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Original Research Articles

Exosomal sorting of the viral oncoprotein LMP1 is restrained by TRAF2 association at signalling endosomes

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Article: 26334 | Received 16 Oct 2014, Accepted 03 Feb 2015, Published online: 10 Apr 2015

References

  • Scita G, Di Fiore PP. The endocytic matrix. Nature. 2010; 463: 464–73. [PubMed Abstract].
  • Joffre C, Barrow R, Menard L, Calleja V, Hart IR, Kermorgant S. A direct role for Met endocytosis in tumorigenesis. Nat Cell Biol. 2011; 13: 827–37. [PubMed Abstract].
  • Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med. 2012; 18: 883–91. [PubMed Abstract] [PubMed CentralFull Text].
  • "/>Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, Guha A et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol. 2008; 10: 619–24. [PubMed Abstract].
  • Sandilands E, Frame MC. Endosomal trafficking of Src tyrosine kinase. Trends Cell Biol. 2008; 18: 322–9. [PubMed Abstract].
  • Verweij FJ, van Eijndhoven MA, Hopmans ES, Vendrig T, Wurdinger T, Cahir-McFarland E et al. LMP1 association with CD63 in endosomes and secretion via exosomes limits constitutive NF-kappaB activation. EMBO J. 2011; 30: 2115–29. [PubMed Abstract] [PubMed CentralFull Text].
  • Meckes DG Jr., Shair KH, Marquitz AR, Kung CP, Edwards RH, Raab-Traub N. Human tumor virus utilizes exosomes for intercellular communication. Proc Natl Acad Sci USA. 2010; 107: 20370–5. [PubMed Abstract] [PubMed CentralFull Text].
  • Thorley-Lawson DA. Epstein-Barr virus: exploiting the immune system. Nat Rev Immunol. 2001; 1: 75–82. [PubMed Abstract].
  • Thorley-Lawson DA, Gross A. Persistence of the Epstein–Barr virus and the origins of associated lymphomas. N Engl J Med. 2004; 350: 1328–37. [PubMed Abstract].
  • Kulwichit W, Edwards RH, Davenport EM, Baskar JF, Godfrey V, Raab-Traub N. Expression of the Epstein-Barr virus latent membrane protein 1 induces B cell lymphoma in transgenic mice. Proc Natl Acad Sci USA. 1998; 95: 11963–8. [PubMed Abstract] [PubMed CentralFull Text].
  • Hömig-Hölzel C, Hojer C, Rastelli J, Casola S, Strobl LJ, Müller W et al. Constitutive CD40 signaling in B cells selectively activates the noncanonical NF-kappaB pathway and promotes lymphomagenesis. J Exp Med. 2008; 205: 1317–29.
  • Chung CH, Parker JS, Ely K, Carter J, Yi Y, Murphy BA et al. Gene expression profiles identify epithelial-to-mesenchymal transition and activation of nuclear factor-kappaB signaling as characteristics of a high-risk head and neck squamous cell carcinoma. Cancer Res. 2006; 66: 8210–18. [PubMed Abstract].
  • Yasui T, Luftig M, Soni V, Kieff E. Latent infection membrane protein transmembrane FWLY is critical for intermolecular interaction, raft localization. and signaling. Proc Natl Acad Sci USA. 2004; 101: 278–83.
  • Soni V, Yasui T, Cahir-McFarland E, Kieff E. LMP1 transmembrane domain 1 and 2 (TM1-2) FWLY mediates intermolecular interactions with TM3-6 to activate NF-kappa. B J Virol. 2006; 80: 10787–93.
  • Lee J, Sugden B. A membrane leucine heptad contributes to trafficking, signaling, and transformation by latent membrane protein 1. J Virol. 2007; 81: 9121–30. [PubMed Abstract] [PubMed CentralFull Text].
  • Sandberg M, Hammerschmidt W, Sugden B. Characterization of LMP-1's association with TRAF1, TRAF2, and TRAF3. J Virol. 1997; 71: 4649–56. [PubMed Abstract] [PubMed CentralFull Text].
  • Arcipowski KM, Stunz LL, Graham JP, Kraus ZJ, Vanden Bush TJ, Bishop GA. Molecular mechanisms of TNFR-associated factor 6 (TRAF6) utilization by the oncogenic viral mimic of CD40, latent membrane protein 1 (LMP1). J Biol Chem. 2011; 286: 9948–55. [PubMed Abstract] [PubMed CentralFull Text].
  • Guasparri I, Bubman D, Cesarman E. EBV LMP2A affects LMP1-mediated NF-kappaB signaling and survival of lymphoma cells by regulating TRAF2 expression. Blood. 2008; 111: 3813–20. [PubMed Abstract] [PubMed CentralFull Text].
  • Masui H, Wells A, Lazar CS, Rosenfeld MG, Gill GN. Enhanced tumorigenesis of NR6 cells which express non-down-regulating epidermal growth factor receptors. Cancer Res. 1991; 51: 6170–5. [PubMed Abstract].
  • Bobrie A, Colombo M, Raposo G, Théry C. Exosome secretion: molecular mechanisms and roles in immune responses. Traffic. 2011; 12: 1659–68. [PubMed Abstract].
  • Eden ER, White IJ, Futter CE. Down-regulation of epidermal growth factor receptor signalling within multivesicular bodies. Biochem Soc Trans. 2009; 37: 173–7. [PubMed Abstract].
  • Shen B, Wu N, Yang JM, Gould SJ. Protein targeting to exosomes/microvesicles by plasma membrane anchors. J Biol Chem. 2011; 286: 14383–95. [PubMed Abstract] [PubMed CentralFull Text].
  • Grandal MV, Zandi R, Pedersen MW, Willumsen BM, van Deurs B, Poulsen HS. EGFRvIII escapes down-regulation due to impaired internalization and sorting to lysosomes. Carcinogenesis. 2007; 28: 1408–17. [PubMed Abstract].
  • Verweij FJ, van Eijndhoven MAJ, Middeldorp J, Pegtel DM. Analysis of viral microRNA exchange via exosomes in vitro and in vivo. Methods Mol Biol. 2013; 1024: 53–68. [PubMed Abstract].
  • Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL et al. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA. 2010; 107: 6328–33. [PubMed Abstract] [PubMed CentralFull Text].
  • Verweij FJ, Middeldorp JM, Pegtel DM. Intracellular signaling controlled by the endosomal-exosomal pathway. Commun Integr Biol. 2012; 5: 88–93. [PubMed Abstract] [PubMed CentralFull Text].
  • Cai H, Smith DA, Memarzadeh S, Lowell CA, Cooper JA, Witte ON. Differential transformation capacity of Src family kinases during the initiation of prostate cancer. Proc Natl Acad Sci USA. 2011; 108: 6579–84. [PubMed Abstract] [PubMed CentralFull Text].
  • Demetrick DJ, Herlyn D, Tretiak M, Creasey D, Clevers H, Donoso LA et al. ME491 melanoma-associated glycoprotein family: antigenic identity of ME491, NKI/C-3, neuroglandular antigen (NGA), and CD63 proteins. J Natl Cancer Inst. 1992; 84: 422–9. [PubMed Abstract].
  • Luftig M, Prinarakis E, Yasui T, Tsichritzis T, Cahir-McFarland E, Inoue J et al. Epstein-Barr virus latent membrane protein 1 activation of NF-kappaB through IRAK1 and TRAF6. Proc Natl Acad Sci USA. 2003; 100: 15595–600. [PubMed Abstract] [PubMed CentralFull Text].
  • Albrethsen J, Knol JC, Piersma SR, Pham TV, de Wit M, Mongera S et al. Subnuclear proteomics in colorectal cancer: identification of proteins enriched in the nuclear matrix fraction and regulation in adenoma to carcinoma progression. Mol Cell Proteomics. 2010; 9: 988–1005. [PubMed Abstract] [PubMed CentralFull Text].
  • Piersma SR, Fiedler U, Span S, Lingnau A, Pham TV, Hoffmann S et al. Workflow comparison for label-free, quantitative secretome proteomics for cancer biomarker discovery: method evaluation, differential analysis, and verification in serum. J Proteome Res. 2010; 9: 1913–22. [PubMed Abstract].
  • Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol. 2008; 26: 1367–72. [PubMed Abstract].
  • Rink J, Ghigo E, Kalaidzidis Y, Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell. 2005; 122: 735–49. [PubMed Abstract].
  • Lebrand C, Corti M, Goodson H, Cosson P, Cavalli V, Mayran N et al. Late endosome motility depends on lipids via the small GTPase Rab7. EMBO J. 2002; 21: 1289–300. [PubMed Abstract] [PubMed CentralFull Text].
  • Aga M, Bentz GL, Raffa S, Torrisi MR, Kondo S, Wakisaka N et al. Exosomal HIF1α supports invasive potential of nasopharyngeal carcinoma-associated LMP1-positive exosomes. Oncogene. 2014; 33: 4613–22. [PubMed Abstract] [PubMed CentralFull Text].
  • Muralidharan-Chari V, Clancy J, Plou C, Romao M, Chavrier P, Raposo G et al. ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Curr Biol. 2009; 19: 1875–85. [PubMed Abstract] [PubMed CentralFull Text].
  • Ben-Neriah Y, Karin M. Inflammation meets cancer, with NF-κB as the matchmaker. Nat Immunol. 2011; 12: 715–23. [PubMed Abstract].
  • Le Clorennec C, Ouk T-S, Youlyouz-Marfak I, Panteix S, Martin C-C, Rastelli J et al. Molecular basis of cytotoxicity of Epstein-Barr virus (EBV) latent membrane protein 1 (LMP1) in EBV latency III B cells: LMP1 induces type II ligand-independent autoactivation of CD95/Fas with caspase 8-mediated apoptosis. J Virol. 2008; 82: 6721–33. [PubMed Abstract] [PubMed CentralFull Text].
  • Devergne O, Hatzivassiliou E, Izumi KM, Kaye KM, Kleijnen MF, Kieff E et al. Association of TRAF1, TRAF2, and TRAF3 with an Epstein-Barr virus LMP1 domain important for B-lymphocyte transformation: role in NF-kappaB activation. Mol Cell Biol. 1996; 16: 7098–108. [PubMed Abstract] [PubMed CentralFull Text].
  • Dukers DF, Meij P, Vervoort MB, Vos W, Scheper RJ, Meijer CJ et al. Direct immunosuppressive effects of EBV-encoded latent membrane protein 1. J Immunol. 2000; 165: 663–70. [PubMed Abstract].
  • Higuchi M, Izumi KM, Kieff E. Epstein-Barr virus latent-infection membrane proteins are palmitoylated and raft-associated: protein 1 binds to the cytoskeleton through TNF receptor cytoplasmic factors. Proc Natl Acad Sci USA. 2001; 98: 4675–80. [PubMed Abstract] [PubMed CentralFull Text].
  • Palacios F, Tushir JS, Fujita Y, D'Souza-Schorey C. Lysosomal targeting of E-cadherin: a unique mechanism for the down-regulation of cell-cell adhesion during epithelial to mesenchymal transitions. Mol Cell Biol. 2005; 25: 389–402. [PubMed Abstract] [PubMed CentralFull Text].
  • Roberts R, Barbieri M, Pryse K, Chua M, Morisaki J, Stahl P. Endosome fusion in living cells overexpressing GFP-rab5. J Cell Sci. 1999; 112: 3667–75. [PubMed Abstract].
  • Sato I, Obata Y, Kasahara K, Nakayama Y, Fukumoto Y, Yamasaki T et al. Differential trafficking of Src, Lyn, Yes and Fyn is specified by the state of palmitoylation in the SH4 domain. J Cell Sci. 2009; 122: 965–75. [PubMed Abstract].
  • Kasahara K, Nakayama Y, Kihara A, Matsuda D, Ikeda K, Kuga T et al. Rapid trafficking of c-Src, a non-palmitoylated Src-family kinase, between the plasma membrane and late endosomes/lysosomes. Exp Cell Res. 2007; 313: 2651–66. [PubMed Abstract].
  • Chairoungdua A, Smith DL, Pochard P, Hull M, Caplan MJ. Exosome release of beta-catenin: a novel mechanism that antagonizes Wnt signaling. J Cell Biol. 2010; 190: 1079–91. [PubMed Abstract] [PubMed CentralFull Text].
  • Bijlmakers M-J, Marsh M. The on-off story of protein palmitoylation. Trends Cell Biol. 2003; 13: 32–42. [PubMed Abstract].
  • Ren W, Jhala US, Du K. Proteomic analysis of protein palmitoylation in adipocytes. Adipocyte. 2013; 2: 17–28. [PubMed Abstract] [PubMed CentralFull Text].
  • Middeldorp JM, Pegtel DM. Multiple roles of LMP1 in Epstein-Barr virus induced immune escape. Semin Cancer Biol. 2008; 18: 388–96. [PubMed Abstract].
  • Pegtel DM. Oncogenic herpesviruses sending mixed signals. Proc Natl Acad Sci USA. 2013; 110: 12503–4. [PubMed Abstract] [PubMed CentralFull Text].
  • Meckes DG Jr., Gunawardena HP, Dekroon RM, Heaton PR, Edwards RH, Ozgur S. Modulation of B-cell exosome proteins by gamma herpesvirus infection. Proc Natl Acad Sci USA. 2013; 110(31): [PubMed CentralFull Text].
  • Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008; 319: 1244–7. [PubMed Abstract].
  • Williamson R, Thompson AJ, Abu M, Hye A, Usardi A, Lynham S et al. Isolation of detergent resistant microdomains from cultured neurons: detergent dependent alterations in protein composition. BMC Neurosci. 2010; 11: 120. [PubMed Abstract] [PubMed CentralFull Text].
  • Brown KD, Hostager BS, Bishop GA. Regulation of TRAF2 signaling by self-induced degradation. J Biol Chem. 2002; 277: 19433–8. [PubMed Abstract].
  • Murphy JE, Padilla BE, Hasdemir B, Cottrell GS, Bunnett NW. Endosomes: a legitimate platform for the signaling train. Proc Natl Acad Sci USA. 2009; 106: 17615–22. [PubMed Abstract] [PubMed CentralFull Text].
  • Liu HP, Wu CC, Chang YS. PRA1 promotes the intracellular trafficking and NF-kappaB signaling of EBV latent membrane protein 1. EMBO J. 2006; 25: 4120–30. [PubMed Abstract] [PubMed CentralFull Text].
  • Ceresa BP. Regulation of EGFR endocytic trafficking by rab proteins. Histol Histopathol. 2006; 21: 987–93. [PubMed Abstract].
  • Jia L, Chisari M, Maktabi MH, Sobieski C, Zhou H, Konopko AM et al. A mechanism regulating G protein-coupled receptor signaling that requires cycles of protein palmitoylation and depalmitoylation. J Biol Chem. 2014; 289: 6249–57. [PubMed Abstract] [PubMed CentralFull Text].
  • Mo M-L, Li M-R, Chen Z, Liu X-W, Sheng Q, Zhou H-M. Inhibition of the Wnt palmitoyltransferase porcupine suppresses cell growth and downregulates the Wnt/β-catenin pathway in gastric cancer. Oncol Lett. 2013; 5: 1719–23. [PubMed Abstract] [PubMed CentralFull Text].
  • Linder ME, Jennings BC. Mechanism and function of DHHC S-acyltransferases. Biochem Soc Trans. 2013; 41: 29–34. [PubMed Abstract].
  • Ménard L, Parker PJ, Kermorgant S. Receptor tyrosine kinase c-Met controls the cytoskeleton from different endosomes via different pathways. Nat Commun. 2014; 5: 3907.
  • Taelman VF, Dobrowolski R, Plouhinec JL, Fuentealba LC, Vorwald PP, Gumper I et al. Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell. 2010; 143: 1136–48. [PubMed Abstract] [PubMed CentralFull Text].
  • Irannejad R, Tomshine JC, Tomshine JR, Chevalier M, Mahoney JP, Steyaert J et al. Conformational biosensors reveal GPCR signalling from endosomes. Nature. 2013; 495: 534–8. [PubMed Abstract].
  • Luga V, Zhang L, Viloria-Petit AM, Ogunjimi AA, Inanlou MR, Chiu E et al. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell. 2012; 151: 1542–56. [PubMed Abstract].