Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-05T04:20:22.316Z Has data issue: false hasContentIssue false
  • English
  • Français

Application of AFM to the Nanomechanics of Cancer

Published online by Cambridge University Press:  11 April 2016

Shivani Sharma  and
James K Gimzewski
Shivani Sharma
Affiliation:
California NanoSystems Institute, Los Angeles, California, USA
James K Gimzewski*
Affiliation:
California NanoSystems Institute, Los Angeles, California, USA Department of Chemistry and Biochemistry, University of California, Los Angeles, California, USA International Center for Materials Nanoarchitectonics Satellite (MANA), National Institute for Materials Science (NIMS), Tsukuba, Japan
*
*(Email: [email protected])
Get access

Abstract

Cancer cell metastasis is a leading cause of mortality whereby cancer cells migrate from a tumor and spread to distant sites in the body. Understanding metastasis requires a deeper understanding of biomechanics and mechanobiology at the cellular level. We have established the use of Atomic Force Microscopy to infer the mechanical properties of single cells in cultures by measurement of their Young’s modulus. Here we discuss the main advantages, challenges, technological limitations and applicability of AFM based cell mechanics studies along with other emerging high throughput techniques for the development of single cell mechanical based clinical assays for cancer detection and management.

Keywords

nano-indentationbiomaterialbiomedical
Type
Articles
Information
MRS Advances , Volume 1 , Issue 25: Theory, Characterization, and Modeling , 2016 , pp. 1817 - 1827
Copyright
Copyright © Materials Research Society 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Fritsch, A., Hockel, M., Kiessling, T., Nnetu, K. D., Wetzel, F., Zink, M., and Kas, J. A., “Are biomechanical changes necessary for tumour progression?,” Nature Physics, vol. 6, pp. 730–732, Oct 2010.Google Scholar
Suresh, S., “Biomechanics and biophysics of cancer cells,” Acta Biomater, vol. 3, pp. 413–38, Jul 2007.Google Scholar
Yallapu, M. M., Katti, K. S., Katti, D. R., Mishra, S. R., Khan, S., Jaggi, M., and Chauhan, S. C., “The roles of cellular nanomechanics in cancer,” Med Res Rev, vol. 35, pp. 198–223, Jan 2015.CrossRefGoogle Scholar
Cross, S. E., Jin, Y. S., Rao, J., and Gimzewski, J. K., “Nanomechanical analysis of cells from cancer patients,” Nature Nanotechnology, vol. 2, pp. 780–783, Dec 2007.Google Scholar
Li, Q. S., Lee, G. Y. H., Ong, C. N., and Lim, C. T., “AFM indentation study of breast cancer cells,” Biochemical and Biophysical Research Communications, vol. 374, pp. 609–613, Oct 3 2008.Google Scholar
Corbin, E. A., Kong, F., Lim, C. T., King, W. P., and Bashir, R., “Biophysical properties of human breast cancer cells measured using silicon MEMS resonators and atomic force microscopy,” Lab on a Chip, vol. 15, pp. 839–847, 2015.CrossRefGoogle Scholar
Hou, H. W., Li, Q. S., Lee, G. Y. H., Kumar, A. P., Ong, C. N., and Lim, C. T., “Deformability study of breast cancer cells using microfluidics,” Biomedical Microdevices, vol. 11, pp. 557–564, Jun 2009.CrossRefGoogle Scholar
Guck, J., Schinkinger, S., Lincoln, B., Wottawah, F., Ebert, S., Romeyke, M., Lenz, D., Erickson, H. M., Ananthakrishnan, R., Mitchell, D., Kas, J., Ulvick, S., and Bilby, C., “Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence,” Biophysical Journal, vol. 88, pp. 3689–3698, May 2005.Google Scholar
Plodinec, M., Loparic, M., Monnier, C. A., Obermann, E. C., Zanetti-Dallenbach, R., Oertle, P., Hyotyla, J. T., Aebi, U., Bentires-Alj, M., Lim, R. Y. H., and Schoenenberger, C. A., “The nanomechanical signature of breast cancer,” Nature Nanotechnology, vol. 7, pp. 757–765, Nov 2012.Google Scholar
Lekka, M., Gil, D., Pogoda, K., Dulinska-Litewka, J., Jach, R., Gostek, J., Klymenko, O., Prauzner-Bechcicki, S., Stachura, Z., Wiltowska-Zuber, J., Okon, K., and Laidler, P., “Cancer cell detection in tissue sections using AFM,” Archives of Biochemistry and Biophysics, vol. 518, pp. 151–156, Feb 15 2012.Google Scholar
Lekka, M., Pogoda, K., Gostek, J., Klymenko, O., Prauzner-Bechcicki, S., Wiltowska-Zuber, J., Jaczewska, J., Lekki, J., and Stachura, Z., “Cancer cell recognition - Mechanical phenotype,” Micron, vol. 43, pp. 1259–1266, Dec 2012.Google Scholar
Samani, A. and Plewes, D., “A method to measure the hyperelastic parameters of ex vivo breast tissue samples,” Physics in Medicine and Biology, vol. 49, pp. 4395–4405, Sep 21 2004.Google Scholar
Lekka, M., Laidler, P., Gil, D., Lekki, J., Stachura, Z., and Hrynkiewicz, A. Z., “Elasticity of normal and cancerous human bladder cells studied by scanning force microscopy,” European Biophysics Journal with Biophysics Letters, vol. 28, pp. 312–316, 1999.Google Scholar
Canetta, E., Riches, A., Borger, E., Herrington, S., Dholakia, K., and Adya, A. K., “Discrimination of bladder cancer cells from normal urothelial cells with high specificity and sensitivity: Combined application of atomic force microscopy and modulated Raman spectroscopy,” Acta Biomaterialia, vol. 10, pp. 2043–2055, May 2014.Google Scholar
Shojaei-Baghini, E., Zheng, Y., Jewett, M. A. S., Geddie, W. B., and Sun, Y., “Mechanical characterization of benign and malignant urothelial cells from voided urine,” Applied Physics Letters, vol. 102, Mar 25 2013.Google Scholar
Sharma, S., Santiskulvong, C., Bentolila, L. A., Rao, J. Y., Dorigo, O., and Gimzewski, J. K., “Correlative nanomechanical profiling with super-resolution F-actin imaging reveals novel insights into mechanisms of cisplatin resistance in ovarian cancer cells,” Nanomedicine-Nanotechnology Biology and Medicine, vol. 8, pp. 757–766, Jul 2012.Google Scholar
Xu, W. W., Mezencev, R., Kim, B., Wang, L. J., McDonald, J., and Sulchek, T., “Cell Stiffness Is a Biomarker of the Metastatic Potential of Ovarian Cancer Cells,” Plos One, vol. 7, Oct 4 2012.Google Scholar
Swaminathan, V., Mythreye, K., O’Brien, E. T., Berchuck, A., Blobe, G. C., and Superfine, R., “Mechanical Stiffness Grades Metastatic Potential in Patient Tumor Cells and in Cancer Cell Lines,” Cancer Research, vol. 71, pp. 5075–5080, Aug 1 2011.CrossRefGoogle Scholar
Ding, Y. X., Cheng, Y., Sun, Q. M., Zhang, Y. Y., You, K., Guo, Y. L., Han, D., and Geng, L., “Mechanical characterization of cervical squamous carcinoma cells by atomic force microscopy at nanoscale,” Medical Oncology, vol. 32, Mar 2015.Google Scholar
Palmieri, V., Lucchetti, D., Maiorana, A., Papi, M., Maulucci, G., Ciasca, G., Svelto, M., De Spirito, M., and Sgambato, A., “Biomechanical investigation of colorectal cancer cells,” Applied Physics Letters, vol. 105, Sep 22 2014.CrossRefGoogle Scholar
Rebelo, L. M., de Sousa, J. S., Mendes, J., and Radmacher, M., “Comparison of the viscoelastic properties of cells from different kidney cancer phenotypes measured with atomic force microscopy,” Nanotechnology, vol. 24, Feb 8 2013.Google Scholar
Rosenbluth, M. J., Lam, W. A., and Fletcher, D. A., “Force microscopy of nonadherent cells: A comparison of leukemia cell deformability,” Biophysical Journal, vol. 90, pp. 2994–3003, Apr 2006.CrossRefGoogle Scholar
Tan, Y. H., Fung, T. K., Wan, H. X., Wang, K. Q., Leung, A. Y. H., and Sun, D., “Biophysical characterization of hematopoietic cells from normal and leukemic sources with distinct primitiveness,” Applied Physics Letters, vol. 99, Aug 22 2011.Google Scholar
Zheng, Y., Wen, J., Nguyen, J., Cachia, M. A., Wang, C., and Sun, Y., “Decreased deformability of lymphocytes in chronic lymphocytic leukemia,” Scientific Reports, vol. 5, Jan 9 2015.Google Scholar
Suganuma, M., Takahashi, A., Watanabe, T., Akiyama, H., Nakajima, Y., Mondal, A., and Fujiki, H., “Abstract 2640A: Cell stiffness as a new indicator of diagnosis for human lung cancer cells and their metastasis,” Cancer Research, vol. 73, p. 2640A, April 15, 2013 2013.Google Scholar
Watanabe, T., Kuramochi, H., Takahashi, A., Imai, K., Katsuta, N., Nakayama, T., Fujiki, H., and Suganuma, M., “Higher cell stiffness indicating lower metastatic potential in B16 melanoma cell variants and in (-)-epigallocatechin gallate-treated cells,” Journal of Cancer Research and Clinical Oncology, vol. 138, pp. 859–866, May 2012.Google Scholar
Weder, G., Hendriks-Balk, M. C., Smajda, R., Rimoldi, D., Liley, M., Heinzelmann, H., Meister, A., and Mariotti, A., “Increased plasticity of the stiffness of melanoma cells correlates with their acquisition of metastatic properties,” Nanomedicine-Nanotechnology Biology and Medicine, vol. 10, pp. 141–148, Jan 2014.Google Scholar
Gossett, D. R., Tse, H. T. K., Lee, S. A., Ying, Y., Lindgren, A. G., Yang, O. O., Rao, J. Y., Clark, A. T., and Di Carlo, D., “Hydrodynamic stretching of single cells for large population mechanical phenotyping,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, pp. 7630–7635, May 15 2012.Google Scholar
Tse, H. T. K., Gossett, D. R., Moon, Y. S., Masaeli, M., Sohsman, M., Ying, Y., Mislick, K., Adams, R. P., Rao, J. Y., and Di Carlo, D., “Quantitative Diagnosis of Malignant Pleural Effusions by Single-Cell Mechanophenotyping,” Science Translational Medicine, vol. 5, Nov 20 2013.Google Scholar
Cross, S. E., Jin, Y. S., Tondre, J., Wong, R., Rao, J., and Gimzewski, J. K., “AFM-based analysis of human metastatic cancer cells,” Nanotechnology, vol. 19, Sep 24 2008.CrossRefGoogle Scholar
Faria, E. C., Ma, N., Gazi, E., Gardner, P., Brown, M., Clarke, N. W., and Snooka, R. D., “Measurement of elastic properties of prostate cancer cells using AFM,” Analyst, vol. 133, pp. 1498–1500, 2008.Google Scholar
Chen, C. L., Mahalingam, D., Osmulski, P., Jadhav, R. R., Wang, C. M., Leach, R. J., Chang, T. C., Weitman, S. D., Kumar, A. P., Sun, L. Z., Gaczynska, M. E., Thompson, I. M., and Huang, T. H. M., “Single-cell analysis of circulating tumor cells identifies cumulative expression patterns of EMT-related genes in metastatic prostate cancer,” Prostate, vol. 73, pp. 813–826, Jun 2013.Google Scholar
Ahn, B. M., Kim, J., Ian, L., Rha, K. H., and Kim, H. J., “Mechanical Property Characterization of Prostate Cancer Using a Minimally Motorized Indenter in an Ex Vivo Indentation Experiment,” Urology, vol. 76, pp. 1007–1011, Oct 2010.Google Scholar
Shin, T. Y., Kim, Y. J., Lim, S. K., Kim, J., and Rha, K. H., “Robotic Mechanical Localization of Prostate Cancer Correlates with Magnetic Resonance Imaging Scans,” Yonsei Medical Journal, vol. 54, pp. 907–911, Jul 1 2013.Google Scholar
Tan, Y. and Sun, D., “Apply Robot-Tweezers Manipulation to Cell Stretching for Biomechanical Characterization,” in Nanorobotics, Mavroidis, C. and Ferreira, A., Eds., ed: Springer New York, 2013, pp. 223–239.Google Scholar
Lekka, M. and Laidler, P., “Applicability of AFM in cancer detection,” Nature Nanotechnology, vol. 4, pp. 72–72, Feb 2009.Google Scholar
Pajerowski, J. D., Dahl, K. N., Zhong, F. L., Sammak, P. J., and Discher, D. E., "Physical plasticity of the nucleus in stem cell differentiation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, pp. 15619–15624, Oct 2 2007.Google Scholar
Hochmuth, R. M., “Micropipette aspiration of living cells,” Journal of Biomechanics, vol. 33, pp. 15–22, Jan 2000.Google Scholar
Rosenbluth, M. J., Lam, W. A., and Fletcher, D. A., “Analyzing cell mechanics in hematologic diseases with microfluidic biophysical flow cytometry,” Lab on a Chip, vol. 8, pp. 1062–1070, 2008.Google Scholar
Bow, H., Pivkin, I. V., Diez-Silva, M., Goldfless, S. J., Dao, M., Niles, J. C., Suresh, S., and Han, J. Y., “A microfabricated deformability-based flow cytometer with application to malaria,” Lab on a Chip, vol. 11, pp. 1065–1073, 2011.Google Scholar
Chen, J., Zheng, Y., Tan, Q. Y., Shojaei-Baghini, E., Zhang, Y. L., Li, J., Prasad, P., You, L. D., Wu, X. Y., and Sun, Y., “Classification of cell types using a microfluidic device for mechanical and electrical measurement on single cells,” Lab on a Chip, vol. 11, pp. 3174–3181, 2011.Google Scholar
Abkarian, M., Faivre, M., and Stone, H. A., “High-speed microfluidic differential manometer for cellular-scale hydrodynamics,” Proc Natl Acad Sci U S A, vol. 103, pp. 538–42, Jan 17 2006.CrossRefGoogle Scholar
Katsumoto, Y., Tatsumi, K., Doi, T., and Nakabe, K., “Electrical classification of single red blood cell deformability in high-shear microchannel flows,” International Journal of Heat and Fluid Flow, vol. 31, pp. 985–995, 2010.Google Scholar
Remmerbach, T. W., Wottawah, F., Dietrich, J., Lincoln, B., Wittekind, C., and Guck, J., “Oral Cancer Diagnosis by Mechanical Phenotyping,” Cancer Research, vol. 69, pp. 1728–1732, Mar 1 2009.Google Scholar
Forsyth, A. M., Wan, J. D., Ristenpart, W. D., and Stone, H. A., “The dynamic behavior of chemically "stiffened" red blood cells in microchannel flows,” Microvascular Research, vol. 80, pp. 37–43, Jul 2010.Google Scholar
Hoelzle, D. J., Varghese, B. A., Chan, C. K., and Rowat, A. C., “A microfluidic technique to probe cell deformability,” J Vis Exp, p. e51474, 2014.Google Scholar
Osmulski, P., Mahalingam, D., Gaczynska, M. E., Liu, J., Huang, S., Horning, A. M., Wang, C. M., Thompson, I. M., Huang, T. H., and Chen, C. L., “Nanomechanical biomarkers of single circulating tumor cells for detection of castration resistant prostate cancer,” Prostate, vol. 74, pp. 1297–307, Sep 2014.Google Scholar
Plodinec, M., Loparic, M., Monnier, C. A., Obermann, E. C., Zanetti-Dallenbach, R., Oertle, P., Hyotyla, J. T., Aebi, U., Bentires-Alj, M., Lim, R. Y., and Schoenenberger, C. A., “The nanomechanical signature of breast cancer,” Nature Nanotechnology, vol. 7, pp. 757–65, Nov 2012.Google Scholar
Roduit, C., Sekatski, S., Dietler, G., Catsicas, S., Lafont, F., and Kasas, S., “Stiffness tomography by atomic force microscopy,” Biophys J, vol. 97, pp. 674–7, Jul 22 2009.Google Scholar
Braunsmann, C., Seifert, J., Rheinlaender, J., and Schaffer, T. E., “High-speed force mapping on living cells with a small cantilever atomic force microscope,” Review of Scientific Instruments, vol. 85, Jul 2014.Google Scholar
Slade, A., Pittenger, B., Milani, P., Boudaoud, A., Hamant, O., Kioschis, P., Ponce, L. M., and Hafner, M., “Investigating cell mechanics with atomic force microscopy,” Microscopy and Analysis, vol. 28, pp. S6–S9, 2014.Google Scholar
Pittenger, B., Erina, N., and Su, C., “Quantitative mechanical property mapping at the nanoscale with PeakForce QNM,” Bruker Application Note #128, 2011.Google Scholar
Ushiki, T., Hitomi, J., Umemoto, T., Yamamoto, S., Kanazawa, H., and Shigeno, M., “Imaging of living cultured cells of an epithelial nature by atomic force microscopy,” Archives of Histology and Cytology, vol. 62, pp. 47–55, Mar 1999.Google Scholar
Ross, B., Motherby, H., Saurenbach, F., Frohn, J., Kube, M., and Bocking, A., “Atomic force microscopy in effusion cytology,” Analytical and Quantitative Cytology and Histology, vol. 20, pp. 97–104, Apr 1998.Google Scholar
Sharma, S., Santiskulvong, C., Bentolila, L. A., Rao, J., Dorigo, O., and Gimzewski, J. K., “Correlative nanomechanical profiling with super-resolution F-actin imaging reveals novel insights into mechanisms of cisplatin resistance in ovarian cancer cells,” Nanomedicine, vol. 8, pp. 757–66, Jul 2012.Google Scholar