Influence of Silica Matrix Composition and Functional Component Additives on the Bioactivity and Viability of Encapsulated Living Cells

ACS Biomaterials Science and Engineering

Volumn 1, Issue 12, 2015, Pages 1231-1238

  Savage, Travis J ^a   Dunphy, Darren R ^a   Harbaugh, Svetlana ^b   Kelley Loughnane, Nancy ^b   Harper, Jason C ^c   Brinker, C Jeffrey ^a,c  

^a MSC01 1070   (United States)

^b AIR FORCE RESEARCH LABORATORY   (United States)

^c SANDIA NATIONAL LABORATORIES   (United States)

Author keywords

bioactivity; cell encapsulation; cell viability; glycerol modified silanes; living hybrid biomaterials; whole cell based biosensors

Indexed keywords

ALKOXYSILANE; AQUEOUS SILICATE; GLYCEROL; MONOMER; NANOMATERIAL; NUCLEIC ACID; PROPIDIUM IODIDE; SILICA GEL; SILICON DIOXIDE; SODIUM; TETRAETHOXYSILANE; THEOPHYLLINE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BIOLOGICAL ACTIVITY; BIOSENSOR; CELL ENCAPSULATION; CELL VIABILITY; CULTURE MEDIUM; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; NONHUMAN; PARTICLE SIZE; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RIBOSWITCH;

EID: 84969132819     PISSN: None     EISSN: 23739878     Source Type: Journal    
DOI: 10.1021/acsbiomaterials.5b00261     Document Type: Article

References (50)

1. Ruiz-Hitzky, E.; Darder, M.; Aranda, P.; Ariga, K. Advances in Biomimetic and Nanostructured Biohybrid Materials Adv. Mater. 2010, 22, 323-336 10.1002/adma.200901134
2. Wang, S.; Guo, Z. Bio-Inspired Encapsulation and Functionalization of Living Cells with Artificial Shells Colloids Surf., B 2014, 113, 483-500 10.1016/j.colsurfb.2013.09.024
3. Ben-Yoav, H.; Melamed, S.; Freeman, A.; Shacham-Diamond, Y.; Belkin, S. Whole-Cell Biochips for Bio-Sensing: Integration of Live Cells and Inanimate Surfaces Crit. Rev. Biotechnol. 2011, 31, 337-353 10.3109/07388551.2010.532767
4. Nassif, N.; Livage, J. From Diatoms to Silica-Based Biohybrids Chem. Soc. Rev. 2011, 40, 849-859 10.1039/C0CS00122H
5. Leonard, A.; Dandoy, P.; Danloy, E.; Leroux, G.; Meunier, C. F.; Rooke, J. C.; Su, B.-L. Whole-Cell Based Hybrid Materials for Green Energy Production, Environmental Remediation and Smart Cell-Therapy Chem. Soc. Rev. 2011, 40, 860-885 10.1039/c0cs00024h
6. Meunier, C. F.; Rooke, J. C.; Leonard, A.; Xie, H.; Su, B. L. Living Hybrid Materials Capable of Energy Conversion and CO2 Assimilation Chem. Commun. 2010, 46, 3843-3859 10.1039/c001799j
7. Carnes, E. C.; Lopez, D. M.; Donegan, N. P.; Cheung, A.; Gresham, H.; Timmins, G. S.; Brinker, C. J. Confinement-Induced Quorum Sensing of Individual Staphylococcus aureus Bacteria Nat. Chem. Biol. 2010, 6, 41-45 10.1038/nchembio.264
8. Carballeria, J. D.; Quezada, M. A.; Hoyos, P.; Simeó, Y.; Hernaiz, M. J.; Alcantara, A. R.; Sinisterra, J. V. Microbial Cells As Catalysts for Stereoselective Red-Ox Reactions Biotechnol. Adv. 2009, 27, 686-714 10.1016/j.biotechadv.2009.05.001
9. Coradin, T.; Boissiére, M.; Livage, J. Sol-Gel Chemistry in Medicinal Science Curr. Med. Chem. 2006, 13, 99-108 10.2174/092986706789803044
10. 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 10.1080/10408340600713652
11. Yap, F. L.; Zhang, Y. Proteins and Cell Micropatterning and its Integration with Micro/Nanoparticles Assembly Biosens. Bioelectron. 2007, 22, 775-788 10.1016/j.bios.2006.03.016
12. Gupta, R.; Chaudhury, N. K. Entrapment of Biomolecules in Sol-Gel Matrix for Applications in Biosensors: Problems and Future Prospects Biosens. Bioelectron. 2007, 22, 2387-2399 10.1016/j.bios.2006.12.025
13. Gill, I. Bio-Doped Nanocomposite Polymers: Sol-Gel Bioencapsulates Chem. Mater. 2001, 13, 3404-3421 10.1021/cm0102483
14. Gill, I.; Ballesteros, A. Bioencapsulation within Synthetic Polymers (Part 1): Sol-Gel Encapsulated Biologicals Trends Biotechnol. 2000, 18, 282-296 10.1016/S0167-7799(00)01457-8
15. Yamanaka, S.; Nishida, F.; Ellerby, L. M.; Nishida, C. R.; Dunn, B.; Valentine, J. S.; Zink, J. I. Enzymatic-Activity of Glucose-Oxidase Encapsulated in Transparent Glass by the Sol-Gel Method Chem. Mater. 1992, 4, 495-497 10.1021/cm00021a001
16. Ispas, C.; Sokolov, I.; Andreescu, S. Enzyme-Functionalized Mesoporous Silica for Bioanalytical Applications Anal. Bioanal. Chem. 2009, 393, 543-554 10.1007/s00216-008-2250-2
17. Brennan, J. D. Biofriendly Sol-Gel Processing for the Entrapment of Soluble and Membrane-Bound Proteins: Toward Novel Solid-Phase Assays for High-Throughput Screening Acc. Chem. Res. 2007, 40, 827-835 10.1021/ar6000268
18. Jin, W.; Brennan, J. D. Properties and Applications of Proteins Encapsulated within Sol-Gel Derived Materials Anal. Chim. Acta 2002, 461, 1-36 10.1016/S0003-2670(02)00229-5
19. Carnes, E. C.; Harper, J. C.; Ashley, C. E.; Lopez, D. M.; Brinker, L. M.; Liu, J. W.; Singh, S.; Brozik, S. M.; Brinker, C. J. Cell-Directed Localization and Orientation of a Functional Foreign Transmembrane Protein within a Silica Nanostructure J. Am. Chem. Soc. 2009, 131, 14255-14257 10.1021/ja906055m
20. Bhatia, R. B.; Brinker, C. J.; Gupta, A. K.; Singh, A. K. Aqueous Sol-Gel Process for Protein Encapsulation Chem. Mater. 2000, 12, 2434-2441 10.1021/cm000260f
21. Meunier, C. F.; Dandoy, P.; Su, B.-L. Encapsulation of Cells within Silica Matrixes: Towards a New Advance in the Conception of Living Hybrid Materials J. Colloid Interface Sci. 2010, 342, 211-224 10.1016/j.jcis.2009.10.050
22. Harper, J. C.; Khirpin, C. Y.; Carnes, E. C.; Ashley, C. E.; Lopez, D. M.; Savage, T.; Jones, H. D. T.; Davis, R. W.; Nunez, D. E.; Brinker, L. M.; Kaehr, B.; Brozik, S. M.; Brinker, C. J. Cell-Directed Integration into Three-Dimensional Lipid-Silica Nanostructured Matrices ACS Nano 2010, 4, 5539-5550 10.1021/nn101793u
23. Baca, H. K.; Ashley, C.; Carnes, E.; Lopez, D.; Flemming, J.; Dunphy, D.; Singh, S.; Chen, Z.; Liu, N. G.; Fan, H. Y.; Lopez, G. P.; Brozik, S. M.; Werner-Washburne, M.; Brinker, C. J. Cell-Directed Assembly of Lipid-Silica Nanostructures Providing Extended Cell Viability Science 2006, 313, 337-341 10.1126/science.1126590
24. Livage, J.; Coradin, T. Living Cells in Oxide Glasses Rev. Mineral. Geochem. 2006, 64, 315-332 10.2138/rmg.2006.64.10
25. Carturan, G.; Dal Toso, R.; Boninsegna, S.; Dal Monte, R. Encapsulation of Functional Cells by Sol-Gel Silica: Actual Progress and Perspectives for Cell Therapy J. Mater. Chem. 2004, 14, 2087-2098 10.1039/b401450b
26. Coradin, T.; Allouche, J.; Boissiére, M.; Livage, J. Sol-Gel Biopolymer/Silica Nanocomposites in Biotechnology Curr. Nanosci. 2006, 2, 219-230 10.2174/1573413710602030219
27. Avnir, D.; Coradin, T.; Lev, O.; Livage, J. Recent Bio-Applications of Sol-Gel Materials J. Mater. Chem. 2006, 16, 1013-1030 10.1039/B512706H
28. Depagne, C.; Roux, C.; Coradin, T. How to Design Cell-Based Biosensors Using the Sol-Gel Process Anal. Bioanal. Chem. 2011, 400, 965-976 10.1007/s00216-010-4351-y
29. Nassif, N.; Roux, C.; Coradin, T.; Rager, M. N.; Bouvet, O. M. M.; Livage, J. A Sol-Gel Matrix to Preserve the Viability of Encapsulated Bacteria J. Mater. Chem. 2003, 13, 203-208 10.1039/b210167j
30. Conroy, J. F. T.; Power, M. E.; Martin, J.; Earp, B.; Hosticka, B.; Daitch, C. E.; Norris, P. M. Cells in Sol-Gels I: A Cytocompatible Route for the Production of Macroporous Silica Gels J. Sol-Gel Sci. Technol. 2000, 18, 269-283 10.1023/A:1008704208324
31. Ferrer, M. L.; Garcia-Carvajal, Z. Y.; Yuste, L.; Rojo, F.; del Monte, F. Bacteria Viability in Sol-Gel Materials Revisited: Cryo-SEM as a Suitable Tool to Study the Structural Integrity of Encapsulated Bacteria Chem. Mater. 2006, 18, 1458-1463 10.1021/cm0522275
32. Nassif, N.; Bouvet, O.; Rager, M. N.; Roux, C.; Coradin, T.; Livage, J. Living Bacteria in Silica Gels Nat. Mater. 2002, 1, 42-44 10.1038/nmat709
33. Harper, J. C.; Edwards, T. L.; Savage, T.; Harbaugh, S.; Kelly-Loughnane, N.; Stone, M. O.; Brinker, C. J.; Brozik, S. M. Orthogonal Cell-Based Biosensing: Fluorescent, Electrochemical, and Colorimetric Detection with Silica-Immobilized Cellular Communities Integrated with an ITO-Glass/Plastic Laminate Cartridge Small 2012, 8, 2743-2751 10.1002/smll.201200343
34. Back, J. P.; Kroll, R. G. The Differential Fluorescence of Bacteria Stained with Acridine-Orange and the Effects of Heat J. Appl. Bacteriol. 1991, 71, 51-58 10.1111/j.1365-2672.1991.tb04662.x
35. Davey, H. M.; Hexley, P. Red but Not Dead? Membranes of Stressed Saccharomyces cerevisiae are Permeable to Propidium Iodide Environ. Microbiol. 2011, 13, 163-171 10.1111/j.1462-2920.2010.02317.x
36. Harper, J. C.; Lopez, D. M.; Larkin, E.; Economides, M.K.; McIntyre, S. K.; Alan, T. M.; Tartis, M. S.; Werner-Washburne, M.; Brinker, C. J.; Brozik, S. M.; Wheeler, D. R. Encapsulation of S. cerevisiae in Poly(glycerol) Silicate Derived Matrices: Effect of Matrix Additives and Cell Metabolic Phase on Long-Term Viability and Rate of Gene Expression Chem. Mater. 2011, 23, 2555-2564 10.1021/cm103525u
37. Blondeau, M.; Brayner, R.; Guyot, F.; Coradin, T. Correlating Biological Methods to Assess Escherichia coli Bacteria Viability in Silica Gels Anal. Methods 2014, 6, 2429-2431 10.1039/c4ay00111g
38. Lleo, M. M.; Bonato, B.; Tafi, M. C.; Signoretto, C.; Boaretti, M.; Canepari, P. Resuscitation Rate in Different Enterococcal Species in the Viable but Non-Culturable State J. Appl. Microbiol. 2001, 91, 1095-1102 10.1046/j.1365-2672.2001.01476.x
39. Oliver, J. D. The Viable but Nonculturable State in Bacteria J. Microbiol. 2005, 43, 93-100
40. Heim, S.; Del Mar Lleo, M.; Bonato, B.; Guzman, C. A.; Canepari, P. The Viable but Nonculturable State and Starvation are Different Stress Responses of Enterococcus faecalis, as Determined by Proteome Analysis J. Bacteriol. 2002, 184, 6739-6745 10.1128/JB.184.23.6739-6745.2002
41. Bomati, E. K.; Haley, J. E.; Noel, J. P.; Deheyn, D. D. Spectral and Structural Comparison Between Bright and Dim Green Fluorescent Proteins in Amphioxus Sci. Rep. 2014, 4, 5469 10.1038/srep05469
42. Bomati, E. K.; Manning, G.; Deheyn, D. D. Amphioxus Encodes the Largest Known Family of Green Fluorescent Proteins, which have Diversified into Distinct Functional Classes BMC Evol. Biol. 2009, 9, 77 10.1186/1471-2148-9-77
43. Harbaugh, S.; Kelley-Loughnane, N.; Davidson, M.; Narayanan, L.; Trott, S.; Chushak, Y. G.; Stone, M. O. FRET-Based Optical Assay for Monitoring Riboswitch Activation Biomacromolecules 2009, 10, 1055-1060 10.1021/bm801117f
44. Carlson, E. D.; Gan, R.; Hodgman, C. E.; Jewett, M. C. Cell-Free Protein Synthesis: Applications Come of Age Biotechnol. Adv. 2012, 30, 1185-1194 10.1016/j.biotechadv.2011.09.016
45. Park, N.; Um, S. H.; Funabashi, H.; Xu, J.; Luo, D. A Cell-Free Protein-Producing Gel Nat. Mater. 2009, 8, 432-437 10.1038/nmat2419
46. Eleftheriou, N. M.; Ge, X.; Kolesnik, J.; Falconer, S. B.; Harris, R. J.; Khurigara, C.; Brown, E. D.; Brennan, J. D. Entrapment of Living Bacterial Cells in Low-Concentration Silica Materials Preserves Cell Division and Promoter Regulation Chem. Mater. 2013, 25, 4798-4805 10.1021/cm403198z
47. Coiffier, A.; Coradin, T.; Roux, C.; Bouvet, O. M. M.; Livage, J. Sol-Gel Encapsulation of Bacteria: A Comparison Between Alkoxide and Aqueous Routes J. Mater. Chem. 2001, 11, 2039-2044 10.1039/b101308o
48. Carturan, G.; Dal Monte, R.; Pressi, G.; Secondin, S.; Verza, P. Production of Valuable Drugs from Plant Cells Immobilized by Hybrid Sol-Gel SiO2 J. Sol-Gel Sci. Technol. 1998, 13, 273-276 10.1023/A:1008676904085
49. Campostrini, R.; Carturan, G.; Ciniato, R.; Piovan, A.; Filippini, R.; Innocenti, G.; Cappelletti, E. M. Immobilization of Plant Cells in Hybrid Sol-Gel Materials J. Sol-Gel Sci. Technol. 1996, 7, 87-97 10.1007/BF00401888
50. Gray, J. V.; Petsko, G. A.; Johnston, G. C.; Ringe, D.; Singer, R. A.; Werner-Washburne, M. "Sleeping Beauty": Quiescence in Saccharomyces cerevisiae Microbiol. Mol. Biol. Rev. 2004, 68, 187-206 10.1128/MMBR.68.2.187-206.2004