1932

Abstract

Nature has inspired the development of biomimetic membrane sensors in which the functionalities of biological molecules, such as proteins and lipids, are harnessed for sensing applications. This review provides an overview of the recent developments for biomembrane sensors compatible with either bulk or planar sensing applications, namely using lipid vesicles or supported lipid bilayers, respectively. We first describe the individual components required for these sensing platforms and the design principles that are considered when constructing them, and we segue into recent applications being implemented across multiple fields. Our goal for this review is to illustrate the versatility of nature's biomembrane toolbox and simultaneously highlight how biosensor platforms can be enhanced by harnessing it.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-anchem-061622-042618
2024-07-17
2025-04-23
Loading full text...

Full text loading...

/deliver/fulltext/anchem/17/1/annurev-anchem-061622-042618.html?itemId=/content/journals/10.1146/annurev-anchem-061622-042618&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Sperelakis N. 2001.. Cell Physiology Sourcebook: A Molecular Approach. San Diego, CA:: Academic
    [Google Scholar]
  2. 2.
    Misawa N, Osaki T, Takeuchi S. 2018.. Membrane protein–based biosensors. . J. R. Soc. Interface 15::20170952
    [Crossref] [Google Scholar]
  3. 3.
    Lubrano C, Matrone GM, Iaconis G, Santoro F. 2020.. New frontiers for selective biosensing with biomembrane-based organic transistors. . ACS Nano 14::1227180
    [Crossref] [Google Scholar]
  4. 4.
    Jayaram A, Pappa A-M, Ghosh S, Manzer Z, Traberg W, et al. 2022.. Biomembranes in bioelectronic sensing. . Trends Biotechnol. 40::10723
    [Crossref] [Google Scholar]
  5. 5.
    Arakawa T, Dao DV, Mitsubayashi K. 2022.. Biosensors and chemical sensors for healthcare monitoring: a review. . IEEJ Trans. Electrical Electron. Eng. 17::62636
    [Crossref] [Google Scholar]
  6. 6.
    Srivastava S, Khare E. 2021.. Biosensors based medical devices for disease monitoring therapy. . IJARSCT 4:(2):26378
    [Crossref] [Google Scholar]
  7. 7.
    van den Hurk R, Evoy S. 2015.. A review of membrane-based biosensors for pathogen detection. . Sensors 15::1404578
    [Crossref] [Google Scholar]
  8. 8.
    Grasso G, Zane D, Dragone R. 2022.. Field and remote sensors for environmental health and food safety diagnostics: an open challenge. . Biosensors 12::285
    [Crossref] [Google Scholar]
  9. 9.
    McConnell EM, Nguyen J, Li Y. 2020.. Aptamer-based biosensors for environmental monitoring. . Front. Chem. 8::434
    [Crossref] [Google Scholar]
  10. 10.
    Antonacci A, Zappi D, Giardi MT, Scognamiglio V. 2021.. Photosynthesis-based biosensors for environmental analysis of herbicides. Case Stud. . Chem. Environ. Eng. 4::100157
    [Google Scholar]
  11. 11.
    Curulli A. 2021.. Electrochemical biosensors in food safety: challenges and perspectives. . Molecules 26::2940
    [Crossref] [Google Scholar]
  12. 12.
    Kuswandi B, Hidayat MA, Noviana E. 2022.. Based electrochemical biosensors for food safety analysis. . Biosensors 12::1088
    [Crossref] [Google Scholar]
  13. 13.
    Yasmin J, Ahmed MR, Cho B-K. 2016.. Biosensors and their applications in food safety: a review. . J. Biosyst. Eng. 41::24054
    [Crossref] [Google Scholar]
  14. 14.
    Ding W, Palaiokostas M, Wang W, Orsi M. 2015.. Effects of lipid composition on bilayer membranes quantified by all-atom molecular dynamics. . J. Phys. Chem. B 119::1526374
    [Crossref] [Google Scholar]
  15. 15.
    Harris NJ, Charalambous K, Findlay HE, Booth PJ. 2018.. Lipids modulate the insertion and folding of the nascent chains of alpha helical membrane proteins. . Biochem. Soc. Trans. 46::135566
    [Crossref] [Google Scholar]
  16. 16.
    Palaiokostas M, Ding W, Shahane G, Orsi M. 2018.. Effects of lipid composition on membrane permeation. . Soft Matter 14::8496508
    [Crossref] [Google Scholar]
  17. 17.
    Teixeira MH, Arantes GM. 2019.. Effects of lipid composition on membrane distribution and permeability of natural quinones. . RSC Adv. 9::1689299
    [Crossref] [Google Scholar]
  18. 18.
    Findlay HE, Booth PJ. 2017.. The folding, stability and function of lactose permease differ in their dependence on bilayer lipid composition. . Sci. Rep. 7::13056
    [Crossref] [Google Scholar]
  19. 19.
    Nilsson T, Lundin CR, Nordlund G, Ädelroth P, von Ballmoos C, Brzezinski P. 2016.. Lipid-mediated protein-protein interactions modulate respiration-driven ATP synthesis. . Sci. Rep. 6::24113
    [Crossref] [Google Scholar]
  20. 20.
    Corey RA, Song W, Duncan AL, Ansell TB, Sansom MS, Stansfeld PJ. 2021.. Identification and assessment of cardiolipin interactions with E. coli inner membrane proteins. . Sci. Adv. 7::eabh2217
    [Crossref] [Google Scholar]
  21. 21.
    Corradi V, Sejdiu BI, Mesa-Galloso H, Abdizadeh H, Noskov SY, et al. 2019.. Emerging diversity in lipid–protein interactions. . Chem. Rev. 119::5775848
    [Crossref] [Google Scholar]
  22. 22.
    Koebnik R, Locher KP, Van Gelder P. 2000.. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. . Mol. Microbiol. 37::23953
    [Crossref] [Google Scholar]
  23. 23.
    Xian H, Liou Y-C. 2021.. Functions of outer mitochondrial membrane proteins: mediating the crosstalk between mitochondrial dynamics and mitophagy. . Cell Death Differ. 28::82742
    [Crossref] [Google Scholar]
  24. 24.
    Ravikumar S, Baylon MG, Park SJ, Choi J. 2017.. Engineered microbial biosensors based on bacterial two-component systems as synthetic biotechnology platforms in bioremediation and biorefinery. . Microb. Cell Fact. 16::62
    [Crossref] [Google Scholar]
  25. 25.
    Vendrell-Fernández S, Lozano-Picazo P, Cuadros-Sánchez P, Tejero-Ojeda MM, Giraldo R. 2021.. Conversion of the OmpF porin into a device to gather amyloids on the E. coli outer membrane. . ACS Synth. Biol. 11::65567
    [Crossref] [Google Scholar]
  26. 26.
    Ilangumaran Ponmalar I, Sarangi NK, Basu JK, Ayappa KG. 2021.. Pore forming protein induced biomembrane reorganization and dynamics: a focused review. . Front. Mol. Biosci. 8::737561
    [Crossref] [Google Scholar]
  27. 27.
    Panchal R, Smart M, Bowser D, Williams D, Petrou S. 2002.. Pore-forming proteins and their application in biotechnology. . Curr. Pharm. Biotechnol. 3::99115
    [Crossref] [Google Scholar]
  28. 28.
    Vivier D, Bennis K, Lesage F, Ducki S. 2016.. Perspectives on the two-pore domain potassium channel TREK-1 (TWIK-related K+ channel 1). A novel therapeutic target?. J. Med. Chem. 59::514957
    [Crossref] [Google Scholar]
  29. 29.
    Shoshan-Barmatz V, De Pinto V, Zweckstetter M, Raviv Z, Keinan N, Arbel N. 2010.. VDAC, a multi-functional mitochondrial protein regulating cell life and death. . Mol. Aspects Med. 31::22785
    [Crossref] [Google Scholar]
  30. 30.
    Ollivier M, Beudez J, Linck N, Grutter T, Compan V, Rassendren F. 2021.. P2X-GCaMPs as versatile tools for imaging extracellular ATP signaling. . eNeuro 8::ENEURO.0185-20.2020
    [Crossref] [Google Scholar]
  31. 31.
    Labrou NE. 2014.. Protein purification: an overview. . In Protein Downstream Processing: Design, Development and Application of High and Low-Resolution Methods, ed. NE Labrou , pp. 310. Totowa, NJ:: Humana
    [Google Scholar]
  32. 32.
    Lin S-H, Guidotti G. 2009.. Purification of membrane proteins. . Methods Enzymol. 463::61929
    [Crossref] [Google Scholar]
  33. 33.
    Orwick-Rydmark M, Arnold T, Linke D. 2016.. The use of detergents to purify membrane proteins. . Curr. Protoc. Protein Sci. 84::4.8.135
    [Crossref] [Google Scholar]
  34. 34.
    Seddon AM, Curnow P, Booth PJ. 2004.. Membrane proteins, lipids and detergents: not just a soap opera. . Biochim. Biophys. Acta Biomembr. 1666::10517
    [Crossref] [Google Scholar]
  35. 35.
    Has C, Pan S. 2021.. Vesicle formation mechanisms: an overview. . J. Liposome Res. 31::90111
    [Crossref] [Google Scholar]
  36. 36.
    Seo H, Lee H. 2021.. Recent developments in microfluidic synthesis of artificial cell-like polymersomes and liposomes for functional bioreactors. . Biomicrofluidics 15::021301
    [Crossref] [Google Scholar]
  37. 37.
    Yandrapalli N, Petit J, Bäumchen O, Robinson T. 2021.. Surfactant-free production of biomimetic giant unilamellar vesicles using PDMS-based microfluidics. . Commun. Chem. 4::100
    [Crossref] [Google Scholar]
  38. 38.
    Kamiya K, Osaki T, Takeuchi S. 2021.. Formation of nano-sized lipid vesicles with asymmetric lipid components using a pulsed-jet flow method. . Sens. Actuators B Chem. 327::128917
    [Crossref] [Google Scholar]
  39. 39.
    Pautot S, Frisken BJ, Weitz D. 2003.. Production of unilamellar vesicles using an inverted emulsion. . Langmuir 19::287079
    [Crossref] [Google Scholar]
  40. 40.
    Zhang Y, Obuchi H, Toyota T. 2023.. A practical guide to preparation and applications of giant unilamellar vesicles formed via centrifugation of water-in-oil emulsion droplets. . Membranes 13::440
    [Crossref] [Google Scholar]
  41. 41.
    Olson F, Hunt CA, Szoka FC, Vail WJ, Papahadjopoulos D. 1979.. Preparation of liposomes of defined size distribution by extrusion through polycarbonate membranes. . Biochim. Biophys. Acta Biomembr. 557::923
    [Crossref] [Google Scholar]
  42. 42.
    Horger KS, Estes DJ, Capone R, Mayer M. 2009.. Films of agarose enable rapid formation of giant liposomes in solutions of physiologic ionic strength. . J. Am. Chem. Soc. 131::181019
    [Crossref] [Google Scholar]
  43. 43.
    Tsai F-C, Stuhrmann B, Koenderink GH. 2011.. Encapsulation of active cytoskeletal protein networks in cell-sized liposomes. . Langmuir 27::1006171
    [Crossref] [Google Scholar]
  44. 44.
    Hansen JS, Thompson JR, Hélix-Nielsen C, Malmstadt N. 2013.. Lipid directed intrinsic membrane protein segregation. . J. Am. Chem. Soc. 135::1729497
    [Crossref] [Google Scholar]
  45. 45.
    Weinberger A, Tsai F-C, Koenderink GH, Schmidt TF, Itri R, et al. 2013.. Gel-assisted formation of giant unilamellar vesicles. . Biophys. J. 105::15464
    [Crossref] [Google Scholar]
  46. 46.
    Deshpande S, Caspi Y, Meijering AE, Dekker C. 2016.. Octanol-assisted liposome assembly on chip. . Nat. Commun. 7::10447
    [Crossref] [Google Scholar]
  47. 47.
    Zhang Y, Murakami K, Borra VJ, Ozen MO, Demirci U, et al. 2022.. A label-free electrical impedance spectroscopy for detection of clusters of extracellular vesicles based on their unique dielectric properties. . Biosensors 12::104
    [Crossref] [Google Scholar]
  48. 48.
    Cha M, Jeong SH, Bae S, Park JH, Baeg Y, et al. 2023.. Efficient labeling of vesicles with lipophilic fluorescent dyes via the salt-change method. . Anal. Chem. 95::584349
    [Crossref] [Google Scholar]
  49. 49.
    Mousseau F, Berret J-F, Oikonomou EK. 2019.. Design and applications of a fluorescent labeling technique for lipid and surfactant preformed vesicles. . ACS Omega 4::1048593
    [Crossref] [Google Scholar]
  50. 50.
    Morla-Folch J, Vargas-Nadal G, Fuentes E, Illa-Tuset S, Köber M, et al. 2022.. Ultrabright Föster resonance energy transfer nanovesicles: the role of dye diffusion. . Chem. Mater. 34::851727
    [Crossref] [Google Scholar]
  51. 51.
    Woodley JM. 2008.. New opportunities for biocatalysis: making pharmaceutical processes greener. . Trends Biotechnol. 26::32127
    [Crossref] [Google Scholar]
  52. 52.
    Halevy R, Rozek A, Kolusheva S, Hancock RE, Jelinek R. 2003.. Membrane binding and permeation by indolicidin analogs studied by a biomimetic lipid/polydiacetylene vesicle assay. . Peptides 24::175361
    [Crossref] [Google Scholar]
  53. 53.
    Yadav MK, Kumar V, Singh B, Tiwari SK. 2017.. Phospholipid/polydiacetylene vesicle-based colorimetric assay for high-throughput screening of bacteriocins and halocins. . Appl. Biochem. Biotechnol. 182::14254
    [Crossref] [Google Scholar]
  54. 54.
    Chiu MH, Prenner EJ. 2011.. Differential scanning calorimetry: an invaluable tool for a detailed thermodynamic characterization of macromolecules and their interactions. . J. Pharm. Bioallied Sci. 3::39
    [Crossref] [Google Scholar]
  55. 55.
    Grieshaber D, MacKenzie R, Vörös J, Reimhult E. 2008.. Electrochemical biosensors: sensor principles and architectures. . Sensors 8::140058
    [Crossref] [Google Scholar]
  56. 56.
    Fletcher M, Zhu J, Rubio-Sánchez R, Sandler SE, Nahas KA, et al. 2022.. DNA-based optical quantification of ion transport across giant vesicles. . ACS Nano 16::1712838
    [Crossref] [Google Scholar]
  57. 57.
    Boyd MA, Davis AM, Chambers NR, Tran P, Prindle A, Kamat NP. 2021.. Vesicle-based sensors for extracellular potassium detection. . Cell. Mol. Bioeng. 14::45969
    [Crossref] [Google Scholar]
  58. 58.
    Górecki K, Hansen JS, Li P, Nayeri N, Lindkvist-Petersson K, Gourdon P. 2022.. Microfluidic-derived detection of protein-facilitated copper flux across lipid membranes. . Anal. Chem. 94::1183137
    [Crossref] [Google Scholar]
  59. 59.
    Zhang Z, Wang F, Chen X. 2019.. Recent advances in the development of polydiacetylene-based biosensors. . Chinese Chem. Lett. 30::174557
    [Crossref] [Google Scholar]
  60. 60.
    Jelinek R. 2006.. Polydiacetylene bio- and chemo-sensors. . In Encyclopedia of Analytical Chemistry: Applications, Theory and Instrumentation, ed. RA Meyers , pp. 124. New York:: Wiley Online Lib.
    [Google Scholar]
  61. 61.
    Yadav MK, Tiwari SK. 2021.. Polydiacetylene vesicles acting as colorimetric sensor for the detection of plantaricin LD1. . Anal. Biochem. 631::114368
    [Crossref] [Google Scholar]
  62. 62.
    Kim KW, Lee JM, Kwon YM, Choi T-Y, Kim JYH, et al. 2018.. Polyamine-functionalized polydiacetylene (PDA) vesicles for colorimetric sensing of carbon dioxide. . Macromol. Res. 26::28490
    [Crossref] [Google Scholar]
  63. 63.
    Rizo J, Südhof TC. 1998.. Mechanics of membrane fusion. . Nat. Struct. Biol. 5::83942
    [Crossref] [Google Scholar]
  64. 64.
    Lira RB, Robinson T, Dimova R, Riske KA. 2019.. Highly efficient protein-free membrane fusion: a giant vesicle study. . Biophys. J. 116::7991
    [Crossref] [Google Scholar]
  65. 65.
    Zhao J, Zhang Y, Zhang X, Li C, Du H, et al. 2022.. Mimicking cellular metabolism in artificial cells: universal molecule transport across the membrane through vesicle fusion. . Anal. Chem. 94::381118
    [Crossref] [Google Scholar]
  66. 66.
    Quinn SD, Dresser L, Graham S, Conteduca D, Shepherd J, Leake MC. 2022.. Crowding-induced morphological changes in synthetic lipid vesicles determined using smFRET. . Front. Bioeng. Biotechnol. 10::958026
    [Crossref] [Google Scholar]
  67. 67.
    Thorsteinsson K, Olsén E, Schmidt E, Pace H, Bally M. 2020.. FRET-based assay for the quantification of extracellular vesicles and other vesicles of complex composition. . Anal. Chem. 92::1533643
    [Crossref] [Google Scholar]
  68. 68.
    Huang H, Ge B, Zhang S, Li J, Sun C, et al. 2019.. Using fluorescence quenching titration to determine the orientation of a model transmembrane protein in mimic membranes. . Materials 12::349
    [Crossref] [Google Scholar]
  69. 69.
    Tashiro S, Kakimoto Y, Shinmyo M, Fujimoto S, Tamura Y. 2020.. Improved split-GFP systems for visualizing organelle contact sites in yeast and human cells. . Front. Cell Dev. Biol. 8::571388
    [Crossref] [Google Scholar]
  70. 70.
    Shimizu Y, Inoue A, Tomari Y, Suzuki T, Yokogawa T, et al. 2001.. Cell-free translation reconstituted with purified components. . Nat. Biotechnol. 19::75155
    [Crossref] [Google Scholar]
  71. 71.
    Borkowski O, Bricio C, Murgiano M, Rothschild-Mancinelli B, Stan G-B, Ellis T. 2018.. Cell-free prediction of protein expression costs for growing cells. . Nat. Commun. 9::1457
    [Crossref] [Google Scholar]
  72. 72.
    Manzer ZA, Selivanovitch E, Ostwalt AR, Daniel S. 2023.. Membrane protein synthesis: no cells required. . Trends Biochem. Sci. 48::64254
    [Crossref] [Google Scholar]
  73. 73.
    Mironov AS, Gusarov I, Rafikov R, Lopez LE, Shatalin K, et al. 2002.. Sensing small molecules by nascent RNA: a mechanism to control transcription in bacteria. . Cell 111::74756
    [Crossref] [Google Scholar]
  74. 74.
    Boyd MA, Thavarajah W, Lucks JB, Kamat NP. 2023.. Robust and tunable performance of a cell-free biosensor encapsulated in lipid vesicles. . Sci. Adv. 9::eadd6605
    [Crossref] [Google Scholar]
  75. 75.
    Martini L, Mansy SS. 2011.. Cell-like systems with riboswitch controlled gene expression. . Chem. Commun. 47::1073436
    [Crossref] [Google Scholar]
  76. 76.
    Adamala KP, Martin-Alarcon DA, Guthrie-Honea KR, Boyden ES. 2017.. Engineering genetic circuit interactions within and between synthetic minimal cells. . Nat. Chem. 9::43139
    [Crossref] [Google Scholar]
  77. 77.
    Lind TK, Cárdenas M. 2016.. Understanding the formation of supported lipid bilayers via vesicle fusion—a case that exemplifies the need for the complementary method approach. . Biointerphases 11::020801
    [Crossref] [Google Scholar]
  78. 78.
    Kurniawan J, Ventrici de Souza JF, Dang AT, Liu G-y, Kuhl TL. 2018.. Preparation and characterization of solid-supported lipid bilayers formed by Langmuir–Blodgett deposition: a tutorial. . Langmuir 34::1562239
    [Crossref] [Google Scholar]
  79. 79.
    Ferhan AR, Yoon BK, Park S, Sut TN, Chin H, et al. 2019.. Solvent-assisted preparation of supported lipid bilayers. . Nat. Protoc. 14::2091118
    [Crossref] [Google Scholar]
  80. 80.
    Chien Y-AA, Alford BK, Wasik BR, Weichert WS, Parrish CR, Daniel S. 2023.. Single particle analysis of H3N2 influenza entry differentiates the impact of the sialic acids (Neu5Ac and Neu5Gc) on virus binding and membrane fusion. . J. Virol. 97::e01463-22
    [Crossref] [Google Scholar]
  81. 81.
    Armistead FJ, Batchelor DV, Johnson BR, Evans SD. 2023.. QCM-D investigations on cholesterol–DNA tethering of liposomes to microbubbles for therapy. . J. Phys. Chem. B 127::246674
    [Crossref] [Google Scholar]
  82. 82.
    Kanazawa KK, Gordon J. 1985.. II. Frequency of a quartz microbalance in contact with liquid. . Anal. Chem 557::177172
    [Google Scholar]
  83. 83.
    Voinova MV, Rodahl M, Jonson M, Kasemo B. 1999.. Viscoelastic acoustic response of layered polymer films at fluid-solid interfaces: continuum mechanics approach. . Phys. Scr. 59::391
    [Crossref] [Google Scholar]
  84. 84.
    Cho N-J, Frank CW, Kasemo B, Höök F. 2010.. Quartz crystal microbalance with dissipation monitoring of supported lipid bilayers on various substrates. . Nat. Protoc. 5::1096106
    [Crossref] [Google Scholar]
  85. 85.
    Briand E, Zäch M, Svedhem S, Kasemo B, Petronis S. 2010.. Combined QCM-D and EIS study of supported lipid bilayer formation and interaction with pore-forming peptides. . Analyst 135::34350
    [Crossref] [Google Scholar]
  86. 86.
    Jonsson MP, Jönsson P, Höök F. 2008.. Simultaneous nanoplasmonic and quartz crystal microbalance sensing: analysis of biomolecular conformational changes and quantification of the bound molecular mass. . Anal. Chem. 80::798895
    [Crossref] [Google Scholar]
  87. 87.
    Weng KC, Kanter JL, Robinson WH, Frank CW. 2006.. Fluid supported lipid bilayers containing monosialoganglioside GM1: a QCM-D and FRAP study. . Colloids Surf. B Biointerfaces 50::7684
    [Crossref] [Google Scholar]
  88. 88.
    Mohamed Z, Shin J-H, Ghosh S, Sharma AK, Pinnock F, et al. 2021.. Clinically relevant bacterial outer membrane models for antibiotic screening applications. . ACS Infect. Dis. 7::270722
    [Crossref] [Google Scholar]
  89. 89.
    Ulmefors H, Nissa J, Pace H, Wahlsten O, Gunnarsson A, et al. 2021.. Formation of supported lipid bilayers derived from vesicles of various compositional complexity on conducting polymer/silica substrates. . Langmuir 37::5494505
    [Crossref] [Google Scholar]
  90. 90.
    Elnaggar M, Hasan ML, Bhang SH, Joung YK. 2021.. Endothelial cell–derived tethered lipid bilayers generating nitric oxide for endovascular implantation. . ACS Appl. Bio Mater. 4::638193
    [Crossref] [Google Scholar]
  91. 91.
    Kang JY, Yoon BK, Baek H, Ko Y, Bhang SH, et al. 2022.. Facile and scalable fabrication of exosome-mimicking nanovesicles through PEGylated lipid detergent–aided cell extrusion. . Nanoscale 14::1658189
    [Crossref] [Google Scholar]
  92. 92.
    Almeida-Marrero V, Bethlehem F, Longo S, Bertolino MC, Torres T, et al. 2022.. Tailored multivalent targeting of siglecs with photosensitizing liposome nanocarriers. . Angew. Chem. 134::e202206900
    [Crossref] [Google Scholar]
  93. 93.
    Nikoleli G-P, Siontorou CG, Nikolelis M-T, Bratakou S, Bendos DK. 2019.. Recent lipid membrane–based biosensing platforms. . Appl. Sci. 9::1745
    [Crossref] [Google Scholar]
  94. 94.
    Richards MJ, Hsia C-Y, Singh RR, Haider H, Kumpf J, et al. 2016.. Membrane protein mobility and orientation preserved in supported bilayers created directly from cell plasma membrane blebs. . Langmuir 32::296374
    [Crossref] [Google Scholar]
  95. 95.
    Floyd DL, Ragains JR, Skehel JJ, Harrison SC, van Oijen AM. 2008.. Single-particle kinetics of influenza virus membrane fusion. . PNAS 105::1538287
    [Crossref] [Google Scholar]
  96. 96.
    Lee SH, Lindquist NC, Wittenberg NJ, Jordan LR, Oh S-H. 2012.. Real-time full-spectral imaging and affinity measurements from 50 microfluidic channels using nanohole surface plasmon resonance. . Lab Chip 12::388290
    [Crossref] [Google Scholar]
  97. 97.
    Hinman SS, Ruiz CJ, Drakakaki G, Wilkop TE, Cheng Q. 2015.. On-demand formation of supported lipid membrane arrays by trehalose-assisted vesicle delivery for SPR imaging. . ACS Appl. Mater. Interfaces 7::1712230
    [Crossref] [Google Scholar]
  98. 98.
    Gritsch S, Nollert P, Jähnig F, Sackmann E. 1998.. Impedance spectroscopy of porin and gramicidin pores reconstituted into supported lipid bilayers on indium–tin-oxide electrodes. . Langmuir 14::311825
    [Crossref] [Google Scholar]
  99. 99.
    Wiegand G, Arribas-Layton N, Hillebrandt H, Sackmann E, Wagner P. 2002.. Electrical properties of supported lipid bilayer membranes. . J. Phys. Chem. B 106::424554
    [Crossref] [Google Scholar]
  100. 100.
    Kılıç A, Jadidi MF, Özer , Kök FN. 2017.. The effect of thiolated phospholipids on formation of supported lipid bilayers on gold substrates investigated by surface-sensitive methods. . Colloids Surf. B Biointerfaces 160::11725
    [Crossref] [Google Scholar]
  101. 101.
    Marquês JT, De Almeida RFM, Viana AS. 2014.. Lipid bilayers supported on bare and modified gold—formation, characterization and relevance of lipid rafts. . Electrochim. Acta 126::13950
    [Crossref] [Google Scholar]
  102. 102.
    Sessolo M, Khodagholy D, Rivnay J, Maddalena F, Gleyzes M, et al. 2013.. Easy-to-fabricate conducting polymer microelectrode arrays. . Adv. Mater. 25::213539
    [Crossref] [Google Scholar]
  103. 103.
    Rivnay J, Leleux P, Ferro M, Sessolo M, Williamson A, et al. 2015.. High-performance transistors for bioelectronics through tuning of channel thickness. . Sci. Adv. 1::e1400251
    [Crossref] [Google Scholar]
  104. 104.
    Zhang Y, Inal S, Hsia CY, Ferro M, Ferro M, et al. 2016.. Supported lipid bilayer assembly on PEDOT:PSS films and transistors. . Adv. Funct. Mater. 26::730413
    [Crossref] [Google Scholar]
  105. 105.
    Liu H-Y, Pappa A-M, Hidalgo TC, Inal S, Owens RM, Daniel S. 2020.. Biomembrane-based organic electronic devices for ligand–receptor binding studies. . Anal. Bioanal. Chem. 412::626573
    [Crossref] [Google Scholar]
  106. 106.
    Su H, Liu H-Y, Pappa A-M, Hidalgo TC, Cavassin P, et al. 2019.. Facile generation of biomimetic-supported lipid bilayers on conducting polymer surfaces for membrane biosensing. . ACS Appl. Mater. Interfaces 11::43799810
    [Crossref] [Google Scholar]
  107. 107.
    Liu H-Y, Pappa A-M, Pavia A, Pitsalidis C, Thiburce Q, et al. 2020.. Self-assembly of mammalian-cell membranes on bioelectronic devices with functional transmembrane proteins. . Langmuir 36::732531
    [Crossref] [Google Scholar]
  108. 108.
    Pappa A-M, Liu H-Y, Traberg-Christensen W, Thiburce Q, Savva A, et al. 2020.. Optical and electronic ion channel monitoring from native human membranes. . ACS Nano 14::1253845
    [Crossref] [Google Scholar]
  109. 109.
    Tang T, Savva A, Traberg WC, Xu C, Thiburce Q, et al. 2021.. Functional infectious nanoparticle detector: finding viruses by detecting their host entry functions using organic bioelectronic devices. . ACS Nano 15::1814252
    [Crossref] [Google Scholar]
  110. 110.
    Chao Z, Selivanovitch E, Kallitsis K, Lu Z, Pachaury A, et al. 2023.. Recreating the biological steps of viral infection on a bioelectronic platform to profile viral variants of concern. . bioRxiv 2023.11.11.566634. https://doi.org/10.1101/2023.11.11.566634
  111. 111.
    Rivnay J, Inal S, Collins BA, Sessolo M, Stavrinidou E, et al. 2016.. Structural control of mixed ionic and electronic transport in conducting polymers. . Nat. Commun. 7::11287
    [Crossref] [Google Scholar]
  112. 112.
    Tang T, Savva A, Traberg WC, Xu C, Thiburce Q, et al. 2021.. Functional infectious nanoparticle detector: finding viruses by detecting their host entry functions using organic bioelectronic devices. . ACS Nano 15::1814252
    [Crossref] [Google Scholar]
  113. 113.
    Haleem A, Javaid M, Singh RP, Suman R, Rab S. 2021.. Biosensors applications in medical field: a brief review. . Sens. Int. 2::100100
    [Crossref] [Google Scholar]
  114. 114.
    Jayanthi VSA, Das AB, Saxena U. 2017.. Recent advances in biosensor development for the detection of cancer biomarkers. . Biosens. Bioelectron. 91::1523
    [Crossref] [Google Scholar]
  115. 115.
    Yang G, Xiao Z, Tang C, Deng Y, Huang H, He Z. 2019.. Recent advances in biosensor for detection of lung cancer biomarkers. . Biosens. Bioelectron. 141::111416
    [Crossref] [Google Scholar]
  116. 116.
    Salek-Maghsoudi A, Vakhshiteh F, Torabi R, Hassani S, Ganjali MR, et al. 2018.. Recent advances in biosensor technology in assessment of early diabetes biomarkers. . Biosens. Bioelectron. 99::12235
    [Crossref] [Google Scholar]
  117. 117.
    Ouyang M, Tu D, Tong L, Sarwar M, Bhimaraj A, et al. 2021.. A review of biosensor technologies for blood biomarkers toward monitoring cardiovascular diseases at the point-of-care. . Biosens. Bioelectron. 171::112621
    [Crossref] [Google Scholar]
  118. 118.
    Soler M, Huertas CS, Lechuga LM. 2019.. Label-free plasmonic biosensors for point-of-care diagnostics: a review. . Expert Rev. Mol. Diagn. 19::7181
    [Crossref] [Google Scholar]
  119. 119.
    Luchini A, Vitiello G. 2020.. Mimicking the mammalian plasma membrane: an overview of lipid membrane models for biophysical studies. . Biomimetics 6::3
    [Crossref] [Google Scholar]
  120. 120.
    Carro AC, Damonte EB. 2013.. Requirement of cholesterol in the viral envelope for dengue virus infection. . Virus Res. 174::7887
    [Crossref] [Google Scholar]
  121. 121.
    Yang S-T, Kreutzberger AJ, Lee J, Kiessling V, Tamm LK. 2016.. The role of cholesterol in membrane fusion. . Chem. Phys. Lipids 199::13643
    [Crossref] [Google Scholar]
  122. 122.
    Park C, Kim E, Park G, Kim BC, Vellampatti S, et al. 2023.. Membrane rigidity-tunable fusogenic nanosensor for high throughput detection of fusion-competent influenza A virus. . Adv. Funct. Mater. 33::2214603
    [Crossref] [Google Scholar]
  123. 123.
    Rao VB, Rossmann MG. 2012.. Viral Molecular Machines. New York:: Springer
    [Google Scholar]
  124. 124.
    Ning B, Huang Z, Youngquist BM, Scott JW, Niu A, et al. 2021.. Liposome-mediated detection of SARS-CoV-2 RNA–positive extracellular vesicles in plasma. . Nat. Nanotechnol. 16::103944
    [Crossref] [Google Scholar]
  125. 125.
    Faizal NDFM, Amin MCIM. 2022.. Recent updates on liposomal formulations for detection, prevention and treatment of coronavirus disease (COVID-19). . Int. J. Pharm 630::122421
    [Crossref] [Google Scholar]
  126. 126.
    Murugathas T, Hamiaux C, Colbert D, Kralicek AV, Plank NO, Carraher C. 2020.. Evaluating insect odorant receptor display formats for biosensing using graphene field effect transistors. . ACS Appl. Electron. Mater. 2::361017
    [Crossref] [Google Scholar]
  127. 127.
    AminJafari A, Ghasemi S. 2020.. The possible of immunotherapy for COVID-19: a systematic review. . Int. Immunopharmacol. 83::106455
    [Crossref] [Google Scholar]
  128. 128.
    Batool R, Soler M, Colavita F, Fabeni L, Matusali G, Lechuga LM. 2023.. Biomimetic nanoplasmonic sensor for rapid evaluation of neutralizing SARS-CoV-2 monoclonal antibodies as antiviral therapy. . Biosens. Bioelectron. 226::115137
    [Crossref] [Google Scholar]
  129. 129.
    Zhou F, Pan W, Chang Y, Su X, Duan X, Xue Q. 2022.. A supported lipid bilayer–based lab-on-a-chip biosensor for the rapid electrical screening of coronavirus drugs. . ACS Sens. 7::208492
    [Crossref] [Google Scholar]
  130. 130.
    Şen Karaman D, Ercan UK, Bakay E, Topaloğlu N, Rosenholm JM. 2020.. Evolving technologies and strategies for combating antibacterial resistance in the advent of the postantibiotic era. . Adv. Funct. Mater. 30::1908783
    [Crossref] [Google Scholar]
  131. 131.
    Romanholo PV, Razzino CA, Raymundo-Pereira PA, Prado TM, Machado SA, Sgobbi LF. 2021.. Biomimetic electrochemical sensors: new horizons and challenges in biosensing applications. . Biosens. Bioelectron. 185::113242
    [Crossref] [Google Scholar]
  132. 132.
    Zhou J, Duan M, Huang D, Shao H, Zhou Y, Fan Y. 2022.. Label-free visible colorimetric biosensor for detection of multiple pathogenic bacteria based on engineered polydiacetylene liposomes. . J. Colloid Interface Sci. 606::168494
    [Crossref] [Google Scholar]
  133. 133.
    Bint E Naser SF, Su H, Liu H-Y, Manzer ZA, Chao Z, et al. 2021.. Detection of ganglioside-specific toxin binding with biomembrane-based bioelectronic sensors. . ACS Appl. Bio Mater. 4::794250
    [Crossref] [Google Scholar]
  134. 134.
    Ghosh S, Mohamed Z, Shin J-H, Naser SFBE, Bali K, et al. 2022.. Impedance sensing of antibiotic interactions with a pathogenic E. coli outer membrane supported bilayer. . Biosens. Bioelectron. 204::114045
    [Crossref] [Google Scholar]
  135. 135.
    Santajit S, Indrawattana N. 2016.. Mechanisms of antimicrobial resistance in ESKAPE pathogens. . Biomed. Res. Int. 2016::2475067
    [Crossref] [Google Scholar]
  136. 136.
    Karthik V, Karuna B, Kumar PS, Saravanan A, Hemavathy R. 2022.. Development of lab-on-chip biosensor for the detection of toxic heavy metals: a review. . Chemosphere 299::134427
    [Crossref] [Google Scholar]
  137. 137.
    Harms H, Wells MC, Van der Meer JR. 2006.. Whole-cell living biosensors—are they ready for environmental application?. Appl. Microbiol. Biotechnol. 70::27380
    [Crossref] [Google Scholar]
  138. 138.
    Gui Q, Lawson T, Shan S, Yan L, Liu Y. 2017.. The application of whole cell–based biosensors for use in environmental analysis and in medical diagnostics. . Sensors 17::1623
    [Crossref] [Google Scholar]
  139. 139.
    Gumpu MB, Sethuraman S, Krishnan UM, Rayappan JBB. 2015.. A review on detection of heavy metal ions in water—an electrochemical approach. . Sens. Actuators B Chem. 213::51533
    [Crossref] [Google Scholar]
  140. 140.
    Fuller R, Landrigan P, Balakrishnan K, Bathan G, Bose-O'Reilly S, et al. 2022.. Pollution and health: a progress update. . Lancet Planet. Health 6::e53547
    [Crossref] [Google Scholar]
  141. 141.
    Wang D-E, Wang Y, Tian C, Zhang L, Han X, et al. 2015.. Polydiacetylene liposome–encapsulated alginate hydrogel beads for Pb2+ detection with enhanced sensitivity. . J. Mater. Chem. A 3::2169098
    [Crossref] [Google Scholar]
  142. 142.
    Lim JW, Kim T-Y, Woo M-A. 2021.. Trends in sensor development toward next-generation point-of-care testing for mercury. . Biosens. Bioelectron. 183::113228
    [Crossref] [Google Scholar]
  143. 143.
    Zhang S, Shi B, Yang G. 2020.. A selective colorimetric sensor for Pb2+ detection by using phenylboronic acid functionalized polydiacetylene liposomes. . Macromol. Res. 28::5156
    [Crossref] [Google Scholar]
  144. 144.
    Chen S-W, Chen X, Li Y, Yang Y, Dong Y, et al. 2022.. Polydiacetylene-based colorimetric and fluorometric sensors for lead ion recognition. . RSC Adv. 12::2221018
    [Crossref] [Google Scholar]
  145. 145.
    De Leo V, Maurelli AM, Ingrosso C, Lupone F, Catucci L. 2021.. Easy preparation of liposome@PDA microspheres for fast and highly efficient removal of methylene blue from water. . Int. J. Mol. Sci. 22::11916
    [Crossref] [Google Scholar]
  146. 146.
    Annapure US, Sathyanarayana SR. 2023.. Liposomes as biosensors in the food sector. . In Liposomal Encapsulation in Food Science and Technology, ed. C Anandharamakrishnan, S Dutta , pp. 23954. Mumbai:: Academic
    [Google Scholar]
  147. 147.
    Shukla S, Haldorai Y, Hwang SK, Bajpai VK, Huh YS, Han Y-K. 2017.. Current demands for food-approved liposome nanoparticles in food and safety sector. . Front. Microbiol. 8::2398
    [Crossref] [Google Scholar]
  148. 148.
    Weston M, Mazur F, Chandrawati R. 2020.. Monitoring of food spoilage using polydiacetylene- and liposome-based sensors. . In Smart Sensors for Environmental and Medical Applications, ed. H Hallil, H Heidari , pp. 81102. Hoboken, NJ:: IEEE
    [Google Scholar]
  149. 149.
    Nie D, Guo D, Huang Q, Guo W, Wang J, et al. 2021.. A novel insight into fluorescent sensor for patulin detection using thiol-terminated liposomes with encapsulated coumarin-6 as signal probe. . Sens. Actuators B Chem. 345::130366
    [Crossref] [Google Scholar]
  150. 150.
    Yadav S, Nair SS, Sai V, Satija J. 2019.. Nanomaterials based optical and electrochemical sensing of histamine: progress and perspectives. . Food Res. Int. 119::99109
    [Crossref] [Google Scholar]
  151. 151.
    Dwidar M, Seike Y, Kobori S, Whitaker C, Matsuura T, Yokobayashi Y. 2019.. Programmable artificial cells using histamine-responsive synthetic riboswitch. . J. Am. Chem. Soc. 141::1110314
    [Crossref] [Google Scholar]
  152. 152.
    Bajpai VK, Oh C, Khan I, Haldorai Y, Gandhi S, et al. 2020.. Fluorescent immunoliposomal nanovesicles for rapid multi-well immuno-biosensing of histamine in fish samples. . Chemosphere 243::125404
    [Crossref] [Google Scholar]
  153. 153.
    Nikoleli G-P. 2020.. Advanced lipid based biosensors for food analysis. . Adv. Food Nutr. Res. 91::30121
    [Crossref] [Google Scholar]
  154. 154.
    Castellana ET, Cremer PS. 2006.. Solid supported lipid bilayers: from biophysical studies to sensor design. . Surf. Sci. Rep. 61::42944
    [Crossref] [Google Scholar]
  155. 155.
    Zhang L, Guo W, Lu Y. 2020.. Advances in cell-free biosensors: principle, mechanism, and applications. . Biotechnol. J. 15::2000187
    [Crossref] [Google Scholar]
  156. 156.
    Silverman AD, Karim AS, Jewett MC. 2020.. Cell-free gene expression: an expanded repertoire of applications. . Nat. Rev. Genet. 21::15170
    [Crossref] [Google Scholar]
  157. 157.
    Asadi K, Gholami A. 2021.. Virosome-based nanovaccines; a promising bioinspiration and biomimetic approach for preventing viral diseases: a review. . Int. J. Biol. Macromol. 182::64858
    [Crossref] [Google Scholar]
  158. 158.
    Wen KY, Cameron L, Chappell J, Jensen K, Bell DJ, et al. 2017.. A cell-free biosensor for detecting quorum sensing molecules in P. aeruginosa–infected respiratory samples. . ACS Synth. Biol. 6::2293301
    [Crossref] [Google Scholar]
  159. 159.
    Mayeux G, Gayet L, Liguori L, Odier M, Martin DK, et al. 2021.. Cell-free expression of the outer membrane protein OprF of Pseudomonas aeruginosa for vaccine purposes. . Life Sci. Alliance 4::202000958
    [Crossref] [Google Scholar]
  160. 160.
    Manzer ZA, Ghosh S, Jacobs ML, Krishnan S, Zipfel WR, et al. 2021.. Cell-free synthesis of a transmembrane mechanosensitive channel protein into a hybrid-supported lipid bilayer. . ACS Appl. Bio Mater. 4::310112
    [Crossref] [Google Scholar]
  161. 161.
    Bailey-Hytholt CM, Shen T-L, Nie B, Tripathi A, Shukla A. 2020.. Placental trophoblast–inspired lipid bilayers for cell-free investigation of molecular interactions. . ACS Appl. Mater. Interfaces 12::31099111
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-anchem-061622-042618
Loading
/content/journals/10.1146/annurev-anchem-061622-042618
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error