Synapsin I is an oligomannose-carrying glycoprotein, acts as an oligomannose-binding lectin, and promotes neurite outgrowth and neuronal survival when released via glia-derived exosomes

Journal of Neuroscience

Volumn 31, Issue 20, 2011, Pages 7275-7290

  Wang, Shiwei ^a,c   Cesca, Fabrizia ^b   Loers, Gabriele ^a   Schweizer, Michaela ^a   Buck, Friedrich ^a   Benfenati, Fabio ^b   Schachner, Melitta ^a,d,e   Kleene, Ralf ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^c DALIAN MEDICAL UNIVERSITY   (China)

^d RUTGERS UNIVERSITY   (United States)

^e SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

SYNAPSIN I;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL ADHESION; CELL DEATH; CELL SURFACE; CELL SURVIVAL; CONTROLLED STUDY; EXOSOME; GLIA CELL; HIPPOCAMPUS; MOUSE; NERVE CELL; NERVE FIBER GROWTH; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN TARGETING;

EID: 79956324370     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6476-10.2011     Document Type: Article

References (53)

1. Antonicek H, Schachner M (1988) The adhesion molecule on glia (AMOG) incorporated into lipid vesicles binds to subpopulations of neurons. J Neurosci 8:2961-2966.
2. Bähler M, Greengard P (1987) Synapsin I bundles F-actin in a phosphorylation-dependent manner. Nature 326:704-707.
3. Bergles DE, Jabs R, Steinhäuser C (2010) Neuron-glia synapses in the brain. Brain Res Rev 63:130-137.
4. Bustos R, Kolen ER, Braiterman L, Baines AJ, Gorelick FS, Hubbard AL (2001) Synapsin I is expressed in epithelial cells: localization to a unique trans-Golgi compartment. J Cell Sci 114:3695-3704.
5. Candiani S, Moronti L, Pennati R, De Bernardi F, Benfenati F, Pestarino M (2010) The synapsin gene family in basal chordates: evolutionary perspectives in metazoans. BMC Evol Biol 10:32.
6. Cesca F, Baldelli P, Valtorta F, Benfenati F (2010) The synapsins: key actors of synapse function and plasticity. Prog Neurobiol 91:313-348.
7. Chandrasekaran S, Dean JW 3rd, Giniger MS, Tanzer ML (1991) Laminin carbohydrates are implicated in cell signaling. J Cell Biochem 46:115-124.
8. Chen S, Mantei N, Dong L, Schachner M (1999) Prevention of neuronal cell death by neural adhesion molecules L1 and CHL1. J Neurobiol 38:428-439.
9. Chin LS, Li L, Ferreira A, Kosik KS, Greengard P (1995) Impairment of axonal development and of synaptogenesis in hippocampal neurons of synapsin I-deficient mice. Proc Natl Acad Sci U S A 92:9230-9234.
10. Corradi A, Zanardi A, Giacomini C, Onofri F, Valtorta F, Zoli M, Benfenati F (2008) Synapsin-I-and synapsin-II-null mice display an increased agedependent cognitive impairment. J Cell Sci 121:3042-3051.
11. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Kraemer P, Scheff S, Barthels D, Rajewsky K, Wille W (1994) Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367:455-459.
12. De Camilli P, Cameron R, Greengard P (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. I. Its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections. J Cell Biol 96:1337-1354.
13. Fahrig T, Schmitz B, Weber D, Kücherer-Ehret A, Faissner A, Schachner M (1990) Two monoclonal antibodies recognizing carbohydrate epitopes on neural adhesion molecules interfere with cell interactions. Eur J Neurosci 2:153-161.
14. Fassio A, Merlo D, Mapelli J, Menegon A, Corradi A, Mete M, Zappettini S, Bonanno G, Valtorta F, D'Angelo E, Benfenati F (2006) The synapsin domain E accelerates the exoendocytotic cycle of synaptic vesicles in cerebellar Purkinje cells. J Cell Sci 119:4257-4268.
15. Fornasiero EF, Bonanomi D, Benfenati F, Valtorta F (2010) The role of synapsins in neuronal development. Cell Mol Life Sci 67:1383-1396.
16. Fu SC, Gurd JW (1983) Developmental changes in the oligosaccharide composition of synaptic junctional glycoproteins. J Neurochem 41:1726-1734.
17. Gitler D, Takagishi Y, Feng J, Ren Y, Rodriguiz RM, Wetsel WC, Greengard P, Augustine GJ (2004) Different presynaptic roles of synapsins at excitatory and inhibitory synapses. J Neurosci 24:11368-11380.
18. 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.
19. Heller M, von der Ohe M, Kleene R, Mohajeri MH, Schachner M (2003) The immunoglobulin-superfamily molecule basigin is a binding protein for oligomannosidic carbohydrates: an anti-idiotypic approach. J Neurochem 84:557-565.
20. Hilfiker S, Schweizer FE, Kao HT, Czernik AJ, Greengard P, Augustine GJ (1998) Two sites of action for synapsin domain E in regulating neurotransmitter release. Nat Neurosci 1:29-35.
21. 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.
22. Husmann K, Faissner A, Schachner M (1992) Tenascin promotes cerebellar granule cell migration and neurite outgrowth by different domains in the fibronectin type III repeats. J Cell Biol 116:1475-1486.
23. Irwin A, Walz W (1999) Spreading depression waves as mediators of secondary injury and of protective mechanisms. In: Cerebral ischemia (Walz W, ed), pp 35-44Totowa, NJ: Humana.
24. Johnson MA, Rotondo A, Pinto BM (2002) NMR studies of the antibodybound conformation of a carbohydrate-mimetic peptide. Biochemistry 41:2149-2157.
25. Kaech S, Banker G (2006) Culturing hippocampal neurons. Nat Protoc 1:2406-2415.
26. Kao HT, Porton B, Hilfiker S, Stefani G, Pieribone VA, DeSalle R, Greengard P (1999) Molecular evolution of the synapsin gene family. J Exp Zool 285:360-377.
27. Kleene R, Schachner M (2004) Glycans and neural cell interactions. Nat Rev Neurosci 5:195-208.
28. 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.
29. 2+/calmodulin-dependent protein kinase II in pancreatic beta TC3 cells: synapsin I is not associated with insulin secretory granules. Diabetes 48:499-506.
30. Kücherer A, Faissner A, Schachner M (1987) The novel carbohydrate epitope L3 is shared by some neural cell adhesion molecules. J Cell Biol 104:1597-1602.
31. Lakkaraju A, Rodriguez-Boulan E (2008) Itinerant exosomes: emerging roles in cell and tissue polarity. Trends Cell Biol 18:199-209.
32. Lauritzen M, Dreier JP, Fabricius M, Hartings JA, Graf R, Strong AJ (2011) Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury. J Cereb Blood Flow Metab 31:17-35.
33. Lüthl A, Laurent JP, Figurov A, Muller D, Schachner M (1994) Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM. Nature 372:777-779.
34. Maienschein V, Marxen M, Volknandt W, Zimmermann H (1999) A plethora of presynaptic proteins associated with ATP-storing organelles in cultured astrocytes. Glia 26:233-244.
35. 2+/calmodulin-dependent protein kinase II and synapsin I-like protein in mouse insulinoma MIN6 cells. Endocrinology 136:3784-3793.
36. Monzavi-Karbassi B, Cunto-Amesty G, Luo P, Kieber-Emmons T (2002) Peptide mimotopes as surrogate antigens of carbohydrates in vaccine discovery. Trends Biotechnol 20:207-214.
37. Murrey HE, Gama CI, Kalovidouris SA, Luo WI, Driggers EM, Porton B, Hsieh-Wilson LC (2006) Protein fucosylation regulates synapsin Ia/Ib expression and neuronal morphology in primary hippocampal neurons. Proc Natl Acad Sci U S A 103:21-26.
38. Pirofski LA (2001) Polysaccharides, mimotopes and vaccines for fungal and encapsulated pathogens. Trends Microbiol 9:445-451.
39. Ploughman M, Granter-Button S, Chernenko G, Tucker BA, Mearow KM, Corbett D (2005) Endurance exercise regimens induce differential effects on brain-derived neurotrophic factor, synapsin-I and insulin-like growth factor I after focal ischemia. Neuroscience 136:991-1001.
40. Revest JM, Kaouane N, Mondin M, Le Roux A, Rougé-Pont F, Vallée M, Barik J, Tronche F, Desmedt A, Piazza PV (2010) The enhancement of stressrelated memory by glucocorticoids depends on synapsin-Ia/Ib. Mol Psychiatry 15:1140-1151.
41. Romano C, Nichols RA, Greengard P, Greene LA (1987) Synapsin I in PC12 cells. I. Characterization of the phosphoprotein and effect of chronic NGF treatment. J Neurosci 7:1294-1299.
42. Schmid RS, Graff RD, Schaller MD, Chen S, Schachner M, Hemperly JJ, Maness PF (1999) NCAM stimulates the Ras-MAPK pathway and CREB phosphorylation in neuronal cells. J Neurobiol 38:542-558.
43. Schmidt JT, Schachner M (1998) Role for cell adhesion and glycosyl (HNK-1 and oligomannoside) recognition in the sharpening of the regenerating retinotectal projection in goldfish. J Neurobiol 37:659-671.
44. Simon-Haldi M, Mantei N, Franke J, Voshol H, Schachner M (2002) Identification of a peptide mimic of the L2/HNK-1 carbohydrate epitope. J Neurochem 83:1380-1388.
45. Simons M, Raposo G (2009) Exosomes-vesicular carriers for intercellular communication. Curr Opin Cell Biol 21:575-581.
46. Simpson RJ, Jensen SS, Lim JW (2008) Proteomic profiling of exosomes: current perspectives. Proteomics 8:4083-4099.
47. Spielhaupter C, Schätzl HM (2001) PrPC directly interacts with proteins involved in signaling pathways. J Biol Chem 276:44604-44612.
48. Stout C, Charles A (2003) Modulation of intercellular calcium signaling in astrocytes by extracellular calcium and magnesium. Glia 43:265-273.
49. Tanzer ML, Giniger MS, Chandrasekaran S (1993) Laminin oligosaccharides play a pivotal role in cell spreading. Symp Soc Exp Biol 47:147-154.
50. Tooze J, Hollinshead M, Fuller SD, Tooze SA, Huttner WB (1989) Morphological and biochemical evidence showing neuronal properties in At T-20 cells and their growth cones. Eur J Cell Biol 49:259-273.
51. Trotter J, Karram K, Nishiyama A (2010) NG2 cells: properties, progeny and origin. Brain Res Rev 63:72-82.
52. Wigley R, Butt AM (2009) Integration of NG2-glia (synantocytes) into the neuroglial network. Neuron Glia Biol 5:21-28.
53. Won CL, Oh YS (2000) cAMP-induced stellation in primary astrocyte cultures with regional heterogeneity. Brain Res 887:250-258.