Second harmonic generation reveals collagen fibril remodeling in fibroblast-populated collagen gels

Cell Structure and Function

Volumn 38, Issue 2, 2013, Pages 227-236

  Toki, Fujio ^a   Honkura, Naoki ^b   Shirakata, Yuji ^b,c   Imamura, Takeshi ^a,b,c   Higashiyama, Shigeki ^a,b   Nanba, Daisuke ^a  

^a EHIME UNIVERSITY   (Japan)

^b EHIME UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c EHIME UNIVERSITY HOSPITAL   (Japan)

Author keywords

Collagen; Collagen gel contraction; Fibroblasts; Mutiphoton microscopy; Second harmonic generation

Indexed keywords

COLLAGEN FIBRIL; COLLAGEN GEL; MYOSIN ADENOSINE TRIPHOSPHATASE; COLLAGEN; GELS;

ACTIN POLYMERIZATION; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMAGING; MULTIPHOTON MICROSCOPY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SECOND HARMONIC GENERATION IMAGING; SKIN FIBROBLAST; CELLS, CULTURED; CHEMISTRY; CYTOLOGY; EXTRACELLULAR MATRIX; FIBROBLASTS; GELS; HUMANS; METABOLISM; METHODS; MICROSCOPY, FLUORESCENCE, MULTIPHOTON;

CELLS, CULTURED; COLLAGEN; EXTRACELLULAR MATRIX; FIBROBLASTS; GELS; HUMANS; MICROSCOPY, FLUORESCENCE, MULTIPHOTON;

EID: 84888876873     PISSN: 03867196     EISSN: 13473700     Source Type: Journal    
DOI: 10.1247/csf.13017     Document Type: Article

References (42)

1. Amano, M., Nakayama, M., and Kaibuchi, K. 2010. Rho-kinase/ROCK: A key regulator of the cytoskeleton and cell polarity. Cytoskeleton (Hoboken, NJ), 67: 545-554.
2. Bell, E., Ivarsson, B., and Merrill, C. 1979. Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc. Natl. Acad. Sci. USA, 76: 1274-1278.
3. Brown, E., McKee, T., diTomaso, E., Pluen, A., Seed, B., Boucher, Y., and Jain, R.K. 2003. Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation. Nat. Med., 9: 796-800.
4. Brown, R.A. and Phillips, J.B. 2007. Cell responses to biomimetic protein scaffolds used in tissue repair and engineering. Int. Rev. Cytol., 262: 75-150.
5. Campagnola, P.J., Wei, M.D., Lewis, A., and Loew, L.M. 1999. High-resolution nonlinear optical imaging of live cells by second harmonic generation. Biophys. J., 77: 3341-3349.
6. Campagnola, P.J., Millard, A.C., Terasaki, M., Hoppe, P.E., Malone, C.J., and Mohler, W.A. 2002. Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in bio-logical tissues. Biophys. J., 82: 493-508.
7. Campagnola, P.J. and Loew, L.M. 2003. Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms. Nat. Biotechnol., 21: 1356-1360.
8. Chen, A.C., McNeilly, C., Liu, A.P., Flaim, C.J., Cuttle, L., Kendall, M., Kimble, R.M., Shimizu, H., and McMillan, J.R. 2011. Second harmonic generation and multiphoton microscopic detection of collagen without the need for species specific antibodies. Burns, 37: 1001-1009.
9. Cicchi, R., Sestini, S., De Giorgi, V., Massi, D., Lotti, T., and Pavone, F.S. 2008. Nonlinear laser imaging of skin lesions. J. Biophotonics, 1: 62-73.
10. Clark, R.A., Ghosh, K., and Tonnesen, M.G. 2007. Tissue engineering for cutaneous wounds. J. Invest. Dermatol., 127: 1018-1029.
11. Engler, A.J., Sen, S., Sweeney, H.L., and Discher, D.E. 2006. Matrix elasticity directs stem cell lineage specification. Cell, 126: 677-689.
12. Ghajar, C.M., Suresh, V., Peyton, S.R., Raub, C.B., Meyskens, F.L., Jr., George, S.C., and Putnam, A.J. 2007. A novel three-dimensional model to quantify metastatic melanoma invasion. Mol. Cancer Ther., 6: 552-561.
13. Grinnell, F. and Lamke, C.R. 1984. Reorganization of hydrated collagen lattices by human skin fibroblasts. J. Cell Sci., 66: 51-63.
14. Grinnell, F. 2000. Fibroblast-collagen-matrix contraction: growth-factor signalling and mechanical loading. Trends Cell Biol., 10: 362-365.
15. Grinnell, F. and Petroll, W.M. 2010. Cell motility and mechanics in three-dimensional collagen matrices. Annu. Rev. Cell Dev. Biol., 26: 335-361.
16. Guidry, C. and Grinnell, F. 1987. Contraction of hydrated collagen gels by fibroblasts: evidence for two mechanisms by which collagen fibrils are stabilized. Coll. Relat. Res., 6: 515-529.
17. Gurtner, G.C., Dauskardt, R.H., Wong, V.W., Bhatt, K.A., Wu, K., Vial, I.N., Padois, K., Korman, J.M., and Longaker, M.T. 2011. Improving cutaneous scar formation by controlling the mechanical environment: large animal and phase I studies. Ann. Surg., 254: 217-225.
18. Jawerth, L.M., Munster, S., Vader, D.A., Fabry, B., and Weitz, D.A. 2010. A blind spot in confocal reflection microscopy: the dependence of fiber brightness on fiber orientation in imaging biopolymer networks. Biophys. J., 98: L1-3.
19. Kim, A., Lakshman, N., and Petroll, W.M. 2006. Quantitative assessment of local collagen matrix remodeling in 3-D culture: the role of Rho kinase. Exp. Cell Res., 312: 3683-3692.
20. Konig, K. and Riemann, I. 2003. High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution. J. Biomed. Opt., 8: 432-439.
21. Kuroda, Y., Kitada, M., Wakao, S., Nishikawa, K., Tanimura, Y., Makinoshima, H., Goda, M., Akashi, H., Inutsuka, A., Niwa, A., Shigemoto, T., Nabeshima, Y., Nakahata, T., Nabeshima, Y., Fujiyoshi, Y., and Dezawa, M. 2010. Unique multipotent cells in adult human mesenchymal cell populations. Proc. Natl. Acad. Sci. USA, 107: 8639-8643.
22. Lin, S.J., Jee, S.H., Kuo, C.J., Wu, R.J., Lin, W.C., Chen, J.S., Liao, Y.H., Hsu, C.J., Tsai, T.F., Chen, Y.F., and Dong, C.Y. 2006. Discrimination of basal cell carcinoma from normal dermal stroma by quantitative multiphoton imaging. Opt. Lett., 31: 2756-2758.
23. Lutolf, M.P. and Hubbell, J.A. 2005. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat. Biotechnol., 23: 47-55.
24. MacNeil, S. 2007. Progress and opportunities for tissue-engineered skin. Nature, 445: 874-880.
25. Maekawa, M., Ishizaki, T., Boku, S., Watanabe, N., Fujita, A., Iwamatsu, A., Obinata, T., Ohashi, K., Mizuno, K., and Narumiya, S. 1999. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science, 285: 895-898.
26. Mammoto, A. and Ingber, D.E. 2009. Cytoskeletal control of growth and cell fate switching. Curr. Opin. Cell Biol., 21: 864-870.
27. Mauch, C., Hatamochi, A., Scharffetter, K., and Krieg, T. 1988. Regulation of collagen synthesis in fibroblasts within a three-dimensional collagen gel. Exp. Cell Res., 178: 493-503.
28. Nanba, D., Toki, F., Matsushita, N., Matsushita, S., Higashiyama, S., and Barrandon, Y. 2013. Actin filament dynamics impacts keratinocyte stem cell maintenance. EMBO Mol. Med., 5: 640-653.
29. Nogawa, H. and Nakanishi, Y. 1987. Mechanical aspects of the mesenchy-mal influence on epithelial branching morphogenesis of mouse salivary gland. Development, 101: 491-500.
30. Parry, D.A., Barnes, G.R., and Craig, A.S. 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.
31. Prockop, D.J. and Kivirikko, K.I. 1995. Collagens: molecular biology, diseases, and potentials for therapy. Annu. Rev. Biochem., 64: 403-434.
32. Roth, S. and Freund, I. 1979. Second harmonic generation in collagen. J. Chem. Phys., 70: 1637-1643.
33. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.Y., White, D.J., Hartenstein, V., Eliceire, K., Tomancak, P., and Cardona, A. 2012. Fiji: an open-source platform for biological-image analysis. Nat. Methods., 9: 676-682.
34. Stoller, P., Reiser, K.M., Celliers, P.M., and Rubenchik, A.M. 2002. Polarization-modulated second harmonic generation in collagen. Bio-phys. J., 82: 3330-3342.
35. Sun, Y., Chen, W.L., Lin, S.J., Jee, S.H., Chen, Y.F., Lin, L.C., So, P.T., and Dong, C.Y. 2006. Investigating mechanisms of collagen thermal denaturation by high resolution second-harmonic generation imaging. Biophys. J., 91: 2620-2625.
36. Toma, J.G., Akhavan, M., Fernandes, K.J., Barnabe-Heider, F., Sadikot, A., Kaplan, D.R., and Miller, F.D. 2001. Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat. Cell Biol., 3: 778-784.
37. Wong, C.E., Paratore, C., Dours-Zimmermann, M.T., Rochat, A., Pietri, T., Suter, U., Zimmermann, D.R., Dufour, S., Thiery, J.P., Meijer, D., Beemann, F., Barrandon, Y., and Dommer, L. 2006. Neural crest-derived cells with stem cell features can be traced back to multiple lineages in the adult skin. J. Cell Biol., 175: 1005-1015.
38. Wong, V.W., Rustad, K.C., Akaishi, S., Sorkin, M., Glotzbach, J.P., Januszyk, M., Nelson, E.R., Levi, K., Paterno, J., Vial, I.N., Kuang, A.A., Longaker, M.T., and Gurtner, G.C. 2012. Focal adhesion kinase links mechanical force to skin fibrosis via inflammatory signaling. Nat. Med., 18: 148-152.
39. Yamato, M., Adachi, E., Yamamoto, K., and Hayashi, T. 1995. Condensation of collagen fibrils to the direct vicinity of fibroblasts as a cause of gel contraction. J. Biochem., 117: 940-946.
40. Yasui, T., Tohno, Y., and Araki, T. 2004. Characterization of collagen orientation in human dermis by two-dimensional second-harmonic-generation polarimetry. J. Biomed. Opt., 9, 259-264.
41. Zaman, M.H., Trapani, L.M., Sieminski, A.L., Mackellar, D., Gong, H., Kamm, R.D., Wells, A., Lauffenburger, D.A., and Matsudaira, P. 2006. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc. Natl. Acad. Sci. USA, 103: 10889-10894.
42. Zipfel, W.R., Williams, R.M., Christie, R., Nikitin, A.Y., Hyman, B.T., and Webb, W.W. 2003. Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation. Proc. Natl. Acad. Sci. USA, 100: 7075-7080.