Correction of murine sickle cell disease by allogeneic haematopoietic cell transplantation with anti-3rd party veto cells.
Journal
Bone marrow transplantation
ISSN: 1476-5365
Titre abrégé: Bone Marrow Transplant
Pays: England
ID NLM: 8702459
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
received:
26
10
2020
accepted:
02
02
2021
revised:
19
01
2021
pubmed:
5
3
2021
medline:
14
10
2021
entrez:
4
3
2021
Statut:
ppublish
Résumé
Despite advances in gene therapy allogeneic hematopoietic stem cell transplants (HSCT) remains the most effective way to cure sickle cell disease (SCD). However, there are substantial challenges including lack of suitable donors, therapy-related toxicity (TRM) and risk of graft-versus-host disease (GvHD). Perhaps the most critical question is when to do a transplant for SCD. Safer transplant protocols for HLA-disparate HSCT is needed before transplants are widely accepted for SCD. Although risk of GvHD and TRM are less with T-cell-deplete HSCT and reduced-intensity conditioning (RIC), transplant rejection is a challenge. We have reported graft rejection of T cell-depleted non-myeloablative HSCT can be overcome in wild type fully mis-matched recipient mice, using donor-derived anti-3rd party central memory CD8-positive veto cells combined with short-term low-dose rapamycin. Here, we report safety and efficacy of this approach in a murine model for SCD. Durable donor-derived chimerism was achieved using this strategy with reversal of pathological parameters of SCD, including complete conversion to normal donor-derived red cells, and correction of splenomegaly and the levels of circulating reticulocytes, hematocrit, and hemoglobin.
Identifiants
pubmed: 33658643
doi: 10.1038/s41409-021-01237-6
pii: 10.1038/s41409-021-01237-6
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1818-1827Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature Limited part of Springer Nature.
Références
Herrick JB. Peculiar elongated and sickle-shaped red blood corpuscles in a case of severe anemia. 1910. Yale J Biol Med. 2001;74:179–84.
pubmed: 11501714
pmcid: 2588723
Weatherall DJ, Clegg JB. Inherited haemoglobin disorders: an increasing global health problem. Bull World Health Organ. 2001;79:704–12.
pubmed: 11545326
pmcid: 2566499
Glassberg J. Evidence-based management of sickle cell disease in the emergency department. Emerg Med Pract. 2011;13:1–20. quiz 20.
pubmed: 22164362
Centre for Disease Control and Prevention. Data and statistics of sickle cell disease (SCD). https://www.cdc.gov/ncbddd/sicklecell/data.html . Accessed 21 Oct 2019.
Esham KS, Rodday AM, Smith HP, Noubary F, Weidner RA, Buchsbaum RJ, et al. Assessment of health-related quality of life among adults hospitalized with sickle cell disease vaso-occlusive crisis. Blood Adv. 2020;4:19–27.
pubmed: 31891655
doi: 10.1182/bloodadvances.2019000128
El Hoss S, Cochet S, Marin M, Lapoumeroulie C, Dussiot M, Bouazza N, et al. Insights into determinants of spleen injury in sickle cell anemia. Blood Adv. 2019;3:2328–36.
pubmed: 31391165
pmcid: 6693014
doi: 10.1182/bloodadvances.2019000106
Badawy SM, Payne AB. Association between clinical outcomes and metformin use in adults with sickle cell disease and diabetes mellitus. Blood Adv. 2019;3:3297–306.
pubmed: 31698459
pmcid: 6855104
doi: 10.1182/bloodadvances.2019000838
Reeves SL, Jary HK, Gondhi JP, Kleyn M, Dombkowski KJ. Health outcomes and services in children with sickle cell trait, sickle cell anemia, and normal hemoglobin. Blood Adv. 2019;3:1574–80.
pubmed: 31101648
pmcid: 6538867
doi: 10.1182/bloodadvances.2018028043
Bolaños-Meade J, Fuchs EJ, Luznik L, Lanzkron SM, Gamper CJ, Jones RJ, et al. HLA-haploidentical bone marrow transplantation with posttransplant cyclophosphamide expands the donor pool for patients with sickle cell disease. Blood. 2012;120:4285–91.
pubmed: 22955919
pmcid: 3507140
doi: 10.1182/blood-2012-07-438408
Dallas MH, Triplett B, Shook DR, Hartford C, Srinivasan A, Laver J, et al. Long-term outcome and evaluation of organ function in pediatric patients undergoing haploidentical and matched related hematopoietic cell transplantation for sickle cell disease. Biol Blood Marrow Transpl. 2013;19:820–30.
doi: 10.1016/j.bbmt.2013.02.010
Fitzhugh CD, Hsieh MM, Taylor T, Coles W, Roskom K, Wilson D, et al. Cyclophosphamide improves engraftment in patients with SCD and severe organ damage who undergo haploidentical PBSCT. Blood Adv. 2017;1:652–61.
pubmed: 29296707
pmcid: 5727815
doi: 10.1182/bloodadvances.2016002972
Shenoy S, Eapen M, Panepinto JA, Logan BR, Wu J, Abraham A, et al. A trial of unrelated donor marrow transplantation for children with severe sickle cell disease. Blood. 2016;128:2561–7.
pubmed: 27625358
pmcid: 5123194
doi: 10.1182/blood-2016-05-715870
Luznik L, O’Donnell PV, Symons HJ, Chen AR, Leffell MS, Zahurak M, et al. HLA-haploidentical bone marrow transplantation for hematologic malignancies using nonmyeloablative conditioning and high-dose, posttransplantation cyclophosphamide. Biol Blood Marrow Transpl. 2008;14:641–50.
doi: 10.1016/j.bbmt.2008.03.005
La Nasa G, Giardini C, Argiolu F, Locatelli F, Arras M, De Stefano P, et al. Unrelated donor bone marrow transplantation for thalassemia: the effect of extended haplotypes. Blood. 2002;99:4350–6.
pubmed: 12036861
doi: 10.1182/blood.V99.12.4350
Li C, Wu X, Feng X, He Y, Liu H, Pei F, et al. A novel conditioning regimen improves outcomes in beta-thalassemia major patients using unrelated donor peripheral blood stem cell transplantation. Blood. 2012;120:3875–81.
pubmed: 22968457
doi: 10.1182/blood-2012-03-417998
Or-Geva N, Reisner Y. The evolution of T-cell depletion in haploidentical stem-cell transplantation. Br J Haematol. 2016;172:667–84.
pubmed: 26684279
doi: 10.1111/bjh.13868
Rachamim N, Gan J, Segall H, Krauthgamer R, Marcus H, Berrebi A, et al. Tolerance induction by “megadose” hematopoietic transplants: donor-type human CD34 stem cells induce potent specific reduction of host anti-donor cytotoxic T lymphocyte precursors in mixed lymphocyte culture. Transplantation. 1998;65:1386–93.
pubmed: 9625023
doi: 10.1097/00007890-199805270-00017
Miller RG. An immunological suppressor cell inactivating cytotoxic T-lymphocyte precursor cells recognizing it. Nature. 1980;287:544–6.
pubmed: 6448351
doi: 10.1038/287544a0
Reisner Y, Or-Geva N. Veto cells for safer nonmyeloablative haploidentical HSCT and CAR T cell therapy. Semin Hematol. 2019;56:173–82.
pubmed: 31202427
doi: 10.1053/j.seminhematol.2019.03.003
Ophir E, Eidelstein Y, Afik R, Bachar-Lustig E, Reisner Y. Induction of tolerance to bone marrow allografts by donor-derived host nonreactive ex vivo-induced central memory CD8 T cells. Blood. 2010;115:2095–104.
pubmed: 20042725
pmcid: 2837324
doi: 10.1182/blood-2009-10-248716
Ophir E, Or-Geva N, Gurevich I, Tal O, Eidelstein Y, Shezen E, et al. Murine anti-third-party central-memory CD8(+) T cells promote hematopoietic chimerism under mild conditioning: lymph-node sequestration and deletion of anti-donor T cells. Blood. 2013;121:1220–8.
pubmed: 23223359
pmcid: 4467899
doi: 10.1182/blood-2012-07-441493
Kean LS, Durham MM, Adams AB, Hsu LL, Perry JR, Dillehay D, et al. A cure for murine sickle cell disease through stable mixed chimerism and tolerance induction after nonmyeloablative conditioning and major histocompatibility complex–mismatched bone marrow transplantation. Blood. 2002;99:1840–9.
pubmed: 11861303
doi: 10.1182/blood.V99.5.1840
Pestina TI, Hargrove PW, Zhao H, Mead PE, Smeltzer MP, Weiss MJ, et al. Amelioration of murine sickle cell disease by nonablative conditioning and gamma-globin gene-corrected bone marrow cells. Mol Ther Methods Clin Dev. 2015;2:15045.
pubmed: 26665131
pmcid: 4667717
doi: 10.1038/mtm.2015.45
Hulbert ML, Shenoy S. Hematopoietic stem cell transplantation for sickle cell disease: progress and challenges. Pediatr Blood Cancer. 2018;65:e27263.
pubmed: 29797658
doi: 10.1002/pbc.27263
Javazon EH, Radhi M, Gangadharan B, Perry J, Archer DR. Hematopoietic stem cell function in a murine model of sickle cell disease. Anemia. 2012;2012:387385.
pubmed: 22701784
pmcid: 3372279
doi: 10.1155/2012/387385
Shenoy S. Hematopoietic stem cell transplantation for sickle cell disease: current practice and emerging trends. Hematol Am Soc Hematol Educ Program. 2011;2011:273–9.
doi: 10.1182/asheducation-2011.1.273
Robinson TM, Fuchs EJ. Allogeneic stem cell transplantation for sickle cell disease. Curr Opin Hematol. 2016;23:524–9.
pubmed: 27496639
pmcid: 5130409
doi: 10.1097/MOH.0000000000000282
Brodsky RA, Luznik L, Bolaños-Meade J, Leffell MS, Jones RJ, Fuchs EJ. Reduced intensity HLA-haploidentical BMT with post transplantation cyclophosphamide in nonmalignant hematologic diseases. Bone Marrow Transpl. 2008;42:523–7.
doi: 10.1038/bmt.2008.203
Park SH, Lee CM, Dever DP, Davis TH, Camarena J, Srifa W, et al. Highly efficient editing of the beta-globin gene in patient-derived hematopoietic stem and progenitor cells to treat sickle cell disease. Nucleic Acids Res. 2019;47:7955–72.
pubmed: 31147717
pmcid: 6735704
doi: 10.1093/nar/gkz475
Romero Z, Lomova A, Said S, Miggelbrink A, Kuo CY, Campo-Fernandez B, et al. Editing the sickle cell disease mutation in human hematopoietic stem cells: comparison of endonucleases and homologous donor templates. Mol Ther. 2019;27:1389–406.
pubmed: 31178391
pmcid: 6697408
doi: 10.1016/j.ymthe.2019.05.014
Kawai T, Andrews D, Colvin RB, Sachs DH, Cosimi AB. Thromboembolic complications after treatment with monoclonal antibody against CD40 ligand. Nat Med. 2000;6:114.
pubmed: 10655072
doi: 10.1038/72162
Boumpas DT, Furie R, Manzi S, Illei GG, Wallace DJ, Balow JE, et al. A short course of BG9588 (anti-CD40 ligand antibody) improves serologic activity and decreases hematuria in patients with proliferative lupus glomerulonephritis. Arthritis Rheum. 2003;48:719–27.
pubmed: 12632425
doi: 10.1002/art.10856
Vincenti F. What’s in the pipeline? New immunosuppressive drugs in transplantation. Am J Transpl. 2002;2:898–903.
doi: 10.1034/j.1600-6143.2002.21005.x
Shock A, Burkly L, Wakefield I, Peters C, Garber E, Ferrant J, et al. CDP7657, an anti-CD40L antibody lacking an Fc domain, inhibits CD40L-dependent immune responses without thrombotic complications: an in vivo study. Arthritis Res Ther. 2015;17:234.
pubmed: 26335795
pmcid: 4558773
doi: 10.1186/s13075-015-0757-4
Reich-Zeliger S, Zhao Y, Krauthgamer R, Bachar-Lustig E, Reisner Y. Anti-third party CD8+ CTLs as potent veto cells: coexpression of CD8 and FasL is a prerequisite. Immunity. 2000;13:507–15.
pubmed: 11070169
doi: 10.1016/S1074-7613(00)00050-9
Delgoffe GM, Kole TP, Zheng Y, Zarek PE, Matthews KL, Xiao B, et al. The mTOR kinase differentially regulates effector and regulatory T cell lineage commitment. Immunity. 2009;30:832–44.
pubmed: 19538929
pmcid: 2768135
doi: 10.1016/j.immuni.2009.04.014
Battaglia M, Stabilini A, Roncarolo MG. Rapamycin selectively expands CD4+CD25+FoxP3+ regulatory T cells. Blood. 2005;105:4743–8.
pubmed: 15746082
doi: 10.1182/blood-2004-10-3932
Qu Y, Zhang B, Zhao L, Liu G, Ma H, Rao E, et al. The effect of immunosuppressive drug rapamycin on regulatory CD4+CD25+Foxp3+T cells in mice. Transpl Immunol. 2007;17:153–61.
pubmed: 17331841
doi: 10.1016/j.trim.2007.01.002
Hale DA, Gottschalk R, Fukuzaki T, Wood ML, Maki T, Monaco AP. Extended skin allo- and xenograft survival in mice treated with rapamycin, antilymphocyte serum, and donor-specific bone marrow transfusion. Transpl Proc. 1996;28:3269.
Hale DA, Gottschalk R, Fukuzaki T, Wood ML, Maki T, Monaco AP. Superiority of sirolimus (rapamycin) over cyclosporine in augmenting allograft and xenograft survival in mice treated with antilymphocyte serum and donor-specific bone marrow. Transplantation. 1997;63:359–64.
pubmed: 9039923
doi: 10.1097/00007890-199702150-00005
Hale DA, Gottschalk R, Umemura A, Maki T, Monaco AP. Establishment of stable multilineage hematopoietic chimerism and donor-specific tolerance without irradiation. Transplantation. 2000;69:1242–51.
pubmed: 10798737
doi: 10.1097/00007890-200004150-00008
Pilat N, Klaus C, Gattringer M, Jaeckel E, Wrba F, Golshayan D, et al. Therapeutic efficacy of polyclonal tregs does not require rapamycin in a low-dose irradiation bone marrow transplantation model. Transplantation. 2011;92:280–8.
pubmed: 21697774
doi: 10.1097/TP.0b013e3182241133