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Abstract:

The neural cell adhesion molecule (NCAM; CD56) is a member of the immunoglobulin protein superfamily. It has been described as a key molecule for the regulation of neuronal differentiation, synaptogenesis, memory formation, and neuronal plasticity. Alternative splicing gives rise to at least 20-30 NCAM isoforms in mice and humans, NCAM120, NCAM140, and NCAM180 being the more abundant. There are many different modes of alternative splicing; the difference between NCAM140 and NCAM180 is the inclusion or exclusion of an alternative exon. During neuronal differentiation, the alternative splicing pattern of NCAM changes, favoring the expression of NCAM180 to the detriment of NCAM140. In this work we review the most relevant information about NCAM structure and function and present the molecular basis of alternative splicing and its regulation with particular emphasis on how changes in chromatin structure are key for the regulation of NCAM splicing during neuronal differentiation and upon membrane depolarization. © 2015 Elsevier Inc. All rights reserved.

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Documento: Parte de libro
Título:Fundamentals of NCAM Expression, Function, and Regulation of Alternative Splicing in Neuronal Differentiation
Autor:Fiszbein, A.; Schor, I.E.; Kornblihtt, A.R.
Filiación:Laboratorio de Fisiologia y Biologia Molecular, Departamento de Fisiologia, Biología Molecular y Celular, IFIBYNE-CONICET, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
European Molecular Biology Laboratory, Heidelberg, Germany
Palabras clave:Alternative splicing; CD56; Chromatin structure; NCAM; Neuronal differentiation; Transcription rate; Cell adhesion; Chromosomes; Molecules; Alternative splicing; CD56; Chromatin structure; NCAM; Neuronal differentiation; Neurons
Año:2015
Página de inicio:131
Página de fin:140
DOI: http://dx.doi.org/10.1016/B978-0-12-800781-5.00011-6
Título revista:Neural Surface Antigens: From Basic Biology Towards Biomedical Applications
Título revista abreviado:Neural Surf. Antigens: From Basic Biol. Towards Biomed. Appl.
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_97801280_v_n_p131_Fiszbein

Referencias:

  • Rutishauser, U., Thiery, J.P., Brackenbury, R., Sela, B.A., Edelman, G.M., Mechanisms of adhesion among cells from neural tissues of the chick embryo (1976) Proc Natl Acad Sci USA, 73, pp. 577-581
  • Thiery, J.P., Brackenbury, R., Rutishauser, U., Edelman, G.M., Characterization of a cell adhesion molecule from neural retina. II. Purification and adhesion among neural cells of the chick embryo (1977) J Biol Chem, 252, pp. 6841-6845
  • Andersson, A.M., Olsen, M., Zhernosekov, D., Gaardsvoll, H., Krog, L., Linnemann, D., Age-related changes in expression of the neural cell adhesion molecule in skeletal muscle: a comparative study of newborn, adult and aged rats (1993) Biochem J, 290, pp. 641-648
  • Pruszak, J., Sonntag, K., Aung, M.H., Sanchez-Pernaute, R., Isacson, O., Markers and methods for cell sorting of human embryonic stem cell-derived neural cell populations (2007) Stem Cells, 25 (9), pp. 2257-2268
  • Poli, A., Michel, T., Thérésine, M., Andràs, E., Hentges, F., Zimmer, J., CD56bright natural killer (NK) cells: an important NK cell subset (2009) Immunology, 126 (4), pp. 458-465
  • Zola, H., Swart, B., Cholson, I., Voss, E., (2007) CD56. Leukocyte and stromal cell molecules-the CD markers, pp. 138-139. , Wiley-Liss, New Jersey
  • Buhring, H.J., Battula, V.L., Treml, S., Schewe, B., Kanz, L., Vogel, W., Novel markers for the prospective isolation of human MSC (2007) Ann NY Acad Sci, 1106, pp. 262-271
  • Gattenlöhner, S., Stühmer, T., Leich, E., Reinhard, M., Etschmann, B., Völker, H.U., Specific detection of CD56 (NCAM) isoforms for the identification of aggressive malignant neoplasms with progressive development (2009) Am J Pathol, 174 (4), pp. 1160-1171
  • Graveley, B.R., Kaur, A., Gunning, D., Zipursky, S.L., Rowen, L., Clemens, J.C., The organization and evolution of the dipteran and hymenopteran down syndrome cell adhesion molecule (Dscam) genes (2004) RNA, 10 (10), pp. 1499-1506
  • Walsh, F.S., Putt, W., Dickson, J.G., Quinn, C.A., Cox, R.D., Webb, M., Human N-CAM gene: mapping to chromosome 11 by analysis of somatic cell hybrids with mouse and human cDNA probes (1986) Brain Res, 387, pp. 197-200
  • Goridis, C., Brunet, J.F., NCAM: structural diversity, function and regulation of expression (1992) Semin Cell Biol, 3, pp. 189-197
  • Kolkova, K., Biosynthesis of NCAM (2010) Adv Exp Med Biol, 663, pp. 213-225
  • Edelman, G.M., Crossin, K.L., Cell adhesion molecules: implications for a molecular histology (1991) Annu Rev Biochem, 60, pp. 155-190
  • Byeon, M.K., Sugi, Y., Markwald, R.R., Hoffman, S., NCAM polypeptides in heart development: association with Z discs of forms that contain the muscle-specific domain (1995) J Cell Biol, 128 (1-2), pp. 209-221
  • Walmod, P.S., Kolkova, K., Berezin, V., Bock, E., Zippers make signals: NCAM-mediated molecular interactions and signal transduction (2004) Neurochem Res, 29, pp. 2015-2035
  • He, H.T., Barbet, J., Chaix, J.C., Goridis, C., Phosphatidylinositol is involved in the membrane attachment of NCAM-120, the smallest component of the neural cell adhesion molecule (1986) EMBO J, 5, pp. 2489-2494
  • Hinkle, C.L., Diestel, S., Lieberman, J., Maness, P.F., Metalloprotease-induced ectodomain shedding of neural cell adhesion molecule (NCAM) (2006) J Neurobiol, 66, pp. 1378-1395
  • Gibbons, A.S., Thomas, E.A., Dean, B., Regional and duration of illness differences in the alteration of NCAM-180 mRNA expression within the cortex of subjects with schizophrenia (2009) Schizophr Res, 112 (1-3), pp. 65-71
  • Doherty, P., Rimon, G., Mann, D.A., Walsh, F.S., Alternative splicing of the cytoplasmic domain of neural cell adhesion molecule alters its ability to act as a substrate for neurite outgrowth (1992) J Neurochem, 58, pp. 2338-2341
  • Persohn, E., Schachner, M., Immunohistological localization of the neural adhesion molecules L1 and N-CAM in the developing hippocampus of the mouse (1990) J Neurocytol, 19, pp. 807-819
  • Sytnyk, V., Leshchyns'ka, I., Nikonenko, A.G., Schachner, M., NCAM promotes assembly and activity-dependent remodeling of the postsynaptic signaling complex (2006) J Cell Biol, 174, pp. 1071-1085
  • Kasper, C., Rasmussen, H., Kastrup, J.S., Ikemizu, S., Jones, E.Y., Berezin, V., Structural basis of cell-cell adhesion by NCAM (2000) Nat Struct Biol, 5, pp. 389-393
  • Horstkorte, R., Schachner, M., Magyar, J.P., Vorherr, T., Schmitz, B., The fourth immunoglobulin-like domain of NCAM contains a carbohydrate recognition domain for oligomannosidic glycans implicated in association with L1 and neurite outgrowth (1993) J Cell Biol, 121, pp. 1409-1421
  • Brümmendorf, T., Rathjen, F.G., Structure/function relationships of axon-associated adhesion receptors of the immunoglobulin superfamily (1996) Curr Opin Neurobiol, 6, pp. 584-593
  • Kiselyov, V.V., Skladchikova, G., Hinsby, A.M., Jensen, P.H., Kulahin, N., Soroka, V., Structural basis for a direct interaction between FGFR1 and NCAM and evidence for a regulatory role of ATP (2003) Structure, 11, pp. 691-701
  • Doherty, P., Walsh, F., CAM-FGF receptor interactions: a model for axonal growth (1996) Mol Cell Neurosci, 8, pp. 99-111
  • Kiselyov, V.V., NCAM and the FGF-Receptor (2010) Adv Exp Med Biol, 663, pp. 67-79
  • Rougon, G., Structure, metabolism and cell biology of polysialic acids (1993) Eur J Cell Biol, 61 (2), pp. 197-207
  • Mühlenhoff, M., Eckhardt, M., Gerardy-Schahn, R., Polysialic acid: three-dimensional structure, biosynthesis and function (1998) Curr Opin Struct Biol, 8 (5), pp. 558-564
  • Finne, J., Finne, U., Deagostini-Bazin, H., Goridis, C., Ocurrende of alpha 2-8 linked polysialosyl units in a neural cell adheseion molecule (1983) Biochem Biophys Res Commun, 112 (2), pp. 482-487
  • Rutishauser, U., Landmesser, L., Polysialic acid in the vertebrate nervous system: a promotor of plasticity in cell-cell interactions (1996) Trends Neurosci, 19 (10), pp. 422-427
  • Tang, J., Landmesser, L., Reduction of intramuscular nerve branching and synaptogenesis is correlated with decreased motoneuron survival (1993) J Neurosci, 13 (7), pp. 3095-3103
  • Tang, J., Landmesser, L., Rutishauser, U., Polysialic acid influences specific pathfinding by avian motoneurons (1992) Neuron, 8 (6), pp. 1031-1044
  • Angata, K., Nakayama, J., Fredette, B., Chong, K., Ranscht, B., Fukuda, M., Human STX polysialyltransferase forms the embryonic form of the neural cell adhesion molecule. Tissue-specific expression, neurite outgrowth, and chromosomal localization in comparison with another polysialyltransferase, PST (1997) J Biol Chem, 272 (11), pp. 7182-7190
  • Hildebrandt, H., Becker, C., Murau, M., Gerardy-Schahn, R., Rahmann, H., Heterogeneous expression of the polysialyltransferases ST8Sia II and ST8Sia IV during postnatal rat brain development (1998) J Neurochem, 71 (6), pp. 2339-2348
  • Eckhardt, M., Bukalo, O., Chazal, G., Wang, L., Goridis, C., Schachner, M., Mice deficient in the polysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity (2000) J Neurosci, 20 (14), pp. 5234-5244
  • Kiss, J.Z., Wang, C., Olive, S., Rougon, G., Lang, J., Baetens, D., Activity-dependent mobilization of the adhesion molecule polysialic NCAM to the cell surface of neurons and endocrine cells (1994) EMBO J, 13 (22), pp. 5284-5292
  • Wang, C., Pralong, W.F., Schulz, M.F., Rougon, G., Aubry, J.M., Pagliusi, S., Functional N-methyl-D-aspartate receptors in O-2A glial precursor cells: a critical role in regulating polysialic acid-neural cell adhesion molecule expression and cell migration (1996) J Cell Biol, 135 (6), pp. 1565-1581
  • Bouzioukh, F., Tell, F., Rougon, G., Jean, A., Dual effects of NMDA receptor activation on polysialylated neural cell adhesion molecule expression during brainstem postnatal development (2001) Eur J Neurosci, 14 (8), pp. 1194-1202
  • Cole, G.J., Loewy, A., Glaser, L., Neuronal cell-cell adhesion depends on interactions of N-CAM with heparin-like molecules (1986) Nature, 320, pp. 445-447
  • Bruses, J.L., Chauvet, N., Rubio, M.E., Rutishauser, U., Polysialic acid and the formation of oculomotor synapses on chick ciliary neurons (2002) J Comp Neurol, 446, pp. 244-256
  • Gascon, E., Vutskits, L., Kiss, J.Z., Polysialic acid-neural cell adhesion molecule in brain plasticity: from synapses to integration of new neurons (2007) Brain Res Rev, 56 (1), pp. 101-118
  • Cremer, H., Chazal, G., Carleton, A., Goridis, C., Vincent, J.D., Lledo, P.M., Long-term but not short-term plasticity at mossy fiber synapses is impaired in neural cell adhesion molecule-deficient mice (1998) Proc Natl Acad Sci USA, 95, pp. 13242-13247
  • Angata, K., Long, J.M., Bukalo, O., Lee, W., Dityatev, A., Wynshaw-Boris, A., Sialyltransferase ST8Sia-II assembles a subset of polysialic acid that directs hippocampal axonal targeting and promotes fear behavior (2004) J Biol Chem, 279 (31), pp. 32603-32613
  • Aonurm-Helm, A., Jurgenson, M., Zharkovsky, T., Sonn, K., Berezin, V., Bock, E., Depression-like behaviour in neural cell adhesion molecule (NCAM)-deficient mice and its reversal by an NCAM-derived peptide, FGL (2008) Eur J Neurosci, 28, pp. 1618-1628
  • Bonfati, L., PSA-NCAM in mammalian structural plasticity and neurogenesis (2006) Prog Neurobiol, 80 (3), pp. 129-164
  • Vutskits, L., Gascon, E., Zgraggen, E., Kiss, J.Z., The polysialylated neural cell adhesion molecule promotes neurogenesis in vitro (2006) Neurochem Res, 31, pp. 215-225
  • Amoureux, M.C., Cunningham, B.A., Edelman, G.M., Crossin, K.L., N-CAM binding inhibits the proliferation of hippocampal progenitor cells and promotes their differentiation to a neuronal phenotype (2000) J Neurosci, 20, pp. 3631-3640
  • Kim, B.W., Son, H., Neural cell adhesion molecule (NCAM) induces neuronal phenotype acquisition in dominant negative MEK1-expressing hippocampal neural progenitor cells (2006) Exp Mol Med, 38 (6), pp. 732-738
  • Röckle, I., Seidenfaden, R., Weinhold, B., Mühlenhoff, M., Gerardy-Schahn, R., Hildebrandt, H., Polysialic acid controls NCAM-induced differentiation of neuronal precursors into calretinin-positive olfactory bulb interneurons (2008) Dev Neurobiol, 68, pp. 1170-1184
  • Walsh, F.S., Hobbs, C., Wells, D.J., Slater, C.R., Fazeli, S., Ectopic expression of NCAM in skeletal muscle of transgenic mice results in terminal sprouting at the neuromuscular junction and altered structure but not function (2000) Mol Cell Neurosci, 15 (3), pp. 244-261
  • Dallérac, G., Rampon, C., Doyàre, V., NCAM function in the adult brain: lessons from mimetic peptides and therapeutic potential (2013) Neurochem Res, 38 (6), pp. 1163-1173
  • Gomez-Climent, M.A., Guirado, R., Castillo-Gomez, E., Varea, E., Gutierrez-Mecinas, M., Gilabert-Juan, J., 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 (2011) Cereb Cortex, 21, pp. 1028-1041
  • Nacher, J., Guirado, R., Castillo-Gómez, E., Structural plasticity of interneurons in the adult brain: role of PSA-NCAM and implications for psychiatric disorders (2005) Neurochem Res, 38 (6), pp. 1122-1133
  • Castren, E., Is mood chemistry? (2005) Nat Rev Neurosci, 6, pp. 241-246
  • Lewis, D.A., Gonzalez-Burgos, G., Neuroplasticity of neocortical circuits in schizophrenia (2008) Neuropsychopharmacology, 33, pp. 141-165
  • Pollerberg, G.E., Schachner, M., Davoust, J., Differentiation state-dependent surface mobilities of two forms of the neural cell adhesion molecule (1986) Nature, 324 (6096), pp. 462-465
  • Pollerberg, G.E., Burridge, K., Krebs, K.E., Goodman, S.R., Schachner, M., The 180-kD component of the neural cell adhesion molecule N-CAM is involved in cell-cell contact and cytoskeleton-membrane interactions (1987) Cell Tissue Res, 250 (1), pp. 227-236
  • Takei, K., Chan, T.A., Wang, F.S., Deng, H., Rutishauser, U., Jay, D.J., The neural cell adhesion molecules L1 and NCAM-180 act in different steps of neurite outgrowth (1999) J Neurosci, 19 (21), pp. 9469-9479
  • Kiss, J.Z., Troncoso, E., Djebbara, Z., Vutskits, L., Muller, D., The role of neural cell adhesion molecules in plasticity and repair (2001) Brain Res Rev, 36 (2001), pp. 175-184
  • Prodromidou, K., Papastefanaki, F., Sklaviadis, T., Matsas, R., Functional cross-talk between the cellular prion protein and the neural cell adhesion molecule NCAM is critical for neuronal differentiation of neural stem/precursor cells (2014) Stem Cells, 32 (6), pp. 1674-1687
  • Burge, C.B., Tuschl, T., Sharp, P.A., Splicing of precursors to mRNAs by the spliceosomes (1999) RNA World, pp. 525-560
  • Black, D.L., Grabowski, P.J., Alternative pre-mRNA splicing and neuronal function (2003) Prog Mol Subcell Biol, 31, pp. 187-216
  • Kornblihtt, A.R., Schor, I.E., Alló, M., Dujardin, G., Petrillo, E., Muñoz, M.J., Alternative splicing: a pivotal step between eukaryotic transcription and translation (2013) Nat Rev Mol Cell Biol, 14 (3), pp. 153-165
  • Black, D.L., Protein diversity from alternative splicing: a challenge for bioinformatics and post-genome biology (2000) Cell, 103, pp. 367-370
  • Smith, C.W., Nadal-Ginard, B., Mutually exclusive splicing of alpha-tropomyosin exons enforced by an unusual lariat branch point location: implications for constitutive splicing (1989) Cell, 56 (5), pp. 749-758
  • Beyer, A.L., Osheim, Y.N., Splice site selection, rate of splicing and alternative splicing on nascent transcripts (1988) Genes Dev, 2 (6), pp. 754-765
  • Conaway, J.W., Shilatifard, A., Dvir, A., Conaway, R.C., Control of elongation by RNA polymerase II (2000) TIBS, 25 (8), pp. 375-380
  • de la Mata, M., Alonso, C.R., Kadener, S., Fededa, J.P., Blaustein, M., Pelisch, F., A slow RNA polymerase II affects alternative splicing in vivo (2003) Mol Cell, 12 (2), pp. 525-532
  • Cramer, P., Pesce, C.G., Baralle, F.E., Kornblihtt, A.R., Functional association between promoter structure and transcript alternative splicing (1997) Proc Natl Acad Sci USA, 94 (21), pp. 11456-11460
  • Adami, G., Babiss, L.E., DNA template effect on RNA splicing: two copies of the same gene in the same nucleus are processed differently (1991) EMBO J, 10, pp. 3457-3465
  • Nogues, G., Kadener, S., Cramer, P., Bentley, D., Kornblihtt, A.R., Transcriptional activators differ in their abilities to control alternative splicing (2002) J Biol Chem, 277 (45), pp. 43110-43114
  • Lorincz, M.C., Dickerson, D.R., Schmitt, M., Groudine, M., Intragenic DNA methylation alters chromatin structure and elongation efficiency in mammalian cells (2004) Nat Struct Mol Biol, 11 (11), pp. 1068-1075
  • Luco, R.F., Pan, Q., Tominaga, K., Blencowe, B.J., Pereira-Smith, O.M., Misteli, T., Regulation of alternative splicing by histone modifications (2010) Science, 327 (5968), pp. 996-1000
  • Ameyar-Zazoua, M., Rachez, C., Souidi, M., Robin, P., Fritsch, L., Young, R., Argonaute proteins couple chromatin silencing to alternative splicing (2012) Nat Struct Mol Biol, 19 (10), pp. 998-1004
  • Saint-Andre, V., Batsche, E., Rachez, C., Muchardt, C., Histone H3 lysine 9 trimethylation and HP1gamma favor inclusion of alternative exons (2011) Nat Struct Mol Biol, 18 (3), pp. 337-344
  • Allemand, E., Batsché, E., Muchardt, C., Splicing, transcription, and chromatin: a ménageàtrois (2008) Curr Opin Genet Dev, 18 (2), pp. 145-151
  • Kolasinska-Zwierz, P., Down, T., Latorre, I., Liu, T., Liu, X.S., Ahringer, J., Differential chromatin marking of introns and expressed exons by H3K36me3 (2009) Nat Genet, 41 (3), pp. 376-381
  • Andersson, R., Enroth, S., Rada-Iglesias, A., Wadelius, C., Komorowski, J., Nucleosomes are well positioned in exons and carry characteristic histone modifications (2009) Genome Res, 19 (10), pp. 1732-1741
  • Berget, S.M., Exon recognition in vertebrate splicing (1995) J Biol Chem, 270 (6), pp. 2411-2414
  • Tacke, R., Goridis, C., Alternative splicing in the neural cell adhesion molecule pre-mRNA: regulation of exon 18 skipping depends on the 5'-splice site (1991) Genes Dev, 5 (8), pp. 1416-1429
  • Côté, J., Simard, M.J., Chabot, B., An element in the 5' common exon of the NCAM alternative splicing unit interacts with SR proteins and modulates 5' splice site selection (1999) Nucleic Acids Res, 27 (12), pp. 2529-2537
  • Côté, J., Chabot, B., Natural base-pairing interactions between 5' splice site and branch site sequences affect mammalian 5' splice site selection (1997) RNA, 3 (11), pp. 1248-1261
  • Schor, I.E., Rascovan, N., Pelisch, F., Alló, M., Kornblihtt, A.R., Neuronal cell depolarization induces intragenic chromatin modifications affecting NCAM alternative splicing (2009) Proc Natl Acad Sci USA, 106 (11), pp. 4325-4330
  • Schor, I.E., Fiszbein, A., Petrillo, E., Kornblihtt, A.R., Intragenic epigenetic changes modulate NCAM alternative splicing in neuronal differentiation (2013) EMBO J, 32 (16), pp. 2264-2274
  • Singh, J., Padgett, R.A., Rates of in situ transcription and splicing in large human genes (2009) Nat Struct Mol Biol, 16 (11), pp. 1128-1133
  • Alló, M., Buggiano, V., Fededa, J.P., Petrillo, E., Schor, I., de la Mata, M., Control of alternative splicing through siRNA-mediated transcriptional gene silencing (2009) Nat Struct Mol Biol, 16 (7), pp. 717-724

Citas:

---------- APA ----------
Fiszbein, A., Schor, I.E. & Kornblihtt, A.R. (2015) . Fundamentals of NCAM Expression, Function, and Regulation of Alternative Splicing in Neuronal Differentiation. Neural Surface Antigens: From Basic Biology Towards Biomedical Applications, 131-140.
http://dx.doi.org/10.1016/B978-0-12-800781-5.00011-6
---------- CHICAGO ----------
Fiszbein, A., Schor, I.E., Kornblihtt, A.R. "Fundamentals of NCAM Expression, Function, and Regulation of Alternative Splicing in Neuronal Differentiation" . Neural Surface Antigens: From Basic Biology Towards Biomedical Applications (2015) : 131-140.
http://dx.doi.org/10.1016/B978-0-12-800781-5.00011-6
---------- MLA ----------
Fiszbein, A., Schor, I.E., Kornblihtt, A.R. "Fundamentals of NCAM Expression, Function, and Regulation of Alternative Splicing in Neuronal Differentiation" . Neural Surface Antigens: From Basic Biology Towards Biomedical Applications, 2015, pp. 131-140.
http://dx.doi.org/10.1016/B978-0-12-800781-5.00011-6
---------- VANCOUVER ----------
Fiszbein, A., Schor, I.E., Kornblihtt, A.R. Fundamentals of NCAM Expression, Function, and Regulation of Alternative Splicing in Neuronal Differentiation. Neural Surf. Antigens: From Basic Biol. Towards Biomed. Appl. 2015:131-140.
http://dx.doi.org/10.1016/B978-0-12-800781-5.00011-6