Bisphosphonate therapy in the treatment of multiple myeloma

Current Pharmaceutical Design

Volumn 16, Issue 27, 2010, Pages 3028-3036

  Lawson, M A ^a   Ashcroft, J ^b   Croucher, P I ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b PINDERFIELDS GENERAL HOSPITAL   (United Kingdom)

Author keywords

Anti resorptive; Anti tumour; Bisphosphonates; Bone; Myeloma; Osteoclasts; Osteolytic lesions

Indexed keywords

ALKALINE PHOSPHATASE; BISPHOSPHONIC ACID DERIVATIVE; CLODRONIC ACID; ETIDRONIC ACID; IBANDRONIC ACID; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; OSTEOCLAST DIFFERENTIATION FACTOR; PAMIDRONIC ACID; RISEDRONIC ACID; SCATTER FACTOR; TUMOR NECROSIS FACTOR ALPHA; ZOLEDRONIC ACID;

ALKALINE PHOSPHATASE BLOOD LEVEL; ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; BONE DISEASE; BONE LESION; BONE PAIN; CANCER MODEL; CANCER SURVIVAL; CELL ACTIVITY; CELL EXPANSION; CELL PROLIFERATION; CELL SURVIVAL; CLINICAL TRIAL; DRUG MECHANISM; HUMAN; MULTIPLE MYELOMA; MYELOMA; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUALITY OF LIFE; REVIEW; UPREGULATION; VERTEBRA FRACTURE;

ANIMALS; ANTINEOPLASTIC AGENTS; BONE DENSITY CONSERVATION AGENTS; BONE DISEASES; DIPHOSPHONATES; DRUG DESIGN; HUMANS; MULTIPLE MYELOMA; OSTEOCLASTS;

EID: 78649868193     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/138161210793563608     Document Type: Review

References (98)

1. Kyle RA, Rajkumar SV. Monoclonal gammopathies of undetermined significance: a review. Immunol Rev 2003; 194: 112-139.
2. Kyle RA, Rajkumar SV. Multiple myeloma. N Engl J Med 2004; 351(18): 1860-1873.
3. Singer CR. ABC of clinical haematology. Multiple myeloma and related conditions. BMJ 1997; 314(7085): 960-963.
4. Smith ML, Newland AC. Treatment of myeloma. QJM 1999; 92(1): 11-14.
5. Alexander DD, Mink PJ, Adami HO, et al. Multiple myeloma: a review of the epidemiologic literature. Int J Cancer 2007; 120 (Suppl 12): 40-61.
6. Brown LM, Pottern LM, Silverman DT, et al. Multiple myeloma among Blacks and Whites in the United States: role of cigarettes and alcoholic beverages. Cancer Causes Control 1997; 8(4): 610-614.
7. Smith A, Wisloff F, Samson D. Guidelines on the diagnosis and management of multiple myeloma 2005. Br J Haematol 2006; 132(4): 410-451.
8. Croucher PI, De Hendrik R, Perry MJ, et al. Zoledronic acid treatment of 5T2MM-bearing mice inhibits the development of myeloma bone disease: evidence for decreased osteolysis, tumor burden and angiogenesis, and increased survival. J Bone Miner Res 2003; 18(3): 482-492.
9. Heath DJ, Vanderkerken K, Cheng X, et al. An osteoprotegerinlike peptidomimetic inhibits osteoclastic bone resorption and osteolytic bone disease in myeloma. Cancer Res 2007; 67(1): 202-208.
10. Lawson MA, Coulton L, Ebetino FH, Vanderkerken K, Croucher PI. Geranylgeranyl transferase type II inhibition prevents myeloma bone disease. Biochem Biophys Res Commun 2008; 377(2): 453-457.
11. Libouban H, Moreau MF, Basle MF, Bataille R, Chappard D. Increased bone remodeling due to ovariectomy dramatically increases tumoral growth in the 5T2 multiple myeloma mouse model. Bone 2003; 33(3): 283-292.
12. Oyajobi BO, Franchin G, Williams PJ, et al. Dual effects of macrophage inflammatory protein-1alpha on osteolysis and tumor burden in the murine 5TGM1 model of myeloma bone disease. Blood 2003; 102(1): 311-319.
13. Pearse RN, Sordillo EM, Yaccoby S, et al. Multiple myeloma disrupts the TRANCE/ osteoprotegerin cytokine axis to trigger bone destruction and promote tumor progression. Proc Natl Acad Sci USA 2001; 98(20): 11581-11586.
14. Vanderkerken K, De Leenheer E, Shipman C, et al. Recombinant osteoprotegerin decreases tumor burden and increases survival in a murine model of multiple myeloma. Cancer Res 2003; 63(2): 287-289.
15. 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(2): 278-290.
16. Melton LJ, Kyle RA, Achenbach SJ, Oberg AL, Rajkumar SV. Fracture risk with multiple myeloma: a population-based study. J Bone Miner Res 2005; 20(3): 487-493.
17. Melton LJ, Rajkumar SV, Khosla S, Achenbach SJ, Oberg AL, Kyle RA. Fracture risk in monoclonal gammopathy of undetermined significance. J Bone Miner Res 2004; 19(1): 25-30.
18. Farrugia AN, Atkins GJ, et al. Receptor activator of nuclear factorkappaB ligand expression by human myeloma cells mediates osteoclast formation in vitro and correlates with bone destruction in vivo. Cancer Res 2003; 63(17): 5438-5445.
19. Oba Y, Lee JW, Ehrlich LA, et al. MIP-1alpha utilizes both CCR1 and CCR5 to induce osteoclast formation and increase adhesion of myeloma cells to marrow stromal cells. Exp Hematol 2005; 33(3): 272-278.
20. Oyajobi BO, Mundy GR. Receptor activator of NF-kappaB ligand, macrophage inflammatory protein-1alpha, and the proteasome: novel therapeutic targets in myeloma. Cancer 2003; 97(3 Suppl): 813-817.
21. Roodman GD, Choi SJ. MIP-1 alpha and myeloma bone disease. Cancer Treat Res 2004; 118: 83-100.
22. 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.
23. Zannettino AC, Farrugia AN, Atkins GJ. An in vitro osteoclastforming assay to measure myeloma cell-derived osteoclastactivating factors. Methods Mol Med 2005; 113: 245-256.
24. Choi SJ, Oba T, Callander NS, Jelinek DF, Roodman GD. AML-1A and AML-1B regulation of MIP-1alpha expression in multiple myeloma. Blood 2003; 101(10): 3778-3783.
25. Hjertner O, Torgersen ML, Seidel C, et al. Hepatocyte growth factor (HGF) induces interleukin-11 secretion from osteoblasts: a possible role for HGF in myeloma-associated osteolytic bone disease. Blood 1999; 94(11): 3883-3888.
26. Lichtenstein A, Berenson J, Norman D, Chang MP, Carlile A. Production of cytokines by bone marrow cells obtained from patients with multiple myeloma. Blood 1989; 74(4): 1266-1273.
27. Zhang XG, Klein B, Bataille R. Interleukin-6 is a potent myelomacell growth factor in patients with aggressive multiple myeloma. Blood 1989; 74(1): 11-13.
28. Abe M, Kido S, Hiasa M, et al. BAFF and APRIL as osteoclastderived survival factors for myeloma cells: a rationale for TACI-Fc treatment in patients with multiple myeloma. Leukemia 2006; 20(7): 1313-1315.
29. Moreaux J, Legouffe E, Jourdan E, et al. BAFF and APRIL protect myeloma cells from apoptosis induced by interleukin 6 deprivation and dexamethasone. Blood 2004; 103(8): 3148-3157.
30. Oshima T, Abe M, Asano J, et al. Myeloma cells suppress bone formation by secreting a soluble Wnt inhibitor, sFRP-2. Blood 2005; 106(9): 3160-3165.
31. Tian E, Zhan F, Walker R, et al. The role of the Wnt-signaling antagonist DKK1 in the development of osteolytic lesions in multiple myeloma. N Engl J Med 2003; 349(26): 2483-2494.
32. Qiang YW, Chen Y, Stephens O, et al. Myeloma-derived Dickkopf-1 disrupts Wnt-regulated osteoprotegerin and RANKL production by osteoblasts: a potential mechanism underlying osteolytic bone lesions in multiple myeloma. Blood 2008; 112(1): 196-207.
33. Qiang YW, Shaughnessy JD, Jr., Yaccoby S. Wnt3a signaling within bone inhibits multiple myeloma bone disease and tumor growth. Blood 2008; 112(2): 374-382.
34. Qiang YW, Chen Y, Brown N, et al. Characterization of Wnt/betacatenin signalling in osteoclasts in multiple myeloma. Br J Haematol 2010; 148(5): 726-738.
35. Rabin N, Kyriakou C, Coulton L, et al. A new xenograft model of myeloma bone disease demonstrating the efficacy of human mesenchymal stem cells expressing osteoprotegerin by lentiviral gene transfer. Leukemia 2007; 21(10): 2181-2191.
36. Body JJ, Facon T, Coleman RE, et al. A study of the biological receptor activator of nuclear factor-kappaB ligand inhibitor, denosumab, in patients with multiple myeloma or bone metastases from breast cancer. Clin Cancer Res 2006; 12(4): 1221-1228.
37. Heath DJ, Chantry AD, Buckle CH, et al. Inhibiting Dickkopf-1 (Dkk1) removes suppression of bone formation and prevents the development of osteolytic bone disease in multiple myeloma. J Bone Miner Res 2009; 24(3): 425-436.
38. Yaccoby S, Ling W, Zhan F, Walker R, Barlogie B, Shaughnessy JD, Jr. Antibody-based inhibition of DKK1 suppresses tumorinduced bone resorption and multiple myeloma growth in vivo. Blood 2007; 109(5): 2106-2111.
39. 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.
40. Berenson JR, Lichtenstein A, Porter L, et al. Long-term pamidronate treatment of advanced multiple myeloma patients reduces skeletal events. Myeloma Aredia Study Group. J Clin Oncol 1998; 16(2): 593-602.
41. Lahtinen R, Laakso M, Palva I, Virkkunen P, Elomaa I. Randomised, placebo-controlled multicentre trial of clodronate in multiple myeloma. Finnish Leukaemia Group. Lancet 1992; 340(8827): 1049-1052.
42. McCloskey EV, MacLennan IC, Drayson MT, Chapman C, Dunn J, Kanis JA. A randomized trial of the effect of clodronate on skeletal morbidity in multiple myeloma. MRC Working Party on Leukaemia in Adults. Br J Haematol 1998; 100(2): 317-325.
43. Menssen HD, Sakalova A, Fontana A, et al. Effects of long-term intravenous ibandronate therapy on skeletal-related events, survival, and bone resorption markers in patients with advanced multiple myeloma. J Clin Oncol 2002; 20(9): 2353-2359.
44. Rosen LS, Gordon D, Kaminski M, et al. Long-term efficacy and safety of zoledronic acid compared with pamidronate disodium in the treatment of skeletal complications in patients with advanced multiple myeloma or breast carcinoma: a randomized, doubleblind, multicenter, comparative trial. Cancer 2003; 98(8): 1735-1744.
45. Thompson K, Rogers MJ, Coxon FP, Crockett JC. Cytosolic entry of bisphosphonate drugs requires acidification of vesicles after fluid-phase endocytosis. Mol Pharmacol 2006; 69(5): 1624-1632.
46. Frith JC, Monkkonen J, Blackburn GM, Russell RG, Rogers MJ. Clodronate and liposome-encapsulated clodronate are metabolized to a toxic ATP analog, adenosine 5'-(beta, gamma-dichloromethylene) triphosphate, by mammalian cells in vitro. J Bone Miner Res 1997; 12(9): 1358-1367.
47. Bergstrom JD, Bostedor RG, Masarachia PJ, Reszka AA, Rodan G. Alendronate is a specific, nanomolar inhibitor of farnesyl diphosphate synthase. Arch Biochem Biophys 2000; 373(1): 231-41.
48. van Beek E, Pieterman E, Cohen L, Lowik C, Papapoulos S. Farnesyl pyrophosphate synthase is the molecular target of nitrogen-containing bisphosphonates. Biochem Biophys Res Commun 1999; 264(1): 108-11.
49. van Beek E, Pieterman E, Cohen L, Lowik C, Papapoulos S. Nitrogen-containing bisphosphonates inhibit isopentenyl pyrophosphate isomerase/farnesyl pyrophosphate synthase activity with relative potencies corresponding to their antiresorptive potencies in vitro and in vivo. Biochem Biophys Res Commun 1999; 255(2): 491-4.
50. Luckman SP, Coxon FP, Ebetino FH, Russell RG, Rogers MJ. Heterocycle-containing bisphosphonates cause apoptosis and inhibit bone resorption by preventing protein prenylation: evidence from structure-activity relationships in J774 macrophages. J Bone Miner Res 1998; 13(11): 1668-78.
51. Luckman SP, Hughes DE, Coxon FP, Graham R, Russell G, Rogers MJ. Nitrogen-containing bisphosphonates inhibit the mevalonate pathway and prevent post-translational prenylation of GTP-binding proteins, including Ras. J Bone Miner Res 1998; 13(4): 581-9.
52. Rogers MJ. New insights into the molecular mechanisms of action of bisphosphonates. Curr Pharm Des 2003; 9(32): 2643-58.
53. Russell RG, Watts NB, Ebetino FH, Rogers MJ. Mechanisms of action of bisphosphonates: similarities and differences and their potential influence on clinical efficacy. Osteoporos Int 2008; 19(6): 733-59.
54. Radl J, Croese JW, Zurcher C, et al. Influence of treatment with APD-bisphosphonate on the bone lesions in the mouse 5T2 multiple myeloma. Cancer 1985; 55(5): 1030-1040.
55. Man Z, Otero AB, Rendo P, Barazzutti L, Sanchez Avalos JC. Use of pamidronate for multiple myeloma osteolytic lesions. Lancet 1990; 335(8690): 663.
56. Thiebaud D, Leyvraz S, von Fliedner V, et al. Treatment of bone metastases from breast cancer and myeloma with pamidronate. Eur J Cancer 1991; 27(1): 37-41.
57. Dallas SL, Garrett IR, Oyajobi BO, et al. Ibandronate reduces osteolytic lesions but not tumor burden in a murine model of myeloma bone disease. Blood 1999; 93(5): 1697-1706.
58. Cruz JC, Alsina M, Craig F, et al. Ibandronate decreases bone disease development and osteoclast stimulatory activity in an in vivo model of human myeloma. Exp Hematol 2001; 29(4): 441-447.
59. Yaccoby S, Barlogie B, Epstein J. Primary myeloma cells growing in SCID-hu mice: a model for studying the biology and treatment of myeloma and its manifestations. Blood 1998; 92(8): 2908-2913.
60. Croese JW, Zurcher C, Van den Enden-Vieveen MHM, Radl J. Effect of long-term treatment with the bisphosphonate APD on 5T2 mouse multiple myeloma. In: Radl J, Van Camp B, Eds. Monoclonal gammopathies.III. Clinical significance and basic mechanisms. The Netherlands: Eurage, Leiden 1991; pp. 199-203.
61. Aparicio A, Gardner A, Tu Y, Savage A, Berenson J, Lichtenstein A. In vitro cytoreductive effects on multiple myeloma cells induced by bisphosphonates. Leukemia 1998; 12(2): 220-229.
62. Shipman CM, Rogers MJ, Apperley JF, Russell RG, Croucher PI. Bisphosphonates induce apoptosis in human myeloma cell lines: a novel anti-tumour activity. Br J Haematol 1997; 98(3): 665-672.
63. Takahashi R, Shimazaki C, Inaba T, et al. A newly developed bisphosphonate, YM529, is a potent apoptosis inducer of human myeloma cells. Leuk Res 2001; 25(1): 77-83.
64. Baulch-Brown C, Molloy TJ, Yeh SL, Ma D, Spencer A. Inhibitors of the mevalonate pathway as potential therapeutic agents in multiple myeloma. Leuk Res 2007; 31(3): 341-352.
65. Derenne S, Amiot M, Barille S, et al. Zoledronate is a potent inhibitor of myeloma cell growth and secretion of IL-6 and MMP-1 by the tumoral environment. J Bone Miner Res 1999; 14(12): 2048-2056.
66. Tassone P, Forciniti S, Galea E, et al. Growth inhibition and synergistic induction of apoptosis by zoledronate and dexamethasone in human myeloma cell lines. Leukemia 2000; 14(5): 841-844.
67. Roelofs AJ, Hulley PA, Meijer A, Ebetino FH, Russell RG, Shipman CM. Selective inhibition of Rab prenylation by a phosphonocarboxylate analogue of risedronate induces apoptosis, but not S-phase arrest, in human myeloma cells. Int J Cancer 2006; 119(6): 1254-1261.
68. Shipman CM, Croucher PI, Russell RG, Helfrich MH, Rogers MJ. The bisphosphonate incadronate (YM175) causes apoptosis of human myeloma cells in vitro by inhibiting the mevalonate pathway. Cancer Res 1998; 58(23): 5294-5297.
69. van Beek ER, Cohen LH, Leroy IM, Ebetino FH, Lowik CW, Papapoulos SE. Differentiating the mechanisms of antiresorptive action of nitrogen containing bisphosphonates. Bone 2003; 33(5): 805-811.
70. Shipman CM, Vanderkerken K, Rogers MJ, et al. The potent bisphosphonate ibandronate does not induce myeloma cell apoptosis in a murine model of established multiple myeloma. Br J Haematol 2000; 111(1): 283-286.
71. Green JR. Bisphosphonates: preclinical review. Oncologist 2004; 9 Suppl 4: 3-13.
72. Terpos E, Sezer O, Croucher PI, et al. The use of bisphosphonates in multiple myeloma: recommendations of an expert panel on behalf of the European Myeloma Network. Ann Oncol 2009; 20(8): 1303-1317.
73. Djulbegovic B, Wheatley K, Ross J, et al. Bisphosphonates in multiple myeloma. Cochrane Database Syst Rev 2002(3): CD003188.
74. Belch AR, Bergsagel DE, Wilson K, et al. Effect of daily etidronate on the osteolysis of multiple myeloma. J Clin Oncol 1991; 9(8): 1397-1402.
75. McCloskey EV, Dunn JA, Kanis JA, MacLennan IC, Drayson MT. Long-term follow-up of a prospective, double-blind, placebocontrolled randomized trial of clodronate in multiple myeloma. Br J Haematol 2001; 113(4): 1035-1043.
76. Berenson JR, Rosen LS, Howell A, et al. Zoledronic acid reduces skeletal-related events in patients with osteolytic metastases. Cancer 2001; 91(7): 1191-1200.
77. Rosen LS, Gordon D, Kaminski M, et al. Zoledronic acid versus pamidronate in the treatment of skeletal metastases in patients with breast cancer or osteolytic lesions of multiple myeloma: a phase III, double-blind, comparative trial. Cancer J 2001; 7(5): 377-387.
78. Kyle RA, Yee GC, Somerfield MR, et al. American Society of Clinical Oncology 2007 clinical practice guideline update on therole of bisphosphonates in multiple myeloma. J Clin Oncol 2007; 25(17): 2464-2472.
79. Lacy MQ, Dispenzieri A, Gertz MA, et al. Mayo clinic consensus statement for the use of bisphosphonates in multiple myeloma. Mayo Clin Proc 2006; 81(8): 1047-1053.
80. Crawford BS, McNulty RM, Kraut EH, Turowski RC. Extended use of intravenous bisphosphonate therapy for the prevention of skeletal complications in patients with cancer. Cancer Invest 2009; 27(10): 984-988.
81. Dimopoulos MA, Kastritis E, Bamia C, et al. Reduction of osteonecrosis of the jaw (ONJ) after implementation of preventive measures in patients with multiple myeloma treated with zoledronic acid. Ann Oncol 2009; 20(1): 117-120.
82. Berenson JR. Role of bisphosphonates in the management of Myeloma. Haematologica 2007; 92(Suppl. 2): abstract n. S3.3.
83. Vogel CL, Yanagihara RH, Wood AJ, et al. Safety and pain palliation of zoledronic acid in patients with breast cancer, prostate cancer, or multiple myeloma who previously received bisphosphonate therapy. Oncologist 2004; 9(6): 687-695.
84. Berenson JR, Lichtenstein A, Porter L, et al. Efficacy of pamidronate in reducing skeletal events in patients with advanced multiple myeloma. Myeloma Aredia Study Group. N Engl J Med 1996; 334(8): 488-493.
85. Wong R, Wiffen PJ. Bisphosphonates for the relief of pain secondary to bone metastases. Cochrane Database Syst Rev 2002(2): CD002068.
86. Cocks K, Cohen D, Wisloff F, et al. An international field study of the reliability and validity of a disease-specific questionnaire module (the QLQ-MY20) in assessing the quality of life of patients with multiple myeloma. Eur J Cancer 2007; 43(11): 1670-1678.
87. Carter GD, Goss AN. Bisphosphonates and avascular necrosis of the jaws. Aust Dent J 2003; 48(4): 268.
88. Khosla S, Burr D, Cauley J, et al. Bisphosphonate-associated osteonecrosis of the jaw: report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res 2007; 22(10): 1479-1491.
89. Badros A, Weikel D, Salama A, et al. Osteonecrosis of the jaw in multiple myeloma patients: clinical features and risk factors. J Clin Oncol 2006; 24(6): 945-952.
90. Dimopoulos MA, Kastritis E, Anagnostopoulos A, et al. Osteonecrosis of the jaw in patients with multiple myeloma treated with bisphosphonates: evidence of increased risk after treatment with zoledronic acid. Haematologica 2006; 91(7): 968-971.
91. Mavrokokki T, Cheng A, Stein B, Goss A. Nature and frequency of bisphosphonate-associated osteonecrosis of the jaws in Australia. J Oral Maxillofac Surg 2007; 65(3): 415-423.
92. Zervas K, Verrou E, Teleioudis Z, et al. Incidence, risk factors and management of osteonecrosis of the jaw in patients with multiple myeloma: a single-centre experience in 303 patients. Br J Haematol 2006; 134(6): 620-623.
93. Boonyapakorn T, Schirmer I, Reichart PA, Sturm I, Massenkeil G. Bisphosphonate-induced osteonecrosis of the jaws: prospective study of 80 patients with multiple myeloma and other malignancies. Oral Oncol 2008; 44(9): 857-869.
94. Weitzman R, Sauter N, Eriksen EF, et al. Critical review: updated recommendations for the prevention, diagnosis, and treatment of osteonecrosis of the jaw in cancer patients--May 2006. Crit Rev Oncol Hematol 2007; 62(2): 148-152.
95. Barker K, Rogers S. Bisphosphonate-associated Osteonecrosis of the jaws: a guide for the general dental practitioner. Dent Update 2006; 33(5): 270-272, 5.
96. Buckle CH, Neville-Webbe HL, Croucher PI, Lawson MA. Targeting RANK/RANKL in the Treatment of Solid Tumours and Myeloma. Curr Pharm Des 2010; 16(11): 1272-1283.
97. Holen I, Coleman RE. Bisphosphonates as Treatment of Bone Metastases. Curr Pharm Des 2010; 15(11): 1262-1271.
98. Uludag H. Bisphosphonates as a foundation of drug delivery to bone. Curr Pharm Des 2002; 8(21): 1929-1944.