Regulation of cell cytoskeleton and membrane mechanics by electric field: Role of linker proteins

Biophysical Journal

Volumn 96, Issue 2, 2009, Pages 717-728

  Titushkin, Igor ^a   Cho, Michael ^a  

^a University of Illinois at Chicago   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 58849087168     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.09.035     Document Type: Article

References (63)

1. Boscolo, P., M. Di Gioacchino, L. Di Giampaolo, A. Antonucci, and S. Di Luzio. 2007. Combined effects of electromagnetic fields on immune and nervous responses. Int. J. Immunopathol. Pharmacol. 20:59-63.
2. Mycielska, M. E., and M. B. Djamgoz. 2004. Cellular mechanisms of direct-current electric field effects: galvanotaxis and metastatic disease. J. Cell Sci. 117:1631-1639.
3. Song, B., M. Zhao, J. Forrester, and C. McCaig. 2004. Nerve regeneration and wound healing are stimulated and directed by an endogenous electrical field in vivo. J. Cell Sci. 117:4681-4690.
4. Hotary, K. B., and K. R. Robinson. 1994. Endogenous electrical currents and voltage gradients in Xenopus embryos and the consequences of their disruption. Dev. Biol. 166:789-800.
5. Revest, P. A., H. C. Jones, and N. J. Abbott. 1994. Transendothelial electrical potential across pial vessels in anesthetized rats: a study of ion permeability and transport at the blood-brain barrier. Brain Res. 652:76-82.
6. Nuccitelli, R. 2003. A role for endogenous electric fields in wound healing. Curr. Top. Dev. Biol. 58:1-26.
7. Cho, M. R., H. S. Thatte, R. C. Lee, and D. E. Golan. 1996. Reorganization of microfilament structure induced by ac electric fields. FASEB J. 10:1552-1558.
8. Li, X., and J. Kolega. 2002. Effects of direct current electric fields on cell migration and actin filament distribution in bovine vascular endothelial cells. J. Vasc Res. 39:391-404.
9. Cho, M. R., H. S. Thatte, R. C. Lee, and D. E. Golan. 1994. Induced redistribution of cell surface receptors by alternating current electric fields. FASEB J. 8:771-776.
10. Zhao, M., A. Dick, J. V. Forrester, and C. D. McCaig. 1999. Electric field-directed cell motility involves up-regulated expression and asymmetric redistribution of the epidermal growth factor receptors and is enhanced by fibronectin and laminin. Mol. Biol. Cell. 10:1259-1276.
11. Cho, M. R., H. S. Thatte, M. T. Silvia, and D. E. Golan. 1999. Transmembrane calcium influx induced by ac electric fields. FASEB J. 13:677-683.
12. Khatib, L., D. E. Golan, and M. Cho. 2004. Physiologic electrical stimulation provokes intracellular calcium increase mediated by phospholipase C activation in human osteoblasts. FASEB J. 18:1903-1905.
13. Titushkin, I. A., V. S. Rao, and M. R. Cho. 2004. Mode- and cell-type dependent calcium responses induced by electrical stimulus. IEEE Trans. Plasma Sci. IEEE Nucl. Plasma Sci. Soc. 32:1614-1619.
14. Sun, S., I. Titushkin, and M. Cho. 2006. Regulation of mesenchymal stem cell adhesion and orientation in 3D collagen scaffold by electrical stimulus. Bioelectrochemistry. 69:133-141.
15. Wang, E., M. Zhao, J. V. Forrester, and C. D. McCaig. 2003. Bi-directional migration of lens epithelial cells in a physiological electrical field. Exp. Eye Res. 76:29-37.
16. McCaig, C. D., L. Sangster, and R. Stewart. 2000. Neurotrophins enhance electric field-directed growth cone guidance and directed nerve branching. Dev. Dyn. 217:299-308.
17. Sauer, H., G. Rahimi, J. Hescheler, and M. Wartenberg. 1999. Effects of electrical fields on cardiomyocyte differentiation of embryonic stem cells. J. Cell. Biochem. 75:710-723.
18. Sun, S., Y. Liu, S. Lipsky, and M. Cho. 2007. Physical manipulation of calcium oscillations facilitates osteodifferentiation of human mesen-chymal stem cells. FASEB J. 21:1472-1480.
19. Bai, H., C. D. McCaig, J. V. Forrester, and M. Zhao. 2004. DC electric fields induce distinct preangiogenic responses in microvascular and macrovascular cells. Arterioscler. Thromb. Vasc. Biol. 24:1234-1239.
20. Zhao, M., H. Bai, E. Wang, J. V. Forrester, and C. D. McCaig. 2004. Electrical stimulation directly induces pre-angiogenic responses in vascular endothelial cells by signaling through VEGF receptors. J. Cell Sci. 117:397-405.
21. Ciombor, D. M., and R. K. Aaron. 2005. The role of electrical stimulation in bone repair. Foot Ankle Clin. 10:579-593.
22. Gordon, G. A. 2007. Designed electromagnetic pulsed therapy: clinical applications. J. Cell. Physiol. 212:579-582.
23. Janigro, D., C. Perju, V. Fazio, K. Hallene, G. Dini, et al. 2006. Alternating current electrical stimulation enhanced chemotherapy: a novel strategy to bypass multidrug resistance in tumor cells. BMC Cancer. 6::72.
24. Markov, M. S. 2007. Expanding use of pulsed electromagnetic field therapies. Electromagn. Biol. Med. 26:257-274.
25. Sisken, B. F., J. Walker, and M. Orgel. 1993. Prospects on clinical applications of electrical stimulation for nerve regeneration. J. Cell. Biochem. 51:404-409.
26. Lee, R. C., D. J. Canaday, and H. Doong. 1993. A review of the biophysical basis for the clinical application of electric fields in soft-tissue repair. J. Burn Care Rehabil. 14:319-335.
27. McCaig, C. D., A. M. Rajnicek, B. Song, and M. Zhao. 2005. Controlling cell behavior electrically: current views and future potential. Physiol. Rev. 85:943-978.
28. Huang, H., R. D. Kamm, and R. T. Lee. 2004. Cell mechanics and me-chanotransduction: pathways, probes, and physiology. Am. J. Physiol. Cell Physiol. 287:C1-C11.
29. Janmey, P. A., and C. A. McCulloch. 2007. Cell mechanics: integrating cell responses to mechanical stimuli. Annu. Rev. Biomed. Eng. 9:1-34.
30. Lim, C. T., E. H. Zhou, and S. T. Quek. 2006. Mechanical models for living cells-a review. J. Biomech. 39:195-216.
31. Ingber, D. E. 2006. Cellular mechanotransduction: putting all the pieces together again. FASEB J. 20:811-827.
32. Orr, A. W., B. P. Helmke, B. R. Blackman, and M. A. Schwartz. 2006. Mechanisms of mechanotransduction. Dev. Cell. 10:11-20.
33. Wang, J. H., B. P. Thampatty, J. S. Lin, and H. J. Im. 2007. Mechanor-egulation of gene expression in fibroblasts. Gene. 391:1-15.
34. Jena, B. P. 2007. Secretion machinery at the cell plasma membrane. Curr. Opin. Struct. Biol. 17:437-443.
35. Morris, C. E., and U. Homann. 2001. Cell surface area regulation and membrane tension. J. Membr. Biol. 179:79-102.
36. Raucher, D., and M. P. Sheetz. 1999. Characteristics of a -membrane reservoir buffering membrane tension. Biophys. J. 77: 1992-2002.
37. Sun, M., N. Northup, F. Marga, T. Huber, F. J. Byfield, et al. 2007. The effect of cellular cholesterol on membrane-cytoskeleton adhesion. J. Cell Sci. 120:2223-2231.
38. Sheetz, M. P., J. E. Sable, and H. G. Dobereiner. 2006. Continuous membrane-cytoskeleton adhesion requires continuous accommodation to lipid and cytoskeleton dynamics. Annu. Rev. Biophys. Biomol. Struct. 35:417-434.
39. Titushkin, I., and M. Cho. 2006. Distinct membrane mechanical properties of human mesenchymal stem cells determined using laser optical tweezers. Biophys. J. 90:2582-2591.
40. Shieh, A. C., and K. A. Athanasiou. 2003. Principles of cell mechanics for cartilage tissue engineering. Ann. Biomed. Eng. 31:1-11.
41. Titushkin, I., and M. Cho. 2007. Modulation of cellular mechanics during osteogenic differentiation of human mesenchymal stem cells. Biophys. J. 93:3693-3702.
42. Hutter, J. L., and J. Bechhoefer. 1993. Calibration of atomic-force microscope tips. Rev. Sci. Instrum. 64:1868-1873.
43. Reference deleted in proof.
44. Radmacher, M. 2002. Measuring the elastic properties of living cells by the atomic force microscope. Methods Cell Biol. 68:67-90.
45. Neuman, K. C., and S. M. Block. 2004. Optical trapping. Rev. Sci. Instrum. 75:2787-2809.
46. Coates, T. D., R. G. Watts, R. Hartman, and T. H. Howard. 1992. Relationship of F-actin distribution to development of polar shape in human polymorphonuclear neutrophils. J. Cell Biol. 117:765-774.
47. Sauer, H., R. Stanelle, J. Hescheler, and M. Wartenberg. 2002. The DCelectrical-field-induced Ca(2+) response and growth stimulation of multicellular tumor spheroids are mediated by ATP release and purinergic receptor stimulation. J. Cell Sci. 115:3265-3273.
48. Trickey, W. R., T. P. Vail, and F. Guilak. 2004. The role of the cytoskeleton in the viscoelastic properties of human articular chondrocytes. J. Orthop. Res. 22:131-139.
49. Chen, H., I. Titushkin, M. Stroscio, and M. Cho. 2007. Altered membrane dynamics of quantum dot-conjugated integrins during osteogenic differentiation of human bone marrow derived progenitor cells. Biophys. J. 92:1399-1408.
50. Seegers, J. C., M. L. Lottering, A. M. Joubert, F. Joubert, A. Koorts, et al. 2002. A pulsed DC electric field affects P2-purinergic receptor functions by altering the ATP levels in in vitro and in vivo systems. Med. Hypotheses. 58:171-176.
51. Fiévet, B., D. Louvard, and M. Arpin. 2007. ERM proteins in epithelial cell organization and functions. Biochim. Biophys. Acta.1773:653-660.
52. Louvet-Vallée, S. 2000. ERM proteins: from cellular architecture to cell signaling. Biol. Cell. 92:305-316.
53. Mangeat, P., C. Roy, and M. Martin. 1999. ERM proteins in cell adhesion and membrane dynamics. Trends Cell Biol. 9:187-192.
54. Poo, M. 1981. In situ electrophoresis of membrane components. Annu. Rev. Biophys. Bioeng. 10:245-276.
55. Cho, M. R. 2002. A review of electrocoupling mechanisms mediating facilitated wound healing. IEEE Trans. Plasma Sci. IEEE Nucl. Plasma Sci. Soc. 30:1504-1515.
56. dos Remedios, C. G., D. Chhabra, M. Kekic, I. V. Dedova, M. Tsuba-kihara, et al. 2003. Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol. Rev. 83:433-473.
57. Paavilainen, V. O., E. Bertling, S. Falck, and P. Lappalainen. 2004.Regulation of cytoskeletal dynamics by actin-monomer-binding proteins. Trends Cell Biol. 14:386-394.
58. Chen, J., and M. C. Wagner. 2001. Altered membrane-cytoskeleton linkage and membrane blebbing in energy-depleted renal proximal tubular cells. Am. J. Physiol. Renal Physiol. 280:F619-F627.
59. Katsuragi, T., T. Tokunaga, M. Ohba, C. Sato, and T. Furukawa. 1993. Implication of ATP released from atrial, but not papillary, muscle segments of guinea pig by isoproterenol and forskolin. Life Sci. 53:961-967.
60. Wang, Y., R. Roman, S. D. Lidofsky, and J. G. Fitz. 1996. Autocrine signaling through ATP release represents a novel mechanism for cell volume regulation. Proc. Natl. Acad. Sci. USA. 93:12020-12025.
61. Kawano, S., K. Otsu, A. Kuruma, S. Shoji, E. Yanagida, et al. 2006. ATP autocrine/paracrine signaling induces calcium oscillations and NFAT activation in human mesenchymal stem cells. Cell Calcium. 39:313-324.
62. Wojtczak, L. 1996. The Crabtree effect: a new look at the old problem. Acta Biochim. Pol. 43:361-368.
63. Dai, J., M. P. Sheetz, X. Wan, and C. E. Morris. 1998. Membrane tension in swelling and shrinking molluscan neurons. J. Neurosci. 18:6681-6692.