Structure and dynamics of spin-labeled insulin entrapped in a silica matrix by the sol-gel method

Biomacromolecules

Volumn 14, Issue 8, 2013, Pages 2582-2592

  Vanea, E ^a   Gruian, C ^a   Rickert, C ^b   Steinhoff, H J ^b   Simon, V ^a  

^a BABE BOLYAI UNIVERSITY   (Romania)

^b UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONAL DYNAMICS; CONTINUOUS WAVES; DOUBLE ELECTRON-ELECTRON RESONANCE; ELECTRON PARAMAGNETIC RESONANCE SPECTROSCOPY; INSULIN MOLECULES; POROUS OXIDE MATRIX; SECONDARY STRUCTURES; STRUCTURE AND DYNAMICS;

CONFORMATIONS; FOURIER TRANSFORM INFRARED SPECTROSCOPY; INSULIN; MAGNETIC RESONANCE; PARAMAGNETISM; SILICA; SOL-GEL PROCESS; SOLS; SPIN DYNAMICS;

ELECTRON SPIN RESONANCE SPECTROSCOPY;

INSULIN; IODOACETAMIDE; NITROXIDE; SILICON DIOXIDE; ANTIDIABETIC AGENT; DRUG CARRIER; NANOPARTICLE; SILICA GEL; SPIN LABELING;

ARTICLE; DOUBLE ELECTRON ELECTRON RESONANCE; DRUG CONFORMATION; DRUG RELEASE; DRUG STRUCTURE; ELECTRON SPIN RESONANCE; ENCAPSULATION; INFRARED SPECTROSCOPY; LOW TEMPERATURE PROCEDURES; NONHUMAN; POROSITY; PRIORITY JOURNAL; PROCEDURES; ROOM TEMPERATURE; SOL GEL METHOD; SPIN LABELING; ANIMAL; BOVINAE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG FORMULATION; HUMAN; PARTICLE SIZE; PHASE TRANSITION; PROTEIN SECONDARY STRUCTURE;

ANIMALS; CATTLE; DRUG CARRIERS; DRUG COMPOUNDING; ELECTRON SPIN RESONANCE SPECTROSCOPY; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; MODELS, MOLECULAR; NANOPARTICLES; PARTICLE SIZE; PHASE TRANSITION; POROSITY; PROTEIN STRUCTURE, SECONDARY; SILICA GEL; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SPIN LABELS;

EID: 84881562821     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/bm4003893     Document Type: Article

References (55)

1. Silva, C. M.; Ribeiro, A. J.; Ferreira, D.; Veiga, F. Insulin encapsulation in reinforced alginate microspheres prepared by internal gelation Eur. J. Pharm. Sci. 2006, 29, 148-159
2. Cui, F.; Shi, K.; Zhang, L.; Tao, A.; Kawashima, Y. Biodegradable nanoparticles loaded with insulin-phospholipid complex for oral delivery: Preparation, in vitro characterization and in vivo evaluation J. Controlled Release 2006, 114, 242-250
3. Jin, W.; Brennan, J. D. Properties and applications of proteins encapsulated within sol-gel derived materials Anal. Chim. Acta 2002, 461, 1-36
4. Shivanand, P. Silica particles as a tool for controlled release of drugs and biologicals Arch. Appl. Sci. Res. 2010, 2, 19-22
5. McCool, B. A.; Cashon, R.; Karles, G.; DeSisto, W. J. Silica encapsulated hemoglobin and myoglobin powders prepared by an aqueous fast-freezing technique J. Non-Cryst. Solids 2004, 333, 143-149
6. Macmillan, A. M.; Panek, D.; McGuinness, C. D.; Pickup, J. C.; Graham, D.; Smith, W. E.; Birch, D. J. S.; Karolin, J. Improved biocompatibility of protein encapsulation in sol-gel materials J. Sol-Gel Sci. Technol. 2009, 49, 380-384
7. Brems, D. N.; Brown, P. L.; Heckenlaible, L. A.; Frank, B. H. Equilibrium denaturation of insulin and proinsulin Biochemistry 1990, 29, 9289-9293
8. Livage, J.; Coradin, T. Encapsulation of enzymes, antibodies and bacteria. In Sol-Gel Science and Technology-Processing Characterization and Applications; Sakka, S., Ed.; Kluwer Academic Publishers: New York, 2005; pp 486-503.
9. Zako, T.; Sakono, M.; Hashimoto, N.; Ihara, M.; Maeda, M. Bovine insulin filaments induced by reducing disulfide bonds show a different morphology, secondary structure, and cell toxicity from intact insulin amyloid fibrils Biophys. J. 2009, 96, 3331-3340
10. Hinds, K. D.; Kim, S. W. Effects of PEG conjugation on insulin properties Adv. Drug Deliver Rev. 2002, 54, 505-530
11. Falconi, M.; Cambria, M. T.; Cambria, A.; Desideri, A. Structure and stability of the insulin dimer investigated by molecular dynamics simulation J. Biomol. Struct. Dyn. 2001, 18, 761-772
12. Grodsky, G. M.; Forsham, P. H. Insulin and the pancreas Annu. Rev. Physiol. 1966, 28, 347-380
13. Severcana, M.; Severcanb, F.; Haris, P. I. Estimation of protein secondary structure from FTIR spectra using neural networks J. Mol. Struct. 2001, 565-566, 383-387
14. Kandimalla, V. B.; Tripathi, V. S.; Ju, H. Immobilization of biomolecules in sol-gels: Biological and analytical applications Crit. Rev. Anal. Chem. 2006, 36, 73-106
15. Hubbell, W. L.; Cafiso, D. S.; Altenbach, C. Identifying conformational changes with site-directed spin labeling Nat. Struct. Biol. 2000, 7, 735-739
16. Klare, J. P.; Steinhoff, H.-J. Spin labeling EPR Photosynth. Res. 2009, 102, 377-390
17. Bordignon, E.; Steinhoff, H.-J. Membrane protein structure and dynamics studied by side-directed spin labeling ESR. In ESR Spectroscopy in Membrane Biophysics; Hemminga, M. A.; Berliner, L. J., Eds.; Springer Science and Business Media: New York, 2007.
18. Farahbakhsh, Z. T.; Huang, Q. L.; Ding, L. L.; Altenbach, C.; Steinhoff, H.-J.; Horwitz, J.; Hubbell, W. L. Interaction of α-Crystallin with spin-labeled peptides Biochemistry 1995, 34, 509-516
19. Steinhoff, H.-J.; Radzwill, N.; Thevis, W.; Lenz, V.; Brandenburg, D.; Antson, A.; Dodson, G.; Wollmeri, A. Determination of interspin distances between spin labels attached to insulin: Comparison of electron paramagnetic resonance data with the X-ray structure Biophys. J. 1997, 73, 3287-3298
20. Gruian, C.; Vulpoi, A.; Steinhoff, H.-J.; Simon, S. Structural changes of methemoglobin after adsorption on bioactive glass, as a function of surface functionalization and salt concentration J. Mol. Struct. 2012, 1015, 20-26
21. Vulpoi, A.; Gruian, C.; Vanea, E.; Baia, L.; Simon, S.; Steinhoff, H.-J.; Göller, G.; Simon, V. Bioactivity and protein attachment onto bioactive glasses containing silver nanoparticles J. Biomed. Mater. Res. A 2012, 100, 1179-1186
22. Jacobsen, K.; Hubbell, W. L.; Ernst, O. P.; Risse, T. Details of the partial unfolding of T4 lysozyme on quartz using site-directed spin labeling Angew. Chem., Int. Ed. 2006, 45, 3874-3877
23. Besheer, A.; Wood, K. M.; Peppas, N. A.; Mader, K. Loading and mobility of spin-labeled insulin in physiologically responsive complexation hydrogels intended for oral administration J. Controlled Release 2006, 111, 73-80
24. Fleissner, M. R.; Bridges, M. D.; Brooks, E. K.; Cascio, D.; Kalai, T.; Hideg, K.; Hubbell, W. L. Structure and dynamics of a conformationally constrained nitroxide side chain and applications in EPR spectroscopy Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 16241-16246
25. Jeschke, G.; Polyhach, Y. Distance measurements on spin-labeled biomacromolecules by pulsed electron paramagnetic resonance Phys. Chem. Chem. Phys. 2007, 9, 1895-1910
26. Steinhoff, H.-J. A simple method for determination of rotational correlation times and separation of rotational and polarity effects from EPR spectra of spin-labeled biomolecules in a wide correlation time range J. Biochem. Biophys. Methods 1988, 17, 237-248
27. Brutlach, H.; Bordignon, E.; Urban, L.; Klare, J. P.; Reyer, H.-J.; Engelhard, M.; Steinhoff, H.-J. Heterogeneity in the nitroxide micro-environment: Polarity and proticity effects in spin-labeled proteins studied by multi-frequency Appl. Magn. Reson. 2006, 30, 359-372
28. Plato, M.; Steinhoff, H.-J.; Wegener, C.; Torring, J. T.; Savitsky, A.; Mobius, K. Molecular orbital study of polarity and hydrogen bonding effects on the g and hyperfine tensors of site directed NO spin labeled bacteriorhodopsin Mol. Phys. 2002, 100, 3711-3721
29. Jeschke, G.; Chechik, V.; Ionita, P.; Godt, A.; Zimmermann, H.; Banham, J.; Timmel, C. R.; Hilger, D.; Jung, H. DeerAnalysis2006-A comprehensive software package for analyzing pulsed ELDOR data Appl. Magn. Reson. 2006, 30, 473-498
30. Klose, D.; Klare, J. P.; Grohmann, D.; Kay, C. W. M.; Werner, F.; Steinhoff, H.-J. Simulation vs. Reality: A comparison of in silico distance predictions with DEER and FRET measurements PLoS One 2012, 7, e39492
31. Smith, G. D.; Pangborn, W. A.; Blessing, R. H. The structure of T6 bovine insulin Acta Crystallogr. D 2005, 61, 1476-1482
32. Polyhach, Y.; Bordignon, E.; Jeschke, G. Rotamer libraries of spin labeled cysteines for protein studies Phys. Chem. Chem. Phys. 2011, 13, 2356-2366
33. Pettersen, E. F.; Goddard, T. D.; Huang, C. C.; Couch, G. S.; Greenblatt, D. M.; Meng, E. C.; Ferrin, T. E. UCSF Chimera-A visualization system for exploratory research and analysis J. Comput. Chem. 2004, 25 (13) 1605-1612
34. Brunauer, S.; Emmett, P. H.; Teller, E. Adsorption of gases in multimolecular layers J. Am. Chem. Soc. 1938, 60, 309-319
35. Dong, A.; Prestrelski, S. J.; Allison, S. D.; Carpenter, J. F. Infrared spectroscopic studies of lyophilization- and temperature-induced protein aggregation J. Pharm. Sci. 1995, 84, 415-424
36. Kong, J.; Yu, S. Fourier transform infrared spectroscopic analysis of protein secondary structures Acta Biochim. Biophys. Sin. 2007, 39, 549-559
37. Sideratou, Z.; Sterioti, N.; Tsiourvas, D.; Tziveleka, L. A.; Thanassoulas, A.; Nounesis, G.; Paleo, C. M. Arginine end-functionalized poly(l -lysine) dendrigrafts for the stabilization and controlled release of insulin J. Colloid Interface Sci. 2010, 351, 433-441
38. Stoll, S.; Lee, Y.-T.; Zhang, M.; Wilson, R. F.; Britt, R. D.; Goodin, D. B. Double electron-electron resonance shows cytochrome P450cam undergoes a conformational change in solution upon binding substrate Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 12888-12893
39. Steinhoff, H.-J. Methods for study of protein dynamics and protein-protein interaction in protein-ubiquitination by electron paramagnetic resonance spectroscopy Front. Biosci. 2002, 7, c97-110
40. Hubbel, W. L.; Altenbach, C. Investigation of structure and dynamics in membrane proteins using site directed spin labeling Curr. Opin. Struc. Biol. 1994, 4, 566-573
41. Jiang, G.; Woo, B.; Kang, F.; Singh, J.; DeLuca, P. Assessment of protein release kinetics, stability and protein polymer interaction of lysozyme encapsulated poly(d, l -lactide- co -glycolide) microspheres J. Controlled Release 2002, 79, 137-145
42. Crotts, G.; Park, T. G. Stability and release of bovine serum albumin encapsulated within poly(d, l -lactide- co -glycolide) microparticles J. Controlled Release 1997, 44, 123-134
43. Steinhoff, H.-J.; Dombrowsky, O.; Karim, C.; Schneiderhahn, C. Two dimensional diffusion of small molecules on protein surfaces: An EPR study of the restricted translational diffusion of protein-bound spin labels Eur. Biophys. J. 1991, 20, 293-303
44. Kokorin, A. I.; Zamaraev, K. I.; Grigorian, G. L.; Ivanov, V. P.; Rozantsev, E. G. Measurement of the distance between paramagnetic centres in solid solutions of nitrosyl radicals, biradicals and spin-labeled proteins Biofizika 1972, 17, 34-41
45. Sun, J.; Voss, J.; Hubbell, W. L.; Kaback, H. R. Proximity between periplasmic loops in the lactose permease of Escherichia coli as determined by site-directed spin labeling Biochemistry 1999, 38, 3100-3105
46. Bhatia, R. B.; Brinker, C. J. Aqueous sol-gel process for protein encapsulation Chem. Mater. 2000, 12, 2434-2441
47. Gruian, C.; Vanea, E.; Simon, S.; Simon, V. FTIR and XPS studies of protein adsorption onto functionalized bioactive glass Biochim. Biophys. Acta, Proteins Proteomics 2012, 1824, 873-881
48. Vanea, E.; Tamasan, M.; Albon, C.; Simon, V. Synthesis and characterization of a new composite aluminosilicate bioceramic J. Non-Cryst. Solids 2011, 357, 3791-3796
49. Vanea, E.; Simon, V. XPS study of protein adsorption onto nanocrystalline aluminosilicate microparticles Appl. Surf. Sci. 2011, 257, 2346-2352
50. Griebenow, K.; Klibanov, A. M. On protein denaturation in aqueous-organic mixtures but not in pure organic solvents J. Am. Chem. Soc. 1996, 118, 11695-11700
51. Han, Y.; Tian, H.; He, P.; Chen, X.; Jing, X. Insulin nanoparticle preparation and encapsulation into poly(lactic- co -glycolic acid) microspheres by using an anhydrous system Int. J. Pharm. 2009, 378, 159-166
52. Natalello, A.; Ami, D.; Brocca, S.; Lotti, M.; Doglia, S. M. Secondary structure, conformational stability and glycosylation of a recombinant Candida rugosa lipase studied by Fourier-transform infrared spectroscopy Biochem. J. 2005, 385, 511-517
53. Pikal, M. J.; Rigsbee, D. R. The stability of insulin in crystalline and amorphous solids: Observation of greater stability for the amorphous form Pharm. Res. 1997, 14, 1379-1387
54. Sarmento, B.; Ferreira, D. C.; Jorgensen, L.; van de Weert, M. Probing insulin's secondary structure after entrapment into alginate/chitosan nanoparticles Eur. J. Pharm. Biopharm. 2007, 65, 10-17
55. Witold, K. S.; Henry, H. M. Infrared absorption methods for examining protein structure. In Spectroscopic Methods For Determining Protein Structure in Solution; Havel, H. A., Ed.; VCH Publishers, Inc.: New York, 1996; pp 135-150.