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The endocytic matrix

Nature volume 463, pages 464–473 (2010)Cite this article

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Abstract

Endocytosis has long been thought of as simply a way for cells to internalize nutrients and membrane-associated molecules. But an explosive growth in knowledge has given a new dimension to our understanding of this process. It now seems that endocytosis is a master organizer of signalling circuits, with one of its main roles being the resolution of signals in space and time. Many of the functions of endocytosis that are emerging from recent research cannot yet be reconciled with the canonical view of intracellular trafficking but, instead, point to endocytosis being integrated at a deeper level in the cellular 'master plan' (the cellular network of signalling circuits that lie at the base of the cell's make-up). Deconvolution of this level, which we call the 'endocytic matrix', might uncover a fundamental aspect of how a cell is built.

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Figure 1: Endocytic trafficking of signalling receptors.
Figure 2: Endocytosis controls signals at the plasma membrane.
Figure 3: The signalling endosome.
Figure 4: Cell migration harnesses EECs.
Figure 5: The endocytic machinery in cell-cycle progression, transcription and mitosis.

References

  1. Doherty, G. J. & McMahon, H. T. Mechanisms of endocytosis. Annu. Rev. Biochem. 78, 857–902 (2009).

    Article  CAS  PubMed  Google Scholar 

  2. Mayor, S. & Pagano, R. E. Pathways of clathrin-independent endocytosis. Nature Rev. Mol. Cell Biol. 8, 603–612 (2007).

    Article  CAS  Google Scholar 

  3. Sorkin, A. & von Zastrow, M. Endocytosis and signalling: intertwining molecular networks. Nature Rev. Mol. Cell Biol. 10, 609–622 (2009).

    Article  CAS  Google Scholar 

  4. Lanzetti, L. & Di Fiore, P. P. Endocytosis and cancer: an 'insider' network with dangerous liaisons. Traffic 9, 2011–2021 (2008).

    Article  CAS  PubMed  Google Scholar 

  5. Mills, I. G. The interplay between clathrin-coated vesicles and cell signalling. Semin. Cell Dev. Biol. 18, 459–470 (2007).

    Article  CAS  PubMed  Google Scholar 

  6. Fortini, M. E. Notch signaling: the core pathway and its posttranslational regulation. Dev. Cell 16, 633–647 (2009).

    Article  CAS  PubMed  Google Scholar 

  7. Di Guglielmo, G. M., Le Roy, C., Goodfellow, A. F. & Wrana, J. L. Distinct endocytic pathways regulate TGF-β receptor signalling and turnover. Nature Cell Biol. 5, 410–421 (2003).

    Article  PubMed  CAS  Google Scholar 

  8. Sigismund, S. et al. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev. Cell 15, 209–219 (2008).

    Article  CAS  PubMed  Google Scholar 

  9. Yamamoto, H., Sakane, H., Michiue, T. & Kikuchi, A. Wnt3a and Dkk1 regulate distinct internalization pathways of LRP6 to tune the activation of β-catenin signaling. Dev. Cell 15, 37–48 (2008).

    Article  CAS  PubMed  Google Scholar 

  10. Fehrenbacher, N., Bar-Sagi, D. & Philips, M. Ras/MAPK signaling from endomembranes. Mol. Oncol. 3, 297–307 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Pawson, T. Dynamic control of signaling by modular adaptor proteins. Curr. Opin. Cell Biol. 19, 112–116 (2007).

    Article  CAS  PubMed  Google Scholar 

  12. Tsukazaki, T., Chiang, T. A., Davison, A. F., Attisano, L. & Wrana, J. L. SARA, a FYVE domain protein that recruits Smad2 to the TGFβ receptor. Cell 95, 779–791 (1998).

    Article  CAS  PubMed  Google Scholar 

  13. Hayes, S., Chawla, A. & Corvera, S. TGFβ receptor internalization into EEA1-enriched early endosomes: role in signaling to Smad2. J. Cell Biol. 158, 1239–1249 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Chen, Y. G., Wang, Z., Ma, J., Zhang, L. & Lu, Z. Endofin, a FYVE domain protein, interacts with Smad4 and facilitates transforming growth factor-β signaling. J. Biol. Chem. 282, 9688–9695 (2007).

    Article  CAS  PubMed  Google Scholar 

  15. Miaczynska, M. et al. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116, 445–456 (2004).

    Article  CAS  PubMed  Google Scholar 

  16. Schenck, A. et al. The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell 133, 486–497 (2008). In zebrafish, Appl1 was shown to spatially restrict the activity of the signalling receptor Akt in endosomes, resulting in Akt substrates being biased towards Gsk3β and increased cell survival during animal development.

    Article  CAS  PubMed  Google Scholar 

  17. Zoncu, R. et al. A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 136, 1110–1121 (2009). Signalling through EGFR is controlled by the diversity and plasticity of the early endosome, which undergoes discrete maturation steps through a phosphoinositide switch from an early APPL endosome (where the induction of mitosis by EGFR is enhanced) to an endosome rich in PtdIns(3)P and EEA1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Birtwistle, M. R. & Kholodenko, B. N. Endocytosis and signalling: a meeting with mathematics. Mol. Oncol. 3, 308–320 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kholodenko, B. N. Four-dimensional organization of protein kinase signaling cascades: the roles of diffusion, endocytosis and molecular motors. J. Exp. Biol. 206, 2073–2082 (2003).

    Article  CAS  PubMed  Google Scholar 

  20. Maeder, C. I. et al. Spatial regulation of Fus3 MAP kinase activity through a reaction-diffusion mechanism in yeast pheromone signalling. Nature Cell Biol. 9, 1319–1326 (2007).

    Article  CAS  PubMed  Google Scholar 

  21. Perlson, E. et al. Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve. Neuron 45, 715–726 (2005).

    Article  CAS  PubMed  Google Scholar 

  22. Markevich, N. I., Tsyganov, M. A., Hoek, J. B. & Kholodenko, B. N. Long-range signaling by phosphoprotein waves arising from bistability in protein kinase cascades. Mol. Syst. Biol. 2, 61 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Disanza, A., Frittoli, E., Palamidessi, A. & Scita, G. Endocytosis and spatial restriction of cell signaling. Mol. Oncol. 3, 280–296 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Traynor, D. & Kay, R. R. Possible roles of the endocytic cycle in cell motility. J. Cell Sci. 120, 2318–2327 (2007).

    Article  CAS  PubMed  Google Scholar 

  25. Bryant, D. M. & Mostov, K. E. From cells to organs: building polarized tissue. Nature Rev. Mol. Cell Biol. 9, 887–901 (2008).

    Article  CAS  Google Scholar 

  26. Altschuler, S. J., Angenent, S. B., Wang, Y. & Wu, L. F. On the spontaneous emergence of cell polarity. Nature 454, 88–889 (2008).

    Article  CAS  Google Scholar 

  27. Jekely, G., Sung, H. H., Luque, C. M. & Rorth, P. Regulators of endocytosis maintain localized receptor tyrosine kinase signaling in guided migration. Dev. Cell 9, 197–207 (2005).

    Article  CAS  PubMed  Google Scholar 

  28. Palamidessi, A. et al. Endocytic trafficking of Rac is required for its activation and for the spatial restriction of signaling in cell migration. Cell 134, 135–147 (2008).

    Article  CAS  PubMed  Google Scholar 

  29. Caswell, P. T. et al. Rab25 associates with α5β1 integrin to promote invasive migration in 3D microenvironments. Dev. Cell 13, 496–510 (2007). RAB25 binds to the promigratory and invasive molecule α 5 β 1 -integrin, promoting rapid, spatially restricted recycling of the integrin, ultimately resulting in increased cellular migration and invasion in three-dimensional matrices.

    Article  CAS  PubMed  Google Scholar 

  30. del Pozo, M. A. et al. Integrins regulate Rac targeting by internalization of membrane domains. Science 303, 839–842 (2004).

    Article  CAS  PubMed  ADS  Google Scholar 

  31. del Pozo, M. A. et al. Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nature Cell Biol. 7, 901–908 (2005).

    Article  CAS  PubMed  Google Scholar 

  32. Balasubramanian, N., Scott, D. W., Castle, J. D., Casanova, J. E. & Schwartz, M. A. Arf6 and microtubules in adhesion-dependent trafficking of lipid rafts. Nature Cell Biol. 9, 1381–1391 (2007).

    Article  CAS  PubMed  Google Scholar 

  33. Royle, S. J., Bright, N. A. & Lagnado, L. Clathrin is required for the function of the mitotic spindle. Nature 434, 1152–1157 (2005).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  34. Thompson, H. M., Cao, H., Chen, J., Euteneuer, U. & McNiven, M. A. Dynamin 2 binds γ-tubulin and participates in centrosome cohesion. Nature Cell Biol. 6, 335–342 (2004).

    Article  CAS  PubMed  Google Scholar 

  35. Lehtonen, S. et al. The endocytic adaptor protein ARH associates with motor and centrosomal proteins and is involved in centrosome assembly and cytokinesis. Mol. Biol. Cell 19, 2949–2961 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Miserey-Lenkei, S. et al. A role for the Rab6A' GTPase in the inactivation of the Mad2-spindle checkpoint. EMBO J. 25, 278–289 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Boucrot, E. & Kirchhausen, T. Endosomal recycling controls plasma membrane area during mitosis. Proc. Natl Acad. Sci. USA 104, 7939–7944 (2007).

    Article  CAS  PubMed  ADS  Google Scholar 

  38. Meyers, J., Craig, J. & Odde, D. J. Potential for control of signaling pathways via cell size and shape. Curr. Biol. 16, 1685–1693 (2006).

    Article  CAS  PubMed  Google Scholar 

  39. Schweitzer, J. K., Burke, E. E., Goodson, H. V. & D' Souza-Schorey, C. Endocytosis resumes during late mitosis and is required for cytokinesis. J. Biol. Chem. 280, 41628–41635 (2005).

    Article  CAS  PubMed  Google Scholar 

  40. Baluska, F., Menzel, D. & Barlow, P. W. Cytokinesis in plant and animal cells: endosomes 'shut the door'. Dev. Biol. 294, 1–10 (2006).

    Article  CAS  PubMed  Google Scholar 

  41. Furthauer, M. & Gonzalez-Gaitan, M. Endocytosis, asymmetric cell division, stem cells and cancer: unus pro omnibus, omnes pro uno. Mol. Oncol. 3, 339–353 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Santolini, E. et al. Numb is an endocytic protein. J. Cell Biol. 151, 1345–1352 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Berdnik, D., Torok, T., Gonzalez-Gaitan, M. & Knoblich, J. A. The endocytic protein α-Adaptin is required for Numb-mediated asymmetric cell division in Drosophila. Dev. Cell 3, 221–231 (2002).

    Article  CAS  PubMed  Google Scholar 

  44. Hutterer, A. & Knoblich, J. A. Numb and α-Adaptin regulate Sanpodo endocytosis to specify cell fate in Drosophila external sensory organs. EMBO Rep. 6, 836–842 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Emery, G. et al. Asymmetric Rab11 endosomes regulate Delta recycling and specify cell fate in the Drosophila nervous system. Cell 122, 763–773 (2005).

    Article  CAS  PubMed  Google Scholar 

  46. Nilsson, L. et al. Caenorhabditis elegans num-1 negatively regulates endocytic recycling. Genetics 179, 375–387 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. McGill, M. A., Dho, S. E., Weinmaster, G. & McGlade, C. J. Numb regulates post-endocytic trafficking and degradation of Notch1. J. Biol. Chem. 284, 26427–26438 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Andrews, R. & Ahringer, J. Asymmetry of early endosome distribution in C. elegans embryos. PLoS ONE 2, e493 (2007).

    Article  PubMed  PubMed Central  ADS  CAS  Google Scholar 

  49. Beckmann, J., Scheitza, S., Wernet, P., Fischer, J. C. & Giebel, B. Asymmetric cell division within the human hematopoietic stem and progenitor cell compartment: identification of asymmetrically segregating proteins. Blood 109, 5494–5501 (2007).

    Article  CAS  PubMed  Google Scholar 

  50. Coumailleau, F., Furthauer, M., Knoblich, J. A. & Gonzalez-Gaitan, M. Directional Delta and Notch trafficking in Sara endosomes during asymmetric cell division. Nature 458, 1051–1055 (2009). During the asymmetrical division of fly sensory-organ-precursor cells, the asymmetrical partitioning of SARA endosomes containing Notch and its ligand Delta to the pIIa daughter cell limits Notch signalling in the pIIb cell, thereby maintaining the asymmetrical configuration of the pIIb–pIIa pair.

    Article  CAS  PubMed  ADS  Google Scholar 

  51. Gillette, J. M., Larochelle, A., Dunbar, C. E. & Lippincott-Schwartz, J. Intercellular transfer to signalling endosomes regulates an ex vivo bone marrow niche. Nature Cell Biol. 11, 303–311 (2009). A specialized membrane domain of haematopoietic progenitor cells is trans -endocytosed by osteoblasts and trafficked to SARA endosomes, where it triggers signalling that leads to attenuation of the SMAD2 and SMAD3 pathway and to expression of chemokines that promote the homing of haematopoietic progenitor cells.

    Article  CAS  PubMed  Google Scholar 

  52. Simons, M. & Raposo, G. Exosomes: vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 21, 575–581 (2009).

    Article  CAS  PubMed  Google Scholar 

  53. Valadi, H. et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature Cell Biol. 9, 654–659 (2007). A new endocytic-based mechanism of intercellular communication was uncovered, in which mRNA and microRNA are transported by exosomes, which can be transferred between the mast cells of different species, regulating gene transcription and protein expression.

    Article  CAS  PubMed  Google Scholar 

  54. Irion, U. & St Johnston, D. bicoid RNA localization requires specific binding of an endosomal sorting complex. Nature 445, 554–558 (2007). Components of ESCRT-II are found to bind to, and control, the localization of bicoid mRNA, which encodes a homeodomain-containing transcription factor that organizes anterior development in the fly, to the anterior of the D. melanogaster egg.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  55. Skog, J. et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nature Cell Biol. 10, 1470–1476 (2008).

    Article  CAS  PubMed  Google Scholar 

  56. Colaluca, I. N. et al. NUMB controls p53 tumour suppressor activity. Nature 451, 76–80 (2008).

    Article  CAS  PubMed  ADS  Google Scholar 

  57. Cicalese, A. et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 138, 1083–1095 (2009). An essential role for p53 in the regulation of cancer stem cells was uncovered in this study. In the Erbb2 -transgenic mouse model, decreased levels of p53 lead to breast cancer stem cells undergoing symmetrical divisions at a greater frequency, and pharmacological restoration of p53 levels in these animals results in increased asymmetrical division of breast cancer stem cells and a reduction in tumour growth.

    Article  CAS  PubMed  Google Scholar 

  58. Yu, X., Riley, T. & Levine, A. J. The regulation of the endosomal compartment by p53 the tumor suppressor gene. FEBS J. 276, 2201–2212 (2009).

    Article  CAS  PubMed  Google Scholar 

  59. Muller, P. A. J. et al. Mutant p53 drives invasion by promoting integrin recycling. Cell 139, 1327–1341 (2009). Gain-of-function mutants of p53 increase the endocytic recycling of α 5 β 1 -integrin and EGFR in cooperation with p63, promoting invasion and metastasis.

    Article  PubMed  Google Scholar 

  60. Pyrzynska, B., Pilecka, I. & Miaczynska, M. Endocytic proteins in the regulation of nuclear signaling, transcription and tumorigenesis. Mol. Oncol. 3, 321–338 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Stauffer, D. R., Howard, T. L., Nyun, T. & Hollenberg, S. M. CHMP1 is a novel nuclear matrix protein affecting chromatin structure and cell-cycle progression. J. Cell Sci. 114, 2383–2393 (2001).

    CAS  PubMed  Google Scholar 

  62. Enari, M., Ohmori, K., Kitabayashi, I. & Taya, Y. Requirement of clathrin heavy chain for p53-mediated transcription. Genes Dev. 20, 1087–1099 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Ohmori, K. et al. Monomeric but not trimeric clathrin heavy chain regulates p53-mediated transcription. Oncogene 27, 2215–2227 (2008).

    Article  CAS  PubMed  Google Scholar 

  64. Xiao, K. et al. Functional specialization of β-arrestin interactions revealed by proteomic analysis. Proc. Natl Acad. Sci. USA 104, 12011–12016 (2007).

    Article  CAS  PubMed  ADS  Google Scholar 

  65. Isokane, M. et al. Plasma-membrane-anchored growth factor pro-amphiregulin binds A-type lamin and regulates global transcription. J. Cell Sci. 121, 3608–3618 (2008).

    Article  CAS  PubMed  Google Scholar 

  66. Hieda, M. et al. Membrane-anchored growth factor, HB-EGF, on the cell surface targeted to the inner nuclear membrane. J. Cell Biol. 180, 763–769 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Mills, I. G. et al. Huntingtin interacting protein 1 modulates the transcriptional activity of nuclear hormone receptors. J. Cell Biol. 170, 191–200 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Jekely, G. Origin of eukaryotic endomembranes: a critical evaluation of different model scenarios. Adv. Exp. Med. Biol. 607, 38–51 (2007).

    Article  PubMed  Google Scholar 

  69. Ohya, T. et al. Reconstitution of Rab- and SNARE-dependent membrane fusion by synthetic endosomes. Nature 459, 1091–1097 (2009).

    Article  CAS  PubMed  ADS  Google Scholar 

  70. Snijder, B. et al. Population context determines cell-to-cell variability in endocytosis and virus infection. Nature 461, 520–523 (2009).

    Article  CAS  PubMed  ADS  Google Scholar 

  71. Pelkmans, L. et al. Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 436, 78–86 (2005).

    Article  CAS  PubMed  ADS  Google Scholar 

  72. Stenmark, H. Rab GTPases as coordinators of vesicle traffic. Nature Rev. Mol. Cell Biol. 10, 513–525 (2009).

    Article  CAS  Google Scholar 

  73. Donaldson, J. G. Arfs, phosphoinositides and membrane traffic. Biochem. Soc. Trans. 33, 1276–1278 (2005).

    Article  CAS  PubMed  Google Scholar 

  74. Raiborg, C. & Stenmark, H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445–452 (2009).

    Article  CAS  PubMed  ADS  Google Scholar 

  75. Zhao, C., Du, G., Skowronek, K., Frohman, M. A. & Bar-Sagi, D. Phospholipase D2-generated phosphatidic acid couples EGFR stimulation to Ras activation by Sos. Nature Cell Biol. 9, 706–712 (2007).

    CAS  PubMed  Google Scholar 

  76. Nada, S. et al. The novel lipid raft adaptor p18 controls endosome dynamics by anchoring the MEK–ERK pathway to late endosomes. EMBO J. 28, 477–489 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. DeWire, S. M., Ahn, S., Lefkowitz, R. J. & Shenoy, S. K. β-Arrestins and cell signaling. Annu. Rev. Physiol. 69, 483–510 (2007).

    Article  CAS  PubMed  Google Scholar 

  78. Pasternak, S. H. et al. Presenilin-1, nicastrin, amyloid precursor protein, and γ-secretase activity are co-localized in the lysosomal membrane. J. Biol. Chem. 278, 26687–26694 (2003).

    Article  CAS  PubMed  Google Scholar 

  79. Pei, Z. & Baker, N. E. Competition between Delta and the Abruptex domain of Notch. BMC Dev. Biol. 8, 4 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Vaccari, T., Lu, H., Kanwar, R., Fortini, M. E. & Bilder, D. Endosomal entry regulates Notch receptor activation in Drosophila melanogaster. J. Cell Biol. 180, 755–762 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Wilkin, M. et al. Drosophila HOPS and AP-3 complex genes are required for a Deltex-regulated activation of Notch in the endosomal trafficking pathway. Dev. Cell 15, 762–772 (2008).

    Article  CAS  PubMed  Google Scholar 

  82. Grande-Garcia, A. et al. Caveolin-1 regulates cell polarization and directional migration through Src kinase and Rho GTPases. J. Cell Biol. 177, 683–694 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We apologize to those colleagues whose primary research papers or important discoveries could not be properly acknowledged because of space constraints. We thank A. Sorkin and M. von Zastrow for sharing, ahead of publication, their excellent review on endocytosis and signalling. We also thank P. R. Romano for critically editing the manuscript. Work in the authors' laboratories is supported by grants from the following: the Italian Association for Cancer Research (AIRC) and the Italian Ministry of Education, University and Scientific Research (MIUR) (to G.S. and P.P.D.F.); the Association for International Cancer Research (G.S.); and the Italian Ministry of Health, the European Community, the European Research Council, the Cariplo Foundation, the Ferrari Foundation and the Monzino Foundation (P.P.D.F.).

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  1. IFOM, the FIRC Institute for Molecular Oncology Foundation, at the IFOM-IEO Campus, Via Adamello 16, Milan, 20139, Italy

    Giorgio Scita & Pier Paolo Di Fiore

  2. Department of Medicine, Surgery and Dentistry, Università degli Studi di Milano, Via A. Di Rudini 8, Milan, 20122, Italy

    Giorgio Scita & Pier Paolo Di Fiore

  3. Department of Experimental Oncology, European Institute of Oncology, at the IFOM-IEO Campus, Via Adamello 16, Milan, 20139, Italy

    Pier Paolo Di Fiore

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Scita, G., Di Fiore, P. The endocytic matrix. Nature 463, 464–473 (2010). https://doi.org/10.1038/nature08910

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