Bone mineral density loci specific to the skull portray potential pleiotropic effects on craniosynostosis.


Journal

Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179

Informations de publication

Date de publication:
04 07 2023
Historique:
received: 20 07 2022
accepted: 25 04 2023
medline: 6 7 2023
pubmed: 5 7 2023
entrez: 4 7 2023
Statut: epublish

Résumé

Skull bone mineral density (SK-BMD) provides a suitable trait for the discovery of key genes in bone biology, particularly to intramembranous ossification, not captured at other skeletal sites. We perform a genome-wide association meta-analysis (n ~ 43,800) of SK-BMD, identifying 59 loci, collectively explaining 12.5% of the trait variance. Association signals cluster within gene-sets involved in skeletal development and osteoporosis. Among the four novel loci (ZIC1, PRKAR1A, AZIN1/ATP6V1C1, GLRX3), there are factors implicated in intramembranous ossification and as we show, inherent to craniosynostosis processes. Functional follow-up in zebrafish confirms the importance of ZIC1 on cranial suture patterning. Likewise, we observe abnormal cranial bone initiation that culminates in ectopic sutures and reduced BMD in mosaic atp6v1c1 knockouts. Mosaic prkar1a knockouts present asymmetric bone growth and, conversely, elevated BMD. In light of this evidence linking SK-BMD loci to craniofacial abnormalities, our study provides new insight into the pathophysiology, diagnosis and treatment of skeletal diseases.

Identifiants

pubmed: 37402774
doi: 10.1038/s42003-023-04869-0
pii: 10.1038/s42003-023-04869-0
pmc: PMC10319806
doi:

Substances chimiques

Transcription Factors 0

Types de publication

Meta-Analysis Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

691

Subventions

Organisme : NCATS NIH HHS
ID : UL1 TR000128
Pays : United States
Organisme : NIA NIH HHS
ID : U01 AG042124
Pays : United States
Organisme : NIA NIH HHS
ID : U01 AG042145
Pays : United States
Organisme : NIA NIH HHS
ID : U01 AG042168
Pays : United States
Organisme : NIA NIH HHS
ID : U01 AG042140
Pays : United States
Organisme : NIA NIH HHS
ID : U24 AG051129
Pays : United States
Organisme : NICHD NIH HHS
ID : R01 HD058886
Pays : United States
Organisme : NIAMS NIH HHS
ID : R01 AR051124
Pays : United States
Organisme : NIA NIH HHS
ID : U01 AG027810
Pays : United States
Organisme : NIAMS NIH HHS
ID : U01 AR066160
Pays : United States
Organisme : NIAMS NIH HHS
ID : RC2 AR058973
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : NCRR NIH HHS
ID : M01 RR000240
Pays : United States
Organisme : NIA NIH HHS
ID : U01 AG042143
Pays : United States
Organisme : NCRR NIH HHS
ID : UL1 RR026314
Pays : United States
Organisme : NIA NIH HHS
ID : U01 AG042139
Pays : United States

Informations de copyright

© 2023. The Author(s).

Références

Mamm Genome. 2015 Oct;26(9-10):413-21
pubmed: 26314589
J Biol Chem. 2012 Mar 23;287(13):10236-10250
pubmed: 22215674
Genome Res. 2010 Sep;20(9):1297-303
pubmed: 20644199
Hum Mol Genet. 2014 Jun 1;23(11):3054-68
pubmed: 24430505
Elife. 2018 Oct 25;7:
pubmed: 30375332
Nat Genet. 2017 Oct;49(10):1468-1475
pubmed: 28869591
Dev Biol. 2002 Jan 1;241(1):106-16
pubmed: 11784098
Nat Genet. 2016 May;48(5):481-7
pubmed: 27019110
Nature. 2015 Oct 1;526(7571):112-7
pubmed: 26367794
Nat Protoc. 2014 May;9(5):1192-212
pubmed: 24762786
Bone. 2010 Mar;46(3):604-12
pubmed: 19922823
Curr Biol. 2012 Apr 10;22(7):601-7
pubmed: 22386310
J Bone Miner Res. 2018 Jun;33(6):1044-1051
pubmed: 29473973
Nat Genet. 2012 Apr 15;44(5):491-501
pubmed: 22504420
Biochem J. 2009 Jan 1;417(1):195-203
pubmed: 18657050
Osteoporos Int. 2016 Nov;27(11):3343-3354
pubmed: 27311723
Cell. 2011 Dec 23;147(7):1628-39
pubmed: 22196736
Bioinformatics. 2014 Apr 1;30(7):923-30
pubmed: 24227677
Nucleic Acids Res. 2019 Jan 8;47(D1):D801-D806
pubmed: 30407599
Am J Med Genet A. 2018 Feb;176(2):290-300
pubmed: 29168297
Genome Biol. 2016 Jun 15;17(1):127
pubmed: 27306882
Nat Genet. 2013 Oct;45(10):1238-1243
pubmed: 24013639
Am J Hum Genet. 2015 Feb 5;96(2):329-39
pubmed: 25640676
PLoS Genet. 2013;9(2):e1003247
pubmed: 23437003
BMJ. 2018 Aug 29;362:k3225
pubmed: 30158200
Proc Natl Acad Sci U S A. 2005 Nov 29;102(48):17507-12
pubmed: 16291808
Nat Genet. 2015 Nov;47(11):1236-41
pubmed: 26414676
Am J Med Genet A. 2020 Dec;182(12):2994-2998
pubmed: 32975022
Dev Biol. 2014 Feb 15;386(2):461-72
pubmed: 24360906
Nucleic Acids Res. 2015 Dec 15;43(22):e157
pubmed: 26253739
Nat Genet. 2012 Mar 18;44(4):369-75, S1-3
pubmed: 22426310
J Bone Miner Res. 2020 Sep;35(9):1782-1797
pubmed: 32379366
J Korean Neurosurg Soc. 2016 May;59(3):192-6
pubmed: 27226848
Nat Commun. 2019 Mar 19;10(1):1260
pubmed: 30890710
PLoS Genet. 2014 May 15;10(5):e1004383
pubmed: 24830394
Biotech Histochem. 2007 Feb;82(1):23-8
pubmed: 17510811
Osteoporos Int. 2012 Feb;23(2):781-7
pubmed: 21625884
Dev Cell. 2012 Apr 17;22(4):879-86
pubmed: 22516203
Am J Hum Genet. 2015 Sep 3;97(3):378-88
pubmed: 26340333
Mol Biol Cell. 2013 Jun;24(12):1895-903
pubmed: 23615448
ACS Biomater Sci Eng. 2017 Nov 13;3(11):2733-2743
pubmed: 31106260
Bone. 2008 Sep;43(3):452-8
pubmed: 18625577
Nature. 2015 Feb 19;518(7539):317-30
pubmed: 25693563
Am J Hum Genet. 2018 Jan 4;102(1):88-102
pubmed: 29304378
Nat Commun. 2017 Jul 12;8:16015
pubmed: 29313844
Acta Neuropathol. 2013 Apr;125(4):469-89
pubmed: 23525521
Am J Obstet Gynecol. 2006 Aug;195(2):373-88
pubmed: 16890548
Development. 2017 Aug 1;144(15):2798-2809
pubmed: 28684625
Nature. 2012 Sep 6;489(7414):57-74
pubmed: 22955616
Nat Commun. 2017 Nov 28;8(1):1826
pubmed: 29184056
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
Genome Biol. 2020 Mar 26;21(1):80
pubmed: 32216834
Nat Commun. 2015 Jan 19;6:5890
pubmed: 25597830
Front Endocrinol (Lausanne). 2022 Sep 26;13:1020821
pubmed: 36225206
Hum Mutat. 2002 Mar;19(3):209-16
pubmed: 11857736
J Appl Genet. 2018 May;59(2):133-147
pubmed: 29392564
Commun Biol. 2019 Aug 2;2:285
pubmed: 31396565
Bioinformatics. 2010 Sep 1;26(17):2190-1
pubmed: 20616382
Nat Genet. 2019 Feb;51(2):343-353
pubmed: 30692680
Nat Genet. 2012 Apr 15;44(5):532-538
pubmed: 22504419
Bioinformatics. 2017 Jan 15;33(2):272-279
pubmed: 27663502
Bone. 2019 Sep;126:37-50
pubmed: 30763636
Dev Biol. 2016 May 15;413(2):160-72
pubmed: 26992365
Stem Cell Reports. 2017 Apr 11;8(4):947-960
pubmed: 28344004
Heredity (Edinb). 2016 Jan;116(1):1-11
pubmed: 26174022
J Bone Miner Res. 2021 Sep;36(9):1749-1764
pubmed: 33957005
J Biol Chem. 2012 Aug 3;287(32):26829-39
pubmed: 22685294
Front Endocrinol (Lausanne). 2019 Jan 29;10:6
pubmed: 30761080
Mol Endocrinol. 2010 Aug;24(8):1559-68
pubmed: 20534695
PLoS Genet. 2014 Jun 19;10(6):e1004423
pubmed: 24945404
Genes Dev. 2016 Jan 15;30(2):208-19
pubmed: 26744418
Mol Syndromol. 2019 Feb;10(1-2):6-23
pubmed: 30976276
Nat Genet. 2019 Feb;51(2):258-266
pubmed: 30598549

Auteurs

Carolina Medina-Gomez (C)

Department of Internal Medicine, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.

Benjamin H Mullin (BH)

Department of Endocrinology and Diabetes, Sir Charles Gairdner Hospital, Nedlands, WA, 6009, Australia.
School of Biomedical Sciences, University of Western Australia, Nedlands, WA, 6009, Australia.

Alessandra Chesi (A)

Division of Human Genetics, Children's Hospital of Philadelphia, Philadelphia, PA, 19104, USA.

Vid Prijatelj (V)

Department of Oral and Maxillofacial Surgery, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.

John P Kemp (JP)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD, 4072, Australia.
The University of Queensland Diamantina Institute, The University of Queensland, Brisbane, QLD, 4102, Australia.
MRC Integrative Epidemiology Unit, Bristol Medical School, University of Bristol, Bristol, BS8 2BN, UK.

Chen Shochat-Carvalho (C)

Azrieli Faculty of Medicine, Bar-Ilan University, Safed, 1311502, Israel.

Katerina Trajanoska (K)

Department of Internal Medicine, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.
Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.

Carol Wang (C)

School of Women's and Infants' Health, University of Western Australia, Crawley, WA, 6009, Australia.

Raimo Joro (R)

Institute of Biomedicine, Physiology, University of Eastern Finland, Kuopio, 70211, Finland.

Tavia E Evans (TE)

Department of Clinical Genetics, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.
Department of Radiology & Nuclear Medicine, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.

Katharina E Schraut (KE)

Centre for Global Health Research, Usher Institute, University of Edinburgh, Edinburgh, EH16 4UX, Scotland.
Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, EH8 9AG, Scotland.

Ruifang Li-Gao (R)

Department of Clinical Epidemiology, Leiden University Medical Centre, 2333 ZA, Leiden, The Netherlands.

Tarunveer S Ahluwalia (TS)

COPSAC, Copenhagen Prospective Studies on Asthma in Childhood, Herlev and Gentofte Hospital, University of Copenhagen, Copenhagen, 2820, Denmark.
Steno Diabetes Center Copenhagen, Herlev, 2820, Denmark.
The Bioinformatics Center, Department of Biology, University of Copenhagen, Copenhagen, 2200, Denmark.

M Carola Zillikens (MC)

Department of Internal Medicine, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.

Kun Zhu (K)

Department of Endocrinology and Diabetes, Sir Charles Gairdner Hospital, Nedlands, WA, 6009, Australia.
Medical School, University of Western Australia, Perth, WA, 6009, Australia.

Dennis O Mook-Kanamori (DO)

Department of Clinical Epidemiology, Leiden University Medical Centre, 2333 ZA, Leiden, The Netherlands.
Department of Public Health and Primary Care, Leiden University Medical Centre, 2333 ZA, Leiden, The Netherlands.

Daniel S Evans (DS)

California Pacific Medical Center Research Institute, San Francisco, CA, 94107, USA.

Maria Nethander (M)

Bioinformatics Core Facility, Sahlgrenska Academy, University of Gothenburg, 413 90, Gothenburg, Sweden.
Center for Bone and Arthritis Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, 413 90, Gothenburg, Sweden.

Maria J Knol (MJ)

Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.

Gudmar Thorleifsson (G)

deCODE Genetics/Amgen, Reykjavik, IC-101, Iceland.

Ivana Prokic (I)

Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.

Babette Zemel (B)

Department of Pediatrics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
Division of GI, Hepatology, and Nutrition, Children's Hospital of Philadelphia, Philadelphia, PA, 19104, USA.

Linda Broer (L)

Department of Internal Medicine, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.

Fiona E McGuigan (FE)

Clinical and Molecular Osteoporosis Research Unit, Department of Clinical Sciences Malmö, Lund University, 205 02, Malmö, Sweden.

Natasja M van Schoor (NM)

Department of Epidemiology and Data Science, Amsterdam UMC, 1081 HV, Amsterdam, The Netherlands.

Sjur Reppe (S)

Department of Plastic and Reconstructive Surgery, Oslo University Hospital, 0372, Oslo, Norway.
Department of Medical Biochemistry, Oslo University Hospital, 0372, Oslo, Norway.
Unger-Vetlesen Institute, Lovisenberg Diaconal Hospital, 0456, Oslo, Norway.

Mikolaj A Pawlak (MA)

Department of Clinical Genetics, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.
Department of Neurology, Poznan University of Medical Sciences, 61-701, Poznan, Poland.

Stuart H Ralston (SH)

Centre for Genomic and Experimental Medicine, Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, EH4 2XU, Scotland.

Nathalie van der Velde (N)

Department of Internal Medicine, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.
Department of Geriatric Medicine, Amsterdam Public Health Research Institute, Amsterdam UMC, 1105 AZ, Amsterdam, The Netherlands.

Mattias Lorentzon (M)

Center for Bone and Arthritis Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, 413 90, Gothenburg, Sweden.
Mary MacKillop Institute for Health Research, Australian Catholic University, Melbourne, VIC, 3000, Australia.

Kari Stefansson (K)

deCODE Genetics/Amgen, Reykjavik, IC-101, Iceland.

Hieab H H Adams (HHH)

Department of Clinical Genetics, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.
Department of Radiology & Nuclear Medicine, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.
Latin American Brain Health (BrainLat), Universidad Adolfo Ibáñez, Santiago, Chile.

Scott G Wilson (SG)

Department of Endocrinology and Diabetes, Sir Charles Gairdner Hospital, Nedlands, WA, 6009, Australia.
School of Biomedical Sciences, University of Western Australia, Nedlands, WA, 6009, Australia.
Department of Twin Research & Genetic Epidemiology, King's College London, London, SE1 7EH, UK.

M Arfan Ikram (MA)

Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.

John P Walsh (JP)

Department of Endocrinology and Diabetes, Sir Charles Gairdner Hospital, Nedlands, WA, 6009, Australia.
Medical School, University of Western Australia, Perth, WA, 6009, Australia.

Timo A Lakka (TA)

Institute of Biomedicine, Physiology, University of Eastern Finland, Kuopio, 70211, Finland.
Kuopio Research Institute of Exercise Medicine, Kuopio, 70100, Finland.
Department of Clinical Physiology and Nuclear Medicine, University of Eastern Finland, Kuopio, 70210, Finland.

Kaare M Gautvik (KM)

Unger-Vetlesen Institute, Lovisenberg Diaconal Hospital, 0456, Oslo, Norway.

James F Wilson (JF)

Centre for Global Health Research, Usher Institute, University of Edinburgh, Edinburgh, EH16 4UX, Scotland.
MRC Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, Edinburgh, EH4 2XU, Scotland.

Eric S Orwoll (ES)

Department of Public Health & Preventive Medicine, Oregon Health & Science University, Portland, OR, OR97239, USA.

Cornelia M van Duijn (CM)

Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.

Klaus Bønnelykke (K)

COPSAC, Copenhagen Prospective Studies on Asthma in Childhood, Herlev and Gentofte Hospital, University of Copenhagen, Copenhagen, 2820, Denmark.

Andre G Uitterlinden (AG)

Department of Internal Medicine, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.

Unnur Styrkársdóttir (U)

deCODE Genetics/Amgen, Reykjavik, IC-101, Iceland.

Kristina E Akesson (KE)

Clinical and Molecular Osteoporosis Research Unit, Department of Clinical Sciences Malmö, Lund University, 205 02, Malmö, Sweden.
Department of Orthopedics Malmö, Skåne University Hospital, S-21428, Malmö, Sweden.

Timothy D Spector (TD)

Department of Twin Research & Genetic Epidemiology, King's College London, London, SE1 7EH, UK.

Jonathan H Tobias (JH)

MRC Integrative Epidemiology Unit, Bristol Medical School, University of Bristol, Bristol, BS8 2BN, UK.
Musculoskeletal Research Unit, Translational Health Sciences, Bristol Medical School, Bristol, BS10 5NB, UK.

Claes Ohlsson (C)

Center for Bone and Arthritis Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, 413 90, Gothenburg, Sweden.
Department of Drug Treatment, Sahlgrenska University Hospital, Region Västra Götaland, SE-413 45, Gothenburg, Sweden.

Janine F Felix (JF)

The Generation R Study Group, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.
Department of Pediatrics, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.

Hans Bisgaard (H)

COPSAC, Copenhagen Prospective Studies on Asthma in Childhood, Herlev and Gentofte Hospital, University of Copenhagen, Copenhagen, 2820, Denmark.

Struan F A Grant (SFA)

Division of Human Genetics, Children's Hospital of Philadelphia, Philadelphia, PA, 19104, USA.
Department of Pediatrics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
Division of Endocrinology, The Children's Hospital of Philadelphia, Philadelphia, PA, 19104, USA.

J Brent Richards (JB)

Department of Twin Research & Genetic Epidemiology, King's College London, London, SE1 7EH, UK.
Lady Davis Institute, Jewish General Hospital, Montreal, H3T 1E2, QC, Canada.

David M Evans (DM)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD, 4072, Australia.
The University of Queensland Diamantina Institute, The University of Queensland, Brisbane, QLD, 4102, Australia.
MRC Integrative Epidemiology Unit, Bristol Medical School, University of Bristol, Bristol, BS8 2BN, UK.

Bram van der Eerden (B)

Department of Internal Medicine, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.

Jeroen van de Peppel (J)

Department of Internal Medicine, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands.

Cheryl Ackert-Bicknell (C)

Department of Orthopedics, University of Colorado, Aurora, CO, 80045, USA.

David Karasik (D)

Azrieli Faculty of Medicine, Bar-Ilan University, Safed, 1311502, Israel.
Marcus Institute for Aging Research, Hebrew SeniorLife, Roslindale, MA, 02131, USA.

Erika Kague (E)

The School of Physiology, Pharmacology and Neuroscience, Biomedical Sciences, University of Bristol, Bristol, BS8 1TD, UK.

Fernando Rivadeneira (F)

Department of Oral and Maxillofacial Surgery, Erasmus MC, University Medical Center Rotterdam, 3000 CA, Rotterdam, The Netherlands. f.rivadeneira@erasmusmc.nl.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH