DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Representing Kidney Development Using the Gene Ontology

Abstract

Gene Ontology (GO) provides dynamic controlled vocabularies to aid in the description of the functional biological attributes and subcellular locations of gene products from all taxonomic groups (www.geneontology.org). Here we describe collaboration between the renal biomedical research community and the GO Consortium to improve the quality and quantity of GO terms describing renal development. In the associated annotation activity, the new and revised terms were associated with gene products involved in renal development and function. This project resulted in a total of 522 GO terms being added to the ontology and the creation of approximately 9,600 kidney-related GO term associations to 940 UniProt Knowledgebase (UniProtKB) entries, covering 66 taxonomic groups. We demonstrate the impact of these improvements on the interpretation of GO term analyses performed on genes differentially expressed in kidney glomeruli affected by diabetic nephropathy. In summary, we have produced a resource that can be utilized in the interpretation of data from small- and large-scale experiments investigating molecular mechanisms of kidney function and development and thereby help towards alleviating renal disease.

Authors:
 [1];  [2];  [1];  [3];  [1];  [4];  [4];  [5];  [6];  [7];  [8];  [2];  [9];  [1];  [1];  [1]
  1. Wellcome Trust Genome Campus, Cambridge (United Kingdom). European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI)
  2. The Jackson Lab., Bar Harbor, ME (United States)
  3. Univ. of Cambridge (United Kingdom). Cambridge Systems Biology Centre. Dept. of Biochemistry
  4. Univ. of Cambridge (United Kingdom). Dept. of Genetics. FlyBase
  5. Univ. of Oregon, Eugene, OR (United States). The Zebrafish Model Organism Database (ZFIN)
  6. Univ. Paris-Sud, Orsay (France). Centre National de la Recherche Scientifique (CNRS). IR4M UMR8081
  7. Western General Hospital, Edinburgh (United Kingdom). Inst. of Genetics and Molecular Medicine. MRC Human Genetics Unit
  8. Univ. of Manchester (United Kingdom). Faculty of Medical and Human Sciences. Inst. of Human Development
  9. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Genomics Division
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
OSTI Identifier:
1627704
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 9; Journal Issue: 6; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Science & Technology - Other Topics

Citation Formats

Alam-Faruque, Yasmin, Hill, David P., Dimmer, Emily C., Harris, Midori A., Foulger, Rebecca E., Tweedie, Susan, Attrill, Helen, Howe, Douglas G., Thomas, Stephen Randall, Davidson, Duncan, Woolf, Adrian S., Blake, Judith A., Mungall, Christopher J., O’Donovan, Claire, Apweiler, Rolf, and Huntley, Rachael P. Representing Kidney Development Using the Gene Ontology. United States: N. p., 2014. Web. doi:10.1371/journal.pone.0099864.
Alam-Faruque, Yasmin, Hill, David P., Dimmer, Emily C., Harris, Midori A., Foulger, Rebecca E., Tweedie, Susan, Attrill, Helen, Howe, Douglas G., Thomas, Stephen Randall, Davidson, Duncan, Woolf, Adrian S., Blake, Judith A., Mungall, Christopher J., O’Donovan, Claire, Apweiler, Rolf, & Huntley, Rachael P. Representing Kidney Development Using the Gene Ontology. United States. https://doi.org/10.1371/journal.pone.0099864
Alam-Faruque, Yasmin, Hill, David P., Dimmer, Emily C., Harris, Midori A., Foulger, Rebecca E., Tweedie, Susan, Attrill, Helen, Howe, Douglas G., Thomas, Stephen Randall, Davidson, Duncan, Woolf, Adrian S., Blake, Judith A., Mungall, Christopher J., O’Donovan, Claire, Apweiler, Rolf, and Huntley, Rachael P. Wed . "Representing Kidney Development Using the Gene Ontology". United States. https://doi.org/10.1371/journal.pone.0099864. https://www.osti.gov/servlets/purl/1627704.
@article{osti_1627704,
title = {Representing Kidney Development Using the Gene Ontology},
author = {Alam-Faruque, Yasmin and Hill, David P. and Dimmer, Emily C. and Harris, Midori A. and Foulger, Rebecca E. and Tweedie, Susan and Attrill, Helen and Howe, Douglas G. and Thomas, Stephen Randall and Davidson, Duncan and Woolf, Adrian S. and Blake, Judith A. and Mungall, Christopher J. and O’Donovan, Claire and Apweiler, Rolf and Huntley, Rachael P.},
abstractNote = {Gene Ontology (GO) provides dynamic controlled vocabularies to aid in the description of the functional biological attributes and subcellular locations of gene products from all taxonomic groups (www.geneontology.org). Here we describe collaboration between the renal biomedical research community and the GO Consortium to improve the quality and quantity of GO terms describing renal development. In the associated annotation activity, the new and revised terms were associated with gene products involved in renal development and function. This project resulted in a total of 522 GO terms being added to the ontology and the creation of approximately 9,600 kidney-related GO term associations to 940 UniProt Knowledgebase (UniProtKB) entries, covering 66 taxonomic groups. We demonstrate the impact of these improvements on the interpretation of GO term analyses performed on genes differentially expressed in kidney glomeruli affected by diabetic nephropathy. In summary, we have produced a resource that can be utilized in the interpretation of data from small- and large-scale experiments investigating molecular mechanisms of kidney function and development and thereby help towards alleviating renal disease.},
doi = {10.1371/journal.pone.0099864},
journal = {PLoS ONE},
number = 6,
volume = 9,
place = {United States},
year = {Wed Jun 18 00:00:00 EDT 2014},
month = {Wed Jun 18 00:00:00 EDT 2014}
}

Works referenced in this record:

Genome-wide gene expression profiling reveals renal genes regulated during metabolic acidosis
journal, February 2008


Gene expression profiling analysis in nephrology: towards molecular definition of renal disease
journal, June 2006

  • Yasuda, Yoshinari; Cohen, Clemens D.; Henger, Anna
  • Clinical and Experimental Nephrology, Vol. 10, Issue 2
  • DOI: 10.1007/s10157-006-0421-z

Atlas of Gene Expression in the Developing Kidney at Microanatomic Resolution
journal, November 2008


Differential Protein Expressions in Renal Cell Carcinoma: New Biomarker Discovery by Mass Spectrometry
journal, August 2009

  • Siu, K. W. Michael; DeSouza, Leroi V.; Scorilas, Andreas
  • Journal of Proteome Research, Vol. 8, Issue 8
  • DOI: 10.1021/pr800389e

Diabetes-induced changes in the renal cortical proteome assessed with two-dimensional gel electrophoresis and mass spectrometry
journal, May 2007

  • Tilton, Ronald G.; Haidacher, Sigmund J.; LeJeune, Wanda S.
  • PROTEOMICS, Vol. 7, Issue 10
  • DOI: 10.1002/pmic.200700017

Proteomics in renal research
journal, February 2007

  • Janech, Michael G.; Raymond, John R.; Arthur, John M.
  • American Journal of Physiology-Renal Physiology, Vol. 292, Issue 2
  • DOI: 10.1152/ajprenal.00298.2006

Proteomic Analysis of Cellular Response to Osmotic Stress in Thick Ascending Limb of Henle’s Loop (TALH) Cells
journal, October 2005

  • Dihazi, Hassan; Asif, Abdul R.; Agarwal, Nitin K.
  • Molecular & Cellular Proteomics, Vol. 4, Issue 10
  • DOI: 10.1074/mcp.M400184-MCP200

The GUDMAP database - an online resource for genitourinary research
journal, June 2011

  • Harding, S. D.; Armit, C.; Armstrong, J.
  • Development, Vol. 138, Issue 13
  • DOI: 10.1242/dev.063594

Drosophila provides rapid modeling of renal development, function, and disease
journal, December 2010

  • Dow, Julian A. T.; Romero, Michael F.
  • American Journal of Physiology-Renal Physiology, Vol. 299, Issue 6
  • DOI: 10.1152/ajprenal.00521.2010

A standard nomenclature for structures of the kidney
journal, January 1988

  • Schafer, James A.; Andreoli, Thomas E.; Thurau, Klaus
  • Kidney International, Vol. 33, Issue 1, p. 1-7
  • DOI: 10.1038/ki.1988.1

A high-resolution anatomical ontology of the developing murine genitourinary tract
journal, June 2007


The Renal Gene Ontology Annotation Initiative
journal, April 2010

  • Alam-Faruque, Yasmin; Dimmer, Emily C.; Huntley, Rachael P.
  • Organogenesis, Vol. 6, Issue 2
  • DOI: 10.4161/org.6.2.11294

Logical Development of the Cell Ontology
journal, January 2011

  • Meehan, Terrence F.; Masci, Anna Maria; Abdulla, Amina
  • BMC Bioinformatics, Vol. 12, Issue 1
  • DOI: 10.1186/1471-2105-12-6

Uberon, an integrative multi-species anatomy ontology
journal, January 2012

  • Mungall, Christopher J.; Torniai, Carlo; Gkoutos, Georgios V.
  • Genome Biology, Vol. 13, Issue 1
  • DOI: 10.1186/gb-2012-13-1-r5

Cross-product extensions of the Gene Ontology
journal, February 2011

  • Mungall, Christopher J.; Bada, Michael; Berardini, Tanya Z.
  • Journal of Biomedical Informatics, Vol. 44, Issue 1
  • DOI: 10.1016/j.jbi.2010.02.002

A MOD(ern) perspective on literature curation
journal, March 2010

  • Hirschman, Jodi; Berardini, Tanya Z.; Drabkin, Harold J.
  • Molecular Genetics and Genomics, Vol. 283, Issue 5
  • DOI: 10.1007/s00438-010-0525-8

A guide to best practices for Gene Ontology (GO) manual annotation
journal, January 2013


Analysis Tool Web Services from the EMBL-EBI
journal, May 2013

  • McWilliam, Hamish; Li, Weizhong; Uludag, Mahmut
  • Nucleic Acids Research, Vol. 41, Issue W1
  • DOI: 10.1093/nar/gkt376

EnsemblCompara GeneTrees: Complete, duplication-aware phylogenetic trees in vertebrates
journal, December 2008

  • Vilella, A. J.; Severin, J.; Ureta-Vidal, A.
  • Genome Research, Vol. 19, Issue 2
  • DOI: 10.1101/gr.073585.107

The Mouse Genome Database: integration of and access to knowledge about the laboratory mouse
journal, November 2013

  • Blake, Judith A.; Bult, Carol J.; Eppig, Janan T.
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1225

FlyBase 102—advanced approaches to interrogating FlyBase
journal, November 2013

  • St. Pierre, Susan E.; Ponting, Laura; Stefancsik, Raymund
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1092

ZFIN, the Zebrafish Model Organism Database: increased support for mutants and transgenics
journal, October 2012

  • Howe, Douglas G.; Bradford, Yvonne M.; Conlin, Tom
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks938

MAPPFinder: using Gene Ontology and GenMAPP to create a global gene-expression profile from microarray data
journal, January 2003

  • Doniger, Scott W.; Salomonis, Nathan; Dahlquist, Kam D.
  • Genome Biology, Vol. 4, Issue 1, p. R7
  • DOI: 10.1186/gb-2003-4-1-r7

GO-Elite: a flexible solution for pathway and ontology over-representation
journal, June 2012


Ontologizer 2.0--a multifunctional tool for GO term enrichment analysis and data exploration
journal, May 2008


Gene expression profiling in glomeruli from human kidneys with diabetic nephropathy
journal, April 2004

  • Baelde, Hans J.; Eikmans, Michael; Doran, Peter P.
  • American Journal of Kidney Diseases, Vol. 43, Issue 4
  • DOI: 10.1053/j.ajkd.2003.12.028

The representation of heart development in the gene ontology
journal, June 2011


Muscle Research and Gene Ontology: New standards for improved data integration
journal, January 2009

  • Feltrin, Erika; Campanaro, Stefano; Diehl, Alexander D.
  • BMC Medical Genomics, Vol. 2, Issue 1
  • DOI: 10.1186/1755-8794-2-6

Organization of the pronephric kidney revealed by large-scale gene expression mapping
journal, January 2008


Odd-skipped genes encode repressors that control kidney development
journal, January 2007


Pax2 and Pax8 Regulate Branching Morphogenesis and Nephron Differentiation in the Developing Kidney
journal, February 2007

  • Narlis, Melina; Grote, David; Gaitan, Yaned
  • Journal of the American Society of Nephrology, Vol. 18, Issue 4
  • DOI: 10.1681/ASN.2006070739

PAX2 mutations in oligomeganephronia
journal, February 2001


Synergism between Pax-8 and lim-1 in Embryonic Kidney Development
journal, October 1999


Suppression of Ureteric Bud Apoptosis Rescues Nephron Endowment and Adult Renal Function in Pax2 Mutant Mice
journal, May 2006

  • Dziarmaga, Alison; Eccles, Michael; Goodyer, Paul
  • Journal of the American Society of Nephrology, Vol. 17, Issue 6
  • DOI: 10.1681/ASN.2005101074

A dual requirement for Iroquois genes during Xenopus kidney development
journal, August 2008

  • Alarcon, P.; Rodriguez-Seguel, E.; Fernandez-Gonzalez, A.
  • Development, Vol. 135, Issue 19
  • DOI: 10.1242/dev.023697

The prepattern transcription factor Irx3 directs nephron segment identity
journal, September 2007

  • Reggiani, L.; Raciti, D.; Airik, R.
  • Genes & Development, Vol. 21, Issue 18
  • DOI: 10.1101/gad.450707

Apoptosis in the kidneys of patients with type II diabetic nephropathy
journal, November 2007

  • Verzola, D.; Gandolfo, M. T.; Ferrario, F.
  • Kidney International, Vol. 72, Issue 10
  • DOI: 10.1038/sj.ki.5002531

Targeted Glomerular Angiopoietin-1 Therapy for Early Diabetic Kidney Disease
journal, September 2013

  • Dessapt-Baradez, Cecile; Woolf, Adrian S.; White, Kathryn E.
  • Journal of the American Society of Nephrology, Vol. 25, Issue 1
  • DOI: 10.1681/ASN.2012121218

The Impact of Focused Gene Ontology Curation of Specific Mammalian Systems
journal, December 2011


Insulin Signaling to the Glomerular Podocyte Is Critical for Normal Kidney Function
journal, October 2010


Nitric oxide deficiency in chronic kidney disease
journal, January 2008


Diabetic Endothelial Nitric Oxide Synthase Knockout Mice Develop Advanced Diabetic Nephropathy
journal, January 2007

  • Nakagawa, Takahiko; Sato, Waichi; Glushakova, Olena
  • Journal of the American Society of Nephrology, Vol. 18, Issue 2
  • DOI: 10.1681/ASN.2006050459

Ontological analysis of gene expression data: current tools, limitations, and open problems
journal, June 2005


Synergism between Pax-8 and lim-1 in Embryonic Kidney Development
journal, October 1999


A MOD(ern) perspective on literature curation
journal, March 2010

  • Hirschman, Jodi; Berardini, Tanya Z.; Drabkin, Harold J.
  • Molecular Genetics and Genomics, Vol. 283, Issue 5
  • DOI: 10.1007/s00438-010-0525-8

Gene expression profiling analysis in nephrology: towards molecular definition of renal disease
journal, June 2006

  • Yasuda, Yoshinari; Cohen, Clemens D.; Henger, Anna
  • Clinical and Experimental Nephrology, Vol. 10, Issue 2
  • DOI: 10.1007/s10157-006-0421-z

An IRKO in the Podo: Impaired Insulin Signaling in Podocytes and the Pathogenesis of Diabetic Nephropathy
journal, October 2010


The role of TGF-β and epithelial-to mesenchymal transition in diabetic nephropathy
journal, July 2011


Atlas of Gene Expression in the Developing Kidney at Microanatomic Resolution
journal, November 2008


Cross-product extensions of the Gene Ontology
journal, February 2011

  • Mungall, Christopher J.; Bada, Michael; Berardini, Tanya Z.
  • Journal of Biomedical Informatics, Vol. 44, Issue 1
  • DOI: 10.1016/j.jbi.2010.02.002

A high-resolution anatomical ontology of the developing murine genitourinary tract
journal, June 2007


Odd-skipped genes encode repressors that control kidney development
journal, January 2007


Pax2 and Pax8 regulate branching morphogenesis and nephron differentiation in the developing kidney
journal, June 2007


The representation of heart development in the gene ontology
journal, June 2011


Differential Protein Expressions in Renal Cell Carcinoma: New Biomarker Discovery by Mass Spectrometry
journal, August 2009

  • Siu, K. W. Michael; DeSouza, Leroi V.; Scorilas, Andreas
  • Journal of Proteome Research, Vol. 8, Issue 8
  • DOI: 10.1021/pr800389e

Evidence of apoptosis in human diabetic kidney
journal, April 2004


Apoptosis in the kidneys of patients with type II diabetic nephropathy
journal, November 2007

  • Verzola, D.; Gandolfo, M. T.; Ferrario, F.
  • Kidney International, Vol. 72, Issue 10
  • DOI: 10.1038/sj.ki.5002531

PAX2 mutations in oligomeganephronia
journal, February 2001


Gene expression profiling in glomeruli from human kidneys with diabetic nephropathy
journal, April 2004

  • Baelde, Hans J.; Eikmans, Michael; Doran, Peter P.
  • American Journal of Kidney Diseases, Vol. 43, Issue 4
  • DOI: 10.1053/j.ajkd.2003.12.028

Ontologizer 2.0--a multifunctional tool for GO term enrichment analysis and data exploration
journal, May 2008


GO-Elite: a flexible solution for pathway and ontology over-representation
journal, June 2012


A guide to best practices for Gene Ontology (GO) manual annotation
journal, January 2013


ZFIN, the Zebrafish Model Organism Database: increased support for mutants and transgenics
journal, October 2012

  • Howe, Douglas G.; Bradford, Yvonne M.; Conlin, Tom
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks938

The Mouse Genome Database: integration of and access to knowledge about the laboratory mouse
journal, November 2013

  • Blake, Judith A.; Bult, Carol J.; Eppig, Janan T.
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1225

Analysis Tool Web Services from the EMBL-EBI
journal, May 2013

  • McWilliam, Hamish; Li, Weizhong; Uludag, Mahmut
  • Nucleic Acids Research, Vol. 41, Issue W1
  • DOI: 10.1093/nar/gkt376

Endothelial Cell Apoptosis during Glomerular Capillary Lumen Formation In Vivo
journal, May 2003


Podocytes, glucose and insulin
journal, January 2010


The prepattern transcription factor Irx3 directs nephron segment identity
journal, September 2007

  • Reggiani, L.; Raciti, D.; Airik, R.
  • Genes & Development, Vol. 21, Issue 18
  • DOI: 10.1101/gad.450707

Proteomics in renal research
journal, February 2007

  • Janech, Michael G.; Raymond, John R.; Arthur, John M.
  • American Journal of Physiology-Renal Physiology, Vol. 292, Issue 2
  • DOI: 10.1152/ajprenal.00298.2006

Nitric oxide deficiency in chronic kidney disease
journal, January 2008


Drosophila provides rapid modeling of renal development, function, and disease
journal, December 2010

  • Dow, Julian A. T.; Romero, Michael F.
  • American Journal of Physiology-Renal Physiology, Vol. 299, Issue 6
  • DOI: 10.1152/ajprenal.00521.2010

Uberon, an integrative multi-species anatomy ontology
journal, January 2012

  • Mungall, Christopher J.; Torniai, Carlo; Gkoutos, Georgios V.
  • Genome Biology, Vol. 13, Issue 1
  • DOI: 10.1186/gb-2012-13-1-r5

A dual requirement for Iroquois genes during Xenopus kidney development
journal, October 2008

  • Alarcón, Pilar; Rodríguez-Seguel, Elisa; Fernández-González, Ana
  • Development, Vol. 135, Issue 20
  • DOI: 10.1242/dev.022053

The GUDMAP database - an online resource for genitourinary research
journal, June 2011

  • Harding, S. D.; Armit, C.; Armstrong, J.
  • Development, Vol. 138, Issue 13
  • DOI: 10.1242/dev.063594

Activation of Tubular Epithelial Cells in Diabetic Nephropathy and the Role of the Peroxisome Proliferator–Activated Receptor-γ Agonist
journal, May 2006

  • Tang, Sydney C. W.; Leung, Joseph C. K.; Chan, Loretta Y. Y.
  • Journal of the American Society of Nephrology, Vol. 17, Issue 6
  • DOI: 10.1681/asn.2005101113

The Vasculature in Diabetic Nephropathy
journal, January 2014

  • Maski, Manish R.; Parikh, Samir M.
  • Journal of the American Society of Nephrology, Vol. 25, Issue 1
  • DOI: 10.1681/asn.2013090966

Muscle Research and Gene Ontology: New standards for improved data integration.
journalarticle, January 2009

  • Feltrin, Erika; Campanaro, Stefano; Diehl, Alexander D.
  • Springer Science and Business Media LLC
  • DOI: 10.17863/cam.33415

The Renal Gene Ontology Annotation Initiative
journal, April 2010

  • Alam-Faruque, Yasmin; Dimmer, Emily C.; Huntley, Rachael P.
  • Organogenesis, Vol. 6, Issue 2
  • DOI: 10.4161/org.6.2.11294

Works referencing / citing this record:

The GOA database: Gene Ontology annotation updates for 2015
journal, November 2014

  • Huntley, Rachael P.; Sawford, Tony; Mutowo-Meullenet, Prudence
  • Nucleic Acids Research, Vol. 43, Issue D1
  • DOI: 10.1093/nar/gku1113

A statistical approach to identify, monitor, and manage incomplete curated data sets
journal, April 2018


The Cell Ontology 2016: enhanced content, modularization, and ontology interoperability
journal, July 2016

  • Diehl, Alexander D.; Meehan, Terrence F.; Bradford, Yvonne M.
  • Journal of Biomedical Semantics, Vol. 7, Issue 1
  • DOI: 10.1186/s13326-016-0088-7

Urinary MicroRNA Profiling Predicts the Development of Microalbuminuria in Patients with Type 1 Diabetes
journal, July 2015

  • Argyropoulos, Christos; Wang, Kai; Bernardo, Jose
  • Journal of Clinical Medicine, Vol. 4, Issue 7
  • DOI: 10.3390/jcm4071498

The GOA database: Gene Ontology annotation updates for 2015
journal, November 2014

  • Huntley, Rachael P.; Sawford, Tony; Mutowo-Meullenet, Prudence
  • Nucleic Acids Research, Vol. 43, Issue D1
  • DOI: 10.1093/nar/gku1113

The Cell Ontology 2016: enhanced content, modularization, and ontology interoperability
journal, July 2016

  • Diehl, Alexander D.; Meehan, Terrence F.; Bradford, Yvonne M.
  • Journal of Biomedical Semantics, Vol. 7, Issue 1
  • DOI: 10.1186/s13326-016-0088-7

Urinary MicroRNA Profiling Predicts the Development of Microalbuminuria in Patients with Type 1 Diabetes
journal, July 2015

  • Argyropoulos, Christos; Wang, Kai; Bernardo, Jose
  • Journal of Clinical Medicine, Vol. 4, Issue 7
  • DOI: 10.3390/jcm4071498