Asymmetric division of Drosophila neural stem cells: A basis for neural diversity

Current Opinion in Neurobiology

Volumn 10, Issue 1, 2000, Pages 38-44

  Matsuzaki, Fumio ^a  

^a JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; NOTCH RECEPTOR;

BIODIVERSITY; CELL DIVISION; CELL FATE; CELL POLARITY; CELLULAR DISTRIBUTION; DEVELOPMENT; DROSOPHILA; EPITHELIUM CELL; GENE LOCATION; MITOSIS SPINDLE; NERVE CELL DIFFERENTIATION; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; ZYGOTE;

EID: 0033953269     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(99)00052-5     Document Type: Review

References (64)

1. Horvitz H.R., Herskowitz I. Mechanisms of asymmetric cell division: two Bs or not two Bs, that is the question. Cell. 68:1992;237-255.
2. Knoblich J.A. Mechanisms of asymmetric cell division during animal development. Curr Opin Cell Biol. 9:1997;833-841.
3. Lin H., Schagat T. Neuroblasts: a model for the asymmetric division of stem cells. Trends Genet. 13:1997;33-39.
4. Jan Y.N., Jan L.Y. Asymmetric cell division. Nature. 392:1998;775-778.
5. Doe C.Q., Skeath J.B. Neurogenesis in the insect central nervous system. Curr Opin Neurobiol. 6:1996;18-24.
6. Doe C.Q. Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development. 116:1992;855-863.
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. 179:1996;41-64.
8. Schmidt H., Rickert C., Bossing T., Vef O., Urban J., Technau G.M. The embryonic central nervous system lineages of Drosophila melanogaster: II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev Biol. 189:1997;186-204.
9. Schmid A., Chiba A., Doe C.Q. Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development. 126:1999;4653-4689.
10. Vervoort M., Dambly-Chaudiere C., Ghysen A. Cell fate determination in Drosophila. Curr Opin Neurobiol. 7:1997;21-28.
11. 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. 76:1994;477-491.
12. Knoblich J.A., Jan L.Y., Jan Y.N. Asymmetric segregation of Numb and Prospero during cell division. Nature. 377:1995;624-627.
13. Hirata J., Nakagoshi H., Nabeshima Y., Matsuzaki F. Asymmetric segregation of the homeoprotein Prospero during Drosophila development. Nature. 377:1995;627-630.
14. Spana E.P., Doe C.Q. The Prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development. 121:1995;3187-3195.
15. Doe C.Q., Chu-LaGraff Q., Wright D.M., Scott M.P. The prospero gene specifies cell fates in the Drosophila central nervous system. Cell. 65:1991;451-465.
16. Vaessin H., Grell E., Wolff E., Bier E., Jan L.Y., Jan Y.N. prospero is expressed in neuronal precursors and encodes a nuclear protein that is involved in the control of axonal outgrowth in Drosophila. Cell. 67:1991;942-953.
17. Matsuzaki F., Koizumi K., Hama C., Yoshioka T., Nabeshima Y. Cloning of the Drosophila prospero gene and its expression in ganglion mother cells. Biochem Biophys Res Comm. 182:1992;1326-1332.
18. Uemura T., Shepherd S., Ackerman L., Jan L.Y., Jan Y.N. numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell. 58:1989;349-360.
19. Guo M., Jan L.Y., Jan Y.N. Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron. 17:1996;27-41.
20. Spana E.P., Kopczynski C., Goodman C.S., Doe C.Q. Asymmetric localization of Numb autonomously determines sibling neuron identity in Drosophila CNS. Development. 121:1995;3489-3494.
21. Spana E.P., Doe C.Q. Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron. 17:1996;21-26.
22. •].
23. •] show that muscle formation requires asymmetric Notch signaling between daughter cells of muscle progenitor cells. During the divisions of these cells, Inscuteable controls Numb localization as in the CNS and PNS, providing the first evidence for the presence of Inscuteable-dependent cell polarity in mesodermal cells.
24. 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 USA. 93:1996;11925-11932.
25. Buescher M., Yeo S.L., Udolph G., Zavortink M., Yang X., Tear G., Chia W. Binary sibling neuronal cell fate decisions in the Drosophila embryonic central nervous system are nonstochastic and require inscuteable-mediated asymmetry of ganglion mother cells. Genes Dev. 12:1998;1858-1870. Demonstrates that, like neuroblasts, GMCs have an Inscuteable-dependent cell polarity. This polarity induces asymmetric Numb segregation into one of the two daughter neurons, in order to distinguish their binary cell fates. In addition, the authors demonstrate that differences in cell size between daughter neurons of one GMC depends on inscuteable.
26. Dye C.A., Lee J-K., Atkinson R.C., Brewster R., Han P-L., Bellen H.J. The Drosophila sanpodo gene controls sibling cell fate and encodes a tropomodulin homolog, an actin/tropomyosin-associated protein. Development. 125:1998;1845-1856. Shows that a Tropomodulin homologue Sanpodo functions in combination with the Notch/Numb pathway in the development of the PNS, suggesting the involvement of an actin-based process in this signaling pathway.
27. •], shows that sanpodo acts downstream of numb to facilitate Notch signaling. The authors also observe that sanpodo and numb are not involved in lateral inhibition during neuroblast formation in the neuroectoderm, another Notch-dependent process.
28. Zeng C., Younger-Shepherd S., Jan L.Y., Jan Y.N. Delta and Serrate are redundant Notch ligands required for asymmetric cell divisions within the Drosophila sensory organ lineage. Genes Dev. 12:1998;1086-1091. Shows that Delta and Serrate act as redundant ligands of Notch receptors in cell fate decisions in a PNS lineage. Notch signaling between daughter cells is required in specifying cell fates within the SOP cell lineage. This result is in contrast to the cell fate decision of MP2 daughter cells in the CNS, where the Notch ligand appears to be supplied from cells outside the lineage (see [21]).
29. Shen C-P., Jan L.Y., Jan Y.N. Miranda is required for the asymmetric localization of Prospero during mitosis in Drosophila. Cell. 90:1997;449-458.
30. 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. 390:1997;625-629.
31. 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. 95:1998;225-235. Identifies a novel protein, Partner of Numb (Pon), that binds the Numb phosphotyrosine binding (PTB) domain in order to localize Numb during embryogenesis. This protein is asymmetrically localized during mitosis in neuroblasts, SOP cells and muscle progenitor cells. Loss of pon function disrupts Numb localization in muscle progenitors and delays Numb-crescent formation in neural precursor cells. Ectopically expressed Pon is basally localized in epithelial cells and is able to induce Numb localization, suggesting common molecular machinery to localize the Pon/Numb complex in both neuroblasts and epithelial cells.
32. ••].
33. ••] show asymmetric segregation of prospero mRNA during neuroblast mitosis. This paper demonstrates that the RNA-binding protein Staufen is asymmetrically localized to the basal cortex in dividing neuroblasts to be segregated, together with prospero mRNA, into the sibling GMC. Genetic interactions between staufen and prospero mutants are also presented.
34. Akiyama-Oda Y., Hosoya T., Hotta Y. Asymmetric cell division of thoracic neuroblast 6-4 bifurcate glial and neuronal lineage in Drosophila. Development. 126:1999;1967-1974. The authors describe an analysis of a neuroglioblast lineage and its division into a glioblast and neuroblast, indicating the role of asymmetric mRNA segregation in this binary fate decision. NB6-4 transcribes glial cell missing (gcm) mRNA and divides parallel to the neuroepithelial cells in the dorso-ventral orientation. Asymmetric gcm mRNA segregation between the two daughter cells is probably essential for the bifurcation of glioblast and neuroblast lineages.
35. •] show that Miranda localizes Staufen in order to segregate prospero mRNA, and they characterized the functional domains of Miranda protein; the amino-terminal region acts for its own localization and the middle region binds to Staufen and Prospero. In addition, this paper demonstrates the interactions of Miranda with Numb and Inscuteable in vitro.
36. •].
37. •].
38. •].
39. Jones B.W., Fetter R.D., Tear G., Goodman C.S. glial cell missing, a genetic switch that controls glial versus neuronal fate. Cell. 82:1995;1013-1023.
40. Hosoya T., Takizawa K., Nitta K., Hotta Y. glial cells missing, a binary switch between neuronal and glial determination in Drosophila. Cell. 82:1995;1025-1036.
41. Vincent S., Vonesch J.L., Giangrande A. glide directs glial fate commitment and cell fate switch between neurones and glia. Development. 122:1996;131-139.
42. Bernardino R., Kammerer M., Vonesch J-L., Giangrande A. Gliogenesis depends on glide/gcm through asymmetric division of neuroglioblasts. Dev Biol. 216:1999;265-275.
43. Kraut R., Campos-Ortega J.A. inscuteable, a neural precursor gene of Drosophila, encodes a candidate for a cytoskeleton adapter protein. Dev Biol. 174:1996;65-81.
44. Kraut R., Chia W., Jan L.Y., Jan Y.N., Knoblich J.A. Role of inscuteable in orienting asymmetric cell division in Drosophila. Nature. 383:1996;50-55.
45. Knoblich J.A., Jan L.Y., Jan Y.N. Deletion analysis of the Drosophila Inscuteable protein reveals domains for cortical localization and asymmetric localization. Curr Biol. 9:1999;155-158.
46. Tio M., Zavortink M., Yang X., Chia W. A functional analysis of inscuteable and its roles during Drosophila asymmetric cell divisions. J Cell Sci. 112:1999;1541-1551.
47. Huttner W.B., Brand M. Asymmetric division and polarity of neuroepithelial cells. Curr Opin Neurobiol. 7:1997;29-39.
48. Eaton S., Simons K. Apical, basal and lateral cues for epithelial polarization. Cell. 82:1995;5-8.
49. Kuchinke U., Grawe F., Knust E. Control of spindle orientation in Drosophila by the Par-3-related PDZ-domain protein Bazooka. Curr Biol. 8:1998;1357-1365. This paper reveals that the bazooka gene encodes a PDZ protein homologous to C. elegans Par-3 protein. This protein is localized transiently during the cell cycle to the apical cell cortex of neuroblasts just like Inscuteable. Neuroblasts divide in abnormal orientation in zygotic bazooka embryos.
50. Muller H.A.J., Wieschaus E. armadillo, bazooka, and stardust are critical for early stages in formation of the zonula adherens and maintenance of the polarized blastoderm epithelium in Drosophila. J Cell Biol. 134:1996;149-163.
51. ••].
52. ••] demonstrate the critical role played by Bazooka in the formation of neuroblast polarity and also provide the first genetic evidence for a conserved mechanism with which to create cell polarity in both neuroblasts and epithelial cells. Bazooka is colocalized with Inscuteable at the apical cortex both in delaminating neuroblasts and in dividing neuroblasts. Bazooka binds to the Inscuteable localization domain, both in vitro and in vivo. Bazooka recruits Inscuteable to the apical cortex and probably establishes and maintains cell polarity in neuroblasts. The authors observe that Miranda, Prospero and Numb are localized into the budding GMC in neuroblasts lacking either Bazooka, or Inscuteable, or both, suggesting an unknown mechanism that localizes those proteins at the late mitotic phase.
53. Izumi Y., Hirose T., Tamai Y., Hirai S., Nagashima Y., Fujimoto T., Tabuse Y., Kemphues K.J., Ohno S. An atypical PKC directly associates and colocalizes at the epithelial tight junction with ASIP, a mammalian homologue of Caenorhabditis elegans polarity protein PAR-3. J Cell Biol. 143:1998;95-106.
54. 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. 83:1995;743-752.
55. Guo S., Kemphues K.J. Molecular genetics of asymmetric cleavage in the early Caenorhabditis elegans embryo. Curr Opin Genet Dev. 6:1996;408-415.
56. Tabuse T., Izumi Y., Piano F., Kemphues K.J., Miwa J., Ohno S. Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development. 125:1998;3607-3614. Indicates that PAR-3 function in creating the A-P polarity is closely associated with the activity of an atypical protein kinase C, PKC-3. PAR-3 and PKC-3 can form protein complexes to be colocalized at the anterior cortex of fertilized eggs. Loss of PKC-3 activity causes a similar phenotype to that seen in par-3 mutants.
57. Boyd L., Guo S., Levitan D., Stinchcomb D., Kemphues K.J. PAR-2 is asymmetrically distributed and promotes association of P-granules and PAR-1 with the cortex in C. elegans embryos. Development. 122:1996;3075-3084.
58. Broadus J., Doe C.Q. Extrinsic cues, intrinsic cues and microfilaments regulate asymmetric protein localization in Drosophila neuroblasts. Curr Biol. 7:1997;827-835.
59. Knoblich J.A., Jan L.Y., Jan Y.N. The N-terminus of Drosophila Numb protein directs membrane association and actin-dependent asymmetric localization. Proc Natl Acad Sci USA. 94:1997;13005-13010.
60. Guo S., Kemphues K.J. A non-muscle myosin required for embryonic polarity in Caenorhabditis elegans. Nature. 382:1996;455-458.
61. Long R.M., Singer R.H., Meng X., Gonzalez I., Nasmyth K., Jansen R.P. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science. 277:1997;383-387.
62. Takizawa P.A., Sil A., Swedlow J.R. Herskowitz, Vale, R. D. Actin dependent localization of an RNA encoding a cell-fate determinant in yeast. Nature. 389:1997;90-93.
63. Gho M., Schweisguth F. Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila. Nature. 393:1998;178-181. This paper provides the first evidence for the role of Frizzled signaling in the orientation of asymmetric SOP cell divisions. In a PNS lineage, SOP cells divide along the anterior-posterior axis. frizzled mutations randomize the orientation of these divisions, but do not affect the intracellular SOP polarity including the coordination between the division axis and polar Numb localization.
64. Adler P.N. The genetic control of tissue polarity in Drosophila. Bioessays. 14:1992;735-741.