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Neural Plasticity
Volume 2016 (2016), Article ID 3760702, 15 pages
http://dx.doi.org/10.1155/2016/3760702
Research Article

Cellular Zinc Homeostasis Contributes to Neuronal Differentiation in Human Induced Pluripotent Stem Cells

1Institute for Anatomy and Cell Biology, Ulm University, 89081 Ulm, Germany
2Department of Anaesthesiology, University of Ulm, 89081 Ulm, Germany
3Institute of Neuroanatomy, Eberhard Karls University of Tübingen, 72074 Tübingen, Germany
4WG Molecular Analysis of Synaptopathies, Neurology Department, Neurocenter of Ulm University, 89081 Ulm, Germany

Received 23 February 2016; Accepted 24 March 2016

Academic Editor: Bruno Poucet

Copyright © 2016 Stefanie Pfaender et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. R. Morris and C. W. Levenson, “Zinc regulation of transcriptional activity during retinoic acid-induced neuronal differentiation,” Journal of Nutritional Biochemistry, vol. 24, no. 11, pp. 1940–1944, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. W. Chowanadisai, D. M. Graham, C. L. Keen, R. B. Rucker, and M. A. Messerli, “A zinc transporter gene required for development of the nervous system,” Communicative and Integrative Biology, vol. 6, no. 6, Article ID e26207, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. C. W. Levenson and D. Morris, “Zinc and neurogenesis: making new neurons from development to adulthood,” Advances in Nutrition, vol. 2, no. 2, pp. 96–100, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. P. A. Marks, “Histone deacetylase inhibitors: a chemical genetics approach to understanding cellular functions,” Biochimica et Biophysica Acta (BBA)—Gene Regulatory Mechanisms, vol. 1799, no. 10–12, pp. 717–725, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. H. Tapiero and K. D. Tew, “Trace elements in human physiology and pathology: zinc and metallothioneins,” Biomedicine and Pharmacotherapy, vol. 57, no. 9, pp. 399–411, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. L. P. Freedman and B. F. Luisi, “On the mechanism of DNA binding by nuclear hormone receptors: a structural and functional perspective,” Journal of Cellular Biochemistry, vol. 51, no. 2, pp. 140–150, 1993. View at Publisher · View at Google Scholar · View at Scopus
  7. T. V. O'Halloran, “Transition metals in control of gene expression,” Science, vol. 261, no. 5122, pp. 715–725, 1993. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Klug and J. W. Schwabe, “Protein motifs 5. Zinc fingers,” The FASEB Journal, vol. 9, no. 8, pp. 597–604, 1995. View at Google Scholar · View at Scopus
  9. A. M. Grabrucker, “Environmental factors in autism,” Frontiers in Psychiatry, vol. 3, article 118, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Grabrucker, L. Jannetti, M. Eckert et al., “Zinc deficiency dysregulates the synaptic ProSAP/Shank scaffold and might contribute to autism spectrum disorders,” Brain, vol. 137, no. 1, pp. 137–152, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Grabrucker, T. M. Boeckers, and A. M. Grabrucker, “Gender dependent evaluation of autism like behavior in mice exposed to prenatal zinc deficiency,” Frontiers in Behavioral Neuroscience, vol. 10, article 37, 2016. View at Publisher · View at Google Scholar
  12. D. E. K. Sutherland and M. J. Stillman, “The ‘magic numbers’ of metallothionein,” Metallomics, vol. 3, no. 5, pp. 444–463, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. B. Floriańczyk, “Role of Zinc in nervous system cells,” Journal of Pre-Clinical and Clinical Research, vol. 5, no. 1, pp. 12–15, 2011. View at Google Scholar
  14. S. D. Gower-Winter, R. S. Corniola, T. J. Morgan Jr., and C. W. Levenson, “Zinc deficiency regulates hippocampal gene expression and impairs neuronal differentiation,” Nutritional Neuroscience, vol. 16, no. 4, pp. 174–182, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. L. Linta, M. Stockmann, K. N. Kleinhans et al., “Rat embryonic fibroblasts improve reprogramming of human keratinocytes into induced pluripotent stem cells,” Stem Cells and Development, vol. 21, no. 6, pp. 965–976, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. A. M. Vitale, E. Wolvetang, and A. MacKay-Sim, “Induced pluripotent stem cells: a new technology to study human diseases,” International Journal of Biochemistry and Cell Biology, vol. 43, no. 6, pp. 843–846, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Takahashi and S. Yamanaka, “Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors,” Cell, vol. 126, no. 4, pp. 663–676, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Okano and S. Yamanaka, “iPS cell technologies: significance and applications to CNS regeneration and disease,” Molecular Brain, vol. 7, no. 1, article 22, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. B.-Y. Hu and S.-C. Zhang, “Differentiation of spinal motor neurons from pluripotent human stem cells,” Nature Protocols, vol. 4, no. 9, pp. 1295–1304, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Hagmeyer, K. Mangus, T. M. Boeckers, and A. M. Grabrucker, “Effects of trace metal profiles characteristic for autism on synapses in cultured neurons,” Neural Plasticity, vol. 2015, Article ID 985083, 16 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. E. L. Que, D. W. Domaille, and C. J. Chang, “Metals in neurobiology: probing their chemistry and biology with molecular imaging,” Chemical Reviews, vol. 108, no. 5, pp. 1517–1549, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. L. A. Lichten and R. J. Cousins, “Mammalian zinc transporters: nutritional and physiologic regulation,” Annual Review of Nutrition, vol. 29, pp. 153–176, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. R. J. Cousins, J. P. Liuzzi, and L. A. Lichten, “Mammalian zinc transport, trafficking, and signals,” The Journal of Biological Chemistry, vol. 281, no. 34, pp. 24085–24089, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. J. P. Bressler, L. Olivi, J. H. Cheong, Y. Kim, A. Maerten, and D. Bannon, “Metal transporters in intestine and brain: their involvement in metal-associated neurotoxicities,” Human & Experimental Toxicology, vol. 26, pp. 221–229, 2007. View at Google Scholar
  25. R. Su, X. Mei, Y. Wang, and L. Zhang, “Regulation of zinc transporter 1 expression in dorsal horn of spinal cord after acute spinal cord injury of rats by dietary zinc,” Biological Trace Element Research, vol. 149, no. 2, pp. 219–226, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Lindau and E. Neher, “Patch-clamp techniques for time-resolved capacitance measurements in single cells,” Pflügers Archiv, vol. 411, no. 2, pp. 137–146, 1988. View at Publisher · View at Google Scholar
  27. M. Stockmann, L. Linta, K. J. Föhr et al., “Developmental and functional nature of human iPSC derived motoneurons,” Stem Cell Reviews and Reports, vol. 9, no. 4, pp. 475–492, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. A. M. Grabrucker, “A role for synaptic zinc in ProSAP/Shank PSD scaffold malformation in autism spectrum disorders,” Developmental Neurobiology, vol. 74, no. 2, pp. 136–146, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. A. M. Tokheim, I. M. Armitage, and B. L. Martin, “Antiserum specific for the intact isoform-3 of metallothionein,” Journal of Biochemical and Biophysical Methods, vol. 63, no. 1, pp. 43–52, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. M. K. Baron, T. M. Boeckers, B. Vaida et al., “An architectural framework that may lie at the core of the postsynaptic density,” Science, vol. 311, no. 5760, pp. 531–535, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. A. M. Grabrucker, M. J. Knight, C. Proepper et al., “Concerted action of zinc and ProSAP/Shank in synaptogenesis and synapse maturation,” The EMBO Journal, vol. 30, no. 3, pp. 569–581, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Raab, T. M. Boeckers, and W. L. Neuhuber, “Proline-rich synapse-associated protein-1 and 2 (ProSAP1/Shank2 and ProSAP2/Shank3)-scaffolding proteins are also present in postsynaptic specializations of the peripheral nervous system,” Neuroscience, vol. 171, no. 2, pp. 421–433, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Grabrucker, C. Proepper, K. Mangus et al., “The PSD protein ProSAP2/Shank3 displays synapto-nuclear shuttling which is deregulated in a schizophrenia-associated mutation,” Experimental Neurology, vol. 253, pp. 126–137, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. H. H. Sandstead, G. J. Fosmire, E. S. Halas, D. Strobel, and J. Duerre, “Zinc: brain and behavioral development,” in Trace Element Metabolsim in Man and Animals, M. Kirchgessner, Ed., pp. 203–206, University Munich, Freising, Germany, 3rd edition, 1977. View at Google Scholar
  35. G. Vela, P. Stark, M. Socha, A. K. Sauer, S. Hagmeyer, and A. M. Grabrucker, “Zinc in gut-brain interaction in autism and neurological disorders,” Neural Plasticity, vol. 2015, Article ID 972791, 15 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Hagmeyer, J. C. Haderspeck, and A. M. Grabrucker, “Behavioral impairments in animal models for zinc deficiency,” Frontiers in Behavioral Neuroscience, vol. 8, article 443, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. L. Caulfield and R. E. Black, “Zinc deficiency,” in Comparative Quantification of Health Risks: Global and Regional Burden of Disease Attributable to Selected Major Risk Factors, M. Ezzati, A. D. Lopez, A. Rodgers, and C. J. L. Murray, Eds., pp. 257–279, World Health Organization, Geneva, Switzerland, 2004. View at Google Scholar
  38. C. W. Habela, H. Song, and G. L. Ming, “Modeling synaptogenesis in schizophrenia and autism using human iPSC derived neurons,” Molecular and Cellular Neuroscience, 2015. View at Publisher · View at Google Scholar
  39. L. Volk, S.-L. Chiu, K. Sharma, and R. L. Huganir, “Glutamate synapses in human cognitive disorders,” Annual Review of Neuroscience, vol. 38, pp. 127–149, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. M. S. Clegg, L. A. Hanna, B. J. Niles, T. Y. Momma, and C. L. Keen, “Zinc deficiency-induced cell death,” IUBMB Life, vol. 57, no. 10, pp. 661–669, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. R. S. Corniola, N. M. Tassabehji, J. Hare, G. Sharma, and C. W. Levenson, “Zinc deficiency impairs neuronal precursor cell proliferation and induces apoptosis via p53-mediated mechanisms,” Brain Research, vol. 1237, pp. 52–61, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. W. Chowanadisai, S. L. Kelleher, and B. Lönnerdal, “Zinc deficiency is associated with increased brain zinc import and LIV-1 expression and decreased ZnT-1 expression in neonatal rats,” Journal of Nutrition, vol. 135, no. 5, pp. 1002–1007, 2005. View at Google Scholar · View at Scopus
  43. R. J. Cousins, R. K. Blanchard, M. P. Popp et al., “A global view of the selectivity of zinc deprivation and excess on genes expressed in human THP-1 mononuclear cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 12, pp. 6952–6957, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Penkowa, M. Giralt, P. S. Thomsen, J. Carrasco, and J. Hidalgo, “Zinc or copper deficiency-induced impaired inflammatory response to brain trauma may be caused by the concomitant metallothionein changes,” Journal of Neurotrauma, vol. 18, no. 4, pp. 447–463, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. M. L. Baumann and T. L. Kemper, “Neuroanatomic observations of the brain in autism,” in The Neurobiology of Autism, M. L. Baumann and T. L. Kemper, Eds., pp. 119–145, John Hopkins University Press, Baltimore, Md, USA, 1994. View at Google Scholar
  46. P. M. Lippiello, “Nicotinic cholinergic antagonists: a novel approach for the treatment of autism,” Medical Hypotheses, vol. 66, no. 5, pp. 985–990, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. W. Pang, X. Leng, H. Lu et al., “Depletion of intracellular zinc induces apoptosis of cultured hippocampal neurons through suppression of ERK signaling pathway and activation of caspase-3,” Neuroscience Letters, vol. 552, pp. 140–145, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. A. M. Adamo and P. I. Oteiza, “Zinc deficiency and neurodevelopment: the case of neurons,” BioFactors, vol. 36, no. 2, pp. 117–124, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. S. W. Suh, S. J. Won, A. M. Hamby et al., “Decreased brain zinc availability reduces hippocampal neurogenesis in mice and rats,” Journal of Cerebral Blood Flow and Metabolism, vol. 29, no. 9, pp. 1579–1588, 2009. View at Publisher · View at Google Scholar · View at Scopus