Persistent cortical plasticity by upregulation of chondroitin 6-sulfation

Nature Neuroscience

Volumn 15, Issue 3, 2012, Pages 414-422

  Miyata, Shinji ^a,b   Komatsu, Yukio ^c   Yoshimura, Yumiko ^d   Taya, Choji ^e   Kitagawa, Hiroshi ^a,b  

^a KOBE PHARMACEUTICAL UNIVERSITY   (Japan)

^b KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^e TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN 4 SULFATE; CHONDROITIN 6 SULFATE; PARVALBUMIN; PROTEOCHONDROITIN SULFATE; TRANSCRIPTION FACTOR OTX2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; EXTRACELLULAR MATRIX; FEMALE; GENE OVEREXPRESSION; INTERNEURON; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SULFATION; UPREGULATION; VISUAL CORTEX;

ACTION POTENTIALS; AGE FACTORS; AGGRECANS; AMPHETAMINES; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BACTERIAL PROTEINS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CHONDROITIN SULFATE PROTEOGLYCANS; CHONDROITIN SULFATES; ELECTROPORATION; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; LUMINESCENT PROTEINS; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; OTX TRANSCRIPTION FACTORS; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; PLANT LECTINS; RECEPTORS, N-ACETYLGLUCOSAMINE; SENSORY DEPRIVATION; SULFOTRANSFERASES; TIME FACTORS; UP-REGULATION; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 84857641919     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3023     Document Type: Article

References (49)

1. Wiesel, T. N. & Hubel, D. H. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26, 1003-1017 (1963).
2. Hensch, T. K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6, 877-888 (2005).
3. Gordon, J. A. & Stryker, M. P. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J. Neurosci. 16, 3274-3286 (1996).
4. Yazaki-Sugiyama, Y., Kang, S., Câteau, H., Fukai, T. & Hensch, T. K. Bidirectional plasticity in fast-spiking GABA circuits by visual experience. Nature 462, 218-221 (2009).
5. Sugiyama, S. et al. Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity. Cell 134, 508-520 (2008).
6. Sugahara, K. & Mikami, T. Chondroitin/dermatan sulfate in the central nervous system. Curr. Opin. Struct. Biol. 17, 536-545 (2007).
7. Celio, M. R., Spreafico, R., De Biasi, S. & Vitellaro-Zuccarello, L. Perineuronal nets: past and present. Trends Neurosci. 21, 510-515 (1998).
8. Galtrey, C. M. & Fawcett, J. W. The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res. Rev. 54, 1-18 (2007).
9. Carulli, D. et al. Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of their components. J. Comp. Neurol. 494, 559-577 (2006).
10. Pizzorusso, T. et al. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248-1251 (2002).
11. Bradbury, E. J. et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636-640 (2002).
12. Gama, C. I. et al. Sulfation patterns of glycosaminoglycans encode molecular recognition and activity. Nat. Chem. Biol. 2, 467-473 (2006).
13. Mikami, T., Yasunaga, D. & Kitagawa, H. Contactin-1 is a functional receptor for neuroregulatory chondroitin sulfate-E. J. Biol. Chem. 284, 4494-4499 (2009).
14. Nadanaka, S., Ishida, M., Ikegami, M. & Kitagawa, H. Chondroitin 4-O-sulfotransferase-1 modulates Wnt-3a signaling through control of E disaccharide expression of chondroitin sulfate. J. Biol. Chem. 283, 27333-27343 (2008).
15. Kitagawa, H., Tsutsumi, K., Tone, Y. & Sugahara, K. Developmental regulation of the sulfation profile of chondroitin sulfate chains in the chicken embryo brain. J. Biol. Chem. 272, 31377-31381 (1997).
16. Properzi, F. et al. Chondroitin 6-sulphate synthesis is up-regulated in injured CNS, induced by injury-related cytokines and enhanced in axon-growth inhibitory glia. Eur. J. Neurosci. 21, 378-390 (2005).
17. Fox, K. & Wong, R. O. A comparison of experience-dependent plasticity in the visual and somatosensory systems. Neuron 48, 465-477 (2005).
18. Maeda, N. et al. Heterogeneity of the chondroitin sulfate portion of phosphacan/6B4 proteoglycan regulates its binding affinity for pleiotrophin/heparin binding growth associated molecule. J. Biol. Chem. 278, 35805-35811 (2003).
19. Frenkel, M. Y. & Bear, M. F. How monocular deprivation shifts ocular dominance in visual cortex of young mice. Neuron 44, 917-923 (2004).
20. Godement, P., Salaün, J. & Imbert, M. Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse. J. Comp. Neurol. 230, 552-575 (1984).
21. Sato, M. & Stryker, M. P. Distinctive features of adult ocular dominance plasticity. J. Neurosci. 28, 10278-10286 (2008).
22. Härtig, W., Brauer, K. & Brückner, G. Wisteria foribunda agglutinin-labeled nets surround parvalbumin-containing neurons. Neuroreport 3, 869-872 (1992).
23. Matthews, R. T. et al. Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J. Neurosci. 22, 7536-7547 (2002).
24. Erisir, A. & Dreusicke, M. Quantitative morphology and postsynaptic targets of thalamocortical axons in critical period and adult ferret visual cortex. J. Comp. Neurol. 485, 11-31 (2005).
25. Marín, O. & Rubenstein, J. L. A long, remarkable journey: tangential migration in the telencephalon. Nat. Rev. Neurosci. 2, 780-790 (2001).
26. Tanaka, D. H. et al. Random walk behavior of migrating cortical interneurons in the marginal zone: time-lapse analysis in flat-mount cortex. J. Neurosci. 29, 1300-1311 (2009).
27. Borrell, V., Yoshimura, Y. & Callaway, E. M. Targeted gene delivery to telencephalic inhibitory neurons by directional in utero electroporation. J. Neurosci. Methods 143, 151-158 (2005).
28. Kawaguchi, Y. & Kondo, S. Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. J. Neurocytol. 31, 277-287 (2002).
29. Connors, B. W. & Gutnick, M. J. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 13, 99-104 (1990).
30. Kawaguchi, Y. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J. Neurosci. 15, 2638-2655 (1995).
31. Goldberg, E. M. et al. Rapid developmental maturation of neocortical FS cell intrinsic excitability. Cereb. Cortex 21, 666-682 (2011).
32. Hensch, T. K. et al. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282, 1504-1508 (1998).
33. Bavelier, D., Levi, D. M., Li, R. W., Dan, Y. & Hensch, T. K. Removing brakes on adult brain plasticity: from molecular to behavioral interventions. J. Neurosci. 30, 14964-14971 (2010).
34. Morishita, H., Miwa, J. M., Heintz, N. & Hensch, T. K. Lynxl, a cholinergic brake, limits plasticity in adult visual cortex. Science 330, 1238-1240 (2010).
35. McGee, A. W., Yang, Y., Fischer, Q. S., Daw, N. W. & Strittmatter, S. M. Experiencedriven plasticity of visual cortex limited by myelin and Nogo receptor. Science 309, 2222-2226 (2005).
36. Harauzov, A. et al. Reducing intracortical inhibition in the adult visual cortex promotes ocular dominance plasticity. J. Neurosci. 30, 361-371 (2010).
37. Jiang, B., Huang, Z. J., Morales, B. & Kirkwood, A. Maturation of GABAergic transmission and the timing of plasticity in visual cortex. Brain Res. Brain Res. Rev. 50, 126-133 (2005).
38. Schwaller, B. et al. Parvalbumin deficiency affects network properties resulting in increased susceptibility to epileptic seizures. Mol. Cell. Neurosci. 25, 650-663 (2004).
39. Rudy, B. & McBain, C. J. Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing. Trends Neurosci. 24, 517-526 (2001).
40. Carulli, D. et al. Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 133, 2331-2347 (2010).
41. Tropea, D. et al. Gene expression changes and molecular pathways mediating activity-dependent plasticity in visual cortex. Nat. Neurosci. 9, 660-668 (2006).
42. Miyata, S., Nishimura, Y., Hayashi, N. & Oohira, A. Construction of perineuronal net-like structure by cortical neurons in culture. Neuroscience 136, 95-104 (2005).
43. Lander, C., Zhang, H. & Hockfield, S. Neurons produce a neuronal cell surface-associated chondroitin sulfate proteoglycan. J. Neurosci. 18, 174-183 (1998).
44. Chang, M. C. et al. Narp regulates homeostatic scaling of excitatory synapses on parvalbumin-expressing interneurons. Nat. Neurosci. 13, 1090-1097 (2010).
45. Lewis, D. A., Hashimoto, T. & Volk, D. W. Cortical inhibitory neurons and schizophrenia. Nat. Rev. Neurosci. 6, 312-324 (2005).
46. Pantazopoulos, H., Woo, T. U., Lim, M. P., Lange, N. & Berretta, S. Extracellular matrix-glial abnormalities in the amygdala and entorhinal cortex of subjects diagnosed with schizophrenia. Arch. Gen. Psychiatry 67, 155-166 (2010).
47. Niwa, H., Yamamura, K. & Miyazaki, J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199 (1991).
48. Kitagawa, H., Kinoshita, A. & Sugahara, K. Microanalysis of glycosaminoglycanderived disaccharides labeled with the fluorophore 2-aminoacridone by capillary electrophoresis and high-performance liquid chromatography. Anal. Biochem. 232, 114-121 (1995).
49. 2+ channels in the potentiation of synaptic and visual responses during the critical period in rat visual cortex. Eur. J. Neurosci. 28, 730-743 (2008).