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J. Biol. Chem., Vol. 278, Issue 19, 17573-17579, May 9, 2003

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A Winged Helix Forkhead (FOXD2) Tunes Sensitivity to cAMP in T Lymphocytes through Regulation of cAMP-dependent Protein Kinase RI^*

C. Christian Johansson^§, Maria K. Dahle^§, Sandra Rodrigo Blomqvist^¶, Line M. Grønning, Einar M. Aandahl, Sven Enerbäck^¶, and Kjetil Taskén

From the  Department of Medical Biochemistry, Institute of Basic Medical Sciences, University of Oslo, N-0317 Oslo, Norway and ^¶ Medical Genetics, Department of Medical Biochemistry, Göteborg University, SE-405 30 Göteborg, Sweden

Forkhead/winged helix (FOX) transcription factors are essential for control of the cell cycle and metabolism. Here, we show that spleens from Mf2/ (FOXD2/) mice have reduced mRNA (50%) and protein (35%) levels of the RI subunit of the cAMP-dependent protein kinase. In T cells from Mf2/ mice, reduced levels of RI translates functionally into ~2-fold less sensitivity to cAMP-mediated inhibition of proliferation triggered through the T cell receptor-CD3 complex. In Jurkat T cells, FOXD2 overexpression increased the endogenous levels of RI through induction of the RI1b promoter. FOXD2 overexpression also increased the sensitivity of the promoter to cAMP. Finally, co-expression experiments demonstrated that protein kinase B/Akt1 work together with FOXD2 to induce the RI1b promoter (10-fold) and increase endogenous RI protein levels further. Taken together, our data indicate that FOXD2 is a physiological regulator of the RI1b promoter in vivo working synergistically with protein kinase B to induce cAMP-dependent protein kinase RI expression, which increases cAMP sensitivity and sets the threshold for cAMP-mediated negative modulation of T cell activation.

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