Bruton tyrosine kinase inhibition is a novel therapeutic strategy targeting tumor in the bone marrow microenvironment in multiple myeloma

Blood

Volumn 120, Issue 9, 2012, Pages 1877-1887

  Tai, Yu Tzu ^a   Chang, Betty Y ^b   Kong, Sun Young ^a,c   Fulciniti, Mariateresa ^a   Yang, Guang ^d   Calle, Yolanda ^e   Hu, Yiguo ^a   Lin, Jianhong ^a   Zhao, Jian Jun ^a   Cagnetta, Antonia ^a   Cea, Michele ^a   Sellitto, Michael A ^a   Zhong, Mike Y ^a   Wang, Qiuju ^f   Acharya, Chirag ^a   Carrasco, Daniel R ^a,g   Buggy, Joseph J ^b   Elias, Laurence ^b   Treon, Steven P ^d   Matsui, William ^f   Richardson, Paul ^a   Munshi, Nikhil C ^a,h   Anderson, Kenneth C ^a   more..

^a HARVARD MEDICAL SCHOOL   (United States)

^b PHARMACYCLICS INC   (United States)

^c National Cancer Center   (South Korea)

^d DANA FARBER CANCER INSTITUTE   (United States)

^e KING'S COLLEGE LONDON   (United Kingdom)

^f JOHNS HOPKINS UNIVERSITY   (United States)

^g BRIGHAM AND WOMEN S HOSPITAL   (United States)

^h VA BOSTON HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IBRUTINIB; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; PHOSPHOLIPASE C GAMMA2; STROMAL CELL DERIVED FACTOR 1;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; BONE MARROW; CELL CULTURE; CELL GROWTH; CELL MIGRATION; CELL SURVIVAL; COCULTURE; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MULTIPLE MYELOMA; NONHUMAN; OSTEOCLASTOGENESIS; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; SCID MOUSE; STEM CELL; STROMA CELL; TUMOR MICROENVIRONMENT;

EID: 84865585752     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-12-396853     Document Type: Article

References (49)

1. Minter AR, Simpson H, Weiss BM, Landgren O. Bone disease from monoclonal gammopathy of undetermined significance to multiple myeloma: pathogenesis, interventions, and future opportunities. Semin Hematol. 2011;48(1):55-65.
2. Raje N, Roodman GD. Advances in the biology and treatment of bone disease in multiple myeloma. Clin Cancer Res. 2011;17(6):1278-1286.
3. de Weers M, Mensink RG, Kraakman ME, Schuurman RK, Hendriks RW. Mutation analysis of the Bruton's tyrosine kinase gene in X-linked agammaglobulinemia: identification of a mutation which affects the same codon as is altered in immunodeficient xid mice. Hum Mol Genet. 1994;3(1):161-166.
4. Qiu Y, Kung HJ. Signaling network of the Btk family kinases. Oncogene. 2000;19(49):5651-5661.
5. Conley ME, Mathias D, Treadaway J, Minegishi Y, Rohrer J. Mutations in btk in patients with presumed X-linked agammaglobulinemia. Am J Hum Genet. 1998;62(5):1034-1043.
6. Samuels J, Ng YS, Coupillaud C, Paget D, Meffre E. Human B cell tolerance and its failure in rheumatoid arthritis. Ann N Y Acad Sci. 2005;1062:116-126.
7. Koprulu AD, Ellmeier W. The role of Tec family kinases in mononuclear phagocytes. Crit Rev Immunol. 2009;29(4):317-333.
8. Di Paolo JA, Huang T, Balazs M, et al. Specific Btk inhibition suppresses B cell- and myeloid cell-mediated arthritis. Nat Chem Biol. 2011;7(1):41-50.
9. Honigberg LA, Smith AM, Sirisawad M, et al. The Bruton tyrosine kinase inhibitor PCI-32765 blocks B-cell activation and is efficacious in models of autoimmune disease and B-cell malignancy. Proc Natl Acad Sci U S A. 2010;107(29):13075-13080.
10. Hendriks RW. Drug discovery: new Btk inhibitor holds promise. Nat Chem Biol. 2011;7(1):4-5.
11. Liu L, Paolo JD, Barbosa J, Rong H, Reif K, Wong H. Antiarthritis effect of a novel Bruton's tyrosine kinase (BTK) inhibitor in rat collageninduced arthritis and mechanism-based pharmacokinetic/pharmacodynamic modeling: relationships between inhibition of BTK phosphorylation and efficacy. J Pharmacol Exp Ther. 2011;338(1):154-163.
12. Chang BY, Huang MM, Francesco M, et al. The Bruton tyrosine kinase inhibitor PCI-32765 ameliorates autoimmune arthritis by inhibition of multiple effector cells. Arthritis Res Ther. 2011;13(4):R115.
13. Weniger MA, Wiestner A. Molecular targeted approaches in mantle cell lymphoma. Semin Hematol. 2011;48(3):214-226.
14. Herman SE, Gordon AL, Hertlein E, et al. Bruton tyrosine kinase represents a promising therapeutic target for treatment of chronic lymphocytic leukemia and is effectively targeted by PCI-32765. Blood. 2011;117(23):6287- 6296.
15. Shinohara M, Koga T, Okamoto K, et al. Tyrosine kinases Btk and Tec regulate osteoclast differentiation by linking RANK and ITAM signals. Cell. 2008;132(5):794-806.
16. Lee SH, Kim T, Jeong D, Kim N, Choi Y. The tec family tyrosine kinase Btk regulates RANKL-induced osteoclast maturation. J Biol Chem. 2008;283(17):11526-11534.
17. Tai YT, Fulciniti M, Hideshima T, et al. Targeting MEK induces myeloma-cell cytotoxicity and inhibits osteoclastogenesis. Blood. 2007;110(5):1656-1663.
18. Tai YT, Dillon M, Song W, et al. Anti-CS1 humanized monoclonal antibody HuLuc63 inhibits myeloma cell adhesion and induces antibodydependent cellular cytotoxicity in the bone marrow milieu. Blood. 2008;112(4):1329-1337.
19. Tai YT, Li XF, Breitkreutz I, et al. Role of B-cell-activating factor in adhesion and growth of human multiple myeloma cells in the bone marrow microenvironment. Cancer Res. 2006;66(13):6675-6682.
20. Kim K, Kong SY, Fulciniti M, et al. Blockade of the MEK/ERK signalling cascade by AS703026, a novel selective MEK1/2 inhibitor, induces pleiotropic anti-myeloma activity in vitro and in vivo. Br J Haematol. 2010;149(4):537-549.
21. Tai YT, Podar K, Catley L, et al. Insulin-like growth factor-1 induces adhesion and migration in human multiple myeloma cells via activation of beta1-integrin and phosphatidylinositol 3′-kinase/AKT signaling. Cancer Res. 2003;63(18):5850-5858.
22. de Gorter DJ, Beuling EA, Kersseboom R, et al. Bruton's tyrosine kinase and phospholipase Cgamma2 mediate chemokine-controlled B cell migration and homing. Immunity. 2007;26(1):93-104.
23. Tassone P, Goldmacher VS, Neri P, et al. Cytotoxic activity of the maytansinoid immunoconjugate B-B4-DM1 against CD138+ multiple myeloma cells. Blood. 2004;104(12):3688-3696.
24. Neri P, Kumar S, Fulciniti MT, et al. Neutralizing B-cell activating factor antibody improves survival and inhibits osteoclastogenesis in a severe combined immunodeficient human multiple myeloma model. Clin Cancer Res. 2007;13(19):5903-5909.
25. Matsui W, Huff CA, Wang Q, et al. Characterization of clonogenic multiple myeloma cells. Blood. 2004;103(6):2332-2336.
26. Brennan SK, Wang Q, Tressler R, et al. Telomerase inhibition targets clonogenic multiple myeloma cells through telomere length-dependent and independent mechanisms. PLoS One. 2010;5(9). pii: e12487.
27. Moreaux J, Cremer FW, Reme T, et al. The level of TACI gene expression in myeloma cells is associated with a signature of microenvironment dependence versus a plasmablastic signature. Blood. 2005;106(3):1021-1030.
28. Vallet S, Mukherjee S, Vaghela N, et al. Activin A promotes multiple myeloma-induced osteolysis and is a promising target for myeloma bone disease. Proc Natl Acad Sci U S A. 2010;107(11):5124-5129.
29. Halleen JM, Alatalo SL, Suominen H, Cheng S, Janckila AJ, Vaananen HK. Tartrate-resistant acid phosphatase 5b: a novel serum marker of bone resorption. J Bone Miner Res. 2000;15(7):1337-1345.
30. Body JJ, Lipton A, Gralow J, et al. Effects of denosumab in patients with bone metastases with and without previous bisphosphonate exposure. J Bone Miner Res. 2010;25(3):440-446.
31. Chauhan D, Auclair D, Robinson EK, et al. Identification of genes regulated by dexamethasone in multiple myeloma cells using oligonucleotide arrays. Oncogene. 2002;21(9):1346-1358.
32. Alsayed Y, Ngo H, Runnels J, et al. Mechanisms of regulation of CXCR4/SDF-1 (CXCL12)-dependent migration and homing in multiple myeloma. Blood. 2007;109(7):2708-2717.
33. Fulciniti M, Tassone P, Hideshima T, et al. Anti-DKK1 mAb (BHQ880) as a potential therapeutic agent for multiple myeloma. Blood. 2009;114(2):371-379.
34. Abe M, Hiura K, Ozaki S, Kido S, Matsumoto T. Vicious cycle between myeloma cell binding to bone marrow stromal cells via VLA-4-VCAM-1 adhesion and macrophage inflammatory protein-1alpha and MIP-1beta production. J Bone Miner Metab. 2009;27(1):16-23.
35. Vallet S, Raje N, Ishitsuka K, et al. MLN3897, a novel CCR1 inhibitor, impairs osteoclastogenesis and inhibits the interaction of multiple myeloma cells and osteoclasts. Blood. 2007;110(10):3744-3752.
36. Matsumoto T, Abe M. Bone destruction in multiple myeloma. Ann N Y Acad Sci. 2006;1068:319-326.
37. Zannettino AC, Farrugia AN, Kortesidis A, et al. Elevated serum levels of stromal-derived factor-1alpha are associated with increased osteoclast activity and osteolytic bone disease in multiple myeloma patients. Cancer Res. 2005;65(5):1700-1709.
38. Diamond P, Labrinidis A, Martin SK, et al. Targeted disruption of the CXCL12/CXCR4 axis inhibits osteolysis in a murine model of myeloma-associated bone loss. J Bone Miner Res. 2009;24(7):1150-1161.
39. Takeuchi K, Abe M, Hiasa M, et al. Tgf-Beta inhibition restores terminal osteoblast differentiation to suppress myeloma growth. PLoS One. 2010;5(3):e9870.
40. Moreaux J, Veyrune JL, De Vos J, Klein B. APRIL is overexpressed in cancer: link with tumor progression. BMC Cancer. 2009;9:83.
41. Quinn J, Glassford J, Percy L, et al. APRIL promotes cell-cycle progression in primary multiple myeloma cells: influence of D-type cyclin group and translocation status. Blood. 2011;117(3):890-901.
42. Chauhan D, Singh AV, Brahmandam M, et al. Functional interaction of plasmacytoid dendritic cells with multiple myeloma cells: a therapeutic target. Cancer Cell. 2009;16(4):309-323.
43. Kline M, Donovan K, Wellik L, et al. Cytokine and chemokine profiles in multiple myeloma: significance of stromal interaction and correlation of IL-8 production with disease progression. Leuk Res. 2007;31(5):591-598.
44. Colla S, Tagliaferri S, Morandi F, et al. The new tumor-suppressor gene inhibitor of growth family member 4 (ING4) regulates the production of proangiogenic molecules by myeloma cells and suppresses hypoxia-inducible factor-1 alpha (HIF-1alpha) activity: involvement in myeloma-induced angiogenesis. Blood. 2007;110(13):4464-4475.
45. Jain N, Weinstein RS. Giant osteoclasts after long-term bisphosphonate therapy: diagnostic challenges. Nat Rev Rheumatol. 2009;5(6):341-346.
46. Weinstein RS, Roberson PK, Manolagas SC. Giant osteoclast formation and long-term oral bis-phosphonate therapy. N Engl J Med. 2009;360(1):53-62.
47. Calle Y, Jones GE, Jagger C, et al. WASp deficiency in mice results in failure to form osteoclast sealing zones and defects in bone resorption. Blood. 2004;103(9):3552-3561.
48. Danks L, Workman S, Webster D, Horwood NJ. Elevated cytokine production restores bone resorption by human Btk-deficient osteoclasts. J Bone Miner Res. 2011;26(1):182-192.
49. Matsuda T, Takahashi-Tezuka M, Fukada T, et al. Association and activation of Btk and Tec tyrosine kinases by gp130, a signal transducer of the interleukin-6 family of cytokines. Blood. 1995;85(3):627-633.