The Exception that Reinforces the Rule: Crosspriming by Cytosolic Peptides that Escape Degradation

Immunity

Volumn 28, Issue 6, 2008, Pages 787-798

  Lev, Avital ^a   Takeda, Kazuyo ^a   Zanker, Damien ^c   Maynard, Jason C ^d   Dimberu, Peniel ^a   Waffarn, Elizabeth ^a   Gibbs, James ^a   Netzer, Nir ^a   Princiotta, Michael F ^e   Neckers, Len ^b   Picard, Didier ^f   Nicchitta, Christopher V ^d   Chen, Weisan ^c   Reiter, Yoram ^g   Bennink, Jack R ^a   Yewdell, Jonathan W ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c LUDWIG INSTITUTE FOR CANCER RESEARCH   (Australia)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e State University of New York Upstate Medical University: College of Medicine   (United States)

^f UNIVERSITY OF GENEVA   (Switzerland)

^g TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

MOLIMMUNO

Indexed keywords

ANTIGEN; GLUCOSE REGULATED PROTEIN 94; GLYCOPROTEIN GP 96; HEAT SHOCK PROTEIN 90; IMMUNOGLOBULIN F(AB) FRAGMENT; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; OLIGOPEPTIDE; PROTEASOME; T LYMPHOCYTE RECEPTOR;

ADOLESCENT; ANIMAL EXPERIMENT; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS PRESENTATION; ENDOPLASMIC RETICULUM; FEMALE; HUMAN; HUMAN CELL; IMMUNOGENICITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN SYNTHESIS INHIBITION;

ANIMALS; ANTIBODIES; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HSP90 HEAT-SHOCK PROTEINS; HUMANS; INFLUENZA A VIRUS; MICE; PEPTIDES; RECOMBINANT PROTEINS;

EID: 44649084957     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2008.04.015     Document Type: Article

References (44)

1. Andersen P.S., Stryhn A., Hansen B.E., Fugger L., Engberg L., and Buus S. A recombinant antibody with the antigen-specific major histocompatibility complex-restricted specificity of T cells. Proc. Natl. Acad. Sci. USA 93 (1996) 1820-1824
2. Anton L.C., Yewdell J.W., and Bennink J.R. MHC class I-associated peptides produced from endogenous gene products with vastly different efficiencies. J. Immunol. 158 (1997) 2535-2542
3. Baker-LePain J.C., Sarzotti M., Fields T.A., Li C.Y., and Nicchitta C.V. GRP94 (gp96) and GRP94 N-terminal geldanamycin binding domain elicit tissue nonrestricted tumor suppression. J. Exp. Med. 196 (2002) 1447-1459
4. Basta S., Stoessel R., Basler M., van den Broek M., and Groettrup M. Cross-presentation of the long-lived lymphocytic choriomeningitis virus nucleoprotein does not require neosynthesis and is enhanced via heat shock proteins. J. Immunol. 175 (2005) 796-805
5. + T cell responses to influenza A virus: roles for cross-presentation and lysis-independent immunodomination. J. Immunol. 173 (2004) 5021-5027
6. Cho Y., Basta S., Chen W., Bennink J.R., and Yewdell J.W. Heat-aggregated noninfectious influenza virus induces a more balanced CD8(+)-T-lymphocyte immunodominance hierarchy than infectious virus. J. Virol. 77 (2003) 4679-4684
7. de Haard H.J., van Neer N., Reurs A., Hufton S.E., Roovers R.C., Henderikx P., de Bruine A.P., Arends J.-W., and Hoogenboom H.R. A large non-immunized human Fab fragment phage library that permits rapid isolation and kinetic analysis of high-affinity antibodies. J. Biol. Chem. 274 (1999) 18218-18230
8. Demine R., and Walden P. Testing the role of gp96 as peptide chaperone in antigen processing. J. Biol. Chem. 280 (2005) 17573-17578
9. Denkberg G., and Reiter Y. Recombinant antibodies with T-cell receptor-like specificity: novel tools to study MHC class I presentation. Autoimmun. Rev. 5 (2006) 252-257
10. Donohue K.B., Grant J.M., Tewalt E.F., Palmer D.C., Theoret M.R., Restifo N.P., and Norbury C.C. Cross-priming utilizes antigen not available to the direct presentation pathway. Immunology 119 (2006) 63-73
11. Eisenlohr L.C., Huang L., and Golovina T.N. Rethinking peptide supply to MHC class I molecules. Nat. Rev. Immunol. 7 (2007) 403-410
12. Falk K., Rötzschke O., and Rammensee H.G. Cellular peptide composition governed by major histocompatibility complex class I molecules. Nature 348 (1990) 248-251
13. Flynn G.C., Chappell T.G., and Rothman J.E. Peptide binding and release by proteins implicated as catalysts of protein assembly. Science 245 (1989) 385-390
14. Flynn G.C., Pohl J., Flocco M.T., and Rothman J.E. Peptide-binding specificity of the molecular chaperone BiP. Nature 353 (1991) 726-730
15. Fourie A.M., Sambrook J.F., and Gething M.J. Common and divergent peptide binding specificities of hsp70 molecular chaperones. J. Biol. Chem. 269 (1994) 30470-30478
16. Freigang S., Eschli B., Harris N., Geuking M., Quirin K., Schrempf S., Zellweger R., Weber J., Hengartner H., and Zinkernagel R.M. A lymphocytic choriomeningitis virus glycoprotein variant that is retained in the endoplasmic reticulum efficiently cross-primes CD8(+) T cell responses. Proc. Natl. Acad. Sci. USA 104 (2007) 13426-13431
17. Gasteiger G., Kastenmuller W., Ljapoci R., Sutter G., and Drexler I. Crosspriming of cytotoxic T cells dictates antigen requisites for modified vaccinia virus Ankara vector vaccines. J. Virol. 81 (2007) 11925-11936
18. Isaacs J.S., Xu W., and Neckers L. Heat shock protein 90 as a molecular target for cancer therapeutics. Cancer Cell 3 (2003) 213-217
19. Javid B., MacAry P.A., and Lehner P.J. Structure and function: heat shock proteins and adaptive immunity. J. Immunol. 179 (2007) 2035-2040
20. Kisselev A.F., Akopian T.N., and Goldberg A.L. Range of sizes of peptide products generated during degradation of different proteins by archaeal proteasomes. J. Biol. Chem. 273 (1998) 1982-1989
21. Koopmann J.O., Albring J., Huter E., Bulbuc N., Spee P., Neefjes J., Hammerling G.J., and Momburg F. Export of antigenic peptides from the endoplasmic reticulum intersects with retrograde protein translocation through the Sec61p channel. Immunity 13 (2000) 117-127
22. Kunisawa J., and Shastri N. Hsp90alpha chaperones large C-terminally extended proteolytic intermediates in the MHC class I antigen processing pathway. Immunity 24 (2006) 523-534
23. Lev A., Denkberg G., Cohen C.J., Tzukerman M., Skorecki K.L., Chames P., Hoogenboom H.R., and Reiter Y. Isolation and characterization of human recombinant antibodies endowed with the antigen-specific, major histocompatibility complex-restricted specificity of T cells directed toward the widely expressed tumor T-cell epitopes of the telomerase catalytic subunit. Cancer Res. 62 (2002) 3184-3194
24. Neijssen J., Herberts C., Drijfhout J.W., Reits E., Janssen L., and Neefjes J. Cross-presentation by intercellular peptide transfer through gap junctions. Nature 434 (2005) 83-88
25. Neijssen J., Pang B., and Neefjes J. Gap junction-mediated intercellular communication in the immune system. Prog. Biophys. Mol. Biol. 94 (2007) 207-218
26. Nicchitta C.V., Carrick D.M., and Baker-Lepain J.C. The messenger and the message: gp96 (GRP94)-peptide interactions in cellular immunity. Cell Stress Chaperones 9 (2004) 325-331
27. + T cell cross-priming via transfer of proteasome substrates. Science 304 (2004) 1318-1321
28. Oizumi S., Strbo N., Pahwa S., Deyev V., and Podack E.R. Molecular and cellular requirements for enhanced antigen cross-presentation to CD8 cytotoxic T lymphocytes. J. Immunol. 179 (2007) 2310-2317
29. Picard D., Suslova E., and Briand P.A. 2-color photobleaching experiments reveal distinct intracellular dynamics of two components of the Hsp90 complex. Exp. Cell Res. 312 (2006) 3949-3958
30. Porgador A., Yewdell J.W., Deng Y., Bennink J.R., and Germain R.N. Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 6 (1997) 715-726
31. Princiotta M.F., Finzi D., Qian S.B., Gibbs J., Schuchmann S., Buttgereit F., Bennink J.R., and Yewdell J.W. Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 18 (2003) 343-354
32. Reits E., Griekspoor A., Neijssen J., Groothuis T., Jalink K., van Veelen P., Janssen H., Calafat J., Drijfhout J.W., and Neefjes J. Peptide diffusion, protection, and degradation in nuclear and cytoplasmic compartments before antigen presentation by MHC class I. Immunity 18 (2003) 97-108
33. Reits E., Neijssen J., Herberts C., Benckhuijsen W., Janssen L., Drijfhout J.W., and Neefjes J. A major role for TPPII in trimming proteasomal degradation products for MHC class I antigen presentation. Immunity 20 (2004) 495-506
34. Roelse J., Grommé M., Momburg F., Hämmerling G., and Neefjes J. Trimming of TAP-translocated peptides in the endoplasmic reticulum and in the cytosol during recycling. J. Exp. Med. 180 (1994) 1591-1597
35. Serna A., Ramirez M.C., Soukhanova A., and Sigal L.J. Cutting edge: efficient MHC class I cross-presentation during early vaccinia infection requires the transfer of proteasomal intermediates between antigen donor and presenting cells. J. Immunol. 171 (2003) 5668-5672
36. Shen L., and Rock K.L. Cellular protein is the source of cross-priming antigen in vivo. Proc. Natl. Acad. Sci. USA 101 (2004) 3035-3040
37. Shen L., and Rock K.L. Priming of T cells by exogenous antigen cross-presented on MHC class I molecules. Curr. Opin. Immunol. 18 (2006) 85-91
38. Speidel K., Osen W., Faath S., Hilgert I., Obst R., Braspenning J., Momburg F., Hammerling G.J., and Rammensee H.G. Priming of cytotoxic T lymphocytes by five heat-aggregated antigens in vivo: conditions, efficiency, and relation to antibody responses. Eur. J. Immunol. 27 (1997) 2391-2399
39. Srivastava P. Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annu. Rev. Immunol. 20 (2002) 395-425
40. Wallin R.P., Lundqvist A., More S.H., von Bonin A., Kiessling R., and Ljunggren H.G. Heat-shock proteins as activators of the innate immune system. Trends Immunol. 23 (2002) 130-135
41. Wolkers M.C., Brouwenstijn N., Bakker A.H., Toebes M., and Schumacher T.N. Antigen bias in T cell cross-priming. Science 304 (2004) 1314-1317
42. Yewdell J.W. Plumbing the sources of endogenous MHC class I peptide ligands. Curr. Opin. Immunol. 19 (2007) 79-86
43. Yewdell J.W., and Bennink J.R. Brefeldin A specifically inhibits presentation of protein antigens to cytotoxic T lymphocytes. Science 244 (1989) 1072-1075
44. 2+. FEBS J. 273 (2006) 513-522