TgrC1 mediates cell-cell adhesion by interacting with TgrB1 via mutual IPT/TIG domains during development of Dictyostelium discoideum

Biochemical Journal

Volumn 452, Issue 2, 2013, Pages 259-269

  Chen, Gong ^a   Wang, Jun ^b   Xu, Xiaoqun ^c,d   Wu, Xiangfu ^c   Piao, Ruihan ^a   Siu, Chi Hung ^c  

^a UNIVERSITY OF TORONTO   (Canada)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c UNIVERSITY OF TORONTO   (Canada)

^d SHANDONG PROVINCIAL HOSPITAL AFFILIATED TO SHANDONG FIRST MEDICAL UNIVERSITY   (China)

Author keywords

Cell adhesion molecule; Dictyostelium discoideum; Heterophilic interaction; IPT TIG domain; Mass spectrometry

Indexed keywords

MEMBRANE PROTEIN; PROTEIN TGRB1; PROTEIN TGRC1; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL ADHESION; CELL AGGREGATION; CELL DIFFERENTIATION; CELL MEMBRANE; CHROMOSOME 3; CONTROLLED STUDY; DICTYOSTELIUM DISCOIDEUM; FRUITING BODY; IN VITRO STUDY; LIQUID CULTURE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; VEGETATIVE GROWTH;

CELL ADHESION; CELL ADHESION MOLECULES; CELL COMMUNICATION; DICTYOSTELIUM; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84877724261     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121674     Document Type: Article

References (53)

1. King, N., Hittinger, C. T. and Carroll, S. B. (2003) Evolution of key cell signaling and adhesion protein families predates animal origins. Science 301, 361-363
2. Vogel, C. and Chothia, C. (2006) Protein family expansions and biological complexity. PLoS Comput. Biol. 2, e48
3. Abedin, M. and King, N. (2010) Diverse evolutionary paths to cell adhesion. Trends Cell Biol. 20, 734-742
4. Kessin, R. H. (2001) A history of research on Dictyostelium discoideum. In Dictyostelium: Evolution, Cell Biology, and the Development of Multicellularity, pp. 9-19, Cambridge University Press, Cambridge
5. Müller-Taubenberger, A. and Bozzaro, S. (2006) From cell-cell adhesion and cellular oscillations to spectacular views inside the cell: 50 years of research with Dictyostelium. Eur. J. Cell Biol. 85, 851-858
6. Coates, J. C. and Harwood, A. J. (2001) Cell-cell adhesion and signal transduction during Dictyostelium development. J. Cell Sci. 114, 4349-4358
7. Siu, C.-H., Harris, T. J., Wang, J. and Wong, E. (2004) Regulation of cell-cell adhesion during Dictyostelium development. Semin. Cell Dev. Biol. 15, 633-641
8. Siu, C.-H., Sriskanthadevan, S., Wang, J., Hou, L., Chen, G., Xu, X., Thomson, A. and Yang, C. (2011) Regulation of spatiotemporal expression of cell-cell adhesion molecules during development of Dictyostelium discoideum. Dev. Growth Differ. 53, 518-527
9. 2+-dependent mechanism. J. Biol. Chem. 268, 24902-24909
10. 2+-dependent cell-cell adhesion molecule, in Dictyostelium discoideum. J. Biol. Chem. 271, 16399-16408
11. 2+-dependent cell adhesion molecule DdCAD-1 is regulated by multiple factors during Dictyostelium development. Differentiation 61, 275-284
12. 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
13. Siu, C.-H., Lam, T. Y. and Choi, A. H. (1985) Inhibition of cell-cell binding at the aggregation stage of Dictyostelium discoideum development by monoclonal antibodies directed against an 80,000-dalton surface glycoprotein. J. Biol. Chem. 260, 16030-16036
14. Kamboj, R. K., Gariepy, J. and Siu, C.-H. (1989) Identification of an octapeptide involved in homophilic interaction of the cell adhesion molecule gp80 of Dictyostelium discoideum. Cell 59, 615-625
15. Stein, T. and Gerisch, G. (1996) Oriented binding of a lipid-anchored cell adhesion protein onto a biosensor surface using hydrophobic immobilization and photoactive crosslinking. Anal. Biochem. 237, 252-259
16. Harris, T. J. and Siu, C.-H. (2002) Reciprocal raft-receptor interactions and the assembly of adhesion complexes. BioEssays 24, 996-1003
17. Gao, E. N., Shier, P. and Siu, C.-H. (1992) Purification and partial characterization of a cell adhesion molecule (gp150) involved in postaggregation stage cell-cell binding in Dictyostelium discoideum. J. Biol. Chem. 267, 9409-9415
18. Dynes, J. L., Clark, A. M., Shaulsky, G., Kuspa, A., Loomis, W. F. and Firtel, R. A. (1994) LagC is required for cell-cell interactions that are essential for cell-type differentiation in Dictyostelium. Genes Dev. 8, 948-958
19. 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
20. Sriskanthadevan, S., Zhu, Y., Manoharan, K., Yang, C. and Siu, C.-H. (2011) The cell adhesion molecule DdCAD-1 regulates morphogenesis through differential spatiotemporal expression in Dictyostelium discoideum. Development 138, 2487-2497
21. Kamboj, R. K., Lam, T. Y. and Siu, C.-H. (1990) Regulation of slug size by the cell adhesion molecule gp80 in Dictyostelium discoideum. Cell Regul. 1, 715-729
22. 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
23. Iranfar, N., Fuller, D., Sasik, R., Hwa, T., Laub, M. and Loomis, W. F. (2001) Expression patterns of cell-type-specific genes in Dictyostelium. Mol. Biol. Cell 12, 2590-2600
24. Kibler, K., Svetz, J., Nguyen, T. L., Shaw, C. and Shaulsky, G. (2003) A cell-adhesion pathway regulates intercellular communication during Dictyostelium development. Dev. Biol. 264, 506-521
25. 2+-dependent cell-cell adhesion. Nat. Struct. Mol. Biol. 13, 1016-1022
26. Benabentos, R., Hirose, S., Sucgang, R., Curk, T., Katoh, M., Ostrowski, E. A., Strassmann, J. E., Queller, D. C., Zupan, B., Shaulsky, G. and Kuspa, A. (2009) Polymorphic members of the lag gene family mediate kin discrimination in Dictyostelium. Curr. Biol. 19, 567-572
27. Niemann, H. H., Jager, V., Butler, J. G., van den Heuvel, J., Schmidt, S., Ferraris, D., Gherardi, E. and Heinz, D. W. (2007) Structure of the human receptor tyrosine kinase Met in complex with the Listeria invasion protein lnlB. Cell 130, 235-246
28. Wang, J., An, H., Mayo, M. W., Baldwin, A. S. and Yarbrough, W. G. (2007) LZAP, a putative tumor suppressor, selectively inhibits NF-κB. Cell 12, 239-251
29. Treiber, N., Treiber, T., Zocher, G. and Grosschedl, R. (2010) Structure of an Ebf1, DNA complex reveals unusual DNA recognition and structural homology with Rel proteins. Genes Dev. 24, 2270-2275
30. 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
31. Fey, P., Kowal, A. S., Gaudet, P., Pilcher, K. E. and Chisholm, R. L. (2007) Protocols for growth and development of Dictyostelium discoideum. Nat. Protoc. 2, 1307-1316
32. Gaudet, P., Pilcher, K. E., Fey, P. and Chisholm, R. L (2007) Transformation of Dictyostelium discoideum with plasmid DNA. Nat. Protoc. 2, 1317-1324
33. Poulsen, B. E., Rath, A. and Deber, C. M. (2009) The assembly motif of a bacterial small multidrug resistance protein. J. Biol. Chem. 284, 9870-9875
34. Springer, W. R. and Barondes, S. H. (1980) Cell adhesion molecules: detection with univalent second antibody. J. Cell Biol. 87, 703-707
35. Albertsson, P. A. (1970) Partition of cell particles and macromolecules in polymer two-phase systems. Adv. Prot. Chem. 24, 309-341
36. Siu, C.-H., Author, P., Richard, A. L. and William, F. L. (1977) Rapid accumulation and disappearance of plasma membrane proteins during development of wild-type and mutant strains of Dictyostelium discoideum. J. Mol. Biol. 116, 469-488
37. Harris, T. J., Awrey, D. E., Cox, B. J., Ravandi, A., Tsang, A. and Siu, C.-H. (2001) Involvement of a triton-insoluble floating fraction in Dictyostelium cell-cell adhesion. J. Biol. Chem. 276, 18640-18648
38. Hirose, S., Benabentos, R., Ho, H. I., Kuspa, A. and Shaulsky, G. (2011) Self-recognition in social amoebae is mediated by allelic pairs of tiger genes. Science 333, 467-470
39. May, I., Blusch, J., Sachse, A. and Nellen, W. (1991) A cis-acting element responsible for early gene induction by extracellular cAMP in Dictyostelium discoideum. Mech. Dev. 33, 147-155
40. Desbarats, L., Lam, T. Y., Wong, L. M. and Siu, C.-H. (1992) Identification of a unique cAMP-response element in the gene encoding the cell adhesion molecule gp80 in Dictyostelium discoideum. J. Biol. Chem. 267, 19655-19664
41. Marchalonis, J. J. and Schluter, S. F. (1989) Evolution of variable and constant domains and joining segments of rearranging immunoglobulins. FASEB J. 3, 2469-2479
42. Sukumaran, S., Brown, J. M., Firtel, R. A. and McNally, J. G. (1998) lagC-null and gbf-null cells define key steps in the morphogenesis of Dictyostelium mounds. Dev. Biol. 200, 16-26
43. Siu, C.-H., Des Roches, B. and Lam, T. Y. (1983) Involvement of a cell-surface glycoprotein in the cell-sorting process of Dictyostelium discoideum. Proc. Natl. Acad. Sci. U.S.A. 80, 6596-6600
44. Daburon, V., Mella, S., Plouhinec, J. L., Mazan, S., Crozatier, M. and Vincent, A (2008) The metazoan history of the COE transcription factors. Selection of a variant HLH motif by mandatory inclusion of a duplicated exon in vertebrates. BMC Evol. Biol. 8, 131
45. Onuchic, L. F., Furu, L., Nagasawa, Y., Hou, X., Eggermann, T., Ren, Z., Bergmann, C., Senderek, J., Esquivel, E., Zeltner, R. et al. (2002) PKHD1, the polycystic kidney and hepatic disease 1 gene, encodes a novel large protein containing multiple immunoglobulin-like plexin-transcription-factor domains and parallel β-helix 1 repeats. Am. J. Hum. Genet. 70, 1305-1317
46. Hota, P. K. and Buck, M. (2012) Plexin structures are coming: opportunities for multilevel investigations of semaphorin guidance receptors, their cell signaling mechanisms, and functions. Cell. Mol. Life Sci. 69, 3765-3785
47. Ghosh, G., van Duyne, G., Ghosh, S. and Sigler, P. B. (1995) Structure of NF-κB p50 homodimer bound to a κB site. Nature 373, 303-310
48. Müller, C. W., Rey, F. A., Sodeoka, M., Verdine, G. L. and Harrison, S. C. (1995) Structure of the NF-κB p50 homodimer bound to DNA. Nature 373, 311-317
49. Siponen, M. I., Wisniewska, M., Lehtiö, L., Johansson, I., Svensson, L., Raszewski, G., Nilsson, L., Sigvardsson, M. and Berglund, H. (2010) Structural determination of functional domains in early B-cell factor (EBF) family of transcription factors reveals similarities to Rel DNA-binding proteins and a novel dimerization motif. J. Biol. Chem. 285, 25875-25879
50. Ma, Q., Zhang, K., Guin, S., Zhou, Y. Q. and Wang, M. H. (2010) Deletion or insertion in the first immunoglobulin-plexin-transcription (IPT) domain differentially regulates expression and tumorigenic activities of RON receptor tyrosine kinase. Mol. Cancer 9, 307
51. Zhang, K., Zhou, Y. Q., Yao, H. P. and Wang, M. H. (2010) Alterations in a defined extracellular region of the RON receptor tyrosine kinase promote RON-mediated motile and invasive phenotypes in epithelial cells. Int. J. Oncol. 36, 255-264
52. Weijer, C. J. (2009) Collective cell migration in development. J. Cell Sci. 122, 3215-3223
53. Kim, S., Jeon, T. J., Oberai, A., Yang, D., Schmidt, J. J. and Bowie, J. U. (2005) Transmembrane glycine zippers: physiological and pathological roles in membrane proteins. Proc. Natl. Acad. Sci. U.S.A. 102, 14278-14283