1932

Abstract

Nature has evolved a wide range of strategies to create self-assembled protein nanostructures with structurally defined architectures that serve a myriad of highly specialized biological functions. With the advent of biological tools for site-specific protein modifications and de novo protein design, a wide range of customized protein nanocarriers have been created using both natural and synthetic biological building blocks to mimic these native designs for targeted biomedical applications. In this review, different design frameworks and synthetic decoration strategies for achieving these functional protein nanostructures are summarized. Key attributes of these designer protein nanostructures, their unique functions, and their impact on biosensing and therapeutic applications are discussed.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-chembioeng-101519-121526
2020-06-07
2024-06-23
Loading full text...

Full text loading...

/deliver/fulltext/chembioeng/11/1/annurev-chembioeng-101519-121526.html?itemId=/content/journals/10.1146/annurev-chembioeng-101519-121526&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Zhang Y, Chan HF, Leong KW 2013. Advanced materials and processing for drug delivery: the past and the future. Adv. Drug Deliv. Rev. 65:104–20
    [Google Scholar]
  2. 2. 
    Papapostolou D, Howorka S. 2009. Engineering and exploiting protein assemblies in synthetic biology. Mol. BioSyst. 5:723–32
    [Google Scholar]
  3. 3. 
    Qi Y, Ge H. 2006. Modularity and dynamics of cellular networks. PLOS Comput. Biol. 2:e174
    [Google Scholar]
  4. 4. 
    Sowmya G, Breen EJ, Ranganathan S 2015. Linking structural features of protein complexes and biological function. Protein Sci 24:1486–94
    [Google Scholar]
  5. 5. 
    Mallagaray A, Creutznacher R, Dülfer J, Mayer PHO, Grimm LL et al. 2019. A post-translational modification of human Norovirus capsid protein attenuates glycan binding. Nat. Commun. 10:1320
    [Google Scholar]
  6. 6. 
    Roos WH, Ivanovska IL, Evilevitch A, Wuite GJ 2007. Viral capsids: mechanical characteristics, genome packaging and delivery mechanisms. Cell. Mol. Life Sci. 64:1484–97
    [Google Scholar]
  7. 7. 
    Chen Q, Sun Q, Molino NM, Wang S-W, Boder ET, Chen W 2015. Sortase A-mediated multi-functionalization of protein nanoparticles. Chem. Commun. 51:12107–10
    [Google Scholar]
  8. 8. 
    Raeeszadeh-Sarmazdeh M, Hartzell E, Price JV, Chen W 2016. Protein nanoparticles as multifunctional biocatalysts and health assessment sensors. Curr. Opin. Chem. Eng. 13:109–18
    [Google Scholar]
  9. 9. 
    Jordan PC, Patterson DP, Saboda KN, Edwards EJ, Miettinen HM et al. 2015. Self-assembling biomolecular catalysts for hydrogen production. Nat. Chem. 8:179–85
    [Google Scholar]
  10. 10. 
    Sun Q, Chen Q, Blackstock D, Chen W 2015. Post-translational modification of bionanoparticles as a modular platform for biosensor assembly. ACS Nano 9:8554–61
    [Google Scholar]
  11. 11. 
    Lieser RM, Chen W, Sullivan MO 2019. Controlled epidermal growth factor receptor ligand display on cancer suicide enzymes via unnatural amino acid engineering for enhanced intracellular delivery in breast cancer cells. Bioconjugate Chem 30:432–42
    [Google Scholar]
  12. 12. 
    Rohovie M, Nagasawa M, Swartz J 2017. Virus-like particles: next-generation nanoparticles for targeted therapeutic delivery. Bioeng. Transl. Med. 2:43–57
    [Google Scholar]
  13. 13. 
    Veronese FM, Mero A. 2008. The impact of PEGylation on biological therapies. BioDrugs 22:315–29
    [Google Scholar]
  14. 14. 
    Mao HY, Hart SA, Schink A, Pollok BA 2004. Sortase-mediated protein ligation: a new method for protein engineering. J. Am. Chem. Soc. 126:2670–71
    [Google Scholar]
  15. 15. 
    Swartz AR, Chen W. 2018. SpyTag/SpyCatcher functionalization of E2 nanocages with stimuli-responsive Z-ELP affinity domains for tunable monoclonal antibody binding and precipitation properties. Bioconjugate Chem 29:3113–21
    [Google Scholar]
  16. 16. 
    Cristie-David AS, Sciore A, Badieyan S, Escheweiler JD, Koldewey P et al. 2017. Evaluation of de novo-designed coiled coils as off-the-shelf components for protein assembly. Mol. Syst. Des. Eng. 2:140–48
    [Google Scholar]
  17. 17. 
    Patterson DP, Prevelige PE, Douglas T 2012. Nanoreactors by programmed enzyme encapsulation inside the capsid of the bacteriophage P22. ACS Nano 6:5000–9
    [Google Scholar]
  18. 18. 
    Chen RP, Blackstock D, Sun Q, Chen W 2018. Dynamic protein assembly by programmable DNA strand displacement. Nat. Chem. 10:474–81
    [Google Scholar]
  19. 19. 
    Heddle J, Chakraborti S, Iwasaki K 2017. Natural and artificial protein cages: design, structure and therapeutic applications. Curr. Opin. Struct. Biol. 43:148–55
    [Google Scholar]
  20. 20. 
    Aniagyei S, DuFort C, Kao C, Dragnea B 2008. Self-assembly approaches to nanomaterial encapsulation in viral protein cages. J. Mater. Chem. 18:3763–74
    [Google Scholar]
  21. 21. 
    Lee E, Lee S, Kang Y, Ryu J, Kwon K et al. 2015. Engineered proteinticles for targeted delivery of siRNA to cancer cells. Adv. Funct. Mater. 25:1279–86
    [Google Scholar]
  22. 22. 
    Wen A, Steinmetz N. 2016. Design of virus-based nanomaterials for medicine, biotechnology, and energy. Chem. Soc. Rev. 45:4074–126
    [Google Scholar]
  23. 23. 
    Brown S, Fiedler J, Finn M 2009. Assembly of hybrid bacteriophage Qβ virus-like particles. Biochemistry 48:11155–57
    [Google Scholar]
  24. 24. 
    Bundy B, Swartz J. 2011. Efficient disulfide bond formation in virus-like particles. J. Biotechnol. 154:230–39
    [Google Scholar]
  25. 25. 
    Patterson DP, Schwarz B, Waters RS, Gedeon T, Douglas T 2014. Encapsulation of an enzyme cascade within the bacteriophage P22 virus-like particle. ACS Chem. Biol. 9:359–65
    [Google Scholar]
  26. 26. 
    Brasino M, Lee JH, Cha JN 2015. Creating highly amplified enzyme-linked immunosorbent assay signals from genetically engineered bacteriophage. Anal. Biochem. 470:7–13
    [Google Scholar]
  27. 27. 
    Glasgow J, Tullman-Ercek D. 2014. Production and applications of engineered viral capsids. Appl. Microbiol. Biotechnol. 98:5847–58
    [Google Scholar]
  28. 28. 
    Walker A, Skamel C, Nassal M 2011. SplitCore: an exceptionally versatile viral nanoparticle for native whole protein display regardless of 3D structure. Sci. Rep. 1:5
    [Google Scholar]
  29. 29. 
    Schoonen L, Eising S, van Eldijk MB, Bresseleers J, van der Pijl M et al. 2018. Modular, bioorthogonal strategy for the controlled loading of cargo into a protein nanocage. Bioconjugate Chem 29:1186–93
    [Google Scholar]
  30. 30. 
    Lee EJ, Lee E, Kim HJ, Lee JH, Ahn KY et al. 2014. Self-assembled proteinticle nanostructures for 3-dimensional display of antibodies. Nanoscale 6:14919–25
    [Google Scholar]
  31. 31. 
    Harrison P, Arosio P. 1996. Ferritins: molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Acta 1275:161–203
    [Google Scholar]
  32. 32. 
    Lee E, Lee N, Kim I 2016. Bioengineered protein-based nanocage for drug delivery. Adv. Drug Deliv. Rev. 106:157–71
    [Google Scholar]
  33. 33. 
    Jakob U, Gaestel M, Engel K, Buchner J 1993. Small heat-shock proteins are molecular chaperones. J. Biol. Chem. 268:1517–20
    [Google Scholar]
  34. 34. 
    Kim K, Kim R, Kim S 1998. Crystal structure of a small heat-shock protein. Nature 394:595–99
    [Google Scholar]
  35. 35. 
    Murata M, Narahara S, Kawano T, Hamano N, Piao J et al. 2015. Design and function of engineered protein nanocages as a drug delivery system for targeting pancreatic cancer cells via neuropilin-1. Mol. Pharm. 12:1422–30
    [Google Scholar]
  36. 36. 
    Swartz AR, Sun Q, Chen W 2017. Ligand-induced cross-linking of Z-elastin-like polypeptide-functionalized E2 protein nanoparticles for enhanced affinity precipitation of antibodies. Biomacromolecules 18:1654–59
    [Google Scholar]
  37. 37. 
    Bhaskar S, Lim S. 2017. Engineering protein nanocages as carriers for biomedical applications. NPG Asia Mater 9:e371
    [Google Scholar]
  38. 38. 
    Padilla JE, Colovos C, Yeates TO 2001. Nanohedra: using symmetry to design self assembling protein cages, layers, crystals, and filaments. PNAS 98:2217–21
    [Google Scholar]
  39. 39. 
    Sinclair JC, Davies KM, Venien-Bryan C, Noble MEM 2011. Generation of protein lattices by fusing proteins with matching rotational symmetry. Nat. Nano 6:558–62
    [Google Scholar]
  40. 40. 
    King NP, Bale JB, Sheffler W, McNamara DE, Gonen S et al. 2014. Accurate design of co-assembling multi-component protein nanomaterials. Nature 510:103–8
    [Google Scholar]
  41. 41. 
    Sugimoto K, Kanamaru S, Iwasaki K, Arisaka F, Yamashita I 2006. Construction of a ball-and-spike protein supramolecule. Angew. Chem. 45:2725–28
    [Google Scholar]
  42. 42. 
    Lai Y-T, Reading E, Hura GL, Tsai K-L, Laganowsky A et al. 2014. Structure of a designed protein cage that self-assembles into a highly porous cube. Nat. Chem. 6:1065–71
    [Google Scholar]
  43. 43. 
    Gradisar H, Bozic S, Doles T, Vengust D, Hafner-Bratkovic I et al. 2013. Design of a single-chain polypeptide tetrahedron assembled from coiled-coil segments. Nat. Chem. Biol. 9:362–66
    [Google Scholar]
  44. 44. 
    Sciore A, Su M, Koldewey P, Eschweiler JD, Diffley KA et al. 2016. Flexible, symmetry-directed approach to assembling protein cages. PNAS 113:8681–86
    [Google Scholar]
  45. 45. 
    King NP, Sheffler W, Sawaya MR, Vollmar BS, Sumida JP et al. 2012. Computational design of self-assembling protein nanomaterials with atomic level accuracy. Science 336:1171–74
    [Google Scholar]
  46. 46. 
    Bale JB, Gonen S, Liu Y, Sheffler W, Ellis D et al. 2016. Accurate design of megadalton-scale two-component icosahedral protein complexes. Science 353:389–94
    [Google Scholar]
  47. 47. 
    Kostal J, Mulchandani A, Chen W 2001. Tunable biopolymers for heavy metal removal. Macromolecules 34:2257–61
    [Google Scholar]
  48. 48. 
    MacKay JA, Chen M, McDaniel JR, Liu W, Simnick AJ, Chilkoti A 2009. Self-assembling chimeric polypeptide-doxorubicin conjugate nanoparticles that abolish tumours after a single injection. Nat. Mater. 8:993–99
    [Google Scholar]
  49. 49. 
    Costa SA, Mozhdehi D, Dzuricky MJ, Isaacs FJ, Brustad EM, Chilkoti A 2019. Active targeting of cancer cells by nanobody decorated polypeptide micelle with bio-orthogonally conjugated drug. Nano Lett 19:247–54
    [Google Scholar]
  50. 50. 
    Fletcher J, Harniman R, Barnes F, Boyle A, Collins A et al. 2013. Self-assembling cages from coiled-coil peptide modules. Science 340:595–99
    [Google Scholar]
  51. 51. 
    Zaccai NR, Chi B, Thomson AR, Boyle AL, Bartlett GJ et al. 2011. A de novo peptide hexamer with a mutable channel. Nat. Chem. Biol. 7:935–41
    [Google Scholar]
  52. 52. 
    Ljubetič A, Lapenta F, Gradišar H, Drobnak I, Aupič J et al. 2017. Design of coiled-coil protein-origami cages that self-assemble in vitro and in vivo. Nat. . Biotechnol 35:1094–101
    [Google Scholar]
  53. 53. 
    Park WM, Champion JA. 2014. Thermally triggered self-assembly of folded proteins into vesicles. J. Am. Chem. Soc. 136:17906–9
    [Google Scholar]
  54. 54. 
    Ding D, Guerette P, Fu J, Zhang L, Irvine S, Miserez A 2015. From soft self-healing gels to stiff films in suckerin-based materials through modulation of crosslink density and β-sheet content. Adv. Mater. 27:3953–61
    [Google Scholar]
  55. 55. 
    Ping Y, Ding D, Ramos R, Mohanram H, Deepankumar K et al. 2017. Supramolecular β-sheets stabilized protein nanocarriers for drug delivery and gene transfection. ACS Nano 11:4528–41
    [Google Scholar]
  56. 56. 
    Uchida M, Flenniken ML, Allen M, Willits DA, Crowley BE et al. 2006. Targeting of cancer cells with ferrimagnetic ferritin cage nanoparticles. J. Am. Chem. Soc. 128:16626–33
    [Google Scholar]
  57. 57. 
    Choi K-M, Kim K, Kwon IC, Kim I-S, Ahn HJ 2013. Systemic delivery of siRNA by chimeric capsid protein: tumor targeting and RNAi activity in vivo. Mol. . Pharm 10:18–25
    [Google Scholar]
  58. 58. 
    Yoo L, Park J-S, Kwon KC, Kim S-E, Jin X et al. 2012. Fluorescent viral nanoparticles with stable in vitro and in vivo activity. Biomaterials 33:6194–200
    [Google Scholar]
  59. 59. 
    van Vught R, Pieters RJ, Breukink E 2014. Site-specific functionalization of proteins and their applications to therapeutic antibodies. Comput. Struct. Biotechnol. J. 9:e201402001
    [Google Scholar]
  60. 60. 
    De Las Rivas J, Fontanillo C 2010. Protein-protein interactions essentials: key concepts to building and analyzing interactome networks. PLOS Comput. Biol. 6:e1000807
    [Google Scholar]
  61. 61. 
    Park JS, Cho MK, Lee EJ, Ahn KY, Lee KE et al. 2009. A highly sensitive and selective diagnostic assay based on virus nanoparticles. Nat. Nanotechnol. 4:259–64
    [Google Scholar]
  62. 62. 
    Jung YW, Lee JM, Kim JW, Yoon JW, Cho HM, Chung BH 2009. Photoactivable antibody binding protein: site-selective and covalent coupling of antibody. Anal. Chem. 81:936–42
    [Google Scholar]
  63. 63. 
    Jung YW, Kang HJ, Lee JM, Jung SO, Yun WS et al. 2008. Controlled antibody immobilization onto immunoanalytical platforms by synthetic peptide. Anal. Biochem. 374:99–105
    [Google Scholar]
  64. 64. 
    Richman DD, Cleveland PH, Oxman MN, Johnson KM 1982. The binding of staphylococcal protein-A by the sera of different animal species. J. Immunol. 128:2300–5
    [Google Scholar]
  65. 65. 
    Guss B, Eliasson M, Olsson A, Uhlen M, Frej AK et al. 1986. Structure of the IGG-binding regions of streptococcal protein-G. EMBO J 5:1567–75
    [Google Scholar]
  66. 66. 
    Min J, Song EK, Kim H, Kim KT, Park TJ, Kang S 2016. A recombinant secondary antibody mimic as a target-specific signal amplifier and an antibody immobilizer in immunoassays. Sci. Rep. 6:10
    [Google Scholar]
  67. 67. 
    Hwang MP, Lee JW, Lee KE, Lee KH 2013. Think modular: a simple apoferritin-based platform for the multifaceted detection of pancreatic cancer. ACS Nano 7:8167–74
    [Google Scholar]
  68. 68. 
    Bjorck L, Kronvall G. 1984. Purification and some properties of streptococcal protein-G, protein-A novel IGG-binding reagent. J. Immunol. 133:969–74
    [Google Scholar]
  69. 69. 
    Nilsson B, Moks T, Jansson B, Abrahmsen L, Elmblad A et al. 1987. A synthetic IGG-binding domain based on staphylococcal protein-A. Protein Eng 1:107–13
    [Google Scholar]
  70. 70. 
    Graille M, Stura EA, Corper AL, Sutton BJ, Taussig MJ et al. 2000. Crystal structure of a Staphylococcus aureus protein A domain complexed with the Fab fragment of a human IgM antibody: structural basis for recognition of B-cell receptors and superantigen activity. PNAS 97:5399–404
    [Google Scholar]
  71. 71. 
    Ljungquist C, Jansson B, Moks T, Uhlen M 1989. Thiol-directed immobilization of recombinant IGG-binding receptors. Eur. J. Biochem. 186:557–61
    [Google Scholar]
  72. 72. 
    Sauer-Eriksson AE, Kleywegt GJ, Uhlén M, Jones TA 1995. Crystal-structure of the C2 fragment of streptococcal protein-G in complex with the FC domain of human-IGG. Structure 3:265–78
    [Google Scholar]
  73. 73. 
    Chen YJ, Chen M, Cheng TL, Roffler SR, Lin SY et al. 2019. Simply mixing poly protein G with detection antibodies enhances the detection limit and sensitivity of immunoassays. Anal. Chem. 91:8310–17
    [Google Scholar]
  74. 74. 
    Feng B, Huang SR, Ge F, Luo YP, Jia DY, Dai YZ 2011. 3D antibody immobilization on a planar matrix surface. Biosens. Bioelectron. 28:91–96
    [Google Scholar]
  75. 75. 
    Choe W, Durgannavar TA, Chung SJ 2016. Fc-binding ligands of immunoglobulin G: an overview of high affinity proteins and peptides. Materials 9:994
    [Google Scholar]
  76. 76. 
    DeLano WL, Ultsch MH, de Vos AM, Wells JA 2000. Convergent solutions to binding at a protein-protein interface. Science 287:1279–83
    [Google Scholar]
  77. 77. 
    Kang HJ, Kang YJ, Lee YM, Shin HH, Chung SJ, Kang S 2012. Developing an antibody-binding protein cage as a molecular recognition drug modular nanoplatform. Biomaterials 33:5423–30
    [Google Scholar]
  78. 78. 
    Yu FF, Alesand V, Nygren P-Å 2018. Site-specific photoconjugation of beta-lactamase fragments to monoclonal antibodies enables sensitive analyte detection via split-enzyme complementation. Biotechnol. J. 13:e1700688
    [Google Scholar]
  79. 79. 
    Westerlund K, Vorobyeva A, Mitran B, Orlova A, Tolmachev V et al. 2019. Site-specific conjugation of recognition tags to trastuzumab for peptide nucleic acid-mediated radionuclide HER2 pretargeting. Biomaterials 203:73–85
    [Google Scholar]
  80. 80. 
    Hui JZ, Al Zaki A, Cheng ZL, Popik V, Zhang HT et al. 2014. Facile method for the site-specific, covalent attachment of full-length IgG onto nanoparticles. Small 10:3354–63
    [Google Scholar]
  81. 81. 
    Perols A, Famme MA, Karlström AE 2015. Site-specific antibody labeling by covalent photoconjugation of Z domains functionalized for alkyne-azide cycloaddition reactions. ChemBioChem 16:2522–29
    [Google Scholar]
  82. 82. 
    Park J, Lee Y, Ko BJ, Yoo TH 2018. Peptide-directed photo-cross-linking for site-specific conjugation of IgG. Bioconjugate Chem 29:3240–44
    [Google Scholar]
  83. 83. 
    Sano T, Cantor CR. 2000. Streptavidin-containing chimeric proteins: design and production. Methods Enzymol 326:305–11
    [Google Scholar]
  84. 84. 
    Cui XP, Vasylieva N, Shen D, Barnych B, Yang J et al. 2018. Biotinylated single-chain variable fragment-based enzyme-linked immunosorbent assay for glycocholic acid. Analyst 143:2057–65
    [Google Scholar]
  85. 85. 
    Beckett D, Kovaleva E, Schatz PJ 1999. A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation. Protein Sci 8:921–29
    [Google Scholar]
  86. 86. 
    Valadon P, Darsow B, Buss TN, Czarny M, Griffin NM et al. 2010. Designed auto-assembly of nanostreptabodies for rapid tissue-specific targeting in vivo. J. Biol. Chem 285:713–22
    [Google Scholar]
  87. 87. 
    Zhu M, Gong X, Hu YH, Ou WJ, Wan YK 2014. Streptavidin-biotin-based directional double Nanobody sandwich ELISA for clinical rapid and sensitive detection of influenza H5N1. J. Transl. Med. 12:352
    [Google Scholar]
  88. 88. 
    Men D, Zhang ZP, Guo YC, Zhu DH, Bi LJ et al. 2010. An auto-biotinylated bifunctional protein nanowire for ultra-sensitive molecular biosensing. Biosens. Bioelectron. 26:1137–41
    [Google Scholar]
  89. 89. 
    Thrane S, Janitzek CM, Agerbaek , Ditlev SB, Resende M et al. 2015. A novel virus-like particle based vaccine platform displaying the placental malaria antigen VAR2CSA. PLOS ONE 10:e0143071
    [Google Scholar]
  90. 90. 
    Tienken L, Drude N, Schau I, Winz OH, Temme A et al. 2018. Evaluation of a pretargeting strategy for molecular imaging of the prostate stem cell antigen with a single chain antibody. Sci. Rep. 8:3755
    [Google Scholar]
  91. 91. 
    Block H, Maertens B, Spriestersbach A, Brinker N, Kubicek J et al. 2009. Immobilized-metal affinity chromatography (IMAC): a review. In Guide to Protein Purification, ed. RR Burgess. MP Deutscher 463439–73 San Diego, CA: Elsevier Acad, 2nd ed..
    [Google Scholar]
  92. 92. 
    Hochuli E, Bannwarth W, Dobeli H, Gentz R, Stüber D 1988. Genetic approach to facilitate purification of recombinant proteins with a novel metal chelate adsorbent. Nat. Biotechnol. 6:1321–25
    [Google Scholar]
  93. 93. 
    Le DHT, Commandeur U, Steinmetz NF 2019. Presentation and delivery of tumor necrosis factor-related apoptosis-inducing ligand via elongated plant viral nanoparticle enhances antitumor efficacy. ACS Nano 13:2501–10
    [Google Scholar]
  94. 94. 
    Goldsmith LE, Pupols M, Kickhoefer VA, Rome LH, Monbouquette HG 2009. Utilization of a protein “shuttle” to load vault nanocapsules with gold probes and proteins. ACS Nano 3:3175–83
    [Google Scholar]
  95. 95. 
    Matsuura K, Nakamura T, Watanabe K, Noguchi T, Minamihata K et al. 2016. Self-assembly of Ni-NTA-modified β-annulus peptides into artificial viral capsids and encapsulation of His-tagged proteins. Org. Biomol. Chem. 14:7869–74
    [Google Scholar]
  96. 96. 
    Antos JM, Truttmann MC, Ploegh HL 2016. Recent advances in sortase-catalyzed ligation methodology. Curr. Opin. Struct. Biol. 38:111–18
    [Google Scholar]
  97. 97. 
    Dorr BM, Ham HO, An C, Chaikof EL, Liu DR 2014. Reprogramming the specificity of sortase enzymes. PNAS 111:13343–48
    [Google Scholar]
  98. 98. 
    Hess GT, Cragnolini JJ, Popp MW, Allen MA, Dougan SK et al. 2012. M13 bacteriophage display framework that allows sortase-mediated modification of surface-accessible phage proteins. Bioconjugate Chem 23:1478–87
    [Google Scholar]
  99. 99. 
    Shah NH, Muir TW. 2014. Inteins: nature's gift to protein chemists. Chem. Sci. 5:446–61
    [Google Scholar]
  100. 100. 
    Paulus H. 2000. Protein splicing and related forms of protein autoprocessing. Annu. Rev. Biochem. 69:447–96
    [Google Scholar]
  101. 101. 
    Lockless SW, Muir TW. 2009. Traceless protein splicing utilizing evolved split inteins. PNAS 106:10999–1004
    [Google Scholar]
  102. 102. 
    Siu K-H, Chen W. 2017. Control of the yeast mating pathway by reconstitution of functional α-factor using split intein-catalyzed reactions. ACS Synth. Biol. 6:1453–60
    [Google Scholar]
  103. 103. 
    Zakeri B, Fierer JO, Celik E, Chittock EC, Schwarz-Linek U et al. 2012. Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin. PNAS 109:E690–97
    [Google Scholar]
  104. 104. 
    Fierer JO, Veggiani G, Howarth M 2014. SpyLigase peptide-peptide ligation polymerizes affibodies to enhance magnetic cancer cell capture. PNAS 111:E1176–81
    [Google Scholar]
  105. 105. 
    Veggiani G, Nakamura T, Brenner MD, Gayet RV, Yan J et al. 2016. Programmable polyproteams built using twin peptide superglues. PNAS 113:1202–7
    [Google Scholar]
  106. 106. 
    Tan LL, Hoon SS, Wong FT 2016. Kinetic controlled tag-catcher interactions for directed covalent protein assembly. PLOS ONE 11:e0165074
    [Google Scholar]
  107. 107. 
    Brune KD, Buldun CM, Li YY, Taylor IJ, Brod F et al. 2017. Dual plug-and-display synthetic assembly using orthogonal reactive proteins for twin antigen immunization. Bioconjugate Chem 28:1544–51
    [Google Scholar]
  108. 108. 
    Nguyen DL, Kim H, Kim D, Lee JO, Gye MC, Kim YP 2018. Detection of matrix metalloproteinase activity by bioluminescence via intein-mediated biotinylation of luciferase. Sensors 18:875
    [Google Scholar]
  109. 109. 
    Madej MP, Coia G, Williams CC, Caine JM, Pearce LA et al. 2012. Engineering of an anti-epidermal growth factor receptor antibody to single chain format and labeling by sortase A-mediated protein ligation. Biotechnol. Bioeng. 109:1461–70
    [Google Scholar]
  110. 110. 
    Anderson GP, Liu JL, Shriver-Lake LC, Zabetakis D, Sugiharto VA et al. 2019. Oriented immobilization of single-domain antibodies using SpyTag/SpyCatcher yields improved limits of detection. Anal. Chem. 91:9424–29
    [Google Scholar]
  111. 111. 
    Chen L, Cohen J, Song X, Zhao A, Ye Z et al. 2016. Improved variants of SrtA for site-specific conjugation on antibodies and proteins with high efficiency. Sci. Rep. 6:31899
    [Google Scholar]
  112. 112. 
    Ismail NF, Lim TS. 2016. Site-specific scFv labelling with invertase via Sortase A mechanism as a platform for antibody-antigen detection using the personal glucose meter. Sci. Rep. 6:19338
    [Google Scholar]
  113. 113. 
    Jeon H, Lee E, Kim D, Lee M, Ryu J et al. 2018. Cell-based biosensors based on intein-mediated protein engineering for detection of biologically active signaling molecules. Anal. Chem. 90:9779–86
    [Google Scholar]
  114. 114. 
    Gallo E, Vasilev KV, Jarvik J 2014. Fluorogen-activating-proteins as universal affinity biosensors for immunodetection. Biotechnol. Bioeng. 111:475–84
    [Google Scholar]
  115. 115. 
    Paterson BM, Alt K, Jeffery CM, Price RI, Jagdale S et al. 2014. Enzyme-mediated site-specific bioconjugation of metal complexes to proteins: sortase-mediated coupling of copper-64 to a single-chain antibody. Angew. Chem. 53:6115–19
    [Google Scholar]
  116. 116. 
    Uchida M, Kosuge H, Terashima M, Willits DA, Liepold LO et al. 2011. Protein cage nanoparticles bearing the LyP-1 peptide for enhanced imaging of macrophage-rich vascular lesions. ACS Nano 5:2493–502
    [Google Scholar]
  117. 117. 
    Liepold L, Abedin M, Buckhouse E, Frank J, Young M, Douglas T 2009. Supramolecular protein cage composite MR contrast agents with extremely efficient relaxivity properties. Nano Lett 9:4520–26
    [Google Scholar]
  118. 118. 
    Aime S, Frullano L, Crich S 2002. Compartmentalization of a gadolinium complex in the apoferritin cavity: a route to obtain high relaxivity contrast agents for magnetic resonance imaging. Angew. Chem. 41:1017–19
    [Google Scholar]
  119. 119. 
    Lin X, Xie J, Niu G, Zhang F, Gao H et al. 2011. Chimeric ferritin nanocages for multiple function loading and multimodal imaging. Nano Lett 11:814–19
    [Google Scholar]
  120. 120. 
    Ma Y, Nolte R, Cornelissen J 2012. Virus-based nanocarriers for drug delivery. Adv. Drug Deliv. Rev. 64:811–25
    [Google Scholar]
  121. 121. 
    Yan F, Zhang Y, Yuan H, Gregas M, Vo-Dinh T 2008. Apoferritin protein cages: a novel drug nanocarrier for photodynamic therapy. Chem. Commun. 38:4579–81
    [Google Scholar]
  122. 122. 
    Yang Z, Wang X, Diao H, Zhang J, Li H et al. 2007. Encapsulation of platinum anticancer drugs by apoferritin. Chem. Commun. 33:3453–55
    [Google Scholar]
  123. 123. 
    Liang M, Fan K, Zhou M, Duan D, Zheng J et al. 2014. H-ferritin-nanocaged doxorubicin nanoparticles specifically target and kill tumors with a single-dose injection. PNAS 111:14900–5
    [Google Scholar]
  124. 124. 
    Bellini M, Mazzucchelli S, Galbiati E, Sommaruga S, Fiandra L et al. 2014. Protein nanocages for self-triggered nuclear delivery of DNA-targeted chemotherapeutics in cancer cells. J. Control. Release 196:184–96
    [Google Scholar]
  125. 125. 
    Flenniken M, Liepold L, Crowley B, Willits D, Young M, Douglas T 2005. Selective attachment and release of a chemotherapeutic agent from the interior of a protein cage architecture. Chem. Commun. 28:447–49
    [Google Scholar]
  126. 126. 
    Toita R, Murata M, Abe K, Narahara S, Piao J et al. 2013. A nanocarrier based on a genetically engineered protein cage to deliver doxorubicin to human hepatocellular carcinoma cells. Chem. Commun. 49:7442–44
    [Google Scholar]
  127. 127. 
    Prel A, Caval V, Gayon R, Ravassard P, Duthoit C et al. 2015. Highly efficient in vitro and in vivo delivery of functional RNAs using new versatile MS2-chimeric retrovirus-like particles. Mol. Therapy Methods Clin. Dev. 2:15039
    [Google Scholar]
  128. 128. 
    Choi K-M, Choi SH, Jeon H, Kim IS, Ahn HJ 2011. Chimeric capsid protein as a nanocarrier for siRNA delivery: stability and cellular uptake of encapsulated siRNA. ACS Nano 5:8690–99
    [Google Scholar]
  129. 129. 
    Qazi S, Miettinen H, Wilkinson R, McCoy K, Douglas T, Wiedenheft B 2016. Programmed self-assembly of an active P22-Cas9 nanocarrier system. Mol. Pharm. 13:1191–96
    [Google Scholar]
  130. 130. 
    Kelly P, Anand P, Uvaydov A, Chakravartula S, Sherpa C et al. 2015. Developing a dissociative nanocontainer for peptide drug delivery. Int. J. Environ. Res. Public Health 12:12543–55
    [Google Scholar]
  131. 131. 
    Frutos S, Hernández JL, Otero A, Calvis C, Adan J et al. 2018. Site-specific antibody drug conjugates using streamlined expressed protein ligation. Bioconjugate Chem 29:3503–8
    [Google Scholar]
  132. 132. 
    Pirzer T, Becher KS, Rieker M, Meckel T, Mootz HD, Kolmar H 2018. Generation of potent anti-HER1/2 immunotoxins by protein ligation using split inteins. ACS Chem. Biol. 13:2058–66
    [Google Scholar]
  133. 133. 
    Beerli RR, Hell T, Merkel AS, Grawunder U 2015. Sortase enzyme-mediated generation of site-specifically conjugated antibody drug conjugates with high in vitro and in vivo potency. PLOS ONE 10:e0131177
    [Google Scholar]
  134. 134. 
    Kornberger P, Skerra A. 2014. Sortase-catalyzed in vitro functionalization of a HER2-specific recombinant Fab for tumor targeting of the plant cytotoxin gelonin. mAbs 6:354–66
    [Google Scholar]
  135. 135. 
    Vance N, Zacharias N, Ultsch M, Li GM, Fourie A et al. 2019. Development, optimization, and structural characterization of an efficient peptide-based photoaffinity cross-linking reaction for generation of homogeneous conjugates from wild-type antibodies. Bioconjugate Chem 30:148–60
    [Google Scholar]
  136. 136. 
    Pinheiro A, Han D, Shih W, Yan H 2011. Challenges and opportunities for structural DNA nanotechnology. Nat. Nanotechnol. 6:763–72
    [Google Scholar]
  137. 137. 
    Hong F, Zhang F, Liu Y, Yan H 2017. DNA origami: scaffolds for creating higher order structures. Chem. Rev. 117:12584–640
    [Google Scholar]
  138. 138. 
    Fu J, Yang Y, Johnson-Buck A, Liu M, Liu Y et al. 2014. Multi-enzyme complexes on DNA scaffolds capable of substrate channelling with an artificial swinging arm. Nat. Nanotechnol. 9:531–36
    [Google Scholar]
  139. 139. 
    Berckman E, Chen W. 2019. Exploiting dCas9 fusion proteins for dynamic assembly of synthetic metabolons. Chem. Commun. 55:8219–22
    [Google Scholar]
  140. 140. 
    Chauhan V, Jain R. 2013. Strategies for advancing cancer nanomedicine. Nat. Mater. 12:958–62
    [Google Scholar]
  141. 141. 
    Douglas S, Bachelet I, Church G 2012. A logic-gated nanorobot for targeted transport of molecular payloads. Science 335:831–34
    [Google Scholar]
  142. 142. 
    Du Y, Jiang Q, Beziere N, Song L, Zhang Q et al. 2016. DNA-nanostructure-gold-nanorod hybrids for enhanced in vivo optoacoustic imaging and photothermal therapy. Adv. Mater. 28:10000–7
    [Google Scholar]
  143. 143. 
    Liu J, Song L, Liu S, Jiang Q, Liu Q et al. 2018. A DNA-based nanocarrier for efficient gene delivery and combined cancer therapy. Nano Lett 18:3328–34
    [Google Scholar]
  144. 144. 
    Li S, Jiang Q, Liu S, Zhang Y, Tian Y et al. 2018. A DNA nanorobot functions as a cancer therapeutic in response to a molecular trigger in vivo. Nat. . Biotechnol 36:258–64
    [Google Scholar]
  145. 145. 
    Shen X, Jiang Q, Wang J, Dai L, Zou G et al. 2012. Visualization of the intracellular location and stability of DNA origami with a label-free fluorescent probe. Chem. Commun. 48:11301–3
    [Google Scholar]
  146. 146. 
    Monroy-Contreras R, Vaca L. 2011. Molecular beacons: powerful tools for imaging RNA in living cells. J. Nucleic Acids 2011:741723
    [Google Scholar]
  147. 147. 
    Blackstock D, Sun Q, Chen W 2015. Fluorescent protein-based molecular beacons by zinc finger protein-guided assembly. Biotechnol. Bioeng. 112:236–41
    [Google Scholar]
  148. 148. 
    Blackstock D, Chen W. 2014. Halo-tag mediated self-labeling of fluorescent proteins to molecular beacons for nucleic acid detection. Chem. Commun. 50:13735–38
    [Google Scholar]
  149. 149. 
    Park HJ, Yoo TH. 2018. Nucleic acid detection by a target-assisted proximity proteolysis reaction. ACS Sens 3:2066–70
    [Google Scholar]
  150. 150. 
    Zhang D, Seelig G. 2011. Dynamic DNA nanotechnology using strand-displacement reactions. Nat. Chem. 3:103–13
    [Google Scholar]
  151. 151. 
    Han D, Zhu Z, Wu C, Peng L, Zhou L et al. 2012. A logical molecular circuit for programmable and autonomous regulation of protein activity using DNA aptamer-protein interactions. J. Am. Chem. Soc. 134:20797–804
    [Google Scholar]
  152. 152. 
    Hochrein LM, Schwarzkopf M, Shahgholi M, Yin P, Pierce NA 2013. Conditional dicer substrate formation via shape and sequence transduction with small conditional RNAs. J. Am. Chem. Soc. 135:17322–30
    [Google Scholar]
/content/journals/10.1146/annurev-chembioeng-101519-121526
Loading
/content/journals/10.1146/annurev-chembioeng-101519-121526
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