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Figure 1.

Expression, localization and stimulus-dependent regulation of β2-syntrophin.

A) Confocal microscopy for β2-syntrophin in INS-1 cells and for GFP-β2-syntrophin or GFP in transfected INS-1 cells. β2-syntrophin was detected with the pan-syntrophin antibody 1351. White arrows indicate the enrichment of β2-syntrophin at the cell periphery. Bars: 5 µm. B) Western blots (WB) with anti-syntrophin or anti-GFP antibodies on extracts of INS-1 cells (left panel) or GFP-β2-syntrophin INS-1 cells (right panel). Cells were previously kept at rest (0 mM glucose, 5 mM KCl) or stimulated with high (25 mM) glucose and low (5 mM) KCl (HGLK), low (0 mM) glucose and high (55 mM) KCl (LGHK) or high glucose and high KCl (HGHK).

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Figure 2.

Insulin content and secretion of INS-1 cells in relation to β2-syntrophin expression levels.

A) Immunoblots with the anti-syntrophin antibody on immunoprecipitates obtained with the same antibody from extracts of INS-1 cells and three INS-1 cell clones (G1, G6 and G8) stably transfected with GFP-β2-syntrophin. B) Insulin content (IC) and basal insulin secretion (BIS) of INS-1 cells, GFP-β2-syntrophin INS-1 cell clones G1, G6, G8 and INS-1 cells stably transfected with GFP. C) Insulin secretion Stimulation Index (SI) of INS-1 cells, GFP-β2-syntrophin INS-1 cell clones G1, G6, G8 and GFP INS-1 cells. D) Immunoblots with anti-syntrophin and anti-γ-tubulin antibodies on extracts of INS-1 cells transfected with a scrambled shRNA (scr shRNA) or an shRNA for the knockdown of β2-syntrophin (β2-syn shRNA). E) IC and BIS of INS-1 cells transfected with β2-syn or scr shRNAs. F) SI of INS-1 cells transfected with β2-syn or scr shRNAs. n = number of independent experiments; *, p = 0.05; **, p = 0.01; ***, p = 0.005. p-values in B and C are relative to INS-1 cells, while in E and F they are relative to INS-1 cells transfected with scr shRNA.

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Figure 3.

Granule density and mobility in GFP-β2-syntrophin INS-1 cells.

A–D) Frames from TIRFM movies tracking the motion of CgB-mRFP1+ granules (red) in resting INS-1 cells expressing GFP (GFP/CgB-mRFP1 INS-1) (A, C) or GFP-β2-syntrophin (GFP-β2-syn/CgB-mRFP1 INS-1) (B, D). In C and D each blue line shows the motion of an individual CgB-mRFP1+ granule tracked for 40 sec. Scale bars: 4 µm. E, F) Mean speed velocity (E) and square displacement (F) of CgB-mRFP1+ granules in resting INS-1 cells expressing GFP (black) or GFP-β2-syntrophin (red). In F the green and blue lines show the weighted least square fit of the initial (first 4 sec) mean square displacement points. The mean square displacement slope of linear dependency is K = 4D, where D is the diffusion coefficient in µm2 sec−1. G) Density of granules expressed as the number of granules/100 µm2 in resting (black bars) and stimulated (red bars) GFP/and GFP-β2-syntrophin/CgB-mRFP1 INS-1 cells. H, I) Mean speed velocities (H) and diffusion coefficients (I) of CgB-mRFP1+ granules in resting (black bars) or HGHK-stimulated (red bars) INS-1 cells expressing GFP or GFP-β2-syntrophin. m = number of movies examined for each condition from four independent experiments.

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Figure 4.

Phosphorylation/dephosporylation of β2-syntrophin.

A) Immunoblots with the anti-syntrophin or anti-GFP antibodies following immunoprecipitations with the same antibodies from extracts of INS-1 and GFP-β2-syntrophin INS-1 cells, respectively. Alkaline phosphatase (AP) was added to the immunoprecipitates, while okadaic acid (OA) was added before cell extraction. β2-syntrophin species the levels of which are reduced upon AP treatment are marked with a gray arrow, while black arrows indicated species increased upon OA incubation. B) The two panels on the left show the autoradiographies of 32P-GFP-β2-syntrophin immunoprecipitated with the rabbit anti-GFP antibody from extracts of GFP-β2-syntrophin INS-1 cells labeled with 32P kept in culture media. A control immunoprecipitation from the same cells was performed using rabbit control IgG. The right panel shows the immunoblot with the anti-GFP antibody on the same immunoprecipitated material visualized by autoradiography. C) Domain structure of β2-syntrophin, including the phosphoserines identified by mass spectrometry. PH = Pleckstrin Homology domain, PDZ = PSD95/Dlg/ZO-1 domain, SU = Syntrophin Unique domain.

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Figure 5.

Characterization of β2-syntrophin phosphomutants.

A) Confocal microscopy images of GFP-β2-syntrophin and mutants with single or dual replacements of serine (S) 75, 90 and 213 with either aspartate (D) or alanine (A). Bars: 5 µm. B) Expression pattern of GFP-β2-syntrophin variants in INS-1 cells as detected by western blotting with the anti-GFP antibody.

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Figure 6.

Binding of β2-syntrophin phosphomutants to ICA512 and impact on granule density, mobility and insulin secretion.

A) Autoradiography of in vitro transcribed-translated 35S-labeled His-β2-syntrophin (His-β2-syn) S/D and S/A mutants following pull down assay with GST-ICA512601–979 or GST. B) Insulin content (IC), basal insulin secretion (BIS) and insulin secretion Stimulation Index (SI) of INS-1 cells transfected with the S75 and S90 GFP-β2-syntrophin mutants. Wild-type and GFP INS-1 cells were used as controls. n = number of independent experiments; *, p = 0.05; **, p = 0.01; ***, p = 0.005; p-values of IC, BIS, and SI were calculated relative to those in INS-1 cells. C–E) Density (C), mean speed velocity (D) and diffusion coefficient (E) of CgB-mRFP1+ granules in resting INS-1 cells expressing GFP, GFP-β2-syntrophin or the GFP-β2-syntrophin S75D and S90D phosphomutants. m = number of movies examined for each condition from six independent experiments.

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Figure 7.

Phosphorylation of endogenous and GFP-β2-syntrophin and the S/D mutants by Cdk5.

A) Immunoblots with anti-syntrophin or anti-GFP antibodies on rat islet extracts (right panel) or immunoprecipitates obtained with the same antibodies from extracts of INS-1 cells (left panel) or GFP-β2-syntrophin INS-1 cells (middle panel) treated with the Cdk5 inhibitor roscovitine or the Erk1/2 inhibitor PD98059. Asterisks indicate the β2-syntrophin species sensitive to roscovitine. B) Immunoblots with the anti-GFP antibody on immunoprecipitates obtained with the same antibody from extracts of INS-1 cells expressing GFP-β2-syntrophin variants and treated with roscovitine. Gray and black arrows point to β2-syntrophin species the levels of which decreased or increased in response to roscovitine, respectively. C) Autoradiographies and immunoblots of β2-syntrophin (left panels) and GFP-β2-syntrophin (right panels) immunoprecipitated with anti-syntrophin or anti-GFP antibodies from INS-1 and GFP-β2-syntrophin INS-1 cells, respectively. Immunoprecipitates were incubated with or without the Cdk5/p25 complex in the presence of 32P-γ-ATP. D) Autoradiography of GFP-β2-syntrophin variants immunoprecipitated with the anti-GFP antibody from GFP-β2-syntrophin INS-1 cells and incubated with the Cdk5/p25 complex as in C. An asterisk indicates the β2-syntrophin species that is lacking in the GFP-β2-syntrophin S75D mutant.

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Figure 8.

Expression of β2-syntrophin species upon Cdk5 depletion.

A) Immunoblots with anti-syntrophin, anti-Cdk5 and anti-γ-tubulin antibodies on extracts of INS-1 (left panels), GFP-β2-syntrophin INS-1 (middle panels) and GFP-β2-syntrophin S75D INS-1 (right panels) cells following the knockdown of Cdk5 (Cdk5 shRNA). As control, INS-1 cells were transfected with a scrambled shRNA. Gray and black arrows point to the β2-syntrophin species the levels of which decreased or increased upon Cdk5-depletion, respectively. The β2-syntrophin species were numbered from top to bottom B) Quantification of the immunoblots shown in A. p-values are relative to cells transfected with scr shRNA. n = number of experiments. *, p = 0.05; **, p = 0.01; ***, p = 0.005.

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