry 46:25-28.
17. Goldberg JS and Hirschi KK (2009) Diverse roles of the vasculature within the neural stem cell niche. Regen Med 4:879-897.
18. Grassi-Oliveira R, Brieztke E, Teixeira A, Pezzi JC, Zanini M, Lopes RP, and Bauer ME (2012) Peripheral chemokine levels in women with recurrent major depression with suicidal ideation. Rev Bras Psiquiatr 34:71-75.
19. Greenwood J, Luthert PJ, Pratt OE, and Lantos PL (1985) Maintenance of the integrity of the blood-brain barrier in the rat during an in situ saline-based perfusion. Neurosci Lett 56:223-227.
20. Grontoft O (1954) Intracranial haemorrhage and blood-brain barrier problems in the new-born; a pathologico-Anatomical and experimental investigation. Acta Pathol Microbiol Scand Suppl 100:8-109.
21. Gutierrez EG, Banks WA, and Kastin AJ (1993) Murine tumor necrosis factor alpha is transported from blood to brain in the mouse. J Neuroimmunol 47:169-176.
22. Hinderling PH (1997) Red blood cells: a neglected compartment in pharmacokinetics and pharmacodynamics. Pharmacol Rev 49:279-295.
23. Jacquez JA (1984) Red blood cell as glucose carrier: significance for placental and cerebral glucose transfer. Am J Physiol 246:R289-R298.
24. Jorm AF (2000) Is depression a risk factor for dementia or cognitive decline? A review. Gerontology 46:219-227.
25. Kastin AJ, Akerstrom V, and Pan W (2001) Validity of multiple-time regression analysis in measurement of tritiated and iodinated leptin crossing the blood-brain barrier: meaningful controls. Peptides 22:2127-2136.
26. Kempermann G, Wiskott L, and Gage FH (2004) Functional significance of adult neurogenesis. Curr Opin Neurobiol 14:186-191.
27. Khan NA, Di Cello F, Stins M, and Kim KS (2007) Gp120-mediated cytotoxicity of human brain microvascular endothelial cells is dependent on p38 mitogen-Activated protein kinase activation. J Neurovirol 13:242-251.
28. Kitaura M, Nakajima T, Imai T, Harada S, Combadiere C, Tiffany HL, Murphy PM, and Yoshie O (1996) Molecular cloning of human eotaxin, an eosinophil-selective CC chemokine, and identification of a specific eosinophil eotaxin receptor, CC chemokine receptor 3. J Biol Chem 271:7725-7730.
29. Krieglstein G, Krieglstein J, and Urban W (1972) Long survival time of an isolated perfused rat brain. J Neurochem 19:885-886.
30. Leung R, Proitsi P, Simmons A, Lunnon K, Güntert A, Kronenberg D, Pritchard M, Tsolaki M, Mecocci P, and Kloszewska I, et al. (2013) Inflammatory proteins in plasma are associated with severity of Alzheimer's disease. PLoS ONE 8:e64971.
31. Mukhtar M, Harley S, Chen P, BouHamdan M, Patel C, Acheampong E, and Pomerantz RJ (2002) Primary isolated human brain microvascular endothelial cells express diverse HIV/SIV-Associated chemokine coreceptors and DC-SIGN and L-SIGN. Virology 297:78-88.
32. Perrière N, Demeuse P, Garcia E, Regina A, Debray M, Andreux JP, Couvreur P, Scherrmann JM, Temsamani J, and Couraud PO, et al. (2005) Puromycin-based purification of rat brain capillary endothelial cell cultures. Effect on the expression of blood-brain barrier-specific properties. J Neurochem 93:279-289.
33. Ponath PD, Qin S, Ringler DJ, Clark-Lewis I, Wang J, Kassam N, Smith H, Shi X, Gonzalo JA, and Newman W, et al. (1996) Cloning of the human eosinophil che-moattractant, eotaxin. Expression, receptor binding, and functional properties suggest a mechanism for the selective recruitment of eosinophils. J Clin Invest 97: 604-612.
34. Rankin SM, Conroy DM, and Williams TJ (2000) Eotaxin and eosinophil recruitment: implications for human disease. Mol Med Today 6:20-27.
35. Shibata M, Yamada S, Kumar SR, Calero M, Bading J, Frangione B, Holtzman DM, Miller CA, Strickland DK, and Ghiso J, et al. (2000) 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 106:1489-1499.
36. Shurin GV, Yurkovetsky ZR, Chatta GS, Tourkova IL, Shurin MR, and Lokshin AE (2007) Dynamic alteration of soluble serum biomarkers in healthy aging. Cytokine 39:123-129.
37. Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, and Doetsch F (2008) A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3:279-288.
38. Teixeira AL, Reis HJ, Nicolato R, Brito-Melo G, Correa H, Teixeira MM, and Romano-Silva MA (2008) Increased serum levels of CCL11/eotaxin in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 32:710-714.
39. Triguero D, Buciak J, and Pardridge WM (1990) Capillary depletion method for quantification of blood-brain barrier transport of circulating peptides and plasma proteins. J Neurochem 54:1882-1888.
40. Vasudevan AR, Wu H, Xydakis AM, Jones PH, Smith EO, Sweeney JF, Corry DB, and Ballantyne CM (2006) Eotaxin and obesity. J Clin Endocrinol Metab 91: 256-261.
41. Villeda SA, Luo J, Mosher KI, Zou B, Britschgi M, Bieri G, Stan TM, Fainberg N, Ding Z, and Eggel A, et al. (2011) The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 477:90-94.
42. Wainwright DA, Xin J, Mesnard NA, Beahrs TR, Politis CM, Sanders VM, and Jones KJ (2009) Exacerbation of facial motoneuron loss after facial nerve axotomy in CCR3-deficient mice. ASN Neuro 1:e00024.