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Cited by 41Monoclonal and Polyclonal Antibodies ResearchProtein purification and stabilityBacteriophages and microbial interactions

Advances in the production and batch reformatting of phage antibody libraries

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Reader, Rose H., Workman, Robert G., Maddison, Ben C., Gough, Kevin C.·2019·Molecular Biotechnology
DOI 10.1007/s12033-019-00207-0PMC PMC6785589
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Abstract

Phage display antibody libraries have proven an invaluable resource for the isolation of diagnostic and potentially therapeutic antibodies, the latter usually being antibody fragments converted into IgG formats. Recent advances in the production of highly diverse and functional antibody libraries are considered here, including for Fabs, scFvs and nanobodies. These advances include codon optimisation during generation of CDR diversity, improved display levels using novel signal sequences, molecular chaperones and isomerases and the use of highly stable scaffolds with relatively high expression levels. In addition, novel strategies for the batch reformatting of scFv and Fab phagemid libraries, derived from phage panning, into IgG formats are described. These strategies allow the screening of antibodies in the end-use format, facilitating more efficient selection of potential therapeutics.

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  • In the case of scFvs and nanobodies, reduced size and single polypeptide nature make them amenable to high-throughput selection technologies such as phage display, cell display, yeast display and ribosomal display.

    “Moreover, in the case of scFvs and nanobodies, the reduced size and the single polypeptide nature make antibody fragments readily amenable to high-throughput selection technologies such as phage display, cell display, yeast display and ribosomal display [39].”

    From Evolution of Escherichia coli Expression System in Producing Antibody Recombinant Fragments (2020) · cites this paper as [39]

    The Introduction describes scFvs as single chains and nanobodies as small, single-domain fragments that can be displayed on phage. The scFv section also describes selection using phage and yeast surface display with cell sorting. Our copy does not establish the claimed suitability for ribosomal display or explicitly attribute suitability across all the listed methods to reduced size and single-polypeptide structure. (LLM, conf=0.86)

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  1. [1]Smith GP Petrenko VA Phage display Chemical Reviews 1997 97 391 410 11848876
  2. [2]Carmen S Lutz J Concepts in antibody phage display Briefings in Functional Genomics Proteomics 2002 1 189 203 15239904
  3. [3]Paschke M Phage display systems and their applications Applied Microbiology and Biotechnology 2006 70 2 11 16365766
  4. [4]Zhang H Torkmani A Jones TM Ruiz DI Pons J Lerner RA Phenotype-information-phenotype cycle for deconvolution of combinatorial antibody libraries selected against complex systems Proceedings of the National Academy of Sciences USA 2011 108 13456 13461 PMC3158238 21825149
  5. [5]D’Angelo S Kumar S Naranjo L Ferrara F Kiss C Bradbury ARM From deep sequencing to actual clones Protein Engineering, Design & Selection 2014 27 301 307 PMC4191444 25183780
  6. [6]Miyazaki N Kiyose N Akazawa Y Takashima M Hagihara Y Inoue N Matsuda T Ogawa R Inoue S Ito Y Isolation and characterisation of antigen-specific alpaca (Lama pacos) VHH antibodies by biopanning followed by high-throughput sequencing Journal of Biochemistry 2015 158 205 215 25888581
  7. [7]Li Y Cockburn W Kilpatrick JB Whitelam GC High affinity scFvs from a single rabbit immunized with multiple haptens Biochemical and Biophysical Research Communications 2000 16 398 404 10679216
  8. [8]Gough KC Maddison BC Shikotra A Moiseeva AP Yang W Jarvis S Bradding P Evidence for a novel Kit adhesion domain mediating human mast cell adhesion to structural airway cells Respiratory Research 2015 16 86 26173671 PMC4501212
  9. [9]Kühne SA La Hawes WS Ragion RM Woodward MJ Whitelam GC Gough KC Isolation of recombinant antibodies against espA and intimin of of Escherichia coli O157:H7 Journal of Clinical Microbiology 2004 42 2966 2976 15243046 PMC446247
  10. [10]Omar N Lim TS Hust M Lim TS Construction of naïve and immune human Fab phage-display libraries Phage display, vol 1701: Methods in molecular biology 2018 New York Humana Press 25 44 29116498
  11. [11]Rahumatullah A Ahmad A Rahmah N Lim TS Delineation of BmSXP antibody V-gene usage from a lymphatic filariasis based immune scFv antibody library Molecular Immunology 2015 67 512 523 26277276
  12. [12]Vaughan TJ Williams AJ Pritchard K Osbourn JK Pope AR Earnshaw JC McCafferty J Hodits RA Wilton J Johnson KS Human antibodies with sub-nanomolar affinities isolated from a large non-immunized phage display library Nature Biotechnology 1996 14 309 314 9630891
  13. [13]Goletz S Christensen PA Kristensen P Blohm D Tomlinson I Winter G Karsten U Selection of large diversities of antiidiotypic antibody fragments by phage display Journal of Molecular Biology 2002 315 1087 1097 11827478
  14. [14]Knappik A Ge L Honegger A Pack P Fischer M Wellnhofer G Hoess A Plückthun A Virnekäs B Fully synthetic human combinatorial antibody libraries (HuCAL) based on modular consensus frameworks and CDRs randomized with trinucleotides Journal of Molecular Biology 2000 296 57 86 10656818
  15. [15]Rauchenberger R Borges E Thomassen-Wolf E Rom E Adar R Yaniv Y Maika M Chumakov I Kotzer S Resnitzky D Knappik A Reiffert S Prassler J Jury K Waldherr D Bauer S Kretzscmar T Yayon A Rothe C Human combinatorial Fab library yielding specific and functional antibodies against the human fibroblast growth factor receptor 3 Journal of Biological Chemistry 2003 278 38194 38205 12842902
  16. [16]Rothe C Urlinger S Löhning C Prassler J Stark Y Jäger U Hubner B Bardroff M Pradel I Boss M Bittlingmaier R Bataa T Frisch C Brocks B Honegger A Urban M The human combinatorial antibody library HuCAL GOLD combines diversification of all six CDRs according to the natural immune system with a novel display method for efficient selection of high-affinity antibodies Journal of Molecular Biology 2008 376 1182 1200 18191144
  17. [17]Kang AS Barbas CF Janda KD Benkovic SJ Lerner RA Linkage of recognition and replication functions by assembling combinatorial antibody Fab libraries along phage surfaces Proceedings of the National Academy of Sciences USA 1991 88 4363 4366 PMC51659 1903540
  18. [18]Yan J Li G Hu Y Ou W Wan Y Construction of a synthetic phage-displayed Nanobody library with CDR3 regions randomized by trinucleotide cassettes for diagnostic applications Journal of Translational Medicine 2014 12 343 25496223 PMC4269866
  19. [19]Feng M Bian H Wu X Fu T Fu Y Hong J Fleming BD Flajnik MF Ho M Construction and next generation sequencing analysis of a large phage-displayed VNAR single-domain antibody library from six naïve nurse sharks Antibody Therapeutics 2019 2 1 11 30627698 PMC6312525
  20. [20]Gonzalez-Sapienza G Rossotti MA Tabares-da Rosa S Single-domain antibodies as versatile affinity reagents for analytical and diagnostic applications Frontiers in Immunology 2017 8 977 28871254 PMC5566570
  21. [21]Jostock T Vanhove M Brepoels E Van Gool R Daukandt M Wehnert A Van Hegelsom R Dransfield D Sexton D Devlin M Ley A Hoogenboom H Müllberg J Rapid generation of functional human IgG antibodies derived from Fab-on-phage display libraries Journal of Immunological Methods 2004 289 65 80 15251413
  22. [22]Frenzel A Kügler J Helmsing S Meier D Schirrmann T Hust M Dübel S Designing human antibodies by phage display Transfusion Medicine and Hemotherapy 2017 44 312 318 29070976 PMC5649246
  23. [23]Frenzel A Schirrmann T Hust M Phage display-derived human antibodies in clinical development and therapy mAbs 2016 8 1177 1194 27416017 PMC5058633
  24. [24]Kaplon H Reichert M Antibodies to watch in 2019 mAbs 2019 11 219 238 30516432 PMC6380461
  25. [25]Koerber JT Hornsby MJ Wells JA An improved single-chain Fab platform for efficient display and recombinant expression Journal of Molecular Biology 2015 427 576 586 25481745 PMC4297586
  26. [26]Tesar D Hötzel I A dual host vector for Fab phage display and expression of native IgG in mammalian cells Protein Engineering, Design & Selection 2013 26 655 662 24065833
  27. [27]Nelson RS Valadon P A universal phage display system for the seamless construction of Fab libraries Journal of Immunological Methods 2017 450 41 49 28756139
  28. [28]Weber J Peng H Rader C From rabbit antibody repertoires to rabbit monoclonal antibodies Experimental & Molecular Medicine 2017 49 e305 28336958 PMC5382564
  29. [29]Peng H Nerreter T Chang J Qi J Li X Karunadharma P Martinez GJ Fallahi M Soden J Freeth J Beerli RR Grawunder U Hudecek M Rader C Mining naïve rabbit antibody repertoires by phage display for monoclonal antibodies of therapeutic utility Journal of Molecular Biology 2017 429 2954 2973 28818634 PMC5610937
  30. [30]Tiller T Schuster I Deppe D Siegers K Strohner R Herrmann T Berenguer M Poujol D Stehle J Stark Y Heßling M Daubert D Felderer K Kaden S Kölln J Enzelberger M Urlinger S A fully synthetic human Fab antibody library based on fixed VH/VL framework pairings with favorable biophysical properties mAbs 2013 5 445 470 23571156 PMC4169037
  31. [31]Lee CV Sidhu SS Fuh G Bivalent antibody phage display mimics natural immunoglobulin Journal of Immunological Methods 2004 284 119 132 14736422
  32. [32]Entzminger KC Johnson JL Hyun J Lieberman RL Maynard JA Increased Fab thermoresistance via VH-targeted directed evolution Protein Engineering, Design & Selection 2015 10 365 377 PMC4596279 26283664
  33. [33]Wolf Perez A-M Sormanni P Andersen JS Sakhnini LI Rodriguez-Leon I Bjelke JR De Gajhede AJ Maria L Otzen DE Vendruscolo M Lorenzen N In vitro and in silico assessment of the developability of a designed monoclonal antibody library mAbs 2019 11 388 400 30523762 PMC6380425
  34. [34]Loh Q Leong SW Tye GJ Choong YS Lim TS Improved Fab presentation on phage surface with the use of molecular chaperone coplasmid system Analytical Biochemistry 2015 477 56 61 25769419
  35. [35]Huovinen T Syrjänpää M Sanmark H Seppä T Akter S Khan LM Lamminmäki U The selection performance of an antibody library displayed on filamentous phage coat proteins p9, p3 and truncated p3 BMC Research Notes 2014 7 661 25238965 PMC4176855
  36. [36]Levy R Ahluwalia K Bohmann DJ Giang HM Schwimmer LJ Issafras H Reddy NB Chan C Horwitz AH Takeuchi T Enhancement of antibody fragment secretion into the Escherichia coli periplasm by co-expression with the peptidyl prolyl isomerase, FkpA, in the cytoplasm Journal of Immunological Methods 2013 394 10 21 23624043
  37. [37]Zuberbühler K Palumbo A Bacci C Giovannoni L Sommavilla R Kaspar M Trachsel E Neri D A general method for the selection of high-level scFv and IgG antibody expression by stably transfected mammalian cells Protein Engineering, Design & Selection 2008 22 169 174 19022802
  38. [38]Skerra A Pfitzinger I Plückthun A The functional expression of antibody Fv fragments in Escherichia coli: Improved vectors and a generally applicable purification technique Bio/Technology 1993 9 273 278 1367302
  39. [39]Bird RE Walker BW Single chain variable regions Trends in Biotechnology 1991 9 132 137 1367550
  40. [40]Weisser NE Hall JC Applications of single-chain variable fragment antibodies in therapeutics and diagnostics Biotechnology Advances 2009 27 502 520 19374944
  41. [41]Schwimmer LJ Huang B Giang H Cotter RL Chemla-Vogel DS Dy FV Tam EM Zhang F Toy P Bohmann DJ Watson SR Beaber JW Reddy N Kuan HF Bedinger DH Rondon IJ Discovery of diverse and functional antibodies from large human repertoire antibody libraries Journal of Immunological Methods 2013 391 60 71 23454004
  42. [42]Putelli A Kiefer JD Zadory M Matasci M Neri D A fibrin-specific monoclonal antibody from a designed phage display library inhibits clot formation and localizes to tumors in vivo Journal of Molecular Biology 2014 426 3606 3618 25073100
  43. [43]Kügler J Wilke S Meier D Tomszak F Frenzel A Schirrmann T Dübel S Garritsen H Hock B Toleikis L Schütte M Hust M Generation and analysis of the improved human HAL9/10 antibody phage display libraries BMC Biotechnology 2015 15 10 25888378 PMC4352240
  44. [44]Clark M Antibody humanization: a case of the ‘Emperor’s new clothes’? Immunology Today 2000 21 397 402 10916143
  45. [45]Verhaar MJ Chester KA Keep PA Robson L Pedley RB Boden JA Hawkins RE Begent RH A single chain Fv derived from a filamentous phage library has distinct tumor targeting advantages over one derived from a hybridoma International Journal of Cancer 1995 61 497 501 7759155
  46. [46]Mao S Gao C Lo CH Wirsching P Wong CH Janda KD Phage-display library selection of high-affinity human single-chain antibodies to tumor-associated carbohydrate antigens sialyl Lewisx and Lewisx Proceedings of the National Academy of Sciences USA 1999 96 6953 6958 PMC22023 10359820
  47. [47]Dorfmueller S Tan HC Ngoh ZX Toh KY Peh G Ang HP Seah XY Chin A Choo A Mehta JS Sun W Isolation of a recombinant antibody specific for a surface marker of the corneal endothelium by phage display Scientific Reports 2016 6 21661 26902886 PMC4763205
  48. [48]Ossysek K Uchański T Kulesza M Bzowska M Klaus T Woś K Madej M Bereta J A new expression vector facilitating production and functional analysis of scFv antibody fragments selected from Tomlinson I + J phagemid libraries Immunology Letters 2015 167 95 102 26219832
  49. [49]Nishi M Jian N Yamamoto K Seto H Nishida Y Tonoyama Y Shimizu N Nishi Y Ligation-based assembly for constructing mouse synthetic scFv libraries by chain shuffling with in vivo-amplified VH and VL fragments Journal of Immunological Methods 2014 412 53 69 25010461
  50. [50]Weber M Bujak E Putelli A Villa A Matasci M Gualandi L Hemmerle T Wulhfard S Neri D A highly functional synthetic phage display library containing over 40 billion human antibody clones PLoS ONE 2014 9 e100000 24950200 PMC4065035
  51. [52]Säll A Walle M Wingren C Müller S Nyman T Vala A Ohlin M Borrebaeck CAK Persson H Generation and analyses of human synthetic antibody libraries and their application for protein microarrays Protein Engineering, Design & Selection 2016 29 427 437 27590051
  52. [53]Valadon P Pérez-Tapia SM Nelson RS Guzmán-Bringas OU Arrieta-Oliva HI Gómez-Castellano KM Pohl MA Almagro JC ALTHEA Gold Libraries™: Antibody libraries for therapeutic antibody discovery mAbs 2019 11 516 531 30663541 PMC6512909
  53. [54]Zhao Q Buhr D Gunter C Frenette J Ferguson M Sanford E Holland E Rajagopal C Batonick M Kiss MM Wiener MP Rational library design by functional CDR resampling New Biotechnology 2018 45 89 97 29242049 PMC5995609
  54. [55]Sormanni P Amery L Ekizoglou S Vendruscolo M Popovic B Rapid and accurate in silico solubility screening of a monoclonal antibody library Scientific Reports 2018 7 8200 PMC5558012 28811609
  55. [56]Xiao X Chen Y Mugabe S Gao C Tkaczyk C Mazor Y Pavlik P Wu H Dall’Acqua W Chowdhury PS A novel dual expression platform for high throughput functional screening of phage libraries in product like format PLoS ONE 2015 10 e0140691 26468955 PMC4607404
  56. [57]Liu Y Gu M Wu Y Wang W Wang R Du M Ma P Zhou X Wang Y Cao Y Zhang H High-throughput reformatting of phage-displayed antibody fragments to IgGs by one-step emulsion PCR Protein Engineering, Design & Selection 2018 31 427 436 31096267
  57. [58]Batonick M Kiss MM Fuller EP Magadan CM Holland EG Zhao Q Wang D Kay BK Weiner MP pMINERVA: A donor-acceptor system for the in vivo recombineering of scFv into IgG molecules Journal of Immunological Methods 2016 431 22 30 26851519 PMC4792691
  58. [59]Xiao X Douthwaite JA Chen Y Kemp B Kidd S Percival-Alwyn J Smith A Goode K Swerdlow B Lowe D Wu H Dall’Acqua WF Chowdhury PS A high-throughput platform for population reformatting and mammalian expression of phage display libraries to enable functional screening as full-length IgG mAbs 2017 9 996 1006 28613102 PMC5540111
  59. [60]Park J Throop AL LaBaer J Site-specific recombinational cloning using gateway and in-fusion cloning schemes Current Protocols in Molecular Biology 2015 110 3.20.1 3.20.23 25827088 PMC4492480
  60. [61]Jäger V Büssow K Wagner A Weber S Hust M Frenzel A Schirrmann T High level transient production of recombinant antibodies and antibody fusion proteins in HEK293 cells BMC Biotechnology 2013 13 52 23802841 PMC3699382
  61. [62]Nilsson P Paavilainen L Larsson K Odling J Sundberg M Andersson AC Kampf C Persson A Al-Khalili Szigyarto C Ottosson J Towards a human proteome atlas: high-throughput generation of monospecific antibodies for tissue profiling Proteomics 2005 5 4327 4337 16237735
  62. [63]Ferrara F D’Angelo S Gaiotto T Naranjo L Tian H Graslund S Dobrovetsky E Hraber P Lund-Johansen F Saragozza S Sblattero D Kiss C Bradbury ARM Recombinant renewable polyclonal antibodies mAbs 2015 7 32 41 25530082 PMC4622072
  63. [64]Henry KA Kandalaft H Lowden MJ van Rossotti MA Faassen H Hussack G Durocher Y Kim DY Tanha J A disulfide-stabilized human VL single-domain antibody library is a source of soluble and highly thermostable binders Molecular Immunology 2017 90 190 196 28820969
  64. [65]Henry KA Tanha J Performance evaluation of phage-displayed synthetic human single-domain antibody libraries: A retrospective analysis Journal of Immunological Methods 2018 456 81 86 29462605
  65. [66]Henry KA Kim DY Kandalaft H Lowden MJ Yang Q Schrag JD Hussack G MacKenzie CR Tanha J Stability-diversity tradeoffs impose fundamental constraints on selection of synthetic human VH/VL single-domain antibodies from in vitro display libraries Frontiers in Immunology 2017 8 1759 29375542 PMC5763143
  66. [67]Hamers-Casterman C Atarhouch T Muyldermans S Robinson G Hamers C Songa EB Bendahman N Hamers R Naturally occurring antibodies devoid of light chains Nature 1993 363 446 448 8502296
  67. [68]Maassa DR Sepulvedac J Pernthanerb A Shoemakerc CB Alpaca (Lama pacos) as a convenient source of recombinant camelid heavy chain antibodies (VHHs) Journal of Immunological Methods 2007 324 13 25 17568607 PMC2014515
  68. [69]Sabir JSM Atef A El-Domyati FM Edris S Hajrah N Alzohairy AM Bahieldin A Construction of naïve camelids VHH repertoire in phage display-based library Comptes Rendus Biologies 2014 337 244 249 24702893
  69. [70]Govaert J Pellis M Deschacht N Vincke C Conrath K Muyldermans S Saerens D Dual beneficial effect of interloop disulfide bond for single domain antibody fragments Journal of Biological Chemistry 2012 287 1970 1979 22128183 PMC3283254
  70. [71]Liu JL Goldman ER Zabetakis D Walper SA Turner KB Shriver-Lake LC Anderson GP Enhanced production of a single domain antibody with an engineered stabilizing extra disulfide bond Microbial Cell Factories 2015 14 158 26449768 PMC4599338
  71. [72]Dona V Urrutia M Bayardo M Alzogaray V Goldbaum FA Chirdo FG Single domain antibodies are specially suited for quantitative determination of gliadins under denaturing conditions Journal of Agriculture and Food Chemistry 2010 58 918 926 20039674
  72. [73]De Vos J Devoogdt N Lahoutte T Muyldermans S Camelid single-domain antibody-fragment engineering for (pre)clinical in vivo molecular imaging applications: Adjusting the bullet to its target Expert Opinion on Biological Therapy 2013 13 1149 1160 23675652
  73. [75]Huang L Gainkam LO Caveliers V Vanhove C Keyaerts M De Baetselier P Bossuyt A Revets H Lahoutte T SPECT imaging with 99mTc-labeled EGFR-specific nanobody for in vivo monitoring of EGFR expression Molecular Imaging & Biology 2008 10 167 175 18297364
  74. [76]Schoonooghe S Laoui D Van Ginderachter JA Devoogdt N Lahoutte T De Baetselier P Raes G Novel applications of nanobodies for in vivo bio-imaging of inflamed tissues in inflammatory diseases and cancer Immunobiology 2012 217 1266 1272 22884356
  75. [77]Keyaerts M Xavier C Heemskerk J Devoogdt N Everaert H Ackaert C Vanhoeij M Duhoux FP Gevaert T Simon P Schallier D Fontaine C Vaneycken I Vanhove C De Greve J Lamote J Caveliers V Lahoutte T Phase I study of 68 Ga-HER2-nanobody for PET/CT assessment of HER2 expression in breast carcinoma Journal of Nuclear Medicine 2016 57 27 33 26449837
  76. [78]Mejias MP Hiriart Y Lauche C Fernandez-Brando RJ Pardo R Bruballa A Ramos MV Goldbaum FA Palermo MS Zylberman V Development of camelid single chain antibodies against Shiga toxin type 2 (Stx2) with therapeutic potential against hemolytic uremic syndrome (HUS) Scientific Reports 2016 6 24913 27118524 PMC4847011
  77. [79]Malik AA Imtong C Sookrung N Katzenmeier G Chaicumpa W Angsuthanasombat C Structural characterization of humanized nanobodies with neutralizing activity against the Bordetella pertussis CyaA-hemolysin: Implications for a potential epitope of toxin-protective antigen Toxins (Basel) 2016 8 99 27043627 PMC4848625
  78. [80]Lemaire M D’huyvetter M Lahoutte T Van Valckenborgh E Menu E De Bruyne E Kronenberger P Wernery U Muyldermans S Devoogdt N Vanderkerken K Imaging and radioimmunotherapy of multiple myeloma with anti-idiotypic Nanobodies Leukemia 2014 28 444 447 24166214
  79. [81]Comor L Dolinska S Bhide K Pulzova L Jiménez-Munguía I Bencurova E Flachbartova Z Potocnakova L Kanova E Bhide M Joining the in vitro immunization of alpaca lymphocytes and phage display: rapid and cost effective pipeline for sdAb synthesis Microbial Cell Factories 2017 16 13 28114943 PMC5259998
  80. [82]Monegal A Ami D Martinelli C Huang H Aliprandi M Capasso P Francavilla C Ossolengo G de Marco A Immunological applications of single domain llama recombinant antibodies isolated from a naïve library Protein Engineering, Design & Selection 2009 22 273 280 19196718
  81. [83]Dong J Thompson AA Fan Y Lou J Conrad F Ho M Pires-Alves M Wilson BA Stevens RC Marks JD A single-domain llama antibody potently inhibits the enzymatic activity of botulinum neurotoxin by binding to the non-catalytic alpha-exosite binding region Journal of Molecular Biology 2010 397 1106 1118 20138889 PMC2903050
  82. [84]Thanongsaksrikul J Srimanote P Maneewatch S Choowongkomon K Tapchaisri P Makino S Kurazono H Chaicumpa W A VHH that neutralizes the zinc metalloproteinase activity of botulinum neurotoxin type A Journal of Biological Chemistry 2010 285 9657 9666 20093370 PMC2843216
  83. [85]Verheesen P de Roussis A Haard HJ Groot AJ den Stam JC Dunnen JT Frants RR Verkleij AJ Theo Verrips C van der Maarel SM Reliable and controllable antibody fragment selections from Camelid non-immune libraries for target validation Biochimica et Biophysica Acta 2006 1764 1307 1319 16872921
  84. [86]Saerens D Pellis M Loris R Pardon E Dumoulin M Matagne A Wyns L Muyldermans S Conrath K Identification of a universal VHH framework to graft non-canonical antigen-binding loops of camel single-domain antibodies Journal of Molecular Biology 2005 352 597 607 16095608
  85. [87]Hagihara Y Mine S Uegaki K Stabilization of an immunoglobulin fold domain by an engineered disulfide bond at the buried hydrophobic region Journal of Biological Chemistry 2007 282 36489 36495 17932041
  86. [88]Saerens D Conrath K Govaert J Muyldermans S Disulfide bond introduction for general stabilization of immunoglobulin heavy-chain variable domains Journal of Molecular Biology 2008 377 478 488 18262543
  87. [89]Qasemi M Behdani M Shokrgozar MA Molla-Kazemiha V Mohseni-Kuchesfahani H Habibi-Anbouhi M Construction and expression of an anti-VEGFR2 nanobody-Fc fusionbody in NS0 host cells Protein Expression and Purification 2016 123 19 25 26996993
  88. [90]Dooley H Flajnik MF Porter AJ Selection and characterization of naturally occurring single-domain (IgNAR) antibody fragments from immunized sharks by phage display Molecular Immunology 2003 40 25 33 12909128
  89. [91]Zielonka S Ampting M Grzeschik J Könning D Barelle CJ Kolmar H Structural insights and biomedical potential of IgNAR scaffolds from sharks mAbs 2015 7 15 25 25523873 PMC4622739
  90. [92]Nuttall SD Krishnan UV Hattarki M De Gori R Irving RA Hudson PJ Isolation of a new antigen receptor from wobbegong sharks, and use as a scaffold for the display of protein loop libraries Molecular Immunology 2001 38 313 326 11566324
  91. [93]Nuttall SD Krishnan UV Hattarki Doughty Nathanielsz L Ally A Pike N Hudson RN Kortt PJ Kortt AA Irving RA A naturally occurring NAR variable domain binds the Kgp protease from Porphyrmonas gingivalis FEBS Letters 2002 516 80 86 11959108
  92. [94]Goodchild SA Dooley H Schoepp RJ Flajnik M Lonsdale SG Isolation and characterisation of Ebolavirus-specific recombinant antibody fragments from murine and shark immune libraries Molecular Immunology 2011 48 2027 2037 21752470
  93. [95]Leow CH Fischer K Leow CY Braet K Cheng Q McCarthy J Isolation and characterization of malaria PfHRP2 specific VNAR antibody fragments from immunized shark phage display library Malaria Journal 2018 17 383 30355309 PMC6201582
  94. [96]Liu JL Anderson GP Delehanty JB Baumann R Hayhurst A Goldman ER Selection of cholera toxin specific IgNAR single-domain antibodies from a naïve shark library Molecular Immunology 2007 44 1775 1783 17007931
  95. [97]Ohtani M Hikima J Jung TS Kondo H Hirono I Aoki T Construction of an artificially randomized IgNAR phage display library: Screening of variable region that bind to hen white lysozyme Marine Biotechnology 2013 15 56 62 22552958
  96. [98]Zadeh AS Grässer A Dinter H Hermes M Schindowski K Efficient onstruction and effective screening of synthetic domain antibody libraries Methods and Protocols 2019 2 17 PMC6481084 31164599
  97. [99]Kovaleva M Johnson K Steven J Barelle CJ Porter A Therpaeutic potetnia of shark anti-ICOSL VNAR domains is exemplified in a murine model of autoimmune non-infectious uveitis Frontiers in Immunology 2017 8 1121 28993766 PMC5622306
  98. [100]Hattori T Lai D Dementieva IS Montaño SP Kurosawa K Zheng Y Akin LR Świst-Rosowska KM Grzybowski AT Koide A Krajewski K Strahl BD Kelleher NL Ruthenburg AJ Koide S Antigen clasping by two antigen-binding sites of an exceptionally specific antibody for histone methylation Proceedings of the National Academy of Sciences USA 2016 113 2092 2097 PMC4776465 26862167
  99. [101]Henry KA Tanha J Hussack G Identification of cross-reactive single-domain antibodies against serum albumin using next-generation DNA sequencing Protein Engineering, Design & Selection 2015 28 379 383 26319004
  100. [102]Skottrup PD Leonard P Kaczmarek JZ Veillard F Enghild JJ O’Kennedy R Sroka A Clausen RP Potempa J Riise E Diagnostic evaluation of a nanobody with picomolar affinity toward the protease RgpB from Porphyromonas gingivalis Analytical Biochemistry 2011 415 158 167 21569755 PMC3114108

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Authors
Reader, R. H., Workman, R. G., Maddison, B. C., & Gough, K. C.
Affiliations
University of Nottingham (GB)
Corresponding author
Gough, Kevin C.
ORCID
Gough, Kevin C.
Venue
Molecular Biotechnology
Publisher
Springer Science and Business Media LLC
Published
2019-08-29
Volume
61
Issue
11
Pages
801-815
ISSN
  • 1073-6085 (ISSN-L)
  • 1559-0305
DOI
10.1007/s12033-019-00207-0
PMC
PMC6785589
OpenAlex
W2970957853
Cited by
41
References
2
Citations by year
2026: 5 · 2025: 7 · 2024: 3 · 2023: 3 · 2022: 9 · 2021: 9 · 2020: 5
FWCI
0.86
Type
journal article
Language
en
Open access
Licence
Locations
  • Molecular Biotechnology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Repository@Nottingham (University of Nottingham) (publishedVersion, other-oa)
  • Repository@Nottingham (University of Nottingham) (submittedVersion, cc-by)
Funders
Biotechnology and Biological Sciences Research Council (BB/J014508/1)
Topics
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Monoclonal and Polyclonal Antibodies Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein purification and stability
  • Physical Sciences › Environmental Science › Ecology › Bacteriophages and microbial interactions
Keywords
phage display, antibody libraries, Fab fragment, scFv, nanobodies, codon optimization, signal peptide, molecular chaperones, isomerase, therapeutic antibodies, antibody selection
MeSH terms
Camelidae, Animals, Antibody Affinity, Bacteriophages, Genetic Vectors, Humans, Immunoglobulin G, Immunoglobulin Fab Fragments, Sharks, Peptide Library, Complementarity Determining Regions, Single-Chain Antibodies, Cell Surface Display Techniques

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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