An Artemis polymorphic variant reduces Artemis activity and confers cellular radiosensitivity

DNA Repair

Volumn 9, Issue 9, 2010, Pages 1003-1010

  Woodbine, Lisa ^a   Grigoriadou, Sofia ^b   Goodarzi, Aaron A ^a   Riballo, Enriqueta ^a   Tape, Christopher ^a   Oliver, Antony W ^c   van Zelm, Menno C ^d   Buckland, Matthew S ^b   Davies, E Graham ^e   Pearl, Laurence H ^f   Jeggo, Penny A ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b ROYAL LONDON HOSPITAL   (United Kingdom)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^d ERASMUS MEDICAL CENTER   (Netherlands)

^e GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^f UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

DNA double strand break repair; Immunodeficiency; Radiosensitivity; V(D)J recombination

Indexed keywords

ARTEMIS PROTEIN; COMPLEMENTARY DNA; PROTEIN; UNCLASSIFIED DRUG;

ADULT; ALLELE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CASE REPORT; CELL CYCLE G2 PHASE; CHILD; DISEASE PREDISPOSITION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; FEMALE; FIBROBLAST; GENE MUTATION; GENETIC RECOMBINATION; HUMAN; HUMAN CELL; LYMPHOMA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RADIOSENSITIVITY; SEVERE COMBINED IMMUNODEFICIENCY;

ANIMALS; ARTEMISIA; BASE SEQUENCE; DNA PRIMERS; FLUORESCENT ANTIBODY TECHNIQUE; POLYMORPHISM, GENETIC; RADIATION TOLERANCE;

HUMAN HERPESVIRUS 4;

EID: 77955983966     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2010.07.001     Document Type: Article

References (39)

1. Gellert M. V(D)J recombination: RAG proteins, repair factors, and regulation. Annu. Rev. Biochem. 2002, 71:101-132.
2. McBlane J.F., van Gent D.C., Ramsden D.A., Romeo C., Cuomo C.A., Gellert M., Oettinger M.A. Cleavage at a V(D)J recombination signal requires only RAG1 and RAG2 proteins and occurs in two steps. Cell 1995, 83:387-395.
3. Jeggo P.A., Concannon P. Immune diversity and genomic stability: opposite goals but similar paths. J. Photochem. Photobiol. B 2001, 65:88-96.
4. Taccioli G.E., Rathbun G., Oltz E., Stamato T., Jeggo P.A., Alt F.W. Impairment of V(D)J recombination in double-strand break repair mutants. Science 1993, 260:207-210.
5. Wyman C., Kanaar R. DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 2006, 40:363-383.
6. Meek K., Douglas P., Cui X., Ding Q., Lees-Miller S.P. Trans autophosphorylation at DNA-dependent protein kinase's two major autophosphorylation site clusters facilitates end processing but not end joining. Mol. Cell. Biol. 2007, 27:3881-3890.
7. Block W.D., Yu Y., Merkle D., Gifford J.L., Ding Q., Meek K., Lees-Miller S.P. Autophosphorylation-dependent remodeling of the DNA-dependent protein kinase catalytic subunit regulates ligation of DNA ends. Nucleic Acids Res. 2004, 32:4351-4357.
8. Moshous D., Callebaut I., de Chasseval R., Corneo B., Cavazzana-Calvo M., Le Deist F., Tezcan I., Sanal O., Bertrand Y., Philippe N., Fischer A., de Villartay J.P. Artemis, a novel DNA double-strand break repair/V(D)J recombination protein, is mutated in human severe combined immune deficiency. Cell 2001, 105:177-186.
9. Riballo E., Kuhne M., Rief N., Doherty A., Smith G.C., Recio M.J., Reis C., Dahm K., Fricke A., Krempler A., Parker A.R., Jackson S.P., Gennery A., Jeggo P.A., Lobrich M. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol. Cell 2004, 16:715-724.
10. Goodarzi A.A., Noon A.T., Deckbar D., Ziv Y., Shiloh Y., Lobrich M., Jeggo P.A. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell 2008, 31:167-177.
11. Callebaut I., Moshous D., Mornon J.P., de Villartay J.P. Metallo-beta-lactamase fold within nucleic acids processing enzymes: the beta-CASP family. Nucleic Acids Res. 2002, 30:3592-3601.
12. Poinsignon C., Moshous D., Callebaut I., de Chasseval R., Villey I., de Villartay J.P. The metallo-beta-lactamase/beta-CASP domain of Artemis constitutes the catalytic core for V(D)J recombination. J. Exp. Med. 2004, 199:315-321.
13. Ma Y., Pannicke U., Schwarz K., Lieber M.R. 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.
14. Weterings E., Verkaik N.S., Keijzers G., Florea B.I., Wang S.Y., Ortega L.G., Uematsu N., Chen D.J., van Gent D.C. The Ku80 carboxy terminus stimulates joining and Artemis-mediated processing of DNA ends. Mol. Cell. Biol. 2009, 29:1134-1142.
15. Goodarzi A.A., Yu Y., Riballo E., Douglas P., Walker S.A., Ye R., Harer C., Marchetti C., Morrice N., Jeggo P.A., Lees-Miller S.P. DNA-PK autophosphorylation facilitates Artemis endonuclease activity. EMBO J. 2006, 25:3880-3889.
16. Soubeyrand S., Pope L., De Chasseval R., Gosselin D., Dong F., de Villartay J.P., Hache R.J. Artemis phosphorylated by DNA-dependent protein kinase associates preferentially with discrete regions of chromatin. J. Mol. Biol. 2006, 358:1200-1211.
17. Nicolas N., Moshous D., Cavazzana-Calvo M., Papadopoulo D., de Chasseval R., Le Deist F., Fischer A., de Villartay J.P. A human severe combined immunodeficiency (SCID) condition with increased sensitivity to ionizing radiations and impaired V(D)J rearrangements defines a new DNA recombination/repair deficiency. J. Exp. Med. 1998, 188:627-634.
18. O'Driscoll M., Cerosaletti K.M., Girard P.-M., Dai Y., Stumm M., Kysela B., Hirsch B., Gennery A., Palmer S.E., Seidel J., Gatti R.A., Varon R., Oettinger M.A., Sperling K., Jeggo P.A., Concannon P. DNA ligase IV mutations identified in patients exhibiting development delay and immunodeficiency. Mol. Cell 2001, 8:1175-1185.
19. O'Driscoll M., Jeggo P. Immunological disorders and DNA repair. Mutat. Res. 2002, 509:109-126.
20. O'Driscoll M., Jeggo P.A. The role of double-strand break repair - insights from human genetics. Nat. Rev. Genet. 2006, 7:45-54.
21. Buck D., Malivert L., de Chasseval R., Barraud A., Fondaneche M.C., Sanal O., Plebani A., Stephan J.L., Hufnagel M., le Deist F., Fischer A., Durandy A., de Villartay J.P., Revy P. Cernunnos, a novel nonhomologous end-joining factor, is mutated in human immunodeficiency with microcephaly. Cell 2006, 124:287-299.
22. van der Burg M., Ijspeert H., Verkaik N.S., Turul T., Wiegant W.W., Morotomi-Yano K., Mari P.O., Tezcan I., Chen D.J., Zdzienicka M.Z., van Dongen J.J., van Gent D.C. 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.
23. Riballo E., Doherty A.J., Dai Y., Stiff T., Oettinger M.A., Jeggo P.A., Kysela B. Cellular and biochemical impact of a mutation in DNA ligase IV conferring clinical radiosensitivity. J. Biol. Chem. 2001, 276:31124-31132.
24. van der Burg M., van Veelen L.R., Verkaik N.S., Wiegant W.W., Hartwig N.G., Barendregt B.H., Brugmans L., Raams A., Jaspers N.G., Zdzienicka M.Z., van Dongen J.J., van Gent D.C. A new type of radiosensitive T-B-NK+ severe combined immunodeficiency caused by a LIG4 mutation. J. Clin. Invest. 2006, 116:137-145.
25. Toita N., Hatano N., Ono S., Yamada M., Kobayashi R., Kobayashi I., Kawamura N., Okano M., Satoh A., Nakagawa A., Ohshima K., Shindoh M., Takami T., Kobayashi K., Ariga T. Epstein-Barr virus-associated B-cell lymphoma in a patient with DNA ligase IV (LIG4) syndrome. Am. J. Med. Genet. A 2007, 143:742-745.
26. Enders A., Fisch P., Schwarz K., Duffner U., Pannicke U., Nikolopoulos E., Peters A., Orlowska-Volk M., Schindler D., Friedrich W., Selle B., Niemeyer C., Ehl S. A severe form of human combined immunodeficiency due to mutations in DNA ligase IV. J. Immunol. 2006, 176:5060-5068.
27. Rooney S., Sekiguchi J., Zhu C., Cheng H.L., Manis J., Whitlow S., DeVido J., Foy D., Chaudhuri J., Lombard D., Alt F.W. Leaky Scid phenotype associated with defective V(D)J coding end processing in Artemis-deficient mice. Mol. Cell 2002, 10:1379-1390.
28. Moshous D., Pannetier C., Chasseval Rd R., Deist Fl F., Cavazzana-Calvo M., Romana S., Macintyre E., Canioni D., Brousse N., Fischer A., Casanova J.L., Villartay J.P. Partial T and B lymphocyte immunodeficiency and predisposition to lymphoma in patients with hypomorphic mutations in Artemis. J. Clin. Invest. 2003, 111:381-387.
29. Ege M., Ma Y., Manfras B., Kalwak K., Lu H., Lieber M.R., Schwarz K., Pannicke U. Omenn syndrome due to ARTEMIS mutations. Blood 2005, 105:4179-4186.
30. 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. 2006, 15:1303-1311.
31. van der Burg M., Verkaik N.S., den Dekker A.T., Barendregt B.H., Pico-Knijnenburg I., Tezcan I., vanDongen J.J., van Gent D.C. Defective Artemis nuclease is characterized by coding joints with microhomology in long palindromic-nucleotide stretches. Eur. J. Immunol. 2007, 37:3522-3528.
32. Kobayashi N., Agematsu K., Sugita K., Sako M., Nonoyama S., Yachie A., Kumaki S., Tsuchiya S., Ochs H.D., Fukushima Y., Komiyama A. Novel Artemis gene mutations of radiosensitive severe combined immunodeficiency in Japanese families. Hum. Genet. 2003, 112:348-352.
33. Darroudi F., Wiegant W., Meijers M., Friedl A.A., van der Burg M., Fomina J., van Dongen J.J., van Gent D.C., Zdzienicka M.Z. Role of Artemis in DSB repair and guarding chromosomal stability following exposure to ionizing radiation at different stages of cell cycle. Mutat. Res. 2007, 615:111-124.
34. Wang J., Pluth J.M., Cooper P.K., Cowan M.J., Chen D.J., Yannone S.M. Artemis deficiency confers a DNA double-strand break repair defect and Artemis phosphorylation status is altered by DNA damage and cell cycle progression. DNA Repair (Amst.) 2005, 4:556-570.
35. Beucher A., Birraux J., Tchouandong L., Barton O., Shibata A., Conrad S., Goodarzi A.A., Krempler A., Jeggo P.A., Lobrich M. ATM and Artemis promote homologous recombination of radiation-induced DNA double-strand breaks in G2. EMBO J. 2009, 28:3413-3427.
36. Li L., Moshous D., Zhou Y., Wang J., Xie G., Salido E., Hu D., de Villartay J.P., Cowan M.J. A founder mutation in Artemis, an SNM1-like protein, causes SCID in Athabascan-speaking Native Americans. J. Immunol. 2002, 168:6323-6329.
37. Girard P.-M., Kysela B., Harer C.J., Doherty A.J., Jeggo P.A. Analysis of DNA ligase IV mutations found in LIG4 syndrome patients: the impact of two linked polymorphisms. Hum. Mol. Genet. 2004, 13:2369-2376.
38. Pannicke U., Ma Y., Hopfner K.P., Niewolik D., Lieber M.R., Schwarz K. Functional and biochemical dissection of the structure-specific nuclease ARTEMIS. EMBO J. 2004, 23:1987-1997.
39. Kelley L.A., Sternberg M.J. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 2009, 4:363-371.