Cortical aPKC kinase activity distinguishes neural stem cells from progenitor cells by ensuring asymmetric segregation of Numb

Developmental Biology

Volumn 365, Issue 1, 2012, Pages 219-228

  Haenfler, Jill M ^a   Kuang, Chaoyuan ^a   Lee, Cheng Yu ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Asymmetric division; Cell polarity; Intermediate neural progenitor; Lethal (2) giant larvae; Neuroblast; Numb

Indexed keywords

ACYL COENZYME A; PROTEIN KINASE C;

ARTICLE; BRAIN CORTEX; CELL FATE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE SEGREGATION; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; STEM CELL;

EID: 84862829813     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.02.027     Document Type: Article

References (46)

1. Albertson R., Doe C.Q. Dlg, Scrib and Lgl regulate neuroblast cell size and mitotic spindle asymmetry. Nat. Cell Biol. 2003, 5:166-170.
2. Bayraktar O.A., Boone J.Q., Drummond M.L., Doe C.Q. Drosophila type II neuroblast lineages keep Prospero levels low to generate large clones that contribute to the adult brain central complex. Neural Dev. 2010, 26. Oct 1.
3. Beatty A., Morton D., Kemphues K. The C. elegans homolog of Drosophila Lethal giant larvae functions redundantly with PAR-2 to maintain polarity in the early embryo. Development 2010, 137:3995-4004.
4. Bello B.C., Izergina N., Caussinus E., Reichert H. Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural Dev. 2008, 3.
5. Betschinger J., Mechtler K., Knoblich J.A. The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl. Nature 2003, 422:326-330.
6. Bischof J., Basler K. Recombinases and their use in gene activation, gene inactivation, and transgenesis. Methods Mol. Biol. 2008, 420:175-195.
7. Boone J.Q., Doe C.Q. Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells. Dev. Neurobiol. 2008, 68:1185-1195.
8. Bowman S.K., Rolland V., Betschinger J., Kinsey K.A., Emery G., Knoblich J.A. The tumor suppressors Brat and Numb regulate transit-amplifying neuroblast lineages in Drosophila. Dev. Cell 2008, 14:535-546.
9. Cai Y., Chia W., Yang X. A family of snail-related zinc finger proteins regulates two distinct and parallel mechanisms that mediate Drosophila neuroblast asymmetric divisions. EMBO J. 2001, 20:1704-1714.
10. Chia W., Somers W.G., Wang H. Drosophila neuroblast asymmetric divisions: cell cycle regulators, asymmetric protein localization, and tumorigenesis. J. Cell Biol. 2008, 180:267-272.
11. Chung H.M., Struhl G. Nicastrin is required for Presenilin-mediated transmembrane cleavage in Drosophila. Nat. Cell Biol. 2001, 3:1129-1132.
12. Dho S.E., Trejo J., Siderovski D.P., McGlade C.J. Dynamic regulation of mammalian numb by G protein-coupled receptors and protein kinase C activation: structural determinants of numb association with the cortical membrane. Mol. Biol. Cell 2006, 17:4142-4155.
13. Doe C.Q. Neural stem cells: balancing self-renewal with differentiation. Development 2008, 135:1575-1587.
14. Egger B., Chell J.M., Brand A.H. Insights into neural stem cell biology from flies. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2008, 363:39-56.
15. Frise E., Knoblich J.A., Younger-Shepherd S., Jan L.Y., Jan Y.N. The Drosophila Numb protein inhibits signaling of the Notch receptor during cell-cell interaction in sensory organ lineage. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:11925-11932.
16. Guo M., Jan L.Y., Jan Y.N. Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 1996, 17:27-41.
17. Hirata J., Nakagoshi H., Nabeshima Y., Matsuzaki F. Asymmetric segregation of the homeodomain protein Prospero during Drosophila development. Nature 1995, 377:627-630.
18. Hoege C., Constantinescu A.T., Schwager A., Goehring N.W., Kumar P., Hyman A.A. LGL can partition the cortex of one-cell Caenorhabditis elegans embryos into two domains. Curr. Biol. 2010, 20:1296-1303.
19. Knoblich J.A. Mechanisms of asymmetric stem cell division. Cell 2008, 132:583-597.
20. Knoblich J.A. Asymmetric cell division: recent developments and their implications for tumour biology. Nat. Rev. Mol. Cell Biol. 2010, 11:849-860.
21. Knoblich J.A., Jan L.Y., Jan Y.N. Asymmetric segregation of Numb and Prospero during cell division. Nature 1995, 377:624-627.
22. Knoblich J.A., Jan L.Y., Jan Y.N. The N terminus of the Drosophila Numb protein directs membrane association and actin-dependent asymmetric localization. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:13005-13010.
23. Lee C.Y., Robinson K.J., Doe C.Q. Lgl, Pins and aPKC regulate neuroblast self-renewal versus differentiation. Nature 2006, 439:594-598.
24. Lu B., Rothenberg M., Jan L.Y., Jan Y.N. Partner of Numb colocalizes with Numb during mitosis and directs Numb asymmetric localization in Drosophila neural and muscle progenitors. Cell 1998, 95:225-235.
25. Neumüller R.A., Knoblich J.A. Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev. 2009, 23:2675-2699.
26. Nishimura T., Kaibuchi K. Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev. Cell 2007, 13:15-28.
27. Peng C.Y., Manning L., Albertson R., Doe C.Q. The tumour-suppressor genes lgl and dlg regulate basal protein targeting in Drosophila neuroblasts. Nature 2000, 408:596-600.
28. Pfeiffer B.D., Jenett A., Hammonds A.S., Ngo T.T., Misra S., Murphy C., Scully A., Carlson J.W., Wan K.H., Laverty T.R., Mungall C., Svirskas R., Kadonaga J.T., Doe C.Q., Eisen M.B., Celniker S.E., Rubin G.M. Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:9715-9720.
29. Prehoda K.E. Polarization of Drosophila neuroblasts during asymmetric division. Cold Spring Harb. Perspect. Biol. 2009, 1:a001388. Aug.
30. Rhyu M.S., Jan L.Y., Jan Y.N. Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 1994, 76:477-491.
31. Rolls M.M., Albertson R., Shih H.P., Lee C.Y., Doe C.Q. Drosophila aPKC regulates cell polarity and cell proliferation in neuroblasts and epithelia. J. Cell Biol. 2003, 163:1089-1098.
32. San-Juán B.P., Baonza A. The bHLH factor deadpan is a direct target of Notch signaling and regulates neuroblast self-renewal in Drosophila. Dev. Biol. 2011, 352:70-82.
33. Shen C.P., Jan L.Y., Jan Y.N. Miranda is required for the asymmetric localization of Prospero during mitosis in Drosophila. Cell 1997, 90:449-458.
34. Smith C.A., Lau K.M., Rahmani Z., Dho S.E., Brothers G., She Y.M., Berry D.M., Bonneil E., Thibault P., Schweisguth F., Le Borgne R., McGlade C.J. aPKC-mediated phosphorylation regulates asymmetric membrane localization of the cell fate determinant Numb. EMBO J. 2007, 26:468-480.
35. Song Y., Lu B. Regulation of cell growth by Notch signaling and its differential requirement in normal vs. tumor-forming stem cells in Drosophila. Genes Dev. 2011, 25:2644-2658.
36. Sotillos S., Díaz-Meco M.T., Caminero E., Moscat J., Campuzano S. DaPKC-dependent phosphorylation of Crumbs is required for epithelial cell polarity in Drosophila. J. Cell Biol. 2004, 166:549-557.
37. Spana E.P., Doe C.Q. The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development 1995, 121:3187-3195.
38. Wang H., Somers G.W., Bashirullah A., Heberlein U., Yu F., Chia W. Aurora-A acts as a tumor suppressor and regulates self-renewal of Drosophila neuroblasts. Genes Dev. 2006, 20:3453-3463.
39. Weng M., Golden K.L., Lee C.Y. dFezf/Earmuff maintains the restricted developmental potential of intermediate neural progenitors in Drosophila. Dev. Cell 2010, 18:126-135.
40. Weng M., Haenfler J.M., Lee C.Y. Changes in Notch signaling coordinates maintenance and differentiation of the Drosophila larval optic lobe neuroepithelia. Dev. Neurobiol 2011, 10.1002/dneu.20995.
41. Weng M., Lee C.Y. Keeping neural progenitor cells on a short leash during Drosophila neurogenesis. Curr. Opin. Neurobiol. 2011, 21:36-42.
42. 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 2008, 135:161-173.
43. Yaich L., Ooi J., Park M., Borg J.P., Landry C., Bodmer R., Margolis B. Functional analysis of the Numb phosphotyrosine-binding domain using site-directed mutagenesis. J. Biol. Chem. 1998, 273:10381-10388.
44. Zhong W., Jiang M.M., Weinmaster G., Jan L.Y., Jan Y.N. Differential expression of mammalian Numb, Numblike and Notch1 suggests distinct roles during mouse cortical neurogenesis. Development 1997, 124:1887-1897.
45. Zhou Y., Atkins J.B., Rompani S.B., Bancescu D.L., Petersen P.H., Tang H., Zou K., Stewart S.B., Zhong W. The mammalian Golgi regulates numb signaling in asymmetric cell division by releasing ACBD3 during mitosis. Cell 2007, 129:163-178.
46. Zhu S., Lin S., Kao C.F., Awasaki T., Chiang A.S., Lee T. Gradients of the Drosophila Chinmo BTB-zinc finger protein govern neuronal temporal identity. Cell 2006, 127(2):409-422.