Gap junction protein connexin43 exacerbates lung vascular permeability

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  O'Donnell III, James J ^a   Birukova, Anna A ^a   Beyer, Eric C ^a   Birukov, Konstantin G ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBENOXOLONE; CONNEXIN 43; LIPOPOLYSACCHARIDE; LUCIFER YELLOW; MESSENGER RNA; MYOSIN LIGHT CHAIN; PLACEBO; SMALL INTERFERING RNA; THROMBIN; AUTACOID;

ARTICLE; BLOOD VESSEL PERMEABILITY; CELL COMMUNICATION; CELL ELONGATION; CONTROLLED STUDY; CX43 GENE; DOWN REGULATION; DRUG TARGETING; ENDOTHELIUM CELL; GENE; GENE EXPRESSION REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; INFLAMMATION; LUNG BLOOD VESSEL; LUNG ENDOTHELIUM; MICROVASCULAR ENDOTHELIAL CELL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION; CAPILLARY PERMEABILITY; CELL LINE; DRUG EFFECTS; GAP JUNCTION; GENE EXPRESSION; GENETICS; INTRACELLULAR SPACE; LUNG; LUNG ALVEOLUS CELL; METABOLISM; PHOSPHORYLATION;

CAPILLARY PERMEABILITY; CARBENOXOLONE; CELL LINE; CONNEXIN 43; ENDOTHELIAL CELLS; GAP JUNCTIONS; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; HUMANS; INFLAMMATION MEDIATORS; INTRACELLULAR SPACE; LIPOPOLYSACCHARIDES; LUNG; MYOSIN LIGHT CHAINS; PHOSPHORYLATION; PNEUMOCYTES; RNA, SMALL INTERFERING; THROMBIN;

EID: 84903388363     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100931     Document Type: Article

References (45)

1. Agrawal A, Zhuo H, Brady S, Levitt J, Steingrub J, et al. (2012) Pathogenetic and predictive value of biomarkers in patients with ALI and lower severity of illness: results from two clinical trials. Am J Physiol Lung Cell Mol Physiol 303: L634-L639. ajplung.00195.2012 [pii];10.1152/ajplung.00195.2012 [doi].
2. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, et al. (2001) Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 29: 1303-1310. (Pubitemid 32641789)
3. Birukov KG, Zebda N, Birukova AA (2013) Barrier enhancing signals in pulmonary edema. Compr Physiol 3: 429-484. 10.1002/cphy.c100066 [doi].
4. Ziliene V, Reingardiene D, Tereseviciute N, Slavinskas R (2004) [Diagnosis of acute respiratory failure and nosocomial pneumonia]. Medicina (Kaunas) 40: 1124-1129. 0411-12 [pii].
5. Davey A, McAuley DF, O'Kane CM (2011) Matrix metalloproteinases in acute lung injury: mediators of injury and drivers of repair. Eur Respir J 38: 959-970. 09031936.00032111 [pii];10.1183/09031936.00032111 [doi].
6. Lucas R, Verin AD, Black SM, Catravas JD (2009) Regulators of endothelial and epithelial barrier integrity and function in acute lung injury. Biochem Pharmacol 77: 1763-1772. S0006-2952(09)00049-5 [pii];10.1016/j.bcp.2009.01.014 [doi].
7. Zhou X, Dai Q, Huang X (2012) Neutrophils in acute lung injury. Front Biosci (Landmark Ed) 17: 2278-2283. 4051 [pii].
8. Lum H, Malik AB (1994) Regulation of vascular endothelial barrier function. Am J Physiol 267: L223-L241.
9. Mehta D, Malik AB (2006) Signaling mechanisms regulating endothelial permeability. Physiol Rev 86: 279-367. 86/1/279 [pii];10.1152/physrev. 00012.2005 [doi].
10. Yeager M, Harris AL (2007) Gap junction channel structure in the early 21st century: facts and fantasies. Curr Opin Cell Biol 19: 521-528. S0955- 0674(07)00123-8 [pii];10.1016/j.ceb.2007.09.001 [doi].
11. Kwak BR, Veillard N, Pelli G, Mulhaupt F, James RW, et al. (2003) Reduced connexin43 expression inhibits atherosclerotic lesion formation in low-density lipoprotein receptor-deficient mice. Circulation 107: 1033-1039. (Pubitemid 36258728)
12. Wong CW, Christen T, Roth I, Chadjichristos CE, Derouette JP, et al. (2006) Connexin37 protects against atherosclerosis by regulating monocyte adhesion. Nat Med 12: 950-954. nm1441 [pii];10.1038/nm1441 [doi].
13. Chadjichristos CE, Scheckenbach KE, van Veen TA, Richani Sarieddine MZ, de Wit C, et al. (2010) Endothelial-specific deletion of connexin40 promotes atherosclerosis by increasing CD73-dependent leukocyte adhesion. Circulation 121: 123-131. CIRCULATIONAHA.109.867176 [pii];10.1161/CIRCULATIONAHA. 109.867176 [doi].
14. Bastarache JA, Ware LB, Bernard GR (2006) The role of the coagulation cascade in the continuum of sepsis and acute lung injury and acute respiratory distress syndrome. Semin Respir Crit Care Med 27: 365-376. 10.1055/s-2006- 948290 [doi].
15. Birukova AA, Smurova K, Birukov KG, Kaibuchi K, Garcia JG, et al. (2004) Role of Rho GTPases in thrombin-induced lung vascular endothelial cells barrier dysfunction. Microvasc Res 67: 64-77. S0026286203000748 [pii].
16. Birukova AA, Lee S, Starosta V, Wu T, Ho T, et al. (2012) A role for VEGFR2 activation in endothelial responses caused by barrier disruptive OxPAPC concentrations. PLoS One 7: e30957. 10.1371/journal.pone.0030957 [doi];- PONE-D-11-15810 [pii].
17. Birukova AA, Fu P, Chatchavalvanich S, Burdette D, Oskolkova O, et al. (2007) Polar head groups are important for barrier-protective effects of oxidized phospholipids on pulmonary endothelium. Am J Physiol Lung Cell Mol Physiol 292: L924-L935. 00395.2006 [pii];10.1152/ajplung.00395.2006 [doi].
18. Birukova AA, Moldobaeva N, Xing J, Birukov KG (2008) Magnitude-dependent effects of cyclic stretch on HGF- and VEGF-induced pulmonary endothelial remodeling and barrier regulation. Am J Physiol Lung Cell Mol Physiol 295: L612-L623. 90236.2008 [pii];10.1152/ajplung.90236.2008 [doi].
19. Starosta V, Wu T, Zimman A, Pham D, Tian X, et al. (2012) Differential regulation of endothelial cell permeability by high and low doses of oxidized 1- palmitoyl-2-arachidonyl-sn-glycero-3-phosphocholine. Am J Respir Cell Mol Biol 46: 331-341. 2011-0153OC [pii];10.1165/rcmb.2011-0153OC [doi].
20. Birukova AA, Tian Y, Dubrovskyi O, Zebda N, Sarich N, et al. (2012) VE-cadherin trans-interactions modulate Rac activation and enhancement of lung endothelial barrier by iloprost. J Cell Physiol 227: 3405-3416. 10.1002/ jcp.24041 [doi].
21. Birukova AA, Malyukova I, Poroyko V, Birukov KG (2007) Paxillin-beta-catenin interactions are involved in Rac/Cdc42-mediated endothelial barrier-protective response to oxidized phospholipids. Am J Physiol Lung Cell Mol Physiol 293: L199-L211. 00020.2007 [pii];10.1152/ajplung.00020. 2007 [doi].
22. Gemel J, Nelson TK, Burt JM, Beyer EC (2012) Inducible coexpression of connexin37 or connexin40 with connexin43 selectively affects intercellular molecular transfer. J Membr Biol 245: 231-241. 10.1007/s00232-012-9444-4 [doi].
23. Birukova AA, Tian Y, Meliton A, Leff A, Wu T, et al. (2012) Stimulation of Rho signaling by pathologic mechanical stretch is a ''second hit'' to Rho-independent lung injury induced by IL-6. Am J Physiol Lung Cell Mol Physiol 302: L965-L975. ajplung.00292.2011 [pii];10.1152/ajplung.00292.2011 [doi].
24. Meliton AY, Munoz NM, Meliton LN, Birukova AA, Leff AR, et al. (2013) Mechanical induction of group V phospholipase A(2) causes lung inflammation and acute lung injury. Am J Physiol Lung Cell Mol Physiol 304: L689-L700. ajplung.00047.2013 [pii];10.1152/ajplung.00047.2013 [doi].
25. Birukov KG, Jacobson JR, Flores AA, Ye SQ, Birukova AA, et al. (2003) Magnitude-dependent regulation of pulmonary endothelial cell barrier function by cyclic stretch. Am J Physiol Lung Cell Mol Physiol 285: L785-L797. 10.1152/ajplung.00336.2002 [doi];00336.2002 [pii].
26. Birukova AA, Chatchavalvanich S, Rios A, Kawkitinarong K, Garcia JG, et al. (2006) Differential regulation of pulmonary endothelial monolayer integrity by varying degrees of cyclic stretch. Am J Pathol 168: 1749-1761. S0002- 9440(10)62195-5 [pii];10.2353/ajpath.2006.050431 [doi].
27. Juszczak GR, Swiergiel AH (2009) Properties of gap junction blockers and their behavioural, cognitive and electrophysiological effects: animal and human studies. Prog Neuropsychopharmacol Biol Psychiatry 33: 181-198. S0278-5846(08)00398-9 [pii];10.1016/j.pnpbp.2008.12.014 [doi].
28. Larson DM, Haudenschild CC, Beyer EC (1990) Gap junction messenger RNA expression by vascular wall cells. Circ Res 66: 1074-1080. (Pubitemid 20126437)
29. Fernandez-Cobo M, Gingalewski C, De MA (1998) Expression of the connexin 43 gene is increased in the kidneys and the lungs of rats injected with bacterial lipopolysaccharide. Shock 10: 97-102. (Pubitemid 128463840)
30. Sarieddine MZ, Scheckenbach KE, Foglia B, Maass K, Garcia I, et al. (2009) Connexin43 modulates neutrophil recruitment to the lung. J Cell Mol Med 13: 4560-4570.
31. Fernandez-Cobo M, Gingalewski C, Drujan D, De MA (1999) Downregulation of connexin 43 gene expression in rat heart during inflammation. The role of tumour necrosis factor. Cytokine 11: 216-224. S1043-4666(98)90422-7 [pii];10.1006/cyto.1998.0422 [doi].
32. Jara PI, Boric MP, Saez JC (1995) Leukocytes express connexin 43 after activation with lipopolysaccharide and appear to form gap junctions with endothelial cells after ischemia-reperfusion. Proc Natl Acad Sci U S A 92: 7011- 7015.
33. Bolon ML, Kidder GM, Simon AM, Tyml K (2007) Lipopolysaccharide reduces electrical coupling in microvascular endothelial cells by targeting connexin40 in a tyrosine-, ERK1/2-, PKA-, and PKC-dependent manner. J Cell Physiol 211: 159-166. (Pubitemid 46363905)
34. Tyml K (2011) Role of connexins in microvascular dysfunction during inflammation. Can J Physiol Pharmacol 89: 1-12.
35. Rignault S, Haefliger JA, Waeber B, Liaudet L, Feihl F (2007) Acute inflammation decreases the expression of connexin 40 in mouse lung. Shock 28: 78-85. (Pubitemid 46956467)
36. Baker SM, Kim N, Gumpert AM, Segretain D, Falk MM (2008) Acute internalization of gap junctions in vascular endothelial cells in response to inflammatory mediator-induced G-protein coupled receptor activation. FEBS Lett 582: 4039-4046. S0014-5793(08)00875-2 [pii];10.1016/j.febslet. 2008.10.043 [doi].
37. De Vuyst E, Decrock E, De Bock M, Yamasaki H, Naus CC, et al. (2007) Connexin hemichannels and gap junction channels are differentially influenced by lipopolysaccharide and basic fibroblast growth factor. Mol Biol Cell 18: 34- 46.
38. Seminario-Vidal L, Kreda S, Jones L, O'Neal W, Trejo J, et al. (2009) Thrombin promotes release of ATP from lung epithelial cells through coordinated activation of rho- and Ca2 +-dependent signaling pathways. J Biol Chem 284: 20638-20648. M109.004762 [pii];10.1074/jbc.M109.004762 [doi].
39. Salameh A, Dhein S (2013) Effects of mechanical forces and stretch on intercellular gap junction coupling. Biochim Biophys Acta 1828: 147-156. S0005-2736(11)00467-6 [pii];10.1016/j.bbamem.2011.12.030 [doi].
40. Parthasarathi K, Ichimura H, Monma E, Lindert J, Quadri S, et al. (2006) Connexin 43 mediates spread of Ca2+-dependent proinflammatory responses in lung capillaries. J Clin Invest 116: 2193-2200. 10.1172/JCI26605 [doi]. (Pubitemid 44162328)
41. Parthasarathi K (2012) Endothelial connexin43 mediates acid-induced increases in pulmonary microvascular permeability. Am J Physiol Lung Cell Mol Physiol 303: L33-L42. ajplung.00219.2011 [pii];10.1152/ajplung.00219.2011 [doi].
42. Nagasawa K, Chiba H, Fujita H, Kojima T, Saito T, et al. (2006) Possible involvement of gap junctions in the barrier function of tight junctions of brain and lung endothelial cells. J Cell Physiol 208: 123-132. 10.1002/jcp.20647 [doi]. (Pubitemid 43848996)
43. Harris AL (2007) Connexin channel permeability to cytoplasmic molecules. Prog Biophys Mol Biol 94: 120-143. S0079-6107(07)00007-7 [pii];10.1016/j. pbiomolbio. 2007.03.011 [doi].
44. Lim PK, Bliss SA, Patel SA, Taborga M, Dave MA, et al. (2011) Gap junction-mediated import of microRNA from bone marrow stromal cells can elicit cell cycle quiescence in breast cancer cells. Cancer Res 71: 1550-1560. 0008-5472.CAN-10-2372 [pii];10.1158/0008-5472.CAN-10-2372 [doi].
45. Harris AL (2001) Emerging issues of connexin channels: biophysics fills the gap. Q Rev Biophys 34: 325-472.