The critical role of bisphosphonates to target bone cancer metastasis: an overview

References

• Bray F, Jemal A, Grey N, et al. Global cancer transitions according to the Human Development Index (2008–2030): a population-based study. Lancet Oncol 2012;13:790–801
   PubMed Web of Science ®Google Scholar
• Roodman GD. Mechanisms of bone metastasis. New Engl J Med 2004;350:1655–64
   PubMed Web of Science ®Google Scholar
• Coleman R. The use of bisphosphonates in cancer treatment. Ann New York Acad Sci 2011;1218:3–14
   PubMed Web of Science ®Google Scholar
• Ara T, De Clerck YA. Interleukin-6 in bone metastasis and cancer progression. Eur J Cancer 2010;46:1223–31
   PubMed Web of Science ®Google Scholar
• Padalecki SS, Guise TA. Actions of bisphosphonates in animal models of breast cancer. Breast Cancer Res 2002;4:35–41
   PubMed Web of Science ®Google Scholar
• Clarke B. Normal bone anatomy and physiology. Clin J Am Soc Nephrology 2008;3:S131–9
   PubMed Web of Science ®Google Scholar
• Sosnoski DM, Krishnan V, Kraemer WJ, et al. Changes in cytokines of the bone microenvironment during breast cancer metastasis. Int J Breast Cancer 2012;2012:1–9
   Google Scholar
• Roelofs AJ, Thompson K, Gordon S, Rogers MJ. Molecular mechanisms of action of bisphosphonates: current status. Clin Cancer Res 2006;12:6222s–30s
   PubMed Web of Science ®Google Scholar
• Rebucci M, Michiels C. Molecular aspects of cancer cell resistance to chemotherapy. Biochem Pharmacol 2013;85:1219–26
   PubMed Web of Science ®Google Scholar
• Wu CP, Hsieh CH, Wu YS. The emergence of drug transporter-mediated multidrug resistance to cancer chemotherapy. Mol Pharm 2011;8:1996–2011
   PubMed Web of Science ®Google Scholar
• Xu L, Li H, Wang Y, et al. Enhanced activity of doxorubicin in drug resistant A549 tumor cells by encapsulation of P glycoprotein inhibitor in PLGA based nanovectors. Oncol Lett 2013;7:387–92
   PubMed Web of Science ®Google Scholar
• Heymann D, Ory B, Gouin F, et al. Bisphosphonates: new therapeutic agents for the treatment of bone tumors. Trend Mol Med 2004;10:337–43
   PubMed Web of Science ®Google Scholar
• Rogers, MJ. New insights into the molecular mechanisms of action of bisphosphonates. Curr Pharm Des 2003;9:2643–58
   PubMedGoogle Scholar
• Monkkonen H, Rogers MJ, Makkonen N, et al. The cellular uptake and metabolism of clodronate in RAW 264 macrophages. Pharm Res 2011;18:1550–5
   Web of Science ®Google Scholar
• Lane KT, Beese LS. Thematic review series: lipid posttranslational modifications. Structural biology of protein farnesyltransferase and geranylgeranyltransferase type I. J Lipid Res 2006;47:681–99
   PubMed Web of Science ®Google Scholar
• McTaggart S. Isoprenylated proteins. Cell Mol Life Sci 2006;63:255–67
   PubMed Web of Science ®Google Scholar
• Alakangas A, Selander K, Mulari M, et al. Alendronate disturbs vesicular trafficking in osteoclasts. Calcif Tissue Int 2002;70:40–7
   PubMed Web of Science ®Google Scholar
• Ohno K, Mori K, Orita M, Takeuchi M. Computational insights into binding of bisphosphates to farnesyl pyrophosphate synthase. Curr Med Chem 2011;18:220–33
   PubMed Web of Science ®Google Scholar
• Casimiro S, Guise TA, Chirgwin J. The critical role of the bone microenvironment in cancer metastases. Mol Cell Endocrinol 2009;310:71–81
   PubMed Web of Science ®Google Scholar
• Yoneda T, Hiraga T. Crosstalk between cancer cells and bone microenvironment in bone metastasis. Biochem Biophys Res Commun 2005;328:679–87
   PubMed Web of Science ®Google Scholar
• Schmalhofer O, Brabletz S, Brabletz T. E-cadherin, β-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev 2009;28:151–66
   PubMed Web of Science ®Google Scholar
• Chu K, Cheng CJ, Ye X, et al. Cadherin-11 promotes the metastasis of prostate cancer cells to bone. Mol Cancer Res 2008;6:1259–67
   PubMed Web of Science ®Google Scholar
• Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer, trials and tribulations. Science 2002;295:2387–92
   PubMed Web of Science ®Google Scholar
• Makrilia N, Kollias A, Manolopoulos L, Syrigos K. Cell adhesion molecules: role and clinical significance in cancer. Cancer Invest 2009;27:1023–37
   PubMed Web of Science ®Google Scholar
• Aft R, Perez J-R, Raje N, et al. Could targeting bone delay cancer progression? Potential mechanisms of action of bisphosphonates. Crit Rev Oncol Hematol 2012;82:233–48
   PubMed Web of Science ®Google Scholar
• Eyles J, Puaux A-L, Wang X, et al. Tumor cells disseminate early, but immunosurveillance limits metastatic outgrowth, in a mouse model of melanoma. J Clin Invest 2010;120:2030–9
   PubMed Web of Science ®Google Scholar
• Kim M-Y, Oskarsson T, Acharyya S, et al. Tumor self-seeding by circulating cancer cells. Cell 2009;139:1315–26
   PubMed Web of Science ®Google Scholar
• Coghlin C, Murray GI. Current and emerging concepts in tumour metastasis. J Pathol 2010;222:1–15
   PubMed Web of Science ®Google Scholar
• Bellahcene A, Bachelier R, Detry C, et al. Transcriptome analysis reveals an osteoblast-like phenotype for human osteotropic breast cancer cells. Breast Cancer Res Tr 2007;101:135–48
   PubMed Web of Science ®Google Scholar
• Rucci N, Teti A. Osteomimicry: how tumor cells try to deceive the bone. Front Biosci 2010;2:907–15
   Google Scholar
• Weilbaecher KN, Guise TA, McCauley LK. Cancer to bone: a fatal attraction. Nat Rev Cancer 2011;11:411–25
   PubMed Web of Science ®Google Scholar
• Lipton A, Jun S. RANKL inhibition in the treatment of bone metastases. Curr Opin Support Palliat Care 2008;2:197–203
   PubMedGoogle Scholar
• Wong M, Pavlakis N. Optimal management of bone metastases in breast cancer patients. Breast Cancer Target Ther 2011;3:35–60
   PubMedGoogle Scholar
• Terpos E, Efstathiou E, Christoulas D, et al. RANKL inhibition: clinical implications for the management of patients with multiple myeloma and solid tumors with bone metastases. Expert Opin Bio Ther 2009;9:465–79
   PubMed Web of Science ®Google Scholar
• Meads MB, Hazlehurst LA, Dalton WS. The bone marrow microenvironment as a tumor sanctuary and contributor to drug resistance. Clin Cancer Res 2008;14:2519–26
   PubMed Web of Science ®Google Scholar
• Shiozawa Y, Havens A, Pienta K, Taichman R. The bone marrow niche: habitat to hematopoietic and mesenchymal stem cells, and unwitting host to molecular parasites. Leukemia 2008;22:941–50
   PubMed Web of Science ®Google Scholar
• Corso A, Ferretti E, Lazzarino M. Zoledronic acid exerts its antitumor effect in multiple myeloma interfering with the bone marrow microenvironment. Hematology 2005;10:215–24
   PubMed Web of Science ®Google Scholar
• Shaked Y, Voest EE. Bone marrow derived cells in tumor angiogenesis and growth: are they the good, the bad or the evil? Biochimica Biophys Acta Rev Cancer 2009;1796:1–4
   PubMed Web of Science ®Google Scholar
• Li Calzi S, Neu MB, Shaw LC, et al. EPCs and pathological angiogenesis: when good cells go bad. Microvasc Res 2010;79:207–16
   PubMed Web of Science ®Google Scholar
• Araki K, Sangai T, Miyamoto Si, et al. Inhibition of bone-derived insulin-like growth factors by a ligand-specific antibody suppresses the growth of human multiple myeloma in the human adult bone explanted in NOD/SCID mouse. Int J Cancer 2006;118:2602–8
   PubMed Web of Science ®Google Scholar
• Kimura T, Kuwata T, Ashimine S, et al. Targeting of bone-derived insulin-like growth factor-II by a human neutralizing antibody suppresses the growth of prostate cancer cells in a human bone environment. Clin Cancer Res 2010;16:121–9
   PubMed Web of Science ®Google Scholar
• Normanno N, Gallo M, Lamura L, De Luca A. Effect of zoledronic acid acts on the interaction between mesenchymal stem cells and breast cancer cells within the bone microenvironment. J Clin Oncol 2012;82:233–48
   Google Scholar
• Allgayer H, Aguirre-Ghiso JA. The urokinase receptor (u-PAR) – a link between tumor cell dormancy and minimal residual disease in bone marrow? APMIS 2008;116:602–14
   PubMed Web of Science ®Google Scholar
• Suzuki M, Mose ES, Montel V, Tarin D. Dormant cancer cells retrieved from metastasis-free organs regain tumorigenic and metastatic potency. Am J Pathol 2006;169:673–81
   PubMed Web of Science ®Google Scholar
• Reuben JM, Lee BN, Gao H, et al. Primary breast cancer patients with high risk clinicopathologic features have high percentages of bone marrow epithelial cells with ALDH activity and CD44(+)CD24(lo) cancer stem cell phenotype. Eur J Cancer 2011;47:1527–36
   PubMed Web of Science ®Google Scholar
• Watson MA, Ylagan LR, Trinkaus KM. Isolation and molecular profiling of bone marrow micrometastases identifies TWIST1 as a marker of early tumor relapse in breast cancer patients. Clin Cancer Res 2007;13:5001–9
   PubMed Web of Science ®Google Scholar
• Liu W, Hajibeigi A, Lin M, et al. An osteoclast-targeting agent for imaging and therapy of bone metastasis. Bioorg Med Chem Lett 2008;18:4789–93
   PubMed Web of Science ®Google Scholar
• Muller V, Stahmann N, Riethdorf S, et al. Circulating tumor cells in breast cancer: correlation to bone marrow micrometastases, heterogeneous response to systemic therapy and low proliferative activity. Clin Cancer Res 2005;11:3678–85
   PubMed Web of Science ®Google Scholar
• Braun S, Vogl FD, Naume B. A pooled analysis of bone marrow micrometastasis in breast cancer. N Engl J Med 2005;353:793–802
   PubMed Web of Science ®Google Scholar
• Schindlbeck C, Kampik T, Janni W. Prognostic relevance of disseminated tumor cells in the bone marrow and biological factors of 65 primary breast carcinomas. Breast Cancer Res 2005;7:1174–85
   Web of Science ®Google Scholar
• Berg A, Berner A, Lilleby W, et al. Impact of disseminated tumor cells in bone marrow at diagnosis in patients with nonmetastatic prostate cancer treated by definitive radiotherapy. Int J Cancer 2007;120:1603–9
   PubMed Web of Science ®Google Scholar
• Bidard F-C, Kirova Y, Vincent-Salomon A, et al. Disseminated tumor cells and the risk of locoregional recurrence in nonmetastatic breast cancer. Ann Oncol 2009;20:1836–41
   PubMed Web of Science ®Google Scholar
• Bidard FC, Vincent-Salomon A, Gomme S, et al. Disseminated tumor cells of breast cancer patients: a strong prognostic factor for distant and local relapse. Clin Cancer Res 2008;14:3306–11
   PubMed Web of Science ®Google Scholar
• Brunsvig PF, Flatmark K, Aamdal S, et al. Bone marrow micrometastases in advanced stage non-small cell lung carcinoma patients. Lung Cancer 2008;61:170–6
   PubMed Web of Science ®Google Scholar
• Cristofanilli M, Hayes DF, Budd GT, et al. Circulating tumor cells: a novel prognostic factor for newly diagnosed metastatic breast cancer. J Clin Oncol 2005;23:1420–30
   PubMed Web of Science ®Google Scholar
• Garcia JA, Rosenberg JE, Weinberg V, et al. Evaluation and significance of circulating epithelial cells in patients with hormone-refractory prostate cancer. BJU Int 2007;99:519–24
   PubMed Web of Science ®Google Scholar
• Kollermann J, Weikert S, Schostak M, et al. Prognostic significance of disseminated tumor cells in the bone marrow of prostate cancer patients treated with neoadjuvant hormone treatment. J Clin Oncol 2008;26:4928–33
   PubMed Web of Science ®Google Scholar
• Morgan TM, Lange PH, Porter MP, et al. Disseminated tumor cells in prostate cancer patients after radical prostatectomy and without evidence of disease predicts biochemical recurrence. Clin Cancer Res 2009;15:677–83
   PubMed Web of Science ®Google Scholar
• Kakonen SM, Mundy GR. Mechanisms of osteolytic bone metastases inbreast carcinoma. Cancer 2003;97:834–9
   PubMed Web of Science ®Google Scholar
• Zhang Y, Ma B, Fan Q. Mechanisms of breast cancer bone metastasis. Cancer Lett 2010;292:1–7
   PubMed Web of Science ®Google Scholar
• Boyce BF, Xing L. Biology of RANK, RANKL, and osteoprotegerin. Arthrit Res Ther 2007;9:S1
   PubMed Web of Science ®Google Scholar
• De Marinis F, Eberhardt W, Harper PG, et al. Bisphosphonate use in patients with lung cancer and bone metastases: recommendations of a European expert panel. J Thorac Oncol 2009;4:1280–8
   PubMed Web of Science ®Google Scholar
• Russell RGG. Bisphosphonates: The first 40 years. Bone 2011;49:2–19
   PubMed Web of Science ®Google Scholar
• Aapro M, Saad F, Costa L. Optimizing clinical benefits of bisphosphonates in cancer patients with bone metastases. The Oncologist 2010;15:1147–58
   PubMed Web of Science ®Google Scholar
• Costa L, Major PP. Effect of bisphosphonates on pain and quality of life in patients with bone metastases. Nature Clin Pract Oncol 2009;6:163–74
   PubMedGoogle Scholar
• Lawson M, Xia Z, Barnett B, et al. Differences between bisphosphonates in binding affinities for hydroxyapatite. J Biomed Mat Res 2010;92:149–55
   Web of Science ®Google Scholar
• Bridges EM, Harris AL. The angiogenic process as a therapeutic target in cancer. Biochem Pharmacol 2011;81:1183–91
   PubMed Web of Science ®Google Scholar
• Clézardin P, Benzaïd I, Croucher PI. Bisphosphonates in preclinical bone oncology. Bone 2011;49:66–70
   PubMed Web of Science ®Google Scholar
• Fitch M, Maxwell C, Ryan C, et al. Bone metastases from advanced cancers. Clin J Oncol Nur 2009;13:701–10
   PubMed Web of Science ®Google Scholar
• Saag KG, Geusens P. Progress in osteoporosis and fracture prevention: focus on postmenopausal women. Arthritis Res Ther 2009;11:420–425
   Web of Science ®Google Scholar
• Zeisberger SM, Odermatt B, Marty C, et al. Clodronate-liposome-mediated depletion of tumourassociated macrophages: a new and highly effective antiangiogenic therapy approach. Br J Cancer 2006;95:272–81
   PubMed Web of Science ®Google Scholar
• Hafeman S, London C, Elmslie R, Dow S. Evaluation of liposomal clodronate for treatment of malignant histiocytosis in dogs. Cancer Immun Immunother 2010;59:441–52
   PubMed Web of Science ®Google Scholar
• Lipton A, Cook RJ, Major P, et al. Zoledronic acid and survival in breast cancer patients with bone metastases and elevated markers of osteoclast activity. Oncologist 2007;12:1035–43
   PubMed Web of Science ®Google Scholar
• Machado M, Cruz LS, Tannus G, Fonseca M. Efficacy of clodronate, pamidronate, and zoledronate in reducing morbidity and mortality in cancer patients with bone metastasis: a meta-analysis of randomized clinical trials. Clin Ther 2009;31:962–79
   PubMed Web of Science ®Google Scholar
• Miller K, Eldar-Boock A, Polyak D, et al. Antiangiogenic antitumor activity of HPMA copolymer–paclitaxel– alendronate conjugate on breast cancer bone metastasis mouse model. Mol Pharm 2011;8:1052–62
   PubMed Web of Science ®Google Scholar
• Thamake SI, Raut SL, Gryczynski Z, et al. Alendronate coated poly-lactic-co-glycolic acid (PLGA) nanoparticles for active targeting of metastatic breast cancer. Biomaterials 2012;33:7164–73
   PubMed Web of Science ®Google Scholar
• Katsumi H, Nakatani M, Sano J-I, et al. Absorption and safety of alendronate, a nitrogen-containing bisphosphonate, after intrapulmonary administration in rats. Int J Pharm 2010;400:124–30
   PubMed Web of Science ®Google Scholar
• Naniwa T, Maeda T, Mizoshita T, et al. Alendronate-induced esophagitis: possible pathogenic role of hypersensitivity to alendronate. Int Med (Tokyo, Japan) 2008;47:2083–5
   PubMed Web of Science ®Google Scholar
• Marra M, Salzano G, Leonetti C, et al. Nanotechnologies to use bisphosphonates as potent anticancer agents: the effects of zoledronic acid encapsulated into liposomes. Nanomedicine 2011;7:955–64
   PubMed Web of Science ®Google Scholar
• Sevcik MA, Luger NM, Mach DB, et al. Bone cancer pain: the effects of the bisphosphonate alendronate on pain, skeletal remodeling, tumor growth and tumor necrosis. Pain 2004;111:169–80
   PubMed Web of Science ®Google Scholar
• Wang G, Mostafa NZ, Incani V, et al. Bisphosphonate-decorated lipid nanoparticles designed as drug carriers for bone diseases. J Biomed Mat Res 2012;100:684–93
   Web of Science ®Google Scholar
• Baliga MS, Meleth S, Katiyar SK. Growth inhibitory and antimetastatic effect of green tea polyphenols on metastasis-specific mouse mammary carcinoma 4T1 cells in vitro and in vivo systems. Clin Cancer Res 2005;11:1918–27
   PubMed Web of Science ®Google Scholar
• Body J-J, Diel I, Lichinitzer M, et al. Oral ibandronate reduces the risk of skeletal complications in breast cancer patients with metastatic bone disease: results from two randomised, placebo-controlled phase III studies. Brit J Cancer 2004;90:1133–7
   PubMed Web of Science ®Google Scholar
• Choo R, Lukka H, Cheung P, et al. Randomized, double-blinded, placebo-controlled, trial of risedronate for the prevention of bone mineral density loss in nonmetastatic prostate cancer patients receiving radiation therapy plus androgen deprivation therapy. Int J Radiat Oncol Biol Phys 2013;85:1239–45
   PubMed Web of Science ®Google Scholar
• Nancollas G, Tang R, Phipps R, et al. Novel insights into actions of bisphosphonates on bone: differences in interactions with hydroxyapatite. Bone 2006;38:617–27
   PubMed Web of Science ®Google Scholar
• He M, Fan W, Zhang X. Adjuvant zoledronic acid therapy for patients with early stage breast cancer: an updated systematic review and meta-analysis. J Hematol Oncol 2013;6:1–8
   PubMed Web of Science ®Google Scholar
• Hirbe AC, Roelofs AJ, Floyd DH, et al. The bisphosphonate zoledronic acid decreases tumor growth in bone in mice with defective osteoclasts. Bone 2009;44:908–16
   PubMed Web of Science ®Google Scholar
• Krempien R, Niethammer A, Harms W, Debus J. Bisphosphonates and bone metastases: current status and future directions. Expert Rev 2005;5:295–305
   Web of Science ®Google Scholar
• Rosen LS, Gordon D, Dugan W. Zoledronic acid is superior to pamidronate for the treatment of bone metastasis in breast carcinoma patients with at least one osteolytic lesion. Cancer 2004;100:36–43
   PubMed Web of Science ®Google Scholar
• Green JR, Guenther A. The backbone of progress–preclinical studies and innovations with zoledronic acid. Crit Rev Oncol Hemat 2011;77:S3–12
   PubMed Web of Science ®Google Scholar
• Korpal M, Yan J, Lu X, et al. Imaging transforming growth factor-beta signaling dynamics and therapeutic response in breast cancer bone metastasis. Nature Med 2009;15:960–6
   PubMed Web of Science ®Google Scholar
• Horie N, Murata H, Kimura S, et al. Combined effects of a third-generation bisphosphonate, zoledronic acid with other anticancer agents against murine osteosarcoma. Br J Cancer 2007;96:255–61
   PubMed Web of Science ®Google Scholar
• Philippe Cleźardin P. Anti-tumour activity of zoledronic acid. Cancer Treat Rev 2005;31:S1–8
   PubMed Web of Science ®Google Scholar
• Chaudhari KR, Kumar A, Khandelwal MVK, et al. Bone metastasis targeting: a novel approach to reach bone using Zoledronate anchored PLGA nanoparticle as carrier system loaded with Docetaxel. J Control Release 2012;158:470–8
   PubMed Web of Science ®Google Scholar
• Hengst V, Oussoren C, Kissel T, Storm G. Bone targeting potential of bisphosphonate-targeted liposomes: preparation, characterization and hydroxyapatite binding in vitro. Int J Pharm 2007;331:224–7
   PubMed Web of Science ®Google Scholar
• Anada T, Takeda Y, Honda Y, et al. Synthesis of calcium phosphate-binding liposome for drug delivery. Bioorg Med Chem Lett 2009;19:4148–50
   PubMed Web of Science ®Google Scholar
• Leu C-T, Luegmayr E, Freedman LP, et al. Relative binding affinities of bisphosphonates for human bone and relationship to antiresorptive efficacy. Bone 2006;38:628–36
   PubMed Web of Science ®Google Scholar
• Choi S-W, Kim J-H. Design of surface-modified poly (d, l-lactide-co-glycolide) nanoparticles for targeted drug delivery to bone. J Control Release 2007;122:24–30
   PubMed Web of Science ®Google Scholar
• Pignatello R, Cenni E, Micieli D, et al. A novel biomaterial for osteotropic drug nanocarriers: synthesis and biocompatibility evaluation of a PLGA-ALE conjugate. Nanomedicine 2009;4:161–75
   PubMed Web of Science ®Google Scholar
• Bain SD, Bailey MC, Celino DL, et al. High-dose estrogen inhibits bone resorption and stimulates bone formation in the ovariectomized mouse. J Bone Miner Res 1993;8:435–42
   PubMed Web of Science ®Google Scholar
• Colditz GA, Hankinson SE, Hunter DJ, et al. The use of estrogens and progestins and the risk of breast cancer in postmenopausal women. New Engl J Med 1995;332:1589–93
   PubMed Web of Science ®Google Scholar
• Fujisaki J, Tokunaga Y, Takahashi T, et al. Osteotropic drug delivery system (ODDS) based on bisphosphonic prodrug-IV – effects of osteotropic estradiol on bone mineral density and uterine weight in ovariectomized rats. J Drug Target 1998;5:129–38
   PubMed Web of Science ®Google Scholar
• Bauss F, Esswein A, Reiff K, et al. Effect of 17β-estradiol-bisphosphonate conjugates, potential bone-seeking estrogen pro-drugs, on 17β-estradiol serum kinetics and bone mass in rats. Calcif Tissue Int 1996;59:168–73
   PubMed Web of Science ®Google Scholar
• Morioka M, Kamizono A, Takikawa H, et al. Design, synthesis, and biological evaluation of novel estradiol–bisphosphonate conjugates as bone-specific estrogens. Bioorg Med Chem 2010;18:1143–8
   PubMed Web of Science ®Google Scholar
• Arns S, Gibe R, Moreau A, et al. Design and synthesis of novel bone-targeting dual-action pro-drugs for the treatment and reversal of osteoporosis. Bioorg Med Chem Lett 2012;20:2131–40
   Web of Science ®Google Scholar
• Clementi C, Miller K, Mero A, et al. Dendritic poly (ethylene glycol) bearing paclitaxel and alendronate for targeting bone neoplasms. Mol Pharm 2011;8:1063–72
   PubMed Web of Science ®Google Scholar
• Bodei L, Lam M, Chiesa C, et al. EANM procedure guideline for treatment of refractory metastatic bone pain. Eur J Nucl Med Mol Imaging 2008;35:1934–40
   PubMed Web of Science ®Google Scholar
• Paes FM, Serafini AN. Systemic metabolic radiopharmaceutical therapy in the treatment of metastatic bone pain. Semin Nucl Med 2010;40:89–104
   PubMed Web of Science ®Google Scholar
• De Klerk J, Van Dijk A, Zonnenberg B, Rijk P. Pharmacokinetics of rhenium-186 after administration of rhenium-186-HEDP to patients with bone metastases. J Nucl Med 1992;33:646–51
   PubMed Web of Science ®Google Scholar
• Ogawa K, Mukai T, Asano D, et al. Therapeutic effects of a 186Re-complex–conjugated bisphosphonate for the palliation of metastatic bone pain in an animal model. J Nucl Med 2007;48:122–7
   PubMed Web of Science ®Google Scholar
• Torres Martin de Rosales R, Finucane C, Foster J, et al. 188Re (CO) 3-dipicolylamine-alendronate: a new bisphosphonate conjugate for the radiotherapy of bone metastases. Bioconjugate Chem 2010;21:811–15
   PubMed Web of Science ®Google Scholar
• Reinholz MM, Zinnen SP, Dueck AC, et al. A promising approach for treatment of tumor-induced bone diseases: utilizing bisphosphonate derivatives of nucleoside antimetabolites. Bone 2010;47:12–22
   PubMed Web of Science ®Google Scholar
• McPherson JC III, Runner R, Buxton TB, et al. Synthesis of osteotropic hydroxybisphosphonate derivatives of fluoroquinolone antibacterials. Eur J Med Chem 2012;47:615–18
   PubMed Web of Science ®Google Scholar
• Bhandari KH, Newa M, Chapman J, Doschak MR. Synthesis, characterization and evaluation of bone targeting salmon calcitonin analogs in normal and osteoporotic rats. J Control Release 2012;158:44–52
   PubMed Web of Science ®Google Scholar
• Wright JE, Gittens SA, Bansal G, et al. A comparison of mineral affinity of bisphosphonate–protein conjugates constructed with disulfide and thioether linkages. Biomaterials 2006;27:769–84
   PubMed Web of Science ®Google Scholar
• Ehrick RS, Capaccio M, Puleo DA, Bachas LG. Ligand-modified aminobisphosphonate for linking proteins to hydroxyapatite and bone surface. Bioconjugate Chem 2007;19:315–21
   PubMed Web of Science ®Google Scholar
• Murphy MB, Hartgerink JD, Goepferich A, Mikos AG. Synthesis and in vitro hydroxyapatite binding of peptides conjugated to calcium-binding moieties. Biomacromolecules 2007;8:2237–43
   PubMed Web of Science ®Google Scholar
• Guan M, Yao W, Liu R, et al. Directing mesenchymal stem cells to bone to augment bone formation and increase bone mass. Nat Med 2012;18:456–62
   PubMed Web of Science ®Google Scholar
• Segal E, Pan H, Benayoun L, et al. Enhanced anti-tumor activity and safety profile of targeted nano-scaled HPMA copolymer-alendronate-TNP-470 conjugate in the treatment of bone malignances. Biomaterials 2011;32:4450–63
   PubMed Web of Science ®Google Scholar