Rho GEFs in endothelial junctions effector selectivity and signaling integration determine junctional response

Tissue Barriers

Volumn 1, Issue 5, 2013, Pages

  Ngok, Siu P ^a   Anastasiadis, Panos Z ^a  

^a MAYO CLINIC   (United States)

Author keywords

Adhesion; Cadherin; Cell junctions; Endothelial; Epithelial; GEFs; References; Rho GTPases

Indexed keywords

ANGIOPOIETIN 1; CADHERIN; CATENIN; DIA1 PROTEIN; PDZ PROTEIN; PEPTIDES AND PROTEINS; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHO KINASE; SYNECTIN BINDING RHOA EXCHANGE FACTOR; TIGHT JUNCTION PROTEIN; TUMOR ENDOTHELIAL MARKER 4; UNCLASSIFIED DRUG; UVOMORULIN; VASCULOTROPIN; ZONULA OCCLUDENS PROTEIN;

CELL JUNCTION; CELL MIGRATION; ENDOTHELIUM; ENDOTHELIUM CELL; HUMAN; NONHUMAN; NOTE; SIGNAL TRANSDUCTION;

EID: 84922249070     PISSN: 21688362     EISSN: 21688370     Source Type: Journal    
DOI: None     Document Type: Note

References (60)

1. Hartsock A, Nelson WJ. Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta 2008; 1778:660-9. PMID:17854762 http://dx.doi. org/10.1016/j.bbamem.2007.07.012
2. Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature 2002; 420:629-35. PMID:12478284 http://dx.doi.org/10.1038/nature01148
3. Ngok SP, Geyer R, Liu M, Kourtidis A, Agrawal S, Wu C, Seerapu HR, Lewis-Tuffin LJ, Moodie KL, Huveldt D, et al. VEGF and Angiopoietin-1 exert opposing effects on cell junctions by regulating the Rho GEF Syx. J Cell Biol 2012; 199:1103-15. PMID:23253477 http://dx.doi.org/10.1083/ jcb.201207009
4. De Toledo M, Coulon V, Schmidt S, Fort P, Blangy A. The gene for a new brain specific RhoA exchange factor maps to the highly unstable chromosomal region 1p36.2-1p36.3. Oncogene 2001; 20:7307-17. PMID:11704860 http://dx.doi.org/10.1038/ sj.onc.1204921
5. Marx R, Henderson J, Wang J, Baraban JM. Tech: a RhoA GEF selectively expressed in hippocampal and cortical neurons. J Neurochem 2005; 92:850-8. PMID:15686487 http://dx.doi. org/10.1111/j.1471-4159.2004.02930.x
6. Ngok SP, Geyer R, Kourtidis A, Storz P, Anastasiadis PZ. Phosphorylation-mediated 14-3-3 protein binding regulates the function of the rho-specific guanine nucleotide exchange factor (RhoGEF) Syx. J Biol Chem 2013; 288:6640-50. PMID:23335514 http:// dx.doi.org/10.1074/jbc.M112.432682
7. Liu M, Horowitz A. A PDZ-binding motif as a critical determinant of Rho guanine exchange factor function and cell phenotype. Mol Biol Cell 2006; 17:1880-7. PMID:16467373 http://dx.doi.org/10.1091/mbc. E06-01-0002
8. Garnaas MK, Moodie KL, Liu ML, Samant GV, Li K, Marx R, Baraban JM, Horowitz A, Ramchandran R. Syx, a RhoA guanine exchange factor, is essential for angiogenesis in Vivo. Circ Res 2008; 103:710-6. PMID:18757825 http://dx.doi.org/10.1161/ CIRCRESAHA.108.181388
9. Estévez MA, Henderson JA, Ahn D, Zhu XR, Poschmann G, Lübbert H, Marx R, Baraban JM. The neuronal RhoA GEF, Tech, interacts with the synaptic multi-PDZ-domain-containing protein, MUPP1. J Neurochem 2008; 106:1287-97. PMID:18537874 http://dx.doi.org/10.1111/j.1471-4159.2008.05472.x
10. Ernkvist M, Luna Persson N, Audebert S, Lecine P, Sinha I, Liu M, Schlueter M, Horowitz A, Aase K, Weide T, et al. The Amot/Patj/Syx signaling complex spatially controls RhoA GTPase activity in migrating endothelial cells. Blood 2009; 113:244-53. PMID:18824598 http://dx.doi.org/10.1182/ blood-2008-04-153874
11. Huang H, Bhat A, Woodnutt G, Lappe R. Targeting the ANGPT-TIE2 pathway in malignancy. Nat Rev Cancer 2010; 10:575-85. PMID:20651738 http:// dx.doi.org/10.1038/nrc2894
12. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 1996; 87:1171-80. PMID:8980224 http://dx.doi.org/10.1016/ S0092-8674(00)81813-9
13. Thurston G, Rudge JS, Ioffe E, Zhou H, Ross L, Croll SD, Glazer N, Holash J, McDonald DM, Yancopoulos GD. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat Med 2000; 6:460-3. PMID:10742156 http://dx.doi.org/10.1038/74725
14. Thurston G, Suri C, Smith K, McClain J, Sato TN, Yancopoulos GD, McDonald DM. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science 1999; 286:2511-4. PMID:10617467 http://dx.doi.org/10.1126/ science.286.5449.2511
15. Esser S, Lampugnani MG, Corada M, Dejana E, Risau W. Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J Cell Sci 1998; 111:1853-65. PMID:9625748
16. Gavard J, Patel V, Gutkind JS. Angiopoietin-1 prevents VEGF-induced endothelial permeability by sequestering Src through mDia. Dev Cell 2008; 14:25-36. PMID:18194650 http://dx.doi. org/10.1016/j.devcel.2007.10.019
17. Antonetti DA, Barber AJ, Hollinger LA, Wolpert EB, Gardner TW. Vascular endothelial growth factor induces rapid phosphorylation of tight junction proteins occludin and zonula occluden 1. A potential mechanism for vascular permeability in diabetic retinopathy and tumors. J Biol Chem 1999; 274:23463-7. PMID:10438525 http://dx.doi.org/10.1074/ jbc.274.33.23463
18. Pedram A, Razandi M, Levin ER. Deciphering vascular endothelial cell growth factor/vascular permeability factor signaling to vascular permeability. Inhibition by atrial natriuretic peptide. J Biol Chem 2002; 277:44385-98. PMID:12213803 http://dx.doi.org/10.1074/jbc.M202391200
19. Parikh SM, Mammoto T, Schultz A, Yuan HT, Christiani D, Karumanchi SA, Sukhatme VP. Excess circulating angiopoietin-2 may contribute to pulmonary vascular leak in sepsis in humans. PLoS Med 2006; 3:e46. PMID:16417407 http://dx.doi. org/10.1371/journal.pmed.0030046
20. Mackow ER, Gavrilovskaya IN. Hantavirus regulation of endothelial cell functions. Thromb Haemost 2009; 102:1030-41. PMID:19967132
21. Weis SM, Cheresh DA. Pathophysiological consequences of VEGF-induced vascular permeability. Nature 2005; 437:497-504. PMID:16177780 http://dx.doi.org/10.1038/nature03987
22. Smalley-Freed WG, Efimov A, Burnett PE, Short SP, Davis MA, Gumucio DL, Washington MK, Coffey RJ, Reynolds AB. p120-catenin is essential for maintenance of barrier function and intestinal homeostasis in mice. J Clin Invest 2010; 120:1824-35. PMID:20484816 http://dx.doi.org/10.1172/ JCI41414
23. Cho JH, Nicolae DL, Ramos R, Fields CT, Rabenau K, Corradino S, Brant SR, Espinosa R, LeBeau M, Hanauer SB, et al. Linkage and linkage disequilibrium in chromosome band 1p36 in American Chaldeans with inflammatory bowel disease. Hum Mol Genet 2000; 9:1425-32. PMID:10814724 http://dx.doi.org/10.1093/hmg/9.9.1425
24. Marshall B, Isidro G, Martins AG, Boavida MG. Loss of heterozygosity at chromosome 9p21 in primary neuroblastomas: evidence for two deleted regions. Cancer Genet Cytogenet 1997; 96:134-9. PMID:9216721 http://dx.doi.org/10.1016/ S0165-4608(96)00300-7
25. Shin K, Wang Q, Margolis B. PATJ regulates directional migration of mammalian epithelial cells. EMBO Rep 2007; 8:158-64. PMID:17235357 http://dx.doi.org/10.1038/sj.embor.7400890
26. Breitsprecher D, Goode BL. Formins at a glance. J Cell Sci 2013; 126:1-7. PMID:23516326 http:// dx.doi.org/10.1242/jcs.107250
27. Rath N, Olson MF. Rho-associated kinases in tumorigenesis: re-considering ROCK inhibition for cancer therapy. EMBO Rep 2012; 13:900-8. PMID:22964758 http://dx.doi.org/10.1038/ embor.2012.127
28. Watanabe N, Kato T, Fujita A, Ishizaki T, Narumiya S. Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nat Cell Biol 1999; 1:136-43. PMID:10559899 http://dx.doi. org/10.1038/11056
29. Gavard J, Gutkind JS. VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol 2006; 8:1223-34. PMID:17060906 http://dx.doi. org/10.1038/ncb1486
30. Carramusa L, Ballestrem C, Zilberman Y, Bershadsky AD. Mammalian diaphanous-related formin Dia1 controls the organization of E-cadherin-mediated cell-cell junctions. J Cell Sci 2007; 120:3870-82. PMID:17940061 http://dx.doi.org/10.1242/ jcs.014365
31. Kobielak A, Pasolli HA, Fuchs E. Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables. Nat Cell Biol 2004; 6:21-30. PMID:14647292 http://dx.doi. org/10.1038/ncb1075
32. Thumkeo D, Shinohara R, Watanabe K, Takebayashi H, Toyoda Y, Tohyama K, Ishizaki T, Furuyashiki T, Narumiya S. Deficiency of mDia, an actin nucleator, disrupts integrity of neuroepithelium and causes periventricular dysplasia. PLoS One 2011; 6:e25465. PMID:21980468 http://dx.doi.org/10.1371/journal.pone.0025465
33. Xie H, Xue YX, Liu LB, Liu YH, Wang P. Role of RhoA/ROCK signaling in endothelial-monocyte-activating polypeptide II opening of the blood-tumor barrier: role of RhoA/ROCK signaling in EMAP II opening of the BTB. J Mol Neurosci 2012; 46:666-76. PMID:21647708 http://dx.doi.org/10.1007/ s12031-011-9564-9
34. Sanchez T, Skoura A, Wu MT, Casserly B, Harrington EO, Hla T. Induction of vascular permeability by the sphingosine-1-phosphate receptor-2 (S1P2R) and its downstream effectors ROCK and PTEN. Arterioscler Thromb Vasc Biol 2007; 27:1312-8. PMID:17431187 http://dx.doi.org/10.1161/ATVBAHA.107.143735
35. Zandy NL, Playford M, Pendergast AM. Abl tyrosine kinases regulate cell-cell adhesion through Rho GTPases. Proc Natl Acad Sci U S A 2007; 104:17686-91. PMID:17965237 http://dx.doi.org/10.1073/ pnas.0703077104
36. Sahai E, Marshall CJ. ROCK and Dia have opposing effects on adherens junctions downstream of Rho. Nat Cell Biol 2002; 4:408-15. PMID:11992112 http://dx.doi.org/10.1038/ncb796
37. Chang YW, Marlin JW, Chance TW, Jakobi R. RhoA mediates cyclooxygenase-2 signaling to disrupt the formation of adherens junctions and increase cell motility. Cancer Res 2006; 66:11700-8. PMID:17178865 http://dx.doi.org/10.1158/0008- 5472.CAN-06-1818
38. 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. J Cell Sci 2003; 116:4615-28. PMID:14576355 http://dx.doi.org/10.1242/jcs.00755
39. Wojciak-Stothard B, Ridley AJ. Rho GTPases and the regulation of endothelial permeability. Vascul Pharmacol 2002; 39:187-99. PMID:12747959 http://dx.doi.org/10.1016/S1537-1891(03)00008-9
40. Ma T, Liu L, Wang P, Xue Y. Evidence for involvement of ROCK signaling in bradykinin-induced increase in murine blood-tumor barrier permeability. J Neurooncol 2012; 106:291-301. PMID:21892742 http://dx.doi.org/10.1007/s11060-011-0685-3
41. Gavard J, Gutkind JS. Protein kinase C-related kinase and ROCK are required for thrombin-induced endothelial cell permeability downstream from Galpha12/13 and Galpha11/q. J Biol Chem 2008; 283:29888-96. PMID:18713748 http://dx.doi. org/10.1074/jbc.M803880200
42. van Nieuw Amerongen GP, Beckers CM, Achekar ID, Zeeman S, Musters RJ, van Hinsbergh VW. Involvement of Rho kinase in endothelial barrier maintenance. Arterioscler Thromb Vasc Biol 2007; 27:2332-9. PMID:17761936 http://dx.doi. org/10.1161/ATVBAHA.107.152322
43. Smith AL, Dohn MR, Brown MV, Reynolds AB. Association of Rho-associated protein kinase 1 with E-cadherin complexes is mediated by p120-catenin. Mol Biol Cell 2012; 23:99-110. PMID:22031287 http://dx.doi.org/10.1091/mbc.E11-06-0497
44. Walsh SV, Hopkins AM, Chen J, Narumiya S, Parkos CA, Nusrat A. Rho kinase regulates tight junction function and is necessary for tight junction assembly in polarized intestinal epithelia. Gastroenterology 2001; 121:566-79. PMID:11522741 http://dx.doi. org/10.1053/gast.2001.27060
45. Miyake Y, Inoue N, Nishimura K, Kinoshita N, Hosoya H, Yonemura S. Actomyosin tension is required for correct recruitment of adherens junction components and zonula occludens formation. Exp Cell Res 2006; 312:1637-50. PMID:16519885 http://dx.doi.org/10.1016/j.yexcr.2006.01.031
46. Shewan AM, Maddugoda M, Kraemer A, Stehbens SJ, Verma S, Kovacs EM, Yap AS. Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol Biol Cell 2005; 16:4531-42. PMID:16030252 http://dx.doi. org/10.1091/mbc.E05-04-0330
47. Shimada H, Rajagopalan LE. Rho kinase-2 activation in human endothelial cells drives lysophosphatidic acid-mediated expression of cell adhesion molecules via NF-kappaB p65. J Biol Chem 2010; 285:12536-42. PMID:20164172 http://dx.doi.org/10.1074/jbc.M109.099630
48. Bryan BA, Dennstedt E, Mitchell DC, Walshe TE, Noma K, Loureiro R, Saint-Geniez M, Campaigniac JP, Liao JK, D'Amore PA. RhoA/ROCK signaling is essential for multiple aspects of VEGF-mediated angiogenesis. FASEB J 2010; 24:3186-95. PMID:20400538 http://dx.doi.org/10.1096/ fj.09-145102
49. Montalvo J, Spencer C, Hackathorn A, Masterjohn K, Perkins A, Doty C, Arumugam A, Ongusaha PP, Lakshmanaswamy R, Liao JK, et al. ROCK1 & 2 perform overlapping and unique roles in angiogenesis and angiosarcoma tumor progression. Curr Mol Med 2013; 13:205-19. PMID:22934846 http://dx.doi. org/10.2174/156652413804486296
50. Nishimura T, Takeichi M. Shroom3-mediated recruitment of Rho kinases to the apical cell junctions regulates epithelial and neuroepithelial planar remodeling. Development 2008; 135:1493-502. PMID:18339671 http://dx.doi.org/10.1242/ dev.019646
51. Terry SJ, Zihni C, Elbediwy A, Vitiello E, Leefa Chong San IV, Balda MS, Matter K. Spatially restricted activation of RhoA signalling at epithelial junctions by p114RhoGEF drives junction formation and morphogenesis. Nat Cell Biol 2011; 13:159-66. PMID:21258369 http://dx.doi.org/10.1038/ ncb2156
52. Narumiya S, Tanji M, Ishizaki T. Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion. Cancer Metastasis Rev 2009; 28:65-76. PMID:19160018 http://dx.doi.org/10.1007/ s10555-008-9170-7
53. Taguchi K, Ishiuchi T, Takeichi M. Mechanosensitive EPLIN-dependent remodeling of adherens junctions regulates epithelial reshaping. J Cell Biol 2011; 194:643-56. PMID:21844208 http://dx.doi. org/10.1083/jcb.201104124
54. Takeya R, Taniguchi K, Narumiya S, Sumimoto H. The mammalian formin FHOD1 is activated through phosphorylation by ROCK and mediates thrombin-induced stress fibre formation in endothelial cells. EMBO J 2008; 27:618-28. PMID:18239683 http:// dx.doi.org/10.1038/emboj.2008.7
55. Hannemann S, Madrid R, Stastna J, Kitzing T, Gasteier J, Schönichen A, Bouchet J, Jimenez A, Geyer M, Grosse R, et al. The Diaphanous-related Formin FHOD1 associates with ROCK1 and promotes Src-dependent plasma membrane blebbing. J Biol Chem 2008; 283:27891-903. PMID:18694941 http://dx.doi.org/10.1074/jbc.M801800200
56. Staus DP, Taylor JM, Mack CP. Enhancement of mDia2 activity by Rho-kinase-dependent phosphorylation of the diaphanous autoregulatory domain. Biochem J 2011; 439:57-65. PMID:21699497 http://dx.doi.org/10.1042/BJ20101700
57. Shi Y, Zhang J, Mullin M, Dong B, Alberts AS, Siminovitch KA. The mDial formin is required for neutrophil polarization, migration, and activation of the LARG/RhoA/ROCK signaling axis during chemotaxis. J Immunol 2009; 182:3837-45. PMID:19265163 http://dx.doi.org/10.4049/ jimmunol.0803838
58. Kitzing TM, Sahadevan AS, Brandt DT, Knieling H, Hannemann S, Fackler OT, Grosshans J, Grosse R. Positive feedback between Dia1, LARG, and RhoA regulates cell morphology and invasion. Genes Dev 2007; 21:1478-83. PMID:17575049 http://dx.doi. org/10.1101/gad.424807
59. Ngok SP, Geyer R, Kourtidis A, Mitin N, Feathers R, Der C, Anastasiadis PZ. TEM4 is a junctional Rho GEF required for cell-cell adhesion, monolayer integrity and barrier function. J Cell Sci 2013; 126:3271-7. PMID:23729734 http://dx.doi.org/10.1242/ jcs.123869
60. Ratheesh A, Gomez GA, Priya R, Verma S, Kovacs EM, Jiang K, Brown NH, Akhmanova A, Stehbens SJ, Yap AS. Centralspindlin and α-catenin regulate Rho signalling at the epithelial zonula adherens. Nat Cell Biol 2012; 14:818-28. PMID:22750944 http:// dx.doi.org/10.1038/ncb2532