Vangl2 regulates E-Cadherin in epithelial cells

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Nagaoka, Tadahiro ^a   Inutsuka, Ayumu ^b   Begum, Khadiza ^c   Musabbir Bin Hafiz, Khandakar ^c   Kishi, Masashi ^a  

^a NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

^c BANGLADESH AGRICULTURAL UNIVERSITY   (Bangladesh)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; DYNAMIN; LTAP PROTEIN, MOUSE; NERVE PROTEIN; RAB PROTEIN;

ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; CELL ADHESION; CELL COUNT; CELL JUNCTION; CELL MEMBRANE; CELL POLARITY; CYTOLOGY; ENDOCYTOSIS; EPITHELIUM CELL; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; KIDNEY; METABOLISM; MOUSE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ADHERENS JUNCTIONS; ANIMALS; CADHERINS; CELL ADHESION; CELL COUNT; CELL MEMBRANE; CELL POLARITY; DYNAMINS; EMBRYO, MAMMALIAN; ENDOCYTOSIS; EPITHELIAL CELLS; FIBROBLASTS; GENE EXPRESSION REGULATION; KIDNEY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; PROTEIN TRANSPORT; RAB5 GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 84938904224     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep06940     Document Type: Article

References (54)

1. Simons, M. &Mlodzik, M. Planar cell polarity signaling: from fly development to human disease. Annu Rev Genet 42, 517-540, doi:10.1146/annurev.genet.42.110807.091432 (2008).
2. Vladar, E. K., Antic, D. & Axelrod, J. D. Planar cell polarity signaling: the developing cell's compass. Cold Spring Harb Perspect Biol 1, a002964, doi:10.1101/cshperspect.a002964 (2009).
3. Wallingford, J. B. Planar cell polarity and the developmental control of cell behavior in vertebrate embryos. Annu Rev Cell Dev Biol 28, 627-653, doi:10.1146/annurev-cellbio-092910-154208 (2012).
4. Montcouquiol, M. et al. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423, 173-177, doi:10.1038/nature01618 (2003).
5. Devenport, D. & Fuchs, E. Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles. Nat Cell Biol 10, 1257-1268, doi:10.1038/ncb1784 (2008).
6. Wallingford, J. B. et al. Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405, 81-85, doi:10.1038/35011077 (2000).
7. Bertet, C., Sulak, L. & Lecuit, T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429, 667-671, doi:10.1038/nature02590 (2004).
8. Walck-Shannon, E. & Hardin, J. Cell intercalation from top to bottom. Nat Rev Mol Cell Biol 15, 34-48, doi:10.1038/nrm3723 (2014).
9. Usui, T. et al. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98, 585-595 (1999).
10. Strutt, H.,Warrington, S. J. & Strutt, D. Dynamics of core planar polarity protein turnover and stable assembly into discrete membrane subdomains. Dev Cell 20, 511-525, doi:10.1016/j.devcel.2011.03.018 (2011).
11. Nishimura, T., Honda, H. & Takeichi, M. Planar cell polarity links axes of spatial dynamics in neural-tube closure. Cell 149, 1084-1097, doi:10.1016/j.cell.2012.04.021 (2012).
12. Rauzi, M., Lenne, P. F. & Lecuit, T. Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468, 1110-1114, doi:10.1038/nature09566 (2010).
13. Zallen, J. A. & Blankenship, J. T. Multicellular dynamics during epithelial elongation. Semin Cell Dev Biol 19, 263-270, doi:10.1016/j.semcdb.2008.01.005 (2008).
14. Nagaoka, T. et al. The Wnt/Planar Cell Polarity Pathway Component Vangl2 Induces Synapse Formation through Direct Control of N-Cadherin. Cell Rep 6, 916-927, doi:10.1016/j.celrep.2014.01.044 (2014).
15. Togashi, H. et al. Cadherin regulates dendritic spine morphogenesis. Neuron 35, 77-89 (2002).
16. Uchida, N.,Honjo, Y., Johnson, K. R.,Wheelock, M. J.&Takeichi, M. The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones. J Cell Biol 135, 767-779 (1996).
17. Yagi, T. & Takeichi, M. Cadherin superfamily genes: functions, genomic organization, and neurologic diversity. Genes Dev 14, 1169-1180 (2000).
18. Suyama, K., Shapiro, I., Guttman,M. & Hazan, R. B. A signaling pathway leading to metastasis is controlled by N-cadherin and the FGF receptor. Cancer Cell 2, 301-314 (2002).
19. Ulrich, F. et al. Wnt11 functions in gastrulation by controlling cell cohesion through Rab5c and E-cadherin. Dev Cell 9, 555-564, doi:10.1016/j.devcel.2005.08.011 (2005).
20. Warrington, S. J., Strutt, H. & Strutt, D. The Frizzled-dependent planar polarity pathway locally promotes E-cadherin turnover via recruitment of RhoGEF2. Development 140, 1045-1054, doi:10.1242/dev.088724 (2013).
21. Karner, C. M. et al. Wnt9b signaling regulates planar cell polarity and kidney tubule morphogenesis. Nat Genet 41, 793-799, doi:10.1038/ng.400 (2009).
22. Lienkamp, S. S. et al. Vertebrate kidney tubules elongate using a planar cell polarity-dependent, rosette-based mechanism of convergent extension. Nat Genet 44, 1382-1387, doi:10.1038/ng.2452 (2012).
23. Odintsova, E., Sugiura, T. & Berditchevski, F. Attenuation of EGF receptor signaling by a metastasis suppressor, the tetraspanin CD82/KAI-1. Curr Biol 10, 1009-1012 (2000).
24. Jenny, A., Darken, R. S., Wilson, P. A. &Mlodzik, M. Prickle and Strabismus form a functional complex to generate a correct axis during planar cell polarity signaling. EMBO J 22, 4409-4420, doi:10.1093/emboj/cdg424 (2003).
25. Wolff, T. & Rubin, G. M. Strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. Development 125, 1149-1159 (1998).
26. Ozawa, M., Baribault, H. & Kemler, R. The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J 8, 1711-1717 (1989).
27. Stappert, J. & Kemler, R. A short core region of E-cadherin is essential for catenin binding and is highly phosphorylated. Cell Adhes Commun 2, 319-327 (1994).
28. McEwen, A. E., Maher, M. T., Mo, R.&Gottardi, C. J. E-cadherin phosphorylation occurs during its biosynthesis to promote its cell surface stability and adhesion. Mol Biol Cell 25, 2365-2374, doi:10.1091/mbc.E14-01-0690 (2014).
29. Suzuki, M. et al. Defective membrane expression of the Na(1)-HCO(3)(-) cotransporter NBCe1 is associated with familial migraine. Proc Natl Acad Sci U S A 107, 15963-15968, doi:10.1073/pnas.1008705107 (2010).
30. Le, T. L., Yap, A. S. & Stow, J. L. Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics. J Cell Biol 146, 219-232 (1999).
31. Bohdanowicz, M., Balkin, D. M., De Camilli, P. & Grinstein, S. Recruitment of OCRL and Inpp5B to phagosomes by Rab5 and APPL1 depletes phosphoinositides and attenuates Akt signaling. Mol Biol Cell 23, 176-187, doi:10.1091/mbc.E11-06-0489 (2012).
32. Lee, E. & De Camilli, P. Dynamin at actin tails. Proc Natl Acad Sci U S A 99, 161-166, doi:10.1073/pnas.012607799 (2002).
33. Yates, L. L. et al. The planar cell polarity gene Vangl2 is required for mammalian kidney-branching morphogenesis and glomerular maturation. Hum Mol Genet 19, 4663-4676, doi:10.1093/hmg/ddq397 (2010).
34. Fukunaga, Y. et al. Defining the roles of beta-catenin and plakoglobin in cell-cell adhesion: isolation of beta-catenin/plakoglobin-deficient F9 cells. Cell Struct Funct 30, 25-34 (2005).
35. Kibar, Z. et al. Ltap, amammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nat Genet 28, 251-255, doi:10.1038/90081 (2001).
36. Gravel, M., Iliescu, A., Horth, C., Apuzzo, S. & Gros, P. Molecular and cellular mechanisms underlying neural tube defects in the loop-tail mutant mouse. Biochemistry 49, 3445-3455, doi:10.1021/bi902180m (2010).
37. Guyot, M. C. et al. A novel hypomorphic Looptail allele at the planar cell polarity Vangl2 gene. Dev Dyn : an official publication of the American Association of Anatomists 240, 839-849, doi:10.1002/dvdy.22577 (2011).
38. Yin, H., Copley, C. O., Goodrich, L. V. & Deans, M. R. Comparison of phenotypes between different vangl2 mutants demonstrates dominant effects of the Looptail mutation during hair cell development. PloS One 7, e31988, doi:10.1371/journal.pone.0031988 (2012).
39. Willingham, M. C. Fluorescence labeling of surface antigens of attached or suspended tissue-culture cells. Methods Mol Biol 588, 143-151, doi:10.1007/978- 1-59745-324-0-17 (2010).
40. Vestweber, D. & Kemler, R. Identification of a putative cell adhesion domain of uvomorulin. EMBO J 4, 3393-3398 (1985).
41. Lindqvist, M. et al. Vang-like protein 2 and Rac1 interact to regulate adherens junctions. J Cell Sci 123, 472-483, doi:10.1242/jcs.048074 (2010).
42. Classen, A. K., Anderson, K. I., Marois, E. & Eaton, S. Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. Dev Cell 9, 805-817, doi:10.1016/j.devcel.2005.10.016 (2005).
43. Shafer, B., Onishi, K., Lo, C., Colakoglu, G. & Zou, Y. Vangl2 promotes Wnt/planar cell polarity-like signaling by antagonizing Dvl1-mediated feedback inhibition in growth cone guidance. Dev Cell 20, 177-191, doi:10.1016/j.devcel.2011.01.002 (2011).
44. Williams, B. B. et al. VANGL2 regulates membrane trafficking of MMP14 to control cell polarity and migration. J Cell Sci 125, 2141-2147, doi:10.1242/jcs.097964 (2012).
45. Jessen, J. R. et al. Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat Cell Biol 4, 610-615, doi:10.1038/ncb828 (2002).
46. Babayeva, S. et al. Planar cell polarity pathway regulates nephrin endocytosis in developing podocytes. J Biol Chem 288, 24035-24048, doi:10.1074/jbc.M113.452904 (2013).
47. Babayeva, S., Zilber, Y. & Torban, E. Planar cell polarity pathway regulates actin rearrangement, cell shape, motility, and nephrin distribution in podocytes. Am J Physiol Renal Physiol 300, F549-560, doi:10.1152/ajprenal.00566.2009 (2011).
48. Dohn, M. R.,Mundell, N. A., Sawyer, L. M., Dunlap, J. A. & Jessen, J. R. Planar cell polarity proteins differentially regulate extracellular matrix organization and assembly during zebrafish gastrulation. Dev Biol 383, 39-51, doi:10.1016/j.ydbio.2013.08.027 (2013).
49. Benzing, T., Simons, M. & Walz, G. Wnt signaling in polycystic kidney disease. J Am Soc Nephrol : JASN 18, 1389-1398, doi:10.1681/ASN.2006121355 (2007).
50. Matis, M. & Axelrod, J. D. Regulation of PCP by the Fat signaling pathway. Genes Dev 27, 2207-2220, doi:10.1101/gad.228098.113 (2013).
51. McNeill, H. Planar cell polarity and the kidney. J Am Soc Nephrol : JASN 20, 2104-2111, doi:10.1681/ASN.2008111173 (2009).
52. Clark, H. F. et al. Dachsous encodes a member of the cadherin superfamily that controls imaginal disc morphogenesis in Drosophila. Genes Dev 9, 1530-1542 (1995).
53. Kim, J. B. et al. N-Cadherin extracellular repeat 4 mediates epithelial to mesenchymal transition and increased motility. J Cell Biol 151, 1193-1206 (2000).
54. Smith, L. J. & Stein, K. F. Axial elongation in the mouse and its retardation in homozygous looptail mice. J Embryol Exp Morphol 10, 73-87 (1962).