Shear stress regulates aquaporin-5 and airway epithelial barrier function

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 9, 2008, Pages 3345-3350

  Sidhaye, Venkataramana K ^a   Schweitzer, Kelly S ^a   Caterina, Michael J ^a   Shimoda, Larissa ^a   King, Landon S ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cytoskeleton; Epithelium; Permeability; Transient receptor potential vanilloid; Voltage gated calcium channel

Indexed keywords

NIFEDIPINE; RUTHENIUM RED; VANILLOID RECEPTOR 4; VOLTAGE GATED CALCIUM CHANNEL; AQUAPORIN 5; CALCIUM; CALCIUM CHANNEL L TYPE; TRPV4 PROTEIN, HUMAN; UNCLASSIFIED DRUG; VANILLOID RECEPTOR; WATER;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; CYTOSKELETON; DRUG INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY EPITHELIUM; SHEAR STRESS; ANIMAL; HUMAN; MECHANICAL STRESS; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; RESPIRATORY TRACT MUCOSA; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; AQUAPORIN 5; BIOLOGICAL TRANSPORT; CALCIUM; CALCIUM CHANNELS, L-TYPE; CELL MEMBRANE PERMEABILITY; HUMANS; MICE; MICE, KNOCKOUT; RESPIRATORY MUCOSA; STRESS, MECHANICAL; TRPV CATION CHANNELS; WATER;

EID: 42149154821     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0712287105     Document Type: Article

References (51)

1. White CR, Stevens HY, Haidekker M, Frangos JA (2005) Temporal gradients in shear, but not spatial gradients, stimulate ERK1/2 activation in human endothelial cells. Am J Physiol 289:H2350-H2355.
2. White CR, Haidekker MA, Stevens HY, Frangos JA (2004) Extracellular signal-regulated kinase activation and endothelin-1 production in human endothelial cells exposed to vibration. J Physiol 555:565-572.
3. Haidekker MA, White CR, Frangos JA (2001) Analysis of temporal shear stress gradients during the onset phase of flow over a backward-facing step. J Biomech Eng 123:455-463.
4. White CR, Haidekker M, Bao X, Frangos JA (2001) Temporal gradients in shear, but not spatial gradients, stimulate endothelial cell proliferation. Circulation 103:2508-2513.
5. Kapur S, Baylink DJ, Lau KH (2003) Fluid flow shear stress stimulates human osteoblast proliferation and differentiation through multiple interacting and competing signal transduction pathways. Bone 32:241-251.
6. Savla U, Sporn PH, Waters CM (1997) Cyclic stretch of airway epithelium inhibits prostanoid synthesis. Am J Physiol 273:L1013-L1019.
7. Cebral JR, Summers RM (2004) Tracheal and central bronchial aerodynamics using virtual bronchoscopy and computational fluid dynamics. IEEE Trans Med Imaging 23:1021-1033.
8. Tarran R, et al. (2005) Normal and cystic fibrosis airway surface liquid homeostasis. The effects of phasic shear stress and viral infections. J Biol Chem 280:35751-35759.
9. Olman MA (2003) Epithelial cell modulation of airway fibrosis in asthma. Am J Respir Cell Mol Biol 28:125-128.
10. Ballermann BJ, Dardik A, Eng E, Liu A (1998) Shear stress and the endothelium. Kidney Int Suppl 67:S100-S108.
11. Davies PF, Spaan JA, Krams R (2005) Shear stress biology of the endothelium. Ann Biomed Eng 33:1714-1718.
12. Davies PF, Zilberberg J, Helmke BP (2003) Spatial microstimuli in endothelial mechanosignaling. Circ Res 92:359-370.
13. Davies PF (2002) Multiple signaling pathways in flow-mediated endothelial mechanotransduction: PYK-ing the right location. Arterioscler Thromb Vasc Biol 22:1755-1757.
14. Davies PF, Polacek DC, Shi C, Helmke BP (2002) The convergence of haemodynamics, genomics, and endothelial structure in studies of the focal origin of atherosclerosis. Biorheology 39:299-306.
15. Helmke BP, Davies PF (2002) The cytoskeleton under external fluid mechanical forces: Hemodynamic forces acting on the endothelium. Ann Biomed Eng 30:284-296.
16. Helmke BP, Thakker DB, Goldman RD, Davies PF (2001) Spatiotemporal analysis of flow-induced intermediate filament displacement in living endothelial cells. Biophys J 80:184-194.
17. Huynh TT, Davies MG, Trovato MJ, Svendsen E, Hagen PO (1999) Alterations in wall tension and shear stress modulate tyrosine kinase signaling and wall remodeling in experimental vein grafts. J Vasc Surg 29:334-344.
18. Davies PF, et al. (1997) Spatial relationships in early signaling events of flow-mediated endothelial mechanotransduction. Annu Rev Physiol 59:527-549.
19. Davies PF, Mundel T, Barbee KA (1995) A mechanism for heterogeneous endothelial responses to flow in vivo and in vitro. J Biomech 28:1553-1560.
20. Davies PF (1995) Flow-mediated endothelial mechanotransduction. Physiol Rev 75:519-560.
21. Morita T, et al. (1994) Role of Ca2+ and protein kinase C in shear stress-induced actin depolymerization and endothelin 1 gene expression. Circ Res 75:630-636.
22. Kohler R, et al. (2006) Evidenceforafunctional role of endothelial transient receptor potential V4 in shear stress-induced vasodilatation. Arterioscler Thromb Vasc Biol 26:1495-1502.
23. Tschumperlin DJ, et al. (2004) Mechanotransduction through growth-factor shedding into the extracellular space. Nature 429:83-86.
24. Winters SL, Davis CW, Boucher RC (2007) Mechanosensitivity of mouse tracheal ciliary beat frequency: Roles for Ca2+, purinergic signaling, tonicity, and viscosity. Am J Physiol 292:L614-L624.
25. Liu X, et al. (2006) A role for AQP5 in activation of TRPV4 by hypotonicity: Concerted involvement of AQP5 and TRPV4 in regulation of cell volume recovery. J Biol Chem 281:15485-15495.
26. Sidhaye VK, et al. (2006) Transient receptor potential vanilloid 4 regulates aquaporin-5 abundance under hypotonic conditions. Proc Natl Acad Sci USA 103:4747-4752.
27. Nilius B, Voets T (2004) Diversity of TRP channel activation. Novartis Found Symp 258:140-149; discussion 149-159, 263-266.
28. Nilius B, Vriens J, Prenen J, Droogmans G, Voets T (2004) TRPV4 calcium entry channel: A paradigm for gating diversity. Am J Physiol 286:C195-C205.
29. Gao X, Wu L, O'Neil RG (2003) Temperature-modulated diversity of TRPV4 channel gating: Activation by physical stresses and phorbol ester derivatives through protein kinase C-dependent and -independent pathways. J Biol Chem 278:27129-27137.
30. O'Neil RG, Heller S (2005) The mechanosensitive nature of TRPV channels. Pflugers Arch 451:193-203.
31. Nilius B, Droogmans G, Wondergem R (2003) Transient receptor potential channels in endothelium: Solving the calcium entry puzzle? Endothelium 10:5-15.
32. Alvarez DF, et al. (2006) Transient receptor potential vanilloid 4-mediated disruption of the alveolar septal barrier: A novel mechanism of acute lung injury. Circ Res 99:988-995.
33. King LS, Kozono D, Agre P (2004) From structure to disease: The evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 5:687-698.
34. Kawedia JD, et al. (2007) Interaction between transcellular and paracellular water transport pathways through Aquaporin 5 and the tight junction complex. Proc Natl Acad Sci USA 104:3621-3626.
35. Jen CJ, Jhiang SJ, Chen HI (2000) Invited review: Effects of flow on vascular endothelial intracellular calcium signaling of rat aortas ex vivo. J Appl Physiol 89:1657-1662; discussion 1656.
36. Worthen LM, Nollert MU (2000) Intracellular calcium response of endothelial cells exposed to flow in the presence of thrombin or histamine. J Vasc Surg 32:593-601.
37. Sidhaye V, Hoffert JD, King LS (2005) cAMP has distinct acute and chronic effects on aquaporin-5 in lung epithelial cells. J Biol Chem 280:3590-3596.
38. Humlicek AL, et al. (2007) Paracellular permeability restricts airway epithelial responses to selectively allow activation by mediators at the basolateral surface. J Immunol 178:6395-6403.
39. Winter MC, Shasby SS, Ries DR, Shasby DM (2006) PAR2 activation interrupts E-cadherin adhesion and compromises the airway epithelial barrier: Protective effect of beta-agonists. Am J Physiol 291:L628-L635.
40. Coyne CB, et al. (2002) Regulation of airway tight junctions by proinflammatory cytokines. Mol Biol Cell 13:3218-3234.
41. Hogg JC, Pare PD, Boucher RC (1979) Bronchial mucosal permeability. FedProc 38:197-201.
42. Zabner J, et al. (2003) Histamine alters E-cadherin cell adhesion to increase human airway epithelial permeability. J Appl Physiol 95:394-401.
43. McCarthy KM, et al. (1996) Occludin is a functional component of the tight junction. J Cell Sci 109(Pt 9):2287-2298.
44. Balda MS, et al. (1996) Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J Cell Biol 134:1031-1049.
45. Reiter B, et al. (2006) TRPV4-mediated regulation of epithelial permeability. Faseb J 20:1802-1812.
46. Hamanaka K, et al. (2007) TRPV4 initiates the acute calcium-dependent permeability increase during ventilator-induced lung injury in isolated mouse lungs. Am J Physiol 293:L923-L932.
47. Noda Y, Horikawa S, Katayama Y, Sasaki S (2004) Water channel aquaporin-2 directly binds to actin. Biochem Biophys Res Commun 322:740-745.
48. Lindsey Rose KM, et al. (2006) The C terminus of lens aquaporin 0 interacts with the cytoskeletal proteins filensin and CP49. Invest Ophthalmol Vis Sci 47:1562-1570.
49. Wang J, Shimoda LA, Sylvester JT (2004) Capacitative calcium entry and TRPC channel proteins are expressed in rat distal pulmonary arterial smooth muscle. Am J Physiol 286:L848-L858.
50. Bird RB, WES, Lightfoot EN (1960) Transport Phenomena (Wiley, New York), pp 42-51.
51. Suzuki M, Mizuno A, Kodaira K, Imai M (2003) Impaired pressure sensation in mice lacking TRPV4. J Biol Chem 278:22664-22668.