CD69 on CD56+ NK cells and response to chemoimmunotherapy in metastatic melanoma

European Journal of Clinical Investigation

Volumn 37, Issue 11, 2007, Pages 887-896

  Konjevic G ^a,b   Jovic V ^a   Vuletic A ^a   Radulovic S ^a   Jelic S ^a   Spuzic I ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b INSTITUTE FOR ONCOLOGY AND RADIOLOGY OF SERBIA   (Serbia)

Author keywords

13 cis retinoic acid; CD69; Dacarbazine; Interferon ; Melanoma; NK cells

Indexed keywords

DACARBAZINE; ISOTRETINOIN; RECOMBINANT ALPHA2A INTERFERON;

ADULT; ARTICLE; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; FOLLOW UP; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MALE; MELANOMA; NATURAL KILLER CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TREATMENT OUTCOME; UPREGULATION;

ADULT; AGED; ANTIGENS, CD; ANTIGENS, CD56; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CASE-CONTROL STUDIES; DACARBAZINE; FEMALE; HUMANS; IMMUNOTHERAPY; INTERFERON ALFA-2A; INTERFERON REGULATORY FACTOR-1; KILLER CELLS, NATURAL; MALE; MELANOMA; MIDDLE AGED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SKIN NEOPLASMS; TRETINOIN;

EID: 35648973297     PISSN: 00142972     EISSN: 13652362     Source Type: Journal    
DOI: 10.1111/j.1365-2362.2007.01873.x     Document Type: Article

References (63)

1. Plummer ER, Middleton MR, Jones C, Olsen A, Hickson I, McHugh P et al. Temozolomide pharmacodynamics in patients with metastatic melanoma: DNA damage and activity of repair enzymes O6-alkylguanine alkyltransferase and poly (ADP-ribose) polymerase-1. Clin Cancer Res 2005 11 : 3402 9.
2. Bajetta E, Di Leo A, Zampino MG, Sertoli MR, Comella G, Barduagni M et al. Multicenter randomized trial of dacarbazine alone or in combination with two different doses and schedules of interferon alfa-2a in the treatment of advanced melanoma. J Clin Oncol 1994 12 : 806 11.
3. Legha SS, Ring S, Eton O, Bedikian A, Buzaid AC, Plager C et al. Development of a biochemotherapy regimen with concurrent administration of cisplatin, vinblastine, dacarbazine, interferon alfa, and interleukin-2 for patients with metastatic melanoma. J Clin Oncol 1998 16 : 1752 9.
4. Atkins MB. Immunotherapy and experimental approaches for metastatic melanoma. Hematol Oncol Clin North Am 1998 12 : 877 902.
5. Agarwala SS, Kirkwood JM. Interferons in the therapy of solid tumors. Oncology 1994 51 : 129 36.
6. Tarhini AA, Agarwala SS. Interleukin-2 for the treatment of melanoma. Curr Opin Invest Drugs 2005 6 : 1234 9.
7. Konjević G, Jović V, Jurišić V, Jelić S, Radulović S, Spužić I. IL-2-mediated augmentation of NK-cell activity and activation antigen expression on NK- and T-cell subsets in patients with metastatic melanoma treated with interferon-alpha and DTIC. Clin Exp Metastasis 2003 20 : 647 55.
8. Weber RW, O'Day S, Rose M, Deck R, Ames P, Good J et al. Low-dose outpatient chemobiotherapy with temozolomide, granulocyte-macrophage colony stimulating factor, interferon-alpha2b, and recombinant interleukin-2 for the treatment of metastatic melanoma. J Clin Oncol 2005 23 : 8992 9000.
9. Thyrell L, Hjortsberg L, Arulampalam V, Panaretakis T, Uhles S, Dagnell M et al. Interferon alpha-induced apoptosis in tumor cells is mediated through the phosphoinositide 3-kinase/mammalian target of rapamycin signaling pathway. J Biol Chem 2004 279 : 24152 62.
10. Bremers AJ, Parmiani G. Immunology and immunotherapy of human cancer: present concepts and clinical developments. Crit Rev Oncol Hematol 2000 34 : 1 25.
11. Tompkins WA. Immunomodulation and therapeutic effects of the oral use of interferon-alpha: mechanism of action. J Interferon Cytokine Res 1999 19 : 817 28.
12. Au WC, Moore PA, Lowther W, Juang YT, Pitha PM. Identification of a member of the interferon regulatory factor family that binds to the interferon-stimulated response element and activates expression of interferon-induced genes. Proc Natl Acad Sci USA 1995 92 : 11657 61.
13. Pelicano L, Li F, Schindler C, Chelbi-Alix MK. Retinoic acid enhances the expression of interferon-induced proteins: evidence for multiple mechanisms of action. Oncogene 1997 15 : 2349 59.
14. Sidell N, Famatiga E, Shau H, Golub SH. Immunological aspects of retinoids in humans. III. Effects of retinoic acid on the natural killing of tumor cells. J Biol Response Mod 1985 4 : 240 50.
15. Nagy L, Thomazy VA, Heyman RA, Davies PJ. Retinoid-induced apoptosis in normal and neoplastic tissues. Cell Death Differ 1998 5 : 11 9.
16. Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol 2001 22 : 633 40.
17. Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Ann Rev Immunol 1999 17 : 189 220.
18. Diefenbach A, Raulet D. The innate immune response to tumors and its role in the induction of T-cell immunity. Immunol Rev 2002 188 : 9 21.
19. Konjevic G, Jurisic V, Banicevic B, Spuzic I. The difference in NK-cell activity between patients with non-Hodgkin's lymphomas and Hodgkin's disease. Br J Haematol 1999 104 : 144 51.
20. Jacobs R, Hintzen G, Kemper A, Beul K, Kempf S, Behrens G et al. CD56 bright cells differ in their KIR repertoire and cytotoxic features from CD56dim NK cells. Eur J Immunol 2001 31 : 3121 7.
21. Yacyshyn MB, Poppema S, Berg A, MacLean GD, Reddish MA, Meikle A et al. CD69+ and HLA-DR+ activation antigens on peripheral blood lymphocytes populations in metastatic breast and ovarian cancer patients: correlation with survival following active specific immunotherapy. Int J Cancer 1995 61 : 470 4.
22. Pisegna S, Zingoni A, Pirozzi G, Cinque B, Cifone MG, Morrone S et al. Src-Dependent Syk Activation controls CD69-mediated signaling and function on human NK cells. J Immunol 2002 169 : 68 74.
23. Motzer RJ, Murphy BA, Bacik J, Schwartz LH, Nanus DM, Mariani T et al. Phase III trial of interferon alfa-2a with or without 13-cis-retinoic acid for patients with advanced renal cell carcinoma. J Clin Oncol 2000 18 : 2972 80.
24. Shin DM, Khuri FR, Murphy B, Garden AS, Clayman G, Francisco M et al. Combined interferon-alfa, 13-cis-retinoic acid, and alpha-tocopherol in locally advanced head and neck squamous cell carcinoma: novel bioadjuvant phase II trial. J Clin Oncol 2001 1 : 3010 7.
25. Rosenthal MA, Oratz R. Phase II clinical trial of recombinant alpha 2b interferon and 13 cis retinoic acid in patients with metastatic melanoma. Am J Clin Oncol 1998 21 : 352 4.
26. Sondak VK, Liu PY, Tuthill RJ, Kempf RA, Unger JM, Sosman JA et al. A phase II evaluation of all-trans-retinoic acid plus interferon alfa-2a in stage IV melanoma: a Southwest Oncology Group study. Cancer J Sci Am 1999 5 : 41 7.
27. Triozzi PL, Walker MJ, Pellegrini AE, Dayton MA. Isotretinoin and recombinant interferon alfa-2a therapy of metastatic malignant melanoma. Cancer Invest 1996 14 : 293 8.
28. Hernberg M, Muhonen T, Turunen JP, Hahka-Kemppinen M, Pyrhonen S. The CD4+/CD8+ ratio as a prognostic factor in patients treated with chemo-immunotherapy with metastatic melanoma. J Clin Oncol 1996 14 : 1690 6.
29. Jovic V, Konjevic G, Radulovic S, Jelic S, Spuzic I. Impaired perforin-dependent NK cell cytotoxicity and proliferative activity of peripheral blood T cells is associated with metastatic melanoma. Tumori 2001 87 : 324 9.
30. Jackson A, Warner N. Preparation, staining and analysis by flow cytometry of peripheral blood leukocytes. In : Rose N, Friedman H, Fahey J, editors. Manual of Clinical Lab Immunology, 3rd edn. Washington DC : American Society for Microbiology 1986. pp. 226 35.
31. Brown RL, Ortaldo JR, Griffith RL, Blanca I, Rabin H. The proliferation and function of human mononuclear leukocytes and natural killer cells in serum-free medium. J Immunol Meth 1985 81 : 207 14.
32. Eggermont AM, Kirkwood JM. Re-evaluating the role of dacarbazine in metastatic melanoma: what have we learned in 30 years? Eur J Cancer 2004 40 : 1825 36.
33. Huncharek M, Caubet JF, McGarry R. Single-agent DTIC versus combination chemotherapy with or without immunotherapy in metastatic melanoma: a meta-analysis of 3273 patients from 20 randomized trials. Melanoma Res 2001 11 : 75 81.
34. Robertson MJ, Ritz J. Biology and clinical relevance of human natural killer cells. Blood 1990 76 : 2421 38.
35. Sibbitt WL Jr., Bankhurst AD, Jumonville AJ, Saiki JH, Saiers JH, Doberneck RC. Defects in natural killer cell activity and interferon response in human lung carcinoma and malignant melanoma. Cancer Res 1984 44 : 852 6.
36. Konjević G, Jović V, Radulović S, Jelić S, Spužić I. Immunomodulating and clinical response of patients with metastatic melanoma receiving two chemoimmunotherapy regimens. Immunology, Medimond S.r.1. International Proceedings. Bologna (Italy) : Monduzzi editore 2004. pp. 449 52.
37. Krasagakis K, Tholke D, Farthmann B, Eberle J, Mansmann U, Orfanos CE. Elevated plasma levels of transforming growth factor (TGF)-beta1 and TGF-beta2 in patients with disseminated malignant melanoma. Br J Cancer 1998 77 : 1492 4.
38. Knoefel B, Nuske K, Steiner T, Junker K, Kosmehl H, Rebstock K et al. Renal cell carcinomas produce IL-6, IL-10, IL-11, and TGF-beta 1 in primary cultures and modulate T lymphocyte blast transformation. J Interferon Cytokine Res 1997 17 : 95 102.
39. Konjevic G, Spuzic I. Evaluation of different effects of sera of breast cancer patients on the activity of natural killer cells. J Clin Lab Immunol 1992 38 : 83 93.
40. Ferlazzo G, Thomas D, Lin SL, Goodman K, Morandi B, Muller WA et al. The abundant NK cells in human secondary lymphoid tissues require activation to express killer cell Ig-like receptors and become cytolytic. J Immunol 2004 172 : 1455 62.
41. Jewett A, Cavalcanti M, Bonavida B. Pivotal role of endogenous TNF-alpha in the induction of functional inactivation and apoptosis in NK cells. J Immunol 1997 159 : 4815 22.
42. Cavalcanti M, Jewett A, Bonavida B. Irreversible cancer cell-induced functional anergy and apoptosis in resting and activated NK cells. Int J Oncol 1999 14 : 361 6.
43. Konjević G, Schlesinger B, Cheng L, Olsen KJ, Podack ER, Spužić I. Analysis of perforin expression in human peripheral blood lymphocytes, CD56+ natural killer cell subsets and its induction by interleukin-2. Immunol Invest 1995 24 : 449 507.
44. Whiteside TI, Herberman RB. The role of natural killer cells in immune surveillance of cancer. Curr Opin Immunol 1995 7 : 704 10.
45. Fehniger TA, Cooper MA, Nuovo GJ, Cella M, Facchetti F, Colonna M et al. CD56 bright natural killer cells are present in human lymph nodes and are activated by T cell-derived IL-2: a potential new link between adaptive and innate immunity. Blood 2003 101 : 3052 7.
46. Cooper MA, Fehniger TA, Turner SC, Chen KS, Ghaheri BA, Ghayur T et al. Human natural killer cells: a unique innate immunoregulatory role for the CD56 (bright) subset. Blood 2001 97 : 3146 51.
47. Jacobs R, Hintzen G, Kemper A, Beul K, Kempf S, Behrens G et al. CD56bright cells differ in their KIR repertoire and cytotoxic features from CD56dim NK cells. Eur J Immunol 2001 31 : 3121 7.
48. Verhagen A, Mackay IR, Rowley M, Tymms M. Comparison of augmentation of human natural killer cell cytotoxicity by interferon-alpha subtypes. Nat Immun Cell Growth Regul 1990 9 : 325 33.
49. Song H, Hur JD, Kim K-E, Park H, Kim T, Kim C-W et al. IL-12/IL-18 prevent the down-modulation of NKG2D by TGF-β in NK cells via the c-Jun N-terminal kinase (JNK) pathway. Cell Immunol 2006 242 : 39 45.
50. Konjevic G, Mirjacic Martinovic K, Vuletic A, Jovic V, Jurisic V, Babovic N et al. Low expression of CD161 and NKG2D activating NK receptor is associated with impaired NK cell cytotoxicity in metastatic melanoma patients. Clin Exp Metastasis 2007 24 (1 1 11.
51. Bauernhofer T, Kuss I, Henderson B, Baum AS, Whiteside TL. Preferential apoptosis of CD56dim natural killer cell subset in patients with cancer. Eur J Immunol 2003 33 : 119 24.
52. Mogensen KE, Lewerenz M, Reboul J, Lutfalla G, Uze G. The type I interferon receptor: structure, function, and evolution of a family business. J Interferon Cytokine Res 1999 19 : 1069 98.
53. Matikainen S, Sareneva T, Ronni T, Lehtonen A, Koskinen PJ, Julkunen I. Interferon-alpha activates multiple STAT proteins and upregulates proliferation-associated IL-2Ralpha, c-myc, and pim-1 genes in human T cells. Blood 1999 93 : 1980 91.
54. Ullman KS, Flanagan WM, Cothesy B, Kuo P, Northrop JP, Crabtree GR. Site of action of cyclosporine and FK 506 in the pathways of communication between the T-lymphocyte antigen receptor and the early activation genes. J Clin Invest 1991 8 : 1690 6.
55. Craston R, Koh M, McDermott A, Ray N, Prentice HG, Lowdell MW. Temporal dynamics of CD69 expression on lymphoid cells. J Immunol Meth 1997 209 : 37 45.
56. Borrego F, Masilamani M, Marusina AI, Tang X, Coligan JE. The CD94/NKG2 family of receptors: from molecules and cells to clinical relevance. Immunol Res 2006 35 : 263 78.
57. Lopez-Cabrera M, Goodson DZ, Herschbach DR, Morgani JD 3rd. Molecular cloning, expression, and chromosomal localization of the human earliest lymphocyte activation antigen AIM/CD69, a new member of the C-type animal lectin superfamily of signal-transmitting receptors. J Exp Med 1993 178 : 537 47.
58. Jewett A, Bonavida B. Target-induced anergy of natural killer cytotoxic function is restricted to the NK-target conjugate subset. Cell Immunol 1995 160 : 91 7.
59. Clausen J, Vergeiner B, Enk M, Petzer AL, Gastl G, Gunsilius E. CD69 is a useful marker for cytotoxic activity of NK cells. Immunobiology 2003 207 : 85 93.
60. Gerosa F, Tommasi M, Benati C, Gandini G, Libonati M, Tridente G et al. Differential effects of tyrosine kinase inhibition in CD69 antigen expression and lytic activity induced by rIL-2, rIL-12, and rIFN-alpha in human NK cells. Cell Immunol 1993 150 : 382 90.
61. Lehtonen A, Lund R, Lahesmaa R, Julkunen I, Sareneva T, Matikainen S. IFN-alpha and IL-12 activate IFN regulatory factor 1 (IRF-1), IRF-4, and IRF-8 gene expression in human NK and T cells. Cytokine 2003 24 : 81 90.
62. Duncan GS, Mittrucker HW, Kagi D, Matsuyama T, Mak TW. The transcription factor interferon regulatory factor-1 is essential for natural killer cell function in vivo. J Exp Med 1996 184 : 2043 8.
63. Enzinger PC, Ilson DH, Saltz LB, Martin LK, Kelsen DP. Phase II clinical trial of 13-cis-retinoic acid and interferon-alpha-2a in patients with advanced esophageal carcinoma. Cancer 1999 85 : 1213 7.