The WNT1


Journal

Bone research
ISSN: 2095-4700
Titre abrégé: Bone Res
Pays: China
ID NLM: 101608652

Informations de publication

Date de publication:
10 Nov 2021
Historique:
received: 06 11 2020
accepted: 27 06 2021
revised: 28 05 2021
entrez: 11 11 2021
pubmed: 12 11 2021
medline: 12 11 2021
Statut: epublish

Résumé

The recent identification of homozygous WNT1 mutations in individuals with osteogenesis imperfecta type XV (OI-XV) has suggested that WNT1 is a key ligand promoting the differentiation and function of bone-forming osteoblasts. Although such an influence was supported by subsequent studies, a mouse model of OI-XV remained to be established. Therefore, we introduced a previously identified disease-causing mutation (G177C) into the murine Wnt1 gene. Homozygous Wnt1

Identifiants

pubmed: 34759273
doi: 10.1038/s41413-021-00170-0
pii: 10.1038/s41413-021-00170-0
pmc: PMC8580994
doi:

Types de publication

Journal Article

Langues

eng

Pagination

48

Subventions

Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : YO 299/1-1
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : SE2373/1-1
Organisme : China Scholarship Council (CSC)
ID : not applicable
Organisme : EC | Seventh Framework Programme (EC Seventh Framework Programm)
ID : 602300
Organisme : EC | Seventh Framework Programme (EC Seventh Framework Programm)
ID : 602300
Organisme : Bundesministerium für Bildung und Forschung (Federal Ministry of Education and Research)
ID : DIMEOS

Informations de copyright

© 2021. The Author(s).

Références

Compston, J. E., McClung, M. R. & Leslie, W. D. Osteoporosis. Lancet 393, 364–376 (2019).
pubmed: 30696576
Khosla, S. & Hofbauer, L. C. Osteoporosis treatment: recent developments and ongoing challenges. Lancet Diabetes Endocrinol. 5, 898–907 (2017).
pubmed: 28689769 pmcid: 5798872 doi: 10.1016/S2213-8587(17)30188-2
Saag, K. G. et al. Romosozumab or alendronate for fracture prevention in women with osteoporosis. N. Engl. J. Med. 377, 1417–1427 (2017).
pubmed: 28892457 doi: 10.1056/NEJMoa1708322
Baron, R. & Kneissel, M. WNT signaling in bone homeostasis and disease: from human mutations to treatments. Nat. Med. 19, 179–192 (2013).
pubmed: 23389618 doi: 10.1038/nm.3074
Little, R. D. et al. A mutation in the LDL receptor-related protein 5 gene results in the autosomal dominant high-bone-mass trait. Am. J. Hum. Genet. 70, 11–19 (2002).
pubmed: 11741193 doi: 10.1086/338450
Balemans, W. et al. Increased bone density in sclerosteosis is due to the deficiency of a novel secreted protein (SOST). Hum. Mol. Genet. 10, 537–543 (2001).
pubmed: 11181578 doi: 10.1093/hmg/10.5.537
Li, X. et al. Sclerostin binds to LRP5/6 and antagonizes canonical Wnt signaling. J. Biol. Chem. 280, 19883–19887 (2005).
pubmed: 15778503 doi: 10.1074/jbc.M413274200
Semenov, M., Tamai, K. & He, X. SOST is a ligand for LRP5/LRP6 and a Wnt signaling inhibitor. J. Biol. Chem. 280, 26770–26775 (2005).
pubmed: 15908424 doi: 10.1074/jbc.M504308200
Laine, C. M. et al. WNT1 mutations in early-onset osteoporosis and osteogenesis imperfecta. N. Engl. J. Med. 368, 1809–1816 (2013).
pubmed: 23656646 pmcid: 3709450 doi: 10.1056/NEJMoa1215458
Pyott, S. M. et al. WNT1 mutations in families affected by moderately severe and progressive recessive osteogenesis imperfecta. Am. J. Hum. Genet. 92, 590–597 (2013).
pubmed: 23499310 pmcid: 3617391 doi: 10.1016/j.ajhg.2013.02.009
Keupp, K. et al. Mutations in WNT1 cause different forms of bone fragility. Am. J. Hum. Genet. 92, 565–574 (2013).
pubmed: 23499309 pmcid: 3617378 doi: 10.1016/j.ajhg.2013.02.010
Fahiminiya, S. et al. Mutations in WNT1 are a cause of osteogenesis imperfecta. J. Med. Genet. 50, 345–348 (2013).
pubmed: 23434763 doi: 10.1136/jmedgenet-2013-101567
Thomas, K. R. & Capecchi, M. R. Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature 346, 847–850 (1990).
pubmed: 2202907 doi: 10.1038/346847a0
McMahon, A. P. & Bradley, A. The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 62, 1073–1085 (1990).
pubmed: 2205396 doi: 10.1016/0092-8674(90)90385-R
Joeng, K. S. et al. The swaying mouse as a model of osteogenesis imperfecta caused by WNT1 mutations. Hum. Mol. Genet. 23, 4035–4042 (2014).
pubmed: 24634143 pmcid: 4082367 doi: 10.1093/hmg/ddu117
Joeng, K. S. et al. Osteocyte-specific WNT1 regulates osteoblast function during bone homeostasis. J. Clin. Invest. 127, 2678–2688 (2017).
pubmed: 28628032 pmcid: 5490765 doi: 10.1172/JCI92617
Wang, F. et al. Mesenchymal cell-derived juxtacrine Wnt1 signaling regulates osteoblast activity and osteoclast differentiation. J. Bone Miner. Res. 34, 1129–1142 (2019).
pubmed: 30690791 doi: 10.1002/jbmr.3680
Luther, J. et al. Wnt1 is an Lrp5-independent bone-anabolic Wnt ligand. Sci. Transl. Med. 10, eaau7137 (2018).
Yorgan, T. A. et al. Mice carrying a ubiquitous R235W mutation of Wnt1 display a bone-specific phenotype. J. Bone Miner. Res. 35, 1726–1737 (2020).
Palomo, T., Vilaca, T. & Lazaretti-Castro, M. Osteogenesis imperfecta: diagnosis and treatment. Curr. Opin. Endocrinol. Diabetes Obes. 24, 381–388 (2017).
pubmed: 28863000 doi: 10.1097/MED.0000000000000367
Thomas, K. R., Musci, T. S., Neumann, P. E. & Capecchi, M. R. Swaying is a mutant allele of the proto-oncogene Wnt-1. Cell 67, 969–976 (1991).
pubmed: 1835670 doi: 10.1016/0092-8674(91)90369-A
Kelly, N. H., Schimenti, J. C., Ross, F. P. & van der Meulen, M. C. Transcriptional profiling of cortical versus cancellous bone from mechanically-loaded murine tibiae reveals differential gene expression. Bone 86, 22–29 (2016).
pubmed: 26876048 pmcid: 4833881 doi: 10.1016/j.bone.2016.02.007
Yorgan, T. A. et al. Mice lacking plastin-3 display a specific defect of cortical bone acquisition. Bone 130, 115062 (2020).
pubmed: 31678489 doi: 10.1016/j.bone.2019.115062
Keller, H. & Kneissel, M. SOST is a target gene for PTH in bone. Bone 37, 148–158 (2005).
pubmed: 15946907 doi: 10.1016/j.bone.2005.03.018
Silva, B. C. & Bilezikian, J. P. Parathyroid hormone: anabolic and catabolic actions on the skeleton. Curr. Opin. Pharmacol. 22, 41–50 (2015).
pubmed: 25854704 pmcid: 5407089 doi: 10.1016/j.coph.2015.03.005
Heckt, T. et al. Parathyroid hormone induces expression and proteolytic processing of Rankl in primary murine osteoblasts. Bone 92, 85–93 (2016).
pubmed: 27554428 doi: 10.1016/j.bone.2016.08.016
Yorgan, T. A. et al. The anti-osteoanabolic function of sclerostin is blunted in mice carrying a high bone mass mutation of Lrp5. J. Bone Miner. Res. 30, 1175–1183 (2015).
pubmed: 25640331 doi: 10.1002/jbmr.2461
Albers, J. et al. Control of bone formation by the serpentine receptor Frizzled-9. J. Cell Biol. 192, 1057–1072 (2011).
pubmed: 21402791 pmcid: 3063134 doi: 10.1083/jcb.201008012
Richards, J. S. et al. Either Kras activation or Pten loss similarly enhance the dominant-stable CTNNB1-induced genetic program to promote granulosa cell tumor development in the ovary and testis. Oncogene 31, 1504–1520 (2012).
pubmed: 21860425 doi: 10.1038/onc.2011.341
Takahashi, M. et al. Isolation of a novel human gene, APCDD1, as a direct target of the beta-Catenin/T-cell factor 4 complex with probable involvement in colorectal carcinogenesis. Cancer Res. 62, 5651–5656 (2002).
pubmed: 12384519
Schneider, A. J., Branam, A. M. & Peterson, R. E. Intersection of AHR and Wnt signaling in development, health, and disease. Int. J. Mol. Sci. 15, 17852–17885 (2014).
pubmed: 25286307 pmcid: 4227194 doi: 10.3390/ijms151017852
Li, Z. Q. et al. Cyr61/CCN1 is regulated by Wnt/beta-catenin signaling and plays an important role in the progression of hepatocellular carcinoma. PLoS One 7, e35754 (2012).
pubmed: 22540002 pmcid: 3335098 doi: 10.1371/journal.pone.0035754
Gerbaix, M., Vico, L., Ferrari, S. L. & Bonnet, N. Periostin expression contributes to cortical bone loss during unloading. Bone 71, 94–100 (2015).
pubmed: 25445447 doi: 10.1016/j.bone.2014.10.011
Marini, J. C. et al. Osteogenesis imperfecta. Nat. Rev. Dis. Prim. 3, 17052 (2017).
pubmed: 28820180 doi: 10.1038/nrdp.2017.52
Marini, J. C., Reich, A. & Smith, S. M. Osteogenesis imperfecta due to mutations in non-collagenous genes: lessons in the biology of bone formation. Curr. Opin. Pediatr. 26, 500–507 (2014).
pubmed: 25007323 pmcid: 4183132 doi: 10.1097/MOP.0000000000000117
Schulze, J. et al. Negative regulation of bone formation by the transmembrane Wnt antagonist Kremen-2. PLoS One 5, e10309 (2010).
pubmed: 20436912 pmcid: 2860505 doi: 10.1371/journal.pone.0010309
Glatt, V., Canalis, E., Stadmeyer, L. & Bouxsein, M. L. Age-related changes in trabecular architecture differ in female and male C57BL/6J mice. J. Bone Miner. Res. 22, 1197–1207 (2007).
pubmed: 17488199 doi: 10.1359/jbmr.070507
Moverare-Skrtic, S. et al. Osteoblast-derived WNT16 represses osteoclastogenesis and prevents cortical bone fragility fractures. Nat. Med. 20, 1279–1288 (2014).
pubmed: 25306233 pmcid: 4392888 doi: 10.1038/nm.3654
van Dijk, F. S. et al. PLS3 mutations in X-linked osteoporosis with fractures. N. Engl. J. Med. 369, 1529–1536 (2013).
pubmed: 24088043 doi: 10.1056/NEJMoa1308223
Vahle, J. L. et al. Skeletal changes in rats given daily subcutaneous injections of recombinant human parathyroid hormone (1-34) for 2 years and relevance to human safety. Toxicol. Pathol. 30, 312–321 (2002).
pubmed: 12051548 doi: 10.1080/01926230252929882
Joiner, D. M., Ke, J., Zhong, Z., Xu, H. E. & Williams, B. O. LRP5 and LRP6 in development and disease. Trends Endocrinol. Metab. 24, 31–39 (2013).
pubmed: 23245947 pmcid: 3592934 doi: 10.1016/j.tem.2012.10.003
Bonnet, N., Garnero, P. & Ferrari, S. Periostin action in bone. Mol. Cell. Endocrinol. 432, 75–82 (2016).
pubmed: 26721738 doi: 10.1016/j.mce.2015.12.014
Bonnet, N. et al. Periostin deficiency increases bone damage and impairs injury response to fatigue loading in adult mice. PLoS One 8, e78347 (2013).
pubmed: 24167618 pmcid: 3805534 doi: 10.1371/journal.pone.0078347
Tashima, T., Nagatoishi, S., Sagara, H., Ohnuma, S. & Tsumoto, K. Osteomodulin regulates diameter and alters shape of collagen fibrils. Biochem. Biophys. Res. Commun. 463, 292–296 (2015).
pubmed: 26003732 doi: 10.1016/j.bbrc.2015.05.053
Tashima, T. et al. Molecular basis for governing the morphology of type-I collagen fibrils by Osteomodulin. Commun. Biol. 1, 33 (2018).
pubmed: 30271919 pmcid: 6123635 doi: 10.1038/s42003-018-0038-2
Gatti, D. et al. Intravenous bisphosphonate therapy increases radial width in adults with osteogenesis imperfecta. J. Bone Miner. Res. 20, 1323–1326 (2005).
pubmed: 16007328 doi: 10.1359/JBMR.050312
Zimmermann, E. A. et al. Mechanical competence and bone quality develop during skeletal growth. J. Bone Miner. Res. 34, 1461–1472 (2019).
pubmed: 30913317 doi: 10.1002/jbmr.3730
Albers, J. et al. Canonical Wnt signaling inhibits osteoclastogenesis independent of osteoprotegerin. J. Cell Biol. 200, 537–549 (2013).
pubmed: 23401003 pmcid: 3575535 doi: 10.1083/jcb.201207142
Bouxsein, M. L. et al. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J. Bone Miner. Res. 25, 1468–1486 (2010).
doi: 10.1002/jbmr.141 pubmed: 20533309
Dempster, D. W. et al. Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J. Bone Miner. Res. 28, 2–17 (2013).
pubmed: 23197339 doi: 10.1002/jbmr.1805
Rueden, C. T. et al. ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinforma. 18, 529 (2017).
doi: 10.1186/s12859-017-1934-z
Busse, B. et al. Decrease in the osteocyte lacunar density accompanied by hypermineralized lacunar occlusion reveals failure and delay of remodeling in aged human bone. Aging Cell 9, 1065–1075 (2010).
pubmed: 20874757 doi: 10.1111/j.1474-9726.2010.00633.x
Koehne, T. et al. Trends in trabecular architecture and bone mineral density distribution in 152 individuals aged 30-90 years. Bone 66, 31–38 (2014).
pubmed: 24859568 doi: 10.1016/j.bone.2014.05.010

Auteurs

Nele Vollersen (N)

Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany.

Wenbo Zhao (W)

Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany.

Tim Rolvien (T)

Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany.

Fabiola Lange (F)

Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany.

Felix Nikolai Schmidt (FN)

Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany.

Stephan Sonntag (S)

PolyGene AG, 8153, Rümlang, Switzerland.
ETH Phenomics Center (EPIC), ETH Zürich, 8092, Zürich, Switzerland.

Doron Shmerling (D)

PolyGene AG, 8153, Rümlang, Switzerland.

Simon von Kroge (S)

Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany.

Kilian Elia Stockhausen (KE)

Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany.

Ahmed Sharaf (A)

Neuronal and Cellular Signal Transduction, Center for Molecular Neurobiology Hamburg (ZMNH), University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany.

Michaela Schweizer (M)

Center for Molecular Neurobiology Hamburg (ZMNH), University Medical Center, Hamburg-Eppendorf, 20246, Hamburg, Germany.

Meliha Karsak (M)

Neuronal and Cellular Signal Transduction, Center for Molecular Neurobiology Hamburg (ZMNH), University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany.

Björn Busse (B)

Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany.

Ernesto Bockamp (E)

Institute for Translational Immunology and Research Center for Immunotherapy, University Medical Center, Johannes Gutenberg University, D 55131, Mainz, Germany.

Oliver Semler (O)

Faculty of Medicine and University Hospital Cologne, Department of Pediatrics, University of Cologne, 50937, Cologne, Germany.

Michael Amling (M)

Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany.

Ralf Oheim (R)

Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany.

Thorsten Schinke (T)

Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany. schinke@uke.de.

Timur Alexander Yorgan (TA)

Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany. t.yorgan@uke.de.

Classifications MeSH