Terminal Selectors of Neuronal Identity

Current Topics in Developmental Biology

Volumn 116, Issue , 2016, Pages 455-475

  Hobert, Oliver ^a  

^a Howard Hughes Medical Institute   (United States)

Author keywords

Neuronal differentiation; Neuronal identity; Transcriptional regulation

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN;

ANIMAL; CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CYTOLOGY; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; NEUROGENESIS; NEURONS;

EID: 84954304814     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.ctdb.2015.12.007     Document Type: Chapter

References (74)

1. Alon U. An introduction to systems biology: Design principles of biological circuits. 1st ed. 2006, Chapman & Hall/CRC, London, UK.
2. Altun Z.F., Chen B., Wang Z.W., Hall D.H. High resolution map of Caenorhabditis elegans gap junction proteins. Developmental Dynamics 2009, 238:1936-1950.
3. Altun-Gultekin Z., Andachi Y., Tsalik E.L., Pilgrim D., Kohara Y., 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 2001, 128:1951-1969.
4. Baran R., Aronoff R., Garriga G. The C. elegans homeodomain gene unc-42 regulates chemosensory and glutamate receptor expression. Development 1999, 126:2241-2251.
5. Bargmann C.I., Hartwieg E., Horvitz H.R. Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 1993, 74:515-527.
6. Bargmann C.I., Horvitz H.R. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 1991, 7:729-742.
7. Baum P.D., Guenther C., Frank C.A., Pham B.V., Garriga G. The Caenorhabditis elegans gene ham-2 links Hox patterning to migration of the HSN motor neuron. Genes & Development 1999, 13:472-483.
8. Bertrand V., Hobert O. Linking asymmetric cell division to the terminal differentiation program of postmitotic neurons in C. elegans. Developmental Cell 2009, 16:563-575.
9. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
10. Burghoorn J., Piasecki B.P., Crona F., Phirke P., Jeppsson K.E., Swoboda P. The in vivo dissection of direct RFX-target gene promoters in C. elegans reveals a novel cis-regulatory element, the C-box. Developmental Biology 2012, 368:415-426.
11. Cassata G., Kagoshima H., Andachi Y., Kohara Y., Durrenberger M.B., Hall D.H., et al. The LIM homeobox gene ceh-14 confers thermosensory function to the AFD neurons in Caenorhabditis elegans. Neuron 2000, 25:587-597.
12. Chalfie M., Sulston J. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Developmental Biology 1981, 82:358-370.
13. Chalfie M., Sulston J.E., White J.G., Southgate E., Thomson J.N., Brenner S. The neural circuit for touch sensitivity in Caenorhabditis elegans. The Journal of Neuroscience 1985, 5:956-964.
14. Chalfie M., Tu Y., Euskirchen G., Ward W.W., Prasher D.C. Green fluorescent protein as a marker for gene expression. Science 1994, 263:802-805.
15. Chang S., Johnston R.J., Hobert O. A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C. elegans. Genes & Development 2003, 17:2123-2137.
16. Cinar H., Keles S., Jin Y. Expression profiling of GABAergic motor neurons in Caenorhabditis elegans. Current Biology 2005, 15:340-346.
17. Deneris E.S., Hobert O. Maintenance of postmitotic neuronal cell identity. Nature Neuroscience 2014, 17:899-907.
18. Desai C., Garriga G., McIntire S.L., Horvitz H.R. A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature 1988, 336:638-646.
19. Doitsidou M., Flames N., Topalidou I., Abe N., Felton T., Remesal L., et al. A combinatorial regulatory signature controls terminal differentiation of the dopaminergic nervous system in C. elegans. Genes & Development 2013, 27:1391-1405.
20. Duggan A., Ma C., Chalfie M. Regulation of touch receptor differentiation by the Caenorhabditis elegans mec-3 and unc-86 genes. Development 1998, 125:4107-4119.
21. Eastman C., Horvitz H.R., Jin Y. Coordinated transcriptional regulation of the unc-25 glutamic acid decarboxylase and the unc-47 GABA vesicular transporter by the Caenorhabditis elegans UNC-30 homeodomain protein. The Journal of Neuroscience 1999, 19:6225-6234.
22. Edlund T., Jessell T.M. Progression from extrinsic to intrinsic signaling in cell fate specification: A view from the nervous system. Cell 1999, 96:211-224.
23. Enriquez J., Venkatasubramanian L., Baek M., Peterson M., Aghayeva U., Mann R.S. Specification of individual adult motor neuron morphologies by combinatorial transcription factor codes. Neuron 2015, 86:955-970.
24. Etchberger J.F., Flowers E.B., Poole R.J., Bashllari E., Hobert O. Cis-regulatory mechanisms of left/right asymmetric neuron-subtype specification in C. elegans. Development 2009, 136:147-160.
25. Etchberger J.F., Lorch A., Sleumer M.C., Zapf R., Jones S.J., Marra M.A., et al. The molecular signature and cis-regulatory architecture of a C. elegans gustatory neuron. Genes & Development 2007, 21:1653-1674.
26. Finney M., Ruvkun G., Horvitz H.R. The C. elegans cell lineage and differentiation gene unc-86 encodes a protein with a homeodomain and extended similarity to transcription factors. Cell 1988, 55:757-769.
27. Flames N., Hobert O. Gene regulatory logic of dopamine neuron differentiation. Nature 2009, 458:885-889.
28. Garcia-Bellido A. Genetic control of wing disc development in Drosophila. Ciba Foundation Symposium 1975, 29:161-182.
29. Gonzalez-Barrios M., Fierro-Gonzalez J.C., Krpelanova E., Mora-Lorca J.A., Pedrajas J.R., Penate X., et al. Cis- and trans-regulatory mechanisms of gene expression in the ASJ sensory neuron of Caenorhabditis elegans. Genetics 2015, 200:123-134.
30. Gordon P.M., Hobert O. A competition mechanism for a homeotic neuron identity transformation in C. elegans. Developmental Cell 2015, 34:206-219.
31. Guillermin M.L., Castelletto M.L., Hallem E.A. Differentiation of carbon dioxide-sensing neurons in Caenorhabditis elegans requires the ETS-5 transcription factor. Genetics 2011, 189:1327-1339.
32. Hedgecock E.M., Russell R.L. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America 1975, 72:4061-4065.
33. Hemmati-Brivanlou A., Melton D. Vertebrate neural induction. Annual Review of Neuroscience 1997, 20:43-60.
34. Hobert O. Regulatory logic of neuronal diversity: Terminal selector genes and selector motifs. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:20067-20071.
35. Hobert O. Regulation of terminal differentiation programs in the nervous system. Annual Review of Cell and Developmental Biology 2011, 27:681-696.
36. Hobert O. Development of left/right asymmetry in the Caenorhabditis elegans nervous system: From zygote to postmitotic neuron. Genesis 2014, 52:528-543.
37. Hobert O., Mori I., Yamashita Y., Honda H., Ohshima Y., Liu Y., et al. Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron 1997, 19:345-357.
38. Holmberg J., Perlmann T. Maintaining differentiated cellular identity. Nature Reviews. Genetics 2012, 13:429-439.
39. Howell K., White J.G., Hobert O. Spatiotemporal control of a novel synaptic organizer molecule. Nature 2015, 523:83-87.
40. Hutter H. Extracellular cues and pioneers act together to guide axons in the ventral cord of C. elegans. Development 2003, 130:5307-5318.
41. Jin Y., Hoskins R., Horvitz H.R. Control of type-D GABAergic neuron differentiation by C. elegans UNC-30 homeodomain protein. Nature 1994, 372:780-783.
42. Kim K., Kim R., Sengupta P. The HMX/NKX homeodomain protein MLS-2 specifies the identity of the AWC sensory neuron type via regulation of the ceh-36 Otx gene in C. elegans. Development 2010, 137:963-974.
43. Kratsios P., Pinan-Lucarre B., Kerk S.Y., Weinreb A., Bessereau J.L., Hobert O. Transcriptional coordination of synaptogenesis and neurotransmitter signaling. Current Biology 2015, 25:1282-1295.
44. Kratsios P., Stolfi A., Levine M., Hobert O. Coordinated regulation of cholinergic motor neuron traits through a conserved terminal selector gene. Nature Neuroscience 2011, 15:205-214.
45. Laguna A., Schintu N., Nobre A., Alvarsson A., Volakakis N., Jacobsen J.K., et al. Dopaminergic control of autophagic-lysosomal function implicates Lmx1b in Parkinson's disease. Nature Neuroscience 2015, 18:826-835.
46. Lanjuin A., VanHoven M.K., Bargmann C.I., Thompson J.K., Sengupta P. Otx/otd homeobox genes specify distinct sensory neuron identities in C. elegans. Developmental Cell 2003, 5:621-633.
47. Lewis J.A., Hodgkin J.A. Specific neuroanatomical changes in chemosensory mutants of the nematode Caenorhabditis elegans. The Journal of Comparative Neurology 1977, 172:489-510.
48. McIntire S.L., Jorgensen E., Horvitz H.R. Genes required for GABA function in Caenorhabditis elegans. Nature 1993, 364:334-337.
49. Mori I., Ohshima Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 1995, 376:344-348.
50. Murgan S., Kari W., Rothbacher U., Iche-Torres M., Melenec P., Hobert O., et al. Atypical transcriptional activation by TCF via a Zic transcription factor in C. elegans neuronal precursors. Developmental Cell 2015, 33:737-745.
51. Nokes E.B., Van Der Linden A.M., Winslow C., Mukhopadhyay S., Ma K., Sengupta P. Cis-regulatory mechanisms of gene expression in an olfactory neuron type in Caenorhabditis elegans. Developmental Dynamics 2009, 238:3080-3092.
52. Pereira L., Kratsios P., Serrano-Saiz E., Sheftel H., Mayo A., Hall D.H., et al. A cellular and regulatory map of the cholinergic nervous system of C. elegans. Elife 2015, 4. pii: e12432. doi: 10.7554/eLife.12432.
53. Prasad B.C., Ye B., Zackhary R., Schrader K., Seydoux G., Reed R.R. unc-3, a gene required for axonal guidance in Caenorhabditis elegans, encodes a member of the O/E family of transcription factors. Development 1998, 125:1561-1568.
54. Sagasti A., Hobert O., Troemel E.R., Ruvkun G., Bargmann C.I. Alternative olfactory neuron fates are specified by the LIM homeobox gene lim-4. Genes & Development 1999, 13:1794-1806.
55. Satterlee J.S., Sasakura H., Kuhara A., Berkeley M., Mori I., Sengupta P. Specification of thermosensory neuron fate in C. elegans requires ttx-1, a homolog of otd/Otx. Neuron 2001, 31:943-956.
56. Sengupta P., Colbert H.A., Bargmann C.I. The C. elegans gene odr-7 encodes an olfactory-specific member of the nuclear receptor superfamily. Cell 1994, 79:971-980.
57. Serrano-Saiz E., Poole R.J., Felton T., Zhang F., de la Cruz E.D., Hobert O. Modular control of glutamatergic neuronal identity in C. elegans by distinct homeodomain proteins. Cell 2013, 155:659-673.
58. Stefanakis N., Carrera I., Hobert O. Regulatory logic of pan-neuronal gene expression in C. elegans. Neuron 2015, 87:733-750.
59. Sulston J.E. Neuronal cell lineages in the nematode Caenorhabditis elegans. Cold Spring Harbor Symposia on Quantitative Biology 1983, 48:443-452.
60. Swoboda P., Adler H.T., Thomas J.H. The RFX-type transcription factor DAF-19 regulates sensory neuron cilium formation in C. elegans. Molecular Cell 2000, 5:411-421.
61. Sze J.Y., Zhang S., Li J., Ruvkun G. The C. elegans POU-domain transcription factor UNC-86 regulates the tph-1 tryptophan hydroxylase gene and neurite outgrowth in specific serotonergic neurons. Development 2002, 129:3901-3911.
62. Tsalik E.L., Hobert O. Functional mapping of neurons that control locomotory behavior in Caenorhabditis elegans. Journal of Neurobiology 2003, 56:178-197.
63. Tursun B., Patel T., Kratsios P., Hobert O. Direct conversion of C. elegans germ cells into specific neuron types. Science 2011, 331:304-308.
64. Uchida O., Nakano H., Koga M., Ohshima Y. The C. elegans che-1 gene encodes a zinc finger transcription factor required for specification of the ASE chemosensory neurons. Development 2003, 130:1215-1224.
65. Van Buskirk C., Sternberg P.W. Paired and LIM class homeodomain proteins coordinate differentiation of the C. elegans ALA neuron. Development 2010, 137:2065-2074.
66. Waddington C.H. The strategy of the genes 1957, Allen and Unwin, London, UK.
67. Way J.C., Chalfie M. mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans. Cell 1988, 54:5-16.
68. Way J.C., Chalfie M. The mec-3 gene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. Genes & Development 1989, 3:1823-1833.
69. Wenick A.S., Hobert O. Genomic cis-regulatory architecture and trans-acting regulators of a single interneuron-specific gene battery in C. elegans. Developmental Cell 2004, 6:757-770.
70. White J.G., Southgate E., Thomson J.N., Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 1986, 314:1-340.
71. Winnier A.R., Meir J.Y., Ross J.M., Tavernarakis N., Driscoll M., Ishihara T., et al. UNC-4/UNC-37-dependent repression of motor neuron-specific genes controls synaptic choice in Caenorhabditis elegans. Genes & Development 1999, 13:2774-2786.
72. Xue D., Tu Y., Chalfie M. Cooperative interactions between the Caenorhabditis elegans homeoproteins UNC-86 and MEC-3. Science 1993, 261:1324-1328.
73. Zhang F., Bhattacharya A., Nelson J.C., Abe N., Gordon P., Lloret-Fernandez C., et al. The LIM and POU homeobox genes ttx-3 and unc-86 act as terminal selectors in distinct cholinergic and serotonergic neuron types. Development 2014, 141:422-435.
74. Zhang Y., Ma C., Delohery T., Nasipak B., Foat B.C., Bounoutas A., et al. Identification of genes expressed in C. elegans touch receptor neurons. Nature 2002, 418:331-335.