Reduced CaM/FLIP binding by a single point mutation in c-FLIPL modulates Fas-mediated apoptosis and decreases tumorigenesis

Laboratory Investigation

Volumn 92, Issue 1, 2012, Pages 82-90

  Jing, Gu ^a   Yuan, Kaiyu ^a   Liang, Qiuli ^a   Sun, Yong ^a   Mao, Xia ^a   McDonald, Jay M ^a,b   Chen, Yabing ^a,b  

^a University of Alabama at Birmingham   (United States)

^b BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

apoptosis; calmodulin; cholangiocarcinoma; death inducing signaling complex (DISC); FLICE like inhibitory protein (FLIP); point mutation; tumorigenesis

Indexed keywords

AMINO ACID; CALMODULIN; CASPASE 3; CASPASE 8; FAS ANTIGEN; FLICE INHIBITORY PROTEIN;

APOPTOSIS; ARTICLE; BILE DUCT CARCINOMA; CARCINOGENESIS; HUMAN; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; TUMOR GROWTH;

EID: 84855251212     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2011.131     Document Type: Article

References (46)

1. Cohen GM. Caspases: the executioners of apoptosis. Biochem J 1997;326:1-16. (Pubitemid 27386911)
2. Pawar P, Ma L, Byon CH, et al. Molecular mechanisms of tamoxifen therapy for cholangiocarcinoma: role of calmodulin. Clin Cancer Res 2009;15:1288-1296.
3. Pan G, Vickers SM, Pickens A, et al. Apoptosis and tumorigenesis in human cholangiocarcinoma cells. Involvement of Fas/APO-1 (CD95) and calmodulin. Am J Pathol 1999;155:193-203. (Pubitemid 29318717)
4. Chen Y, Xu J, Jhala N, et al. Fas-mediated apoptosis in cholangiocarcinoma cells is enhanced by 3,30-diindolylmethane through inhibition of AKT signaling and FLICE-like inhibitory protein. Am J Pathol 2006;169:1833-1842. (Pubitemid 351182012)
5. Ahn EY, Pan G, Oh JH, et al. The combination of calmodulin antagonists and interferon-g induces apoptosis through caspasedependent and -independent pathways in cholangiocarcinoma cells. Am J Pathol 2003;163:2053-2063. (Pubitemid 37310035)
6. Vickers SM, Jhala NC, Ahn EY, et al. Tamoxifen (TMX)/Fas induced growth inhibition of human cholangiocarcinoma (HCC) by g interferon (IFN-g). Ann Surg 2002;235:872-878. (Pubitemid 34547307)
7. Ahn EY, Pan G, Vickers SM, et al. IFN-gamma upregulates apoptosisrelated molecules and enhances Fas-mediated apoptosis in human cholangiocarcinoma. Int J Cancer 2002;100:445-451.
8. Que FG, Phan VA, Phan VH, et al. Cholangiocarcinomas express Fas ligand and disable the Fas receptor. Hepatology 1999;30:1398-1404.
9. Jing G, Yuan K, Turk AN, et al. Tamoxifen enhances therapeutic effects of gemcitabine on cholangiocarcinoma tumorigenesis. Lab Invest 2011;91:896-904.
10. Chaigne-Delalande B, Moreau JF, Legembre P. Rewinding the DISC. Arch Immunol Ther Exp (Warsz) 2008;56:9-14.
11. Baumler C, Duan F, Onel K, et al. Differential recruitment of caspase 8 to cFlip confers sensitivity or resistance to Fas-mediated apoptosis in a subset of familial lymphoma patients. Leuk Res 2003;27: 841-851. (Pubitemid 36683332)
12. Irmler M, Thome M, Hahne M, et al. Inhibition of death receptor signals by cellular FLIP. Nature 1997;388:190-195. (Pubitemid 27297457)
13. Thome M, Schneider P, Hofmann K, et al. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 1997;386:517-521. (Pubitemid 27164081)
14. Shu HB, Halpin DR, Goeddel DV. Casper is a FADD- and caspase-related inducer of apoptosis. Immunity 1997;6:751-763. (Pubitemid 27305737)
15. Peter ME, Krammer PH. The CD95(APO-1/Fas) DISC and beyond. Cell Death Differ 2003;10:26-35. (Pubitemid 36511830)
16. 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. (Pubitemid 34787044)
17. Scaffidi C, Schmitz I, Krammer PH, et al. The role of c-FLIP in modulation of CD95-induced apoptosis. J Biol Chem 1999;274: 1541-1548.
18. Dohrman A, Russell JQ, Cuenin S, et al. Cellular FLIP long form augments caspase activity and death of T cells through heterodimerization with and activation of caspase-8. J Immunol 2005;175: 311-318. (Pubitemid 40884333)
19. Thome M, Tschopp J. Regulation of lymphocyte proliferation and death by FLIP. Nat Rev Immunol 2001;1:50-58. (Pubitemid 33741975)
20. Babu YS, Sack JS, Greenhough TJ, et al. Three-dimensional structure of calmodulin. Nature 1985;315:37-40. (Pubitemid 15064895)
21. Dowd DR, MacDonald PN, Komm BS, et al. Evidence for early induction of calmodulin gene expression in lymphocytes undergoing glucocorticoidmediated apoptosis. J Biol Chem 1991;266:18423-18426. (Pubitemid 21908098)
22. Gerner C, Frohwein U, Gotzmann J, et al. The Fas-induced apoptosis analyzed by high throughput proteome analysis. J Biol Chem 2000;275:39018-39026. (Pubitemid 32058914)
23. Yuan K, Jing G, Chen J, et al. Calmodulin mediates FAS-induced FADDindependent survival signaling in pancreatic cancer cells via activation of Src-ERK. J Biol Chem 2011;286:24776-24784.
24. Ahn EY, Lim ST, Cook WJ, et al. Calmodulin binding to the Fas death domain. Regulation by Fas activation. J Biol Chem 2004;279: 5661-5666. (Pubitemid 38220594)
25. Pawar PS, Micoli KJ, Ding H, et al. Calmodulin binding to cellular FLICE-like inhibitory protein modulates Fas-induced signaling. Biochem J 2008;412:459-468. (Pubitemid 351846411)
26. Knuth A, Gabbert H, Dippold W, et al. Biliary adenocarcinoma. Characterisation of three new human tumor cell lines. J Hepatol 1985;1:579-596. (Pubitemid 15015131)
27. Ustundag Y, Bronk SF, Gores GJ. Proteasome inhibition-induces endoplasmic reticulum dysfunction and cell death of human cholangiocarcinoma cells. World J Gastroenterol 2007;13:851-857. (Pubitemid 46470294)
28. Sacks DB, Porter SE, Ladenson JH, et al. Monoclonal antibody to calmodulin: development, characterization, and comparison with polyclonal anti-calmodulin antibodies. Anal Biochem 1991;194:369-377.
29. Byon CH, Javed A, Dai Q, et al. Oxidative stress induces vascular calcification through modulation of the osteogenic transcription factor Runx2 by AKT signalling. J Biol Chem 2008;283:15319-15327.
30. Chen J, Sun Y, Mao X, et al. RANKL up-regulates brain-type creatine kinase via poly(ADP-ribose) polymerase-1 during osteoclastogenesis. J Biol Chem 2010;285:36315-36321.
31. Wu X, Wakefield JK, Liu H, et al. Development of a novel trans-lentiviral vector that affords predictable safety. Mol Ther 2000;2:47-55.
32. Chen Y, Pawar P, Pan G, et al. Calmodulin binding to the Fas-mediated death-inducing signaling complex in cholangiocarcinoma cells. J Cell Biochem 2008;103:788-799. (Pubitemid 351240615)
33. Beneteau M, Daburon S, Moreau JF, et al. Dominant-negative Fas mutation is reversed by down-expression of c-FLIP. Cancer Res 2007;67:108-115. (Pubitemid 46142765)
34. Legembre P, Barnhart BC, Peter ME. The relevance of NF-kappaB for CD95 signaling in tumor cells. Cell Cycle 2004;3:1235-1239. (Pubitemid 40268600)
35. Rhoads AR, Friedberg F. Sequence motifs for calmodulin recognition. FASEB J 1997;11:331-340. (Pubitemid 27193937)
36. O'Day DH. CaMBOT: profiling and characterizing calmodulin-binding proteins. Cell Signalling 2003;15:347-354. (Pubitemid 36254907)
37. Irmler M, Thome M, Hahne M, et al. Inhibition of death receptor signals by cellular FLIP. Nature 1997;388:190-195. (Pubitemid 27297457)
38. Golks A, Brenner D, Fritsch C, et al. c-FLIPR, a new regulator of death receptor-induced apoptosis. J Biol Chem 2005;280: 14507-14513. (Pubitemid 40562792)
39. Kischkel FC, Hellbardt S, Behrmann I, et al. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a deathinducing signaling complex (DISC) with the receptor. EMBO J 1995;14:5579-5588.
40. Salvesen GS, Dixit VM. Caspase activation: The induced-proximity model. Proc Natl Acad Sci USA 1999;96:10964-10967. (Pubitemid 29487313)
41. Legembre P, Barnhart BC, Zheng L, et al. Induction of apoptosis and activation of NF-kappaB by CD95 require different signaling thresholds. EMBO Rep 2004;5:1084-1089. (Pubitemid 39600208)
42. Desbarats J, Newell MK. Fas engagement accelerates liver regeneration after partial hepatectomy. Nat Med 2000;6:920-923. (Pubitemid 30644752)
43. Hu WH, Johnson H, Shu HB. Activation of NF-kappaB by FADD, Casper, and caspase-8. J Biol Chem 2000;275:10838-10844. (Pubitemid 30212715)
44. Chaudhary PM, Jasmin A, Eby MT, et al. Modulation of the NFkappa B pathway by virally encoded death effector domains-containing proteins. Oncogene 1999;18:5738-5746. (Pubitemid 29507427)
45. Kataoka T, Budd RC, Holler N, et al. The caspase-8 inhibitor FLIP promotes activation of NF-kappaB and Erk signaling pathways. Curr Biol 2000;10:640-648. (Pubitemid 30354699)
46. Tran SE, Holmstrom TH, Ahonen M, et al. MAPK/ERK overrides the apoptotic signaling from Fas, TNF, and TRAIL receptors. J Biol Chem 2001;276:16484-16490.