C. elegans bicd-1, homolog of the Drosophila dynein accessory factor Bicaudal D, regulates the branching of PVD sensory neuron dendrites

Development

Volumn 138, Issue 3, 2011, Pages 507-518

  Aguirre Chen, Cristina ^a   Bülow, Hannes E ^a   Kaprielian, Zaven ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Bicaudal D; Caenorhabditis elegans; Dendrite morphogenesis; PVD

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; MOLECULAR MOTOR;

ARTICLE; BICD 1 GENE; CAENORHABDITIS ELEGANS; CELL ORGANELLE; CONTROLLED STUDY; DENDRITE; GENE; GENE FUNCTION; GENE IDENTIFICATION; GENETIC SCREENING; MOLECULAR INTERACTION; NERVE CELL NETWORK; NERVE FIBER GROWTH; NOCICEPTIVE RECEPTOR; NONHUMAN; PRIORITY JOURNAL; PVD NERVE CELL; SENSORY NERVE CELL; SENSORY STIMULATION;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE PROTEINS; CYTOPLASMIC DYNEINS; DENDRITES; DROSOPHILA PROTEINS; KINESIN; PROTEIN BINDING; RNA INTERFERENCE; SENSORY RECEPTOR CELLS;

CAENORHABDITIS ELEGANS; VERTEBRATA;

EID: 78751564789     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.060939     Document Type: Article

References (65)

1. Ashrafi, K., Chang, F. Y., Watts, J. L., Fraser, A. G., Kamath, R. S., Ahringer, J. and Ruvkun, G. (2003). Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421, 268-272.
2. Baens, M. and Marynen, P. (1997). A human homologue (BICD1) of the Drosophila bicaudal-D gene. Genomics 45, 601-606.
3. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
4. Bullock, S. L. and Ish-Horowicz, D. (2001). Conserved signals and machinery for RNA transport in Drosophila oogenesis and embryogenesis. Nature 414, 611-616.
5. Bullock, S. L., Nicol, A., Gross, S. P. and Zicha, D. (2006). Guidance of bidirectional motor complexes by mRNA cargoes through control of dynein number and activity. Curr. Biol. 16, 1447-1452.
6. Bülow, H. E., Berry, K. L., Topper, L. H., Peles, E. and Hobert, O. (2002). Heparan sulfate proteoglycan-dependent induction of axon branching and axon misrouting by the Kallmann syndrome gene kal-1. Proc. Natl. Acad. Sci. USA 99, 6346-6351.
7. Chatzigeorgiou, M., Yoo, S., Watson, J. D., Lee, W. H., Spencer, W. C., Kindt, K. S., Hwang, S. W., Miller, D. M., III, Treinin, M., Driscoll, M. et al. (2010). Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors. Nat. Neurosci. 13, 861-868.
8. Corty, M. M., Matthews, B. J. and Grueber, W. B. (2009). Molecules and mechanisms of dendrite development in Drosophila. Development 136, 1049-1061.
9. Dalvin, S., Anselmo, M. A., Prodhan, P., Komatsuzaki, K., Schnitzer, J. J. and Kinane, T. B. (2003). Expression of Netrin-1 and its two receptors DCC and UNC5H2 in the developing mouse lung. Gene. Expr. Patterns 3, 279-283.
10. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E. and Mello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811.
11. Fraser, A. G., Kamath, R. S., Zipperlen, P., Martinez-Campos, M., Sohrmann, M. and Ahringer, J. (2000). Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408, 325-330.
12. Fridolfsson, H. N. and Starr, D. A. (2010). Kinesin-1 and dynein at the nuclear envelope mediate the bidirectional migrations of nuclei. J. Cell Biol. 191, 115-128.
13. Fridolfsson, H. N., Ly, N., Meyerzon, M. and Starr, D. A. (2010). UNC-83 coordinates kinesin-1 and dynein activities at the nuclear envelope during nuclear migration. Dev. Biol. 338, 237-250.
14. Fumoto, K., Hoogenraad, C. C. and Kikuchi, A. (2006). GSK-3beta-regulated interaction of BICD with dynein is involved in microtubule anchorage at centrosome. EMBO. J. 25, 5670-5682.
15. Grueber, W. B., Yang, C. H., Ye, B. and Jan, Y. N. (2005). The development of neuronal morphology in insects. Curr. Biol. 15, R730-R738.
16. Hamelin, M., Zhou, Y., Su, M. W., Scott, I. M. and Culotti, J. G. (1993). Expression of the UNC-5 guidance receptor in the touch neurons of C. elegans steers their axons dorsally. Nature 364, 327-330.
17. Hamilton, B., Dong, Y., Shindo, M., Liu, W., Odell, I., Ruvkun, G. and Lee, S. S. (2005). A systematic RNAi screen for longevity genes in C. elegans. Genes Dev. 19, 1544-1555.
18. Hausser, M., Spruston, N. and Stuart, G. J. (2000). Diversity and dynamics of dendritic signaling. Science 290, 739-744.
19. Hedgecock, E. M., Culotti, J. G. and Hall, D. H. (1990). 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 4, 61-85.
20. Hobert, O. (2002). PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32, 728-730.
21. Hoogenraad, C. C., Akhmanova, A., Howell, S. A., Dortland, B. R., De Zeeuw, C. I., Willemsen, R., Visser, P., Grosveld, F. and Galjart, N. (2001). Mammalian Golgi-associated Bicaudal-D2 functions in the dynein-dynactin pathway by interacting with these complexes. EMBO J. 20, 4041-4054.
22. Hoogenraad, C. C., Wulf, P., Schiefermeier, N., Stepanova, T., Galjart, N., Small, J. V., Grosveld, F., de Zeeuw, C. I. and Akhmanova, A. (2003). Bicaudal D induces selective dynein-mediated microtubule minus end-directed transport. EMBO J. 22, 6004-6015.
23. Horton, A. C. and Ehlers, M. D. (2003). Dual modes of endoplasmic reticulumto-Golgi transport in dendrites revealed by live-cell imaging. J. Neurosci. 23, 6188-6199.
24. Horton, A. C., Rácz, B., Monson, E. E., Lin, A. L., Weinberg, R. J. and Ehlers, M. D. (2005). Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48, 757-771.
25. Jan, Y. N. and Jan, L. Y. (2010). Branching out: mechanisms of dendritic arborization. Nat. Rev. Neurosci. 11, 316-328.
26. Kakimoto, T., Katoh, H. and Negishi, M. (2006). Regulation of neuronal morphology by Toca-1, an F-BAR/EFC protein that induces plasma membrane invagination. J. Biol. Chem. 281, 29042-29053.
27. Kamath, R. S. and Ahringer, J. (2003). Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313-321.
28. Kamath, R. S., Fraser, A. G., Dong, Y., Poulin, G., Durbin, R., Gotta, M., Kanapin, A., Le Bot, N., Moreno, S., Sohrmann, M. et al. (2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231-237.
29. Killeen, M., Tong, J., Krizus, A., Steven, R., Scott, I., Pawson, T. and Culotti, J. (2002). UNC-5 function requires phosphorylation of cytoplasmic tyrosine 482, but its UNC-40-independent functions also require a region between the ZU-5 and death domains. Dev. Biol. 251, 348-366.
30. Kim, K. and Li, C. (2004). Expression and regulation of an FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. J. Comp. Neurol. 475, 540-550.
31. Kim, M. J., Liu, I. H., Song, Y., Lee, J. A., Halfter, W., Balice-Gordon, R. J., Linney, E. and Cole, G. J. (2007). Agrin is required for posterior development and motor axon outgrowth and branching in embryonic zebrafish. Glycobiology 17, 231-247.
32. Koushika, S. P., Schaefer, A. M., Vincent, R., Willis, J. H., Bowerman, B. and Nonet, M. L. (2004). Mutations in Caenorhabditis elegans cytoplasmic dynein components reveal specificity of neuronal retrograde cargo. J. Neurosci. 24, 3907-3916.
33. Larsen, K. S., Xu, J., Cermelli, S., Shu, Z. and Gross, S. P. (2008). BicaudalD actively regulates microtubule motor activity in lipid droplet transport. PLoS ONE 3, e3763.
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. Li, X., Kuromi, H., Briggs, L., Green, D. B., Rocha, J. J., Sweeney, S. T. and Bullock, S. L. (2010). Bicaudal-D binds clathrin heavy chain to promote its transport and augments synaptic vesicle recycling. EMBO J. 29, 992-1006.
36. Liu, Y., Stein, E., Oliver, T., Li, Y., Brunken, W. J., Koch, M., Tessier-Lavigne, M. and Hogan, B. L. M. (2004). Novel role for netrins in regulating epithelial behavior during lung branching morphogenesis. Curr. Biol. 14, 897-905.
37. Lu, X., le Noble, F., Yuan, L., Jiang, Q., de Lafarge, B., Sugiyama, D., Breant, C., Claes, F., De Smet, F., Thomas, J. L. et al. (2004). The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 432, 179-186.
38. Mallik, R., Petrov, D., Lex, S. A., King, S. J. and Gross, S. P. (2005). Building complexity: an in vitro study of cytoplasmic dynein with in vivo implications. Curr. Biol. 15, 2075-2085.
39. Marshak, S., Nikolakopoulou, A. M., Dirks, R., Martens, G. J. and Cohen-Cory, S. (2007). Cell-autonomous TrkB signaling in presynaptic retinal ganglion cells mediates axon arbor growth and synapse maturation during the establishment of retinotectal synaptic connectivity. J. Neurosci. 27, 2444-2456.
40. Matanis, T., Akhmanova, A., Wulf, P., Del Nery, E., Weide, T., Stepanova, T., Galjart, N., Grosveld, F., Goud, B., De Zeeuw, C. I. et al. (2002). Bicaudal-D regulates COPI-independent Golgi-ER transport by recruiting the dyneindynactin motor complex. Nat. Cell Biol. 4, 986-992.
41. Miyashita, T., Yeo, S. Y., Hirate, Y., Segawa, H., Wada, H., Little, M. H., Yamada, T., Takahashi, N. and Okamoto, H. (2004). PlexinA4 is necessary as a downstream target of Islet2 to mediate Slit signaling for promotion of sensory axon branching. Development 131, 3705-3715.
42. Mohler, J. and Wieschaus, E. F. (1986). Dominant maternal-effect mutations of Drosophila melanogaster causing the production of double-abdomen embryos. Genetics 112, 803-822.
43. Navankasattusas, S., Whitehead, K. J., Suli, A., Sorensen, L. K., Lim, A. H., Zhao, J., Park, K. W., Wythe, J. D., Thomas, K. R., Chien, C. B. et al. (2008). The netrin receptor UNC5B promotes angiogenesis in specific vascular beds. Development 135, 659-667.
44. Ogura, K. and Goshima, Y. (2006). The autophagy-related kinase UNC-51 and its binding partner UNC-14 regulate the subcellular localization of the Netrin receptor UNC-5 in Caenorhabditis elegans. Development 133, 3441-3450.
45. Oren-Suissa, M., Hall, D. H., Treinin, M., Shemer, G. and Podbilewicz, B. (2010). The fusogen EFF-1 controls sculpting of mechanosensory dendrites. Science 328, 1285-1288.
46. Patel, N., Thierry-Mieg, D. and Mancillas, J. R. (1993). Cloning by insertional mutagenesis of a cDNA encoding Caenorhabditis elegans kinesin heavy chain. Proc. Natl. Acad. Sci. USA 90, 9181-9185.
47. Sakamoto, R., Byrd, D. T., Brown, H. M., Hisamoto, N., Matsumoto, K. and Jin, Y. (2005). The Caenorhabditis elegans UNC-14 RUN domain protein binds to the Kinesin-1 and UNC-16 complex and regulates synaptic vesicle localization. Mol. Biol. Cell 16, 483-496.
48. Satoh, D., Sato, D., Tsuyama, T., Saito, M., Ohkura, H., Rolls, M. M., Ishikawa, F. and Uemura, T. (2008). Spatial control of branching within dendritic arbors by dynein-dependent transport of Rab5-endosomes. Nat. Cell Biol. 10, 1164-1171.
49. Schmitz, C., Kinge, P. and Hutter, H. (2007). Axon guidance genes identified in a large-scale RNAi screen using the RNAi-hypersensitive Caenorhabditis elegans strain nre-1(hd20) lin-15b(hd126). Proc. Natl. Acad. Sci. USA 104, 834-839.
50. Smith, C. J., Watson, J. D., Spencer, W. C., O'Brien, T., Cha, B., Albeg, A., Treinin, M. and Miller, D. M, III (2010). Time-lapse imaging and cell-specific expression profiling reveal dynamic branching and molecular determinants of a multi-dendritic nociceptor in C. elegans. Dev. Biol. 345, 18-33.
51. Struckhoff, E. C. and Lundquist, E. A. (2003). The actin-binding protein UNC-115 is an effector of Rac signaling during axon pathfinding in C. elegans. Development 130, 693-704.
52. Su, M., Merz, D. C., Killeen, M. T., Zhou, Y., Zheng, H., Kramer, J. M., Hedgecock, E. M. and Culotti, J. G. (2000). Regulation of the UNC-5 netrin receptor initiates the first reorientation of migrating distal tip cells in Caenorhabditis elegans. Development 127, 585-594.
53. Suter, B., Romberg, L. M. and Steward, R. (1989). Bicaudal-D, a Drosophila gene involved in developmental asymmetry: localized transcript accumulation in ovaries and sequence similarity to myosin heavy chain tail domains. Genes Dev. 3, 1957-1968.
54. Swan, A., Nguyen, T. and Suter, B. (1999). Drosophila Lissencephaly-1 functions with Bic-D and dynein in oocyte determination and nuclear positioning. Nat. Cell Biol. 1, 444-449.
55. Tsalik, E. L., Niacaris, T., Wenick, A. S., Pau, K., Avery, L. and Hobert, O. (2003). LIM homeobox gene-dependent expression of biogenic amine receptors in restricted regions of the C. elegans nervous system. Dev. Biol. 263, 81-102.
56. Urbanska, M., Blazejczyk, M. and Jaworski, J. (2008). Molecular Basis of Dendrite Arborization. Acta Neurobiol. Exp. (Wars.) 68, 264-288.
57. Wanschers, B. F. J., van de Vorstenbosch, R., Schlager, M. A., Splinter, D., Akhmanova, A., Hoogenraad, C. C., Wieringa, B. and Fransen, J. A. M. (2007). A role for the Rab6B Bicaudal-D1 interaction in retrograde transport in neuronal cells. Exp. Cell Res. 313, 3408-3420.
58. Way, J. C. and Chalfie, M. (1988). mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans. Cell 54, 5-16.
59. Way, J. C. and Chalfie, M. (1989). The mec-3 gene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. Genes Dev. 3, 1823-1833.
60. Welte, M. A. (2004). Bidirectional transport along microtubules. Curr. Biol. 14, R525-R537.
61. Wharton, R. P. and Struhl, G. (1989). Structure of the Drosophila BicaudalD protein and its role in localizing the posterior determinant nanos. Cell 59, 881-892.
62. Wolters, N. M. and MacKeigan, J. P. (2008). From sequence to function: using RNAi to elucidate mechanisms of human disease. Cell Death Differ. 15, 809-819.
63. Yassin, L., Gillo, B., Kahan, T., Halevi, S., Eshel, M., Treinin, M. (2001). Characterization of the DEG-3/DES-2 receptor: a nicotinic acetylcholine receptor that mutates to cause neuronal degeneration. Mol. Cell. Neurosci. 17, 589-599.
64. Ye, B., Zhang, Y., Song, W., Younger, S. H., Jan, L. Y. and Jan, Y. N. (2007). Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130, 717-729.
65. Zheng, Y., Wildonger, J., Ye, B., Zhang, Y., Kita, A., Younger, S. H., Zimmerman, S., Jan, L. Y. and Jan, Y. N. (2008). Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat. Cell Biol. 10, 1172-1180.