Modeling Edar expression reveals the hidden dynamics of tooth signaling center patterning

When patterns are set during embryogenesis, it is expected that they are straightly established rather than subsequently modified. The patterning of the three mouse molars is, however, far from straight, likely as a result of mouse evolutionary history. The first-formed tooth signaling centers, call...

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Published inPLoS biology Vol. 17; no. 2; p. e3000064
Main Authors Sadier, Alexa, Twarogowska, Monika, Steklikova, Klara, Hayden, Luke, Lambert, Anne, Schneider, Pascal, Laudet, Vincent, Hovorakova, Maria, Calvez, Vincent, Pantalacci, Sophie
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 07.02.2019
Public Library of Science (PLoS)
Subjects
Activation
Animals
Bernard, Claude (1813-1878)
Biochemistry, Molecular Biology
Biology and Life Sciences
Body Patterning
Cell aggregation
Chemotaxis
Development Biology
Developmental biology
Edar Receptor - genetics
Edar Receptor - metabolism
Embryogenesis
Embryology and Organogenesis
Embryonic growth stage
Epithelium - embryology
Epithelium - metabolism
Funding
Gene expression
Gene Expression Regulation, Developmental
Genetic aspects
Genomics
Hair
Hair - embryology
Insects
Life Sciences
Medicine and Health Sciences
Mice
Mice, Mutant Strains
Models, Biological
Molars
Morphogenesis
Observations
Pattern formation
Patterning
Premolars
Signal Transduction
Signaling
Supervision
Teeth
Tooth - embryology
Tooth - metabolism
Tooth Germ - embryology
Tooth Germ - metabolism
Los Angeles California
Czech Republic
California
France
United States > US
Jaw
Teeth
Molars
Signaling centers
Epithelium
Chemotaxis
Embryos
Embryonic pattern formation
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Abstract When patterns are set during embryogenesis, it is expected that they are straightly established rather than subsequently modified. The patterning of the three mouse molars is, however, far from straight, likely as a result of mouse evolutionary history. The first-formed tooth signaling centers, called MS and R2, disappear before driving tooth formation and are thought to be vestiges of the premolars found in mouse ancestors. Moreover, the mature signaling center of the first molar (M1) is formed from the fusion of two signaling centers (R2 and early M1). Here, we report that broad activation of Edar expression precedes its spatial restriction to tooth signaling centers. This reveals a hidden two-step patterning process for tooth signaling centers, which was modeled with a single activator-inhibitor pair subject to reaction-diffusion (RD). The study of Edar expression also unveiled successive phases of signaling center formation, erasing, recovering, and fusion. Our model, in which R2 signaling center is not intrinsically defective but erased by the broad activation preceding M1 signaling center formation, predicted the surprising rescue of R2 in Edar mutant mice, where activation is reduced. The importance of this R2-M1 interaction was confirmed by ex vivo cultures showing that R2 is capable of forming a tooth. Finally, by introducing chemotaxis as a secondary process to RD, we recapitulated in silico different conditions in which R2 and M1 centers fuse or not. In conclusion, pattern formation in the mouse molar field relies on basic mechanisms whose dynamics produce embryonic patterns that are plastic objects rather than fixed end points.
AbstractList When patterns are set during embryogenesis, it is expected that they are straightly established rather than subsequently modified. The patterning of the three mouse molars is, however, far from straight, likely as a result of mouse evolutionary history. The first-formed tooth signaling centers, called MS and R2, disappear before driving tooth formation and are thought to be vestiges of the premolars found in mouse ancestors. Moreover, the mature signaling center of the first molar (M1) is formed from the fusion of two signaling centers (R2 and early M1). Here, we report that broad activation of Edar expression precedes its spatial restriction to tooth signaling centers. This reveals a hidden two-step patterning process for tooth signaling centers, which was modeled with a single activator-inhibitor pair subject to reaction-diffusion (RD). The study of Edar expression also unveiled successive phases of signaling center formation, erasing, recovering, and fusion. Our model, in which R2 signaling center is not intrinsically defective but erased by the broad activation preceding M1 signaling center formation, predicted the surprising rescue of R2 in Edar mutant mice, where activation is reduced. The importance of this R2-M1 interaction was confirmed by ex vivo cultures showing that R2 is capable of forming a tooth. Finally, by introducing chemotaxis as a secondary process to RD, we recapitulated in silico different conditions in which R2 and M1 centers fuse or not. In conclusion, pattern formation in the mouse molar field relies on basic mechanisms whose dynamics produce embryonic patterns that are plastic objects rather than fixed end points.When patterns are set during embryogenesis, it is expected that they are straightly established rather than subsequently modified. The patterning of the three mouse molars is, however, far from straight, likely as a result of mouse evolutionary history. The first-formed tooth signaling centers, called MS and R2, disappear before driving tooth formation and are thought to be vestiges of the premolars found in mouse ancestors. Moreover, the mature signaling center of the first molar (M1) is formed from the fusion of two signaling centers (R2 and early M1). Here, we report that broad activation of Edar expression precedes its spatial restriction to tooth signaling centers. This reveals a hidden two-step patterning process for tooth signaling centers, which was modeled with a single activator-inhibitor pair subject to reaction-diffusion (RD). The study of Edar expression also unveiled successive phases of signaling center formation, erasing, recovering, and fusion. Our model, in which R2 signaling center is not intrinsically defective but erased by the broad activation preceding M1 signaling center formation, predicted the surprising rescue of R2 in Edar mutant mice, where activation is reduced. The importance of this R2-M1 interaction was confirmed by ex vivo cultures showing that R2 is capable of forming a tooth. Finally, by introducing chemotaxis as a secondary process to RD, we recapitulated in silico different conditions in which R2 and M1 centers fuse or not. In conclusion, pattern formation in the mouse molar field relies on basic mechanisms whose dynamics produce embryonic patterns that are plastic objects rather than fixed end points.
When patterns are set during embryogenesis, it is expected that they are straightly established rather than subsequently modified. The patterning of the three mouse molars is, however, far from straight, likely as a result of mouse evolutionary history. The first-formed tooth signaling centers, called MS and R2, disappear before driving tooth formation and are thought to be vestiges of the premolars found in mouse ancestors. Moreover, the mature signaling center of the first molar (M1) is formed from the fusion of two signaling centers (R2 and early M1). Here, we report that broad activation of Edar expression precedes its spatial restriction to tooth signaling centers. This reveals a hidden two-step patterning process for tooth signaling centers, which was modeled with a single activator–inhibitor pair subject to reaction–diffusion (RD). The study of Edar expression also unveiled successive phases of signaling center formation, erasing, recovering, and fusion. Our model, in which R2 signaling center is not intrinsically defective but erased by the broad activation preceding M1 signaling center formation, predicted the surprising rescue of R2 in Edar mutant mice, where activation is reduced. The importance of this R2–M1 interaction was confirmed by ex vivo cultures showing that R2 is capable of forming a tooth. Finally, by introducing chemotaxis as a secondary process to RD, we recapitulated in silico different conditions in which R2 and M1 centers fuse or not. In conclusion, pattern formation in the mouse molar field relies on basic mechanisms whose dynamics produce embryonic patterns that are plastic objects rather than fixed end points.
When patterns are set during embryogenesis, it is expected that they are straightly established rather than subsequently modified. The patterning of the three mouse molars is, however, far from straight, likely as a result of mouse evolutionary history. The first-formed tooth signaling centers, called MS and R2, disappear before driving tooth formation and are thought to be vestiges of the premolars found in mouse ancestors. Moreover, the mature signaling center of the first molar (M1) is formed from the fusion of two signaling centers (R2 and early M1). Here, we report that broad activation of Edar expression precedes its spatial restriction to tooth signaling centers. This reveals a hidden two-step patterning process for tooth signaling centers, which was modeled with a single activator–inhibitor pair subject to reaction–diffusion (RD). The study of Edar expression also unveiled successive phases of signaling center formation, erasing, recovering, and fusion. Our model, in which R2 signaling center is not intrinsically defective but erased by the broad activation preceding M1 signaling center formation, predicted the surprising rescue of R2 in Edar mutant mice, where activation is reduced. The importance of this R2–M1 interaction was confirmed by ex vivo cultures showing that R2 is capable of forming a tooth. Finally, by introducing chemotaxis as a secondary process to RD, we recapitulated in silico different conditions in which R2 and M1 centers fuse or not. In conclusion, pattern formation in the mouse molar field relies on basic mechanisms whose dynamics produce embryonic patterns that are plastic objects rather than fixed end points. The generation of patterns during development is generally viewed as a direct process, but this study of mouse tooth development shows how embryonic patterns can be constructed and erased in a very dynamic manner before the correct pattern is achieved. Organs, such as teeth, that form regular patterns are of particular interest to developmental biologists. These patterns are established early in the embryo, and it has generally been thought the organs appear in what is their final position. Recent studies that focus on the dynamics of patterning events challenge this view, suggesting that pattern formation can be more complex than previously thought. For example, mouse molars form from “organizing centers,” which appear, disappear, or fuse in a complex sequence of events, until the final pattern is stabilized. Based on the dynamics of expression of the Edar gene, we built a mathematical model of how tooth “organizing centers” form. We reveal that a newly formed organizing center can actively impair or erase a previously formed one. We call this phenomenon a developmental “palimpsest,” from the terminology of old manuscripts that were scraped to be reused again. This indirect developmental process likely reflects the evolutionary history of mice, which lost premolars while maintaining their embryonic organizing centers. More broadly, we believe that overwriting or correcting previously established patterns during development might be more common than anticipated, simply due to the fact that developmental programs are modified by incrementation during evolution.
Audience Academic
Author Calvez, Vincent
Laudet, Vincent
Hayden, Luke
Twarogowska, Monika
Sadier, Alexa
Lambert, Anne
Steklikova, Klara
Schneider, Pascal
Pantalacci, Sophie
Hovorakova, Maria
AuthorAffiliation 4 Institute of Experimental Medicine, The Czech Academy of Sciences, Prague, Czech Republic
Cancer Research UK London Research Laboratories, UNITED KINGDOM
6 Department of Biochemistry, University of Lausanne, CH-1066 Epalinges, Switzerland
1 Laboratoire de Biologie et Modélisation de la Cellule, Université de Lyon, ENS de Lyon, Univ Claude Bernard, CNRS UMR 5239, INSERM U1210, Lyon, France
7 Institut Camille Jordan, Université de Lyon, Université Claude Bernard, CNRS UMR 5208, Lyon, France
2 Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, ENS de Lyon, Univ Claude Bernard, CNRS UMR 5239, Lyon, France
3 Unité de Mathématiques Pures et Appliquées, project team Inria NUMED, Université de Lyon, ENS de Lyon, CNRS UMR 5669, Lyon, France
5 Department of Cell Biology, Faculty of Science, Charles University, Prague, Czech Republic
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30730874$$D View this record in MEDLINE/PubMed
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Cites_doi 10.1242/dev.127.21.4711
10.1016/j.tig.2013.08.006
10.1083/jcb.201512074
10.1242/dev.056051
10.1242/dev.02708
10.1002/ar.20804
10.1242/dev.02278
10.1111/j.1525-142X.2010.00425.x
10.1002/jez.b.21093
10.1038/nature02927
10.1016/j.ydbio.2008.04.023
10.1242/dev.081927
10.1002/dvdy.22596
10.1016/j.devcel.2006.05.014
10.1038/ng.1090
10.1038/nature06153
10.1002/1521-1878(200008)22:8<753::AID-BIES9>3.0.CO;2-Z
10.1016/j.ydbio.2016.10.001
10.1016/j.cels.2015.10.004
10.1002/jez.b.22502
10.1242/dev.148080
10.1016/0092-8674(93)90627-3
10.1074/jbc.M113.535740
10.1242/dev.127.21.4691
10.1007/BF02476407
10.1016/j.archoralbio.2004.10.020
10.1016/j.biosystems.2014.06.003
10.1111/j.1525-142X.2011.00491.x
10.1080/03008200290000673
10.1016/j.devcel.2014.02.003
10.1073/pnas.1002784107
10.1126/scisignal.2002414
10.1073/pnas.0600825103
10.1242/dev.01163
10.1098/rstb.1952.0012
10.1002/jez.b.21266
10.1126/science.301.5631.277
10.1073/pnas.1112801108
10.1073/pnas.0808622106
10.1016/j.cell.2004.07.024
10.1371/journal.pone.0004985
10.1186/s12861-015-0070-0
10.1126/science.1179047
10.1038/s41437-017-0033-2
10.1007/s00285-008-0201-3
10.1016/j.cels.2015.10.002
10.1016/j.semcdb.2014.01.007
10.1038/nature08838
10.1371/journal.pbio.2003174
10.1126/science.1226804
10.1242/bio.013672
10.1093/ejo/cjr049
10.1016/j.devcel.2011.07.006
10.1242/dev.079558
10.1016/j.devcel.2009.05.011
10.1016/0003-9969(87)90055-0
10.1016/j.jmb.2007.01.089
10.1371/journal.pbio.2002439
10.1016/j.semcdb.2010.01.007
10.1006/dbio.2000.9955
10.1387/ijdb.041958mm
10.1242/dev.00425
10.1016/j.jtbi.2017.10.026
10.1242/dev.114991
10.1371/journal.pcbi.1005285
10.1038/11943
10.1371/journal.pbio.2002117
10.1034/j.1600-0544.2002.02225.x
10.1016/0022-5193(70)90092-5
10.1016/j.smim.2014.05.002
10.1242/dev.054668
10.1016/j.semcdb.2007.01.007
10.1242/dev.126.20.4557
10.1016/j.gde.2012.11.013
ContentType Journal Article
Copyright COPYRIGHT 2019 Public Library of Science
2019 Sadier et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Distributed under a Creative Commons Attribution 4.0 International License
2019 Sadier et al 2019 Sadier et al
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– notice: 2019 Sadier et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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ISSN 1545-7885
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IsDoiOpenAccess true
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Issue 2
Keywords Jaw
Teeth
Molars
Signaling centers
Epithelium
Chemotaxis
Embryos
Embryonic pattern formation
Language English
License Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0
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content type line 14
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Current address: Observatoire Océanologique de Banyuls-sur-Mer, UMR CNRS 7232 BIOM, Sorbonne Université, Banyuls-sur-Mer, France
Current address: Department of Ecology and Evolutionary Biology, University of California at Los Angeles, Los Angeles, California, United States of America
The authors have declared that no competing interests exist.
ORCID 0000-0002-9907-3714
0000-0002-1939-5714
0000-0003-0677-9409
0000-0002-7082-4377
0000-0002-0771-8985
0000-0002-3674-1965
OpenAccessLink http://journals.scholarsportal.info/openUrl.xqy?doi=10.1371/journal.pbio.3000064
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References PK Maini (ref66) 2015; 1
M Gaete (ref24) 2015; 4
I Miletich (ref65) 2011; 108
RE Baker (ref69) 2008
L. Wolpert (ref2) 2016
PM Munne (ref58) 2010; 12
B Verd (ref77) 2018; 16
C Mou (ref12) 2006; 103
C Charles (ref54) 2009; 292
S-W Cho (ref31) 2011; 138
N Navarro (ref32) 2018; 121
J Cotterell (ref15) 2015; 1
AS Tucker (ref51) 2000; 127
Y Ahn (ref40) 2010; 137
S Kondo (ref4) 2010; 329
C. Patlak (ref21) 1953; 15
P Kristenová (ref55) 2002; 5
M Mina (ref61) 1987; 32
OD Klein (ref72) 2006; 11
SA Alfaqeeh (ref84) 2013
DS Eom (ref17) 2015; 4
AT Kangas (ref52) 2004; 432
S Pascoal (ref68) 2007; 368
T Mammoto (ref28) 2011; 21
R Peterkova (ref39) 2009; 312B
S Lefebvre (ref43) 2014; 26
ML Mikkola (ref59) 2007; 18
M Bei (ref62) 2000; 127
I Salazar-Ciudad (ref8) 2010; 464
H Lesot (ref25) 1996; 40
AM Turing (ref5) 1952; 237
L Ahtiainen (ref49) 2016; 214
H Meinhardt (ref16) 2000; 22
A Sadier (ref44) 2014; 30
R Peterkova (ref26) 1996; 40
E. Clark (ref75) 2017; 15
M Peterka (ref80) 2002; 43
M Pummila (ref56) 2007; 134
Y Echelard (ref82) 1993; 75
DJ O’Connell (ref27) 2012; 5
KD Kavanagh (ref30) 2007; 449
MT Cobourne (ref70) 2004; 131
JD Glover (ref11) 2017; 15
BD Harfe (ref81) 2004; 118
S Jia (ref64) 2016; 420
AD Economou (ref13) 2012; 44
A Nakamasu (ref18) 2009; 106
R DasGupta (ref78) 1999; 126
JBA Green (ref3) 2015; 142
R Peterkova (ref35) 2006; 306B
E Harjunmaa (ref50) 2014
L Li (ref73) 2011; 240
LC Biggs (ref29) 2014; 25–26
C Charles (ref53) 2009; 4
S Jia (ref63) 2013; 140
Sheth Rushikesh (ref14) 2012; 338
S Lagronova-Churava (ref42) 2013; 320
KJ Painter (ref22) 2018; 437
MT Cobourne (ref37) 2010; 21
O Haara (ref41) 2012; 139
A Crombach (ref76) 2014; 123
J Laurikkala (ref47) 2001; 229
J Prochazka (ref33) 2010; 107
F Jacob (ref74) 1977; 196
I. Salazar-Ciudad (ref7) 2003; 130
C Kowalczyk-Quintas (ref83) 2014; 289
R Peterková (ref38) 2005; 50
L Marcon (ref10) 2012; 22
R. Schmidt-Ullrich (ref45) 2006; 133
EF Keller (ref20) 1970; 26
B Verd (ref9) 2017; 13
T Hillen (ref19) 2009; 58
HG Rodrigues (ref23) 2011; 13
L Viriot (ref34) 2002; 44
L Ahtiainen (ref48) 2014; 28
Y Zhang (ref46) 2009; 17
M Maroto (ref67) 2005; 49
DJ Headon (ref79) 1999; 22
Wolpert L. Chapter (ref1) 1971
I Fliniaux (ref57) 2008; 320
K Lochovska (ref36) 2015; 15
T Porntaveetus (ref71) 2012; 34
M Prochazkova (ref60) 2017; 144
D. Duboule (ref6) 2003; 301
References_xml – volume: 127
  start-page: 4711
  year: 2000
  ident: ref62
  article-title: BMP4 rescues a non-cell-autonomous function of Msx1 in tooth development
  publication-title: Development
  doi: 10.1242/dev.127.21.4711
– volume: 40
  start-page: 1009
  year: 1996
  ident: ref26
  article-title: Mouse molar morphogenesis revisited by three dimensional reconstruction. I. Analysis of initial stages of the first upper molar development revealed two transient buds
  publication-title: Int J Dev Biol
– volume: 30
  start-page: 24
  year: 2014
  ident: ref44
  article-title: The ectodysplasin pathway: from diseases to adaptations
  publication-title: Trends Genet
  doi: 10.1016/j.tig.2013.08.006
– volume: 214
  start-page: 753
  year: 2016
  ident: ref49
  article-title: Early epithelial signaling center governs tooth budding morphogenesis
  publication-title: J Cell Biol
  doi: 10.1083/jcb.201512074
– start-page: 597
  year: 2016
  ident: ref2
  article-title: Current Topics in Developmental Biology
– volume: 138
  start-page: 1807
  year: 2011
  ident: ref31
  article-title: Interactions between Shh, Sostdc1 and Wnt signaling and a new feedback loop for spatial patterning of the teeth
  publication-title: Development
  doi: 10.1242/dev.056051
– volume: 134
  start-page: 117
  year: 2007
  ident: ref56
  article-title: Ectodysplasin has a dual role in ectodermal organogenesis: inhibition of Bmp activity and induction of Shh expression
  publication-title: Development
  doi: 10.1242/dev.02708
– volume: 292
  start-page: 299
  year: 2009
  ident: ref54
  article-title: Effect of eda Loss of Function on Upper Jugal Tooth Morphology
  publication-title: Anat Rec Adv Integr Anat Evol Biol
  doi: 10.1002/ar.20804
– volume: 44
  start-page: 233
  year: 2002
  ident: ref34
  article-title: The presence of rudimentary odontogenic structures in the mouse embryonic mandible requires reinterpretation of developmental control of first lower molar histomorphogenesis
  publication-title: Int J Dev Biol
– volume: 133
  start-page: 1045
  year: 2006
  ident: ref45
  article-title: NF- B transmits Eda A1/EdaR signalling to activate Shh and cyclin D1 expression, and controls post-initiation hair placode down growth
  publication-title: Development
  doi: 10.1242/dev.02278
– volume: 12
  start-page: 383
  year: 2010
  ident: ref58
  article-title: Splitting placodes: effects of bone morphogenetic protein and Activin on the patterning and identity of mouse incisors: Splitting placodes
  publication-title: Evol Dev
  doi: 10.1111/j.1525-142X.2010.00425.x
– volume: 306B
  start-page: 234
  year: 2006
  ident: ref35
  article-title: Phylogenetic memory of developing mammalian dentition
  publication-title: J Exp Zoolog B Mol Dev Evol
  doi: 10.1002/jez.b.21093
– volume: 432
  start-page: 211
  year: 2004
  ident: ref52
  article-title: Nonindependence of mammalian dental characters
  publication-title: Nature
  doi: 10.1038/nature02927
– volume: 320
  start-page: 60
  year: 2008
  ident: ref57
  article-title: Identification of dkk4 as a target of Eda-A1/Edar pathway reveals an unexpected role of ectodysplasin as inhibitor of Wnt signalling in ectodermal placodes
  publication-title: Dev Biol
  doi: 10.1016/j.ydbio.2008.04.023
– volume: 196
  start-page: 1161
  year: 1977
  ident: ref74
  article-title: Evolution and Tinkering
  publication-title: Evolution and Tinkering
– volume: 140
  start-page: 423
  year: 2013
  ident: ref63
  article-title: Roles of Bmp4 during tooth morphogenesis and sequential tooth formation
  publication-title: Development
  doi: 10.1242/dev.081927
– start-page: 183
  year: 2008
  ident: ref69
  article-title: Current Topics in Developmental Biology
– volume: 240
  start-page: 1344
  year: 2011
  ident: ref73
  article-title: Exogenous fibroblast growth factor 8 rescues development of mouse diastemal vestigial tooth ex vivo
  publication-title: Dev Dyn
  doi: 10.1002/dvdy.22596
– volume: 11
  start-page: 181
  year: 2006
  ident: ref72
  article-title: Sprouty Genes Control Diastema Tooth Development via Bidirectional Antagonism of Epithelial-Mesenchymal FGF Signaling
  publication-title: Dev Cell
  doi: 10.1016/j.devcel.2006.05.014
– volume: 44
  start-page: 348
  year: 2012
  ident: ref13
  article-title: Periodic stripe formation by a Turing mechanism operating at growth zones in the mammalian palate
  publication-title: Nat Genet
  doi: 10.1038/ng.1090
– volume: 449
  start-page: 427
  year: 2007
  ident: ref30
  article-title: Predicting evolutionary patterns of mammalian teeth from development
  publication-title: Nature
  doi: 10.1038/nature06153
– volume: 22
  start-page: 753
  year: 2000
  ident: ref16
  article-title: Pattern formation by local self-activation and lateral inhibition
  publication-title: Bioessays
  doi: 10.1002/1521-1878(200008)22:8<753::AID-BIES9>3.0.CO;2-Z
– volume: 420
  start-page: 110
  year: 2016
  ident: ref64
  article-title: Bmp4-Msx1 signaling and Osr2 control tooth organogenesis through antagonistic regulation of secreted Wnt antagonists
  publication-title: Dev Biol
  doi: 10.1016/j.ydbio.2016.10.001
– volume: 4
  year: 2015
  ident: ref17
  article-title: Long-distance communication by specialized cellular projections during pigment pattern development and evolution
  publication-title: eLife
– volume: 1
  start-page: 248
  year: 2015
  ident: ref66
  article-title: Rethinking Models of Pattern Formation in Somitogenesis
  publication-title: Cell Syst
  doi: 10.1016/j.cels.2015.10.004
– volume: 320
  start-page: 307
  year: 2013
  ident: ref42
  article-title: The dynamics of supernumerary tooth development are differentially regulated by Sprouty genes
  publication-title: J Exp Zoolog B Mol Dev Evol
  doi: 10.1002/jez.b.22502
– volume: 144
  start-page: 2212
  year: 2017
  ident: ref60
  article-title: FGF signaling refines Wnt gradients to regulate the patterning of taste papillae
  publication-title: Development
  doi: 10.1242/dev.148080
– volume: 75
  start-page: 1417
  year: 1993
  ident: ref82
  article-title: Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity
  publication-title: Cell
  doi: 10.1016/0092-8674(93)90627-3
– volume: 289
  start-page: 4273
  year: 2014
  ident: ref83
  article-title: Generation and Characterization of Function-blocking Anti-ectodysplasin A (EDA) Monoclonal Antibodies That Induce Ectodermal Dysplasia
  publication-title: J Biol Chem
  doi: 10.1074/jbc.M113.535740
– volume: 127
  start-page: 4691
  year: 2000
  ident: ref51
  article-title: Edar/Eda interactions regulate enamel knot formation in tooth morphogenesis
  publication-title: Development
  doi: 10.1242/dev.127.21.4691
– volume: 15
  start-page: 311
  year: 1953
  ident: ref21
  article-title: Random walk with persistence and external bias
  publication-title: Bull Math Biophys
  doi: 10.1007/BF02476407
– volume: 50
  start-page: 219
  year: 2005
  ident: ref38
  article-title: The supernumerary cheek tooth in tabby/EDA mice—a reminiscence of the premolar in mouse ancestors
  publication-title: Arch Oral Biol
  doi: 10.1016/j.archoralbio.2004.10.020
– volume: 123
  start-page: 74
  year: 2014
  ident: ref76
  article-title: Evolution of early development in dipterans: Reverse-engineering the gap gene network in the moth midge Clogmia albipunctata (Psychodidae)
  publication-title: Biosystems
  doi: 10.1016/j.biosystems.2014.06.003
– volume: 13
  start-page: 361
  year: 2011
  ident: ref23
  article-title: Evolutionary and developmental dynamics of the dentition in Muroidea and Dipodoidea (Rodentia, Mammalia): Evo-devo of muroid and dipodoid teeth
  publication-title: Evol Dev
  doi: 10.1111/j.1525-142X.2011.00491.x
– volume: 43
  start-page: 186
  year: 2002
  ident: ref80
  article-title: Body weight in mouse embryos specifies staging of tooth development
  publication-title: Connect Tissue Res
  doi: 10.1080/03008200290000673
– volume: 28
  start-page: 588
  year: 2014
  ident: ref48
  article-title: Directional Cell Migration, but Not Proliferation, Drives Hair Placode Morphogenesis
  publication-title: Dev Cell
  doi: 10.1016/j.devcel.2014.02.003
– year: 2014
  ident: ref50
  article-title: Replaying evolutionary transitions from the dental fossil record
  publication-title: Nature
– start-page: 183
  year: 1971
  ident: ref1
  article-title: Current Topics in Developmental Biology
– volume: 107
  start-page: 15497
  year: 2010
  ident: ref33
  article-title: Patterning by heritage in mouse molar row development
  publication-title: Proc Natl Acad Sci
  doi: 10.1073/pnas.1002784107
– volume: 5
  start-page: ra4
  year: 2012
  ident: ref27
  article-title: A Wnt-bmp feedback circuit controls intertissue signaling dynamics in tooth organogenesis
  publication-title: Sci Signal
  doi: 10.1126/scisignal.2002414
– volume: 103
  start-page: 9075
  year: 2006
  ident: ref12
  article-title: Generation of the primary hair follicle pattern
  publication-title: Proc Natl Acad Sci
  doi: 10.1073/pnas.0600825103
– volume: 131
  start-page: 2875
  year: 2004
  ident: ref70
  article-title: Restriction of sonic hedgehog signalling during early tooth development
  publication-title: Development
  doi: 10.1242/dev.01163
– volume: 237
  start-page: 37
  year: 1952
  ident: ref5
  article-title: The chemical basis of morphogenesis
  publication-title: Philos Trans R Soc Lond B Biol Sci
  doi: 10.1098/rstb.1952.0012
– volume: 312B
  start-page: 292
  year: 2009
  ident: ref39
  article-title: Revitalization of a diastemal tooth primordium in Spry2 null mice results from increased proliferation and decreased apoptosis
  publication-title: J Exp Zoolog B Mol Dev Evol
  doi: 10.1002/jez.b.21266
– volume: 301
  start-page: 277
  year: 2003
  ident: ref6
  article-title: Time for Chronomics?
  publication-title: Science
  doi: 10.1126/science.301.5631.277
– volume: 108
  start-page: 19270
  year: 2011
  ident: ref65
  article-title: Developmental stalling and organ-autonomous regulation of morphogenesis
  publication-title: Proc Natl Acad Sci
  doi: 10.1073/pnas.1112801108
– volume: 106
  start-page: 8429
  year: 2009
  ident: ref18
  article-title: Interactions between zebrafish pigment cells responsible for the generation of Turing patterns
  publication-title: Proc Natl Acad Sci
  doi: 10.1073/pnas.0808622106
– volume: 118
  start-page: 517
  year: 2004
  ident: ref81
  article-title: Evidence for an Expansion-Based Temporal Shh Gradient in Specifying Vertebrate Digit Identities
  publication-title: Cell
  doi: 10.1016/j.cell.2004.07.024
– volume: 4
  start-page: e4985
  year: 2009
  ident: ref53
  article-title: Distinct Impacts of Eda and Edar Loss of Function on the Mouse Dentition
  publication-title: PLoS ONE
  doi: 10.1371/journal.pone.0004985
– volume: 15
  year: 2015
  ident: ref36
  article-title: Sprouty gene dosage influences temporal-spatial dynamics of primary enamel knot formation
  publication-title: BMC Dev Biol
  doi: 10.1186/s12861-015-0070-0
– volume: 329
  start-page: 1616
  year: 2010
  ident: ref4
  article-title: Reaction-Diffusion Model as a Framework for Understanding Biological Pattern Formation
  publication-title: Science
  doi: 10.1126/science.1179047
– volume: 121
  start-page: 1
  year: 2018
  ident: ref32
  article-title: Genetic mapping of molar size relations identifies inhibitory locus for third molars in mice
  publication-title: Heredity
  doi: 10.1038/s41437-017-0033-2
– volume: 58
  start-page: 183
  year: 2009
  ident: ref19
  article-title: A user’s guide to PDE models for chemotaxis
  publication-title: J Math Biol
  doi: 10.1007/s00285-008-0201-3
– volume: 1
  start-page: 257
  year: 2015
  ident: ref15
  article-title: A Local, Self-Organizing Reaction-Diffusion Model Can Explain Somite Patterning in Embryos
  publication-title: Cell Syst
  doi: 10.1016/j.cels.2015.10.002
– volume: 25–26
  start-page: 11
  year: 2014
  ident: ref29
  article-title: Early inductive events in ectodermal appendage morphogenesis
  publication-title: Semin Cell Dev Biol
  doi: 10.1016/j.semcdb.2014.01.007
– volume: 464
  start-page: 583
  year: 2010
  ident: ref8
  article-title: A computational model of teeth and the developmental origins of morphological variation
  publication-title: Nature
  doi: 10.1038/nature08838
– volume: 40
  start-page: 1017
  year: 1996
  ident: ref25
  article-title: Mouse molar morphogenesis revisited by three-dimensional reconstruction. II. Spatial distribution of mitoses and apoptosis in cap to bell staged first and second upper molar teeth
  publication-title: Int J Dev Biol
– volume: 16
  start-page: 24
  year: 2018
  ident: ref77
  article-title: A damped oscillator imposes temporal order on posterior gap gene expression in Drosophila
  publication-title: PLoS Biol
  doi: 10.1371/journal.pbio.2003174
– volume: 338
  start-page: 1476
  year: 2012
  ident: ref14
  article-title: Hox Genes Regulate Digit Patterning by Controlling the Wavelength of a Turing-Type Mechanism
  publication-title: Science
  doi: 10.1126/science.1226804
– volume: 4
  start-page: 1625
  year: 2015
  ident: ref24
  article-title: Epithelial topography for repetitive tooth formation
  publication-title: Biol Open
  doi: 10.1242/bio.013672
– volume: 34
  start-page: 518
  year: 2012
  ident: ref71
  article-title: Wnt signaling in the murine diastema
  publication-title: Eur J Orthod
  doi: 10.1093/ejo/cjr049
– volume: 21
  start-page: 758
  year: 2011
  ident: ref28
  article-title: Mechanochemical Control of Mesenchymal Condensation and Embryonic Tooth Organ Formation
  publication-title: Dev Cell
  doi: 10.1016/j.devcel.2011.07.006
– volume: 139
  start-page: 3189
  year: 2012
  ident: ref41
  article-title: Ectodysplasin regulates activator-inhibitor balance in murine tooth development through Fgf20 signaling
  publication-title: Development
  doi: 10.1242/dev.079558
– volume: 17
  start-page: 49
  year: 2009
  ident: ref46
  article-title: Reciprocal Requirements for EDA/EDAR/NF-κB and Wnt/β-Catenin Signaling Pathways in Hair Follicle Induction
  publication-title: Dev Cell
  doi: 10.1016/j.devcel.2009.05.011
– volume: 32
  start-page: 123
  year: 1987
  ident: ref61
  article-title: The induction of odontogenesis in non-dental mesenchyme combined with early murine mandibular arch epithelium
  publication-title: Arch Oral Biol
  doi: 10.1016/0003-9969(87)90055-0
– volume: 368
  start-page: 303
  year: 2007
  ident: ref68
  article-title: A Molecular Clock Operates During Chick Autopod Proximal-distal Outgrowth
  publication-title: J Mol Biol
  doi: 10.1016/j.jmb.2007.01.089
– volume: 15
  start-page: e2002439
  year: 2017
  ident: ref75
  article-title: Dynamic patterning by the Drosophila pair-rule network reconciles long-germ and short-germ segmentation
  publication-title: PLoS Biol
  doi: 10.1371/journal.pbio.2002439
– volume: 21
  start-page: 314
  year: 2010
  ident: ref37
  article-title: Making up the numbers: The molecular control of mammalian dental formula
  publication-title: Semin Cell Dev Biol
  doi: 10.1016/j.semcdb.2010.01.007
– volume: 229
  start-page: 443
  year: 2001
  ident: ref47
  article-title: TNF Signaling via the Ligand–Receptor Pair Ectodysplasin and Edar Controls the Function of Epithelial Signaling Centers and Is Regulated by Wnt and Activin during Tooth Organogenesis
  publication-title: Dev Biol
  doi: 10.1006/dbio.2000.9955
– volume: 49
  start-page: 309
  year: 2005
  ident: ref67
  article-title: Synchronised cycling gene oscillations in presomitic mesoderm cells require cell-cell contact
  publication-title: Int J Dev Biol
  doi: 10.1387/ijdb.041958mm
– volume: 130
  start-page: 2027
  year: 2003
  ident: ref7
  article-title: Mechanisms of pattern formation in development and evolution
  publication-title: Development
  doi: 10.1242/dev.00425
– volume: 437
  start-page: 225
  year: 2018
  ident: ref22
  article-title: A chemotaxis model of feather primordia pattern formation during avian development
  publication-title: J Theor Biol
  doi: 10.1016/j.jtbi.2017.10.026
– volume: 142
  start-page: 1203
  year: 2015
  ident: ref3
  article-title: Positional information and reaction-diffusion: two big ideas in developmental biology combine
  publication-title: Development
  doi: 10.1242/dev.114991
– volume: 13
  start-page: e1005285
  year: 2017
  ident: ref9
  article-title: Dynamic Maternal Gradients Control Timing and Shift-Rates for Drosophila Gap Gene Expression
  publication-title: PLoS Comput Biol
  doi: 10.1371/journal.pcbi.1005285
– volume: 22
  start-page: 370
  year: 1999
  ident: ref79
  article-title: Involvement of a novel Tnf receptor homologue in hair follicle induction
  publication-title: Nat Genet
  doi: 10.1038/11943
– volume: 15
  start-page: e2002117
  year: 2017
  ident: ref11
  article-title: Hierarchical patterning modes orchestrate hair follicle morphogenesis
  publication-title: PLoS Biol
  doi: 10.1371/journal.pbio.2002117
– volume: 5
  start-page: 205
  year: 2002
  ident: ref55
  article-title: Different morphotypes of functional dentition in the lower molar region of tabby (EDA) mice
  publication-title: Orthod Craniofac Res
  doi: 10.1034/j.1600-0544.2002.02225.x
– volume: 26
  start-page: 399
  year: 1970
  ident: ref20
  article-title: Initiation of slime mold aggregation viewed as an instability
  publication-title: J Theor Biol
  doi: 10.1016/0022-5193(70)90092-5
– volume: 26
  start-page: 220
  year: 2014
  ident: ref43
  article-title: Ectodysplasin research—Where to next?
  publication-title: Semin Immunol
  doi: 10.1016/j.smim.2014.05.002
– volume: 137
  start-page: 3221
  year: 2010
  ident: ref40
  article-title: Inhibition of Wnt signaling by Wise (Sostdc1) and negative feedback from Shh controls tooth number and patterning
  publication-title: Development
  doi: 10.1242/dev.054668
– volume: 18
  start-page: 225
  year: 2007
  ident: ref59
  article-title: Genetic basis of skin appendage development
  publication-title: Semin Cell Dev Biol
  doi: 10.1016/j.semcdb.2007.01.007
– volume: 126
  start-page: 4557
  year: 1999
  ident: ref78
  article-title: Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation
  publication-title: Development
  doi: 10.1242/dev.126.20.4557
– volume: 22
  start-page: 578
  year: 2012
  ident: ref10
  article-title: Turing patterns in development: what about the horse part?
  publication-title: Curr Opin Genet Dev
  doi: 10.1016/j.gde.2012.11.013
– year: 2013
  ident: ref84
  article-title: The Slice Culture Method for Following Development of Tooth Germs In Explant Culture
  publication-title: J Vis Exp
RelatedPersons Bernard, Claude (1813-1878)
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Snippet When patterns are set during embryogenesis, it is expected that they are straightly established rather than subsequently modified. The patterning of the three...
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SubjectTerms Activation
Animals
Bernard, Claude (1813-1878)
Biochemistry, Molecular Biology
Biology and Life Sciences
Body Patterning
Cell aggregation
Chemotaxis
Development Biology
Developmental biology
Edar Receptor - genetics
Edar Receptor - metabolism
Embryogenesis
Embryology and Organogenesis
Embryonic growth stage
Epithelium - embryology
Epithelium - metabolism
Funding
Gene expression
Gene Expression Regulation, Developmental
Genetic aspects
Genomics
Hair
Hair - embryology
Insects
Life Sciences
Medicine and Health Sciences
Mice
Mice, Mutant Strains
Models, Biological
Molars
Morphogenesis
Observations
Pattern formation
Patterning
Premolars
Signal Transduction
Signaling
Supervision
Teeth
Tooth - embryology
Tooth - metabolism
Tooth Germ - embryology
Tooth Germ - metabolism
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Title Modeling Edar expression reveals the hidden dynamics of tooth signaling center patterning
URI https://www.ncbi.nlm.nih.gov/pubmed/30730874
https://www.proquest.com/docview/2249961146
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https://pubmed.ncbi.nlm.nih.gov/PMC6382175
https://doaj.org/article/2d86638a11a24fde8759aa2c29f1eea6
http://dx.doi.org/10.1371/journal.pbio.3000064
Volume 17
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