Hts, the Drosophila homologue of adducin, physically interacts with the transmembrane receptor golden goal to guide photoreceptor axons

Developmental Dynamics

Volumn 240, Issue 1, 2011, Pages 135-148

  Ohler, Stephan ^a   Hakeda Suzuki, Satoko ^a   Suzuki, Takashi ^a  

^a MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

Drosophila visual system; Growth cone cytoskeleton; Photoreceptor axon guidance

Indexed keywords

ACTIN; ADDUCIN; INSECT PROTEIN; PROTEIN GOGO; PROTEIN HTS; SPECTRIN; UNCLASSIFIED DRUG;

ARTICLE; DROSOPHILA; FILOPODIUM; GENE OVEREXPRESSION; GROWTH CONE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; CALMODULIN-BINDING PROTEINS; CELL MOVEMENT; CELLS, CULTURED; DROSOPHILA; DROSOPHILA PROTEINS; EYE PROTEINS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; PHOTORECEPTOR CELLS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PSEUDOPODIA; RECEPTORS, CELL SURFACE; SEQUENCE HOMOLOGY;

EID: 78650321863     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22515     Document Type: Article

References (59)

1. Bard L, Boscher C, Lambert M, Mege RM, Choquet D, Thoumine O. 2008. A molecular clutch between the actin flow and N-cadherin adhesions drives growth cone migration. J Neurosci 28: 5879-5890.
2. Bennett V, Stenbuck PJ. 1979. Identification and partial purification of ankyrin, the high affinity membrane attachment site for human erythrocyte spectrin. J Biol Chem 254: 2533-2541.
3. Bennett V, Gardner K, Steiner JP. 1988. Brain adducin: a protein kinase C substrate that may mediate site-directed assembly at the spectrin-actin junction. J Biol Chem 263: 5860-5869.
4. Berger J, Senti KA, Senti G, Newsome TP, Asling B, Dickson BJ, Suzuki T. 2008. Systematic identification of genes that regulate neuronal wiring in the Drosophila visual system. PLoS Genet 4: e1000085.
5. Cavener DR. 1987. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res 15: 1353-1361.
6. Chan CE, Odde DJ. 2008. Traction dynamics of filopodia on compliant substrates. Science 322: 1687-1691.
7. Conde C, Caceres A. 2009. Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10: 319-332.
8. de Cuevas M, Lee JK, Spradling AC. 1996. alpha-spectrin is required for germline cell division and differentiation in the Drosophila ovary. Development 122: 3959-3968.
9. Dent EW, Gertler FB. 2003. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40: 209-227.
10. Ding D, Parkhurst SM, Lipshitz HD. 1993. Different genetic requirements for anterior RNA localization revealed by the distribution of Adducin-like transcripts during Drosophila oogenesis. Proc Natl Acad Sci USA 90: 2512-2516.
11. Edwards RA, Bryan J. 1995. Fascins, a family of actin bundling proteins. Cell Motil Cytoskeleton 32: 1-9.
12. Ellis MC, O'Neill EM, Rubin GM. 1993. Expression of Drosophila glass protein and evidence for negative regulation of its activity in non-neuronal cells by another DNA-binding protein. Development 119: 855-865.
13. Eugene OE, Yund MA, Fristrom JW. 1979. Preparative isolation and short-term organ culture of imaginal discs of Drosophila melanogaster. Tissue Culture Assoc Manual 5: 1053-1062.
14. Gardner K, Bennett V. 1987. Modulation of spectrin-actin assembly by erythrocyte adducin. Nature 328: 359-362.
15. Geraldo S, Gordon-Weeks PR. 2009. Cytoskeletal dynamics in growth-cone steering. J Cell Sci 122: 3595-3604.
16. Goodman SR, Zagon IS. 1984. Brain spectrin: a review. Brain Res Bull 13: 813-832.
17. Goodman SR, Zagon IS. 1986. The neural cell spectrin skeleton: a review. Am J Physiol 250: C347-360.
18. Gordon-Weeks PR. 2004. Microtubules and growth cone function. J Neurobiol 58: 70-83.
19. Hughes CA, Bennett V. 1995. Adducin: a physical model with implications for function in assembly of spectrin-actin complexes. J Biol Chem 270: 18990-18996.
20. Hulsmeier J, Pielage J, Rickert C, Technau GM, Klambt C, Stork T. 2007. Distinct functions of alpha-Spectrin and beta-Spectrin during axonal pathfinding. Development 134: 713-722.
21. Joshi R, Bennett V. 1990. Mapping the domain structure of human erythrocyte adducin. J Biol Chem 265: 13130-13136.
22. Joshi R, Gilligan DM, Otto E, McLaughlin T, Bennett V. 1991. Primary structure and domain organization of human alpha and beta adducin. J Cell Biol 115: 665-675.
23. Kalil K, Dent EW. 2005. Touch and go: guidance cues signal to the growth cone cytoskeleton. Curr Opin Neurobiol 15: 521-526.
24. Koundakjian EJ, Cowan DM, Hardy RW, Becker AH. 2004. The Zuker collection: a resource for the analysis of autosomal gene function in Drosophila melanogaster. Genetics 167: 203-206.
25. Kuhlman PA, Hughes CA, Bennett V, Fowler VM. 1996. A new function for adducin. Calcium/calmodulin-regulated capping of the barbed ends of actin filaments. J Biol Chem 271: 7986-7991.
26. Li X, Matsuoka Y, Bennett V. 1998. Adducin preferentially recruits spectrin to the fast growing ends of actin filaments in a complex requiring the MARCKS-related domain and a newly defined oligomerization domain. J Biol Chem 273: 19329-19338.
27. Lin H, Yue L, Spradling AC. 1994. The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 120: 947-956.
28. Lowery LA, Van Vactor D. 2009. The trip of the tip: understanding the growth cone machinery. Nat Rev Mol Cell Biol 10: 332-343.
29. Mallavarapu A, Mitchison T. 1999. Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction. J Cell Biol 146: 1097-1106.
30. Matsuoka Y, Hughes CA, Bennett V. 1996. Adducin regulation. Definition of the calmodulin-binding domain and sites of phosphorylation by protein kinases A and C. J Biol Chem 271: 25157-25166.
31. Matsuoka Y, Li X, Bennett V. 1998. Adducin is an in vivo substrate for protein kinase C: phosphorylation in the MARCKS-related domain inhibits activity in promoting spectrin-actin complexes and occurs in many cells, including dendritic spines of neurons. J Cell Biol 142: 485-497.
32. Matsuoka Y, Li X, Bennett V. 2000. Adducin: structure, function and regulation. Cell Mol Life Sci 57: 884-895.
33. Maurel-Zaffran C, Suzuki T, Gahmon G, Treisman JE, Dickson BJ. 2001. Cell-autonomous and -nonautonomous functions of LAR in R7 photoreceptor axon targeting. Neuron 32: 225-235.
34. Mische SM, Mooseker MS, Morrow JS. 1987. Erythrocyte adducin: a calmodulin-regulated actin-bundling protein that stimulates spectrin-actin binding. J Cell Biol 105: 2837-2845.
35. Newsome TP, Asling B, Dickson BJ. 2000. Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127: 851-860.
36. Nishimura K, Yoshihara F, Tojima T, Ooashi N, Yoon W, Mikoshiba K, Bennett V, Kamiguchi H. 2003. L1-dependent neuritogenesis involves ankyrinB that mediates L1-CAM coupling with retrograde actin flow. J Cell Biol 163: 1077-1088.
37. Petrella LN, Smith-Leiker T, Cooley L. 2007. The Ovhts polyprotein is cleaved to produce fusome and ring canal proteins required for Drosophila oogenesis. Development 134: 703-712.
38. Pollard TD, Cooper JA. 1986. Actin and actin-binding proteins. A critical evaluation of mechanisms and functions. Annu Rev Biochem 55: 987-1035.
39. Robinson DN, Smith-Leiker TA, Sokol NS, Hudson AM, Cooley L. 1997. Formation of the Drosophila ovarian ring canal inner rim depends on cheerio. Genetics 145: 1063-1072.
40. Rodriguez OC, Schaefer AW, Mandato CA, Forscher P, Bement WM, Waterman-Storer CM. 2003. Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat Cell Biol 5: 599-609.
41. Samson ML, Lisbin MJ, White K. 1995. Two distinct temperature-sensitive alleles at the elav locus of Drosophila are suppressed nonsense mutations of the same tryptophan codon. Genetics 141: 1101-1111.
42. Sobue K, Kanda K. 1989. Alpha-actinins, calspectin (brain spectrin or fodrin), and actin participate in adhesion and movement of growth cones. Neuron 3: 311-319.
43. Spradling AC, Stern D, Beaton A, Rhem EJ, Laverty T, Mozden N, Misra S, Rubin GM. 1999. The Berkeley Drosophila Genome Project gene disruption project: Single P-element insertions mutating 25% of vital Drosophila genes. Genetics 153: 135-177.
44. Suter DM, Forscher P. 2000. Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. J Neurobiol 44: 97-113.
45. Tayler TD, Garrity PA. 2003. Axon targeting in the Drosophila visual system. Curr Opin Neurobiol 13: 90-95.
46. Taylor KA, Taylor DW. 1994. Formation of two-dimensional complexes of F-actin and crosslinking proteins on lipid monolayers: demonstration of unipolar alpha-actinin-F-actin crosslinking. Biophys J 67: 1976-1983.
47. Telonis-Scott M, Kopp A, Wayne ML, Nuzhdin SV, McIntyre LM. 2009. Sex-specific splicing in Drosophila: widespread occurrence, tissue specificity and evolutionary conservation. Genetics 181: 421-434.
48. Ting CY, Yonekura S, Chung P, Hsu SN, Robertson HM, Chiba A, Lee CH. 2005. Drosophila N-cadherin functions in the first stage of the two-stage layer-selection process of R7 photoreceptor afferents. Development 132: 953-963.
49. Tomasi T, Hakeda-Suzuki S, Ohler S, Schleiffer A, Suzuki T. 2008. The transmembrane protein Golden goal regulates R8 photoreceptor axon-axon and axon-target interactions. Neuron 57: 691-704.
50. Voas MG, Rebay I. 2004. Signal integration during development: insights from the Drosophila eye. Dev Dyn 229: 162-175.
51. Washburn T, O'Tousa JE. 1992. Nonsense suppression of the major rhodopsin gene of Drosophila. Genetics 130: 585-595.
52. Wen Z, Zheng JQ. 2006. Directional guidance of nerve growth cones. Curr Opin Neurobiol 16: 52-58.
53. Whittaker KL, Ding D, Fisher WW, Lipshitz HD. 1999. Different 3' untranslated regions target alternatively processed hu-li tai shao (hts) transcripts to distinct cytoplasmic locations during Drosophila oogenesis. J Cell Sci 112: 3385-3398.
54. Wilson PG. 2005. Centrosome inheritance in the male germ line of Drosophila requires hu-li tai-shao function. Cell Biol Int 29: 360-369.
55. Yue L, Spradling AC. 1992. hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis, encodes a homolog of adducin. Genes Dev 6: 2443-2454.
56. Zaccai M, Lipshitz HD. 1996a. Differential distributions of two adducin-like protein isoforms in the Drosophila ovary and early embryo. Zygote 4: 159-166.
57. Zaccai M, Lipshitz HD. 1996b. Role of Adducin-like (hu-li tai shao) mRNA and protein localization in regulating cytoskeletal structure and function during Drosophila Oogenesis and early embryogenesis. Dev Genet 19: 249-257.
58. Zhou FQ, Cohan CS. 2004. How actin filaments and microtubules steer growth cones to their targets. J Neurobiol 58: 84-91.
59. Zhou FQ, Snider WD. 2006. Intracellular control of developmental and regenerative axon growth. Phil Trans R Soc Lond B Biol Sci 361: 1575-1592.