Abstract
Cell adhesion molecules (CAMs) mediate cell-to-cell interactions and interactions between cells and the extracellular matrix (ECM). The neural cell adhesion molecule (NCAM), a prototypic member of the immunoglobulin (Ig) superfamily of CAMs, mediates adhesion through homophilic and heterophilic interactions, thereby modulating a range of biological processes. This review summarizes interactions between NCAM and other CAMs and ECM proteins. Additionally, the role of NCAM as a receptor for rabies virus, and its implications in rabies infections is briefly described. Interactions between NCAM and its heterophilic partners involve most of the NCAM extracellular modules and are mediated via amino acids and carbohydrates. The interactions promote cell adhesion and trigger signal transduction and alterations in cytoskeletal dynamics and organization. Heterophilic NCAM interactions may modulate, or be modulated by, homophilic NCAM interactions. Furthermore, some of the interactions are mutually exclusive, whereas others might lead to the formation of multimeric protein complexes. Consequently, biological processes affected by NCAM interactions are regulated in a complex manner involving many extracellular protein interactions.
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Abbreviations
- CAH:
-
Carbonic anhydrase
- CAM:
-
Cell adhesion molecule
- CHL1:
-
Close homolog of L1
- CNS:
-
Central nervous system
- CSPG:
-
Chondroitin sulfate proteoglycans
- ECM:
-
Extracellular matrix
- FGFR:
-
Fibroblast growth factor receptor
- FnIII:
-
Fibronectin type 3
- GAG:
-
Glycosaminoglycans
- GDNF:
-
Glial cell line-derived neurotrophic factor
- GPI:
-
Glycosylphosphatidylinositol
- HB-GAM:
-
Heparin-binding growth-associated molecule
- HBD:
-
Heparin binding domain
- HNK-1:
-
Human natural killer-1
- HSPG:
-
Heparan sulfate proteoglycans
- Kd:
-
Equilibrium dissociation constant
- LRP:
-
Laminin receptor precursor
- MSD1:
-
Muscle-specific domain 1
- NCAM:
-
Neural cell adhesion molecule
- NMR:
-
Nuclear magnetic resonance
- PG:
-
Proteoglycans
- PI-PLC:
-
Phosphatidylinositol-specific phospholipase C
- PrP:
-
Protease resistant protein
- RPTP:
-
Receptor protein tyrosine phosphatase
- PSA:
-
Polysialic acid
- RABV:
-
Rabies virus
- SOS:
-
Sucrose octasulfate
- SPR:
-
Surface plasmon resonance
- VASE:
-
Variable alternative spliced exon
References
Filiz S, Dalcik H, Yardimoglu M, Gonca S, Ceylan S (2002) Localization of neural cell adhesion molecule (N-CAM) immunoreactivity in adult rat tissues. Biotech Histochem 77:127-135
Burroughs CL, Watanabe M, Morse DE (1991) Distribution of the neural cell adhesion molecule (NCAM) during heart development. J Mol Cell Cardiol 23:1411-1422
Gaardsvoll H, Krog L, Zhernosekov D, Andersson AM, Edvardsen K, Olsen M, Bock E, Linnemann D (1993) Age-related changes in expression of neural cell adhesion molecule (NCAM) in heart: a comparative study of newborn, adult and aged rats. Eur J Cell Biol 61:100-107
Reyes AA, Small SJ, Akeson R (1991) At least 27 alternatively spliced forms of the neural cell adhesion molecule mRNA are expressed during rat heart development. Mol Cell Biol 11:1654-1661
Fidzianska A, Kaminska A (1995) Neural cell adhesion molecule (N-CAM) as a marker of muscle tissue alternations: review of the literature and own observations. Folia Neuropathol 33:125-128
Carson W, Caligiuri M (1996) Natural killer cell subsets and development. Methods 9:327-343
Farag SS, Caligiuri MA (2006) Human natural killer cell development and biology. Blood Rev 20:123-137
Kontogianni K, Nicholson AG, Butcher D, Sheppard MN (2005) CD56: a useful tool for the diagnosis of small cell lung carcinomas on biopsies with extensive crush artefact. J Clin Pathol 58:978-980
Bataille R, Jego G, Robillard N, Barille-Nion S, Harousseau JL, Moreau P, Amiot M, Pellat-Deceunynck C (2006) The phenotype of normal, reactive and malignant plasma cells: identification of “many and multiple myelomas” and of new targets for myeloma therapy. Haematologica 91:1234-1240
Garnache-Ottou F, Feuillard J, Saas P (2007) Plasmacytoid dendritic cell leukaemia/lymphoma: towards a well defined entity? Br J Haematol 136:539-548
Walmod PS, Pedersen MV, Berezin V, Bock E (2007) Cell adhesion molecules of the immunoglobulin superfamily in the nervous system. In: Lajtha A, Banik N (eds) Handbook of neurochemistry and molecular neurobiology: neural protein metabolism and function, 3rd edn. Springer, New York, pp 35-151
Kiselyov VV, Skladchikova G, Hinsby AM, Jensen PH, Kulahin N, Soroka V, Pedersen N, Tsetlin V, Poulsen FM, Berezin V, Bock E (2003) Structural basis for a direct interaction between FGFR1 and NCAM and evidence for a regulatory role of ATP. Structure 11:691-701
Paratcha G, Ledda F, Ibanez CF (2003) The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 113:867-879
Sjostrand D, Carlsson J, Paratcha G, Persson B, Ibanez CF (2007) Disruption of the GDNF binding site in NCAM dissociates ligand binding and homophilic cell adhesion. J Biol Chem 282:12734-12740
Kiselyov VV, Soroka V, Berezin V, Bock E (2005) Structural biology of NCAM homophilic binding and activation of FGFR. J Neurochem 94:1169-1179
Ditlevsen DK, Povlsen GK, Berezin V, Bock E (2007) NCAM-induced intracellular signaling revisited. J Neurosci Res 86:727-743
Sariola H, Saarma M (2003) Novel functions and signalling pathways for GDNF. J Cell Sci 116:3855-3862
Hubschmann MV, Skladchikova G, Bock E, Berezin V (2005) Neural cell adhesion molecule function is regulated by metalloproteinase-mediated ectodomain release. J Neurosci Res 80:826-837
Kalus I, Bormann U, Mzoughi M, Schachner M, Kleene R (2006) Proteolytic cleavage of the neural cell adhesion molecule by ADAM17/TACE is involved in neurite outgrowth. J Neurochem 98:78-88
He HT, Barbet J, Chaix JC, Goridis C (1986) Phosphatidylinositol is involved in the membrane attachment of NCAM-120, the smallest component of the neural cell adhesion molecule. EMBO J 5:2489-2494
He HT, Finne J, Goridis C (1987) Biosynthesis, membrane association, and release of N-CAM-120, a phosphatidylinositol-linked form of the neural cell adhesion molecule. J Cell Biol 105:2489-2500
Bock E, Edvardsen K, Gibson A, Linnemann D, Lyles JM, Nybroe O (1987) Characterization of soluble forms of NCAM. FEBS Lett 225:33-36
Gower HJ, Barton CH, Elsom VL, Thompson J, Moore SE, Dickson G, Walsh FS (1988) Alternative splicing generates a secreted form of N-CAM in muscle and brain. Cell 55:955-964
Cunningham BA, Hemperly JJ, Murray BA, Prediger EA, Brackenbury R, Edelman GM (1987) Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science 236:799-806
Small SJ, Haines SL, Akeson RA (1988) Polypeptide variation in an N-CAM extracellular immunoglobulin-like fold is developmentally regulated through alternative splicing. Neuron 1:1007-1017
Dickson G, Gower HJ, Barton CH, Prentice HM, Elsom VL, Moore SE, Cox RD, Quinn C, Putt W, Walsh FS (1987) Human muscle neural cell adhesion molecule (N-CAM): identification of a muscle-specific sequence in the extracellular domain. Cell 50:1119-1130
Thompson J, Dickson G, Moore SE, Gower HJ, Putt W, Kenimer JG, Barton CH, Walsh FS (1989) Alternative splicing of the neural cell adhesion molecule gene generates variant extracellular domain structure in skeletal muscle and brain. Genes Dev 3:348-357
Santoni MJ, Barthels D, Vopper G, Boned A, Goridis C, Wille W (1989) Differential exon usage involving an unusual splicing mechanism generates at least eight types of NCAM cDNA in mouse brain. EMBO J 8:385-392
Albach C, Damoc E, Denzinger T, Schachner M, Przybylski M, Schmitz B (2004) Identification of N-glycosylation sites of the murine neural cell adhesion molecule NCAM by MALDI-TOF and MALDI-FTICR mass spectrometry. Anal Bioanal Chem 378:1129-1135
Walsh FS, Parekh RB, Moore SE, Dickson G, Barton CH, Gower HJ, Dwek RA, Rademacher TW (1989) Tissue specific O-linked glycosylation of the neural cell adhesion molecule (N-CAM). Development 105:803-811
Liedtke S, Geyer H, Wuhrer M, Geyer R, Frank G, Gerardy-Schahn R, Zahringer U, Schachner M (2001) Characterization of N-glycans from mouse brain neural cell adhesion molecule. Glycobiology 11:373-384
von Der Ohe M, Wheeler SF, Wuhrer M, Harvey DJ, Liedtke S, Muhlenhoff M, Gerardy-Schahn R, Geyer H, Dwek RA, Geyer R, Wing DR, Schachner M (2002) Localization and characterization of polysialic acid-containing N-linked glycans from bovine NCAM. Glycobiology 12:47-63
Wuhrer M, Geyer H, von Der Ohe M, Gerardy-Schahn R, Schachner M, Geyer R (2003) Localization of defined carbohydrate epitopes in bovine polysialylated NCAM. Biochimie 85:207-218
Bonfanti L (2006) PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog Neurobiol 80:129-164
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
Rutishauser U (2008) Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci 9:26-35
Kruse J, Mailhammer R, Wernecke H, Faissner A, Sommer I, Goridis C, Schachner M (1984) Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature 311:153-155
Cole GJ, Schachner M (1987) Localization of the L2 monoclonal antibody binding site on chicken neural cell adhesion molecule (NCAM) and evidence for its role in NCAM-mediated cell adhesion. Neurosci Lett 78:227-232
Ong E, Suzuki M, Belot F, Yeh JC, Franceschini I, Angata K, Hindsgaul O, Fukuda M (2002) Biosynthesis of HNK-1 glycans on O-linked oligosaccharides attached to the neural cell adhesion molecule (NCAM): the requirement for core 2β1, 6-N-acetylglucosaminyltransferase and the muscle-specific domain in NCAM. J Biol Chem 277:18182-18190
Yoshihara Y, Kawasaki M, Tamada A, Fujita H, Hayashi H, Kagamiyama H, Mori K (1997) OCAM: a new member of the neural cell adhesion molecule family related to zone-to-zone projection of olfactory and vomeronasal axons. J Neurosci 17:5830-5842
Paoloni-Giacobino A, Chen H, Antonarakis SE (1997) Cloning of a novel human neural cell adhesion molecule gene (NCAM2) that maps to chromosome region 21q21 and is potentially involved in Down syndrome. Genomics 43:43-51
McGarry RC, Helfand SL, Quarles RH, Roder JC (1983) Recognition of myelin-associated glycoprotein by the monoclonal antibody HNK-1. Nature 306:376-378
Shih IM, Elder DE, Speicher D, Johnson JP, Herlyn M (1994) Isolation and functional characterization of the A32 melanoma-associated antigen. Cancer Res 54:2514-2520
Holm J, Hillenbrand R, Steuber V, Bartsch U, Moos M, Lubbert H, Montag D, Schachner M (1996) Structural features of a close homologue of L1 (CHL1) in the mouse: a new member of the L1 family of neural recognition molecules. Eur J Neurosci 8:1613-1629
Hillenbrand R, Molthagen M, Montag D, Schachner M (1999) The close homologue of the neural adhesion molecule L1 (CHL1): patterns of expression and promotion of neurite outgrowth by heterophilic interactions. Eur J Neurosci 11:813-826
Kleene R, Schachner M (2004) Glycans and neural cell interactions. Nat Rev Neurosci 5:195-208
Yu RK, Yanagisawa M (2006) Glycobiology of neural stem cells. CNS Neurol Disord Drug Targets 5:415-423
Key B, Akeson RA (1990) Olfactory neurons express a unique glycosylated form of the neural cell adhesion molecule (N-CAM). J Cell Biol 110:1729-1743
Key B, Akeson RA (1991) Delineation of olfactory pathways in the frog nervous system by unique glycoconjugates and N-CAM glycoforms. Neuron 6:381-396
Pestean A, Krizbai I, Bottcher H, Parducz A, Joo F, Wolff JR (1995) Identification of the Ulex europaeus agglutinin-I-binding protein as a unique glycoform of the neural cell adhesion molecule in the olfactory sensory axons of adults rats. Neurosci Lett 195:117-120
Dowsing B, Puche A, Hearn C, Key B (1997) Presence of novel N-CAM glycoforms in the rat olfactory system. J Neurobiol 32:659-670
Hu W, Rosenberg RN, Stuve O (2007) Prion proteins: a biological role beyond prion diseases. Acta Neurol Scand 116:75-82
Sakaguchi S (2007) Molecular biology of prion protein and its first homologous protein. J Med Invest 54:211-223
Rieger R, Edenhofer F, Lasmezas CI, Weiss S (1997) The human 37-kDa laminin receptor precursor interacts with the prion protein in eukaryotic cells. Nat Med 3:1383-1388
Graner E, Mercadante AF, Zanata SM, Forlenza OV, Cabral AL, Veiga SS, Juliano MA, Roesler R, Walz R, Minetti A, Izquierdo I, Martins VR, Brentani RR (2000) Cellular prion protein binds laminin and mediates neuritogenesis. Brain Res Mol Brain Res 76:85-92
Schmitt-Ulms G, Legname G, Baldwin MA, Ball HL, Bradon N, Bosque PJ, Crossin KL, Edelman GM, DeArmond SJ, Cohen FE, Prusiner SB (2001) Binding of neural cell adhesion molecules (N-CAMs) to the cellular prion protein. J Mol Biol 314:1209-1225
Zanata SM, Lopes MH, Mercadante AF, Hajj GN, Chiarini LB, Nomizo R, Freitas AR, Cabral AL, Lee KS, Juliano MA, de Oliveira E, Jachieri SG, Burlingame A, Huang L, Linden R, Brentani RR, Martins VR (2002) Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection. EMBO J 21:3307-3316
Santuccione A, Sytnyk V, Leshchyns’ka I, Schachner M (2005) Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth. J Cell Biol 169:341-354
Hajj GN, Lopes MH, Mercadante AF, Veiga SS, da Silveira RB, Santos TG, Ribeiro KC, Juliano MA, Jacchieri SG, Zanata SM, Martins VR (2007) Cellular prion protein interaction with vitronectin supports axonal growth and is compensated by integrins. J Cell Sci 120:1915-1926
Kleene R, Loers G, Langer J, Frobert Y, Buck F, Schachner M (2007) Prion protein regulates glutamate-dependent lactate transport of astrocytes. J Neurosci 27:12331-12340
Korshunova I, Novitskaya V, Kiryushko D, Pedersen N, Kolkova K, Kropotova E, Mosevitsky M, Rayko M, Morrow JS, Ginzburg I, Berezin V, Bock E (2007) GAP-43 regulates NCAM-180-mediated neurite outgrowth. J Neurochem 100:1599-1612
Little EB, Edelman GM, Cunningham BA (1998) Palmitoylation of the cytoplasmic domain of the neural cell adhesion molecule N-CAM serves as an anchor to cellular membranes. Cell Adhes Commun 6:415-430
Bodrikov V, Leshchyns’ka I, Sytnyk V, Overvoorde J, den Hertog J, Schachner M (2005) RPTPα is essential for NCAM-mediated p59fyn activation and neurite elongation. J Cell Biol 168:127-139
Niethammer P, Delling M, Sytnyk V, Dityatev A, Fukami K, Schachner M (2002) Cosignaling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis. J Cell Biol 157:521-532
Chiarini LB, Freitas AR, Zanata SM, Brentani RR, Martins VR, Linden R (2002) Cellular prion protein transduces neuroprotective signals. EMBO J 21:3317-3326
Chen S, Mange A, Dong L, Lehmann S, Schachner M (2003) Prion protein as trans-interacting partner for neurons is involved in neurite outgrowth and neuronal survival. Mol Cell Neurosci 22:227-233
Coitinho AS, Lopes MH, Hajj GN, Rossato JI, Freitas AR, Castro CC, Cammarota M, Brentani RR, Izquierdo I, Martins VR (2007) Short-term memory formation and long-term memory consolidation are enhanced by cellular prion association to stress-inducible protein 1. Neurobiol Dis 26:282-290
Solforosi L, Criado JR, McGavern DB, Wirz S, Sanchez-Alavez M, Sugama S, DeGiorgio LA, Volpe BT, Wiseman E, Abalos G, Masliah E, Gilden D, Oldstone MB, Conti B, Williamson RA (2004) Cross-linking cellular prion protein triggers neuronal apoptosis in vivo. Science 303:1514-1516
Novitskaya V, Bocharova OV, Bronstein I, Baskakov IV (2006) Amyloid fibrils of mammalian prion protein are highly toxic to cultured cells and primary neurons. J Biol Chem 281:13828-13836
Furley AJ, Morton SB, Manalo D, Karagogeos D, Dodd J, Jessell TM (1990) The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. Cell 61:157-170
Denaxa M, Chan CH, Schachner M, Parnavelas JG, Karagogeos D (2001) The adhesion molecule TAG-1 mediates the migration of cortical interneurons from the ganglionic eminence along the corticofugal fiber system. Development 128:4635-4644
Freigang J, Proba K, Leder L, Diederichs K, Sonderegger P, Welte W (2000) The crystal structure of the ligand binding module of axonin-1/TAG-1 suggests a zipper mechanism for neural cell adhesion. Cell 101:425-433
Kunz B, Lierheimer R, Rader C, Spirig M, Ziegler U, Sonderegger P (2002) Axonin-1/TAG-1 mediates cell-cell adhesion by a cis-assisted trans-interaction. J Biol Chem 277:4551-4557
Mortl M, Sonderegger P, Diederichs K, Welte W (2007) The crystal structure of the ligand-binding module of human TAG-1 suggests a new mode of homophilic interaction. Protein Sci 16:2174-2183
Milev P, Maurel P, Haring M, Margolis RK, Margolis RU (1996) TAG-1/axonin-1 is a high-affinity ligand of neurocan, phosphacan/protein-tyrosine phosphatase-ζ/β and N-CAM. J Biol Chem 271:15716-15723
Pavlou O, Theodorakis K, Falk J, Kutsche M, Schachner M, Faivre-Sarrailh C, Karagogeos D (2002) Analysis of interactions of the adhesion molecule TAG-1 and its domains with other immunoglobulin superfamily members. Mol Cell Neurosci 20:367-381
Malhotra JD, Tsiotra P, Karagogeos D, Hortsch M (1998) Cis-activation of L1-mediated ankyrin recruitment by TAG-1 homophilic cell adhesion. J Biol Chem 273:33354-33359
Morales G, Hubert M, Brummendorf T, Treubert U, Tarnok A, Schwarz U, Rathjen FG (1993) Induction of axonal growth by heterophilic interactions between the cell surface recognition proteins F11 and Nr-CAM/Bravo. Neuron 11:1113-1122
Volkmer H, Zacharias U, Norenberg U, Rathjen FG (1998) Dissection of complex molecular interactions of neurofascin with axonin-1, F11, and tenascin-R, which promote attachment and neurite formation of tectal cells. J Cell Biol 142:1083-1093
Felsenfeld DP, Hynes MA, Skoler KM, Furley AJ, Jessell TM (1994) TAG-1 can mediate homophilic binding, but neurite outgrowth on TAG-1 requires an L1-like molecule and β1 integrins. Neuron 12:675-690
Kunz S, Spirig M, Ginsburg C, Buchstaller A, Berger P, Lanz R, Rader C, Vogt L, Kunz B, Sonderegger P (1998) Neurite fasciculation mediated by complexes of axonin-1 and Ng cell adhesion molecule. J Cell Biol 143:1673-1690
Schurmann G, Haspel J, Grumet M, Erickson HP (2001) Cell adhesion molecule L1 in folded (horseshoe) and extended conformations. Mol Biol Cell 12:1765-1773
Haspel J, Grumet M (2003) The L1CAM extracellular region: a multi-domain protein with modular and cooperative binding modes. Front Biosci 8:s1210-s1225
Brummendorf T, Hubert M, Treubert U, Leuschner R, Tarnok A, Rathjen FG (1993) The axonal recognition molecule F11 is a multifunctional protein: specific domains mediate interactions with Ng-CAM and restrictin. Neuron 10:711-727
Kadmon G, von Bohlen und Halbach F, Horstkorte R, Eckert M, Altevogt P, Schachner M (1995) Evidence for cis interaction and cooperative signalling by the heat-stable antigen nectadrin (murine CD24) and the cell adhesion molecule L1 in neurons. Eur J Neurosci 7:993-1004
Falk J, Bonnon C, Girault JA, Faivre-Sarrailh C (2002) F3/contactin, a neuronal cell adhesion molecule implicated in axogenesis and myelination. Biol Cell 94:327-334
Kulahin N, Li S, Hinsby A, Kiselyov V, Berezin V, Bock E (2007) Fibronectin type III (FN3) modules of the neuronal cell adhesion molecule L1 interact directly with the fibroblast growth factor (FGF) receptor. Mol Cell Neurosci 37:528-536
Horstkorte R, Schachner M, Magyar JP, Vorherr T, Schmitz B (1993) The fourth immunoglobulin-like domain of NCAM contains a carbohydrate recognition domain for oligomannosidic glycans implicated in association with L1 and neurite outgrowth. J Cell Biol 121:1409-1421
Heiland PC, Griffith LS, Lange R, Schachner M, Hertlein B, Traub O, Schmitz B (1998) Tyrosine and serine phosphorylation of the neural cell adhesion molecule L1 is implicated in its oligomannosidic glycan dependent association with NCAM and neurite outgrowth. Eur J Cell Biol 75:97-106
Kadmon G, Kowitz A, Altevogt P, Schachner M (1990) The neural cell adhesion molecule N-CAM enhances L1-dependent cell-cell interactions. J Cell Biol 110:193-208
Kadmon G, Kowitz A, Altevogt P, Schachner M (1990) Functional cooperation between the neural adhesion molecules L1 and N-CAM is carbohydrate dependent. J Cell Biol 110:209-218
Kristiansen LV, Marques FA, Soroka V, Ronn LC, Kiselyov V, Pedersen N, Berezin V, Bock E (1999) Homophilic NCAM interactions interfere with L1 stimulated neurite outgrowth. FEBS Lett 464:30-34
Kristiansen G, Sammar M, Altevogt P (2004) Tumour biological aspects of CD24, a mucin-like adhesion molecule. J Mol Histol 35:255-262
Kleene R, Yang H, Kutsche M, Schachner M (2001) The neural recognition molecule L1 is a sialic acid-binding lectin for CD24, which induces promotion and inhibition of neurite outgrowth. J Biol Chem 276:21656-21663
Sammar M, Aigner S, Altevogt P (1997) Heat-stable antigen (mouse CD24) in the brain: dual but distinct interaction with P-selectin and L1. Biochim Biophys Acta 1337:287-294
Liakhovich AV, Aksenov NL (2000) Topography of cell ahesion molecules CD9, CD24, L1 and N-CAM on the surface of neuroblastoma cells studied using chemical cross linking. Tsitologiia 42:399-403
Calaora V, Chazal G, Nielsen PJ, Rougon G, Moreau H (1996) mCD24 expression in the developing mouse brain and in zones of secondary neurogenesis in the adult. Neuroscience 73:581-594
Bandtlow CE, Zimmermann DR (2000) Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol Rev 80:1267-1290
Cole GJ, Schubert D, Glaser L (1985) Cell-substratum adhesion in chick neural retina depends upon protein-heparan sulfate interactions. J Cell Biol 100:1192-1199
Bjork I, Lindahl U (1982) Mechanism of the anticoagulant action of heparin. Mol Cell Biochem 48:161-182
Cole GJ, Glaser L (1986) A heparin-binding domain from N-CAM is involved in neural cell-substratum adhesion. J Cell Biol 102:403-412
Cole GJ, Loewy A, Cross NV, Akeson R, Glaser L (1986) Topographic localization of the heparin-binding domain of the neural cell adhesion molecule N-CAM. J Cell Biol 103:1739-1744
Cole GJ, Akeson R (1989) Identification of a heparin binding domain of the neural cell adhesion molecule N-CAM using synthetic peptides. Neuron 2:1157-1165
Reyes AA, Akeson R, Brezina L, Cole GJ (1990) Structural requirements for neural cell adhesion molecule-heparin interaction. Cell Regul 1:567-576
Kiselyov VV, Berezin V, Maar TE, Soroka V, Edvardsen K, Schousboe A, Bock E (1997) The first immunoglobulin-like neural cell adhesion molecule (NCAM) domain is involved in double-reciprocal interaction with the second immunoglobulin-like NCAM domain and in heparin binding. J Biol Chem 272:10125-10134
Frei T, von Bohlen und Halbach F, Wille W, Schachner M (1992) Different extracellular domains of the neural cell adhesion molecule (N-CAM) are involved in different functions. J Cell Biol 118:177-194
Kulahin N, Rudenko O, Kiselyov V, Poulsen FM, Berezin V, Bock E (2005) Modulation of the homophilic interaction between the first and second Ig modules of neural cell adhesion molecule by heparin. J Neurochem 95:46-55
Nybroe O, Moran N, Bock E (1989) Equilibrium binding analysis of neural cell adhesion molecule binding to heparin. J Neurochem 52:1947-1949
Herndon ME, Stipp CS, Lander AD (1999) Interactions of neural glycosaminoglycans and proteoglycans with protein ligands: assessment of selectivity, heterogeneity and the participation of core proteins in binding. Glycobiology 9:143-155
Jensen PH, Soroka V, Thomsen NK, Ralets I, Berezin V, Bock E, Poulsen FM (1999) Structure and interactions of NCAM modules 1 and 2, basic elements in neural cell adhesion. Nat Struct Biol 6:486-493
Moran N, Bock E (1988) Characterization of the kinetics of neural cell adhesion molecule homophilic binding. FEBS Lett 242:121-124
Burg MA, Halfter W, Cole GJ (1995) Analysis of proteoglycan expression in developing chicken brain: characterization of a heparan sulfate proteoglycan that interacts with the neural cell adhesion molecule. J Neurosci Res 41:49-64
Storms SD, Kim AC, Tran BH, Cole GJ, Murray BA (1996) NCAM-mediated adhesion of transfected cells to agrin. Cell Adhes Commun 3:497-509
Storms SD, Anvekar VM, Adams LD, Murray BA (1996) Heterophilic NCAM-mediated cell adhesion to proteoglycans from chick embryonic brain membranes. Exp Cell Res 223:385-394
Storms SD, Rutishauser U (1998) A role for polysialic acid in neural cell adhesion molecule heterophilic binding to proteoglycans. J Biol Chem 273:27124-27129
Prag S, Lepekhin EA, Kolkova K, Hartmann-Petersen R, Kawa A, Walmod PS, Belman V, Gallagher HC, Berezin V, Bock E, Pedersen N (2002) NCAM regulates cell motility. J Cell Sci 115:283-292
Dityatev A, Dityateva G, Sytnyk V, Delling M, Toni N, Nikonenko I, Muller D, Schachner M (2004) Polysialylated neural cell adhesion molecule promotes remodeling and formation of hippocampal synapses. J Neurosci 24:9372-9382
Kasper C, Rasmussen H, Kastrup JS, Ikemizu S, Jones EY, Berezin V, Bock E, Larsen IK (2000) Structural basis of cell-cell adhesion by NCAM. Nat Struct Biol 7:389-393
Cole GJ, Loewy A, Glaser L (1986) Neuronal cell-cell adhesion depends on interactions of N-CAM with heparin-like molecules. Nature 320:445-447
Doherty P, Barton CH, Dickson G, Seaton P, Rowett LH, Moore SE, Gower HJ, Walsh FS (1989) Neuronal process outgrowth of human sensory neurons on monolayers of cells transfected with cDNAs for five human N-CAM isoforms. J Cell Biol 109:789-798
Doherty P, Fruns M, Seaton P, Dickson G, Barton CH, Sears TA, Walsh FS (1990) A threshold effect of the major isoforms of NCAM on neurite outgrowth. Nature 343:464-466
Soroka V, Kolkova K, Kastrup JS, Diederichs K, Breed J, Kiselyov VV, Poulsen FM, Larsen IK, Welte W, Berezin V, Bock E, Kasper C (2003) Structure and interactions of NCAM Ig1-2-3 suggest a novel zipper mechanism for homophilic adhesion. Structure 11:1291-1301
Kroger S, Schroder JE (2002) Agrin in the developing CNS: new roles for a synapse organizer. News Physiol Sci 17:207-212
Ngo ST, Noakes PG, Phillips WD (2007) Neural agrin: a synaptic stabiliser. Int J Biochem Cell Biol 39:863-867
Cotman SL, Halfter W, Cole GJ (1999) Identification of extracellular matrix ligands for the heparan sulfate proteoglycan agrin. Exp Cell Res 249:54-64
Bezakova G, Ruegg MA (2003) New insights into the roles of agrin. Nat Rev Mol Cell Biol 4:295-308
Bowe MA, Deyst KA, Leszyk JD, Fallon JR (1994) Identification and purification of an agrin receptor from Torpedo postsynaptic membranes: a heteromeric complex related to the dystroglycans. Neuron 12:1173-1180
Bixby JL, Baerwald-De la Torre K, Wang C, Rathjen FG, Ruegg MA (2002) A neuronal inhibitory domain in the N-terminal half of agrin. J Neurobiol 50:164-179
Martin PT, Sanes JR (1997) Integrins mediate adhesion to agrin and modulate agrin signaling. Development 124:3909-3917
Aricescu AR, McKinnell IW, Halfter W, Stoker AW (2002) Heparan sulfate proteoglycans are ligands for receptor protein tyrosine phosphatase σ. Mol Cell Biol 22:1881-1892
Denzer AJ, Brandenberger R, Gesemann M, Chiquet M, Ruegg MA (1997) Agrin binds to the nerve-muscle basal lamina via laminin. J Cell Biol 137:671-683
Daggett DF, Cohen MW, Stone D, Nikolics K, Rauvala H, Peng HB (1996) The role of an agrin-growth factor interaction in ACh receptor clustering. Mol Cell Neurosci 8:272-285
Meier T, Masciulli F, Moore C, Schoumacher F, Eppenberger U, Denzer AJ, Jones G, Brenner HR (1998) Agrin can mediate acetylcholine receptor gene expression in muscle by aggregation of muscle-derived neuregulins. J Cell Biol 141:715-726
Cotman SL, Halfter W, Cole GJ (2000) Agrin binds to β-amyloid (Aβ), accelerates Aβ fibril formation, and is localized to Aβ deposits in Alzheimer’s disease brain. Mol Cell Neurosci 15:183-198
Cole GJ, Burg M (1989) Characterization of a heparan sulfate proteoglycan that copurifies with the neural cell adhesion molecule. Exp Cell Res 182:44-60
Marneros AG, Olsen BR (2001) The role of collagen-derived proteolytic fragments in angiogenesis. Matrix Biol 20:337-345
Halfter W, Dong S, Schurer B, Cole GJ (1998) Collagen XVIII is a basement membrane heparan sulfate proteoglycan. J Biol Chem 273:25404-25412
Sasaki T, Hohenester E, Timpl R (2002) Structure and function of collagen-derived endostatin inhibitors of angiogenesis. IUBMB Life 53:77-84
Sasaki T, Fukai N, Mann K, Gohring W, Olsen BR, Timpl R (1998) Structure, function and tissue forms of the C-terminal globular domain of collagen XVIII containing the angiogenesis inhibitor endostatin. EMBO J 17:4249-4256
Sasaki T, Larsson H, Tisi D, Claesson-Welsh L, Hohenester E, Timpl R (2000) Endostatins derived from collagens XV and XVIII differ in structural and binding properties, tissue distribution and anti-angiogenic activity. J Mol Biol 301:1179-1190
Karumanchi SA, Jha V, Ramchandran R, Karihaloo A, Tsiokas L, Chan B, Dhanabal M, Hanai JI, Venkataraman G, Shriver Z, Keiser N, Kalluri R, Zeng H, Mukhopadhyay D, Chen RL, Lander AD, Hagihara K, Yamaguchi Y, Sasisekharan R, Cantley L, Sukhatme VP (2001) Cell surface glypicans are low-affinity endostatin receptors. Mol Cell 7:811-822
Rehn M, Veikkola T, Kukk-Valdre E, Nakamura H, Ilmonen M, Lombardo C, Pihlajaniemi T, Alitalo K, Vuori K (2001) Interaction of endostatin with integrins implicated in angiogenesis. Proc Natl Acad Sci USA 98:1024-1029
Dong S, Cole GJ, Halfter W (2003) Expression of collagen XVIII and localization of its glycosaminoglycan attachment sites. J Biol Chem 278:1700-1707
Grumet M, Flaccus A, Margolis RU (1993) Functional characterization of chondroitin sulfate proteoglycans of brain: interactions with neurons and neural cell adhesion molecules. J Cell Biol 120:815-824
Friedlander DR, Milev P, Karthikeyan L, Margolis RK, Margolis RU, Grumet M (1994) The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth. J Cell Biol 125:669-680
Milev P, Friedlander DR, Sakurai T, Karthikeyan L, Flad M, Margolis RK, Grumet M, Margolis RU (1994) Interactions of the chondroitin sulfate proteoglycan phosphacan, the extracellular domain of a receptor-type protein tyrosine phosphatase, with neurons, glia, and neural cell adhesion molecules. J Cell Biol 127:1703-1715
Milev P, Meyer-Puttlitz B, Margolis RK, Margolis RU (1995) Complex-type asparagine-linked oligosaccharides on phosphacan and protein-tyrosine phosphatase-ζ/β mediate their binding to neural cell adhesion molecules and tenascin. J Biol Chem 270:24650-24653
Retzler C, Gohring W, Rauch U (1996) Analysis of neurocan structures interacting with the neural cell adhesion molecule N-CAM. J Biol Chem 271:27304-27310
Probstmeier R, Kuhn K, Schachner M (1989) Binding properties of the neural cell adhesion molecule to different components of the extracellular matrix. J Neurochem 53:1794-1801
Kallapur SG, Akeson RA (1992) The neural cell adhesion molecule (NCAM) heparin binding domain binds to cell surface heparan sulfate proteoglycans. J Neurosci Res 33:538-548
Bovolenta P, Fernaud-Espinosa I (2000) Nervous system proteoglycans as modulators of neurite outgrowth. Prog Neurobiol 61:113-132
Retzler C, Wiedemann H, Kulbe G, Rauch U (1996) Structural and electron microscopic analysis of neurocan and recombinant neurocan fragments. J Biol Chem 271:17107-17113
Grumet M, Milev P, Sakurai T, Karthikeyan L, Bourdon M, Margolis RK, Margolis RU (1994) Interactions with tenascin and differential effects on cell adhesion of neurocan and phosphacan, two major chondroitin sulfate proteoglycans of nervous tissue. J Biol Chem 269:12142-12146
Milev P, Chiba A, Haring M, Rauvala H, Schachner M, Ranscht B, Margolis RK, Margolis RU (1998) High affinity binding and overlapping localization of neurocan and phosphacan/protein-tyrosine phosphatase-ζ/β with tenascin-R, amphoterin, and the heparin-binding growth-associated molecule. J Biol Chem 273:6998-7005
Feng K, Arnold-Ammer I, Rauch U (2000) Neurocan is a heparin binding proteoglycan. Biochem Biophys Res Commun 272:449-455
Li H, Leung TC, Hoffman S, Balsamo J, Lilien J (2000) Coordinate regulation of cadherin and integrin function by the chondroitin sulfate proteoglycan neurocan. J Cell Biol 149:1275-1288
Milev P, Monnerie H, Popp S, Margolis RK, Margolis RU (1998) The core protein of the chondroitin sulfate proteoglycan phosphacan is a high-affinity ligand of fibroblast growth factor-2 and potentiates its mitogenic activity. J Biol Chem 273:21439-21442
Maeda N, Nishiwaki T, Shintani T, Hamanaka H, Noda M (1996) 6B4 proteoglycan/phosphacan, an extracellular variant of receptor-like protein-tyrosine phosphatase ζ/RPTPβ binds pleiotrophin/heparin-binding growth-associated molecule (HB-GAM). J Biol Chem 271:21446-21452
Peles E, Nativ M, Campbell PL, Sakurai T, Martinez R, Lev S, Clary DO, Schilling J, Barnea G, Plowman GD, Grumet M, Schlessinger J (1995) The carbonic anhydrase domain of receptor tyrosine phosphatase β is a functional ligand for the axonal cell recognition molecule contactin. Cell 82:251-260
Maeda N, Ichihara-Tanaka K, Kimura T, Kadomatsu K, Muramatsu T, Noda M (1999) A receptor-like protein-tyrosine phosphatase PTPζ/RPTPβ binds a heparin-binding growth factor midkine: involvement of arginine 78 of midkine in the high affinity binding to PTPζ. J Biol Chem 274:12474-12479
Rauch U, Feng K, Zhou XH (2001) Neurocan: a brain chondroitin sulfate proteoglycan. Cell Mol Life Sci 58:1842-1856
Viapiano MS, Matthews RT (2006) From barriers to bridges: chondroitin sulfate proteoglycans in neuropathology. Trends Mol Med 12:488-496
Barnea G, Grumet M, Milev P, Silvennoinen O, Levy JB, Sap J, Schlessinger J (1994) Receptor tyrosine phosphatase β is expressed in the form of proteoglycan and binds to the extracellular matrix protein tenascin. J Biol Chem 269:14349-14352
Martini R, Schachner M (1986) Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and MAG) and their shared carbohydrate epitope and myelin basic protein in developing sciatic nerve. J Cell Biol 103:2439-2448
Martini R, Schachner M (1988) Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and myelin-associated glycoprotein) in regenerating adult mouse sciatic nerve. J Cell Biol 106:1735-1746
Probstmeier R, Fahrig T, Spiess E, Schachner M (1992) Interactions of the neural cell adhesion molecule and the myelin-associated glycoprotein with collagen type I: involvement in fibrillogenesis. J Cell Biol 116:1063-1070
Sheard P, Paul A, Duxson M (2002) Intramuscular force transmission. Adv Exp Med Biol 508:495-499
Luckenbill-Edds L (1997) Laminin and the mechanism of neuronal outgrowth. Brain Res Brain Res Rev 23:1-27
Lafon M (2005) Rabies virus receptors. J Neurovirol 11:82-87
Finke S, Conzelmann KK (2005) Replication strategies of rabies virus. Virus Res 111:120-131
World Health Organization (2006) Rabies (WHO Fact Sheet No. 99). World Health Organization, Geneva. www.who.int/mediacentre/factsheets/fs099/en/ (accessed 29 Feb 2008)
Thoulouze MI, Lafage M, Schachner M, Hartmann U, Cremer H, Lafon M (1998) The neural cell adhesion molecule is a receptor for rabies virus. J Virol 72:7181-7190
Hotta K, Motoi Y, Okutani A, Kaku Y, Noguchi A, Inoue S, Yamada A (2007) Role of GPI-anchored NCAM-120 in rabies virus infection. Microbes Infect 9:167-174
Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, Hong JS, Horwitz MS, Crowell RL, Finberg RW (1997) Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320-1323
Geraghty RJ, Krummenacher C, Cohen GH, Eisenberg RJ, Spear PG (1998) Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 280:1618-1620
Warner MS, Geraghty RJ, Martinez WM, Montgomery RI, Whitbeck JC, Xu R, Eisenberg RJ, Cohen GH, Spear PG (1998) A cell surface protein with herpesvirus entry activity (HveB) confers susceptibility to infection by mutants of herpes simplex virus type 1, herpes simplex virus type 2, and pseudorabies virus. Virology 246:179-189
Koike S, Ise I, Sato Y, Yonekawa H, Gotoh O, Nomoto A (1992) A second gene for the African green monkey poliovirus receptor that has no putative N-glycosylation site in the functional N-terminal immunoglobulin-like domain. J Virol 66:7059-7066
Wang J (2002) Protein recognition by cell surface receptors: physiological receptors versus virus interactions. Trends Biochem Sci 27:122-126
DiMilla PA, Barbee K, Lauffenburger DA (1991) Mathematical model for the effects of adhesion and mechanics on cell migration speed. Biophys J 60:15-37
Palecek SP, Loftus JC, Ginsberg MH, Lauffenburger DA, Horwitz AF (1997) Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385:537-540
Fujimoto I, Bruses JL, Rutishauser U (2001) Regulation of cell adhesion by polysialic acid: effects on cadherin, immunoglobulin cell adhesion molecule, and integrin function and independence from neural cell adhesion molecule binding or signaling activity. J Biol Chem 276:31745-31751
Johnson CP, Fujimoto I, Rutishauser U, Leckband DE (2005) Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion. J Biol Chem 280:137-145
Ingber DE (2003) Tensegrity I: cell structure and hierarchical systems biology. J Cell Sci 116:1157-1173
Ingber DE (2003) Tensegrity II: how structural networks influence cellular information processing networks. J Cell Sci 116:1397-1408
Ingber DE (2006) Mechanical control of tissue morphogenesis during embryological development. Int J Dev Biol 50:255-266
Pollerberg GE, Burridge K, Krebs KE, Goodman SR, Schachner M (1987) The 180-kD component of the neural cell adhesion molecule N-CAM is involved in cell-cell contacts and cytoskeleton-membrane interactions. Cell Tissue Res 250:227-236
Minana R, Duran JM, Tomas M, Renau-Piqueras J, Guerri C (2001) Neural cell adhesion molecule is endocytosed via a clathrin-dependent pathway. Eur J Neurosci 13:749-756
Diestel S, Schaefer D, Cremer H, Schmitz B (2007) NCAM is ubiquitylated, endocytosed and recycled in neurons. J Cell Sci 120:4035-4049
Foley AG, Hartz BP, Gallagher HC, Ronn LC, Berezin V, Bock E, Regan CM (2000) A synthetic peptide ligand of neural cell adhesion molecule (NCAM) IgI domain prevents NCAM internalization and disrupts passive avoidance learning. J Neurochem 74:2607-2613
Garwood J, Heck N, Reichardt F, Faissner A (2003) Phosphacan short isoform, a novel non-proteoglycan variant of phosphacan/receptor protein tyrosine phosphatase-β interacts with neuronal receptors and promotes neurite outgrowth. J Biol Chem 278:24164-24173
Rader C, Stoeckli ET, Ziegler U, Osterwalder T, Kunz B, Sonderegger P (1993) Cell-cell adhesion by homophilic interaction of the neuronal recognition molecule axonin-1. Eur J Biochem 215:133-141
Miura M, Asou H, Kobayashi M, Uyemura K (1992) Functional expression of a full-length cDNA coding for rat neural cell adhesion molecule L1 mediates homophilic intercellular adhesion and migration of cerebellar neurons. J Biol Chem 267:10752-10758
Mauro VP, Krushel LA, Cunningham BA, Edelman GM (1992) Homophilic and heterophilic binding activities of Nr-CAM, a nervous system cell adhesion molecule. J Cell Biol 119:191-202
Pruss T, Niere M, Kranz EU, Volkmer H (2004) Homophilic interactions of chick neurofascin in trans are important for neurite induction. Eur J Neurosci 20:3184-3188
Acknowledgments
The financial support from “Snedkermester Sophus Jacobsen og hustru Astrid Jacobsens Fond”, “Det Lægevidenskabelige Fakultets Fond for videnskabeligt ansatte kandidater og studerende ved Københavns Universitet”, ENKAM Pharmaceuticals A/S, and the Graduate School of Neuroscience, University of Copenhagen, and the EU-funded brain research consortium PROMEMORIA (LSHM-CT-2005-512012) is gratefully acknowledged.
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Nielsen, J., Kulahin, N., Walmod, P.S. (2010). Extracellular Protein Interactions Mediated by the Neural Cell Adhesion Molecule, NCAM: Heterophilic Interactions Between NCAM and Cell Adhesion Molecules, Extracellular Matrix Proteins, and Viruses. In: Berezin, V. (eds) Structure and Function of the Neural Cell Adhesion Molecule NCAM. Advances in Experimental Medicine and Biology, vol 663. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-1170-4_2
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