Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin
Protein interactions with peptides generally have low thermodynamic and mechanical stability. Streptococcus pyogenes fibronectin-binding protein FbaB contains a domain with a spontaneous isopeptide bond between Lys and Asp. By splitting this domain and rational engineering of the fragments, we obtai...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 109; no. 12; pp. E690 - E697 |
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| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
20.03.2012
National Acad Sciences |
| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Protein interactions with peptides generally have low thermodynamic and mechanical stability. Streptococcus pyogenes fibronectin-binding protein FbaB contains a domain with a spontaneous isopeptide bond between Lys and Asp. By splitting this domain and rational engineering of the fragments, we obtained a peptide (SpyTag) which formed an amide bond to its protein partner (SpyCatcher) in minutes. Reaction occurred in high yield simply upon mixing and amidst diverse conditions of pH, temperature, and buffer. SpyTag could be fused at either terminus or internally and reacted specifically at the mammalian cell surface. Peptide binding was not reversed by boiling or competing peptide. Single-molecule dynamic force spectroscopy showed that SpyTag did not separate from SpyCatcher until the force exceeded 1 nN, where covalent bonds snap. The robust reaction conditions and irreversible linkage of SpyTag shed light on spontaneous isopeptide bond formation and should provide a targetable lock in cells and a stable module for new protein architectures. |
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| AbstractList | Protein interactions with peptides generally have low thermodynamic and mechanical stability. Streptococcus pyogenes fibronectin-binding protein FbaB contains a domain with a spontaneous isopeptide bond between Lys and Asp. By splitting this domain and rational engineering of the fragments, we obtained a peptide (SpyTag) which formed an amide bond to its protein partner (SpyCatcher) in minutes. Reaction occurred in high yield simply upon mixing and amidst diverse conditions of pH, temperature, and buffer. SpyTag could be fused at either terminus or internally and reacted specifically at the mammalian cell surface. Peptide binding was not reversed by boiling or competing peptide. Single-molecule dynamic force spectroscopy showed that SpyTag did not separate from SpyCatcher until the force exceeded 1 nN, where covalent bonds snap. The robust reaction conditions and irreversible linkage of SpyTag shed light on spontaneous isopeptide bond formation and should provide a targetable lock in cells and a stable module for new protein architectures. Protein interactions with peptides generally have low thermodynamic and mechanical stability. Streptococcus pyogenes fibronectin-binding protein FbaB contains a domain with a spontaneous isopeptide bond between Lys and Asp. By splitting this domain and rational engineering of the fragments, we obtained a peptide (SpyTag) which formed an amide bond to its protein partner (SpyCatcher) in minutes. Reaction occurred in high yield simply upon mixing and amidst diverse conditions of pH, temperature, and buffer. SpyTag could be fused at either terminus or internally and reacted specifically at the mammalian cell surface. Peptide binding was not reversed by boiling or competing peptide. Single-molecule dynamic force spectroscopy showed that SpyTag did not separate from SpyCatcher until the force exceeded 1 nN, where covalent bonds snap. The robust reaction conditions and irreversible linkage of SpyTag shed light on spontaneous isopeptide bond formation and should provide a targetable lock in cells and a stable module for new protein architectures. Protein interactions with peptides generally have low thermodynamic and mechanical stability. Streptococcus pyogenes fibronectin-binding protein FbaB contains a domain with a spontaneous isopeptide bond between Lys and Asp. By splitting this domain and rational engineering of the fragments, we obtained a peptide (SpyTag) which formed an amide bond to its protein partner (SpyCatcher) in minutes. Reaction occurred in high yield simply upon mixing and amidst diverse conditions of pH, temperature, and buffer. SpyTag could be fused at either terminus or internally and reacted specifically at the mammalian cell surface. Peptide binding was not reversed by boiling or competing peptide. Single-molecule dynamic force spectroscopy showed that SpyTag did not separate from SpyCatcher until the force exceeded 1 nN, where covalent bonds snap. The robust reaction conditions and irreversible linkage of SpyTag shed light on spontaneous isopeptide bond formation and should provide a targetable lock in cells and a stable module for new protein architectures. Protein interactions with peptides generally have low thermodynamic and mechanical stability. Streptococcus pyogenes fibronectin-binding protein FbaB contains a domain with a spontaneous isopeptide bond between Lys and Asp. By splitting this domain and rational engineering of the fragments, we obtained a peptide (SpyTag) which formed an amide bond to its protein partner (SpyCatcher) in minutes. Reaction occurred in high yield simply upon mixing and amidst diverse conditions of pH, temperature, and buffer. SpyTag could be fused at either terminus or internally and reacted specifically at the mammalian cell surface. Peptide binding was not reversed by boiling or competing peptide. Single-molecule dynamic force spectroscopy showed that SpyTag did not separate from SpyCatcher until the force exceeded 1 nN, where covalent bonds snap. The robust reaction conditions and irreversible linkage of SpyTag shed light on spontaneous isopeptide bond formation and should provide a targetable lock in cells and a stable module for new protein architectures. [PUBLICATION ABSTRACT] Protein interactions with peptides generally have low thermodynamic and mechanical stability. Streptococcus pyogenes fibronectin-binding protein FbaB contains a domain with a spontaneous isopeptide bond between Lys and Asp. By splitting this domain and rational engineering of the fragments, we obtained a peptide (SpyTag) which formed an amide bond to its protein partner (SpyCatcher) in minutes. Reaction occurred in high yield simply upon mixing and amidst diverse conditions of pH, temperature, and buffer. SpyTag could be fused at either terminus or internally and reacted specifically at the mammalian cell surface. Peptide binding was not reversed by boiling or competing peptide. Single-molecule dynamic force spectroscopy showed that SpyTag did not separate from SpyCatcher until the force exceeded 1 nN, where covalent bonds snap. The robust reaction conditions and irreversible linkage of SpyTag shed light on spontaneous isopeptide bond formation and should provide a targetable lock in cells and a stable module for new protein architectures. For decades people have studied how force affects the body, such as exercise leading to a bigger heart and stronger bones. Many of the biological effects of force at the molecular level have only started to be appreciated in recent years ( 3 ). Proteins that can turn activated chemical precursors into movement (termed molecular motors), such as those synthesizing RNA or moving cargo on tracks around the cell, are able to break the strongest noncovalent interactions in seconds ( 4 , 5 ). For this reason it has been difficult to provide barriers or locks to such motors inside cells. Using the atomic force microscope, one can tug on single molecules and by pulling hard enough even snap covalent bonds; SpyTag held on to SpyCatcher at forces dramatically greater than gold-standard noncovalent interactions. Molecular motors should not be able to break the covalent bond formed by SpyTag, so this system should provide a way to control motor activity and thereby determine the role of the motor’s force generation for the cell. Interactions among peptides or proteins in the cell nearly always occur through transient noncovalent interactions. This transience is because the macromolecular machines of the cell are not built to last, but are constantly dismantled and rebuilt so the cell can respond to rapidly changing circumstances. Exceptions are the covalent bonds formed between proteins that provide strength to hair and skin. When proteins interact through covalent bonds, such as those catalyzed by transglutaminase enzymes, proteins are often cross-linked indiscriminately. Hence transglutaminase is exploited in industry (and avant-garde haute cuisine) to bond together diverse proteins and so provide texture to food. Unlike transglutaminases, SpyTag and SpyCatcher formed a covalent bond with high specificity at the surface of human cells: SpyTag and SpyCatcher reacted with each other but not the many other proteins present. Many protein-catalyzed reactions are highly sensitive to their conditions, occurring only within a narrow range of pH values and temperatures and requiring particular cofactors or metal ions. The SpyTag reaction, by contrast, worked well in all buffers tested, including in the presence of detergents. The reaction also proceeded well over a range of temperatures, from ice-cold to body temperature, while bond formation proceeded efficiently at neutral pH and under the more acidic conditions found in certain cellular compartments. With this high tolerance to its surroundings and requiring no artificial amino acids or added cofactors, SpyTag may find use in a wide range of situations inside and outside of the cell. Abbreviating Streptococcus pyogenes to Spy, we termed the peptide “SpyTag” and the protein partner “SpyCatcher” ( Fig. P1 ). We found that SpyTag docked with SpyCatcher and then rapidly formed an amide bond, thereby locking the two partners together. Both SpyTag and SpyCatcher are composed of the usual 20 amino acids common to all organisms. Therefore, they can be genetically fused to any protein of interest and expressed in different organisms, or alternatively purified by overexpressing in biochemists’ favorite factotum, Escherichia coli . Fig. P1. A domain of a protein involved in binding to human cells, from an invasive strain of Streptococcus pyogenes (Spy), was genetically dissected to generate a protein partner (SpyCatcher) and a peptide tag (SpyTag) (cartoon based on the crystal structure 2X5P). Upon mixing, SpyCatcher and SpyTag reacted rapidly and specifically to form a spontaneous amide bond, which was not reversed by boiling or mechanical stress. Fusion to SpyTag should provide a simple tool for irreversibly grasping proteins inside or outside cells. Here, through rational protein engineering, we have harnessed the protein chemistry of this pathogen to develop a tool for biochemical research. The bacterium uses the protein FbaB to help invade human cells. We genetically split a domain of FbaB into two parts- a small peptide component and a larger protein component. Thus, rather than the amide bond formation occurring within the protein, amide bond formation could serve to lock two separate molecules together. The bacterium Streptococcus pyogenes causes a range of illnesses, from sore throats to life-threatening necrotizing fasciitis, also known as “flesh-eating bacteria syndrome.” While most organisms stabilize proteins by disulfide bonds (-S-S-), Streptococcus pyogenes grows well in low oxygen environments, where it is hard to form such bonds. Like a number of other bacterial species, Streptococcus pyogenes has evolved a special chemistry which endows some of its proteins with high stability ( 1 ): two amino acid side chains spontaneously react to form an amide bond (between lysine and aspartic acid or asparagine) ( 2 ). This reaction irreversibly locks together distant parts of the protein. Manipulating and observing proteins is at the heart of biochemical research. Antibodies are important observers, with the ability to recognize one type of protein amidst thousands. Rather than recognizing the whole protein, many antibodies recognize just a short stretch of the amino acids that comprise the protein, a ‘peptide tag.’ This peptide tag can often be genetically transferred to a new protein, so that one immediately can use the same antibody to follow where this new protein travels and what partners it associates with. However, antibodies and other binding proteins struggle to get a firm grip on tags, as a result of the tag’s small size and flexibility. Inspired by chemistry from a flesh-eating bacterium, we developed a way to rapidly bind a peptide tag and never let go. |
| Author | Zakeri, Bijan Celik, Emrah Chittock, Emily C Schwarz-Linek, Ulrich Fierer, Jacob O Moy, Vincent T Howarth, Mark |
| Author_xml | – sequence: 1 fullname: Zakeri, Bijan – sequence: 2 fullname: Fierer, Jacob O – sequence: 3 fullname: Celik, Emrah – sequence: 4 fullname: Chittock, Emily C – sequence: 5 fullname: Schwarz-Linek, Ulrich – sequence: 6 fullname: Moy, Vincent T – sequence: 7 fullname: Howarth, Mark |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22366317$$D View this record in MEDLINE/PubMed |
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| Notes | http://dx.doi.org/10.1073/pnas.1115485109 ObjectType-Article-2 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 23 ObjectType-Article-1 ObjectType-Feature-2 Author contributions: B.Z., J.O.F., E.C., U.S.-L., V.T.M., and M.H. designed research; B.Z., J.O.F., E.C., E.C.C., U.S.-L., and M.H. performed research; B.Z., J.O.F., E.C., U.S.-L., V.T.M., and M.H. analyzed data; and M.H. wrote the paper. 1B.Z. and J.O.F. contributed equally to this work. Edited by James A. Wells, University of California, San Francisco, CA, and approved January 17, 2012 (received for review September 21, 2011) |
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| Snippet | Protein interactions with peptides generally have low thermodynamic and mechanical stability. Streptococcus pyogenes fibronectin-binding protein FbaB contains... Protein interactions with peptides generally have low thermodynamic and mechanical stability. Streptococcus pyogenes fibronectin-binding protein FbaB contains... |
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| SubjectTerms | Adhesins Adhesins, Bacterial - metabolism amides Amides - chemistry Bacteria Biological Sciences Biophysics - methods Boiling Cell Membrane - metabolism Cell surface Cells Chemical bonds engineering Fibronectin-binding protein Fibronectins - chemistry HeLa Cells Humans Hydrogen-Ion Concentration Mammalian cells mammals Microscopy, Atomic Force - methods mixing Molecular Sequence Data Molecules Peptides Peptides - chemistry pH effects PNAS Plus Protein Binding Protein Engineering - methods Protein interaction Protein Structure, Tertiary Proteins Spectrometry, Mass, Electrospray Ionization - methods Spectroscopy Spectrum analysis Splitting Streptococcus pyogenes Streptococcus pyogenes - metabolism Temperature Temperature effects Thermodynamics |
| Title | Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin |
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