Polarity mediates asymmetric trafficking of the Gβ heterotrimeric G-protein subunit GPB-1 in C. elegans embryos

Development

Volumn 138, Issue 13, 2011, Pages 2773-2782

  Thyagarajan, Kalyani ^a   Afshar, Katayoun ^a   Gönczy, Pierre ^a  

^a EPFL   (Switzerland)

Author keywords

Asymmetric spindle positioning; C. elegans; Endosomes; Heterotrimeric G proteins; Intracellular trafficking

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; DYNAMIN; G BETA HETEROTRIMERIC G PROTEIN SUBUNIT GPB 1; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 1; G PROTEIN COUPLED RECEPTOR 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CELL CYCLE; CELL DIVISION; CELL MEMBRANE; CELL POLARITY; CONTROLLED STUDY; EMBRYO; ENDOSOME; MALE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SPINDLE CELL;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE; CELL POLARITY; EMBRYO, NONMAMMALIAN; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GTP-BINDING PROTEIN BETA SUBUNITS; MITOSIS; PROTEIN TRANSPORT;

CAENORHABDITIS ELEGANS;

EID: 79958118138     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.063354     Document Type: Article

References (42)

1. Afshar, K., Willard, F. S., Colombo, K., Johnston, C. A., McCudden, C. R., Siderovski, D. P. and Gönczy, P. (2004). RIC-8 is required for GPR-1/2-dependent Galpha function during asymmetric division of C. elegans embryos. Cell 119, 219-230.
2. Afshar, K., Willard, F. S., Colombo, K., Siderovski, D. P. and Gönczy, P. (2005). Cortical localization of the Galpha protein GPA-16 requires RIC-8 function during C. elegans asymmetric cell division. Development 132, 4449-4459.
3. Afshar, K., Werner, M. E., Tse, Y. C., Glotzer, M. and Gönczy, P. (2010). Regulation of cortical contractility and spindle positioning by the protein phosphatase 6 PPH-6 in one-cell stage C. elegans embryos. Development 137, 237-247.
4. Allen, J. A., Yu, J. Z., Donati, R. J. and Rasenick, M. M. (2005). Betaadrenergic receptor stimulation promotes G alpha s internalization through lipid rafts: a study in living cells. Mol. Pharmacol. 67, 1493-1504.
5. Andrews, R. and Ahringer, J. (2007). Asymmetry of early endosome distribution in C. elegans embryos. PLoS ONE 2, e493.
6. Audhya, A., Desai, A. and Oegema, K. (2007). A role for Rab5 in structuring the endoplasmic reticulum. J. Cell Biol. 178, 43-56.
7. Balklava, Z., Pant, S., Fares, H. and Grant, B. D. (2007). Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat. Cell Biol. 9, 1066-1073.
8. Bellanger, J. M. and Gönczy, P. (2003). TAC-1 and ZYG-9 form a complex that promotes microtubule assembly in C. elegans embryos. Curr. Biol. 13, 1488-1498.
9. Boucrot, E. and Kirchhausen, T. (2007). Endosomal recycling controls plasma membrane area during mitosis. Proc. Natl. Acad. Sci. USA 104, 7939-7944.
10. Cheng, N. N., Kirby, C. M. and Kemphues, K. J. (1995). Control of cleavage spindle orientation in Caenorhabditis elegans: the role of the genes par-2 and par-3. Genetics 139, 549-559.
11. Chisari, M., Saini, D. K., Kalyanaraman, V. and Gautam, N. (2007). Shuttling of G protein subunits between the plasma membrane and intracellular membranes. J. Biol. Chem. 282, 24092-24098.
12. Clark, S. G., Shurland, D. L., Meyerowitz, E. M., Bargmann, C. I. and van der Bliek, A. M. (1997). A dynamin GTPase mutation causes a rapid and reversible temperature-inducible locomotion defect in C. elegans. Proc. Natl. Acad. Sci. USA 94, 10438-10443.
13. Colombo, K., Grill, S. W., Kimple, R. J., Willard, F. S., Siderovski, D. P. and Gönczy, P. (2003). Translation of polarity cues into asymmetric spindle positioning in Caenorhabditis elegans embryos. Science 300, 1957-1961.
14. Coumailleau, F., Furthauer, M., Knoblich, J. A. and Gonzalez-Gaitan, M. (2009). Directional Delta and Notch trafficking in Sara endosomes during asymmetric cell division. Nature 458, 1051-1055.
15. Couwenbergs, C., Labbe, J. C., Goulding, M., Marty, T., Bowerman, B. and Gotta, M. (2007). Heterotrimeric G protein signaling functions with dynein to promote spindle positioning in C. elegans. J. Cell Biol. 179, 15-22.
16. Damke, H., Baba, T., van der Bliek, A. M. and Schmid, S. L. (1995). Clathrinindependent pinocytosis is induced in cells overexpressing a temperaturesensitive mutant of dynamin. J. Cell Biol. 131, 69-80.
17. Emery, G., Hutterer, A., Berdnik, D., Mayer, B., Wirtz-Peitz, F., Gaitan, M. G. and Knoblich, J. A. (2005). Asymmetric Rab 11 endosomes regulate delta recycling and specify cell fate in the Drosophila nervous system. Cell 122, 763-773.
18. Garcia-Regalado, A., Guzman-Hernandez, M. L., Ramirez-Rangel, I., Robles-Molina, E., Balla, T., Vazquez-Prado, J. and Reyes-Cruz, G. (2008). G protein-coupled receptor-promoted trafficking of Gbeta1gamma2 leads to AKT activation at endosomes via a mechanism mediated by Gbeta1gamma2-Rab11a interaction. Mol. Biol. Cell 19, 4188-4200.
19. Gönczy, P. (2008). Mechanisms of asymmetric cell division: flies and worms pave the way. Nat. Rev. Mol. Cell Biol. 9, 355-366.
20. Gönczy, P., Echeverri, C., Oegema, K., Coulson, A., Jones, S. J., Copley, R. R., Duperon, J., Oegema, J., Brehm, M., Cassin, E. et al. (2000). Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 408, 331-336.
21. Gotta, M. and Ahringer, J. (2001). Distinct roles for Galpha and Gbetagamma in regulating spindle position and orientation in Caenorhabditis elegans embryos. Nat. Cell Biol. 3, 297-300.
22. Gotta, M., Dong, Y., Peterson, Y. K., Lanier, S. M. and Ahringer, J. (2003). Asymmetrically distributed C. elegans homologs of AGS3/PINS control spindle position in the early embryo. Curr. Biol. 13, 1029-1037.
23. Grill, S. W., Gönczy, P., Stelzer, E. H. and Hyman, A. A. (2001). Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 409, 630-633.
24. Grill, S. W., Howard, J., Schaffer, E., Stelzer, E. H. and Hyman, A. A. (2003). The distribution of active force generators controls mitotic spindle position. Science 301, 518-521.
25. Hutterer, A. and Knoblich, J. A. (2005). Numb and alpha-Adaptin regulate Sanpodo endocytosis to specify cell fate in Drosophila external sensory organs. EMBO Rep. 6, 836-842.
26. Hynes, T. R., Mervine, S. M., Yost, E. A., Sabo, J. L. and Berlot, C. H. (2004). Live cell imaging of Gs and the beta2-adrenergic receptor demonstrates that both alphas and beta1gamma7 internalize upon stimulation and exhibit similar trafficking patterns that differ from that of the beta2-adrenergic receptor. J. Biol. Chem. 279, 44101-44112.
27. Knoblich, J. A. (2008). Mechanisms of asymmetric stem cell division. Cell 132, 583-597.
28. Marrari, Y., Crouthamel, M., Irannejad, R. and Wedegaertner, P. B. (2007). Assembly and trafficking of heterotrimeric G proteins. Biochemistry 46, 7665-7677.
29. Nakayama, Y., Shivas, J. M., Poole, D. S., Squirrell, J. M., Kulkoski, J. M., Schleede, J. B. and Skop, A. R. (2009). Dynamin participates in the maintenance of anterior polarity in the Caenorhabditis elegans embryo. Dev. Cell 16, 889-900.
30. Nguyen-Ngoc, T., Afshar, K. and Gönczy, P. (2007). Coupling of cortical dynein and G alpha proteins mediates spindle positioning in Caenorhabditis elegans. Nat. Cell Biol. 9, 1294-1302.
31. Panbianco, C., Weinkove, D., Zanin, E., Jones, D., Divecha, N., Gotta, M. and Ahringer, J. (2008). A casein kinase 1 and PAR proteins regulate asymmetry of a PIP(2) synthesis enzyme for asymmetric spindle positioning. Dev. Cell 15, 198-208.
32. Park, D. H. and Rose, L. S. (2008). Dynamic localization of LIN-5 and GPR-1/2 to cortical force generation domains during spindle positioning. Dev. Biol. 315, 42-54.
33. Praefcke, G. J. and McMahon, H. T. (2004). The dynamin superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell Biol. 5, 133-147.
34. Praitis, V., Casey, E., Collar, D. and Austin, J. (2001). Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157, 1217-1226.
35. Saini, D. K., Kalyanaraman, V., Chisari, M. and Gautam, N. (2007). A family of G protein betagamma subunits translocate reversibly from the plasma membrane to endomembranes on receptor activation. J. Biol. Chem. 282, 24099-24108.
36. Sato, M., Sato, K., Liou, W., Pant, S., Harada, A. and Grant, B. D. (2008). Regulation of endocytic recycling by C. elegans Rab35 and its regulator RME-4, a coated-pit protein. EMBO J. 27, 1183-1196.
37. Srinivasan, D. G., Fisk, R. M., Xu, H. and van den Heuvel, S. (2003). A complex of LIN-5 and GPR proteins regulates G protein signaling and spindle function in C elegans. Genes Dev. 17, 1225-1239.
38. Thompson, H. M., Skop, A. R., Euteneuer, U., Meyer, B. J. and McNiven, M. A. (2002). The large GTPase dynamin associates with the spindle midzone and is required for cytokinesis. Curr. Biol. 12, 2111-2117.
39. Timmons, L. and Fire, A. (1998). Specific interference by ingested dsRNA. Nature 395, 854.
40. Tsou, M. F., Hayashi, A. and Rose, L. S. (2003). LET-99 opposes Galpha/GPR signaling to generate asymmetry for spindle positioning in response to PAR and MES-1/SRC-1 signaling. Development 130, 5717-5730.
41. Vida, T. A. and Emr, S. D. (1995). A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128, 779-792.
42. Zwaal, R. R., Ahringer, J., van Luenen, H. G., Rushforth, A., Anderson, P. and Plasterk, R. H. (1996). G proteins are required for spatial orientation of early cell cleavages in C. elegans embryos. Cell 86, 619-629.