Experience-dependent development of perineuronal nets and chondroitin sulfate proteoglycan receptors in mouse visual cortex

Matrix Biology

Volumn 32, Issue 6, 2013, Pages 352-363

  Ye, Qian ^a,b   Miao, Qing long ^b  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b Chinese Academy of Sciences   (China)

Author keywords

Critical period plasticity; CSPG receptor; Mouse visual cortex; Parvalbumin interneuron; Perineuronal net

Indexed keywords

AGGLUTININ; AGGRECAN; CD45 ANTIGEN; HYALURONIC ACID; LECTIN; LINK PROTEIN; PARVALBUMIN; PHOSPHATASE; PROTEIN NOGO; PROTEOCHONDROITIN SULFATE; TENASCIN;

ANIMAL BEHAVIOR; ANIMAL TISSUE; ARTICLE; BIRTH; BRAIN CORTEX; CELL COUNT; CELL DENSITY; CENTRAL NERVOUS SYSTEM; EXPERIENCE; EXTRACELLULAR MATRIX; FLUORESCENCE; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PERINATAL PERIOD; PERINEURONAL NET; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REARING; STRIATE CORTEX;

ANIMALIA; MUS; WISTERIA FLORIBUNDA;

EID: 84882649975     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2013.04.001     Document Type: Article

References (58)

1. Ajmo J.M., Eakin A.K., Hamel M.G., Gottschall P.E. Discordant localization of WFA reactivity and brevican/ADAMTS-derived fragment in rodent brain. BMC Neurosci. 2008, 9:14.
2. Asher R.A., Morgenstern D.A., Fidler P.S., Adcock K.H., Oohira A., Braistead J.E., Levine J.M., Margolis R.U., Rogers J.H., Fawcett J.W. Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J. Neurosci. 2000, 20:2427-2438.
3. Beurdeley M., Spatazza J., Lee H.H., Sugiyama S., Bernard C., Di Nardo A.A., Hensch T.K., Prochiantz A. Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex. J. Neurosci. 2012, 32:9429-9437.
4. Bruckner G., Grosche J. Perineuronal nets show intrinsic patterns of extracellular matrix differentiation in organotypic slice cultures. Exp. Brain Res. 2001, 137:83-93.
5. Bruckner G., Brauer K., Hartig W., Wolff J.R., Rickmann M.J., Derouiche A., Delpech B., Girard N., Oertel W.H., Reichenbach A. Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain. Glia 1993, 8:183-200.
6. Bruckner G., Seeger G., Brauer K., Hartig W., Kacza J., Bigl V. Cortical areas are revealed by distribution patterns of proteoglycan components and parvalbumin in the Mongolian gerbil and rat. Brain Res. 1994, 658:67-86.
7. Bruckner G., Grosche J., Schmidt S., Hartig W., Margolis R.U., Delpech B., Seidenbecher C.I., Czaniera R., Schachner M. Postnatal development of perineuronal nets in wild-type mice and in a mutant deficient in tenascin-R. J. Comp. Neurol. 2000, 428:616-629.
8. Carulli D., Rhodes K.E., Brown D.J., Bonnert T.P., Pollack S.J., Oliver K., Strata P., Fawcett J.W. Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of their components. J. Comp. Neurol. 2006, 494:559-577.
9. Carulli D., Rhodes K.E., Fawcett J.W. Upregulation of aggrecan, link protein 1, and hyaluronan synthases during formation of perineuronal nets in the rat cerebellum. J. Comp. Neurol. 2007, 501:83-94.
10. Carulli D., Pizzorusso T., Kwok J.C., Putignano E., Poli A., Forostyak S., Andrews M.R., Deepa S.S., Glant T.T., Fawcett J.W. Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 2010, 133:2331-2347.
11. Celio M.R. Parvalbumin in Most Gamma-Aminobutyric-Acid Containing Neurons of the Rat Cerebral-Cortex. Science 1986, 231:995-997.
12. Celio M.R., Blumcke I. Perineuronal nets-a specialized form of extracellular matrix in the adult nervous system. Brain Res. Brain Res. Rev. 1994, 19:128-145.
13. Deepa S.S., Carulli D., Galtrey C., Rhodes K., Fukuda J., Mikami T., Sugahara K., Fawcett J.W. Composition of perineuronal net extracellular matrix in rat brain: a different disaccharide composition for the net-associated proteoglycans. J. Biol. Chem. 2006, 281:17789-17800.
14. del Rio J.A., de Lecea L., Ferrer I., Soriano E. The development of parvalbumin-immunoreactivity in the neocortex of the mouse. Brain Res. Dev. Brain Res. 1994, 81:247-259.
15. Dickendesher T.L., Baldwin K.T., Mironova Y.A., Koriyama Y., Raiker S.J., Askew K.L., Wood A., Geoffroy C.G., Zheng B., Liepmann C.D., Katagiri Y., Benowitz L.I., Geller H.M., Giger R.J. NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat. Neurosci. 2012, 15:703-712.
16. Espinosa J.S., Stryker M.P. Development and plasticity of the primary visual cortex. Neuron 2012, 75:230-249.
17. Fagiolini M., Fritschy J.M., Low K., Mohler H., Rudolph U., Hensch T.K. Specific GABAA circuits for visual cortical plasticity. Science 2004, 303:1681-1683.
18. Fisher D., Xing B., Dill J., Li H., Hoang H.H., Zhao Z., Yang X.L., Bachoo R., Cannon S., Longo F.M., Sheng M., Silver J., Li S. Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors. J. Neurosci. 2011, 31:14051-14066.
19. Fitch M.T., Silver J. Glial cell extracellular matrix: boundaries for axon growth in development and regeneration. Cell Tissue Res. 1997, 290:379-384.
20. Foscarin S., Ponchione D., Pajaj E., Leto K., Gawlak M., Wilczynski G.M., Rossi F., Carulli D. Experience-dependent plasticity and modulation of growth regulatory molecules at central synapses. PLoS One 2011, 6:e16666.
21. Galtrey C.M., Kwok J.C., Carulli D., Rhodes K.E., Fawcett J.W. Distribution and synthesis of extracellular matrix proteoglycans, hyaluronan, link proteins and tenascin-R in the rat spinal cord. Eur. J. Neurosci. 2008, 27:1373-1390.
22. Gonchar Y., Wang Q., Burkhalter A. Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front. Neuroanat. 2007, 1:3.
23. Gordon J.A., Stryker M.P. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J. Neurosci. 1996, 16:3274-3286.
24. Grumet M., Friedlander D.R., Sakurai T. Functions of brain chondroitin sulfate proteoglycans during developments: interactions with adhesion molecules. Perspect. Dev. Neurobiol. 1996, 3:319-330.
25. Guimaraes A., Zaremba S., Hockfield S. Molecular and morphological changes in the cat lateral geniculate nucleus and visual cortex induced by visual deprivation are revealed by monoclonal antibodies Cat-304 and Cat-301. J. Neurosci. 1990, 10:3014-3024.
26. Hagihara K., Miura R., Kosaki R., Berglund E., Ranscht B., Yamaguchi Y. Immunohistochemical evidence for the brevican-tenascin-R interaction: colocalization in perineuronal nets suggests a physiological role for the interaction in the adult rat brain. J. Comp. Neurol. 1999, 410:256-264.
27. Hartig W., Brauer K., Bruckner G. Wisteria floribunda agglutinin-labelled nets surround parvalbumin-containing neurons. Neuroreport 1992, 3:869-872.
28. Hartig W., Brauer K., Bigl V., Bruckner G. Chondroitin sulfate proteoglycan-immunoreactivity of lectin-labeled perineuronal nets around parvalbumin-containing neurons. Brain Res. 1994, 635:307-311.
29. Hensch T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 2005, 6:877-888.
30. Hockfield S., Kalb R.G., Zaremba S., Fryer H. Expression of neural proteoglycans correlates with the acquisition of mature neuronal properties in the mammalian brain. Cold Spring Harb. Symp. Quant. Biol. 1990, 55:505-514.
31. Huang Z.J., Kirkwood A., Pizzorusso T., Porciatti V., Morales B., Bear M.F., Maffei L., Tonegawa S. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 1999, 98:739-755.
32. Kind P.C., Beaver C.J., Mitchell D.E. Effects of early periods of monocular deprivation and reverse lid suture on the development of Cat-301 immunoreactivity in the dorsal lateral geniculate nucleus (dLGN) of the cat. J. Comp. Neurol. 1995, 359:523-536.
33. Kind P.C., Sengpiel F., Beaver C.J., Crocker-Buque A., Kelly G.M., Matthews R.T., Mitchell D.E. The development and activity-dependent expression of aggrecan in the cat visual cortex. Cereb. Cortex 2013, 23:349-360.
34. Klein R. Eph/ephrin signaling in morphogenesis, neural development and plasticity. Curr. Opin. Cell Biol. 2004, 16:580-589.
35. Koppe G., Bruckner G., Brauer K., Hartig W., Bigl V. Developmental patterns of proteoglycan-containing extracellular matrix in perineuronal nets and neuropil of the postnatal rat brain. Cell Tissue Res. 1997, 288:33-41.
36. Koppe G., Bruckner G., Hartig W., Delpech B., Bigl V. Characterization of proteoglycan-containing perineuronal nets by enzymatic treatments of rat brain sections. Histochem. J. 1997, 29:11-20.
37. Kosaka T., Heizmann C.W. Selective staining of a population of parvalbumin-containing GABAergic neurons in the rat cerebral cortex by lectins with specific affinity for terminal N-acetylgalactosamine. Brain Res. 1989, 483:158-163.
38. Kwok J.C., Carulli D., Fawcett J.W. In vitro modeling of perineuronal nets: hyaluronan synthase and link protein are necessary for their formation and integrity. J. Neurochem. 2010, 114:1447-1459.
39. Kwok J.C., Dick G., Wang D., Fawcett J.W. Extracellular matrix and perineuronal nets in CNS repair. Dev. Neurobiol. 2011, 71:1073-1089.
40. Lander C., Kind P., Maleski M., Hockfield S. A family of activity-dependent neuronal cell-surface chondroitin sulfate proteoglycans in cat visual cortex. J. Neurosci. 1997, 17:1928-1939.
41. Liu B.P., Cafferty W.B., Budel S.O., Strittmatter S.M. Extracellular regulators of axonal growth in the adult central nervous system. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2006, 361:1593-1610.
42. Matsui F., Nishizuka M., Yasuda Y., Aono S., Watanabe E., Oohira A. Occurrence of a N-terminal proteolytic fragment of neurocan, not a C-terminal half, in a perineuronal net in the adult rat cerebrum. Brain Res. 1998, 790:45-51.
43. Matthews R.T., Kelly G.M., Zerillo C.A., Gray G., Tiemeyer M., Hockfield S. Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J. Neurosci. 2002, 22:7536-7547.
44. McKeon R.J., Jurynec M.J., Buck C.R. The chondroitin sulfate proteoglycans neurocan and phosphacan are expressed by reactive astrocytes in the chronic CNS glial scar. J. Neurosci. 1999, 19:10778-10788.
45. McRae P.A., Rocco M.M., Kelly G., Brumberg J.C., Matthews R.T. Sensory deprivation alters aggrecan and perineuronal net expression in the mouse barrel cortex. J. Neurosci. 2007, 27:5405-5413.
46. Mukhopadhyay A., McGuire T., Peng C.Y., Kessler J.A. Differential effects of BMP signaling on parvalbumin and somatostatin interneuron differentiation. Development 2009, 136:2633-2642.
47. Niederost B.P., Zimmermann D.R., Schwab M.E., Bandtlow C.E. Bovine CNS myelin contains neurite growth-inhibitory activity associated with chondroitin sulfate proteoglycans. J. Neurosci. 1999, 19:8979-8989.
48. Oohira A., Matsui F., Katoh-Semba R. Inhibitory effects of brain chondroitin sulfate proteoglycans on neurite outgrowth from PC12D cells. J. Neurosci. 1991, 11:822-827.
49. Pizzorusso T., Medini P., Berardi N., Chierzi S., Fawcett J.W., Maffei L. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 2002, 298:1248-1251.
50. Pizzorusso T., Medini P., Landi S., Baldini S., Berardi N., Maffei L. Structural and functional recovery from early monocular deprivation in adult rats. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:8517-8522.
51. Ren J.Q., Aika Y., Heizmann C.W., Kosaka T. Quantitative analysis of neurons and glial cells in the rat somatosensory cortex, with special reference to GABAergic neurons and parvalbumin-containing neurons. Exp. Brain Res. 1992, 92:1-14.
52. Schweizer M., Streit W.J., Muller C.M. Postnatal development and localization of an N-acetylgalactosamine containing glycoconjugate associated with nonpyramidal neurons in cat visual cortex. J. Comp. Neurol. 1993, 329:313-327.
53. Shen Y., Tenney A.P., Busch S.A., Horn K.P., Cuascut F.X., Liu K., He Z., Silver J., Flanagan J.G. PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 2009, 326:592-596.
54. Snow D.M., Brown E.M., Letourneau P.C. Growth cone behavior in the presence of soluble chondroitin sulfate proteoglycan (CSPG), compared to behavior on CSPG bound to laminin or fibronectin. Int. J. Dev. Neurosci. 1996, 14:331-349.
55. Sugiyama S., Di Nardo A.A., Aizawa S., Matsuo I., Volovitch M., Prochiantz A., Hensch T.K. Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity. Cell 2008, 134:508-520.
56. Sur M., Frost D.O., Hockfield S. Expression of a surface-associated antigen on Y-cells in the cat lateral geniculate nucleus is regulated by visual experience. J. Neurosci. 1988, 8:874-882.
57. Wang D., Fawcett J. The perineuronal net and the control of CNS plasticity. Cell Tissue Res. 2012, 349:147-160.
58. Zaremba S., Guimaraes A., Kalb R.G., Hockfield S. Characterization of an activity-dependent, neuronal surface proteoglycan identified with monoclonal antibody Cat-301. Neuron 1989, 2:1207-1219.