APKC phosphorylates NuMA-related LIN-5 to position the mitotic spindle during asymmetric division

Nature Cell Biology

Volumn 13, Issue 9, 2011, Pages 1132-1140

  Galli, Matilde ^a   Muñoz, Javier ^b,c   Portegijs, Vincent ^a   Boxem, Mike ^a   Grill, Stephan W ^d,e   Heck, Albert J R ^b,c   Van Den Heuvel, Sander ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c Netherlands Proteomics Center   (Netherlands)

^d MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^e MAX PLANCK INSTITUT FÜR PHYSIK KOMPLEXER SYSTEME   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABNORMAL CELL LINEAGE 5 PROTEIN; CELL PROTEIN; GLUTATHIONE TRANSFERASE; NUMA PROTEIN; PROTEIN KINASE C; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE PROGRESSION; CELL DIVISION; CELL MIGRATION; CELL POLARITY; CYTOKINESIS; EMBRYO; ENZYME PHOSPHORYLATION; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; IN VITRO STUDY; MASS SPECTROMETRY; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; QUANTITATIVE ANALYSIS; RNA INTERFERENCE; TELOPHASE;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE PROTEINS; CELL DIVISION; CELL POLARITY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EMBRYO, NONMAMMALIAN; GREEN FLUORESCENT PROTEINS; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MICROSCOPY, CONFOCAL; MITOTIC SPINDLE APPARATUS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR MATRIX-ASSOCIATED PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASE C; RNA INTERFERENCE; SERINE;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 80052494501     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2315     Document Type: Article

References (40)

1. Knoblich, J. A. Asymmetric cell division: recent developments and their implications for tumour biology. Nat. Rev. Mol. Cell Biol. 11, 849-860 (2010).
2. Siller, K. H. & Doe, C. Q. Spindle orientation during asymmetric cell division. Nat. Cell Biol. 11, 365-374 (2009).
3. Galli, M. & van den Heuvel, S. Determination of the cleavage plane in early C. elegans embryos. Annu. Rev. Genet. 42, 389-411 (2008).
4. Srinivasan, D. G., Fisk, R. M., Xu, H. & van den Heuvel, S. A complex of LIN-5 and GPR proteins regulates G protein signaling and spindle function in C. elegans. Genes Dev. 17, 1225-1239 (2003). (Pubitemid 36583166)
5. Colombo, K. et al. Translation of polarity cues into asymmetric spindle positioning in Caenorhabditis elegans embryos. Science 300, 1957-1961 (2003). (Pubitemid 36734605)
6. Gotta, M. et al. Asymmetrically distributed C. elegans homologs of AGS3/PINS control spindle position in the early embryo. Curr. Biol. 13, 1029-1037 (2003). (Pubitemid 36726038)
7. Etemad-Moghadam, B., Guo, S. & Kemphues, K. J. Asymmetrically distributed PAR-3 protein contributes to cell polarity and spindle alignment in early C. elegans embryos. Cell 83, 743-752 (1995).
8. Hung, T. J. & Kemphues, K. J. PAR-6 is a conserved PDZ domain-containing protein that colocalizes with PAR-3 in Caenorhabditis elegans embryos. Development 126, 127-135 (1999). (Pubitemid 29045906)
9. Tabuse, Y. et al. Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development 125, 3607-3614 (1998). (Pubitemid 28469961)
10. Cuenca, A. A. et al. Polarization of the C. elegans zygote proceeds via distinct establishment and maintenance phases. Development 130, 1255-1265 (2003). (Pubitemid 36410775)
11. Boyd, L. et al. PAR-2 is asymmetrically distributed and promotes association of P granules and PAR-1 with the cortex in C. elegans embryos. Development 122, 3075-3084 (1996). (Pubitemid 26371973)
12. Guo, S. & Kemphues, K. J. par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 81, 611-620 (1995).
13. Hao, Y., Boyd, L. & Seydoux, G. Stabilization of cell polarity by the C. elegans RING protein PAR-2. Dev. Cell 10, 199-208 (2006). (Pubitemid 43174953)
14. Grill, S. W., Gonczy, P., Stelzer, E. H. & Hyman, A. A. Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 409, 630-633 (2001). (Pubitemid 32154816)
15. van der Voet, M. et al. NuMA-related LIN-5, ASPM-1, calmodulin and dynein promote meiotic spindle rotation independently of cortical LIN-5/GPR/G. Nat. Cell Biol. 11, 269-277 (2009).
16. Nguyen-Ngoc, T., Afshar, K. & Gonczy, P. Coupling of cortical dynein and Gα proteins mediates spindle positioning in Caenorhabditis elegans. Nat. Cell Biol. 9, 1294-1302 (2007). (Pubitemid 350042361)
17. Bowman, S. K. et al. The Drosophila NuMA homolog Mud regulates spindle orientation in asymmetric cell division. Dev. Cell 10, 731-742 (2006). (Pubitemid 43779107)
18. Du, Q. & Macara, I. G. Mammalian Pins is a conformational switch that links NuMA to heterotrimeric G proteins. Cell 119, 503-516 (2004). (Pubitemid 39482350)
19. Izumi, Y. et al. Drosophila Pins-binding protein Mud regulates spindle-polarity coupling and centrosome organization. Nat. Cell Biol. 8, 586-593 (2006). (Pubitemid 43827351)
20. Siller, K. H., Cabernard, C. & Doe, C. Q. The NuMA-related Mud protein binds Pins and regulates spindle orientation in Drosophila neuroblasts. Nat. Cell Biol. 8, 594-600 (2006). (Pubitemid 43827352)
21. Krijgsveld, J. et al. Metabolic labeling of C. elegans and D. melanogaster for quantitative proteomics. Nat. Biotechnol. 21, 927-931 (2003). (Pubitemid 36936200)
22. Goulding, M. B. et al. Control of nuclear centration in the C. elegans zygote by receptor-independent Gα signaling and myosin II. J. Cell Biol. 178, 1177-1191 (2007). (Pubitemid 47480225)
23. Labbe, J. C., McCarthy, E. K. & Goldstein, B. The forces that position a mitotic spindle asymmetrically are tethered until after the time of spindle assembly. J. Cell Biol. 167, 245-256 (2004). (Pubitemid 39435068)
24. Wirtz-Peitz, F., Nishimura, T. & Knoblich, J. A. Linking cell cycle to asymmetric division: Aurora-A phosphorylates the Par complex to regulate Numb localization. Cell 135, 161-173 (2008).
25. Frokjaer-Jensen, C. et al. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat. Genet. 40, 1375-1383 (2008).
26. Lorson, M. A., Horvitz, H. R. & van den Heuvel, S. LIN-5 is a novel component of the spindle apparatus required for chromosome segregation and cleavage plane specification in Caenorhabditis elegans. J. Cell Biol. 148, 73-86 (2000). (Pubitemid 30046783)
27. Park, D. H. & Rose, L. S. Dynamic localization of LIN-5 and GPR-1/2 to cortical force generation domains during spindle positioning. Dev. Biol. 315, 42-54 (2008).
28. Panbianco, C. et al. A casein kinase 1 and PAR proteins regulate asymmetry of a PIP(2) synthesis enzyme for asymmetric spindle positioning. Dev. Cell 15, 198-208 (2008).
29. Rose, L. S. & Kemphues, K. The let-99 gene is required for proper spindle orientation during cleavage of the C. elegans embryo. Development 125, 1337-1346 (1998). (Pubitemid 28203948)
30. Krueger, L. E., Wu, J. C., Tsou, M. F. & Rose, L. S. LET-99 inhibits lateral posterior pulling forces during asymmetric spindle elongation in C. elegans embryos. J. Cell Biol. 189, 481-495 (2010).
31. Hao, Y. et al. Par3 controls epithelial spindle orientation by aPKC-mediated phosphorylation of apical Pins. Curr. Biol. 20, 1809-1818 (2010).
32. Boxem, M. et al. A protein domain-based interactome network for C. elegans early embryogenesis. Cell 134, 534-545 (2008).
33. Vidal, M. et al. Reverse two-hybrid and one-hybrid systems to detect dissociation of protein-protein and DNA-protein interactions. Proc. Natl Acad. Sci. USA 93, 10315-10320 (1996). (Pubitemid 26314619)
34. Fisk Green, R. et al. Identification of critical domains and putative partners for the Caenorhabditis elegans spindle component LIN-5. Mol. Genet. Genom. 271, 532-544 (2004). (Pubitemid 38916396)
35. Golden, A. et al. Metaphase to anaphase (mat) transition-defective mutants in Caenorhabditis elegans. J. Cell Biol. 151, 1469-1482 (2000). (Pubitemid 32047596)
36. Anderson, D. C., Gill, J. S., Cinalli, R. M. & Nance, J. Polarization of the C. elegans embryo by RhoGAP-mediated exclusion of PAR-6 from cell contacts. Science 320, 1771-1774 (2008). (Pubitemid 351931290)
37. Pinkse, M. W. et al. Highly robust, automated, and sensitive online TiO2-based phosphoproteomics applied to study endogenous phosphorylation in Drosophila melanogaster. J. Proteome Res. 7, 687-697 (2008). (Pubitemid 351294031)
38. Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individu-alized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372 (2008).
39. Olsen, J. V. et al. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648 (2006). (Pubitemid 44647421)
40. Gouw, J. W. et al. In vivo stable isotope labeling of fruit flies reveals post-transcriptional regulation in the maternal-to-zygotic transition. Mol. Cell Proteom. 8, 1566-1578 (2009).