Mechanical phenotyping of mouse embryonic stem cells: Increase in stiffness with differentiation

Cellular Reprogramming

Volumn 13, Issue 4, 2011, Pages 371-380

  Pillarisetti, Anand ^a,c   Desai, Jaydev P ^a   Ladjal, Hamid ^b   Schiffmacher, Andrew ^a   Ferreira, Antoine ^b   Keefer, Carol L ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b ENSI de Bourges   (France)

^c TEXAS INSTRUMENTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTIC METHOD; ANIMAL CELL; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; EMBRYONIC STEM CELL; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SURFACE PROPERTY; YOUNG MODULUS;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; ELASTIC MODULUS; EMBRYONIC STEM CELLS; MICE; MICROSCOPY, ATOMIC FORCE; PHENOTYPE; STRESS, MECHANICAL;

EID: 79961037334     PISSN: 21524971     EISSN: 21524998     Source Type: Journal    
DOI: 10.1089/cell.2011.0028     Document Type: Article

References (48)

1. Alcaraz, J., Buscemi, L., Grabulosa, M., et al. (2003). Microrheology of human lung epithelial cells measured by atomic force microscopy. Biophys. J. 84, 2071-2079. (Pubitemid 36322968)
2. Bilodeau, G. G. (1992). Regular pyramid punch problem. J. Appl. Mech. 59, 519-523. (Pubitemid 23590265)
3. Bourne, S., Polak, J. M., Hughes, S. P. F., et al. (2004). Osteogenic differentiation of mouse embryonic stem cells: differential gene expression analysis by cDNA microarray and purification of osteoblasts by cadherin-11 magnetically activated cell sorting. Tissue Eng. 10, 796-806. (Pubitemid 38880398)
4. Cao, Y., Yang, D., and Soboyejoy, W. (2005). Nanoindentation method for determining the initial contact and adhesion characteristics of soft polydimethylsiloxane. J. Mater. Res. 20, 2004-2011. (Pubitemid 41763303)
5. Chambers, I., and Smith, A. (2004). Self-renewal of teratocarcinoma and embryonic stem cells. Oncogene 23, 7150-7160. (Pubitemid 39382149)
6. Chowdhury, F., Na, S., Li, D., et al. (2010). Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells. Nat. Mater. 9, 82-88.
7. Christoforou, N., Miller, R. A., Hill, C. M., et al. (2008). Mouse ES cell-derived cardiac precursor cells are multipotent and facilitate identification of novel cardiac genes. J. Clin. Invest. 118, 894-903. (Pubitemid 351364597)
8. Collinsworth, A. M., Zhang, S., Kraus, W. E., et al. (2002). Apparent elastic modulus and hysteresis of skeletal muscle cells throughout differentiation. Am. J. Physiol. Cell Physiol. 283, 1219-1227.
9. Constantinescu, D., Gray, H. L., Sammak, P. J., et al. (2006). Lamin A/C expression is a marker of mouse and human embryonic stem cell differentiation. Stem Cells 24, 177-185.
10. Daniels, B. R., Hale, C. M., Khatau, S. B., et al. (2010). Differences in the microrheology of human embryonic stem cells and human induced pluripotent stem cells. Biophys. J. 99, 3563-3570.
11. Danti, S., D'Acunto, M., Trombi, L., et al. (2007). A micro/nanoscale surface mechanical study on morpho-functional changes in multilineage- differentiated human mesenchymal stem cells. Macromol. Biosci. 7, 589-598. (Pubitemid 47264632)
12. Dechat, T., Pfleghaar, K., Sengupta, K., et al. (2008). Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev. 22, 832-853. (Pubitemid 351482836)
13. Dechat, T., Adam, S. A., and Goldman, R. D. (2009). Nuclear lamins and chromatin: when structure meets function. Adv. Enzyme Regul. 49, 157-166.
14. Docheva, D., Padula, D., Popov, C., et al. (2008). Researching into the cellular shape, volume and elasticity of mesenchymal stem cells, osteoblasts and osteosarcoma cells by atomic force microscopy. J. Cell Mol. Med. 12, 537-552. (Pubitemid 351555133)
15. Donovan, P. J., and Gearhart, J. (2001). The end of the beginning for pluripotent stem cells. Nature 414, 92-97.
16. Girot, M., Boukallel, M., and Régnier, S. (2006). Modeling soft contact mechanism of biological cells using an atomic force bio-microscope. In International Conference on Intelligent Robots and Systems, Beijing, China, pp. 1831-1836. (Pubitemid 46928161)
17. Goldmann, W. H. (2002). Mechanical aspects of cell shape regulation and signaling. Cell Biol. Int. 26, 313-317.
18. Hammerick, K. E., Huang, Z., Sun, N., et al. (2011). Elastic properties of induced pluripotent stem cells. Tissue Eng Part A 17, 495-502.
19. He, S., Pant, D., Schiffmacher, A., et al. (2006). Developmental expression of pluripotency determining factors in caprine embryos: novel pattern of NANOG protein localization in the nucleolus. Mol. Reprod. Dev. 73, 1512-1522. (Pubitemid 44631020)
20. He, S., Pant, D., Schiffmacher, A., et al. (2008). Lymphoid enhancer factor 1-mediated Wnt signaling promotes the initiation of trophoblast lineage differentiation in mouse embryonic stem cells. Stem Cells 26, 842-849.
21. Hutter, J. L., and Bechhoefer, J. (1993). Calibration of atomic force microscope tips. Rev. Sci. Instrum. 64, 1868-1873.
22. Johnson, K. L. (1982). One hundred years of Hertz contact. In Proc Inst Mech Eng 196.
23. Kolossov, E., Fleischmann, B. K., Liu, Q., et al. (1998). Functional characteristics of ES cell-derived cardiac precursor cells identified by tissue specific expression of the green fluorescent protein. J. Cell Biol. 143, 2045-2056. (Pubitemid 29022623)
24. Kwon, E., Kim, Y., Park, J., et al. (2007). Measurement of pull-off forces by atomic force microscope in liquids used for biological applications. Exp. Tech. 31, 40-45.
25. Ladjal, H., Hanus, J. L., Pillarisetti, A., et al. (2010). Reality-based real-time cell indentation stimulator. IEEE/ASME Trans. Mech. PP, 1-12.
26. Maugis, D. (2000). Contact, Adhesion and Rupture of Elastic Solids (Springer, New York).
27. Nagano, K., Yoshida, Y., and Isobe, T. (2008). Cell surface biomarkers of embryonic stem cells. Proteomics 8, 4025-4035.
28. Odorico, J. S., Kaufman, D. S., and Thomson, J. A. (2001). Multilineage differentiation from human embryonic stem cell lines. Stem Cells 19, 193-204. (Pubitemid 32524540)
29. Pajerowski, J. D., Dahl, K. N., Zhong, F. L., et al. (2007). Physical plasticity of the nucleus in stem cell differentiation. Proc. Natl. Acad. Sci. USA 104, 15619-15624. (Pubitemid 350035348)
30. Pillarisetti, A. (2009). Mechanical Manipulation and Characterization of Biological Cells (University of Maryland, College Park, MD).
31. Pillarisetti, A., Ladjal, H., Ferreira, A., Keefer, C., and Desai, J. P. (2009). Mechanical characterization of mouse embryonic stem cells. In 31st Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Minneapolis, Minnesota, pp. 1176-1179.
32. Pillarisetti, A., Keefer, C., and Desai, J. P. (2008). Mechanical response of embryonic stem cells using haptics-enabled atomic force microscopy. In International Symposium on Experimental Robotics, Athens, Greece.
33. Rico, F., Roca-Cusachs, P., Gavara, N., et al. (2005). Probing mechanical properties of living cells by atomic force microscopy with blunted pyramidal cantilever tips. Phys. Rev. E 72, 1-10. (Pubitemid 41520946)
34. Rober, R. A., Weber, K., and Osborn, M. (1989). Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: a developmental study. Development 105, 365-378. (Pubitemid 19053283)
35. Rosenbluth, M. J., Lam, W. A., and Fletcher, D. A. (2006). Force microscopy of nonadherent cells: a comparison of leukemia cell deformability. Biophys. J. 90, 2994-3003.
36. Schillers, H., Walte, M., Urbanova, K., et al. (2010). Real-time monitoring of cell elasticity reveals oscillating myosin activity. Biophys. J. 99, 3639-3646.
37. Sharova, L. V., Sharov, A. A., Piao, Y., et al. (2007). Global gene expression profiling reveals similarities and differences among mouse pluripotent stem cells of different origins and strains. Dev. Biol. 307, 446-459. (Pubitemid 47001365)
38. Shumaker, D. K., Kuczmarski, E. R., and Goldman, R. D. (2003). The nucleoskeleton: lamins and actin are major players in essential nuclear functions. Curr. Opin. Cell Biol. 15, 358-366. (Pubitemid 36638656)
39. Smith, A. G. (2001). Embryo-derived stem cells: of mice and men. Annu. Rev. Cell Dev. Biol. 17, 435-462. (Pubitemid 33096183)
40. Sneddon, I. N. (1948). Boussinesq's problem for a rigid cone. Math. Proc. Cambridge Philos. Soc. 44, 492-507.
41. Stewart, C., and Burke, B. (1987). Teratocarcinoma stem cells and early mouse embryos contain only a single major lamin polypeptide closely resembling lamin B. Cell 51, 383-392.
42. Stewart, R., Yang, C., Anyfantis, G., et al. (2008). Silencing of the expression of pluripotent driven-reporter genes stably transfected into human pluripotent cells. Regen. Med. 3, 505-522.
43. Takahashi, T., Lord, B., Schulze, P. S., et al. (2003). Ascorbic acid enhances differentiation of embryonic stem cells into cardiac myocytes. Basic Sci. Rep. 107, 1912-1916. (Pubitemid 36444134)
44. Titushkin, I., and Cho, M. (2007). Modulation of cellular mechanics during osteogenic differentiation of human mesenchymal stem cells. Biophys. J. 93, 3693-3702. (Pubitemid 350190831)
45. Touhami, A., Nysten, B., and Dufrêne, Y. F. (2003). Nanoscale mapping of the elasticity of microbial cells by atomic force microscopy. Langmuir 19, 4539-4543.
46. Vinckier, A., and Semenza, G. (1998). Measuring elasticity of biological materials by atomic force microscopy. FEBS Lett. 430, 12-16. (Pubitemid 28307023)
47. Weisenhorn, A. L., Khorsandi, M., Kasas, S., et al. (1993). Deformation and height anomaly of soft surfaces studied with an AFM. Nanotechnology 4, 106-113. (Pubitemid 23683376)
48. Yourek, G., Hussain, M. A., and Mao, J. J. (2007). Cytoskeletal changes of mesenchymal stem cells during differentiation. Asaio J. 53, 219-228. (Pubitemid 46597573)