RANKL expression, function, and therapeutic targeting in multiple myeloma and chronic lymphocytic leukemia

Cancer Research

Volumn 73, Issue 2, 2013, Pages 683-694

  Schmiedel, Benjamin Joachim ^a   Scheible, Carolin Andrea ^a   Nuebling, Tina ^a   Kopp, Hans Georg ^a   Wirths, Stefan ^a   Azuma, Miyuki ^b   Schneider, Pascal ^c   Jung, Gundram ^a   Grosse Hovest, Ludger ^a   Salih, Helmut Rainer ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; DENOSUMAB; FC RECEPTOR; HYBRID PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; OSTEOCLAST DIFFERENTIATION FACTOR; RANK FC FUSION PROTEIN; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; CANCER IMMUNOTHERAPY; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKEMIA CELL; MULTIPLE MYELOMA; MYELOMA CELL; NATURAL KILLER CELL; NUCLEOTIDE SEQUENCE; OSTEOCLASTOGENESIS; PRIORITY JOURNAL; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

ANTIBODIES, MONOCLONAL, HUMANIZED; CELL LINE, TUMOR; HUMANS; KILLER CELLS, NATURAL; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MULTIPLE MYELOMA; RANK LIGAND; RECEPTORS, FC; RECOMBINANT FUSION PROTEINS; TRANSFECTION;

EID: 84872505990     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-2280     Document Type: Article

References (50)

1. Hofbauer LC, Heufelder AE. Role of receptor activator of nuclear factor-kappaB ligand and osteoprotegerin in bone cell biology. J Mol Med 2001;79: 243-53.
2. Secchiero P, Corallini F, Barbarotto E, Melloni E, di IasioMG, 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: 158-64.
3. Pearse RN, Sordillo EM, Yaccoby S, Wong BR, Liau DF, Colman N, et al. Multiple myeloma disrupts the TRANCE/osteoprotegerin cytokine axis to trigger bone destruction and promote tumor progression. Proc Natl Acad Sci U S A 2001;98: 11581-6.
4. Croucher PI, Shipman CM, Lippitt J, Perry M, Asosingh K, Hijzen A, et al. Osteoprotegerin inhibits the development of osteolytic bone disease in multiple myeloma. Blood 2001;98: 3534-40.
5. Yaccoby S, Pearse RN, Johnson CL, Barlogie B, Choi Y, Epstein J. Myeloma interacts with the bone marrow microenvironment to induce osteoclastogenesis and is dependent on osteoclast activity. Br J Haematol 2002;116: 278-90.
6. Sordillo EM, Pearse RN. RANK-Fc: a therapeutic antagonist for RANKL in myeloma. Cancer 2003;97: 802-12.
7. Terpos E, Szydlo R, Apperley JF, Hatjiharissi E, Politou M, Meletis J, et al. Soluble receptor activator of nuclear factor kappaB ligand- osteoprotegerin ratio predicts survival in multiple myeloma: proposal for a novel prognostic index. Blood 2003;102: 1064-9.
8. Farrugia AN, Atkins GJ, To LB, Pan B, Horvath N, Kostakis P, et al. Receptor activator of nuclear factor-kappaB ligand expression by human myeloma cells mediates osteoclast formation in vitro and correlateswith bone destruction in vivo. Cancer Res 2003;63: 5438-45.
9. Heider U, Langelotz C, Jakob C, Zavrski I, Fleissner C, Eucker J, et al. Expression of receptor activator of nuclear factor kappaB ligand on bone marrow plasma cells correlates with osteolytic bone disease in patients with multiple myeloma. Clin Cancer Res 2003;9: 1436-40.
10. Giuliani N, Bataille R, Mancini C, Lazzaretti M, Barille S. Myeloma cells induce imbalance in the osteoprotegerin/osteoprotegerin ligand system in the human bone marrow environment. Blood 2001;98: 3527-33.
11. Cummings SR, San Martin J, McClung MR, Siris ES, Eastell R, Reid IR, et al. Denosumab for prevention of fractures in postmenopausal women with osteoporosis. N Engl J Med 2009;361: 756-65.
12. Smith MR, Egerdie B, Hernandez TN, Feldman R, Tammela TL, Saad F, et al. Denosumab in men receiving androgen-deprivation therapy for prostate cancer. N Engl J Med 2009;361: 745-55.
13. Vij R, Horvath N, Spencer A, Taylor K, Vadhan-Raj S, Vescio R, et al. An open-label, phase 2 trial of denosumab in the treatment of relapsed or plateau-phase multiple myeloma. Am J Hematol 2009;84: 650-6.
14. Schwarz EM, Ritchlin CT. Clinical development of anti-RANKL therapy. Arthritis Res Ther 2007;9 Suppl 1:S7.
15. Keating GM. Rituximab: a review of its use in chronic lymphocytic leukaemia, low-grade or follicular lymphoma and diffuse large B-cell lymphoma. Drugs 2010;70: 1445-76.
16. Weiner GJ. Rituximab: mechanism of action. Semin Hematol 2010;47: 115-23.
17. Beck A, Wurch T, Bailly C, Corvaia N. Strategies and challenges for the next generation of therapeutic antibodies. Nat Rev Immunol 2010;10: 345-52.
18. Horton HM, Bernett MJ, Peipp M, Pong E, Karki S, Chu SY, et al. Fcengineered anti-CD40 antibody enhances multiple effector functions and exhibits potent in vitro and in vivo antitumor activity against hematologic malignancies. Blood 2010;116: 3004-12.
19. Robak T. GA-101, a third-generation, humanized and glyco-engineered anti-CD20 mAb for the treatment of B-cell lymphoid malignancies. Curr Opin Investig Drugs 2009;10: 588-96.
20. Kraj M, Kopec-Szlezak J, Poglod R, Kruk B. Flow cytometric immunophenotypic characteristics of 36 cases of plasma cell leukemia. Leuk Res 2011;35: 169-76.
21. Tai YT, Horton HM, Kong SY, Pong E, Chen H, Cemerski S, et al. Potent in vitro and in vivo activity of an Fc-engineered humanized anti-HM1.24 antibody against multiple myeloma via augmented effector function. Blood 2012;119: 2074-82.
22. Lazar GA, Dang W, Karki S, Vafa O, Peng JS, Hyun L, et al. Engineered antibody Fc variants with enhanced effector function. Proc Natl Acad Sci U S A 2006;103: 4005-10.
23. Kanamaru F, Iwai H, Ikeda T, Nakajima A, Ishikawa I, Azuma M. Expression of membrane-bound and soluble receptor activator of NF-kappaB ligand (RANKL) in human T cells. Immunol Lett 2004;94: 239-46.
24. Baessler T, Charton JE, Schmiedel BJ, Grunebach F, Krusch M, Wacker A, et al. CD137 ligand mediates opposite effects in human and mouse NK cells and impairs NK-cell reactivity against human acute myeloid leukemia cells. Blood 2010;115: 3058-69.
25. Hsu H, Lacey DL, Dunstan CR, Solovyev I, Colombero A, Timms E, et al. Tumor necrosis factor receptor family member RANK mediates osteoclast differentiation and activation induced by osteoprotegerin ligand. Proc Natl Acad Sci U S A 1999;96: 3540-5.
26. Schmiedel BJ, Arelin V, Gruenebach F, Krusch M, Schmidt SM, Salih HR. Azacytidine impairs NK cell reactivity while decitabine augments NK cell responsiveness toward stimulation. Int J Cancer 2011;128: 2911-22.
27. Baessler T, Krusch M, Schmiedel BJ, Kloss M, Baltz KM, Wacker A, et al. Glucocorticoid-induced tumor necrosis factor receptor-related protein ligand subverts immunosurveillance of acute myeloid leukemia in humans. Cancer Res 2009;69: 1037-45.
28. Ferrajoli A, Keating MJ, Manshouri T, Giles FJ, Dey A, Estrov Z, et al. The clinical significance of tumor necrosis factor-alpha plasma level in patients having chronic lymphocytic leukemia. Blood 2002;100: 1215-9.
29. Lai R, O'Brien S, Maushouri T, Rogers A, Kantarjian H, Keating M, et al. Prognostic value of plasma interleukin-6 levels in patients with chronic lymphocytic leukemia. Cancer 2002;95: 1071-5.
30. Wierda WG, Johnson MM, Do KA, 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: 452-6.
31. Kuku I, Bayraktar MR, Kaya E, Erkurt MA, Bayraktar N, Cikim K, et al. Serum proinflammatory mediators at different periods of therapy in patients with multiplemyeloma. Mediators Inflamm 2005;2005: 171-4.
32. Armour KL, Clark MR, Hadley AG, Williamson LM. Recombinant human IgG molecules lacking Fc gamma receptor I binding and monocyte triggering activities. Eur J Immunol 1999;29: 2613-24.
33. Hikita A, Yana I, Wakeyama H, Nakamura M, Kadono Y, Oshima Y, et al. Negative regulation of osteoclastogenesis by ectodomain shedding of receptor activator of NF-kappaB ligand. J Biol Chem 2006;281: 36846-55.
34. Roodman GD. Pathogenesis of myeloma bone disease. Leukemia 2009;23: 435-41.
35. Eissner G, Kolch W, Scheurich P. Ligands working as receptors: reverse signaling by members of the TNF superfamily enhance the plasticity of the immune system. Cytokine Growth Factor Rev 2004;15: 353-66.
36. Chen NJ, Huang MW, Hsieh SL. Enhanced secretion of IFN-gamma by activated Th1 cells occurs via reverse signaling through TNF-related activation-induced cytokine. J Immunol 2001;166: 270-6.
37. Mitsiades CS, Mitsiades N, Munshi NC, Anderson KC. Focus on multiple myeloma. Cancer Cell 2004;6: 439-44.
38. Sati HI, Greaves M, Apperley JF, Russell RG, Croucher PI. Expression of interleukin-1beta and tumour necrosis factor-alpha in plasma cells from patients with multiple myeloma. Br J Haematol 1999;104: 350-7.
39. Kawano M, Tanaka H, Ishikawa H, Nobuyoshi M, Iwato K, Asaoku H, et al. Interleukin-1 accelerates autocrine growth of myeloma cells through interleukin-6 in human myeloma. Blood 1989;73: 2145-8.
40. Ma Y, Lin BR, Lin B, Hou S, Qian WZ, Li J, et al. Pharmacokinetics of CTLA4Ig fusion protein in healthy volunteers and patients with rheumatoid arthritis. Acta Pharmacol Sin 2009;30: 364-71.
41. Yonemori K, Fujiwara Y, Minami H, Kitagawa K, Fujii H, Arai T, et al. Phase 1 trial of denosumab safety, pharmacokinetics, and pharmacodynamics in Japanese women with breast cancer-related bone metastases. Cancer Sci 2008;99: 1237-42.
42. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, et al. Innate or adaptive immunity? The example of natural killer cells. Science 2011;331: 44-9.
43. Ljunggren HG, Malmberg KJ. Prospects for the use of NK cells in immunotherapy of human cancer. Nat Rev Immunol 2007;7: 329-39.
44. Koene HR, Kleijer M, Algra J, Roos D, dem Borne AE, de Haas M. Fc gammaRIIIa-158V/F polymorphism influences the binding of IgG by natural killer cell Fc gammaRIIIa, independently of the Fc gammaRIIIa- 48L/R/H phenotype. Blood 1997;90: 1109-14.
45. Maki G, Hayes GM, Naji A, Tyler T, Carosella ED, Rouas-Freiss N, et al. NK resistance of tumor cells from multiple myeloma and chronic lymphocytic leukemia patients: implication of HLA-G. Leukemia 2008;22: 998-1006.
46. Jaglowski SM, Alinari L, Lapalombella R, Muthusamy N, Byrd JC. The clinical application of monoclonal antibodies in chronic lymphocytic leukemia. Blood 2010;116: 3705-14.
47. Taylor RP, LindorferMA.Immunotherapeuticmechanisms of anti-CD20 monoclonal antibodies. Curr Opin Immunol 2008;20: 444-9.
48. Gluck WL, Hurst D, Yuen A, Levine AM, Dayton MA, Gockerman JP, et al. Phase I studies of interleukin (IL)-2 and rituximab in B-cell nonhodgkin's lymphoma: IL-2 mediated natural killer cell expansion correlations with clinical response. Clin Cancer Res 2004;10: 2253-64.
49. Bryceson YT, March ME, Ljunggren HG, Long EO. Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood 2006;107: 159-66.
50. McLaughlin P, Grillo-Lopez AJ, Link BK, Levy R, Czuczman MS, Williams ME, et al. Rituximab chimeric anti-CD20 monoclonal antibody therapy for relapsed indolent lymphoma: half of patients respond to a four-dose treatment program. J Clin Oncol 1998;16: 2825-33.