Alternative Ii-independent antigen-processing pathway in leukemic blasts involves TAP-dependent peptide loading of HLA class II complexes

Cancer Immunology, Immunotherapy

Volumn 59, Issue 12, 2010, Pages 1825-1838

  Van Luijn, Marvin M ^a,b   Chamuleau, Martine E D ^a   Ressing, Maaike E ^c,d   Wiertz, Emmanuel J ^c,d   Ostrand Rosenberg, Suzanne ^e   Souwer, Yuri ^b   Zevenbergen, Adri ^a   Ossenkoppele, Gert J ^a   Van De Loosdrecht, Arjan A ^a   Van Ham, S Marieke ^b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

Author keywords

Antigen presentation; Immune surveillance; Leukemia; MHC class II; Tumor cells

Indexed keywords

CARRIER PROTEIN; CLASS II ASSOCIATED INVARIANT CHAIN PEPTIDE; HLA ANTIGEN CLASS 2; HLA DR ANTIGEN; PEPTIDE; PROTEASOME; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING; UNCLASSIFIED DRUG; ABC TRANSPORTER; B LYMPHOCYTE ANTIGEN; INVARIANT CHAIN; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING (TAP);

ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ARTICLE; BLAST CELL; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INVARIANT CHAIN; LEUKEMIA; LEUKEMIA CELL; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN TRANSPORT; WESTERN BLOTTING; BLAST CELL CRISIS; IMMUNOLOGY; MYELOID LEUKEMIA; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANTIGEN PRESENTATION; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; ATP-BINDING CASSETTE TRANSPORTERS; BLAST CRISIS; CELL LINE, TUMOR; HISTOCOMPATIBILITY ANTIGENS CLASS II; HLA-DR ANTIGENS; HUMANS; LEUKEMIA, MYELOID; PROTEASOME ENDOPEPTIDASE COMPLEX;

EID: 77957678117     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-010-0908-z     Document Type: Article

References (44)

1. D Nandi P Tahiliani A Kumar D Chandu 2006 The ubiquitin-proteasome system J Biosci 31 137 155 1:CAS:528:DC%2BD28XjvFWjs7Y%3D 10.1007/BF02705243 16595883
2. MJ Androlewicz KS Anderson P Cresswell 1993 Evidence that transporters associated with antigen processing translocate a major histocompatibility complex class I-binding peptide into the endoplasmic reticulum in an ATP-dependent manner Proc Natl Acad Sci USA 90 9130 9134 1:CAS:528: DyaK3sXmsVOmtr8%3D 10.1073/pnas.90.19.9130 8415666 (Pubitemid 23306465)
3. T Serwold F Gonzalez J Kim R Jacob N Shastri 2002 ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum Nature 419 480 483 1:CAS:528:DC%2BD38XnsFais70%3D 10.1038/nature01074 12368856
4. V Lotteau L Teyton A Peleraux T Nilsson L Karlsson SL Schmid V Quaranta PA Peterson 1990 Intracellular transport of class II MHC molecules directed by invariant chain Nature 348 600 605 1:CAS:528:DyaK3MXmtVWjsA%3D%3D 10.1038/348600a0 2250716
5. JJ Neefjes V Stollorz PJ Peters HJ Geuze HL Ploegh 1990 The biosynthetic pathway of MHC class II but not class I molecules intersects the endocytic route Cell 61 171 183 1:CAS:528:DyaK3cXitlelsbg%3D 10.1016/0092-8674(90)90224-3 2156628 (Pubitemid 20134388)
6. MS Anderson J Miller 1992 Invariant chain can function as a chaperone protein for class II major histocompatibility complex molecules Proc Natl Acad Sci USA 89 2282 2286 1:CAS:528:DyaK38XitFamsbk%3D 10.1073/pnas.89.6.2282 1549594
7. J Pieters O Bakke B Dobberstein 1993 The MHC class II-associated invariant chain contains two endosomal targeting signals within its cytoplasmic tail J Cell Sci 106 Pt 3 831 846 1:CAS:528:DyaK2cXhs1SqurY%3D 8308066
8. P Romagnoli RN Germain 1994 The CLIP region of invariant chain plays a critical role in regulating major histocompatibility complex class II folding, transport, and peptide occupancy J Exp Med 180 1107 1113 1:CAS:528: DyaK2cXlsFGit7c%3D 10.1084/jem.180.3.1107 8064228 (Pubitemid 24256623)
9. VS Sloan P Cameron G Porter M Gammon M Amaya E Mellins DM Zaller 1995 Mediation by HLA-DM of dissociation of peptides from HLA-DR Nature 375 802 806 1:CAS:528:DyaK2MXmvVymurk%3D 10.1038/375802a0 7596415
10. P Guermonprez L Saveanu M Kleijmeer J Davoust EP van S Amigorena 2003 ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells Nature 425 397 402 1:CAS:528:DC%2BD3sXnsV2kt74%3D 10.1038/nature01911 14508489 (Pubitemid 37187268)
11. S Burgdorf C Scholz A Kautz R Tampe C Kurts 2008 Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation Nat Immunol 9 558 566 1:CAS:528:DC%2BD1cXkvVOqtb8%3D 10.1038/ni.1601 18376402 (Pubitemid 351560525)
12. A Dani A Chaudhry P Mukherjee D Rajagopal S Bhatia A George V Bal S Rath 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 1:CAS:528:DC%2BD2cXotlGrt7k%3D 10.1242/jcs.01288 15316082 (Pubitemid 39328309)
13. J Dengjel O Schoor R Fischer M Reich M Kraus M Muller K Kreymborg F Altenberend J Brandenburg H Kalbacher R Brock C Driessen HG Rammensee S Stevanovic 2005 Autophagy promotes MHC class II presentation of peptides from intracellular source proteins Proc Natl Acad Sci USA 102 7922 7927 1:CAS:528:DC%2BD2MXkvF2ju74%3D 10.1073/pnas.0501190102 15894616 (Pubitemid 40781039)
14. C Paludan D Schmid M Landthaler M Vockerodt D Kube T Tuschl C Munz 2005 Endogenous MHC class II processing of a viral nuclear antigen after autophagy Science 307 593 596 1:CAS:528:DC%2BD2MXmslOhsg%3D%3D 10.1126/science.1104904 15591165 (Pubitemid 40165684)
15. D Zhou P Li Y Lin JM Lott AD Hislop DH Canaday RR Brutkiewicz JS Blum 2005 Lamp-2a facilitates MHC class II presentation of cytoplasmic antigens Immunity 22 571 581 1:CAS:528:DC%2BD2MXkslOqsb0%3D 10.1016/j.immuni.2005.03.009 15894275 (Pubitemid 40719193)
16. JD Lich JF Elliott JS 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 1:CAS:528:DC%2BD3cXivFKgtL0%3D 10.1084/jem.191.9.1513 10790426 (Pubitemid 30257348)
17. P Mukherjee A Dani S Bhatia N Singh AY Rudensky A George V Bal S Mayor 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 1:CAS:528:DC%2BD3MXmtlSjt7w%3D 11509605
18. TD Armstrong VK Clements BK Martin JP Ting S Ostrand-Rosenberg 1997 Major histocompatibility complex class II-transfected tumor cells present endogenous antigen and are potent inducers of tumor-specific immunity Proc Natl Acad Sci USA 94 6886 6891 1:CAS:528:DyaK2sXktF2ru7k%3D 10.1073/pnas.94.13.6886 9192661 (Pubitemid 27281960)
19. Y Zhao D Boczkowski SK Nair E Gilboa 2003 Inhibition of invariant chain expression in dendritic cells presenting endogenous antigens stimulates CD4+ T-cell responses and tumor immunity Blood 102 4137 4142 1:CAS:528: DC%2BD3sXpsFals7k%3D 10.1182/blood-2003-06-1867 12920018 (Pubitemid 37486999)
20. EO Long T LaVaute V Pinet D Jaraquemada 1994 Invariant chain prevents the HLA-DR-restricted presentation of a cytosolic peptide J Immunol 153 1487 1494 1:CAS:528:DyaK2cXlslOisrc%3D 8046228
21. PA Roche P Cresswell 1990 Invariant chain association with HLA-DR molecules inhibits immunogenic peptide binding Nature 345 615 618 1:CAS:528:DyaK3cXksFOjsL4%3D 10.1038/345615a0 2190094 (Pubitemid 20181883)
22. MK Tewari G Sinnathamby D Rajagopal LC Eisenlohr 2005 A cytosolic pathway for MHC class II-restricted antigen processing that is proteasome and TAP dependent Nat Immunol 6 287 294 1:CAS:528:DC%2BD2MXhtleqt7Y%3D 10.1038/ni1171 15711549 (Pubitemid 41724766)
23. MM van Luijn ME Chamuleau JA Thompson S Ostrand-Rosenberg TM Westers Y Souwer GJ Ossenkoppele SM van Ham AA van de Loosdrecht 2009 CLIP down-modulation enhances the immunogenicity of myeloid leukemic blasts resulting in increased CD4+ T cell responses Haematologica 95 485 493 10.3324/haematol.2009.010595 19903675
24. PA Roche MS Marks P Cresswell 1991 Formation of a nine-subunit complex by HLA class II glycoproteins and the invariant chain Nature 354 392 394 1:CAS:528:DyaK38XhvFCgsA%3D%3D 10.1038/354392a0 1956401 (Pubitemid 21896847)
25. AD Hislop ME Ressing D van Leeuwen VA Pudney D Horst D Koppers-Lalic NP Croft JJ Neefjes AB Rickinson EJ Wiertz 2007 A CD8+ T cell immune evasion protein specific to Epstein-Barr virus and its close relatives in Old World primates J Exp Med 204 1863 1873 1:CAS:528:DC%2BD2sXptVyjsLg%3D 10.1084/jem.20070256 17620360 (Pubitemid 47236322)
26. D Koppers-Lalic EA Reits ME Ressing AD Lipinska R Abele J Koch RM Marcondes P Admiraal LD van K Bienkowska-Szewczyk TC Mettenleiter FA Rijsewijk R Tampe J Neefjes EJ Wiertz 2005 Varicelloviruses avoid T cell recognition by UL49.5-mediated inactivation of the transporter associated with antigen processing Proc Natl Acad Sci USA 102 5144 5149 1:CAS:528:DC%2BD2MXjsFemtLk%3D 10.1073/pnas.0501463102 15793001
27. JA Thompson SK Dissanayake BR Ksander KL Knutson ML Disis S Ostrand-Rosenberg 2006 Tumor cells transduced with the MHC class II Transactivator and CD80 activate tumor-specific CD4+ T cells whether or not they are silenced for invariant chain Cancer Res 66 1147 1154 1:CAS:528: DC%2BD28XlsFOnsw%3D%3D 10.1158/0008-5472.CAN-05-2289 16424052 (Pubitemid 43165984)
28. MC Verweij D Koppers-Lalic S Loch F Klauschies SH de la E Quinten PJ Lehner A Mulder MR Knittler R Tampe J Koch ME Ressing EJ Wiertz 2008 The varicellovirus UL49.5 protein blocks the transporter associated with antigen processing (TAP) by inhibiting essential conformational transitions in the 6 + 6 transmembrane TAP core complex J Immunol 181 4894 4907 1:CAS:528: DC%2BD1cXhtFarurbP 18802093
29. TE Adams JG Bodmer WF Bodmer 1983 Production and characterization of monoclonal antibodies recognizing the alpha-chain subunits of human ia alloantigens Immunology 50 613 624 1:CAS:528:DyaL2cXkvFOrsA%3D%3D 6197354
30. G Plewnia K Schulze C Hunte R Tampe J Koch 2007 Modulation of the antigenic peptide transporter TAP by recombinant antibodies binding to the last five residues of TAP1 J Mol Biol 369 95 107 1:CAS:528:DC%2BD2sXkslagtr4%3D 10.1016/j.jmb.2007.02.102 17418234 (Pubitemid 46635432)
31. WT Schaiff KA Hruska Jr DW McCourt M Green BD Schwartz 1992 HLA-DR associates with specific stress proteins and is retained in the endoplasmic reticulum in invariant chain negative cells J Exp Med 176 657 666 1:CAS:528:DyaK38XlsVyru7g%3D 10.1084/jem.176.3.657 1512535
32. S Viville J Neefjes V Lotteau A Dierich M Lemeur H Ploegh C Benoist D Mathis 1993 Mice lacking the MHC class II-associated invariant chain Cell 72 635 648 1:CAS:528:DyaK3sXhs1Kqtb4%3D 10.1016/0092-8674(93)90081-Z 7679955 (Pubitemid 23077750)
33. CR Berkers M Verdoes E Lichtman E Fiebiger BM Kessler KC Anderson HL Ploegh H Ovaa PJ Galardy 2005 Activity probe for in vivo profiling of the specificity of proteasome inhibitor bortezomib Nat Methods 2 357 362 1:CAS:528:DC%2BD2MXjsVyls70%3D 10.1038/nmeth759 15846363 (Pubitemid 41130981)
34. KL Knutson ML Disis 2005 Tumor antigen-specific T helper cells in cancer immunity and immunotherapy Cancer Immunol Immunother 54 721 728 1:CAS:528:DC%2BD2MXmtVajt78%3D 10.1007/s00262-004-0653-2 16010587 (Pubitemid 40977140)
35. MM van Luijn W van den Ancker ME Chamuleau GJ Ossenkoppele SM van Ham AA van de Loosdrecht 2010 Impaired antigen presentation in neoplasia: basic mechanisms and implications for acute myeloid leukemia Immunotherapy 2 85 97 10.2217/imt.09.84 20635891
36. PE Harris A Maffei AI Colovai J Kinne S Tugulea N Suciu-Foca 1996 Predominant HLA-class II bound self-peptides of a hematopoietic progenitor cell line are derived from intracellular proteins Blood 87 5104 5112 1:CAS:528:DyaK28XjsFGitr0%3D 8652823
37. I Teobald DJ Dunnion M Whitbread SJ Curnow MJ Browning 2008 Phenotypic and functional differentiation of KG-1 into dendritic-like cells Immunobiology 213 75 86 1:CAS:528:DC%2BD1cXisFSnsrw%3D 10.1016/j.imbio.2007.06.001 18207029
38. ST Smiley AY Rudensky LH Glimcher MJ Grusby 1996 Truncation of the class II beta-chain cytoplasmic domain influences the level of class II/invariant chain-derived peptide complexes Proc Natl Acad Sci USA 93 241 244 1:CAS:528:DyaK28XjslyhtQ%3D%3D 10.1073/pnas.93.1.241 8552613 (Pubitemid 26038135)
39. A Simonsen E Stang B Bremnes M Roe K Prydz O Bakke 1997 Sorting of MHC class II molecules and the associated invariant chain (Ii) in polarized MDCK cells J Cell Sci 110 Pt 5 597 609 1:CAS:528:DyaK2sXitlamsrw%3D 9092942
40. SK Dissanayake N Tuera 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 1:CAS:528:DC%2BD2MXhtV2ku7g%3D 15699107
41. L Qi S Ostrand-Rosenberg 2000 MHC class II presentation of endogenous tumor antigen by cellular vaccines depends on the endocytic pathway but not H2-M Traffic 1 152 160 1:CAS:528:DC%2BD3cXktl2ms7g%3D 10.1034/j.1600-0854.2000. 010207.x 11208095
42. EF Posthuma JH Falkenburg JF Apperley A Gratwohl B Hertenstein RF Schipper M Oudshoorn JH Biezen J Hermans R Willemze E Roosnek D Niederwieser 2000 HLA-DR4 is associated with a diminished risk of the development of chronic myeloid leukemia (CML). Chronic Leukemia Working Party of the European Blood and Marrow Transplant Registry Leukemia 14 859 862 1:CAS:528:DC%2BD3cXjsFCqtLw%3D 10.1038/sj.leu.2401774 10803518
43. JA Thompson MK Srivastava JJ Bosch VK Clements BR Ksander S Ostrand-Rosenberg 2008 The absence of invariant chain in MHC II cancer vaccines enhances the activation of tumor-reactive type 1 CD4(+) T lymphocytes Cancer Immunol Immunother 57 389 398 1:CAS:528:DC%2BD2sXhsVGhurvI 10.1007/s00262-007- 0381-5 17724589 (Pubitemid 350295383)
44. BC Hulette G Rowden CA Ryan CM Lawson SM Dawes GM Ridder GF Gerberick 2001 Cytokine induction of a human acute myelogenous leukemia cell line (KG-1) to a CD1a+ dendritic cell phenotype Arch Dermatol Res 293 147 158 1:CAS:528:DC%2BD3MXjvVensLw%3D 10.1007/s004030000201 11357229 (Pubitemid 32247248)