The role of Fas ligand and transforming growth factor β in tumor progression: Molecular mechanisms of immune privilege via Fas-mediated apoptosis and potential targets for cancer therapy

Cancer

Volumn 100, Issue 11, 2004, Pages 2281-2291

  Kim, Ryungsa ^a   Emi, Manabu ^a   Tanabe, Kazuaki ^a   Uchida, Yoko ^a   Toge, Tetsuya ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Apoptosis; Fas ligand; Immune privilege; Transforming growth factor ; Tumor microenvironment

Indexed keywords

FAS LIGAND; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1; TRANSFORMING GROWTH FACTOR BETA;

APOPTOSIS; CANCER INHIBITION; CANCER THERAPY; CYTOTOXIC T LYMPHOCYTE; HUMAN; IMMUNOSURVEILLANCE; METASTASIS; NATURAL KILLER CELL; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; SOLID TUMOR; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH;

APOPTOSIS; FAS LIGAND PROTEIN; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; MEMBRANE GLYCOPROTEINS; NEOPLASMS; NEUTROPHILS; RECEPTORS, TUMOR NECROSIS FACTOR; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 2442674389     PISSN: 0008543X     EISSN: None     Source Type: Journal    
DOI: 10.1002/cncr.20270     Document Type: Review

References (107)

1. Folkman J. Angiogenesis and apoptosis. Semin Cancer Biol. 2003;13:159-167.
2. Ferlini C, D'Amelio R, Scambia G. Apoptosis induced by ionizing radiation. The biological basis of radiosensitivity. Subcell Biochem. 2002;36:171-186.
3. Kim R, Tanabe K, Uchida Y, Emi M, Inoue H, Toge T. Current status of the molecular mechanisms of anticancer drug-induced apoptosis. The contribution of molecular-level analysis to cancer chemotherapy. Cancer Chemother Pharmacol. 2002;50:343-352.
4. Reichmann E. The biological role of the Fas/FasL system during tumor formation and progression. Semin Cancer Biol. 2002;12:309-315.
5. Green DR, Droin N, Pinkoski M. Activation-induced cell death in T cells. Immunol Rev. 2003;193:70-81.
6. Rivoltini L, Carrabba M, Huber V, et al. Immunity to cancer: attack and escape in T lymphocyte-tumor cell interaction. Immunol Rev. 2002;188:97-113.
7. Attisano L, Wrana JL. Signal transduction by the TGF-beta superfamily. Science. 2002;296:1646-1647.
8. Moustakas A, Pardali K, Gaal A, Heldin CH. Mechanisms of TGF-β signaling in regulation of cell growth and differentiation. Immunol Lett. 2002;82:85-91.
9. Tang B, Vu M, Booker T, et al. TGF-beta switches from tumor suppressor to prometastatic factor in a model of breast cancer progression. J Clin Invest. 2003;112:1116-1124.
10. Cappello F, Bellafiore M, Palma A, Bucchieri F. Defective apoptosis and tumorigenesis: role of p53 mutation and Fas/FasL system dysregulation. Eur J Histochem. 2002;46:199-208.
11. Ferguson TA, Green DR, Griffith TS. Expression of functional Fas ligand in choriocarcinoma. Am J Reprod Immunol. 2002;48:226-234.
12. Redondo P, Solano T, Vazquez B, Bauza A, Idoate M. Fas and Fas ligand: expression and soluble circulating levels in cutaneous malignant melanoma. Br J Dermatol. 2002;147:80-86.
13. Verbeke CS, Wenthe U, Grobholz R, Zentgraf H. Fas ligand expression in Hodgkin lymphoma. Am J Surg Pathol. 2001;25:388-394.
14. Kase S, Osaki M, Adachi H, Kaibara N, Ito H. Expression of Fas and Fas ligand in esophageal tissue mucosa and carcinomas. Int J Oncol. 2002;20:291-297.
15. Lim SC. Expression of Fas ligand and sFas ligand in human gastric adenocarcinomas. Oncol Rep. 2002;9:103-107.
16. Nozoe T, Yasuda M, Honda M, Inutsuka S, Korenaga D. Fas ligand expression is correlated with metastasis in colorectal carcinoma. Oncology. 2003;65:83-88.
17. Muschen M, Moers C, Warskulat U, Even J, Niederacher D, Beckmann MW. CD95 ligand expression as a mechanism of immune escape in breast cancer. Immunology. 2000;99:69-77.
18. Mitsiades N, Poulaki V, Kotoula V, Leone A, Tsokos M. Fas ligand is present in tumors of the Ewing's sarcoma family and is cleaved into a soluble form by a metalloproteinase. Am J Pathol. 1998;153:1947-1956.
19. Martinez-Lorenzo MJ, Anel A, Gamen S, et al. Activated human T cells release bioactive Fas ligand and APO2 ligand in microvesicles. J Immunol. 1999;163:1274-1281.
20. Suda T, Okazaki T, Naito Y, et al. Expression of the Fas ligand in cells of T cell lineage. J Immunol. 1995;154:3806-3813.
21. Strand S, Hofmann WJ, Hug H, et al. Lymphocyte apoptosis induced by CD95 (APO-1/Fas) ligand-expressing tumor cells - a mechanism of immune evasion? Nat Med. 1996;2:1361-1366.
22. Huang B, Eberstadt M, Olejniczak ET, Meadows RP, Fesik SW. NMR structure and mutagenesis of the Fas (APO-1/CD95) death domain. Nature. 1996;384:638-641.
23. Oyaizu N, McCloskey TW, Than S, Hu R, Kalyanaraman VS, Pahwa S. Cross-linking of CD4 molecules upregulates Fas antigen expression in lymphocytes by inducing interferon-gamma and tumor necrosis factor-alpha secretion. Blood. 1994;84:2622-2631.
24. Weber CH, Vincenz C. A docking model of key components of the DISC complex: death domain superfamily interactions redefined. FEBS Lett. 2001;492:171-176.
25. Govinden R, Bhoola KD. Genealogy, expression, and cellular function of transforming growth factor-β. Pharmacol Ther. 2003;98:257-265.
26. Shi Y, Massague J. Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell. 2003;113:685-700.
27. Attisano L, Wrana JL. Signal transduction by the TGF-beta superfamily. Science. 2002;296:1646-1647.
28. Moustakas A, Souchelnytskyi S, Heldin CH. Smad regulation in TGF-β signal transduction. J Cell Sci. 2001;114:4359-4369.
29. Herrera RE, Makela TP, Weinberg RA. Active transcriptional repression by the Rb-E2F complex mediates G1 arrest triggered by p16INK4a, TGF beta, and contact inhibition. Cell. 1999;97:53-61.
30. Zhou GH, Sechrist GL, Periyasamy S, Brattain MG, Mulder KM. Transforming growth factor beta isoform-specific differences in interactions with type I and II transforming growth factor beta receptors. Cancer Res. 1995;55:2056-2062.
31. Yan Z, Kim GY, Deng X, Friedman E. Transforming growth factor β1 induces proliferation in colon carcinoma cells by Ras-dependent, smad-independent down-regulation of p21cip1. J Biol Chem. 2002;277:9870-9879.
32. Tobin SW, Douville K, Benbow U, Brinckerhoff CE, Memoli VA, Arrick BA. Consequences of altered TGF-beta expression and responsiveness in breast cancer: evidence for autocrine and paracrine effects. Oncogene. 2002;21:108-118.
33. Simeone DM, Pham T, Logsdon CD. Disruption of TGFβ signaling pathways in human pancreatic cancer cells. Ann Surg. 2000;232:73-80.
34. Olschwang S, Hamelin R, Laurent-Puig P, et al. Alternative genetic pathways in colorectal carcinogenesis. Proc Natl Acad Sci U S A. 1997;94:12122-12127.
35. Tannergard P, Liu T, Weger A, Nordenskjold M, Lindblom A. Tumorigenesis in colorectal tumors from patients with hereditary non-polyposis colorectal cancer. Hum Genet. 1997;101:51-55.
36. Grady WM, Myeroff LL, Swinler SE, et al. Mutational inactivation of transforming growth factor β receptor type II in microsatellite stable colon cancers. Cancer Res. 1999;59:320-324.
37. Prunier C, Mazars A, Noe V, et al. Evidence that Smad2 is a tumor suppressor implicated in the control of cellular invasion. J Biol Chem. 1999;274:22919-22922.
38. Mamot C, Mild G, Reuter J, et al. Infrequent mutation of the tumour-suppressor gene Smad4 in early-stage colorectal cancer. Br J Cancer. 2003;88:420-423.
39. Shim KS, Kim KH, Han WS, Park EB. Elevated serum levels of transforming growth factor-β1 in patients with colorectal carcinoma: its association with tumor progression and its significant decrease after curative surgical resection. Cancer. 1999;85:554-561.
40. Shin I, Bakin AV, Rodeck U, Brunet A, Arteaga CL. Transforming growth factor β enhances epithelial cell survival via Akt-dependent regulation of FKHRL1. Mol Biol Cell. 2001;12:3328-3339.
41. Lu PJ, Lu QL, Rughetti A, Taylor-Papadimitriou J. bcl-2 overexpression inhibits cell death and promotes the morphogenesis, but not tumorigenesis of human mammary epithelial cells. J Cell Biol. 1995;129:1363-1378.
42. Portella G, Cumming SA, Liddell J, et al. Transforming growth factor beta is essential for spindle cell conversion of mouse skin carcinoma in vivo: implications for tumor invasion. Cell Growth Differ. 1998;9:393-404.
43. Cui W, Fowlis DJ, Bryson S, et al. TGF β1 inhibits the formation of benign skin tumors, but enhances progression to invasive spindle carcinomas in transgenic mice. Cell. 1996;86:531-542.
44. Oft M, Peli J, Rudaz C, Schwarz H, Beug H, Reichmann E. TGF-β1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells. Genes Dev. 1996;10:2462-2477.
45. Zhang X, Wang T, Batist G, Tsao MS. Transforming growth factor beta 1 promotes spontaneous transformation of cultured rat liver epithelial cells. Cancer Res. 1994;54:6122-6128.
46. Hsu PN, Lin HH, Tu CF, et al. Expression of human Fas ligand on mouse beta islet cells does not induce insulitis but is insufficient to confer immune privilege for islet grafts. J Biomed Sci. 2001;8:262-269.
47. Nagata S. Fas ligand-induced apoptosis. Annu Rev Genet. 1999;33:29-55.
48. Whiteside TL. Tumor-induced death of immune cells: its mechanisms and consequences. Semin Cancer Biol. 2002;12:43-50.
49. Bennett MW, O'Connell J, Houston A, et al. Fas ligand upregulation is an early event in colonic carcinogenesis. J Clin Pathol. 2001;54:598-604.
50. Shiraki K, Tsuji N, Shioda T, Isselbacher KJ, Takahashi H. Expression of Fas ligand in liver metastases of human colonic adenocarcinomas. Proc Natl Acad Sci U S A. 1997;94:6420-6425.
51. O'Connell J, Bennett MW, O'Sullivan GC, Collins JK, Shanahan F. Resistance to Fas (APO-1/CD95)-mediated apoptosis and expression of Fas ligand in esophageal cancer: the Fas counterattack. Dis Esophagus. 1999;12:83-89.
52. Tsutsumi S, Kuwano H, Shimura T, Morinaga N, Mochiki E, Asao T. Circulating soluble Fas ligand in patients with gastric carcinoma. Cancer. 2000;89:2560-2564.
53. Bennett MW, O'Connell J, O'Sullivan GC, et al. Expression of Fas ligand by human gastric adenocarcinomas: a potential mechanism of immune escape in stomach cancer. Gut. 1999;44:156-162.
54. Koyama S, Koike N, Adachi S. Fas receptor counterattack against tumor-infiltrating lymphocytes in vivo as a mechanism of immune escape in gastric carcinoma. J Cancer Res Clin Oncol. 2001;127:20-26.
55. Hahne M, Rimoldi D, Schroter M, et al. Melanoma cell expression of Fas (Apo-1/CD95) ligand: implications for tumor immune escape. Science. 1996;274:1363-1366.
56. Gastman BR, Atarshi Y, Reichert TE, et al. Fas ligand is expressed on human squamous cell carcinomas of the head and neck, and it promotes apoptosis of T lymphocytes. Cancer Res. 1999;59:5356-5364.
57. Bennett MW, O'Connell J, O'Sullivan GC, et al. The Fas counterattack in vivo: apoptotic depletion of tumor-infiltrating lymphocytes associated with Fas ligand expression by human esophageal carcinoma. J Immunol. 1998;160:5669-5675.
58. Reichert TE, Strauss L, Wagner EM, Gooding W, Whiteside TL. Signaling abnormalities, apoptosis, and reduced proliferation of circulating and tumor-infiltrating lymphocytes in patients with oral carcinoma. Clin Cancer Res. 2002;8:3137-3145.
59. Zusman I, Gurevich P, Gurevich E, Ben-Hur H. The immune system, apoptosis and apoptosis-related proteins in human ovarian tumors (a review). Int J Oncol. 2001;18:965-972.
60. Mottolese M, Buglioni S, Bracalenti C, et al. Prognostic relevance of altered Fas (CD95)-system in human breast cancer. Int J Cancer. 2000;89:127-132.
61. Munakata S, Enomoto T, Tsujimoto M, et al. Expressions of Fas ligand and other apoptosis-related genes and their prognostic significance in epithelial ovarian neoplasms. Br J Cancer. 2000;82:1446-1452.
62. Qin LX, Tang ZY. The prognostic molecular markers in hepatocellular carcinoma. World J Gastroenterol. 2002;8:385-392.
63. Shibakita M, Tachibana M, Dhar DK, et al. Prognostic significance of Fas and Fas ligand expressions in human esophageal cancer. Clin Cancer Res. 1999;5:2464-2469.
64. Chen JJ, Sun Y, Nabel GJ. Regulation of the proinflammatory effects of Fas ligand (CD95L). Science. 1998;282:1714-1717.
65. Shen L, Liang AC, Lu L, et al. Frequent deletion of Fas gene sequences encoding death and transmembrane domains in nasal natural killer/T-cell lymphoma. Am J Pathol. 2002;161:2123-2131.
66. Lee SH, Shin MS, Park WS, et al. Alterations of Fas (APO1/CD95) gene in transitional cell carcinomas of urinary bladder. Cancer Res. 1999;59:3068-3072.
67. Yamamoto H, Gil J, Schwartz S Jr., Perucho M. Frameshift mutations in Fas, Apaf-1, and Bcl-10 in gastro-intestinal cancer of the microsatellite mutator phenotype. Cell Death Differ. 2000;7:238-239.
68. Shin MS, Park WS, Kim SY, et al. Alterations of Fas (Apo1/CD95) gene in cutaneous malignant melanoma. Am J Pathol. 1999;154:1785-1791.
69. Shannon AM, Bouchier-Hayes DJ, Condron CM, Toomey D. Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies. Cancer Treat Rev. 2003;29:297-307.
70. Zalcenstein A, Stambolsky P, Weisz L, et al. Mutant p53 gain of function: repression of CD95(Fas/APO-1) gene expression by tumor-associated p53 mutants. Oncogene. 2003;22:5667-5676.
71. Ivanov VN, Krasilnikov M, Ronai Z. Regulation of Fas expression by STAT3 and c-Jun is mediated by phosphatidylinositol 3-kinase-AKT signaling. J Biol Chem. 2002;277:4932-4944.
72. Genestier L, Kasibhatla S, Brunner T, Green DR. Transforming growth factor β1 inhibits Fas ligand expression and subsequent activation-induced cell death in T cells via downregulation of c-Myc. J Exp Med. 1999;189:231-239.
73. Takahashi A, Kono K, Ichihara F, et al. Macrophages in tumor-draining lymph node with different characteristics induce T-cell apoptosis in patients with advanced stage-gastric cancer. Int J Cancer. 2003;104:393-399.
74. Whiteside TL. Apoptosis of immune cells in the tumor microenvironment and peripheral circulation of patients with cancer: implications for immunotherapy. Vaccine. 2002;20:A46-A51.
75. Dworacki G, Meidenbauer N, Kuss I, et al. Decreased zeta chain expression and apoptosis in CD3+ peripheral blood T lymphocytes of patients with melanoma. Clin Cancer Res. 2001;7(3 Suppl):947s-957s.
76. Gastman BR, Johnson DE, Whiteside TL, Rabinowich H. Caspase-mediated degradation of T-cell receptor ζ-chain. Cancer Res. 1999;59:1422-1427.
77. Hoffmann TK, Dworacki G, Tsukihiro T, et al. Spontaneous apoptosis of circulating T lymphocytes in patients with head and neck cancer and its clinical importance. Clin Cancer Res. 2002;8:2553-2562.
78. Takahashi A, Kono K, Amemiya H, Iizuka H, Fujii H, Matsumoto Y. Elevated caspase-3 activity in peripheral blood T cells coexists with increased degree of T-cell apoptosis and down-regulation of TCR zeta molecules in patients with gastric cancer. Clin Cancer Res. 2001;7:74-80.
79. Viola A. The amplification of TCR signaling by dynamic membrane microdomains. Trends Immunol. 2001;22:322-327.
80. Abrahams VM, Straszewski SL, Kamsteeg M, et al. Epithelial ovarian cancer cells secrete functional Fas ligand. Cancer Res. 2003;63:5573-5581.
81. Tillman DM, Petak I, Houghton JA. A Fas-dependent component in 5-fluorouracil/leucovorin-induced cytotoxicity in colon carcinoma cells. Clin Cancer Res. 1999;5:425-430.
82. Schwartzberg LS, Petak I, Stewart C, et al. Modulation of the Fas signaling pathway by IFN-γ in therapy of colon cancer: Phase I trial and correlative studies of IFN-γ, 5-fluorouracil, and leucovorin. Clin Cancer Res. 2002;8:2488-2498.
83. Sakon M, Nagano H, Dono K, et al. Combined intraarterial 5-fluorouracil and subcutaneous interferon-α therapy for advanced hepatocellular carcinoma with tumor thrombi in the major portal branches. Cancer. 2002;94:435-442.
84. Takaoka A, Hayakawa S, Yanai H, et al. Integration of interferon-α/β signalling to p53 responses in tumour suppression and antiviral defense. Nature. 2003;424:516-523.
85. Lacour S, Micheau O, Hammann A, et al. Chemotherapy enhances TNF-related apoptosis-inducing ligand DISC assembly in HT29 human colon cancer cells. Oncogene. 2003;22:1807-1816.
86. Evdokiou A, Bouralexis S, Atkins GJ, et al. Chemotherapeutic agents sensitize osteogenic sarcoma cells, but not normal human bone cells, to Apo2L/TRAIL-induced apoptosis. Int J Cancer. 2002;99:491-504.
87. Pinkoski MJ, Brunner T, Green DR, Lin T. Fas and Fas ligand in gut and liver. Am J Physiol Gastrointest Liver Physiol. 2000;278:G354-G366.
88. Mitsiades N, Poulaki V, Leone A, Tsokos M. Fas-mediated apoptosis in Ewing's sarcoma cell lines by metalloproteinase inhibitors. J Natl Cancer Inst. 1999;91:1678-1684.
89. Mitsiades N, Yu WH, Poulaki V, Tsokos M, Stamenkovic I. Matrix metalloproteinase-7-mediated cleavage of Fas ligand protects tumor cells from chemotherapeutic drug cytotoxicity. Cancer Res. 2001;61:577-581.
90. Richardson PG, Barlogie B, Berenson J, et al. A Phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med. 2003;348:2609-2617.
91. Orlowski RZ, Dees EC. The role of the ubiquitination-proteasome pathway in breast cancer: applying drugs that affect the ubiquitin-proteasome pathway to the therapy of breast cancer. Breast Cancer Res. 2003;5:1-7.
92. Adams J. Development of the proteasome inhibitor PS-341. Oncologist. 2002;7:9-16.
93. Nawrocki ST, Bruns CJ, Harbison MT, et al. Effects of the proteasome inhibitor PS-341 on apoptosis and angiogenesis in orthotopic human pancreatic tumor xenografts. Mol Cancer Ther. 2002;1:1243-1253.
94. Ling YH, Liebes L, Ng B, et al. PS-341, a novel proteasome inhibitor, induces Bcl-2 phosphorylation and cleavage in association with G2-M phase arrest and apoptosis. Mol Cancer Ther. 2002;1:841-849.
95. Saveanu L, Fruci D, van Endert P. Beyond the proteasome: trimming, degradation and generation of MHC Class I ligands by auxiliary proteases. Mol Immunol. 2002;39:203-215.
96. Drake CG, Pardoll DM. Tumor immunology - towards a paradigm of reciprocal research. Semin Cancer Biol. 2002;12:73-80.
97. Komlosh A, Momburg F, Weinschenk T, et al. A role for a novel luminal endoplasmic reticulum aminopeptidase in final trimming of 26S proteasome-generated major histocompatability complex Class I antigenic peptides. J Biol Chem. 2001;276:30050-30056.
98. Yang YA, Dukhanina O, Tang B, et al. Lifetime exposure to a soluble TGF-β antagonist protects mice against metastasis without adverse side effects. J Clin Invest. 2002;109:1607-1615.
99. Muraoka RS, Dumont N, Ritter CA, et al. Blockade of TGF-β inhibits mammary tumor cell viability, migration, and metastases. J Clin Invest. 2002;109:1551-1559.
100. Dumont N, Bakin AV, Arteaga CL. Autocrine transforming growth factor-β signaling mediates Smad-independent motility in human cancer cells. J Biol Chem. 2003;278:3275-3285.
101. Maggard M, Meng L, Ke B, Allen R, Devgan L, Imagawa DK. Antisense TGF-β2 immunotherapy for hepatocellular carcinoma: treatment in a rat tumor model. Ann Surg Oncol. 2001;8:32-37.
102. Benigni A, Zoja C, Corna D, et al. Add-on anti-TGF-β antibody to ACE inhibitor arrests progressive diabetic nephropathy in the rat. J Am Soc Nephrol. 2003;14:1816-1824.
103. Mead AL, Wong TT, Cordeiro MF, Anderson IK, Khaw PT. Evaluation of anti-TGF-β2 antibody as a new postoperative anti-scarring agent in glaucoma surgery. Invest Ophthalmol Vis Sci. 2003;44:3394-3401.
104. Ehrhart EJ, Segarini P, Tsang ML, Carroll AG, Barcellos-Hoff MH. Latent transforming growth factor β1 activation in situ: quantitative and functional evidence after low-dose gamma-irradiation. FASEB J. 1997;11:991-1002.
105. Arteaga CL, Hurd SD, Winnier AR, Johnson MD, Fendly BM, Forbes JT. Anti-transforming growth factor (TGF)-beta antibodies inhibit breast cancer cell tumorigenicity and increase mouse spleen natural killer cell activity. Implications for a possible role of tumor cell/host TGF-beta interactions in human breast cancer progression. J Clin Invest. 1993;92:2569-2576.
106. Laping NJ, Grygielko E, Mathur A, et al. Inhibition of transforming growth factor (TGF)-β1-induced extracellular matrix with a novel inhibitor of the TGF-β type I receptor kinase activity: SB-431542. Mol Pharmacol. 2002;62:58-64.
107. Marzo AL, Fitzpatrick DR, Robinson BW, Scott B. Antisense oligonucleotides specific for transforming growth factor β2 inhibit the growth of malignant mesothelioma both in vitro and in vivo. Cancer Res. 1997;57:3200-3207.