Hepatocyte growth factor switches orientation of polarity and mode of movement during morphogenesis of multicellular epithelial structures

Molecular Biology of the Cell

Volumn 14, Issue 2, 2003, Pages 748-763

  Yu, Wei ^a,b   O'Brien, Lucy E ^a,b   Wang, Fei ^b   Bourne, Henry ^a,b   Mostov, Keith E ^a,b   Zegers, Mirjam M P ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; RHO KINASE; SCATTER FACTOR;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; CELL COUNT; CELL DIVISION; CELL MOTILITY; CELL POLARITY; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIUM; EPITHELIUM CELL; GOLGI COMPLEX; MICROTUBULE; MITOSIS SPINDLE; MONOLAYER CULTURE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACTINS; ANIMALS; BLOTTING, WESTERN; CELL DIVISION; CELL LINE; CELL MOVEMENT; CELLS, CULTURED; CYTOSKELETON; DOGS; EPITHELIAL CELLS; GREEN FLUORESCENT PROTEINS; HEPATOCYTE GROWTH FACTOR; IMAGE PROCESSING, COMPUTER-ASSISTED; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MICROTUBULES; MITOMYCIN; PROTEIN-SERINE-THREONINE KINASES; TIME FACTORS; TRANSFECTION; TUBULIN;

ANIMALIA;

EID: 0037328574     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-06-0350     Document Type: Article

References (69)

1. Adams, R.J. (1996). Metaphase spindles rotate in the neuroepithelium of rat cerebral cortex. J. Neurosci. 16, 7610-7618.
2. Alblas, J., Ulfman, L., Hordijk, P., and Koenderman, L. (2001). Activation of Rhoa and ROCK are essential for detachment of migrating leukocytes. Mol. Biol. Cell 12, 2137-2145.
3. Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., Matsuura, Y., and Kaibuchi, K. (1996). Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271, 20246-20249.
4. Arias, A.M. (2001). Epithelial mesenchymal interactions in cancer and development. Cell 105, 425-431.
5. Birchmeier, C., and Gherardi, E. (1998). Developmental roles of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol. 8, 404-410.
6. Bishop, A.L., and Hall, A. (2000). Rho GTPases, and their effector proteins. Biochem. J. 348 Pt 2, 241-255.
7. Bradley, P.L., and Andrew, D.J. (2001). ribbon encodes a novel BTB/POZ protein required for directed cell migration in Drosophila melanogaster. Development 128, 3001-3015.
8. Breitfeld, P., Casanova, J.E., Harris, J.M., Simister, N.E., and Mostov, K.E. (1989). Expression and analysis of the polymeric immunoglobulin receptor. Methods Cell Biol. 32, 329-337.
9. Chenn, A., and McConnell, S.K. (1995). Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 82, 631-641.
10. Chrzanowska-Wodnicka, M., and Burridge, K. (1996). Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133, 1403-1415.
11. Comer, F.I., and Parent, C.A. (2002). PI 3-Kinases and PTEN. How opposites chemoattract. Cell 109, 541-544.
12. Comoglio, P.M., and Boccaccio, C. (2001). Scatter factors and invasive growth. Semin. Cancer Biol. 11, 153-165.
13. Cukierman, E., Pankov, R., Stevens, D.R., and Yamada, K.M. (2001). Taking cell-matrix adhesions to the third dimension. Science 294, 1708-1712.
14. Drubin, D.G., and Nelson, W.J. (1996). Origins of cell polarity. Cell 84, 335-344.
15. Du, Q., Stukenberg, P.T., and Macara, I.G. (2001). A mammalian partner of inscuteable binds NuMA and regulates mitotic spindle organization. Nat. Cell Biol. 3, 1069-1075.
16. Dujardin, D.L., and Vallee, R.B. (2002). Dynein at the cortex. Curr. Opin. Cell Biol. 14, 44-49.
17. Estivill-Torrus, G., Pearson, H., van Heyningen, V., Price, D.J., and Rashbass, P. (2002). Pax6 is required to regulate the cell cycle and the rate of progression from symmetrical to asymmetrical division in mammalian cortical progenitors. Development 129, 455-466.
18. Etienne-Manneville, S., and Hall, A. (2001). Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCξ. Cell 106, 489-498.
19. Faulkner, N.E., Dujardin, D.L., Tai, C.Y., Vaughan, K.T., O'Connell, C.B., Wang, Y., and Vallee, R.B. (2000). A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat. Cell Biol. 2, 784-791.
20. Firtel, R.A., and Chung, C.Y. (2000). The molecular genetics of chemotaxis: sensing and responding to chemoattractant gradients. Bioessays 22, 603-615.
21. Franz, C.M., Jones, G.E., and Ridley, A.J. (2002). Cell migration in development and disease. Dev. Cell 2, 153-158.
22. Gundersen, G.G. (2002). Evolutionary conservation of microtubule-capture mechanisms. Nat. Rev. Mol. Cell. Biol. 3, 6-14.
23. Haugh, J.M., Codazzi, F., Teruel, M., and Meyer, T. (2000). Spatial sensing in fibroblasts mediated by 3′ phosphoinositides. J. Cell Biol. 151, 1269-1280.
24. Heins, N., Cremisi, F., Malatesta, P., Gangemi, R.M., Corte, G., Price, J., Goudreau, G., Gruss, P., and Gotz, M. (2001). Emx2 promotes symmetric cell divisions and a multipotential fate in precursors from the cerebral cortex. Mol. Cell. Neurosci. 18, 485-502.
25. Hirose, M., Ishizaki, T., Watanabe, N., Uehata, M., Kranenburg, O., Moolenaar, W.H., Matsumura, F., Maekawa, M., Bito, H., and Narumiya, S. (1998). Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J. Cell Biol. 141, 1625-1636.
26. Hogan, B.L.M., and Kolodziej, P.A. (2002). Organogenesis: molecular mechanisms of tubulogenesis. Nat. Rev. Genet. 3, 513-523.
27. Huang, S., and Ingber, D.E. (1999). The structural and mechanical complexity of cell-growth control. Nat. Cell Biol. 1, E131-E138.
28. Jan, Y.N., and Jan, L.Y. (2001). Asymmetric cell division in the Drosophila nervous system. Nat. Rev. Neurosci. 2, 772-779.
29. Kamikura, D.M., Khoury, H., Maroun, C., Naujokas, M.A., and Park, M. (2000). Enhanced transformation by a plasma membrane-associated met oncoprotein: activation of a phosphoinositide 3′-kinase-dependent autocrine loop involving hyaluronic acid and CD44. Mol. Cell. Biol. 10, 3482-3496.
30. Khwaja, A., Lehmann, K., Marte, B.M., and Downward, J. (1998). Phosphoinositide 3-kinase induces scattering and tubulogenesis in epithelial cells through a novel pathway. J. Biol. Chem. 273, 18793-18801.
31. Kimura, K., et al. (1996). Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
32. Knoblich, J.A. (2001). Asymmetric cell division during animal development. Nat. Rev. Mol. Cell. Biol. 2, 11-20.
33. Lipschutz, J.H., Guo, W., O'Brien, L.E., Nguyen, Y.H., Novick, P., and Mostov, K.E. (2000). 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.
34. Lipschutz, J.H., O'Brien, L.E., Altschuler, Y., Avrahami, D., Nguyen, Y., Tang, K., and Mostov, K.E. (2001). Analysis of membrane traffic in polarized epithelial cells. Curr. Prot. Cell Biol. 15, 5.
35. Lu, B., Roegiers, F., Jan, L.Y., and Jan, Y.N. (2001). Adherens junctions inhibit asymmetric division in the Drosophila epithelium. Nature 409, 522-525.
36. Metzger, R.J., and Krasnow, M.A. (1999). Genetic control of branching morphogenesis. Science 284, 1635-1639.
37. Mollard, R., and Dziadek, M. (1998). A correlation between epithelial proliferation rates, basement membrane component localization patterns, and morphogenetic potential in the embryonic mouse lung. Am. J. Respir. Cell Mol. Biol. 19, 71-82.
38. Montesano, R., Matsumoto, K., Nakamura, T., and Orci, L. (1991a). Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor. Cell 67, 901-908.
39. Montesano, R., Schaller, G., and Orci, L. (1991b). Induction of epithelial tubular morphogenesis in vitro by fibroblast-derived soluble factors. Cell 66, 697-711.
40. Mostov, K.E., Verges, M., and Altschuler, Y. (2000). Membrane traffic in polarized epithelial cells. Curr. Op. Cell Biol. 12, 483-490.
41. Nabi, I.R. (1999). The polarization of the motile cell. J. Cell Sci. 112, 1803-1811.
42. Nobes, C.D., and Hall, A. (1999). Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144, 1235-1244.
43. Nogawa, H., Morita, K., and Cardoso, W.V. (1998). Bud formation precedes the appearance of differential cell proliferation during branching morphogenesis of mouse lung epithelium in vitro. Dev. Dyn. 213, 228-235.
44. O'Brien, L.E., Jou, T.S., Pollack, A.L., Zhang, Q., Hansen, S.H., Yurchenco, P., and Mostov, K.E. (2001). Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat. Cell Biol. 3, 831-838.
45. O'Brien, L.E., Zegers, M.M.P., and Mostov, K.E. (2002). Opinion. Building epithelial architecture: insights from three-dimensional culture models. Nat. Rev. Mol. Cell. Biol. 3, 531-537.
46. Pollack, A.L., Barth, A.I., Altschuler, Y., Nelson, W.J., and Mostov, K.E. (1997). Dynamics of beta-catenin interactions with APC protein regulate epithelial tubulogenesis. J. Cell Biol. 137, 1651-1662.
47. Pollack, A.L., Runyan, R.B., and Mostov, K.E. (1998). 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.
48. Reinsch, S., and Karsenti, E. (1994). Orientation of spindle axis and distribution of plasma membrane proteins during cell division in polarized MDCKII cells. J. Cell Biol. 126, 1509-1526.
49. Ridley, A.J. (2001). Rho family proteins: coordinating cell responses. Trends Cell Biol. 11, 471-477.
50. Ridley, A.J., Comoglio, P.M., and Hall, A. (1995). Regulation of scatter factor/hepatocyte growth factor responses by Ras, Rac, and Rho in MDCK cells. Mol. Cell. Biol. 15, 1110-1122.
51. Roegiers, F., Younger-Shepherd, S., Jan, L.Y., and Jan, Y.N. (2001). Two types of asymmetric divisions in the Drosophila sensory organ precursor cell lineage. Nat. Cell Biol. 3, 58-67.
52. Savagner, P. (2001). Leaving the neighborhood: molecular mechanisms involved during epithelial-mesenchymal transition. Bioessays 23, 912-923.
53. Schliwa, M., and Hõner, B. (1993). Microtubules, centrosomes and intermediate filaments in directed cell movement. Trends Cell Biol. 3, 377-380.
54. Servant, G., Weiner, O.D., Herzmark, P., Balla, T., Sedat, J.W., and Bourne, H.R. (2000). Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 287, 1037-1040.
55. Shim, K., Blake, K.J., Jack, J., and Krasnow, M.A. (2001). The Drosophila ribbon gene encodes a nuclear BTB domain protein that promotes epithelial migration and morphogenesis. Development 128, 4923-4933.
56. Song, B., Zhao, M., Forrester, J.V., and McCaig, C.D. (2002). Electrical cues regulate the orientation and frequency of cell division and the rate of wound healing in vivo. Proc. Natl. Acad. Sci. USA 99, 13577-13582.
57. Stowers, L., Yelon, D., Berg, L.J., and Chant, J. (1995). Regulation of the polarization of T cells toward antigen-presenting cells by Ras-related GTPase CDC42. Proc. Natl. Acad. Sci. USA 92, 5027-5031.
58. Uehata, M., et al. (1997). Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994.
59. Vasquez, R.J., Howell, B., Yvon, A.M., Wadsworth, P., and Cassimeris, L. (1997). Nanomolar concentrations of nocodazole alter microtubule dynamic instability in vivo and in vitro. Mol. Biol. Cell 8, 973-985.
60. Walsh, S.V., Hopkins, A.M., Chen, J., Narumiya, S., Parkos, C.A., and Nusrat, A. (2001). Rho kinase regulates tight junction function and is necessary for tight junction assembly in polarized intestinal epithelia. Gastroenterology 121, 566-579.
61. Wang, F., Herzmark, P., Weiner, O.D., Srinivasan, S., Servant, G., and Bourne, H.R. (2002). Lipid products of PI(3)Ks maintain persistent cell polarity and directed motility in neutrophils. Nat. Cell Biol. 4, 513-518.
62. Ward, Y., Yap, S.F., Ravichandran, V., Matsumura, F., Ito, M., Spinelli, B., and Kelly, K. (2002). The GTP binding proteins Gem and Rad are negative regulators of the Rho-Rho kinase pathway. J. Cell Biol. 157, 291-302.
63. Watton, S.J., and Downward, J. (1999). Akt/PKB localization and 3′ phosphoinositide generation at sites of epithelial cell-matrix and cell-cell interaction. Curr. Biol. 9, 433-436.
64. Webb, D.J., Parsons, J.T., and Horwitz, A.F. (2002). Adhesion assembly, disassembly and turnover in migrating cells - over and over and over again. Nat. Cell Biol. 4, E97-E100.
65. Wittmann, T., and Waterman-Storer, C.M. (2001). Cell motility: can Rho GTPases and microtubules point the way? J. Cell Sci. 114, 3795-3803.
66. Wodarz, A. (2002). Establishing cell polarity in development. Nat. Cell Biol. 4, E39-E44.
67. Worthylake, R.A., Lemoine, S., Watson, J.M., and Burridge, K. (2001). RhoA is required for monocyte tail retraction during trans-endothelial migration. J. Cell Biol. 154, 147-160.
68. Yvon, A.M., Walker, J.W., Danowski, B., Fagerstrom, C., Khodjakov, A., and Wadsworth, P. (2002). Centrosome reorientation in wound-edge cells is cell type specific. Mol. Biol. Cell 13, 1871-1880.
69. Zegers, M.M.P., O'Brien, L.E., Yu, W., Datta, A., and Mostov, K.E. (2003). Epithelial polarity and tubulogenesis in vitro. Trends Cell Biol. (in press).