Abstract

HER2-amplified (HER2 + ) breast cancers are treated with the anti-HER2 monoclonal antibody trastuzumab. Although trastuzumab reduces production of the angiogenic factor VEGF in HER2 + tumors, the acute and sustained effects of trastuzumab on the tumor vasculature are not understood fully, particularly in trastuzumab-resistant tumors. We used mouse models of trastuzumab sensitive and trastuzumab-resistant HER2 + breast cancers to measure dynamic changes in tumor microvessel density and hemoglobin oxygenation (sO2) in vivo using quantitative hyperspectral imaging at 2, 5, 9, and 14 days after antibody treatment. Further analysis quantified the distribution of microvessels into low and high oxygenation groups, and monitored changes in these distributions with trastuzumab treatment. Gold standard immunohistochemistry was performed to validate complementary markers of tumor cell and vascular response to treatment. Trastuzumab treatment in both responsive and resistant tumors resulted in decreased sO2 5 days after initial treatment when compared to IgG-treated controls (p<0.05). Importantly, responsive tumors showed significantly higher vessel density and significantly lower sO2 than all other groups at 5 days post-treatment (p<0.05). Distribution analysis of vessel sO2 showed a significant (p<0.05) shift of highly oxygenated vessels towards lower oxygenation over the time-course in both trastuzumab-treated responsive and resistant tumors. This study suggests that longitudinal hyperspectral imaging of microvessel sO2 and density could distinguish trastuzumab-responsive from trastuzumab-resistant tumors, a finding that could be exploited in the post-neoadjuvant setting to guide post-surgical treatment decisions.

© 2014 Optical Society of America

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2014 (1)

2013 (4)

H. C. Hendargo, R. Estrada, S. J. Chiu, C. Tomasi, S. Farsiu, and J. A. Izatt, “Automated non-rigid registration and mosaicing for robust imaging of distinct retinal capillary beds using speckle variance optical coherence tomography,” Biomed. Opt. Express4(6), 803–821 (2013).
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A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical metabolic imaging identifies glycolytic levels, subtypes, and early-treatment response in breast cancer,” Cancer Res.73(20), 6164–6174 (2013).
[CrossRef] [PubMed]

T. D. O’Sullivan, A. Leproux, J.-H. Chen, S. Bahri, A. Matlock, D. Roblyer, C. E. McLaren, W.-P. Chen, A. E. Cerussi, M. Y. Su, and B. J. Tromberg, “Optical imaging correlates with magnetic resonance imaging breast density and reveals composition changes during neoadjuvant chemotherapy,” Breast Cancer Res.15(1), R14 (2013).
[CrossRef] [PubMed]

J. F. De Los Santos, A. Cantor, K. D. Amos, A. Forero, M. Golshan, J. K. Horton, C. A. Hudis, N. M. Hylton, K. McGuire, F. Meric-Bernstam, I. M. Meszoely, R. Nanda, and E. S. Hwang, “Magnetic resonance imaging as a predictor of pathologic response in patients treated with neoadjuvant systemic treatment for operable breast cancer. Translational Breast Cancer Research Consortium trial 017,” Cancer119(10), 1776–1783 (2013).
[CrossRef] [PubMed]

2012 (2)

C. V. Pastuskovas, E. E. Mundo, S. P. Williams, T. K. Nayak, J. Ho, S. Ulufatu, S. Clark, S. Ross, E. Cheng, K. Parsons-Reponte, G. Cain, M. Van Hoy, N. Majidy, S. Bheddah, J. dela Cruz Chuh, K. R. Kozak, N. Lewin-Koh, P. Nauka, D. Bumbaca, M. Sliwkowski, J. Tibbitts, F. P. Theil, P. J. Fielder, L. A. Khawli, and C. A. Boswell, “Effects of anti-VEGF on pharmacokinetics, biodistribution, and tumor penetration of trastuzumab in a preclinical breast cancer model,” Mol. Cancer Ther.11(3), 752–762 (2012).
[CrossRef] [PubMed]

S. H. Park, W. K. Moon, N. Cho, J. M. Chang, S.-A. Im, I. A. Park, K. W. Kang, W. Han, and D.-Y. Noh, “Comparison of diffusion-weighted MR imaging and FDG PET/CT to predict pathological complete response to neoadjuvant chemotherapy in patients with breast cancer,” Eur. Radiol.22(1), 18–25 (2012).
[CrossRef] [PubMed]

2011 (3)

G. Shen, H. Huang, A. Zhang, T. Zhao, S. Hu, L. Cheng, J. Liu, W. Xiao, B. Ling, Q. Wu, L. Song, and W. Wei, “In vivo activity of novel anti-ErbB2 antibody chA21 alone and with Paclitaxel or Trastuzumab in breast and ovarian cancer xenograft models,” Cancer Immunol. Immunother.60(3), 339–348 (2011).
[CrossRef] [PubMed]

M. Potente, H. Gerhardt, and P. Carmeliet, “Basic and therapeutic aspects of angiogenesis,” Cell146(6), 873–887 (2011).
[CrossRef] [PubMed]

G. M. Palmer, A. N. Fontanella, S. Shan, G. Hanna, G. Zhang, C. L. Fraser, and M. W. Dewhirst, “In vivo optical molecular imaging and analysis in mice using dorsal window chamber models applied to hypoxia, vasculature and fluorescent reporters,” Nat. Protoc.6(9), 1355–1366 (2011).
[CrossRef] [PubMed]

2009 (5)

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med.15(10), 1219–1223 (2009).
[CrossRef] [PubMed]

K. Vishwanath, H. Yuan, W. T. Barry, M. W. Dewhirst, and N. Ramanujam, “Using optical spectroscopy to longitudinally monitor physiological changes within solid tumors,” Neoplasia11(9), 889–900 (2009).
[PubMed]

M. E. Hardee, R. J. Eapen, Z. N. Rabbani, M. R. Dreher, J. Marks, K. L. Blackwell, and M. W. Dewhirst, “Her2/neu signaling blockade improves tumor oxygenation in a multifactorial fashion in Her2/neu+ tumors,” Cancer Chemother. Pharmacol.63(2), 219–228 (2009).
[CrossRef] [PubMed]

C. Shah, T. W. Miller, S. K. Wyatt, E. T. McKinley, M. G. Olivares, V. Sanchez, D. D. Nolting, J. R. Buck, P. Zhao, M. S. Ansari, R. M. Baldwin, J. C. Gore, R. Schiff, C. L. Arteaga, and H. C. Manning, “Imaging biomarkers predict response to anti-HER2 (ErbB2) therapy in preclinical models of breast cancer,” Clin. Cancer Res.15(14), 4712–4721 (2009).
[CrossRef] [PubMed]

M. W. Dewhirst, “Relationships between cycling hypoxia, HIF-1, angiogenesis and oxidative stress,” Radiat. Res.172(6), 653–665 (2009).
[CrossRef] [PubMed]

2007 (4)

G. Valabrega, F. Montemurro, and M. Aglietta, “Trastuzumab: mechanism of action, resistance and future perspectives in HER2-overexpressing breast cancer,” Ann. Oncol.18(6), 977–984 (2007).
[CrossRef] [PubMed]

A. Cerussi, D. Hsiang, N. Shah, R. Mehta, A. Durkin, J. Butler, and B. J. Tromberg, “Predicting response to breast cancer neoadjuvant chemotherapy using diffuse optical spectroscopy,” Proc. Natl. Acad. Sci. U.S.A.104(10), 4014–4019 (2007).
[CrossRef] [PubMed]

G. Brockhoff, B. Heckel, E. Schmidt-Bruecken, M. Plander, F. Hofstaedter, A. Vollmann, and S. Diermeier, “Differential impact of Cetuximab, Pertuzumab and Trastuzumab on BT474 and SK-BR-3 breast cancer cell proliferation,” Cell Prolif.40(4), 488–507 (2007).
[CrossRef] [PubMed]

C. A. Ritter, M. Perez-Torres, C. Rinehart, M. Guix, T. Dugger, J. A. Engelman, and C. L. Arteaga, “Human breast cancer cells selected for resistance to trastuzumab in vivo overexpress epidermal growth factor receptor and ErbB ligands and remain dependent on the ErbB receptor network,” Clin. Cancer Res.13(16), 4909–4919 (2007).
[CrossRef] [PubMed]

2005 (3)

B. S. Sorg, B. J. Moeller, O. Donovan, Y. Cao, and M. W. Dewhirst, “Hyperspectral imaging of hemoglobin saturation in tumor microvasculature and tumor hypoxia development,” J. Biomed. Opt.10(4), 044004 (2005).
[CrossRef] [PubMed]

R. K. Jain, “Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy,” Science307(5706), 58–62 (2005).
[CrossRef] [PubMed]

M. J. Piccart-Gebhart, M. Procter, B. Leyland-Jones, A. Goldhirsch, M. Untch, I. Smith, L. Gianni, J. Baselga, R. Bell, C. Jackisch, D. Cameron, M. Dowsett, C. H. Barrios, G. Steger, C. S. Huang, M. Andersson, M. Inbar, M. Lichinitser, I. Láng, U. Nitz, H. Iwata, C. Thomssen, C. Lohrisch, T. M. Suter, J. Rüschoff, T. Suto, V. Greatorex, C. Ward, C. Straehle, E. McFadden, M. S. Dolci, R. D. Gelber, and Herceptin Adjuvant (HERA) Trial Study Team, “Trastuzumab after Adjuvant Chemotherapy in HER2-Positive Breast Cancer,” N. Engl. J. Med.353(16), 1659–1672 (2005).
[CrossRef] [PubMed]

2004 (1)

D. B. Jakubowski, A. E. Cerussi, F. Bevilacqua, N. Shah, D. Hsiang, J. Butler, and B. J. Tromberg, “Monitoring neoadjuvant chemotherapy in breast cancer using quantitative diffuse optical spectroscopy: a case study,” J. Biomed. Opt.9(1), 230–238 (2004).
[CrossRef] [PubMed]

2003 (1)

H. Degani, M. Chetrit-Dadiani, L. Bogin, and E. Furman-Haran, “Magnetic resonance imaging of tumor vasculature,” Thromb. Haemost.89(1), 25–33 (2003).
[PubMed]

2002 (4)

C. L. Vogel, M. A. Cobleigh, D. Tripathy, J. C. Gutheil, L. N. Harris, L. Fehrenbacher, D. J. Slamon, M. Murphy, W. F. Novotny, M. Burchmore, S. Shak, S. J. Stewart, and M. Press, “Efficacy and Safety of Trastuzumab as a Single Agent in First-Line Treatment of HER2-Overexpressing Metastatic Breast Cancer,” J. Clin. Oncol.20(3), 719–726 (2002).
[CrossRef] [PubMed]

Y. Izumi, L. Xu, E. di Tomaso, D. Fukumura, and R. K. Jain, “Tumour biology: herceptin acts as an anti-angiogenic cocktail,” Nature416(6878), 279–280 (2002).
[CrossRef] [PubMed]

C. L. Vogel, M. A. Cobleigh, D. Tripathy, J. C. Gutheil, L. N. Harris, L. Fehrenbacher, D. J. Slamon, M. Murphy, W. F. Novotny, M. Burchmore, S. Shak, S. J. Stewart, and M. Press, “Efficacy and Safety of Trastuzumab as a Single Agent in First-Line Treatment of HER2-Overexpressing Metastatic Breast Cancer,” J. Clin. Oncol.20(3), 719–726 (2002).
[CrossRef] [PubMed]

K. J. Zuzak, M. D. Schaeberle, E. N. Lewis, and I. W. Levin, “Visible Reflectance Hyperspectral Imaging: Characterization of a Noninvasive, in Vivo System for Determining Tissue Perfusion,” Anal. Chem.74(9), 2021–2028 (2002).
[CrossRef] [PubMed]

2000 (1)

G. D. Yancopoulos, S. Davis, N. W. Gale, J. S. Rudge, S. J. Wiegand, and J. Holash, “Vascular-specific growth factors and blood vessel formation,” Nature407(6801), 242–248 (2000).
[CrossRef] [PubMed]

1998 (1)

J. S. Ross and J. A. Fletcher, “The HER-2/neu oncogene in breast cancer: prognostic factor, predictive factor, and target for therapy,” Stem Cells16(6), 413–428 (1998).
[CrossRef] [PubMed]

1993 (1)

P. Santago and H. D. Gage, “Quantification of MR brain images by mixture density and partial volume modeling,” IEEE Trans. Med. Imaging12(3), 566–574 (1993).
[CrossRef] [PubMed]

1989 (1)

D. J. Slamon, W. Godolphin, L. A. Jones, J. A. Holt, S. G. Wong, D. E. Keith, W. J. Levin, S. G. Stuart, J. Udove, A. Ullrich, and et, “Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer,” Science244(4905), 707–712 (1989).
[CrossRef] [PubMed]

1974 (1)

H. Akaike, “A new look at the statistical model identification,” IEEE Trans. Automat. Contr.19(6), 716–723 (1974).
[CrossRef]

Agani, F.

J. O. A. Forsythe, B. Jiang, N. V Iyer, F. Agani, and S. W. Leung, “Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor Activation of Vascular Endothelial Growth Factor Gene Transcription by Hypoxia-Inducible Factor 1” (1996).

Aglietta, M.

G. Valabrega, F. Montemurro, and M. Aglietta, “Trastuzumab: mechanism of action, resistance and future perspectives in HER2-overexpressing breast cancer,” Ann. Oncol.18(6), 977–984 (2007).
[CrossRef] [PubMed]

Akaike, H.

H. Akaike, “A new look at the statistical model identification,” IEEE Trans. Automat. Contr.19(6), 716–723 (1974).
[CrossRef]

Amos, K. D.

J. F. De Los Santos, A. Cantor, K. D. Amos, A. Forero, M. Golshan, J. K. Horton, C. A. Hudis, N. M. Hylton, K. McGuire, F. Meric-Bernstam, I. M. Meszoely, R. Nanda, and E. S. Hwang, “Magnetic resonance imaging as a predictor of pathologic response in patients treated with neoadjuvant systemic treatment for operable breast cancer. Translational Breast Cancer Research Consortium trial 017,” Cancer119(10), 1776–1783 (2013).
[CrossRef] [PubMed]

Andersson, M.

M. J. Piccart-Gebhart, M. Procter, B. Leyland-Jones, A. Goldhirsch, M. Untch, I. Smith, L. Gianni, J. Baselga, R. Bell, C. Jackisch, D. Cameron, M. Dowsett, C. H. Barrios, G. Steger, C. S. Huang, M. Andersson, M. Inbar, M. Lichinitser, I. Láng, U. Nitz, H. Iwata, C. Thomssen, C. Lohrisch, T. M. Suter, J. Rüschoff, T. Suto, V. Greatorex, C. Ward, C. Straehle, E. McFadden, M. S. Dolci, R. D. Gelber, and Herceptin Adjuvant (HERA) Trial Study Team, “Trastuzumab after Adjuvant Chemotherapy in HER2-Positive Breast Cancer,” N. Engl. J. Med.353(16), 1659–1672 (2005).
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C. V. Pastuskovas, E. E. Mundo, S. P. Williams, T. K. Nayak, J. Ho, S. Ulufatu, S. Clark, S. Ross, E. Cheng, K. Parsons-Reponte, G. Cain, M. Van Hoy, N. Majidy, S. Bheddah, J. dela Cruz Chuh, K. R. Kozak, N. Lewin-Koh, P. Nauka, D. Bumbaca, M. Sliwkowski, J. Tibbitts, F. P. Theil, P. J. Fielder, L. A. Khawli, and C. A. Boswell, “Effects of anti-VEGF on pharmacokinetics, biodistribution, and tumor penetration of trastuzumab in a preclinical breast cancer model,” Mol. Cancer Ther.11(3), 752–762 (2012).
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C. V. Pastuskovas, E. E. Mundo, S. P. Williams, T. K. Nayak, J. Ho, S. Ulufatu, S. Clark, S. Ross, E. Cheng, K. Parsons-Reponte, G. Cain, M. Van Hoy, N. Majidy, S. Bheddah, J. dela Cruz Chuh, K. R. Kozak, N. Lewin-Koh, P. Nauka, D. Bumbaca, M. Sliwkowski, J. Tibbitts, F. P. Theil, P. J. Fielder, L. A. Khawli, and C. A. Boswell, “Effects of anti-VEGF on pharmacokinetics, biodistribution, and tumor penetration of trastuzumab in a preclinical breast cancer model,” Mol. Cancer Ther.11(3), 752–762 (2012).
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M. J. Piccart-Gebhart, M. Procter, B. Leyland-Jones, A. Goldhirsch, M. Untch, I. Smith, L. Gianni, J. Baselga, R. Bell, C. Jackisch, D. Cameron, M. Dowsett, C. H. Barrios, G. Steger, C. S. Huang, M. Andersson, M. Inbar, M. Lichinitser, I. Láng, U. Nitz, H. Iwata, C. Thomssen, C. Lohrisch, T. M. Suter, J. Rüschoff, T. Suto, V. Greatorex, C. Ward, C. Straehle, E. McFadden, M. S. Dolci, R. D. Gelber, and Herceptin Adjuvant (HERA) Trial Study Team, “Trastuzumab after Adjuvant Chemotherapy in HER2-Positive Breast Cancer,” N. Engl. J. Med.353(16), 1659–1672 (2005).
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C. L. Vogel, M. A. Cobleigh, D. Tripathy, J. C. Gutheil, L. N. Harris, L. Fehrenbacher, D. J. Slamon, M. Murphy, W. F. Novotny, M. Burchmore, S. Shak, S. J. Stewart, and M. Press, “Efficacy and Safety of Trastuzumab as a Single Agent in First-Line Treatment of HER2-Overexpressing Metastatic Breast Cancer,” J. Clin. Oncol.20(3), 719–726 (2002).
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C. Shah, T. W. Miller, S. K. Wyatt, E. T. McKinley, M. G. Olivares, V. Sanchez, D. D. Nolting, J. R. Buck, P. Zhao, M. S. Ansari, R. M. Baldwin, J. C. Gore, R. Schiff, C. L. Arteaga, and H. C. Manning, “Imaging biomarkers predict response to anti-HER2 (ErbB2) therapy in preclinical models of breast cancer,” Clin. Cancer Res.15(14), 4712–4721 (2009).
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K. Vishwanath, H. Yuan, W. T. Barry, M. W. Dewhirst, and N. Ramanujam, “Using optical spectroscopy to longitudinally monitor physiological changes within solid tumors,” Neoplasia11(9), 889–900 (2009).
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Figures (6)

Fig. 1
Fig. 1

Tumor response in trastuzumab-responsive (a-c) and –resistant (d-f) xenografts treated with control IgG and trastuzumab. BT474 (trastuzumab-responsive) tumor growth curves (a). Percent of cells positive for Ki67 (% Ki67 + ), in BT474 tumors (b), and percent of cells positive for CC-3 (% cleaved caspase-3 + ), in BT474 tumors (c) at days 2, 5, and 14 post treatment. HR6 (trastuzumab-resistant) tumor growth curves (d). Ki67 immunohistochemistry in HR6 tumors (e), and CC-3 immunohistochemistry in HR6 tumors (f) at days 2, 5, and 14 post treatment. Green arrows in (a) and (d) indicate treatment timepoints (days 0, 3, 7, 10). Asterisks (*) indicate p<0.05 between control IgG and trastuzumab treated groups. Bar indicates mean with SEM error bars.(modified from Walsh et al, 2013 [31]).

Fig. 2
Fig. 2

Immunohistochemistry of BT474 (a, c) and HR6 (b, d) tumor xenografts. (a, b) VEGF area percentage (number of high expression tumor cells divided by total number of tumor cells) for control IgG and trastuzumab-treated tumors at 2, 5, and 14 days after initial treatment in trastuzumab-responsive BT474 tumors (a) and trastuzumab-resistant HR6 tumors (b). (c, d) CD31 vessel density (number of high expression pixels divided by total number of non-necrotic tumor pixels) in BT474 (c) and HR6 (d) tumors. Bars indicate mean and SEM of data. Asterisks (*) indicate p<0.05 between control IgG and trastuzumab treated groups

Fig. 3
Fig. 3

Representative in vivo hyperspectral time-courses for a single mouse in each treatment group. Colormap indicates sO2 percentage, from 0% (dark blue) to 100% (dark red). Non-vascular tissue is segmented out and indicated by black background. Changes in microvascular morphology and sO2 are seen in all treatment groups. Scale bar (500 microns) is in BT474 Control IgG, Day 2 image.

Fig. 4
Fig. 4

Oxygen saturation (sO2) and vessel densities derived from in vivo hyperspectral time-course. Average vessel sO2 for control IgG and trastuzumab-treated (a) BT474 and (b) HR6 tumors imaged 2, 5, 9, and 14 days after initial treatment. Percent vessel density (vessel area divided by total area) calculated from BT474 (c) and HR6 (d) xenografts. Bars indicate mean and SEM of all images acquired in each group. Asterisks (*) indicate p<0.05 between control IgG and trastuzumab treated groups. Daggers (†) indicate p<0.05 versus day 2 in the same group.

Fig. 5
Fig. 5

Distribution analysis of microvessel segment sO2. (a) Representative histogram and two-Gaussian fit for the sO2 of microvessel segments in BT474 control tumors on day 2 post-treatment. Red x’s indicate histogram probability value, blue curve indicates optimum fit. Changes in the distributions over the time-course (days 2, 5, 9, and 14 post-treatment) for (b) control IgG, and (c) trastuzumab-treated BT474 tumors. Changes in the distributions over the time-course (days 2, 5, 9, and 14 post-treatment) for (d) control IgG, and (e) trastuzumab-treated HR6 tumors.

Fig. 6
Fig. 6

Vessel segment sO2 values of “high sO2” and “low sO2” contributions over the treatment time-course. The sO2 of the “high” component from (a) BT474, and (b) HR6 tumors on days 2, 5, 9, and 14 after initial treatment. sO2 of “low” component from (c) BT474 and (d) HR6 tumors. Asterisks (*) indicate p<0.05 between control IgG and trastuzumab-treated groups. Daggers (†) indicate p<0.05 versus day 2 in the same group. Bars represent mean ± SEM.

Tables (1)

Tables Icon

Table 1 Time-points at which significant changes in histological and hyperspectral endpoints were measured with trastuzumab treatment in BT474 and HR6 xenografts.

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