Maintenance of axo-oligodendroglial paranodal junctions requires DCC and netrin-1

Journal of Neuroscience

Volumn 28, Issue 43, 2008, Pages 11003-11014

  Jarjour, Andrew A ^a,b   Bull, Sarah Jane ^a,b   Almasieh, Mohammadali ^c   Rajasekharan, Sathyanath ^a,b   Baker, K Adam ^a,b   Mui, Jeannie ^b   Antel, Jack P ^a,b   Di Polo, Adriana ^c   Kennedy, Timothy E ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Axoglial junction; Caspr; Myelin; Neurofascin; Paranode; Septate like junctions

Indexed keywords

CHEMOTACTIC FACTOR; MYELIN; NETRIN 1; POTASSIUM CHANNEL; PROTEIN DELETED IN COLORECTAL CANCER; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; CELL SURFACE RECEPTOR; CNTNAP1 PROTEIN, MOUSE; DCC PROTEIN, RAT; MYELIN BASIC PROTEIN; NERVE CELL ADHESION MOLECULE; NERVE GROWTH FACTOR; NETRIN-1; NFASC PROTEIN, MOUSE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CELL MATURATION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONTROLLED STUDY; MALE; MUTATIONAL ANALYSIS; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; ULTRASTRUCTURE; ANIMAL; CELL JUNCTION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IN VITRO STUDY; METABOLISM; METHODOLOGY; MOUSE; MOUSE MUTANT; NEWBORN; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; RETINA; SPRAGUE DAWLEY RAT; STEM CELL; STEM CELL TRANSPLANTATION; TIME; TRANSMISSION ELECTRON MICROSCOPY; TRANSPLANTATION;

ANIMALS; ANIMALS, NEWBORN; AXONS; CELL ADHESION MOLECULES; CELL ADHESION MOLECULES, NEURONAL; CEREBELLUM; GAP JUNCTIONS; GENE EXPRESSION REGULATION; MALE; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; MYELIN BASIC PROTEINS; NERVE GROWTH FACTORS; OLIGODENDROGLIA; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CELL SURFACE; RETINA; STEM CELL TRANSPLANTATION; STEM CELLS; TIME FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 58149161906     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3285-08.2008     Document Type: Article

References (48)

1. Baker KA, Moore SW, Jarjour AA, Kennedy TE (2006) When a diffusible axon guidance cue stops diffusing: roles for netrins in adhesion and morphogenesis. Curr Opin Neurobiol 16:529-534.
2. Berliner ML (1931) Cytologic studies on the retina. I. Normal coexistence of oligodendroglia and myelinated nerve fibers. Arch Ophthalmol 6:740-751.
3. Bhat MA, Rios JC, Lu Y, Garcia-Fresco GP, Ching W, St Martin M, Li J, Einheber S, Chesler M, Rosenbluth J, Salzer JL, Bellen HJ (2001) Axonglia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron 30:369-383.
4. Bonnon C, Bel C, Goutebroze L, Maigret B, Girault JA, Faivre-Sarrailh C (2007) PGY repeats and N-glycans govern the trafficking of paranodin and its selective association with contactin and neurofascin-155. Mol Biol Cell 18:229-241.
5. Boyle ME, Berglund EO, Murai KK, Weber L, Peles E, Ranscht B (2001) Contactin orchestrates assembly of the septate-like junctions at the paranode in myelinated peripheral nerve. Neuron 30:385-397.
6. Charles P, Tait S, Faivre-Sarrailh C, Barbin G, Gunn-Moore F, Denisenko-Nehrbass N, Guennoc AM, Girault JA, Brophy PJ, Lubetzki C (2002) Neurofascin is a glial receptor for the paranodin/Caspr-contactin axonal complex at the axoglial junction. Curr Biol 12:217-220.
7. Chiu SY, Zhou L, Zhang CL, Messing A (1999) Analysis of potassium channel functions in mammalian axons by gene knockouts. J Neurocytol 28:349-364.
8. Dupree JL, Coetzee T, Blight A, Suzuki K, Popko B (1998) Myelin galactolipids are essential for proper node of Ranvier formation in the CNS. J Neurosci 18:1642-1649.
9. Dupree JL, Girault JA, Popko B (1999) Axo-glial interactions regulate the localization of axonal paranodal proteins. J Cell Biol 147:1145-1152.
10. Einheber S, Zanazzi G, Ching W, Scherer S, Milner TA, Peles E, Salzer JL (1997) The axonal membrane protein Caspr, a homologue of neurexin IV, is a component of the septate-like paranodal junctions that assemble during myelination. J Cell Biol 139:1495-1506.
11. Faivre-Sarrailh C, Gauthier F, Denisenko-Nehrbass N, Le Bivic A, Rougon G, Girault JA (2000) The glycosylphosphatidyl inositol-anchored adhesion molecule F3/contactin is required for surface transport of paranodin/contactin- associated protein (caspr). J Cell Biol 149:491-502.
12. Fazeli A, Dickinson SL, Hermiston ML, Tighe RV, Steen RG, Small CG, Stoeckli ET, Keino-Masu K, Masu M, Rayburn H, Simons J, Bronson RT, Gordon JI, Tessier-Lavigne M, Weinberg RA (1997) Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 386:796-804.
13. Foran DR, Peterson AC (1992) Myelin acquisition in the central nervous system of the mouse revealed by an MBP-Lac Z transgene. J Neurosci 12:4890-4897.
14. Ishibashi T, Dupree JL, Ikenaka K, Hirahara Y, Honke K, Peles E, Popko B, Suzuki K, Nishino H, Baba H (2002) A myelin galactolipid, sulfatide, is essential for maintenance of ion channels on myelinated axon but not essential for initial cluster formation. J Neurosci 22:6507-6514.
15. Jarjour AA, Manitt C, Moore SW, Thompson KM, Yuh SJ, Kennedy TE (2003) Netrin-1 is a chemorepellent for oligodendrocyte precursor cells in the embryonic spinal cord. J Neurosci 23:3735-3744.
16. Kappler J, Franken S, Junghans U, Hoffmann R, Linke T, Müller HW, Koch KW (2000) Glycosaminoglycan-binding properties and secondary structure of the C-terminus of netrin-1. Biochem Biophys Res Commun 271:287-291.
17. Laeng P, Molthagen M, Yu EG, Bartsch U (1996) Transplantation of oligodendrocyte progenitor cells into the rat retina: extensive myelination of retinal ganglion cell axons. Glia 18:200-210.
18. Li W, Lee J, Vikis HG, Lee SH, Liu G, Aurandt J, Shen TL, Fearon ER, Guan JL, Han M, Rao Y, Hong K, Guan KL (2004) Activation of FAK and Src are receptor-proximal events required for netrin signaling. Nat Neurosci 7:1213-1221.
19. Manitt C, Colicos MA, Thompson KM, Rousselle E, Peterson AC, Kennedy TE (2001) Widespread expression of netrin-1 by neurons and oligodendrocytes in the adult mammalian spinal cord. J Neurosci 21:3911-3922.
20. Manitt C, Thompson KM, Kennedy TE (2004) Developmental shift in expression of netrin receptors in the rat spinal cord: predominance of UNC-5 homologues in adulthood. J Neurosci Res 77:690-700.
21. Marcus J, Dupree JL, Popko B (2002) Myelin-associated glycoprotein and myelin galactolipids stabilize developing axo-glial interactions. J Cell Biol 156:567-577.
22. Menon K, Rasband MN, Taylor CM, Brophy P, Bansal R, Pfeiffer SE (2003) The myelin-axolemmal complex: biochemical dissection and the role of galactosphingolipids. J Neurochem 87:995-1009.
23. Meriane M, Tcherkezian J, Webber CA, Danek EI, Triki I, McFarlane S, Bloch-Gallego E, Lamarche-Vane N (2004) Phosphorylation of DCC by Fyn mediates Netrin-1 signaling in growth cone guidance. J Cell Biol 167:687-698.
24. Moore SW, Tessier-Lavigne M, Kennedy TE (2007) Netrins and their receptors. Adv Exp Med Biol 621:17-31.
25. Notterpek LM, Bullock PN, Malek-Hedayat S, Fisher R, Rome LH (1993) Myelination in cerebellar slice cultures: development of a system amenable to biochemical analysis. J Neurosci Res 36:621-634.
26. Osterhout DJ, Wolven A, Wolf RM, Resh MD, Chao MV (1999) Morphological differentiation of oligodendrocytes requires activation of Fyn tyrosine kinase. J Cell Biol 145:1209-1218.
27. Pedraza L, Huang JK, Colman DR (2001) Organizing principles of the axoglial apparatus. Neuron 30:335-344.
28. Poliak S, Peles E (2003) The local differentiation of myelinated axons at nodes of Ranvier. Nat Rev Neurosci 4:968-980.
29. Rasband MN, Taylor CM, Bansal R (2003) Paranodal transverse bands are required for maintenance but not initiation of Nav1.6 sodium channel clustering in CNS optic nerve axons. Glia 44:173-182.
30. Rasband MN, Tayler J, Kaga Y, Yang Y, Lappe-Siefke C, Nave KA, Bansal R (2005) CNP is required for maintenance of axon-glia interactions at nodes of Ranvier in the CNS. Glia 50:86-90.
31. Reynolds R, Wilkin GP (1988) Development of macroglial cells in rat cerebellum. II. An in situ immunohistochemical study of oligodendroglial lineage from precursor to mature myelinating cell. Development 102:409-425.
32. Rios JC, Melendez-Vasquez CV, Einheber S, Lustig M, Grumet M, Hemperly J, Peles E, Salzer JL (2000) Contactin-associated protein (Caspr) and contactin form a complex that is targeted to the paranodal junctions during myelination. J Neurosci 20:8354-8364.
33. Sapieha PS, Duplan L, Uetani N, Joly S, Tremblay ML, Kennedy TE, Di Polo A (2005) Receptor protein tyrosine phosphatase sigma inhibits axon regrowth in the adult injured CNS. Mol Cell Neurosci 28:625-635.
34. Schaeren-Wiemers N, Bonnet A, Erb M, Erne B, Bartsch U, Kern F, Mantei N, Sherman D, Suter U (2004) The raft-associated protein MAL is required for maintenance of proper axon-glia interactions in the central nervous system. J Cell Biol 166:731-742.
35. Schafer DP, Bansal R, Hedstrom KL, Pfeiffer SE, Rasband MN (2004) Does paranode formation and maintenance require partitioning of neurofascin 155 into lipid rafts? J Neurosci 24:3176-3185.
36. Serafini T, Kennedy TE, Galko MJ, Mirzayan C, Jessell TM, Tessier-Lavigne M (1994) The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78:409-424.
37. Serafini T, Colamarino SA, Leonardo ED, Wang H, Beddington R, Skarnes WC, Tessier-Lavigne M (1996) Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87:1001-1014.
38. Shekarabi M, Kennedy TE (2002) The netrin-1 receptor DCC promotes filopodia formation and cell spreading by activating Cdc42 and Rac1. Mol Cell Neurosci 19:1-17.
39. Shekarabi M, Moore SW, Tritsch NX, Morris SJ, Bouchard JF, Kennedy TE (2005) Deleted in colorectal cancer binding netrin-1 mediates cell substrate adhesion and recruits Cdc42, Rac1, Pak1, and N-WASP into an intracellular signaling complex that promotes growth cone expansion. J Neurosci 25:3132-3141.
40. 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.
41. Sperber BR, Boyle-Walsh EA, Engleka MJ, Gadue P, Peterson AC, Stein PL, Scherer SS, McMorris FA (2001) A unique role for Fyn in CNS myelination. J Neurosci 21:2039-2047.
42. Suzuki N, Toyoda H, Sano M, Nishiwaki K (2006) Chondroitin acts in the guidance of gonadal distal tip cells in C. elegans. Dev Biol 300:635-646.
43. Svenningsen AF, Shan WS, Colman DR, Pedraza L (2003) Rapid method for culturing embryonic neuron-glial cell cocultures. J Neurosci Res 72:565-573.
44. Tait S, Gunn-Moore F, Collinson JM, Huang J, Lubetzki C, Pedraza L, Sherman DL, Colman DR, Brophy PJ (2000) An oligodendrocyte cell adhesion molecule at the site of assembly of the paranodal axo-glial junction. J Cell Biol 150:657-666.
45. Tao-Cheng JH, Rosenbluth J (1983) Axolemmal differentiation in myelinated fibers of rat peripheral nerves. Brain Res 285:251-263.
46. Thurnherr T, Benninger Y, Wu X, Chrostek A, Krause SM, Nave KA, Franklin RJ, Brakebusch C, Suter U, Relvas JB (2006) Cdc42 and Rac1 signaling are both required for and act synergistically in the correct formation of myelin sheaths in the CNS. J Neurosci 26:10110-10119.
47. Vabnick I, Trimmer JS, Schwarz TL, Levinson SR, Risal D, Shrager P (1999) Dynamic potassium channel distributions during axonal development prevent aberrant firing patterns. J Neurosci 19:747-758.
48. + channels in terminal and juxtaparanodal regions of neurons. Nature 365:75-79.