Molecular sled is an eleven-amino acid vehicle facilitating biochemical interactions via sliding components along DNA

Mangel, Walter F.; McGrath, William J.; Xiong, Kan; Graziano, Vito; Blainey, Paul C.

doi:10.1038/ncomms10202

Title: Molecular sled is an eleven-amino acid vehicle facilitating biochemical interactions via sliding components along DNA

Journal Article · Tue Feb 02 00:00:00 EST 2016 · Nature Communications

DOI:https://doi.org/10.1038/ncomms10202· OSTI ID:1258647

Mangel, Walter F. ^[1]; McGrath, William J. ^[1]; Xiong, Kan ^[2]; Graziano, Vito ^[1]; Blainey, Paul C. ^[2]

Brookhaven National Lab. (BNL), Upton, NY (United States)
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Broad Institute of MIT and Harvard, Cambridge, MA (United States)

Recently, we showed the adenovirus proteinase interacts productively with its protein substrates in vitro and in vivo in nascent virus particles via one-dimensional diffusion along the viral DNA. The mechanism by which this occurs has heretofore been unknown. We show sliding of these proteins along DNA occurs on a new vehicle in molecular biology, a ‘molecular sled’ named pVIc. This 11-amino acid viral peptide binds to DNA independent of sequence. pVIc slides on DNA, exhibiting the fastest one-dimensional diffusion constant, 26±1.8 × 10⁶ (bp)²s^-1. pVIc is a ‘molecular sled,’ because it can slide heterologous cargos along DNA, for example, a streptavidin tetramer. Similar peptides, for example, from the C terminus of β-actin or NLSIII of the p53 protein, slide along DNA. Finally, characteristics of the ‘molecular sled’ in its milieu (virion, nucleus) have implications for how proteins in the nucleus of cells interact and imply a new form of biochemistry, one-dimensional biochemistry.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: R01AI41599; R21AI113565

OSTI ID:: 1258647

Journal Information:: Nature Communications, Vol. 7; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 16 works

Citation information provided by
Web of Science

References (59)

Mechanics of DNA packaging in viruses Purohit, P. K.; Kondev, J.; Phillips, R. Proceedings of the National Academy of Sciences, Vol. 100, Issue 6 https://doi.org/10.1073/pnas.0737893100	journal	March 2003
Single Qdot-labeled glycosylase molecules use a wedge amino acid to probe for lesions while scanning along DNA Dunn, Andrew R.; Kad, Neil M.; Nelson, Shane R. Nucleic Acids Research, Vol. 39, Issue 17 https://doi.org/10.1093/nar/gkr459	journal	June 2011
Single-Molecule Enzymatic Dynamics Lu, H. P. Science, Vol. 282, Issue 5395 https://doi.org/10.1126/science.282.5395.1877	journal	December 1998
Transport of Nucleosome Core Particles in Semidilute DNA Solutions Mangenot, Stéphanie; Keller, Simon; Rädler, Joachim Biophysical Journal, Vol. 85, Issue 3 https://doi.org/10.1016/s0006-3495(03)74610-4	journal	September 2003
DNA Binding Provides a Molecular Strap Activating the Adenovirus Proteinase Gupta, Sayan; Mangel, Walter F.; McGrath, William J. Molecular & Cellular Proteomics, Vol. 3, Issue 10 https://doi.org/10.1074/mcp.M400037-MCP200	journal	June 2004
Switch from capsid protein import to adenovirus assembly by cleavage of nuclear transport signals Wodrich, H. The EMBO Journal, Vol. 22, Issue 23 https://doi.org/10.1093/emboj/cdg614	journal	December 2003
Nuclear Functions of Actin Visa, N.; Percipalle, P. Cold Spring Harbor Perspectives in Biology, Vol. 2, Issue 4 https://doi.org/10.1101/cshperspect.a000620	journal	March 2010
Technical Reports: Mapping a Functional Viral Protein in Solution Using Synchrotron X-ray Footprinting Technology Gupta, Sayan; Mangel, Walter F.; Sullivan, Michael Synchrotron Radiation News, Vol. 18, Issue 1 https://doi.org/10.1080/08940880500457537	journal	January 2005
Nonspecifically bound proteins spin while diffusing along DNA Blainey, Paul C.; Luo, Guobin; Kou, S. C. Nature Structural & Molecular Biology, Vol. 16, Issue 12 https://doi.org/10.1038/nsmb.1716	journal	November 2009
Specific interactions of the adenovirus proteinase with the viral DNA, an 11-amino-acid viral peptide, and the cellular protein actin Mangel, W. F.; Baniecki, M. L.; McGrath, W. J. Cellular and Molecular Life Sciences (CMLS), Vol. 60, Issue 11 https://doi.org/10.1007/s00018-003-2318-2	journal	November 2003
Regulation of a Viral Proteinase by a Peptide and DNA in One-dimensional Space: II. ADENOVIRUS PROTEINASE IS ACTIVATED IN AN UNUSUAL ONE-DIMENSIONAL BIOCHEMICAL REACTION Graziano, Vito; Luo, Guobin; Blainey, Paul C. Journal of Biological Chemistry, Vol. 288, Issue 3 https://doi.org/10.1074/jbc.M112.407312	journal	October 2012
Interaction of the Human Adenovirus Proteinase with Its 11-Amino Acid Cofactor pVIc Baniecki, Mary Lynn; McGrath, William J.; McWhirter, Sarah M. Biochemistry, Vol. 41, Issue 1 https://doi.org/10.1021/bi015150g	journal	January 2002
Speeding up biomolecular interactions by molecular sledding Turkin, Alexander; Zhang, Lei; Marcozzi, Alessio Chemical Science, Vol. 7, Issue 2 https://doi.org/10.1039/C5SC03063C	journal	January 2016
Regulation of a Viral Proteinase by a Peptide and DNA in One-dimensional Space: I. BINDING TO DNA AND TO HEXON OF THE PRECURSOR TO PROTEIN VI, pVI, OF HUMAN ADENOVIRUS Graziano, Vito; McGrath, William J.; Suomalainen, Maarit Journal of Biological Chemistry, Vol. 288, Issue 3 https://doi.org/10.1074/jbc.M112.377150	journal	October 2012
Processing of the L1 52/55k Protein by the Adenovirus Protease: a New Substrate and New Insights into Virion Maturation Perez-Berna, A. J.; Mangel, W. F.; McGrath, W. J. Journal of Virology, Vol. 88, Issue 3 https://doi.org/10.1128/jvi.02884-13	journal	November 2013
Live wire Service, R. F. Science, Vol. 346, Issue 6215 https://doi.org/10.1126/science.346.6215.1284	journal	December 2014
A base-excision DNA-repair protein finds intrahelical lesion bases by fast sliding in contact with DNA Blainey, P. C.; van Oijen, A. M.; Banerjee, A. Proceedings of the National Academy of Sciences, Vol. 103, Issue 15 https://doi.org/10.1073/pnas.0509723103	journal	April 2006
Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA Bruner, Steven D.; Norman, Derek P. G.; Verdine, Gregory L. Nature, Vol. 403, Issue 6772 https://doi.org/10.1038/35002510	journal	February 2000
A structural basis for processivity Breyer, Wendy A.; Matthews, Brian W. Protein Science, Vol. 10, Issue 9 https://doi.org/10.1110/ps.10301	journal	September 2001
A general expression for bimolecular association rates with orientational constraints Schlosshauer, Maximilian; Baker, David arXiv https://doi.org/10.48550/arxiv.physics/0401127	text	January 2004
Diffusion in correlated random potentials, with applications to DNA Slutsky, Michael; Kardar, Mehran; Mirny, Leonid Physical Review E, Vol. 69, Issue 6 https://doi.org/10.1103/physreve.69.061903	journal	June 2004
Protein Conformational Dynamics Probed by Single-Molecule Electron Transfer Yang, H. Science, Vol. 302, Issue 5643 https://doi.org/10.1126/science.1086911	journal	October 2003
Human Adenovirus Proteinase: DNA Binding and Stimulation of Proteinase Activity by DNA ^† McGrath, William J.; Baniecki, Mary Lynn; Li, Caroline Biochemistry, Vol. 40, Issue 44 https://doi.org/10.1021/bi0111653	journal	November 2001
Tumor Suppressor p53 Slides on DNA with Low Friction and High Stability Tafvizi, Anahita; Huang, Fang; Leith, Jason S. Biophysical Journal, Vol. 95, Issue 1 https://doi.org/10.1529/biophysj.108.134122	journal	July 2008
An end to 40 years of mistakes in DNA–protein association kinetics? Halford, Stephen E. Biochemical Society Transactions, Vol. 37, Issue 2 https://doi.org/10.1042/bst0370343	journal	March 2009
Viral DNA and a viral peptide can act as cofactors of adenovirus virion proteinase activity Mangel, Walter F.; McGrath, William J.; Toledo, Diana L. Nature, Vol. 361, Issue 6409 https://doi.org/10.1038/361274a0	journal	January 1993
Interaction of actin and its 11-amino acid C-terminal peptide as cofactors with the adenovirus proteinase Brown, Mark T.; Mangel, Walter F. FEBS Letters, Vol. 563, Issue 1-3 https://doi.org/10.1016/s0014-5793(04)00285-6	journal	March 2004
Nuclear Actin and Actin-Related Proteins in Chromatin Remodeling Olave, Ivan A.; Reck-Peterson, Samara L.; Crabtree, Gerald R. Annual Review of Biochemistry, Vol. 71, Issue 1 https://doi.org/10.1146/annurev.biochem.71.110601.135507	journal	June 2002
Direct Observation of the Ion-Pair Dynamics at a Protein–DNA Interface by NMR Spectroscopy Anderson, Kurtis M.; Esadze, Alexandre; Manoharan, Mariappan Journal of the American Chemical Society, Vol. 135, Issue 9 https://doi.org/10.1021/ja312314b	journal	February 2013
A General Expression for Bimolecular Association Rates with Orientational Constraints Schlosshauer, Maximilian; Baker, David The Journal of Physical Chemistry B, Vol. 106, Issue 46 https://doi.org/10.1021/jp025894j	journal	November 2002
Different modes of inhibition of human adenovirus proteinase, probably a cysteine proteinase, by bovine pancreatic trypsin inhibitor Brown, Mark T.; McGrath, William J.; Toledo, Diana L. FEBS Letters, Vol. 388, Issue 2-3 https://doi.org/10.1016/0014-5793(96)00569-8	journal	June 1996
Diffusion Constant of a Nonspecifically Bound Protein Undergoing Curvilinear Motion along DNA ^† Bagchi, Biman; Blainey, Paul C.; Xie, X. Sunney The Journal of Physical Chemistry B, Vol. 112, Issue 19 https://doi.org/10.1021/jp077568f	journal	May 2008
From The Cover: Measurement of the contributions of 1D and 3D pathways to the translocation of a protein along DNA Gowers, D. M.; Wilson, G. G.; Halford, S. E. Proceedings of the National Academy of Sciences, Vol. 102, Issue 44 https://doi.org/10.1073/pnas.0505378102	journal	October 2005
A single-molecule characterization of p53 search on DNA Tafvizi, A.; Huang, F.; Fersht, A. R. Proceedings of the National Academy of Sciences, Vol. 108, Issue 2 https://doi.org/10.1073/pnas.1016020107	journal	December 2010
Single-Molecule Kinetics of Exonuclease Reveal Base Dependence and Dynamic Disorder van Oijen, A. M. Science, Vol. 301, Issue 5637 https://doi.org/10.1126/science.1084387	journal	August 2003
Recognition Dynamics Up to Microseconds Revealed from an RDC-Derived Ubiquitin Ensemble in Solution Lange, O. F.; Lakomek, N. -A.; Fares, C. Science, Vol. 320, Issue 5882 https://doi.org/10.1126/science.1157092	journal	June 2008
Kinetics for the Life Sciences Gutfreund, H. Cambridge University Press https://doi.org/10.1017/CBO9780511626203	journal	January 2010
Actin Can Act as a Cofactor for a Viral Proteinase in the Cleavage of the Cytoskeleton Brown, Mark T.; McBride, Kevin M.; Baniecki, Mary Lynn Journal of Biological Chemistry, Vol. 277, Issue 48 https://doi.org/10.1074/jbc.m202988200	journal	August 2002
Differences in Hydration Coupled to Specific and Nonspecific Competitive Binding and to Specific DNA Binding of the Restriction Endonuclease BamHI Sidorova, Nina Y.; Muradymov, Shakir; Rau, Donald C. Journal of Biological Chemistry, Vol. 281, Issue 47 https://doi.org/10.1074/jbc.M608018200	journal	September 2006
Linear diffusion of the restriction endonuclease EcoRV on DNA is essential for the in vivo function of the enzyme. Jeltsch, A.; Wenz, C.; Stahl, F. The EMBO Journal, Vol. 15, Issue 18 https://doi.org/10.1002/j.1460-2075.1996.tb00891.x	journal	September 1996
Crystallographic structure at 1.6-Å resolution of the human adenovirus proteinase in a covalent complex with its 11-amino-acid peptide cofactor: insights on a new fold McGrath, William J.; Ding, Jianzhong; Didwania, Aashish Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1648, Issue 1-2 https://doi.org/10.1016/s1570-9639(03)00024-4	journal	May 2003
DNA sense-and-respond protein modules for mammalian cells Slomovic, Shimyn; Collins, James J. Nature Methods, Vol. 12, Issue 11 https://doi.org/10.1038/nmeth.3585	journal	September 2015
Characterization of Three Components of Human Adenovirus Proteinase Activity in Vitro Mangel, Walter F.; Toledo, Diana L.; Brown, Mark T. Journal of Biological Chemistry, Vol. 271, Issue 1 https://doi.org/10.1074/jbc.271.1.536	journal	January 1996
Evidence for the internal location of actin in the pseudorabies virion Wong, Min-Liang; Chen, Chi-Hung Virus Research, Vol. 56, Issue 2 https://doi.org/10.1016/S0168-1702(98)00072-0	journal	August 1998
The lac represser-operator interaction Riggs, Arthur D.; Bourgeois, Suzanne; Cohn, Melvin Journal of Molecular Biology, Vol. 53, Issue 3 https://doi.org/10.1016/0022-2836(70)90074-4	journal	November 1970
Hopping of a processivity factor on DNA revealed by single-molecule assays of diffusion Komazin-Meredith, G.; Mirchev, R.; Golan, D. E. Proceedings of the National Academy of Sciences, Vol. 105, Issue 31 https://doi.org/10.1073/pnas.0802676105	journal	July 2008
In the Virion, the 11-Amino-Acid Peptide Cofactor pVIc Is Covalently Linked to the Adenovirus Proteinase McGrath, William J.; Aherne, Katharine S.; Mangel, Walter F. Virology, Vol. 296, Issue 2 https://doi.org/10.1006/viro.2002.1394	journal	May 2002
Ellman's reagent: 5,5′-dithiobis(2-nitrobenzoic acid)—a reexamination Riddles, Peter W.; Blakeley, Robert L.; Zerner, Burt Analytical Biochemistry, Vol. 94, Issue 1, p. 75-81 https://doi.org/10.1016/0003-2697(79)90792-9	journal	April 1979
Diffusion-driven mechanisms of protein translocation on nucleic acids. 3. The Escherichia coli lac repressor-operator interaction: kinetic measurements and conclusions Winter, Robert B.; Berg, Otto G.; Von Hippel, Peter H. Biochemistry, Vol. 20, Issue 24 https://doi.org/10.1021/bi00527a030	journal	November 1981
The adenovirus protease is activated by a virus-coded disulphide-linked peptide Webster, Ailsa; Hay, Ronald T.; Kemp, Graham Cell, Vol. 72, Issue 1 https://doi.org/10.1016/0092-8674(93)90053-S	journal	January 1993
Ever-fluctuating single enzyme molecules: Michaelis-Menten equation revisited English, Brian P.; Min, Wei; van Oijen, Antoine M. Nature Chemical Biology, Vol. 2, Issue 2 https://doi.org/10.1038/nchembio759	journal	December 2005
Structure, Function and Dynamics in Adenovirus Maturation Mangel, Walter; San Martín, Carmen Viruses, Vol. 6, Issue 11 https://doi.org/10.3390/v6114536	journal	November 2014
Interaction of the Human Adenovirus Proteinase with Its 11-Amino Acid Cofactor pVIc ^† Baniecki, Mary Lynn; McGrath, William J.; McWhirter, Sarah M. Biochemistry, Vol. 40, Issue 41 https://doi.org/10.1021/bi0109008	journal	October 2001
Extreme electric fields power catalysis in the active site of ketosteroid isomerase Fried, Stephen D.; Bagchi, Sayan; Boxer, Steven G. Science, Vol. 346, Issue 6216 https://doi.org/10.1126/science.1259802	journal	December 2014
Proliferating Cell Nuclear Antigen Uses Two Distinct Modes to Move along DNA Kochaniak, Anna B.; Habuchi, Satoshi; Loparo, Joseph J. Journal of Biological Chemistry, Vol. 284, Issue 26 https://doi.org/10.1074/jbc.m109.008706	journal	May 2009
Ion effects on ligand-nucleic acid interactions Record, M. Thomas; Lohman, Timothy M.; Haseth, Pieter de Journal of Molecular Biology, Vol. 107, Issue 2 https://doi.org/10.1016/S0022-2836(76)80023-X	journal	October 1976
Crystal structure of the human adenovirus proteinase with its 11 amino acid cofactor. Ding, J.; McGrath, W. J.; Sweet, R. M. The EMBO Journal, Vol. 15, Issue 8 https://doi.org/10.1002/j.1460-2075.1996.tb00526.x	journal	April 1996
Regulation of a Viral Proteinase by a Peptide and DNA in One-dimensional Space: IV. VIRAL PROTEINASE SLIDES ALONG DNA TO LOCATE AND PROCESS ITS SUBSTRATES Blainey, Paul C.; Graziano, Vito; Pérez-Berná, Ana J. Journal of Biological Chemistry, Vol. 288, Issue 3 https://doi.org/10.1074/jbc.M112.407460	journal	October 2012
Facilitated Target Location in Biological Systems von Hippel, P. H.; Berg, O. G. Journal of Biological Chemistry, Vol. 264, Issue 2 https://doi.org/10.1016/S0021-9258(19)84994-3	journal	January 1989

Cited By (2)

Molecular sled sequences are common in mammalian proteins Xiong, Kan; Blainey, Paul C. Nucleic Acids Research, Vol. 44, Issue 5 https://doi.org/10.1093/nar/gkw035	journal	February 2016
Catalytic transport of molecular cargo using diffusive binding along a polymer track Zheng, Lifei; Zhao, Hui; Han, Yanxiao Nature Chemistry, Vol. 11, Issue 4 https://doi.org/10.1038/s41557-018-0204-7	journal	January 2019

Similar Records

Structure, function and dynamics in adenovirus maturation

Journal Article · Fri Nov 21 00:00:00 EST 2014 · Viruses · OSTI ID:1258647

Mangel, Walter F.; San Martín, Carmen

Speeding up biomolecular interactions by molecular sledding

Journal Article · Wed Oct 07 00:00:00 EDT 2015 · Chemical Science · OSTI ID:1258647

Turkin, Alexander; Zhang, Lei; Marcozzi, Alessio; +3 more

Single-molecule imaging at high fluorophore concentrations by local activation of dye

Journal Article · Tue Feb 17 00:00:00 EST 2015 · Biophysical Journal · OSTI ID:1258647

Geertsema, Hylkje J.; Mangel, Walter F.; Schulte, Aartje C.; +6 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Molecular sled is an eleven-amino acid vehicle facilitating biochemical interactions via sliding components along DNA

Citation Formats

References (59)

Cited By (2)

Similar Records

Related Subjects