Export file:

Format

  • RIS(for EndNote,Reference Manager,ProCite)
  • BibTex
  • Text

Content

  • Citation Only
  • Citation and Abstract

Salmon calcitonin: conformational changes and stabilizer effects

Laboratory of Pharmaceutics & Biopharmaceutics, Department of Biotechnology and Pharmaceutical Technology, Yuanpei University, Hsin Chu 30015, Taiwan, ROC

Topical Section: Protein: Structure and Function

The therapeutic activity of peptides or protein drugs is highly dependent on their conformational structure. The protein structure is flexible and responds to external conditions, which may compromise the protein's native conformation and influence its physical and chemical stability. The physical and chemical stability of peptides or protein drugs are important characteristics of biopharmaceutical products. Calcitonin (CT) is a polypeptide hormone that participates in diverse physiological functions in humans; therefore, it is a potentially useful protein for investigations of different aspects of pharmacology and drug delivery systems. Of the different types of CT available for clinical use, salmon CT (sCT) is one of the most potent. In this review article, the commercially available sCT was selected as a suitable peptide candidate for the discussion of its stability and conformational changes in the aqueous and solid states using Fourier transform infrared (FTIR) spectroscopic analysis under different external conditions, including pH, temperature, drying method, and added excipients. Particularly, excipients that have been optimized as stabilizers of sCT in aqueous solution and as lyophilized and spray-dried drug formulations are also discussed.
  Figure/Table
  Supplementary
  Article Metrics

Keywords Salmon calcitonin; conformation; stability; solution; solid state; stabilizer

Citation: Shan-Yang Lin. Salmon calcitonin: conformational changes and stabilizer effects. AIMS Biophysics, 2015, 2(4): 695-723. doi: 10.3934/biophy.2015.4.695

References

  • 1. Fosgerau K, Hoffmann T (2015) Peptide therapeutics: current status and future directions. Drug Discov Today 20: 122-128.    
  • 2. Leader B, Baca QJ, Golan DE (2008) Protein therapeutics: a summary and pharmacological classification. Nat Rev Drug Discov 7: 21-39.    
  • 3. Craik DJ, Fairlie DP, Liras S, et al. (2013) The future of peptide-based drugs. Chem Biol Drug Des 81: 136-147.    
  • 4. Bruno BJ, Miller GD, Lim CS (2013) Basics and recent advances in peptide and protein drug delivery. Ther Deliv 4: 1443-1467.    
  • 5. Ratnaparkhi MP, Chaudhari SP, Pandya VA (2011) Peptides and proteins in pharmaceuticals. Int J Curr Pharm Res 3 (2): 1-9.
  • 6. Mullard A (2011) 2010 FDA Approvals. Nat Rev Drug Discov 10: 82-85.    
  • 7. Kneller R (2010) The importance of new companies for drug discovery: Origins of a decade of new drugs. Nat Rev Drug Discov 9: 867-882.    
  • 8. Uhlig T, Kyprianou TD, Martinelli FG, et al. (2014) The emergence of peptides in the pharmaceutical business: From exploration to exploitation. EuPA Open Proteom 4: 58-69.    
  • 9. Frokjaer S, Otzen DE (2005) Protein drug stability: a formulation challenge. Nat Rev Drug Discov 4: 298-306.    
  • 10. van de Weert M, Randolph TW (2012) Physical instability of peptides and pProteins, In: Hovgaard L, Frokjaer S, Van De Weert M, Pharmaceutical Formulation Development of Peptides and Proteins, 2 Eds. , Florida: CRC Press, 107-129.
  • 11. Rathore N, Rajan RS (2008) Current perspectives on stability of protein drug products during formulation, fill and finish operations. Biotechnol Prog 24: 504-514.    
  • 12. Taverna DM, Goldstein RA (2002) Why are proteins marginally stable? Proteins 46: 105-109.    
  • 13. Williams PD, Pollock DD, Goldstein RA (2006) Functionality and the evolution of marginal stability in proteins: Inferences from lattice simulations. Evol Bioinform Online 2: 91-101.
  • 14. Chang BS, Yeung B (2010) Physical stability of protein pharmaceuticals, In: Jameel F, Hershenson S, Formulation and Process Development Strategies for Manufacturing Biopharmaceuticals, New Jersey: John Wiley & Sons Inc, 69-104.
  • 15. Lai MC, Topp EM (1999) Solid-state chemical stability of proteins and peptides. J Pharm Sci 88: 489-500.    
  • 16. Chaudhuri R, Cheng Y, Middaugh CR, et al. (2014) High-throughput biophysical analysis of protein therapeutics to examine interrelationships between aggregate formation and conformational stability. AAPS J 16: 48-64.    
  • 17. Jacob S, Shirwaikar A, Srinivasan K, et al. (2006) Stability of proteins in aqueous solution and solid state. Indian J Pharm Sci 68: 154-163.
  • 18. Manning MC, Chou DK, Murphy BM, et al. (2010) Stability of protein pharmaceuticals: an update. Pharm Res 27: 544-575.    
  • 19. Carpenter JF, Manning MC (2002) Rational Design of Stable Protein Formulations: Theory and Practice, New York: Kluwert Academic /Plenum Publishers.
  • 20. Pace CN, Grimsley GR, Scholtz JM, et al. (2014) Protein stability. In: eLS. John Wiley & Sons Ltd, Chichester. Available from: http://onlinelibrary. wiley. com/doi/10. 1002/9780470015902. a0003002. pub3/otherversions
  • 21. Banga AK (2015) Therapeutic Peptides and Proteins: Formulation, Processing, and Delivery Systems, 3 Eds. , Florida: CRC Press.
  • 22. Ohtake S, Wang W (2013) Protein and peptide formulation development. Pharmaceutical Sciences Encyclopedia 11: 1-44.
  • 23. Krishnamurthy R, Manning MC (2002) The stability factor: importance in formulation development. Curr Pharm Biotechnol 3: 361-371.    
  • 24. Cicerone MT, Pikal MJ, Qian KK (2015) Stabilization of proteins in solid form. Adv Drug Deliv Rev doi: 10. 1016/j. addr. 2015. 05. 006.
  • 25. Murphy KP (2001) Protein structure, stability, and folding, Series: Methods in Molecular Biology, Vol. 168, New Jersey: Humana Press.
  • 26. Scheeff ED, Fink JL (2003) Fundamentals of protein structure. Methods Biochem Anal 44: 15-39.
  • 27. Adler MJ, Jamieson AG, Hamilton AD (2011) Hydrogen-bonded synthetic mimics of protein secondary structure as disruptors of protein-protein interactions. Curr Top Microbiol Immunol 348: 1-23.
  • 28. Kwok SC, Mant CT, Hodges RS (2002) Importance of secondary structural specificity determinants in protein folding: insertion of a native beta-sheet sequence into an alpha-helical coiled-coil. Protein Sci 11: 1519-1531.
  • 29. Jorgensen L, Hostrup S, Moeller EH, et al. (2009) Recent trends in stabilizing peptides and proteins in pharmaceutical formulation - considerations in the choice of excipients. Expert Opin Drug Deliv 6: 1219-1230.    
  • 30. Hirsch PF, Baruch H (2003) Is calcitonin an important physiological substance? Endocrine 21: 201-208.    
  • 31. Huang CL, Sun L, Moonga BS, et al. (2006) Molecular physiology and pharmacology of calcitonin. Cell Mol Biol 52: 33-43.
  • 32. Väänänen K (2005) Mechanism of osteoclast mediated bone resorption--rationale for the design of new therapeutics. Adv Drug Deliv Rev 57: 959-971.    
  • 33. Davey RA, Findlay DM (2013) Calcitonin: physiology or fantasy? J Bone Miner Res 28: 973-979.    
  • 34. Felsenfeld AJ, Levine BS (2015) Calcitonin, the forgotten hormone: does it deserve to be forgotten? Clin Kidney J 8: 180-187.    
  • 35. Pondel M (2000) Calcitonin and calcitonin receptors: bone and beyond. Int J Exp Pathol 81: 405-422.
  • 36. Endres DB, Rude RK (1999) Mineral and bone metabolism, In: Burtis CA, Ashwood ER Author, Textbook of Clinical Chemistry, 3 Eds. , Pennsylvania: W B Saunders Company, 1395-1457
  • 37. Ramasamy I (2006) Recent advances in physiological calcium homeostasis. Clin Chem Lab Med 44: 237-273.
  • 38. Chesnut CH 3rd, Azria M, Silverman S, et al. (2008) Salmon calcitonin: a review of current and future therapeutic indications. Osteoporos Int 19: 479-491.    
  • 39. Chakraborty C, Nandi S, Sinha S (2004) Overexpression, purification and characterization of recombinant salmon calcitonin, a therapeutic protein, in Streptomyces avermitilis. Protein Pept Lett 11: 165-173.    
  • 40. O'Connell MB (2006) Prescription drug therapies for prevention and treatment of postmenopausal osteoporosis. J Manag Care Pharm 12(6 Suppl A): S10-9, quiz S26-8.
  • 41. Sexton PM, Findlay DM, Martin TJ (1999) Calcitonin. Curr Med Chem 6: 1067-1093.
  • 42. Windich V, De Luccia F, Herman F, et al. (1997) Degradation pathways of salmon calcitonin in aqueous solution. J Pharm Sci 86: 359-364.    
  • 43. Torres-Lugo M, Peppas NA (2000) Transmucosal delivery systems for calcitonin: a review. Biomaterials 21: 1191-1196.    
  • 44. Azria M (2003) Osteoporosis management in day-to-day practice. The role of calcitonin. J Musculoskelet Neuronal Interact 3: 210-213.
  • 45. Karsdal MA, Henriksen K, Arnold M , et al. (2008) Calcitonin: a drug of the past or for the future? Physiologic inhibition of bone resorption while sustaining osteoclast numbers improves bone quality. BioDrugs 22: 137-144.
  • 46. Azria M, Copp DH, Zanelli JM (1995) 25 years of salmon-calcitonin—from synthesis to therapeutic use. Calcif Tissue Int 57: 405-408.    
  • 47. D'Hondt M, Van Dorpe S, Mehuys E, et al. (2010) Quality analysis of salmon calcitonin in a polymeric bioadhesive pharmaceutical formulation: sample preparation optimization by DOE. J Pharm Biomed Anal 53: 939-945.    
  • 48. Hong B, Wu B, Li Y (2003) Production of C-terminal amidated recombinant salmon calcitonin in Streptomyces lividans. Appl Biochem Biotechnol 110: 113-123.    
  • 49. Andreassen KV, Hjuler ST, Furness SG, et al. (2014) Prolonged calcitonin receptor signaling by salmon, but not human calcitonin, reveals ligand bias. PLoS One 9: e92042.    
  • 50. Stevenson JC, Evans IM (1981) Pharmacology and therapeutic use of calcitonin. Drugs 21: 257-272.    
  • 51. Renukuntla J, Vadlapudi AD, Patel A, et al. (2013) Approaches for enhancing oral bioavailability of peptides and proteins. Int J Pharm 447: 75-93.    
  • 52. Hoyer H, Perera G, Bernkop-Schnürch A (2010) Noninvasive delivery systems for peptides and proteins in osteoporosis therapy: a retroperspective. Drug Dev Ind Pharm 36: 31-44.    
  • 53. Satoh T, Yoshida G, Orito Y, et al. (1998) Drug delivery system for the treatment of osteoporosis. Nihon Rinsho 56: 742-747.
  • 54. Sinsuebpol C, Chatchawalsaisin J, Kulvanich P (2013) Preparation and in vivo absorption evaluation of spray dried powders containing salmon calcitonin loaded chitosan nanoparticles for pulmonary delivery. Drug Des Devel Ther 7: 861-873.
  • 55. Tas C, Mansoor S, Kalluri H, et al. (2012) Delivery of salmon calcitonin using a microneedle patch. Int J Pharm 423: 257-263.    
  • 56. Cholewinsky M, Luckel B, Horn H (1996) Degradation pathways, analytical characterization and formulation strategies of a peptide and a protein Calcitonin and human growth hormone in comparison. Pharm Acta Helv 71: 405-419.    
  • 57. Uda K, Kobayashi Y, Hisada T, et al. (1999) Stable human calcitonin analogues with high potency on bone together with reduced anorectic and renal actions. Biol Pharm Bull 22: 244-252.    
  • 58. Cudd A, Arvinte T, Das RE, et al. (1995) Enhanced potency of human calcitonin when fibrillation is avoided. J Pharm Sci 84: 717-719.    
  • 59. Wang W, Roberts CJ (2010) Aggregation of Therapeutic Proteins, 1 Eds. , New Jersey: John Wiley & Sons Inc.
  • 60. den Engelsman J, Garidel P, Smulders R, et al. (2011) Strategies for the assessment of protein aggregates in pharmaceutical biotech product development. Pharm Res 28: 920-933.    
  • 61. Bryan J (2014) Protein aggregation: formulating a problem. Pharm J 293: 7826.
  • 62. Mahler HC, Friess W, Grauschopf U, et al. (2009) Protein aggregation: pathways, induction factors, and analysis. J Pharm Sci 98: 2909-2934.    
  • 63. Brange J, Andersen L, Laursen ED, et al. (1997) Toward understanding insulin fibrillation. J Pharm Sci 86: 517-525.    
  • 64. Shire SJ, Shahrokh Z, Liu J (2004) Challenges in the development of high protein concentration formulations. J Pharm Sci 93: 1390-1402.    
  • 65. Thirumangalathu R, Krishnan S, Brems DN, et al. (2006) Effects of pH, temperature, and sucrose on benzyl alcohol-induced aggregation of recombinant human granulocyte colony stimulating factor. J Pharm Sci 95: 1480-1497.    
  • 66. Wang W, Wang YJ, Wang DQ (2008) Dual effects of Tween 80 on protein stability. Int J Pharm 347: 31-38.    
  • 67. Carpenter JF, Pikal MJ, Chang BS, et al. (1997) Rational design of stable lyophilized protein formulations: Some practical advice. Pharm Res 14: 969-975.    
  • 68. Chi EY, Weickmann J, Carpenter JF, et al. (2005) Heterogeneous nucleation-controlled particulate formation of recombinant human platelet-activating factor acetylhydrolase in pharmaceutical formulation. J Pharm Sci 94: 256-274.    
  • 69. KatakamM, Bell LN, Banga AK (1995) Effect of surfactants on the physical stability of recombinant human growth hormone. J Pharm Sci 84: 713-716.    
  • 70. Taylor JW, Jin QK, Sbacchi M, et al. (2002) Side-chain lactam-bridge conformational constraints differentiate the activities of salmon and human calcitonins and reveal a new design concept for potent calcitonin analogues. J Med Chem 45: 1108-1121.    
  • 71. Karsdal MA, Henriksen K, Arnold M, et al. (2008) Calcitonin: a drug of the past or for the future? Physiologic inhibition of bone resorption while sustaining osteoclast numbers improves bone quality. BioDrugs 22: 137-144.
  • 72. Kapurniotu A, Taylor JW (1995) Structural and conformational requirements for human calcitonin activity: Design, synthesis, and study of lactam-bridged Analogues. J Med Chem 3: 836-847.
  • 73. Cholewinski M, Lückel B, Horn H. (1996) Degradation pathways, analytical characterization and formulation strategies of a peptide and a protein calcitonine and human growth hormone in comparison. Pharm Acta Helv 71: 405-419.
  • 74. Wang W (1999) Instability, stabilization, and formulation of liquid protein pharmaceuticals. Int J Pharm 185: 129-188.
  • 75. Wang W (2000) Lyophilization and development of solid protein pharmaceuticals. Int J Pharm 203: 1-60.
  • 76. Rathore N, Rajan RS (2008) Current perspectives on stability of protein drug products during formulation, fill and finish operations. Biotechnol Prog 24: 504-514.    
  • 77. Krishnamurthy R, Manning MC (2002) The stability factor: importance in formulation development. Curr Pharm Biotechnol 3: 361-371.    
  • 78. Chang SL, Hofmann GA, Zhang L, et al. (2003) Stability of a transdermal salmon calcitonin formulation. Drug Deliv 10: 41-45.    
  • 79. Bauer HH, Aebi U, Häner M, et al. (1995) Architecture and polymorphism of fibrillar supramolecular assemblies produced by in vitro aggregation of human calcitonin. J Struct Biol 115: 1-15.    
  • 80. Avidan-Shpalter C, Gazit E (2006) The early stages of amyloid formation: biophysical and structural characterization of human calcitonin pre-fibrillar assemblies. Amyloid 13: 216-225.    
  • 81. Diociaiuti M, Gaudiano MC, Malchiodi-Albedi F (2011) The slowly aggregating salmon Calcitonin: a useful tool for the study of the amyloid oligomers structure and activity. Int J Mol Sci 12: 9277-9295.    
  • 82. Seyferth S, Lee G (2003) Structural studies of EDTA-induced fibrillation of salmon calcitonin. Pharm Res 20: 73-80.    
  • 83. Nakamuta H, Orlowski RC, Epand RM (1990) Evidence for calcitonin receptor heterogenecity: binding studies with non-helical analogs. Endocrinology 127: 163-169.    
  • 84. Siligardi G, Samori B, Melandri S, et al. (1994) Correlations between biological activities and conformation properties for human, salmon, eel, porcine calcitonins and Elcatonin elucidated by CD spectroscopy. Eur J Biochem 221: 1117-1125.    
  • 85. Moriarty DF, Vagts S, Raleigh DP (1998) A role for the C-terminus of calcitonin in aggregation and gel formation: a comparative study of C-terminal Fragments of human and salmon calcitonin. Biochem Biophys Res Commun 245: 344-348.    
  • 86. van Dijkhuizen-Radersma R, Nicolas HM, van de Weert M, et al. (2002) Stability aspects of salmon calcitonin entrapped in poly(ether-ester) sustained release systems. Int J Pharm 248: 229-237.    
  • 87. Tang Y, Singh J (2010) Thermosensitive drug delivery system of salmon calcitonin: in vitro release, in vivo absorption, bioactivity and therapeutic efficacies. Pharm Res 27: 272-284.    
  • 88. Windisch V, Deluccia F, Duhau L, et al. (1997) Degradation pathways of salmon calcitonin in aqueous solution. J Pharm Sci 86: 359-364.    
  • 89. Lucke A, Kiermaier J, Gopferich A (2002) Peptide acylation by poly(α-hydroxy esters). Pharm Res 19: 175-181.    
  • 90. Montgomerie S, Sundararaj S, Gallin WJ, et al. (2006) Improving the accuracy of protein secondary structure prediction using structural alignment. BMC Bioinformatics 7: 301.    
  • 91. Rost B (2001) Review: protein secondary structure prediction continues to rise. J Struct Biol 134: 204-218.
  • 92. Pirovano W, Heringa J (2010) Protein secondary structure prediction. Methods Mol Biol 609: 327-348.    
  • 93. Kwok SC, Mant CT, Hodges RS (2002) Importance of secondary structural specificity determinants in protein folding: insertion of a native beta-sheet sequence into an alpha-helical coiled-coil. Protein Sci 11: 1519-1531.    
  • 94. Ji YY, Li YQ (2010) The role of secondary structure in protein structure selection. Eur Phys J E Soft Matter 32: 103-107.    
  • 95. Haris PI, Chapman D (1995) The conformational analysis of peptides using Fourier transform IR spectroscopy. Biopolymers 37: 251-263.    
  • 96. Manning MC (2005) Use of infrared spectroscopy to monitor protein structure and stability. Expert Rev Proteomics 2: 731-743.    
  • 97. Kong J, Yu S (2007) Fourier transform infrared spectroscopic analysis of protein secondary structures. Acta Biochim Biophys Sinica 39: 549-559
  • 98. Carpenter JF, Chang BS, Garzon-Rodriguez W, et al. (2002) Rational design of stable lyophilized protein formulations: Theory and practice. Pharm Biotechnol 13: 109-133.    
  • 99. Chang LL, Pikal MJ (2009) Mechanisms of protein stabilization in the solid state. J Pharm Sci 98: 2886-2908.    
  • 100. Wang W (2000) Lyophilization and development of solid protein pharmaceuticals. Int J Pharm 203: 1-60.    
  • 101. Maa Y-F, Prestrelski SJ (2000) Biopharmaceutical powders: Particle formation and formulation considerations. Curr Pharm Biotechnol 1: 283-302.    
  • 102. Abdul-Fattah AM, Kalonia DS, Pikal MJ (2007) The challenge of drying method selection for protein pharmaceuticals: Product quality implications. J Pharm Sci 96: 1886-1916.    
  • 103. Abdul-Fattah AM, Truong-Le V, Yee L, et al. (2007) Drying induced variations in physico-chemical properties of amorphous pharmaceuticals and their impact on stability (I): Stability of a monoclonal antibody. J Pharm Sci 96: 1983-2008.    
  • 104. Klibanov AM, Schefiliti JA (2004) On the relationship between conformation and stability in solid pharmaceutical protein formulations. Biotechnol Lett 26: 1103-1106.    
  • 105. Angkawinitwong U, Sharma G, Khaw PT, et al. (2015) Solid-state protein formulations. Ther Deliv 6: 59-82.    
  • 106. Lee TH, Cheng WT, Lin SY (2010) Thermal stability and conformational structure of salmon calcitonin in the solid and liquid states. Biopolymers 93: 200-207.    
  • 107. Stevenson CL, Tan MM (2000) Solution stability of salmon calcitonin at high concentration for delivery in an implantable system. J Pept Res 55: 129-139.    
  • 108. Dong A, Huang P, Caughey WS (1990) Protein secondary structures in water from second-derivative amide I infrared spectra. Biochemistry 29: 3303-3308.    
  • 109. Kanari K, Nosaka A (1995) Study of human calcitonin fibrillation by proton nuclear magnetic resonance spectroscopy. Biochemistry 34: 12138-12143.
  • 110. Arvinte T, Drake A (1993) Comparative study of human and salmon calcitonin secondary structure in solutions with low dielectric constants. J Biol Chem 268: 6408-6414.
  • 111. Lee SL, Yu LX, Cai B, et al. (2011) Scientific considerations for generic synthetic salmon calcitonin nasal spray products. AAPS J 13: 14-19.    
  • 112. Binkley N, Bone H, Gilligan JP, et al. (2014) Efficacy and safety of oral recombinant calcitonin tablets in postmenopausal women with low bone mass and increased fracture risk: a randomized, placebo-controlled trial. Osteoporos Int 25: 2649-2656.    
  • 113. Murphy LR, Matubayasi N, Payne VA, et al. (1998) Protein hydration and unfolding-insights from experimental partial specific volumes and unfolded protein models. Fold Des 3: 105-118.    
  • 114. Schiffer CA, Dötsch V (1996) The role of protein-solvent interactions in protein unfolding. Curr Opin Biotechnol 7: 428-432.    
  • 115. Lee JC (2000) Biopharmaceutical formulation. Curr Opin Biotechnol 11: 81-84.    
  • 116. Canchi DR, García AE (2013) Cosolvent effects on protein stability. Annu Rev Phys Chem 64: 273-293.    
  • 117. England JL, Haran G (2011) Role of solvation effects in protein denaturation: from thermodynamics to single molecules and back. Annu Rev Phys Chem 62: 257-277.    
  • 118. Lee TH, Lin SY (2011) Pluronic F68 enhanced the conformational stability of salmon calcitonin in both aqueous solution and lyophilized solid form. Biopolymers 95: 785-791.
  • 119. Lee TH, Lin SY (2011) Additives affecting thermal stability of salmon calcitonin in aqueous solution and structural similarity in lyophilized solid form. Process Biochem 46: 2163-2169.    
  • 120. Andreotti G, Méndez BL, Amodeo P, et al. (2006) Structural determinants of salmon calcitonin bioactivity: the role of the Leu-based amphipathic alpha-helix. J Biol Chem 281: 24193-24203.    
  • 121. Carpenter JF, Prestrelski SJ, Dong A (1998) Application of infrared spectroscopy to development of stable lyophilized protein formulations. Eur J Pharm Biopharm 45: 231-238.    
  • 122. Haris PI, Chapman D (1994) Analysis of polypeptide and protein structures using Fourier transform infrared spectroscopy. Methods Mol Biol 22: 183-202.
  • 123. Pedone E, Bartolucci S, Rossi M, et al. (2003) Structural and thermal stability analysis of Escherichia coli and Alicyclobacillus acidocaldarius thioredoxin revealed a molten globule-like state in thermal denaturation pathway of the proteins: an infrared spectroscopic study. Biochem J 373: 875-883.    
  • 124. Cook TJ, Shenoy SS (2002) Stability of calcitonin salmon in nasal spray at elevated temperatures. Am J Health Syst Pharm 59: 713-715.
  • 125. Lee KC, Lee YJ, Song HM, et al. (1992) Degradation of synthetic salmon calcitonin in aqueous solution. Pharm Res 9: 1521-1523.    
  • 126. Windisch V, DeLuccia F, Duhau L, et al. (1997) Degradation pathways of salmon calcitonin in aqueous solution. J Pharm Sci 86: 359-364.    
  • 127. Kamihira M, Naito A, Tuzi S, et al. (2000) Conformational transitions and fibrillation mechanism of human calcitonin as studied by high-resolution solid-state 13C NMR. Protein Sci 9: 867-877.    
  • 128. Andreotti G, Motta A (2004) Modulating calcitonin fibrillogenesis: an antiparallel alpha-helical dimer inhibits fibrillation of salmon calcitonin. J Biol Chem 279: 6364-6370.
  • 129. Gaudiano MC, Colone M, Bombelli C, et al. (2005) Early stages of salmon calcitonin aggregation: effect induced by ageing and oxidation processes in water and in the presence of model membranes. Biochim Biophys Acta 1750: 134-145.    
  • 130. Diociaiuti M, Macchia G, Paradisi S, et al. (2014) Native metastable prefibrillar oligomers are the most neurotoxic species among amyloid aggregates. Biochim Biophys Acta 1842: 1622-1629.    
  • 131. Gilchrist PJ, Bradshow JP (1993) Amyloid formation by salmon calcitonin. Biochim Biophys Acta 1182: 111-114.    
  • 132. Arvinte T, Cudd A, Drake AF (1993) The structure and mechanism of formation of human calcitonin fibrils. J Biol Chem 268: 6415-6422.
  • 133. Rastogi N, Mitra K, Kumar D, et al. (2012) Metal ions as cofactors for aggregation of therapeutic peptide salmon calcitonin. Inorg Chem 51: 5642-5650.    
  • 134. Diociaiuti M, Macchia G, Paradisi S, et al. (2014) Native metastable prefibrillar oligomers are the most neurotoxic species among amyloid aggregates. Biochim Biophys Acta 1842: 1622-1629.    
  • 135. Rawat A, Kumar D (2013) NMR investigations of structural and dynamics features of natively unstructured drug peptide-salmon calcitonin: implication to rational design of potent sCT analogs. J Pept Sci 19: 33-45.    
  • 136. Allison SD, Randolph TW, Manning MC, et al. (1998) Effects of drying methods and additives on structure and function of actin: mechanisms of dehydration-induced damage and its inhibition. Arch Biochem Biophys 358: 171-181.    
  • 137. Bhatnagar BS, Bogner RH, Pikal MJ (2007) Protein stability during freezing: separation of stresses and mechanisms of protein stabilization. Pharm Dev Technol 12: 505-523.
  • 138. Jain NK, Roy I (2009) Effect of trehalose on protein structure. Protein Sci 18: 24-36.
  • 139. Capelle MA, Gurny R, Arvinte T (2007) High throughput screening of protein formulation stability: practical considerations. Eur J Pharm Biopharm 65: 131-148.    
  • 140. Kamerzell TJ, Esfandiary R, Joshi SB, et al. (2011) Protein-excipient interactions: mechanisms and biophysical characterization applied to protein formulation development. Adv Drug Deliv Rev 63: 1118-1159.    
  • 141. Ohtake S, Kita Y, Arakawa T (2011) Interactions of formulation excipients with proteins in solution and in the dried state. Adv Drug Deliv Rev 63: 1053-1073.    
  • 142. Porfire AS, Tomuţa I, Irache JM, et al. (2009) The influence of the formulation factors on physico-chemical properties of dextran associated Gantrez an nanoparticles. Farmacia 57: 463-472.
  • 143. Torres-Lugo M, Peppas NA (1999) Molecular design and in vitro studies of novel pH-sensitive hydrogels for the oral delivery of calcitonin. Macromolecules 32: 6646-6651.
  • 144. Szelke H, Schübel S, Harenberg J, et al. (2010) Interaction of heparin with cationic molecular probes: probe charge is a major determinant of binding stoichiometry and affinity. Bioorg Med Chem Lett 20: 1445-1447.    
  • 145. Houska M, Brynda E (1997) Interactions of proteins with polyelectrolytes at solid/liquid interfaces: Sequential adsorption of albumin and heparin. J Colloid Interface Sci 188: 243-250.    
  • 146. Guo B, Anzai J, Osa T (1996) Adsorption behavior of serum albumin on electrode surfaces and the effects of electrode potential. Chem Pharm Bull (Tokyo) 44: 800-803.    
  • 147. Langer K, Balthasar S, Vogel V, et al. (2003) Optimization of the preparation process for human serum albumin (HSA) nanoparticles. Int J Pharm 257: 169-180.    
  • 148. Prestrelski SJ, Pikal KA, Arakawa T (1995) Optimization of lyophilization conditions for recombinant human interleukin-2 by dried-state conformational analysis using fourier-transform infrared spectroscopy. Pharm Res 12: 1250-1259.    
  • 149. van Dijkhuizen-Radersma R, Nicolas HM, van de Weert M, et al. (2002) Stability aspects of salmon calcitonin entrapped in poly(ether-ester) sustained release systems. Int J Pharm 248: 229-237.    
  • 150. Baudys M, Mix D, Kim SW (1996) Stabilization and intestinal absorption of human calcitonin. J Control Rel 39: 145-151.    
  • 151. Sigurjónsdóttir JF, Loftsson T, Másson M (1999) Influence of cyclodextrins on the stability of the peptide salmon calcitonin in aqueous solution. Int J Pharm 186: 205-213.    
  • 152. Mueller C, Capelle MA, Arvinte T, et al. (2011) Noncovalent pegylation by dansyl-poly(ethylene glycol)s as a new means against aggregation of salmon calcitonin. J Pharm Sci 100: 1648-1662.    
  • 153. Mueller C, Capelle MA, Arvinte T, et al. (2011) Tryptophan-mPEGs: novel excipients that stabilize salmon calcitonin against aggregation by non-covalent PEGylation. Eur J Pharm Biopharm 79: 646-657.    
  • 154. Mueller C, Capelle MA, Seyrek E, et al. (2012) Noncovalent PEGylation: different effects of dansyl-, L-tryptophan-, phenylbutylamino-, benzyl- and cholesteryl-PEGs on the aggregation of salmon calcitonin and lysozyme. J Pharm Sci 101: 1995-2008.    
  • 155. Remmele RL, Krishnan S, Callahan WJ (2012) Development of stable lyophilized protein drug products. Curr Pharm Biotechnol 13: 471-496.    
  • 156. Kasper JC, Friess W (2011) The freezing step in lyophilization: physico-chemical fundamentals, freezing methods and consequences on process performance and quality attributes of biopharmaceuticals. Eur J Pharm Biopharm 78: 248-263.    
  • 157. Costantino HR, Pikal MJ (2004) Lyophilization of Biopharmaceuticals. Virginia: AAPS Press.
  • 158. Susi H, Byler DM (1983) Protein structure by Fourier transform infrared spectroscopy: second derivative spectra. Biochem Biophys Res Commun 115: 391-397.    
  • 159. Prestrelski SJ, Tedeschi N, Arakawa T, et al. (1993) Dehydration-induced conformational transitions in proteins and their inhibition by stabilizers. Biophys J 65: 661-671.    
  • 160. Lee HE, Lee MJ, Park CR, et al. (2010) Preparation and characterization of salmon calcitonin-sodium triphosphate ionic complex for oral delivery. J Control Rel 143: 251-257.    
  • 161. Steckel H, Brandes HG (2004) A novel spray-drying technique to produce low density particles for pulmonary delivery. Int J Pharm 278: 187-195.    
  • 162. Seville PC, Li HY, Learoyd TP (2007) Spray-dried powders for pulmonary drug delivery. Crit Rev Ther Drug Carrier Syst 24: 307-360.    
  • 163. Sollohub K, Cal K (2010) Spray drying technique: II. Current applications in pharmaceutical technology. J Pharm Sci 99: 587-597.
  • 164. Telko M, Hickey A (2005) Dry powder inhaler formulation. Respir Care 50: 1209-1227.
  • 165. Ameri M, Maa Y (2006) Spray Drying of Biopharmaceuticals: Stability and Process Considerations. Drying Technol: A Int J 24: 763-768.    
  • 166. Chan HK, Clark AR, Feeley JC, et al. (2004) Physical stability of salmon calcitonin spray-dried powders for inhalation. J Pharm Sci 93: 792-804.    
  • 167. Yang M, Velaga S, Yamamoto H, et al. (2007) Characterisation of salmon calcitonin in spray-dried powder for inhalation. Effect of chitosan. Int J Pharm 331: 176-181.
  • 168. Sinsuebpol C, Chatchawalsaisin J, Kulvanich P (2013) Preparation and in vivo absorption evaluation of spray dried powders containing salmon calcitonin loaded chitosan nanoparticles for pulmonary delivery. Drug Des Devel Ther 7: 861-873.
  • 169. Amaro MI, Tewes F, Gobbo O, et al. (2015) Formulation, stability and pharmacokinetics of sugar-based salmon calcitonin-loaded nanoporous/nanoparticulate microparticles (NPMPs) for inhalation. Int J Pharm 483: 6-18.
  • 170. Lechuga-Ballesteros D, Charan C, Stults CL, et al. (2008) Trileucine improves aerosol performance and stability of spray-dried powders for inhalation. J Pharm Sci 97: 287-302.    
  • 171. Tewes F, Gobbo OL, Amaro MI, et al. (2011) Evaluation of HP βCD-PEG microparticles for salmon calcitonin administration via pulmonary delivery. Mol Pharm 8: 1887-1898.    
  • 172. Epand RM, Epand RF, Orlowski RC, et al. (1983) Amphipathic helix and its relationship to the interaction of calcitonin with phospholipids. Biochemistry 22: 5074-5084.
  • 173. Epand RM, Epand RF (1986) Conformational flexibility and biological activity of salmon calcitonin. Biochemistry 25: 1964-1968.
  • 174. Green FR 3rd, Lynch B, Kaiser ET (1987) 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: 8340-8344.    
  • 175. Nabuchi Y, Asoh Y, Takayama M (2004) Folding analysis of hormonal polypeptide calcitonins and the oxidized calcitonins using electrospray ionization mass spectrometry combined with H/D exchange. J Am Soc Mass Spectrom 15: 1556-1564.    
  • 176. Siligardi G, Samorí B, Melandri S, et al. (1994) Correlations between biological activities and conformational properties for human, salmon, eel, porcine calcitonins and Elcatonin elucidated by CD spectroscopy. Eur J Biochem 221: 1117-1125.    
  • 177. Andreotti G, Méndez BL, Amodeo P, et al. (2006) Structural determinants of salmon calcitonin bioactivity: the role of the Leu-based amphipathic alpha-helix. J Biol Chem 281: 24193-24203.    
  • 178. Stefani M (2004) Protein misfolding and aggregation: new examples in medicine and biology of the dark side of the protein world. Biochim Biophys Acta 1739: 5-25.    
  • 179. Renukuntla J, Vadlapudi AD, Patel A, et al. (2013) Approaches for enhancing oral bioavailability of peptides and proteins. Int J Pharm 447: 75-93.    
  • 180. Choonara BF, Choonara YE, Kumar P, et al. (2014) A review of advanced oral drug delivery technologies facilitating the protection and absorption of protein and peptide molecules. Biotechnol Adv 32: 1269-1282.    
  • 181. Smart AL, Gaisford S, Basit AW (2014) Oral peptide and protein delivery: intestinal obstacles and commercial prospects. Expert Opin Drug Deliv 11: 1323-1335.    
  • 182. Franks F, Hatley RHM, Mathias SF (1991) Materials science and the production of shelf-stable biologicals. Pharm Technol Int 3: 24-34.
  • 183. Slade L, Levine H (1991) Beyond water activity: Recent advances based on an alternative approach to the assessment of food quality and safety. Crit Rev Food Sci Nutri 30: 115-360.    
  • 184. Carpenter JF, Prestrelski SJ, Arakawa T (1993) Separation of freezing- and drying-induced denaturation of lyophilized proteins using stress-specific stabilization. I. Enzyme activity and calorimetric studies. Arch Biochem Biophys 303: 456-464.
  • 185. Carpenter JF, Crowe JH (1989) An infrared spectroscopic study of the interactions of carbohydrates with dried proteins. Biochemistry 28: 3916-3922.    
  • 186. Crowe JH, Crowe LM, Carpenter JF (1993) Preserving dry biomaterials: The water replacement hypothesis, Part 1. BioPharm 6: 28-29, 32-33.
  • 187. Crowe JH, Crowe LM, Carpenter JF (1993) Preserving dry biomaterials: the water replacement hypothesis, Part 2. BioPharm 6: 40-43.

 

This article has been cited by

  • 1. Lindsey Lipp, Divya Sharma, Amrita Banerjee, Jagdish Singh, Controlled Delivery of Salmon Calcitonin Using Thermosensitive Triblock Copolymer Depot for Treatment of Osteoporosis, ACS Omega, 2019, 4, 1, 1157, 10.1021/acsomega.8b02781

Reader Comments

your name: *   your email: *  

Copyright Info: 2015, Shan-Yang Lin, licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution Licese (http://creativecommons.org/licenses/by/4.0)

Download full text in PDF

Export Citation

Copyright © AIMS Press All Rights Reserved