Interleukin 10 decreases MICA expression on melanoma cell surface

Immunology and Cell Biology

Volumn 89, Issue 3, 2011, Pages 447-457

  Serrano, Antonio E ^a   Menares Castillo, Evelyn ^a   Garrido Tapia, MacArena ^a   Ribeiro, Carolina Hager ^a   Hernández, Carolina J ^a   Mendoza Naranjo, Ariadna ^b   Gatica Andrades, Marcela ^a   Valenzuela Diaz, Rodrigo ^a   Z̃iga, Roberto ^a   López, Mercedes N ^a   Salazar Onfray, Flavio ^a   Aguillón, Juan Carlos ^a   Molina, María Carmen ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

immune evasion; interleukin 10; melanoma cells; natural killer cell; NKG2D ligands

Indexed keywords

INTERLEUKIN 10 RECEPTOR; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MESSENGER RNA; NATURAL KILLER CELL RECEPTOR NKG2D; RECOMBINANT INTERLEUKIN 10; STAT3 PROTEIN;

ARTICLE; CELL ACTIVATION; CELL ISOLATION; CELL SURFACE; CELL THERAPY; CYTOTOXICITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOMODULATION; LYSIS; MAJOR HISTOCOMPATIBILITY COMPLEX; MELANOMA CELL; RECEPTOR BLOCKING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; INTERLEUKIN-10; K562 CELLS; KILLER CELLS, NATURAL; LIGANDS; LYMPHOCYTE ACTIVATION; MELANOMA; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; RECEPTORS, INTERLEUKIN-10;

EID: 79952817937     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2010.100     Document Type: Article

References (70)

1. Houchins JP, Yabe T, McSherry C, Bach FH. DNA sequence analysis of NKG2, a family of related cDNA clones encoding type II integral membrane proteins on human natural killer cells. J Exp Med 1991; 173: 1017-1020.
2. Groh V, Wu J, Yee C, Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 2002; 419: 734-738. (Pubitemid 35177960)
3. Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL et al. Activation of NK cells and Tcells by NKG2D, a receptorforstress-inducible MICA. Science 1999; 285: 727-729.
4. Bahram S, Bresnahan M, Geraghty DE, Spies T. A second lineage of mammalian major histocompatibility complex class I genes. Proc Natl Acad Sci USA 1994; 91: 6259-6263. (Pubitemid 24200639)
5. Hayakawa Y, Smyth MJ. NKG2D and cytotoxic effector function in tumor immune surveillance. Semin Immunol 2006; 18: 176-185. (Pubitemid 43817565)
6. Cosman D, Mullberg J, Sutherland CL, Chin W, Armitage R, Fanslow W et al. ULBPs, novel MHC class I-related molecules, bindto CMV glycoprote in UL16 and stimulate NK cytotoxicitythrough the NKG2D receptor. Immunity 2001; 14: 123-133. (Pubitemid 32206515)
7. Radosavljevic M, Cuillerier B, Wilson MJ, Clement O, Wicker S, Gilfillan S et al. A cluster of ten novel MHC class I related genes on human chromosome 6q24.2-q25.3. Genomics 2002; 79: 114-123.
8. Nausch N, Cerwenka A. NKG2D ligands in tumor immunity. Oncogene 2008; 27: 5944-5958.
9. Skov S, Pedersen MT, Andresen L, Straten PT, Woetmann A, Odum N. Cancer cells become susceptible to natural killer cell killing after exposure to histone deacetylase inhibitors due to glycogen synthase kinase-3-dependent expression of MHC class I-relatedchain AandB. Cancer Res 2005; 65: 11136-11145. (Pubitemid 41713385)
10. Caligiuri MA. Human natural killer cells. Blood 2008; 112: 461-469.
11. Vales-Gomez M, Chisholm SE, Cassady-Cain RL, Roda-Navarro P, Reyburn HT. Selec-tive induction of expression of a ligand for the NKG2D receptor by proteasome inhibitors. Cancer Res 2008; 68: 1546-1554. (Pubitemid 351346864)
12. Bryceson YT, Ljunggren HG. Tumor cell recognition by the NK cell activating receptor NKG2D. Eur J Immunol 2008; 38: 2957-2961.
13. Guerra N, Tan YX, Joncker NT, Choy A, Gallardo F, Xiong N et al. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 2008; 28: 571-580.
14. Unni AM, Bondar T, Medzhitov R. Intrinsic sensor of oncogenic transformation induces a signal for innate immunosurveillance. Proc Natl Acad Sci USA 2008; 105: 1686-1691. (Pubitemid 351346575)
15. Salih HR, Rammensee HG, Steinle A. Cuttingedge: down-regulation of MICA on human tumors by proteolytic shedding. J Immunol 2002; 169: 4098-4102. (Pubitemid 35178177)
16. Raffaghello L, Prigione I, Airoldi I, Camoriano M, Levreri I, Gambini C et al. Down-regulation and/or release of NKG2D ligands as immune evasion strategy of human neuroblastoma. Neoplasia 2004; 6: 558-568. (Pubitemid 39411093)
17. Waldhauer I, Goehlsdorf D, Gieseke F, Weinschenk T, Wittenbrink M, Ludwig A et al. Tumor-associated MICA is shed by ADAM proteases. Cancer Res 2008; 68: 6368-6376.
18. Waldhauer I, Steinle A. Proteolytic release of soluble UL16-binding protein 2 from tumor cells. Cancer Res 2006; 66: 2520-2526.
19. Coudert JD, Zimmer J, Tomasello E, Cebecauer M, Colonna M, Vivier E et al. Altered NKG2Dfunction in NK cells induced bychronic exposureto NKG2D ligand-expressing tumorcells. Blood 2005; 106: 1711-1717. (Pubitemid 41208585)
20. Oppenheim DE, Roberts SJ, Clarke SL, Filler R, Lewis JM, Tigelaar RE et al. Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat Immunol 2005; 6: 928-937. (Pubitemid 43090448)
21. Wiemann K, Mittrucker HW, Feger U, Welte SA, Yokoyama WM, Spies T et al. Systemic NKG2D down-regulation impairs NK and CD8 T cell responses in vivo. J Immunol 2005; 175: 720-729. (Pubitemid 41094952)
22. Fuertes MB, Girart MV, Molinero LL, Domaica CI, Rossi LE, Barrio MM et al. Intracellular retention of the NKG2D ligand MHC class I chain-related gene A in human melanomas confers immune privilege and prevents NK cell-mediated cytotoxi-city. J Immunol 2008; 180: 4606-4614.
23. Zhang C, Niu J, Zhang J, Wang Y, Zhou Z, Tian Z. Opposing effects of interferon-alpha and interferon-gamma on the expression of major histocompatibility complex class I chain-related A in tumors. Cancer Sci 2008; 99: 1279-1286. (Pubitemid 351676642)
24. Schwinn N, Vokhminova D, Sucker A, Textor S, Striegel S, Moll I et al. Interferon-gamma down-regulates NKG2D ligand expression and impairs the NKG2D-mediated cytolysis of MHC class I-deficient melanoma by natural killer cells. Int J Cancer 2009; 124: 1594-1604.
25. Eisele G, Wischhusen J, Mittelbronn M, Meyermann R, Waldhauer I, Steinle A et al. TGF-beta and metalloproteinases differentiallysuppress NKG2D ligand surface expres-sion on malignant glioma cells. Brain 2006; 129: 2416-2425. (Pubitemid 44522126)
26. Salazar-Onfray F. Interleukin-10: a cytokine used by tumors to escape immunosurveil-lance. Med Oncol 1999; 16: 86-94. (Pubitemid 29349854)
27. de Waal Malefyt R, Haanen J, Spits H, Roncarolo MG, te Velde A, Figdor C et al. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human Tcell proliferation by diminishing the antigen-presenting capacity of monocytes via down-regulation of class II major histocompatibility complex expression. J Exp Med 1991; 174: 915-924.
28. Matsuda M, Salazar F, Petersson M, Masucci G, Hansson J, Pisa P et al. Interleukin 10 pretreatment protects target cells from tumor-and allo-specific cytotoxic T cells and downregulates HLA class I expression. J Exp Med 1994; 180: 2371-2376.
29. Gastl GA, Abrams JS, Nanus DM, Oosterkamp 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 1993; 55: 96-101. (Pubitemid 23261713)
30. Kruger-Krasagakes S, Krasagakis K, Garbe C, Schmitt E, Huls C, Blankenstein Tet al. Expression of interleukin 10 in human melanoma. Br J Cancer 1994; 70: 1182-1185. (Pubitemid 24358959)
31. Fortis C, Foppoli M, Gianotti L, Galli L, Citterio G, Consogno G et al. Increased interleukin-10 serum levels in patientswith solidtumours. Cancer Lett 1996; 104: 1-5. (Pubitemid 26154004)
32. Weiss E, Mamelak AJ, La Morgia S, Wang B, Feliciani C, Tulli A et al. The role of interleukin 10 in the pathogenesisand potential treatment of skin diseases. J Am Acad Dermatol 2004; 50: 657-675; quiz 676-678.
33. Hagenbaugh A, Sharma S, Dubinett SM, Wei SH, Aranda R, Cheroutre H et al. Altered immune responses in interleukin 10 transgenic mice. J Exp Med 1997; 185: 2101-2110. (Pubitemid 27265994)
34. Dummer W, Bastian BC, Ernst N, Schanzle C, Schwaaf A, Brocker EB. Interleukin-10 production in malignant melanoma: preferential detection of IL-10-secreting tumor cells in metastatic lesions. Int J Cancer 1996; 66: 607-610. (Pubitemid 26197925)
35. Maccalli C, Nonaka D, Piris A, Pende D, Rivoltini L, Castelli C et al. NKG2D-mediated antitumor activity bytumor-infiltrating lymphocytes and antigen-specific T-cell clones isolated from melanoma patients. Clin Cancer Res 2007; 13: 7459-7468.
36. Pende D, Rivera P, Marcenaro S, Chang CC, Biassoni R, Conte R et al. Major histocompatibility complex class I-related chain A and UL16-binding protein expres-sion on tumor cell lines of different histotypes: analysis of tumor susceptibility to NKG2D-dependent natural killercell cytotoxicity. Cancer Res 2002; 62: 6178-6186. (Pubitemid 35244469)
37. Vetter CS, Lieb W, Brocker EB, Becker JC. Lossof nonclassical MHC molecules MIC-A/B expression during progression of uveal melanoma. Br J Cancer 2004; 91: 1495-1499. (Pubitemid 39486354)
38. Petersson M, Charo J, Salazar-Onfray F, Noffz G, Mohaupt M, Qin Z et al. Constitutive IL-10 production accounts for the high N Ksensitivity, low MHC class I expression, and poortransporter associatedwith antigen processing (TAP)-1/2 function in the prototype NK target YAC-1. J Immunol 1998; 161: 2099-2105. (Pubitemid 28397018)
39. Liu Y, de Waal Malefyt R, Briere F, Parham C, Bridon JM, Banchereau J et al. The EBV IL-10 homologue is a selective agonist with impaired bindingto the IL-10 receptor. J Immunol 1997; 158: 604-613. (Pubitemid 127492636)
40. Wehinger J, Gouilleux F, Groner B, Finke J, Mertelsmann R, Weber-Nordt RM. IL-10 induces DNA binding activity of threeSTAT proteins (Stat1, Stat3, and Stat5) andtheir distinct combinatorial assembly in the promoters of selected genes. FEBS Lett 1996; 394: 365-370. (Pubitemid 26341476)
41. Bryceson YT, March ME, Barber DF, Ljunggren HG, Long EO. Cytolytic granule polarization and degranulation controlled by different receptors in resting NK cells. J Exp Med 2005; 202: 1001-1012. (Pubitemid 41396899)
42. Rubio V, Stuge TB, Singh N, Betts MR, Weber JS, Roederer M et al. Ex vivo identification, isolation and analysis of tumor-cytolytic T cells. Nat Med 2003; 9: 1377-1382. (Pubitemid 37466186)
43. Wolint P, Betts MR, Koup RA, Oxenius A. Immediate cytotoxicity but not degranulation distinguishes effector and memory subsets of CD8+ T cells. J Exp Med 2004; 199: 925-936. (Pubitemid 38481084)
44. Stern-Ginossar N, Gur C, Biton M, Horwitz E, Elboim M, Stanietsky N et al. Human microRNAs regulate stress-induced immune responses mediated by the receptor NKG2D. Nat Immunol 2008; 9: 1065-1073.
45. Spies T. Regulation of NKG2D ligands: a purposeful but delicate affair. Nat Immunol 2008; 9: 1013-1015.
46. Yadav D, Ngolab J, Lim RS, Krishnamurthy S, Bui JD. Cuttingedge: down-regulation of MHC class I-related chain A on tumor cells by IFN-gamma-induced microRNA. J Immunol 2009; 182: 39-43.
47. Venkataraman GM, Suciu D, Groh V, Boss JM, Spies T. Promoter regionarchitectureand transcriptional regulation of the genes for the MHC class I-related chain A and B ligands of NKG2D. J Immunol 2007; 178: 961-969. (Pubitemid 46095169)
48. Eagle RA, Traherne JA, Ashiru O, Wills MR, Trowsdale J. Regulation of NKG2D ligand geneexpression. Hum Immunol 2006; 67: 159-169.
49. Aguera-Gonzalez S, Boutet P, Reyburn HT, Vales-Gomez M. Brief residence at the plasma membrane of the MHC class I-related chain B is due to clathrin-mediated cholesterol-dependentendocytosis and shedding. J Immunol 2009; 182: 4800-4808.
50. Kurte M, Lopez M, Aguirre A, Escobar A, Aguillon JC, Charo J et al. Asynthetic peptide homologous to functional domain of human IL-10 down-regulates expression of MHC class I and transporter associated with antigen processing 1/2 in human melanoma cells. J Immunol 2004; 173: 1731-1737. (Pubitemid 38971604)
51. Lanier LL. Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol 2008; 9: 495-502. (Pubitemid 351560518)
52. Espinoza JL, Takami A, Onizuka M, Sao H, Akiyama H, Miyamura K et al. NKG2D gene polymorphism has a significant impact on transplant outcomes after HLA-fully-matched unrelated bone marrow transplantation for standard risk hematologic malig-nancies. Haematologica 2009; 94: 1427-1434.
53. Kabalak G, Thomas RM, Martin J, Ortego-Centeno N, Jimenez-Alonso J, de Ramon E et al. Association of an NKG2D genevariantwith systemic lupus erythematosus in two populations. Hum Immunol 2010; 71: 74-78.
54. Alter G, Malenfant JM, Altfeld M. CD107a as a functional marker for the identification of natural killer cell activity. J Immunol Methods 2004; 294: 15-22. (Pubitemid 39626587)
55. Fauriat C, Long EO, Ljunggren HG, Bryceson YT. Regulation of human NK-cell cytokine and chemokine production bytarget cell recognition. Blood 2010; 115: 2167-2176.
56. Carrega P, Pezzino G, Queirolo P, Bonaccorsi I, Falco M, Vita G et al. Susceptibility of human melanoma cells to autologous natural killer (NK) cell killing: HLA-related effector mechanisms and role of unlicensed NK cells. PLoS One 2009; 4: e 8132.
57. Anfossi N, Andre P, Guia S, Falk CS, Roetynck S, Stewart CA et al. Human NK cell education by inhibitory receptors for MHC class I. Immunity 2006; 25: 331-342. (Pubitemid 44224147)
58. Lakshmikanth T, Burke S, Ali TH, Kimpfler S, Ursini F, Ruggeri L et al. NCRs and DNAM-1 mediate NK cell recognition and lysis of human and mouse melanoma cell lines in vitro and in vivo. J Clin Invest 2009; 119: 1251-1263.
59. El-Sherbiny YM, Meade JL, Holmes TD, McGonagle D, Mackie SL, Morgan AW et al. The requirement for DNAM-1, NKG2D, and NKp46 in the natural killer cell-mediated killing of myeloma cells. Cancer Res 2007; 67: 8444-8449. (Pubitemid 47437416)
60. Andre P, Castriconi R, Espeli M, Anfossi N, Juarez T, Hue S et al. Comparativeanalysis of human NK cell activation induced by NKG2D and natural cytotoxicity receptors. Eur J Immunol 2004; 34: 961-971. (Pubitemid 39255974)
61. Friese MA, Wischhusen J, Wick W, Weiler M, Eisele G, Steinle A et al. RNA interference targeting transforming growth factor-beta enhances NKG2D-mediated antiglioma immune response, inhibits glioma cell migration and invasiveness, and abrogates tumorigenicity in vivo. Cancer Res 2004; 64: 7596-7603. (Pubitemid 39372105)
62. Lee JC, Lee KM, Kim DW, Heo DS. Elevated TGF-beta1 secretion and down-modulation of NKG2D underlies impaired NK cytotoxicity in cancer patients. J Immunol 2004; 172:7335-7340. (Pubitemid 38747593)
63. Kaiser BK, Yim D, Chow IT, Gonzalez S, Dai Z, Mann HH et al. Disulphide-isomerase-enabled sheddingoftumour-associated NKG2D ligands. Nature 2007; 447: 482-486.
64. Moore KW, Vieira P, Fiorentino DF, Trounstine ML, Khan TA, Mosmann TR. Homologyof cytokine synthesis inhibitory factor (IL-10) to the Epstein-Barr virus gene BCRFI. Science 1990; 248: 1230-1234.
65. Zdanov A, Schalk-Hihi C, Menon S, Moore KW, Wlodawer A. Crystal structure of Epstein-Barr virus protein BCRF1, a homolog of cellular interleukin-10. J Mol Biol 1997; 268: 460-467. (Pubitemid 27208067)
66. Kortylewski M, Jove R, Yu H. Targeting STAT3 affects melanoma on multiple fronts. Cancer Metast Rev 2005; 24: 315-327. (Pubitemid 40922802)
67. Bogenrieder T, Herlyn M. Axis of evil: molecular mechanisms of cancer metastasis. Oncogene 2003; 22: 6524-6536. (Pubitemid 37372332)
68. Xie TX, Wei D, Liu M, Gao AC, Ali-Osman F, Sawaya R et al. Stat3 activation regulates the expression of matrix metalloproteinase-2 and tumor invasion and metastasis. Oncogene 2004; 23: 3550-3560. (Pubitemid 38658421)
69. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162: 156-159. (Pubitemid 17064313)
70. Brunner KT, Mauel J, Cerottini JC, Chapuis B. Quantitative assay of the lytic action of immune lymphoid cells on 51-Cr-labelled allogeneic target cells in vitro; inhibition by isoantibodyandbydrugs. Immunology 1968; 14: 181-196.