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Original Research Articles

Nanoparticle analysis sheds budding insights into genetic drivers of extracellular vesicle biogenesis

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Article: 31295 | Received 12 Feb 2016, Accepted 07 Jun 2016, Published online: 13 Jul 2016

References

  • Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics. 2010; 73: 1907–20. [PubMed Abstract].
  • Théry C. Exosomes: secreted vesicles and intercellular communications. F1000 Biol Rep. 2011; 3: 15.
  • Bobrie A, Colombo M, Raposo G, Théry C. Exosome secretion: molecular mechanisms and roles in immune responses. Traffic. 2011; 12: 1659–68. [PubMed Abstract].
  • Graner MW, Alzate O, Dechkovskaia AM, Keene JD, Sampson JH, Mitchell DA, etal. Proteomic and immunologic analyses of brain tumor exosomes. FASEB J. 2009; 23: 1541–57. [PubMed Abstract] [PubMed CentralFull Text].
  • Théry C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002; 2: 569–79.
  • Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur BK, etal. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 2015; 17: 816–26. [PubMed Abstract].
  • Park JE, Tan HS, Datta A, Lai RC, Zhang H, Meng W, etal. Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes. Mol Cell Proteomics. 2010; 9: 1085–99. [PubMed Abstract] [PubMed CentralFull Text].
  • Rajendran L, Honsho M, Zahn TR, Keller P, Geiger KD, Verkade P, etal. Alzheimer's disease beta-amyloid peptides are released in association with exosomes. Proc Natl Acad Sci USA. 2006; 103: 11172–7. [PubMed Abstract] [PubMed CentralFull Text].
  • Pegtel DM, Peferoen L, Amor S. Extracellular vesicles as modulators of cell-to-cell communication in the healthy and diseased brain. Philos Trans R Soc Lond B Biol Sci. 2014; 369: 20130516
  • Meckes DG, 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].
  • Meckes DG, Raab-Traub N. Microvesicles and viral infection. J Virol. 2011; 85: 12844–54. [PubMed Abstract] [PubMed CentralFull Text].
  • Meckes DG. Exosomal communication goes viral. J Virol. 2015; 89: 5200–3. [PubMed Abstract] [PubMed CentralFull Text].
  • Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL, etal. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA. 2010; 107: 6328–33. [PubMed Abstract].
  • Rabinowits G, Gerçel-Taylor C, Day JM, Taylor DD, Kloecker GH. Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer. 2009; 10: 42–6. [PubMed Abstract].
  • Simpson RJ, Lim JW, Moritz RL, Mathivanan S. Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics. 2009; 6: 267–83. [PubMed Abstract].
  • Théry C. Cancer: diagnosis by extracellular vesicles. Nature. 2015; 523: 161–2.
  • Boukouris S, Mathivanan S. Exosomes in bodily fluids are a highly stable resource of disease biomarkers. Proteomics Clin Appl. 2015; 9: 358–67. [PubMed Abstract].
  • Taraboletti G, D'Ascenzo S, Borsotti P, Giavazzi R, Pavan A, Dolo V. Shedding of the matrix metalloproteinases MMP-2, MMP-9, and MT1-MMP as membrane vesicle-associated components by endothelial cells. Am J Pathol. 2002; 160: 673–80. [PubMed Abstract] [PubMed CentralFull Text].
  • Dolo V, D'Ascenzo S, Violini S, Pompucci L, Festuccia C, Ginestra A, etal. Matrix-degrading proteinases are shed in membrane vesicles by ovarian cancer cells in vivo and in vitro. Clin Exp Metastasis. 1999; 17: 131–40. [PubMed Abstract].
  • Ginestra A, La Placa MD, Saladino F, Cassarà D, Nagase H, Vittorelli ML. The amount and proteolytic content of vesicles shed by human cancer cell lines correlates with their in vitro invasiveness. Anticancer Res. 1998; 18: 3433–7. [PubMed Abstract].
  • Keerthikumar S, Gangoda L, Liem M, Fonseka P, Atukorala I, Ozcitti C, etal. Proteogenomic analysis reveals exosomes are more oncogenic than ectosomes. Oncotarget. 2015; 6: 15375–96. [PubMed Abstract] [PubMed CentralFull Text].
  • Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood. 1999; 94: 3791–9. [PubMed Abstract].
  • Gan X, Gould SJ. Identification of an inhibitory budding signal that blocks the release of HIV particles and exosome/microvesicle proteins. Mol Biol Cell. 2011; 22: 817–30. [PubMed Abstract] [PubMed CentralFull Text].
  • Salzer U, Hinterdorfer P, Hunger U, Borken C, Prohaska R. Ca(++)-dependent vesicle release from erythrocytes involves stomatin-specific lipid rafts, synexin (annexin VII), and sorcin. Blood. 2002; 99: 2569–77. [PubMed Abstract].
  • Muralidharan-Chari V, Clancy JW, Sedgwick A, D'Souza-Schorey C. Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci. 2010; 123: 1603–11. [PubMed Abstract] [PubMed CentralFull Text].
  • Masi G, Mercati D, Vannuccini E, Paccagnini E, Riparbelli MG, Lupetti P, etal. p66Shc regulates vesicle-mediated secretion in mast cells by affecting F-actin dynamics. J Leukoc Biol. 2014; 95: 285–92. [PubMed Abstract].
  • Muralidharan-Chari V, Clancy J, Plou C, Romao M, Chavrier P, Raposo G, etal. ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Curr Biol. 2009; 19: 1875–85. [PubMed Abstract] [PubMed CentralFull Text].
  • Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell. 1983; 33: 967–78. [PubMed Abstract].
  • Pan BT, Teng K, Wu C, Adam M, Johnstone RM. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol. 1985; 101: 942–8. [PubMed Abstract].
  • Futter CE, Pearse A, Hewlett LJ, Hopkins CR. Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J Cell Biol. 1996; 132: 1011–23. [PubMed Abstract].
  • Prag G, Watson H, Kim YC, Beach BM, Ghirlando R, Hummer G, etal. The Vps27/Hse1 complex is a GAT domain-based scaffold for ubiquitin-dependent sorting. Dev Cell. 2007; 12: 973–86. [PubMed Abstract] [PubMed CentralFull Text].
  • Hurley JH. ESCRT complexes and the biogenesis of multivesicular bodies. Curr Opin Cell Biol. 2008; 20: 4–11. [PubMed Abstract] [PubMed CentralFull Text].
  • Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, etal. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol. 2012; 14: 677–85. [PubMed Abstract].
  • Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, etal. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008; 319: 1244–7. [PubMed Abstract].
  • Colombo M, Moita C, van Niel G, Kowal J, Vigneron J, Benaroch P, etal. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J Cell Sci. 2013; 126: 5553–65. [PubMed Abstract].
  • Escola JM, Kleijmeer MJ, Stoorvogel W, Griffith JM, Yoshie O, Geuze HJ. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem. 1998; 273: 20121–7. [PubMed Abstract].
  • van Niel G, Charrin S, Simoes S, Romao M, Rochin L, Saftig P, etal. The tetraspanin CD63 regulates ESCRT-independent and-dependent endosomal sorting during melanogenesis. Dev Cell. 2011; 21: 708–21. [PubMed Abstract] [PubMed CentralFull Text].
  • Andreu Z, Yáñez-Mó M. Tetraspanins in extracellular vesicle formation and function. Front Immunol. 2014; 5: 442. [PubMed Abstract] [PubMed CentralFull Text].
  • Perez-Hernandez D, Gutiérrez-Vázquez C, Jorge I, López-Martín S, Ursa A, Sánchez-Madrid F, etal. The intracellular interactome of tetraspanin-enriched microdomains reveals their function as sorting machineries toward exosomes. J Biol Chem. 2013; 288: 11649–61. [PubMed Abstract] [PubMed CentralFull Text].
  • Colombo M, Raposo G, Théry C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014; 30: 255–89. [PubMed Abstract].
  • Salaün C, Gould GW, Chamberlain LH. Lipid raft association of SNARE proteins regulates exocytosis in PC12 cells. J Biol Chem. 2005; 280: 19449–53.
  • Hyenne V, Apaydin A, Rodriguez D, Spiegelhalter C, Hoff-Yoessle S, Diem M, etal. RAL-1 controls multivesicular body biogenesis and exosome secretion. J Cell Biol. 2015; 211: 27–37. [PubMed Abstract] [PubMed CentralFull Text].
  • Savina A, Fader CM, Damiani MT, Colombo MI. Rab11 promotes docking and fusion of multivesicular bodies in a calcium-dependent manner. Traffic. 2005; 6: 131–43. [PubMed Abstract].
  • Hsu C, Morohashi Y, Yoshimura S, Manrique-Hoyos N, Jung S, Lauterbach MA, etal. Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J Cell Biol. 2010; 189: 223–32. [PubMed Abstract] [PubMed CentralFull Text].
  • Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, etal. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol. 2010; 12: 19–30; sup pp 1–13. [PubMed Abstract].
  • Gillingham AK, Sinka R, Torres IL, Lilley KS, Munro S. Toward a comprehensive map of the effectors of rab GTPases. Dev Cell. 2014; 31: 358–73. [PubMed Abstract] [PubMed CentralFull Text].
  • Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol. 2009; 10: 513–25. [PubMed Abstract].
  • Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013; 200: 373–83. [PubMed Abstract] [PubMed CentralFull Text].
  • Shankavaram UT, Varma S, Kane D, Sunshine M, Chary KK, Reinhold WC, etal. CellMiner: a relational database and query tool for the NCI-60 cancer cell lines. BMC Genomics. 2009; 10: 277. [PubMed Abstract] [PubMed CentralFull Text].
  • Reinhold WC, Sunshine M, Liu H, Varma S, Kohn KW, Morris J, etal. CellMiner: a web-based suite of genomic and pharmacologic tools to explore transcript and drug patterns in the NCI-60 cell line set. Cancer Res. 2012; 72: 3499–511. [PubMed Abstract] [PubMed CentralFull Text].
  • Genomics & Bioinformatics Group L, CCR, NCI. CellMiner. 2009. [Database Version:1.6.1] [Cited 2015 Nov 23]. Available from: http://discover.nci.nih.gov/cellminer/analysis.do.
  • Simpson RJ, Kalra H, Mathivanan S. ExoCarta as a resource for exosomal research. J Extracell Vesicles. 2012; 1: 18374.
  • Kalra H, Simpson RJ, Ji H, Aikawa E, Altevogt P, Askenase P, etal. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol. 2012; 10: e1001450. [PubMed Abstract] [PubMed CentralFull Text].
  • Benito-Martin A, Peinado H. FunRich proteomics software analysis, let the fun begin!. Proteomics. 2015; 15: 2555–6. [PubMed Abstract].
  • Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013; 8: 2281–308. [PubMed Abstract] [PubMed CentralFull Text].
  • Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, etal. RNA-guided human genome engineering via Cas9. Science. 2013; 339: 823–6. [PubMed Abstract] [PubMed CentralFull Text].
  • Rider MA, Hurwitz SN, Meckes DG. ExtraPEG: a polyethylene glycol-based method for enrichment of extracellular vesicles. Sci Rep. 2016; 6: 23978. [PubMed Abstract] [PubMed CentralFull Text].
  • Pathan M, Keerthikumar S, Ang CS, Gangoda L, Quek CY, Williamson NA, etal. FunRich: an open access standalone functional enrichment and interaction network analysis tool. Proteomics. 2015; 15: 2597–601. [PubMed Abstract].
  • Keerthikumar S, Chisanga D, Ariyaratne D, Al Saffar H, Anand S, Zhao K, etal. ExoCarta: a web-based compendium of exosomal cargo. J Mol Biol. 2015; 428:688–92
  • Mathivanan S, Simpson RJ. ExoCarta: a compendium of exosomal proteins and RNA. Proteomics. 2009; 9: 4997–5000. [PubMed Abstract].
  • Mathivanan S, Fahner CJ, Reid GE, Simpson RJ. ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic Acids Res. 2012; 40: D1241–4. [PubMed Abstract].
  • Sung BH, Ketova T, Hoshino D, Zijlstra A, Weaver AM. Directional cell movement through tissues is controlled by exosome secretion. Nat Commun. 2015; 6: 7164. [PubMed Abstract] [PubMed CentralFull Text].
  • Tauro BJ, Greening DW, Mathias RA, Ji H, Mathivanan S, Scott AM, etal. Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods. 2012; 56: 293–304. [PubMed Abstract].
  • Van Deun J, Mestdagh P, Sormunen R, Cocquyt V, Vermaelen K, Vandesompele J, etal. The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J Extracell Vesicles. 2014; 3: 24858. http://dx.doi.org/10.3402/jev.v3.24858.
  • Ji H, Greening DW, Barnes TW, Lim JW, Tauro BJ, Rai A, etal. Proteome profiling of exosomes derived from human primary and metastatic colorectal cancer cells reveal differential expression of key metastatic factors and signal transduction components. Proteomics. 2013; 13: 1672–86. [PubMed Abstract].
  • Page-McCaw A, Ewald AJ, Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol. 2007; 8: 221–33. [PubMed Abstract] [PubMed CentralFull Text].
  • Kowal J, Arras G, Colombo M, Jouve M, Morath JP, Primdal-Bengtson B, etal. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci USA. 2016; 113: E968–77. [PubMed Abstract].
  • Savina A, Vidal M, Colombo MI. The exosome pathway in K562 cells is regulated by Rab11. J Cell Sci. 2002; 115: 2505–15. [PubMed Abstract].
  • Théry C, Boussac M, Véron P, Ricciardi-Castagnoli P, Raposo G, Garin J, etal. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol. 2001; 166: 7309–18.
  • Greening DW, Xu R, Ji H, Tauro BJ, Simpson RJ. A protocol for exosome isolation and characterization: evaluation of ultracentrifugation, density-gradient separation, and immunoaffinity capture methods. Methods Mol Biol. 2015; 1295: 179–209. [PubMed Abstract].
  • Pols MS, Klumperman J. Trafficking and function of the tetraspanin CD63. Exp Cell Res. 2009; 315: 1584–92. [PubMed Abstract].
  • Asensio CS, Sirkis DW, Maas JW, Egami K, To TL, Brodsky FM, etal. Self-assembly of VPS41 promotes sorting required for biogenesis of the regulated secretory pathway. Dev Cell. 2013; 27: 425–37. [PubMed Abstract] [PubMed CentralFull Text].
  • Lundmark R, Carlsson SR. SNX9 – a prelude to vesicle release. J Cell Sci. 2009; 122(Pt 1): 5–11. [PubMed Abstract].
  • Pryor PR, Mullock BM, Bright NA, Lindsay MR, Gray SR, Richardson SC, etal. Combinatorial SNARE complexes with VAMP7 or VAMP8 define different late endocytic fusion events. EMBO Rep. 2004; 5: 590–5. [PubMed Abstract] [PubMed CentralFull Text].
  • Wong M, Munro S. Membrane trafficking. The specificity of vesicle traffic to the Golgi is encoded in the golgin coiled-coil proteins. Science. 2014; 346: 1256898. [PubMed Abstract] [PubMed CentralFull Text].
  • Takahashi K, Mitsui K, Yamanaka S. Role of ERas in promoting tumour-like properties in mouse embryonic stem cells. Nature. 2003; 423: 541–5. [PubMed Abstract].
  • Matsumoto K, Asano T, Endo T. Novel small GTPase M-Ras participates in reorganization of actin cytoskeleton. Oncogene. 1997; 15: 2409–17. [PubMed Abstract].
  • Chavrier P, Goud B. The role of ARF and Rab GTPases in membrane transport. Curr Opin Cell Biol. 1999; 11: 466–75. [PubMed Abstract].
  • Donaldson JG, Jackson CL. ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat Rev Mol Cell Biol. 2011; 12: 362–75. [PubMed Abstract] [PubMed CentralFull Text].
  • Lai C, Xie C, Shim H, Chandran J, Howell BW, Cai H. Regulation of endosomal motility and degradation by amyotrophic lateral sclerosis 2/alsin. Mol Brain. 2009; 2: 23. [PubMed Abstract] [PubMed CentralFull Text].
  • Liégeois S, Benedetto A, Garnier JM, Schwab Y, Labouesse M. The V0-ATPase mediates apical secretion of exosomes containing Hedgehog-related proteins in Caenorhabditis elegans . J Cell Biol. 2006; 173: 949–61.
  • Cullen PJ. Endosomal sorting and signalling: an emerging role for sorting nexins. Nat Rev Mol Cell Biol. 2008; 9: 574–82. [PubMed Abstract].
  • Abdul-Hammed M, Breiden B, Adebayo MA, Babalola JO, Schwarzmann G, Sandhoff K. Role of endosomal membrane lipids and NPC2 in cholesterol transfer and membrane fusion. J Lipid Res. 2010; 51: 1747–60. [PubMed Abstract] [PubMed CentralFull Text].
  • Gallala HD, Breiden B, Sandhoff K. Regulation of the NPC2 protein-mediated cholesterol trafficking by membrane lipids. J Neurochem. 2011; 116: 702–7. [PubMed Abstract].
  • Carvelli L, Libin Y, Morales CR. Prosaposin: a protein with differential sorting and multiple functions. Histol Histopathol. 2015; 30: 647–60. [PubMed Abstract].
  • Silva J, Garcia V, Rodriguez M, Compte M, Cisneros E, Veguillas P, etal. Analysis of exosome release and its prognostic value in human colorectal cancer. Genes Chromosomes Cancer. 2012; 51: 409–18. [PubMed Abstract].
  • Hutagalung AH, Novick PJ. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev. 2011; 91: 119–49. [PubMed Abstract] [PubMed CentralFull Text].
  • Li Y, Meng X, Feng H, Zhang G, Liu C, Li P. Over-expression of the RAB5 gene in human lung adenocarcinoma cells with high metastatic potential. Chin Med Sci J. 1999; 14: 96–101. [PubMed Abstract].
  • Fukui K, Tamura S, Wada A, Kamada Y, Igura T, Kiso S, etal. Expression of Rab5a in hepatocellular carcinoma: possible involvement in epidermal growth factor signaling. Hepatol Res. 2007; 37: 957–65. [PubMed Abstract].
  • Li W, Hu Y, Jiang T, Han Y, Han G, Chen J, etal. Rab27A regulates exosome secretion from lung adenocarcinoma cells A549: involvement of EPI64. APMIS. 2014; 122: 1080–7. [PubMed Abstract].
  • Yang X, Claas C, Kraeft SK, Chen LB, Wang Z, Kreidberg JA, etal. Palmitoylation of tetraspanin proteins: modulation of CD151 lateral interactions, subcellular distribution, and integrin-dependent cell morphology. Mol Biol Cell. 2002; 13: 767–81. [PubMed Abstract] [PubMed CentralFull Text].
  • Hemler ME. Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol. 2005; 6: 801–11. [PubMed Abstract].
  • Zhijun X, Shulan Z, Zhuo Z. Expression and significance of the protein and mRNA of metastasis suppressor gene ME491/CD63 and integrin alpha5 in ovarian cancer tissues. Eur J Gynaecol Oncol. 2007; 28: 179–83. [PubMed Abstract].
  • Kwon MS, Shin SH, Yim SH, Lee KY, Kang HM, Kim TM, etal. CD63 as a biomarker for predicting the clinical outcomes in adenocarcinoma of lung. Lung Cancer. 2007; 57: 46–53. [PubMed Abstract].
  • Sauer G, Kurzeder C, Grundmann R, Kreienberg R, Zeillinger R, Deissler H. Expression of tetraspanin adaptor proteins below defined threshold values is associated with in vitro invasiveness of mammary carcinoma cells. Oncol Rep. 2003; 10: 405–10. [PubMed Abstract].
  • Sordat I, Decraene C, Silvestre T, Petermann O, Auffray C, Piétu G, etal. Complementary DNA arrays identify CD63 tetraspanin and alpha3 integrin chain as differentially expressed in low and high metastatic human colon carcinoma cells. Lab Invest. 2002; 82: 1715–24. [PubMed Abstract].
  • Verweij FJ, van Eijndhoven MA, Hopmans ES, Vendrig T, Wurdinger T, Cahir-McFarland E, etal. LMP1 association with CD63 in endosomes and secretion via exosomes limits constitutive NF-κB activation. EMBO J. 2011; 30: 2115–29. [PubMed Abstract] [PubMed CentralFull Text].
  • Petersen SH, Odintsova E, Haigh TA, Rickinson AB, Taylor GS, Berditchevski F. The role of tetraspanin CD63 in antigen presentation via MHC class II. Eur J Immunol. 2011; 41: 2556–61. [PubMed Abstract].