Myelin-associated glycoprotein and complementary axonal ligands, gangliosides, mediate axon stability in the CNS and PNS: Neuropathology and behavioral deficits in single- and double-null mice

Experimental Neurology

Volumn 195, Issue 1, 2005, Pages 208-217

  Pan, Baohan ^a   Fromholt, Susan E ^a   Hess, Ellen J ^a   Crawford, Thomas O ^a   Griffin, John W ^a   Sheikh, Kazim A ^a   Schnaar, Ronald L ^a,b  

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

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Axon degeneration; Axon diameter; Hyperactivity; MAG; Motor deficit; Neurofilament spacing

Indexed keywords

GANGLIOSIDE; GANGLIOSIDE GD 1A; GANGLIOSIDE GD 1B; LECTIN; LIGAND; MYELIN ASSOCIATED GLYCOPROTEIN; SIALIC ACID;

ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CENTRAL NERVOUS SYSTEM; COMPARATIVE STUDY; CONTROLLED STUDY; HISTOPATHOLOGY; LOCOMOTION; MOTOR DYSFUNCTION; MOUSE; MOUSE STRAIN; NERVE FIBER; NERVE FIBER DEGENERATION; NEUROFILAMENT; NEUROPATHOLOGY; NONHUMAN; NULL ALLELE; PATHOGENESIS; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS;

ANIMALS; AXONS; BEHAVIOR, ANIMAL; BRAIN CHEMISTRY; CENTRAL NERVOUS SYSTEM; GANGLIOSIDES; GENOTYPE; LIGANDS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; MOTOR ACTIVITY; MYELIN-ASSOCIATED GLYCOPROTEIN; N-ACETYLGALACTOSAMINYLTRANSFERASES; NERVE DEGENERATION; PERIPHERAL NERVOUS SYSTEM; REFLEX; SPINAL CORD; TREMOR;

EID: 23644441748     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2005.04.017     Document Type: Article

References (56)

1. S. Bartsch, D. Montag, M. Schachner, and U. Bartsch Increased number of unmyelinated axons in optic nerves of adult mice deficient in the myelin-associated glycoprotein (MAG) Brain Res. 762 1997 231 234
2. C. Bjartmar, X. Yin, and B.D. Trapp Axonal pathology in myelin disorders J. Neurocytol. 28 1999 383 395
3. C. Bjartmar, G. Kidd, S. Mork, R. Rudick, and B.D. Trapp Neurological disability correlates with spinal cord axonal loss and reduced N-acetyl aspartate in chronic multiple sclerosis patients Ann. Neurol. 48 2000 893 901
4. C. Bjartmar, J.R. Wujek, and B.D. Trapp Axonal loss in the pathology of MS: consequences for understanding the progressive phase of the disease J. Neurol. Sci. 206 2003 165 171
5. W. Bruck, and C. Stadelmann Inflammation and degeneration in multiple sclerosis Neurol. Sci. 24 2003 S265 S267
6. S. Chiavegatto, J. Sun, R.J. Nelson, and R.L. Schnaar A functional role for complex gangliosides: motor deficits in GM2/GD2 synthase knockout mice Exp. Neurol. 166 2000 227 234
7. M.P. Coleman, and V.H. Perry Axon pathology in neurological disease: a neglected therapeutic target Trends Neurosci. 25 2002 532 537
8. B.E. Collins, M. Kiso, A. Hasegawa, M.B. Tropak, J.C. Roder, P.R. Crocker, and R.L. Schnaar Binding specificities of the sialoadhesin family of I-type lectins. Sialic acid linkage and substructure requirements for binding of myelin-associated glycoprotein, Schwann cell myelin protein, and sialoadhesin J. Biol. Chem. 272 1997 16889 16895
9. B.E. Collins, L.J.S. Yang, G. Mukhopadhyay, M.T. Filbin, M. Kiso, A. Hasegawa, and R.L. Schnaar Sialic acid specificity of myelin-associated glycoprotein binding J. Biol. Chem. 272 1997 1248 1255
10. P.R. Crocker Siglecs: sialic-acid-binding immunoglobulin-like lectins in cell-cell interactions and signalling Curr. Opin. Struct. Biol. 12 2002 609 615
11. P.R. Crocker, S. Kelm, A. Hartnell, S. Freeman, D. Nath, M. Vinson, and S. Mucklow Sialoadhesin and related cellular recognition molecules of the immunoglobulin superfamily Biochem. Soc. Trans. 24 1996 150 156
12. S.M. Curristin, A. Cao, W.B. Stewart, H. Zhang, J.A. Madri, J.S. Morrow, and L.R. Ment Disrupted synaptic development in the hypoxic newborn brain Proc. Natl. Acad. Sci. U. S. A. 99 2002 15729 15734
13. G.H. DeVries, and C.J. Zmachinski The lipid composition of rat CNS axolemma-enriched fractions J. Neurochem. 34 1980 424 430
14. M. Domeniconi, Z. Cao, T. Spencer, R. Sivasankaran, K. Wang, E. Nikulina, N. Kimura, H. Cai, K. Deng, Y. Gao, Z. He, and M. Filbin Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth Neuron 35 2002 283 290
15. J.M. Edgar, and J. Garbern The myelinated axon is dependent on the myelinating cell for support and maintenance: molecules involved J. Neurosci. Res. 76 2004 593 598
16. M.T. Filbin Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS Nat. Rev., Neurosci. 4 2003 703 713
17. R. Frei, S. Motzing, I. Kinkelin, M. Schachner, M. Koltzenburg, and R. Martini Loss of distal axons and sensory Merkel cells and features indicative of muscle denervation in hindlimbs of P0-deficient mice J. Neurosci. 19 1999 6058 6067
18. M. Fruttiger, D. Montag, M. Schachner, and R. Martini Crucial role for the myelin-associated glycoprotein in the maintenance of axon-myelin integrity Eur. J. Neurosci. 7 1995 511 515
19. N. Fujita, A. Kemper, J. Dupree, H. Nakayasu, U. Bartsch, M. Schachner, N. Maeda, K. Suzuki, and B. Popko The cytoplasmic domain of the large myelin-associated glycoprotein isoform is needed for proper CNS but not peripheral nervous system myelination J. Neurosci. 18 1998 1970 1978
20. K. Furukawa, K. Takamiya, and K. Furukawa β1,4-N- acetylgalactosaminyltransferase-GM2/GD2 synthase: a key enzyme to control the synthesis of brain-enriched complex gangliosides Biochim. Biophys. Acta 1573 2002 356 362
21. K.K. Galli, R.A. Zimmerman, G.P. Jarvik, G. Wernovsky, M.K. Kuypers, R.R. Clancy, L.M. Montenegro, W.T. Mahle, M.F. Newman, A.M. Saunders, S.C. Nicolson, T.L. Spray, and J.W. Gaynor Periventricular leukomalacia is common after neonatal cardiac surgery J. Thorac. Cardiovasc. Surg. 127 2004 692 704
22. H. Kawai, M.L. Allende, R. Wada, M. Kono, K. Sango, C. Deng, T. Miyakawa, J.N. Crawley, N. Werth, U. Bierfreund, K. Sandhoff, and R.L. Proia Mice expressing only monosialoganglioside GM3 exhibit lethal audiogenic seizures J. Biol. Chem. 276 2001 6885 6888
23. K.M. Krajewski, R.A. Lewis, D.R. Fuerst, C. Turansky, S.R. Hinderer, J. Garbern, J. Kamholz, and M.E. Shy Neurological dysfunction and axonal degeneration in Charcot-Marie-Tooth disease type 1A Brain 123 2000 1516 1527
24. P.L. Kuhn, E. Petroulakis, G.A. Zazanis, and R.D. McKinnon Motor function analysis of myelin mutant mice using a rotarod Int. J. Dev. Neurosci. 13 1995 715 722
25. H. Lassmann, U. Bartsch, D. Montag, and M. Schachner Dying-back oligodendrogliopathy: a late sequel of myelin-associated glycoprotein deficiency Glia 19 1997 104 110
26. C. Li, M.B. Tropak, R. Gerial, S. Clapoff, W. Abramow-Newerly, B. Trapp, A. Peterson, and J. Roder Myelination in the absence of myelin-associated glycoprotein Nature 369 1994 747 750
27. Y. Liu, R. Wada, H. Kawai, K. Sango, C. Deng, T. Tai, M.P. McDonald, K. Araujo, J.N. Crawley, U. Bierfreund, K. Sandhoff, K. Suzuki, and R.L. Proia A genetic model of substrate deprivation therapy for a glycosphingolipid storage disorder J. Clin. Invest. 103 1999 497 505
28. B.P. Liu, A. Fournier, T. GrandPre, and S.M. Strittmatter Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor Science 297 2002 1190 1193
29. J. Marcus, J.L. Dupree, and B. Popko Myelin-associated glycoprotein and myelin galactolipids stabilize developing axo-glial interactions J. Cell Biol. 156 2002 567 577
30. T.M. Mayhew An efficient sampling scheme for estimating fibre number from nerve cross sections: the fractionator J. Anat. 157 1988 127 134
31. T.M. Mayhew, and A.K. Sharma Sampling schemes for estimating nerve fibre size. I. Methods for nerve trunks of mixed fascicularity J. Anat. 139 1984 45 58
32. L. McKerracher, S. David, D.L. Jackson, V. Kottis, R.J. Dunn, and P.E. Braun Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth Neuron 13 1994 805 811
33. D. Montag, K.P. Giese, U. Bartsch, R. Martini, Y. Lang, H. Bluthmann, J. Karthingasan, D.A. Kirschner, E.S. Wintergerst, K.-A. Nave, J. Zielasek, K.V. Toyka, H.-P. Lipp, and M. Schachner Mice deficient for the myelin-associated glycoprotein show subtle abnormalities in myelin Neuron 13 1994 229 246
34. R.E. Morris, G.M. Ciraolo, D.A. Cohen, and H.C. Bubel In situ fixation of cultured mouse peritoneal exudate cells: comparison of fixation methods In Vitro 16 1980 136 146
35. G. Mukhopadhyay, P. Doherty, F.S. Walsh, P.R. Crocker, and M.T. Filbin A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration Neuron 13 1994 757 767
36. R.H. Quarles Myelin sheaths: glycoproteins involved in their formation, maintenance and degeneration Cell. Mol. Life Sci. 59 2002 1851 1871
37. A. Sandvig, M. Berry, L.B. Barrett, A. Butt, and A. Logan Myelin-, reactive glia-, and scar-derived CNS axon growth inhibitors: expression, receptor signaling, and correlation with axon regeneration Glia 46 2004 225 251
38. R.L. Schnaar Glycobiology of the nervous system B. Ernst G.W. Hart P. Sinaÿ Carbohydrates in Chemistry and Biology, Part II: Biology of Saccharides 2000 Wiley-VCH Weinheim, Germany 1013 1027.
39. K.A. Sheikh, J. Sun, Y. Liu, H. Kawai, T.O. Crawford, R.L. Proia, J.W. Griffin, and R.L. Schnaar Mice lacking complex gangliosides develop Wallerian degeneration and myelination defects Proc. Natl. Acad. Sci. U. S. A. 96 1999 7532 7537
40. M.A. Simpson, H. Cross, K. Gurtz, D.A. Priestman, D.C.A. Neville, G. Reinkensmeier, M. Wiznitzer, C. Proukakis, A. Verganelaki, A. Pryde, M.A. Patton, R.A. Dwek, T.D. Butters, F.M. Platt, and A.H. Crosby Infantile onset symptomatic epilepsy syndrome caused by homozygous loss of function mutations in GM3 synthase Nat. Genet. 36 2004 1225 1229
41. J. Sun, N.L. Shaper, S. Itonori, M. Heffer-Lauc, K.A. Sheikh, and R.L. Schnaar Myelin-associated glycoprotein (Siglec-4) expression is progressively and selectively decreased in the brains of mice lacking complex gangliosides Glycobiology 14 2004 851 857
42. L. Svennerholm Designation and schematic structure of gangliosides and allied glycosphingolipids Prog. Brain Res. 101 1994 xi xiv
43. S. Takashima, M. Kono, N. Kurosawa, Y. Yoshida, Y. Tachida, M. Inoue, T. Kanematsu, and S. Tsuji Genomic organization and transcriptional regulation of the mouse GD3 synthase gene (ST8Sia I): comparison of genomic organization of the mouse sialyltransferase genes J. Biochem. (Tokyo) 128 2000 1033 1043
44. M.E. Taylor, and K. Drickamer Introduction to Glycobiology 2003 Oxford Univ. Press Oxford 207 pp.
45. G. Tettamanti, F. Bonali, S. Marchesini, and V. Zambotti A new procedure for the extraction, purification and fractionation of brain gangliosides Biochim. Biophys. Acta 296 1973 160 170
46. B.D. Trapp Myelin-associated glycoprotein. Location and potential functions Ann. N. Y. Acad. Sci. 605 1990 29 43
47. B.D. Trapp, S.B. Andrews, C. Cootauco, and R. Quarles The myelin-associated glycoprotein is enriched in multivesicular bodies and periaxonal membranes of actively myelinating oligodendrocytes J. Cell Biol. 109 1989 2417 2426
48. T. Uschkureit, O. Sporkel, J. Stracke, H. Bussow, and W. Stoffel Early onset of axonal degeneration in double (plp-/-mag-/-) and hypomyelinosis in triple (plp-/-mbp-/-mag-/-) mutant mice J. Neurosci. 20 2000 5225 5233
49. M.D. Weiss, C.A. Luciano, and R.H. Quarles Nerve conduction abnormalities in aging mice deficient for myelin-associated glycoprotein Muscle Nerve 24 2001 1380 1387
50. J. Weiss, B. Takizawa, A. McGee, W.B. Stewart, H. Zhang, L. Ment, M. Schwartz, and S. Strittmatter Neonatal hypoxia suppresses oligodendrocyte Nogo-A and increases axonal sprouting in a rodent model for human prematurity Exp. Neurol. 189 2004 141 149
51. G. Wu, X. Xie, Z.H. Lu, and R.W. Ledeen Cerebellar neurons lacking complex gangliosides degenerate in the presence of depolarizing levels of potassium Proc. Natl. Acad. Sci. U. S. A. 98 2001 307 312
52. J.R. Wujek, C. Bjartmar, E. Richer, R.M. Ransohoff, M. Yu, V.K. Tuohy, and B.D. Trapp Axon loss in the spinal cord determines permanent neurological disability in an animal model of multiple sclerosis J. Neuropathol. Exp. Neurol. 61 2002 23 32
53. Z. Xu, J.R. Marszalek, M.K. Lee, P.C. Wong, J. Folmer, T.O. Crawford, S.T. Hsieh, J.W. Griffin, and D.W. Cleveland Subunit composition of neurofilaments specifies axonal diameter J. Cell Biol. 133 1996 1061 1069
54. L.J.S. Yang, C.B. Zeller, N.L. Shaper, M. Kiso, A. Hasegawa, R.E. Shapiro, and R.L. Schnaar Gangliosides are neuronal ligands for myelin-associated glycoprotein Proc. Natl. Acad. Sci. U. S. A. 93 1996 814 818
55. X. Yin, T.O. Crawford, J.W. Griffin, P. Tu, V.M. Lee, C. Li, J. Roder, and B.D. Trapp Myelin-associated glycoprotein is a myelin signal that modulates the caliber of myelinated axons J. Neurosci. 18 1998 1953 1962
56. G. Yiu, and Z. He Signaling mechanisms of the myelin inhibitors of axon regeneration Curr. Opin. Neurobiol. 13 2003 545 551