Potential role of atomic force microscopy in systems biology

Wiley Interdisciplinary Reviews: Systems Biology and Medicine

Volumn 3, Issue 6, 2011, Pages 702-716

  Ramachandran, Srinivasan ^a,b   Teran Arce, Fernando ^a,b   Lal, Ratnesh ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PLASMA PROTEIN; PROTEOME;

ATOMIC FORCE MICROSCOPY; GENOME; HUMAN; HUMAN GENOME; METABOLISM; REVIEW; SYSTEMS BIOLOGY;

BLOOD PROTEINS; GENOME; GENOME, HUMAN; HUMANS; MICROSCOPY, ATOMIC FORCE; PROTEOME; SYSTEMS BIOLOGY;

EID: 80053469055     PISSN: 19395094     EISSN: 1939005X     Source Type: Journal    
DOI: 10.1002/wsbm.154     Document Type: Review

References (105)

1. Ideker T, Galitski T, Hood L. A new approach to decoding life: systems biology. Ann Rev Genom Hum Genet 2001, 2:343-372.
2. Archakov AI, Ivanov YD, Lisitsa AV, Zgoda VG. AFM fishing nanotechnology is the way to reverse the Avogadro number in proteomics. Proteomics 2007, 7:4-9.
3. Binnig G, Rohrer H. Scanning tunneling microscopy. Helvet Phys Acta 1982, 55:726-735.
4. Binnig G, Rohrer H. Scanning tunneling microscopy-from birth to adolescence (Nobel Lecture). Available at: (Accessed June 13, 2011).
5. Binnig G, Rohrer H. The scanning tunneling microscope. Sci Am 1985, 253:50.
6. Binnig G, Quate CF, Gerber C. Atomic force microscope. Phys Rev Lett 1986, 56:930-933.
7. Giessibl FJ. Atomic-resolution of the silicon (1 1 1)-(7 × 7) surface by atomic-force microscopy. Science 1995, 267:68-71.
8. Giessibl FJ, Hembacher S, Bielefeldt H, Mannhart J. Subatomic features on the silicon (1 1 1)-(7×7) surface observed by atomic force microscopy. Science 2000, 289:422-425.
9. Giessibl FJ. Advances in atomic force microscopy. Rev Mod Phys 2003, 75:949-983.
10. Kasas S, Dietler G. Probing nanomechanical properties from biomolecules to living cells. Pflugers Arch-Eur J Physiol 2008, 456:13-27.
11. Weihs TP, Nawaz Z, Jarvis SP, Pethica JB. Limits of imaging resolution for atomic force microscopy of molecules. Appl Phys Lett 1991, 59:3536-3538.
12. Hoh JH, Lal R, John SA, Revel JP, Arnsdorf MF. Atomic force microscopy and dissection of gap-junctions. Science 1991, 253:1405-1408.
13. Hoh JH, Sosinsky GE, Revel JP, Hansma PK. Structure of the extracellular surface of the gap junction by atomic-force microscopy. Biophys J 1993, 65:149-163.
14. Muller DJ, Fotiadis D, Scheuring S, Muller SA, Engel A. Electrostatically balanced subnanometer imaging of biological specimens by atomic force microscope. Biophys J 1999, 76:1101-1111.
15. Quist A, Doudevski L, Lin H, Azimova R, Ng D, Frangione B, Kagan B, Ghiso J, Lal R. Amyloid ion channels: a common structural link for protein-misfolding disease. Proc Natl Acad Sci U S A 2005, 102:10427-10432.
16. Thimm J, Mechler A, Lin H, Rhee S, Lal R. Calcium-dependent open/closed conformations and interfacial energy maps of reconstituted hemichannels. J Biol Chem 2005, 280:10646-10654.
17. Cappella B, Dietler G. Force-distance curves by atomic force microscopy. Surf Sci Rep 1999, 34:1.
18. Butt HJ, Cappella B, Kappl M. Force measurements with the atomic force microscope: technique, interpretation and applications. Surf Sci Rep 2005, 59:1-152.
19. Drake B, Prater CB, Weisenhorn AL, Gould SAC, Albrecht TR, Quate CF, Cannell DS, Hansma HG, Hansma PK. Imaging crystals, polymers, and processes in water with the atomic force microscope. Science 1989, 243:1586-1589.
20. Barrena E, Kopta S, Ogletree DF, Charych DH, Salmeron M. Relationship between friction and molecular structure: alkylsilane lubricant films under pressure. Phys Rev Lett 1999, 82:2880-2883.
21. Carpick RW, Salmeron M. Scratching the surface: fundamental investigations of tribology with atomic force microscopy. Chem Rev 1997, 97:1163-1194.
22. Hansma PK, Cleveland JP, Radmacher M, Walters DA, Hillner PE, Bezanilla M, Fritz M, Vie D, Hansma HG, Prater CB, et al. Tapping mode atomic-force microscopy in liquids. Appl Phys Lett 1994, 64:1738-1740.
23. Bustamante C, Vesenka J, Tang CL, Rees W, Guthold M, Keller R. Circular DNA-molecules imaged in air by scanning force microscopy. Biochem 1992, 31:22-26.
24. Lindsay SM, Nagahara LA, Thundat T, Knipping U, Rill RL, Drake B, Prater CB, Weisenhorn AL, Gould SAC, Hansma PK. Stm and Afm images of nucleosome DNA under water. J Biomol Struct Dyn 1989, 7:279-287.
25. Lyubchenko YL, Jacobs BL, Lindsay SM. Atomic force microscopy of reovirus Dsrna-a routine technique for length measurements. Nucleic Acids Res 1992, 20:3983-3986.
26. Vesenka J, Guthold M, Tang CL, Keller D, Delaine E, Bustamante C. Substrate preparation for reliable imaging of DNA-molecules with the scanning force microscope. Ultramicroscopy 1992, 42:1243-1249.
27. Arce FT, Carlson R, Monds J, Veeh R, Hu FZ, Stewart PS, Lal R, Ehrlich GD, Avci R. Nanoscale structural and mechanical properties of nontypeable haemophilus influenzae biofilms. J Bacteriol 2009, 191:2512-2520.
28. Arce FT, Whitlock JL, Birukova AA, Birukov KG, Arnsdorf MF, Lal R, Garcia JGN, Dudek SM. Regulation of the micromechanical properties of pulmonary endothelium by S1P and thrombin: role of cortactin. Biophys J 2008, 95:886-894.
29. Almqvist N, Bhatia R, Primbs G, Desai N, Banerjee S, Lal R. Elasticity and adhesion force mapping reveals real-time clustering of growth factor receptors and associated changes in local cellular rheological properties. Biophys J 2004, 86:1753-1762.
30. Jang H, Arce FT, Mustata M, Ramachandran S, Capone R, Nussinov R, Lal R. Antimicrobial Protegrin-1 forms amyloid-like fibrils with rapid kinetics suggesting a functional link. Biophys J 2011, 100:1775-1783.
31. Kellermayer MSZ, Karsai A, Benke M, Soos K, Penke B. Stepwise dynamics of epitaxially growing single amyloid fibrils. Proc Natl Acad Sci U S A 2008, 105:141-144.
32. Fantner GE, BR J, GD S, Belcher AM. Kinetics of antimicrobial peptide activity measured on individual bacterial cells using high-speed atomic force microscopy. Nat Nanotechnol 2010, 5:280-285.
33. Hansma PK, Schitter G, Fantner GE, Prater C. High-speed atomic force microscopy. Science 2006, 314:601-602.
34. Ando T, Kodera N, Takai E, Maruyama D, Saito K, Toda A. A high-speed atomic force microscope for studying biological macromolecules. Proc Natl Acad Sci U S A 2001, 98:12468-12472.
35. Humphris ADL, Miles MJ, Hobbs JK. A mechanical microscope: high-speed atomic force microscopy. Appl Phy Lett 2005, 86:034106-1-034106-3.
36. Giannotti MI, Vancso GJ. Interrogation of single synthetic polymer chains and polysaccharides by AFM-based force spectroscopy. Chemphyschem 2007, 8:2290-2307.
37. Marszalek PE, Li HB, Fernandez JM. Fingerprinting polysaccharides with single-molecule atomic force microscopy. Nat Biotechnol 2001, 19:258-262.
38. Hinterdorfer P, Baumgartner W, Gruber HJ, Schilcher K, Schindler H. Detection and localization of individual antibody-antigen recognition events by atomic force microscopy. Proc Natl Acad Sci U S A 1996, 93:3477-3481.
39. Zhong Q, Inniss D, Kjoller K, Elings VB. Fractured polymer silica fiber surface studied by tapping mode atomic-force microscopy. Surf Sci 1993, 290:L688-L692.
40. Stark M, Bercu BN, Marchi F, Chevrier J, Huant S. Marking the difference: interferometric detection vs optical beam deflection in AFM. AIP Conference Proceedings, Eindhoven, The Netherlands: American Institute of Physics; 2003.
41. Putman CAJ, Vanderwerf KO, Degrooth BG, Vanhulst NF, Greve J. Tapping mode atomic-force microscopy in liquid. Appl Phys Lett 1994, 64: 2454-2456.
42. Bezanilla M, Drake B, Nudler E, Kashlev M, Hansma PK, Hansma HG. Motion and enzymatic degradation of DNA in the atomic-force microscope. Biophys J 1994, 67:2454-2459.
43. Lal R, John SA. Biological applications of atomic-force microscopy. Am J Physiol 1994, 266:C1.
44. Liu F, Arce FT, Ramachandran S, Lal R. Nanomechanics of hemichannel conformations-connexin flexibility underlying channel opening and closing. J Biol Chem 2006, 281:23207-23217.
45. Marszalek PE, Lu H, Li HB, Carrion-Vazquez M, Oberhauser AF, Schulten K, Fernandez JM. Mechanical unfolding intermediates in titin modules. Nature 1999, 402:100-103.
46. Marszalek PE, Oberhauser AF, Pang YP, Fernandez JM. Polysaccharide elasticity governed by chair-boat transitions of the glucopyranose ring. Nature 1998, 396:661-664.
47. Lin H, Bhatia R, Lal R. Amyloid ß protein forms ion channels: implications for Alzheimer's disease pathophysiology. The FASEB J 2001, 15:2433-2444.
48. Lal R, Proksch R. Multimodal atomic force microscopy: biological imaging using atomic force microscopy combined with light fluorescence and confocal microscopies and electrophysiologic recording. Int J Imag Syst Tech 1997, 8:293-300.
49. Hansma PK, Drake B, Grigg D, Prater CB, Yashar F, Gurley G, Eling SV, Feinstein S, Lal R. A new, optical-lever based atomic-force microscope. J Appl Phys 1994, 76:796-799.
50. Quist AP, Chand A, Ramachandran S, Daraio C, Jin S, Lal R. Atomic force microscopy imaging and electrical recording of lipid bilayers supported over microfabricated silicon chip nanopores: lab-on-a-chip system for lipid membranes and ion channels. Langmuir 2007, 23:1375-1380.
51. Hansma HG, Vesenka J, Siegerist C, Kelderman G, Morrett H, Sinsheimer RL, Elings V, Bustamante C, Hansma PK. Reproducible imaging and dissection of plasmid DNA under liquid with the atomic force microscope. Science 1992, 256:1180-1184.
52. Weisenhorn AL, Maivald P, Butt HJ, Hansma PK. Measuring adhesion, attraction, and repulsion between surfaces in liquids with an atomic-force microscope. Phys Rev B 1992, 45:11226-11232.
53. Allison DP, Bottomley LA, Thundat T, Brown GM, Woychik RP, Schrick JJ, Jacobson KB, Warmack RJ. Immobilization of DNA for scanning probe microscopy. Proc Natl Acad Sci U S A 1992, 89: 10129-10133.
54. Hansma HG, Bezanilla M, Zenhausern F, Adrian M, Sinsheimer RL. Atomic force microscopy of DNA in aqueous-solutions. Nucleic Acids Res 1993, 21:505-512.
55. Lyubchenko YL, Gall AA, Shlyakhtenko LS, Harrington RE, Jacobs BL, Oden PI, Lindsay SM. Atomic force microscopy imaging of double-stranded DNA and RNA. J Biomol Struct Dyn 1992, 10:589-606.
56. Hegner M, Wagner P, Semenza G. Immobilizing DNA on gold via thiol modification for atomic-force microscopy imaging in buffer solutions. FEBS Lett 1993, 336:452-456.
57. Hansma HG, Laney DE, Bezanilla M, Sinsheimer RL, Hansma PK. Applications for atomic-force microscopy of DNA. Biophys J 1995, 68:1672-1677.
58. Rees WA, Keller RW, Vesenka JP, Yang GL, Bustamante C. Evidence of DNA bending in transcription complexes imaged by scanning force microscopy. Science 1993, 260:1646-1649.
59. Pietrasanta LI, Schaper A, Jovin TM. Probing specific molecular-conformations with the scanning force microscope-complexes of plasmid DNA and Anti-Z-DNA antibodies. Nucleic Acids Res 1994, 22:3288-3292.
60. Wyman C, Grotkopp E, Bustamante C, Nelson HCM. Determination of heat-shock transcription factor-2 stoichiometry at looped DNA complexes using scanning force microscopy. Embo J 1995, 14:117-123.
61. van Noort SJT, van der Werf KO, Eker APM, Wyman C, de Grooth BG, van Hulst NF, Greve J. Direct visualization of dynamic protein-DNA interactions with a dedicated atomic force microscope. Biophys J 1998, 74:2840-2849.
62. Lindsay SM, Philipp M. Can the scanning tunneling microscope sequence DNA. Genet Anal-Biomol Eng 1991, 8:8-13.
63. Hansma HG, Weisenhorn AL, Gould SAC, Sinsheimer RL, Gaub HE, Stucky GD, Zaremba CM, Hansma PK. Progress in sequencing deoxyribonucleic-acid with an atomic force microscope. J Vac Sci Technol B 1991, 9:1282-1284.
64. Nygaard V, Holden M, Loland A, Langaas M, Myklebost O, Hovig E. Limitations of mRNA amplification from small-size cell samples. BMC Genom 2005, 6:147. doi:10.1186/1471-2164-6-147.
65. Nygaard V, Loland A, Holden M, Langaas M, Rue H, Liu F, Myklebost O, Fodstad O, Hovig E, Smith-Sorensen B. Effects of mRNA amplification on gene expression ratios in cDNA experiments estimated by analysis of variance. BMC Genom 2003, 4:11. doi:10.1186/1471-2164-4-11.
66. Nguyen DC, Keller RA, Jett JH, Martin JC. Detection of single molecules of phycoerythrin in hydrodynamically focused flows by laser-induced fluorescence. Anal Chem 1987, 59:2158-2161.
67. Jett JH, Keller RA, Martin JC, Marrone BL, Moyzis RK, Ratliff RL, Seitzinger NK, Shera EB, Stewart CC. High-speed DNA sequencing-an approach based upon fluorescence detection of single molecules. J Biomol Struct Dyn 1989, 7:301-309.
68. Treffer R, Deckert V. Recent advances in single-molecule sequencing. Curr Opin Biotechnol 2010, 21:4-11.
69. Rosenthal A, Brenner S. DNA Sequencing Method. 2000; 4.
70. Allison DP, Kerper PS, Doktycz MJ, Spain JA, Modrich P, Larimer FW, Thundat T, Warmack RJ. Direct atomic force microscope imaging of EcoRI endonuclease site specifically bound to plasmid DNA molecules. Proc Natl Acad Sci U S A 1996, 93:8826-8829.
71. Allison DP, Kerper PS, Doktycz MJ, Thundat T, Modrich P, Larimer FW, Johnson DK, Hoyt PR, Mucenski ML, Warmack RJ. Mapping individual cosmid DNAs by direct AFM imaging. Genomics 1997, 41:379-384.
72. Nakamura T, Maeda Y, Oka T, Tabata H, Futai M, Kawai T. Atomic force microscope observation of plasmid deoxyribose nucleic acid with restriction enzyme. J Vac Sci Technol B 1999, 17:288-293.
73. Reed J, Mishra B, Pittenger B, Magonov S, Troke J, Teitell MA, Gimzewski JK. Single molecule transcription profiling with AFM. Nanotechnology 2007, 18: 044032.
74. Sommer SS, Cohen JE. The size distributions of proteins, messenger-RNA and nuclear-RNA. J Mol Evol 1980, 15:37-57.
75. Hames BD. In: Lewin B, ed. Gene Expression 2, Eukaryotic Chromosomes, 2nd ed. Chichester: John Wiley & Sons; 1980, 1160. ISBN:0-471-01977-1; Biochem Ed 1982, 10:158.
76. Ramachandran S, Quist AP, Kumar S, Lal R. Cisplatin nanoliposomes for cancer therapy: AFM and fluorescence Imaging of cisplatin encapsulation, stability, cellular uptake, and toxicity. Langmuir 2006, 22:8156-8162.
77. Bailo E, Deckert V. Tip-enhanced Raman spectroscopy of single RNA strands: towards a novel direct-sequencing method. Angew Chem Int Ed 2008, 47:1658-1661.
78. Schafer AJ, Hawkins JR. DNA variation and the future of human genetics. Nat Biotechnol 1998, 16:33-39.
79. Clausen-Schaumann H, Seitz M, Krautbauer R, Gaub HE. Force spectroscopy with single bio-molecules. Curr Opin Chem Biol 2000, 4:524-530.
80. Hinterdorfer P, Dufrene YF. Detection and localization of single molecular recognition events using atomic force microscopy. Nat Methods 2006, 3:347-355.
81. Fritz J, Baller MK, Lang HP, Rothuizen H, Vettiger P, Meyer E, Guntherodt HJ, Gerber C, Gimzewski JK. Translating biomolecular recognition into nanomechanics. Science 2000, 288:316-318.
82. Hansen KM, Ji HF, Wu GH, Datar R, Cote R, Majumdar A, Thundat T. Cantilever-based optical deflection assay for discrimination of DNA single-nucleotide mismatches. Anal Chem 2001, 73: 1567-1571.
83. Stowe TD, Yasumura K, Kenny TW, Botkin D, Wago K, Rugar D. Attonewton force detection using ultrathin silicon cantilevers. Appl Phys Lett 1997, 71:288-290.
84. Cox J, Mann M. Is proteomics the new genomics? Cell 2007, 130:395-398.
85. Abadal G, Davis ZJ, Helbo B, Borrise X, Ruiz R, Boisen A, Campabadal F, Esteve J, Figueras E, Perez-Murano F, et al. Electromechanical model of a resonating nano-cantilever-based sensor for high-resolution and high-sensitivity mass detection. Nanotechnology 2001, 12:100-104.
86. Davis ZJ, Abadal G, Kuhn O, Hansen O, Grey F, Boisen A. Fabrication and characterization of nanoresonating devices for mass detection. J Vac Sci Technol B 2000, 18:612-616.
87. Dugdale TM, Dagastine R, Chiovitti A, Mulvaney P, Wetherbee R. Single adhesive nanofibers from a live diatom have the signature fingerprint of modular proteins. Biophys J 2005, 89:4252-4260.
88. Fernandez JM. Fingerprinting single molecules in vivo. Biophys J 2005, 89:3676-3677.
89. Avci R, Schweitzer MH, Boyd RD, Wittmeyer JL, Arce FT, Calvo JO. Preservation of bone collagen from the late cretaceous period studied by immunological techniques and atomic force microscopy. Langmuir 2005, 21:3584-3590.
90. Schweitzer MH, Suo Z, Avci R, Asara JM, Allen MA, Arce FT, Horner JR. Analyses of soft tissue from Tyrannosaurus rex suggest the presence of protein. Science 2007, 316:277-280.
91. Kasas S, Thomson NH, Smith BL, Hansma PK, Miklossy J, Hansma HG. Biological applications of the AFM: from single molecules to organs. Int J Imaging Syst Technol 1997, 8:151-161.
92. Parot P, Dufrene YF, Hinterdorfer P, Le Grimellee C, Navajas D, Pellequer JL, Scheuring S. Past, present and future of atomic force microscopy in life sciences and medicine. J Mol Recognit 2007, 20:418-431.
93. Muller DJ, Hand GM, Engel A, Sosinsky GE. Conformational changes in surface structures of isolated connexin 26 gap junctions. Embo J 2002, 21:3598-3607.
94. Bahatyrova S, Frese RN, Siebert CA, Olsen JD, van der Werf KO, van Grondelle R, Niederman RA, Bullough PA, Otto C, Hunter CN. The native architecture of a photosynthetic membrane. Nature 2004, 430:1058-1062.
95. Frederix PLTM, Bosshart PD, Engel A. Atomic force microscopy of biological membranes. Biophys J 2009, 96:329-338.
96. Jang H, Arce FT, Ramachandran S, Capone R, Azimova R, Kagan BL, Nussinov R, Lal R. Truncated β-amyloid peptide channels provide an alternative mechanism for Alzheimer's Disease and Down syndrome. Proc Natl Acad Sci U S A 2010, 107:6538-6543.
97. Mustata M, Capone R, Jang H, Arce FT, Ramachandran S, Lal R, Nussinov R. K3 fragment of amyloidogenic β(2)-microglobulin forms ion channels: implication for dialysis related amyloidosis. J Am Chem Soc 2009, 131:14938-14945.
98. Lin H, Clegg DO, Lal R. Imaging real-time proteolysis of single collagen I molecules with an atomic force microscope. Biochem 1999, 38:9956-9963.
99. Barbee KA, Davies PF, Lal R. Shear stress-induced reorganization of the surface-topography of living endothelial-cells imaged by atomic-force microscopy. Circ Res 1994, 74:163-171.
100. Lin H, Lal R, Clegg DO. Imaging and mapping heparin-binding sites on single fibronectin molecules with atomic force microscopy. Biochem 2000, 39:3192-3196.
101. Vergara D, Martignago R, Leporatti S, Bonsegna S, Maruccio G, De Nuccio F, Santino A, Cingolani R, Nicolardi G, Maffia M, et al. Biomechanical and proteomic analysis of INF-β-treated astrocytes. Nanotechnology 2009, 20.
102. Ramachandran S, Lal R. Scope of atomic force microscopy in the advancement of nanomedicine. Ind J Exp Biol 2010, 48:1020-1036.
103. Lal R, Ramachandran S, Arnsdorf M. Multidimensional atomic force microscopy: a versatile novel technology for nanopharmacology research. AAPS J 2010, 12:716-728.
104. Davies PF, Barbee KA, Lal R, Robotewskyj A, Griem ML. Hemodynamics and atherogenesis-endothelial surface dynamics in flow signal-transduction. Atherosclerosis Iii: Recent Adv Atherosclerosis Res 1995, 748:86-103.
105. Barbee KA, Mundel T, Lal R, Davies PF. Altered subcellular shear-stress distribution by the flow-realignment response of endothelial-cells. Faseb J 1995, 9:A588.