Mesenchymal stem cell mechanics from the attached to the suspended state

Biophysical Journal

Volumn 99, Issue 8, 2010, Pages 2479-2487

  Maloney, John M ^a   Nikova, Dessy ^a   Lautenschläger, Franziska ^c   Clarke, Emer ^d   Langer, Robert ^a,b   Guck, Jochen ^c   Van Vliet, Krystyn J ^a,b  

^a Department of Materials Science and Engineering ^*  (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d ReachBio   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 78049343321     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.08.052     Document Type: Article

References (52)

1. Pittenger, M. F., A. M. Mackay, ⋯, D. R. Marshak. 1999. Multilineage potential of adult human mesenchymal stem cells. Science. 284: 143-147.
2. Horwitz, E. M., D. J. Prockop, ⋯, M. K. Brenner. 1999. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat. Med. 5:309-313.
3. Chen, S. L., W. W. Fang, ⋯, J. P. Sun. 2004. Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am. J. Cardiol. 94:92-95.
4. Bruder, S. P., N. Jaiswal, and S. E. Haynesworth. 1997. Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J. Cell. Biochem. 64:278-294.
5. Dominici, M., K. Le Blanc, ⋯, E. Horwitz. 2006. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 8: 315-317.
6. Engler, A. J., S. Sen, ⋯, D. E. Discher. 2006. Matrix elasticity directs stem cell lineage specification. Cell. 126:677-689.
7. Chowdhury, F., S. Na, ⋯, N. Wang. 2009. Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells. Nat. Mater. 9:82-88.
8. Banfi, A., A. Muraglia, ⋯, R. Quarto. 2000. Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: Implications for their use in cell therapy. Exp. Hematol. 28:707-715.
9. Bonab, M. M., K. Alimoghaddam, ⋯, B. Nikbin. 2006. Aging of mesenchymal stem cell in vitro. BMC Cell Biol. 7:14.
10. Kim, J., J.W. Kang,., H. S. Kim. 2009. Biological characterization of long-term cultured human mesenchymal stem cells. Arch. Pharm. Res. 32:117-126.
11. Mets, T., and G. Verdonk. 1981. In vitro aging of human bone marrow derived stromal cells. Mech. Ageing Dev. 16:81-89.
12. Colter, D. C., I. Sekiya, and D. J. Prockop. 2001. Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc. Natl. Acad. Sci. USA. 98:7841-7845.
13. Petersen, N. O., W. B. McConnaughey, and E. L. Elson. 1982. Dependence of locally measured cellular deformability on position on the cell, temperature, and cytochalasin B. Proc. Natl. Acad. Sci. USA. 79:5327-5331.
14. Rotsch, C., and M. Radmacher. 2000. Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: An atomic force microscopy study. Biophys. J. 78:520-535.
15. Guck, J., R. Ananthakrishnan, ⋯, J. Käs. 2001. The optical stretcher: A novel laser tool to micromanipulate cells. Biophys. J. 81:767-784.
16. Guck, J., S. Schinkinger, ⋯, C. Bilby. 2005. Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophys. J. 88:3689-3698.
17. Harrison, C. J., and T. D. Allen. 1979. Cell surface morphology after trypsinization depends on initial cell shape. Differentiation. 15:61-66.
18. Garnett, H. M. 1980. A scanning electron microscope study of the sequential changes in morphology occurring in human fibroblasts placed in suspension culture. Cytobios. 27:7-18.
19. Kinn, S. R., and T. D. Allen. 1981. Conversion of blebs to microvilli: Cell surface reorganization after trypsin. Differentiation. 20:168-173.
20. Charras, G. T., M. Coughlin,., L. Mahadevan. 2008. Life and times of a cellular bleb. Biophys. J. 94:1836-1853.
21. Fackler, O. T., and R. Grosse. 2008. Cell motility through plasma membrane blebbing. J. Cell Biol. 181:879-884.
22. Fabry, B., G. N. Maksym, ⋯, J. J. Fredberg. 2001. Scaling the microrheology of living cells. Phys. Rev. Lett. 87:148102.
23. Fabry, B., G. N. Maksym,., J. J. Fredberg. 2003. Time scale and other invariants of integrative mechanical behavior in living cells. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 68:041914.
24. Puig-de Morales, M., E. Millet, ⋯, J. J. Fredberg. 2004. Cytoskeletal mechanics in the adherent human airway smooth muscle cell: Probe specificity and scaling of protein-protein dynamics. Am. J. Physiol. Cell Physiol. 287:C643-C654.
25. Balland, M., N. Desprat,., F. Gallet. 2006. Power laws in microrheology experiments on living cells: Comparative analysis and modeling. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 74:021911.
26. Lenormand, G., A. M. Alencar, ⋯, J. J. Fredberg. 2008. The cytoskeleton of the living cell as an out-of-equilibrium system. In Phase Transitions in Cell Biology. Springer, Dordrecht, The Netherlands. 111-141.
27. Zhou, E. H., S. T. Quek, and C. T. Lim. 2010. Power-law rheology analysis of cells undergoing micropipette aspiration. Biomech. Model. Mechanobiol. 10.1007/s10237-010-0197-207
28. Icard-Arcizet, D., O. Cardoso, ⋯, S. Hénon. 2008. Cell stiffening in response to external stress is correlated to actin recruitment. Biophys. J. 94:2906-2913.
29. Smith, B. A., B. Tolloczko,., P. Grütter. 2005. Probing the viscoelastic behavior of cultured airway smooth muscle cells with atomic force microscopy: Stiffening induced by contractile agonist. Biophys. J. 88:2994-3007.
30. Roca-Cusachs, P., I. Almendros, ⋯, D. Navajas. 2006. Rheology of passive and adhesion-activated neutrophils probed by atomic force microscopy. Biophys. J. 91:3508-3518.
31. Hemmer, J. D., J. Nagatomi,., M. Laberge. 2009. Role of cytoskeletal components in stress-relaxation behavior of adherent vascular smooth muscle cells. J. Biomech. Eng. 131:041001.
32. Sunyer, R., X. Trepat, ⋯, D. Navajas. 2009. The temperature dependence of cell mechanics measured by atomic force microscopy. Phys. Biol. 6:025009.
33. Hiratsuka, S., Y. Mizutani,., T. Okajima. 2009. The number distribution of complex shear modulus of single cells measured by atomic force microscopy. Ultramicroscopy. 109:937-941.
34. Wottawah, F., S. Schinkinger, ⋯, J. Käs. 2005. Optical rheology of biological cells. Phys. Rev. Lett. 94:098103.
35. Wottawah, F., S. Schinkinger, ⋯, J. Guck. 2005. Characterizing single suspended cells by optorheology. Acta Biomater. 1:263-271.
36. Lee, S., A. Zeiger,., I. M. Herman. 2010. Pericyte actomyosin-mediated contraction at the cell-material interface can modulate the microvascular niche. J. Phys. Condens. Matter. 22:194115.
37. Pal, R., M. Hanwate, ⋯, S. Totey. 2009. Phenotypic and functional comparison of optimum culture conditions for upscaling of bone marrow-derived mesenchymal stem cells. J. Tissue Eng. Regen. Med. 3:163-174.
38. Wagner, W., P. Horn, ⋯, A. D. Ho. 2008. Replicative senescence of mesenchymal stem cells: A continuous and organized process. PLoS ONE. 3:e2213.
39. Sekiya, I., B. L. Larson, ⋯, D. J. Prockop. 2002. Expansion of human adult stem cells from bone marrow stroma: Conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells. 20:530-541.
40. Docheva, D., D. Padula, ⋯, M. Schieker. 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.
41. Digirolamo, C. M., D. Stokes,., D. J. Prockop. 1999. Propagation and senescence of human marrow stromal cells in culture: A simple colonyforming assay identifies samples with the greatest potential to propagate and differentiate. Br. J. Haematol. 107:275-281.
42. Darling, E. M., M. Topel,., F. Guilak. 2008. Viscoelastic properties of human mesenchymally-derived stem cells and primary osteoblasts, chondrocytes, and adipocytes. J. Biomech. 41:454-464.
43. Lautenschläger, F., S. Paschke, ⋯, J. Guck. 2009. The regulatory role of cell mechanics for migration of differentiating myeloid cells. Proc. Natl. Acad. Sci. USA. 106:15696-15701.
44. Erickson, C. A., and J. P. Trinkaus. 1976. Microvilli and blebs as sources of reserve surface membrane during cell spreading. Exp. Cell Res. 99:375-384.
45. Rovensky, Y. A., and J. M. Vasiliev. 1984. Surface topography of suspended tissue cells. Int. Rev. Cytol. 90:273-307.
46. Bursac, P., G. Lenormand,., J. J. Fredberg. 2005. Cytoskeletal remodeling and slow dynamics in the living cell. Nat. Mater. 4:557-561.
47. Pullarkat, P. A., P. A. Fernández, and A. Ott. 2007. Rheological properties of the eukaryotic cell cytoskeleton. Phys. Rep. 449:29-53.
48. Hoffman, B. D., and J. C. Crocker. 2009. Cell mechanics: Dissecting the physical responses of cells to force. Annu. Rev. Biomed. Eng. 11: 259-288.
49. Dahl, K. N., A. J. Engler,., D. E. Discher. 2005. Power-law rheology of isolated nuclei with deformation mapping of nuclear substructures. Biophys. J. 89:2855-2864.
50. Kollmannsberger, P. 2009. Nonlinear microrheology of living cells. PhD thesis. University of Erlangen-Nürnberg, Germany.
51. Stamenovic, D., B. Suki, ⋯, J. J. Fredberg. 2004. Rheology of airway smooth muscle cells is associated with cytoskeletal contractile stress. J. Appl. Physiol. 96:1600-1605.
52. Ludwig, T., R. Kirmse, ⋯, U. S. Schwarz. 2008. Probing cellular microenvironments and tissue remodeling by atomic force microscopy. Pflugers Arch. 456:29-49.