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Bacterial Surface Layer Proteins: From Moonlighting to Biomimetics: A New Horizonto Lead

DOI: 10.4236/abb.2018.98023, PP. 352-372

Keywords: Moonlighting, Biomimetic, Surface Layer Proteins, Self-Assembly, Nano-Biotechnology

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Abstract:

The landmark discovery of moonlighting proteins embarks the significant progress in understanding the biological complexity and their closed-circuit analysis. The growing continuum in the variety of moonlighting functions paved the way for further elucidation of structural-functional aspects of protein evolution and design of proteins with novel functions. Currently, the moonlighting functions in various adhesive properties of surface layer proteins, an essential component of cell surface architecture of archaea and all phylogenetic groups of eubacteria become more prominently recognized. The remarkable credentials of surface layer proteins to self-assemble into supramolecular structures at nano-scale dimension have been exploited for the production of smart biomaterials in the form of biomimetics has been thrust area of research. The finely tuned topological features in terms of shape, size, geometry and surface chemistry of surface layer proteins are crucial for the production of biomimetics. The current developments of biomimetic lipid bilayers and composite membranes find applicability in understanding the functional dynamism of evolutionary relationship of bacterial cell envelopes and vaccine development, drug development and drug delivery. Though the development of biomimetics embraces fascination but faces with technological challenges. The plethora of literature has been available for the moonlighting aspects and nano-technological applications separately but none of the review describes towards the rhythmic transition from moonlighting functions of surface layer proteins of bacteria to biomimetics development and applications. Therefore, this review describes certain basic aspects of moonlighting functions and their mechanism of action, surface layer proteins and their moonlighting functions of commensal bacteria and their transition towards biomimetics. The recent developments of biomimetics based on surface layer proteins have been summarized and also posited different challenges and future prospects.

References

[1]  Beadle, G.W. and Tatum, E.L. (1941) Genetic Control of Biochemical Reactions in Neurospora. Proceedings of the National Academy of Sciences, 27, 499-506.
https://doi.org/10.1073/pnas.27.11.499
[2]  Piatigorsky, J. and Wistow, G.J. (1989) Enzyme/Crystallins: Gene Sharing as an Evolutionary Strategy. Cell, 57, 197-199.
https://doi.org/10.1016/0092-8674(89)90956-2
[3]  Copley, S.D. (2012) Moonlighting Is Mainstream: Paradigm Adjustment Required. Bioessays, 34, 578-588.
https://doi.org/10.1002/bies.201100191
[4]  Henderson, B. and Martin, A.C.R. (2014) Protein Moonlighting: A New Factor in Biology and Medicine. Biochemical Society Transactions, 42, 1671-1678.
https://doi.org/10.1042/BST20140273
[5]  Bielli, P. and Calabrese, L. (2002) Structure to Function Relationships in Ceruloplasmin: A Moonlighting Protein. Cellular and Molecular Life Sciences CMLS, 59, 1413-1427.
https://doi.org/10.1007/s00018-002-8519-2
[6]  Jeffery, C.J. (1999) Moonlighting Proteins. Trends in Biochemical Sciences, 24, 8-11.
https://doi.org/10.1016/S0968-0004(98)01335-8
[7]  Huberts, D.H.E.W. and van der Klei, I.J. (2010) Moonlighting Proteins: An Intriguing Mode of Multitasking. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1803, 520-525.
https://doi.org/10.1016/j.bbamcr.2010.01.022
[8]  Jeffery, C.J. (2003) Moonlighting Proteins: Old Proteins Learning New Tricks. TRENDS in Genetics, 19, 415-417.
https://doi.org/10.1016/S0168-9525(03)00167-7
[9]  Sleytr, U.B., Messner, P., Pum, D. and Sára, M. (1999) Crystalline Bacterial Cell Surface Layers (S Layers): From Supramolecular Cell Structure to Biomimetics and Nanotechnology. Angewandte Chemie International Edition, 38, 1034-1054.
https://doi.org/10.1002/(SICI)1521-3773(19990419)38:8<1034::AID-ANIE1034>3.0.CO;2-#
[10]  Sára, M. and Sleytr, U.B. (2000) S-Layer Proteins. Journal of Bacteriology, 182, 859-868.
https://doi.org/10.1128/JB.182.4.859-868.2000
[11]  Wang, G.Q., Xia, Y., Cui, J., Gu, Z.N., Song, Y.D., Chen, Y.Q., Chen, H.Q., Zhang, H. and Chen, W. (2013) The Roles of Moonlighting Proteins in Bacteria. Current Issues in Molecular Biology, 16, 15-22.
[12]  Guan, Z.B. (2007) Supramolecular Design in Biopolymers and Biomimetic Polymers for Advanced Mechanical Properties. Polymer International, 56, 467-473.
https://doi.org/10.1002/pi.2245
[13]  Karger-Kocsis, J. (2014) Biodegradable Polyester-Based Shape Memory Polymers: Concepts of (supra) Molecular Architecturing. Express Polymer Letters, 8, 397-412.
https://doi.org/10.3144/expresspolymlett.2014.44
[14]  Di Natale, C., Martinelli, E., Paolesse, R., Amico, A., Filippini, D. and Lundstrom, I. (2008) An Experimental Biomimetic Platform for Artificial Olfaction. PLoS One, 3, e3139.
https://doi.org/10.1371/journal.pone.0003139
[15]  Justyna, K.-K. and Kozik, A. (2014) Moonlighting Proteins as Virulence Factors of Pathogenic Fungi, Parasitic Protozoa and Multicellular Parasites. Molecular Oral Microbiology, 29, 270-283.
https://doi.org/10.1111/omi.12078
[16]  Henderson, B. and Martin, A. (2011) Bacterial Virulence in the Moonlight: Multitasking Bacterial Moonlighting Proteins Are Virulence Determinants in Infectious Disease. Infection and Immunity, 79, 3476-3491.
https://doi.org/10.1128/IAI.00179-11
[17]  Pavkov-Keller, T., Howorka, S. and Keller, W. (2011) The Structure of Bacterial S-Layer Proteins. Progress in Molecular Biology and Translational Science, 103, 73-130.
https://doi.org/10.1016/B978-0-12-415906-8.00004-2
[18]  Ilk, N., Egelseer, E.M. and Sleytr, U.B. (2011) S-Layer Fusion Proteins—Construction Principles and Applications. Current Opinion in Biotechnology, 22, 824-831.
https://doi.org/10.1016/j.copbio.2011.05.510
[19]  Fagan, R.P. and Fairweather, N.F. (2014) Biogenesis and Functions of Bacterial S-Layers. Nature Reviews Microbiology, 12, 211-222.
https://doi.org/10.1038/nrmicro3213
[20]  Schuster, B. and Sleytr, U.B. (2014) Biomimetic Interfaces Based on S-Layer Proteins, Lipid Membranes and Functional Biomolecules. Journal of the Royal Society Interface, 11, Article ID: 20140232.
https://doi.org/10.1098/rsif.2014.0232
[21]  Arbing, M.A., Chan, S., Shin, A., Phan, T., Ahn, C.J., Rohlin, L. and Gunsalus, R.P. (2012) Structure of the Surface Layer of the Methanogenic Archaea Methanosarcina acetivorans. Proceedings of the National Academy of Sciences, 109, 11812-11817.
https://doi.org/10.1073/pnas.1120595109
[22]  Rothbauer, M., Kupcu, S., Sticker, D., Sleytr, U.B. and Ertl, P. (2013) Exploitation of S-Layer Anisotropy: pH-Dependent Nanolayer Orientation for Cellular Micropatterning. ACS Nano, 7, 8020-8030.
https://doi.org/10.1021/nn403198a
[23]  Sengupta, S., Ghosh, S. and Nagaraja, V. (2008) Moonlighting Function of Glutamate Racemase from Mycobacterium tuberculosis: Racemization and DNA Gyrase Inhibition Are Two Independent Activities of the Enzyme. Microbiology, 154, 2796-2803.
https://doi.org/10.1099/mic.0.2008/020933-0
[24]  Pum, D. and Sleytr, U.B. (2014) Reassembly of S-Layer Proteins. Nanotechnology, 25, Article ID: 312001.
https://doi.org/10.1088/0957-4484/25/31/312001
[25]  Sriram, G., Martinez, J.A., McCabe, E.R., Liao, J.C. and Dipple, K.M. (2005) Single-Gene Disorders: What Role Could Moonlighting Enzymes Play? The American Journal of Human Genetics, 76, 911-924.
https://doi.org/10.1086/430799
[26]  Gancedo, C. and Carmen-Lisset, F. (2008) Moonlighting Proteins in Yeasts. Microbiology and Molecular Biology Reviews, 72, 197-210.
https://doi.org/10.1128/MMBR.00036-07
[27]  Piatigorsky, J. (2007) Gene Sharing and Evolution: The Diversity of Protein Functions. Harvard University Press, Cambridge, 471-505.
https://doi.org/10.4159/9780674042124
[28]  Copley, S.D. (2003) Enzymes with Extra Talents: Moonlighting Functions and Catalytic Promiscuity. Current Opinion in Chemical Biology, 7, 265-272.
https://doi.org/10.1016/S1367-5931(03)00032-2
[29]  Fares, M.A. (2014) The Evolution of Protein Moonlighting: Adaptive Traps and Promiscuity in the Chaperonins. Biochemical Society Transactions, 42, 1709-1714.
https://doi.org/10.1042/BST20140225
[30]  Todd, A.E., Orengo, C.A. and Thornton, J.M. (1999) Evolution of Protein Function, from a Structural Perspective. Current Opinion in Chemical Biology, 3, 548-556.
https://doi.org/10.1016/S1367-5931(99)00007-1
[31]  Kainulainen, V. and Korhonen, T.K. (2014) Dancing to Another Tune—Adhesive Moonlighting Proteins in Bacteria. Biology, 3, 178-204.
https://doi.org/10.3390/biology3010178
[32]  Górska, S., Buda, B., Brzozowska, E., Schwarzer, M., Srutkova, D., Kozakova, H. and Gamian, A. (2016) Identification of Lactobacillus Proteins with Different Recognition Patterns between Immune Rabbit Sera and Nonimmune Mice or Human Sera. BMC Microbiology, 16, 17.
https://doi.org/10.1186/s12866-016-0631-9
[33]  Sheokand, N., Malhotra, H., Kumar, S., Tillu, V.A., Chauhan, A.S., Raje, C.I. and Raje, M. (2014) Moonlighting Cell-Surface GAPDH Recruits Apotransferrin to Effect Iron Egress from Mammalian Cells. Journal of Cell Science, 127, 4279-4291.
https://doi.org/10.1242/jcs.154005
[34]  Granato, D., Bergonzelli, G.E., Pridmore, R.D., Marvin, L., Rouvet, M. and Corthésy-Theulaz, I.E. (2004) Cell Surface-Associated Elongation Factor Tu Mediates the Attachment of Lactobacillus johnsonii NCC533 (La1) to Human Intestinal Cells and Mucins. Infection and Immunity, 72, 2160-2169.
https://doi.org/10.1128/IAI.72.4.2160-2169.2004
[35]  Bergonzelli, G.E., Granato, D., Pridmore, R.D., Marvin-Guy, L.F., Donnicola, D. and Corthésy-Theulaz, I.E. (2006) GroEL of Lactobacillus johnsonii La1 (NCC 533) Is Cell Surface Associated: Potential Role in Interactions with the Host and the Gastric Pathogen Helicobacter pylori. Infection and Immunity, 74, 425-434.
https://doi.org/10.1128/IAI.74.1.425-434.2006
[36]  Beck, H.C., Madsen, S.M., Glenting, J., Petersen, J., Israelsen, H., Norrelykke, M., Antonsson, M. and Hansen, A.M. (2009) Proteomic Analysis of Cell Surface-Associated Proteins from Probiotic Lactobacillus plantarum. FEMS Microbiology Letters, 297, 61-66.
https://doi.org/10.1111/j.1574-6968.2009.01662.x
[37]  Pachathundikandi, S.K., Lind, J., Tegtmeyer, N., El-Omar, E.M. and Backert, S. (2015) Interplay of the Gastric Pathogen Helicobacter pylori with Toll-Like Receptors. BioMed Research International, 2015, Article ID: 192420.
https://doi.org/10.1155/2015/192420
[38]  Saroj, S.D., Maudsdotter, L., Tavares, R. and Jonsson, A.B. (2016) Lactobacilli Interfere with Streptococcus pyogenes Hemolytic Activity and Adherence to Host Epithelial Cells. Frontiers in Microbiology, 7, 1176.
https://doi.org/10.3389/fmicb.2016.01176
[39]  Kainulainen, V. (2012) Moonlighting Proteins of Lactobacillus crispatus: Extracellular Localization, Cell Wall Anchoring and Interactions with the Host. Dissertationes Biocentri Viikki Universitatis Helsingiensis.
http://hdl.handle.net/10138/28809
[40]  Morrill, J., Kulcinskaja, E., Sulewska, A.M., Lahtinen, S., Stalbrand, H., Svensson, B. and Hachem, M.A. (2015) The GH5 1,4-β-Mannanase from Bifidobacteriumanimalis subsp. lacti s Bl-04 Possesses a Low-Affinity Mannan-Binding Module and Highlights the Diversity of Mannanolytic Enzymes. BMC Biochemistry, 16, 26.
https://doi.org/10.1186/s12858-015-0055-4
[41]  Bhattacharya, S., Ploplis, V.A. and Castellino, F.J. (2012) Bacterial Plasminogen Receptors Utilize Host Plasminogen System for Effective Invasion and Dissemination. Journal of Biomedicine and Biotechnology, 2012, Article ID: 482096.
https://doi.org/10.1155/2012/482096
[42]  Sanderson-Smith, M.L., De Oliveira, D.M., Ranson, M. and McArthur, J.D. (2012) Bacterial Plasminogen Receptors: Mediators of a Multifaceted Relationship. Journal of Biomedicine and Biotechnology, 2012, Article ID: 272148.
https://doi.org/10.1155/2012/272148
[43]  Salazar, N., Castiblanco-Valencia, M.M., da Silva, L., de Castro, í., Monaris, D., Masuda, H.P., Barbosa, A.S. and MattosArêas, A.P. (2014) Staphylococcus aureus Manganese Transport Protein C (MntC) Is an Extracellular Matrix- and Plasminogen-Binding Protein. PLoS ONE, 9, e112730.
https://doi.org/10.1371/journal.pone.0112730
[44]  Candela, M. (2010) DnaK from Bifidobacteriumanimalis subsp. lactis Is a Surface-Exposed Human Plasminogen Receptor Upregulated in Response to Bile Salts. Microbiology, 156, 1609-1618.
https://doi.org/10.1099/mic.0.038307-0
[45]  Westermann, C., Gleinser, M., Corr, S.C. and Riedel, C.U. (2016) A Critical Evaluation of Bifidobacterial Adhesion to the Host Tissue. Frontiers in Microbiology, 7, 1220.
https://doi.org/10.3389/fmicb.2016.01220
[46]  Castaldo, C., Vastano, V., Siciliano, R.A., Candela, M., Vici, M., Muscariello, L., Marasco, R. and Sacco, M. (2009) Surface Displaced Alfa-Enolase of Lactobacillus plantarum Is a Fibronectin Binding Protein. Microbial Cell Factories, 8, 14.
https://doi.org/10.1186/1475-2859-8-14
[47]  Das, M.R. (2016) Molecular Association of Glucose-6-Phosphate Isomerase and Pyruvate Kinase M2 with Glyceraldehyde-3-Phosphate Dehydrogenase in Cancer Cells. BMC Cancer, 16, 152.
https://doi.org/10.1186/s12885-016-2172-x
[48]  Aziz, M. (2016) Biomimicry as an Approach for Bio-Inspired Structure with the Aid of Computation. Alexandria Engineering Journal, 55, 707-714.
https://doi.org/10.1016/j.aej.2015.10.015
[49]  Bhushan, B. (2009) Biomimetics: Lessons from Nature—An Overview. Philosophical Transactions of the Royal Society: A Mathematical Physical and Engineering Sciences, 367, 1445-1486.
https://doi.org/10.1098/rsta.2009.0011
[50]  McCarty, M. (2009) Life of Bionics Founder a Fine Adventure. Dayton Daily News.
[51]  Vincent, J.F., Bogatyreva, O.A., Bogatyrev, N.R., Bowyer, A. and Pahl, A.K. (2006) Biomimetics: Its Practice and Theory. Journal of the Royal Society Interface, 3, 471-482.
https://doi.org/10.1098/rsif.2006.0127
[52]  Shimomura, M. (2012) Engineering Biomimetics: Integration of Biology and Nanotechnology. In: Design for Innovative Value towards a Sustainable Society, Springer, Dordrecht, 905-907.
https://doi.org/10.1007/978-94-007-3010-6_186
[53]  Hwang, J., Jeong, Y., Park, J.M., Lee, K.H., Hong, J.W. and Choi, J. (2015) Biomimetics: Forecasting the Future of Science, Engineering, and Medicine. International Journal of Nanomedicine, 10, 5701.
[54]  Romei, F. (2008) Leonardo Da Vinci. The Oliver Press, Minneapolis.
[55]  Sanchez, C., Arribart, H. and Guille, M.M. (2005) Biomimetism and Bioinspiration as Tools for the Design of Innovative Materials and Systems. Nature Materials, 4, 277-288.
https://doi.org/10.1038/nmat1339
[56]  Vincent, J.F.V. (2009) Biomimetics—A Review. Proceedings of the Institution of Mechanical Engineers, Part H: Journal of Engineering in Medicine, 223, 919-939.
https://doi.org/10.1243/09544119JEIM561
[57]  Sleytr, U.B., Schuster, B., Egelseer, E.M. and Pum, D. (2014) S-Layers: Principles and Applications. FEMS Microbiology Reviews, 38, 823-864.
https://doi.org/10.1111/1574-6976.12063
[58]  Ucisik, M.H., Sleytr, U.B. and Schuster, B. (2015) Emulsomes Meet S-Layer Proteins: An Emerging Targeted Drug Delivery System. Current Pharmaceutical Biotechnology, 16, 392-405.
https://doi.org/10.2174/138920101604150218112656
[59]  Watson, H. (2015) Biological Membranes. Essays in Biochemistry, 59, 43-69.
https://doi.org/10.1042/bse0590043
[60]  Von Heijne, G. (2006) Membrane-Protein Topology. Nature Reviews Molecular Cell Biology, 7, 909-918.
https://doi.org/10.1038/nrm2063
[61]  Giess, F., Friedrich, M.G., Heberle, J., Naumann, R.L. and Knoll, W. (2004) The Protein-Tethered Lipid Bilayer: A Novel Mimic of the Biological Membrane. Biophysical Journal, 87, 3213-3220.
https://doi.org/10.1529/biophysj.104.046169
[62]  Schuster, B., Pum, D. and Sleytr, U.B. (2008) S-Layer Stabilized Lipid Membranes. Biointerphases, 3, FA3-FA11.
https://doi.org/10.1116/1.2889067
[63]  Schuster, B., et al. (2004) S-Layer Proteins as Supporting Scaffoldings for Functional Lipid Membranes. IEEE Transactions on Nanobioscience, 3, 16-21.
https://doi.org/10.1109/TNB.2004.824267
[64]  Rodrigues-Oliveira, T., et al. (2017) Archaeal S-Layers: Overview and Current State of the Art. Frontiers in Microbiology, 8, 2597.
https://doi.org/10.3389/fmicb.2017.02597
[65]  Albers, S.-V. and Meyer, B.H. (2011) The Archaeal Cell Envelope. Nature Reviews Microbiology, 9, 414-426.
https://doi.org/10.1038/nrmicro2576
[66]  Ford, M.J., Nomellini, J.F. and Smit, J. (2007) S-Layer Anchoring and Localization of an S-Layer-Associated Protease in Caulobacter crescentus. Journal of Bacteriology, 189, 2226-2237.
https://doi.org/10.1128/JB.01690-06
[67]  Weygand, M., Wetzer, B., Pum, D., Sleytr, U.B., Cuvillier, N., Kjaer, K., Howes, P.B. and Losche, M. (1999) Bacterial S-Layer Protein Coupling to Lipids: X-Ray Reflectivity and Grazing Incidence Diffraction Studies. Biophysical Journal, 76, 458-468.
https://doi.org/10.1016/S0006-3495(99)77213-9
[68]  Lagny, T.J. and Bassereau, P. (2015) Bioinspired Membrane-Based Systems for a Physical Approach of Cell Organization and Dynamics: Usefulness and Limitations. Interface Focus, 5, Article ID: 20150038.
https://doi.org/10.1098/rsfs.2015.0038
[69]  Khan, M.S., Dosoky, N.S. and Williams, J.D. (2013) Engineering Lipid Bilayer Membranes for Protein Studies. International Journal of Molecular Sciences, 14, 21561-21597.
https://doi.org/10.3390/ijms141121561
[70]  Kunitake, T. (1992) Synthetic Bilayer Membranes: Molecular Design, Self-Organization, and Application. Angewandte Chemie International Edition, 31, 709-726.
https://doi.org/10.1002/anie.199207091
[71]  Hirano-Iwata, A., et al. (2009) Free-Standing Lipid Bilayers in Silicon Chips—Membrane Stabilization Based on Microfabricated Apertures with a Nanometer-Scale Smoothness. Langmuir, 26, 1949-1952.
https://doi.org/10.1021/la902522j
[72]  Ricker, J.V., Tsvetkova, N.M., Wolkers, W.F., Leidy, C., Tablin, F., Longo, M. and Crowe, J.H. (2003) Trehalose Maintains Phase Separation in an Air-Dried Binary Lipid Mixture. Biophysical Journal, 84, 3045-3051.
https://doi.org/10.1016/S0006-3495(03)70030-7
[73]  Schuster, B. and Sleytr, U.B. (2009) Composite S-Layer Lipid Structures. Journal of Structural Biology, 168, 207-216.
https://doi.org/10.1016/j.jsb.2009.03.004
[74]  Knoll, W., Naumann, R., Friedrich, M., Robertson, J.W.F., Losche, M., Heinrich, F., McGillivray, D.J., et al. (2008) Solid Supported Lipid Membranes: New Concepts for the Biomimetic Functionalization of Solid Surfaces. Biointerphases, 3, FA125-FA135.
https://doi.org/10.1116/1.2913612
[75]  Lei, G. and MacDonald, R.C. (2003) Lipid Bilayer Vesicle Fusion: Intermediates Captured by High-Speed Microfluorescence Spectroscopy. Biophysical Journal, 85, 1585-1599.
https://doi.org/10.1016/S0006-3495(03)74590-1
[76]  Monteiro, N., Martins, A., Reis, R.L. and Neves, N.M. (2014) Liposomes in Tissue Engineering and Regenerative Medicine. Journal of the Royal Society Interface, 11, Article ID: 20140459.
https://doi.org/10.1098/rsif.2014.0459
[77]  Ucisik, M.H., Küpcü, S., Debreczeny, M., Schuster, B. and Sleytr, U.B. (2013) S-Layer Coated Emulsomes as Potential Nanocarriers. Small, 9, 2895-2904.
https://doi.org/10.1002/smll.201203116
[78]  Lombardo, D., et al. (2016) Soft Interaction in Liposome Nanocarriers for Therapeutic Drug Delivery. Nanomaterials, 6, 125.
https://doi.org/10.3390/nano6070125
[79]  Hynonen, U. and Palva, A. (2013) Lactobacillus Surface Layer Proteins: Structure, Function and Applications. Applied Microbiology and Biotechnology, 97, 5225-5243.
https://doi.org/10.1007/s00253-013-4962-2
[80]  Ma, Y., Goyette, J., Poole, K. and Gaus, K. (2017) Introducing Membrane Charge and Membrane Potential to T Cell Signalling. Frontiers in Immunology, 8, 1513.
https://doi.org/10.3389/fimmu.2017.01513
[81]  Hollmann, A., Delfederico, L., Glikmann, G., De Antoni, G., Semorile, L. and Disalvo, E.A. (2007) Characterization of Liposomes Coated with S-Layer Proteins from Lactobacilli. Biochimica et BiophysicaActa (BBA) Biomembranes, 1768, 393-400.
https://doi.org/10.1016/j.bbamem.2006.09.009
[82]  Pouwels, P.H., Leer, R.J., Shaw, M., den Bak-Glashouwer, M.-J.H., Tielen, F.D., Smit, E., Martinez, B., Jore, J. and Conway, P.L. (1998) Lactic Acid Bacteria as Antigen Delivery Vehicles for Oral Immunization Purposes. International Journal of Food Microbiology, 41, 155-167.
https://doi.org/10.1016/S0168-1605(98)00048-8
[83]  Sleytr, U.B., Huber, C., Ilk, N., Pum, D., Schuster, B. and Egelseer, E.M. (2007) S-Layers as a Tool Kit for Nanobiotechnological Applications. FEMS Microbiology Letters, 267, 131-144.
https://doi.org/10.1111/j.1574-6968.2006.00573.x
[84]  Mader, C., Küpcü, S., Sleytr, U.B. and Sára, M. (2000) S-Layer-Coated Liposomes as a Versatile System for Entrapping and Binding Target Molecules. Biochimica et BiophysicaActa (BBA) Biomembranes, 1463, 142-150.
https://doi.org/10.1016/S0005-2736(99)00190-X
[85]  Del Rosario, R.B., Baron, L.A., Lawton, R.G. and Wahl, R.L. (1992) Streptavidin-Biotinylated IgG Conjugates: A Simple Procedure for Reducing Polymer Formation. International Journal of Radiation Applications and Instrumentation. Part B. Nuclear Medicine and Biology, 19, 417-421.
https://doi.org/10.1016/0883-2897(92)90128-L
[86]  Guo, X., Wu, Z. and Guo, Z. (2012) New Method for Site-Specific Modification of Liposomes with Proteins Using Sortase A-Mediated Transpeptidation. Bioconjugate Chemistry, 23, 650-655.
https://doi.org/10.1021/bc200694t
https://pubs.acs.org/doi/abs/10.1021/bc200694t
[87]  Bozzuto, G. and Molinari, A. (2015) Liposomes as Nanomedical Devices. International Journal of Nanomedicine, 10, 975.
https://doi.org/10.2147/IJN.S68861
[88]  Gill, B., Singh, J., Sharma, V. and Kumar, S.H. (2012) Emulsomes: An Emerging Vesicular Drug Delivery System. Asian Journal of Pharmaceutics, 6, 87.
https://doi.org/10.4103/0973-8398.102930
[89]  Major, M., Prieur, E., Tocanne, J.F., Betbeder, D. and Sautereau, A.M. (1997) Characterisation and Phase Behaviour of Phospholipid Bilayers Adsorbed on Spherical Polysaccharidic Nanoparticles. Biochimica et BiophysicaActa (BBA) Biomembranes, 1327, 32-40.
https://doi.org/10.1016/S0005-2736(97)00041-2
[90]  Goni, F.M. (2014) The Basic Structure and Dynamics of Cell Membranes: An Update of the Singer-Nicolson Model. Biochimica et BiophysicaActa (BBA) Biomembranes, 1838, 1467-1476.
https://doi.org/10.1016/j.bbamem.2014.01.006
[91]  Ziani, K., Fang, Y. and McClements, D.J. (2012) Encapsulation of Functional Lipophilic Components in Surfactant-Based Colloidal Delivery Systems: Vitamin E, Vitamin D, and Lemon Oil. Food Chemistry, 134, 1106-1112.
https://doi.org/10.1016/j.foodchem.2012.03.027
[92]  Lin, C.H., Chen, C.H., Lin, Z.C. and Fang, J.Y. (2017) Recent Advances in Oral Delivery of Drugs and Bioactive Natural Products Using Solid Lipid Nanoparticles as the Carriers. Journal of Food and Drug Analysis, 25, 219-234.
https://doi.org/10.1016/j.jfda.2017.02.001
[93]  Ucisik, M.H., Küpcü, S., Schuster, B. and Sleytr, U.B. (2013) Characterization of Curcuemulsomes: Nanoformulation for Enhanced Solubility and Delivery of Curcumin. Journal of Nanobiotechnology, 11, 37.
https://doi.org/10.1186/1477-3155-11-37
[94]  Walsh, T.J., Finberg, R.W., Arndt, C., Hiemenz, J., Schwartz, C., Bodensteiner, D., Pappas, P., et al. (1999) Liposomal Amphotericin B for Empirical Therapy in Patients with Persistent Fever and Neutropenia. New England Journal of Medicine, 340, 764-771.
https://doi.org/10.1056/NEJM199903113401004
[95]  Vyas, S.P., Subhedar, R. and Jain, S. (2006) Development and Characterization of Emulsomes for Sustained and Targeted Delivery of an Antiviral Agent to Liver. Journal of Pharmacy and Pharmacology, 58, 321-326.
https://doi.org/10.1211/jpp.58.3.0005
[96]  Khan, Z.A., Tripathi, R. and Mishra, B. (2012) Methotrexate: A Detailed Review on Drug Delivery and Clinical Aspects. Expert Opinion on Drug Delivery, 9, 151-169.
https://doi.org/10.1517/17425247.2012.642362
[97]  Liou, J.W., Hung, Y.J., Yang, C.H. and Chen, Y.C. (2015) The Antimicrobial Activity of Gramicidin A Is Associated with Hydroxyl Radical Formation. PLoS ONE, 10, e0117065.
https://doi.org/10.1371/journal.pone.0117065
[98]  Hladky, S.B., Leung, J.C. and Fitzgerald, W.J. (1995) The Mechanism of Ion Conduction by Valinomycin: Analysis of Charge Pulse Responses. Biophysical Journal, 69, 1758-1772.
https://doi.org/10.1016/S0006-3495(95)80046-9
[99]  Volinsky, R., Kolusheva, S., Berman, A. and Jelinek, R. (2006) Investigations of Antimicrobial Peptides in Planar Film Systems. Biochimica et BiophysicaActa (BBA) Biomembranes, 1758, 1393-1407.
https://doi.org/10.1016/j.bbamem.2006.03.002
[100]  Bechinger, B. (1997) Structure and Functions of Channel-Forming Peptides: Magainins, Cecropins, Melittin and Alamethicin. The Journal of Membrane Biology, 156, 197-211.
https://doi.org/10.1007/s002329900201
[101]  Sankararamakrishnan, R., Adcock, C. and Sansom, M.S. (1996) The Pore Domain of the Nicotinic Acetylcholine Receptor: Molecular Modeling, Pore Dimensions, and Electrostatics. Biophysical Journal, 71, 1659-1671.
https://doi.org/10.1016/S0006-3495(96)79370-0
[102]  Reddish, F.N., Miller, C.L., Gorkhali, R. and Yang, J.J. (2017) Calcium Dynamics Mediated by the Endoplasmic/Sarcoplasmic Reticulum and Related Diseases. International Journal of Molecular Sciences, 18, 1024.
https://doi.org/10.3390/ijms18051024

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