1,725
Views
31
CrossRef citations to date
0
Altmetric
Review

Lipid mediators in the regulation of endothelial barriers

&
Article: e1385573 | Received 14 Aug 2017, Accepted 22 Sep 2017, Published online: 30 Oct 2017

References

  • Kim JA, Montagnani M, Chandrasekran S, Quon MJ. Role of lipotoxicity in endothelial dysfunction. Heart Fail Clin. 2012;8:589–607. doi:10.1016/j.hfc.2012.06.012. PMID:22999242.
  • Berg AH, Scherer PE. Adipose tissue, inflammation, and cardiovascular disease. Circ Res. 2005;96:939–49. doi:10.1161/01.RES.0000163635.62927.34. PMID:15890981.
  • Steinberg HO, Chaker H, Leaming R, Johnson A, Brechtel G, Baron AD. Obesity/insulin resistance is associated with endothelial dysfunction. Implications for the syndrome of insulin resistance. J Clin Invest. 1996;97:2601–10. doi:10.1172/JCI118709. PMID:8647954.
  • Berliner JA, Gharavi NM. Endothelial cell regulation by phospholipid oxidation products. Free Radic Biol Med. 2008;45:119–23. doi:10.1016/j.freeradbiomed.2008.04.013. PMID:18460347.
  • Lee S, Birukov KG, Romanoski CE, Springstead JR, Lusis AJ, Berliner JA. Role of phospholipid oxidation products in atherosclerosis. Circ Res. 2012;111:778–99. doi:10.1161/CIRCRESAHA.111.256859. PMID:22935534.
  • Bochkov VN, Oskolkova OV, Birukov KG, Levonen AL, Binder CJ, Stockl J. Generation and biological activities of oxidized phospholipids. Antioxid Redox Signaling. 2010;12:1009–59. doi:10.1089/ars.2009.2597.
  • Bochkov V, Gesslbauer B, Mauerhofer C, Philippova M, Erne P, Oskolkova OV. Pleiotropic effects of oxidized phospholipids. Free Radic Biol Med. 2016;111:6–24. doi:10.1016/j.freeradbiomed.2016.12.034. PMID:28027924.
  • Zebda N, Tian Y, Tian X, Gawlak G, Higginbotham K, Reynolds AB, Birukova AA, Birukov KG. Interaction of p190RhoGAP with C-terminal domain of p120-catenin modulates endothelial cytoskeleton and permeability. J Biol Chem. 2013;288:18290–9. doi:10.1074/jbc.M112.432757. PMID:23653363.
  • Garcia-Ponce A, Citalan-Madrid AF, Velazquez-Avila M, Vargas-Robles H, Schnoor M. The role of actin-binding proteins in the control of endothelial barrier integrity. Thromb Haemost. 2015;113:20–36. doi:10.1160/TH14-04-0298. PMID:25183310.
  • Spindler V, Schlegel N, Waschke J. Role of GTPases in control of microvascular permeability. Cardiovasc Res. 2010;87:243–53. doi:10.1093/cvr/cvq086. PMID:20299335.
  • Trani M, Dejana E. New insights in the control of vascular permeability: vascular endothelial-cadherin and other players. Curr Opin Hematol. 2015;22:267–72. doi:10.1097/MOH.0000000000000137. PMID:25767951.
  • Oldenburg J, de Rooij J. Mechanical control of the endothelial barrier. Cell Tissue Res. 2014;355:545–55. doi:10.1007/s00441-013-1792-6. PMID:24519624.
  • Vandenbroucke E, Mehta D, Minshall R, Malik AB. Regulation of endothelial junctional permeability. Ann N Y Acad Sci. 2008;1123:134–45. doi:10.1196/annals.1420.016. PMID:18375586.
  • van Nieuw Amerongen GP, van Delft S, Vermeer MA, Collard JG, van Hinsbergh VW. Activation of RhoA by thrombin in endothelial hyperpermeability: role of Rho kinase and protein tyrosine kinases. Circ Res. 2000;87:335–40. doi:10.1161/01.RES.87.4.335. PMID:10948069.
  • Kumar P, Shen Q, Pivetti CD, Lee ES, Wu MH, Yuan SY. Molecular mechanisms of endothelial hyperpermeability: implications in inflammation. Expert Rev Mol Med. 2009;11:e19. doi:10.1017/S1462399409001112. PMID:19563700.
  • Wang L, Dudek SM. Regulation of vascular permeability by sphingosine 1-phosphate. Microvasc Res. 2009;77:39–45. doi:10.1016/j.mvr.2008.09.005. PMID:18973762.
  • Worthylake RA, Burridge K. RhoA and ROCK promote migration by limiting membrane protrusions. J Biol Chem. 2003;278:13578–84. doi:10.1074/jbc.M211584200. PMID:12574166.
  • Bustos RI, Forget MA, Settleman JE, Hansen SH. Coordination of Rho and Rac GTPase function via p190B RhoGAP. Curr Biol. 2008;18:1606–11. doi:10.1016/j.cub.2008.09.019. PMID:18948007.
  • Birukova AA, Tian X, Tian Y, Higginbotham K, Birukov KG. Rap-afadin axis in control of Rho signaling and endothelial barrier recovery. Mol Biol Cell. 2013;24:2678–88. doi:10.1091/mbc.E13-02-0098. PMID:23864716.
  • Birukova AA, Zagranichnaya T, Fu P, Alekseeva E, Chen W, Jacobson JR, Birukov KG. Prostaglandins PGE(2) and PGI(2) promote endothelial barrier enhancement via PKA- and Epac1/Rap1-dependent Rac activation. Exp Cell Res. 2007;313:2504–20. doi:10.1016/j.yexcr.2007.03.036. PMID:17493609.
  • Zhang C. The role of inflammatory cytokines in endothelial dysfunction. Basic Res Cardiol. 2008;103:398–406. doi:10.1007/s00395-008-0733-0. PMID:18600364.
  • Pober JS, Sessa WC. Evolving functions of endothelial cells in inflammation. Nat Rev Immunol. 2007;7:803–15. doi:10.1038/nri2171. PMID:17893694.
  • DiStasi MR, Ley K. Opening the flood-gates: how neutrophil-endothelial interactions regulate permeability. Trends Immunol. 2009;30:547–56. doi:10.1016/j.it.2009.07.012. PMID:19783480.
  • Clark PR, Manes TD, Pober JS, Kluger MS. Increased ICAM-1 expression causes endothelial cell leakiness, cytoskeletal reorganization and junctional alterations. J Invest Dermatol. 2007;127:762–74. doi:10.1038/sj.jid.5700670. PMID:17195014.
  • Cook-Mills JM, Marchese ME, Abdala-Valencia H. Vascular cell adhesion molecule-1 expression and signaling during disease: regulation by reactive oxygen species and antioxidants. Antioxid Redox Signaling. 2011;15:1607–38. doi:10.1089/ars.2010.3522.
  • Wessel F, Winderlich M, Holm M, Frye M, Rivera-Galdos R, Vockel M, Linnepe R, Ipe U, Stadtmann A, Zarbock A, et al. Leukocyte extravasation and vascular permeability are each controlled in vivo by different tyrosine residues of VE-cadherin. Nat Immunol. 2014;15:223–30. doi:10.1038/ni.2824. PMID:24487320.
  • Heemskerk N, Schimmel L, Oort C, van Rijssel J, Yin T, Ma B, van Unen J, Pitter B, Huveneers S, Goedhart J, et al. F-actin-rich contractile endothelial pores prevent vascular leakage during leukocyte diapedesis through local RhoA signalling. Nat Commun. 2016;7:10493. doi:10.1038/ncomms10493. PMID:26814335.
  • Bochkov VN, Leitinger N. Anti-inflammatory properties of lipid oxidation products. J Mol Med (Berl). 2003;81:613–26. doi:10.1007/s00109-003-0467-2. PMID:13679995.
  • Huber J, Vales A, Mitulovic G, Blumer M, Schmid R, Witztum JL, Binder BR, Leitinger N. Oxidized membrane vesicles and blebs from apoptotic cells contain biologically active oxidized phospholipids that induce monocyte-endothelial interactions. Arterioscler Thromb Vasc Biol. 2002;22:101–7. doi:10.1161/hq0102.101525. PMID:11788468.
  • Leitinger N. Oxidized phospholipids as modulators of inflammation in atherosclerosis. Curr Opin Lipidol. 2003;14:421–30. doi:10.1097/00041433-200310000-00002. PMID:14501580.
  • Chabot F, Mitchell JA, Gutteridge JM, Evans TW. Reactive oxygen species in acute lung injury. Eur Respir J. 1998;11:745–57. PMID:9596132.
  • Wood LG, Gibson PG, Garg ML. Biomarkers of lipid peroxidation, airway inflammation and asthma. Eur Respir J. 2003;21:177–86. doi:10.1183/09031936.03.00017003a. PMID:12570126.
  • Kalyanaraman B. Nitrated lipids: a class of cell-signaling molecules. Proc Natl Acad Sci U S A. 2004;101:11527–8. doi:10.1073/pnas.0404309101. PMID:15292510.
  • Pennathur S, Bergt C, Shao B, Byun J, Kassim SY, Singh P, Green PS, McDonald TO, Brunzell J, Chait A, et al. Human atherosclerotic intima and blood of patients with established coronary artery disease contain high density lipoprotein damaged by reactive nitrogen species. J Biol Chem. 2004;279:42977–83. doi:10.1074/jbc.M406762200. PMID:15292228.
  • Carpenter CT, Price PV, Christman BW. Exhaled breath condensate isoprostanes are elevated in patients with acute lung injury or ARDS. Chest. 1998;114:1653–9. doi:10.1378/chest.114.6.1653. PMID:9872202.
  • Cracowski JL, Cracowski C, Bessard G, Pepin JL, Bessard J, Schwebel C, Stanke-Labesque F, Pison C. Increased lipid peroxidation in patients with pulmonary hypertension. Am J Respir Crit Care Med. 2001;164:1038–42. doi:10.1164/ajrccm.164.6.2104033. PMID:11587993.
  • Montuschi P, Corradi M, Ciabattoni G, Nightingale J, Kharitonov SA, Barnes PJ. Increased 8-isoprostane, a marker of oxidative stress, in exhaled condensate of asthma patients. Am J Respir Crit Care Med. 1999;160:216–20. doi:10.1164/ajrccm.160.1.9809140. PMID:10390403.
  • Montuschi P, Kharitonov SA, Ciabattoni G, Corradi M, van Rensen L, Geddes DM, Hodson ME, Barnes PJ. Exhaled 8-isoprostane as a new non-invasive biomarker of oxidative stress in cystic fibrosis. Thorax. 2000;55:205–9. doi:10.1136/thorax.55.3.205. PMID:10679539.
  • Greig FH, Kennedy S, Spickett CM. Physiological effects of oxidized phospholipids and their cellular signaling mechanisms in inflammation. Free Radic Biol Med. 2012;52:266–80. doi:10.1016/j.freeradbiomed.2011.10.481. PMID:22080084.
  • Gugiu BG, Mouillesseaux K, Duong V, Herzog T, Hekimian A, Koroniak L, Vondriska TM, Watson AD. Protein targets of oxidized phospholipids in endothelial cells. J Lipid Res. 2008;49:510–20. doi:10.1194/jlr.M700264-JLR200. PMID:18071189.
  • Cole AL, Subbanagounder G, Mukhopadhyay S, Berliner JA, Vora DK. Oxidized phospholipid-induced endothelial cell/monocyte interaction is mediated by a cAMP-dependent R-Ras/PI3-kinase pathway. Arterioscler Thromb Vasc Biol. 2003;23:1384–90. doi:10.1161/01.ATV.0000081215.45714.71. PMID:12805072.
  • Patricia MK, Kim JA, Harper CM, Shih PT, Berliner JA, Natarajan R, Nadler JL, Hedrick CC. Lipoxygenase products increase monocyte adhesion to human aortic endothelial cells. Arterioscler Thromb Vasc Biol. 1999;19:2615–22. doi:10.1161/01.ATV.19.11.2615. PMID:10559003.
  • Shih PT, Elices MJ, Fang ZT, Ugarova TP, Strahl D, Territo MC, Frank JS, Kovach NL, Cabanas C, Berliner JA, et al. Minimally modified low-density lipoprotein induces monocyte adhesion to endothelial connecting segment-1 by activating beta1 integrin. J Clin Invest. 1999;103:613–25. doi:10.1172/JCI5710. PMID:10074478.
  • Gargalovic PS, Imura M, Zhang B, Gharavi NM, Clark MJ, Pagnon J, Yang WP, He A, Truong A, Patel S, et al. Identification of inflammatory gene modules based on variations of human endothelial cell responses to oxidized lipids. Proc Natl Acad Sci U S A. 2006;103:12741–6. doi:10.1073/pnas.0605457103. PMID:16912112.
  • Yeh M, Gharavi NM, Choi J, Hsieh X, Reed E, Mouillesseaux KP, Cole AL, Reddy ST, Berliner JA. Oxidized phospholipids increase interleukin 8 (IL-8) synthesis by activation of the c-src/signal transducers and activators of transcription (STAT)3 pathway. J Biol Chem. 2004;279:30175–81. doi:10.1074/jbc.M312198200. PMID:15143062.
  • Bochkov VN, Mechtcheriakova D, Lucerna M, Huber J, Malli R, Graier WF, Hofer E, Binder BR, Leitinger N. Oxidized phospholipids stimulate tissue factor expression in human endothelial cells via activation of ERK/EGR-1 and Ca(++)/NFAT. Blood. 2002;99:199–206. doi:10.1182/blood.V99.1.199. PMID:11756172.
  • Lusis AJ. Atherosclerosis. Nature. 2000;407:233–41. doi:10.1038/35025203. PMID:11001066.
  • Watson AD, Leitinger N, Navab M, Faull KF, Horkko S, Witztum JL, Palinski W, Schwenke D, Salomon RG, Sha W, et al. Structural identification by mass spectrometry of oxidized phospholipids in minimally oxidized low density lipoprotein that induce monocyte/endothelial interactions and evidence for their presence in vivo. J Biol Chem. 1997;272:13597–607. doi:10.1074/jbc.272.21.13597. PMID:9153208.
  • Bochkov VN, Kadl A, Huber J, Gruber F, Binder BR, Leitinger N. Protective role of phospholipid oxidation products in endotoxin-induced tissue damage. Nature. 2002;419:77–81. doi:10.1038/nature01023. PMID:12214235.
  • Ma Z, Li J, Yang L, Mu Y, Xie W, Pitt B, Li S. Inhibition of LPS- and CpG DNA-induced TNF-alpha response by oxidized phospholipids. Am J Physiol Lung Cell Mol Physiol. 2004;286:L808–16. doi:10.1152/ajplung.00220.2003. PMID:14644758.
  • Birukov KG, Bochkov VN, Birukova AA, Kawkitinarong K, Rios A, Leitner A, Verin AD, Bokoch GM, Leitinger N, Garcia JG. Epoxycyclopentenone-containing oxidized phospholipids restore endothelial barrier function via Cdc42 and Rac. Circ Res. 2004;95:892–901. doi:10.1161/01.RES.0000147310.18962.06. PMID:15472119.
  • Nonas S, Miller I, Kawkitinarong K, Chatchavalvanich S, Gorshkova I, Bochkov VN, Leitinger N, Natarajan V, Garcia JG, Birukov KG. Oxidized phospholipids reduce vascular leak and inflammation in rat model of acute lung injury. Am J Respir Crit Care Med. 2006;173:1130–8. doi:10.1164/rccm.200511-1737OC. PMID:16514111.
  • Nonas S, Birukova AA, Fu P, Xing J, Chatchavalvanich S, Bochkov VN, Leitinger N, Garcia JG, Birukov KG. Oxidized phospholipids reduce ventilator-induced vascular leak and inflammation in vivo. Crit Care. 2008;12:R27. doi:10.1186/cc6805. PMID:18304335.
  • Meliton AY, Meng F, Tian Y, Sarich N, Mutlu GM, Birukova AA, Birukov KG. Oxidized phospholipids protect against lung injury and endothelial barrier dysfunction caused by heat-inactivated Staphylococcus aureus. Am J Physiol Lung Cell Mol Physiol. 2015;308:L550–62. doi:10.1152/ajplung.00248.2014. PMID:25575515.
  • Birukova AA, Fu P, Chatchavalvanich S, Burdette D, Oskolkova O, Bochkov VN, Birukov KG. Polar head groups are important for barrier-protective effects of oxidized phospholipids on pulmonary endothelium. Am J Physiol Lung Cell Mol Physiol. 2007;292:L924–35. doi:10.1152/ajplung.00395.2006. PMID:17158600.
  • Birukov KG, Leitinger N, Bochkov VN, Garcia JG. Signal transduction pathways activated in human pulmonary endothelial cells by OxPAPC, a bioactive component of oxidized lipoproteins. Microvasc Res. 2004;67:18–28. doi:10.1016/j.mvr.2003.09.004. PMID:14709399.
  • Birukova AA, Malyukova I, Mikaelyan A, Fu P, Birukov KG. Tiam1 and betaPIX mediate Rac-dependent endothelial barrier protective response to oxidized phospholipids. J Cell Physiol. 2007;211:608–17. doi:10.1002/jcp.20966. PMID:17219408.
  • Birukova AA, Alekseeva E, Cokic I, Turner CE, Birukov KG. Cross talk between paxillin and Rac is critical for mediation of barrier-protective effects by oxidized phospholipids. Am J Physiol Lung Cell Mol Physiol. 2008;295:L593–602. doi:10.1152/ajplung.90257.2008. PMID:18676874.
  • Birukova AA, Chatchavalvanich S, Oskolkova O, Bochkov VN, Birukov KG. Signaling pathways involved in OxPAPC-induced pulmonary endothelial barrier protection. Microvasc Res. 2007;73:173–81. doi:10.1016/j.mvr.2006.12.004. PMID:17292425.
  • Birukova AA, Malyukova I, Poroyko V, Birukov KG. Paxillin-beta-catenin interactions are involved in Rac/Cdc42-mediated endothelial barrier-protective response to oxidized phospholipids. Am J Physiol Lung Cell Mol Physiol. 2007;293:L199–211. doi:10.1152/ajplung.00020.2007. PMID:17513457.
  • Birukova AA, Zebda N, Fu P, Poroyko V, Cokic I, Birukov KG. Association between adherens junctions and tight junctions via Rap1 promotes barrier protective effects of oxidized phospholipids. J Cell Physiol. 2011;226:2052–62. doi:10.1002/jcp.22543. PMID:21520057.
  • Birukova AA, Fu P, Wu T, Dubrovskyi O, Sarich N, Poroyko V, Birukov KG. Afadin controls p120-catenin-ZO-1 interactions leading to endothelial barrier enhancement by oxidized phospholipids. J Cell Physiol. 2012;227:1883–90. doi:10.1002/jcp.22916. PMID:21732359.
  • Singleton PA, Chatchavalvanich S, Fu P, Xing J, Birukova AA, Fortune JA, Klibanov AM, Garcia JG, Birukov KG. Akt-mediated transactivation of the S1P1 receptor in caveolin-enriched microdomains regulates endothelial barrier enhancement by oxidized phospholipids. Circ Res. 2009;104:978–86. doi:10.1161/CIRCRESAHA.108.193367. PMID:19286607.
  • Birukova AA, Singleton PA, Gawlak G, Tian X, Mirzapoiazova T, Mambetsariev B, Dubrovskyi O, Oskolkova OV, Bochkov VN, Birukov KG. GRP78 is a novel receptor initiating a vascular barrier protective response to oxidized phospholipids. Mol Biol Cell. 2014;25:2006–16. doi:10.1091/mbc.E13-12-0743. PMID:24829380.
  • Birukova AA, Zebda N, Cokic I, Fu P, Wu T, Dubrovskyi O, Birukov KG. p190RhoGAP mediates protective effects of oxidized phospholipids in the models of ventilator-induced lung injury. Exp Cell Res. 2011;317:859–72. doi:10.1016/j.yexcr.2010.11.011. PMID:21111731.
  • Birukova AA, Shah AS, Tian Y, Moldobaeva N, Birukov KG. Dual role of vinculin in barrier-disruptive and barrier-enhancing endothelial cell responses. Cell Signal. 2016;28:541–51. doi:10.1016/j.cellsig.2016.02.015. PMID:26923917.
  • Tian Y, Tian X, Gawlak G, Sarich N, Sacks DB, Birukova AA, Birukov KG. Role of IQGAP1 in endothelial barrier enhancement caused by OxPAPC. Am J Physiol Lung Cell Mol Physiol. 2016;311:L800–L809. doi:10.1152/ajplung.00095.2016. PMID:27566003.
  • Zimman A, Mouillesseaux KP, Le T, Gharavi NM, Ryvkin A, Graeber TG, Chen TT, Watson AD, Berliner JA. Vascular endothelial growth factor receptor 2 plays a role in the activation of aortic endothelial cells by oxidized phospholipids. Arterioscler Thromb Vasc Biol. 2007;27:332–8. doi:10.1161/01.ATV.0000252842.57585.df. PMID:17110601.
  • Pegorier S, Stengel D, Durand H, Croset M, Ninio E. Oxidized phospholipid: POVPC binds to platelet-activating-factor receptor on human macrophages. Implications in atherosclerosis. Atherosclerosis. 2006;188:433–43. doi:10.1016/j.atherosclerosis.2005.11.015. PMID:16386258.
  • Li R, Mouillesseaux KP, Montoya D, Cruz D, Gharavi N, Dun M, Koroniak L, Berliner JA. Identification of prostaglandin E2 receptor subtype 2 as a receptor activated by OxPAPC. Circ Res. 2006;98:642–50. doi:10.1161/01.RES.0000207394.39249.fc. PMID:16456101.
  • Podrez EA, Poliakov E, Shen Z, Zhang R, Deng Y, Sun M, Finton PJ, Shan L, Gugiu B, Fox PL, et al. Identification of a novel family of oxidized phospholipids that serve as ligands for the macrophage scavenger receptor CD36. J Biol Chem. 2002;277:38503–16. doi:10.1074/jbc.M203318200 10.1074/jbc.M205924200. PMID:12105195.
  • Walton KA, Hsieh X, Gharavi N, Wang S, Wang G, Yeh M, Cole AL, Berliner JA. Receptors involved in the oxidized 1-palmitoyl-2-arachidonoyl-sn-glycero-3-phosphorylcholine-mediated synthesis of interleukin-8. A role for Toll-like receptor 4 and a glycosylphosphatidylinositol-anchored protein. J Biol Chem. 2003;278:29661–6. doi:10.1074/jbc.M300738200. PMID:12777373.
  • Lee H, Shi W, Tontonoz P, Wang S, Subbanagounder G, Hedrick CC, Hama S, Borromeo C, Evans RM, Berliner JA, et al. Role for peroxisome proliferator-activated receptor alpha in oxidized phospholipid-induced synthesis of monocyte chemotactic protein-1 and interleukin-8 by endothelial cells. Circ Res. 2000;87:516–21. doi:10.1161/01.RES.87.6.516. PMID:10988245.
  • Oskolkova O, Gawlak G, Tian Y, Ke Y, Sarich N, Son S, Andreasson K, Bochkov VN, Birukova AA, Birukov KG. Prostaglandin E receptor-4 receptor mediates endothelial barrier-enhancing and anti-inflammatory effects of oxidized phospholipids. FASEB J. 2017;31(9):4187–202. doi:10.1096/fj.201601232RR. PMID:28572443.
  • Ke Y, Zebda N, Oskokova O, Afonyushkin T, Berdyshev E, Tian Y, Meng F, Sarich N, Bochkov VN, Wang JM, et al. Anti-inflammatory effects of OxPAPC involve endothelial cell mediated generation of LXA4. Circ Res. 2017;121(3):244–57. doi:10.1161/CIRCRESAHA.116.310308. PMID:28522438.
  • Cezar-de-Mello PF, Nascimento-Silva V, Villela CG, Fierro IM. Aspirin-triggered Lipoxin A4 inhibition of VEGF-induced endothelial cell migration involves actin polymerization and focal adhesion assembly. Oncogene. 2006;25:122–9. PMID:16132039.
  • Vieira AM, Neto EH, Figueiredo CC, Barja Fidalgo C, Fierro IM, Morandi V. ATL-1, a synthetic analog of lipoxin, modulates endothelial permeability and interaction with tumor cells through a VEGF-dependent mechanism. Biochem Pharmacol. 2014;90:388–96. doi:10.1016/j.bcp.2014.05.019. PMID:24887589.
  • Birukova AA, Lee S, Starosta V, Wu T, Ho T, Kim J, Berliner JA, Birukov KG. A role for VEGFR2 activation in endothelial responses caused by barrier disruptive OxPAPC concentrations. PLoS One. 2012;7:e30957. doi:10.1371/journal.pone.0030957. PMID:22303475.
  • Birukova AA, Starosta V, Tian X, Higginbotham K, Koroniak L, Berliner JA, Birukov KG. Fragmented oxidation products define barrier disruptive endothelial cell response to OxPAPC. Transl Res. 2013;161:495–504. doi:10.1016/j.trsl.2012.12.008. PMID:23305708.
  • Yeh M, Cole AL, Choi J, Liu Y, Tulchinsky D, Qiao JH, Fishbein MC, Dooley AN, Hovnanian T, Mouilleseaux K, et al. Role for sterol regulatory element-binding protein in activation of endothelial cells by phospholipid oxidation products. Circ Res. 2004;95:780–8. doi:10.1161/01.RES.0000146030.53089.18. PMID:15388640.
  • Bochkov VN, Philippova M, Oskolkova O, Kadl A, Furnkranz A, Karabeg E, Afonyushkin T, Gruber F, Breuss J, Minchenko A, et al. Oxidized phospholipids stimulate angiogenesis via autocrine mechanisms, implicating a novel role for lipid oxidation in the evolution of atherosclerotic lesions. Circ Res. 2006;99:900–8. doi:10.1161/01.RES.0000245485.04489.ee. PMID:16973904.
  • Oskolkova OV, Afonyushkin T, Leitner A, von Schlieffen E, Gargalovic PS, Lusis AJ, Binder BR, Bochkov VN. ATF4-dependent transcription is a key mechanism in VEGF up-regulation by oxidized phospholipids: critical role of oxidized sn-2 residues in activation of unfolded protein response. Blood. 2008;112:330–9. doi:10.1182/blood-2007-09-112870. PMID:18451308.
  • Starosta V, Wu T, Zimman A, Pham D, Tian X, Oskolkova O, Bochkov V, Berliner JA, Birukova AA, Birukov KG. 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. 2012;46:331–41. doi:10.1165/rcmb.2011-0153OC. PMID:21997484.
  • Alcaide P, Newton G, Auerbach S, Sehrawat S, Mayadas TN, Golan DE, Yacono P, Vincent P, Kowalczyk A, Luscinskas FW. p120-Catenin regulates leukocyte transmigration through an effect on VE-cadherin phosphorylation. Blood. 2008;112:2770–9. doi:10.1182/blood-2008-03-147181. PMID:18641366.
  • Potter MD, Barbero S, Cheresh DA. Tyrosine phosphorylation of VE-cadherin prevents binding of p120- and beta-catenin and maintains the cellular mesenchymal state. J Biol Chem. 2005;280:31906–12. doi:10.1074/jbc.M505568200. PMID:16027153.
  • Allingham MJ, van Buul JD, Burridge K. ICAM-1-mediated, Src- and Pyk2-dependent vascular endothelial cadherin tyrosine phosphorylation is required for leukocyte transendothelial migration. J Immunol. 2007;179:4053–64. doi:10.4049/jimmunol.179.6.4053. PMID:17785844.
  • Buland JR, Wasserloos KJ, Tyurin VA, Tyurina YY, Amoscato AA, Mallampalli RK, Chen BB, Zhao J, Zhao Y, Ofori-Acquah S, et al. Biosynthesis of oxidized lipid mediators via lipoprotein-associated phospholipase A2 hydrolysis of extracellular cardiolipin induces endothelial toxicity. Am J Physiol Lung Cell Mol Physiol. 2016;311:L303–16. PMID:27233995.
  • Birukov KG. Oxidized lipids: the two faces of vascular inflammation. Curr Atheroscler Rep. 2006;8:223–31. doi:10.1007/s11883-006-0077-x. PMID:16640959.
  • Heffern CT, Pocivavsek L, Birukova AA, Moldobaeva N, Bochkov VN, Lee KY, Birukov KG. Thermodynamic and kinetic investigations of the release of oxidized phospholipids from lipid membranes and its effect on vascular integrity. Chem Phys Lipids. 2013;175–176:9–19. doi:10.1016/j.chemphyslip.2013.07.003. PMID:23911706.
  • Ozaki H, Hla T, Lee MJ. Sphingosine-1-phosphate signaling in endothelial activation. J Atheroscler Thromb. 2003;10:125–31. doi:10.5551/jat.10.125. PMID:14564080.
  • Hla T. Signaling and biological actions of sphingosine 1-phosphate. Pharmacol Res. 2003;47:401–7. doi:10.1016/S1043-6618(03)00046-X. PMID:12676514.
  • Abbasi T, Garcia JG. Sphingolipids in lung endothelial biology and regulation of vascular integrity. Handb Exp Pharmacol. 2013;216:201–26. doi:10.1007/978-3-7091-1511-4_10. PMID:23563658.
  • Lo SK, Burhop KE, Kaplan JE, Malik AB. Role of platelets in maintenance of pulmonary vascular permeability to protein. Am J Physiol. 1988;254:H763–71. PMID:3354701.
  • Haselton FR, Alexander JS. Platelets and a platelet-released factor enhance endothelial barrier. Am J Physiol. 1992;263:L670–8. PMID:1476205.
  • 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. doi:10.1172/JCI12450. PMID:11544274.
  • Takuwa Y. Subtype-specific differential regulation of Rho family G proteins and cell migration by the Edg family sphingosine-1-phosphate receptors. Biochimica Et Biophysica Acta. 2002;1582:112–20. doi:10.1016/S1388-1981(02)00145-2. PMID:12069818.
  • McVerry BJ, Garcia JG. In vitro and in vivo modulation of vascular barrier integrity by sphingosine 1-phosphate: mechanistic insights. Cell Signal. 2005;17:131–9. doi:10.1016/j.cellsig.2004.08.006. PMID:15494205.
  • Shikata Y, Birukov KG, Garcia JG. S1P induces FA remodeling in human pulmonary endothelial cells: role of Rac, GIT1, FAK, and paxillin. J Appl Physiol (1985). 2003;94:1193–203. doi:10.1152/japplphysiol.00690.2002. PMID:12482769.
  • Li Q, Chen B, Zeng C, Fan A, Yuan Y, Guo X, Huang X, Huang Q. Differential activation of receptors and signal pathways upon stimulation by different doses of sphingosine-1-phosphate in endothelial cells. Exp Physiol. 2015;100:95–107. doi:10.1113/expphysiol.2014.082149. PMID:25557733.
  • Galvani S, Sanson M, Blaho VA, Swendeman SL, Obinata H, Conger H, Dahlbäck B, Kono M, Proia RL, Smith JD, et al. HDL-bound sphingosine 1-phosphate acts as a biased agonist for the endothelial cell receptor S1P1 to limit vascular inflammation. Sci Signal. 2015;8:ra79. doi:10.1126/scisignal.aaa2581. PMID:26268607.
  • Zhang G, Yang L, Kim GS, Ryan K, Lu S, O'Donnell RK, Spokes K, Shapiro N, Aird WC, Kluk MJ, et al. Critical role of sphingosine-1-phosphate receptor 2 (S1PR2) in acute vascular inflammation. Blood. 2013;122:443–55. doi:10.1182/blood-2012-11-467191. PMID:23723450.
  • Nussbaum C, Bannenberg S, Keul P, Graler MH, Goncalves-de-Albuquerque CF, Korhonen H, von Wnuck Lipinski K, Heusch G, de Castro Faria Neto HC, Rohwedder I, et al. Sphingosine-1-phosphate receptor 3 promotes leukocyte rolling by mobilizing endothelial P-selectin. Nat Commun. 2015;6:6416. doi:10.1038/ncomms7416. PMID:25832730.
  • Peng X, Hassoun PM, Sammani S, McVerry BJ, Burne MJ, Rabb H, Pearse D, Tuder RM, Garcia JG. Protective effects of sphingosine 1-phosphate in murine endotoxin-induced inflammatory lung injury. Am J Respir Crit Care Med. 2004;169:1245–51. doi:10.1164/rccm.200309-1258OC. PMID:15020292.
  • McVerry BJ, Peng X, Hassoun PM, Sammani S, Simon BA, Garcia JG. Sphingosine 1-phosphate reduces vascular leak in murine and canine models of acute lung injury. Am J Respir Crit Care Med. 2004;170:987–93. doi:10.1164/rccm.200405-684OC. PMID:15282202.
  • Sammani S, Moreno-Vinasco L, Mirzapoiazova T, Singleton PA, Chiang ET, Evenoski CL, Wang T, Mathew B, Husain A, Moitra J, et al. Differential effects of sphingosine 1-phosphate receptors on airway and vascular barrier function in the murine lung. Am J Respir Cell Mol Biol. 2010;43:394–402. doi:10.1165/rcmb.2009-0223OC. PMID:19749179.
  • Winkler MS, Nierhaus A, Poppe A, Greiwe G, Graler MH, Daum G. Sphingosine-1-Phosphate: A potential biomarker and therapeutic target for endothelial dysfunction and sepsis? Shock (Augusta, Ga). 2017;47:666–72. doi:10.1097/SHK.0000000000000814. PMID:27922551.
  • 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;279:24692–700. doi:10.1074/jbc.M313969200. PMID:15056655.
  • Birukov KG, Zebda N, Birukova AA. Barrier enhancing signals in pulmonary edema. Compr Physiol. 2013;3:429–84. PMID:23720293.
  • Mehta D, Konstantoulaki M, Ahmmed GU, Malik AB. Sphingosine 1-phosphate-induced mobilization of intracellular Ca2+ mediates rac activation and adherens junction assembly in endothelial cells. J Biol Chem. 2005;280:17320–8. doi:10.1074/jbc.M411674200. PMID:15728185.
  • Mandala S, Hajdu R, Bergstrom J, Quackenbush E, Xie J, Milligan J, Thornton R, Shei GJ, Card D, Keohane C, et al. Alteration of lymphocyte trafficking by sphingosine-1-phosphate receptor agonists. Science. 2002;296:346–9. doi:10.1126/science.1070238. PMID:11923495.
  • Natarajan V, Dudek SM, Jacobson JR, Moreno-Vinasco L, Huang LS, Abassi T, Mathew B, Zhao Y, Wang L, Bittman R, et al. Sphingosine-1-phosphate, FTY720, and sphingosine-1-phosphate receptors in the pathobiology of acute lung injury. Am J Respir Cell Mol Biol. 2013;49:6–17. doi:10.1165/rcmb.2012-0411TR. PMID:23449739.
  • 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;19:1754–64. doi:10.1016/j.cellsig.2007.03.011. PMID:17475445.
  • Frink M, Kaudel CP, Hildebrand F, Pape HC, Klempnauer J, Winkler M, Krettek C, van Griensven M. FTY720 improves survival after transient ischemia and reperfusion of the hind limbs. J Trauma. 2007;63:263–7. doi:10.1097/TA.0b013e3180d0a6fc. PMID:17693822.
  • Liu HB, Cui NQ, Wang Q, Li DH, Xue XP. Sphingosine-1-phosphate and its analogue FTY720 diminish acute pulmonary injury in rats with acute necrotizing pancreatitis. Pancreas. 2008;36:e10–5. doi:10.1097/MPA.0b013e31815f3905. PMID:18362832.
  • Farmer PJ, Bernier SG, Lepage A, Guillemette G, Regoli D, Sirois P. Permeability of endothelial monolayers to albumin is increased by bradykinin and inhibited by prostaglandins. Am J Physiol Lung Cell Mol Physiol. 2001;280:L732–8. PMID:11238014.
  • Fukuhara S, Sakurai A, Sano H, Yamagishi A, Somekawa S, Takakura N, Saito Y, Kangawa K, Mochizuki N. Cyclic AMP potentiates vascular endothelial cadherin-mediated cell-cell contact to enhance endothelial barrier function through an Epac-Rap1 signaling pathway. Mol Cell Biol. 2005;25:136–46. doi:10.1128/MCB.25.1.136-146.2005. PMID:15601837.
  • Park GY, Christman JW. Involvement of cyclooxygenase-2 and prostaglandins in the molecular pathogenesis of inflammatory lung diseases. Am J Physiol Lung Cell Mol Physiol. 2006;290:L797–805. doi:10.1152/ajplung.00513.2005. PMID:16603593.
  • Kobayashi K, Tsubosaka Y, Hori M, Narumiya S, Ozaki H, Murata T. Prostaglandin D2-DP signaling promotes endothelial barrier function via the cAMP/PKA/Tiam1/Rac1 pathway. Arterioscler Thromb Vasc Biol. 2013;33:565–71. doi:10.1161/ATVBAHA.112.300993. PMID:23307871.
  • Howard LS, Morrell NW. New therapeutic agents for pulmonary vascular disease. Paediatr Respir Rev. 2005;6:285–91. doi:10.1016/j.prrv.2005.09.006. PMID:16298312.
  • Ueno Y, Koike H, Annoh S, Nishio S. Anti-inflammatory effects of beraprost sodium, a stable analogue of PGI2, and its mechanisms. Prostaglandins. 1997;53:279–89. doi:10.1016/S0090-6980(97)89601-3. PMID:9167214.
  • Birukova AA, Fu P, Xing J, Birukov KG. Rap1 mediates protective effects of iloprost against ventilator-induced lung injury. J Appl Physiol (Bethesda, Md: 1985). 2009;107:1900–10. doi:10.1152/japplphysiol.00462.2009.
  • Birukova AA, Fu P, Xing J, Cokic I, Birukov KG. Lung endothelial barrier protection by iloprost in the 2-hit models of ventilator-induced lung injury (VILI) involves inhibition of Rho signaling. Transl Res. 2010;155:44–54. doi:10.1016/j.trsl.2009.09.002. PMID:20004361.
  • Birukova AA, Wu T, Tian Y, Meliton A, Sarich N, Tian X, Leff A, Birukov KG. Iloprost improves endothelial barrier function in lipopolysaccharide-induced lung injury. Eur Respir J. 2013;41:165–76. doi:10.1183/09031936.00148311. PMID:22790920.
  • Langeler EG, van Hinsbergh VW. Norepinephrine and iloprost improve barrier function of human endothelial cell monolayers: role of cAMP. Am J Physiol. 1991;260:C1052–9. PMID:1709785.
  • Birukova AA, Meng F, Tian Y, Meliton A, Sarich N, Quilliam LA, Birukov KG. Prostacyclin post-treatment improves LPS-induced acute lung injury and endothelial barrier recovery via Rap1. Biochimica Et Biophysica Acta. 2015;1852:778–91. doi:10.1016/j.bbadis.2014.12.016. PMID:25545047.
  • Ke Y, Oskolkova O, Sarich N, Tian Y, Sitikov A, Tulapurkar M, Son S, Birukova AA, Birukov KG. Effects of prostaglandin lipid mediators on agonist-induced lung endothelial permeability and inflammation. Am J Physiol Lung Cell Mol Physiol. 2017;313(4):L710–L721. doi:10.1152/ajplung.00519.2016. PMID:28663336.
  • Ohmura T, Tian Y, Sarich N, Ke Y, Meliton A, Shah AS, Andreasson K, Birukov KG, Birukova AA. Regulation of lung endothelial permeability and inflammatory responses by prostaglandin A2: role of EP4 receptor. Mol Biol Cell. 2017;28(12):1622–35. doi:10.1091/mbc.E16-09-0639. PMID:28428256.
  • Moloney ED, Evans TW. Pathophysiology and pharmacological treatment of pulmonary hypertension in acute respiratory distress syndrome. Eur Respir J. 2003;21:720–7. doi:10.1183/09031936.03.00120102. PMID:12762363.
  • Ali AE, Barrett JC, Eling TE. Prostaglandin and thromboxane production by fibroblasts and vascular endothelial cells. Prostaglandins. 1980;20:667–88. doi:10.1016/0090-6980(80)90107-0. PMID:7008090.
  • Huang JS, Ramamurthy SK, Lin X, Le Breton GC. Cell signalling through thromboxane A2 receptors. Cell Signal. 2004;16:521–33. doi:10.1016/j.cellsig.2003.10.008. PMID:14751539.
  • Klausner JM, Abu-Abid S, Alexander JS, Hanshke-Mineau R, Goldman G, Morel N, Valeri CR, Shepro D, Hechtman HB. Thromboxane modulates endothelial permeability. Mediators Inflamm. 1994;3:149–53. doi:10.1155/S0962935194000190. PMID:18472934.
  • Kim SR, Bae SK, Park HJ, Kim MK, Kim K, Park SY, Jang HO, Yun I, Kim YJ, Yoo MA, et al. Thromboxane A(2) increases endothelial permeability through upregulation of interleukin-8. Biochem Biophys Res Commun. 2010;397:413–9. doi:10.1016/j.bbrc.2010.05.106. PMID:20510674.
  • Deby-Dupont G, Braun M, Lamy M, Deby C, Pincemail J, Faymonville ME, Damas P, Bodson L, Lecart MP, Goutier R. Thromboxane and prostacyclin release in adult respiratory distress syndrome. Intensive Care Med. 1987;13:167–74. doi:10.1007/BF00254700. PMID:3584647.
  • Goff CD, Corbin RS, Theiss SD, Frierson HF Jr, Cephas GA, Tribble CG, Kron IL, Young JS. Postinjury thromboxane receptor blockade ameliorates acute lung injury. Ann Thorac Surg. 1997;64:826–9. doi:10.1016/S0003-4975(97)00490-6. PMID:9307481.
  • Zarbock A, Singbartl K, Ley K. Complete reversal of acid-induced acute lung injury by blocking of platelet-neutrophil aggregation. J Clin Invest. 2006;116:3211–9. doi:10.1172/JCI29499. PMID:17143330.
  • Kobayashi K, Horikami D, Omori K, Nakamura T, Yamazaki A, Maeda S, Murata T. Thromboxane A2 exacerbates acute lung injury via promoting edema formation. Sci Rep. 2016;6:32109. doi:10.1038/srep32109. PMID:27562142.
  • Zhao Z, Hu J, Gao X, Liang H, Yu H, Liu S, Liu Z. Hyperglycemia via activation of thromboxane A2 receptor impairs the integrity and function of blood-brain barrier in microvascular endothelial cells. Oncotarget. 2017;8:30030–8. PMID:28415790.
  • Knezevic II, Predescu SA, Neamu RF, Gorovoy MS, Knezevic NM, Easington C, Malik AB, Predescu DN. Tiam1 and Rac1 are required for platelet-activating factor-induced endothelial junctional disassembly and increase in vascular permeability. J Biol Chem. 2009;284:5381–94. doi:10.1074/jbc.M808958200. PMID:19095647.
  • Fang W, Geng X, Deng Y, Li Y, Shang E, Cen J, Lv P. Platelet activating factor induces blood brain barrier permeability alteration in vitro. J Neuroimmunol. 2011;230:42–7. doi:10.1016/j.jneuroim.2010.08.015. PMID:20870297.
  • Meng F OT, Yang MM, Birukova A, Birukov K,. Esterification of iloprost enhances its barrier protective effects on pulmonary endothelium. Am J Respir Crit Care Med. 2017;195:A4779.
  • McIntyre TM, Prescott SM, Stafforini DM. The emerging roles of PAF acetylhydrolase. J Lipid Res. 2009;50(Suppl):S255–9. doi:10.1194/jlr.R800024-JLR200. PMID:18838739.
  • Latchoumycandane C, Marathe GK, Zhang R, McIntyre TM. Oxidatively truncated phospholipids are required agents of tumor necrosis factor alpha (TNFalpha)-induced apoptosis. J Biol Chem. 2012;287:17693–705. doi:10.1074/jbc.M111.300012. PMID:22433871.
  • Deigner HP, Hermetter A. Oxidized phospholipids: emerging lipid mediators in pathophysiology. Curr Opin Lipidol. 2008;19:289–94. doi:10.1097/MOL.0b013e3282fe1d0e. PMID:18460921.
  • Florens N, Calzada C, Lyasko E, Juillard L, Soulage CO. Modified lipids and lipoproteins in chronic kidney disease: A new class of uremic toxins. Toxins (Basel). 2016;8:E376. doi:10.3390/toxins8120376. PMID:27999257.
  • Sharma S, Ruffenach G, Umar S, Motayagheni N, Reddy ST, Eghbali M. Role of oxidized lipids in pulmonary arterial hypertension. Pulm Circ. 2016;6:261–73. doi:10.1086/687293. PMID:27683603.
  • Philippova M, Resink T, Erne P, Bochkov V. Oxidised phospholipids as biomarkers in human disease. Swiss Med Wkly. 2014;144:w14037. PMID:25539162.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.