eNOS-derived nitric oxide regulates endothelial barrier function through VE-cadherin and Rho GTPases

Journal of Cell Science

Volumn 126, Issue 24, 2013, Pages 5541-5552

  Lorenzo, Annarita Di ^a   Lin, Michelle I ^a   Murata, Takahisa ^b   Landskroner Eiger, Shira ^a   Schleicher, Michael ^a   Kothiya, Milankumar ^c   Iwakiri, Yasuko ^a   Yu, Jun ^a   Huang, Paul L ^d   Sessa, William C ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Cadherin 5; Cytoskeleton; eNOS; Nitric oxide; Src; VE cadherin; VEGF

Indexed keywords

ACTIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; HISTAMINE; NITRIC OXIDE; PROTEIN TYROSINE KINASE; RAC GUANINE NUCLEOTIDE EXCHANGE FACTOR TIAM1; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO KINASE; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN;

ANIMAL EXPERIMENT; ARTICLE; BLOOD VESSEL PERMEABILITY; CELL JUNCTION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE MUTATION; HUMAN; HUMAN CELL; IN VIVO STUDY; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; STRESS FIBER; VASCULAR ENDOTHELIUM;

CADHERIN 5; CYTOSKELETON; ENOS; NITRIC OXIDE; SRC; VE-CADHERIN; VEGF;

ADHERENS JUNCTIONS; ANIMALS; ANTIGENS, CD; CADHERINS; CAPILLARY PERMEABILITY; CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; SRC-FAMILY KINASES; STRESS FIBERS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84890497863     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.115972     Document Type: Article

References (62)

1. Ackah, E., Yu, J., Zoellner, S., Iwakiri, Y., Skurk, C., Shibata, R., Ouchi, N., Easton, R.M., Galasso, G., Birnbaum, M.J. et al. (2005). Akt1/protein kinase Balpha is critical for ischemic and VEGF-mediated angiogenesis. J. Clin. Invest. 115, 2119-2127.
2. Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., Matsuura, Y. and Kaibuchi, K. (1996). Phosphorylation and activation of myosin by Rhoassociated kinase (Rho-kinase). J. Biol. Chem. 271, 20246-20249.
3. Andriopoulou, P., Navarro, P., Zanetti, A., Lampugnani, M.G. and Dejana, E. (1999). Histamine induces tyrosine phosphorylation of endothelial cell-to-cell adherens junctions. Arterioscler. Thromb. Vasc. Biol. 19, 2286-2297.
4. Angelini, D.J., Hyun, S.W., Grigoryev, D.N., Garg, P., Gong, P., Singh, I.S., Passaniti, A., Hasday, J.D. and Goldblum, S.E. (2006). TNF-alpha increases tyrosine phosphorylation of vascular endothelial cadherin and opens the paracellular pathway through fyn activation in human lung endothelia. Am. J. Physiol. 291, L1232-L1245.
5. Aramoto, H., Breslin, J.W., Pappas, P.J., Hobson, R.W., 2nd and Durán, W.N. (2004). Vascular endothelial growth factor stimulates differential signaling pathways in in vivo microcirculation. Am. J. Physiol. 287, H1590-H1598.
6. Benard, V., Bohl, B.P. and Bokoch, G.M. (1999). Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J. Biol. Chem. 274, 13198-13204.
7. Bernatchez, P.N., Bauer, P.M., Yu, J., Prendergast, J.S., He, P. and Sessa, W.C. (2005). Dissecting the molecular control of endothelial NO synthase by caveolin-1 using cell-permeable peptides. Proc. Natl. Acad. Sci. USA 102, 761-766.
8. Broermann, A., Winderlich, M., Block, H., Frye, M., Rossaint, J., Zarbock, A., Cagna, G., Linnepe, R., Schulte, D., Nottebaum, A.F. et al. (2011). Dissociation of VE-PTP from VE-cadherin is required for leukocyte extravasation and for VEGFinduced vascular permeability in vivo. J. Exp. Med. 208, 2393-2401.
9. Bucci, M., Gratton, J.P., Rudic, R.D., Acevedo, L., Roviezzo, F., Cirino, G. and Sessa, W.C. (2000). In vivo delivery of the caveolin-1 scaffolding domain inhibits nitric oxide synthesis and reduces inflammation. Nat. Med. 6, 1362-1367.
10. Burridge, K. and Wennerberg, K. (2004). Rho and Rac take center stage. Cell 116, 167-179.
11. Catling, A.D., Wyke, J.A. and Frame, M.C. (1993). Mitogenesis of quiescent chick fibroblasts by v-Src: dependence on events at the membrane leading to early changes in AP-1. Oncogene 8, 1875-1886.
12. Dejana, E. (2004). Endothelial cell-cell junctions: happy together. Nat. Rev. Mol. Cell Biol. 5, 261-270.
13. Di Lorenzo, A., Fernández-Hernando, C., Cirino, G. and Sessa, W.C. (2009). Akt1 is critical for acute inflammation and histamine-mediated vascular leakage. Proc. Natl. Acad. Sci. USA 106, 14552-14557.
14. Eliceiri, B.P., Paul, R., Schwartzberg, P.L., Hood, J.D., Leng, J. and Cheresh, D.A. (1999). Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol. Cell 4, 915-924.
15. Esser, S., Lampugnani, M.G., Corada, M., Dejana, E. and Risau, W. (1998). Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J. Cell Sci. 111, 1853-1865.
16. Feng, D., Nagy, J.A., Pyne, K., Hammel, I., Dvorak, H.F. and Dvorak, A.M. (1999). Pathways of macromolecular extravasation across microvascular endothelium in response to VPF/VEGF and other vasoactive mediators. Microcirculation 6, 23-44.
17. Ferrara, N., Gerber, H.P. and LeCouter, J. (2003). The biology of VEGF and its receptors. Nat. Med. 9, 669-676.
18. Fincham, V.J., Unlu, M., Brunton, V.G., Pitts, J.D., Wyke, J.A. and Frame, M.C. (1996). Translocation of Src kinase to the cell periphery is mediated by the actin cytoskeleton under the control of the Rho family of small G proteins. J. Cell Biol. 135, 1551-1564.
19. Fukumura, D., Yuan, F., Endo, M. and Jain, R.K. (1997). Role of nitric oxide in tumor microcirculation. Blood flow, vascular permeability, and leukocyte-endothelial interactions. Am. J. Pathol. 150, 713-725.
20. Fukumura, D., Gohongi, T., Kadambi, A., Izumi, Y., Ang, J., Yun, C.O., Buerk, D.G., Huang, P.L. and Jain, R.K. (2001). Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc. Natl. Acad. Sci. USA 98, 2604-2609.
21. Garcia, J.G., Liu, F., Verin, A.D., Birukova, A., Dechert, M.A., Gerthoffer, W.T., Bamberg, J.R. and English, D. (2001). Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J. Clin. Invest. 108, 689-701.
22. Gratton, J.P., Lin, M.I., Yu, J., Weiss, E.D., Jiang, Z.L., Fairchild, T.A., Iwakiri, Y., Groszmann, R., Claffey, K.P., Cheng, Y.C. et al. (2003a). Selective inhibition of tumor microvascular permeability by cavtratin blocks tumor progression in mice. Cancer Cell 4, 31-39.
23. Gratton, J.P., Yu, J., Griffith, J.W., Babbitt, R.W., Scotland, R.S., Hickey, R., Giordano, F.J. and Sessa, W.C. (2003b). Cell-permeable peptides improve cellular uptake and therapeutic gene delivery of replication-deficient viruses in cells and in vivo. Nat. Med. 9, 357-362.
24. Hall, A. (1998a). G proteins and small GTPases: distant relatives keep in touch. Science 280, 2074-2075.
25. Hall, A. (1998b). Rho GTPases and the actin cytoskeleton. Science 279, 509-514.
26. Hatakeyama, T., Pappas, P.J., Hobson, R.W., I. I, Boric, M.P., Sessa, W.C. and Durán, W.N. (2006). Endothelial nitric oxide synthase regulates microvascular hyperpermeability in vivo. J. Physiol. 574, 275-281.
27. Hordijk, P.L., ten Klooster, J.P., van der Kammen, R.A., Michiels, F., Oomen, L.C. and Collard, J.G. (1997). Inhibition of invasion of epithelial cells by Tiam1-Rac signaling. Science 278, 1464-1466.
28. Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J., Nakano, T., Okawa, K. et al. (1996). Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
29. Kiosses, W.B., Daniels, R.H., Otey, C., Bokoch, G.M. and Schwartz, M.A. (1999). A role for p21-activated kinase in endothelial cell migration. J. Cell Biol. 147, 831-844.
30. Lal, B.K., Varma, S., Pappas, P.J., Hobson, R.W., II and Durán, W.N. (2001). VEGF increases permeability of the endothelial cell monolayer by activation of PKB/ akt, endothelial nitric-oxide synthase, and MAP kinase pathways. Microvasc. Res. 62, 252-262.
31. Lampugnani, M.G., Corada, M., Andriopoulou, P., Esser, S., Risau, W. and Dejana, E. (1997). Cell confluence regulates tyrosine phosphorylation of adherens junction components in endothelial cells. J. Cell Sci. 110, 2065-2077.
32. Lampugnani, M.G., Zanetti, A., Breviario, F., Balconi, G., Orsenigo, F., Corada, M., Spagnuolo, R., Betson, M., Braga, V. and Dejana, E. (2002). VE-cadherin regulates endothelial actin activating Rac and increasing membrane association of Tiam. Mol. Biol. Cell 13, 1175-1189.
33. Lee, K.H., Lee, S.H., Kim, D., Rhee, S., Kim, C., Chung, C.H., Kwon, H. and Kang, M.S. (1999). Promotion of skeletal muscle differentiation by K252a with tyrosine phosphorylation of focal adhesion: a possible involvement of small GTPase Rho. Exp. Cell Res. 252, 401-415.
34. Marín, N., Zamorano, P., Carrasco, R., Mujica, P., González, F.G., Quezada, C., Meininger, C.J., Boric, M.P., Durán, W.N. and Sánchez, F.A. (2012). SNitrosation of b-catenin and p120 catenin: a novel regulatory mechanism in endothelial hyperpermeability. Circ. Res. 111, 553-563.
35. Mayhan, W.G. (1999). VEGF increases permeability of the blood-brain barrier via a nitric oxide synthase/cGMP-dependent pathway. Am. J. Physiol. 276, C1148-C1153.
36. Murohara, T., Asahara, T., Silver, M., Bauters, C., Masuda, H., Kalka, C., Kearney, M., Chen, D., Symes, J.F., Fishman, M.C. et al. (1998). Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J. Clin. Invest. 101, 2567-2578.
37. Papapetropoulos, A., Garciá-Cardeñ a, G., Madri, J.A. and Sessa, W.C. (1997). Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J. Clin. Invest. 100, 3131-3139.
38. Primo, L., Roca, C., Ferrandi, C., Lanfrancone, L. and Bussolino, F. (2000). Human endothelial cells expressing polyoma middle T induce tumors. Oncogene 19, 3632-3641.
39. Rahman, M.A., Senga, T., Ito, S., Hyodo, T., Hasegawa, H. and Hamaguchi, M. (2010). S-nitrosylation at cysteine 498 of c-Src tyrosine kinase regulates nitric oxide-mediated cell invasion. J. Biol. Chem. 285, 3806-3814.
40. Reid, T., Furuyashiki, T., Ishizaki, T., Watanabe, G., Watanabe, N., Fujisawa, K., Morii, N., Madaule, P. and Narumiya, S. (1996). Rhotekin, a new putative target for Rho bearing homology to a serine/threonine kinase, PKN, and rhophilin in the rhobinding domain. J. Biol. Chem. 271, 13556-13560.
41. Ridley, A.J. (2001). Rho family proteins: coordinating cell responses. Trends Cell Biol. 11, 471-477.
42. Ridley, A.J. and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
43. Ridley, A.J., Paterson, H.F., Johnston, C.L., Diekmann, D. and Hall, A. (1992). The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410.
44. Sander, E.E., van Delft, S., ten Klooster, J.P., Reid, T., van der Kammen, R.A., Michiels, F. and Collard, J.G. (1998). Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J. Cell Biol. 143, 1385-1398.
45. Sander, E.E., ten Klooster, J.P., van Delft, S., van der Kammen, R.A. and Collard, J.G. (1999). Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J. Cell Biol. 147, 1009-1022.
46. Schleicher, M., Yu, J., Murata, T., Derakhshan, B., Atochin, D., Qian, L., Kashiwagi, S., Di Lorenzo, A., Harrison, K.D., Huang, P.L. et al. (2009). The Akt1-eNOS axis illustrates the specificity of kinase-substrate relationships in vivo. Sci. Signal. 2, ra41.
47. Scotland, R.S., Morales-Ruiz, M., Chen, Y., Yu, J., Rudic, R.D., Fulton, D., Gratton, J.P. and Sessa, W.C. (2002). Functional reconstitution of endothelial nitric oxide synthase reveals the importance of serine 1179 in endothelium-dependent vasomotion. Circ. Res. 90, 904-910.
48. Sessa, W.C. (2004). eNOS at a glance. J. Cell Sci. 117, 2427-2429.
49. Shasby, D.M., Ries, D.R., Shasby, S.S. and Winter, M.C. (2002). Histamine stimulates phosphorylation of adherens junction proteins and alters their link to vimentin. Am. J. Physiol. 282, L1330-L1338.
50. Shikata, Y., Birukov, K.G., Birukova, A.A., Verin, A. and Garcia, J.G. (2003a). Involvement of site-specific FAK phosphorylation in sphingosine-1 phosphate-and thrombin-induced focal adhesion remodeling: role of Src and GIT. FASEB J. 17, 2240-2249.
51. Shikata, Y., Birukov, K.G. and Garcia, J.G. (2003b). S1P induces FA remodeling in human pulmonary endothelial cells: role of Rac, GIT1, FAK, and paxillin. J. Appl. Physiol. 94, 1193-1203.
52. Siddiqui, M.R., Komarova, Y.A., Vogel, S.M., Gao, X., Bonini, M.G., Rajasingh, J., Zhao, Y.Y., Brovkovych, V. and Malik, A.B. (2011). Caveolin-1-eNOS signaling promotes p190RhoGAP-A nitration and endothelial permeability. J. Cell Biol. 193, 841-850.
53. Soga, N., Namba, N., McAllister, S., Cornelius, L., Teitelbaum, S.L., Dowdy, S.F., Kawamura, J. and Hruska, K.A. (2001). Rho family GTPases regulate VEGFstimulated endothelial cell motility. Exp. Cell Res. 269, 73-87.
54. Thibeault, S., Rautureau, Y., Oubaha, M., Faubert, D., Wilkes, B.C., Delisle, C. and Gratton, J.P. (2010). S-nitrosylation of beta-catenin by eNOS-derived NO promotes VEGF-induced endothelial cell permeability. Mol. Cell 39, 468-476.
55. van Nieuw Amerongen, G.P., Koolwijk, P., Versteilen, A. and van Hinsbergh, V.W. (2003). Involvement of RhoA/Rho kinase signaling in VEGF-induced endothelial cell migration and angiogenesis in vitro. Arterioscler. Thromb. Vasc. Biol. 23, 211-217.
56. Verin, A.D., Birukova, A., Wang, P., Liu, F., Becker, P., Birukov, K. and Garcia, J.G. (2001). Microtubule disassembly increases endothelial cell barrier dysfunction: role of MLC phosphorylation. Am. J. Physiol. 281, L565-L574.
57. Weis, W.I. and Nelson, W.J. (2006). Re-solving the cadherin-catenin-actin conundrum. J. Biol. Chem. 281, 35593-35597.
58. Weis, S., Cui, J., Barnes, L. and Cheresh, D. (2004). Endothelial barrier disruption by VEGF-mediated Src activity potentiates tumor cell extravasation and metastasis. J. Cell Biol. 167, 223-229.
59. Wojciak-Stothard, B. and Ridley, A.J. (2002). Rho GTPases and the regulation of endothelial permeability. Vascul. Pharmacol. 39, 187-199.
60. Zachary, I. and Gliki, G. (2001). Signaling transduction mechanisms mediating biological actions of the vascular endothelial growth factor family. Cardiovasc. Res. 49, 568-581.
61. Zeng, Q., Lagunoff, D., Masaracchia, R., Goeckeler, Z., Côté, G. and Wysolmerski, R. (2000). Endothelial cell retraction is induced by PAK2 monophosphorylation of myosin II.J. Cell Sci. 113, 471-482.
62. Ziche, M., Morbidelli, L., Choudhuri, R., Zhang, H.T., Donnini, S., Granger, H.J. and Bicknell, R. (1997). Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J. Clin. Invest. 99, 2625-2634.