Proteasomes, TAP, and endoplasmic reticulum-associated aminopeptidase associated with antigen processing control CD4+ Th cell responses by regulating indirect presentation of MHC class II-restricted cytoplasmic antigens

Journal of Immunology

Volumn 186, Issue 12, 2011, Pages 6683-6692

  Dragovic, Srdjan M ^a   Hill, Timothy ^a   Christianson, Gregory J ^b   Kim, Sungjune ^a   Elliott, Tim ^c   Scott, Diane ^d   Roopenian, Derry C ^b   Van Kaer, Luc ^a   Joyce, Sebastian ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JACKSON LABORATORY   (United States)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^d HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOPEPTIDASE; BACTERIAL ANTIGEN; ENDOPLASMIC RETICULUM ASSOCIATED AMINOPEPTIDASE; HY ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEASOME; TAPASIN; UNCLASSIFIED DRUG;

ALLOGRAFT; ANIMAL CELL; ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; ANTIGENIC MODULATION; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOSOL; FEMALE; HELPER CELL; HUMAN; LISTERIA MONOCYTOGENES; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

AMINOPEPTIDASES; ANTIGEN PRESENTATION; ANTIGENS, BACTERIAL; ATP-BINDING CASSETTE TRANSPORTERS; CYTOPLASM; ENDOPLASMIC RETICULUM; HISTOCOMPATIBILITY ANTIGENS CLASS II; LISTERIA MONOCYTOGENES; PROTEASOME ENDOPEPTIDASE COMPLEX; T-LYMPHOCYTES, HELPER-INDUCER; TRANSPLANTATION, HOMOLOGOUS;

EID: 79959549901     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100525     Document Type: Article

References (74)

1. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
2. Reis e Sousa, C. 2004. Activation of dendritic cells: translating innate into adaptive immunity. Curr. Opin. Immunol. 16: 21-25.
3. Trombetta, E. S., and I. Mellman. 2005. Cell biology of antigen processing in vitro and in vivo. Annu. Rev. Immunol. 23: 975-1028.
4. Cresswell, P., A. L. Ackerman, A. Giodini, D. R. Peaper, and P. A. Wearsch. 2005. Mechanisms of MHC class I-restricted antigen processing and cross-presentation. Immunol. Rev. 207: 145-157.
5. Wilson, N. S., and J. A. Villadangos. 2005. Regulation of antigen presentation and cross-presentation in the dendritic cell network: facts, hypothesis, and immunological implications. Adv. Immunol. 86: 241-305.
6. Chen, Y., Y. Demir, A. Valujskikh, and P. S. Heeger. 2003. The male minor transplantation antigen preferentially activates recipient CD4+ T cells through the indirect presentation pathway in vivo. J. Immunol. 171: 6510-6518.
7. Théry, C., L. Duban, E. Segura, P. Véron, O. Lantz, and S. Amigorena. 2002. Indirect activation of naïve CD4+ T cells by dendritic cell-derived exosomes. Nat. Immunol. 3: 1156-1162.
8. Rüssmann, H., U. Gerdemann, E. I. Igwe, K. Panthel, J. Heesemann, S. Garbom, H. Wolf-Watz, and G. Geginat. 2003. Attenuated Yersinia pseudotuberculosis carrier vaccine for simultaneous antigen-specific CD4 and CD8 T-cell induction. Infect. Immun. 71: 3463-3472.
9. Valentino, M. D., L. L. Hensley, D. Skrombolas, P. L. McPherson, M. D. Woolard, T. H. Kawula, J. A. Frelinger, and J. G. Frelinger. 2009. Identification of a dominant CD4 T cell epitope in the membrane lipoprotein Tul4 from Francisella tularensis LVS. Mol. Immunol. 46: 1830-1838.
10. Matyszak, M. K., J. L. Young, and J. S. Gaston. 2002. Uptake and processing of Chlamydia trachomatis by human dendritic cells. Eur. J. Immunol. 32: 742-751.
11. Dissanayake, S. K., N. Tuera, and S. Ostrand-Rosenberg. 2005. Presentation of endogenously synthesized MHC class II-restricted epitopes by MHC class II cancer vaccines is independent of transporter associated with Ag processing and the proteasome. J. Immunol. 174: 1811-1819. (Pubitemid 40223920)
12. Nimmerjahn, F., S. Milosevic, U. Behrends, E. M. Jaffee, D. M. Pardoll, G. W. Bornkamm, and J. Mautner. 2003. Major histocompatibility complex class II-restricted presentation of a cytosolic antigen by autophagy. Eur. J. Immunol. 33: 1250-1259.
13. Paludan, C., D. Schmid, M. Landthaler, M. Vockerodt, D. Kube, T. Tuschl, and C. Münz. 2005. Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 307: 593-596. (Pubitemid 40165684)
14. Zhou, D., P. Li, Y. Lin, J. M. Lott, A. D. Hislop, D. H. Canaday, R. R. Brutkiewicz, and J. S. Blum. 2005. Lamp-2a facilitates MHC class II presentation of cytoplasmic antigens. Immunity 22: 571-581.
15. Jacobson, S., R. P. Sekaly, C. L. Jacobson, H. F. McFarland, and E. O. Long. 1989. HLA class II-restricted presentation of cytoplasmic measles virus antigens to cytotoxic T cells. J. Virol. 63: 1756-1762.
16. Jaraquemada, D., M. Marti, and E. O. Long. 1990. An endogenous processing pathway in vaccinia virus-infected cells for presentation of cytoplasmic antigens to class II-restricted T cells. J. Exp. Med. 172: 947-954.
17. Wang, R. F., X. Wang, A. C. Atwood, S. L. Topalian, and S. A. Rosenberg. 1999. Cloning genes encoding MHC class II-restricted antigens: mutated CDC27 as a tumor antigen. Science 284: 1351-1354.
18. Brooks, A., S. Hartley, L. Kjer-Nielsen, J. Perera, C. C. Goodnow, A. Basten, and J. McCluskey. 1991. Class II-restricted presentation of an endogenously derived immunodominant T-cell determinant of hen egg lysozyme. Proc. Natl. Acad. Sci. USA 88: 3290-3294.
19. Chicz, R. M., R. G. Urban, J. C. Gorga, D. A. Vignali, W. S. Lane, and J. L. Strominger. 1993. Specificity and promiscuity among naturally processed peptides bound to HLA-DR alleles. J. Exp. Med. 178: 27-47.
20. Dongre, A. R., S. Kovats, P. deRoos, A. L. McCormack, T. Nakagawa, V. Paharkova-Vatchkova, J. Eng, H. Caldwell, J. R. Yates, III, and A. Y. Rudensky. 2001. In vivo MHC class II presentation of cytosolic proteins revealed by rapid automated tandem mass spectrometry and functional analyses. Eur. J. Immunol. 31: 1485-1494.
21. Rudensky AYu, P., S. C. Preston-Hurlburt, A. Hong, Barlow, and C. A. Janeway, Jr. 1991. Sequence analysis of peptides bound to MHC class II molecules. Nature 353: 622-627.
22. Bird, P. I., J. A. Trapani, and J. A. Villadangos. 2009. Endolysosomal proteases and their inhibitors in immunity. Nat. Rev. Immunol. 9: 871-882.
23. Lee, H. K., L. M. Mattei, B. E. Steinberg, P. Alberts, Y. H. Lee, A. Chervonsky, N. Mizushima, S. Grinstein, and A. Iwasaki. 2010. In vivo requirement for Atg5 in antigen presentation by dendritic cells. Immunity 32: 227-239.
24. Michalek, M. T., B. Benacerraf, and K. L. Rock. 1992. The class II MHC-restricted presentation of endogenously synthesized ovalbumin displays clonal variation, requires endosomal/lysosomal processing, and is up-regulated by heat shock. J. Immunol. 148: 1016-1024.
25. Reed, A. J., H. Noorchashm, S. Y. Rostami, Y. Zarrabi, A. R. Perate, A. N. Jeganathan, A. J. Caton, and A. Naji. 2003. Alloreactive CD4 T cell activation in vivo: an autonomous function of the indirect pathway of alloantigen presentation. J. Immunol. 171: 6502-6509. (Pubitemid 37532079)
26. Richards, D. M., S. L. Dalheimer, B. D. Ehst, T. L. Vanasek, M. K. Jenkins, M. I. Hertz, and D. L. Mueller. 2004. Indirect minor histocompatibility antigen presentation by allograft recipient cells in the draining lymph node leads to the activation and clonal expansion of CD4+ T cells that cause obliterative airways disease. J. Immunol. 172: 3469-3479.
27. Hammer, G. E., F. Gonzalez, M. Champsaur, D. Cado, and N. Shastri. 2006. The aminopeptidase ERAAP shapes the peptide repertoire displayed by major histocompatibility complex class I molecules. Nat. Immunol. 7: 103-112.
28. Hammer, G. E., F. Gonzalez, E. James, H. Nolla, and N. Shastri. 2007. In the absence of aminopeptidase ERAAP, MHC class I molecules present many unstable and highly immunogenic peptides. Nat. Immunol. 8: 101-108.
29. Yan, J., V. V. Parekh, Y. Mendez-Fernandez, D. Olivares- Villagómez, S. Dragovic, T. Hill, D. C. Roopenian, S. Joyce, and L. Van Kaer. 2006. In vivo role of ER-associated peptidase activity in tailoring peptides for presentation by MHC class Ia and class Ib molecules. J. Exp. Med. 203: 647-659.
30. York, I. A., M. A. Brehm, S. Zendzian, C. F. Towne, and K. L. Rock. 2006. Endoplasmic reticulum aminopeptidase 1 (ERAP1) trims MHC class I-presented peptides in vivo and plays an important role in immunodominance. Proc. Natl. Acad. Sci. USA 103: 9202-9207.
31. Lich, J. D., J. F. Elliott, and J. S. Blum. 2000. Cytoplasmic processing is a prerequisite for presentation of an endogenous antigen by major histocompatibility complex class II proteins. J. Exp. Med. 191: 1513-1524.
32. Tewari, M. K., G. Sinnathamby, D. Rajagopal, and L. C. Eisenlohr. 2005. A cytosolic pathway for MHC class II-restricted antigen processing that is proteasome and TAP dependent. Nat. Immunol. 6: 287-294.
33. Mukherjee, P., A. Dani, S. Bhatia, N. Singh, A. Y. Rudensky, A. George, V. Bal, S. Mayor, and S. Rath. 2001. Efficient presentation of both cytosolic and endogenous transmembrane protein antigens on MHC class II is dependent on cytoplasmic proteolysis. J. Immunol. 167: 2632-2641. (Pubitemid 32768892)
34. Testa, J. S., G. S. Apcher, J. D. Comber, and L. C. Eisenlohr. 2010. Exosome-driven antigen transfer for MHC class II presentation facilitated by the receptor binding activity of influenza hemagglutinin. J. Immunol. 185: 6608-6616.
35. Malnati, M. S., M. Marti, T. LaVaute, D. Jaraquemada, W. Biddison, R. DeMars, and E. O. Long. 1992. Processing pathways for presentation of cytosolic antigen to MHC class II-restricted T cells. Nature 357: 702-704.
36. Dani, A., A. Chaudhry, P. Mukherjee, D. Rajagopal, S. Bhatia, A. George, V. Bal, S. Rath, and S. Mayor. 2004. The pathway for MHCII-mediated presentation of endogenous proteins involves peptide transport to the endo-lysosomal compartment. J. Cell Sci. 117: 4219-4230. (Pubitemid 39328309)
37. Guéguen, M., and E. O. Long. 1996. Presentation of a cytosolic antigen by major histocompatibility complex class II molecules requires a long-lived form of the antigen. Proc. Natl. Acad. Sci. USA 93: 14692-14697.
38. Oxenius, A., M. F. Bachmann, P. G. Ashton-Rickardt, S. Tonegawa, R. M. Zinkernagel, and H. Hengartner. 1995. Presentation of endogenous viral proteins in association with major histocompatibility complex class II: on the role of intracellular compartmentalization, invariant chain and the TAP transporter system. Eur. J. Immunol. 25: 3402-3411.
39. Loss, G. E., Jr., C. G. Elias, P. E. Fields, R. K. Ribaudo, M. McKisic, and A. J. Sant. 1993. Major histocompatibility complex class II-restricted presentation of an internally synthesized antigen displays cell-type variability and segregates from the exogenous class II and endogenous class I presentation pathways. J. Exp. Med. 178: 73-85.
40. Heath, W. R., and F. R. Carbone. 2001. Cross-presentation, dendritic cells, tolerance and immunity. Annu. Rev. Immunol. 19: 47-64.
41. Gao, B., R. Adhikari, M. Howarth, K. Nakamura, M. C. Gold, A. B. Hill, R. Knee, M. Michalak, and T. Elliott. 2002. Assembly and antigen-presenting function of MHC class I molecules in cells lacking the ER chaperone calreticulin. Immunity 16: 99-109. (Pubitemid 34143220)
42. Xiao, X., X. Zuo, A. A. Davis, D. R. McMillan, B. B. Curry, J. A. Richardson, and I. J. Benjamin. 1999. HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J. 18: 5943-5952.
43. Scott, D., C. Addey, P. Ellis, E. James, M. J. Mitchell, N. Saut, S. Jurcevic, and E. Simpson. 2000. Dendritic cells permit identification of genes encoding MHC class II-restricted epitopes of transplantation antigens. Immunity 12: 711-720.
44. Yoshimura, Y., R. Yadav, G. J. Christianson, W. U. Ajayi, D. C. Roopenian, and S. Joyce. 2004. Duration of alloantigen presentation and avidity of T cell antigen recognition correlate with immunodominance of CTL response to minor histocompatibility antigens. J. Immunol. 172: 6666-6674. (Pubitemid 38669102)
45. Bezbradica, J. S., A. K. Stanic, N. Matsuki, H. Bour-Jordan, J. A. Bluestone, J. W. Thomas, D. Unutmaz, L. Van Kaer, and S. Joyce. 2005. Distinct roles of dendritic cells and B cells in Va14Ja18 natural T cell activation in vivo. J. Immunol. 174: 4696-4705.
46. Spencer, C. T., P. Gilchuk, S. M. Dragovic, and S. Joyce. 2010. Minor histocompatibility antigens: presentation principles, recognition logic and the potential for a healing hand. Curr. Opin. Organ Transplant. 15: 512-525.
47. Mazeyrat, S., N. Saut, C. A. Sargent, S. Grimmond, G. Longepied, I. E. Ehrmann, P. S. Ellis, A. Greenfield, N. A. Affara, and M. J. Mitchell. 1998. The mouse Y chromosome interval necessary for spermatogonial proliferation is gene dense with syntenic homology to the human AZFa region. Hum. Mol. Genet. 7: 1713-1724.
48. Jung, S., D. Unutmaz, P. Wong, G. Sano, K. De los Santos, T. Sparwasser, S. Wu, S. Vuthoori, K. Ko, F. Zavala, et al. 2002. In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens. Immunity 17: 211-220.
49. Aoshi, T., B. H. Zinselmeyer, V. Konjufca, J. N. Lynch, X. Zhang, Y. Koide, and M. J. Miller. 2008. Bacterial entry to the splenic white pulp initiates antigen presentation to CD8+ T cells. Immunity 29: 476-486.
50. Hildner, K., B. T. Edelson, W. E. Purtha, M. Diamond, H. Matsushita, M. Kohyama, B. Calderon, B. U. Schraml, E. R. Unanue, M. S. Diamond, et al. 2008. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 322: 1097-1100.
51. Skoberne, M., S. Schenk, H. Hof, and G. Geginat. 2002. Cross-presentation of Listeria monocytogenes-derived CD4 T cell epitopes. J. Immunol. 169: 1410-1418. (Pubitemid 34809186)
52. Lara-Tejero, M., and E. G. Pamer. 2004. T cell responses to Listeria monocytogenes. Curr. Opin. Microbiol. 7: 45-50.
53. Geginat, G., S. Schenk, M. Skoberne, W. Goebel, and H. Hof. 2001. A novel approach of direct ex vivo epitope mapping identifies dominant and subdominant CD4 and CD8 T cell epitopes from Listeria monocytogenes. J. Immunol. 166:1877-1884. (Pubitemid 32114674)
54. Tourne, S., H. M. van Santen, M. van Roon, A. Berns, C. Benoist, D. Mathis, and H. Ploegh. 1996. Biosynthesis of major histocompatibility complex molecules and generation of T cells in Ii TAP1 double-mutant mice. Proc. Natl. Acad. Sci. USA 93: 1464-1469.
55. Kroeger, H., E. Miranda, I. MacLeod, J. Pérez, D. C. Crowther, S. J. Marciniak, and D. A. Lomas. 2009. Endoplasmic reticulum-associated degradation (ERAD) and autophagy cooperate to degrade polymerogenic mutant serpins. J. Biol. Chem. 284: 22793-22802.
56. Mylin, L. M., T. D. Schell, D. Roberts, M. Epler, A. Boesteanu, E. J. Collins, J. A. Frelinger, S. Joyce, and S. S. Tevethia. 2000. Quantitation of CD8(+) T-lymphocyte responses to multiple epitopes from simian virus 40 (SV40) large T antigen in C57BL/6 mice immunized with SV40, SV40 T-antigen-transformed cells, or vaccinia virus recombinants expressing full-length T antigen or epitope minigenes. J. Virol. 74: 6922-6934.
57. Meng, L., R. Mohan, B. H. Kwok, M. Elofsson, N. Sin, and C. M. Crews. 1999. Epoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo anti-inflammatory activity. Proc. Natl. Acad. Sci. USA 96: 10403-10408.
58. Schwarz, K., R. de Giuli, G. Schmidtke, S. Kostka, M. van den Broek, K. B. Kim, C. M. Crews, R. Kraft, and M. Groettrup. 2000. The selective proteasome inhibitors lactacystin and epoxomicin can be used to either up- or downregulate antigen presentation at nontoxic doses. J. Immunol. 164: 6147-6157. (Pubitemid 30408791)
59. Lev, A., K. Takeda, D. Zanker, J. C. Maynard, P. Dimberu, E. Waffarn, J. Gibbs, N. Netzer, M. F. Princiotta, L. Neckers, et al. 2008. The exception that reinforces the rule: crosspriming by cytosolic peptides that escape degradation. Immunity 28: 787-798. (Pubitemid 351778406)
60. Srivastava, P. 2002. Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annu. Rev. Immunol. 20: 395-425.
61. Berwin, B., J. P. Hart, S. Rice, C. Gass, S. V. Pizzo, S. R. Post, and C. V. Nicchitta. 2003. Scavenger receptor-A mediates gp96/GRP94 and calreticulin internalization by antigen-presenting cells. EMBO J. 22: 6127-6136.
62. de la Salle, H., D. Hanau, D. Fricker, A. Urlacher, A. Kelly, J. Salamero, S. H. Powis, L. Donato, H. Bausinger, M. Laforet, et al. 1994. Homozygous human TAP peptide transporter mutation in HLA class I deficiency. Science 265: 237-241. (Pubitemid 24259925)
63. Matamoros, N., J. Milà, M. Llano, A. Balas, J. L. Vicario, J. Pons, C. Crespí, N. Martinez, J. Iglesias-Alzueta, and M. López-Botet. 2001. Molecular studies and NK cell function of a new case of TAP2 homozygous human deficiency. Clin. Exp. Immunol. 125: 274-282.
64. Andrés, A. M., M. Y. Dennis, W. W. Kretzschmar, J. L. Cannons, S. Q. Lee-Lin, B. Hurle, P. L. Schwartzberg, S. H. Williamson, C. D. Bustamante, R. Nielsen, et al; NISC Comparative Sequencing Program. 2010. Balancing selection maintains a form of ERAP2 that undergoes nonsense-mediated decay and affects antigen presentation. PLoS Genet. 6: e1001157.
65. Ljunggren, H. G., L. Van Kaer, H. L. Ploegh, and S. Tonegawa. 1994. Altered natural killer cell repertoire in Tap-1 mutant mice. Proc. Natl. Acad. Sci. USA 91: 6520-6524.
66. Goldszmid, R. S., A. Bafica, D. Jankovic, C. G. Feng, P. Caspar, R. Winkler-Pickett, G. Trinchieri, and A. Sher. 2007. TAP-1 indirectly regulates CD4+ T cell priming in Toxoplasma gondii infection by controlling NK cell IFN-gamma production. J. Exp. Med. 204: 2591-2602.
67. Raposo, G., H. M. van Santen, R. Leijendekker, H. J. Geuze, and H. L. Ploegh. 1995. Misfolded major histocompatibility complex class I molecules accumulate in an expanded ER-Golgi intermediate compartment. J. Cell Biol. 131: 1403-1419.
68. Ackerman, A. L., A. Giodini, and P. Cresswell. 2006. A role for the endoplasmic reticulum protein retrotranslocation machinery during crosspresentation by dendritic cells. Immunity 25: 607-617. (Pubitemid 44529035)
69. Singh, R., A. Jamieson, and P. Cresswell. 2008. GILT is a critical host factor for Listeria monocytogenes infection. Nature 455: 1244-1247.
70. Singh, R., and P. Cresswell. 2010. Defective cross-presentation of viral antigens in GILT-free mice. Science 328: 1394-1398.
71. Chen, W., C. C. Norbury, Y. Cho, J. W. Yewdell, and J. R. Bennink. 2001. Immunoproteasomes shape immunodominance hierarchies of antiviral CD8(+) T cells at the levels of T cell repertoire and presentation of viral antigens. J. Exp. Med. 193: 1319-1326.
72. Hensley, S. E., D. Zanker, B. P. Dolan, A. David, H. D. Hickman, A. C. Embry, C. N. Skon, K. M. Grebe, T. A. Griffin, W. Chen, et al. 2010. Unexpected role for the immunoproteasome subunit LMP2 in antiviral humoral and innate immune responses. J. Immunol. 184: 4115-4122.
73. Gardai, S. J., K. A. McPhillips, S. C. Frasch, W. J. Janssen, A. Starefeldt, J. E. Murphy-Ullrich, D. L. Bratton, P. A. Oldenborg, M. Michalak, and P. M. Henson. 2005. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123: 321-334.
74. Obeid, M., A. Tesniere, F. Ghiringhelli, G. M. Fimia, L. Apetoh, J. L. Perfettini, M. Castedo, G. Mignot, T. Panaretakis, N. Casares, et al. 2007. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 13: 54-61.