Brg1 coordinates multiple processes during retinogenesis and is a tumor suppressor in retinoblastoma

Aldiri, I.; Ajioka, I.; Xu, B.; Zhang, J.; Chen, X.; Benavente, C.; Finkelstein, D.; Johnson, D.; Akiyama, J.; Pennacchio, L. A.; Dyer, M. A.

doi:10.1242/dev.124800

Title: Brg1 coordinates multiple processes during retinogenesis and is a tumor suppressor in retinoblastoma

Journal Article · Tue Dec 01 00:00:00 EST 2015 · Development (Cambridge)

DOI:https://doi.org/10.1242/dev.124800· OSTI ID:1378673

Aldiri, I. ^[1]; Ajioka, I. ^[2]; Xu, B. ^[3]; Zhang, J. ^[1]; Chen, X. ^[3]; Benavente, C. ^[1]; Finkelstein, D. ^[3]; Johnson, D. ^[4]; Akiyama, J. ^[5]; Pennacchio, L. A. ^[5]; Dyer, M. A. ^[6]

St. Jude's Children's Research Hospital, Memphis, TN (United States). Dept. of Developmental Neurobiology
Tokyo Medical and Dental Univ. (Japan). Center for Brain Integration Research
St. Jude's Research Hospital, Memphis, TN (United States). Dept. of Computational Biology
Univ. of Tennessee, Memphis, TN (United States). Health Science Center
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Genomics Division; USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
St. Jude's Children's Research Hospital, Memphis, TN (United States). Dept. of Developmental Neurobiology; Univ. of Tennessee, Memphis, TN (United States). Health Science Center; Howard Hughes Medical Inst., Chevy Chase, MD (United States)

Retinal development requires precise temporal and spatial coordination of cell cycle exit, cell fate specification, cell migration and differentiation. When this process is disrupted, retinoblastoma, a developmental tumor of the retina, can form. Epigenetic modulators are central to precisely coordinating developmental events, and many epigenetic processes have been implicated in cancer. Studying epigenetic mechanisms in development is challenging because they often regulate multiple cellular processes; therefore, elucidating the primary molecular mechanisms involved can be difficult. Here we explore the role of Brg1 (Smarca4) in retinal development and retinoblastoma in mice using molecular and cellular approaches. Brg1 was found to regulate retinal size by controlling cell cycle length, cell cycle exit and cell survival during development. Brg1 was not required for cell fate specification but was required for photoreceptor differentiation and cell adhesion/polarity programs that contribute to proper retinal lamination during development. The combination of defective cell differentiation and lamination led to retinal degeneration in Brg1-deficient retinae. Despite the hypocellularity, premature cell cycle exit, increased cell death and extended cell cycle length, retinal progenitor cells persisted in Brg1-deficient retinae, making them more susceptible to retinoblastoma. In conclusion, ChIP-Seq analysis suggests that Brg1 might regulate gene expression through multiple mechanisms.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1378673

Alternate ID(s):: OSTI ID: 1256950

Journal Information:: Development (Cambridge), Vol. 142, Issue 23; ISSN 0950-1991

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 25 works

Citation information provided by
Web of Science

References (99)

Differentiated Horizontal Interneurons Clonally Expand to Form Metastatic Retinoblastoma in Mice Ajioka, Itsuki; Martins, Rodrigo A. P.; Bayazitov, Ildar T. Cell, Vol. 131, Issue 2 https://doi.org/10.1016/j.cell.2007.09.036	journal	October 2007
Brg1 modulates enhancer activation in mesoderm lineage commitment Alexander, J. M.; Hota, S. K.; He, D. Development, Vol. 142, Issue 8 https://doi.org/10.1242/dev.109496	journal	March 2015
Tissue-specific SMARCA4 binding at active and repressed regulatory elements during embryogenesis Attanasio, C.; Nord, A. S.; Zhu, Y. Genome Research, Vol. 24, Issue 6 https://doi.org/10.1101/gr.168930.113	journal	April 2014
Chromatin remodelers HELLS and UHRF1 mediate the epigenetic deregulation of genes that drive retinoblastoma tumor progression Benavente, Claudia A.; Finkelstein, David; Johnson, Dianna A. Oncotarget, Vol. 5, Issue 20 https://doi.org/10.18632/oncotarget.2468	journal	October 2014
Erratum: A mammalian microRNA cluster controls DNA methylation and telomere recombination via Rbl2-dependent regulation of DNA methyltransferases Benetti, Roberta; Gonzalo, Susana; Jaco, Isabel Nature Structural & Molecular Biology, Vol. 15, Issue 9 https://doi.org/10.1038/nsmb0908-998b	journal	September 2008
SWI/SNF Deficiency Results in Aberrant Chromatin Organization, Mitotic Failure, and Diminished Proliferative Capacity Bourgo, Ryan J.; Siddiqui, Hasan; Fox, Sejal Molecular Biology of the Cell, Vol. 20, Issue 14 https://doi.org/10.1091/mbc.E08-12-1224	journal	July 2009
Characterization of mammary tumors from Brg1 heterozygous mice Bultman, S. J.; Herschkowitz, J. I.; Godfrey, V. Oncogene, Vol. 27, Issue 4 https://doi.org/10.1038/sj.onc.1210664	journal	July 2007
Functional Characterization of the Opitz Syndrome Gene Product (Midin): Evidence for Homodimerization and Association With Microtubules Throughout the Cell Cycle Cainarca, S.; Messali, S.; Ballabio, A. Human Molecular Genetics, Vol. 8, Issue 8 https://doi.org/10.1093/hmg/8.8.1387	journal	August 1999
Cell fate determination in the vertebrate retina. Cepko, C. L.; Austin, C. P.; Yang, X. Proceedings of the National Academy of Sciences, Vol. 93, Issue 2 https://doi.org/10.1073/pnas.93.2.589	journal	January 1996
Development and diversification of retinal amacrine interneurons at single cell resolution Cherry, T. J.; Trimarchi, J. M.; Stadler, M. B. Proceedings of the National Academy of Sciences, Vol. 106, Issue 23 https://doi.org/10.1073/pnas.0903264106	journal	May 2009
Covalent histone modifications — miswritten, misinterpreted and mis-erased in human cancers Chi, Ping; Allis, C. David; Wang, Gang Greg Nature Reviews Cancer, Vol. 10, Issue 7 https://doi.org/10.1038/nrc2876	journal	July 2010
Mutations in ABCD4 cause a new inborn error of vitamin B12 metabolism Coelho, David; Kim, Jaeseung C.; Miousse, Isabelle R. Nature Genetics, Vol. 44, Issue 10 https://doi.org/10.1038/ng.2386	journal	August 2012
Developmental defects in Rb-deficient retinae Donovan, Stacy L.; Dyer, Michael A. Vision Research, Vol. 44, Issue 28 https://doi.org/10.1016/j.visres.2004.08.007	journal	December 2004
Compensation by tumor suppressor genes during retinal development in mice and humans Donovan, Stacy L.; Schweers, Brett; Martins, Rodrigo BMC Biology, Vol. 4, Issue 1 https://doi.org/10.1186/1741-7007-4-14	journal	May 2006
The retinoblastoma protein and BRG1 form a complex and cooperate to induce cell cycle arrest Dunaief, Joshua L.; Strober, Bruce E.; Guha, Sushovan Cell, Vol. 79, Issue 1 https://doi.org/10.1016/0092-8674(94)90405-7	journal	October 1994
The search for the retinoblastoma cell of origin Dyer, Michael A.; Bremner, Rod Nature Reviews Cancer, Vol. 5, Issue 2 https://doi.org/10.1038/nrc1545	journal	February 2005
p57(Kip2) regulates progenitor cell proliferation and amacrine interneuron development in the mouse retina Dyer, M. A.; Cepko, C. L. Development, Vol. 127, Issue 16 https://doi.org/10.1242/dev.127.16.3593	journal	August 2000
Regulating proliferation during retinal development Dyer, Michael A.; Cepko, Constance L. Nature Reviews Neuroscience, Vol. 2, Issue 5 https://doi.org/10.1038/35072555	journal	May 2001
Prox1 function controls progenitor cell proliferation and horizontal cell genesis in the mammalian retina Dyer, Michael A.; Livesey, Frederick J.; Cepko, Constance L. Nature Genetics, Vol. 34, Issue 1 https://doi.org/10.1038/ng1144	journal	April 2003
Proximity Interactions among Centrosome Components Identify Regulators of Centriole Duplication Firat-Karalar, Elif Nur; Rauniyar, Navin; Yates, John R. Current Biology, Vol. 24, Issue 6 https://doi.org/10.1016/j.cub.2014.01.067	journal	March 2014
A human DNA segment with properties of the gene that predisposes to retinoblastoma and osteosarcoma Friend, Stephen H.; Bernards, Rene; Rogelj, Snezna Nature, Vol. 323, Issue 6089 https://doi.org/10.1038/323643a0	journal	October 1986
β-catenin is essential for lamination but not neurogenesis in mouse retinal development Fu, Xueyao; Sun, Hongxia; Klein, William H. Developmental Biology, Vol. 299, Issue 2 https://doi.org/10.1016/j.ydbio.2006.08.015	journal	November 2006
Role of Rb Family in the Epigenetic Definition of Chromatin Gonzalo, Susana; Blasco, Maria A. Cell Cycle, Vol. 4, Issue 6 https://doi.org/10.4161/cc.4.6.1720	journal	April 2005
Positional cloning of the young mutation identifies an essential role for the Brahma chromatin remodeling complex in mediating retinal cell differentiation Gregg, R. G.; Willer, G. B.; Fadool, J. M. Proceedings of the National Academy of Sciences, Vol. 100, Issue 11 https://doi.org/10.1073/pnas.0631813100	journal	May 2003
Chromatin regulation by Brg1 underlies heart muscle development and disease Hang, Calvin T.; Yang, Jin; Han, Pei Nature, Vol. 466, Issue 7302 https://doi.org/10.1038/nature09130	journal	July 2010
In Vivo Function of the ER-Golgi Transport Protein LMAN1 in Photoreceptor Homeostasis Hao, Hong; Gregorski, Janina; Qian, Haohua Retinal Degenerative Diseases https://doi.org/10.1007/978-1-4614-3209-8_50	book	January 2014
ATP-dependent chromatin remodeling: genetics, genomics and mechanisms Hargreaves, Diana C.; Crabtree, Gerald R. Cell Research, Vol. 21, Issue 3 https://doi.org/10.1038/cr.2011.32	journal	March 2011
A Landscape of Driver Mutations in Melanoma Hodis, Eran; Watson, Ian R.; Kryukov, Gregory V. Cell, Vol. 150, Issue 2 https://doi.org/10.1016/j.cell.2012.06.024	journal	July 2012
Functional epigenetics approach identifies BRM/SMARCA2 as a critical synthetic lethal target in BRG1-deficient cancers Hoffman, G. R.; Rahal, R.; Buxton, F. Proceedings of the National Academy of Sciences, Vol. 111, Issue 8 https://doi.org/10.1073/pnas.1316793111	journal	February 2014
Regulation of nucleosome landscape and transcription factor targeting at tissue-specific enhancers by BRG1 Hu, G.; Schones, D. E.; Cui, K. Genome Research, Vol. 21, Issue 10 https://doi.org/10.1101/gr.121145.111	journal	July 2011
The extracellular matrix component WIF-1 is expressed during, and can modulate, retinal development Hunter, Dale D.; Zhang, Minlei; Ferguson, Jill W. Molecular and Cellular Neuroscience, Vol. 27, Issue 4 https://doi.org/10.1016/j.mcn.2004.08.003	journal	December 2004
Nectin-dependent localization of ZO-1 at puncta adhaerentia junctions between the mossy fiber terminals and the dendrites of the pyramidal cells in the CA3 area of adult mouse hippocampus Inagaki, Maiko; Irie, Kenji; Deguchi-Tawarada, Maki The Journal of Comparative Neurology, Vol. 460, Issue 4 https://doi.org/10.1002/cne.10653	journal	April 2003
Roles of cell-adhesion molecules nectin 1 and nectin 3 in ciliary body development Inagaki, Maiko; Irie, Kenji; Ishizaki, Hiroyoshi Development, Vol. 132, Issue 7 https://doi.org/10.1242/dev.01697	journal	April 2005
Identification of novel E2F1 target genes regulated in cell cycle-dependent and independent manners Iwanaga, R.; Komori, H.; Ishida, S. Oncogene, Vol. 25, Issue 12 https://doi.org/10.1038/sj.onc.1209210	journal	November 2005
Genomic organisation and alternative splicing of human RIM1, a gene implicated in autosomal dominant cone-rod dystrophy (CORD7)☆ Johnson, Samantha; Halford, Stephanie; Morris, Alex G. Genomics, Vol. 81, Issue 3 https://doi.org/10.1016/S0888-7543(03)00010-7	journal	March 2003
Mosaic deletion ofRb arrests rod differentiation and stimulates ectopic synaptogenesis in the mouse retina Johnson, Dianna A.; Donovan, Stacy L.; Dyer, Michael A. The Journal of Comparative Neurology, Vol. 498, Issue 1 https://doi.org/10.1002/cne.21059	journal	January 2006
The Cep192-Organized Aurora A-Plk1 Cascade Is Essential for Centrosome Cycle and Bipolar Spindle Assembly Joukov, Vladimir; Walter, Johannes C.; De Nicolo, Arcangela Molecular Cell, Vol. 55, Issue 4 https://doi.org/10.1016/j.molcel.2014.06.016	journal	August 2014
Centrosomes Tune in to Metabolic State and Turn on to Oxygen Kim, Sehyun; Dynlacht, Brian D. Developmental Cell, Vol. 26, Issue 4 https://doi.org/10.1016/j.devcel.2013.08.001	journal	August 2013
Mutation and Cancer: Statistical Study of Retinoblastoma Knudson, A. G. Proceedings of the National Academy of Sciences, Vol. 68, Issue 4 https://doi.org/10.1073/pnas.68.4.820	journal	April 1971
PP2A Counterbalances Phosphorylation of pRB and Mitotic Proteins by Multiple CDKs: Potential Implications for PP2A Disruption in Cancer Kurimchak, A.; Grana, X. Genes & Cancer, Vol. 3, Issue 11-12 https://doi.org/10.1177/1947601912473479	journal	November 2012
PP2A holoenzymes negatively and positively regulate cell cycle progression by dephosphorylating pocket proteins and multiple CDK substrates Kurimchak, Alison; Graña, Xavier Gene, Vol. 499, Issue 1 https://doi.org/10.1016/j.gene.2012.02.015	journal	May 2012
The cell adhesion gene PVRL3 is associated with congenital ocular defects Lachke, Salil A.; Higgins, Anne W.; Inagaki, Maiko Human Genetics, Vol. 131, Issue 2 https://doi.org/10.1007/s00439-011-1064-z	journal	July 2011
Baf60c is a component of the neural progenitor-specific BAF complex in developing retina Lamba, Deepak A.; Hayes, Susan; Karl, Mike O. Developmental Dynamics, Vol. 237, Issue 10 https://doi.org/10.1002/dvdy.21697	journal	September 2008
Regulation of PP2A activity by Mid1 controls cranial neural crest speed and gangliogenesis Latta, Elizabeth J.; Golding, Jon P. Mechanisms of Development, Vol. 128, Issue 11-12 https://doi.org/10.1016/j.mod.2012.01.002	journal	January 2012
The zebrafish young mutation acts non-cell-autonomously to uncouple differentiation from specification for all retinal cells Link, B. A.; Fadool, J. M.; Malicki, J. Development, Vol. 127, Issue 10 https://doi.org/10.1242/dev.127.10.2177	journal	May 2000
Vertebrate neural cell-fate determination: Lessons from the retina Livesey, F. J.; Cepko, C. L. Nature Reviews Neuroscience, Vol. 2, Issue 2 https://doi.org/10.1038/35053522	journal	February 2001
The genetic landscape of mutations in Burkitt lymphoma Love, Cassandra; Sun, Zhen; Jima, Dereje Nature Genetics, Vol. 44, Issue 12 https://doi.org/10.1038/ng.2468	journal	November 2012
A genome-wide RNA interference screen identifies putative chromatin regulators essential for E2F repression Lu, J.; Ruhf, M. -L.; Perrimon, N. Proceedings of the National Academy of Sciences, Vol. 104, Issue 22 https://doi.org/10.1073/pnas.0610279104	journal	May 2007
Modular mechanism of Wnt signaling inhibition by Wnt inhibitory factor 1 Malinauskas, Tomas; Aricescu, A. Radu; Lu, Weixian Nature Structural & Molecular Biology, Vol. 18, Issue 8 https://doi.org/10.1038/nsmb.2081	journal	July 2011
Glutamate regulates retinal progenitors cells proliferation during development Martins, Rodrigo A. P.; Linden, Rafael; Dyer, Michael A. European Journal of Neuroscience, Vol. 24, Issue 4 https://doi.org/10.1111/j.1460-9568.2006.04966.x	journal	August 2006
Brg1 is required for murine neural stem cell maintenance and gliogenesis Matsumoto, Steven; Banine, Fatima; Struve, Jaime Developmental Biology, Vol. 289, Issue 2 https://doi.org/10.1016/j.ydbio.2005.10.044	journal	January 2006
Coexpression of Normally Incompatible Developmental Pathways in Retinoblastoma Genesis McEvoy, Justina; Flores-Otero, Jacqueline; Zhang, Jiakun Cancer Cell, Vol. 20, Issue 2 https://doi.org/10.1016/j.ccr.2011.07.005	journal	August 2011
Frequent BRG1/SMARCA4-inactivating mutations in human lung cancer cell lines Medina, Pedro P.; Romero, Octavio A.; Kohno, Takashi Human Mutation, Vol. 29, Issue 5 https://doi.org/10.1002/humu.20730	journal	April 2008
A detailed study of the phenotype of an autosomal dominant cone-rod dystrophy (CORD7) associated with mutation in the gene for RIM1 Michaelides, M. British Journal of Ophthalmology, Vol. 89, Issue 2 https://doi.org/10.1136/bjo.2004.050773	journal	February 2005
Notch1 is required in newly postmitotic cells to inhibit the rod photoreceptor fate Mizeracka, Karolina; DeMaso, Christina R.; Cepko, Constance L. Development, Vol. 140, Issue 15 https://doi.org/10.1242/dev.090696	journal	August 2013
Analysis of gene expression in wild‐type and Notch1 mutant retinal cells by single cell profiling Mizeracka, Karolina; Trimarchi, Jeffrey M.; Stadler, Michael B. Developmental Dynamics, Vol. 242, Issue 10 https://doi.org/10.1002/dvdy.24006	journal	September 2013
PHD1 Links Cell-Cycle Progression to Oxygen Sensing through Hydroxylation of the Centrosomal Protein Cep192 Moser, Sandra C.; Bensaddek, Dalila; Ortmann, Brian Developmental Cell, Vol. 26, Issue 4 https://doi.org/10.1016/j.devcel.2013.06.014	journal	August 2013
E2Fs regulate the expression of genes involved in differentiation, development, proliferation, and apoptosis Muller, H. Genes & Development, Vol. 15, Issue 3 https://doi.org/10.1101/gad.864201	journal	February 2001
Protein phosphatase 2A associates with and regulates atypical PKC and the epithelial tight junction complex Nunbhakdi-Craig, Viyada; Machleidt, Thomas; Ogris, Egon Journal of Cell Biology, Vol. 158, Issue 5 https://doi.org/10.1083/jcb.200206114	journal	August 2002
Validation of oligoarrays for quantitative exploration of the transcriptome Nygaard, Vigdis; Liu, Fang; Holden, Marit BMC Genomics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2164-9-258	journal	January 2008
The Genetic Landscape of the Childhood Cancer Medulloblastoma Parsons, D. W.; Li, M.; Zhang, X. Science, Vol. 331, Issue 6016 https://doi.org/10.1126/science.1198056	journal	December 2010
Progression of neuronal and synaptic remodeling in the rd10 mouse model of retinitis pigmentosa Phillips, M. Joseph; Otteson, Deborah C.; Sherry, David M. The Journal of Comparative Neurology, Vol. 518, Issue 11 https://doi.org/10.1002/cne.22322	journal	June 2010
Opitz G/BBB syndrome, a defect of midline development, is due to mutations in a new RING finger gene on Xp22 Quaderi, Nandita A.; Schweiger, Susann; Gaudenz, Karin Nature Genetics, Vol. 17, Issue 3 https://doi.org/10.1038/ng1197-285	journal	November 1997
The SWI/SNF complex and cancer Reisman, D.; Glaros, S.; Thompson, E. A. Oncogene, Vol. 28, Issue 14 https://doi.org/10.1038/onc.2009.4	journal	February 2009
E2F integrates cell cycle progression with DNA repair, replication, and G2/M checkpoints Ren, B. Genes & Development, Vol. 16, Issue 2 https://doi.org/10.1101/gad.949802	journal	January 2002
Novel mutations target distinct subgroups of medulloblastoma Robinson, Giles; Parker, Matthew; Kranenburg, Tanya A. Nature, Vol. 488, Issue 7409 https://doi.org/10.1038/nature11213	journal	June 2012
Massive parallel DNA pyrosequencing analysis of the tumor suppressor BRG1/SMARCA4 in lung primary tumors Rodriguez-Nieto, Salvador; Cañada, Andres; Pros, Eva Human Mutation, Vol. 32, Issue 2 https://doi.org/10.1002/humu.21415	journal	December 2010
The transcriptome of retinal Müller glial cells Roesch, Karin; Jadhav, Ashutosh P.; Trimarchi, Jeffrey M. The Journal of Comparative Neurology, Vol. 509, Issue 2 https://doi.org/10.1002/cne.21730	journal	July 2008
Genetic analysis of the homeodomain transcription factor Chx10 in the retina using a novel multifunctional BAC transgenic mouse reporter Rowan, Sheldon; Cepko, Constance L. Developmental Biology, Vol. 271, Issue 2 https://doi.org/10.1016/j.ydbio.2004.03.039	journal	July 2004
The Natural History of Retinal Degeneration in Association with Cobalamin C (cbl C) Disease Schimel, Andrew M.; Mets, Marilyn Baird Ophthalmic Genetics, Vol. 27, Issue 1 https://doi.org/10.1080/13816810500481758	journal	January 2006
Convergent structural alterations define SWItch/Sucrose NonFermentable (SWI/SNF) chromatin remodeler as a central tumor suppressive complex in pancreatic cancer Shain, A. H.; Giacomini, C. P.; Matsukuma, K. Proceedings of the National Academy of Sciences, Vol. 109, Issue 5 https://doi.org/10.1073/pnas.1114817109	journal	January 2012
Human Cep192 and Cep152 cooperate in Plk4 recruitment and centriole duplication Sonnen, K. F.; Gabryjonczyk, A. -M.; Anselm, E. Journal of Cell Science, Vol. 126, Issue 14 https://doi.org/10.1242/jcs.129502	journal	May 2013
An E2F Binding-Deficient Rb1 Protein Partially Rescues Developmental Defects Associated with Rb1 Nullizygosity Sun, Huifang; Chang, Yanjie; Schweers, Brett Molecular and Cellular Biology, Vol. 26, Issue 4 https://doi.org/10.1128/MCB.26.4.1527-1537.2006	journal	February 2006
Nectin and afadin: novel organizers of intercellular junctions Takai, Y. Journal of Cell Science, Vol. 116, Issue 1 https://doi.org/10.1242/jcs.00167	journal	January 2003
Nectins and nectin-like molecules: Roles in cell adhesion, migration, and polarization Takai, Yoshimi; Irie, Kenji; Shimizu, Kazuya Cancer Science, Vol. 94, Issue 8 https://doi.org/10.1111/j.1349-7006.2003.tb01499.x	journal	August 2003
The roles of cadherins and nectins in interneuronal synapse formation Takai, Y. Current Opinion in Neurobiology, Vol. 13, Issue 5 https://doi.org/10.1016/j.conb.2003.09.003	journal	October 2003
Molecular heterogeneity of developing retinal ganglion and amacrine cells revealed through single cell gene expression profiling Trimarchi, Jeffrey M.; Stadler, Michael B.; Roska, Botond The Journal of Comparative Neurology, Vol. 502, Issue 6 https://doi.org/10.1002/cne.21368	journal	June 2007
Individual Retinal Progenitor Cells Display Extensive Heterogeneity of Gene Expression Trimarchi, Jeffrey M.; Stadler, Michael B.; Cepko, Constance L. PLoS ONE, Vol. 3, Issue 2 https://doi.org/10.1371/journal.pone.0001588	journal	February 2008
Identification of genes expressed preferentially in the developing peripheral margin of the optic cup Trimarchi, Jeffrey M.; Cho, Seo-Hee; Cepko, Constance L. Developmental Dynamics, Vol. 238, Issue 9 https://doi.org/10.1002/dvdy.21973	journal	September 2009
Differential distribution and developmental expression of synaptic vesicle protein 2 isoforms in the mouse retina Wang, Meng M.; Janz, Roger; Belizaire, Roger The Journal of Comparative Neurology, Vol. 460, Issue 1 https://doi.org/10.1002/cne.10636	journal	May 2003
The identification of E2F1-specific target genes Wells, Julie; Graveel, Carrie R.; Bartley, Stephanie M. Proceedings of the National Academy of Sciences, Vol. 99, Issue 6 https://doi.org/10.1073/pnas.062047499	journal	March 2002
Epigenetic regulation of gene expression by Drosophila Myb and E2F2-RBF via the Myb-MuvB/dREAM complex Wen, H.; Andrejka, L.; Ashton, J. Genes & Development, Vol. 22, Issue 5 https://doi.org/10.1101/gad.1626308	journal	March 2008
Rb regulates proliferation and rod photoreceptor development in the mouse retina Zhang, Jiakun; Gray, Jonathan; Wu, Lizhao Nature Genetics, Vol. 36, Issue 4 https://doi.org/10.1038/ng1318	journal	February 2004
A novel retinoblastoma therapy from genomic and epigenetic analyses Zhang, Jinghui; Benavente, Claudia A.; McEvoy, Justina Nature, Vol. 481, Issue 7381 https://doi.org/10.1038/nature10733	journal	January 2012
Molecular basis of LMAN1 in coordinating LMAN1-MCFD2 cargo receptor formation and ER-to-Golgi transport of FV/FVIII Zheng, Chunlei; Liu, Hui-hui; Yuan, Shuguang Blood, Vol. 116, Issue 25 https://doi.org/10.1182/blood-2010-04-278325	journal	December 2010
Structural Characterization of Carbohydrate Binding by LMAN1 Protein Provides New Insight into the Endoplasmic Reticulum Export of Factors V (FV) and VIII (FVIII) Zheng, Chunlei; Page, Richard C.; Das, Vaijayanti Journal of Biological Chemistry, Vol. 288, Issue 28 https://doi.org/10.1074/jbc.M113.461434	journal	July 2013
Role of each immunoglobulin-like loop of nectin for its cell–cell adhesion activity Yasumi, Masato; Shimizu, Kazuya; Honda, Tomoyuki Biochemical and Biophysical Research Communications, Vol. 302, Issue 1 https://doi.org/10.1016/s0006-291x(03)00106-2	journal	February 2003
A Brg1 Null Mutation in the Mouse Reveals Functional Differences among Mammalian SWI/SNF Complexes Bultman, Scott; Gebuhr, Tom; Yee, Della Molecular Cell, Vol. 6, Issue 6 https://doi.org/10.1016/s1097-2765(00)00127-1	journal	December 2000
Emerging roles for E2F: Beyond the G1/S transition and DNA replication Cam, Hugh; Dynlacht, Brian David Cancer Cell, Vol. 3, Issue 4 https://doi.org/10.1016/s1535-6108(03)00080-1	journal	April 2003
A mammalian microRNA cluster controls DNA methylation and telomere recombination via Rbl2-dependent regulation of DNA methyltransferases Benetti, Roberta; Gonzalo, Susana; Jaco, Isabel Nature Structural & Molecular Biology, Vol. 15, Issue 3 https://doi.org/10.1038/nsmb.1399	journal	March 2008
Impaired cell fate through gain-of-function mutations in a chromatin reader Wan, Liling; Chong, Shasha; Xuan, Fan Nature, Vol. 577, Issue 7788 https://doi.org/10.1038/s41586-019-1842-7	journal	December 2019
SEER and Gene Expression Data Analysis Deciphers Racial Disparity Patterns in Prostate Cancer Mortality and the Public Health Implication Zhang, Wensheng; Dong, Yan; Sartor, Oliver Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-63764-4	journal	April 2020
Implications of Nectin-like Molecule-2/IGSF4/RA175/SgIGSF/TSLC1/SynCAM1 in Cell-Cell Adhesion and Transmembrane Protein Localization in Epithelial Cells Shingai, Tatsushi; Ikeda, Wataru; Kakunaga, Shigeki Journal of Biological Chemistry, Vol. 278, Issue 37 https://doi.org/10.1074/jbc.m305387200	journal	September 2003
BRG1-Mediated Chromatin Remodeling Regulates Differentiation and Gene Expression of T Helper Cells Wurster, Andrea L.; Pazin, Michael J. Molecular and Cellular Biology, Vol. 28, Issue 24 https://doi.org/10.1128/mcb.00835-08	journal	December 2008
Residual Complexes Containing SMARCA2 (BRM) Underlie the Oncogenic Drive of SMARCA4 ( BRG1 ) Mutation Wilson, Boris G.; Helming, Katherine C.; Wang, Xiaofeng Molecular and Cellular Biology, Vol. 34, Issue 6 https://doi.org/10.1128/mcb.01372-13	journal	March 2014
Role for E2F in Control of Both DNA Replication and Mitotic Functions as Revealed from DNA Microarray Analysis Ishida, S.; Huang, E.; Zuzan, H. Molecular and Cellular Biology, Vol. 21, Issue 14 https://doi.org/10.1128/mcb.21.14.4684-4699.2001	journal	July 2001
Use of Chromatin Immunoprecipitation To Clone Novel E2F Target Promoters Weinmann, Amy S.; Bartley, Stephanie M.; Zhang, Theresa Molecular and Cellular Biology, Vol. 21, Issue 20 https://doi.org/10.1128/mcb.21.20.6820-6832.2001	journal	October 2001
Neuronal Differentiation and Synaptogenesis in Retinoblastoma Johnson, Dianna A.; Zhang, Jiakun; Frase, Sharon Cancer Research, Vol. 67, Issue 6 https://doi.org/10.1158/0008-5472.can-06-3754	journal	March 2007
Targeted Knockout of BRG1 Potentiates Lung Cancer Development Glaros, Selina; Cirrincione, Georgina M.; Palanca, Ariel Cancer Research, Vol. 68, Issue 10 https://doi.org/10.1158/0008-5472.can-07-6652	journal	May 2008

Cited By (6)

Inhibition of EZH2 induces NK cell-mediated differentiation and death in muscle-invasive bladder cancer Ramakrishnan, Swathi; Granger, Victoria; Rak, Monika Cell Death & Differentiation, Vol. 26, Issue 10 https://doi.org/10.1038/s41418-019-0278-9	journal	January 2019
Epigenetic regulation of human retinoblastoma Singh, Usha; Malik, Manzoor Ahmad; Goswami, Sandeep Tumor Biology, Vol. 37, Issue 11 https://doi.org/10.1007/s13277-016-5308-3	journal	September 2016
Differential Expression of Sox11 and Bdnf mRNA Isoforms in the Injured and Regenerating Nervous Systems Struebing, Felix L.; Wang, Jiaxing; Li, Ying Frontiers in Molecular Neuroscience, Vol. 10 https://doi.org/10.3389/fnmol.2017.00354	journal	November 2017
Loss of BRG1 induces CRC cell senescence by regulating p53/p21 pathway Wang, Guihua; Fu, Yinjia; Hu, Fuqing Cell Death & Disease, Vol. 8, Issue 2 https://doi.org/10.1038/cddis.2017.1	journal	February 2017
Structural changes of the macula and optic nerve head in the remaining eyes after enucleation for retinoblastoma: an optical coherence tomography study Said, Azza Mohamed Ahmed; Elbayomi, Ahmed Mohamed; Shaat, Ashraf Abdelsalam Kandeel BMC Ophthalmology, Vol. 17, Issue 1 https://doi.org/10.1186/s12886-017-0650-9	journal	December 2017
Brg1 chromatin remodeling ATPase balances germ layer patterning by amplifying the transcriptional burst at midblastula transition Wagner, Gabriele; Singhal, Nishant; Nicetto, Dario PLOS Genetics, Vol. 13, Issue 5 https://doi.org/10.1371/journal.pgen.1006757	journal	May 2017

Similar Records

Roles of miR-204 in retinal development and maintenance

Journal Article · Wed Sep 15 00:00:00 EDT 2021 · Experimental Cell Research · OSTI ID:1378673

Bereimipour, Ahmad; Najafi, Hadi; Mirsane, Elahe Sadat; +2 more

Hepatocyte-specific deletion of Brg1 alleviates methionine-and-choline-deficient diet (MCD) induced non-alcoholic steatohepatitis in mice

Journal Article · Sat Sep 15 00:00:00 EDT 2018 · Biochemical and Biophysical Research Communications · OSTI ID:1378673

Kong, Ming; Chen, Xuyang; Xu, Huihui; +3 more

Brg1 modulates enhancer activation in mesoderm lineage commitment

Journal Article · Thu Mar 26 00:00:00 EDT 2015 · Development (Cambridge) · OSTI ID:1378673

Alexander, Jeffrey M.; Hota, Swetansu K.; He, Daniel; +4 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
SWI/SNF
epigenetics
retina development
retinoblastoma
mouse

Title: Brg1 coordinates multiple processes during retinogenesis and is a tumor suppressor in retinoblastoma

Citation Formats

References (99)

Cited By (6)

Similar Records

Related Subjects