PIRCHE-II: an algorithm to predict indirectly recognizable HLA epitopes in solid organ transplantation
Tóm tắt
Human leukocyte antigen (HLA) mismatches between donors and recipients may lead to alloreactivity after solid organ transplantation. Over the last few decades, our knowledge of the complexity of the HLA system has dramatically increased, as numerous new HLA alleles have been identified. As a result, the likelihood of alloreactive responses towards HLA mismatches after solid organ transplantation cannot easily be assessed. Algorithms are promising solutions to estimate the risk for alloreactivity after solid organ transplantation. In this review, we show that the recently developed PIRCHE-II (Predicted Indirectly ReCognizable HLA Epitopes) algorithm can be used to minimize alloreactivity towards HLA mismatches. Together with the use of other algorithms and simulation approaches, the PIRCHE-II algorithm aims for a better estimated alloreactive risk for individual patients and eventually an improved graft survival after solid organ transplantation.
Từ khóa
Tài liệu tham khảo
Abraham JP, Barker DJ, Robinson J, Maccari G, Marsh SGE (2018) The IPD Databases: Cataloguing and Understanding Allele Variants Methods Mol Biol
Ali JM, Bolton EM, Bradley JA, Pettigrew GJ (2013) Allorecognition pathways in transplant rejection and tolerance. Transplantation 96:681–688
Andreatta M, Karosiene E, Rasmussen M, Stryhn A, Buus S, Nielsen M (2015) Accurate pan-specific prediction of peptide-MHC class II binding affinity with improved binding core identification. Immunogenetics 67:641–650. https://doi.org/10.1007/s00251-015-0873-y
Ansari D, Bucin D, Nilsson J (2014) Human leukocyte antigen matching in heart transplantation: systematic review and meta-analysis. Transpl Int 27:793–804. https://doi.org/10.1111/tri.12335
Badell IR, Ford ML (2016) T follicular helper cells in the generation of alloantibody and graft rejection. Curr Opin Organ Transplant 21:1–6. https://doi.org/10.1097/MOT.0000000000000260
Baker RJ, Hernandez-Fuentes MP, Brookes PA, Chaudhry AN, Cook HT, Lechler RI (2001) Loss of direct and maintenance of indirect alloresponses in renal allograft recipients: implications for the pathogenesis of chronic allograft nephropathy. J Immunol 167:7199–7206
Benichou G, Takizawa PA, Olson CA, McMillan M, Sercarz EE (1992) Donor major histocompatibility complex (MHC) peptides are presented by recipient MHC molecules during graft rejection. J Exp Med 175:305–308
Bohringer D, Daub F, Schwartzkopff J, Maier P, Birnbaum F, Sundmacher R, Reinhard T (2010) Operational post-keratopasty graft tolerance due to differential HLAMatchmaker matching. Mol Vis 16:2362–2367
Carapito R, Radosavljevic M, Bahram S (2016) Next-Generation Sequencing of the HLA locus: Methods and impacts on HLA typing, population genetics and disease association studies. Human Immunol 77:1016–1023
Chaigne B et al. (2016) Immunogenicity of anti-HLA antibodies in pancreas and islet transplantation Cell Transplant
Claas FHJ, Heidt S (2017) Epitope-Based HLA Matching: A Useful Strategy With Many Shortcomings to Overcome Transplantation
Claas FH, Dankers MK, Oudshoorn M, van Rood J, Mulder A, Roelen DL, Duquesnoy RJ, Doxiadis II (2005) Differential immunogenicity of HLA mismatches in clinical transplantation. Transpl Immunol 14:187–191
Conlon TM et al (2012) Germinal center alloantibody responses are mediated exclusively by indirect-pathway CD4 T follicular helper cells. J Immunol 188:2643–2652. https://doi.org/10.4049/jimmunol.1102830
Daniels L et al (2018) The clinical significance of epitope mismatch load in kidney transplantation: A multicentre study. Transpl Immunol 50:55–59
Dankers MK, Roelen DL, Nagelkerke NJ, de Lange P, Persijn GG, Doxiadis II, Claas FH (2004a) The HLA-DR phenotype of the responder is predictive of humoral response against HLA class I antigens. Hum Immunol 65:13–19
Dankers MK et al (2004b) The number of amino acid triplet differences between patient and donor is predictive for the antibody reactivity against mismatched human leukocyte antigens. Transplantation 77:1236–1239
de Graav GN et al (2015) Follicular T helper cells and humoral reactivity in kidney transplant patients. Clin Exp Immunol 180:329–340. https://doi.org/10.1111/cei.12576
De Oliveira DB et al (2000) Structural analysis of two HLA-DR-presented autoantigenic epitopes: crucial role of peripheral but not central peptide residues for T-cell receptor recognition. Mol Immunol 37:813–825
Doxiadis II, Smits JM, Schreuder GM, Persijn GG, van Howelingen HC, van Rood JJ, Claas FH (1996) Association between specific HLA combinations and probability of kidney allograft loss: the taboo concept. Lancet 348:850–853
Doxiadis, II, Smits JM, Persijn GG, U Frei, Claas FH (2004) It takes six to boogie: allocating cadaver kidneys in Eurotransplant Transplantation
Duke JL et al. (2019) Resolving MiSeq-Generated Ambiguities in HLA-DPB1 Typing by Using the Oxford Nanopore Technology J Mol Diagn
Duquesnoy RJ (2002) HLAMatchmaker: a molecularly based algorithm for histocompatibility determination. I. Description of the algorithm. Hum Immunol 63:339–352
Duquesnoy RJ (2006) A structurally based approach to determine HLA compatibility at the humoral immune level. Hum Immunol 67:847–862
Duquesnoy RJ (2008) Clinical usefulness of HLAMatchmaker in HLA epitope matching for organ transplantation. Curr Opin Immunol 20:594–601
Duquesnoy RJ (2016) Reflections on HLA Epitope-Based Matching for Transplantation. Front Immunol 28:7
Duquesnoy RJ (2017) Are We Ready for Epitope-Based HLA Matching in Clinical Organ Transplantation? Transplantation. https://doi.org/10.1097/TP.0000000000001667
Duquesnoy RJ et al (2008a) Retransplant candidates have donor-specific antibodies that react with structurally defined HLA-DR,DQ,DP epitopes. Transpl Immunol 18:352–360. https://doi.org/10.1016/j.trim.2007.10.001
Duquesnoy RJ, Spellman S, Haagenson M, Wang T, Horowitz MM, Oudshoorn M (2008b) HLAMatchmaker-defined triplet matching is not associated with better survival rates of patients with class I HLA allele mismatched hematopoietic cell transplants from unrelated donors. Biol Blood Marrow Transplant 14:1064–1071
Ekong UD, Antala S, Bow L, Sese D, Morotti R, Rodriguez-Davalos M, Gan G, Deng Y, Emre SH (2019) HLA, Non-HLA Antibodies, and Eplet Mismatches in Pediatric Liver Transplantation: Observations From a Small, Single-Center Cohort. Exp Clin Transplant 17:6–17. https://doi.org/10.6002/ect.MESOT2018.L30
Everly MJ et al (2013) Incidence and impact of de novo donor-specific alloantibody in primary renal allografts. Transplantation 95:410–417. https://doi.org/10.1097/TP.0b013e31827d62e3
Fangmann J, Dalchau R, Fabre JW (1992) Rejection of skin allografts by indirect allorecognition of donor class I major histocompatibility complex peptides. J Exp Med 175:1521–1529
Fernandez-Vina MA et al (2013) Multiple mismatches at the low expression HLA loci DP, DQ, and DRB3/4/5 associate with adverse outcomes in hematopoietic stem cell transplantation. Blood 121:4603–4610. https://doi.org/10.1182/blood-2013-02-481945
Fuller TC, Fuller A (1999) The humoral immune response against an HLA class I allodeterminant correlates with the HLA-DR phenotype of the responder. Transplantation 68:173–182
Game DS, Lechler RI (2002) Pathways of allorecognition: implications for transplantation tolerance. Transplant Immunol 10:101–108
Geneugelijk K, Thus KA, Spierings E (2014) Predicting alloreactivity in transplantation. J Immunol Res 2014:159479. https://doi.org/10.1155/2014/159479
Geneugelijk K et al (2015) Predicted Indirectly Recognizable HLA Epitopes Presented by HLA-DRB1 Are Related to HLA Antibody Formation During Pregnancy. Am J Transplant 15:3112–3122. https://doi.org/10.1111/ajt.13508
Geneugelijk K, Niemann M, de Hoop T, Spierings E (2016) Completion of HLA protein sequences by automated homology-based nearest-neighbor extrapolation of HLA database sequences Hum Immunol
Geneugelijk K, Wissing J, Koppenaal D, Niemann M, Spierings E (2017) Computational Approaches to Facilitate Epitope-Based HLA Matching in Solid Organ Transplantation. J Immunol Res 2017:1–9
Geneugelijk K, Niemann M, Drylewicz J, van Zuilen A, Joosten I, Allebes WA, van der Meer A, Hilbrands LB, Baas MC, Hack CE, van Reekum F, Verhaar MC, Kamburova EG, Bots ML, Seelen MAJ, Sanders JS, Hepkema BG, Lambeck AJ, Bungener LB, Roozendaal C, Tilanus MGJ, Vanderlocht J, Voorter CE, Wieten L, van Duijnhoven E, Gelens M, Christiaans MHL, van Ittersum F, Nurmohamed A, Lardy JNM, Swelsen W, van der Pant K, van der Weerd N, ten Berge I, Bemelman FJ, Hoitsma A, van der Boog P, de Fijter JW, Betjes MGH, Heidt S, Roelen DL, Claas FH, Otten HG, Spierings E (2018) PIRCHE-II Is Related to Graft Failure after Kidney Transplantation. Front Immunol 9:321. https://doi.org/10.3389/fimmu.2018.00321
Goodwin S, Gurtowski J, Ethe-Sayers S, Deshpande P, Schatz MC, McCombie WR (2015) Oxford Nanopore sequencing, hybrid error correction, and de novo assembly of a eukaryotic genome. Genome Res 25:1750–1756. https://doi.org/10.1101/gr.191395.115
Hornick PI, Mason PD, Baker RJ, Hernandez-Fuentes M, Frasca L, Lombardi G, Taylor K, Weng L, Rose ML, Yacoub MH, Batchelor R, Lechler RI (2000) Significant frequencies of T cells with indirect anti-donor specificity in heart graft recipients with chronic rejection. Circulation 101:2405–2410
Karosiene E, Rasmussen M, Blicher T, Lund O, Buus S, Nielsen M (2013) NetMHCIIpan-3.0, a common pan-specific MHC class II prediction method including all three human MHC class II isotypes, HLA-DR, HLA-DP and HLA-DQ. Immunogenetics 65:711–724. https://doi.org/10.1007/s00251-013-0720-y
Kosmoliaptsis V, Bradley JA, Sharples LD, Chaudhry A, Key T, Goodman RS, Taylor CJ (2008) Predicting the immunogenicity of human leukocyte antigen class I alloantigens using structural epitope analysis determined by HLAMatchmaker. Transplantation 85:1817–1825
Kubal CA et al (2018) Class II Human Leukocyte Antigen Epitope Mismatch Predicts De Novo Donor-Specific Antibody Formation After Liver Transplantation. Liver Transplant 24:1101–1108. https://doi.org/10.1002/lt.25286
Lachmann N et al (2017) Donor Recipient Matching Based on Predicted Recognizable HLA Epitopes Predicts the Incidence of De Novo Donor-Specific HLA Antibodies Following Renal Transplantation. Am J Transplant. https://doi.org/10.1111/ajt.14393
Lee RS, Grusby MJ, Glimcher LH, Winn HJ, Auchincloss H Jr (1994) Indirect recognition by helper cells can induce donor-specific cytotoxic T lymphocytes in vivo. J Exp Med 179:865–872
Lee RS et al (2001) Indirect recognition of allopeptides promotes the development of cardiac allograft vasculopathy. Proc Natl Acad Sci U S A 98:3276–3281. https://doi.org/10.1073/pnas.051584498
Liu C, Xiao F, Hoisington-Lopez J, Lang K, Quenzel P, Duffy B, Mitra RD (2018) Accurate Typing of Human Leukocyte Antigen Class I Genes by Oxford Nanopore Sequencing J Mol Diagn
Lovegrove E, Pettigrew GJ, Bolton EM, Bradley JA (2001) Epitope mapping of the indirect T cell response to allogeneic class I MHC: sequences shared by donor and recipient MHC may prime T cells that provide help for alloantibody production. J Immunol 167:4338–4344
Marino J, Paster J, Benichou G (2016) Allorecognition by T Lymphocytes and Allograft Rejection. Front Immunol 7:582. https://doi.org/10.3389/fimmu.2016.00582
McCaughan JA et al (2018) Identification of risk epitope mismatches associated with de novo donor-specific HLA antibody development in cardiothoracic transplantation. Am J Transplant 18:2924–2933. https://doi.org/10.1111/ajt.14951
McCutcheon JA, Gumperz J, Smith KD, Lutz CT, Parham P (1995) Low HLA-C expression at cell surfaces correlates with increased turnover of heavy chain mRNA. J Exp Med 181:2085–2095
Meszaros M et al (2019) Class II Human Leukocyte Antigen Epitope Mismatch Predicts De Novo Donor-Specific Antibody Formation After Liver Transplantation. Liver Transplant 25:184–185. https://doi.org/10.1002/lt.25357
Mettu RR, Charles T, Landry SJ (2016) CD4+ T-cell epitope prediction using antigen processing constraints. J Immunol Methods 432:72–81. https://doi.org/10.1016/j.jim.2016.02.013
Mitchison NA (2004) T-cell-B-cell cooperation. Nat Rev Immunol 4:308–312. https://doi.org/10.1038/nri1334
Nielsen M, Justesen S, Lund O, Lundegaard C, Buus S (2010) NetMHCIIpan-2.0 - Improved pan-specific HLA-DR predictions using a novel concurrent alignment and weight optimization training procedure. Immunome Res 6:9-7580–7586-7589. https://doi.org/10.1186/1745-7580-6-9
Otten HG, Calis JJ, Kesmir C, van Zuilen AD, Spierings E (2013) Predicted indirectly recognizable HLA epitopes presented by HLA-DR correlate with the de novo development of donor-specific HLA IgG antibodies after kidney transplantation. Hum Immunol 74:290–296. https://doi.org/10.1016/j.humimm.2012.12.004
Persijn GG (2006) Allocation of organs, particularly kidneys, within Eurotransplant. Hum Immunol 67:419–423. https://doi.org/10.1016/j.humimm.2006.03.008
Petersdorf EW et al (2014) HLA-C expression levels define permissible mismatches in hematopoietic cell transplantation. Blood 124:3996–4003. https://doi.org/10.1182/blood-2014-09-599969
Robinson J, Halliwell JA, Hayhurst JD, Flicek P, Parham P, Marsh SG (2015) The IPD and IMGT/HLA database: allele variant databases. Nucleic Acids Res 43:D423–D431. https://doi.org/10.1093/nar/gku1161
Robinson J, Soormally AR, Hayhurst JD, Marsh SGE (2016) The IPD-IMGT/HLA Database - New developments in reporting HLA variation Hum Immunol
Rudolph MG, Stanfield RL, Wilson IA (2006) How TCRs bind MHCs, peptides, and coreceptors. Annu Rev Immunol 24:419–466
Sauve D, Baratin M, Leduc C, Bonin K, Daniel C (2004) Alloantibody production is regulated by CD4+ T cells' alloreactive pathway, rather than precursor frequency or Th1/Th2 differentiation. Am J Transplant 4:1237–1245. https://doi.org/10.1111/j.1600-6143.2004.00520.x
SivaSai KS et al (1999) Indirect recognition of donor HLA class I peptides in lung transplant recipients with bronchiolitis obliterans syndrome. Transplantation 67:1094–1098
Southwood S et al (1998) Several common HLA-DR types share largely overlapping peptide binding repertoires. J Immunol 160:3363–3373
Steele DJ, Laufer TM, Smiley ST, Ando Y, Grusby MJ, Glimcher LH, Auchincloss H Jr (1996) Two levels of help for B cell alloantibody production. J Exp Med 183:699–703
Suciu-Foca N, Ciubotariu R, Itescu S, Rose EA, Cortesini R (1998) Indirect allorecognition of donor HLA-DR peptides in chronic rejection of heart allografts. Transplant Proc 30:3999–4000
Sullivan PM, Warner P, Kemna MS, Albers EL, Law SP, Weiss NS, Law YM (2015) HLA molecular epitope mismatching and long-term graft loss in pediatric heart transplant recipients. J Heart Lung Transplant 34:950–957. https://doi.org/10.1016/j.healun.2014.12.017
Susal C, Opelz G (2013) Current role of human leukocyte antigen matching in kidney transplantation. Curr Opin Organ transplant 18:438–444. https://doi.org/10.1097/MOT.0b013e3283636ddf
Talayero P et al. (2018) Donor-Specific Antibodies in Pediatric Intestinal and Multivisceral Transplantation: The Role of Liver and Human Leukocyte Antigen Mismatching Liver Transplantation
Terasaki PI, Cai J (2008) Human leukocyte antigen antibodies and chronic rejection: from association to causation. Transplantation 86:377–383
Vella JP, Spadafora-Ferreira M, Murphy B, Alexander SI, Harmon W, Carpenter CB, Sayegh MH (1997) Indirect allorecognition of major histocompatibility complex allopeptides in human renal transplant recipients with chronic graft dysfunction. Transplantation 64:795–800
Walton DC et al (2016) HLA Matching at the Eplet Level Protects Against Chronic Lung Allograft Dysfunction. Am J Transplant 16:2695–2703. https://doi.org/10.1111/ajt.13798
Walton DC et al (2018) HLA class II Eplet mismatch predicts De Novo DSA formation post lung transplant. Transpl Immunol 51:73–75. https://doi.org/10.1016/j.trim.2018.10.002
Wiebe C et al (2013) Class II HLA epitope matching-A strategy to minimize de novo donor-specific antibody development and improve outcomes. Am J Transplant 13:3114–3122. https://doi.org/10.1111/ajt.12478