Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease

Nature Medicine

Volumn 16, Issue 2, 2010, Pages 198-204

  Stein, Stefan ^a   Ott, Marion G ^b   Schultze Strasser, Stephan ^a   Jauch, Anna ^c   Burwinkel, Barbara ^c,d   Kinner, Andrea ^a   Schmidt, Manfred ^d   Krämer, Alwin ^e   Schwäble, Joachim ^b   Glimm, Hanno ^d   Koehl, Ulrike ^b   Preiss, Carolin ^a   Ball, Claudia ^d   Martin, Hans ^b   Göhring, Gudrun ^f   Schwarzwaelder, Kerstin ^d   Hofmann, Wolf Karsten ^g   Karakaya, Kadin ^e   Tchatchou, Sandrine ^c,d   Yang, Rongxi ^c,d   Reinecke, Petra ^h   Kühlcke, Klaus ⁱ   Schlegelberger, Brigitte ^f   Thrasher, Adrian J ^j   Hoelzer, Dieter ^b   Seger, Reinhard ^k   Von Kalle, Christof ^d   Grez, Manuel ^a   more..

^a Institute for Biomedical Research   (Germany)

^b UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^c UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e UNIVERSITY OF HEIDELBERG   (Germany)

^f HANNOVER MEDICAL SCHOOL   (Germany)

^g CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^h HEINRICH HEINE UNIVERSITY   (Germany)

ⁱ BIONTECH AG   (Germany)

^j GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^k UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE COLONY STIMULATING FACTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ADULT; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ARTICLE; CASE REPORT; CHRONIC GRANULOMATOUS DISEASE; EXTRAMEDULLARY HEMATOPOIESIS; GENE EXPRESSION; GENE SILENCING; GENE THERAPY; GENOMIC INSTABILITY; HISTOPATHOLOGY; HUMAN; IMMUNE DEFICIENCY; MONOSOMY 7; MYELODYSPLASTIC SYNDROME; PRIORITY JOURNAL; SPLENECTOMY; SPLENOMEGALY; TRANSGENE; TREATMENT OUTCOME;

ADULT; CHROMOSOMES, HUMAN, PAIR 7; DNA-BINDING PROTEINS; GENE THERAPY; GENOMIC INSTABILITY; GRANULOMATOUS DISEASE, CHRONIC; HUMANS; MONOSOMY; MYELODYSPLASTIC SYNDROMES; NADPH OXIDASE; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENES; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS);

EID: 76249131912     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2088     Document Type: Article

References (59)

1. Cavazzana-Calvo, M., et al. Gene therapy of human severe combined immunodefciency (SCID)-X1 disease. Science 288, 669-672 (2000). (Pubitemid 30241569)
2. Aiuti, A., et al. Correction of ADA-SCID by stem cell gene therapy combined with nonmyeloablative conditioning. Science 296, 2410-2413 (2002).
3. Gaspar, H.B., et al. Gene therapy of X-linked severe combined immunodefciency by use of a pseudotyped gammaretroviral vector. Lancet 364, 2181-2187 (2004).
4. Gaspar, H.B., et al. Successful reconstitution of immunity in ADA-SCID by stem cell gene therapy following cessation of PEG-ADA and use of mild preconditioning. Mol. Ther. 14, 505-513 (2006).
5. Aiuti, A., et al. Gene therapy for immunodefciency due to adenosine deaminase defciency. N. Engl. J. Med. 360, 447-458 (2009).
6. Hacein-Bey-Abina, S., et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302, 415-419 (2003).
7. Hacein-Bey-Abina, S., et al. A serious adverse event after successful gene therapy for X-linked severe combined immunodefciency. N. Engl. J. Med. 348, 255-256 (2003).
8. Howe, S.J., et al. Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J. Clin. Invest. 118, 3143-3150 (2008).
9. Hacein-Bey-Abina, S., et al. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J. Clin. Invest. 118, 3132-3142 (2008).
10. Dinauer, M.C. The respiratory burst oxidase and the molecular genetics of chronic granulomatous disease. Crit. Rev. Clin. Lab. Sci. 30, 329-369 (1993).
11. Roos, D. The genetic basis of chronic granulomatous disease. Immunol. Rev. 138, 121-157 (1994). (Pubitemid 24147419)
12. Segal, A.W. The NADPH oxidase and chronic granulomatous disease. Mol. Med. Today 2, 129-135 (1996).
13. Malech, H.L. & Hickstein, D.D. Genetics, biology and clinical management of myeloid cell primary immune defciencies: chronic granulomatous disease and leukocyte adhesion defciency. Curr. Opin. Hematol. 14, 29-36 (2007).
14. Ott, M.G., et al. Correction of X-linked chronic granulomatous disease by gene therapy, augmented by insertional activation of MDS1-EVI1, PRDM16 or SETBP1. Nat. Med. 12, 401-409 (2006).
15. Fears, S., et al. Intergenic splicing of MDS1 and EVI1 occurs in normal tissues as well as in myeloid leukemia and produces a new member of the PR domain family. Proc. Natl. Acad. Sci. USA 93, 1642-1647 (1996).
16. Hamaguchi, H., et al. Establishment of a novel human myeloid leukaemia cell line (HNT-34) with t(3;3)(q21;q26), t(9;22)(q34;q11) and the expression of EVI1 gene, P210 and P190 BCR/ABL chimaeric transcripts from a patient with AML after MDS with 3q21q26 syndrome. Br. J. Haematol. 98, 399-407 (1997).
17. Claus, R. & Lubbert, M. Epigenetic targets in hematopoietic malignancies. Oncogene 22, 6489-6496 (2003).
18. Nolte, F. & Hofmann, W.K. Myelodysplastic syndromes: molecular pathogenesis and genomic changes. Ann. Hematol. 87, 777-795 (2008).
19. Christiansen, D.H., Andersen, M.K. & Pedersen-Bjergaard, J. Methylation of p15INK4B is common, is associated with deletion of genes on chromosome arm 7q and predicts a poor prognosis in therapy-related myelodysplasia and acute myeloid leukemia. Leukemia 17, 1813-1819 (2003).
20. Rogakou, E.P., Pilch, D.R., Orr, A.H., Ivanova, V.S. & Bonner, W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858-5868 (1998).
21. Khanna, K.K. & Jackson, S.P. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 27, 247-254 (2001).
22. Fernandez-Capetillo, O., Celeste, A. & Nussenzweig, A. Focusing on foci: H2AX and the recruitment of DNA-damage response factors. Cell Cycle 2, 426-427 (2003).
23. Kearns, W.G., Yamaguchi, H., Young, N.S. & Liu, J.M. Centrosome amplifcation and aneuploidy in bone marrow failure patients. Genes Chromosomes Cancer 40, 329-333 (2004).
24. Neben, K., Giesecke, C., Schweizer, S., Ho, A.D. & Kramer, A. Centrosome aberrations in acute myeloid leukemia are correlated with cytogenetic risk profle. Blood 101, 289-291 (2003).
25. Ganem, N.J., Godinho, S.A. & Pellman, D. A mechanism linking extra centrosomes to chromosomal instability. Nature 460, 278-282 (2009).
26. Dinauer, M.C., Curnutte, J.T., Rosen, H. & Orkin, S.H. A missense mutation in the neutrophil cytochrome b heavy chain in cytochrome-positive X-linked chronic granulomatous disease. J. Clin. Invest. 84, 2012-2016 (1989).
27. Wang, L., Robbins, P.B., Carbonaro, D.A. & Kohn, D.B. High-resolution analysis of cytosine methylation in the 5′ long terminal repeat of retroviral vectors. Hum. Gene Ther. 9, 2321-2330 (1998).
28. Frank, O., et al. Tumor cells escape suicide gene therapy by genetic and epigenetic instability. Blood 104, 3543-3549 (2004).
29. Burns, W.R., Zheng, Z., Rosenberg, S.A. & Morgan, R.A. Lack of specifc gamma-retroviral vector long terminal repeat promoter silencing in patients receiving genetically engineered lymphocytes and activation upon lymphocyte restimulation. Blood 114, 2888-2899 (2009).
30. Metais, J.Y. & Dunbar, C.E. The MDS1-EVI1 gene complex as a retrovirus integration site: impact on behavior of hematopoietic cells and implications for gene therapy. Mol. Ther. 16, 439-449 (2008).
31. Du, Y., Jenkins, N.A. & Copeland, N.G. Insertional mutagenesis identifes genes that promote the immortalization of primary bone marrow progenitor cells. Blood 106, 3932-3939 (2005).
32. Calmels, B., et al. Recurrent retroviral vector integration at the MDS1-EVI1 locus in non-human primate hematopoietic cells. Blood 106, 2530-2533 (2005).
33. Li, Z., et al. Murine leukemia induced by retroviral gene marking. Science 296, 497 (2002).
34. Modlich, U., et al. Leukemia induction after a single retroviral vector insertion in Evi1 or Prdm16. Leukemia 22, 1519-1528 (2008).
35. Buonamici, S., et al. EVI1 induces myelodysplastic syndrome in mice. J. Clin. Invest. 114, 713-719 (2004).
36. Du, Y., Spence, S.E., Jenkins, N.A. & Copeland, N.G. Cooperating cancer-gene identifcation through oncogenic-retrovirus-induced insertional mutagenesis. Blood 106, 2498-2505 (2005).
37. Nucifora, G. The EVI1 gene in myeloid leukemia. Leukemia 11, 2022-2031 (1997).
38. Dreyfus, F., et al. Expression of the Evi-1 gene in myelodysplastic syndromes. Leukemia 9, 203-205 (1995).
39. Barjesteh van Waalwijk van Doorn-Khosrovani, S, et al. High EVI1 expression predicts poor survival in acute myeloid leukemia: a study of 319 de novo AML patients. Blood 101, 837-845 (2003).
40. Charrin, C., et al. Structural rearrangements of chromosome 3 in 57 patients with acute myeloid leukemia: clinical, hematological and cytogenetic features. Hematol. J. 3, 21-31 (2002).
41. Lin, P., Medeiros, L.J., Yin, C.C. & Abruzzo, L.V. Translocation (3;8)(q26;q24): a recurrent chromosomal abnormality in myelodysplastic syndrome and acute myeloid leukemia. Cancer Genet. Cytogenet. 166, 82-85 (2006).
42. Stevens-Kroef, M., et al. Translocation t(2;3)(p15-23;q26-27) in myeloid malignancies: report of 21 new cases, clinical, cytogenetic and molecular genetic features. Leukemia 18, 1108-1114 (2004).
43. Trubia, M., et al. Characterization of a recurrent translocation t(2;3)(p15-22;q26) occurring in acute myeloid leukaemia. Leukemia 20, 48-54 (2006).
44. Laricchia-Robbio, L. & Nucifora, G. Signifcant increase of self-renewal in hematopoietic cells after forced expression of EVI1. Blood Cells Mol. Dis. 40, 141-147 (2007).
45. Perkins, A.S., Mercer, J.A., Jenkins, N.A. & Copeland, N.G. Patterns of Evi-1 expression in embryonic and adult tissues suggest that Evi-1 plays an important regulatory role in mouse development. Development 111, 479-487 (1991).
46. Kustikova, O.S., et al. Retroviral vector insertion sites associated with dominant hematopoietic clones mark "stemness" pathways. Blood 109, 1897-1907 (2007).
47. Senyuk, V., et al. Repression of RUNX1 activity by EVI1: a new role of EVI1 in leukemogenesis. Cancer Res. 67, 5658-5666 (2007).
48. Chi, Y., Senyuk, V., Chakraborty, S. & Nucifora, G. EVI1 promotes cell proliferation by interacting with BRG1 and blocking the repression of BRG1 on E2F1 activity. J. Biol. Chem. 278, 49806-49811 (2003).
49. Cattaneo, F. & Nucifora, G. EVI1 recruits the histone methyltransferase SUV39H1 for transcription repression. J. Cell. Biochem. 105, 344-352 (2008).
50. Spensberger, D. & Delwel, R. A novel interaction between the proto-oncogene Evi1 and histone methyltransferases, SUV39H1 and G9a. FEBS Lett. 582, 2761-2767 (2008).
51. Spensberger, D., et al. Myeloid transforming protein Evi1 interacts with methyl-CpG binding domain protein 3 and inhibits in vitro histone deacetylation by Mbd3/Mi-2/ NuRD. Biochemistry 47, 6418-6426 (2008).
52. Kondo, Y., et al. Downregulation of histone H3 lysine 9 methyltransferase G9a induces centrosome disruption and chromosome instability in cancer cells. PLoS One 3, e2037 (2008).
53. Krämer, A., Neben, K. & Ho, A.D. Centrosome replication, genomic instability and cancer. Leukemia 16, 767-775 (2002).
54. Zhang, Y., et al. MLL5 contributes to hematopoietic stem cell ftness and homeostasis. Blood 113, 1455-1463 (2009).
55. Heuser, M., et al. Loss of MLL5 results in pleiotropic hematopoietic defects, reduced neutrophil immune function, and extreme sensitivity to DNA demethylation. Blood 113, 1432-1443 (2009).
56. Madan, V., et al. Impaired function of primitive hematopoietic cells in mice lacking the mixed-lineage-leukemia homolog MLL5. Blood 113, 1444-1454 (2009).
57. Sebastian, S., et al. MLL5, a trithorax homolog, indirectly regulates H3K4 methylation, represses cyclin A2 expression, and promotes myogenic differentiation. Proc. Natl. Acad. Sci. USA 106, 4719-4724 (2009).
58. Cartier, N., et al. Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326, 818-823 (2009).
59. Schmidt, M., et al. High-resolution insertion-site analysis by linear amplifcation-mediated PCR (LAM-PCR). Nat. Methods 4, 1051-1057 (2007).