Ulocuplumab (BMS-936564/MDX1338): A fully human anti- CXCR4 antibody induces cell death in chronic lymphocytic leukemia mediated through a reactive oxygen speciesdependent pathway

Oncotarget

Volumn 7, Issue 3, 2016, Pages 2809-2822

  Kashyap, Manoj K ^a   Kumar, Deepak ^a   Jones, Harrison ^a   Amaya Chanaga, Carlos I ^a   Choi, Michael Y ^a   Melo Cardenas, Johanna ^a   Ale Ali, Amine ^a   Kuhne, Michelle R ^c   Sabbatini, Peter ^c   Cohen, Lewis J ^c   Shelat, Suresh G ^c   Rassenti, Laura Z ^b   Kipps, Thomas J ^a,b   Cardarelli, Pina M ^c   Castro, Januario E ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b CLL Research Consortium   (United States)

^c BRISTOL MYERS SQUIBB   (United States)

Author keywords

BMS 936564; Chronic lymphocytic leukemia; CXCR4; Reactive oxygen species; Ulocuplumab

Indexed keywords

CASPASE; CHEMOKINE RECEPTOR CXCR4; F ACTIN; PLERIXAFOR; PROTEIN P53; REACTIVE OXYGEN METABOLITE; STROMAL CELL DERIVED FACTOR 1; ULOCUPLUMAB; ACTIN; ANTINEOPLASTIC AGENT; CXCL12 PROTEIN, HUMAN; CXCR4 PROTEIN, HUMAN; HETEROCYCLIC COMPOUND; IMINOSUGAR; PYRIMIDINONE DERIVATIVE; TP53 PROTEIN, HUMAN; ULODESINE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BINDING AFFINITY; CANCER PROGNOSIS; CELL ACTIVATION; CELL MIGRATION; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; DRUG CYTOTOXICITY; ENZYME ACTIVATION; HIGH RISK PATIENT; HUMAN; HUMAN CELL; MITOSIS INHIBITION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; PROTEIN TARGETING; STROMA CELL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL MOTION; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECTS; JURKAT CELL LINE; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; METABOLISM; MONONUCLEAR CELL; TUMOR CELL CULTURE;

ACTINS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; CHEMOKINE CXCL12; ENZYME ACTIVATION; HETEROCYCLIC COMPOUNDS; HUMANS; IMINO FURANOSES; JURKAT CELLS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LEUKOCYTES, MONONUCLEAR; PYRIMIDINONES; REACTIVE OXYGEN SPECIES; RECEPTORS, CXCR4; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84962209379     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6465     Document Type: Article

References (44)

1. Chiorazzi N, Rai KR, Ferrarini M. Chronic lymphocytic leukemia. N Engl J Med 2005;352:804-815.
2. Keshava Prasad TS, Goel R, Kandasamy K, Keerthikumar S, Kumar S, Mathivanan S, Telikicherla D, Raju R, Shafreen B, Venugopal A, Balakrishnan L, Marimuthu A, Banerjee S, Somanathan DS, Sebastian A, Rani S, Ray S, Harrys Kishore CJ, Kanth S, Ahmed M, Kashyap MK, Mohmood R, Ramachandra YL, Krishna V, Rahiman BA, Mohan S, Ranganathan P, Ramabadran S, Chaerkady R, Pandey A. Human Protein Reference Database-2009 update. Nucleic acids research 2009;37:D767-772.
3. Lee B, Sharron M, Montaner LJ, Weissman D, Doms RW. Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages. Proceedings of the National Academy of Sciences of the United States of America 1999;96:5215-5220.
4. Murdoch C. CXCR4: chemokine receptor extraordinaire. Immunological reviews 2000;177:175-184.
5. Teicher BA, Fricker SP. CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clinical cancer research: an official journal of the American Association for Cancer Research 2010;16:2927-2931.
6. Burger M, Hartmann T, Krome M, Rawluk J, Tamamura H, Fujii N, Kipps TJ, Burger JA. Small peptide inhibitors of the CXCR4 chemokine receptor (CD184) antagonize the activation, migration, and antiapoptotic responses of CXCL12 in chronic lymphocytic leukemia B cells. Blood 2005;106:1824-1830.
7. Balkwill F. The significance of cancer cell expression of the chemokine receptor CXCR4. Seminars in cancer biology 2004;14:171-179.
8. Burger JA, Burkle A. The CXCR4 chemokine receptor in acute and chronic leukaemia: a marrow homing receptor and potential therapeutic target. British journal of haematology 2007;137:288-296.
9. Burger JA, Tsukada N, Burger M, Zvaifler NJ, Dell'Aquila M, Kipps TJ. 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.
10. Nishio M, Endo T, Tsukada N, Ohata J, Kitada S, Reed JC, Zvaifler NJ, Kipps TJ. Nurselike cells express BAFF and APRIL, which can promote survival of chronic lymphocytic leukemia cells via a paracrine pathway distinct from that of SDF-1alpha. Blood 2005;106:1012-1020.
11. Panayiotidis P, Jones D, Ganeshaguru K, Foroni L, Hoffbrand AV. 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. Kyriakou C, Rabin N, Pizzey A, Nathwani A, Yong K. Factors that influence short-term homing of human bone marrow-derived mesenchymal stem cells in a xenogeneic animal model. Haematologica 2008;93:1457-1465.
13. Gillette JM, Larochelle A, Dunbar CE, Lippincott-Schwartz J. Intercellular transfer to signalling endosomes regulates an ex vivo bone marrow niche. Nature cell biology 2009;11:303-311.
14. Vianello F, Villanova F, Tisato V, Lymperi S, Ho KK, Gomes AR, Marin D, Bonnet D, Apperley J, Lam EW, Dazzi F. Bone marrow mesenchymal stromal cells non-selectively protect chronic myeloid leukemia cells from imatinib-induced apoptosis via the CXCR4/CXCL12 axis. Haematologica 2010;95:1081-1089.
15. Cheng Z, Zhou S, Wang X, Xie F, Wu H, Liu G, Wang Q, Chen Y, Hu Y, Lu B, Zhang X. Characterization and application of two novel monoclonal antibodies against human CXCR4: cell proliferation and migration regulation for glioma cell line in vitro by CXCR4/SDF-1alpha signal. Hybridoma 2009;28:33-41.
16. Baribaud F, Edwards TG, Sharron M, Brelot A, Heveker N, Price K, Mortari F, Alizon M, Tsang M, Doms RW. Antigenically distinct conformations of CXCR4. J Virol 2001;75:8957-8967.
17. Kuhne MR, Mulvey T, Belanger B, Chen S, Pan C, Chong C, Cao F, Niekro W, Kempe T, Henning KA, Cohen LJ, Korman AJ, Cardarelli PM. BMS-936564/MDX-1338: a fully human anti-CXCR4 antibody induces apoptosis in vitro and shows antitumor activity in vivo in hematologic malignancies. Clin Cancer Res 2013;19:357-366.
18. Karpova D, Dauber K, Spohn G, Chudziak D, Wiercinska E, Schulz M, Pettit AR, Levesque JP, Romagnoli B, Patel K, Chevalier E, Dembowsky K, Bonig H. The novel CXCR4 antagonist POL5551 mobilizes hematopoietic stem and progenitor cells with greater efficiency than Plerixafor. Leukemia 2013;27:2322-2331.
19. Förster R, Kremmer E, Schubel A, Breitfeld D, Kleinschmidt A, Nerl C, Bernhardt G, Lipp M. Intracellular and surface expression of the HIV-1 coreceptor CXCR4/fusin on various leukocyte subsets: rapid internalization and recycling upon activation. J Immunol 1998;160:1522-1531.
20. Rettig MP, Ramirez P, Nervi B, DiPersio JF. CXCR4 and mobilization of hematopoietic precursors. Methods Enzymol 2009;460:57-90.
21. Uy GL, Rettig MP, Motabi IH, McFarland K, Trinkaus KM, Hladnik LM, Kulkarni S, Abboud CN, Cashen AF, Stockerl-Goldstein KE, Vij R, Westervelt P, DiPersio JF. A phase 1/2 study of chemosensitization with the CXCR4 antagonist plerixafor in relapsed or refractory acute myeloid leukemia. Blood 2012;119:3917-3924.
22. Rosenwald A, Chuang EY, Davis RE, Wiestner A, Alizadeh AA, Arthur DC, Mitchell JB, Marti GE, Fowler DH, Wilson WH, Staudt LM. Fludarabine treatment of patients with chronic lymphocytic leukemia induces a p53-dependent gene expression response. Blood 2004;104:1428-1434.
23. Honeychurch J, Alduaij W, Azizyan M, Cheadle EJ, Pelicano H, Ivanov A, Huang P, Cragg MS, Illidge TM. Antibody-induced nonapoptotic cell death in human lymphoma and leukemia cells is mediated through a novel reactive oxygen species-dependent pathway. Blood 2012;119:3523-3533.
24. Han YH, Park WH. Tiron, a ROS scavenger, protects human lung cancer Calu-6 cells against antimycin A-induced cell death. Oncol Rep 2009;21:253-261.
25. Kim BM, Choi YJ, Han Y, Yun YS, Hong SH. N, N-dimethyl phytosphingosine induces caspase-8-dependent cytochrome c release and apoptosis through ROS generation in human leukemia cells. Toxicol Appl Pharmacol 2009;239:87-97.
26. Ten Hacken E, Burger JA. Microenvironment dependency in Chronic Lymphocytic Leukemia: The basis for new targeted therapies. Pharmacol Ther 2014;144:338-348.
27. Hutchings CJ, Koglin M, Marshall FH. Therapeutic antibodies directed at G protein-coupled receptors. mAbs 2010;2:594-606.
28. Burger JA. Nurture versus nature: the microenvironment in chronic lymphocytic leukemia. Hematology Am Soc Hematol Educ Program 2011;2011:96-103.
29. Kashyap MK A-CC, Jones H, AlMahasnah EA, Choi MY, Kuhne MR, Sabbatini P, Cohen L, Kipps TJ, Cardarelli PM, Castro JE. BMS-936564 (Anti-CXCR4 Antibody) Induces Specific Leukemia Cell Mobilization and Objective Clinical Responses In CLL Patients Treated Under a Phase I Clinical Trial. Blood 2013;21:4190.
30. Ghobrial IM, Bone ND, Stenson MJ, Novak A, Hedin KE, Kay NE, Ansell SM. Expression of the chemokine receptors CXCR4 and CCR7 and disease progression in B-cell chronic lymphocytic leukemia/small lymphocytic lymphoma. Mayo Clin Proc 2004;79:318-325.
31. Burger JA, Burger M, Kipps TJ. Chronic lymphocytic leukemia B cells express functional CXCR4 chemokine receptors that mediate spontaneous migration beneath bone marrow stromal cells. Blood 1999;94:3658-3667.
32. Möhle R, Failenschmid C, Bautz F, Kanz L. Overexpression of the chemokine receptor CXCR4 in B cell chronic lymphocytic leukemia is associated with increased functional response to stromal cell-derived factor-1 (SDF-1). Leukemia 1999;13:1954-1959.
33. Veliz M, Pinilla-Ibarz J. Treatment of relapsed or refractory chronic lymphocytic leukemia. Cancer Control 2012;19:37-53.
34. Sison E, Magoon D, Brown Patrick. Extended exposure to the CXCR4 inhibitor plerixafor may lead to enhanced microenvironment interactions in acute lymphoblastic leukemia (ALL). Blood 2013;122.
35. Endres MJ, Clapham PR, Marsh M, Ahuja M, Turner JD, McKnight A, Thomas JF, Stoebenau-Haggarty B, Choe S, Vance PJ, Wells TN, Power CA, Sutterwala SS, Doms RW, Landau NR, Hoxie JA. CD4-independent infection by HIV-2 is mediated by fusin/CXCR4. Cell 1996;87:745-756.
36. Stamatopoulos B, Meuleman N, De Bruyn C, Pieters K, Mineur P, Le Roy C, Saint-Georges S, Varin-Blank N, Cymbalista F, Bron D, Lagneaux L. AMD3100 disrupts the cross-talk between chronic lymphocytic leukemia cells and a mesenchymal stromal or nurse-like cell-based microenvironment: pre-clinical evidence for its association with chronic lymphocytic leukemia treatments. Haematologica 2012;97:608-615.
37. Kroemer G, Martin SJ. Caspase-independent cell death. Nat Med 2005;11:725-730.
38. Tait SW, Green DR. Caspase-independent cell death: leaving the set without the final cut. Oncogene 2008;27:6452-6461.
39. Matutes E, Owusu-Ankomah K, Morilla R, Garcia Marco J, Houlihan A, Que TH, Catovsky D. The immunological profile of B-cell disorders and proposal of a scoring system for the diagnosis of CLL. Leukemia 1994;8:1640-1645.
40. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 2000;284:3043-3045.
41. Kashyap MK, Kumar D, Villa R, La Clair JJ, Benner C, Sasik R, Jones H, Ghia EM, Rassenti LZ, Kipps TJ, Burkart MD, Castro JE. Targeting the spliceosome in chronic lymphocytic leukemia with the macrolides FD-895 and pladienolide-B. Haematologica 2015;100:945-954.
42. Matutes E, Attygalle A, Wotherspoon A, Catovsky D. Diagnostic issues in chronic lymphocytic leukaemia (CLL). Best Pract Res Clin Haematol 2010;23:3-20.
43. Kato K, Cantwell MJ, Sharma S, Kipps TJ. Gene transfer of CD40-ligand induces autologous immune recognition of chronic lymphocytic leukemia B cells. J Clin Invest 1998;101:1133-1141.
44. Castro JE, Prada CE, Aguillon RA, Kitada S, Fukuda T, Motta M, Wu C, Dicker F, Sun G, Wang JY, Carson DA, Reed JC, Kipps TJ. Thymidine-phosphorothioate oligonucleotides induce activation and apoptosis of CLL cells independently of CpG motifs or BCL-2 gene interference. Leukemia 2006;20:680-688.