Doublecortin (DCX) mediates endocytosis of neurofascin independently of microtubule binding

Journal of Neuroscience

Volumn 32, Issue 22, 2012, Pages 7439-7453

  Yap, Chan Choo ^a   Vakulenko, Max ^a   Kruczek, Kamil ^a   Motamedi, Bashir ^a   Digilio, Laura ^a   Liu, Judy S ^b   Winckler, Bettina ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; DOUBLECORTIN; NERVE CELL ADHESION MOLECULE L1; NEUROFASCIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; DOWN REGULATION; ENDOCYTOSIS; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MALE; MICROTUBULE ASSEMBLY; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT;

ANIMALS; ANKYRINS; CELL ADHESION MOLECULES; CELL MEMBRANE; CELL POLARITY; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; DENDRITES; EMBRYO, MAMMALIAN; ENDOCYTOSIS; FEMALE; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; HUMANS; IMMUNOPRECIPITATION; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MALE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NERVE GROWTH FACTORS; NEURONS; NEUROPEPTIDES; POINT MUTATION; PROTEIN BINDING; RATS; RNA, SMALL INTERFERING; SODIUM CHANNELS; STATISTICS, NONPARAMETRIC; TIME FACTORS; TRANSFECTION;

EID: 84861624234     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5318-11.2012     Document Type: Article

References (57)

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. Bai J, Ramos RL, Ackman JB, Thomas AM, Lee RV, LoTurco JJ (2003) RNAi reveals doublecortin is required for radial migration in rat neocortex. Nat Neurosci 6:1277-1283.
3. Benmerah A, Bayrou M, Cerf-Bensussan N, Dautry-Varsat A (1999) Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J Cell Sci 112:1303-1311.
4. Boiko T, Vakulenko M, Ewers H, Yap CC, Norden C, Winckler B (2007) Ankyrin-dependent and -independent mechanisms orchestrate axonal compartmentalization of L1 family members neurofascin and L1/neuron-glia cell adhesion molecule. J Neurosci 27:590-603.
5. Bréchet A, Fache MP, Brachet A, Ferracci G, Baude A, Irondelle M, Pereira S, Leterrier C, Dargent B (2008) Protein kinase CK2 contributes to the organization of sodium channels in axonal membranes by regulating their interactions with ankyrin G. J Cell Biol 183:1101-1114.
6. Burkarth N, Kriebel M, Kranz EU, Volkmer H (2007) Neurofascin regulates the formation of gephyrin clusters and their subsequent translocation to the axon hillock of hippocampal neurons. Mol Cell Neurosci 36:59-70.
7. Caspi M, Atlas R, Kantor A, Sapir T, Reiner O (2000) Inter action between LIS1 and doublecortin, two lissencephaly gene products. HumMol Genet 9:2205-2213.
8. Cohen D, Segal M, Reiner O (2008) Doublecortin supports the development of dendritic arbors in primary hippocampal neurons. Dev Neurosci 30:187-199.
9. des Portes V, Francis F, Pinard JM, Desguerre I, Moutard ML, Snoeck I, Meiners LC, Capron F, Cusmai R, Ricci S, Motte J, Echenne B, Ponsot G, Dulac O, Chelly J, Beldjord C (1998) doublecortin is the major gene causing X-linked subcortical laminar heterotopia (SCLH). Hum Mol Genet 7:1063-1070.
10. Deuel TA, Liu JS, Corbo JC, Yoo SY, Rorke-Adams LB, Walsh CA (2006) Genetic interactions between doublecortin and doublecortin-like kinase in neuronal migration and axon outgrowth. Neuron 49:41-53.
11. Dzhashiashvili Y, Zhang Y, Galinska J, Lam I, Grumet M, Salzer JL (2007) Nodes of Ranvier and axon initial segments are ankyrin G-dependent domains that assemble by distinct mechanisms. J Cell Biol 177:857-870.
12. Fourgeaud L, Bessis AS, Rossignol F, Pin JP, Olivo-Marin JC, Hémar A (2003) The metabotropic glutamate receptor mGluR5 is endocytosed by a clathrin-independent pathway. J Biol Chem 278:12222-12230.
13. Friocourt G, Chafey P, Billuart P, Koulakoff A, Vinet MC, Schaar BT, McConnell SK, Francis F, Chelly J (2001) Doublecortin interacts with mu subunits of clathrin adaptor complexes in the developing nervous system. Mol Cell Neurosci 18:307-319.
14. Friocourt G, Koulakoff A, Chafey P, Boucher D, Fauchereau F, Chelly J, Francis F (2003) Doublecortin functions at the extremities of growing neuronal processes. Cereb Cortex 13:620-626.
15. Gleeson JG, Allen KM, Fox JW, Lamperti ED, Berkovic S, Scheffer I, Cooper EC, Dobyns WB, Minnerath SR, Ross ME, Walsh CA (1998) Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 92: 63-72.
16. Grubb MS, Burrone J (2010) Building and maintaining the axon initial segment. Curr Opin Neurobiol 20:481-488.
17. Hedstrom KL, Rasband MN (2006) Intrinsic and extrinsic determinants of ion channel localization in neurons. J Neurochem 98:1345-1352.
18. Hedstrom KL, Xu X, Ogawa Y, Frischknecht R, Seidenbecher CI, Shrager P, Rasband MN (2007) Neurofascin assembles a specialized extracellular matrix at the axon initial segment. J Cell Biol 178:875-886.
19. Horton AC, Ehlers MD (2003) Neuronal polarity and trafficking. Neuron 40:277-295.
20. Hortsch M (2000) Structural and functional evolution of the L1 family: are four adhesion molecules better than one? Mol Cell Neurosci 15:1-10.
21. Kappeler C, Dhenain M, Phan Dinh Tuy F, Saillour Y, Marty S, Fallet-Bianco C, Souville I, Souil E, Pinard JM, Meyer G, Encha-Razavi F, Volk A, Beldjord C, Chelly J, Francis F (2007) Magnetic resonance imaging and histological studies of corpus callosal and hippocampal abnormalities linked to doublecortin deficiency. J Comp Neurol 500:239-254.
22. Kawauchi T, Sekine K, Shikanai M, Chihama K, Tomita K, Kubo K, Nakajima K, Nabeshima Y, Hoshino M (2010) Rab GTPases-dependent endocytic pathways regulate neuronal migration and maturation through N-cadherin trafficking. Neuron 67:588-602.
23. Kerjan G, Gleeson JG (2007) Genetic mechanisms underlying abnormal neuronal migration in classical lissencephaly. Trends Genet 23:623-630.
24. Kerjan G, Koizumi H, Han EB, Dubé CM, Djakovic SN, Patrick GN, Baram TZ, Heinemann SF, Gleeson JG (2009) Mice lacking doublecortin and doublecortin-like kinase 2 display altered hippocampal neuronal maturationand spontaneous seizures. Proc Natl Acad Sci U S A 106:6766-6771.
25. Kim MH, Cierpicki T, Derewenda U, Krowarsch D, Feng Y, Devedjiev Y, Dauter Z, Walsh CA, Otlewski J, Bushweller JH, Derewenda ZS (2003) The DCX-domain tandems of doublecortin and doublecortin-like kinase. Nat Struct Biol 10:324-333.
26. 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.
27. Kriebel M, Metzger J, Trinks S, Chugh D, Harvey RJ, Harvey K, Volkmer H (2011) The cell adhesion molecule neurofascin stabilizes axo-axonic GABAergic terminals at the axon initial segment. J Biol Chem 286:24385-24393.
28. Kuba H (2010) Plasticity at the axon initial segment. Commun Integr Biol 3:597-598.
29. Lasiecka ZM, Yap CC, Vakulenko M, Winckler B (2009) Compartmentalizing the neuronal plasma membrane from axon initial segments to synapses. Int Rev Cell Mol Biol 272:303-389.
30. Leger PL, Souville I, Boddaert N, Elie C, Pinard JM, Plouin P, Moutard ML, des Portes V, Van Esch H, Joriot S, Renard JL, Chelly J, Francis F, Beldjord C, Bahi-Buisson N (2008) The location of DCX mutations predicts malformation severity in X-linked lissencephaly. Neurogenetics 9:277-285.
31. Liu JS (2011) Molecular genetics of neuronal migration disorders. Curr Neurol Neurosci Rep 11:171-178.
32. LoTurco JJ, Bai J (2006) The multipolar stage and disruptions in neuronal migration. Trends Neurosci 29:407-413.
33. 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.
34. Ogawa Y, Rasband MN (2008) The functional organization and assembly of the axon initial segment. Curr Opin Neurobiol 18:307-313.
35. Pruss T, Niere M, Kranz EU, Volkmer H (2004) Homophilic interactions of chick neurofascin in trans are important for neurite induction. Eur J Neurosci 20:3184-3188.
36. Pruss T, Kranz EU, Niere M, Volkmer H (2006) A regulated switch of chick neurofascin isoforms modulates ligand recognition and neurite extension. Mol Cell Neurosci 31:354-365.
37. Rasband MN (2010) The axon initial segment and the maintenance of neuronal polarity. Nat Rev Neurosci 11:552-562.
38. Salzer JL (2003) Polarized domains of myelinated axons. Neuron 40: 297-318.
39. Salzer JL, Brophy PJ, Peles E (2008) Molecular domains of myelinated axons in the peripheral nervous system. Glia 56:1532-1540.
40. Sapir T, Horesh D, Caspi M, Atlas R, Burgess HA, Wolf SG, Francis F, Chelly J, Elbaum M, Pietrokovski S, Reiner O (2000) Doublecortin mutations cluster in evolutionarily conserved functional domains. Hum Mol Genet 9:703-712.
41. Schaar BT, Kinoshita K, McConnell SK (2004) Doublecortin microtubule affinity is regulated by a balance of kinase and phosphatase activity at the leading edge of migrating neurons. Neuron 41:203-213.
42. Sherman DL, Tait S, Melrose S, Johnson R, Zonta B, Court FA, Macklin WB, Meek S, Smith AJ, Cottrell DF, Brophy PJ (2005) Neurofascins are required to establish axonal domains for saltatory conduction. Neuron 48:737-742.
43. Shieh JC, Schaar BT, Srinivasan K, Brodsky FM, McConnell SK (2011) Endocytosis regulates cell soma translocation and the distribution of adhesion proteins in migrating neurons. PLoS One 6:e17802.
44. Tanaka T, Serneo FF, Higgins C, Gambello MJ, Wynshaw-Boris A, Gleeson JG (2004) Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J Cell Biol 165:709-721.
45. Tint I, Jean D, Baas PW, Black MM (2009) Doublecortin associates with microtubules preferentially in regions of the axon displaying actin-rich protrusive structures. J Neurosci 29:10995-11010.
46. Tsukada M, Prokscha A, Oldekamp J, Eichele G (2003) Identification of neurabin II as a novel doublecortin interacting protein. Mech Dev 120:1033-1043.
47. 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 U S A 94:12957-12962.
48. Vacher H, Yang JW, Cerda O, Autillo-Touati A, Dargent B, Trimmer JS (2011) Cdk-mediated phosphorylation of the Kvbeta2 auxiliary subunit regulates Kv1 channel axonal targeting. J Cell Biol 192:813-824.
49. Volkmer H, Leuschner R, Zacharias U, Rathjen FG (1996) Neurofascin induces neurites by heterophilic interactions with axonal NrCAM while NrCAM requires F11 on the axonal surface to extend neurites. J Cell Biol 135:1059-1069.
50. Winckler B, Mellman I (2010) Trafficking guidance receptors. Cold Spring Harb Perspect Biol 2:a001826.
51. Wisco D, Anderson ED, Chang MC, Norden C, Boiko T, Fölsch H, Winckler B (2003) Uncovering multiple axonal targeting pathways in hippocampal neurons. J Cell Biol 162:1317-1328.
52. Yap CC, Wisco D, Kujala P, Lasiecka ZM, Cannon JT, Chang MC, Hirling H, Klumperman J, Winckler B (2008a) The somatodendritic endosomal regulator NEEP21 facilitates axonal targeting of L1/NgCAM. J Cell Biol 180:827-842.
53. Yap CC, Nokes RL, Wisco D, Anderson E, Fölsch H, Winckler B (2008b) Pathway selection to the axon depends on multiple targeting signals in NgCAM. J Cell Sci 121:1514-1525.
54. Yap CC, Lasiecka ZM, Caplan S, Winckler B (2010) Alterations of EHD1/EHD4 protein levels interfere with L1/NgCAM endocytosis in neurons and disrupt axonal targeting. J Neurosci 30:6646-6657.
55. Zhang X, Davis JQ, Carpenter S, Bennett V (1998) Structural requirements for association of neurofascin with ankyrin. J Biol Chem 273:30785-30794.
56. Zhang Y, Bekku Y, Dzhashiashvili Y, Armenti S, Meng X, Sasaki Y, Milbrandt J, Salzer JL (2012) Assembly and maintenance of nodes of ranvier rely on distinct sources of proteins and targeting mechanisms. Neuron 73: 92-107.
57. Zonta B, Desmazieres A, Rinaldi A, Tait S, Sherman DL, Nolan MF, Brophy PJ (2011) A critical role for Neurofascin in regulating action potential initiation through maintenance of the axon initial segment. Neuron 69:945-956.