Endogenous IL-8 acts as a CD16 co-activator for natural killer-mediated anti-CD20 B cell depletion in chronic lymphocytic leukemia

Leukemia Research

Volumn 37, Issue 4, 2013, Pages 440-446

  Laprevotte, Emilie ^a,b,c   Ysebaert, Loïc ^a,b,c,d   Klein, Christian ^e   Valleron, Wilfried ^a,b,c   Blanc, Amandine ^a,b,c   Gross, Emilie ^a,b,c   Laurent, Guy ^a,b,c,d   Fournié, Jean Jacques ^a,b,c   Quillet Mary, Anne ^a,b,c  

^a CANCER RESEARCH CENTER OF TOULOUSE   (France)

^b ERL 5294 CNRS   (France)

^c UNIVERSITÉ DE TOULOUSE   (France)

^d CHU PURPAN   (France)

^e Roche Glycart AG   (Switzerland)

Author keywords

ADCC; Anti CD20 monoclonal antibodies; CLL; IL 8; NK

Indexed keywords

CD16 ANTIGEN; CD20 ANTIGEN; INTERLEUKIN 8; OBINUTUZUMAB; RITUXIMAB;

ADULT; AGED; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; B LYMPHOCYTE; CELL ACTIVATION; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; LYMPHOCYTE DEPLETION; MAJOR CLINICAL STUDY; MALE; NATURAL KILLER CELL; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL;

ANTIBODIES, MONOCLONAL; ANTIGENS, CD20; B-LYMPHOCYTES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; INTERLEUKIN-8; KILLER CELLS, NATURAL; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LYMPHOCYTE DEPLETION; RECEPTORS, IGG;

EID: 84875376406     PISSN: 01452126     EISSN: 18735835     Source Type: Journal    
DOI: 10.1016/j.leukres.2012.11.015     Document Type: Article

References (48)

1. Tam C.S., O'Brien S., Wierda W., Kantarjian H., Wen S., Do K.A., et al. Long-term results of the fludarabine, cyclophosphamide, and rituximab regimen as initial therapy of chronic lymphocytic leukemia. Blood 2008, 112:975-980.
2. Hallek M., Fischer K., Fingerle-Rowson G., Fink A.M., Busch R., Mayer J., et al. Addition of rituximab to fludarabine and cyclophosphamide in patients with chronic lymphocytic leukaemia: a randomised, open-label, phase 3 trial. Lancet 2010, 376:1164-1174.
3. Glennie M.J., French R.R., Cragg M.S., Taylor R.P. Mechanisms of killing by anti-CD20 monoclonal antibodies. Mol Immunol 2007, 44:3823-3837.
4. Bezombes C., Grazide S., Garret C., Fabre C., Quillet-Mary A., Müller S., et al. Rituximab antiproliferative effect in B-lymphoma cells is associated with acid-sphingomyelinase activation in raft microdomains. Blood 2004, 104:1166-1173.
5. Harjunpaa A., Junnikkala S., Meri S. Rituximab (anti-CD20) therapy of B-cell lymphomas: direct complement killing is superior to cellular effector mechanisms. Scand J Immunol 2000, 51:634-641.
6. Bologna L., Gotti E., Manganini M., Rambaldi A., Intermesoli T., Introna M., et al. Mechanism of action of type II, glycoengineered, anti-CD20 monoclonal antibody GA101 in B-chronic lymphocytic leukemia whole blood assays in comparison with rituximab and alemtuzumab. J Immunol 2011, 186:3762-3769.
7. Golay J., Manganini M., Facchinetti V., Gramigna R., Broady R., Borleri G., et al. Rituximab-mediated antibody-dependent cellular cytotoxicity against neoplastic B cells is stimulated strongly by interleukin-2. Haematologica 2003, 88:1002-1012.
8. Fischer L., Penack O., Gentilini C., Nogai A., Muessig A., Thiel E., et al. The anti-lymphoma effect of antibody-mediated immunotherapy is based on an increased degranulation of peripheral blood natural killer (NK) cells. Exp Hematol 2006, 34:753-759.
9. Ysebaert L., Gross E., Kühlein E., Blanc A., Corre J., Fournié J.J., et al. Immune recovery after fludarabine-cyclophosphamide-rituximab treatment in B-chronic lymphocytic leukemia: implication for maintenance immunotherapy. Leukemia 2010, 24:1310-1316.
10. Mössner E., Brünker P., Moser S., Püntener U., Schmidt C., Herter S., et al. Increasing the efficacy of CD20 antibody therapy through the engineering of a new type II anti-CD20 antibody with enhanced direct and immune effector cell-mediated B-cell cytotoxicity. Blood 2010, 115:4393-4402.
11. Panayiotidis P., Jones D., Ganeshaguru K., Foroni L., Hoffbrand A.V. Human bone marrow stromal cells prevent apoptosis and support the survival of chronic lymphocytic leukaemia cells in vitro. Br J Haematol 1996, 92:97-103.
12. Söderberg O. Growth and survival of B-chronic lymphocytic leukaemia cells. Med Oncol 1998, 15:73-78.
13. Burger J.A., Tsukada N., Burger M., Zvaifler N.J., Dell'Aquila M., Kipps T.J. Blood-derived nurse-like cells protect chronic lymphocytic leukemia B cells from spontaneous apoptosis through stromal cell-derived factor-1. Blood 2000, 96:2655-2663.
14. Aguilar-Santelises M., Gigliotti D., Osorio L.M., Santiago A.D., Mellstedt H., Jondal M. Cytokine expression in B-CLL in relation to disease progression and in vitro activation. Med Oncol 1999, 16:289-295.
15. Schröttner P., Leick M., Burger M. The role of chemokines in B cell chronic lymphocytic leukaemia: pathophysiological aspects and clinical impact. Ann Hematol 2010, 89:437-446.
16. di Celle P.F., Carbone A., Marchis D., Zhou D., Sozzani S., Zupo S., et al. Cytokine gene expression in B-cell chronic lymphocytic leukemia: evidence of constitutive interleukin-8 (IL-8) mRNA expression and secretion of biologically active IL-8 protein. Blood 1994, 84:220-228.
17. Burger J.A. Chemokines and chemokine receptors in chronic lymphocytic leukemia (CLL): from understanding the basics towards therapeutic targeting. Semin Cancer Biol 2010, 20:424-430.
18. Kremer J.P., Reisbach G., Nerl C., Dörmer P. B-cell chronic lymphocytic leukaemia cells express and release transforming growth factor-beta. Br J Haematol 1992, 80:480-487.
19. Bellone G., Aste-Amezaga M., Trinchieri G., Rodeck U. Regulation of NK cell functions by TGF-beta 1. J Immunol 1995, 155:1066-1073.
20. Trotta R., Dal Col J., Yu J., Ciarlariello D., Thomas B., Zhang X., et al. TGF-beta utilizes SMAD3 to inhibit CD16-mediated IFN-gamma production and antibody-dependent cellular cytotoxicity in human NK cells. J Immunol 2008, 181:3784-3792.
21. Osorio L.M., Aguilar-Santelises M., De Santiago A., Hachiya T., Mellstedt H., Jondal M. Increased serum levels of soluble Fas in progressive B-CLL. Eur J Haematol 2001, 66:342-346.
22. Kara I.O., Sahin B., Gunesacar R. Expression of soluble CD27 and interleukins-8 and -10 in B-cell chronic lymphocytic leukemia: correlation with disease stage and prognosis. Adv Ther 2007, 24:29-40.
23. Wierda W.G., Johnson M.M., Do K.A., Manshouri T., Dey A., O'Brien S., et al. Plasma interleukin 8 level predicts for survival in chronic lymphocytic leukaemia. Br J Haematol 2003, 120:452-456.
24. Molica S., Vitelli G., Levato D., Levato L., Dattilo A., Gandolfo G.M. Clinico-biological implications of increased serum levels of interleukin-8 in B-cell chronic lymphocytic leukemia. Haematologica 1999, 84:208-211.
25. Schröttner P., Wollner S., Catusse J., Burger M. Detection of elevated serum levels of the chemokine CCL18 in B-cell chronic lymphocytic leukaemia: identification of a novel biomarker. Acta Haematol 2010, 124:110-114.
26. Yoon J.Y., Lafarge S., Dawe D., Lakhi S., Kumar R., Morales C., et al. Association of interleukin-6 and interleukin-8 with poor prognosis in elderly chronic lymphocytic leukemia patients. Leuk Lymphoma 2012, 53:1735-1742.
27. Francia di Celle P., Mariani S., Riera L., Stacchini A., Reato G., Foa R. Interleukin-8 induces the accumulation of B-cell chronic lymphocytic leukemia cells by prolonging survival in an autocrine fashion. Blood 1996, 87:4382-4389.
28. Secchiero P., Corallini F., Barbarotto E., Melloni E., di Iasio M.G., Tiribelli M., et al. Role of the RANKL/RANK system in the induction of interleukin-8 (IL-8) in B chronic lymphocytic leukemia (B-CLL) cells. J Cell Physiol 2006, 207:158-164.
29. Loetscher P., Clark-Lewis I. Agonistic and antagonistic activities of chemokines. J Leukoc Biol 2001, 69:881-884.
30. Mukaida N. Interleukin-8: an expanding universe beyond neutrophil chemotaxis and activation. Int J Hematol 2000, 72:391-398.
31. Burke S.M., Issekutz T.B., Mohan K., Lee P.W., Shmulevitz M., Marshall J.S. Human mast cell activation with virus-associated stimuli leads to the selective chemotaxis of natural killer cells by a CXCL8-dependent mechanism. Blood 2008, 111:5467-5476.
32. Sivori S., Falco M., Della Chiesa M., Carlomagno S., Vitale M., Moretta L., et al. CpG and double-stranded RNA trigger human NK cells by Toll-like receptors: induction of cytokine release and cytotoxicity against tumors and dendritic cells. Proc Natl Acad Sci USA 2004, 101:10116-10121.
33. Hayashi S., Kurdowska A., Miller E.J., Albright M.E., Girten B.E., Cohen A.B. Synthetic hexa- and heptapeptides that inhibit IL-8 from binding to and activating human blood neutrophils. J Immunol 1995, 154:814-824.
34. Snoussi K., Mahfoudh W., Bouaouina N., Ahmed S.B., Helal A.N., Chouchane L. Genetic variation in IL-8 associated with increased risk and poor prognosis of breast carcinoma. Hum Immunol 2006, 67:13-21.
35. Seiffert M., Schulz A., Ohl S., Döhner H., Stilgenbauer S., Lichter P. Soluble CD14 is a novel monocyte-derived survival factor for chronic lymphocytic leukemia cells, which is induced by CLL cells in vitro and present at abnormally high levels in vivo. Blood 2010, 116:4223-4230.
36. + dim NK cells from CLL patients: evidence supporting a therapeutic strategy with optimized anti-CD20 monoclonal antibodies. Leukemia 2011, 25:101-109.
37. Hallek M., Pflug N. State of the art treatment of chronic lymphocytic leukaemia. Blood Rev 2011, 25:1-9.
38. Farag S.S., Flinn I.W., Modali R., Lehman T.A., Young D., Byrd J.C. Fc gamma RIIIa and Fc gamma RIIa polymorphisms do not predict response to rituximab in B-cell chronic lymphocytic leukemia. Blood 2004, 103:1472-1474.
39. Niederfellner G., Lammens A., Mundigl O., Georges G.J., Schaefer W., Schwaiger M., et al. Epitope characterization and crystal structure of GA101 provide insights into the molecular basis for type I/II distinction of CD20 antibodies. Blood 2011, 118:358-367.
40. Alduaij W., Ivanov A., Honeychurch J., Cheadle E.J., Potluri S., Lim S.H., et al. Novel type II anti-CD20 monoclonal antibody (GA101) evokes homotypic adhesion and actin-dependent, lysosome-mediated cell death in B-cell malignancies. Blood 2011, 117:4519-4529.
41. Trotta R., Puorro K.A., Paroli M., Azzoni L., Abebe B., Eisenlohr L.C., et al. Dependence of both spontaneous and antibody-dependent, granule exocytosis-mediated NK cell cytotoxicity on extracellular signal-regulated kinases. J Immunol 1998, 161:6648-6656.
42. Waugh D.J., Wilson C. The interleukin-8 pathway in cancer. Clin Cancer Res 2008, 14:6735-6741.
43. Patz M., Isaeva P., Forcob N., Müller B., Frenzel L.P., Wendtner C.M., et al. Comparison of the in vitro effects of the anti-CD20 antibodies rituximab and GA101 on chronic lymphocytic leukaemia cells. Br J Haematol 2011, 152:295-306.
44. Dalle S., Reslan L., Besseyre de Horts T., Herveau S., Herting F., Plesa A., et al. Preclinical studies on the mechanism of action and the anti-lymphoma activity of the novel anti-CD20 antibody GA101. Mol Cancer Ther 2011, 10:178-185.
45. Razmkhah M., Jaberipour M., Hosseini A., Safaei A., Khalatbari B., Ghaderi A. Expression profile of IL-8 and growth factors in breast cancer cells and adipose-derived stem cells (ASCs) isolated from breast carcinoma. Cell Immunol 2010, 265:80-85.
46. Cho M.L., Ju J.H., Kim H.R., Oh H.J., Kang C.M., Jhun J.Y., et al. Toll-like receptor 2 ligand mediates the upregulation of angiogenic factor, vascular endothelial growth factor and interleukin-8/CXCL8 in human rheumatoid synovial fibroblasts. Immunol Lett 2007, 108:121-128.
47. Bartosik-Psujek H., Stelmasiak Z. The levels of chemokines CXCL8. CCL2 and CCL5 in multiple sclerosis patients are linked to the activity of the disease. Eur J Neurol 2005, 12:49-54.
48. Townsend M.J., Monroe J.G., Chan A.C. B-cell targeted therapies in human autoimmune diseases: an updated perspective. Immunol Rev 2010, 237:264.