Integrated multimodal microscopy, time-resolved fluorescence, and optical-trap rheometry: Toward single molecule mechanobiology

Journal of Biomedical Optics

Volumn 12, Issue 1, 2007, Pages

  Gullapalli, Ramachandra R ^a   Tabouillot, Tristan ^a   Mathura, Rishi ^b   Dangaria, Jhanvi H ^a   Butler, Peter J ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b City University of New York   (United States)

Author keywords

Endothelial cell; Fluorescence correlation spectroscopy; Mechanotransduction; Membrane; Time correlated single photon counting; Total internal reflection fluorescence

Indexed keywords

ARTICLE; BIOLOGY; BIOMECHANICS; CELL SEPARATION; CONFOCAL MICROSCOPY; EQUIPMENT; EQUIPMENT DESIGN; EVALUATION; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; INSTRUMENTATION; METHODOLOGY; MICROFLUIDIC ANALYSIS; MOLECULAR BIOLOGY; OPTICAL TWEEZERS; SYSTEM ANALYSIS;

BIOLOGY; BIOMECHANICS; CELL SEPARATION; EQUIPMENT DESIGN; EQUIPMENT FAILURE ANALYSIS; FLOW CYTOMETRY; MICROFLUIDIC ANALYTICAL TECHNIQUES; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MOLECULAR BIOLOGY; OPTICAL TWEEZERS; SYSTEMS INTEGRATION;

BIOCHEMISTRY; CELL MEMBRANES; COMPUTER SIMULATION; CONFOCAL MICROSCOPY; DECONVOLUTION; FLUORESCENCE SPECTROSCOPY; MOLECULAR DYNAMICS; SINGLE PHOTON EMISSION COMPUTED TOMOGRAPHY;

CONFOCAL MOLECULAR DYNAMICS MICROSCOPE; DIFFERENTIAL INTERFERENCE CONTRAST; TIME-CORRELATED SINGLE-PHOTON COUNTING; TOTAL-INTERNAL-REFLECTION FLUORESCENCE;

MEDICAL IMAGING;

EID: 34247581295     PISSN: 10833668     EISSN: 15602281     Source Type: Journal    
DOI: 10.1117/1.2673245     Document Type: Article

References (53)

1. A. W. Orr, B. P. Helmke, B. R. Blackman, and M. A. Schwartz, " Mechanisms of mechanotransduction," Dev. Cell 10, 11-20 (2006). (Pubitemid 43025673)
2. D. E. Ingber, " Mechanobiology and diseases of mechanotransduction, " Ann. Med. 35, 564-577 (2003). (Pubitemid 38005314)
3. P. F. Davies, " Overview: temporal and spatial relationships in shear stress-mediated endothelial signalling," J. Vasc. Res. 34, 208-211 (1997). (Pubitemid 27281695)
4. K. A. Barbee, T. Mundel, R. Lal, and P. F. Davies, " Subcellular distribution of shear stress at the surface of flow-aligned and non-aligned endothelial monolayers," Am. J. Physiol. 268, H1765-H1772 (1995).
5. A. B. Mathur, G. A. Truskey, and W. M. Reichert, " Atomic force and total internal reflection fluorescence microscopy for the study of force transmission in endothelial cells," Biophys. J. 78, 1725-1735 (2000). (Pubitemid 30183571)
6. A. Trache and G. A. Meininger, " Atomic force-multi-optical imaging integrated microscope for monitoring molecular dynamics in live cells," J. Biomed. Opt. 10, 064023(1-17)(2005).
7. Y. Wang, E. L. Botvinick, Y. Zhao, M. W. Berns, S. Usami, R. Y. Tsien, and S. Chien, " Visualizing the mechanical activation of Src," Nature (London) 434, 1040-1045 (2005). (Pubitemid 40586054)
8. H. Huang, C. Y. Dong, H. S. Kwon, J. D. Sutin, R. D. Kamm, and P. T. So, " Three-dimensional cellular deformation analysis with a two-photon magnetic manipulator workstation," Biophys. J. 82, 22112223 (2002).
9. G. T. Charras and M. A. Horton, " Determination of cellular strains by combined atomic force microscopy and finite element modeling," Biophys. J. 83, 858-879 (2002). (Pubitemid 34803622)
10. M. C. Ferko, B. P. Patterson, and P. J. Butler, " High-resolution solid modeling of biological samples imaged with 3-D fluorescence microscopy," Microsc. Res. Tech. 69(8), 648-655 (2006). (Pubitemid 44290002)
11. E. A. Osborn, A. Rabodzey, C. F. Dewey, Jr., and J. H. Hartwig, " Endothelial actin cytoskeleton remodeling during mechanostimula-tion with fluid shear stress," Am. J. Physiol.: Cell Physiol. 290, C444-C452 (2006).
12. C. Sultan, D. Stamenovic, and D. E. Ingber, " A computational tensegrity model predicts dynamic rheological behaviors in living cells," Ann. Biomed. Eng. 32, 520-530 (2004).
13. N. Wang and Z. Suo, " Long-distance propagation of forces in a cell," Biochem. Biophys. Res. Commun. 328, 1133-1138 (2005). (Pubitemid 40238752)
14. R. V. Geiger, B. C. Berk, R. W. Alexander, and R. M. Nerem, " Flow-induced calcium transients in single endothelial cells: spatial and temporal analysis," Am. J. Physiol. 262, C1411-C1417 (1992).
15. I. Levitan, A. E. Christian, T. N. Tulenko, and G. H. Rothblat, " Membrane cholesterol content modulates activation of volume-regulated anion current in bovine endothelial cells," J. Genet. Physiol. 115, 405-416 (2000). (Pubitemid 30196589)
16. S. Li, M. Kim, Y. L. Hu, S. Jalali, D. D. Schlaepfer, T. Hunter, S. Chien, and J. Y. Shyy, " Fluid shear stress activation of focal adhesion kinase. Linking to mitogen-activated protein kinases," J. Biol. Chem. 272, 30455-30462 (1997). (Pubitemid 27512256)
17. S. M. McCormick, S. G. Eskin, L. V. McIntire, C. L. Teng, C. M. Lu, G. Russell, and K. K. Chittur, " DNA microarray reveals changes in gene expression of shear stressed human umbilical vein endothelial cells," Proc. Natl. Acad. Sci. U.S.A. 98, 8955-8960 (2001). (Pubitemid 32743851)
18. S. T. Hess, S. Huang, A. A. Heikal, and W. W. Webb, " Biological and chemical applications of fluorescence correlation spectroscopy: a review," Biochemistry 41, 697-705 (2002). (Pubitemid 34065283)
19. V. Vukojevic, A. Pramanik, T. Yakovleva, R. Rigler, L. Terenius, and G. Bakalkin, " Study of molecular events in cells by fluorescence correlation spectroscopy," Cell. Mol. Life Sci. 62, 535-550 (2005). (Pubitemid 40392450)
20. E. Haustein and P. Schwille, " Ultrasensitive investigations of biological systems by fluorescence correlation spectroscopy," Methods 29, 153-166 (2003). (Pubitemid 36269202)
21. E. Elson and D. Magde, " Fluorescence correlation spectroscopy. I. Conceptual basis and theory," Biopolymers 13, 1-27 (1974).
22. D. Magde, E. Elson, and W. W. Webb, " Fluorescence correlation spectroscopy. II. An experimental realization," Biopolymers 13, 29-61 (1974).
23. C. Zander, J. Enderlein, and R. A. Keller, Single-Molecule Detection in Solution Methods and Applications, Wiley, Berlin (2002).
24. P. Schwille, J. Korlach, and W. W. Webb, " Fluorescence correlation spectroscopy with single-molecule sensitivity on cell and model membranes," Cytometry 36, 176-182 (1999). (Pubitemid 29291466)
25. J. R. Lakowicz, Principles of Fluorescence Spectroscopy, 2nd ed., Springer, New York (1999).
26. K. C. Neuman and S. M. Block, " Optical trapping," Rev. Sci. Instrum. 75, 2787-2809 (2004).
27. M. Yanai, J. P. Butler, T. Suzuki, H. Sasaki, and H. Higuchi, " Regional rheological differences in locomoting neutrophils," Am. J. Physiol.: Cell Physiol. 287, C603-C611 (2004). (Pubitemid 39095846)
28. R. M. Simmons, J. T. Finer, S. Chu, and J. A. Spudich, " Quantitative measurements of force and displacement using an optical trap," Bio-phys. J. 70, 1813-1822 (1996). (Pubitemid 26103954)
29. L. A. Hough and H. D. Ou-Yang, " A new probe for mechanical testing of nanostructures in soft materials," J. Nanopart. Res. 1, 495499 (1999).
30. W. H. Guilford, D. E. Dupuis, G. Kennedy, J. Wu, J. B. Patlak, and M. Warshaw, " Smooth muscle and skeletal muscle myosins produce similar unitary forces and displacements in the laser trap," Bio-phys. J. 72, 1006-1021 (1997). (Pubitemid 27113629)
31. M. C. Ferko, M. B. Garcia, and P. J. Butler, " Finite element stress analysis of a muticomponent model of sheared and focally-adhered endothelial cells," Ann. Biomed. Eng. 35, 208-223 (2007). (Pubitemid 46122177)
32. S. T. Hess and W. W. Webb, " Focal volume optics and experimental artifacts in confocal fluorescence correlation spectroscopy," Biophys. J. 83, 2300-2317 (2002).
33. W. Becker, Advanced Time-Correlated Single Photon Counting Techniques, Springer-Verlag, Berlin (2006).
34. J. Gelles, B. J. Schnapp, and M. P. Sheetz, " Tracking kinesin-driven movements with nanometre-scale precision," Nature (London) 331, 450-453 (1988). (Pubitemid 18064370)
35. S. Yamada, D. Wirtz, and S. C. Kuo, " Mechanics of living cells measured by laser tracking microrheology," Biophys. J. 78,17361747 (2000).
36. A. Pralle, M. Prummer, E. L. Florin, E. H. K. Stelzer, and J. K. H. Horber, " Three-dimensional high-resolution particle tracking for optical tweezers by forward scattered light," Microsc. Res. Tech. 44, 378-386 (1999). (Pubitemid 29122775)
37. D. S. Dimitrov and M. I. Angelova, " Swelling and electroswelling of lipids-theory and experiment," Stud. Biophys. 113, 15-20 (1986).
38. J. Widengren, U. Mets, and R. Rigler, " Fluorescence correlation spectroscopy of triplet states in solution: a theoretical and experimental study," J. Phys. Chem. 99, 13368-13379 (1995).
39. R. F. Kubin and A. N. Fletcher, " Fluorescence quantum yields of some rhodamine dyes," J. Lumin. 27, 455-462 (1982). (Pubitemid 13505734)
40. E. Gielen, J. Vercammen, J. Sykora, J. Humpolickova, M. Vandeven, A. Benda, N. Hellings, M. Hof, Y. Engelborghs, P. Steels, and M. Ameloot, " Diffusion of sphingomyelin and myelin oligodendrocyte glycoprotein in the membrane of OLN-93 oligodendroglial cells studied by fluorescence correlation spectroscopy," C. R. Biol. 328, 10571064 (2005).
41. B. S. Packard and D. E. Wolf, " Fluorescence lifetimes of carbocya-nine lipid analogues in phospholipid bilayers," Biochemistry 24, 5176-5181 (1985).
42. V. Buschmann, K. D. Weston, and M. Sauer, " Spectroscopic study and evaluation of red-absorbing fluorescent dyes," Bioconjugate Chem. 14, 195-204 (2003). (Pubitemid 36169033)
43. W. Becker, A. Bergmann, E. Haustein, Z. Petrasek, P. Schwille, C. Biskup, L. Kelbauskas, K. Benndorf, N. Klocker, T. Anhut, I. Riemann, and K. Konig, " Fluorescence lifetime images and correlation spectra obtained by multidimensional time-correlated single photon counting," Microsc. Res. Tech. 69, 186-195 (2006).
44. M. Wahl, I. Gregor, M. Patting, and J. Enderlein, " Fast calculation of fluorescence correlation data with asynchronous time-correlated single-photon counting," Opt. Express 11, 3583-3591 (2003).
45. A. Pramanik and R. Rigler, " Ligand-receptor interactions in the membrane of cultured cells monitored by fluorescence correlation spectroscopy," Biol. Chem. 382, 371-378 (2001). (Pubitemid 32377164)
46. P. J. Butler, G. Norwich, S. Weinbaum, and S. Chien, " Shear stress induces a time- and position-dependent increase in endothelial cell membrane fluidity," Am. J. Physiol.: Cell Physiol. 280, C962-C969 (2001 ).
47. J. Korlach, P. Schwille, W. W. Webb, and G. W. Feigenson, " Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy," Proc. Natl. Acad. Sci. U.S.A. 96, 8461-8466 (1999). (Pubitemid 29354813)
48. K. Bacia, D. Scherfeld, N. Kahya, and P. Schwille, " Fluorescence correlation spectroscopy relates rafts in model and native membranes," Biophys. J. 87, 1034-1043 (2004). (Pubitemid 39095082)
49. P. F. Almeida, W. L. Vaz, and T. E. Thompson, " Lateral diffusion in the liquid phases of dimyristoylphosphatidylcholine/cholesterol lipid bilayers: a free volume analysis," Biochemistry 31, 6739-6747 (1992).
50. W. L. C. Vaz, R. M. Clegg, and D. Hallmann, " Translational diffusion of lipids in liquid-crystalline phase phosphatidylcholine multibilayers-a comparison of experiment with theory," Biochemistry 24, 781-786 (1985).
51. G. J. Schutz, H. Schindler, and T. Schmidt, " Single-molecule microscopy on model membranes reveals anomalous diffusion," Biophys. J. 73, 1073-1080 (1997). (Pubitemid 27337641)
52. A. Kusumi and K. Suzuki, " Toward understanding the dynamics of membrane-raft-based molecular interactions," Biochim. Biophys. Acta 1746, 234-251 (2005). (Pubitemid 41815019)
53. J. M. Tarbell and M. Y. Pahakis, " Mechanotransduction and the gly-cocalyx," J. Intern Med. 259, 339-350 (2006).