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Review

Relationship between G proteins coupled receptors and tight junctions

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Article: e1414015 | Received 01 Sep 2017, Accepted 23 Nov 2017, Published online: 08 Feb 2018

References

  • Cereijido M, Valdes J, Shoshani L, Contreras RG. Role of tight junctions in establishing and maintaining cell polarity. Annual Rev Physiol. 1998;60:161–77. doi:10.1146/annurev.physiol.60.1.161.
  • van Meer G, Simons K. The function of tight junctions in maintaining differences in lipid composition between the apical and the basolateral cell surface domains of MDCK cells. EMBO J. 1986;5(7):1455–64.
  • Dragsten PR, Blumenthal R, Handler JS. Membrane asymmetry in epithelia: Is the tight junction a barrier to diffusion in the plasma membrane? Nature. 1981;294(5843):718–22. doi:10.1038/294718a0.
  • Nava P, Lopez S, Arias CF, Islas S, Gonzalez-Mariscal L. The rotavirus surface protein VP8 modulates the gate and fence function of tight junctions in epithelial cells. J Cell Sci. 2004;117(Pt 23):5509–19. Epub 2004/10/21. doi:10.1242/jcs.01425.
  • Baas AF, Kuipers J, van der Wel NN, Batlle E, Koerten HK, Peters PJ, Clevers HC. Complete polarization of single intestinal epithelial cells upon activation of LKB1 by STRAD. Cell. 2004;116(3):457–66. doi:10.1016/S0092-8674(04)00114-X.
  • Farquhar MG, Palade GE. Junctional complexes in various epithelia. J Cell Biol 1963;17:375–412. Epub 1963/05/01. doi:10.1083/jcb.17.2.375.
  • Staehelin LA. Further observations on the fine structure of freeze-cleaved tight junctions. J Cell Sci. 1973;13(3):763–86.
  • Staehelin LA. Structure and function of intercellular junctions. Int Rev Cytol. 1974;39:191–283. doi:10.1016/S0074-7696(08)60940-7.
  • Furuse M. Molecular basis of the core structure of tight junctions. Cold Spring Harbor Perspectives Biol. 2010;2(1):a002907. doi:10.1101/cshperspect.a002907.
  • Gunzel D, Yu AS. Claudins and the modulation of tight junction permeability. Physiological reviews. 2013;93(2):525–69. Epub 2013/04/17. doi:10.1152/physrev.00019.2012.
  • Raleigh DR, Marchiando AM, Zhang Y, Shen L, Sasaki H, Wang Y, Long M, Turner JR. Tight junction-associated MARVEL proteins marveld3, tricellulin, and occludin have distinct but overlapping functions. Mol Biol Cell. 2010;21(7):1200–13. doi:10.1091/mbc.E09-08-0734.
  • Ikenouchi J, Furuse M, Furuse K, Sasaki H, Tsukita S, Tsukita S. Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J Cell Biol. 2005;171(6):939–45. doi:10.1083/jcb.200510043.
  • Garrido-Urbani S, Bradfield PF, Imhof BA. Tight junction dynamics: The role of junctional adhesion molecules (JAMs). Cell Tissue Res. 2014;355(3):701–15. doi:10.1007/s00441-014-1820-1.
  • Furuse M, Izumi Y, Oda Y, Higashi T, Iwamoto N. Molecular organization of tricellular tight junctions. Tissue barriers. 2014;2:e28960. doi:10.4161/tisb.28960.
  • Gonzalez-Mariscal LM, Ortega-Olvera JM, Gallego-Guitierrez H, Raya-Sandino A, Vargas-Sierra O. Involvement of tight junction plaque proteins in cancer. Curr Pathobiol Reports. 2016;4:117. doi:10.1007/s40139-016-0108-4.
  • Gonzalez-Mariscal LM, Ortega-Olvera JM, Gallego-Guitierrez H, Raya-Sandino A, Vargas-Sierra O. Zonula occludens proteins in cancer. Curr Pathobiol Reports. 2016;4:107. doi:10.1007/s40139-016-0109-3.
  • Gonzalez-Mariscal L, Tapia R, Chamorro D. Crosstalk of tight junction components with signaling pathways. Biochim Et Biophys Acta. 2008;1778(3):729–56. Epub 2007/10/24. doi:10.1016/j.bbamem.2007.08.018.
  • Stevens RC, Cherezov V, Katritch V, Abagyan R, Kuhn P, Rosen H, Wüthrich K. The GPCR Network: A large-scale collaboration to determine human GPCR structure and function. Nat Rev Drug Discovery. 2013;12(1):25–34. doi:10.1038/nrd3859.
  • Luttrell LM, Lefkowitz RJ. The role of beta-arrestins in the termination and transduction of G-protein-coupled receptor signals. J Cell Sci. 2002;115(Pt 3):455–65.
  • Wu J, Xie N, Zhao X, Nice EC, Huang C. Dissection of aberrant GPCR signaling in tumorigenesis–a systems biology approach. Cancer genomics & proteomics. 2012;9(1):37–50.
  • Balda MS, Gonzalez-Mariscal L, Contreras RG, Macias-Silva M, Torres-Marquez ME, Garcia-Sainz JA, Cereijido M. Assembly and sealing of tight junctions: possible participation of G-proteins, phospholipase C, protein kinase C and calmodulin. J Membrane Biol. 1991;122(3):193–202. doi:10.1007/BF01871420.
  • Meyer TN, Schwesinger C, Denker BM. Zonula occludens-1 is a scaffolding protein for signaling molecules. Galpha(12) directly binds to the Src homology 3 domain and regulates paracellular permeability in epithelial cells. J Biol Chem. 2002;277(28):24855–8. doi:10.1074/jbc.C200240200.
  • Sabath E, Negoro H, Beaudry S, Paniagua M, Angelow S, Shah J, Grammatikakis N, Yu AS, Denker BM. Galpha12 regulates protein interactions within the MDCK cell tight junction and inhibits tight-junction assembly. J Cell Sci. 2008;121(Pt 6):814–24. doi:10.1242/jcs.014878.
  • Denker BM, Saha C, Khawaja S, Nigam SK. Involvement of a heterotrimeric G protein alpha subunit in tight junction biogenesis. J Biol Chem. 1996;271(42):25750–3. doi:10.1074/jbc.271.42.25750.
  • Saha C, Nigam SK, Denker BM. Involvement of Galphai2 in the maintenance and biogenesis of epithelial cell tight junctions. J Biol Chem. 1998;273(34):21629–33. doi:10.1074/jbc.273.34.21629.
  • Tuteja N. Signaling through G protein coupled receptors. Plant Signal Behav. 2009;4(10):942–7. doi:10.4161/psb.4.10.9530.
  • Mohebbi N, Benabbas C, Vidal S, Daryadel A, Bourgeois S, Velic A, Ludwig MG, Seuwen K, Wagner CA. The proton-activated G protein coupled receptor OGR1 acutely regulates the activity of epithelial proton transport proteins. Cell Physiol Biochem. 2012;29(3-4):313–24. doi:10.1159/000338486.
  • Ludwig MG, Vanek M, Guerini D, Gasser JA, Jones CE, Junker U, Hofstetter H, Wolf RM, Seuwen K. Proton-sensing G-protein-coupled receptors. Nature. 2003;425(6953):93–8. doi:10.1038/nature01905.
  • de Valliere C, Vidal S, Clay I, Jurisic G, Tcymbarevich I, Lang S, Ludwig MG, Okoniewski M, Eloranta JJ, Kullak-Ublick GA, et al. The pH-sensing receptor OGR1 improves barrier function of epithelial cells and inhibits migration in an acidic environment. Am J Physiol Gastrointestinal Liver Physiol. 2015;309(6):G475–90. doi:10.1152/ajpgi.00408.2014.
  • de Valliere C Wang Y, Eloranta JJ, Vidal S, Clay I, Spalinger MR, Tcymbarevich I, Terhalle A, Ludwig MG, Suply T, et al. G Protein-coupled pH-sensing Receptor OGR1 Is a Regulator of Intestinal Inflammation. Inflammatory Bowel Dis. 2015;21(6):1269–81.
  • Roohani N, Hurrell R, Kelishadi R, Schulin R. Zinc and its importance for human health: An integrative review. J Res Med Sci. 2013;18(2):144–57.
  • Besser L, Chorin E, Sekler I, Silverman WF, Atkin S, Russell JT, Hershfinkel M. Synaptically released zinc triggers metabotropic signaling via a zinc-sensing receptor in the hippocampus. J Neurosci Official J Soc Neurosci. 2009;29(9):2890–901. doi:10.1523/JNEUROSCI.5093-08.2009.
  • Moechars D, Depoortere I, Moreaux B, de Smet B, Goris I, Hoskens L, Daneels G, Kass S, Ver Donck L, Peeters T, et al. Altered gastrointestinal and metabolic function in the GPR39-obestatin receptor-knockout mouse. Gastroenterology. 2006;131(4):1131–41. doi:10.1053/j.gastro.2006.07.009.
  • Hershfinkel M, Moran A, Grossman N, Sekler I. A zinc-sensing receptor triggers the release of intracellular Ca2+ and regulates ion transport. Proc Natl Acad Sci U S A. 2001;98(20):11749–54. doi:10.1073/pnas.201193398.
  • McKee KK, Tan CP, Palyha OC, Liu J, Feighner SD, Hreniuk DL, Smith RG, Howard AD, Van der Ploeg LH. Cloning and characterization of two human G protein-coupled receptor genes (GPR38 and GPR39) related to the growth hormone secretagogue and neurotensin receptors. Genomics. 1997;46(3):426–34. doi:10.1006/geno.1997.5069.
  • Zhang JV, Ren PG, Avsian-Kretchmer O, Luo CW, Rauch R, Klein C, Hsueh AJ. Obestatin, a peptide encoded by the ghrelin gene, opposes ghrelin's effects on food intake. Science. 2005;310(5750):996–9. doi:10.1126/science.1117255.
  • Cohen L, Sekler I, Hershfinkel M. The zinc sensing receptor, ZnR/GPR39, controls proliferation and differentiation of colonocytes and thereby tight junction formation in the colon. Cell Death Dis. 2014;5:e1307. doi:10.1038/cddis.2014.262.
  • Sunuwar L, Medini M, Cohen L, Sekler I, Hershfinkel M. The zinc sensing receptor, ZnR/GPR39, triggers metabotropic calcium signalling in colonocytes and regulates occludin recovery in experimental colitis. Philos Trans R Soc Lond B Biol Sci. 2016;371(1700):20150420. doi:10.1098/rstb.2015.0420.
  • Shao YX, Lei Z, Wolf PG, Gao Y, Guo YM, Zhang BK. Zinc Supplementation, via GPR39, Upregulates PKCzeta to Protect Intestinal Barrier Integrity in Caco-2 Cells Challenged by Salmonella enterica Serovar Typhimurium. J Nutr. 2017;147:1282. doi:10.3945/jn.116.243238.
  • Sharir H, Zinger A, Nevo A, Sekler I, Hershfinkel M. Zinc released from injured cells is acting via the Zn2+-sensing receptor, ZnR, to trigger signaling leading to epithelial repair. J Biol Chem. 2010;285(34):26097–106. doi:10.1074/jbc.M110.107490.
  • Greger R. Ion transport mechanisms in thick ascending limb of Henle's loop of mammalian nephron. Physiol Rev. 1985;65(3):760–97.
  • Hou J, Renigunta A, Gomes AS, Hou M, Paul DL, Waldegger S, Goodenough DA. Claudin-16 and claudin-19 interaction is required for their assembly into tight junctions and for renal reabsorption of magnesium. Proc Natl Acad Sci U S A. 2009;106(36):15350–5. doi:10.1073/pnas.0907724106.
  • Hou J, Renigunta A, Konrad M, Gomes AS, Schneeberger EE, Paul DL, Waldegger S, Goodenough DA. Claudin-16 and claudin-19 interact and form a cation-selective tight junction complex. J Clin Invest. 2008;118(2):619–28.
  • Gong Y, Renigunta V, Himmerkus N, Zhang J, Renigunta A, Bleich M, Hou J. Claudin-14 regulates renal Ca(+)(+) transport in response to CaSR signalling via a novel microRNA pathway. EMBO J. 2012;31(8):1999–2012. doi:10.1038/emboj.2012.49.
  • Ikari A, Okude C, Sawada H, Sasaki Y, Yamazaki Y, Sugatani J, Degawa M, Miwa M. Activation of a polyvalent cation-sensing receptor decreases magnesium transport via claudin-16. Biochim Et Biophys Acta. 2008;1778(1):283–90. doi:10.1016/j.bbamem.2007.10.002.
  • Toka HR, Al-Romaih K, Koshy JM, DiBartolo S, 3rd Kos CH, Quinn SJ, Curhan GC, Mount DB, Brown EM, Pollak MR. Deficiency of the calcium-sensing receptor in the kidney causes parathyroid hormone-independent hypocalciuria. J Am Soc Nephrol. 2012;23(11):1879–90. doi:10.1681/ASN.2012030323.
  • Gong Y, Hou J. Claudin-14 underlies Ca(+)(+)-sensing receptor-mediated Ca(+)(+) metabolism via NFAT-microRNA-based mechanisms. J Am Soc Nephrol. 2014;25(4):745–60. doi:10.1681/ASN.2013050553.
  • Gong Y, Himmerkus N, Plain A, Bleich M, Hou J. Epigenetic regulation of microRNAs controlling CLDN14 expression as a mechanism for renal calcium handling. J Am Soc Nephrol. 2015;26(3):663–76. doi:10.1681/ASN.2014020129.
  • Troy TC, Li Y, O'Malley L, Turksen K. The temporal and spatial expression of Claudins in epidermal development and the accelerated program of epidermal differentiation in K14-CaSR transgenic mice. Gene Expression Patterns: GEP. 2007;7(4):423–30. doi:10.1016/j.modgep.2006.11.006.
  • Jouret F, Wu J, Hull M, Rajendran V, Mayr B, Schofl C, Geibel J, Caplan MJ. Activation of the Ca(2)+-sensing receptor induces deposition of tight junction components to the epithelial cell plasma membrane. J Cell Sci. 2013;126(Pt 22):5132–42. doi:10.1242/jcs.127555.
  • Muanprasat C, Wongkrasant P, Satitsri S, Moonwiriyakit A, Pongkorpsakol P, Mattaveewong T, Pichyangkura R, Chatsudthipong V. Activation of AMPK by chitosan oligosaccharide in intestinal epithelial cells: Mechanism of action and potential applications in intestinal disorders. Biochem Pharmacol. 2015;96(3):225–36. doi:10.1016/j.bcp.2015.05.016.
  • Garcia-Ponce A, Chanez Paredes S, Castro Ochoa KF, Schnoor M. Regulation of endothelial and epithelial barrier functions by peptide hormones of the adrenomedullin family. Tissue Barriers. 2016;4(4):e1228439. doi:10.1080/21688370.2016.1228439.
  • Koyama T, Ochoa-Callejero L, Sakurai T, Kamiyoshi A, Ichikawa-Shindo Y, Iinuma N, Arai T, Yoshizawa T, Iesato Y, Lei Y, et al. Vascular endothelial adrenomedullin-RAMP2 system is essential for vascular integrity and organ homeostasis. Circulation. 2013;127(7):842–53. doi:10.1161/CIRCULATIONAHA.112.000756.
  • Garcia Ponce A, Citalan Madrid AF, Vargas Robles H, Chanez Paredes S, Nava P, Betanzos A, Zarbock A, Rottner K, Vestweber D, Schnoor M. Loss of cortactin causes endothelial barrier dysfunction via disturbed adrenomedullin secretion and actomyosin contractility. Scientific Reports. 2016;6:29003. doi:10.1038/srep29003.
  • Hippenstiel S, Witzenrath M, Schmeck B, Hocke A, Krisp M, Krull M, Seybold J, Seeger W, Rascher W, Schütte H, et al. Adrenomedullin reduces endothelial hyperpermeability. Circulation Res. 2002;91(7):618–25. doi:10.1161/01.RES.0000036603.61868.F9.
  • Aslam M, Pfeil U, Gunduz D, Rafiq A, Kummer W, Piper HM, Noll T. Intermedin (adrenomedullin2) stabilizes the endothelial barrier and antagonizes thrombin-induced barrier failure in endothelial cell monolayers. Br J Pharmacol. 2012;165(1):208–22. doi:10.1111/j.1476-5381.2011.01540.x.
  • Aslam M, Gunduz D, Schuler D, Li L, Sharifpanah F, Sedding D, Piper HM, Noll T. Intermedin induces loss of coronary microvascular endothelial barrier via derangement of actin cytoskeleton: role of RhoA and Rac1. Cardiovascular Res. 2011;92(2):276–86. doi:10.1093/cvr/cvr213.
  • Muller-Redetzky HC, Kummer W, Pfeil U, Hellwig K, Will D, Paddenberg R, Tabeling C, Hippenstiel S, Suttorp N, Witzenrath M. Intermedin stabilized endothelial barrier function and attenuated ventilator-induced lung injury in mice. PloS One. 2012;7(5):e35832. doi:10.1371/journal.pone.0035832.
  • Dunworth WP, Fritz-Six KL, Caron KM. Adrenomedullin stabilizes the lymphatic endothelial barrier in vitro and in vivo. Peptides. 2008;29(12):2243–9. doi:10.1016/j.peptides.2008.09.009.
  • Hoopes SL, Willcockson HH, Caron KM. Characteristics of multi-organ lymphangiectasia resulting from temporal deletion of calcitonin receptor-like receptor in adult mice. PloS One. 2012;7(9):e45261. doi:10.1371/journal.pone.0045261.
  • Honda M, Nakagawa S, Hayashi K, Kitagawa N, Tsutsumi K, Nagata I, Niwa M. Adrenomedullin improves the blood-brain barrier function through the expression of claudin-5. Cell Mol Neurobiol. 2006;26(2):109–18. doi:10.1007/s10571-006-9028-x.
  • Kis B, Deli MA, Kobayashi H, Abraham CS, Yanagita T, Kaiya H, Isse T, Nishi R, Gotoh S, Kangawa K, et al. Adrenomedullin regulates blood-brain barrier functions in vitro. Neuroreport. 2001;12(18):4139–42. doi:10.1097/00001756-200112210-00055.
  • Kis B, Snipes JA, Deli MA, Abraham CS, Yamashita H, Ueta Y, Busija DW. Chronic adrenomedullin treatment improves blood-brain barrier function but has no effects on expression of tight junction proteins. Acta Neurochirurgica Supplement. 2003;86:565–8.
  • Imai A, Toriyama Y, Iesato Y, Hirabayashi K, Sakurai T, Kamiyoshi A, Ichikawa-Shindo Y, Kawate H, Tanaka M, Liu T, et al. Adrenomedullin suppresses vascular endothelial growth factor-induced vascular Hyperpermeability and inflammation in retinopathy. Am J Pathol. 2017;187(5):999–1015. doi:10.1016/j.ajpath.2017.01.014.
  • Xiao F, Wang LJ, Zhao H, Tan C, Wang DN, Zhang H, Wei YG, Liu J, Zhang W. Intermedin restricts vessel sprouting by inhibiting the loosening of endothelial junction. Biochem Biophys Res Commun. 2015;458(1):174–9. doi:10.1016/j.bbrc.2015.01.090.
  • Ashizuka S, Inagaki-Ohara K, Kuwasako K, Kato J, Inatsu H, Kitamura K. Adrenomedullin treatment reduces intestinal inflammation and maintains epithelial barrier function in mice administered dextran sulphate sodium. Microbiol Immunol. 2009;53(10):573–81. doi:10.1111/j.1348-0421.2009.00159.x.
  • Yi Z, Fan H, Liu X, Tang Q, Zuo D, Yang J. Adrenomedullin improves intestinal epithelial barrier function by downregulating myosin light chain phosphorylation in ulcerative colitis rats. Mol Med Reports. 2015;12(3):3615–20. doi:10.3892/mmr.2015.3887.
  • Temmesfeld-Wollbruck B, Brell B, zu Dohna C, Dorenberg M, Hocke AC, Martens H, Klar J, Suttorp N, Hippenstiel S. Adrenomedullin reduces intestinal epithelial permeability in vivo and in vitro. Am J Physiol Gastrointestinal Liver Physiol. 2009;297(1):G43–51. doi:10.1152/ajpgi.90532.2008.
  • Basivireddy J, Somvanshi RK, Romero IA, Weksler BB, Couraud PO, Oger J, Kumar U. Somatostatin preserved blood brain barrier against cytokine induced alterations: possible role in multiple sclerosis. Biochem Pharmacol. 2013;86(4):497–507. doi:10.1016/j.bcp.2013.06.001.
  • Lei S, Cheng T, Guo Y, Li C, Zhang W, Zhi F. Somatostatin ameliorates lipopolysaccharide-induced tight junction damage via the ERK-MAPK pathway in Caco2 cells. Eur J Cell Biol. 2014;93(7):299–307. doi:10.1016/j.ejcb.2014.05.003.
  • Liew CW, Vockel M, Glassmeier G, Brandner JM, Fernandez-Ballester GJ, Schwarz JR, Schulz S, Buck F, Serrano L, Richter D, et al. Interaction of the human somatostatin receptor 3 with the multiple PDZ domain protein MUPP1 enables somatostatin to control permeability of epithelial tight junctions. FEBS Letters. 2009;583(1):49–54. doi:10.1016/j.febslet.2008.11.048.
  • Vockel M, Breitenbach U, Kreienkamp HJ, Brandner JM. Somatostatin regulates tight junction function and composition in human keratinocytes. Exp Dermatol. 2010;19(10):888–94. doi:10.1111/j.1600-0625.2010.01101.x.
  • Van Itallie C, Rahner C, Anderson JM. Regulated expression of claudin-4 decreases paracellular conductance through a selective decrease in sodium permeability. J Clin Invest. 2001;107(10):1319–27. doi:10.1172/JCI12464.
  • Fukuda S, Nakagawa S, Tatsumi R, Morofuji Y, Takeshita T, Hayashi K, Tanaka K, Matsuo T, Niwa M. Glucagon-Like Peptide-1 strengthens the barrier integrity in primary cultures of rat brain endothelial cells under basal and hyperglycemia conditions. J Mol Neurosci. 2016;59(2):211–9. doi:10.1007/s12031-015-0696-1.
  • Fan Y, Liu K, Wang Q, Ruan Y, Ye W, Zhang Y. Exendin-4 alleviates retinal vascular leakage by protecting the blood-retinal barrier and reducing retinal vascular permeability in diabetic Goto-Kakizaki rats. Exp Eye Res. 2014;127:104–16. doi:10.1016/j.exer.2014.05.004.
  • Rossi S, Maisto R, Gesualdo C, Trotta MC, Ferraraccio F, Kaneva MK, Getting SJ, Surace E, Testa F, Simonelli F, et al. Activation of melanocortin receptors MC 1 and MC 5 attenuates retinal damage in experimental diabetic retinopathy. Mediators Inflammation. 2016;2016:7368389. doi:10.1155/2016/7368389.
  • Manna SK, Aggarwal BB. Alpha-melanocyte-stimulating hormone inhibits the nuclear transcription factor NF-kappa B activation induced by various inflammatory agents. J Immunol. 1998;161(6):2873–80.
  • Iizuka Y, Okuno T, Saeki K, Uozaki H, Okada S, Misaka T, Sato T, Toh H, Fukayama M, Takeda N, et al. Protective role of the leukotriene B4 receptor BLT2 in murine inflammatory colitis. FASEB J Official Publication Federation Am Soc Exp Biol. 2010;24(12):4678–90. doi:10.1096/fj.10-165050.
  • Ishii Y, Saeki K, Liu M, Sasaki F, Koga T, Kitajima K, Meno C, Okuno T, Yokomizo T. Leukotriene B4 receptor type 2 (BLT2) enhances skin barrier function by regulating tight junction proteins. FASEB J Official Publication Federation Am Soc Exp Biol. 2016;30(2):933–47. doi:10.1096/fj.15-279653.
  • Chiba T, Nakahara T, Hashimoto-Hachiya A, Yokomizo T, Uchi H, Furue M. The leukotriene B4 receptor BLT2 protects barrier function via actin polymerization with phosphorylation of myosin phosphatase target subunit 1 in human keratinocytes. Exp Dermatol. 2016;25(7):532–6. doi:10.1111/exd.12976.
  • Grumbach Y, Quynh NV, Chiron R, Urbach V. LXA4 stimulates ZO-1 expression and transepithelial electrical resistance in human airway epithelial (16HBE14o-) cells. Am J Physiol Lung Cell Mol Physiol. 2009;296(1):L101–8. doi:10.1152/ajplung.00018.2008.
  • Higgins G, Fustero Torre C, Tyrrell J, McNally P, Harvey BJ, Urbach V. Lipoxin A4 prevents tight junction disruption and delays the colonization of cystic fibrosis bronchial epithelial cells by Pseudomonas aeruginosa. Am J Physiol Lung Cell Mol Physiol. 2016;310(11):L1053–61. doi:10.1152/ajplung.00368.2015.
  • Lu TS, Avraham HK, Seng S, Tachado SD, Koziel H, Makriyannis A, Avraham S. Cannabinoids inhibit HIV-1 Gp120-mediated insults in brain microvascular endothelial cells. J Immunol. 2008;181(9):6406–16. doi:10.4049/jimmunol.181.9.6406.
  • Yang MC, Zhang HZ, Wang Z, You FL, Wang YF. The molecular mechanism and effect of cannabinoid-2 receptor agonist on the blood-spinal cord barrier permeability induced by ischemia-reperfusion injury. Brain Res. 2016;1636:81–92. doi:10.1016/j.brainres.2016.01.047.
  • Ramirez SH, Hasko J, Skuba A, Fan S, Dykstra H, McCormick R, Reichenbach N, Krizbai I, Mahadevan A, Zhang M, et al. Activation of cannabinoid receptor 2 attenuates leukocyte-endothelial cell interactions and blood-brain barrier dysfunction under inflammatory conditions. J Neurosci Official J Soc Neurosci. 2012;32(12):4004–16. doi:10.1523/JNEUROSCI.4628-11.2012.
  • Fujii M, Sherchan P, Krafft PR, Rolland WB, Soejima Y, Zhang JH. Cannabinoid type 2 receptor stimulation attenuates brain edema by reducing cerebral leukocyte infiltration following subarachnoid hemorrhage in rats. J Neurol Sci. 2014;342(1-2):101–6. doi:10.1016/j.jns.2014.04.034.
  • Feng YJ, Li YY, Lin XH, Li K, Cao MH. Anti-inflammatory effect of cannabinoid agonist WIN55, 212 on mouse experimental colitis is related to inhibition of p38MAPK. World J Gastroenterol. 2016;22(43):9515–24. doi:10.3748/wjg.v22.i43.9515.
  • Alhamoruni A, Lee AC, Wright KL, Larvin M, O'Sullivan SE. Pharmacological effects of cannabinoids on the Caco-2 cell culture model of intestinal permeability. J Pharmacol Exp Therapeutics. 2010;335(1):92–102. doi:10.1124/jpet.110.168237.
  • Yang YY, Hsieh SL, Lee PC, Yeh YC, Lee KC, Hsieh YC, Wang YW, Lee TY, Huang YH, Chan CC, et al. Long-term cannabinoid type 2 receptor agonist therapy decreases bacterial translocation in rats with cirrhosis and ascites. J Hepatol. 2014;61(5):1004–13. doi:10.1016/j.jhep.2014.05.049.
  • Shang VC, Kendall DA, Roberts RE. Delta9-Tetrahydrocannabinol reverses TNFalpha-induced increase in airway epithelial cell permeability through CB2 receptors. Biochem Pharmacol. 2016;120:63–71. doi:10.1016/j.bcp.2016.09.008.
  • Fujii M, Sherchan P, Soejima Y, Doycheva D, Zhao D, Zhang JH. Cannabinoid Receptor Type 2 Agonist Attenuates Acute Neurogenic Pulmonary Edema by Preventing Neutrophil Migration after Subarachnoid Hemorrhage in Rats. Acta Neurochirurgica Supplement. 2016;121:135–9. doi:10.1007/978-3-319-18497-5_24.
  • Barutta F, Corbelli A, Mastrocola R, Gambino R, Di Marzo V, Pinach S, Rastaldi MP, Perin PC, Gruden G. Cannabinoid receptor 1 blockade ameliorates albuminuria in experimental diabetic nephropathy. Diabetes. 2010;59(4):1046–54. doi:10.2337/db09-1336.
  • Miyamoto J, Mizukure T, Park SB, Kishino S, Kimura I, Hirano K, Bergamo P, Rossi M, Suzuki T, Arita, et al. A gut microbial metabolite of linoleic acid, 10-hydroxy-cis-12-octadecenoic acid, ameliorates intestinal epithelial barrier impairment partially via GPR40-MEK-ERK pathway. J Biol Chem. 2015;290(5):2902–18. doi:10.1074/jbc.M114.610733.
  • 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(17):17286–93. doi:10.1074/jbc.M412427200.
  • Feistritzer C, Riewald M. Endothelial barrier protection by activated protein C through PAR1-dependent sphingosine 1-phosphate receptor-1 crossactivation. Blood. 2005;105(8):3178–84. doi:10.1182/blood-2004-10-3985.
  • Wang L, Bittman R, Garcia JG, Dudek SM. Junctional complex and focal adhesion rearrangement mediates pulmonary endothelial barrier enhancement by FTY720 S-phosphonate. Microvasc Res. 2015;99:102–9. doi:10.1016/j.mvr.2015.03.007.
  • Fan L, Yan H. FTY720 attenuates retinal inflammation and protects blood-retinal barrier in diabetic rats. Invest Ophthalmol Visual Sci. 2016;57(3):1254–63. doi:10.1167/iovs.15-18658.
  • Altay O, Suzuki H, Hasegawa Y, Caner B, Krafft PR, Fujii M, Tang J, Zhang JH. Isoflurane attenuates blood-brain barrier disruption in ipsilateral hemisphere after subarachnoid hemorrhage in mice. Stroke J Cerebral Circulation. 2012;43(9):2513–6. doi:10.1161/STROKEAHA.112.661728.
  • Dong J, Wang H, Zhao J, Sun J, Zhang T, Zuo L, Zhu W, Gong J, Li Y, Gu L, Li J. SEW2871 protects from experimental colitis through reduced epithelial cell apoptosis and improved barrier function in interleukin-10 gene-deficient mice. Immunol Res. 2015;61(3):303–11. doi:10.1007/s12026-015-8625-5.
  • 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(1):95–107. doi:10.1113/expphysiol.2014.082149.
  • Chen T, Huang Z, Liu R, Yang J, Hylemon PB, Zhou H. Sphingosine-1 phosphate promotes intestinal epithelial cell proliferation via S1PR2. Front Biosci (Landmark Ed). 2017;22:596–608. doi:10.2741/4505.
  • Rosales MA, Silva KC, Duarte DA, Rossato FA, Lopes de Faria JB, Lopes de Faria JM. Endocytosis of tight junctions caveolin nitrosylation dependent is improved by cocoa via opioid receptor on RPE cells in diabetic conditions. Invest Ophthalmol Visual Sci. 2014;55(9):6090–100. doi:10.1167/iovs.14-14234.
  • Patel N, Itakura T, Gonzalez JM, Jr, Schwartz SG, Fini ME. GPR158, an orphan member of G protein-coupled receptor Family C: glucocorticoid-stimulated expression and novel nuclear role. PloS one. 2013;8(2):e57843. doi:10.1371/journal.pone.0057843.
  • Kiatsurayanon C, Niyonsaba F, Smithrithee R, Akiyama T, Ushio H, Hara M, Okumura K, Ikeda S, Ogawa H. Host defense (Antimicrobial) peptide, human beta-defensin-3, improves the function of the epithelial tight-junction barrier in human keratinocytes. J Invest Dermatol. 2014;134(8):2163–73. doi:10.1038/jid.2014.143.
  • Chen Y, Zhang Y, Tang J, Liu F, Hu Q, Luo C, Tang J, Feng H, Zhang JH. Norrin protected blood-brain barrier via frizzled-4/beta-catenin pathway after subarachnoid hemorrhage in rats. Stroke J Cerebral Circulation. 2015;46(2):529–36. doi:10.1161/STROKEAHA.114.007265.
  • Wang Y, Rattner A, Zhou Y, Williams J, Smallwood PM, Nathans J. Norrin/Frizzled4 signaling in retinal vascular development and blood brain barrier plasticity. Cell. 2012;151(6):1332–44. doi:10.1016/j.cell.2012.10.042.
  • Ye X, Wang Y, Cahill H, Yu M, Badea TC, Smallwood PM, Peachey NS, Nathans J. Norrin, frizzled-4, and Lrp5 signaling in endothelial cells controls a genetic program for retinal vascularization. Cell. 2009;139(2):285–98. doi:10.1016/j.cell.2009.07.047.
  • Paes KT, Wang E, Henze K, Vogel P, Read R, Suwanichkul A, Kirkpatrick LL, Potter D, Newhouse MM, Rice DS. Frizzled 4 is required for retinal angiogenesis and maintenance of the blood-retina barrier. Invest Ophthalmol Visual Sci. 2011;52(9):6452–61. doi:10.1167/iovs.10-7146.
  • Campbell M, Humphries M, Kennan A, Kenna P, Humphries P, Brankin B. Aberrant retinal tight junction and adherens junction protein expression in an animal model of autosomal dominant Retinitis pigmentosa: the Rho(-/-) mouse. Exp Eye Res. 2006;83(3):484–92. doi:10.1016/j.exer.2006.01.032.
  • Omri S, Omri B, Savoldelli M, Jonet L, Thillaye-Goldenberg B, Thuret G, Gain P, Jeanny JC, Crisanti P, Behar-Cohen F. The outer limiting membrane (OLM) revisited: clinical implications. Clin Ophthalmol. 2010;4:183–95.
  • Shah GV, Thomas S, Muralidharan A, Liu Y, Hermonat PL, Williams J, Chaudhary J. Calcitonin promotes in vivo metastasis of prostate cancer cells by altering cell signaling, adhesion, and inflammatory pathways. Endocr Relat Cancer. 2008;15(4):953–64. doi:10.1677/ERC-08-0136.
  • Shah GV, Muralidharan A, Gokulgandhi M, Soan K, Thomas S. Cadherin switching and activation of beta-catenin signaling underlie proinvasive actions of calcitonin-calcitonin receptor axis in prostate cancer. J Biol Chem. 2009;284(2):1018–30. doi:10.1074/jbc.M807823200.
  • Aljameeli A, Thakkar A, Thomas S, Lakshmikanthan V, Iczkowski KA, Shah GV. Calcitonin Receptor-Zonula Occludens-1 Interaction Is Critical for Calcitonin-Stimulated Prostate Cancer Metastasis. PloS One. 2016;11(3):e0150090. doi:10.1371/journal.pone.0150090.
  • Aljameeli A, Thakkar A, Shah G. Calcitonin receptor increases invasion of prostate cancer cells by recruiting zonula occludens-1 and promoting PKA-mediated TJ disassembly. Cell Signal. 2017;36:1–13. doi:10.1016/j.cellsig.2017.04.008.
  • Wu L, Oshima T, Tomita T, Ohda Y, Fukui H, Watari J, Miwa H. Serotonin disrupts esophageal mucosal integrity: an investigation using a stratified squamous epithelial model. J Gastroenterol. 2016;51(11):1040–9. doi:10.1007/s00535-016-1195-z.
  • Stull MA, Pai V, Vomachka AJ, Marshall AM, Jacob GA, Horseman ND. Mammary gland homeostasis employs serotonergic regulation of epithelial tight junctions. Proc Natl Acad Sci U S A. 2007;104(42):16708–13. doi:10.1073/pnas.0708136104.
  • Pai VP, Horseman ND. Biphasic regulation of mammary epithelial resistance by serotonin through activation of multiple pathways. J Biol Chem. 2008;283(45):30901–10. doi:10.1074/jbc.M802476200.
  • Cong X, Zhang Y, Li J, Mei M, Ding C, Xiang RL, Zhang LW, Wang Y, Wu LL, Yu GY. Claudin-4 is required for modulation of paracellular permeability by muscarinic acetylcholine receptor in epithelial cells. J Cell Sci. 2015;128(12):2271–86. doi:10.1242/jcs.165878.
  • Takeuchi K, Kishioka C, Ishinaga H, Sakakura Y, Majima Y. Histamine alters gene expression in cultured human nasal epithelial cells. J Allergy Clin Immunol. 2001;107(2):310–4. doi:10.1067/mai.2001.112127.
  • Canonica GW, Blaiss M. Antihistaminic, anti-inflammatory, and antiallergic properties of the nonsedating second-generation antihistamine desloratadine: a review of the evidence. World Allergy Organ J. 2011;4(2):47–53. doi:10.1097/WOX.0b013e3182093e19.
  • Hirase T, Kawashima S, Wong EY, Ueyama T, Rikitake Y, Tsukita S, Yokoyama M, Staddon JM. Regulation of tight junction permeability and occludin phosphorylation by Rhoa-p160ROCK-dependent and -independent mechanisms. J Biol Chem. 2001;276(13):10423–31. doi:10.1074/jbc.M007136200.
  • Breslin JW. ROCK and cAMP promote lymphatic endothelial cell barrier integrity and modulate histamine and thrombin-induced barrier dysfunction. Lymphatic Res Biol. 2011;9(1):3–11. doi:10.1089/lrb.2010.0016.
  • Sato M, Sasaki N, Ato M, Hirakawa S, Sato K, Sato K. Microcirculation-on-a-Chip: A Microfluidic Platform for Assaying Blood- and Lymphatic-Vessel Permeability. PloS one. 2015;10(9):e0137301. doi:10.1371/journal.pone.0137301.
  • Wang Z, Cai XJ, Qin J, Xie FJ, Han N, Lu HY. The role of histamine in opening blood-tumor barrier. Oncotarget. 2016;7(21):31299–310. doi:10.18632/oncotarget.8896.
  • Guo M, Breslin JW, Wu MH, Gottardi CJ, Yuan SY. VE-cadherin and beta-catenin binding dynamics during histamine-induced endothelial hyperpermeability. Am J Physiol Cell Physiol. 2008;294(4):C977–84. doi:10.1152/ajpcell.90607.2007.
  • Ratcliffe MJ, Smales C, Staddon JM. Dephosphorylation of the catenins p120 and p100 in endothelial cells in response to inflammatory stimuli. Biochem J. 1999;338 (Pt 2):471–8. doi:10.1042/bj3380471.
  • Shasby DM, Ries DR, Shasby SS, Winter MC. Histamine stimulates phosphorylation of adherens junction proteins and alters their link to vimentin. Am J Physiol Lung Cell Mol Physiol 2002;282(6):L1330–8. doi:10.1152/ajplung.00329.2001.
  • Lennon FE, Mirzapoiazova T, Mambetsariev B, Poroyko VA, Salgia R, Moss J, Singleton PA. The Mu opioid receptor promotes opioid and growth factor-induced proliferation, migration and Epithelial Mesenchymal Transition (EMT) in human lung cancer. PloS One. 2014;9(3):e91577. doi:10.1371/journal.pone.0091577.
  • Biki B, Mascha E, Moriarty DC, Fitzpatrick JM, Sessler DI, Buggy DJ. Anesthetic technique for radical prostatectomy surgery affects cancer recurrence: a retrospective analysis. Anesthesiology. 2008;109(2):180–7. doi:10.1097/ALN.0b013e31817f5b73.
  • Christopherson R, James KE, Tableman M, Marshall P, Johnson FE. Long-term survival after colon cancer surgery: a variation associated with choice of anesthesia. Anesthesia Analgesia. 2008;107(1):325–32. doi:10.1213/ane.0b013e3181770f55.
  • Zhang K, Tian L, Liu L, Feng Y, Dong YB, Li B, Shang DS, Fang WG, Cao YP, Chen YH. CXCL1 contributes to beta-amyloid-induced transendothelial migration of monocytes in Alzheimer's disease. PloS one. 2013;8(8):e72744. doi:10.1371/journal.pone.0072744.
  • Huang J, Li Y, Tang Y, Tang G, Yang GY, Wang Y. CXCR4 antagonist AMD3100 protects blood-brain barrier integrity and reduces inflammatory response after focal ischemia in mice. Stroke J Cerebral Circulation. 2013;44(1):190–7. doi:10.1161/STROKEAHA.112.670299.
  • Xia XM, Wang FY, Zhou J, Hu KF, Li SW, Zou BB. CXCR4 antagonist AMD3100 modulates claudin expression and intestinal barrier function in experimental colitis. PloS one. 2011;6(11):e27282. doi:10.1371/journal.pone.0027282.
  • Lammers KM, Lu R, Brownley J, Lu B, Gerard C, Thomas K, Rallabhandi P, Shea-Donohue T, Tamiz A, Alkan S, et al. Gliadin induces an increase in intestinal permeability and zonulin release by binding to the chemokine receptor CXCR3. Gastroenterology. 2008;135(1):194–204 e3. doi:10.1053/j.gastro.2008.03.023.
  • Stamatovic SM, Shakui P, Keep RF, Moore BB, Kunkel SL, Van Rooijen N Andjelkovic AV. Monocyte chemoattractant protein-1 regulation of blood-brain barrier permeability. J Cereb Blood Flow Metab. 2005;25(5):593–606. doi:10.1038/sj.jcbfm.9600055.
  • Stamatovic SM, Keep RF, Kunkel SL, Andjelkovic AV. Potential role of MCP-1 in endothelial cell tight junction 'opening': Signaling via Rho and Rho kinase. Journal of cell science. 2003;116(Pt 22):4615–28. doi:10.1242/jcs.00755.
  • Dimitrijevic OB, Stamatovic SM, Keep RF, Andjelkovic AV. Effects of the chemokine CCL2 on blood-brain barrier permeability during ischemia-reperfusion injury. J Cereb Blood Flow Metab. 2006;26(6):797–810. doi:10.1038/sj.jcbfm.9600229.
  • Jamaluddin MS, Wang X, Wang H, Rafael C, Yao Q, Chen C. Eotaxin increases monolayer permeability of human coronary artery endothelial cells. Arterioscler Thromb Vasc Biol. 2009;29(12):2146–52. doi:10.1161/ATVBAHA.109.194134.
  • Mahajan SD, Parikh NU, Woodruff TM, Jarvis JN, Lopez M, Hennon T, Cunningham P, Quigg RJ, Schwartz SA, Alexander JJ. C5a alters blood-brain barrier integrity in a human in vitro model of systemic lupus erythematosus. Immunology. 2015;146(1):130–43. doi:10.1111/imm.12489.
  • Jacob A, Hack B, Chen P, Quigg RJ, Alexander JJ. C5a/CD88 signaling alters blood-brain barrier integrity in lupus through nuclear factor-kappaB. Journal of neurochemistry. 2011;119(5):1041–51. doi:10.1111/j.1471-4159.2011.07490.x.
  • Hu WH, Hu Z, Shen X, Dong LY, Zhou WZ, Yu XX. C5a receptor enhances hepatocellular carcinoma cell invasiveness via activating ERK1/2-mediated epithelial-mesenchymal transition. Exp Mol Pathol. 2016;100(1):101–8. doi:10.1016/j.yexmp.2015.10.001.
  • Kim JY, Ko AR, Hyun HW, Kang TC. ETB receptor-mediated MMP-9 activation induces vasogenic edema via ZO-1 protein degradation following status epilepticus. Neuroscience. 2015;304:355–67. doi:10.1016/j.neuroscience.2015.07.065.
  • Leung JW, Chung SS, Chung SK. Endothelial endothelin-1 over-expression using receptor tyrosine kinase tie-1 promoter leads to more severe vascular permeability and blood brain barrier breakdown after transient middle cerebral artery occlusion. Brain research. 2009;1266:121–9. doi:10.1016/j.brainres.2009.01.070.
  • Gene Family. G protein-coupled receptors, Class F frizzled (FZD). Available from: www.genenames.org/cgi-bin/genefamilies/set/286.
  • Li VS, Ng SS, Boersema PJ, Low TY, Karthaus WR, Gerlach JP, Mohammed S, Heck AJ, Maurice MM, Mahmoudi T, et al. Wnt signaling through inhibition of beta-catenin degradation in an intact Axin1 complex. Cell. 2012;149(6):1245–56. Epub 2012/06/12. doi:10.1016/j.cell.2012.05.002.
  • Clevers H, Nusse R. Wnt/beta-catenin signaling and disease. Cell. 2012;149(6):1192–205. doi:10.1016/j.cell.2012.05.012.
  • Ikenouchi J, Matsuda M, Furuse M, Tsukita S. Regulation of tight junctions during the epithelium-mesenchyme transition: Direct repression of the gene expression of claudins/occludin by Snail. Journal of cell science. 2003;116(Pt 10):1959–67. doi:10.1242/jcs.00389.
  • Zhou BP, Deng J, Xia W, Xu J, Li YM, Gunduz M, Hung MC. Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol. 2004;6(10):931–40. doi:10.1038/ncb1173.
  • Yook JI, Li XY, Ota I, Fearon ER, Weiss SJ. Wnt-dependent regulation of the E-cadherin repressor snail. Journal of biological chemistry. 2005;280(12):11740–8. doi:10.1074/jbc.M413878200.
  • Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Molecular and cellular biology. 2002;22(4):1172–83. doi:10.1128/MCB.22.4.1172-1183.2002.
  • Yook JI, Li XY, Ota I, Hu C, Kim HS, Kim NH, Fearon ER, Weiss SJ. A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells. Nat Cell Biol. 2006;8(12):1398–406. doi:10.1038/ncb1508.
  • Lu J, Zhang S, Nakano H, Simmons DG, Wang S, Kong S, Wang Q, Shen L, Tu Z, Wang W, et al. A positive feedback loop involving Gcm1 and Fzd5 directs chorionic branching morphogenesis in the placenta. PLoS biology. 2013;11(4):e1001536. doi:10.1371/journal.pbio.1001536.
  • 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. Journal of biological chemistry. 2009;284(8):5381–94. doi:10.1074/jbc.M808958200.
  • Adamson RH, Zeng M, Adamson GN, Lenz JF, Curry FE. PAF- and bradykinin-induced hyperpermeability of rat venules is independent of actin-myosin contraction. Am J Physiol Heart Circ Physiol. 2003;285(1):H406–17. doi:10.1152/ajpheart.00021.2003.
  • Jeewandara C, Gomes L, Wickramasinghe N, Gutowska-Owsiak D, Waithe D, Paranavitane SA, Shyamali NL, Ogg GS, Malavige GN. Platelet activating factor contributes to vascular leak in acute dengue infection. PLoS Negl Trop Dis. 2015;9(2):e0003459. doi:10.1371/journal.pntd.0003459.
  • Travis SP, Jewell DP. Regional differences in the response to platelet-activating factor in rabbit colon. Clin Sci (Lond). 1992;82(6):673–80. doi:10.1042/cs0820673.
  • Abu-Farsakh S, Wu T, Lalonde A, Sun J, Zhou Z. High expression of Claudin-2 in esophageal carcinoma and precancerous lesions is significantly associated with the bile salt receptors VDR and TGR5. BMC Gastroenterol. 2017;17(1):33. doi:10.1186/s12876-017-0590-0.
  • Aung PP, Mitani Y, Sanada Y, Nakayama H, Matsusaki K, Yasui W. Differential expression of claudin-2 in normal human tissues and gastrointestinal carcinomas. Virchows Arch. 2006;448(4):428–34. Epub 2005/12/06. doi:10.1007/s00428-005-0120-2.
  • Gyorffy H. [Study of claudins and prognostic factors in some gastrointestinal diseases]. Magyar onkologia. 2009;53(4):377–83. Epub 2010/01/15.
  • Gyorffy H, Holczbauer A, Nagy P, Szabo Z, Kupcsulik P, Paska C, Papp J, Schaff Z, Kiss A. Claudin expression in Barrett's esophagus and adenocarcinoma. Virchows Arch. 2005;447(6):961–8. Epub 2005/09/01. doi:10.1007/s00428-005-0045-9.
  • Weber CR, Nalle SC, Tretiakova M, Rubin DT, Turner JR. Claudin-1 and claudin-2 expression is elevated in inflammatory bowel disease and may contribute to early neoplastic transformation. Lab Invest. 2008;88(10):1110–20. Epub 2008/08/20. doi:10.1038/labinvest.2008.78.
  • Ulbricht TLV. Purines, Pyrimidines and Nucleotides and the Chemistry of Nucleic Acids. NEW YORK: THE MACMILLAN COMPANY;1964.
  • Li WH, Qiu Y, Zhang HQ, Liu Y, You JF, Tian XX, Fang WG. P2Y2 receptor promotes cell invasion and metastasis in prostate cancer cells. Br J Cancer. 2013;109(6):1666–75. doi:10.1038/bjc.2013.484.
  • Loma P, Guzman-Aranguez A, Perez de Lara MJ, Pintor J. Diadenosine tetraphosphate induces tight junction disassembly thus increasing corneal epithelial permeability. British journal of pharmacology. 2015;172(4):1045–58. doi:10.1111/bph.12972.
  • Carman AJ, Mills JH, Krenz A, Kim DG, Bynoe MS. Adenosine receptor signaling modulates permeability of the blood-brain barrier. J Neurosci. 2011;31(37):13272–80. doi:10.1523/JNEUROSCI.3337-11.2011.
  • Kim DG, Bynoe MS. A2A Adenosine Receptor Regulates the Human Blood-Brain Barrier Permeability. Mol Neurobiol. 2015;52(1):664–78. doi:10.1007/s12035-014-8879-2.
  • Gao X, Qian J, Zheng S, Changyi Y, Zhang J, Ju S, Zhu J, Li C. Overcoming the blood-brain barrier for delivering drugs into the brain by using adenosine receptor nanoagonist. ACS nano. 2014;8(4):3678–89. doi:10.1021/nn5003375.
  • Yang Y, Qiu Y, Wang W, Xiao W, Liang H, Zhang C, Yang H, Teitelbaum DH, Sun LH, Yang H. Adenosine A2B receptor modulates intestinal barrier function under hypoxic and ischemia/reperfusion conditions. Int J Clin Exp Pathol. 2014;7(5):2006–18.
  • Schenck LP, Hirota SA, Hirota CL, Boasquevisque P, Tulk SE, Li Y, Wadhwani A, Doktorchik CT, Macnaughton WK, Beck PL, et al. Attenuation of Clostridium difficile toxin-induced damage to epithelial barrier by ecto-5'-nucleotidase (CD73) and adenosine receptor signaling. Neurogastroenterol Motil. 2013;25(6):e441–53. doi:10.1111/nmo.12139.
  • Groschwitz KR, Wu D, Osterfeld H, Ahrens R, Hogan SP. Chymase-mediated intestinal epithelial permeability is regulated by a protease-activating receptor/matrix metalloproteinase-2-dependent mechanism. Am J Physiol Gastrointest Liver Physiol. 2013;304(5):G479–89. doi:10.1152/ajpgi.00186.2012.
  • Cenac N, Coelho AM, Nguyen C, Compton S, Andrade-Gordon P, MacNaughton WK, Wallace JL, Hollenberg MD, Bunnett NW, Garcia-Villar R, et al. Induction of intestinal inflammation in mouse by activation of proteinase-activated receptor-2. American journal of pathology. 2002;161(5):1903–15. doi:10.1016/S0002-9440(10)64466-5.
  • Jacob C, Yang PC, Darmoul D, Amadesi S, Saito T, Cottrell GS, Coelho AM, Singh P, Grady EF, Perdue M, et al. Mast cell tryptase controls paracellular permeability of the intestine. J Biol Chem. 2005;280(36):31936–48. doi:10.1074/jbc.M506338200.
  • Bustos D, Negri G, De Paula JA Di Carlo M, Yapur V, Facente A, De Paula A. Colonic proteinases: Increased activity in patients with ulcerative colitis. Medicina (B Aires). 1998;58(3):262–4.
  • Raithel M, Winterkamp S, Pacurar A, Ulrich P, Hochberger J, Hahn EG. Release of mast cell tryptase from human colorectal mucosa in inflammatory bowel disease. Scand J Gastroenterol. 2001;36(2):174–9. doi:10.1080/003655201750065933.
  • Gecse K, Roka R, Ferrier L, Leveque M, Eutamene H, Cartier C, Ait-Belgnaoui A, Rosztóczy A, Izbéki F, Fioramonti J, et al. Increased faecal serine protease activity in diarrhoeic IBS patients: a colonic lumenal factor impairing colonic permeability and sensitivity. Gut. 2008;57(5):591–9. doi:10.1136/gut.2007.140210.
  • Cenac N, Chin AC, Garcia-Villar R, Salvador-Cartier C, Ferrier L, Vergnolle N, Buret AG, Fioramonti J, Bueno L. PAR2 activation alters colonic paracellular permeability in mice via IFN-gamma-dependent and -independent pathways. J Physiol. 2004;558(Pt 3):913–25. doi:10.1113/jphysiol.2004.061721.
  • Goldblum SE, Rai U, Tripathi A, Thakar M, De Leo L Di Toro N, Not T, Ramachandran R, Puche AC, Hollenberg MD, et al. The active Zot domain (aa 288-293) increases ZO-1 and myosin 1C serine/threonine phosphorylation, alters interaction between ZO-1 and its binding partners, and induces tight junction disassembly through proteinase activated receptor 2 activation. FASEB J. 2011;25(1):144–58. doi:10.1096/fj.10-158972.
  • Cenac N, Garcia-Villar R, Ferrier L, Larauche M, Vergnolle N, Bunnett NW, Coelho AM, Fioramonti J, Bueno L. Proteinase-activated receptor-2-induced colonic inflammation in mice: Possible involvement of afferent neurons, nitric oxide, and paracellular permeability. J Immunol. 2003;170(8):4296–300. doi:10.4049/jimmunol.170.8.4296.
  • Zhong CJ, Wang K, Zhang L, Yang CQ, Zhang K, Zhou SP, Duan LP. Mast cell activation is involved in stress-induced epithelial barrier dysfunction in the esophagus. J Dig Dis. 2015;16(4):186–96. doi:10.1111/1751-2980.12226.
  • Enjoji S, Ohama T, Sato K. Regulation of epithelial cell tight junctions by protease-activated receptor 2. J Vet Med Sci. 2014;76(9):1225–9. doi:10.1292/jvms.14-0191.
  • Szabo R, Peters DE, Kosa P, Camerer E, Bugge TH. Regulation of feto-maternal barrier by matriptase- and PAR-2-mediated signaling is required for placental morphogenesis and mouse embryonic survival. PLoS Genet. 2014;10(7):e1004470. doi:10.1371/journal.pgen.1004470.
  • Cirino G, Severino B. Thrombin receptors and their antagonists: an update on the patent literature. Expert Opin Ther Pat. 2010;20(7):875–84. doi:10.1517/13543776.2010.487864.
  • McLaughlin JN, Shen L, Holinstat M, Brooks JD, Dibenedetto E, Hamm HE. Functional selectivity of G protein signaling by agonist peptides and thrombin for the protease-activated receptor-1. Journal of biological chemistry. 2005;280(26):25048–59. doi:10.1074/jbc.M414090200.
  • Xue M, Hollenberg MD, Demchuk A, Yong VW. Relative importance of proteinase-activated receptor-1 versus matrix metalloproteinases in intracerebral hemorrhage-mediated neurotoxicity in mice. Stroke. 2009;40(6):2199–204. doi:10.1161/STROKEAHA.108.540393.
  • Cheng Y, Xi G, Jin H, Keep RF, Feng J, Hua Y. Thrombin-induced cerebral hemorrhage: role of protease-activated receptor-1. Transl Stroke Res. 2014;5(4):472–5. doi:10.1007/s12975-013-0288-8.
  • Gao D, Ding F, Lei G, Luan G, Zhang S, Li K, Wang D, Zhang L, Dai D. Effects of focal mild hypothermia on thrombin-induced brain edema formation and the expression of protease activated receptor-1, matrix metalloproteinase-9 and aquaporin 4 in rats. Molecular medicine reports. 2015;11(4):3009–14. doi:10.3892/mmr.2014.3111.
  • Kim HN, Kim YR, Ahn SM, Lee SK, Shin HK, Choi BT. Protease activated receptor-1 antagonist ameliorates the clinical symptoms of experimental autoimmune encephalomyelitis via inhibiting breakdown of blood-brain barrier. Journal of neurochemistry. 2015;135(3):577–88. doi:10.1111/jnc.13285.
  • Riewald M, Petrovan RJ, Donner A, Mueller BM, Ruf W. Activation of endothelial cell protease activated receptor 1 by the protein C pathway. Science. 2002;296(5574):1880–2. doi:10.1126/science.1071699.
  • Soh UJ, Trejo J. Activated protein C promotes protease-activated receptor-1 cytoprotective signaling through beta-arrestin and dishevelled-2 scaffolds. Proc Natl Acad Sci U S A. 2011;108(50):E1372–80. doi:10.1073/pnas.1112482108.
  • Mosnier LO, Sinha RK, Burnier L, Bouwens EA, Griffin JH. Biased agonism of protease-activated receptor 1 by activated protein C caused by noncanonical cleavage at Arg46. Blood. 2012;120(26):5237–46. doi:10.1182/blood-2012-08-452169.
  • Stavenuiter F, Mosnier LO. Noncanonical PAR3 activation by factor Xa identifies a novel pathway for Tie2 activation and stabilization of vascular integrity. Blood. 2014;124(23):3480–9. doi:10.1182/blood-2014-06-582775.
  • Minhas N, Xue M, Fukudome K, Jackson CJ. Activated protein C utilizes the angiopoietin/Tie2 axis to promote endothelial barrier function. FASEB J. 2010;24(3):873–81. doi:10.1096/fj.09-134445.
  • Bernard GR, Vincent JL, Laterre PF, LaRosa SP, Dhainaut JF, Lopez-Rodriguez A, Steingrub JS, Garber GE, Helterbrand JD, Ely EW, et al. Efficacy and safety of recombinant human activated protein C for severe sepsis. New England journal of medicine. 2001;344(10):699–709. doi:10.1056/NEJM200103083441001.
  • Xue M, Chow SO, Dervish S, Chan YK, Julovi SM, Jackson CJ. Activated protein C enhances human keratinocyte barrier integrity via sequential activation of epidermal growth factor receptor and Tie2. Journal of biological chemistry. 2011;286(8):6742–50. doi:10.1074/jbc.M110.181388.
  • Fukasawa H, Bornheimer S, Kudlicka K, Farquhar MG. Slit diaphragms contain tight junction proteins. J Am Soc Nephrol. 2009;20(7):1491–503. doi:10.1681/ASN.2008101117.
  • Macconi D, Abbate M, Morigi M, Angioletti S, Mister M, Buelli S, Bonomelli M, Mundel P, Endlich K, Remuzzi G, et al. Permselective dysfunction of podocyte-podocyte contact upon angiotensin II unravels the molecular target for renoprotective intervention. American journal of pathology. 2006;168(4):1073–85. doi:10.2353/ajpath.2006.050701.
  • Macconi D, Ghilardi M, Bonassi ME, Mohamed EI, Abbate M, Colombi F, Remuzzi G, Remuzzi A. Effect of angiotensin-converting enzyme inhibition on glomerular basement membrane permeability and distribution of zonula occludens-1 in MWF rats. J Am Soc Nephrol. 2000;11(3):477–89.
  • Rincon-Choles H, Vasylyeva TL, Pergola PE, Bhandari B, Bhandari K, Zhang JH, Wang W, Gorin Y, Barnes JL, Abboud HE. ZO-1 expression and phosphorylation in diabetic nephropathy. Diabetes. 2006;55(4):894–900. doi:10.2337/diabetes.55.04.06.db05-0355.
  • Zhang Z, Zhang Y, Ning G, Deb DK, Kong J, Li YC. Combination therapy with AT1 blocker and vitamin D analog markedly ameliorates diabetic nephropathy: Blockade of compensatory renin increase. Proc Natl Acad Sci U S A. 2008;105(41):15896–901. doi:10.1073/pnas.0803751105.
  • Kim JH, Kim JH, Yu YS, Cho CS, Kim KW. Blockade of angiotensin II attenuates VEGF-mediated blood-retinal barrier breakdown in diabetic retinopathy. J Cereb Blood Flow Metab. 2009;29(3):621–8. doi:10.1038/jcbfm.2008.154.
  • Fleegal-DeMotta MA, Doghu S, Banks WA. Angiotensin II modulates BBB permeability via activation of the AT(1) receptor in brain endothelial cells. J Cereb Blood Flow Metab. 2009;29(3):640–7. doi:10.1038/jcbfm.2008.158.
  • Wosik K, Cayrol R, Dodelet-Devillers A, Berthelet F, Bernard M, Moumdjian R, Bouthillier A, Reudelhuber TL, Prat A. Angiotensin II controls occludin function and is required for blood brain barrier maintenance: relevance to multiple sclerosis. J Neurosci. 2007;27(34):9032–42. doi:10.1523/JNEUROSCI.2088-07.2007.
  • Jin L, Chen J, Li L, Li C, Chen C, Li S. CRH suppressed TGFbeta1-induced Epithelial-Mesenchymal Transition via induction of E-cadherin in breast cancer cells. Cellular signalling. 2014;26(4):757–65. doi:10.1016/j.cellsig.2013.12.017.
  • Buckley MM, O'Halloran KD, Rae MG, Dinan TG, O'Malley D. Modulation of enteric neurons by interleukin-6 and corticotropin-releasing factor contributes to visceral hypersensitivity and altered colonic motility in a rat model of irritable bowel syndrome. Journal of physiology. 2014;592(23):5235–50. doi:10.1113/jphysiol.2014.279968.
  • Zhu H, Liu Y, Chen S, Wang X, Pi D, Leng W, Chen F, Zhang J, Kang P. Fish oil enhances intestinal barrier function and inhibits corticotropin-releasing hormone/corticotropin-releasing hormone receptor 1 signalling pathway in weaned pigs after lipopolysaccharide challenge. British journal of nutrition. 2016;115(11):1947–57. doi:10.1017/S0007114516001100.
  • Ulitzky L, Lafer MM, KuKuruga MA, Silberstein E, Cehan N, Taylor DR. A New Signaling Pathway for HCV Inhibition by Estrogen: GPR30 Activation Leads to Cleavage of Occludin by MMP-9. PloS one. 2016;11(1):e0145212. doi:10.1371/journal.pone.0145212.
  • Tian PC, Wang HL, Chen GH, Luo Q, Chen Z, Wang Y, Liu YF. 2,2',4,4'-Tetrabromodiphenyl ether promotes human neuroblastoma SH-SY5Y cells migration via the GPER/PI3K/Akt signal pathway. Hum Exp Toxicol. 2016;35(2):124–34. doi:10.1177/0960327115578974.
  • Lu D, Qu Y, Shi F, Feng D, Tao K, Gao G, He S, Zhao T. Activation of G protein-coupled estrogen receptor 1 (GPER-1) ameliorates blood-brain barrier permeability after global cerebral ischemia in ovariectomized rats. Biochem Biophys Res Commun. 2016;477(2):209–14. doi:10.1016/j.bbrc.2016.06.044.
  • Martin-Venegas R, Roig-Perez S, Ferrer R, Moreno JJ. Arachidonic acid cascade and epithelial barrier function during Caco-2 cell differentiation. Journal of lipid research. 2006;47(7):1416–23. doi:10.1194/jlr.M500564-JLR200.
  • Rodriguez-Lagunas MJ, Martin-Venegas R, Moreno JJ, Ferrer R. PGE2 promotes Ca2+-mediated epithelial barrier disruption through EP1 and EP4 receptors in Caco-2 cell monolayers. American journal of physiology Cell physiology. 2010;299(2):C324–34. doi:10.1152/ajpcell.00397.2009.
  • Tanaka MN, Diaz BL, de Souza W, Morgado-Diaz JA. Prostaglandin E2-EP1 and EP2 receptor signaling promotes apical junctional complex disassembly of Caco-2 human colorectal cancer cells. BMC cell biology. 2008;9:63. doi:10.1186/1471-2121-9-63.
  • Lejeune M, Moreau F, Chadee K. Loss of EP2 receptor subtype in colonic cells compromise epithelial barrier integrity by altering claudin-4. PloS one. 2014;9(11):e113270. doi:10.1371/journal.pone.0113270.
  • Frankowski JC, DeMars KM, Ahmad AS, Hawkins KE, Yang C, Leclerc JL, Doré S, Candelario-Jalil E. Detrimental role of the EP1 prostanoid receptor in blood-brain barrier damage following experimental ischemic stroke. Scientific reports. 2015;5:17956. doi:10.1038/srep17956.
  • Elliott PJ, Hayward NJ, Huff MR, Nagle TL, Black KL, Bartus RT. Unlocking the blood-brain barrier: A role for RMP-7 in brain tumor therapy. Experimental neurology. 1996;141(2):214–24. doi:10.1006/exnr.1996.0156.
  • Inamura T, Nomura T, Bartus RT, Black KL. Intracarotid infusion of RMP-7, a bradykinin analog: A method for selective drug delivery to brain tumors. Journal of neurosurgery. 1994;81(5):752–8. doi:10.3171/jns.1994.81.5.0752.
  • Barnett FH, Rainov NG, Ikeda K, Schuback DE, Elliott P, Kramm CM, Chase M, Qureshi NH, Harsh G 4th, Chiocca EA, et al. Selective delivery of herpes virus vectors to experimental brain tumors using RMP-7. Cancer gene therapy. 1999;6(1):14–20. doi:10.1038/sj.cgt.7700003.
  • Liu LB, Xue YX, Liu YH, Wang YB. Bradykinin increases blood-tumor barrier permeability by down-regulating the expression levels of ZO-1, occludin, and claudin-5 and rearranging actin cytoskeleton. Journal of neuroscience research. 2008;86(5):1153–68. doi:10.1002/jnr.21558.
  • Ma T, Xue Y. RhoA-mediated potential regulation of blood-tumor barrier permeability by bradykinin. J Mol Neurosci. 2010;42(1):67–73. doi:10.1007/s12031-010-9345-x.
  • Ma T, Liu L, Wang P, Xue Y. Evidence for involvement of ROCK signaling in bradykinin-induced increase in murine blood-tumor barrier permeability. Journal of neuro-oncology. 2012;106(2):291–301. doi:10.1007/s11060-011-0685-3.
  • Liu LB, Liu XB, Ma J, Liu YH, Li ZQ, Ma T, Zhao XH, Xi Z, Xue YX. Bradykinin increased the permeability of BTB via NOS/NO/ZONAB-mediating down-regulation of claudin-5 and occludin. Biochem Biophys Res Commun. 2015;464(1):118–25. doi:10.1016/j.bbrc.2015.06.082.
  • Marcon R, Claudino RF, Dutra RC, Bento AF, Schmidt EC, Bouzon ZL, Sordi R, Morais RL, Pesquero JB, Calixto JB. Exacerbation of DSS-induced colitis in mice lacking kinin B(1) receptors through compensatory up-regulation of kinin B(2) receptors: The role of tight junctions and intestinal homeostasis. British journal of pharmacology. 2013;168(2):389–402. doi:10.1111/j.1476-5381.2012.02136.x.
  • Dey M, Baldys A, Sumter DB, Gooz P, Luttrell LM, Raymond JR, Göoz M. Bradykinin decreases podocyte permeability through ADAM17-dependent epidermal growth factor receptor activation and zonula occludens-1 rearrangement. Journal of pharmacology and experimental therapeutics. 2010;334(3):775–83. doi:10.1124/jpet.110.168054.
  • Yu M, He P, Liu Y, He Y, Du Y, Wu M, Zhang G, Yang C, Gao F. Hyaluroan-regulated lymphatic permeability through S1P receptors is crucial for cancer metastasis. Medical Oncol. 2015;32(1):381. doi:10.1007/s12032-014-0381-1.

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