Regulation of Rap1 activity is required for differential adhesion, cell-type patterning and morphogenesis in Dictyostelium

Journal of Cell Science

Volumn 122, Issue 3, 2009, Pages 335-344

  Parkinson, Katie ^a   Bolourani, Parvin ^b   Traynor, David ^c   Aldren, Nicola L ^a   Kay, Robert R ^c   Weeks, Gerald ^b   Thompson, Christopher R L ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Differential cell adhesion; Morphogenesis; Pattern formation; Rap1; RapGAP

Indexed keywords

F ACTIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; RAP1 GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; RAP1 PROTEIN; UNCLASSIFIED DRUG; TELOMERE BINDING PROTEIN;

ARTICLE; CELL ADHESION; CELL LEVEL; CELL MATURATION; CELL SELECTION; CELL TYPE; CHEMOTAXIS; CONTROLLED STUDY; DICTYOSTELIUM; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN PROTEIN INTERACTION; WILD TYPE; AMINO ACID SEQUENCE; ANIMAL; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; GENE INACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; SEQUENCE ALIGNMENT;

DICTYOSTELIUM;

AMINO ACID SEQUENCE; ANIMALS; CELL ADHESION; CELL DIFFERENTIATION; CELL MOVEMENT; DICTYOSTELIUM; GENE KNOCKOUT TECHNIQUES; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; RAP1 GTP-BINDING PROTEINS; SEQUENCE ALIGNMENT; TELOMERE-BINDING PROTEINS;

EID: 63349091530     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.036822     Document Type: Article

References (50)

1. Abe, T., Langenick, J. and Williams, J. G. (2003). Rapid generation of gene disruption constructs by in vitro transposition and identification of a Dictyostelium protein kinase that regulates its rate of growth and development. Nucleic Acids Res. 31, 107-111.
2. Bolourani, P., Spiegelman, G. B. and Weeks, G. (2008). Rap1 activation in response to cAMP occurs downstream of Ras activation during Dictyostelium aggregation. J. Biol. Chem. 283, 10232-10240.
3. Bos, J. L. (1998). All in the family? New insights and questions regarding interconnectivity of Ras, Rap1 and Ral. EMBO J. 17, 6776-6782.
4. Bos, J. L. (2005). Linking Rap to cell adhesion. Curr. Opin. Cell Biol. 17, 123-128.
5. Bosgraaf, L., Waijer, A., Engel, R., Visser, A. J. W. G., Wesseis, D., Soll, D. and van Haastert, P. J. M. (2005). RasGEF-containing proteins GbpC and GbpD have differential effects on cell polarity and chemotaxis in Dictyostelium. J. Cell Sci. 118, 1899-1910.
6. Chisholm, R. L. and Firtel, R. A. (2004). Insights into morphogenesis from a simple developmental system. Nat. Rev. Mol. Cell. Biol. 5, 531-541.
7. Coates, J. C., Grimson, M. J., Williams, R. S., Bergman, W., Blanton, R. L. and Harwood, A. J. (2002). Loss of the beta-catenin homologue aardvark causes ectopic stalk formation in Dictyostelium. Mech. Dev. 116, 117-127.
8. Cornillon, S., Gebbie, L., Benghezal, M., Nair, P., Keller, S., Wehrle-Haller, B., Charette, S. J., Bruckert, F., Letourneur, F. and Cosson, P. (2006). An adhesion molecule in free-living Dictyostelium amoebae with integrin beta features. EMBO Rep. 7, 617-621.
9. Early, A. E., Gaskell, M. J., Traynor, D. and Williams, J. G. (1993). Two distinct populations of prestalk cells within the tip of the migratory Dictyostelium slug with differing fates at culmination. Development 118, 353-362.
10. Early, A., Abe, T. and Williams, J. (1995). Evidence for positional differentiation of prestalk cells and for a morphogenetic gradient in Dictyostelium. Cell 83, 91-99.
11. Fey, P., Stephens, S., Titus, M. A. and Chisholm, R. L. (2002). SadA, a novel adhesion receptor in Dictyostelium. J. Cell Biol. 159, 1109-1119.
12. Fujita, Y., Hogan, C. and Braga, V. M. M. (2006). Regulation of cell-cell adhesion by Rap1. Methods Enzymol. 407, 359-372.
13. Gebbie, L., Benghezal, M., Cornillon, S., Froquet, R., Cherix, N., Malbouyres, M., Lefkir, Y., Grangeasse, C., Fache, S., Dalous, J. et al. (2004). Phg2, a kinase involved in adhesion and focal site modeling in Dictyostelium. Mol. Biol. Cell 15, 3915-3925.
14. Ginger, R. S., Drury, L., Baader, C., Zhukovskaya, N. V. and Williams, J. G. (1998). A novel Dictyostelium cell surface protein important for both cell adhesion and cell sorting. Development 125, 3343-3352.
15. Gomer, R., Gao, T., Tang, Y. T., Knecht, D. and Titus, M. A. (2002). Cell motility mediates tissue size regulation in Dictyostelium. J. Muscle Res. Cell Motil. 23, 809-815.
16. Grimson, M. J., Coates, J. C., Reynolds, J. P., Shipman, M., Blanton, R. L. and Harwood, A. J. (2000). Adherens junctions and beta-catenin-mediated cell signalling in a non- metazoan organism. Nature 408, 727-731.
17. Harloff, C., Gerisch, G. and Noegel, A. A. (1989). Selective elimination of the contact site A protein of Dictyostelium discoideum by gene disruption. Genes Dev. 3, 2011-2019.
18. Jeon, T. J., Lee, D. J., Lee, S., Weeks, G. and Firtel, R. A. (2007a). Regulation of Rap1 activity by RapGAP1 controls cell adhesion at the front of chemotaxing cells. J. Cell Biol. 179, 833-843.
19. Jeon, T. J., Lee, D. J., Merlot, S., Weeks, G. and Firtel, R. A. (2007b). Rap1 controls cell adhesion and cell motility through the regulation of myosin II. J. Cell Biol. 176, 1021-1033.
20. Kae, H., Lim, C. J., Spiegelman, G. B. and Weeks, G. (2004). Chemoattractant-induced Ras activation during Dictyostelium aggregation. EMBO Rep. 5, 602-606.
21. Kang, R. J., Kae, H., Ip, H., Spiegelman, G. B. and Weeks, G. (2002). Evidence for a role for the Dictyostelium Rap1 in cell viability and the response to osmotic stress. J. Cell Sci. 115, 3675-3682.
22. Kessin, R. H. (2001). Dictyostelium. Cambridge: Cambridge University Press.
23. Kitayama, H., Sugimoto, Y., Matsuzaki, T., Ikawa, Y. and Noda, M. (1989). A Ras-related gene with transformation suppressor activity. Cell 56, 77-84.
24. Knecht, D. A., Cohen, S. M., Loomis, W. F. and Lodish, H. F. (1986). Developmental regulation of Dictyostelium discoideum actin gene fusions carried on low-copy and high-copy transformation vectors. Mol. Cell. Biol. 6, 3973-3983.
25. Knox, A. L. and Brown, N. H. (2002). Rap1 GTPase regulation of adherens junction positioning and cell adhesion. Science 295, 1285-1288.
26. Kooistra, M. R., Dube, N. and Bos, J. L. (2007). Rap1: a key regulator in cell-cell junction formation. J. Cell Sci. 120, 17-22.
27. Kortholt, A., Rehmann, H., Kae, H., Bosgraaf, L., Keizer-Gunnink, I., Weeks, G., Wittinghofer, A. and Van Haastert, P. J. M. (2006). Characterization of the GbpD-activated Rap1 pathway regulating adhesion and cell polarity in Dictyostelium discoideum. J. Biol. Chem. 281, 23367-23376.
28. Krieg, M., Arboleda-Estudillo, Y., Puech, P. H., Kafer, J., Graner, F., Muller, D. J. and Heisenberg, C. P. (2008). Tensile forces govern germ-layer organization in zebrafish. Nat. Cell Biol. 10, 429-436.
29. Lam, T. Y., Pickering, G., Geltosky, J. and Siu, C. H. (1981). Differential cell cohesiveness expressed by prespore and prestalk cells of Dictyostelium discoideum. Differentiation 20, 22-28.
30. Lorenowicz, M. J., van Gils, J., de Boer, M., Hordijk, P. L. and Fernandez-Borja, M. (2006). Epac1-Rap1 signaling regulates monocyte adhesion and chemotaxis. J. Leukoc. Biol. 80, 1542-1552.
31. Louis, S. A., Weeks, G. and Spiegelman, G. B. (1997). Rap1 overexpression reveals that activated RasD induces separable defects during Dictyostelium development. Dev. Biol. 190, 273-283.
32. Maeda, M., Haruyo, S., Maruo, T., Ogihara, S., Iranfar, N., Fuller, D., Morio, T., Urushihara, H., Tanaka, T. and Loomis, W. F. (2003). Changing patterns of gene expression in prestalk cell subtypes of Dictyostelium recognised by in situ hybridisation with genes from microarray analyses. Eukaryotic Cell 2, 627-637.
33. Maruo, T., Sakamoto, H., Iranfar, N., Fuller, D., Morio, T., Urushihara, H., Tanaka, Y., Maeda, M. and Loomis, W. F. (2004). Control of cell type proportioning in Dictyostelium discoideum by differentiation-inducing factor as determined by in situ hybridization. Eukaryotic Cell 3, 124-128.
34. Matsukuma, S. and Durston, A. J. (1979). Chemotactic cell sorting in Dictyostelium discoideum. J. Embryol. Exp. Morphol. 50, 243-251.
35. McLeod, S. J., Shum, A. J., Lee, R. L., Takei, F. and Gold, M. R. (2004). The Rap GTPases regulate integrin-mediated adhesion, cell spreading, actin polymerization, and Pyk2 tyrosine phosphorylation in B lymphocytes. J. Biol. Chem. 279, 12009-12019.
36. Rebstein, P. J., Cardelli, J., Weeks, G. and Spiegelman, G. B. (1997). Mutational analysis of the role of Rap1 in regulating cytoskeletal function in Dictyostelium. Exp. Cell Res. 231, 276-283.
37. Reedquist, K. A., Ross, E., Koop, E. A., Wolthuis, R. M., Zwartkruis, F. J., van Kooyk, Y., Salmon, M., Buckley, C. D. and Bos, J. L. (2000). The small GTPase, Rap1, mediates CD31-induced integrin adhesion. J. Cell Biol. 148, 1151-1158.
38. Robbins, S. M., Suttorp, V. V., Weeks, G. and Spiegelman, G. B. (1990). A Ras-related gene from the lower eukaryote dictyostelium that is highly conserved relative to the human Rap genes. Nucleic Acids Res. 18, 5265-5269.
39. Roisin-Bouffay, C., Jang, W., Caprette, D. R. and Gomer, R. H. (2000). A precise group size in Dictyostelium is generated by a cell-counting factor modulating cell-cell adhesion. Mol. Cell 6, 953-959.
40. Seastone, D. J., Zhang, L., Buczynski, G., Rebstein, P., Weeks, G., Spiegelman, G. and Cardelli, J. (1999). The small Mr Ras-like GTPase Rap1 and the phospholipase C pathway act to regulate phagocytosis in Dictyostelium discoideum. Mol. Biol. Cell 10, 393-406.
41. Shimonaka, M., Katagiri, K., Nakayama, T., Fujita, N., Tsuruo, T., Yoshie, O. and Kinashi, T. (2003). Rap1 translates chemokine signals to integrin activation, cell polarization, and motility across vascular endothelium under flow. J. Cell Biol. 161, 417-427.
42. Steinberg, M. S. and Takeichi, M. (1994). Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. Proc. Natl. Acad. Sci. USA 91, 206-209.
43. Sussman, M. (1987). Cultivation and synchronous morphogenesis of Dictyostelium under controlled experimental conditions. Methods Cell Biol. 28, 9-29.
44. Thompson, C. R. L., Reichelt, S. and Kay, R. R. (2004). A demonstration of pattern formation without positional information in Dictyostelium. Dev. Growth Differ. 46, 363-369.
45. Wang, J., Hou, L., Awrey, D., Loomis, W. F., Firtel, R. A. and Siu, C. H. (2000). The membrane glycoprotein gp150 is encoded by the lagC gene and mediates cell-cell adhesion by heterophilic binding during Dictyostelium development. Dev. Biol. 227, 734-745.
46. Weeks, G., Gaudet, P. and Insall, R. (2005). The small GTPase superfamily. In Dictyostelium Genomics (ed. W. F. Loomis and A. Kuspa), pp. 173-210. Norfolk: Horizon Bioscience.
47. Williams, J. G., Duffy, K. T., Lane, D. P., Mcrobbie, S. J., Harwood, A. J., Traynor, D., Kay, R. R. and Jermyn, K. A. (1989). Origins of the prestalk-prespore pattern in Dictyostelium development. Cell 59, 1157-1163.
48. Wong, E., Yang, C., Wang, J., Fuller, D., Loomis, W. F. and Siu, C. H. (2002). Disruption of the gene encoding the cell adhesion molecule DdCAD-1 leads to aberrant cell sorting and cell-type proportioning during Dictyostelium development. Development 129, 3839-3850.
49. Yamada, Y., Sakamoto, S., Ogihara, S. and Maeda, Y. (2005). Novel patterns of the gene expression regulation in the prestalk region along the antero-posterior axis during multicellular development of Dictyostelium. Gene Expr. Patterns 6, 63-68.
50. Zhang, Z. C., Rehmann, H., Price, L. S., Riedl, J. and Bos, J. L. (2005). AF6 negatively regulates Rap1-induced cell adhesion. J. Biol. Chem. 280, 33200-33205.