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Structural changes in mixed Col I/Col V collagen gels probed by SHG microscopy: implications for probing stromal alterations in human breast cancerVisar Ajeti, Oleg Nadiarnykh, Suzanne M. Ponik, Patricia J. Keely, Kevin W. Eliceiri, and Paul J. Campagnola »View Author Affiliations
Visar Ajeti,1,2
Oleg Nadiarnykh,3
Suzanne M. Ponik,2,4
Patricia J. Keely,1,2,4
Kevin W. Eliceiri,1,2
and Paul J. Campagnola1,2,*
1Department of Biomedical Engineering, University of Wisconsin-Madison, Madison, Wisconsin 53706, USA 2Laboratory for Optical and Computational Instrumentation (LOCI), University of Wisconsin-Madison, Madison Wisconsin 53706, USA 3Present Address: Department of Physics, University of Utrecht, The Netherlands 4Department of Cell and Regenerative Biology, University of Wisconsin-Madison, Madison, Wisconsin 53706, USA *Corresponding author: pcampagnola@wisc.edu |
Biomedical Optics Express, Vol. 2, Issue 8, pp. 2307-2316 (2011)
http://dx.doi.org/10.1364/BOE.2.002307
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Abstract
Second Harmonic Generation (SHG) microscopy has been previously used to describe the morphology of collagen in the extracellular matrix (ECM) in different stages of invasion in breast cancer. Here this concept is extended by using SHG to provide quantitative discrimination of self-assembled collagen gels, consisting of mixtures of type I (Col I) and type V (Col V) isoforms which serve as models of changes in the ECM during invasion in vivo. To investigate if SHG is sensitive to changes due to Col V incorporation into Col I fibrils, gels were prepared with 0-20% Col V with the balance consisting of Col I. Using the metrics of SHG intensity, fiber length, emission directionality, and depth-dependent intensities, we found similar responses for gels comprised of 100% Col I, and 95% Col I/5% Col V, where these metrics were all significantly different from those of the 80% Col I/20% Col V gels. Specifically, the gels of lower Col V content produce brighter SHG, are characterized by longer fibers, and have a higher forward/backward emission ratio. These attributes are all consistent with more highly organized collagen fibrils/fibers and are in agreement with previous TEM characterization as well as predictions based on phase matching considerations. These results suggest that SHG can be developed to discriminate Col I/Col V composition in tissues to characterize and follow breast cancer invasion.
© 2011 OSA
OCIS Codes
(180.6900) Microscopy : Three-dimensional microscopy
(190.2620) Nonlinear optics : Harmonic generation and mixing
(190.4180) Nonlinear optics : Multiphoton processes
(290.7050) Scattering : Turbid media
(170.6935) Medical optics and biotechnology : Tissue characterization
ToC Category:
Microscopy
History
Original Manuscript: May 31, 2011
Revised Manuscript: July 12, 2011
Manuscript Accepted: July 14, 2011
Published: July 20, 2011
Citation
Visar Ajeti, Oleg Nadiarnykh, Suzanne M. Ponik, Patricia J. Keely, Kevin W. Eliceiri, and Paul J. Campagnola, "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)
http://www.opticsinfobase.org/boe/abstract.cfm?URI=boe-2-8-2307
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- N. Théret, O. Musso, B. Turlin, D. Lotrian, P. Bioulac-Sage, J. P. Campion, K. Boudjéma, and B. Clément, “Increased extracellular matrix remodeling is associated with tumor progression in human hepatocellular carcinomas,” Hepatology 34(1), 82–88 (2001). [CrossRef] [PubMed]
- H. Hugo, M. L. Ackland, T. Blick, M. G. Lawrence, J. A. Clements, E. D. Williams, and E. W. Thompson, “Epithelial--mesenchymal and mesenchymal--epithelial transitions in carcinoma progression,” J. Cell. Physiol. 213(2), 374–383 (2007). [CrossRef] [PubMed]
- E. Sahai, J. Wyckoff, U. Philippar, J. E. Segall, F. Gertler, and J. Condeelis, “Simultaneous imaging of GFP, CFP and collagen in tumors in vivo using multiphoton microscopy,” BMC Biotechnol. 5(1), 14 (2005). [CrossRef] [PubMed]
- M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned collagen is a prognostic signature for survival in human breast carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011). [CrossRef] [PubMed]
- C. Luparello, F. David, G. Campisi, and R. Sirchia, “T47-D cells and type V collagen: a model for the study of apoptotic gene expression by breast cancer cells,” Biol. Chem. 384(6), 965–975 (2003). [CrossRef] [PubMed]
- R. Cicchi, S. Sestini, V. De Giorgi, P. Carli, D. Massi, and F. S. Pavone, “Basal cell carcinoma imaging and characterization by multiple nonlinear microscopy techniques,” Biophys. J. , 157a–157a (2007).
- E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003). [CrossRef] [PubMed]
- D. E. Birk, J. M. Fitch, J. P. Babiarz, K. J. Doane, and T. F. Linsenmayer, “Collagen fibrillogenesis in vitro: interaction of types I and V collagen regulates fibril diameter,” J. Cell Sci. 95(Pt 4), 649–657 (1990). [PubMed]
- P. J. Su, W. L. Chen, Y. F. Chen, and C. Y. Dong, “Determination of collagen nanostructure from second-order susceptibility tensor analysis,” Biophys. J. 100(8), 2053–2062 (2011). [CrossRef] [PubMed]
- S. J. Lin, S. H. Jee, C. J. Kuo, R. J. Wu, W. C. Lin, J. S. Chen, Y. H. Liao, C. J. Hsu, T. F. Tsai, Y. F. Chen, and C. Y. Dong, “Discrimination of basal cell carcinoma from normal dermal stroma by quantitative multiphoton imaging,” Opt. Lett. 31(18), 2756–2758 (2006). [CrossRef] [PubMed]
- P. M. McGowan and M. J. Duffy, “Matrix metalloproteinase expression and outcome in patients with breast cancer: analysis of a published database,” Ann. Oncol. 19(9), 1566–1572 (2008). [CrossRef] [PubMed]
- M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned collagen is a prognostic signature for survival in human breast carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011). [CrossRef] [PubMed]
- T. Sørlie, C. M. Perou, R. Tibshirani, T. Aas, S. Geisler, H. Johnsen, T. Hastie, M. B. Eisen, M. van de Rijn, S. S. Jeffrey, T. Thorsen, H. Quist, J. C. Matese, P. O. Brown, D. Botstein, P. Eystein Lønning, and A. L. Børresen-Dale, “Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications,” Proc. Natl. Acad. Sci. U.S.A. 98(19), 10869–10874 (2001). [CrossRef] [PubMed]
- M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned collagen is a prognostic signature for survival in human breast carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011). [CrossRef] [PubMed]
- P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008). [CrossRef] [PubMed]
- P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006). [CrossRef] [PubMed]
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- J. M. Pellikainen, K. M. Ropponen, V. V. Kataja, J. K. Kellokoski, M. J. Eskelinen, and V. M. Kosma, “Expression of matrix metalloproteinase (MMP)-2 and MMP-9 in breast cancer with a special reference to activator protein-2, HER2, and prognosis,” Clin. Cancer Res. 10(22), 7621–7628 (2004). [CrossRef] [PubMed]
- P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008). [CrossRef] [PubMed]
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- R. Lacomb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, “Phase Matching considerations in Second Harmonic Generation from tissues: Effects on emission directionality, conversion efficiency and observed morphology,” Opt. Commun. 281(7), 1823–1832 (2008). [CrossRef] [PubMed]
- R. Lacomb, O. Nadiarnykh, and P. Campagnola, “Quantitative second harmonic generation imaging of the diseased state osteogenesis imperfecta: experiment and simulation,” Biophys. J. 94(11), 4504–4514 (2008). [CrossRef]
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- S. Y. Huang, M. Van Arsdall, S. Tedjarati, M. McCarty, W. J. Wu, R. Langley, and I. J. Fidler, “Contributions of stromal metalloproteinase-9 to angiogenesis and growth of human ovarian carcinoma in mice,” J. Natl. Cancer Inst. 94(15), 1134–1142 (2002). [PubMed]
- H. Hugo, M. L. Ackland, T. Blick, M. G. Lawrence, J. A. Clements, E. D. Williams, and E. W. Thompson, “Epithelial--mesenchymal and mesenchymal--epithelial transitions in carcinoma progression,” J. Cell. Physiol. 213(2), 374–383 (2007). [CrossRef] [PubMed]
- F. Légaré, C. Pfeffer, and B. R. Olsen, “The role of backscattering in SHG tissue imaging,” Biophys. J. 93(4), 1312–1320 (2007). [CrossRef] [PubMed]
- D. E. Birk, J. M. Fitch, J. P. Babiarz, K. J. Doane, and T. F. Linsenmayer, “Collagen fibrillogenesis in vitro: interaction of types I and V collagen regulates fibril diameter,” J. Cell Sci. 95(Pt 4), 649–657 (1990). [PubMed]
- S. H. Barsky, C. N. Rao, G. R. Grotendorst, and L. A. Liotta, “Increased content of Type V Collagen in desmoplasia of human breast carcinoma,” Am. J. Pathol. 108(3), 276–283 (1982). [PubMed]
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- C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J. 92(6), 2212–2222 (2007). [CrossRef] [PubMed]
- R. Cicchi, S. Sestini, V. De Giorgi, P. Carli, D. Massi, and F. S. Pavone, “Basal cell carcinoma imaging and characterization by multiple nonlinear microscopy techniques,” Biophys. J. , 157a–157a (2007).
- T. Sørlie, C. M. Perou, R. Tibshirani, T. Aas, S. Geisler, H. Johnsen, T. Hastie, M. B. Eisen, M. van de Rijn, S. S. Jeffrey, T. Thorsen, H. Quist, J. C. Matese, P. O. Brown, D. Botstein, P. Eystein Lønning, and A. L. Børresen-Dale, “Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications,” Proc. Natl. Acad. Sci. U.S.A. 98(19), 10869–10874 (2001). [CrossRef] [PubMed]
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- C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J. 92(6), 2212–2222 (2007). [CrossRef] [PubMed]
- S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006). [CrossRef] [PubMed]
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- S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006). [CrossRef] [PubMed]
- N. Théret, O. Musso, B. Turlin, D. Lotrian, P. Bioulac-Sage, J. P. Campion, K. Boudjéma, and B. Clément, “Increased extracellular matrix remodeling is associated with tumor progression in human hepatocellular carcinomas,” Hepatology 34(1), 82–88 (2001). [CrossRef] [PubMed]
- O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer 10(1), 94 (2010). [CrossRef] [PubMed]
- R. Lacomb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, “Phase Matching considerations in Second Harmonic Generation from tissues: Effects on emission directionality, conversion efficiency and observed morphology,” Opt. Commun. 281(7), 1823–1832 (2008). [CrossRef] [PubMed]
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- R. Lacomb, O. Nadiarnykh, and P. Campagnola, “Quantitative second harmonic generation imaging of the diseased state osteogenesis imperfecta: experiment and simulation,” Biophys. J. 94(11), 4504–4514 (2008). [CrossRef]
- O. Nadiarnykh, R. B. Lacomb, P. J. Campagnola, and W. A. Mohler, “Coherent and incoherent SHG in fibrillar cellulose matrices,” Opt. Express 15(6), 3348–3360 (2007). [CrossRef] [PubMed]
- F. Légaré, C. Pfeffer, and B. R. Olsen, “The role of backscattering in SHG tissue imaging,” Biophys. J. 93(4), 1312–1320 (2007). [CrossRef] [PubMed]
- R. Cicchi, S. Sestini, V. De Giorgi, P. Carli, D. Massi, and F. S. Pavone, “Basal cell carcinoma imaging and characterization by multiple nonlinear microscopy techniques,” Biophys. J. , 157a–157a (2007).
- M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned collagen is a prognostic signature for survival in human breast carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011). [CrossRef] [PubMed]
- J. M. Pellikainen, K. M. Ropponen, V. V. Kataja, J. K. Kellokoski, M. J. Eskelinen, and V. M. Kosma, “Expression of matrix metalloproteinase (MMP)-2 and MMP-9 in breast cancer with a special reference to activator protein-2, HER2, and prognosis,” Clin. Cancer Res. 10(22), 7621–7628 (2004). [CrossRef] [PubMed]
- T. Sørlie, C. M. Perou, R. Tibshirani, T. Aas, S. Geisler, H. Johnsen, T. Hastie, M. B. Eisen, M. van de Rijn, S. S. Jeffrey, T. Thorsen, H. Quist, J. C. Matese, P. O. Brown, D. Botstein, P. Eystein Lønning, and A. L. Børresen-Dale, “Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications,” Proc. Natl. Acad. Sci. U.S.A. 98(19), 10869–10874 (2001). [CrossRef] [PubMed]
- F. Légaré, C. Pfeffer, and B. R. Olsen, “The role of backscattering in SHG tissue imaging,” Biophys. J. 93(4), 1312–1320 (2007). [CrossRef] [PubMed]
- E. Sahai, J. Wyckoff, U. Philippar, J. E. Segall, F. Gertler, and J. Condeelis, “Simultaneous imaging of GFP, CFP and collagen in tumors in vivo using multiphoton microscopy,” BMC Biotechnol. 5(1), 14 (2005). [CrossRef] [PubMed]
- S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006). [CrossRef] [PubMed]
- E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003). [CrossRef] [PubMed]
- M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned collagen is a prognostic signature for survival in human breast carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011). [CrossRef] [PubMed]
- P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008). [CrossRef] [PubMed]
- P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006). [CrossRef] [PubMed]
- S. M. Pupa, S. Ménard, S. Forti, and E. Tagliabue, “New insights into the role of extracellular matrix during tumor onset and progression,” J. Cell. Physiol. 192(3), 259–267 (2002). [CrossRef] [PubMed]
- C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J. 92(6), 2212–2222 (2007). [CrossRef] [PubMed]
- T. Sørlie, C. M. Perou, R. Tibshirani, T. Aas, S. Geisler, H. Johnsen, T. Hastie, M. B. Eisen, M. van de Rijn, S. S. Jeffrey, T. Thorsen, H. Quist, J. C. Matese, P. O. Brown, D. Botstein, P. Eystein Lønning, and A. L. Børresen-Dale, “Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications,” Proc. Natl. Acad. Sci. U.S.A. 98(19), 10869–10874 (2001). [CrossRef] [PubMed]
- S. H. Barsky, C. N. Rao, G. R. Grotendorst, and L. A. Liotta, “Increased content of Type V Collagen in desmoplasia of human breast carcinoma,” Am. J. Pathol. 108(3), 276–283 (1982). [PubMed]
- C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J. 92(6), 2212–2222 (2007). [CrossRef] [PubMed]
- C. Ricciardelli and R. J. Rodgers, “Extracellular matrix of ovarian tumors,” Semin. Reprod. Med. 24(4), 270–282 (2006). [CrossRef] [PubMed]
- M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned collagen is a prognostic signature for survival in human breast carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011). [CrossRef] [PubMed]
- C. Ricciardelli and R. J. Rodgers, “Extracellular matrix of ovarian tumors,” Semin. Reprod. Med. 24(4), 270–282 (2006). [CrossRef] [PubMed]
- J. M. Pellikainen, K. M. Ropponen, V. V. Kataja, J. K. Kellokoski, M. J. Eskelinen, and V. M. Kosma, “Expression of matrix metalloproteinase (MMP)-2 and MMP-9 in breast cancer with a special reference to activator protein-2, HER2, and prognosis,” Clin. Cancer Res. 10(22), 7621–7628 (2004). [CrossRef] [PubMed]
- P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008). [CrossRef] [PubMed]
- E. Sahai, J. Wyckoff, U. Philippar, J. E. Segall, F. Gertler, and J. Condeelis, “Simultaneous imaging of GFP, CFP and collagen in tumors in vivo using multiphoton microscopy,” BMC Biotechnol. 5(1), 14 (2005). [CrossRef] [PubMed]
- P. J. Keely, A. M. Fong, M. M. Zutter, and S. A. Santoro, “Alteration of collagen-dependent adhesion, motility, and morphogenesis by the expression of antisense alpha 2 integrin mRNA in mammary cells,” J. Cell Sci. 108(Pt 2), 595–607 (1995). [PubMed]
- E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003). [CrossRef] [PubMed]
- E. Sahai, J. Wyckoff, U. Philippar, J. E. Segall, F. Gertler, and J. Condeelis, “Simultaneous imaging of GFP, CFP and collagen in tumors in vivo using multiphoton microscopy,” BMC Biotechnol. 5(1), 14 (2005). [CrossRef] [PubMed]
- R. Cicchi, S. Sestini, V. De Giorgi, P. Carli, D. Massi, and F. S. Pavone, “Basal cell carcinoma imaging and characterization by multiple nonlinear microscopy techniques,” Biophys. J. , 157a–157a (2007).
- C. Luparello, F. David, G. Campisi, and R. Sirchia, “T47-D cells and type V collagen: a model for the study of apoptotic gene expression by breast cancer cells,” Biol. Chem. 384(6), 965–975 (2003). [CrossRef] [PubMed]
- T. Sørlie, C. M. Perou, R. Tibshirani, T. Aas, S. Geisler, H. Johnsen, T. Hastie, M. B. Eisen, M. van de Rijn, S. S. Jeffrey, T. Thorsen, H. Quist, J. C. Matese, P. O. Brown, D. Botstein, P. Eystein Lønning, and A. L. Børresen-Dale, “Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications,” Proc. Natl. Acad. Sci. U.S.A. 98(19), 10869–10874 (2001). [CrossRef] [PubMed]
- P. J. Su, W. L. Chen, Y. F. Chen, and C. Y. Dong, “Determination of collagen nanostructure from second-order susceptibility tensor analysis,” Biophys. J. 100(8), 2053–2062 (2011). [CrossRef] [PubMed]
- C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J. 92(6), 2212–2222 (2007). [CrossRef] [PubMed]
- S. M. Pupa, S. Ménard, S. Forti, and E. Tagliabue, “New insights into the role of extracellular matrix during tumor onset and progression,” J. Cell. Physiol. 192(3), 259–267 (2002). [CrossRef] [PubMed]
- S. Y. Huang, M. Van Arsdall, S. Tedjarati, M. McCarty, W. J. Wu, R. Langley, and I. J. Fidler, “Contributions of stromal metalloproteinase-9 to angiogenesis and growth of human ovarian carcinoma in mice,” J. Natl. Cancer Inst. 94(15), 1134–1142 (2002). [PubMed]
- N. Théret, O. Musso, B. Turlin, D. Lotrian, P. Bioulac-Sage, J. P. Campion, K. Boudjéma, and B. Clément, “Increased extracellular matrix remodeling is associated with tumor progression in human hepatocellular carcinomas,” Hepatology 34(1), 82–88 (2001). [CrossRef] [PubMed]
- H. Hugo, M. L. Ackland, T. Blick, M. G. Lawrence, J. A. Clements, E. D. Williams, and E. W. Thompson, “Epithelial--mesenchymal and mesenchymal--epithelial transitions in carcinoma progression,” J. Cell. Physiol. 213(2), 374–383 (2007). [CrossRef] [PubMed]
- T. Sørlie, C. M. Perou, R. Tibshirani, T. Aas, S. Geisler, H. Johnsen, T. Hastie, M. B. Eisen, M. van de Rijn, S. S. Jeffrey, T. Thorsen, H. Quist, J. C. Matese, P. O. Brown, D. Botstein, P. Eystein Lønning, and A. L. Børresen-Dale, “Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications,” Proc. Natl. Acad. Sci. U.S.A. 98(19), 10869–10874 (2001). [CrossRef] [PubMed]
- T. Sørlie, C. M. Perou, R. Tibshirani, T. Aas, S. Geisler, H. Johnsen, T. Hastie, M. B. Eisen, M. van de Rijn, S. S. Jeffrey, T. Thorsen, H. Quist, J. C. Matese, P. O. Brown, D. Botstein, P. Eystein Lønning, and A. L. Børresen-Dale, “Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications,” Proc. Natl. Acad. Sci. U.S.A. 98(19), 10869–10874 (2001). [CrossRef] [PubMed]
- R. Lacomb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, “Phase Matching considerations in Second Harmonic Generation from tissues: Effects on emission directionality, conversion efficiency and observed morphology,” Opt. Commun. 281(7), 1823–1832 (2008). [CrossRef] [PubMed]
- C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J. 92(6), 2212–2222 (2007). [CrossRef] [PubMed]
- N. Théret, O. Musso, B. Turlin, D. Lotrian, P. Bioulac-Sage, J. P. Campion, K. Boudjéma, and B. Clément, “Increased extracellular matrix remodeling is associated with tumor progression in human hepatocellular carcinomas,” Hepatology 34(1), 82–88 (2001). [CrossRef] [PubMed]
- B. Eyden and M. Tzaphlidou, “Structural variations of collagen in normal and pathological tissues: role of electron microscopy,” Micron 32(3), 287–300 (2001). [CrossRef] [PubMed]
- S. Y. Huang, M. Van Arsdall, S. Tedjarati, M. McCarty, W. J. Wu, R. Langley, and I. J. Fidler, “Contributions of stromal metalloproteinase-9 to angiogenesis and growth of human ovarian carcinoma in mice,” J. Natl. Cancer Inst. 94(15), 1134–1142 (2002). [PubMed]
- T. Sørlie, C. M. Perou, R. Tibshirani, T. Aas, S. Geisler, H. Johnsen, T. Hastie, M. B. Eisen, M. van de Rijn, S. S. Jeffrey, T. Thorsen, H. Quist, J. C. Matese, P. O. Brown, D. Botstein, P. Eystein Lønning, and A. L. Børresen-Dale, “Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications,” Proc. Natl. Acad. Sci. U.S.A. 98(19), 10869–10874 (2001). [CrossRef] [PubMed]
- R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005). [CrossRef] [PubMed]
- P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008). [CrossRef] [PubMed]
- P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006). [CrossRef] [PubMed]
- H. Hugo, M. L. Ackland, T. Blick, M. G. Lawrence, J. A. Clements, E. D. Williams, and E. W. Thompson, “Epithelial--mesenchymal and mesenchymal--epithelial transitions in carcinoma progression,” J. Cell. Physiol. 213(2), 374–383 (2007). [CrossRef] [PubMed]
- R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005). [CrossRef] [PubMed]
- S. Y. Huang, M. Van Arsdall, S. Tedjarati, M. McCarty, W. J. Wu, R. Langley, and I. J. Fidler, “Contributions of stromal metalloproteinase-9 to angiogenesis and growth of human ovarian carcinoma in mice,” J. Natl. Cancer Inst. 94(15), 1134–1142 (2002). [PubMed]
- E. Sahai, J. Wyckoff, U. Philippar, J. E. Segall, F. Gertler, and J. Condeelis, “Simultaneous imaging of GFP, CFP and collagen in tumors in vivo using multiphoton microscopy,” BMC Biotechnol. 5(1), 14 (2005). [CrossRef] [PubMed]
- P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008). [CrossRef] [PubMed]
- R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005). [CrossRef] [PubMed]
- P. J. Keely, A. M. Fong, M. M. Zutter, and S. A. Santoro, “Alteration of collagen-dependent adhesion, motility, and morphogenesis by the expression of antisense alpha 2 integrin mRNA in mammary cells,” J. Cell Sci. 108(Pt 2), 595–607 (1995). [PubMed]
Am. J. Pathol.
- M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned collagen is a prognostic signature for survival in human breast carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011). [CrossRef] [PubMed]
- S. H. Barsky, C. N. Rao, G. R. Grotendorst, and L. A. Liotta, “Increased content of Type V Collagen in desmoplasia of human breast carcinoma,” Am. J. Pathol. 108(3), 276–283 (1982). [PubMed]
Ann. Oncol.
- P. M. McGowan and M. J. Duffy, “Matrix metalloproteinase expression and outcome in patients with breast cancer: analysis of a published database,” Ann. Oncol. 19(9), 1566–1572 (2008). [CrossRef] [PubMed]
Biol. Chem.
- C. Luparello, F. David, G. Campisi, and R. Sirchia, “T47-D cells and type V collagen: a model for the study of apoptotic gene expression by breast cancer cells,” Biol. Chem. 384(6), 965–975 (2003). [CrossRef] [PubMed]
Biophys. J.
- C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J. 92(6), 2212–2222 (2007). [CrossRef] [PubMed]
- R. Lacomb, O. Nadiarnykh, and P. Campagnola, “Quantitative second harmonic generation imaging of the diseased state osteogenesis imperfecta: experiment and simulation,” Biophys. J. 94(11), 4504–4514 (2008). [CrossRef]
- R. Cicchi, S. Sestini, V. De Giorgi, P. Carli, D. Massi, and F. S. Pavone, “Basal cell carcinoma imaging and characterization by multiple nonlinear microscopy techniques,” Biophys. J. , 157a–157a (2007).
- S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006). [CrossRef] [PubMed]
- R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005). [CrossRef] [PubMed]
- F. Légaré, C. Pfeffer, and B. R. Olsen, “The role of backscattering in SHG tissue imaging,” Biophys. J. 93(4), 1312–1320 (2007). [CrossRef] [PubMed]
- P. J. Su, W. L. Chen, Y. F. Chen, and C. Y. Dong, “Determination of collagen nanostructure from second-order susceptibility tensor analysis,” Biophys. J. 100(8), 2053–2062 (2011). [CrossRef] [PubMed]
BMC Biotechnol.
- E. Sahai, J. Wyckoff, U. Philippar, J. E. Segall, F. Gertler, and J. Condeelis, “Simultaneous imaging of GFP, CFP and collagen in tumors in vivo using multiphoton microscopy,” BMC Biotechnol. 5(1), 14 (2005). [CrossRef] [PubMed]
BMC Cancer
- O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer 10(1), 94 (2010). [CrossRef] [PubMed]
BMC Med.
- P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006). [CrossRef] [PubMed]
- P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008). [CrossRef] [PubMed]
Clin. Cancer Res.
- J. M. Pellikainen, K. M. Ropponen, V. V. Kataja, J. K. Kellokoski, M. J. Eskelinen, and V. M. Kosma, “Expression of matrix metalloproteinase (MMP)-2 and MMP-9 in breast cancer with a special reference to activator protein-2, HER2, and prognosis,” Clin. Cancer Res. 10(22), 7621–7628 (2004). [CrossRef] [PubMed]
Hepatology
- N. Théret, O. Musso, B. Turlin, D. Lotrian, P. Bioulac-Sage, J. P. Campion, K. Boudjéma, and B. Clément, “Increased extracellular matrix remodeling is associated with tumor progression in human hepatocellular carcinomas,” Hepatology 34(1), 82–88 (2001). [CrossRef] [PubMed]
J. Biomed. Opt.
- R. LaComb, O. Nadiarnykh, S. Carey, and P. J. Campagnola, “Quantitative second harmonic generation imaging and modeling of the optical clearing mechanism in striated muscle and tendon,” J. Biomed. Opt. 13(2), 021109 (2008). [CrossRef] [PubMed]
J. Cell Sci.
- D. E. Birk, J. M. Fitch, J. P. Babiarz, K. J. Doane, and T. F. Linsenmayer, “Collagen fibrillogenesis in vitro: interaction of types I and V collagen regulates fibril diameter,” J. Cell Sci. 95(Pt 4), 649–657 (1990). [PubMed]
- P. J. Keely, A. M. Fong, M. M. Zutter, and S. A. Santoro, “Alteration of collagen-dependent adhesion, motility, and morphogenesis by the expression of antisense alpha 2 integrin mRNA in mammary cells,” J. Cell Sci. 108(Pt 2), 595–607 (1995). [PubMed]
J. Cell. Physiol.
- S. M. Pupa, S. Ménard, S. Forti, and E. Tagliabue, “New insights into the role of extracellular matrix during tumor onset and progression,” J. Cell. Physiol. 192(3), 259–267 (2002). [CrossRef] [PubMed]
- H. Hugo, M. L. Ackland, T. Blick, M. G. Lawrence, J. A. Clements, E. D. Williams, and E. W. Thompson, “Epithelial--mesenchymal and mesenchymal--epithelial transitions in carcinoma progression,” J. Cell. Physiol. 213(2), 374–383 (2007). [CrossRef] [PubMed]
J. Natl. Cancer Inst.
- S. Y. Huang, M. Van Arsdall, S. Tedjarati, M. McCarty, W. J. Wu, R. Langley, and I. J. Fidler, “Contributions of stromal metalloproteinase-9 to angiogenesis and growth of human ovarian carcinoma in mice,” J. Natl. Cancer Inst. 94(15), 1134–1142 (2002). [PubMed]
J. Struct. Biol.
- D. J. Hulmes, “Building collagen molecules, fibrils, and suprafibrillar structures,” J. Struct. Biol. 137(1-2), 2–10 (2002). [CrossRef] [PubMed]
Micron
- B. Eyden and M. Tzaphlidou, “Structural variations of collagen in normal and pathological tissues: role of electron microscopy,” Micron 32(3), 287–300 (2001). [CrossRef] [PubMed]
- D. E. Birk, “Type V collagen: heterotypic type I/V collagen interactions in the regulation of fibril assembly,” Micron 32(3), 223–237 (2001). [CrossRef] [PubMed]
Nat. Biotechnol.
- P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21(11), 1356–1360 (2003). [CrossRef] [PubMed]
Nat. Med.
- E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003). [CrossRef] [PubMed]
Opt. Commun.
- R. Lacomb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, “Phase Matching considerations in Second Harmonic Generation from tissues: Effects on emission directionality, conversion efficiency and observed morphology,” Opt. Commun. 281(7), 1823–1832 (2008). [CrossRef] [PubMed]
Opt. Express
- O. Nadiarnykh, R. B. Lacomb, P. J. Campagnola, and W. A. Mohler, “Coherent and incoherent SHG in fibrillar cellulose matrices,” Opt. Express 15(6), 3348–3360 (2007). [CrossRef] [PubMed]
- F. Tiaho, G. Recher, and D. Rouède, “Estimation of helical angles of myosin and collagen by second harmonic generation imaging microscopy,” Opt. Express 15(19), 12286–12295 (2007). [CrossRef] [PubMed]
- X. X. Han and E. Brown, “Measurement of the ratio of forward-propagating to back-propagating second harmonic signal using a single objective,” Opt. Express 18(10), 10538–10550 (2010). [CrossRef] [PubMed]
Opt. Lett.
- S. J. Lin, S. H. Jee, C. J. Kuo, R. J. Wu, W. C. Lin, J. S. Chen, Y. H. Liao, C. J. Hsu, T. F. Tsai, Y. F. Chen, and C. Y. Dong, “Discrimination of basal cell carcinoma from normal dermal stroma by quantitative multiphoton imaging,” Opt. Lett. 31(18), 2756–2758 (2006). [CrossRef] [PubMed]
Proc. Natl. Acad. Sci. U.S.A.
- T. Sørlie, C. M. Perou, R. Tibshirani, T. Aas, S. Geisler, H. Johnsen, T. Hastie, M. B. Eisen, M. van de Rijn, S. S. Jeffrey, T. Thorsen, H. Quist, J. C. Matese, P. O. Brown, D. Botstein, P. Eystein Lønning, and A. L. Børresen-Dale, “Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications,” Proc. Natl. Acad. Sci. U.S.A. 98(19), 10869–10874 (2001). [CrossRef] [PubMed]
Semin. Reprod. Med.
- C. Ricciardelli and R. J. Rodgers, “Extracellular matrix of ovarian tumors,” Semin. Reprod. Med. 24(4), 270–282 (2006). [CrossRef] [PubMed]
Other
- Y. R. Shen, The Principles of Nonlinear Optics (John Wiley and Sons, 1984).
2011, Conklin, Am. J. Pathol.
- M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned collagen is a prognostic signature for survival in human breast carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011). [CrossRef] [PubMed]
- P. J. Su, W. L. Chen, Y. F. Chen, and C. Y. Dong, “Determination of collagen nanostructure from second-order susceptibility tensor analysis,” Biophys. J. 100(8), 2053–2062 (2011). [CrossRef] [PubMed]
- O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer 10(1), 94 (2010). [CrossRef] [PubMed]
- P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008). [CrossRef] [PubMed]
- R. Lacomb, O. Nadiarnykh, and P. Campagnola, “Quantitative second harmonic generation imaging of the diseased state osteogenesis imperfecta: experiment and simulation,” Biophys. J. 94(11), 4504–4514 (2008). [CrossRef]
- R. LaComb, O. Nadiarnykh, S. Carey, and P. J. Campagnola, “Quantitative second harmonic generation imaging and modeling of the optical clearing mechanism in striated muscle and tendon,” J. Biomed. Opt. 13(2), 021109 (2008). [CrossRef] [PubMed]
- R. Lacomb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, “Phase Matching considerations in Second Harmonic Generation from tissues: Effects on emission directionality, conversion efficiency and observed morphology,” Opt. Commun. 281(7), 1823–1832 (2008). [CrossRef] [PubMed]
- P. M. McGowan and M. J. Duffy, “Matrix metalloproteinase expression and outcome in patients with breast cancer: analysis of a published database,” Ann. Oncol. 19(9), 1566–1572 (2008). [CrossRef] [PubMed]
- H. Hugo, M. L. Ackland, T. Blick, M. G. Lawrence, J. A. Clements, E. D. Williams, and E. W. Thompson, “Epithelial--mesenchymal and mesenchymal--epithelial transitions in carcinoma progression,” J. Cell. Physiol. 213(2), 374–383 (2007). [CrossRef] [PubMed]
- F. Légaré, C. Pfeffer, and B. R. Olsen, “The role of backscattering in SHG tissue imaging,” Biophys. J. 93(4), 1312–1320 (2007). [CrossRef] [PubMed]
- R. Cicchi, S. Sestini, V. De Giorgi, P. Carli, D. Massi, and F. S. Pavone, “Basal cell carcinoma imaging and characterization by multiple nonlinear microscopy techniques,” Biophys. J. , 157a–157a (2007).
- C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J. 92(6), 2212–2222 (2007). [CrossRef] [PubMed]
- P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006). [CrossRef] [PubMed]
- S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006). [CrossRef] [PubMed]
- C. Ricciardelli and R. J. Rodgers, “Extracellular matrix of ovarian tumors,” Semin. Reprod. Med. 24(4), 270–282 (2006). [CrossRef] [PubMed]
- R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005). [CrossRef] [PubMed]
- E. Sahai, J. Wyckoff, U. Philippar, J. E. Segall, F. Gertler, and J. Condeelis, “Simultaneous imaging of GFP, CFP and collagen in tumors in vivo using multiphoton microscopy,” BMC Biotechnol. 5(1), 14 (2005). [CrossRef] [PubMed]
- J. M. Pellikainen, K. M. Ropponen, V. V. Kataja, J. K. Kellokoski, M. J. Eskelinen, and V. M. Kosma, “Expression of matrix metalloproteinase (MMP)-2 and MMP-9 in breast cancer with a special reference to activator protein-2, HER2, and prognosis,” Clin. Cancer Res. 10(22), 7621–7628 (2004). [CrossRef] [PubMed]
- P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21(11), 1356–1360 (2003). [CrossRef] [PubMed]
- E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003). [CrossRef] [PubMed]
- C. Luparello, F. David, G. Campisi, and R. Sirchia, “T47-D cells and type V collagen: a model for the study of apoptotic gene expression by breast cancer cells,” Biol. Chem. 384(6), 965–975 (2003). [CrossRef] [PubMed]
- D. J. Hulmes, “Building collagen molecules, fibrils, and suprafibrillar structures,” J. Struct. Biol. 137(1-2), 2–10 (2002). [CrossRef] [PubMed]
- S. Y. Huang, M. Van Arsdall, S. Tedjarati, M. McCarty, W. J. Wu, R. Langley, and I. J. Fidler, “Contributions of stromal metalloproteinase-9 to angiogenesis and growth of human ovarian carcinoma in mice,” J. Natl. Cancer Inst. 94(15), 1134–1142 (2002). [PubMed]
- S. M. Pupa, S. Ménard, S. Forti, and E. Tagliabue, “New insights into the role of extracellular matrix during tumor onset and progression,” J. Cell. Physiol. 192(3), 259–267 (2002). [CrossRef] [PubMed]
- N. Théret, O. Musso, B. Turlin, D. Lotrian, P. Bioulac-Sage, J. P. Campion, K. Boudjéma, and B. Clément, “Increased extracellular matrix remodeling is associated with tumor progression in human hepatocellular carcinomas,” Hepatology 34(1), 82–88 (2001). [CrossRef] [PubMed]
- T. Sørlie, C. M. Perou, R. Tibshirani, T. Aas, S. Geisler, H. Johnsen, T. Hastie, M. B. Eisen, M. van de Rijn, S. S. Jeffrey, T. Thorsen, H. Quist, J. C. Matese, P. O. Brown, D. Botstein, P. Eystein Lønning, and A. L. Børresen-Dale, “Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications,” Proc. Natl. Acad. Sci. U.S.A. 98(19), 10869–10874 (2001). [CrossRef] [PubMed]
- B. Eyden and M. Tzaphlidou, “Structural variations of collagen in normal and pathological tissues: role of electron microscopy,” Micron 32(3), 287–300 (2001). [CrossRef] [PubMed]
- D. E. Birk, “Type V collagen: heterotypic type I/V collagen interactions in the regulation of fibril assembly,” Micron 32(3), 223–237 (2001). [CrossRef] [PubMed]
- P. J. Keely, A. M. Fong, M. M. Zutter, and S. A. Santoro, “Alteration of collagen-dependent adhesion, motility, and morphogenesis by the expression of antisense alpha 2 integrin mRNA in mammary cells,” J. Cell Sci. 108(Pt 2), 595–607 (1995). [PubMed]
- D. E. Birk, J. M. Fitch, J. P. Babiarz, K. J. Doane, and T. F. Linsenmayer, “Collagen fibrillogenesis in vitro: interaction of types I and V collagen regulates fibril diameter,” J. Cell Sci. 95(Pt 4), 649–657 (1990). [PubMed]
- S. H. Barsky, C. N. Rao, G. R. Grotendorst, and L. A. Liotta, “Increased content of Type V Collagen in desmoplasia of human breast carcinoma,” Am. J. Pathol. 108(3), 276–283 (1982). [PubMed]
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OSA is a member of 