Mechanical properties of elastomeric proteins studied by single molecule force spectroscopy

Zhou Hao-Tian; Gao Xiang; Zheng Peng; Qin Meng; Cao Yi; Wang Wei

doi:10.7498/aps.65.188703

Abstract

Elastomeric proteins are a special class of proteins with unique mechanical functions. They bear, transduce mechanical forces inside cell, and serve as biomaterials of high elasticities and strengths outside cell. Depending on their functions, the mechanical properties of elastomeric proteins are very diverse. Some of them are of high mechanical stability and the others are of high extensibility and toughness. Although many elastomeric proteins are engineered for the applications in the fields of biomaterials and nanotechnology, the molecular determinant of the mechanical stability remains elusive. In this review, we summarize recent advances in the field of protein mechanics studied by using single molecule force spectroscopy. Force spectroscopy enables people to probe the unfolding properties of protein domains, thus paving the way for building special proteins with characteristic mechanical functions. To begin with, it is necessary to clarify the factors and their relations with the unfolding force, which is deduced based on Bell's expression. It turns out that the unfolding force is proportional to pulling speed when the speed is relatively small, and has a logarithmic relation in the high-speed approximation. After the external determinant of the force probe is clarified, some intrinsic factors are to be discussed. Hydrogen bound and electrostatic force, rather than covalent bond, contribute to the mechanical performances of proteins. Those interactions rely on the topology structures of protein molecules. By changing the structures of proteins, researchers now manage to change the mechanical characteristics of certain proteins. Since single protein is unable to be detected by traditional optic microscope, three devices used to observe and manipulate single protein are introduced in the present paper. These include atomic force microscopy, magnetic tweezers and optical tweezers. Among them, a more detailed explanation of atomic force microscope (AFM) is provided, which briefly describes the basic mechanism and structure of AFM and possible explanation for the formation of force-extension curves. After that, several recent advances for improving the AFM based single molecule force spectroscopy techniques are highlighted. For example, Tom Perkins group [Sullan R M A, Churnside A B, Nguyen D M, Bull M S, Perkins T T 2013 Methods 60 131] has discovered that the gold-stripped tip gives more accurate and reproducible results than a gold-coated one. Matthias Rief group [Schlierf M, Berkemeier F, Rief M 2007 Biophys. J. 93 3989] has managed to increase the resolution of AFM, pushing it in pair with optical tweezers. Hermann Gaub et al. [Otten M, Ott W, Jobst M A, Milles L F, Verdorfer T, Pippig D A, Nash M A, Gaub H E 2014 Nat. Methods 11 1127] combined the microfluidic chip and DNA expression in vitro to increase the yields of interpretable single-molecule interaction traces. Toshio Ando et al. [Ando T, Uchihashi T, Fukuma T 2008 Prog. Surf. Sci. 83 337] have developed methods to increase the imaging speed of AFM. Finally, the rationally designing the mechanical properties of protein-based materials pioneered by Hongbin Li group is highlighted. They have discovered direct relationship between the mechanical properties of individual proteins and those of the protein materials. To sum up, with AFM, scientists now can explore mechanical properties of a wide range of proteins, which enables them to build biomaterials with exceptional mechanical features.

Keywords:

Authors and contacts

1.
School of Physics, Nanjing University, Nanjing 210093, China;
2.
School of Chemistry and Chemical Engineering, Nanjing University, Nanjing 210046, China

Corresponding author: Qin Meng, qinmeng@nju.edu.cn;caoyi@nju.edu.cn ; Cao Yi, qinmeng@nju.edu.cn;caoyi@nju.edu.cn ;

Funds: Project supported by Six Talent Peaks Project in Jiangsu Province China and the National Natural Science Foundation of China (Grant Nos. 21522402, 11374148, 11334004, 81121062).

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[44]	Cao Y, Balamurali M M, Sharma D, Li H 2007 Proc. Natl. Acad. Sci. USA 104 15677
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[47]	Carrion-Vazquez M, Li H, Lu H, Marszalek P E, Oberhauser A F, Fernandez J M 2003 Nat. Struct. Biol. 10 738
[48]	Dietz H, Berkemeier F, Bertz M, Rief M 2006 Proc. Natl. Acad. Sci. USA 103 12724
[49]	Hinterdorfer P, Dufrene Y F 2006 Nat. Methods 3 347
[50]	Muller D J, Dufrene Y F 2008 Nat. Nanotechnol. 3 261
[51]	Hoffman T, Dougan L 2012 Chem. Soc. Rev. 41 4773
[52]	Sullan R M A, Churnside A B, Nguyen D M, Bull M S, Perkins T T 2013 Methods 60 131
[53]	Junker J P, Ziegler F, Rief M 2009 Science 323 633
[54]	Schlierf M, Berkemeier F, Rief M 2007 Biophys. J. 93 3989
[55]	Otten M, Ott W, Jobst M A, Milles L F, Verdorfer T, Pippig D A, Nash M A, Gaub H E 2014 Nat. Methods 11 1127
[56]	Baumann F, Heucke S F, Pippig D A, Gaub H E 2015 Rev. Sci. Instrum. 86 035109
[57]	Ando T, Uchihashi T, Fukuma T 2008 Prog. Surf. Sci. 83 337
[58]	Lee H, Scherer N F, Messersmith P B 2006 Proc. Natl. Acad. Sci. USA 103 12999
[59]	Li Y, Qin M, Li Y, Cao Y, Wang W 2014 Langmuir 30 4358

Cited By

[1]	Strong M 2004 PLoS Biol. 2 305
[2]	Berkemeier F, Bertz M, Xiao S, Pinotsis N, Wilmanns M, Grater F, Rief M 2011 Proc. Natl. Acad. Sci. USA 108 14139
[3]	Bullard B, Garcia T, Benes V, Leake M C, Linke W A, Oberhauser A F 2006 Proc. Natl. Acad. Sci. USA 103 4451
[4]	Scharnagl C, Reif M, Friedrich J 2005 Biochim. Biophys. Acta 1749 187
[5]	Neuman K C, Nagy A 2008 Nat. Methods 5 491
[6]	Rief M, Gautel M, Oesterhelt F, Fernandez J M, Gaub H E 1997 Science 276 1109
[7]	Oberhauser A F, Marszalek P E, Erickson H P, Fernandez J M 1998 Nature 393 181
[8]	Rief M, Gautel M, Schemmel A, Gaub H E 1998 Biophys. J. 75 3008
[9]	Rief M, Pascual J, Saraste M, Gaub H E 1999 J. Mol. Biol. 286 553
[10]	Rief M, Gautel M, Gaub H E 2000 Adv. Exp. Med. Biol. 481 129
[11]	Schwaiger I, Sattler C, Hostetter D R, Rief M 2002 Nat. Mater. 1 232
[12]	Urry D W, Parker T M 2002 J. Muscle Res. Cell Motil. 23 543
[13]	Guerette P A, Ginzinger D G, Weber B H, Gosline J M 1996 Science 272 112
[14]	Smith B L, Schaffer T E, Viani M, Thompson J B, Frederick N A, Kindt J, Belcher A, Stucky G D, Morse D E, Hansma P K 1999 Nature 399 761
[15]	Ardell D H, Andersen S O 2001 Insect Biochem. Mol. Biol. 31 965
[16]	Becker N, Oroudjev E, Mutz S, Cleveland J P, Hansma P K, Hayashi C Y, Makarov D E, Hansma H G 2003 Nat. Mater. 2 278
[17]	Elvin C M, Carr A G, Huson M G, Maxwell J M, Pearson R D, Vuocolo T, Liyou N E, Wong D C, Merritt D J, Dixon N E 2005 Nature 437 999
[18]	Lyons R E, Lesieur E, Kim M, Wong D C, Huson M G, Nairn K M, Brownlee A G, Pearson R D, Elvin C M 2007 Protein Eng. Des. Sel. 20 25
[19]	Heim M, Keerl D, Scheibel T 2009 Angew. Chem. Int. Ed. Engl. 48 3584
[20]	Wong J Y, McDonald J, Taylor-Pinney M, Spivak D I, Kaplan D L, Buehler M J 2012 Nano Today 7 488
[21]	Li H 2007 Org. Biomol. Chem. 5 3399
[22]	Li H 2008 Adv. Funct. Mater. 18 2643
[23]	Li H, Cao Y 2010 Acc. Chem. Res. 43 1331
[24]	Hoffmann T, Tych K M, Hughes M L, Brockwell D J, Dougan L 2013 Phys. Chem. Chem. Phys. 15 15767
[25]	Bell G I 1978 Science 200 618
[26]	Evans E, Ritchie K 1997 Biophys. J. 72 1541
[27]	Evans E, Ritchie K 1999 Biophys. J. 76 2439
[28]	Best R B, Li B, Steward A, Daggett V, Clarke J 2001 Biophys. J. 81 2344
[29]	Cao Y, Lam C, Wang M, Li H 2006 Angew. Chem. Int. Ed. Engl. 45 642
[30]	Cao Y, Li H 2007 Nat. Mater. 6 109
[31]	Brockwell D J, Beddard G S, Paci E, West D K, Olmsted P D, Smith D A, Radford S E 2005 Biophys. J. 89 506
[32]	Dietz H, Rief M 2004 Proc. Natl. Acad. Sci. USA 101 16192
[33]	Cao Y, Li H 2008 Nat. Nanotechnol. 3 512
[34]	Sharma D, Perisic O, Peng Q, Cao Y, Lam C, Lu H, Li H 2007 Proc. Natl. Acad. Sci. USA 104 9278
[35]	Balamurali M M, Sharma D, Chang A, Khor D, Chu R, Li H 2008 Protein Sci. 17 1815
[36]	Ng S P, Billings K S, Ohashi T, Allen M D, Best R B, Randles L G, Erickson H P, Clarke J 2007 Proc. Natl. Acad. Sci. USA 104 9633
[37]	Perez-Jimenez R, Garcia-Manyes S, Ainavarapu S R, Fernandez J M 2006 J. Biol. Chem. 281 40010
[38]	Peng Q, Li H 2008 Proc. Natl. Acad. Sci. USA 105 1885
[39]	Aggarwal V, Kulothungan S R, Balamurali M M, Saranya S R, Varadarajan R, Ainavarapu S R 2011 J. Biol. Chem. 286 28056
[40]	Puchner E M, Alexandrovich A, Kho A L, Hensen U, Schafer L V, Brandmeier B, Grater F, Grubmuller H, Gaub H E, Gautel M 2008 Proc. Natl. Acad. Sci. USA 105 13385
[41]	Pernigo S, Fukuzawa A, Bertz M, Holt M, Rief M, Steiner R A, Gautel M 2010 Proc. Natl. Acad. Sci. USA 107 2908
[42]	Cao Y, Yoo T, Li H 2008 Proc. Natl. Acad. Sci. USA 105 11152
[43]	Grandbois M, Beyer M, Rief M, Clausen-Schaumann H, Gaub H E 1999 Science 283 1727
[44]	Cao Y, Balamurali M M, Sharma D, Li H 2007 Proc. Natl. Acad. Sci. USA 104 15677
[45]	Cao Y, Li H 2008 J. Mol. Biol. 375 316
[46]	Brockwell D J, Paci E, Zinober R C, Beddard G S, Olmsted P D, Smith D A, Perham R N, Radford S E 2003 Nat. Struct. Biol. 10 731
[47]	Carrion-Vazquez M, Li H, Lu H, Marszalek P E, Oberhauser A F, Fernandez J M 2003 Nat. Struct. Biol. 10 738
[48]	Dietz H, Berkemeier F, Bertz M, Rief M 2006 Proc. Natl. Acad. Sci. USA 103 12724
[49]	Hinterdorfer P, Dufrene Y F 2006 Nat. Methods 3 347
[50]	Muller D J, Dufrene Y F 2008 Nat. Nanotechnol. 3 261
[51]	Hoffman T, Dougan L 2012 Chem. Soc. Rev. 41 4773
[52]	Sullan R M A, Churnside A B, Nguyen D M, Bull M S, Perkins T T 2013 Methods 60 131
[53]	Junker J P, Ziegler F, Rief M 2009 Science 323 633
[54]	Schlierf M, Berkemeier F, Rief M 2007 Biophys. J. 93 3989
[55]	Otten M, Ott W, Jobst M A, Milles L F, Verdorfer T, Pippig D A, Nash M A, Gaub H E 2014 Nat. Methods 11 1127
[56]	Baumann F, Heucke S F, Pippig D A, Gaub H E 2015 Rev. Sci. Instrum. 86 035109
[57]	Ando T, Uchihashi T, Fukuma T 2008 Prog. Surf. Sci. 83 337
[58]	Lee H, Scherer N F, Messersmith P B 2006 Proc. Natl. Acad. Sci. USA 103 12999
[59]	Li Y, Qin M, Li Y, Cao Y, Wang W 2014 Langmuir 30 4358

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