TRAIL and its receptors as targets for cancer therapy (original) (raw)
Abstract
Tumor necrosis factor (TNF)‐related apoptosis‐inducing ligand (TRAIL) is a member of the TNF family of cytokines, which can induce apoptotic cell death in a variety of tumor cells by engaging the death receptors DR4 and DR5, while sparing most normal cells. Preclinical studies in mice and non‐human primates have shown the potential utility of recombinant soluble TRAIL and agonistic anti‐DR5 or DR4 antibodies for cancer therapy. Moreover, we have recently revealed a vital role for endogenously expressed TRAIL in immunosurveillance of developing and meta‐static tumors. In this review, we summarize recent knowledge about TRAIL and its receptors as promising targets for cancer therapy.
References
- 1.Wiley SR, Schooley K, Smolak PJ, Din WS, Huang CP, Nicholl JK, Sutherland GR, Smith TD, Rauch C, Smith CA, Goodwin RG. Identification and characterization of a new member of the TNF family that induces apo‐ptosis. Immunity 1995; 3: 673–82. [DOI] [PubMed] [Google Scholar]
- 2.Pitti RM, Marsters SA, Ruppert S, Donahue CJ, Moore A, Ashkenazi A. Induction of apoptosis by Apo‐2 ligand, a new member of the tumor necrosis factor cytokine family. J Biol Chem 1996; 271: 12687–90. [DOI] [PubMed] [Google Scholar]
- 3.Kayagaki N, Yamaguchi N, Nakayama M, Kawasaki A, Akiba H, Okumura K, Yagita H. Involvement of TNF‐related apoptosis‐inducing ligand in human CD4+ T cell‐mediated cytotoxicity. J Immunol 1999; 162: 2639–47. [PubMed] [Google Scholar]
- 4.Kayagaki N, Yamaguchi N, Nakayama M, Eto H, Okumura K, Yagita H. Type I interferons (IFNs) regulate tumor necrosis factor‐related apoptosis‐inducing ligand (TRAIL) expression on human T cells: A novel mechanism for the antitumor effects of type I IFNs. J Exp Med 1999; 189: 1451–60. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Kayagaki N, Yamaguchi N, Nakayama M, Takeda K, Akiba H, Tsutsui H, Okamura H, Nakanishi K, Okumura K, Yagita H. Expression and function of TNF‐related apoptosis‐inducing ligand on murine activated NK cells. J Immunol 1999; 163: 1906–13. [PubMed] [Google Scholar]
- 6.Griffith TS, Wiley SR, Kubin MZ, Sedger LM, Maliszewski CR, Fanger NA. Monocyte‐mediated tumoricidal activity via the tumor necrosis factor‐related cytokine, TRAIL. J Exp Med 1999; 189: 1343–54. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Nakayama M, Kayagaki N, Yamaguchi N, Okumura K, Yagita H. Involvement of TWEAK in interferon‐T‐stimulated monocyte cytotoxicity. J Exp Med 2000; 192: 1373–80. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Fanger NA, Maliszewski CR, Schooley K, Griffith TS. Human dendritic cells mediate cellular apoptosis via tumor necrosis factor‐related apoptosis‐inducing ligand (TRAIL). J Exp Med 1999; 190: 1155–64. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Koga Y, Matsuzaki A, Suminoe A, Hattori H, Hara T. Neutrophil‐derived TNF‐related apoptosis‐inducing ligand (TRAIL): a novel mechanism of anti‐tumor effect by neutrophils. Cancer Res 2004; 64: 1037–43. [DOI] [PubMed] [Google Scholar]
- 10.Cretney E, Takeda K, Yagita H, Glaccum M, Peschon JJ, Smyth MJ. Increased susceptibility to tumor initiation and metastasis in TNF‐related apoptosis‐inducing ligand‐deficient mice. J Immunol 2002; 168: 1356–61. [DOI] [PubMed] [Google Scholar]
- 11.Sedger LM, Glaccum MB, Schuh JC, Kanaly ST, Williamson E, Kayagaki N, Yun T, Smolak P, Le T, Goodwin R, Gliniak B. Characterization of the in vivo function of TNF‐alpha‐related apoptosis‐inducing ligand, TRAIL/ Apo2L, using TRAIL/Apo2L gene‐deficient mice. Eur J Immunol 2002; 32: 2246–54. [DOI] [PubMed] [Google Scholar]
- 12.Lamhamedi‐Cherradi SE, Zheng SJ, Maguschak KA, Peschon J, Chen YH. Defective thymocyte apoptosis and accelerated autoimmune diseases in TRAIL–/– mice. Nat Immunol 2003; 4: 255–60. [DOI] [PubMed] [Google Scholar]
- 13.Ashkenazi A. Targeting death and decoy receptors of the tumour‐necrosis factor superfamily. Nat Rev Cancer 2002; 2: 420–30. [DOI] [PubMed] [Google Scholar]
- 14.Wang S, El‐Deiry WS. TRAIL and apoptosis induction by TNF‐family death receptors. Oncogene 2003; 22: 8628–33. [DOI] [PubMed] [Google Scholar]
- 15.Schneider P, Olson D, Tardivel A, Browning B, Lugovskoy A, Gong D, Dobles M, Hertig S, Hofmann K, van Vlijmen H, Hsu YM, Burkly LC, Tschopp J, Zheng TS. Identification of a new murine tumor necrosis factor receptor locus that contains two novel murine receptors for tumor necrosis factor‐related apoptosis‐inducing ligand (TRAIL). J Biol Chem 2003; 278: 5444–54. [DOI] [PubMed] [Google Scholar]
- 16.Zhang XD, Franco AV, Nguyen T, Gray CP, Hersey P. Differential localization and regulation of death and decoy receptors for TNF‐related apoptosis‐inducing ligand (TRAIL) in human melanoma cells. J Immunol 2000; 164: 3961–70. [DOI] [PubMed] [Google Scholar]
- 17.Wang Y, Engels IH, Knee DA, Nasoff M, Deveraux QL, Quon KC. Synthetic lethal targeting of MYC by activation of the DR5 death receptor pathway. Cancer Cell 2004; 5: 501–12. [DOI] [PubMed] [Google Scholar]
- 18.Nesterov A, Nikrad M, Johnson T, Kraft AS. Oncogenic Ras sensitizes normal human cells to tumor necrosis factor‐alpha‐related apoptosis‐inducing ligand‐induced apoptosis. Cancer Res 2004; 64: 3922–7. [DOI] [PubMed] [Google Scholar]
- 19.van Noesel MM, van Bezouw S, Salomons GS, Voute PA, Pieters R, Baylin SB, Herman JG, Versteeg R. Tumor‐specific down‐regulation of the tumor necrosis factor‐related apoptosis‐inducing ligand decoy receptors DcR1 and DcR2 is associated with dense promoter hypermethylation. Cancer Res 2002; 62: 2157–61. [PubMed] [Google Scholar]
- 20.Spierings DC, De Vries EG, Vellenga E, Van Den Heuvel FA, Koornstra JJ, Wesseling J, Hollema H, de Jong S. Tissue distribution of the death ligand TRAIL and its receptors. J Histochem Cytochem 2004; 52: 821–31. [DOI] [PubMed] [Google Scholar]
- 21.Degli‐Esposti M. To die or not to die‐the quest of the TRAIL receptors. J Leukoc Biol 1999; 65: 535–42. [DOI] [PubMed] [Google Scholar]
- 22.Sheridan JP, Marsters SA, Pitti RM, Gurney A, Skubatch M, Baldwin D, Ramakrishnan L, Gray CL, Baker K, Wood WI, Goddard AD, Godowski P, Ashkenazi A. Control of TRAIL‐induced apoptosis by a family of signaling and decoy receptors. Science 1997; 277: 818–21. [DOI] [PubMed] [Google Scholar]
- 23.Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M, Chin W, Jones J, Woodward A, Le T, Smith C, Smolak P, Goodwin RG, Rauch CT, Schuh JC, Lynch DH. Tumoricidal activity of tumor necrosis factor‐related apoptosis‐inducing ligand in vivo. Nat Med 1999; 5: 157–63. [DOI] [PubMed] [Google Scholar]
- 24.Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, Marsters SA, Blackie C, Chang L, McMurtrey AE, Hebert A, DeForge L, Koumenis IL, Lewis D, Harris L, Bussiere J, Koeppen H, Shahrokh Z, Schwall RH. Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 1999; 104: 155–62. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Gliniak B, Le T. Tumor necrosis factor‐related apoptosis‐inducing ligand's antitumor activity in vivo is enhanced by the chemotherapeutic agent CPT‐11. Cancer Res 1999; 59: 6153–8. [PubMed] [Google Scholar]
- 26.Chinnaiyan AM, Prasad U, Shankar S, Hamstra DA, Shanaiah M, Chenevert TL, Ross BD, Rehemtulla A. Combined effect of tumor necrosis factor‐related apoptosis‐inducing ligand and ionizing radiation in breast cancer therapy. Proc Natl Acad Sci USA 2000; 97: 1754–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Shankar S, Srivastava RK. Enhancement of therapeutic potential of TRAIL by cancer chemotherapy and irradiation: mechanisms and clinical implications. Drug Resist Updat 2004; 7: 139–56. [DOI] [PubMed] [Google Scholar]
- 28.Wajant H, Pfizenmaier K, Scheurich P. TNF‐related apoptosis inducing ligand (TRAIL) and its receptors in tumor surveillance and cancer therapy. Apoptosis 2002; 7: 449–59. [DOI] [PubMed] [Google Scholar]
- 29.Hersey P, Zhang XD. How melanoma cells evade TRAIL‐induced apoptosis. Nat Rev Cancer 2001; 1: 142–50. [DOI] [PubMed] [Google Scholar]
- 30.Wang S, El‐Deiry WS. Requirement of p53 targets in chemosensitization of colonic carcinoma to death ligand therapy. Proc Natl Acad Sci USA 2003; 100: 15095–100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Shankar S, Singh TR, Chen X, Thakkar H, Firnin J, Srivastava RK. The sequential treatment with ionizing radiation followed by TRAIL/Apo‐2L reduces tumor growth and induces apoptosis of breast tumor xenografts in nude mice. Int J Oncol 2004; 24: 1133–40. [PubMed] [Google Scholar]
- 32.Sayers TJ, Brooks AD, Koh CY, Ma W, Seki N, Raziuddin A, Blazar BR, Zhang X, Elliott PJ, Murphy WJ. The proteasome inhibitor PS‐341 sensitizes neoplastic cells to TRAIL‐mediated apoptosis by reducing levels of c‐FLIP. Blood 2003; 102: 303–10. [DOI] [PubMed] [Google Scholar]
- 33.Johnson TR, Stone K, Nikrad M, Yeh T, Zong WX, Thompson CB, Nesterov A, Kraft AS. The proteasome inhibitor PS‐341 overcomes TRAIL resistance in Bax and caspase 9‐negative or Bcl‐xL overexpressing cells. Oncogene 2003; 22: 4953–63. [DOI] [PubMed] [Google Scholar]
- 34.He Q, Huang Y, Sheikh MS. Proteasome inhibitor MG132 upregulates death receptor 5 and cooperates with Apo2L/TRAIL to induce apoptosis in Bax‐proficient and ‐deficient cells. Oncogene 2004; 23: 2554–8. [DOI] [PubMed] [Google Scholar]
- 35.Kim S, Choi K, Kwon D, Benveniste EN, Choi C. Ubiquitin‐proteasome pathway as a primary defender against TRAIL‐mediated cell death. Cell Mol Life Sci 2004; 61: 1075–81. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Jo M, Kim TH, Seol DW, Esplen JE, Dorko K, Billiar TR, Strom SC. Apoptosis induced in normal human hepatocytes by tumor necrosis factor‐related apoptosis‐inducing ligand. Nat Med 2000; 6: 564–7. [DOI] [PubMed] [Google Scholar]
- 37.Lawrence D, Shahrokh Z, Marsters S, Achilles K, Shih D, Mounho B, Hillan K, Totpal K, DeForge L, Schow P, Hooley J, Sherwood S, Pai R, Leung S, Khan L, Gliniak B, Bussiere J, Smith CA, Strom SS, Kelley S, Fox JA, Thomas D, Ashkenazi A. Differential hepatocyte toxicity of recombinant Apo2L/TRAIL versions. Nat Med 2001; 7: 383–5. [DOI] [PubMed] [Google Scholar]
- 38.Qin J, Chaturvedi V, Bonish B, Nickoloff BJ. Avoiding premature apoptosis of normal epidermal cells. Nat Med 2001; 7: 385–6. [DOI] [PubMed] [Google Scholar]
- 39.Armeanu S, Lauer UM, Smirnow I, Schenk M, Weiss TS, Gregor M, Bitzer M. Adenoviral gene transfer of tumor necrosis factor‐related apoptosis‐inducing ligand overcomes an impaired response of hepatoma cells but causes severe apoptosis in primary human hepatocytes. Cancer Res 2003; 63: 2369–72. [PubMed] [Google Scholar]
- 40.Mundt B, Kuhnel F, Zender L, Paul Y, Tillmann H, Trautwein C, Manns MP, Kubicka S. Involvement of TRAIL and its receptors in viral hepatitis. FASEB J 2003; 17: 94–6. [DOI] [PubMed] [Google Scholar]
- 41.Ichikawa K, Liu W, Zhao L, Wang Z, Liu D, Ohtsuka T, Zhang H, Mountz JD, Koopman WJ, Kimberly RP, Zhou T. Tumoricidal activity of a novel anti‐human DR5 monoclonal antibody without hepatocyte cytotoxicity. Nat Med 2001; 7: 954–60. [DOI] [PubMed] [Google Scholar]
- 42.Higuchi H, Bronk SF, Taniai M, Canbay A, Gores GJ. Cholestasis increases tumor necrosis factor‐related apoptotis‐inducing ligand (TRAIL)‐R2/DR5 expression and sensitizes the liver to TRAIL‐mediated cytotoxicity. J Phar-macol Exp Ther 2002; 303: 461–7. [DOI] [PubMed] [Google Scholar]
- 43.Zheng SJ, Wang P, Tsabary G, Chen YH. Critical roles of TRAIL in hepatic cell death and hepatic inflammation. J Clin Invest 2004; 113: 58–64. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Leverkus M, Sprick MR, Wachter T, Mengling T, Baumann B, Serfling E, Brocker EB, Goebeler M, Neumann M, Walczak H. Proteasome inhibition results in TRAIL sensitization of primary keratinocytes by removing the resistance‐mediating block of effector caspase maturation. Mol Cell Biol 2003; 23: 777–90. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Leverkus M, Neumann M, Mengling T, Rauch CT, Brocker EB, Krammer PH, Walczak H. Regulation of tumor necrosis factor‐related apoptosis‐inducing ligand sensitivity in primary and transformed human keratinocytes. Cancer Res 2000; 60: 553–9. [PubMed] [Google Scholar]
- 46.Li JH, Kirkiles‐Smith NC, McNiff JM, Pober JS. TRAIL induces apoptosis and inflammatory gene expression in human endothelial cells. J Immunol 2003; 171: 1526–33. [DOI] [PubMed] [Google Scholar]
- 47.Griffith TS, Rauch CT, Smolak PJ, Waugh JY, Boiani N, Lynch DH, Smith CA, Goodwin RG, Kubin MZ. Functional analysis of TRAIL receptors using monoclonal antibodies. J Immunol 1999; 162: 2597–605. [PubMed] [Google Scholar]
- 48.Chuntharapai A, Dodge K, Grimmer K, Schroeder K, Marsters SA, Koeppen H, Ashkenazi A, Kim KJ. Isotype‐dependent inhibition of tumor growth in vivo by monoclonal antibodies to death receptor 4. J Immunol 2001; 166: 4891–8. [DOI] [PubMed] [Google Scholar]
- 49.Mori E, Thomas M, Motoki K, Nakazawa K, Tahara T, Tomizuka K, Ishida I, Kataoka S. Human normal hepatocytes are susceptible to apoptosis signal mediated by both TRAIL‐R1 and TRAIL‐R2. Cell Death Differ 2004; 11: 203–7. [DOI] [PubMed] [Google Scholar]
- 50.Ohtsuka T, Buchsbaum D, Oliver P, Makhija S, Kimberly R, Zhou T. Synergistic induction of tumor cell apoptosis by death receptor antibody and chemotherapy agent through JNK/p38 and mitochondrial death pathway. Oncogene 2003; 22: 2034–44. [DOI] [PubMed] [Google Scholar]
- 51.Takeda K, Yamaguchi N, Akiba H, Kojima Y, Hayakawa Y, Tanner JE, Sayers TJ, Seki N, Okumura K, Yagita H, Smyth MJ. Induction of tumor‐specific T cell immunity by anti‐DR5 antibody therapy. J Exp Med 2004; 199: 437–48. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Ludwig AT, Moore JM, Luo Y, Chen X, Saltsgaver NA, O'Donnell MA, Griffith TS. Tumor necrosis factor‐related apoptosis‐inducing ligand: a novel mechanism for Bacillus Calmette‐Guerin‐induced antitumor activity. Cancer Res 2004; 64: 3386–90. [DOI] [PubMed] [Google Scholar]
- 53.Chen Q, Gong B, Mahmoud‐Ahmed AS, Zhou A, Hsi ED, Hussein M, Almasan A. Apo2L/TRAIL and Bcl‐2‐related proteins regulate type I inter‐feron‐induced apoptosis in multiple myeloma. Blood 2001; 98: 2183–92. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 54.Oshima K, Yanase N, Ibukiyama C, Yamashina A, Kayagaki N, Yagita H, Mizuguchi J. Involvement of TRAIL/TRAIL‐R interaction in IFN‐alpha‐in‐duced apoptosis of Daudi B lymphoma cells. Cytokine 2001; 14: 193–201. [DOI] [PubMed] [Google Scholar]
- 55.Altucci L, Rossin A, Raffelsberger W, Reitmair A, Chomienne C, Gronemeyer H. Retinoic acid‐induced apoptosis in leukemia cells is mediated by paracrine action of tumor‐selective death ligand TRAIL. Nat Med 2001; 7: 680–6. [DOI] [PubMed] [Google Scholar]
- 56.Takeda K, Hayakawa Y, Smyth MJ, Kayagaki N, Yamaguchi N, Kakuta S, Iwakura Y, Yagita H, Okumura K. Involvement of tumor necrosis factor‐related apoptosis‐inducing ligand in surveillance of tumor metastasis by liver natural killer cells. Nat Med 2001; 7: 94–100. [DOI] [PubMed] [Google Scholar]
- 57.Seki N, Hayakawa Y, Brooks AD, Wine J, Wiltrout RH, Yagita H, Tanner JE, Smyth MJ, Sayers TJ. Tumor necrosis factor‐related apoptosis‐inducing ligand‐mediated apoptosis is an important endogenous mechanism for resistance to liver metastases in murine renal cancer. Cancer Res 2003; 63: 207–13. [PubMed] [Google Scholar]
- 58.Smyth MJ, Cretney E, Takeda K, Wiltrout RH, Sedger LM, Kayagaki N, Yagita H, Okumura K. Tumor necrosis factor‐related apoptosis‐inducing ligand (TRAIL) contributes to interferon gamma‐dependent natural killer cell protection from tumor metastasis. J Exp Med 2001; 193: 661–70. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59.Takeda K, Smyth MJ, Cretney E, Hayakawa Y, Kayagaki N, Yagita H, Okumura K. Critical role for tumor necrosis factor‐related apoptosis‐inducing ligand in immune surveillance against tumor development. J Exp Med 2002; 195: 161–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 60.Schmaltz C, Alpdogan O, Kappel BJ, Muriglan SJ, Rotolo JA, Ongchin J, Willis LM, Greenberg AS, Eng JM, Crawford JM, Murphy GF, Yagita H, Walczak H, Peschon JJ, van den Brink MR. T cells require TRAIL for optimal graft‐versus‐tumor activity. Nat Med 2002; 8: 1433–7. [DOI] [PubMed] [Google Scholar]
- 61.Tsukada N, Kobata T, Aizawa Y, Yagita H, Okumura K. Graft‐versus‐leuke‐mia effect and graft‐versus‐host disease can be differentiated by cytotoxic mechanisms in a murine model of allogeneic bone marrow transplantation. Blood 1999; 93: 2738–47. [PubMed] [Google Scholar]
- 62.Ursini‐Siegel J, Zhang W, Altmeyer A, Hatada EN, Do RK, Yagita H, Chen‐Kiang S. TRAIL/Apo‐2 ligand induces primary plasma cell apoptosis. J Immunol 2002; 169: 5505–13. [DOI] [PubMed] [Google Scholar]
- 63.Kayagaki N, Yamaguchi N, Abe M, Hirose S, Shirai T, Okumura K, Yagita H. Suppression of antibody production by TNF‐related apoptosis‐inducing ligand (TRAIL). Cell Immunol 2002; 219: 82–91. [DOI] [PubMed] [Google Scholar]
- 64.Hayakawa Y, Screpanti V, Yagita H, Grandien A, Ljunggren HG, Smyth MJ, Chambers BJ. NK cell TRAIL eliminates immature dendritic cells in vivo and limits dendritic cell vaccination efficacy. J Immunol 2004; 172: 123–9. [DOI] [PubMed] [Google Scholar]
- 65.Lunemann JD, Waiczies S, Ehrlich S, Wendling U, Seeger B, Kamradt T, Zipp F. Death ligand TRAIL induces no apoptosis but inhibits activation of human (auto)antigen‐specific T cells. J Immunol 2002; 168: 4881–8. [DOI] [PubMed] [Google Scholar]
- 66.Song K, Chen Y, Goke R, Wilmen A, Seidel C, Goke A, Hilliard B. Tumor necrosis factor‐related apoptosis‐inducing ligand (TRAIL) is an inhibitor of autoimmune inflammation and cell cycle progression. J Exp Med 2000; 191: 1095–104. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 67.Hilliard B, Wilmen A, Seidel C, Liu TS, Goke R, Chen Y. Roles of TNF‐related apoptosis‐inducing ligand in experimental autoimmune encephalomy‐elitis. J Immunol 2001; 166: 1314–9. [DOI] [PubMed] [Google Scholar]