Building epithelial architecture: insights from three-dimensional culture models (original) (raw)

References

  1. Hogan, B. & Kolodzeij, P. A. Molecular mechanisms of tubulogenesis. Nature Rev. Genetics 3, 513–523 (2002).
    Article CAS Google Scholar
  2. Metzger, R. J. & Krasnow, M. A. Genetic control of branching morphogenesis. Science 284, 1635–1639 (1999).
    Article CAS Google Scholar
  3. Vainio, S. & Lin, Y. Coordinating early kidney development: lessons from gene targeting. Nature Rev. Genetics 3, 529–539 (2002).
    Article Google Scholar
  4. Mostov, K. E., Verges, M. & Altschuler, Y. Membrane traffic in polarized epithelial cells. Curr. Opin. Cell Biol. 12, 483–490 (2000).
    Article CAS Google Scholar
  5. Drubin, D. G. & Nelson, W. J. Origins of cell polarity. Cell 84, 335–344 (1996).
    Article CAS Google Scholar
  6. Hagios, C., Lochter, A. & Bissell, M. J. Tissue architecture: the ultimate regulator of epithelial function? Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 857–870 (1998).
    Article CAS Google Scholar
  7. Walpita, D. & Hay, E. Studying actin-dependent processes in tissue culture. Nature Rev. Mol. Cell Biol. 3, 137–141 (2002).
    Article CAS Google Scholar
  8. Montesano, R., Matsumoto, K., Nakamura, T. & Orci, L. Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor. Cell 67, 901–908 (1991).
    Article CAS Google Scholar
  9. Montesano, R., Schaller, G. & Orci, L. Induction of epithelial tubular morphogenesis in vitro by fibroblast-derived soluble factors. Cell 66, 697–711 (1991).
    Article CAS Google Scholar
  10. Saelman, E. U., Keely, P. J. & Santoro, S. A. Loss of MDCK cellα2β1 integrin expression results in reduced cyst formation, failure of hepatocyte growth factor/scatter factor-induced branching morphogenesis, and increased apoptosis. J. Cell Sci. 108, 3531–3540 (1995).
    CAS Google Scholar
  11. Ervasti, J. M. & Campbell, K. P. A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol. 122, 809–823 (1993).
    Article CAS Google Scholar
  12. Yamada, K. M. & Geiger, B. Molecular interactions in cell adhesion complexes. Curr. Opin. Cell Biol. 9, 76–85 (1997).
    Article CAS Google Scholar
  13. Troxell, M. L., Loftus, D. J., Nelson, W. J. & Marrs, J. A. Mutant cadherin affects epithelial morphogenesis and invasion, but not transformation. J. Cell Sci. 114, 1237–1246 (2001).
    CAS Google Scholar
  14. Zuk, A. & Matlin, K. S. Apical β1 integrin in polarized MDCK cells mediates tubulocyst formation in response to type I collagen overlay. J. Cell Sci. 109, 1875–1889 (1996).
    CAS Google Scholar
  15. Ojakian, G. K. & Schwimmer, R. Regulation of epithelial cell surface polarity reversal by β1 integrins. J. Cell Sci. 107, 561–576 (1994).
    CAS Google Scholar
  16. Schwimmer, R. & Ojakian, G. K. The α2β1 integrin regulates collagen-mediated MDCK epithelial membrane remodeling and tubule formation. J. Cell Sci. 108, 2487–2498 (1995).
    CAS Google Scholar
  17. Guo, S. & Kemphues, K. J. par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 81, 611–620 (1995).
    Article CAS Google Scholar
  18. Chambard, M., Verrier, B., Gabrion, J. & Mauchamp, J. Polarity reversal of inside–out thyroid follicles cultured within collagen gel: reexpression of specific functions. Biol. Cell 51, 315–325 (1984).
    Article CAS Google Scholar
  19. Wang, A. Z., Ojakian, G. K. & Nelson, W. J. Steps in the morphogenesis of a polarized epithelium. I. Uncoupling the roles of cell–cell and cell–substratum contact in establishing plasma membrane polarity in multicellular epithelial (MDCK) cysts. J. Cell Sci. 95, 137–151 (1990).
    Google Scholar
  20. Wang, A. Z., Ojakian, G. K. & Nelson, W. J. Steps in the morphogenesis of a polarized epithelium. II. Disassembly and assembly of plasma membrane domains during reversal of epithelial cell polarity in multicellular epithelial (MDCK) cysts. J. Cell Sci. 95, 153–165 (1990).
    Google Scholar
  21. Wang, A. Z., Wang, J. C., Ojakian, G. K. & Nelson, W. J. Determinants of apical membrane formation and distribution in multicellular epithelial MDCK cysts. Am. J. Physiol. 267, C473–C481 (1994).
    Article CAS Google Scholar
  22. Yeaman, C., Grindstaff, K. K. & Nelson, W. J. New perspectives on mechanisms involved in generating epithelial cell polarity. Physiol. Rev. 79, 73–98 (1999).
    Article CAS Google Scholar
  23. Ojakian, G. K., Nelson, W. J. & Beck, K. A. Mechanisms for de novo biogenesis of an apical membrane compartment in groups of simple epithelial cells surrounded by extracellular matrix. J. Cell Sci. 110, 2781–2794 (1997).
    CAS Google Scholar
  24. Yap, A. S., Stevenson, B. R., Armstrong, J. W., Keast, J. R. & Manley, S. W. Thyroid epithelial morphogenesis in vitro: a role for bumetanide-sensitive Cl− secretion during follicular lumen development. Exp. Cell Res. 213, 319–326 (1994).
    Article CAS Google Scholar
  25. Vega-Salas, D. E., Salas, P. J. & Rodriguez-Boulan, E. Exocytosis of vacuolar apical compartment (VAC): a cell–cell contact controlled mechanism for the establishment of the apical plasma membrane domain in epithelial cells. J. Cell Biol. 107, 1717–1728 (1988).
    Article CAS Google Scholar
  26. Folkman, J. & Haudenschild, C. Angiogenesis in vitro. Nature 288, 551–556 (1980).
    Article CAS Google Scholar
  27. Davis, G. E. & Bayless, K. K. An integrin and Rho GTPase-dependent pinocytic vacuole mechanism controls capillary lumen formation in collagen and fibrin matrices. Microcirculation (in the press).
  28. Colony, P. C. & Neutra, M. R. Epithelial differentiation in the fetal rat colon. I. Plasma membrane phosphatase activities. Dev. Biol. 97, 349–363 (1983).
    Article CAS Google Scholar
  29. Gilbert, T. & Rodriguez-Boulan, E. Induction of vacuolar apical compartments in the Caco-2 intestinal epithelial cell line. J. Cell Sci. 100, 451–458 (1991).
    Google Scholar
  30. Yap, A. S., Stevenson, B. R., Keast, J. R. & Manley, S. W. Cadherin-mediated adhesion and apical membrane assembly define distinct steps during thyroid epithelial polarization and lumen formation. Endocrinology 136, 4672–4680 (1995).
    Article CAS Google Scholar
  31. Coucouvanis, E. & Martin, G. R. Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo. Cell 83, 279–287 (1995).
    Article CAS Google Scholar
  32. Lin, H. H., Yang, T. P., Jiang, S. T., Yang, H. Y. & Tang, M. J. Bcl-2 overexpression prevents apoptosis-induced Madin-Darby canine kidney simple epithelial cyst formation. Kidney Int. 55, 168–178 (1999).
    Article CAS Google Scholar
  33. Blatchford, D. R. et al. Influence of microenvironment on mammary epithelial cell survival in primary culture. J. Cell Physiol. 181, 304–311 (1999).
    Article CAS Google Scholar
  34. Muthuswamy, S. K., Li, D., Lelievre, S., Bissell, M. J. & Brugge, J. S. ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nature Cell Biol. 3, 785–792 (2001).
    Article CAS Google Scholar
  35. Klein, G., Langegger, M., Timpl, R. & Ekblom, P. Role of laminin A chain in the development of epithelial cell polarity. Cell 55, 331–341 (1988).
    Article CAS Google Scholar
  36. Schuger, L., Yurchenco, P., Relan, N. K. & Yang, Y. Laminin fragment E4 inhibition studies: basement membrane assembly and embryonic lung epithelial cell polarization requires laminin polymerization. Int. J. Dev. Biol. 42, 217–220 (1998).
    CAS Google Scholar
  37. Weaver, V. M. et al. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J. Cell Biol. 137, 231–245 (1997).
    Article CAS Google Scholar
  38. O'Brien, L. E. et al. Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nature Cell Biol. 3, 831–838 (2001).
    Article CAS Google Scholar
  39. Gudjonsson, T. et al. Normal and tumor-derived myoepithelial cells differ in their ability to interact with luminal breast epithelial cells for polarity and basement membrane deposition. J. Cell Sci. 115, 39–50 (2002).
    CAS Google Scholar
  40. Birchmeier, C. & Gherardi, E. Developmental roles of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol. 8, 404–410 (1998).
    Article CAS Google Scholar
  41. Schmidt, C. et al. Scatter factor/hepatocyte growth factor is essential for liver development. Nature 373, 699–702 (1995).
    Article CAS Google Scholar
  42. Uehara, Y. et al. Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 373, 702–705 (1995).
    Article CAS Google Scholar
  43. Sonnenberg, E., Meyer, D., Weidner, K. M. & Birchmeier, C. Scatter factor/hepatocyte growth factor and its receptor, the c-met tyrosine kinase, can mediate a signal exchange between mesenchyme and epithelia during mouse development. J. Cell Biol. 123, 223–235 (1993).
    Article CAS Google Scholar
  44. Woolf, A. S. et al. Roles of hepatocyte growth factor/scatter factor and the met receptor in the early development of the metanephros. J. Cell Biol. 128, 171–184 (1995).
    Article CAS Google Scholar
  45. Santos, O. F. et al. Involvement of hepatocyte growth factor in kidney development. Dev. Biol. 163, 525–529 (1994).
    Article CAS Google Scholar
  46. Van Adelsberg, J. et al. Activation of hepatocyte growth factor (HGF) by endogenous HGF activator is required for metanephric kidney morphogenesis in vitro. J. Biol. Chem. 276, 15099–15106 (2001).
    Article CAS Google Scholar
  47. Sakurai, H., Barros, E. J., Tsukamoto, T., Barasch, J. & Nigam, S. K. An in vitro tubulogenesis system using cell lines derived from the embryonic kidney shows dependence on multiple soluble growth factors. Proc. Natl Acad. Sci. USA 94, 6279–6284 (1997).
    Article CAS Google Scholar
  48. Pollack, A. L., Runyan, R. B. & Mostov, K. E. Morphogenetic mechanisms of epithelial tubulogenesis: MDCK cell polarity is transiently rearranged without loss of cell–cell contact during scatter factor/hepatocyte growth factor-induced tubulogenesis. Dev. Biol. 204, 64–79 (1998).
    Article CAS Google Scholar
  49. Savagner, P. Leaving the neighborhood: molecular mechanisms involved during epithelial–mesenchymal transition. Bioessays 23, 912–923 (2001).
    Article CAS Google Scholar
  50. Nathke, I. S., Adams, C. L., Polakis, P., Sellin, J. H. & Nelson, W. J. The adenomatous polyposis coli tumor suppressor protein localizes to plasma membrane sites involved in active cell migration. J. Cell Biol. 134, 165–179 (1996).
    Article CAS Google Scholar
  51. Pollack, A. L., Barth, A. I. M., Altschuler, Y., Nelson, W. J. & Mostov, K. E. Dynamics of β-catenin interactions with APC protein regulate epithelial tubulogenesis. J. Cell Biol. 137, 1651–1662 (1997).
    Article CAS Google Scholar
  52. Gautreau, A., Louvard, D. & Arpin, M. Morphogenic effects of ezrin require a phosphorylation-induced transition from oligomers to monomers at the plasma membrane. J. Cell Biol. 150, 193–203 (2000).
    Article CAS Google Scholar
  53. TerBush, D. R., Maurice, T., Roth, D. & Novick, P. The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 15, 6483–6494 (1996).
    Article CAS Google Scholar
  54. Grindstaff, K. K. et al. Sec6/8 complex is recruited to cell–cell contacts and specifies transport vesicle delivery to the basal–lateral membrane in epithelial cells. Cell 93, 731–740 (1998).
    Article CAS Google Scholar
  55. Lipschutz, J. H. et al. Exocyst is involved in cystogenesis and tubulogenesis and acts by modulating synthesis and delivery of basolateral plasma membrane and secretory proteins. Mol. Biol. Cell 11, 4259–4275 (2000).
    Article CAS Google Scholar
  56. Kadono, Y. et al. Membrane type 1-matrix metalloproteinase is involved in the formation of hepatocyte growth factor/scatter factor-induced branching tubules in Madin–Darby Canine Kidney epithelial cells. Biochem. Biophys. Res. Commun. 251, 681–687 (1998).
    Article CAS Google Scholar
  57. Hotary, K., Allen, E., Punturieri, A., Yana, I. & Weiss, S. J. Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2, and 3. J. Cell Biol. 149, 1309–1323 (2000).
    Article CAS Google Scholar
  58. Reinsch, S. & Karsenti, E. Orientation of spindle axis and distribution of plasma membrane proteins during cell division in polarized MDCKII cells. J. Cell Biol. 126, 1509–1526 (1994).
    Article CAS Google Scholar
  59. Kuchinke, U., Grawe, F. & Knust, E. Control of spindle orientation in Drosophila by the Par-3-related PDZ-domain protein Bazooka. Curr. Biol. 8, 1357–1365 (1998).
    Article CAS Google Scholar
  60. Lu, B., Roegiers, F., Jan, L. Y. & Jan, Y. N. Adherens junctions inhibit asymmetric division in the Drosophila epithelium. Nature 409, 522–525 (2001).
    Article CAS Google Scholar
  61. Petronczki, M. & Knoblich, J. A. DmPAR-6 directs epithelial polarity and asymmetric cell division of neuroblasts in Drosophila. Nature Cell Biol. 3, 43–49 (2001).
    CAS Google Scholar
  62. Kamei, T. et al. Coendocytosis of cadherin and c-Met coupled to disruption of cell–cell adhesion in MDCK cells—regulation by Rho, Rac and Rab small G proteins. Oncogene 18, 6776–6784 (1999).
    Article CAS Google Scholar

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