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J. Biol. Chem., Vol. 281, Issue 24, 16377-16383, June 16, 2006

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A Protein in Crude Cytosol Regulates Glucose-6-phosphatase Activity in Crude Microsomes to Regulate Group Size in Dictyostelium^*

From the Howard Hughes Medical Institute and Department of Biochemistry and Cell Biology, Rice University, Houston, Texas 77005

Dictyostelium discoideum form groups of 2 x 10⁴ cells. The group size is regulated in part by a negative feedback pathway mediated by a secreted multipolypeptide complex called counting factor (CF). The CF signal transduction pathway involves CF-repressing internal glucose levels by increasing the K_m of glucose-6-phosphatase. Little is known about how this enzyme is regulated. Glucose-6-phosphatase is associated with microsomes in both Dictyostelium and mammals. We find that the activity of glucose-6-phosphatase in crude microsomes from cells with high, normal, or low CF activity had a negative correlation with the amount of CF present in these cell lines. In crude cytosols (supernatants from ultracentrifugation of cell lysates), the glucose-6-phosphatase activity had a positive correlation with CF accumulation. The crude cytosols were further fractionated into a fraction containing molecules greater than 10 kDa (S>10K) and molecules less than 10 KDa (S<10K). S>10K from wild-type cells strongly repressed the activity of glucose-6-phosphatase in wild-type microsomes, whereas S>10K from countin^– cells (cells with low CF activity) significantly increased the activity of glucose-6-phosphatase in wild-type microsomes by decreasing K_m. The regulatory activities in the wild-type and countin^– S>10Ks are heat-labile and protease-sensitive, suggesting that they are proteins. S<10K from both wild-type and countin^– cells did not significantly change glucose-6-phosphatase activity. Together, the data suggest that, as a part of a pathway modulating multicellular group size, CF regulates one or more proteins greater than 10 KDa in crude cytosol that affect microsome-associated glucose-6-phosphatase activity.

Received for publication, September 12, 2005 , and in revised form, March 10, 2006.

^* This work was supported by Robert A. Welch Foundation Grant C-1555. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ An investigator of the Howard Hughes Medical Institute. To whom correspondence should be addressed: Dept. of Biochemistry and Cell Biology, MS-140, Rice University, 6100 S. Main St., Houston, TX 77005-1892. Tel.: 713-348-4872; Fax: 713-348-5154; E-mail: richard{at}rice.edu.

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