Over-expression of alpha-actinin with a GFP fusion protein is sufficient to increase whole-cell stiffness in human osteoblasts

Annals of Biomedical Engineering

Volumn 36, Issue 10, 2008, Pages 1605-1614

  Jackson, Wesley M ^a,b   Jaasma, Michael J ^a   Baik, Andrew D ^a   Keaveny, Tony M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

AFM; Crosslinking; Cytoskeleton; hFOB; Mechanical behavior

Indexed keywords

COMPUTER NETWORKS; CYTOLOGY; FUSION REACTIONS; MECHANICAL ENGINEERING; OSTEOBLASTS; PRESSURE EFFECTS; STIFFNESS;

AFM; CROSSLINKING; CYTOSKELETON; HFOB; MECHANICAL BEHAVIOR;

ACTINIDES;

ACTININ; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; BIOSYNTHESIS; CELL CULTURE; CYTOSKELETON; ELASTICITY; GENE EXPRESSION; GENETIC TRANSFECTION; GENETICS; HUMAN; MECHANICAL STRESS; OSTEOBLAST; PHYSIOLOGY; PLASMID; SHEAR STRENGTH; ULTRASTRUCTURE; UPREGULATION;

ACTININ; CELLS, CULTURED; CYTOSKELETON; ELASTICITY; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; HUMANS; MICROSCOPY, ATOMIC FORCE; OSTEOBLASTS; PLASMIDS; RECOMBINANT FUSION PROTEINS; SHEAR STRENGTH; STRESS, MECHANICAL; TRANSFECTION; UP-REGULATION;

EID: 51549094739     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-008-9533-9     Document Type: Article

References (59)

1. Bell, P. B., Jr. The application of scanning electron microscopy to the study of the cytoskeleton of cells in culture. Scan. Electron Microsc. 139-157, 1981.
2. Blanchard A., V. Ohanian, D. Critchley. The structure and function of alpha-actinin. J Muscle Res Cell Motil 10: 280-289, 1989
3. Broers J. L., E. A. Peeters, H. J. Kuijpers, J. Endert, C. V. Bouten, C. W. Oomens, F. P. Baaijens, F. C. Ramaekers. Decreased mechanical stiffness in lmna-/- cells is caused by defective nucleo-cytoskeletal integrity: Implications for the development of laminopathies. Hum Mol Genet 13: 2567-2580, 2004
4. Butt D. B., M. Jaschke. Calculation of thermal noise in atomic force microscopy. Nanotechnology 6: 1-6, 1995
5. Carvalho R. S., J. E. Scott, D. M. Suga, E. H. Yen. Stimulation of signal transduction pathways in osteoblasts by mechanical strain potentiated by parathyroid hormone. J Bone Miner Res 9: 999-1011, 1994
6. Charras G. T., M. A. Horton. Determination of cellular strains by combined atomic force microscopy and finite element modeling. Biophys J 83: 858-879, 2002
7. Charras G. T., M. A. Horton. Single cell mechanotransduction and its modulation analyzed by atomic force microscope indentation. Biophys J 82: 2970-2981, 2002
8. Charras G. T., P. P. Lehenkari, M. A. Horton. Atomic force microscopy can be used to mechanically stimulate osteoblasts and evaluate cellular strain distributions. Ultramicroscopy 86: 85-95, 2001
9. Costa K. D., F. C. Yin. Analysis of indentation: Implications for measuring mechanical properties with atomic force microscopy. J Biomech Eng 121: 462-471, 1999
10. Discher D. E., P. Janmey, Y. L. Wang. Tissue cells feel and respond to the stiffness of their substrate. Science 310: 1139-1143, 2005
11. Edlund M., M. A. Lotano, C. A. Otey. Dynamics of alpha-actinin in focal adhesions and stress fibers visualized with alpha-actinin-green fluorescent protein. Cell Motil Cytoskeleton 48: 190-200, 2001
12. Forgacs G., S. H. Yook, P. A. Janmey, H. Jeong, C. G. Burd. Role of the cytoskeleton in signaling networks. J Cell Sci 117: 2769-2775, 2004
13. Fraley T. S., C. B. Pereira, T. C. Tran, C. Singleton, J. A. Greenwood. Phosphoinositide binding regulates alpha-actinin dynamics: Mechanism for modulating cytoskeletal remodeling. J Biol Chem 280: 15479-15482, 2005
14. Freshney R. I. Culture of animal cells. New York: Wiley-Liss, 2000
15. Frost H. M. Does bone design intend to minimize fatigue failures? A case for the affirmative. J Bone Miner Metab 18: 278-282, 2000
16. Gardel M. L., J. H. Shin, F. C. MacKintosh, L. Mahadevan, P. Matsudaira, D. A. Weitz. Elastic behavior of cross-linked and bundled actin networks. Science 304: 1301-1305, 2004
17. Glogauer M., P. Arora, G. Yao, I. Sokholov, J. Ferrier, C. McCulloch. Calcium ions and tyrosine phosphorylation interact coordinately with actin to regulate cytoprotective responses to stretching. J Cell Sci 110: 11-21, 1997
18. Goldmann W. H., R. Galneder, M. Ludwig, W. Xu, E. D. Adamson, N. Wang, R. M. Ezzell. Differences in elasticity of vinculin-deficient f9 cells measured by magnetometry and atomic force microscopy. Exp Cell Res 239: 235-242, 1998
19. Goldmann W. H., D. E. Ingber. Intact vinculin protein is required for control of cell shape, cell mechanics, and rac-dependent lamellipodia formation. Biochem Biophys Res Commun 290: 749-755, 2002
20. Hartwig J. H., D. J. Kwiatkowski. Actin-binding proteins. Curr Opin Cell Biol 3: 87-97, 1991
21. Heidemann S. R., D. Wirtz. Towards a regional approach to cell mechanics. Trends Cell Biol 14: 160-166, 2004
22. Hutter, J. L. and J. Bechhoefer. Calibration of atomic-force microscope tips. Rev. Sci. Instrum. 64:1868-1873, 1993
23. Ingber D. E. Cellular tensegrity: Defining new rules of biological design that govern the cytoskeleton. J Cell Sci 104: 613-627, 1993
24. Ingber D. E. Tensegrity ii. How structural networks influence cellular information processing networks. J Cell Sci 116: 1397-1408, 2003
25. Inoue D., S. Kido, T. Matsumoto. Transcriptional induction of fosb/deltafosb gene by mechanical stress in osteoblasts. J Biol Chem 279: 49795-49803, 2004
26. Jaasma, M. Osteoblast mechanical behavior and its adaptation to mechanical loading, Ph.D., Berkeley, UC Berkeley, 2004.
27. Jaasma M. J., W. M. Jackson, T. M. Keaveny. The effects of morphology, confluency, and phenotype on whole-cell mechanical behavior. Ann Biomed Eng 34: 759-768, 2006
28. Jaasma M. J., W. M. Jackson, T. M. Keaveny. Measurement and characterization of whole-cell mechanical behavior. Ann Biomed Eng 34: 748-758, 2006
29. Jaasma M. J., W. M. Jackson, R. Y. Tang, T. M. Keaveny. Adaptation of cellular mechanical behavior to mechanical loading for osteoblastic cells. J Biomech 40: 1938-1945, 2007
30. Jackson, W. M., M. J. Jaasma, and T. M. Keaveny. Human pre-osteoblasts respond to fluid shear by up-regulating alpha-actinin in the cytoskeleton. In: Proceedings of the Biomedical Engineering Society Annual Conference. Baltimore, MD, #1086, 2005.
31. Janmey P. A. Mechanical properties of cytoskeletal polymers. Curr Opin Cell Biol 3: 4-11, 1991
32. Janmey P. A., D. A. Weitz. Dealing with mechanics: Mechanisms of force transduction in cells. Trends Biochem Sci 29: 364-370, 2004
33. Klein-Nulend J., M. H. Helfrich, J. G. Sterck, H. MacPherson, M. Joldersma, S. H. Ralston, C. M. Semeins, E. H. Burger. Nitric oxide response to shear stress by human bone cell cultures is endothelial nitric oxide synthase dependent. Biochem Biophys Res Commun 250: 108-114, 1998
34. Knothe Tate M. L., U. Knothe, P. Niederer. Experimental elucidation of mechanical load-induced fluid flow and its potential role in bone metabolism and functional adaptation. Am J Med Sci 316: 189-195, 1998
35. Lee J. S., P. Panorchan, C. M. Hale, S. B. Khatau, T. P. Kole, Y. Tseng, D. Wirtz. Ballistic intracellular nanorheology reveals rock-hard cytoplasmic stiffening response to fluid flow. J Cell Sci 119: 1760-1768, 2006
36. Lindroth M., P. B. Bell Jr., B. A. Fredriksson, X. D. Liu. Preservation and visualization of molecular structure in detergent-extracted whole mounts of cultured cells. Microsc Res Tech 22: 130-150, 1992
37. Maciver, S. K. Microfilament organization and actin-binding proteins. In: The Cytoskeleton, edited by J. E. Hesketh and I. F. Pryme. JAI Press Inc., 1995, pp. 1-45.
38. Mahaffy R. E., C. K. Shih, F. C. MacKintosh, J. Kas. Scanning probe-based frequency-dependent microrheology of polymer gels and biological cells. Phys Rev Lett 85: 880-883, 2000
39. Malone, A., C. Anderson, P. Tummala, T. Sterns, and C. Jacobs. Are Primary Cillia Mechanosensory Organelles in Bone Cells? Chicago, IL: Trans Orthopaedic Research Society, p. 369, 2006.
40. McGarry J. G., J. Klein-Nulend, M. G. Mullender, P. J. Prendergast. A comparison of strain and fluid shear stress in stimulating bone cell responses-a computational and experimental study. Faseb J 19: 482-484, 2005
41. Mukhina S., Y. L. Wang, M. Murata-Hori. Alpha-actinin is required for tightly regulated remodeling of the actin cortical network during cytokinesis. Dev Cell 13: 554-565, 2007
42. Nauman E. A., R. L. Satcher, T. M. Keaveny, B. P. Halloran, D. D. Bikle. Osteoblasts respond to pulsatile fluid flow with short-term increases in pge(2) but no change in mineralization. J Appl Physiol 90: 1849-1854, 2001
43. Otey C. A., O. Carpen. Alpha-actinin revisited: A fresh look at an old player. Cell Motil Cytoskeleton 58: 104-111, 2004
44. Pavalko F. M., N. X. Chen, C. H. Turner, D. B. Burr, S. Atkinson, Y.-F. Hsieh, J. Qiu, R. L. Duncan. Fluid shear-induced mechanical signaling in mc3t3-e1 osteoblasts requires cytoskeleton-integrin interactions. Am J Physiol Cell Physiol 275: C1591-1601, 1998
45. Pellegrin S., H. Mellor. Actin stress fibres. J Cell Sci 120: 3491-3499, 2007
46. Pelletier O., E. Pokidysheva, L. S. Hirst, N. Bouxsein, Y. Li, C. R. Safinya. Structure of actin cross-linked with alpha-actinin: A network of bundles. Phys Rev Lett 91: 148102, 2003
47. Ponik S. M., F. M. Pavalko. Formation of focal adhesions on fibronectin promotes fluid shear stress induction of cox-2 and pge2 release in mc3t3-e1 osteoblasts. J Appl Physiol 97: 135-142, 2004
48. Rivero F., B. Koppel, B. Peracino, S. Bozzaro, F. Siegert, C. J. Weijer, M. Schleicher, R. Albrecht, A. A. Noegel. The role of the cortical cytoskeleton: F-actin crosslinking proteins protect against osmotic stress, ensure cell size, cell shape and motility, and contribute to phagocytosis and development. J Cell Sci 109 (Pt 11): 2679-2691, 1996
49. Rotsch C., M. Radmacher. Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: An atomic force microscopy study. Biophys J 78: 520-535, 2000
50. Saez A., A. Buguin, P. Silberzan, B. Ladoux. Is the mechanical activity of epithelial cells controlled by deformations or forces? Biophys J 89: L52-54, 2005
51. Sato M., G. Leimbach, W. H. Schwarz, T. D. Pollard. Mechanical properties of actin. J Biol Chem 260: 8585-8592, 1985
52. Stossel T. P., J. Condeelis, L. Cooley, J. H. Hartwig, A. Noegel, M. Schleicher, S. S. Shapiro. Filamins as integrators of cell mechanics and signalling. Nat Rev Mol Cell Biol 2: 138-145, 2001
53. Tseng Y., T. P. Kole, J. S. Lee, E. Fedorov, S. C. Almo, B. W. Schafer, D. Wirtz. How actin crosslinking and bundling proteins cooperate to generate an enhanced cell mechanical response. Biochem Biophys Res Commun 334: 183-192, 2005
54. Tseng Y., T. P. Kole, D. Wirtz. Micromechanical mapping of live cells by multiple-particle-tracking microrheology. Biophys J 83: 3162-3176, 2002
55. Tseng Y., B. W. Schafer, S. C. Almo, D. Wirtz. Functional synergy of actin filament cross-linking proteins. J Biol Chem 277: 25609-25616, 2002
56. Tseng Y., D. Wirtz. Mechanics and multiple-particle tracking microheterogeneity of {alpha}-actinin-cross-linked actin filament networks. Biophys J 81: 1643-1656, 2001
57. Wachsstock D. H., W. H. Schwartz, T. D. Pollard. Affinity of alpha-actinin for actin determines the structure and mechanical properties of actin filament gels. Biophys J 65: 205-214, 1993
58. Wang N., K. Naruse, D. Stamenovic, J. J. Fredberg, S. M. Mijailovich, I. M. Tolic-Norrelykke, T. Polte, R. Mannix, D. E. Ingber. Mechanical behavior in living cells consistent with the tensegrity model. Proc Natl Acad Sci U S A 98: 7765-7770, 2001
59. Ziros P. G., A.-P. R. Gil, T. Georgakopoulos, I. Habeos, D. Kletsas, E. K. Basdra, A. G. Papavassiliou. The bone-specific transcriptional regulator cbfa1 is a target of mechanical signals in osteoblastic cells. J Biol Chem 277: 23934-23941, 2002