Artemis splice defects cause atypical SCID and can be restored in vitro by an antisense oligonucleotide

Genes and Immunity

Volumn 12, Issue 6, 2011, Pages 434-444

  Ijspeert, H ^a   Lankester, A C ^b   Van Den Berg, J M ^c   Wiegant, W ^b   Van Zelm, M C ^a   Weemaes, C M R ^d   Warris, A ^d   Pan Hammarstrom Q ^e   Pastink, A ^b   Van Tol, M J D ^b   Van Dongen, J J M ^a   Van Gent, D C ^a   Van Der Burg, M ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^e KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

antisense oligonucleotides; Artemis; granulomas; severe combined immunodeficiency; splicing; V(D)J recombination

Indexed keywords

ALEMTUZUMAB; ANTISENSE OLIGONUCLEOTIDE; BUSULFAN; CELL PROTEIN; CYCLOPHOSPHAMIDE; FLUDARABINE; IMMUNOGLOBULIN; PROTEIN ARTEMIS; THYMOCYTE ANTIBODY; UNCLASSIFIED DRUG;

ANTIBIOTIC PROPHYLAXIS; ARTICLE; CASE REPORT; CHILD; FEMALE; GENETIC RECOMBINATION; GRAFT REJECTION; GRANULOMATOUS SKIN DISEASE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOGLOBULIN DEFICIENCY; IN VITRO STUDY; IONIZING RADIATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; RADIOSENSITIVITY; RECURRENT INFECTION; RNA SPLICING; SCHOOL CHILD; SEVERE COMBINED IMMUNODEFICIENCY; STEM CELL TRANSPLANTATION; VDJ EXON;

B-LYMPHOCYTES; BASE SEQUENCE; CELLS, CULTURED; CHILD; FEMALE; HUMANS; MUTATION; NUCLEAR PROTEINS; OLIGORIBONUCLEOTIDES, ANTISENSE; RADIATION TOLERANCE; RADIATION, IONIZING; RNA SPLICE SITES; SEQUENCE ANALYSIS, DNA; SEVERE COMBINED IMMUNODEFICIENCY; T-LYMPHOCYTES;

EID: 80052290127     PISSN: 14664879     EISSN: 14765470     Source Type: Journal    
DOI: 10.1038/gene.2011.16     Document Type: Article

References (54)

1. Cowan MJ, Neven B, Cavazanna-Calvo M, Fischer A, Puck J. Hematopoietic stem cell transplantation for severe combined immunodeficiency diseases. Biol Blood Marrow Transplant 2008; 14: 73-75.
2. Pike-Overzet K, van der Burg M, Wagemaker G, van Dongen JJ, Staal FJ. New insights and unresolved issues regarding insertional mutagenesis in X-linked SCID gene therapy. Mol Ther 2007; 15: 1910-1916. (Pubitemid 350011729)
3. Cavazzana-Calvo M, Fischer A. Gene therapy for severe combined immunodeficiency: are we there yet? J Clin Invest 2007; 117: 1456-1465. (Pubitemid 46871328)
4. Buckley RH, Schiff RI, Schiff SE, Markert ML, Williams LW, Harville TO et al. Human severe combined immunodeficiency: genetic, phenotypic, and functional diversity in one hundred eight infants. J Pediatr 1997; 130: 378-387. (Pubitemid 27492681)
5. Geha RS, Notarangelo LD, Casanova JL, Chapel H, Conley ME, Fischer A et al. Primary immunodeficiency diseases: an update from the international union of immunological societies primary immunodeficiency diseases classification committee. J Allergy Clin Immunol 2007; 120: 776-794.
6. McBlane JF, van Gent DC, Ramsden DA, Romeo C, Cuomo CA, Gellert M et al. Cleavage at a V(D)J recombination signal requires only RAG1 and RAG2 proteins and occurs in two steps. Cell 1995; 83: 387-395.
7. van Gent DC, McBlane JF, Ramsden DA, Sadofsky MJ, Hesse JE, Gellert M. Initiation of V(D)J recombination in a cell-free system. Cell 1995; 81: 925-934.
8. Weterings E, van Gent DC. The mechanism of non-homologous end-joining: a synopsis of synapsis. DNA Repair (Amst) 2004; 3: 1425-1435. (Pubitemid 39221740)
9. Douglas P, Sapkota GP, Morrice N, Yu Y, Goodarzi AA, Merkle D et al. Identification of in vitro and in vivo phosphorylation sites in the catalytic subunit of the DNA-dependent protein kinase. Biochem J 2002; 368: 243-251. (Pubitemid 35463427)
10. Ma Y, Pannicke U, Schwarz K, Lieber MR. Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 2002; 108: 781-794. (Pubitemid 34327530)
11. Benedict CL, Gilfillan S, Thai TH, Kearney JF. Terminal deoxynucleotidyl transferase and repertoire development. Immunol Rev 2000; 175: 150-157. (Pubitemid 30427165)
12. Ahnesorg P, Smith P, Jackson SP. XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell 2006; 124: 301-313. (Pubitemid 43121979)
13. Buck D, Malivert L, de Chasseval R, Barraud A, Fondaneche MC, Sanal O et al. Cernunnos, a novel nonhomologous endjoining factor, is mutated in human immunodeficiency with microcephaly. Cell 2006; 124: 287-299. (Pubitemid 43121978)
14. Moshous D, Callebaut I, de Chasseval R, Corneo B, Cavazzana-Calvo M, Le Deist F et al. Artemis, a novel DNA doublestrand break repair/V(D)J recombination protein, is mutated in human severe combined immune deficiency. Cell 2001; 105: 177-186. (Pubitemid 32429508)
15. van Gent DC, van der Burg M. Non-homologous end-joining, a sticky affair. Oncogene 2007; 26: 7731-7740. (Pubitemid 350242453)
16. Noordzij JG, Verkaik NS, van der Burg M, van Veelen LR, de Bruin-Versteeg S, Wiegant W et al. Radiosensitive SCID patients with Artemis gene mutations show a complete Bcell differentiation arrest at the pre-B-cell receptor checkpoint in bone marrow. Blood 2003; 101: 1446-1452. (Pubitemid 36182519)
17. O'Driscoll M, Gennery AR, Seidel J, Concannon P, Jeggo PA. An overview of three new disorders associated with genetic instability: LIG4 syndrome, RS-SCID and ATR-Seckel syndrome. DNA Repair (Amst) 2004; 3: 1227-1235. (Pubitemid 38997966)
18. van der Burg M, van Veelen LR, Verkaik NS, Wiegant WW, Hartwig NG, Barendregt BH et al. A new type of radiosensitive T-B-NK+ severe combined immunodeficiency caused by a LIG4 mutation. J Clin Invest 2006; 116: 137-145. (Pubitemid 43121798)
19. van der Burg M, Ijspeert H, Verkaik NS, Turul T,WiegantWW, 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 2009; 119: 91-98.
20. Villa A, Santagata S, Bozzi F, Giliani S, Frattini A, Imberti L et al. Partial V(D)J recombination activity leads to Omenn syndrome. Cell 1998; 93: 885-896. (Pubitemid 28257593)
21. Ege M, Ma Y, Manfras B, Kalwak K, Lu H, Lieber MR et al. Omenn syndrome due to ARTEMIS mutations. Blood 2005; 105: 4179-4186. (Pubitemid 40720760)
22. de Saint-Basile G, Le Deist F, de Villartay JP, Cerf-Bensussan N, Journet O, Brousse N et al. Restricted heterogeneity of T lymphocytes in combined immunodeficiency with hypereosinophilia (Omenn0s syndrome). J Clin Invest 1991; 87: 1352-1359.
23. Du L, van der Burg M, Popov SW, Kotnis A, van Dongen JJ, Gennery AR et al. Involvement of Artemis in nonhomologous end-joining during immunoglobulin class switch recombination. J Exp Med 2008; 205: 3031-3040.
24. Schuetz C, Huck K, Gudowius S, Megahed M, Feyen O, Hubner B et al. An immunodeficiency disease with RAG mutations and granulomas. N Engl J Med 2008; 358: 2030-2038. (Pubitemid 351656457)
25. de Jager M, Blokx W, Warris A, Bergers M, Link M, Weemaes C et al. Immunohistochemical features of cutaneous granulomas in primary immunodeficiency disorders: a comparison with cutaneous sarcoidosis. J Cutan Pathol 2008; 35: 467-472. (Pubitemid 351519416)
26. Rohr J, Pannicke U, Doring M, Schmitt-Graeff A, Wiech E, Busch A et al. Chronic inflammatory bowel disease as key manifestation of atypical ARTEMIS deficiency. J Clin Immunol 2010; 30: 314-320.
27. van der Burg M, Verkaik NS, den Dekker AT, Barendregt BH, Pico-Knijnenburg I, Tezcan I et al. Defective Artemis nuclease is characterized by coding joints with microhomology in long palindromic-nucleotide stretches. Eur J Immunol 2007; 37: 3522-3528.
28. Jurka J, Milosavljevic A. Reconstruction and analysis of human Alu genes. J Mol Evol 1991; 32: 105-121.
29. Jung D, Giallourakis C, Mostoslavsky R, Alt FW. Mechanism and control of V(D)J recombination at the immunoglobulin heavy chain locus. Annu Rev Immunol 2006; 24: 541-570.
30. Pan Q, Petit-Frere C, Lahdesmaki A, Gregorek H, Chrzanowska KH, Hammarstrom L. Alternative end joining during switch recombination in patients with ataxia-telangiectasia. Eur J Immunol 2002; 32: 1300-1308. (Pubitemid 34546257)
31. Lahdesmaki A, Taylor AM, Chrzanowska KH, Pan-Hammarstrom Q. Delineation of the role of the Mre11 complex in class switch recombination. J Biol Chem 2004; 279: 16479-16487. (Pubitemid 38509346)
32. Aartsma-Rus A, van Ommen GJ. Antisense-mediated exon skipping: a versatile tool with therapeutic and research applications. RNA 2007; 13: 1609-1624. (Pubitemid 47481669)
33. 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: 183-192.
34. Lev-Maor G, Sorek R, Shomron N, Ast G. The birth of an alternatively spliced exon: 30 splice-site selection in Alu exons. Science 2003; 300: 1288-1291. (Pubitemid 36618239)
35. van Zelm MC, Geertsema C, Nieuwenhuis N, de Ridder D, Conley ME, Schiff C et al. Gross deletions involving IGHM, BTK, or Artemis: a model for genomic lesions mediated by transposable elements. Am J Hum Genet 2008; 82: 320-332. (Pubitemid 351726105)
36. Grosso AR, Gomes AQ, Barbosa-Morais NL, Caldeira S, Thorne NP, Grech G et al. Tissue-specific splicing factor gene expression signatures. Nucleic Acids Res 2008; 36: 4823-4832.
37. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C et al. Alternative isoform regulation in human tissue transcriptomes. Nature 2008; 456: 470-476. (Pubitemid 352759009)
38. Rivera-Munoz P, Soulas-Sprauel P, Le Guyader G, Abramowski V, Bruneau S, Fischer A et al. Reduced immunoglobulin class switch recombination in the absence of Artemis. Blood 2009; 114: 3601-3609.
39. Notarangelo LD, Forino C, Mazzolari E. Stem cell transplantation in primary immunodeficiencies. Curr Opin Allergy Clin Immunol 2006; 6: 443-448. (Pubitemid 44714157)
40. Qasim W, Gaspar HB, Thrasher AJ. Progress and prospects: gene therapy for inherited immunodeficiencies. Gene Ther 2009; 16: 1285-1291.
41. 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: 4114-4124.
42. Hacein-Bey-Abina S, Von Kalle C, Schmidt M, McCormack MP, Wulffraat N, Leboulch P et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCIDX1. Science 2003; 302: 415-419. (Pubitemid 37296260)
43. Hu H, Gatti RA. New approaches to treatment of primary immunodeficiencies: fixing mutations with chemicals. Curr Opin Allergy Clin Immunol 2008; 8: 540-546.
44. van Deutekom JC, Janson AA, Ginjaar IB, Frankhuizen WS, Aartsma-Rus A, Bremmer-Bout M et al. Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med 2007; 357: 2677-2686.
45. Noordzij JG, de Bruin-Versteeg S, Verkaik NS, Vossen JM, de Groot R, Bernatowska E et al. The immunophenotypic and immunogenotypic B-cell differentiation arrest in bone marrow of RAG-deficient SCID patients corresponds to residual recombination activities of mutated RAG proteins. Blood 2002; 100: 2145-2152. (Pubitemid 35001250)
46. van der Velden VH, Hochhaus A, Cazzaniga G, Szczepanski T, Gabert J, van Dongen JJ. Detection of minimal residual disease in hematologic malignancies by real-time quantitative PCR: principles, approaches, and laboratory aspects. Leukemia 2003; 17: 1013-1034. (Pubitemid 36722231)
47. Lefranc MP. IMGT databases, web resources and tools for immunoglobulin and T cell receptor sequence analysis http://imgt.cines.fr Leukemia 2003; 17: 260-266.
48. Pan Q, Petit-Frere C, Dai S, Huang P, Morton HC, Brandtzaeg P, et al. Regulation of switching and production of IgA in human B cells in donors with duplicated alpha1 genes. Eur J Immunol 2001; 31: 3622-3630. (Pubitemid 34030975)
49. Pan-Hammarstrom Q, Jones AM, Lahdesmaki A, Zhou W, Gatti RA, Hammarstrom L et al. Impact of DNA ligase IV on nonhomologous end joining pathways during class switch recombination in human cells. J Exp Med 2005; 201: 189-194. (Pubitemid 40189427)
50. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003; 31: 3406-3415. (Pubitemid 37442169)
51. Aartsma-Rus A, van Vliet L, Hirschi M, Janson AA, Heemskerk H, de Winter CL et al. Guidelines for antisense oligonucleotide design and insight into splice-modulating mechanisms. Mol Ther 2009; 17: 548-553.
52. van Dongen JJ, Macintyre EA, Gabert JA, Delabesse E, Rossi V, Saglio G et al. Standardized RT-PCR analysis of fusion gene transcripts from chromosome aberrations in acute leukemia for detection of minimal residual disease. Report of the BIOMED-1 Concerted Action: investigation of minimal residual disease in acute leukemia. Leukemia 1999; 13: 1901-1928.
53. Comans-Bitter WM, de Groot R, van den Beemd R, Neijens HJ, Hop WC, Groeneveld K et al. Immunophenotyping of blood lymphocytes in childhood. Reference values for lymphocyte subpopulations. J Pediatr 1997; 130: 388-393. (Pubitemid 27492682)
54. de Vries E, Kuijpers TW, van Tol MJD, van der Meer JWM, Weemaes CMR, van Dongen JJM. Diagnostiek bij vermoeden van een afweerstoornis:inleiding. Ned Tijdschr Geneeskd 2000; 144: 2192-2196.