67
Views
23
CrossRef citations to date
0
Altmetric
Article

Loss of the Mammalian DREAM Complex Deregulates Chondrocyte Proliferation

, , , , , , , , , , , , , , & show all
Pages 2221-2234 | Received 18 Nov 2013, Accepted 27 Mar 2014, Published online: 20 Mar 2023

REFERENCES

  • Lipsick JS. 2004. synMuv verite—Myb comes into focus. Genes Dev. 18:2837–2844. http://dx.doi.org/10.1101/gad.1274804.
  • Sadasivam S, DeCaprio JA. 2013. The DREAM complex: master coordinator of cell cycle-dependent gene expression. Nat. Rev. Cancer. 13:585–595. http://dx.doi.org/10.1038/nrc3556.
  • Ferguson EL, Horvitz HR. 1989. The multivulva phenotype of certain Caenorhabditis elegans mutants results from defects in two functionally redundant pathways. Genetics 123:109–121.
  • Ceol CJ, Horvitz HR. 2004. A new class of C. elegans synMuv genes implicates a Tip60/NuA4-like HAT complex as a negative regulator of Ras signaling. Dev. Cell 6:563–576. http://dx.doi.org/10.1016/S1534-5807(04)00065-6.
  • 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. Proc. Natl. Acad. Sci. U. S. A. 103:16782–16787. http://dx.doi.org/10.1073/pnas.0608461103.
  • Korenjak M, Taylor-Harding B, Binne UK, Satterlee JS, Stevaux O, Aasland R, White-Cooper H, Dyson N, Brehm A. 2004. Native E2F/RBF complexes contain Myb-interacting proteins and repress transcription of developmentally controlled E2F target genes. Cell 119:181–193. http://dx.doi.org/10.1016/j.cell.2004.09.034.
  • 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. 18:2929–2940. http://dx.doi.org/10.1101/gad.1255204.
  • 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 7:461–473. http://dx.doi.org/10.1016/S1097-2765(01)00194-0.
  • Lu X, Horvitz HR. 1998. lin-35 and lin-53, two genes that antagonize a C. elegans Ras pathway, encode proteins similar to Rb and its binding protein RbAp48. Cell 95:981–991. http://dx.doi.org/10.1016/S0092-8674(00)81722-5.
  • 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 420:833–837. http://dx.doi.org/10.1038/nature01228.
  • Lee H, Ragusano L, Martinez A, Gill J, Dimova DK. 2012. A dual role for the dREAM/MMB complex in the regulation of differentiation-specific E2F/RB target genes. Mol. Cell. Biol. 32:2110–2120. http://dx.doi.org/10.1128/MCB.06314-11.
  • Litovchick L, Sadasivam S, Florens L, Zhu X, Swanson SK, Velmurugan S, Chen R, Washburn MP, Liu XS, DeCaprio JA. 2007. Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol. Cell 26:539–551. http://dx.doi.org/10.1016/j.molcel.2007.04.015.
  • 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 26:7535–7543. http://dx.doi.org/10.1038/sj.onc.1210562.
  • Schmit F, Korenjak M, Mannefeld M, Schmitt K, Franke C, von Eyss B, Gagrica S, Hanel F, Brehm A, Gaubatz S. 2007. LINC, a human complex that is related to pRB-containing complexes in invertebrates regulates the expression of G2/M genes. Cell Cycle 6:1903–1913. http://dx.doi.org/10.4161/cc.6.15.4512.
  • Osterloh L, von Eyss B, Schmit F, Rein L, Hubner D, Samans B, Hauser S, Gaubatz S. 2007. The human synMuv-like protein LIN-9 is required for transcription of G2/M genes and for entry into mitosis. EMBO J. 26:144–157. http://dx.doi.org/10.1038/sj.emboj.7601478.
  • Sadasivam S, Duan S, DeCaprio JA. 2012. The MuvB complex sequentially recruits B-Myb and FoxM1 to promote mitotic gene expression. Genes Dev. 26:474–489. http://dx.doi.org/10.1101/gad.181933.111.
  • Litovchick L, Florens LA, Swanson SK, Washburn MP, DeCaprio JA. 2011. DYRK1A protein kinase promotes quiescence and senescence through DREAM complex assembly. Genes Dev. 25:801–813. http://dx.doi.org/10.1101/gad.2034211.
  • 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 28:1737–1747. http://dx.doi.org/10.1038/onc.2009.22.
  • Pilkinton M, Sandoval R, Song J, Ness SA, Colamonici OR. 2007. Mip/LIN-9 regulates the expression of B-Myb and the induction of cyclin A, cyclin B, and CDK1. J. Biol. Chem. 282:168–175. http://dx.doi.org/10.1074/jbc.M609924200.
  • Reichert N, Wurster S, Ulrich T, Schmitt K, Hauser S, Probst L, Gotz R, Ceteci F, Moll R, Rapp U, Gaubatz S. 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. 30:2896–2908. http://dx.doi.org/10.1128/MCB.00028-10.
  • Calbo J, Parreno M, Sotillo E, Yong T, Mazo A, Garriga J, Grana X. 2002. G1 cyclin/cyclin-dependent kinase-coordinated phosphorylation of endogenous pocket proteins differentially regulates their interactions with E2F4 and E2F1 and gene expression. J. Biol. Chem. 277:50263–50274. http://dx.doi.org/10.1074/jbc.M209181200.
  • Kurimchak A, Haines DS, Garriga J, Wu S, De Luca F, Sweredoski MJ, Deshaies RJ, Hess S, Grana X. 2013. Activation of p107 by fibroblast growth factor, which is essential for chondrocyte cell cycle exit, is mediated by the protein phosphatase 2A/B55α holoenzyme. Mol. Cell. Biol. 33:3330–3342. http://dx.doi.org/10.1128/MCB.00082-13.
  • Lee EY, Cam H, Ziebold U, Rayman JB, Lees JA, Dynlacht BD. 2002. E2F4 loss suppresses tumorigenesis in Rb mutant mice. Cancer Cell 2:463–472. http://dx.doi.org/10.1016/S1535-6108(02)00207-6.
  • Cobrinik D, Lee MH, Hannon G, Mulligan G, Bronson RT, Dyson N, Harlow E, Beach D, Weinberg RA, Jacks T. 1996. Shared role of the pRB-related p130 and p107 proteins in limb development. Genes Dev. 10:1633–1644. http://dx.doi.org/10.1101/gad.10.13.1633.
  • Lee M-H, Williams BO, Mulligan G, Mukai S, Bronson RT, Dyson N, Harlow E, Jacks T. 1996. Targeted disruption of p107: functional overlap between p107 and Rb. Genes Dev. 10:1621–1632. http://dx.doi.org/10.1101/gad.10.13.1621.
  • Laplantine E, Rossi F, Sahni M, Basilico C, Cobrinik D. 2002. FGF signaling targets the pRb-related p107 and p130 proteins to induce chondrocyte growth arrest. J. Cell Biol. 158:741–750. http://dx.doi.org/10.1083/jcb.200205025.
  • LeCouter JE. 1998. Strain-dependent embryonic lethality in mice lacking the retinoblastoma-related p130 gene. Development 125:4669–4679.
  • LeCouter JE, Kablar B, Hardy WR, Ying C, Megeney LA, May LL, Rudnicki MA. 1998. Strain-dependent myeloid hyperplasia, growth deficiency, and accelerated cell cycle in mice lacking the Rb-related p107 gene. Mol. Cell. Biol. 18:7455–7465.
  • Hurford RKJr, Cobrinik D, Lee MH, Dyson N. 1997. pRB and p107/p130 are required for the regulated expression of different sets of E2F responsive genes. Genes Dev. 11:1447–1463. http://dx.doi.org/10.1101/gad.11.11.1447.
  • Mulligan GJ, Wong J, Jacks T. 1998. p130 is dispensable in peripheral T lymphocytes: evidence for functional compensation by p107 and pRB. Mol. Cell. Biol. 18:206–220.
  • Cecchini MJ, Dick FA. 2011. The biochemical basis of CDK phosphorylation-independent regulation of E2F1 by the retinoblastoma protein. Biochem. J. 434:297–308. http://dx.doi.org/10.1042/BJ20101210.
  • Lakso M, Pichel JG, Gorman JR, Sauer B, Okamoto Y, Lee E, Alt FW, Westphal H. 1996. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl. Acad. Sci. U. S. A. 93:5860–5865. http://dx.doi.org/10.1073/pnas.93.12.5860.
  • Cecchini MJ, Amiri M, Dick FA. 2012. Analysis of cell cycle position in mammalian cells. J. Vis. Exp. 59:pii3491. http://dx.doi.org/10.3791/3491.
  • Talluri S, Dick FA. 2014. The retinoblastoma protein and PML collaborate to organize heterochromatin and silence E2F-responsive genes during senescence. Cell Cycle 13:641–651. http://dx.doi.org/10.4161/cc.27527.
  • McLeod MJ. 1980. Differential staining of cartilage and bone in whole mouse fetuses by Alcian blue and alizarin red S. Teratology 22:299–301. http://dx.doi.org/10.1002/tera.1420220306.
  • Ulici V, Hoenselaar KD, Agoston H, McErlain DD, Umoh J, Chakrabarti S, Holdsworth DW, Beier F. 2009. The role of Akt1 in terminal stages of endochondral bone formation: angiogenesis and ossification. Bone 45:1133–1145. http://dx.doi.org/10.1016/j.bone.2009.08.003.
  • Gillespie JR, Ulici V, Dupuis H, Higgs A, Dimattia A, Patel S, Woodgett JR, Beier F. 2011. Deletion of glycogen synthase kinase-3β in cartilage results in up-regulation of glycogen synthase kinase-3α protein expression. Endocrinology 152:1755–1766. http://dx.doi.org/10.1210/en.2010-1412.
  • Umoh JU, Sampaio AV, Welch I, Pitelka V, Goldberg HA, Underhill TM, Holdsworth DW. 2009. In vivo micro-CT analysis of bone remodeling in a rat calvarial defect model. Phys. Med. Biol. 54:2147–2161. http://dx.doi.org/10.1088/0031-9155/54/7/020.
  • Agoston H, Khan S, James CG, Gillespie JR, Serra R, Stanton LA, Beier F. 2007. C-type natriuretic peptide regulates endochondral bone growth through p38 MAP kinase-dependent and -independent pathways. BMC Dev. Biol. 7:18. http://dx.doi.org/10.1186/1471-213X-7-18.
  • Ulici V, Hoenselaar KD, Gillespie JR, Beier F. 2008. The PI3K pathway regulates endochondral bone growth through control of hypertrophic chondrocyte differentiation. BMC Dev. Biol. 8:40. http://dx.doi.org/10.1186/1471-213X-8-40.
  • Dick FA. 2007. Structure-function analysis of the retinoblastoma tumor suppressor protein: is the whole a sum of its parts? Cell Div. 2:26. http://dx.doi.org/10.1186/1747-1028-2-26.
  • Dick FA, Rubin SM. 2013. Molecular mechanisms underlying RB protein function. Nat. Rev. Mol. Cell Biol. 14:297–306. http://dx.doi.org/10.1038/nrm3567.
  • Bourgo RJ, Thangavel C, Ertel A, Bergseid J, McClendon AK, Wilkens L, Witkiewicz AK, Wang JY, Knudsen ES. 2011. RB restricts DNA damage-initiated tumorigenesis through an LXCXE-dependent mechanism of transcriptional control. Mol. Cell 43:663–672. http://dx.doi.org/10.1016/j.molcel.2011.06.029.
  • Ferreira R, Magnaghi-Jaulin L, Robin P, Harel-Bellan A, Trouche D. 1998. The three members of the pocket proteins family share the ability to repress E2F activity through recruitment of a histone deacetylase. Proc. Natl. Acad. Sci. U. S. A. 95:10493–10498. http://dx.doi.org/10.1073/pnas.95.18.10493.
  • Luo RX, Postigo AA, Dean DC. 1998. Rb interacts with histone deacetylase to repress transcription. Cell 92:463–473. http://dx.doi.org/10.1016/S0092-8674(00)80940-X.
  • Magnaghi-Jaulin L, Groisman R, Naguibneva I, Robin P, Lorain S, Le Villain JP, Troalen F, Trouche D, Harel-Bellan A. 1998. Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature 391:601–605. http://dx.doi.org/10.1038/35410.
  • Fine DA, Rozenblatt-Rosen O, Padi M, Korkhin A, James RL, Adelmant G, Yoon R, Guo L, Berrios C, Zhang Y, Calderwood MA, Velmurgan S, Cheng J, Marto JA, Hill DE, Cusick ME, Vidal M, Florens L, Washburn MP, Litovchick L, DeCaprio JA. 2012. Identification of FAM111A as an SV40 host range restriction and adenovirus helper factor. PLoS Pathog. 8:e1002949. http://dx.doi.org/10.1371/journal.ppat.1002949.
  • 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. 92:2620–2627. http://dx.doi.org/10.1099/vir.0.035352-0.
  • Dick FA, Sailhamer E, Dyson NJ. 2000. Mutagenesis of the pRB pocket reveals that cell cycle arrest functions are separable from binding to viral oncoproteins. Mol. Cell. Biol. 20:3715–3727. http://dx.doi.org/10.1128/MCB.20.10.3715-3727.2000.
  • Moberg K, Starz MA, Lees JA. 1996. E2F-4 switches from p130 to p107 and pRB in response to cell cycle reentry. Mol. Cell. Biol. 16:1436–1449.
  • Takahashi Y, Rayman JB, Dynlacht BD. 2000. Analysis of promoter binding by the E2F and pRB families in vivo: distinct E2F proteins mediate activation and repression. Genes Dev. 14:804–816.
  • Wells J, Boyd K, Fry C, Bartley S, Farnham P. 2000. Target gene specificity of E2F and pocket protein family members in living cells. Mol. Cell. Biol. 20:5797–5807. http://dx.doi.org/10.1128/MCB.20.16.5797-5807.2000.
  • 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. 14:3051–3064. http://dx.doi.org/10.1101/gad.847700.
  • Sage J, Mulligan G, Attardi L, Miller A, Chen S, Williams B, Theodorou E, Jacks T. 2000. Targeted disruption of the three Rb-related genes leads to loss of G1 control and immortalization. Genes Dev. 14:3037–3050. http://dx.doi.org/10.1101/gad.843200.
  • Rossi F, MacLean HE, Yuan W, Francis RO, Semenova E, Lin CS, Kronenberg HM, Cobrinik D. 2002. p107 and p130 Coordinately regulate proliferation, Cbfa1 expression, and hypertrophic differentiation during endochondral bone development. Dev. Biol. 247:271–285. http://dx.doi.org/10.1006/dbio.2002.0691.
  • Henley SA, Dick FA. 2012. The retinoblastoma family of proteins and their regulatory functions in the mammalian cell division cycle. Cell Div. 7:10. http://dx.doi.org/10.1186/1747-1028-7-10.
  • Sim CK, Perry S, Tharadra SK, Lipsick JS, Ray A. 2012. Epigenetic regulation of olfactory receptor gene expression by the Myb-MuvB/dREAM complex. Genes Dev. 26:2483–2498. http://dx.doi.org/10.1101/gad.201665.112.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.