The polysialylated form of the neural cell adhesion molecule (PSA-NCAM) is expressed in a subpopulation of mature cortical interneurons characterized by reduced structural features and connectivity

Cerebral Cortex

Volumn 21, Issue 5, 2011, Pages 1028-1041

  Gómez Climent, María Ángeles ^a   Guirado, Ramón ^a   Castillo Gómez, Esther ^a   Varea, Emilio ^a   Gutierrez Mecinas, María ^a,d   Gilabert Juan, Javier ^a,b   García Mompó, Clara ^a   Vidueira, Sandra ^a   Sanchez Mataredona, David ^a   Hernández, Samuel ^a   Blasco Ibáñez, José Miguel ^a   Crespo, Carlos ^a   Rutishauser, Urs ^b   Schachner, Melitta ^c   Nacher, Juan ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

dendrite remodeling; dendritic arborization; interneuron subtypes; NCAM; neuronal structural plasticity; spine remodeling

Indexed keywords

NERVE CELL ADHESION MOLECULE; POLYSIALYLATED NERVE CELL ADHESION MOLECULE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL DENSITY; DENDRITIC SPINE; EMBRYO; INTERNEURON; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; CELL DIFFERENTIATION; CELL SHAPE; CEREBRAL CORTEX; INTERNEURONS; MALE; NEURAL CELL ADHESION MOLECULE L1; NEURAL INHIBITION; NEURAL PATHWAYS; NEUROGENESIS; NEURONAL PLASTICITY; RATS; RATS, SPRAGUE-DAWLEY; SIALIC ACIDS;

EID: 79954603170     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhq177     Document Type: Article

References (60)

1. Abrous DN, Montaron MF, Petry KG, Rougon G, Darnaudery M, Le Moal M, Mayo W. 1997. Decrease in highly polysialylated neuronal cell adhesion molecules and in spatial learning during ageing are not correlated. Brain Res. 744:285-292. (Pubitemid 27032345)
2. Arellano JI, DeFelipe J, Munoz A. 2002. PSA-NCAM immunoreactivity in chandelier cell axon terminals of the human temporal cortex. Cereb Cortex. 12:617-624. (Pubitemid 34533652)
3. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsaki G, Cauli B, Defelipe J, Fairen A, et al. 2008. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci. 9:557-568. (Pubitemid 351873463)
4. Babb TL, Pretorius JK, Kupfer WR, Brown WJ. 1988. Distribution of glutamate-decarboxylase-immunoreactive neurons and synapses in the rat and monkey hippocampus: light and electron microscopy. J Comp Neurol. 278:121-138. (Pubitemid 19012357)
5. Barbeau D, Liang JJ, Robitalille Y, Quirion R, Srivastava LK. 1995. Decreased expression of the embryonic form of the neural cell adhesion molecule in schizophrenic brains. Proc Natl Acad Sci USA. 92:2785-2789.
6. Bonfanti L. 2006. PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog Neurobiol. 80:129-164. (Pubitemid 44739166)
7. Bonfanti L, Olive S, Poulain DA, Theodosis DT. 1992. Mapping of the distribution of polysialylated neural cell adhesion molecule throughout the central nervous system of the adult rat: an immunohistochemical study. Neuroscience. 49:419-436.
8. Bukalo O, Fentrop N, Lee AY, Salmen B, Law JW, Wotjak CT, Schweizer M, Dityatev A, Schachner M. 2004. Conditional ablation of the neural cell adhesion molecule reduces precision of spatial learning, long-term potentiation, and depression in the CA1 subfield of mouse hippocampus.J Neurosci. 24:1565-1577. (Pubitemid 38240951)
9. Cameron HA, Dayer AG. 2008. New interneurons in the adult neocortex: small, sparse, but significant? Biol Psychiatry. 63: 650-655.
10. Castillo-Gomez E, Gomez-Climent MA Varea E, Guirado R, Blasco-Ibanez JM, Crespo C, Martinez-Guijarro FJ, Nacher J. 2008. Dopamine acting through D2 receptors modulates the expression of PSA-NCAM, a molecule related to neuronal structural plasticity, in the medial prefrontal cortex of adult rats. Exp Neurol. 214(1):97-111.
11. Close BE, Colley KJ. 1998. In vivo autopolysialylation and localization of the polysialyltransferases PST and STX. J Biol Chem. 273: 34586-34593. (Pubitemid 29008942)
12. Cordero MI, Rodriguez JJ, Davies HA, Peddie CJ, Sandi C, Stewart MG. 2005. Chronic restraint stress down-regulates amygdaloid expres-sion of polysialylated neural cell adhesion molecule. Neuroscience. 133:903-910. (Pubitemid 40814598)
13. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Kraemer P, Scheff S. 1994. Inactivation ofthe N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature. 367:455-459. (Pubitemid 24046046)
14. Curreli S, Arany Z, Gerardy-Schahn R, Mann D, Stamatos NM. 2007. Polysialylated neuropilin-2 is expressed on the surface of human dendritic cells and modulates dendritic cell-T lymphocyte inter-actions. J Biol Chem. 282:30346-30356. (Pubitemid 350035196)
15. De Paola V, Arber S, Caroni P. 2003. AMPA receptors regulate dynamic equilibrium of presynaptic terminals in mature hippocampal networks. Nat Neurosci. 6:491-500. (Pubitemid 36514697)
16. Dityatev A, Dityateva G, Schachner M. 2000. Synaptic strength as a function of post-versus presynaptic expression of the neural cell adhesion molecule NCAM. Neuron. 26:207-217.
17. Foley AG, Ronn LC, Murphy KJ, Regan CM. 2003. Distribution of polysialylated neural cell adhesion molecule in rat septal nuclei and septohippocampal pathway transient increase of polysialylated interneurons in the subtriangular septal zone during memory consolidation. J Neurosci Res. 74:807-817. (Pubitemid 37490413)
18. Freund TF, Buzsaki G. 1996. Interneurons of the hippocampus. Hippocampus. 6:1-470.
19. Fritschy JM, Harvey RJ, Schwarz G. 2008. Gephyrin: where do we stand, where do we go? Trends Neurosci. 31:257-264.
20. Galuska SP, Rollenhagen M, Kaup M, Eggers K, Oltmann-Norden I, Schiff M, Hartmann M, Weinhold B, Hildebrandt H, Geyer R, et al. 2010. Synaptic cell adhesion molecule SynCAM 1 is a target for polysialylation in postnatal mouse brain. Proc Natl Acad Sci USA. 107:10250-10255.
21. Gascon E, Vutskits L, Kiss JZ. 2007. Polysialic acid-neural cell adhesion molecule in brain plasticity from synapses to integration of new neurons. Brain Res Rev. 56:101-118. (Pubitemid 350100865)
22. Gogolla N, Galimberti I, Deguchi Y, Caroni P. 2009. Wnt signaling mediates experience-related regulation of synapse numbers and mossy fiber connectivities in the adult hippocampus. Neuron. 62:510-525.
23. Gomez-Climent MA, Castillo-Gomez E, Varea E, Guirado R, BlascoIbanez JM, Crespo C, Martinez-Guijarro FJ, Nacher J. 2008. A population of prenatally generated cells in the rat paleocortex maintains an immature neuronal phenotype into adulthood. Cereb Cortex. 18:2229.
24. Greengard P, Valtorta F, Czernik AJ, Benfenati F. 1993. Synaptic vesicle phosphoproteins and regulation of synaptic function. Science. 259:780-785. (Pubitemid 23066304)
25. Hildebrandt H, Muhlenhoff M, Gerardy-Schahn R. 2008. Polysialylation ofNCAM. Neurochem Res. doi:10.1007/s11064-008-9724-7.
26. Kochlamazashvili G, Senkov O, Grebenyuk S, Robinson C, Xiao MF, Stummeyer K, Gerardy-Schahn R Engel AK, Feig L, Semyanov A et al. 2010. Neural cell adhesion molecule-associated polysialic acid regulates synaptic plasticity and learning by restraining the signaling through GluN2B-containing NMDA receptors. J Neurosci. 30:4171-4183.
27. Lee WC, Chen JL, Huang H, Leslie JH, Amitai Y, So PT, Nedivi E. 2008. A dynamic zone defines interneuron remodeling in the adult cortex. Proc Natl Acad Sci USA. 105:6.
28. Lee WC, Huang H, Feng G, Sanes JR, Brown EN, So PT, Nedivi E. 2006. Dynamic remodeling of dendritic arbors in GABAergic interneurons of adult visual cortex. PLoS Biol. 4:e29.
29. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. 2004. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci. 5:793-807. (Pubitemid 39336216)
30. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM. 1997. Identification and characterization of the vesicular GABA transporter. Nature. 389:870-876. (Pubitemid 27462983)
31. Mikkonen M, Soininen H, Tapiola T, Alafuzoff I, Miettinen R. 1999. Hippocampal plasticity in Alzheimer's disease: changes in highly polysialylated NCAM immunoreactivity in the hippocampal formation. Eur J Neurosci. 11:1754-1764. (Pubitemid 29192250)
32. Muhlenhoff M, Eckhardt M, Bethe A, Frosch M, Gerardy-Schahn R. 1996. Autocatalytic polysialylation of polysialyltransferase-1. EMBO J. 15:6943-6950. (Pubitemid 27023265)
33. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development. 116:201-211.
34. Muller D, Wang C, Skibo G, Toni N, Cremer H, Calaora V, Rougon G, Kiss JZ. 1996. PSA-NCAM is required for activity-induced synaptic plasticity. Neuron. 17:413-422. (Pubitemid 26322213)
35. Nacher J, Alonso-Llosa G, Rosell DR, McEwen BS. 2002. PSA-NCAM expression in the piriform cortex of the adult rat. Modulation by NMDA receptor antagonist administration. Brain Res. 927:111-121. (Pubitemid 34124118)
36. Nacher J, Blasco-Ibanez JM, McEwen BS. 2002. Non-granule PSA-NCAM immunoreactive neurons in the rat hippocampus. Brain Res. 930:1-11. (Pubitemid 34195622)
37. Nacher J, Varea E, Blasco-Ibanez JM, Castillo-Gomez E, Crespo C, Martinez-Guijarro FJ, McEwen BS. 2005. Expression of the transcription factor Pax 6 in the adult rat dentate gyrus. J Neurosci Res. 81:753-761. (Pubitemid 41532141)
38. Ohira K, Furuta T, Hioki H, Nakamura KC, Kuramoto E, Tanaka Y, Funatsu N, Shimizu K, Oishi T, Hayashi M, et al. 2010. Ischemiainduced neurogenesis of neocortical layer 1 progenitor cells. Nat Neurosci. 13:173-179.
39. Paxinos G, Franklin KBJ. 1997. The mouse brain in stereotaxic coordinates. London: Academic Press.
40. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates. London: Academic Press.
41. Pham K, Nacher J, Hof PR, McEwen BS. 2003. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expres-sion in the adult rat dentate gyrus. Eur J Neurosci. 17:879-886. (Pubitemid 36315258)
42. Rougon G, Dubois C, Buckley N, Magnani JL, Zollinger W. 1986. A monoclonal antibody against meningococcus group B polysacchar-ides distinguishes embryonic from adult N-CAM. J Cell Biol. 103:2429-2437. (Pubitemid 17216667)
43. Rousselot P, Lois C, Alvarez-Buylla A. 1995. Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J Comp Neurol. 351:51-61.
44. Rutishauser U. 2008. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci. 9:26-35. (Pubitemid 350295686)
45. Sairanen M, O'Leary OF, Knuuttila JE, Castren E. 2007. Chronic antidepressant treatment selectively increases expression of plasticity-related proteins in the hippocampus and medial prefrontal cortex of the rat. Neuroscience. 144:368-374. (Pubitemid 44839045)
46. Schuster T, Krug M, Stalder M, Hackel N, Gerardy-Schahn R, Schachner M. 2001. Immunoelectron microscopic localization of the neural recognition molecules L1, NCAM, and its isoform NCAM180, the NCAM-associated polysialic acid, beta1 integrin and the extracellular matrix molecule tenascin-R in synapses of the adult rat hippocampus. J Neurobiol. 49:142-158. (Pubitemid 32973367)
47. Schwartzkroin PA, Kunkel DD. 1985. Morphology of identified interneurons in the CA1 regions of guinea pig hippocampus. J Comp Neurol. 232:205-218. (Pubitemid 15162319)
48. Seki T, Arai Y. 1991. Expression of highly polysialylated NCAM in the neocortex and piriform cortex of the developing and the adult rat. Anat Embryol (Berl). 184:395-401.
49. Seki T, Arai Y. 1993a. Distribution and possible roles of the highly polysialylated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system. Neurosci Res. 17:265-290. (Pubitemid 23298835)
50. Seki T, Arai Y. 1993b. Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J Neurosci. 13:2351-2358. (Pubitemid 23151752)
51. Seki T, Arai Y. 1995. Age-related production of new granule cells in the adult dentate gyrus. Neuroreport. 6:2479-2482. (Pubitemid 26031190)
52. Seki T, Arai Y. 1999. Different polysialic acid-neural cell adhesion molecule expression patterns in distinct types of mossy fiber boutons in the adult hippocampus.J Comp Neurol. 410:115-125. (Pubitemid 29284224)
53. Sholl DA. 1953. Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat. 87:387-406.
54. Varea E, Blasco-Ibanez JM, Gomez-Climent MA, Castillo-Gomez E, Crespo C, Martinez-Guijarro FJ, Nacher J. 2007. Chronic fluoxetine treatment increases the expression of PSA-NCAM in the medial prefrontal cortex. Neuropsychopharmacology. 32: 803-812. (Pubitemid 46426182)
55. Varea E, Castillo-Gomez E, Gomez-Climent MA, Blasco-Ibanez JM, Crespo C, Martinez-Guijarro FJ, Nacher J. 2007a. Chronic antide-pressant treatment induces contrasting patterns of synaptophysin and PSA-NCAM expression in different regions of the adult rat telencephalon. Eur Neuropsychopharmacol. 17:546-557. (Pubitemid 46766591)
56. Varea E, Castillo-Gomez E, Gomez-Climent MA, Blasco-Ibanez JM, Crespo C, Martinez-Guijarro FJ, Nacher J. 2007b. PSA-NCAM expression in the human prefrontal cortex. J Chem Neuroanat. 33:202-209. (Pubitemid 46755541)
57. Varea E, Castillo-Gomez E, Gomez-Climent MA, Guirado R, Blasco-Ibanez JM, Crespo C, Martinez-Guijarro FJ, Nacher J. 2009. Differential evolution of PSA-NCAM expression during aging of the rat telencephalon. Neurobiol Aging. 30:11.
58. Varea E, Nacher J, Blasco-Ibanez JM, Gomez-Climent MA, Castillo-Gomez E, Crespo C, Martinez-Guijarro FJ. 2005. PSA-NCAM expression in the rat medial prefrontal cortex. Neuroscience. 136:435-443. (Pubitemid 41607892)
59. West MJ. 1993. New stereological methods for counting neurons. Neurobiol Aging. 14:275-285. (Pubitemid 23214693)
60. Zuber C, Lackie PM, Catterall WA, Roth J. 1992. Polysialic acid is associated with sodium channels and the neural cell adhesion molecule N-CAM in adult rat brain. J Biol Chem. 267:9965-9971.