Imaging Fibrosis and Separating Collagens using Second Harmonic Generation and Phasor Approach to Fluorescence Lifetime Imaging

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Ranjit, Suman ^a   Dvornikov, Alexander ^a   Stakic, Milka ^a   Hong, Suk Hyun ^c   Levi, Moshe ^b   Evans, Ronald M ^c   Gratton, Enrico ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; GEL;

ANIMAL; CHICKEN; FEMUR; FIBROSIS; FLUORESCENCE IMAGING; GEL; HUMAN; ISOLATION AND PURIFICATION; MOUSE; PATHOLOGY; PROCEDURES; RAT; SIGNAL PROCESSING;

ANIMALS; CHICKENS; COLLAGEN; FEMUR; FIBROSIS; GELS; HUMANS; MICE; OPTICAL IMAGING; RATS; SIGNAL PROCESSING, COMPUTER-ASSISTED;

EID: 84939785058     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13378     Document Type: Article

References (38)

1. Leask, A. & Abraham, D. J. TGF-Î2 signaling and the fibrotic response. The FASEB Journal 18, 816-827 (2004).
2. Raub, C. B. et al. Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy. Biophys. J. 92, 2212-2222 (2007).
3. Pauschinger, M. et al. Dilated cardiomyopathy is associated with significant changes in collagen type I/III ratio. Circulation 99, 2750-2756 (1999).
4. Siegel, J. et al. Studying biological tissue with fluorescence lifetime imaging: microscopy, endoscopy, and complex decay profiles. Appl. Opt. 42, 2995-3004 (2003).
5. Soufen, H. N. et al. Collagen content, but not the ratios of collagen type III/I mRNAs, differs among hypertensive, alcoholic, and idiopathic dilated cardiomyopathy. Braz. J. Med. Biol. Res. 41, 1098-1104 (2008).
6. Soylemezoglu, O. et al. Urinary and serum type III collagen: markers of renal fibrosis. Nephrol. Dial. Transplant. 12, 1883-1889 (1997).
7. Raghu, G., Masta, S., Meyers, D. & Narayanan, A. S. Collagen synthesis by normal and fibrotic human lung fibroblasts and the effect of transforming growth factor-Î2. Am. Rev. Respir. Dis. 140, 95-100 (1989).
8. Pataridis, S. et al. Identification of collagen types in tissues using HPLC-MS/MS. J. Sep. Sci. 31, 3483-3488 (2008).
9. Bailey, A. J., Sims, T. J., Le Lous, M. & Bazin, S. Collagen polymorphism in experimental granulation tissue. Biochem. Biophys. Res. Commun. 66, 1160-1165 (1975).
10. Chen, X., Nadiarynkh, O., Plotnikov, S. & Campagnola, P. J. Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure. Nat. Protocols. 7, 654-669 (2012).
11. Raub. C. R., Tromberg. B. & George. S. C. Second harmonic generation imaging, 245-270 (Taylor & Francis, 2013).
12. Ely, J. J. et al. Use of biomarkers of collagen types I and III fibrosis metabolism to detect cardiovascular and renal disease in chimpanzees (Pan troglodytes). Comp. Med. 60, 154-158 (2009).
13. Eyre, D. R., Weis, M. A. & Wu, J.-J. Advances in collagen cross-link analysis. Methods (San Diego, Calif.) 45, 65-74 (2008).
14. Becker, W. Fluorescence lifetime imaging-techniques and applications. J. Microsc. 247, 119-136 (2012).
15. Dowling, K. et al. Fluorescence lifetime imaging with picosecond resolution for biomedical applications. Opt. Lett. 23, 810-812 (1998).
16. Lutz, V. et al. Impact of collagen crosslinking on the second harmonic generation signal and the fluorescence lifetime of collagen autofluorescence. Skin. Res.Technol. 18, 168-179 (2012).
17. Zoumi, A., Yeh, A. T. & Tromberg, B. J. Imaging cells and extracellular matrix in vivo using second-harmonic generation and two-photon excited fluorescence, Proc. Natl. Acad. Sci. USA., 99, 11014-11019 (2002).
18. Phipps, J. E., Sun, Y., Fishbein, M. C. & Marcu, L. A fluorescence lifetime imaging classification method to investigate the collagen to lipid ratio in fibrous caps of atherosclerotic plaque. Lasers. Surg. Med. 44, 564-571 (2012).
19. Prabhu, V. et al. Objective assessment of endogenous collagen in vivo during tissue repair by laser induced fluorescence. PLoS One 9, e98609 1-15 (2014).
20. Zoumi, A., Yeh, A. & Tromberg, B. J. Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence. Proc. Natl. Acad. Sci. USA. 99, 11014-11019 (2002).
21. Ajeti, V. et al. Structural changes in mixed Col I/Col V collagen gels probed by SHG microscopy: implications for probing stromal alterations in human breast cancer. Biomed. Opt. Express. 2, 2307-2316 (2011).
22. Birk, D. E. et al. Collagen fibrillogenesis in vitro: interaction of types I and V collagen regulates fibril diameter. J. Cell Sci. 95, 649-657 (1990).
23. Moise, N., Carp, C. & Pascu, M.-L. Laser-induced fluorescence of collagen and cholesterol. Proc. SPIE. 2461, 386-390 (1995).
24. Zipfel, W. R. et al. Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation. Proc. Natl. Acad. Sci. USA. 100, 7075-7080 (2003).
25. Bastiaens, P. I. H. & Squire, A. Fluorescence lifetime imaging microscopy: spatial resolution of biochemical processes in the cell. Trends. Cell. Biol 9, 48-52 (1999).
26. Clayton, A. H. A., Hanley, Q. S. & Ver Veer, P. J. Graphical representation and multicomponent analysis of single-frequency fluorescence lifetime imaging microscopy data. J. Microsc. 213, 1-5 (2004).
27. Redford, G. & Clegg, R. Polar plot representation for frequency-domain analysis of fluorescence lifetimes. J. Fluoresc. 15, 805-815 (2005).
28. Caiolfa, V. R., Gratton, E. & Zamai, M. Phasor-FLIM analysis of FRET for homotypic and heterotypic non-covalent interactions: stimulated membrane receptors in live cells. EMC 2008 14th European Microscopy Congress 1â"5 September 2008, Aachen, Germany, 157-158 (Springer Berlin Heidelberg, 2008).
29. Digman, M. A., Caiolfa, V. R., Zamai, M. & Gratton, E. The phasor approach to fluorescence lifetime imaging analysis. Biophys. J. 94, L14-L16 (2008).
30. Stringari, C. et al. Metabolic trajectory of cellular differentiation in small intestine by Phasor Fluorescence Lifetime Microscopy of NADH. Scientific Reports 2, 568-1-568-9 (2012).
31. Åtefl, M., James, N. G., Ross, J. A. & Jameson, D. M. Applications of phasors to in vitro time-resolved fluorescence measurements. Anal. Biochem. 410, 62-69 (2011).
32. Hong, S.-H. et al. Rescue of a primary myelofibrosis model by retinoid-antagonist therapy. Proc. Natl. Acad. Sci. USA. 110, 18820-18825 (2013).
33. Marcu, L. et al. In vivo detection of macrophages in a rabbit atherosclerotic model by time-resolved laser-induced fluorescence spectroscopy. Atherosclerosis 181, 295-303 (2005).
34. Nofsinger, R. R. et al. SMRT repression of nuclear receptors controls the adipogenic set point and metabolic homeostasis. Proc. Natl. Acad. Sci. USA. 105, 20021-20026 (2008).
35. Crosignani, V. et al. Deep tissue fluorescence imaging and in vivo biological applications. J. Biomed. Opt. 17, 116023 (2012).
36. Crosignani, V., Dvornikov, A. S. & Gratton, E. Enhancement of imaging depth in turbid media using a wide area detector. J. Biophotonics 4, 592-599 (2011).
37. Ranjit, S. et al. Application of three-photon excitation FCS to the study of protein oligomerization. J. Phys. Chem. B 118, 14627-14631 (2014).
38. Arnesano, C., Santoro, Y. & Gratton, E. Digital parallel frequency-domain spectroscopy for tissue imaging. J. Biomed. Opt. 17, 096014 (2012).