Evidence for involvement of ROCK signaling in bradykinin-induced increase in murine blood-tumor barrier permeability

Journal of Neuro-Oncology

Volumn 106, Issue 2, 2012, Pages 291-301

  Ma, Teng ^a   Liu, Libo ^a   Wang, Ping ^a   Xue, Yixue ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Actin rearrangement; Blood tumor barrier; Bradykinin; Cofilin; Myosin light chain; ROCK; Tight junction

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; BRADYKININ; CLAUDIN 5; COFILIN; MYOSIN LIGHT CHAIN; OCCLUDIN; PROTEIN SERINE THREONINE KINASE; RHO KINASE; RHO KINASE 1; RHO KINASE 2; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BLOOD TUMOR BARRIER; CONTROLLED STUDY; CYTOPLASM; ELECTRIC RESISTANCE; ENZYME ACTIVITY; ENZYME INHIBITION; IN VITRO STUDY; NONHUMAN; PERMEABILITY BARRIER; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; PROTEIN TRANSPORT; RAT; SIGNAL TRANSDUCTION; STRESS FIBER; TIGHT JUNCTION;

EID: 82955247595     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-011-0685-3     Document Type: Article

References (61)

1. KL Black NS Ningaraj 2004 Modulation of brain tumor capillaries for enhanced drug delivery selectively to brain tumor Cancer Control 11 165 173 15153840 (Pubitemid 38758221)
2. K Samoto GC Perng M Ehtesham Y Liu SL Wechsler AB Nesburn KL Black JS Yu 2001 A herpes simplex virus type 1 mutant deleted for gamma 34.5 and LAT kills glioma cells in vitro and is inhibited for in vivo reactivation Cancer Gene Therapy 8 269 277 11393279 10.1038/sj.cgt.7700306 1:CAS:528:DC%2BD3MXjsl2nsL4%3D (Pubitemid 32480063)
3. JK Fenstermacher AS Cowles 1977 Theoretic limitations of intracarotid infusions in brain tumor chemotherapy Cancer Treat Rep 61 519 526 884689 1:CAS:528:DyaE2sXkvFGnsL4%3D
4. LL Muldoon C Soussain K Jahnke C Johanson T Siegal QR Smith WA Hall K Hynynen PD Senter DM Peereboom EA Neuwelt 2007 Chemotherapy delivery issues in central nervous system malignancy: a reality check J Clin Oncol 25 2295 2305 17538176 10.1200/JCO.2006.09.9861 1:CAS:528:DC%2BD2sXnsVShu7o%3D (Pubitemid 46954658)
5. PR Lockman RK Mittapalli KS Taskar V Rudraraju B Gril KA Bohn CE Adkins A Roberts HR Thorsheim JA Gaasch S Huang D Palmieri PS Steeg QR Smith 2010 Heterogeneous blood-tumor barrier permeability determines drug efficacy in experimental brain metastases of breast cancer Clin Cancer Res 16 5664 5678 20829328 10.1158/1078-0432.CCR-10-1564 1:CAS:528:DC%2BC3cXhsFamtL3F
6. LB Liu YX Xue YH Liu YB Wang 2008 Bradykinin increases blood-tumor barrier permeability by down-regulating the expression levels of ZO-1, occludin, and claudin-5 and rearranging actin cytoskeleton J Neurosci Res 86 1153 1168 18183615 10.1002/jnr.21558 1:CAS:528:DC%2BD1cXksVGqtrc%3D (Pubitemid 351441313)
7. T Ma Y Xue 2010 RhoA-mediated potential regulation of blood-tumor barrier permeability by bradykinin J Mol Neurosci 42 67 73 20369389 10.1007/s12031-010-9345-x
8. J Yin FS Yu 2008 Rho kinases regulate corneal epithelial wound healing Am J Physiol Cell Physiol 295 C378 C387 18495812 10.1152/ajpcell.90624.2007 1:CAS:528:DC%2BD1cXhtVaktr7F (Pubitemid 352755785)
9. SV Walsh AM Hopkins J Chen S Narumiya CA Parkos A Nusrat 2001 Rho kinase regulates tight junction function and is necessary for tight junction assembly in polarized intestinal epithelia Gastroenterology 121 566 579 11522741 10.1053/gast.2001.27060 1:CAS:528:DC%2BD3MXntVKnsb8%3D (Pubitemid 32822572)
10. B Li WD Zhao ZM Tan WG Fang L Zhu YH Chen 2006 Involvement of Rho/ROCK signalling in small cell lung cancer migration through human brain microvascular endothelial cells FEBS Lett 580 4252 4260 16828752 10.1016/j.febslet.2006.06. 056 1:CAS:528:DC%2BD28XntV2qs7k%3D (Pubitemid 44037578)
11. SD Calaminus JM Auger OJ McCarty MJ Wakelam LM Machesky SP Watson 2007 MyosinIIa contractility is required for maintenance of platelet structure during spreading on collagen and contributes to thrombus stability J Thromb Haemost 5 2136 2145 17645784 10.1111/j.1538-7836.2007.02696.x 1:CAS:528:DC%2BD2sXht1WmsrbE (Pubitemid 47450034)
12. B Wojciak-Stothard AJ Ridley 2002 Rho GTPases and the regulation of endothelial permeability Vascul Pharmacol 39 187 199 12747959 10.1016/S1537-1891(03)00008-9 1:CAS:528:DC%2BD3sXjs1eksbc%3D (Pubitemid 37492962)
13. M Essler JM Staddon PC Weber M Aepfelbacher 2000 Cyclic AMP blocks bacterial lipopolysaccharide-induced myosin light chain phosphorylation in endothelial cells through inhibition of Rho/Rho kinase signaling J Immunol 164 6543 6549 10843713 1:CAS:528:DC%2BD3cXktFWltbc%3D (Pubitemid 30408840)
14. GP van Nieuw Amerongen S van Delft MA Vermeer JG Collard VW van Hinsbergh 2000 Activation of RhoA by thrombin in endothelial hyperpermeability: role of Rho kinase and protein tyrosine kinases Circ Res 87 335 340 10948069 (Pubitemid 30655976)
15. M Aepfelbacher M Essler 2001 Disturbance of endothelial barrier function by bacterial toxins and atherogenic mediators: a role for Rho/Rho kinase Cell Microbiol 3 649 658 11580750 10.1046/j.1462-5822.2001.00145.x 1:CAS:528:DC%2BD3MXnslGntbk%3D (Pubitemid 32976336)
16. T Hirase S Kawashima EY Wong T Ueyama Y Rikitake S Tsukita M Yokoyama JM Staddon 2001 Regulation of tight junction permeability and occludin phosphorylation by Rhoa-p160ROCK-dependent and -independent mechanisms J Biol Chem 276 10423 10431 11139571 10.1074/jbc.M007136200 1:CAS:528: DC%2BD3MXis1Oktb0%3D
17. B Wojciak-Stothard S Potempa T Eichholtz AJ Ridley 2001 Rho and Rac but not Cdc42 regulate endothelial cell permeability J Cell Sci 114 1343 1355 11257000 1:CAS:528:DC%2BD3MXjt1OmtLs%3D (Pubitemid 32409470)
18. RD Hurst IB Fritz 1996 Properties of an immortalised vascular endothelial/glioma cell co-culture model of the blood-brain barrier J Cell Physiol 167 81 88 8698844 10.1002/(SICI)1097-4652(199604)167:1<81::AID- JCP9>3.0.CO;2-8 1:CAS:528:DyaK28XhvVSntLY%3D (Pubitemid 26108736)
19. AS Easton NJ Abbott 2002 Brandykinin increases permeability by calcium and 5-lipoxygenase in the ECV304/C6 cell culture model of the blood-brain barrier Brain Res 953 157 169 12384249 10.1016/S0006-8993(02)03281-X 1:CAS:528:DC%2BD38XnvVOlu7k%3D (Pubitemid 35217817)
20. D Wong K Dorovini-Zis SR Vincent 2004 Cytokines, nitric oxide, and cGMP modulate the permeability of an in vitro model of the human blood-brain barrier Exp Neurol 190 446 455 15530883 10.1016/j.expneurol.2004.08.008 1:CAS:528:DC%2BD2cXpsVOkt7o%3D (Pubitemid 39504999)
21. E Fuller C Duckham E Wood 2007 Disruption of epithelial tight junctions by yeast enhances the paracellular delivery of a model protein Pharm Res 24 37 47 16969693 10.1007/s11095-006-9124-0 1:CAS:528:DC%2BD28Xht1yis7zI (Pubitemid 44902568)
22. KP Nunes CS Rigsby RC Webb 2010 RhoA/Rho-kinase and vascular diseases: what is the link? Cell Mol Life Sci 67 3823 3836 20668910 10.1007/s00018-010- 0460-1 1:CAS:528:DC%2BC3cXht12qurrP
23. JK Liao M Seto K Noma 2007 Rho kinase (ROCK) inhibitors J Cardiovasc Pharmacol 50 17 24 17666911 10.1097/FJC.0b013e318070d1bd 1:CAS:528: DC%2BD2sXosFGju7o%3D (Pubitemid 47220442)
24. SP Davies H Reddy M Caivano P Cohen 2000 Specificity and mechanism of action of some commonly used protein kinase inhibitors Biochem J 351 95 105 10998351 10.1042/0264-6021:3510095 1:CAS:528:DC%2BD3cXnslWltrY%3D
25. ST Narumiya M Ishizaki Uehata 2000 Use and properties of ROCKspecific inhibitor Y-27632 Methods Enzymol 325 273 284 11036610 10.1016/S0076-6879(00) 25449-9 1:CAS:528:DC%2BD3cXot1ajtr8%3D
26. AJ Ridley 2001 Rho family proteins: coordinating cell responses Trends Cell Biol 11 471 477 11719051 10.1016/S0962-8924(01)02153-5 1:CAS:528: DC%2BD3MXosFKls78%3D (Pubitemid 33079138)
27. O Nakagawa K Fujisawa T Ishizaki Y Saito K Nakao S Narumiya 1996 ROCK-I and ROCK-II, two isoforms of Rho-associated coiled-coil forming protein serine/threonine kinase in mice FEBS Lett 392 189 193 8772201 10.1016/0014-5793(96)00811-3 1:CAS:528:DyaK28Xlt1Kitrk%3D (Pubitemid 26276745)
28. F Di Cunto S Imarisio E Hirsch V Broccoli A Bulfone A Migheli C Atzori E Turco R Triolo GP Dotto L Silengo F Altruda 2000 Defective neurogenesis in citron kinase knockout mice by altered cytokinesis and massive apoptosis Neuron 28 115 127 11086988 10.1016/S0896-6273(00)00090-8 1:CAS:528:DC%2BD3cXnvVGlt7Y%3D
29. L Wei W Roberts L Wang M Yamada S Zhang Z Zhao SA Rivkees RJ Schwartz K Imanaka-Yoshida 2001 Rho kinases play an obligatory role in vertebrate embryonic organogenesis Development 128 2953 2962 11532918 1:CAS:528:DC%2BD3MXmtlCrtLo%3D (Pubitemid 32771627)
30. PY Liu JK Liao 2008 A method for measuring Rho kinase activity in tissues and cells Methods Enzymol 39 181 189 10.1016/S0076-6879(07)00414-4
31. NM Rubenstein JA Callahan DH Lo GL Firestone 2007 Selective glucocorticoid control of Rho kinase isoforms regulate cell-cell interactions Biochem Biophys Res Commun 354 603 607 17240358 10.1016/j.bbrc.2007.01.024 1:CAS:528:DC%2BD2sXhtlOgtb0%3D (Pubitemid 46161368)
32. PY Mong Q Wang 2009 Activation of Rho kinase isoforms in lung endothelial cells during inflammation J Immunol 182 2385 2394 19201893 10.4049/jimmunol. 0802811 1:CAS:528:DC%2BD1MXhsFKrsL0%3D
33. NS Harhaj DA Antonetti 2004 Regulation of tight junctions and loss of barrier function in pathophysiology Int J Biochem Cell Biol 36 1206 1237 15109567 10.1016/j.biocel.2003.08.007 1:CAS:528:DC%2BD2cXjsVWnsb8%3D (Pubitemid 38519069)
34. CB Collares-Buzato MA Jepson NL Simmons BH Hirst 1998 Increased tyrosine phosphorylation causes redistribution of adherens junction and tight junction proteins and perturbs paracellular barrier function in MDCK epithelia Eur J Cell Biol 76 85 92 9696347 1:CAS:528:DyaK1cXktVKltb4%3D (Pubitemid 28312630)
35. AV Keita JD Söderholm 2010 The intestinal barrier and its regulation by neuroimmune factors Neurogastroenterol Motil 22 718 733 20377785 10.1111/j.1365-2982.2010.01498.x 1:CAS:528:DC%2BC3cXps1emtrg%3D
36. K Kubota M Furuse H Sasaki N Sonoda K Fujita A Nagafuchi S Tsukita 1999 Ca(2 +)-independent cell-adhesion activity of claudins, a family of integral membrane proteins localized at tight junctions Curr Biol 9 1035 1038 10508613 10.1016/S0960-9822(99)80452-7 1:CAS:528:DyaK1MXmtlags7Y%3D (Pubitemid 29456172)
37. LL Mitic CM Van Itallie JM Anderson 2000 Molecular physiology and pathophysiology of tight junctions I. Tight junction structure and function: lessons from mutant animals and proteins Am J Physiol Gastrointest Liver Physiol 279 G250 G254 10915631 1:CAS:528:DC%2BD3cXmtFyjtb4%3D
38. D Olivera C Knall S Boggs J Seagrave 2010 Cytoskeletal modulation and tyrosine phosphorylation of tight junction proteins are associated with mainstream cigarette smoke-induced permeability of airway epithelium Exp Toxicol Pathol 62 133 143 19376691 10.1016/j.etp.2009.03.002 1:CAS:528: DC%2BC3cXlsFSmu70%3D
39. DS Olivera SE Boggs C Beenhouwer J Aden C Knall 2007 Cellular mechanisms of mainstream cigarette smoke-induced lung epithelial tight junction permeability changes in vitro Inhal Toxicol 19 13 22 17127639 10.1080/08958370600985768 1:CAS:528:DC%2BD2sXjsVSjtbs%3D (Pubitemid 44863600)
40. SH Chen MF Stins SH Huang YH Chen KJ Kwon-Chung Y Chang KS Kim K Suzuki AY Jong 2003 Cryptococcus deformans induces alterations in the cytoskeleton of human brain microvascular endothelial cells J Med Microbiol 52 961 970 14532340 10.1099/jmm.0.05230-0 1:CAS:528:DC%2BD2cXktVGmtbs%3D (Pubitemid 38648135)
41. T Tenenbaum D Matalon R Adam A Seibt C Wewer C Schwerk HJ Galla H Schroten 2008 Dexamethasone prevents alteration of tight junction-associated proteins and barrier function in porcine choroid plexus epithelial cells after infection with Streptococcus suis in vitro Brain Res 1229 1 17 18644352 10.1016/j.brainres.2008.06.118 1:CAS:528:DC%2BD1cXhtVejsrbM
42. Q Li Q Zhang C Wang X Liu L Qu L Gu N Li J Li 2009 Altered distribution of tight junction proteins after intestinal ischaemia/reperfusion injury in rats J Cell Mol Med 13 4061 4076 19929946 10.1111/j.1582-4934.2009.00975.x
43. PK Nighot AJ Moeser KA Ryan T Ghashghaei AT Blikslager 2009 ClC-2 is required for rapid restoration of epithelial tight junctions in ischemic-injured murine jejunum Exp Cell Res 315 110 118 18976652 10.1016/j.yexcr.2008.10.001 1:CAS:528:DC%2BD1cXhsVOis7%2FN
44. SM Dudek JG Garcia 2001 Cytoskeletal regulation of pulmonary vascular permeability J Appl Physiol 91 1487 1500 11568129 1:CAS:528:DC%2BD3MXnsFSlsr8%3D (Pubitemid 32900340)
45. AA Birukova K Smurova KG Birukovm K Kaibuchi JG Garcia AD Verin 2004 Role of Rho GTPases in thrombin-induced lung vascular endothelial cells barrier dysfunction Microvasc Res 67 64 77 14709404 10.1016/j.mvr.2003.09.007 1:CAS:528:DC%2BD2cXosF2j (Pubitemid 38050225)
46. JW Breslin SY Yuan 2004 Involvement of RhoA and Rho kinase in neutrophil-stimulated endothelial hyperpermeability Am J Physiol Heart Circ Physiol 286 H1057 H1062 14630629 10.1152/ajpheart.00841.2003 1:CAS:528:DC%2BD2cXitlShsbw%3D
47. SL Müller M Portwich A Schmidt DI Utepbergenov O Huber IE Blasig G Krause 2005 The tight junction protein occludin and the adherens junction protein alpha-catenin share a common interaction mechanism with ZO-1 J Biol Chem 280 3747 3756 15548514 10.1074/jbc.M411365200 (Pubitemid 40223843)
48. AM Hopkins SV Walsh P Verkade P Boquet A Nusrat 2003 Constitutive activation of Rho proteins by CNF-1 influences tight junction structure and epithelial barrier function J Cell Sci 116 725 742 12538773 10.1242/jcs.00300 1:CAS:528:DC%2BD3sXhvVOkuro%3D (Pubitemid 36231311)
49. R Niwa K Nagata-Ohashi M Takeichi K Mizuno T Uemura 2002 Control of actin reorganization by slingshot, a family of phosphatases that dephosphorylate ADF/cofilin Cell 108 233 246 11832213 10.1016/S0092-8674(01)00638-9 1:CAS:528:DC%2BD38XhtV2hsbo%3D (Pubitemid 34161143)
50. M Brown D Adyshev V Bindokas J Moitra JG Garcia SM Dudek 2010 Quantitative distribution and colocalization of non-muscle myosin light chain kinase isoforms and cortactin in human lung endothelium Microvasc Res 80 75 88 20053363 10.1016/j.mvr.2009.12.010 1:CAS:528:DC%2BC3cXmslGltrw%3D
51. M Ikebe DJ Hartshorne 1985 Phosphorylation of smooth muscle myosin at two distinct sites by myosin light chain kinase J Biol Chem 260 10027 10031 3839510 1:CAS:528:DyaL2MXltlOls7g%3D (Pubitemid 16244088)
52. K Kimura M Ito M Amano K Chihara Y Fukata M Nakafuku B Yamamori J Feng T Nakano K Okawa A Iwamatsu K Kaibuchi 1996 Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase) Science 273 245 248 8662509 10.1126/science.273.5272.245 1:CAS:528:DyaK28Xkt1Crs7Y%3D (Pubitemid 26285892)
53. RA Moyer MK Wendt PA Johanesen JR Turner MB Dwinell 2007 Rho activation regulates CXCL12 chemokine stimulated actin rearrangement and restitution in model intestinal epithelia Lab Invest 87 807 817 17572689 10.1038/labinvest. 3700595 1:CAS:528:DC%2BD2sXnvVektr4%3D (Pubitemid 47077260)
54. WY Lui WM Lee CY Cheng 2003 Sertoli-germ cell adherens junction dynamics in the testis are regulated by RhoB GTPase via the ROCK/LIMK signaling pathway Biol Reprod 68 2189 2206 12606349 10.1095/biolreprod.102.011379 1:CAS:528:DC%2BD3sXks1Ggsbg%3D (Pubitemid 36687012)
55. JR Bamburg 1999 Proteins of the ADF/cofilin family: essential regulators of actin dynamics Annu Rev Cell Dev Biol 15 185 230 10611961 10.1146/annurev.cellbio.15.1.185 1:CAS:528:DC%2BD3cXhtVSnurw%3D (Pubitemid 32250375)
56. Y Nagumo J Han A Bellila H Isoda T Tanaka 2008 Cofilin mediates tight-junction opening by redistributing actin and tight-junction proteins Biochem Biophys Res Commun 377 921 925 18952063 10.1016/j.bbrc.2008.10.071 1:CAS:528:DC%2BD1cXhsVais7vO
57. M Amano M Ito K Kimura Y Fukata K Chihara T Nakano Y Matsuura K Kaibuchi 1996 Phosphorylation and activation of myosin by Rho-associated kinase(Rho-kinase) J Biol Chem 271 20246 20249 8702756 10.1074/jbc.271.34.20246 1:CAS:528:DyaK28Xlt1ygt7Y%3D (Pubitemid 26281788)
58. AS Easton NJ Abbott 1997 The effects of bradykinin on a cell culture model of the blood-brain barrier J Physiol 505 49 50
59. TJ Manning Jr JC Parker H Sontheimer 2000 Role of lysophosphatidic acid and rho in glioma cell motility Cell Motil Cytoskeleton 5 185 199 10.1002/(SICI)1097-0169(200003)45:3<185::AID-CM2>3.0.CO;2-G (Pubitemid 30151738)
60. C Liu J Zuo LJ Janssen 2006 Regulation of airway smooth muscle RhoA/ROCK activities by cholinergic and bronchodilator stimuli Eur Respir J 28 703 711 16774953 10.1183/09031936.06.00025506 (Pubitemid 46335530)
61. R Arita Y Hata S Nakao T Kita M Miura S Kawahara S Zandi L Almulki F Tayyari H Shimokawa A Hafezi-Moghadam T Ishibashi 2009 Rho kinase inhibition by fasudil ameliorates diabetes-induced microvascular damage Diabetes 58 215 226 18840783 10.2337/db08-0762 1:CAS:528:DC%2BD1MXptVCnsA%3D%3D