Drebrin preserves endothelial integrity by stabilizing nectin at adherens junctions

Journal of Cell Science

Volumn 126, Issue 16, 2013, Pages 3756-3769

  Rehm, Kerstin ^a   Panzer, Linda ^a   van Vliet, Vanessa ^a   Genot, Elisabeth ^b   Linder, Stefan ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b INSTITUT EUROPÉEN DE CHIMIE ET BIOLOGIE   (France)

Author keywords

Actin cytoskeleton; Afadin; Cell cell junctions; Drebrin; Endothelial cells; Nectin

Indexed keywords

AFADIN; DREBRIN; F ACTIN; GLYCOPROTEIN; NECTIN; PROLINE DERIVATIVE; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; BLOOD FLOW; CELL CONTACT; CELL JUNCTION; CONTROLLED STUDY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LYSOSOME; PDZ DOMAIN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; VASCULAR ENDOTHELIUM;

ACTIN CYTOSKELETON; AFADIN; CELL-CELL JUNCTIONS; DREBRIN; ENDOTHELIAL CELLS; NECTIN;

ACTIN CYTOSKELETON; ACTINS; ADHERENS JUNCTIONS; CELL ADHESION MOLECULES; CELL CULTURE TECHNIQUES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; NEUROPEPTIDES; PROTEIN BINDING; TRANSFECTION;

EID: 84883316505     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.129437     Document Type: Article

References (74)

1. Akhmanova, A., Stehbens, S. J. and Yap, A. S. (2009). Touch, grasp, deliver and control: functional cross-talk between microtubules and cell adhesions. Traffic 10, 268-274.
2. Asada, M., Irie, K., Morimoto, K., Yamada, A., Ikeda, W., Takeuchi, M. and Takai, Y. (2003). ADIP, a novel Afadin- and alpha-actinin-binding protein localized at cellcell adherens junctions. J. Biol. Chem. 278, 4103-4111.
3. Bazellières, E., Massey-Harroche, D., Barthélémy-Requin, M., Richard, F., Arsanto, J. P. and Le Bivic, A. (2012). Apico-basal elongation requires a drebrin-E-EB3 complex in columnar human epithelial cells. J. Cell Sci. 125, 919-931.
4. Bazzoni, G. and Dejana, E. (2004). Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol. Rev. 84, 869-901.
5. Beaudoin, G. M., 3rd, Schofield, C. M., Nuwal, T., Zang, K., Ullian, E. M., Huang, B. and Reichardt, L. F. (2012). Afadin, a Ras/Rap effector that controls cadherin function, promotes spine and excitatory synapse density in the hippocampus. J. Neurosci. 32, 99-110.
6. Biou, V., Brinkhaus, H., Malenka, R. C. and Matus, A. (2008). Interactions between drebrin and Ras regulate dendritic spine plasticity. Eur. J. Neurosci. 27, 2847-2859.
7. Brakeman, P. R., Liu, K. D., Shimizu, K., Takai, Y. and Mostov, K. E. (2009). Nectin proteins are expressed at early stages of nephrogenesis and play a role in renal epithelial cell morphogenesis. Am. J. Physiol. 296, F564-F574.
8. Brown, W. J., Constantinescu, E. and Farquhar, M. G. (1984). Redistribution of mannose-6-phosphate receptors induced by tunicamycin and chloroquine. J. Cell Biol. 99, 320-326.
9. Butkevich, E., Hülsmann, S., Wenzel, D., Shirao, T., Duden, R. and Majoul, I. (2004). Drebrin is a novel connexin-43 binding partner that links gap junctions to the submembrane cytoskeleton. Curr. Biol. 14, 650-658.
10. Cereijido, M., Robbins, E. S., Dolan, W. J., Rotunno, C. A. and Sabatini, D. D. (1978). Polarized monolayers formed by epithelial cells on a permeable and translucent support. J. Cell Biol. 77, 853-880.
11. Chen, P. M., Gombart, Z. J. and Chen, J. W. (2011). Chloroquine treatment of ARPE-19 cells leads to lysosome dilation and intracellular lipid accumulation: possible implications of lysosomal dysfunction in macular degeneration. Cell. Biosci. 1, 10.
12. Cheng, X. T., Hayashi, K. and Shirao, T. (2000). Non-muscle myosin IIB-like immunoreactivity is present at the drebrin-binding cytoskeleton in neurons. Neurosci. Res. 36, 167-173.
13. Dai, G., Kaazempur-Mofrad, M. R., Natarajan, S., Zhang, Y., Vaughn, S., Blackman, B. R., Kamm, R. D., García-Cardeña, G. and Gimbrone, M. A., Jr (2004). Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and -resistant regions of human vasculature. Proc. Natl. Acad. Sci. USA 101, 14871-14876.
14. Dejana, E. (2004). Endothelial cell-cell junctions: happy together. Nat. Rev. Mol. Cell Biol. 5, 261-270.
15. Dejana, E. and Giampietro, C. (2012). Vascular endothelial-cadherin and vascular stability. Curr. Opin. Hematol. 19, 218-223.
16. dela Paz, N. G., Walshe, T. E., Leach, L. L., Saint-Geniez, M. and D'Amore, P. A. (2012). Role of shear-stress-induced VEGF expression in endothelial cell survival. J. Cell Sci. 125, 831-843.
17. Duffy, H. S., Delmar, M. and Spray, D. C. (2002). Formation of the gap junction nexus: binding partners for connexins. J. Physiol. Paris 96, 243-249.
18. Fabre-Lafay, S., Monville, F., Garrido-Urbani, S., Berruyer-Pouyet, C., Ginestier, C., Reymond, N., Finetti, P., Sauvan, R., Adélaïde, J., Geneix, J. et al. (2007). Nectin-4 is a new histological and serological tumor associated marker for breast cancer. BMC Cancer 7, 73.
19. Fournier, G., Cabaud, O., Josselin, E., Chaix, A., Adélaïde, J., Isnardon, D., Restouin, A., Castellano, R., Dubreuil, P., Chaffanet, M. et al. (2011). Loss of AF6/afadin, a marker of poor outcome in breast cancer, induces cell migration, invasiveness and tumor growth. Oncogene 30, 3862-3874.
20. Geraldo, S., Khanzada, U. K., Parsons, M., Chilton, J. K. and Gordon-Weeks, P. R. (2008). Targeting of the F-actin-binding protein drebrin by the microtubule plus-tip protein EB3 is required for neuritogenesis. Nat. Cell Biol. 10, 1181-1189.
21. Giepmans, B. N. (2004). Gap junctions and connexin-interacting proteins. Cardiovasc. Res. 62, 233-245.
22. Grintsevich, E. E., Galkin, V. E., Orlova, A., Ytterberg, A. J., Mikati, M. M., Kudryashov, D. S., Loo, J. A., Egelman, E. H. and Reisler, E. (2010). Mapping of drebrin binding site on F-actin. J. Mol. Biol. 398, 542-554.
23. Harigaya, Y., Shoji, M., Shirao, T. and Hirai, S. (1996). Disappearance of actinbinding protein, drebrin, from hippocampal synapses in Alzheimer's disease. J. Neurosci. Res. 43, 87-92.
24. Hartsock, A. and Nelson, W. J. (2008). Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim. Biophys. Acta 1778, 660-669.
25. Hayashi, K. and Shirao, T. (1999). Change in the shape of dendritic spines caused by overexpression of drebrin in cultured cortical neurons. J. Neurosci. 19, 3918-3925.
26. Hayashi, K., Ishikawa, R., Kawai-Hirai, R., Takagi, T., Taketomi, A. and Shirao, T. (1999). Domain analysis of the actin-binding and actin-remodeling activities of drebrin. Exp. Cell Res. 253, 673-680.
27. Ikeda, W., Nakanishi, H., Miyoshi, J., Mandai, K., Ishizaki, H., Tanaka, M., Togawa, A., Takahashi, K., Nishioka, H., Yoshida, H. et al. (1999). Afadin: A key molecule essential for structural organization of cell-cell junctions of polarized epithelia during embryogenesis. J. Cell Biol. 146, 1117-1132.
28. Ilan, N., Cheung, L., Pinter, E. and Madri, J. A. (2000). Platelet-endothelial cell adhesion molecule-1 (CD31), a scaffolding molecule for selected catenin family members whose binding is mediated by different tyrosine and serine/threonine phosphorylation. J. Biol. Chem. 275, 21435-21443.
29. Ishikawa, R., Hayashi, K., Shirao, T., Xue, Y., Takagi, T., Sasaki, Y. and Kohama, K. (1994). Drebrin, a development-associated brain protein from rat embryo, causes the dissociation of tropomyosin from actin filaments. J. Biol. Chem. 269, 29928-29933.
30. Ishikawa, R., Katoh, K., Takahashi, A., Xie, C., Oseki, K., Watanabe, M., Igarashi, M., Nakamura, A. and Kohama, K. (2007). Drebrin attenuates the interaction between actin and myosin-V. Biochem. Biophys. Res. Commun. 359, 398-401.
31. Kessels, M. M. and Qualmann, B. (2002). Syndapins integrate N-WASP in receptor-mediated endocytosis. EMBO J. 21, 6083-6094.
32. Kopp, P., Lammers, R., Aepfelbacher, M., Woehlke, G., Rudel, T., Machuy, N., Steffen, W. and Linder, S. (2006). The kinesin KIF1C and microtubule plus ends regulate podosome dynamics in macrophages. Mol. Biol. Cell 17, 2811-2823.
33. Kovacs, E. M., Ali, R. G., McCormack, A. J. and Yap, A. S. (2002). E-cadherin homophilic ligation directly signals through Rac and phosphatidylinositol 3-kinase to regulate adhesive contacts. J. Biol. Chem. 277, 6708-6718.
34. Kubota, H., Ishikawa, R., Ohki, T., Ishizuka, J., Mikhailenko, S. V. and Ishiwata, S. (2010). Modulation of the mechano-chemical properties of myosin V by drebrin-E. Biochem. Biophys. Res. Commun. 400, 643-648.
35. Kurita, S., Ogita, H. and Takai, Y. (2011). Cooperative role of nectin-nectin and nectin-afadin interactions in formation of nectin-based cell-cell adhesion. J. Biol. Chem. 286, 36297-36303.
36. Lampugnani, M. G. and Dejana, E. (1997). Interendothelial junctions: structure, signalling and functional roles. Curr. Opin. Cell Biol. 9, 674-682.
37. Ley, K., Laudanna, C., Cybulsky, M. I. and Nourshargh, S. (2007). Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7, 678-689.
38. Lim, S. T., Chang, A., Giuliano, R. E. and Federoff, H. J. (2012). Ectodomain shedding of nectin-1 regulates the maintenance of dendritic spine density. J. Neurochem. 120, 741-751.
39. Linder, S., Nelson, D., Weiss, M. and Aepfelbacher, M. (1999). Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc. Natl. Acad. Sci. USA 96, 9648-9653.
40. Lopez, M., Aoubala, M., Jordier, F., Isnardon, D., Gomez, S. and Dubreuil, P. (1998). The human poliovirus receptor related 2 protein is a new hematopoietic/endothelial homophilic adhesion molecule. Blood 92, 4602-4611.
41. Mammoto, A., Sasaki, T., Asakura, T., Hotta, I., Imamura, H., Takahashi, K., Matsuura, Y., Shirao, T. and Takai, Y. (1998). Interactions of drebrin and gephyrin with profilin. Biochem. Biophys. Res. Commun. 243, 86-89.
42. Mandai, K., Nakanishi, H., Satoh, A., Obaishi, H., Wada, M., Nishioka, H., Itoh, M., Mizoguchi, A., Aoki, T., Fujimoto, T. et al. (1997). Afadin: A novel actin filament-binding protein with one PDZ domain localized at cadherin-based cell-to-cell adherens junction. J. Cell Biol. 139, 517-528.
43. Meyrelles, S. S., Peotta, V. A., Pereira, T. M. and Vasquez, E. C. (2011). Endothelial dysfunction in the apolipoprotein E-deficient mouse: insights into the influence of diet, gender and aging. Lipids Health Dis. 10, 211.
44. Ooshio, T., Irie, K., Morimoto, K., Fukuhara, A., Imai, T. and Takai, Y. (2004). Involvement of LMO7 in the association of two cell-cell adhesion molecules, nectin and E-cadherin, through afadin and alpha-actinin in epithelial cells. J. Biol. Chem. 279, 31365-31373.
45. Ooshio, T., Kobayashi, R., Ikeda, W., Miyata, M., Fukumoto, Y., Matsuzawa, N., Ogita, H. and Takai, Y. (2010). Involvement of the interaction of afadin with ZO-1 in the formation of tight junctions in Madin-Darby canine kidney cells. J. Biol. Chem. 285, 5003-5012.
46. Osiak, A. E., Zenner, G. and Linder, S. (2005). Subconfluent endothelial cells form podosomes downstream of cytokine and RhoGTPase signaling. Exp. Cell Res. 307, 342-353.
47. Peitsch, W. K., Grund, C., Kuhn, C., Schnölzer, M., Spring, H., Schmelz, M. and Franke, W. W. (1999). Drebrin is a widespread actin-associating protein enriched at junctional plaques, defining a specific microfilament anchorage system in polar epithelial cells. Eur. J. Cell Biol. 78, 767-778.
48. Peitsch, W. K., Hofmann, I., Prätzel, S., Grund, C., Kuhn, C., Moll, I., Langbein, L. and Franke, W. W. (2001). Drebrin particles: components in the ensemble of proteins regulating actin dynamics of lamellipodia and filopodia. Eur. J. Cell Biol. 80, 567-579.
49. Peitsch, W. K., Hofmann, I., Endlich, N., Prätzel, S., Kuhn, C., Spring, H., Gröne, H. J., Kriz, W. and Franke, W. W. (2003). Cell biological and biochemical characterization of drebrin complexes in mesangial cells and podocytes of renal glomeruli. J. Am. Soc. Nephrol. 14, 1452-1463.
50. Peitsch, W. K., Hofmann, I., Bulkescher, J., Hergt, M., Spring, H., Bleyl, U., Goerdt, S. and Franke, W. W. (2005). Drebrin, an actin-binding, cell-type characteristic protein: induction and localization in epithelial skin tumors and cultured keratinocytes. J. Invest. Dermatol. 125, 761-774.
51. Pokutta, S., Drees, F., Takai, Y., Nelson, W. J. and Weis, W. I. (2002). Biochemical and structural definition of the l-afadin- and actin-binding sites of alpha-catenin. J. Biol. Chem. 277, 18868-18874.
52. Poukkula, M., Kremneva, E., Serlachius, M. and Lappalainen, P. (2011). Actin-depolymerizing factor homology domain: a conserved fold performing diverse roles in cytoskeletal dynamics. Cytoskeleton 68, 471-490.
53. Prochnow, N. and Dermietzel, R. (2008). Connexons and cell adhesion: a romantic phase. Histochem. Cell Biol. 130, 71-77.
54. Reymond, N., Borg, J. P., Lecocq, E., Adelaide, J., Campadelli-Fiume, G., Dubreuil, P. and Lopez, M. (2000). Human nectin3/PRR3: a novel member of the PVR/PRR/nectin family that interacts with afadin. Gene 255, 347-355.
55. Riedl, J., Crevenna, A. H., Kessenbrock, K., Yu, J. H., Neukirchen, D., Bista, M., Bradke, F., Jenne, D., Holak, T. A., Werb, Z. et al. (2008). Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5, 605-607.
56. Sasaki, Y., Hayashi, K., Shirao, T., Ishikawa, R. and Kohama, K. (1996). Inhibition by drebrin of the actin-bundling activity of brain fascin, a protein localized in filopodia of growth cones. J. Neurochem. 66, 980-988.
57. Sawyer, J. K., Choi, W., Jung, K. C., He, L., Harris, N. J. and Peifer, M. (2011). A contractile actomyosin network linked to adherens junctions by Canoe/afadin helps drive convergent extension. Mol. Biol. Cell 22, 2491-2508.
58. Schneeberger, E. E. and Lynch, R. D. (2004). The tight junction: a multifunctional complex. Am. J. Physiol. 286, C1213-C1228
59. Sharma, S., Grintsevich, E. E., Phillips, M. L., Reisler, E. and Gimzewski, J. K. (2011). Atomic force microscopy reveals drebrin induced remodeling of f-actin with subnanometer resolution. Nano Lett. 11, 825-827.
60. Stehbens, S. J., Paterson, A. D., Crampton, M. S., Shewan, A. M., Ferguson, C., Akhmanova, A., Parton, R. G. and Yap, A. S. (2006). Dynamic microtubules regulate the local concentration of E-cadherin at cell-cell contacts. J. Cell Sci. 119, 1801-1811.
61. Taguchi, K., Ishiuchi, T. and Takeichi, M. (2011). Mechanosensitive EPLIN-dependent remodeling of adherens junctions regulates epithelial reshaping. J. Cell Biol. 194, 643-656.
62. Takahashi, K., Nakanishi, H., Miyahara, M., Mandai, K., Satoh, K., Satoh, A., Nishioka, H., Aoki, J., Nomoto, A., Mizoguchi, A. et al. (1999). Nectin/PRR: an immunoglobulin-like cell adhesion molecule recruited to cadherin-based adherens junctions through interaction with Afadin, a PDZ domain-containing protein. J. Cell Biol. 145, 539-549.
63. Takai, Y. and Nakanishi, H. (2003). Nectin and afadin: novel organizers of intercellular junctions. J. Cell Sci. 116, 17-27.
64. Takai, Y., Ikeda, W., Ogita, H. and Rikitake, Y. (2008a). The immunoglobulin-like cell adhesion molecule nectin and its associated protein afadin. Annu. Rev. Cell Dev. Biol. 24, 309-342.
65. Takai, Y., Miyoshi, J., Ikeda, W. and Ogita, H. (2008b). Nectins and nectin-like molecules: roles in contact inhibition of cell movement and proliferation. Nat. Rev. Mol. Cell Biol. 9, 603-615.
66. Vaid, K. S., Guttman, J. A., Babyak, N., Deng, W., McNiven, M. A., Mochizuki, N., Finlay, B. B. and Vogl, A. W. (2007). The role of dynamin 3 in the testis. J. Cell. Physiol. 210, 644-654.
67. van Zijl, P. C., Hua, J. and Lu, H. (2012). The BOLD post-stimulus undershoot, one of the most debated issues in fMRI. Neuroimage 62, 1092-1102.
68. Vestweber, D. (2007). Adhesion and signaling molecules controlling the transmigration of leukocytes through endothelium. Immunol. Rev. 218, 178-196.
69. Vestweber, D., Winderlich, M., Cagna, G. and Nottebaum, A. F. (2009). Cell adhesion dynamics at endothelial junctions: VE-cadherin as a major player. Trends Cell Biol. 19, 8-15.
70. Wibo, M. and Poole, B. (1974). Protein degradation in cultured cells. II. The uptake of chloroquine by rat fibroblasts and the inhibition of cellular protein degradation and cathepsin B1. J. Cell Biol. 63, 430-440.
71. Woodfin, A., Voisin, M. B., Beyrau, M., Colom, B., Caille, D., Diapouli, F. M., Nash, G. B., Chavakis, T., Albelda, S. M., Rainger, G. E. et al. (2011). The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo. Nat. Immunol. 12, 761-769.
72. Xu, W. and Stamnes, M. (2006). The actin-depolymerizing factor homology and charged/helical domains of drebrin and mAbp1 direct membrane binding and localization via distinct interactions with actin. J. Biol. Chem. 281, 11826-11833.
73. Yuan, S. Y., Shen, Q., Rigor, R. R. and Wu, M. H. (2012). Neutrophil transmigration, focal adhesion kinase and endothelial barrier function. Microvasc. Res. 83, 82-88.
74. Zhao, L., Ma, Q. L., Calon, F., Harris-White, M. E., Yang, F., Lim, G. P., Morihara, T., Ubeda, O. J., Ambegaokar, S., Hansen, J. E. et al. (2006). Role of p21-activated kinase pathway defects in the cognitive deficits of Alzheimer disease. Nat. Neurosci. 9, 234-242.