Calcium influx through L-type CaV1.2 Ca2+ channels regulates mandibular development
Open accessAbstract
The identification of a gain-of-function mutation in CACNA1C as the cause of Timothy Syndrome (TS), a rare disorder characterized by cardiac arrhythmias and syndactyly, highlighted unexpected roles for the L-type voltage-gated Ca2+ channel CaV1.2 in nonexcitable cells. How abnormal Ca2+ influx through CaV1.2 underlies phenotypes such as the accompanying syndactyly or craniofacial abnormalities in the majority of affected individuals is not readily explained by established CaV1.2 roles. Here, we show that CaV1.2 is expressed in the first and second pharyngeal arches within the subset of cells that give rise to jaw primordia. Gain-of-function and loss-of-function studies in mouse, in concert with knockdown/rescue and pharmacological approaches in zebrafish, demonstrated that Ca2+ influx through CaV1.2 regulates jaw development. Cranial neural crest migration was unaffected by CaV1.2 knockdown, suggesting a role for CaV1.2 later in development. Focusing on the mandible, we observed that cellular hypertrophy and hyperplasia depended upon Ca2+ signals through CaV1.2, including those that activated the calcineurin signaling pathway. Together, these results provide new insights into the role of voltage-gated Ca2+ channels in nonexcitable cells during development.
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Timothy Syndrome-causing point mutations in CACNA1C disrupt development of neuronal dendrites, bone, and skin, and also affect ongoing electrical function in heart and brain.
“For example, point mutations in CACNA1C that underlie Timothy Syndrome perturb the development of neuronal dendrites (Krey and Dolmetsch, 2007), bones (Ramachandran et al., 2013), and skin (Yucel et al., 2013), as well as ongoing electrophysiological function of heart and brain (Krey and Dolmetsch, 2007; Splawski et al., 2005; Splawski et al., 2004).”
From Unifying Views of Autism Spectrum Disorders: A Consideration of Autoregulatory Feedback Loops (2016) · cites this paper as Ramachandran et al., 2013
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CaV1.2 Calcium Channel Dysfunction Causes a Multisystem Disorder Including Arrhythmia and Autism
Splawski, I., Timothy, K. W., Sharpe, L. M., Decher, N., Kumar, P., Bloise, R., Napolitano, C., Schwartz, P. J., Joseph, R. M., Condouris, K., et al. (2004) · Cell · doi:10.1016/j.cell.2004.09.011 · Cited by 1,586 · see citing works
Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis
Chai, Y., Jiang, X., Ito, Y., Bringas, P., Han, J., Rowitch, D. H., Soriano, P. M., McMahon, A. P., & Sucov, H. M. (2000) · Development · doi:10.1242/dev.127.8.1671 · Cited by 1,464 · see citing works
Matrix-embedded cells control osteoclast formation
Xiong, J., Onal, M., Jilka, R. L., Weinstein, R. S., Manolagas, S. C., & O'Brien, C. A. (2011) · Nature Medicine · doi:10.1038/nm.2448 · Cited by 1,304 · see citing works
Expression of Cre recombinase in the developing mouse limb bud driven by a Prxl enhancer
Logan, M., Martin, J. F., Nagy, A., Lobe, C., Olson, E., & Tabin, C. (2002) · Genesis · doi:10.1002/gene.10092 · Cited by 1,022 · see citing works
FK-506- and CsA-sensitive activation of the interleukin-2 promoter by calcineurin
O’Keefe, S. J., Tamura, J., Kincaid, R. L., Tocci, M. J., & O’Neill, E. A. (1992) · Nature · doi:10.1038/357692a0 · Cited by 841 · see citing works
Primary culture and phenotyping of murine chondrocytes
Gosset, M., Berenbaum, F., Thirion, S., & Jacques, C. (2008) · Nature Protocols · doi:10.1038/nprot.2008.95 · Cited by 735 · see citing works
Zebrafish : a practical approach
Nüsslein‐Volhard, C., & Dahm, R. (2002) · Cited by 697 · see citing works
Connexin 43 (GJA1) Mutations Cause the Pleiotropic Phenotype of Oculodentodigital Dysplasia
Paznekas, W. A., Boyadjiev, S. A., Shapiro, R. E., Daniëls, O., Wollnik, B., Keegan, C. E., Innis, J. W., Dinulos, M. B., Christian, C., Hannibal, M., et al. (2003) · The American Journal of Human Genetics · doi:10.1086/346090 · Cited by 620 · see citing works
Molecular determinants of Ca2+ selectivity and ion permeation in L-type Ca2+ channels
Yang, J., Elllnor, P. T., Sather, W. A., Zhang, J.-F., & Tsien, R. W. (1993) · Nature · doi:10.1038/366158a0 · Cited by 617 · see citing works
(2002) · doi:10.1093/oso/9780199638086.001.0001 · Cited by 589 · see citing works
Using iPSC-derived neurons to uncover cellular phenotypes associated with Timothy syndrome
Paşca, S. P., Portmann, T., Voineagu, I., Yazawa, M., Shcheglovitov, A., Paşca, A. M., Cord, B., Palmer, T. D., Chikahisa, S., Nishino, S., et al. (2011) · Nature Medicine · doi:10.1038/nm.2576 · Cited by 585 · see citing works
Self-citationCalcium–calcineurin signaling in the regulation of cardiac hypertrophy
Wilkins, B. J., & Molkentin, J. D. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.07.121 · Cited by 439 · see citing works
Calcineurin/NFAT Signaling in Osteoblasts Regulates Bone Mass
Winslow, M. M., Pan, M., Starbuck, M. W., Gallo, E. M., Deng, L., Karsenty, G., & Crabtree, G. R. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.04.006 · Cited by 354 · see citing works
Aliprantis, A. O., Ueki, Y., Sulyanto, R. M., Park, A., Sigrist, K. S., Sharma, S. M., Ostrowski, M. C., Olsen, B. R., & Glimcher, L. H. (2008) · Journal of Clinical Investigation · doi:10.1172/jci35711 · Cited by 346 · see citing works
Oliveria, S. F., Dell'Acqua, M. L., & Sather, W. A. (2007) · Neuron · doi:10.1016/j.neuron.2007.06.032 · Cited by 344 · see citing works
A field of myocardial-endocardial NFAT signaling underlies heart valve morphogenesis
Chang, C.-P., Neilson, J. R., Bayle, J. H., Gestwicki, J. E., Kuo, A., Stankunas, K., Graef, I. A., & Crabtree, G. R. (2004) · Cell · doi:10.1016/j.cell.2004.08.010 · Cited by 331 · see citing works
A direct role for Sox10 in specification of neural crest-derived sensory neurons
Carney, T. J., Dutton, K. A., Greenhill, E., Delfino-Machín, M., Dufourcq, P., Blader, P., & Kelsh, R. N. (2006) · Development · doi:10.1242/dev.02668 · Cited by 307 · see citing works
Quantitative proteomics of the Cav2 channel nano-environments in the mammalian brain
Müller, C. S., Haupt, A., Bildl, W., Schindler, J., Knaus, H., Meissner, M., Rammner, B., Striessnig, J., Flockerzi, V., Fakler, B., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005940107 · Cited by 299 · see citing works
Functional Modulation of Cardiac Form through Regionally Confined Cell Shape Changes
Auman, H. J., Coleman, H., Riley, H. E., Olale, F., Tsai, H., & Yelon, D. L. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050053 · Cited by 286 · see citing works
Seisenberger, C., Specht, V., Welling, A., Platzer, J., Pfeifer, A., Kühbandner, S., Striessnig, J., Klugbauer, N., Feil, R., & Hofmann, F. B. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m006467200 · Cited by 269 · see citing works
Rottbauer, W., Baker, K. H., Wo, Z. G., Mohideen, M.-A. P. K., Cantiello, H. F., & Fishman, M. C. (2001) · Developmental Cell · doi:10.1016/s1534-5807(01)00023-5 · Cited by 197 · see citing works
Collazo, A., Bronner-Fraser, M. E., & Fraser, S. E. (1993) · Development · doi:10.1242/dev.118.2.363 · Cited by 194 · see citing works
Identification of the Components Controlling Inactivation of Voltage-Gated Ca2+ Channels
Kim, J., Ghosh, S., Nunziato, D. A., & Pitt, G. S. (2004) · Neuron · doi:10.1016/s0896-6273(04)00081-9 · Cited by 160 · see citing works
Self-citationRelationship between Neural Crest Cells and Cranial Mesoderm during Head Muscle Development
Grenier, J., Teillet, M., Grifone, R., Kelly, R. G., & Duprez, D. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004381 · Cited by 149 · see citing works
Wnt11 patterns a myocardial electrical gradient through regulation of the L-type Ca2+ channel
Panáková, D., Werdich, A. A., & MacRae, C. A. (2010) · Nature · doi:10.1038/nature09249 · Cited by 139 · see citing works
BMP signals control limb bud interdigital programmed cell death by regulating FGF signaling
Pajni-Underwood, S., Wilson, C. P., Elder, C., Mishina, Y. M., & Lewandoski, M. B. (2007) · Development · doi:10.1242/dev.001677 · Cited by 132 · see citing works
A new form of long QT syndrome associated with syndactyly
Marks, M. L., Whisler, S. L., Clericuzio, C. L., & Keating, M. T. (1995) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(94)00318-k · Cited by 117 · see citing works
Physical and Functional Interaction Between Calcineurin and the Cardiac L-Type Ca 2+ Channel
Tandan, S., Wang, Y., Wang, T. T., Jiang, N., Hall, D. D., Hell, J. W., Luo, X., Rothermel, B. A., & Hill, J. A. (2009) · Circulation Research · doi:10.1161/circresaha.109.199828 · Cited by 112 · see citing works
Calcium influx through Cav1.2 is a proximal signal for pathological cardiomyocyte hypertrophy
Chen, X., Nakayama, H., Zhang, X., Ai, X., Harris, D. M., Tang, M., Zhang, H., Szeto, C., Stockbower, K., Berretta, R. M., et al. (2010) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2010.11.012 · Cited by 107 · see citing works
Bohnsack, B. L., Gallina, D., & Kahana, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022991 · Cited by 67 · see citing works
Ebert, A. M., McAnelly, C. A., Srinivasan, A., Linker, J. L., Horne, W. A., & Garrity, D. M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707948105 · Cited by 33 · see citing works
In Vivo Calcium Dynamics During Neural Crest Cell Migration and Patterning Using GCaMP3
McKinney, M. C., & Kulesa, P. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.08.004 · Cited by 29 · see citing works
Moran, D. J. (1991) · American Journal of Anatomy · doi:10.1002/aja.1001920103 · Cited by 24 · see citing works
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Zamponi, G., Striessnig, J., Koschak, A., & Dolphin, A. (2015) · Pharmacological Reviews · doi:10.1124/pr.114.009654 · Cited by 1,004 · see citing works
Genetic disruption of voltage-gated calcium channels in psychiatric and neurological disorders
Heyes, S., Pratt, W. S., Rees, E., Dahimène, S., Ferron, L., Owen, M. J., & DOLPHIN, A. C. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.09.002 · Cited by 234 · see citing works
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Nishimura, Y., Inoue, A., Sasagawa, S., Koiwa, J., Kawaguchi, K., Kawase, R., Maruyama, T., Kim, S., & Tanaka, T. (2015) · Congenital Anomalies · doi:10.1111/cga.12142 · Cited by 203 · see citing works
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Adams, D. S., Uzel, S. G. M., Akagi, J., Włodkowic, D., Andreeva, V., Yelick, P. C., Devitt‐Lee, A., Paré, J., & Levin, M. G. (2016) · The Journal of Physiology · doi:10.1113/jp271930 · Cited by 129 · see citing works
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Doyle, J. J., Doyle, A. J., Wilson, N. K., Habashi, J. P., Bedja, D., Whitworth, R., Lindsay, M. E., Schoenhoff, F., Myers, L. A., Huso, N., et al. (2015) · eLife · doi:10.7554/elife.08648 · Cited by 122 · see citing works
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Dick, I. E., Joshi-Mukherjee, R., Yang, W.-J., & Yue, D. T. (2016) · Nature Communications · doi:10.1038/ncomms10370 · Cited by 97 · see citing works
Wemhöner, K., Friedrich, C., Stallmeyer, B., Coffey, A. J., Grace, A. A., Zumhagen, S., Seebohm, G., Ortiz‐Bonnin, B., Rinné, S., Sachse, F. B., et al. (2015) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2015.01.002 · Cited by 91 · see citing works
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Zhang, Q., Chen, J.-J., Qin, Y., Wang, J.-J., & Zhou, L. (2018) · Channels · doi:10.1080/19336950.2018.1499368 · Cited by 74 · see citing works
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Davis, E. E., Frangakis, S. G., & Katsanis, N. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2014.05.024 · Cited by 75 · see citing works
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Pitt, G. S., Matsui, M., & Cao, C. (2020) · Annual Review of Physiology · doi:10.1146/annurev-physiol-031620-091043 · Cited by 71 · see citing works
Self-citationDougnon, G., & Matsui, H. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23147550 · Cited by 71 · see citing works
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Self-citationLaGuardia, J. S., Shariati, K., Bedar, M., Ren, X., Moghadam, S., Huang, K. X., Chen, W., Kang, Y., Yamaguchi, D. T., & Lee, J. C. (2023) · Advanced Healthcare Materials · doi:10.1002/adhm.202301081 · Cited by 42 · see citing works
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Zhang, Z., Hao, Z., Xian, C., Zhang, J., & Wu, J. (2023) · Chemical Engineering Journal · doi:10.1016/j.cej.2023.145061 · Cited by 30 · see citing works
Giudicessi, J. R., & Ackerman, M. J. (2016) · Circulation Arrhythmia and Electrophysiology · doi:10.1161/circep.116.002480 · Cited by 30 · see citing works
Sørhus, E., Incardona, J. P., Furmanek, T., Jentoft, S., Meier, S., & Edvardsen, R. B. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.02.012 · Cited by 24 · see citing works
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Ozekin, Y. H., Isner, T. J., & Bates, E. A. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00099 · Cited by 21 · see citing works
Andersen, N. D., Ramachandran, K. V., Bao, M., Kirby, M. L., Pitt, G. S., & Hutson, M. R. (2014) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2014.12.016 · Cited by 21 · see citing works
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Self-citationLaugel-Haushalter, V., Morkmued, S., Stoetzel, C., Geoffroy, V., Muller, J., Boland, A., Deleuze, J., Chennen, K., Pitiphat, W., Dollfus, H., et al. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01329 · Cited by 15 · see citing works
Current updates on arrhythmia within Timothy syndrome: genetics, mechanisms and therapeutics
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Alam, S., Sargeant, M. S., Patel, R., & Jayaram, P. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13226641 · Cited by 14 · see citing works
Li, C., Korcari, A., Ciufo, D. J., Mendias, C. L., Rodeo, S. A., Buckley, M. R., Loiselle, A. E., Pitt, G. S., & Cao, C. (2023) · The FASEB Journal · doi:10.1096/fj.202300607r · Cited by 13 · see citing works
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Scala, M., Khan, K., Bénéteau, C., Fox, R. G., Hardenberg, S. V., Khan, A., Joubert, M., Fievet, L., Musquer, M. D., Vaillant, C. L., et al. (2023) · Genetics in Medicine · doi:10.1016/j.gim.2023.101057 · Cited by 9 · see citing works
Chatterjee, D., Mahabir, S., Chatterjee, D., & Gerlai, R. T. (2021) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2021.110327 · Cited by 8 · see citing works
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Shrestha, A., More, C. B., Keshwar, S., Shrestha, B., & Raut, T. (2019) · Current Oral Health Reports · doi:10.1007/s40496-019-00223-8 · Cited by 3 · see citing works
Chen, Q., Pan, Y., Hu, Y., Chen, G., Chen, X., Xie, Y., Wang, M., Li, Z., Huang, J. C., Shi, Y., et al. (2024) · Eye and Vision · doi:10.1186/s40662-024-00401-5 · Cited by 3 · see citing works
Zebrafish: A Model System to Study the Architecture of Human Genetic Disease
Davis, E. E., & Katsanis, N. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809468-6.00025-5 · Cited by 3 · see citing works
The influence of calcium signaling on the development of autism spectrum disorders
Solovieva, N. V., Витальевна, Ч. С., Kichuk, I. V., & Макарова, Е. В. (2020) · Zhurnal «Patologicheskaia fiziologiia i eksperimental`naia terapiia» · doi:10.25557/0031-2991.2020.04.106-117 · Cited by 2 · see citing works
Inherited Ventricular Arrhythmia in Zebrafish: Genetic Models and Phenotyping Tools
Sieliwończyk, E., Matchkov, V. V., Vandendriessche, B., Alaerts, M., Bakkers, J., Loeys, B., & Schepers, D. (2021) · Reviews of physiology, biochemistry and pharmacology · doi:10.1007/112_2021_65 · Cited by 3 · see citing works
A bioelectrical phase transition patterns the first beats of a vertebrate heartPreprint
Jia, B., Qi, Y., Wong-Campos, J. D., Megason, S. G., & Cohen, A. E. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.12.06.519309 · Cited by 3 · see citing works
Luo, P., Zhao, S., Zhang, Z., Guo, R. Z., & Zhang, Q. (2025) · Scientific Reports · doi:10.1038/s41598-025-04557-5 · Cited by 2 · see citing works
Zhu, Y., Wagener, F. A. D. T. G., Metz, J. R., & den Hoff, J. W. V. (2026) · Bone · doi:10.1016/j.bone.2026.117926 · Cited by 2 · see citing works
Voltage-gated calcium channels (CaV) in GtoPdb v.2021.3
Catterall, W., Perez-Reyes, E., Snutch, T., & Striessnig, J. (2021) · IUPHAR/BPS Guide to Pharmacology CITE · doi:10.2218/gtopdb/f80/2021.3 · Cited by 2 · see citing works
Napolitano, C., Timothy, K. W., Bloise, R., & Priori, S. G. (2021) · Cited by 2 · see citing works
Voltage-gated calcium channels in GtoPdb v.2021.2
Catterall, W., Perez-Reyes, E., Snutch, T., & Striessnig, J. (2021) · IUPHAR/BPS Guide to Pharmacology CITE · doi:10.2218/gtopdb/f80/2021.2 · Cited by 2 · see citing works
Excitation–Contraction Coupling in the Goldfish (Carassius auratus) Intact Heart
Bazmi, M., & Escobar, A. L. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.01103 · Cited by 2 · see citing works
Voltage-gated calcium channels (version 2020.5) in the IUPHAR/BPS Guide to Pharmacology Database
Catterall, W., Perez-Reyes, E., Snutch, T., & Striessnig, J. (2020) · IUPHAR/BPS Guide to Pharmacology CITE · doi:10.2218/gtopdb/f80/2020.5 · Cited by 2 · see citing works
Rhythm Genes Sing More Than One Tune
Akhirome, E., & Jay, P. Y. (2015) · Circulation Arrhythmia and Electrophysiology · doi:10.1161/circep.115.002834 · Cited by 2 · see citing works
Banono, N. S., Gaweł, K., Mäki‐Marttunen, T., van der Ent, W., Kukula-Koch, W. A., Fyhn, M., Einevoll, G. T., Andreassen, O. A., & Esguerra, C. V. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.30.462600 · Cited by 2 · see citing works
Kurata, T., Suzuki, Y., Tateno, S., Miyaki, S., Kondo, R., Bernotienė, E., Mobasheri, A., Giles, W. R., Imaizumi, Y., & Yamamura, H. (2026) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00381.2025 · Cited by 1 · see citing works
Zu, Y., Jia, H., Wang, B., Xu, H., He, H., & Chen, L. (2026) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2026.04.003 · Cited by 1 · see citing works
Semenova, S. A., Sams, A. M., Nammi, D., Menold, M. T., Margolin, G., Sinclair, J. L., Robertson, K. A., Larkin, K. A., Kelly, S., Golden, A., et al. (2026) · Communications Biology · doi:10.1038/s42003-026-10657-3 · Cited by 1 · see citing works
- Authors
- Ramachandran, K. V., Hennessey, J. A., Barnett, A. S., Yin, X., Stadt, H. A., Foster, E., Shah, R. A., Yazawa, M., Dolmetsch, R. E., Kirby, M. L., & Pitt, G. S.
- Affiliations
- Duke Medical Center (US)
- Duke University (US)
- Stanford Medicine (US)
- Corresponding author
- Pitt, Geoffrey S.
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2013-03-15
- Volume
- 123
- Issue
- 4
- Pages
- 1638-1646
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC3613930
- OpenAlex
- W2123350196
- Cited by
- 75
- References
- 33
- Citations by year
- 2026: 4 · 2025: 1 · 2024: 4 · 2023: 8 · 2022: 6 · 2021: 11 · 2020: 10 · 2019: 5 · 2018: 5 · 2017: 3 · 2016: 5 · 2015: 10 · 2014: 3
- FWCI
- 2.67
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- March of Dimes Foundation
- American Heart Association
- University of Pittsburgh
- National Heart, Lung, and Blood Institute (T32HL007101, R01HL071165)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Craniofacial Disorders and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- CACNA1C, Timothy syndrome, mandibular growth, branchial arches, craniofacial anomalies, syndactyly, calcium influx, calcineurin signaling, cell hypertrophy, non-excitable cells
- MeSH terms
- Animals, Autistic Disorder, Branchial Region, Cell Movement, Cells, Cultured, Embryo, Mammalian, Embryo, Nonmammalian, Heart, Humans, Hyperplasia, Hypertrophy, Long QT Syndrome, Mandible, Mice, Inbred C57BL, Neural Crest, Stem Cells, Syndactyly, Zebrafish, Gene Expression, Calcineurin, Calcium Signaling, Mutation, Missense, Calcium Channels, L-Type, Zebrafish Proteins, Mice, Gene Knockdown Techniques, Mice, 129 Strain, Morpholinos
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 ›
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