An ankyrin-related gene (unc-44) is necessary for proper axonal guidance in Caenorhabditis elegans

Journal of Cell Biology

Volumn 129, Issue 4, 1995, Pages 1081-1092

  Otsuka, Anthony J ^a,b   Franco, Rodrigo ^b,d   Yang, Bin ^a   Shim, Kyu Hwan ^a   Tang, Lan Zhao ^a   Zhang, Yu Yong ^a   Boontrakulpoontawee, Pratumtip ^a   Jeyaprakash, Ayyamperumal ^b,e   Hedgecock, Edward ^c   Wheaton, Virginia I ^b   Sobery, Alan ^a  

^a ILLINOIS STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d PFIZER INC   (United States)

^e UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN;

ALLELE; ALTERNATIVE RNA SPLICING; ARTICLE; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; GENE MUTATION; NERVE GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; REVERTANT; TRANSPOSON;

CAENORHABDITIS ELEGANS;

EID: 0029074731     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.129.4.1081     Document Type: Article

References (58)

1. Aviv, H., and P. Leder. 1972. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc. Natl. Acad. Sci. USA. 69:1408-1412.
2. Barstead, R. J., and R. H. Waterston. 1989. The basal component of the nematode dense-body is vinculin. J. Biol. Chem. 264:10177-10185.
3. Bennett, V. 1990. Spectrin-based membrane skeleton: a multipotential adaptor between plasma membrane and cytoplasm. Physiol Rev. 70:1029-1065.
4. Bennett, V. 1992. Ankyrins: adaptors between diverse plasma membrane proteins and the cytoplasm. J. Biol. Chem. 267:8703-8706.
5. Brenner, S. 1974. The genetics of Caenorhabditis elegans. Genetics. 77:71-94.
6. B: structure of the major developmentally regulated domain and selective localization in unmyelinated axons. J. Cell Biol. 123:1463-1473.
7. Collins, J., B. Saari, and P. Anderson. 1987. Activation of a transposable element in the germ line but not the soma of Caenorhabditis elegans. Nature (Lond.). 328:726-728.
8. Coulson, A., J. Sulston, S. Brenner, and J. Karn. 1986. Toward a physical map of the genome of the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 83:7821-7825.
9. Davis, J., L. Davis, and V. Bennett. 1989. Diversity in membrane binding sites of ankyrins: brain ankyrin, erythrocyte ankyrin, and processed erythrocyte ankyrin associate with distinct sites in kidney microsomes. J. Biol. Chem. 264:6417-6426.
10. Davis, J. Q., T. McLaughlin, and V. Bennett. 1993. Ankyrin-binding proteins related to nervous system cell adhesion molecules: candidates to provide transmembrane and intracellular connections in adult brain. J. Cell Biol. 121:121-133.
11. Davis, L. H., and V. Bennett. 1990. Mapping the binding sites of human erythrocyte ankyrin for the anion exchanger and spectrin. J. Biol. Chem. 265: 10589-10596.
12. Davis, L. H., J. Q. Davis, and V. Bennett. 1992. Ankyrin regulation: an alternatively spliced segment of the regulatory domain functions as an intramolecular modulator. J. Biol. Chem. 267:18966-18972.
13. Dodd, J., and T. M. Jessell. 1988. Axon guidance and the patterning of neuronal projections in vertebrates. Science (Wash. DC). 242:692-699.
14. Drenckhahn, D., and V. Bennett. 1987. Polarized distribution of Mr 210,000 and 190,000 analogs of erythrocyte ankyrin along the plasma membrane of transporting epithelia, neurons and photoreceptors. Eur. J. Cell Biol. 43: 479-486.
15. Emmons, S. W., and L. Yesner. 1984. High-frequency excision of transposable element Tc1 in the nematode Caenorhabditis elegans is limited to somatic cells. Cell. 36:599-605.
16. Georgatos, S. D., K. Weber, N. Geisler, and G. Blobel. 1987. Binding of two desmin derivatives to the plasma membrane and the nuclear envelope of avian erythrocytes: evidence for a conserved site-specificity in intermediate filament-membrane interactions. Proc. Natl. Acad. Sci. USA. 84:6780-6784.
17. Gumbiner, B. M. 1993. Proteins associated with the cytoplasmic surface of adhesion molecules. Neuron. 11:551-564.
18. Hall, T. G., and V. Bennett. 1987. Regulatory domains of erythrocyte ankyrin. J. Biol. Chem. 262:10537-10545.
19. Hedgecock, E. M., J. G. Culotti, and D. H. Hall. 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.
20. Hedgecock, E. M., J. G. Culotti, D. H. Hall, and B. D. Stern. 1987. Genetics of cell and axon migrations in Caenorhabditis elegans. Development. 100:365-382.
21. Hedgecock, E. M., J. G. Culotti, J. N. Thomson, and L. A. Perkins. 1985. Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Dev. Biol. 111:158-170.
22. Henikoff, S. 1984. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene (Amst.). 28:351-359.
23. Jessell, T. M. 1988. Adhesion molecules and the hierarchy of neural development. Neuron. 1:3-13.
24. Kunimoto, M., E. Otto, and V. Bennett. 1991. A new 440-kD isoform is the major ankyrin in the neonatal rat brain. J. Cell Biol. 115:1319-1331.
25. Lambert, S., and V. Bennett. 1993. From anemia to cerebellar dysfunction - a review of the ankyrin gene family. Eur. J. Biochem. 211:1-6.
26. Lambert, S., H. Yu, J. T. Prchal, J. Lawler, P. Ruff, D. Speicher, M. C. Cheung, Y. W. Kan, and J. Palek. 1990. cDNA sequence for human erythrocyte ankyrin. Proc. Natl. Acad. Sci. USA. 87:1730-1734.
27. Lazarides, E., and C. Woods. 1989. Biogenesis of the red blood cell membrane skeleton and the control of erythroid morphogenesis. Annu. Rev. Cell Biol. 5:427-452.
28. Lehrach, H., D. Diamond, J. M. Wozney, and H. Boedtker. 1977. RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry. 16:4743-4751.
29. Leung-Hagesteijn, C., A. M. Spence, B. D. Stern, Y. Zhou, M.-W. Su, E. M. Hedgecock, and J. G. Culotti. 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.
30. Lux, S. E., K. M. John, and V. Bennett. 1990. Analysis of cDNA for human erythrocyte ankyrin indicates a repeated structure with homology to tissue-differentiation and cell-cycle control proteins. Nature (Lond.). 344:36-42.
31. MacLeod, A. R., J. Karn, and S. Brenner. 1981. Molecular analysis of the unc-54 myosin heavy-chain gene of Caenorhabditis elegans. Nature (Lond.). 291:386-390.
32. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
33. McIntire, S. L., G. Garriga, J. White, D. Jacobson, and H. R. Horvitz. 1992. Genes necessary for directed axonal elongation or fasciculation in C elegans. Neuron. 8:307-322.
34. Michaely, P., and V. Bennett. 1992. The ANK repeat: a ubiquitous motif involved in macromolecular recognition. Trends Cell Biol. 2:127-129.
35. Mori, I., D. G. Moerman, and R. H. Waterston. 1988. Analysis of a mutator activity necessary for germline transposition and excision of Tc1 transposable elements in Caenorhabditis elegans. Genetics. 120:397-407.
36. Mount, S. M., M. M. Green, and G. M. Rubin. 1988. Partial revertants of the transposable element-associated suppressible allele white-apricot in Drosophila melanogaster: structures and responsiveness to genetic modifiers. Genetics. 118:221-224.
37. Otsuka, A. J., V. I. Wheaton, and E. Hedgecock. 1987. Transposon tagging of genes affecting axonal outgrowth in Caenorhabditis elegans. UCLA Symp. Mol. Cell. Biol 51:66S-671.
38. Otto, E., M. Kunimoto, T. McLaughlin, and V. Bennett. 1991. Isolation and characterization of cDNAs encoding human brain ankyrins reveal a family of alternatively spliced genes. J. Cell Biol. 114:241-253.
39. Peters, L. L., and S. E. Lux. 1993. Ankyrins: structure and function in normal cells and hereditary spherocytes. Semin. Hematol. 30:85-118.
40. Platt, O. S., S. E. Lux, and J. F. Falcone. 1993. A highly conserved region of human erythrocyte ankyrin contains the capacity to bind spectrin. J. Biol. Chem. 268:24421-24426.
41. Rathjen, F. G., U. Norenberg, and H. Volkmer. 1992. Glycoproteins implicated in neural cell adhesion and axonal growth. Biochem. Soc. Trans. 20:405-409.
42. Sanes, J. R. 1989. Extracellular matrix molecules that influence neural development. Annu. Rev. Neurosci. 12:491-516.
43. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chainterminating inhibitors. Proc. Natl. Acad. Sci. USA. 74:5463-5467.
44. Serafini, T., T. E. Kennedy, M. J. Galko, C. Mirzayan, T. M. Jessell, and M. Tessier-Lavigne. 1994. The netrins define a family of axon outgrowthpromoting proteins homologous to C. elegans UNC-6. Cell. 78:409-424.
45. Siddiqui, S. S. 1990. Mutations affecting axonal growth and guidance of motor neurons and mechanosensory neurons in the nematode Caenorhabditis elegans. Neurosci. Res. (Suppl.). 13:171-190.
46. Siddiqui, S. S., and J. G. Culotti. 1991. Examination of neurons in wild type and mutants of Caenorhabditis elegans using antibodies to horseradish peroxidase. J. Neurogenetics. 7:193-211.
47. Singer, I. I., D. W. Kawka, S. Scott, R. A. Mumford, and M. W. Lark. 1987. The fibronectin cell attachment sequence arg-gly-asp-ser promotes focal contact formation during early fibroblast attachment and spreading. J. Cell Biol. 104:573-584.
48. Steinert, P. M., and D. R. Roop. 1988. Molecular and cellular biology of intermediate filaments. Annu. Rev. Biochem. 57:593-625.
49. Sulston, J. E., and S. Brenner. 1974. The DNA of Caenorhabditis elegans. Genetics. 77:95-104.
50. Takeichi, M. 1988. The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development. 102:639-655.
51. Takeichi, M. 1991. Cadherin cell adhesion receptors as a morphogenetic regulator. Science (Wash. DC). 251:1451-1455.
52. Tse, W. T. 1990. A molecular analysis of the spectrin and ankyrin genes in normal and abnormal red blood cells. Ph. D. thesis. Yale University, New Haven, CT. pp. 1-191.
53. Wadsworth, W. G., and E. M. Hedgecock. 1992. Guidance of neuroblast migrations and axonal projections in Caenorhabditis elegans. Curr. Opin. Neurobiol 2:36-41.
54. Wallin, R., E. N. Culp, D. B. Coleman, and S. R. Goodman. 1984. A structural model of human erythrocyte band 2.1: alignment of chemical and functional domains. Proc. Natl. Acad. Sci. USA. 81:4095-4099.
55. Weaver, D. C., and V. T. Marchesi. 1984. The structural basis of ankyrin function: I. Identification of two structural domains. J. Biol. Chem. 259:6165-6169.
56. Weaver, D. C., G. R. Pasternack, and V. T. Marchesi. 1984. The structural basis of ankyrin function: II. Identification of two functional domains. J. Biol. Chem. 259:6170-6175.
57. White, J. G., E. Southgate, J. N. Thomson, and S. Brenner. 1986. The structure of the nervous system of the nematode Caenorhabditis elegans. Phil. Trans. Roy. Soc. Lond. 314:1-340.
58. White, R. A., C. S. Birkenmeier, L. L. Peters, J. E. Barker, and S. E. Lux. 1992. Murine erythrocyte ankyrin cDNA: highly conserved regions of the regulatory domain. Mamm. Genome. 3:281-285.