L1CAM/Neuroglian controls the axon-axon interactions establishing layered and lobular mushroom body architecture

Journal of Cell Biology

Volumn 208, Issue 7, 2015, Pages 1003-1018

  Siegenthaler, Dominique ^a,b   Enneking, Eva Maria ^a,b   Moreno, Eliza ^a   Pielage, Jan ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; ANKYRIN 2; CELL PROTEIN; FASCICLIN II; IMMUNOGLOBULIN; MEMBRANE ASSOCIATED GUANYLATE CYCLASE KINASE; MOESIN; NERVE CELL ADHESION MOLECULE; NERVE CELL ADHESION MOLECULE L1; TYROSINE; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; DROSOPHILA PROTEIN; NRG PROTEIN, DROSOPHILA;

ADULT; AMINO ACID SUBSTITUTION; ARTICLE; BETA NERVE FIBER; BINDING AFFINITY; CELL ADHESION; CELL AGGREGATION; CELL INTERACTION; CELL MUTANT; CELL STRUCTURE; CONTROLLED STUDY; DEFENSE MECHANISM; DROSOPHILA; DROSOPHILA MELANOGASTER; EMBRYO; FEMALE; GAMMA NERVE FIBER; GENE INTERACTION; HEMISPHERE; IN VITRO STUDY; IN VIVO STUDY; INNERVATION; LARVAL DEVELOPMENT; LARVAL STAGE; LEARNING; MALE; MORPHOGENESIS; MUSHROOM BODY; NERVE FIBER; NONHUMAN; OLFACTORY MEMORY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; TRANSIENT TRANSFECTION; ANIMAL; AXON; CELL LINE; CEREBRAL PEDUNCLE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MEMORY; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

BASIDIOMYCOTA; DROSOPHILA MELANOGASTER;

ANIMALS; ANKYRINS; AXONS; CELL ADHESION; CELL ADHESION MOLECULES, NEURONAL; CELL AGGREGATION; CELL LINE; CEREBRAL PEDUNCLE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MEMORY; MICROFILAMENT PROTEINS; MUSHROOM BODIES; NEURAL CELL ADHESION MOLECULE L1; PROTEIN STRUCTURE, TERTIARY;

EID: 84928242229     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201407131     Document Type: Article

References (71)

1. Adams, M.D., S.E. Celniker, R.A. Holt, C.A. Evans, J.D. Gocayne, P.G. Amanatides, S.E. Scherer, P.W. Li, R.A. Hoskins, R.F. Galle, et al. 2000. The genome sequence of Drosophila melanogaster. Science. 287:2185-2195. http://dx.doi.org/10.1126/science.287.5461.2185
2. Aso, Y., K. Grübel, S. Busch, A.B. Friedrich, I. Siwanowicz, and H. Tanimoto. 2009. The mushroom body of adult Drosophila characterized by GAL4 drivers. J. Neurogenet. 23:156-172. http://dx.doi.org/10.1080/01677060802471718
3. Bates, K.E., C.S. Sung, and S. Robinow. 2010. The unfulfilled gene is required for the development of mushroom body neuropil in Drosophila. Neural Dev. 5:4. http://dx.doi.org/10.1186/1749-8104-5-4
4. Bieber, A.J., P.M. Snow, M. Hortsch, N.H. Patel, J.R. Jacobs, Z.R. Traquina, J. Schilling, and C.S. Goodman. 1989. Drosophila neuroglian: a member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1. Cell. 59:447-460. http://dx.doi .org/10.1016/0092-8674(89)90029-9
5. Bischof, J., R.K. Maeda, M. Hediger, F. Karch, and K. Basler. 2007. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA. 104:3312-3317. http://dx.doi.org/10.1073/pnas.0611511104
6. Blum, A.L., W. Li, M. Cressy, and J. Dubnau. 2009. Short- and long-term memory in Drosophila require cAMP signaling in distinct neuron types. Curr. Biol. 19:1341-1350. http://dx.doi.org/10.1016/j.cub.2009.07.016
7. Boyle, M., A. Nighorn, and J.B. Thomas. 2006. Drosophila Eph receptor guides specific axon branches of mushroom body neurons. Development. 133:1845-1854. http://dx.doi.org/10.1242/dev.02353
8. Carhan, A., F. Allen, J.D. Armstrong, M. Hortsch, S.F. Goodwin, and K.M. O'Dell. 2005. Female receptivity phenotype of icebox mutants caused by a mutation in the L1-type cell adhesion molecule neuroglian. Genes Brain Behav. 4:449-465. (published erratum appears in Genes Brain Behav. 5:432) http://dx.doi.org/10.1111/j.1601-183X.2004.00117.x
9. Castellani, V., E. De Angelis, S. Kenwrick, and G. Rougon. 2002. Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3A. EMBO J. 21:6348-6357. http://dx.doi.org/10.1093/emboj/cdf645
10. Chen, Y., D. Magnani, T. Theil, T. Pratt, and D.J. Price. 2012. Evidence that descending cortical axons are essential for thalamocortical axons to cross the pallial-subpallial boundary in the embryonic forebrain. PLoS ONE. 7:e33105. http://dx.doi.org/10.1371/journal.pone.0033105
11. Cheng, L., K. Itoh, and V. Lemmon. 2005. L1-mediated branching is regulated by two ezrin-radixin-moesin (ERM)-binding sites, the RSLE region and a novel juxtamembrane ERM-binding region. J. Neurosci. 25:395-403. http://dx.doi.org/10.1523/JNEUROSCI.4097-04.2005
12. Crittenden, J.R., E.M. Skoulakis, K.A. Han, D. Kalderon, and R.L. Davis. 1998. Tripartite mushroom body architecture revealed by antigenic markers. Learn. Mem. 5:38-51.
13. Davis, J.Q., and V. Bennett. 1994. Ankyrin binding activity shared by the neurofascin/L1/NrCAM family of nervous system cell adhesion molecules. J. Biol. Chem. 269:27163-27166.
14. de Belle, J.S., and M. Heisenberg. 1994. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science. 263:692-695. http://dx.doi.org/10.1126/science.8303280
15. Dickson, T.C., C.D. Mintz, D.L. Benson, and S.R. Salton. 2002. Functional binding interaction identified between the axonal CAM L1 and members of the ERM family. J. Cell Biol. 157:1105-1112. http://dx.doi.org/10.1083/jcb.200111076
16. Dubreuil, R.R., G. MacVicar, S. Dissanayake, C. Liu, D. Homer, and M. Hortsch. 1996. Neuroglian-mediated cell adhesion induces assembly of the membrane skeleton at cell contact sites. J. Cell Biol. 133:647-655. http://dx.doi .org/10.1083/jcb.133.3.647
17. Enneking, E.M., S.R. Kudumala, E. Moreno, R. Stephan, J. Boerner, T.A. Godenschwege, and J. Pielage. 2013. Transsynaptic coordination of synaptic growth, function, and stability by the L1-type CAM Neuroglian. PLoS Biol. 11:e1001537. http://dx.doi.org/10.1371/journal.pbio.1001537
18. Fransen, E., V. Lemmon, G. Van Camp, L. Vits, P. Coucke, and P.J. Willems. 1995. CRASH syndrome: clinical spectrum of corpus callosum hypoplasia, retardation, adducted thumbs, spastic paraparesis and hydrocephalus due to mutations in one single gene, L1. Eur. J. Hum. Genet. 3:273-284.
19. Fransen, E., G. Van Camp, R. D'Hooge, L. Vits, and P.J. Willems. 1998. Genotype-phenotype correlation in L1 associated diseases. J. Med. Genet. 35:399-404. http://dx.doi.org/10.1136/jmg.35.5.399
20. Fushima, K., and H. Tsujimura. 2007. Precise control of fasciclin II expression is required for adult mushroom body development in Drosophila. Dev. Growth Differ. 49:215-227. http://dx.doi.org/10.1111/j.1440-169X.2007.00922.x
21. Gallarda, B.W., D. Bonanomi, D. Müller, A. Brown, W.A. Alaynick, S.E. Andrews, G. Lemke, S.L. Pfaff, and T. Marquardt. 2008. Segregation of axial motor and sensory pathways via heterotypic trans-axonal signaling. Science. 320: 233-236. http://dx.doi.org/10.1126/science.1153758
22. García-Alonso, L., S. Romani, and F. Jiménez. 2000. The EGF and FGF receptors mediate neuroglian function to control growth cone decisions during sensory axon guidance in Drosophila. Neuron. 28:741-752. http://dx.doi .org/10.1016/S0896-6273(00)00150-1
23. Gardiol, A., and D. St Johnston. 2014. Staufen targets coracle mRNA to Drosophila neuromuscular junctions and regulates GluRIIA synaptic accumulation and bouton number. Dev. Biol. 392:153-167. http://dx.doi.org/10.1016/j.ydbio.2014.06.007
24. Garver, T.D., Q. Ren, S. Tuvia, and V. Bennett. 1997. Tyrosine phosphorylation at a site highly conserved in the L1 family of cell adhesion molecules abolishes ankyrin binding and increases lateral mobility of neurofascin. J. Cell Biol. 137:703-714. http://dx.doi.org/10.1083/jcb.137.3.703
25. Genova, J.L., and R.G. Fehon. 2003. Neuroglian, Gliotactin, and the Na+/K+ ATPase are essential for septate junction function in Drosophila. J. Cell Biol. 161:979-989. http://dx.doi.org/10.1083/jcb.200212054
26. Gil, O.D., T. Sakurai, A.E. Bradley, M.Y. Fink, M.R. Cassella, J.A. Kuo, and D.P. Felsenfeld. 2003. Ankyrin binding mediates L1CAM interactions with static components of the cytoskeleton and inhibits retrograde movement of L1CAM on the cell surface. J. Cell Biol. 162:719-730. http://dx.doi .org/10.1083/jcb.200211011
27. Goossens, T., Y.Y. Kang, G. Wuytens, P. Zimmermann, Z. Callaerts-Végh, G. Pollarolo, R. Islam, M. Hortsch, and P. Callaerts. 2011. The Drosophila L1CAM homolog Neuroglian signals through distinct pathways to control different aspects of mushroom body axon development. Development. 138:1595-1605. http://dx.doi.org/10.1242/dev.052787
28. Gordon, M.D., and K. Scott. 2009. Motor control in a Drosophila taste circuit. Neuron. 61:373-384. http://dx.doi.org/10.1016/j.neuron.2008.12.033
29. Grillenzoni, N., A. Flandre, C. Lasbleiz, and J.M. Dura. 2007. Respective roles of the DRL receptor and its ligand WNT5 in Drosophila mushroom body development. Development. 134:3089-3097. http://dx.doi.org/10.1242/dev.02876
30. Hall, S.G., and A.J. Bieber. 1997. Mutations in the Drosophila neuroglian cell adhesion molecule affect motor neuron pathfinding and peripheral nervous system patterning. J. Neurobiol. 32:325-340. http://dx.doi.org/10.1002/(SICI)1097-4695(199703)32:3325::AID-NEU63.0.CO;2-9
31. Heisenberg, M. 2003. Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 4:266-275. http://dx.doi.org/10.1038/nrn1074
32. Hortsch, M. 2000. Structural and functional evolution of the L1 family: are four adhesion molecules better than one? Mol. Cell. Neurosci. 15:1-10. http://dx.doi.org/10.1006/mcne.1999.0809
33. Hortsch, M., A.J. Bieber, N.H. Patel, and C.S. Goodman. 1990. Differential splicing generates a nervous system-specific form of Drosophila neuroglian. Neuron. 4:697-709. http://dx.doi.org/10.1016/0896-6273(90)90196-M
34. Hortsch, M., Y.M. Wang, Y. Marikar, and A.J. Bieber. 1995. The cytoplasmic domain of the Drosophila cell adhesion molecule neuroglian is not essential for its homophilic adhesive properties in S2 cells. J. Biol. Chem. 270:18809-18817. http://dx.doi.org/10.1074/jbc.270.32.18809
35. Hortsch, M., D. Homer, J.D. Malhotra, S. Chang, J. Frankel, G. Jefford, and R.R. Dubreuil. 1998. Structural requirements for outside-in and insideout signaling by Drosophila neuroglian, a member of the L1 family of cell adhesion molecules. J. Cell Biol. 142:251-261. http://dx.doi.org/10.1083/jcb.142.1.251
36. Jouet, M., A. Rosenthal, G. Armstrong, J. MacFarlane, R. Stevenson, J. Paterson, A. Metzenberg, V. Ionasescu, K. Temple, and S. Kenwrick. 1994. X-linked spastic paraplegia (SPG1), MASA syndrome and X-linked hydrocephalus result from mutations in the L1 gene. Nat. Genet. 7:402-407. http://dx.doi.org/10.1038/ng0794-402
37. Kamiguchi, H., M.L. Hlavin, M. Yamasaki, and V. Lemmon. 1998. Adhesion molecules and inherited diseases of the human nervous system. Annu. Rev. Neurosci. 21:97-125. http://dx.doi.org/10.1146/annurev.neuro.21.1.97
38. Koester, S.E., and D.D. O'Leary. 1994. Axons of early generated neurons in cingulate cortex pioneer the corpus callosum. J. Neurosci. 14:6608-6620.
39. Kolodkin, A.L., and M. Tessier-Lavigne. 2011. Mechanisms and molecules of neuronal wiring: a primer. Cold Spring Harb. Perspect. Biol. 3:a001727. http://dx.doi.org/10.1101/cshperspect.a001727
40. Krashes, M.J., A.C. Keene, B. Leung, J.D. Armstrong, and S. Waddell. 2007. Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron. 53:103-115. http://dx.doi.org/10.1016/j .neuron.2006.11.021
41. Kurusu, M., T. Awasaki, L.M. Masuda-Nakagawa, H. Kawauchi, K. Ito, and K. Furukubo-Tokunaga. 2002. Embryonic and larval development of the Drosophila mushroom bodies: concentric layer subdivisions and the role of fasciclin II. Development. 129:409-419.
42. Lee, T., and L. Luo. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron. 22:451-461. http://dx.doi.org/10.1016/S0896-6273(00)80701-1
43. Lee, T., A. Lee, and L. Luo. 1999. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development. 126:4065-4076.
44. Lyuksyutova, A.I., C.C. Lu, N. Milanesio, L.A. King, N. Guo, Y. Wang, J. Nathans, M. Tessier-Lavigne, and Y. Zou. 2003. Anterior-posterior guidance of commissural axons by Wnt-frizzled signaling. Science. 302:1984-1988. http://dx.doi.org/10.1126/science.1089610
45. Maness, P.F., and M. Schachner. 2007. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat. Neurosci. 10:19-26. http://dx.doi.org/10.1038/nn1827
46. McCartney, B.M., and R.G. Fehon. 1996. Distinct cellular and subcellular patterns of expression imply distinct functions for the Drosophila homologues of moesin and the neurofibromatosis 2 tumor suppressor, merlin. J. Cell Biol. 133:843-852. http://dx.doi.org/10.1083/jcb.133.4.843
47. Ng, J., T. Nardine, M. Harms, J. Tzu, A. Goldstein, Y. Sun, G. Dietzl, B.J. Dickson, and L. Luo. 2002. Rac GTPases control axon growth, guidance and branching. Nature. 416:442-447. http://dx.doi.org/10.1038/416442a
48. Nishikimi, M., K. Oishi, and K. Nakajima. 2013. Axon guidance mechanisms for establishment of callosal connections. Neural Plast. 2013:149060.
49. Pielage, J., L. Cheng, R.D. Fetter, P.M. Carlton, J.W. Sedat, and G.W. Davis. 2008. A presynaptic giant ankyrin stabilizes the NMJ through regulation of presynaptic microtubules and transsynaptic cell adhesion. Neuron. 58: 195-209. http://dx.doi.org/10.1016/j.neuron.2008.02.017
50. Pielage, J., V. Bulat, J.B. Zuchero, R.D. Fetter, and G.W. Davis. 2011. Hts/ Adducin controls synaptic elaboration and elimination. Neuron. 69:1114-1131. http://dx.doi.org/10.1016/j.neuron.2011.02.007
51. Qin, H., M. Cressy, W. Li, J.S. Coravos, S.A. Izzi, and J. Dubnau. 2012. Gamma neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila. Curr. Biol. 22:608-614. http://dx.doi .org/10.1016/j.cub.2012.02.014
52. Ramel, D., X. Wang, C. Laflamme, D.J. Montell, and G. Emery. 2013. Rab11 regulates cell-cell communication during collective cell movements. Nat. Cell Biol. 15:317-324. http://dx.doi.org/10.1038/ncb2681
53. Sakurai, T. 2012. The role of NrCAM in neural development and disorders-beyond a simple glue in the brain. Mol. Cell. Neurosci. 49:351-363. http://dx .doi.org/10.1016/j.mcn.2011.12.002
54. Sakurai, T., O.D. Gil, J.D. Whittard, M. Gazdoiu, T. Joseph, J. Wu, A. Waksman, D.L. Benson, S.R. Salton, and D.P. Felsenfeld. 2008. Interactions between the L1 cell adhesion molecule and ezrin support traction-force generation and can be regulated by tyrosine phosphorylation. J. Neurosci. Res. 86:2602-2614. http://dx.doi.org/10.1002/jnr.21705
55. Schmidt, E.R., S. Brignani, Y. Adolfs, S. Lemstra, J. Demmers, M. Vidaki, A.L. Donahoo, K. Lilleväli, E. Vasar, L.J. Richards, et al. 2014. Subdomainmediated axon-axon signaling and chemoattraction cooperate to regulate afferent innervation of the lateral habenula. Neuron. 83:372-387. http://dx.doi.org/10.1016/j.neuron.2014.05.036
56. Schwabe, T., J.A. Borycz, I.A. Meinertzhagen, and T.R. Clandinin. 2014. Differential adhesion determines the organization of synaptic fascicles in the Drosophila visual system. Curr. Biol. 24:1304-1313. http://dx.doi.org/10.1016/j.cub.2014.04.047
57. Shin, J.E., and A. DiAntonio. 2011. Highwire regulates guidance of sister axons in the Drosophila mushroom body. J. Neurosci. 31:17689-17700. http://dx.doi.org/10.1523/JNEUROSCI.3902-11.2011
58. Strauss, R., and M. Heisenberg. 1993. A higher control center of locomotor behavior in the Drosophila brain. J. Neurosci. 13:1852-1861.
59. Suter, D.M., L.D. Errante, V. Belotserkovsky, and P. Forscher. 1998. The Ig superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substrate-cytoskeletal coupling. J. Cell Biol. 141:227-240. http://dx.doi.org/10.1083/jcb.141.1.227
60. Tanaka, N.K., H. Tanimoto, and K. Ito. 2008. Neuronal assemblies of the Drosophila mushroom body. J. Comp. Neurol. 508:711-755. http://dx.doi.org/10.1002/cne.21692
61. Tovar-Moll, F., J. Moll, R. de Oliveira-Souza, I. Bramati, P.A. Andreiuolo, and R. Lent. 2007. Neuroplasticity in human callosal dysgenesis: a diffusion tensor imaging study. Cereb. Cortex. 17:531-541. http://dx.doi .org/10.1093/cercor/bhj178
62. Trannoy, S., C. Redt-Clouet, J.M. Dura, and T. Preat. 2011. Parallel processing of appetitive short- and long-term memories in Drosophila. Curr. Biol. 21:1647-1653. http://dx.doi.org/10.1016/j.cub.2011.08.032
63. Tuvia, S., T.D. Garver, and V. Bennett. 1997. The phosphorylation state of the FIGQY tyrosine of neurofascin determines ankyrin-binding activity and patterns of cell segregation. Proc. Natl. Acad. Sci. USA. 94:12957-12962. http://dx.doi.org/10.1073/pnas.94.24.12957
64. Venken, K.J., J.W. Carlson, K.L. Schulze, H. Pan, Y. He, R. Spokony, K.H. Wan, M. Koriabine, P.J. de Jong, K.P. White, et al. 2009. Versatile P[acman] BAC libraries for transgenesis studies in Drosophila melanogaster. Nat. Methods. 6:431-434. http://dx.doi.org/10.1038/nmeth.1331
65. Vits, L., G. Van Camp, P. Coucke, E. Fransen, K. De Boulle, E. Reyniers, B. Korn, A. Poustka, G. Wilson, C. Schrander-Stumpel, et al. 1994. MASA syndrome is due to mutations in the neural cell adhesion gene L1CAM. Nat. Genet. 7:408-413. http://dx.doi.org/10.1038/ng0794-408
66. Wang, J., C.T. Zugates, I.H. Liang, C.H. Lee, and T. Lee. 2002. Drosophila Dscam is required for divergent segregation of sister branches and suppresses ectopic bifurcation of axons. Neuron. 33:559-571. http://dx.doi .org/10.1016/S0896-6273(02)00570-6
67. Wong, E.V., S. Kenwrick, P. Willems, and V. Lemmon. 1995. Mutations in the cell adhesion molecule L1 cause mental retardation. Trends Neurosci. 18:168-172. http://dx.doi.org/10.1016/0166-2236(95)93896-6
68. Wu, C.L., M.F. Shih, P.T. Lee, and A.S. Chiang. 2013. An octopamine-mushroom body circuit modulates the formation of anesthesia-resistant memory in Drosophila. Curr. Biol. 23:2346-2354. http://dx.doi.org/10.1016/j.cub .2013.09.056
69. Yamasaki, M., P. Thompson, and V. Lemmon. 1997. CRASH syndrome: mutations in L1CAM correlate with severity of the disease. Neuropediatrics. 28:175-178. http://dx.doi.org/10.1055/s-2007-973696
70. Yoshikawa, S., R.D. McKinnon, M. Kokel, and J.B. Thomas. 2003. Wnt-mediated axon guidance via the Drosophila Derailed receptor. Nature. 422:583-588. http://dx.doi.org/10.1038/nature01522
71. Zhan, X.L., J.C. Clemens, G. Neves, D. Hattori, J.J. Flanagan, T. Hummel, M.L. Vasconcelos, A. Chess, and S.L. Zipursky. 2004. Analysis of Dscam diversity in regulating axon guidance in Drosophila mushroom bodies. Neuron. 43:673-686. http://dx.doi.org/10.1016/j.neuron.2004.07.020