Frequent loss of BTG1 activity and impaired interactions with the Caf1 subunit of the Ccr4–Not deadenylase in non-Hodgkin lymphoma

References

• Winkler GS. The mammalian anti-proliferative BTG/Tob protein family. J Cell Physiol. 2010;222(1):66–72.
   PubMed Web of Science ®Google Scholar
• Yuniati L, Scheijen B, van der Meer LT, et al. Tumor suppressors BTG1 and BTG2: beyond growth control. J Cell Physiol. 2019;234(5):5379–5389.
   PubMed Web of Science ®Google Scholar
• Buanne P, Corrente G, Micheli L, et al. Cloning of PC3B, a novel member of the PC3/BTG/TOB family of growth inhibitory genes, highly expressed in the olfactory epithelium. Genomics. 2000;68(3):253–263.
   PubMed Web of Science ®Google Scholar
• Ikematsu N, Yoshida Y, Kawamura-Tsuzuku J, et al. Tob2, a novel anti-proliferative Tob/BTG1 family member, associates with a component of the CCR4 transcriptional regulatory complex capable of binding cyclin-dependent kinases. Oncogene. 1999;18(52):7432–7441.
   PubMed Web of Science ®Google Scholar
• Matsuda S, Kawamura-Tsuzuku J, Ohsugi M, et al. Tob, a novel protein that interacts with p185erbB2, is associated with anti-proliferative activity. Oncogene. 1996;12(4):705–713.
   PubMed Web of Science ®Google Scholar
• Montagnoli A, Guardavaccaro D, Starace G, et al. Overexpression of the nerve growth factor-inducible PC3 immediate early gene is associated with growth inhibition. Cell Growth Differ. 1996;7:1327–1336.
   PubMedGoogle Scholar
• Rouault J, Rimokh R, Tessa C, et al. BTG1, a member of a new family of antiproliferative genes. EMBO J. 1992;11(4):1663–1670.
   PubMed Web of Science ®Google Scholar
• Guardavaccaro D, Corrente G, Covone F, et al. Arrest of G(1)-S progression by the p53-inducible gene PC3 is Rb dependent and relies on the inhibition of cyclin D1 transcription. Mol Cell Biol. 2000;20(5):1797–1815.
   PubMed Web of Science ®Google Scholar
• Rouault J-P, Falette N, Guéhenneux F, et al. Identification of BTG2, an antiproliferative p53-dependent component of the DNA damage cellular response pathway. Nat Genet. 1996;14(4):482–486.
   PubMed Web of Science ®Google Scholar
• Yang X, Morita M, Wang H, et al. Crystal structures of human BTG2 and mouse TIS21 involved in suppression of CAF1 deadenylase activity. Nucleic Acids Res. 2008;36(21):6872–6881.
   PubMed Web of Science ®Google Scholar
• Rouault J-P, Prévôt D, Berthet C, et al. Interaction of BTG1 and p53-regulated BTG2 gene products with mCaf1, the murine homolog of a component of the yeast CCR4 transcriptional regulatory complex. J Biol Chem. 1998;273(35):22563–22569.
   PubMed Web of Science ®Google Scholar
• Prévôt D, Morel A-P, Voeltzel T, et al. Relationships of the antiproliferative proteins BTG1 and BTG2 with CAF1, the human homolog of a component of the yeast CCR4 transcriptional complex: involvement in estrogen receptor alpha signaling pathway. J Biol Chem. 2001;276(13):9640–9648.
   PubMed Web of Science ®Google Scholar
• Yoshida Y, Hosoda E, Nakamura T, et al. Association of ANA, a member of the antiproliferative Tob family proteins, with a Caf1 component of the CCR4 transcriptional regulatory complex. Jpn J Cancer Res. 2001;92(6):592–596.
   PubMedGoogle Scholar
• Busson M, Carazo A, Seyer P, et al. Coactivation of nuclear receptors and myogenic factors induces the major BTG1 influence on muscle differentiation. Oncogene. 2005;24(10):1698–1710.
   PubMed Web of Science ®Google Scholar
• Ou YH, Chung PH, Hsu FF, et al. The candidate tumor suppressor BTG3 is a transcriptional target of p53 that inhibits E2F1. EMBO J. 2007;26(17):3968–3980.
   PubMed Web of Science ®Google Scholar
• Doidge R, Mittal S, Aslam A, et al. The anti-proliferative activity of BTG/TOB proteins is mediated via the Caf1a (CNOT7) and Caf1b (CNOT8) deadenylase subunits of the Ccr4–Not complex. PLoS One. 2012;7(12):e51331.
   PubMed Web of Science ®Google Scholar
• Ezzeddine N, Chen C-YA, Shyu A-B. Evidence providing new insights into TOB-promoted deadenylation and supporting a link between TOB's deadenylation-enhancing and antiproliferative activities. Mol Cell Biol. 2012;32(6):1089–1098.
   PubMed Web of Science ®Google Scholar
• Pasternak M, Pfender S, Santhanam B, et al. The BTG4 and CAF1 complex prevents the spontaneous activation of eggs by deadenylating maternal mRNAs. Open Biol. 2016;6(9):160184.
   PubMed Web of Science ®Google Scholar
• Yu C, Ji S-Y, Sha Q-Q, et al. BTG4 is a meiotic cell cycle-coupled maternal–zygotic-transition licensing factor in oocytes. Nat Struct Mol Biol. 2016;23(5):387–394.
   PubMed Web of Science ®Google Scholar
• Wahle E, Winkler GS. RNA decay machines: deadenylation by the Ccr4–Not and Pan2–Pan3 complexes. Biochim Biophys Acta. 2013;1829(6–7):561–570.
   PubMed Web of Science ®Google Scholar
• Stupfler B, Birck C, Séraphin B, et al. BTG2 bridges PABPC1 RNA-binding domains and CAF1 deadenylase to control cell proliferation. Nat Commun. 2016;7:10811.
   PubMed Web of Science ®Google Scholar
• Ezzeddine N, Chang T-C, Zhu W, et al. Human TOB, an antiproliferative transcription factor, is a poly(A)-binding protein-dependent positive regulator of cytoplasmic mRNA deadenylation. Mol Cell Biol. 2007;27(22):7791–7801.
   PubMed Web of Science ®Google Scholar
• Funakoshi Y, Doi Y, Hosoda N, et al. Mechanism of mRNA deadenylation: evidence for a molecular interplay between translation termination factor eRF3 and mRNA deadenylases. Genes Dev. 2007;21(23):3135–3148.
   PubMed Web of Science ®Google Scholar
• Prévôt D, Voeltzel T, Birot A-M, et al. The leukemia-associated protein Btg1 and the p53-regulated protein Btg2 interact with the homeoprotein Hoxb9 and enhance its transcriptional activation. J Biol Chem. 2000;275(1):147–153.
   PubMed Web of Science ®Google Scholar
• Lin W-J, Gary JD, Yang MC, et al. The mammalian immediate-early TIS21 protein and the leukemia-associated BTG1 protein interact with a protein-arginine N-methyltransferase. J Biol Chem. 1996;271(25):15034–15044.
   PubMed Web of Science ®Google Scholar
• Kanda M, Sugimoto H, Nomoto S, et al. B-cell translocation gene 1 serves as a novel prognostic indicator of hepatocellular carcinoma. J Oncol. 2015;46:641–648.
   Web of Science ®Google Scholar
• Kanda M, Oya H, Nomoto S, et al. Diversity of clinical implication of B-cell translocation gene 1 expression by histopathologic and anatomic subtypes of gastric cancer. Dig Dis Sci. 2015;60(5):1256–1264.
   PubMed Web of Science ®Google Scholar
• Kawakubo H, Brachtel E, Hayashida T, et al. Loss of B-cell translocation gene-2 in estrogen receptor-positive breast carcinoma is associated with tumor grade and overexpression of cyclin d1 protein. Cancer Res. 2006;66(14):7075–7082.
   PubMed Web of Science ®Google Scholar
• Struckmann K, Schraml P, Simon R, et al. Impaired expression of the cell cycle regulator BTG2 is common in clear cell renal cell carcinoma. Cancer Res. 2004;64(5):1632–1638.
   PubMed Web of Science ®Google Scholar
• Ficazzola MA, Fraiman M, Gitlin J, et al. Antiproliferative B cell translocation gene 2 protein is down-regulated post-transcriptionally as an early event in prostate carcinogenesis. Carcinogenesis. 2001;22(8):1271–1279.
   PubMed Web of Science ®Google Scholar
• Waanders E, Scheijen B, van der Meer LT, et al. The origin and nature of tightly clustered BTG1 deletions in precursor B-cell acute lymphoblastic leukemia support a model of multiclonal evolution. PLoS Genet. 2012;8(2):e1002533.
   PubMed Web of Science ®Google Scholar
• Morin RD, Mendez-Lago M, Mungall AJ, et al. Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature. 2011;476(7360):298–303.
   PubMed Web of Science ®Google Scholar
• Lohr JG, Stojanov P, Lawrence MS, et al. Discovery and prioritization of somatic mutations in diffuse large B-cell lymphoma (DLBCL) by whole-exome sequencing. Proc Natl Acad Sci U S A. 2012;109(10):3879–3884.
   PubMed Web of Science ®Google Scholar
• Love C, Sun Z, Jima D, et al. The genetic landscape of mutations in Burkitt lymphoma. Nat Genet. 2012;44(12):1321–1325.
   PubMed Web of Science ®Google Scholar
• Walker BA, Wardell CP, Melchor L, et al. Intraclonal heterogeneity and distinct molecular mechanisms characterize the development of t(4;14) and t(11;14) myeloma. Blood. 2012;120(5):1077–1086.
   PubMed Web of Science ®Google Scholar
• Zhang J, Grubor V, Love CL, et al. Genetic heterogeneity of diffuse large B-cell lymphoma. Proc Natl Acad Sci U S A. 2013;110(4):1398–1403.
   PubMed Web of Science ®Google Scholar
• Reddy A, Zhang J, Davis NS, et al. Genetic and functional drivers of diffuse large B cell lymphoma. Cell. 2017;171(2):481–494.e15.
   PubMed Web of Science ®Google Scholar
• Forbes SA, Bindal N, Bamford S, et al. COSMIC: mining complete cancer genomes in the catalogue of somatic mutations in cancer. Nucleic Acids Res. 2011;39(Database issue):D945–D950.
   PubMed Web of Science ®Google Scholar
• Kumar P, Henikoff S, Ng PC. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc. 2009;4(7):1073–1081.
   PubMed Web of Science ®Google Scholar
• Kelley LA, Mezulis S, Yates CM, et al. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc. 2015;10(6):845–858.
   PubMed Web of Science ®Google Scholar
• Sampathkumar P, Romero R, Wasserman S, et al. Crystal structure of human B-cell translocation gene (BTG2); 2008;2.
   Google Scholar
• Meng EC, Pettersen EF, Couch GS, et al. Tools for integrated sequence-structure analysis with UCSF Chimera. BMC Bioinformatics. 2006;7:339.
   PubMed Web of Science ®Google Scholar
• Horiuchi M, Takeuchi K, Noda N, et al. Structural basis for the antiproliferative activity of the Tob–hCaf1 complex. J Biol Chem. 2009;284(19):13244–13255.
   PubMed Web of Science ®Google Scholar
• Clarke ST, Calderon V, Bradford JA. Click chemistry for analysis of cell proliferation in flow cytometry. Curr Protoc Cytometry. 2017;82(1):7.49.1–7.49.30.
   Google Scholar
• Li Y, Choi PS, Casey SC, Dill DL, et al. MYC through miR-17-92 suppresses specific target genes to maintain survival, autonomous proliferation, and a neoplastic state. Cancer Cell. 2014;26(2):262–272.
   PubMed Web of Science ®Google Scholar
• He L, Thomson JM, Hemann MT, et al. A microRNA polycistron as a potential human oncogene. Nature. 2005;435(7043):828–833.
   PubMed Web of Science ®Google Scholar
• Bai Y, Qiao L, Xie N, et al. Expression and prognosis analyses of the Tob/BTG antiproliferative (APRO) protein family in human cancers. PLoS One. 2017;12(9):e0184902.
   PubMed Web of Science ®Google Scholar
• Iwanaga K, Sueoka N, Sato A, et al. Alteration of expression or phosphorylation status of tob, a novel tumor suppressor gene product, is an early event in lung cancer. Cancer Lett. 2003;202(1):71–79.
   PubMed Web of Science ®Google Scholar
• Yoneda M, Suzuki T, Nakamura T, et al. Deficiency of antiproliferative family protein Ana correlates with development of lung adenocarcinoma. Cancer Sci. 2009;100(2):225–232.
   PubMed Web of Science ®Google Scholar
• Faraji F, Hu Y, Yang HH, et al. Post-transcriptional control of tumor cell autonomous metastatic potential by CCR4–NOT deadenylase CNOT7. PLoS Genet. 2016;12(1):e1005820.
   PubMed Web of Science ®Google Scholar
• Helms MW, Kemming D, Contag CH, et al. TOB1 is regulated by EGF-dependent HER2 and EGFR signaling, is highly phosphorylated, and indicates poor prognosis in node-negative breast cancer. Cancer Res. 2009;69(12):5049–5056.
   PubMed Web of Science ®Google Scholar