1932

Abstract

Antigen cross-presentation is an adaptation of the cellular process of loading MHC-I molecules with endogenous peptides during their biosynthesis within the endoplasmic reticulum. Cross-presented peptides derive from internalized proteins, microbial pathogens, and transformed or dying cells. The physical separation of internalized cargo from the endoplasmic reticulum, where the machinery for assembling peptide–MHC-I complexes resides, poses a challenge. To solve this problem, deliberate rewiring of organelle communication within cells is necessary to prepare for cross-presentation, and different endocytic receptors and vesicular traffic patterns customize the emergent cross-presentation compartment to the nature of the peptide source. Three distinct pathways of vesicular traffic converge to form the ideal cross-presentation compartment, each regulated differently to supply a unique component that enables cross-presentation of a diverse repertoire of peptides. Delivery of centerpiece MHC-I molecules is the critical step regulated by microbe-sensitive Toll-like receptors. Defining the subcellular sources of MHC-I and identifying sites of peptide loading during cross-presentation remain key challenges.

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2018-04-26
2024-03-29
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Literature Cited

  1. Bjorkman PJ. 1.  1997. MHC restriction in three dimensions: a view of T cell receptor/ligand interactions. Cell 89:167–70 [Google Scholar]
  2. Blum JS, Wearsch PA, Cresswell P. 2.  2013. Pathways of antigen processing. Annu. Rev. Immunol. 31:443–73 [Google Scholar]
  3. Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC. 3.  1987. Structure of the human class I histocompatibility antigen, HLA-A2. Nature 329:506–12 [Google Scholar]
  4. Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC. 4.  1987. The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 329:512–18 [Google Scholar]
  5. Schwartz RH. 5.  1992. Costimulation of T lymphocytes: the role of CD28, CTLA-4, and B7/BB1 in interleukin-2 production and immunotherapy. Cell 71:1065–68 [Google Scholar]
  6. Mueller DL, Jenkins MK, Schwartz RH. 6.  1989. Clonal expansion versus functional clonal inactivation: a costimulatory signalling pathway determines the outcome of T cell antigen receptor occupancy. Annu. Rev. Immunol. 7:445–80 [Google Scholar]
  7. Liu Y, Janeway CA Jr. 7.  1991. Microbial induction of co-stimulatory activity for CD4 T-cell growth. Int. Immunol. 3:323–32 [Google Scholar]
  8. Liu Y, Janeway CA Jr. 8.  1992. Cells that present both specific ligand and costimulatory activity are the most efficient inducers of clonal expansion of normal CD4 T cells. PNAS 89:3845–49 [Google Scholar]
  9. Medzhitov R, Preston-Hurlburt P, Janeway CA Jr. 9.  1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394–97 [Google Scholar]
  10. Janeway CA Jr. 10.  1989. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 54:Part 11–13 [Google Scholar]
  11. Takeuchi O, Akira S. 11.  2010. Pattern recognition receptors and inflammation. Cell 140:805–20 [Google Scholar]
  12. Perreault C. 12.  2010. The origin and role of MHC class I-associated self-peptides. Prog. Mol. Biol. Transl. Sci. 92:41–60 [Google Scholar]
  13. Alloatti A, Kotsias F, Magalhaes JG, Amigorena S. 13.  2016. Dendritic cell maturation and cross-presentation: Timing matters! Immunol. . Rev 272:97–108 [Google Scholar]
  14. Blander JM. 14.  2016. The comings and goings of MHC class I molecules herald a new dawn in cross-presentation. Immunol. Rev. 272:65–79 [Google Scholar]
  15. Cruz FM, Colbert JD, Merino E, Kriegsman BA, Rock KL. 15.  2017. The biology and underlying mechanisms of cross-presentation of exogenous antigens on MHC-I molecules. Annu. Rev. Immunol. 35:149–76 [Google Scholar]
  16. Grotzke JE, Sengupta D, Lu Q, Cresswell P. 16.  2017. The ongoing saga of the mechanism(s) of MHC class I-restricted cross-presentation. Curr. Opin. Immunol. 46:89–96 [Google Scholar]
  17. Gutierrez-Martinez E, Planes R, Anselmi G, Reynolds M, Menezes S. 17.  et al. 2015. Cross-presentation of cell-associated antigens by MHC class I in dendritic cell subsets. Front. Immunol. 6:363 [Google Scholar]
  18. van Endert P. 18.  2016. Intracellular recycling and cross-presentation by MHC class I molecules. Immunol. Rev. 272:80–96 [Google Scholar]
  19. Delany I, Rappuoli R, De Gregorio E. 19.  2014. Vaccines for the 21st century. EMBO Mol. Med. 6:708–20 [Google Scholar]
  20. McMichael A, Picker LJ, Moore JP, Burton DR. 20.  2013. Another HIV vaccine failure: where to next?. Nat. Med. 19:1576–77 [Google Scholar]
  21. Gilbert SC. 21.  2012. T-cell-inducing vaccines—what's the future. Immunology 135:19–26 [Google Scholar]
  22. Stoll-Keller F, Barth H, Fafi-Kremer S, Zeisel MB, Baumert TF. 22.  2009. Development of hepatitis C virus vaccines: challenges and progress. Expert Rev. Vaccines 8:333–45 [Google Scholar]
  23. Fehres CM, Unger WW, Garcia-Vallejo JJ, van Kooyk Y. 23.  2014. Understanding the biology of antigen cross-presentation for the design of vaccines against cancer. Front. Immunol. 5:149 [Google Scholar]
  24. Savina A, Amigorena S. 24.  2007. Phagocytosis and antigen presentation in dendritic cells. Immunol. Rev. 219:143–56 [Google Scholar]
  25. Briseno CG, Haldar M, Kretzer NM, Wu X, Theisen DJ. 25.  et al. 2016. Distinct transcriptional programs control cross-priming in classical and monocyte-derived dendritic cells. Cell Rep 15:2462–74 [Google Scholar]
  26. Segura E, Villadangos JA. 26.  2009. Antigen presentation by dendritic cells in vivo. Curr. Opin. Immunol. 21:105–10 [Google Scholar]
  27. Igyarto BZ, Kaplan DH. 27.  2013. Antigen presentation by Langerhans cells. Curr. Opin. Immunol. 25:115–19 [Google Scholar]
  28. Poulin LF, Reyal Y, Uronen-Hansson H, Schraml BU, Sancho D. 28.  et al. 2012. DNGR-1 is a specific and universal marker of mouse and human Batf3-dependent dendritic cells in lymphoid and nonlymphoid tissues. Blood 119:6052–62 [Google Scholar]
  29. Bachem A, Hartung E, Guttler S, Mora A, Zhou X. 29.  et al. 2012. Expression of XCR1 characterizes the Batf3-dependent lineage of dendritic cells capable of antigen cross-presentation. Front. Immunol. 3:214 [Google Scholar]
  30. Segura E, Amigorena S. 30.  2014. Cross-presentation by human dendritic cell subsets. Immunol. Lett. 158:73–78 [Google Scholar]
  31. van der Aa E, van Montfoort N, Woltman AM. 31.  2015. BDCA3+CLEC9A+ human dendritic cell function and development. Semin. Cell Dev. Biol. 41:39–48 [Google Scholar]
  32. Tel J, Schreibelt G, Sittig SP, Mathan TS, Buschow SI. 32.  et al. 2013. Human plasmacytoid dendritic cells efficiently cross-present exogenous Ags to CD8+ T cells despite lower Ag uptake than myeloid dendritic cell subsets. Blood 121:459–67 [Google Scholar]
  33. Mangan MS, Vega-Ramos J, Joeckel LT, Mitchell AJ, Rizzitelli A. 33.  et al. 2017. Serpinb9 is a marker of antigen cross-presenting dendritic cells. Mol. Immunol. 82:50–56 [Google Scholar]
  34. Brewitz A, Eickhoff S, Dahling S, Quast T, Bedoui S. 34.  et al. 2017. CD8+ T cells orchestrate pDC-XCR1+ dendritic cell spatial and functional cooperativity to optimize priming. Immunity 46:205–19 [Google Scholar]
  35. Rogers GL, Shirley JL, Zolotukhin I, Kumar SRP, Sherman A. 35.  et al. 2017. Plasmacytoid and conventional dendritic cells cooperate in crosspriming AAV capsid-specific CD8+ T cells. Blood 129:3184–95 [Google Scholar]
  36. Ebrahimkhani MR, Mohar I, Crispe IN. 36.  2011. Cross-presentation of antigen by diverse subsets of murine liver cells. Hepatology 54:1379–87 [Google Scholar]
  37. Fukui K, Yang Q, Cao Y, Takahashi N, Hatakeyama H. 37.  et al. 2005. The HNF-1 target collectrin controls insulin exocytosis by SNARE complex formation. Cell Metab 2:373–84 [Google Scholar]
  38. Dolina JS, Cechova S, Rudy CK, Sung SJ, Tang WW. 38.  et al. 2017. Cross-presentation of soluble and cell-associated antigen by murine hepatocytes is enhanced by collectrin expression. J. Immunol. 198:2341–51 [Google Scholar]
  39. Akpinar P, Kuwajima S, Krutzfeldt J, Stoffel M. 39.  2005. Tmem27: a cleaved and shed plasma membrane protein that stimulates pancreatic beta cell proliferation. Cell Metab 2:385–97 [Google Scholar]
  40. Helft J, Bottcher J, Chakravarty P, Zelenay S, Huotari J. 40.  et al. 2015. GM-CSF mouse bone marrow cultures comprise a heterogeneous population of CD11c+MHCII+ macrophages and dendritic cells. Immunity 42:1197–211 [Google Scholar]
  41. Shortman K, Naik SH. 41.  2007. Steady-state and inflammatory dendritic-cell development. Nat. Rev. Immunol. 7:19–30 [Google Scholar]
  42. Cheong C, Matos I, Choi JH, Dandamudi DB, Shrestha E. 42.  et al. 2010. Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209+ dendritic cells for immune T cell areas. Cell 143:416–29 [Google Scholar]
  43. Rapoport TA, Li L, Park E. 43.  2017. Structural and mechanistic insights into protein translocation. Annu. Rev. Cell Dev. Biol. 33:369–90 [Google Scholar]
  44. Cresswell P, Ackerman AL, Giodini A, Peaper DR, Wearsch PA. 44.  2005. Mechanisms of MHC class I-restricted antigen processing and cross-presentation. Immunol. Rev. 207:145–57 [Google Scholar]
  45. Paulsson K, Wang P. 45.  2003. Chaperones and folding of MHC class I molecules in the endoplasmic reticulum. Biochim. Biophys. Acta 1641:1–12 [Google Scholar]
  46. Hulpke S, Tampe R. 46.  2013. The MHC I loading complex: a multitasking machinery in adaptive immunity. Trends Biochem. Sci. 38:412–20 [Google Scholar]
  47. Neefjes J, Jongsma ML, Paul P, Bakke O. 47.  2011. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat. Rev. Immunol. 11:823–36 [Google Scholar]
  48. Spiliotis ET, Manley H, Osorio M, Zuniga MC, Edidin M. 48.  2000. Selective export of MHC class I molecules from the ER after their dissociation from TAP. Immunity 13:841–51 [Google Scholar]
  49. Paquet ME, Cohen-Doyle M, Shore GC, Williams DB. 49.  2004. Bap29/31 influences the intracellular traffic of MHC class I molecules. J. Immunol. 172:7548–55 [Google Scholar]
  50. Abe F, Van Prooyen N, Ladasky JJ, Edidin M. 50.  2009. Interaction of Bap31 and MHC class I molecules and their traffic out of the endoplasmic reticulum. J. Immunol. 182:4776–83 [Google Scholar]
  51. Appenzeller-Herzog C, Hauri HP. 51.  2006. The ER-Golgi intermediate compartment (ERGIC): in search of its identity and function. J. Cell Sci. 119:2173–83 [Google Scholar]
  52. Springer S. 52.  2015. Transport and quality control of MHC class I molecules in the early secretory pathway. Curr. Opin. Immunol. 34:83–90 [Google Scholar]
  53. Donaldson JG, Williams DB. 53.  2009. Intracellular assembly and trafficking of MHC class I molecules. Traffic 10:1745–52 [Google Scholar]
  54. Raposo G, van Santen HM, Leijendekker R, Geuze HJ, Ploegh HL. 54.  1995. Misfolded major histocompatibility complex class I molecules accumulate in an expanded ER-Golgi intermediate compartment. J. Cell Biol. 131:1403–19 [Google Scholar]
  55. Van Hateren A, James E, Bailey A, Phillips A, Dalchau N, Elliott T. 55.  2010. The cell biology of major histocompatibility complex class I assembly: towards a molecular understanding. Tissue Antigens 76:259–75 [Google Scholar]
  56. Cebrian I, Visentin G, Blanchard N, Jouve M, Bobard A. 56.  et al. 2011. Sec22b regulates phagosomal maturation and antigen crosspresentation by dendritic cells. Cell 147:1355–68 [Google Scholar]
  57. Wearsch PA, Cresswell P. 57.  2008. The quality control of MHC class I peptide loading. Curr. Opin. Cell Biol. 20:624–31 [Google Scholar]
  58. Ghanem E, Fritzsche S, Al-Balushi M, Hashem J, Ghuneim L. 58.  et al. 2010. The transporter associated with antigen processing (TAP) is active in a post-ER compartment. J. Cell Sci. 123:4271–79 [Google Scholar]
  59. Kuhns ST, Pease LR. 59.  1998. A region of conformational variability outside the peptide-binding site of a class I MHC molecule. J. Immunol. 161:6745–50 [Google Scholar]
  60. Nair-Gupta P, Baccarini A, Tung N, Seyffer F, Florey O. 60.  et al. 2014. TLR signals induce phagosomal MHC-I delivery from the endosomal recycling compartment to allow cross-presentation. Cell 158:506–21 [Google Scholar]
  61. Neefjes JJ, Stollorz V, Peters PJ, Geuze HJ, Ploegh HL. 61.  1990. The biosynthetic pathway of MHC class II but not class I molecules intersects the endocytic route. Cell 61:171–83 [Google Scholar]
  62. Kirchhausen T, Owen D, Harrison SC. 62.  2014. Molecular structure, function, and dynamics of clathrin-mediated membrane traffic. Cold Spring Harb. Perspect. Biol. 6:a016725 [Google Scholar]
  63. Sandvig K, Torgersen ML, Raa HA, van Deurs B. 63.  2008. Clathrin-independent endocytosis: from nonexisting to an extreme degree of complexity. Histochem. Cell Biol. 129:267–76 [Google Scholar]
  64. Mayor S, Parton RG, Donaldson JG. 64.  2014. Clathrin-independent pathways of endocytosis. Cold Spring Harb. Perspect. Biol. 6:a016758 [Google Scholar]
  65. Naslavsky N, Weigert R, Donaldson JG. 65.  2004. Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol. Biol. Cell 15:3542–52 [Google Scholar]
  66. Radhakrishna H, Donaldson JG. 66.  1997. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 139:49–61 [Google Scholar]
  67. Jovic M, Sharma M, Rahajeng J, Caplan S. 67.  2010. The early endosome: a busy sorting station for proteins at the crossroads. Histol. Histopathol. 25:99–112 [Google Scholar]
  68. Naslavsky N, Weigert R, Donaldson JG. 68.  2003. Convergence of non-clathrin- and clathrin-derived endosomes involves Arf6 inactivation and changes in phosphoinositides. Mol. Biol. Cell 14:417–31 [Google Scholar]
  69. Lizee G, Basha G, Tiong J, Julien JP, Tian M. 69.  et al. 2003. Control of dendritic cell cross-presentation by the major histocompatibility complex class I cytoplasmic domain. Nat. Immunol. 4:1065–73 [Google Scholar]
  70. MacAry PA, Lindsay M, Scott MA, Craig JI, Luzio JP, Lehner PJ. 70.  2001. Mobilization of MHC class I molecules from late endosomes to the cell surface following activation of CD34-derived human Langerhans cells. PNAS 98:3982–87 [Google Scholar]
  71. Kleijmeer MJ, Escola JM, UytdeHaag FG, Jakobson E, Griffith JM. 71.  et al. 2001. Antigen loading of MHC class I molecules in the endocytic tract. Traffic 2:124–37 [Google Scholar]
  72. Hanson PI, Cashikar A. 72.  2012. Multivesicular body morphogenesis. Annu. Rev. Cell Dev. Biol. 28:337–62 [Google Scholar]
  73. Maxfield FR, McGraw TE. 73.  2004. Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5:121–32 [Google Scholar]
  74. Grant BD, Donaldson JG. 74.  2009. Pathways and mechanisms of endocytic recycling. Nat. Rev. Mol. Cell Biol. 10:597–608 [Google Scholar]
  75. Gruenberg J. 75.  2001. The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell Biol. 2:721–30 [Google Scholar]
  76. Hopkins CR. 76.  1983. Intracellular routing of transferrin and transferrin receptors in epidermoid carcinoma A431 cells. Cell 35:321–30 [Google Scholar]
  77. Yamashiro DJ, Tycko B, Fluss SR, Maxfield FR. 77.  1984. Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway. Cell 37:789–800 [Google Scholar]
  78. Ren M, Xu G, Zeng J, De Lemos-Chiarandini C, Adesnik M, Sabatini DD. 78.  1998. Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. PNAS 95:6187–92 [Google Scholar]
  79. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG. 79.  1996. Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135:913–24 [Google Scholar]
  80. Wilcke M, Johannes L, Galli T, Mayau V, Goud B, Salamero J. 80.  2000. Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-Golgi network. J. Cell Biol. 151:1207–20 [Google Scholar]
  81. Choudhury A, Sharma DK, Marks DL, Pagano RE. 81.  2004. Elevated endosomal cholesterol levels in Niemann-Pick cells inhibit rab4 and perturb membrane recycling. Mol. Biol. Cell 15:4500–11 [Google Scholar]
  82. van der Sluijs P, Hull M, Webster P, Male P, Goud B, Mellman I. 82.  1992. The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell 70:729–40 [Google Scholar]
  83. Daro E, van der Sluijs P, Galli T, Mellman I. 83.  1996. Rab4 and cellubrevin define different early endosome populations on the pathway of transferrin receptor recycling. PNAS 93:9559–64 [Google Scholar]
  84. Klinkert K, Echard A. 84.  2016. Rab35 GTPase: a central regulator of phosphoinositides and F-actin in endocytic recycling and beyond. Traffic 17:1063–77 [Google Scholar]
  85. Powelka AM, Sun J, Li J, Gao M, Shaw LM. 85.  et al. 2004. Stimulation-dependent recycling of integrin β1 regulated by ARF6 and Rab11. Traffic 5:20–36 [Google Scholar]
  86. Weigert R, Yeung AC, Li J, Donaldson JG. 86.  2004. Rab22a regulates the recycling of membrane proteins internalized independently of clathrin. Mol. Biol. Cell 15:3758–70 [Google Scholar]
  87. Caplan S, Naslavsky N, Hartnell LM, Lodge R, Polishchuk RS. 87.  et al. 2002. A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane. EMBO J 21:2557–67 [Google Scholar]
  88. Giridharan SS, Cai B, Vitale N, Naslavsky N, Caplan S. 88.  2013. Cooperation of MICAL-L1, syndapin2, and phosphatidic acid in tubular recycling endosome biogenesis. Mol. Biol. Cell 24:1776–90 S1–15 [Google Scholar]
  89. Sharma M, Giridharan SS, Rahajeng J, Naslavsky N, Caplan S. 89.  2009. MICAL-L1 links EHD1 to tubular recycling endosomes and regulates receptor recycling. Mol. Biol. Cell 20:5181–94 [Google Scholar]
  90. Maldonado-Baez L, Williamson C, Donaldson JG. 90.  2013. Clathrin-independent endocytosis: a cargo-centric view. Exp. Cell Res. 319:2759–69 [Google Scholar]
  91. Xie S, Bahl K, Reinecke JB, Hammond GR, Naslavsky N, Caplan S. 91.  2016. The endocytic recycling compartment maintains cargo segregation acquired upon exit from the sorting endosome. Mol. Biol. Cell 27:108–26 [Google Scholar]
  92. Naslavsky N, Caplan S. 92.  2011. EHD proteins: key conductors of endocytic transport. Trends Cell Biol 21:122–31 [Google Scholar]
  93. Xie S, Naslavsky N, Caplan S. 93.  2014. Diacylglycerol kinase alpha regulates tubular recycling endosome biogenesis and major histocompatibility complex class I recycling. J. Biol. Chem. 289:31914–26 [Google Scholar]
  94. Grant BD, Caplan S. 94.  2008. Mechanisms of EHD/RME-1 protein function in endocytic transport. Traffic 9:2043–52 [Google Scholar]
  95. Lin SX, Grant B, Hirsh D, Maxfield FR. 95.  2001. Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat. Cell Biol. 3:567–72 [Google Scholar]
  96. Cebrian I, Croce C, Guerrero NA, Blanchard N, Mayorga LS. 96.  2016. Rab22a controls MHC-I intracellular trafficking and antigen cross-presentation by dendritic cells. EMBO Rep 17:1753–65 [Google Scholar]
  97. Ackerman AL, Cresswell P. 97.  2003. Regulation of MHC class I transport in human dendritic cells and the dendritic-like cell line KG-1. J. Immunol. 170:4178–88 [Google Scholar]
  98. Compeer EB, Flinsenberg TW, Boon L, Hoekstra ME, Boes M. 98.  2014. Tubulation of endosomal structures in human dendritic cells by Toll-like receptor ligation and lymphocyte contact accompanies antigen cross-presentation. J. Biol. Chem. 289:520–28 [Google Scholar]
  99. Compeer EB, Boes M. 99.  2014. MICAL-L1-related and unrelated mechanisms underlying elongated tubular endosomal network (ETEN) in human dendritic cells. Commun. Integr. Biol. 7:e994969 [Google Scholar]
  100. Delamarre L, Holcombe H, Mellman I. 100.  2003. Presentation of exogenous antigens on major histocompatibility complex (MHC) class I and MHC class II molecules is differentially regulated during dendritic cell maturation. J. Exp. Med. 198:111–22 [Google Scholar]
  101. Barral DC, Cavallari M, McCormick PJ, Garg S, Magee AI. 101.  et al. 2008. CD1a and MHC class I follow a similar endocytic recycling pathway. Traffic 9:1446–57 [Google Scholar]
  102. Salamero J, Bausinger H, Mommaas AM, Lipsker D, Proamer F. 102.  et al. 2001. CD1a molecules traffic through the early recycling endosomal pathway in human Langerhans cells. J. Investig. Dermatol. 116:401–8 [Google Scholar]
  103. Aderem A. 103.  2002. How to eat something bigger than your head. Cell 110:5–8 [Google Scholar]
  104. Cox D, Lee DJ, Dale BM, Calafat J, Greenberg S. 104.  2000. A Rab11-containing rapidly recycling compartment in macrophages that promotes phagocytosis. PNAS 97:680–85 [Google Scholar]
  105. Gagnon E, Duclos S, Rondeau C, Chevet E, Cameron PH. 105.  et al. 2002. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 110:119–31 [Google Scholar]
  106. Burgdorf S, Kurts C. 106.  2008. Endocytosis mechanisms and the cell biology of antigen presentation. Curr. Opin. Immunol. 20:89–95 [Google Scholar]
  107. Moretti J, Blander JM. 107.  2014. Insights into phagocytosis-coupled activation of pattern recognition receptors and inflammasomes. Curr. Opin. Immunol. 26:100–10 [Google Scholar]
  108. Iwasaki A, Medzhitov R. 108.  2010. Regulation of adaptive immunity by the innate immune system. Science 327:291–95 [Google Scholar]
  109. Bevan MJ. 109.  2006. Cross-priming. Nat. Immunol. 7:363–65 [Google Scholar]
  110. Caminschi I, Maraskovsky E, Heath WR. 110.  2012. targeting dendritic cells in vivo for cancer therapy. Front. Immunol. 3:13 [Google Scholar]
  111. Kreutz M, Tacken PJ, Figdor CG. 111.  2013. Targeting dendritic cells—why bother?. Blood 121:2836–44 [Google Scholar]
  112. van Dinther D, Stolk DA, van de Ven R, van Kooyk Y, de Gruijl TD, den Haan JMM. 112.  2017. Targeting C-type lectin receptors: a high-carbohydrate diet for dendritic cells to improve cancer vaccines. J. Leukoc. Biol. 102:1017–34 [Google Scholar]
  113. Rauen J, Kreer C, Paillard A, van Duikeren S, Benckhuijsen WE. 113.  et al. 2014. Enhanced cross-presentation and improved CD8+ T cell responses after mannosylation of synthetic long peptides in mice. PLOS ONE 9:e103755 [Google Scholar]
  114. Harvey DJ, Wing DR, Kuster B, Wilson IB. 114.  2000. Composition of N-linked carbohydrates from ovalbumin and co-purified glycoproteins. J. Am. Soc. Mass Spectrom. 11:564–71 [Google Scholar]
  115. Burgdorf S, Kautz A, Bohnert V, Knolle PA, Kurts C. 115.  2007. Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316:612–16 [Google Scholar]
  116. Burgdorf S, Lukacs-Kornek V, Kurts C. 116.  2006. The mannose receptor mediates uptake of soluble but not of cell-associated antigen for cross-presentation. J. Immunol. 176:6770–76 [Google Scholar]
  117. Streng-Ouwehand I, Ho NI, Litjens M, Kalay H, Boks MA. 117.  et al. 2016. Glycan modification of antigen alters its intracellular routing in dendritic cells, promoting priming of T cells. eLife 5:e11765 [Google Scholar]
  118. Lizee G, Basha G, Jefferies WA. 118.  2005. Tails of wonder: endocytic-sorting motifs key for exogenous antigen presentation. Trends Immunol 26:141–49 [Google Scholar]
  119. Fehres CM, Kalay H, Bruijns SC, Musaafir SA, Ambrosini M. 119.  et al. 2015. Cross-presentation through langerin and DC-SIGN targeting requires different formulations of glycan-modified antigens. J. Control Release 203:67–76 [Google Scholar]
  120. Schreibelt G, Klinkenberg LJ, Cruz LJ, Tacken PJ, Tel J. 120.  et al. 2012. The C-type lectin receptor CLEC9A mediates antigen uptake and (cross-)presentation by human blood BDCA3+ myeloid dendritic cells. Blood 119:2284–92 [Google Scholar]
  121. Klechevsky E, Flamar AL, Cao Y, Blanck JP, Liu M. 121.  et al. 2010. Cross-priming CD8+ T cells by targeting antigens to human dendritic cells through DCIR. Blood 116:1685–97 [Google Scholar]
  122. Saluja SS, Hanlon DJ, Sharp FA, Hong E, Khalil D. 122.  et al. 2014. Targeting human dendritic cells via DEC-205 using PLGA nanoparticles leads to enhanced cross-presentation of a melanoma-associated antigen. Int. J. Nanomed. 9:5231–46 [Google Scholar]
  123. Fehres CM, van Beelen AJ, Bruijns SC, Ambrosini M, Kalay H. 123.  et al. 2015. In situ delivery of antigen to DC-SIGN+CD14+ dermal dendritic cells results in enhanced CD8+ T-cell responses. J. Investig. Dermatol. 135:2228–36 [Google Scholar]
  124. Ahrens S, Zelenay S, Sancho D, Hanc P, Kjaer S. 124.  et al. 2012. F-actin is an evolutionarily conserved damage-associated molecular pattern recognized by DNGR-1, a receptor for dead cells. Immunity 36:635–45 [Google Scholar]
  125. Zhang JG, Czabotar PE, Policheni AN, Caminschi I, Wan SS. 125.  et al. 2012. The dendritic cell receptor Clec9A binds damaged cells via exposed actin filaments. Immunity 36:646–57 [Google Scholar]
  126. Hanc P, Fujii T, Iborra S, Yamada Y, Huotari J. 126.  et al. 2015. Structure of the complex of F-actin and DNGR-1, a C-type lectin receptor involved in dendritic cell cross-presentation of dead cell-associated antigens. Immunity 42:839–49 [Google Scholar]
  127. Iborra S, Izquierdo HM, Martinez-Lopez M, Blanco-Menendez N, Reis e Sousa C, Sancho D. 127.  2012. The DC receptor DNGR-1 mediates cross-priming of CTLs during vaccinia virus infection in mice. J. Clin. Investig. 122:1628–43 [Google Scholar]
  128. Sancho D, Joffre OP, Keller AM, Rogers NC, Martinez D. 128.  et al. 2009. Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 458:899–903 [Google Scholar]
  129. Zelenay S, Keller AM, Whitney PG, Schraml BU, Deddouche S. 129.  et al. 2012. The dendritic cell receptor DNGR-1 controls endocytic handling of necrotic cell antigens to favor cross-priming of CTLs in virus-infected mice. J. Clin. Investig. 122:1615–27 [Google Scholar]
  130. Sancho D, Mourao-Sa D, Joffre OP, Schulz O, Rogers NC. 130.  et al. 2008. Tumor therapy in mice via antigen targeting to a novel, DC-restricted C-type lectin. J. Clin. Investig. 118:2098–110 [Google Scholar]
  131. Hanc P, Schulz O, Fischbach H, Martin SR, Kjaer S, Reis ESC. 131.  2016. A pH- and ionic strength-dependent conformational change in the neck region regulates DNGR-1 function in dendritic cells. EMBO J 35:2484–97 [Google Scholar]
  132. Lahoud MH, Proietto AI, Ahmet F, Kitsoulis S, Eidsmo L. 132.  et al. 2009. The C-type lectin Clec12A present on mouse and human dendritic cells can serve as a target for antigen delivery and enhancement of antibody responses. J. Immunol. 182:7587–94 [Google Scholar]
  133. Hutten TJ, Thordardottir S, Fredrix H, Janssen L, Woestenenk R. 133.  et al. 2016. CLEC12A-mediated antigen uptake and cross-presentation by human dendritic cell subsets efficiently boost tumor-reactive T cell responses. J. Immunol. 197:2715–25 [Google Scholar]
  134. Lahoud MH, Ahmet F, Kitsoulis S, Wan SS, Vremec D. 134.  et al. 2011. Targeting antigen to mouse dendritic cells via Clec9A induces potent CD4 T cell responses biased toward a follicular helper phenotype. J. Immunol. 187:842–50 [Google Scholar]
  135. Macri C, Dumont C, Panozza S, Lahoud MH, Caminschi I. 135.  et al. 2017. Antibody-mediated targeting of antigen to C-type lectin-like receptors Clec9A and Clec12A elicits different vaccination outcomes. Mol. Immunol. 81:143–50 [Google Scholar]
  136. Chatterjee B, Smed-Sorensen A, Cohn L, Chalouni C, Vandlen R. 136.  et al. 2012. Internalization and endosomal degradation of receptor-bound antigens regulate the efficiency of cross presentation by human dendritic cells. Blood 120:2011–20 [Google Scholar]
  137. Mahnke K, Guo M, Lee S, Sepulveda H, Swain SL. 137.  et al. 2000. The dendritic cell receptor for endocytosis, DEC-205, can recycle and enhance antigen presentation via major histocompatibility complex class II-positive lysosomal compartments. J. Cell Biol. 151:673–84 [Google Scholar]
  138. Sun SC. 138.  2011. Non-canonical NF-κB signaling pathway. Cell Res 21:71–85 [Google Scholar]
  139. Katakam AK, Brightbill H, Franci C, Kung C, Nunez V. 139.  et al. 2015. Dendritic cells require NIK for CD40-dependent cross-priming of CD8+ T cells. PNAS 112:14664–69 [Google Scholar]
  140. Platzer B, Stout M, Fiebiger E. 140.  2014. Antigen cross-presentation of immune complexes. Front. Immunol. 5:140 [Google Scholar]
  141. Boross P, van Montfoort N, Stapels DA, van der Poel CE, Bertens C. 141.  et al. 2014. FcRγ-chain ITAM signaling is critically required for cross-presentation of soluble antibody-antigen complexes by dendritic cells. J. Immunol. 193:5506–14 [Google Scholar]
  142. Ho NI, Camps MGM, de Haas EFE, Trouw LA, Verbeek JS, Ossendorp F. 142.  2017. C1q-dependent dendritic cell cross-presentation of in vivo-formed antigen-antibody complexes. J. Immunol. 198:4235–43 [Google Scholar]
  143. Murshid A, Gong J, Calderwood SK. 143.  2012. The role of heat shock proteins in antigen cross presentation. Front. Immunol. 3:63 [Google Scholar]
  144. Binder RJ. 144.  2014. Functions of heat shock proteins in pathways of the innate and adaptive immune system. J. Immunol. 193:5765–71 [Google Scholar]
  145. Calderwood SK, Mambula SS, Gray PJ Jr., Theriault JR. 145.  2007. Extracellular heat shock proteins in cell signaling. FEBS Lett 581:3689–94 [Google Scholar]
  146. Basu S, Binder RJ, Ramalingam T, Srivastava PK. 146.  2001. CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70, and calreticulin. Immunity 14:303–13 [Google Scholar]
  147. Binder RJ, Srivastava PK. 147.  2004. Essential role of CD91 in re-presentation of gp96-chaperoned peptides. PNAS 101:6128–33 [Google Scholar]
  148. Zhu H, Fang X, Zhang D, Wu W, Shao M. 148.  et al. 2015. Membrane-bound heat shock proteins facilitate the uptake of dying cells and cross-presentation of cellular antigen. Apoptosis 21:96–109 [Google Scholar]
  149. Vo MC, Nguyen-Pham TN, Lee HJ, Jung SH, Choi NR. 149.  et al. 2017. Chaetocin enhances dendritic cell function via the induction of heat shock protein and cancer testis antigens in myeloma cells. Oncotarget 8:46047–56 [Google Scholar]
  150. Mantegazza AR, Magalhaes JG, Amigorena S, Marks MS. 150.  2013. Presentation of phagocytosed antigens by MHC class I and II. Traffic 14:135–52 [Google Scholar]
  151. Nair-Gupta P, Blander JM. 151.  2013. An updated view of the intracellular mechanisms regulating cross-presentation. Front. Immunol. 4:401 [Google Scholar]
  152. Gil-Torregrosa BC, Lennon-Dumenil AM, Kessler B, Guermonprez P, Ploegh HL. 152.  et al. 2004. Control of cross-presentation during dendritic cell maturation. Eur. J. Immunol. 34:398–407 [Google Scholar]
  153. Alloatti A, Kotsias F, Pauwels AM, Carpier JM, Jouve M. 153.  et al. 2015. Toll-like receptor 4 engagement on dendritic cells restrains phago-lysosome fusion and promotes cross-presentation of antigens. Immunity 43:1087–100 [Google Scholar]
  154. Garrett WS, Chen LM, Kroschewski R, Ebersold M, Turley S. 154.  et al. 2000. Developmental control of endocytosis in dendritic cells by Cdc42. Cell 102:325–34 [Google Scholar]
  155. Weck MM, Grunebach F, Werth D, Sinzger C, Bringmann A, Brossart P. 155.  2007. TLR ligands differentially affect uptake and presentation of cellular antigens. Blood 109:3890–94 [Google Scholar]
  156. Wilson NS, Behrens GM, Lundie RJ, Smith CM, Waithman J. 156.  et al. 2006. Systemic activation of dendritic cells by Toll-like receptor ligands or malaria infection impairs cross-presentation and antiviral immunity. Nat. Immunol. 7:165–72 [Google Scholar]
  157. Villadangos JA, Schnorrer P, Wilson NS. 157.  2005. Control of MHC class II antigen presentation in dendritic cells: a balance between creative and destructive forces. Immunol. Rev. 207:191–205 [Google Scholar]
  158. Hochheiser K, Klein M, Gottschalk C, Hoss F, Scheu S. 158.  et al. 2016. Cutting edge: The RIG-I ligand 3pRNA potently improves CTL cross-priming and facilitates antiviral vaccination. J. Immunol. 196:2439–43 [Google Scholar]
  159. Xu J, Lee MH, Chakhtoura M, Green BL, Kotredes KP. 159.  et al. 2016. STAT2 is required for TLR-induced murine dendritic cell activation and cross-presentation. J. Immunol. 197:326–36 [Google Scholar]
  160. Rock KL, Shen L. 160.  2005. Cross-presentation: underlying mechanisms and role in immune surveillance. Immunol. Rev. 207:166–83 [Google Scholar]
  161. Joffre OP, Segura E, Savina A, Amigorena S. 161.  2012. Cross-presentation by dendritic cells. Nat. Rev. Immunol. 12:557–69 [Google Scholar]
  162. Wagner CS, Grotzke JE, Cresswell P. 162.  2012. Intracellular events regulating cross-presentation. Front. Immunol. 3:138 [Google Scholar]
  163. Saveanu L, Carroll O, Weimershaus M, Guermonprez P, Firat E. 163.  et al. 2009. IRAP identifies an endosomal compartment required for MHC class I cross-presentation. Science 325:213–17 [Google Scholar]
  164. Weimershaus M, Evnouchidou I, Saveanu L, van Endert P. 164.  2013. Peptidases trimming MHC class I ligands. Curr. Opin. Immunol. 25:90–96 [Google Scholar]
  165. Becker T, Volchuk A, Rothman JE. 165.  2005. Differential use of endoplasmic reticulum membrane for phagocytosis in J774 macrophages. PNAS 102:4022–26 [Google Scholar]
  166. McNew JA, Parlati F, Fukuda R, Johnston RJ, Paz K. 166.  et al. 2000. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 407:153–59 [Google Scholar]
  167. Touret N, Paroutis P, Terebiznik M, Harrison RE, Trombetta S. 167.  et al. 2005. Quantitative and dynamic assessment of the contribution of the ER to phagosome formation. Cell 123:157–70 [Google Scholar]
  168. Nunes-Hasler P, Demaurex N. 168.  2017. The ER phagosome connection in the era of membrane contact sites. Biochim. Biophys. Acta 1864:1513–24 [Google Scholar]
  169. Oliveira SC, Splitter GA. 169.  1995. CD8+ type 1 CD44hi CD45 RBlo T lymphocytes control intracellular Brucella abortus infection as demonstrated in major histocompatibility complex class I- and class II-deficient mice. Eur. J. Immunol. 25:2551–57 [Google Scholar]
  170. Turner J, Dockrell HM. 170.  1996. Stimulation of human peripheral blood mononuclear cells with live Mycobacterium bovis BCG activates cytolytic CD8+ T cells in vitro. Immunology 87:339–42 [Google Scholar]
  171. Canaday DH, Ziebold C, Noss EH, Chervenak KA, Harding CV, Boom WH. 171.  1999. Activation of human CD8+ alpha beta TCR+ cells by Mycobacterium tuberculosis via an alternate class I MHC antigen-processing pathway. J. Immunol. 162:372–79 [Google Scholar]
  172. Belkaid Y, Von Stebut E, Mendez S, Lira R, Caler E. 172.  et al. 2002. CD8+ T cells are required for primary immunity in C57BL/6 mice following low-dose, intradermal challenge with Leishmania major. . J. Immunol. 168:3992–4000 [Google Scholar]
  173. Pfeifer JD, Wick MJ, Roberts RL, Findlay K, Normark SJ, Harding CV. 173.  1993. Phagocytic processing of bacterial antigens for class I MHC presentation to T cells. Nature 361:359–62 [Google Scholar]
  174. da Conceicao-Silva F, Perlaza BL, Louis JA, Romero P. 174.  1994. Leishmania major infection in mice primes for specific major histocompatibility complex class I-restricted CD8+ cytotoxic T cell responses. Eur. J. Immunol. 24:2813–17 [Google Scholar]
  175. da Silva Santos C, Brodskyn CI. 175.  2014. The role of CD4 and CD8 T cells in human cutaneous leishmaniasis. Front. Public Health 2:165 [Google Scholar]
  176. Lin PL, Flynn JL. 176.  2015. CD8 T cells and Mycobacterium tuberculosis infection. Semin. Immunopathol. 37:239–49 [Google Scholar]
  177. Celli J, de Chastellier C, Franchini DM, Pizarro-Cerda J, Moreno E, Gorvel JP. 177.  2003. Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J. Exp. Med. 198:545–56 [Google Scholar]
  178. Blanchard N, Gonzalez F, Schaeffer M, Joncker NT, Cheng T. 178.  et al. 2008. Immunodominant, protective response to the parasite Toxoplasma gondii requires antigen processing in the endoplasmic reticulum. Nat. Immunol. 9:937–44 [Google Scholar]
  179. Goldszmid RS, Coppens I, Lev A, Caspar P, Mellman I, Sher A. 179.  2009. Host ER–parasitophorous vacuole interaction provides a route of entry for antigen cross-presentation in Toxoplasma gondii–infected dendritic cells. J. Exp. Med. 206:399–410 [Google Scholar]
  180. Dupont CD, Christian DA, Selleck EM, Pepper M, Leney-Greene M. 180.  et al. 2014. Parasite fate and involvement of infected cells in the induction of CD4+ and CD8+ T cell responses to Toxoplasma gondii. . PLOS Pathog 10:e1004047 [Google Scholar]
  181. Mordue DG, Hakansson S, Niesman I, Sibley LD. 181.  1999. Toxoplasma gondii resides in a vacuole that avoids fusion with host cell endocytic and exocytic vesicular trafficking pathways. Exp. Parasitol. 92:87–99 [Google Scholar]
  182. Guermonprez P, Saveanu L, Kleijmeer M, Davoust J, van Endert P, Amigorena S. 182.  2003. ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 425:397–402 [Google Scholar]
  183. Houde M, Bertholet S, Gagnon E, Brunet S, Goyette G. 183.  et al. 2003. Phagosomes are competent organelles for antigen cross-presentation. Nature 425:402–6 [Google Scholar]
  184. Alloatti A, Rookhuizen DC, Joannas L, Carpier JM, Iborra S. 184.  et al. 2017. Critical role for Sec22b-dependent antigen cross-presentation in antitumor immunity. J. Exp. Med. 214:2231–41 [Google Scholar]
  185. Wu SJ, Niknafs YS, Kim SH, Oravecz-Wilson K, Zajac C. 185.  et al. 2017. A critical analysis of the role of SNARE protein SEC22B in antigen cross-presentation. Cell Rep 19:2645–56 [Google Scholar]
  186. Montealegre S, van Endert P. 186.  2017. MHC class I cross-presentation: stage lights on Sec22b. Trends Immunol 38:618–21 [Google Scholar]
  187. Cotter K, Stransky L, McGuire C, Forgac M. 187.  2015. Recent insights into the structure, regulation, and function of the V-ATPases. Trends Biochem. Sci. 40:611–22 [Google Scholar]
  188. Delamarre L, Pack M, Chang H, Mellman I, Trombetta ES. 188.  2005. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 307:1630–34 [Google Scholar]
  189. Settembre C, Fraldi A, Medina DL, Ballabio A. 189.  2013. Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat. Rev. Mol. Cell Biol. 14:283–96 [Google Scholar]
  190. Sardiello M, Palmieri M, di Ronza A, Medina DL, Valenza M. 190.  et al. 2009. A gene network regulating lysosomal biogenesis and function. Science 325:473–77 [Google Scholar]
  191. Samie M, Cresswell P. 191.  2015. The transcription factor TFEB acts as a molecular switch that regulates exogenous antigen-presentation pathways. Nat. Immunol. 16:729–36 [Google Scholar]
  192. Calmette J, Bertrand M, Vetillard M, Ellouze M, Flint S. 192.  et al. 2016. Glucocorticoid-induced leucine zipper protein controls macropinocytosis in dendritic cells. J. Immunol. 197:4247–56 [Google Scholar]
  193. Lam GY, Huang J, Brumell JH. 193.  2010. The many roles of NOX2 NADPH oxidase-derived ROS in immunity. Semin. Immunopathol. 32:415–30 [Google Scholar]
  194. Savina A, Jancic C, Hugues S, Guermonprez P, Vargas P. 194.  et al. 2006. NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 126:205–18 [Google Scholar]
  195. Savina A, Peres A, Cebrian I, Carmo N, Moita C. 195.  et al. 2009. The small GTPase Rac2 controls phagosomal alkalinization and antigen crosspresentation selectively in CD8+ dendritic cells. Immunity 30:544–55 [Google Scholar]
  196. Dingjan I, Linders PT, van den Bekerom L, Baranov MV, Halder P. 196.  et al. 2017. Oxidized phagosomal NOX2 complex is replenished from lysosomes. J. Cell Sci. 130:1285–98 [Google Scholar]
  197. Kotsias F, Hoffmann E, Amigorena S, Savina A. 197.  2013. Reactive oxygen species production in the phagosome: impact on antigen presentation in dendritic cells. Antioxid. Redox Signal. 18:714–29 [Google Scholar]
  198. Mantegazza AR, Savina A, Vermeulen M, Perez L, Geffner J. 198.  et al. 2008. NADPH oxidase controls phagosomal pH and antigen cross-presentation in human dendritic cells. Blood 112:4712–22 [Google Scholar]
  199. Jancic C, Savina A, Wasmeier C, Tolmachova T, El-Benna J. 199.  et al. 2007. Rab27a regulates phagosomal pH and NADPH oxidase recruitment to dendritic cell phagosomes. Nat. Cell Biol. 9:367–78 [Google Scholar]
  200. Rybicka JM, Balce DR, Chaudhuri S, Allan ER, Yates RM. 200.  2012. Phagosomal proteolysis in dendritic cells is modulated by NADPH oxidase in a pH-independent manner. EMBO J 31:932–44 [Google Scholar]
  201. Hari A, Ganguly A, Mu L, Davis SP, Stenner MD. 201.  et al. 2015. Redirecting soluble antigen for MHC class I cross-presentation during phagocytosis. Eur. J. Immunol. 45:383–95 [Google Scholar]
  202. Allan ER, Tailor P, Balce DR, Pirzadeh P, McKenna NT. 202.  et al. 2014. NADPH oxidase modifies patterns of MHC class II-restricted epitopic repertoires through redox control of antigen processing. J. Immunol. 192:4989–5001 [Google Scholar]
  203. Datta SK, Raz E. 203.  2005. Induction of antigen cross-presentation by Toll-like receptors. Springer Semin. Immunopathol. 26:247–55 [Google Scholar]
  204. Nair P, Amsen D, Blander JM. 204.  2011. Co-ordination of incoming and outgoing traffic in antigen-presenting cells by pattern recognition receptors and T cells. Traffic 12:1669–76 [Google Scholar]
  205. Vulcano M, Dusi S, Lissandrini D, Badolato R, Mazzi P. 205.  et al. 2004. Toll receptor-mediated regulation of NADPH oxidase in human dendritic cells. J. Immunol. 173:5749–56 [Google Scholar]
  206. Blander JM, Medzhitov R. 206.  2004. Regulation of phagosome maturation by signals from Toll-like receptors. Science 304:1014–18 [Google Scholar]
  207. Trombetta ES, Ebersold M, Garrett W, Pypaert M, Mellman I. 207.  2003. Activation of lysosomal function during dendritic cell maturation. Science 299:1400–3 [Google Scholar]
  208. Wang T, Hong W. 208.  2002. Interorganellar regulation of lysosome positioning by the Golgi apparatus through Rab34 interaction with Rab-interacting lysosomal protein. Mol. Biol. Cell 13:4317–32 [Google Scholar]
  209. Kasmapour B, Gronow A, Bleck CK, Hong W, Gutierrez MG. 209.  2012. Size-dependent mechanism of cargo sorting during lysosome-phagosome fusion is controlled by Rab34. PNAS 109:20485–90 [Google Scholar]
  210. Drutman SB, Trombetta ES. 210.  2010. Dendritic cells continue to capture and present antigens after maturation in vivo. J. Immunol. 185:2140–46 [Google Scholar]
  211. Dingjan I, Paardekooper LM, Verboogen DRJ, von Mollard GF, Ter Beest M, van den Bogaart G. 211.  2017. VAMP8-mediated NOX2 recruitment to endosomes is necessary for antigen release. Eur. J. Cell Biol. 96:705–14 [Google Scholar]
  212. Matheoud D, Moradin N, Bellemare-Pelletier A, Shio MT, Hong WJ. 212.  et al. 2013. Leishmania evades host immunity by inhibiting antigen cross-presentation through direct cleavage of the SNARE VAMP8. Cell Host Microbe 14:15–25 [Google Scholar]
  213. Ding Y, Guo Z, Liu Y, Li X, Zhang Q. 213.  et al. 2016. The lectin Siglec-G inhibits dendritic cell cross-presentation by impairing MHC class I–peptide complex formation. Nat. Immunol. 17:1167–75 [Google Scholar]
  214. Chen W, Han C, Xie B, Hu X, Yu Q. 214.  et al. 2013. Induction of Siglec-G by RNA viruses inhibits the innate immune response by promoting RIG-I degradation. Cell 152:467–78 [Google Scholar]
  215. Thrasher AJ, Burns SO. 215.  2010. WASP: a key immunological multitasker. Nat. Rev. Immunol. 10:182–92 [Google Scholar]
  216. Baptista MA, Keszei M, Oliveira M, Sunahara KK, Andersson J. 216.  et al. 2016. Deletion of Wiskott-Aldrich syndrome protein triggers Rac2 activity and increased cross-presentation by dendritic cells. Nat. Commun. 7:12175 [Google Scholar]
  217. Baptista MAP, Westerberg LS. 217.  2017. Activation of compensatory pathways via Rac2 in the absence of the Cdc42 effector Wiskott-Aldrich syndrome protein in dendritic cells. Small GTPases Jan 27:1–8 [Google Scholar]
  218. Shen L, Sigal LJ, Boes M, Rock KL. 218.  2004. Important role of cathepsin S in generating peptides for TAP-independent MHC class I crosspresentation in vivo. Immunity 21:155–65 [Google Scholar]
  219. Shi GP, Munger JS, Meara JP, Rich DH, Chapman HA. 219.  1992. Molecular cloning and expression of human alveolar macrophage cathepsin S, an elastinolytic cysteine protease. J. Biol. Chem. 267:7258–62 [Google Scholar]
  220. Lin ML, Zhan Y, Proietto AI, Prato S, Wu L. 220.  et al. 2008. Selective suicide of cross-presenting CD8+ dendritic cells by cytochrome c injection shows functional heterogeneity within this subset. PNAS 105:3029–34 [Google Scholar]
  221. Baleeiro RB, Walden P. 221.  2017. Immature human DCs efficiently translocate endocytosed antigens into the cytosol for proteasomal processing. Mol. Immunol. 88:148–54 [Google Scholar]
  222. Giodini A, Cresswell P. 222.  2008. Hsp90-mediated cytosolic refolding of exogenous proteins internalized by dendritic cells. EMBO J 27:201–11 [Google Scholar]
  223. Zehner M, Chasan AI, Schuette V, Embgenbroich M, Quast T. 223.  et al. 2011. Mannose receptor polyubiquitination regulates endosomal recruitment of p97 and cytosolic antigen translocation for cross-presentation. PNAS 108:9933–38 [Google Scholar]
  224. Zehner M, Burgdorf S. 224.  2013. Regulation of antigen transport into the cytosol for cross-presentation by ubiquitination of the mannose receptor. Mol. Immunol. 55:146–48 [Google Scholar]
  225. Dingjan I, Verboogen DR, Paardekooper LM, Revelo NH, Sittig SP. 225.  et al. 2016. Lipid peroxidation causes endosomal antigen release for cross-presentation. Sci. Rep. 6:22064 [Google Scholar]
  226. Tretter T, Pereira FP, Ulucan O, Helms V, Allan S. 226.  et al. 2013. ERAD and protein import defects in a sec61 mutant lacking ER-lumenal loop 7. BMC Cell Biol 14:56 [Google Scholar]
  227. Kaiser ML, Romisch K. 227.  2015. Proteasome 19S RP binding to the Sec61 channel plays a key role in ERAD. PLOS ONE 10:e0117260 [Google Scholar]
  228. Grotzke JE, Cresswell P. 228.  2015. Are ERAD components involved in cross-presentation?. Mol. Immunol. 68:112–15 [Google Scholar]
  229. Romisch K. 229.  2017. A case for Sec61 channel involvement in ERAD. Trends Biochem. Sci. 42:171–79 [Google Scholar]
  230. Imai J, Hasegawa H, Maruya M, Koyasu S, Yahara I. 230.  2005. Exogenous antigens are processed through the endoplasmic reticulum-associated degradation (ERAD) in cross-presentation by dendritic cells. Int. Immunol. 17:45–53 [Google Scholar]
  231. Zehner M, Marschall AL, Bos E, Schloetel JG, Kreer C. 231.  et al. 2015. The translocon protein Sec61 mediates antigen transport from endosomes in the cytosol for cross-presentation to CD8+ T cells. Immunity 42:850–63 [Google Scholar]
  232. Schauble N, Cavalie A, Zimmermann R, Jung M. 232.  2014. Interaction of Pseudomonas aeruginosa Exotoxin A with the human Sec61 complex suppresses passive calcium efflux from the endoplasmic reticulum. Channels 8:76–83 [Google Scholar]
  233. Ackerman AL, Giodini A, Cresswell P. 233.  2006. A role for the endoplasmic reticulum protein retrotranslocation machinery during crosspresentation by dendritic cells. Immunity 25:607–17 [Google Scholar]
  234. Ye Y, Meyer HH, Rapoport TA. 234.  2001. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414:652–56 [Google Scholar]
  235. Menager J, Ebstein F, Oger R, Hulin P, Nedellec S. 235.  et al. 2014. Cross-presentation of synthetic long peptides by human dendritic cells: a process dependent on ERAD component p97/VCP but not sec61 and/or Derlin-1. PLOS ONE 9:e89897 [Google Scholar]
  236. Baron L, Paatero AO, Morel JD, Impens F, Guenin-Mace L. 236.  et al. 2016. Mycolactone subverts immunity by selectively blocking the Sec61 translocon. J. Exp. Med. 213:2885–96 [Google Scholar]
  237. George KM, Chatterjee D, Gunawardana G, Welty D, Hayman J. 237.  et al. 1999. Mycolactone: a polyketide toxin from Mycobacterium ulcerans required for virulence. Science 283:854–57 [Google Scholar]
  238. McKenna M, Simmonds RE, High S. 238.  2016. Mechanistic insights into the inhibition of Sec61-dependent co- and post-translational translocation by mycolactone. J. Cell Sci. 129:1404–15 [Google Scholar]
  239. McKenna M, Simmonds RE, High S. 239.  2017. Mycolactone reveals the substrate-driven complexity of Sec61-dependent transmembrane protein biogenesis. J. Cell Sci. 130:1307–20 [Google Scholar]
  240. Grotzke JE, Kozik P, Morel JD, Impens F, Pietrosemoli N. 240.  et al. 2017. Sec61 blockade by mycolactone inhibits antigen cross-presentation independently of endosome-to-cytosol export. PNAS 114:29E5910–19 [Google Scholar]
  241. Bougneres L, Helft J, Tiwari S, Vargas P, Chang BH. 241.  et al. 2009. A role for lipid bodies in the cross-presentation of phagocytosed antigens by MHC class I in dendritic cells. Immunity 31:232–44 [Google Scholar]
  242. Martens S, Parvanova I, Zerrahn J, Griffiths G, Schell G. 242.  et al. 2005. Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLOS Pathog 1:e24 [Google Scholar]
  243. Ling YM, Shaw MH, Ayala C, Coppens I, Taylor GA. 243.  et al. 2006. Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J. Exp. Med. 203:2063–71 [Google Scholar]
  244. Khan IA, Ely KH, Kasper LH. 244.  1991. A purified parasite antigen (p30) mediates CD8+ T cell immunity against fatal Toxoplasma gondii infection in mice. J. Immunol. 147:3501–6 [Google Scholar]
  245. Kwok LY, Lutjen S, Soltek S, Soldati D, Busch D. 245.  et al. 2003. The induction and kinetics of antigen-specific CD8 T cells are defined by the stage specificity and compartmentalization of the antigen in murine toxoplasmosis. J. Immunol. 170:1949–57 [Google Scholar]
  246. Gregg B, Dzierszinski F, Tait E, Jordan KA, Hunter CA, Roos DS. 246.  2011. Subcellular antigen location influences T-cell activation during acute infection with Toxoplasma gondii. . PLOS ONE 6:e22936 [Google Scholar]
  247. Lopez J, Bittame A, Massera C, Vasseur V, Effantin G. 247.  et al. 2015. Intravacuolar membranes regulate CD8 T cell recognition of membrane-bound Toxoplasma gondii protective antigen. Cell Rep 13:2273–86 [Google Scholar]
  248. Carlson EJ, Pitonzo D, Skach WR. 248.  2006. p97 functions as an auxiliary factor to facilitate TM domain extraction during CFTR ER-associated degradation. EMBO J 25:4557–66 [Google Scholar]
  249. Bertholet S, Goldszmid R, Morrot A, Debrabant A, Afrin F. 249.  et al. 2006. Leishmania antigens are presented to CD8+ T cells by a transporter associated with antigen processing-independent pathway in vitro and in vivo. J. Immunol. 177:3525–33 [Google Scholar]
  250. Ndjamen B, Kang BH, Hatsuzawa K, Kima PE. 250.  2010. Leishmania parasitophorous vacuoles interact continuously with the host cell's endoplasmic reticulum; parasitophorous vacuoles are hybrid compartments. Cell Microbiol 12:1480–94 [Google Scholar]
  251. Ackerman AL, Kyritsis C, Tampe R, Cresswell P. 251.  2003. Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens. PNAS 100:12889–94 [Google Scholar]
  252. Fischbach H, Doring M, Nikles D, Lehnert E, Baldauf C. 252.  et al. 2015. Ultrasensitive quantification of TAP-dependent antigen compartmentalization in scarce primary immune cell subsets. Nat. Commun. 6:6199 [Google Scholar]
  253. Zuo D, Subjeck J, Wang XY. 253.  2016. Unfolding the role of large heat shock proteins: new insights and therapeutic implications. Front. Immunol. 7:75 [Google Scholar]
  254. Wang H, Yu X, Guo C, Zuo D, Fisher PB. 254.  et al. 2013. Enhanced endoplasmic reticulum entry of tumor antigen is crucial for cross-presentation induced by dendritic cell-targeted vaccination. J. Immunol. 191:6010–21 [Google Scholar]
  255. Ackerman AL, Kyritsis C, Tampe R, Cresswell P. 255.  2005. Access of soluble antigens to the endoplasmic reticulum can explain cross-presentation by dendritic cells. Nat. Immunol. 6:107–13 [Google Scholar]
  256. Johannes L, Popoff V. 256.  2008. Tracing the retrograde route in protein trafficking. Cell 135:1175–87 [Google Scholar]
  257. Burgdorf S, Scholz C, Kautz A, Tampe R, Kurts C. 257.  2008. Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nat. Immunol. 9:558–66 [Google Scholar]
  258. Lawand M, Abramova A, Manceau V, Springer S, van Endert P. 258.  2016. TAP-dependent and -independent peptide import into dendritic cell phagosomes. J. Immunol. 197:3454–63 [Google Scholar]
  259. Di Pucchio T, Chatterjee B, Smed-Sorensen A, Clayton S, Palazzo A. 259.  et al. 2008. Direct proteasome-independent cross-presentation of viral antigen by plasmacytoid dendritic cells on major histocompatibility complex class I. Nat. Immunol. 9:551–57 [Google Scholar]
  260. Stow JL, Manderson AP, Murray RZ. 260.  2006. SNAREing immunity: the role of SNAREs in the immune system. Nat. Rev. Immunol. 6:919–29 [Google Scholar]
  261. Husebye H, Aune MH, Stenvik J, Samstad E, Skjeldal F. 261.  et al. 2010. The Rab11a GTPase controls Toll-like receptor 4-induced activation of interferon regulatory factor-3 on phagosomes. Immunity 33:583–96 [Google Scholar]
  262. Le Bon A, Etchart N, Rossmann C, Ashton M, Hou S. 262.  et al. 2003. Cross-priming of CD8+ T cells stimulated by virus-induced type I interferon. Nat. Immunol. 4:1009–15 [Google Scholar]
  263. Snyder DA, Kelly ML, Woodbury DJ. 263.  2006. SNARE complex regulation by phosphorylation. Cell Biochem. Biophys. 45:111–23 [Google Scholar]
  264. Wickner W, Schekman R. 264.  2008. Membrane fusion. Nat. Struct. Mol. Biol. 15:658–64 [Google Scholar]
  265. Kretzer NM, Theisen DJ, Tussiwand R, Briseno CG, Grajales-Reyes GE. 265.  et al. 2016. RAB43 facilitates cross-presentation of cell-associated antigens by CD8α+ dendritic cells. J. Exp. Med. 213:2871–83 [Google Scholar]
  266. De Angelis Rigotti F, De Gassart A, Pforr C, Cano F, N'Guessan P. 266.  et al. 2017. MARCH9-mediated ubiquitination regulates MHC I export from the TGN. Immunol. Cell Biol. 95:753–64 [Google Scholar]
  267. Bock JB, Klumperman J, Davanger S, Scheller RH. 267.  1997. Syntaxin 6 functions in trans-Golgi network vesicle trafficking. Mol. Biol. Cell 8:1261–71 [Google Scholar]
  268. Falguieres T, Castle D, Gruenberg J. 268.  2012. Regulation of the MVB pathway by SCAMP3. Traffic 13:131–42 [Google Scholar]
  269. Roche PA, Marks MS, Cresswell P. 269.  1991. Formation of a nine-subunit complex by HLA class II glycoproteins and the invariant chain. Nature 354:392–94 [Google Scholar]
  270. Lamb CA, Cresswell P. 270.  1992. Assembly and transport properties of invariant chain trimers and HLA-DR-invariant chain complexes. J. Immunol. 148:3478–82 [Google Scholar]
  271. Sugita M, Brenner MB. 271.  1995. Association of the invariant chain with major histocompatibility complex class I molecules directs trafficking to endocytic compartments. J. Biol. Chem. 270:1443–48 [Google Scholar]
  272. Vigna JL, Smith KD, Lutz CT. 272.  1996. Invariant chain association with MHC class I: preference for HLA class I/beta 2-microglobulin heterodimers, specificity, and influence of the MHC peptide-binding groove. J. Immunol. 157:4503–10 [Google Scholar]
  273. Basha G, Omilusik K, Chavez-Steenbock A, Reinicke AT, Lack N. 273.  et al. 2012. A CD74-dependent MHC class I endolysosomal cross-presentation pathway. Nat. Immunol. 13:237–45 [Google Scholar]
  274. Greenfield JJ, High S. 274.  1999. The Sec61 complex is located in both the ER and the ER-Golgi intermediate compartment. J. Cell Sci. 112:Part 101477–86 [Google Scholar]
  275. Casbon AJ, Allen LA, Dunn KW, Dinauer MC. 275.  2009. Macrophage NADPH oxidase flavocytochrome B localizes to the plasma membrane and Rab11-positive recycling endosomes. J. Immunol. 182:2325–39 [Google Scholar]
  276. Arango Duque G, Fukuda M, Descoteaux A. 276.  2013. Synaptotagmin XI regulates phagocytosis and cytokine secretion in macrophages. J. Immunol. 190:1737–45 [Google Scholar]
  277. Ma W, Zhang Y, Vigneron N, Stroobant V, Thielemans K. 277.  et al. 2016. Long-peptide cross-presentation by human dendritic cells occurs in vacuoles by peptide exchange on nascent MHC class I molecules. J. Immunol. 196:1711–20 [Google Scholar]
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