Anti-CCR7 monoclonal antibodies as a novel tool for the treatment of chronic lymphocyte leukemia

Journal of Leukocyte Biology - Tập 79 Số 6 - Trang 1157-1165 - 2006
Manuel Alfonso-Pérez1, Sonia López-Giral1, Nuria Quintana1, Javier Loscertales2, Patricia Martín‐Jiménez3, Cecilia Muñoz1
1Departments of Immunology, Hospital Universitario de La Princesa , Madrid, Spain
2Departments of Hematology, Hospital Universitario de La Princesa , Madrid, Spain
3Department of Hematology, Hospital Clínico Universitario de Salamanca , Spain

Tóm tắt

Abstract

To date, chronic lymphocytic leukemia (CLL) remains incurable with current treatments, which include the monoclonal antibodies (mAbs) rituximab and alemtuzumab. The efficacy of rituximab is modest when used as single agent, and alemtuzumab induces severe immunosuppression. To develop more potent and specific therapies, we propose the CC chemokine receptor 7 (CCR7) as an attractive target molecule to treat CLL, as it not only fulfills the requirements of a high-surface expression and a good level of tissue specificity, but it also plays a crucial role in mediating the migration of the tumor cells to lymph nodes (LNs) and thus, in the development of clinical lymphadenopathy. In the current work, murine anti-human CCR7 mAb mediated a potent, complement-dependent cytotoxicity (CDC) against CLL cells while sparing normal T lymphocytes from the same patients. The sensitivity to CDC was related to the antigenic density of CCR7. Moreover, these mAb blocked the in vitro migration of CLL cells in response to CC chemokine ligand 19 (CC219), one of the physiological ligands of CCR7. Conversely, CLL cells were poorly lysed through antibody-dependent, cell-mediated cytotoxicity (ADCC), probably as a result of the murine origin and the isotype of the anti-CCR7 mAb used. Molecular engineering techniques will allow us to obtain chimeric or humanized anti-CCR7 mAb to reach the best clinical response for this common and yet incurable leukemia.

Từ khóa


Tài liệu tham khảo

Byrd, 2003, Randomized phase 2 study of fludarabine with concurrent versus sequential treatment with rituximab in symptomatic, untreated patients with B-cell chronic lymphocytic leukemia: results from Cancer and Leukemia Group B 9712 (CALGB 9712), Blood, 101, 6, 10.1182/blood-2002-04-1258

Byrd, 2005, Addition of rituximab to fludarabine may prolong progression-free survival and overall survival in patients with previously untreated chronic lymphocytic leukemia: an updated retrospective comparative analysis of CALGB 9712 and CALGB 9011, Blood, 105, 49, 10.1182/blood-2004-03-0796

Keating, 2005, Early results of a chemo-immunotherapy regimen of fludarabine, cyclophosphamide, and rituximab as initial therapy for chronic lymphocytic leukemia, J. Clin. Oncol., 23, 4079, 10.1200/JCO.2005.12.051

Wierda, 2005, Chemoimmunotherapy with fludarabine, cyclophosphamide, and rituximab for relapsed and refractory chronic lymphocytic leukemia, J. Clin. Oncol., 23, 4070, 10.1200/JCO.2005.12.516

Kay, 2006, Treatment and evaluation of CLL: a complicated affair, Blood, 107, 848, 10.1182/blood-2005-11-4501

Countouriotis, 2002, Cell surface antigen and molecular targeting in the treatment of hematologic malignancies, Stem Cells, 20, 215, 10.1634/stemcells.20-3-215

Villamor, 2003, Mechanism of action and resistance to monoclonal antibody therapy, Semin. Oncol., 30, 424, 10.1016/S0093-7754(03)00261-6

Olszewski, 2004, Empowering targeted therapy: lessons from rituximab, Sci. STKE, 2004, pe30, 10.1126/stke.2412004pe30

Lopez-Giral, 2004, Chemokine receptors that mediate B cell homing to secondary lymphoid tissues are highly expressed in B cell chronic lymphocytic leukemia and non-Hodgkin lymphomas with widespread nodular dissemination, J. Leukoc. Biol., 76, 462, 10.1189/jlb.1203652

Till, 2002, The chemokine receptor CCR7 and α4 integrin are important for migration of chronic lymphocytic leukemia cells into lymph nodes, Blood, 99, 2977, 10.1182/blood.V99.8.2977

Hasegawa, 2000, Increased chemokine receptor CCR7/EBI1 expression enhances the infiltration of lymphoid organs by adult T-cell leukemia cells, Blood, 95, 30, 10.1182/blood.V95.1.30.001k09_30_38

Hopken, 2002, Up-regulation of the chemokine receptor CCR7 in classical but not in lymphocyte-predominant Hodgkin disease correlates with distinct dissemination of neoplastic cells in lymphoid organs, Blood, 99, 1109, 10.1182/blood.V99.4.1109

Kallinich, 2003, Chemokine receptor expression on neoplastic and reactive T cells in the skin at different stages of mycosis fungoides, J. Invest. Dermatol., 121, 1045, 10.1046/j.1523-1747.2003.12555.x

Forster, 2001, Lessons learned from lymphocytes: CC chemokine receptor-7 involved in lymphogenic metastasis of melanoma, J. Natl. Cancer Inst., 93, 1588, 10.1093/jnci/93.21.1588

Muller, 2001, Involvement of chemokine receptors in breast cancer metastasis, Nature, 410, 50, 10.1038/35065016

Mashino, 2002, Expression of chemokine receptor CCR7 is associated with lymph node metastasis of gastric carcinoma, Cancer Res., 62, 2937

Ding, 2003, Association of CC chemokine receptor 7 with lymph node metastasis of esophageal squamous cell carcinoma, Clin. Cancer Res., 9, 3406

Takanami, 2003, Overexpression of CCR7 mRNA in nonsmall cell lung cancer: correlation with lymph node metastasis, Int. J. Cancer, 105, 186, 10.1002/ijc.11063

Wang, 2004, Expression pattern of chemokine receptor 6 (CCR6) and CCR7 in squamous cell carcinoma of the head and neck identifies a novel metastatic phenotype, Cancer Res., 64, 1861, 10.1158/0008-5472.CAN-03-2968

Cyster, 1999, Chemokines and cell migration in secondary lymphoid organs, Science, 286, 2098, 10.1126/science.286.5447.2098

Potsch, 1999, Distinct migration patterns of naive and effector CD8 T cells in the spleen: correlation with CCR7 receptor expression and chemokine reactivity, Eur. J. Immunol., 29, 3562, 10.1002/(SICI)1521-4141(199911)29:11<3562::AID-IMMU3562>3.0.CO;2-R

Okada, 2002, Chemokine requirements for B cell entry to lymph nodes and Peyer's patches, J. Exp. Med., 196, 65, 10.1084/jem.20020201

Reif, 2002, Balanced responsiveness to chemoattractants from adjacent zones determines B-cell position, Nature, 416, 94, 10.1038/416094a

Muller, 2003, Shaping up adaptive immunity: the impact of CCR7 and CXCR5 on lymphocyte trafficking, Microcirculation, 10, 325, 10.1080/mic.10.3-4.325.334

Junt, 2004, Impact of CCR7 on priming and distribution of antiviral effector and memory CTL, J. Immunol., 173, 6684, 10.4049/jimmunol.173.11.6684

Yoshie, 1997, Novel lymphocyte-specific CC chemokines and their receptors, J. Leukoc. Biol., 62, 634, 10.1002/jlb.62.5.634

Dieu, 1998, Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites, J. Exp. Med., 188, 373, 10.1084/jem.188.2.373

Kim, 1998, CK β-11/macrophage inflammatory protein-3 β/EBI1-ligand chemokine is an efficacious chemoattractant for T and B cells, J. Immunol., 160, 2418, 10.4049/jimmunol.160.5.2418

Sallusto, 1998, Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation, Eur. J. Immunol., 28, 2760, 10.1002/(SICI)1521-4141(199809)28:09<2760::AID-IMMU2760>3.0.CO;2-N

Sozzani, 1998, Differential regulation of chemokine receptors during dendritic cell maturation: a model for their trafficking properties, J. Immunol., 161, 1083, 10.4049/jimmunol.161.3.1083

Willimann, 1998, The chemokine SLC is expressed in T cell areas of lymph nodes and mucosal lymphoid tissues and attracts activated T cells via CCR7, Eur. J. Immunol., 28, 2025, 10.1002/(SICI)1521-4141(199806)28:06<2025::AID-IMMU2025>3.0.CO;2-C

Yoshida, 1998, EBI1-ligand chemokine (ELC) attracts a broad spectrum of lymphocytes: activated T cells strongly up-regulate CCR7 and efficiently migrate toward ELC, Int. Immunol., 10, 901, 10.1093/intimm/10.7.901

van Dongen, 2003, Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: report of the BIOMED-2 Concerted Action BMH4-CT98–3936, Leukemia, 17, 2257, 10.1038/sj.leu.2403202

Gonzalez, 1999, Heteroduplex analysis of VDJ amplified segments from rearranged IgH genes for clonality assessments in B-cell non-Hodgkin's lymphoma. A comparison between different strategies, Haematologica, 84, 779

Cook, 1995, The human immunoglobulin VH repertoire, Immunol. Today, 16, 237, 10.1016/0167-5699(95)80166-9

Bleul, 1997, The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes, Proc. Natl. Acad. Sci. USA, 94, 1925, 10.1073/pnas.94.5.1925

Tarasova, 1998, Spontaneous and ligand-induced trafficking of CXC-chemokine receptor 4, J. Biol. Chem., 273, 15883, 10.1074/jbc.273.26.15883

Manches, 2003, In vitro mechanisms of action of rituximab on primary non-Hodgkin lymphomas, Blood, 101, 949, 10.1182/blood-2002-02-0469

Pangalis, 2001, Campath-1H (anti-CD52) monoclonal antibody therapy in lymphoproliferative disorders, Med. Oncol., 18, 99, 10.1385/MO:18:2:99

Huhn, 2001, Rituximab therapy of patients with B-cell chronic lymphocytic leukemia, Blood, 98, 1326, 10.1182/blood.V98.5.1326

Bertolini, 2002, CXCR4 neutralization, a novel therapeutic approach for non-Hodgkin's lymphoma, Cancer Res., 62, 3106

Tavor, 2004, CXCR4 regulates migration and development of human acute myelogenous leukemia stem cells in transplanted NOD/SCID mice, Cancer Res., 64, 2817, 10.1158/0008-5472.CAN-03-3693

Niwa, 2004, Defucosylated chimeric anti-CC chemokine receptor 4 IgG1 with enhanced antibody-dependent cellular cytotoxicity shows potent therapeutic activity to T-cell leukemia and lymphoma, Cancer Res., 64, 2127, 10.1158/0008-5472.CAN-03-2068

Harjunpaa, 2000, Rituximab (anti-CD20) therapy of B-cell lymphomas: direct complement killing is superior to cellular effector mechanisms, Scand. J. Immunol., 51, 634, 10.1046/j.1365-3083.2000.00745.x

Golay, 2001, CD20 levels determine the in vitro susceptibility to rituximab and complement of B-cell chronic lymphocytic leukemia: further regulation by CD55 and CD59, Blood, 98, 3383, 10.1182/blood.V98.12.3383

Harjunpaa, 2001, Complement activation in circulation and central nervous system after rituximab (anti-CD20) treatment of B-cell lymphoma, Leuk. Lymphoma, 42, 731, 10.3109/10428190109099335

Di Gaetano, 2003, Complement activation determines the therapeutic activity of rituximab in vivo, J. Immunol., 171, 1581, 10.4049/jimmunol.171.3.1581

Cragg, 2004, Antibody specificity controls in vivo effector mechanisms of anti-CD20 reagents, Blood, 103, 2738, 10.1182/blood-2003-06-2031

Kennedy, 2004, Rituximab infusion promotes rapid complement depletion and acute CD20 loss in chronic lymphocytic leukemia, J. Immunol., 172, 3280, 10.4049/jimmunol.172.5.3280

Golay, 2003, Rituximab-mediated antibody-dependent cellular cytotoxicity against neoplastic B cells is stimulated strongly by interleukin-2, Haematologica, 88, 1002

Byrd, 2002, The mechanism of tumor cell clearance by rituximab in vivo in patients with B-cell chronic lymphocytic leukemia: evidence of caspase activation and apoptosis induction, Blood, 99, 1038, 10.1182/blood.V99.3.1038

Pedersen, 2002, The chimeric anti-CD20 antibody rituximab induces apoptosis in B-cell chronic lymphocytic leukemia cells through a p38 mitogen activated protein-kinase-dependent mechanism, Blood, 99, 1314, 10.1182/blood.V99.4.1314

Dyall, 1999, Cellular requirements for the monoclonal antibody-mediated eradication of an established solid tumor, Eur. J. Immunol., 29, 30, 10.1002/(SICI)1521-4141(199901)29:01<30::AID-IMMU30>3.0.CO;2-D

Cragg, 2003, Complement-mediated lysis by anti-CD20 mAb correlates with segregation into lipid rafts, Blood, 101, 1045, 10.1182/blood-2002-06-1761

Teeling, 2004, Characterization of new human CD20 monoclonal antibodies with potent cytolytic activity against non-Hodgkin lymphomas, Blood, 104, 1793, 10.1182/blood-2004-01-0039

Katrinakis, 1996, Defective natural killer cell activity in B-cell chronic lymphocytic leukaemia is associated with impaired release of natural killer cytotoxic factor(s) but not of tumour necrosis factor-α, Acta Haematol., 96, 16, 10.1159/000203709

Scrivener, 2003, Abnormal T-cell function in B-cell chronic lymphocytic leukaemia, Leuk. Lymphoma, 44, 383, 10.1080/1042819021000029993

Farag, 2004, Fc γ RIIIa and Fc γ RIIa polymorphisms do not predict response to rituximab in B-cell chronic lymphocytic leukemia, Blood, 103, 1472, 10.1182/blood-2003-07-2548

Lin, 2005, FCGR3A and FCGR2A polymorphisms may not correlate with response to alemtuzumab in chronic lymphocytic leukemia, Blood, 105, 289, 10.1182/blood-2004-02-0651

Forster, 1999, CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs, Cell, 99, 23, 10.1016/S0092-8674(00)80059-8

Ghobrial, 2004, Expression of the chemokine receptors CXCR4 and CCR7 and disease progression in B-cell chronic lymphocytic leukemia/small lymphocytic lymphoma, Mayo Clin. Proc., 79, 318, 10.4065/79.3.318

Carter, 2001, Improving the efficacy of antibody-based cancer therapies, Nat. Rev. Cancer, 1, 118, 10.1038/35101072

Kipriyanov, 2004, Generation and production of engineered antibodies, Mol. Biotechnol., 26, 39, 10.1385/MB:26:1:39