Paradoxical effects of cytokines in tumor immune surveillance and tumor immune escape

Cytokine and Growth Factor Reviews

Volumn 18, Issue 1-2, 2007, Pages 171-182

  Salazar Onfray, Flavio ^a   López, Mercedes N ^a,b   Mendoza Naranjo, Ariadna ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b HOSPITAL CLÍNICO UNIVERSIDAD DE CHILE   (Chile)

Author keywords

Antigen presenting cells; Cytokines; IL 10; Immunotherapy; Melanoma; Tumor; Tumor immunology

Indexed keywords

ALPHA INTERFERON; CYTOKINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR VACCINE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; RECOMBINANT ALPHA2B INTERFERON; RECOMBINANT CYTOKINE; RECOMBINANT INTERLEUKIN 10; RECOMBINANT INTERLEUKIN 1BETA; RECOMBINANT INTERLEUKIN 2; RECOMBINANT INTERLEUKIN 4; RECOMBINANT INTERLEUKIN 6; TRANSFORMING GROWTH FACTOR BETA;

ADJUVANT THERAPY; ANGIOGENESIS; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CANCER THERAPY; CLINICAL TRIAL; CLONING; CYTOTOXICITY; DRUG EFFECT; DRUG MEGADOSE; HUMAN; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOSURVEILLANCE; INFLAMMATORY CELL; INHIBITION KINETICS; LOW DRUG DOSE; LYMPHOCYTOPENIA; MELANOMA; MONOCYTOSIS; MULTIPLE CYCLE TREATMENT; NATURAL KILLER CELL; NEUTROPHILIA; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SIDE EFFECT; SINGLE DRUG DOSE; THROMBOCYTE COUNT; TUMOR ESCAPE; TUMOR GROWTH; TUMOR IMMUNITY; TUMOR IMMUNOLOGY;

ANIMALS; CYTOKINES; HUMANS; IMMUNITY, NATURAL; IMMUNOLOGIC SURVEILLANCE; KILLER CELLS, NATURAL; NEOPLASMS; OLIGOPEPTIDES; TUMOR ESCAPE;

EID: 33947110880     PISSN: 13596101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2007.01.015     Document Type: Article

References (106)

1. Burnet F.M. Cancer-a biological approach. BMJ 1 (1957) 841-847
2. Thomas L. In: Lawrence H.S. (Ed). Cellular and Humoral Aspects of the Hypersensitive States (1959), Hoeber-Harper, New York 529-532
3. Dunn G.P., Bruce A.T., Ikeda H., Old L.J., and Schreiber R.D. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 3 (2002) 991-998
4. Gallucci S., Lolkema M., and Matzinger P. Natural adjuvants: endogenous activators of dendritic cells. Nat Med 5 (1999) 1249-1255
5. Dranoff G. Cytokines in cancer pathogenesis and cancer therapy. Nat Rev Cancer 4 (2004) 11-22
6. Falcone M., and Sarvetnick N. Cytokines that regulate autoimmune responses. Curr Opin Immunol 11 (1999) 670-676
7. Bach E.A., Aguet M., and Schreiber R.D. The IFN gamma receptor: a paradigm for cytokine receptor signaling. Annu Rev Immunol 15 (1997) 563-591
8. Boehm U., Klamp T., Groot M., and Howard J.C. Cellular responses to interferon-gamma. Annu Rev Immunol 15 (1997) 749-795
9. Munder M., Mallo M., Eichmann K., and Modolell M. Murine macrophages secrete interferon gamma upon combined stimulation with interleukin (IL)-12 and IL-18: A novel pathway of autocrine macrophage activation. J Exp Med 187 (1998) 2103-2108
10. Harris D.P., Haynes L., Sayles P.C., et al. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat Immunol 1 (2000) 475-482
11. Janeway C.A., Travers P., Walport M., and Shlomchik M. Immunobiology (2001), Garland Publishing, New York 732
12. Ikeda H., Old L.J., and Schreiber R.D. The roles of IFN gamma in protection against tumor development and cancer immunoediting. Cytokine Growth Factor Rev 13 (2002) 95-109
13. Dighe A.S., Richards E., Old L.J., and Schreiber R.D. Enhanced in vivo growth and resistance to rejection of tumor cells expressing dominant negative IFN gamma receptors. Immunity 1 (1994) 447-456
14. Kaplan D.H., Shankaran V., Dighe A.S., et al. Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci USA 95 (1998) 7556-7561
15. Shankaran V., Ikeda H., Bruce A.T., et al. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410 (2001) 1107-1111
16. Street S.E., Trapani J.A., MacGregor D., and Smyth M.J. Suppression of lymphoma and epithelial malignancies effected by interferon gamma. J Exp Med 196 (2002) 129-134
17. Brunda M.J., Luistro L., Hendrzak J.A., Fountoulakis M., Garotta G., and Gately M.K. Role of interferon-gamma in mediating the antitumor efficacy of interleukin-12. J Immunother Emphasis Tumor Immunol 17 (1995) 71-77
18. Enzler T., Gillessen S., Manis J.P., et al. Deficiencies of GM-CSF and interferon gamma link inflammation and cancer. J Exp Med 197 (2003) 1213-1219
19. Yao L., Sgadari C., Furuke K., et al. Contribution of natural killer cells to inhibition of angiogenesis by interleukin-12. Blood 93 (1999) 1612-1621
20. Wolf S.F., Temple P.A., Kobayashi M., et al. Cloning of cDNA for natural killer cell stimulatory factor, a heterodimeric cytokine with multiple biologic effects on T and natural killer cells. J Immunol 146 (1991) 3074-3081
21. Manetti R., Parronchi P., Giudizi M.G., et al. Natural killer cell stimulatory factor (interleukin 12 [IL-12]) induces T helper type 1 (Th1)-specific immune responses and inhibits the development of IL-4-producing Th cells. J Exp Med 177 (1993) 1199-1204
22. Nastala C.L., Edington H.D., McKinney T.G., et al. Recombinant IL-12 administration induces tumor regression in association with IFN-gamma production. J Immunol 153 (1994) 1697-1706
23. Mu J., Zou J.P., Yamamoto N., et al. Administration of recombinant interleukin 12 prevents outgrowth of tumor cells metastasizing spontaneously to lung and lymph nodes. Cancer Res 55 (1995) 4404-4408
24. Dranoff G., Jaffee E., Lazenby A., et al. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc Natl Acad Sci USA 90 (1993) 3539-3543
25. Markowicz S., and Engleman E.G. Granulocyte-macrophage colony-stimulating factor promotes differentiation and survival of human peripheral blood dendritic cells in vitro. J Clin Invest 85 (1990) 955-961
26. Nathan C. Points of control in inflammation. Nature 420 (2002) 846-852
27. Coussens L.M., and Werb Z. Inflammation and cancer. Nature 420 (2002) 860-867
28. Balkwill F., and Mantovani A. Inflammation and cancer: back to Virchow?. Lancet 357 (2001) 539-545
29. O'Byrne K.J., and Dalgleish A.G. Chronic immune activation and inflammation as the cause of malignancy. Br J Cancer 85 (2001) 473-483
30. Balkwill F. Tumor necrosis factor or tumor promoting factor?. Cytokine Growth Factor Rev 13 (2002) 135-141
31. Huang C., Li J., Ma W.Y., and Dong Z. JNK activation is required for JB6 cell transformation induced by tumor necrosis factor-alpha but not by 12-O-tetradecanoylphorbol-13-acetate. J Biol Chem 274 (1999) 29672-29676
32. Pollard J.W. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 4 (2004) 71-78
33. Micheau O., and Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114 (2003) 181-190
34. Ogata A., Chauhan D., Teoh G., et al. IL-6 triggers cell growth via the Ras-dependent mitogen-activated protein kinase cascade. J Immunol 159 (1997) 2212-2221
35. Hodge D.R., Peng B., Cherry J.C., et al. Interleukin 6 supports the maintenance of p53 tumor suppressor gene promoter methylation. Cancer Res 65 11 (2005) 4673-4682
36. Yu C.Y., Wang L., Khaletskiy A., et al. STAT3 activation is required for interleukin-6 induced transformation in tumor-promotion sensitive mouse skin epithelial cells. Oncogene 21 (2002) 3949-3960
37. Mullen C.A., Coale M.M., Levy A.T., et al. Fibrosarcoma cells transduced with the IL-6 gene exhibit reduced tumorigenicity, increased immunogenicity, and decreased metastatic potential. Cancer Res 52 (1992) 6020-6024
38. Sun W.H., Kreisle R.A., Phillips A.W., et al. In vivo and in vitro characteristics of interleukin 6-transfected B16 melanoma cells. Cancer Res 52 (1992) 5412-5415
39. Khong H.T., and Restifo N.P. Natural selection of tumor variants in the generation of tumor escape phenotypes. Nat Immunol 3 (2002) 999-1005
40. Massague J. TGF-beta signal transduction. Annu Rev Biochem 67 (1998) 753-791
41. Letterio J.J., and Roberts A.B. Regulation of immune responses by TGF-beta. Annu Rev Inmunol 16 (1998) 137-161
42. Leveen P., Larsson J., Ehinger M., et al. Induced disruption of the transforming growth factor beta type II receptor gene in mice causes a lethal inflammatory disorder that is transplantable. Blood 100 (2002) 560-568
43. Dang H., Geiser A.G., Letterio J.J., Nakabayashi T., Kong L., Fernandes G., et al. SLE-like autoantibodies and Sjogren's syndrome-like lymphoproliferation in TGF-beta knockout mice. J Immunol 155 (1995) 3205-3212
44. Gorelick L., and Flavell R.A. Transforming growth factor-β in T cell biology. Nat Rev Immunol 2 (2002) 46-53
45. Sakaguchi S. Regulatory T cells in immune surveillance and treatment of cancer. Semin Cancer Biol 16 (2006) 115-123
46. Nishimura E., Sakihama T., Setoguchi R., et al. Induction of antigen-specific immunologic tolerance by in vivo and in vitro antigen-specific expansion of naturally arising Foxp3+CD25+CD4+ regulatory T cells. Int Immunol 16 (2004) 1189-1201
47. Lopez M., Aguilera R., Perez C., Mendoza-Naranjo A., Pereda C., Ramirez M., et al. The role of regulatory T lymphocytes in the induced immune response mediated by biological vaccines. Immunobiology 211 (2006) 127-136
48. Nomura T., and Sakaguchi S. Naturally arising CD25+CD4+ regulatory T cells in tumor immunity. Curr Top Microbiol Immunol 293 (2005) 287-302
49. Dudley M.E., Wunderlich J.R., Yang J.C., Sherry R.M., Topalian S.L., Restifo N.P., et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 23 (2005) 2346-2357
50. Li M.O., Sanjabi S., and Flavell R.A. Transforming growth factor-beta controls development, homeostasis, and tolerance of T cells by regulatory T cell-dependent and -independent mechanisms. Immunity 25 (2006) 455-471
51. Jarnicki A.G., Lysaght J., Todryk S., and Mills K.H. Suppression of antitumor immunity by IL-10 and TGF-beta-producing T cells infiltrating the growing tumor: influence of tumor environment on the induction of CD4+ and CD8+ regulatory T cells. J Immunol 177 (2006) 896-904
52. Veldhoen M., Hocking R.J., Atkins C.J., et al. TGF beta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24 (2006) 179-189
53. de Waal-Malefty R., Abrams J., Bennett J., Figdor C., and y de Vries J. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med 174 (1991) 1209-1220
54. Fiorentino D., Bond M., and y Mosmann T. Two types of mouse T helper cells. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med 170 (1989) 2080-2095
55. Matsuda M., Salazar F., Petersson M., Masucci G., Hansson J., Pisa P., et al. Interleukin-10 pre-treatment protects target cells from tumor- and allo-specific cytotoxic T-cells and down-regulates HLA class I expression. J Exp Med 180 (1994) 2371-2376
56. Salazar-Onfray F. Interleukin-10: a cytokine used by tumors to escape immunosurveillance. Med Oncol 16 (1999) 86-94
57. Chen W. Dendritic cells and (CD4+)CD25+ T regulatory cells: crosstalk between two professionals in immunity versus tolerance. Front Biosci 11 (2006) 1360-1370
58. Mills K.H. Regulatory T cells: Friend or for in immunity to infection?. Nat Rev Immunol 4 (2004) 841-855
59. Suffia I.J., Reckling S.K., Piccirillo C.A., Goldszmid R.S., and Belkaid Y. Infected site-restricted Foxp3+ natural regulatory T cells are specific for microbial antigens. J Exp Med 203 (2006) 777-788
60. Mocellin S., Marincola F.M., and Young H.A. Interleukin-10 and the immune response against cancer: a counterpoint. J Leuk Biol 78 (2005) 1043-1051
61. Pennline K.J., Roque-Gaffney E., and Monaham R. Recombinant human IL-10 prevents the onset of diabetes in the nonobese diabetic mouse. Clin Immunol Immunopathol 71 (1994) 169-175
62. Hill N., and Sarvertnick N. Cytokines: promoters and dampeners of autoimmunity. Curr Opin Immunol 14 (2002) 791-797
63. Rosenbaum J.T., and Angell E. Paradoxical effects of IL-10 in endotoxin-induced uveitis. J Immunol 155 (1995) 4090-4094
64. Zhang G.X., Xiao B.G., Yu L., van der Meide P.H., and Link H. Interleukin 10 aggravates experimental autoimmune myasthenia gravis through inducing Th2 and B cell response to AchR. J Neuroimmunol 113 (2001) 10-18
65. Ishida H., Muchamuel S.S., Sakaguchi S., Andrade S., Menon S., and Howard M. Continuous administration of anti-interleukin-10 antibodies delays the onset of autoimmunity in NZB/W FI mice. J Exp Med 179 (1994) 305-310
66. Gastle G., Abrams J., Nanus D., Osterkamp R., Silver J., Liu F., et al. Interleukin-10 production by human carcinoma cell lines and its relationship to interleukin-6 expression. Int J Cancer 55 (1993) 96
67. Huang M., Wang J., Lee P., Sharma S., Mao H., Meissner H., et al. Human non-small lung cancer cells express a type 2 cytokine pattern. Cancer Res 55 (1995) 3847
68. Kruger-Krasagakes S., Krasagakis K., Garbe C., Schmitt E., Huls C., Blankenstein T., et al. Expression of interleukin 10 in human melanoma. Br J Cancer 70 (1994) 1182
69. Gotlieb W.H., Abrams J.S., Watson J.M., Velu T.J., Berek J.S., and Martínez-Maza O. Presence of interleukin 10 (IL-10) in the ascites of patients with ovarian and other intra-abdominal cancers. Cytokine 4 (1992) 385
70. Pisa P., Halapi E., Pisa E., Gerdin E., Hising C., Bucht A., et al. Selective expression of interleukin 10, interferon-g and granulocyte-macrophage colony-stimulating factor in ovarian cancer biopsies. Proc Natl Acad Sci USA 89 (1992) 7708
71. Dummer W., Bastian B.C., Ernst N., Schanzle C., Schwaaf A., and Brocker E.B. Interleukin-10 production in malignant melanoma: preferential detection of IL-10-secreting tumor cells in metastatic lesions. Int J Cancer 66 (1996) 607
72. Yue F.Y., Dummer R., Geertsen R., Hofbauer G., Laine E., Manolio S., et al. Interleukin-10 is a growth factor for human melanoma cells and down-regulates HLA class-I, HLA class-II and ICAM-1 molecules. Int J Cancer 71 (1997) 630
73. Salazar-Onfray F., Petersson M., Franksson L., Matsuda M., Blankenstein T., Kärre K., et al. IL-10 converts mouse lymphoma cells to a CTL-resistant, NK sensitive phenotype with low but peptide-inducible MHC class I expression. J Immunol 154 (1995) 6291
74. Salazar-Onfray F., Charo J., Petersson M., Freland S., Noffz G., Qin Z., et al. Down-regulation of the expression and function of TAP in murine tumor cell lines expressing Interleukin-10. J Immunol 159 (1997) 3195
75. Zeidler R., Eissner G., Meissner P., Uebel S., Tampe R., Lazis S., et al. Downregulation of TAP1 in B lymphocytes by cellular and Epstein-Barr virus-encoded interleukin-10. Blood 90 (1997) 2390
76. Petersson M., Charo J., Salazar-Onfray F., Noffz G., Qin Z., Klein G., et al. Constitutive IL-10 production accounts for the high NK sensitivity, low MHC class I expression and poor TAP1/2 function in the prototype NK target YAC-1. J Immunol 161 (1998) 2099
77. Garcia-Hernandez M.L., Hernandez-Pando R., Gariglio P., and Berumen J. Interleukin-10 promotes B16-melanoma growth by inhibition of macrophage functions and induction of tumour and vascular cell proliferation. Immunology 105 (2002) 231
78. Giovarelli M., Musiani P., Modesti A., Dellabona P., Casorati G., Allione A., et al. Local release of IL-10 by transfected mouse mammary adenocarcinoma cells does not suppress but enhances anti tumor reaction and elicits a strong cytotoxic lymphocyte and antibody-dependent immune memory. J Immunol 155 (1995) 3112
79. Zheng L.M., Ojcius D.M., Garaud F., Roth C., Maxwell E., Li Z., et al. Interleukin-10 inhibits tumor metastasis through an NK cell-dependent mechanism. J Exp Med 184 (1996) 579-584
80. Kundu N., Beaty T.L., Jackson M.J., and Fulton A.M. Antimetastatic and antitumor activities of interleukin 10 in a murine model of breast cancer. J Natl Cancer Inst 88 (1996) 536-541
81. Kundu N., and Fulton A.M. Interleukin-10 inhibits tumor metastasis, downregulates MHC class I, and enhances NK lysis. Cell Immunol 180 (1997) 55-61
82. Richter G., Kruger-Krasagakes S., Hein G., Huls C., Schmitt E., Diamantstein T., et al. Interleukin 10 transfected into chinese hamster ovary cells prevents tumor growth and macrophage infiltration. Cancer Res 53 (1993) 4134
83. Hagenbaugh A., Sharma S., Dubinett S.M., Wei S.H.Y., Aranda R., Cheroutre H., et al. Altered immune responses in interleukin 10 transgenic mice. J Exp Med 185 (1997) 2101
84. Barth Jr. R.J., Coppola M.A., and Green W.R. In vivo effects of locally secreted IL-10 on the murine antitumor immune response. Ann Surg Oncol 3 (1996) 381-386
85. Kurte M., López M., Aguirre A., Escobar A., Aguillón J.C., Charo J., et al. A synthetic peptide homologous to the functional domain of human interleukin 10 downregulates the expression of the MHC class I alpha chain and TAP1/2 in human melanoma cells. J Immunol 173 (2004) 1731-1737
86. Veltri S., and Smith J.W. Interleukin 1 trials in cancer patients: a review of the toxicity, antitumor and hematopoietic effects. Stem Cells 14 (1996) 164-176
87. Abroun S., Ishikawa H., Tsuyama N., Liu S., Li F.J., Otsuyama K., et al. Receptor synergy of interleukin-6 (IL-6) and insulin-like growth factor-I in myeloma cells that highly express IL-6 receptor alpha. Blood 103 6 (2004) 2291-2298
88. Quesada J.R., Hersh E.M., Manning J., et al. Treatment of hairy cell leukemia with recombinant alfa-interferon. Blood 68 (1986) 493-497
89. Allan N.C., Richards S.M., and Shepherd P.C. UK Medical Research Council randomized, multicenter trial of interferon alfa n1 for chronic myeloid leukaemia: improved survival irrespective of cytogenetic response. Lancet 345 (1995) 1392-1397
90. Sertoli M.R., Bernego M.G., Ardizzoni A., et al. Phase II trial of recombinant alfa-2b interferon in the treatment of metastatic skin melanoma. Oncology 46 (1989) 96-98
91. Kirkwood J.M., Strawderman M.H., Ernstoff M.S., Smith T.J., Borden E.C., and Blum R.H. Interferon alfa-2b adjuvant therapy of high-risk resected cutaneous melanoma: the Eastern Cooperative Oncology Group Trial EST 1684. J Clin Oncol 14 (1996) 7-17
92. Rosenberg S.A., Yang Y.C., Topalian S.L., et al. Treatment of 283 consecutive patients with metastatic melanoma or renal cell cancer using high-dose bolus interleukin-2. JAMA 271 (1994) 907-913
93. Tourani J.M., Lucas V., Mayeur D., et al. Subcutaneous recombinant interleukin-2 (rIL-2) in outpatients with metastatic renal cell carcinoma. Results of a multicenter SCAPP1 trial. Ann Oncol 7 (1996) 525-528
94. Eager R., and Nemunaitis J. GM-CSF gene-transduced tumor vaccines. Mol Ther 12 (2005) 18-27
95. Lee P., Wang F., Kuniyoshi J., et al. Effects of interleukin-12 on the immune response to a multipeptide vaccine for resected metastatic melanoma. J Clin Oncol 19 (2001) 3836-3847
96. Huhn R.D., Radwanski E., O'Connell S.M., Sturgill M.G., Clarke L., Cody R.P., et al. Pharmacokinetics and immunomodulatory properties of intravenously administered recombinant human interleukin-10 in healthy volunteers. Blood 87 (1996) 699-705
97. Moore K., de Waal-Malefyt R., Coffman L., Mosmann T., and y O'Garra A. Interleukin-10 and Interleukin-10 receptor. Annu Rev Immunol 19 (2001) 683-765
98. Andersen S.R., Lambrecht L.J., Swan S.K., Cutler D.L., Radwanski E., Affrime M.B., et al. Disposition of recombinant human interleukin-10 in subjects with various degrees of renal function. J Clin Pharmacol 39 (1999) 1015-1020
99. Suzuki T., Tahara H., and Narula S. Viral interleukin 10 (IL-10), the human herpes virus 4 cellular IL-10 homologue, induces local anergy to allogeneic and syngeneic tumors. J Exp Med 182 (1995) 477-486
100. Fujii S., Shimizu K., Shimizu T., and Lotze M. Interleukin-10 promotes the maintenance of antitumor CD8(+) T-cell effector function in situ. Blood 98 (2001) 2143-2151
101. Segal B., Glass D., and Shevach E. Cutting edge: IL-10-producing CD4+ T cells mediate tumor rejection. J Immunol 168 (2002) 1-4
102. Escobar E., López M., Serrano A., Ramirez M., Pérez C., Aguirre A., et al. Dendritic cell immunizations alone or combined with low doses interleukin-2 induce specific immune responses in melanoma patients. Clin Exp Immunol 142 (2005) 555-568
103. Gatenby R.A., Gawlinski E.T., Gmitro A.F., Kaylor B., and Gillies R.J. Acid-mediated tumor invasion: a multidisciplinary study. Cancer Res 66 (2006) 5216-5223
104. Rabinovich GA, Gabrilovich D, Sotomayor EM. Immunosuppressive strategies that are mediated by tumor cells. Annu. Rev. Immunol. 25 (doi:10.1146/annurev.immunol.25.022106.141609), Epub ahead of print.
105. Andreola G., Rivoltini L., Castelli C., Huber V., Perego P., Deho P., et al. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J Exp Med 195 10 (2002) 1303-1316
106. Lugini L., Matarrese P., Tinari A., Lozupone F., Federici C., Iessi E., et al. Cannibalism of live lymphocytes by human metastatic but not primary melanoma cells. Cancer Res 66 (2006) 3629-3638