Protein adsorption by nanomechanical mass spectrometry: Beyond the real-time molecular weighting

. 2022 ; 9 () : 1058441. [epub] 20230105

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid36685281

During past decades, enormous progress in understanding the mechanisms of the intermolecular interactions between the protein and surface at the single-molecule level has been achieved. These advances could only be possible by the ongoing development of highly sophisticated experimental methods such as atomic force microscopy, optical microscopy, surface plasmon resonance, ellipsometry, quartz crystal microbalance, conventional mass spectrometry, and, more recently, the nanomechanical systems. Here, we highlight the main findings of recent studies on the label-free single-molecule (protein) detection by nanomechanical systems including those focusing on the protein adsorption on various substrate surfaces. Since the nanomechanical techniques are capable of detecting and manipulating proteins even at the single-molecule level, therefore, they are expected to open a new way of studying the dynamics of protein functions. It is noteworthy that, in contrast to other experimental methods, where only given protein properties like molecular weight or protein stiffness can be determined, the nanomechanical systems enable a real-time measurement of the multiple protein properties (e.g., mass, stiffness, and/or generated surface stress), making them suitable for the study of protein adsorption mechanisms. Moreover, we also discuss the possible future trends in label-free detection and analysis of dynamics of protein complexes with these nanomechanical systems.

Zobrazit více v PubMed

Aebersold R., Mann M. (2003). Mass spectrometry-based proteomics. Nature 422, 198–207. 10.1038/nature01511 PubMed DOI

Angel T. E., Aryal U. K., Hengel S. M., Baker E. S., Kelly R. T., Robinson E. W., et al. (2012). Mass spectrometry-based proteomics: Existing capabilities and future directions. Chem. Soc. Rev. 41, 3912–3928. 10.1039/c2cs15331a PubMed DOI PMC

Boisen A., Dohn S., keller S. S., Schmid S., Tenje M. (2011). Cantilever-like micromechanical sensors. Rep. Prog. Phys. 74, 036101. 10.1088/0034-4885/74/3/036101 DOI

Burg T. P., Godin M., Knudsen S. M., Shen W., Carlson G., Foster J. S., et al. (2007). Weighing of biomolecules, single cells and single nanoparticles in fluid. Nature 446, 1066–1069. 10.1038/nature05741 PubMed DOI

Chaste J., Eichler A., Moser J., Ceballos G., Rurali R., Bachtold A., et al. (2012). A nanomechanical mass sensor with yoctogram resolution. Nat. Nanotechnol. 7, 301–304. 10.1038/nnano.2012.42 PubMed DOI

De Pastina A., Maillard D., Villanueva L. G. (2018). Fabrication of suspended microchannel resonators with integrated piezoelectric transduction. Microelectron. Eng. 192, 83–87. 10.1016/j.mee.2018.02.011 DOI

Deng F., Zhai W., Yin Y., Peng C., Ning C. (2021). Advanced protein adsorption properties of a novel silicate-based bioceramic: A proteomic analysis. Bioact. Mat. 6, 208–218. 10.1016/j.bioactmat.2020.08.011 PubMed DOI PMC

Dohn S., Sandberg R., Svendsen W., Boisen A. (2005). Enhanced functionality of cantilever based mass sensors using higher modes. Appl. Phys. Lett. 86, 233501. 10.1063/1.1948521 DOI

Dohn S., Schmid S., Amiot F., Boisen A. (2007). Position and mass determination of multiple particles using cantilever based mass sensors. Appl. Phys. Lett. 97, 044103. 10.1063/1.3473761 DOI

Dominguez-Medina S., Fostner S., Defoort M., Sansa M., Stark A.-K., Halim M. A., et al. (2018). Neutral mass spectrometry of virus capsids above 100 megadaltons with nanomechanical resonators. Science 362, 918–922. 10.1126/science.aat6457 PubMed DOI

Dorignac J., Kalinowski A., Erramilli S., Mohanty P. (2006). Dynamical response of nanomechanical oscillators in immiscible viscous fluid for in vitro biomolecular recognition. Phys. Rev. Lett. 96, 186105. 10.1103/PhysRevLett.96.186105 PubMed DOI

Eisner V., Picard M., Hajnóczky G. (2018). Mitochondrial dynamics in adaptive and maladaptive cellular stress responses. Nat. Cell. Biol. 20, 755–765. 10.1038/s41556-018-0133-0 PubMed DOI PMC

Ekinci K., Yang Y. T., Roukes M. L. (2004). Ultimate limits to inertial mass sensing based upon nanoelectromechanical systems. J. Appl. Phys. 95, 2682–2689. 10.1063/1.1642738 DOI

Eom K., Park H-S., Yoon D. S., Kwon T. (2011). Nanomechanical resonators and their applications in biological/chemical detection: Nanomechanics principles. Phys. Rep. 503, 115–163. 10.1016/j.physrep.2011.03.002 DOI

Erdogan R. T., Alkhaled M., Kaynak B. E., Alhmoud H., Pisheh H. S., Kellici M., et al. (2022). Atmospheric pressure mass spectrometry of single viruses and nanoparticles by nanoelectromechanical systems. ACS Nano 16, 3821–3833. 10.1021/acsnano.1c08423 PubMed DOI

Ghatkesar M. K., Barwich V., Braun T., Ramseyer J.-P., Gerber C., Hegner M., et al. (2007). Higher modes of vibration increase mass sensitivity in nanomechanical microcantilevers. Nanotechnology 18, 445502. 10.1088/0957-4484/18/44/445502 DOI

Gil-Santos E., Ramos D., Martínez F., RegúlezGarcía J. M. R., San Paulo A., Garcia R., et al. (2010). Nanomechanical mass sensing and stiffness spectrometry based on two-dimensional vibrations of resonant nanowires. Nat. Nanotech. 5, 641–645. 10.1038/nnano.2010.151 PubMed DOI

Gil-Santos E., Ruz J. J., Malvar O., Favero I., Lemaître A., Kosaka P. M., et al. (2020). Optomechanical detection of vibration modes of a single bacterium. Nat. Nanotech. 15, 469–474. 10.1038/s41565-020-0672-y PubMed DOI

Gruber G., Urgell C., Tavernarakis A., Stavrinadis A., Tepsic S., magen C., et al. (2019). Mass sensing for the advanced fabrication of nanomechanical resonators. Nano Lett. 19, 6987–6992. 10.1021/acs.nanolett.9b02351 PubMed DOI PMC

Gupta A. K., Nair P. R., Akin D., Ladisch M. R., Broyles S., Alam M. A., et al. (2006). Anomalous resonance in a nanomechanical biosensor. Proc. Natl. Acad. Sci. U. S. A. 5, 13362–13367. 10.1073/pnas.0602022103 PubMed DOI PMC

Hanay M. S., Kelber S., Naik A. K., Chi D., Hentz S., Bullard E., et al. (2012). Single-protein nanomechanical mass spectrometry in real time. Nat. Nanotechnol. 7, 602–608. 10.1038/nnano.2012.119 PubMed DOI PMC

Jensen K., Kim K., Zettl A. (2008). An atomic-resolution nanomechanical mass sensor. Nat. Nanotechnol. 3, 533–537. 10.1038/nnano.2008.200 PubMed DOI

Johnson E. C. B., Dammer E. B., Duong D. M., Ping L., Zhou M., Yin L., et al. (2020). Large-scale proteomic analysis of Alzheimer’s disease brain and cerebrospinal fluid reveals early changes in energy metabolism associated with microglia and astrocyte activation. Nat. Med. 26, 769–780. 10.1038/s41591-020-0815-6 PubMed DOI PMC

Juan J. M. S., No M. L., Schuh C. A. (2008). Superelasticity and shape memory in micro- and nanometer-scale pillars. Adv. Mat. 20, 272–278. 10.1002/adma.200701527 DOI

Karabalin R. B., Villanueva L. G., Matheny M. H., Sader J. E., Roukes M. L. (2012). Stress-induced variations in the stiffness of micro- and nanocantilever beams. Phys. Rev. Lett. 108, 236101. 10.1103/PhysRevLett.108.236101 PubMed DOI PMC

Keifer D. Z., Pierson E. E., Jarrold M. F. (2017). Charge detection mass spectrometry: Weighing heavier things. Analyst 142, 1654–1671. 10.1039/C7AN00277G PubMed DOI

Kidane S., Ishida H., Sawada K., Takahashi K. (2020). A suspended-graphene based optical interferometric surface stress sensor for selective biomolecular detection. Nanoscale Adv. 2, 1431–1436. 10.1039/C9NA00788A PubMed DOI PMC

Kim J., Song J., Kim K., Kim S., Song J., Kim N., et al. (2016). Hollow microtube resonators via silicon self-assembly toward subattogram mass sensing applications. Nano Lett. 16, 1537–1545. 10.1021/acs.nanolett.5b03703 PubMed DOI

Kozinsky I., Postma H. W. Ch., Bargatin I., Roukes M. L. (2006). Tuning nonlinearity, dynamic range, and frequency of nanomechanical resonators. Appl. Phys. Lett. 88, 253101. 10.1063/1.2209211 DOI

Kubiak-Ossowska K., Jachimska B., Al Qaraghuli M., Mulheran P. A. (2019). Protein interactions with negatively charged inorganic surfaces. Curr. Opin. Colloid Interface Sci. 41, 104–117. 10.1016/j.cocis.2019.02.001 DOI

Lachut M. J., Sader J. E. (2007). Effect of surface stress on the stiffness of cantilever plates. Phys. Rev. Lett. 99, 206102. 10.1103/PhysRevLett.99.206102 PubMed DOI

Lachut M. J., Sader J. E. (2012). Effect of surface stress on the stiffness of thin elastic plates and beams. Phys. Rev. B 85, 085440. 10.1103/PhysRevB.85.085440 PubMed DOI

Lamberti F-R., Palanchoke U., Geurts T. P. J., Gely M., Regord S., Banniard L., et al. (2022). Real-time sensing with multiplexed optomechanical resonators. Nano Lett. 22, 1866–1873. 10.1021/acs.nanolett.1c04017 PubMed DOI

Li M.-L., Wang W., Jin Z.-B. (2021). Circular RNAs in the central nervous system. Front. Mol. Biosci. 8, 629593. 10.3389/fmolb.2021.629593 PubMed DOI PMC

Liu W., Wang J., Yu Y., Chang Y., Tang N., Qu H., et al. (2015). Tuning the resonant frequency of resonators using molecular surface self-assembly approach. ACS Appl. Mat. Interfaces 7, 950–958. 10.1021/am507640g PubMed DOI

Lyu M., Zhao J., Kacem N., Liu P., Tang B., Xiong Z., et al. (2020). Exploiting nonlinearity to enhance the sensitivity of mode-localized mass sensor based on electrostatically coupled MEMS resonators. Int. J. Non-Linear Mech. 121, 103455. 10.1016/j.ijnonlinmec.2020.103455 DOI

Ma S., Li M., Wang S., Liu H., Wang H., Ren L., et al. (2022). Multiple particle identification by sequential frequency-shift measurement of a micro-plate. Int. J. Mech. Sci. 231, 107587. 10.1016/j.ijmecsci.2022.107587 DOI

Malvar O., Ruz J. J., Kosaka P. M., Dominguez C. M., Gil-Santos E., Calleja M., et al. (2016). Mass and stiffness spectrometry of nanoparticles and whole intact bacteria by multimode nanomechanical resonators. Nat. Commun. 11, 13452. 10.1038/ncomms13452 PubMed DOI PMC

Minami K., Shiba K., Yoshikawa G. (2021). Sorption-induced static mode nanomechanical sensing with viscoelastic receptor layers for multistep injection-purge cycles. J. Appl. Phys. 129, 124503. 10.1063/5.0039045 DOI

Minami K., Yoshikawa G. (2021). Effects of partial attachment at the interface between receptor and substrate on nanomechanical cantilever sensing. Sens. Act. A Phys. 319, 112533. 10.1016/j.sna.2020.112533 DOI

Naik A. K., Hanay M. S., Hiebert W. K., Feng X. L., Roukes M. L. (2009). Towards single-molecule nanomechanical mass spectrometry. Nat. Nanotechnol. 4, 445–450. 10.1038/nnano.2009.152 PubMed DOI PMC

Pfeifer C. R., Alveya C. M., Iriantoa J., Dischera D. E. (2017). Genome variation across cancers scales with tissue stiffness – An invasion-mutation mechanism and implications for immune cell infiltration. Curr. Opin. Syst. Biol. 2, 103–114. 10.1016/j.coisb.2017.04.005 PubMed DOI PMC

Richard P. J. (2019). Protein flexibility and stiffness enable efficient enzymatic catalysis. J. Am. Chem. Soc. 141, 3320–3331. 10.1021/jacs.8b10836 PubMed DOI PMC

Rocha R. T., Alfosail F., Zhao W., Younis M. I., Masri S. F. (2021). Nonparametric identification of a micro-electromechanical resonator. Mech. Syst. Sig. Proc. 161, 107932. 10.1016/j.ymssp.2021.107932 DOI

Ruz J. J., Malvar O., Gil-Santos E., Ramos D., Calleja M., Tamayo J. (2021). A review on theory and modelling of nanomechanical sensors for biological applications. Process 9, 164. 10.3390/pr9010164 DOI

Ruz J. J., Tamayo J., Pini V., Kosaka P. M., Calleja M. (2014) Physics of nanomechanical spectrometry of viruses. Sci. Rep. 4, 6051; 10.1038/srep06051 PubMed DOI PMC

Sader J. E., Hanay M. S., Neumann A. P., Roukes M. L. (2018). Mass spectrometry using nanomechanical systems: Beyond the point-mass approximation. Nano Lett. 18, 1608–1614. 10.1021/acs.nanolett.7b04301 PubMed DOI

Sage E., Brenac A., Alava T., Morel R., Dupré C., Hanay M. S., et al. (2015). Neutral particle mass spectrometry with nanomechanical systems. Nat. Commun. 6, 6482. 10.1038/ncomms7482 PubMed DOI PMC

Sage E., Sansa M., Fostner S., Defoort M., Gely M., Naik A. K., et al. (2018). Single-particle mass spectrometry with arrays of frequency-addressed nanomechanical resonators. Nat. Commun. 9, 3283. 10.1038/s41467-018-05783-4 PubMed DOI PMC

Sansa M., Defoort M., Brenac A., Hermouet M., Banniard L., Fafin A., et al. (2020). Optomechanical mass spectrometry. Nat. Commun. 11, 3781. 10.1038/s41467-020-17592-9 PubMed DOI PMC

Satzer P., Svec F., Sekot G., Jungbauer A. (2015). Protein adsorption onto nanoparticles induces conformational changes: Particle size dependency, kinetics, and mechanisms. Eng. Life. Sci. 16, 238–246. 10.1002/elsc.201500059 PubMed DOI PMC

Schmid S., Dohn S., Boisen A. (2010). Real-time particle mass spectrometry based on resonant micro strings. Sensors 10, 8092–8100. 10.3390/s100908092 PubMed DOI PMC

Senese N. B., Rasenick M. M., Traynor J. R. (2018). The role of G-proteins and G-protein regulating proteins in depressive disorders. Front. Pharmacol. 9, 1289. 10.3389/fphar.2018.01289 PubMed DOI PMC

Shen L., de Sousa F. B., Tay N. B., Lang T. S., Kaixin V. L., Han J., et al. (2020). Deformation behavior of normal human enamel: A study by nanoindentation. J. Mech. Behav. Biomed. Mat. 108, 103799. 10.1016/j.jmbbm.2020.103799 PubMed DOI

Snijder J., Rose R. J., Veesler D., Johnson J. E., Heck A. J. R. (2013). Studying 18MDa virus assemblies with native mass spectrometry. Angew. Chem. Int. Ed. 52, 4020–4023. 10.1002/anie.201210197 PubMed DOI PMC

Stachiv I., Alarcon E., Lamac M. (2021). Shape memory alloys and polymers for MEMS/NEMS applications: Review on recent findings and challenges in design, preparation, and characterization. Metals 11, 415. 10.3390/met11030415 DOI

Stachiv I., Fedorchenko A. I., Chen Y-L. (2012). Mass detection by means of the vibrating nanomechanical resonators. Appl. Phys. Lett. 100, 093110. 10.1063/1.3691195 DOI

Stachiv I., Gan L. (2019). Hybrid shape memory alloy-based nanomechanical resonators for ultrathin film elastic properties determination and heavy mass spectrometry. Materials 12, 3593. 10.3390/ma12213593 PubMed DOI PMC

Stachiv I., Gan L., Kuo C.-Y., Sittner P., Sevecek O. (2020). Mass spectrometry of heavy analytes and large biological aggregates by monitoring changes in the quality factor of nanomechanical resonators in air. ACS Sens. 5, 2128–2135. 10.1021/acssensors.0c00756 PubMed DOI

Stachiv I. (2014). Impact of surface and residual stresses and electro-/magnetostatic axial loading on the suspended nanomechanical based mass sensors: A theoretical study. J. Appl. Phys. 115, 214310. 10.1063/1.4880396 DOI

Stachiv I., Machu Z., Sevecek O., Jeng Y.-R., Li W.-L., Kotoul M., et al. (2022b). Achievable accuracy of resonating nanomechanical systems for mass sensing of larger analytes in GDa range. Int. J. Mech. Sci. 224, 107353. 10.1016/j.ijmecsci.2022.107353 DOI

Stachiv I., Machu Z., Sevecek O., Tuhovcak O., Kotoul M., Jeng Y.-R. (2022a). Resolving measurement of large (∼ GDa) chemical/biomolecule complexes with multimode nanomechanical resonators. Sens. Act. B Chem. 353, 131062. 10.1016/j.snb.2021.131062 DOI

Stachiv I., Sittner P. (2018). Nanocantilevers with adjustable static deflection and significantly tunable spectrum resonant frequencies for applications in nanomechanical mass sensors. Nanomaterials 8, 116. 10.3390/nano8020116 PubMed DOI PMC

Stachiv I., Sittner P., Olejnicek J., Landa M., Heller L. (2017). Exploiting NiTi shape memory alloy films in design of tunable high frequency microcantilever resonators. Appl. Phys. Lett. 111, 213105. 10.1063/1.4998006 DOI

Stachiv I., Zapomel J., Chen Y-L. (2014). Simultaneous determination of the elastic modulus and density/thickness of ultrathin films utilizing micro-/nanoresonators under applied axial force. J. Appl. Phys. 115, 124304. 10.1063/1.4869415 DOI

Stassi S., De Laurentis G., Chakraborty D., Bejtka K., Chiodoni A., Sader J. E., et al. (2019). Large-scale parallelization of nanomechanical mass spectrometry with weakly-coupled resonators. Nat. Commun. 10, 3647. 10.1038/s41467-019-11647-2 PubMed DOI PMC

Su Renay S-C., Gill E. E., Kim Y., Liu J. C. (2019). Characterization of resilin-like proteins with tunable mechanical properties. J. Mech. Behav. Biomed. Mat. 91, 68–75. 10.1016/j.jmbbm.2018.11.015 PubMed DOI PMC

Talha M., Ma Y., Kumar P., Lin Y., Singh A. (2019). Role of protein adsorption in the bio corrosion of metallic implants – a review. Colloids Surf. B Biointerfaces 176, 494–506. 10.1016/j.colsurfb.2019.01.038 PubMed DOI

Tamayo J., Kosaka P. M., Ruz J. J., San Paulo A., Calleja M. (2013). Biosensors based on nanomechanical systems. Chem. Soc. Rev. 42, 1287–1311. 10.1039/C2CS35293A PubMed DOI

Tamayo J., Ramos D., Mertens J., Calleja M. (2006). Effect of the adsorbate stiffness on the resonance response of microcantilever sensors. Appl. Phys. Lett. 89, 224104. 10.1063/1.2388925 DOI

Urbanska M., Muñoz H. E., Shaw B., Otto O., Manalis S. R., Di Carlo D., et al. (2020). A comparison of microfluidic methods for high-throughput cell deformability measurements. Nat. Methods 17, 587–593. 10.1038/s41592-020-0818-8 PubMed DOI PMC

Wingert B., Krieger J., Li H., Bahar I. (2021). Adaptability and specificity: How do proteins balance opposing needs to achieve function? Curr. Opin. Struct. Biol. 67, 25–32. 10.1016/j.sbi.2020.08.009 PubMed DOI PMC

Xia C., Wang D. F., Ono T., Itoh T., Esashi M. (2021). Internal resonance in coupled oscillators – Part I: A double amplification mass sensing scheme without duffing nonlinearity. Mech. Syst. Sig. Proc. 159, 107886. 10.1016/j.ymssp.2021.107886 DOI

Xu B., Zhang P., Zhu J., Liu Z., Eichler A., Zheng X.-Q., et al. (2022). Nanomechanical resonators: Toward atomic scale. ACS Nano 16, 15545–15585. (accepted). 10.1021/acsnano.2c01673 PubMed DOI PMC

Yang B., Liu Z., Liu H., Nash M. A. (2020). Next generation methods for single-molecule force spectroscopy on polyproteins and receptor-ligand complexes. Front. Mol. Biosci. 7, 85. 10.3389/fmolb.2020.00085 PubMed DOI PMC

Yang D., Ward A., Halvorsen K., Wong W. P. (2016). Multiplexed single-molecule force spectroscopy using a centrifuge. Nat. Commun. 7, 11026. 10.1038/ncomms11026 PubMed DOI PMC

Yang Y. T., Callegari C., Feng X. L., Ekinci K. L., Rooukes M. L. (2006). Zeptogram-scale nanomechanical mass sensing. Nano Lett. 6, 583–586. 10.1021/nl052134m PubMed DOI

Yi X., Duan H. L. (2009). Surface stress induced by interactions of adsorbates and its effect on deformation and frequency of microcantilever sensors. J. Mech. Phys. Solids 57, 1254–1266. 10.1016/j.jmps.2009.04.010 DOI

Yuksel M., Orhan E., Yanik C., Ari A. B., Demir A., Hanay M. S. (2019). Nonlinear nanomechanical mass spectrometry at the single-nanoparticle level. Nano Lett. 19, 3583–3589. 10.1021/acs.nanolett.9b00546 PubMed DOI

Zhang G., Li C., Wu S., Zhang Q. (2018). Label-free aptamer-based detection of microcystin-LR using a microcantilever array biosensor. Sens. Act. B Chem. 260, 42–47. 10.1016/j.snb.2017.12.112 DOI

Zhang W.-M., Hu K.-M., Peng Z.-K., Meng G. (2015). Tunable micro- and nanomechanical resonators. Sensors 15, 26478–26566. 10.3390/s151026478 PubMed DOI PMC

Zhao D., Liu Y., Zhang Q., Zhang Y., Zhang W., Duan Q., et al. (2019). Surface stress-based biosensor with stable conductive AuNPs network for biomolecules detection. Appl. Surf. Sci. 491, 443450–450. 10.1016/j.apsusc.2019.06.178 DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...