Polarization-dependent second-harmonic generation for collagen-based differentiation of breast cancer samples.
breast cancer
collagen
diagnosis
nonlinear optical microscopy
polarization-dependent measurements
second harmonic generation imaging
Journal
Journal of biophotonics
ISSN: 1864-0648
Titre abrégé: J Biophotonics
Pays: Germany
ID NLM: 101318567
Informations de publication
Date de publication:
10 2020
10 2020
Historique:
received:
08
05
2020
revised:
29
06
2020
accepted:
06
07
2020
pubmed:
10
7
2020
medline:
29
5
2021
entrez:
10
7
2020
Statut:
ppublish
Résumé
Nonlinear optical imaging techniques have been widely used to reveal biological structures for accurate diagnosis at the cellular as well as the tissue level. In the present study, polarization-dependent second-harmonic generation (PSHG) was used to determine collagen orientation in breast cancer biopsy tissues (grades 0, I, II and III). The obtained data were processed using fast Fourier transform (FFT) analysis, while second-harmonic generation (SHG) anisotropy and the "ratio parameter" values were also calculated. Such measurements were shown to be able to distinguish collagen structure modifications in different cancer grades tested. The analysis presented herein suggests that PSHG imaging could provide a quantitative evaluation of the tumor state and the distinction of malignant from benign breast tissues. The obtained results also allowed the development of a biophysical model, which can explain the aforementioned differentiations and is in agreement with the simulations relating the SHG anisotropy values with the mechanical tension applied to the collagen during cancer progression. The current approach could be a step forward for the development of new, nondestructive, label free optical diagnostic tools for cancer reducing the need of recalls and unnecessary biopsies, while potentially improving cancer detection rates.
Identifiants
pubmed: 32643819
doi: 10.1002/jbio.202000180
doi:
Substances chimiques
Collagen
9007-34-5
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e202000180Informations de copyright
© 2020 Wiley-VCH GmbH.
Références
K. Harpel, R. D. Baker, B. Amirsolaimani, S. Mehravar, J. Vagner, T. O. Matsunaga, B. Banerjee, K. Kieu, Biomed. Opt. Express 2016, 7, 2849.
K. Palikaras, M. Mari, B. Petanidou, A. Pasparaki, G. Filippidis, A. N. Tavernarakis, J. Lipid Res 2017, 58, 72.
M. G. Giacomelli, T. Yoshitake, L. C. Cahill, H. Vardeh, L. M. Quintana, B. E. Faulkner-Jones, J. Brooker, J. L. Connolly, J. G. Fujimoto, Biomed. Opt. Express 2018, 9, 2457.
E. Gavgiotaki, G. Filippidis, H. Markomanolaki, G. Kenanakis, S. Agelaki, V. Georgoulias, I. Athanassakis, J. Biophotonics 2017, 10, 1152.
E. Gavgiotaki, V. Tsafas, S. Bovasianos, S. Agelaki, V. Georgoulias, M. Tzardi, I. Athanassakis, G. Filippidis, Proc SPIE 2019, 11076, 18.
S. You, H. Tu, E. J. Chaney, Y. Sun, Y. Zhao, A. J. Bower, Y. Z. Liu, M. Marjanovic, S. Sinha, Y. Pu, S. A. Boppart, Nat. Commun 2018, 9, 1.
D. Tokarz, R. Cisek, M. N. Wein, R. Turcotte, C. Haase, S.-C. A. Yeh, S. Bharadwaj, A. P. Raphael, H. Paudel, C. Alt, T.-M. Liu, H. M. Kronenberg, C. P. Lin, PLoS One 2017, 12, 0186846.
T. Hompland, A. Erikson, M. Lindgren, T. Lindmo, C. de Lange Davies, J. Biomed. Opt 2008, 13, 054050.
N. D. Kirkpatrick, M. A. Brewer, U. Utzinger, Cancer Epidemiol. Biomarkers Prev 2007, 16, 2048.
C. Morrison, J. Thornhill, E. Gaffney, Urol. Res 2000, 28, 304.
J. Smolle, M. Fiebiger, R. Hofmann-Wellenhof, H. Kerl, Am. J. Dermatopathol 1996, 18, 358.
P. J. Campagnola, L. M. Loew, Nat. Biotechnol 2003, 21, 1356.
M. Fang, J. Yuan, C. Peng, Y. Li, Tumor Biol 2014, 35, 2871.
B. Brodsky, A. V. Persikov, Adv. Protein Chem 2005, 70, 301.
P. A. Torzilli, J. W. Bourne, T. Cigler, C. T. Vincent, Semin. Cancer Biol 2012, 22, 385.
P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, P. J. Keely, BMC Med 2006, 4, 38.
X. Tang, T. B. Kuhlenschmidt, J. Zhou, P. Bell, F. Wang, M. S. Kuhlenschmidt, T. A. Saif, Biophys. J 2010, 99, 2460.
L. Bingle, N. J. Brown, C. E. Lewis, J. Pathol 2002, 196, 254.
J. N. Wolfe, Cancer 1976, 37, 2486.
A. M. Kabel, J. Oncol. Sci 2017, 3, 5.
S. K. Paidi, A. Rizwan, C. Zheng, M. Cheng, K. Glunde, I. Barman, Cancer Res 2017, 77, 247.
W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, C. Y. Dong, Appl. Phys. Lett 2009, 94, 183902.
S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, C. K. Sun, Biophys. J 2004, 86, 3914.
M. Pinsard, S. Laverty, H. Richard, J. Dubuc, M. C. Schanne-Klein, F. Légaré, Sci. Rep 2019, 9, 1.
S. V. Plotnikov, A. C. Millard, P. J. Campagnola, W. A. Mohler, Biophys. J 2006, 90, 693.
Z. Y. Zhuo, C. S. Liao, C. H. Huang, J. Y. Yu, Y. Y. Tzeng, W. Lo, C. Y. Dong, H. C. Chui, Y. C. Huang, H. M. Lai, S. W. Chu, J. Struct. Biol 2010, 171, 88.
F. Tiaho, G. Recher, D. Rouède, Opt. Express 2007, 15, 12286.
P. Stoller, K. M. Reiser, P. M. Celliers, A. M. Rubenchik, Biophys. J 2002, 82, 3330.
G. Ducourthial, J. S. Affagard, M. Schmeltz, X. Solinas, M. Lopez-Poncelas, C. Bonod-Bidaud, R. Rubio-Amador, F. Ruggiero, J. M. Allain, E. Beaurepaire, M. C. Schanne-Klein, J. Biophotonics 2019, 12, 201800336.
K. R. Campbell, R. Chaudhary, J. M. Handel, M. S. Patankar, P. J. Campagnola, J. Biomed. Opt 2018, 23, 1.
I. Amat-Roldan, S. Psilodimitrakopoulos, P. Loza-Alvarez, D. Artigas, Opt. Express 2010, 18, 17209.
D. Rouède, E. Schaub, J. J. Bellanger, F. Ezan, J. C. Scimeca, G. Baffet, F. Tiaho, Sci. Rep 2017, 7, 1.
A. H. Fischer, K. A. Jacobson, J. Rose, R. Zeller, Cold Spring Harb. Protoc 2008, 3, 4986.
M. G. Monaghan, S. Kroll, S. Y. Brucker, K. Schenke-Layland, Tissue Eng. Part C Methods 2016, 22, 517.
E. Gavgiotaki, G. Filippidis, I. Zerva, G. Kenanakis, E. Archontakis, S. Agelaki, V. Georgoulias, I. Athanassakis, J. Biophotonics 2019, 12, 201800277.
C.-K. Chou, W.-L. Chen, P. T. Fwu, S.-J. Lin, H.-S. Lee, C.-Y. Dong, J. Biomed. Opt 2008, 13, 014005.
S. Psilodimitrakopoulos, L. Mouchliadis, I. Paradisanos, A. Lemonis, G. Kioseoglou, E. Stratakis, Light Sci. Appl 2018, 7, 18005.
R. M. Williams, W. R. Zipfel, W. W. Webb, Biophys. J 2005, 88, 1377.
A. Erikson, J. Örtegren, T. Hompland, C. de Lange Davies, M. Lindgren, J. Biomed. Opt 2007, 12, 044002.
A. S. Quigley, S. Bancelin, D. Deska-Gauthier, F. Légaré, L. Kreplak, S. P. Veres, Sci. Rep 2018, 8, 1.
E. I. Romijn, A. Finnøy, M. B. Lilledahl, J. Biophotonics 2019, 12, 201800090.
S. Z. Despotović, Đ. N. Milićević, A. J. Krmpot, A. M. Pavlović, V. D. Živanović, Z. Krivokapić, V. B. Pavlović, S. Lević, G. Nikolić, M. D. Rabasović, Sci. Rep 2020, 10, 1.
L. Mostaço-Guidolin, N. L. Rosin, T. L. Hackett, Int. J. Mol. Sci 2017, 18, 1772.
P. Matteini, F. Ratto, F. Rossi, R. Cicchi, C. Stringari, D. Kapsokalyvas, F. S. Pavone, R. Pini, Opt. Express 2009, 17, 4868.
D. J. S. Hulmes, Journal of Structural Biology 2002, 137, 2.
F. J. Ávila, O. Del Barco, J. M. Bueno, J. Biomed. Opt 2015, 20, 86001.
R. Mercatelli, S. Mattana, L. Capozzoli, F. Ratto, F. Rossi, R. Pini, D. Fioretto, F. S. Pavone, S. Caponi, R. Cicchi, Commun. Biol 2019, 2(1), 117.
R. Mercatelli, T. Triulzi, F. S. Pavone, R. Orlandi, R. Cicchi, J. Biophotonics 2020, e202000159. https://doi.org/10.1002/jbio.202000159.
C. Teulon, I. Gusachenko, G. Latour, M.-C. Schanne-Klein, Opt. Express 2015, 23, 9313.
M. Zimmerley, P. Mahou, D. Débarre, M. C. Schanne-Klein, E. Beaurepaire, Phys. Rev. X 2013, 3, 011002.
G. Ducourthial, P. Leclerc, T. Mansuryan, M. Fabert, J. Brevier, R. Habert, F. Braud, R. Batrin, C. Vever-Bizet, G. Bourg-Heckly, L. Thiberville, A. Druilhe, A. Kudlinski, F. Louradour, Sci. Rep 2015, 5, 1.
A. Lombardini, V. Mytskaniuk, S. Sivankutty, E. R. Andresen, X. Chen, J. Wenger, M. Fabert, N. Joly, F. Louradour, A. Kudlinski, H. Rigneault, Light Sci. Appl 2018, 7(1), 10.
D. F. Holmes, Y. Lu, T. Starborg, K. E. Kadler, Current Topics in Developmental Biology, Vol. 130, Academic Press Inc, Manchester, London, 2018, p. 107.
M. J. Buehler, Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 12285.