Pulmonary Insulin-like Growth Factor i Delivery from Trehalose and Silk-Fibroin Microparticles

ACS Biomaterials Science and Engineering

Volumn 1, Issue 2, 2015, Pages 119-129

  Schultz, Isabel ^a   Vollmers, Frederic ^a   Lühmann, Tessa ^a   Rybak, Jens Christoph ^a   Wittmann, Ronja ^b   Stank, Katharina ^b   Steckel, Hartwig ^b   Kardziev, Boris ^c   Schmidt, Michael ^a   Högger, Petra ^a   Meinel, Lorenz ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

^c Thoraxzentrum Bezirk Unterfranken   (Germany)

Author keywords

Calu 3 transepithelial transport; conformation; human lung lobe model; IGF I; pulmonary delivery; silk fibroin

Indexed keywords

SILK FIBROIN; SOMATOMEDIN C; TREHALOSE;

ARTICLE; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG TRANSPORT; DRUG UPTAKE; IN VITRO STUDY; LUNG PERFUSION; PRIORITY JOURNAL;

EID: 84969134482     PISSN: None     EISSN: 23739878     Source Type: Journal    
DOI: 10.1021/ab500101c     Document Type: Article

References (72)

1. Roubenoff, R. Catabolism of aging: is it an inflammatory process? Curr. Opin. Clin. Nutr. Metab. Care 2003, 6, 295-299 10.1097/01.mco.0000068965.34812.62
2. Goldspink, G. Changes in muscle mass and phenotype and the expression of autocrine and systemic growth factors by muscle in response to stretch and overload J. Anat. 1999, 194, 323-334 10.1046/j.1469-7580.1999.19430323.x
3. Dela, F.; Kjaer, M. Resistance training, insulin sensitivity and muscle function in the elderly Essays Biochem. 2006, 42, 75-88 10.1042/bse0420075
4. Perrini, S.; Laviola, L.; Carreira, M. C.; Cignarelli, A.; Natalicchio, A.; Giorgino, F. The GH/IGF1 axis and signaling pathways in the muscle and bone: mechanisms underlying age-related skeletal muscle wasting and osteoporosis J. Endocrinol. 2010, 205, 201-210 10.1677/JOE-09-0431
5. Mourkioti, F.; Rosenthal, N. IGF-1, inflammation and stem cells: interactions during muscle regeneration Trends Immunol. 2005, 26, 535-542 10.1016/j.it.2005.08.002
6. Rommel, C.; Bodine, S. C.; Clarke, B. A.; Rossman, R.; Nunez, L.; Stitt, T. N.; Yancopoulos, G. D.; Glass, D. J. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways Nat. Cell Biol. 2001, 3, 1009-1013 10.1038/ncb1101-1009
7. Solomon, A. M.; Bouloux, P. M. G. Modifying muscle mass-the endocrine perspective J. Endocrinol. 2006, 191, 349-360 10.1677/joe.1.06837
8. Vinciguerra, M.; Musaro, A.; Rosenthal, N. Regulation of muscle atrophy in aging and disease. In Protein Metabolism and Homeostasis in Aging; Advances in Experimental Medicine and Biology; Springer: New York, 2010; Vol. 694, pp 211-233.
9. Guler, H. P.; Zapf, J.; Schmid, C.; Froesch, E. R. Insulin-like growth factors I and II in healthy man. Estimations of half-lives and production rates Acta Endocrinol. 1989, 121, 753-758 10.1530/acta.0.1210753
10. Frystyk, J. Free insulin-like growth factors - measurements and relationships to growth hormone secretion and glucose homeostasis Growth Horm IGF Res. 2004, 14, 337-375 10.1016/j.ghir.2004.06.001
11. Denley, A.; Cosgrove, L. J.; Booker, G. W.; Wallace, J. C.; Forbes, B. E. Molecular interactions of the IGF system Cytokine Growth Factor Rev. 2005, 16, 421-439 10.1016/j.cytogfr.2005.04.004
12. Patton, J. S.; Byron, P. R. Inhaling medicines: delivering drugs to the body through the lungs Nat. Rev. Drug Discovery 2007, 6, 67-74 10.1038/nrd2153
13. Santos Cavaiola, T.; Edelman, S. Inhaled Insulin: A Breath of Fresh Air? A Review of Inhaled Insulin Clin. Ther. 2014, 36, 1275-1289 10.1016/j.clinthera.2014.06.025
14. Patton, J. S. Mechanisms of macromolecule absorption by the lungs Adv. Drug Delivery Rev. 1996, 19, 3-36 10.1016/0169-409X(95)00113-L
15. Clemmons, D. R. Insulin-like growth factors-their binding proteins and growth regulation. In Skeletal Growth Factors; Canalis, E., Ed.; Lippincott Williams & Wilkins: Philadelphia, 2000.
16. Clark, R. G. Recombinant human insulin-like growth factor I (IGF-I): risks and benefits of normalizing blood IGF-I concentrations Horm. Res. 2005, 62, 93-100 10.1159/000080766
17. Exubera: EPAR-All Authorized Presentations; European Medicines Agency, London, 2008.
18. Exubera: EPAR-Scientific Discussion; European Medicines Agency: London, 2008.
19. Luginbuehl, V.; Zoidis, E.; Meinel, L.; von, R. B.; Gander, B.; Merkle, H. P. Impact of IGF-I release kinetics on bone healing: A preliminary study in sheep Eur. J. Pharm. Biopharm. 2013, 85, 99-106 10.1016/j.ejpb.2013.03.004
20. Luginbuehl, V.; Wenk, E.; Koch, A.; Gander, B.; Merkle, H. P.; Meinel, L. Insulin-like Growth Factor I-Releasing Alginate-Tricalciumphosphate Composites for Bone Regeneration Pharm. Res. 2005, 22, 940-950 10.1007/s11095-005-4589-9
21. Luginbuehl, V.; Meinel, L.; Merkle, H. P.; Gander, B. Localized delivery of growth factors for bone repair Eur. J. Pharm. Biopharm. 2004, 58, 197-208 10.1016/j.ejpb.2004.03.004
22. Meinel, L.; Zoidis, E.; Zapf, J.; Hassa, P.; Hottiger, M. O.; Auer, J. A.; Schneider, R.; Gander, B.; Luginbuehl, V.; Bettschart-Wolfisberger, R.; Illi, O. E.; Merkle, H. P.; von, R. B. Localized insulin-like growth factor I delivery to enhance new bone formation Bone 2003, 33, 660-672 10.1016/S8756-3282(03)00207-2
23. Meinel, L.; Illi, O. E.; Zapf, J.; Malfanti, M.; Peter, M. H.; Gander, B. Stabilizing insulin-like growth factor-I in poly(d,l-lactide-co-glycolide) microspheres J. Controlled Release 2001, 70, 193-202 10.1016/S0168-3659(00)00352-7
24. Guziewicz, N. A.; Massetti, A. J.; Perez-Ramirez, B. J.; Kaplan, D. L. Mechanisms of monoclonal antibody stabilization and release from silk biomaterials Biomaterials 2013, 34, 7766-7775 10.1016/j.biomaterials.2013.06.039
25. Wenk, E.; Merkle, H. P.; Meinel, L. Silk fibroin as a vehicle for drug delivery applications J. Controlled Release 2011, 150, 128-141 10.1016/j.jconrel.2010.11.007
26. Meinel, L.; Hofmann, S.; Karageorgiou, V.; Zichner, L.; Langer, R.; Kaplan, D.; Vunjak-Novakovic, G. Engineering cartilage-like tissue using human mesenchymal stem cells and silk protein scaffolds Biotechnol. Bioeng. 2004, 88, 379-391 10.1002/bit.20252
27. Edelhoch, H. Spectroscopic determination of tryptophan and tyrosine in proteins Biochemistry 1967, 6, 1948-1954 10.1021/bi00859a010
28. Uebersax, L.; Apfel, T.; Nuss, K. M. R.; Vogt, R.; Kim, H. Y.; Meinel, L.; Kaplan, D. L.; Auer, J. A.; Merkle, H. P.; von, R. B. Biocompatibility and osteoconduction of macroporous silk fibroin implants in cortical defects in sheep Eur. J. Pharm. Biopharm. 2013, 85, 107-118 10.1016/j.ejpb.2013.05.008
29. Meinel, L.; Kaplan, D. L. Silk constructs for delivery of musculoskeletal therapeutics Adv. Drug Delivery Rev. 2012, 64, 1111-1122 10.1016/j.addr.2012.03.016
30. Wang, X.; Wenk, E.; Zhang, X.; Meinel, L.; Vunjak, G.; Kaplan, D. L. Growth factor gradients via microsphere delivery in biopolymer scaffolds for osteochondral tissue engineering J. Controlled Release 2010, 134, 81-90 10.1016/j.jconrel.2008.10.021
31. Uebersax, L.; Merkle, H. P.; Meinel, L. Insulin-like growth factor I releasing silk fibroin scaffolds induce chondrogenic differentiation of human mesenchymal stem cells J. Controlled Release 2008, 127, 12-21 10.1016/j.jconrel.2007.11.006
32. Fransson, J. R. Oxidation of human insulin-like growth factor I in formulation studies. 3. Factorial experiments of the effects of ferric ions, EDTA, and visible light on methionine oxidation and covalent aggregation in aqueous solution J. Pharmaceutical Sci. 1997, 86, 1046-1050 10.1021/js960484q
33. LAEMMLI, U. K. Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 Nature 1970, 227, 680-685 10.1038/227680a0
34. McLellan, T. Electrophoresis buffers for polyacrylamide gels at various pH Anal. Biochem. 1982, 126, 94-99 10.1016/0003-2697(82)90113-0
35. Wenk, E.; Wandrey, A. J.; Merkle, H. P.; Meinel, L. Silk fibroin spheres as a platform for controlled drug delivery J. Controlled Release 2008, 132, 26-34 10.1016/j.jconrel.2008.08.005
36. Ehrhardt, C.; Fiegel, J.; Fuchs, S.; Abu-Dahab, R.; Schaefer, U. F.; Hanes, J.; Lehr, C.-M. Drug absorption by the respiratory mucosa: cell culture models and particulate drug carriers J. Aerosol Med. 2002, 15, 131-139 10.1089/089426802320282257
37. Vllasaliu, D.; Fowler, R.; Garnett, M.; Eaton, M.; Stolnik, S. Barrier characteristics of epithelial cultures modelling the airway and intestinal mucosa: a comparison Biochem. Biophys. Res. Commun. 2011, 415, 579-585 10.1016/j.bbrc.2011.10.108
38. Bahhady, R.; Kim, K.-J.; Borok, Z.; Crandall, E. D.; Shen, W.-C. Characterization of protein factor(s) in rat bronchoalveolar lavage fluid that enhance insulin transport via transcytosis across primary rat alveolar epithelial cell monolayers Eur. J. Pharm. Biopharm. 2008, 69, 808-816 10.1016/j.ejpb.2008.01.028
39. Gnadt, M.; Trammer, B.; Kardziev, B.; Bayliss, M. K.; Edwards, C. D.; Schmidt, M.; Hoegger, P. Comparison of the bronchodilating effects of inhaled β2-agonists after methacholine challenge in a human lung reperfusion model Eur. J. Pharm. Biopharm. 2012, 81, 617-626 10.1016/j.ejpb.2012.04.013
40. Gnadt, M.; Trammer, B.; Freiwald, M.; Kardziev, B.; Bayliss, M. K.; Edwards, C. D.; Schmidt, M.; Friedel, G.; Hoegger, P. Methacholine delays pulmonary absorption of inhaled β2-agonists due to competition for organic cation/carnitine transporters Pulm. Pharmacol. Ther. 2012, 25, 124-134 10.1016/j.pupt.2011.12.009
41. Freiwald, M.; Valotis, A.; Kirschbaum, A.; McClellan, M.; Murdter, T.; Fritz, P.; Friedel, G.; Thomas, M.; Hogger, P. Monitoring the initial pulmonary absorption of two different beclomethasone dipropionate aerosols employing a human lung reperfusion model Respir Res. 2005, 6, 21 10.1186/1465-9921-6-21
42. Mathias, N. R.; Timoszyk, J.; Stetsko, P. I.; Megill, J. R.; Smith, R. L.; Wall, D. A. Permeability characteristics of Calu-3 human bronchial epithelial cells: in vitro-in vivo correlation to predict lung absorption in rats J. Drug Targeting 2002, 10, 31-40 10.1080/10611860290007504
43. Florea, B. I.; Cassara, M. L.; Junginger, H. E.; Borchard, G. Drug transport and metabolism characteristics of the human airway epithelial cell line Calu-3 J. Controlled Release 2003, 87, 131-138 10.1016/S0168-3659(02)00356-5
44. Breitfeld, P. P.; McKinnon, W. C.; Mostov, K. E. Effect of nocodazole on vesicular traffic to the apical and basolateral surfaces of polarized MDCK cells J. Cell Biol. 1990, 111, 2365-2373 10.1083/jcb.111.6.2365
45. Hastings, R. H.; Folkesson, H. G.; Matthav, M. A. Mechanisms of alveolar protein clearance in the intact lung Am. J. Physiol. 2004, 286, L679-L689
46. Oda, K.; Yumoto, R.; Nagai, J.; Katayama, H.; Takano, M. Mechanism underlying insulin uptake in alveolar epithelial cell line RLE-6TN Eur. J. Pharmacol. 2011, 672, 62-69 10.1016/j.ejphar.2011.10.003
47. Kirchhausen, T.; Macia, E.; Pelish, H. E. Use of dynasore, the small molecule inhibitor of dynamin, in the regulation of endocytosis Methods Enzymol. 2008, 438, 77-91 10.1016/S0076-6879(07)38006-3
48. Macia, E.; Ehrlich, M.; Massol, R.; Boucrot, E.; Brunner, C.; Kirchhausen, T. Dynasore, a cell-permeable inhibitor of dynamin Dev. Cell 2006, 10, 839-850 10.1016/j.devcel.2006.04.002
49. Lu, Q.; Hu, X.; Wang, X.; Kluge, J. A.; Lu, S.; Cebe, P.; Kaplan, D. L. Water-insoluble silk films with silk I structure Acta Biomater. 2010, 6, 1380-1387 10.1016/j.actbio.2009.10.041
50. Sohn, S.; Strey, H. H.; Gido, S. P. Phase Behavior and Hydration of Silk Fibroin Biomacromolecules 2004, 5, 751-757 10.1021/bm0343693
51. Li, M.; Ogiso, M.; Minoura, N. Enzymatic degradation behavior of porous silk fibroin sheets Biomaterials 2003, 24, 357-365 10.1016/S0142-9612(02)00326-5
52. Marsh, R. E.; Corey, R. B.; Pauling, L. An investigation of the structure of silk fibroin Biochim. Biophys. Acta 1955, 16, 1-34 10.1016/0006-3002(55)90178-5
53. Teramoto, H.; Miyazawa, M. Molecular Orientation Behavior of Silk Sericin Film as Revealed by ATR Infrared Spectroscopy Biomacromolecules 2005, 6, 2049-2057 10.1021/bm0500547
54. Hu, X.; Kaplan, D.; Cebe, P. Determining Beta-Sheet Crystallinity in Fibrous Proteins by Thermal Analysis and Infrared Spectroscopy Macromolecules 2006, 39, 6161-6170 10.1021/ma0610109
55. Goormaghtigh, E.; Cabiaux, V.; Ruysschaert, J. M. Secondary structure and dosage of soluble and membrane proteins by attenuated total reflection Fourier-transform infrared spectroscopy on hydrated films Eur. J. Biochem. 1990, 193, 409-420 10.1111/j.1432-1033.1990.tb19354.x
56. Chen, X.; Knight, D. P.; Shao, Z.; Vollrath, F. Regenerated Bombyx silk solutions studied with rheometry and FTIR Polymer 2001, 42, 09969-09974 10.1016/S0032-3861(01)00541-9
57. Ha, S.-W.; Tonelli, A. E.; Hudson, S. M. Structural Studies of Bombyx mori Silk Fibroin during Regeneration from Solutions and Wet Fiber Spinning Biomacromolecules 2005, 6, 1722-1731 10.1021/bm050010y
58. Zhao, H.; Heusler, E.; Jones, G.; Werner, V.; Germershaus, O.; Ritzer, J.; Luehmann, T.; Li, L.; Meinel, L. Decoration of silk fibroin by click chemistry for biomedical application J. Struct Biol. 2014, 186, 420-430 10.1016/j.jsb.2014.02.009
59. Germershaus, O.; Schultz, I.; Luhmann, T.; Beck-Broichsitter, M.; Hogger, P.; Meinel, L. Insulin-like growth factor-I aerosol formulations for pulmonary delivery Eur. J. Pharm. Biopharm. 2013, 85, 61-68 10.1016/j.ejpb.2013.03.011
60. Grainger, C. I.; Greenwell, L. L.; Lockley, D. J.; Martin, G. P.; Forbes, B. Culture of Calu-3 Cells at the Air Interface Provides a Representative Model of the Airway Epithelial Barrier Pharm. Res. 2006, 23, 1482-1490 10.1007/s11095-006-0255-0
61. Lindahl, M.; Stahlbom, B.; Svartz, J.; Tagesson, C. Protein patterns of human nasal and bronchoalveolar lavage fluids analyzed with two-dimensional gel electrophoresis Electrophoresis 1998, 19, 3222-3229 10.1002/elps.1150191828
62. Rehman, A. A.; Ahsan, H.; Khan, F. H. Alpha-2-macroglobulin: A physiological guardian J. Cell. Physiol. 2013, 228, 1665-1675 10.1002/jcp.24266
63. Westwood, M.; Aplin, J. D.; Collinge, I. A.; Gill, A.; White, A.; Gibson, J. M. α2-Macroglobulin: a new component in the insulin-like growth factor/insulin-like growth factor binding protein-1 axis J. Biol. Chem. 2001, 276, 41668-41674 10.1074/jbc.M102793200
64. Ikehata, M.; Yumoto, R.; Kato, Y.; Nagai, J.; Takano, M. Mechanism of insulin uptake in rat alveolar type II and type I-like epithelial cells Biol. Pharm. Bull. 2009, 32, 1765-1769 10.1248/bpb.32.1765
65. Pezron, I.; Mitra, R.; Pal, D.; Mitra, A. K. Insulin aggregation and asymmetric transport across human bronchial epithelial cell monolayers (Calu-3) J. Pharm. Sci. 2002, 91, 1135-1146 10.1002/jps.10114
66. Cheng, Q.; Peng, T.-Z.; Hu, X.-B.; Yang, C. F. Charge-selective recognition at fibroin-modified electrodes for analytical application Anal. Bioanal. Chem. 2005, 382, 80-84 10.1007/s00216-005-3150-3
67. Germershaus, O.; Werner, V.; Kutscher, M.; Meinel, L. Deciphering the mechanism of protein interaction with silk fibroin for drug delivery systems Biomaterials 2014, 35, 3427-3434 10.1016/j.biomaterials.2013.12.083
68. Hino, T.; Tanimoto, M.; Shimabayashi, S. Change in secondary structure of silk fibroin during preparation of its microspheres by spray-drying and exposure to humid atmosphere J. Colloid Interface Sci. 2003, 266, 68-73 10.1016/S0021-9797(03)00584-8
69. Samal, S. K.; Kaplan, D. L.; Chiellini, E. Ultrasound Sonication Effects on Silk Fibroin Protein Macromol. Mater. Eng. 2013, 298, 1201-1208 10.1002/mame.201200377
70. Bonner, J. C. Lung fibrotic responses to particle exposure Toxicol. Pathol. 2007, 35, 148-153 10.1080/01926230601060009
71. Lammel, A. S.; Hu, X.; Park, S.-H.; Kaplan, D. L.; Scheibel, T. R. Controlling silk fibroin particle features for drug delivery Biomaterials 2010, 31, 4583-4591 10.1016/j.biomaterials.2010.02.024
72. Meinel, L.; Hofmann, S.; Karageorgiou, V.; Kirker-Head, C.; McCool, J.; Gronowicz, G.; Zichner, L.; Langer, R.; Vunjak-Novakovic, G.; Kaplan, D. L. The inflammatory responses to silk films in vitro and in vivo Biomaterials 2005, 26, 147-155 10.1016/j.biomaterials.2004.02.047