The UNC-3 Olf/EBF protein represses alternate neuronal programs to specify chemosensory neuron identity

Developmental Biology

Volumn 286, Issue 1, 2005, Pages 136-148

  Kim, Kyuhyung ^a   Colosimo, Marc E ^a,b   Yeung, Helen ^a   Sengupta, Piali ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b MITRE CORPORATION   (United States)

Author keywords

ASI; Caenorhabditis elegans; Chemosensory neuron; Olf EBF; unc 3

Indexed keywords

EARLY B CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CAENORHABDITIS ELEGANS; CELL MATURATION; CHEMOSENSITIVITY; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION REGULATION; GENE REPRESSION; GENETIC CONSERVATION; MODEL; MOLECULAR BIOLOGY; NONHUMAN; OLFACTORY NERVE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

CAENORHABDITIS ELEGANS;

EID: 25844503698     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2005.07.024     Document Type: Article

References (76)

1. M. Ailion, and J.H. Thomas Dauer formation induced by high temperatures in Caenorhabditis elegans Genetics 156 2000 1047 1067
2. S. Arber, B. Han, M. Mendelsohn, M. Smith, T.M. Jessell, and S. Sockanathan Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity Neuron 23 1999 659 674
3. K.T. Arndt, C. Styles, and G.R. Fink Multiple global regulators control HIS4 transcription in yeast Science 237 1987 874 880
4. C.I. Bargmann, and H.R. Horvitz Control of larval development by chemosensory neurons in Caenorhabditis elegans Science 251 1991 1243 1246
5. C.I. Bargmann, and I. Mori Chemotaxis and thermotaxis D.S. Riddle T. Blumenthal B.J. Meyer J.R. Priess C. elegans II 1997 Cold Spring Harbor Press Cold Spring Harbor 717 737
6. C.I. Bargmann, E. Hartwieg, and H.R. Horvitz Odorant-selective genes and neurons mediate olfaction in C. elegans Cell 74 1993 515 527
7. S. Chang, R.J. Johnston Jr., and O. Hobert A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C. elegans Genes Dev. 17 2003 2123 2137
8. S. Chang, R.J. Johnston Jr., C. Frokjaer-Jensen, S. Lockery, and O. Hobert MicroRNAs act sequentially and asymmetrically to control chemosensory laterality in the nematode Nature 430 2004 785 789
9. L.S. da Graca, K.K. Zimmerman, M.C. Mitchell, M. Kozhan-Gorodetska, K. Sekiewicz, Y. Morales, and G.I. Patterson DAF-5 is a Ski oncoprotein homolog that functions in a neuronal TGF beta pathway to regulate C. elegans dauer development Development 131 2004 435 446
10. M. Driscoll, and M. Chalfie The mec-4 gene is a member of a family of Caenorhabditis elegans genes that can mutate to induce neuronal degeneration Nature 349 1991 588 593
11. L. Dubois, and A. Vincent The COE-Collier/Olf1/EBF-transcription factors: structural conservation and diversity of developmental functions Mech. Dev. 108 2001 3 12
12. J. Ericson, P. Rashbass, A. Schedl, S. Brenner-Morton, A. Kawakami, V. van Heyningen, T.M. Jessell, and J. Briscoe Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling Cell 90 1997 169 180
13. M. Garcia-Dominguez, C. Poquet, S. Garel, and P. Charnay Ebf gene function is required for coupling neuronal differentiation and cell cycle exit Development 130 2003 6013 6025
14. S. Garel, F. Marin, R. Grosschedl, and P. Charnay Ebf1 controls early cell differentiation in the embryonic striatum Development 126 1999 5285 5294
15. J. Hirota, and P. Mombaerts The LIM-homeodomain protein Lhx2 is required for complete development of mouse olfactory sensory neurons Proc. Natl. Acad. Sci. U. S. A. 101 2004 8751 8755
16. O. Hobert PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans Biotechniques 32 2002 728 730
17. O. Hobert, K. Tessmar, and G. Ruvkun The Caenorhabditis elegans lim-6 LIM homeobox gene regulates neurite outgrowth and function of particular GABAergic neurons Development 126 1999 1547 1562
18. R. Hoppe, M. Weimer, A. Beck, H. Breer, and J. Strotmann Sequence analyses of the olfactory receptor gene cluster mOR37 on mouse chromosome 4 Genomics 66 2000 284 295
19. R. Hoppe, H. Frank, H. Breer, and J. Strotmann The clustered olfactory receptor gene family 262: genomic organization, promotor elements, and interacting transcription factors Genome Res. 13 2003 2674 2685
20. G. Jansen, K.L. Thijssen, P. Werner, M. van der Horst, E. Hazendonk, and R.H. Plasterk The complete family of genes encoding G proteins of Caenorhabditis elegans Nat. Genet. 21 1999 414 419
21. Y. Jin, E. Jorgensen, E. Hartwieg, and H.R. Horvitz The Caenorhabditis elegans gene unc-25 encodes glutamic acid decarboxylase and is required for synaptic transmission but not synaptic development J. Neurosci. 19 1999 539 548
22. R.J. Johnston Jr., and O. Hobert A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans Nature 426 2003 845 849
23. K. Kim, and C. Li Expression and regulation of an FMRFamide-related neuropeptide gene family in Caenorhabditis elegans J. Comp. Neurol. 475 2004 540 550
24. M. Koga, and Y. Ohshima The C. elegans ceh-36 gene encodes a putative homeodomain transcription factor involved in chemosensory functions of ASE and AWC neurons J. Mol. Biol. 336 2004 579 587
25. K. Kudrycki, C. Steinizsak, C. Behn, and M. Grillo Olf-1 binding site-Characterization of an olfactory neuron-specific promoter motif Mol. Cell. Biol. 13 1993 3002 3014
26. A. Lanjuin, and P. Sengupta Regulation of chemosensory receptor expression and sensory signaling by the KIN-29 Ser/Thr kinase Neuron 33 2002 369 381
27. A. Lanjuin, and P. Sengupta Specification of chemosensory neuron subtype identities in Caenorhabditis elegans Curr. Opin. Neurobiol. 14 2004 22 30
28. A. Lanjuin, M.K. VanHoven, C.I. Bargmann, J.K. Thompson, and P. Sengupta Otx/otd homeobox genes specify distinct sensory neuron identities in C. elegans Dev. Cell 5 2003 621 633
29. N.D. L'Etoile, and C.I. Bargmann Olfaction and odor discrimination are mediated by the C. elegans guanylyl cyclase ODR-1 Neuron 25 2000 575 586
30. J.W. Lewcock, and R.R. Reed A feedback mechanism regulates monoallelic odorant receptor expression Proc. Natl. Acad. Sci. U. S. A. 101 2004 1069 1074
31. D. Liberg, M. Sigvardsson, and P. Akerblad The EBF/Olf/Collier family of transcription factors: regulators of differentiation in cells originating from all three embryonal germ layers Mol. Cell. Biol. 22 2002 8389 8397
32. T. Melkman, and P. Sengupta The worm's sense of smell: development of functional diversity in the chemosensory system of C. elegans Dev. Biol. 265 2004 302 319
33. S. Mitani, H. Du, D.H. Hall, M. Driscoll, and M. Chalfie Combinatorial control of touch receptor neuron expression in Caenorhabditis elegans Development 119 1993 773 783
34. T. Mori, M. Sakai, I. Matsuoka, and K. Kurihara Analysis of promoter activity of 5′-upstream regions of zebrafish olfactory receptor genes Biol. Pharm. Bull. 23 2000 165 173
35. J. Muhr, E. Andersson, M. Persson, T.M. Jessell, and J. Ericson Groucho-mediated transcriptional repression establishes progenitor cell pattern and neuronal fate in the ventral neural tube Cell 104 2001 861 873
36. K.M. Nolan, T.R. Sarafi-Reinach, J.G. Horne, A.M. Saffer, and P. Sengupta The DAF-7 TGF-beta signaling pathway regulates chemosensory receptor gene expression in C. elegans Genes Dev. 16 2002 3061 3073
37. R.E. Palmer, T. Inoue, D.R. Sherwood, L.I. Jiang, and P.W. Sternberg Caenorhabditis elegans cog-1 locus encodes GTX/Nkx6.1 homeodomain proteins and regulates multiple aspects of reproductive system development Dev. Biol. 252 2002 202 213
38. G.I. Patterson, A. Koweek, A. Wong, Y. Liu, and G. Ruvkun The DAF-3 Smad protein antagonizes TGF-beta-related receptor signaling in the Caenorhabditis elegans dauer pathway Genes Dev. 11 1997 2679 2690
39. E.L. Peckol, E.R. Troemel, and C.I. Bargmann Sensory experience and sensory activity regulate chemosensory receptor gene expression in C. elegans Proc. Natl. Acad. Sci. U. S. A. 98 2001 11032 11038
40. J.T. Pierce-Shimomura, S. Faumont, M.R. Gaston, B.J. Pearson, and S.R. Lockery The homeobox gene lim-6 is required for distinct chemosensory representations in C. elegans Nature 410 2001 694 698
41. B.C. Prasad, B. Ye, R. Zackhary, K. Schrader, G. Seydoux, and R.R. Reed unc-3, a gene required for axonal guidance in Caenorhabditis elegans, encodes a member of the O/E family of transcription factors Development 125 1998 1561 1568
42. P. Ren, C.S. Lim, R. Johnsen, P.S. Albert, D. Pilgrim, and D.L. Riddle Control of C. elegans larval development by neuronal expression of a TGF-beta homolog Science 274 1996 1389 1391
43. D.L. Riddle, M.M. Swanson, and P.S. Albert Interacting genes in nematode dauer larva formation Nature 290 1981 668 671
44. A. Sagasti, O. Hobert, E.R. Troemel, G. Ruvkun, and C.I. Bargmann Alternative olfactory neuron fates are specified by the LIM homeobox gene lim-4 Genes Dev. 13 1999 1794 1806
45. A. Sagasti, N. Hisamoto, J. Hyodo, M. Tanaka-Hino, K. Matsumoto, and C.I. Bargmann The CaMKII UNC-43 activates the MAPKKK NSY-1 to execute a lateral signaling decision required for asymmetric olfactory neuron fates Cell 105 2001 221 232
46. W.S. Schackwitz, T. Inoue, and J.H. Thomas Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans Neuron 17 1996 719 728
47. P. Sengupta, H.A. Colbert, and C.I. Bargmann The C. elegans gene odr-7 encodes an olfactory-specific member of the nuclear receptor superfamily Cell 79 1994 971 980
48. P. Sengupta, J.H. Chou, and C.I. Bargmann odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl Cell 84 1996 899 909
49. S. Serizawa, K. Miyamichi, H. Nakatani, M. Suzuki, M. Saito, Y. Yoshihara, and H. Sakano Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse Science 302 2003 2088 2094
50. K. Sharma, H.Z. Sheng, K. Lettieri, H. Li, A. Karavanov, S. Potter, H. Westphal, and S.L. Pfaff LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons Cell 95 1998 817 828
51. R. Shirasaki, and S.L. Pfaff Transcriptional codes and the control of neuronal identity Annu. Rev. Neurosci. 25 2002 251 281
52. B.M. Shykind, S.C. Rohani, S. O'Donnell, A. Nemes, M. Mendelsohn, Y. Sun, R. Axel, and G. Barnea Gene switching and the stability of odorant receptor gene choice Cell 117 2004 801 815
53. J.E. Sulston, E. Schierenberg, J.G. White, and J.N. Thomson The embryonic cell lineage of the nematode Caenorhabditis elegans Dev. Biol. 100 1983 64 119
54. A. Tahayato, R. Sonneville, F. Pichaud, M.F. Wernet, D. Papatsenko, P. Beaufils, T. Cook, and C. Desplan Otd/Crx, a dual regulator for the specification of ommatidia subtypes in the Drosophila retina Dev. Cell 5 2003 391 402
55. Y. Tanabe, C. William, and T.M. Jessell Specification of motor neuron identity by the MNR2 homeodomain protein Cell 95 1998 67 80
56. J. Thaler, K. Harrison, K. Sharma, K. Lettieri, J. Kehrl, and S.L. Pfaff Active suppression of interneuron programs within developing motor neurons revealed by analysis of homeodomain factor HB9 Neuron 23 1999 675 687
57. J.H. Thomas, D.A. Birnby, and J.J. Vowels Evidence for parallel processing of sensory information controlling dauer formation in Caenorhabditis elegans Genetics 134 1993 1105 1117
58. D. Tobin, D. Madsen, A. Kahn-Kirby, E. Peckol, G. Moulder, R. Barstead, A. Maricq, and C. Bargmann Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons Neuron 35 2002 307 318
59. E.R. Troemel, A. Sagasti, and C.I. Bargmann Lateral signaling mediated by axon contact and calcium entry regulates asymmetric odorant receptor expression in C. elegans Cell 99 1999 387 398
60. R.Y. Tsai, and R.R. Reed Cloning and functional characterization of Roaz, a zinc finger protein that interacts with O/E-1 to regulate gene expression: implications for olfactory neuronal development J. Neurosci. 17 1997 4159 4169
61. R.Y. Tsai, and R.R. Reed Identification of DNA recognition sequences and protein interaction domains of the multiple-Zn-finger protein Roaz Mol. Cell. Biol. 18 1998 6447 6456
62. O. Uchida, H. Nakano, M. Koga, and Y. Ohshima The C. elegans che-1 gene encodes a zinc finger transcription factor required for specification of the ASE chemosensory neurons Development 130 2003 1215 1224
63. A. Vassalli, A. Rothman, P. Feinstein, M. Zapotocky, and P. Mombaerts Minigenes impart odorant receptor-specific axon guidance in the olfactory bulb Neuron 35 2002 681 696
64. M.G. Voas, and I. Rebay Signal integration during development: insights from the Drosophila eye Dev. Dyn. 229 2004 162 175
65. M. Wang, and R. Reed Molecular cloning of the olfactory neuronal transcription factor Olf-1 by genetic selection in yeast Nature 364 1993 121 126
66. M.M. Wang, R.Y.L. Tsai, K.A. Scrader, and R.A. Reed Genes encoding components of the olfactory signal transduction cascade contain a DNA binding site that may direct neuronal expression Mol. Cell. Biol. 13 1993 5805 5813
67. S.S. Wang, R.Y.L. Tsai, and R.R. Reed The characterization of the Olf-1/EBF-like HLH transcription factor family: implications in olfactory gene regulation and neuronal development J. Neurosci. 17 1997 4149 4158
68. S.S. Wang, A.G. Betz, and R.R. Reed Cloning of a novel Olf-1/EBF-like gene, O/E-4, by degenerate oligo-based direct selection Mol. Cell. Neurosci. 20 2002 404 414
69. S.S. Wang, J.W. Lewcock, P. Feinstein, P. Mombaerts, and R.R. Reed Genetic disruptions of O/E2 and O/E3 genes reveal involvement in olfactory receptor neuron projection Development 131 2004 1377 1388
70. S. Ward, N. Thomson, J.G. White, and S. Brenner Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans J. Comp. Neurol. 160 1975 313 337
71. J.C. Way, and M. Chalfie mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans Cell 54 1988 5 16
72. A.S. Wenick, and O. Hobert Genomic cis-regulatory architecture and trans-acting regulators of a single interneuron-specific gene battery in C. elegans Dev. Cell 6 2004 757 770
73. J.G. White, E. Southgate, J.N. Thomson, and S. Brenner The structure of the nervous system of the nematode Caenorhabditis elegans Philos. Trans. R. Soc. Lond., Ser. B Biol. Sci. 314 1986 1 340
74. B. Wightman, R. Baran, and G. Garriga Genes that guide growth cones along the C. elegans ventral nerve cord Development 124 1997 2571 2580
75. S. Yu, L. Avery, E. Baude, and D.A. Garbers Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors Proc. Natl. Acad. Sci. U. S. A. 94 1997 3384 3387
76. F. Zhao, R. McCarrick-Walmsley, P. Akerblad, M. Sigvardsson, and T. Kadesch Inhibition of p300/CBP by early B-cell factor Mol. Cell. Biol. 23 2003 3837 3846