Radiation-sensitive severe combined immunodeficiency: The arguments for and against conditioning before hematopoietic cell transplantation—what to do?

Journal of Allergy and Clinical Immunology

Volumn 136, Issue 5, 2015, Pages 1178-1185

  Cowan, Morton J ^a   Gennery, Andrew R ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Newcastle Upon Tyne Hospitals NHS Foundation Trust   (United Kingdom)

Author keywords

DNA repair; hematopoietic cell transplantation; nonhomologous end joining; radiation sensitivity; Severe combined immunodeficiency

Indexed keywords

BUSULFAN; CYCLOPHOSPHAMIDE; FLUDARABINE; STEM CELL FACTOR RECEPTOR; ATP DEPENDENT DNA LIGASE; CELL CYCLE PROTEIN; DCLRE1C PROTEIN, HUMAN; DNA BINDING PROTEIN; DNA DEPENDENT PROTEIN KINASE; DNA LIGASE; LIG4 PROTEIN, HUMAN; NBN PROTEIN, HUMAN; NHEJ1 PROTEIN, HUMAN; NUCLEAR PROTEIN; PRKDC PROTEIN, HUMAN;

ARTICLE; DNA END JOINING REPAIR; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; PHENOTYPE; PRIORITY JOURNAL; RADIOSENSITIVITY; SEVERE COMBINED IMMUNODEFICIENCY; TRANSPLANTATION CONDITIONING; TREATMENT OUTCOME; ANIMAL; DNA REPAIR; GENE THERAPY; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; PROCEDURES; RADIATION; RADIATION TOLERANCE;

ANIMALS; CELL CYCLE PROTEINS; DNA LIGASE ATP; DNA LIGASES; DNA REPAIR; DNA REPAIR ENZYMES; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; GENETIC THERAPY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; IMMUNOTHERAPY; NUCLEAR PROTEINS; RADIATION; RADIATION TOLERANCE; SEVERE COMBINED IMMUNODEFICIENCY; TRANSPLANTATION CONDITIONING;

EID: 84930336698     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2015.04.027     Document Type: Article

References (49)

1. Iyama, T., Wilson, D.M. 3rd, DNA repair mechanisms in dividing and non-dividing cells. DNA Repair (Amst) 12 (2013), 620–636.
2. Czornak, K., Chughtai, S., Chrzanowska, K.H., Mystery of DNA repair: the role of the MRN complex and ATM kinase in DNA damage repair. J Appl Genet 49 (2008), 383–396.
3. Pietzner, J., Baer, P.C., Duecker, R.P., Merscher, M.B., Satzger-Prodinger, C., Bechmann, I., et al. Bone marrow transplantation improves the outcome of Atm-deficient mice through the migration of ATM-competent cells. Hum Mol Genet 22 (2013), 493–507.
4. Deriano, L., Roth, D.B., Modernizing the nonhomologous end-joining repertoire: alternative and classical NHEJ share the stage. Annu Rev Genet 47 (2013), 433–455.
5. Moshous, D., Callebaut, I., de Chasseval, R., Corneo, B., Cavazzana-Calvo, M., Le Deist, F., et al. Artemis, a novel DNA double-strand break repair/V(D)J recombination protein, is mutated in human severe combined immune deficiency. Cell 105 (2001), 177–186.
6. van der Burg, M., Ijspeert, H., Verkaik, N.S., Turul, T., Wiegant, W.W., Morotomi-Yano, K., et al. A DNA-PKcs mutation in a radiosensitive T-B- SCID patient inhibits Artemis activation and nonhomologous end-joining. J Clin Invest 119 (2009), 91–98.
7. Enders, A., Fisch, P., Schwarz, K., Duffner, U., Pannicke, U., Nikolopoulos, E., et al. A severe form of human combined immunodeficiency due to mutations in DNA ligase IV. J Immunol 176 (2006), 5060–5068.
8. Buck, D., Malivert, L., de Chasseval, R., Barraud, A., Fondanèche, M.C., Sanal, O., et al. Cernunnos, a novel nonhomologous end-joining factor, is mutated in human immunodeficiency with microcephaly. Cell 124 (2006), 287–299.
9. Felgentreff, K., Du, L., Weinacht, K.G., Dobbs, K., Bartish, M., Giliani, S., et al. Differential role of nonhomologous end joining factors in the generation, DNA damage response, and myeloid differentiation of human induced pluripotent stem cells. Proc Natl Acad Sci U S A 111 (2014), 8889–8894.
10. Musio, A., Marrella, V., Sobacchi, C., Rucci, F., Fariselli, L., Giliani, S., et al. Damaging-agent sensitivity of Artemis-deficient cell lines. Eur J Immunol 35 (2005), 1250–1256.
11. Evans, P.M., Woodbine, L., Riballo, E., Gennery, A.R., Hubank, M., Jeggo, P.A., Radiation-induced delayed cell death in a hypomorphic Artemis cell line. Hum Mol Genet 15 (2006), 1303–1311.
12. Lavin, M.F., Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat Rev Mol Cell Biol 10 (2008), 759–769.
13. Ussowicz, M., Musiał J., Duszeńko, E., Haus, O., Kałwak, K., Long-term survival after allogeneic-matched sibling PBSC transplantation with conditioning consisting of low-dose busilvex and fludarabine in a 3-year-old boy with ataxia-telangiectasia syndrome and ALL. Bone Marrow Transplant 48 (2013), 740–741.
14. Haddad, E., Leroy, S., Buckley, R.H., B-cell reconstitution for SCID: should a conditioning regimen be used in SCID treatment?. J Allergy Clin Immunol 131 (2013), 994–1000.
15. 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 113 (2009), 4114–4124.
16. Pai, S.Y., Logan, B.R., Griffith, L.M., Buckley, R.H., Parrott, R.E., Dvorak, C.C., et al. Transplantation outcomes for severe combined immunodeficiency, 2000-2009. N Engl J Med 371 (2014), 434–446.
17. Buckley, R.H., Win, C.M., Moser, B.K., Parrott, R.E., Sajaroff, E., Sarzotti-Kelsoe, M., Post-transplantation B cell function in different molecular types of SCID. J Clin Immunol 33 (2013), 96–110.
18. Dvorak, C.C., Hassan, A., Slatter, M.A., Hönig, M., Lankester, A.C., Buckley, R.H., et al. Comparison of outcomes of hematopoietic stem cell transplantation without chemotherapy conditioning by using matched sibling and unrelated donors for treatment of severe combined immunodeficiency. J Allergy Clin Immunol 134 (2014), 935–943.e15.
19. Dvorak, C.C., Hung, G.Y., Horn, B., Dunn, E., Oon, C.Y., Cowan, M.J., Megadose CD34(+) cell grafts improve recovery of T cell engraftment but not B cell immunity in patients with severe combined immunodeficiency disease undergoing haplocompatible nonmyeloablative transplantation. Biol Blood Marrow Transplant 14 (2008), 1125–1133.
20. Schuetz, C., Neven, B., Dvorak, C.C., Leroy, S., Ege, M.J., Pannicke, U., et al. SCID patients with ARTEMIS vs RAG deficiencies following HCT: increased risk of late toxicity in ARTEMIS-deficient SCID. Blood 123 (2014), 281–289.
21. Dvorak, C.C., Horn, B.N., Puck, J.M., Adams, S., Veys, P., Czechowicz, A., et al. A trial of Alemtuzumab adjunctive therapy in allogeneic hematopoietic cell transplantation with minimal conditioning for severe combined immunodeficiency. Pediatr Transplant 18 (2014), 609–616.
22. Kwan, A., Abraham, R.S., Currier, R., Brower, A., Andruszewski, K., Abbott, J.K., et al. Newborn screening for severe combined immunodeficiency in 11 screening programs in the United States. JAMA 312 (2014), 729–738.
23. Grunebaum, E., Bates, A., Roifman, C.M., Omenn syndrome is associated with mutations in DNA ligase IV. J Allergy Clin Immunol 122 (2008), 1219–1220.
24. O'Driscoll, M., Cerosaletti, K.M., Girard, P.M., Dai, Y., Stumm, M., Kysela, B., et al. DNA ligase IV mutations identified in patients exhibiting developmental delay and immunodeficiency. Mol Cell 8 (2001), 1175–1185.
25. Gruhn, B., Seidel, J., Zintl, F., Varon, R., Tönnies, H., Neitzel, H., et al. Successful bone marrow transplantation in a patient with DNA ligase IV deficiency and bone marrow failure. Orphanet J Rare Dis, 2, 2007, 5.
26. Buck, D., Moshous, D., de Chasseval, R., Ma, Y., le Deist, F., Cavazzana-Calvo, M., et al. Severe combined immunodeficiency and microcephaly in siblings with hypomorphic mutations in DNA ligase IV. Eur J Immunol 36 (2006), 224–235.
27. van der Burg, M., van Veelen, L.R., Verkaik, N.S., Wiegant, W.W., Hartwig, N.G., Barendregt, B.H., et al. A new type of radiosensitive T-B-NK+ severe combined immunodeficiency caused by a LIG4 mutation. J Clin Invest 116 (2006), 137–145.
28. Straathof, K.C., Rao, K., Eyrich, M., Hale, G., Bird, P., Berrie, E., et al. Haemopoietic stem-cell transplantation with antibody-based minimal-intensity conditioning: a phase 1/2 study. Lancet 374 (2009), 912–920.
29. Unal, S., Cerosaletti, K., Uckan-Cetinkaya, D., Cetin, M., Gumruk, F., A novel mutation in a family with DNA ligase IV deficiency syndrome. Pediatr Blood Cancer 53 (2009), 482–484.
30. Faraci, M., Lanino, E., Micalizzi, C., Morreale, G., Di Martino, D., Banov, L., et al. Unrelated hematopoietic stem cell transplantation for Cernunnos-XLF deficiency. Pediatr Transplant 13 (2009), 785–789.
31. Dai, Y., Kysela, B., Hanakahi, L.A., Manolis, K., Riballo, E., Stumm, M., et al. Nonhomologous end joining and V(D)J recombination require an additional factor. Proc Natl Acad Sci U S A 100 (2003), 2462–2467.
32. Çağdaş D., Özgür, T.T., Asal, G.T., Revy, P., De Villartay, J.P., van der Burg, M., et al. Two SCID cases with Cernunnos-XLF deficiency successfully treated by hematopoietic stem cell transplantation. Pediatr Transplant 16 (2012), E167–E171.
33. Ivović V., Ajzenberg, D., Djurković-Djaković O., Atypical strain of Toxoplasma gondii causing fatal reactivation after hematopoietic stem cell transplantation in a patient with an underlying immunological deficiency. J Clin Microbiol 51 (2013), 2686–2690.
34. Albert, M.H., Gennery, A.R., Greil, J., Cale, C.M., Kalwak, K., Kondratenko, I., et al. Successful SCT for Nijmegen breakage syndrome. Bone Marrow Transplant 45 (2010), 622–626.
35. Woźniak, M., Krzywoń M., Hołda, M.K., Goździk, J., Reduced-intensity conditioning umbilical cord blood transplantation in Nijmegen breakage syndrome. Pediatr Transplant 19 (2015), E51–E55.
36. O'Marcaigh, A.S., DeSantes, K., Hu, D., Pabst, H., Horn, B., Li, L., et al. Bone marrow transplantation for T-B- severe combined immunodeficiency disease in Athabascan-speaking native Americans. Bone Marrow Transplant 27 (2001), 703–709.
37. Mazzolari, E., Forino, C., Guerci, S., Imberti, L., Lanfranchi, A., Porta, F., et al. Long-term immune reconstitution and clinical outcome after stem cell transplantation for severe T-cell immunodeficiency. J Allergy Clin Immunol 120 (2007), 892–899.
38. Cavazzana-Calvo, M., Carlier, F., Le Deist, F., Morillon, E., Taupin, P., Gautier, D., et al. Long-term T-cell reconstitution after hematopoietic stem-cell transplantation in primary T-cell-immunodeficient patients is associated with myeloid chimerism and possibly the primary disease phenotype. Blood 109 (2007), 4575–4581.
39. Woodbine, L., Neal, J.A., Sasi, N.K., Shimada, M., Deem, K., Coleman, H., et al. PRKDC mutations in a SCID patient with profound neurological abnormalities. J Clin Invest 123 (2013), 2969–2980.
40. Slatter, M.A., Bhattacharya, A., Abinun, M., Flood, T.J., Cant, A.J., Gennery, A.R., Outcome of boost haemopoietic stem cell transplant for decreased donor chimerism or graft dysfunction in primary immunodeficiency. Bone Marrow Transplant 35 (2005), 683–689.
41. Savic, R.M., Cowan, M.J., Dvorak, C.C., Pai, S.Y., Pereira, L., Bartelink, I.H., et al. Effect of weight and maturation on busulfan clearance in infants and small children undergoing hematopoietic cell transplantation. Biol Blood Marrow Transplant 19 (2013), 1608–1614.
42. Czechowicz, A., Kraft, D., Weissman, I.L., Bhattacharya, D., Efficient transplantation via antibody-based clearance of hematopoietic stem cell niches. Science 318 (2007), 1296–1299.
43. Robertson, L.E., Denny, A.W., Huh, Y.O., Plunkett, W., Keating, M.J., Nelson, J.A., Natural killer cell activity in chronic lymphocytic leukemia patients treated with fludarabine. Cancer Chemother Pharmacol 37 (1996), 445–450.
44. Burroughs, L.M., Nemecek, E.R., Torgerson, T.R., Storer, B.E., Talano, J.A., Domm, J., et al. Treosulfan-based conditioning and hematopoietic cell transplantation for nonmalignant diseases: a prospective multicenter trial. Biol Blood Marrow Transplant 12 (2014), 1996–2003.
45. Railey, M.D., Lokhnygina, Y., Buckley, R.H., Long-term clinical outcome of patients with severe combined immunodeficiency who received related donor bone marrow transplants without pretransplant chemotherapy or post-transplant GVHD prophylaxis. J Pediatr 155 (2009), 834–840.
46. van der Burg, M., Weemaes, C.M., Preijers, F., Brons, P., Barendregt, B.H., van Tol, M.J., et al. B-cell recovery after stem cell transplantation of Artemis-deficient SCID requires elimination of autologous bone marrow precursor-B-cells. Haematologica 91 (2006), 1705–1709.
47. Myers, L.A., Patel, D.D., Puck, J.M., Buckley, R.H., Hematopoietic stem cell transplantation for severe combined immunodeficiency in the neonatal period leads to superior thymic output and improved survival. Blood 99 (2002), 872–878.
48. Mostoslavsky, G., Fabian, A.J., Rooney, S., Alt, F.W., Mulligan, R.C., Complete correction of murine Artemis immunodeficiency by lentiviral vector-mediated gene transfer. Proc Natl Acad Sci U S A 103 (2006), 16406–16411.
49. Benjelloun, F., Garrigue, A., Demerens-de Chappedelaine, C., Soulas-Sprauel, P., Malassis-Séris, M., Stockholm, D., et al. Stable and functional lymphoid reconstitution in Artemis-deficient mice following lentiviral artemis gene transfer into hematopoietic stem cells. Mol Ther 16 (2008), 1490–1499.