1932

Abstract

Despite tremendous gains over the past decade, methods for characterizing proteins have generally lagged behind those for nucleic acids, which are characterized by extremely high sensitivity, dynamic range, and throughput. However, the ability to directly characterize proteins at nucleic acid levels would address critical biological challenges such as more sensitive medical diagnostics, deeper protein quantification, large-scale measurement, and discovery of alternate protein isoforms and modifications and would open new paths to single-cell proteomics. In response to this need, there has been a push to radically improve protein sequencing technologies by taking inspiration from high-throughput nucleic acid sequencing, with a particular focus on developing practical methods for single-molecule protein sequencing (SMPS). SMPS technologies fall generally into three categories: sequencing by degradation (e.g., mass spectrometry or fluorosequencing), sequencing by transit (e.g., nanopores or quantum tunneling), and sequencing by affinity (as in DNA hybridization–based approaches). We describe these diverse approaches, which range from those that are already experimentally well-supported to the merely speculative, in this nascent field striving to reformulate proteomics.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-102121-103615
2022-05-09
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/biophys/51/1/annurev-biophys-102121-103615.html?itemId=/content/journals/10.1146/annurev-biophys-102121-103615&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Aebersold R, Mann M. 2003. Mass spectrometry-based proteomics. Nature 422:6928198–207
    [Google Scholar]
  2. 2.
    Alfaro JA, Bohländer P, Dai M, Filius M, Howard CJ et al. 2021. The emerging landscape of single-molecule protein sequencing technologies. Nat. Methods 18:6604–17
    [Google Scholar]
  3. 3.
    Asandei A, Schiopu I, Chinappi M, Seo CH, Park Y, Luchian T 2016. Electroosmotic trap against the electrophoretic force near a protein nanopore reveals peptide dynamics during capture and translocation. ACS Appl. Mater. Interfaces 8:2013166–79
    [Google Scholar]
  4. 4.
    Aubin-Tam M-E, Olivares AO, Sauer RT, Baker TA, Lang MJ 2011. Single-molecule protein unfolding and translocation by an ATP-fueled proteolytic machine. Cell 145:2257–67
    [Google Scholar]
  5. 5.
    Avrameas S. 1969. Coupling of enzymes to proteins with glutaraldehyde: use of the conjugates for the detection of antigens and antibodies. Immunochemistry 6:143–52
    [Google Scholar]
  6. 6.
    Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J et al. 2008. Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456:721853–59
    [Google Scholar]
  7. 7.
    Bloom S, Liu C, Kölmel DK, Qiao JX, Zhang Y et al. 2018. Decarboxylative alkylation for site-selective bioconjugation of native proteins via oxidation potentials. Nat. Chem. 10:2205–11
    [Google Scholar]
  8. 8.
    Borgo B, Havranek JJ. 2014. Motif-directed redesign of enzyme specificity. Protein Sci. 23:3312–20
    [Google Scholar]
  9. 9.
    Borgo B, Havranek JJ. 2015. Computer-aided design of a catalyst for Edman degradation utilizing substrate-assisted catalysis. Protein Sci. 24:4571–79
    [Google Scholar]
  10. 10.
    Brinkerhoff H, Kang ASW, Liu J, Aksimentiev A, Dekker C 2021. Infinite re-reading of single proteins at single-amino-acid resolution using nanopore sequencing. bioRxiv 2021.07.13.452225. https://doi.org/10.1101/2021.07.13.452225
    [Crossref]
  11. 11.
    Brodbelt JS. 2014. Photodissociation mass spectrometry: new tools for characterization of biological molecules. Chem. Soc. Rev. 43:82757–83
    [Google Scholar]
  12. 12.
    Brunner A-D, Thielert M, Vasilopoulou CG, Ammar C, Coscia F et al. 2021. Ultra-high sensitivity mass spectrometry quantifies single-cell proteome changes upon perturbation. bioRxiv 2020.12.22.423933. https://doi.org/10.1101/2020.12.22.423933
    [Crossref]
  13. 13.
    Burnette WN. 1981.. “ Western blotting”: electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal. Biochem. 112:2195–203
    [Google Scholar]
  14. 14.
    Bush J, Maulbetsch W, Lepoitevin M, Wiener B, Mihovilovic Skanata M et al. 2017. The nanopore mass spectrometer. Rev. Sci. Instrum. 88:11113307
    [Google Scholar]
  15. 15.
    Bustamante C, Alexander L, Maciuba K, Kaiser CM 2020. Single-molecule studies of protein folding with optical tweezers. Annu. Rev. Biochem. 89:443–70
    [Google Scholar]
  16. 16.
    Callahan N, Tullman J, Kelman Z, Marino J 2020. Strategies for development of a next-generation protein sequencing platform. Trends Biochem. Sci. 45:176–89
    [Google Scholar]
  17. 17.
    Cao C, Cirauqui N, Marcaida MJ, Buglakova E, Duperrex A et al. 2019. Single-molecule sensing of peptides and nucleic acids by engineered aerolysin nanopores. Nat. Commun. 10:4918
    [Google Scholar]
  18. 18.
    Chandrasekaran AR, Punnoose JA, Zhou L, Dey P, Dey BK, Halvorsen K. 2019. DNA nanotechnology approaches for microRNA detection and diagnosis. Nucleic Acids Res 47:2010489–505
    [Google Scholar]
  19. 19.
    Chen T, Ren L, Liu X, Zhou M, Li L et al. 2018. DNA nanotechnology for cancer diagnosis and therapy. Int. J. Mol. Sci. 19:61671
    [Google Scholar]
  20. 20.
    Cherf GM, Lieberman KR, Rashid H, Lam CE, Karplus K, Akeson M 2012. Automated forward and reverse ratcheting of DNA in a nanopore at 5-Å precision. Nat. Biotechnol. 30:4344–48
    [Google Scholar]
  21. 21.
    Cheung TK, Lee C-Y, Bayer FP, McCoy A, Kuster B, Rose CM. 2021. Defining the carrier proteome limit for single-cell proteomics. Nat. Methods 18:176–83
    [Google Scholar]
  22. 22.
    Chi Q, Yang Z, Xu K, Wang C, Liang H 2020. DNA nanostructure as an efficient drug delivery platform for immunotherapy. Front. Pharmacol. 10:1585
    [Google Scholar]
  23. 23.
    Chinappi M, Cecconi F. 2018. Protein sequencing via nanopore based devices: a nanofluidics perspective. J. Phys. Condens. Matter. 30:20204002
    [Google Scholar]
  24. 24.
    Clarke J, Wu H-C, Jayasinghe L, Patel A, Reid S, Bayley H 2009. Continuous base identification for single-molecule nanopore DNA sequencing. Nat. Nanotechnol. 4:4265–70
    [Google Scholar]
  25. 25.
    Dai M, Jungmann R, Yin P 2016. Optical imaging of individual biomolecules in densely packed clusters. Nat. Nanotechnol. 11:9798–807
    [Google Scholar]
  26. 26.
    de Lannoy C, Filius M, van Wee R, Joo C, de Ridder D. 2021. Evaluation of FRET X for single-molecule protein fingerprinting. bioRxiv 2021.06.30.450512. https://doi.org/10.1101/2021.06.30.450512
    [Crossref]
  27. 27.
    Di Ventra M, Taniguchi M. 2016. Decoding DNA, RNA and peptides with quantum tunnelling. Nat. Nanotechnol. 11:2117–26
    [Google Scholar]
  28. 28.
    Donis-Keller H, Maxam AM, Gilbert W. 1977. Mapping adenines, guanines, and pyrimidines in RNA. Nucleic Acids Res 4:82527–38
    [Google Scholar]
  29. 29.
    Edman P. 1949. A method for the determination of amino acid sequence in peptides. Arch. Biochem. 22:3475
    [Google Scholar]
  30. 30.
    Eid J, Fehr A, Gray J, Luong K, Lyle J et al. 2009. Real-time DNA sequencing from single polymerase molecules. Science 323:5910133–38
    [Google Scholar]
  31. 31.
    Filius M, Kim SH, Severins I, Joo C. 2021. High-resolution single-molecule FRET via DNA eXchange (FRET X). Nano Lett 21:73295–301
    [Google Scholar]
  32. 32.
    Free RB, Hazelwood LA, Sibley DR. 2009. Identifying novel protein-protein interactions using co-immunoprecipitation and mass spectroscopy. Curr. Protoc. Neurosci. 46:5.28.114
    [Google Scholar]
  33. 33.
    Gold L, Ayers D, Bertino J, Bock C, Bock A et al. 2010. Aptamer-based multiplexed proteomic technology for biomarker discovery. PLOS ONE 5:12e15004
    [Google Scholar]
  34. 34.
    Gopalkrishnan N, Punthambaker S, Schaus TE, Church GM, Yin P. 2020. A DNA nanoscope that identifies and precisely localizes over a hundred unique molecular features with nanometer accuracy. bioRxiv 2020.08.27.271072. https://doi.org/10.1101/2020.08.27.271072
    [Crossref]
  35. 35.
    Govindarajan R, Duraiyan J, Kaliyappan K, Palanisamy M. 2012. Microarray and its applications. J. Pharm. Bioallied Sci. 4:Suppl. 2S310–12
    [Google Scholar]
  36. 36.
    He P, Williams BA, Trout D, Marinov GK, Amrhein H et al. 2020. The changing mouse embryo transcriptome at whole tissue and single-cell resolution. Nature 583:7818760–67
    [Google Scholar]
  37. 37.
    Heather JM, Chain B. 2016. The sequence of sequencers: the history of sequencing DNA. Genomics 107:11–8
    [Google Scholar]
  38. 38.
    Heller MJ. 2002. DNA microarray technology: devices, systems, and applications. Annu. Rev. Biomed. Eng. 4:129–53
    [Google Scholar]
  39. 39.
    Hernandez ET, Swaminathan J, Marcotte EM, Anslyn EV. 2017. Solution-phase and solid-phase sequential, selective modification of side chains in KDYWEC and KDYWE as models for usage in single-molecule protein sequencing. New J. Chem. 41:2462–69
    [Google Scholar]
  40. 40.
    Houghtaling J, Ying C, Eggenberger OM, Fennouri A, Nandivada S et al. 2019. Estimation of shape, volume, and dipole moment of individual proteins freely transiting a synthetic nanopore. ACS Nano 13:55231–42
    [Google Scholar]
  41. 41.
    Howard CJ, Floyd BM, Bardo AM, Swaminathan J, Marcotte EM, Anslyn EV. 2020. Solid-phase peptide capture and release for bulk and single-molecule proteomics. ACS Chem. Biol. 15:61401–7
    [Google Scholar]
  42. 42.
    Hu Q, Li H, Wang L, Gu H, Fan C. 2019. DNA nanotechnology-enabled drug delivery systems. Chem. Rev. 119:106459–506
    [Google Scholar]
  43. 43.
    Hu Z-L, Huo M-Z, Ying Y-L, Long Y-T. 2021. Biological nanopore approach for single-molecule protein sequencing. Angew. Chem. Int. Ed. 60:2714738–49
    [Google Scholar]
  44. 44.
    Huang B, Wu H, Bhaya D, Grossman A, Granier S et al. 2007. Counting low-copy number proteins in a single cell. Science 315:580881–84
    [Google Scholar]
  45. 45.
    Huang G, Voet A, Maglia G. 2019. FraC nanopores with adjustable diameter identify the mass of opposite-charge peptides with 44 dalton resolution. Nat. Commun. 10:835
    [Google Scholar]
  46. 46.
    Huang G, Willems K, Bartelds M, van Dorpe P, Soskine M, Maglia G 2020. Electro-osmotic vortices promote the capture of folded proteins by PlyAB nanopores. Nano Lett. 20:53819–27
    [Google Scholar]
  47. 47.
    Jain M, Olsen HE, Paten B, Akeson M 2016. The Oxford Nanopore MinION: delivery of nanopore sequencing to the genomics community. Genome Biol 17:1239
    [Google Scholar]
  48. 48.
    Kaboord B, Perr M. 2008. Isolation of proteins and protein complexes by immunoprecipitation. Methods Mol. Biol. 424:349–64
    [Google Scholar]
  49. 49.
    Kafader JO, Melani RD, Senko MW, Makarov AA, Kelleher NL, Compton PD. 2019. Measurement of individual ions sharply increases the resolution of Orbitrap mass spectra of proteins. Anal. Chem. 91:42776–83
    [Google Scholar]
  50. 50.
    Kasianowicz JJ, Brandin E, Branton D, Deamer DW. 1996. Characterization of individual polynucleotide molecules using a membrane channel. PNAS 93:2413770–73
    [Google Scholar]
  51. 51.
    Keifer DZ, Jarrold MF. 2017. Single-molecule mass spectrometry. Mass Spectrom. Rev. 36:6715–33
    [Google Scholar]
  52. 52.
    Kennedy E, Dong Z, Tennant C, Timp G. 2016. Reading the primary structure of a protein with 0.07 nm3 resolution using a subnanometre-diameter pore. Nat. Nanotechnol. 11:11968–76
    [Google Scholar]
  53. 53.
    Kothapalli R, Yoder SJ, Mane S, Loughran TP. 2002. Microarray results: How accurate are they?. BMC Bioinform. 3:22
    [Google Scholar]
  54. 54.
    Kuchino Y, Nishimura S. 1989. Enzymatic RNA sequencing. Methods Enzymol 180:154–63
    [Google Scholar]
  55. 55.
    Laursen RA. 1971. Solid-phase Edman degradation. Eur. J. Biochem. 20:189–102
    [Google Scholar]
  56. 56.
    Li S, Wu X-Y, Li M-Y, Liu S-C, Ying Y-L, Long Y-T. 2020. T232K/K238Q aerolysin nanopore for mapping adjacent phosphorylation sites of a single tau peptide. Small Methods 4:112000014
    [Google Scholar]
  57. 57.
    Li SFY, Wu YS. 2000. Capillary electrophoresis. Encyclopedia of Separation Science ID Wilson 1176–87 Oxford, UK: Academic
    [Google Scholar]
  58. 58.
    Luo L, Boerwinkle E, Xiong M 2011. Association studies for next-generation sequencing. Genome Res 21:71099–108
    [Google Scholar]
  59. 59.
    MacDonald JI, Munch HK, Moore T, Francis MB 2015. One-step site-specific modification of native proteins with 2-pyridinecarboxyaldehydes. Nat. Chem. Biol. 11:5326–31
    [Google Scholar]
  60. 60.
    Mahdessian D, Cesnik AJ, Gnann C, Danielsson F, Stenström L et al. 2021. Spatiotemporal dissection of the cell cycle with single-cell proteogenomics. Nature 590:7847649–54
    [Google Scholar]
  61. 61.
    Maillard RA, Chistol G, Sen M, Righini M, Tan J et al. 2011. ClpX(P) generates mechanical force to unfold and translocate its protein substrates. Cell 145:3459–69
    [Google Scholar]
  62. 62.
    Mann M. 2016. The rise of mass spectrometry and the fall of Edman degradation. Clin. Chem. 62:1293–94
    [Google Scholar]
  63. 63.
    Manrao EA, Derrington IM, Laszlo AH, Langford KW, Hopper MK et al. 2012. Reading DNA at single-nucleotide resolution with a mutant MspA nanopore and phi29 DNA polymerase. Nat. Biotechnol. 30:4349–53
    [Google Scholar]
  64. 64.
    Marx V. 2019. A dream of single-cell proteomics. Nat. Methods 16:9809–12
    [Google Scholar]
  65. 65.
    Matheron L, van den Toorn H, Heck AJR, Mohammed S. 2014. Characterization of biases in phosphopeptide enrichment by Ti4+-immobilized metal affinity chromatography and TiO2 using a massive synthetic library and human cell digests. Anal. Chem. 86:168312–20
    [Google Scholar]
  66. 66.
    Maulbetsch W, Wiener B, Poole W, Bush J, Stein D. 2016. Preserving the sequence of a biopolymer's monomers as they enter an electrospray mass spectrometer. Phys. Rev. Appl. 6:5054006
    [Google Scholar]
  67. 67.
    Mereuta L, Roy M, Asandei A, Lee JK, Park Y et al. 2014. Slowing down single-molecule trafficking through a protein nanopore reveals intermediates for peptide translocation. Sci. Rep. 4:3885
    [Google Scholar]
  68. 68.
    Nivala J, Marks DB, Akeson M. 2013. Unfoldase-mediated protein translocation through an α-hemolysin nanopore. Nat. Biotechnol. 31:3247–50
    [Google Scholar]
  69. 69.
    Nivala J, Mulroney L, Li G, Schreiber J, Akeson M. 2014. Discrimination among protein variants using an unfoldase-coupled nanopore. ACS Nano 8:1212365–75
    [Google Scholar]
  70. 70.
    Ohayon S, Girsault A, Nasser M, Shen-Orr S, Meller A. 2019. Simulation of single-protein nanopore sensing shows feasibility for whole-proteome identification. PLOS Comput. Biol. 15:5e1007067
    [Google Scholar]
  71. 71.
    Ohshiro T, Tsutsui M, Yokota K, Furuhashi M, Taniguichi M, Kawai T 2014. Detection of post-translational modifications in single peptides using electron tunnelling currents. Nat. Nanotechnol. 9:10835–40
    [Google Scholar]
  72. 72.
    Ouldali H, Sarthak K, Ensslen T, Piguet F, Manivet P et al. 2020. Electrical recognition of the twenty proteinogenic amino acids using an aerolysin nanopore. Nat. Biotechnol. 38:2176–81
    [Google Scholar]
  73. 73.
    Palmblad M. 2021. Theoretical considerations for next-generation proteomics. J. Proteome Res. 20:63395–99
    [Google Scholar]
  74. 74.
    Petelski AA, Emmott E, Leduc A, Huffman RG, Specht H et al. 2021. Multiplexed single-cell proteomics using SCoPE2. bioRxiv 2021.03.12.435034. https://doi.org/10.1101/2021.03.12.435034
    [Crossref]
  75. 75.
    Piguet F, Ouldali H, Pastoriza-Gallego M, Manivet P, Pelta J, Oukhaled A 2018. Identification of single amino acid differences in uniformly charged homopolymeric peptides with aerolysin nanopore. Nat. Commun. 9:966
    [Google Scholar]
  76. 76.
    Ren R, Zhang Y, Nadappuram BP, Akpinar B, Klenerman D et al. 2017. Nanopore extended field-effect transistor for selective single-molecule biosensing. Nat. Commun. 8:586
    [Google Scholar]
  77. 77.
    Restrepo-Pérez L, Huang G, Bohländer PR, Worp N, Eelkema R et al. 2019. Resolving chemical modifications to a single amino acid within a peptide using a biological nanopore. ACS Nano 13:1213668–76
    [Google Scholar]
  78. 78.
    Restrepo-Pérez L, Joo C, Dekker C 2018. Paving the way to single-molecule protein sequencing. Nat. Nanotechnol. 13:9786–96
    [Google Scholar]
  79. 79.
    Restrepo-Pérez L, Wong CH, Maglia G, Dekker C, Joo C. 2019. Label-free detection of post-translational modifications with a nanopore. Nano Lett 19:117957–64
    [Google Scholar]
  80. 80.
    Riley NM, Coon JJ. 2016. Phosphoproteomics in the age of rapid and deep proteome profiling. Anal. Chem. 88:174–94
    [Google Scholar]
  81. 81.
    Rodriguez-Larrea D. 2021. Single-amino acid discrimination in proteins with homogeneous nanopore sensors and neural networks. Biosens. Bioelectron. 180:113108
    [Google Scholar]
  82. 82.
    Rodriguez-Larrea D, Bayley H. 2013. Multistep protein unfolding during nanopore translocation. Nat. Nanotechnol. 8:4288–95
    [Google Scholar]
  83. 83.
    Rodriques SG, Marblestone AH, Boyden ES. 2019. A theoretical analysis of single molecule protein sequencing via weak binding spectra. PLOS ONE 14:3e0212868
    [Google Scholar]
  84. 84.
    Rose RJ, Damoc E, Denisov E, Makarov A, Heck AJR 2012. High-sensitivity Orbitrap mass analysis of intact macromolecular assemblies. Nat. Methods 9:111084–86
    [Google Scholar]
  85. 85.
    Rozenblatt-Rosen O, Shin JW, Rood JE, Hupalowska A, Regev A, Heyn H 2021. Building a high-quality Human Cell Atlas. Nat. Biotechnol. 39:2149–53
    [Google Scholar]
  86. 86.
    Sampath G. 2015. Amino acid discrimination in a nanopore and the feasibility of sequencing peptides with a tandem cell and exopeptidase. RSC Adv 5:30694–700
    [Google Scholar]
  87. 87.
    Sanger F, Thompson EOP. 1953. The amino-acid sequence in the glycyl chain of insulin. 2. The investigation of peptides from enzymic hydrolysates. Biochem. J. 53:3366–74
    [Google Scholar]
  88. 88.
    Sanger F, Tuppy H. 1951. The amino-acid sequence in the phenylalanyl chain of insulin. 1. The identification of lower peptides from partial hydrolysates. Biochem. J. 49:4463–81
    [Google Scholar]
  89. 89.
    Schaus TE, Woo S, Xuan F, Chen X, Yin P 2017. A DNA nanoscope via auto-cycling proximity recording. Nat. Commun. 8:696
    [Google Scholar]
  90. 90.
    Schmid S, Stömmer P, Dietz H, Dekker C. 2021. Nanopore electro-osmotic trap for the label-free study of single proteins and their conformations. bioRxiv 2021.03.09.434634. https://doi.org/10.1101/2021.03.09.434634
    [Crossref]
  91. 91.
    Schnitzbauer J, Strauss MT, Schlichthaerle T, Schueder F, Jungmann R. 2017. Super-resolution microscopy with DNA-PAINT. Nat. Protoc. 12:61198–228
    [Google Scholar]
  92. 92.
    Smith RD, Cheng X, Brace JE, Hofstadler SA, Anderson GA. 1994. Trapping, detection and reaction of very large single molecular ions by mass spectrometry. Nature 369:6476137–39
    [Google Scholar]
  93. 93.
    Steen H, Mann M. 2004. The abc's (and xyz's) of peptide sequencing. Nat. Rev. Mol. Cell Biol. 5:9699–711
    [Google Scholar]
  94. 94.
    Storm AJ, Storm C, Chen J, Zandbergen H, Joanny J-F, Dekker C. 2005. Fast DNA translocation through a solid-state nanopore. Nano Lett 5:71193–97
    [Google Scholar]
  95. 95.
    Swaminathan J, Boulgakov AA, Hernandez ET, Bardo AM, Bachman JL et al. 2018. Highly parallel single-molecule identification of proteins in zeptomole-scale mixtures. Nat. Biotechnol. 36:111076–82
    [Google Scholar]
  96. 96.
    Swaminathan J, Boulgakov AA, Marcotte EM. 2015. A theoretical justification for single molecule peptide sequencing. PLOS Comput. Biol. 11:2e1004080
    [Google Scholar]
  97. 97.
    Takagi T, Suzuki M, Baba T, Minegishi K, Sasaki S. 1984. Complete amino acid sequence of amelogenin in developing bovine enamel. Biochem. Biophys. Res. Commun. 121:2592–97
    [Google Scholar]
  98. 98.
    Timp W, Timp G. 2020. Beyond mass spectrometry, the next step in proteomics. Sci. Adv. 6:2eaax8978
    [Google Scholar]
  99. 99.
    Towbin H, Staehelin T, Gordon J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. PNAS 76:94350–54
    [Google Scholar]
  100. 100.
    Tullman J, Callahan N, Ellington B, Kelman Z, Marino JP 2019. Engineering ClpS for selective and enhanced N-terminal amino acid binding. Appl. Microbiol. Biotechnol. 103:62621–33
    [Google Scholar]
  101. 101.
    van Ginkel J, Filius M, Szczepaniak M, Tulinski P, Meyer AS, Joo C. 2018. Single-molecule peptide fingerprinting. PNAS 115:133338–43
    [Google Scholar]
  102. 102.
    Wagner DE, Klein AM. 2020. Lineage tracing meets single-cell omics: opportunities and challenges. Nat. Rev. Genet. 21:7410–27
    [Google Scholar]
  103. 103.
    Wang L, Li PCH 2011. Microfluidic DNA microarray analysis: a review. Anal. Chim. Acta 687:112–27
    [Google Scholar]
  104. 104.
    Wang R, Gilboa T, Song J, Huttner D, Grinstaff MW, Meller A. 2018. Single-molecule discrimination of labeled DNAs and polypeptides using photoluminescent-free TiO2 nanopores. ACS Nano 12:1111648–56
    [Google Scholar]
  105. 105.
    Wei X, Ma D, Jing L, Wang LY, Wang X et al. 2020. Enabling nanopore technology for sensing individual amino acids by a derivatization strategy. J. Mater. Chem. B 8:316792–97
    [Google Scholar]
  106. 106.
    Wingren C. 2016. Antibody-based proteomics. Proteogenomics Á Végvári 163–79 Berlin: Springer
    [Google Scholar]
  107. 107.
    Wiśniewski JR, Zougman A, Nagaraj N, Mann M. 2009. Universal sample preparation method for proteome analysis. Nat. Methods 6:5359–62
    [Google Scholar]
  108. 108.
    Yalow RS, Berson SA. 1960. Immunoassay of endogenous plasma insulin in man. J. Clin. Investig. 39:1157–75
    [Google Scholar]
  109. 109.
    Yao Y, Docter M, van Ginkel J, de Ridder D, Joo C. 2015. Single-molecule protein sequencing through fingerprinting: computational assessment. Phys. Biol. 12:5055003
    [Google Scholar]
  110. 110.
    Yates JR, Ruse CI, Nakorchevsky A. 2009. Proteomics by mass spectrometry: approaches, advances, and applications. Annu. Rev. Biomed. Eng. 11:49–79
    [Google Scholar]
  111. 111.
    Yusko EC, Bruhn BR, Eggenberger OM, Houghtaling J, Rollings RC et al. 2017. Real-time shape approximation and fingerprinting of single proteins using a nanopore. Nat. Nanotechnol. 12:4360–67
    [Google Scholar]
  112. 112.
    Zhang L, Floyd BM, Chilamari M, Mapes J, Swaminathan J et al. 2021. Photoredox-catalyzed decarboxylative C-terminal differentiation for bulk and single molecule proteomics. bioRxiv 2021.07.08.451692. https://doi.org/10.1101/2021.07.08.451692
    [Crossref]
  113. 113.
    Zhang S, Huang G, Versloot R, Herwig BM, de Souza PCT et al. 2020. Bottom-up fabrication of a multi-component nanopore sensor that unfolds, processes and recognizes single proteins. bioRxiv 2020.12.04.411884. https://doi.org/10.1101/2020.12.04.411884
    [Crossref]
  114. 114.
    Zhao Y, Ashcroft B, Zhang P, Liu H, Sen S et al. 2014. Single-molecule spectroscopy of amino acids and peptides by recognition tunnelling. Nat. Nanotechnol. 9:6466–73
    [Google Scholar]
  115. 115.
    Zubarev RA. 2013. The challenge of the proteome dynamic range and its implications for in-depth proteomics. Proteomics 13:5723–26
    [Google Scholar]
  116. 116.
    Zwolak M, Di Ventra M. 2005. Electronic signature of DNA nucleotides via transverse transport. Nano Lett 5:3421–24
    [Google Scholar]
/content/journals/10.1146/annurev-biophys-102121-103615
Loading
/content/journals/10.1146/annurev-biophys-102121-103615
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