Calcium Sets the Clock in Ameloblasts

Stromal interaction molecule 1 ( ) is one of the main components of the store operated Ca entry (SOCE) signaling pathway. Individuals with mutated present severely hypomineralized enamel characterized as amelogenesis imperfecta (AI) but the downstream molecular mechanisms involved remain unclear. Ci...

Full description

Saved in:
Bibliographic Details
Published inFrontiers in physiology Vol. 11; p. 920
Main Authors Said, Raed, Lobanova, Liubov, Papagerakis, Silvana, Papagerakis, Petros
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 31.07.2020
Subjects
ameloblast
calcium
circadian clock
enamel
Physiology
STIM1
store operated Ca2+ channels
calcium
STIM1
enamel
ameloblast
circadian clock
amelogenesis
amelogenesis imperfecta
store operated Ca2+ channels
Online AccessGet full text

Cover

Abstract Stromal interaction molecule 1 ( ) is one of the main components of the store operated Ca entry (SOCE) signaling pathway. Individuals with mutated present severely hypomineralized enamel characterized as amelogenesis imperfecta (AI) but the downstream molecular mechanisms involved remain unclear. Circadian clock signaling plays a key role in regulating the enamel thickness and mineralization, but the effects of -mediated AI on circadian clock are unknown. The aim of this study is to examine the potential links between SOCE and the circadian clock during amelogenesis. We have generated mice with ameloblast-specific deletion of ( /Amelx-iCre , cKO) and analyzed circadian gene expression profile in compared to control ( /Amelx-iCre ) using ameloblast micro-dissection and RNA micro-array of 84 circadian genes. Expression level changes were validated by qRT-PCR and immunohistochemistry. deletion has resulted in significant upregulation of the core circadian activator gene Brain and Muscle Aryl Hydrocarbon Receptor Nuclear Translocation 1 ( ) and downregulation of the circadian inhibitor Period 2 ( ). Our analyses also revealed that SOCE disruption results in dysregulation of two additional circadian regulators; p38α mitogen-activated protein kinase (MAPK14) and transforming growth factor-beta1 (TGF-β1). Both MAPK14 and TGF-β1 pathways are known to play major roles in enamel secretion and their dysregulation has been previously implicated in the development of AI phenotype. These data indicate that disruption of SOCE significantly affects the ameloblasts molecular circadian clock, suggesting that alteration of the circadian clock may be partly involved in the development of -mediated AI.
AbstractList Stromal interaction molecule 1 ( ) is one of the main components of the store operated Ca entry (SOCE) signaling pathway. Individuals with mutated present severely hypomineralized enamel characterized as amelogenesis imperfecta (AI) but the downstream molecular mechanisms involved remain unclear. Circadian clock signaling plays a key role in regulating the enamel thickness and mineralization, but the effects of -mediated AI on circadian clock are unknown. The aim of this study is to examine the potential links between SOCE and the circadian clock during amelogenesis. We have generated mice with ameloblast-specific deletion of ( /Amelx-iCre , cKO) and analyzed circadian gene expression profile in compared to control ( /Amelx-iCre ) using ameloblast micro-dissection and RNA micro-array of 84 circadian genes. Expression level changes were validated by qRT-PCR and immunohistochemistry. deletion has resulted in significant upregulation of the core circadian activator gene Brain and Muscle Aryl Hydrocarbon Receptor Nuclear Translocation 1 ( ) and downregulation of the circadian inhibitor Period 2 ( ). Our analyses also revealed that SOCE disruption results in dysregulation of two additional circadian regulators; p38α mitogen-activated protein kinase (MAPK14) and transforming growth factor-beta1 (TGF-β1). Both MAPK14 and TGF-β1 pathways are known to play major roles in enamel secretion and their dysregulation has been previously implicated in the development of AI phenotype. These data indicate that disruption of SOCE significantly affects the ameloblasts molecular circadian clock, suggesting that alteration of the circadian clock may be partly involved in the development of -mediated AI.
BackgroundStromal interaction molecule 1 (STIM1) is one of the main components of the store operated Ca2+ entry (SOCE) signaling pathway. Individuals with mutated STIM1 present severely hypomineralized enamel characterized as amelogenesis imperfecta (AI) but the downstream molecular mechanisms involved remain unclear. Circadian clock signaling plays a key role in regulating the enamel thickness and mineralization, but the effects of STIM1-mediated AI on circadian clock are unknown.ObjectivesThe aim of this study is to examine the potential links between SOCE and the circadian clock during amelogenesis.MethodsWe have generated mice with ameloblast-specific deletion of Stim1 (Stim1fl/fl/Amelx-iCre+/+, Stim1 cKO) and analyzed circadian gene expression profile in Stim1 cKO compared to control (Stim1fl/fl/Amelx-iCre–/–) using ameloblast micro-dissection and RNA micro-array of 84 circadian genes. Expression level changes were validated by qRT-PCR and immunohistochemistry.ResultsStim1 deletion has resulted in significant upregulation of the core circadian activator gene Brain and Muscle Aryl Hydrocarbon Receptor Nuclear Translocation 1 (Bmal1) and downregulation of the circadian inhibitor Period 2 (Per2). Our analyses also revealed that SOCE disruption results in dysregulation of two additional circadian regulators; p38α mitogen-activated protein kinase (MAPK14) and transforming growth factor-beta1 (TGF-β1). Both MAPK14 and TGF-β1 pathways are known to play major roles in enamel secretion and their dysregulation has been previously implicated in the development of AI phenotype.ConclusionThese data indicate that disruption of SOCE significantly affects the ameloblasts molecular circadian clock, suggesting that alteration of the circadian clock may be partly involved in the development of STIM1-mediated AI.
BACKGROUNDStromal interaction molecule 1 (STIM1) is one of the main components of the store operated Ca2+ entry (SOCE) signaling pathway. Individuals with mutated STIM1 present severely hypomineralized enamel characterized as amelogenesis imperfecta (AI) but the downstream molecular mechanisms involved remain unclear. Circadian clock signaling plays a key role in regulating the enamel thickness and mineralization, but the effects of STIM1-mediated AI on circadian clock are unknown. OBJECTIVESThe aim of this study is to examine the potential links between SOCE and the circadian clock during amelogenesis. METHODSWe have generated mice with ameloblast-specific deletion of Stim1 (Stim1 fl/fl/Amelx-iCre+/+, Stim1 cKO) and analyzed circadian gene expression profile in Stim1 cKO compared to control (Stim1 fl/fl/Amelx-iCre-/-) using ameloblast micro-dissection and RNA micro-array of 84 circadian genes. Expression level changes were validated by qRT-PCR and immunohistochemistry. RESULTSStim1 deletion has resulted in significant upregulation of the core circadian activator gene Brain and Muscle Aryl Hydrocarbon Receptor Nuclear Translocation 1 (Bmal1) and downregulation of the circadian inhibitor Period 2 (Per2). Our analyses also revealed that SOCE disruption results in dysregulation of two additional circadian regulators; p38α mitogen-activated protein kinase (MAPK14) and transforming growth factor-beta1 (TGF-β1). Both MAPK14 and TGF-β1 pathways are known to play major roles in enamel secretion and their dysregulation has been previously implicated in the development of AI phenotype. CONCLUSIONThese data indicate that disruption of SOCE significantly affects the ameloblasts molecular circadian clock, suggesting that alteration of the circadian clock may be partly involved in the development of STIM1-mediated AI.
Author Papagerakis, Silvana
Said, Raed
Papagerakis, Petros
Lobanova, Liubov
AuthorAffiliation 1 Department of Anatomy, Physiology and Pharmacology, College of Medicine, University of Saskatchewan , Saskatoon, SK , Canada
2 College of Dentistry, University of Saskatchewan , Saskatoon, SK , Canada
3 Department of Surgery, College of Medicine, University of Saskatchewan , Saskatoon, SK , Canada
AuthorAffiliation_xml – name: 2 College of Dentistry, University of Saskatchewan , Saskatoon, SK , Canada
– name: 3 Department of Surgery, College of Medicine, University of Saskatchewan , Saskatoon, SK , Canada
– name: 1 Department of Anatomy, Physiology and Pharmacology, College of Medicine, University of Saskatchewan , Saskatoon, SK , Canada
Author_xml – sequence: 1
  givenname: Raed
  surname: Said
  fullname: Said, Raed
  organization: College of Dentistry, University of Saskatchewan, Saskatoon, SK, Canada
– sequence: 2
  givenname: Liubov
  surname: Lobanova
  fullname: Lobanova, Liubov
  organization: College of Dentistry, University of Saskatchewan, Saskatoon, SK, Canada
– sequence: 3
  givenname: Silvana
  surname: Papagerakis
  fullname: Papagerakis, Silvana
  organization: Department of Surgery, College of Medicine, University of Saskatchewan, Saskatoon, SK, Canada
– sequence: 4
  givenname: Petros
  surname: Papagerakis
  fullname: Papagerakis, Petros
  organization: College of Dentistry, University of Saskatchewan, Saskatoon, SK, Canada
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32848861$$D View this record in MEDLINE/PubMed
BookMark eNpVkbtrHDEQh0WwiR9xnypsE0hzl9FjtVITMEfsGAwpnEA6ocfIt452dVntGfzfW75zjK1Gw-g33wi-E3Iw5hEJ-UhhybnSX-Nm_VCWDBgsATSDd-SYSikWINifg1f1ETkr5Q7qETUL9D054kwJpSQ9Jp9XNvl-OzQ3OJdmXmOzStn_bfqxOR8wZZdsmcsHchhtKnj2fJ-S3xfff61-LK5_Xl6tzq8XXkg2L3x0AhBlK13XCaA6BsraQJ3nbVS8C44517rgQy1RuzailZR1UWup0QE_JVd7bsj2zmymfrDTg8m2N7tGnm6NnebeJzQAqqXIuAqaCW61BeA-ttQGHqVyWFnf9qzN1g0YPI7zZNMb6NuXsV-b23xvOkEpVaICvjwDpvxvi2U2Q188pmRHzNti6tquxjrd1ijso37KpUwYX9ZQME-yzE6WeZJldrLqyKfX33sZ-K-GPwI9bJJc
CitedBy_id crossref_primary_10_1016_j_mehy_2023_111249
crossref_primary_10_1039_D2BM00072E
crossref_primary_10_1097_MD_0000000000033229
crossref_primary_10_3389_fphys_2023_1100714
crossref_primary_10_3390_children8090720
crossref_primary_10_3389_fmolb_2024_1387576
Cites_doi 10.1016/j.tcb.2013.07.002
10.1016/j.tins.2003.09.012
10.1523/JNEUROSCI.2211-05.2005
10.1177/0022034519858976
10.1038/s41413-017-0005-4
10.1016/j.neuint.2003.09.005
10.3791/57081
10.1172/jci.insight.91166
10.1016/j.ceca.2019.03.004
10.1113/JP272775
10.1111/j.1600-0722.2009.00612.x
10.3109/07420528.2012.679330
10.1038/nrg.2016.150
10.1177/0748730412442830
10.1016/j.ceca.2018.07.012
10.1002/jcp.22965
10.1186/s12864-015-1783-y
10.1016/j.molcel.2016.10.012
10.1096/fj.201600532R
10.1101/gad.5.1.105
10.1139/cjpp-2015-0398
10.1016/j.bone.2013.02.011
10.1371/journal.pone.0145155
10.1177/10454411000110040401
10.1002/dvdy.24307
10.1016/j.yexcr.2014.02.007
10.3389/fphys.2019.00399
10.1038/sj.embor.7400920
10.1152/physrev.00020.2014
10.1111/j.1600-0722.2011.00881.x
10.1042/BST20110691
10.18632/oncotarget.25672
10.1038/nprot.2008.211
10.1007/978-94-007-2888-2_40
10.1523/ENEURO.0160-17.2017
10.1177/0022034517719872
10.1152/ajprenal.00483.2016
10.1203/00006450-199604000-00013
10.1371/journal.pone.0082267
10.1177/0022034515598144
10.1371/journal.pgen.1007433
10.1016/j.gep.2010.12.002
10.1038/s41583-018-0026-z
10.1038/srep33644
10.1016/B978-0-12-407870-3.00010-X
10.1111/j.1600-0722.2011.00918.x
10.1038/srep41733
10.1038/s41477-018-0224-8
10.1002/ar.1092240212
10.1242/jcs.070300
10.3390/ijms20092363
10.1186/s12903-019-0720-x
10.1038/srep15803
10.1101/cshperspect.a027706
10.1177/0022034510375829
10.1016/j.ceca.2017.03.006
10.1101/gad.249417.114
10.1073/pnas.1302560110
10.3389/fphys.2018.00257
10.5772/intechopen.78587
10.1177/0022034513505768
10.1073/pnas.1323618111
10.1074/jbc.M114.599274
ContentType Journal Article
Copyright Copyright © 2020 Said, Lobanova, Papagerakis and Papagerakis.
Copyright © 2020 Said, Lobanova, Papagerakis and Papagerakis. 2020 Said, Lobanova, Papagerakis and Papagerakis
Copyright_xml – notice: Copyright © 2020 Said, Lobanova, Papagerakis and Papagerakis.
– notice: Copyright © 2020 Said, Lobanova, Papagerakis and Papagerakis. 2020 Said, Lobanova, Papagerakis and Papagerakis
DBID NPM
AAYXX
CITATION
7X8
5PM
DOA
DOI 10.3389/fphys.2020.00920
DatabaseName PubMed
CrossRef
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle PubMed
CrossRef
MEDLINE - Academic
DatabaseTitleList PubMed

MEDLINE - Academic
Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
EISSN 1664-042X
EndPage 920
ExternalDocumentID oai_doaj_org_article_00851e238d9243a9a003cf51ad3f68be
10_3389_fphys_2020_00920
32848861
Genre Journal Article
GroupedDBID 53G
5VS
9T4
AAFWJ
AAKDD
ACGFO
ACGFS
ACXDI
ADBBV
ADRAZ
AENEX
AFPKN
ALMA_UNASSIGNED_HOLDINGS
AOIJS
BCNDV
DIK
EMOBN
F5P
GROUPED_DOAJ
GX1
HYE
IAO
IEA
IHR
IHW
IPNFZ
ISR
KQ8
M48
M~E
NPM
O5R
O5S
OK1
PGMZT
RIG
RNS
RPM
AAYXX
CITATION
7X8
5PM
ID FETCH-LOGICAL-c462t-cfb40ee656b774019fd125d1bc35f837db2bb5bdcd7dbe9b5fea6127f9969eb03
IEDL.DBID RPM
ISSN 1664-042X
IngestDate Tue Oct 22 15:13:09 EDT 2024
Tue Sep 17 21:09:49 EDT 2024
Fri Oct 25 04:00:01 EDT 2024
Thu Sep 26 18:27:15 EDT 2024
Sat Sep 28 08:20:39 EDT 2024
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Keywords calcium
STIM1
enamel
ameloblast
circadian clock
amelogenesis
amelogenesis imperfecta
store operated Ca2+ channels
Language English
License Copyright © 2020 Said, Lobanova, Papagerakis and Papagerakis.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c462t-cfb40ee656b774019fd125d1bc35f837db2bb5bdcd7dbe9b5fea6127f9969eb03
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
Reviewed by: Marianna Bei, Harvard Medical School, United States; Javier Catón, Universidad Complutense de Madrid, Spain
Edited by: Maisa Hanna-Maija Seppala, King’s College London, United Kingdom
This article was submitted to Craniofacial Biology and Dental Research, a section of the journal Frontiers in Physiology
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7411184/
PMID 32848861
PQID 2437843795
PQPubID 23479
PageCount 1
ParticipantIDs doaj_primary_oai_doaj_org_article_00851e238d9243a9a003cf51ad3f68be
pubmedcentral_primary_oai_pubmedcentral_nih_gov_7411184
proquest_miscellaneous_2437843795
crossref_primary_10_3389_fphys_2020_00920
pubmed_primary_32848861
PublicationCentury 2000
PublicationDate 2020-07-31
PublicationDateYYYYMMDD 2020-07-31
PublicationDate_xml – month: 07
  year: 2020
  text: 2020-07-31
  day: 31
PublicationDecade 2020
PublicationPlace Switzerland
PublicationPlace_xml – name: Switzerland
PublicationTitle Frontiers in physiology
PublicationTitleAlternate Front Physiol
PublicationYear 2020
Publisher Frontiers Media S.A
Publisher_xml – name: Frontiers Media S.A
References Bailleul-Forestier (B5) 1996; 39
Mitchell (B39) 1991; 5
Kobayashi-Kinoshita (B29) 2016; 6
Lacruz (B31); 27
Hastings (B19) 2018; 19
Martí Ruiz (B37) 2018; 4
Prakriya (B50) 2015; 95
Ye (B61) 2014; 28
Noguchi (B41) 2012; 29
Houari (B24) 2018; 133
Eckstein (B13) 2017; 2
Lacruz (B30) 2017; 65
Furukawa (B17) 2017; 96
Shim (B54) 2007; 8
Liu (B35) 2015; 16
Greenblatt (B18) 2015; 290
Palacios-Muñoz (B46) 2018; 14
Said (B51) 2019; 98
Tsuchiya (B59) 2009; 117
Athanassiou-Papaefthymiou (B3) 2011; 119
Samakai (B52) 2016; 30
Bawden (B6) 1989; 224
Enoki (B14) 2017; 7
Berdal (B7) 1995; 39
Janjiæ (B28) 2019; 19
Bhattacharya (B8) 2018; 9
Nurbaeva (B42); 5
Zheng (B65) 2015; 244
Hubbard (B26) 2000; 11
Martin-Romero (B38) 2018
Pouly (B49) 2016; 11
Zheng (B62) 2014; 325
Lacruz (B33) 2011; 119
Chaudhari (B9) 2017; 313
St. John (B56) 2014; 111
Noguchi (B40) 2017; 4
Tonelli (B58) 2012; 740
Xu (B60) 2018; 6
Zheng (B63) 2011
Partch (B48) 2014; 24
Hoth (B23) 2013; 71
Cho (B11) 2013; 8
Lundkvist (B36) 2005; 25
O’Neill (B45) 2012; 40
Simmer (B55) 2010; 89
Eckstein (B12) 2018; 75
Fahrner (B15) 2018
Shi (B53) 2013; 110
Huang (B25) 2009; 4
Nurbaeva (B44); 94
Zheng (B64) 2013; 55
Adeola (B1) 2019; 10
Nurbaeva (B43) 2017; 595
Papagerakis (B47) 2014; 93
Hegazi (B20) 2019; 20
Honma (B22) 2003; 26
Feske (B16) 2019; 80
Lacruz (B32); 227
Chen (B10) 2016; 94
Herzog (B21) 2017; 9
Huber (B27) 2016; 64
Avila-Medina (B4) 2018; 9
Takahashi (B57) 2017; 18
Agostino (B2) 2004; 44
Lee (B34) 2010; 123
References_xml – volume: 24
  start-page: 90
  year: 2014
  ident: B48
  article-title: Molecular architecture of the mammalian circadian clock.
  publication-title: Trends Cell Biol.
  doi: 10.1016/j.tcb.2013.07.002
  contributor:
    fullname: Partch
– volume: 26
  start-page: 650
  year: 2003
  ident: B22
  article-title: The biological clock: Ca2+ links the pendulum to the hands.
  publication-title: Trends Neurosci.
  doi: 10.1016/j.tins.2003.09.012
  contributor:
    fullname: Honma
– volume: 25
  start-page: 7682
  year: 2005
  ident: B36
  article-title: A calcium flux is required for circadian rhythm generation in mammalian pacemaker neurons.
  publication-title: J. Neurosci.
  doi: 10.1523/JNEUROSCI.2211-05.2005
  contributor:
    fullname: Lundkvist
– volume: 98
  start-page: 1002
  year: 2019
  ident: B51
  article-title: Generation of amelx-iCre mice supports ameloblast-specific role for Stim1.
  publication-title: J. Dent. Res.
  doi: 10.1177/0022034519858976
  contributor:
    fullname: Said
– volume: 6
  year: 2018
  ident: B60
  article-title: Transforming growth factor-β in stem cells and tissue homeostasis.
  publication-title: Bone Res.
  doi: 10.1038/s41413-017-0005-4
  contributor:
    fullname: Xu
– volume: 44
  start-page: 617
  year: 2004
  ident: B2
  article-title: Diurnal, circadian and photic regulation of calcium/calmodulin-dependent kinase II and neuronal nitric oxide synthase in the hamster suprachiasmatic nuclei.
  publication-title: Neurochem. Int.
  doi: 10.1016/j.neuint.2003.09.005
  contributor:
    fullname: Agostino
– volume: 133
  year: 2018
  ident: B24
  article-title: Micro-dissection of enamel organ from mandibular incisor of rats exposed to environmental toxicants.
  publication-title: J. Vis. Exp.
  doi: 10.3791/57081
  contributor:
    fullname: Houari
– volume: 2
  year: 2017
  ident: B13
  article-title: Store-operated Ca2+ entry controls ameloblast cell function and enamel development.
  publication-title: JCI Insight
  doi: 10.1172/jci.insight.91166
  contributor:
    fullname: Eckstein
– volume: 39
  start-page: 257
  year: 1995
  ident: B7
  article-title: Ameloblasts and odontoblasts, target-cells for 1,25-dihydroxyvitamin D3: a review.
  publication-title: Int. J. Dev. Biol.
  contributor:
    fullname: Berdal
– volume: 80
  start-page: 112
  year: 2019
  ident: B16
  article-title: CRAC channels and disease – from human CRAC channelopathies and animal models to novel drugs.
  publication-title: Cell Calcium
  doi: 10.1016/j.ceca.2019.03.004
  contributor:
    fullname: Feske
– volume: 595
  start-page: 3015
  year: 2017
  ident: B43
  article-title: Ca 2+ transport and signalling in enamel cells: calcium in enamel cells.
  publication-title: J. Physiol.
  doi: 10.1113/JP272775
  contributor:
    fullname: Nurbaeva
– volume: 117
  start-page: 105
  year: 2009
  ident: B59
  article-title: TGF-β1 expression is up-regulated in maturation stage enamel organ and may induce ameloblast apoptosis.
  publication-title: Eur. J. Oral Sci.
  doi: 10.1111/j.1600-0722.2009.00612.x
  contributor:
    fullname: Tsuchiya
– volume: 29
  start-page: 653
  year: 2012
  ident: B41
  article-title: Fibroblast circadian rhythms of PER2 expression depend on membrane potential and intracellular calcium.
  publication-title: Chronobiol. Int.
  doi: 10.3109/07420528.2012.679330
  contributor:
    fullname: Noguchi
– volume: 18
  start-page: 164
  year: 2017
  ident: B57
  article-title: Transcriptional architecture of the mammalian circadian clock.
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg.2016.150
  contributor:
    fullname: Takahashi
– volume: 27
  start-page: 237
  ident: B31
  article-title: The circadian clock modulates enamel development.
  publication-title: J. Biol. Rhythms
  doi: 10.1177/0748730412442830
  contributor:
    fullname: Lacruz
– volume: 75
  start-page: 14
  year: 2018
  ident: B12
  article-title: CRAC channels in dental enamel cells.
  publication-title: Cell Calcium
  doi: 10.1016/j.ceca.2018.07.012
  contributor:
    fullname: Eckstein
– volume: 227
  start-page: 2264
  ident: B32
  article-title: Identification of novel candidate genes involved in mineralization of dental enamel by genome-wide transcript profiling.
  publication-title: J. Cell. Physiol.
  doi: 10.1002/jcp.22965
  contributor:
    fullname: Lacruz
– volume: 16
  year: 2015
  ident: B35
  article-title: Cell cycle control, DNA damage repair, and apoptosis-related pathways control pre-ameloblasts differentiation during tooth development.
  publication-title: BMC Genomics
  doi: 10.1186/s12864-015-1783-y
  contributor:
    fullname: Liu
– volume: 64
  start-page: 774
  year: 2016
  ident: B27
  article-title: CRY2 and FBXL3 cooperatively degrade c-MYC.
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2016.10.012
  contributor:
    fullname: Huber
– volume: 30
  start-page: 3878
  year: 2016
  ident: B52
  article-title: Novel STIM1−dependent control of Ca 2+ clearance regulates NFAT activity during T−cell activation.
  publication-title: FASEB J.
  doi: 10.1096/fj.201600532R
  contributor:
    fullname: Samakai
– volume: 5
  start-page: 105
  year: 1991
  ident: B39
  article-title: Transcription factor AP-2 is expressed in neural crest cell lineages during mouse embryogenesis.
  publication-title: Genes Dev.
  doi: 10.1101/gad.5.1.105
  contributor:
    fullname: Mitchell
– volume: 94
  start-page: 1023
  year: 2016
  ident: B10
  article-title: CLOCK-BMAL1 regulate the cardiac L-type calcium channel subunit CACNA1C through PI3K-Akt signaling pathway.
  publication-title: Can. J. Physiol. Pharmacol.
  doi: 10.1139/cjpp-2015-0398
  contributor:
    fullname: Chen
– volume: 55
  start-page: 158
  year: 2013
  ident: B64
  article-title: Circadian rhythms regulate amelogenesis.
  publication-title: Bone
  doi: 10.1016/j.bone.2013.02.011
  contributor:
    fullname: Zheng
– volume: 11
  year: 2016
  ident: B49
  article-title: USP2-45 is a circadian clock output effector regulating calcium absorption at the post-translational level.
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0145155
  contributor:
    fullname: Pouly
– volume: 11
  start-page: 437
  year: 2000
  ident: B26
  article-title: Calcium transport across the dental enamel epithelium.
  publication-title: Crit. Rev. Oral Biol. Med.
  doi: 10.1177/10454411000110040401
  contributor:
    fullname: Hubbard
– volume: 244
  start-page: 1249
  year: 2015
  ident: B65
  article-title: Orai1 expression pattern in tooth and craniofacial ectodermal tissues and potential functions during ameloblast differentiation.
  publication-title: Dev. Dyn.
  doi: 10.1002/dvdy.24307
  contributor:
    fullname: Zheng
– volume: 325
  start-page: 83
  year: 2014
  ident: B62
  article-title: The tick tock of odontogenesis.
  publication-title: Exp. Cell Res.
  doi: 10.1016/j.yexcr.2014.02.007
  contributor:
    fullname: Zheng
– volume: 10
  year: 2019
  ident: B1
  article-title: Systems biology approaches and precision oral health: a circadian clock perspective.
  publication-title: Front. Physiol.
  doi: 10.3389/fphys.2019.00399
  contributor:
    fullname: Adeola
– volume: 8
  start-page: 366
  year: 2007
  ident: B54
  article-title: Rapid activation of CLOCK by Ca2+-dependent protein kinase C mediates resetting of the mammalian circadian clock.
  publication-title: EMBO Rep.
  doi: 10.1038/sj.embor.7400920
  contributor:
    fullname: Shim
– volume: 95
  start-page: 1383
  year: 2015
  ident: B50
  article-title: Store-operated calcium channels.
  publication-title: Physiol. Rev.
  doi: 10.1152/physrev.00020.2014
  contributor:
    fullname: Prakriya
– volume: 119
  start-page: 149
  year: 2011
  ident: B33
  article-title: Gene expression analysis of early and late maturation stage rat enamel organ.
  publication-title: Eur. J. Oral Sci.
  doi: 10.1111/j.1600-0722.2011.00881.x
  contributor:
    fullname: Lacruz
– volume: 40
  start-page: 44
  year: 2012
  ident: B45
  article-title: The essential role of cAMP/Ca2+ signalling in mammalian circadian timekeeping.
  publication-title: Biochem. Soc. Trans.
  doi: 10.1042/BST20110691
  contributor:
    fullname: O’Neill
– volume: 9
  start-page: 29468
  year: 2018
  ident: B8
  article-title: The calcium channel proteins ORAI3 and STIM1 mediate TGF-β induced Snai1 expression.
  publication-title: Oncotarget
  doi: 10.18632/oncotarget.25672
  contributor:
    fullname: Bhattacharya
– volume: 4
  start-page: 44
  year: 2009
  ident: B25
  article-title: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources.
  publication-title: Nat. Protoc.
  doi: 10.1038/nprot.2008.211
  contributor:
    fullname: Huang
– volume: 740
  start-page: 891
  year: 2012
  ident: B58
  article-title: Stem cells and calcium signaling.
  publication-title: Adv. Exp. Med. Biol.
  doi: 10.1007/978-94-007-2888-2_40
  contributor:
    fullname: Tonelli
– volume: 4
  year: 2017
  ident: B40
  article-title: Calcium circadian rhythmicity in the suprachiasmatic nucleus: cell autonomy and network modulation.
  publication-title: eNeuro
  doi: 10.1523/ENEURO.0160-17.2017
  contributor:
    fullname: Noguchi
– volume: 96
  start-page: 1422
  year: 2017
  ident: B17
  article-title: Stim1 regulates enamel mineralization and ameloblast modulation.
  publication-title: J. Dent. Res.
  doi: 10.1177/0022034517719872
  contributor:
    fullname: Furukawa
– volume: 313
  start-page: F729
  year: 2017
  ident: B9
  article-title: Store-operated calcium entry suppressed the TGF-β1/Smad3 signaling pathway in glomerular mesangial cells.
  publication-title: Am. J. Physiol. Renal Physiol.
  doi: 10.1152/ajprenal.00483.2016
  contributor:
    fullname: Chaudhari
– volume: 39
  start-page: 636
  year: 1996
  ident: B5
  article-title: Immunolocalization of vitamin D receptor and calbindin-D28k in human tooth germ.
  publication-title: Pediatr. Res.
  doi: 10.1203/00006450-199604000-00013
  contributor:
    fullname: Bailleul-Forestier
– volume: 8
  year: 2013
  ident: B11
  article-title: TGF-ß regulates enamel mineralization and maturation through KLK4 expression.
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0082267
  contributor:
    fullname: Cho
– volume: 94
  start-page: 1471
  ident: B44
  article-title: Store-operated Ca 2+ entry modulates the expression of enamel genes.
  publication-title: J. Dent. Res.
  doi: 10.1177/0022034515598144
  contributor:
    fullname: Nurbaeva
– volume: 14
  year: 2018
  ident: B46
  article-title: Calcium and cAMP directly modulate the speed of the Drosophila circadian clock.
  publication-title: PLoS Genet.
  doi: 10.1371/journal.pgen.1007433
  contributor:
    fullname: Palacios-Muñoz
– start-page: 202
  year: 2011
  ident: B63
  article-title: Expression of clock proteins in developing tooth.
  publication-title: Gene Expr. Patterns
  doi: 10.1016/j.gep.2010.12.002
  contributor:
    fullname: Zheng
– volume: 19
  start-page: 453
  year: 2018
  ident: B19
  article-title: Generation of circadian rhythms in the suprachiasmatic nucleus.
  publication-title: Nat. Rev. Neurosci.
  doi: 10.1038/s41583-018-0026-z
  contributor:
    fullname: Hastings
– volume: 6
  start-page: 1
  year: 2016
  ident: B29
  article-title: TGF-β1 autocrine signalling and enamel matrix components.
  publication-title: Sci. Rep.
  doi: 10.1038/srep33644
  contributor:
    fullname: Kobayashi-Kinoshita
– volume: 71
  start-page: 237
  year: 2013
  ident: B23
  article-title: The neglected CRAC proteins: Orai2, Orai3, and STIM2.
  publication-title: Curr. Top. Membr.
  doi: 10.1016/B978-0-12-407870-3.00010-X
  contributor:
    fullname: Hoth
– volume: 119
  start-page: 35
  year: 2011
  ident: B3
  article-title: Molecular and circadian controls of ameloblasts: regulation of ameloblast differentiation.
  publication-title: Eur. J. Oral Sci.
  doi: 10.1111/j.1600-0722.2011.00918.x
  contributor:
    fullname: Athanassiou-Papaefthymiou
– volume: 7
  start-page: 1
  year: 2017
  ident: B14
  article-title: Dual origins of the intracellular circadian calcium rhythm in the suprachiasmatic nucleus.
  publication-title: Sci. Rep.
  doi: 10.1038/srep41733
  contributor:
    fullname: Enoki
– volume: 4
  start-page: 690
  year: 2018
  ident: B37
  article-title: Circadian oscillations of cytosolic free calcium regulate the Arabidopsis circadian clock.
  publication-title: Nat. Plants
  doi: 10.1038/s41477-018-0224-8
  contributor:
    fullname: Martí Ruiz
– volume: 224
  start-page: 226
  year: 1989
  ident: B6
  article-title: Calcium transport during mineralization.
  publication-title: Anat. Rec.
  doi: 10.1002/ar.1092240212
  contributor:
    fullname: Bawden
– volume: 123
  start-page: 3547
  year: 2010
  ident: B34
  article-title: Coactivation of the CLOCK–BMAL1 complex by CBP mediates resetting of the circadian clock.
  publication-title: J. Cell Sci.
  doi: 10.1242/jcs.070300
  contributor:
    fullname: Lee
– volume: 20
  year: 2019
  ident: B20
  article-title: A symphony of signals: intercellular and intracellular signaling mechanisms underlying circadian timekeeping in mice and flies.
  publication-title: IJMS
  doi: 10.3390/ijms20092363
  contributor:
    fullname: Hegazi
– volume: 19
  year: 2019
  ident: B28
  article-title: Chronodentistry: the role and potential of molecular clocks in oral medicine.
  publication-title: BMC Oral Health
  doi: 10.1186/s12903-019-0720-x
  contributor:
    fullname: Janjiæ
– volume: 5
  ident: B42
  article-title: Dental enamel cells express functional SOCE channels.
  publication-title: Sci. Rep.
  doi: 10.1038/srep15803
  contributor:
    fullname: Nurbaeva
– volume: 9
  year: 2017
  ident: B21
  article-title: Regulating the suprachiasmatic nucleus (SCN) circadian clockwork: interplay between cell-autonomous and circuit-level mechanisms.
  publication-title: Cold Spring Harb. Perspect. Biol.
  doi: 10.1101/cshperspect.a027706
  contributor:
    fullname: Herzog
– volume: 89
  start-page: 1024
  year: 2010
  ident: B55
  article-title: Regulation of dental enamel shape and hardness.
  publication-title: J. Dent. Res.
  doi: 10.1177/0022034510375829
  contributor:
    fullname: Simmer
– volume: 65
  start-page: 1
  year: 2017
  ident: B30
  article-title: Enamel: molecular identity of its transepithelial ion transport system.
  publication-title: Cell Calcium
  doi: 10.1016/j.ceca.2017.03.006
  contributor:
    fullname: Lacruz
– volume: 28
  start-page: 1989
  year: 2014
  ident: B61
  article-title: Dual modes of CLOCK:BMAL1 inhibition mediated by cryptochrome and period proteins in the mammalian circadian clock.
  publication-title: Genes Dev.
  doi: 10.1101/gad.249417.114
  contributor:
    fullname: Ye
– volume: 110
  start-page: 4750
  year: 2013
  ident: B53
  article-title: Dual roles of FBXL3 in the mammalian circadian feedback loops are important for period determination and robustness of the clock.
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.1302560110
  contributor:
    fullname: Shi
– year: 2018
  ident: B15
  article-title: Studies of structure-function and subunit composition of Orai/STIM channel
  publication-title: Calcium Entry Channels in Non-Excitable Cells
  contributor:
    fullname: Fahrner
– volume: 9
  year: 2018
  ident: B4
  article-title: The complex role of store operated calcium entry pathways and related proteins in the function of cardiac, skeletal and vascular smooth muscle cells.
  publication-title: Front. Physiol.
  doi: 10.3389/fphys.2018.00257
  contributor:
    fullname: Avila-Medina
– year: 2018
  ident: B38
  article-title: Regulation of calcium signaling by STIM1 and ORAI1
  publication-title: Calcium and Signal Transduction
  doi: 10.5772/intechopen.78587
  contributor:
    fullname: Martin-Romero
– volume: 93
  start-page: 27
  year: 2014
  ident: B47
  article-title: The circadian clock in oral health and diseases.
  publication-title: J. Dent. Res.
  doi: 10.1177/0022034513505768
  contributor:
    fullname: Papagerakis
– volume: 111
  start-page: 2040
  year: 2014
  ident: B56
  article-title: Spatiotemporal separation of PER and CRY posttranslational regulation in the mammalian circadian clock.
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.1323618111
  contributor:
    fullname: St. John
– volume: 290
  start-page: 284
  year: 2015
  ident: B18
  article-title: p38α MAPK Is required for tooth morphogenesis and enamel secretion.
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M114.599274
  contributor:
    fullname: Greenblatt
SSID ssj0000402001
Score 2.3246648
Snippet Stromal interaction molecule 1 ( ) is one of the main components of the store operated Ca entry (SOCE) signaling pathway. Individuals with mutated present...
BACKGROUNDStromal interaction molecule 1 (STIM1) is one of the main components of the store operated Ca2+ entry (SOCE) signaling pathway. Individuals with...
BackgroundStromal interaction molecule 1 (STIM1) is one of the main components of the store operated Ca2+ entry (SOCE) signaling pathway. Individuals with...
SourceID doaj
pubmedcentral
proquest
crossref
pubmed
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
StartPage 920
SubjectTerms ameloblast
calcium
circadian clock
enamel
Physiology
STIM1
store operated Ca2+ channels
SummonAdditionalLinks – databaseName: DOAJ Directory of Open Access Journals
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV3PS8MwFA7iyYso_qq_qKAHD2Xpj7TNcQ7HEPSig91CXvOCw60T1_3_vqTb2ETw4q20hYTvpXnfl6TfY-w2BWlLmeSRQW6jTPI00kUuIgvOisUkkIP7wfn5JR8Ms6eRGG2U-nJnwlp74Ba4jucESInFkFJItdQ0DCsrYm1Sm5eAfvblckNM-TnYySIet_uSpMJkx7qVAtKDiTvKJV1574085O36f-OYP49KbuSe_gHbX5LGsNt29pDtYH3E7np6Uo0X0_AVm3lIPC7sUWL6CMd12J3iZAbEi5v5MRv2H996g2hZ9CCqsjxpospCxhGJZkHhquVJa4iDmBiqVFhSkwYSAAGmMnSJEoRFTSylsCRcJAJPT9huPavxjIWkLjARmghDjJkWxES45JU0CWr6ri0P2P0KAvXZelso0gQOLuXhUg4u5eEK2IPDaP2ec6X2NyhWahkr9VesAnazQljRKHZbE7rG2YIaytKidNaIImCnLeLrplLKoGWZxwErtmKx1ZftJ_X43TtlE10iAZWd_0fnL9ieg6Nd171ku83XAq-IkDRw7cfeN1-63cE
  priority: 102
  providerName: Directory of Open Access Journals
– databaseName: Scholars Portal Journals: Open Access(OpenAccess)
  dbid: M48
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV3BjtMwELVQ98IFsWKBsLsoK8GBQyCxYyc-rFaloqqQ4AKVeovseAwVbQJtKu3-PTNOtlDUA7coieLkZex5zx7PMPZKWO1LzVXiIPVJrlORmELJxFtKxeK4VZY2OH_6rGbz_ONCLv5sjx4A3B6VdlRPar5Zvb39dXeDHf6aFCf623eeJgFQ6nGK0tIcBfwJz1GnUyDfQPbDuExSKdRDzpSi6Au-6Nctjz7kwE-FdP7HOOi_oZR_-abpY_ZoIJXxuLeCU_YAmifs9cSs6uVuHX-Bbhsjz4sn6Lh-xMsmHq9h1Vrkzd32jM2nH75OZslQFCGpc8W7pPY2TwGQhtmCqulp75CjuMzWQnpUm85ya6V1tcND0FZ6MMhiCo_CRoNNxVM2atoGnrMY1QdwaZBQZJAbiUwl1WmtHQeD_d6nEXtzD0H1s899UaFmILiqAFdFcFUBroi9J4z291HW6nCi3Xyrhk5QBX4HSBIcqj5htMEhpfYyM054VVqI2NU9whVaOS1dmAbaHTaUi6Kk1IkyYs96xPdNCfSwZamyiBUH_-LgXQ6vNMvvIZM20ikUWPmL_2j3nD2kr-2ndS_YqNvs4BL5SGdfBjP7DRe33Vs
  priority: 102
  providerName: Scholars Portal
Title Calcium Sets the Clock in Ameloblasts
URI https://www.ncbi.nlm.nih.gov/pubmed/32848861
https://search.proquest.com/docview/2437843795
https://pubmed.ncbi.nlm.nih.gov/PMC7411184
https://doaj.org/article/00851e238d9243a9a003cf51ad3f68be
Volume 11
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1LT-MwEB5BT1wQK16BpcpKuwcOoXk5iY9QgRBSVysBErfIY4-hok0RpP-fsdMgijjtJYrykK1vRp7vs8djgN8ZSlvJtIgMxTbKZZxFqixEZNGVYjEpFug2OE_-Ftf3-c2DeNgA0e-F8Un7GqdnzWx-1kyffG7ly1yP-jyx0b_JmKMg8-J8tAmb7KCfJLoffp0iipNuSZIFmBxZN0nAUjB1WVwydYe_ZTwqV1WRrEUjX7T_O6b5NWHyUwS62oHtFXUMz7su_oANanbhz1jN9HQ5D2-pfQuZzYVjDk_P4bQJz-c0WyCz4_ZtD-6vLu_G19Hq6INI50XaRtpiHhMx2cLSnZknrWEmYhLUmbCsKQ2miAKNNnxLEoUlxVyltCxfJGGc7cOgWTR0CCFrDEqFYtqQUK4E85FYxlqalBSDZ-MATnsI6peuwkXNysAhV3vkaodc7ZEL4MJh9PGdq03tHyxeH-uVhWrP4oipgGFtlympeODQViTKZLaokAL41SNcsy-7BQrV0GLJDeVZWbkCiSKAgw7xj6Z6iwVQrtlirS_rb9h9fL3slbsc_fefx7DlMOimdH_CoH1d0glzkRaHXsPzdZJXQ--H73MV4F0
link.rule.ids 230,315,730,783,787,867,888,2109,24330,27936,27937,53804,53806
linkProvider National Library of Medicine
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1LT9wwEB5RemgvfYg-AgVSiR56yK7zcBIfYVW0bVlUqVBxszx-tCt2swiyl_76jp0NYlEvcIvykJ357PH32eMxwEGOwtUiKxNjmUsKwfJEVSVPHPpULCbDEv0G58lpOT4vvl3wiw3g_V6YELSvcTpoZvNBM_0TYiuv5nrYx4kNf0xGNAoSLy6GT-Ap9VdW3BHpwQF7TcTSblGSJJgYOj9NQGIw83FcIvPHv-Xkl-u6TNfGo5C2_39c837I5J0x6Pgl_Opr34WeXA6WLQ7033uJHR_8e6_gxYqVxofd49ewYZst-DRSMz1dzuOftr2JiSjGIxr5LuNpEx_O7WyBRLzbmzdwfvzlbDROVqcqJLooszbRDgtmLfE4rPxxfMIZIjkmRZ1zR3LVYIbI0WhDl1Ygd1YRDaocKSNhkeVvYbNZNPY9xCRfbMYVMZLUFooT1WGCaWEyq8hxOBbB59628qpLniFJdHhIZIBEekhkgCSCI2_82_d82utwY3H9W66sIwNBtMQyDMnGXAlFPkk7niqTu7JGG8HHHjpJ3cSvfajGLpZUUJFXtc-9yCN410F5W1TfFCKo1kBeq8v6E4IupOJeQbX96C_34dn4bHIiT76eft-B594e3czxB9hsr5d2lyhPi3uhgf8D194AjQ
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9QwEB5BkRAXKOLRAKVBggOHbJyHk_hYlq7Ko1UlqFRxsTx-wKq72VWbvfDrGTubarfi1FuUOHLsz575PnsyBnhfoHCNyKvEWOaSUrAiUXXFE4c-FYvJsUL_g_PJaXV8Xn694BcbR32FoH2N01E7m4_a6Z8QW7mc63SIE0vPTsbkBYkXl-nSuPQ-PKA5y6oNoR6MsNdFLOs3JkmGidT5pQIShLmP5RK5PwKuINvcNFW25ZNC6v7_8c3bYZMbfmjyBH4NLejDTy5Hqw5H-u-t5I53auIuPF6z0_iwL_IU7tn2GXwYq5merubxD9tdx0QY4zF5wMt42saHcztbIBHw7vo5nE-Ofo6Pk_XpCokuq7xLtMOSWUt8Dmt_LJ9whsiOyVAX3JFsNZgjcjTa0KUVyJ1VRIdqRwpJWGTFC9hpF63dg5hkjM25ImaS2VJxojxMMC1MbhUZEMci-Dj0r1z2STQkiQ8PiwywSA-LDLBE8MkDcFPOp78ONxZXv-W6h2QgipbYhiH5WCihyDZpxzNlClc1aCN4N8Anabr4PRDV2sWKKiqLuvE5GHkEL3s4b6oahkME9RbQW9-y_YTgCym513C9uvObB_Dw7PNEfv9y-u01PPLd0S8gv4Gd7mpl94n5dPg2jPF_73gDDQ
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Calcium+Sets+the+Clock+in+Ameloblasts&rft.jtitle=Frontiers+in+physiology&rft.au=Said%2C+Raed&rft.au=Lobanova%2C+Liubov&rft.au=Papagerakis%2C+Silvana&rft.au=Papagerakis%2C+Petros&rft.date=2020-07-31&rft.issn=1664-042X&rft.eissn=1664-042X&rft.volume=11&rft.spage=920&rft.epage=920&rft_id=info:doi/10.3389%2Ffphys.2020.00920&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1664-042X&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1664-042X&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1664-042X&client=summon