Perineuronal nets affect parvalbumin expression in GABAergic neurons of the mouse hippocampus

European Journal of Neuroscience

Volumn 41, Issue 3, 2015, Pages 368-378

  Yamada, J ^a   Ohgomori, T ^a   Jinno, S ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Chondroitinase ABC; Neural plasticity; Vulnerability; Wisteria floribunda agglutinin

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; AGGLUTININ; CALCIUM BINDING PROTEIN; CHONDROITIN ABC LYASE; LECTIN; PARVALBUMIN; MESSENGER RNA; N ACETYLGLUCOSAMINE RECEPTOR; PLANT LECTIN; WISTERIA LECTIN;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CONNECTOME; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GABAERGIC SYSTEM; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN MOTIF; WISTERIA; YOUNG ADULT; ANIMAL; C57BL MOUSE; DRUG EFFECTS; FLUORESCENCE IMAGING; METABOLISM; MICROPHOTOGRAPHY; PROTEIN DEGRADATION; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; CHONDROITIN ABC LYASE; EXTRACELLULAR MATRIX; GABAERGIC NEURONS; HIPPOCAMPUS; MALE; MICE, INBRED C57BL; OPTICAL IMAGING; PARVALBUMINS; PHOTOMICROGRAPHY; PLANT LECTINS; PROTEOLYSIS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, N-ACETYLGLUCOSAMINE; RNA, MESSENGER;

EID: 84922722204     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12792     Document Type: Article

References (46)

1. Bandtlow, C.E. & Zimmermann, D.R. (2000) Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol. Rev., 80, 1267-1290.
2. Best, N., Mitchell, J., Baimbridge, K.G. & Wheal, H.V. (1993) Changes in parvalbumin-immunoreactive neurons in the rat hippocampus following a kainic acid lesion. Neurosci. Lett., 155, 1-6.
3. Beurdeley, M., Spatazza, J., Lee, H.H., Sugiyama, S., Bernard, C., Di Nardo, A.A., Hensch, T.K. & Prochiantz, A. (2012) Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex. J. Neurosci., 32, 9429-9437.
4. Brückner, G., Hausen, D., Härtig, W., Drlicek, M., Arendt, T. & Brauer, K. (1999) Cortical areas abundant in extracellular matrix chondroitin sulphate proteoglycans are less affected by cytoskeletal changes in Alzheimer's disease. Neuroscience, 92, 791-805.
5. Cabungcal, J.H., Steullet, P., Morishita, H., Kraftsik, R., Cuenod, M., Hensch, T.K. & Do, K.Q. (2013) Perineuronal nets protect fast-spiking interneurons against oxidative stress. Proc. Natl. Acad. Sci. USA, 110, 9130-9135.
6. 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. (2010) Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain, 133, 2331-2347.
7. Celio, M.R. (1986) Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science, 231, 995-997.
8. Celio, M.R. (1993) Perineuronal nets of extracellular matrix around parvalbumin-containing neurons of the hippocampus. Hippocampus, 3, 55-60.
9. Chevaleyre, V. & Piskorowski, R. (2014) Modulating excitation through plasticity at inhibitory synapses. Front. Cell Neurosci., 8, 93.
10. Cossart, R., Dinocourt, C., Hirsch, J.C., Merchan-Perez, A., De Felipe, J., Ben-Ari, Y., Esclapez, M. & Bernard, C. (2001) Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat. Neurosci., 4, 52-62.
11. Del Río, M.R. & DeFelipe, J. (1994) A study of SMI 32-stained pyramidal cells, parvalbumin-immunoreactive chandelier cells, and presumptive thalamocortical axons in the human temporal neocortex. J. Comp. Neurol., 342, 389-408.
12. Dinocourt, C., Petanjek, Z., Freund, T.F., Ben-Ari, Y. & Esclapez, M. (2003) Loss of interneurons innervating pyramidal cell dendrites and axon initial segments in the CA1 region of the hippocampus following pilocarpine-induced seizures. J. Comp. Neurol., 459, 407-425.
13. Dityatev, A., Brückner, G., Dityateva, G., Grosche, J., Kleene, R. & Schachner, M. (2007) Activity-dependent formation and functions of chondroitin sulfate-rich extracellular matrix of perineuronal nets. Dev. Neurobiol., 67, 570-588.
14. Donato, F., Rompani, S.B. & Caroni, P. (2013) Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning. Nature, 504, 272-276.
15. Franklin, G. & Paxinos, K.B.J. (1997) The Mouse Brain in Stereotaxic Coordinates. Academic Press, London.
16. Giamanco, K.A. & Matthews, R.T. (2012) Deconstructing the perineuronal net: cellular contributions and molecular composition of the neuronal extracellular matrix. Neuroscience, 218, 367-384.
17. Guirado, R., Perez-Rando, M., Sanchez-Matarredona, D., Castrén, E. & Nacher, J. (2014) Chronic fluoxetine treatment alters the structure, connectivity and plasticity of cortical interneurons. Int. J. Neuropsychop., 30, 1-12.
18. Gundersen, H.J.G. (1977) Notes on the estimation of the numerical density of arbitrary profiles: the edge effect. J. Microsc., 111, 219-223.
19. Hensch, T.K., Fagiolini, M., Mataga, N., Stryker, M.P., Baekkeskov, S. & Kash, S.F. (1998) Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science, 282, 1504-1508.
20. Huang, Z.J., Kirkwood, A., Pizzorusso, T., Porciatti, V., Morales, B., Bear, M.F., Maffei, L. & Tonegawa, S. (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell, 98, 739-755.
21. Hylin, M.J., Orsi, S.A., Moore, A.N. & Dash, P.K. (2013) Disruption of the perineuronal net in the hippocampus or medial prefrontal cortex impairs fear conditioning. Learn. Memory, 20, 267-273.
22. Jinno, S. & Kosaka, T. (2000) Colocalization of parvalbumin and somatostatin-like immunoreactivity in the mouse hippocampus: quantitative analysis with optical dissector. J. Comp. Neurol., 428, 377-388.
23. Jinno, S. & Kosaka, T. (2002) Patterns of expression of calcium binding proteins and neuronal nitric oxide synthase in different populations of hippocampal GABAergic neurons in mice. J. Comp. Neurol., 449, 1-25.
24. Jinno, S., Aika, Y., Fukuda, T. & Kosaka, T. (1998) Quantitative analysis of GABAergic neurons in the mouse hippocampus, with optical disector using confocal laser scanning microscope. Brain Res., 814, 55-70.
25. Karetko, M. & Skangiel-Kramska, J. (2009) Diverse functions of perineuronal nets. Acta Neurobiol. Exp., 69, 564-577.
26. Kosaka, T. & Heizmann, C.W. (1989) 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., 483, 158-163.
27. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res., 419, 119-130.
28. Makara, J.K., Katona, I., Nyiri, G., Nemeth, B., Ledent, C., Watanabe, M., de Vente, J., Freund, T.F. & Hajos, N. (2007) Involvement of nitric oxide in depolarization-induced suppression of inhibition in hippocampal pyramidal cells during activation of cholinergic receptors. J. Neurosci., 27, 10211-10222.
29. Mayhew, T.M. & Gundersen, H.J. (1996) If you assume, you can make an ass out of u and me: a decade of the disector for stereological counting of particles in 3D space. J. Anat., 188, 1-15.
30. McRae, P.A., Rocco, M.M., Kelly, G., Brumberg, J.C. & Matthews, R.T. (2007) Sensory deprivation alters aggrecan and perineuronal net expression in the mouse barrel cortex. J. Neurosci., 27, 5405-5413.
31. Morawski, M., Brückner, M.K., Riederer, P., Brückner, G. & Arendt, T. (2004) Perineuronal nets potentially protect against oxidative stress. Exp. Neurol., 188, 309-315.
32. Nowicka, D., Soulsby, S., Skangiel-Kramska, J. & Glazewski, S. (2009) Parvalbumin-containing neurons, perineuronal nets and experience-dependent plasticity in murine barrel cortex. Eur. J. Neurosci., 30, 2053-2063.
33. Ohira, K., Takeuchi, R., Iwanaga, T. & Miyakawa, T. (2013) Chronic fluoxetine treatment reduces parvalbumin expression and perineuronal nets in gamma-aminobutyric acidergic interneurons of the frontal cortex in adult mice. Mol. Brain, 6, 43.
34. Okamoto, M., Mori, S., Ichimura, M. & Endo, H. (1994) Chondroitin sulfate proteoglycans protect cultured rat's cortical and hippocampal neurons from delayed cell death induced by excitatory amino acids. Neurosci. Lett., 172, 51-54.
35. Orduz, D., Bischop, D.P., Schwaller, B., Schiffmann, S.N. & Gall, D. (2013) Parvalbumin tunes spike-timing and efferent short-term plasticity in striatal fast spiking interneurons. J. Physiol., 59, 3215-3232.
36. Piskorowski, R.A. & Chevaleyre, V. (2013) Delta-opioid receptors mediate unique plasticity onto parvalbumin-expressing interneurons in area CA2 of the hippocampus. J. Neurosci., 33, 14567-14578.
37. Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J.W. & Maffei, L. (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science, 298, 1248-1251.
38. Romberg, C., Yang, S., Melani, R., Andrews, M.R., Horner, A.E., Spillantini, M.G., Bussey, T.J., Fawcett, J.W., Pizzorusso, T. & Saksida, L.M. (2013) Depletion of perineuronal nets enhances recognition memory and long-term depression in the perirhinal cortex. J. Neurosci., 33, 7057-7065.
39. Schüppel, K., Brauer, K., Härtig, W., Grosche, J., Earley, B., Leonard, B.E. & Brückner, G. (2002) Perineuronal nets of extracellular matrix around hippocampal interneurons resist destruction by activated microglia in trimethyltin-treated rats. Brain Res., 958, 448-453.
40. Shah, A. & Lodge, D.J. (2013) A loss of hippocampal perineuronal nets produces deficits in dopamine system function: relevance to the positive symptoms of schizophrenia. Transl. Psychiatry, 3, e215.
41. Sterio, D.C. (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J. Microsc., 134, 127-136.
42. Stichel, C.C., Singer, W., Heizmann, C.W. & Norman, A.W. (1987) Immunohistochemical localization of calcium-binding proteins, parvalbumin and calbindin-D 28k, in the adult and developing visual cortex of cats: a light and electron microscopic study. J. Comp. Neurol., 262, 563-577.
43. Sugiyama, S., Di Nardo, A.A., Aizawa, S., Matsuo, I., Volovitch, M., Prochiantz, A. & Hensch, T.K. (2008) Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity. Cell, 134, 508-520.
44. Suttkus, A., Rohn, S., Weigel, S., Glöckner, P., Arendt, T. & Morawski, M. (2014) Aggrecan, link protein and tenascin-R are essential components of the perineuronal net to protect neurons against iron-induced oxidative stress. Cell Death Dis., 5, e1119.
45. Wang, D. & Fawcett, J. (2012) The perineuronal net and the control of CNS plasticity. Cell Tissue Res., 349, 147-160.
46. Yamada, J. & Jinno, S. (2013) Spatio-temporal differences in perineuronal net expression in the mouse hippocampus, with reference to parvalbumin. Neuroscience, 253, 368-379.