Force-controlled manipulation of single cells: From AFM to FluidFM

Trends in Biotechnology

Volumn 32, Issue 7, 2014, Pages 381-388

  Guillaume Gentil, Orane ^a   Potthoff, Eva ^a   Ossola, Dario ^a   Franz, Clemens M ^b   Zambelli, Tomaso ^a   Vorholt, Julia A ^a  

^a ETH ZURICH   (Switzerland)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

Atomic force microscopy; Fluidic force microscopy; Single cell analysis; Single cell perturbation

Indexed keywords

ATOMIC FORCE MICROSCOPY; CELLS; CYTOLOGY; NANOCANTILEVERS;

FORCE MICROSCOPY; INDIVIDUAL CELLS; OPTICAL CONTROL; PRESSURE CONTROLLERS; PROOF OF CONCEPT; SINGLE CELLS; SINGLE-CELL LEVEL; SINGLECELL ANALYSIS;

MOLECULAR BIOLOGY;

ATOMIC FORCE MICROSCOPY; CELL ADHESION; CELL ISOLATION; CELL MANIPULATION; FLUIDIC FORCE MICROSCOPY; HUMAN; MICROFLUIDICS; MICROSCOPY; NANOPIPETTE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SINGLE CELL ANALYSIS; SPECTROSCOPY; CHEMISTRY; DEVICES; PARTICLE SIZE; PROCEDURES; ULTRASTRUCTURE;

NANOMATERIAL;

HUMANS; MICROFLUIDICS; MICROSCOPY, ATOMIC FORCE; NANOSTRUCTURES; PARTICLE SIZE; SINGLE-CELL ANALYSIS;

EID: 84903578209     PISSN: 01677799     EISSN: 18793096     Source Type: Journal    
DOI: 10.1016/j.tibtech.2014.04.008     Document Type: Review

References (93)

1. Binnig G., et al. Atomic force microscope. Phys. Rev. Lett. 1986, 56:930-933.
2. Binnig G., et al. Surface studies by scanning tunneling microscopy. Phys. Rev. Lett. 1982, 49:57-61.
3. Albrecht T.R., et al. Microfabrication of cantilever styli for the atomic force microscope. J. Vac. Sci. Technol. 1990, 8:3386-3396.
4. Meyer G., Amer N.M. Novel optical approach to atomic force microscopy. Appl. Phys. Lett. 1988, 53:1045-1047.
5. Baró A.M., Reifenberger R.G. Atomic Force Microscopy in Liquid: Biological Applications 2012, Wiley-VCH.
6. Johnson B.N., Mutharasan R. Biosensing using dynamic-mode cantilever sensors: a review. Biosens. Bioelect. 2012, 32:1-18.
7. Tamayo J., et al. Biosensors based on nanomechanical systems. Chem. Soc. Rev. 2013, 42:1287-1311.
8. Longo G., et al. Rapid detection of bacterial resistance to antibiotics using AFM cantilevers as nanomechanical sensors. Nat. Nano 2013, 8:522-526.
9. Meister A., et al. FluidFM: combining atomic force microscopy and nanofluidics in a universal liquid delivery system for single cell applications and beyond. Nano Lett. 2009, 9:2501-2507.
10. Putman C.A.J., et al. Atomic force microscope with integrated optical microscope for biological applications. Rev. Sci. Instrum. 1992, 63:1914-1917.
11. Ashkin A. Acceleration and trapping of particles by radiation pressure. Phys. Rev. Lett. 1970, 24:156-159.
12. Crick F.H.C., Hughes A.F.W. The physical properties of cytoplasm: a study by means of the magnetic particle method, part 1. Experimental. Exp. Cell Res. 1950, 1:37-80.
13. Smith S.B., et al. Direct mechanical measurements of the elasticity of single DNA-molecules by using magnetic beads. Science 1992, 258:1122-1126.
14. Dholakia K., Cizmar T. Shaping the future of manipulation. Nat. Photonics 2011, 5:335-342.
15. Difato F., et al. Cell signaling experiments driven by optical manipulation. Int. J. Mol. Sci. 2013, 14:8963-8984.
16. Gould S.A.C., et al. From atoms to integrated circuit chips, blood cells, and bacteria with the atomic force microscope. J. Vac. Sci. Technol. 1990, 8:369-373.
17. Haberle W., et al. Force microscopy on living cells. J. Vac. Sci. Technol. 1991, 9:1210-1213.
18. Butt H.J., et al. Imaging cells with the atomic force microscope. J. Struct. Biol. 1990, 105:54-61.
19. Ando T., et al. A high-speed atomic force microscope for studying biological macromolecules. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:12468-12472.
20. Ando T., et al. High-speed AFM for observing dynamic processes in liquid. Atomic Force Microscopy in Liquid 2012, 189-209. Wiley-VCH.
21. Suzuki Y., et al. High-speed atomic force microscopy combined with inverted optical microscopy for studying cellular events. Sci. Rep. 2013, 3:2131.
22. Fantner G.E., et al. Kinetics of antimicrobial peptide activity measured on individual bacterial cells using high-speed atomic force microscopy. Nat. Nanotechnol. 2010, 5:280-285.
23. Frisbie C.D., et al. Functional group imaging by chemical force microscopy. Science 1994, 265:2071-2074.
24. Ito T., et al. Chemical-force microscopy for materials characterization. Trends Anal. Chem. 2010, 29:225-233.
25. Dague E., et al. High-resolution cell surface dynamics of germinating Aspergillus fumigatus conidia. Biophys. J. 2008, 94:656-660.
26. Hansma P.K., et al. The scanning ion-conductance microscope. Science 1989, 243:641-643.
27. Novak P., et al. Nanoscale live-cell imaging using hopping probe ion conductance microscopy. Nat. Methods 2009, 6:279-281.
28. Muller D.J., et al. Force probing surfaces of living cells to molecular resolution. Nat. Chem. Biol. 2009, 5:383-390.
29. Helenius J., et al. Single-cell force spectroscopy. J. Cell Sci. 2008, 121:1785-1791.
30. Alsteens D., et al. Single-cell force spectroscopy of Als-mediated fungal adhesion. Anal. Methods 2013, 5:3657-3662.
31. Alsteens D., et al. Force-induced formation and propagation of adhesion nanodomains in living fungal cells. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:20744-20749.
32. Kang S., Elimelech M. Bioinspired single bacterial cell force spectroscopy. Langmuir 2009, 25:9656-9659.
33. Selhuber-Unkel C., et al. Cooperativity in adhesion cluster formation during initial cell adhesion. Biophys. J. 2008, 95:5424-5431.
34. Taubenberger A., et al. Revealing early steps of alpha(2)beta(1) integrin-mediated adhesion to collagen type I by using single-cell force spectroscopy. Mol. Biol. Cell 2007, 18:1634-1644.
35. Beaussart A., et al. Single-cell force spectroscopy of probiotic bacteria. Biophys. J. 2013, 104:1886-1892.
36. Thwala J.M., et al. Bacteria-polymeric membrane interactions: atomic force microscopy and XDLVO predictions. Langmuir 2013, 29:13773-13782.
37. Benoit M., et al. Discrete interactions in cell adhesion measured by single-molecule force spectroscopy. Nat. Cell Biol. 2000, 2:313-317.
38. Canale C., et al. A new quantitative experimental approach to investigate single cell adhesion on multifunctional substrates. Biosens. Bioelectron. 2013, 48:172-179.
39. Panorchan P., et al. Single-molecule analysis of cadherin-mediated cell-cell adhesion. J. Cell Sci. 2006, 119:66-74.
40. Dobrowsky T.M., et al. Live-cell single-molecule force spectroscopy. Methods Cell Biol. 2008, 89:411-432.
41. Friedrichs J., et al. Stimulated single-cell force spectroscopy to quantify cell adhesion receptor crosstalk. Proteomics 2010, 10:1455-1462.
42. Xie H., et al. In situ quantification of living cell adhesion forces: single cell force spectroscopy with a nanotweezer. Langmuir 2014, 30:2952-2959.
43. Lin D.C., Horkay F. Nanomechanics of polymer gels and biological tissues: A critical review of analytical approaches in the Hertzian regime and beyond. Soft Matter 2008, 4:669-682.
44. Hoh J.H., Schoenenberger C.A. Surface morphology and mechanical properties of MDCK monolayers by atomic force microscopy. J. Cell Sci. 1994, 107:1105-1114.
45. Dufrene Y.F., Pelling A.E. Force nanoscopy of cell mechanics and cell adhesion. Nanoscale 2013, 5:4094-4104.
46. Kasas S., et al. Mechanical properties of biological specimens explored by atomic force microscopy. J. Phys. D: Appl. Phys. 2013, 46:133001.
47. Radmacher M., et al. Measuring the viscoelastic properties of human platelets with the atomic force microscope. Biophys. J. 1996, 70:556-567.
48. Longo G., et al. Force volume and stiffness tomography investigation on the dynamics of stiff material under bacterial membranes. J. Mol. Recognit. 2012, 25:278-284.
49. Longo G., et al. Antibiotic-induced modifications of the stiffness of bacterial membranes. J. Microbiol. Methods 2013, 93:80-84.
50. Cross S.E., et al. Nanomechanical analysis of cells from cancer patients. Nat. Nanotechnol. 2007, 2:780-783.
51. Plodinec M., et al. The nanomechanical signature of breast cancer. Nat. Nanotechnol. 2012, 7:757-765.
52. Stewart M.P., et al. Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 2011, 469:226-230.
53. Raman A., et al. Mapping nanomechanical properties of live cells using multi-harmonic atomic force microscopy. Nat. Nanotechnol. 2011, 6:809-814.
54. Osada T., et al. mRNA analysis of single living cells. J. Nanobiotechnology 2003, 1:2.
55. Nawarathna D., et al. Selective probing of mRNA expression levels within a living cell. Appl. Phys. Lett. 2009, 95:083117.
56. Nawarathna D., et al. Targeted messenger RNA profiling of transfected breast cancer gene in a living cell. Anal. Biochem. 2011, 408:342-344.
57. Cuerrier C.M., et al. Single cell transfection using plasmid decorated AFM probes. Biochem. Biophys. Res. Commun. 2007, 355:632-636.
58. Yum K., et al. Nanoneedle: a multifunctional tool for biological studies in living cells. Nanoscale 2010, 2:363-372.
59. Han S.W., et al. Gene expression using an ultrathin needle enabling accurate displacement and low invasiveness. Biochem. Biophys. Res. Commun. 2005, 332:633-639.
60. Han S.W., et al. High-efficiency DNA injection into a single human mesenchymal stem cell using a nanoneedle and atomic force microscopy. Nanomedicine 2008, 4:215-225.
61. Chen X., et al. A cell nanoinjector based on carbon nanotubes. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:8218-8222.
62. Suo Z., et al. Bacteria survive multiple puncturings of their cell walls. Langmuir 2009, 25:4588-4594.
63. Guillaume-Gentil O., et al. Isolation of single mammalian cells from adherent cultures by fluidic force microscopy. Lab Chip 2014, 14:402-414.
64. Stiefel P., et al. Cooperative Vaccinia infection demonstrated at the single-cell level using FluidFM. Nano Lett. 2012, 12:4219-4227.
65. Dörig P., et al. Force-controlled spatial manipulation of viable mammalian cells and micro-organisms by means of FluidFM technology. Appl. Phys. Lett. 2010, 97:023701.
66. Stiefel P., et al. Isolation of optically targeted single bacteria using FluidFM applied to aerobic anoxygenic phototrophs from the phyllosphere. Appl. Environ. Microbiol. 2013, 79:4895-4905.
67. Dörig P., et al. Exchangeable colloidal AFM probes for the quantification of irreversible and long-term interactions. Biophys. J. 2013, 105:463-472.
68. Ducker W.A., et al. Direct measurement of colloidal forces using an atomic force microscope. Nature 1991, 353:239-241.
69. Butt H.J. Measuring electrostatic, Vanderwaals, and hydration forces in electrolyte-solutions with an atomic force microscope. Biophys. J. 1991, 60:1438-1444.
70. Potthoff E., et al. Rapid and serial quantification of adhesion forces of yeast and mammalian cells. PLoS ONE 2012, 7:e52712.
71. Potthoff E., et al. Toward a rational design of surface textures promoting endothelialization. Nano Lett. 2014, 14:1069-1079.
72. Guillaume-Gentil O., et al. Force-controlled fluidic injection into single cell nuclei. Small 2013, 9:1904-1907.
73. Meister A., et al. Nanodispenser for attoliter volume deposition using atomic force microscopy probes modified by focused-ion-beam milling. Appl. Phys. Lett. 2004, 85:6260-6262.
74. Deladi S., et al. Micromachined fountain pen for atomic force microscope-based nanopatterning. Appl. Phys. Lett. 2004, 85:5361-5363.
75. Kim K.H., et al. A nanofountain probe with sub-100-nm molecular writing resolution. Small 2005, 1:632-635.
76. Hug T.S., et al. Generic fabrication technology for transparent and suspended microfluidic and nanofluidic channels. TRANSDUCERS'05. The 13th Int. Conf. on Solid-State Sensors, Actuators and Microsystems, 2005. Digest of Technical Papers 2005, Vol. 2:1191-1194. IEEE.
77. Meister A., et al. Hollow atomic force microscopy probes for nanoscale dispensing of liquids. NSTI-Nanotech 2008 2008, 3:273-276.
78. Kato N., et al. Micromachining of a newly designed AFM probe integrated with hollow microneedle for cellular function analysis. Microelectron. Eng. 2010, 87:1185-1189.
79. Loh O., et al. Nanofountain-probe-based high-resolution patterning and single-cell injection of functionalized nanodiamonds. Small 2009, 5:1667-1674.
80. Shibata T., et al. Fabrication and characterization of bioprobe integrated with a hollow nanoneedle for novel AFM applications in cellular function analysis. Microelectron. Eng. 2013, 111:325-331.
81. Kang W., et al. Nanofountain probe electroporation (NFP-E) of single cells. Nano Lett. 2013, 13:2448-2457.
82. Proksch R., et al. Imaging the internal and external pore structure of membranes in fluid: TappingMode scanning ion conductance microscopy. Biophys. J. 1996, 71:2155-2157.
83. Lewis A., et al. Fountain pen nanochemistry: atomic force control of chrome etching. Appl. Phys. Lett. 1999, 75:2689-2691.
84. Bruckbauer A., et al. Writing with DNA and protein using a nanopipet for controlled delivery. J. Am. Chem. Soc. 2002, 124:8810-8811.
85. Seger R.A., et al. Voltage controlled nano-injection system for single-cell surgery. Nanoscale 2012, 4:5843-5846.
86. Actis P., et al. Compartmental genomics in living cells revealed by single-cell nanobiopsy. ACS Nano 2013, 8:546-553.
87. Singhal R., et al. Multifunctional carbon-nanotube cellular endoscopes. Nat. Nanotechnol. 2011, 6:57-64.
88. Ainla A., et al. Hydrodynamic flow confinement technology in microfluidic perfusion devices. Micromachines 2012, 3:442-461.
89. Sarkar A., et al. Microfluidic probe for single-cell analysis in adherent tissue culture. Nat. Commun. 2014, 5:3421.
90. Kaigala G.V., et al. A vertical microfluidic probe. Langmuir 2011, 27:5686-5693.
91. Lovchik R.D., et al. Micro-immunohistochemistry using a microfluidic probe. Lab Chip 2012, 12:1040-1043.
92. Berenschot E.J.W., et al. 3D nanofabrication of fluidic components by corner lithography. Small 2012, 8:3702.
93. Ghatkesar M.K., et al. Hollow AFM cantilever pipette. Microelectron. Eng. 2014, 124:22-25.