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Current Topics in Medicinal Chemistry


ISSN (Print): 1568-0266
ISSN (Online): 1873-4294

Review Article

Atomic Force Microscopy: The Characterisation of Amyloid Protein Structure in Pathology

Author(s): Maria J.E. Visser and Etheresia Pretorius*

Volume 19, Issue 32, 2019

Page: [2958 - 2973] Pages: 16

DOI: 10.2174/1568026619666191121143240

Price: $65


Proteins are versatile macromolecules that perform a variety of functions and participate in virtually all cellular processes. The functionality of a protein greatly depends on its structure and alterations may result in the development of diseases. Most well-known of these are protein misfolding disorders, which include Alzheimer’s and Parkinson’s diseases as well as type 2 diabetes mellitus, where soluble proteins transition into insoluble amyloid fibrils. Atomic Force Microscopy (AFM) is capable of providing a topographical map of the protein and/or its aggregates, as well as probing the nanomechanical properties of a sample. Moreover, AFM requires relatively simple sample preparation, which presents the possibility of combining this technique with other research modalities, such as confocal laser scanning microscopy, Raman spectroscopy and stimulated emission depletion microscopy. In this review, the basic principles of AFM are discussed, followed by a brief overview of how it has been applied in biological research. Finally, we focus specifically on its use as a characterisation method to study protein structure at the nanoscale in pathophysiological conditions, considering both molecules implicated in disease pathogenesis and the plasma protein fibrinogen. In conclusion, AFM is a userfriendly tool that supplies multi-parametric data, rendering it a most valuable technique.

Keywords: Atomic force microscopy, Protein structure, Amyloid, Disease, Correlative microscopy, NMR.

Graphical Abstract
Berg, J.M.; Tymoczko, J.L.; Stryer, L. Biochemistry, 5th ed; W.H. Freeman: New York, 2002.
Geyer, P.E.; Holdt, L.M.; Teupser, D.; Mann, M. Revisiting biomarker discovery by plasma proteomics. Mol. Syst. Biol., 2017, 13(9), 942.
[] [PMID: 28951502]
Anderson, N.L.; Anderson, N.G. The human plasma proteome: history, character, and diagnostic prospects. Mol. Cell. Proteomics, 2002, 1(11), 845-867.
[] [PMID: 12488461]
Chiti, F.; Dobson, C.M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem., 2006, 75, 333-366.
[] [PMID: 16756495]
Eisenberg, D.; Jucker, M. The amyloid state of proteins in human diseases. Cell, 2012, 148(6), 1188-1203.
[] [PMID: 22424229]
Toyama, B.H.; Weissman, J.S. Amyloid structure: conformational diversity and consequences. Annu. Rev. Biochem., 2011, 80, 557-585.
[] [PMID: 21456964]
Wechalekar, A.D.; Gillmore, J.D.; Hawkins, P.N. Systemic amyloidosis. Lancet, 2016, 387(10038), 2641-2654.
[] [PMID: 26719234]
Jackson, M.P.; Hewitt, E.W. Why are functional amyloids non-toxic in humans? Biomolecules, 2017, 7(4), 1-13.
[] [PMID: 28937655]
Smyth, M.S.; Martin, J.H.J. X Ray crystallography. Mol. Pathol., 2000, 53, 8-14.
Marion, D. An introduction to biological NMR spectroscopy. Mol. Cell. Proteomics, 2013, 12(11), 3006-3025.
[] [PMID: 23831612]
Binnig, G.; Rohrer, H.; Gerber, C.; Weibel, E. Surface studies by scanning tunneling microscopy. Phys. Rev. Lett., 1982, 49, 57-61.
Binnig, G.; Quate, C.F.; Gerber, C. Atomic force microscope. Phys. Rev. Lett., 1986, 56(9), 930-933.
[] [PMID: 10033323]
Bowen, W.R.; Hilal, N. Atomic force microscopy in process engineering– An introduction to AFM for improved processes and products micro/nanoengineering and AFM for cellular sensing, 1st ed; Butterworth-Heinemann: Oxford, 2009.
Giessibl, F.J. Advances in atomic force microscopy. Rev. Mod. Phys., 2003, 75, 949-983.
Binnig, G.; Gerber, C.; Stoll, E.; Albrecht, T.R.; Quate, C.F. Atomic resolution with atomic force microscope. Europhys. Lett., 1987, 3, 1281-1286.
Vinckier, A.; Semenza, G. Measuring elasticity of biological materials by atomic force microscopy. FEBS Lett., 1998, 430(1-2), 12-16.
[] [PMID: 9678586]
Zlatanova, J.; Lindsay, S.M.; Leuba, S.H. Single molecule force spectroscopy in biology using the atomic force microscope. Prog. Biophys. Mol. Biol., 2000, 74(1-2), 37-61.
[] [PMID: 11106806]
Alessandrini, A.; Facci, P. AFM: a versatile tool in biophysics. Meas. Sci. Technol., 2005, 16, 65-92.
McConney, M.E.; Singamaneni, S.; Tsukruk, V.V. Probing soft matter with the atomic force microscopies: imaging and force spectroscopy. Polym. Rev. (Phila. Pa.), 2010, 50, 235-286.
Buechner, C.N.; Tessmer, I. DNA substrate preparation for atomic force microscopy studies of protein-DNA interactions. J. Mol. Recognit., 2013, 26(12), 605-617.
[] [PMID: 24277605]
Lyubchenko, Y.L.; Shlyakhtenko, L.S.; Ando, T. Imaging of nucleic acids with atomic force microscopy. Methods, 2011, 54(2), 274-283.
[] [PMID: 21310240]
Li, M.; Liu, L.; Xi, N.; Wang, Y.; Dong, Z.; Xiao, X.; Zhang, W. Atomic force microscopy imaging of live mammalian cells. Sci. China Life Sci., 2013, 56(9), 811-817.
[] [PMID: 23929002]
Vadillo-Rodríguez, V.; Busscher, H.J.; Norde, W.; De Vries, J.; Dijkstra, R.J.; Stokroos, I.; Van Der Mei, H.C. Comparison of atomic force microscopy interaction forces between bacteria and silicon nitride substrata for three commonly used immobilization methods. Appl. Environ. Microbiol., 2004, 70(9), 5441-5446.
[] [PMID: 15345431]
Bolshakova, A.V.; Kiselyova, O.I.; Yaminsky, I.V. Microbial surfaces investigated using atomic force microscopy. Biotechnol. Prog., 2004, 20(6), 1615-1622.
[] [PMID: 15575691]
Doktycz, M.J.; Sullivan, C.J.; Hoyt, P.R.; Pelletier, D.A.; Wu, S.; Allison, D.P. AFM imaging of bacteria in liquid media immobilized on gelatin coated mica surfaces. Ultramicroscopy, 2003, 97(1-4), 209-216.
[] [PMID: 12801673]
Micic, M.; Hu, D.; Suh, Y.D.; Newton, G.; Romine, M.; Lu, H.P. Correlated atomic force microscopy and fluorescence lifetime imaging of live bacterial cells. Colloids Surf. B Biointerfaces, 2004, 34(4), 205-212.
[] [PMID: 15261059]
Dupres, V.; Menozzi, F.D.; Locht, C.; Clare, B.H.; Abbott, N.L.; Cuenot, S.; Bompard, C.; Raze, D.; Dufrêne, Y.F. Nanoscale mapping and functional analysis of individual adhesins on living bacteria. Nat. Methods, 2005, 2(7), 515-520.
[] [PMID: 15973422]
Touhami, A.; Jericho, M.H.; Beveridge, T.J. Atomic force microscopy of cell growth and division in Staphylococcus aureus. J. Bacteriol., 2004, 186(11), 3286-3295.
[] [PMID: 15150213]
Butt, H-J.; Cappella, B.; Kappl, M. Force measurements with the atomic force microscope: Technique, interpretation and applications. Surf. Sci. Rep., 2005, 59, 1-152.
Persson, B.N.J.; Albohr, O.; Tartaglino, U.I. V. A.; Tosatti, E. On the nature of surface roughness with application to contact mechanics, sealing, rubber friction and adhesion. J. Phys. Condens. Matter, 2005, 17, 1-62.
Bhushan, B. The nature of surfaces. In: Modern Tribology Handbook, Two Volume Set; CRC Press: Florida, 2001; p. 1760.
Gadelmawla, E.S.; Koura, M.M.; Maksoud, T.M.A.; Elewa, I.M.; Soliman, H.H. Roughness parameters. J. Mater. Process. Technol., 2002, 123, 133-145.
Lee, C.-W.; Wang, C.-C.; Lee, C.-H. Mechanoprofiling on membranes of living cells with atomic force microscopy and optical nano- profilometry. Advances in Physics: X, 2017, 2, 608-621.
Simpson, G.J.; Sedin, D.L.; Rowlen, K.L. Surface roughness by contact versus tapping mode atomic force microscopy. Langmuir, 1999, 15, 1429-1434.
Sedin, D.L.; Rowlen, K.L. Influence of tip size on AFM roughness measurements. Appl. Surf. Sci., 2001, 182, 40-48.
Kim, K.S.; Cho, C.H.; Park, E.K.; Jung, M.H.; Yoon, K.S.; Park, H-K. AFM-detected apoptotic changes in morphology and biophysical property caused by paclitaxel in Ishikawa and HeLa cells. PLoS One, 2012, 7(1) e30066
[] [PMID: 22272274]
Hu, M.; Wang, J.; Zhao, H.; Dong, S.; Cai, J. Nanostructure and nanomechanics analysis of lymphocyte using AFM: from resting, activated to apoptosis. J. Biomech., 2009, 42(10), 1513-1519.
[] [PMID: 19477449]
Buys, A.V.; Van Rooy, M-J.; Soma, P.; Van Papendorp, D.; Lipinski, B.; Pretorius, E. Changes in red blood cell membrane structure in type 2 diabetes: a scanning electron and atomic force microscopy study. Cardiovasc. Diabetol., 2013, 12, 25.
[] [PMID: 23356738]
Wang, Y.; Xu, C.; Jiang, N.; Zheng, L.; Zeng, J.; Qiu, C.; Yang, H.; Xie, S. Quantitative analysis of the cell-surface roughness and viscoelasticity for breast cancer cells discrimination using atomic force microscopy. Scanning, 2016, 38(6), 558-563.
[] [PMID: 26750438]
Girasole, M.; Pompeo, G.; Cricenti, A.; Longo, G.; Boumis, G.; Bellelli, A.; Amiconi, S. The how, when, and why of the aging signals appearing on the human erythrocyte membrane: an atomic force microscopy study of surface roughness. Nanomedicine (Lond.), 2010, 6(6), 760-768.
[] [PMID: 20603227]
Kuznetsova, T. G.; Starodubtseva, M. N.; Yegorenkov, N. I.; Chizhik, S. A.; Zhdanov, R. I. Atomic force microscopy probing of cell elasticity. Micron (Oxford, England : 1993), 2007, 38, 824-833.
Berthold, T.; Benstetter, G.; Frammelsberger, W.; Rodriguez, R.; Nafrid, A.M. Numerical study of hydrodynamic forces for AFM operations in liquid. Scanning, 2017, 2017, 12.
Grant, C.A.; Brockwell, D.J.; Radford, S.E.; Thomson, N.H. Tuning the elastic modulus of hydrated collagen fibrils. Biophys. J., 2009, 97(11), 2985-2992.
[] [PMID: 19948128]
Dulińska, I.; Targosz, M.; Strojny, W.; Lekka, M.; Czuba, P.; Balwierz, W.; Szymoński, M. Stiffness of normal and pathological erythrocytes studied by means of atomic force microscopy. J. Biochem. Biophys. Methods, 2006, 66(1-3), 1-11.
[] [PMID: 16443279]
Wu, X.; Muthuchamy, M.; Reddy, D.S. Atomic force microscopy protocol for measurement of membrane plasticity and extracellular interactions in single neurons in epilepsy. Front. Aging Neurosci., 2016, 8, 88.
[] [PMID: 27199735]
Lieber, S.C.; Aubry, N.; Pain, J.; Diaz, G.; Kim, S-J.; Vatner, S.F. Aging increases stiffness of cardiac myocytes measured by atomic force microscopy nanoindentation. Am. J. Physiol. Heart Circ. Physiol., 2004, 287(2), H645-H651.
[] [PMID: 15044193]
Zahn, J.T.; Louban, I.; Jungbauer, S.; Bissinger, M.; Kaufmann, D.; Kemkemer, R.; Spatz, J.P. Age-dependent changes in microscale stiffness and mechanoresponses of cells. Small, 2011, 7(10), 1480-1487.
[] [PMID: 21538869]
Xiao, L.; Tang, M.; Li, Q.; Zhou, A. Non-invasive detection of biomechanical and biochemical responses of human lung cells to short time chemotherapy exposure using AFM and confocal Raman spectroscopy. Anal. Methods, 2013, 5(4), 874-879.
Xu, W.; Mezencev, R.; Kim, B.; Wang, L.; McDonald, J.; Sulchek, T. Cell stiffness is a biomarker of the metastatic potential of ovarian cancer cells. PLoS One, 2012, 7(10)e46609
[] [PMID: 23056368]
Li, Q.S.; Lee, G.Y.H.; Ong, C.N.; Lim, C.T. AFM indentation study of breast cancer cells. Biochem. Biophys. Res. Commun., 2008, 374(4), 609-613.
[] [PMID: 18656442]
Smith, C. Microscopy: Two microscopes are better than one. Nature, 2012, 492(7428), 293-297.
[] [PMID: 23235883]
Jahn, K. A.; Barton, D. A.; Kobayashi, K.; Ratinac, K. R.; Overall, R. L.; Braet, F. Correlative microscopy: Providing new understanding in the biomedical and plant sciences. Micron. (Oxford, England: 1993), 2012, 43, 565-582.
Cascione, M.; de Matteis, V.; Rinaldi, R.; Leporatti, S. Atomic force microscopy combined with optical microscopy for cells investigation. Microsc. Res. Tech., 2017, 80(1), 109-123.
[] [PMID: 27324056]
Hauser, M.; Wojcik, M.; Kim, D.; Mahmoudi, M.; Li, W.; Xu, K. Correlative super-resolution microscopy: new dimensions and new opportunities. Chem. Rev., 2017, 117(11), 7428-7456.
[] [PMID: 28045508]
Paddock, S.W. Principles and practices of laser scanning confocal microscopy. Mol. Biotechnol., 2000, 16(2), 127-149.
[] [PMID: 11131973]
St Croix, C.M.; Shand, S.H.; Watkins, S.C. Confocal microscopy: comparisons, applications, and problems. Biotechniques, 2005, 39(6)(Suppl.), S2-S5.
[] [PMID: 20158500]
Laskowski, P.R.; Pfreundschuh, M.; Stauffer, M.; Ucurum, Z.; Fotiadis, D.; Müller, D.J. High-resolution imaging and multiparametric characterization of native membranes by combining confocal microscopy and an atomic force microscopy-based toolbox. ACS Nano, 2017, 11(8), 8292-8301.
[] [PMID: 28745869]
Deng, Z.; Zink, T.; Chen, H.Y.; Walters, D.; Liu, F.T.; Liu, G.Y. Impact of actin rearrangement and degranulation on the membrane structure of primary mast cells: a combined atomic force and laser scanning confocal microscopy investigation. Biophys. J., 2009, 96(4), 1629-1639.
[] [PMID: 19217878]
Kuyukina, M.S.; Ivshina, I.B.; Korshunova, I.O.; Rubtsova, E.V. Assessment of bacterial resistance to organic solvents using a combined confocal laser scanning and atomic force microscopy (CLSM/AFM). J. Microbiol. Methods, 2014, 107, 23-29.
[] [PMID: 25193441]
Shaw, J.E.; Alattia, J.R.; Verity, J.E.; Privé, G.G.; Yip, C.M. Mechanisms of antimicrobial peptide action: studies of indolicidin assembly at model membrane interfaces by in situ atomic force microscopy. J. Struct. Biol., 2006, 154(1), 42-58.
[] [PMID: 16459101]
Krause, M.; Te Riet, J.; Wolf, K. Probing the compressibility of tumor cell nuclei by combined atomic force-confocal microscopy. Phys. Biol., 2013, 10(6)065002
[] [PMID: 24304807]
Staunton, J.R.; Doss, B.L.; Lindsay, S.; Ros, R. Correlating confocal microscopy and atomic force indentation reveals metastatic cancer cells stiffen during invasion into collagen I matrices. Sci. Rep., 2016, 6, 19686.
[] [PMID: 26813872]
Rosso, G.; Liashkovich, I.; Young, P.; Shahin, V. Nano-scale biophysical and structural investigations on intact and neuropathic nerve fibers by simultaneous combination of atomic force and confocal microscopy. Front. Mol. Neurosci., 2017, 10, 277.
[] [PMID: 28912683]
Hanlon, E.B.; Manoharan, R.; Koo, T-W.; Shafer, K.E.; Motz, J.T.; Fitzmaurice, M.; Kramer, J.R.; Itzkan, I.; Dasari, R.R.; Feld, M.S. Prospects for in vivo Raman spectroscopy. Phys. Med. Biol., 2000, 45(2), R1-R59.
[] [PMID: 10701500]
Movasaghi, Z.; Rehman, S.; Rehman, I.U. Raman Spectroscopy of Biological Tissues. Appl. Spectrosc. Rev., 2007, 42, 493-541.
Maase, M.; Rygula, A.; Pacia, M.Z.; Proniewski, B.; Mateuszuk, L.; Sternak, M.; Kaczor, A.; Chlopicki, S.; Kusche-Vihrog, K. Combined Raman- and AFM-based detection of biochemical and nanomechanical features of endothelial dysfunction in aorta isolated from ApoE/LDLR-/- mice. Nanomedicine (Lond.), 2019, 16, 97-105.
[] [PMID: 30550804]
Apetri, M.M.; Maiti, N.C.; Zagorski, M.G.; Carey, P.R.; Anderson, V.E. Secondary structure of alpha-synuclein oligomers: characterization by raman and atomic force microscopy. J. Mol. Biol., 2006, 355(1), 63-71.
[] [PMID: 16303137]
Brauchle, E.; Kasper, J.; Daum, R.; Schierbaum, N.; Falch, C.; Kirschniak, A.; Schäffer, T.E.; Schenke-Layland, K. Biomechanical and biomolecular characterization of extracellular matrix structures in human colon carcinomas. Matrix Biol., 2018, 68-69, 180-193.
[] [PMID: 29605717]
Tang, M.; McEwen, G.D.; Wu, Y.; Miller, C.D.; Zhou, A. Characterization and analysis of mycobacteria and Gram-negative bacteria and co-culture mixtures by Raman microspectroscopy, FTIR, and atomic force microscopy. Anal. Bioanal. Chem., 2013, 405(5), 1577-1591.
[] [PMID: 23196750]
Hell, S.W.; Wichmann, J. Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt. Lett., 1994, 19(11), 780-782.
[] [PMID: 19844443]
Blom, H.; Widengren, J. Stimulated emission depletion microscopy. Chem. Rev., 2017, 117(11), 7377-7427.
[] [PMID: 28262022]
Vangindertael, J.; Camacho, R.; Sempels, W.; Mizuno, H.; Dedecker, P.; Janssen, K.P.F. An introduction to optical super-resolution microscopy for the adventurous biologist. Methods Appl. Fluoresc., 2018, 6(2) 022003
[] [PMID: 29422456]
Chacko, J.V.; Zanacchi, F.C.; Diaspro, A. Probing cytoskeletal structures by coupling optical superresolution and AFM techniques for a correlative approach. Cytoskeleton (Hoboken), 2013, 70(11), 729-740.
[] [PMID: 24027190]
Chacko, J.V.; Harke, B.; Canale, C.; Diaspro, A. Cellular level nanomanipulation using atomic force microscope aided with superresolution imaging. J. Biomed. Opt., 2014, 19(10)105003
[] [PMID: 25291208]
Harke, B.; Chacko, J.V.; Haschke, H.; Canale, C.; Diaspro, A. A novel nanoscopic tool by combining AFM with STED microscopy. Opt. Nanoscopy, 2012, 1, 1-6.
Chacko, J.V.; Canale, C.; Harke, B.; Diaspro, A. Sub-diffraction nano manipulation using STED AFM. PLoS One, 2013, 8(6) e66608
[] [PMID: 23799123]
Curry, N.; Ghézali, G.; Kaminski Schierle, G.S.; Rouach, N.; Kaminski, C.F. Correlative STED and atomic force microscopy on live astrocytes reveals plasticity of cytoskeletal structure and membrane physical properties during polarized Migration. Front. Cell. Neurosci., 2017, 11, 104.
[] [PMID: 28469559]
Gan, Y. Atomic and subnanometer resolution in ambient conditions by atomic force microscopy. Surf. Sci. Rep., 2009, 64(3), 99-121.
Alcaraz, J.; Buscemi, L.; Grabulosa, M.; Trepat, X.; Fabry, B.; Farré, R.; Navajas, D. Microrheology of human lung epithelial cells measured by atomic force microscopy. Biophys. J., 2003, 84(3), 2071-2079.
[] [PMID: 12609908]
Mathur, A.B.; Collinsworth, A.M.; Reichert, W.M.; Kraus, W.E.; Truskey, G.A. Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy. J. Biomech., 2001, 34(12), 1545-1553.
[] [PMID: 11716856]
Docheva, D.; Padula, D.; Popov, C.; Mutschler, W.; Clausen-Schaumann, H.; Schieker, M. Researching into the cellular shape, volume and elasticity of mesenchymal stem cells, osteoblasts and osteosarcoma cells by atomic force microscopy. J. Cell. Mol. Med., 2008, 12(2), 537-552.
[] [PMID: 18419596]
Fritz, M.; Radmacher, M.; Gaub, H.E. Granula motion and membrane spreading during activation of human platelets imaged by atomic force microscopy. Biophys. J., 1994, 66(5), 1328-1334.
[] [PMID: 8061188]
Girasole, M.; Pompeo, G.; Cricenti, A.; Congiu-Castellano, A.; Andreola, F.; Serafino, A.; Frazer, B.H.; Boumis, G.; Amiconi, G. Roughness of the plasma membrane as an independent morphological parameter to study RBCs: a quantitative atomic force microscopy investigation. Biochim. Biophys. Acta, 2007, 1768(5), 1268-1276.
[] [PMID: 17320813]
Hsieh, C-H.; Lin, Y-H.; Lin, S.; Tsai-Wu, J-J.; Herbert Wu, C.H.; Jiang, C-C. Surface ultrastructure and mechanical property of human chondrocyte revealed by atomic force microscopy. Osteoarthritis Cartilage, 2008, 16(4), 480-488.
[] [PMID: 17869545]
Zhang, X.; Chen, A.; Leon, D.D.; Li, H.; Noiri, E.; Moy, V.T.; Goligorsky, M.S. Atomic force microscopy measurement of leukocyte-endothelial interaction. Am. J. Physiol. Heart Circ. Physiol., 2004, 286, 359-367.
Amro, N.A.; Kotra, L.P.; Wadu-mesthrige, K.; Bulychev, A.; Mobashery, S.; Liu, G-y. High-resolution atomic force microscopy studies of the escherichia coli outer membrane: structural basis for permeability. Langmuir, 2000, 16, 2789-2796.
Scheuring, S.; Sturgis, J.N. Chromatic adaptation of photosynthetic membranes. Science, 2005, 309(5733), 484-487.
[] [PMID: 16020739]
Camesano, T.A.; Natan, M.J.; Logan, B.E. Observation of changes in bacterial cell morphology using tapping mode atomic force Microscopy. Langmuir, 2000, 16, 4563-4572.
Meincken, M.; Holroyd, D.L.; Rautenbach, M. Atomic force microscopy study of the effect of antimicrobial peptides on the cell envelope of Escherichia coli. Antimicrob. Agents Chemother., 2005, 49(10), 4085-4092.
[] [PMID: 16189084]
Kuznetsov, Y.G.; Victoria, J.G.; Robinson, W.E., Jr; McPherson, A. Atomic force microscopy investigation of human immunodeficiency virus (HIV) and HIV-infected lymphocytes. J. Virol., 2003, 77(22), 11896-11909.
[] [PMID: 14581526]
Malkin, A.J.; McPherson, A.; Gershon, P.D. Structure of intracellular mature vaccinia virus visualized by in situ atomic force microscopy. J. Virol., 2003, 77(11), 6332-6340.
[] [PMID: 12743290]
Kuznetsov, Y.G.; Xiao, C.; Sun, S.; Raoult, D.; Rossmann, M.; McPherson, A. Atomic force microscopy investigation of the giant mimivirus. Virology, 2010, 404(1), 127-137.
[] [PMID: 20552732]
Castellanos, M.; Pérez, R.; Carrasco, C.; Hernando-Pérez, M.; Gómez-Herrero, J.; de Pablo, P.J.; Mateu, M.G. Mechanical elasticity as a physical signature of conformational dynamics in a virus particle. Proc. Natl. Acad. Sci. USA, 2012, 109(30), 12028-12033.
[] [PMID: 22797893]
Alsteens, D.; Newton, R.; Schubert, R.; Martinez-Martin, D.; Delguste, M.; Roska, B.; Müller, D.J. Nanomechanical mapping of first binding steps of a virus to animal cells. Nat. Nanotechnol., 2017, 12(2), 177-183.
[] [PMID: 27798607]
Schaap, I.A.T.; Eghiaian, F.; des Georges, A.; Veigel, C. Effect of envelope proteins on the mechanical properties of influenza virus. J. Biol. Chem., 2012, 287(49), 41078-41088.
[] [PMID: 23048030]
Kuznetsov, Y.G.; Daijogo, S.; Zhou, J.; Semler, B.L.; McPherson, A. Atomic force microscopy analysis of icosahedral virus RNA. J. Mol. Biol., 2005, 347(1), 41-52.
[] [PMID: 15733916]
Kasas, S.; Thomson, N.H.; Smith, B.L.; Hansma, H.G.; Zhu, X.; Guthold, M.; Bustamante, C.; Kool, E.T.; Kashlev, M.; Hansma, P.K. Escherichia coli RNA polymerase activity observed using atomic force microscopy. Biochemistry, 1997, 36(3), 461-468.
[] [PMID: 9012661]
Lyubchenko, Y.L.; Shlyakhtenko, L.S. Visualization of supercoiled DNA with atomic force microscopy in situ. Proc. Natl. Acad. Sci. USA, 1997, 94(2), 496-501.
[] [PMID: 9012812]
Suzuki, Y.; Higuchi, Y.; Hizume, K.; Yokokawa, M.; Yoshimura, S.H.; Yoshikawa, K.; Takeyasu, K. Molecular dynamics of DNA and nucleosomes in solution studied by fast-scanning atomic force microscopy. Ultramicroscopy, 2010, 110(6), 682-688.
[] [PMID: 20236766]
Alonso-Sarduy, L.; Roduit, C.; Dietler, G.; Kasas, S. Human topoisomerase II-DNA interaction study by using atomic force microscopy. FEBS Lett., 2011, 585(19), 3139-3145.
[] [PMID: 21907712]
Hansma, H.G.; Oroudjev, E.; Baudrey, S.; Jaeger, L. TectoRNA and ‘kissing-loop’ RNA: atomic force microscopy of self-assembling RNA structures. J. Microsc., 2003, 212(Pt 3), 273-279.
[] [PMID: 14629553]
Kidoaki, S.; Matsuda, T. Adhesion forces of the blood plasma proteins on self-assembled monolayer surfaces of alkanethiolates with different functional groups measured by an atomic force microscope. Langmuir, 1999, 15, 7639-7646.
Marchin, K.L.; Berrie, C.L. Conformational changes in the plasma protein fibrinogen upon adsorption to graphite and mica investigated by atomic force microscopy. Langmuir, 2003, 19(23), 9883-9888.
Zhmurov, A.; Brown, A.E.X.; Litvinov, R.I.; Dima, R.I.; Weisel, J.W.; Barsegov, V. Mechanism of fibrin(ogen) forced unfolding. Structure, 2011, 19(11), 1615-1624.
[] [PMID: 22078561]
Tsapikouni, T.S.; Missirlis, Y.F. pH and ionic strength effect on single fibrinogen molecule adsorption on mica studied with AFM. Colloids Surf. B Biointerfaces, 2007, 57(1), 89-96.
[] [PMID: 17337166]
Taatjes, D.J.; Quinn, A.S.; Jenny, R.J.; Hale, P.; Bovill, E.G.; McDonagh, J. Tertiary structure of the hepatic cell protein fibrinogen in fluid revealed by atomic force microscopy. Cell Biol. Int., 1997, 21(11), 715-726.
[] [PMID: 9768470]
Lim, B.B.; Lee, E.H.; Sotomayor, M.; Schulten, K. Molecular basis of fibrin clot elasticity. Structure, 2008, 16(3), 449-459.
[] [PMID: 18294856]
Chiti, F.; Dobson, C.M. Protein misfolding, amyloid formation, and human disease: a summary of progress over the last decade. Annu. Rev. Biochem., 2017, 86, 27-68.
[] [PMID: 28498720]
Ballard, C.; Gauthier, S.; Corbett, A.; Brayne, C.; Aarsland, D.; Jones, E. Alzheimer’s disease. Lancet, 2011, 377(9770), 1019-1031.
[] [PMID: 21371747]
Mastrangelo, I.A.; Ahmed, M.; Sato, T.; Liu, W.; Wang, C.; Hough, P.; Smith, S.O. High-resolution atomic force microscopy of soluble Abeta42 oligomers. J. Mol. Biol., 2006, 358(1), 106-119.
[] [PMID: 16499926]
Banerjee, S.; Sun, Z.; Hayden, E.Y.; Teplow, D.B.; Lyubchenko, Y.L. Nanoscale dynamics of amyloid β-42 oligomers as revealed by high-speed atomic force microscopy. ACS Nano, 2017, 11(12), 12202-12209.
[] [PMID: 29165985]
Blackley, H.K.L.; Sanders, G.H.W.; Davies, M.C.; Roberts, C.J.; Tendler, S.J.B.; Wilkinson, M.J. In-situ atomic force microscopy study of beta-amyloid fibrillization. J. Mol. Biol., 2000, 298(5), 833-840.
[] [PMID: 10801352]
Economou, N.J.; Giammona, M.J.; Do, T.D.; Zheng, X.; Teplow, D.B.; Buratto, S.K.; Bowers, M.T. Amyloid β-protein assembly and alzheimer’s disease: Dodecamers of aβ42, but not of aβ40, seed fibril Formation. J. Am. Chem. Soc., 2016, 138(6), 1772-1775.
[] [PMID: 26839237]
Watanabe-Nakayama, T.; Ono, K.; Itami, M.; Takahashi, R.; Teplow, D.B.; Yamada, M. High-speed atomic force microscopy reveals structural dynamics of amyloid β1-42 aggregates. Proc. Natl. Acad. Sci. USA, 2016, 113(21), 5835-5840.
[] [PMID: 27162352]
Legleiter, J.; Czilli, D.L.; Gitter, B.; DeMattos, R.B.; Holtzman, D.M.; Kowalewski, T. Effect of different anti-Abeta antibodies on Abeta fibrillogenesis as assessed by atomic force microscopy. J. Mol. Biol., 2004, 335(4), 997-1006.
[] [PMID: 14698294]
Downey, M.A.; Giammona, M.J.; Lang, C.A.; Buratto, S.K.; Singh, A.; Bowers, M.T. Inhibiting and remodeling toxic amyloid-beta oligomer formation using a computationally designed drug molecule that targets Alzheimer’s disease. J. Am. Soc. Mass Spectrom., 2019, 30(1), 85-93.
[] [PMID: 29713966]
Lee, B.Y.; Attwood, S.J.; Turnbull, S.; Leonenko, Z. Effect of varying concentrations of docosahexaenoic acid on amyloid beta (1-42) aggregation: an atomic force microscopy study. Molecules, 2018, 23, 1-14.
Yu, M.; Chen, X.; Liu, J.; Ma, Q.; Zhuo, Z.; Chen, H.; Zhou, L.; Yang, S.; Zheng, L.; Ning, C.; Xu, J.; Gao, T.; Hou, S.T. Gallic acid disruption of Aβ1-42 aggregation rescues cognitive decline of APP/PS1 double transgenic mouse. Neurobiol. Dis., 2019, 124, 67-80.
[] [PMID: 30447302]
Lees, A.J.; Hardy, J.; Revesz, T. Parkinson’s disease. Lancet, 2009, 373(9680), 2055-2066.
[] [PMID: 19524782]
Zhang, Y.; Hashemi, M.; Lv, Z.; Williams, B.; Popov, K.I.; Dokholyan, N.V.; Lyubchenko, Y.L. High-speed atomic force microscopy reveals structural dynamics of α-synuclein monomers and dimers. J. Chem. Phys., 2018, 148(12)123322
[] [PMID: 29604892]
Yu, J.; Malkova, S.; Lyubchenko, Y.L. alpha-Synuclein misfolding: single molecule AFM force spectroscopy study. J. Mol. Biol., 2008, 384(4), 992-1001.
[] [PMID: 18948117]
Sweers, K.K.M.; Segers-Nolten, I.M.J.; Bennink, M.L.; Subramaniam, V. Structural model for a -synuclein fibrils derived from high resolution imaging and nanomechanical studies using atomic force microscopy. Soft Matter, 2012, 8, 7215-7222.
Ruggeri, F.S.; Benedetti, F.; Knowles, T.P.J.; Lashuel, H.A.; Sekatskii, S.; Dietler, G. Identification and nanomechanical characterization of the fundamental single-strand protofilaments of amyloid α-synuclein fibrils. Proc. Natl. Acad. Sci. USA, 2018, 115(28), 7230-7235.
[] [PMID: 29941606]
Yu, J.; Warnke, J.; Lyubchenko, Y.L. Nanoprobing of α-synuclein misfolding and aggregation with atomic force microscopy. Nanomedicine (Lond.), 2011, 7(2), 146-152.
[] [PMID: 20817126]
Sweers, K.; van der Werf, K.; Bennink, M.; Subramaniam, V. Nanomechanical properties of α-synuclein amyloid fibrils: a comparative study by nanoindentation, harmonic force microscopy, and Peakforce QNM. Nanoscale Res. Lett., 2011, 6(1), 270.
[] [PMID: 21711775]
Westermark, P.; Andersson, A.; Westermark, G.T. Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. Physiol. Rev., 2011, 91(3), 795-826.
[] [PMID: 21742788]
Abedini, A.; Schmidt, A.M. Mechanisms of islet amyloidosis toxicity in type 2 diabetes. FEBS Lett., 2013, 587(8), 1119-1127.
[] [PMID: 23337872]
Green, J.D.; Goldsbury, C.; Kistler, J.; Cooper, G.J.; Aebi, U. Human amylin oligomer growth and fibril elongation define two distinct phases in amyloid formation. J. Biol. Chem., 2004, 279(13), 12206-12212.
[] [PMID: 14704152]
Zhang, S.; Andreasen, M.; Nielsen, J.T.; Liu, L.; Nielsen, E.H.; Song, J.; Ji, G.; Sun, F.; Skrydstrup, T.; Besenbacher, F.; Nielsen, N.C.; Otzen, D.E.; Dong, M. Coexistence of ribbon and helical fibrils originating from hIAPP(20-29) revealed by quantitative nanomechanical atomic force microscopy. Proc. Natl. Acad. Sci. USA, 2013, 110(8), 2798-2803.
[] [PMID: 23388629]
Gao, M.; Estel, K.; Seeliger, J.; Friedrich, R.P.; Dogan, S.; Wanker, E.E.; Winter, R.; Ebbinghaus, S. Modulation of human IAPP fibrillation: cosolutes, crowders and chaperones. Phys. Chem. Chem. Phys., 2015, 17(13), 8338-8348.
[] [PMID: 25406896]
Green, J.D.; Kreplak, L.; Goldsbury, C.; Li Blatter, X.; Stolz, M.; Cooper, G.S.; Seelig, A.; Kistler, J.; Aebi, U. Atomic force microscopy reveals defects within mica supported lipid bilayers induced by the amyloidogenic human amylin peptide. J. Mol. Biol., 2004, 342(3), 877-887.
[] [PMID: 15342243]
Hajiraissi, R.; Hanke, M.; Yang, Y.; Duderija, B.; Gonzalez Orive, A.; Grundmeier, G.; Keller, A. Adsorption and fibrillization of islet amyloid polypeptide at self-assembled monolayers studied by QCM-D, AFM and PM-IRRAS. Langmuir, 2018, 34(11), 3517-3524.
[] [PMID: 29489382]
de Waal, G.M.; Engelbrecht, L.; Davis, T.; de Villiers, W.J.S.; Kell, D.B.; Pretorius, E. correlative light-electron microscopy detects lipopolysaccharide and its association with fibrin fibres in parkinson’s disease, alzheimer’s Disease and Type 2 Diabetes Mellitus. Sci. Rep., 2018, 8(1), 16798.
[] [PMID: 30429533]
Pretorius, E.; Bester, J.; Page, M.J.; Kell, D.B. The potential of LPS-binding protein to reverse amyloid formation in plasma fibrin of individuals with alzheimer-type dementia. Front. Aging Neurosci., 2018, 10(257), 257.
[] [PMID: 30186156]
Pretorius, E.; Page, M.J.; Hendricks, L.; Nkosi, N.B.; Benson, S.R.; Kell, D.B. Both lipopolysaccharide and lipoteichoic acids potently induce anomalous fibrin amyloid formation: assessment with novel Amytracker™ stains. J. R. Soc. Interface, 2018, 15(139)20170941
[] [PMID: 29445039]
Pretorius, E.; Page, M.J.; Mbotwe, S.; Kell, D.B. Lipopolysaccharide-binding protein (LBP) can reverse the amyloid state of fibrin seen or induced in Parkinson’s disease. PLoS One, 2018, 13(3)e0192121
[] [PMID: 29494603]
Pretorius, E.; Mbotwe, S.; Kell, D.B. Lipopolysaccharide-binding protein (LBP) reverses the amyloid state of fibrin seen in plasma of type 2 diabetics with cardiovascular co-morbidities. Sci. Rep., 2017, 7(1), 9680.
[] [PMID: 28851981]
Pretorius, E.; Page, M.J.; Engelbrecht, L.; Ellis, G.C.; Kell, D.B. Substantial fibrin amyloidogenesis in type 2 diabetes assessed using amyloid-selective fluorescent stains. Cardiovasc. Diabetol., 2017, 16(1), 141.
[] [PMID: 29096623]
Pretorius, E.; Mbotwe, S.; Bester, J.; Robinson, C.J.; Kell, D.B. Acute induction of anomalous and amyloidogenic blood clotting by molecular amplification of highly substoichiometric levels of bacterial lipopolysaccharide. J. R. Soc. Interface, 2016, 13(122)20160539
[] [PMID: 27605168]
Randeria, S.N.; Thomson, G.J.A.; Nell, T.A.; Roberts, T.; Pretorius, E. Inflammatory cytokines in type 2 diabetes mellitus as facilitators of hypercoagulation and abnormal clot formation. Cardiovasc. Diabetol., 2019, 18(1), 72.
[] [PMID: 31164120]
Bester, J.; Pretorius, E. Effects of IL-1β, IL-6 and IL-8 on erythrocytes, platelets and clot viscoelasticity. Sci. Rep., 2016, 6, 32188.
[] [PMID: 27561337]
Page, M.J.; Bester, J.; Pretorius, E. The inflammatory effects of TNF-α and complement component 3 on coagulation. Sci. Rep., 2018, 8(1), 1812.
[] [PMID: 29379088]
Page, M.J.; Bester, J.; Pretorius, E. Interleukin-12 and its procoagulant effect on erythrocytes, platelets and fibrin(ogen): the lesser known side of inflammation. Br. J. Haematol., 2018, 180(1), 110-117.
[] [PMID: 29143311]
Bester, J.; Matshailwe, C.; Pretorius, E. Simultaneous presence of hypercoagulation and increased clot lysis time due to IL-1β, IL-6 and IL-8. Cytokine, 2018, 110, 237-242.
[] [PMID: 29396046]
Bester, J.; Buys, A.V.; Lipinski, B.; Kell, D.B.; Pretorius, E. High ferritin levels have major effects on the morphology of erythrocytes in Alzheimer’s disease. Front. Aging Neurosci., 2013, 5, 88.
[] [PMID: 24367334]
Burnouf, T.; Chou, M.L.; Goubran, H.; Cognasse, F.; Garraud, O.; Seghatchian, J. An overview of the role of microparticles/micro-vesicles in blood components: Are they clinically beneficial or harmful? Transfus. Apheresis Sci., 2015, 53(2), 137-145.
Leal, J.K.F.; Adjobo-Hermans, M.J.W.; Bosman, G.J.C.G.M. Red blood cell homeostasis: mechanisms and effects of microvesicle generation in health and disease. Front. Physiol., 2018, 9, 703-703.
[] [PMID: 29937736]
Pretorius, E.; Kell, D.B. Diagnostic morphology: biophysical indicators for iron-driven inflammatory diseases. Integr. Biol., 2014, 6(5), 486-510.
Pretorius, E.; Olumuyiwa-Akeredolu, O.O.; Mbotwe, S.; Bester, J. Erythrocytes and their role as health indicator: Using structure in a patient-orientated precision medicine approach. Blood Rev., 2016, 30(4), 263-274.
[] [PMID: 26878812]
Ghoshal, K.; Bhattacharyya, M. Overview of platelet physiology: its hemostatic and nonhemostatic role in disease pathogenesis. ScientificWorldJournal, 2014, 2014781857
[] [PMID: 24729754]
Smith, T.L.; Weyrich, A.S. Platelets as central mediators of systemic inflammatory responses. Thromb. Res., 2011, 127(5), 391-394.
[] [PMID: 21074247]
Strukova, S.M. Role of platelets and serine proteinases in coupling of blood coagulation and inflammation. Biochemistry (Mosc.), 2004, 69(10), 1067-1081.
[] [PMID: 15527406]
Kell, D.B.; Pretorius, E. The simultaneous occurrence of both hypercoagulability and hypofibrinolysis in blood and serum during systemic inflammation, and the roles of iron and fibrin(ogen). Integr. Biol., 2015, 7(1), 24-52.
[] [PMID: 25335120]
Levi, M.; van der Poll, T.; Büller, H.R. Bidirectional relation between inflammation and coagulation. Circulation, 2004, 109(22), 2698-2704.
[] [PMID: 15184294]
Witkowski, M.; Landmesser, U.; Rauch, U. Tissue factor as a link between inflammation and coagulation. Trends Cardiovasc. Med., 2016, 26(4), 297-303.
[] [PMID: 26877187]
Bester, J.; Soma, P.; Kell, D.B.; Pretorius, E. Viscoelastic and ultrastructural characteristics of whole blood and plasma in Alzheimer-type dementia, and the possible role of bacterial lipopolysaccharides (LPS). Oncotarget, 2015, 6(34), 35284-35303.
[] [PMID: 26462180]
Pretorius, E.; Bester, J.; Vermeulen, N.; Alummoottil, S.; Soma, P.; Buys, A.V.; Kell, D.B. Poorly controlled type 2 diabetes is accompanied by significant morphological and ultrastructural changes in both erythrocytes and in thrombin-generated fibrin: implications for diagnostics. Cardiovasc. Diabetol., 2015, 14(1), 30.
[] [PMID: 25848817]
Pretorius, L.; Thomson, G.J.A.; Adams, R.C.M.; Nell, T.A.; Laubscher, W.A.; Pretorius, E. Platelet activity and hypercoagulation in type 2 diabetes. Cardiovasc. Diabetol., 2018, 17(1), 141.
[] [PMID: 30388964]

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