A novel category of antigens enabling CTL immunity to tumor escape variants: Cinderella antigens

Cancer Immunology, Immunotherapy

Volumn 61, Issue 1, 2012, Pages 119-125

  Seidel, Ursula J E ^a   Oliveira, Claudia C ^a   Lampen, Margit H ^a   Van Hall, Thorbald ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Antigen processing; CIMT2011; Cytotoxic T lymphocytes (CTL); T cell epitopes associated with impaired peptide processing (TEIPP); Transporter associated with peptide processing (TAP); Tumor immune escape

Indexed keywords

CARRIER PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; T CELL EPITOPE ASSOCIATED WITH IMPAIRED PEPTIDE PROCESSING PROTEIN; TRANSPORTER ASSOCIATED WITH PEPTIDE PROCESSING; TUMOR PROTEIN; UNCLASSIFIED DRUG;

ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; CANCER IMMUNOTHERAPY; CELL MEDIATED CYTOTOXICITY; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; HUMAN; IMMUNOSURVEILLANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; TUMOR ESCAPE;

ANIMALS; ANTIGEN PRESENTATION; ATP-BINDING CASSETTE TRANSPORTERS; EPITOPES, T-LYMPHOCYTE; HUMANS; IMMUNOTHERAPY; NEOPLASMS; T-LYMPHOCYTES, CYTOTOXIC; TUMOR ESCAPE;

EID: 84856729500     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-011-1160-x     Document Type: Review

References (49)

1. F Cavallo C De Giovanni P Nanni G Forni PL Lollini 2011 2011: the immune hallmarks of cancer Cancer Immunol Immunother 60 3 319 326 10.1007/s00262-010- 0968-0 21267721 10.1007/s00262-010-0968-0 1:CAS:528:DC%2BC3MXit1Gqsb0%3D
2. DJ Hicklin FM Marincola S Ferrone 1999 HLA class I antigen downregulation in human cancers: T-cell immunotherapy revives an old story Mol Med Today 5 4 178 186 S1357-4310(99)01451-3 10203751 10.1016/S1357-4310(99)01451-3 1:CAS:528:DyaK1MXisFamurw%3D (Pubitemid 29279236)
3. HT Khong NP Restifo 2002 Natural selection of tumor variants in the generation of "tumor escape" phenotypes Nat Immunol 3 11 999 1005 10.1038/ni1102-999 12407407 10.1038/ni1102-999 1:CAS:528:DC%2BD38Xot1Chs7o%3D (Pubitemid 35363649)
4. F Garrido I Algarra 2001 MHC antigens and tumor escape from immune surveillance Adv Cancer Res 83 117 158 11665717 10.1016/S0065-230X(01)83005-0 1:CAS:528:DC%2BD38Xitl2jsb4%3D (Pubitemid 32959264)
5. F Garrido T Cabrera N Aptsiauri 2010 "Hard" and "soft" lesions underlying the HLA class I alterations in cancer cells: implications for immunotherapy Int J Cancer 127 2 249 256 10.1002/ijc.25270 20178101 1:CAS:528:DC%2BC3cXmsVGntbo%3D
6. B Seliger 2008 Molecular mechanisms of MHC class I abnormalities and APM components in human tumors Cancer Immunol Immunother 57 11 1719 1726 10.1007/s00262-008-0515-4 18408926 10.1007/s00262-008-0515-4 1:CAS:528:DC%2BD1cXhtVejsbbO
7. CC Chang M Campoli S Ferrone 2003 HLA class I defects in malignant lesions: what have we learned? Keio J Med 52 4 220 229 14748474 10.2302/kjm.52.220 1:CAS:528:DC%2BD2cXhvFOntLs%3D (Pubitemid 38139923)
8. KS Ryu YS Lee BK Kim YG Park YW Kim SY Hur TE Kim IK Kim JW Kim 2001 Alterations of HLA class I and II antigen expression in preinvasive, invasive and metastatic cervical cancers Exp Mol Med 33 3 136 144 11642549 1:CAS:528:DC%2BD3MXnvVGgsL0%3D (Pubitemid 32954690)
9. D Berghuis AS de Hooge SJ Santos D Horst EJ Wiertz MC van Eggermond PJ van den Elsen AH Taminiau L Ottaviano KL Schaefer U Dirksen E Hooijberg A Mulder CJ Melief RM Egeler MW Schilham ES Jordanova PC Hogendoorn AC Lankester 2009 Reduced human leukocyte antigen expression in advanced-stage Ewing sarcoma: implications for immune recognition J Pathol 218 2 222 231 10.1002/path.2537 19274709 10.1002/path.2537 1:CAS:528:DC%2BD1MXms1Kiu7g%3D
10. M Meissner TE Reichert M Kunkel W Gooding TL Whiteside S Ferrone B Seliger 2005 Defects in the human leukocyte antigen class I antigen processing machinery in head and neck squamous cell carcinoma: association with clinical outcome Clin Cancer Res 11 7 2552 2560 10.1158/1078-0432.CCR-04-2146 15814633 10.1158/1078-0432.CCR-04-2146 1:CAS:528:DC%2BD2MXivFKisro%3D (Pubitemid 40569453)
11. ES Jordanova A Gorter O Ayachi F Prins LG Durrant GG Kenter SH van der Burg GJ Fleuren 2008 Human leukocyte antigen class I, MHC class I chain-related molecule A, and CD8 +/regulatory T-cell ratio: which variable determines survival of cervical cancer patients? Clin Cancer Res 14 7 2028 2035 10.1158/1078-0432.CCR-07-4554 18381941 10.1158/1078-0432.CCR-07-4554 1:CAS:528:DC%2BD1cXkt1akurs%3D (Pubitemid 351551112)
12. AM Mehta ES Jordanova GG Kenter S Ferrone GJ Fleuren 2008 Association of antigen processing machinery and HLA class I defects with clinicopathological outcome in cervical carcinoma Cancer Immunol Immunother 57 2 197 206 10.1007/s00262-007-0362-8 17622526 10.1007/s00262-007-0362-8 1:CAS:528:DC%2BD2sXhtlaqt7vK (Pubitemid 350159921)
13. T Cabrera E Lara JM Romero I Maleno LM Real F Ruiz-Cabello P Valero FM Camacho F Garrido 2007 HLA class I expression in metastatic melanoma correlates with tumor development during autologous vaccination Cancer Immunol Immunother 56 5 709 717 10.1007/s00262-006-0226-7 16960691 10.1007/s00262-006-0226-7 1:CAS:528:DC%2BD2sXisVaqtbg%3D (Pubitemid 46348739)
14. R Carretero JM Romero F Ruiz-Cabello I Maleno F Rodriguez FM Camacho LM Real F Garrido T Cabrera 2008 Analysis of HLA class I expression in progressing and regressing metastatic melanoma lesions after immunotherapy Immunogenetics 60 8 439 447 10.1007/s00251-008-0303-5 18545995 10.1007/s00251-008-0303-5 1:CAS:528:DC%2BD1cXotV2jtLo%3D
15. B Seliger F Ruiz-Cabello F Garrido 2008 IFN inducibility of major histocompatibility antigens in tumors Adv Cancer Res 101 249 276 10.1016/S0065-230X(08)00407-7 19055946 10.1016/S0065-230X(08)00407-7 1:CAS:528:DC%2BD1MXht1CrtL%2FO
16. MJ Maeurer SM Gollin D Martin W Swaney J Bryant C Castelli P Robbins G Parmiani WJ Storkus MT Lotze 1996 Tumor escape from immune recognition: lethal recurrent melanoma in a patient associated with downregulation of the peptide transporter protein TAP-1 and loss of expression of the immunodominant MART-1/Melan-A antigen J Clin Invest 98 7 1633 1641 10.1172/JCI118958 8833913 10.1172/JCI118958 1:STN:280:DyaK28vjtVygsw%3D%3D (Pubitemid 26327874)
17. PM van Endert 1999 Genes regulating MHC class I processing of antigen Curr Opin Immunol 11 1 82 88 10047538 10.1016/S0952-7915(99)80015-6 (Pubitemid 29082342)
18. EZ Wolpert M Petersson BJ Chambers JK Sandberg R Kiessling HG Ljunggren K Karre 1997 Generation of CD8 + T cells specific for transporter associated with antigen processing deficient cells Proc Natl Acad Sci U S A 94 21 11496 11501 9326638 10.1073/pnas.94.21.11496 1:CAS:528:DyaK2sXmslaru7o%3D (Pubitemid 27451027)
19. T van Hall EZ Wolpert P van Veelen S Laban M van der Veer M Roseboom S Bres P Grufman A de Ru H Meiring A de Jong K Franken A Teixeira R Valentijn JW Drijfhout F Koning M Camps F Ossendorp K Karre HG Ljunggren CJ Melief R Offringa 2006 Selective cytotoxic T-lymphocyte targeting of tumor immune escape variants Nat Med 12 4 417 424 10.1038/nm1381 16550190 10.1038/nm1381
20. B Chambers P Grufman V Fredriksson K Andersson M Roseboom S Laban M Camps EZ Wolpert EJ Wiertz R Offringa HG Ljunggren T van Hall 2007 Induction of protective CTL immunity against peptide transporter TAP-deficient tumors through dendritic cell vaccination Cancer Res 67 18 8450 8455 10.1158/0008-5472.CAN-07- 1092 17875682 10.1158/0008-5472.CAN-07-1092 1:CAS:528:DC%2BD2sXhtVCit7zO (Pubitemid 47437417)
21. CC Oliveira PA van Veelen B Querido A de Ru M Sluijter S Laban JW Drijfhout SH van der Burg R Offringa T van Hall 2010 The nonpolymorphic MHC Qa-1b mediates CD8+ T cell surveillance of antigen-processing defects J Exp Med 207 1 207 221 10.1084/jem.20091429 20038604 10.1084/jem.20091429 1:CAS:528:DC%2BC3cXht1ekt7o%3D
22. MH Lampen MC Verweij B Querido SH van der Burg EJ Wiertz T van Hall 2010 CD8+ T cell responses against TAP-inhibited cells are readily detected in the human population J Immunol 185 11 6508 6517 10.4049/jimmunol.1001774 20980626 10.4049/jimmunol.1001774 1:CAS:528:DC%2BC3cXhsVaqt7zJ
23. T van Hall CC Oliveira SA Joosten TH Ottenhoff 2010 The other Janus face of Qa-1 and HLA-E: diverse peptide repertoires in times of stress Microbes Infect 12 12-13 910 918 10.1016/j.micinf.2010.07.011 20670688 10.1016/j.micinf.2010.07.011
24. MH Lampen T van Hall 2011 Strategies to counteract MHC-I defects in tumors Curr Opin Immunol 23 2 293 298 10.1016/j.coi.2010.12.005 21295956 10.1016/j.coi.2010.12.005 1:CAS:528:DC%2BC3MXkt1KitrY%3D
25. CC Oliveira B Querido M Sluijter J Derbinski SH van der Burg T van Hall 2011 Peptide transporter TAP mediates between competing antigen sources generating distinct surface MHC-I peptide repertoires Eur J Immunol 41 11 3114 3124 10.1002/eji.201141836 21898382 10.1002/eji.201141836 1:CAS:528: DC%2BC3MXhtlGktb7E
26. T van Hall S Laban D Koppers-Lalic J Koch C Precup P Asmawidjaja R Offringa EJ Wiertz 2007 The varicellovirus-encoded TAP inhibitor UL49.5 regulates the presentation of CTL epitopes by Qa-1b1 J Immunol 178 2 657 662 17202325 (Pubitemid 46095137)
27. MC Verweij ME Ressing W Knetsch E Quinten A Halenius N van Bel H Hengel JW Drijfhout T van Hall EJ Wiertz 2011 Inhibition of mouse TAP by immune evasion molecules encoded by non-murine herpesviruses Mol Immunol 48 6-7 835 845 10.1016/j.molimm.2010.12.008 21292324 10.1016/j.molimm.2010.12.008 1:CAS:528:DC%2BC3MXitFagtrc%3D
28. C Riebeling JC Allegood E Wang AH Merrill Jr AH Futerman 2003 Two mammalian longevity assurance gene (LAG1) family members, trh1 and trh4, regulate dihydroceramide synthesis using different fatty acyl-CoA donors J Biol Chem 278 44 43452 43459 10.1074/jbc.M307104200 12912983 10.1074/jbc.M307104200 1:CAS:528:DC%2BD3sXosFSrs7g%3D (Pubitemid 37345968)
29. LarsenMV NM A Weinzierl O Lund 2006 TAP-independent MHC class I presentation Immunol Rev 2 233 245 10.2174/157339506778018550
30. M Del Val S Iborra M Ramos S Lazaro 2011 Generation of MHC class I ligands in the secretory and vesicular pathways Cell Mol Life Sci 68 9 1543 1552 10.1007/s00018-011-0661-2 21387141 10.1007/s00018-011-0661-2 1:CAS:528:DC%2BC3MXktlyjt7w%3D
31. VM Braud DS Allan CA O'Callaghan K Soderstrom A D'Andrea GS Ogg S Lazetic NT Young JI Bell JH Phillips LL Lanier AJ McMichael 1998 HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C Nature 391 6669 795 799 10.1038/35869 9486650 10.1038/35869 1:CAS:528:DyaK1cXhtlCjtbo%3D (Pubitemid 28099678)
32. JR Rodgers RG Cook 2005 MHC class Ib molecules bridge innate and acquired immunity Nat Rev Immunol 5 6 459 471 10.1038/nri1635 15928678 10.1038/nri1635 1:CAS:528:DC%2BD2MXks1GmsLY%3D (Pubitemid 40835034)
33. PE Jensen BA Sullivan LM Reed-Loisel DA Weber 2004 Qa-1, a nonclassical class I histocompatibility molecule with roles in innate and adaptive immunity Immunol Res 29 1-3 81 92 10.1385/IR:29:1-3:081 15181272 10.1385/IR:29:1-3:081 1:CAS:528:DC%2BD2cXlsFGitbw%3D (Pubitemid 38822399)
34. JR Kraft RE Vance J Pohl AM Martin DH Raulet PE Jensen 2000 Analysis of Qa-1(b) peptide binding specificity and the capacity of CD94/NKG2A to discriminate between Qa-1-peptide complexes J Exp Med 192 5 613 624 10974028 10.1084/jem.192.5.613 1:CAS:528:DC%2BD3cXmtlegsb0%3D
35. A DeCloux AS Woods RJ Cotter MJ Soloski J Forman 1997 Dominance of a single peptide bound to the class I(B) molecule, Qa-1b J Immunol 158 5 2183 2191 9036964 1:CAS:528:DyaK2sXhtlGqt74%3D (Pubitemid 127470001)
36. N Lee DR Goodlett A Ishitani H Marquardt DE Geraghty 1998 HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences J Immunol 160 10 4951 4960 9590243 1:CAS:528:DyaK1cXjtVanurk%3D (Pubitemid 28215330)
37. WF Lo AS Woods A DeCloux RJ Cotter ES Metcalf MJ Soloski 2000 Molecular mimicry mediated by MHC class Ib molecules after infection with gram-negative pathogens Nat Med 6 2 215 218 10.1038/72329 10655113 10.1038/72329 1:CAS:528:DC%2BD3cXosF2jtA%3D%3D (Pubitemid 30082369)
38. A Davies S Kalb B Liang CJ Aldrich FA Lemonnier H Jiang R Cotter MJ Soloski 2003 A peptide from heat shock protein 60 is the dominant peptide bound to Qa-1 in the absence of the MHC class Ia leader sequence peptide Qdm J Immunol 170 10 5027 5033 12734347 1:CAS:528:DC%2BD3sXjsVGqs7Y%3D (Pubitemid 36554733)
39. G Pietra C Romagnani C Manzini L Moretta MC Mingari 2010 The emerging role of HLA-E-restricted CD8 + T lymphocytes in the adaptive immune response to pathogens and tumors J Biomed Biotechnol 2010 907092 10.1155/2010/907092 20634877 10.1155/2010/907092
40. LC Sullivan CS Clements J Rossjohn AG Brooks 2008 The major histocompatibility complex class Ib molecule HLA-E at the interface between innate and adaptive immunity Tissue Antigens 72 5 415 424 18946929 10.1111/j.1399-0039.2008.01138.x 1:CAS:528:DC%2BD1cXhsVCmsbbP
41. RA Henderson H Michel K Sakaguchi J Shabanowitz E Appella DF Hunt VH Engelhard 1992 HLA-A2.1-associated peptides from a mutant cell line: a second pathway of antigen presentation Science 255 5049 1264 1266 1546329 10.1126/science.1546329 1:CAS:528:DyaK38XhslWrsLg%3D
42. ML Wei P Cresswell 1992 HLA-A2 molecules in an antigen-processing mutant cell contain signal sequence-derived peptides Nature 356 6368 443 446 10.1038/356443a0 1557127 10.1038/356443a0 1:CAS:528:DyaK38XitFamtr4%3D
43. AO Weinzierl D Rudolf N Hillen S Tenzer P van Endert H Schild HG Rammensee S Stevanovic 2008 Features of TAP-independent MHC class I ligands revealed by quantitative mass spectrometry Eur J Immunol 38 6 1503 1510 10.1002/eji.200838136 18446792 10.1002/eji.200838136 1:CAS:528: DC%2BD1cXnsF2hur0%3D
44. D Horst MC Verweij AJ Davison ME Ressing EJ Wiertz 2011 Viral evasion of T cell immunity: ancient mechanisms offering new applications Curr Opin Immunol 23 1 96 103 10.1016/j.coi.2010.11.005 21146386 10.1016/j.coi.2010.11.005 1:CAS:528:DC%2BC3MXit1ygu7k%3D
45. F El Hage V Stroobant I Vergnon JF Baurain H Echchakir V Lazar S Chouaib PG Coulie F Mami-Chouaib 2008 Preprocalcitonin signal peptide generates a cytotoxic T lymphocyte-defined tumor epitope processed by a proteasome- independent pathway Proc Natl Acad Sci USA 105 29 10119 10124 10.1073/pnas.0802753105 18626012 10.1073/pnas.0802753105 1:CAS:528: DC%2BD1cXptFOgsrs%3D
46. XL Li YY Liu D Knight Y Odaka JM Mathis R Shi J Glass QJ Zhang 2009 Effect of B7.1 costimulation on T-cell based immunity against TAP-negative cancer can be facilitated by TAP1 expression PLoS One 4 7 e6385 10.1371/journal.pone.0006385 19629186 10.1371/journal.pone.0006385
47. XL Li D Zhang D Knight Y Odaka J Glass JM Mathis QJ Zhang 2009 Priming of immune responses against transporter associated with antigen processing (TAP)-deficient tumours: tumour direct priming Immunology 128 3 420 428 10.1111/j.1365-2567.2009.03127.x 20067541 10.1111/j.1365-2567.2009.03127.x 1:CAS:528:DC%2BD1MXhtlClt7vO
48. Vergati M, Intrivici C, Huen NY, Schlom J, Tsang KY (2010) Strategies for cancer vaccine development. J Biomed Biotechnol. doi: 10.1155/2010/596432
49. Durgeau A, El Hage F, Vergnon I, Validire P, de Montpreville V, Besse B, Soria JC, van Hall T, Mami-Chouaib F (2011) Different expression levels of the TAP peptide transporter lead to recognition of different antigenic peptides by tumor-specific CTL. J Immunol 187(11):5532-5539. doi: 10.4049/jimmunol.1102060