Targeting proteins to distinct subcellular compartments reveals unique requirements for MHC class I and II presentation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 41, 2009, Pages 17463-17468

  Belizaire, Roger ^a   Unanue, Emil R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cross presentation; Endosome; Liposomes

Indexed keywords

BREFELDIN A; CATHEPSIN S INHIBITOR; CD4 ANTIGEN; CD8 ANTIGEN; CHLOROQUINE; DEXTRAN DERIVATIVE; EGG WHITE; INTERLEUKIN 2; LIPOSOME; LYSOZYME; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEASOME; PROTEASOME INHIBITOR; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1;

ACIDIFICATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTATION; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; CROSS PRESENTATION; DENDRITIC CELL; ENCAPSULATION; ENDOSOME; ENZYME ACTIVITY; ENZYME STRUCTURE; HEN; HYBRIDOMA; MACROPHAGE; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN TARGETING; SOLUBILITY;

ANIMALS; BREFELDIN A; CHICKENS; CHLOROQUINE; DENDRITIC CELLS; ENDOCYTOSIS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; LIPOSOMES; MACROPHAGES; MICE; MICE, INBRED NOD; MURAMIDASE;

EID: 70350434312     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0908583106     Document Type: Article

References (48)

1. Trombetta ES, Mellman I (2005) Cell biology of antigen processing in vitro and in vivo. Annu Rev Immunol 23:975-1028. (Pubitemid 40563191)
2. Lindner R, Unanue ER (1996) Distinct antigen MHC class II complexes generated by separate processing pathways. EMBO J 15:6910-6920. (Pubitemid 27023262)
3. Griffin JP, Chu R, Harding CV (1997) Early endosomes and a late endocytic compartment generate different peptide-class II MHC complexes via distinct processing mechanisms. J Immunol 158:1523-1532. (Pubitemid 127469504)
4. Cresswell P, Ackerman AL, Giodini A, Peaper DR, Wearsch PA (2005) Mechanisms of MHC class I-restricted antigen processing and cross-presentation. Immunol Rev 207:145-157. (Pubitemid 41415014)
5. Shen LJ, Sigal LJ, Boes M, Rock KL (2004) Important role of cathepsin S in generating peptides for TAP-independent MHC class I crosspresentation in vivo. Immunity 21:155-165. (Pubitemid 39094046)
6. Burgdorf S, Scholz C, Kautz A, Tampe R, Kurts C (2008) Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nat Immunol 9:558-566. (Pubitemid 351560525)
7. Kovacsovics-Bankowski M, Rock KL (1995) A phagosome-to-cytosol pathway for exogenous antigens presented on MHC class I molecules. Science 267:243-246.
8. Rodriguez A, Regnault A, Kleijmeer M, Ricciardi-Castagnoli P, Amigorena S (1999) Selective transport of internalized antigens to the cytosol for MHC class I presentation in dendritic cells. Nat Cell Biol 1:362-368. (Pubitemid 129493579)
9. Houde M, et al. (2003) Phagosomes are competent organelles for antigen cross-presentation. Nature 425:402-406. (Pubitemid 37187269)
10. Ackerman AL, Kyritsis C, Tampe R, Cresswell P (2003) Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens. Proc Natl Acad Sci USA 100:12889-12894. (Pubitemid 37339995)
11. Pfeifer JD, et al. (1993) Phagocytic processing of bacterial antigens for class I MHC presentation to T cells. Nature 361:359-362. (Pubitemid 23041629)
12. Groothuis TAM, Neefjes J (2005) The many roads to cross-presentation. J Exp Med 202:1313-1318.
13. Harding CV, Collins DS, Slot JW, Geuze HJ, Unanue ER (1991) Liposome-encapsulated antigens are processed in lysosomes, recycled, and presented to T cells. Cell 64:393-401.
14. Harding CV, Collins DS, Kanagawa O, Unanue ER (1991) Liposome- encapsulated antigens engender lysosomal processing for class II MHC presentation and cytosolic processing for class I presentation. J Immunol 147:2860-2863.
15. Seifert U, et al. (2003) An essential role for tripeptidyl peptidase in the generation of an MHC class I epitope. Nat Immunol 4:375-379. (Pubitemid 36432321)
16. -/- macrophages are deficient in vacuolar alternate class IMHC (MHC-I) processing due to decreased MHC-I stability at phagolysosomal pH. J Immunol 170:5825-5833.
17. Rammensee HG, Bachmann J, Emmerich NPN, Bachor OA, Stevanovic S (1999) SYFPEITHI: Database for MHC ligands and peptide motifs. Immunogenetics 50:213-219. (Pubitemid 30099526)
18. Ziegler HK, Unanue ER (1982) Decrease in macrophage antigen catabolism caused by ammonia and chloroquine is associated with inhibition of antigen presentation to T cells. Proc Natl Acad Sci USA 79:175-178.
19. Schirmbeck R, Melber K, Reimann J (1995) Hepatitis B virus small surface antigen particles are processed in a novel endosomal pathway for major histocompatibility complex class I-restricted epitope presentation. Eur J Immunol 25:1063-1070.
20. Rock KL, Shen L (2005) Cross-presentation: Underlying mechanisms and role in immune surveillance. Immunol Rev 207:166-183. (Pubitemid 41415016)
21. Klausner RD, Donaldson JG, Lippincott-Schwartz J (1992) Brefeldin A: Insights into the control of membrane traffic and organelle structure. J Cell Biol 116:1071-1080.
22. Radhakrishna H, Donaldson JG (1997) ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J Cell Biol 139:49-61. (Pubitemid 27444080)
23. Lehner PJ, Hoer S, Dodd R, Duncan LM (2005) Downregulation of cell surface receptors by the K3 family of viral and cellular ubiquitin E3 ligases. Immunol Rev 207:112-125. (Pubitemid 41415012)
24. Wang ZQ, et al. (2008) Activation of CXCR4 triggers ubiquitination and down-regulation of major histocompatibility complex class I (MHC-I) on epithelioid carcinoma HeLa cells. J Biol Chem 283:3951-3959.
25. Lorenzo ME, Jung JU, Ploegh HL (2002) Kaposi's sarcoma-associated herpesvirus K3 utilizes the ubiquitin-proteasome system in routing class I major histocompatibility complexes to late endocytic compartments. J Virol 76:5522-5531.
26. Savina A, et al. (2006) NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 126:205-218. (Pubitemid 44026552)
27. + T cells by a transporter associated with antigen processing-independent pathway in vitro and in vivo. J Immunol 177:3525-3533.
28. Di Pucchio T, et al. (2008) Direct proteasome-independent cross-presentation of viral antigen by plasmacytoid dendritic cells on major histocompatibility complex class I. Nat Immunol 9:551-557. (Pubitemid 351560524)
29. Lopez D, Del Val M (1997) Cutting edge: Selective involvement of proteasomes and cysteine proteases in MHC class I antigen presentation. J Immunol 159:5769-5772. (Pubitemid 127471508)
30. Campbell DJ, Serwold T, Shastri N (2000) Bacterial proteins can be processed by macrophages in a transporter associated with antigen processing-independent, cysteine protease-dependent manner for presentation by MHC class I molecules. J Immunol 164:168-175. (Pubitemid 30012987)
31. Lennon-Dumenil AM, et al. (2002) Analysis of protease activity in live antigen-presenting cells shows regulation of the phagosomal proteolytic contents during dendritic cell activation. J Exp Med 196:529-539.
32. Kirschke H, Wiederanders B, Bromme D, Rinne A (1989) Cathepsin S from bovine spleen: Purification, distribution, intracellular localization and action on proteins. Biochem J 264:467-473. (Pubitemid 20024516)
33. Lutzner N, Kalbacher H (2008) Quantifying cathepsin S activity in antigen presenting cells using a novel specific substrate. J Biol Chem 283:36185-36194.
34. Burgdorf S, Kautz A, Bohnert V, Knolle PA, Kurts C (2007) Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316:612-616. (Pubitemid 46683149)
35. Gorbenko GP, Ioffe VM, Kinnunen PKJ (2007) Binding of lysozyme to phospholipid bilayers: Evidence for protein aggregation upon membrane association. Biophys J 93:140-153.
36. Lemansky P, Hasilik A (2001) Chondroitin sulfate is involved in lysosomal transport of lysozyme in U937 cells. J Cell Sci 114:345-352. (Pubitemid 32149576)
37. Lovitch SB, Unanue ER (2005) Conformational isomers of a peptide-class II major histocompatibility complex. Immunol Rev 207:293-313. (Pubitemid 41415025)
38. Heath WR, et al. (2004) Cross-presentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol Rev 199:9-26. (Pubitemid 38736761)
39. + dendritic cells in cytotoxic T cell immunity. Science 322:1097-1100.
40. Bonifaz L, et al. (2002) Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J Exp Med 196:1627-1638. (Pubitemid 36026474)
41. Sancho D, et al. (2008) Tumor therapy in mice via antigen targeting to a novel, DC-restricted C-type lectin. J Clin Invest 118:2098-2110. (Pubitemid 351872329)
42. Lin ML, Zhan YF, Villadangos JA, Lew AM (2008) The cell biology of cross-presentation and the role of dendritic cell subsets. Immunol Cell Biol 86:353-362. (Pubitemid 351667998)
43. Pozzi LAM, Maciaszek JW, Rock KL (2005) Both dendritic cells and macrophages can stimulate naive CD8 T cells in vivo to proliferate, develop effector function, and differentiate into memory cells. J Immunol 175:2071-2081.
44. Yates RM, Hermetter A, Taylor GA, Russell DG (2007) Macrophage activation downregulates the degradative capacity of the phagosome. Traffic 8:241-250. (Pubitemid 46656515)
45. Trost M, et al. (2009) The phagosomal proteome in interferon-γ- activated macrophages. Immunity 30:143-154.
46. Giodini A, Rahner C, Cresswell P (2009) Receptor-mediated phagocytosis elicits crosspresentation in nonprofessional antigen-presenting cells. Proc Natl Acad Sci USA 106:3324-3329.
47. Pu Z, Lovitch SB, Bikoff EK, Unanue ER (2004) T cells distinguish MHC-peptide complexes formed in separate vesicles and edited by H2-DM. Immunity 20:467-476. (Pubitemid 38482124)
48. Velazquez C, Vidavsky I, van der Drift K, Gross ML, Unanue ER (2002) Chemical identification of a low abundance lysozyme peptide family bound to I-Ak histocompatibility molecules. J Biol Chem 277:42514-42522. (Pubitemid 35285618)