DICE: A novel tumor surveillance mechanism - A new therapy for cancer?

Cell Cycle

Volumn 13, Issue 9, 2014, Pages 1373-1378

  Peter, Marcus E ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Cancer; Cell death; Fas; Immune system; Surveillance

Indexed keywords

CASPASE 2; DEATH RECEPTOR; FAS LIGAND; GAMMA INTERFERON; GRANZYME; GROWTH PROMOTOR; FAS ANTIGEN;

ANTIGEN FUNCTION; APOPTOSIS; CANCER CELL; CANCER REGRESSION; CANCER THERAPY; CD8+ T LYMPHOCYTE; CELL DEATH; CELL PROLIFERATION; CELL VIABILITY; HUMAN; IMMUNOCOMPETENT CELL; NONHUMAN; PHYSIOLOGY; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; FAS LIGAND PROTEIN; HUMANS; NEOPLASMS; SIGNAL TRANSDUCTION;

EID: 84899766549     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.28673     Document Type: Review

References (69)

1. Peter ME, Krammer PH. The CD95(APO-1/Fas) DISC and beyond. Cell Death Differ 2003; 10:26-35; PMID:12655293; http://dx.doi.org/10.1038/sj.cdd.4401186
2. Nagata S. Fas ligand-induced apoptosis. Annu Rev Genet 1999; 33:29-55; PMID:10690403; http://dx.doi.org/10.1146/annurev.genet.33.1.29
3. Peter ME, Barnhart BC, Algeciras-Schimnich A. The Cytokine Handbook: CD95L/FasL and its receptor CD95 (APO-1/Fas). The Cytokine Handbook 2003; 2:885-911; http://dx.doi.org/10.1016/B978-012689663-3/50042-9
4. Rieux-Laucat F, Blachère S, Danielan S, De Villartay JP, Oleastro M, Solary E, Bader-Meunier B, Arkwright P, Pondaré C, Bernaudin F, et al. Lymphoproliferative syndrome with autoimmunity: A possible genetic basis for dominant expression of the clinical manifestations. Blood 1999; 94:2575-82; PMID:10515860
5. Drappa J, Vaishnaw AK, Sullivan KE, Chu JL, Elkon KB. Fas gene mutations in the Canale-Smith syndrome, an inherited lymphoproliferative disorder associated with autoimmunity. N Engl J Med 1996; 335:1643-9; PMID:8929361; http://dx.doi.org/10.1056/NEJM199611283352204
6. Martin DA, Zheng L, Siegel RM, Huang B, Fisher GH, Wang J, Jackson CE, Puck JM, Dale J, Straus SE, et al. Defective CD95/APO-1/Fas signal complex formation in the human autoimmune lymphoproliferative syndrome, type Ia. Proc Natl Acad Sci U S A 1999; 96:4552-7; PMID:10200300; http://dx.doi.org/10.1073/ pnas.96.8.4552
7. Rieux-Laucat F, Le Deist F, Hivroz C, Roberts IA, Debatin KM, Fischer A, de Villartay JP. Mutations in Fas associated with human lymphoproliferative syndrome and autoimmunity. Science 1995; 268:1347-9; PMID:7539157; http://dx.doi.org/10.1126/science.7539157
8. Straus SE, Jaffe ES, Puck JM, Dale JK, Elkon KB, Rösen-Wolff A, Peters AM, Sneller MC, Hallahan CW, Wang J, 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; PMID:11418480; http://dx.doi.org/10.1182/blood.V98.1.194
9. Berke G. Killing mechanisms of cytotoxic lymphocytes. Curr Opin Hematol 1997; 4:32-40; PMID:9050377; http://dx.doi.org/10.1097/00062752-199704010-00006
10. Algeciras-Schimnich A, Pietras EM, Barnhart BC, Legembre P, Vijayan S, Holbeck SL, Peter ME. Two CD95 tumor classes with different sensitivities to antitumor drugs. Proc Natl Acad Sci U S A 2003; 100:11445-50; PMID:14504390; http://dx.doi.org/10.1073/pnas.2034995100
11. Peter ME, Budd RC, Desbarats J, Hedrick SM, Hueber AO, Newell MK, Owen LB, Pope RM, Tschopp J, Wajant H, et al. The CD95 receptor: apoptosis revisited. Cell 2007; 129:447-50; PMID:17482535; http://dx.doi.org/10.1016/j.cell.2007.04. 031
12. Wajant H, Pfizenmaier K, Scheurich P. Nonapoptotic Fas signaling. Cytokine Growth Factor Rev 2003; 14:53-66; PMID:12485619; http://dx.doi.org/10. 1016/S1359-6101(02)00072-2
13. Martin-Villalba A, Llorens-Bobadilla E, Wollny D. CD95 in cancer: tool or target? Trends Mol Med 2013; 19:329-35; PMID:23540716; http://dx.doi.org/10. 1016/j.molmed.2013.03.002
14. Chen L, Park SM, Tumanov AV, Hau A, Sawada K, Feig C, Turner JR, Fu YX, Romero IL, Lengyel E, et al. CD95 promotes tumour growth. Nature 2010; 465:492-6; PMID:20505730; http://dx.doi.org/10.1038/nature09075
15. Desbarats J, Newell MK. Fas engagement accelerates liver regeneration after partial hepatectomy. Nat Med 2000; 6:920-3; PMID:10932231; http://dx.doi.org/10.1038/78688
16. Desbarats J, Birge RB, Mimouni-Rongy M, Weinstein DE, Palerme JS, Newell MK. Fas engagement induces neurite growth through ERK activation and p35 upregulation. Nat Cell Biol 2003; 5:118-25; PMID:12545171; http://dx.doi.org/10. 1038/ncb916
17. Zuliani C, Kleber S, Klussmann S, Wenger T, Kenzelmann M, Schreglmann N, Martinez A, del Rio JA, Soriano E, Vodrazka P, et al. Control of neuronal branching by the death receptor CD95 (Fas/Apo-1). Cell Death Differ 2006; 13:31-40; PMID:16003386; http://dx.doi.org/10.1038/sj.cdd.4401720
18. Corsini NS, Sancho-Martinez I, Laudenklos S, Glagow D, Kumar S, Letellier E, Koch P, Teodorczyk M, Kleber S, Klussmann S, et al. The death receptor CD95 activates adult neural stem cells for working memory formation and brain repair. Cell Stem Cell 2009; 5:178-90; PMID:19664992; http://dx.doi.org/10.1016/j.stem. 2009.05.004
19. Lee JK, Sayers TJ, Back TC, Wigginton JM, Wiltrout RH. Lack of FasL-mediated killing leads to in vivo tumor promotion in mouse Lewis lung cancer. Apoptosis 2003; 8:151-60; PMID:12766475; http://dx.doi.org/10.1023/A: 1022918625509
20. Zhang Y, Liu Q, Zhang M, Yu Y, Liu X, Cao X. Fas signal promotes lung cancer growth by recruiting myeloid-derived suppressor cells via cancer cell-derived PGE2. J Immunol 2009; 182:3801-8; PMID:19265159; http://dx.doi.org/10.4049/jimmunol.0801548
21. Hoogwater FJ, Nijkamp MW, Smakman N, Steller EJ, Emmink BL, Westendorp BF, Raats DA, Sprick MR, Schaefer U, Van Houdt WJ, et al. Oncogenic K-Ras turns death receptors into metastasis-promoting receptors in human and mouse colorectal cancer cells. Gastroenterology 2010; 138:2357-67; PMID:20188103; http://dx.doi.org/10.1053/j.gastro.2010.02.046
22. Nijkamp MW, Hoogwater FJ, Steller EJ, Westendorp BF, van der Meulen TA, Leenders MW, Borel Rinkes IH, Kranenburg O. CD95 is a key mediator of invasion and accelerated outgrowth of mouse colorectal liver metastases following radiofrequency ablation. J Hepatol 2010; 53:1069-77; PMID:20832890; http://dx.doi.org/10.1016/j.jhep.2010.04.040
23. Park SM, Chen L, Zhang M, Ashton-Rickardt P, Turner JR, Peter ME. CD95 is cytoprotective for intestinal epithelial cells in colitis. Inflamm Bowel Dis 2010; 16:1063-70; PMID:20049944; http://dx.doi.org/10.1002/ibd.21195
24. Li H, Fan X, Stoicov C, Liu JH, Zubair S, Tsai E, Ste Marie R, Wang TC, Lyle S, Kurt-Jones E, et al. Human and mouse colon cancer utilizes CD95 signaling for local growth and metastatic spread to liver. Gastroenterology 2009; 137:934-44, e1-4; PMID:19524576; http://dx.doi.org/10.1053/j.gastro.2009. 06.004
25. Zheng H, Li W, Wang Y, Liu Z, Cai Y, Xie T, Shi M, Wang Z, Jiang B. Glycogen synthase kinase-3 beta regulates Snail and β-catenin expression during Fas-induced epithelial-mesenchymal transition in gastrointestinal cancer. Eur J Cancer 2013; 49:2734-46; PMID:23582741; http://dx.doi.org/10.1016/j.ejca. 2013.03.014
26. Zheng HX, Cai YD, Wang YD, Cui XB, Xie TT, Li WJ, Peng L, Zhang Y, Wang ZQ, Wang J, et al. Fas signaling promotes motility and metastasis through epithelial-mesenchymal transition in gastrointestinal cancer. Oncogene 2013; 32:1183-92; PMID:22508480; http://dx.doi.org/10.1038/onc.2012.126
27. Yuan K, Jing G, Chen J, Liu H, Zhang K, Li Y, Wu H, McDonald JM, Chen Y. Calmodulin mediates Fas-induced FADD-independent survival signaling in pancreatic cancer cells via activation of Srcextracellular signal-regulated kinase (ERK). J Biol Chem 2011; 286:24776-84; PMID:21613217; http://dx.doi.org/10.1074/jbc.M110.202804
28. Trauzold A, Röder C, Sipos B, Karsten K, Arlt A, Jiang P, Martin-Subero JI, Siegmund D, Müerköster S, Pagerols-Raluy L, et al. CD95 and TRAF2 promote invasiveness of pancreatic cancer cells. FASEB J 2005; 19:620-2; PMID:15670977
29. Kleber S, Sancho-Martinez I, Wiestler B, Beisel A, Gieffers C, Hill O, Thiemann M, Mueller W, Sykora J, Kuhn A, et al. Yes and PI3K bind CD95 to signal invasion of glioblastoma. Cancer Cell 2008; 13:235-48; PMID:18328427; http://dx.doi.org/10.1016/j.ccr.2008.02.003
30. Barnhart BC, Legembre P, Pietras E, Bubici C, Franzoso G, Peter ME. CD95 ligand induces motility and invasiveness of apoptosis-resistant tumor cells. EMBO J 2004; 23:3175-85; PMID:15272306; http://dx.doi.org/10.1038/sj.emboj. 7600325
31. Hadji A, Ceppi P, Murmann AE, Brockway S, Pattanayak A, Bhinder B, Hau A, De Chant S, Parimi V, Kolesza P, et al. Death induced by CD95 or CD95 ligand elimination. Cell Rep 2014; In press; PMID:24656822; http://dx.doi.org/10.1016/ j.celrep.2014.02.035.
32. Strasser A, Jost PJ, Nagata S. The many roles of FAS receptor signaling in the immune system. Immunity 2009; 30:180-92; PMID:19239902; http://dx.doi.org/10.1016/j.immuni.2009.01.001
33. Shrestha B, Diamond MS. Fas ligand interactions contribute to CD8+ T-cell-mediated control of West Nile virus infection in the central nervous system. J Virol 2007; 81:11749-57; PMID:17804505; http://dx.doi.org/10.1128/JVI. 01136-07
34. Tirosh R, Berke G. T-Lymphocyte-mediated cytolysis as an excitatory process of the target. I. Evidence that the target cell may be the site of Ca2+ action. Cell Immunol 1985; 95:113-23; PMID:3928177; http://dx.doi.org/10.1016/ 0008-8749(85)90300-4
35. Kägi D, Ledermann B, Bürki K, Seiler P, Odermatt B, Olsen KJ, Podack ER, Zinkernagel RM, Hengartner H. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 1994; 369:31-7; PMID:8164737; http://dx.doi.org/10.1038/369031a0
36. MacLennan IC, Gotch FM, Golstein P. Limited specific T-cell mediated cytolysis in the absence of extracellular Ca2+. Immunology 1980; 39:109-17; PMID:6769782
37. Rouvier E, Luciani MF, Golstein P. Fas involvement in Ca(2+)-independent T cell-mediated cytotoxicity. J Exp Med 1993; 177:195-200; PMID:7678113; http://dx.doi.org/10.1084/jem.177.1.195
38. Lowin B, Hahne M, Mattmann C, Tschopp J. Cytolytic T-cell cytotoxicity is mediated through perforin and Fas lytic pathways. Nature 1994; 370:650-2; PMID:7520535; http://dx.doi.org/10.1038/370650a0
39. Kägi D, Vignaux F, Ledermann B, Bürki K, Depraetere V, Nagata S, Hengartner H, Golstein P. Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science 1994; 265:528-30; PMID:7518614; http://dx.doi.org/10.1126/science.7518614
40. Kojima H, Shinohara N, Hanaoka S, Someya-Shirota Y, Takagaki Y, Ohno H, Saito T, Katayama T, Yagita H, Okumura K, et al. Two distinct pathways of specific killing revealed by perforin mutant cytotoxic T lymphocytes. Immunity 1994; 1:357-64; PMID:7533644; http://dx.doi.org/10.1016/1074-7613(94)90066-3
41. Seki N, Brooks AD, Carter CR, Back TC, Parsoneault EM, Smyth MJ, Wiltrout RH, Sayers TJ. Tumor-specific CTL kill murine renal cancer cells using both perforin and Fas ligand-mediated lysis in vitro, but cause tumor regression in vivo in the absence of perforin. J Immunol 2002; 168:3484-92; PMID:11907109
42. Shimizu M, Takeda Y, Yagita H, Yoshimoto T, Matsuzawa A. Antitumor activity exhibited by Fas ligand (CD95L) overexpressed on lymphoid cells against Fas+ tumor cells. Cancer Immunol Immunother 1998; 47:143-8; PMID:9829839; http://dx.doi.org/10.1007/s002620050514
43. Caldwell SA, Ryan MH, McDuffie E, Abrams SI. The Fas/Fas ligand pathway is important for optimal tumor regression in a mouse model of CTL adoptive immunotherapy of experimental CMS4 lung metastases. J Immunol 2003; 171:2402-12; PMID:12928387
44. Dobrzanski MJ, Reome JB, Hollenbaugh JA, Hylind JC, Dutton RW. Effector cell-derived lymphotoxin alpha and Fas ligand, but not perforin, promote Tc1 and Tc2 effector cell-mediated tumor therapy in established pulmonary metastases. Cancer Res 2004; 64:406-14; PMID:14729652; http://dx.doi.org/10.1158/0008-5472. CAN-03-2580
45. Chakraborty M, Abrams SI, Camphausen K, Liu K, Scott T, Coleman CN, Hodge JW. Irradiation of tumor cells up-regulates Fas and enhances CTL lytic activity and CTL adoptive immunotherapy. J Immunol 2003; 170:6338-47; PMID:12794167
46. Braun MY, Lowin B, French L, Acha-Orbea H, Tschopp J. Cytotoxic T cells deficient in both functional fas ligand and perforin show residual cytolytic activity yet lose their capacity to induce lethal acute graft-versus-host disease. J Exp Med 1996; 183:657-61; PMID:8627178; http://dx.doi.org/10.1084/ jem.183.2.657
47. Winter H, Hu HM, Urba WJ, Fox BA. Tumor regression after adoptive transfer of effector T cells is independent of perforin or Fas ligand (APO-1L/CD95L). J Immunol 1999; 163:4462-72; PMID:10510388
48. Lee SH, Bar-Haim E, Machlenkin A, Goldberger O, Volovitz I, Vadai E, Tzehoval E, Eisenbach L. In vivo rejection of tumor cells dependent on CD8 cells that kill independently of perforin and FasL. Cancer Gene Ther 2004; 11:237-48; PMID:14739939; http://dx.doi.org/10.1038/sj.cgt.7700678
49. Qin Z, Schwartzkopff J, Pradera F, Kammertoens T, Seliger B, Pircher H, Blankenstein T. A critical requirement of interferon gamma-mediated angiostasis for tumor rejection by CD8+ T cells. Cancer Res 2003; 63:4095-100; PMID:12874012
50. Böhm W, Thoma S, Leithäuser F, Möller P, Schirmbeck R, Reimann J. T cell-mediated, IFN-gamma-facilitated rejection of murine B16 melanomas. J Immunol 1998; 161:897-908; PMID:9670968
51. Wigginton JM, Gruys E, Geiselhart L, Subleski J, Komschlies KL, Park JW, Wiltrout TA, Nagashima K, Back TC, Wiltrout RH. IFN-gamma and Fas/FasL are required for the antitumor and antiangiogenic effects of IL-12/pulse IL-2 therapy. J Clin Invest 2001; 108:51-62; PMID:11435457; http://dx.doi.org/10. 1172/JCI200110128
52. Kowalczyk DW, Wlazlo AP, Giles-Davis W, Kammer AR, Mukhopadhyay S, Ertl HC. Vaccine-induced CD8+ T cells eliminate tumors by a two-staged attack. Cancer Gene Ther 2003; 10:870-8; PMID:14712313; http://dx.doi.org/10.1038/sj.cgt. 7700653
53. Barth RJ Jr., Mulé JJ, Spiess PJ, Rosenberg SA. Interferon gamma and tumor necrosis factor have a role in tumor regressions mediated by murine CD8+ tumor-infiltrating lymphocytes. J Exp Med 1991; 173:647-58; PMID:1900079; http://dx.doi.org/10.1084/jem.173.3.647
54. Prévost-Blondel A, Roth E, Rosenthal FM, Pircher H. Crucial role of TNF-alpha in CD8 T cell-mediated elimination of 3LL-A9 Lewis lung carcinoma cells in vivo. J Immunol 2000; 164:3645-51; PMID:10725721
55. Hollenbaugh JA, Reome J, Dobrzanski M, Dutton RW. The rate of the CD8-dependent initial reduction in tumor volume is not limited by contact-dependent perforin, Fas ligand, or TNF-mediated cytolysis. J Immunol 2004; 173:1738-43; PMID:15265903
56. Stalder T, Hahn S, Erb P. Fas antigen is the major target molecule for CD4+ T cell-mediated cytotoxicity. J Immunol 1994; 152:1127-33; PMID:7507960
57. Ju ST, Cui H, Panka DJ, Ettinger R, Marshak-Rothstein A. Participation of target Fas protein in apoptosis pathway induced by CD4+ Th1 and CD8+ cytotoxic T cells. Proc Natl Acad Sci U S A 1994; 91:4185-9; PMID:7514297; http://dx.doi.org/10.1073/pnas.91.10.4185
58. Listopad JJ, Kammertoens T, Anders K, Silkenstedt B, Willimsky G, Schmidt K, Kuehl AA, Loddenkemper C, Blankenstein T. Fas expression by tumor stroma is required for cancer eradication. Proc Natl Acad Sci U S A 2013; 110:2276-81; PMID:23341634; http://dx.doi.org/10.1073/pnas.1218295110
59. Trauth BC, Klas C, Peters AM, Matzku S, Möller P, Falk W, Debatin KM, Krammer PH. Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science 1989; 245:301-5; PMID:2787530; http://dx.doi.org/10.1126/ science.2787530
60. Yonehara S, Ishii A, Yonehara M. A cell-killing monoclonal antibody (anti-Fas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. J Exp Med 1989; 169:1747-56; PMID:2469768; http://dx.doi.org/10.1084/jem.169.5.1747
61. Ogasawara J, Watanabe-Fukunaga R, Adachi M, Matsuzawa A, Kasugai T, Kitamura Y, Itoh N, Suda T, Nagata S. Lethal effect of the anti-Fas antibody in mice. Nature 1993; 364:806-9; PMID:7689176; http://dx.doi.org/10.1038/364806a0
62. Leontieva OV, Lenzo F, Demidenko ZN, Blagosklonny MV. Hyper-mitogenic drive coexists with mitotic incompetence in senescent cells. Cell Cycle 2012; 11:4642-9; PMID:23187803; http://dx.doi.org/10.4161/cc.22937
63. Adachi M, Suematsu S, Kondo T, Ogasawara J, Tanaka T, Yoshida N, Nagata S. Targeted mutation in the Fas gene causes hyperplasia in peripheral lymphoid organs and liver. Nat Genet 1995; 11:294-300; PMID:7581453; http://dx.doi.org/ 10.1038/ng1195-294
64. Karray S, Kress C, Cuvellier S, Hue-Beauvais C, Damotte D, Babinet C, Lévi-Strauss M. Complete loss of Fas ligand gene causes massive lymphoproliferation and early death, indicating a residual activity of gld allele. J Immunol 2004; 172:2118-25; PMID:14764677
65. Senju S, Negishi I, Motoyama N, Wang F, Nakayama K, Nakayama K, Lucas PJ, Hatakeyama S, Zhang Q, Yonehara S, et al. Functional significance of the Fas molecule in naive lymphocytes. Int Immunol 1996; 8:423-31; PMID:8671629; http://dx.doi.org/10.1093/intimm/8.3.423
66. Hao Z, Hampel B, Yagita H, Rajewsky K. T cell-specific ablation of Fas leads to Fas ligand-mediated lymphocyte depletion and inflammatory pulmonary fibrosis. J Exp Med 2004; 199:1355-65; PMID:15148335; http://dx.doi.org/10.1084/ jem.20032196
67. Peter ME, Legembre P, Barnhart BC. Does CD95 have tumor promoting activities? Biochim Biophys Acta 2005; 1755:25-36; PMID:15907590
68. Eck MJ, Manley PW. The interplay of structural information and functional studies in kinase drug design: insights from BCR-Abl. Curr Opin Cell Biol 2009; 21:288-95; PMID:19217274; http://dx.doi.org/10.1016/j.ceb.2009.01.014
69. Bollag G, Tsai J, Zhang J, Zhang C, Ibrahim P, Nolop K, Hirth P. Vemurafenib: the first drug approved for BRAF-mutant cancer. Nat Rev Drug Discov 2012; 11:873-86; PMID:23060265; http://dx.doi.org/10.1038/nrd3847