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Title: 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:
 [1];  [2];  [3];  [1];  [3];  [1];  [3];  [4];  [5];  [5];  [6]
  1. St. Jude's Children's Research Hospital, Memphis, TN (United States). Dept. of Developmental Neurobiology
  2. Tokyo Medical and Dental Univ. (Japan). Center for Brain Integration Research
  3. St. Jude's Research Hospital, Memphis, TN (United States). Dept. of Computational Biology
  4. Univ. of Tennessee, Memphis, TN (United States). Health Science Center
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Genomics Division; USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. 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}
}

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Baf60c is a component of the neural progenitor-specific BAF complex in developing retina
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journal, September 2009

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Analysis of gene expression in wild‐type and Notch1 mutant retinal cells by single cell profiling
journal, September 2013

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journal, April 2008

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Massive parallel DNA pyrosequencing analysis of the tumor suppressor BRG1/SMARCA4 in lung primary tumors
journal, December 2010

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The cell adhesion gene PVRL3 is associated with congenital ocular defects
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The retinoblastoma protein and BRG1 form a complex and cooperate to induce cell cycle arrest
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Coexpression of Normally Incompatible Developmental Pathways in Retinoblastoma Genesis
journal, August 2011


Differentiated Horizontal Interneurons Clonally Expand to Form Metastatic Retinoblastoma in Mice
journal, October 2007


A Landscape of Driver Mutations in Melanoma
journal, July 2012


The roles of cadherins and nectins in interneuronal synapse formation
journal, October 2003


PHD1 Links Cell-Cycle Progression to Oxygen Sensing through Hydroxylation of the Centrosomal Protein Cep192
journal, August 2013


Centrosomes Tune in to Metabolic State and Turn on to Oxygen
journal, August 2013


The extracellular matrix component WIF-1 is expressed during, and can modulate, retinal development
journal, December 2004

  • Hunter, Dale D.; Zhang, Minlei; Ferguson, Jill W.
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Regulation of PP2A activity by Mid1 controls cranial neural crest speed and gangliogenesis
journal, January 2012


The Cep192-Organized Aurora A-Plk1 Cascade Is Essential for Centrosome Cycle and Bipolar Spindle Assembly
journal, August 2014


Developmental defects in Rb-deficient retinae
journal, December 2004


Brg1 is required for murine neural stem cell maintenance and gliogenesis
journal, January 2006


β-catenin is essential for lamination but not neurogenesis in mouse retinal development
journal, November 2006


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journal, October 1986

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  • Nature, Vol. 323, Issue 6089
  • DOI: 10.1038/323643a0

Vertebrate neural cell-fate determination: Lessons from the retina
journal, February 2001

  • Livesey, F. J.; Cepko, C. L.
  • Nature Reviews Neuroscience, Vol. 2, Issue 2
  • DOI: 10.1038/35053522

Regulating proliferation during retinal development
journal, May 2001

  • Dyer, Michael A.; Cepko, Constance L.
  • Nature Reviews Neuroscience, Vol. 2, Issue 5
  • DOI: 10.1038/35072555

ATP-dependent chromatin remodeling: genetics, genomics and mechanisms
journal, March 2011

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Chromatin regulation by Brg1 underlies heart muscle development and disease
journal, July 2010


A novel retinoblastoma therapy from genomic and epigenetic analyses
journal, January 2012

  • Zhang, Jinghui; Benavente, Claudia A.; McEvoy, Justina
  • Nature, Vol. 481, Issue 7381
  • DOI: 10.1038/nature10733

Mutations in ABCD4 cause a new inborn error of vitamin B12 metabolism
journal, August 2012

  • Coelho, David; Kim, Jaeseung C.; Miousse, Isabelle R.
  • Nature Genetics, Vol. 44, Issue 10
  • DOI: 10.1038/ng.2386

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