Sensory neuron fates are distinguished by a transcriptional switch that regulates dendrite branch stabilization

Neuron

Volumn 79, Issue 2, 2013, Pages 266-280

  Smith, Cody J ^a   O'Brien, Timothy ^a   Chatzigeorgiou, Marios ^b   Clay Spencer, W ^a   Feingold Link, Elana ^a   Husson, Steven J ^c,d   Hori, Sayaka ^e   Mitani, Shohei ^e   Gottschalk, Alexander ^c   Schafer, WilliamR ^b   Miller, DavidM ^a,f,g  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d GOETHE UNIVERSITY   (Germany)

^e TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^f VANDERBILT UNIVERSITY   (United States)

^g VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AHR 1 PROTEIN; AROMATIC HYDROCARBON RECEPTOR; BRAIN PROTEIN; CLAUDIN; MEC 3 PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ZAG 1 PROTEIN; ZINC FINGER PROTEIN;

ARTICLE; AVM CELL; CAENORHABDITIS ELEGANS; CELL FATE; CELL STRUCTURE; CONCENTRATION (PARAMETERS); DENDRITE; DENDRITE BRANCH STABILIZATION; MECHANORECEPTOR; NEURAL STEM CELL; NEUROMODULATION; NONHUMAN; PAIN RECEPTOR; PRIORITY JOURNAL; PROTEIN FUNCTION; PVD CELL; REGULATORY MECHANISM; SENSORY NERVE CELL; SENSORY RECEPTOR;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; DENDRITES; DENDRITIC SPINES; NEUROGENESIS; SENSORY RECEPTOR CELLS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84880670177     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.05.009     Document Type: Article

References (68)

1. Albeg A., Smith C.J., Chatzigeorgiou M., Feitelson D.G., Hall D.H., Schafer W.R., Miller D.M., Treinin M. C.elegans multi-dendritic sensory neurons: morphology and function. Mol. Cell. Neurosci. 2011, 46:308-317.
2. Bolstad B.M., Irizarry R.A., Astrand M., Speed T.P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003, 19:185-193.
3. Basbaum A.I., Bautista D.M., Scherrer G., Julius D. Cellular and molecular mechanisms of pain. Cell 2009, 139:267-284.
4. Chalfie M., Sulston J.E. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev. Biol. 1981, 82:358-370.
5. Chalfie M., Sulston J.E., White J.G., Southgate E., Thomson J.N., Brenner S. The neural circuit for touch sensitivity in Caenorhabditis elegans. J.Neurosci. 1985, 5:956-964.
6. Chatzigeorgiou M., Schafer W.R. Lateral facilitation between primary mechanosensory neurons controls nose touch perception in C. elegans. Neuron 2011, 70:299-309.
7. Chatzigeorgiou M., Grundy L., Kindt K.S., Lee W.H., Driscoll M., Schafer W.R. Spatial asymmetry in the mechanosensory phenotypes of the C. elegans DEG/ENaC gene mec-10. J.Neurophysiol. 2010, 104:3334-3344.
8. Chatzigeorgiou M., Yoo S., Watson J.D., Lee W.H., Spencer W.C., Kindt K.S., Hwang S.W., Miller D.M., Treinin M., Driscoll M., Schafer W.R. Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors. Nat. Neurosci. 2010, 13:861-868.
9. Clark S.G., Chiu C. C.elegans ZAG-1, a Zn-finger-homeodomain protein, regulates axonal development and neuronal differentiation. Development 2003, 130:3781-3794.
10. Conradt B., Horvitz H.R. The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein CED-9. Cell 1998, 93:519-529.
11. Cubelos B., Sebastián-Serrano A., Beccari L., Calcagnotto M.E., Cisneros E., Kim S., Dopazo A., Alvarez-Dolado M., Redondo J.M., Bovolenta P., et al. Cux1 and Cux2 regulate dendritic branching, spine morphology, and synapses of the upper layer neurons of the cortex. Neuron 2010, 66:523-535.
12. Delmas P., Hao J., Rodat-Despoix L. Molecular mechanisms of mechanotransduction in mammalian sensory neurons. Nat. Rev. Neurosci. 2011, 12:139-153.
13. Earls L.R., Hacker M.L., Watson J.D., Miller D.M. Coenzyme Q protects Caenorhabditis elegans GABA neurons from calcium-dependent degeneration. Proc. Natl. Acad. Sci. USA 2010, 107:14460-14465.
14. Geffeney S.L., Cueva J.G., Glauser D.A., Doll J.C., Lee T.H., Montoya M., Karania S., Garakani A.M., Pruitt B.L., Goodman M.B. DEG/ENaC but not TRP channels are the major mechanoelectrical transduction channels in a C. elegans nociceptor. Neuron 2011, 71:845-857.
15. Grueber W.B., Jan L.Y., Jan Y.N. Different levels of the homeodomain protein cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons. Cell 2003, 112:805-818.
16. Hahn M.E. Aryl hydrocarbon receptors: diversity and evolution. Chem. Biol. Interact. 2002, 141:131-160.
17. Halevi S., McKay J., Palfreyman M., Yassin L., Eshel M., Jorgensen E., Treinin M. The C. elegans ric-3 gene is required for maturation of nicotinic acetylcholine receptors. EMBO J. 2002, 21:1012-1020.
18. Hall D.H., Treinin M. How does morphology relate to function in sensory arbors?. Trends Neurosci. 2011, 34:443-451.
19. Han C., Wang D., Soba P., Zhu S., Lin X., Jan L.Y., Jan Y.N. Integrins regulate repulsion-mediated dendritic patterning of Drosophila sensory neurons by restricting dendrites in a 2D space. Neuron 2012, 73:64-78.
20. Huang X., Powell-Coffman J.A., Jin Y. The AHR-1 aryl hydrocarbon receptor and its co-factor the AHA-1 aryl hydrocarbon receptor nuclear translocator specify GABAergic neuron cell fate in C. elegans. Development 2004, 131:819-828.
21. Husson S.J., Costa W.S., Wabnig S., Stirman J.N., Watson J.D., Spencer W.C., Akerboom J., Looger L.L., Treinin M., Miller D.M., et al. Optogenetic analysis of a nociceptor neuron and network reveals ion channels acting downstream of primary sensors. Curr. Biol. 2012, 22:743-752.
22. Hwang R.Y., Zhong L., Xu Y., Johnson T., Zhang F., Deisseroth K., Tracey W.D. Nociceptive neurons protect Drosophila larvae from parasitoid wasps. Curr. Biol. 2007, 17:2105-2116.
23. Irizarry R.A., Bolstad B.M., Collin F., Cope L.M., Hobbs B., Speed T.P. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 2003, 31:e15.
24. Jan Y.N., Jan L.Y. Branching out: mechanisms of dendritic arborization. Nat. Rev. Neurosci. 2010, 11:316-328.
25. Jinushi-Nakao S., Arvind R., Amikura R., Kinameri E., Liu A.W., Moore A.W. Knot/Collier and cut control different aspects of dendrite cytoskeleton and synergize to define final arbor shape. Neuron 2007, 56:963-978.
26. Karim M.R., Moore A.W. Convergent local identity and topographic projection of sensory neurons. J.Neurosci. 2011, 31:17017-17027.
27. Kim M.D., Jan L.Y., Jan Y.N. The bHLH-PAS protein Spineless isnecessary for the diversification of dendrite morphology of Drosophila dendritic arborization neurons. Genes Dev. 2006, 20:2806-2819.
28. Kim M.E., Shrestha B.R., Blazeski R., Mason C.A., Grueber W.B. Integrins establish dendrite-substrate relationships that promote dendritic self-avoidance and patterning in Drosophila sensory neurons. Neuron 2012, 73:79-91.
29. Labouesse M. Epithelial junctions and attachments. WormBook 2006, January 13, 1-21. PMID: 18050482.
30. Li W., Kang L., Piggott B.J., Feng Z., Xu X.Z. The neural circuits and sensory channels mediating harsh touch sensation in Caenorhabditis elegans. Nat. Commun. 2011, 2:315.
31. Liu O.W., Shen K. The transmembrane LRR protein DMA-1 promotes dendrite branching and growth in C. elegans. Nat. Neurosci. 2012, 15:57-63.
32. McKinsey G.L., Lindtner S., Trzcinski B., Visel A., Pennacchio L.A., Huylebroeck D., Higashi Y., Rubenstein J.L. Dlx1&2-dependent expression of Zfhx1b (Sip1, Zeb2) regulates the fate switch between cortical and striatal interneurons. Neuron 2013, 77:83-98.
33. Moore A.W., Jan L.Y., Jan Y.N. hamlet, a binary genetic switch between single- and multiple- dendrite neuron morphology. Science 2002, 297:1355-1358.
34. Oren-Suissa M., Hall D.H., Treinin M., Shemer G., Podbilewicz B. The fusogen EFF-1 controls sculpting of mechanosensory dendrites. Science 2010, 328:1285-1288.
35. Parrish J.Z., Kim M.D., Jan L.Y., Jan Y.N. Genome-wide analyses identify transcription factors required for proper morphogenesis of Drosophila sensory neuron dendrites. Genes Dev. 2006, 20:820-835.
36. Petersen S.C., Watson J.D., Richmond J.E., Sarov M., Walthall W.W., Miller D.M. A transcriptional program promotes remodeling of GABAergic synapses in Caenorhabditis elegans. J.Neurosci. 2011, 31:15362-15375.
37. Powell-Coffman J.A., Bradfield C.A., Wood W.B. Caenorhabditis elegans orthologs of the aryl hydrocarbon receptor and its heterodimerization partner the aryl hydrocarbon receptor nuclear translocator. Proc. Natl. Acad. Sci. USA 1998, 95:2844-2849.
38. Qin H., Powell-Coffman J.A. The Caenorhabditis elegans aryl hydrocarbon receptor, AHR-1, regulates neuronal development. Dev. Biol. 2004, 270:64-75.
39. Siegel D.A., Huang M.K., Becker S.F. Ectopic dendrite initiation: CNS pathogenesis as a model of CNS development. Int. J. Dev. Neurosci. 2002, 20:373-389.
40. Simske J.S., Hardin J. Claudin family proteins in Caenorhabditis elegans. Methods Mol. Biol. 2011, 762:147-169.
41. Smith C.J., Watson J.D., Spencer W.C., O'Brien T., Cha B., Albeg A., Treinin M., Miller D.M. Time-lapse imaging and cell-specific expression profiling reveal dynamic branching and molecular determinants of a multi-dendritic nociceptor in C. elegans. Dev. Biol. 2010, 345:18-33.
42. Smith C.J., Watson J.D., VanHoven M.K., Colón-Ramos D.A., Miller D.M. Netrin (UNC-6) mediates dendritic self-avoidance. Nat. Neurosci. 2012, 15:731-737.
43. Smyth G.K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 2004, 3:1544-6115.
44. Spencer W.C., Zeller G., Watson J.D., Henz S.R., Watkins K.L., McWhirter R.D., Petersen S., Sreedharan V.T., Widmer C., Jo J., et al. A spatial and temporal map of C. elegans gene expression. Genome Res. 2011, 21:325-341.
45. Steed E., Balda M.S., Matter K. Dynamics and functions of tight junctions. Trends Cell Biol. 2010, 20:142-149.
46. Struhl G. Spineless-aristapedia: a homeotic gene that does not control the development of specific compartments in Drosophila. Genetics 1982, 102:737-749.
47. Sulkowski M.J., Iyer S.C., Kurosawa M.S., Iyer E.P., Cox D.N. Turtle functions downstream of Cut in differentially regulating class specific dendrite morphogenesis in Drosophila. PLoS ONE 2011, 6:e22611.
48. Sulston J.E., Horvitz H.R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 1977, 56:110-156.
49. Sulston J.E., Schierenberg E., White J.G., Thomson J.N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 1983, 100:64-119.
50. Suzuki H., Kerr R., Bianchi L., Frøkjaer-Jensen C., Slone D., Xue J., Gerstbrein B., Driscoll M., Schafer W.R. Invivo imaging of C. elegans mechanosensory neurons demonstrates a specific role for the MEC-4 channel in the process of gentle touch sensation. Neuron 2003, 39:1005-1017.
51. Topalidou I., Chalfie M. Shared gene expression in distinct neurons expressing common selector genes. Proc. Natl. Acad. Sci. USA 2011, 108:19258-19263.
52. Topalidou I., van Oudenaarden A., Chalfie M. Caenorhabditis elegans aristaless/Arx gene alr-1 restricts variable gene expression. Proc. Natl. Acad. Sci. USA 2011, 108:4063-4068.
53. Treinin M., Gillo B., Liebman L., Chalfie M. Two functionally dependent acetylcholine subunits are encoded in a single Caenorhabditis elegans operon. Proc. Natl. Acad. Sci. USA 1998, 95:15492-15495.
54. Tsalik E.L., Niacaris T., Wenick A.S., 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.
55. Tsukita S., Furuse M. The structure and function of claudins, cell adhesion molecules at tight junctions. Ann. N Y Acad. Sci. 2000, 915:129-135.
56. Tsunozaki M., Bautista D.M. Mammalian somatosensory mechanotransduction. Curr. Opin. Neurobiol. 2009, 19:362-369.
57. Von Stetina S.E., Fox R.M., Watkins K.L., Starich T.A., Shaw J.E., Miller D.M. UNC-4 represses CEH-12/HB9 to specify synaptic inputs to VA motor neurons in C. elegans. Genes Dev. 2007, 21:332-346.
58. Wacker I., Schwarz V., Hedgecock E.M., Hutter H. zag-1, a Zn-finger homeodomain transcription factor controlling neuronal differentiation and axon outgrowth in C. elegans. Development 2003, 130:3795-3805.
59. Watson J.D., Wang S., Von Stetina S.E., Spencer W.C., Levy S., Dexheimer P.J., Kurn N., Heath J.D., Miller D.M. Complementary RNA amplification methods enhance microarray identificationof transcripts expressed in the C. elegans nervous system. BMC Genomics 2008, 9:84.
60. Way J.C., Chalfie M. mec-3, a homeobox-containing gene thatspecifies differentiation of the touch receptor neurons in C. elegans. Cell 1988, 54:5-16.
61. 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 Dev. 1989, 3(12A):1823-1833.
62. Wernet M.F., Mazzoni E.O., Celik A., Duncan D.M., Duncan I., Desplan C. Stochastic spineless expression creates the retinal mosaic for colour vision. Nature 2006, 440:174-180.
63. White J.G., Southgate E., Thomson J.N., 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.
64. Wilson C.L., Safe S. Mechanisms of ligand-induced aryl hydrocarbon receptor-mediated biochemical and toxic responses. Toxicol. Pathol. 1998, 26:657-671.
65. Wood W.B. Introduction to C.elegans Biology. The Nematode Caenorhabditis elegans 1988, 1-16. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. W.B. Wood (Ed.).
66. Wu J., Duggan A., Chalfie M. Inhibition of touch cell fate by egl-44 and egl-46 in C. elegans. Genes Dev. 2001, 15:789-802.
67. Xue D., Finney M., Ruvkun G., Chalfie M. Regulation of the mec-3 gene by the C.elegans homeoproteins UNC-86 and MEC-3. EMBO J. 1992, 11:4969-4979.
68. Zhang Y., Ma C., Delohery T., Nasipak B., Foat B.C., Bounoutas A., Bussemaker H.J., Kim S.K., Chalfie M. Identification of genes expressed in C. elegans touch receptor neurons. Nature 2002, 418:331-335.