Bisphosphonate-modified biomaterials for drug delivery and bone tissue engineering

Expert Opinion on Drug Delivery

Volumn 12, Issue 9, 2015, Pages 1443-1458

  Ossipov, Dmitri A ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

bisphosphonates; bone cancer; bone regeneration; growth factor delivery; hydrogels; nanoparticles; osteoporosis

Indexed keywords

ALENDRONIC ACID; ANTINEOPLASTIC AGENT; BIOMATERIAL; BISPHOSPHONIC ACID DERIVATIVE; BORTEZOMIB; CALCIUM ION; CAMPTOTHECIN; DICLOFENAC; DOCETAXEL; DOXORUBICIN; ENZYME; FUMAGILLOL CHLOROACETYLCARBAMATE; GADOLINIUM PENTETATE; GATIFLOXACIN; GROWTH FACTOR; MEDRONATE TECHNETIUM TC 99M; NANOCARRIER; NANOCOMPOSITE; NANOMATERIAL; OSTEOPROTEGERIN; PACLITAXEL; PAMIDRONIC ACID; POLYMER; PRODRUG; PROSTAGLANDIN E2; PROTEIN; SALCATONIN; TETRAXETAN; UNINDEXED DRUG; ZOLEDRONIC ACID; HYDROGEL;

ADHESION; BINDING AFFINITY; BIOLOGICAL ACTIVITY; BONE; BONE TISSUE; CALCIUM BINDING; CONTROLLED DRUG RELEASE; CROSS LINKING; DRUG CONJUGATION; DRUG DELIVERY SYSTEM; DRUG HALF LIFE; DRUG PROTEIN BINDING; DRUG SOLUBILITY; DRUG STABILITY; DRUG TARGETING; GENETIC TRANSFECTION; HUMAN; HYDROGEL; IN VITRO STUDY; MOLECULAR IMAGING; MOLECULAR WEIGHT; MOLECULE; NONHUMAN; OSSIFICATION; POLYMERIZATION; REVIEW; TISSUE ENGINEERING; ANIMAL; CHEMISTRY; METABOLISM; PROCEDURES;

ANIMALS; BIOCOMPATIBLE MATERIALS; BONE AND BONES; DIPHOSPHONATES; DRUG DELIVERY SYSTEMS; HUMANS; HYDROGELS; NANOCOMPOSITES; POLYMERS; TISSUE ENGINEERING;

EID: 84939621958     PISSN: 17425247     EISSN: 17447593     Source Type: Journal    
DOI: 10.1517/17425247.2015.1021679     Document Type: Review

References (77)

1. Delmas PD. Treatment of postmenopausal osteoporosis. Lancet 2002; 359 (9322): 2018-26
2. Sato M, Grasser W, Endo N, et al. Bisphosphonate action. Alendronate localization in rat bone and effects on osteoclast ultrastructure. J Clin Invest 1991; 88 (6): 2095-105
3. Lehenkari PP, Kellinsalmi M, Napankangas JP, et al. Further insight into mechanism of action of clodronate: inhibition of mitochondrial ADP/ATP translocase by a nonhydrolyzable, adenine-containing metabolite. Mol Pharmacol 2002; 61 (5): 1255-62
4. Luckman SP, Coxon FP, Ebetino FH, et al. 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
5. Clezardin P, Benzaid I, Croucher PI. Bisphosphonates in preclinical bone oncology. Bone 2011; 49 (1): 66-70
6. Fleisch H, Russell RG, Simpson B, Muhlbauer RC. Prevention by a diphosphonate of immobilization "osteoporosis" in rats. Nature 1969; 223 (5202): 211-12
7. Russell RG. Bisphosphonates: the first 40 years. Bone 2011; 49 (1): 2-19
8. Wilkinson JM, Little DG. Bisphosphonates in orthopedic applications. Bone 2011; 49 (1): 95-102
9. Aspenberg P. Bisphosphonates and implants: an overview. Acta Orthop 2009; 80 (1): 119-23
10. Cattalini JP, Boccaccini AR, Lucangioli S, Mourino V. Bisphosphonate-based strategies for bone tissue engineering and orthopedic implants. Tissue Eng Part B Rev 2012; 18 (5): 323-40
11. Hirabayashi H, Sawamoto T, Fujisaki J, et al. Dose-dependent pharmacokinetics and disposition of bisphosphonic prodrug of diclofenac based on osteotropic drug delivery system (ODDS). Biopharm Drug Dispos 2002; 23 (8): 307-15
12. Hirabayashi H, Sawamoto T, Fujisaki J, et al. Relationship between physicochemical and osteotropic properties of bisphosphonic derivatives: rational design for osteotropic drug delivery system (ODDS). Pharm Res 2001; 18 (5): 646-51
13. Yan SX, Wang Y, Peng GJ, et al. Effects of technetium-99 methylenediphosphonate on cytokine-induced activation of retro-ocular fibroblasts from patients with Graves ophthalmopathy. Nucl Med Commun 2011; 32 (2): 142-6
14. Zhao Y, Wang L, Liu Y, et al. Technetium-99 conjugated with methylene diphosphonate ameliorates ovariectomy-induced osteoporotic phenotype without causing osteonecrosis in the jaw. Calcif Tissue Int 2012; 91 (6): 400-8
15. Diel IJ, Fogelman I, Al-Nawas B, et al. Pathophysiology, risk factors and management of bisphosphonate-associated osteonecrosis of the jaw: is there a diverse relationship of amino- and non-aminobisphosphonates? Crit Rev Oncol Hematol 2007; 64 (3): 198-207
16. Kashemirov BA, Bala JL, Chen X, et al. Fluorescently labeled risedronate and related analogues: "magic linker" synthesis. Bioconjug Chem 2008; 19 (12): 2308-10
17. Bhushan KR, Tanaka E, Frangioni JV. Synthesis of conjugatable bisphosphonates for molecular imaging of large animals. Angew Chem 2007; 46 (42): 7969-71
18. Kubicek V, Rudovsky J, Kotek J, et al. A bisphosphonate monoamide analogue of DOTA: a potential agent for bone targeting. J Am Chem Soc 2005; 127 (47): 16477-85
19. Verbeke K, Rozenski J, Cleynhens B, et al. Development of a conjugate of (99m)Tc-EC with aminomethylenediphosphonate in the search for a bone tracer with fast clearance from soft tissue. Bioconjug Chem 2002; 13 (1): 16-22
20. El-Mabhouh A, Angelov C, McEwan A, et al. Preclinical investigations of drug and radionuclide conjugates of bisphosphonates for the treatment of metastatic bone cancer. Cancer Biother Radiopharm 2004; 19 (5): 627-40
21. 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. Bioconjug Chem 2010; 21 (5): 811-15
22. Ogawa K, Ishizaki A, Takai K, et al. Development of novel radiogallium-labeled bone imaging agents using oligo-aspartic acid peptides as carriers. PLoS One 2013; 8 (12): e84335
23. Erez R, Ebner S, Attali B, Shabat D. Chemotherapeutic bone-targeted bisphosphonate prodrugs with hydrolytic mode of activation. Bioorg Med Chem Lett 2008; 18 (2): 816-20
24. Hirabayashi H, Takahashi T, Fujisaki J, et al. Bone-specific delivery and sustained release of diclofenac, a non-steroidal anti-inflammatory drug, via bisphosphonic prodrug based on the Osteotropic Drug Delivery System (ODDS). J Control Release 2001; 70 (1-2): 183-91
25. Houghton TJ, Tanaka KS, Kang T, et al. Linking bisphosphonates to the free amino groups in fluoroquinolones: preparation of osteotropic prodrugs for the prevention of osteomyelitis. J Med Chem 2008; 51 (21): 6955-69
26. Gil L, Han Y, Opas EE, et al. Prostaglandin E2-bisphosphonate conjugates: potential agents for treatment of osteoporosis. Bioorg Med Chem 1999; 7 (5): 901-19
27. Maruyama T, Asada M, Shiraishi T, et al. Design and synthesis of a selective EP4-receptor agonist. Part 3: 16-phenyl-5-thiaPGE(1) and 9-beta-halo derivatives with improved stability. Bioorg Med Chem 2002; 10 (6): 1743-59
28. 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 2012; 20 (6): 2131-40
29. Murphy MB, Hartgerink JD, Goepferich A, Mikos AG. Synthesis and in vitro hydroxyapatite binding of peptides conjugated to calcium-binding moieties. Biomacromolecules 2007; 8 (7): 2237-43
30. Uludag H, Kousinioris N, Gao T, Kantoci D. Bisphosphonate conjugation to proteins as a means to impart bone affinity. Biotechnol Prog 2000; 16 (2): 258-67
31. Gittens SA, Bansal G, Kucharski C, et al. Imparting mineral affinity to fetuin by bisphosphonate conjugation: a comparison of three bisphosphonate conjugation schemes. Mol Pharm 2005; 2 (5): 392-406
32. Doschak MR, Kucharski CM, Wright JE, et al. Improved bone delivery of osteoprotegerin by bisphosphonate conjugation in a rat model of osteoarthritis. Mol Pharm 2009; 6 (2): 634-40
33. 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 (1): 44-52
34. Zheng Y, Nishikawa M, Ikemura M, et al. Development of bone-targeted catalase derivatives for inhibition of bone metastasis of tumor cells in mice. J Pharm Sci 2012; 101 (2): 552-7
35. Low SA, Kopecek J. Targeting polymer therapeutics to bone. Adv Drug Deliv Rev 2012; 64 (12): 1189-204
36. Wang D, Sima M, Mosley RL, et al. Pharmacokinetic and biodistribution studies of a bone-targeting drug delivery system based on N-(2-hydroxypropyl)methacrylamide copolymers. Mol Pharm 2006; 3 (6): 717-25
37. Wang D, Miller SC, Shlyakhtenko LS, et al. Osteotropic Peptide that differentiates functional domains of the skeleton. Bioconjug Chem 2007; 18 (5): 1375-8
38. Liu J, Jo J, Kawai Y, et al. Preparation of polymer-based multimodal imaging agent to visualize the process of bone regeneration. J Control Release 2012; 157 (3): 398-405
39. 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 (2): 161-75
40. Pignatello R, Sarpietro MG, Castelli F. Synthesis and biological evaluation of a new polymeric conjugate and nanocarrier with osteotropic properties. J Funct Biomater 2012; 3 (1): 79-99
41. Choi SW, Kim JH. Design of surface-modified poly(D,L-lactide-co-glycolide) nanoparticles for targeted drug delivery to bone. J Control Release 2007; 122 (1): 24-30
42. Ramanlal Chaudhari K, Kumar A, Megraj Khandelwal VK, 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 (3): 470-8
43. Swami A, Reagan MR, Basto P, et al. Engineered nanomedicine for myeloma and bone microenvironment targeting. Proc Natl Acad Sci USA 2014; 111 (28): 10287-92
44. Chen H, Li G, Chi H, et al. Alendronate-conjugated amphiphilic hyperbranched polymer based on Boltorn H40 and poly(ethylene glycol) for bone-targeted drug delivery. Bioconjug Chem 2012; 23 (9): 1915-24
45. Miller K, Erez R, Segal E, et al. Targeting bone metastases with a bispecific anticancer and antiangiogenic polymer-alendronate-taxane conjugate. Angew Chem 2009; 48 (16): 2949-54
46. 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 (4): 1052-62
47. 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 (19): 4450-63
48. Miller K, Clementi C, Polyak D, et al. Poly(ethylene glycol)-paclitaxel-alendronate self-assembled micelles for the targeted treatment of breast cancer bone metastases. Biomaterials 2013; 34 (15): 3795-806
49. Gluz E, Mizrahi DM, Margel S. Synthesis and characterization of new poly(ethylene glycol)bisphosphonate vinylic monomer and non-fluorescent and NIR-fluorescent bisphosphonate micrometer-sized particles. Polymer (Guildf) 2013; 54 (2): 565-71
50. Heller DA, Levi Y, Pelet JM, et al. Modular click-in-emulsion bone-targeted nanogels. Adv Mater 2013; 25 (10): 1449-54
51. Wang G, Babadagli ME, Uludag H. Bisphosphonate-derivatized liposomes to control drug release from collagen/hydroxyapatite scaffolds. Mol Pharm 2011; 8 (4): 1025-34
52. Gittens SA, Bagnall K, Matyas JR, et al. Imparting bone mineral affinity to osteogenic proteins through heparin-bisphosphonate conjugates. J Control Release 2004; 98 (2): 255-68
53. Yewle JN, Wei Y, Puleo DA, et al. Oriented immobilization of proteins on hydroxyapatite surface using bifunctional bisphosphonates as linkers. Biomacromolecules 2012; 13 (6): 1742-9
54. Ehrick RS, Capaccio M, Puleo DA, Bachas LG. Ligand-modified aminobisphosphonate for linking proteins to hydroxyapatite and bone surface. Bioconjug Chem 2008; 19 (1): 315-21
55. 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 (3): 456-62
56. Ong HT, Loo JSC, Boey FYC, et al. Exploiting the high-affinity phosphonate-hydroxyapatite nanoparticles interaction for delivery of radiation and drugs. J Nanopart Res 2008; 10 (1): 141-50
57. Giger EV, Puigmarti-Luis J, Schlatter R, et al. Gene delivery with bisphosphonate-stabilized calcium phosphate nanoparticles. J Control Release 2011; 150 (1): 87-93
58. Giger EV, Castagner B, Raikkonen J, et al. siRNA transfection with calcium phosphate nanoparticles stabilized with PEGylated chelators. Adv Healthc Mater 2013; 2 (1): 134-44
59. Fishbein I, Alferiev IS, Nyanguile O, et al. Bisphosphonate-mediated gene vector delivery from the metal surfaces of stents. Proc Natl Acad Sci USA 2006; 103 (1): 159-64
60. Lalatonne Y, Paris C, Serfaty JM, et al. Bis-phosphonates-ultra small superparamagnetic iron oxide nanoparticles: a platform towards diagnosis and therapy. Chem Commun 2008; 22): 2553-5
61. Torres Martin de Rosales R, Tavare R, Glaria A, et al. J. ((9)(9)m)Tc-bisphosphonate-iron oxide nanoparticle conjugates for dual-modality biomedical imaging. Bioconjug Chem 2011; 22 (3): 455-65
62. Sandiford L, Phinikaridou A, Protti A, et al. Bisphosphonate-anchored PEGylation and radiolabeling of superparamagnetic iron oxide: long-circulating nanoparticles for in vivo multimodal (T1 MRI-SPECT) imaging. ACS Nano 2013; 7 (1): 500-12
63. Lalatonne Y, Monteil M, Jouni H, et al. Superparamagnetic bifunctional bisphosphonates nanoparticles: a potential MRI contrast agent for osteoporosis therapy and diagnostic. J Osteoporos 2010; 2010: 747852
64. Řehoř I, Kubíček V, Kotek J, et al. 1H NMR relaxivity of aqueous suspensions of titanium dioxide nanoparticles coated with a gadolinium(III) chelate of a DOTA-monoamide with a phenylphosphonate pendant arm. J Mater Chem 2009; 19 (10): 1494-500
65. Liu D, Kramer SA, Huxford-Phillips RC, et al. Coercing bisphosphonates to kill cancer cells with nanoscale coordination polymers. Chem Commun 2012; 48 (21): 2668-70
66. Nejadnik MR, Yang X, Bongio M, et al. Self-healing hybrid nanocomposites consisting of bisphosphonated hyaluronan and calcium phosphate nanoparticles. Biomaterials 2014; 35 (25): 6918-29
67. Wang L, Zhang M, Yang Z, Xu B. The first pamidronate containing polymer and copolymer. Chem Commun 2006; 26): 2795-7
68. Rayment EA, Dargaville TR, Shooter GK, et al. Attenuation of protease activity in chronic wound fluid with bisphosphonate-functionalised hydrogels. Biomaterials 2008; 29 (12): 1785-95
69. Nejadnik MR, Yang X, Mimura T, et al. Calcium-mediated secondary cross-linking of bisphosphonated oligo(poly(ethylene glycol) fumarate) hydrogels. Macromol Biosci 2013; 13 (10): 1308-13
70. Yang X, Akhtar S, Rubino S, et al. Direct ″Click″ synthesis of hybrid bisphosphonate-hyaluronic acid hydrogel in aqueous solution for biomineralization. Chem Mater 2012; 24 (9): 1690-7
71. Varghese OP, Sun W, Hilborn J, Ossipov DA. In situ cross-linkable high molecular weight hyaluronan-bisphosphonate conjugate for localized delivery and cell-specific targeting: a hydrogel linked prodrug approach. J Am Chem Soc 2009; 131 (25): 8781-3
72. Rensing S, Arendt M, Springer A, et al. Optimization of a synthetic arginine receptor. Systematic tuning of noncovalent interactions. J Org Chem 2001; 66 (17): 5814-21
73. Renner C, Piehler J, Schrader T. Arginine- and lysine-specific polymers for protein recognition and immobilization. J Am Chem Soc 2006; 128 (2): 620-8
74. Hulsart-Billstrom G, Yuen PK, Marsell R, et al. Bisphosphonate-linked hyaluronic acid hydrogel sequesters and enzymatically releases active bone morphogenetic protein-2 for induction of osteogenic differentiation. Biomacromolecules 2013; 14 (9): 3055-63
75. Katsumi H, Takashima M, Sano J, et al. Development of polyethylene glycol-conjugated alendronate, a novel nitrogen-containing bisphosphonate derivative: evaluation of absorption, safety, and effects after intrapulmonary administration in rats. J Pharm Sci 2011; 100 (9): 3783-92
76. Cenni E, Avnet S, Granchi D, et al. The effect of poly(d,l-lactide-co-glycolide)-alendronate conjugate nanoparticles on human osteoclast precursors. J Biomater Sci Polym Ed 2011. [. Epub ahead of print]
77. Holmberg AR, Lerner UH, Alayia AA, et al. Development of a novel poly bisphosphonate conjugate for treatment of skeletal metastasis and osteoporosis. Int J Oncol 2010; 37 (3): 563-7