Advertisement

Chemoenzymatic Bioconjugation of Antibodies: Linking Proteins for Biomedical Applications

  • Soo Khim Chan
  • Yee Siew Choong
  • Chee Yuen Gan
  • Theam Soon Lim
Chapter

Abstract

Antibodies are useful biomolecules applied in many biomedical applications. The selectivity and specificity of antibodies against the target antigens have gained wide interest for both diagnostic and therapeutic applications. The antibodies are capable of functioning as target-specific carriers to allow site-specific delivery of payloads. However, the challenge has always revolved around the ability to attach designer proteins, enzymes, or drugs to the antibody molecule. The conventional approach involves the use of chemical-based modifications with the introduction of chemical linkers and alteration of chemical functional groups to initiate a covalent attachment of molecules to the antibodies. However, the use of chemically modified strategies to attach antibodies to various molecules has provided several setbacks throughout the years. The major consideration involves the conjugation efficiency, the yield of conjugated product recovered post-conjugation, and more importantly the effects to the antibody-binding sites. Therefore, the introduction of bioconjugation approaches utilizing biologically active enzymes to initiate conjugation processes provided researchers with a much-anticipated alternative that was less toxic to the native proteins. This chapter focuses on the application of biologically inspired enzymes that have been used successfully to conjugate proteins or drugs to antibodies in a “green” manner. The enzymes highlighted in this chapter would include sortase, transglutaminase, and formylglycine-generating enzymes. The chapter also highlights the applications of these methods to generate conjugates that have been applied either for diagnostic or therapeutic application.

Keywords

Antibody Chemoenzymatic Formylglycine-generating enzyme Sortase Transglutaminase 

Notes

Acknowledgment

The authors would like to acknowledge the support of the Malaysian Ministry of Education through the Higher Institution Centre of Excellence (HICoE) Grant (Grant No.311/CIPPM/44001005) and Universiti Sains Malaysia RUI Grant (1001/CABR/8011045).

References

  1. Acchione M, Kwon H, Jochheim CM et al (2012) Impact of linker and conjugation chemistry on antigen binding, Fc receptor binding and thermal stability of model antibody-drug conjugates. MAbs 4:362–372PubMedPubMedCentralCrossRefGoogle Scholar
  2. Agarwal P, Bertozzi CR (2015) Site-specific antibody–drug conjugates: the nexus of bioorthogonal chemistry, protein engineering, and drug development. Bioconjug Chem 26:176–192PubMedCrossRefGoogle Scholar
  3. Akkapeddi P, Azizi S-A, Freedy AM et al (2016) Construction of homogeneous antibody–drug conjugates using site-selective protein chemistry. Chem Sci 7:2954–2963PubMedPubMedCentralCrossRefGoogle Scholar
  4. Alberts B, Johnson A, Lewis J et al (2002) The adaptive immune system. Garland Science, New YorkGoogle Scholar
  5. Ando H, Adachi M, Umeda K et al (1989) Purification and characteristics of a novel transglutaminase derived from microorganisms. Agric Biol Chem 53:2613–2617Google Scholar
  6. Appel MJ, Bertozzi CR (2014) Formylglycine, a post-translationally generated residue with unique catalytic capabilities and biotechnology applications. ACS Chem Biol 10:72–84CrossRefGoogle Scholar
  7. Autuori F, Farrace MG, Oliverio S et al (1998) “Tissue” transglutaminase and apoptosis. Adv Biochem Eng Biotechnol 62:129–136PubMedGoogle Scholar
  8. Badescu G, Bryant P, Bird M et al (2014) Bridging disulfides for stable and defined antibody drug conjugates. Bioconjug Chem 25:1124–1136PubMedCrossRefGoogle Scholar
  9. Bailon P, Won C-Y (2009) PEG-modified biopharmaceuticals. Expert Opin Drug Deliv 6:1–16PubMedCrossRefGoogle Scholar
  10. Basle E, Joubert N, Pucheault M (2010) Protein chemical modification on endogenous amino acids. Chem Biol 17:213–227PubMedCrossRefGoogle Scholar
  11. Beerli RR, Hell T, Merkel AS et al (2015) Sortase enzyme-mediated generation of site-specifically conjugated antibody drug conjugates with high in vitro and in vivo potency. PLoS One 10:e0131177PubMedPubMedCentralCrossRefGoogle Scholar
  12. Behrens CR, Liu B (2014) Methods for site-specific drug conjugation to antibodies. MAbs 6:46–53PubMedCrossRefGoogle Scholar
  13. Boylan NJ, Zhou W, Proos RJ et al (2013) Conjugation site heterogeneity causes variable electrostatic properties in Fc conjugates. Bioconjug Chem 24:1008–1016PubMedPubMedCentralCrossRefGoogle Scholar
  14. Brotzel F, Mayr H (2007) Nucleophilicities of amino acids and peptides. Org Biomol Chem 5:3814–3820PubMedCrossRefGoogle Scholar
  15. Brun M-P, Gauzy-Lazo L (2013) Protocols for lysine conjugation. In: L D (ed) Antibody-drug conjugates. Methods in molecular biology (Methods and protocols). Humana Press, Totowa, pp 173–187CrossRefGoogle Scholar
  16. Cal PM, Bernardes GJ, Gois PM (2014) Cysteine-selective reactions for antibody conjugation. Angew Chem Int Ed 53:10585–10587CrossRefGoogle Scholar
  17. Caminschi I, Lahoud MH, Shortman K (2009) Enhancing immune responses by targeting antigen to DC. Eur J Immunol 39:931–938PubMedCrossRefGoogle Scholar
  18. Carlson BL, Ballister ER, Skordalakes E et al (2008) Function and structure of a prokaryotic formylglycine-generating enzyme. J Biol Chem 283:20117–20125PubMedPubMedCentralCrossRefGoogle Scholar
  19. Carrico IS, Carlson BL, Bertozzi CR (2007) Introducing genetically encoded aldehydes into proteins. Nat Chem Biol 3:321–322PubMedCrossRefGoogle Scholar
  20. Cascioferro S, Totsika M, Schillaci D (2014) Sortase A: an ideal target for anti-virulence drug development. Microb Pathog 77:105–112PubMedCrossRefGoogle Scholar
  21. Chalker JM, Bernardes GJ, Lin YA et al (2009) Chemical modification of proteins at cysteine: opportunities in chemistry and biology. Chem Asian J 4:630–640PubMedCrossRefGoogle Scholar
  22. Chapman AP (2002) PEGylated antibodies and antibody fragments for improved therapy: a review. Adv Drug Deliv Rev 54:531–545PubMedCrossRefGoogle Scholar
  23. Chen JS, Mehta K (1999) Tissue transglutaminase: an enzyme with a split personality. Int J Biochem Cell Biol 31:817–836PubMedCrossRefGoogle Scholar
  24. Chen I, Dorr BM, Liu DR (2011) A general strategy for the evolution of bond-forming enzymes using yeast display. Proc Natl Acad Sci 108:11399–11404PubMedCrossRefGoogle Scholar
  25. Chen L, Cohen J, Song X et al (2016) Improved variants of Srt A for site-specific conjugation on antibodies and proteins with high efficiency. Sci Rep 6:31899PubMedPubMedCentralCrossRefGoogle Scholar
  26. Chih HW, Gikanga B, Yang Y et al (2011) Identification of amino acid residues responsible for the release of free drug from an antibody–drug conjugate utilizing lysine–succinimidyl ester chemistry. J Pharm Sci 100:2518–2525PubMedCrossRefGoogle Scholar
  27. Cohen JD, Zou P, Ting AY (2012) Site-specific protein modification using lipoic acid ligase and bis-aryl hydrazone formation. ChemBioChem 13:888–894PubMedPubMedCentralCrossRefGoogle Scholar
  28. Comfort D, Clubb RT (2004) A comparative genome analysis identifies distinct sorting pathways in gram-positive bacteria. Infect Immun 72:2710–2722PubMedPubMedCentralCrossRefGoogle Scholar
  29. Coquerel Y, Boddaert T, Presset M et al (2010) Ideas in chemistry and molecular sciences: advances in synthetic chemistry. Wiley, WeinheimGoogle Scholar
  30. Coussons P, Price N, Kelly S et al (1992) Factors that govern the specificity of transglutaminase-catalyzed modification of proteins and peptides. Biochem J 282:929–930PubMedPubMedCentralCrossRefGoogle Scholar
  31. Cowan AJ, Laszlo GS, Estey EH et al (2013) Antibody-based therapy of acute myeloid leukemia with gemtuzumab ozogamicin. Front Biosci (Landmark Edition) 18:1311CrossRefGoogle Scholar
  32. Crankshaw MW, Grant GA (2001) Modification of cysteine. Curr Protoc Protein Sci 3:15.1.1–15.1.18Google Scholar
  33. Dale JW (2012) Understanding microbes: an introduction to a small world. Wiley, New YorkGoogle Scholar
  34. Del Duca S, Verderio E, Serafini-Fracassini D et al (2014) The plant extracellular transglutaminase: what mammal analogues tell. Amino Acids 46:777–792PubMedCrossRefGoogle Scholar
  35. Dennler P, Chiotellis A, Fischer E et al (2014) Transglutaminase-based chemo-enzymatic conjugation approach yields homogeneous antibody–drug conjugates. Bioconjug Chem 25:569–578PubMedCrossRefGoogle Scholar
  36. Dennler P, Fischer E, Schibli R (2015) Antibody conjugates: from heterogeneous populations to defined reagents. Antibodies 4:197–224CrossRefGoogle Scholar
  37. Dierks T, Schmidt B, Von Figura K (1997) Conversion of cysteine to formylglycine: a protein modification in the endoplasmic reticulum. Proc Natl Acad Sci 94:11963–11968PubMedCrossRefGoogle Scholar
  38. Dimitrov DS (2010) Therapeutic antibodies, vaccines and antibodyomes. MAbs 2:347–356PubMedPubMedCentralCrossRefGoogle Scholar
  39. Dorywalska M, Strop P, Melton-Witt JA et al (2015) Site-dependent degradation of a non-cleavable auristatin-based linker-payload in rodent plasma and its effect on ADC efficacy. PLoS One 10:e0132282PubMedPubMedCentralCrossRefGoogle Scholar
  40. Dozier JK, Khatwani SL, Wollack JW et al (2014) Engineering protein farnesyltransferase for enzymatic protein labeling applications. Bioconjug Chem 25:1203–1212PubMedPubMedCentralCrossRefGoogle Scholar
  41. Drake PM, Albers AE, Baker J et al (2014) Aldehyde tag coupled with HIPS chemistry enables the production of ADCs conjugated site-specifically to different antibody regions with distinct in vivo efficacy and PK outcomes. Bioconjug Chem 25:1331–1341PubMedPubMedCentralCrossRefGoogle Scholar
  42. Dramsi S, Trieu-Cuot P, Bierne H (2005) Sorting sortases: a nomenclature proposal for the various sortases of gram-positive bacteria. Res Microbiol 156:289–297PubMedCrossRefGoogle Scholar
  43. Duarte JN, Cragnolini JJ, Swee LK, Bilate AM, Bader J, Ingram JR, Rashidfarrokhi A, Fang T, Schiepers A, Hanke L (2016) Generation of Immunity against Pathogens via Single-Domain Antibody–Antigen Constructs. J Immunol 197(12): 4838–4847PubMedCrossRefGoogle Scholar
  44. Farias SE, Strop P, Delaria K et al (2014) Mass spectrometric characterization of transglutaminase based site-specific antibody–drug conjugates. Bioconjug Chem 25:240–250PubMedCrossRefGoogle Scholar
  45. Fierer JO, Veggiani G, Howarth M (2014) SpyLigase peptide–peptide ligation polymerizes affibodies to enhance magnetic cancer cell capture. Proc Natl Acad Sci 111:E1176–E1181PubMedCrossRefGoogle Scholar
  46. Folk J, Cole P (1966) Mechanism of action of Guinea pig liver transglutaminase I. Purification and properties of the enzyme: identification of a functional cysteine essential for activity. J Biol Chem 241:5518–5525PubMedGoogle Scholar
  47. Frenzel A, Schirrmann T, Hust M (2016) Phage display-derived human antibodies in clinical development and therapy. MAbs 8:1177–1194PubMedPubMedCentralCrossRefGoogle Scholar
  48. Garandeau C, Réglier-Poupet H, Dubail I et al (2002) The sortase SrtA of Listeria monocytogenes is involved in processing of internalin and in virulence. Infect Immun 70:1382–1390PubMedPubMedCentralCrossRefGoogle Scholar
  49. Gong H, Holcomb I, Ooi A et al (2016) Simple method to prepare oligonucleotide-conjugated antibodies and its application in multiplex protein detection in single cells. Bioconjug Chem 27:217–225PubMedCrossRefGoogle Scholar
  50. Griffin M, Casadio R, Bergamini CM (2002) Transglutaminases: nature’s biological glues. Biochem J 368:377–396PubMedPubMedCentralCrossRefGoogle Scholar
  51. Grünewald J, Klock HE, Cellitti SE et al (2015) Efficient preparation of site-specific antibody–drug conjugates using phosphopantetheinyl transferases. Bioconjug Chem 26:2554–2562PubMedCrossRefGoogle Scholar
  52. Gundersen MT, Keillor JW, Pelletier JN (2014) Microbial transglutaminase displays broad acyl-acceptor substrate specificity. Appl Microbiol Biotechnol 98:219–230PubMedCrossRefGoogle Scholar
  53. Hagemeyer CE, Alt K, Johnston AP et al (2015) Particle generation, functionalization and sortase A–mediated modification with targeting of single-chain antibodies for diagnostic and therapeutic use. Nat Protoc 10:90–105PubMedCrossRefGoogle Scholar
  54. Hamann PR, Hinman LM, Hollander I et al (2002) Gemtuzumab ozogamicin, a potent and selective anti-CD33 antibody− calicheamicin conjugate for treatment of acute myeloid leukemia. Bioconjug Chem 13:47–58PubMedCrossRefGoogle Scholar
  55. Hofer T, Skeffington LR, Chapman CM et al (2009) Molecularly defined antibody conjugation through a selenocysteine interface. Biochemistry 48:12047–12057PubMedPubMedCentralCrossRefGoogle Scholar
  56. Hull EA, Livanos M, Miranda E et al (2014) Homogeneous bispecifics by disulfide bridging. Bioconjug Chem 25:1395–1401PubMedPubMedCentralCrossRefGoogle Scholar
  57. Ikura K, Sasaki R, Motoki M (1992) Use of transglutaminase in quality-improvement and processing of food proteins. Comments. Agric Food Chem 2:389–407Google Scholar
  58. 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 6:19338PubMedPubMedCentralCrossRefGoogle Scholar
  59. Jackson DY (2016) Processes for constructing homogeneous antibody drug conjugates. Org Process Res Dev 20:852–866CrossRefGoogle Scholar
  60. Jazayeri MH, Amani H, Pourfatollah AA et al (2016) Various methods of gold nanoparticles (GNPs) conjugation to antibodies. Sens Biosensing Res 9:17–22CrossRefGoogle Scholar
  61. Jeger S, Zimmermann K, Blanc A et al (2010) Site-specific and stoichiometric modification of antibodies by bacterial transglutaminase. Angew Chem Int Ed 49:9995–9997CrossRefGoogle Scholar
  62. Jevševar S, Kusterle M, Kenig M (2012) PEGylation of antibody fragments for half-life extension. In: Antibody methods and protocols. Springer, New York, pp 233–246CrossRefGoogle Scholar
  63. Johansson L, Gafvelin G, Arnér ES (2005) Selenocysteine in proteins—properties and biotechnological use. Biochim Biophys Acta 1726:1–13PubMedCrossRefGoogle Scholar
  64. Johnston MV, Adams HP, Fatemi A (2016) Neurobiology of disease. Oxford University Press, Oxford/New YorkGoogle Scholar
  65. Jones MW, Strickland RA, Schumacher FF et al (2012) Polymeric dibromomaleimides as extremely efficient disulfide bridging bioconjugation and pegylation agents. J Am Chem Soc 134:1847–1852PubMedCrossRefGoogle Scholar
  66. Josten A, Haalck L, Spener F et al (2000) Use of microbial transglutaminase for the enzymatic biotinylation of antibodies. J Immunol Methods 240:47–54PubMedCrossRefGoogle Scholar
  67. Junutula JR, Raab H, Clark S et al (2008) Site-specific conjugation of a cytotoxic drug to an antibody improves the therapeutic index. Nat Biotechnol 26:925–932PubMedCrossRefGoogle Scholar
  68. Kamiya N, Mori Y (2015) Substrate engineering of microbial transglutaminase for site-specific protein modification and bioconjugation. In: Hitomi K, Kojima S, Fesus L (eds) Transglutaminases. Springer, Tokyo, pp 373–383Google Scholar
  69. Kamiya N, Takazawa T, Tanaka T et al (2003) Site-specific cross-linking of functional proteins by transglutamination. Enzym Microb Technol 33:492–496CrossRefGoogle Scholar
  70. Kieliszek M, Misiewicz A (2014) Microbial transglutaminase and its application in the food industry. A review. Folia Microbiol (Praha) 59:241–250CrossRefGoogle Scholar
  71. Kim HJ, Ha S, Lee HY et al (2015) ROSics: chemistry and proteomics of cysteine modifications in redox biology. Mass Spectrom Rev 34:184–208PubMedCrossRefGoogle Scholar
  72. Kline T, Steiner AR, Penta K et al (2015) Methods to make homogenous antibody drug conjugates. Pharm Res 32:3480–3493PubMedCrossRefGoogle Scholar
  73. Köhler G, Milstein C (1975) Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256:495–497PubMedCrossRefGoogle Scholar
  74. Koniev O, Wagner A (2015) Developments and recent advancements in the field of endogenous amino acid selective bond forming reactions for bioconjugation. Chem Soc Rev 44:5495–5551PubMedCrossRefGoogle Scholar
  75. 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 6:354–366PubMedCrossRefGoogle Scholar
  76. Landgrebe J, Dierks T, Schmidt B et al (2003) The human SUMF1 gene, required for posttranslational sulfatase modification, defines a new gene family which is conserved from pro-to eukaryotes. Gene 316:47–56PubMedCrossRefGoogle Scholar
  77. Lee JH, Song C, Kim DH et al (2013) Glutamine (Q)-peptide screening for transglutaminase reaction using mRNA display. Biotechnol Bioeng 110:353–362PubMedCrossRefGoogle Scholar
  78. Levary DA, Parthasarathy R, Boder ET et al (2011) Protein-protein fusion catalyzed by sortase A. PLoS One 6:e18342PubMedPubMedCentralCrossRefGoogle Scholar
  79. Li X, Yang J, Rader C (2014) Antibody conjugation via one and two C-terminal selenocysteines. Methods 65:133–138PubMedCrossRefGoogle Scholar
  80. Li W, Prabakaran P, Chen W et al (2016) Antibody aggregation: insights from sequence and structure. Antibodies 5:19CrossRefGoogle Scholar
  81. Lin C-W, Ting AY (2006) Transglutaminase-catalyzed site-specific conjugation of small-molecule probes to proteins in vitro and on the surface of living cells. J Am Chem Soc 128:4542–4543PubMedPubMedCentralCrossRefGoogle Scholar
  82. Lorand L, Graham RM (2003) Transglutaminases: crosslinking enzymes with pleiotropic functions. Mol Cell Biol 4:140–156Google Scholar
  83. Luciano FB, Arntfield S (2012) Use of transglutaminases in foods and potential utilization of plants as a transglutaminase source–review. Biotemas 25:1–11Google Scholar
  84. Mariathasan S, Tan M-W (2017) Antibody–antibiotic conjugates: a novel therapeutic platform against bacterial infections. Trends Mol Med 23:135–149PubMedCrossRefGoogle Scholar
  85. Mazmanian SK, Liu G, Ton-That H et al (1999) Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 285:760–763PubMedCrossRefGoogle Scholar
  86. McAuley A, Jacob J, Kolvenbach CG et al (2008) Contributions of a disulfide bond to the structure, stability, and dimerization of human IgG1 antibody CH3 domain. Protein Sci 17:95–106PubMedPubMedCentralCrossRefGoogle Scholar
  87. McCombs JR, Owen SC (2015) Antibody drug conjugates: design and selection of linker, payload and conjugation chemistry. AAPS J 17:339–351PubMedPubMedCentralCrossRefGoogle Scholar
  88. McCracken MN, Radu CG (2015) Targeted noninvasive imaging of the innate immune response. Proc Natl Acad Sci 112:5868–5869PubMedCrossRefGoogle Scholar
  89. McDonagh CF, Turcott E, Westendorf L et al (2006) Engineered antibody–drug conjugates with defined sites and stoichiometries of drug attachment. Protein Eng Des Sel 19:299–307PubMedCrossRefGoogle Scholar
  90. McFarland JM, Rabuka D (2015) Recent advances in chemoenzymatic bioconjugation methods. Org Chem Insights 5:7–14CrossRefGoogle Scholar
  91. McLaughlin J, LoRusso P (2016) Antibody–Drug Conjugates (ADCs) in clinical development. In: Olivier KJ Jr, Hurvitz SA (eds) Antibody-drug conjugates: fundamentals, drug development, and clinical outcomes to target cancer. Wiley, Hoboken, pp 321–344CrossRefGoogle Scholar
  92. Mindt TL, Jungi V, Wyss S et al (2007) Modification of different IgG1 antibodies via glutamine and lysine using bacterial and human tissue transglutaminase. Bioconjug Chem 19:271–278PubMedCrossRefGoogle Scholar
  93. Motoki M, Nio N (1983) Crosslinking between different food proteins by transglutaminase. J Food Sci 48:561–566CrossRefGoogle Scholar
  94. Navarre WW, Schneewind O (1994) Proteolytic cleavage and cell wall anchoring at the LPXTG motif of surface proteins in Gram-positive bacteria. Mol Microbiol 14:115–121PubMedCrossRefGoogle Scholar
  95. Ohtsuka T, Ota M, Nio N et al (2000) Comparison of substrate specificities of transglutaminases using synthetic peptides as acyl donors. Biosci Biotechnol Biochem 64:2608–2613PubMedCrossRefGoogle Scholar
  96. Okeley NM, Toki BE, Zhang X et al (2013) Metabolic engineering of monoclonal antibody carbohydrates for antibody–drug conjugation. Bioconjug Chem 24:1650–1655PubMedCrossRefGoogle Scholar
  97. Ornes S (2013) Antibody–drug conjugates. Proc Natl Acad Sci U S A 110:13695PubMedPubMedCentralCrossRefGoogle Scholar
  98. Pallen MJ, Lam AC, Antonio M et al (2001) An embarrassment of sortases–a richness of substrates? Trends Microbiol 9:97–101PubMedCrossRefGoogle Scholar
  99. Panowski S, Bhakta S, Raab H et al (2014) Site-specific antibody drug conjugates for cancer therapy. MAbs 6:34–45PubMedCrossRefGoogle Scholar
  100. Parthasarathy R, Subramanian S, Boder ET (2007) Sortase A as a novel molecular “stapler” for sequence-specific protein conjugation. Bioconjug Chem 18:469–476PubMedCrossRefGoogle Scholar
  101. Pasut G, Veronese FM (2012) State of the art in PEGylation: the great versatility achieved after forty years of research. J Control Release 161:461–472PubMedCrossRefGoogle Scholar
  102. Perez HL, Cardarelli PM, Deshpande S et al (2014) Antibody–drug conjugates: current status and future directions. Drug Discov Today 19:869–881PubMedCrossRefGoogle Scholar
  103. Perry AM, Ton-That H, Mazmanian SK et al (2002) Anchoring of surface proteins to the cell wall of Staphylococcus aureus III Lipid II is an in vivo peptidoglycan substrate for sortase-catalyzed surface protein anchoring. J Biol Chem 277:16241–16248PubMedCrossRefGoogle Scholar
  104. Pharma F (2010) FDA: Pfizer voluntarily withdraws cancer treatment Mylotarg from US market [Online]. Available: https://www.fiercepharma.com/pharma/fda-pfizer-voluntarily-withdraws-cancer-treatment-mylotarg-from-u-s-market. Accessed June 21 2010
  105. Rachel NM, Pelletier JN (2013) Biotechnological applications of transglutaminases. Biomol Ther 3:870–888Google Scholar
  106. Rashidian M, Dozier JK, Distefano MD (2013) Enzymatic labeling of proteins: techniques and approaches. Bioconjug Chem 24:1277–1294PubMedPubMedCentralCrossRefGoogle Scholar
  107. Rickert M, Strop P, Lui V et al (2016) Production of soluble and active microbial transglutaminase in Escherichia coli for site-specific antibody drug conjugation. Protein Sci 25:442–455PubMedCrossRefGoogle Scholar
  108. Roux KJ, Kim DI, Raida M et al (2012) A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells. J Cell Biol 196:801–810PubMedPubMedCentralCrossRefGoogle Scholar
  109. Rowland A, Pietersz GA, McKenzie IF (1993) Preclinical investigation of the antitumour effects of anti-CD19-idarubicin immunoconjugates. Cancer Immunol Immunother 37:195–202PubMedCrossRefGoogle Scholar
  110. Sakamoto T, Sawamoto S, Tanaka T et al (2010) Enzyme-mediated site-specific antibody-protein modification using a ZZ domain as a linker. Bioconjug Chem 21:2227–2233PubMedCrossRefGoogle Scholar
  111. Schroeder DD, Tankersky DL, Lundblad JL (1981) A new preparation of modified immune serum globulin (human) suitable for intravenous administration. Vox Sang 40:383–394PubMedCrossRefGoogle Scholar
  112. Schumacher D, Hackenberger CP, Leonhardt H et al (2016) Current status: site-specific antibody drug conjugates. J Clin Immunol 36:100–107PubMedPubMedCentralCrossRefGoogle Scholar
  113. Senter PD, Sievers EL (2012) The discovery and development of brentuximab vedotin for use in relapsed Hodgkin lymphoma and systemic anaplastic large cell lymphoma. Nat Biotechnol 30:631–637PubMedCrossRefGoogle Scholar
  114. Sesay MA (2003) Monoclonal antibody conjugation via chemical modification. Biopharm Int 16:32–39Google Scholar
  115. Sharkey RM, Goldenberg DM (2008) Use of antibodies and immunoconjugates for the therapy of more accessible cancers. Adv Drug Deliv Rev 60:1407–1420PubMedPubMedCentralCrossRefGoogle Scholar
  116. Shinya A, Yamashita K, Kohno H et al (2000) Involvement of transglutaminase in the receptor-mediated endocytosis of mouse peritoneal macrophages. Biol Pharm Bull 23:1511–1513CrossRefGoogle Scholar
  117. Siegmund V, Schmelz S, Dickgiesser S et al (2015) Locked by design: a conformationally constrained transglutaminase tag enables efficient site-specific conjugation. Angew Chem Int Ed 54:13420–13424CrossRefGoogle Scholar
  118. Siegmund V, Piater B, Zakeri B et al (2016) Spontaneous isopeptide bond formation as a powerful tool for engineering site-specific antibody-drug conjugates. Sci Rep 6:39291PubMedPubMedCentralCrossRefGoogle Scholar
  119. Smith EL, Giddens JP, Iavarone AT et al (2014) Chemoenzymatic Fc glycosylation via engineered aldehyde tags. Bioconjug Chem 25:788–795PubMedPubMedCentralCrossRefGoogle Scholar
  120. Sochaj AM, Świderska KW, Otlewski J (2015) Current methods for the synthesis of homogeneous antibody–drug conjugates. Biotechnol Adv 33:775–784PubMedCrossRefGoogle Scholar
  121. Spolaore B, Raboni S, Satwekar AA et al (2016) Site-specific transglutaminase-mediated conjugation of interferon α-2b at glutamine or lysine residues. Bioconjug Chem 27:2695–2706PubMedCrossRefGoogle Scholar
  122. Steffen W, Ko FC, Patel J et al (2017) Discovery of a microbial transglutaminase enabling highly site-specific labeling of proteins. J Biol Chem 292:15622–15635PubMedPubMedCentralCrossRefGoogle Scholar
  123. Stephanopoulos N, Francis MB (2011) Choosing an effective protein bioconjugation strategy. Nat Chem Biol 7:876–884PubMedCrossRefGoogle Scholar
  124. Strop P (2014) Versatility of microbial transglutaminase. Bioconjug Chem 25:855–862PubMedCrossRefGoogle Scholar
  125. Strop P, Dorywalska MG, Rajpal A et al (2012 November 22) Engineered polypeptide conjugates and methods for making thereof using transglutaminase. PCT/IB2011/054899Google Scholar
  126. Strop P, Liu S-H, Dorywalska M et al (2013) Location matters: site of conjugation modulates stability and pharmacokinetics of antibody drug conjugates. Chem Biol 20:161–167PubMedCrossRefGoogle Scholar
  127. Strop P, Tran T-T, Dorywalska M et al (2016) RN927C, a site-specific trop-2 antibody–drug conjugate (ADC) with enhanced stability, is highly efficacious in preclinical solid tumor models. Mol Cancer Ther 15:2698–2708PubMedCrossRefGoogle Scholar
  128. Sueda S, Yoneda S, Hayashi H (2011) Site-specific labeling of proteins by using biotin protein ligase conjugated with fluorophores. ChemBioChem 12:1367–1375PubMedCrossRefGoogle Scholar
  129. Suedhoff T, Birckbichler P, Lee K et al (1990) Differential expression of transglutaminase in human erythroleukemia cells in response to retinoic acid. Cancer Res 50:7830–7834PubMedGoogle Scholar
  130. Sugimura Y, Hosono M, Wada F et al (2006) Screening for the preferred substrate sequence of transglutaminase using a phage-displayed peptide library identification of peptide substrates for TGASE 2 and factor XIIIA. J Biol Chem 281:17699–17706PubMedCrossRefGoogle Scholar
  131. Sugimura Y, Yokoyama K, Nio N et al (2008) Identification of preferred substrate sequences of microbial transglutaminase from Streptomyces mobaraensis using a phage-displayed peptide library. Arch Biochem Biophys 477:379–383PubMedCrossRefGoogle Scholar
  132. Sun MM, Beam KS, Cerveny CG et al (2005) Reduction− alkylation strategies for the modification of specific monoclonal antibody disulfides. Bioconjug Chem 16:1282–1290PubMedPubMedCentralCrossRefGoogle Scholar
  133. Swee LK, Guimaraes CP, Sehrawat S et al (2013) Sortase-mediated modification of αDEC205 affords optimization of antigen presentation and immunization against a set of viral epitopes. Proc Natl Acad Sci 110:1428–1433PubMedCrossRefGoogle Scholar
  134. Ta H, Prabhu S, Leitner E et al (2011) Enzymatic single-chain antibody tagging: a universal approach to targeted molecular imaging and cell homing in cardiovascular disease. Circ Res 109:365–373PubMedCrossRefGoogle Scholar
  135. Tesfaw A, Assefa F (2014) Applications of transglutaminase in textile, wool, and leather processing. Int J Tex Sci 3:64–69Google Scholar
  136. Theile CS, Witte MD, Blom AE et al (2013) Site-specific N-terminal labeling of proteins using sortase-mediated reactions. Nat Protoc 8:1800PubMedPubMedCentralCrossRefGoogle Scholar
  137. Tong H, Zhang L, Kaspar A et al (2013) Peptide-conjugation induced conformational changes in human IgG1 observed by optimized negative-staining and individual-particle electron tomography. Sci Rep 3:1089PubMedPubMedCentralCrossRefGoogle Scholar
  138. Torres M, Casadevall A (2008) The immunoglobulin constant region contributes to affinity and specificity. Trends Immunol 29:91–97PubMedCrossRefGoogle Scholar
  139. Tsuchikama K, An Z (2016) Antibody-drug conjugates: recent advances in conjugation and linker chemistries. Protein Cell 9(1):1–14Google Scholar
  140. van de Donk NW, Dhimolea E (2012) Brentuximab vedotin. MAbs 4:458–465 Taylor & FrancisPubMedPubMedCentralCrossRefGoogle Scholar
  141. von Behring E, Kitasato S (1890) The mechanism of immunity in animals to diphtheria and tetanus. Deutsche Med Wochenschr 16:1113–1114CrossRefGoogle Scholar
  142. Wagner K, Kwakkenbos MJ, Claassen YB et al (2014) Bispecific antibody generated with sortase and click chemistry has broad antiinfluenza virus activity. Proc Natl Acad Sci 111:16820–16825PubMedCrossRefGoogle Scholar
  143. Wakankar AA, Feeney MB, Rivera J et al (2010) Physicochemical stability of the antibody− drug conjugate trastuzumab-DM1: changes due to modification and conjugation processes. Bioconjug Chem 21:1588–1595PubMedCrossRefGoogle Scholar
  144. Wen X, Wu Q-P, Lu Y et al (2001) Poly (ethylene glycol)-conjugated anti-EGF receptor antibody C225 with radiometal chelator attached to the termini of polymer chains. Bioconjug Chem 12:545–553PubMedCrossRefGoogle Scholar
  145. Williamson DJ, Fascione MA, Webb ME et al (2012) Efficient N-terminal labeling of proteins by use of sortase. Angew Chem Int Ed 51:9377–9380CrossRefGoogle Scholar
  146. Witte MD, Cragnolini JJ, Dougan SK et al (2012) Preparation of unnatural N-to-N and C-to-C protein fusions. Proc Natl Acad Sci 109:11993–11998PubMedCrossRefGoogle Scholar
  147. Witte MD, Theile C, Wu T et al (2013) Production of unnaturally linked chimeric proteins using a combination of sortase-catalyzed transpeptidation and click chemistry. Nat Protoc 8:1808PubMedPubMedCentralCrossRefGoogle Scholar
  148. Wu P, Shui W, Carlson BL et al (2009) Site-specific chemical modification of recombinant proteins produced in mammalian cells by using the genetically encoded aldehyde tag. Proc Natl Acad Sci 106:3000–3005PubMedCrossRefGoogle Scholar
  149. Yokoyama K, Nio N, Kikuchi Y (2004) Properties and applications of microbial transglutaminase. Appl Microbiol Biotechnol 64:447–454PubMedCrossRefGoogle Scholar
  150. Yokoyama K, Utsumi H, Nakamura T et al (2010) Screening for improved activity of a transglutaminase from Streptomyces mobaraensis created by a novel rational mutagenesis and random mutagenesis. Appl Microbiol Biotechnol 87:2087–2096PubMedCrossRefGoogle Scholar
  151. York D, Baker J, Holder PG et al (2016) Generating aldehyde-tagged antibodies with high titers and high formylglycine yields by supplementing culture media with copper (II). BMC Biotechnol 16:23PubMedPubMedCentralCrossRefGoogle Scholar
  152. Younes A, Bartlett NL, Leonard JP et al (2010) Brentuximab vedotin (SGN-35) for relapsed CD30-positive lymphomas. N Engl J Med 363:1812–1821PubMedCrossRefGoogle Scholar
  153. Zuberbühler K, Casi G, Bernardes GJ et al (2012) Fucose-specific conjugation of hydrazide derivatives to a vascular-targeting monoclonal antibody in IgG format. Chem Commun 48:7100–7102CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Soo Khim Chan
    • 1
  • Yee Siew Choong
    • 1
  • Chee Yuen Gan
    • 2
  • Theam Soon Lim
    • 1
    • 2
  1. 1.Institute for Research in Molecular MedicineUniversiti Sains MalaysiaPenangMalaysia
  2. 2.Analytical Biochemistry Research CentreUniversiti Sains MalaysiaPenangMalaysia

Personalised recommendations