An Adaptor Molecule Afadin Regulates Lymphangiogenesis by Modulating RhoA Activity in the Developing Mouse Embryo

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Majima, Takashi ^a,d   Takeuchi, Keisuke ^b   Sano, Keigo ^c   Hirashima, Masanori ^c   Zankov, Dimitar P ^b   Tanaka Okamoto, Miki ^a   Ishizaki, Hiroyoshi ^a   Miyoshi, Jun ^a   Ogita, Hisakazu ^b  

^a OSAKA MEDICAL CENTER FOR CANCER AND CARDIOVASCULAR DISEASES   (Japan)

^b SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^c KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d OHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; AFADIN; F ACTIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; ACTIN BINDING PROTEIN;

ARTICLE; BLOOD VESSEL; CELL JUNCTION; CELL SHAPE; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPH VESSEL; LYMPHANGIOGENESIS; MICROVASCULATURE; MORPHOLOGY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REGULATORY MECHANISM; SKIN EDEMA; ANIMAL; CELL ADHESION; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; KNOCKOUT MOUSE; MAMMALIAN EMBRYO; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE; VASCULAR ENDOTHELIUM;

MUS;

ANIMALS; CELL ADHESION; CELL PROLIFERATION; CELLS, CULTURED; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; ENDOTHELIUM, VASCULAR; HUMANS; INTERCELLULAR JUNCTIONS; LYMPHANGIOGENESIS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; RHOA GTP-BINDING PROTEIN;

EID: 84879488758     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068134     Document Type: Article

References (47)

1. Farquhar MG, Palade GE, (1963) Junctional complexes in various epithelia. J Cell Biol 17: 375-412.
2. Takeichi M, (1988) The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development 102: 639-655.
3. Yagi T, Takeichi M, (2000) Cadherin superfamily genes: functions, genomic organization, and neurologic diversity. Genes Dev 14: 1169-1180.
4. Ogita H, Takai Y, (2008) Cross-talk among integrin, cadherin, and growth factor receptor: roles of nectin and nectin-like molecule. Int Rev Cytol 265: 1-54.
5. Mandai K, Nakanishi H, Satoh A, Obaishi H, Wada M, 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.
6. Takai Y, Miyoshi J, Ikeda W, Ogita H, (2008) Nectins and nectin-like molecules: roles in contact inhibition of cell movement and proliferation. Nat Rev Mol Cell Biol 9: 603-615.
7. Takai Y, Ikeda W, Ogita H, Rikitake Y, (2008) The Immunoglobulin-like Cell Adhesion Molecule Nectin and Its Associated Protein Afadin. Annu Rev Cell Dev Biol 24: 309-342.
8. Ooshio T, Kobayashi R, Ikeda W, Miyata M, Fukumoto Y, et al. (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.
9. Tsukita S, Furuse M, (1999) Occludin and claudins in tight-junction strands: leading or supporting players? Trends Cell Biol 9: 268-273.
10. Tsukita S, Furuse M, Itoh M, (2001) Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2: 285-293.
11. Fukumoto Y, Kurita S, Takai Y, Ogita H, (2011) Role of scaffold protein afadin dilute domain-interacting protein (ADIP) in platelet-derived growth factor-induced cell movement by activating Rac protein through Vav2 protein. J Biol Chem 286: 43537-43548.
12. Kanzaki N, Ogita H, Komura H, Ozaki M, Sakamoto Y, et al. (2008) Involvement of the nectin-afadin complex in PDGF-induced cell survival. J Cell Sci 121: 2008-2017.
13. Miyata M, Ogita H, Komura H, Nakata S, Okamoto R, et al. (2009) Localization of nectin-free afadin at the leading edge and its involvement in directional cell movement induced by platelet-derived growth factor. J Cell Sci 122: 4319-4329.
14. Komura H, Ogita H, Ikeda W, Mizoguchi A, Miyoshi J, et al. (2008) Establishment of cell polarity by afadin during the formation of embryoid bodies. Genes Cells 13: 79-90.
15. Ikeda W, Nakanishi H, Miyoshi J, Mandai K, Ishizaki 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.
16. Zhadanov AB, Provance DW Jr, Speer CA, Coffin JD, Goss D, et al. (1999) Absence of the tight junctional protein AF-6 disrupts epithelial cell-cell junctions and cell polarity during mouse development. Curr Biol 9: 880-888.
17. Birukova AA, Fu P, Wu T, Dubrovskyi O, Sarich N, et al. (2012) Afadin controls p120-catenin-ZO-1 interactions leading to endothelial barrier enhancement by oxidized phospholipids. J Cell Physiol 227: 1883-1890.
18. Tawa H, Rikitake Y, Takahashi M, Amano H, Miyata M, et al. (2010) Role of Afadin in Vascular Endothelial Growth Factor- and Sphingosine 1-Phosphate-Induced Angiogenesis. Circ Res 106: 1731-1742.
19. Majima T, Ogita H, Yamada T, Amano H, Togashi H, et al. (2009) Involvement of afadin in the formation and remodeling of synapses in the hippocampus. Biochem Biophys Res Commun 385: 539-544.
20. Hirashima M, Sano K, Morisada T, Murakami K, Rossant J, et al. (2008) Lymphatic vessel assembly is impaired in Aspp1-deficient mouse embryos. Dev Biol 316: 149-159.
21. Miyata M, Rikitake Y, Takahashi M, Nagamatsu Y, Yamauchi Y, et al. (2009) Regulation by afadin of cyclical activation and inactivation of Rap1, Rac1, and RhoA small G proteins at leading edges of moving NIH3T3 cells. J Biol Chem 284: 24595-24609.
22. Lampugnani MG, Resnati M, Raiteri M, Pigott R, Pisacane A, et al. (1992) A novel endothelial-specific membrane protein is a marker of cell-cell contacts. J Cell Biol 118: 1511-1522.
23. Baluk P, McDonald DM, (2008) Markers for microscopic imaging of lymphangiogenesis and angiogenesis. Ann NY Acad Sci 1131: 1-12.
24. Severs NJ, Rothery S, Dupont E, Coppen SR, Yeh HI, et al. (2001) Immunocytochemical analysis of connexin expression in the healthy and diseased cardiovascular system. Microsc Res Tech 52: 301-322.
25. Wang HU, Chen ZF, Anderson DJ, (1998) Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93: 741-753.
26. Wigle JT, Harvey N, Detmar M, Lagutina I, Grosveld G, et al. (2002) An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J 21: 1505-1513.
27. Hall A, (1998) Rho GTPases and the actin cytoskeleton. Science 279: 509-514.
28. Gorovoy M, Han J, Pan H, Welch E, Neamu R, et al. (2009) LIM kinase 1 promotes endothelial barrier disruption and neutrophil infiltration in mouse lungs. Circ Res 105: 549-556.
29. Ogita H, Kunimoto S, Kamioka Y, Sawa H, Masuda M, et al. (2003) EphA4-mediated Rho activation via Vsm-RhoGEF expressed specifically in vascular smooth muscle cells. Circ Res 93: 23-31.
30. Sabin FR, (1902) On the origin of the lymphatic system from the veins and the development of the lymph hearts and thoracic duct in the pig. Am J Anat 1: 367-389.
31. Wigle JT, Oliver G, (1999) Prox1 function is required for the development of the murine lymphatic system. Cell 98: 769-778.
32. Adams RH, Alitalo K, (2007) Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 8: 464-478.
33. Hosking B, Makinen T, (2007) Lymphatic vasculature: a molecular perspective. Bioessays 29: 1192-1202.
34. Hammerling B, Grund C, Boda-Heggemann J, Moll R, Franke WW, (2006) The complexus adhaerens of mammalian lymphatic endothelia revisited: a junction even more complex than hitherto thought. Cell Tissue Res 324: 55-67.
35. Cattelino A, Liebner S, Gallini R, Zanetti A, Balconi G, et al. (2003) The conditional inactivation of the beta-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility. J Cell Biol 162: 1111-1122.
36. Oas RG, Xiao K, Summers S, Wittich KB, Chiasson CM, et al. (2010) p120-Catenin is required for mouse vascular development. Circ Res 106: 941-951.
37. Hirashima M, Bernstein A, Stanford WL, Rossant J, (2004) Gene-trap expression screening to identify endothelial-specific genes. Blood 104: 711-718.
38. Lohela M, Bry M, Tammela T, Alitalo K, (2009) VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol 21: 154-165.
39. Karkkainen MJ, Haiko P, Sainio K, Partanen J, Taipale J, et al. (2004) Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol 5: 74-80.
40. Abtahian F, Guerriero A, Sebzda E, Lu MM, Zhou R, et al. (2003) Regulation of blood and lymphatic vascular separation by signaling proteins SLP-76 and Syk. Science 299: 247-251.
41. Kiefer F, Brumell J, Al-Alawi N, Latour S, Cheng A, et al. (1998) The Syk protein tyrosine kinase is essential for Fcgamma receptor signaling in macrophages and neutrophils. Mol Cell Biol 18: 4209-4220.
42. Sebzda E, Hibbard C, Sweeney S, Abtahian F, Bezman N, et al. (2006) Syk and Slp-76 mutant mice reveal a cell-autonomous hematopoietic cell contribution to vascular development. Dev Cell 11: 349-361.
43. Honda T, Sakisaka T, Yamada T, Kumazawa N, Hoshino T, et al. (2006) Involvement of nectins in the formation of puncta adherentia junctions and the mossy fiber trajectory in the mouse hippocampus. Mol Cell Neurosci 31: 315-325.
44. Ozaki-Kuroda K, Nakanishi H, Ohta H, Tanaka H, Kurihara H, et al. (2002) Nectin couples cell-cell adhesion and the actin scaffold at heterotypic testicular junctions. Curr Biol 12: 1145-1150.
45. Wakamatsu K, Ogita H, Okabe N, Irie K, Tanaka-Okamoto M, et al. (2007) Up-regulation of loricrin expression by cell adhesion molecule nectin-1 through Rap1-ERK signaling in keratinocytes. J Biol Chem 282: 18173-18181.
46. Noda K, Zhang J, Fukuhara S, Kunimoto S, Yoshimura M, et al. (2010) Vascular endothelial-cadherin stabilizes at cell-cell junctions by anchoring to circumferential actin bundles through alpha- and beta-catenins in cyclic AMP-Epac-Rap1 signal-activated endothelial cells. Mol Biol Cell 21: 584-596.
47. Waschke J, Curry FE, Adamson RH, Drenckhahn D, (2005) Regulation of actin dynamics is critical for endothelial barrier functions. Am J Physiol Heart Circ Physiol 288: H1296-305.