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J Biol Chem, Vol. 273, Issue 37, 23722-23728, September 11, 1998
From the Department of Biochemistry and Molecular Biology,
Georgetown University Medical Center, Washington, DC 20007 and
§ Department of Biochemistry and the Lucille P. Markey
Cancer Center, University of Kentucky Medical Center, Lexington,
Kentucky 40536-0084
Sphingosine-1-phosphate (SPP) is a
novel lipid messenger that has dual function. Intracellularly it
regulates proliferation and survival, and extracellularly, it is a
ligand for the G protein-coupled receptor Edg-1. Based on peptide
sequences obtained from purified rat kidney sphingosine kinase, the
enzyme that regulates SPP levels, we report here the cloning,
identification, and characterization of the first mammalian sphingosine
kinases (murine SPHK1a and SPHK1b). Sequence analysis indicates that
these are novel kinases, which are not similar to other known kinases,
and that they are evolutionarily conserved. Comparison with
Saccharomyces cerevisiae and Caenorhabditis
elegans sphingosine kinase sequences shows that several blocks
are highly conserved in all of these sequences. One of these blocks
contains an invariant, positively charged motif, GGKGK, which may be
part of the ATP binding site. From Northern blot analysis of multiple
mouse tissues, we observed that expression was highest in adult lung
and spleen, with barely detectable levels in skeletal muscle and liver.
Human embryonic kidney cells and NIH 3T3 fibroblasts transiently
transfected with either sphingosine kinase expression vectors had
marked increases (more than 100-fold) in sphingosine kinase activity.
The enzyme specifically phosphorylated
D-erythro-sphingosine and did not catalyze the
phosphorylation of phosphatidylinositol, diacylglycerol, ceramide,
D,L-threo-dihydrosphingosine or
N,N-dimethylsphingosine. The latter two
sphingolipids were competitive inhibitors of sphingosine kinase in the
transfected cells as was previously found with the purified rat kidney
enzyme. Transfected cells also had a marked increase in mass levels of
SPP with a concomitant decrease in levels of sphingosine and, to a
lesser extent, in ceramide levels. Our data suggest that sphingosine
kinase is a prototypical member of a new class of lipid kinases.
Cloning of sphingosine kinase is an important step in corroborating the
intracellular role of SPP as a second messenger.
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