32
Views
8
CrossRef citations to date
0
Altmetric
Article

Inactivation of Rb and E2f8 Synergizes To Trigger Stressed DNA Replication during Erythroid Terminal Differentiation

, , , , , , , , & show all
Pages 2833-2847 | Received 13 Dec 2013, Accepted 13 May 2014, Published online: 20 Mar 2023

REFERENCES

  • Hattangadi SM, Wong P, Zhang L, Flygare J, Lodish HF. 2011. From stem cell to red cell: regulation of erythropoiesis at multiple levels by multiple proteins, RNAs, and chromatin modifications. Blood 118:6258–6268. http://dx.doi.org/10.1182/blood-2011-07-356006.
  • Steinman RA. 2002. Cell cycle regulators and hematopoiesis. Oncogene 21:3403–3413. http://dx.doi.org/10.1038/sj.onc.1205325.
  • Walkley CR, Sankaran VG, Orkin SH. 2008. Rb and hematopoiesis: stem cells to anemia. Cell Div. 3:13. http://dx.doi.org/10.1186/1747-1028-3-13.
  • Dyson N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev. 12:2245–2262. http://dx.doi.org/10.1101/gad.12.15.2245.
  • Nevins JR. 1998. Toward an understanding of the functional complexity of the E2F and retinoblastoma families. Cell Growth Differ. 9:585–593.
  • Clarke AR, Maandag ER, van Roon M, van der Lugt NM, van der Valk M, Hooper ML, Berns A, te Riele H. 1992. Requirement for a functional Rb-1 gene in murine development. Nature 359:328–330. http://dx.doi.org/10.1038/359328a0.
  • Jacks T, Fazeli A, Schmitt EM, Bronson RT, Goodell MA, Weinberg RA. 1992. Effects of an Rb mutation in the mouse. Nature 359:295–300. http://dx.doi.org/10.1038/359295a0.
  • Lee EY, Chang CY, Hu N, Wang YC, Lai CC, Herrup K, Lee WH, Bradley A. 1992. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359:288–294. http://dx.doi.org/10.1038/359288a0.
  • de Bruin A, Wu L, Saavedra HI, Wilson P, Yang Y, Rosol TJ, Weinstein M, Robinson ML, Leone G. 2003. Rb function in extraembryonic lineages suppresses apoptosis in the CNS of Rb-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 100:6546–6551. http://dx.doi.org/10.1073/pnas.1031853100.
  • Wu L, de Bruin A, Saavedra HI, Starovic M, Trimboli A, Yang Y, Opavska J, Wilson P, Thompson JC, Ostrowski MC, Rosol TJ, Woollett LA, Weinstein M, Cross JC, Robinson ML, Leone G. 2003. Extra-embryonic function of Rb is essential for embryonic development and viability. Nature 421:942–947. http://dx.doi.org/10.1038/nature01417.
  • Daria D, Filippi MD, Knudsen ES, Faccio R, Li Z, Kalfa T, Geiger H. 2008. The retinoblastoma tumor suppressor is a critical intrinsic regulator for hematopoietic stem and progenitor cells under stress. Blood 111:1894–1902. http://dx.doi.org/10.1182/blood-2007-02-071746.
  • Hu T, Ghazaryan S, Sy C, Wiedmeyer C, Chang V, Wu L. 2012. Concomitant inactivation of Rb and E2f8 in hematopoietic stem cells synergizes to induce severe anemia. Blood 119:4532–4542. http://dx.doi.org/10.1182/blood-2011-10-388231.
  • Sankaran VG, Orkin SH, Walkley CR. 2008. Rb intrinsically promotes erythropoiesis by coupling cell cycle exit with mitochondrial biogenesis. Genes Dev. 22:463–475. http://dx.doi.org/10.1101/gad.1627208.
  • Walkley CR, Shea JM, Sims NA, Purton LE, Orkin SH. 2007. Rb regulates interactions between hematopoietic stem cells and their bone marrow microenvironment. Cell 129:1081–1095. http://dx.doi.org/10.1016/j.cell.2007.03.055.
  • Iavarone A, King ER, Dai XM, Leone G, Stanley ER, Lasorella A. 2004. Retinoblastoma promotes definitive erythropoiesis by repressing Id2 in fetal liver macrophages. Nature 432:1040–1045. http://dx.doi.org/10.1038/nature03068.
  • Wenzel PL, Wu L, de Bruin A, Chong JL, Chen WY, Dureska G, Sites E, Pan T, Sharma A, Huang K, Ridgway R, Mosaliganti K, Sharp R, Machiraju R, Saltz J, Yamamoto H, Cross JC, Robinson ML, Leone G. 2007. Rb is critical in a mammalian tissue stem cell population. Genes Dev. 21:85–97. http://dx.doi.org/10.1101/gad.1485307.
  • Bracken AP, Ciro M, Cocito A, Helin K. 2004. E2F target genes: unraveling the biology. Trends Biochem. Sci. 29:409–417. http://dx.doi.org/10.1016/j.tibs.2004.06.006.
  • Chen HZ, Tsai SY, Leone G. 2009. Emerging roles of E2Fs in cancer: an exit from cell cycle control. Nat. Rev. Cancer 9:785–797. http://dx.doi.org/10.1038/nrc2696.
  • Dimova DK, Dyson NJ. 2005. The E2F transcriptional network: old acquaintances with new faces. Oncogene 24:2810–2826. http://dx.doi.org/10.1038/sj.onc.1208612.
  • Trimarchi JM, Lees JA. 2002. Sibling rivalry in the E2F family. Nat. Rev. Mol. Cell Biol. 3:11–20. http://dx.doi.org/10.1038/nrm714.
  • Trimarchi JM, Fairchild B, Wen J, Lees JA. 2001. The E2F6 transcription factor is a component of the mammalian Bmi1-containing polycomb complex. Proc. Natl. Acad. Sci. U. S. A. 98:1519–1524. http://dx.doi.org/10.1073/pnas.98.4.1519.
  • Chong JL, Tsai SY, Sharma N, Opavsky R, Price R, Wu L, Fernandez SA, Leone G. 2009. E2f3a and E2f3b contribute to the control of cell proliferation and mouse development. Mol. Cell. Biol. 29:414–424. http://dx.doi.org/10.1128/MCB.01161-08.
  • Dirlam A, Spike BT, Macleod KF. 2007. Deregulated E2f-2 underlies cell cycle and maturation defects in retinoblastoma null erythroblasts. Mol. Cell. Biol. 27:8713–8728. http://dx.doi.org/10.1128/MCB.01118-07.
  • 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.
  • Lee EY, Yuan TL, Danielian PS, West JC, Lees JA. 2009. E2F4 cooperates with pRB in the development of extra-embryonic tissues. Dev. Biol. 332:104–115. http://dx.doi.org/10.1016/j.ydbio.2009.05.541.
  • Parisi T, Yuan TL, Faust AM, Caron AM, Bronson R, Lees JA. 2007. Selective requirements for E2f3 in the development and tumorigenicity of Rb-deficient chimeric tissues. Mol. Cell. Biol. 27:2283–2293. http://dx.doi.org/10.1128/MCB.01854-06.
  • Saavedra HI, Wu L, de Bruin A, Timmers C, Rosol TJ, Weinstein M, Robinson ML, Leone G. 2002. Specificity of E2F1, E2F2, and E2F3 in mediating phenotypes induced by loss of Rb. Cell Growth Differ. 13:215–225. http://cgd.aacrjournals.org/cgi/content/full/13/5/215.
  • Ziebold U, Lee EY, Bronson RT, Lees JA. 2003. E2F3 loss has opposing effects on different pRB-deficient tumors, resulting in suppression of pituitary tumors but metastasis of medullary thyroid carcinomas. Mol. Cell. Biol. 23:6542–6552. http://dx.doi.org/10.1128/MCB.23.18.6542-6552.2003.
  • Ziebold U, Reza T, Caron A, Lees JA. 2001. E2F3 contributes both to the inappropriate proliferation and to the apoptosis arising in Rb mutant embryos. Genes Dev. 15:386–391. http://dx.doi.org/10.1101/gad.858801.
  • Heinrich AC, Pelanda R, Klingmuller U. 2004. A mouse model for visualization and conditional mutations in the erythroid lineage. Blood 104:659–666. http://dx.doi.org/10.1182/blood-2003-05-1442.
  • Kuhn R, Schwenk F, Aguet M, Rajewsky K. 1995. Inducible gene targeting in mice. Science 269:1427–1429. http://dx.doi.org/10.1126/science.7660125.
  • Li J, Ran C, Li E, Gordon F, Comstock G, Siddiqui H, Cleghorn W, Chen HZ, Kornacker K, Liu CG, Pandit SK, Khanizadeh M, Weinstein M, Leone G, de Bruin A. 2008. Synergistic function of E2F7 and E2F8 is essential for cell survival and embryonic development. Dev. Cell 14:62–75. http://dx.doi.org/10.1016/j.devcel.2007.10.017.
  • Vooijs M, te Riele H, van der Valk M, Berns A. 2002. Tumor formation in mice with somatic inactivation of the retinoblastoma gene in interphotoreceptor retinol binding protein-expressing cells. Oncogene 21:4635–4645. http://dx.doi.org/10.1038/sj.onc.1205575.
  • Liu J, Zhang J, Ginzburg Y, Li H, Xue F, De Franceschi L, Chasis JA, Mohandas N, An X. 2013. Quantitative analysis of murine terminal erythroid differentiation in vivo: novel method to study normal and disordered erythropoiesis. Blood 121:e43–e49. http://dx.doi.org/10.1182/blood-2012-09-456079.
  • Peslak SA, Wenger J, Bemis JC, Kingsley PD, Frame JM, Koniski AD, Chen Y, Williams JP, McGrath KE, Dertinger SD, Palis J. 2011. Sublethal radiation injury uncovers a functional transition during erythroid maturation. Exp. Hematol. 39:434–445. http://dx.doi.org/10.1016/j.exphem.2011.01.010.
  • McGrath KE, Bushnell TP, Palis J. 2008. Multispectral imaging of hematopoietic cells: where flow meets morphology. J. Immunol. Methods 336:91–97. http://dx.doi.org/10.1016/j.jim.2008.04.012.
  • Shuga J, Zhang J, Samson LD, Lodish HF, Griffith LG. 2007. In vitro erythropoiesis from bone marrow-derived progenitors provides a physiological assay for toxic and mutagenic compounds. Proc. Natl. Acad. Sci. U. S. A. 104:8737–8742. http://dx.doi.org/10.1073/pnas.0701829104.
  • Fu H, Maunakea AK, Martin MM, Huang L, Zhang Y, Ryan M, Kim R, Lin CM, Zhao K, Aladjem MI. 2013. Methylation of histone H3 on lysine 79 associates with a group of replication origins and helps limit DNA replication once per cell cycle. PLoS Genet. 9:e1003542. http://dx.doi.org/10.1371/journal.pgen.1003542.
  • Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U. S. A. 102:15545–15550. http://dx.doi.org/10.1073/pnas.0506580102.
  • Zhang J, Socolovsky M, Gross AW, Lodish HF. 2003. Role of Ras signaling in erythroid differentiation of mouse fetal liver cells: functional analysis by a flow cytometry-based novel culture system. Blood 102:3938–3946. http://dx.doi.org/10.1182/blood-2003-05-1479.
  • Ishida S, Huang E, Zuzan H, Spang R, Leone G, West M, Nevins JR. 2001. Role for E2F in control of both DNA replication and mitotic functions as revealed from DNA microarray analysis. Mol. Cell. Biol. 21:4684–4699. http://dx.doi.org/10.1128/MCB.21.14.4684-4699.2001.
  • Huh MS, Parker MH, Scime A, Parks R, Rudnicki MA. 2004. Rb is required for progression through myogenic differentiation but not maintenance of terminal differentiation. J. Cell Biol. 166:865–876. http://dx.doi.org/10.1083/jcb.200403004.
  • Wickramasinghe SN, Cooper EH, Chalmers DG. 1968. A study of erythropoiesis by combined morphologic, quantitative cytochemical and autoradiographic methods. Normal human bone marrow, vitamin B12 deficiency and iron deficiency anemia. Blood 31:304–313.
  • Yoshida Y, Todo A, Shirakawa S, Wakisaka G, Uchino H. 1968. Proliferation of megaloblasts in pernicious anemia as observed from nucleic acid metabolism. Blood 31:292–303.
  • Wong P, Hattangadi SM, Cheng AW, Frampton GM, Young RA, Lodish HF. 2011. Gene induction and repression during terminal erythropoiesis are mediated by distinct epigenetic changes. Blood 118:e128–e138. http://dx.doi.org/10.1182/blood-2011-03-341404.
  • Classon M, Harlow E. 2002. The retinoblastoma tumour suppressor in development and cancer. Nat. Rev. Cancer 2:910–917. http://dx.doi.org/10.1038/nrc950.
  • DeGregori J. 2004. The Rb network. J. Cell Sci. 117:3411–3413. http://dx.doi.org/10.1242/jcs.01189.
  • Nevins JR. 2001. The Rb/E2F pathway and cancer. Hum. Mol. Genet. 10:699–703. http://dx.doi.org/10.1093/hmg/10.7.699.
  • van den Heuvel S, Dyson NJ. 2008. Conserved functions of the pRB and E2F families. Nat. Rev. Mol. Cell Biol. 9:713–724. http://dx.doi.org/10.1038/nrm2469.
  • Angus SP, Mayhew CN, Solomon DA, Braden WA, Markey MP, Okuno Y, Cardoso MC, Gilbert DM, Knudsen ES. 2004. RB reversibly inhibits DNA replication via two temporally distinct mechanisms. Mol. Cell. Biol. 24:5404–5420. http://dx.doi.org/10.1128/MCB.24.12.5404-5420.2004.
  • Bester AC, Roniger M, Oren YS, Im MM, Sarni D, Chaoat M, Bensimon A, Zamir G, Shewach DS, Kerem B. 2011. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 145:435–446. http://dx.doi.org/10.1016/j.cell.2011.03.044.
  • Kadri Z, Shimizu R, Ohneda O, Maouche-Chretien L, Gisselbrecht S, Yamamoto M, Romeo PH, Leboulch P, Chretien S. 2009. Direct binding of pRb/E2F-2 to GATA-1 regulates maturation and terminal cell division during erythropoiesis. PLoS Biol. 7:e1000123. http://dx.doi.org/10.1371/journal.pbio.1000123.

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.