Septin-2 mediates airway epithelial barrier function in physiologic and pathologic conditions

American Journal of Respiratory Cell and Molecular Biology

Volumn 45, Issue 1, 2011, Pages 120-126

  Sidhaye, Venkataramana K ^a   Chau, Eric ^a   Breysse, Patrick N ^b   King, Landon S ^a  

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

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Actin cytoskeleton; Epithelial barrier function; Paracellular permeability; Septin 2

Indexed keywords

ACTIN; EPIDERMAL GROWTH FACTOR; SEPTIN; SEPTIN 2; UNCLASSIFIED DRUG;

ARTICLE; CELL PERMEABILIZATION; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; PARTICULATE MATTER; PERMEABILITY BARRIER; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; RESPIRATORY EPITHELIUM; SHEAR STRESS; SIGNAL TRANSDUCTION; STIMULUS RESPONSE;

ACTINS; ANIMALS; CELL LINE; CELL MEMBRANE; DOGS; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; PROTEIN TRANSPORT; RESPIRATORY MUCOSA; SEPTINS; SIGNAL TRANSDUCTION;

EID: 80051562608     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2010-0235OC     Document Type: Article

References (47)

1. Anderson JM, Van Itallie CM. Tight junctions and the molecular basis for regulation of paracellular permeability. Am J Physiol 1995;269:G467-G475.
2. Youakim A, Ahdieh M. Interferon-gamma decreases barrier function in T84 cells by reducing ZO-1 levels and disrupting apical actin. Am J Physiol 1999;276:G1279-G1288. (Pubitemid 29251928)
3. Nusrat A, Madara JL. Rho protein regulates tight junctions and perijunctional actin organization in polarized epithelia. Proc Natl Acad Sci USA 1995;92:10629-10633.
4. Nusrat A, Madara JL. Modulation of intercellular junctions of epithelia by scatter factor (hepatocyte growth factor). EXS 1995;74:69-87.
5. Garcia JG, Liu F, Verin AD, Birukova A, Dechert MA, Gerthoffer WT, Bamberg JR, English D. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest 2001;108:689-701. (Pubitemid 32906197)
6. Liu F, Schaphorst KL, Verin AD, Jacobs K, Birukova A, Day RM, Bogatcheva N, Bottaro DP, Garcia JG. Hepatocyte growth factor enhances endothelial cell barrier function and cortical cytoskeletal rearrangement: potential role of glycogen synthase kinase-3beta. FASEB J 2002;16:950-962. (Pubitemid 34753501)
7. Fanning AS, Ma TY, Anderson JM. Isolation and functional characterization of the actin binding region in the tight junction protein ZO-1. FASEB J 2002;16:1835-1837.
8. Longtine MS, Bi E. Regulation of septin organization and function in yeast. Trends Cell Biol 2003;13:403-409. (Pubitemid 36897644)
9. Schmidt K, Nichols BJ. Functional interdependence between septin and actin cytoskeleton. BMC Cell Biol 2004;5:43.
10. Kim SK, Shindo A, Park TJ, Oh EC, Ghosh S, Gray RS, Lewis RA, Johnson CA, Attie-Bittach T, Katsanis N, Wallingford JB. Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science 2010;329:1337-1340.
11. Larisch S, Yi Y, Lotan R, Kerner H, Eimerl S, Tony Parks W, Gottfried Y, Birkey Reffey S, de Caestecker MP, Danielpour D, Book-Melamed N, et al. A novel mitochondrial septin-like protein, ARTS, mediates apoptosis dependent on its P-loop motif. Nat Cell Biol 2000;2:915-921.
12. Sidhaye V, Schweitzer K, Caterina MJ, Shimoda LA, King LS. Shear stress regulates AQP5 and airway epithelial barrier function. Proc Natl Acad Sci U S A 2008;105:3345-3350. (Pubitemid 351723555)
13. Dimmeler S, Haendeler J, Rippmann V, Nehls M, Zeiher AM. Shear stress inhibits apoptosis of human endothelial cells. FEBS Lett 1996;399:71-74. (Pubitemid 27007954)
14. Dudek SM, Jacobson JR, Chiang ET, Birukov KG, Wang P, Zhan X, Garcia JG. Pulmonary endothelial cell barrier enhancement by sphingosine 1-phosphate: roles for cortactin and myosin light chain kinase. J Biol Chem 2004;279:24692-24700. (Pubitemid 38725337)
15. Sidhaye V, Hoffert JD, King LS. cAMP has distinct acute and chronic effects on aquaporin-5 in lung epithelial cells. J Biol Chem 2005;280:3590-3596. (Pubitemid 40223825)
16. Herrlich A, Leitch V, King LS. Role of proneuregulin 1 cleavage and human epidermal growth factor receptor activation in hypertonic aquaporin induction. Proc Natl Acad Sci USA 2004;101:15799-15804. (Pubitemid 39473568)
17. Wang T, Chiang ET, Moreno-Vinasco L, Lang GD, Pendyala S, Samet JM, Geyh AS, Breysse PN, Chillrud SN, Natarajan V, Garcia JG. Particulate matter disrupts human lung endothelial barrier integrity via ROS- and p38 MAPK-dependent pathways. Am J Respir Cell Mol Biol 2010;42:442-449.
18. Williams MA, Rangasamy T, Bauer SM, Killedar S, Karp M, Kensler TM, Yamamoto M, Breysse P, Biswal S, Georas SN. Disruption of the transcription factor Nrf2 promotes pro-oxidative dendritic cells that stimulate Th2-like immunoresponsiveness upon activation by ambient particulate matter. J Immunol 2008;181:4545-4559.
19. Arce FT, Whitlock JL, Birukova AA, Birukov KG, Arnsdorf MG, Lal R, Garcia JG, Dudek SM. Regulation of the micromechanical properties of pulmonary endothelium by S1P and thrombin: role of cortactin. Biophys J 2008;95:886-894.
20. Birukov KG, Birukova AA, Dudek SM, Verin Ad, Crow MT, Zhan X, DePaola N, Garcia JG. Shear stress-mediated cytoskeletal remodeling and cortactin translocation in pulmonary endothelial cells. Am J Respir Cell Mol Biol 2002;26:453-464. (Pubitemid 34253930)
21. Birukova AA, Arce AA, Moldobaeva N, Dudek SM, Garcia JG, Lal R, Birukov KG. Endothelial permeability is controlled by spatially defined cytoskeletal mechanics: atomic force microscopy force mapping of pulmonary endothelial monolayer. Nanomedicine 2009;5:30-41.
22. Brown MD, Adyshev D, Bindokas V, Moitra J, Garcia JG, Dudek SM, et al. Quantitative distribution and colocalization of non-muscle myosin light chain kinase isoforms and cortactin in human lung endothelium. Microvasc Res 2010;80:75-88.
23. Chiang ET, Camp SM, Dudek SM, Brown ME, Usatyuk PV, Zaborina O, Alverdy JC, Garcia JG. Protective effects of high-molecular weight polyethylene glycol (PEG) in human lung endothelial cell barrier regulation: role of actin cytoskeletal rearrangement. Microvasc Res 2009;77:174-186.
24. Dudek SM, Camp SM, Chiang ET, Singleton PA, Usatyuk PV, Zhao Y, Natarajan V, Garcia JG. Pulmonary endothelial cell barrier enhancement by FTY720 does not require the S1P1 receptor. Cell Signal 2007;19:1754-1764. (Pubitemid 46935431)
25. Dudek SM, Garcia JG. Cytoskeletal regulation of pulmonary vascular permeability. J Appl Physiol 2001;91:1487-1500. (Pubitemid 32900340)
26. Finigan JH, Dudek SM, Singleton PA, Chiang ET, Jacobson JR, Camp SM, Ye SQ, Garcia JG. Activated protein C mediates novel lung endothelial barrier enhancement: role of sphingosine 1-phosphate receptor transactivation. J Biol Chem 2005;280:17286-17293. (Pubitemid 41389197)
27. Jacobson JR, Dudek SM, Birukov KG, Ye SQ, Grigoryev DN, Girgis RE, Garcia JG. Cytoskeletal activation and altered gene expression in endothelial barrier regulation by simvastatin. Am J Respir Cell Mol Biol 2004;30:662-670. (Pubitemid 38591217)
28. Jacobson JR, Dudek SM, Singleton PA, Kolosova IA, Verin AD, Garcia JG. Endothelial cell barrier enhancement by ATP is mediated by the small GTPase Rac and cortactin. Am J Physiol Lung Cell Mol Physiol 2006;291:L289-L295. (Pubitemid 44148114)
29. Ma SF, Flores C, Wade MS, Dudek SM, Nicolae DL, Ober C, Garcia JG. A common cortactin gene variation confers differential susceptibility to severe asthma. Genet Epidemiol 2008;32:757-766.
30. Singleton PA, Dudek SM, Chiang ET, Garcia JG. Regulation of sphingosine 1-phosphate-induced endothelial cytoskeletal rearrangement and barrier enhancement by S1P1 receptor, PI3 kinase, Tiam1/Rac1, and alpha-actinin. FASEB J 2005;19:1646-1656. (Pubitemid 41429522)
31. Singleton PA, Dudek SM, Ma SF, Garcia JG. Transactivation of sphingosine 1-phosphate receptors is essential for vascular barrier regulation: novel role for hyaluronan and CD44 receptor family. J Biol Chem 2006;281:34381-34393. (Pubitemid 46036646)
32. Usatyuk PV, Romer LH, He D, Parinandi NL, Kleinberg ME, Zhan S, Jacobson JR, Dudek SM, Pendyala S, Garcia JG, et al. Regulation of hyperoxia-induced NADPH oxidase activation in human lung endothelial cells by the actin cytoskeleton and cortactin. J Biol Chem 2007;282:23284-23295. (Pubitemid 47311961)
33. Wang L, Dudek SM. Regulation of vascular permeability by sphingosine 1-phosphate. Microvasc Res 2009;77:39-45.
34. Hu Q, Nelson WJ, Spiliotis ET. Forchlorfenuron alters mammalian septin assembly, organization, and dynamics. J Biol Chem 2008;283:29563-29571.
35. Humlicek AL, Manzel LJ, Chin CL, Shi L, Excoffon KJ, Winter MC, Shasby DM, Look DC. Paracellular permeability restricts airway epithelial responses to selectively allow activation by mediators at the basolateral surface. J Immunol 2007;178:6395-6403. (Pubitemid 46717423)
36. Saunders V, Breysse P, Clark J, Sproles A, Davila M, Wills-Karp M. Particulate matter induced airway hyperresponsiveness is lymphocyte dependent. Environ Health Perspect 2010;118:640-646.
37. Zhao Y, Usatyuk PV, Gorshkova IA, He D, Wang T, Moreno-Vinasco L, Geyh AS, Breysse PN, Samet JM, Spannhake EW, et al. Regulation of COX-2 expression and IL-6 release by particulate matter in airway epithelial cells. Am J Respir Cell Mol Biol 2009;40:19-30.
38. Wang T, Moreno-Vinaasco L, Huang Y, Lang GD, Linares JD, Goonwardena SN, Grabavoy A, Samet JM, Geyh AS, Breysse PN, et al. Murine lung responses to ambient particulate matter: genomic analysis and influence on airway hyperresponsiveness. Environ Health Perspect 2008;116:1500-1508.
39. Gabrielson EW, Yu XY, Spannhake EW. Comparison of the toxic effects of hydrogen peroxide and ozone on cultured human bronchial epithelial cells. Environ Health Perspect 1994;102:972-974.
40. Yu XY, Schofield BH, Croxton T, Takahashi N, Gabrielson EW, Spannhake EW. Physiologic modulation of bronchial epithelial cell barrier function by polycationic exposure. Am J Respir Cell Mol Biol 1994;11:188-198.
41. Yu XY, Takahashi N, Croxton TL, Spannhake EW. Modulation of bronchial epithelial cell barrier function by in vitro ozone exposure. Environ Health Perspect 1994;102:1068-1072.
42. Rothen-Rutishauser B, Blank F, Muhlfeld C, Gehr P. In vitro models of the human epithelial airway barrier to study the toxic potential of particulate matter. Expert Opin Drug Metab Toxicol 2008;4:1075-1089.
43. Winter MC, Shasby SS, Ries DR, Shasby DM. PAR2 activation interrupts E-cadherin adhesion and compromises the airway epithelial barrier: protective effect of beta-agonists. Am J Physiol Lung Cell Mol Physiol 2006;291:L628-L635. (Pubitemid 44498473)
44. Vermeer PD, Einwalter LA, Moninger TO, Rokhlina T, Kern JA, Zabner J, Welsh MJ. Segregation of receptor and ligand regulates activation of epithelial growth factor receptor. Nature 2003;422:322-326. (Pubitemid 36378360)
45. Kremer BE, Adang LA, Macara IG. Septins regulate actin organization and cell-cycle arrest through nuclear accumulation of NCK mediated by SOCS7. Cell 2007;130:837-850. (Pubitemid 47332569)
46. Krause JE, Chenard BL, Cortright DN. Transient receptor potential ion channels as targets for the discovery of pain therapeutics. Curr Opin Investig Drugs 2005;6:48-57.
47. Green AS. Modelling of peak-flow wall shear stress in major airways of the lung. J Biomech 2004;37:661-667. (Pubitemid 38445028)