Integrins Regulate Repulsion-Mediated Dendritic Patterning of Drosophila Sensory Neurons by Restricting Dendrites in a 2D Space

Neuron

Volumn 73, Issue 1, 2012, Pages 64-78

  Han, Chun ^a   Wang, Denan ^a   Soba, Peter ^a   Zhu, Sijun ^a   Lin, Xinhua ^b,c   Jan, Lily Yeh ^a   Jan, Yuh Nung ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; FURRY PROTEIN; INTEGRIN; LAMININ; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; SAPK INTERACTING PROTEIN 1; TRICORNERED PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL EXPANSION; CELL INTERACTION; CELL MUTANT; CONTROLLED STUDY; DENDRITE; DROSOPHILA; EMBRYO; EXTRACELLULAR MATRIX; FEMALE; GENE; GENE INTERACTION; LAMININ GENE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SENSORY NERVE CELL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CLONING, MOLECULAR; DENDRITES; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTEGRINS; LAMININ; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; NEUROIMAGING; RNA INTERFERENCE; SENSE ORGANS; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION;

EID: 84862907988     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.10.036     Document Type: Article

References (65)

1. Barczyk M., Carracedo S., Gullberg D. Integrins. Cell Tissue Res. 2010, 339:269-280.
2. Beumer K.J., Rohrbough J., Prokop A., Broadie K. A role for PS integrins in morphological growth and synaptic function at the postembryonic neuromuscular junction of Drosophila. Development 1999, 126:5833-5846.
3. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
4. Brower D.L. Platelets with wings: the maturation of Drosophila integrin biology. Curr. Opin. Cell Biol. 2003, 15:607-613.
5. Brower D.L., Bunch T.A., Mukai L., Adamson T.E., Wehrli M., Lam S., Friedlander E., Roote C.E., Zusman S. Nonequivalent requirements for PS1 and PS2 integrin at cell attachments in Drosophila: genetic analysis of the alpha PS1 integrin subunit. Development 1995, 121:1311-1320.
6. Bunch T.A., Salatino R., Engelsgjerd M.C., Mukai L., West R.F., Brower D.L. Characterization of mutant alleles of myospheroid, the gene encoding the beta subunit of the Drosophila PS integrins. Genetics 1992, 132:519-528.
7. Cabodi S., Di Stefano P., del Pilar M., Tinnirello A., Bisaro B., Morello V., Damiano L., Aramu S., Repetto D., Tornillo G., Defilippi P. Integrins and signal transduction. Adv. Exp. Med. Biol. 2010, 674:43-54.
8. Cong J., Geng W., He B., Liu J., Charlton J., Adler P.N. The furry gene of Drosophila is important for maintaining the integrity of cellular extensions during morphogenesis. Development 2001, 128:2793-2802.
9. Dacey D.M., Peterson B.B., Robinson F.R., Gamlin P.D. Fireworks in the primate retina: invitro photodynamics reveals diverse LGN-projecting ganglion cell types. Neuron 2003, 37:15-27.
10. Denda S., Reichardt L.F. Studies on integrins in the nervous system. Methods Enzymol. 2007, 426:203-221.
11. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
12. Durbeej M. Laminins. Cell Tissue Res. 2010, 339:259-268.
13. Emoto K., He Y., Ye B., Grueber W.B., Adler P.N., Jan L.Y., Jan Y.N. Control of dendritic branching and tiling by the Tricornered-kinase/Furry signaling pathway in Drosophila sensory neurons. Cell 2004, 119:245-256.
14. Emoto K., Parrish J.Z., Jan L.Y., Jan Y.N. The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance. Nature 2006, 443:210-213.
15. Feinberg E.H., Vanhoven M.K., Bendesky A., Wang G., Fetter R.D., Shen K., Bargmann C.I. GFP Reconstitution Across Synaptic Partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 2008, 57:353-363.
16. Fuerst P.G., Koizumi A., Masland R.H., Burgess R.W. Neurite arborization and mosaic spacing in the mouse retina require DSCAM. Nature 2008, 451:470-474.
17. Fuerst P.G., Bruce F., Tian M., Wei W., Elstrott J., Feller M.B., Erskine L., Singer J.H., Burgess R.W. DSCAM and DSCAML1 function in self-avoidance in multiple cell types in the developing mouse retina. Neuron 2009, 64:484-497.
18. Fuerst P.G., Harris B.S., Johnson K.R., Burgess R.W. A novel null allele of mouse DSCAM survives to adulthood on an inbred C3H background with reduced phenotypic variability. Genesis 2010, 48:578-584.
19. Gallegos M.E., Bargmann C.I. Mechanosensory neurite termination and tiling depend on SAX-2 and the SAX-1 kinase. Neuron 2004, 44:239-249.
20. Geng W., He B., Wang M., Adler P.N. The tricornered gene, which is required for the integrity of epidermal cell extensions, encodes the Drosophila nuclear DBF2-related kinase. Genetics 2000, 156:1817-1828.
21. Grotewiel M.S., Beck C.D., Wu K.H., Zhu X.R., Davis R.L. Integrin-mediated short-term memory in Drosophila. Nature 1998, 391:455-460.
22. Grueber W.B., Sagasti A. Self-avoidance and tiling: mechanisms of dendrite and axon spacing. Cold Spring Harb. Perspect. Biol. 2010, 2:a001750.
23. Grueber W.B., Jan L.Y., Jan Y.N. Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 2002, 129:2867-2878.
24. Grueber W.B., Ye B., Moore A.W., Jan L.Y., Jan Y.N. Dendrites of distinct classes of Drosophila sensory neurons show different capacities for homotypic repulsion. Curr. Biol. 2003, 13:618-626.
25. Grueber W.B., Ye B., Yang C.H., Younger S., Borden K., Jan L.Y., Jan Y.N. Projections of Drosophila multidendritic neurons in the central nervous system: links with peripheral dendrite morphology. Development 2007, 134:55-64.
26. Halfon M.S., Gisselbrecht S., Lu J., Estrada B., Keshishian H., Michelson A.M. New fluorescent protein reporters for use with the Drosophila Gal4 expression system and for vital detection of balancer chromosomes. Genesis 2002, 34:135-138.
27. Han C., Jan L.Y., Jan Y.N. Enhancer-driven membrane markers for analysis of nonautonomous mechanisms reveal neuron-glia interactions in Drosophila. Proc. Natl. Acad. Sci. USA 2011, 108:9673-9678.
28. Henchcliffe C., García-Alonso L., Tang J., Goodman C.S. Genetic analysis of laminin A reveals diverse functions during morphogenesis in Drosophila. Development 1993, 118:325-337.
29. Hietakangas V., Cohen S.M. Re-evaluating AKT regulation: role of TOR complex 2 in tissue growth. Genes Dev. 2007, 21:632-637.
30. Huckfeldt R.M., Schubert T., Morgan J.L., Godinho L., Di Cristo G., Huang Z.J., Wong R.O. Transient neurites of retinal horizontal cells exhibit columnar tiling via homotypic interactions. Nat. Neurosci. 2009, 12:35-43.
31. Hughes M.E., Bortnick R., Tsubouchi A., Bäumer P., Kondo M., Uemura T., Schmucker D. Homophilic Dscam interactions control complex dendrite morphogenesis. Neuron 2007, 54:417-427.
32. Hummel T., Vasconcelos M.L., Clemens J.C., Fishilevich Y., Vosshall L.B., Zipursky S.L. Axonal targeting of olfactory receptor neurons in Drosophila is controlled by Dscam. Neuron 2003, 37:221-231.
33. Humphries J.D., Byron A., Humphries M.J. Integrin ligands at a glance. J. Cell Sci. 2006, 119:3901-3903.
34. Hynes R.O., Zhao Q. The evolution of cell adhesion. J. Cell Biol. 2000, 150:F89-F96.
35. Jan Y.N., Jan L.Y. Branching out: mechanisms of dendritic arborization. Nat. Rev. Neurosci. 2010, 11:316-328.
36. Kaneko M., Yamaguchi K., Eiraku M., Sato M., Takata N., Kiyohara Y., Mishina M., Hirase H., Hashikawa T., Kengaku M. Remodeling of monoplanar Purkinje cell dendrites during cerebellar circuit formation. PLoS ONE 2011, 6:e20108.
37. Kapfhammer J.P., Schwab M.E. Modulators of neuronal migration and neurite growth. Curr. Opin. Cell Biol. 1992, 4:863-868.
38. Kelso R.J., Buszczak M., Quiñones A.T., Castiblanco C., Mazzalupo S., Cooley L. Flytrap, a database documenting a GFP protein-trap insertion screen in Drosophila melanogaster. Nucleic Acids Res. 2004, 32(Database issue):D418-D420.
39. Koike-Kumagai M., Yasunaga K., Morikawa R., Kanamori T., Emoto K. The target of rapamycin complex 2 controls dendritic tiling of Drosophila sensory neurons through the Tricornered kinase signalling pathway. EMBO J. 2009, 28:3879-3892.
40. Kolb H., Linberg K.A., Fisher S.K. Neurons of the human retina: a Golgi study. J.Comp. Neurol. 1992, 318:147-187.
41. Kramer A.P., Stent G.S. Developmental arborization of sensory neurons in the leech Haementeria ghilianii. II. Experimentally induced variations in the branching pattern. J.Neurosci. 1985, 5:768-775.
42. Larsen C.W., Hirst E., Alexandre C., Vincent J.P. Segment boundary formation in Drosophila embryos. Development 2003, 130:5625-5635.
43. Lee T., Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999, 22:451-461.
44. Long H., Ou Y., Rao Y., van Meyel D.J. Dendrite branching and self-avoidance are controlled by Turtle, a conserved IgSF protein in Drosophila. Development 2009, 136:3475-3484.
45. Lunde K., Biehs B., Nauber U., Bier E. The knirps and knirps-related genes organize development of the second wing vein in Drosophila. Development 1998, 125:4145-4154.
46. Mariani A.P. Amacrine cells of the rhesus monkey retina. J.Comp. Neurol. 1990, 301:382-400.
47. Martin-Bermudo M.D., Dunin-Borkowski O.M., Brown N.H. Specificity of PS integrin function during embryogenesis resides in the alpha subunit extracellular domain. EMBO J. 1997, 16:4184-4193.
48. Martin D., Zusman S., Li X., Williams E.L., Khare N., DaRocha S., Chiquet-Ehrismann R., Baumgartner S. Wing blister, a new Drosophila laminin alpha chain required for cell adhesion and migration during embryonic and imaginal development. J. Cell Biol. 1999, 145:191-201.
49. Matthews B.J., Kim M.E., Flanagan J.J., Hattori D., Clemens J.C., Zipursky S.L., Grueber W.B. Dendrite self-avoidance is controlled by Dscam. Cell 2007, 129:593-604.
50. Morin X., Daneman R., Zavortink M., Chia W. A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proc. Natl. Acad. Sci. USA 2001, 98:15050-15055.
51. Nakamoto T., Kain K.H., Ginsberg M.H. Neurobiology: new connections between integrins and axon guidance. Curr. Biol. 2004, 14:R121-R123.
52. Parrish J.Z., Xu P., Kim C.C., Jan L.Y., Jan Y.N. The microRNA bantam functions in epithelial cells to regulate scaling growth of dendrite arbors in Drosophila sensory neurons. Neuron 2009, 63:788-802.
53. Perry V.H., Linden R. Evidence for dendritic competition in the developing retina. Nature 1982, 297:683-685.
54. Sagasti A., Guido M.R., Raible D.W., Schier A.F. Repulsive interactions shape the morphologies and functional arrangement of zebrafish peripheral sensory arbors. Curr. Biol. 2005, 15:804-814.
55. Sdrulla A.D., Linden D.J. Dynamic imaging of cerebellar Purkinje cells reveals a population of filopodia which cross-link dendrites during early postnatal development. Cerebellum 2006, 5:105-115.
56. Soba P., Zhu S., Emoto K., Younger S., Yang S.J., Yu H.H., Lee T., Jan L.Y., Jan Y.N. Drosophila sensory neurons require Dscam for dendritic self-avoidance and proper dendritic field organization. Neuron 2007, 54:403-416.
57. Song W., Onishi M., Jan L.Y., Jan Y.N. Peripheral multidendritic sensory neurons are necessary for rhythmic locomotion behavior in Drosophila larvae. Proc. Natl. Acad. Sci. USA 2007, 104:5199-5204.
58. Stevens A., Jacobs J.R. Integrins regulate responsiveness to slit repellent signals. J.Neurosci. 2002, 22:4448-4455.
59. Sugimura K., Yamamoto M., Niwa R., Satoh D., Goto S., Taniguchi M., Hayashi S., Uemura T. Distinct developmental modes and lesion-induced reactions of dendrites of two classes of Drosophila sensory neurons. J.Neurosci. 2003, 23:3752-3760.
60. Wang J., Zugates C.T., Liang I.H., Lee C.H., Lee T. Drosophila Dscam is required for divergent segregation of sister branches and suppresses ectopic bifurcation of axons. Neuron 2002, 33:559-571.
61. Wang J., Ma X., Yang J.S., Zheng X., Zugates C.T., Lee C.H., Lee T. Transmembrane/juxtamembrane domain-dependent Dscam distribution and function during mushroom body neuronal morphogenesis. Neuron 2004, 43:663-672.
62. Yamagata M., Sanes J.R. Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 2008, 451:465-469.
63. Yamagata M., Sanes J.R. Synaptic localization and function ofSidekick recognition molecules require MAGI scaffolding proteins. J.Neurosci. 2010, 30:3579-3588.
64. Yamagata M., Weiner J.A., Sanes J.R. Sidekicks: synaptic adhesion molecules that promote lamina-specific connectivity in the retina. Cell 2002, 110:649-660.
65. Zhu H., Hummel T., Clemens J.C., Berdnik D., Zipursky S.L., Luo L. Dendritic patterning by Dscam and synaptic partner matching in the Drosophila antennal lobe. Nat. Neurosci. 2006, 9:349-355.