The secreted protein C1ql1 and its receptor BAI3 control the synaptic connectivity of excitatory inputs converging on cerebellar purkinje cells
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Precise patterns of connectivity are established by different types of afferents on a given target neuron, leading to well-defined and non-overlapping synaptic territories. What regulates the specific characteristics of each type of synapse, in terms of number, morphology, and subcellular localization, remains to be understood. Here, we show that the signaling pathway formed by the secreted complement C1Q-related protein C1QL1 and its receptor, the adhesion-GPCR brain angiogenesis inhibitor 3 (BAI3), controls the stereotyped pattern of connectivity established by excitatory afferents on cerebellar Purkinje cells. The BAI3 receptor modulates synaptogenesis of both parallel fiber and climbing fiber afferents. The restricted and timely expression of its ligand C1QL1 in inferior olivary neurons ensures the establishment of the proper synaptic territory for climbing fibers. Given the broad expression of C1QL and BAI proteins in the developing mouse brain, our study reveals a general mechanism contributing to the formation of a functional brain.
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Both the ADGRB3 receptor (BAI3) and kainate receptors are bound postsynaptically by C1ql proteins, regulating synaptogenesis in the case of ADGRB3 binding and postsynaptic recruitment in the case of kainate receptors.
“Both the ADGRB3 receptor (BAI3) and kainate receptors are bound postsynaptically by C1ql proteins, regulating synaptogenesis in the case of ADGRB3 binding and postsynaptic recruitment in the case of kainate receptors (Sigoillot et al., 2015;Matsuda et al., 2016;Bolliger et al., 2011;Yuzaki, 2017;Martinelli et al., 2016).”
From Glutamate receptors in domestication and modern human evolution (2020) · cites this paper as Sigoillot et al., 2015
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The Classical Complement Cascade Mediates CNS Synapse Elimination
Stevens, B., Allen, N. J., Vazquez, L. E., Howell, G. R., Christopherson, K. S., Nouri, N., Micheva, K. D., Mehalow, A. K., Huberman, A. D., Stafford, B., et al. (2007) · Cell · doi:10.1016/j.cell.2007.10.036 · Cited by 3,313 · see citing works
CHEMOAFFINITY IN THE ORDERLY GROWTH OF NERVE FIBER PATTERNS AND CONNECTIONS
Sperry, R. W. (1963) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.50.4.703 · Cited by 1,946 · see citing works
Neuroligins and neurexins link synaptic function to cognitive disease
Südhof, T. C. (2008) · Nature · doi:10.1038/nature07456 · Cited by 1,849 · see citing works
BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module
Park, D., Tosello‐Trampont, A., Elliott, M. R., Lu, M., Haney, L. B., Ma, Z., Klibanov, A. L., Mandell, J. W., & Ravichandran, K. S. (2007) · Nature · doi:10.1038/nature06329 · Cited by 848 · see citing works
Actin Cytoskeleton Regulation in Neuronal Morphogenesis and Structural Plasticity
Luo, L. (2002) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.18.031802.150501 · Cited by 658 · see citing works
Genesis of dendritic spines: insights from ultrastructural and imaging studies
Yuste, R., & Bonhoeffer, T. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1300 · Cited by 628 · see citing works
Rodriguez, A., Ehlenberger, D. B., Dickstein, D. L., Hof, P. R., & Wearne, S. L. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001997 · Cited by 571 · see citing works
Uemura, T., Lee, S.-J., Yasumura, M., Takeuchi, T., Yoshida, T., Ra, M., Taguchi, R., Sakimura, K., & Mishina, M. (2010) · Cell · doi:10.1016/j.cell.2010.04.035 · Cited by 496 · see citing works
Collins, M., Husi, H., Yu, L., Brandon, J. M., Anderson, C. N. G., Blackstock, W., Choudhary, J., & Grant, S. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03507.x · Cited by 448 · see citing works
Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina
Yamagata, M., & Sanes, J. R. (2008) · Nature · doi:10.1038/nature06469 · Cited by 378 · see citing works
Ango, F., Cristo, G. D., Higashiyama, H., Bennett, V., Wu, P., & Huang, Z. J. (2004) · Cell · doi:10.1016/j.cell.2004.10.004 · Cited by 371 · see citing works
Cbln1 Is a Ligand for an Orphan Glutamate Receptor δ2, a Bidirectional Synapse Organizer
Matsuda, K., Miura, E., Miyazaki, T., Kakegawa, W., Emi, K., Narumi, S., Fukazawa, Y., Ito-Ishida, A., Kondo, T., Shigemoto, R., et al. (2010) · Science · doi:10.1126/science.1185152 · Cited by 332 · see citing works
Cbln1 is essential for synaptic integrity and plasticity in the cerebellum
Hirai, H., Pang, Z., Bao, D., Miyazaki, T., Li, L., Miura, E., Parris, J., Rong, Y., Watanabe, M., Yuzaki, M., et al. (2005) · Nature Neuroscience · doi:10.1038/nn1576 · Cited by 325 · see citing works
Many Paths to Synaptic Specificity
Sanes, J. R., & Yamagata, M. (2009) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.24.110707.175402 · Cited by 307 · see citing works
Genetics and Cell Biology of Building Specific Synaptic Connectivity
Shen, K., & Scheiffele, P. (2010) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135302 · Cited by 212 · see citing works
Deep molecular diversity of mammalian synapses: why it matters and how to measure it
O'Rourke, N. A., Weiler, N. C., Micheva, K. D., & Smith, S. J. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3170 · Cited by 210 · see citing works
Cadherin-9 Regulates Synapse-Specific Differentiation in the Developing Hippocampus
Williams, M. E., Wilke, S. A., Daggett, A., Davis, E. K., Otto, S. J., Ravi, D., Ripley, B. A., Bushong, E. A., Ellisman, M. H., Klein, G., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.06.019 · Cited by 202 · see citing works
Sia, G.-M., Béïque, J.-C., Rumbaugh, G., Cho, R., Worley, P. F., & Huganir, R. L. (2007) · Neuron · doi:10.1016/j.neuron.2007.06.020 · Cited by 201 · see citing works
The cell-adhesion G protein-coupled receptor BAI3 is a high-affinity receptor for C1q-like proteins
Bolliger, M. F., Martinelli, D. C., & Südhof, T. C. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019577108 · Cited by 189 · see citing works
Wnt Signaling in the Vertebrate Central Nervous System: From Axon Guidance to Synaptic FunctionPreprint
Salinas, P. C. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a008003 · Cited by 189 · see citing works
Hashimoto, K., Ichikawa, R., Kitamura, K., Watanabe, M., & Kano, M. (2009) · Neuron · doi:10.1016/j.neuron.2009.06.008 · Cited by 187 · see citing works
Cerebellar synaptogenesis: what we can learn from mutant mice
Sotelo, C. (1990) · Journal of Experimental Biology · doi:10.1242/jeb.153.1.225 · Cited by 138 · see citing works
Ango, F., Wu, C., van der Want, J. J. L., Wu, P., Schachner, M., & Huang, Z. J. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060103 · Cited by 138 · see citing works
Duman, J. G., Tzeng, C. P., Tu, Y.-K., Munjal, T., Schwechter, B., Ho, T. S., & Tolias, K. F. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3978-12.2013 · Cited by 132 · see citing works
Iijima, T., Miura, E., Watanabe, M., & Yuzaki, M. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07202.x · Cited by 101 · see citing works
The Genetics of Symptom-Based Phenotypes: Toward a Molecular Classification of Schizophrenia
DeRosse, P., Lencz, T., Burdick, K. E., Siris, S. G., Kane, J. M., & Malhotra, A. K. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn076 · Cited by 94 · 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
Reciprocal trophic interactions in the adult climbing fibre-Purkinje cell system
Rossi, F., & Strata, P. (1995) · Progress in Neurobiology · doi:10.1016/0301-0082(95)80006-t · Cited by 76 · see citing works
Cbln1 and its family proteins in synapse formation and maintenance
Yuzaki, M. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.01.010 · Cited by 76 · see citing works
C. elegans Punctin specifies cholinergic versus GABAergic identity of postsynaptic domains
Pinan‐Lucarré, B., Tu, H., Pierron, M., Cruceyra, P. I., Zhan, H., Stigloher, C., Richmond, J. E., & Bessereau, J. (2014) · Nature · doi:10.1038/nature13313 · Cited by 68 · see citing works
Proteomic Studies of a Single CNS Synapse Type: The Parallel Fiber/Purkinje Cell Synapse
Selimi, F., Cristea, I. M., Heller, E. A., Chait, B. T., & Heintz, N. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000083 · Cited by 66 · see citing works
Avci, H. X., Lebrun, C., Wehrlé, R., Doulazmi, M., Chatonnet, F., Morel, M., Ema, M., Vodjdani, G., Sotelo, C., Flamant, F., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1119853109 · Cited by 66 · see citing works
Ito, A., Miyazaki, T., Miura, E., Matsuda, K., Watanabe, M., Yuzaki, M., & Okabe, S. (2012) · Neuron · doi:10.1016/j.neuron.2012.07.027 · Cited by 62 · see citing works
Uemura, T., Kakizawa, S., Yamasaki, M., Sakimura, K., Watanabe, M., Iino, M., & Mishina, M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2680-07.2007 · Cited by 60 · see citing works
Cesa, R., & Strata, P. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.02.061 · Cited by 60 · see citing works
Liao, H.-M., Chao, Y.-L., Huang, A.-L., Cheng, M.-C., Chen, Y.-J., Lee, K.-F., Fang, J., Hsu, C.-H., & Chen, C. (2012) · Schizophrenia Research · doi:10.1016/j.schres.2012.05.015 · Cited by 53 · see citing works
Antidepressant-like behavior in brain-specific angiogenesis inhibitor 2-deficient mice
Okajima, D., Kudo, G., & Yokota, H. (2011) · The Journal of Physiological Sciences · doi:10.1007/s12576-010-0120-0 · Cited by 49 · see citing works
Eph Receptors Are Involved in the Activity-Dependent Synaptic Wiring in the Mouse Cerebellar Cortex
Cesa, R., Premoselli, F., Renna, A., Ethell, I. M., Pasquale, E. B., & Strata, P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019160 · Cited by 18 · see citing works
The Ins and Outs of GluD2—Why and How Purkinje Cells Use the Special Glutamate Receptor
Yuzaki, M. (2011) · The Cerebellum · doi:10.1007/s12311-011-0328-4 · Cited by 7 · see citing works
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Trubetskoy, V., Pardiñas, A. F., Qi, T., Panagiotaropoulou, G., Awasthi, S., Bigdeli, T. B., Bryois, J., Chen, C.-Y., Dennison, C. A., Hall, L. S., et al. (2022) · Nature · doi:10.1038/s41586-022-04434-5 · Cited by 2,964 · see citing works
Synaptic Neurexin Complexes: A Molecular Code for the Logic of Neural Circuits
Südhof, T. C. (2017) · Cell · doi:10.1016/j.cell.2017.10.024 · Cited by 810 · see citing works
Towards an Understanding of Synapse Formation
Südhof, T. C. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.040 · Cited by 698 · see citing works
Specification of synaptic connectivity by cell surface interactions
de Wit, J., & Ghosh, A. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn.2015.3 · Cited by 410 · see citing works
The cell biology of synapse formation
Südhof, T. C. (2021) · Journal of Cell Biology · doi:10.1083/jcb.202103052 · Cited by 358 · see citing works
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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
Two Classes of Secreted Synaptic Organizers in the Central Nervous System
Yuzaki, M. (2018) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021317-121322 · Cited by 125 · see citing works
A synthetic synaptic organizer protein restores glutamatergic neuronal circuits
Suzuki, K., Elegheert, J., Song, I., Sasakura, H., Senkov, O., Matsuda, K., Kakegawa, W., Clayton, A. J., Chang, V. T.-C., Ferrer-Ferrer, M., et al. (2020) · Science · doi:10.1126/science.abb4853 · 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
Adhesion 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
Martinelli, D. C., Chew, K. S., Rohlmann, A., Lum, M. Y., Ressl, S., Hattar, S. S., Brünger, A. T., Missler, M., & Südhof, T. C. (2016) · Neuron · doi:10.1016/j.neuron.2016.07.002 · Cited by 98 · see citing works
RTN4/NoGo-receptor binding to BAI adhesion-GPCRs regulates neuronal development
Wang, J., Miao, Y., Wicklein, R., Sun, Z., Wang, J., Jude, K. M., Fernandes, R. A., Merrill, S. A., Wernig, M., García, K. C., et al. (2021) · Cell · doi:10.1016/j.cell.2021.10.016 · Cited by 99 · see citing works
Wang, X., Zhou, R., Xiong, Y., Zhou, L., Yan, X., Wang, M., Fan, L., Xie, C., Zhang, Y., Huang, Z., et al. (2021) · Cell Research · doi:10.1038/s41422-020-00451-z · Cited by 96 · see citing works
Rival, C. M., Xu, W., Shankman, L. S., Morioka, S., Arandjelovic, S., Lee, C. S., Wheeler, K. M., Smith, R. P., Haney, L. B., Isakson, B. E., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12406-z · Cited by 88 · see citing works
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Druart, M., & Magueresse, C. L. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00573 · Cited by 84 · see citing works
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Yuzaki, M. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.02.002 · Cited by 83 · see citing works
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Lala, T., & Hall, R. A. (2022) · Physiological Reviews · doi:10.1152/physrev.00027.2021 · Cited by 79 · see citing works
Latrophilin GPCR signaling mediates synapse formation
Sando, R. C., & Südhof, T. C. (2021) · eLife · doi:10.7554/elife.65717 · Cited by 75 · see citing works
Condomitti, G., Wierda, K. D. B., Schroeder, A., Rubio, S. E., Vennekens, K. M., Orlandi, C., Martemyanov, K. A., Gounko, N. V., Savas, J. N., & de Wit, J. (2018) · Neuron · doi:10.1016/j.neuron.2018.08.038 · Cited by 72 · see citing works
Structures of C1q-like Proteins Reveal Unique Features among the C1q/TNF Superfamily
Ressl, S., Vu, B. K., Vivona, S., Martinelli, D. C., Südhof, T. C., & Brünger, A. T. (2015) · Structure · doi:10.1016/j.str.2015.01.019 · Cited by 72 · 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
Tu, Y.-K., Duman, J. G., & Tolias, K. F. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.3461-17.2018 · Cited by 60 · see citing works
Hamoud, N., Tran, V., Aimi, T., Kakegawa, W., Lahaie, S. C., Thibault, M.-P., Pelletier, A., Wong, G. W., Kim, I.-S., Kania, A., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-06897-5 · Cited by 58 · see citing works
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Wang, C. Y., Liu, Z., Ng, Y. H., & Südhof, T. C. (2020) · Neuron · doi:10.1016/j.neuron.2020.04.004 · Cited by 57 · see citing works
Emerging Roles of BAI Adhesion-GPCRs in Synapse Development and Plasticity
Duman, J. G., Tu, Y.-K., & Tolias, K. F. (2016) · Neural Plasticity · doi:10.1155/2016/8301737 · Cited by 56 · see citing works
Gupta, R., Nguyen, D. C., Schaid, M. D., Lei, X., Balamurugan, A. N., Wong, G. W., Kim, J., Koltes, J. E., Kimple, M. E., & Bhatnagar, S. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.005403 · Cited by 55 · see citing works
Glutamate receptors in domestication and modern human evolution
O’Rourke, T., & Boeckx, C. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.10.004 · Cited by 50 · see citing works
Leung, C., & Wong, Y. (2017) · Molecules · doi:10.3390/molecules22071239 · Cited by 48 · see citing works
Emerging roles of adhesion G protein-coupled receptors
Rosa, M., Noel, T., Harris, M., & Ladds, G. (2021) · Biochemical Society Transactions · doi:10.1042/bst20201144 · Cited by 46 · see citing works
Synaptamide activates the adhesion GPCR GPR110 (ADGRF1) through GAIN domain binding
Huang, B. X., Hu, X., Kwon, H.-S., Fu, C., Lee, J., Southall, N. T., Marugán, J., & Kim, H. (2020) · Communications Biology · doi:10.1038/s42003-020-0831-6 · Cited by 44 · see citing works
Lai, S., Nakayama, H., Miyazaki, T., Nakazawa, T., Tabuchi, K., Hashimoto, K., Watanabe, M., & Kano, M. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.676891 · Cited by 40 · see citing works
Sticco, M. J., Palomino, P. A. P., Lukacsovich, D., Thompson, B. L., Földy, C., Ressl, S., & Martinelli, D. C. (2020) · The FASEB Journal · doi:10.1096/fj.202000351rr · Cited by 40 · see citing works
Extracellular matrix and synapse formation
Yang, L., Wei, M., Xing, B., & Zhang, C. (2022) · Bioscience Reports · doi:10.1042/bsr20212411 · Cited by 40 · see citing works
Modeling the quantitative nature of neurodevelopmental disorders using Collaborative Cross mice
Molenhuis, R. T., Bruining, H., Brandt, M. J. V., van Soldt, P. E., Atamni, H. J. A., Burbach, J. P. H., Iraqi, F. A., Mott, R., & Kas, M. J. (2018) · Molecular Autism · doi:10.1186/s13229-018-0252-2 · Cited by 33 · see citing works
Synapse biology in the ‘circuit-age’—paths toward molecular connectomics
Schreiner, D., Savas, J. N., Herzog, É., Brose, N., & de Wit, J. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.12.004 · Cited by 33 · see citing works
Purcell, R. H., Toro, C., Gahl, W. A., & Hall, R. A. (2017) · Human Mutation · doi:10.1002/humu.23336 · Cited by 28 · see citing works
Scuderi, C., Saccuzzo, L., Vinci, M., Castiglia, L., Galesi, O., Salemi, M., Mattina, T., Borgione, E., Città, S., Romano, C., et al. (2019) · European Journal of Human Genetics · doi:10.1038/s41431-018-0321-1 · Cited by 29 · see citing works
Liu, F., Tan, A., Yang, R., Xue, Y., Zhang, M., Chen, L., Xiao, L., Yang, X., & Yu, Y. (2016) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-016-2842-7 · Cited by 28 · see citing works
Sushi domain-containing protein 4 controls synaptic plasticity and motor learning
González-Calvo, I., Iyer, K., Carquin, M., Khayachi, A., Giuliani, F. A., Sigoillot, S. M., Vincent, J. D., Sevéno, M., Veleanu, M., Tahraoui, S., et al. (2021) · eLife · doi:10.7554/elife.65712 · Cited by 29 · see citing works
Versatile Signaling Activity of Adhesion GPCRs
Kishore, A., & Hall, R. A. (2016) · Handbook of experimental pharmacology · doi:10.1007/978-3-319-41523-9_7 · Cited by 26 · see citing works
Adhesion GPCR-Related Protein Networks
Knapp, B., & Uwe Wolfrum, B. (2016) · Handbook of experimental pharmacology · doi:10.1007/978-3-319-41523-9_8 · Cited by 26 · see citing works
Lu, X., Ding, F., Chen, Y., Ke, S., Yuan, S., Qiu, H., Xiao, L., & Yu, Y. (2022) · Endocrinology · doi:10.1210/endocr/bqac048 · Cited by 25 · see citing works
Paziewska, A., Habior, A., Rogowska, A., Zych, W., Goryca, K., Karczmarski, J., Dąbrowska, M., Ambrożkiewicz, F., Walewska‐Zielecka, B., Krawczyk, M., et al. (2017) · BMC Medical Genomics · doi:10.1186/s12920-016-0239-9 · Cited by 24 · see citing works
Anatomical and Behavioral Investigation of C1ql3 in the Mouse Suprachiasmatic Nucleus
Chew, K. S., Fernandez, D. C., Hattar, S. S., Südhof, T. C., & Martinelli, D. C. (2017) · Journal of Biological Rhythms · doi:10.1177/0748730417704766 · Cited by 23 · see citing works
Iung, L. H. D. S., Mulder, H. A., Neves, H. H. D. R., & Carvalheiro, R. (2018) · BMC Genomics · doi:10.1186/s12864-018-5003-4 · Cited by 23 · see citing works
Moon, S. Y., Shin, S.-A., Oh, Y., Park, H. H., & Lee, C. S. (2018) · Genes · doi:10.3390/genes9120597 · Cited by 21 · see citing works
Synaptic recognition molecules in development and disease
Chowdhury, D., Watters, K. E., & Biederer, T. (2021) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2020.12.009 · Cited by 23 · see citing works
Tan, A., Ke, S., Chen, Y., Chen, L., Lu, X., Ding, F., Yang, L., Tang, Y., & Yu, Y. (2019) · The FASEB Journal · doi:10.1096/fj.201801620rr · Cited by 21 · see citing works
Adhesion G protein-coupled receptor gluing action guides tissue development and disease
Sreepada, A., Tiwari, M., & Pal, K. (2022) · Journal of Molecular Medicine · doi:10.1007/s00109-022-02240-0 · Cited by 21 · see citing works
Aimi, T., Matsuda, K., & Yuzaki, M. (2023) · Molecular Brain · doi:10.1186/s13041-023-01048-4 · Cited by 23 · see citing works
Fu, C.-H., Han, X., Tong, L., Nie, P.-Y., Hu, Y., & Ji, L.-L. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113485 · Cited by 20 · see citing works
Unroe, K. A., Glover, M. E., Shupe, E. A., Feng, N., & Clinton, S. M. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.07.007 · Cited by 19 · see citing works
Gonda, X., Eszlári, N., Török, D., Gál, Z., Bokor, J., Millinghoffer, A., Baksa, D., Petschner, P., Antal, P., Breen, G. D., et al. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01436-1 · Cited by 19 · see citing works
Cell‐type‐specific visualisation and biochemical isolation of endogenous synaptic proteins in mice
Zhu, F., Collins, M., Harmse, J., Choudhary, J., Grant, S., & Komiyama, N. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14597 · Cited by 10 · see citing works
Qiu, X., Feng, J., Wang, F., Chen, P., Chen, X., Zhou, R., Chang, Y., Liu, J., & Zhao, Q. (2017) · Molecular Medicine Reports · doi:10.3892/mmr.2017.8210 · Cited by 18 · see citing works
The Purkinje cell as a model of synaptogenesis and synaptic specificity
Sassoé‐Pognetto, M., & Patrizi, A. (2016) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2016.10.004 · Cited by 18 · see citing works
Wang, X., Yang, Q., Zhou, X., Keene, C. D., Ryazanov, A. G., & Ma, T. (2024) · Alzheimer's & Dementia · doi:10.1002/alz.13916 · Cited by 17 · see citing works
C1ql1 is expressed in adult outer hair cells of the cochlea in a tonotopic gradient
Biswas, J., Pijewski, R. S., Makol, R., Miramontes, T. G., Thompson, B. L., Kresic, L. C., Burghard, A. L., Oliver, D. L., & Martinelli, D. C. (2021) · PLoS ONE · doi:10.1371/journal.pone.0251412 · Cited by 17 · see citing works
Complement drives circuit modulation in the adult brain
Parker, S. E., Bellingham, M. C., & Woodruff, T. M. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102282 · Cited by 18 · see citing works
What would a synthetic connectome look like?
Rabinowitch, I. (2019) · Physics of Life Reviews · doi:10.1016/j.plrev.2019.06.005 · Cited by 16 · see citing works
CTRP4 ablation impairs associative learning and memory
Sarver, D. C., Xu, C., Cheng, Y., Terrillion, C. E., & Wong, G. W. (2021) · The FASEB Journal · doi:10.1096/fj.202100733rr · Cited by 16 · see citing works
Liu, Z., Jiang, M., Liakath‐Ali, K., Sclip, A., Ko, J., Zhang, R. S., & Südhof, T. C. (2022) · eLife · doi:10.7554/elife.70664 · Cited by 15 · see citing works
Banerji, J. (2015) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2015.2285 · Cited by 16 · see citing works
Deletion of C1ql1 Causes Hearing Loss and Abnormal Auditory Nerve Fibers in the Mouse Cochlea
Qi, Y., Xiong, W., Yu, S., Du, Z., Qu, T., He, L., Wei, W., Zhang, L., Liu, K., Li, Y., et al. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.713651 · Cited by 15 · see citing works
CTRP14 inactivation alters physical activity and food intake response to fasting and refeeding
Sarver, D. C., Xu, C., Aja, S. M., & Wong, G. W. (2022) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00002.2022 · Cited by 14 · see citing works
CTRP11 contributes modestly to systemic metabolism and energy balance
Sarver, D. C., Xu, C., Carreno, D., Arking, A., Terrillion, C. E., Aja, S. M., & Wong, G. W. (2022) · The FASEB Journal · doi:10.1096/fj.202200189rr · Cited by 14 · see citing works
Sigoillot, S. M., Monk, K. R., Piao, X., Selimi, F., & Harty, B. L. (2016) · Handbook of experimental pharmacology · doi:10.1007/978-3-319-41523-9_12 · Cited by 14 · see citing works
González-Calvo, I., Cizeron, M., Bessereau, J., & Selimi, F. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.866444 · Cited by 11 · see citing works
Veleanu, M., Urrieta-Chávez, B., Sigoillot, S. M., Paul, M. A., Usardi, A., Iyer, K., Delagrange, M., Doyle, J., Heintz, N., Bécamel, C., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2122544119 · Cited by 13 · see citing works
Glover, M. E., McCoy, C. R., Shupe, E. A., Unroe, K. A., Jackson, N. L., & Clinton, S. M. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14315 · Cited by 13 · see citing works
Ramos, H., Bogdanov, P. M., Simó, R., Deàs-Just, A., & Hernández, C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms24010571 · Cited by 12 · see citing works
Alsharif, H. A., Latimer, M. N., Perez, K. C., Alexander, J., Rahman, M. M., Challa, A. K., Kim, J., Ramanadham, S., Young, M. E., & Bhatnagar, S. (2023) · Metabolites · doi:10.3390/metabo13060711 · Cited by 12 · see citing works
Generation and initial characterization of mice lacking full‐length BAI3 (ADGRB3) expression
Shiu, F. H., Wong, J. C., Bhattacharya, D., Kuranaga, Y., Parag, R. R., Alsharif, H. A., Bhatnagar, S., Meir, E. G. V., & Escayg, A. (2023) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/bcpt.13917 · Cited by 12 · see citing works
Park, D., Bae, S., Yoon, T. H., & Ko, J. (2018) · Europe PMC (PubMed Central) · doi:10.14348/molcells.2018.0081 · Cited by 12 · see citing works
Adhesion G protein-coupled receptors
Langenhan, T., Anderson, G. R., Araç, D., Aust, G., Avila-Zozaya, M., Bagger, S. M., Barth, P., Berndt, S., Blacklow, S. C., Blanco-Redondo, B., et al. (2026) · Pharmacological Reviews · doi:10.1016/j.pharmr.2026.100116 · Cited by 13 · see citing works
Genome-wide association studies (GWAS) and post-GWAS analyses of impulsivity: A systematic review
Wang, J., Gu, R., Kong, X., Luan, S., & Luo, Y. L. L. (2024) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2024.110986 · Cited by 11 · see citing works
Synaptic Gα12/13 signaling establishes hippocampal PV inhibitory circuits
Garbett, K. A., Tosun, B., Lopez, J. M., Smith, C. M., Honkanen, K., & Sando, R. C. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2407828121 · Cited by 11 · see citing works
Functional mosaic organization of neuroligins in neuronal circuits
Qin, L., Guo, S., Han, Y., Wang, X., & Zhang, B. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03478-y · Cited by 11 · see citing works
He, Z., Zhang, H., Li, X., Tu, S., Wang, Z., Han, S., Du, X., Shen, L., Li, N., & Liu, Q. (2022) · Phytomedicine · doi:10.1016/j.phymed.2022.154555 · Cited by 11 · see citing works
Mapping and targeting of C1ql1-expressing cells in the mouse
Moghimyfiroozabad, S., Paul, M. A., Sigoillot, S. M., & Selimi, F. (2023) · Scientific Reports · doi:10.1038/s41598-023-42924-2 · Cited by 10 · see citing works
Kakegawa, W., Paternain, A. V., Matsuda, K., Aller, M. I., Iida, I., Miura, E., Nozawa, K., Yamasaki, T., Sakimura, K., Yuzaki, M., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114427 · Cited by 10 · see citing works
C1ql1 expression in oligodendrocyte progenitor cells promotes oligodendrocyte differentiation
Altunay, Z. M., Biswas, J., Cheung, H. W., Pijewski, R. S., Papile, L. E., Akinlaja, Y. O., Tang, A., Kresic, L. C., Schouw, A. D., Ugrak, M. V., et al. (2024) · FEBS Journal · doi:10.1111/febs.17256 · Cited by 10 · see citing works
UNC-30/PITX coordinates neurotransmitter identity with postsynaptic GABA receptor clustering
Correa, E., Mialon, M., Cizeron, M., Bessereau, J., Pinan‐Lucarré, B., & Kratsios, P. (2024) · Development · doi:10.1242/dev.202733 · Cited by 10 · see citing works
CTRP13 ablation improves systemic glucose and lipid metabolism
Chen, F., Sarver, D. C., Saqib, M., Zhou, M., Aja, S. M., Seldin, M. M., & Wong, G. W. (2023) · Molecular Metabolism · doi:10.1016/j.molmet.2023.101824 · Cited by 9 · see citing works
Stepwise molecular specification of excitatory synapse diversity onto cerebellar Purkinje cells
Paul, M. A., Sigoillot, S. M., Marti, L., Quiroz, F. J. U., Delagrange, M., Cheung, H. W., Martinelli, D. C., Oriol, E., Hakim, V., Mailly, P., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01826-w · Cited by 10 · see citing works
Essential Role of Latrophilin-1 Adhesion GPCR Nanoclusters in Inhibitory Synapses
Matúš, D., Lopez, J. M., Sando, R. C., & Südhof, T. C. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1978-23.2024 · Cited by 8 · see citing works
Palomino, P. A. P., Black, K. C., & Ressl, S. (2023) · Biochemical Society Transactions · doi:10.1042/bst20220439 · Cited by 7 · see citing works
Structure of the complex of C1q-like 3 protein with adhesion-GPCR BAI3
Miao, Y., Wang, H., Jude, K. M., Wang, J., Wang, J., Wernig, M., & Südhof, T. C. (2025) · Communications Biology · doi:10.1038/s42003-025-08112-w · Cited by 7 · see citing works
Moghimyfiroozabad, S., Paul, M. A., Bellenger, L., & Selimi, F. (2024) · PLoS Biology · doi:10.1371/journal.pbio.3002655 · Cited by 8 · see citing works
Gao, Y., Chen, F., & Zhang, L. (2021) · Journal of Chemotherapy · doi:10.1080/1120009x.2021.1906035 · Cited by 7 · see citing works
Noncanonical Regulation of cAMP-dependent Insulin Secretion and Its Implications in Type 2 Diabetes
Ramanadham, S., Turk, J., & Bhatnagar, S. (2023) · Comprehensive Physiology · doi:10.1002/j.2040-4603.2023.tb00278.x · Cited by 10 · see citing works
Loss of CTRP10 results in female obesity with preserved metabolic healthPreprint
Chen, F., Sarver, D. C., Saqib, M., Vélez, L. M., Aja, S. M., Seldin, M. M., & Wong, G. W. (2024) · eLife · doi:10.7554/elife.93373.3 · Cited by 7 · see citing works
Noncanonical Regulation of cAMP‐Dependent Insulin Secretion and Its Implications in Type 2 Diabetes
Ramanadham, S., TURK, J. W., & Bhatnagar, S. (2023) · Comprehensive physiology · doi:10.1002/cphy.c220031 · Cited by 6 · see citing works
Pan, Y., Cai, Z., Wang, Y., Zhang, J., Sheng, H., Shao, D., Cui, D., Guo, X., Zheng, P., & Lai, B. (2024) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2024.150076 · Cited by 5 · see citing works
The spiny relationship between parallel fibers, climbing fibers, and Purkinje cells
Masoli, S., Rizza, M. F., Moccia, F. D., & D'Angelo, E. U. (2025) · Frontiers in Physiology · doi:10.3389/fphys.2025.1671271 · Cited by 5 · see citing works
Meyer, C. M., Vafaeva, O., Low, H., Speca, D. J., & Dı́az, E. (2025) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2025.104015 · Cited by 5 · see citing works
Kano, M., & Watanabe, M. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814411-4.00004-4 · Cited by 5 · see citing works
C1QL1/CTRP14 Is Largely Dispensable for Atherosclerosis Formation in Apolipoprotein-E-Deficient Mice
Guan, H., Shi, T., Liu, M., Wang, X., & Guo, F. (2022) · Journal of Cardiovascular Development and Disease · doi:10.3390/jcdd9100341 · Cited by 5 · see citing works
Patient mutations in DRP1 perturb synaptic maturation of cortical neuronsPreprint
Baum, T., Bodnya, C., Costanzo, J., & Gama, V. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.08.23.609462 · Cited by 5 · see citing works
Structural basis of calcium-dependent C1ql1/BAI3 assemblies in synaptic connectivity
Liao, L., Han, Y., Niu, F., Wang, Y., Lu, Y., Xu, S., Zhu, H., Lin, L., Xiao, J., Tou, H. I., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-66254-1 · Cited by 4 · see citing works
- Authors
- Sigoillot, S. M., Iyer, K., Binda, F., González-Calvo, I., Talleur, M., Vodjdani, G., Isope, P., & Selimi, F.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Inserm (FR)
- Corresponding author
- Selimi, Fekrije
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2015-02
- Volume
- 10
- Issue
- 5
- Pages
- 820-832
- ISSN
- 2211-1247 (ISSN-L)
- OpenAlex
- W1997258848
- Cited by
- 144
- References
- 39
- Citations by year
- 2026: 13 · 2025: 13 · 2024: 16 · 2023: 11 · 2022: 16 · 2021: 18 · 2020: 9 · 2019: 9 · 2018: 11 · 2017: 11 · 2016: 13 · 2015: 4
- FWCI
- 6.06
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by-nc-nd)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- univOAK (4 institutions : Université de Strasbourg, Université de Haute Alsace, INSA Strasbourg, Bibliothèque Nationale et Universitaire de Strasbourg) (submittedVersion, cc-by-nc-nd)
- Funders
- Agence Nationale de la Recherche (10-LABX-54, ANR-11-IDEX-0001, ANR11IDEX000102, ANR–10–LABX–54, ANR-11IDEX-0001-02 PSL, ANR-10-IDEX-0001, ANR-11-IDEX, ANR-13-SAMA-0010, ANR-10, IDEX-0001-02)
- Centre National de la Recherche Scientifique (ANR-11-IDEX-0001-02)
- Interreg
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- C1QL1, BAI3, Purkinje cells, synaptic connectivity, synaptogenesis, adhesion GPCRs, brain development
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