The LIM and POU homeobox genes ttx-3 and unc-86 act as terminal selectors in distinct cholinergic and serotonergic neuron types

Development (Cambridge)

Volumn 141, Issue 2, 2014, Pages 422-435

  Zhang, Feifan ^a   Bhattacharya, Abhishek ^a   Nelson, Jessica C ^b   Abe, Namiko ^a   Gordon, Patricia ^a   Lloret Fernandez, Carla ^c   Maicas, Miren ^c   Flames, Nuria ^a,c   Mann, Richard S ^a   Colón Ramos, Daniel A ^b   Hobert, Oliver ^a  

^a NewYork Presbyterian Hospital   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

Author keywords

Caenorhabditis elegans; Homeobox; Neuron differentiation

Indexed keywords

NEUROPEPTIDE; NEUROTRANSMITTER; NEUROTRANSMITTER RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TTX 3; TRANSCRIPTION FACTOR UNC 86; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CHOLINERGIC NERVE CELL; INTERNEURON; MOTONEURON; NERVE CELL DIFFERENTIATION; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SEROTONINERGIC NERVE CELL;

EID: 84891536562     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.099721     Document Type: Article

References (62)

1. Albertson, D. G. and Thomson, J. N. (1976). The pharynx of Caenorhabditis elegans. Philos. Trans. R. Soc. B 275, 299-325.
2. Altun, Z. F., Herndon, L. A., Crocker, C., Lints, R. and Hall, D. H. (eds) (2002-2013). WormAtlas, http://www.wormatlas.org.
3. Altun-Gultekin, Z., Andachi, Y., Tsalik, E. L., Pilgrim, D., Kohara, Y. and Hobert, O. (2001). 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, 1951-1969.
4. Aspöck, G., Ruvkun, G. and Bürglin, T. R. (2003). The Caenorhabditis elegans ems class homeobox gene ceh-2 is required for M3 pharynx motoneuron function. Development 130, 3369-3378.
5. Axäng, C., Rauthan, M., Hall, D. H. and Pilon, M. (2008). Developmental genetics of the C. elegans pharyngeal neurons NSML and NSMR. BMC Dev. Biol. 8, 38.
6. Baumeister, R., Liu, Y. and Ruvkun, G. (1996). Lineage-specific regulators couple cell lineage asymmetry to the transcription of the Caenorhabditis elegans POU gene unc-86 during neurogenesis. Genes Dev. 10, 1395-1410.
7. Berger, M. F., Badis, G., Gehrke, A. R., Talukder, S., Philippakis, A. A., Peña-Castillo, L., Alleyne, T. M., Mnaimneh, S., Botvinnik, O. B., Chan, E. T. et al. (2008). Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 133, 1266-1276.
8. Bertrand, V. and Hobert, O. (2009). Linking asymmetric cell division to the terminal differentiation program of postmitotic neurons in C. elegans. Dev. Cell 16, 563-575.
9. Clark, S. G. and Chiu, C. (2003). C. elegans ZAG-1, a Zn-finger-homeodomain protein, regulates axonal development and neuronal differentiation. Development 130, 3781-3794.
10. Deneris, E. S. and Wyler, S. C. (2012). Serotonergic transcriptional networks and potential importance to mental health. Nat. Neurosci. 15, 519-527.
11. Desai, C., Garriga, G., McIntire, S. L. and Horvitz, H. R. (1988). A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature 336, 638-646.
12. Ditch, L. M., Shirangi, T., Pitman, J. L., Latham, K. L., Finley, K. D., Edeen, P. T., Taylor, B. J. and McKeown, M. (2005). Drosophila retained/dead ringer is necessary for neuronal pathfinding, female receptivity and repression of fruitless independent male courtship behaviors. Development 132, 155-164.
13. Doitsidou, M., Flames, N., Topalidou, I., Abe, N., Felton, T., Remesal, L., Popovitchenko, T., Mann, R., Chalfie, M. and Hobert, O. (2013). A combinatorial regulatory signature controls terminal differentiation of the dopaminergic nervous system in C. elegans. Genes Dev. 27, 1391-1405.
14. Duggan, A., Ma, C. and Chalfie, M. (1998). Regulation of touch receptor differentiation by the Caenorhabditis elegans mec-3 and unc-86 genes. Development 125, 4107-4119.
15. 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. (2007). The molecular signature and cis-regulatory architecture of a C. elegans gustatory neuron. Genes Dev. 21, 1653-1674.
16. Finney, M. and Ruvkun, G. (1990). The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell 63, 895-905.
17. Flames, N. and Hobert, O. (2009). Gene regulatory logic of dopamine neuron differentiation. Nature 458, 885-889.
18. Gray, P. A., Fu, H., Luo, P., Zhao, Q., Yu, J., Ferrari, A., Tenzen, T., Yuk, D. I., Tsung, E. F., Cai, Z. et al. (2004). Mouse brain organization revealed through direct genome-scale TF expression analysis. Science 306, 2255-2257.
19. Greer, E. R., Perez, C. L., Van Gilst, M. R., Lee, B. H. and Ashrafi, K. (2008). Neural and molecular dissection of a C. elegans sensory circuit that regulates fat and feeding. Cell Metab. 8, 118-131.
20. Harris, G., Korchnak, A., Summers, P., Hapiak, V., Law, W. J., Stein, A. M., Komuniecki, P. and Komuniecki, R. (2011). Dissecting the serotonergic food signal stimulating sensory-mediated aversive behavior in C. elegans. PLoS ONE 6, e21897.
21. Hirota, J. and Mombaerts, P. (2004). The LIM-homeodomain protein Lhx2 is required for complete development of mouse olfactory sensory neurons. Proc. Natl. Acad. Sci. USA 101, 8751-8755.
22. Hobert, O. (2008). Regulatory logic of neuronal diversity: terminal selector genes and selector motifs. Proc. Natl. Acad. Sci. USA 105, 20067-20071.
23. Hobert, O. (2011). Regulation of terminal differentiation programs in the nervous system. Annu. Rev. Cell Dev. Biol. 27, 681-696.
24. Hobert, O. and Ruvkun, G. (1998). A common theme for LIM homeobox gene function across phylogeny? Biol. Bull. 195, 377-380.
25. Hobert, O. and Westphal, H. (2000). Functions of LIM-homeobox genes. Trends Genet. 16, 75-83.
26. Hobert, O., Mori, I., Yamashita, Y., Honda, H., Ohshima, Y., Liu, Y. and Ruvkun, G. (1997). Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron 19, 345-357.
27. Horvitz, H. R., Chalfie, M., Trent, C., Sulston, J. E. and Evans, P. D. (1982). Serotonin and octopamine in the nematode Caenorhabditis elegans. Science 216, 1012-1014.
28. Jafari, G., Xie, Y., Kullyev, A., Liang, B. and Sze, J. Y. (2011). Regulation of extrasynaptic 5-HT by serotonin reuptake transporter function in 5-HT-absorbing neurons underscores adaptation behavior in Caenorhabditis elegans. J. Neurosci. 31, 8948-8957.
29. Kolterud, A., Alenius, M., Carlsson, L. and Bohm, S. (2004). The Lim homeobox gene Lhx2 is required for olfactory sensory neuron identity. Development 131, 5319-5326.
30. Lee, M. H. and Salvaterra, P. M. (2002). Abnormal chemosensory jump 6 is a positive transcriptional regulator of the cholinergic gene locus in Drosophila olfactory neurons. J. Neurosci. 22, 5291-5299.
31. Lee, R. Y., Sawin, E. R., Chalfie, M., Horvitz, H. R. and Avery, L. (1999). EAT-4, a homolog of a mammalian sodium-dependent inorganic phosphate cotransporter, is necessary for glutamatergic neurotransmission in caenorhabditis elegans. J. Neurosci. 19, 159-167.
32. Lee, H., Choi, M. K., Lee, D., Kim, H. S., Hwang, H., Kim, H., Park, S., Paik, Y. K. and Lee, J. (2012). Nictation, a dispersal behavior of the nematode Caenorhabditis elegans, is regulated by IL2 neurons. Nat. Neurosci. 15, 107-112.
33. Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J. et al. (2007). Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168-176.
34. Leung-Hagesteijn, C., Spence, A. M., Stern, B. D., Zhou, Y., Su, M. W., Hedgecock, E. M. and Culotti, J. G. (1992). UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migrations in C. elegans. Cell 71, 289-299.
35. Liu, C., Maejima, T., Wyler, S. C., Casadesus, G., Herlitze, S. and Deneris, E. S. (2010). Pet-1 is required across different stages of life to regulate serotonergic function. Nat. Neurosci. 13, 1190-1198.
36. Lopes, R., Verhey van Wijk, N., Neves, G. and Pachnis, V. (2012). Transcription factor LIM homeobox 7 (Lhx7) maintains subtype identity of cholinergic interneurons in the mammalian striatum. Proc. Natl. Acad. Sci. USA 109, 3119-3124.
37. Mangale, V. S., Hirokawa, K. E., Satyaki, P. R., Gokulchandran, N., Chikbire, S., Subramanian, L., Shetty, A. S., Martynoga, B., Paul, J., Mai, M. V. et al. (2008). Lhx2 selector activity specifies cortical identity and suppresses hippocampal organizer fate. Science 319, 304-309.
38. Moreno, N., Bachy, I., Rétaux, S. and González, A. (2005). LIM-homeodomain genes as territory markers in the brainstem of adult and developing Xenopus laevis. J. Comp. Neurol. 485, 240-254.
39. Nathoo, A. N., Moeller, R. A., Westlund, B. A. and Hart, A. C. (2001). Identification of neuropeptide-like protein gene families in Caenorhabditis elegans and other species. Proc. Natl. Acad. Sci. USA 98, 14000-14005.
40. Nelson, J. C. and Colón-Ramos, D. A. (2013). Serotonergic neurosecretory synapse targeting is controlled by netrin-releasing guidepost neurons in Caenorhabditis elegans. J. Neurosci. 33, 1366-1376.
41. Ortiz, C. O., Etchberger, J. F., Posy, S. L., Frøkjaer-Jensen, C., Lockery, S., Honig, B. and Hobert, O. (2006). Searching for neuronal left/right asymmetry: genomewide analysis of nematode receptor-type guanylyl cyclases. Genetics 173, 131-149.
42. Ouellet, J., Li, S. and Roy, R. (2008). Notch signalling is required for both dauer maintenance and recovery in C. elegans. Development 135, 2583-2592.
43. Peden, E. M. and Barr, M. M. (2005). The KLP-6 kinesin is required for male mating behaviors and polycystin localization in Caenorhabditis elegans. Curr. Biol. 15, 394-404.
44. Peukert, D., Weber, S., Lumsden, A. and Scholpp, S. (2011). Lhx2 and Lhx9 determine neuronal differentiation and compartition in the caudal forebrain by regulating Wnt signaling. PLoS Biol. 9, e1001218.
45. Ranganathan, R., Sawin, E. R., Trent, C. and Horvitz, H. R. (2001). Mutations in the Caenorhabditis elegans serotonin reuptake transporter MOD-5 reveal serotonindependent and-independent activities of fluoxetine. J. Neurosci. 21, 5871-5884.
46. Rhee, J. M., Gruber, C. A., Brodie, T. B., Trieu, M. and Turner, E. E. (1998). Highly cooperative homodimerization is a conserved property of neural POU proteins. J. Biol. Chem. 273, 34196-34205.
47. Röhrig, S. (2000). Modulation of UNC-86 Activity During Caenorhabditis elegans Neurogenesis. München, Germany: Herbert Utz Verlag.
48. Serrano-Saiz, E., Poole, R. J., Felton, T., Zhang, F., De La Cruz, E. and Hobert, O. (2013). Modular control of glutamatergic neuronal identity in C. elegans by distinct homeodomain proteins. Cell 155, 659-673.
49. Shaham, S. and Bargmann, C. I. (2002). Control of neuronal subtype identity by the C. elegans ARID protein CFI-1. Genes Dev. 16, 972-983.
50. Shinkai, Y., Yamamoto, Y., Fujiwara, M., Tabata, T., Murayama, T., Hirotsu, T., Ikeda, D. D., Tsunozaki, M., Iino, Y., Bargmann, C. I. et al. (2011). Behavioral choice between conflicting alternatives is regulated by a receptor guanylyl cyclase, GCY-28, and a receptor tyrosine kinase, SCD-2, in AIA interneurons of Caenorhabditis elegans. J. Neurosci. 31, 3007-3015.
51. Simmons, D. K., Pang, K. and Martindale, M. Q. (2012). Lim homeobox genes in the Ctenophore Mnemiopsis leidyi: the evolution of neural cell type specification. Evodevo 3, 2.
52. Smidt, M. P. and Burbach, J. P. (2009). Terminal differentiation of mesodiencephalic dopaminergic neurons: the role of Nurr1 and Pitx3. Adv. Exp. Med. Biol. 651, 47-57.
53. Srivastava, M., Larroux, C., Lu, D. R., Mohanty, K., Chapman, J., Degnan, B. M. and Rokhsar, D. S. (2010). Early evolution of the LIM homeobox gene family. BMC Biol. 8, 4.
54. Sulston, J. E., Schierenberg, E., White, J. G. and Thomson, J. N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64-119.
55. Sze, J. Y., Zhang, S., Li, J. and Ruvkun, G. (2002). The C. elegans POU-domain transcription factor UNC-86 regulates the tph-1 tryptophan hydroxylase gene and neurite outgrowth in specific serotonergic neurons. Development 129, 3901-3911.
56. Tomioka, M., Adachi, T., Suzuki, H., Kunitomo, H., Schafer, W. R. and Iino, Y. (2006). The insulin/PI 3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron 51, 613-625.
57. Tong, Y. G. and Bürglin, T. R. (2010). Conditions for dye-filling of sensory neurons in Caenorhabditis elegans. J. Neurosci. Methods 188, 58-61.
58. Treinin, M., Gillo, B., Liebman, L. and Chalfie, M. (1998). Two functionally dependent acetylcholine subunits are encoded in a single Caenorhabditis elegans operon. Proc. Natl. Acad. Sci. USA 95, 15492-15495.
59. Tursun, B., Cochella, L., Carrera, I. and Hobert, O. (2009). A toolkit and robust pipeline for the generation of fosmid-based reporter genes in C. elegans. PLoS ONE 4, e4625.
60. Wenick, A. S. and Hobert, O. (2004). Genomic cis-regulatory architecture and transacting regulators of a single interneuron-specific gene battery in C. elegans. Dev. Cell 6, 757-770.
61. White, J. G., Southgate, E., Thomson, J. N. and Brenner, S. (1986). The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. B 314, 1-340.
62. Zetterström, R. H., Williams, R., Perlmann, T. and Olson, L. (1996). Cellular expression of the immediate early transcription factors Nurr1 and NGFI-B suggests a gene regulatory role in several brain regions including the nigrostriatal dopamine system. Brain Res. Mol. Brain Res. 41, 111-120.