ATM kinase activity modulates Fas sensitivity through the regulation of FLIP in lymphoid cells

Blood

Volumn 111, Issue 2, 2008, Pages 829-837

  Stagni, Venturina ^a,b   Di Bari, Maria Giovanna ^a,b   Cursi, Silvia ^a,b   Condò, Ivano ^a   Cencioni, Maria Teresa ^b   Testi, Roberto ^a   Lerenthal, Yaniv ^c   Cundari, Enrico ^d   Barilà, Daniela ^a,b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c TEL AVIV UNIVERSITY   (Israel)

^d Istituto Di Biologia E Patologia Molecolari Rome   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; CASPASE 8; FAS ANTIGEN; FLICE INHIBITORY PROTEIN;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INACTIVATION; HODGKIN DISEASE; HUMAN; HUMAN CELL; IMMUNOREGULATION; LYMPHOID CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; T LYMPHOCYTE; UPREGULATION;

EID: 38349087547     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2007-04-085399     Document Type: Article

References (51)

1. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature. 2003;421:499-506.
2. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer. 2003;3:155-167.
3. Khanna KK, Jackson SP. DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet. 2001;27:247-254.
4. Gumy-Pause F, Wacker P, Sappino AP. ATM gene and lymphoid malignancies. Leukemia. 2004;18:238-242.
5. Taylor AM, Metcalfe JA, Thick J, Mak YF. Leukemia and lymphoma in ataxia telangiectasia. Blood. 1996;87:423-438.
6. Matei IR, Guidos CJ, Danska JS. ATM-dependent DNA damage surveillance in T-cell development and leukemogenesis: the DSB connection. Immunol Rev. 2006;209:142-158.
7. Starczynski J, Simmons W, Flavell JR, et al. Variations in ATM protein expression during normal lymphoid differentiation and among B-cell-derived neoplasias. Am J Pathol. 2003;163:423-432.
8. Greiner TC, Dasgupta C, Ho VV, et al. Mutation and genomic deletion status of ataxia telangiectasia mutated (ATM) and p53 confer specific gene expression profiles in mantle cell lymphoma. Proc Natl Acad Sci U S A. 2006;103:2352-2357.
9. Takagi M, Tsuchida R, Oguchi K, et al. Identification and characterization of polymorphic variations of the ataxia telangiectasia mutated (ATM) gene in childhood Hodgkin disease. Blood. 2004;103:283-290.
10. Oguchi K, Takagi M, Tsuchida R, et al. Missense mutation and defective function of ATM in a childhood acute leukemia patient with MLL gene rearrangement. Blood. 2003;101:3622-3627.
11. Wallach D, Varfolomeev EE, Malinin NL, Goltsev YV, Kovalenko AV, Boldin MP. Tumor necrosis factor receptor and Fas signaling mechanisms. Annu Rev Immunol. 1999;17:331-367.
12. Juo P, Kuo CJ, Yuan J, Blenis J. Essential requirement for caspase-8/FLICE in the initiation of the Fas-induced apoptotic cascade. Curr Biol. 1998;8:1001-1008.
13. Peter ME. The flip side of FLIP. Biochem J. 2004;382:e1-e3.
14. Chang DW, Xing Z, Pan Y, et al. c-FLIP(L) is a dual function regulator for caspase-8 activation and CD95-mediated apoptosis. EMBO J. 2002;21:3704-3714.
15. Krammer PH. CD95's deadly mission in the immune system. Nature. 2000;407:789-795.
16. Takahashi Y, Ohta H, Takemori T. Fas is required for clonal selection in germinal centers and the subsequent establishment of the memory B cell repertoire. Immunity. 2001;14:181-192.
17. Siegel RM, Chan FK, Chun HJ, Lenardo MJ. The multifaceted role of Fas signaling in immune cell homeostasis and autoimmunity. Nat Immunol. 2000;1:469-474.
18. Defrance T, Casamayor-Palleja M, Krammer PH. The life and death of a B cell. Adv Cancer Res. 2002;86:195-225.
19. Adachi M, Suematsu S, Kondo T, et al. Targeted mutation in the Fas gene causes hyperplasia in peripheral lymphoid organs and liver. Nat Genet. 1995;11:294-300.
20. Davidson WF, Giese T, Fredrickson TN. Spontaneous development of plasmacytoid tumors in mice with defective Fas-Fas ligand interactions. J Exp Med. 1998;187:1825-1838.
21. Fleisher TA, Puck JM, Strober W, et al. The autoimmune lymphoproliferative syndrome: a disorder of human lymphocyte apoptosis. Clin Rev Allergy Immunol. 2001;20:109-120.
22. Straus SE, Jaffe ES, Puck JM, et al. The development of lymphomas in families with autoimmune lymphoproliferative syndrome with germline Fas mutations and defective lymphocyte apoptosis. Blood. 2001;98:194-200.
23. Muschen M, Rajewsky K, Kronke M, Kuppers R. The origin of CD95-gene mutations in B-cell lymphoma. Trends Immunol. 2002;23:75-80.
24. Kuppers R, Schwering I, Brauninger A, Rajewsky K, Hansmann ML. Biology of Hodgkin's lymphoma. Ann Oncol. 2002;13(suppl 1):11-18.
25. Re D, Hofmann A, Wolf J, Diehl V, Staratschek-Jox A. Cultivated H-RS cells are resistant to CD95L-mediated apoptosis despite expression of wild-type CD95. Exp Hematol. 2000;28:348.
26. Dutton A, O'Neil JD, Milner AE, et al. Expression of the cellular FLICE-inhibitory protein (c-FLIP) protects Hodgkin's lymphoma cells from autonomous Fas-mediated death. Proc Natl Acad Sci U S A. 2004;101:6611-6616.
27. Mathas S, Lietz A, Anagnostopoulos I, Hummel F, et al. c-FLIP mediates resistance of Hodgkin/Reed-Sternberg cells to death receptor-induced apoptosis. J Exp Med. 2004;199:1041-1052.
28. Lespinet V, Terraz F, Recher C, et al. Single-cell analysis of loss of heterozygosity at the ATM gene locus in Hodgkin and Reed-Sternberg cells of Hodgkin's lymphoma: ATM loss of heterozygosity is a rare event. Int J Cancer. 2005;114:909-916.
29. Dutton A, Woodman CB, Chukwuma MB, et al. BMI-1 is induced by the Epstein-Barr virus oncogene LMP1, and regulates the expression of viral target genes in Hodgkin's lymphoma cells. Blood. 2007;109:2597-603.
30. Ganten TM, Haas TL, Sykora J, et al. Enhanced caspase-8 recruitment to and activation at the DISC is critical for sensitisation of human hepatocellular carcinoma cells to TRAIL-induced apoptosis by chemotherapeutic drugs. Cell Death Differ. 2004;11(suppl 1):S86-S96.
31. Perez OD, Krutzik PO, Nolan GP. Flow cytometric analysis of kinase signaling cascades. Methods Mol Biol. 2004;263:67-94.
32. Tritarelli A, Oricchio E, Ciciarello M, et al. p53 localization at centrosomes during mitosis and postmitotic checkpoint are ATM-dependent and require serine 15 phosphorylation. Mol Biol Cell. 2004;15:3751-3757.
33. Barilà D, Rufini A, Condo I, et al. Caspase-dependent cleavage of c-Abl contributes to apoptosis. Mol Cell Biol. 2003;23:2790-2799.
34. Salon C, Eymin B, Micheau O, et al. E2F1 induced apoptosis and sensitizes human lung adenocarcinoma cells to death-receptor-mediated apoptosis through specific downregulation of c-FLIP short. Cell Death Differ. 2006;13:260-272.
35. Gilad S, Bar-Shira A, Harnik R, Shkedy D, et al. Ataxia-telangiectasia: founder effect among north African Jews. Hum Mol Genet. 1996;5:2033-2037.
36. Lavin MF, Davidson M. Repair of strand breaks in superhelical DNA of ataxia telangiectasia lymphoblastoid cells. J Cell Sci. 1981;48:383-391.
37. Ahn JY, Schwarz JK, Piwnica-Worms H, Canman CE. Threonine 68 phosphorylation by ataxia telangiectasia mutated is required for efficient activation of Chk2 in response to ionizing radiation. Cancer Res. 2000;60:5934-5936.
38. Khanna KK, Keating KE, Kozlov S, et al. ATM associates with and phosphorylates p53: mapping the region of interaction. Nat Genet. 1998;20:398-400.
39. Matsuoka S, Rotman G, Ogawa A, Shiloh Y, Tamai K, Elledge SJ. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc Natl Acad Sci U S A. 2000;97:10389-10394.
40. Burma S, Chen BP, Murphy M, Kurimasa A, Chen DJ. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem. 2001;276:42462-42467.
41. Wang H, Wang M, Bocker W, Iliakis G. Complex H2AX phosphorylation patterns by multiple kinases including ATM and DNA-PK in human cells exposed to ionizing radiation and treated with kinase inhibitors. J Cell Physiol. 2005;202:492-502.
42. Uziel T, Lerenthal Y, Moyal L, Andegeko Y, Mittelman L, Shiloh Y. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 2003;22:5612-5621.
43. Smith GCM, D'Adda di Fagagna F, Lakin ND, Jackson SP. Cleavage and inactivation of ATM during apoptosis. Mol Cell Biol. 1999;19:6076-6084.
44. Hickson I, Zhao Y, Richardson CJ, et al. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 2004;64:9152-9159.
45. Thome M, Tschopp J. Regulation of lymphocyte proliferation and death by FLIP. Nat Rev Immunol. 2001;1:50-58.
46. Banin S, Shieh SY, Taya Y, et al. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science. 1998;281:1674-1677.
47. Kozlov S, Gueven N, Keating K, Ramsay J, Lavin MF. ATP activates ataxia-telangiectasia mutated (ATM) in vitro: importance of autophosphorylation. J Biol Chem. 2003;278:9309-9317.
48. Kreuz S, Siegmund D, Scheurich P, Wajant H. NF-kappaB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling. Mol Cell Biol. 2001;21:3964-3973.
49. Hinz M, Lemke P, Anagnostopoulos I, et al. Nuclear factor kappaB-dependent gene expression profiling of Hodgkin's disease tumor cells, pathogenetic significance, and link to constitutive signal transducer and activator of transcription 5a activity. J Exp Med. 2002;196:605-617.
50. Mathas S, Hinz M, Anagnostopoulos I, et al. Aberrantly expressed c-Jun and JunB are a hallmark of Hodgkin lymphoma cells, stimulate proliferation and synergize with NF-kappa B. EMBO J. 2002;21:4104-4113.
51. Hinz M, Loser P, Mathas S, Krappmann D, Dorken B, Scheidereit C. Constitutive NF-kappaB maintains high expression of a characteristic gene network, including CD40, CD86, and a set of antiapoptotic genes in Hodgkin/Reed-Sternberg cells. Blood. 2001;97:2798-2807.