Multimer monitoring of CMV-specific T cells in research and in clinical applications

Borchers, Sylvia; Ogonek, Justyna; Varanasi, Pavankumar R.; Tischer, Sabine; Bremm, Melanie; Eiz-Vesper, Britta; Koehl, Ulrike; Weissinger, Eva M.

doi:10.1016/j.diagmicrobio.2013.11.007

Cited by 18Cytomegalovirus and herpesvirus researchT-cell and B-cell ImmunologyImmunotherapy and Immune Responses

Multimer monitoring of CMV-specific T cells in research and in clinical applications

Borchers, Sylvia, Ogonek, Justyna, Varanasi, Pavankumar R., Tischer, Sabine, Bremm, Melanie, Eiz-Vesper, Britta, Koehl, Ulrike, Weissinger, Eva M.·2014·Diagnostic Microbiology and Infectious Disease

DOI 10.1016/j.diagmicrobio.2013.11.007

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Abstract

Multimer monitoring has become a standard technique for detection of antigen-specific T cells. The term "multimer" refers to a group of reagents based on the multimerisation of molecules in order to raise avidity and thus stabilize binding to their ligand. Multimers for detection of antigen-specific T-cell responses are based on major histocompatibility complex class I peptide complexes. Multimer staining enables fast and direct visualization of antigen-specific T cells; thus, it is widely applied to assess antiviral immunity, e.g., monitor patients in vaccination trials or confirm purity of cell products for adoptive transfer. Assessment of T-cell immunity against persistent pathogens like cytomegalovirus (CMV) is of major importance in immunosuppressed patients. Recent advancements of multimers facilitate reversible labeling and allow isolation of epitope-specific T cells for adoptive transfer. Here, we give an overview on the different multimers and their applications, with an emphasis on CMV-specific T-cell responses.

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This methodology is limited to common human leukocyte antigen (HLA)-types and is usually restricted to immunodominant antigens rather than the full spectrum of virus proteins that T cells target.
“However, this methodology is limited to common human leukocyte antigen (HLA)-types and is usually restricted to immunodominant antigens rather than the full spectrum of virus proteins that T cells target (Borchers et al. 2014).”
From Is immunosenescence influenced by our lifetime “dose” of exercise? (2016) · cites this paper as Borchers et al. 2014
This methodology will not identify the proportion of antigen-specific cells that are senescent/exhausted, unless functional measurements are incorporated in tandem or post hoc.
“Moreover, this methodology will not identify the proportion of antigen-specific cells that are senescent/exhausted, unless functional measurements are incorporated in tandem or post hoc (Borchers et al. 2014; Klenerman et al. 2002).”
From Is immunosenescence influenced by our lifetime “dose” of exercise? (2016) · cites this paper as Borchers et al. 2014

Phenotypic Analysis of Antigen-Specific T Lymphocytes
Altman, J. D., Moss, P. A. H., Goulder, P. J. R., Barouch, D. H., McHeyzer-Williams, M. G., Bell, J. I., McMichael, A. J., & Davis, M. M. (1996) · Science · doi:10.1126/science.274.5284.94 · Cited by 3,544 · see citing works
Brefeldin A: insights into the control of membrane traffic and organelle structure.
Klausner, R. D., Donaldson, J. G., & Lippincott‐Schwartz, J. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.116.5.1071 · Cited by 1,852 · see citing works
Reconstitution of Cellular Immunity against Cytomegalovirus in Recipients of Allogeneic Bone Marrow by Transfer of T-Cell Clones from the Donor
Walter, E. A., Greenberg, P. D., Gilbert, M. J., Finch, R. J., Watanabe, K. S., Thomas, E. D., & Riddell, S. R. (1995) · New England Journal of Medicine · doi:10.1056/nejm199510193331603 · Cited by 1,766 · see citing works
Broadly targeted human cytomegalovirus-specific CD4 <b>+</b> and CD8 <b>+</b> T cells dominate the memory compartments of exposed subjects
Sylwester, A. W., Mitchell, B. L., Edgar, J. B., Taormina, C., Pelte, C., Ruchti, F., Sleath, P. R., Grabstein, K. H., Hosken, N. A., Kern, F., et al. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20050882 · Cited by 1,339 · cited 1× · see citing works
“However, not all individuals do react to the same extend, as the immune response is very broad (Sylwester et al., 2005).”
Background
Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients
Lee, P. P., Yee, C., Savage, P. A., Fong, L. H., Brockstedt, D. G., Weber, J. S., Johnson, D. L., Swetter, S. M., Thompson, J. A., Greenberg, P. D., et al. (1999) · Nature Medicine · doi:10.1038/9525 · Cited by 1,117 · see citing works
Detection of intracellular cytokines by flow cytometry
Jung, T., Schauer, U., Heusser, C., Neumann, C. R., & Rieger, C. (1993) · Journal of Immunological Methods · doi:10.1016/0022-1759(93)90158-4 · Cited by 976 · see citing works
CD1 Recognition by Mouse NK1 + T Lymphocytes
Bendelac, A. S., Lantz, O. J., Quimby, M. E., Yewdell, J. W., Bennink, J. R., & Brutkiewicz, R. R. (1995) · Science · doi:10.1126/science.7538697 · Cited by 912 · see citing works
Tracking the Response of Natural Killer T Cells to a Glycolipid Antigen Using Cd1d Tetramers
Matsuda, J. L., Naidenko, O. V., Gapin, L., Nakayama, T., Taniguchi, M., Wang, C.-R., Koezuka, Y., & Kronenberg, M. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.5.741 · Cited by 887 · see citing works
Infusion of cytomegalovirus (CMV)–specific T cells for the treatment of CMV infection not responding to antiviral chemotherapy
Einsele, H., Roosnek, E. E., Rufer, N., Sinzger, C., Riegler, S., Löffler, J., Grigoleit, U., Moris, A., Rammensee, H., Kanz, L., et al. (2002) · Blood · doi:10.1182/blood.v99.11.3916 · Cited by 699 · see citing works
In Vivo Identification of Glycolipid Antigen–Specific T Cells Using Fluorescent Cd1d Tetramers
Benlagha, K., Weiss, A. H., Beavis, A. J., Teyton, L., & Bendelac, A. S. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.191.11.1895 · Cited by 555 · see citing works
Ex Vivo Staining of Metastatic Lymph Nodes by Class I Major Histocompatibility Complex Tetramers Reveals High Numbers of Antigen-experienced Tumor-specific Cytolytic T Lymphocytes
Romero, P. J., Dunbar, P. R., Valmori, D., Pittet, M. J., Ogg, G. S., Rimoldi, D., Chen, J., Líénard, D., Cerottini, J., & Cerundolo, V. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.188.9.1641 · Cited by 521 · see citing works
Adoptive transfer of cytomegalovirus-specific CTL to stem cell transplant patients after selection by HLA–peptide tetramers
Cobbold, M., Khan, N., Pourgheysari, B., Tauro, S., McDonald, D., Osman, H., Assenmacher, M., Billingham, L., Steward, C., Crawley, C., et al. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20040613 · Cited by 480 · see citing works
Antiviral drugs for cytomegalovirus diseases
Biron, K. K. (2006) · Antiviral Research · doi:10.1016/j.antiviral.2006.05.002 · Cited by 469 · see citing works
Detection of Antigen-Specific T Cells with Multivalent Soluble Class II MHC Covalent Peptide Complexes
Crawford, F., Kozono, H., White, J., Marrack, P., & Kappler, J. W. (1998) · Immunity · doi:10.1016/s1074-7613(00)80572-5 · Cited by 459 · see citing works
Assessment of Cytokines by Immunofluorescence and the Paraformaldehyde‐Saponin Procedure
Sander, B., Andersson, J., & Andersson, U. (1991) · Immunological Reviews · doi:10.1111/j.1600-065x.1991.tb00578.x · Cited by 456 · see citing works
Cytomegalovirus in hematopoietic stem cell transplant recipients: current status, known challenges, and future strategies
Boeckh, M., Nichols, W. G., Papanicolaou, G. A., et al. (2003) · Transplantation and Cellular Therapy · doi:10.1016/s1083-8791(03)00287-8 · Cited by 432 · see citing works
Isolation of High Avidity Melanoma-Reactive CTL from Heterogeneous Populations Using Peptide-MHC Tetramers
Yee, C., Savage, P. A., Lee, P. P., Davis, M. M., & Greenberg, P. D. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.4.2227 · Cited by 415 · see citing works
MHC class II tetramers identify peptide-specific human CD4+ T cells proliferating in response to influenza A antigen
Novak, E. J., Liu, A. W., Nepom, G. T., & Kwok, W. W. (1999) · Journal of Clinical Investigation · doi:10.1172/jci8476 · Cited by 376 · see citing works
Treatment of Epstein-Barr-virus-positive post-transplantation lymphoproliferative disease with partly HLA-matched allogeneic cytotoxic T cells
Haque, T., Wilkie, G. M., Taylor, C., et al. (2002) · The Lancet · doi:10.1016/s0140-6736(02)09672-1 · Cited by 365 · see citing works
Protection from cytomegalovirus after transplantation is correlated with immediate early 1–specific CD8 T cells
Bunde, T., Kirchner, A., Hoffmeister, B., Habedank, D., Hetzer, R., Черепнев, Г. В., Prösch, S., Reinke, P., Volk, H., Lehmkuhl, H. B., et al. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20042384 · Cited by 364 · see citing works
Direct visualization of cytomegalovirus-specific T-cell reconstitution after allogeneic stem cell transplantation
Cwynarski, K., Ainsworth, J., Cobbold, M., Wagner, S. D., Mahendra, P., Apperley, J. F., Goldman, J. M., Craddock, C., & Moss, P. A. H. (2001) · Blood · doi:10.1182/blood.v97.5.1232 · Cited by 292 · see citing works
Tetramer-based quantification of cytomegalovirus (CMV)–specific CD8+ T lymphocytes in T-cell–depleted stem cell grafts and after transplantation may identify patients at risk for progressive CMV infection
Gratama, J. W., van Esser, J. W. J., Lamers, C. H. J., Tournay, C., Löwenberg, B., Bolhuis, R. L. H., & Cornelissen, J. J. (2001) · Blood · doi:10.1182/blood.v98.5.1358 · Cited by 277 · see citing works
Critical Role for Cd8 in T Cell Receptor Binding and Activation by Peptide/Major Histocompatibility Complex Multimers
Daniëls, M. A., & Jameson, S. C. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.191.2.335 · Cited by 269 · see citing works
Optimization and validation of an 8-color intracellular cytokine staining (ICS) assay to quantify antigen-specific T cells induced by vaccination
Horton, H., Thomas, E. P., Stucky, J., Frank, I., Moodie, Z., Huang, Y., Chiu, Y.-L., McElrath, M. J., & Rosa, S. C. D. (2007) · Journal of Immunological Methods · doi:10.1016/j.jim.2007.03.002 · Cited by 260 · see citing works
Rapidly Generated Multivirus-specific Cytotoxic T Lymphocytes for the Prophylaxis and Treatment of Viral Infections
Gerdemann, U., Keirnan, J. M., Katari, U. L., et al. (2012) · Molecular Therapy · doi:10.1038/mt.2012.130 · Cited by 251 · see citing works
Adoptive transfer and selective reconstitution of streptamer‐selected cytomegalovirus‐specific CD8+ T cells leads to virus clearance in patients after allogeneic peripheral blood stem cell transplantation
Schmitt, A., Tonn, T., Busch, D. H., Grigoleit, G. U., Einsele, H., Odendahl, M., Germeroth, L., Ringhoffer, M., Ringhoffer, S., Wiesneth, M., et al. (2010) · Transfusion · doi:10.1111/j.1537-2995.2010.02940.x · Cited by 226 · see citing works
Reversible MHC multimer staining for functional isolation of T-cell populations and effective adoptive transfer
Knabel, M., Franz, T. J., Schiemann, M., Wulf, A., Villmow, B., Schmidt, B., Bernhard, H., Wagner, H., & Busch, D. H. (2002) · Nature Medicine · doi:10.1038/nm0602-631 · Cited by 211 · see citing works
Cytomegalovirus reactivation following allogeneic stem cell transplantation is associated with the presence of dysfunctional antigen-specific CD8+ T cells
Özdemir, E., John, L. S. S., Gillespie, G. M. A., Rowland‐Jones, S., Champlin, R. E., Molldrem, J. J., & Komanduri, K. V. (2002) · Blood · doi:10.1182/blood-2002-05-1387 · Cited by 211 · see citing works
“MIATA”—Minimal Information about T Cell Assays
Janetzki, S., Britten, C. M., Kalos, M. D., Levitsky, H. I., Maecker, H. T., Melief, C. J. M., Old, L. J., Romero, P. J., Hoos, A., & Davis, M. M. (2009) · Immunity · doi:10.1016/j.immuni.2009.09.007 · Cited by 192 · see citing works
Enumeration of human antigen–specific naive CD8+ T cells reveals conserved precursor frequencies
Alanio, C., Lemaı̂tre, F., Law, H., Hasan, M., & Albert, M. L. (2010) · Blood · doi:10.1182/blood-2009-10-251124 · Cited by 179 · see citing works
Rapid generation of combined CMV-specific CD4+ and CD8+ T-cell lines for adoptive transfer into recipients of allogeneic stem cell transplants
Rauser, G., Einsele, H., Sinzger, C., Wernet, D., Kuntz, G., Assenmacher, M., Campbell, J. D. M., & Topp, M. S. (2003) · Blood · doi:10.1182/blood-2003-09-3056 · Cited by 166 · see citing works
Impact of donor CMV status on viral infection and reconstitution of multifunction CMV-specific T cells in CMV-positive transplant recipients
Zhou, W., Longmate, J., Lacey, S. F., Palmer, J. M., Gallez-Hawkins, G. M., Thao, L., Spielberger, R. T., Nakamura, R., Forman, S. J., Zaia, J. A., et al. (2009) · Blood · doi:10.1182/blood-2009-02-203307 · Cited by 151 · see citing works
The CIMT-monitoring panel: a two-step approach to harmonize the enumeration of antigen-specific CD8+ T lymphocytes by structural and functional assays
Britten, C. M., Gouttefangeas, C., Welters, M. J. P., Pawelec, G., Koch, S. D., Ottensmeier, C. H. H., Mander, A., Walter, S., Paschen, A., Müller‐Berghaus, J., et al. (2007) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-007-0378-0 · Cited by 143 · see citing works
Direct enumeration of Borrelia -reactive CD4 T cells ex vivo by using MHC class II tetramers
Meyer, A. L., Trollmo, C., Crawford, F., Marrack, P., Steere, A. C., Huber, B. T., Kappler, J. W., & Hafler, D. A. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.190335897 · Cited by 142 · see citing works
A soluble divalent class I major histocompatibility complex molecule inhibits alloreactive T cells at nanomolar concentrations.
Porto, J. D., Johansen, T. E., Čatipović, B., et al. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.14.6671 · Cited by 141 · see citing works
Ex Vivo Expansion and Prophylactic Infusion of CMV-pp65 Peptide-Specific Cytotoxic T-Lymphocytes following Allogeneic Hematopoietic Stem Cell Transplantation
Micklethwaite, K. P., Hansen, A. M., Foster, A. E., et al. (2007) · Transplantation and Cellular Therapy · doi:10.1016/j.bbmt.2007.02.004 · Cited by 134 · see citing works
Cytomegalovirus‐Specific Cellular Immune Responses and Viremia in Recipients of Allogeneic Stem Cell Transplants
Aubert, G., Hassan‐Walker, A. F., Madrigal, J. A., Emery, V. C., Morte, C., Grace, S., Koh, M., Potter, M. N., Prentice, H. G., Dodi, I. A., et al. (2001) · The Journal of Infectious Diseases · doi:10.1086/323354 · Cited by 127 · see citing works
Interrogating the repertoire: broadening the scope of peptide–MHC multimer analysis
Davis, M. M., Altman, J. D., & Newell, E. W. (2011) · Nature Reviews Immunology · doi:10.1038/nri3020 · Cited by 124 · see citing works
RECONSTITUTION OF CELLULAR IMMUNITY AGAINST CYTOMEGALOVIRUS IN RECIPIENTS OF ALLOGENEIC BONE MARROW BY TRANSFER OF T-CELL CLONES FROM THE DONOR
Alter, E. L. A. W., Hilip, P., Reenberg, D. G., Ilbert, M. A. J. G., Inch, R. O. J. F., Atanabe, S. W., Onnall, E. D., Homas, T., & Iddell, S. T. R. R. (2011) · Cited by 117 · see citing works
Immune monitoring with iTAg MHC Tetramers for prediction of recurrent or persistent cytomegalovirus infection or disease in allogeneic hematopoietic stem cell transplant recipients: a prospective multicenter study
Gratama, J. W., Boeckh, M., Nakamura, R., Cornelissen, J. J., Brooimans, R. A., Zaia, J. A., Forman, S. J., Gaal, K. K., Bray, K. R., Gasior, G. H., et al. (2010) · Blood · doi:10.1182/blood-2010-03-273508 · Cited by 111 · see citing works
Human cytomegalovirus-specific CD4+ and CD8+ T-cell reconstitution in adult allogeneic hematopoietic stem cell transplant recipients and immune control of viral infection
Lilleri, D., Fornara, C., Chiesa, A., Caldera, D., Alessandrino, E. P., & Gerna, G. (2008) · Haematologica · doi:10.3324/haematol.11912 · Cited by 106 · see citing works
Prospective simultaneous quantification of human cytomegalovirus-specific CD4+ and CD8+ T-cell reconstitution in young recipients of allogeneic hematopoietic stem cell transplants
Lilleri, D., Gerna, G., Fornara, C., et al. (2006) · Blood · doi:10.1182/blood-2005-11-012864 · Cited by 100 · see citing works
Relative dominance of HLA-B*07 restricted CD8+ T-Lymphocyte immune responses to human cytomegalovirus pp65 in persons sharing HLA-A*02 and HLA-B*07 alleles
Lacey, S. F., Villacres, M. C., Rosa, C. L., Wang, Z., Longmate, J., Martinez, J., Brewer, J. C., Mekhoubad, S., Maas, R., Leedom, J. M., et al. (2003) · Human Immunology · doi:10.1016/s0198-8859(03)00028-4 · Cited by 95 · see citing works
CHARACTERIZATION OF CMVpp65-SPECIFIC CD8+ T LYMPHOCYTES USING MHC TETRAMERS IN KIDNEY TRANSPLANT PATIENTS AND HEALTHY PARTICIPANTS1
Engstrand, M., Tournay, C., Peyrat, M. A., Eriksson, B., Wadström, J., Wirgart, B. Z., Romagn, F., Bonneville, M., tterman, T. H. T., & Korsgren, O. (2000) · Transplantation · doi:10.1097/00007890-200006150-00005 · Cited by 89 · see citing works
Population analysis of antiviral T cell responses using MHC class I-peptide tetramers
Komatsu, H., Sierro, S. R., Cuero, A., & Klenerman, P. (2003) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.2003.02266.x · Cited by 86 · see citing works
Monitoring cytomegalovirus IE‐1 and pp65‐specific CD4+ and CD8+ T‐cell responses after allogeneic stem cell transplantation may identify patients at risk for recurrent CMV reactivations
Gratama, J. W., Brooimans, R. A., van der Holt, B., Sintnicolaas, K., van Doornum, G., Niesters, H. G. M., Löwenberg, B., & Cornelissen, J. J. (2008) · Cytometry Part B Clinical Cytometry · doi:10.1002/cyto.b.20420 · Cited by 80 · see citing works
CMV-, EBV- and ADV-Specific T Cell Immunity: Screening and Monitoring of Potential Third-Party Donors to Improve Post-Transplantation Outcome
Sukdolak, C., Tischer, S., Dieks, D., Figueiredo, C., Goudeva, L., Heuft, H., Verboom, M., Immenschuh, S., Heim, A., Borchers, S., et al. (2013) · Transplantation and Cellular Therapy · doi:10.1016/j.bbmt.2013.07.015 · Cited by 80 · see citing works
Self-citation
Natural Killer T cell obsession with self-antigens
Gapin, L., Godfrey, D. I., & Rossjohn, J. (2013) · Current Opinion in Immunology · doi:10.1016/j.coi.2013.01.002 · Cited by 80 · see citing works
Unique Strengths of ELISPOT for T Cell Diagnostics
Lehmann, P., & Zhang, W. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-325-7_1 · Cited by 78 · see citing works
Enumerating Antigen-Specific T-Cell Responses in Peripheral Blood
Hobeika, A. C., Morse, M. A., Osada, T., Ghanayem, M., Niedzwiecki, D., Barrier, R. C., Lyerly, H. K., & Clay, T. M. (2004) · Journal of Immunotherapy · doi:10.1097/00002371-200501000-00008 · Cited by 72 · see citing works
New Methods for Assessing T-Cell Responses
Bercovici, N., Duffour, M., Agrawal, S., Salcedo, M., & Abastado, J. (2000) · Clinical and Diagnostic Laboratory Immunology · doi:10.1128/cdli.7.6.859-864.2000 · Cited by 71 · see citing works
Conclusions and Future Perspectives
Fanelli, R. (2011) · doi:10.1002/9781118000816.ch19 · Cited by 70 · see citing works
CMV-specific T cell therapy
Einsele, H., Kapp, M., & Grigoleit, G. U. (2007) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2007.07.002 · Cited by 69 · see citing works
Harmonization guidelines for HLA-peptide multimer assays derived from results of a large scale international proficiency panel of the Cancer Vaccine Consortium
for the HLA-peptide Multimer Proficiency Panel of the CVC-CRI Immune Assay Working Group, Britten, C. M., Janetzki, S., Ben‐Porat, L., Clay, T. M., Kalos, M. D., Maecker, H. T., Odunsi, K. O., Pride, M. W., Old, L. J., et al. (2009) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-009-0681-z · Cited by 65 · see citing works
Cellular responses to cytomegalovirus in immunosuppressed patients: circulating CD8+ T cells recognizing CMVpp65 are present but display functional impairment
Engstrand, M., Lidehäll, A. K., Tötterman, T. H., et al. (2003) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.2003.02098.x · Cited by 64 · see citing works
Dextramers: New generation of fluorescent MHC class I/peptide multimers for visualization of antigen-specific CD8+ T cells
Batard, P., Peterson, D. A., Devêvre, E., Guillaume, P., Cerottini, J., Rimoldi, D., Speiser, D. E., Winther, L., & Romero, P. J. (2006) · Journal of Immunological Methods · doi:10.1016/j.jim.2006.01.006 · Cited by 61 · see citing works
Monitoring of Human Cytomegalovirus and Virus-Specific T-Cell Response in Young Patients Receiving Allogeneic Hematopoietic Stem Cell Transplantation
Lilleri, D., Gerna, G., Zelini, P., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041648 · Cited by 60 · see citing works
Assessment of cellular immunity to human cytomegalovirus in recipients of allogeneic stem cell transplants
Lacey, S. F., Diamond, D. J., & Zaia, J. A. (2004) · Transplantation and Cellular Therapy · doi:10.1016/j.bbmt.2003.12.004 · Cited by 59 · see citing works
Purification of cytomegalovirus‐specific CD8 T cells from peripheral blood using HLA–peptide tetramers
Keenan, R., Ainsworth, J., Khan, N., et al. (2001) · British Journal of Haematology · doi:10.1046/j.1365-2141.2001.03106.x · Cited by 59 · see citing works
Tetramer monitoring to assess risk factors for recurrent cytomegalovirus reactivation and reconstitution of antiviral immunity post allogeneic hematopoietic stem cell transplantation
Borchers, S., Luther, S., Lips, U., et al. (2011) · Transplant Infectious Disease · doi:10.1111/j.1399-3062.2011.00626.x · Cited by 54 · see citing works
Self-citation
Pretransplantation CMV-specific T cells protect recipients of T-cell-depleted grafts against CMV-related complications
Chalandon, Y., Degermann, S., Villard, J., et al. (2005) · Blood · doi:10.1182/blood-2005-07-2746 · Cited by 54 · see citing works
Anti-CD8 Antibodies Can Inhibit or Enhance Peptide-MHC Class I (pMHCI) Multimer Binding: This Is Paralleled by Their Effects on CTL Activation and Occurs in the Absence of an Interaction between pMHCI and CD8 on the Cell Surface
Wooldridge, L., Hutchinson, S., Choi, E. M.-L., et al. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.12.6650 · Cited by 54 · see citing works
Multiplex mapping of CD4 T cell epitopes using class II tetramers
Yang, J., James, E. A., Huston, L., Danke, N. A., Liu, A. W., & Kwok, W. W. (2006) · Clinical Immunology · doi:10.1016/j.clim.2006.03.008 · Cited by 52 · see citing works
Soluble, High-Affinity Dimers of T-Cell Receptors and Class II Major Histocompatibility Complexes: Biochemical Probes for Analysis and Modulation of Immune Responses
Lebowitz, M., O’Herrin, S. M., Hamad, A.-R. A., Fahmy, T. M., Marguet, D., Barnes, N. C., Pardoll, D. M., Bieler, J. G., & Schneck, J. P. (1999) · Cellular Immunology · doi:10.1006/cimm.1999.1441 · Cited by 47 · see citing works
Protective Immunity Transferred by Infusion of Cytomegalovirus-Specific CD8+ T Cells within Donor Grafts: Its Associations with Cytomegalovirus Reactivation Following Unmanipulated Allogeneic Hematopoietic Stem Cell Transplantation
Luo, X., Huang, X., Liu, K., et al. (2010) · Transplantation and Cellular Therapy · doi:10.1016/j.bbmt.2010.02.007 · Cited by 46 · see citing works
Production of good manufacturing practice-grade cytotoxic T lymphocytes specific for Epstein–Barr virus, cytomegalovirus and adenovirus to prevent or treat viral infections post-allogeneic hematopoietic stem cell transplant
Sili, U., Leen, A. M., Vera, J. F., et al. (2011) · Cytotherapy · doi:10.3109/14653249.2011.636963 · Cited by 45 · see citing works
Detection of autoreactive CD4 T cells using major histocompatibility complex class II dextramers
Massilamany, C., Upadhyaya, B., Gangaplara, A., KUSZYNSKI, C. A., & Reddy, J. (2011) · BMC Immunology · doi:10.1186/1471-2172-12-40 · Cited by 45 · see citing works
Human CD8 co–receptor is strictly involved in MHC–peptide tetramer–TCR binding and T cell activation
Campanelli, R., Palermo, B., Garbelli, S., et al. (2002) · International Immunology · doi:10.1093/intimm/14.1.39 · Cited by 45 · see citing works
Multimer Staining of Cytomegalovirus Phosphoprotein 65–Specific T Cells for Diagnosis and Therapeutic Purposes: A Comparative Study
Yao, J., Bechter, C., Wiesneth, M., et al. (2008) · Clinical Infectious Diseases · doi:10.1086/587749 · Cited by 44 · see citing works
Multimer technologies for detection and adoptive transfer of antigen-specific T cells
Casalegno‐Garduño, R., Schmitt, A., Yao, J., Wang, X., Xu, X., Freund, M., & Schmitt, M. W. (2009) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-009-0778-4 · Cited by 41 · see citing works
Class II major histocompatibility complex–peptide tetramer staining in relation to functional avidity and T cell receptor diversity in the mouse CD4+ T cell response to a rheumatoid arthritis–associated antigen
Falta, M. T., Fontenot, A. P., Rosloniec, E. F., Crawford, F., Roark, C. L., Bill, J. R., Marrack, P., Kappler, J. W., & Kotzin, B. L. (2005) · Arthritis & Rheumatism · doi:10.1002/art.21098 · Cited by 34 · see citing works
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Borchers, S., Bremm, M., Lehrnbecher, T., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050248 · Cited by 33 · see citing works
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Schneck, J. P., Slansky, J. E., O’Herrin, S. M., et al. (2000) · Current Protocols in Immunology · doi:10.1002/0471142735.im1702s35 · Cited by 32 · see citing works
Simultaneous Generation of Multivirus-specific and Regulatory T Cells for Adoptive Immunotherapy
Lugthart, G., Albon, S. J., Ricciardelli, I., et al. (2011) · Journal of Immunotherapy · doi:10.1097/cji.0b013e31823569e2 · Cited by 29 · see citing works
Analytical performance of a standardized single‐platform MHC tetramer assay for the identification and enumeration of CMV‐specific CD8+ T lymphocytes
Brooimans, R. A., Boyce, C. S., Popma, J., Broyles, D. A., Gratama, J. W., Southwick, P. C., & Keeney, M. (2008) · Cytometry Part A · doi:10.1002/cyto.a.20641 · Cited by 25 · see citing works
Evaluation of cytomegalovirus-specific cytotoxic T-lymphocytes in patients with the HLA-A*02 or HLA-A*24 phenotype undergoing hematopoietic stem cell transplantation
Morita, Y., Hosokawa, M., Ebisawa, M., Sugita, T., Miura, O., Takaue, Y., & Heike, Y. (2005) · Bone Marrow Transplantation · doi:10.1038/sj.bmt.1705133 · Cited by 24 · see citing works
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Bunse, C. E., Borchers, S., Varanasi, P. R., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077925 · Cited by 24 · see citing works
Self-citation
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Giest, S., Grace, S., Senegaglia, A. C., Pasqüini, R., Gonzalo‐Daganzo, R. M., Mn, F., Mackinnon, S., Madrigal, J. A., & Travers, P. J. (2009) · British Journal of Haematology · doi:10.1111/j.1365-2141.2009.07969.x · Cited by 22 · see citing works
HLA tetramers and anti-CMV immune responses: from epitope to immunotherapy
Chen, F., Aubert, G., Travers, P. M., et al. (2002) · Cytotherapy · doi:10.1080/146532402317251518 · Cited by 22 · see citing works
Enumeration of antigen‐specific CD8+ T lymphocytes by single‐platform, HLA tetramer‐based flow cytometry: A European multicenter evaluation
Heijnen, I., Barnett, D. B., Arroz, M. J., Barry, S. M., Bonneville, M., Brando, B., D'hautcourt, J., Kern, F., Tötterman, T. H., Marijt, E. W. A., et al. (2004) · Cytometry Part B Clinical Cytometry · doi:10.1002/cyto.b.20028 · Cited by 21 · see citing works
Characterizing the Impact of CD8 Antibodies on Class I MHC Multimer Binding
Holman, P. O., Walsh, E. R., & Jameson, S. C. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.7.3986 · Cited by 19 · see citing works
A recombinant human HLA-class I antigen linked to dextran elicits innate and adaptive immune responses
Schøller, J., Singh, M., Bergmeier, L. A., Brunstedt, K., Wang, Y., Whittall, T., Rahman, D., Pido-Lopez, J., & Lehner, T. (2010) · Journal of Immunological Methods · doi:10.1016/j.jim.2010.05.008 · Cited by 17 · see citing works
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Ramírez, N., & Olavarría, E. (2013) · Bone Marrow Transplantation · doi:10.1038/bmt.2012.262 · Cited by 16 · see citing works
Successful isolation and expansion of CMV ‐reactive T cells from G ‐ CSF mobilized donors that retain a strong cytotoxic effector function
Samuel, E. R., Newton, K. R., Mackinnon, S., et al. (2012) · British Journal of Haematology · doi:10.1111/bjh.12082 · Cited by 16 · see citing works
Reconstitution of Cytomegalovirus Specific T Cells after Pediatric Allogeneic Stem Cell Transplantation: Results from a Pilot Study Using a Multi-Allele CMV Tetramer Group
Koehl, U., Dirkwinkel, E., Koenig, M., et al. (2008) · Klinische Pädiatrie · doi:10.1055/s-0028-1086029 · Cited by 15 · see citing works
Self-citation
Establishment of the reversible peptide-major histocompatibility complex (pMHC) class I Histamer technology: tool for visualization and selection of functionally active antigen-specific CD8+ T lymphocytes
Tischer, S., Kaireit, T. F., Figueiredo, C., Hiller, O., Maecker‐Kolhoff, B., Geyeregger, R., Immenschuh, S., Blasczyk, R., & Eiz‐Vesper, B. (2012) · International Immunology · doi:10.1093/intimm/dxs059 · Cited by 15 · see citing works
Self-citation
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Borchers, S., Weissinger, E. M., Pabst, B., et al. (2013) · Transplant Infectious Disease · doi:10.1111/tid.12101 · Cited by 13 · see citing works
Self-citation
Analysis of HLA-A24-restricted CMVpp65 peptide-specific CTL with HLA-A*2402-CMVpp65 tetramer
Akiyama, Y., Kuzushima, K., Tsurumi, T., et al. (2004) · Immunology Letters · doi:10.1016/j.imlet.2004.07.010 · Cited by 11 · see citing works
Validation of Cytomegalovirus Immune Competence Assays for the Characterization of CD8+T Cell Responses Posttransplant
Ravkov, E. V., Pavlov, I. Y., Hanson, K. E., & Delgado, J. C. (2012) · Clinical and Developmental Immunology · doi:10.1155/2012/451059 · Cited by 9 · see citing works
HIV-1 pathogenesis and therapeutic intervention in the SCID-hu Thy/Liv mouse: a model for primary HIV-1 infection in the human thymus
Su, L. (1997) · Reviews in Medical Virology · doi:10.1002/(sici)1099-1654(199709)7:3 · Cited by 7 · see citing works
MHC class II/ESO tetramer-based generation of in vitro primed anti-tumor T-helper lines for adoptive cell therapy of cancer
Poli, C., Raffin, C., Dojcinovic, D., Luescher, I. F., Ayyoub, M., & Valmori, D. (2012) · Haematologica · doi:10.3324/haematol.2012.071712 · Cited by 7 · see citing works
Tracking Antigen-Specific CD8+ T Cells Using MHC Class I Multimers
Alanio, C., Bouvier, I., Jusforgues-Saklani, H., & Albert, M. L. (2012) · Methods in molecular biology · doi:10.1007/978-1-62703-218-6_23 · Cited by 5 · see citing works

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Authors: Borchers, S., Ogonek, J., Varanasi, P. R., Tischer, S., Bremm, M., Eiz-Vesper, B., Koehl, U., & Weissinger, E. M.
Affiliations: Medizinische Hochschule Hannover (DE)
Goethe University Frankfurt (DE)
Corresponding author: Borchers, Sylvia
ORCID: Borchers, Sylvia
Ogonek, Justyna
Varanasi, Pavankumar R.
Koehl, Ulrike
Weissinger, Eva M.
Venue: Diagnostic Microbiology and Infectious Disease
Publisher: Elsevier BV
Published: 2014-03
Volume: 78
Issue: 3
Pages: 201-212
ISSN: 0732-8893 (ISSN-L)
DOI: 10.1016/j.diagmicrobio.2013.11.007
OpenAlex: W2091352201
Cited by: 18
References: 92
Citations by year: 2025: 1 · 2023: 1 · 2021: 2 · 2018: 2 · 2017: 3 · 2016: 7 · 2015: 1 · 2014: 1
FWCI: 0.36
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Diagnostic Microbiology and Infectious Disease (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Epidemiology › Cytomegalovirus and herpesvirus research
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Keywords: cytomegalovirus, CMV-specific T cells, peptide-MHC complex, antiviral immunity, adoptive T cell therapy, immunocompromised patients, viral persistence, vaccination monitoring, epitope-specific T cells
MeSH terms: Cytomegalovirus, Humans, Major Histocompatibility Complex, Staining and Labeling, Epitopes, T-Lymphocyte, Adoptive Transfer, Protein Multimerization

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Multimer monitoring of CMV-specific T cells in research and in clinical applications

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