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Hagemeyer Heidt, A.K.N. Nair, H. Pearce, C. Von Zur Muhlen, X Enzymatic Single-Chain Antibody Tagging : A Universal Approach to Targeted Molecular Imaging and Cell Homing in Cardiovascular Disease H.T. Ta, S. Prabhu, E. Leitner, F. Jia, D. von Elverfeldt, Katherine E. Jackson, T. Heidt, A.K.N. Nair, H. Pearce, C. von zur Muhlen, X. Wang, K. Peter and C.E. Hagemeyer Circulation Research 2011, 109:365-373: originally published online June 23, 2011 doi: 10.1161/CIRCRESAHA.111.249375 Circulation Research is published by the American Heart Association. 7272 Greenville Avenue, Dallas, TX 72514 Copyright © 2011 American Heart Association. All rights reserved. Print ISSN: 0009-7330. Online ISSN: 1524-4571 The online version of this article, along with updated information and services, is located on the World Wide Web at: http://circres.ahajournals.org/content/109/4/365 Data Supplement (unedited) at: http://circres.ahajournals.org/content/suppl/2011/06/23/CIRCRESAHA.111.249375.DC1.html Subscriptions: Information about subscribing to Circulation Research is online at http://circres.ahajournals.org//subscriptions/ Permissions: Permissions & Rights Desk, Lippincott Williams & Wilkins, a division of Wolters Kluwer Health, 351 West Camden Street, Baltimore, MD 21202-2436. Phone: 410-528-4050. Fax: 410-528-8550. E-mail: [email protected] Reprints: Information about reprints can be found online at http://www.lww.com/reprints Downloaded from http://circres.ahajournals.org/ at Monash University on October 10, 2011 New Methods in Cardiovascular Biology Enzymatic Single-Chain Antibody Tagging A Universal Approach to Targeted Molecular Imaging and Cell Homing in Cardiovascular Disease H.T. Ta, S. Prabhu, E. Leitner, F. Jia, D. von Elverfeldt, Katherine E. Jackson, T. Heidt, A.K.N. Nair, H. Pearce, C. von zur Muhlen, X. Wang, K. Peter,* C.E. Hagemeyer* Rationale: Antibody-targeted delivery of imaging agents can enhance the sensitivity and accuracy of current imaging techniques. Similarly, homing of effector cells to disease sites increases the efficacy of regenerative cell therapy while reducing the number of cells required. Currently, targeting can be achieved via chemical conjugation to specific antibodies, which typically results in the loss of antibody functionality and in severe cell damage. An ideal conjugation technique should ensure retention of antigen-binding activity and functionality of the targeted biological component. Objective: To develop a biochemically robust, highly reproducible, and site-specific coupling method using the Staphylococcus aureus sortase A enzyme for the conjugation of a single-chain antibody (scFv) to nanoparticles and cells for molecular imaging and cell homing in cardiovascular diseases. This scFv specifically binds to activated platelets, which play a pivotal role in thrombosis, atherosclerosis, and inflammation. Methods and Results: The conjugation procedure involves chemical and enzyme-mediated coupling steps. The scFv was successfully conjugated to iron oxide particles (contrast agents for magnetic resonance imaging) and to model cells. Conjugation efficiency ranged between 50% and 70%, and bioactivity of the scFv after coupling was preserved. The targeting of scFv-coupled cells and nanoparticles to activated platelets was strong and specific as demonstrated in in vitro static adhesion assays, in a flow chamber system, in mouse intravital microscopy, and in in vivo magnetic resonance imaging of mouse carotid arteries. Conclusions: This unique biotechnological approach provides a versatile and broadly applicable tool for procuring targeted regenerative cell therapy and targeted molecular imaging in cardiovascular and inflamma- tory diseases and beyond. (Circ Res. 2011;109:365-373.) Key Words: molecular imaging Ⅲ platelets Ⅲ thrombosis Ⅲ antibodies Ⅲ targeted molecular therapy Ⅲ sortase A Ⅲ cell therapy argeted delivery increases the efficacy of drugs and groups are commonly distributed throughout the antibody Tregenerative cell therapy, reduces the dose required, structure. If the conjugation involves critical residues and consequently minimizes potential negative side ef- essential for antigen binding, the functionality of antibod- fects. Similarly, targeted delivery of imaging agents can ies, particularly small recombinant antibody fragments, localize and retain contrast at disease sites, enhancing the will be impaired. Conjugation can also take place by use of sensitivity and accuracy of current imaging techniques. the carbohydrate chains typically attached to the constant Targeting can be achieved via conjugation to antibodies heavy chain domain within the crystallizable fragment that possess a number of functional groups, such as amine, region of the antibody3;however,thismethodislimitedto thiol, and carboxylate groups suitable for chemical conju- glycosylated antibodies. Furthermore, conventional bioconjuga- gation purposes.1 Most antibody conjugation methods tion typically leads to multicomponent heterogenous mixtures target endogenous amino acids, such as the amino group of that are incapable of complying with regulatory requirements. lysine or the thiol group of cysteine2;however,these Overall, a single and covalent bond between an antibody and a Original received December 3, 2010; resubmission received May 26, 2011; revised resubmission received June 7, 2011; accepted June 14, 2011. In May 2011, the average time from submission to first decision for all original research papers submitted to Circulation Research was 14.5 days. From Atherothrombosis and Vascular Biology (H.T.T., S.P., E.L., F.J., K.E.J., A.K.N.N., H.P., X.W., K. Peter, C.E.H.), Baker IDI Heart and Diabetes Institute, Melbourne, Victoria, Australia; Departments of Medicine (S.P., X.W., K.P.), Clinical Haematology (A.K.N.N., C.E.H.), and Immunology (K.P., C.E.H.), Monash University, Melbourne, Victoria, Australia; Department of Medical Physics (D.v.E.), University Medical Center, Freiburg, Germany; and Department of Cardiology (T.H., C.v.z.M.), University Hospital, Freiburg, Germany. *These authors were equally contributing senior authors. Correspondence to Christoph E. Hagemeyer, PhD, Atherothrombosis and Vascular Biology, Baker IDI Heart and Diabetes Institute, PO Box 6492, St Kilda Rd Central, Victoria 8008, Australia. E-mail [email protected] © 2011 American Heart Association, Inc. Circulation Research is available at http://circres.ahajournals.org DOI: 10.1161/CIRCRESAHA.111.249375 Downloaded from http://circres.ahajournals.org/365 at Monash University on October 10, 2011 366 Circulation Research August 5, 2011 surface of activated platelets and critical players in athero- Non-standard Abbreviations and Acronyms sclerosis, thrombosis, and inflammation.9,10 The conjuga- CHO Chinese hamster ovary tion method described in the present report comprises 2 LIBS ligand-induced binding sites stages: (1) the introduction of GGG peptides (as sortase MPIO microparticles of iron oxide nucleophiles) to the surface of magnetic particles and cells scFv single-chain antibody by a series of chemical reactions, and (2) the incubation of triglycine-tagged components with the sortase A enzyme and anti-LIBS scFv (Figure 1). We demonstrate this novel use of sortase A for the selective labeling of imaging contrast particles and live cells conjugation partner that preserves the functionality of both with scFvs suitable for targeted molecular imaging and cell components is of critical importance and has a multitude of homing. This method is universally applicable and is partic- potential applications in the field of diagnostic and therapeutic ularly suitable for the antibody “tagging” of proteins, parti- antibody development. cles, or cells. Current coupling approaches for site-specific conjugation are based on the introduction of unique functional groups Methods such as ketones and azides into proteins not present in natural An expanded Methods section is available in the Online Data amino acids. They can be incorporated into proteins by Supplement at http://circres.ahajournals.org. chemical modification of the N-terminus of the protein,4 by unnatural amino acid mutagenesis,5 or by the use of enzymes Generation and Production of Proteins that transfer prosthetic groups to proteins.6 However, these The generation of the anti-LIBS scFv from a hybridoma cell line that expresses a monoclonal antibody against LIBS epitopes on methods face practical limitations in terms of feasibility, GP IIb/IIIa has been described previously.11 The LPETG motif scalability, and efficacy.7 was introduced to the C-terminal end of anti-LIBS scFv, and the In the present study, we demonstrate a new chemoenzy- scFv was subcloned into a pMT vector (Invitrogen, Carlsbad, CA) matic method to conjugate a single-chain antibody (scFv) for expression in insect cells (Invitrogen). The GGG motif was to enhanced green fluorescent protein (eGFP), Chinese introduced to the N-terminal end of the eGFP sequence by polymerase chain reaction, and GGG-eGFP was expressed in hamster ovarian (CHO) cells, human cord blood mononu- BL21-DE3 Escherichia coli (New England Biolabs, Ipswich, clear cells, and microparticles of iron oxide (MPIOs) in a MA). The generation of the plasmid construct Staphylococcus site-specific manner. This procedure uses Staphylococcus aureus sortase8 and the expression and production of soluble aureus enzyme sortase A, an enzyme that recognizes sortase A12 were described previously. diverse substrates via an LPXTG motif, and conjugates 8 Conjugation of Anti-LIBS to GGG-eGFP, this tag to a polyglycine nucleophile.
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