Synthesis, characterization and evaluation of bone targeting salmon calcitonin analogs in normal and osteoporotic rats

Journal of Controlled Release

Volumn 158, Issue 1, 2012, Pages 44-52

  Bhandari, Krishna Hari ^a   Newa, Madhuri ^a   Chapman, Jillian ^a   Doschak, Michael R ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Bisphosphonate; Bone targeting; Calcitonin; Micro CT; Osteoporosis; Polyethylene glycol (PEG)

Indexed keywords

ANTIBODY BINDING; BINDING ABILITIES; BINDING ASSAYS; BISPHOSPHONATES; BONE MINERAL DENSITY; BONE MINERALS; BONE VOLUME; BREAST CANCER CELLS; CALCITONIN; CALCIUM SALTS; CHEMICAL COUPLING; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE RAT; IN-VITRO; IN-VIVO; INTRACELLULAR CAMP; MALDI-TOF; MATRIX-ASSISTED LASER DESORPTION IONIZATION; MICRO CT; OSTEOPOROSIS; OSTEOPOROTIC; PEGYLATION; PHARMACOKINETIC PROFILES; PLASMA LEVELS; RAT MODEL; SALMON CALCITONIN; SECONDARY STRUCTURES; THERAPEUTIC EFFICACY; TIME OF FLIGHT; TRABECULAR MICRO-ARCHITECTURE;

ANIMALS; ANTIBODIES; CALCIUM PHOSPHATE; CELL CULTURE; COMPUTERIZED TOMOGRAPHY; DISEASES; HYDROXYAPATITE; POLYETHYLENE GLYCOLS; RATING; RATS; SALTS; SURGERY;

BONE;

BISPHOSPHONIC ACID DERIVATIVE; CALCITONIN ANTIBODY; CALCIUM; CALCIUM PHOSPHATE; CALCIUM SALT; CYCLIC AMP; HORMONE ANTIBODY; HYDROXYAPATITE; PEGYLATED SALMON CALCITONIN DERIVATIVE; PLACEBO; SALCATONIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; BINDING ASSAY; BONE DENSITY; BREAST CANCER; CALCIUM BLOOD LEVEL; CANCER CELL CULTURE; CIRCULAR DICHROISM; CONTROLLED STUDY; DRUG CONJUGATION; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG EFFICACY; DRUG SCREENING; DRUG STRUCTURE; DRUG SYNTHESIS; DRUG TARGETING; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN CELL; HYPOCALCEMIA; IN VITRO STUDY; IN VIVO STUDY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MICRO-COMPUTED TOMOGRAPHY; MONOCYTE; NONHUMAN; OSTEOPOROSIS; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; RAT;

ANIMALS; BONE DENSITY; BONE DENSITY CONSERVATION AGENTS; CALCITONIN; CALCIUM; CALCIUM COMPOUNDS; CELL LINE; CELL SURVIVAL; DIPHOSPHONATES; DURAPATITE; FEMALE; MICE; OSTEOPOROSIS; OVARIECTOMY; POLYETHYLENE GLYCOLS; RATS; RATS, SPRAGUE-DAWLEY; SULFHYDRYL COMPOUNDS;

EID: 84857912381     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2011.09.096     Document Type: Article

References (84)

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2. Y. Okubo, K. Bessho, K. Fujimura, K. Kusumoto, Y. Ogawa, and T. Iizuka Effect of e-calcitonin on oeteoinduction by recombinant human bone morphogenetic perotein-2 Biochem. Biophys. Res. Commun. 269 2000 317 321 (Pubitemid 30440296)
3. K.H. Song, S.J. Chung, and C.K. Shim Preparation and evaluation of proliposomes containing salmon calcitonin J. Control. Release 84 2002 27 37
4. K. Overgaard, D. Agnusdei, M.A. Hansen, E. Maioli, C. Christiansen, and C. Gennari Dose response bioactivity and bioavailability of salmon calcitonin in premenopausal and postmenopausal women J. Clin. Endocrinol. Metab. 72 1991 344 349 (Pubitemid 21921697)
5. S. Jevsevar, M. Kunstelj, and V.G. Porekar PEGylation of therapeutic proteins Biotechnol. J. 5 2010 113 128
6. J.S. Kang, P.P. Deluca, and K.C. Lee Emerging PEGylated drugs Expert Opin. Emerg. Drugs 14 2009 363 380
7. F.M. Veronese, and G. Pasut PEGylation, successful approach to drug delivery Drug Discov. Today 10 2005 1451 1458 (Pubitemid 41483874)
8. C.J. Fee Size comparison between proteins PEGylated with branched and linear poly(ethylene glycol) molecules Biotechnol. Bioeng. 98 2007 725 731 (Pubitemid 350032676)
9. M. Hamidi, A. Azadi, and P. Rafiei Pharmacokinetic consequences of PEGylation Drug Deliv. 13 2006 399 4099
10. S.M. Ryan, J.M. Frias, X. Wang, C.T. Sayers, D.M. Haddletin, and D.J. Brayden PK/PD modelling of comb-shaped PEGylated salmon calcitonin conjugates of differing molecular weights J. Control. Release 149 2011 126 132
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13. 2+/inositol phosphate signaling pathways Mol. Endocrinol. 6 1992 551 556
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15. D. Goltzman Interaction of calcitonin and calcitonin gene-related peptide at receptor sites in target tissues Science 227 1985 1343 1345 (Pubitemid 15138521)
16. P.M. Fouchereau, M.S. Moukhtar, A.A. Benson, and G. Milhaud Characterization of specific receptors for calcitonin in porcine lung Proc. Natl. Acad. Sci. U. S. A. 78 1981 3973 3975 (Pubitemid 11060599)
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23. M. Morioka, A. Kamizono, H. Takikawa, A. Mori, H. Ueno, S. Kadowaki, Y. Nakao, K. Kato, and K. Umezawa Design, synthesis, and biological evaluation of novel estradiol-bisphosphonate conjugates as bone-specific estrogens Bioorg. Med. Chem. 18 2010 143 1488
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26. H.M. Lamb, and D. Faulds Samarium 153Sm lexidronam Drugs Aging 11 1997 413 418
27. D. Wang, S.C. Miller, M. Sima, P. Kopeckova, and J. Kopecek Synthesis of polymeric bone-targeting drug delivery systems Bioconjug. Chem. 14 2003 853 859 (Pubitemid 37157997)
28. S.A. Gittens, G. Bansal, R.F. Zernicke, and H. Uludag Designing proteins for bone targeting Adv. Drug Deliv. Rev. 57 2005 1011 1036 (Pubitemid 40703886)
29. G. Siligardi, B. SamorI, S. Melandri, M. Visconti, and A.F. Drake Correlations between biological activities and conformational properties for human, salmon, eel, porcine calcitonins and Elcatonin elucidated by CD spectroscopy Eur. J. Biochem. 221 1994 1117 1125 (Pubitemid 24146216)
30. R.M. Epand, R.F. Epand, R.C. Orlowski, R.J. Schlueter, L.T. Boni, and S.W. Hui Amphipathic helix and its relationship to the interaction of calcitonin with phospholipids Biochemistry 22 1983 5014 5084
31. W. Rittel, R. Maier, B. Brugger, B. Kamber, B. Rimker, and P. Sieber Structure-activity relationship of human calcitonin III. Biological activity of synthetic analogs with shortened or terminally modified peptide chains Experientia 32 1976 246 248
32. C.S. D'Santos, G.C. Nicholson, J.M. Moseley, T. Evans, T.J. Martin, and B.E. Kemp Biologically active, derivatizable salmon calcitonin analog: design, synthesis and applications Endocrinology 123 1988 1483 1488
33. M. Newa, K.H. Bhandari, L. Tang, R. Kalvapalle, M. Suresh, and M.R. Doschak Antibody-mediated "universal" osteoclast targeting platform using calcitonin as a model drug Pharm. Res. 28 2011 1131 1143
34. M.R. Doschak, C.M. Kucharski, J.E.I. Wright, R.F. Zernicke, and H. Uludag Improved bone delivery of osteoprotegerin by bisphosphonate conjugation in a rat model of osteoarthritis Mol. Pharm. 6 2009 634 640
35. H.H. Bauer, U. Aebi, M. Häner, R. Hermann, M. Müller, T. Arvinte, and H.P. Merkle Architecture and polymorphism of fibrillar supramolecular assemblies produced by in vitro aggregation of human calcitonin J. Struct. Biol. 115 1995 1 15
36. F.R. Green III, B. Lynch, and E.T. Kaiser Biological and physical properties of a model calcitonin containing a glutamate residue interrupting the hydrophobic face of the idealized amphiphilic alpha-helical region Proc. Natl. Acad. Sci. U. S. A. 84 1987 8340 8344
37. E. Querol, J.A. Perez-Pons, and A. Mozo-Villarias Analysis of protein conformational characteristics related to thermostability Protein Eng. 9 1996 265 271 (Pubitemid 26148306)
38. D. Stigter, and K.D. Dill Theory for protein solubilities Fluid Phase Equilib. 82 1993 237 249 (Pubitemid 23637735)
39. G.B. Fields, D.O.V. Alonso, and D. Stigter Theory for the aggregation of proteins and copolymers J. Phys. Chem. 96 1992 3974 3981 (9)
40. K.H. Bhandari, M. Newa, H. Uludag, and M.R. Doschak Synthesis, characterization and in vitro evaluation of a bone targeting delivery system for salmon calcitonin Int. J. Pharm. 394 2010 26 34
41. T.J. Martin, D.M. Findlay, I. MacIntyre, J.A. Eisman, V.P. Michelangeli, J.M. Mosley, and N.C. Partridge Calcitonin receptors in a cloned human breast cancer cell line (MCF-7) Biochem. Biophys. Res. Commun. 96 1980 150 156 (Pubitemid 11246646)
42. L.J. Deftos, J.J. Nolan, B.L. Seely, P.L. Clopton, G.J. Cote, C.L. Whitham, L.J. Florek, T.A. Christensen, and M.R. Hill Intrapulmonary drug delivery of salmon calcitonin Calcif. Tissue Int. 61 1997 345 347 (Pubitemid 27430121)
43. G.A. Rodan, and T.J. Martin Therapeutic approaches to bone diseases Science 289 2000 1508 1514
44. Y. Okubo, K. Bessho, K. Fujimura, K. Kusumoto, Y. Ogawa, and T. Iizuka Effect of e-calcitonin on oeteoinduction by recombinant human bone morphogenetic perotein-2 Biochem. Biophys. Res. Commun. 269 2000 317 321 (Pubitemid 30440296)
45. K.H. Song, S.J. Chung, and C.K. Shim Preparation and evaluation of proliposomes containing salmon calcitonin J. Control. Release 84 2002 27 37
46. K. Overgaard, D. Agnusdei, M.A. Hansen, E. Maioli, C. Christiansen, and C. Gennari Dose response bioactivity and bioavailability of salmon calcitonin in premenopausal and postmenopausal women J. Clin. Endocrinol. Metab. 72 1991 344 349 (Pubitemid 21921697)
47. S. Jevsevar, M. Kunstelj, and V.G. Porekar PEGylation of therapeutic proteins Biotechnol. J. 5 2010 113 128
48. J.S. Kang, P.P. Deluca, and K.C. Lee Emerging PEGylated drugs Expert Opin. Emerg. Drugs 14 2009 363 380
49. F.M. Veronese, and G. Pasut PEGylation, successful approach to drug delivery Drug Discov. Today 10 2005 1451 1458 (Pubitemid 41483874)
50. C.J. Fee Size comparison between proteins PEGylated with branched and linear poly(ethylene glycol) molecules Biotechnol. Bioeng. 98 2007 725 731 (Pubitemid 350032676)
51. M. Hamidi, A. Azadi, and P. Rafiei Pharmacokinetic consequences of PEGylation Drug Deliv. 13 2006 399 4099
52. S.M. Ryan, J.M. Frias, X. Wang, C.T. Sayers, D.M. Haddletin, and D.J. Brayden PK/PD modelling of comb-shaped PEGylated salmon calcitonin conjugates of differing molecular weights J. Control. Release 149 2011 126 132
53. B. Warshafsky, J.E. Aubin, and J.N. Heersche Cytoskeleton rearrangements during calcitonin-induced changes in osteoclast motility in vitro Bone 6 1985 179 185 (Pubitemid 15021920)
54. P.M. Sexton, D.M. Findlay, and T.J. Martin Calcitonin Curr. Med. Chem. 6 1999 1067 1093 (Pubitemid 29496041)
55. 2+/inositol phosphate signaling pathways Mol. Endocrinol. 6 1992 551 556
56. H. Warshawsky, D. Goltzman, M.F. Rouleau, and J.J.M. Bergeron Direct in vivo demonstration by radioautography of specific binding sites for calcitonin in skeletal and renal tissues of the rat J. Cell Biol. 85 1980 682 694 (Pubitemid 10007437)
57. D. Goltzman Interaction of calcitonin and calcitonin gene-related peptide at receptor sites in target tissues Science 227 1985 1343 1345 (Pubitemid 15138521)
58. P.M. Fouchereau, M.S. Moukhtar, A.A. Benson, and G. Milhaud Characterization of specific receptors for calcitonin in porcine lung Proc. Natl. Acad. Sci. U. S. A. 78 1981 3973 3975 (Pubitemid 11060599)
59. G.C. Nicholson, C.S. D'Santos, T. Evans, J.M. Moseley, B.E. Kemp, V.P. Michelangeli, and T.J. Martin Human placental calcitonin receptors Biochem. J. 250 1988 877 882 (Pubitemid 18077492)
60. A.H. Gorn, H.Y. Lin, M. Yamin, P.E. Auron, M.R. Flannery, D.R. Tapp, C.A. Manning, H.F. Lodish, S.M. Krane, and S.R. Goldring Cloning, characterization and expression of a human calcitonin receptor from an ovarian carcinoma cell line J. Clin. Invest. 90 1992 1726 1735
61. L. Silvestroni, A. Menditto, G. Frajese, and L. Gnessi Identification of calcitonin receptors in human spermatozoa J. Clin. Endocrinol. Metab. 65 1987 742 746 (Pubitemid 17157395)
62. S.D. Yoo, H. Jun, B.S. Shin, H.S. Lee, M.O. Park, P.P. DeLuca, and K.C. Lee Pharmacokinetic disposition of polyethylene glycol-modified salmon calcitonin Chem. Pharm. Bull. 48 2000 1921 1924 (Pubitemid 32011521)
63. S. Kasugai, R. Fujisawa, Y. Waki, K. Miyamoto, and K. Ohya Selective drug delivery system to bone: small peptide (Asp)6 conjugation J. Bone Miner. Res. 15 2000 936 943 (Pubitemid 30233418)
64. H. Hirabayashi, and J. Fujisaki Bone-specific drug delivery systems: approaches via chemical modification of bone-seeking agents Clin. Pharmacokinet. 42 2003 1319 1330 (Pubitemid 38045839)
65. M. Morioka, A. Kamizono, H. Takikawa, A. Mori, H. Ueno, S. Kadowaki, Y. Nakao, K. Kato, and K. Umezawa Design, synthesis, and biological evaluation of novel estradiol-bisphosphonate conjugates as bone-specific estrogens Bioorg. Med. Chem. 18 2010 143 1488
66. D. Wang, S.C. Miller, P. Kopeckova, and J. Kopecek Bone-targeting macromolecular therapeutics Adv. Drug Deliv. Rev. 57 2005 1049 1076 (Pubitemid 40692291)
67. M.D. Fancis, and I. Fogelman 99mTc diphosphonate uptake mechanism on bone I. Fogelman, Bone Scanning in Clinical Practice 1987 Springer-Verlag New York 7 17
68. H.M. Lamb, and D. Faulds Samarium 153Sm lexidronam Drugs Aging 11 1997 413 418
69. D. Wang, S.C. Miller, M. Sima, P. Kopeckova, and J. Kopecek Synthesis of polymeric bone-targeting drug delivery systems Bioconjug. Chem. 14 2003 853 859 (Pubitemid 37157997)
70. S.A. Gittens, G. Bansal, R.F. Zernicke, and H. Uludag Designing proteins for bone targeting Adv. Drug Deliv. Rev. 57 2005 1011 1036 (Pubitemid 40703886)
71. G. Siligardi, B. SamorI, S. Melandri, M. Visconti, and A.F. Drake Correlations between biological activities and conformational properties for human, salmon, eel, porcine calcitonins and Elcatonin elucidated by CD spectroscopy Eur. J. Biochem. 221 1994 1117 1125 (Pubitemid 24146216)
72. R.M. Epand, R.F. Epand, R.C. Orlowski, R.J. Schlueter, L.T. Boni, and S.W. Hui Amphipathic helix and its relationship to the interaction of calcitonin with phospholipids Biochemistry 22 1983 5014 5084
73. W. Rittel, R. Maier, B. Brugger, B. Kamber, B. Rimker, and P. Sieber Structure-activity relationship of human calcitonin III. Biological activity of synthetic analogs with shortened or terminally modified peptide chains Experientia 32 1976 246 248
74. C.S. D'Santos, G.C. Nicholson, J.M. Moseley, T. Evans, T.J. Martin, and B.E. Kemp Biologically active, derivatizable salmon calcitonin analog: design, synthesis and applications Endocrinology 123 1988 1483 1488
75. M. Newa, K.H. Bhandari, L. Tang, R. Kalvapalle, M. Suresh, and M.R. Doschak Antibody-mediated "universal" osteoclast targeting platform using calcitonin as a model drug Pharm. Res. 28 2011 1131 1143
76. M.R. Doschak, C.M. Kucharski, J.E.I. Wright, R.F. Zernicke, and H. Uludag Improved bone delivery of osteoprotegerin by bisphosphonate conjugation in a rat model of osteoarthritis Mol. Pharm. 6 2009 634 640
77. H.H. Bauer, U. Aebi, M. Häner, R. Hermann, M. Müller, T. Arvinte, and H.P. Merkle Architecture and polymorphism of fibrillar supramolecular assemblies produced by in vitro aggregation of human calcitonin J. Struct. Biol. 115 1995 1 15
78. F.R. Green III, B. Lynch, and E.T. Kaiser Biological and physical properties of a model calcitonin containing a glutamate residue interrupting the hydrophobic face of the idealized amphiphilic alpha-helical region Proc. Natl. Acad. Sci. U. S. A. 84 1987 8340 8344
79. E. Querol, J.A. Perez-Pons, and A. Mozo-Villarias Analysis of protein conformational characteristics related to thermostability Protein Eng. 9 1996 265 271 (Pubitemid 26148306)
80. D. Stigter, and K.D. Dill Theory for protein solubilities Fluid Phase Equilib. 82 1993 237 249 (Pubitemid 23637735)
81. G.B. Fields, D.O.V. Alonso, and D. Stigter Theory for the aggregation of proteins and copolymers J. Phys. Chem. 96 1992 3974 3981 (9)
82. K.H. Bhandari, M. Newa, H. Uludag, and M.R. Doschak Synthesis, characterization and in vitro evaluation of a bone targeting delivery system for salmon calcitonin Int. J. Pharm. 394 2010 26 34
83. T.J. Martin, D.M. Findlay, I. MacIntyre, J.A. Eisman, V.P. Michelangeli, J.M. Mosley, and N.C. Partridge Calcitonin receptors in a cloned human breast cancer cell line (MCF-7) Biochem. Biophys. Res. Commun. 96 1980 150 156 (Pubitemid 11246646)
84. L.J. Deftos, J.J. Nolan, B.L. Seely, P.L. Clopton, G.J. Cote, C.L. Whitham, L.J. Florek, T.A. Christensen, and M.R. Hill Intrapulmonary drug delivery of salmon calcitonin Calcif. Tissue Int. 61 1997 345 347 (Pubitemid 27430121)