Cytomegalovirus-Associated Inhibition of Hematopoiesis Is Preventable by Cytoimmunotherapy With Antiviral CD8 T Cells

Angélique Renzaho1, Jürgen Podlech1, Birgit Kühnapfel1, Franziska Blaum1, Matthias J. Reddehase1, Niels A. W. Lemmermann1
1Institute for Virology and Research Center for Immunotherapy (FZI), University Medical Center of the Johannes Gutenberg-University of Mainz, Mainz, Germany

Tóm tắt

Từ khóa


Tài liệu tham khảo

Alterio de Goss, 1998, Control of cytomegalovirus in bone marrow transplantation chimeras lacking the prevailing antigen-presenting molecule in recipient tissues rests primarily on recipient-derived CD8 T cells, J. Virol., 72, 7733, 10.1128/JVI.72.10.7733-7744.1998

Apperley, 1989, The effect of cytomegalovirus on hemopoiesis: in vitro evidence for selective infection of marrow stromal cells, Exp. Hematol., 17, 38

Böhm, 2008, Epitope-specific in vivo protection against cytomegalovirus disease by CD8 T cells in the murine model of preemptive immunotherapy, Med. Microbiol. Immunol., 197, 135, 10.1007/s00430-008-0092-3

Busch, 1991, Rescue of myeloid lineage-committed preprogenitor cells from cytomegalovirus-infected bone marrow stroma, J. Virol., 65, 981, 10.1128/JVI.65.2.981-984.1991

Chabannon, 1992, Stem cell-stromal cell interactions, Curr. Top. Microbiol. Immunol., 177, 123, 10.1007/978-3-642-76912-2_10

Chemaly, 2019, Definitions of resistant and refractory cytomegalovirus infection and disease in transplant recipients for use in clinical trials, Clin Infec Dis., 68, 1420, 10.1093/cid/ciy696

Dobonici, 1998, Evidence against a key role for transforming growth factor-beta1 in cytomegalovirus-induced bone marrow aplasia, J. Gen. Virol., 79, 867, 10.1099/0022-1317-79-4-867

Ebert, 2012, Parameters determining the efficacy of adoptive CD8 T-cell therapy of cytomegalovirus infection, Med. Microbiol. Immunol., 201, 527, 10.1007/s00430-012-0258-x

Feuchtinger, 2010, Adoptive transfer of pp65-specific T cells for the treatment of chemorefractory cytomegalovirus disease or reactivation after haploidentical and matched unrelated stem cell transplantation, Blood., 116, 4360, 10.1182/blood-2010-01-262089

Fink, 2014, Noncanonical expression of a murine cytomegalovirus early protein CD8 T-cell epitope as an immediate early epitope based on transcription from an upstream gene, Viruses., 6, 808, 10.3390/v6020808

Gubbay, 1990, A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes, Nature., 346, 245, 10.1038/346245a0

Hancock, 2020, Human cytomegalovirus miRNAs regulate TGF-β to mediate myelosuppression while maintaining viral latency in CD34+ hematopoietic progenitor cells, Cell Host Microb., 27, 104, 10.1016/j.chom.2019.11.013

Holtappels, 2008, CD8 T-cell-based immunotherapy of cytomegalovirus infection: “proof of concept” provided by the murine model, Med. Microbiol. Immunol., 197, 125, 10.1007/s00430-008-0093-2

Holtappels, 1998, Control of murine cytomegalovirus in the lungs: relative but not absolute immunodominance of the immediate-early 1 nonapeptide during the antiviral cytolytic T-lymphocyte response in pulmonary infiltrates, J. Virol., 72, 7201, 10.1128/JVI.72.9.7201-7212.1998

Holtappels, 2002, Two antigenic peptides from genes m123 and m164 of murine cytomegalovirus quantitatively dominate CD8 T-cell memory in the H-2d haplotype, J. Virol., 76, 151, 10.1128/jvi.76.1.151-164.2002

Koopman, 1990, Expression of a candidate sex-determining gene during mouse testis differentiation, Nature., 348, 450, 10.1038/348450a0

Kurz, 1997, Latency versus persistence or intermittent recurrences: evidence for a latent state of murine cytomegalovirus in the lungs, J. Virol., 71, 2980, 10.1128/JVI.71.4.2980-2987.1997

Lee, 2020, Role of growth factors in hematopoietic stem cell niche, Cell Biol. Toxicol., 10.1007/s10565-019-09510-7

Lemmermann, 2012, Murine cytomegalovirus immune evasion proteins operative in the MHC class I pathway of antigen processing and presentation: state of knowledge, revisions, and questions, Med. Microbiol. Immunol., 201, 497, 10.1007/s00430-012-0257-y

Lemmermann, 2015, Non-redundant and redundant roles of cytomegalovirus gH/gL complexes in host organ entry and intra-tissue spread, PLoS Pathog., 11, e1004640, 10.1371/journal.ppat.1004640

Lemmermann, 2010, CD8 T cell immunotherapy of cytomegalovirus disease in the murine model,, Methods in Microbiology, Vol. 37, Immunology of Infection, 369

Ljungman, 2017, Definitions of cytomegalovirus infection and disease in transplant patients for use in clinical trials, Clin. Infect. Dis., 64, 87, 10.1093/cid/ciw668

Ljungman, 2019, Guidelines for the management of cytomegalovirus infection in patients with haematological malignancies and after stem cell transplantation from the 2017 European Conference on Infections in Leukaemia (ECIL 7), Lancet Infect. Dis., 19, e260, 10.1016/S1473-3099(19)30107-0

Maffini, 2016, Treatment of CMV infection after allogeneic hematopoietic stem cell transplantation, Expert Rev. Hematol., 9, 585, 10.1080/17474086.2016.1174571

Mayer, 1997, Bone marrow failure by cytomegalovirus is associated with an in vivo deficiency in the expression of essential stromal hemopoietin genes, J. Virol., 71, 4589, 10.1128/JVI.71.6.4589-4598.1997

Moss, 2005, Cellular immunotherapy for viral infection after HSC transplantation, Nat. Rev. Immunol., 5, 9, 10.1038/nri1526

Mutter, 1988, Failure in generating hemopoietic stem cells is the primary cause of death from cytomegalovirus disease in the immunocompromised host, J. Exp. Med., 167, 1645, 10.1084/jem.167.5.1645

Nauerth, 2013, TCR-ligand koff rate correlates with the protective capacity of antigen-specific CD8+ T cells for adoptive transfer, Sci. Transl. Med., 5, 192r, 10.1126/scitranslmed.3005958

Neuenhahn, 2017, Transfer of minimally manipulated CMV-specific T cells from stem cell or third-party donors to treat CMV infection after allo-HSCT, Leukemia., 31, 2161, 10.1038/leu.2017.16

Pei, 2017, Cytomegalovirus-specific T-cell transfer for refractory cytomegalovirus infection after haploidentical stem cell transplantation: the quantitative and qualitative immune recovery for cytomegalovirus, J. Infect. Dis., 216, 945, 10.1093/infdis/jix357

Pinto, 2006, Coordinated function of murine cytomegalovirus genes completely inhibits CTL lysis, J. Immunol., 177, 3225, 10.4049/jimmunol.177.5.3225

Podlech, 2002, Animal models: Murine cytomegalovirus,, Methods in Microbiology, Immunology of Infection, 493, 10.1016/S0580-9517(02)32103-2

Podlech, 2000, Murine model of interstitial cytomegalovirus pneumonia in syngeneic bone marrow transplantation: persistence of protective pulmonary CD8-T-cell infiltrates after clearance of acute infection, J. Virol., 74, 7496, 10.1128/JVI.74.16.7496-7507.2000

Podlech, 1998, Reconstitution of CD8 T cells is essential for the prevention of multiple-organ cytomegalovirus histopathology after bone marrow transplantation, J. Gen. Virol., 79, 2099, 10.1099/0022-1317-79-9-2099

Randolph-Habecker, 2002, Cytomegalovirus mediated myelosuppression, J. Clin. Virol., 25, 51, 10.1016/S1386-6532(02)00092-6

Reddehase, 2016, Mutual interference between cytomegalovirus and reconstitution of protective immunity after hematopoietic cell transplantation, Front. Immunol., 7, 294, 10.3389/fimmu.2016.00294

Reddehase, 1992, Hematopoietic stem cell deficiency resulting from cytomegalovirus infection of bone marrow stroma, Ann. Hematol., 64, A125, 10.1007/BF01715364

Reddehase, 2018, Mouse model of cytomegalovirus disease and immunotherapy in the immunocompromised host: predictions for medical translation that survived the Test of Time, Viruses., 10, 693, 10.3390/v10120693

Reddehase, 2019, Cellular reservoirs of latent cytomegaloviruses, Med. Microbiol. Immunol., 208, 391, 10.1007/s00430-019-00592-y

Reddehase, , In vivo application of recombinant interleukin 2 in the immunotherapy of established cytomegalovirus infection, J. Exp. Med., 165, 650, 10.1084/jem.165.3.650

Reddehase, , CD8-positive T lymphocytes specific for murine cytomegalovirus immediate-early antigens mediate protective immunity, J. Virol., 61, 3102, 10.1128/JVI.61.10.3102-3108.1987

Reddehase, 1985, Interstitial murine cytomegalovirus pneumonia after irradiation: characterization of cells that limit viral replication during established infection of the lungs, J. Virol., 55, 264, 10.1128/JVI.55.2.264-273.1985

Renzaho, 2019, Transcripts expressed in cytomegalovirus latency coding for an antigenic IE/E phase peptide that drives memory inflation, Med. Microbiol. Immunol., 208, 439, 10.1007/s00430-019-00615-8

Riddell, 1992, Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones, Science., 257, 238, 10.1126/science.1352912

Roemhild, 2016, Virus-specific T-cell therapy in solid organ transplantation, Transpl. Int., 29, 515, 10.1111/tri.12659

Sacher, 2008, The major virus-producing cell type during murine cytomegalovirus infection, the hepatocyte, is not the source of virus dissemination in the host, Cell Host Microbe., 3, 263, 10.1016/j.chom.2008.02.014

Seckert, 2008, Hematopoietic stem cell transplantation with latently infected donors does not transmit virus to immunocompromised recipients in the murine model of cytomegalovirus infection, Med. Microbiol. Immunol., 197, 251, 10.1007/s00430-008-0094-1

Seckert, 2009, Liver sinusoidal endothelial cells are a site of murine cytomegalovirus latency and reactivation, J. Virol., 83, 8869, 10.1128/JVI.00870-09

Seo, 2013, Clinical cytomegalovirus research: hematopoietic cell transplantation,, Cytomegaloviruses: From Molecular Pathogenesis to Intervention. Vol. 2, 337

Simmons, 1990, Mechanisms of cytomegalovirus-mediated myelosuppression: perturbation of stromal cell function versus direct infection of myeloid cells, Proc. Natl. Acad. Sci. U.S.A, 87, 1386, 10.1073/pnas.87.4.1386

Simon, 2005, Role for tumor necrosis factor alpha in murine cytomegalovirus transcriptional reactivation in latently infected lungs, J. Virol., 79, 326, 10.1128/JVI.79.1.326-340.2005

Steffens, , Preemptive CD8 T-cell immunotherapy of acute cytomegalovirus infection prevents lethal disease, limits the burden of latent viral genomes, and reduces the risk of virus recurrence, J. Virol., 72, 1797, 10.1128/JVI.72.3.1797-1804.1998

Steffens, , Cytomegalovirus inhibits the engraftment of donor bone marrow cells by downregulation of hemopoietin gene expression in recipient stroma, J. Virol., 72, 5006, 10.1128/JVI.72.6.5006-5015.1998

Stern, 2019, Human cytomegalovirus latency and reactivation in allogeneic hematopoietic stem cell transplant recipients, Front. Microbiol., 10, 1186, 10.3389/fmicb.2019.01186

Torok-Storb, 1997, Association of specific cytomegalovirus genotypes with death from myelosuppression after marrow transplantation, Blood., 90, 2097, 10.1182/blood.V90.5.2097

Walter, 1995, Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor, N. Engl. J. Med., 333, 1038, 10.1056/NEJM199510193331603

Yu, 2016, Hematopoietic stem cell and its bone marrow niche, Curr. Top. Dev. Biol., 118, 21, 10.1016/bs.ctdb.2016.01.009

Zhang, 2019, A clinically relevant murine model unmasks a two-hit mechanism for reactivation and dissemination of cytomegalovirus after kidney transplant, Am. J. Transplant., 19, 2421, 10.1111/ajt.15376