Near-infrared fluorescent probe traces bisphosphonate delivery and retention in vivo

Journal of Bone and Mineral Research

Volumn 25, Issue 8, 2010, Pages 1748-1758

  Kozloff, Kenneth M ^a,c   Volakis, Leo I ^a,c   Marini, Joan C ^b   Caird, Michelle S ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Bisphosphonates; Fluorescence; Molecular imaging; Osteogenesis imperfecta; Osteonecrosis of the jaw

Indexed keywords

OSTEOSENSE; PAMIDRONIC ACID; UNCLASSIFIED DRUG;

ALVEOLAR BONE; ANIMAL EXPERIMENT; ARTICLE; BONE TURNOVER; CORTICAL BONE; DRUG BONE LEVEL; DRUG RETENTION; FLUORESCENCE; JAW OSTEONECROSIS; MALE; MANDIBLE; MOLAR TOOTH; MOLECULAR IMAGING; MOUSE; NONHUMAN; PERIODONTAL LIGAMENT; TOOTH ROOT;

ANIMALS; BIOLOGICAL ASSAY; DIPHOSPHONATES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG DELIVERY SYSTEMS; FEMUR; FLUORESCENT DYES; MICE; MICE, INBRED BALB C; SPECTROSCOPY, NEAR-INFRARED; TIBIA; TIME FACTORS;

EID: 77955736518     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1002/jbmr.66     Document Type: Article

References (73)

1. Rodan GA, Martin TJ. Therapeutic approaches to bone diseases. Science. 2000;289:1508-1514.
2. Russell RG, Rogers MJ. Bisphosphonates: from the laboratory to the clinic and back again. Bone. 1999;25:97-106.
3. Hickey J, Lemons D, Waber P, Seikaly MG. Bisphosphonate use in children with bone disease. J Am Acad Orthop Surg. 2006;14:638-644.
4. Ramachandran M, Ward K, Brown RR, Munns CF, Cowell CT, Little DG. Intravenous bisphosphonate therapy for traumatic osteonecrosis of the femoral head in adolescents. J Bone Joint Surg Am. 2007;89: 1727-1734. (Pubitemid 47229879)
5. Sholas MG, Tann B, Gaebler-Spira D. Oral bisphosphonates to treat disuse osteopenia in children with disabilities: a case series. J Pediatr Orthop. 2005;25:326-331.
6. Glorieux FH, Bishop NJ, Plotkin H, Chabot G, Lanoue G, Travers R. Cyclic administration of pamidronate in children with severe osteogenesis imperfecta. N Engl J Med. 1998;339:947-952. (Pubitemid 28455096)
7. Neviaser AS, Lane JM, Lenart BA, Edobor-Osula F, Lorich DG. Low-energy femoral shaft fractures associated with alendronate use. J Orthop Trauma. 2008;22:346-350.
8. Boskey AL, Spevak L, Weinstein RS. Spectroscopic markers of bone quality in alendronate-treated postmenopausal women. Osteoporos Int. 2009;20:793-800.
9. Durchschlag E, Paschalis EP, Zoehrer R, et al. Bone material properties in trabecular bone from human iliac crest biopsies after 3- and 5-year treatment with risedronate. J Bone Miner Res. 2006;21:1581-1590.
10. Munns CF, Rauch F, Zeitlin L, Fassier F, Glorieux FH. Delayed osteotomy but not fracture healing in pediatric osteogenesis imperfecta patients receiving pamidronate. J Bone Miner Res. 2004;19:1779-1786. (Pubitemid 41103428)
11. Kamoun-Goldrat A, Ginisty D, Le Merrer M. Effects of bisphosphonates on tooth eruption in children with osteogenesis imperfecta. Eur J Oral Sci. 2008;116:195-198.
12. Grissom LE, Harcke HT. Radiographic features of bisphosphonate therapy in pediatric patients. Pediatr Radiol. 2003;33:226-229.
13. Rauch F, Travers R, Munns C, Glorieux FH. Sclerotic metaphyseal lines in a child treated with pamidronate: histomorphometric analysis. J Bone Miner Res. 2004;19:1191-1193. (Pubitemid 41110572)
14. van Persijn van Meerten EL, Kroon HM, Papapoulos SE. Epi- and metaphyseal changes in children caused by administration of bisphosphonates. Radiology. 1992;184:249-254.
15. Rauch F, Cornibert S, Cheung M, Glorieux FH. Long-bone changes after pamidronate discontinuation in children and adolescents with osteogenesis imperfecta. Bone. 2007;40:821-827.
16. Uveges T, Kozloff KM, Ty JM, et al. Alendronate treatment of Brtl osteogenesis imperfecta mouse improves femoral geometry and load response before fracture but has detrimental effects on osteoblasts and bone formation and decreases predicted material properties. Journal of Bone and Mineral Research. 2009;24:849-859.
17. American Association of Oral and Maxillofacial Surgeons position paper on bisphosphonate-related osteonecrosis of the jaws. J Oral Maxillofac Surg. 2007;65:369-376.
18. 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;22:1479-1491.
19. Marx RE. Pamidronate (Aredia) and zoledronate (Zometa) induced avascular necrosis of the jaws: a growing epidemic. J Oral Maxillofac Surg. 2003;61:1115-1117.
20. Rizzoli R, Burlet N, Cahall D, et al. Osteonecrosis of the jaw and bisphosphonate treatment for osteoporosis. Bone. 2008;42:841-847.
21. Ruggiero SL, Mehrotra B, Rosenberg TJ, Engroff SL. Osteonecrosis of the jaws associated with the use of bisphosphonates: a review of 63 cases. J Oral Maxillofac Surg. 2004;62:527-534. (Pubitemid 38542516)
22. Papapoulos SE, Cremers SC. Prolonged bisphosphonate release after treatment in children. N Engl J Med. 2007;356:1075-1076.
23. Al Muderis M, Azzopardi T, Cundy P. Zebra lines of pamidronate therapy in children. J Bone Joint Surg Am. 2007;89:1511-1516.
24. Kozloff KM, Weissleder R, Mahmood U. Non-invasive optical detection of bone mineral. J Bone Miner Res. 2007;22:1208-1216. (Pubitemid 351339703)
25. Zaheer A, Lenkinski RE, Mahmood A, Jones AG, Cantley LC, Frangioni JV. In vivo near-infrared fluorescence imaging of osteoblastic activity. Nat Biotechnol. 2001;19:1148-1154.
26. Zilberman Y, Kallai I, Gafni Y, et al. Fluorescence molecular tomography enables in vivo visualization and quantification of nonunion fracture repair induced by genetically engineered mesenchymal stem cells. J Orthop Res. 2008;26:522-530.
27. Lenkinski RE, Ahmed M, Zaheer A, Frangioni JV, Goldberg SN. Near-infrared fluorescence imaging of microcalcification in an animal model of breast cancer. Acad Radiol. 2003;10:1159-1164.
28. Aikawa E, Nahrendorf M, Figueiredo JL, et al. Osteogenesis associates with inflammation in early-stage atherosclerosis evaluated by molecular imaging in vivo. Circulation. 2007;116:2841-2850.
29. Figueiredo JL, Passerotti CC, Sponholtz T, Nguyen HT, Weissleder R. A novel method of imaging calcium urolithiasis using fluorescence. J Urol. 2008;179:1610-1614.
30. Coxon FP, Thompson K, Roelofs AJ, Ebetino FH, Rogers MJ. Visualizing mineral binding and uptake of bisphosphonate by osteoclasts and non-resorbing cells. Bone. 2008;42:848-860.
31. Weissleder R, Ntziachristos V. Shedding light onto live molecular targets. Nat Med. 2003;9:123-128. (Pubitemid 36098273)
32. Forlino A, Porter FD, Lee EJ, Westphal H, Marini JC. Use of the Cre/lox recombination system to develop a non-lethal knock-in murine model for osteogenesis imperfecta with an a1(I) G349C substitution. Variability in phenotype in BrtlIV mice. J Biol Chem. 1999;274:37923-37931.
33. Kozloff KM, Carden A, Bergwitz C, et al. Brittle IV mouse model for osteogenesis imperfecta IV demonstrates postpubertal adaptations to improve whole bone strength. J Bone Miner Res. 2004;19:614-622.
34. Hoggarth CR, Bennett R, Daley-Yates PT. The pharmacokinetics and distribution of pamidronate for a range of doses in the mouse. Calcif Tissue Int. 1991;49:416-420.
35. Fleisch H, Russell RG, Francis MD. Diphosphonates inhibit hydroxyapatite dissolution in vitro and bone resorption in tissue culture and in vivo. Science. 1969;165:1262-1264.
36. Little DG, Peat RA, McEvoy A, Williams PR, Smith EJ, Baldock PA. Zoledronic acid treatment results in retention of femoral head structure after traumatic osteonecrosis in young Wistar rats. J Bone Miner Res. 2003;18:2016-2022.
37. Tanzer M, Karabasz D, Krygier JJ, Cohen R, Bobyn JD. The Otto Aufranc Award: bone augmentation around and within porous implants by local bisphosphonate elution. Clin Orthop Relat Res. 2005;441:30-39. (Pubitemid 44384201)
38. Jarrett SJ, Conaghan PG, Sloan VS, et al. Preliminary evidence for a structural benefit of the new bisphosphonate zoledronic acid in early rheumatoid arthritis. Arthritis Rheum. 2006;54:1410-1414.
39. Plotkin LI, Lezcano V, Thostenson J, Weinstein RS, Manolagas SC, Bellido T. Connexin 43 is required for the anti-apoptotic effect of bisphosphonates on osteocytes and osteoblasts in vivo. J Bone Miner Res. 2008;23:1712-1721.
40. Plotkin LI, Weinstein RS, Parfitt AM, Roberson PK, Manolagas SC, Bellido T. Prevention of osteocyte and osteoblast apoptosis by bisphosphonates and calcitonin. J Clin Invest. 1999;104:1363-1374.
41. Iwata K, Li J, Follet H, Phipps RJ, Burr DB. Bisphosphonates suppress periosteal osteoblast activity independently of resorption in rat femur and tibia. Bone. 2006;39:1053-1058.
42. Nakamura M, Udagawa N, Matsuura S, et al. Osteoprotegerin regulates bone formation through a coupling mechanism with bone resorption. Endocrinology. 2003;144:5441-5449.
43. Kunzmann V, Bauer E, Feurle J, Weissinger F, Tony HP, Wilhelm M. Stimulation of gammadelta T cells by aminobisphosphonates and induction of antiplasma cell activity in multiple myeloma. Blood. 2000;96:384-392. (Pubitemid 30463353)
44. Leu CT, Luegmayr E, Freedman LP, Rodan GA, Reszka AA. Relative binding affinities of bisphosphonates for human bone and relationship to antiresorptive efficacy. Bone. 2006;38:628-636.
45. Francis MD, Ferguson DL, Tofe AJ, Bevan JA, Michaels SE. Comparative evaluation of three diphosphonates: in vitro adsorption (C- 14 labeled) and in vivo osteogenic uptake (Tc-99m complexed). J Nucl Med. 1980;21:1185-1189.
46. Jung A, Bisaz S, Fleisch H. The binding of pyrophosphate and two diphosphonates by hydroxyapatite crystals. Calcif Tissue Res. 1973;11:269-280.
47. Mitterhauser M, Toegel S, Wadsak W, et al. Binding studies of [18F]-fluoride and polyphosphonates radiolabelled with [99mTc], [111In], [153Sm] and [188Re] on bone compartments: Verification of the pre vivo model? Bone. 2005;37:404-412.
48. van Beek E, Hoekstra M, van de Ruit M, Lowik C, Papapoulos S. Structural requirements for bisphosphonate actions in vitro. J Bone Miner Res. 1994;9:1875-1882. (Pubitemid 24363143)
49. Nancollas GH, Tang R, Phipps RJ, et al. Novel insights into actions of bisphosphonates on bone: differences in interactions with hydroxyapatite. Bone. 2006;38:617-627.
50. Sato M, Grasser W, Endo N, et al. Bisphosphonate action. Alendronate localization in rat bone and effects on osteoclast ultrastructure. J Clin Invest. 1991;88:2095-2105.
51. Cremers SC, Papapoulos SE, Gelderblom H, et al. Skeletal retention of bisphosphonate (pamidronate) and its relation to the rate of bone resorption in patients with breast cancer and bone metastases. J Bone Miner Res. 2005;20:1543-1547.
52. Masarachia P, Weinreb M, Balena R, Rodan GA. Comparison of the distribution of 3H-alendronate and 3H-etidronate in rat and mouse bones. Bone. 1996;19:281-290. (Pubitemid 26305769)
53. Lin JH, Chen IW, Duggan DE. Effects of dose, sex, and age on the disposition of alendronate, a potent antiosteolytic bisphosphonate, in rats. Drug Metab Dispos. 1992;20:473-478.
54. Letocha AD, Cintas HL, Troendle JF, et al. Controlled trial of pamidronate in children with types III and IV osteogenesis imperfecta confirms vertebral gains but not short-term functional improvement. J Bone Miner Res. 2005;20:977-986.
55. Burnett-Bowie SM, Saag K, Sebba A, et al. Prediction of changes in bone mineral density in postmenopausal women treated with once-weekly bisphosphonates. J Clin Endocrinol Metab. 2009;94:1097-1103.
56. Uveges TE, Collin-Osdoby P, Cabral WA, et al. Cellular mechanism of decreased bone in Brtl mouse model of OI: Imbalance of decreased osteoblast function and increased osteoclasts and their precursors. J Bone Miner Res. 2008;23:1983-1994.
57. Boskey AL. Bone mineral crystal size. Osteoporos Int. 2003;14(Suppl 5):S16-20; discussion S20-1.
58. Gourion-Arsiquaud S, Faibish D, Myers E, et al. Use of FTIR spectroscopic imaging to identify parameters associated with fragility fracture. J Bone Miner Res. 2009;24:1565-1571.
59. McCreadie BR, Morris MD, Chen TC, et al. Bone tissue compositional differences in women with and without osteoporotic fracture. Bone. 2006;39:1190-1195.
60. Marini JC. Bone: Use of bisphosphonates in children-proceed with caution. Nat Rev Endocrinol. 2009;5:241-243.
61. Gatti D, Antoniazzi F, Prizzi R, et al. Intravenous neridronate in children with osteogenesis imperfecta: a randomized controlled study. J Bone Miner Res. 2005;20:758-763.
62. Rauch F, Munns CF, Land C, Cheung M, Glorieux FH. Risedronate in the treatment of mild pediatric osteogenesis imperfecta: a randomized placebo-controlled study. J Bone Miner Res. 2009;24:1282-1289.
63. Sakkers R, Kok D, Engelbert R, et al. Skeletal effects and functional outcome with olpadronate in children with osteogenesis imperfecta: a 2-year randomised placebo-controlled study. Lancet. 2004;363:1427-1431.
64. Marini JC. Should children with osteogenesis imperfecta be treated with bisphosphonates? Nat Clin Pract Endocrinol Metab. 2006;2:14-15.
65. Barragan-Adjemian C, Lausten L, Ang DB, Johnson M, Katz J, Bonewald LF. Bisphosphonate-related osteonecrosis of the jaw: model and diagnosis with cone beam computerized tomography. Cells Tissues Organs. 2009;189:284-288.
66. Li J, Mori S, Kaji Y, Kawanishi J, Akiyama T, Norimatsu H. Concentration of bisphosphonate (incadronate) in callus area and its effects on fracture healing in rats. J Bone Miner Res. 2000;15:2042-2051.
67. Gerstenfeld LC, Sacks DJ, Pelis M, et al. Comparison of effects of the bisphosphonate alendronate versus the RANKL inhibitor denosumab on murine fracture healing. J Bone Miner Res. 2009;24:196-208.
68. Ntziachristos V, Tung CH, Bremer C, Weissleder R. Fluorescence molecular tomography resolves protease activity in vivo. Nat Med. 2002;8:757-760. (Pubitemid 34778731)
69. Montet X, Figueiredo JL, Alencar H, Ntziachristos V, Mahmood U, Weissleder R. Tomographic fluorescence imaging of tumor vascular volume in mice. Radiology. 2007;242:751-758. (Pubitemid 46310087)
70. Ntziachristos V, Bremer C, Graves EE, Ripoll J, Weissleder R. In vivo tomographic imaging of near-infrared fluorescent probes. Mol Imaging. 2002;1:82-88.
71. Kozloff KM, Quinti L, Patntirapong S, et al. Non-invasive optical detection of cathepsin K-mediated fluorescence reveals osteoclast activity in vitro and in vivo. Bone. 2009;44:190-198.
72. Kalajzic I, Kalajzic Z, Kaliterna M, et al. Use of type I collagen green fluorescent protein transgenes to identify subpopulations of cells at different stages of the osteoblast lineage. J Bone Miner Res. 2002;17:15-25.
73. Dallas SL, Veno PA, Rosser JL, et al. Time lapse imaging techniques for comparison of mineralization dynamics in primary murine osteoblasts and the late osteoblast/early osteocyte-like cell line MLO-A5. Cells Tissues Organs. 2009;189:6-11.