Retinal horizontal cells lacking Rb1 sustain persistent DNA damage and survive as polyploid giant cells

Molecular Biology of the Cell

Volumn 23, Issue 22, 2012, Pages 4362-4372

  Donovan, Stacy L ^a   Corbo, Joseph C ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; RETINOBLASTOMA PROTEIN;

ANEUPLOIDY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CYCLE CHECKPOINT; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL POPULATION; CELL SURVIVAL; CELL TYPE; CENTROSOME; CONTROLLED STUDY; DNA CONTENT; DNA DAMAGE; GENE; GENE INACTIVATION; GENOME; GIANT CELL; MITOSIS; MITOSIS SPINDLE; MOUSE; MUTANT; NEWBORN; NONHUMAN; PHENOTYPE; POLYPLOIDY; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RB1 GENE; RETINA DEGENERATION; RETINA HORIZONTAL NERVE CELL; STEM CELL;

ANIMALS; CENTROSOME; DNA DAMAGE; GIANT CELLS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MITOTIC SPINDLE APPARATUS; POLYPLOIDY; RETINA; RETINAL HORIZONTAL CELLS; RETINOBLASTOMA PROTEIN;

EID: 84869209703     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-04-0293     Document Type: Article

References (53)

1. Ajioka I, Martins RA, Bayazitov IT, Donovan S, Johnson DA, Frase S, Cicero SA, Boyd K, Zakharenko SS, Dyer MA (2007). Differentiated horizontal interneurons clonally expand to form metastatic retinoblastoma in mice. Cell 131, 378-390. (Pubitemid 47576143)
2. Bogenmann E, Lochrie MA, Simon MI (1988). Cone cell-specific genes expressed in retinoblastoma. Science 240, 76-78.
3. Bourgo RJ, Ehmer U, Sage J, Knudsen ES (2011). RB deletion disrupts coordination between DNA replication licensing and mitotic entry in vivo. Mol Biol Cell 22, 931-939.
4. Chen D, Livne-bar I, Vanderluit JL, Slack RS, Agochiya M, Bremner R (2004). Cell-specific effects of RB or RB/p107 loss on retinal development implicate an intrinsically death-resistant cell-of-origin in retinoblastoma. Cancer Cell 5, 539-551. (Pubitemid 38748916)
5. Chen D, Opavsky R, Pacal M, Tanimoto N, Wenzel P, Seeliger MW, Leone G, Bremner R (2007). Rb-mediated neuronal differentiation through cell-cycle-independent regulation of E2f3a. PLoS Biol 5, e179.
6. 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.
7. Corson TW, Gallie BL (2007). One hit, two hits, three hits, more? Genomic changes in the development of retinoblastoma. Genes Chromosomes Cancer 46, 617-634. (Pubitemid 46802329)
8. Coschi CH, Dick FA (2012). Chromosome instability and deregulated proliferation: an unavoidable duo. Cell Mol Life Sci 69, 2009-2024.
9. Dannenberg JH, Schuijff L, Dekker M, van der Valk M, te Riele H (2004). Tissue-specific tumor suppressor activity of retinoblastoma gene homologs p107 and p130. Genes Dev 18, 2952-2962. (Pubitemid 39602313)
10. Davoli T, de Lange T (2011). The causes and consequences of polyploidy in normal development and cancer. Annu Rev Cell Dev Biol 27, 585-610.
11. Donovan SL, Schweers B, Martins R, Johnson D, Dyer MA (2006). Compensation by tumor suppressor genes during retinal development in mice and humans. BMC Biol 4, 14.
12. Dotiwala F, Harrison JC, Jain S, Sugawara N, Haber JE (2010). Mad2 prolongs DNA damage checkpoint arrest caused by a double-strand break via a centromere-dependent mechanism. Curr Biol 20, 328-332.
13. Dyer MA, Bremner R (2005). The search for the retinoblastoma cell of origin. Nat Rev Cancer 5, 91-101. (Pubitemid 40215858)
14. Furuta Y, Lagutin O, Hogan BL, Oliver GC (2000). Retina- and ventral forebrain-specific Cre recombinase activity in transgenic mice. Genesis 26, 130-132. (Pubitemid 30158097)
15. Ganguly A, Shields CL (2010). Differential gene expression profile of retinoblastoma compared to normal retina. Mol Vis 16, 1292-1303.
16. Gimenez E, Montoliu L (2001). A simple polymerase chain reaction assay for genotyping the retinal degeneration mutation (Pdeb(rd1)) in FVB/N-derived transgenic mice. Lab Anim 35, 153-156. (Pubitemid 32273187)
17. Glubrecht DD, Kim JH, Russell L, Bamforth JS, Godbout R (2009). Differential CRX and OTX2 expression in human retina and retinoblastoma. J Neurochem 111, 250-263.
18. Haverkamp S, Wassle H (2000). Immunocytochemical analysis of the mouse retina. J Comp Neurol 424, 1-23. (Pubitemid 30602070)
19. Hernando E et al. (2004). Rb inactivation promotes genomic instability by uncoupling cell cycle progression from mitotic control. Nature 430, 797-802. (Pubitemid 39071352)
20. Hurwitz RL, Bogenmann E, Font RL, Holcombe V, Clark D (1990). Expression of the functional cone phototransduction cascade in retinoblastoma. J Clin Invest 85, 1872-1878. (Pubitemid 20192962)
21. 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.
22. Johnson DA, Zhang J, Frase S, Wilson M, Rodriguez-Galindo C, Dyer MA (2007). Neuronal differentiation and synaptogenesis in retinoblastoma. Cancer Res 67, 2701-2711. (Pubitemid 46548958)
23. Knudsen ES, Knudsen KE (2008). Tailoring to RB: tumour suppressor status and therapeutic response. Nat Rev Cancer 8, 714-724.
24. Knudsen ES, Sexton CR, Mayhew CN (2006). Role of the retinoblastoma tumor suppressor in the maintenance of genome integrity. Curr Mol Med 6, 749-757. (Pubitemid 44725568)
25. Laurie NA et al. (2006). Inactivation of the p53 pathway in retinoblastoma. Nature 444, 61-66. (Pubitemid 44684754)
26. 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.
27. Maandag EC, van der Valk M, Vlaar M, Feltkamp C, O'Brien J, van Roon M, van der Lugt N, Berns A, te Riele H (1994). Developmental rescue of an embryonic-lethal mutation in the retinoblastoma gene in chimeric mice. EMBO J 13, 4260-4268. (Pubitemid 24295198)
28. MacPherson D, Sage J, Kim T, Ho D, McLaughlin ME, Jacks T (2004). Cell type-specific effects of Rb deletion in the murine retina. Genes Dev 18, 1681-1694. (Pubitemid 38938185)
29. Manning AL, Dyson NJ (2011). pRB, a tumor suppressor with a stabilizing presence. Trends Cell Biol 21, 433-441.
30. Marino S, Hoogervoorst D, Brandner S, Berns A (2003). Rb and p107 are required for normal cerebellar development and granule cell survival but not for Purkinje cell persistence. Development 130, 3359-3368. (Pubitemid 37010000)
31. Markey M, Siddiqui H, Knudsen ES (2004). Geminin is targeted for repression by the retinoblastoma tumor suppressor pathway through intragenic E2F sites. J Biol Chem 279, 29255-29262. (Pubitemid 38915801)
32. Marquardt T, Ashery-Padan R, Andrejewski N, Scardigli R, Guillemot F, Gruss P (2001). Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105, 43-55. (Pubitemid 32323915)
33. Marti TM, Hefner E, Feeney L, Natale V, Cleaver JE (2006). H2AX phosphorylation within the G1 phase after UV irradiation depends on nucleotide excision repair and not DNA double-strand breaks. Proc Natl Acad Sci USA 103, 9891-9896. (Pubitemid 43993593)
34. Mayhew CN, Bosco EE, Fox SR, Okaya T, Tarapore P, Schwemberger SJ, Babcock GF, Lentsch AB, Fukasawa K, Knudsen ES (2005). Liver-specific pRB loss results in ectopic cell cycle entry and aberrant ploidy. Cancer Res 65, 4568-4577. (Pubitemid 40740792)
35. McGarry TJ, Kirschner MW (1998). Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93, 1043-1053. (Pubitemid 28280797)
36. Morrow EM, Belliveau MJ, Cepko CL (1998). Two phases of rod photoreceptor differentiation during rat retinal development. J Neurosci 18, 3738-3748. (Pubitemid 28225681)
37. Munier FL, Balmer A, van Melle G, Gailloud C (1994). Radial asymmetry in the topography of retinoblastoma. Clues to the cell of origin. Ophthalmic Genet 15, 101-106.
38. Muresan V, Joshi HC, Besharse JC (1993). Gamma-tubulin in differentiated cell types: localization in the vicinity of basal bodies in retinal photoreceptors and ciliated epithelia. J Cell Sci 104, 1229-1237. (Pubitemid 23154330)
39. Robanus-Maandag E, Dekker M, van der Valk M, Carrozza ML, Jeanny JC, Dannenberg JH, Berns A, te Riele H (1998). p107 is a suppressor of retinoblastoma development in pRb-deficient mice. Genes Dev 12, 1599-1609. (Pubitemid 28299512)
40. Rogakou EP, Boon C, Redon C, Bonner WM (1999). Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146, 905-916.
41. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998). DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273, 5858-5868. (Pubitemid 28124064)
42. Sangwan M, McCurdy SR, Livne-Bar I, Ahmad M, Wrana JL, Chen D, Bremner R (2012). Established and new mouse models reveal E2f1 and Cdk2 dependency of retinoblastoma, and expose effective strategies to block tumor initiation. Oncogene, doi:10.1038/onc.2011.654.
43. Santagata S, Maire CL, Idbaih A, Geffers L, Correll M, Holton K, Quackenbush J, Ligon KL (2009). CRX is a diagnostic marker of retinal and pineal lineage tumors. PLoS One 4, e7932.
44. Schvartzman JM, Duijf PH, Sotillo R, Coker C, Benezra R (2011). Mad2 is a critical mediator of the chromosome instability observed upon Rb and p53 pathway inhibition. Cancer Cell 19, 701-714.
45. Viatour P, Sage J (2011). Newly identified aspects of tumor suppression by RB. Dis Model Mech 4, 581-585.
46. 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. (Pubitemid 34833141)
47. Weinberg RA (1995). The retinoblastoma protein and cell cycle control. Cell 81, 323-330.
48. Williams BO, Schmitt EM, Remington L, Bronson RT, Albert DM, Weinberg RA, Jacks T (1994). Extensive contribution of Rb-deficient cells to adult chimeric mice with limited histopathological consequences. EMBO J 13, 4251-4259. (Pubitemid 24295197)
49. Xu XL, Fang Y, Lee TC, Forrest D, Gregory-Evans C, Almeida D, Liu A, Jhanwar SC, Abramson DH, Cobrinik D (2009). Retinoblastoma has properties of a cone precursor tumor and depends upon cone-specific MDM2 signaling. Cell 137, 1018-1031.
50. Young RW (1984). Cell death during differentiation of the retina in the mouse. J Comp Neurol 229, 362-373.
51. Zacksenhaus E, Jiang Z, Chung D, Marth JD, Phillips RA, Gallie BL (1996). pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev 10, 3051-3064. (Pubitemid 26412531)
52. Zhang J et al. (2012). A novel retinoblastoma therapy from genomic and epigenetic analyses. Nature 481, 329-334.
53. Zhang J, Schweers B, Dyer MA (2004). The first knockout mouse model of retinoblastoma. Cell Cycle 3, 952-959. (Pubitemid 40185382)