The Rap1-Rgl-Ral signaling network regulates neuroblast cortical polarity and spindle orientation

Journal of Cell Biology

Volumn 195, Issue 4, 2011, Pages 553-562

  Carmena, Ana ^a   Makarova, Aljona ^a   Speicher, Stephan ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PAR6 PROTEIN; PDZ PROTEIN; PROTEIN KINASE C; RAL PROTEIN; RAP1 PROTEIN; RAS PROTEIN; RGL PROTEIN; UNCLASSIFIED DRUG;

ANAPHASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIVISION; CELL FATE; CELL POLARITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; EMBRYO; GAIN OF FUNCTION MUTATION; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; METAPHASE; MITOSIS; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SPINDLE CELL;

ANIMALS; CELL POLARITY; DROSOPHILA MELANOGASTER; FEMALE; MALE; MITOTIC SPINDLE APPARATUS; NEURAL STEM CELLS; RAL GTP-BINDING PROTEINS; RAL GUANINE NUCLEOTIDE EXCHANGE FACTOR; RAP1 GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

BASIDIOMYCOTA; DROSOPHILA MELANOGASTER; VERTEBRATA;

EID: 81355147419     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201108112     Document Type: Article

References (50)

1. Asha, H., N.D. de Ruiter, M.G. Wang, and I.K. Hariharan. 1999. The Rap1 GTPase functions as a regulator of morphogenesis in vivo. EMBO J. 18:605-615. http://dx.doi.org/10.1093/emboj/18.3.605
2. Boettner, B., E.E. Govek, J. Cross, and L. Van Aelst. 2000. The junctional multidomain protein AF-6 is a binding partner of the Rap1A GTPase and associates with the actin cytoskeletal regulator profilin. Proc. Natl. Acad. Sci. USA. 97:9064-9069. http://dx.doi.org/10.1073/pnas.97.16.9064
3. Boettner, B., P. Harjes, S. Ishimaru, M. Heke, H.Q. Fan, Y. Qin, L. Van Aelst, and U. Gaul. 2003. The AF-6 homolog canoe acts as a Rap1 effector during dorsal closure of the Drosophila embryo. Genetics. 165:159-169.
4. Bowman, S.K., R.A. Neumüller, M. Novatchkova, Q. Du, and J.A. Knoblich. 2006. The Drosophila NuMA Homolog Mud regulates spindle orientation in asymmetric cell division. Dev. Cell. 10:731-742. http://dx.doi.org/10.1016/j.devcel.2006.05.005
5. Broadus, J., J.B. Skeath, E.P. Spana, T. Bossing, G. Technau, and C.Q. Doe. 1995. New neuroblast markers and the origin of the aCC/pCC neurons in the Drosophila central nervous system. Mech. Dev. 53:393-402. http://dx.doi.org/10.1016/0925-4773(95)00454-8
6. Cabernard, C., and C.Q. Doe. 2009. Apical/basal spindle orientation is required for neuroblast homeostasis and neuronal differentiation in Drosophila. Dev. Cell. 17:134-141. http://dx.doi.org/10.1016/j.devcel.2009.06.009
7. Cai, Y., F. Yu, S. Lin, W. Chia, and X. Yang. 2003. Apical complex genes control mitotic spindle geometry and relative size of daughter cells in Drosophila neuroblast and pI asymmetric divisions. Cell. 112:51-62. http://dx.doi.org/10.1016/S0092-8674(02)01170-4
8. Caron, E. 2003. Cellular functions of the Rap1 GTP-binding protein: a pattern emerges. J. Cell Sci. 116:435-440. http://dx.doi.org/10.1242/jcs.00238
9. Chia, W., W.G. Somers, and H. Wang. 2008. Drosophila neuroblast asymmetric divisions: cell cycle regulators, asymmetric protein localization, and tumorigenesis. J. Cell Biol. 180:267-272. http://dx.doi.org/ 10.1083/jcb.200708159
10. Doe, C.Q. 2008. Neural stem cells: balancing self-renewal with differentiation. Development. 135:1575-1587. http://dx.doi.org/10.1242/dev.014977
11. Frasch, M., T. Hoey, C. Rushlow, H. Doyle, and M. Levine. 1987. Characterization and localization of the even-skipped protein of Drosophila. EMBO J. 6:749-759.
12. Hariharan, I.K., R.W. Carthew, and G.M. Rubin. 1991. The Drosophila roughened mutation: activation of a rap homolog disrupts eye development and interferes with cell determination. Cell. 67:717-722. http://dx.doi.org/10.1016/0092-8674(91)90066-8
13. Hirata, J., H. Nakagoshi, Y. Nabeshima, and F. Matsuzaki. 1995. Asymmetric segregation of the homeodomain protein Prospero during Drosophila development. Nature. 377:627-630. http://dx.doi.org/10.1038/377627a0
14. Ikeshima-Kataoka, H., J.B. Skeath, Y. Nabeshima, C.Q. Doe, and F. Matsuzaki. 1997. Miranda directs Prospero to a daughter cell during Drosophila asymmetric divisions. Nature. 390:625-629. http://dx.doi.org/10.1038/37641
15. Izumi, Y., N. Ohta, K. Hisata, T. Raabe, and F. Matsuzaki. 2006. Drosophila Pins-binding protein Mud regulates spindle-polarity coupling and centrosome organization. Nat. Cell Biol. 8:586-593. http://dx.doi.org/10.1038/ncb1409
16. Johnston, C.A., K. Hirono, K.E. Prehoda, and C.Q. Doe. 2009. Identification of an Aurora-A/PinsLINKER/Dlg spindle orientation pathway using induced cell polarity in S2 cells. Cell. 138:1150-1163. http://dx.doi.org/10.1016/j.cell.2009.07.041
17. Knoblich, J.A. 2008. Mechanisms of asymmetric stem cell division. Cell. 132:583-597. http://dx.doi.org/10.1016/j.cell.2008.02.007
18. Knoblich, J.A., L.Y. Jan, and Y.N. Jan. 1995. Asymmetric segregation of Numb and Prospero during cell division. Nature. 377:624-627. http://dx.doi.org/10.1038/377624a0
19. Knox, A.L., and N.H. Brown. 2002. Rap1 GTPase regulation of adherens junction positioning and cell adhesion. Science. 295:1285-1288. http://dx.doi.org/10.1126/science.1067549
20. Kooistra, M.R., N. Dubé, and J.L. Bos. 2007. Rap1: a key regulator in cellcell junction formation. J. Cell Sci. 120:17-22. http://dx.doi.org/10.1242/jcs.03306
21. Martín-Bermudo, M.D., C. Martínez, A. Rodríguez, and F. Jiménez. 1991. Distribution and function of the lethal of scute gene product during early neurogenesis in Drosophila. Development. 113:445-454.
22. Mirey, G., M. Balakireva, S. L'Hoste, C. Rossé, S. Voegeling, and J. Camonis. 2003. A Ral guanine exchange factor-Ral pathway is conserved in Drosophila melanogaster and sheds new light on the connectivity of the Ral, Ras, and Rap pathways. Mol. Cell. Biol. 23:1112-1124. http://dx.doi.org/10.1128/MCB.23.3.1112-1124.2003
23. Miyamoto, H., I. Nihonmatsu, S. Kondo, R. Ueda, S. Togashi, K. Hirata, Y. Ikegami, and D. Yamamoto. 1995. canoe encodes a novel protein containing a GLGF/DHR motif and functions with Notch and scabrous in common developmental pathways in Drosophila. Genes Dev. 9:612-625. http://dx.doi.org/10.1101/gad.9.5.612
24. Morrison, S.J., and A.C. Spradling. 2008. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell. 132:598-611. http://dx.doi.org/10.1016/j.cell.2008.01.038
25. Moskalenko, S., D.O. Henry, C. Rosse, G. Mirey, J.H. Camonis, and M.A. White. 2001. The exocyst is a Ral effector complex. Nat. Cell Biol. 4:66-72. http://dx.doi.org/10.1038/ncb728
26. Nipper, R.W., K.H. Siller, N.R. Smith, C.Q. Doe, and K.E. Prehoda. 2007. Galphai generates multiple Pins activation states to link cortical polarity and spindle orientation in Drosophila neuroblasts. Proc. Natl. Acad. Sci. USA. 104:14306-14311. http://dx.doi.org/10.1073/pnas.0701812104
27. O'Keefe, D.D., E. Gonzalez-Niño, M. Burnett, L. Dylla, S.M. Lambeth, E. Licon, C. Amesoli, B.A. Edgar, and J. Curtiss. 2009. Rap1 maintains adhesion between cells to affect Egfr signaling and planar cell polarity in Drosophila. Dev. Biol. 333:143-160. http://dx.doi.org/10.1016/j.ydbio.2009.06.032
28. Parmentier, M.L., D. Woods, S. Greig, P.G. Phan, A. Radovic, P. Bryant, and C.J. O'Kane. 2000. Rapsynoid/partner of inscuteable controls asymmetric division of larval neuroblasts in Drosophila. J. Neurosci. 20:RC84.
29. Price, L.S., A. Hajdo-Milasinovic, J. Zhao, F.J. Zwartkruis, J.G. Collard, and J.L. Bos. 2004. Rap1 regulates E-cadherin-mediated cell-cell adhesion. J. Biol. Chem. 279:35127-35132. http://dx.doi.org/10.1074/jbc.M404917200
30. Rhyu, M.S., L.Y. Jan, and Y.N. Jan. 1994. Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell. 76:477-491. http://dx.doi.org/10.1016/0092-8674(94)90112-0
31. Schaefer, M., A. Shevchenko, A. Shevchenko, and J.A. Knoblich. 2000. A protein complex containing Inscuteable and the Galpha-binding protein Pins orients asymmetric cell divisions in Drosophila. Curr. Biol. 10:353-362. http://dx.doi.org/10.1016/S0960-9822(00)00401-2
32. Schober, M., M. Schaefer, and J.A. Knoblich. 1999. Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts. Nature. 402:548-551. http://dx.doi.org/10.1038/990135
33. Schuldt, A.J., J.H. Adams, C.M. Davidson, D.R. Micklem, J. Haseloff, D. St Johnston, and A.H. Brand. 1998. Miranda mediates asymmetric protein and RNA localization in the developing nervous system. Genes Dev. 12:1847-1857. http://dx.doi.org/10.1101/gad.12.12.1847
34. Schwamborn, J.C., and A.W. Püschel. 2004. The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat. Neurosci. 7:923-929. http://dx.doi.org/10.1038/nn1295
35. Shen, C.P., L.Y. Jan, and Y.N. Jan. 1997. Miranda is required for the asymmetric localization of Prospero during mitosis in Drosophila. Cell. 90:449-458. http://dx.doi.org/10.1016/S0092-8674(00)80505-X
36. Siegrist, S.E., and C.Q. Doe. 2005. Microtubule-induced Pins/Galphai cortical polarity in Drosophila neuroblasts. Cell. 123:1323-1335. http://dx.doi.org/10.1016/j.cell.2005.09.043
37. Siegrist, S.E., and C.Q. Doe. 2006. Extrinsic cues orient the cell division axis in Drosophila embryonic neuroblasts. Development. 133:529-536. http://dx.doi.org/10.1242/dev.02211
38. Siller, K.H., and C.Q. Doe. 2009. Spindle orientation during asymmetric cell division. Nat. Cell Biol. 11:365-374. http://dx.doi.org/10.1038/ncb0409-365
39. Siller, K.H., C. Cabernard, and C.Q. Doe. 2006. The NuMA-related Mud protein binds Pins and regulates spindle orientation in Drosophila neuroblasts. Nat. Cell Biol. 8:594-600. http://dx.doi.org/10.1038/ncb1412
40. Spana, E.P., and C.Q. Doe. 1995. The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development. 121:3187-3195.
41. Speicher, S., L. García-Alonso, A. Carmena, M.D. Martín-Bermudo, S. de la Escalera, and F. Jiménez. 1998. Neurotactin functions in concert with other identified CAMs in growth cone guidance in Drosophila. Neuron. 20:221-233. http://dx.doi.org/10.1016/S0896-6273(00)80451-1
42. Speicher, S., A. Fischer, J. Knoblich, and A. Carmena. 2008. The PDZ protein Canoe regulates the asymmetric division of Drosophila neuroblasts and muscle progenitors. Curr. Biol. 18:831-837. http://dx.doi.org/10.1016/j.cub.2008.04.072
43. Tepass, U. 1996. Crumbs, a component of the apical membrane, is required for zonula adherens formation in primary epithelia of Drosophila. Dev. Biol. 177:217-225. http://dx.doi.org/10.1006/dbio.1996.0157
44. Wang, H., S.R. Singh, Z. Zheng, S.W. Oh, X. Chen, K. Edwards, and S.X. Hou. 2006. Rap-GEF signaling controls stem cell anchoring to their niche through regulating DE-cadherin-mediated cell adhesion in the Drosophila testis. Dev. Cell. 10:117-126. http://dx.doi.org/10.1016/j.devcel.2005.11.004
45. Wirtz-Peitz, F., T. Nishimura, and J.A. Knoblich. 2008. Linking cell cycle to asymmetric division: Aurora-A phosphorylates the Par complex to regulate Numb localization. Cell. 135:161-173. http://dx.doi.org/10.1016/j.cell.2008.07.049
46. Wodarz, A., and W.B. Huttner. 2003. Asymmetric cell division during neurogenesis in Drosophila and vertebrates. Mech. Dev. 120:1297-1309. http://dx.doi.org/10.1016/j.mod.2003.06.003
47. Wodarz, A., A. Ramrath, U. Kuchinke, and E. Knust. 1999. Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature. 402:544-547. http://dx.doi.org/10.1038/990128
48. Wodarz, A., A. Ramrath, A. Grimm, and E. Knust. 2000. Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J. Cell Biol. 150:1361-1374. http://dx.doi.org/10.1083/jcb.150.6.1361
49. Yaffe, M.B., G.G. Leparc, J. Lai, T. Obata, S. Volinia, and L.C. Cantley. 2001. A motif-based profile scanning approach for genome-wide prediction of signaling pathways. Nat. Biotechnol. 19:348-353. http://dx.doi.org/10.1038/86737
50. Yu, F., X. Morin, Y. Cai, X. Yang, and W. Chia. 2000. Analysis of partner of inscuteable, a novel player of Drosophila asymmetric divisions, reveals two distinct steps in inscuteable apical localization. Cell. 100:399-409. http://dx.doi.org/10.1016/S0092-8674(00)80676-5