The role of shear stress in Blood-Brain Barrier endothelial physiology

BMC Neuroscience

Volumn 12, Issue , 2011, Pages

  Cucullo, Luca ^a   Hossain, Mohammed ^a   Puvenna, Vikram ^a   Marchi, Nicola ^a   Janigro, Damir ^a,b  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CLEVELAND CLINIC LERNER COLLEGE OF MEDICINE   (United States)

Author keywords

Alternative,In vitro; Cell Cycle; Cerebral blood flowShear stress; Inflammation

Indexed keywords

CARBOXYLIC ACID; CARRIER PROTEIN; CELL ADHESION MOLECULE; CYTOCHROME P450; CYTOSKELETON PROTEIN; GLUCOSE; INTEGRIN; ION CHANNEL; LACTATE DEHYDROGENASE; LACTIC ACID; MULTIDRUG RESISTANCE PROTEIN; PROTEIN BTG; RNA; UNCLASSIFIED DRUG; VASCULAR ADHESION PROTEIN 1;

ARTICLE; BIOENERGY; BLOOD BRAIN BARRIER; CELL CYCLE; CELL DIFFERENTIATION; CELL INTERACTION; CELL JUNCTION; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; CITRIC ACID CYCLE; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; GENE INDUCTION; GENE REPRESSION; GLUCOSE METABOLISM; GLYCOLYSIS; HUMAN; HUMAN CELL; NEUROLOGIC DISEASE; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SHEAR STRESS; TIGHT JUNCTION; VASCULAR ENDOTHELIUM; ASTROCYTE; BIOLOGICAL MODEL; CELL CULTURE; ENERGY METABOLISM; GENE EXPRESSION REGULATION; INFLAMMATION; MECHANICAL STRESS; METABOLISM; PHYSIOLOGY;

ASTROCYTES; BLOOD-BRAIN BARRIER; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GLUCOSE; HUMANS; INFLAMMATION; MODELS, BIOLOGICAL; STRESS, MECHANICAL;

EID: 79955752356     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-12-40     Document Type: Article

References (51)

1. Emmi A, Wenzel HJ, Schwartzkroin PA, Taglialatela M, Castaldo P, Bianchi L, et al. Do glia have heart? Expression and functional role for ether-a-go-go currents in hippocampal astrocytes. J Neurosci 2000, 20:3915-3925.
2. Cornford EM, Hyman S. Localization of brain endothelial luminal and abluminal transporters with immunogold electron microscopy. NeuroRx 2005, 2:27-43. 10.1602/neurorx.2.1.27, 539318, 15717055.
3. Dauchy S, Dutheil F, Weaver RJ, Chassoux F, Daumas-Duport C, Couraud PO, et al. ABC transporters, cytochromes P450 and their main transcription factors: expression at the human blood-brain barrier. J Neurochem 2008, 107:1518-1528. 10.1111/j.1471-4159.2008.05720.x, 19094056.
4. Cornford EM, Varesi JB, Hyman S, Damian RT, Raleigh MJ. Mitochondrial content of choroid plexus epithelium. Exp Brain Res 1997, 116:399-405. 10.1007/PL00005768, 9372289.
5. Steiner O, Coisne C, Cecchelli R, Boscacci R, Deutsch U, Engelhardt B, et al. Differential roles for endothelial ICAM-1, ICAM-2, and VCAM-1 in shear-resistant T cell arrest, polarization, and directed crawling on blood-brain barrier endothelium. J Immunol 2010, 185:4846-4855. 10.4049/jimmunol.0903732, 20861356.
6. Koutsiaris AG, Tachmitzi SV, Batis N, Kotoula MG, Karabatsas CH, Tsironi E, et al. Volume flow and wall shear stress quantification in the human conjunctival capillaries and post-capillary venules in vivo. Biorheology 2007, 44:375-386.
7. Dewey CF, Bussolari SR, Gimbrone MA, Davies PF. The dynamic response of vascular endothelial cells to fluid shear stress. J Biomech Eng 1981, 103:177-185. 10.1115/1.3138276, 7278196.
8. Schnittler HJ. Structural and functional aspects of intercellular junctions in vascular endothelium. Basic Res Cardiol 1998, 93(Suppl 3):30-39.
9. Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006, 7:41-53. 10.1038/nrn1824, 16371949.
10. Warren MS, Zerangue N, Woodford K, Roberts LM, Tate EH, Feng B, et al. Comparative gene expression profiles of ABC transporters in brain microvessel endothelial cells and brain in five species including human. Pharmacol Res 2009, 59:404-413. 10.1016/j.phrs.2009.02.007, 19429473.
11. Ghosh C, Gonzalez-Martinez J, Hossain M, Cucullo L, Fazio V, Janigro D, et al. Pattern of P450 expression at the human blood-brain barrier: roles of epileptic condition and laminar flow. Epilepsia 2010, 51:1408-1417. 10.1111/j.1528-1167.2009.02428.x, 20074231.
12. Meyer RP, Gehlhaus M, Knoth R, Volk B. Expression and function of cytochrome p450 in brain drug metabolism. Curr Drug Metab 2007, 8:297-306. 10.2174/138920007780655478, 17504219.
13. Wong D, Prameya R, Dorovini-Zis K. Adhesion and migration of polymorphonuclear leukocytes across human brain microvessel endothelial cells are differentially regulated by endothelial cell adhesion molecules and modulate monolayer permeability. J Neuroimmunol 2007, 184:136-148. 10.1016/j.jneuroim.2006.12.003, 17291598.
14. Doring A, Wild M, Vestweber D, Deutsch U, Engelhardt B. E- and P-selectin are not required for the development of experimental autoimmune encephalomyelitis in C57BL/6 and SJL mice. J Immunol 2007, 179:8470-8479.
15. Cheng YF, Kramer RH. Human microvascular endothelial cells express integrin-related complexes that mediate adhesion to the extracellular matrix. J Cell Physiol 1989, 139:275-286. 10.1002/jcp.1041390209, 2469686.
16. Santaguida S, Janigro D, Hossain M, Oby E, Rapp E, Cucullo L. Side by side comparison between dynamic versus static models of blood-brain barrier in vitro: a permeability study. Brain Res 2006, 1109:1-13. 10.1016/j.brainres.2006.06.027, 16857178.
17. Berthet C, Guehenneux F, Revol V, Samarut C, Lukaszewicz A, Dehay C, et al. Interaction of PRMT1 with BTG/TOB proteins in cell signalling: molecular analysis and functional aspects. Genes Cells 2002, 7:29-39. 10.1046/j.1356-9597.2001.00497.x, 11856371.
18. Huang S, Litt M, Felsenfeld G. Methylation of histone H4 by arginine methyltransferase PRMT1 is essential in vivo for many subsequent histone modifications. Genes Dev 2005, 19:1885-1893. 10.1101/gad.1333905, 1186188, 16103216.
19. Tashiro E, Tsuchiya A, Imoto M. Functions of cyclin D1 as an oncogene and regulation of cyclin D1 expression. Cancer Sci 2007, 98:629-635. 10.1111/j.1349-7006.2007.00449.x, 17359287.
20. Hayashi A, Horiuchi A, Kikuchi N, Hayashi T, Fuseya C, Suzuki A, et al. Type-specific roles of histone deacetylase (HDAC) overexpression in ovarian carcinoma: HDAC1 enhances cell proliferation and HDAC3 stimulates cell migration with downregulation of E-cadherin. Int J Cancer 2010, 127:1332-1346. 10.1002/ijc.25151, 20049841.
21. Ando J, Yamamoto K. Vascular mechanobiology: endothelial cell responses to fluid shear stress. Circ J 2009, 73:1983-1992. 10.1253/circj.CJ-09-0583, 19801852.
22. Ballermann BJ, Dardik A, Eng E, Liu A. Shear stress and the endothelium. Kidney Int Suppl 1998, 67:S100-S108.
23. Desai SY, Marroni M, Cucullo L, Krizanac-Bengez L, Mayberg MR, Hossain MT, et al. Mechanisms of endothelial survival under shear stress. Endothelium 2002, 9:89-102. 10.1080/10623320212004, 12200960.
24. Wolburg H, Lippoldt A. Tight junctions of the blood-brain barrier: development, composition and regulation. Vascul Pharmacol 2002, 38:323-337. 10.1016/S1537-1891(02)00200-8, 12529927.
25. Abbruscato TJ, Davis TP. Protein expression of brain endothelial cell E-cadherin after hypoxia/aglycemia: influence of astrocyte contact. Brain Res 1999, 842:277-286. 10.1016/S0006-8993(99)01778-3, 10526124.
26. Kiptoo P, Sinaga E, Calcagno AM, Zhao H, Kobayashi N, Tambunan US, et al. Enhancement of drug absorption through the blood-brain barrier and inhibition of intercellular tight junction resealing by E-cadherin peptides. Mol Pharm 2011, 8:239-249. 10.1021/mp100293m, 21128658.
27. Sivapackiam J, Harpstrite SE, Prior JL, Gu H, Rath NP, Sharma V. Synthesis, molecular structure, and validation of metalloprobes for assessment of MDR1 P-glycoprotein-mediated functional transport. Dalton Trans 2010, 39:5842-5850. 10.1039/c002361b, 20505882.
28. Zhou SF, Wang LL, Di YM, Xue CC, Duan W, Li CG, et al. Substrates and inhibitors of human multidrug resistance associated proteins and the implications in drug development. Curr Med Chem 2008, 15:1981-2039. 10.2174/092986708785132870, 18691054.
29. Kubota H, Ishihara H, Langmann T, Schmitz G, Stieger B, Wieser HG, et al. Distribution and functional activity of P-glycoprotein and multidrug resistance-associated proteins in human brain microvascular endothelial cells in hippocampal sclerosis. Epilepsy Res 2006, 68:213-228. 10.1016/j.eplepsyres.2005.11.011, 16361082.
30. Mahar Doan KM, Humphreys JE, Webster LO, Wring SA, Shampine LJ, Serabjit-Singh CJ, et al. Passive permeability and P-glycoprotein-mediated efflux differentiate central nervous system (CNS) and non-CNS marketed drugs. J Pharmacol Exp Ther 2002, 303:1029-1037. 10.1124/jpet.102.039255, 12438524.
31. Wilson AC, Clemente L, Liu T, Bowen RL, Meethal SV, Atwood CS. Reproductive hormones regulate the selective permeability of the blood-brain barrier. Biochim Biophys Acta 2008, 1782:401-407.
32. Dietrich JB. Endothelial cells of the blood-brain barrier: a target for glucocorticoids and estrogens?. Front Biosci 2004, 9:684-693. 10.2741/1272, 14766400.
33. Bavner A, Shafaati M, Hansson M, Olin M, Shpitzen S, Meiner V, et al. On the mechanism of accumulation of cholestanol in the brain of mice with a disruption of sterol 27-hydroxylase. J Lipid Res 2010, 51:2722-2730. 10.1194/jlr.M008326, 20511491.
34. Xie C, Lund EG, Turley SD, Russell DW, Dietschy JM. Quantitation of two pathways for cholesterol excretion from the brain in normal mice and mice with neurodegeneration. J Lipid Res 2003, 44:1780-1789. 10.1194/jlr.M300164-JLR200, 12810827.
35. Yoshida Y, Sue W, Okano M, Oyama T, Yamane T, Mitsumata M. The effects of augmented hemodynamic forces on the progression and topography of atherosclerotic plaques. Ann N Y Acad Sci 1990, 598:256-273. 10.1111/j.1749-6632.1990.tb42298.x, 2248444.
36. Gendelman HE, Ding S, Gong N, Liu J, Ramirez SH, Persidsky Y, et al. Monocyte chemotactic protein-1 regulates voltage-gated K+ channels and macrophage transmigration. J Neuroimmune Pharmacol 2009, 4:47-59. 10.1007/s11481-008-9135-1, 2657224, 19034671.
37. Wilhelm I, Farkas AE, Nagyoszi P, Varo G, Balint Z, Vegh GA, et al. Regulation of cerebral endothelial cell morphology by extracellular calcium. Phys Med Biol 2007, 52:6261-6274. 10.1088/0031-9155/52/20/012, 17921584.
38. Hu J, Yuan X, Ko MK, Yin D, Sacapano MR, Wang X, et al. Calcium-activated potassium channels mediated blood-brain tumor barrier opening in a rat metastatic brain tumor model. Mol Cancer 2007, 6:22. 10.1186/1476-4598-6-22, 1831484, 17359538.
39. Mantych GJ, James DE, Devaskar SU. Jejunal/kidney glucose transporter isoform (Glut-5) is expressed in the human blood-brain barrier. Endocrinology 1993, 132:35-40. 10.1210/en.132.1.35, 8419132.
40. Farrell CL, Pardridge WM. Blood-brain barrier glucose transporter is asymmetrically distributed on brain capillary endothelial lumenal and ablumenal membranes: an electron microscopic immunogold study. Proc Natl Acad Sci USA 1991, 88:5779-5783. 10.1073/pnas.88.13.5779, 51961, 2062858.
41. Winkler GS. The mammalian anti-proliferative BTG/Tob protein family. J Cell Physiol 2010, 222:66-72. 10.1002/jcp.21919, 19746446.
42. Davies PF, Remuzzi A, Gordon EJ, Dewey CF, Gimbrone MA. Turbulent fluid shear stress induces vascular endothelial cell turnover in vitro. Proc Natl Acad Sci USA 1986, 83:2114-2117. 10.1073/pnas.83.7.2114, 323241, 3457378.
43. Ando J, Kamiya A. Flow-dependent regulation of gene expression in vascular endothelial cells. Jpn Heart J 1996, 37:19-32.
44. Davies PF, Remuzzi A, Gordon EJ, Dewey CF, Gimbrone MA. Turbulent fluid shear stress induces vascular endothelial cell turnover in vitro. Proc Natl Acad Sci USA 1986, 83:2114-2117. 10.1073/pnas.83.7.2114, 323241, 3457378.
45. Fukushima T, Azuma T. The horseshoe vortex: a secondary flow generated in arteries with stenosis, bifurcation, and branchings. Biorheology 1982, 19:143-154.
46. Kunz J, Schreiter B, Schubert B, Voss K, Krieg K. [Experimental investigations on the regeneration of aortic endothelial cells. Automatic and visual evaluation of autoradiograms (author's transl)]. Acta Histochem 1978, 61:53-63.
47. Yoshida Y, Sue W, Okano M, Oyama T, Yamane T, Mitsumata M. The effects of augmented hemodynamic forces on the progression and topography of atherosclerotic plaques. Ann N Y Acad Sci 1990, 598:256-273. 10.1111/j.1749-6632.1990.tb42298.x, 2248444.
48. Shusta EV. Blood-brain barrier genomics, proteomics, and new transporter discovery. NeuroRx 2005, 2:151-161. 10.1602/neurorx.2.1.151, 539336, 15717066.
49. Mazzone P, Tierney W, Hossain M, Puvenna V, Janigro D, Cucullo L. Pathophysiological impact of cigarette smoke exposure on the cerebrovascular system with a focus on the blood-brain barrier: expanding the awareness of smoking toxicity in an underappreciated area. Int J Environ Res Public Health 2010, 7:4111-4126. 10.3390/ijerph7124111, 3037043, 21317997.
50. Cucullo L, Hossain M, Rapp E, Manders T, Marchi N, Janigro D. Development of a humanized in vitro blood-brain barrier model to screen for brain penetration of antiepileptic drugs. Epilepsia 2007, 48:505-516. 10.1111/j.1528-1167.2006.00960.x, 17326793.
51. Cucullo L, Marchi N, Hossain M, Janigro D. A dynamic in vitro BBB model for the study of immune cell trafficking into the central nervous system. J Cereb Blood Flow Metab 2010,