Interpreting second-harmonic generation images of collagen I fibrils

Biophysical Journal

Volumn 88, Issue 2, 2005, Pages 1377-1386

  Williams, Rebecca M ^a,b   Zipfel, Warren R ^a   Webb, Watt W ^a  

^a School of Operations Research and Industrial Engineering   (United States)

^b NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; FIBRILLAR COLLAGEN;

ANIMAL TISSUE; ARTICLE; IMAGING SYSTEM; IONIC STRENGTH; MATHEMATICAL ANALYSIS; MICROSCOPY; NONHUMAN; NONLINEAR SYSTEM; OPTICS; PROTEIN STRUCTURE; RAT; SECOND HARMONIC GENERATION MICROSCOPY; TISSUE STRUCTURE; ALGORITHM; ANIMAL; CHEMISTRY; COMPUTER ASSISTED DIAGNOSIS; CONFOCAL MICROSCOPY; EVALUATION; IMAGE ENHANCEMENT; IN VITRO STUDY; METABOLISM; METHODOLOGY; POLARIZATION MICROSCOPY; PROTEIN CONFORMATION; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; SPRAGUE DAWLEY RAT; TENDON; ULTRASTRUCTURE;

ALGORITHMS; ANIMALS; COLLAGEN TYPE I; FIBRILLAR COLLAGENS; IMAGE ENHANCEMENT; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MICROSCOPY, CONFOCAL; MICROSCOPY, POLARIZATION; PROTEIN CONFORMATION; RATS; RATS, SPRAGUE-DAWLEY; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; TENDONS;

EID: 21244479321     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.047308     Document Type: Article

References (50)

1. Baas, P. W., J. S. Deitch, M. M. Black, and G. A. Banker. 1988. Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc. Natl. Acad. Sci. USA. 85:8335-8339.
2. Barad, Y., H. Eisenberg, M. Horowitz, and Y. Silberberg. 1997. Nonlinear scanning laser microscopy by third harmonic generation. Appl. Phys. Lett. 70:922-924.
3. Birk, D. E., and T. F. Linsenmayer. 1994. Collagen fibril assembly, deposition, and organization into tissue-specific matrices. In Extracellular Matrix Assembly and Structure. P. D. Yurchenco, D. E. Birk, and R. P. Mecham, editors. Academic Press, San Diego, CA. 91-128.
4. Born, M., and E. Wolf. 1980. Principles of Optics. Pergamon Press, New York, NY.
5. Boyd, R. W. 1992. Nonlinear Optics. Academic Press, Boston, MA.
6. Brown, E., T. McKee, E. DiTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain. 2003. Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation. Nat. Med. 9:796-800.
7. Campagnola, P. J., A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler. 2002. Three-dimensional high-resolution second harmonic generation imaging of endogenous structural proteins in biological tissues. Biophys. J. 82:493-508.
8. Cheng, J. X., A. Volkmer, and X. S. Xie. 2002. Theoretical and experimental characterization of coherent anti-Stokes Raman scattering microscopy. J. Opt. Soc. Am. B. Opt. Phys. 19:1363-1375.
9. Craig, A. S., and D. A. Parry. 1981. Growth and development of collagen fibrils in immature tissues from rat and sheep. Proc. R. Soc. Lond. B Biol. Sci. 212:85-92.
10. Denk, W., J. H. Strickler, and W. W. Webb. 1990. Two-photon laser scanning fluorescence microscopy. Science. 248:73-76.
11. Dombeck, D. A., K. A. Kasischke, H. D. Vishwasrao, M. Ingelsson, B. T. Hyman, and W. W. Webb. 2003. Uniform polarity microtubule assemblies imaged in native brain tissue by second-harmonic generation microscopy. Proc. Natl. Acad. Sci. USA. 100:7081-7086.
12. Fine, S., and W. P. Hansen. 1971. Optical second harmonic generation in biological systems. Appl. Opt. 10:2350-2353.
13. Flesken-Nikitin, A., R. M. Williams, W. R. Zipfel, W. W. Webb, and A. Y. Nikitin. 2004. Use of multiphoton imaging for studying cell migration in the mouse. In Cell Migration: Developmental Methods and Protocols, Vol. 294. G.-L. Guan, editor. Humana Press Totona, NJ. 335-345.
14. Freund, I., and M. Deutsch. 1986. Second-harmonic microscopy of biological tissue. Opt. Lett. 11:94-96.
15. Freund, I., M. Deutsch, and A. Sprecher. 1986. Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon. Biophys. J. 50:693-712.
16. Guo, Y., H. E. Savage, F. Liu, S. P. Schantz, P. P. Ho, and R. R. Alfano. 1999. Subsurface tumor progression investigated by noninvasive optical second harmonic tomography. Proc. Natl. Acad. Sci. USA. 96:10854-10856.
17. Gutsmann, T., G. E. Fantner, M. Venturoni, A. Ekani-Nkodo, J. B. Thompson, J. H. Kindt, D. E. Morse, D. K. Fygenson, and P. K. Hansma. 2003. Evidence that collagen fibrils in tendons are inhomogeneously structured in a tubelike manner. Biophys. J. 84:2593-2598.
18. Haut, T. L., and R. C. Haut. 1997. The state of tissue hydration determines the strain-rate-sensitive stiffness of human patellar tendon. J. Biomech. 30:79-81.
19. Heino, J. 1996. Biology of tumor cell invasion: interplay of cell adhesion and matrix degradation. Int. J. Cancer. 65:717-722.
20. Heinz, T. F. 1991. Second-order nonlinear optical effects at surfaces and interlaces. In Nonlinear Surface Electromagnetic Phenomena. H-E. Ponath and G. I. Stegeman, editors. North-Holland, New York, NY. 353-416.
21. Hellwarth, R., and P. Christensen. 1974. Nonlinear optical microscopic examination of structure in polycrystalline ZnSe. Opt. Commun. 12:318-322.
22. Mulmes, D. J., T. J. Wess, D. J. Prockop, and P. Fratzl. 1995. Radial packing, order, and disorder in collagen fibrils. Biophys. J. 68:1661-1670.
23. Kobayashi, A., M. Sugisaka, K. Takehana, M. Yamaguchi, Eerdunchaolu, E. K. Iwasa, and M. Abe. 1999. Morphological and histochemical analysis of a case of superficial digital flexor tendon injury in the horse. J. Comp. Pathol. 120:403-414.
24. Larson, D. R., W. R. Zipfel, R. M. Williams, S. W. Clark, M. P. Bruchez, F. W. Wise, and W. W. Webb. 2003. Water-soluble quantum dots for multiphoton fluorescence imaging in vivo. Science. 300:1434-1436.
25. Leikin, S., D. C. Rau, and V. A. Parsegian. 1994. Direct measurement of forces between self-assembled proteins: temperature-dependent exponential forces between collagen triple helices. Proc. Natl. Acad. Sci. USA. 91:276-280.
26. Mertz, J., and L. Moreaux. 2001. Second-harmonic generation by focused excitation of inhomogeneously distributed scatterers. Opt. Commun. 196:325-330.
27. Monnier, V. M., R. R. Kohn, and A. Cerami. 1984. Accelerated age-related browning of human collagen in diabetes mellitus. Proc. Natl. Acad. Sci. USA. 81:583-587.
28. Moreaux, L., O. Sandre, and J. Mertz. 2000. Membrane imaging by second-harmonic generation microscopy. J. Opt. Soc. Am. B. 17:1685-1694.
29. Muller, M., J. Squier, K. R. Wilson, and G. J. Brakenhoff. 1998. 3D microscopy of transparent objects using third-harmonic generation. J. Microsc. 191:266-274.
30. Ouzounov, D. G., K. D. Moll, M. A. Foster, W. R. Zipfel, W. W. Webb, and A. L. Gaeta. 2002. Delivery of nanojoule femtosecond pulses through large-core microstructured fibers. Opt. Lett. 27:1513-1515.
31. Parry, D. A., G. R. Barnes, and A. S. Craig. 1978. A comparison of the size distribution of collagen fibrils in connective tissues as a function of age and a possible relation between fibril size distribution and mechanical properties. Proc. R. Soc. Lond. B Biol. Sci. 203:305-321.
32. Parry, D. A., and A. S. Craig. 1977. Quantitative electron microscope observations of the collagen fibrils in rat-tail tendon. Biopolymers. 16:1015-1031.
33. Price, R. I., S. Lees, and D. A. Kirschner. 1997. X-ray diffraction analysis of tendon collagen at ambient and cryogenic temperatures: role of hydration. Int. J. Biol. Macromol. 20:23-33.
34. Richards, B., and E. Wolf. 1959. Electromagnetic diffraction in optical systems.2. Structure of the image field in an aplanatic system. Proc. R. Soc. Lond. A. Math. Phys. Sci. 253:358-379.
35. Roth, S., and I. Freund. 1979. Second harmonic-generation in collagen. J. Chem. Phys. 70:1637-1643.
36. Roth, S., and I. Freund. 1981. Optical second-harmonic scattering in rat-tail tendon. Biopolymers. 20:1271-1290.
37. Sarkar, S. K., C. E. Sullivan, and D. A. Torchia. 1983. Solid state 13C NMR study of collagen molecular dynamics in hard and soft tissues. J. Biol. Chem. 258:9762-9767.
38. Stoller, P., B. M. Kim, A. M. Rubenchik, K. M. Reiser, and L. B. Da Silva. 2002a. Polarization-dependent optical second-harmonic imaging of a rat-tail tendon. J. Biomed. Opt. 7:205-214.
39. Stoller, P., K. M. Reiser, P. M. Celliers, and A. M. Rubenchik. 2002b. Polarization-modulated second harmonic generation in collagen. Biophys. J. 82:3330-3342.
40. Svendsen, K. H., and M. H. Koch. 1982. X-ray diffraction evidence of collagen molecular packing and cross-linking in fibrils of rat tendon observed by synchrotron radiation. EMBO J. 1:669-674.
41. Thornton, G. M., N. G. Shrive, and C. B. Frank. 2001. Altering ligament water content affects ligament pre-stress and creep behaviour. J. Orthop. Res. 19:845-851.
42. Trelstad, R. L., and K. Hayashi. 1979. Tendon collagen fibrillogenesis: intracellular subassemblies and cell surface changes associated with fibril growth. Dev. Biol. 71:228-242.
43. Volkmer, A., J. X. Cheng, and X. S. Xie. 2001. Vibrational imaging with high sensitivity via epidetected coherent anti-Stokes Raman scaitering microscopy. Phys. Rev. Lett. 8702:023901.
44. Wang, W., J. B. Wyckoff, V. C. Frohlich, Y. Oleynikov, S. Huttelmaier, J. Zavadil, L. Cermak, E. P. Bottinger, R. H. Singer, J. G. White, J. E. Segall, and J. S. Condeelis. 2002. Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling. Cancer Res. 62:6278-6288.
45. Willens, A., J. E. Rice, D. M. Burland, and D. P. Shelton. 1992. Problems in the comparison of theoretical and experimental hyperpolarizabilities. J. Chem. Phys. 97:7590-7599.
46. Williams, R. M., J. B. Shear, W. R. Zipfel, S. Maiti, and W. W. Webb. 1999. Mucosal mast cell secretion processes imaged using three-photon microscopy of 5-hydroxytryptamine autofluorescence. Biophys. J. 76:1835-1846.
47. Williams, R. M., W. R. Zipfel, and W. W. Webb. 2001. Multiphoton microscopy in biological research. Curr. Opin. Chem. Biol. 5:603-608.
48. Woodhead-Galloway, J. 1980. Structure of the collagen fibril: some variations on a theme of tetragonally packed dimers. Proc. R. Soc. Lond. B. Biol. Sci. 209:275-297.
49. Zipfel, W. R., R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb. 2003a. Live tissue intrinsic emission microscopy using multiphoton excited intrinsic fluorescence and second harmonic generation. Proc. Natl. Acad. Sci. USA. 100:7075-7080.
50. Zipfel, W. R., R. M. Williams, arid W. W. Webb. 2003b. Nonlinear magic: multiphoton microscopy in the biosciences. Nat. Biotechnol. 21:1369-1377.