Brg1 coordinates multiple processes during retinogenesis and is a tumor suppressor in retinoblastoma
Abstract
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.
- Authors:
-
- 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)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1378673
- Alternate Identifier(s):
- OSTI ID: 1256950
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Development (Cambridge)
- Additional Journal Information:
- Journal Name: Development (Cambridge); Journal Volume: 142; Journal Issue: 23; Journal ID: ISSN 0950-1991
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; SWI/SNF; epigenetics; retina development; retinoblastoma; mouse
Citation Formats
Aldiri, I., Ajioka, I., Xu, B., Zhang, J., Chen, X., Benavente, C., Finkelstein, D., Johnson, D., Akiyama, J., Pennacchio, L. A., and Dyer, M. A.. Brg1 coordinates multiple processes during retinogenesis and is a tumor suppressor in retinoblastoma. United States: N. p., 2015.
Web. doi:10.1242/dev.124800.
Aldiri, I., Ajioka, I., Xu, B., Zhang, J., Chen, X., Benavente, C., Finkelstein, D., Johnson, D., Akiyama, J., Pennacchio, L. A., & Dyer, M. A.. Brg1 coordinates multiple processes during retinogenesis and is a tumor suppressor in retinoblastoma. United States. https://doi.org/10.1242/dev.124800
Aldiri, I., Ajioka, I., Xu, B., Zhang, J., Chen, X., Benavente, C., Finkelstein, D., Johnson, D., Akiyama, J., Pennacchio, L. A., and Dyer, M. A.. Tue .
"Brg1 coordinates multiple processes during retinogenesis and is a tumor suppressor in retinoblastoma". United States. https://doi.org/10.1242/dev.124800. https://www.osti.gov/servlets/purl/1378673.
@article{osti_1378673,
title = {Brg1 coordinates multiple processes during retinogenesis and is a tumor suppressor in retinoblastoma},
author = {Aldiri, I. and Ajioka, I. and Xu, B. and Zhang, J. and Chen, X. and Benavente, C. and Finkelstein, D. and Johnson, D. and Akiyama, J. and Pennacchio, L. A. and Dyer, M. A.},
abstractNote = {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.},
doi = {10.1242/dev.124800},
journal = {Development (Cambridge)},
number = 23,
volume = 142,
place = {United States},
year = {Tue Dec 01 00:00:00 EST 2015},
month = {Tue Dec 01 00:00:00 EST 2015}
}
Web of Science
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Coexpression of Normally Incompatible Developmental Pathways in Retinoblastoma Genesis
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Differentiated Horizontal Interneurons Clonally Expand to Form Metastatic Retinoblastoma in Mice
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PHD1 Links Cell-Cycle Progression to Oxygen Sensing through Hydroxylation of the Centrosomal Protein Cep192
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Centrosomes Tune in to Metabolic State and Turn on to Oxygen
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PP2A holoenzymes negatively and positively regulate cell cycle progression by dephosphorylating pocket proteins and multiple CDK substrates
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The extracellular matrix component WIF-1 is expressed during, and can modulate, retinal development
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Regulation of PP2A activity by Mid1 controls cranial neural crest speed and gangliogenesis
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The Cep192-Organized Aurora A-Plk1 Cascade Is Essential for Centrosome Cycle and Bipolar Spindle Assembly
journal, August 2014
- Joukov, Vladimir; Walter, Johannes C.; De Nicolo, Arcangela
- Molecular Cell, Vol. 55, Issue 4
Developmental defects in Rb-deficient retinae
journal, December 2004
- Donovan, Stacy L.; Dyer, Michael A.
- Vision Research, Vol. 44, Issue 28
Genetic analysis of the homeodomain transcription factor Chx10 in the retina using a novel multifunctional BAC transgenic mouse reporter
journal, July 2004
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