Assessment of non-myelotoxic agents as a preparatory regimen for hematopoietic stem cell gene therapy.
Animals
Cyclams
/ pharmacology
Benzylamines
Hematopoietic Stem Cell Transplantation
/ methods
Granulocyte Colony-Stimulating Factor
/ pharmacology
Genetic Therapy
/ methods
Female
Mice
Male
Busulfan
DNA-Binding Proteins
/ genetics
Heterocyclic Compounds
/ administration & dosage
Hematopoietic Stem Cells
Transplantation Conditioning
/ methods
Humans
Mice, Inbred C57BL
AMD3100
Conditioning
G-CSF
Gene therapy
Hematopoietic stem cell transplantation
RAG2
VLA-4I
Journal
Human cell
ISSN: 1749-0774
Titre abrégé: Hum Cell
Pays: Japan
ID NLM: 8912329
Informations de publication
Date de publication:
26 Oct 2024
26 Oct 2024
Historique:
received:
05
02
2024
accepted:
07
10
2024
medline:
26
10
2024
pubmed:
26
10
2024
entrez:
26
10
2024
Statut:
epublish
Résumé
RAG2 deficiency is characterized by a lack of B and T lymphocytes, causing severe lethal infections. Currently, RAG2 deficiency is treated with a Hematopoietic Stem Cell transplantation (HSCT). Most conditioning regimens used before HSCT consist of alkylating myelotoxic agents with or without irradiation and affect growth and development of pediatric patients. Here, we developed a non-myelotoxic regimen using G-CSF, VLA-4I or AMD3100. These agents are known HSC mobilizers or affect bone marrow (BM) permeability and may support the homing of HSCs to the BM, without inducing major side effects. Female Rag2
Identifiants
pubmed: 39460845
doi: 10.1007/s13577-024-01130-6
pii: 10.1007/s13577-024-01130-6
doi:
Substances chimiques
Cyclams
0
plerixafor
S915P5499N
Benzylamines
0
Granulocyte Colony-Stimulating Factor
143011-72-7
Busulfan
G1LN9045DK
DNA-Binding Proteins
0
Heterocyclic Compounds
0
Rag2 protein, mouse
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
9Subventions
Organisme : Scientific and Technological Research Council of Turkey (TÜBİTAK)
ID : 1002-220S338
Organisme : Scientific and Technological Research Council of Turkey (TÜBİTAK)
ID : 2221-2017/2
Organisme : Hacettepe Üniversitesi
ID : TUK-2019-17760
Organisme : Hacettepe Üniversitesi
ID : TAY2022-20436
Organisme : European Union Framework Program 7
ID : HEALTH-2010-261387
Informations de copyright
© 2024. The Author(s) under exclusive licence to Japan Human Cell Society.
Références
van der Burg M, Gennery AR. Educational paper. Eur J Pediatr. 2011;170(5):561. https://doi.org/10.1007/s00431-011-1452-3 .
doi: 10.1007/s00431-011-1452-3
pubmed: 21479529
pmcid: 3078321
Gelfand EW. SCID continues to point the way. N Engl J Med. 1990;322(24):1741–3. https://doi.org/10.1056/nejm199006143222410 .
doi: 10.1056/nejm199006143222410
pubmed: 2288565
Worth AJ, Booth C, Veys P. Stem cell transplantation for primary immune deficiency. Curr Opin Hematol. 2013;20(6):501–8. https://doi.org/10.1097/MOH.0b013e328365a13b .
doi: 10.1097/MOH.0b013e328365a13b
pubmed: 24104410
Niehues T, Perez-Becker R, Schuetz C. More than just SCID–the phenotypic range of combined immunodeficiencies associated with mutations in the recombinase activating genes (RAG) 1 and 2. Clin Immunol. 2010;135(2):183–92. https://doi.org/10.1016/j.clim.2010.01.013 .
doi: 10.1016/j.clim.2010.01.013
pubmed: 20172764
Ru H, Chambers MG, Fu TM, Tong AB, Liao M, Wu H. Molecular mechanism of V(D)J recombination from synaptic RAG1-RAG2 complex structures. Cell. 2015;163(5):1138–52. https://doi.org/10.1016/j.cell.2015.10.055 .
doi: 10.1016/j.cell.2015.10.055
pubmed: 26548953
pmcid: 4690471
Villa A, Notarangelo LD. RAG gene defects at the verge of immunodeficiency and immune dysregulation. Immunol Rev. 2019;287(1):73–90. https://doi.org/10.1111/imr.12713 .
doi: 10.1111/imr.12713
pubmed: 30565244
pmcid: 6309314
Felfly H, Haddad GG. Hematopoietic stem cells: potential new applications for translational medicine. J Stem Cells. 2014;9(3):163–97.
pubmed: 25157450
Yates F, Malassis-Séris M, Stockholm D, Bouneaud C, Larousserie F, Noguiez-Hellin P, et al. Gene therapy of RAG-2-/- mice: sustained correction of the immunodeficiency. Blood. 2002;100(12):3942–9. https://doi.org/10.1182/blood-2002-03-0782 .
doi: 10.1182/blood-2002-03-0782
pubmed: 12393742
Bushman FD. Retroviral integration and human gene therapy. J Clin Invest. 2007;117(8):2083–6. https://doi.org/10.1172/jci32949 .
doi: 10.1172/jci32949
pubmed: 17671645
pmcid: 1934602
Cavazzana M, Six E, Lagresle-Peyrou C, André-Schmutz I, Hacein-Bey-Abina S. Gene therapy for X-linked severe combined immunodeficiency: where do we stand? Hum Gene Ther. 2016;27(2):108–16. https://doi.org/10.1089/hum.2015.137 .
doi: 10.1089/hum.2015.137
pubmed: 26790362
pmcid: 4779287
Kohn LA, Kohn DB. Gene therapies for primary immune deficiencies. Front Immunol. 2021;12: 648951. https://doi.org/10.3389/fimmu.2021.648951 .
doi: 10.3389/fimmu.2021.648951
pubmed: 33717203
pmcid: 7946985
van Til NP, de Boer H, Mashamba N, Wabik A, Huston M, Visser TP, et al. Correction of murine Rag2 severe combined immunodeficiency by lentiviral gene therapy using a codon-optimized RAG2 therapeutic transgene. Mol Ther. 2012;20(10):1968–80. https://doi.org/10.1038/mt.2012.110 .
doi: 10.1038/mt.2012.110
pubmed: 22692499
pmcid: 3464632
Capo V, Castiello MC, Fontana E, Penna S, Bosticardo M, Draghici E, et al. Efficacy of lentivirus-mediated gene therapy in an Omenn syndrome recombination-activating gene 2 mouse model is not hindered by inflammation and immune dysregulation. J Allergy Clin Immunol. 2018;142(3):928-41e8. https://doi.org/10.1016/j.jaci.2017.11.015 .
doi: 10.1016/j.jaci.2017.11.015
pubmed: 29241731
Gyurkocza B, Sandmaier BM. Conditioning regimens for hematopoietic cell transplantation: one size does not fit all. Blood. 2014;124(3):344–53. https://doi.org/10.1182/blood-2014-02-514778 .
doi: 10.1182/blood-2014-02-514778
pubmed: 24914142
pmcid: 4102707
Lum SH, Hoenig M, Gennery AR, Slatter MA. Conditioning regimens for hematopoietic cell transplantation in primary immunodeficiency. Curr Allergy Asthma Rep. 2019;19(11):52. https://doi.org/10.1007/s11882-019-0883-1 .
doi: 10.1007/s11882-019-0883-1
pubmed: 31741098
pmcid: 6861349
Steward CG, Jarisch A. Haemopoietic stem cell transplantation for genetic disorders. Arch Dis Child. 2005;90(12):1259. https://doi.org/10.1136/adc.2005.074278 .
doi: 10.1136/adc.2005.074278
pubmed: 16301554
pmcid: 1720237
McNerney ME, Godley LA, Le Beau MM. Therapy-related myeloid neoplasms: when genetics and environment collide. Nat Rev Cancer. 2017;17(9):513–27. https://doi.org/10.1038/nrc.2017.60 .
doi: 10.1038/nrc.2017.60
pubmed: 28835720
pmcid: 5946699
Morton LM, Dores GM, Schonfeld SJ, Linet MS, Sigel BS, Lam CJK, et al. Association of Chemotherapy for solid tumors with development of therapy-related myelodysplastic syndrome or acute myeloid leukemia in the modern era. JAMA Oncol. 2019;5(3):318–25. https://doi.org/10.1001/jamaoncol.2018.5625 .
doi: 10.1001/jamaoncol.2018.5625
pubmed: 30570657
Overbeek A, van den Berg MH, van Leeuwen FE, Kaspers GJL, Kremer LCM, Lambalk CB, et al. Chemotherapy-related late adverse effects on ovarian function in female survivors of childhood cancer and cancer in the reproductive age. Cochrane Database Syst Rev. 2019;2019(4):CD009127. https://doi.org/10.1002/14651858.CD009127.pub2 .
doi: 10.1002/14651858.CD009127.pub2
pmcid: 6564077
Bacigalupo A, Ballen K, Rizzo D, Giralt S, Lazarus H, Ho V, et al. Defining the intensity of conditioning regimens: working definitions. Biol Blood Marrow Transplant. 2009;15(12):1628–33. https://doi.org/10.1016/j.bbmt.2009.07.004 .
doi: 10.1016/j.bbmt.2009.07.004
pubmed: 19896087
pmcid: 2861656
Heimall J, Logan BR, Cowan MJ, Notarangelo LD, Griffith LM, Puck JM, et al. Immune reconstitution and survival of 100 SCID patients post-hematopoietic cell transplant: a PIDTC natural history study. Blood. 2017;130(25):2718–27. https://doi.org/10.1182/blood-2017-05-781849 .
doi: 10.1182/blood-2017-05-781849
pubmed: 29021228
pmcid: 5746165
Cancrini C, Ferrua F, Scarselli A, Brigida I, Romiti ML, Barera G, et al. Role of reduced intensity conditioning in T-cell and B-cell immune reconstitution after HLA-identical bone marrow transplantation in ADA-SCID. Haematologica. 2010;95(10):1778–82. https://doi.org/10.3324/haematol.2010.025098 .
doi: 10.3324/haematol.2010.025098
pubmed: 20460637
pmcid: 2948105
Iguchi A, Kawamura N, Kobayashi R, Takezaki SI, Ohkura Y, Inamoto J, et al. Successful reduced-intensity SCT from unrelated cord blood in three patients with X-linked SCID. Bone Marrow Transplant. 2011;46(12):1526–31. https://doi.org/10.1038/bmt.2010.338 .
doi: 10.1038/bmt.2010.338
pubmed: 21258424
pmcid: 3234418
Haddad E, Logan BR, Griffith LM, Buckley RH, Parrott RE, Prockop SE, et al. SCID genotype and 6-month posttransplant CD4 count predict survival and immune recovery. Blood. 2018;132(17):1737–49. https://doi.org/10.1182/blood-2018-03-840702 .
doi: 10.1182/blood-2018-03-840702
pubmed: 30154114
pmcid: 6202916
Neven B, Leroy S, Decaluwe H, Le Deist F, Picard C, Moshous D, et al. Long-term outcome after hematopoietic stem cell transplantation of a single-center cohort of 90 patients with severe combined immunodeficiency. Blood. 2009;113(17):4114–24. https://doi.org/10.1182/blood-2008-09-177923 .
doi: 10.1182/blood-2008-09-177923
pubmed: 19168787
Huston MW, Riegman AR, Yadak R, van Helsdingen Y, de Boer H, van Til NP, et al. Pretransplant mobilization with granulocyte colony-stimulating factor improves B-cell reconstitution by lentiviral vector gene therapy in SCID-X1 mice. Hum Gene Ther. 2014;25(10):905–14. https://doi.org/10.1089/hum.2014.101 .
doi: 10.1089/hum.2014.101
pubmed: 25222508
pmcid: 4180299
To LB, Haylock DN, Simmons PJ, Juttner CA. The biology and clinical uses of blood stem cells. Blood. 1997;89(7):2233–58. https://doi.org/10.1182/blood.V89.7.2233 .
doi: 10.1182/blood.V89.7.2233
pubmed: 9116266
Winkler IG, Pettit AR, Raggatt LJ, Jacobsen RN, Forristal CE, Barbier V, et al. Hematopoietic stem cell mobilizing agents G-CSF, cyclophosphamide or AMD3100 have distinct mechanisms of action on bone marrow HSC niches and bone formation. Leukemia. 2012;26(7):1594–601. https://doi.org/10.1038/leu.2012.17 .
doi: 10.1038/leu.2012.17
pubmed: 22266913
Broxmeyer HE, Orschell CM, Clapp DW, Hangoc G, Cooper S, Plett PA, et al. Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med. 2005;201(8):1307–18. https://doi.org/10.1084/jem.20041385 .
doi: 10.1084/jem.20041385
pubmed: 15837815
pmcid: 2213145
DiPersio JF, Uy GL, Yasothan U, Kirkpatrick P. Plerixafor. Nat Rev Drug Discov. 2009;8(2):105–7. https://doi.org/10.1038/nrd2819 .
doi: 10.1038/nrd2819
pubmed: 19180104
Jacobsen K, Kravitz J, Kincade PW, Osmond DG. Adhesion receptors on bone marrow stromal cells: in vivo expression of vascular cell adhesion molecule-1 by reticular cells and sinusoidal endothelium in normal and gamma-irradiated mice. Blood. 1996;87(1):73–82.
doi: 10.1182/blood.V87.1.73.73
pubmed: 8547679
Papayannopoulou T, Craddock C, Nakamoto B, Priestley GV, Wolf NS. The VLA4/VCAM-1 adhesion pathway defines contrasting mechanisms of lodgement of transplanted murine hemopoietic progenitors between bone marrow and spleen. Proc Natl Acad Sci USA. 1995;92(21):9647–51. https://doi.org/10.1073/pnas.92.21.9647 .
doi: 10.1073/pnas.92.21.9647
pubmed: 7568190
pmcid: 40859
Ramirez P, Rettig MP, Uy GL, Deych E, Holt MS, Ritchey JK, et al. BIO5192, a small molecule inhibitor of VLA-4, mobilizes hematopoietic stem and progenitor cells. Blood. 2009;114(7):1340–3. https://doi.org/10.1182/blood-2008-10-184721 .
doi: 10.1182/blood-2008-10-184721
pubmed: 19571319
pmcid: 2727418
van Til NP, Wagemaker G. Lentiviral gene transduction of mouse and human hematopoietic stem cells. Methods Mol Biol. 2014;1185:311–9. https://doi.org/10.1007/978-1-4939-1133-2_21 .
doi: 10.1007/978-1-4939-1133-2_21
pubmed: 25062638
Zhang F, Frost AR, Blundell MP, Bales O, Antoniou MN, Thrasher AJ. A ubiquitous chromatin opening element (UCOE) confers resistance to DNA methylation-mediated silencing of lentiviral vectors. Mol Ther. 2010;18(9):1640–9. https://doi.org/10.1038/mt.2010.132 .
doi: 10.1038/mt.2010.132
pubmed: 20588258
pmcid: 2956914
Zhang F, Thornhill SI, Howe SJ, Ulaganathan M, Schambach A, Sinclair J, et al. Lentiviral vectors containing an enhancer-less ubiquitously acting chromatin opening element (UCOE) provide highly reproducible and stable transgene expression in hematopoietic cells. Blood. 2007;110(5):1448–57. https://doi.org/10.1182/blood-2006-12-060814 .
doi: 10.1182/blood-2006-12-060814
pubmed: 17456723
pmcid: 2629730
Chevaleyre J, Duchez P, Rodriguez L, Vlaski M, Villacreces A, Conrad-Lapostolle V, et al. Busulfan administration flexibility increases the applicability of scid repopulating cell assay in NSG mouse model. PLoS ONE. 2013;8(9): e74361. https://doi.org/10.1371/journal.pone.0074361 .
doi: 10.1371/journal.pone.0074361
pubmed: 24069300
pmcid: 3775811
Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc. 1958;53(282):457–81.
doi: 10.1080/01621459.1958.10501452
Mantel N. Evaluation of survival data and two new rank order statistics arising in its consideration. Cancer Chemother Rep. 1966;50(3):163–70.
pubmed: 5910392
Pai SY, Logan BR, Griffith LM, Buckley RH, Parrott RE, Dvorak CC, et al. Transplantation outcomes for severe combined immunodeficiency, 2000–2009. N Engl J Med. 2014;371(5):434–46. https://doi.org/10.1056/NEJMoa1401177 .
doi: 10.1056/NEJMoa1401177
pubmed: 25075835
pmcid: 4183064
Omer-Javed A, Pedrazzani G, Albano L, Ghaus S, Latroche C, Manzi M, et al. Mobilization-based chemotherapy-free engraftment of gene-edited human hematopoietic stem cells. Cell. 2022;185(13):2248-64e21. https://doi.org/10.1016/j.cell.2022.04.039 .
doi: 10.1016/j.cell.2022.04.039
pubmed: 35617958
pmcid: 9240327
Czechowicz A, Palchaudhuri R, Scheck A, Hu Y, Hoggatt J, Saez B, et al. Selective hematopoietic stem cell ablation using CD117-antibody-drug-conjugates enables safe and effective transplantation with immunity preservation. Nat Commun. 2019;10(1):617. https://doi.org/10.1038/s41467-018-08201-x .
doi: 10.1038/s41467-018-08201-x
pubmed: 30728354
pmcid: 6365495
Mehta HM, Malandra M, Corey SJ. G-CSF and GM-CSF in neutropenia. J Immunol. 2015;195(4):1341–9. https://doi.org/10.4049/jimmunol.1500861 .
doi: 10.4049/jimmunol.1500861
pubmed: 26254266
Larochelle A, Krouse A, Metzger M, Orlic D, Donahue RE, Fricker S, et al. AMD3100 mobilizes hematopoietic stem cells with long-term repopulating capacity in nonhuman primates. Blood. 2006;107(9):3772–8. https://doi.org/10.1182/blood-2005-09-3592 .
doi: 10.1182/blood-2005-09-3592
pubmed: 16439684
pmcid: 1895780
Domingues MJ, Nilsson SK, Cao B. New agents in HSC mobilization. Int J Hematol. 2017;105(2):141–52. https://doi.org/10.1007/s12185-016-2156-2 .
doi: 10.1007/s12185-016-2156-2
pubmed: 27905003
Rettig MP, Ansstas G, DiPersio JF. Mobilization of hematopoietic stem and progenitor cells using inhibitors of CXCR4 and VLA-4. Leukemia. 2012;26(1):34–53. https://doi.org/10.1038/leu.2011.197 .
doi: 10.1038/leu.2011.197
pubmed: 21886173
Cao B, Zhang Z, Grassinger J, Williams B, Heazlewood CK, Churches QI, et al. Therapeutic targeting and rapid mobilization of endosteal HSC using a small molecule integrin antagonist. Nat Commun. 2016;7:11007. https://doi.org/10.1038/ncomms11007 .
doi: 10.1038/ncomms11007
pubmed: 26975966
pmcid: 4796355
Karpova D, Rettig MP, Ritchey J, Cancilla D, Christ S, Gehrs L, et al. Targeting VLA4 integrin and CXCR2 mobilizes serially repopulating hematopoietic stem cells. J Clin Invest. 2019;129(7):2745–59. https://doi.org/10.1172/JCI124738 .
doi: 10.1172/JCI124738
pubmed: 31085833
pmcid: 6597242
Cosgun KN, Rahmig S, Mende N, Reinke S, Hauber I, Schäfer C, et al. Kit regulates HSC engraftment across the human-mouse species barrier. Cell Stem Cell. 2014;15(2):227–38. https://doi.org/10.1016/j.stem.2014.06.001 .
doi: 10.1016/j.stem.2014.06.001
pubmed: 25017720
Bernitz JM, Daniel MG, Fstkchyan YS, Moore K. Granulocyte colony-stimulating factor mobilizes dormant hematopoietic stem cells without proliferation in mice. Blood. 2017;129(14):1901–12. https://doi.org/10.1182/blood-2016-11-752923 .
doi: 10.1182/blood-2016-11-752923
pubmed: 28179275
pmcid: 5383874
Hölig K. G-CSF in healthy allogeneic stem cell donors. Transfus Med Hemother. 2013;40(4):225–35. https://doi.org/10.1159/000354196 .
doi: 10.1159/000354196
pubmed: 24179471
pmcid: 3776391
Pantin J, Purev E, Tian X, Cook L, Donohue-Jerussi T, Cho E, et al. Effect of high-dose plerixafor on CD34(+) cell mobilization in healthy stem cell donors: results of a randomized crossover trial. Haematologica. 2017;102(3):600–9. https://doi.org/10.3324/haematol.2016.147132 .
doi: 10.3324/haematol.2016.147132
pubmed: 27846612
pmcid: 5394957
Welschinger R, Liedtke F, Basnett J, Dela Pena A, Juarez JG, Bradstock KF, et al. Plerixafor (AMD3100) induces prolonged mobilization of acute lymphoblastic leukemia cells and increases the proportion of cycling cells in the blood in mice. Exp Hematol. 2013;41(3):293-302.e1. https://doi.org/10.1016/j.exphem.2012.11.004 .
doi: 10.1016/j.exphem.2012.11.004
pubmed: 23178377
Winkler IG, Wiercinska E, Barbier V, Nowlan B, Bonig H, Levesque JP. Mobilization of hematopoietic stem cells with highest self-renewal by G-CSF precedes clonogenic cell mobilization peak. Exp Hematol. 2016;44(4):303-14.e1. https://doi.org/10.1016/j.exphem.2016.01.001 .
doi: 10.1016/j.exphem.2016.01.001
pubmed: 26827874
Garcia-Perez L, van Roon L, Schilham MW, Lankester AC, Pike-Overzet K, Staal FJT. Combining mobilizing agents with busulfan to reduce chemotherapy-based conditioning for hematopoietic stem cell transplantation. Cells. 2021. https://doi.org/10.3390/cells10051077 .
doi: 10.3390/cells10051077
pubmed: 33946560
pmcid: 8147230