Remyelination after cuprizone induced demyelination is accelerated in mice deficient in the polysialic acid synthesizing enzyme St8siaIV

Neuroscience

Volumn 171, Issue 1, 2010, Pages 235-244

  Koutsoudaki, P N ^a,b   Hildebrandt, H ^a,b   Gudi, V ^a,b   Skripuletz, T ^a   Skuljec J ^a,b   Stangel, M ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

Author keywords

C57BL 6J mice; Cuprizone; Myelin; Polysialic acid; Polysialyltransferases

Indexed keywords

CUPRIZONE; GLIAL FIBRILLARY ACIDIC PROTEIN; MYELIN PROTEIN; POLYSIALIC ACID; POLYSIALYLTRANSFERASE ST8SIAIV; SIALYLTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; CORPUS CALLOSUM; DEMYELINATION; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REMYELINIZATION;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ANTIGENS; ANTIGENS, DIFFERENTIATION; CELL COUNT; CELL DIFFERENTIATION; CEREBRAL CORTEX; CORPUS CALLOSUM; CUPRIZONE; DEMYELINATING DISEASES; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOAMINE OXIDASE INHIBITORS; MYELIN BASIC PROTEINS; MYELIN PROTEINS; MYELIN PROTEOLIPID PROTEIN; MYELIN-ASSOCIATED GLYCOPROTEIN; NEURAL CELL ADHESION MOLECULES; NEUROGLIA; NEURONS; PROTEOGLYCANS; REGENERATION; SIALIC ACIDS; SIALYLTRANSFERASES;

EID: 77957878657     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.08.070     Document Type: Article

References (44)

1. Angata K., Fukuda M. Polysialyltransferases: major players in polysialic acid synthesis on the neural cell adhesion molecule. Biochimie 2003, 85:195-206.
2. Bartsch U., Kirchhoff F., Schachner M. Highly sialylated N-CAM is expressed in adult mouse optic nerve and retina. J Neurocytol 1990, 19:550-565.
3. Charles P., Hernandez M.P., Stankoff B., Aigrot M.S., Colin C., Rougon G., Zalc B., Lubetzki C. Negative regulation of central nervous system myelination by polysialylated-neural cell adhesion molecule. Proc Natl Acad Sci U S A 2000, 97:7585-7590.
4. Charles P., Reynolds R., Seilhean D., Rougon G., Aigrot M.S., Niezgoda A., Zalc B., Lubetzki C. Re-expression of PSA-NCAM by demyelinated axons: an inhibitor of remyelination in multiple sclerosis?. Brain 2002, 125:1972-1979.
5. Chung W.W., Lagenaur C.F., Yan Y.M., Lund J.S. Developmental expression of neural cell adhesion molecules in the mouse neocortex and olfactory bulb. J Comp Neurol 1991, 314:290-305.
6. Crawford D.K., Mangiardi M., Xia X., López-Valdés H.E., Tiwari-Woodruff S.K. Functional recovery of callosal axons following demyelination: a critical window. Neuroscience 2009, 164:1407-1421.
7. Eckhardt M., Bukalo O., Chazal G., Wang L., Goridis C., Schachner M., Gerardy-Schahn R., Cremer H., Dityatev A. Mice deficient in the polysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity. J Neurosci 2000, 20:5234-5244.
8. Fewou S.N., Ramakrishnan H., Bussow H., Gieselmann V., Eckhardt M. Down-regulation of polysialic acid is required for efficient myelin formation. J Biol Chem 2007, 282:16700-16711.
9. Franklin R.J. Why does remyelination fail in multiple sclerosis?. Nat Rev Neurosci 2002, 3:705-714.
10. Franklin R.J., Ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 2008, 9:839-855.
11. Frohman E.M., Racke M.K., Raine C.S. Multiple sclerosis-the plaque and its pathogenesis. N Engl J Med 2006, 354:942-955.
12. Frosch M., Gorgen I., Boulnois G.J., Timmis K.N., Bitter-Suermann D. NZB mouse system for production of monoclonal antibodies to weak bacterial antigens: isolation of an IgG antibody to the polysaccharide capsules of Escherichia coli K1 and group B meningococci. Proc Natl Acad Sci U S A 1985, 82:1194-1198.
13. Gudi V., Moharregh-Khiabani D., Skripuletz T., Koutsoudaki P.N., Kotsiari A., Skuljec J., Trebst C., Stangel M. Regional differences between grey and white matter in cuprizone induced demyelination. Brain Res 2009, 1283:127-138.
14. Hildebrandt H., Becker C., Murau M., Gerardy-Schahn R., Rahmann H. Heterogeneous expression of the polysialyltransferases ST8Sia II and ST8Sia IV during postnatal rat brain development. J Neurochem 1998, 71:2339-2348.
15. Hildebrandt H., Muhlenhoff M., Gerardy-Schahn R. Polysialylation of NCAM. Adv Exp Med Biol 2010, 663:95-109.
16. Hiremath M.M., Saito Y., Knapp G.W., Ting J.P., Suzuki K., Matsushima G.K. Microglial/macrophage accumulation during cuprizone-induced demyelination in C57BL/6 mice. J Neuroimmunol 1998, 92:38-49.
17. Koutsoudaki P.N., Skripuletz T., Gudi V., Moharregh-Khiabani D., Hildebrandt H., Trebst C., Stangel M. Demyelination of the hippocampus is prominent in the cuprizone model. Neurosci Lett 2009, 451:83-88.
18. Lindner M., Heine S., Haastert K., Garde N., Fokuhl J., Linsmeier F., Grothe C., Baumgartner W., Stangel M. Sequential myelin protein expression during remyelination reveals fast and efficient repair after central nervous system demyelination. Neuropathol Appl Neurobiol 2008, 34:105-114.
19. Lindner M., Trebst C., Heine S., Skripuletz T., Koutsoudaki P.N., Stangel M. The chemokine receptor CXCR2 is differentially regulated on glial cells in vivo but is not required for successful remyelination after cuprizone-induced demyelination. Glia 2008, 56:1104-1113.
20. Lubetzki C., Williams A., Stankoff B. Promoting repair in multiple sclerosis: problems and prospects. Curr Opin Neurol 2005, 18:237-244.
21. Lucchinetti C., Bruck W., Noseworthy J. Multiple sclerosis: recent developments in neuropathology, pathogenesis, magnetic resonance imaging studies and treatment. Curr Opin Neurol 2001, 14:259-269.
22. Maness P.F., Schachner M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 2007, 10:19-26.
23. Matsushima G.K., Morell P. The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol 2001, 11:107-116.
24. Nacher J., Guirado R., Varea E., Alonso-Llosa G., Röckle I., Hildebrandt H. Divergent impact of the polysialyltransferases ST8SiaII and ST8SiaIV on polysialic acid expression in immature neurons and interneurons of the adult cerebral cortex. Neuroscience 2010, 167:825-837.
25. Norkute A., Hieble A., Braun A., Johann S., Clarner T., Baumgartner W., Beyer C., Kipp M. Cuprizone treatment induces demyelination and astrocytosis in the mouse hippocampus. J Neurosci Res 2009, 87:1343-1355.
26. Oltmann-Norden I., Galuska S.P., Hildebrandt H., Geyer R., Gerardy-Schahn R., Geyer H., Muhlenhoff M. Impact of the polysialyltransferases ST8SiaII and ST8SiaIV on polysialic acid synthesis during postnatal mouse brain development. J Biol Chem 2008, 283:1463-1471.
27. Oumesmar B.N., Vignais L., Duhamel-Clerin E., Avellana-Adalid V., Rougon G., Baron-Van Evercooren A. Expression of the highly polysialylated neural cell adhesion molecule during postnatal myelination and following chemically induced demyelination of the adult mouse spinal cord. Eur J Neurosci 1995, 7:480-491.
28. Patrikios P., Stadelmann C., Kutzelnigg A., Rauschka H., Schmidbauer M., Laursen H., Sorensen P.S., Bruck W., Lucchinetti C., Lassmann H. Remyelination is extensive in a subset of multiple sclerosis patients. Brain 2006, 129:3165-3172.
29. Paxinos G., Franklin K. The mouse brain in stereotaxic coordinates 2001, Academic Press, New York, NY.
30. Rehbinder C., Baneux P., Forbes D., van Herck H., Nicklas W., Rugaya Z., Winkler G. FELASA recommendations for the health monitoring of mouse, rat, hamster, gerbil, guinea pig and rabbit experimental units. Report of the Federation of European Laboratory Animal Science Associations (FELASA) Working Group on Animal Health Accepted by the FELASA Board of Management, November 1995. Lab Anim 1996, 30:193-208.
31. Remington L.T., Babcock A.A., Zehntner S.P., Owens T. Microglial recruitment, activation, and proliferation in response to primary demyelination. Am J Pathol 2007, 170:1713-1724.
32. Rodriguez M. A function of myelin is to protect axons from subsequent injury: implications for deficits in multiple sclerosis. Brain 2003, 126:751-752.
33. Rutishauser U. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci 2008, 9:26-35.
34. Seki T., Arai Y. The persistent expression of a highly polysialylated NCAM in the dentate gyrus of the adult rat. Neurosci Res 1991, 12:503-513.
35. Seki T., Arai Y. Distribution and possible roles of the highly polysialylated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system. Neurosci Res 1993, 17:265-290.
36. Seki T. Hippocampal adult neurogenesis occurs in a microenvironment provided by PSA-NCAM-expressing immature neurons. J Neurosci Res 2002, 69:772-783.
37. Skripuletz T., Bussmann J.H., Gudi V., Koutsoudaki P.N., Pul R., Moharregh-Khiabani D., Lindner M., Stangel M. Cerebellar cortical demyelination in the murine cuprizone model. Brain Pathol 2010, 20:301-312.
38. Skripuletz T., Lindner M., Kotsiari A., Garde N., Fokuhl J., Linsmeier F., Trebst C., Stangel M. Cortical demyelination is prominent in the murine cuprizone model and is strain-dependent. Am J Pathol 2008, 172:1053-1061.
39. Stangel M. Neuroprotection and neuroregeneration in multiple sclerosis. J Neurol 2008, 255(Suppl 6):77-81.
40. Stangel M., Trebst C. Remyelination strategies: new advancements toward a regenerative treatment in multiple sclerosis. Curr Neurol Neurosci Rep 2006, 6:229-235.
41. Stummeyer K., Dickmanns A., Muhlenhoff M., Gerardy-Schahn R., Ficner R. Crystal structure of the polysialic acid-degrading endosialidase of bacteriophage K1F. Nat Struct Mol Biol 2005, 12:90-96.
42. Torkildsen O., Brunborg L.A., Myhr K.M., Bo L. The cuprizone model for demyelination. Acta Neurol Scand Suppl 2008, 188:72-76.
43. Trotter J., Bitter-Suermann D., Schachner M. Differentiation-regulated loss of the polysialylated embryonic form and expression of the different polypeptides of the neural cell adhesion molecule by cultured oligodendrocytes and myelin. J Neurosci Res 1989, 22:369-383.
44. Weinhold B., Seidenfaden R., Rockle I., Muhlenhoff M., Schertzinger F., Conzelmann S., Marth J.D., Gerardy-Schahn R., Hildebrandt H. Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J Biol Chem 2005, 280:42971-42977.