Skip to main content
SpringerLink
Log in

Lipid bilayer membrane technologies: A review on single-molecule studies of DNA sequencing by using membrane nanopores

  • Review Article
  • Published:
Microchimica Acta Aims and scope Submit manuscript

Abstract

Nanopores based on α-hemolysin and MspA represent attractive sensing platforms due to easy production and operation with relatively low background noise. Such characteristics make them highly favorable for sequencing nucleic acids. Artificial lipid bilayer membranes, also referred to as black lipid membranes, in conjunction with membrane nanopores, can be applied to both the detection and highly efficient sequencing of DNA on a single-molecule level. However, the inherently weak physical properties of the membrane have impeded progress in these areas. Current issues impeding the ultimate recognition of the artificial lipid bilayer as a viable platform for detection and sequencing of DNA include membrane stability, lifespan, and automation. This review (with 105 references) highlights attempts to improve the attributes of the artificial lipid bilayer membrane starting with an overview on the present state and limitations. The first main section covers lipid bilayer membranes (BLM) in general. The following section reviews the various kinds of lipid bilayer membrane platforms with subsections on polymer membranes, solid-supported membranes, hydrogel-encapsulated membranes, shippable and storable membrane platforms, and droplet interface bilayers. A further section covers engineered biological nanopore sensor applications using BLMs with subsections offering a comparative view of different DNA sequencing methods, a detailed look at DNA Sequencing by synthesis using alpha-hemolysin nanopores, sequencing by synthesis using the MspA nanopore and quadromer map, and on limitations of sequencing based on synthesis technology. We present an outlook at the end that discusses current research trends on single-molecule sequencing to highlight the significance of this technology and its potential in the medical and environmental fields.

Sequencing by Synthesis, a novel method of sequencing DNA, uses the αHL biological nanopore and the artificial lipid bilayer membrane platform. Polymer tags attached to nucleotides bind to the polymerase-primer–template complex and are characterized by the nanopore upon release.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Alberts B (2004) Essential cell biology, 2nd edn. Garland Science Pub, New York

    Google Scholar 

  2. Alberts B, Bray D, Hopkin K, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2013) Essential Cell Biology, 4th edn Taylor & Francis Group

    Google Scholar 

  3. Urban M, Tampé R (2016) Membranes on nanopores for multiplexed single-transporter analyses. Microchim Acta 183(3):965–971. doi:10.1007/s00604-015-1676-4

    Article  CAS  Google Scholar 

  4. Matthews B, Judy JW, Northrup MA, Jensen KF, Harrison DJ (2003) Towards a fully automated planar patch clamp based dose-response measurement system. International Conference on Miniaturized Chemical and BIochemical Analysis Systems

  5. Kay AR, Wong RKS (1986) Isolation of neurons suitable for patch-clamping from adult mammalian central nervous systems. J Neurosci Methods 16(3):227–238. doi:10.1016/0165-0270(86)90040-3

    Article  CAS  Google Scholar 

  6. Mueller P, Rudin DO, Ti Tien H, Wescott WC (1962) Reconstitution of cell membrane structure in vitro and its transformation into an excitable system. Nature 194(4832):979–980

    Article  CAS  Google Scholar 

  7. Coronado R (1986) Recent advances in planar phospholipid bilayer techniques for monitoring ION channels. Annu Rev Biophys Biophys Chem 15(1):259–277. doi:10.1146/annurev.bb.15.060186.001355

    Article  CAS  Google Scholar 

  8. Morera FJ, Vargas G, Gonzalez C, Rosenmann E, Latorre R (2007) Ion-channel reconstitution. Methods Mol Biol 400:571–585. doi:10.1007/978-1-59745-519-0_38

    Article  CAS  Google Scholar 

  9. Stevens CF (1986) Electrophysiological methods: ion channel reconstitution. Science 234(4779):1016. doi:10.1126/science.234.4779.1016

    Article  CAS  Google Scholar 

  10. Bakas L, Chanturiya A, Herlax V, Zimmerberg J (2006) Paradoxical lipid dependence of pores formed by the Escherichia coli Alpha-hemolysin in planar phospholipid bilayer membranes. Biophys J 91(10):3748–3755. doi:10.1529/biophysj.106.090019

    Article  CAS  Google Scholar 

  11. Cohen FS, Niles WD (1993) Reconstituting channels into planar membranes: a conceptual framework and methods for fusing vesicles to planar bilayer phospholipid membranes. Methods Enzymol 220:50–68

    Article  CAS  Google Scholar 

  12. Huang HW (1986) Deformation free energy of bilayer membrane and its effect on gramicidin channel lifetime. Biophys J 50(6):1061–1070

    Article  CAS  Google Scholar 

  13. Ladha S, Mackie AR, Harvey LJ, Clark DC, Lea EJ, Brullemans M, Duclohier H (1996) Lateral diffusion in planar lipid bilayers: a fluorescence recovery after photobleaching investigation of its modulation by lipid composition, cholesterol, or alamethicin content and divalent cations. Biophys J 71(3):1364–1373

    Article  CAS  Google Scholar 

  14. Schindler H (1989) Planar lipid-protein membranes: strategies of formation and of detecting dependencies of ion transport functions on membrane conditions. Methods Enzymol 171:225–253

    Article  CAS  Google Scholar 

  15. Bayley H (2006) Sequencing single molecules of DNA. Curr Opin Chem Biol 10(6):628–637. doi:10.1016/j.cbpa.2006.10.040

    Article  CAS  Google Scholar 

  16. Bayley H, Cremer PS (2001) Stochastic sensors inspired by biology. Nature 413(6852):226–230

    Article  CAS  Google Scholar 

  17. Blake S, Mayer T, Mayer M, Yang J (2006) Monitoring chemical reactions by using ion-channel-forming peptides. Chembiochem 7(3):433–435. doi:10.1002/cbic.200500532

    Article  CAS  Google Scholar 

  18. Schmidt J (2005) Stochastic sensors. J Mater Chem 15(8):831–840. doi:10.1039/B414551H

    Article  CAS  Google Scholar 

  19. Mirzabekov TA, Silberstein AY, Kagan BL (1999) Use of planar lipid bilayer membranes for rapid screening of membrane active compounds. Methods Enzymol 294:661–674

    Article  CAS  Google Scholar 

  20. Shim J, Gu L-Q (2012) Single-molecule investigation of G-quadruplex using a nanopore sensor. Methods 57(1):40–46

    Article  CAS  Google Scholar 

  21. Shim JW, Tan Q, Gu L-Q (2009) Single-molecule detection of folding and unfolding of the G-quadruplex aptamer in a nanopore nanocavity. Nucleic Acids Res 37(3):972–982

    Article  CAS  Google Scholar 

  22. Shim JW, Gu L-Q (2008) Encapsulating a single G-quadruplex aptamer in a protein nanocavity. J Phys Chem B 112(28):8354–8360

    Article  CAS  Google Scholar 

  23. Kasianowicz JJ, Brandin E, Branton D, Deamer DW (1996) Characterization of individual polynucleotide molecules using a membrane channel. Proc Natl Acad Sci U S A 93(24):13770–13773

    Article  CAS  Google Scholar 

  24. Nakane JJ, Akeson M, Marziali A (2003) Nanopore sensors for nucleic acid analysis. J Phys-Condens Mat 15(32):R1365–R1393

    Article  CAS  Google Scholar 

  25. Knoll W, Frank CW, Heibel C, Naumann R, Offenhäusser A, Rühe J, Schmidt EK, Shen WW, Sinner A (2000) Functional tethered lipid bilayers. Rev Mol Biotechnol 74(3):137–158. doi:10.1016/S1389-0352(00)00012-X

    Article  CAS  Google Scholar 

  26. Koper I (2007) Insulating tethered bilayer lipid membranes to study membrane proteins. Mol BioSyst 3(10):651–657. doi:10.1039/B707168J

    Article  Google Scholar 

  27. Römer W, Steinem C (2004) Impedance analysis and Single-Channel recordings on Nano-black lipid membranes based on porous alumina. Biophys J 86(2):955–965

    Article  Google Scholar 

  28. Costello RF, Peterson IR, Heptinstall J, Walton DJ (1999) Improved gel-protected bilayers. Biosens Bioelectron 14(3):265–271. doi:10.1016/S0956-5663(99)00003-2

    Article  CAS  Google Scholar 

  29. Ide T, Yanagida T (1999) An artificial lipid bilayer formed on an agarose-coated glass for simultaneous electrical and optical measurement of single ion channels. Biochem Biophys Res Commun 265(2):595–599. doi:10.1006/bbrc.1999.1720

    Article  CAS  Google Scholar 

  30. Jeon T-J, Malmstadt N, Schmidt JJ (2006) Hydrogel-encapsulated lipid membranes. J Am Chem Soc 128(1):42–43. doi:10.1021/ja056901v

    Article  CAS  Google Scholar 

  31. Jeon T-J, Malmstadt N, Schmidt J (2006) Mechanical studies of hydrogel encapsulated membranes MRS Proc 926. doi:10.1557/PROC-0926-CC04-03

  32. Jeon TJ, Malmstadt N, Schmidt JJ (2007) Creating conjugated hydrogel encapsulated membranes. Mater res Soc Symp Proc 950:0950-D0909-0901

  33. Malmstadt N, Jeon TJ, Schmidt JJ (2008) Long-lived planar lipid bilayer membranes anchored to an in situ polymerized hydrogel. Adv Mater 20(1):84–89. doi:10.1002/adma.200700810

    Article  CAS  Google Scholar 

  34. X-f K, Cheley S, Rice-Ficht AC, Bayley H (2007) A storable encapsulated bilayer Chip containing a single protein Nanopore. J Am Chem Soc 129(15):4701–4705. doi:10.1021/ja068654g

    Article  Google Scholar 

  35. Shim JW, Gu LQ (2007) Stochastic sensing on a modular chip containing a single-ion channel. Anal Chem 79(6):2207–2213

    Article  CAS  Google Scholar 

  36. Lieleg O, Baumgärtel RM, Bausch AR (2009) Selective filtering of particles by the extracellular matrix: an electrostatic bandpass. Biophys J 97(6):1569–1577. doi:10.1016/j.bpj.2009.07.009

    Article  CAS  Google Scholar 

  37. Schmidt J (2016) Membrane platforms for biological nanopore sensing and sequencing. Curr Opin Biotechnol 39:17–27. doi:10.1016/j.copbio.2015.12.015

    Article  CAS  Google Scholar 

  38. Guggenheim EA (1977) Thermodynamics: an advanced treatment for chemists and physicists, 6th edn. North-Holland Pub. Co., Amsterdam

    Google Scholar 

  39. Miller C (1986) Ion channel reconstitution. Plenum Press, New York

    Book  Google Scholar 

  40. Takagi M, Azuma K, Kishimoto U (1965) A new method for the formation of bilayer membranes in aqueous solutions. Annu Rep Biol Fac Sci Osaka 13:107–110

    CAS  Google Scholar 

  41. Montal M, Mueller P (1972) Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. Proc Natl Acad Sci U S A 69(12):3561–3566

    Article  CAS  Google Scholar 

  42. Pattus F, Desnuelle P, Verger R (1978) Spreading of liposomes at the air/water interface. Biochim Biophys Acta Biomembr 507(1):62–70. doi:10.1016/0005-2736(78)90374-7

    Article  CAS  Google Scholar 

  43. Schindler H (1979) Exchange and interactions between lipid layers at the surface of a liposome solution. Biochim Biophys Acta 555(2):316–336

    Article  CAS  Google Scholar 

  44. Schindler H (1980) Formation of planar bilayers from artificial or native membrane-vesicles. FEBS Lett 122(1):77–79

    Article  CAS  Google Scholar 

  45. Eriksson JC (1971) Thermodynamics of surface-phase systems. VI On the rigorous thermodynamics of insoluble surface films J Colloid Interface Sci 37(4):659–667. doi:10.1016/0021-9797(71)90344-4

    Article  CAS  Google Scholar 

  46. Phillips MC, Hauser H (1974) Spreading of solid glycerides and phospholipids at the air—water interface. J Colloid Interface Sci 49(1):31–39. doi:10.1016/0021-9797(74)90295-1

    Article  CAS  Google Scholar 

  47. Tajima K, Gershfeld NL (1978) Equilibrium studies of lecithin-cholesterol interactions. II. Phase relations in surface films: analysis of the "condensing" effect of cholesterol. Biophys J 22(3):489–500

    Article  CAS  Google Scholar 

  48. Nardin C, Thoeni S, Widmer J, Winterhalter M, Meier W (2000) Nanoreactors based on (polymerized) ABA-triblock copolymer vesicles. Chem Commun 15:1433–1434. doi:10.1039/B004280N

    Article  Google Scholar 

  49. Nardin C, Hirt T, Leukel J, Meier W (2000) Polymerized ABA triblock copolymer vesicles. Langmuir 16(3):1035–1041. doi:10.1021/la990951u

    Article  CAS  Google Scholar 

  50. Nardin C, Widmer J, Winterhalter M, Meier W (2001) Amphiphilic block copolymer nanocontainers as bioreactors. Eur Phys J E 4(4):403–410. doi:10.1007/s101890170095

    Article  CAS  Google Scholar 

  51. Nardin C, Meier W (2002) Hybrid materials from amphiphilic block copolymers and membrane proteins. Rev Mol Biotechnol 90(1):17–26. doi:10.1016/S1389-0352(01)00052-6

    Article  CAS  Google Scholar 

  52. Castellana ET, Cremer PS (2006) Solid supported lipid bilayers: from biophysical studies to sensor design. Surf Sci Rep 61(10):429–444. doi:10.1016/j.surfrep.2006.06.001

    Article  CAS  Google Scholar 

  53. Andersson J, Köper I (2016) Tethered and polymer supported bilayer lipid membranes: structure and function. Membranes 6(2). doi:10.3390/membranes6020030

  54. Bright LK, Baker CA, Bränström R, Saavedra SS, Aspinwall CA (2015) Methacrylate polymer scaffolding enhances the stability of suspended lipid bilayers for Ion Channel recordings and biosensor development. ACS Biomater Sci Eng 1(10):955–963. doi:10.1021/acsbiomaterials.5b00205

    Article  CAS  Google Scholar 

  55. Jeon T-J (2008) Development and characterization of biomimetic membrane architecture for single molecule sensors and electrophysiological studies. University of California, Los Angeles

    Google Scholar 

  56. Hemmatian Z, Keene S, Josberger E, Miyake T, Arboleda C, Soto-Rodríguez J, Baneyx F, Rolandi M (2016) Electronic control of H+ current in a bioprotonic device with gramicidin a and Alamethicin. Nat Commun 7:12981. doi:10.1038/ncomms12981 http://www.nature.com/articles/ncomms12981#supplementary-information

    Article  CAS  Google Scholar 

  57. Baumann P, Tanner P, Onaca O, Palivan CG (2011) Bio-decorated polymer membranes: a new approach in diagnostics and therapeutics. Polymers 3(1):173

    Article  CAS  Google Scholar 

  58. Schuster B, Sleytr UB (2014) Biomimetic interfaces based on S-layer proteins, lipid membranes and functional biomolecules. J R Soc Interface 11(96):20140232. doi:10.1098/rsif.2014.0232

    Article  Google Scholar 

  59. Cornell BA, Braach-Maksvytis VLB, King LG, Osman PDJ, Raguse B, Wieczorek L, Pace RJ (1997) A biosensor that uses ion-channel switches. Nature 387(6633):580–583 http://www.nature.com/nature/journal/v387/n6633/suppinfo/387580a0_S1.html

    Article  CAS  Google Scholar 

  60. Wagner ML, Tamm LK (2000) Tethered polymer-supported planar lipid bilayers for reconstitution of integral membrane proteins: silane-polyethyleneglycol-lipid as a cushion and covalent linker. Biophys J 79(3):1400–1414

    Article  CAS  Google Scholar 

  61. Su Z, Jiang Y, Velázquez-Manzanares M, Jay Leitch J, Kycia A, Lipkowski J (2013) Electrochemical and PM-IRRAS studies of floating lipid bilayers assembled at the au(111) electrode pre-modified with a hydrophilic monolayer. J Electroanal Chem 688:76–85. doi:10.1016/j.jelechem.2012.09.044

    Article  CAS  Google Scholar 

  62. Ibragimova S, Stibius K, Szewczykowski P, Perry M, Bohr H, Hélix-Nielsen C (2012) Hydrogels for in situ encapsulation of biomimetic membrane arrays. Polymer Adv Tech 23(2):182–189. doi:10.1002/pat.1850

    Article  CAS  Google Scholar 

  63. Majd S, Mayer M (2005) Hydrogel stamping of arrays of supported lipid bilayers with various lipid compositions for the screening of drug–membrane and protein–membrane interactions. Angew Chem Int Ed 44(41):6697–6700. doi:10.1002/anie.200502189

    Article  CAS  Google Scholar 

  64. Moran-Mirabal JM, Edel JB, Meyer GD, Throckmorton D, Singh AK, Craighead HG (2005) Micrometer-sized supported lipid bilayer arrays for bacterial toxin Binding studies through Total internal reflection fluorescence microscopy. Biophys J 89(1):296–305. doi:10.1529/biophysj.104.054346

    Article  CAS  Google Scholar 

  65. Suzuki H, Tabata KV, Noji H, Takeuchi S (2006) Highly reproducible method of planar lipid bilayer reconstitution in Polymethyl methacrylate microfluidic Chip. Langmuir 22(4):1937–1942. doi:10.1021/la052534p

    Article  CAS  Google Scholar 

  66. Malmstadt N, Nash MA, Purnell RF, Schmidt JJ (2006) Automated formation of lipid-bilayer membranes in a microfluidic device. Nano Lett 6(9):1961–1965

    Article  CAS  Google Scholar 

  67. Funakoshi K, Suzuki H, Takeuchi S (2006) Lipid bilayer formation by contacting monolayers in a microfluidic device for membrane protein analysis. Anal Chem 78(24):8169–8174. doi:10.1021/ac0613479

    Article  CAS  Google Scholar 

  68. Michelmann HW, Nayudu P (2006) Cryopreservation of human embryos. Cell Tissue Bank 7(2):135–141. doi:10.1007/s10561-005-0877-1

    Article  CAS  Google Scholar 

  69. Rubinsky B (2003) Principles of low temperature cell preservation. Heart Fail Rev 8(3):277–284

    Article  CAS  Google Scholar 

  70. Wolkers WF, Tablin F, Crowe JH (2002) From anhydrobiosis to freeze-drying of eukaryotic cells. Comp Biochem Physiol A Mol Integr Physiol 131(3):535–543. doi:10.1016/S1095-6433(01)00505-0

    Article  Google Scholar 

  71. Choi S, Yoon S, Ryu H, Kim SM, Jeon T-J (2016) Automated lipid bilayer membrane formation using a polydimethylsiloxane thin film. (113):e54258. doi:10.3791/54258

  72. Ryu H, Choi S, Park J, Yoo Y-E, Yoon JS, Seo YH, Kim Y-R, Kim SM, Jeon T-J (2014) Automated lipid membrane formation using a polydimethylsiloxane film for Ion Channel measurements. Anal Chem 86(18):8910–8915. doi:10.1021/ac501397t

    Article  CAS  Google Scholar 

  73. Tsofina LM, Liberman EA, Babakov AV (1966) Production of bimolecular protein-lipid membranes in aqueous solution. Nature 212(5063):681–683

    Article  CAS  Google Scholar 

  74. Poulos JL, Portonovo SA, Bang H, Schmidt JJ (2010) Automatable lipid bilayer formation and ion channel measurement using sessile droplets. J Phys Condens Matter 22(45):454105

    Article  CAS  Google Scholar 

  75. Thapliyal T, Poulos JL, Schmidt JJ (2011) Automated lipid bilayer and ion channel measurement platform. Biosens Bioelectron 26(5):2651–2654. doi:10.1016/j.bios.2010.01.017

    Article  CAS  Google Scholar 

  76. Acharya SA, Portman A, Salazar CS, Schmidt JJ (2013) Hydrogel-stabilized droplet bilayers for high speed solution exchange. Sci Rep 3:3139. doi:10.1038/srep03139 http://www.nature.com/articles/srep03139#supplementary-information

    Article  Google Scholar 

  77. Kawano R, Tsuji Y, Kamiya K, Kodama T, Osaki T, Miki N, Takeuchi S (2014) A portable lipid bilayer system for environmental sensing with a transmembrane protein. PLoS One 9(7):e102427. doi:10.1371/journal.pone.0102427

    Article  Google Scholar 

  78. Bayley H (2014) Nanopore sequencing: from imagination to reality. Clin Chem 61(1):25

    Article  Google Scholar 

  79. Schatz MC, Delcher AL, Salzberg SL (2010) Assembly of large genomes using second-generation sequencing. Genome Res 20(9):1165–1173. doi:10.1101/gr.101360.109

    Article  CAS  Google Scholar 

  80. Soon WW, Hariharan M, Snyder MP (2013) High-throughput sequencing for biology and medicine. Mol Sys Biol 9:640–640. doi:10.1038/msb.2012.61

    Article  Google Scholar 

  81. Eid J, Fehr A, Gray J, Luong K, Lyle J, Otto G, Peluso P, Rank D, Baybayan P, Bettman B, Bibillo A, Bjornson K, Chaudhuri B, Christians F, Cicero R, Clark S, Dalal R, deWinter A, Dixon J, Foquet M, Gaertner A, Hardenbol P, Heiner C, Hester K, Holden D, Kearns G, Kong X, Kuse R, Lacroix Y, Lin S, Lundquist P, Ma C, Marks P, Maxham M, Murphy D, Park I, Pham T, Phillips M, Roy J, Sebra R, Shen G, Sorenson J, Tomaney A, Travers K, Trulson M, Vieceli J, Wegener J, Wu D, Yang A, Zaccarin D, Zhao P, Zhong F, Korlach J, Turner S (2009) Real-time DNA sequencing from single polymerase molecules. Science 323(5910):133

    Article  CAS  Google Scholar 

  82. Korlach J, Bjornson KP, Chaudhuri BP, Cicero RL, Flusberg BA, Gray JJ, Holden D, Saxena R, Wegener J, Turner SW (2010) Chapter 20- real-time DNA sequencing from single polymerase molecules. In: Nils GW (ed) methods Enzymol, vol 472. Academic press, pp 431–455. doi:10.1016/S0076-6879(10)72001-2

  83. Manrao EA, Derrington IM, Laszlo AH, Langford KW, Hopper MK, Gillgren N, Pavlenok M, Niederweis M, Gundlach JH (2012) Reading DNA at single-nucleotide resolution with a mutant MspA nanopore and phi29 DNA polymerase. Nat Biotech 30(4):349–353. doi:10.1038/nbt.2171 http://www.nature.com/nbt/journal/v30/n4/abs/nbt.2171.html#supplementary-information

    Article  CAS  Google Scholar 

  84. Clarke J, Wu H-C, Jayasinghe L, Patel A, Reid S, Bayley H (2009) Continuous base identification for single-molecule nanopore DNA sequencing. Nat Nano 4(4):265–270 http://www.nature.com/nnano/journal/v4/n4/suppinfo/nnano.2009.12_S1.html

    Article  CAS  Google Scholar 

  85. Kumar S, Tao C, Chien M, Hellner B, Balijepalli A, Robertson JWF, Li Z, Russo JJ, Reiner JE, Kasianowicz JJ, Ju J (2012) PEG-labeled nucleotides and Nanopore detection for single molecule DNA sequencing by synthesis. Sci Rep 2:684. doi:10.1038/srep00684 http://www.nature.com/articles/srep00684#supplementary-information

    Google Scholar 

  86. Branton D, Deamer DW, Marziali A, Bayley H, Benner SA, Butler T, Di Ventra M, Garaj S, Hibbs A, Huang X, Jovanovich SB, Krstic PS, Lindsay S, Ling XS, Mastrangelo CH, Meller A, Oliver JS, Pershin YV, Ramsey JM, Riehn R, Soni GV, Tabard-Cossa V, Wanunu M, Wiggin M, Schloss JA (2008) The potential and challenges of nanopore sequencing. Nat Biotech 26(10):1146–1153

    Article  CAS  Google Scholar 

  87. Fuller CW, Kumar S, Porel M, Chien M, Bibillo A, Stranges PB, Dorwart M, Tao C, Li Z, Guo W, Shi S, Korenblum D, Trans A, Aguirre A, Liu E, Harada ET, Pollard J, Bhat A, Cech C, Yang A, Arnold C, Palla M, Hovis J, Chen R, Morozova I, Kalachikov S, Russo JJ, Kasianowicz JJ, Davis R, Roever S, Church GM, Ju J (2016) Real-time single-molecule electronic DNA sequencing by synthesis using polymer-tagged nucleotides on a nanopore array. Proc Natl Acad Sci U S A 113(19):5233–5238. doi:10.1073/pnas.1601782113

    Article  CAS  Google Scholar 

  88. Li J, Yu D, Zhao Q (2016) Solid-state nanopore-based DNA single molecule detection and sequencing. Microchim Acta 183(3):941–953. doi:10.1007/s00604-015-1542-4

    Article  CAS  Google Scholar 

  89. Feng Y, Zhang Y, Ying C, Wang D, Du C (2015) Nanopore-based fourth-generation DNA sequencing technology. Genomics, Proteomics & Bioinformatics 13(1):4–16. doi:10.1016/j.gpb.2015.01.009

    Article  Google Scholar 

  90. Shi J, Hou J, Fang Y (2016) Recent advances in nanopore-based nucleic acid analysis and sequencing. Microchim Acta 183(3):925–939. doi:10.1007/s00604-015-1503-y

    Article  CAS  Google Scholar 

  91. Gyarfas B, Olasagasti F, Benner S, Garalde D, Lieberman KR, Akeson M (2009) Mapping the position of DNA polymerase-bound DNA templates in a Nanopore at 5 Å resolution. ACS Nano 3(6):1457–1466. doi:10.1021/nn900303g

    Article  CAS  Google Scholar 

  92. Wilson NA, Abu-Shumays R, Gyarfas B, Wang H, Lieberman KR, Akeson M, Dunbar WB (2009) Electronic control of DNA polymerase Binding and unbinding to single DNA molecules. ACS Nano 3(4):995–1003. doi:10.1021/nn9000897

    Article  CAS  Google Scholar 

  93. Hurt N, Wang H, Akeson M, Lieberman KR (2009) Specific nucleotide Binding and rebinding to individual DNA polymerase complexes captured on a Nanopore. J Am Chem Soc 131(10):3772–3778. doi:10.1021/ja809663f

    Article  CAS  Google Scholar 

  94. Cherf GM, Lieberman KR, Rashid H, Lam CE, Karplus K, Akeson M (2012) Automated forward and reverse ratcheting of DNA in a Nanopore at five angstrom precision(). Nat Biotech 30(4):344–348. doi:10.1038/nbt.2147

    Article  CAS  Google Scholar 

  95. Lieberman KR, Cherf GM, Doody MJ, Olasagasti F, Kolodji Y, Akeson M (2010) Processive replication of single DNA molecules in a Nanopore catalyzed by phi29 DNA polymerase. J Am Chem Soc 132(50):17961–17972. doi:10.1021/ja1087612

    Article  CAS  Google Scholar 

  96. Blanco L, Bernad A, Lazaro JM, Martin G, Garmendia C, Salas M (1989) Highly efficient DNA synthesis by the phage phi 29 DNA polymerase. Symmetrical mode of DNA replication. J Biol Chem 264(15):8935–8940

    CAS  Google Scholar 

  97. Lallana E, Riguera R, Fernandez-Megia E (2011) Reliable and efficient procedures for the conjugation of biomolecules through Huisgen Azide–alkyne cycloadditions. Angew Chem Int Ed 50(38):8794–8804. doi:10.1002/anie.201101019

    Article  CAS  Google Scholar 

  98. Movileanu L, Cheley S, Howorka S, Braha O, Bayley H (2001) Location of a constriction in the lumen of a transmembrane pore by targeted covalent attachment of polymer molecules. J Gen Physiol 117(3):239–252

    Article  CAS  Google Scholar 

  99. Stoddart D, Heron AJ, Mikhailova E, Maglia G, Bayley H (2009) Single-nucleotide discrimination in immobilized DNA oligonucleotides with a biological nanopore. Proc Natl Acad Sci U S A 106(19):7702–7707. doi:10.1073/pnas.0901054106

    Article  CAS  Google Scholar 

  100. Yusko EC, Johnson JM, Majd S, Prangkio P, Rollings RC, Li J, Yang J, Mayer M (2011) Controlling protein translocation through nanopores with bio-inspired fluid walls. Nat Nano 6(4):253–260 http://www.nature.com/nnano/journal/v6/n4/abs/nnano.2011.12.html#supplementary-information

    Article  CAS  Google Scholar 

  101. Manrao EA, Derrington IM, Pavlenok M, Niederweis M, Gundlach JH (2011) Nucleotide discrimination with DNA immobilized in the MspA Nanopore. PLoS One 6(10):e25723. doi:10.1371/journal.pone.0025723

    Article  CAS  Google Scholar 

  102. Laszlo AH, Derrington IM, Ross BC, Brinkerhoff H, Adey A, Nova IC, Craig JM, Langford KW, Samson JM, Daza R, Doering K, Shendure J, Gundlach JH (2014) Decoding long nanopore sequencing reads of natural DNA. Nat Biotech 32(8):829–833. doi:10.1038/nbt.2950 http://www.nature.com/nbt/journal/v32/n8/abs/nbt.2950.html#supplementary-information

    Article  CAS  Google Scholar 

  103. Bashir A, Klammer A, Robins WP, Chin C-S, Webster D, Paxinos E, Hsu D, Ashby M, Wang S, Peluso P, Sebra R, Sorenson J, Bullard J, Yen J, Valdovino M, Mollova E, Luong K, Lin S, LaMay B, Joshi A, Rowe L, Frace M, Tarr CL, Turnsek M, Davis BM, Kasarskis A, Mekalanos JJ, Waldor MK, Schadt EE (2012) A hybrid approach for the automated finishing of bacterial genomes. Nat Biotech 30(7):701–707. doi:10.1038/nbt.2288

    Article  CAS  Google Scholar 

  104. Koren S, Schatz MC, Walenz BP, Martin J, Howard JT, Ganapathy G, Wang Z, Rasko DA, McCombie WR, Jarvis ED, Phillippy AM (2012) Hybrid error correction and de novo assembly of single-molecule sequencing reads. Nat Biotech 30(7):693–700 http://www.nature.com/nbt/journal/v30/n7/abs/nbt.2280.html#supplementary-information

    Article  CAS  Google Scholar 

  105. Ribeiro FJ, Przybylski D, Yin S, Sharpe T, Gnerre S, Abouelleil A, Berlin AM, Montmayeur A, Shea TP, Walker BJ, Young SK, Russ C, Nusbaum C, MacCallum I, Jaffe DB (2012) Finished bacterial genomes from shotgun sequence data. Genome Res 22(11):2270–2277. doi:10.1101/gr.141515.112

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Rowan University Startup Fund, Pioneer Research Center Program (NRF-2012-0009575) and National Research Foundation Grants (NRF-2017R1A2B4002523, NRF-2016R1A2B4006987, and NRF-2016K2A9A2A10005545) from National Research Foundation of Korea. This work was also partially supported by Inha University WCSL Research Grant, Korea.

Author information

Authors and Affiliations

  1. Department of Biomedical Engineering, Henry M. Rowan College of Engineering, Rowan University, 201 Mullica Hill Road, Glassboro, NJ, 08028, USA

    Julian Bello & Jiwook Shim

  2. Institute of Life Sciences and Resources & Department of Food Science and Biotechnology, Kyung Hee University, 1732 Deogyeong-daero, Giheung-gu, Yongin-si, 17104, Republic of Korea

    Young-Rok Kim

  3. Department of Mechanical Engineering, Inha University, 100 Inharo, Nam-gu, Incheon, 22212, Republic of Korea

    Sun Min Kim

  4. WCSL of Integrated Human Airway-on-a-Chip, Inha University, 100 Inharo, Nam-gu, Incheon, 22212, South Korea

    Sun Min Kim & Tae-Joon Jeon

  5. Biohybrid Systems Research Center (BSRC), Inha University, 100 Inharo, Nam-gu, Incheon, 22212, South Korea

    Sun Min Kim & Tae-Joon Jeon

  6. Department of Biological Engineering, Inha University, 100 Inharo, Nam-gu, Incheon, 22212, Republic of Korea

    Tae-Joon Jeon

Authors
  1. Julian Bello
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Young-Rok Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sun Min Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tae-Joon Jeon
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jiwook Shim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Tae-Joon Jeon or Jiwook Shim.

Ethics declarations

The authors declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bello, J., Kim, YR., Kim, S.M. et al. Lipid bilayer membrane technologies: A review on single-molecule studies of DNA sequencing by using membrane nanopores. Microchim Acta 184, 1883–1897 (2017). https://doi.org/10.1007/s00604-017-2321-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00604-017-2321-1

Keywords

Search

Navigation