Changes in endothelial connexin 43 expression inversely correlate with microvessel permeability and VE-cadherin expression in endotoxin-challenged lungs

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 309, Issue 6, 2015, Pages L584-L592

  Kandasamy, Kathirvel ^a   Escue, Rachel ^a   Manna, Jayeeta ^a   Adebiyi, Adebowale ^a   Parthasarathi, Kaushik ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Ca2+ communication; Connexin 43; Immunofluorescence; Rat; Short hairpin RNA; Uncaging; Vascular endothelial cadherin

Indexed keywords

CALCIUM ION; CONNEXIN 43; ENDOTOXIN; SHORT HAIRPIN RNA; VASCULAR ENDOTHELIAL CADHERIN; CADHERIN; CXCL2 CHEMOKINE; CXCL2 PROTEIN, MOUSE; GJA1 PROTEIN, MOUSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LEUKOCYTE ANTIGEN; LIPOPOLYSACCHARIDE; STAT1 PROTEIN; STAT1 PROTEIN, MOUSE;

ACUTE LUNG INJURY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; LUNG BLOOD VESSEL; LUNG CAPILLARY; LUNG PARENCHYMA; LUNG VEIN; MALE; MICROVASCULATURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; VENULE; ANGIOGENESIS; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CAPILLARY PERMEABILITY; CELL CULTURE; CELL MOTION; CELL PROLIFERATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; LUNG; METABOLISM; SIGNAL TRANSDUCTION; VASCULARIZATION;

ANIMALS; ANTIGENS, CD; CADHERINS; CAPILLARY PERMEABILITY; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CHEMOKINE CXCL2; CONNEXIN 43; LIPOPOLYSACCHARIDES; LUNG; MICE, INBRED C57BL; MICROVESSELS; NEOVASCULARIZATION, PHYSIOLOGIC; NF-KAPPA B; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR;

EID: 84941754215     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00211.2014     Document Type: Article

References (39)

1. Altemeier WA, Matute-Bello G, Gharib SA, Glenny RW, Martin TR, Liles WC. Modulation of lipopolysaccharide-induced gene transcription and promotion of lung injury by mechanical ventilation. J Immunol 175: 3369–3376, 2005.
2. Bhattacharya J, Matthay MA. Regulation and repair of the alveolarcapillary barrier in acute lung injury. Annu Rev Physiol 75: 593–615, 2013.
3. Birukova AA, Tian X, Tian Y, Higginbotham K, Birukov KG. Rapafadin axis in control of Rho signaling and endothelial barrier recovery. Mol Biol Cell 24: 2678–2688, 2013.
4. Bogatcheva NV, Zemskova MA, Kovalenkov Y, Poirier C, Verin AD. Molecular mechanisms mediating protective effect of cAMP on lipopolysaccharide (LPS)-induced human lung microvascular endothelial cells (HLMVEC) hyperpermeability. J Cell Physiol 221: 750–759, 2009.
5. Chatterjee A, Snead C, Yetik-Anacak G, Antonova G, Zeng J, Catravas JD. Heat shock protein 90 inhibitors attenuate LPS-induced endothelial hyperpermeability. Am J Physiol Lung Cell Mol Physiol 294: L755-L763, 2008.
6. Chava KR, Tauseef M, Sharma T, Mehta D. Cyclic AMP response element-binding protein prevents endothelial permeability increase through transcriptional controlling p190RhoGAP expression. Blood 119: 308–319, 2012.
7. Corada M, Zanetta L, Orsenigo F, Breviario F, Lampugnani MG, Bernasconi S, Liao F, Hicklin DJ, Bohlen P, Dejana E. A monoclonal antibody to vascular endothelial-cadherin inhibits tumor angiogenesis without side effects on endothelial permeability. Blood 100: 905–911, 2002.
8. Cruciani V, Mikalsen SO. Stimulated phosphorylation of intracellular connexin43. Exp Cell Res 251: 285–298, 1999.
9. Di Lorenzo A, Lin MI, Murata T, Landskroner-Eiger S, Schleicher M, Kothiya M, Iwakiri Y, Yu J, Huang PL, Sessa WC. eNOS-derived nitric oxide regulates endothelial barrier function through VE-cadherin and Rho GTPases. J Cell Sci 126: 5541–5552, 2013.
10. Giannotta M, Trani M, Dejana E. VE-cadherin and endothelial adherens junctions: active guardians of vascular integrity. Dev Cell 26: 441–454, 2013.
11. Grigoryev DN, Ma SF, Irizarry RA, Ye SQ, Quackenbush J, Garcia JG. Orthologous gene-expression profiling in multi-species models: search for candidate genes. Genome Biol 5: R34, 2004.
12. Grinnell KL, Chichger H, Braza J, Duong H, Harrington EO. Protection against LPS-induced pulmonary edema through the attenuation of protein tyrosine phosphatase-1B oxidation. Am J Respir Cell Mol Biol 46: 623–632, 2012.
13. Jin LY, Li CF, Zhu GF, Wu CT, Wang J, Yan SF. Effect of siRNA against NF-_B on sepsis-induced acute lung injury in a mouse model. Mol Med Rep 10: 631–637, 2014.
14. Kandasamy K, Bezavada L, Escue RB, Parthasarathi K. Lipopolysaccharide induces endoplasmic store Ca2_-dependent inflammatory responses in lung microvessels. PLoS One 8: e63465, 2013.
15. Kandasamy K, Parthasarathi K. Quantifying single microvessel permeability in isolated blood-perfused rat lung preparation. J Vis Exp 30: e51552, 2014.
16. Kandasamy K, Sahu G, Parthasarathi K. Real-time imaging reveals endothelium-mediated leukocyte retention in LPS-treated lung microvessels. Microvasc Res 83: 323–331, 2012.
17. Knezevic N, Tauseef M, Thennes T, Mehta D. The G protein betagamma subunit mediates reannealing of adherens junctions to reverse endothelial permeability increase by thrombin. J Exp Med 206: 2761–2777, 2009.
18. Komarova Y, Malik AB. Regulation of endothelial permeability via paracellular and transcellular transport pathways. Annu Rev Physiol 72: 463–493, 2010.
19. Liao CK, Jeng CJ, Wang HS, Wang SH, Wu JC. Lipopolysaccharide induces degradation of connexin43 in rat astrocytes via the ubiquitinproteasome proteolytic pathway. PLoS One 8: e79350, 2013.
20. Liu G, Ye X, Miller EJ, Liu SF. NF-αB-to-AP-1 switch: a mechanism regulating transition from endothelial barrier injury to repair in endotoxemic mice. Sci Rep 4: 5543, 2014.
21. Liu SF, Malik AB. NF-αB activation as a pathological mechanism of septic shock and inflammation. Am J Physiol Lung Cell Mol Physiol 290: L622–L645, 2006.
22. Matthay MA, Ware LB, Zimmerman GA. The acute respiratory distress syndrome. J Clin Invest 122: 2731–2740, 2012.
23. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiol Rev 86: 279–367, 2006.
24. Morizono K, Xie Y, Ringpis GE, Johnson M, Nassanian H, Lee B, Wu L, Chen IS. Lentiviral vector retargeting to P-glycoprotein on metastatic melanoma through intravenous injection. Nat Med 11: 346–352, 2005.
25. O’Donnell JJ III, Birukova AA, Beyer EC, Birukov KG. Gap junction protein connexin43 exacerbates lung vascular permeability. PLoS One 9: e100931, 2014.
26. Parthasarathi K. Endothelial connexin43 mediates acid-induced increases in pulmonary microvascular permeability. Am J Physiol Lung Cell Mol Physiol 303: L33–L42, 2012.
27. Parthasarathi K, Bhattacharya J. Localized acid instillation by a wedged-catheter method reveals a role for vascular gap junctions in spatial expansion of acid injury. Anat Rec (Hoboken) 94: 1585–1591, 2011.
28. Parthasarathi K, Ichimura H, Monma E, Lindert J, Quadri S, Issekutz A, Bhattacharya J. Connexin 43 mediates spread of Ca2α-dependent proinflammatory responses in lung capillaries. J Clin Invest 116: 2193–2200, 2006.
29. Rahman A, Fazal F. Blocking NF-αB: an inflammatory issue. Proc Am Thorac Soc 8: 497–503, 2011.
30. Rajput C, Kini V, Smith M, Yazbeck P, Chavez A, Schmidt T, Zhang W, Knezevic N, Komarova Y, Mehta D. Neural Wiskott-Aldrich syndrome protein (N-WASP)-mediated p120-catenin interaction with Arp2- Actin complex stabilizes endothelial adherens junctions. J Biol Chem 288: 4241–4250, 2013.
31. Sawant DA, Tharakan B, Hunter FA, Smythe WR, Childs EW. Role of -catenin in regulating microvascular endothelial cell hyperpermeability. J Trauma 70: 481–487; discussion 487–488, 2011.
32. Schulte D, Kuppers V, Dartsch N, Broermann A, Li H, Zarbock A, Kamenyeva O, Kiefer F, Khandoga A, Massberg S, Vestweber D. Stabilizing the VE-cadherin-catenin complex blocks leukocyte extravasation and vascular permeability. EMBO J 30: 4157–4170, 2011.
33. Setyawati MI, Tay CY, Chia SL, Goh SL, Fang W, Neo MJ, Chong HC, Tan SM, Loo SC, Ng KW, Xie JP, Ong CN, Tan NS, Leong DT. Titanium dioxide nanomaterials cause endothelial cell leakiness by disrupting the homophilic interaction of VE-cadherin. Nat Commun 4: 1673, 2013.
34. Severgnini M, Takahashi S, Tu P, Perides G, Homer RJ, Jhung JW, Bhavsar D, Cochran BH, Simon AR. Inhibition of the Src and Jak kinases protects against lipopolysaccharide-induced acute lung injury. Am J Respir Crit Care Med 171: 858–867, 2005.
35. Vincent PA, Xiao K, Buckley KM, Kowalczyk AP. VE-cadherin: adhesion at arm’s length. Am J Physiol Cell Physiol 286: C987–C997, 2004.
36. Wei CJ, Francis R, Xu X, Lo CW. Connexin43 associated with an N-cadherin-containing multiprotein complex is required for gap junction formation in NIH3T3 cells. J Biol Chem 280: 19925–19936, 2005.
37. Wu X, Huang W, Luo G, Alain LA. Hypoxia induces connexin 43 dysregulation by modulating matrix metalloproteinases via MAPK signaling. Mol Cell Biochem 384: 155–162, 2013.
38. Yeh HI, Rothery S, Dupont E, Coppen SR, Severs NJ. Individual gap junction plaques contain multiple connexins in arterial endothelium. Circ Res 83: 1248–1263, 1998.
39. Zhang Y, Jiang G, Sauler M, Lee PJ. Lung endothelial HO-1 targeting in vivo using lentiviral miRNA regulates apoptosis and autophagy during oxidant injury. FASEB J 27: 4041–4058, 2013.