Tre1 GPCR Signaling Orients Stem Cell Divisions in the Drosophila Central Nervous System

Developmental Cell

Volumn 22, Issue 1, 2012, Pages 79-91

  Yoshiura, Shigeki ^a   Ohta, Nao ^a   Matsuzaki, Fumio ^a  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; PROTEIN TRE1; UNCLASSIFIED DRUG;

ARTICLE; CELL DIVISION; CELL POLARITY; CENTRAL NERVOUS SYSTEM; CENTROSOME; CONTROLLED STUDY; DROSOPHILA; EMBRYO CELL; EMBRYO DEVELOPMENT; EPITHELIUM; GLIA CELL; IMMUNOHISTOCHEMISTRY; NERVE CELL; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SPINDLE CELL; TISSUE GROWTH; WILD TYPE;

ANIMALS; BLOTTING, WESTERN; CELL DIVISION; CELL POLARITY; CELLS, CULTURED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EPITHELIAL CELLS; GTP-BINDING PROTEIN ALPHA SUBUNITS; IMMUNOENZYME TECHNIQUES; IMMUNOPRECIPITATION; MITOTIC SPINDLE APPARATUS; NEURONS; PEPTIDYLPROLYL ISOMERASE; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, G-PROTEIN-COUPLED; RNA, MESSENGER; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 84855976278     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2011.10.027     Document Type: Article

References (75)

1. Awasaki T., Lai S.L., Ito K., Lee T. Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J.Neurosci. 2008, 28:13742-13753.
2. Baena-López L.A., Baonza A., García-Bellido A. The orientation of cell divisions determines the shape of Drosophila organs. Curr. Biol. 2005, 15:1640-1644.
3. Bai J., Chiu W., Wang J., Tzeng T., Perrimon N., Hsu J. The cell adhesion molecule Echinoid defines a new pathway that antagonizes the Drosophila EGF receptor signaling pathway. Development 2001, 128:591-601.
4. Bellaïche Y., Gho M., Kaltschmidt J.A., Brand A.H., Schweisguth F. Frizzled regulates localization of cell-fate determinants and mitotic spindle rotation during asymmetric cell division. Nat. Cell Biol. 2001, 3:50-57.
5. Bellaïche Y., Radovic A., Woods D.F., Hough C.D., Parmentier M.L., O'Kane C.J., Bryant P.J., Schweisguth F. The Partner of Inscuteable/Discs-large complex is required to establish planar polarity during asymmetric cell division in Drosophila. Cell 2001, 106:355-366.
6. Betschinger J., Mechtler K., Knoblich J.A. Asymmetric segregation of the tumor suppressor brat regulates self-renewal in Drosophila neural stem cells. Cell 2006, 124:1241-1253.
7. Bossing T., Udolph G., Doe C.Q., Technau G.M. The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev. Biol. 1996, 179:41-64.
8. Bowman S.K., Neumüller R.A., Novatchkova M., Du Q., Knoblich J.A. The Drosophila NuMA Homolog Mud regulates spindle orientation in asymmetric cell division. Dev. Cell 2006, 10:731-742.
9. David N.B., Martin C.A., Segalen M., Rosenfeld F., Schweisguth F., Bellaïche Y. Drosophila Ric-8 regulates Galphai cortical localization to promote Galphai-dependent planar orientation of the mitotic spindle during asymmetric cell division. Nat. Cell Biol. 2005, 7:1083-1090.
10. Dumstrei K., Wang F., Hartenstein V. Role of DE-cadherin in neuroblast proliferation, neural morphogenesis, and axon tract formation in Drosophila larval brain development. J.Neurosci. 2003, 23:3325-3335.
11. Egger-Adam D., Katanaev V.L. The trimeric G protein Go inflicts a double impact on axin in the Wnt/frizzled signaling pathway. Dev. Dyn. 2010, 239:168-183.
12. Fischer E., Legue E., Doyen A., Nato F., Nicolas J.F., Torres V., Yaniv M., Pontoglio M. Defective planar cell polarity in polycystic kidney disease. Nat. Genet. 2006, 38:21-23.
13. Foe V.E. Mitotic domains reveal early commitment of cells in Drosophila embryos. Development 1989, 107:1-22.
14. Gho M., Schweisguth F. Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila. Nature 1998, 393:178-181.
15. Guillén A., Jallon J.M., Fehrentz J.A., Pantaloni C., Bockaert J., Homburger V. A Go-like protein in Drosophila melanogaster and its expression in memory mutants. EMBO J. 1990, 9:1449-1455.
16. Halter D.A., Urban J., Rickert C., Ner S.S., Ito K., Travers A.A., Technau G.M. The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 1995, 121:317-332.
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. Hoyle G. Glial cells of an insect ganglion. J.Comp. Neurol. 1986, 246:85-103.
19. Ikeshima-Kataoka H., Skeath J.B., Nabeshima Y., Doe C.Q., Matsuzaki F. Miranda directs Prospero to a daughter cell during Drosophila asymmetric divisions. Nature 1997, 390:625-629.
20. Isshiki T., Pearson B., Holbrook S., Doe C.Q. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 2001, 106:511-521.
21. Ito K., Urban J., Technau G. Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Roux's Arch. Dev. Biol. 1995, 204:284-307.
22. Izumi Y., Ohta N., Hisata K., Raabe T., Matsuzaki F. Drosophila Pins-binding protein Mud regulates spindle-polarity coupling and centrosome organization. Nat. Cell Biol. 2006, 8:586-593.
23. Januschke J., Gonzalez C. The interphase microtubule aster is a determinant of asymmetric division orientation in Drosophila neuroblasts. J.Cell Biol. 2010, 188:693-706.
24. Johnston C.A., Hirono K., Prehoda K.E., Doe C.Q. Identification of an Aurora-A/PinsLINKER/Dlg spindle orientation pathway using induced cell polarity in S2 cells. Cell 2009, 138:1150-1163.
25. Kaltschmidt J.A., Davidson C.M., Brown N.H., Brand A.H. Rotation and asymmetry of the mitotic spindle direct asymmetric cell division in the developing central nervous system. Nat. Cell Biol. 2000, 2:7-12.
26. Kamps A.R., Pruitt M.M., Herriges J.C., Coffman C.R. An evolutionarily conserved arginine is essential for Tre1G protein-coupled receptor function during germ cell migration in Drosophila melanogaster. PLoS ONE 2010, 5:e11839.
27. Katanaev V.L., Ponzielli R., Sémériva M., Tomlinson A. Trimeric G protein-dependent frizzled signaling in Drosophila. Cell 2005, 120:111-122.
28. Klein R.S., Rubin J.B. Immune and nervous system CXCL12 and CXCR4: parallel roles in patterning and plasticity. Trends Immunol. 2004, 25:306-314.
29. Knoblich J.A. Asymmetric cell division during animal development. Nat. Rev. Mol. Cell Biol. 2001, 2:11-20.
30. Knoblich J.A. Mechanisms of asymmetric stem cell division. Cell 2008, 132:583-597.
31. Knoblich J.A., Jan L.Y., Jan Y.N. Asymmetric segregation of Numb and Prospero during cell division. Nature 1995, 377:624-627.
32. Konno D., Shioi G., Shitamukai A., Mori A., Kiyonari H., Miyata T., Matsuzaki F. Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat. Cell Biol. 2008, 10:93-101.
33. Kopein D., Katanaev V.L. Drosophila GoLoco-protein Pins is a target of Galpha(o)-mediated G protein-coupled receptor signaling. Mol. Biol. Cell 2009, 20:3865-3877.
34. Kraut R., Chia W., Jan L.Y., Jan Y.N., Knoblich J.A. Role of inscuteable in orienting asymmetric cell divisions in Drosophila. Nature 1996, 383:50-55.
35. Kunwar P.S., Starz-Gaiano M., Bainton R.J., Heberlein U., Lehmann R. Tre1, a G protein-coupled receptor, directs transepithelial migration of Drosophila germ cells. PLoS Biol. 2003, 1:E80.
36. Kunwar P.S., Sano H., Renault A.D., Barbosa V., Fuse N., Lehmann R. Tre1 GPCR initiates germ cell transepithelial migration by regulating Drosophila melanogaster E-cadherin. J.Cell Biol. 2008, 183:157-168.
37. Landgraf M., Jeffrey V., Fujioka M., Jaynes J.B., Bate M. Embryonic origins of a motor system: motor dendrites form a myotopic map in Drosophila. PLoS Biol. 2003, 1:E41.
38. 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.
39. Lundell M.J., Hirsh J. eagle is required for the specification of serotonin neurons and other neuroblast 7-3 progeny in the Drosophila CNS. Development 1998, 125:463-472.
40. Meng J., Glick J.L., Polakis P., Casey P.J. Functional interaction between Galpha(z) and Rap1GAP suggests a novel form of cellular cross-talk. J.Biol. Chem. 1999, 274:36663-36669.
41. Morin X., Jaouen F., Durbec P. Control of planar divisions by the G-protein regulator LGN maintains progenitors in the chick neuroepithelium. Nat. Neurosci. 2007, 10:1440-1448.
42. Moss J., Vaughan M. ADP-ribosylation of guanyl nucleotide-binding regulatory proteins by bacterial toxins. Adv. Enzymol. Relat. Areas Mol. Biol. 1988, 61:303-379.
43. Nipper R.W., Siller K.H., Smith N.R., Doe C.Q., Prehoda K.E. Galphai generates multiple Pins activation states to link cortical polarity and spindle orientation in Drosophila neuroblasts. Proc. Natl. Acad. Sci. USA 2007, 104:14306-14311.
44. Ogawa H., Ohta N., Moon W., Matsuzaki F. Protein phosphatase 2A negatively regulates aPKC signaling by modulating phosphorylation of Par-6 in Drosophila neuroblast asymmetric divisions. J.Cell Sci. 2009, 122:3242-3249.
45. Parmentier M.L., Woods D., Greig S., Phan P.G., Radovic A., Bryant P., O'Kane C.J. Rapsynoid/partner of inscuteable controls asymmetric division of larval neuroblasts in Drosophila. J.Neurosci. 2000, 20:RC84.
46. Petronczki M., Knoblich J.A. DmPAR-6 directs epithelial polarity and asymmetric cell division of neuroblasts in Drosophila. Nat. Cell Biol. 2001, 3:43-49.
47. Prehoda K.E. Polarization of Drosophila neuroblasts during asymmetric division. Cold Spring Harb. Perspect. Biol. 2009, 1:a001388.
48. Purvanov V., Koval A., Katanaev V.L. A direct and functional interaction between Go and Rab5 during G protein-coupled receptor signaling. Sci. Signal. 2010, 3:ra65.
49. Rebollo E., Roldán M., Gonzalez C. Spindle alignment is achieved without rotation after the first cell cycle in Drosophila embryonic neuroblasts. Development 2009, 136:3393-3397.
50. 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.
51. Schaefer M., Shevchenko A., Shevchenko A., Knoblich J.A. Aprotein complex containing Inscuteable and the Galpha-binding protein Pins orients asymmetric cell divisions in Drosophila. Curr. Biol. 2000, 10:353-362.
52. Schaefer M., Petronczki M., Dorner D., Forte M., Knoblich J.A. Heterotrimeric G proteins direct two modes of asymmetric cell division in the Drosophila nervous system. Cell 2001, 107:183-194.
53. Schober M., Schaefer M., Knoblich J.A. Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts. Nature 1999, 402:548-551.
54. Schuster C.M., Davis G.W., Fetter R.D., Goodman C.S. Genetic dissection of structural and functional components of synaptic plasticity. I.Fasciclin II controls synaptic stabilization and growth. Neuron 1996, 17:641-654.
55. Segalen M., Bellaïche Y. Cell division orientation and planar cell polarity pathways. Semin. Cell Dev. Biol. 2009, 20:972-977.
56. Ségalen M., Johnston C.A., Martin C.A., Dumortier J.G., Prehoda K.E., David N.B., Doe C.Q., Bellaïche Y. The Fz-Dsh planar cell polarity pathway induces oriented cell division via Mud/NuMA in Drosophila and zebrafish. Dev. Cell 2010, 19:740-752.
57. 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.
58. Siegrist S.E., Doe C.Q. Microtubule-induced Pins/Galphai cortical polarity in Drosophila neuroblasts. Cell 2005, 123:1323-1335.
59. Siegrist S.E., Doe C.Q. Extrinsic cues orient the cell division axis in Drosophila embryonic neuroblasts. Development 2006, 133:529-536.
60. 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. 2006, 8:594-600.
61. Skene J.H., Virág I. Posttranslational membrane attachment and dynamic fatty acylation of a neuronal growth cone protein, GAP-43. J.Cell Biol. 1989, 108:613-624.
62. Suzuki A., Ohno S. The PAR-aPKC system: lessons in polarity. J.Cell Sci. 2006, 119:979-987.
63. Tang N., Marshall W.F., McMahon M., Metzger R.J., Martin G.R. Control of mitotic spindle angle by the RAS-regulated ERK1/2 pathway determines lung tube shape. Science 2011, 333:342-345.
64. Thomas J.B., Bastiani M.J., Bate M., Goodman C.S. From grasshopper to Drosophila: a common plan for neuronal development. Nature 1984, 310:203-207.
65. Williams S.E., Beronja S., Pasolli H.A., Fuchs E. Asymmetric cell divisions promote Notch-dependent epidermal differentiation. Nature 2011, 470:353-358.
66. Wise A., Watson-Koken M.A., Rees S., Lee M., Milligan G. Interactions of the alpha2A-adrenoceptor with multiple Gi-family G-proteins: studies with pertussis toxin-resistant G-protein mutants. Biochem. J. 1997, 321:721-728.
67. Wodarz A., Ramrath A., Kuchinke U., Knust E. Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature 1999, 402:544-547.
68. Wodarz A., Ramrath A., Grimm A., Knust E. Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J.Cell Biol. 2000, 150:1361-1374.
69. Worby C.A., Simonson-Leff N., Dixon J.E. RNA interference of gene expression (RNAi) in cultured Drosophila cells. Sci. STKE 2001, 95:pl1.
70. Xiong W.C., Okano H., Patel N.H., Blendy J.A., Montell C. repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev. 1994, 8:981-994.
71. Yamashita Y.M., Jones D.L., Fuller M.T. Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science 2003, 301:1547-1550.
72. Yasumi M., Sakisaka T., Hoshino T., Kimura T., Sakamoto Y., Yamanaka T., Ohno S., Takai Y. Direct binding of Lgl2 to LGN during mitosis and its requirement for normal cell division. J.Biol. Chem. 2005, 280:6761-6765.
73. Yu F., Morin X., Cai Y., Yang X., Chia W. Analysis of partner of inscuteable, a novel player of Drosophila asymmetric divisions, reveals two distinct steps in inscuteable apical localization. Cell 2000, 100:399-409.
74. Yu F., Cai Y., Kaushik R., Yang X., Chia W. Distinct roles of Galphai and Gbeta13F subunits of the heterotrimeric G protein complex in the mediation of Drosophila neuroblast asymmetric divisions. J.Cell Biol. 2003, 162:623-633.
75. Yu F., Kuo C.T., Jan Y.N. Drosophila neuroblast asymmetric cell division: recent advances and implications for stem cell biology. Neuron 2006, 51:13-20.