Modulation of semaphorin3A in perineuronal nets during structural plasticity in the adult cerebellum

Molecular and Cellular Neuroscience

Volumn 57, Issue , 2013, Pages 10-22

  Carulli, Daniela ^a   Foscarin, Simona ^a   Faralli, Alessio ^a   Pajaj, Ermira ^a   Rossi, Ferdinando ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

Cartilage link protein 1; Cerebellum; Enriched environment; GAP 43; Perineuronal net; Plasticity

Indexed keywords

HYALURONIC ACID; LINK PROTEIN; NEUROMODULIN; PROTEOCHONDROITIN SULFATE; SEMAPHORIN 3A; TENASCIN; VESICULAR GLUTAMATE TRANSPORTER 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY LABELING; ARTICLE; BINDING AFFINITY; CEREBELLUM; CEREBELLUM NUCLEUS; CONTROLLED STUDY; ENZYMATIC DEGRADATION; EXTRACELLULAR MATRIX; GENE DELETION; INNERVATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PERINEURONAL NETS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PURKINJE CELL; SYNAPSE;

CARTILAGE LINK PROTEIN-1; CEREBELLUM; CHONDROITIN SULFATE PROTEOGLYCAN; CSPG; DCN; DEEP CEREBELLAR NUCLEI; ECM; ENRICHED ENVIRONMENT; EXTRACELLULAR MATRIX; GAP-43; PC; PERINEURONAL NET; PI; PLASTICITY; PNN; PROPIDIUM IODIDIE; PURKINJE CELL; SEMA3A; SEMAPHORIN3A; TG; TRANSGENIC; WFA; WILD-TYPE; WISTERIA FLORIBUNDA AGGLUTININ; WT;

ANIMALS; CEREBELLUM; EXTRACELLULAR MATRIX; MICE; PURKINJE CELLS; SEMAPHORIN-3A;

EID: 84884467537     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2013.08.003     Document Type: Article

References (65)

1. Armstrong D.M., Schild R.F. An investigation of the cerebellar cortico-nuclear projections in the rat using an autoradiographic tracing method. I. Projections from the vermis. Brain Res. 1978, 141:1-19.
2. Bagri A., Cheng H.J., Yaron A., Pleasure S.J., Tessier-Lavigne M. Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family. Cell 2003, 113:285-299.
3. Baroncelli L., Sale A., Viegi A., Maya Vetencourt J.F., De Pasquale R., Baldini S., Maffei L. Experience-dependent reactivation of ocular dominance plasticity in the adult visual cortex. Exp. Neurol. 2010, 226:100-109.
4. Behar O., Golden J.A., Mashimo H., Schoen F.J., Fishman M.C. Semaphorin III is needed for normal patterning and growth of nerves, bones and heart. Nature 1996, 383:525-528.
5. Bekku Y., Su W.D., Hirakawa S., Fassler R., Ohtsuka A., Kang J.S., Sanders J., Murakami T., Ninomiya Y., Oohashi T. Molecular cloning of Bral2, a novel brain-specific link protein, and immunohistochemical colocalization with brevican in perineuronal nets. Mol. Cell. Neurosci. 2003, 24:148-159.
6. Borges L.F., Elliott P.J., Gill R., Iversen S.D., Iversen L.L. Selective extraction of small and large molecules from the cerebrospinal fluid by Purkinje neurons. Science 1985, 228:346-348.
7. Bouchard M., Grote D., Craven S.E., Sun Q., Steinlein P., Busslinger M. Identification of Pax2-regulated genes by expression profiling of the mid-hindbrain organizer region. Development 2005, 132:2633-2643.
8. Bouzioukh F., Daoudal G., Falk J., Debanne D., Rougon G., Castellani V. Semaphorin3A regulates synaptic function of differentiated hippocampal neurons. Eur. J. Neurosci. 2006, 23:2247-2254.
9. Buffo A., Holtmaat A.J., Savio T., Verbeek J.S., Oberdick J., Oestreicher A.B., Gispen W.H., Verhaagen J., Rossi F., Strata P. Targeted overexpression of the neurite growth-associated protein B-50/GAP-43 in cerebellar Purkinje cells induces sprouting after axotomy but not axon regeneration into growth-permissive transplants. J. Neurosci. 1997, 17:8778-8791.
10. Carulli D., Laabs T., Geller H.M., Fawcett J.W. Chondroitin sulfate proteoglycans in neural development and regeneration. Curr. Opin. Neurobiol. 2005, 15:116-120.
11. 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.
12. 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.
13. 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.
14. Cioni J.M., Telley L., Saywell V., Cadilhac C., Jourdan C., Huber A.B., Huang J.Z., Jahannault-Talignani C., Ango F. SEMA3A signaling controls layer-specific interneuron branching in the cerebellum. Curr. Biol 2013, 10.1016/j.cub.2013.04.007.
15. Corvetti L., Rossi F. Degradation of chondroitin sulfate proteoglycans induces sprouting of intact Purkinje axons in the cerebellum of the adult rat. J. Neurosci. 2005, 25:7150-7158.
16. Czipri M., Otto J.M., Cs-Szabo G., Kamath R.V., Vermes C., Firneisz G., Kolman K.J., Watanabe H., Li Y., Roughley P.J., Yamada Y., Olsen B.R., Glant T.T. Genetic rescue of chondrodysplasia and the perinatal lethal effect of cartilage link protein deficiency. J. Biol. Chem. 2003, 278:39214-39223.
17. De Winter F., Oudega M., Lankhorst A.J., Hamers F.P., Blits B., Ruitenberg M.J., Pasterkamp R.J., Gispen W.H., Verhaagen J. Injury-induced class 3 semaphorin expression in the rat spinal cord. Exp. Neurol. 2002, 175:61-75.
18. De Wit J., De Winter F., Klooster J., Verhaagen J. Semaphorin 3A displays a punctate distribution on the surface of neuronal cells and interacts with proteoglycans in the extracellular matrix. Mol. Cell. Neurosci. 2005, 29:40-55.
19. De Zeeuw C.I., Berrebi A.S. Postsynaptic targets of Purkinje cell terminals in the cerebellar and vestibular nuclei of the rat. Eur. J. Neurosci. 1995, 7:2322-2333.
20. 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.
21. Denny J.B. Molecular mechanisms, biological actions, and neuropharmacology of the growth-associated protein GAP-43. Curr. Neuropharmacol. 2006, 4:293-304.
22. 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.
23. 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.
24. Foscarin S., Gianola S., Carulli D., Fazzari P., Mi S., Tamagnone L., Rossi F. Overexpression of GAP-43 modifies the distribution of the receptors for myelin-associated growth-inhibitory proteins in injured Purkinje axons. Eur. J. Neurosci. 2009, 30:1837-1848.
25. 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.
26. Fukuda T., Takeda S., Xu R., Ochi H., Sunamura S., Sato T., Shibata S., Yoshida Y., Gu Z., Kimura A., Ma C., Xu C., Bando W., Fujita K., Shinomiya K., Hirai T., Asou Y., Enomoto M., Okano H., Okawa A., Itoh H. Sema3A regulates bone-mass accrual through sensory innervations. Nature 2013, 10.1038/nature12115.
27. Geissler M., Gottschling C., Aguado A., Rauch U., Wetzel C.H., Hatt H., Faissner A. Primary hippocampal neurons, which lack four crucial extracellular matrix molecules, display abnormalities of synaptic structure and function and severe deficits in perineuronal net formation. J. Neurosci. 2013, 33:7742-7755.
28. Gianola S., Rossi F. GAP-43 overexpression in adult mouse Purkinje cells overrides myelin-derived inhibition of neurite growth. Eur. J. Neurosci. 2004, 19:819-830.
29. Gianola S., Savio T., Schwab M.E., Rossi F. Cell-autonomous mechanisms and myelin-associated factors contribute to the development of Purkinje axon intracortical plexus in the rat cerebellum. J. Neurosci. 2003, 23:4613-4624.
30. Giger R.J., Pasterkamp R.J., Heijnen S., Holtmaat A.J., Verhaagen J. Anatomical distribution of the chemorepellent semaphorin III/collapsin-1 in the adult rat and human brain: predominant expression in structures of the olfactory-hippocampal pathway and the motor system. J. Neurosci. Res. 1998, 52:27-42.
31. Gogolla N., Caroni P., Luthi A., Herry C. Perineuronal nets protect fear memories from erasure. Science 2009, 325:1258-1261.
32. Gutekunst C.A., Stewart E.N., Gross R.E. Immunohistochemical distribution of PlexinA4 in the adult rat central nervous system. Front. Neuroanat. 2010, 4. 10.3389/fnana.2010.00025.
33. Harauzov A., Spolidoro M., DiCristo G., De Pasquale R., Cancedda L., Pizzorusso T., Viegi A., Berardi N., Maffei L. Reducing intracortical inhibition in the adult visual cortex promotes ocular dominance plasticity. J. Neurosci. 2010, 30:361-371.
34. Hartig W., Bruckner G., Brauer K., Schmidt C., Bigl V. Allocation of perineuronal nets and parvalbumin-, calbindin-D28k- and glutamic acid decarboxylase-immunoreactivity in the amygdala of the rhesus monkey. Brain Res. 1995, 698:265-269.
35. Hedstrom K.L., Xu X., Ogawa Y., Frischknecht R., Seidenbecher C.I., Shrager P., Rasband M.N. Neurofascin assembles a specialized extracellular matrix at the axon initial segment. J. Cell Biol. 2007, 178:875-886.
36. Hensch T.K., Fagiolini M. Excitatory-inhibitory balance and critical period plasticity in developing visual cortex. Prog. Brain Res. 2005, 147:115-124.
37. Hoebeek F.E., Khosrovani S., Witter L., De Zeeuw C.I. Purkinje cell input to cerebellar nuclei in tottering: ultrastructure and physiology. Cerebellum 2008, 7:547-558.
38. Holtmaat A.J., Gorter J.A., De Wit J., Tolner E.A., Spijker S., Giger R.J., Lopes da Silva F.H., Verhaagen J. Transient downregulation of Sema3A mRNA in a rat model for temporal lobe epilepsy. A novel molecular event potentially contributing to mossy fiber sprouting. Exp. Neurol. 2003, 182:142-150.
39. Hou S.T., Keklikian A., Slinn J., O'Hare M., Jiang S.X., Aylsworth A. Sustained up-regulation of semaphorin 3A, Neuropilin1, and doublecortin expression in ischemic mouse brain during long-term recovery. Biochem. Biophys. Res. Commun. 2008, 367:109-115.
40. Kaneko S., Iwanami A., Nakamura M., Kishino A., Kikuchi K., Shibata S., Okano H.J., Ikegami T., Moriya A., Konishi O., Nakayama C., Kumagai K., Kimura T., Sato Y., Goshima Y., Taniguchi M., Ito M., He Z., Toyama Y., Okano H. A selective Sema3A inhibitor enhances regenerative responses and functional recovery of the injured spinal cord. Nat. Med. 2006, 12:1380-1389.
41. Kantor D.B., Chivatakarn O., Peer K.L., Oster S.F., Inatani M., Hansen M.J., Flanagan J.G., Yamaguchi Y., Sretavan D.W., Giger R.J., Kolodkin A.L. Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 2004, 44:961-975.
42. Kwok J.C., Dick G., Wang D., Fawcett J.W. Extracellular matrix and perineuronal nets in CNS repair. Dev. Neurobiol. 2011, 71:1073-1089.
43. McRae P.A., Baranov E., Rogers S.L., Porter B.E. Persistent decrease in multiple components of the perineuronal net following status epilepticus. Eur. J. Neurosci. 2012, 36:3471-3482.
44. Moret F., Renaudot C., Bozon M., Castellani V. Semaphorin and neuropilin co-expression in motoneurons sets axon sensitivity to environmental semaphorin sources during motor axon pathfinding. Development 2007, 134:4491-4501.
45. Pasterkamp R.J., Giger R.J., Ruitenberg M.J., Holtmaat A.J., De Wit J., De Winter F., Verhaagen J. Expression of the gene encoding the chemorepellent semaphorin III is induced in the fibroblast component of neural scar tissue formed following injuries of adult but not neonatal CNS. Mol. Cell. Neurosci. 1999, 13:143-166.
46. Pekcec A., Yigitkanli K., Jung J.E., Pallast S., Xing C., Antipenko A., Minchenko M., Nikolov D.B., Holman T.R., Lo E.H., van Leyen K. Following experimental stroke, the recovering brain is vulnerable to lipoxygenase-dependent semaphorin signaling. FASEB J. 2013, 27:437-445.
47. 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.
48. Rabacchi S.A., Solowska J.M., Kruk B., Luo Y., Raper J.A., Baird D.H. Collapsin-1/semaphorin-III/D is regulated developmentally in Purkinje cells and collapses pontocerebellar mossy fiber neuronal growth cones. J. Neurosci. 1999, 19:4437-4448.
49. Ramon y Cajal S. Histologie du systeme nerveux de l'homme et des vertebres 1911, 2. Maloine, Paris.
50. 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. Depletion of perineuronal nets enhances recognition memory and long-term depression in the perirhinal cortex. J. Neurosci. 2013, 33:7057-7065.
51. Rossi F., Cantino D., Strata P. Morphology of Purkinje cell axon terminals in intracerebellar nuclei following inferior olive lesion. Neuroscience 1987, 22:99-112.
52. Rossi F., Borsello T., Vaudano E., Strata P. Regressive modifications of climbing fibres following Purkinje cell degeneration in the cerebellar cortex of the adult rat. Neuroscience 1993, 53:759-778.
53. Rossi F., Borsello T., Strata P. Exposure to kainic acid mimics the effects of axotomy in cerebellar Purkinje cells of the adult rat. Eur. J. Neurosci. 1994, 6:392-402.
54. Rossi F., Jankovski A., Sotelo C. Target neuron controls the integrity of afferent axon phenotype: a study on the Purkinje cell-climbing fiber system in cerebellar mutant mice. J. Neurosci. 1995, 15:2040-2056.
55. Rossi F., Corvetti L., Gianola S. The strange case of Purkinje axon regeneration and plasticity. Cerebellum 2006, 5:163-173.
56. Sahay A., Kim C.H., Sepkuty J.P., Cho E., Huganir R.L., Ginty D.D., Kolodkin A.L. Secreted semaphorins modulate synaptic transmission in the adult hippocampus. J. Neurosci. 2005, 25:3613-3620.
57. Sale A., Maya Vetencourt J.F., Medini P., Cenni M.C., Baroncelli L., De Pasquale R., Maffei L. Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition. Nat. Neurosci. 2007, 10:679-681.
58. Schwarting G.A., Kostek C., Ahmad N., Dibble C., Pays L., Puschel A.W. Semaphorin 3A is required for guidance of olfactory axons in mice. J. Neurosci. 2000, 20:7691-7697.
59. Sharma A., Pollett M.A., Plant G.W., Harvey A.R. Changes in mRNA expression of class 3 semaphorins and their receptors in the adult rat retino-collicular system after unilateral optic nerve injury. Invest. Ophthalmol. Vis. Sci. 2012, 53:8367-8377.
60. 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.
61. Taniguchi M., Yuasa S., Fujisawa H., Naruse I., Saga S., Mishina M., Yagi T. Disruption of semaphorin III/D gene causes severe abnormality in peripheral nerve projection. Neuron 1997, 19:519-530.
62. Taniguchi M., Nagao H., Takahashi Y.K., Yamaguchi M., Mitsui S., Yagi T., Mori K., Shimizu T. Distorted odor maps in the olfactory bulb of semaphorin 3A-deficient mice. J. Neurosci. 2003, 23:1390-1397.
63. Vo T., Carulli D., Ehlert E.M.E., Kwok J.C.F., Dick G., Mecollari V., Moloney E.B., Neufeld G., de Winter F., Fawcett J.W., Verhaagen J. The chemorepulsive axon guidance protein Semaphorin 3A is a constituent of perineuronal nets in the adult rodent brain. Mol. Cell Neurosci. 2013, 56:186-200.
64. Wassef M., Simons J., Tappaz M.L., Sotelo C. Non-Purkinje cell GABAergic innervation of the deep cerebellar nuclei: a quantitative immunocytochemical study in C57BL and in Purkinje cell degeneration mutant mice. Brain Res. 1986, 399:125-135.
65. Zhou D., Lambert S., Malen P.L., Carpenter S., Boland L.M., Bennett V. AnkyrinG is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J. Cell Biol. 1998, 143:1295-1304.