Skip to main content
Top
Published in:

Open Access 01-12-2017 | Review

Heterogeneity in retinoblastoma: a tale of molecules and models

Authors: Sonya Stenfelt, Maria K. E. Blixt, Charlotta All-Ericsson, Finn Hallböök, Henrik Boije

Published in: Clinical and Translational Medicine | Issue 1/2017

Login to get access

Abstract

Retinoblastoma, an intraocular pediatric cancer, develops in the embryonic retina following biallelic loss of RB1. However, there is a wide range of genetic and epigenetic changes that can affect RB1 resulting in different clinical outcomes. In addition, other transformations, such as MYCN amplification, generate particularly aggressive tumors, which may or may not be RB1 independent. Recognizing the cellular characteristics required for tumor development, by identifying the elusive cell-of-origin for retinoblastoma, would help us understand the development of these tumors. In this review we summarize the heterogeneity reported in retinoblastoma on a molecular, cellular and tissue level. We also discuss the challenging heterogeneity in current retinoblastoma models and suggest future platforms that could contribute to improved understanding of tumor initiation, progression and metastasis in retinoblastoma, which may ultimately lead to more patient-specific treatments.
Literature
1.
go back to reference Allison KH, Sledge GW (2014) Heterogeneity and cancer. Oncology (Williston Park). 28(9):772–778PubMed Allison KH, Sledge GW (2014) Heterogeneity and cancer. Oncology (Williston Park). 28(9):772–778PubMed
2.
go back to reference Dyer MA, Bremner R (2005) The search for the retinoblastoma cell of origin. Nat Rev Cancer 5(2):91–101PubMedCrossRef Dyer MA, Bremner R (2005) The search for the retinoblastoma cell of origin. Nat Rev Cancer 5(2):91–101PubMedCrossRef
3.
go back to reference Kivela T (2009) 200 years of success initiated by James Wardrop’s 1809 monograph on retinoblastoma. Acta Ophthalmol 87(8):810–812PubMedCrossRef Kivela T (2009) 200 years of success initiated by James Wardrop’s 1809 monograph on retinoblastoma. Acta Ophthalmol 87(8):810–812PubMedCrossRef
4.
go back to reference Dyer MA (2016) Lessons from retinoblastoma: implications for cancer, development, evolution, and regenerative medicine. Trends Mol Med. 22(10):863–876PubMedPubMedCentralCrossRef Dyer MA (2016) Lessons from retinoblastoma: implications for cancer, development, evolution, and regenerative medicine. Trends Mol Med. 22(10):863–876PubMedPubMedCentralCrossRef
7.
go back to reference Dimaras H, Kimani K, Dimba EA, Gronsdahl P, White A, Chan HS et al (2012) Retinoblastoma. Lancet 379(9824):1436–1446PubMedCrossRef Dimaras H, Kimani K, Dimba EA, Gronsdahl P, White A, Chan HS et al (2012) Retinoblastoma. Lancet 379(9824):1436–1446PubMedCrossRef
8.
go back to reference Mendoza PR, Grossniklaus HE (2015) The biology of retinoblastoma. Prog Mol Biol Transl Sci 134:503–516PubMedCrossRef Mendoza PR, Grossniklaus HE (2015) The biology of retinoblastoma. Prog Mol Biol Transl Sci 134:503–516PubMedCrossRef
11.
12.
go back to reference Li WL, Buckley J, Sanchez-Lara PA, Maglinte DT, Viduetsky L, Tatarinova TV et al (2016) A rapid and sensitive next-generation sequencing method to detect RB1 mutations improves care for retinoblastoma patients and their families. J Mol Diagn 18(4):480–493PubMedCrossRef Li WL, Buckley J, Sanchez-Lara PA, Maglinte DT, Viduetsky L, Tatarinova TV et al (2016) A rapid and sensitive next-generation sequencing method to detect RB1 mutations improves care for retinoblastoma patients and their families. J Mol Diagn 18(4):480–493PubMedCrossRef
13.
go back to reference McEvoy J, Nagahawatte P, Finkelstein D, Richards-Yutz J, Valentine M, Ma J et al (2014) RB1 gene inactivation by chromothripsis in human retinoblastoma. Oncotarget 5(2):438–450PubMedPubMedCentralCrossRef McEvoy J, Nagahawatte P, Finkelstein D, Richards-Yutz J, Valentine M, Ma J et al (2014) RB1 gene inactivation by chromothripsis in human retinoblastoma. Oncotarget 5(2):438–450PubMedPubMedCentralCrossRef
15.
go back to reference Aldiri I, Xu B, Wang L, Chen X, Hiler D, Griffiths L et al (2017) The dynamic epigenetic landscape of the retina during development, reprogramming, and tumorigenesis. Neuron 94(3):550–568PubMedCrossRef Aldiri I, Xu B, Wang L, Chen X, Hiler D, Griffiths L et al (2017) The dynamic epigenetic landscape of the retina during development, reprogramming, and tumorigenesis. Neuron 94(3):550–568PubMedCrossRef
16.
go back to reference Harbour JW (1998) Overview of RB gene mutations in patients with retinoblastoma. Implications clinical genetic screening. Ophthalmology 105(8):1442–1447PubMedCrossRef Harbour JW (1998) Overview of RB gene mutations in patients with retinoblastoma. Implications clinical genetic screening. Ophthalmology 105(8):1442–1447PubMedCrossRef
17.
go back to reference Dommering CJ, Mol BM, Moll AC, Burton M, Cloos J, Dorsman JC et al (2014) RB1 mutation spectrum in a comprehensive nationwide cohort of retinoblastoma patients. J Med Genet 51(6):366–374PubMedCrossRef Dommering CJ, Mol BM, Moll AC, Burton M, Cloos J, Dorsman JC et al (2014) RB1 mutation spectrum in a comprehensive nationwide cohort of retinoblastoma patients. J Med Genet 51(6):366–374PubMedCrossRef
19.
go back to reference Gallie BL, Campbell C, Devlin H, Duckett A, Squire JA (1999) Developmental basis of retinal-specific induction of cancer by RB mutation. Cancer Res 59(7 Suppl):1731s–1735sPubMed Gallie BL, Campbell C, Devlin H, Duckett A, Squire JA (1999) Developmental basis of retinal-specific induction of cancer by RB mutation. Cancer Res 59(7 Suppl):1731s–1735sPubMed
20.
go back to reference Bowles E, Corson TW, Bayani J, Squire JA, Wong N, Lai PB et al (2007) Profiling genomic copy number changes in retinoblastoma beyond loss of RB1. Genes Chromosomes Cancer 46(2):118–129PubMedCrossRef Bowles E, Corson TW, Bayani J, Squire JA, Wong N, Lai PB et al (2007) Profiling genomic copy number changes in retinoblastoma beyond loss of RB1. Genes Chromosomes Cancer 46(2):118–129PubMedCrossRef
21.
go back to reference Lee WH, Murphree AL, Benedict WF (1984) Expression and amplification of the N-myc gene in primary retinoblastoma. Nature 309(5967):458–460PubMedCrossRef Lee WH, Murphree AL, Benedict WF (1984) Expression and amplification of the N-myc gene in primary retinoblastoma. Nature 309(5967):458–460PubMedCrossRef
22.
go back to reference Rushlow DE, Mol BM, Kennett JY, Yee S, Pajovic S, Theriault BL et al (2013) Characterisation of retinoblastomas without RB1 mutations: genomic, gene expression, and clinical studies. Lancet Oncol 14(4):327–334PubMedCrossRef Rushlow DE, Mol BM, Kennett JY, Yee S, Pajovic S, Theriault BL et al (2013) Characterisation of retinoblastomas without RB1 mutations: genomic, gene expression, and clinical studies. Lancet Oncol 14(4):327–334PubMedCrossRef
23.
go back to reference Sampieri K, Mencarelli MA, Epistolato MC, Toti P, Lazzi S, Bruttini M et al (2008) Genomic differences between retinoma and retinoblastoma. Acta Oncol 47(8):1483–1492PubMedCrossRef Sampieri K, Mencarelli MA, Epistolato MC, Toti P, Lazzi S, Bruttini M et al (2008) Genomic differences between retinoma and retinoblastoma. Acta Oncol 47(8):1483–1492PubMedCrossRef
24.
go back to reference Dimaras H, Khetan V, Halliday W, Orlic M, Prigoda NL, Piovesan B et al (2008) Loss of RB1 induces non-proliferative retinoma: increasing genomic instability correlates with progression to retinoblastoma. Hum Mol Genet 17(10):1363–1372PubMedCrossRef Dimaras H, Khetan V, Halliday W, Orlic M, Prigoda NL, Piovesan B et al (2008) Loss of RB1 induces non-proliferative retinoma: increasing genomic instability correlates with progression to retinoblastoma. Hum Mol Genet 17(10):1363–1372PubMedCrossRef
25.
go back to reference Corson TW, Gallie BL (2007) One hit, two hits, three hits, more? Genomic changes in the development of retinoblastoma. Genes Chromosomes Cancer 46(7):617–634PubMedCrossRef Corson TW, Gallie BL (2007) One hit, two hits, three hits, more? Genomic changes in the development of retinoblastoma. Genes Chromosomes Cancer 46(7):617–634PubMedCrossRef
26.
go back to reference Theriault BL, Dimaras H, Gallie BL, Corson TW (2014) The genomic landscape of retinoblastoma: a review. Clin Exp Ophthalmol 42(1):33–52PubMedCrossRef Theriault BL, Dimaras H, Gallie BL, Corson TW (2014) The genomic landscape of retinoblastoma: a review. Clin Exp Ophthalmol 42(1):33–52PubMedCrossRef
27.
go back to reference Lohmann DR, Gallie BL (1993) Retinoblastoma. In: Pagon RA, Adam MP, Ardinger HH, Wallace SE, Amemiya A, Bean LJH, et al., editors. GeneReviews(R). Seattle (WA): University of Washington, Seattle University of Washington, Seattle. GeneReviews is a registered trademark of the University of Washington, Seattle. All rights reserved Lohmann DR, Gallie BL (1993) Retinoblastoma. In: Pagon RA, Adam MP, Ardinger HH, Wallace SE, Amemiya A, Bean LJH, et al., editors. GeneReviews(R). Seattle (WA): University of Washington, Seattle University of Washington, Seattle. GeneReviews is a registered trademark of the University of Washington, Seattle. All rights reserved
28.
go back to reference Woo CW, Tan F, Cassano H, Lee J, Lee KC, Thiele CJ (2008) Use of RNA interference to elucidate the effect of MYCN on cell cycle in neuroblastoma. Pediatr Blood Cancer 50(2):208–212PubMedCrossRef Woo CW, Tan F, Cassano H, Lee J, Lee KC, Thiele CJ (2008) Use of RNA interference to elucidate the effect of MYCN on cell cycle in neuroblastoma. Pediatr Blood Cancer 50(2):208–212PubMedCrossRef
30.
go back to reference Kooi IE, Mol BM, Massink MP, Ameziane N, Meijers-Heijboer H, Dommering CJ et al (2016) Somatic genomic alterations in retinoblastoma beyond RB1 are rare and limited to copy number changes. Sci Rep 6:25264PubMedPubMedCentralCrossRef Kooi IE, Mol BM, Massink MP, Ameziane N, Meijers-Heijboer H, Dommering CJ et al (2016) Somatic genomic alterations in retinoblastoma beyond RB1 are rare and limited to copy number changes. Sci Rep 6:25264PubMedPubMedCentralCrossRef
31.
go back to reference Wu N, Jia D, Bates B, Basom R, Eberhart CG, MacPherson D (2017) A mouse model of MYCN-driven retinoblastoma reveals MYCN-independent tumor reemergence. J Clin Invest. 127(3):888–898PubMedPubMedCentralCrossRef Wu N, Jia D, Bates B, Basom R, Eberhart CG, MacPherson D (2017) A mouse model of MYCN-driven retinoblastoma reveals MYCN-independent tumor reemergence. J Clin Invest. 127(3):888–898PubMedPubMedCentralCrossRef
32.
go back to reference Ewens KG, Bhatti TR, Moran KA, Richards-Yutz J, Shields CL, Eagle RC et al (2017) Phosphorylation of pRb: mechanism for RB pathway inactivation in MYCN-amplified retinoblastoma. Cancer Med 6(3):619–630PubMedPubMedCentralCrossRef Ewens KG, Bhatti TR, Moran KA, Richards-Yutz J, Shields CL, Eagle RC et al (2017) Phosphorylation of pRb: mechanism for RB pathway inactivation in MYCN-amplified retinoblastoma. Cancer Med 6(3):619–630PubMedPubMedCentralCrossRef
33.
go back to reference Zhang J, Schweers B, Dyer MA (2004) The first knockout mouse model of retinoblastoma. Cell Cycle 3(7):952–959PubMedCrossRef Zhang J, Schweers B, Dyer MA (2004) The first knockout mouse model of retinoblastoma. Cell Cycle 3(7):952–959PubMedCrossRef
34.
go back to reference 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(6):539–551PubMedCrossRef 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(6):539–551PubMedCrossRef
35.
go back to reference Xu XL, Fang Y, Lee TC, Forrest D, Gregory-Evans C, Almeida D et al (2009) Retinoblastoma has properties of a cone precursor tumor and depends upon cone-specific MDM2 signaling. Cell 137(6):1018–1031PubMedPubMedCentralCrossRef Xu XL, Fang Y, Lee TC, Forrest D, Gregory-Evans C, Almeida D et al (2009) Retinoblastoma has properties of a cone precursor tumor and depends upon cone-specific MDM2 signaling. Cell 137(6):1018–1031PubMedPubMedCentralCrossRef
36.
go back to reference Xu XL, Singh HP, Wang L, Qi DL, Poulos BK, Abramson DH et al (2014) Rb suppresses human cone-precursor-derived retinoblastoma tumours. Nature 514(7522):385–388PubMedPubMedCentralCrossRef Xu XL, Singh HP, Wang L, Qi DL, Poulos BK, Abramson DH et al (2014) Rb suppresses human cone-precursor-derived retinoblastoma tumours. Nature 514(7522):385–388PubMedPubMedCentralCrossRef
37.
go back to reference Ajioka I, Martins RA, Bayazitov IT, Donovan S, Johnson DA, Frase S et al (2007) Differentiated horizontal interneurons clonally expand to form metastatic retinoblastoma in mice. Cell 131(2):378–390PubMedPubMedCentralCrossRef Ajioka I, Martins RA, Bayazitov IT, Donovan S, Johnson DA, Frase S et al (2007) Differentiated horizontal interneurons clonally expand to form metastatic retinoblastoma in mice. Cell 131(2):378–390PubMedPubMedCentralCrossRef
38.
go back to reference Pajovic S, Corson TW, Spencer C, Dimaras H, Orlic-Milacic M, Marchong MN et al (2011) The TAg-RB murine retinoblastoma cell of origin has immunohistochemical features of differentiated Muller glia with progenitor properties. Invest Ophthalmol Vis Sci 52(10):7618–7624PubMedPubMedCentralCrossRef Pajovic S, Corson TW, Spencer C, Dimaras H, Orlic-Milacic M, Marchong MN et al (2011) The TAg-RB murine retinoblastoma cell of origin has immunohistochemical features of differentiated Muller glia with progenitor properties. Invest Ophthalmol Vis Sci 52(10):7618–7624PubMedPubMedCentralCrossRef
39.
go back to reference Kang SJ, Durairaj C, Kompella UB, O’Brien JM, Grossniklaus HE (2009) Subconjunctival nanoparticle carboplatin in the treatment of murine retinoblastoma. Arch Ophthalmol 127(8):1043–1047PubMedPubMedCentralCrossRef Kang SJ, Durairaj C, Kompella UB, O’Brien JM, Grossniklaus HE (2009) Subconjunctival nanoparticle carboplatin in the treatment of murine retinoblastoma. Arch Ophthalmol 127(8):1043–1047PubMedPubMedCentralCrossRef
40.
go back to reference Wetts R, Fraser SE (1988) Multipotent precursors can give rise to all major cell types of the frog retina. Science 239(4844):1142–1145PubMedCrossRef Wetts R, Fraser SE (1988) Multipotent precursors can give rise to all major cell types of the frog retina. Science 239(4844):1142–1145PubMedCrossRef
41.
go back to reference Blixt MK, Hallbook F (2016) A regulatory sequence from the retinoid X receptor gamma gene directs expression to horizontal cells and photoreceptors in the embryonic chicken retina. Mol Vis 22:1405–1420PubMedPubMedCentral Blixt MK, Hallbook F (2016) A regulatory sequence from the retinoid X receptor gamma gene directs expression to horizontal cells and photoreceptors in the embryonic chicken retina. Mol Vis 22:1405–1420PubMedPubMedCentral
42.
go back to reference Suzuki SC, Bleckert A, Williams PR, Takechi M, Kawamura S, Wong RO (2013) Cone photoreceptor types in zebrafish are generated by symmetric terminal divisions of dedicated precursors. Proc Natl Acad Sci USA 110(37):15109–15114PubMedPubMedCentralCrossRef Suzuki SC, Bleckert A, Williams PR, Takechi M, Kawamura S, Wong RO (2013) Cone photoreceptor types in zebrafish are generated by symmetric terminal divisions of dedicated precursors. Proc Natl Acad Sci USA 110(37):15109–15114PubMedPubMedCentralCrossRef
43.
go back to reference Boije H, Rulands S, Dudczig S, Simons BD, Harris WA (2015) The independent probabilistic firing of transcription factors: a paradigm for clonal variability in the zebrafish retina. Dev Cell 34(5):532–543PubMedPubMedCentralCrossRef Boije H, Rulands S, Dudczig S, Simons BD, Harris WA (2015) The independent probabilistic firing of transcription factors: a paradigm for clonal variability in the zebrafish retina. Dev Cell 34(5):532–543PubMedPubMedCentralCrossRef
44.
go back to reference Suga A, Taira M, Nakagawa S (2009) LIM family transcription factors regulate the subtype-specific morphogenesis of retinal horizontal cells at post-migratory stages. Dev Biol 330(2):318–328PubMedCrossRef Suga A, Taira M, Nakagawa S (2009) LIM family transcription factors regulate the subtype-specific morphogenesis of retinal horizontal cells at post-migratory stages. Dev Biol 330(2):318–328PubMedCrossRef
45.
go back to reference Edqvist PH, Myers SM, Hallböök F (2006) Early identification of retinal subtypes in the developing, pre-laminated chick retina using the transcription factors Prox1, Lim1, Ap2alpha, Pax 6, Isl1, Isl2, Lim3 and Chx10. Eur J Histochem 50(2):147–154PubMed Edqvist PH, Myers SM, Hallböök F (2006) Early identification of retinal subtypes in the developing, pre-laminated chick retina using the transcription factors Prox1, Lim1, Ap2alpha, Pax 6, Isl1, Isl2, Lim3 and Chx10. Eur J Histochem 50(2):147–154PubMed
46.
go back to reference Dormoy V, Beraud C, Lindner V, Thomas L, Coquard C, Barthelmebs M et al (2011) LIM-class homeobox gene Lim1, a novel oncogene in human renal cell carcinoma. Oncogene 30(15):1753–1763PubMedCrossRef Dormoy V, Beraud C, Lindner V, Thomas L, Coquard C, Barthelmebs M et al (2011) LIM-class homeobox gene Lim1, a novel oncogene in human renal cell carcinoma. Oncogene 30(15):1753–1763PubMedCrossRef
47.
go back to reference Tsai KY, Hu Y, Macleod KF, Crowley D, Yamasaki L, Jacks T (1998) Mutation of E2f-1 suppresses apoptosis and inappropriate S phase entry and extends survival of Rb-deficient mouse embryos. Mol Cell 2(3):293–304PubMedCrossRef Tsai KY, Hu Y, Macleod KF, Crowley D, Yamasaki L, Jacks T (1998) Mutation of E2f-1 suppresses apoptosis and inappropriate S phase entry and extends survival of Rb-deficient mouse embryos. Mol Cell 2(3):293–304PubMedCrossRef
48.
go back to reference 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(14):1681–1694PubMedPubMedCentralCrossRef 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(14):1681–1694PubMedPubMedCentralCrossRef
49.
go back to reference Cook B, Portera-Cailliau C, Adler R (1998) Developmental neuronal death is not a universal phenomenon among cell types in the chick embryo retina. J Comp Neurol. 396(1):12–19PubMedCrossRef Cook B, Portera-Cailliau C, Adler R (1998) Developmental neuronal death is not a universal phenomenon among cell types in the chick embryo retina. J Comp Neurol. 396(1):12–19PubMedCrossRef
50.
go back to reference Mayordomo R (2001) Differentiated horizontal cells seem not to be affected by apoptosis during development of the chick retina. Int J Dev Biol 45:S79–S80 Mayordomo R (2001) Differentiated horizontal cells seem not to be affected by apoptosis during development of the chick retina. Int J Dev Biol 45:S79–S80
51.
go back to reference Berta AI, Boesze-Battaglia K, Genini S, Goldstein O, O’Brien PJ, Szel A et al (2011) Photoreceptor cell death, proliferation and formation of hybrid rod/S-cone photoreceptors in the degenerating STK38L mutant retina. PLoS ONE 6(9):e24074PubMedPubMedCentralCrossRef Berta AI, Boesze-Battaglia K, Genini S, Goldstein O, O’Brien PJ, Szel A et al (2011) Photoreceptor cell death, proliferation and formation of hybrid rod/S-cone photoreceptors in the degenerating STK38L mutant retina. PLoS ONE 6(9):e24074PubMedPubMedCentralCrossRef
52.
go back to reference Shirazi Fard S, All-Ericsson C, Hallbook F (2014) The heterogenic final cell cycle of chicken retinal Lim1 horizontal cells is not regulated by the DNA damage response pathway. Cell Cycle 13(3):408–417PubMedCrossRef Shirazi Fard S, All-Ericsson C, Hallbook F (2014) The heterogenic final cell cycle of chicken retinal Lim1 horizontal cells is not regulated by the DNA damage response pathway. Cell Cycle 13(3):408–417PubMedCrossRef
53.
go back to reference Shirazi Fard S, Thyselius M, All-Ericsson C, Hallbook F (2014) The terminal basal mitosis of chicken retinal Lim1 horizontal cells is not sensitive to cisplatin-induced cell cycle arrest. Cell Cycle 13(23):3698–3706PubMedPubMedCentralCrossRef Shirazi Fard S, Thyselius M, All-Ericsson C, Hallbook F (2014) The terminal basal mitosis of chicken retinal Lim1 horizontal cells is not sensitive to cisplatin-induced cell cycle arrest. Cell Cycle 13(23):3698–3706PubMedPubMedCentralCrossRef
54.
55.
go back to reference Kato MV, Shimizu T, Ishizaki K, Kaneko A, Yandell DW, Toguchida J et al (1996) Loss of heterozygosity on chromosome 17 and mutation of the p53 gene in retinoblastoma. Cancer Lett 106(1):75–82PubMedCrossRef Kato MV, Shimizu T, Ishizaki K, Kaneko A, Yandell DW, Toguchida J et al (1996) Loss of heterozygosity on chromosome 17 and mutation of the p53 gene in retinoblastoma. Cancer Lett 106(1):75–82PubMedCrossRef
56.
go back to reference Spengler D, Villalba M, Hoffmann A, Pantaloni C, Houssami S, Bockaert J et al (1997) Regulation of apoptosis and cell cycle arrest by Zac1, a novel zinc finger protein expressed in the pituitary gland and the brain. EMBO J 16(10):2814–2825PubMedPubMedCentralCrossRef Spengler D, Villalba M, Hoffmann A, Pantaloni C, Houssami S, Bockaert J et al (1997) Regulation of apoptosis and cell cycle arrest by Zac1, a novel zinc finger protein expressed in the pituitary gland and the brain. EMBO J 16(10):2814–2825PubMedPubMedCentralCrossRef
57.
go back to reference Fard SS, Blixt M, Hallböök F (2015) The p53 co-activator Zac1 neither induces cell cycle arrest nor apoptosis in chicken Lim1 horizontal progenitor cells. Cell Death Discov 1:15023PubMedPubMedCentralCrossRef Fard SS, Blixt M, Hallböök F (2015) The p53 co-activator Zac1 neither induces cell cycle arrest nor apoptosis in chicken Lim1 horizontal progenitor cells. Cell Death Discov 1:15023PubMedPubMedCentralCrossRef
58.
go back to reference Shirazi Fard S, Jarrin M, Boije H, Fillon V, All-Eriksson C, Hallböök F (2013) Heterogenic final cell cycle by chicken retinal Lim1 horizontal progenitor cells leads to heteroploid cells with a remaining replicated genome. PLoS ONE 8(3):e59133PubMedPubMedCentralCrossRef Shirazi Fard S, Jarrin M, Boije H, Fillon V, All-Eriksson C, Hallböök F (2013) Heterogenic final cell cycle by chicken retinal Lim1 horizontal progenitor cells leads to heteroploid cells with a remaining replicated genome. PLoS ONE 8(3):e59133PubMedPubMedCentralCrossRef
60.
go back to reference Bader JL, Meadows AT, Zimmerman LE, Rorke LB, Voute PA, Champion LA et al (1982) Bilateral retinoblastoma with ectopic intracranial retinoblastoma: trilateral retinoblastoma. Cancer Genet Cytogenet 5(3):203–213PubMedCrossRef Bader JL, Meadows AT, Zimmerman LE, Rorke LB, Voute PA, Champion LA et al (1982) Bilateral retinoblastoma with ectopic intracranial retinoblastoma: trilateral retinoblastoma. Cancer Genet Cytogenet 5(3):203–213PubMedCrossRef
61.
go back to reference Kapatai G, Brundler MA, Jenkinson H, Kearns P, Parulekar M, Peet AC et al (2013) Gene expression profiling identifies different sub-types of retinoblastoma. Br J Cancer 109(2):512–525PubMedPubMedCentralCrossRef Kapatai G, Brundler MA, Jenkinson H, Kearns P, Parulekar M, Peet AC et al (2013) Gene expression profiling identifies different sub-types of retinoblastoma. Br J Cancer 109(2):512–525PubMedPubMedCentralCrossRef
62.
go back to reference Kooi IE, Mol BM, Moll AC, van der Valk P, de Jong MC, de Graaf P et al (2015) Loss of photoreceptorness and gain of genomic alterations in retinoblastoma reveal tumor progression. EBioMedicine 2(7):660–670PubMedPubMedCentralCrossRef Kooi IE, Mol BM, Moll AC, van der Valk P, de Jong MC, de Graaf P et al (2015) Loss of photoreceptorness and gain of genomic alterations in retinoblastoma reveal tumor progression. EBioMedicine 2(7):660–670PubMedPubMedCentralCrossRef
63.
go back to reference Valverde JR, Alonso J, Palacios I, Pestana A (2005) RB1 gene mutation up-date, a meta-analysis based on 932 reported mutations available in a searchable database. BMC Genet 6:53PubMedPubMedCentralCrossRef Valverde JR, Alonso J, Palacios I, Pestana A (2005) RB1 gene mutation up-date, a meta-analysis based on 932 reported mutations available in a searchable database. BMC Genet 6:53PubMedPubMedCentralCrossRef
64.
go back to reference Otterson GA, Chen W, Coxon AB, Khleif SN, Kaye FJ (1997) Incomplete penetrance of familial retinoblastoma linked to germ-line mutations that result in partial loss of RB function. Proc Natl Acad Sci USA 94(22):12036–12040PubMedPubMedCentralCrossRef Otterson GA, Chen W, Coxon AB, Khleif SN, Kaye FJ (1997) Incomplete penetrance of familial retinoblastoma linked to germ-line mutations that result in partial loss of RB function. Proc Natl Acad Sci USA 94(22):12036–12040PubMedPubMedCentralCrossRef
65.
go back to reference Cooper DN, Krawczak M, Polychronakos C, Tyler-Smith C, Kehrer-Sawatzki H (2013) Where genotype is not predictive of phenotype: towards an understanding of the molecular basis of reduced penetrance in human inherited disease. Hum Genet 132(10):1077–1130PubMedPubMedCentralCrossRef Cooper DN, Krawczak M, Polychronakos C, Tyler-Smith C, Kehrer-Sawatzki H (2013) Where genotype is not predictive of phenotype: towards an understanding of the molecular basis of reduced penetrance in human inherited disease. Hum Genet 132(10):1077–1130PubMedPubMedCentralCrossRef
66.
go back to reference Sellers WR, Novitch BG, Miyake S, Heith A, Otterson GA, Kaye FJ et al (1998) Stable binding to E2F is not required for the retinoblastoma protein to activate transcription, promote differentiation, and suppress tumor cell growth. Genes Dev 12(1):95–106PubMedPubMedCentralCrossRef Sellers WR, Novitch BG, Miyake S, Heith A, Otterson GA, Kaye FJ et al (1998) Stable binding to E2F is not required for the retinoblastoma protein to activate transcription, promote differentiation, and suppress tumor cell growth. Genes Dev 12(1):95–106PubMedPubMedCentralCrossRef
67.
go back to reference Ahmad NN, Melo MB, Singh AD, Donoso LA, Shields JA (1999) A possible hot spot in exon 21 of the retinoblastoma gene predisposing to a low penetrant retinoblastoma phenotype? Ophthalmic Genet 20(4):225–231PubMedCrossRef Ahmad NN, Melo MB, Singh AD, Donoso LA, Shields JA (1999) A possible hot spot in exon 21 of the retinoblastoma gene predisposing to a low penetrant retinoblastoma phenotype? Ophthalmic Genet 20(4):225–231PubMedCrossRef
68.
go back to reference Eloy P, Dehainault C, Sefta M, Aerts I, Doz F, Cassoux N et al (2016) A parent-of-origin effect impacts the phenotype in low penetrance retinoblastoma families segregating the c.1981C > T/p.Arg661Trp Mutation of RB1. PLoS Genet 12(2):e1005888PubMedPubMedCentralCrossRef Eloy P, Dehainault C, Sefta M, Aerts I, Doz F, Cassoux N et al (2016) A parent-of-origin effect impacts the phenotype in low penetrance retinoblastoma families segregating the c.1981C > T/p.Arg661Trp Mutation of RB1. PLoS Genet 12(2):e1005888PubMedPubMedCentralCrossRef
69.
go back to reference Klutz M, Brockmann D, Lohmann DR (2002) A parent-of-origin effect in two families with retinoblastoma is associated with a distinct splice mutation in the RB1 gene. Am J Hum Genet 71(1):174–179PubMedPubMedCentralCrossRef Klutz M, Brockmann D, Lohmann DR (2002) A parent-of-origin effect in two families with retinoblastoma is associated with a distinct splice mutation in the RB1 gene. Am J Hum Genet 71(1):174–179PubMedPubMedCentralCrossRef
70.
go back to reference Toriello HV, Meck JM, Professional P, Guidelines C (2008) Statement on guidance for genetic counseling in advanced paternal age. Genet Med. 10(6):457–460PubMedPubMedCentralCrossRef Toriello HV, Meck JM, Professional P, Guidelines C (2008) Statement on guidance for genetic counseling in advanced paternal age. Genet Med. 10(6):457–460PubMedPubMedCentralCrossRef
71.
go back to reference Marr BP, Singh AD (2015) Retinoblastoma: evaluation and diagnosis. In: Singh AD, Murphree AL, Damato BE (eds) Clinical ophthalmic oncology: retinoblastoma. Springer, Berlin, pp 1–11 Marr BP, Singh AD (2015) Retinoblastoma: evaluation and diagnosis. In: Singh AD, Murphree AL, Damato BE (eds) Clinical ophthalmic oncology: retinoblastoma. Springer, Berlin, pp 1–11
72.
go back to reference Aerts I, Pacquement H, Doz F, Mosseri V, Desjardins L, Sastre X et al (2004) Outcome of second malignancies after retinoblastoma: a retrospective analysis of 25 patients treated at the Institut Curie. Eur J Cancer 40(10):1522–1529PubMedCrossRef Aerts I, Pacquement H, Doz F, Mosseri V, Desjardins L, Sastre X et al (2004) Outcome of second malignancies after retinoblastoma: a retrospective analysis of 25 patients treated at the Institut Curie. Eur J Cancer 40(10):1522–1529PubMedCrossRef
73.
go back to reference Kleinerman RA, Yu CL, Little MP, Li Y, Abramson D, Seddon J et al (2012) Variation of second cancer risk by family history of retinoblastoma among long-term survivors. J Clin Oncol 30(9):950–957PubMedPubMedCentralCrossRef Kleinerman RA, Yu CL, Little MP, Li Y, Abramson D, Seddon J et al (2012) Variation of second cancer risk by family history of retinoblastoma among long-term survivors. J Clin Oncol 30(9):950–957PubMedPubMedCentralCrossRef
74.
go back to reference Simpson JL, Carson SA, Cisneros P (2005) Preimplantation genetic diagnosis (PGD) for heritable neoplasia. J Natl Cancer Inst Monogr 34:87–90CrossRef Simpson JL, Carson SA, Cisneros P (2005) Preimplantation genetic diagnosis (PGD) for heritable neoplasia. J Natl Cancer Inst Monogr 34:87–90CrossRef
75.
go back to reference Sang DN, Albert DM (1982) Retinoblastoma: clinical and histopathologic features. Hum Pathol 13(2):133–147PubMedCrossRef Sang DN, Albert DM (1982) Retinoblastoma: clinical and histopathologic features. Hum Pathol 13(2):133–147PubMedCrossRef
76.
go back to reference Singh AD, Santos CM, Shields CL, Shields JA, Eagle RC Jr (2000) Observations on 17 patients with retinocytoma. Arch Ophthalmol 118(2):199–205PubMedCrossRef Singh AD, Santos CM, Shields CL, Shields JA, Eagle RC Jr (2000) Observations on 17 patients with retinocytoma. Arch Ophthalmol 118(2):199–205PubMedCrossRef
77.
go back to reference Shields CL, Lally SE, Leahey AM, Jabbour PM, Caywood EH, Schwendeman R et al (2014) Targeted retinoblastoma management: when to use intravenous, intra-arterial, periocular, and intravitreal chemotherapy. Curr Opin Ophthalmol 25(5):374–385PubMedCrossRef Shields CL, Lally SE, Leahey AM, Jabbour PM, Caywood EH, Schwendeman R et al (2014) Targeted retinoblastoma management: when to use intravenous, intra-arterial, periocular, and intravitreal chemotherapy. Curr Opin Ophthalmol 25(5):374–385PubMedCrossRef
78.
go back to reference Zhang J, Benavente CA, McEvoy J, Flores-Otero J, Ding L, Chen X et al (2012) A novel retinoblastoma therapy from genomic and epigenetic analyses. Nature 481(7381):329–334PubMedPubMedCentral Zhang J, Benavente CA, McEvoy J, Flores-Otero J, Ding L, Chen X et al (2012) A novel retinoblastoma therapy from genomic and epigenetic analyses. Nature 481(7381):329–334PubMedPubMedCentral
79.
go back to reference Laurie NA, Donovan SL, Shih CS, Zhang J, Mills N, Fuller C et al (2006) Inactivation of the p53 pathway in retinoblastoma. Nature 444(7115):61–66PubMedCrossRef Laurie NA, Donovan SL, Shih CS, Zhang J, Mills N, Fuller C et al (2006) Inactivation of the p53 pathway in retinoblastoma. Nature 444(7115):61–66PubMedCrossRef
80.
go back to reference Hurlin PJ, Huang J (2006) The MAX-interacting transcription factor network. Semin Cancer Biol 16(4):265–274PubMedCrossRef Hurlin PJ, Huang J (2006) The MAX-interacting transcription factor network. Semin Cancer Biol 16(4):265–274PubMedCrossRef
81.
go back to reference Lu X, Pearson A, Lunec J (2003) The MYCN oncoprotein as a drug development target. Cancer Lett 197(1–2):125–130PubMedCrossRef Lu X, Pearson A, Lunec J (2003) The MYCN oncoprotein as a drug development target. Cancer Lett 197(1–2):125–130PubMedCrossRef
82.
go back to reference Facchini LM, Penn LZ (1998) The molecular role of Myc in growth and transformation: recent discoveries lead to new insights. FASEB J 12(9):633–651PubMed Facchini LM, Penn LZ (1998) The molecular role of Myc in growth and transformation: recent discoveries lead to new insights. FASEB J 12(9):633–651PubMed
83.
go back to reference Wallick CJ, Gamper I, Thorne M, Feith DJ, Takasaki KY, Wilson SM et al (2005) Key role for p27Kip1, retinoblastoma protein Rb, and MYCN in polyamine inhibitor-induced G1 cell cycle arrest in MYCN-amplified human neuroblastoma cells. Oncogene 24(36):5606–5618PubMedCrossRef Wallick CJ, Gamper I, Thorne M, Feith DJ, Takasaki KY, Wilson SM et al (2005) Key role for p27Kip1, retinoblastoma protein Rb, and MYCN in polyamine inhibitor-induced G1 cell cycle arrest in MYCN-amplified human neuroblastoma cells. Oncogene 24(36):5606–5618PubMedCrossRef
84.
go back to reference Otto T, Horn S, Brockmann M, Eilers U, Schuttrumpf L, Popov N et al (2009) Stabilization of N-Myc is a critical function of Aurora A in human neuroblastoma. Cancer Cell 15(1):67–78PubMedCrossRef Otto T, Horn S, Brockmann M, Eilers U, Schuttrumpf L, Popov N et al (2009) Stabilization of N-Myc is a critical function of Aurora A in human neuroblastoma. Cancer Cell 15(1):67–78PubMedCrossRef
85.
go back to reference Nishida A, Furukawa A, Koike C, Tano Y, Aizawa S, Matsuo I et al (2003) Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nat Neurosci 6(12):1255–1263PubMedCrossRef Nishida A, Furukawa A, Koike C, Tano Y, Aizawa S, Matsuo I et al (2003) Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nat Neurosci 6(12):1255–1263PubMedCrossRef
86.
go back to reference Li J, Di C, Jing J, Di Q, Nakhla J, Adamson DC (2015) OTX2 is a therapeutic target for retinoblastoma and may function as a common factor between C-MYC, CRX, and phosphorylated RB pathways. Int J Oncol 47(5):1703–1710PubMedCrossRef Li J, Di C, Jing J, Di Q, Nakhla J, Adamson DC (2015) OTX2 is a therapeutic target for retinoblastoma and may function as a common factor between C-MYC, CRX, and phosphorylated RB pathways. Int J Oncol 47(5):1703–1710PubMedCrossRef
87.
go back to reference Glubrecht DD, Kim JH, Russell L, Bamforth JS, Godbout R (2009) Differential CRX and OTX2 expression in human retina and retinoblastoma. J Neurochem 111(1):250–263PubMedPubMedCentralCrossRef Glubrecht DD, Kim JH, Russell L, Bamforth JS, Godbout R (2009) Differential CRX and OTX2 expression in human retina and retinoblastoma. J Neurochem 111(1):250–263PubMedPubMedCentralCrossRef
88.
go back to reference Mol BM, Massink MP, van der Hout AH, Dommering CJ, Zaman JM, Bosscha MI et al (2014) High resolution SNP array profiling identifies variability in retinoblastoma genome stability. Genes Chromosomes Cancer 53(1):1–14PubMedCrossRef Mol BM, Massink MP, van der Hout AH, Dommering CJ, Zaman JM, Bosscha MI et al (2014) High resolution SNP array profiling identifies variability in retinoblastoma genome stability. Genes Chromosomes Cancer 53(1):1–14PubMedCrossRef
89.
go back to reference Bunt J, Hasselt NE, Zwijnenburg DA, Hamdi M, Koster J, Versteeg R et al (2012) OTX2 directly activates cell cycle genes and inhibits differentiation in medulloblastoma cells. Int J Cancer 131(2):E21–E32PubMedCrossRef Bunt J, Hasselt NE, Zwijnenburg DA, Hamdi M, Koster J, Versteeg R et al (2012) OTX2 directly activates cell cycle genes and inhibits differentiation in medulloblastoma cells. Int J Cancer 131(2):E21–E32PubMedCrossRef
90.
go back to reference Lu Y, Labak CM, Jain N, Purvis IJ, Guda MR, Bach SE et al (2017) OTX2 expression contributes to proliferation and progression in Myc-amplified medulloblastoma. Am J Cancer Res 7(3):647–656PubMedPubMedCentral Lu Y, Labak CM, Jain N, Purvis IJ, Guda MR, Bach SE et al (2017) OTX2 expression contributes to proliferation and progression in Myc-amplified medulloblastoma. Am J Cancer Res 7(3):647–656PubMedPubMedCentral
91.
go back to reference Adamson DC, Shi Q, Wortham M, Northcott PA, Di C, Duncan CG et al (2010) OTX2 is critical for the maintenance and progression of Shh-independent medulloblastomas. Cancer Res 70(1):181–191PubMedCrossRef Adamson DC, Shi Q, Wortham M, Northcott PA, Di C, Duncan CG et al (2010) OTX2 is critical for the maintenance and progression of Shh-independent medulloblastomas. Cancer Res 70(1):181–191PubMedCrossRef
92.
go back to reference Bunt J, Hasselt NE, Zwijnenburg DA, Koster J, Versteeg R, Kool M (2011) Joint binding of OTX2 and MYC in promotor regions is associated with high gene expression in medulloblastoma. PLoS ONE 6(10):e26058PubMedPubMedCentralCrossRef Bunt J, Hasselt NE, Zwijnenburg DA, Koster J, Versteeg R, Kool M (2011) Joint binding of OTX2 and MYC in promotor regions is associated with high gene expression in medulloblastoma. PLoS ONE 6(10):e26058PubMedPubMedCentralCrossRef
93.
go back to reference Elias WJ, Lopes MB, Golden WL, Jane JA Sr, Gonzalez-Fernandez F (2001) Trilateral retinoblastoma variant indicative of the relevance of the retinoblastoma tumor-suppressor pathway to medulloblastomas in humans. J Neurosurg 95(5):871–878PubMedCrossRef Elias WJ, Lopes MB, Golden WL, Jane JA Sr, Gonzalez-Fernandez F (2001) Trilateral retinoblastoma variant indicative of the relevance of the retinoblastoma tumor-suppressor pathway to medulloblastomas in humans. J Neurosurg 95(5):871–878PubMedCrossRef
94.
go back to reference Jurkiewicz E, Pakula-Kosciesza I, Rutynowska O, Nowak K (2010) Trilateral retinoblastoma: an institutional experience and review of the literature. Childs Nerv Syst 26(1):129–132PubMedCrossRef Jurkiewicz E, Pakula-Kosciesza I, Rutynowska O, Nowak K (2010) Trilateral retinoblastoma: an institutional experience and review of the literature. Childs Nerv Syst 26(1):129–132PubMedCrossRef
95.
go back to reference Mouratova T (2005) Trilateral retinoblastoma: a literature review, 1971–2004. Bull Soc Belge Ophtalmol 297:25–35 Mouratova T (2005) Trilateral retinoblastoma: a literature review, 1971–2004. Bull Soc Belge Ophtalmol 297:25–35
96.
go back to reference Syed NA, Nork TM, Poulsen GL, Riis RC, George C, Albert DM (1997) Retinoblastoma in a dog. Arch Ophthalmol 115(6):758–763PubMedCrossRef Syed NA, Nork TM, Poulsen GL, Riis RC, George C, Albert DM (1997) Retinoblastoma in a dog. Arch Ophthalmol 115(6):758–763PubMedCrossRef
97.
go back to reference McEvoy J, Flores-Otero J, Zhang J, Nemeth K, Brennan R, Bradley C et al (2011) Coexpression of normally incompatible developmental pathways in retinoblastoma genesis. Cancer Cell 20(2):260–275PubMedPubMedCentralCrossRef McEvoy J, Flores-Otero J, Zhang J, Nemeth K, Brennan R, Bradley C et al (2011) Coexpression of normally incompatible developmental pathways in retinoblastoma genesis. Cancer Cell 20(2):260–275PubMedPubMedCentralCrossRef
98.
go back to reference McFall RC, Sery TW, Makadon M (1977) Characterization of a new continuous cell line derived from a human retinoblastoma. Cancer Res 37(4):1003–1010PubMed McFall RC, Sery TW, Makadon M (1977) Characterization of a new continuous cell line derived from a human retinoblastoma. Cancer Res 37(4):1003–1010PubMed
99.
go back to reference Reid TW, Albert DM, Rabson AS, Russell P, Craft J, Chu EW et al (1974) Characteristics of an established cell line of retinoblastoma. J Natl Cancer Inst 53(2):347–360PubMedCrossRef Reid TW, Albert DM, Rabson AS, Russell P, Craft J, Chu EW et al (1974) Characteristics of an established cell line of retinoblastoma. J Natl Cancer Inst 53(2):347–360PubMedCrossRef
100.
go back to reference Laurie N, Mohan A, McEvoy J, Reed D, Zhang J, Schweers B et al (2009) Changes in retinoblastoma cell adhesion associated with optic nerve invasion. Mol Cell Biol 29(23):6268–6282PubMedPubMedCentralCrossRef Laurie N, Mohan A, McEvoy J, Reed D, Zhang J, Schweers B et al (2009) Changes in retinoblastoma cell adhesion associated with optic nerve invasion. Mol Cell Biol 29(23):6268–6282PubMedPubMedCentralCrossRef
101.
go back to reference Kim JH, Kim JH, Yu YS, Kim DH, Kim CJ, Kim KW (2007) Establishment and characterization of a novel, spontaneously immortalized retinoblastoma cell line with adherent growth. Int J Oncol 31(3):585–592PubMed Kim JH, Kim JH, Yu YS, Kim DH, Kim CJ, Kim KW (2007) Establishment and characterization of a novel, spontaneously immortalized retinoblastoma cell line with adherent growth. Int J Oncol 31(3):585–592PubMed
102.
go back to reference Fournier GA, Sang DN, Albert DM, Craft JL (1987) Electron microscopy and HLA expression of a new cell line of retinoblastoma. Invest Ophthalmol Vis Sci 28(4):690–699PubMed Fournier GA, Sang DN, Albert DM, Craft JL (1987) Electron microscopy and HLA expression of a new cell line of retinoblastoma. Invest Ophthalmol Vis Sci 28(4):690–699PubMed
103.
go back to reference Windle JJ, Albert DM, O’Brien JM, Marcus DM, Disteche CM, Bernards R et al (1990) Retinoblastoma in transgenic mice. Nature 343(6259):665–669PubMedCrossRef Windle JJ, Albert DM, O’Brien JM, Marcus DM, Disteche CM, Bernards R et al (1990) Retinoblastoma in transgenic mice. Nature 343(6259):665–669PubMedCrossRef
104.
go back to reference 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 4:14PubMedPubMedCentralCrossRef 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 4:14PubMedPubMedCentralCrossRef
105.
go back to reference Gyda M, Wolman M, Lorent K, Granato M (2012) The tumor suppressor gene retinoblastoma-1 is required for retinotectal development and visual function in zebrafish. PLoS Genet 8(11):e1003106PubMedPubMedCentralCrossRef Gyda M, Wolman M, Lorent K, Granato M (2012) The tumor suppressor gene retinoblastoma-1 is required for retinotectal development and visual function in zebrafish. PLoS Genet 8(11):e1003106PubMedPubMedCentralCrossRef
106.
go back to reference Solin SL, Shive HR, Woolard KD, Essner JJ, McGrail M (2015) Rapid tumor induction in zebrafish by TALEN-mediated somatic inactivation of the retinoblastoma1 tumor suppressor rb1. Sci Rep 5:13745PubMedPubMedCentralCrossRef Solin SL, Shive HR, Woolard KD, Essner JJ, McGrail M (2015) Rapid tumor induction in zebrafish by TALEN-mediated somatic inactivation of the retinoblastoma1 tumor suppressor rb1. Sci Rep 5:13745PubMedPubMedCentralCrossRef
107.
go back to reference Gallie BL, Albert DM, Wong JJ, Buyukmihci N, Pullafito CA (1977) Heterotransplantation of retinoblastoma into the athymic “nude” mouse. Invest Ophthalmol Vis Sci 16(3):256–259PubMed Gallie BL, Albert DM, Wong JJ, Buyukmihci N, Pullafito CA (1977) Heterotransplantation of retinoblastoma into the athymic “nude” mouse. Invest Ophthalmol Vis Sci 16(3):256–259PubMed
108.
go back to reference Chevez-Barrios P, Hurwitz MY, Louie K, Marcus KT, Holcombe VN, Schafer P et al (2000) Metastatic and nonmetastatic models of retinoblastoma. Am J Pathol 157(4):1405–1412PubMedPubMedCentralCrossRef Chevez-Barrios P, Hurwitz MY, Louie K, Marcus KT, Holcombe VN, Schafer P et al (2000) Metastatic and nonmetastatic models of retinoblastoma. Am J Pathol 157(4):1405–1412PubMedPubMedCentralCrossRef
109.
110.
go back to reference Nassr M, Wang X, Mitra S, Freeman-Anderson NE, Patil R, Yates CR et al (2010) Treating retinoblastoma in tissue culture and in a rat model with a novel isoquinoline derivative. Invest Ophthalmol Vis Sci 51(7):3813–3819PubMedCrossRef Nassr M, Wang X, Mitra S, Freeman-Anderson NE, Patil R, Yates CR et al (2010) Treating retinoblastoma in tissue culture and in a rat model with a novel isoquinoline derivative. Invest Ophthalmol Vis Sci 51(7):3813–3819PubMedCrossRef
111.
go back to reference del Cerro M, Seigel GM, Lazar E, Grover D, del Cerro C, Brooks DH et al (1993) Transplantation of Y79 cells into rat eyes: an in vivo model of human retinoblastomas. Invest Ophthalmol Vis Sci 34(12):3336–3346PubMed del Cerro M, Seigel GM, Lazar E, Grover D, del Cerro C, Brooks DH et al (1993) Transplantation of Y79 cells into rat eyes: an in vivo model of human retinoblastomas. Invest Ophthalmol Vis Sci 34(12):3336–3346PubMed
112.
go back to reference Chen X, Wang J, Cao Z, Hosaka K, Jensen L, Yang H et al (2015) Invasiveness and metastasis of retinoblastoma in an orthotopic zebrafish tumor model. Sci Rep 5:10351PubMedPubMedCentralCrossRef Chen X, Wang J, Cao Z, Hosaka K, Jensen L, Yang H et al (2015) Invasiveness and metastasis of retinoblastoma in an orthotopic zebrafish tumor model. Sci Rep 5:10351PubMedPubMedCentralCrossRef
113.
go back to reference Jo DH, Son D, Na Y, Jang M, Choi JH, Kim JH et al (2013) Orthotopic transplantation of retinoblastoma cells into vitreous cavity of zebrafish for screening of anticancer drugs. Mol Cancer 12:71PubMedPubMedCentralCrossRef Jo DH, Son D, Na Y, Jang M, Choi JH, Kim JH et al (2013) Orthotopic transplantation of retinoblastoma cells into vitreous cavity of zebrafish for screening of anticancer drugs. Mol Cancer 12:71PubMedPubMedCentralCrossRef
114.
go back to reference Zhong X, Gutierrez C, Xue T, Hampton C, Vergara MN, Cao LH et al (2014) Generation of three-dimensional retinal tissue with functional photoreceptors from human iPSCs. Nat Commun 5:4047PubMedPubMedCentral Zhong X, Gutierrez C, Xue T, Hampton C, Vergara MN, Cao LH et al (2014) Generation of three-dimensional retinal tissue with functional photoreceptors from human iPSCs. Nat Commun 5:4047PubMedPubMedCentral
115.
go back to reference Zeng S, Liu L, Ouyang Q, Zhao Y, Lin G, Hu L et al (2016) Generation of induced pluripotent stem cells (iPSCs) from a retinoblastoma patient carrying a c.2663G > A mutation in RB1 gene. Stem Cell Res 17(2):208–211PubMedCrossRef Zeng S, Liu L, Ouyang Q, Zhao Y, Lin G, Hu L et al (2016) Generation of induced pluripotent stem cells (iPSCs) from a retinoblastoma patient carrying a c.2663G > A mutation in RB1 gene. Stem Cell Res 17(2):208–211PubMedCrossRef
116.
go back to reference Avior Y, Lezmi E, Yanuka D, Benvenisty N (2017) Modeling developmental and tumorigenic aspects of trilateral retinoblastoma via human embryonic stem cells. Stem Cell Rep 8:1354CrossRef Avior Y, Lezmi E, Yanuka D, Benvenisty N (2017) Modeling developmental and tumorigenic aspects of trilateral retinoblastoma via human embryonic stem cells. Stem Cell Rep 8:1354CrossRef
117.
go back to reference Liao V, Harutyunyan N, Aparicio J, Cobrinik D, Lee TC (2014) Evaluation of human embryonic stem cell-derived retina as a potential retinoblastoma model. Invest Ophthalmol Vis Sci 55(13):2984 Liao V, Harutyunyan N, Aparicio J, Cobrinik D, Lee TC (2014) Evaluation of human embryonic stem cell-derived retina as a potential retinoblastoma model. Invest Ophthalmol Vis Sci 55(13):2984
Metadata
Title
Heterogeneity in retinoblastoma: a tale of molecules and models
Authors
Sonya Stenfelt
Maria K. E. Blixt
Charlotta All-Ericsson
Finn Hallböök
Henrik Boije
Publication date
01-12-2017
Publisher
Springer Berlin Heidelberg
Published in
Clinical and Translational Medicine / Issue 1/2017
Electronic ISSN: 2001-1326
DOI
https://doi.org/10.1186/s40169-017-0173-2