Seeing is believing: the impact of RB on nuclear organization

References

• Bickmore WA. The spatial organization of the human genome. Annu Rev Genomics Hum Genet. 2013;14:67–84.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Sandoval A, Gasser SM. On TADs and LADs: spatial control over gene expression. Trends Genet. 2016;32:485–495.
   PubMed Web of Science ®Google Scholar
• Corces MR, Corces VG. The three-dimensional cancer genome. Curr Opin Genet Dev. 2016;36:1–7.
   PubMed Web of Science ®Google Scholar
• Johnstone SE, Reyes A, Qi Y, et al. Large-scale topological changes restrain malignant progression in colorectal cancer. Cell. 2020;182:1474–1489 e1423.
   PubMed Web of Science ®Google Scholar
• Zink D, Fischer AH, Nickerson JA. Nuclear structure in cancer cells. Nat Rev Cancer. 2004;4:677–687.
   PubMed Web of Science ®Google Scholar
• Akdemir KC, Le VT, Chandran S, et al. Disruption of chromatin folding domains by somatic genomic rearrangements in human cancer. Nat Genet. 2020;52:294–305.
   PubMed Web of Science ®Google Scholar
• Burkhart DL, Sage J. Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat Rev Cancer. 2008;8:671–682.
   PubMed Web of Science ®Google Scholar
• Dick FA, Goodrich DW, Sage J, et al. Non-canonical functions of the RB protein in cancer. Nat Rev Cancer. 2018;18:442–451.
   PubMed Web of Science ®Google Scholar
• Dyson N. The regulation of E2F by Prb-family proteins. Genes Dev. 1998;12:2245–2262.
   PubMed Web of Science ®Google Scholar
• Dyson NJ. RB1: a prototype tumor suppressor and an enigma. Genes Dev. 2016;30:1492–1502.
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100:57–70.
   PubMed Web of Science ®Google Scholar
• Chicas A, Wang X, Zhang C, et al. Dissecting the unique role of the retinoblastoma tumor suppressor during cellular senescence. Cancer Cell. 2010;17:376–387.
   PubMed Web of Science ®Google Scholar
• Narita M, Nunez S, Heard E, et al. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell. 2003;113:703–716.
   PubMed Web of Science ®Google Scholar
• Calo E, Quintero-Estades JA, Danielian PS, et al. Rb regulates fate choice and lineage commitment in vivo. Nature. 2010;466:1110–1114.
   PubMed Web of Science ®Google Scholar
• Thomas DM, Carty SA, Piscopo DM, et al. The retinoblastoma protein acts as a transcriptional coactivator required for osteogenic differentiation. Mol Cell. 2001;8:303–316.
   PubMed Web of Science ®Google Scholar
• Kareta MS, Gorges LL, Hafeez S, et al. Inhibition of pluripotency networks by the Rb tumor suppressor restricts reprogramming and tumorigenesis. Cell Stem Cell. 2015;16:39–50.
   PubMed Web of Science ®Google Scholar
• Ku SY, Rosario S, Wang Y, et al. Rb1 and Trp53 cooperate to suppress prostate cancer lineage plasticity, metastasis, and antiandrogen resistance. Science. 2017;355:78–83.
   PubMed Web of Science ®Google Scholar
• Mu P, Zhang Z, Benelli M, et al. SOX2 promotes lineage plasticity and antiandrogen resistance in TP53- and RB1-deficient prostate cancer. Science. 2017;355:84–88.
   PubMed Web of Science ®Google Scholar
• Walter DM, Yates TJ, Ruiz-Torres M, et al. RB constrains lineage fidelity and multiple stages of tumour progression and metastasis. Nature. 2019;569:423–427.
   PubMed Web of Science ®Google Scholar
• Zhang J, Benavente J CA, McEvoy J, et al. A novel retinoblastoma therapy from genomic and epigenetic analyses. Nature. 2012;481:329–334.
   PubMed Web of Science ®Google Scholar
• Nielsen SJ, Schneider R, Bauer UM, et al. Rb targets histone H3 methylation and HP1 to promoters. Nature. 2001;412:561–565.
   PubMed Web of Science ®Google Scholar
• Ishak CA, Marshall AE, Passos DT, et al. An RB-EZH2 complex mediates silencing of repetitive DNA sequences. Mol Cell. 2016;64:1074–1087.
   PubMed Web of Science ®Google Scholar
• Kotake Y, Cao R, Viatour P, et al. pRB family proteins are required for H3K27 trimethylation and Polycomb repression complexes binding to and silencing p16INK4alpha tumor suppressor gene. Genes Dev. 2007;21:49–54.
   PubMed Web of Science ®Google Scholar
• Watt AC, Cejas P, DeCristo MJ, et al. CDK4/6 inhibition reprograms the breast cancer enhancer landscape by stimulating AP-1 transcriptional activity. Nat Cancer. 2021;2:34–48.
   PubMedGoogle Scholar
• Longworth MS, Herr A, Ji JY, et al. RBF1 promotes chromatin condensation through a conserved interaction with the Condensin II protein Dcap-D3. Genes Dev. 2008;22:1011–1024.
   PubMed Web of Science ®Google Scholar
• Marshall AE, Ishak CA, Dick FA. An RB-Condensin II complex mediates long-range chromosome interactions and influences expression at divergently paired genes. Mol Cell Biol. 2020;40. DOI:10.1128/MCB.00452-19
   PubMed Web of Science ®Google Scholar
• Manning AL, Benes C, Dyson NJ. Whole chromosome instability resulting from the synergistic effects of pRB and p53 inactivation. Oncogene. 2014a;33:2487–2494.
   PubMed Web of Science ®Google Scholar
• Manning AL, Longworth MS, Dyson NJ. Loss of pRB causes centromere dysfunction and chromosomal instability. Genes Dev. 2010;24:1364–1376.
   PubMed Web of Science ®Google Scholar
• Manning AL, Dyson NJ. RB: mitotic implications of a tumour suppressor. Nat Rev Cancer. 2012;12:220–226.
   PubMed Web of Science ®Google Scholar
• Manning AL, Yazinski SA, Nicolay B, et al. Suppression of genome instability in Prb-deficient cells by enhancement of chromosome cohesion. Mol Cell. 2014b;53:993–1004.
   PubMed Web of Science ®Google Scholar
• Sanidas I, Lee H, Rumde PH, et al. Chromatin-bound RB targets promoters, enhancers, and CTCF-bound loci and is redistributed by cell-cycle progression. Mol Cell. 2022;82:3333–3349 e3339.
   PubMed Web of Science ®Google Scholar
• Krishnan B, Yasuhara T, Rumde P, et al., Active RB causes visible changes in nuclear organization. J Cell Bio. 2022;221. DOI:10.1083/jcb.202102144
   Web of Science ®Google Scholar
• Narasimha AM, Kaulich M, Shapiro GS, et al. Cyclin D activates the Rb tumor suppressor by monophosphorylation. Elife. 2014;3. DOI:10.7554/eLife.02872
   Web of Science ®Google Scholar
• Sanidas I, Morris R, Fella KA, et al. A code of monophosphorylation modulates the function of RB. Mol Cell. 2019;73:985–1000 e1006.
   PubMed Web of Science ®Google Scholar
• Goodrich DW. The retinoblastoma tumor-suppressor gene, the exception that proves the rule. Oncogene. 2006;25:5233–5243.
   PubMed Web of Science ®Google Scholar
• Xiao H, Goodrich DW. The retinoblastoma tumor suppressor protein is required for efficient processing and repair of trapped topoisomerase IIDNA-cleavable complexes. Oncogene. 2005;24:8105–8113.
   PubMed Web of Science ®Google Scholar
• Brehm A, Miska EA, McCance DJ, et al. Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature. 1998;391:597–601.
   PubMed Web of Science ®Google Scholar
• Zhang HS, Gavin A M, Dahiya A, et al. Exit from G1 and S phase of the cell cycle is regulated by repressor complexes containing HDAC-Rb-Hswi/SNF/SNF and Rb-Hswi/SNF/SNF. Cell. 2000;101:79–89.
   PubMed Web of Science ®Google Scholar
• Champoux JJ. DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem. 2001;70:369–413.
   PubMed Web of Science ®Google Scholar
• Nitiss JL. DNA topoisomerase II and its growing repertoire of biological functions. Nat Rev Cancer. 2009;9:327–337.
   PubMed Web of Science ®Google Scholar
• Brown CR, Kennedy CJ, Delmar VA, et al. Global histone acetylation induces functional genomic reorganization at mammalian nuclear pore complexes. Genes Dev. 2008;22:627–639.
   PubMed Web of Science ®Google Scholar
• Jiang H, Martin V, Gomez-Manzano C, et al. The RB-E2F1 pathway regulates autophagy. Cancer Res. 2010;70:7882–7893.
   PubMed Web of Science ®Google Scholar
• Vijayaraghavan S, Karakas C, Doostan I, et al. CDK4/6 and autophagy inhibitors synergistically induce senescence in Rb positive cytoplasmic cyclin E negative cancers. Nat Commun. 2017;8:15916.
   PubMed Web of Science ®Google Scholar
• Chandra T, Ewels PA, Schoenfelder S, et al. Global reorganization of the nuclear landscape in senescent cells. Cell Rep. 2015;10:471–483.
   PubMed Web of Science ®Google Scholar
• Criscione SW, De Cecco M, Siranosian B, et al. Reorganization of chromosome architecture in replicative cellular senescence. Sci Adv. 2016a;2:e1500882.
   PubMed Web of Science ®Google Scholar
• Criscione SW, Teo YV, Neretti N. The chromatin landscape of cellular senescence. Trends Genet. 2016b;32:751–761.
   PubMed Web of Science ®Google Scholar
• Rocha A, Dalgarno A, Neretti N. The functional impact of nuclear reorganization in cellular senescence. Brief Funct Genomics. 2022;21:24–34.
   PubMed Web of Science ®Google Scholar
• Sati S, Bonev B, Szabo Q, et al. 4D genome rewiring during oncogene-induced and replicative senescence. Mol Cell. 2020;78:522–538 e529.
   PubMed Web of Science ®Google Scholar
• Zirkel A, Nikolic M, Sofiadis K, et al. HMGB2 loss upon senescence entry disrupts genomic organization and induces CTCF clustering across cell types. Mol Cell. 2018;70:730–744 e736.
   PubMed Web of Science ®Google Scholar
• Swanson EC, Manning B, Zhang H, et al. Higher-order unfolding of satellite heterochromatin is a consistent and early event in cell senescence. J Cell Bio. 2013;203:929–942.
   PubMed Web of Science ®Google Scholar
• White E, Lowe SW. Eating to exit: autophagy-enabled senescence revealed. Genes Dev. 2009;23:784–787.
   PubMed Web of Science ®Google Scholar
• Bhat UG, Raychaudhuri P, Beck WT. Functional interaction between human topoisomerase IIalpha and retinoblastoma protein. Proc Natl Acad Sci U S A. 1999;96:7859–7864.
   PubMed Web of Science ®Google Scholar
• Montoya-Durango DE, Ramos KA, Bojang P, et al. LINE-1 silencing by retinoblastoma proteins is effected through the nucleosomal and remodeling deacetylase multiprotein complex. BMC Cancer. 2016;16:38.
   PubMed Web of Science ®Google Scholar
• Benevolenskaya EV, Murray HL, Branton P, et al. Binding of pRB to the PHD protein RBP2 promotes cellular differentiation. Mol Cell. 2005;18:623–635.
   PubMed Web of Science ®Google Scholar
• Fattaey AR, Helin K, Dembski MS, et al. Characterization of the retinoblastoma binding proteins RBP1 and RBP2. Oncogene. 1993;8:3149–3156.
   PubMed Web of Science ®Google Scholar
• Robertson KD, Ait-Si-Ali S, Yokochi T, et al. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat Genet. 2000;25:338–342.
   PubMed Web of Science ®Google Scholar