Myelin-associated glycoprotein is a myelin signal that modulates the caliber of myelinated axons

Journal of Neuroscience

Volumn 18, Issue 6, 1998, Pages 1953-1962

  Yin, Xinghua ^a   Crawford, Thomas O ^b   Griffin, John W ^b   Tu, Pang Hsien ^c   Lee, Virginia M Y ^c   Li, Chumei ^d   Roder, John ^d   Trapp, Bruce D ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d MOUNT SINAI HOSPITAL   (Canada)

Author keywords

Axonal atrophy; Axonal caliber; Myelin associated glycoprotein; Neurofilament phosphorylation; Neurofilament spacing; Paranodal tomaculi

Indexed keywords

MYELIN ASSOCIATED GLYCOPROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HISTOPATHOLOGY; MOUSE; MYELINATION; NERVE CONDUCTION; NERVE FIBER TRANSPORT; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

EID: 0032521342     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-06-01953.1998     Document Type: Article

References (49)

1. Adlkofer K, Frei R, Neuberg DH-H, Zielasek J, Toyka KV, Suter U (1997) Heterozygous peripheral myelin protein 22-deficient mice are affected by a progressive demyelinating tomaculous neuropathy. J Neurosci 17:4662-4671.
2. Aguayo AJ, Epps J, Charron L, Bray GM (1976) Multipotentiality of Schwann cells in cross anastomosed and grafted myelinated and unmyelinated nerves: quantitative microscopy and radioautography. Brain Res 104:1-20.
3. Arbuthnott ER, Boyd IA, Kalu KU (1980) Ultrastructural dimensions of myelinated peripheral nerve fibres in the cat and their relation to conduction velocity. J Physiol (Lond) 308:125-157.
4. Arquint M, Roder J, Chia L-S, Down J, Wilkinson O, Bayley H, Braun P, Dunn R (1987) Molecular cloning and primary structure of myelin-associated glycoproteins. Proc Natl Acad Sci USA 84:600-604.
5. Carenini S, Montag D, Cremer H, Schachner M, Martini R (1997) Absence of the myelin-associated glycoprotein (MAG) and the neural cell adhesion molecule (N-CAM) interferes with the maintenance, but not with the formation of peripheral myelin. Cell Tissue Res 287:3-9.
6. Ching GY, Liem RK (1993) Assembly of type IV neuronal intermediate filaments in non-neuronal cells in the absence of pre-existing cytoplasmic intermediate filaments. J Cell Biol 122:1323-1335.
7. Cote F, Collard JF, Julien JP (1993) Progressive neuronopathy in transgenic mice expressing the human neurofilament heavy gene: a mouse model of amyotrophic lateral sclerosis. Cell 73:35-46.
8. deWaegh SM, Lee VM-Y, Brady ST (1992) Local modulation of neurofilament phosphorylation, axonal caliber, and slow axonal transport by myelinating Schwann cells. Cell 68:451-463.
9. Eyer J, Peterson A (1994) Neurofilament-deficient axons and perikaryal aggregates in viable transgenic mice expressing a neurofilament-βgalactosidase fusion protein. Neuron 12:389-405.
10. Friede RL, Samorajski T (1971) Axonal caliber related to neurofilaments and microtubules in sciatic nerve fibers of rats and mice. Anat Rec 167:379-387.
11. Fruttiger M, Montag D, Schachner M, Martini R (1995) Crucial role for the myelin-associated glycoprotein in the maintenance of axon-myelin integrity. Eur J Neurosci 7:511-515.
12. Griffin JW, Kidd G, Trapp BD (1993) Interactions between axons and Schwann cells. In: Peripheral neuropathy (Dyek PJ, Thomas PK, eds), pp 317-330. Philadelphia: Saunders.
13. Hirokawa N, Glicksman MA, Willard MB (1984) Organization of mammalian neurofilament polypeptides within the neuronal cytoskeleton. J Cell Biol 98:1523-1536.
14. Hoffman PN, Griffin JW (1992) Regulation of axonal caliber. In: Peripheral neuropathy (Dyek PJ, Thomas PK, Griffin JW, Low PA, Poduslo J. eds), pp 389-402. New York: Raven.
15. Hoffman PN, Lasek RJ (1975) The slow component of axonal transport: identification of major structural polypeptides of the axon and their generality among mammalian neurons. J Cell Biol 66:351-366.
16. Hsieh S-T, Crawford TO, Bouldin TW, Griffin JW (1993) Influence of demyelination and remyelination on axonal organization. Brain Pathol 3:307.
17. Hsieh S-T, Kidd GJ, Crawford TO, Xu Z, Trapp BD, Cleveland DW, Griffin JW (1994) Regional modulation of neurofilament organization by myelination in normal axons. J Neurosci 14:6392-6401.
18. Johnson PW, Abramow-Newerly W, Seilheimer B, Sadoul R, Tropak MB, Arquint M, Dunn RJ, Schachner M, Roder JC (1989) Recombinant myelin-associated glycoprotein confers neural adhesion and neurite outgrowth function. Neuron 3:377-385.
19. Kirkpatrick LL, Brady ST (1994) Modulation of the axonal microtubule cytoskeleton by myelinating Schwann cells. J Neurosci 12:7440-7450.
20. Lai C, Brow MA, Nave K-A, Noronha AB, Quarles RH, Bloom Ft, Milner RJ, Sutcliffe JG (1987) Two forms of 1B236/myelin-associated glycoprotein (MAG), a cell adhesion molecule for postnatal neural development, are produced by alternative splicing. Proc Natl Acad Sci USA 84:4337-4341.
21. cdc2. J Biol Chem 267:25922-25926.
22. Li C, Tropak MB, Gerial R, Clapoff S, Abramow-Newerly W, Trapp B, Peterson A, Roder J (1994) Myelination in the absence of myelin-associatcd glycoprotein. Nature 369:747-750.
23. Li M, Shibata A, Li C, Braun PF, McKerracher L, Roder J, Kater SB, David S (1996) Myelin-associated glycoprotein inhibits neurite axon growth and causes growth cone collapse. J Neurosci Res 46:404-414.
24. McKerracher L, David S, Jackson DL, Kottis V, Dunn RJ, Braun PE (1994) Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13:805-811.
25. Montag D, Giese KP, Bartsch U, Martini R, Land Y, Blüthmann H, Karthigasan J, Kirschner DA, Wintergerst ES, Nave K-A, Zielasek J, Toyka KV, Lipp H, Schachner M (1994) Mice deficient for the myelin-associated glycoprotein show subtle abnormalities in myelin. Neuron 13:229-246.
26. Mukhopadhyay G, Doherty P, Walsh FS, Crocker PR, Filbin MT (1994) A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13:757-767.
27. Nakagawa T, Chen J, Zhang Z, Kanai Y, Hirokawa N (1995) Two distinct functions of the carboxyl-terminal tail domain of NF-M upon neurofilament assembly: cross-bridge formation and longitudinal elongation of filaments. J Cell Biol 129:411-429.
28. Ohara O, Gahara Y, Miyake T, Teraoka H, Kitamura T (1993) Neurofilament deficiency in quail caused by nonsense mutation in neurofilament-L gene. J Cell Biol 121:387-395.
29. Owens GC, Bunge RP (1991) Schwann cells infected with a recombinant retrovirus expressing myelin-associated glycoprotein antisense RNA do not form myelin. Neuron 7:565-575.
30. Owens GC, Boyd CJ, Bunge RP, Salzer JL (1990) Expression of recombinant myelin-associated glycoprotein in primary Schwann cells promotes the initial investment of axons by myelinating Schwann cells. J Cell Biol 111:1171-1182.
31. Pant HC, Veeranna (1995) Neurofilament phosphorylation. Biochem Cell Biol 73:575-592.
32. Poltorak M, Sadoul R, Keilhauer G, Landa C, Fahrig T, Schachner M (1987) Myelin-associated glycoprotein, a member of the L2/HNK-1 family of neural cell adhesion molecules, is involved in neuronoligodendrocyte and oligodendrocyte-oligodendrocyte interaction. J Cell Biol 105:1893-1899.
33. Raine CS, Cross AH (1989) Axonal dystrophy as a consequence of long-term demyelination. Lab Invest 60:714-725.
34. Salzer JL, Holmes WP, Colman DR (1987) The amino acid sequences of the myelin-associated glycoproteins: homology to the immunoglobulin gene superfamily. J Cell Biol 104:957-965.
35. Sanchez I, Hassinger L, Paskevich PA, Shine HD, Nixon RA (1996) Oligodendroglia regulate the regional expansion of axon caliber and local accumulation of neurofilaments during development independently of myelin formation. J Neurosci 16:5095-5105.
36. Shetty KT, Link WT, Pant HC (1993) cdc2-like kinase from rat spinal cord specifically phosphorylates KSPXK motifs in neurofilament proteins: isolation and characterization. Proc Natl Acad Sci USA 90:6844-6848.
37. Sternberger NH, Quarles RH, Itoyama Y, Webster HdeF (1979) Myelin-associated glycoprotein demonstrated immunocytochemically in myelin and myelin-forming cells of developing rats. Proc Natl Acad Sci USA 76:1510-1514.
38. Suter U, Welcher AA, Ozcelik T, Snipes GJ, Kosaras B, Francke U, Billings-Gagliardi S, Sidman RL, Shooter EM (1992) Trembler mouse carries a point mutation in a myelin gene. Nature 356:241-244.
39. Trapp BD, Ouarles RH (1982) Presence of the myclin-associated glycoprotein correlates with alterations in the periodicity of peripheral myelin. J Cell Biol 92:877-882.
40. Trapp BD, Andrews SB, Cootauco C, Ouarles RH (1989) The myelin-associated glycoprotein is enriched in multivesicular bodies and periaxonal membranes of actively myelinating oligodendrocytes. J Cell Biol 109:2417-2426.
41. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mörk S, Bö L (1998) Axonal transection in multiple sclerosis lesions. N Engl J Med 338:278-285.
42. Tu P-H, Elder G, Lazzarini RA, Nelson D, Trojanowski JO, Lee VM-Y (1995) Overexpression of the human NFM subunit in transgenic mice modifies the level of endogenous NFL and the phosphorylation state of NFH subunits. J Cell Biol 129:1629-1640.
43. Veeranna, Shelly KT, Link WT, Jaffe H, Wang J, Panl HC (1995) Neuronal cyclin-dependent kinase-5 phosphorylation sites in neurofilament protein (NF-H) are dephosphorylation by protein phosphatase 2A. J Neurochem 64:2681-2690.
44. Waxman SG (1980) Determinants of conduction velocity in myelinated nerve fiber. Muscle Nerve 3:141-150.
45. Weinberg HJ, Spencer PS (1976) Studies on the control of myelinogenesis. II. Evidence for neuronal regulation of myelin production. Brain Res 113:363-378.
46. Windebank AJ, Word P, Bunge RP, Dyck PJ (1985) Myelination determines the caliber of dorsal root ganglion neurons in culture. J Neurosci 5:1563-1567.
47. Wong PC, Marszalek J, Crawford TO, Xu Z, Hsieh S-T, Griffin JW, Cleveland DW (1995) Increasing neurofilament subunit NF-M expression reduces axonal NF-H, inhibits radial growth, and results in neurofilamentous accumulation in motor neurons. J Cell Biol 130:1413-1422.
48. Xu Z, Marszalek JR, Lee MK, Wong PC, Folmer J, Crawford TO, Hsieh S-T, Griffin JW, Cleveland DW (1996) Subunit composition of neurofilaments specifies axonal diameter. J Cell Biol 133:1061-1069.
49. A/glycogen synthase kinase 3 alpha predominantly phosphorylates the in vivo sites of Ser502, Ser506, Ser603, and Ser666 in neurofilament. J Neurochem 64:1848-1854.