1932

Abstract

Perfectly orchestrated periodic gene expression during cell cycle progression is essential for maintaining genome integrity and ensuring that cell proliferation can be stopped by environmental signals. Genetic and proteomic studies during the past two decades revealed remarkable evolutionary conservation of the key mechanisms that control cell cycle–regulated gene expression, including multisubunit DNA-binding DREAM complexes. DREAM complexes containing a retinoblastoma family member, an E2F transcription factor and its dimerization partner, and five proteins related to products of multivulva (Muv) class B genes , , , , and (comprising the MuvB core) have been described in diverse organisms, from worms to humans. This review summarizes the current knowledge of the structure, function, and regulation of DREAM complexes in different organisms, as well as the role of DREAM in human disease.

Keyword(s): B-Mybcancercell cycleE2FFoxM1transcription
Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-071819-103836
2021-11-23
2024-05-09
Loading full text...

Full text loading...

/deliver/fulltext/genet/55/1/annurev-genet-071819-103836.html?itemId=/content/journals/10.1146/annurev-genet-071819-103836&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abbassi R, Johns TG, Kassiou M, Munoz L. 2015. DYRK1A in neurodegeneration and cancer: molecular basis and clinical implications. Pharmacol. Ther. 151:87–98
    [Google Scholar]
  2. 2. 
    Adayev T, Wegiel J, Hwang Y-W. 2011. Harmine is an ATP-competitive inhibitor for dual-specificity tyrosine phosphorylation-regulated kinase 1A (Dyrk1A). Arch. Biochem. Biophys. 507:212–18
    [Google Scholar]
  3. 3. 
    Allegra CJ, Aberle DR, Ganschow P, Hahn SM, Lee CN et al. 2010. National Institutes of Health State-of-the-Science Conference statement: diagnosis and management of ductal carcinoma in situ September 22–24, 2009. J. Natl. Cancer Inst. 102:161–69
    [Google Scholar]
  4. 4. 
    Andrejka L, Wen H, Ashton J, Grant M, Iori K et al. 2011. Animal-specific C-terminal domain links myeloblastosis oncoprotein (Myb) to an ancient repressor complex. PNAS 108:17438–43
    [Google Scholar]
  5. 5. 
    Aranda S, Laguna A, de la Luna S. 2011. DYRK family of protein kinases: evolutionary relationships, biochemical properties, and functional roles. FASEB J 25:449–62
    [Google Scholar]
  6. 6. 
    Bainor AJ, Saini S, Calderon A, Casado-Polanco R, Giner-Ramirez B et al. 2018. The HDAC-associated Sin3B protein represses DREAM complex targets and cooperates with APC/C to promote quiescence. Cell Rep 25:2797–807.e8
    [Google Scholar]
  7. 7. 
    Beall EL, Bell M, Georlette D, Botchan MR 2004. Dm-myb mutant lethality in Drosophila is dependent upon mip130: positive and negative regulation of DNA replication. Genes Dev 18:1667–80
    [Google Scholar]
  8. 8. 
    Beall EL, Manak JR, Zhou S, Bell M, Lipsick JS, Botchan MR. 2002. Role for a Drosophila Myb-containing protein complex in site-specific DNA replication. Nature 420:833–37
    [Google Scholar]
  9. 9. 
    Becker W. 2018. A wake-up call to quiescent cancer cells—potential use of DYRK1B inhibitors in cancer therapy. FEBS J 285:1203–11
    [Google Scholar]
  10. 10. 
    Becker W, Weber Y, Wetzel K, Eirmbter K, Tejedor FJ, Joost H-G. 1998. Sequence characteristics, subcellular localization, and substrate specificity of DYRK-related kinases, a novel family of dual specificity protein kinases. J. Biol. Chem. 273:25893–902
    [Google Scholar]
  11. 11. 
    Beshiri ML, Holmes KB, Richter WF, Hess S, Islam ABMMK et al. 2012. Coordinated repression of cell cycle genes by KDM5A and E2F4 during differentiation. PNAS 109:18499–504
    [Google Scholar]
  12. 12. 
    Boichuk S, Parry JA, Makielski KR, Litovchick L, Baron JL et al. 2013. The DREAM complex mediates GIST cell quiescence and is a novel therapeutic target to enhance imatinib-induced apoptosis. Cancer Res 73:5120–29
    [Google Scholar]
  13. 13. 
    Boxem M, van den Heuvel S. 2002. C. elegans class B synthetic multivulva genes act in G1 regulation. Curr. Biol. 12:906–11
    [Google Scholar]
  14. 14. 
    Brehm A, Miska EA, McCance DJ, Reid JL, Bannister AJ, Kouzarides T. 1998. Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature 391:597–601
    [Google Scholar]
  15. 15. 
    Carter SL, Eklund AC, Kohane IS, Harris LN, Szallasi Z. 2006. A signature of chromosomal instability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nat. Genet. 38:1043–48
    [Google Scholar]
  16. 16. 
    Ceol CJ, Horvitz HR. 2001. dpl-1 DP and efl-1 E2F act with lin-35 Rb to antagonize Ras signaling in C. elegans vulval development. Mol. Cell 7:461–73
    [Google Scholar]
  17. 17. 
    Chen J-Y, Lin J-R, Tsai F-C, Meyer T 2013. Dosage of Dyrk1a shifts cells within a p21-cyclin D1 signaling map to control the decision to enter the cell cycle. Mol. Cell 52:87–100
    [Google Scholar]
  18. 18. 
    Chen X, Müller GA, Quaas M, Fischer M, Han N et al. 2013. The forkhead transcription factor FOXM1 controls cell cycle-dependent gene expression through an atypical chromatin binding mechanism. Mol. Cell. Biol. 33:227–36
    [Google Scholar]
  19. 19. 
    Classon M, Harlow E. 2002. The retinoblastoma tumour suppressor in development and cancer. Nat. Rev. Cancer 2:910–17
    [Google Scholar]
  20. 20. 
    Classon M, Salama S, Gorka C, Mulloy R, Braun P, Harlow E. 2000. Combinatorial roles for pRB, p107, and p130 in E2F-mediated cell cycle control. PNAS 97:10820–25
    [Google Scholar]
  21. 21. 
    Cobrinik D, Lee MH, Hannon G, Mulligan G, Bronson RT et al. 1996. Shared role of the pRB-related p130 and p107 proteins in limb development. Genes Dev 10:1633–44
    [Google Scholar]
  22. 22. 
    Dannenberg J-H, van Rossum A, Schuijff L, te Riele H. 2000. Ablation of the retinoblastoma gene family deregulates G1 control causing immortalization and increased cell turnover under growth-restricting conditions. Genes Dev 14:3051–64
    [Google Scholar]
  23. 23. 
    DeCaprio JA. 2009. How the Rb tumor suppressor structure and function was revealed by the study of Adenovirus and SV40. Virology 384:274–84
    [Google Scholar]
  24. 24. 
    DeCaprio JA. 2014. Human papillomavirus type 16 E7 perturbs DREAM to promote cellular proliferation and mitotic gene expression. Oncogene 33:4036–38
    [Google Scholar]
  25. 25. 
    DeCaprio JA, Duensing A. 2014. The DREAM complex in antitumor activity of imatinib mesylate in gastrointestinal stromal tumors. Curr. Opin. Oncol. 26:415–21
    [Google Scholar]
  26. 26. 
    DeGregori J. 2002. The genetics of the E2F family of transcription factors: shared functions and unique roles. Biochim. Biophys. Acta Rev. Cancer 1602:131–50
    [Google Scholar]
  27. 27. 
    Dick FA, Goodrich DW, Sage J, Dyson NJ 2018. Non-canonical functions of the RB protein in cancer. Nat. Rev. Cancer 18:442–51
    [Google Scholar]
  28. 28. 
    Dimova DK, Dyson NJ. 2005. The E2F transcriptional network: old acquaintances with new faces. Oncogene 24:2810–26
    [Google Scholar]
  29. 29. 
    Down CF, Millour J, Lam EW-F, Watson RJ. 2012. Binding of FoxM1 to G2/M gene promoters is dependent upon B-Myb. Biochim. Biophys. Acta Gene Regul. Mech. 1819:855–62
    [Google Scholar]
  30. 30. 
    Duchon A, Herault Y. 2016. DYRK1A, a dosage-sensitive gene involved in neurodevelopmental disorders, is a target for drug development in Down syndrome. Front. Behav. Neurosci. 10:104
    [Google Scholar]
  31. 31. 
    Dynlacht BD, Brook A, Dembski M, Yenush L, Dyson N 1994. DNA-binding and trans-activation properties of Drosophila E2F and DP proteins. PNAS 91:6359–63
    [Google Scholar]
  32. 32. 
    Dyson N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev 12:2245–62
    [Google Scholar]
  33. 33. 
    Dyson NJ. 2016. RB1: a prototype tumor suppressor and an enigma. Genes Dev 30:1492–502
    [Google Scholar]
  34. 34. 
    Engeland K. 2018. Cell cycle arrest through indirect transcriptional repression by p53: I have a DREAM. Cell Death Differ 25:114–32
    [Google Scholar]
  35. 35. 
    Ewton DZ, Hu J, Vilenchik M, Deng X, Luk K-c et al. 2011. Inactivation of Mirk/dyrk1b kinase targets quiescent pancreatic cancer cells. Mol. Cancer Ther. 10:2104–14
    [Google Scholar]
  36. 36. 
    Fay DS, Han M. 2000. The synthetic multivulval genes of C. elegans: functional redundancy, Ras-antagonism, and cell fate determination. Genesis 26:279–84
    [Google Scholar]
  37. 37. 
    Fischer M, Grossmann P, Padi M, DeCaprio JA 2016. Integration of TP53, DREAM, MMB-FOXM1 and RB-E2F target gene analyses identifies cell cycle gene regulatory networks. Nucleic Acids Res 44:6070–86
    [Google Scholar]
  38. 38. 
    Fischer M, Grundke I, Sohr S, Quaas M, Hoffmann S et al. 2013. p53 and cell cycle dependent transcription of kinesin family member 23 (KIF23) is controlled via a CHR promoter element bound by DREAM and MMB complexes. PLOS ONE 8:e63187
    [Google Scholar]
  39. 39. 
    Fischer M, Quaas M, Steiner L, Engeland K. 2016. The p53-p21-DREAM-CDE/CHR pathway regulates G2/M cell cycle genes. Nucleic Acids Res 44:164–74
    [Google Scholar]
  40. 40. 
    Florens L, Washburn MP. 2006. Proteomic analysis by multidimensional protein identification technology. Methods Mol. Biol. 328:159–75
    [Google Scholar]
  41. 41. 
    Forristal C, Henley SA, MacDonald JI, Bush JR, Ort C et al. 2014. Loss of the mammalian DREAM complex deregulates chondrocyte proliferation. Mol. Cell. Biol. 34:2221–34
    [Google Scholar]
  42. 42. 
    Friedman E. 2013. Mirk/dyrk1B kinase in ovarian cancer. Int. J. Mol. Sci. 14:5560–75
    [Google Scholar]
  43. 43. 
    Friend SH, Bernards R, Rogelj S, Weinberg RA, Rapaport JM et al. 1986. A human DNA segment with properties of the gene that predisposes to retinoblastoma and osteosarcoma. Nature 323:643–46
    [Google Scholar]
  44. 44. 
    Gagrica S, Hauser S, Kolfschoten I, Osterloh L, Agami R, Gaubatz S 2004. Inhibition of oncogenic transformation by mammalian Lin-9, a pRB-associated protein. EMBO J 23:4627–38
    [Google Scholar]
  45. 45. 
    Georlette D, Ahn S, MacAlpine DM, Cheung E, Lewis PW et al. 2007. Genomic profiling and expression studies reveal both positive and negative activities for the Drosophila Myb–MuvB/dREAM complex in proliferating cells. Genes Dev 21:2880–96
    [Google Scholar]
  46. 46. 
    Goetsch PD, Garrigues JM, Strome S. 2017. Loss of the Caenorhabditis elegans pocket protein LIN-35 reveals MuvB's innate function as the repressor of DREAM target genes. PLOS Genet 13:e1007088
    [Google Scholar]
  47. 47. 
    Gordon RR, Nelson PS. 2012. Cellular senescence and cancer chemotherapy resistance. Drug Resist. Updat. 15:123–31
    [Google Scholar]
  48. 48. 
    Guiley KZ, Iness AN, Saini S, Tripathi S, Lipsick JS et al. 2018. Structural mechanism of Myb–MuvB assembly. PNAS 115:10016–21
    [Google Scholar]
  49. 49. 
    Guiley KZ, Liban TJ, Felthousen JG, Ramanan P, Litovchick L, Rubin SM 2015. Structural mechanisms of DREAM complex assembly and regulation. Genes Dev 29:961–74
    [Google Scholar]
  50. 50. 
    Harrison MM, Ceol CJ, Lu X, Horvitz HR 2006. Some C. elegans class B synthetic multivulva proteins encode a conserved LIN-35 Rb-containing complex distinct from a NuRD-like complex. PNAS 103:16782–87
    [Google Scholar]
  51. 51. 
    Hiebert SW, Chellappan SP, Horowitz JM, Nevins JR. 1992. The interaction of RB with E2F coincides with an inhibition of the transcriptional activity of E2F. Genes Dev 6:177–85
    [Google Scholar]
  52. 52. 
    Himpel S, Tegge W, Frank R, Leder S, Joost HG, Becker W. 2000. Specificity determinants of substrate recognition by the protein kinase DYRK1A. J. Biol. Chem. 275:2431–38
    [Google Scholar]
  53. 53. 
    Hu J, Deng H, Friedman EA. 2013. Ovarian cancer cells, not normal cells, are damaged by Mirk/Dyrk1B kinase inhibition. Int. J. Cancer 132:2258–69
    [Google Scholar]
  54. 54. 
    Iness AN, Felthousen J, Ananthapadmanabhan V, Sesay F, Saini S et al. 2019. The cell cycle regulatory DREAM complex is disrupted by high expression of oncogenic B-Myb. Oncogene 38:1080–92
    [Google Scholar]
  55. 55. 
    Iness AN, Litovchick L. 2018. MuvB: a key to cell cycle control in ovarian cancer. Front. Oncol. 8:223
    [Google Scholar]
  56. 56. 
    Iness AN, Rubinsak L, Meas SJ, Chaoul J, Sayeed S 2021. Oncogenic B-Myb is associated with deregulation of the DREAM-mediated cell cycle gene expression program in high grade serous ovarian carcinoma clinical tumor samples. Front. Oncol. 11:637193
    [Google Scholar]
  57. 57. 
    James CD, Saini S, Sesay F, Ko K, Felthousen-Rusbasan J et al. 2021. Restoring the DREAM complex inhibits the proliferation of high-risk HPV positive human cells. Cancers 13:489
    [Google Scholar]
  58. 58. 
    Joaquin M, Bessa M, Saville MK, Watson RJ. 2002. B-Myb overcomes a p107-mediated cell proliferation block by interacting with an N-terminal domain of p107. Oncogene 21:7923–32
    [Google Scholar]
  59. 59. 
    Kerkhoff E, Fedorov LM, Siefken R, Walter AO, Papadopoulos T, Rapp UR 2000. Lung-targeted expression of the c-Raf-1 kinase in transgenic mice exposes a novel oncogenic character of the wild-type protein. Cell Growth Differ 11:185–90
    [Google Scholar]
  60. 60. 
    Kim H, Lee KS, Kim AK, Choi M, Choi K et al. 2016. A chemical with proven clinical safety rescues Down-syndrome-related phenotypes in through DYRK1A inhibition. Dis. Model. Mech. 9:839–48
    [Google Scholar]
  61. 61. 
    Kim MJ, Cervantes C, Jung Y-S, Zhang X, Zhang J et al. 2021. PAF remodels the DREAM complex to bypass cell quiescence and promote lung tumorigenesis. Mol. Cell 81:81698–714.e6
    [Google Scholar]
  62. 62. 
    Kittler R, Pelletier L, Heninger AK, Slabicki M, Theis M et al. 2007. Genome-scale RNAi profiling of cell division in human tissue culture cells. Nat. Cell Biol. 9:1401–12
    [Google Scholar]
  63. 63. 
    Kleinschmidt MA, Wagner TU, Liedtke D, Spahr S, Samans B, Gaubatz S. 2009. lin9 is required for mitosis and cell survival during early zebrafish development. J. Biol. Chem. 284:13119–27
    [Google Scholar]
  64. 64. 
    Knight AS, Notaridou M, Watson RJ. 2009. A Lin-9 complex is recruited by B-Myb to activate transcription of G2/M genes in undifferentiated embryonal carcinoma cells. Oncogene 28:1737–47
    [Google Scholar]
  65. 65. 
    Kobayashi K, Suzuki T, Iwata E, Nakamichi N, Suzuki T et al. 2015. Transcriptional repression by MYB3R proteins regulates plant organ growth. EMBO J 34:1992–2007
    [Google Scholar]
  66. 66. 
    Korenjak M, Taylor-Harding B, Binne UK, Satterlee JS, Stevaux O et al. 2004. Native E2F/RBF complexes contain Myb-interacting proteins and repress transcription of developmentally controlled E2F target genes. Cell 119:181–93
    [Google Scholar]
  67. 67. 
    Laoukili J, Kooistra MRH, Brás A, Kauw J, Kerkhoven RM et al. 2005. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat. Cell Biol. 7:126–36
    [Google Scholar]
  68. 68. 
    Lee WH, Bookstein R, Hong F, Young LJ, Shew JY, Lee EY. 1987. Human retinoblastoma susceptibility gene: cloning, identification, and sequence. Science 235:1394–99
    [Google Scholar]
  69. 69. 
    Lewis PW, Beall EL, Fleischer TC, Georlette D, Link AJ, Botchan MR. 2004. Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex. Genes Dev 18:2929–40
    [Google Scholar]
  70. 70. 
    Li X, Wang W, Wang J, Malovannaya A, Xi Y et al. 2015. Proteomic analyses reveal distinct chromatin-associated and soluble transcription factor complexes. Mol. Syst. Biol. 11:775
    [Google Scholar]
  71. 71. 
    Liban TJ, Medina EM, Tripathi S, Sengupta S, Henry RW et al. 2017. Conservation and divergence of C-terminal domain structure in the retinoblastoma protein family. PNAS 114:4942–47
    [Google Scholar]
  72. 72. 
    Liban TJ, Thwaites MJ, Dick FA, Rubin SM 2016. Structural conservation and E2F binding specificity within the retinoblastoma pocket protein family. J. Mol. Biol. 428:3960–71
    [Google Scholar]
  73. 73. 
    Litovchick L, Chestukhin A, DeCaprio JA 2004. Glycogen synthase kinase 3 phosphorylates RBL2/p130 during quiescence. Mol. Cell. Biol. 24:8970–80
    [Google Scholar]
  74. 74. 
    Litovchick L, Florens LA, Swanson SK, Washburn MP, DeCaprio JA. 2011. DYRK1A protein kinase promotes quiescence and senescence through DREAM complex assembly. Genes Dev 25:801–13
    [Google Scholar]
  75. 75. 
    Litovchick L, Sadasivam S, Florens L, Zhu X, Swanson SK et al. 2007. Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol. Cell 26:539–51
    [Google Scholar]
  76. 76. 
    MacDonald J, Ramos-Valdes Y, Perampalam P, Litovchick L, DiMattia GE, Dick FA. 2017. A systematic analysis of negative growth control implicates the DREAM complex in cancer cell dormancy. Mol. Cancer Res. 15:371–81
    [Google Scholar]
  77. 77. 
    MacPherson D. 2008. Insights from mouse models into human retinoblastoma. Cell Div 3:9
    [Google Scholar]
  78. 78. 
    Mages CFS, Wintsche A, Bernhart SH, Müller GA 2017. The DREAM complex through its subunit Lin37 cooperates with Rb to initiate quiescence. eLife 6:e26876
    [Google Scholar]
  79. 79. 
    Malumbres M, Barbacid M. 2001. To cycle or not to cycle: a critical decision in cancer. Nat. Rev. Cancer 1:222–31
    [Google Scholar]
  80. 80. 
    Mannefeld M, Klassen E, Gaubatz S. 2009. B-MYB is required for recovery from the DNA damage–induced G2 checkpoint in p53 mutant cells. Cancer Res 69:4073–80
    [Google Scholar]
  81. 81. 
    Marceau AH, Felthousen JG, Goetsch PD, Iness AN, Lee H-W et al. 2016. Structural basis for LIN54 recognition of CHR elements in cell cycle-regulated promoters. Nat. Commun. 7:12301
    [Google Scholar]
  82. 82. 
    Marescal O, Cheeseman IM. 2020. Cellular mechanisms and regulation of quiescence. Dev. Cell 55:259–71
    [Google Scholar]
  83. 83. 
    Matsuo T, Kuramoto H, Kumazaki T, Mitsui Y, Takahashi T. 2012. LIN54 harboring a mutation in CHC domain is localized to the cytoplasm and inhibits cell cycle progression. Cell Cycle 11:3227–36
    [Google Scholar]
  84. 84. 
    Mauro LJ, Seibel MI, Diep CH, Spartz A, Perez Kerkvliet C et al. 2021. Progesterone receptors promote quiescence and ovarian cancer cell phenotypes via DREAM in p53-mutant fallopian tube models. J. Clin. Endocrinol. Metab. 106:71929–55
    [Google Scholar]
  85. 85. 
    Menon VR, Ananthapadmanabhan V, Swanson S, Saini S, Sesay F et al. 2019. DYRK1A regulates the recruitment of 53BP1 to the sites of DNA damage in part through interaction with RNF169. Cell Cycle 18:531–51
    [Google Scholar]
  86. 86. 
    Müller GA, Engeland K. 2010. The central role of CDE/CHR promoter elements in the regulation of cell cycle-dependent gene transcription. FEBS J 277:877–93
    [Google Scholar]
  87. 87. 
    Müller GA, Quaas M, Schümann M, Krause E, Padi M et al. 2012. The CHR promoter element controls cell cycle–dependent gene transcription and binds the DREAM and MMB complexes. Nucleic Acids Res 40:1561–78
    [Google Scholar]
  88. 88. 
    Müller GA, Wintsche A, Stangner K, Prohaska SJ, Stadler PF, Engeland K. 2014. The CHR site: definition and genome-wide identification of a cell cycle transcriptional element. Nucleic Acids Res 42:10331–50
    [Google Scholar]
  89. 89. 
    Ning Y-Q, Liu N, Lan K-K, Su Y-N, Li L et al. 2020. DREAM complex suppresses DNA methylation maintenance genes and precludes DNA hypermethylation. Nat. Plants 6:942–56
    [Google Scholar]
  90. 90. 
    Nor Rashid N, Yusof R, Watson RJ 2011. Disruption of repressive p130–DREAM complexes by human papillomavirus 16 E6/E7 oncoproteins is required for cell-cycle progression in cervical cancer cells. J. Gen. Virol. 92:2620–27
    [Google Scholar]
  91. 91. 
    Odajima J, Saini S, Jung P, Ndassa-Colday Y, Ficaro S et al. 2016. Proteomic landscape of tissue-specific cyclin E functions in vivo. PLOS Genet 12:e1006429
    [Google Scholar]
  92. 92. 
    Ogawa Y, Nonaka Y, Goto T, Ohnishi E, Hiramatsu T et al. 2010. Development of a novel selective inhibitor of the Down syndrome-related kinase Dyrk1A. Nat. Commun. 1:86
    [Google Scholar]
  93. 93. 
    Osterloh L, von Eyss B, Schmit F, Rein L, Hübner D et al. 2007. The human synMuv-like protein LIN-9 is required for transcription of G2/M genes and for entry into mitosis. EMBO J 26:144–57
    [Google Scholar]
  94. 94. 
    Pardee AB. 1989. G1 events and regulation of cell proliferation. Science 246:603–8
    [Google Scholar]
  95. 95. 
    Patel AJ, Wan YW, Al-Ouran R, Revelli JP, Cardenas MF et al. 2019. Molecular profiling predicts meningioma recurrence and reveals loss of DREAM complex repression in aggressive tumors. PNAS 116:21715–26
    [Google Scholar]
  96. 96. 
    Pattschull G, Walz S, Gründl M, Schwab M, Rühl E et al. 2019. The Myb-MuvB complex is required for YAP-dependent transcription of mitotic genes. Cell Rep 27:3533–46.e7
    [Google Scholar]
  97. 97. 
    Perampalam P, Hassan HM, Lilly GE, Passos DT, Torchia J et al. 2021. Disrupting the DREAM transcriptional repressor complex induces apolipoprotein overexpression and systemic amyloidosis in mice. J. Clin. Invest. 131:e140903
    [Google Scholar]
  98. 98. 
    Pilkinton M, Sandoval R, Colamonici OR. 2007. Mammalian Mip/LIN-9 interacts with either the p107, p130/E2F4 repressor complex or B-Myb in a cell cycle-phase-dependent context distinct from the Drosophila dREAM complex. Oncogene 26:7535–43
    [Google Scholar]
  99. 99. 
    Quaas M, Müller GA, Engeland K. 2012. p53 can repress transcription of cell cycle genes through a p21WAF1/CIP1-dependent switch from MMB to DREAM protein complex binding at CHR promoter elements. Cell Cycle 11:4661–72
    [Google Scholar]
  100. 100. 
    Rayman JB, Takahashi Y, Indjeian VB, Dannenberg J-H, Catchpole S et al. 2002. E2F mediates cell cycle-dependent transcriptional repression in vivo by recruitment of an HDAC1/mSin3B corepressor complex. Genes Dev 16:933–47
    [Google Scholar]
  101. 101. 
    Reichert N, Wurster S, Ulrich T, Schmitt K, Hauser S et al. 2010. Lin9, a subunit of the mammalian DREAM complex, is essential for embryonic development, for survival of adult mice, and for tumor suppression. Mol. Cell. Biol. 30:2896–908
    [Google Scholar]
  102. 102. 
    Roberts MS, Sahni JM, Schrock MS, Piemonte KM, Weber-Bonk KL et al. 2020. LIN9 and NEK2 are core regulators of mitotic fidelity that can be therapeutically targeted to overcome taxane resistance. Cancer Res 80:1693–706
    [Google Scholar]
  103. 103. 
    Rubin SM, Gall A-L, Zheng N, Pavletich NP 2005. Structure of the Rb C-terminal domain bound to E2F1-DP1: a mechanism for phosphorylation-induced E2F release. Cell 123:1093–106
    [Google Scholar]
  104. 104. 
    Rubin SM, Sage J, Skotheim JM 2020. Integrating old and new paradigms of G1/S control. Mol. Cell 80:183–92
    [Google Scholar]
  105. 105. 
    Sadasivam S, Duan S, DeCaprio JA 2012. The MuvB complex sequentially recruits B-Myb and FoxM1 to promote mitotic gene expression. Genes Dev 26:474–89
    [Google Scholar]
  106. 106. 
    Sage J, Mulligan GJ, Attardi LD, Miller A, Chen S et al. 2000. Targeted disruption of the three Rb-related genes leads to loss of G1 control and immortalization. Genes Dev 14:3037–50
    [Google Scholar]
  107. 107. 
    Sahni JM, Gayle SS, Webb BM, Weber-Bonk KL, Seachrist DD et al. 2017. Mitotic vulnerability in triple-negative breast cancer associated with LIN9 is targetable with BET inhibitors. Cancer Res 77:5395–408
    [Google Scholar]
  108. 108. 
    Sala A, De Luca A, Giordano A, Peschle C 1996. The retinoblastoma family member p107 binds to B-MYB and suppresses its autoregulatory activity. J. Biol. Chem. 271:28738–40
    [Google Scholar]
  109. 109. 
    Sandoval R, Pilkinton M, Colamonici OR 2009. Deletion of the p107/p130-binding domain of Mip130/LIN-9 bypasses the requirement for CDK4 activity for the dissociation of Mip130/LIN-9 from p107/p130-E2F4 complex. Exp. Cell Res. 315:2914–20
    [Google Scholar]
  110. 110. 
    Sanidas I, Morris R, Fella KA, Rumde PH, Boukhali M et al. 2019. A code of mono-phosphorylation modulates the function of RB. Mol. Cell 73:985–1000.e6
    [Google Scholar]
  111. 111. 
    Schade AE, Oser MG, Nicholson HE, DeCaprio JA. 2019. Cyclin D–CDK4 relieves cooperative repression of proliferation and cell cycle gene expression by DREAM and RB. Oncogene 38:4962–76
    [Google Scholar]
  112. 112. 
    Schmit F, Cremer S, Gaubatz S. 2009. LIN54 is an essential core subunit of the DREAM/LINC complex that binds to the cdc2 promoter in a sequence-specific manner. FEBS J 276:5703–16
    [Google Scholar]
  113. 113. 
    Schmit F, Korenjak M, Mannefeld M, Schmitt K, Franke C et al. 2007. LINC, a human complex that is related to pRB-containing complexes in invertebrates regulates the expression of G2/M genes. Cell Cycle 6:1903–13
    [Google Scholar]
  114. 114. 
    Shin H, Reiner DJ. 2018. The signaling network controlling C. elegans vulval cell fate patterning. J. Dev. Biol. 6:30
    [Google Scholar]
  115. 115. 
    Simmons AR, Davies KA, Wang W, Liu Z, Bergmann DC 2019. SOL1 and SOL2 regulate fate transition and cell divisions in the Arabidopsis stomatal lineage. Development 146:3dev171066
    [Google Scholar]
  116. 116. 
    Solin LJ, Gray R, Baehner FL, Butler SM, Hughes LL et al. 2013. A multigene expression assay to predict local recurrence risk for ductal carcinoma in situ of the breast. J. Natl. Cancer Inst. 105:701–10
    [Google Scholar]
  117. 117. 
    Stiegler P, Kasten M, Giordano A. 1998. The RB family of cell cycle regulatory factors. J. Cell Biochem. Suppl.30–31–30–36
    [Google Scholar]
  118. 118. 
    Tabuchi TM, Deplancke B, Osato N, Zhu LJ, Barrasa MI et al. 2011. Chromosome-biased binding and gene regulation by the Caenorhabditis elegans DRM complex. PLOS Genet 7:e1002074
    [Google Scholar]
  119. 119. 
    Tanaka Y, Patestos NP, Maekawa T, Ishii S 1999. B-myb is required for inner cell mass formation at an early stage of development. J. Biol. Chem. 274:28067–70
    [Google Scholar]
  120. 120. 
    Tassi RA, Todeschini P, Siegel ER, Calza S, Cappella P et al. 2017. FOXM1 expression is significantly associated with chemotherapy resistance and adverse prognosis in non-serous epithelial ovarian cancer patients. J. Exp. Clin. Cancer Res. 36:63
    [Google Scholar]
  121. 121. 
    Trimarchi JM, Lees JA. 2002. Sibling rivalry in the E2F family. Nat. Rev. Mol. Cell Biol. 3:11–20
    [Google Scholar]
  122. 122. 
    Uxa S, Bernhart SH, Mages CFS, Fischer M, Kohler R et al. 2019. DREAM and RB cooperate to induce gene repression and cell-cycle arrest in response to p53 activation. Nucleic Acids Res 47:9087–103
    [Google Scholar]
  123. 123. 
    van den Heuvel S, Dyson NJ. 2008. Conserved functions of the pRB and E2F families. Nat. Rev. Mol. Cell Biol. 9:713–24
    [Google Scholar]
  124. 124. 
    Viens LJ, Henley SJ, Watson M, Markowitz LE, Thomas CC et al. 2016. Human papillomavirus-associated cancers—United States, 2008–2012. Morb. Mortal. Wkly. Rep. 65:661–66
    [Google Scholar]
  125. 125. 
    Vorster PJ, Goetsch P, Wijeratne TU, Guiley KZ, Andrejka L et al. 2020. A long lost key opens an ancient lock: Drosophila Myb causes a synthetic multivulval phenotype in nematodes. Biol. Open 9:bio051508
    [Google Scholar]
  126. 126. 
    Wang W, Sijacic P, Xu P, Lian H, Liu Z. 2018. Arabidopsis TSO1 and MYB3R1 form a regulatory module to coordinate cell proliferation with differentiation in shoot and root. PNAS 115:13E3045–54
    [Google Scholar]
  127. 127. 
    Wang Y, Wen L, Zhao SH, Ai Z, Guo JZ, Liu WC. 2013. FoxM1 expression is significantly associated with cisplatin-based chemotherapy resistance and poor prognosis in advanced non-small cell lung cancer patients. Lung Cancer 79:173–79
    [Google Scholar]
  128. 128. 
    Wen H, Andrejka L, Ashton J, Karess R, Lipsick JS 2008. Epigenetic regulation of gene expression by Drosophila Myb and E2F2-RBF via the Myb-MuvB/dREAM complex. Genes Dev 22:601–14
    [Google Scholar]
  129. 129. 
    Wikenheiser-Brokamp KA. 2004. Rb family proteins differentially regulate distinct cell lineages during epithelial development. Development 131:4299–310
    [Google Scholar]
  130. 130. 
    Yu P, Huang B, Shen M, Lau C, Chan E et al. 2001. p15PAF, a novel PCNA associated factor with increased expression in tumor tissues. Oncogene 20:484–89
    [Google Scholar]
  131. 131. 
    Zhang X, Cheng L, Minn K, Madan R, Godwin AK et al. 2014. Targeting of mutant p53-induced FoxM1 with thiostrepton induces cytotoxicity and enhances carboplatin sensitivity in cancer cells. Oncotarget 5:11365–80
    [Google Scholar]
  132. 132. 
    Zluhan-Martínez E, Pérez-Koldenkova V, Ponce-Castañeda MV, Sánchez MP, García-Ponce B et al. 2020. Beyond what your retina can see: similarities of retinoblastoma function between plants and animals, from developmental processes to epigenetic regulation. Int. J. Mol. Sci. 21:4925
    [Google Scholar]
  133. 133. 
    zur Hausen H. 2009. Papillomaviruses in the causation of human cancers—a brief historical account. Virology 384:260–65
    [Google Scholar]
/content/journals/10.1146/annurev-genet-071819-103836
Loading
/content/journals/10.1146/annurev-genet-071819-103836
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error