Abstract

The Scanning Near-field Optical Microscope (SNOM) is able to detect tiny vertical movement on the cell membrane in the range of only 1 nanometer or less, about 3 orders of magnitude better than conventional optical microscopes. Here we show intriguing data of cell membrane nanometer-scale dynamics associated to different phenomena of the cell’s life, such as cell cycle and cell death, on rat pheochromocytoma line PC12. Working in culture medium with alive and unperturbed samples, we could detect nanometer-sized movements; Fourier components revealed a clear distinct behavior associated to regulation of neurite outgrowth and changes on morphology after necrotic stimulus.

© 2007 Optical Society of America

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    [CrossRef] [PubMed]
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    [CrossRef]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]

2005

R. Piga, R. Micheletto, and Y. Kawakami, "Nano-probing of the membrane dynamics of rat pheochromocytoma by near-field optics," Biophys. Chem. 117, 141-146 (2005).
[CrossRef] [PubMed]

2004

A. E. Pelling, S. Sehati, E. B. Gralla, J. S. Valentine, and J. K. Gimzewski, "Local nanomechanical motion of the cell wall of Saccharomyces cerevisiae," Science 305, 1147-1150 (2004).
[CrossRef] [PubMed]

2002

J. W. Crabb, M. Miyagi, X. Gu, K. Shadrach, K. A. West, H. Sakaguchi, M. Kamei, A. Hasan, L. Yan, M. E. Rayborn, R. G. Salomon, and J. G. Hollyfield, "Drusen proteome analysis: an approach to the etiology of age-related macular degeneration," Proc. Natl. Acad. Sci. U S A 99, 14682-14687 (2002).
[CrossRef] [PubMed]

2001

D. Jiang, N. Jha, R. Boonplueang, and J. K. Andersen, "Caspase 3 inhibition attenuates hydrogen peroxide-induced DNA fragmentation but not cell death in neuronal PC12 cells," J. Neurochem. 76, 1745-1755 (2001).
[CrossRef] [PubMed]

2000

P. Papageorgiou, A. Katsambas, and A. Chu, "Phototherapy with blue (415 nm) and red (660 nm) light in the treatment of acne vulgaris," Br. J. Dermatol. 142, 973-978 (2000).
[CrossRef] [PubMed]

1999

1992

M. F. Arnsdorf and R. Lal, "Recent progress with atomic force microscopy in biology: molecular resolution imaging of cell membranes, constituent biomolecules, and microcrystals," Proc. SPIE 1778, 112-116 (1992).

E. Betzig and J. T. Trautman, "Near-field optics: microscopy, spectroscopy, and surface modification beyond the diffraction limit," Science 257, 189-195 (1992).
[CrossRef] [PubMed]

E. Betzig, P. L. Finn, and J. S. Weiner, "Combined shear force and near-field scanning optical microscopy," Appl. Phys. Lett. 60, 2484-2486 (1992).
[CrossRef]

T. Pangaribuan, K. Yamada, S. D. Jiang, H. Ohsawa, and M. Ohtsu, "Reproducible fabrication technique of nanometric tip diameter fiber probe for photon scanning tunneling microscope," Jpn. J. Appl. Phys. 31, L1302-L1304 (1992).
[CrossRef]

1991

E. Betzig, J. K. Trautman, T. D. Harris, J. S. Weiner, and R. L. Kostelak, "Breaking the diffraction barrier: optical microscopy on a nanometric scale," Science 251, 1468-1470 (1991).
[CrossRef] [PubMed]

1980

A. Shrier and J. R. Clay, "Pacemaker currents in chick embryonic heart cells change with development," Nature 283, 670-671 (1980).
[CrossRef] [PubMed]

1979

L. A. Greene, J. L. Connolly, R. R. Viscarello, and W. D. Riley, "Rapid, sequential changes in surface morphology of PC12 pheochromocytoma cells in response to nerve growth factor," J. Cell Biol. 82, 820-827 (1979).
[CrossRef] [PubMed]

1978

L. A. Greene, "Nerve growth factor prevents the death and stimulates the neuronal differentiation of clonal PC12 pheochromocytoma cells in serum-free medium," J. Cell Biol. 78, 747-755 (1978).
[CrossRef] [PubMed]

1977

L. A. Greene and G. Rein, "Release, storage and uptake of catecholamines by a clonal cell line of nerve growth factor (NGF) responsive pheochromocytoma cells," Brain Res. 129, 247-263 (1977).
[CrossRef] [PubMed]

1976

L. A. Greene and A. S. Tischler, "Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor," Proc. Natl. Acad. Sci. USA 73, 2424-2428 (1976).
[CrossRef] [PubMed]

Andersen, J. K.

D. Jiang, N. Jha, R. Boonplueang, and J. K. Andersen, "Caspase 3 inhibition attenuates hydrogen peroxide-induced DNA fragmentation but not cell death in neuronal PC12 cells," J. Neurochem. 76, 1745-1755 (2001).
[CrossRef] [PubMed]

Arnsdorf, M. F.

M. F. Arnsdorf and R. Lal, "Recent progress with atomic force microscopy in biology: molecular resolution imaging of cell membranes, constituent biomolecules, and microcrystals," Proc. SPIE 1778, 112-116 (1992).

Betzig, E.

E. Betzig and J. T. Trautman, "Near-field optics: microscopy, spectroscopy, and surface modification beyond the diffraction limit," Science 257, 189-195 (1992).
[CrossRef] [PubMed]

E. Betzig, P. L. Finn, and J. S. Weiner, "Combined shear force and near-field scanning optical microscopy," Appl. Phys. Lett. 60, 2484-2486 (1992).
[CrossRef]

E. Betzig, J. K. Trautman, T. D. Harris, J. S. Weiner, and R. L. Kostelak, "Breaking the diffraction barrier: optical microscopy on a nanometric scale," Science 251, 1468-1470 (1991).
[CrossRef] [PubMed]

Boonplueang, R.

D. Jiang, N. Jha, R. Boonplueang, and J. K. Andersen, "Caspase 3 inhibition attenuates hydrogen peroxide-induced DNA fragmentation but not cell death in neuronal PC12 cells," J. Neurochem. 76, 1745-1755 (2001).
[CrossRef] [PubMed]

Chu, A.

P. Papageorgiou, A. Katsambas, and A. Chu, "Phototherapy with blue (415 nm) and red (660 nm) light in the treatment of acne vulgaris," Br. J. Dermatol. 142, 973-978 (2000).
[CrossRef] [PubMed]

Clay, J. R.

A. Shrier and J. R. Clay, "Pacemaker currents in chick embryonic heart cells change with development," Nature 283, 670-671 (1980).
[CrossRef] [PubMed]

Connolly, J. L.

L. A. Greene, J. L. Connolly, R. R. Viscarello, and W. D. Riley, "Rapid, sequential changes in surface morphology of PC12 pheochromocytoma cells in response to nerve growth factor," J. Cell Biol. 82, 820-827 (1979).
[CrossRef] [PubMed]

Crabb, J. W.

J. W. Crabb, M. Miyagi, X. Gu, K. Shadrach, K. A. West, H. Sakaguchi, M. Kamei, A. Hasan, L. Yan, M. E. Rayborn, R. G. Salomon, and J. G. Hollyfield, "Drusen proteome analysis: an approach to the etiology of age-related macular degeneration," Proc. Natl. Acad. Sci. U S A 99, 14682-14687 (2002).
[CrossRef] [PubMed]

Deyner, M.

Finn, P. L.

E. Betzig, P. L. Finn, and J. S. Weiner, "Combined shear force and near-field scanning optical microscopy," Appl. Phys. Lett. 60, 2484-2486 (1992).
[CrossRef]

Gimzewski, J. K.

A. E. Pelling, S. Sehati, E. B. Gralla, J. S. Valentine, and J. K. Gimzewski, "Local nanomechanical motion of the cell wall of Saccharomyces cerevisiae," Science 305, 1147-1150 (2004).
[CrossRef] [PubMed]

Gralla, E. B.

A. E. Pelling, S. Sehati, E. B. Gralla, J. S. Valentine, and J. K. Gimzewski, "Local nanomechanical motion of the cell wall of Saccharomyces cerevisiae," Science 305, 1147-1150 (2004).
[CrossRef] [PubMed]

Greene, L. A.

L. A. Greene, J. L. Connolly, R. R. Viscarello, and W. D. Riley, "Rapid, sequential changes in surface morphology of PC12 pheochromocytoma cells in response to nerve growth factor," J. Cell Biol. 82, 820-827 (1979).
[CrossRef] [PubMed]

L. A. Greene, "Nerve growth factor prevents the death and stimulates the neuronal differentiation of clonal PC12 pheochromocytoma cells in serum-free medium," J. Cell Biol. 78, 747-755 (1978).
[CrossRef] [PubMed]

L. A. Greene and G. Rein, "Release, storage and uptake of catecholamines by a clonal cell line of nerve growth factor (NGF) responsive pheochromocytoma cells," Brain Res. 129, 247-263 (1977).
[CrossRef] [PubMed]

L. A. Greene and A. S. Tischler, "Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor," Proc. Natl. Acad. Sci. USA 73, 2424-2428 (1976).
[CrossRef] [PubMed]

Gu, X.

J. W. Crabb, M. Miyagi, X. Gu, K. Shadrach, K. A. West, H. Sakaguchi, M. Kamei, A. Hasan, L. Yan, M. E. Rayborn, R. G. Salomon, and J. G. Hollyfield, "Drusen proteome analysis: an approach to the etiology of age-related macular degeneration," Proc. Natl. Acad. Sci. U S A 99, 14682-14687 (2002).
[CrossRef] [PubMed]

Hara, M.

Harris, T. D.

E. Betzig, J. K. Trautman, T. D. Harris, J. S. Weiner, and R. L. Kostelak, "Breaking the diffraction barrier: optical microscopy on a nanometric scale," Science 251, 1468-1470 (1991).
[CrossRef] [PubMed]

Hasan, A.

J. W. Crabb, M. Miyagi, X. Gu, K. Shadrach, K. A. West, H. Sakaguchi, M. Kamei, A. Hasan, L. Yan, M. E. Rayborn, R. G. Salomon, and J. G. Hollyfield, "Drusen proteome analysis: an approach to the etiology of age-related macular degeneration," Proc. Natl. Acad. Sci. U S A 99, 14682-14687 (2002).
[CrossRef] [PubMed]

Hollyfield, J. G.

J. W. Crabb, M. Miyagi, X. Gu, K. Shadrach, K. A. West, H. Sakaguchi, M. Kamei, A. Hasan, L. Yan, M. E. Rayborn, R. G. Salomon, and J. G. Hollyfield, "Drusen proteome analysis: an approach to the etiology of age-related macular degeneration," Proc. Natl. Acad. Sci. U S A 99, 14682-14687 (2002).
[CrossRef] [PubMed]

Jha, N.

D. Jiang, N. Jha, R. Boonplueang, and J. K. Andersen, "Caspase 3 inhibition attenuates hydrogen peroxide-induced DNA fragmentation but not cell death in neuronal PC12 cells," J. Neurochem. 76, 1745-1755 (2001).
[CrossRef] [PubMed]

Jiang, D.

D. Jiang, N. Jha, R. Boonplueang, and J. K. Andersen, "Caspase 3 inhibition attenuates hydrogen peroxide-induced DNA fragmentation but not cell death in neuronal PC12 cells," J. Neurochem. 76, 1745-1755 (2001).
[CrossRef] [PubMed]

Jiang, S. D.

T. Pangaribuan, K. Yamada, S. D. Jiang, H. Ohsawa, and M. Ohtsu, "Reproducible fabrication technique of nanometric tip diameter fiber probe for photon scanning tunneling microscope," Jpn. J. Appl. Phys. 31, L1302-L1304 (1992).
[CrossRef]

Kamei, M.

J. W. Crabb, M. Miyagi, X. Gu, K. Shadrach, K. A. West, H. Sakaguchi, M. Kamei, A. Hasan, L. Yan, M. E. Rayborn, R. G. Salomon, and J. G. Hollyfield, "Drusen proteome analysis: an approach to the etiology of age-related macular degeneration," Proc. Natl. Acad. Sci. U S A 99, 14682-14687 (2002).
[CrossRef] [PubMed]

Katsambas, A.

P. Papageorgiou, A. Katsambas, and A. Chu, "Phototherapy with blue (415 nm) and red (660 nm) light in the treatment of acne vulgaris," Br. J. Dermatol. 142, 973-978 (2000).
[CrossRef] [PubMed]

Kawakami, Y.

R. Piga, R. Micheletto, and Y. Kawakami, "Nano-probing of the membrane dynamics of rat pheochromocytoma by near-field optics," Biophys. Chem. 117, 141-146 (2005).
[CrossRef] [PubMed]

Knoll, W.

Kostelak, R. L.

E. Betzig, J. K. Trautman, T. D. Harris, J. S. Weiner, and R. L. Kostelak, "Breaking the diffraction barrier: optical microscopy on a nanometric scale," Science 251, 1468-1470 (1991).
[CrossRef] [PubMed]

Lal, R.

M. F. Arnsdorf and R. Lal, "Recent progress with atomic force microscopy in biology: molecular resolution imaging of cell membranes, constituent biomolecules, and microcrystals," Proc. SPIE 1778, 112-116 (1992).

Micheletto, R.

R. Piga, R. Micheletto, and Y. Kawakami, "Nano-probing of the membrane dynamics of rat pheochromocytoma by near-field optics," Biophys. Chem. 117, 141-146 (2005).
[CrossRef] [PubMed]

R. Micheletto, M. Deyner, M. Scholl, K. Nakajima, A. Offenhauser, M. Hara, and W. Knoll, "Observation of the dynamics of live cardiomyocytes through a free running SNOM setup," Appl. Opt. 38, 6648-6662 (1999).
[CrossRef]

Miyagi, M.

J. W. Crabb, M. Miyagi, X. Gu, K. Shadrach, K. A. West, H. Sakaguchi, M. Kamei, A. Hasan, L. Yan, M. E. Rayborn, R. G. Salomon, and J. G. Hollyfield, "Drusen proteome analysis: an approach to the etiology of age-related macular degeneration," Proc. Natl. Acad. Sci. U S A 99, 14682-14687 (2002).
[CrossRef] [PubMed]

Nakajima, K.

Offenhauser, A.

Ohsawa, H.

T. Pangaribuan, K. Yamada, S. D. Jiang, H. Ohsawa, and M. Ohtsu, "Reproducible fabrication technique of nanometric tip diameter fiber probe for photon scanning tunneling microscope," Jpn. J. Appl. Phys. 31, L1302-L1304 (1992).
[CrossRef]

Ohtsu, M.

T. Pangaribuan, K. Yamada, S. D. Jiang, H. Ohsawa, and M. Ohtsu, "Reproducible fabrication technique of nanometric tip diameter fiber probe for photon scanning tunneling microscope," Jpn. J. Appl. Phys. 31, L1302-L1304 (1992).
[CrossRef]

Pangaribuan, T.

T. Pangaribuan, K. Yamada, S. D. Jiang, H. Ohsawa, and M. Ohtsu, "Reproducible fabrication technique of nanometric tip diameter fiber probe for photon scanning tunneling microscope," Jpn. J. Appl. Phys. 31, L1302-L1304 (1992).
[CrossRef]

Papageorgiou, P.

P. Papageorgiou, A. Katsambas, and A. Chu, "Phototherapy with blue (415 nm) and red (660 nm) light in the treatment of acne vulgaris," Br. J. Dermatol. 142, 973-978 (2000).
[CrossRef] [PubMed]

Pelling, A. E.

A. E. Pelling, S. Sehati, E. B. Gralla, J. S. Valentine, and J. K. Gimzewski, "Local nanomechanical motion of the cell wall of Saccharomyces cerevisiae," Science 305, 1147-1150 (2004).
[CrossRef] [PubMed]

Piga, R.

R. Piga, R. Micheletto, and Y. Kawakami, "Nano-probing of the membrane dynamics of rat pheochromocytoma by near-field optics," Biophys. Chem. 117, 141-146 (2005).
[CrossRef] [PubMed]

Rayborn, M. E.

J. W. Crabb, M. Miyagi, X. Gu, K. Shadrach, K. A. West, H. Sakaguchi, M. Kamei, A. Hasan, L. Yan, M. E. Rayborn, R. G. Salomon, and J. G. Hollyfield, "Drusen proteome analysis: an approach to the etiology of age-related macular degeneration," Proc. Natl. Acad. Sci. U S A 99, 14682-14687 (2002).
[CrossRef] [PubMed]

Rein, G.

L. A. Greene and G. Rein, "Release, storage and uptake of catecholamines by a clonal cell line of nerve growth factor (NGF) responsive pheochromocytoma cells," Brain Res. 129, 247-263 (1977).
[CrossRef] [PubMed]

Riley, W. D.

L. A. Greene, J. L. Connolly, R. R. Viscarello, and W. D. Riley, "Rapid, sequential changes in surface morphology of PC12 pheochromocytoma cells in response to nerve growth factor," J. Cell Biol. 82, 820-827 (1979).
[CrossRef] [PubMed]

Sakaguchi, H.

J. W. Crabb, M. Miyagi, X. Gu, K. Shadrach, K. A. West, H. Sakaguchi, M. Kamei, A. Hasan, L. Yan, M. E. Rayborn, R. G. Salomon, and J. G. Hollyfield, "Drusen proteome analysis: an approach to the etiology of age-related macular degeneration," Proc. Natl. Acad. Sci. U S A 99, 14682-14687 (2002).
[CrossRef] [PubMed]

Salomon, R. G.

J. W. Crabb, M. Miyagi, X. Gu, K. Shadrach, K. A. West, H. Sakaguchi, M. Kamei, A. Hasan, L. Yan, M. E. Rayborn, R. G. Salomon, and J. G. Hollyfield, "Drusen proteome analysis: an approach to the etiology of age-related macular degeneration," Proc. Natl. Acad. Sci. U S A 99, 14682-14687 (2002).
[CrossRef] [PubMed]

Scholl, M.

Sehati, S.

A. E. Pelling, S. Sehati, E. B. Gralla, J. S. Valentine, and J. K. Gimzewski, "Local nanomechanical motion of the cell wall of Saccharomyces cerevisiae," Science 305, 1147-1150 (2004).
[CrossRef] [PubMed]

Shadrach, K.

J. W. Crabb, M. Miyagi, X. Gu, K. Shadrach, K. A. West, H. Sakaguchi, M. Kamei, A. Hasan, L. Yan, M. E. Rayborn, R. G. Salomon, and J. G. Hollyfield, "Drusen proteome analysis: an approach to the etiology of age-related macular degeneration," Proc. Natl. Acad. Sci. U S A 99, 14682-14687 (2002).
[CrossRef] [PubMed]

Shrier, A.

A. Shrier and J. R. Clay, "Pacemaker currents in chick embryonic heart cells change with development," Nature 283, 670-671 (1980).
[CrossRef] [PubMed]

Tischler, A. S.

L. A. Greene and A. S. Tischler, "Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor," Proc. Natl. Acad. Sci. USA 73, 2424-2428 (1976).
[CrossRef] [PubMed]

Trautman, J. K.

E. Betzig, J. K. Trautman, T. D. Harris, J. S. Weiner, and R. L. Kostelak, "Breaking the diffraction barrier: optical microscopy on a nanometric scale," Science 251, 1468-1470 (1991).
[CrossRef] [PubMed]

Trautman, J. T.

E. Betzig and J. T. Trautman, "Near-field optics: microscopy, spectroscopy, and surface modification beyond the diffraction limit," Science 257, 189-195 (1992).
[CrossRef] [PubMed]

Valentine, J. S.

A. E. Pelling, S. Sehati, E. B. Gralla, J. S. Valentine, and J. K. Gimzewski, "Local nanomechanical motion of the cell wall of Saccharomyces cerevisiae," Science 305, 1147-1150 (2004).
[CrossRef] [PubMed]

Viscarello, R. R.

L. A. Greene, J. L. Connolly, R. R. Viscarello, and W. D. Riley, "Rapid, sequential changes in surface morphology of PC12 pheochromocytoma cells in response to nerve growth factor," J. Cell Biol. 82, 820-827 (1979).
[CrossRef] [PubMed]

Weiner, J. S.

E. Betzig, P. L. Finn, and J. S. Weiner, "Combined shear force and near-field scanning optical microscopy," Appl. Phys. Lett. 60, 2484-2486 (1992).
[CrossRef]

E. Betzig, J. K. Trautman, T. D. Harris, J. S. Weiner, and R. L. Kostelak, "Breaking the diffraction barrier: optical microscopy on a nanometric scale," Science 251, 1468-1470 (1991).
[CrossRef] [PubMed]

West, K. A.

J. W. Crabb, M. Miyagi, X. Gu, K. Shadrach, K. A. West, H. Sakaguchi, M. Kamei, A. Hasan, L. Yan, M. E. Rayborn, R. G. Salomon, and J. G. Hollyfield, "Drusen proteome analysis: an approach to the etiology of age-related macular degeneration," Proc. Natl. Acad. Sci. U S A 99, 14682-14687 (2002).
[CrossRef] [PubMed]

Yamada, K.

T. Pangaribuan, K. Yamada, S. D. Jiang, H. Ohsawa, and M. Ohtsu, "Reproducible fabrication technique of nanometric tip diameter fiber probe for photon scanning tunneling microscope," Jpn. J. Appl. Phys. 31, L1302-L1304 (1992).
[CrossRef]

Yan, L.

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Figures (3)

Fig. 1.
Fig. 1.

Schematic representation of the core of the test system. Laser is a He-Cd 442 nm, the objective lens is a Nikon ELWD 40x with 0.6 Numerical Aperture focusing on the fiber tip.

Fig. 2.
Fig. 2.

Time profile of cell recordings for three different cell conditions: normal, NGF and necrosis. (a) control; (b) 24 hours NGF; (c) 4 hours H2O2. Time frame is of 100 seconds total for each recording, sampled at 0.01 sec (10.000 points per plot). Using a numerical algorithm we derived the Fourier spectrum for each sample: (d) control; (e) 24 hours NGF; (f) 4 hours H2O2. Lower frequencies are plotted in the smaller insets for clarity. Obvious differences are visible in the time profile and in the Fourier spectrum. Vertical scale is Volts for the time profiles and Volts/Frequency (Hz) for the Fourier plots.

Fig. 3.
Fig. 3.

The acoustical part of the spectrum of the membrane dynamics studied. (a) control; (b) 24 hours NGF; (c) 4 hours H2O2. Actual sound was generated by means of a transducer. Frequencies from 5 Hz were perceivable and different cell conditions could be distinguished by simply hearing the sound, see text for discussion. Vertical scale is Volts for the time profiles and Volts/Frequency for the Fourier plots.

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