The TAg-RB murine retinoblastoma cell of origin has immunohistochemical features of differentiated müller glia with progenitor properties

Investigative Ophthalmology and Visual Science

Volumn 52, Issue 10, 2011, Pages 7618-7624

  Pajovic, Sanja ^a   Corson, Timothy W ^b   Spencer, Clarellen ^a   Dimaras, Helen ^c,d   Orlic Milacic, Marija ^a,c,d   Marchong, Mellone N ^a,d,e   To, Kwong Him ^a,c,d   Thèriault, Brigitte ^a   Auspitz, Mark ^a   Gallie, Brenda L ^a,c,d,e  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY HEALTH NETWORK   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONATE DEHYDRATASE II; CASPASE 3; CELL SURFACE MARKER; CELLULAR RETINOID BINDING PROTEIN; CHX10 PROTEIN; CLUSTERIN; GLUTAMATE AMMONIA LIGASE; KI 67 ANTIGEN; NEUROFILAMENT PROTEIN; PROTEIN DEK; PROTEIN KINASE C; PROTEIN P75; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG; VIRUS LARGE T ANTIGEN; BETA3 TUBULIN, MOUSE; CASP3 PROTEIN, MOUSE; DNA; TUBULIN; TUMOR MARKER; VIRUS T ANTIGEN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DNA DETERMINATION; EMBRYO; GENE DOSAGE; IMMUNOHISTOCHEMISTRY; MOUSE; MUELLER CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RETINA BIPOLAR GANGLION CELL; RETINOBLASTOMA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; STEM CELL; TUMOR GROWTH; ANIMAL; APOPTOSIS; C57BL MOUSE; CANCER STEM CELL; CELL DIFFERENTIATION; CELL LINEAGE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; GLIA; METABOLISM; PATHOLOGY; PHYSIOLOGY; RETINA TUMOR;

ANIMALS; ANTIGENS, POLYOMAVIRUS TRANSFORMING; APOPTOSIS; CASPASE 3; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; DNA, NEOPLASM; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION REGULATION; GENE SILENCING; KI-67 ANTIGEN; MICE; MICE, INBRED C57BL; NEOPLASTIC STEM CELLS; NEUROGLIA; RETINAL NEOPLASMS; RETINOBLASTOMA; RETINOBLASTOMA PROTEIN; TUBULIN; TUMOR MARKERS, BIOLOGICAL;

EID: 84856402585     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.11-7989     Document Type: Article

References (59)

1. DiCiommo D, Gallie BL, Bremner R. Retinoblastoma: the disease, gene and protein provide critical leads to understand cancer. Semin Cancer Biol. 2000;10:255-269.
2. Clarke AR, Maandag ER, van Roon M, et al. Requirement for a functional Rb-1 gene in murine development. Nature. 1992;359: 328-330.
3. Jacks T, Fazeli A, Schmitt EM, Bronson RT, Goodell MA, Weinberg RA. Effects of an Rb mutation in the mouse. Nature. 1992;359: 295-300.
4. Lee EY, Chang CY, Hu N, et al. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature. 1992;359:288-294.
5. Wu L, de Bruin A, Saavedra HI, et al. Extra-embryonic function of Rb is essential for embryonic development and viability. Nature. 2003;421:942-947.
6. Macpherson D, Conkrite K, Tam M, Mukai S, Mu D, Jacks T. Murine bilateral retinoblastoma exhibiting rapid-onset, metastatic progression and N-myc gene amplification. EMBO J. 2007;26:784-794.
7. MacPherson D, Sage J, Kim T, Ho D, McLaughlin ME, Jacks T. Cell type-specific effects of Rb deletion in the murine retina. Genes Dev. 2004;18:1681-1694.
8. Robanus-Maandag E, Dekker M, van der Valk M, et al. p107 is a suppressor of retinoblastoma development in pRb-deficient mice. Genes Dev. 1998;12:1599-1609.
9. Chen D, Livne-bar I, Vanderluit JL, Slack RS, Agochiya M, Bremner R. Cell-specific effects of RB or RB/p107 loss on retinal development implicate an intrinsically death-resistant cell-of-origin in retinoblastoma. Cancer Cell. 2004;5:539-551.
10. Ali SH, DeCaprio JA. Cellular transformation by SV40 large T antigen: interaction with host proteins. Semin Cancer Biol. 2001;11:15-23.
11. Windle JJ, Albert DM, O'Brien JM, et al. Retinoblastoma in transgenic mice. Nature. 1990;343:665-669.
12. Ts'o MO, Fine BS, Zimmerman LE. The Flexner-Wintersteiner rosettes in retinoblastoma. Arch Pathol. 1969;88:664-671.
13. O'Brien JM, Marcus DM, Bernards R, et al. A transgenic mouse model for trilateral retinoblastoma. Arch Ophthalmol. 1990;108: 1145-1151.
14. Dimaras H, Coburn B, Pajovic S, Gallie BL. The loss of p75 neurotrophin receptor expression accompanies malignant progression to human and murine retinoblastoma. Mol Carcinogen. 2006; 45:333-343.
15. Marchong MN, Chen D, Corson TW, et al. Minimal 16q genomic loss implicates cadherin-11 in retinoblastoma. Mol Cancer Res. 2004;2:495-503.
16. Orlic M, Spencer CE, Wang L, Gallie BL. Expression analysis of 6p22 genomic gain in retinoblastoma. Genes Chromosomes Cancer. 2006;45:72-82.
17. Houston SK, Pina Y, Clarke J, et al. Regional and temporal differences in gene expression of LHBETATAG retinoblastoma tumors. Invest Ophthalmol Vis Sci. 2011.
18. Bajenaru ML, Pina Y, Murray TG, et al. Gelatinase expression in retinoblastoma: modulation of LH(BETA)T(AG) retinal tumor development by anecortave acetate. Invest Ophthalmol Vis Sci. 2010;51:2860-2864.
19. Boutrid H, Jockovich ME, Murray TG, et al. Targeting hypoxia, a novel treatment for advanced retinoblastoma. Invest Ophthalmol Vis Sci. 2008;49:2799-2805.
20. Boutrid H, Pina Y, Cebulla CM, et al. Increased hypoxia following vessel targeting in a murine model of retinoblastoma. Invest Ophthalmol Vis Sci. 2009;50:5537-5543.
21. Hayden B, Jockovich ME, Murray TG, et al. Iontophoretic delivery of carboplatin in a murine model of retinoblastoma. Invest Ophthalmol Vis Sci. 2006;47:3717-3721.
22. Jockovich ME, Bajenaru ML, Pina Y, et al. Retinoblastoma tumor vessel maturation impacts efficacy of vessel targeting in the LH-(BETA)T(AG) mouse model. Invest Ophthalmol Vis Sci. 2007;48: 2476-2482.
23. Jockovich ME, Murray TG, Escalona-Benz E, Hernandez E, Feuer W. Anecortave acetate as single and adjuvant therapy in the treatment of retinal tumors of LH(BETA)T(AG) mice. Invest Ophthalmol Vis Sci. 2006;47:1264-1268.
24. Jockovich ME, Suarez F, Alegret A, et al. Mechanism of retinoblastoma tumor cell death after focal chemotherapy, radiation, and vascular targeting therapy in a mouse model. Invest Ophthalmol Vis Sci. 2007;48:5371-5376.
25. Kang SJ, Durairaj C, Kompella UB, O'Brien JM, Grossniklaus HE. Subconjunctival nanoparticle carboplatin in the treatment of murine retinoblastoma. Arch Ophthalmol. 2009;127:1043-1047.
26. Pina Y, Houston SK, Murray TG, et al. Focal, periocular delivery of 2-deoxy-D-glucose as adjuvant to chemotherapy for treatment of advanced retinoblastoma. Invest Ophthalmol Vis Sci. 2010;51: 6149-6156.
27. Suarez F, Jockovich ME, Hernandez E, Feuer W, Parel JM, Murray TG. Paclitaxel in the treatment of retinal tumors of LH beta-Tag murine transgenic model of retinoblastoma. Invest Ophthalmol Vis Sci. 2007;48:3437-3440.
28. Dimaras H, Marchong MN, Gallie BL. Quantitative analysis of tumor size in a murine model of retinoblastoma. Ophthalmic Genet. 2009;30:84-90.
29. Ruggeri M, Tsechpenakis G, Jiao S, et al. Retinal tumor imaging and volume quantification in mouse model using spectral-domain optical coherence tomography. Opt Express. 2009;17:4074-4083.
30. Ruggeri M, Wehbe H, Jiao S, et al. In vivo three-dimensional high-resolution imaging of rodent retina with spectral-domain optical coherence tomography. Invest Ophthalmol Vis Sci. 2007;48: 1808-1814.
31. Landreville S, Ma D, Wu J, Harbour JW. Loss of Id2 potentiates the tumorigenic effect of Rb inactivation in a mouse model of retinoblastoma. Curr Eye Res. 2010;35:435-439.
32. Marchong MN, Yurkowski C, Ma C, Spencer C, Pajovic S, Gallie BL. Cdh11 acts as a tumor suppressor in a murine retinoblastoma model by facilitating tumor cell death. PLoS Genet. 2010;6: e1000923.
33. Pina Y, Boutrid H, Murray TG, et al. Impact of tumor-associated macrophages in LH(BETA)T(AG) mice on retinal tumor progression: relation to macrophage subtype. Invest Ophthalmol Vis Sci. 2010;51:2671-2677.
34. Pina Y, Boutrid H, Schefler A, et al. Blood vessel maturation in retinoblastoma tumors: spatial distribution of neovessels and mature vessels and its impact on ocular treatment. Invest Ophthalmol Vis Sci. 2009;50:1020-1024.
35. Seigel GM, Campbell LM, Narayan M, Gonzalez-Fernandez F. Cancer stem cell characteristics in retinoblastoma. Mol Vis. 2005;11: 729-737.
36. Vinores SA, Derevjanik NL, Mahlow J, et al. Class III beta-tubulin in human retinal pigment epithelial cells in culture and in epiretinal membranes. Exp Eye Res. 1995;60:385-400.
37. Katsetos CD, Legido A, Perentes E, Mork SJ. Class III beta-tubulin isotype: a key cytoskeletal protein at the crossroads of developmental neurobiology and tumor neuropathology. J Child Neurol. 2003;18:851-866.
38. Blackshaw S, Harpavat S, Trimarchi J, et al. Genomic analysis of mouse retinal development. PLoS Biol. 2004;2:E247.
39. Negishi K, Kato S, Teranishi T. Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neurosci Lett. 1988;94:247-252.
40. Corson TW, Huang A, Tsao MS, Gallie BL. KIF14 is a candidate oncogene in the 1q minimal region of genomic gain in multiple cancers. Oncogene. 2005;24:4741-4753.
41. Bowles E, Corson TW, Bayani J, et al. Profiling genomic copy number changes in retinoblastoma beyond loss of RB1. Genes Chromosomes Cancer. 2007;46:118-129.
42. Pacal M, Bremner R. Insights from animal models on the origins and progression of retinoblastoma. Curr Mol Med. 2006;6:759-781.
43. al-Ubaidi MR, Font RL, Quiambao AB, et al. Bilateral retinal and brain tumors in transgenic mice expressing simian virus 40 large T antigen under control of the human interphotoreceptor retinoidbinding protein promoter. J Cell Biol. 1992;119:1681-1687.
44. Penna D, Schmidt A, Beermann F. Tumors of the retinal pigment epithelium metastasize to inguinal lymph nodes and spleen in tyrosinase-related protein 1/SV40 T antigen transgenic mice. Oncogene. 1998;17:2601-2607.
45. Peachey NS, Roveri L, Messing A, McCall MA. Functional consequences of oncogene-induced horizontal cell degeneration in the retinas of transgenic mice. Vis Neurosci. 1997;14:627-632.
46. Dyer MA, Bremner R. The search for the retinoblastoma cell of origin. Nat Rev Cancer. 2005;5:91-101.
47. Mirshahi M, Boucheix C, Dhermy P, Haye C, Faure JP. Expression of the photoreceptor-specific S-antigen in human retinoblastoma. Cancer. 1986;57:1497-1500.
48. Ohira A, Yamamoto M, Honda O, Ohnishi Y, Inomata H, Honda Y. Glial-, neuronal-and photoreceptor-specific cell markers in rosettes of retinoblastoma and retinal dysplasia. Curr Eye Res. 1994; 13:799-804.
49. Ts'o MO, Fine BS, Zimmerman LE. The nature of retinoblastoma. II. Photoreceptor differentiation: an electron microscopic study. Am J Ophthalmol. 1970;69:350-359.
50. Ts'o MO, Zimmerman LE, Fine BS. The nature of retinoblastoma. I. Photoreceptor differentiation: a clinical and histopathologic study. Am J Ophthalmol. 1970;69:339-349.
51. Nork TM, Schwartz TL, Doshi HM, Millecchia LL. Retinoblastoma. Cell of origin. Arch Ophthalmol. 1995;113:791-802.
52. Perentes E, Herbort CP, Rubinstein LJ, et al. Immunohistochemical characterization of human retinoblastomas in situ with multiple markers. Am J Ophthalmol. 1987;103:647-658.
53. Rowan S, Cepko CL. Genetic analysis of the homeodomain transcription factor Chx10 in the retina using a novel multifunctional BAC transgenic mouse reporter. Dev Biol. 2004;271:388-402.
54. Das AV, Mallya KB, Zhao X, et al. Neural stem cell properties of Muller glia in the mammalian retina: regulation by Notch and Wnt signaling. Dev Biol. 2006;299:283-302.
55. Park KH, Hallows JL, Chakrabarty P, Davies P, Vincent I. Conditional neuronal simian virus 40 T antigen expression induces Alzheimer-like tau and amyloid pathology in mice. J Neurosci. 2007;27:2969-2978.
56. Feddersen RM, Ehlenfeldt R, Yunis WS, Clark HB, Orr HT. Disrupted cerebellar cortical development and progressive degeneration of Purkinje cells in SV40 T antigen transgenic mice. Neuron. 1992;9:955-966.
57. Xu XL, Fang Y, Lee TC, et al. Retinoblastoma has properties of a cone precursor tumor and depends upon cone-specific MDM2 signaling. Cell. 2009;137:1018-1031.
58. Laurie NA, Donovan SL, Shih CS, et al. Inactivation of the p53 pathway in retinoblastoma. Nature. 2006;444:61-66.
59. Guo Y, Pajovic S, Gallie BL. Expression of p14ARF, MDM2, and MDM4 in human retinoblastoma. Biochem Biophys Res Commun. 2008;375:1-5.