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Table 1.

Primers used in this study.

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Table 2.

Predicted SUMOylation sites in the nonstructural and structural proteins of PRRSV.

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Fig 1.

Screening of PRRSV proteins interacting with Ubc9 by yeast two-hybrid.

Yeast Y2HGold cells co-transformed with various bait and prey plasmids were selected on QDO/X/ABA plates. Shown are the blue colonies presenting the interaction of PRRSV Nsp1β, Nsp4, Nsp9, Nsp10 and N protein with Ubc9, and white colonies without interaction of the rest of PRRSV proteins with Ubc9. p53 (Gal4 binding domain fused to the murine p53) and T (Gal4 activation domain fused to the SV40 large T-antigen), Lam (Gal4 binding domain fused to nuclear lamina protein) and T were served as positive control and negative control, respectively. The three spots in the same line mean the replicates of one analysis and each spot represents a different colony.

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Fig 2.

The interaction of PRRSV Nsp1β, Nsp4, Nsp9, Nsp10 and N protein with Ubc9.

(A) The interaction of Nsp1β, Nsp4, Nsp9, Nps10 and N protein with exogenous Ubc9 by using a Co-IP assay. HEK293 cells were co-transfected with the Myc-Ubc9-expressing plasmid and the HA-Nsp1β-, HA-Nsp4-, HA-Nsp9-, HA-Nsp10- and HA-N-expressing plasmid, respectively. The cell lysates were immunoprecipitated with an anti-HA mAb and probed with anti-HA mAb and anti-Myc PAb. The left panel shows the Co-IP analyses of HA-Nsp1β, HA-Nsp4, HA-Nsp9, HA-Nsp10 and HA-N from cell lysates and the right panel indicates the identification of HA-Nsp1β, HA-Nsp4, HA-Nsp9, HA-Nsp10 and HA-N expressed in cell lysates. The asterisk (★) indicates the IgG light chain band with 26 KDa, and the solid triangle (▲) represents the target protein Myc-Ubc9. (B) The interaction of Nsp1β, Nsp4, Nsp9, Nsp10 and N protein with exogenous Ubc9 by using a GST pull-down assay. The cell lysates containing Nsp1β, Nsp4, Nsp9, Nsp10 and N protein individually were pulled down with prokaryotic expressed and purified GST-Ubc9 protein with an anti-GST mAb and probed with anti-HA and anti-GST mAb. (C) The interaction of Nsp1β, Nsp4, Nsp9, Nsp10 and N protein with endogenous Ubc9. MARC-145 cells were transduced with the lentiviruses that were expressing GFP, Nsp1β, Nsp4, Nsp9, Nsp10, or N individually. The cell lysates were immunoprecipitated with an anti-GFP mAb and followed by Western blot analysis with anti-Ubc9 and anti-GFP antibodies. The left panel indicates the identification of GFP, Nsp1β-GFP, Nsp4-GFP, Nsp9-GFP, Nsp10-GFP and N-GFP expressed in cell lysates, while the right panel shows the Co-IP analyses of GFP, Nsp1β-GFP, Nsp4-GFP, Nsp9-GFP, Nsp10-GFP and N-GFP from cell lysates.

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Fig 3.

Co-localization of Nsp1β, Nsp4, Nsp9, Nsp10 and N protein with Ubc9.

(A) Co-localization of Nsp1β, Nsp4, Nsp9, Nsp10 and N protein with exogenous Ubc9 in HEK293 cells. HEK293 cells were co-transfected with pCMV-HA-Nsp1β, pCMV-HA-Nsp4, pCMV-HA-Nsp9, pCMV-HA-Nsp10 and pCMV-HA-N with pCMV-Myc-Ubc9, respectively. The cells were fixed at 36 h post-transfection and processed by immunostaining with a mouse anti-HA mAb or rabbit anti-Myc PAb and TRITC-conjugated goat anti-mouse IgG or FITC-conjugated goat anti-rabbit IgG, and were then examined by confocal microscopy (600×magnification). Nuclei were stained with DAPI. Co-localization of Nsp1β, Nsp4, Nsp9, Nsp10 and N protein with endogenous Ubc9 in mock-infected MARC-145 cells and PRRSV-infected MARC-145 cells (B), mock-infected PAMs and PRRSV-infected PAMs (C). The mock- or PRRSV-infected cells were fixed at 24 h post-infection and processed by immunostaining with a rabbit anti-Ubc9 PAb or mouse anti-Nsp1β, anti-Nsp4, anti-Nsp9, anti-Nsp10 and anti-N mAb, respectively, and then immunostained with TRITC-conjugated goat anti-mouse IgG and FITC-conjugated goat anti-rabbit IgG. Nuclei were stained with DAPI.

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Fig 4.

Inhibition of PRRSV JXwn06 replication by Ubc9.

(A) PRRSV titers in Ubc9-overexpressed MARC-145 cells. MARC-145 cells were transduced with the lentiviruses that were expressing GFP and Ubc9, respectively. The cells were infected with PRRSV JXwn06 at MOI of 0.01 at 24 h post-transduction, and the virus titers were then assayed by a microtitration infectivity assay at the indicated time points post-infection. Data are shown as means ± SD of three independent experiments (**p<0.01). (B) PRRSV RNA replication in Ubc9-overexpressing MARC-145 cells. MARC-145 cells were transduced with the lentiviruses that were expressing GFP and Ubc9, respectively. The cells were infected with PRRSV JXwn06 at MOI of 0.01 at 24 h post-transduction and collected at the indicated time points post-infection. The total cellular RNA was extracted and the mRNA levels of PRRSV N gene were determined by quantitative RT-PCR. Data are shown as means ± SD of three independent experiments (***p<0.001; ns, no significant). (C) SiRNA-mediated knockdown of endogenous Ubc9. MARC-145 cells were transfected with siRNA (siUbc9-1, siUbc9-2, siUbc9-3) and control siRNA (siCon). The cells were harvested at 48 h post-transfection and the cell lysates were probed with an anti-ubc9 antibody. The optical density ratios of Ubc9/β-actin in Ubc9 gene-silenced MARC-145 cells are shown with graphs. Data are shown as means ± SD of three independent experiments (***p<0.001). (D) The optical density ratios of Ubc9/β-actin in Ubc9 gene-silenced MARC-145 cells are shown with graphs. Data are shown as means ± SD of three independent experiments (***p<0.001). (E) PRRSV titers in Ubc9 gene-silenced MARC-145 cells. MARC-145 cells transfected with the siRNA (siUbc9-1) or control siRNA (siCon) for 48 h were infected with PRRSV JXwn06 at MOI of 0.01, and the virus titers were examined at the indicated time points post-infection. Data are shown as means ± SD of three independent experiments (*p<0.05; ***p<0.001; ns, no significant). (F) PRRSV RNA replication in Ubc9-silenced MARC-145 cells. MARC-145 cells transfected with the siRNA (siUbc9-1) or control siRNA (siCon) for 48 h were infected with PRRSV JXwn06 at MOI of 0.01 and collected at the indicated time points post-infection. The total cellular RNA was extracted and the mRNA levels of PRRSV N gene were determined by quantitative RT-PCR. Data are shown as means ± SD of three independent experiments (***p<0.001; ns, no significant). (G) PRRSV growth in the MARC-145 cells treated with GA. Data are shown as means ± SD of three independent experiments (***p<0.001; **p<0.01; ns, no significant).

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Fig 5.

SUMOylation of PRRSV N protein.

(A and B) The expression of Nsp1β, Nsp4, Nsp9, Nsp10 and N proteins in HEK293 cells using a Co-IP assay. HEK293 cells were transfected with pCMV-HA-Nsp1β, pCMV-HA-Nsp4, pCMV-HA-Nsp9, pCMV-HA-Nsp10 and pCMV-HA-N, separately. The cell lysates were immunoprecipitated with an anti-HA mAb and probed with an anti-HA mAb. The left panel indicates the identification of HA-Nsp1β, HA-Nsp4, HA-Nsp9, HA-Nsp10 and HA-N expressed in cell lysates and the right panel shows the Co-IP analyses of HA-Nsp1β, HA-Nsp4, HA-Nsp9, HA-Nsp10 and HA-N from cell lysates. (C) The expression of N and mutated N proteins (C23S and C23A) in HEK293 cells by using a Co-IP assay. HEK293 cells were transfected with pCMV-HA-N, pCMV-HA-N (C23S), pCMV-HA-N (C23A), separately. The cell lysates were immunoprecipitated with an anti-HA mAb and probed with anti-HA mAb. The left panel indicated the identification of HA-N, HA-N (C23S) and HA-N (C23A) expressed in cell lysates and the right panel showed the Co-IP analyses of HA-N, HA-N (C23S) and HA-N (C23A) from cell lysates. (D) The expression of N protein in MARC-145 cells following PRRSV infection using a Co-IP assay. MARC-145 cells were infected with PRRSV JXwn06 at a MOI of 0.1. At 36 h the cell lysates were immunoprecipitated with an anti-N mAb, anti-SUMO1 or anti-SUMO2/3 mAb and probed with these mAb, separately.

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