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PLoS Pathog ; 16(10): e1009006, 2020 10.
Article in English | MEDLINE | ID: mdl-33057440

ABSTRACT

Kaposi's sarcoma-associated herpesvirus (KSHV) vGPCR is a constitutively active G protein-coupled receptor that subverts proliferative and inflammatory signaling pathways to induce cell transformation in Kaposi's sarcoma. Cyclooxygenase-2 (COX-2) is an inflammatory mediator that plays a key regulatory role in the activation of tumor angiogenesis. Using two different transformed mouse models and tumorigenic full KSHV genome-bearing cells, including KSHV-Bac16 based mutant system with a vGPCR deletion, we demostrate that vGPCR upregulates COX-2 expression and activity, signaling through selective MAPK cascades. We show that vGPCR expression triggers signaling pathways that upregulate COX-2 levels due to a dual effect upon both its gene promoter region and, in mature mRNA, the 3'UTR region that control mRNA stability. Both events are mediated by signaling through ERK1/2 MAPK pathway. Inhibition of COX-2 in vGPCR-transformed cells impairs vGPCR-driven angiogenesis and treatment with the COX-2-selective inhibitory drug Celecoxib produces a significant decrease in tumor growth, pointing to COX-2 activity as critical for vGPCR oncogenicity in vivo and indicating that COX-2-mediated angiogenesis could play a role in KS tumorigenesis. These results, along with the overexpression of COX-2 in KS lesions, define COX-2 as a potential target for the prevention and treatment of KSHV-oncogenesis.


Subject(s)
Herpesvirus 8, Human/metabolism , Matrix Metalloproteinase 2/biosynthesis , Receptors, G-Protein-Coupled/metabolism , Sarcoma, Kaposi/blood supply , Animals , Carcinogenesis , Cell Transformation, Neoplastic/genetics , Endothelial Cells/metabolism , GTP-Binding Proteins/genetics , Herpesvirus 8, Human/genetics , MAP Kinase Signaling System , Matrix Metalloproteinase 2/genetics , Matrix Metalloproteinase 2/metabolism , Mice , Mice, Nude , NIH 3T3 Cells , Neovascularization, Pathologic/metabolism , Neovascularization, Pathologic/pathology , Neovascularization, Pathologic/virology , Oncogenes , Receptors, G-Protein-Coupled/genetics , Sarcoma, Kaposi/metabolism , Sarcoma, Kaposi/pathology , Sarcoma, Kaposi/virology , Signal Transduction , Transcriptional Activation
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