A map of terminal regulators of neuronal identity in Caenorhabditis elegans

Wiley Interdisciplinary Reviews: Developmental Biology

Volumn 5, Issue 4, 2016, Pages 474-498

  Hobert, Oliver ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; DOPAMINE; GLUTAMIC ACID; NEUROPEPTIDE; NEUROTRANSMITTER; OCTOPAMINE; SEROTONIN; TRANSCRIPTION FACTOR; TYRAMINE;

CAENORHABDITIS ELEGANS; CHOLINERGIC NERVE CELL; GENE EXPRESSION; GENE FUNCTION; GENE MAPPING; GENE REGULATORY NETWORK; HOMEOBOX; LOSS OF FUNCTION MUTATION; MOTONEURON; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REPORTER GENE; REVIEW; SENSORY NERVE CELL; WNT SIGNALING PATHWAY;

EID: 84975760053     PISSN: 17597684     EISSN: 17597692     Source Type: Journal    
DOI: 10.1002/wdev.233     Document Type: Review

References (168)

1. Brenner S . The genetics of Caenorhabditis elegans . Genetics 1974, 77:71–94.
2. Brenner S . Foreword. In: Wood WB, ed. The Nematode Caenorhabditis elegans. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 1988.
3. Hall DH, Altun Z . C. Elegans Atlas. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 2007.
4. Varshney LR, Chen BL, Paniagua E, Hall DH, Chklovskii DB . Structural properties of the Caenorhabditis elegans neuronal network. PLoS Comput Biol 2011, 7:e1001066.
5. Margeta MA, Wang GJ, Shen K . Clathrin adaptor AP-1 complex excludes multiple postsynaptic receptors from axons in C. elegans . Proc Natl Acad Sci USA 2009, 106:1632–1637.
6. White JG, Southgate E, Thomson JN, Brenner S . The structure of the nervous system of the nematode Caenorhabditis elegans . Philos Trans R Soc Lond B Biol Sci 1986, 314:1–340.
7. Wenick AS, Hobert O . Genomic cis-regulatory architecture and trans-acting regulators of a single interneuron-specific gene battery in C. elegans . Dev Cell 2004, 6:757–770.
8. Pereira L, Kratsios P, Serrano-Saiz E, Sheftel H, Mayo AE, Hall DH, White JG, LeBoeuf B, Garcia LR, Alon U, 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.
9. Jarrell TA, Wang Y, Bloniarz AE, Brittin CA, Xu M, Thomson JN, Albertson DG, Hall DH, Emmons SW . The connectome of a decision-making neural network. Science 2012, 337:437–444.
10. Sulston JE, Horvitz HR . Post-embryonic cell lineages of the nematode, Caenorhabditis elegans . Dev Biol 1977, 56:110–156.
11. Sulston JE, Schierenberg E, White JG, Thomson JN . The embryonic cell lineage of the nematode Caenorhabditis elegans . Dev Biol 1983, 100:64–119.
12. Hedgecock EM, Culotti JG, Hall DH . The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans . Neuron 1990, 4:61–85.
13. Wadsworth WG, Bhatt H, Hedgecock EM . Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron 1996, 16:35–46.
14. Lee RC, Feinbaum RL, Ambros V . The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843–854.
15. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G . The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans . Nature 2000, 403:901–906.
16. Miller DM, Shen MM, Shamu CE, Bürglin TR, Ruvkun G, Dubois ML, Ghee M, Wilson L . C. elegans unc-4 gene encodes a homeodomain protein that determines the pattern of synaptic input to specific motor neurons. Nature 1992, 355:841–845.
17. Sawin ER, Ranganathan R, Horvitz HR . C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 2000, 26:619–631.
18. Hills T, Brockie PJ, Maricq AV . Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans . J Neurosci 2004, 24:1217–1225.
19. Bargmann CI, Horvitz HR . Control of larval development by chemosensory neurons in Caenorhabditis elegans . Science 1991, 251:1243–1246.
20. Chalasani SH, Chronis N, Tsunozaki M, Gray JM, Ramot D, Goodman MB, Bargmann CI . Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans . Nature 2007, 450:63–70.
21. McIntire SL, Jorgensen E, Kaplan J, Horvitz HR . The GABAergic nervous system of Caenorhabditis elegans . Nature 1993, 364:337–341.
22. Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI . Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans . Cell 1995, 83:207–218.
23. Gray JM, Hill JJ, Bargmann CI . A circuit for navigation in Caenorhabditis elegans . Proc Natl Acad Sci USA 2005, 102:3184–3191.
24. Bendena WG, Boudreau JR, Papanicolaou T, Maltby M, Tobe SS, Chin-Sang ID . A Caenorhabditis elegans allatostatin/galanin-like receptor NPR-9 inhibits local search behavior in response to feeding cues. Proc Natl Acad Sci USA 2008, 105:1339–1342.
25. Chalfie M, Sulston JE, White JG, Southgate E, Thomson JN, Brenner S . The neural circuit for touch sensitivity in Caenorhabditis elegans . J Neurosci 1985, 5:956–964.
26. Mori I, Ohshima Y . Neural regulation of thermotaxis in Caenorhabditis elegans . Nature 1995, 376:344–348.
27. Van Buskirk C, Sternberg PW . Epidermal growth factor signaling induces behavioral quiescence in Caenorhabditis elegans . Nat Neurosci 2007, 10:1300–1307.
28. Sanders J, Nagy S, Fetterman G, Wright C, Treinin M, Biron D . The Caenorhabditis elegans interneuron ALA is (also) a high-threshold mechanosensor. BMC Neurosci 2013, 14:156.
29. Chalfie M, Sulston J . Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans . Dev Biol 1981, 82:358–370.
30. Tsalik EL, Hobert O . Functional mapping of neurons that control locomotory behavior in Caenorhabditis elegans . J Neurobiol 2003, 56:178–197.
31. Coates JC, de Bono M . Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Caenorhabditis elegans . Nature 2002, 419:925–929.
32. Gray JM, Karow DS, Lu H, Chang AJ, Chang JS, Ellis RE, Marletta MA, Bargmann CI . Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 2004, 430:317–322.
33. Bargmann CI, Hartwieg E, Horvitz HR . Odorant-selective genes and neurons mediate olfaction in C. elegans . Cell 1993, 74:515–527.
34. Piggott BJ, Liu J, Feng Z, Wescott SA, Xu XZ . The neural circuits and synaptic mechanisms underlying motor initiation in C. elegans . Cell 2011, 147:922–933.
35. Greer ER, Perez CL, Van Gilst MR, Lee BH, Ashrafi K . Neural and molecular dissection of a C. elegans sensory circuit that regulates fat and feeding. Cell Metab 2008, 8:118–131.
36. Kaplan JM, Horvitz HR . A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans . Proc Natl Acad Sci USA 1993, 90:2227–2231.
37. Hart AC, Sims S, Kaplan JM . Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 1995, 378:82–85.
38. Beverly M, Anbil S, Sengupta P . Degeneracy and neuromodulation among thermosensory neurons contribute to robust thermosensory behaviors in Caenorhabditis elegans . J Neurosci 2011, 31:11718–11727.
39. Hardaker LA, Singer E, Kerr R, Zhou G, Schafer WR . Serotonin modulates locomotory behavior and coordinates egg-laying and movement in Caenorhabditis elegans . J Neurobiol 2001, 49:303–313.
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. Macosko EZ, Pokala N, Feinberg EH, Chalasani SH, Butcher RA, Clardy J, Bargmann CI . A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans . Nature 2009, 458:1171–1175.
42. Kratsios P, Pinan-Lucarré B, Kerk SY, Weinreb A, Bessereau JL, Hobert O . Transcriptional coordination of synaptogenesis and neurotransmitter signaling. Curr Biol 2015, 25:1282–1295.
43. Kennerdell JR, Fetter RD, Bargmann CI . Wnt-Ror signaling to SIA and SIB neurons directs anterior axon guidance and nerve ring placement in C. elegans . Development 2009, 136:3801–3810.
44. Biron D, Wasserman S, Thomas JH, Samuel AD, Sengupta P . An olfactory neuron responds stochastically to temperature and modulates Caenorhabditis elegans thermotactic behavior. Proc Natl Acad Sci USA 2008, 105:11002–11007.
45. Li W, Kang L, Piggott BJ, Feng Z, Xu XZ . The neural circuits and sensory channels mediating harsh touch sensation in Caenorhabditis elegans . Nat Commun 2011, 2:315.
46. Hallem EA, Sternberg PW . Acute carbon dioxide avoidance in Caenorhabditis elegans . Proc Natl Acad Sci USA 2008, 105:8038–8043.
47. Li W, Feng Z, Sternberg PW, Xu XZ . A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 2006, 440:684–687.
48. Lee H, Choi MK, Lee D, Kim HS, Hwang H, Kim H, Park S, Paik YK, Lee J . Nictation, a dispersal behavior of the nematode Caenorhabditis elegans, is regulated by IL2 neurons. Nat Neurosci 2012, 15:107–112.
49. Waggoner LE, Zhou GT, Schafer RW, Schafer WR . Control of alternative behavioral states by serotonin in Caenorhabditis elegans . Neuron 1998, 21:203–214.
50. Chang HC, Paek J, Kim DH . Natural polymorphisms in C. elegans HECW-1 E3 ligase affect pathogen avoidance behaviour. Nature 2011, 480:525–529.
51. Hilliard MA, Bargmann CI, Bazzicalupo P . C. elegans responds to chemical repellents by integrating sensory inputs from the head and the tail. Curr Biol 2002, 12:730–734.
52. Aurelio O, Hall DH, Hobert O . Immunoglobulin-domain proteins required for maintenance of ventral nerve cord organization. Science 2002, 295:686–690.
53. Liu S, Schulze E, Baumeister R . Temperature- and touch-sensitive neurons couple CNG and TRPV channel activities to control heat avoidance in Caenorhabditis elegans . PLoS One 2012, 7:e32360.
54. Nelson MD, Trojanowski NF, George-Raizen JB, Smith CJ, Yu CC, Fang-Yen C, Raizen DM . The neuropeptide NLP-22 regulates a sleep-like state in Caenorhabditis elegans . Nat Commun 2013, 4:2846.
55. Chatzigeorgiou M, Yoo S, Watson JD, Lee WH, Spencer WC, Kindt KS, Hwang SW, Miller DM 3rd, Treinin M, Driscoll M, et al. Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors. Nat Neurosci 2010, 13:861–868.
56. Flavell SW, Pokala N, Macosko EZ, Albrecht DR, Larsch J, Bargmann CI . Serotonin and the neuropeptide PDF initiate and extend opposing behavioral states in C. elegans . Cell 2013, 154:1023–1035.
57. Chatzigeorgiou M, Schafer WR . Lateral facilitation between primary mechanosensory neurons controls nose touch perception in C. elegans . Neuron 2011, 70:299–309.
58. Turek M, Lewandrowski I, Bringmann H . An AP2 transcription factor is required for a sleep-active neuron to induce sleep-like quiescence in C. elegans . Curr Biol 2013, 23:2215–2223.
59. Bargmann CI . Chemosensation in C. elegans . WormBook 2006:1–29. PMID: 18050433.
60. Von Stetina SE, Treinin M, Miller DM . The motor circuit. Int Rev Neurobiol 2006, 69:125–167.
61. Huang M, Chalfie M . Gene interactions affecting mechanosensory transduction in Caenorhabditis elegans . Nature 1994, 367:467–470.
62. Sengupta P, Chou JH, Bargmann CI . odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 1996, 84:899–909.
63. Way JC, Chalfie M . mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans. Cell 1988, 54:5–16.
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. Hobert O, Mori I, Yamashita Y, Honda H, Ohshima Y, Liu Y, Ruvkun G . Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron 1997, 19:345–357.
66. Satterlee JS, 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.
67. Ortiz CO, Etchberger JF, Posy SL, Frøkjaer-Jensen C, Lockery S, Honig B, Hobert O . Searching for neuronal left/right asymmetry: genomewide analysis of nematode receptor-type guanylyl cyclases. Genetics 2006, 173:131–149.
68. Nathoo AN, Moeller RA, Westlund BA, Hart AC . Identification of neuropeptide-like protein gene families in Caenorhabditis elegans and other species. Proc Natl Acad Sci USA 2001, 98:14000–14005.
69. Li C, Kim K, Nelson LS . FMRFamide-related neuropeptide gene family in Caenorhabditis elegans . Brain Res 1999, 848:26–34.
70. Salkoff L, Butler A, Fawcett G, Kunkel M, McArdle C, Paz-y-Mino G, Nonet M, Walton N, Wang ZW, Yuan A, et al. Evolution tunes the excitability of individual neurons. Neuroscience 2001, 103:853–859.
71. Tsalik EL, Niacaris T, Wenick AS, Pau K, Avery L, Hobert O . LIM homeobox gene-dependent expression of biogenic amine receptors in restricted regions of the C. elegans nervous system. Dev Biol 2003, 263:81–102.
72. Hunt-Newbury R, Viveiros R, Johnsen R, Mah A, Anastas D, Fang L, Halfnight E, Lee D, Lin J, Lorch A, et al. High-throughput in vivo analysis of gene expression in Caenorhabditis elegans . PLoS Biol 2007, 5:e237.
73. Sunkin SM, Ng L, Lau C, Dolbeare T, Gilbert TL, Thompson CL, Hawrylycz M, Dang C . Allen Brain Atlas: an integrated spatio-temporal portal for exploring the central nervous system. Nucleic Acids Res 2013, 41:D996–D1008.
74. Jenett A, Rubin GM, Ngo TT, Shepherd D, Murphy C, Dionne H, Pfeiffer BD, Cavallaro A, Hall D, Jeter J, et al. A GAL4-driver line resource for Drosophila neurobiology. Cell Rep 2012, 2:991–1001.
75. Hobert O . The neuronal genome of Caenorhabditis elegans . WormBook 2013:1–106. PMID: 18050433.
76. McIntire SL, Jorgensen E, Horvitz HR . Genes required for GABA function in Caenorhabditis elegans . Nature 1993, 364:334–337.
77. Chase DL, Koelle MR . Biogenic amine neurotransmitters in C. elegans . WormBook 2007:1–15. PMID: 18050433.
78. Serrano-Saiz E, Poole RJ, Felton T, Zhang F, De La Cruz ED, Hobert O . Modular control of glutamatergic neuronal identity in C. elegans by distinct homeodomain proteins. Cell 2013, 155:659–673.
79. Duggan A, Chalfie M . Control of neuronal development in Caenorhabditis elegans . Curr Opin Neurobiol 1995, 5:6–9.
80. Hobert O . Development of left/right asymmetry in the Caenorhabditis elegans nervous system: from zygote to postmitotic neuron. Genesis 2014, 52:528–543.
81. Hsieh YW, Alqadah A, Chuang CF . Asymmetric neural development in the Caenorhabditis elegans olfactory system. Genesis 2014, 52:544–554.
82. Doitsidou M, Flames N, Topalidou I, Abe N, Felton T, Remesal L, Popovitchenko T, Mann R, Chalfie M, Hobert O . A combinatorial regulatory signature controls terminal differentiation of the dopaminergic nervous system in C. elegans . Genes Dev 2013, 27:1391–1405.
83. Flames N, Hobert O . Gene regulatory logic of dopamine neuron differentiation. Nature 2009, 458:885–889.
84. Kagoshima H, Kohara Y . Co-expression of the transcription factors CEH-14 and TTX-1 regulates AFD neuron-specific genes gcy-8 and gcy-18 in C. elegans . Dev Biol 2015, 399:325–336.
85. Van Buskirk C, Sternberg PW . Paired and LIM class homeodomain proteins coordinate differentiation of the C. elegans ALA neuron. Development 2010, 137:2065–2074.
86. Gendrel M, Hobert O . Transcription factor combinations specifying the GABAergic nervous system of C. elegans . In preparation.
87. Zhang Y, Ma C, Delohery T, Nasipak B, Foat BC, Bounoutas A, Bussemaker HJ, Kim SK, Chalfie M . Identification of genes expressed in C. elegans touch receptor neurons. Nature 2002, 418:331–335.
88. Gramstrup Petersen J, Rojo Romanos T, Juozaityte V, Redo Riveiro A, Hums I, Traunmüller L, Zimmer M, Pocock R . EGL-13/SoxD specifies distinct O2 and CO2 sensory neuron fates in Caenorhabditis elegans . PLoS Genet 2013, 9:e1003511.
89. Qin H, Powell-Coffman JA . The Caenorhabditis elegans aryl hydrocarbon receptor, AHR-1, regulates neuronal development. Dev Biol 2004, 270:64–75.
90. Feng G, Yi P, Yang Y, Chai Y, Tian D, Zhu Z, Liu J, Zhou F, Cheng Z, Wang X, et al. Developmental stage-dependent transcriptional regulatory pathways control neuroblast lineage progression. Development 2013, 140:3838–3847.
91. Etchberger JF, Lorch A, Sleumer MC, Zapf R, Jones SJ, Marra MA, Holt RA, Moerman DG, Hobert O . The molecular signature and cis-regulatory architecture of a C. elegans gustatory neuron. Genes Dev 2007, 21:1653–1674.
92. Sarafi-Reinach TR, Melkman T, Hobert O, Sengupta P . The lin-11 LIM homeobox gene specifies olfactory and chemosensory neuron fates in C. elegans . Development 2001, 128:3269–3281.
93. Baran R, Aronoff R, Garriga G . The C. elegans homeodomain gene unc-42 regulates chemosensory and glutamate receptor expression. Development 1999, 126:2241–2251.
94. Kim K, Colosimo ME, Yeung H, Sengupta P . The UNC-3 Olf/EBF protein represses alternate neuronal programs to specify chemosensory neuron identity. Dev Biol 2005, 286:136–148.
95. Prasad BC, Ye B, Zackhary R, Schrader K, Seydoux G, Reed RR . 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.
96. Gonzalez-Barrios M, Fierro-González JC, Krpelanova E, Mora-Lorca JA, Pedrajas JR, Peñate X, Chavez S, Swoboda P, Gert Jansen, Miranda-Vizuete A . Cis- and trans-regulatory mechanisms of gene expression in the ASJ sensory neuron of Caenorhabditis elegans . Genetics 2015, 200:123–134.
97. Alqadah A, Hsieh YW, Vidal B, Chang C, Hobert O, Chuang CF . Postmitotic diversification of olfactory neuron types is mediated by differential activities of the HMG-box transcription factor SOX-2. EMBO J 2015, 34:2574–2589.
98. Sagasti A, Hisamoto N, Hyodo J, Tanaka-Hino M, Matsumoto K, Bargmann CI . The CaMKII UNC-43 activates the MAPKKK NSY-1 to execute a lateral signaling decision required for asymmetric olfactory neuron fates. Cell 2001, 105:221–232.
99. Nokes EB, Van Der Linden AM, Winslow C, Mukhopadhyay S, Ma K, Sengupta P . Cis-regulatory mechanisms of gene expression in an olfactory neuron type in Caenorhabditis elegans . Dev Dyn 2009, 238:3080–3092.
100. Lanjuin A, VanHoven MK, Bargmann CI, Thompson JK, Sengupta P . Otx/otd homeobox genes specify distinct sensory neuron identities in C. elegans . Dev Cell 2003, 5:621–633.
101. Koga M, Ohshima Y . The C. elegans ceh-36 gene encodes a putative homemodomain transcription factor involved in chemosensory functions of ASE and AWC neurons. J Mol Biol 2004, 336:579–587.
102. Rojo Romanos T, Petersen JG, Riveiro AR, Pocock R . A novel role for the zinc-finger transcription factor EGL-46 in the differentiation of gas-sensing neurons in Caenorhabditis elegans . Genetics 2015, 199:157–163.
103. Brandt JP, Aziz-Zaman S, Juozaityte V, Martinez-Velazquez LA, Petersen JG, Pocock R, Ringstad N . A single gene target of an ETS-family transcription factor determines neuronal CO2-chemosensitivity. PLoS One 2012, 7:e34014.
104. Vidal B, Santella A, Serrano-Saiz E, Bao Z, Chuang CF, Hobert O . C. elegans SoxB genes are dispensable for embryonic neurogenesis but required for terminal differentiation of specific neuron types. Development 2015, 142:2464–2477.
105. Shaham S, Bargmann CI . Control of neuronal subtype identity by the C. elegans ARID protein CFI-1. Genes Dev 2002, 16:972–983.
106. Zheng C, Diaz-Cuadros M, Chalfie M . Hox Genes promote neuronal subtype diversification through posterior induction in Caenorhabditis elegans . Neuron 2015, 88:514–527.
107. Zhang F, Bhattacharya A, Nelson JC, Abe N, Gordon P, Lloret-Fernandez C, Maicas M, Flames N, Mann RS, Colón-Ramos DA, 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.
108. Altun-Gultekin Z, Andachi Y, Tsalik EL, 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.
109. Sze JY, 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.
110. Kage E, Hayashi Y, Takeuchi H, Hirotsu T, Kunitomo H, Inoue T, Arai H, Iino Y, Kubo T . MBR-1, a novel helix-turn-helix transcription factor, is required for pruning excessive neurites in Caenorhabditis elegans . Curr Biol 2005, 15:1554–1559.
111. Wightman B, Ebert B, Carmean N, Weber K, Clever S . The C. elegans nuclear receptor gene fax-1 and homeobox gene unc-42 coordinate interneuron identity by regulating the expression of glutamate receptor subunits and other neuron-specific genes. Dev Biol 2005, 287:74–85.
112. Brockie PJ, Madsen DM, Zheng Y, Mellem J, Maricq AV . Differential expression of glutamate receptor subunits in the nervous system of Caenorhabditis elegans and their regulation by the homeodomain protein UNC-42. J Neurosci 2001, 21:1510–1522.
113. Schmid C, Schwarz V, Hutter H . AST-1, a novel ETS-box transcription factor, controls axon guidance and pharynx development in C. elegans . Dev Biol 2006, 293:403–413.
114. Wightman B, Baran R, Garriga G . Genes that guide growth cones along the C. elegans ventral nerve cord. Development 1997, 124:2571–2580.
115. Gordon PM, Hobert O . A competition mechanism for a homeotic neuron identity transformation in C. elegans . Dev Cell 2015, 34:206–219.
116. Cameron S, Clark SG, McDermott JB, Aamodt E, Horvitz HR . PAG-3, a Zn-finger transcription factor, determines neuroblast fate in C. elegans . Development 2002, 129:1763–1774.
117. Clark SG, Chiu C . C. elegans ZAG-1, a Zn-finger-homeodomain protein, regulates axonal development and neuronal differentiation. Development 2003, 130:3781–3794.
118. Wacker I, Schwarz V, Hedgecock EM, Hutter H . zag-1, a Zn-finger homeodomain transcription factor controlling neuronal differentiation and axon outgrowth in C. elegans . Development 2003, 130:3795–3805.
119. Hobert O, Tessmar K, Ruvkun G . The Caenorhabditis elegans lim-6 LIM homeobox gene regulates neurite outgrowth and function of particular GABAergic neurons. Development 1999, 126:1547–1562.
120. Aurelio O, Boulin T, Hobert O . Identification of spatial and temporal cues that regulate postembryonic expression of axon maintenance factors in the C. elegans ventral nerve cord. Development 2003, 130:599–610.
121. Kratsios P, Stolfi A, Levine M, Hobert O . Coordinated regulation of cholinergic motor neuron traits through a conserved terminal selector gene. Nat Neurosci 2011, 15:205–214.
122. Winnier AR, Meir JY, Ross JM, Tavernarakis N, Driscoll M, Ishihara T, Katsura I, Miller DM 3rd. UNC-4/UNC-37-dependent repression of motor neuron-specific genes controls synaptic choice in Caenorhabditis elegans . Genes Dev 1999, 13:2774–2786.
123. Lickteig KM, Duerr JS, Frisby DL, Hall DH, Rand JB, Miller DM 3rd. Regulation of neurotransmitter vesicles by the homeodomain protein UNC-4 and its transcriptional corepressor UNC-37/groucho in Caenorhabditis elegans cholinergic motor neurons. J Neurosci 2001, 21:2001–14.
124. Prasad B, Karakuzu O, Reed RR, Cameron S . unc-3-dependent repression of specific motor neuron fates in Caenorhabditis elegans . Dev Biol 2008, 323:207–215.
125. Esmaeili B, Ross JM, Neades C, Miller DM 3rd, Ahringer J . The C. elegans even-skipped homologue, vab-7, specifies DB motoneurone identity and axon trajectory. Development 2002, 129:853–862.
126. Cinar H, Keles S, Jin Y . Expression profiling of GABAergic motor neurons in Caenorhabditis elegans . Curr Biol 2005, 15:340–346.
127. Jin Y, Hoskins R, Horvitz HR . Control of type-D GABAergic neuron differentiation by C. elegans UNC-30 homeodomain protein. Nature 1994, 372:780–783.
128. Eastman C, Horvitz HR, 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. J Neurosci 1999, 19:6225–6234.
129. Petersen SC, Watson JD, Richmond JE, Sarov M, Walthall WW, Miller DM 3rd. A transcriptional program promotes remodeling of GABAergic synapses in Caenorhabditis elegans . J Neurosci 2011, 31:15362–15375.
130. Lloret C, et al. Deep homology of a genetic programs controlling serotonergic neuron differentiation in nematodes and mammals. In preparation.
131. Richard JP, Zuryn S, Fischer N, Pavet V, Vaucamps N, Jarriault S . Direct in vivo cellular reprogramming involves transition through discrete, non-pluripotent steps. Development 2011, 138:1483–1492.
132. Sarin S, Antonio C, Tursun B, Hobert O . The C. elegans Tailless/TLX transcription factor nhr-67 controls neuronal identity and left/right asymmetric fate diversification. Development 2009, 136:2933–2944.
133. Kim J, Yeon J, Choi SK, Huh YH, Fang Z, Park SJ, Kim MO, Ryoo ZY, Kang K, Kweon HS, et al. The evolutionarily conserved LIM homeodomain protein LIM-4/LHX6 specifies the terminal identity of a cholinergic and peptidergic C. elegans sensory/inter/motor neuron-type. PLoS Genet 2015, 11:e1005480.
134. Von Stetina SE, Fox RM, Watkins KL, Starich TA, Shaw JE, Miller DM 3rd. UNC-4 represses CEH-12/HB9 to specify synaptic inputs to VA motor neurons in C. elegans . Genes Dev 2007, 21:332–346.
135. Melkman T, Sengupta P . Regulation of chemosensory and GABAergic motor neuron development by the C. elegans Aristaless/Arx homolog alr-1. Development 2005, 132:1935–1949.
136. Zhou HM, Walthall WW . UNC-55, an orphan nuclear hormone receptor, orchestrates synaptic specificity among two classes of motor neurons in Caenorhabditis elegans . J Neurosci 1998, 18:10438–10444.
137. Deneris ES, Hobert O . Maintenance of postmitotic neuronal cell identity. Nat Neurosci 2014, 17:899–907.
138. Etchberger JF, Hobert O . Vector-free DNA constructs improve transgene expression in C. elegans . Nat Methods 2008, 5:3.
139. Hobert O . Terminal selectors of neuronal identity. Curr Top Dev Biol 2016, 116:455–475.
140. Xue D, Tu Y, Chalfie M . Cooperative interactions between the Caenorhabditis elegans homeoproteins UNC-86 and MEC-3. Science 1993, 261:1324–1328.
141. Tursun B, Patel T, Kratsios P, Hobert O . Direct conversion of C. elegans germ cells into specific neuron types. Science 2011, 331:304–308.
142. Alon U . Network motifs: theory and experimental approaches. Nat Rev Genet 2007, 8:450–461.
143. Hobert O . Maintaining a memory by transcriptional autoregulation. Curr Biol 2011, 21:R146–R147.
144. Etchberger JF, Flowers EB, Poole RJ, Bashllari E, Hobert O . Cis-regulatory mechanisms of left/right asymmetric neuron-subtype specification in C. elegans . Development 2009, 136:147–160.
145. Hobert O . Neurogenesis in the nematode Caenorhabditis elegans . WormBook 2010:1–24. PMID: 20891032.
146. Johnston RJ Jr, Copeland JW, Fasnacht M, Etchberger JF, Liu J, Honig B, Hobert O . An unusual Zn-finger/FH2 domain protein controls a left/right asymmetric neuronal fate decision in C. elegans . Development 2006, 133:3317–3328.
147. Caicedo A, Pereira E, Margolskee RF, Roper SD . Role of the G-protein subunit alpha-gustducin in taste cell responses to bitter stimuli. J Neurosci 2003, 23:9947–9952.
148. Chang S, Johnston RJ Jr, Hobert O . A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C. elegans . Genes Dev 2003, 17:2123–2137.
149. Pflugrad A, Meir JY, Barnes TM, Miller DM 3rd . The Groucho-like transcription factor UNC-37 functions with the neural specificity gene unc-4 to govern motor neuron identity in C. elegans . Development 1997, 124:1699–1709.
150. O'Meara MM, Bigelow H, Flibotte S, Etchberger JF, Moerman DG, Hobert O . Cis-regulatory mutations in the Caenorhabditis elegans homeobox gene locus cog-1 affect neuronal development. Genetics 2009, 181:1679–1686.
151. Sarin S, O'Meara MM, Flowers EB, Antonio C, Poole RJ, Didiano D, Johnston RJ Jr, Chang S, Narula S, Hobert O . Genetic screens for Caenorhabditis elegans mutants defective in left/right asymmetric neuronal fate specification. Genetics 2007, 176:2109–2130.
152. Stefanakis N, Carrera I, Hobert O . Regulatory logic of pan-neuronal gene expression in C. elegans . Neuron 2015, 87:733–750.
153. Kaletta T, Schnabel H, Schnabel R . Binary specification of the embryonic lineage in Caenorhabditis elegans . Nature 1997, 390:294–298.
154. Lin R, Hill RJ, Priess JR . POP-1 and anterior-posterior fate decisions in C. elegans embryos. Cell 1998, 92:229–239.
155. Mizumoto K, Sawa H . Two betas or not two betas: regulation of asymmetric division by beta-catenin. Trends Cell Biol 2007, 17:465–473.
156. Bertrand V, Hobert O . Linking asymmetric cell division to the terminal differentiation program of postmitotic neurons in C. elegans . Dev Cell 2009, 16:563–575.
157. Bertrand V, Hobert O . Lineage programming: navigating through transient regulatory states via binary decisions. Curr Opin Genet Dev 2010, 20:362–368.
158. Murgan S, Kari W, Rothbächer U, Iché-Torres M, Mélénec P, Hobert O, Bertrand V . Atypical transcriptional activation by TCF via a Zic transcription factor in C. elegans neuronal precursors. Dev Cell 2015, 33:737–745.
159. Hobert O . Regulation of terminal differentiation programs in the nervous system. Annu Rev Cell Dev Biol 2011, 27:681–696.
160. Poole RJ, Bashllari E, Cochella L, Flowers EB, Hobert O . A genome-wide RNAi screen for factors involved in neuronal specification in Caenorhabditis elegans . PLoS Genet 2011, 7:e1002109.
161. Zhang Y, Emmons SW . Specification of sense-organ identity by a Caenorhabditis elegans Pax-6 homologue. Nature 1995, 377:55–59.
162. Baumeister R, Liu Y, Ruvkun G . Lineage-specific regulators couple cell lineage asymmetry to the transcription of the Caenorhabditis elegans POU gene unc-86 during neurogenesis. Genes Dev 1996, 10:1395–1410.
163. Reiprich S, Wegner M. From CNS stem cells to neurons and glia: Sox for everyone. Cell Tissue Res 2015, 359:111–124.
164. Good K, Ciosk R, Nance J, Neves A, Hill RJ, Priess JR . The T-box transcription factors TBX-37 and TBX-38 link GLP-1/Notch signaling to mesoderm induction in C. elegans embryos. Development 2004, 131:1967–1978.
165. Walton T, Preston E, Nair G, Zacharias AL, Raj A, Murray JI . The Bicoid class homeodomain factors ceh-36/OTX and unc-30/PITX cooperate in C. elegans embryonic progenitor cells to regulate robust development. PLoS Genet 2015, 11:e1005003.
166. Ruvkun G, Hobert O . The taxonomy of developmental control in Caenorhabditis elegans . Science 1998, 282:2033–2041.
167. Brenner S . The genetics of behavior. Br Med Bull 1973, 29:269–271.
168. Du Z, Santella A, He F, Shah PK, Kamikawa Y, Bao Z . The regulatory landscape of lineage differentiation in a metazoan embryo. Dev Cell 2015, 34:592–607.