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J Biol Chem, Vol. 274, Issue 30, 20916-20924, July 23, 1999
From the Pacific Northwest Research Institute, Seattle, Washington
98122 and the Departments of Pathobiology and Microbiology, University
of Washington, Seattle, Washington 98195
Differentiation and neuritogenesis of
mouse neuroblastoma Neuro2a cells are induced by exogenous ganglioside
but are not induced by nerve growth factor because its receptor is
absent in these cells. In view of the emerging concept of the
"glycosphingolipid-enriched domain" (GEM), we studied the mechanism
of the ganglioside effect, focusing on the structure and function of
such a domain. GEM in Neuro2a cells, separated as a low density
membrane fraction, contains essentially all glycosphingolipids and
sphingomyelin, together with five signal transducer molecules (c-Src,
Lyn, Csk, Rho A, Ha-Ras). 3H-Labeled
Il3NeuAc-LacCer (GM3), Gb4Cer (globoside), and
Il3NeuAc-Gg4Cer (GM1) added exogenously to cells were
incorporated and concentrated in the low density GEM fraction. In
contrast, more than 50% of glycerophospholipids and 30% of
cholesterol were found in the high density fraction.
3H-Labeled phosphatidylcholine added exogenously to cells
was incorporated exclusively in the high density fraction. c-Src, the
predominant signal transducer in the microdomain, was
coimmunoprecipitated with anti-GM3 antibody DH2 or with anti-Csk;
reciprocally, Csk was coimmunoprecipitated with anti-c-Src, indicating
a close association of GM3, c-Src, and Csk. Brief stimulation of an
isolated GEM fraction by the exogenous addition of GM3, but not
lactosylceramide, caused enhanced c-Src phosphorylation with a
concomitant decrease of Csk level in GEM. A decreased Csk/c-Src ratio
in GEM may cause activation of c-Src because Csk is a negative
regulator of c-Src. The effect of exogenous GM3 on c-Src activity was
also observed in intact Neuro2a cells. Activation of c-Src was followed
by rapid and prolonged (60 min) enhancement of mitogen-activated
protein kinase activity leading to neuritogenesis. Thus, the
ganglioside induction of neuritogenesis in Neuro2a cells is mediated by
GEM structure and function.
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