Traffic of proteins and peptides across membranes for immunosurveillance by CD8+ T lymphocytes: A topological challenge

Traffic

Volumn 8, Issue 11, 2007, Pages 1486-1494

  Johnstone, Carolina ^a   Del Val, Margarita ^a,b  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Antigen processing and presentation; Cytotoxic CD81+ T lymphocytes; Peptide; Transporter

Indexed keywords

CARRIER PROTEIN; CELL PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEIN TAP; SECRETORY PROTEIN; TRANSLOCON; UNCLASSIFIED DRUG;

ANTIGEN PRESENTATION; CD8+ T LYMPHOCYTE; CROSS PRESENTATION; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; HUMAN; IMMUNOSURVEILLANCE; MEMBRANE TRANSPORT; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS; BIOLOGICAL TRANSPORT; CD8-POSITIVE T-LYMPHOCYTES; CYTOSOL; ENDOPLASMIC RETICULUM; HUMANS; IMMUNE SYSTEM; LIGANDS; MAJOR HISTOCOMPATIBILITY COMPLEX; MODELS, BIOLOGICAL; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; PROTEINS; T-LYMPHOCYTES;

EID: 35348926889     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2007.00635.x     Document Type: Review

References (82)

1. López D, Del Val M. Selective involvement of proteasomes and cysteine proteases in MHC class I antigen presentation. J Immunol 1997; 159: 5769-5772.
2. Seifert U, Marañón C, Shmueli A, Desoutter JF, Wesoloski L, Janek K, Henklein P, Diescher S, Andrieu M, de la Salle H, Weinschenk T, Schild H, Laderach D, Galy A, Haas G et al. An essential role for tripeptidyl peptidase in the generation of an MHC class I epitope. Nat Immunol 2003; 4: 375-379.
3. Guil S, Rodríguez-Castro M, Aguilar F, Villasevil EM, Antón LC, Del Val M. Need for tripeptidyl-peptidase II in major histocompatibility complex class I viral antigen processing when proteasomes are detrimental. J Biol Chem 2006; 281: 39925-39934.
4. York IA, Mo AXY, Lemerise K, Zeng WY, Shen YL, Abraham CR, Saric T, Goldberg AL, Rock KL. The cytosolic endopeptidase, thimet oligopeptidase, destroys antigenic peptides and limits the extent of MHC class I antigen presentation. Immunity 2003; 18: 429-440.
5. Lévy F, Burri L, Morel S, Peitrequin AL, Lévy N, Bachi A, Hellman U, Van den Eynde BJ, Servis C. The final N-terminal trimming of a subaminoterminal proline-containing HLA class I-restricted antigenic peptide in the cytosol is mediated by two peptidases. J Immunol 2002; 169: 4161-4171.
6. Reits E, Neijssen J, Herberts C, Benckhuijsen W, Janssen L, Drijfhout JW, Neefjes J. A major role for TPPII in trimming proteasomal degradation products for MHC class I antigen presentation. Immunity 2004; 20: 495-506.
7. York IA, Bhutani N, Zendzian S, Goldberg AL, Rock KL. Tripeptidyl peptidase II is the major peptidase needed to trim long antigenic precursors, but is not required for most MHC class I antigen presentation. J Immunol 2006; 177: 1434-1443.
8. Reits E, Griekspoor A, Neijssen J, Groothuis T, Jalink K, van Veelen P, Janssen H, Calafat J, Drijfhout JW, Neefjes J. Peptide diffusion, protection, and degradation in nuclear and cytoplasmic compartments before antigen presentation by MHC class I. Immunity 2003; 18: 97-108.
9. Neefjes JJ, Momburg F, Hämmerling GJ. Selective and ATP-dependent translocation of peptides by the MHC-encoded transporter. Science 1993; 261: 769-771.
10. Shepherd JC, Schumacher TN, Ashton-Rickardt PG, Imaeda S, Ploegh HL, Janeway CA Jr, Tonegawa S. TAP1-dependent peptide translocation in vitro is ATP dependent and peptide selective. Cell 1993; 74: 577-584.
11. van Endert PM, TampéR, Meyer TH, Tisch R, Bach JF, McDevitt HO. A sequential model for peptide binding and transport by the transporters associated with antigen processing. Immunity 1994; 1: 491-500.
12. Koopmann JO, Post M, Neefjes JJ, Hämmerling GJ, Momburg F. Translocation of long peptides by transporters associated with antigen processing (TAP). Eur J Immunol 1996; 26: 1720-1728.
13. Andersen MH, Bonfill JE, Neisig A, Arsequell G, Søndergaard I, Neefjes J, Zeuthen J, Elliott T, Haurum JS. Phosphorylated peptides can be transported by TAP molecules, presented by class I MHC molecules, and recognized by phosphopeptide-specific CTL. J Immunol 1999; 163: 3812-3818.
14. Haurum JS, Høier IB, Arsequell G, Neisig A, Valencia G, Zeuthen J, Neefjes J, Elliott T. Presentation of cytosolic glycosylated peptides by human class I major histocompatibility complex molecules in vivo. J Exp Med 1999; 190: 145-150.
15. van Endert PM, Riganelli D, Greco G, Fleischhauer K, Sidney J, Sette A, Bach JF. The peptide-binding motif for the human transporter associated with antigen processing. J Exp Med 1995; 182: 1883-1895.
16. Peters B, Bulik S, Tampe R, van Endert PM, Holzhütter HG. Identifying MHC class I epitopes by predicting the TAP transport efficiency of epitope precursors. J Immunol 2003; 171: 1741-1749.
17. Serwold T, González F, Kim J, Jacob R, Shastri N. ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 2002; 419: 480-483.
18. York IA, Chang SC, Saric T, Keys JA, Favreau JM, Goldberg AL, Rock KL. The ER aminopeptidase ERAP1 enhances or limits antigen presentation by trimming epitopes to 8-9 residues. Nat Immunol 2002; 3: 1177-1184.
19. Tanioka T, Hattori A, Masuda S, Nomura Y, Nakayama H, Mizutani S, Tsujimoto M. Human leukocyte-derived arginine aminopeptidase - the third member of the oxytocinase subfamily of aminopeptidases. J Biol Chem 2003; 278: 32275-32283.
20. Saveanu L, Carroll O, Lindo V, Del Val M, López D, Lepelletier Y, Greer F, Schomburg L, Fruci D, Niedermann G, van Endert PM. Concerted peptide trimming by human ERAP1 and ERAP2 aminopeptidase complexes in the endoplasmic reticulum. Nat Immunol 2005; 6: 689-697.
21. Day PM, Esquivel F, Lukszo J, Bennink JR, Yewdell JW. Effect of TAP on the generation and intracellular trafficking of peptide-receptive major histocompatibility complex class I molecules. Immunity 1995; 2: 137-147.
22. Sijts AJAM, Pamer EG. Enhaced intracellular dissociation of major histocompatibility complex class I-associated peptides: A mechanism for optimizing the spectrum of cell surface-presented cytotoxic T lymphocyte epitopes. J Exp Med 1997; 185: 1403-1411.
23. Paulsson KM, Kleijmeer MJ, Griffith J, Jevon M, Chen S, Anderson PO, Sjogren HO, Li S, Wang P. Association of tapasin and COPI provides a mechanism for the retrograde transport of major histocompatibility complex (MHC) class I molecules from the Golgi complex to the endoplasmic reticulum. J Biol Chem 2002; 277: 18266-18271.
24. Lippincott-Schwartz J, Donaldson JG, Schweizer A, Berger EG, Hauri HP, Yuan LC, Klausner RD. Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell 1990; 60: 821-836.
25. Johnson AE, van Waes MA. The translocon: A dynamic gateway at the ER membrane. Annu Rev Cell Dev Biol 1999; 15: 799-842.
26. Wei ML, Cresswell P. HLA-A2 molecules in an antigen-processing mutant cell contain signal sequence-derived peptides. Nature 1992; 356: 443-446.
27. Henderson RA, Michel H, Sakaguchi K, Shabanowitz J, Appella E, Hunt DF, Engelhard VH. HLA-A2.1-associated peptides from a mutant cell line: A second pathway of antigen presentation. Science 1992; 255: 1264-1266.
28. Gil-Torregrosa BC, Castaño AR, Del Val M. Major histocompatibility complex class I viral antigen processing in the secretory pathway defined by the trans - Golgi network protease furin. J Exp Med 1998; 188: 1105-1116.
29. Gil-Torregrosa BC, Castaño AR, López D, Del Val M. Generation of MHC class I peptide antigens by protein processing in the secretory route by furin. Traffic 2000; 1: 641-651.
30. Tiwari N, Garbi N, Reinheckel T, Moldenhauer G, Hammerling GJ, Momburg F. A transporter associated with antigen-processing independent vacuolar pathway for the MHC class I-mediated presentation of endogenous transmembrane proteins. J Immunol 2007; 178: 7932-7942.
31. + T cells. Nature 1993; 364: 158-161.
32. + CTL. J Immunol 1995; 154: 6140-6156.
33. Elliott T, Willis A, Cerundolo V, Townsend A. Processing of major histocompatibility class I-restricted antigens in the endoplasmic reticulum. J Exp Med 1995; 181: 1481-1491.
34. Snyder HL, Bacík I, Bennink JR, Kearns G, Behrens TW, Bächi T, Orlowski M, Yewdell JW. Two novel routes of transporter associated with antigen processing (TAP)-independent major histocompatibility complex class I antigen processing. J Exp Med 1997; 186: 1087-1098.
35. Snyder HL, Bacík I, Yewdell JW, Behrens TW, Bennink JR. Promiscuous liberation of MHC-class I-binding peptides from the C termini of membrane and soluble proteins in the secretory pathway. Eur J Immunol 1998; 28: 1339-1346.
36. Wood P, Elliott T. Glycan-regulated antigen processing of a protein in the endoplasmic reticulum can uncover cryptic cytotoxic T cell epitopes. J Exp Med 1998; 188: 773-778.
37. + T cell recognition reveals a proteasome-dependent, transporter associated with antigen processing-independent pathway. J Exp Med 2001; 194: 1053-1068.
38. Zweerink HJ, Gammon MC, Utz U, Sauma SY, Harrer T, Hawkins JC, Johnson RP, Sirotina A, Hermes JD, Walker BD, Biddison WE. Presentation of endogenous peptides to MHC class I-restricted cytotoxic T lymphocytes in transport deletion mutant T2 cells. J Immunol 1993; 150: 1763-1771.
39. Koopmann JO, Albring J, Hüter E, Bulbuc N, Spee P, Neefjes J, Hämmerling GJ, Momburg F. Export of antigenic peptides from the endoplasmic reticulum intersects with retrograde protein translocation through the Sec61p channel. Immunity 2000; 13: 117-127.
40. GromméM, Uytdehaag FGCM, Janssen H, Calafat J, van Binnendijk RS, Kenter MJH, Tulp A, Verwoerd D, Neefjes J. Recycling MHC class I molecules and endosomal peptide loading. Proc Natl Acad Sci U S A 1999; 96: 10326-10331.
41. Neumeister C, Nanan R, Cornu TI, Lüder CGK, ter Meulen V, Naim H, Niewiesk S. Measles virus and canine distemper virus target proteins into a TAP-independent MHC class I-restricted antigen-processing pathway. J Gen Virol 2001; 82: 441-447.
42. Schirmbeck R, Reimann J. Peptide transporter-independent, stress protein-mediated endosomal processing of endogenous protein antigens for major histocompatibility complex class I presentation. Eur J Immunol 1994; 24: 1478-1486.
43. Cuervo AM, Dice JF. A receptor for the selective uptake and degradation of proteins by lysosomes. Science 1996; 273: 501-503.
44. Wolters JC, Abele R, Tampe R. Selective and ATP-dependent translocation of peptides by the homodimeric ATP binding cassette transporter TAP-like (ABCB9). J Biol Chem 2005; 280: 23631-23636.
45. Zhou D, Li P, Lin Y, Lott JM, Hislop AD, Canaday DH, Brutkiewicz RR, Blum JS. Lamp-2a facilitates MHC class II presentation of cytoplasmic antigens. Immunity 2005; 22: 571-581.
46. Schmid D, Pypaert M, Munz C. Antigen-loading compartments for major histocompatibility complex class II molecules continuously receive input from autophagosomes. Immunity 2007; 26: 79-92.
47. d of normal and TAP-deficient cells. Eur J Immunol 2006; 36: 544-557.
48. Kleijmeer MJ, Escola JM, UytdeHaag FG, Jakobson E, Griffith JM, Osterhaus AD, Stoorvogel W, Melief CJ, Rabouille C, Geuze HJ. Antigen loading of MHC class I molecules in the endocytic tract. Traffic 2001; 2: 124-137.
49. Neijssen J, Herberts C, Drijfhout JW, Reits E, Janssen L, Neefjes J. Cross-presentation by intercellular peptide transfer through gap junctions. Nature 2005; 434: 83-88.
50. + T cells results in antigen-specific T-cell tolerance. Nat Med 2000; 6: 1348-1354.
51. Shen L, Rock KL. Priming of T cells by exogenous antigen cross-presented on MHC class I molecules. Curr Opin Immunol 2006; 18: 85-91.
52. Cheadle EJ, O'Donnell D, Selby PJ, Jackson AM. Closely related mycobacterial strains demonstrate contrasting levels of efficacy as antitumor vaccines and are processed for major histocompatibility complex class I presentation by multiple routes in dendritic cells. Infect Immun 2005; 73: 784-794.
53. + T cells by a transporter associated with antigen processing-independent pathway in vitro and in vivo. J Immunol 2006; 177: 3525-3533.
54. Datta SK, Okamoto S, Hayashi T, Shin SS, Mihajlov I, Fermin A, Guiney DG, Fierer J, Raz E. Vaccination with irradiated Listeria induces protective T cell immunity. Immunity 2006; 25: 143-152.
55. Gurnani K, Kennedy J, Sad S, Sprott GD, Krishnan L. Phosphatidylserine receptor-mediated recognition of archaeosome adjuvant promotes endocytosis and MHC class I cross-presentation of the entrapped antigen by phagosome-to-cytosol transport and classical processing. J Immunol 2004; 173: 566-578.
56. Shen L, Sigal LJ, Boes M, Rock KL. Important role of cathepsin S in generating peptides for TAP-independent MHC class I crosspresentation in vivo. Immunity 2004; 21: 155-165.
57. - dendritic cells: A dispensable role for TAP. Eur J Immunol 2002; 32: 818-825.
58. Moron VG, Rueda P, Sedlik C, Leclerc C. In vivo, dendritic cells can cross-present virus-like particles using an endosome-to-cytosol pathway. J Immunol 2003; 171: 2242-2250.
59. Hearn AR, de Haan L, Pemberton AJ, Hirst TR, Rivett AJ. Trafficking of exogenous peptides into proteasome-dependent major histocompatibility complex class I pathway following enterotoxin B subunit-mediated delivery. J Biol Chem 2004; 279: 51315-51322.
60. + T-cell epitopes to dendritic cells and elicits CTL in vivo. Vaccine 2004; 23: 604-614.
61. Castellino F, Boucher PE, Eichelberg K, Mayhew M, Rothman JE, Houghton AN, Germain RN. Receptor-mediated uptake of antigen/heat shock protein complexes results in major histocompatibility complex class I antigen presentation via two distinct processing pathways. J Exp Med 2000; 191: 1957-1964.
62. Palliser D, Guillen E, Ju M, Eisen HN. Multiple intracellular routes in the cross-presentation of a soluble protein by murine dendritic cells. J Immunol 2005; 174: 1879-1887.
63. + T-cell responses. Blood 2006; 107: 4597-4605.
64. Ackerman AL, Kyritsis C, Tampé R, Cresswell P. Access of soluble antigens to the endoplasmic reticulum can explain cross-presentation by dendritic cells. Nat Immunol 2005; 6: 107-113.
65. Lencer WI, Tsai B. The intracellular voyage of cholera toxin: Going retro. Trends Biochem Sci 2003; 28: 639-645.
66. Ackerman AL, Kyritsis C, Tampé R, Cresswell P. Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens. Proc Natl Acad Sci U S A 2003; 100: 12889-12894.
67. Guermonprez P, Saveanu L, Kleijmeer M, Davoust J, van Endert P, Amigorena S. ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 2003; 425: 397-402.
68. Houde M, Bertholet S, Gagnon E, Brunet S, Goyette G, Laplante A, Princiotta MF, Thibault P, Sacks D, Desjardins M. Phagosomes are competent organelles for antigen cross-presentation. Nature 2003; 425: 402-406.
69. Ackerman AL, Giodini A, Cresswell P. A role for the endoplasmic reticulum protein retrotranslocation machinery during crosspresentation by dendritic cells. Immunity 2006; 25: 607-617.
70. Touret N, Paroutis P, Terebiznik M, Harrison RE, Trombetta S, Pypaert M, Chow A, Jiang A, Shaw J, Yip C, Moore HP, van der WN, Houben D, Peters PJ, de Chastellier C et al. Quantitative and dynamic assessment of the contribution of the ER to phagosome formation. Cell 2005; 123: 157-170.
71. Carbonetti NH, Irish TJ, Chen CH, O'Connell CB, Hadley GA, McNamara U, Tuskan RG, Lewis GK. Intracellular delivery of a cytolytic T-lymphocyte epitope peptide by pertussis toxin to major histocompatibility complex class I without involvement of the cytosolic class I antigen processing pathway. Infect Immun 1999; 67: 602-607.
72. Smith DC, Gallimore A, Jones E, Roberts B, Lord JM, Deeks E, Cerundolo V, Roberts LM. Exogenous peptides delivered by ricin require processing by signal peptidase for transporter associated with antigen processing- independent MHC class I-restricted presentation. J Immunol 2002; 169: 99-107.
73. Lu J, Wettstein PJ, Higashimoto Y, Appella E, Celis E. TAP-independent presentation of CTL epitopes by trojan antigens. J Immunol 2001; 166: 7063-7071.
74. Lu J, Higashimoto Y, Appella E, Celis E. Multiepitope trojan antigen peptide vaccines for the induction of antitumor CTL and Th immune responses. J Immunol 2004; 172: 4575-4582.
75. Bettosini F, Fiorillo MT, Magnacca A, Leone L, Torrisi MR, Sorrentino R. The C terminus of the nucleoprotein of influenza A virus delivers antigens transduced by Tat to the trans -Golgi network and promotes an efficient presentation through HLA class I. J Virol 2005; 79: 15537-15546.
76. Zhou X, Glas R, Liu T, Ljunggren HG, Jondal M. Antigen processing mutant T2 cells present viral antigen restricted through H-2K b. Eur J Immunol 1993; 23: 1802-1808.
77. Liu TM, Zhou XZ, Örvell C, Lederer E, Ljunggren HG, Jondal M. Heat-inactivated Sendai virus can enter multiple MHC class I processing pathways and generate cytotoxic T lymphocyte responses in vivo. J Immunol 1995; 154: 3147-3155.
78. + T cell responses to EBV EBNA1: HLA class I presentation of the (Gly-Ala)-containing protein requires exogenous processing. Immunity 1997; 7: 791-802.
79. Martinez-Kinader B, Lipford GB, Wagner H, Heeg K. Sensitization of MHC class I-restricted T cells to exogenous proteins: Evidence for an alternative class I-restricted antigen presentation pathway. Immunology 1995; 86: 287-295.
80. Ulmer JB, Donnelly JJ, Liu MA. Presentation of an exogenous antigen by major histocompatibility complex class I molecules. Eur J Immunol 1994; 24: 1590-1596.
81. de la Salle H, Saulquin X, Mansour I, Klayme S, Fricker D, Zimmer J, Cazenave JP, Hanau D, Bonneville M, Houssaint E, Lefranc G, Naman R. Asymptomatic deficiency in the peptide transporter associated to antigen processing (TAP). Clin Exp Immunol 2002; 128: 525-531.
82. Wölfel C, Drexler I, Van Pel A, Thres T, Leister N, Herr W, Sutter G, Huber C, Wolfel T. Transporter (TAP)- and proteasome-independent presentation of a melanoma-associated tyrosinase epitope. Int J Cancer 2000; 88: 432-438.