The in vivo function of mammalian cell and tissue polarity regulators - How to shape and maintain the epidermal barrier

Journal of Cell Science

Volumn 125, Issue 15, 2012, Pages 3501-3510

  Niessen, Michaela T ^a,b   Iden, Sandra ^c   Niessen, Carien M ^a,c  

^a UNIVERSITY OF COLOGNE   (Germany)

^b Institute for Genetics   (Germany)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Adhesion; Barrier function; Cancer; Cytoskeleton; Epidermis; Hair follicle; Polarity; Signaling

Indexed keywords

ALPHA CATENIN; BETA1 INTEGRIN; EZRIN; HERMES ANTIGEN; MERLIN; MOESIN; MYOSIN ADENOSINE TRIPHOSPHATASE; PROTEIN KINASE C LAMBDA; PROTEIN KINASE C ZETA; RAC PROTEIN; RADIXIN; UVOMORULIN;

CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CELL DIVISION; CELL ELONGATION; CELL FATE; CELL FUNCTION; CELL JUNCTION; CELL LINEAGE; CELL MIGRATION; CELL POLARITY; CELL RENEWAL; CELL SHAPE; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; EPIDERMIS; GENE OVEREXPRESSION; HAIR FOLLICLE; HOMEOSTASIS; IN VITRO STUDY; IN VIVO STUDY; MAMMAL CELL; NONHUMAN; NOTE; PHYSICAL PARAMETERS; POLARIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SKIN CANCER; SKIN EPITHELIUM; TIGHT JUNCTION; TISSUE POLARITY; TISSUE REGENERATION; TISSUE STRUCTURE;

ANIMALS; CELL DIFFERENTIATION; CELL POLARITY; CYTOSKELETON; EPIDERMIS; HUMANS; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 84869108085     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.092890     Document Type: Note

References (90)

1. Aranda, V., Haire, T., Nolan, M. E., Calarco, J. P., Rosenberg, A. Z., Fawcett, J. P., Pawson, T. and Muthuswamy, S. K. (2006). Par6-aPKC uncouples ErbB2 induced disruption of polarized epithelial organization from proliferation control. Nat. Cell Biol. 8, 1235-1245.
2. Assémat, E., Bazelliéres, E., Pallesi-Pocachard, E., Le Bivic, A. and Massey-Harroche, D. (2008). Polarity complex proteins. Biochim. Biophys. Acta 1778, 614-630.
3. Bayly, R. and Axelrod, J. D. (2011). Pointing in the right direction: new developments in the field of planar cell polarity. Nat. Rev. Genet. 12, 385-391.
4. Bilder, D. (2004). Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors. Genes Dev. 18, 1909-1925.
5. Blanpain, C. and Fuchs, E. (2009). Epidermal homeostasis: a balancing act of stem cells in the skin. Nat. Rev. Mol. Cell Biol. 10, 207-217.
6. Bulgakova, N. A. and Knust, E. (2009). The Crumbs complex: from epithelial-cell polarity to retinal degeneration. J. Cell Sci. 122, 2587-2596.
7. Bultje, R. S., Castaneda-Castellanos, D. R., Jan, L. Y., Jan, Y. N., Kriegstein, A. R. and Shi, S. H. (2009). Mammalian Par3 regulates progenitor cell asymmetric division via notch signaling in the developing neocortex. Neuron 63, 189-202.
8. Caddy, J., Wilanowski, T., Darido, C., Dworkin, S., Ting, S. B., Zhao, Q., Rank, G., Auden, A., Srivastava, S., Papenfuss, T. A. et al. (2010). Epidermal wound repair is regulated by the planar cell polarity signaling pathway. Dev. Cell 19, 138-147.
9. Clayton, E., Doupé, D. P., Klein, A. M., Winton, D. J., Simons, B. D. and Jones, P. H. (2007). A single type of progenitor cell maintains normal epidermis. Nature 446, 185-189.
10. Dard, N., Le, T., Maro, B. and Louvet-Vallée, S. (2009). Inactivation of aPKCl reveals a context dependent allocation of cell lineages in preimplantation mouse embryos. PLoS ONE 4, e7117.
11. Devenport, D. and Fuchs, E. (2008). Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles. Nat. Cell Biol. 10, 1257-1268.
12. Devenport, D., Oristian, D., Heller, E. and Fuchs, E. (2011). Mitotic internalization of planar cell polarity proteins preserves tissue polarity. Nat. Cell Biol. 13, 893-902.
13. Dow, L. E., Kauffman, J. S., Caddy, J., Zarbalis, K., Peterson, A. S., Jane, S. M., Russell, S. M. and Humbert, P. O. (2007). The tumour-suppressor Scribble dictates cell polarity during directed epithelial migration: regulation of Rho GTPase recruitment to the leading edge. Oncogene 26, 2272-2282.
14. Durgan, J., Kaji, N., Jin, D. and Hall, A. (2011). Par6B and atypical PKC regulate mitotic spindle orientation during epithelial morphogenesis. J. Biol. Chem. 286, 12461-12474.
15. Farkas, L. M. and Huttner, W. B. (2008). The cell biology of neural stem and progenitor cells and its significance for their proliferation versus differentiation during mammalian brain development. Curr. Opin. Cell Biol. 20, 707-715.
16. Feigin, M. E. and Muthuswamy, S. K. (2009). Polarity proteins regulate mammalian cell-cell junctions and cancer pathogenesis. Curr. Opin. Cell Biol. 21, 694-700.
17. Fields, A. P., Frederick, L. A. and Regala, R. P. (2007). Targeting the oncogenic protein kinase Ci signalling pathway for the treatment of cancer. Biochem. Soc. Trans. 35, 996-1000.
18. Frances, D. and Niemann, C. (2012). Stem cell dynamics in sebaceous gland morphogenesis in mouse skin. Dev. Biol. 363, 138-146.
19. Gardiol, D., Kühne, C., Glaunsinger, B., Lee, S. S., Javier, R. and Banks, L. (1999). Oncogenic human papillomavirus E6 proteins target the discs large tumour suppressor for proteasome-mediated degradation. Oncogene 18, 5487-5496.
20. Gladden, A. B., Hebert, A. M., Schneeberger, E. E. and McClatchey, A. I. (2010). The NF2 tumor suppressor, Merlin, regulates epidermal development through the establishment of a junctional polarity complex. Dev. Cell 19, 727-739.
21. Goldstein, B. and Macara, I. G. (2007). The PAR proteins: fundamental players in animal cell polarization. Dev. Cell 13, 609-622.
22. Greco, V., Chen, T., Rendl, M., Schober, M., Pasolli, H. A., Stokes, N., Dela Cruz-Racelis, J. and Fuchs, E. (2009). A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 4, 155-169.
23. Guo, N., Hawkins, C. and Nathans, J. (2004). Frizzled6 controls hair patterning in mice. Proc. Natl. Acad. Sci. USA 101, 9277-9281.
24. Gurumurthy, S., Hezel, A. F., Sahin, E., Berger, J. H., Bosenberg, M. W. and Bardeesy, N. (2008). LKB1 deficiency sensitizes mice to carcinogen-induced tumorigenesis. Cancer Res. 68, 55-63.
25. Hao, Y., Du, Q., Chen, X., Zheng, Z., Balsbaugh, J. L., Maitra, S., Shabanowitz, J., Hunt, D. F. and Macara, I. G. (2010). Par3 controls epithelial spindle orientation by aPKC-mediated phosphorylation of apical Pins. Curr. Biol. 20, 1809-1818.
26. Hawkins, E. D. and Russell, S. M. (2008). Upsides and downsides to polarity and asymmetric cell division in leukemia. Oncogene 27, 7003-7017.
27. Helfrich, I., Schmitz, A., Zigrino, P., Michels, C., Haase, I., le Bivic, A., Leitges, M. and Niessen, C. M. (2007). Role of aPKC isoforms and their binding partners Par3 and Par6 in epidermal barrier formation. J. Invest. Dermatol. 127, 782-791.
28. Hsu, Y. C., Pasolli, H. A. and Fuchs, E. (2011). Dynamics between stem cells, niche, and progeny in the hair follicle. Cell 144, 92-105.
29. Huang, L. and Muthuswamy, S. K. (2010). Polarity protein alterations in carcinoma: a focus on emerging roles for polarity regulators. Curr. Opin. Genet. Dev. 20, 41-50.
30. Humbert, P. O., Grzeschik, N. A., Brumby, A. M., Galea, R., Elsum, I. and Richardson, H. E. (2008). Control of tumourigenesis by the Scribble/Dlg/Lgl polarity module. Oncogene 27, 6888-6907.
31. Iden, S. and Collard, J. G. (2008). Crosstalk between small GTPases and polarity proteins in cell polarization. Nat. Rev. Mol. Cell Biol. 9, 846-859.
32. Imai, F., Hirai, S., Akimoto, K., Koyama, H., Miyata, T., Ogawa, M., Noguchi, S., Sasaoka, T., Noda, T. and Ohno, S. (2006). Inactivation of aPKCl results in the loss of adherens junctions in neuroepithelial cells without affecting neurogenesis in mouse neocortex. Development 133, 1735-1744.
33. Jansen, M., Ten Klooster, J. P., Offerhaus, G. J. and Clevers, H. (2009). LKB1 and AMPK family signaling: the intimate link between cell polarity and energy metabolism. Physiol. Rev. 89, 777-798.
34. Januschke, J. and Gonzalez, C. (2008). Drosophila asymmetric division, polarity and cancer. Oncogene 27, 6994-7002.
35. Kemphues, K. J., Priess, J. R., Morton, D. G. and Cheng, N. S. (1988). Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52, 311-320.
36. Kirschner, N., Haftek, M., Niessen, C. M., Behne, M. J., Furuse, M., Moll, I. and Brandner, J. M. (2011). CD44 regulates tight-junction assembly and barrier function. J. Invest. Dermatol. 131, 932-943.
37. Klein, T. J. and Mlodzik, M. (2005). Planar cell polarization: an emerging model points in the right direction. Annu. Rev. Cell Dev. Biol. 21, 155-176.
38. Klezovitch, O., Fernandez, T. E., Tapscott, S. J. and Vasioukhin, V. (2004). Loss of cell polarity causes severe brain dysplasia in Lgl1 knockout mice. Genes Dev. 18, 559-571.
39. Knoblich, J. A. (2008). Mechanisms of asymmetric stem cell division. Cell 132, 583-597.
40. Knoblich, J. A. (2010). Asymmetric cell division: recent developments and their implications for tumour biology. Nat. Rev. Mol. Cell Biol. 11, 849-860.
41. Koster, M. I. (2009). Making an epidermis. Ann. N. Y. Acad. Sci. 1170, 7-10.
42. Lamprecht, J. (1990). Symmetric and asymmetric cell division in rat corneal epithelium. Cell Tissue Kinet. 23, 203-216.
43. Lechler, T. and Fuchs, E. (2005). Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 437, 275-280.
44. Lee, C. Y., Robinson, K. J. and Doe, C. Q. (2006). Lgl, Pins and aPKC regulate neuroblast self-renewal versus differentiation. Nature 439, 594-598.
45. Lee, M. and Vasioukhin, V. (2008). Cell polarity and cancer-cell and tissue polarity as a non-canonical tumor suppressor. J. Cell Sci. 121, 1141-1150.
46. Li, R. and Bowerman, B. (2010). Symmetry breaking in biology. Cold Spring Harb. Perspect. Biol. 2, a003475.
47. Luxenburg, C., Pasolli, H. A., Williams, S. E. and Fuchs, E. (2011). Developmental roles for Srf, cortical cytoskeleton and cell shape in epidermal spindle orientation. Nat. Cell Biol. 13, 203-214.
48. Martin-Belmonte, F. and Mostov, K. (2008). Regulation of cell polarity during epithelial morphogenesis. Curr. Opin. Cell Biol. 20, 227-234.
49. McCaffrey, L. M. and Macara, I. G. (2009). Widely conserved signaling pathways in the establishment of cell polarity. Cold Spring Harb. Perspect. Biol. 1, a001370.
50. McNeill, H. (2010). Planar cell polarity: keeping hairs straight is not so simple. Cold Spring Harb. Perspect. Biol. 2, a003376.
51. Mertens, A. E., Rygiel, T. P., Olivo, C., van der Kammen, R. and Collard, J. G. (2005). The Rac activator Tiam1 controls tight junction biogenesis in keratinocytes through binding to and activation of the Par polarity complex. J. Cell Biol. 170, 1029-1037.
52. Montcouquiol, M., Rachel, R. A., Lanford, P. J., Copeland, N. G., Jenkins, N. A. and Kelley, M. W. (2003). Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423, 173-177.
53. Murdoch, J. N., Henderson, D. J., Doudney, K., Gaston-Massuet, C., Phillips, H. M., Paternotte, C., Arkell, R., Stanier, P. and Copp, A. J. (2003). Disruption of scribble (Scrb1) causes severe neural tube defects in the circletail mouse. Hum. Mol. Genet. 12, 87-98.
54. Murray, N. R., Weems, J., Braun, U., Leitges, M. and Fields, A. P. (2009). Protein kinase C bII and PKCi/l: collaborating partners in colon cancer promotion and progression. Cancer Res. 69, 656-662.
55. Nakagawa, S. and Huibregtse, J. M. (2000). Human scribble (Vartul) is targeted for ubiquitin-mediated degradation by the high-risk papillomavirus E6 proteins and the E6AP ubiquitin-protein ligase. Mol. Cell. Biol. 20, 8244-8253.
56. Nelson, W. J. (2003). Adaptation of core mechanisms to generate cell polarity. Nature 422, 766-774.
57. Nelson, W. J. (2009). Remodeling epithelial cell organization: transitions between frontrear and apical-basal polarity. Cold Spring Harb. Perspect. Biol. 1, a000513.
58. Niessen, C. M. and Gottardi, C. J. (2008). Molecular components of the adherens junction. Biochim. Biophys. Acta 1778, 562-571.
59. Nolan, M. E., Aranda, V., Lee, S., Lakshmi, B., Basu, S., Allred, D. C. and Muthuswamy, S. K. (2008). The polarity protein Par6 induces cell proliferation and is overexpressed in breast cancer. Cancer Res. 68, 8201-8209.
60. Pearson, C. G. and Bloom, K. (2004). Dynamic microtubules lead the way for spindle positioning. Nat. Rev. Mol. Cell Biol. 5, 481-492.
61. Pearson, H. B., Perez-Mancera, P. A., Dow, L. E., Ryan, A., Tennstedt, P., Bogani, D., Elsum, I., Greenfield, A., Tuveson, D. A., Simon, R. et al. (2011). SCRIB expression is deregulated in human prostate cancer, and its deficiency in mice promotes prostate neoplasia. J. Clin. Invest. 121, 4257-4267.
62. Pegtel, D. M., Ellenbroek, S. I., Mertens, A. E., van der Kammen, R. A., de Rooij, J. and Collard, J. G. (2007). The Par-Tiam1 complex controls persistent migration by stabilizing microtubule-dependent front-rear polarity. Curr. Biol. 17, 1623-1634.
63. Perez-Losada, J. and Balmain, A. (2003). Stem-cell hierarchy in skin cancer. Nat. Rev. Cancer 3, 434-443.
64. Petersson, M., Brylka, H., Kraus, A., John, S., Rappl, G., Schettina, P. and Niemann, C. (2011). TCF/Lef1 activity controls establishment of diverse stem and progenitor cell compartments in mouse epidermis. EMBO J. 30, 3004-3018.
65. Poulson, N. D. and Lechler, T. (2010). Robust control of mitotic spindle orientation in the developing epidermis. J. Cell Biol. 191, 915-922.
66. Prehoda, K. E. (2009). Polarization of Drosophila neuroblasts during asymmetric division. Cold Spring Harb. Perspect. Biol. 1, a001388.
67. Ravni, A., Qu, Y., Goffinet, A. M. and Tissir, F. (2009). Planar cell polarity cadherin Celsr1 regulates skin hair patterning in the mouse. J. Invest. Dermatol. 129, 2507-2509.
68. Ray, S. and Lechler, T. (2011). Regulation of asymmetric cell division in the epidermis. Cell Div. 6, 12.
69. Regala, R. P., Davis, R. K., Kunz, A., Khoor, A., Leitges, M. and Fields, A. P. (2009). Atypical protein kinase Ci is required for bronchioalveolar stem cell expansion and lung tumorigenesis. Cancer Res. 69, 7603-7611.
70. Roh, M. H. and Margolis, B. (2003). Composition and function of PDZ protein complexes during cell polarization. Am. J. Physiol. Renal Physiol. 285, F377-F387.
71. Saburi, S., Hester, I., Fischer, E., Pontoglio, M., Eremina, V., Gessler, M., Quaggin, S. E., Harrison, R., Mount, R. and McNeill, H. (2008). Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat. Genet. 40, 1010-1015.
72. Schneider, M. R., Schmidt-Ullrich, R. and Paus, R. (2009). The hair follicle as a dynamic miniorgan. Curr. Biol. 19, R132-R142.
73. Sengupta, A., Duran, A., Ishikawa, E., Florian, M. C., Dunn, S. K., Ficker, A. M., Leitges, M., Geiger, H., Diaz-Meco, M., Moscat, J. et al. (2011). Atypical protein kinase C (aPKCf and aPKCl) is dispensable for mammalian hematopoietic stem cell activity and blood formation. Proc. Natl. Acad. Sci. USA 108, 9957-9962.
74. Shin, K., Fogg, V. C. and Margolis, B. (2006). Tight junctions and cell polarity. Annu. Rev. Cell Dev. Biol. 22, 207-235.
75. Simons, M. and Mlodzik, M. (2008). Planar cell polarity signaling: from fly development to human disease. Annu. Rev. Genet. 42, 517-540.
76. Smart, I. H. (1970). Variation in the plane of cell cleavage during the process of stratification in the mouse epidermis. Br. J. Dermatol. 82, 276-282.
77. Sotiropoulou, P. A., Candi, A. and Blanpain, C. (2008). The majority of multipotent epidermal stem cells do not protect their genome by asymmetrical chromosome segregation. Stem Cells 26, 2964-2973.
78. St Johnston, D. and Ahringer, J. (2010). Cell polarity in eggs and epithelia: parallels and diversity. Cell 141, 757-774.
79. Suzuki, A. and Ohno, S. (2006). The PAR-aPKC system: lessons in polarity. J. Cell Sci. 119, 979-987.
80. Tscharntke, M., Pofahl, R., Chrostek-Grashoff, A., Smyth, N., Niessen, C., Niemann, C., Hartwig, B., Herzog, V., Klein, H. W., Krieg, T. et al. (2007). Impaired epidermal wound healing in vivo upon inhibition or deletion of Rac1. J. Cell Sci. 120, 1480-1490.
81. Tunggal, J. A., Helfrich, I., Schmitz, A., Schwarz, H., Günzel, D., Fromm, M., Kemler, R., Krieg, T. and Niessen, C. M. (2005). E-cadherin is essential for in vivo epidermal barrier function by regulating tight junctions. EMBO J. 24, 1146-1156.
82. van de Pavert, S. A., Kantardzhieva, A., Malysheva, A., Meuleman, J., Versteeg, I., Levelt, C., Klooster, J., Geiger, S., Seeliger, M. W., Rashbass, P. et al. (2004). Crumbs homologue 1 is required for maintenance of photoreceptor cell polarization and adhesion during light exposure. J. Cell Sci. 117, 4169-4177.
83. Waghmare, S. K., Bansal, R., Lee, J., Zhang, Y. V., McDermitt, D. J. and Tumbar, T. (2008). Quantitative proliferation dynamics and random chromosome segregation of hair follicle stem cells. EMBO J. 27, 1309-1320.
84. Wang, Y. and Nathans, J. (2007). Tissue/planar cell polarity in vertebrates: new insights and new questions. Development 134, 647-658.
85. Watt, F. M. and Jensen, K. B. (2009). Epidermal stem cell diversity and quiescence. EMBO Mol. Med. 1, 260-267.
86. Williams, S. E., Beronja, S., Pasolli, H. A. and Fuchs, E. (2011). Asymmetric cell divisions promote Notch-dependent epidermal differentiation. Nature 470, 353-358.
87. Wu, M., Smith, C. L., Hall, J. A., Lee, I., Luby-Phelps, K. and Tallquist, M. D. (2010). Epicardial spindle orientation controls cell entry into the myocardium. Dev. Cell 19, 114-125.
88. Zhang, Y. V., Cheong, J., Ciapurin, N., McDermitt, D. J. and Tumbar, T. (2009). Distinct self-renewal and differentiation phases in the niche of infrequently dividing hair follicle stem cells. Cell Stem Cell 5, 267-278.
89. Zhang, Y. V., White, B. S., Shalloway, D. I. and Tumbar, T. (2010). Stem cell dynamics in mouse hair follicles: a story from cell division counting and single cell lineage tracing. Cell Cycle 9, 1504-1510.
90. Zhong, W. and Chia, W. (2008). Neurogenesis and asymmetric cell division. Curr. Opin. Neurobiol. 18, 4-11.