Neurulation and neurite extension require the zinc transporter ZIP12 ( slc39a12 )
Open accessAbstract
Zn 2+ is required for many aspects of neuronal structure and function. However, the regulation of Zn 2+ in the nervous system remains poorly understood. Systematic analysis of tissue-profiling microarray data showed that the zinc transporter ZIP12 ( slc39a12 ) is highly expressed in the human brain. In the work reported here, we confirmed that ZIP12 is a Zn 2+ uptake transporter with a conserved pattern of high expression in the mouse and Xenopus nervous system. Mouse neurons and Neuro-2a cells produce fewer and shorter neurites after ZIP12 knockdown without affecting cell viability. Zn 2+ chelation or loading in cells to alter Zn 2+ availability respectively mimicked or reduced the effects of ZIP12 knockdown on neurite outgrowth. ZIP12 knockdown reduces cAMP response element-binding protein activation and phosphorylation at serine 133, which is a critical pathway for neuronal differentiation. Constitutive cAMP response element-binding protein activation restores impairments in neurite outgrowth caused by Zn 2+ chelation or ZIP12 knockdown. ZIP12 knockdown also reduces tubulin polymerization and increases sensitivity to nocodazole following neurite outgrowth. We find that ZIP12 is expressed during neurulation and early nervous system development in Xenopus tropicalis, where ZIP12 antisense morpholino knockdown impairs neural tube closure and arrests development during neurulation with concomitant reduction in tubulin polymerization in the neural plate. This study identifies a Zn 2+ transporter that is specifically required for nervous system development and provides tangible links between Zn 2+ , neurulation, and neuronal differentiation.
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?
Deficiencies in maternal zinc during pregnancy can be harmful to fetal development, have been identified as causal in neural tube defects, and may contribute to ASD risk.
“Deficiencies in maternal zinc during pregnancy can be harmful to fetal development having been identified as causal in neural tube defects and as possibly contributing to ASD risk [168, 169].”
From The contribution of environmental exposure to the etiology of autism spectrum disorder (2019) · cites this paper as [169]
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
The neurobiology of zinc in health and disease
Frederickson, C. J., Koh, J., & Bush, A. I. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1671 · Cited by 1,841 · see citing works
Barco, A., Alarcon, J. M., & Kandel, E. (2002) · Cell · doi:10.1016/s0092-8674(02)00657-8 · Cited by 595 · see citing works
Parallel Patterns of Evolution in the Genomes and Transcriptomes of Humans and Chimpanzees
Khaitovich, P., Hellmann, I., Enard, W., Nowick, K., Leinweber, M., Franz, H., Weiß, G., Lachmann, M., & Pääbo, S. (2005) · Science · doi:10.1126/science.1108296 · Cited by 590 · see citing works
Measurement of Intracellular Free Zinc in Living Cortical Neurons: Routes of Entry
Sensi, S. L., Canzoniero, L. M. T., Yu, S. P., Ying, H. S.-C., Koh, J., Kerchner, G. A., & Choi, D. W. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-24-09554.1997 · Cited by 465 · see citing works
Ames, B. N. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608757103 · Cited by 411 · see citing works
The SLC39 family of metal ion transporters
Eide, D. J. (2004) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-003-1074-3 · Cited by 405 · see citing works
Ho, E., & Ames, B. N. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.222679399 · Cited by 389 · see citing works
Zinc transporter LIVI controls epithelial-mesenchymal transition in zebrafish gastrula organizer
Yamashita, S., Miyagi, C., Fukada, T., Kagara, N., Che, Y., & Hirano, T. (2004) · Nature · doi:10.1038/nature02545 · Cited by 352 · see citing works
Functional Significance of Zinc-Related Signaling Pathways in Immune Cells
Haase, H., & Rink, L. (2009) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-080508-141119 · Cited by 323 · see citing works
Systematic discovery of nonobvious human disease models through orthologous phenotypes
McGary, K. L., Park, T. J., Woods, J. O., Ji, H. Y., Wallingford, J. B., & Marcotte, E. M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910200107 · Cited by 292 · see citing works
Fukada, T., Civic, N., Furuichi, T., Shimoda, S., Mishima, K., Higashiyama, H., Idaira, Y., Asada, Y., Kitamura, H., Yamasaki, S., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003642 · Cited by 287 · see citing works
Differentiation of mouse Neuro 2A cells into dopamine neurons
Tremblay, R. G., Sikorska, M., Sandhu, J. K., Lanthier, P. H., Ribecco‐Lutkiewicz, M., & Bani‐Yaghoub, M. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.11.004 · Cited by 280 · see citing works
Zinc Deficiency Affects DNA Damage, Oxidative Stress, Antioxidant Defenses, and DNA Repair in Rats
Song, Y., Leonard, S. W., Traber, M. G., & Ho, E. (2009) · Journal of Nutrition · doi:10.3945/jn.109.106369 · Cited by 251 · see citing works
Giunta, C., Elçioglu, N. H., Albrecht, B., Eich, G., Chambaz, C., Janecke, A. R., Yeowell, H., Weis, M., Eyre, D. R., Kraenzlin, M., et al. (2008) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2008.05.001 · Cited by 218 · see citing works
A comprehensive functional analysis of tissue specificity of human gene expression
Dezső, Z., Nikolsky, Y., Sviridov, E., Shi, W., Serebriyskaya, T., Dosymbekov, D., Bugrim, A. E., Rakhmatulin, E. A., Brennan, R., Guryanov, A., et al. (2008) · BMC Biology · doi:10.1186/1741-7007-6-49 · Cited by 213 · see citing works
Rapid effects of retinoic acid on CREB and ERK phosphorylation in neuronal cells
Cañón, E., Cosgaya, J. M., Scsucova, S., & Aranda, A. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-05-0439 · Cited by 184 · see citing works
Crouch, P. J., Savva, M. S., Hung, L. W., Donnelly, P. S., Mot, A. I., Parker, S. J., Greenough, M. A., Volitakis, I., Adlard, P. A., Cherny, R. A., et al. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07402.x · Cited by 183 · see citing works
Aydemir, T. B., Chang, S.-M., Guthrie, G. J., Maki, A. B., Ryu, M., Karabıyık, A., & Cousins, R. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048679 · Cited by 183 · see citing works
Zinc and reproduction: effects of zinc deficiency on prenatal and early postnatal development
Uriu‐Adams, J. Y., & Keen, C. L. (2010) · Birth Defects Research Part B Developmental and Reproductive Toxicology · doi:10.1002/bdrb.20264 · Cited by 166 · see citing works
Self-citationGene expression in the embryonic nervous system of Xenopus laevis.
Richter, K., Grunz, H., & Dawid, I. B. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.21.8086 · Cited by 165 · see citing works
Proteomic Mapping of Brain Plasma Membrane Proteins
Nielsen, P. A., Olsen, J. V., Podtelejnikov, A. V., Andersen, J. R., Mann, M., & Wiśniewski, J. R. (2005) · Molecular & Cellular Proteomics · doi:10.1074/mcp.t500002-mcp200 · Cited by 161 · see citing works
Clioquinol and pyrithione activate TRPA1 by increasing intracellular Zn 2+
Andersson, D. A., Gentry, C., Moss, S., & Bevan, S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812675106 · Cited by 136 · see citing works
Prediction of Human Disease Genes by Human-Mouse Conserved Coexpression Analysis
Ala, U., Piro, R. M., Grassi, E., Damasco, C., Silengo, L., Oti, M., Provero, P., & Di Cunto, F. (2008) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000043 · Cited by 134 · see citing works
Zinc-stimulated Endocytosis Controls Activity of the Mouse ZIP1 and ZIP3 Zinc Uptake Transporters
Wang, F., Dufner‐Beattie, J., Kim, B., Petris, M. J., Andrews, G. K., & Eide, D. J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m400680200 · Cited by 133 · see citing works
Dufner‐Beattie, J., Weaver, B. P., Geiser, J., Bilgen, M., Larson, M. A., Xu, W., & Andrews, G. K. (2007) · Human Molecular Genetics · doi:10.1093/hmg/ddm088 · Cited by 123 · see citing works
MTF-1-Mediated Repression of the Zinc Transporter Zip10 Is Alleviated by Zinc Restriction
Lichten, L. A., Ryu, M., Guo, L., Embury, J. E., & Cousins, R. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021526 · Cited by 115 · see citing works
Velie, E. M., Block, G., Shaw, G. M., Samuels, S. J., Schaffer, D. M., & Kulldorff, M. (1999) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a010059 · Cited by 107 · see citing works
Stathakis, D. G., Burton, D. Y., McIvor, W. E., Krishnakumar, S., Wright, T. R. F., & O’Donnell, J. M. (1999) · Genetics · doi:10.1093/genetics/153.1.361 · Cited by 102 · see citing works
Calcium and neurulation in mammalian embryos
Smedley, M. J., & Stanisstreet, M. (1985) · Development · doi:10.1242/dev.89.1.1 · Cited by 100 · see citing works
Gao, H., Zheng, W., Xin, N., Chi, Z., Wang, Z., Chen, J., & Wang, Z. (2009) · Neurotoxicity Research · doi:10.1007/s12640-009-9072-7 · Cited by 85 · see citing works
Aydemir, T. B., Sitren, H. S., & Cousins, R. J. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.02.046 · Cited by 79 · see citing works
Dvergsten, C. L., Fosmire, G. J., Ollerich, D. A., & Sandstead, H. H. (1984) · Developmental Brain Research · doi:10.1016/0165-3806(84)90057-9 · Cited by 62 · see citing works
The Drosophila transmembrane protein Fear-of-intimacy controls glial cell migration
Pielage, J., Kippert, A., Zhu, M., & Klämbt, C. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.07.039 · Cited by 41 · see citing works
Smedley, M. J., & Stanisstreet, M. (1986) · Development · doi:10.1242/dev.93.1.167 · Cited by 37 · see citing works
A molecular technique for detecting the liberation of intracellular zinc in cultured neurons
Hara, H., & Aizenman, E. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2004.02.018 · Cited by 19 · see citing works
1,10-Phenanthroline and Xenopus laevis Teratology
Jörnvall, H., Falchuk, K. H., Geraci, G., & Vallée, B. L. (1994) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1994.1606 · Cited by 11 · see citing works
Zahm (1996) · doi:10.1002/(sici)1096-9861(19960108)364:2
Flagged first, then by citations
Cited by
Sorted by citations
Kambe, T., Tsuji, T., Hashimoto, A., & Itsumura, N. (2015) · Physiological Reviews · doi:10.1152/physrev.00035.2014 · Cited by 1,158 · see citing works
The contribution of environmental exposure to the etiology of autism spectrum disorder
Bölte, S., Girdler, S., & Marschik, P. B. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2988-4 · Cited by 509 · see citing works
Brain Cell Type Specific Gene Expression and Co-expression Network Architectures
McKenzie, A. T., Wang, M., Hauberg, M. E., Fullard, J. F., Kozlenkov, A., Keenan, A., Hurd, Y. L., Dracheva, S., Casaccia, P., Roussos, P., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-27293-5 · Cited by 481 · see citing works
Chen, B., Yu, P., Chan, W. N., Xie, F., Zhang, Y., Liang, L., Leung, K. T., Lo, K. W., Yu, J., Tse, G. M. K., et al. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01679-y · Cited by 420 · see citing works
The emerging role of zinc transporters in cellular homeostasis and cancer
Bafaro, E. M., Liu, Y., Xu, Y., & Dempski, R. E. (2017) · Signal Transduction and Targeted Therapy · doi:10.1038/sigtrans.2017.29 · Cited by 309 · see citing works
Zinc transporters and their functional integration in mammalian cells
Kambe, T., Taylor, K. M., & Fu, D. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100320 · Cited by 229 · see citing works
Stroke subtype-dependent synapse elimination by reactive gliosis in mice
Shi, X., Luo, L., Wang, J., Shen, H., Li, Y., Mamtilahun, M., Liu, C., Shi, R., Lee, J.-H., Tian, H., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-27248-x · Cited by 218 · see citing works
Cadmium: Toxic effects on placental and embryonic development
Geng, H., & Wang, L. (2019) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2019.02.006 · Cited by 178 · see citing works
The enormity of the zinc deficiency problem and available solutions; an overview
Khan, S. T., Malik, A., Al‐Warthan, A., & Shaik, M. R. (2021) · Arabian Journal of Chemistry · doi:10.1016/j.arabjc.2021.103668 · Cited by 169 · see citing works
The Function and Regulation of Zinc in the Brain
Krall, R. F., Tzounopoulos, T., & Aizenman, E. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.01.010 · Cited by 159 · see citing works
The zinc transporter ZIP12 regulates the pulmonary vascular response to chronic hypoxia
Zhao, L., Oliver, E., Maratou, K., Atanur, S. S., Dubois, O. D., Cotroneo, E., Chen, C.-N., Wang, L., Arce, C., CHABOSSEAU, P. L., et al. (2015) · Nature · doi:10.1038/nature14620 · Cited by 147 · see citing works
Hojyo, S., Miyai, T., Fujishiro, H., Kawamura, M., Yasuda, T., Hijikata, A., Bin, B., Irié, T., Tanaka, J., Atsumi, T., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1323557111 · Cited by 140 · see citing works
Baltacı, A. K., & Yüce, K. (2017) · Neurochemical Research · doi:10.1007/s11064-017-2454-y · Cited by 117 · see citing works
Wang, C., Martins-Bach, A. B., Alfaro‐Almagro, F., Douaud, G., Klein, J. C., Llera, A., Fiscone, C., Bowtell, R. W., Elliott, L. T., Smith, S. M., et al. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01074-w · Cited by 107 · see citing works
Recent Advances in the Role of SLC39A/ZIP Zinc Transporters In Vivo
Takagishi, T., Hara, T., & Fukada, T. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18122708 · Cited by 95 · see citing works
Structural insights of ZIP4 extracellular domain critical for optimal zinc transport
Zhang, T., Sui, D., & Hu, J. P. (2016) · Nature Communications · doi:10.1038/ncomms11979 · Cited by 94 · see citing works
Klingeborn, M., Dismuke, W. M., Skiba, N. P., Kelly, U., Stamer, W. D., & Rickman, C. B. (2017) · Scientific Reports · doi:10.1038/s41598-017-05102-9 · Cited by 93 · see citing works
Numakawa, T., Richards, M., Nakajima, S., Adachi, N., Furuta, M., Odaka, H., & Kunugi, H. (2014) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2014.00136 · Cited by 86 · see citing works
Liu, M., Pi, H., Xi, Y., Wang, L., Tian, L., Chen, M., Xie, J., Deng, P., Zhang, T., Zhou, C., et al. (2020) · Autophagy · doi:10.1080/15548627.2020.1739444 · Cited by 86 · see citing works
Neurobiology of zinc and its role in neurogenesis
Kumar, V., Ashok Kumar, K., Singh, K., Avasthi, K. K., & Kim, J.-J. (2021) · European Journal of Nutrition · doi:10.1007/s00394-020-02454-3 · Cited by 86 · see citing works
Hu, J. P. (2020) · FEBS Journal · doi:10.1111/febs.15658 · Cited by 81 · see citing works
Growth Modulatory Role of Zinc in Prostate Cancer and Application to Cancer Therapeutics
To, P. K., Do, M. H., Cho, J., & Jung, C. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21082991 · Cited by 75 · see citing works
Scarr, E., Udawela, M., Greenough, M. A., Neo, J. H., Seo, M. S., Money, T., Upadhyay, A., Bush, A. I., Everall, I., Thomas, E. A., et al. (2016) · Schizophrenia · doi:10.1038/npjschz.2016.2 · Cited by 61 · see citing works
Endurance Exercise Ability in the Horse: A Trait with Complex Polygenic Determinism
Ricard, A., Robert, C., Blouin, C., Baste, F., Torquet, G., Morgenthaler, C., Rivière, J., Mach, N., Mata, X., Schibler, L., et al. (2017) · Frontiers in Genetics · doi:10.3389/fgene.2017.00089 · Cited by 60 · see citing works
Thingholm, T. E., Rönnstrand, L., & Rosenberg, P. A. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03473-3 · Cited by 63 · see citing works
Copy number variation in Han Chinese individuals with autism spectrum disorder
Gazzellone, M. J., Zhou, X., Lionel, A. C., Uddin, M. J., Thiruvahindrapuram, B., Liang, S., Sun, C., Wang, J., Zou, M., Tammimies, K., et al. (2014) · Journal of Neurodevelopmental Disorders · doi:10.1186/1866-1955-6-34 · Cited by 58 · see citing works
Zinc and its binding proteins: essential roles and therapeutic potential
Kiouri, D. P., Chasapis, C. T., Mavromoustakos, T., Spiliopoulou, C., & Stefanidou, M. E. (2024) · Archives of Toxicology · doi:10.1007/s00204-024-03891-3 · Cited by 56 · see citing works
The trafficking of metal ion transporters of the Zrt‐ and Irt‐like protein family
Bowers, K., & Srai, S. K. (2018) · Traffic · doi:10.1111/tra.12602 · Cited by 56 · see citing works
Kaneko, M., Noguchi, T., Ikegami, S., Sakurai, T., Kakita, A., Toyoshima, Y., Kambe, T., Yamada, M., Inden, M., Hara, H., et al. (2014) · Journal of Neuroscience Research · doi:10.1002/jnr.23491 · Cited by 52 · see citing works
Moon, M., Kim, H. J., Choi, B. Y., Sohn, M., Chung, T. N., & Suh, S. W. (2018) · Stem Cells International · doi:10.1155/2018/5736535 · Cited by 52 · see citing works
Perrin, L., Roudeau, S., Carmona, A., Domart, F., Petersen, J. D., Bohic, S., Yang, Y., Cloetens, P., & Ortega, R. (2017) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.6b00452 · Cited by 51 · see citing works
Zinc supplementation as an adjunct therapy for COVID‐19: Challenges and opportunities
Chinni, V., El-Khoury, H. J., Perera, M., Bellomo, R., Jones, D. A., Bolton, D. M., Ischia, J. J., & Patel, O. (2021) · British Journal of Clinical Pharmacology · doi:10.1111/bcp.14826 · Cited by 47 · see citing works
Impact of Zinc Transport Mechanisms on Embryonic and Brain Development
Willekens, J., & Runnels, L. W. (2022) · Nutrients · doi:10.3390/nu14122526 · Cited by 45 · see citing works
Influx mechanisms in the embryonic and adult rat choroid plexus: a transcriptome study
Saunders, N. R., Dzięgielewska, K. M., Møllgård, K., Habgood, M. D., Wakefield, M. J., Lindsay, H. A., Stratzielle, N., Ghersi‐Egea, J., & Liddelow, S. A. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00123 · Cited by 46 · see citing works
Borodinsky, L. N. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00090 · Cited by 44 · see citing works
Nuttall, J. R. (2015) · Nutritional Neuroscience · doi:10.1080/1028415x.2015.1103437 · Cited by 52 · see citing works
Molecular Basis of Zinc-Dependent Endocytosis of Human ZIP4 Transceptor
Zhang, C., Sui, D., Zhang, T., & Hu, J. P. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107582 · Cited by 42 · see citing works
Structural insights into the elevator-type transport mechanism of a bacterial ZIP metal transporter
Zhang, Y., Jiang, Y., Gao, K., Sui, D., Yu, P., Su, M., Wei, G., & Hu, J. P. (2023) · Nature Communications · doi:10.1038/s41467-023-36048-4 · Cited by 34 · see citing works
Long-term exposure to cadmium disrupts neurodevelopment in mature cerebral organoids
Huang, Y., Guo, X., Lu, S., Chen, Q., Wang, Z., Lai, L., Liu, Q., Zhu, X., Luo, L., Li, J., et al. (2023) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2023.168923 · Cited by 38 · see citing works
Thermogenic adipocyte-derived zinc promotes sympathetic innervation in male mice
Jiang, J., Zhou, D., Zhang, A., Yu, W., Du, L., Yuan, H., Zhang, C., Wang, Z., Jia, X., Zhang, Z., et al. (2023) · Nature Metabolism · doi:10.1038/s42255-023-00751-9 · Cited by 36 · see citing works
Domart, F., Cloetens, P., Roudeau, S., Carmona, A., Verdier, E., Choquet, D., & Ortega, R. (2020) · eLife · doi:10.7554/elife.62334 · Cited by 36 · see citing works
Zhu, X.-Y., Yu, C.-X., Wu, W.-L., Shi, L., Jiang, C.-Y., Wang, L., Ding, Z.-D., & Liu, Y. (2021) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-022-00893-7 · Cited by 31 · see citing works
Directed Neural Stem Cells Differentiation via Signal Communication with Ni–Zn Micromotors
Feng, Y., Gao, C., Xie, D., Liu, L., Chen, B., Liu, S., Yang, H., Gao, Z., Wilson, D. A., Tu, Y., et al. (2023) · Advanced Materials · doi:10.1002/adma.202301736 · Cited by 34 · see citing works
Han, S., Zhang, D., Kao, Y., Zhou, X., Guo, X., Zhang, W., Liu, M., Chen, H., Kong, X., Wei, Z., et al. (2024) · ACS Nano · doi:10.1021/acsnano.4c08863 · Cited by 32 · see citing works
Overview and Introduction to Autism Spectrum Disorder (ASD)
Al-Dewik, N. I. E., Al‐Jurf, R., Styles, M., Tahtamouni, S., Al‐Sharshani, D., Alsharshani, M., Ahmad, A. I., Khattab, A., Rifai, H. A., & Qoronfleh, M. W. (2020) · Advances in neurobiology · doi:10.1007/978-3-030-30402-7_1 · Cited by 33 · see citing works
Benedictis, C. A. D., Haffke, C., Hagmeyer, S., Sauer, A. K., & Grabrucker, A. M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094511 · Cited by 32 · see citing works
Nuttall, J. R., Supasai, S., Kha, J., Vaeth, B. M., Mackenzie, G. G., Adamo, A. M., & Oteiza, P. I. (2015) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2015.05.007 · Cited by 33 · see citing works
Differential expression of zinc transporters accompanies the differentiation of C2C12 myoblasts
Paskavitz, A. L., Quintana, J., Cangussu, D., Tavera‐Montañez, C., Xiao, Y., Ortiz‐Miranda, S., Navea, J. G., & Padilla‐Benavides, T. (2018) · Journal of Trace Elements in Medicine and Biology · doi:10.1016/j.jtemb.2018.04.024 · Cited by 31 · see citing works
Olea‐Flores, M., Kan, J., Carlson, A., Syed, S. A., McCann, C., Mondal, V., Szady, C., Ricker, H. M., McQueen, A., Navea, J. G., et al. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.895433 · Cited by 31 · see citing works
Kuliyev, E., Zhang, C., Sui, D., & Hu, J. P. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100269 · Cited by 29 · see citing works
Ye, C., Lian, G., Wang, T., Chen, A., Chen, W., Gong, J., Luo, L., Wang, H., & Xie, L. (2022) · BMC Pulmonary Medicine · doi:10.1186/s12890-022-01905-3 · Cited by 29 · see citing works
Zinc fate in animal husbandry systems
Roméo, A., Vacchina, V., Legros, S., & Dœlsch, E. (2014) · Metallomics · doi:10.1039/c4mt00062e · Cited by 29 · see citing works
Brügger, D., Hanauer, M., Ortner, J., & Windisch, W. M. (2020) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2020.108576 · Cited by 24 · see citing works
Xiao, G., Lian, G., Wang, T., Chen, W., Zhuang, W., Luo, L., Wang, H., & Xie, L. (2021) · Cell Communication and Signaling · doi:10.1186/s12964-021-00779-y · Cited by 25 · see citing works
Resveratrol–zinc combination for prostate cancer management
Singh, C. K., Pitschmann, A., & Ahmad, N. (2014) · Cell Cycle · doi:10.4161/cc.29334 · Cited by 25 · see citing works
Mulvey, B., & Dougherty, J. D. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01493-6 · Cited by 22 · see citing works
Bogdanovic, M., Asraf, H., Gottesman, N., Sekler, I., Aizenman, E., & Hershfinkel, M. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0908-21.2022 · Cited by 23 · see citing works
Şahiner, N., Güven, O., Demirci, Ş., Suner, S. S., Sahiner, M., Ari, B., & Can, M. (2025) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2025.114669 · Cited by 22 · see citing works
Chowanadisai, W. (2014) · PLoS ONE · doi:10.1371/journal.pone.0111535 · Cited by 22 · see citing works
Self-citationZinc Dyshomeostasis in Cardiomyocytes after Acute Hypoxia/Reoxygenation
Bodiga, V. L., Thokala, S., Kovur, S. M., & Bodiga, S. (2017) · Biological Trace Element Research · doi:10.1007/s12011-017-0957-7 · Cited by 22 · see citing works
Bovine herpesvirus-1 infection in mouse neuroblastoma (Neuro-2A) cells
Fiorito, F., Nocera, F. P., Cantiello, A., Iovane, V., Lambiase, S., Piccolo, M., Ferraro, M. G., Santamaria, R., & Martino, L. D. (2020) · Veterinary Microbiology · doi:10.1016/j.vetmic.2020.108762 · Cited by 20 · see citing works
A role for zinc transporter gene SLC39A12 in the nervous system and beyond
Davis, D. N., Strong, M. D., Chambers, E., Hart, M. D., Bettaieb, A., Clarke, S. L., Smith, B. J., Stoecker, B. J., Lucas, E. A., Lin, D., et al. (2021) · Gene · doi:10.1016/j.gene.2021.145824 · Cited by 20 · see citing works
Self-citationAntiviral Property of the Fungal Metabolite 3-O-Methylfunicone in Bovine Herpesvirus 1 Infection
Fiorito, F., Cerracchio, C., Salvatore, M. M., Serra, F., Pucciarelli, A., Amoroso, M. G., Nicoletti, R., & Andolfi, A. (2022) · Microorganisms · doi:10.3390/microorganisms10010188 · Cited by 20 · see citing works
Disruption of the zinc metabolism in rat fœtal brain after prenatal exposure to cadmium
Mimouna, S. B., Boughammoura, S., Chemek, M., Haouas, Z., Bannı, M., & Messaoudi, I. (2018) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2018.03.005 · Cited by 20 · see citing works
Relevance of biometals during neuronal differentiation and myelination: in vitro and in vivo studies
Chin-Chan, M., Montes, S., Blanco-Álvarez, V. M., Aguirre‐Alarcón, H., Rodríguez, I. H., & Bautista, E. (2022) · BioMetals · doi:10.1007/s10534-022-00380-x · Cited by 19 · see citing works
Ischia, J. J., Bolton, D. M., & Patel, O. (2019) · Metallomics · doi:10.1039/c9mt00079h · Cited by 19 · see citing works
Unlocking the brain’s zinc code: implications for cognitive function and disease
Sabouri, S., Rostamirad, M., & Dempski, R. E. (2024) · Frontiers in Biophysics · doi:10.3389/frbis.2024.1406868 · Cited by 18 · see citing works
Zhu, T., Wang, X., Zheng, Z., Quan, J., Liu, Y., Wang, Y., Liu, T., Liu, X., Wang, M., & Zhang, Z. (2021) · Journal of Cardiovascular Pharmacology · doi:10.1097/fjc.0000000000001156 · Cited by 18 · see citing works
Kanemoto-Kataoka, Y., Oyama, T. M., Ishibashi, H., & Oyama, Y. (2015) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2015.05.014 · Cited by 18 · see citing works
Karweina, D., Kreuzer-Redmer, S., Müller, U., Franken, T., Pieper, R., Baron, U., Olek, S., Zentek, J., & Brockmann, G. A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0143098 · Cited by 18 · see citing works
O'Kane, D. B., Gibson, L., May, C. N., du Plessis, J., Shulkes, A., Baldwin, G. S., Bolton, D. M., Ischia, J. J., & Patel, O. (2018) · BioMetals · doi:10.1007/s10534-018-0125-3 · Cited by 18 · see citing works
Hu, J. P., & Jiang, Y. (2024) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2024.2405476 · Cited by 17 · see citing works
Hong, L.-J., Jiang, Q., Long, S., Wang, H., Zhang, L.-D., Tian, Y., Wang, C., Cao, J.-J., Tao, R., Huang, J.-Y., et al. (2015) · Molecular Neurobiology · doi:10.1007/s12035-014-9085-y · Cited by 17 · see citing works
Canine Coronavirus Activates Aryl Hydrocarbon Receptor during In Vitro Infection
Cerracchio, C., Serra, F., Amoroso, M. G., & Fiorito, F. (2022) · Viruses · doi:10.3390/v14112437 · Cited by 16 · see citing works
Turan, B., & Tuncay, E. (2020) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-020-03964-8 · Cited by 16 · see citing works
Brain Magnetic Resonance Imaging Phenome-Wide Association Study With Metal Transporter Gene SLC39A8
Hermann, E. R., Chambers, E., Davis, D. N., Montgomery, M. R., Lin, D., & Chowanadisai, W. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.647946 · Cited by 16 · see citing works
Self-citationZinc Uptake and Storage During the Formation of the Cerebral Cortex in Mice
Hasna, J., Bohic, S., Lemoine, S., Blugeon, C., & Bouron, A. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-1581-7 · Cited by 16 · see citing works
A zinc transporter gene required for development of the nervous system
Chowanadisai, W., Graham, D. M., Keen, C. L., Rucker, R. B., & Messerli, M. A. (2013) · Communicative & Integrative Biology · doi:10.4161/cib.26207 · Cited by 15 · see citing works
Self-citationStrong, M. D., Hart, M. D., Tang, T. Z., Ojo, B. A., Wu, L., Nacke, M. R., Agidew, W. T., Hwang, H. J., Hoyt, P. R., Bettaieb, A., et al. (2020) · The FASEB Journal · doi:10.1096/fj.202000772r · Cited by 14 · see citing works
Self-citationZinc Transporter Proteins: A Review and a New View from Biochemistry
Kambe, T., Suzuki, E., & Komori, T. (2019) · Springer eBooks · doi:10.1007/978-981-15-0557-7_3 · Cited by 15 · see citing works
Fungal metabolite 6-pentyl-α-pyrone reduces canine coronavirus infection
Cerracchio, C., Sorbo, L. D., Serra, F., Staropoli, A., Amoroso, M. G., Vinale, F., & Fiorito, F. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e28351 · Cited by 13 · see citing works
Excessive apoptosis and ROS induced by ethionine affect neural cell viability and differentiation
Zhang, L., Li, D., Zhang, J., Yan, P., Liu, X., Wang, L., Khan, A., Liu, Z., Mu, J., Xu, J., et al. (2020) · Acta Biochimica et Biophysica Sinica · doi:10.1093/abbs/gmaa093 · Cited by 13 · see citing works
Zhou, Y., Huang, G., Liu, M., Zhang, M., Wu, B., & Gu, J. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1750534 · Cited by 13 · see citing works
Centenarian hippocampus displays high levels of astrocytic metallothioneins
Saenz‐Antoñanzas, A., Muñoz‐Culla, M., Rigo, P., Ruiz‐Barreiro, L., Moreno‐Valladares, M., Alberro, A., Cruces‐Salguero, S., Arroyo‐Izaga, M., Arranz, A. M., Otaegui, D., et al. (2024) · Aging Cell · doi:10.1111/acel.14201 · Cited by 11 · see citing works
Bilirubin-Induced Transcriptomic Imprinting in Neonatal Hyperbilirubinemia
Llido, J. P., Fioriti, E., Pascut, D., Giuffrè, M., Bottin, C., Zanconati, F., Tiribelli, C., & Gazzin, S. (2023) · Biology · doi:10.3390/biology12060834 · Cited by 12 · see citing works
Zhang, Y., Maimaiti, R., Lou, S., Abula, R., Abulaiti, A., & Kelimu, A. (2022) · Journal of Affective Disorders · doi:10.1016/j.jad.2022.08.130 · Cited by 11 · see citing works
Xie, K., & Sheppard, A. M. (2018) · BioEssays · doi:10.1002/bies.201800051 · Cited by 10 · see citing works
Nishikawa, M., Mori, H., & Hara, M. (2017) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2017.05.008 · Cited by 10 · see citing works
Zinc Ions Modulate YY1 Activity: Relevance in Carcinogenesis
Figiel, M., Górka, A. K., & Górecki, A. (2023) · Cancers · doi:10.3390/cancers15174338 · Cited by 9 · see citing works
Biochemical Markers of Zinc Nutrition
Wang, X., Zhang, M. H., Ma, J., Tie, Y., & Wang, S. (2024) · Biological Trace Element Research · doi:10.1007/s12011-024-04091-x · Cited by 9 · see citing works
Dean, B., Hopper, S., & Scarr, E. (2024) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2024.07.017 · Cited by 9 · see citing works
The Cardiac Ryanodine Receptor Provides a Suitable Pathway for the Rapid Transport of Zinc (Zn2+)
Gaburjáková, J., & Gaburjáková, M. (2022) · Cells · doi:10.3390/cells11050868 · Cited by 9 · see citing works
Zinc Transport Proteins and Zinc Signaling
Kambe, T., Tsuji, T., & Fukue, K. (2014) · Springer eBooks · doi:10.1007/978-4-431-55114-0_3 · Cited by 9 · see citing works
Influence of Intracellular Zinc on Cultures of Rat Cardiac Neural Crest Cells
Yang, H., Keen, C. L., & Lanoue, L. (2015) · Birth Defects Research Part B Developmental and Reproductive Toxicology · doi:10.1002/bdrb.21135 · Cited by 8 · see citing works
Self-citationAlluri, K., Nair, K. P. M., & Ghosh, S. (2019) · Nucleosides Nucleotides & Nucleic Acids · doi:10.1080/15257770.2019.1670838 · Cited by 8 · see citing works
Cardona, C. J., Kim, Y., Chowanadisai, W., & Montgomery, M. R. (2024) · Cells · doi:10.3390/cells13181541 · Cited by 7 · see citing works
Self-citationPhysiological Significance of Zinc for Plants, Animals, and Humans
Kaur, H., Devi, K. S., & Yadav, R. (2025) · Springer eBooks · doi:10.1007/978-981-96-4253-3_2 · Cited by 7 · see citing works
In Vitro Evaluation of Aryl Hydrocarbon Receptor Involvement in Feline Coronavirus Infection
Sorbo, L. D., Giugliano, R., Cerracchio, C., Iovane, V., Salvatore, M. M., Serra, F., Amoroso, M. G., Pellegrini, F., Levante, M., Capozza, P., et al. (2025) · Viruses · doi:10.3390/v17020227 · Cited by 7 · see citing works
Manning, A., Mendelson, B. Z., Bender, P. T. R., Bainer, K., Ruby, R., Shifflett, V., Dariano, D. F., Webb, B. A., Geldenhuys, W. J., & Anderson, C. T. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.2067-24.2025 · Cited by 5 · see citing works
Shen, Z., Fan, C., Ding, C., Xu, M., Wu, X. G., Wang, Y., & Tian, X. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e26271 · Cited by 5 · see citing works
- Authors
- Chowanadisai, W., Graham, D. M., Keen, C. L., Rucker, R. B., & Messerli, M. A.
- Affiliations
- Marine Biological Laboratory (US)
- University of California, Davis (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-05-28
- Volume
- 110
- Issue
- 24
- Pages
- 9903-9908
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3683776
- OpenAlex
- W2032713755
- Cited by
- 140
- References
- 37
- Citations by year
- 2026: 5 · 2025: 11 · 2024: 15 · 2023: 11 · 2022: 11 · 2021: 21 · 2020: 17 · 2019: 7 · 2018: 10 · 2017: 9 · 2016: 4 · 2015: 10 · 2014: 8 · 2013: 1
- FWCI
- 7.09
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (P40OD010997)
- National Institute of General Medical Sciences (P30GM092374)
- National Center for Research Resources (P41RR001395, P41 RR001395S1)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Heavy Metal Exposure and Toxicity
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- zinc transporters, zinc uptake, neurite outgrowth, neurulation, neural tube closure, neuronal differentiation, CREB phosphorylation, microtubule assembly, brain development, Xenopus tropicalis, N2a cells
- MeSH terms
- Animals, Brain, Cricetulus, Embryo, Nonmammalian, Cricetinae, Humans, Tubulin, Xenopus, Zinc, Immunoblotting, CHO Cells, Neurites, Cyclic AMP Response Element-Binding Protein, In Situ Hybridization, Reverse Transcriptase Polymerase Chain Reaction, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Cation Transport Proteins, Xenopus Proteins, Cell Line, Tumor, Mice, Neurulation, Gene Knockdown Techniques, Polymerization
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