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      Intraoperative imaging of hepatic cancers using γ-glutamyltranspeptidase-specific fluorophore enabling real-time identification and estimation of recurrence

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          Abstract

          γ-Glutamyltranspeptidase (GGT) is upregulated in a variety of human cancers including primary and secondary hepatic tumors. This motivated us to use γ-glutamyl hydroxymethyl rhodamine green (gGlu-HMRG), a novel fluorophore emitting light at around 520 nm following enzymatic reaction with GGT, as a tool for the intraoperative identification of hepatic tumors. gGlu-HMRG was topically applied to 103 freshly resected hepatic specimens. Fluorescence imaging using gGlu-HMRG identified hepatic tumors with the sensitivity/specificity of 48%/96% for hepatocellular carcinoma, 100%/100% for intrahepatic cholangiocarcinoma, and 87%/100% for colorectal liver metastasis. High gGlu-HMRG fluorescence intensity was positively associated with the incidence of microscopic vascular invasion in HCC and the risk of early postoperative recurrence in CRLM. These results suggest that gGlu-HMRG imaging could not only be a useful intraoperative navigation tool but also provide information related to postoperative disease recurrence.

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          Real-time identification of liver cancers by using indocyanine green fluorescent imaging.

          Koichi Masuda, NORIYOSHI FUKUSHIMA, Taku Aoki … (2009)
          We have often encountered difficulties in identifying small liver cancers during surgery. Fluorescent imaging using indocyanine green (ICG) has the potential to detect liver cancers through the visualization of the disordered biliary excretion of ICG in cancer tissues and noncancerous liver tissues compressed by the tumor. ICG had been intravenously injected for a routine liver function test in 37 patients with hepatocellular carcinoma (HCC) and 12 patients with metastasis of colorectal carcinoma (CRC) before liver resection. Surgical specimens were investigated using a near-infrared light camera system. Among the 49 subjects, the 26 patients examined during the latter period of the study (20 with HCC and 6 with metastasis) underwent ICG-fluorescent imaging of the liver surfaces before resection. ICG-fluorescent imaging identified all of the microscopically confirmed HCCs (n = 63) and CRC metastases (n = 28) in surgical specimens. Among the 63 HCCs, 8 tumors (13%, including 5 early HCCs) were not evident grossly unless observed by ICG-fluorescent imaging. Five false-positive nodules (4 large regenerative nodules and 1 bile duct proliferation) were identified among the fluorescent lesions. Well-differentiated HCCs appeared as uniformly fluorescing lesions with higher lesion-to-liver contrast than that of moderately or poorly differentiated HCCs (162.6 [71.1-218.2] per pixel vs 67.7 [-6.3-211.2] per pixel, P < .001), while CRC metastases were delineated as rim-fluorescing lesions. Fluorescent microscopy confirmed that fluorescence originated in the cytoplasm and pseudoglands of HCC cells and in the noncancerous liver parenchyma surrounding metastases. ICG-fluorescent imaging before resection identified 21 of the 41 HCCs (51%) and all of the 16 metastases that were examined. ICG-fluorescent imaging enables the highly sensitive identification of small and grossly unidentifiable liver cancers in real time, enhancing the accuracy of liver resection and operative staging. (c) 2009 American Cancer Society.
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            High resistance to cisplatin in human ovarian cancer cell lines is associated with marked increase of glutathione synthesis.

            A K Godwin, A MEISTER, P O'Dwyer … (1992)
            Exposure of human ovarian tumor cell lines to cisplatin led to development of cell lines that exhibited increasing degrees of drug resistance, which were closely correlated with increase of the levels of cellular glutathione. Cell lines were obtained that showed 30- to 1000-fold increases in resistance; these cells also had strikingly increased (13- to 50-fold) levels of glutathione as compared with the drug-sensitive cells of origin. These levels of resistance to cisplatin and the cellular glutathione levels are substantially greater than previously reported. Very high cisplatin resistance was associated with enhanced expression of mRNAs for gamma-glutamylcysteine synthetase and gamma-glutamyl transpeptidase; immunoblots showed increase of gamma-glutamylcysteine synthetase but not of glutathione synthetase. Glutathione S-transferase activity was unaffected, as determined with chlorodinitrobenzene as a substrate. These studies suggest the potential value of examining regulation of glutathione synthesis as an indicator of clinical prognosis. The highly resistant cell lines are proving useful for studying the multiple mechanisms by which tumor cells acquire drug- and radiation-resistance.
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              Selective molecular imaging of viable cancer cells with pH-activatable fluorescence probes.

              Yasuteru Urano, Daisuke Asanuma, Yukihiro Hama … (2009)
              A long-term goal of cancer diagnosis is to develop tumor-imaging techniques that have sufficient specificity and sensitivity. To achieve this goal, minimizing the background signal originating from nontarget tissues is crucial. Here we achieve highly specific in vivo cancer visualization by using a newly designed targeted 'activatable' fluorescent imaging probe. This agent is activated after cellular internalization by sensing the pH change in the lysosome. Novel acidic pH-activatable probes based on the boron-dipyrromethene fluorophore were synthesized and then conjugated to a cancer-targeting monoclonal antibody. As proof of concept, ex vivo and in vivo imaging of human epidermal growth factor receptor type 2-positive lung cancer cells in mice was performed. The probe was highly specific for tumors with minimal background signal. Furthermore, because the acidic pH in lysosomes is maintained by the energy-consuming proton pump, only viable cancer cells were successfully visualized. The design concept can be widely adapted to cancer-specific, cell surface-targeting molecules that result in cellular internalization.
              Article 0 comments Cited 159 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Takeaki Ishizawa: tish-tky@umin.ac.jp
                Yasuteru Urano: uranokun@m.u-tokyo.ac.jp
                Journal
                Journal ID (nlm-ta): Sci Rep
                Journal ID (iso-abbrev): Sci Rep
                Title: Scientific Reports
                Publisher: Nature Publishing Group UK (London )
                ISSN (Electronic): 2045-2322
                Publication date (Electronic): 14 June 2017
                Publication date PMC-release: 14 June 2017
                Publication date Collection: 2017
                Volume: 7
                Electronic Location Identifier: 3542
                Affiliations
                [1 ]ISNI 0000 0001 2151 536X, GRID grid.26999.3d, Hepato-Biliary-Pancreatic Surgery Division, Department of Surgery, Graduate School of Medicine, , The University of Tokyo, ; Tokyo, Japan
                [2 ]ISNI 0000 0001 0037 4131, GRID grid.410807.a, Department of Gastroenterological Surgery, Cancer Institute Hospital, , Japanese Foundation for Cancer Research, ; Tokyo, Japan
                [3 ]ISNI 0000 0001 2151 536X, GRID grid.26999.3d, Laboratory of Chemical Biology and Molecular Imaging, Graduate School of Medicine, , The University of Tokyo, ; Tokyo, Japan
                [4 ]ISNI 0000 0004 1754 9200, GRID grid.419082.6, PRESTO, , Japan Science and Technology Agency, ; Saitama, Japan
                [5 ]ISNI 0000 0001 2151 536X, GRID grid.26999.3d, Department of Pathology, Graduate School of Medicine, , The University of Tokyo, ; Tokyo, Japan
                [6 ]ISNI 0000 0001 2151 536X, GRID grid.26999.3d, Graduate School of Pharmaceutical Sciences, , The University of Tokyo, ; Tokyo, Japan
                [7 ]ISNI 0000 0004 5373 4593, GRID grid.480536.c, CREST, , Japan Agency for Medical Research and Development, ; Tokyo, Japan
                Article
                Publisher ID: 3760
                DOI: 10.1038/s41598-017-03760-3
                PMC ID: 5471246
                PubMed ID: 28615696
                SO-VID: be7b7b3a-2681-4bb1-907f-ed2f3ecd5093
                Copyright © © The Author(s) 2017
                License:

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                Date received : 10 February 2017
                Date accepted : 3 May 2017
                Categories
                Subject: Article
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                issue-copyright-statement © The Author(s) 2017

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