Noncentrosomal microtubules and type II myosins potentiate epidermal cell adhesion and barrier formation

Journal of Cell Biology

Volumn 199, Issue 3, 2012, Pages 513-525

  Sumigray, Kaelyn D ^a,b   Foote, Henry P ^a   Lechler, Terry ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN II; MYOSIN IIA; MYOSIN IIB;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL CULTURE; CELL DIFFERENTIATION; CELL JUNCTION; CENTROSOME; CONTROLLED STUDY; EPIDERMIS CELL; KERATINOCYTE; MICROTUBULE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TIGHT JUNCTION;

ADHERENS JUNCTIONS; ANIMALS; BLOTTING, WESTERN; CELL ADHESION; CELL DIFFERENTIATION; CELLS, CULTURED; DESMOSOMES; EPIDERMIS; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOPRECIPITATION; KERATINOCYTES; MICE; MICROTUBULES; MYOSIN TYPE II; TIGHT JUNCTIONS;

EID: 84869145834     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201206143     Document Type: Article

References (39)

1. Cavey, M., and T. Lecuit. 2009. Molecular bases of cell-cell junctions stability and dynamics. Cold Spring Harb. Perspect. Biol. 1:a002998. http://dx.doi.org/10.1101/cshperspect.a002998
2. Dehmelt, L., and S. Halpain. 2005. The MAP2/Tau family of microtubule-associated proteins. Genome Biol. 6:204. http://dx.doi.org/10.1186/gb-2004-6-1-204
3. Delgehyr, N., J. Sillibourne, and M. Bornens. 2005. Microtubule nucleation and anchoring at the centrosome are independent processes linked by ninein function. J. Cell Sci. 118:1565-1575. http://dx.doi.org/10.1242/jcs.02302
4. Derry, W.B., L. Wilson, and M.A. Jordan. 1995. Substoichiometric binding of taxol suppresses microtubule dynamics. Biochemistry. 34:2203-2211. http://dx.doi.org/10.1021/bi00007a014
5. Fabre-Jonca, N., I. Viard, L.E. French, and D. Masson. 1999. Upregulation and redistribution of E-MAP-115 (epithelial microtubule-associated protein of 115 kDa) in terminally differentiating keratinocytes is coincident with the formation of intercellular contacts. J. Invest. Dermatol. 112:216-225. http://dx.doi.org/10.1046/j.1523-1747.1999.00500.x
6. Furuse, M., M. Hata, K. Furuse, Y. Yoshida, A. Haratake, Y. Sugitani, T. Noda, A. Kubo, and S. Tsukita. 2002. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J. Cell Biol. 156:1099-1111. http://dx.doi.org/10.1083/jcb.200110122
7. Gumbiner, B., B. Stevenson, and A. Grimaldi. 1988. The role of the cell adhesion molecule uvomorulin in the formation and maintenance of the epithelial junctional complex. J. Cell Biol. 107:1575-1587. http://dx.doi.org/10.1083/jcb.107.4.1575
8. Guo, J., Z. Yang, W. Song, Q. Chen, F. Wang, Q. Zhang, and X. Zhu. 2006. Nudel contributes to microtubule anchoring at the mother centriole and is involved in both dynein-dependent and -independent centrosomal protein assembly. Mol. Biol. Cell. 17:680-689. http://dx.doi.org/10.1091/mbc.E05-04-0360
9. Hardman, M.J., P. Sisi, D.N. Banbury, and C. Byrne. 1998. Patterned acquisition of skin barrier function during development. Development. 125:1541-1552.
10. Helfrich, I., A. Schmitz, P. Zigrino, C. Michels, I. Haase, A. le Bivic, M. Leitges, and C.M. Niessen. 2007. Role of aPKC isoforms and their binding partners Par3 and Par6 in epidermal barrier formation. J. Invest. Dermatol. 127:782-791. http://dx.doi.org/10.1038/sj.jid.5700621
11. Hopkins, A.M., S.V. Walsh, P. Verkade, P. Boquet, and A. Nusrat. 2003. Constitutive activation of Rho proteins by CNF-1 influences tight junction structure and epithelial barrier function. J. Cell Sci. 116:725-742. http://dx.doi.org/10.1242/jcs.00300
12. Ivanov, A.I., M. Bachar, B.A. Babbin, R.S. Adelstein, A. Nusrat, and C.A. Parkos. 2007. A unique role for nonmuscle myosin heavy chain IIA in regulation of epithelial apical junctions. PLoS ONE. 2:e658. http://dx.doi.org/10.1371/journal.pone.0000658
13. Kee, S.H., and P.M. Steinert. 2001. Microtubule disruption in keratinocytes induces cell-cell adhesion through activation of endogenous E-cadherin. Mol. Biol. Cell. 12:1983-1993.
14. le Duc, Q., Q. Shi, I. Blonk, A. Sonnenberg, N. Wang, D. Leckband, and J. de Rooij. 2010. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J. Cell Biol. 189:1107-1115. http://dx.doi.org/10.1083/jcb.201001149
15. Lechler, T., and E. Fuchs. 2007. Desmoplakin: an unexpected regulator of microtubule organization in the epidermis. J. Cell Biol. 176:147-154. http://dx.doi.org/10.1083/jcb.200609109
16. Ligon, L.A., and E.L. Holzbaur. 2007. Microtubules tethered at epithelial cell junctions by dynein facilitate efficient junction assembly. Traffic. 8:808-819. http://dx.doi.org/10.1111/j.1600-0854.2007.00574.x
17. Liu, Z., J.L. Tan, D.M. Cohen, M.T. Yang, N.J. Sniadecki, S.A. Ruiz, C.M. Nelson, and C.S. Chen. 2010. Mechanical tugging force regulates the sizeof cell-cell junctions. Proc. Natl. Acad. Sci. USA. 107:9944-9949. http://dx.doi.org/10.1073/pnas.0914547107
18. Ma, X., S.S. Jana, M.A. Conti, S. Kawamoto, W.C. Claycomb, and R.S. Adelstein. 2010. Ablation of nonmuscle myosin II-B and II-C reveals a role for nonmuscle myosin II in cardiac myocyte karyokinesis. Mol. Biol. Cell. 21:3952-3962. http://dx.doi.org/10.1091/mbc.E10-04-0293
19. Mattiuzzo, N.R., E. Toulza, N. Jonca, G. Serre, and M. Guerrin. 2011. A largescale multi-technique approach identifies forty-nine new players of keratinocyte terminal differentiation in human epidermis. Exp. Dermatol. 20:113-118. http://dx.doi.org/10.1111/j.1600-0625.2010.01188.x
20. Müsch, A. 2004. Microtubule organization and function in epithelial cells. Traffic. 5:1-9. http://dx.doi.org/10.1111/j.1600-0854.2003.00149.x
21. Orr, G.A., P. Verdier-Pinard, H. McDaid, and S.B. Horwitz. 2003. Mechanisms of Taxol resistance related to microtubules. Oncogene. 22:7280-7295. http://dx.doi.org/10.1038/sj.onc.1206934
22. Paradez, A., A. Wright, and D.W. Ehrhardt. 2006. Microtubule cortical array organization and plant cell morphogenesis. Curr. Opin. Plant Biol. 9:571-578. http://dx.doi.org/10.1016/j.pbi.2006.09.005
23. Patel, S., Z.F. Xi, E.Y. Seo, D. McGaughey, and J.A. Segre. 2006. Klf4 and corticosteroids activate an overlapping set of transcriptional targets to accelerate in utero epidermal barrier acquisition. Proc. Natl. Acad. Sci. USA. 103:18668-18673. http://dx.doi.org/10.1073/pnas.0608658103
24. Perez-Moreno, M., M.A. Davis, E. Wong, H.A. Pasolli, A.B. Reynolds, and E. Fuchs. 2006. p120-catenin mediates inflammatory responses in the skin. Cell. 124:631-644. http://dx.doi.org/10.1016/j.cell.2005.11.043
25. Pizon, V., F. Gerbal, C.C. Diaz, and E. Karsenti. 2005. Microtubule-dependent transport and organization of sarcomeric myosin during skeletal muscle differentiation. EMBO J. 24:3781-3792. http://dx.doi.org/10.1038/sj.emboj.7600842
26. Raymond, A.A., A. Gonzalez de Peredo, A. Stella, A. Ishida-Yamamoto, D. Bouyssie, G. Serre, B. Monsarrat, and M. Simon. 2008. Lamellar bodies of human epidermis: proteomics characterization by high throughput mass spectrometry and possible involvement of CLIP-170 in their trafficking/secretion. Mol. Cell. Proteomics. 7:2151-2175. http://dx.doi.org/10.1074/mcp.M700334-MCP200
27. Reipert, S., H. Kotisch, B. Wysoudil, and G. Wiche. 2008. Rapid microwave fixation of cell monolayers preserves microtubule-associated cell structures. J. Histochem. Cytochem. 56:697-709. http://dx.doi.org/10.1369/jhc.7A7370.2008
28. Shen, L., E.D. Black, E.D. Witkowski, W.I. Lencer, V. Guerriero, E.E. Schneeberger, and J.R. Turner. 2006. Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J. Cell Sci. 119:2095-2106. http://dx.doi.org/10.1242/jcs.02915
29. Shen, L., C.R. Weber, and J.R. Turner. 2008. The tight junction protein complex undergoes rapid and continuous molecular remodeling at steady state. J. Cell Biol. 181:683-695. http://dx.doi.org/10.1083/jcb.200711165
30. Smutny, M., H.L. Cox, J.M. Leerberg, E.M. Kovacs, M.A. Conti, C. Ferguson, N.A. Hamilton, R.G. Parton, R.S. Adelstein, and A.S. Yap. 2010. Myosin II isoforms identify distinct functional modules that support integrity of the epithelial zonula adherens. Nat. Cell Biol. 12:696-702. http://dx.doi.org/10.1038/ncb2072
31. Stehbens, S.J., A.D. Paterson, M.S. Crampton, A.M. Shewan, C. Ferguson, A. Akhmanova, R.G. Parton, and A.S. Yap. 2006. Dynamic microtubules regulate the local concentration of E-cadherin at cell-cell contacts. J. Cell Sci. 119:1801-1811. http://dx.doi.org/10.1242/jcs.02903
32. Straight, A.F., A. Cheung, J. Limouze, I. Chen, N.J. Westwood, J.R. Sellers, and T.J. Mitchison. 2003. Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science. 299:1743-1747. http://dx.doi.org/10.1126/science.1081412
33. Sumigray, K.D., H. Chen, and T. Lechler. 2011. Lis1 is essential for cortical microtubule organization and desmosome stability in the epidermis. J. Cell Biol. 194:631-642. http://dx.doi.org/10.1083/jcb.201104009
34. Taguchi, K., T. Ishiuchi, and M. Takeichi. 2011. Mechanosensitive EPLINdependent remodeling of adherens junctions regulates epithelial reshaping. J. Cell Biol. 194:643-656. http://dx.doi.org/10.1083/jcb.201104124
35. Tinkle, C.L., H.A. Pasolli, N. Stokes, and E. Fuchs. 2008. New insights into cadherin function in epidermal sheet formation and maintenance of tissue integrity. Proc. Natl. Acad. Sci. USA. 105:15405-15410. http://dx.doi.org/10.1073/pnas.0807374105
36. Tunggal, J.A., I. Helfrich, A. Schmitz, H. Schwarz, D. Günzel, M. Fromm, R. Kemler, T. Krieg, and C.M. Niessen. 2005. E-cadherin is essential for in vivo epidermal barrier function by regulating tight junctions. EMBO J. 24:1146-1156. http://dx.doi.org/10.1038/sj.emboj.7600605
37. Walsh, S.V., A.M. Hopkins, J. Chen, S. Narumiya, C.A. Parkos, and A. Nusrat. 2001. Rho kinase regulates tight junction function and is necessary for tight junction assembly in polarized intestinal epithelia. Gastroenterology. 121:566-579. http://dx.doi.org/10.1053/gast.2001.27060
38. Yonemura, S., Y. Wada, T. Watanabe, A. Nagafuchi, and M. Shibata. 2010. alpha-Catenin as a tension transducer that induces adherens junction development. Nat. Cell Biol. 12:533-542. http://dx.doi.org/10.1038/ncb2055
39. Yu, D., A.M. Marchiando, C.R. Weber, D.R. Raleigh, Y. Wang, L. Shen, and J.R. Turner. 2010. MLCK-dependent exchange and actin binding region-dependent anchoring of ZO-1 regulate tight junction barrier function. Proc. Natl. Acad. Sci. USA. 107:8237-8241. http://dx.doi.org/10.1073/pnas.0908869107