{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T12:40:46Z","timestamp":1790685646573,"version":"4.1.0"},"reference-count":48,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2016,2,16]],"date-time":"2016-02-16T00:00:00Z","timestamp":1455580800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2016,2,16]],"date-time":"2016-02-16T00:00:00Z","timestamp":1455580800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat Commun"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Brain development requires a fine-tuned copper homoeostasis. Copper deficiency or excess results in severe neuro-pathologies. We demonstrate that upon neuronal differentiation, cellular demand for copper increases, especially within the secretory pathway. Copper flow to this compartment is facilitated through transcriptional and metabolic regulation. Quantitative real-time imaging revealed a gradual change in the oxidation state of cytosolic glutathione upon neuronal differentiation. Transition from a broad range of redox states to a uniformly reducing cytosol facilitates reduction of the copper chaperone Atox1, liberating its metal-binding site. Concomitantly, expression of Atox1 and its partner, a copper transporter ATP7A, is upregulated. These events produce a higher flux of copper through the secretory pathway that balances copper in the cytosol and increases supply of the cofactor to copper-dependent enzymes, expression of which is elevated in differentiated neurons. Direct link between glutathione oxidation and copper compartmentalization allows for rapid metabolic adjustments essential for normal neuronal function.<\/jats:p>","DOI":"10.1038\/ncomms10640","type":"journal-article","created":{"date-parts":[[2016,2,16]],"date-time":"2016-02-16T12:51:26Z","timestamp":1455627086000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":113,"title":["Neuronal differentiation is associated with a redox-regulated increase of copper flow to the secretory pathway"],"prefix":"10.1038","volume":"7","author":[{"given":"Yuta","family":"Hatori","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ye","family":"Yan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katharina","family":"Schmidt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eri","family":"Furukawa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nesrin M.","family":"Hasan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nan","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chin-Nung","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shanthini","family":"Sockanathan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Svetlana","family":"Lutsenko","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2016,2,16]]},"reference":[{"key":"BFncomms10640_CR1","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1016\/B978-0-12-394390-3.00006-9","volume":"69","author":"NM Hasan","year":"2012","unstructured":"Hasan, N. M. & Lutsenko, S. Regulation of copper transporters in human cells. Curr. Top. Membr. 69, 137\u2013161 (2012).","journal-title":"Curr. Top. Membr."},{"key":"BFncomms10640_CR2","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1023\/A:1021202119942","volume":"34","author":"LS Field","year":"2002","unstructured":"Field, L. S., Luk, E. & Culotta, V. C. Copper chaperones: personal escorts for metal ions. J. Bioenerg. Biomembr. 34, 373\u2013379 (2002).","journal-title":"J. Bioenerg. Biomembr."},{"key":"BFncomms10640_CR3","doi-asserted-by":"publisher","first-page":"36041","DOI":"10.1074\/jbc.M112.370403","volume":"287","author":"NM Hasan","year":"2012","unstructured":"Hasan, N. M. et al. Molecular events initiating exit of a copper-transporting ATPase ATP7B from the trans-Golgi network. J. Biol. Chem. 287, 36041\u201336050 (2012).","journal-title":"J. Biol. Chem."},{"key":"BFncomms10640_CR4","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1016\/j.abb.2008.05.005","volume":"476","author":"S Lutsenko","year":"2008","unstructured":"Lutsenko, S., Gupta, A., Burkhead, J. L. & Zuzel, V. Cellular multitasking: the dual role of human Cu-ATPases in cofactor delivery and intracellular copper balance. Arch. Biochem. Biophys. 476, 22\u201332 (2008).","journal-title":"Arch. Biochem. Biophys."},{"key":"BFncomms10640_CR5","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1038\/nature09018","volume":"465","author":"L Banci","year":"2010","unstructured":"Banci, L. et al. Affinity gradients drive copper to cellular destinations. Nature 465, 645\u2013648 (2010).","journal-title":"Nature"},{"key":"BFncomms10640_CR6","doi-asserted-by":"publisher","first-page":"411","DOI":"10.1038\/nchembio.364","volume":"6","author":"O Yanes","year":"2010","unstructured":"Yanes, O. et al. Metabolic oxidation regulates embryonic stem cell differentiation. Nat. Chem. Biol. 6, 411\u2013417 (2010).","journal-title":"Nat. Chem. Biol."},{"key":"BFncomms10640_CR7","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1016\/j.jneumeth.2010.06.009","volume":"191","author":"RP Orme","year":"2010","unstructured":"Orme, R. P., Gates, M. A. & Fricker-Gates, R. A. A multiplexed quantitative proteomics approach for investigating protein expression in the developing central nervous system. J. Neurosci. Methods 191, 75\u201382 (2010).","journal-title":"J. Neurosci. Methods"},{"key":"BFncomms10640_CR8","doi-asserted-by":"publisher","first-page":"2535","DOI":"10.1002\/jnr.22404","volume":"88","author":"D Bousquet-Moore","year":"2010","unstructured":"Bousquet-Moore, D., Mains, R. E. & Eipper, B. A. Peptidylgycine \u03b1-amidating monooxygenase and copper: a gene-nutrient interaction critical to nervous system function. J. Neurosci. Res. 88, 2535\u20132545 (2010).","journal-title":"J. Neurosci. Res."},{"key":"BFncomms10640_CR9","doi-asserted-by":"publisher","first-page":"3301","DOI":"10.1038\/ncomms4301","volume":"5","author":"M Malinouski","year":"2014","unstructured":"Malinouski, M. et al. Genome-wide RNAi ionomics screen reveals new genes and regulation of human trace element metabolism. Nat. Commun. 5, 3301 (2014).","journal-title":"Nat. Commun."},{"key":"BFncomms10640_CR10","doi-asserted-by":"publisher","first-page":"26678","DOI":"10.1074\/jbc.M112.381178","volume":"287","author":"Y Hatori","year":"2012","unstructured":"Hatori, Y., Clasen, S., Hasan, N. M., Barry, A. N. & Lutsenko, S. Functional partnership of the copper export machinery and glutathione balance in human cells. J. Biol. Chem. 287, 26678\u201326687 (2012).","journal-title":"J. Biol. Chem."},{"key":"BFncomms10640_CR11","doi-asserted-by":"publisher","first-page":"945","DOI":"10.1089\/ars.2012.5086","volume":"19","author":"Y Hatori","year":"2013","unstructured":"Hatori, Y. & Lutsenko, S. An expanding range of functions for the copper chaperone\/antioxidant protein Atox1. Antioxid. Redox Signal. 19, 945\u2013957 (2013).","journal-title":"Antioxid. Redox Signal."},{"key":"BFncomms10640_CR12","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1038\/35049541","volume":"1","author":"TM Jessell","year":"2000","unstructured":"Jessell, T. M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20\u201329 (2000).","journal-title":"Nat. Rev. Genet."},{"key":"BFncomms10640_CR13","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1016\/S0736-5748(00)00093-9","volume":"19","author":"M Hollyday","year":"2001","unstructured":"Hollyday, M. Neurogenesis in the vertebrate neural tube. Int. J. Dev. Neurosci. 19, 161\u2013173 (2001).","journal-title":"Int. J. Dev. Neurosci."},{"key":"BFncomms10640_CR14","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1016\/0006-8993(89)90073-5","volume":"491","author":"L Graham","year":"1989","unstructured":"Graham, L. & Gallop, P. M. Peptidylglycine alpha-amidating monooxygenase activity in spinal cord, dorsal roots, and dorsal root ganglia of Macaca fascicularis. Brain Res. 491, 371\u2013373 (1989).","journal-title":"Brain Res."},{"key":"BFncomms10640_CR15","doi-asserted-by":"publisher","first-page":"66","DOI":"10.1016\/j.regpep.2005.06.008","volume":"131","author":"C-L Lu","year":"2005","unstructured":"Lu, C.-L. et al. Changes of the neuropeptides content and gene expression in spinal cord and dorsal root ganglion after noxious colorectal distension. Regul. Pept. 131, 66\u201373 (2005).","journal-title":"Regul. Pept."},{"key":"BFncomms10640_CR16","doi-asserted-by":"publisher","first-page":"991","DOI":"10.1046\/j.1471-4159.2000.0750991.x","volume":"75","author":"M Encinas","year":"2000","unstructured":"Encinas, M. et al. Sequential treatment of SH-SY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuron-like cells. J. Neurochem. 75, 991\u20131003 (2000).","journal-title":"J. Neurochem."},{"key":"BFncomms10640_CR17","doi-asserted-by":"publisher","first-page":"176","DOI":"10.1016\/j.mad.2012.01.008","volume":"133","author":"Z Xun","year":"2012","unstructured":"Xun, Z. et al. Retinoic acid-induced differentiation increases the rate of oxygen consumption and enhances the spare respiratory capacity of mitochondria in SH-SY5Y cells. Mech. Ageing Dev. 133, 176\u2013185 (2012).","journal-title":"Mech. Ageing Dev."},{"key":"BFncomms10640_CR18","doi-asserted-by":"publisher","first-page":"33949","DOI":"10.1074\/jbc.M109.070201","volume":"284","author":"C White","year":"2009","unstructured":"White, C., Lee, J., Kambe, T., Fritsche, K. & Petris, M. J. A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J. Biol. Chem. 284, 33949\u201333956 (2009).","journal-title":"J. Biol. Chem."},{"key":"BFncomms10640_CR19","doi-asserted-by":"publisher","first-page":"2762","DOI":"10.1093\/jn\/135.12.2762","volume":"135","author":"J-F Monty","year":"2005","unstructured":"Monty, J.-F., Llanos, R. M., Mercer, J. F. B. & Kramer, D. R. Copper exposure induces trafficking of the menkes protein in intestinal epithelium of ATP7A transgenic mice. J. Nutr. 135, 2762\u20132766 (2005).","journal-title":"J. Nutr."},{"key":"BFncomms10640_CR20","doi-asserted-by":"publisher","first-page":"1215","DOI":"10.1073\/pnas.0336230100","volume":"100","author":"I Hamza","year":"2003","unstructured":"Hamza, I., Prohaska, J. & Gitlin, J. D. Essential role for Atox1 in the copper-mediated intracellular trafficking of the Menkes ATPase. Proc. Natl Acad. Sci. USA 100, 1215\u20131220 (2003).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFncomms10640_CR21","doi-asserted-by":"publisher","first-page":"6084","DOI":"10.1002\/j.1460-2075.1996.tb00997.x","volume":"15","author":"MJ Petris","year":"1996","unstructured":"Petris, M. J. et al. Ligand-regulated transport of the Menkes copper P-type ATPase efflux pump from the Golgi apparatus to the plasma membrane: a novel mechanism of regulated trafficking. EMBO J. 15, 6084\u20136095 (1996).","journal-title":"EMBO J."},{"key":"BFncomms10640_CR22","doi-asserted-by":"publisher","first-page":"2855","DOI":"10.1093\/hmg\/11.23.2855","volume":"11","author":"C Cobbold","year":"2002","unstructured":"Cobbold, C. Novel membrane traffic steps regulate the exocytosis of the Menkes disease ATPase. Hum. Mol. Genet. 11, 2855\u20132866 (2002).","journal-title":"Hum. Mol. Genet."},{"key":"BFncomms10640_CR23","doi-asserted-by":"publisher","first-page":"9157","DOI":"10.1074\/jbc.M709463200","volume":"283","author":"S Itoh","year":"2008","unstructured":"Itoh, S. et al. Novel role of antioxidant-1 (Atox1) as a copper-dependent transcription factor involved in cell proliferation. J. Biol. Chem. 283, 9157\u20139167 (2008).","journal-title":"J. Biol. Chem."},{"key":"BFncomms10640_CR24","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1007\/s00775-013-1087-0","volume":"19","author":"W Beaino","year":"2014","unstructured":"Beaino, W., Guo, Y., Chang, A. J. & Anderson, C. J. Roles of Atox1 and p53 in the trafficking of copper-64 to tumor cell nuclei: implications for cancer therapy. J. Biol. Inorg. Chem. 19, 427\u2013438 (2014).","journal-title":"J. Biol. Inorg. Chem."},{"key":"BFncomms10640_CR25","doi-asserted-by":"publisher","first-page":"1209","DOI":"10.1016\/j.cell.2009.06.042","volume":"138","author":"Y Yan","year":"2009","unstructured":"Yan, Y., Sabharwal, P., Rao, M. & Sockanathan, S. The antioxidant enzyme Prdx1 controls neuronal differentiation by thiol-redox-dependent activation of GDE2. Cell 138, 1209\u20131221 (2009).","journal-title":"Cell"},{"key":"BFncomms10640_CR26","doi-asserted-by":"publisher","first-page":"553","DOI":"10.1038\/nmeth.1212","volume":"5","author":"M Gutscher","year":"2008","unstructured":"Gutscher, M. et al. Real-time imaging of the intracellular glutathione redox potential. Nat. Methods 5, 553\u2013559 (2008).","journal-title":"Nat. Methods"},{"key":"BFncomms10640_CR27","doi-asserted-by":"publisher","first-page":"592","DOI":"10.1002\/dvdy.20161","volume":"231","author":"M Rao","year":"2004","unstructured":"Rao, M., Baraban, J. H., Rajaii, F. & Sockanathan, S. In vivo comparative study of RNAi methodologies by inovo electroporation in the chick embryo. Dev. Dyn. 231, 592\u2013600 (2004).","journal-title":"Dev. Dyn."},{"key":"BFncomms10640_CR28","doi-asserted-by":"publisher","first-page":"867","DOI":"10.1023\/A:1023219308890","volume":"28","author":"V Gerbasi","year":"2003","unstructured":"Gerbasi, V., Lutsenko, S. & Lewis, E. J. A mutation in the ATP7B copper transporter causes reduced dopamine beta-hydroxylase and norepinephrine in mouse adrenal. Neurochem. Res. 28, 867\u2013873 (2003).","journal-title":"Neurochem. Res."},{"key":"BFncomms10640_CR29","doi-asserted-by":"publisher","first-page":"46632","DOI":"10.1074\/jbc.M206246200","volume":"277","author":"NE Hellman","year":"2002","unstructured":"Hellman, N. E. et al. Mechanisms of copper incorporation into human ceruloplasmin. J. Biol. Chem. 277, 46632\u201346638 (2002).","journal-title":"J. Biol. Chem."},{"key":"BFncomms10640_CR30","doi-asserted-by":"publisher","first-page":"334","DOI":"10.1096\/fj.05-4564fje","volume":"20","author":"Z Qin","year":"2006","unstructured":"Qin, Z., Itoh, S., Jeney, V., Ushio-Fukai, M. & Fukai, T. Essential role for the Menkes ATPase in activation of extracellular superoxide dismutase: implication for vascular oxidative stress. FASEB J. 20, 334\u2013336 (2006).","journal-title":"FASEB J."},{"key":"BFncomms10640_CR31","doi-asserted-by":"publisher","first-page":"551","DOI":"10.1146\/annurev.bi.57.070188.003003","volume":"57","author":"LC Stewart","year":"1988","unstructured":"Stewart, L. C. & Klinman, J. P. Dopamine beta-hydroxylase of adrenal chromaffin granules: structure and function. Annu. Rev. Biochem. 57, 551\u2013592 (1988).","journal-title":"Annu. Rev. Biochem."},{"key":"BFncomms10640_CR32","doi-asserted-by":"publisher","first-page":"717","DOI":"10.1083\/jcb.117.4.717","volume":"117","author":"SL Milgram","year":"1992","unstructured":"Milgram, S. L., Johnson, R. C. & Mains, R. E. Expression of individual forms of peptidylglycine alpha-amidating monooxygenase in AtT-20 cells: endoproteolytic processing and routing to secretory granules. J. Cell Biol. 117, 717\u2013728 (1992).","journal-title":"J. Cell Biol."},{"key":"BFncomms10640_CR33","doi-asserted-by":"publisher","first-page":"9215","DOI":"10.1074\/jbc.272.14.9215","volume":"272","author":"SJ Lin","year":"1997","unstructured":"Lin, S. J., Pufahl, R. A., Dancis, A., O\u2019Halloran, T. V. & Culotta, V. C. A role for the Saccharomyces cerevisiae ATX1 gene in copper trafficking and iron transport. J. Biol. Chem. 272, 9215\u20139220 (1997).","journal-title":"J. Biol. Chem."},{"key":"BFncomms10640_CR34","doi-asserted-by":"publisher","first-page":"605","DOI":"10.1111\/jnc.12438","volume":"127","author":"ED Gaier","year":"2013","unstructured":"Gaier, E. D. et al. Peptidylglycine \u03b1-amidating monooxygenase heterozygosity alters brain copper handling with region specificity. J. Neurochem. 127, 605\u2013619 (2013).","journal-title":"J. Neurochem."},{"key":"BFncomms10640_CR35","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1038\/sj.bjc.6604833","volume":"100","author":"A Bohlken","year":"2009","unstructured":"Bohlken, A. et al. ATP7A is a novel target of retinoic acid receptor beta2 in neuroblastoma cells. Br. J. Cancer 100, 96\u2013105 (2009).","journal-title":"Br. J. Cancer"},{"key":"BFncomms10640_CR36","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1038\/nrneurol.2010.180","volume":"7","author":"SG Kaler","year":"2011","unstructured":"Kaler, S. G. ATP7A-related copper transport diseases-emerging concepts and future trends. Nat. Rev. Neurol. 7, 15\u201329 (2011).","journal-title":"Nat. Rev. Neurol."},{"key":"BFncomms10640_CR37","doi-asserted-by":"publisher","first-page":"1865","DOI":"10.1089\/ars.2006.8.1865","volume":"8","author":"DP Jones","year":"2006","unstructured":"Jones, D. P. Redefining oxidative stress. Antioxid. Redox Signal. 8, 1865\u20131879 (2006).","journal-title":"Antioxid. Redox Signal."},{"key":"BFncomms10640_CR38","doi-asserted-by":"publisher","first-page":"997","DOI":"10.1038\/nature02989","volume":"431","author":"K Ito","year":"2004","unstructured":"Ito, K. et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431, 997\u20131002 (2004).","journal-title":"Nature"},{"key":"BFncomms10640_CR39","doi-asserted-by":"publisher","first-page":"2636","DOI":"10.1128\/MCB.01194-09","volume":"30","author":"N Coant","year":"2010","unstructured":"Coant, N. et al. NADPH oxidase 1 modulates WNT and NOTCH1 signaling to control the fate of proliferative progenitor cells in the colon. Mol. Cell Biol. 30, 2636\u20132650 (2010).","journal-title":"Mol. Cell Biol."},{"key":"BFncomms10640_CR40","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1038\/nrc2981","volume":"11","author":"RA Cairns","year":"2011","unstructured":"Cairns, R. A., Harris, I. S. & Mak, T. W. Regulation of cancer cell metabolism. Nat. Rev. Cancer 11, 85\u201395 (2011).","journal-title":"Nat. Rev. Cancer"},{"key":"BFncomms10640_CR41","doi-asserted-by":"publisher","first-page":"296","DOI":"10.1126\/science.270.5234.296","volume":"270","author":"M Sundaresan","year":"1995","unstructured":"Sundaresan, M., Yu, Z. X., Ferrans, V. J., Irani, K. & Finkel, T. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 270, 296\u2013299 (1995).","journal-title":"Science"},{"key":"BFncomms10640_CR42","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1023\/A:1006852306789","volume":"174","author":"B Schulz","year":"1997","unstructured":"Schulz, B., Matthews, T., Klockgether, T., Dichgans, J. & Beal, F. The role of mitochondrial dysfunction and neuronal nitric oxide in animal models of neurodegenerative diseases. Mol. Cell Biochem. 174, 193\u2013197 (1997).","journal-title":"Mol. Cell Biochem."},{"key":"BFncomms10640_CR43","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1096\/fj.02-0259fje","volume":"17","author":"T S\u00f6derdahl","year":"2003","unstructured":"S\u00f6derdahl, T. et al. Visualization of the compartmentalization of glutathione and protein-glutathione mixed disulfides in cultured cells. FASEB J. 17, 124\u2013126 (2003).","journal-title":"FASEB J."},{"key":"BFncomms10640_CR44","doi-asserted-by":"publisher","first-page":"196","DOI":"10.1152\/physiolgenomics.00058.2004","volume":"18","author":"JE Conour","year":"2004","unstructured":"Conour, J. E., Graham, W. V. & Gaskins, H. R. A combined in vitro\/bioinformatic investigation of redox regulatory mechanisms governing cell cycle progression. Physiol. Genomics 18, 196\u2013205 (2004).","journal-title":"Physiol. Genomics"},{"key":"BFncomms10640_CR45","doi-asserted-by":"publisher","first-page":"3133","DOI":"10.1517\/14656566.8.18.3133","volume":"8","author":"T Aoki","year":"2007","unstructured":"Aoki, T., Hashimoto, N. & Matsutani, M. Management of glioblastoma. Expert Opin. Pharmacother. 8, 3133\u20133146 (2007).","journal-title":"Expert Opin. Pharmacother."},{"key":"BFncomms10640_CR46","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1038\/nprot.2006.4","volume":"1","author":"H Sch\u00e4gger","year":"2006","unstructured":"Sch\u00e4gger, H. Tricine-SDS-PAGE. Nat. Protoc. 1, 16\u201322 (2006).","journal-title":"Nat. Protoc."},{"key":"BFncomms10640_CR47","doi-asserted-by":"publisher","first-page":"680","DOI":"10.1038\/227680a0","volume":"227","author":"UK Laemmli","year":"1970","unstructured":"Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680\u2013685 (1970).","journal-title":"Nature"},{"key":"BFncomms10640_CR48","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1016\/j.ydbio.2010.02.032","volume":"341","author":"G Periz","year":"2010","unstructured":"Periz, G., Yan, Y., Bitzer, Z. T. & Sockanathan, S. GDP-bound Galphai2 regulates spinal motor neuron differentiation through interaction with GDE2. Dev. Biol. 341, 213\u2013221 (2010).","journal-title":"Dev. Biol."}],"container-title":["Nature Communications"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/ncomms10640.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/ncomms10640","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/ncomms10640.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,4]],"date-time":"2023-01-04T11:44:23Z","timestamp":1672832663000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/ncomms10640"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,2,16]]},"references-count":48,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2016,4,22]]}},"alternative-id":["BFncomms10640"],"URL":"https:\/\/doi.org\/10.1038\/ncomms10640","relation":{},"ISSN":["2041-1723"],"issn-type":[{"value":"2041-1723","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,2,16]]},"assertion":[{"value":"17 August 2015","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 January 2016","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 February 2016","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"10640"}}