GPR56 Regulates Pial Basement Membrane Integrity and Cortical Lamination
Open accessAbstract
GPR56 is a member of the family of adhesion G-protein-coupled receptors that have a large extracellular region containing a GPS (G-protein proteolytic site) domain. Loss-of-function mutations in the GPR56 gene cause a specific human brain malformation called bilateral frontoparietal polymicrogyria (BFPP). BFPP is a radiological diagnosis and its histopathology remains unclear. This study demonstrates that loss of the mouse Gpr56 gene leads to neuronal ectopia in the cerebral cortex, a cobblestone-like cortical malformation. There are four crucial events in the development of cobblestone cortex, namely defective pial basement membrane (BM), abnormal anchorage of radial glial endfeet, mislocalized Cajal–Retzius cells, and neuronal overmigration. By detailed time course analysis, we reveal that the leading causal events are likely the breaches in the pial BM. We show further that GPR56 is present in abundance in radial glial endfeet. Furthermore, a putative ligand of GPR56 is localized in the marginal zone or overlying extracellular matrix. These observations provide compelling evidence that GPR56 functions in regulating pial BM integrity during cortical development.
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 [16]
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 [16]
GPR56 protein is most highly expressed in progenitors in the ventricular and subventricular zones during neurogenesis in mice.
“GPR56 protein is most highly expressed in progenitors in the ventricular and subventricular zones during neurogenesis in mice (16, 18).”
From Evolutionarily Dynamic Alternative Splicing of <i>GPR56</i> Regulates Regional Cerebral Cortical Patterning (2014) · cites this paper as [16]
Loss of GPR56 disrupts radial glia and causes breaches in the pial basement membrane, through which some neurons over-migrate.
“Loss of GPR56 disrupts radial glia and causes breaches in the pial basement membrane, through which some neurons over-migrate (9, 16).”
From Evolutionarily Dynamic Alternative Splicing of <i>GPR56</i> Regulates Regional Cerebral Cortical Patterning (2014) · cites this paper as [16]
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
An ancient retrotransposal insertion causes Fukuyama-type congenital muscular dystrophy
Kobayashi, K., Nakahori, Y., Miyake, M., Matsumura, K., Kondo-Iida, E., Nomura, Y., Segawa, M., Yoshioka, M., Saito, K., Ōsawa, M., et al. (1998) · Nature · doi:10.1038/28653 · Cited by 802 · see citing works
Post-translational disruption of dystroglycan–ligand interactions in congenital muscular dystrophies
Michele, D. E., Barresi, R., Kanagawa, M., Saito, F., Cohn, R. D., Satz, J. S., Dollar, J., Nishino, I., Kelley, R. I., Somer, H., et al. (2002) · Nature · doi:10.1038/nature00837 · Cited by 779 · see citing works
Tissir, F., & Goffinet, A. M. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1113 · Cited by 748 · see citing works
Malatesta, P., Hack, M. A., Hartfuss, E., Kettenmann, H., Klinkert, W. E. F., Kirchhoff, F., & Götz, M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00116-8 · Cited by 744 · see citing works
Yoshida, A., Kobayashi, K., Manya, H., Taniguchi, K., Kano, H., Mizuno, M., Inazu, T., Mitsuhashi, H., Takahashi, S., Takeuchi, M., et al. (2001) · Developmental Cell · doi:10.1016/s1534-5807(01)00070-3 · Cited by 706 · 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
The tetraspanin web modulates immune-signalling complexes
Levy, S., & Shoham, T. (2005) · Nature reviews. Immunology · doi:10.1038/nri1548 · Cited by 622 · see citing works
Brain lipid-binding protein (BLBP): A novel signaling system in the developing mammalian CNS
Feng, L., Hatten, M. E., & Heintz, N. (1994) · Neuron · doi:10.1016/0896-6273(94)90341-7 · Cited by 572 · 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
Self-citationThe matrix reorganized: extracellular matrix remodeling and integrin signaling
Larsen, M., Artym, V. V., Green, J. A., & Yamada, K. M. (2006) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2006.08.009 · Cited by 535 · 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
Mitotic Spindle Regulation by Nde1 Controls Cerebral Cortical Size
Feng, Y., & Walsh, C. A. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.023 · Cited by 353 · see citing works
Self-citationAnton, E. S., Kreidberg, J. A., & RAKIC, P. T. (1999) · Neuron · doi:10.1016/s0896-6273(00)81089-2 · Cited by 351 · 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
A Critical Function of the Pial Basement Membrane in Cortical Histogenesis
Halfter, W. M., Dong, S., Yip, Y.-P., Willem, M., & Mayer, U. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-14-06029.2002 · Cited by 290 · see citing works
Elusive radial glial cells: Historical and evolutionary perspective
RAKIC, P. T. (2003) · Glia · doi:10.1002/glia.10244 · Cited by 279 · 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
Self-citationArcangelis, 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
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
Stacey, M. A., Chang, G.-W., Davies, J. Q., Kwakkenbos, M. J., Sanderson, R. D., Hamann, J., Gordon, S., & Lin, H. (2003) · Blood · doi:10.1182/blood-2002-11-3540 · Cited by 209 · see citing works
Haubst, N., Georges‐Labouesse, E., Arcangelis, A. D., Mayer, U., & Götz, M. (2006) · Development · doi:10.1242/dev.02486 · Cited by 157 · see citing works
Sievers, J., Pehlemann, F. W., Gude, S., & Berry, M. (1994) · Journal of Neurocytology · doi:10.1007/bf01183867 · Cited by 153 · 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-citationChang, 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
Self-citationAn 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-citationNiewmierzycka, 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
Basement membrane: Putting up the barriers
Schwarzbauer, J. E. (1999) · Current Biology · doi:10.1016/s0960-9822(99)80153-5 · Cited by 112 · see citing works
González, J. L., Russo, C. J., Goldowitz, D., Sweet, H. O., Davisson, M. T., & Walsh, C. A. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-23-09204.1997 · Cited by 110 · see citing works
Self-citationHu, H., Yang, Y.-A., Eade, A. M., Xiong, Y., & Qi, Y. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21238 · Cited by 73 · see citing works
Yamamoto, T., Kato, Y., Kawaguchi, M., Shibata, N., & Kobayashi, M. (2004) · Medical Molecular Morphology · doi:10.1007/s00795-004-0260-5 · Cited by 38 · see citing works
Partial nephrectomy for incidental primary renal neuroendocrine carcinoma: case report.
Chen, Y., Chuang, C., Chu, S. H., Ng, K. F., & Liao, S. (1999) · PubMed · Cited by 1 · see citing works
GPR56 and Bilateral Frontoparietal Polymicrogyria
Piao, X., & Walsh, C. A. (2008) · doi:10.1093/oso/9780195306910.003.0148 · Cited by 1 · see citing works
Self-citation
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
Malformations of cortical development: clinical features and genetic causes
Guerrini, R., & Dobyns, W. B. (2014) · The Lancet Neurology · doi:10.1016/s1474-4422(14)70040-7 · Cited by 513 · 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-citationMutations 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
Cerebral 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
Definitions and classification of malformations of cortical development: practical guidelines
Severino, M., Geraldo, A. F., Utz, N., Tortora, D., Pogledić, I., Klonowski, W., Triulzi, F. M., Arrigoni, F., Mankad, K., Leventer, R. J., et al. (2020) · Brain · doi:10.1093/brain/awaa174 · Cited by 312 · see citing works
Luo, R., Jeong, S.-J., Jin, Z., Strokes, N., Li, S., & Piao, X. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104821108 · Cited by 290 · see citing works
Self-citationA developmental and genetic classification for midbrain-hindbrain malformations
Barkovich, A. J., Millen, K. J., & Dobyns, W. B. (2009) · Brain · doi:10.1093/brain/awp247 · Cited by 285 · 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
Clinical and imaging heterogeneity of polymicrogyria: a study of 328 patients
Leventer, R. J., Jansen, A., Pilz, D. T., Stoodley, N., Marini, C., Dubeau, F., Malone, J., Mitchell, L. A., Mandelstam, S. A., Scheffer, I. E., et al. (2010) · Brain · doi:10.1093/brain/awq078 · Cited by 264 · see citing works
Neuronal migration mechanisms in development and disease
Valiente, M., & Marín, Ó. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.12.003 · Cited by 255 · 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-citationDevisme, L., Bouchet, C., Gonzalès, M., Alanio, E., Bazin, A., Bessières, B., Bigi, N., Blanchet, P., Bonneau, D., Bonnières, M., et al. (2012) · Brain · doi:10.1093/brain/awr357 · Cited by 193 · see citing works
Tubulin-related cortical dysgeneses: microtubule dysfunction underlying neuronal migration defects
Jaglin, X. H., & Chelly, J. (2009) · Trends in Genetics · doi:10.1016/j.tig.2009.10.003 · Cited by 194 · see citing works
The N Terminus of the Adhesion G Protein-coupled Receptor GPR56 Controls Receptor Signaling Activity
Paavola, K. J., Stephenson, J. R., Ritter, S. L., Alter, S. P., & Hall, R. A. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.247973 · Cited by 184 · 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-citationA Radial Glia-Specific Role of RhoA in Double Cortex Formation
Cappello, S., Böhringer, C., Bergami, M., Conzelmann, K., Ghanem, A., Tomassy, G. S., Arlotta, P., Mainardi, M., Allegra, M., Caleo, M., et al. (2012) · Neuron · doi:10.1016/j.neuron.2011.12.030 · 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
From genes to folds: a review of cortical gyrification theory
Ronan, L., & Fletcher, P. C. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0961-z · Cited by 145 · 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
Manzini, M. C., & Walsh, C. A. (2011) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2011.01.006 · Cited by 151 · see citing works
Self-citationThe 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-citationIntegrative Mechanisms of Oriented Neuronal Migration in the Developing Brain
Evsyukova, I. Y., Plestant, C., & Anton, E. S. (2013) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-101512-122400 · Cited by 143 · 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-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
The emerging role of the tubulin code: From the tubulin molecule to neuronal function and disease
Chakraborti, S., Natarajan, K., Curiel, J., Janke, C., & Liu, J. S.-H. (2016) · Cytoskeleton · doi:10.1002/cm.21290 · Cited by 144 · see citing works
Dynamic mRNA Transport and Local Translation in Radial Glial Progenitors of the Developing Brain
Pilaz, L., Lennox, A. L., Rouanet, J. P., & Silver, D. L. (2016) · Current Biology · doi:10.1016/j.cub.2016.10.040 · Cited by 144 · see citing works
Specific expression of GPR56 by human cytotoxic lymphocytes
Peng, Y.-M., van de Garde, M. D. B., Cheng, K.-F., Baars, P. A., Remmerswaal, E. B. M., van Lier, R. A. W., Mackay, C. R., Lin, H., & Hamann, J. (2011) · Journal of Leukocyte Biology · doi:10.1189/jlb.0211092 · Cited by 142 · see citing works
Giera, 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-citationLabelle‐Dumais, C., Dilworth, D. J., Harrington, E. P., de Leau, M., Lyons, D., Kabaeva, Z. T., Manzini, M. C., Dobyns, W. B., Walsh, C. A., Michele, D. E., et al. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002062 · Cited by 141 · see citing works
Self-citationCurrent concepts of polymicrogyria
Barkovich, A. J. (2010) · Neuroradiology · doi:10.1007/s00234-009-0644-2 · Cited by 139 · see citing works
Fallet‐Bianco, C., Laquerrière, A., Poirier, K., Encha‐Razavi, F., Guimiot, F., Dias, P., Lœuillet, L., Lascelles, K., Beldjord, C., Carion, N., et al. (2014) · Acta Neuropathologica Communications · doi:10.1186/2051-5960-2-69 · Cited by 134 · 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
Cortical Malformations: Lessons in Human Brain Development
Subramanian, L., Calcagnotto, M. E., & Paredes, M. F. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00576 · Cited by 131 · see citing works
Buchsbaum, I. Y., & Cappello, S. (2019) · Development · doi:10.1242/dev.163766 · Cited by 128 · see citing works
Polymicrogyria: A common and heterogeneous malformation of cortical development
Stutterd, C., & Leventer, R. J. (2014) · American Journal of Medical Genetics Part C Seminars in Medical Genetics · doi:10.1002/ajmg.c.31399 · Cited by 128 · 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
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-citationPolymicrogyria: pathology, fetal origins and mechanisms
Squier, W., & Jansen, A. (2014) · Acta Neuropathologica Communications · doi:10.1186/s40478-014-0080-3 · Cited by 122 · 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-citationGPR56 Regulates VEGF Production and Angiogenesis during Melanoma Progression
Yang, L., Chen, G., Mohanty, S., Scott, G., Fazal, F., Rahman, A., Begum, S., Hynes, R. O., & Xu, L. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-4543 · Cited by 116 · 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-citationNeuronal migration disorders: Focus on the cytoskeleton and epilepsy
Stouffer, M. A., Golden, J. A., & Francis, F. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.08.003 · Cited by 114 · see citing works
Controlling cell surface dynamics and signaling: How CD82/KAI1 suppresses metastasis
Miranti, C. K. (2008) · Cellular Signalling · doi:10.1016/j.cellsig.2008.08.023 · Cited by 100 · see citing works
Koirala, S., & Corfas, G. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009198 · Cited by 91 · see citing works
Self-citationRadner, 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 88 · 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
The histopathology of polymicrogyria: a series of 71 brain autopsy studies
Jansen, A., Robitaille, Y., Honavar, M., Mullatti, N., Leventer, R. J., Andermann, E., Andermann, F., & Squier, W. (2015) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.12840 · Cited by 86 · 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
Mastrokolias, A., Ariyürek, Y., Goeman, J. J., van Duijn, E., Roos, R. A. C., van der Mast, R. C., van Ommen, G. B., den Dunnen, J. T., Hoen, P. A. C. ’., & van Roon‐Mom, W. (2015) · European Journal of Human Genetics · doi:10.1038/ejhg.2014.281 · Cited by 85 · see citing works
Yokota, Y., Eom, T.-Y., Stanco, A., Kim, W.-Y., Rao, S., Snider, W. D., & Anton, E. S. (2010) · Development · doi:10.1242/dev.048637 · Cited by 85 · 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
Chiang, N., Hsiao, C., Huang, Y.-S., Chen, H.-Y., Hsieh, I.-J., Chang, G.-W., & Lin, H. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.183830 · Cited by 82 · see citing works
Molecular regulation of neuronal migration during neocortical development
Huang, Z. (2009) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2009.06.003 · Cited by 78 · 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
Development and Dysgenesis of the Cerebral Cortex: Malformations of Cortical Development
Raybaud, C., & Widjaja, E. (2011) · Neuroimaging Clinics of North America · doi:10.1016/j.nic.2011.05.014 · Cited by 78 · see citing works
Weimer, J. M., Yokota, Y., Stanco, A., Stumpo, D. J., Blackshear, P. J., & Anton, E. S. (2009) · Development · doi:10.1242/dev.036616 · Cited by 74 · 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-citationMemo1-Mediated Tiling of Radial Glial Cells Facilitates Cerebral Cortical Development
Nakagawa, N., Plestant, C., Yabuno-Nakagawa, K., Li, J., Lee, J. C. L., Huang, C.-W., Lee, A., Krupa, O., Adhikari, A., Thompson, S., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.049 · Cited by 67 · 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-citationAdhesion G Protein-Coupled Receptor G1 (ADGRG1/GPR56) and Pancreatic β-Cell Function
Dunér, P., Al-Amily, I. M., Soni, A., Asplund, O., Safi, F., Storm, P., Groop, L., Amisten, S., & Salehi, A. A. (2016) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2016-1884 · Cited by 71 · see citing works
More Than Mortar: Glia as Architects of Nervous System Development and Disease
Lago‐Baldaia, I., Fernandes, V. M., & Ackerman, S. D. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.611269 · Cited by 68 · see citing works
(2013) · Indian Journal of Surgery · doi:10.1007/12262.0973-9793 · Cited by 71 · see citing works
Barber, M., & Pierani, A. (2015) · Developmental Neurobiology · doi:10.1002/dneu.22363 · Cited by 70 · 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-citationBasal process and cell divisions of neural progenitors in the developing brain
Kosodo, Y., & Huttner, W. Β. (2009) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2009.01101.x · Cited by 66 · 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-citationRole of G12 proteins in oncogenesis and metastasis
Juneja, J., & Casey, P. J. (2009) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2009.00180.x · Cited by 68 · 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
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-citationFerent, J., Zaidi, D., & Francis, F. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.578341 · Cited by 64 · see citing works
Neural tube defects and impaired neural progenitor cell proliferation in Gβ1 ‐deficient mice
Okae, H., & Iwakura, Y. (2010) · Developmental Dynamics · doi:10.1002/dvdy.22256 · 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
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-citationAndrade, D. M. (2009) · Human Genetics · doi:10.1007/s00439-009-0702-1 · Cited by 59 · see citing works
Spaethling, J. M., Sánchez-Alavez, M., Lee, J., Xia, F. C., Dueck, H. R., Wang, W., Fisher, S. A., Sul, J., Seale, P., Kim, J., et al. (2015) · The FASEB Journal · doi:10.1096/fj.15-273797 · Cited by 56 · see citing works
GPR56 is essential for testis development and male fertility in mice
Chen, G., Yang, L., Begum, S., & Xu, L. (2010) · Developmental Dynamics · doi:10.1002/dvdy.22468 · Cited by 56 · see citing works
Self-citationOlaniru, 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-citationUnderstanding cadherin EGF LAG seven‐pass G‐type receptors
Wang, X., Zhang, D., Xu, Z., Ma, M., Wang, W., Li, L., Han, X., Huo, Y., Yu, X., & Sun, J. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12955 · 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-citationProgress in demystification of adhesion G protein-coupled receptors
Liebscher, I., Schöneberg, T., & Prömel, S. (2013) · Biological Chemistry · doi:10.1515/hsz-2013-0109 · Cited by 49 · see citing works
Jin, G., Sakitani, K., Wang, H., Jin, Y., Dubeykovskiy, A. N., Worthley, D. L., Tailor, Y. H., & Wang, T. C. (2017) · Oncotarget · doi:10.18632/oncotarget.16506 · Cited by 48 · see citing works
Arrestin‐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
MRI analysis of sulcation morphology in polymicrogyria
Barkovich, A. J. (2010) · Epilepsia · doi:10.1111/j.1528-1167.2009.02436.x · 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
The G protein-coupled receptor GPRC5B contributes to neurogenesis in the developing mouse neocortex
Kurabayashi, N., Nguyen, M. D., & Sanada, K. (2013) · Development · doi:10.1242/dev.099754 · Cited by 46 · see citing works
Qiu, Z., Cang, Y., & Goff, S. P. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2861-10.2010 · Cited by 46 · see citing works
Developmental disorders of the midbrain and hindbrain
Barkovich, A. J. (2012) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2012.00007 · Cited by 46 · see citing works
Dissecting signaling and functions of adhesion G protein–coupled receptors
Araç, D., Aust, G., Calebiro, D., Engel, F. B., Formstone, C. J., Goffinet, A. M., Hamann, J., Kittel, R. J., Liebscher, I., Lin, H., et al. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2012.06820.x · Cited by 45 · see citing works
Self-citationRadial Microcolumnar Cortical Architecture: Maturational Arrest or Cortical Dysplasia?
Sarnat, H. B., & Flores‐Sarnat, L. (2013) · Pediatric Neurology · doi:10.1016/j.pediatrneurol.2012.10.001 · Cited by 45 · see citing works
G protein–coupled receptor modulation with pepducins: moving closer to the clinic
Dimond, P. F., Carlson, K. E., Bouvier, M., Gerard, C. J., Xu, L., Covic, L., Agarwal, A., Ernst, O. P., Janz, J. M., Schwartz, T. W., et al. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06039.x · Cited by 42 · see citing works
Self-citationBasal enrichment within neuroepithelia suggests novel function(s) for Celsr1 protein
Formstone, C. J., Moxon, C. A., Murdoch, J. N., Little, P., & Mason, I. J. (2010) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2010.03.008 · Cited by 42 · see citing works
Genetic animal models of malformations of cortical development and epilepsy
Wong, M., & Roper, S. N. (2015) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2015.04.007 · Cited by 40 · see citing works
Pawlisz, A. S., & Feng, Y. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001172 · Cited by 40 · see citing works
Loss of Col3a1, the Gene for Ehlers-Danlos Syndrome Type IV, Results in Neocortical Dyslamination
Jeong, S., Li, S., Luo, R., Strokes, N., & Piao, X. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029767 · Cited by 40 · see citing works
Self-citationArreguin, A. J., & Colognato, H. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00118 · Cited by 39 · see citing works
- Authors
- Li, S., Jin, Z., Koirala, S., Bu, L., Xu, L., Hynes, R. O., Walsh, C. A., Corfas, G., & Piao, X.
- Affiliations
- Boston Children's Hospital (US)
- Harvard University (US)
- Howard Hughes Medical Institute (US)
- Beth Israel Deaconess Medical Center (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2008-05-28
- Volume
- 28
- Issue
- 22
- Pages
- 5817-5826
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2504715
- OpenAlex
- W2065631407
- Cited by
- 241
- References
- 37
- Citations by year
- 2026: 10 · 2025: 6 · 2024: 8 · 2023: 11 · 2022: 12 · 2021: 7 · 2020: 16 · 2019: 15 · 2018: 8 · 2017: 9 · 2016: 16 · 2015: 19 · 2014: 16 · 2013: 17 · 2012: 16
- FWCI
- 5.39
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Charles H. Hood Foundation
- Flight Attendant Medical Research Institute
- National Institutes of Health
- Genentech
- National Institute of Neurological Disorders and Stroke (R01 NS35884, R01NS057536, K08NS045762, T32NS007484, R01NS035884)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD018655, P30HD-18655)
- 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, adhesion G protein-coupled receptors, cortical lamination, Cajal-Retzius cells, cortical development, extracellular matrix
- MeSH terms
- Animals, Animals, Newborn, Bacterial Outer Membrane Proteins, Basement Membrane, Bromodeoxyuridine, Cell Movement, Cerebral Cortex, Embryo, Mammalian, Mutation, Neuroglia, Neurons, Pia Mater, Stem Cells, Tubulin, Mice, Knockout, Gene Expression Regulation, Developmental, ATP-Binding Cassette Transporters, Lamins, Receptors, G-Protein-Coupled, Mice
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