Present Yourself! By MHC Class I and MHC Class II Molecules

Trends in Immunology

Volumn 37, Issue 11, 2016, Pages 724-737

  Rock, Kenneth L ^a   Reits, Eric ^b   Neefjes, Jacques ^c,d  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

antigen presentation; autoimmune diseases; MHC class I; MHC class II; transplantation; tumor immunology

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; ANTIGEN; CHAPERONE; HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2; PEPTIDE FRAGMENT; PEPTIDE HYDROLASE;

ANTIGEN PRESENTATION; GENETIC VARIATION; HUMAN; MOLECULAR EVOLUTION; NONHUMAN; PATHOGENESIS; REVIEW; TUMOR ESCAPE; ANIMAL; GRAFT REJECTION; IMMUNOLOGY; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; METABOLISM; NEOPLASMS; ORGAN TRANSPLANTATION; PROCEDURES; T LYMPHOCYTE; TRENDS;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS; GRAFT REJECTION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; MOLECULAR CHAPERONES; NEOPLASMS; ORGAN TRANSPLANTATION; PEPTIDE FRAGMENTS; PEPTIDE HYDROLASES; T-LYMPHOCYTES;

EID: 84992702699     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2016.08.010     Document Type: Review

References (129)

1. 1 Flajnik, M.F., Kasahara, M., Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat. Rev. Genet. 11 (2010), 47–59.
2. 2 Brown, J.H., et al. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364 (1993), 33–39.
3. 3 Bjorkman, P.J., et al. The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 329 (1987), 512–518.
4. 4 Zhang, P., et al. Crystal structure of the stress-inducible human heat shock protein 70 substrate-binding domain in complex with peptide substrate. PLoS One, 9, 2014, e103518.
5. 5 Dong, G., et al. Insights into MHC class I peptide loading from the structure of the tapasin–ERp57 thiol oxidoreductase heterodimer. Immunity 30 (2009), 21–32.
6. 6 Teng, M.S., et al. A human TAPBP (TAPASIN)-related gene. TAPBP-R. Eur. J. Immunol. 32 (2002), 1059–1068.
7. 7 Boyle, L.H., et al. Tapasin-related protein TAPBPR is an additional component of the MHC class I presentation pathway. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 3465–3470.
8. 8 Mosyak, L., et al. The structure of HLA-DM, the peptide exchange catalyst that loads antigen onto class II MHC molecules during antigen presentation. Immunity 9 (1998), 377–383.
9. 9 Fremont, D.H., et al. Crystal structure of mouse H2-M. Immunity 9 (1998), 385–393.
10. 10 Guce, A.I., et al. HLA-DO acts as a substrate mimic to inhibit HLA-DM by a competitive mechanism. Nat. Struct. Mol. Biol. 20 (2013), 90–98.
11. 11 Falk, K., et al. Pool sequencing of natural HLA-DR, DQ, and DP ligands reveals detailed peptide motifs, constraints of processing, and general rules. Immunogenetics 39 (1994), 230–242.
12. 12 Falk, K., et al. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 351 (1991), 290–296.
13. 13 Madden, D.R., et al. The antigenic identity of peptide–MHC complexes: a comparison of the conformations of five viral peptides presented by HLA-A2. Cell 75 (1993), 693–708.
14. 14 Smith, K.J., et al. Bound water structure and polymorphic amino acids act together to allow the binding of different peptides to MHC class I HLA-B53. Immunity 4 (1996), 215–228.
15. 15 Walz, S., et al. The antigenic landscape of multiple myeloma: mass spectrometry (re)defines targets for T-cell-based immunotherapy. Blood 126 (2015), 1203–1213.
16. 16 Schmid, B.V., et al. Quantifying how MHC polymorphism prevents pathogens from adapting to the antigen presentation pathway. Epidemics 2 (2010), 99–108.
17. 17 Chaix, R., et al. Is mate choice in humans MHC-dependent?. PLoS Genet., 4, 2008, e1000184.
18. 18 Siddle, H.V., et al. Characterization of major histocompatibility complex class I and class II genes from the Tasmanian devil (Sarcophilus harrisii). Immunogenetics 59 (2007), 753–760.
19. 19 Siddle, H.V., et al. Reversible epigenetic down-regulation of MHC molecules by devil facial tumour disease illustrates immune escape by a contagious cancer. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 5103–5108.
20. 20 Neefjes, J., et al. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat. Rev. Immunol. 11 (2011), 823–836.
21. 21 Michalek, M.T., et al. A role for the ubiquitin-dependent proteolytic pathway in MHC class I-restricted antigen presentation. Nature 363 (1993), 552–554.
22. 22 Rock, K.L., et al. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78 (1994), 761–771.
23. 23 Reits, E., et al. Peptide diffusion, protection, and degradation in nuclear and cytoplasmic compartments before antigen presentation by MHC class I. Immunity 18 (2003), 97–108.
24. 24 Cresswell, P., et al. The nature of the MHC class I peptide loading complex. Immunol. Rev. 172 (1999), 21–28.
25. 25 Wearsch, P.A., Cresswell, P., Selective loading of high-affinity peptides onto major histocompatibility complex class I molecules by the tapasin–ERp57 heterodimer. Nat. Immunol. 8 (2007), 873–881.
26. 26 Garstka, M.A., et al. The first step of peptide selection in antigen presentation by MHC class I molecules. Proc. Natl. Acad. Sci. U.S.A. 112 (2015), 1505–1510.
27. 27 Saveanu, L., et al. Concerted peptide trimming by human ERAP1 and ERAP2 aminopeptidase complexes in the endoplasmic reticulum. Nat. Immunol. 6 (2005), 689–697.
28. 28 Saric, T., et al. An IFN-γ-induced aminopeptidase in the ER, ERAP1, trims precursors to MHC class I-presented peptides. Nat. Immunol. 3 (2002), 1169–1176.
29. 29 Serwold, T., et al. ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 419 (2002), 480–483.
30. 30 Morozov, G.I., et al. Interaction of TAPBPR, a tapasin homolog, with MHC-I molecules promotes peptide editing. Proc. Natl Acad. Sci. U.S.A. 113 (2016), E1006–E1015.
31. 31 Hermann, C., et al. TAPBPR alters MHC class I peptide presentation by functioning as a peptide exchange catalyst. Elife, 4, 2015, e09617.
32. 32 Chang, S.C., et al. The ER aminopeptidase, ERAP1, trims precursors to lengths of MHC class I peptides by a “molecular ruler” mechanism. Proc. Natl Acad. Sci. U.S.A. 102 (2005), 17107–17112.
33. 33 York, I.A., et al. The ER aminopeptidase ERAP1 enhances or limits antigen presentation by trimming epitopes to 8-9 residues. Nat. Immunol. 3 (2002), 1177–1184.
34. 34 Nguyen, T.T., et al. Structural basis for antigenic peptide precursor processing by the endoplasmic reticulum aminopeptidase ERAP1. Nat. Struct. Mol. Biol. 18 (2011), 604–613.
35. 35 Roelse, J., et al. Trimming of TAP-translocated peptides in the endoplasmic reticulum and in the cytosol during recycling. J. Exp. Med. 180 (1994), 1591–1597.
36. 36 Elliott, T., et al. Peptide-induced conformational change of the class I heavy chain. Nature 351 (1991), 402–406.
37. 37 Schumacher, T.N., et al. Direct binding of peptide to empty MHC class I molecules on intact cells and in vitro. Cell 62 (1990), 563–567.
38. 38 Kelly, A., et al. Assembly and function of the two ABC transporter proteins encoded in the human major histocompatibility complex. Nature 355 (1992), 641–644.
39. 39 Neefjes, J.J., Ploegh, H.L., Allele and locus-specific differences in cell surface expression and the association of HLA class I heavy chain with beta 2-microglobulin: differential effects of inhibition of glycosylation on class I subunit association. Eur. J. Immunol. 18 (1988), 801–810.
40. 40 Rammensee, H., et al. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50 (1999), 213–219.
41. 41 Schubert, U., et al. Proteasome inhibition interferes with gag polyprotein processing, release, and maturation of HIV-1 and HIV-2. Proc. Natl. Acad. Sci. U.S.A. 97 (2000), 13057–13062.
42. 42 Princiotta, M.F., et al. Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 18 (2003), 343–354.
43. 43 Reits, E.A., et al. The major substrates for TAP in vivo are derived from newly synthesized proteins. Nature 404 (2000), 774–778.
44. 44 Yewdell, J.W., DRiPs solidify: progress in understanding endogenous MHC class I antigen processing. Trends Immunol. 32 (2011), 548–558.
45. 45 Rock, K.L., et al. Re-examining class-I presentation and the DRiP hypothesis. Trends Immunol. 35 (2014), 144–152.
46. 46 Monaco, J.J., Nandi, D., The genetics of proteasomes and antigen processing. Annu. Rev. Genet. 29 (1995), 729–754.
47. 47 Gaczynska, M., et al. γ-Interferon and expression of MHC genes regulate peptide hydrolysis by proteasomes. Nature 365 (1993), 264–267.
48. 48 Groettrup, M., et al. A third interferon-γ-induced subunit exchange in the 20S proteasome. Eur. J. Immunol. 26 (1996), 863–869.
49. 49 Toes, R.E., et al. Discrete cleavage motifs of constitutive and immunoproteasomes revealed by quantitative analysis of cleavage products. J. Exp. Med. 194 (2001), 1–12.
50. + T cells. Nat. Immunol. 17 (2016), 938–945.
51. 51 Ossendorp, F., et al. A single residue exchange within a viral CTL epitope alters proteasome-mediated degradation resulting in lack of antigen presentation. Immunity 5 (1996), 115–124.
52. 52 Tomaru, U., et al. Exclusive expression of proteasome subunit β5t in the human thymic cortex. Blood 113 (2009), 5186–5191.
53. 53 Yewdell, J.W., et al. Making sense of mass destruction: quantitating MHC class I antigen presentation. Nat. Rev. Immunol. 3 (2003), 952–961.
54. 54 Meyer, V.S., et al. Identification of natural MHC class II presented phosphopeptides and tumor-derived MHC class I phospholigands. J. Proteome Res. 8 (2009), 3666–3674.
55. 55 Haurum, J.S., et al. Presentation of cytosolic glycosylated peptides by human class I major histocompatibility complex molecules in vivo. J. Exp. Med. 190 (1999), 145–150.
56. 56 Petersen, J., et al. Post-translationally modified T cell epitopes: immune recognition and immunotherapy. J. Mol. Med. 87 (2009), 1045–1051.
57. 57 Gromme, M., et al. The rational design of TAP inhibitors using peptide substrate modifications and peptidomimetics. Eur. J. Immunol. 27 (1997), 898–904.
58. 58 Andersen, M.H., et al. Phosphorylated peptides can be transported by TAP molecules, presented by class I MHC molecules, and recognized by phosphopeptide-specific CTL. J. Immunol. 163 (1999), 3812–3818.
59. 59 Mohammed, F., et al. Phosphorylation-dependent interaction between antigenic peptides and MHC class I: a molecular basis for the presentation of transformed self. Nat. Immunol. 9 (2008), 1236–1243.
60. 60 Zarling, A.L., et al. Phosphorylated peptides are naturally processed and presented by major histocompatibility complex class I molecules in vivo. J. Exp. Med. 192 (2000), 1755–1762.
61. 61 Berkers, C.R., et al. Definition of proteasomal peptide splicing rules for high-efficiency spliced peptide presentation by MHC class I molecules. J. Immunol. 195 (2015), 4085–4095.
62. 62 Ploegh, H.L., Viral strategies of immune evasion. Science 280 (1998), 248–253.
63. 63 Ploegh, H.L., Trafficking and assembly of MHC molecules: how viruses elude the immune system. Cold Spring Harb. Symp. Quant. Biol. 60 (1995), 263–266.
64. 64 van Hall, T., et al. The Varicellovirus-encoded TAP inhibitor UL49.5 regulates the presentation of CTL epitopes by Qa-1b1. J. Immunol. 178 (2007), 657–662.
65. 65 Lichtenstein, D.L., Wold, W.S., Experimental infections of humans with wild-type adenoviruses and with replication-competent adenovirus vectors: replication, safety, and transmission. Cancer Gene Ther. 11 (2004), 819–829.
66. 66 Ziegler, H., et al. The luminal part of the murine cytomegalovirus glycoprotein gp40 catalyzes the retention of MHC class I molecules. EMBO J. 19 (2000), 870–881.
67. 67 Mittal, D., et al. New insights into cancer immunoediting and its three component phases – elimination, equilibrium and escape. Curr. Opin. Immunol. 27 (2014), 16–25.
68. 68 Garcia-Lora, A., et al. MHC class I antigens, immune surveillance, and tumor immune escape. J. Cell. Physiol. 195 (2003), 346–355.
69. 69 Snyder, A., et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N. Engl. J. Med. 371 (2014), 2189–2199.
70. 70 Smit, E.F., Baas, P., Lung cancer in 2015: bypassing checkpoints, overcoming resistance, and honing in on new targets. Nat. Rev. Clin. Oncol. 13 (2016), 75–76.
71. 71 Saccheri, F., et al. Bacteria-induced gap junctions in tumors favor antigen cross-presentation and antitumor immunity. Sci. Transl. Med., 2, 2010, 44ra57.
72. 72 Neijssen, J., et al. Cross-presentation by intercellular peptide transfer through gap junctions. Nature 434 (2005), 83–88.
73. 73 Bevan, M.J., Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay. J. Exp. Med. 143 (1976), 1283–1288.
74. 74 Rock, K.L., et al. Presentation of exogenous antigen with class I major histocompatibility complex molecules. Science 249 (1990), 918–921.
75. 75 Kurts, C., et al. Cross-priming in health and disease. Nat. Rev. Immunol. 10 (2010), 403–414.
76. 76 Amigorena, S., Y in X priming. Nat. Immunol. 4 (2003), 1047–1048.
77. 77 Segura, E., Amigorena, S., Cross-presentation in mouse and human dendritic cells. Adv. Immunol. 127 (2015), 1–31.
78. 78 Guermonprez, P., et al. ER–phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 425 (2003), 397–402.
79. 79 Zitvogel, L., et al. Immunological aspects of anticancer chemotherapy. Bull. Acad. Natl. Med. 192 (2008), 1469–1487.
80. 80 Kovacsovics-Bankowski, M., et al. Efficient major histocompatibility complex class I presentation of exogenous antigen upon phagocytosis by macrophages. Proc. Natl. Acad. Sci. U.S.A. 90 (1993), 4942–4946.
81. 81 Matheoud, D., et al. Cross-presentation by dendritic cells from live cells induces protective immune responses in vivo. Blood 115 (2010), 4412–4420.
82. 82 Amigorena, S., Fc gamma receptors and cross-presentation in dendritic cells. J. Exp. Med. 195 (2002), F1–F3.
83. 83 Schuette, V., Burgdorf, S., The ins-and-outs of endosomal antigens for cross-presentation. Curr. Opin. Immunol. 26 (2014), 63–68.
84. 84 Joffre, O.P., et al. Cross-presentation by dendritic cells. Nat. Rev. Immunol. 12 (2012), 557–569.
85. 85 Kovacsovics-Bankowski, M., Rock, K.L., A phagosome-to-cytosol pathway for exogenous antigens presented on MHC class I molecules. Science 267 (1995), 243–246.
86. 86 Gromme, M., et al. Recycling MHC class I molecules and endosomal peptide loading. Proc. Natl. Acad. Sci. U.S.A. 96 (1999), 10326–10331.
87. 87 Dorsey, B.D., et al. Discovery of a potent, selective, and orally active proteasome inhibitor for the treatment of cancer. J. Med. Chem. 51 (2008), 1068–1072.
88. 88 Shen, L., et al. Important role of cathepsin S in generating peptides for TAP-independent MHC class I crosspresentation in vivo. Immunity 21 (2004), 155–165.
89. 89 Nair-Gupta, P., et al. TLR signals induce phagosomal MHC-I delivery from the endosomal recycling compartment to allow cross-presentation. Cell 158 (2014), 506–521.
90. 90 Unanue, E.R., et al. Variations in MHC class II antigen processing and presentation in health and disease. Annu. Rev. Immunol. 34 (2016), 265–297.
91. 91 Waldburger, J.M., et al. Lessons from the bare lymphocyte syndrome: molecular mechanisms regulating MHC class II expression. Immunol. Rev. 178 (2000), 148–165.
92. 92 Jones, E.Y., MHC class I and class II structures. Curr. Opin. Immunol. 9 (1997), 75–79.
93. 93 Malmstrom, M., et al. Unraveling the evolution of the Atlantic cod's (Gadus morhua L.) alternative immune strategy. PLoS One, 8, 2013, e74004.
94. 94 Stern, L.J., et al. Crystal structure of the human class II MHC protein HLA-DR1 complexed with an influenza virus peptide. Nature 368 (1994), 215–221.
95. 95 Suri, A., et al. The wide diversity and complexity of peptides bound to class II MHC molecules. Curr. Opin. Immunol. 18 (2006), 70–77.
96. 96 Cresswell, P., Roche, P.A., Invariant chain-MHC class II complexes: always odd and never invariant. Immunol. Cell Biol. 92 (2014), 471–472.
97. 97 Neefjes, J., CIIV, MIIC and other compartments for MHC class II loading. Eur. J. Immunol. 29 (1999), 1421–1425.
98. 98 Ghosh, P., et al. The structure of an intermediate in class II MHC maturation: CLIP bound to HLA-DR3. Nature 378 (1995), 457–462.
99. 99 Denzin, L.K., Cresswell, P., HLA-DM induces CLIP dissociation from MHC class II alpha beta dimers and facilitates peptide loading. Cell 82 (1995), 155–165.
100. 100 Pos, W., et al. Crystal structure of the HLA-DM–HLA-DR1 complex defines mechanisms for rapid peptide selection. Cell 151 (2012), 1557–1568.
101. 101 Wubbolts, R., et al. Direct vesicular transport of MHC class II molecules from lysosomal structures to the cell surface. J. Cell Biol. 135 (1996), 611–622.
102. 102 Boes, M., et al. T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature 418 (2002), 983–988.
103. 103 Kleijmeer, M., et al. Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells. J. Cell Biol. 155 (2001), 53–63.
104. 104 Nielsen, M., et al. NetMHCIIpan-2.0 – improved pan-specific HLA-DR predictions using a novel concurrent alignment and weight optimization training procedure. Immunome Res., 6, 2010, 9.
105. 105 Fernando, M.M., et al. Defining the role of the MHC in autoimmunity: a review and pooled analysis. PLoS Genet., 4, 2008, e1000024.
106. 106 Sollid, L.M., Jabri, B., Celiac disease and transglutaminase 2: a model for posttranslational modification of antigens and HLA association in the pathogenesis of autoimmune disorders. Curr. Opin. Immunol. 23 (2011), 732–738.
107. 107 Steck, A.K., Rewers, M.J., Genetics of type 1 diabetes. Clin. Chem. 57 (2011), 176–185.
108. 108 Pette, M., et al. Myelin autoreactivity in multiple sclerosis: recognition of myelin basic protein in the context of HLA-DR2 products by T lymphocytes of multiple-sclerosis patients and healthy donors. Proc. Natl. Acad. Sci. U.S.A. 87 (1990), 7968–7972.
109. 109 Wan, X., et al. Class-switched anti-insulin antibodies originate from unconventional antigen presentation in multiple lymphoid sites. J. Exp. Med. 213 (2016), 967–978.
110. 110 Sinnathamby, G., Eisenlohr, L.C., Presentation by recycling MHC class II molecules of an influenza hemagglutinin-derived epitope that is revealed in the early endosome by acidification. J. Immunol. 170 (2003), 3504–3513.
111. 111 Tewari, M.K., et al. A cytosolic pathway for MHC class II-restricted antigen processing that is proteasome and TAP dependent. Nat. Immunol. 6 (2005), 287–294.
112. 112 van Luijn, M.M., et al. Alternative Ii-independent antigen-processing pathway in leukemic blasts involves TAP-dependent peptide loading of HLA class II complexes. Cancer Immunol. Immunother. 59 (2010), 1825–1838.
113. 113 Maric, M., et al. Defective antigen processing in GILT-free mice. Science 294 (2001), 1361–1365.
114. 114 Ziegler, H.K., Unanue, E.R., Decrease in macrophage antigen catabolism caused by ammonia and chloroquine is associated with inhibition of antigen presentation to T cells. Proc. Natl. Acad. Sci. U.S.A. 79 (1982), 175–178.
115. 115 Liljedahl, M., et al. HLA-DO is a lysosomal resident which requires association with HLA-DM for efficient intracellular transport. EMBO J. 15 (1996), 4817–4824.
116. 116 Denzin, L.K., et al. Negative regulation by HLA-DO of MHC class II-restricted antigen processing. Science 278 (1997), 106–109.
117. 117 van Ham, S.M., et al. HLA-DO is a negative modulator of HLA-DM-mediated MHC class II peptide loading. Curr. Biol. 7 (1997), 950–957.
118. 118 Yi, W., et al. Targeted regulation of self-peptide presentation prevents type I diabetes in mice without disrupting general immunocompetence. J. Clin. Invest. 120 (2010), 1324–1336.
119. 119 Cella, M., et al. Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature 388 (1997), 782–787.
120. 120 Pierre, P., et al. Developmental regulation of MHC class II transport in mouse dendritic cells. Nature 388 (1997), 787–792.
121. 121 Thibodeau, J., et al. Interleukin-10-induced MARCH1 mediates intracellular sequestration of MHC class II in monocytes. Eur. J. Immunol. 38 (2008), 1225–1230.
122. 122 Paul, P., et al. A genome-wide multidimensional RNAi screen reveals pathways controlling MHC class II antigen presentation. Cell 145 (2011), 268–283.
123. 123 Mitchell, E.K., et al. Inhibition of cell surface MHC class II expression by Salmonella. Eur. J. Immunol. 34 (2004), 2559–2567.
124. 124 Zwart, W., et al. Spatial separation of HLA-DM/HLA-DR interactions within MIIC and phagosome-induced immune escape. Immunity 22 (2005), 221–233.
125. 125 van Niel, G., et al. Dendritic cells regulate exposure of MHC class II at their plasma membrane by oligoubiquitination. Immunity 25 (2006), 885–894.
126. 126 Pennock, G.K., Chow, L.Q., The evolving role of immune checkpoint inhibitors in cancer treatment. Oncologist 20 (2015), 812–822.
127. 127 Schumacher, T.N., Schreiber, R.D., Neoantigens in cancer immunotherapy. Science 348 (2015), 69–74.
128. 128 Jongsma, M.L., et al. An ER-associated pathway defines endosomal architecture for controlled cargo transport. Cell 166 (2016), 152–166.
129. 129 Saveanu, L., et al. IRAP identifies an endosomal compartment required for MHC class I cross-presentation. Science 325 (2009), 213–217.