Linking Asymmetric Cell Division to the Terminal Differentiation Program of Postmitotic Neurons in C. elegans

Developmental Cell

Volumn 16, Issue 4, 2009, Pages 563-575

  Bertrand, Vincent ^a   Hobert, Oliver ^a  

^a NewYork Presbyterian Hospital   (United States)

Author keywords

DEVBIO; MOLNEURO

Indexed keywords

BETA CATENIN; CAENORHABDITIS ELEGANS PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CEH 10; TRANSCRIPTION FACTOR REF 2; TRANSCRIPTION FACTOR TTX 3; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CELL DIVISION; CHOLINERGIC NERVE CELL; DAUGHTER CELL; EMBRYO DEVELOPMENT; MITOSIS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BASE SEQUENCE; BETA CATENIN; BINDING SITES; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL DIFFERENTIATION; EMBRYO, NONMAMMALIAN; FEMALE; INTERNEURONS; MITOSIS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NEURONS; WNT PROTEINS;

CAENORHABDITIS ELEGANS;

EID: 64549093686     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2009.02.011     Document Type: Article

References (55)

1. Alper S., and Kenyon C. The zinc finger protein REF-2 functions with the Hox genes to inhibit cell fusion in the ventral epidermis of C. elegans. Development 129 (2002) 3335-3348
2. Altun-Gultekin Z., Andachi Y., Tsalik E.L., Pilgrim D., Kohara Y., and Hobert O. A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C. elegans. Development 128 (2001) 1951-1969
3. Arata Y., Kouike H., Zhang Y., Herman M.A., Okano H., and Sawa H. Wnt signaling and a Hox protein cooperatively regulate psa-3/Meis to determine daughter cell fate after asymmetric cell division in C. elegans. Dev. Cell 11 (2006) 105-115
4. Aruga J. The role of Zic genes in neural development. Mol. Cell. Neurosci. 26 (2004) 205-221
5. Asbreuk C.H., van Schaick H.S., Cox J.J., Kromkamp M., Smidt M.P., and Burbach J.P. The homeobox genes Lhx7 and Gbx1 are expressed in the basal forebrain cholinergic system. Neuroscience 109 (2002) 287-298
6. Bischoff M., and Schnabel R. A posterior centre establishes and maintains polarity of the Caenorhabditis elegans embryo by a Wnt-dependent relay mechanism. PLoS Biol. 4 (2006) e396
7. Davidson E.H., McClay D.R., and Hood L. Regulatory gene networks and the properties of the developmental process. Proc. Natl. Acad. Sci. USA 100 (2003) 1475-1480
8. Doe C.Q. Neural stem cells: balancing self-renewal with differentiation. Development 135 (2008) 1575-1587
9. Ebert P.J., Timmer J.R., Nakada Y., Helms A.W., Parab P.B., Liu Y., Hunsaker T.L., and Johnson J.E. Zic1 represses Math1 expression via interactions with the Math1 enhancer and modulation of Math1 autoregulation. Development 130 (2003) 1949-1959
10. Etchberger J.F., Lorch A., Sleumer M.C., Zapf R., Jones S.J., Marra M.A., Holt R.A., Moerman D.G., and Hobert O. The molecular signature and cis-regulatory architecture of a C. elegans gustatory neuron. Genes Dev. 21 (2007) 1653-1674
11. Fire A. Histochemical techniques for locating Escherichia coli beta-galactosidase activity in transgenic organisms. Genet. Anal. Tech. Appl. 9 (1992) 151-158
12. Forrester W.C., Perens E., Zallen J.A., and Garriga G. Identification of Caenorhabditis elegans genes required for neuronal differentiation and migration. Genetics 148 (1998) 151-165
13. Fraser A.G., Kamath R.S., Zipperlen P., Martinez-Campos M., Sohrmann M., and Ahringer J. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408 (2000) 325-330
14. Guenther C., and Garriga G. Asymmetric distribution of the C. elegans HAM-1 protein in neuroblasts enables daughter cells to adopt distinct fates. Development 122 (1996) 3509-3518
15. Hawkins N.C., Ellis G.C., Bowerman B., and Garriga G. MOM-5 frizzled regulates the distribution of DSH-2 to control C. elegans asymmetric neuroblast divisions. Dev. Biol. 284 (2005) 246-259
16. Hobert O. Regulatory logic of neuronal diversity: terminal selector genes and selector motifs. Proc. Natl. Acad. Sci. USA 105 (2008) 20067-20071
17. Hobert O., Mori I., Yamashita Y., Honda H., Ohshima Y., Liu Y., and Ruvkun G. Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron 19 (1997) 345-357
18. Huang S., Shetty P., Robertson S.M., and Lin R. Binary cell fate specification during C. elegans embryogenesis driven by reiterated reciprocal asymmetry of TCF POP-1 and its coactivator beta-catenin SYS-1. Development 134 (2007) 2685-2695
19. Huttner W.B., and Kosodo Y. Symmetric versus asymmetric cell division during neurogenesis in the developing vertebrate central nervous system. Curr. Opin. Cell Biol. 17 (2005) 648-657
20. Inoue T., Ota M., Ogawa M., Mikoshiba K., and Aruga J. Zic1 and Zic3 regulate medial forebrain development through expansion of neuronal progenitors. J. Neurosci. 27 (2007) 5461-5473
21. Kaletta T., Schnabel H., and Schnabel R. Binary specification of the embryonic lineage in Caenorhabditis elegans. Nature 390 (1997) 294-298
22. Karp X., and Greenwald I. Post-transcriptional regulation of the E/Daughterless ortholog HLH-2, negative feedback, and birth order bias during the AC/VU decision in C. elegans. Genes Dev. 17 (2003) 3100-3111
23. Kidd III A.R., Miskowski J.A., Siegfried K.R., Sawa H., and Kimble J. A beta-catenin identified by functional rather than sequence criteria and its role in Wnt/MAPK signaling. Cell 121 (2005) 761-772
24. Knoblich J.A. Mechanisms of asymmetric stem cell division. Cell 132 (2008) 583-597
25. Korswagen H.C., Herman M.A., and Clevers H.C. Distinct beta-catenins mediate adhesion and signalling functions in C. elegans. Nature 406 (2000) 527-532
26. Krause M., Park M., Zhang J.M., Yuan J., Harfe B., Xu S.Q., Greenwald I., Cole M., Paterson B., and Fire A. A C. elegans E/Daughterless bHLH protein marks neuronal but not striated muscle development. Development 124 (1997) 2179-2189
27. Lam N., Chesney M.A., and Kimble J. Wnt signaling and CEH-22/tinman/Nkx2.5 specify a stem cell niche in C. elegans. Curr. Biol. 16 (2006) 287-295
28. Ledent V., and Vervoort M. The basic helix-loop-helix protein family: comparative genomics and phylogenetic analysis. Genome Res. 11 (2001) 754-770
29. Lin R., Hill R.J., and Priess J.R. POP-1 and anterior-posterior fate decisions in C. elegans embryos. Cell 92 (1998) 229-239
30. Livesey F.J., Furukawa T., Steffen M.A., Church G.M., and Cepko C.L. Microarray analysis of the transcriptional network controlled by the photoreceptor homeobox gene Crx. Curr. Biol. 10 (2000) 301-310
31. Maduro M.F., Kasmir J.J., Zhu J., and Rothman J.H. The Wnt effector POP-1 and the PAL-1/Caudal homeoprotein collaborate with SKN-1 to activate C. elegans endoderm development. Dev. Biol. 285 (2005) 510-523
32. Merzdorf C.S. Emerging roles for zic genes in early development. Dev. Dyn. 236 (2007) 922-940
33. Mizumoto K., and Sawa H. Two betas or not two betas: regulation of asymmetric division by beta-catenin. Trends Cell Biol. 17 (2007) 465-473
34. Mori I., and Ohshima Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376 (1995) 344-348
35. Oda Y. Choline acetyltransferase: the structure, distribution and pathologic changes in the central nervous system. Pathol. Int. 49 (1999) 921-937
36. Park F.D., and Priess J.R. Establishment of POP-1 asymmetry in early C. elegans embryos. Development 130 (2003) 3547-3556
37. Park F.D., Tenlen J.R., and Priess J.R. C. elegans MOM-5/frizzled functions in MOM-2/Wnt-independent cell polarity and is localized asymmetrically prior to cell division. Curr. Biol. 14 (2004) 2252-2258
38. Phillips B.T., Kidd III A.R., King R., Hardin J., and Kimble J. Reciprocal asymmetry of SYS-1/beta-catenin and POP-1/TCF controls asymmetric divisions in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 104 (2007) 3231-3236
39. Schnabel R., Hutter H., Moerman D., and Schnabel H. Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: variability of development and regional specification. Dev. Biol. 184 (1997) 234-265
40. Siegfried K.R., and Kimble J. POP-1 controls axis formation during early gonadogenesis in C. elegans. Development 129 (2002) 443-453
41. Siegfried K.R., Kidd III A.R., Chesney M.A., and Kimble J. The sys-1 and sys-3 genes cooperate with Wnt signaling to establish the proximal-distal axis of the Caenorhabditis elegans gonad. Genetics 166 (2004) 171-186
42. Simmer F., Moorman C., Van Der Linden A.M., Kuijk E., Van Den Berghe P.V., Kamath R., Fraser A.G., Ahringer J., and Plasterk R.H. Genome-wide RNAi of C. elegans using the hypersensitive rrf-3 strain reveals novel gene functions. PLoS Biol. 1 (2003) E12
43. Sulston J.E., Schierenberg E., White J.G., and Thomson J.N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100 (1983) 64-119
44. Svendsen P.C., and McGhee J.D. The C. elegans neuronally expressed homeobox gene ceh-10 is closely related to genes expressed in the vertebrate eye. Development 121 (1995) 1253-1262
45. Takeshita H., and Sawa H. Asymmetric cortical and nuclear localizations of WRM-1/beta-catenin during asymmetric cell division in C. elegans. Genes Dev. 19 (2005) 1743-1748
46. Tsalik E.L., and Hobert O. Functional mapping of neurons that control locomotory behavior in Caenorhabditis elegans. J. Neurobiol. 56 (2003) 178-197
47. Wenick A.S., and Hobert O. Genomic cis-regulatory architecture and trans-acting regulators of a single interneuron-specific gene battery in C. elegans. Dev. Cell 6 (2004) 757-770
48. Wodarz A., and Huttner W.B. Asymmetric cell division during neurogenesis in Drosophila and vertebrates. Mech. Dev. 120 (2003) 1297-1309
49. Wolfe S.A., Nekludova L., and Pabo C.O. DNA recognition by Cys2His2 zinc finger proteins. Annu. Rev. Biophys. Biomol. Struct. 29 (2000) 183-212
50. Woodhead G.J., Mutch C.A., Olson E.C., and Chenn A. Cell-autonomous beta-catenin signaling regulates cortical precursor proliferation. J. Neurosci. 26 (2006) 12620-12630
51. Wrobel C.N., Mutch C.A., Swaminathan S., Taketo M.M., and Chenn A. Persistent expression of stabilized beta-catenin delays maturation of radial glial cells into intermediate progenitors. Dev. Biol. 309 (2007) 285-297
52. Yagi K., Satoh N., and Satou Y. Identification of downstream genes of the ascidian muscle determinant gene Ci-macho1. Dev. Biol. 274 (2004) 478-489
53. Zhang Y., Ma C., Delohery T., Nasipak B., Foat B.C., Bounoutas A., Bussemaker H.J., Kim S.K., and Chalfie M. Identification of genes expressed in C. elegans touch receptor neurons. Nature 418 (2002) 331-335
54. Zhang Y., Lu H., and Bargmann C.I. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438 (2005) 179-184
55. Zhao Y., Marin O., Hermesz E., Powell A., Flames N., Palkovits M., Rubenstein J.L., and Westphal H. The LIM-homeobox gene Lhx8 is required for the development of many cholinergic neurons in the mouse forebrain. Proc. Natl. Acad. Sci. USA 100 (2003) 9005-9010