G protein-coupled receptor 56 and collagen III, a receptor-ligand pair, regulates cortical development and lamination
Open accessAbstract
GPR56, an orphan G protein-coupled receptor (GPCR) from the family of adhesion GPCRs, plays an indispensable role in cortical development and lamination. Mutations in the GPR56 gene cause a malformed cerebral cortex in both humans and mice that resembles cobblestone lissencephaly, which is characterized by overmigration of neurons beyond the pial basement membrane. However, the molecular mechanisms through which GPR56 regulates cortical development remain elusive due to the unknown status of its ligand. Here we identify collagen, type III, alpha-1 (gene symbol Col3a1 ) as the ligand of GPR56 through an in vitro biotinylation/proteomics approach. Further studies demonstrated that Col3a1 null mutant mice exhibit overmigration of neurons beyond the pial basement membrane and a cobblestone-like cortical malformation similar to the phenotype seen in Gpr56 null mutant mice. Functional studies suggest that the interaction of collagen III with its receptor GPR56 inhibits neural migration in vitro. As for intracellular signaling, GPR56 couples to the Gα 12/13 family of G proteins and activates RhoA pathway upon ligand binding. Thus, collagen III regulates the proper lamination of the cerebral cortex by acting as the major ligand of GPR56 in the developing brain.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
GPR56 encodes an adhesion heterotrimeric G protein-coupled receptor that is highly expressed in cortical progenitors and binds extracellular matrix proteins.
“GPR56 encodes an adhesion heterotrimeric guanine nucleotide–binding protein (G protein)–coupled receptor that is highly expressed in cortical progenitors (7, 16) and binds extracellular matrix proteins (17).”
From Evolutionarily Dynamic Alternative Splicing of <i>GPR56</i> Regulates Regional Cerebral Cortical Patterning (2014) · cites this paper as [17]
GPR56 likely influences progenitor proliferation by stabilizing the basal process of radial neuroepithelial progenitors.
“GPR56 likely influences progenitor proliferation by stabilizing the basal process of radial neuroepithelial progenitors”
From Evolutionarily Dynamic Alternative Splicing of <i>GPR56</i> Regulates Regional Cerebral Cortical Patterning (2014) · cites this paper as [17]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Regulation of the small GTP‐binding protein Rho by cell adhesion and the cytoskeleton
Ren, X. D., Kiosses, W. B., & Schwartz, M. A. (1999) · The EMBO Journal · doi:10.1093/emboj/18.3.578 · Cited by 1,573 · see citing works
Englund, C., Fink, A., Lau, C., Pham, D., Daza, R. A. M., Bulfone, A., Kowalczyk, T., & Hevner, R. F. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2899-04.2005 · Cited by 1,261 · see citing works
Development of the human cerebral cortex: Boulder Committee revisited
Bystron, I., Blakemore, C., & Rakic, P. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2252 · Cited by 977 · see citing works
C ELL M IGRATION IN THE F OREBRAIN
Marín, Ó., & Rubenstein, J. L. R. (2003) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131058 · Cited by 917 · see citing works
Perlecan Maintains the Integrity of Cartilage and Some Basement Membranes
Costell, M., Gustafsson, E., Aszódi, A., Mörgelin, M., Bloch, W., Hunziker, E. B., Addicks, K., Timpl, R., & Fässler, R. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.147.5.1109 · Cited by 672 · see citing works
Mechanisms of Cortical Development: A View From Mutations in Mice
Caviness, V. S., & RAKIC, P. T. (1978) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.01.030178.001501 · Cited by 653 · see citing works
Trekking across the Brain: The Journey of Neuronal Migration
Ayala, R., Shu, T., & Tsai, L.-H. (2007) · Cell · doi:10.1016/j.cell.2006.12.021 · Cited by 620 · see citing works
Liu, X., Wu, H., Byrne, M., Krane, S., & Jaenisch, R. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.5.1852 · Cited by 614 · see citing works
Heritable Diseases of Collagen
Prockop, D. J., & Kivirikko, K. I. (1984) · New England Journal of Medicine · doi:10.1056/nejm198408093110606 · Cited by 566 · see citing works
Graus-Porta, D., Blaess, S., Senften, M., Littlewood-Evans, A., Damsky, C. H., Huang, Z., Orban, P. C., Klein, R., Schittny, J. C., & Müller, U. (2001) · Neuron · doi:10.1016/s0896-6273(01)00374-9 · Cited by 559 · see citing works
Nieto, M., Monuki, E. S., Tang, H., Imitola, J., Haubst, N., Khoury, S. J., Cunningham, J., Götz, M., & Walsh, C. A. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20322 · Cited by 548 · see citing works
Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion
Narumiya, S., Tanji, M., & Ishizaki, T. (2009) · Cancer and Metastasis Reviews · doi:10.1007/s10555-008-9170-7 · Cited by 530 · see citing works
G Protein-Coupled Receptor-Dependent Development of Human Frontal Cortex
Piao, X., Hill, R. S., Bodell, A., Chang, B. S., Basel-Vanagaite, L., Straussberg, R., Dobyns, W. B., Qasrawi, B., Winter, R. M., Innes, A. M., et al. (2004) · Science · doi:10.1126/science.1092780 · Cited by 517 · see citing works
Self-citationFezl Is Required for the Birth and Specification of Corticospinal Motor Neurons
Molyneaux, B. J., Arlotta, P., Hirata, T., Hibi, M., & Macklis, J. D. (2005) · Neuron · doi:10.1016/j.neuron.2005.08.030 · Cited by 481 · see citing works
Breaching the basement membrane: who, when and how?
Rowe, R. G., & Weiss, S. J. (2008) · Trends in Cell Biology · doi:10.1016/j.tcb.2008.08.007 · Cited by 443 · see citing works
Mutations in the β-tubulin gene TUBB2B result in asymmetrical polymicrogyria
Jaglin, X. H., Poirier, K., Saillour, Y., Buhler, E., Tian, G., Bahi‐Buisson, N., Fallet‐Bianco, C., Tuy, F. P. D., Kong, X., Bomont, P., et al. (2009) · Nature Genetics · doi:10.1038/ng.380 · Cited by 380 · see citing works
Ehlers-Danlos syndrome type IV
Germain, D. P. (2007) · Orphanet Journal of Rare Diseases · doi:10.1186/1750-1172-2-32 · Cited by 374 · see citing works
New Directions in Neuronal Migration
Hatten, M. E. (2002) · Science · doi:10.1126/science.1074572 · Cited by 321 · see citing works
Beggs, H. E., Schahin-Reed, D., Zang, K., Goebbels, S., Nave, K., Gorski, J. A., Jones, K. R., Sretavan, D. W., & Reichardt, L. F. (2003) · Neuron · doi:10.1016/s0896-6273(03)00666-4 · Cited by 305 · see citing works
Essential role of α6 integrins in cortical and retinal lamination
Georges‐Labouesse, E., Mark, M. P., Messaddeq, N., & Gansmüller, A. (1998) · Current Biology · doi:10.1016/s0960-9822(98)70402-6 · Cited by 304 · see citing works
Henstridge, C. M., Balenga, N. A. B., Ford, L., Ross, R. A., Waldhoer, M., & Irving, A. J. (2008) · The FASEB Journal · doi:10.1096/fj.08-108670 · Cited by 285 · see citing works
Xu, L., Begum, S., Hearn, J., & Hynes, R. O. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602681103 · Cited by 278 · see citing works
GPR56 Regulates Pial Basement Membrane Integrity and Cortical Lamination
Li, S., Jin, Z., Koirala, S., Bu, L., Xu, L., Hynes, R. O., Walsh, C. A., Corfas, G., & Piao, X. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.0853-08.2008 · Cited by 241 · see citing works
Self-citationThe multipolar stage and disruptions in neuronal migration
LoTurco, J. J., & Bai, J. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.05.006 · Cited by 231 · see citing works
Arcangelis, A. D., Mark, M. P., Kreidberg, J. A., Sorokin, L. M., & Georges‐Labouesse, E. (1999) · Development · doi:10.1242/dev.126.17.3957 · Cited by 231 · see citing works
Ena/VASP Is Required for Neuritogenesis in the Developing Cortex
Kwiatkowski, A. V., Rubinson, D. A., Dent, E. W., van Veen, J. E., Leslie, J. D., Zhang, J., Mebane, L. M., Philippar, U., Pinheiro, E. M., Burds, A. A., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.09.008 · Cited by 212 · see citing works
Little, K. D., Hemler, M. E., & Stipp, C. S. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-12-0886 · Cited by 211 · see citing works
Iguchi, T., Sakata, K., Yoshizaki, K., Tago, K., Mizuno, N., & Itoh, H. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m708919200 · Cited by 195 · see citing works
Schwarze, U., Schievink, W. I., Petty, E., Jaff, M. R., Babovic-Vuksanovic, D., Cherry, K. J., Pepin, M., & Byers, P. H. (2001) · The American Journal of Human Genetics · doi:10.1086/324123 · Cited by 184 · see citing works
A mutation in the gene for type III procollagen (COL3A1) in a family with aortic aneurysms.
Kontusaari, S., Tromp, G. C., Kuivaniemi, H., Romanic, A. M., & Prockop, D. J. (1990) · Journal of Clinical Investigation · doi:10.1172/jci114863 · Cited by 182 · see citing works
GPR56 is a GPCR that is overexpressed in gliomas and functions in tumor cell adhesion
Shashidhar, S., Lorente, G., Nagavarapu, U., Nelson, A., Kuo, J., Cummins, J., Nikolich, K., Urfer, R., & Foehr, E. D. (2005) · Oncogene · doi:10.1038/sj.onc.1208395 · Cited by 172 · see citing works
Distinct Recognition of Collagen Subtypes by α1β1 and α2β1Integrins
Nykvist, P., Tu, H., Ivaska, J., Käpylä, J., Pihlajaniemi, T. A., & Heino, J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.11.8255 · Cited by 162 · see citing works
G12/G13-mediated signalling in mammalian physiology and disease
Worzfeld, T., Wettschureck, N., & Offermanns, S. (2008) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2008.08.002 · Cited by 152 · see citing works
Genotype–phenotype analysis of human frontoparietal polymicrogyria syndromes
Piao, X., Chang, B. S., Bodell, A., Woods, K., Ben‐Zeev, B., Topçu, M., Guerrini, R., Goldberg‐Stern, H., Sztriha, L., Dobyns, W. B., et al. (2005) · Annals of Neurology · doi:10.1002/ana.20616 · Cited by 151 · see citing works
Self-citationBahi-Buisson, N., Poirier, K., Boddaert, N., Fallet-Bianco, C., Specchio, N., Bertini, E., Caglayan, O., Lascelles, K., Elie, C., Rambaud, J., et al. (2010) · Brain · doi:10.1093/brain/awq259 · Cited by 144 · see citing works
Chang, B. S., Piao, X., Bodell, A., Basel‐Vanagaite, L., Straussberg, R., Dobyns, W. B., Qasrawi, B., Winter, R. M., Innes, A. M., Voït, T., et al. (2003) · Annals of Neurology · doi:10.1002/ana.10520 · Cited by 134 · see citing works
Self-citationSmooth, rough and upside-down neocortical development
Olson, E. C., & Walsh, C. A. (2002) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(02)00305-2 · Cited by 134 · see citing works
A Novel Binding Site in Collagen Type III for Integrins α1β1 and α2β1
Kim, J. K., Xu, Y., Xu, X., Keene, D. R., Gurusiddappa, S., Liang, X., Wary, K. K., & Höök, M. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m502431200 · Cited by 120 · see citing works
An Autosomal Recessive Form of Bilateral Frontoparietal Polymicrogyria Maps to Chromosome 16q12.2-21
Piao, X., Basel‐Vanagaite, L., Straussberg, R., Grant, P. E., Pugh, E., Doheny, K. F., Doan, B. Q., Hong, S. E., Shugart, Y. Y., & Walsh, C. A. (2002) · The American Journal of Human Genetics · doi:10.1086/339552 · Cited by 120 · see citing works
Self-citationDisease-associated mutations affect GPR56 protein trafficking and cell surface expression
Jin, Z., Tietjen, I., Bu, L., Liu‐Yesucevitz, L., Gaur, S. K., Walsh, C. A., & Piao, X. (2007) · Human Molecular Genetics · doi:10.1093/hmg/ddm144 · Cited by 120 · see citing works
Self-citationGPR56-Regulated Granule Cell Adhesion Is Essential for Rostral Cerebellar Development
Koirala, S., Jin, Z., Piao, X., & Corfas, G. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1182-09.2009 · Cited by 116 · see citing works
Self-citationMEKK4 Signaling Regulates Filamin Expression and Neuronal Migration
Sarkisian, M. R., Bartley, C. M., Chi, H., Nakamura, F., Hashimoto‐Torii, K., Torii, M., Flavell, R. A., & RAKIC, P. T. (2006) · Neuron · doi:10.1016/j.neuron.2006.10.024 · Cited by 115 · see citing works
Niewmierzycka, A., Mills, J., St‐Arnaud, R., Dedhar, S., & Reichardt, L. F. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1695-05.2005 · Cited by 115 · see citing works
Platelet-Activating Factor Receptor Stimulation Disrupts Neuronal MigrationIn Vitro
Bix, G. J., & Clark, G. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00307.1998 · Cited by 106 · see citing works
Stacey, M. A., Chang, G.-W., Sanos, S. L., Chittenden, L. R., Stubbs, L. J., Gordon, S., & Lin, H. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204306200 · Cited by 99 · see citing works
Zendman, A. J. W., Cornelissen, I. M. H. A., Weidle, U. H., Ruiter, D. J., & van Muijen, G. N. P. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)00230-6 · Cited by 86 · see citing works
Moers, A., Nürnberg, A., Goebbels, S., Wettschureck, N., & Offermanns, S. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00651-07 · Cited by 74 · see citing works
Microarray analysis of the developing cortex
Semeralul, M. O., Boutros, P. C., Likhodi, O., Okey, A. B., Tol, H. H. M. V., & Wong, A. H. C. (2006) · Journal of Neurobiology · doi:10.1002/neu.20302 · Cited by 45 · see citing works
Kuivaniemi, H., Tromp, G. C., Bergfeld, W. F., Kay, M., & Helm, T. N. (1995) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12320704 · Cited by 39 · see citing works
Genetics of disorders of cortical development
Gaitanis, J. N., & Walsh, C. A. (2004) · Neuroimaging Clinics of North America · doi:10.1016/j.nic.2004.03.007 · Cited by 33 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
A developmental and genetic classification for malformations of cortical development: update 2012
Barkovich, A. J., Guerrini, R., Kuzniecky, R., Jackson, G. D., & Dobyns, W. B. (2012) · Brain · doi:10.1093/brain/aws019 · Cited by 1,110 · see citing works
A guide to the composition and functions of the extracellular matrix
Karamanos, N. K., Theocharis, A. D., Piperigkou, Z., Manou, D., Passi, A. G., Skandalis, S. S., Vynios, D. H., Orian‐Rousseau, V., Ricard‐Blum, S., Schmelzer, C. E. H., et al. (2021) · FEBS Journal · doi:10.1111/febs.15776 · Cited by 1,100 · see citing works
The Concise Guide to PHARMACOLOGY 2013/14: G Protein‐Coupled Receptors
Alexander, S. P. H., Benson, H. E., Faccenda, E., Pawson, A. J., Sharman, J. L., Spedding, M., Peters, J. A., Harmar, A. J., & Collaborators, C. (2013) · British Journal of Pharmacology · doi:10.1111/bph.12445 · Cited by 555 · see citing works
International Union of Basic and Clinical Pharmacology. XCIV. Adhesion G Protein–Coupled Receptors
Hamann, J., Aust, G., Araç, D., Engel, F. B., Formstone, C. J., Fredriksson, R., Hall, R. A., Harty, B. L., Kirchhoff, C., Knapp, B., et al. (2015) · Pharmacological Reviews · doi:10.1124/pr.114.009647 · Cited by 489 · see citing works
Self-citationCerebral cortex expansion and folding: what have we learned?
Fernández, V., Llinares-Benadero, C., & Borrell, V. (2016) · The EMBO Journal · doi:10.15252/embj.201593701 · Cited by 357 · see citing works
Schwann Cell MyelinationPreprint
Salzer, J. L. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020529 · Cited by 365 · see citing works
Davenport, A. P., Alexander, S. P. H., Sharman, J. L., Pawson, A. J., Benson, H. E., Monaghan, A. E., Liew, W. C., Mpamhanga, C. P., Bonner, T. I., Neubig, R. R., et al. (2013) · Pharmacological Reviews · doi:10.1124/pr.112.007179 · Cited by 327 · see citing works
Reciprocal signalling by Notch–Collagen V–CALCR retains muscle stem cells in their niche
Baghdadi, M. B., Castel, D., Machado, L., Fukada, S., Birk, D. E., Relaix, F., Tajbakhsh, S., & Mourikis, P. (2018) · Nature · doi:10.1038/s41586-018-0144-9 · Cited by 299 · see citing works
Signaling pathways in cancer metabolism: mechanisms and therapeutic targets
You, M., Xie, Z., Zhang, N., Zhang, Y., Xiao, D., Liu, S., Zhuang, W., Li, L., & Tao, Y. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01442-3 · Cited by 297 · see citing works
Petersen, S. C., Luo, R., Liebscher, I., Giera, S., Jeong, S., Mogha, A., Ghidinelli, M., Feltri, M. L., Schöneberg, T., Piao, X., et al. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.057 · Cited by 283 · see citing works
Self-citationAdhesion G protein-coupled receptors are activated by exposure of a cryptic tethered agonist
Stoveken, H. M., HAJDUCZOK, A. G., Xu, L., & Tall, G. G. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421785112 · Cited by 278 · see citing works
Sticky Signaling—Adhesion Class G Protein–Coupled Receptors Take the Stage
Langenhan, T., Aust, G., & Hamann, J. (2013) · Science Signaling · doi:10.1126/scisignal.2003825 · Cited by 267 · see citing works
Bae, B.-I., Tietjen, I., Atabay, K. D., Evrony, G. D., Johnson, M. B., Asare, E., Wang, P. P., Murayama, A. Y., Im, K., Lisgo, S. N., et al. (2014) · Science · doi:10.1126/science.1244392 · Cited by 229 · see citing works
Self-citationAn atlas and functional analysis of G-protein coupled receptors in human islets of Langerhans
Amisten, S., Salehi, A. A., Rorsman, P., Jones, P. M., & Persaud, S. J. (2013) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.05.004 · Cited by 196 · see citing works
Type IV collagen is an activating ligand for the adhesion G protein–coupled receptor GPR126
Paavola, K. J., Sidik, H., Zuchero, J. B., Eckart, M. R., & Talbot, W. S. (2014) · Science Signaling · doi:10.1126/scisignal.2005347 · Cited by 187 · see citing works
Mogha, A., Benesh, A. E., Patra, C., Engel, F. B., Schöneberg, T., Liebscher, I., & Monk, K. R. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1809-13.2013 · Cited by 188 · see citing works
Mechanisms of adhesion G protein–coupled receptor activation
Vizurraga, A., Adhikari, R., Yeung, J., Yu, M., & Tall, G. G. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.rev120.007423 · Cited by 179 · see citing works
A splicing isoform of GPR56 mediates microglial synaptic refinement via phosphatidylserine binding
Li, T., Chiou, B., Gilman, C. K., Luo, R., Koshi, T., Yu, D., Oak, H. C., Giera, S., Johnson‐Venkatesh, E., Muthukumar, A. K., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2019104136 · Cited by 177 · see citing works
Self-citationSignals regulating myelination in peripheral nerves and the Schwann cell response to injury
Glenn, T. D., & Talbot, W. S. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.06.010 · Cited by 171 · see citing works
Malformations of Cortical Development and EpilepsyPreprint
Barkovich, A. J., Dobyns, W. B., & Guerrini, R. (2015) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a022392 · Cited by 160 · see citing works
The tethered peptide activation mechanism of adhesion GPCRs
Barros-Álvarez, X., Nwokonko, R. M., Vizurraga, A., Matzov, D., He, F., Papasergi-Scott, M. M., Robertson, M. J., Panova, O., Yardeni, E. H., Seven, A. B., et al. (2022) · Nature · doi:10.1038/s41586-022-04575-7 · Cited by 148 · see citing works
The adhesion GPCR Gpr56 regulates oligodendrocyte development via interactions with Gα12/13 and RhoA
Ackerman, S. D., Garcia, C. M., Piao, X., Gutmann, D. H., & Monk, K. R. (2015) · Nature Communications · doi:10.1038/ncomms7122 · Cited by 149 · see citing works
Self-citationOegema, R., Barakat, T. S., Wilke, M., Stouffs, K., Amrom, D., Aronica, E., Bahi‐Buisson, N., Conti, V., Fry, A. E., Geis, T., et al. (2020) · Nature Reviews Neurology · doi:10.1038/s41582-020-0395-6 · Cited by 147 · see citing works
Liver Immune Profiling Reveals Pathogenesis and Therapeutics for Biliary Atresia
Wang, J., Xu, Y., Chen, Z., Liang, J., Lin, Z., Liang, H., Xu, Y., Wu, Q., Guo, X., Nie, J., et al. (2020) · Cell · doi:10.1016/j.cell.2020.10.048 · Cited by 147 · see citing works
Malformations of cortical development
Desikan, R. S., & Barkovich, A. J. (2016) · Annals of Neurology · doi:10.1002/ana.24793 · Cited by 146 · see citing works
Giera, S., Luo, R., Ying, Y., Ackerman, S. D., Jeong, S.-J., Stoveken, H. M., Folts, C. J., Welsh, C. A., Tall, G. G., Stevens, B., et al. (2018) · eLife · doi:10.7554/elife.33385 · Cited by 145 · see citing works
Self-citationTethered peptide activation mechanism of the adhesion GPCRs ADGRG2 and ADGRG4
Xiao, P., Guo, S., Wen, X., He, Q., Lin, H., Huang, S.-M., Gou, L., Zhang, C., Yang, Z., Zhong, Y.-N., et al. (2022) · Nature · doi:10.1038/s41586-022-04590-8 · Cited by 145 · see citing works
Self-citationGiera, S., Deng, Y., Luo, R., Ackerman, S. D., Mogha, A., Monk, K. R., Ying, Y., Jeong, S., Makinodan, M., Bialas, A. R., et al. (2015) · Nature Communications · doi:10.1038/ncomms7121 · Cited by 141 · see citing works
Self-citationCortical organoids model early brain development disrupted by 16p11.2 copy number variants in autism
Urresti, J., Zhang, P., Losada, P. M., Yu, N., Negraes, P. D., Trujillo, C. A., Antaki, D., Amar, M., Chau, K. K., Pramod, A. B., et al. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01243-6 · Cited by 133 · see citing works
Adhesion G Protein-Coupled Receptors: Signaling, Pharmacology, and Mechanisms of Activation
Paavola, K. J., & Hall, R. A. (2012) · Molecular Pharmacology · doi:10.1124/mol.112.080309 · Cited by 134 · see citing works
Structural Basis for Regulation of GPR56/ADGRG1 by Its Alternatively Spliced Extracellular Domains
Salzman, G., Ackerman, S. D., Ding, C., Koide, A., Leon, K., Luo, R., Stoveken, H. M., Fernandez, C., Tall, G. G., Piao, X., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.08.022 · Cited by 128 · see citing works
Self-citationGenetics and mechanisms leading to human cortical malformations
Romero, D. M., Bahi‐Buisson, N., & Francis, F. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.09.031 · Cited by 126 · see citing works
Outside-in signaling – a brief review of GPCR signaling with a focus on theDrosophilaGPCR family
Hanlon, C. D., & Andrew, D. J. (2015) · Journal of Cell Science · doi:10.1242/jcs.175158 · Cited by 125 · see citing works
The Adhesion G Protein-Coupled Receptor GPR56/ADGRG1 Is an Inhibitory Receptor on Human NK Cells
Chang, G.-W., Hsiao, C., Peng, Y.-M., Braga, F. A. V., Kragten, N. A. M., Remmerswaal, E. B. M., van de Garde, M. D. B., Straussberg, R., König, G. M., Kostenis, E., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.053 · Cited by 121 · see citing works
G protein-coupled receptor 56 regulates mechanical overload-induced muscle hypertrophy
White, J. P., Wrann, C. D., Rao, R. R., Nair, S. K., Jedrychowski, M. P., You, J.-S., Martínez-Redondo, V., Gygi, S. P., Ruas, J. L., Hornberger, T. A., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1417898111 · Cited by 123 · see citing works
Self-citationSoft tissue mechanotransduction in wound healing and fibrosis
Wong, V., Longaker, M. T., & Gurtner, G. C. (2012) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2012.09.010 · Cited by 123 · see citing works
Wang, C., Brisson, B. K., Terajima, M., Li, Q., Hoxha, K., Han, B., Goldberg, A., Liu, X. S., Marcolongo, M. S., Enomoto‐Iwamoto, M., et al. (2019) · Matrix Biology · doi:10.1016/j.matbio.2019.10.001 · Cited by 123 · see citing works
Adhesion G protein-coupled receptors in nervous system development and disease
Langenhan, T., Piao, X., & Monk, K. R. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.86 · Cited by 115 · see citing works
Self-citationAdhesion G Protein–Coupled Receptors as Drug Targets
Purcell, R. H., & Hall, R. A. (2017) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010617-052933 · Cited by 120 · see citing works
Mutations in LAMB1 Cause Cobblestone Brain Malformation without Muscular or Ocular Abnormalities
Radmanesh, F., Çağlayan, A. O., Silhavy, J. L., Yılmaz, C., Cantagrel, V., Omar, T., Rosti, B., Kaymakçalan, H., Gabriel, S., Li, M., et al. (2013) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2013.02.005 · Cited by 117 · see citing works
Malformations of Cortical Development
Aronica, E., Becker, A. J., & Spreafico, R. (2012) · Brain Pathology · doi:10.1111/j.1750-3639.2012.00581.x · Cited by 114 · see citing works
Ohtaka‐Maruyama, C., & Okado, H. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00447 · Cited by 111 · see citing works
Type III Collagen Regulates Osteoblastogenesis and the Quantity of Trabecular Bone
Volk, S. W., Shah, S. R., Cohen, A. J., Wang, Y., Brisson, B. K., Vogel, L. K., Hankenson, K. D., & ADAMS, S. L. (2014) · Calcified Tissue International · doi:10.1007/s00223-014-9843-x · Cited by 110 · see citing works
Tang, X., Jin, R., Qu, G., Wang, X., Li, Z., Yuan, Z., Zhao, C., Siwko, S. K., Shi, T., Wang, P., et al. (2013) · Cancer Research · doi:10.1158/0008-5472.can-13-1049 · Cited by 110 · see citing works
GPR56/ADGRG1 is a platelet collagen-responsive GPCR and hemostatic sensor of shear force
Yeung, J., Adili, R., Stringham, E. N., Luo, R., Vizurraga, A., Rosselli‐Murai, L. K., Stoveken, H. M., Yu, M., Piao, X., Holinstat, M. A., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2008921117 · Cited by 106 · see citing works
Self-citationMatching structure with function: the GAIN domain of Adhesion-GPCR and PKD1-like proteins
Prömel, S., Langenhan, T., & Araç, D. (2013) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2013.06.002 · Cited by 98 · see citing works
Lanoue, V, Usardi, A., Sigoillot, S. M., Talleur, M., Iyer, K., Mariani, J., Isope, P., Vodjdani, G., Heintz, N., & Selimi, F. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.46 · Cited by 90 · see citing works
Radner, S., Banos, C. C., Bachay, G., Li, Y. N., Hunter, D. D., Brunken, W. J., & Yee, K. T. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22057 · Cited by 90 · see citing works
Type IV Collagens and Basement Membrane Diseases
Mao, M., Alavi, M. V., Labelle‐Dumais, C., & Gould, D. B. (2015) · Current topics in membranes · doi:10.1016/bs.ctm.2015.09.002 · Cited by 89 · see citing works
The roles of dystroglycan in the nervous system: insights from animal models of muscular dystrophy
Nickolls, A. R., & Bönnemann, C. G. (2018) · Disease Models & Mechanisms · doi:10.1242/dmm.035931 · Cited by 88 · see citing works
Adhesion G protein-coupled receptors: opportunities for drug discovery
Bassilana, F., Nash, M., & Ludwig, M. (2019) · Nature Reviews Drug Discovery · doi:10.1038/s41573-019-0039-y · Cited by 88 · see citing works
Alexander, S., Mathie, A. A., & Peters, J. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01649_3.x · Cited by 88 · see citing works
Karpus, O. N., Veninga, H., Hoek, R. M., Flierman, D., van Buul, J. D., vandenAkker, C. C., VanBavel, E., Medof, M. E., van Lier, R. A. W., Reedquist, K. A., et al. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1202192 · Cited by 86 · see citing works
Maintenance of the hematopoietic stem cell pool in bone marrow niches by EVI1-regulated GPR56
Saito, Y., Kaneda, K., Suekane, A., Ichihara, E., Nakahata, S., Yamakawa, N., Nagai, K., Mizuno, N., Kogawa, K., Miura, I., et al. (2013) · Leukemia · doi:10.1038/leu.2013.75 · Cited by 84 · see citing works
Molecular composition and function of integrin-based collagen glues—Introducing COLINBRIs
Zeltz, C., Orgel, J. P. R. O., & Gullberg, D. (2013) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2013.12.022 · Cited by 83 · see citing works
Krishnan, A., & Schiöth, H. B. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.110312 · Cited by 81 · see citing works
An atlas of G-protein coupled receptor expression and function in human subcutaneous adipose tissue
Amisten, S., Neville, M. J., Hawkes, R. G., Persaud, S. J., Karpe, F., & Salehi, A. A. (2014) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.09.007 · Cited by 80 · see citing works
Adhesion G protein-coupled receptors: structure, signaling, physiology, and pathophysiology
Lala, T., & Hall, R. A. (2022) · Physiological Reviews · doi:10.1152/physrev.00027.2021 · Cited by 79 · see citing works
The Emerging Role of Adhesion GPCRs in Cancer
Gad, A. A., & Balenga, N. A. B. (2020) · ACS Pharmacology & Translational Science · doi:10.1021/acsptsci.9b00093 · Cited by 74 · see citing works
Orlandi, C., Omori, Y., Wang, Y., Cao, Y., Ueno, A. M., Roux, M. J., Condomitti, G., de Wit, J., Kanagawa, M., Furukawa, T., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.08.068 · Cited by 75 · see citing works
Folding brains: from development to disease modeling
Del-Valle-Anton, L., & Borrell, V. (2021) · Physiological Reviews · doi:10.1152/physrev.00016.2021 · Cited by 78 · see citing works
GPR56/ADGRG1 Inhibits Mesenchymal Differentiation and Radioresistance in Glioblastoma
Moreno, M., Pedrosa, L., Paré, L., Pineda, E., Bejarano, L., Martínez, J., Balasubramaniyan, V., Ezhilarasan, R., Kallarackal, N., Kim, S.-H., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.083 · Cited by 74 · see citing works
Self-citationDisorders of neurogenesis and cortical development
Guarnieri, F. C., de Chevigny, A., Falace, A., & Cardoso, C. (2018) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2018.20.4/ccardoso · Cited by 74 · see citing works
Stoveken, H. M., Larsen, S. D., Smrcka, A. V., & Tall, G. G. (2018) · Molecular Pharmacology · doi:10.1124/mol.117.111476 · Cited by 73 · see citing works
Luo, R., Jeong, S., Yang, A., Wen, M., Saslowsky, D. E., Lencer, W. I., Araç, D., & Piao, X. (2014) · PLoS ONE · doi:10.1371/journal.pone.0100043 · Cited by 72 · see citing works
Self-citationThe BAI subfamily of adhesion GPCRs: synaptic regulation and beyond
Stephenson, J. R., Purcell, R. H., & Hall, R. A. (2014) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2014.02.002 · Cited by 71 · see citing works
Barber, M., & Pierani, A. (2015) · Developmental Neurobiology · doi:10.1002/dneu.22363 · Cited by 70 · see citing works
Ligands and Beyond: Mechanosensitive Adhesion GPCRs
Lin, H., Ng, K., Chen, T., & Tseng, W.-Y. (2022) · Pharmaceuticals · doi:10.3390/ph15020219 · Cited by 69 · see citing works
GPR56 and the Developing Cerebral Cortex: Cells, Matrix, and Neuronal Migration
Singer, K., Luo, R., Jeong, S., & Piao, X. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8343-0 · Cited by 69 · see citing works
Self-citationEvidence for an interaction of neuronostatin with the orphan G protein-coupled receptor, GPR107
Yosten, G. L. C., Redlinger, L. J., & Samson, W. K. (2012) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00336.2012 · Cited by 69 · see citing works
Dihydromunduletone Is a Small-Molecule Selective Adhesion G Protein–Coupled Receptor Antagonist
Stoveken, H. M., Bahr, L. L., Anders, M. W., Wojtovich, A. P., Smrcka, A. V., & Tall, G. G. (2016) · Molecular Pharmacology · doi:10.1124/mol.116.104828 · Cited by 69 · see citing works
Tethered Agonism: A Common Activation Mechanism of Adhesion GPCRs
Liebscher, I., & Schöneberg, T. (2016) · Handbook of experimental pharmacology · doi:10.1007/978-3-319-41523-9_6 · Cited by 68 · see citing works
GPR56/ADGRG1 regulates development and maintenance of peripheral myelin
Ackerman, S. D., Luo, R., Poitelon, Y., Mogha, A., Harty, B. L., D’Rozario, M., Sanchez, N., Lakkaraju, A. K., Gamble, P. G., Li, J., et al. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20161714 · Cited by 68 · see citing works
Self-citationPeeters, M. C., Fokkelman, M., Boogaard, B., Egerod, K. L., van de Water, B., IJzerman, A. P., & Schwartz, T. W. (2015) · Cellular Signalling · doi:10.1016/j.cellsig.2015.08.015 · Cited by 67 · see citing works
Orphan G Protein Coupled Receptors in Affective Disorders
Watkins, L. R., & Orlandi, C. (2020) · Genes · doi:10.3390/genes11060694 · Cited by 67 · see citing works
Dunn, H. A., Orlandi, C., & Martemyanov, K. A. (2019) · Pharmacological Reviews · doi:10.1124/pr.119.018044 · Cited by 66 · see citing works
GPR56/ADGRG1 is associated with response to antidepressant treatment
Belzeaux-R, R., Gorgievski, V., Fiori, L. M., López, J. P., Grenier, J., Lin, R., Nagy, C., Ibrahim, E. C., Gascon, E., Courtet, P., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15423-5 · Cited by 65 · see citing works
Disease-Associated Mutations Prevent GPR56-Collagen III Interaction
Luo, R., Jin, Z., Deng, Y., Strokes, N., & Piao, X. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029818 · Cited by 65 · see citing works
Self-citationhTERT promotes cell adhesion and migration independent of telomerase activity
Liu, H., Liu, Q., Ge, Y., Zhao, Q., Zheng, X., & Zhao, Y. B. (2016) · Scientific Reports · doi:10.1038/srep22886 · Cited by 65 · see citing works
Adhesion G protein–coupled receptors—Candidate metabotropic mechanosensors and novel drug targets
Langenhan, T. (2019) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/bcpt.13223 · Cited by 65 · see citing works
Ferent, J., Zaidi, D., & Francis, F. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.578341 · Cited by 64 · see citing works
Valtcheva, N., Primorac, A., Jurisic, G., Hollmén, M., & Detmar, M. J. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.512954 · Cited by 63 · see citing works
COL4A1 Mutations Cause Neuromuscular Disease with Tissue-Specific Mechanistic Heterogeneity
Labelle‐Dumais, C., Schuitema, V., Hayashi, G., Hoff, K., Gong, W., Dao, D. Q., Ullian, E. M., Oishi, P. E., Margeta, M., & Gould, D. B. (2019) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2019.03.007 · Cited by 63 · see citing works
Zhu, B., Luo, R., Jin, P., Li, T., Oak, H. C., Giera, S., Monk, K. R., Lak, P., Shoichet, B. K., & Piao, X. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.008234 · Cited by 62 · see citing works
Self-citationSchwann cell interactions during the development of the peripheral nervous system
Wilson, E. R., Nunes, G. D., Weaver, M. R., Frick, L. R., & Feltri, M. L. (2020) · Developmental Neurobiology · doi:10.1002/dneu.22744 · Cited by 62 · see citing works
The role of GPR56/ADGRG1 in health and disease
Singh, A. K., & Lin, H. (2021) · Biomedical Journal · doi:10.1016/j.bj.2021.04.012 · Cited by 60 · see citing works
A Comprehensive Mutagenesis Screen of the Adhesion GPCR Latrophilin-1/ADGRL1
Nazarko, O. V., Kibrom, A., Winkler, J., Leon, K., Stoveken, H. M., Salzman, G., Merdas, K., Lu, Y., Narkhede, P., Tall, G. G., et al. (2018) · iScience · doi:10.1016/j.isci.2018.04.019 · Cited by 60 · see citing works
A guide to adhesion GPCR research
Liebscher, I., Cevheroğlu, O., Hsiao, C., Maia, A. F., Schihada, H., Scholz, N., Soave, M., Spieß, K., Trajković, K., Kosloff, M., et al. (2021) · FEBS Journal · doi:10.1111/febs.16258 · Cited by 58 · see citing works
Yu, D., Li, T., Delpech, J.-C., Zhu, B., Kishore, P., Koshi, T., Luo, R., Pratt, K. J. B., Popova, G., Nowakowski, T. J., et al. (2022) · Science Advances · doi:10.1126/sciadv.abm2545 · Cited by 58 · see citing works
Self-citationChiang, N., Chang, G.-W., Huang, Y.-S., Peng, Y.-M., Hsiao, C., Kuo, M., & Lin, H. (2016) · Journal of Cell Science · doi:10.1242/jcs.174458 · Cited by 57 · see citing works
Olaniru, O. E., Pingitore, A., Giera, S., Piao, X., González, R. C., Jones, P. M., & Persaud, S. J. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2846-4 · Cited by 55 · see citing works
Self-citationGpr97 Exacerbates AKI by Mediating Sema3A Signaling
Fang, W., Wang, Z., Li, Q., Wang, X., Zhang, Y., Sun, Y., Tang, W., Ma, C., Sun, J., Li, N., et al. (2018) · Journal of the American Society of Nephrology · doi:10.1681/asn.2017080932 · Cited by 54 · see citing works
Zhang, S., Chatterjee, T., Godoy, C., Wu, L., Liu, Q. J., & Carmon, K. S. (2019) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-19-0436 · Cited by 54 · see citing works
Chiang, N., Peng, Y.-M., Juang, H., Chen, T., Pan, H.-L., Chang, G.-W., & Lin, H. (2016) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2016.10.031 · Cited by 52 · see citing works
Morphological and functional aspects of progenitors perturbed in cortical malformations
Bizzotto, S., & Francis, F. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00030 · Cited by 52 · see citing works
GPR56 Functions Together with α3β1 Integrin in Regulating Cerebral Cortical Development
Jeong, S., Luo, R., Singer, K., Giera, S., Kreidberg, J. A., Kiyozumi, D., Shimono, C., Sekiguchi, K., & Piao, X. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068781 · Cited by 50 · see citing works
Self-citationArrestin‐independent constitutive endocytosis of GPR125/ADGRA3
Spieß, K., Bagger, S. O., Torz, L., Jensen, K. H. R., Walser, A. L., Kvam, J. M., Møgelmose, A. K., Daugvilaite, V., Junnila, R. K., Hjortø, G. M., et al. (2019) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14263 · Cited by 47 · see citing works
Wu, M. P., Doyle, J. R., Barry, B. J., Beauvais, A., Rozkalne, A., Piao, X., Lawlor, M. W., Kopin, A. S., Walsh, C. A., & Gussoni, E. (2013) · FEBS Journal · doi:10.1111/febs.12529 · Cited by 47 · see citing works
Self-citationVandervore, L. V., Stouffs, K., Tanyalçin, I., Vanderhasselt, T., Roelens, F., Holder‐Espinasse, M., Jørgensen, A., Pepin, M. G., Petit, F., Kien, P. K. V., et al. (2017) · Journal of Medical Genetics · doi:10.1136/jmedgenet-2016-104421 · Cited by 47 · see citing works
Diagnostic Approach to Cerebellar Hypoplasia
Accogli, A., Addour-Boudrahem, N., & Srour, M. (2021) · The Cerebellum · doi:10.1007/s12311-020-01224-5 · Cited by 46 · see citing works
- Authors
- Luo, R., Jeong, S.-J., Jin, Z., Strokes, N., Li, S., & Piao, X.
- Affiliations
- Boston Children's Hospital (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2011-07-18
- Volume
- 108
- Issue
- 31
- Pages
- 12925-12930
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3150909
- OpenAlex
- W2083047610
- Cited by
- 290
- References
- 50
- Citations by year
- 2026: 14 · 2025: 21 · 2024: 15 · 2023: 20 · 2022: 17 · 2021: 23 · 2020: 22 · 2019: 26 · 2018: 15 · 2017: 14 · 2016: 26 · 2015: 22 · 2014: 19 · 2013: 18 · 2012: 16
- FWCI
- 5.66
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01NS057536)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- GPR56, type III collagen, COL3A1, G protein-coupled receptor ligands, cortical lamination, cortical development, neuronal migration, cobblestone lissencephaly, adhesion GPCRs, RhoA signaling, cerebral cortex malformation
- MeSH terms
- Animals, Basement Membrane, Brain, Cell Movement, Cells, Cultured, Cerebral Cortex, Humans, Immunohistochemistry, Neurons, Protein Binding, Recombinant Proteins, Immunoblotting, Microscopy, Immunoelectron, Mice, Knockout, rhoA GTP-Binding Protein, Collagen Type III, NIH 3T3 Cells, Receptors, G-Protein-Coupled, GTP-Binding Protein alpha Subunits, G12-G13, Immunoprecipitation, Mice, Cobblestone Lissencephaly
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review