1887

Microbiology Society logo

Volume 156, Issue 3

G5 subunit-mediated signalling requires a D-motif and the MAPK ERK1 in Free

Abstract

The G5 subunit has been shown to reduce cell viability, inhibit folate chemotaxis and accelerate tip morphogenesis and gene expression during multicellular development. Alteration of the D-motif (mitogen-activated protein kinase docking site) at the amino terminus of the G5 subunit or the loss of extracellular signal-regulated kinase (ERK)1 diminished the lethality associated with the overexpression or constitutive activation of the G5 subunit. The amino-terminal D-motif of the G5 subunit was also found to be necessary for the reduced cell size, small aggregate formation and precocious developmental gene expression associated with G5 subunit overexpression. This D-motif also contributed to the aggregation delay in cells expressing a constitutively active G5 subunit, but the D-motif was not necessary for the inhibition of folate chemotaxis. These results suggest that the amino-terminal D-motif is required for some but not all phenotypes associated with elevated G5 subunit functions during growth and development and that ERK1 can function in G5 subunit-mediated signal transduction.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): ERK, extracellular signal-regulated kinase and MAPK, mitogen-activated protein kinase
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.036541-0
2010-03-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/3/789.html?itemId=/content/journal/micro/10.1099/mic.0.036541-0&mimeType=html&fmt=ahah

References

  1. Albert P. R., Robillard L. 2002; G protein specificity: traffic direction required. Cell Signal 14:407–418
     [Google Scholar]
  2. Arnold K., Bordoli L., Kopp J., Schwede T. 2006; The swiss-model workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201
     [Google Scholar]
  3. Aubry L., Firtel R. 1999; Integration of signaling networks that regulate Dictyostelium differentiation. Annu Rev Cell Dev Biol 15:469–517
     [Google Scholar]
  4. Blackwell E., Halatek I. M., Kim H. J., Ellicott A. T., Obukhov A. A., Stone D. E. 2003; Effect of the pheromone-responsive G(alpha) and phosphatase proteins of Saccharomyces cerevisiae on the subcellular localization of the Fus3 mitogen-activated protein kinase. Mol Cell Biol 23:1135–1150
     [Google Scholar]
  5. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
     [Google Scholar]
  6. Brzostowski J. A., Kimmel A. R. 2006; Nonadaptive regulation of ERK2 in Dictyostelium: implications for mechanisms of cAMP relay. Mol Biol Cell 17:4220–4227
     [Google Scholar]
  7. Caunt C. J., Finch A. R., Sedgley K. R., McArdle C. A. 2006; Seven-transmembrane receptor signalling and ERK compartmentalization. Trends Endocrinol Metab 17:276–283
     [Google Scholar]
  8. Feinberg A. P., Vogelstein B. 1983; A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13
     [Google Scholar]
  9. Firtel R. A. 1996; Interacting signaling pathways controlling multicellular development in Dictyostelium. Curr Opin Genet Dev. 6545–554
  10. Firtel R. A., van Haastert P. J., Kimmel A. R., Devreotes P. N. 1989; G protein linked signal transduction pathways in development: Dictyostelium as an experimental system. Cell 58:235–239
     [Google Scholar]
  11. Gaskins C., Maeda M., Firtel R. A. 1994; Identification and functional analysis of a developmentally regulated extracellular signal-regulated kinase gene in Dictyostelium discoideum. Mol Cell Biol 14:6996–7012
     [Google Scholar]
  12. Goldberg J. M., Manning G., Liu A., Fey P., Pilcher K. E., Xu Y., Smith J. L. 2006; The dictyostelium kinome – analysis of the protein kinases from a simple model organism. PLoS Genet 2:e38
     [Google Scholar]
  13. Grewal S., Molina D. M., Bardwell L. 2006; Mitogen-activated protein kinase (MAPK)-docking sites in MAPK kinases function as tethers that are crucial for MAPK regulation in vivo. Cell Signal 18:123–134
     [Google Scholar]
  14. Hadwiger J. A. 2007; Developmental morphology and chemotactic responses are dependent on G alpha subunit specificity in Dictyostelium. Dev Biol 312:1–12
     [Google Scholar]
  15. Hadwiger J. A., Natarajan K., Firtel R. A. 1996; Mutations in the Dictyostelium heterotrimeric G protein α subunit G α5 alter the kinetics of tip morphogenesis. Development 122:1215–1224
     [Google Scholar]
  16. Hildebrandt J. D. 1997; Role of subunit diversity in signaling by heterotrimeric G proteins. Biochem Pharmacol 54:325–339
     [Google Scholar]
  17. Holbrook S. R., Kim S. H. 1989; Molecular model of the G protein alpha subunit based on the crystal structure of the HRAS protein. Proc Natl Acad Sci U S A 86:1751–1755
     [Google Scholar]
  18. Hopper N. A., Sanders G. M., Fosnaugh K. L., Williams J. G., Loomis W. F. 1995; Protein kinase A is a positive regulator of spore coat gene transcription in Dictyostelium. Differentiation 58:183–188
     [Google Scholar]
  19. Hur E. M., Kim K. T. 2002; G protein-coupled receptor signalling and cross-talk: achieving rapidity and specificity. Cell Signal 14:397–405
     [Google Scholar]
  20. Knetsch M. L., Epskamp S. J., Schenk P. W., Wang Y., Segall J. E., Snaar-Jagalska B. E. 1996; Dual role of cAMP and involvement of both G-proteins and ras in regulation of ERK2 in Dictyostelium discoideum. EMBO J 15:3361–3368
     [Google Scholar]
  21. Landry Y., Gies J. P. 2002; Heterotrimeric G proteins control diverse pathways of transmembrane signaling, a base for drug discovery. Mini Rev Med Chem 2:361–372
     [Google Scholar]
  22. Levi S., Polyakov M., Egelhoff T. T. 2000; Green fluorescent protein and epitope tag fusion vectors for Dictyostelium discoideum. Plasmid 44:231–238
     [Google Scholar]
  23. Maeda M., Firtel R. A. 1997; Activation of the mitogen-activated protein kinase ERK2 by the chemoattractant folic acid in Dictyostelium. J Biol Chem 272:23690–23695
     [Google Scholar]
  24. Maeda M., Aubry L., Insall R., Gaskins C., Devreotes P. N., Firtel R. A. 1996; Seven helix chemoattractant receptors transiently stimulate mitogen-activated protein kinase in Dictyostelium – role of heterotrimeric G proteins. J Biol Chem 271:3351–3354
     [Google Scholar]
  25. Maeda M., Lu S., Shaulsky G., Miyazaki Y., Kuwayama H., Tanaka Y., Kuspa A., Loomis W. F. 2004; Periodic signaling controlled by an oscillatory circuit that includes protein kinases ERK2 and PKA. Science 304:875–878
     [Google Scholar]
  26. Mann S. K., Firtel R. A. 1993; cAMP-dependent protein kinase differentially regulates prestalk and prespore differentiation during Dictyostelium development. Development 119:135–146
     [Google Scholar]
  27. Mann S. K., Richardson D. L., Lee S., Kimmel A. R., Firtel R. A. 1994; Expression of cAMP-dependent protein kinase in prespore cells is sufficient to induce spore cell differentiation in Dictyostelium. Proc Natl Acad Sci U S A 91:10561–10565
     [Google Scholar]
  28. Metodiev M. V., Matheos D., Rose M. D., Stone D. E. 2002; Regulation of MAPK function by direct interaction with the mating-specific G α in yeast. Science 296:1483–1486
     [Google Scholar]
  29. Milligan G., Kostenis E. 2006; Heterotrimeric G-proteins: a short history. Br J Pharmacol 147:Suppl. 1S46–S55
     [Google Scholar]
  30. Miranda-Saavedra D., Barton G. J. 2007; Classification and functional annotation of eukaryotic protein kinases. Proteins 68:893–914
     [Google Scholar]
  31. Natarajan K., Ashley C. A., Hadwiger J. A. 2000; Related G α subunits play opposing roles during Dictyostelium development. Differentiation 66:136–146
     [Google Scholar]
  32. Neves S. R., Ram P. T., Iyengar R. 2002; G protein pathways. Science 296:1636–1639
     [Google Scholar]
  33. Nguyen H. N., Hadwiger J. A. 2009; The G α4 G protein subunit interacts with the MAP kinase ERK2 using a D-motif that regulates developmental morphogenesis in Dictyostelium. Dev Biol 335:385–395
     [Google Scholar]
  34. Nguyen H.-N., Raisley B., Hadwiger J. A. 2010; MAP Kinases have different functions in Dictyostelium G Protein-Mediated Signaling. Cell Signal in press [View Article]
     [Google Scholar]
  35. Offermanns S., Simon M. I. 1998; Genetic analysis of mammalian G-protein signalling. Oncogene 17:1375–1381
     [Google Scholar]
  36. Raman M., Chen W., Cobb M. H. 2007; Differential regulation and properties of MAPKs. Oncogene 26:3100–3112
     [Google Scholar]
  37. Remenyi A., Good M. C., Bhattacharyya R. P., Lim W. A. 2005; The role of docking interactions in mediating signaling input, output, and discrimination in the yeast MAPK network. Mol Cell 20:951–962
     [Google Scholar]
  38. Segall J. E., Kuspa A., Shaulsky G., Ecke M., Maeda M., Gaskins C., Firtel R. A., Loomis W. F. 1995; A MAP kinase necessary for receptor-mediated activation of adenylyl cyclase in Dictyostelium. J Cell Biol 128:405–413
     [Google Scholar]
  39. Simon M. I., Strathmann M. P., Gautam N. 1991; Diversity of G proteins in signal transduction. Science 252:802–808
     [Google Scholar]
  40. Sobko A., Ma H., Firtel R. A. 2002; Regulated SUMOylation and ubiquitination of DdMEK1 is required for proper chemotaxis. Dev Cell 2:745–756
     [Google Scholar]
  41. Srinivasan J., Gundersen R. E., Hadwiger J. A. 1999; Activated G α subunits can inhibit multiple signal transduction pathways during dictyostelium development. Dev Biol 215:443–452
     [Google Scholar]
  42. Watts D. J., Ashworth J. M. 1970; Growth of myxameobae of the cellular slime mould Dictyostelium discoideum in axenic culture. Biochem J 119:171–174
     [Google Scholar]
  43. Wilkie T. M., Gilbert D. J., Olsen A. S., Chen X. N., Amatruda T. T., Korenberg J. R., Trask B. J., de Jong P., Reed R. R. other authors 1992; Evolution of the mammalian G protein alpha subunit multigene family. Nat Genet 1:85–91
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.036541-0
Loading
Gα5 subunit-mediated signalling requires a D-motif and the MAPK ERK1 in Dictyostelium
Microbiology 156, 789 (2010); https://doi.org/10.1099/mic.0.036541-0
/content/journal/micro/10.1099/mic.0.036541-0
/content/journal/micro/10.1099/mic.0.036541-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error