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Endosomal sorting of Notch receptors through COMMD9-dependent pathways modulates Notch signaling

Li, Haiying, Koo, Yeon, Mao, Xicheng, Sifuentes-Dominguez, Luis, Morris, Lindsey L., Jia, Da, Miyata, Naoteru, Faulkner, Rebecca A., van Deursen, Jan M., Vooijs, Marc, Billadeau, Daniel D., van de Sluis, Bart, Cleaver, Ondine, Burstein, Ezra·2015·Journal of Cell Biology
DOI 10.1083/jcb.201505108PMC PMC4639872
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Abstract

Notch family members are transmembrane receptors that mediate essential developmental programs. Upon ligand binding, a proteolytic event releases the intracellular domain of Notch, which translocates to the nucleus to regulate gene transcription. In addition, Notch trafficking across the endolysosomal system is critical in its regulation. In this study we report that Notch recycling to the cell surface is dependent on the COMMD–CCDC22–CCDC93 (CCC) complex, a recently identified regulator of endosomal trafficking. Disruption in this system leads to intracellular accumulation of Notch2 and concomitant reduction in Notch signaling. Interestingly, among the 10 copper metabolism MURR1 domain containing (COMMD) family members that can associate with the CCC complex, only COMMD9 and its binding partner, COMMD5, have substantial effects on Notch. Furthermore, Commd9 deletion in mice leads to embryonic lethality and complex cardiovascular alterations that bear hallmarks of Notch deficiency. Altogether, these studies highlight that the CCC complex controls Notch activation by modulating its intracellular trafficking and demonstrate cargo-specific effects for members of the COMMD protein family.

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Crossref · 10.1083/jcb.201505108

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  • Retriever and CCC play crucial roles in endosomal recycling of membrane proteins.

    “Retriever, a trimeric complex of VPS35L, VPS26C and VPS29, together with the CCC complex comprising CCDC22, CCDC93, and COMMD proteins, plays a crucial role in this process.”

    From Structural organization of the retriever–CCC endosomal recycling complex (2024) · cites this paper as [23]

    The Introduction identifies CCC as a COMMD–CCDC22–CCDC93 complex, and the Discussion reports its role in endosomal sorting and delivery of Notch to the cell surface (page numbers unavailable). The paper discusses retromer, not Retriever; it does not establish Retriever’s stated composition or role alongside CCC. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • CCDC22, CCDC93, and seven COMMDs form the CCC complex, which is required for endosomal recycling of certain cargos including copper transporters, Notch family members and LDLR.

    “These form the CCC complex39, shown to be required for the endosomal recycling of certain cargos, including copper transporters39, Notch family members39, 40 and LDLR41.”

    From Retriever is a multiprotein complex for retromer-independent endosomal cargo recycling (2017) · cites this paper as [40]

    The Introduction identifies CCDC22 and CCDC93 as CCC-complex components and reports COMMD1-dependent endosomal sorting of the copper transporter ATP7A. The Results show that loss of COMMD9 or other CCC components reduces cell-surface Notch2 and causes its accumulation in early endosomes. Our copy does not establish that the complex contains exactly seven COMMDs; it instead describes variable COMMD-containing configurations. LDLR is cited separately as reference 41 in the citing sentence, so it is not assessed as a claim attributed to this paper. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • The CCC complex has been recognized for its role in regulating endosomal recycling of various cargos.

    “The CCC complex is a molecular assembly that has been recognized for its role in regulating endosomal recycling of various cargos20,27,30–32,34”

    From Endosomal PI(3)P regulation by the COMMD/CCDC22/CCDC93 (CCC) complex controls membrane protein recycling (2019) · cites this paper as [34]

  • Retriever is a trimeric complex of VPS35L, VPS26C and VPS29.

    “Retriever, a trimeric complex of VPS35L, VPS26C and VPS29, together with the CCC complex comprising CCDC22, CCDC93, and COMMD proteins, plays a crucial role in this process.”

    From Structural organization of the retriever–CCC endosomal recycling complex (2024) · cites this paper as [23]

    The Results section on the COMMD9 interactome identifies CCC components, and the Results section on Notch2 surface levels discusses the retromer subunit VPS35; neither describes Retriever. Searches for Retriever, VPS35L, VPS26C, and the proposed trimer found no passage in our copy establishing its composition. Page numbers were not available. (LLM, conf=0.76)

    Experimental — accuracy not yet measured

  • Loss of VPS35L impairs ITGB1 endosomal recycling, observed in Huh-7 VPS35L knockout cells rescued by empty vector with significant endosomal trapping of ITGB1.

    “Loss of VPS35L is known to impair ITGB1 endosomal recycling22,23, which was also observed in Huh-7 VPS35L knockout cells rescued by empty vector (EV), where we observed significant endosomal trapping of ITGB1 (Fig. 4C, D).”

    From Structural organization of the retriever–CCC endosomal recycling complex (2024) · cites this paper as [23]

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Research works printed but not linked: 64

  1. Baladrón, 2005, dlk acts as a negative regulator of Notch1 activation through interactions with specific EGF-like repeats, Exp. Cell Res., 303, 343, 10.1016/j.yexcr.2004.10.001 · DOI · Paper page
  2. Baron, 2012, Endocytic routes to Notch activation, Semin. Cell Dev. Biol., 23, 437, 10.1016/j.semcdb.2012.01.008 · DOI
  3. Biasio, 2004, Identification of Murr1 as a regulator of the human δ epithelial sodium channel, J. Biol. Chem., 279, 5429, 10.1074/jbc.M311155200 · DOI
  4. Burstein, 2005, COMMD proteins, a novel family of structural and functional homologs of MURR1, J. Biol. Chem., 280, 22222, 10.1074/jbc.M501928200 · DOI · Paper page
  5. Chastagner, 2006, Itch/AIP4 mediates Deltex degradation through the formation of K29-linked polyubiquitin chains, EMBO Rep., 7, 1147, 10.1038/sj.embor.7400822 · DOI
  6. Cotton, 2013, Numb inhibits the recycling of Sanpodo in Drosophila sensory organ precursor, Curr. Biol., 23, 581, 10.1016/j.cub.2013.02.020 · DOI
  7. Couturier, 2013, Numb localizes at endosomes and controls the endosomal sorting of notch after asymmetric division in Drosophila, Curr. Biol., 23, 588, 10.1016/j.cub.2013.03.002 · DOI
  8. Couturier, 2014, A fluorescent tagging approach in Drosophila reveals late endosomal trafficking of Notch and Sanpodo, J. Cell Biol., 207, 351, 10.1083/jcb.201407071 · DOI
  9. Derivery, 2009, The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex, Dev. Cell., 17, 712, 10.1016/j.devcel.2009.09.010 · DOI · Paper page
  10. Derivery, 2012, Actin polymerization controls the organization of WASH domains at the surface of endosomes, PLoS One., 7, e39774, 10.1371/journal.pone.0039774 · DOI · Paper page
  11. Devlin, 2003, HCaRG is a novel regulator of renal epithelial cell growth and differentiation causing G2M arrest, Am. J. Physiol. Renal Physiol., 284, F753, 10.1152/ajprenal.00252.2002 · DOI
  12. Dontje, 2006, Delta-like1-induced Notch1 signaling regulates the human plasmacytoid dendritic cell versus T-cell lineage decision through control of GATA-3 and Spi-B, Blood., 107, 2446, 10.1182/blood-2005-05-2090 · DOI
  13. Drévillon, 2011, COMMD1-mediated ubiquitination regulates CFTR trafficking, PLoS One., 6, e18334, 10.1371/journal.pone.0018334 · DOI
  14. Fischbach, 2005, WAGR syndrome: A clinical review of 54 cases, Pediatrics., 116, 984, 10.1542/peds.2004-0467 · DOI
  15. Fischer, 2004, The Notch target genes Hey1 and Hey2 are required for embryonic vascular development, Genes Dev., 18, 901, 10.1101/gad.291004 · DOI
  16. Fortini, 2009, Endocytic regulation of Notch signaling, Curr. Opin. Genet. Dev., 19, 323, 10.1016/j.gde.2009.04.005 · DOI
  17. Freeman, 2014, RME-8 coordinates the activity of the WASH complex with the function of the retromer SNX dimer to control endosomal tubulation, J. Cell Sci., 127, 2053, 10.1242/jcs.144659 · DOI
  18. Gomez, 2009, A FAM21-containing WASH complex regulates retromer-dependent sorting, Dev. Cell., 17, 699, 10.1016/j.devcel.2009.09.009 · DOI · Paper page
  19. Gomez, 2012, Trafficking defects in WASH-knockout fibroblasts originate from collapsed endosomal and lysosomal networks, Mol. Biol. Cell., 23, 3215, 10.1091/mbc.E12-02-0101 · DOI · Paper page
  20. Gridley, 2010, Notch signaling in the vasculature, Curr. Top. Dev. Biol., 92, 277, 10.1016/S0070-2153(10)92009-7 · DOI
  21. Hamada, 1999, Mutation in ankyrin repeats of the mouse Notch2 gene induces early embryonic lethality, Development., 126, 3415, 10.1242/dev.126.15.3415 · DOI
  22. Harbour, 2012, Recruitment of the endosomal WASH complex is mediated by the extended ‘tail’ of Fam21 binding to the retromer protein Vps35, Biochem. J., 442, 209, 10.1042/BJ20111761 · DOI · Paper page
  23. Hayashi, 2002, Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain, Mech. Dev., 119, S97, 10.1016/S0925-4773(03)00099-6 · DOI
  24. High, 2008, The multifaceted role of Notch in cardiac development and disease, Nat. Rev. Genet., 9, 49, 10.1038/nrg2279 · DOI
  25. Holtwick, 2002, Smooth muscle-selective deletion of guanylyl cyclase-A prevents the acute but not chronic effects of ANP on blood pressure, Proc. Natl. Acad. Sci. USA., 99, 7142, 10.1073/pnas.102650499 · DOI
  26. Hori, 2011, Synergy between the ESCRT-III complex and Deltex defines a ligand-independent Notch signal, J. Cell Biol., 195, 1005, 10.1083/jcb.201104146 · DOI
  27. Hori, 2012, Regulation of ligand-independent Notch signal through intracellular trafficking, Commun. Integr. Biol., 5, 374, 10.4161/cib.19995 · DOI
  28. Jia, 2010, WASH and WAVE actin regulators of the Wiskott-Aldrich syndrome protein (WASP) family are controlled by analogous structurally related complexes, Proc. Natl. Acad. Sci. USA., 107, 10442, 10.1073/pnas.0913293107 · DOI · Paper page
  29. Jia, 2012, Multiple repeat elements within the FAM21 tail link the WASH actin regulatory complex to the retromer, Mol. Biol. Cell., 23, 2352, 10.1091/mbc.E11-12-1059 · DOI · Paper page
  30. Kandachar, 2012, Endocytosis and control of Notch signaling, Curr. Opin. Cell Biol., 24, 534, 10.1016/j.ceb.2012.06.006 · DOI
  31. Kisanuki, 2001, Tie2-Cre transgenic mice: A new model for endothelial cell-lineage analysis in vivo, Dev. Biol., 230, 230, 10.1006/dbio.2000.0106 · DOI · Paper page
  32. Kopan, 2012, Notch signaling, Cold Spring Harb. Perspect. Biol., 4, a011213, 10.1101/cshperspect.a011213 · DOI · Paper page
  33. Lawson, 2001, Notch signaling is required for arterial-venous differentiation during embryonic vascular development, Development., 128, 3675, 10.1242/dev.128.19.3675 · DOI
  34. Liu, 2013, Functional interaction of COMMD3 and COMMD9 with the epithelial sodium channel, Am. J. Physiol. Renal Physiol., 305, F80, 10.1152/ajprenal.00158.2013 · DOI
  35. Maine, 2007, COMMD proteins: COMMing to the scene, Cell. Mol. Life Sci., 64, 1997, 10.1007/s00018-007-7078-y · DOI
  36. Maine, 2007, COMMD1 promotes the ubiquitination of NF-kappaB subunits through a cullin-containing ubiquitin ligase, EMBO J., 26, 436, 10.1038/sj.emboj.7601489 · DOI
  37. Mali, 2013, RNA-guided human genome engineering via Cas9, Science., 339, 823, 10.1126/science.1232033 · DOI · Paper page
  38. McCright, 2006, Generation of new Notch2 mutant alleles, Genesis., 44, 29, 10.1002/gene.20181 · DOI
  39. McFadden, 2005, The Hand1 and Hand2 transcription factors regulate expansion of the embryonic cardiac ventricles in a gene dosage-dependent manner, Development., 132, 189, 10.1242/dev.01562 · DOI
  40. McGill, 2009, Numb regulates post-endocytic trafficking and degradation of Notch1, J. Biol. Chem., 284, 26427, 10.1074/jbc.M109.014845 · DOI
  41. Mizushima, 1990, pEF-BOS, a powerful mammalian expression vector, Nucleic Acids Res., 18, 5322, 10.1093/nar/18.17.5322 · DOI
  42. Phillips-Krawczak, 2015, COMMD1 is linked to the WASH complex and regulates endosomal trafficking of the copper transporter ATP7A, Mol. Biol. Cell., 26, 91, 10.1091/mbc.E14-06-1073 · DOI · Paper page
  43. Reichardt, 2013, Cell biology: Notch recycling is numbed, Curr. Biol., 23, R270, 10.1016/j.cub.2013.03.013 · DOI
  44. Rottner, 2010, WASH, WHAMM and JMY: Regulation of Arp2/3 complex and beyond, Trends Cell Biol., 20, 650, 10.1016/j.tcb.2010.08.014 · DOI
  45. Sakata, 2004, Drosophila Nedd4 regulates endocytosis of notch and suppresses its ligand-independent activation, Curr. Biol., 14, 2228, 10.1016/j.cub.2004.12.028 · DOI
  46. Seaman, 2013, Retromer-mediated endosomal protein sorting: All WASHed up!, Trends Cell Biol., 23, 522, 10.1016/j.tcb.2013.04.010 · DOI
  47. Shalem, 2014, Genome-scale CRISPR-Cas9 knockout screening in human cells, Science., 343, 84, 10.1126/science.1247005 · DOI · Paper page
  48. Smith, 2013, COMMD1 interacts with the COOH terminus of NKCC1 in Calu-3 airway epithelial cells to modulate NKCC1 ubiquitination, Am. J. Physiol. Cell Physiol., 305, C133, 10.1152/ajpcell.00394.2012 · DOI
  49. Starokadomskyy, 2013, CCDC22 deficiency in humans blunts activation of proinflammatory NF-κB signaling, J. Clin. Invest., 123, 2244, 10.1172/JCI66466 · DOI · Paper page
  50. Steinberg, 2013, A global analysis of SNX27-retromer assembly and cargo specificity reveals a function in glucose and metal ion transport, Nat. Cell Biol., 15, 461, 10.1038/ncb2721 · DOI · Paper page
  51. Tao, 2003, The copper toxicosis gene product Murr1 directly interacts with the Wilson disease protein, J. Biol. Chem., 278, 41593, 10.1074/jbc.C300391200 · DOI
  52. Troost, 2012, The tumour suppressor Lethal (2) giant discs is required for the function of the ESCRT-III component Shrub/CHMP4, J. Cell Sci., 125, 763, 10.1242/jcs.097261 · DOI
  53. van de Sluis, 2002, Identification of a new copper metabolism gene by positional cloning in a purebred dog population, Hum. Mol. Genet., 11, 165, 10.1093/hmg/11.2.165 · DOI · Paper page
  54. van de Sluis, 2007, Increased activity of hypoxia-inducible factor 1 is associated with early embryonic lethality in Commd1 null mice, Mol. Cell. Biol., 27, 4142, 10.1128/MCB.01932-06 · DOI · Paper page
  55. van de Sluis, 2010, COMMD1 disrupts HIF-1α/β dimerization and inhibits human tumor cell invasion, J. Clin. Invest., 120, 2119, 10.1172/JCI40583 · DOI
  56. Vonk, 2011, Liver-specific Commd1 knockout mice are susceptible to hepatic copper accumulation, PLoS One., 6, e29183, 10.1371/journal.pone.0029183 · DOI
  57. Wang, 2012, Notch2 and Notch3 function together to regulate vascular smooth muscle development, PLoS One., 7, e37365, 10.1371/journal.pone.0037365 · DOI
  58. Wilkin, 2008, 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, 10.1016/j.devcel.2008.09.002 · DOI
  59. Wilkin, 2004, Regulation of notch endosomal sorting and signaling by Drosophila Nedd4 family proteins, Curr. Biol., 14, 2237, 10.1016/j.cub.2004.11.030 · DOI
  60. Wright, 2009, The aryl hydrocarbon nuclear translocator alters CD30-mediated NF-kappaB-dependent transcription, Science, 323, 251, 10.1126/science.1162818 · DOI
  61. Xu, 2009, Rasip1 is required for endothelial cell motility, angiogenesis and vessel formation, Dev. Biol., 329, 269, 10.1016/j.ydbio.2009.02.033 · DOI
  62. Xu, 2008, Characterization of 11p14-p12 deletion in WAGR syndrome by array CGH for identifying genes contributing to mental retardation and autism, Cytogenet. Genome Res., 122, 181, 10.1159/000172086 · DOI
  63. Zagouras, 1995, Alterations in Notch signaling in neoplastic lesions of the human cervix, Proc. Natl. Acad. Sci. USA., 92, 6414, 10.1073/pnas.92.14.6414 · DOI
  64. Zheng, 2012, ShRNA-targeted COMMD7 suppresses hepatocellular carcinoma growth, PLoS One., 7, e45412, 10.1371/journal.pone.0045412 · DOI

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Metadata

Authors
Li, H., Koo, Y., Mao, X., Sifuentes-Dominguez, L., Morris, L. L., Jia, D., Miyata, N., Faulkner, R. A., van Deursen, J. M., Vooijs, M., Billadeau, D. D., van de Sluis, B., Cleaver, O., & Burstein, E.
Venue
Journal of Cell Biology
Publisher
Rockefeller University Press
Published
2015-11-09
Volume
211
Issue
3
Pages
605-617
ISSN
  • 0021-9525
  • 1540-8140
DOI
10.1083/jcb.201505108
PMC
PMC4639872
Cited by
73
References
1
Language
en

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