Identification of Candidate Immunodominant Epitopes and Their HLA-Binding Prediction on BK Polyomavirus Proteins in Healthy Donors.

Λεπτομέρειες βιβλιογραφικής εγγραφής
Τίτλος: Identification of Candidate Immunodominant Epitopes and Their HLA-Binding Prediction on BK Polyomavirus Proteins in Healthy Donors.
Συγγραφείς: Lara-de-León AG; Advanced & Cell Therapy Services, Banc de Sang i Teixits (Blood and Tissue Bank, BST), Barcelona, Spain., Mora-Buch R; Advanced & Cell Therapy Services, Banc de Sang i Teixits (Blood and Tissue Bank, BST), Barcelona, Spain.; Transfusional Medicine Group, Vall d'Hebron Research Institute, Universitat Autònoma de Barcelona (VHIR-UAB), Barcelona, Spain., Cantó E; Advanced & Cell Therapy Services, Banc de Sang i Teixits (Blood and Tissue Bank, BST), Barcelona, Spain.; Transfusional Medicine Group, Vall d'Hebron Research Institute, Universitat Autònoma de Barcelona (VHIR-UAB), Barcelona, Spain., Peña-Gómez C; Mental Health and Neurosciences, Mixt Unit, Parc Taulí Research and Innovation Institute (I3PT), Barcelona, Spain., Rudilla F; Transfusional Medicine Group, Vall d'Hebron Research Institute, Universitat Autònoma de Barcelona (VHIR-UAB), Barcelona, Spain.; Immunogenetics and Histocompatibility Laboratory, Banc de Sang i Teixits (Blood and Tissue Bank, BST), Barcelona, Spain.
Πηγή: HLA [HLA] 2024 Oct; Vol. 104 (4), pp. e15722.
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Wiley Blackwell Country of Publication: England NLM ID: 101675570 Publication Model: Print Cited Medium: Internet ISSN: 2059-2310 (Electronic) Linking ISSN: 20592302 NLM ISO Abbreviation: HLA Subsets: MEDLINE
Imprint Name(s): Original Publication: Oxford : Wiley Blackwell, [2016]-
Ιατρικοί όροι (MeSH): BK Virus*/immunology , Immunodominant Epitopes*/immunology, Epitopes, T-Lymphocyte/immunology ; Polyomavirus Infections/immunology ; Polyomavirus Infections/virology ; HLA Antigens/immunology ; Viral Proteins/immunology ; Viral Proteins/chemistry ; Humans ; Protein Binding ; Epitope Mapping ; Healthy Volunteers ; Male ; Female ; Adult ; Alleles
Περίληψη: BK polyomavirus infection is an important cause of graft loss in transplant patients, however, currently available therapies lack effectiveness against this pathogen. Identification of immunological targets for potential treatments is therefore necessary. The aim of this study was to predict candidates of immunodominant epitopes within four BK virus proteins (VP1, VP2, VP3 and LTA) using PBMCs from 44 healthy donors. We used the ELISpot epitope mapping method to evaluate the T-cell response, and HLA-peptide binding was predicted using the NetMHCpan algorithm. A total of 11 potential peptides were selected for VP1, 3 for VP2/VP3 and 13 for LTA. Greater reactivity was observed for VP1 and LTA proteins compared with VP2/VP3. Most of the peptides selected as potential immunodominant candidates were restricted towards several HLA class I and II alleles, with predominant HLA class I binding by computational predictions. Based on these findings, the sequences of the selected immunodominant epitopes candidates and their corresponding HLA restrictions could contribute to the optimisation of functional assays and aid in the design and improvement of immunotherapy strategies against BK virus infections.
(© 2024 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.)
References: R. Sharma and M. Zachariah, “Bk Virus Nephropathy: Prevalence, Impact and Management Strategies,” International Journal of Nephrology and Renovascular Disease 13 (2020): 187–192, https://doi.org/10.2147/IJNRD.S236556.
A. Stolt, K. Sasnauskas, P. Koskela, M. Lehtinen, and J. Dillner, “Seroepidemiology of the Human Polyomaviruses,” Journal of General Virology 84, no. 6 (2003): 1499–1504, https://doi.org/10.1099/vir.0.18842‐0.
J. Gras, M. L. Nere, M. N. Peraldi, et al., “BK Virus Genotypes and Humoral Response in Kidney Transplant Recipients With BKV Associated Nephropathy,” Transplant Infectious Disease 25, no. 2 (2023): e14012, https://doi.org/10.1111/tid.14012.
H. H. Hirsch, N. Babel, P. Comoli, et al., “European Perspective on Human Polyomavirus Infection, Replication and Disease in Solid Organ Transplantation,” Clinical Microbiology and Infection 20, no. s7 (2014): 74–88, https://doi.org/10.1111/1469‐0691.12538.
H. Sökmen, G. Öztürk, M. Çimentepe, et al., “BK Virus Infections and Hemorrhagic Cystitis in Allogeneic Hematopoietic Stem Cell Transplant Recipients,” New Microbiologica 46, no. 2 (2023): 141–145.
V. Kesherwani and S. Tarang, “An Immunoinformatic Approach to Universal Therapeutic Vaccine Design Against BK Virus,” Vaccine 37, no. 26 (2019): 3457–3463, https://doi.org/10.1016/j.vaccine.2019.04.096.
O. Johnston, D. Jaswal, J. S. Gill, S. Doucette, D. A. Fergusson, and G. A. Knoll, “Treatment of Polyomavirus Infection in Kidney Transplant Recipients: A Systematic Review,” Transplantation 89, no. 9 (2010): 1057–1070, https://doi.org/10.1097/TP.0b013e3181d0e15e.
A. S. Nelson, N. Yalamarthi, M. K. Yong, and E. Blyth, “Beyond Antivirals: Virus‐Specific T‐Cell Immunotherapy for BK Virus Haemorrhagic Cystitis and JC Virus Progressive Multifocal Leukoencephalopathy,” Current Opinion in Infectious Diseases 34, no. 6 (2021): 627–634, https://doi.org/10.1097/QCO.0000000000000794.
T. Schachtner, K. Müller, M. Stein, et al., “BK Virus‐Specific Immunity Kinetics: A Predictor of Recovery From Polyomavirus BK‐Associated Nephropathy,” American Journal of Transplantation 11, no. 11 (2011): 2443–2452, https://doi.org/10.1111/j.1600‐6143.2011.03693.x.
M. H. Hammer, G. Brestrich, H. Andree, et al., “HLA Type‐Independent Method to Monitor Polyoma BK Virus‐Specific CD4 + and CD8 + T‐Cell Immunity,” American Journal of Transplantation 6, no. 3 (2006): 625–631, https://doi.org/10.1111/j.1600‐6143.2005.01221.x.
S. Binggeli, A. Egli, S. Schaub, et al., “Polyomavirus BK‐Specific Cellular Immune Response to VP1 and Large T‐Antigen in Kidney Transplant Recipients,” American Journal of Transplantation 7, no. 5 (2007): 1131–1139, https://doi.org/10.1111/j.1600‐6143.2007.01754.x.
F. C. Renner, H. Dietrich, N. Bulut, et al., “The Risk of Polyomavirus‐Associated Graft Nephropathy Is Increased by a Combined Suppression of CD8 and CD4 Cell‐Dependent Immune Effects,” Transplantation Proceedings 45, no. 4 (2013): 1608–1610, https://doi.org/10.1016/j.transproceed.2013.01.026.
P. Comoli, M. Cioni, S. Basso, et al., “Immunity to Polyomavirus BK Infection: Immune Monitoring to Regulate the Balance Between Risk of BKV Nephropathy and Induction of Alloimmunity,” Clinical & Developmental Immunology 2013 (2013): 1–6, https://doi.org/10.1155/2013/256923.
G. R. Ambalathingal, R. S. Francis, M. J. Smyth, C. Smith, and R. Khanna, “BK Polyomavirus: Clinical Aspects, Immune Regulation, and Emerging Therapies,” Clinical Microbiology Reviews 30, no. 2 (2017): 503–528, https://doi.org/10.1128/CMR.00074‐16.
T. Ono, Y. Fujita, T. Matano, S. Takahashi, T. Morio, and A. Kawana‐Tachikawa, “Characterization of In Vitro Expanded Virus‐Specific T Cells for Adoptive Immunotherapy Against Virus Infection,” Japanese Journal of Infectious Diseases 71, no. 2 (2018): 122–128, https://doi.org/10.7883/yoken.JJID.2017.500.
U. Gerdemann, J. M. Keirnan, U. L. Katari, et al., “Rapidly Generated Multivirus‐Specific Cytotoxic T Lymphocytes for the Prophylaxis and Treatment of Viral Infections,” Molecular Therapy 20, no. 8 (2012): 1622–1632, https://doi.org/10.1038/mt.2012.130.
S. R. Riddell, K. S. Watanabe, J. M. Goodrich, C. R. Li, M. E. Agha, and P. D. Greenberg, “Restoration of Viral Immunity in Immunodeficient Humans by the Adoptive Transfer of T Cell Clones,” Science 257, no. 5067 (1992): 238–241, https://doi.org/10.1126/science.1352912.
A. J. Barrett and S. B. C. Prockop, “Virus‐Specific T Cells: Broadening Applicability,” Biology of Blood and Marrow Transplantation 24, no. 1 (2018): 13–18, https://doi.org/10.1016/j.bbmt.2017.10.004.VIRUS.
A. Jalili, A. Hajifathali, M. Mohammadian, et al., “Virus‐Specific T Cells: Promising Adoptive T Cell Therapy Against Infectious Diseases Following Hematopoietic Stem Cell Transplantation,” Advanced Pharmaceutical Bulletin 13, no. 3 (2023): 469–482, https://doi.org/10.34172/apb.2023.046.
M. M. Najafabadi, M. Soleimani, M. Ahmadvand, M. S. Zomorrod, and S. A. Mousavi, “In Vitro Generation of BK Polyomavirus‐Specific T Cells for Adoptive Cell Therapy in Refractory Cystitis Hemorrhagic Patients After Hematopoietic Stem Cell Transplantation,” BMC Immunology 23, no. 1 (2022): 1–8, https://doi.org/10.1186/s12865‐022‐00497‐1.
F. Hopfner, N. Möhn, B. Eiz‐Vesper, et al., “Allogeneic BK Virus‐Specific T‐Cell Treatment in 2 Patients With Progressive Multifocal Leukoencephalopathy,” Neurology(R) Neuroimmunology & NeuroInflammation 8, no. 4 (2021): 2–6, https://doi.org/10.1212/NXI.0000000000001020.
M. Muftuoglu, A. Olson, D. Marin, et al., “Allogeneic BK Virus‐Specific T Cells for Progressive Multifocal Leukoencephalopathy,” New England Journal of Medicine 379, no. 15 (2018): 1443–1451, https://doi.org/10.1056/NEJMoa1801540.
L. Grote‐Levi, N. Möhn, A. Bonifacius, et al., “Adoptive Allogeneic T‐Cell Therapy Improves the Clinical Outcome of JC Virus Granule Cell Neuronopathy: A Case Report,” Neurology(R) Neuroimmunology & NeuroInflammation 10, no. 5 (2023): 1–6, https://doi.org/10.1212/NXI.0000000000200138.
L. Krymskaya, M. C. Sharma, J. Martinez, et al., “Cross‐Reactivity of T Lymphocytes Recognizing a Human Cytotoxic T‐Lymphocyte Epitope Within BK and JC Virus VP1 Polypeptides,” Journal of Virology 79, no. 17 (2005): 11170–11178, https://doi.org/10.1128/jvi.79.17.11170‐11178.2005.
G. R. Ambalathingal, R. S. Francis, D. Corvino, et al., “Proteome‐Wide Analysis of T‐Cell Response to BK Polyomavirus in Healthy Virus Carriers and Kidney Transplant Recipients Reveals a Unique Transcriptional and Functional Profile,” Clinical & Translational Immunology 9, no. 1 (2020): e01102, https://doi.org/10.1002/cti2.1102.
M. Cioni, C. Leboeuf, P. Comoli, F. Ginevri, and H. H. Hirsch, “Characterization of Immunodominant BK Polyomavirus 9mer Epitope T Cell Responses,” American Journal of Transplantation 16, no. 4 (2016): 1193–1206, https://doi.org/10.1111/ajt.13598.
J. Mani, L. Wang, A. G. Hückelhoven, et al., “Definition and Characterization of Novel HLA‐*A02‐Restricted CD8+ T Cell Epitopes Derived From JCV Polyomavirus With Clinical Relevance,” Oncotarget 8, no. 2 (2017): 2485–2500, https://doi.org/10.18632/oncotarget.12387.
J. Li, J. Melenhorst, N. Hensel, et al., “T‐Cell Responses to Peptide Fragments of the BK Virus T Antigen: Implications for Cross‐Reactivity of Immune Response to JC Virus,” Journal of General Virology 87, no. 10 (2006): 2951–2960, https://doi.org/10.1099/vir.0.82094‐0.
M. Provenzano, L. Bracci, S. Wyler, et al., “Characterization of Highly Frequent Epitope‐Specific CD45RA+/CCR7+/‐ T Lymphocyte Responses Against p53‐Binding Domains of the Human Polyomavirus BK Large Tumor Antigen in HLA‐A*0201+ BKV‐Seropositive Donors,” Journal of Translational Medicine 4 (2006): 1–15, https://doi.org/10.1186/1479‐5876‐4‐47.
Y. Chen, J. Trofe, J. Gordon, P. Autissier, E. S. Woodle, and I. J. Koralnik, “BKV and JCV Large T Antigen‐Specific CD8+ T Cell Response in HLA A*0201+ Kidney Transplant Recipients With Polyomavirus Nephropathy and Patients With Progressive Multifocal Leukoencephalopathy,” Journal of Clinical Virology 42, no. 2 (2009): 198–202, https://doi.org/10.1016/j.jcv.2008.01.005.BKV.
B. Ramaswami, L. Popescu, C. Macedo, et al., “HLA‐A01‐, ‐A03‐, and ‐A024‐Binding Nanomeric Epitopes in Polyomavirus BK Large T Antigen,” Human Immunology 70, no. 9 (2009): 722–728, 10.1016/j.humimm.2009.05.003.
K. K. Jensen, M. Andreatta, P. Marcatili, et al., “Improved Methods for Predicting Peptide Binding Affinity to MHC Class II Molecules,” Immunology 154, no. 3 (2018): 394–406, https://doi.org/10.1111/imm.12889.
A. A. Lehmann, T. Zhang, P. A. Reche, and P. V. Lehmann, “Discordance Between the Predicted Versus the Actually Recognized CD8+ T Cell Epitopes of HCMV pp65 Antigen and Aleatory Epitope Dominance,” Frontiers in Immunology 11 (February 2021): 1–14, https://doi.org/10.3389/fimmu.2020.618428.
D. Gfeller and M. Bassani‐Sternberg, “Predicting Antigen Presentation‐What Could We Learn From a Million Peptides?,” Frontiers in Immunology 9 (July 2018): 1–17, https://doi.org/10.3389/fimmu.2018.01716.
E. Enrich, E. Campos, L. Martorell, et al., “HLA‐A, ‐B, ‐C, ‐DRB1, and ‐DQB1 Allele and Haplotype Frequencies: An Analysis of Umbilical Cord Blood Units at the Barcelona Cord Blood Bank,” HLA 94, no. 4 (2019): 347–359, https://doi.org/10.1111/tan.13644.
E. Blyth, L. Clancy, R. Simms, et al., “BK Virus‐Specific T Cells for Use in Cellular Therapy Show Specificity to Multiple Antigens and Polyfunctional Cytokine Responses,” Transplantation 92, no. 10 (2011): 1077–1084, https://doi.org/10.1097/TP.0b013e31823328c0.
V. R. Dharnidharka, W. S. Cherikh, and K. C. Abbott, “An OPTN Analysis of National Registry Data on Treatment of BK Virus Allograft Nephropathy in the United States,” Transplantation 87, no. 7 (2009): 1019–1026, https://doi.org/10.1097/TP.0b013e31819cc383.
J. Gras, A. Le Flécher, A. Dupont, et al., “Characteristics, Risk Factors and Outcome of BKV Nephropathy in Kidney Transplant Recipients: A Case‐Control Study,” BMC Infectious Diseases 23, no. 1 (2023): 74, https://doi.org/10.1186/s12879‐023‐08043‐z.
A. S. Nelson, D. Heyenbruch, J. D. Rubinstein, et al., “Virus‐Specific T‐Cell Therapy to Treat BK Polyomavirus Infection in Bone Marrow and Solid Organ Transplant Recipients,” Blood Advances 4, no. 22 (2020): 5745–5754, https://doi.org/10.1182/bloodadvances.2020003073.
E. Espada, M. P. Cheng, H. T. Kim, et al., “BK Virus–Specific T‐Cell Immune Reconstitution After Allogeneic Hematopoietic Cell Transplantation,” Blood Advances 4, no. 9 (2020): 1881–1893, https://doi.org/10.1182/bloodadvances.2019001120.
S. Sharma, V. Kumari, B. V. Kumbhar, A. Mukherjee, R. Pandey, and K. Kondabagil, “Immunoinformatics Approach for a Novel Multi‐Epitope Subunit Vaccine Design Against Various Subtypes of Influenza A Virus,” Immunobiology 226, no. 2 (2021): 152053, https://doi.org/10.1016/j.imbio.2021.152053.
S. Kanse, M. Khandelwal, R. K. Pandey, M. Khokhar, N. Desai, and B. V. Kumbhar, “Designing a Multi‐Epitope Subunit Vaccine Against VP1 Major Coat Protein of JC Polyomavirus,” Vaccines 11, no. 7 (2023): 1182, https://doi.org/10.3390/vaccines11071182.
R. Kumar Pandey, R. Ojha, A. Mishra, and P. V. Kumar, “Designing B‐ and T‐Cell Multi‐Epitope Based Subunit Vaccine Using Immunoinformatics Approach to Control Zika Virus Infection,” Journal of Cellular Biochemistry 119, no. 9 (2018): 7631–7642, https://doi.org/10.1002/jcb.27110.
B. Ramaswami, I. Popescu, C. Macedo, et al., “The Polyomavirus BK Large T‐Antigen‐Derived Peptide Elicits an HLA‐DR Promiscuous and Polyfunctional CD4+ T‐Cell Response,” Clinical and Vaccine Immunology 18, no. 5 (2011): 815–824, https://doi.org/10.1128/CVI.00487‐10.
T. A. Ahmad, A. E. Eweida, and L. H. El‐Sayed, “T‐Cell Epitope Mapping for the Design of Powerful Vaccines,” Vaccine Reports 6 (2016): 13–22, https://doi.org/10.1016/j.vacrep.2016.07.002.
R. K. S. Ahmed and M. J. Maeurer, “T‐Cell Epitope Mapping,” Methods in Molecular Biology, Epitope Mapping Protocols 524 (2009): 427–438, https://doi.org/10.1007/978‐1‐59745‐450‐6.
S. J. Hyun, H. J. Sohn, H. J. Lee, et al., “Comprehensive Analysis of Cytomegalovirus pp65 Antigen‐Specific CD8+ T Cell Responses According to Human Leukocyte Antigen Class I Allotypes and Intraindividual Dominance,” Frontiers in Immunology 8 (November 2017): 1591, https://doi.org/10.3389/fimmu.2017.01591.
Y. Chen, J. Trofe, J. Gordon, et al., “Interplay of Cellular and Humoral Immune Responses Against BK Virus in Kidney Transplant Recipients With Polyomavirus Nephropathy,” Journal of Virology 80, no. 7 (2006): 3495–3505, https://doi.org/10.1128/jvi.80.7.3495‐3505.2006.
K. Mueller, T. Schachtner, A. Sattler, et al., “BK‐VP3 as a New Target of Cellular Immunity in BK Virus Infection,” Transplantation 91, no. 1 (2011): 100–107, https://doi.org/10.1097/TP.0b013e3181fe1335.
J. Sidney, B. Peters, N. Frahm, C. Brander, and A. Sette, “HLA Class I Supertypes: A Revised and Updated Classification,” BMC Immunology 9 (2008): 1–15, https://doi.org/10.1186/1471‐2172‐9‐1.
S. Harjanto, L. F. P. Ng, and J. C. Tong, “Clustering HLA Class I Superfamilies Using Structural Interaction Patterns,” PLoS One 9, no. 1 (2014): e86655, https://doi.org/10.1371/journal.pone.0086655.
M. K. Sahoo, S. K. Tan, S. F. Chen, et al., “Limited Variation in BK Virus T‐Cell Epitopes Revealed by Next‐Generation Sequencing,” Journal of Clinical Microbiology 53, no. 10 (2015): 3226–3233, https://doi.org/10.1128/JCM.01385‐15.
I. Jelčić, L. Aly, T. M. C. Binder, et al., “T Cell Epitope Mapping of JC Polyoma Virus‐Encoded Proteome Reveals Reduced T Cell Responses in HLA‐DRB1*04:01 + Donors,” Journal of Virology 87, no. 6 (2013): 3393–3408, https://doi.org/10.1128/jvi.02803‐12.
I. Tzannou, A. Papadopoulou, S. Naik, et al., “Off‐the‐Shelf Virus‐Specific T Cells to Treat BK Virus, Human Herpesvirus 6, Cytomegalovirus, Epstein‐Barr Virus, and Adenovirus Infections After Allogeneic Hematopoietic Stem‐Cell Transplantation,” Journal of Clinical Oncology 35, no. 31 (2017): 3547–3557, https://doi.org/10.1200/JCO.2017.73.0655.
A. Papadopoulou, U. Gerdemann, U. L. Katari, et al., “Activity of Broad‐Spectrum T Cells as Treatment for AdV, EBV, CMV, BKV, and HHV6 Infections After HSCT Anastasia,” Science Translational Medicine 6, no. 242 (2014): 242ra83, https://doi.org/10.1126/scitranslmed.3008825.
M. Koldehoff, B. Eiz‐Vesper, B. Maecker‐Kolhoff, et al., “Long‐Term Follow‐Up After Adoptive Transfer of BK‐Virus‐Specific T Cells in Hematopoietic Stem Cell Transplant Recipients,” Vaccines 11, no. 4 (2023): 845, https://doi.org/10.3390/vaccines11040845.
J. Craddock, “TETRAVI Multivirus CTL for Treatment of EBV, CMV, Adenovirus, and BK Infections Post Allogeneic SCT. (TETRAVI),” NCT04013802, 2024, https://clinicaltrials.gov/study/NCT04013802.
M. J. Steinhardt, E. Wiercinska, M. Pham, et al., “Progressive Multifocal Leukoencephalopathy in a Patient Post Allo‐HCT Successfully Treated With JC Virus Specific Donor Lymphocytes,” Journal of Translational Medicine 18, no. 1 (2020): 1–6, https://doi.org/10.1186/s12967‐020‐02337‐5.
A. Balduzzi, G. Lucchini, H. H. Hirsch, et al., “Polyomavirus JC‐Targeted T‐Cell Therapy for Progressive Multiple Leukoencephalopathy in a Hematopoietic Cell Transplantation Recipient,” Bone Marrow Transplantation 46, no. 7 (2011): 987–992, https://doi.org/10.1038/bmt.2010.221.
A. N. Hasan, E. Doubrovina, R. Sottile, et al., “Dominant Epitopes Presented by Prevalent HLA Alleles Permit Wide Use of Banked CMVpp65 T Cells in Adoptive Therapy,” Blood Advances 6, no. 16 (2022): 4859–4872, https://doi.org/10.1182/bloodadvances.2022007005.
Contributed Indexing: Keywords: BK virus; ELISpot; HLA; HLA‐binding; LTA; T‐cell epitope; VP1; VP2/VP3
Substance Nomenclature: 0 (Immunodominant Epitopes)
0 (Epitopes, T-Lymphocyte)
0 (HLA Antigens)
0 (Viral Proteins)
Entry Date(s): Date Created: 20241022 Date Completed: 20241022 Latest Revision: 20241025
Update Code: 20260130
DOI: 10.1111/tan.15722
PMID: 39435889
Βάση Δεδομένων: MEDLINE
Περιγραφή
ISSN:2059-2310
DOI:10.1111/tan.15722