L1 interaction with ankyrin regulates mediolateral topography in the retinocollicular projection

Journal of Neuroscience

Volumn 28, Issue 1, 2008, Pages 177-188

  Buhusi, Mona ^a,b   Schlatter, Monika C ^a   Demyanenko, Galina P ^a   Thresher, Randy ^a   Maness, Patricia F ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Ankyrin; Axon guidance; Cell adhesion; EphrinB; L1; Retinocollicular

Indexed keywords

ANKYRIN; EPHRIN RECEPTOR B1; EPHRIN RECEPTOR B2; EPHRIN RECEPTOR B4; EPHRIN RECEPTOR B5; EPHRIN RECEPTOR B6;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ADHESION; CONTROLLED STUDY; CYTOPLASM; FEMALE; GENE EXPRESSION; MALE; MOUSE; NERVE CELL; NERVE FIBER GROWTH; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; RETINA GANGLION CELL; SUPERIOR COLLICULUS;

AMINO ACIDS; ANIMALS; ANIMALS, NEWBORN; ANKYRINS; AXONS; BRAIN MAPPING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTIDINE; IMMUNOPRECIPITATION; MICE; MICE, TRANSGENIC; MUTATION; NEURAL CELL ADHESION MOLECULE L1; RETINA; SUPERIOR COLLICULI; TYROSINE; VISUAL PATHWAYS;

EID: 38149141710     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3573-07.2008     Document Type: Article

References (62)

1. Ango F, di Cristo G, Higashiyama H, Bennett V, Wu P, Huang ZJ (2004) Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at Purkinje axon initial segment. Cell 119:257-272.
2. Birgbauer E, Cowan CA, Sretavan DW, Henkemeyer M (2000) Kinase independent function of EphB receptors in retinal axon pathfinding to the optic disc from dorsal but not ventral retina. Development 127:1231-1241.
3. Brakebusch C, Fassler R (2005) beta 1 integrin function in vivo: adhesion, migration and more. Cancer Metastasis Rev 24:403-411.
4. Burgoon MP, Grumet M, Mauro V, Edelman GM, Cunningham BA (1991) Structure of the chicken neuron-glia cell adhesion molecule, Ng-CAM: origin of the polypeptides and relation to the Ig superfamily. J Cell Biol 112:1017-1029.
5. Chan W, Kordeli E, Bennett V (1993) 440-kD ankyrinB: structure of the major developmentally regulated domain and selective localization in unmyelinated axons. J Cell Biol 123:1463-1473.
6. Cheng L, Itoh K, Lemmon V (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.
7. Davis JQ, Bennett V (1994) Ankyrin binding activity shared by the neurofascin/L1/NrCAM family of cell adhesion molecules. J Biol Chem 269:27163-27166.
8. Demyanenko G, Tsai A, Maness PF (1999) Abnormalities in neuronal process extension, hippocampal development, and the ventricular system of L1 knockout mice. J Neurosci 19:4907-4920.
9. Demyanenko GP, Maness PF (2003) The L1 cell adhesion molecule is essential for topographic mapping of retinal axons. J Neurosci 23:530-538.
10. Dickson TC, Mintz CD, Benson DL, Salton SR (2002) Functional binding interaction identified between the axonal CAM L1 and members of the ERM family. J Cell Biol 157:1105-1112.
11. Drescher U, Kremoser C, Handwerker C, Löschinger J, Noda M, Bonhoeffer F (1995) In vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 82:359-370.
12. Feldheim DA, Kim YI, Bergemann AD, Frisen J, Barbacid M, Flanagan JG (2000) Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping [see comments]. Neuron 25:563-574.
13. Feldheim DA, Nakamoto M, Osterfield M, Gale NW, DeChiara TM, Rohatgi R, Yancopoulos GD, Flanagan JG (2004) Loss-of-function analysis of EphA receptors in retinotectal mapping. J Neurosci 24:2542-2550.
14. Felding-Habermann B, Silletti S, Mei F, Siu CH, Yip PM, Brooks PC, Cheresh DA, O'Toole TE, Ginsberg MH, Montgomery AM (1997) A single immunoglobulin-like domain of the human neural cell adhesion molecule L1 supports adhesion by multiple vascular and platelet integrins. J Cell Biol 139:1567-1581.
15. Flanagan JG (2006) Neural map specification by gradients. Curr Opin Neurobiol 16:59-66.
16. Garver TD, Ren Q, Tuvia S, Bennett V (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.
17. Gil OD, Sakurai T, Bradley AE, Fink MY, Cassella MR, Kuo JA, Felsenfeld DP (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.
18. Godenschwege TA, Kristiansen LV, Uthaman SB, Hortsch M, Murphey RK (2006) A conserved role for Drosophila Neuroglian and human L1-CAM in central-synapse formation. Curr Biol 16:12-23.
19. Gu C, Park S (2001) The EphA8 receptor regulates integrin activity through p110gamma phosphatidylinositol-3 kinase in a tyrosine kinase activity-independent manner. Mol Cell Biol 21:4579-4597.
20. Hansen MJ, Dallal GE, Flanagan JG (2004) Retinal axon response to ephrin-as shows a graded, concentration-dependent transition from growth promotion to inhibition. Neuron 42:717-730.
21. Hindges R, McLaughlin T, Genoud N, Henkemeyer M, O'Leary DD (2002) EphB forward signaling controls directional branch extension and arborization required for dorsal-ventral retinotopic mapping. Neuron 35:475-487.
22. Holash JA, Pasquale EB (1995) Polarized expression of the receptor protein tyrosine kinase Cek5 in the developing avian visual system. Dev. Biol 172:683-693.
23. Hortsch M, Homer D, Malhotra JD, Chang S, Frankel J, Jefford G, Dubreuil RR (1998) Structural requirements for outside-in and inside-out signaling by Drosophila neuroglian, a member of the L1 family of cell adhesion molecules. J Cell Biol 142:251-261.
24. Huynh-Do U, Vindis C, Liu H, Cerretti DP, McGrew JT, Enriquez M, Chen J, Daniel TO (2002) Ephrin-B1 transduces signals to activate integrin-mediated migration, attachment and angiogenesis. J Cell Sci 115:3073-3081.
25. Jenkins SM, Kizhatil K, Kramarcy NR, Sen A, Sealock R, Bennett V (2001) FIGQY phosphorylation defines discrete populations of L1 cell adhesion molecules at sites of cell-cell contact and in migrating neurons. J Cell Sci 114:3823-3835.
26. Kalil K, Dent EW (2005) Touch and go: guidance cues signal to the growth cone cytoskeleton. Curr Opin Neurobiol 15:521-526.
27. Kamiguchi H, Long KE, Pendergast M, Schaefer AW, Rapoport I, Kirchhausen T, Lemmon V (1998) The neural cell adhesion molecule L1 interacts with the AP-2 adaptor and is endocytosed via the clathrin-mediated pathway. J Neurosci 18:5311-5321.
28. Kenwrick S, Watkins A, Angelis ED (2000) Neural cell recognition molecule L1: relating biological complexity to human disease mutations. Hum Mol Genet 9:879-886.
29. Kizhatil K, Wu YX, Sen A, Bennett V (2002) A new activity of doublecortin in recognition of the phospho-FIGQY tyrosine in the cytoplasmic domain of neurofascin. J Neurosci 22:7948-7958.
30. Kunimoto M, Otto E, Bennett V (1991) A new 440-kd isoform is the major ankyrin in neonatal brain. J Cell Biol 115:1319-1331.
31. Lemke G, Reber M (2005) Retinotectal mapping: new insights from molecular genetics. Annu Rev Cell Dev Biol 21:551-580.
32. Lemmon V, McLoon SC (1986) The appearance of an L1-like molecule in the chick primary visual pathway. J Neurosci 6:2987-2994.
33. Lyckman AW, Moya KL, Confaloni A, Jhaveri S (2000) Early postnatal expression of L1 by retinal fibers in the optic tract and synaptic targets of the Syrian hamster. J Comp Neurol 423:40-51.
34. Maness PF, Schachner M (2007) Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10:19-26.
35. Mann F, Harris WA, Holt CE (2004) New views on retinal axon development: a navigation guide. Int J Dev Biol 48:957-964.
36. Matsuoka H, Obama H, Kelly ML, Matsui T, Nakamoto M (2005) Biphasic functions of the kinase-defective Ephb6 receptor in cell adhesion and migration. J Biol Chem 280:29355-29363.
37. McLaughlin T, O'Leary DD (2005) Molecular gradients and development of retinotopic maps. Annu Rev Neurosci 28:327-355.
38. McLaughlin T, Hindges R, O'Leary DD (2003a) Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr Opin Neurobiol 13:57-69.
39. McLaughlin T, Hindges R, Yates PA, O'Leary DD (2003b) Bifunctional action of ephrin-B1 as a repellent and attractant to control bidirectional branch extension in dorsal-ventral retinotopic mapping. Development 130:2407-2418.
40. Mechtersheimer S, Gutwein P, Agmon-Levin N, Stoeck A, Oleszewski M, Riedle S, Fogel M, Lemmon V, Altevogt P (2001) Ectodomain shedding of L1 adhesion molecule promotes cell migration by autocrine binding to integrins. J Cell Biol 155:661-673.
41. Meyer MP, Smith SJ (2006) Evidence from in vivo imaging that synaptogenesis guides the growth and branching of axonal arbors by two distinct mechanisms. J Neurosci 26:3604-3614.
42. Miao H, Strebhardt K, Pasquale EB, Shen TL, Guan JL, Wang B (2005) Inhibition of integrin-mediated cell adhesion but not directional cell migration requires catalytic activity of EphB3 receptor tyrosine kinase. Role of Rho family small GTPases. J Biol Chem 280:923-932.
43. Musial J, Niewiarowski S, Rucinski B, Stewart GJ, Cook JJ, Williams JA, Edmunds Jr LH (1990) Inhibition of platelet adhesion to surfaces of extracorporeal circuits by disintegrins. RGD-containing peptides from viper venoms. Circulation 82:261-273.
44. Needham LK, Thelen K, Maness PF (2001) Cytoplasmic domain mutations of the L1 cell adhesion molecule reduce L1- ankyrin interactions. J Neurosci 21:1490-1500.
45. Otto E, Kunimoto M, McLaughlin T, Bennett V (1991) Isolation and characterization of cDNAs encoding human brain ankyrins reveal a family of alternatively spliced genes. J Cell Biol 114:241-253.
46. Panicker AK, Buhusi M, Erickson A, Maness PF (2006) Endocytosis of beta1 integrins is an early event in migration promoted by the cell adhesion molecule L1. Exp Cell Res 312:299-307.
47. Ruthazer ES, Li J, Cline HT (2006) Stabilization of axon branch dynamics by synaptic maturation. J Neurosci 26:3594-3603.
48. Schmidt JT (2004) Activity-driven sharpening of the retinotectal projection: the search for retrograde synaptic signaling pathways. J Neurobiol 59:114-133.
49. Schmitt AM, Shi J, Wolf AM, Lu CC, King LA, Zou Y (2006) Wnt-Ryk signalling mediates medial-lateral retinotectal topographic mapping. Nature 439:31-37.
50. Scotland P, Zhou D, Benveniste H, Bennett V (1998) Nervous system defects of AnkyrinB (-/-) mice suggest functional overlap between the cell adhesion molecule L1 and 440-kD AnkyrinB in premyelinated axons. J Cell Biol 143:1305-1315.
51. Silletti S, Mei F, Sheppard D, Montgomery AM (2000) Plasmin-sensitive dibasic sequences in the third fibronectin-like domain of L1-cell adhesion molecule (CAM) facilitate homomultimerization and concomitant integrin recruitment. J Cell Biol 149:1485-1502.
52. Simon DK, O'Leary DD (1992) Influence of position along the medial-lateral axis of the superior colliculus on the topographic targeting and survival of retinal axons. Brain Res Dev Brain Res 69:167-172.
53. Stettler EM, Galileo DS (2004) Radial glia produce and align the ligand fibronectin during neuronal migration in the developing chick brain. J Comp Neurol 468:441-451.
54. Stone KE, Sakaguchi DS (1996) Perturbation of the developing Xenopus retinotectal projection following injections of antibodies against beta1 integrin receptors and N-cadherin. Dev Biol 180:297-310.
55. Thelen K, Kedar V, Panicker AK, Schmid RS, Midkiff BR, Maness PF (2002) The neural cell adhesion molecule L1 potentiates integrin-dependent cell migration to extracellular matrix proteins. J Neurosci 22:4918-4931.
56. Tuvia S, Garver TD, Bennett V (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.
57. Whittard JD, Sakurai T, Cassella MR, Gazdoiu M, Felsenfeld DP (2006) MAP kinase pathway-dependent phosphorylation of the L1-CAM ankyrin binding site regulates neuronal growth. Mol Biol Cell 17:2696-2706.
58. Williams SE, Mann F, Erskine L, Sakurai T, Wei S, Rossi DJ, Gale NW, Holt CE, Mason CA, Henkemeyer M (2003) Ephrin-B2 and EphB1 mediate retinal axon divergence at the optic chiasm. Neuron 39:919-935.
59. Williams SE, Grumet M, Colman DR, Henkemeyer M, Mason CA, Sakurai T (2006) A role for Nr-CAM in the patterning of binocular visual pathways. Neuron 50:535-547.
60. Yamagata M, Herman JP, Sanes JR (1995) Lamina-specific expression of adhesion molecules in developing chick optic tectum. J Neurosci 15:4556-4571.
61. Yates PA, Roskies AL, McLaughlin T, O'Leary DD (2001) Topographic-specific axon branching controlled by ephrin-As is the critical event in retinotectal map development. J Neurosci 21:8548-8563.
62. Zisch AH, Stallcup WB, Chong LD, Dahlin-Huppe K, Voshol J, Schachner M, Pasquale EB (1997) Tyrosine phosphorylation of L1 family adhesion molecules: implication of the Eph kinase Cek5. J Neurosci Res 47:655-665.