Inhibition of Glycogen Synthase Kinase 3β Promotes Tight Junction Stability in Brain Endothelial Cells by Half-Life Extension of Occludin and Claudin-5

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Ramirez, Servio H ^a   Fan, Shongshan ^a   Dykstra, Holly ^a   Rom, Slava ^a   Mercer, Aaron ^b   Reichenbach, Nancy L ^a   Gofman, Larisa ^a   Persidsky, Yuri ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; BETA CATENIN; CLAUDIN 5; DOXYCYCLINE; ENZYME INHIBITOR; GLYCOGEN SYNTHASE KINASE 3BETA; GLYCOGEN SYNTHASE KINASE 3BETA INHIBITOR; KENPAULLONE; LITHIUM CHLORIDE; MUTANT PROTEIN; OCCLUDIN; ON TARGET PLUS; PROTEIN SERINE THREONINE KINASE INHIBITOR; PROTEIN ZO1; SMALL INTERFERING RNA; TIGHT JUNCTION PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BLOOD BRAIN BARRIER; BRAIN; BRAIN BLOOD VESSEL; CELL ASSAY; CELL MEMBRANE; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; ENZYME INACTIVATION; ENZYME INHIBITION; HALF LIFE TIME; HUMAN; HUMAN CELL; NERVOUS SYSTEM INFLAMMATION; PROTEIN METABOLISM; PROTEIN STABILITY; TRANSCRIPTION REGULATION;

BENZAZEPINES; BLOOD-BRAIN BARRIER; BRAIN; CELLS, CULTURED; CLAUDIN-5; ELECTRIC IMPEDANCE; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; INDOLES; LITHIUM CHLORIDE; OCCLUDIN; TIGHT JUNCTIONS; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84873896549     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055972     Document Type: Article

References (41)

1. Persidsky Y, Ramirez SH, Haorah J, Kanmogne GD, (2006) Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol 1: 223-236.
2. Coisne C, Engelhardt B, (2011) Tight junctions in brain barriers during central nervous system inflammation. Antioxid Redox Signal 15: 1285-1303.
3. Zlokovic BV, (2011) Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat Rev Neurosci 12: 723-738.
4. Abbott NJ, (2005) Dynamics of CNS barriers: evolution, differentiation, and modulation. Cell Mol Neurobiol 25: 5-23.
5. Neuwelt E, Abbott NJ, Abrey L, Banks WA, Blakley B, et al. (2008) Strategies to advance translational research into brain barriers. Lancet Neurol 7: 84-96.
6. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ, (2010) Structure and function of the blood-brain barrier. Neurobiol Dis 37: 13-25.
7. Klamer G, Song E, Ko KH, O'Brien TA, Dolnikov A, (2010) Using small molecule GSK3beta inhibitors to treat inflammation. Curr Med Chem 17: 2873-2881.
8. Fan S, Ramirez SH, Garcia TM, Dewhurst S, (2004) Dishevelled promotes neurite outgrowth in neuronal differentiating neuroblastoma 2A cells, via a DIX-domain dependent pathway. Brain Res Mol Brain Res 132: 38-50.
9. Wu D, Pan W, (2010) GSK3: a multifaceted kinase in Wnt signaling. Trends Biochem Sci 35: 161-168.
10. Jope RS, Roh MS, (2006) Glycogen synthase kinase-3 (GSK3) in psychiatric diseases and therapeutic interventions. Curr Drug Targets 7: 1421-1434.
11. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA, (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature. 378: 785-789.
12. Ramirez SH, Fan S, Zhang M, Papugani A, Reichenbach N, et al. (2010) Inhibition of glycogen synthase kinase 3beta (GSK3beta) decreases inflammatory responses in brain endothelial cells. Am J Pathol 176: 881-892.
13. Liu F, Schaphorst KL, Verin AD, Jacobs K, Birukova A, et al. (2002) Hepatocyte growth factor enhances endothelial cell barrier function and cortical cytoskeletal rearrangement: potential role of glycogen synthase kinase-3beta. FASEB J 16: 950-962.
14. Liebner S, Corada M, Bangsow T, Babbage J, Taddei A, et al. (2008) Wnt/beta-catenin signaling controls development of the blood-brain barrier. J Cell Biol 183: 409-417.
15. Graesser D, Solowiej A, Bruckner M, Osterweil E, Juedes A, et al. (2002) Altered vascular permeability and early onset of experimental autoimmune encephalomyelitis in PECAM-1-deficient mice. J Clin Invest 109: 383-392.
16. Angers S, Moon RT, (2009) Proximal events in Wnt signal transduction. Nat Rev Mol Cell Biol 10: 468-477.
17. Watanabe K, Dai X, (2011) A WNTer revisit: new faces of beta-catenin and TCFs in pluripotency. Sci Signal 4: pe41.
18. Miwa N, Furuse M, Tsukita S, Niikawa N, Nakamura Y, et al. (2001) Involvement of claudin-1 in the beta-catenin/Tcf signaling pathway and its frequent upregulation in human colorectal cancers. Oncol Res 12: 469-476.
19. Mankertz J, Hillenbrand B, Tavalali S, Huber O, Fromm M, et al. (2004) Functional crosstalk between Wnt signaling and Cdx-related transcriptional activation in the regulation of the claudin-2 promoter activity. Biochem Biophys Res Commun 314: 1001-1007.
20. Medici D, Hay ED, Goodenough DA, (2006) Cooperation between snail and LEF-1 transcription factors is essential for TGF-beta1-induced epithelial-mesenchymal transition. Mol Biol Cell 17: 1871-1879.
21. Wang Z, Wade P, Mandell KJ, Akyildiz A, Parkos CA, et al. (2007) Raf 1 represses expression of the tight junction protein occludin via activation of the zinc-finger transcription factor slug. Oncogene 26: 1222-1230.
22. Bernas MJ, Cardoso FL, Daley SK, Weinand ME, Campos AR, et al. (2010) Establishment of primary cultures of human brain microvascular endothelial cells to provide an in vitro cellular model of the blood-brain barrier. Nat Protoc 5: 1265-1272.
23. Wakatsuki S, Saitoh F, Araki T, (2011) ZNRF1 promotes Wallerian degeneration by degrading AKT to induce GSK3B-dependent CRMP2 phosphorylation. Nat Cell Biol 13: 1415-1423.
24. Yen HC, Xu Q, Chou DM, Zhao Z, Elledge SJ, (2008) Global protein stability profiling in mammalian cells. Science 322: 918-923.
25. Sutherland C, (2011) What Are the bona fide GSK3 Substrates? Int J Alzheimers Dis 2011: 505607.
26. DePaola N, Phelps JE, Florez L, Keese CR, Minnear FL, et al. (2001) Electrical impedance of cultured endothelium under fluid flow. Ann Biomed Eng 29: 648-656.
27. Lo CM, Keese CR, Giaever I, (1995) Impedance analysis of MDCK cells measured by electric cell-substrate impedance sensing. Biophys J 69: 2800-2807.
28. Zhang L, Jouret F, Rinehart J, Sfakianos J, Mellman I, et al. (2011) AMP-activated protein kinase (AMPK) activation and glycogen synthase kinase-3beta (GSK-3beta) inhibition induce Ca2+-independent deposition of tight junction components at the plasma membrane. J Biol Chem 286: 16879-16890.
29. Severson EA, Kwon M, Hilgarth RS, Parkos CA, Nusrat A, (2010) Glycogen Synthase Kinase 3 (GSK-3) influences epithelial barrier function by regulating occludin, claudin-1 and E-cadherin expression. Biochem Biophys Res Commun 397: 592-597.
30. Herve JC, Derangeon M, Bahbouhi B, Mesnil M, Sarrouilhe D, (2007) The connexin turnover, an important modulating factor of the level of cell-to-cell junctional communication: comparison with other integral membrane proteins. J Membr Biol 217: 21-33.
31. Raikwar NS, Vandewalle A, Thomas CP, (2010) Nedd4-2 interacts with occludin to inhibit tight junction formation and enhance paracellular conductance in collecting duct epithelia. Am J Physiol Renal Physiol 299: F436-444.
32. Mandel I, Paperna T, Volkowich A, Merhav M, Glass-Marmor L, et al. (2012) The ubiquitin-proteasome pathway regulates claudin 5 degradation. J Cell Biochem.
33. Murakami T, Felinski EA, Antonetti DA, (2009) Occludin phosphorylation and ubiquitination regulate tight junction trafficking and vascular endothelial growth factor-induced permeability. J Biol Chem 284: 21036-21046.
34. Failor KL, Desyatnikov Y, Finger LA, Firestone GL, (2007) Glucocorticoid-induced degradation of glycogen synthase kinase-3 protein is triggered by serum- and glucocorticoid-induced protein kinase and Akt signaling and controls beta-catenin dynamics and tight junction formation in mammary epithelial tumor cells. Mol Endocrinol 21: 2403-2415.
35. Rajasekaran AK, Hojo M, Huima T, Rodriguez-Boulan E, (1996) Catenins and zonula occludens-1 form a complex during early stages in the assembly of tight junctions. J Cell Biol 132: 451-463.
36. DeBellefeuille S, Hermo L, Gregory M, Dufresne J, Cyr DG, (2003) Catenins in the rat epididymis: their expression and regulation in adulthood and during postnatal development. Endocrinology 144: 5040-5049.
37. Traweger A, Fang D, Liu YC, Stelzhammer W, Krizbai IA, et al. (2002) The tight junction-specific protein occludin is a functional target of the E3 ubiquitin-protein ligase itch. J Biol Chem 277: 10201-10208.
38. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL, (2001) Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci U S A 98: 14440-14445.
39. Dehoux M, Gobier C, Lause P, Bertrand L, Ketelslegers JM, et al. (2007) IGF-I does not prevent myotube atrophy caused by proinflammatory cytokines despite activation of Akt/Foxo and GSK-3beta pathways and inhibition of atrogin-1 mRNA. Am J Physiol Endocrinol Metab 292: E145-150.
40. Escribano C, Delgado-Martin C, Rodriguez-Fernandez JL, (2009) CCR7-dependent stimulation of survival in dendritic cells involves inhibition of GSK3beta. J Immunol 183: 6282-6295.
41. Takahashi S, Iwamoto N, Sasaki H, Ohashi M, Oda Y, et al. (2009) The E3 ubiquitin ligase LNX1p80 promotes the removal of claudins from tight junctions in MDCK cells. J Cell Sci 122: 985-994.