Novel Caenorhabditis elegans unc-119 axon outgrowth defects correlate with behavioral phenotypes that are partially rescued by nonneural UNC-119

Genesis (United States)

Volumn 42, Issue 2, 2005, Pages 104-116

  Materi, Wayne ^a   Pilgrim, David ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Axon; Branching; C. Elegans; Cell autonomy; Dauer larvae; Defasciculation; Ectopic expression; Elongation; Neurite; Neuron; unc 119

Indexed keywords

COMPLEMENTARY DNA; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MESSENGER RNA;

ARTICLE; BEHAVIOR; CAENORHABDITIS ELEGANS; GENE; GENOTYPE; LARVA; NERVE FIBER GROWTH; NERVOUS SYSTEM; NEURITE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; TRANSGENIC ANIMAL; UNC 119 GENE;

CAENORHABDITIS ELEGANS;

EID: 22244457628     PISSN: 1526954X     EISSN: None     Source Type: Journal    
DOI: 10.1002/gene.20130     Document Type: Article

References (50)

1. Altun-Gultekin Z, Andachi Y, Tsalik EL, Pilgrim D, Kohara Y, 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.
2. Bargmann CI, Horvitz HR. 1991. Control of larval development by chemosensory neurons in Caenorhabditis elegans. Science 251: 1243-1246.
3. Barnes WM. 1994. PCR amplification of up to 35-kb DNA with high fidelity and high yield from 1 bacteriophage templates. Proc Natl Acad Sci U S A 91:2216-2220.
4. Bennett V. 1992. Ankyrins. Adaptors between diverse plasma membrane proteins and the cytoplasm. J Biol Chem 267:8703-8706.
5. Bhamidipati A, Lewis SA, Cowan NJ. 2000. ADP ribosylation factor-like protein 2 (Arl2) regulates the interaction of tubulin-folding cofactor D with native tubulin. J Cell Biol 149:1087-1096.
6. Billuart P, Winter CG, Maresh A, Zhao X, Luo L. 2001. Regulating axon branch stability: the role of p190 RhoGAP in repressing a retraction signaling pathway. Cell 107:195-207.
7. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94.
8. Cassada RC, Russell RL. 1975. The dauer larvae, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Dev Biol 46:326-342.
9. Cen O, Gorska MM, Stafford SJ, Sur S, Alam R. 2003. Identification of UNC119 as a novel activator of Src-type tyrosine kinases. J Biol Chem 278:8837-8845.
10. Chalfie M, Sulston J. 1981. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev Biol 82:358-370.
11. Chalfie M, Sulston JE, White JG, Southgate E, Thomson JN, Brenner S. 1985. The neural circuit for touch sensitivity in C. elegans. J Neurosci 5:956-964.
12. Chan SS-Y, Zheng H, Su M-W, Wilk R, Killeen MT, Hedgecock EM, Culotti JG. 1996. UNC-40, a C. elegans homolog of DCC (deleted in colorectal cancer), is required in motile cells responding to UNC-6 netrin cues. Cell 87:187-195.
13. Christensen M, Estevez A, Yin X, Fox R, Morrison R, McDonnell M, Gleason C, Miller DM 3rd, Strange K. 2002. A primary culture system for functional analysis of C. elegans neurons and muscle cells. Neuron 33:503-514.
14. Coburn CM, Mori I, Ohshima Y, Bargmann CI. 1998. A cyclic nucleotide-gated channel inhibits sensory axon outgrowth in larval and adult Caenorhabditis elegans: a distinct pathway for maintenance of sensory axon structure. Development 125:249-258.
15. Colavita A, Krishna S, Zheng H, Padgett RW, Culotti JG. 1998. Pioneer axon guidance by UNC-129, a C. elegans TGF-beta. Science 281:706-709.
16. Fares H, Greenwald I. 2001. Regulation of endocytosis by CUP-5, the Caenorhabditis elegans mucolipin-1 homolog. Nat Genet 28:64-68.
17. Gorska MM, Stafford SJ, Cen O, Sur S, Alam R. 2004. Unc119, a novel activator of lck/fyn, is essential for T cell activation. Exp Med 199:369-379.
18. Hall DH, Hedgecock EM. 1991. Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans. Cell 65:837-847.
19. Harris TW, Schuske K, Jorgensen EM. 2001. Studies of synaptic vesicle endocytosis in the nematode C. elegans. Traffic 2:597-605.
20. Hedgecock EM, Culotti JG, Hall DH. 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 2:61-85.
21. Higashide T, Murakami A, McLaren MJ, Inana G. 1996. Cloning of the cDNA for a novel photoreceptor protein. J Biol Chem. 271:1797-1804.
22. Higashide T, McLaren MJ, Inana G. 1998. Localization of HRG4, a photoreceptor protein homologous to unc-119, in ribbon synapse. Invest Ophthalmol Vis Sci 39:690-698.
23. Kaprielian Z, Runko E, Imondi R. 2001. Axon guidance at the midline choice point. Dev Dyn 221:154-181.
24. King VM, Armstrong DM, Apps R, Trott JR. 1998. Numerical aspects of pontine, lateral reticular, and inferior olivary projections to two paravermal cortical zones of the cat cerebellum. J Comp Neurol 390:537-551.
25. Knobel KM, Davis WS, Jorgensen EM, Bastiani MJ. 2001. UNC-119 suppresses axon branching in C. elegans. Development 128:4079-4092.
26. Krueger NX, Van Vactor D, Wan HI, Gelbart WM, Goodman CS, Saito H. 1996. The transmembrane tyrosine phosphatase DLAR controls motor axon guidance in Drosophila. Cell 84:611-622.
27. Lai CC, Hong K, Kinnell M, Chalfie M, Driscoll M. 1996. Sequence and transmembrane topology of MEC-4, an ion channel subunit required for mechanotransduction in Caenorhabditis elegans. J Cell Biol 133:1071-1081.
28. Lin DM, Fetter RD, Kopczynski C, Grenningloh G, Goodman CS. 1994. Genetic analysis of Fasciclin II in Drosophila: defasciculation, refasciculation, and altered fasciculation. Neuron 13:1055-1069.
29. Maduro M, Pilgrim D. 1995. Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 141:977-988.
30. Maduro MF, Gordon M, Jacobs R, Pilgrim DB. 2000. The UNC-119 family of neural proteins is functionally conserved between humans, Drosophila and C. elegans. J Neurogenet 13:191-212.
31. Manning AG, Crawford BD, Waskiewicz AJ, Pilgrim DB. 2004. unc-119 homolog required for normal development of the zebrafish nervous system. genesis 40:223-230.
32. ts1. J Neurogenet 6:191-206.
33. Mello CC, Kramer JM, Stinchcomb D, Ambros V. 1991. Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10:3959-3970.
34. Ogura K, Wicky C, Magnenat L, Tobler H, Mori I, Muller F, Ohshima Y. 1994. Caenorhabditis elegans unc-51 gene required for axonal elongation encodes a novel serine/threonine kinase. Genes Dev 84:2389-2400.
35. Okazaki N, Yan J, Yuasa S, Ueno T, Kominami E, Masuho Y, Koga H, Muramatsu M. 2000. Interaction of the UNC-51-like kinase and microtubule-associated protein light chain 3 related proteins in the brain: possible role of vesicular transport in axonal elongation. Mol Brain Res 85:1-12.
36. Okkema PG, Harrison SW, Plunger V, Aryana A, Fire A. 1993. Sequence requirements for myosin gene-expression and regulation in Caenorhabditis elegans. Genetics 135:385-404.
37. Otsuka AJ, Jeyaprakash A, Garcia-Anoveros J, Tang LZ, Fisk G, Hartshorne T, Franco R, Born T. 1991. The C. elegans unc-104 gene encodes a putative kinesin heavy chain-like protein. Neuron 6:113-122.
38. Otsuka AJ, Franco R, Yang B, Shim K-H, Lan ZT, Yu YZ, Boontrakulpoontawee P, Jeyaprakash A, Hedgecock E, Wheaton VI, Sobery A. 1995. An ankyrin-related gene (unc-44) is necessary for proper axonal guidance in Caenorhabditis elegans. J Cell Biol 129:1081-1092.
39. Ren P, Lim CS, Johnsen R, Albert PS, Pilgrim D, Riddle DL. 1996. Control of C. elegans larval development by neuronal expression of a TGF-beta homolog. Science 274:1389-1391.
40. Sabo SL, McAllister AK. 2003. Mobility and cycling of synaptic protein-containing vesicles in axonal growth cone filopodia. Nat Neurosci 6:1264-1269.
41. Schaefer AM, Hadwiger GD, Nonet ML. 2000. rpm-1, a conserved neuronal gene that regulates targeting and synaptogenesis in C. elegans. Neuron 26:345-356.
42. Siddiqui SS. 1990. Mutations affecting axonal growth and guidance of motor neurons and mechanosensory neurons in the nematode Caenorhabditis elegans. Neurosci Res S13:171-190.
43. Siddiqui SS, Culotti JG. 1991. Examination of neurons in wildtype and mutants of Caenorhabditis elegans using antibodies to horseradish peroxidase. J Neurogenet 7:193-211.
44. Swanson DA, Chang JT, Campochiaro PA, Zack DJ, Valle D. 1998. Mammalian orthologs of C. elegans unc-119 highly expressed in photoreceptors. Invest Ophthalmol Vis Sci 39:2085-2094.
45. Tanudji M, Hevi S, Chuck SL. 2002. Improperly folded green fluorescent protein is secreted via a non-classical pathway. J Cell Sci 115:3849-3857.
46. Thomas J. 1993. Chemosensory regulation of development in C. elegans. BioEssays 15:791-797.
47. Torre E, McNiven MA, Urrutia R. 1994. Dynamin 1 antisense oligonucleotide treatment prevents neurite formation in cultured hippocampal neurons. J. Biol Chem 269:32411-32417.
48. White JG, Southgate E, Thomson JN, Brenner S. 1986. The structure of the nervous system of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314:1-340.
49. Wood WB. 1988. The nematode Caenorhabditis elegans. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
50. Zhao H, Nonet ML. 2000. A retrograde signal is involved in activity-dependent remodeling at a C. elegans neuromuscular junction. Development 127:1253-1266.