Sequential administration of the high affinity CXCR4 antagonist BKT140 promotes megakaryopoiesis and platelet production

British Journal of Haematology

Volumn 163, Issue 2, 2013, Pages 248-259

  Abraham, Michal ^a   Weiss, Ido D ^b   Wald, Hanna ^a   Wald, Ori ^b   Nagler, Arnon ^c   Beider, Katia ^c   Eizenberg, Orly ^a   Peled, Amnon ^b  

^a Science Park   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

BKT140; CXCR4; Megakaryopoiesis; Platelet production

Indexed keywords

BKT 140; CHEMOKINE RECEPTOR CXCR4 ANTAGONIST; FLUOROURACIL; GRANULOCYTE COLONY STIMULATING FACTOR; PLERIXAFOR; STROMAL CELL DERIVED FACTOR 1; THROMBOPOIETIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW; CELL COUNT; CONTROLLED STUDY; CYTOPENIA; DISEASE DURATION; DISEASE SEVERITY; DRUG DOSE COMPARISON; FEMALE; HEMATOPOIETIC STEM CELL; LEUKOCYTE COUNT; MEGAKARYOPOIESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL MOBILIZATION; THROMBOCYTOPENIA; THROMBOCYTOPOIESIS; TREATMENT OUTCOME;

BKT140; CXCR4; MEGAKARYOPOIESIS; PLATELET PRODUCTION;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOOD PLATELETS; BONE MARROW; BONE MARROW CELLS; FEMALE; HEMATOPOIETIC STEM CELLS; LEUKOCYTE COUNT; MEGAKARYOCYTE PROGENITOR CELLS; MICE; OLIGOPEPTIDES; PLATELET COUNT; RECEPTORS, CXCR4; THROMBOCYTOPENIA; THROMBOPOIESIS; THROMBOPOIETIN;

EID: 84884982900     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.12501     Document Type: Article

References (44)

1. Abraham, M., Biyder, K., Begin, M., Wald, H., Weiss, I.D., Galun, E., Nagler, A. & Peled, A. (2007) Enhanced unique pattern of hematopoietic cell mobilization induced by the CXCR4 antagonist 4F-benzoyl-TN14003. Stem Cells, 25, 2158-2166.
2. Abraham, M., Beider, K., Wald, H., Weiss, I.D., Zipori, D., Galun, E., Nagler, A., Eizenberg, O. & Peled, A. (2009) The CXCR4 antagonist 4F-benzoyl-TN14003 stimulates the recovery of the bone marrow after transplantation. Leukemia, 23, 1378-1388.
3. Anderlini, P., Przepiorka, D., Seong, D., Miller, P., Sundberg, J., Lichtiger, B., Norfleet, F., Chan, K.W., Champlin, R. & Korbling, M. (1996) Clinical toxicity and laboratory effects of granulocyte-colony-stimulating factor (filgrastim) mobilization and blood stem cell apheresis from normal donors, and analysis of charges for the procedures. Transfusion, 36, 590-595.
4. Bedell, C. (2003) Pegfilgrastim for chemotherapy-induced neutropenia. Clin J Oncol Nurs, 7, 55-56, 63-64.
5. Blajchman, M.A., Slichter, S.J., Heddle, N.M. & Murphy, M.F. (2008) New strategies for the optimal use of platelet transfusions. Hematology Am Soc Hematol Educ Program, 2008, 198-204.
6. Bleul, C.C., Farzan, M., Choe, H., Parolin, C., Clark-Lewis, I., Sodroski, J. & Springer, T.A. (1996) The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature, 382, 829-833.
7. Bolan, C.D., Carter, C.S., Wesley, R.A., Yau, Y.Y., Barrett, A.J., Childs, R.W., Read, E.J. & Leitman, S.F. (2003) Prospective evaluation of cell kinetics, yields and donor experiences during a single large-volume apheresis versus two smaller volume consecutive day collections of allogeneic peripheral blood stem cells. British Journal of Haematology, 120, 801-807.
8. Cashman, J., Clark-Lewis, I., Eaves, A. & Eaves, C. (2002) Stromal-derived factor 1 inhibits the cycling of very primitive human hematopoietic cells in vitro and in NOD/SCID mice. Blood, 99, 792-799.
9. Dale, D.C. (2002) Colony-stimulating factors for the management of neutropenia in cancer patients. Drugs, 62, 1-15.
10. Devine, S.M., Flomenberg, N., Vesole, D.H., Liesveld, J., Weisdorf, D., Badel, K., Calandra, G. & DiPersio, J.F. (2004) Rapid mobilization of CD34 + cells following administration of the CXCR4 antagonist AMD3100 to patients with multiple myeloma and non-Hodgkin's lymphoma. Journal of Clinical Oncology, 22, 1095-1102.
11. Flomenberg, N., Devine, S.M., Dipersio, J.F., Liesveld, J.L., McCarty, J.M., Rowley, S.D., Vesole, D.H., Badel, K. & Calandra, G. (2005) The use of AMD3100 plus G-CSF for autologous hematopoietic progenitor cell mobilization is superior to G-CSF alone. Blood, 106, 1867-1874.
12. Fricker, S.P., Anastassov, V., Cox, J., Darkes, M.C., Grujic, O., Idzan, S.R., Labrecque, J., Lau, G., Mosi, R.M., Nelson, K.L., Qin, L., Santucci, Z. & Wong, R.S. (2006) Characterization of the molecular pharmacology of AMD3100: a specific antagonist of the G-protein coupled chemokine receptor, CXCR4. Biochemical Pharmacology, 72, 588-596.
13. Gibellini, D., Bassini, A., Re, M.C., Ponti, C., Miscia, S., Gonelli, A., La Placa, M. & Zauli, G. (2000) Stroma-derived factor 1alpha induces a selective inhibition of human erythroid development via the functional upregulation of Fas/CD95 ligand. British Journal of Haematology, 111, 432-440.
14. Hamada, T., Mohle, R., Hesselgesser, J., Hoxie, J., Nachman, R.L., Moore, M.A. & Rafii, S. (1998) Transendothelial migration of megakaryocytes in response to stromal cell-derived factor 1 (SDF-1) enhances platelet formation. Journal of Experimental Medicine, 188, 539-548.
15. Hatano, R., Takano, F., Fushiya, S., Michimata, M., Tanaka, T., Kazama, I., Suzuki, M. & Matsubara, M. (2004) Water-soluble extracts from Angelica acutiloba Kitagawa enhance hematopoiesis by activating immature erythroid cells in mice with 5-fluorouracil-induced anemia. Experimental Hematology, 32, 918-924.
16. Hendrix, C.W., Collier, A.C., Lederman, M.M., Schols, D., Pollard, R.B., Brown, S., Jackson, J.B., Coombs, R.W., Glesby, M.J., Flexner, C.W., Bridger, G.J., Badel, K., MacFarland, R.T., Henson, G.W. & Calandra, G. (2004) Safety, pharmacokinetics, and antiviral activity of AMD3100, a selective CXCR4 receptor inhibitor, in HIV-1 infection. Journal of Acquired Immune Deficiency Syndromes, 37, 1253-1262.
17. Hodohara, K., Fujii, N., Yamamoto, N. & Kaushansky, K. (2000) Stromal cell-derived factor-1 (SDF-1) acts together with thrombopoietin to enhance the development of megakaryocytic progenitor cells (CFU-MK). Blood, 95, 769-775.
18. Jacobson, O., Weiss, I.D., Kiesewetter, D.O., Farber, J.M. & Chen, X. (2010) PET of tumor CXCR4 expression with 4-18F-T140. Journal of Nuclear Medicine, 51, 1796-1804.
19. Jacobson, O., Weiss, I.D., Szajek, L.P., Niu, G., Ma, Y., Kiesewetter, D.O., Farber, J.M. & Chen, X. (2011) PET imaging of CXCR4 using copper-64 labeled peptide antagonist. Theranostics, 1, 251-262.
20. Kaushansky, K., Lok, S., Holly, R.D., Broudy, V.C., Lin, N., Bailey, M.C., Forstrom, J.W., Buddle, M.M., Oort, P.J., Hagen, F.S., Roth, G.J., Papayannopoulou, T. & Foster, D.C. (1994) Promotion of megakaryocyte progenitor expansion and differentiation by the c-Mpl ligand thrombopoietin. Nature, 369, 568-571.
21. Kowalska, M.A., Ratajczak, J., Hoxie, J., Brass, L.F., Gewirtz, A., Poncz, M. & Ratajczak, M.Z. (1999) Megakaryocyte precursors, megakaryocytes and platelets express the HIV co-receptor CXCR4 on their surface: determination of response to stromal-derived factor-1 by megakaryocytes and platelets. British Journal of Haematology, 104, 220-229.
22. Kraemer, B.F., Borst, O., Gehring, E.M., Schoenberger, T., Urban, B., Ninci, E., Seizer, P., Schmidt, C., Bigalke, B., Koch, M., Martinovic, I., Daub, K., Merz, T., Schwanitz, L., Stellos, K., Fiesel, F., Schaller, M., Lang, F., Gawaz, M. & Lindemann, S. (2010) PI3 kinase-dependent stimulation of platelet migration by stromal cell-derived factor 1 (SDF-1). Journal of Molecular Medicine (Berlin), 88, 1277-1288.
23. Lane, W.J., Dias, S., Hattori, K., Heissig, B., Choy, M., Rabbany, S.Y., Wood, J., Moore, M.A. & Rafii, S. (2000) Stromal-derived factor 1-induced megakaryocyte migration and platelet production is dependent on matrix metalloproteinases. Blood, 96, 4152-4159.
24. Li, J., Yang, C., Xia, Y., Bertino, A., Glaspy, J., Roberts, M. & Kuter, D.J. (2001) Thrombocytopenia caused by the development of antibodies to thrombopoietin. Blood, 98, 3241-3248.
25. Liles, W.C., Broxmeyer, H.E., Rodger, E., Wood, B., Hubel, K., Cooper, S., Hangoc, G., Bridger, G.J., Henson, G.W., Calandra, G. & Dale, D.C. (2003) Mobilization of hematopoietic progenitor cells in healthy volunteers by AMD3100, a CXCR4 antagonist. Blood, 102, 2728-2730.
26. Majka, M., Janowska-Wieczorek, A., Ratajczak, J., Kowalska, M.A., Vilaire, G., Pan, Z.K., Honczarenko, M., Marquez, L.A., Poncz, M. & Ratajczak, M.Z. (2000) Stromal-derived factor 1 and thrombopoietin regulate distinct aspects of human megakaryopoiesis. Blood, 96, 4142-4151.
27. Nagasawa, T., Kikutani, H. & Kishimoto, T. (1994) Molecular cloning and structure of a pre-B-cell growth-stimulating factor. Proceedings of the National Academy of Sciences of the United States of America, 91, 2305-2309.
28. Nagler, A., Shimoni, A., Avivi, I., Rowe, J.M., Beider, K., Hardan, I., Abraham, M., Wald, H., Galun, E., Shaw, H.L., Eizenberg, O. & Peled, A. (2010) BKT140 Is a Novel CXCR4 Antagonist with Stem Cell Mobilization and Antimyeloma Effects: An Open-Label First Human Trial In Patients with Multiple Myeloma Undergoing Stem Cell Mobilization for Autologous Transplantation. Blood (ASH Annual Meeting Abstracts), 116, 2260.
29. Peled, A., Wald, O. & Burger, J. (2012) Development of novel CXCR4-based therapeutics. Expert Opinion on Investigational Drugs, 21, 341-353.
30. Pitchford, S.C., Lodie, T. & Rankin, S.M. (2012) VEGFR1 stimulates a CXCR4-dependent translocation of megakaryocytes to the vascular niche, enhancing platelet production in mice. Blood, 120, 2787-2795.
31. Rich, I.N. (1991) The effect of 5-fluorouracil on erythropoiesis. Blood, 77, 1164-1170.
32. Rossi, D. & Zlotnik, A. (2000) The biology of chemokines and their receptors. Annual Review of Immunology, 18, 217-242.
33. Stroncek, D.F., Clay, M.E., Petzoldt, M.L., Smith, J., Jaszcz, W., Oldham, F.B. & McCullough, J. (1996a) Treatment of normal individuals with granulocyte-colony-stimulating factor: donor experiences and the effects on peripheral blood CD34 + cell counts and on the collection of peripheral blood stem cells. Transfusion, 36, 601-610.
34. Stroncek, D.F., Clay, M.E., Smith, J., Ilstrup, S., Oldham, F. & McCullough, J. (1996b) Changes in blood counts after the administration of granulocyte-colony-stimulating factor and the collection of peripheral blood stem cells from healthy donors. Transfusion, 36, 596-600.
35. Stroncek, D.F., Clay, M.E., Jaszcz, W., Lennon, S., Smith, J. & McCullough, J. (1999) Collection of two peripheral blood stem cell concentrates from healthy donors. Transfusion Medicine (Oxford, England), 9, 37-50.
36. Takatsuki, F., Miyasaka, Y., Kikuchi, T., Suzuki, M. & Hamuro, J. (1996) Improvement of erythroid toxicity by lentinan and erythropoietin in mice treated with chemotherapeutic agents. Experimental Hematology, 24, 416-422.
37. Tamamura, H., Hori, A., Kanzaki, N., Hiramatsu, K., Mizumoto, M., Nakashima, H., Yamamoto, N., Otaka, A. & Fujii, N. (2003) T140 analogs as CXCR4 antagonists identified as anti-metastatic agents in the treatment of breast cancer. FEBS Letters, 550, 79-83.
38. Tamamura, H., Fujisawa, M., Hiramatsu, K., Mizumoto, M., Nakashima, H., Yamamoto, N., Otaka, A. & Fujii, N. (2004) Identification of a CXCR4 antagonist, a T140 analog, as an anti-rheumatoid arthritis agent. FEBS Letters, 569, 99-104.
39. Trent, J.O., Wang, Z.X., Murray, J.L., Shao, W., Tamamura, H., Fujii, N. & Peiper, S.C. (2003) Lipid bilayer simulations of CXCR4 with inverse agonists and weak partial agonists. Journal of Biological Chemistry, 278, 47136-47144.
40. Vadhan-Raj, S. (2000) Clinical experience with recombinant human thrombopoietin in chemotherapy-induced thrombocytopenia. Seminars in Hematology, 37, 28-34.
41. Vadhan-Raj, S. (2009) Management of chemotherapy-induced thrombocytopenia: current status of thrombopoietic agents. Seminars in Hematology, 46, S26-S32.
42. Wang, J.F., Liu, Z.Y. & Groopman, J.E. (1998) The alpha-chemokine receptor CXCR4 is expressed on the megakaryocytic lineage from progenitor to platelets and modulates migration and adhesion. Blood, 92, 756-764.
43. Weiterova, L., Hofer, M., Pospisil, M., Znojil, V., Vacha, J., Vacek, A. & Pipalova, I. (2000) Influence of the joint treatment with granulocyte colony-stimulating factor and drugs elevating extracellular adenosine on erythropoietic recovery following 5-fluorouracil-induced haematotoxicity in mice. European Journal of Haematology, 65, 310-316.
44. Zhang, W.B., Navenot, J.M., Haribabu, B., Tamamura, H., Hiramatu, K., Omagari, A., Pei, G., Manfredi, J.P., Fujii, N., Broach, J.R. & Peiper, S.C. (2002) A point mutation that confers constitutive activity to CXCR4 reveals that T140 is an inverse agonist and that AMD3100 and ALX40-4C are weak partial agonists. Journal of Biological Chemistry, 277, 24515-24521.