In Vivo Lymphatic Imaging of a Human Inflammatory Breast Cancer Model

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Abstract

Background: Inflammatory breast cancer (IBC) remains the most aggressive type of breast cancer with the greatest potential for metastasis and as a result, the highest mortality rate. IBC cells invade and metastasize through dermal lymphatic vessels; however, it is unknown how lymphatic drainage patterns change during IBC growth and metastasis. Herein, we non-invasively and longitudinally imaged lymphatics in an animal model of IBC using near-infrared fluorescence (NIRF) imaging.

Materials and methods: Mice were imaged in vivo prior to, and up to 11 weeks after subcutaneous or orthotopic inoculation of human IBC SUM149 cells, which were stably transfected with infrared fluorescence protein (iRFP) gene reporter (SUM149-iRFP), following intradermal (i.d.) injection of indocyanine green (ICG).

Results: Fluorescence images showed well-defined lymphatic vessels prior to SUM149-iRFP inoculation. However, altered lymphatic drainage patterns including rerouting of lymphatic drainage were detected in mice with SUM149-iRFP, due to lymphatic obstruction of normal lymphatic drainages caused by tumor growth. In addition, we observed tortuous lymphatic vessels and extravasation of ICG-laden lymph in mice with SUM149-iRFP. We also observed increased and dilated fluorescent lymphatic vessels in the tumor periphery, which was confirmed by ex vivo immunohistochemical staining of lymphatic vessels.

Conclusions: Our pre-clinical studies demonstrate that non-invasive NIRF imaging can provide a method to assess changes in lymphatic drainage patterns during IBC growth and metastasis.

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Most cited references 37

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Bright and stable near infra-red fluorescent protein for in vivo imaging

Grigory Filonov, Kiryl D. Piatkevich, Li-Min Ting … (2011)

The ability of non-invasive monitoring of deep-tissue developmental, metabolic, and pathogenic processes will advance modern biotechnology. Imaging of live mammals using fluorescent probes is more feasible within a “near-infrared optical window” (NIRW) 1 . Here we report a phytochrome-based near infra-red fluorescent protein (iRFP) with the excitation/emission maxima at 690/713 nm. Bright fluorescence in a living mouse proved iRFP to be a superior probe for non-invasive imaging of internal mammalian tissues. Its high intracellular stability, low cytotoxicity, and lack of the requirement to add external biliverdin-chromophore makes iRFP as easy to use as conventional GFP-like proteins. Compared to earlier phytochrome-derived fluorescent probes, the iRFP protein has better in vitro characteristics and performs well in cells and in vivo, having greater effective brightness and photostability. Compared to the far-red GFP-like proteins, iRFP has substantially higher signal to background ratio in a mouse model owing to its infra-red shifted spectra.

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Trends in inflammatory breast carcinoma incidence and survival: the surveillance, epidemiology, and end results program at the National Cancer Institute.

Kenneth Hance, Brent Anderson, William H. Levine … (2005)

Inflammatory breast carcinoma (IBC) appears to be a clinicopathologic entity distinct from noninflammatory locally advanced breast cancer (LABC). We examined incidence and survival trends for IBC in Surveillance, Epidemiology, and End Results (SEER) Program data with a case definition designed to capture many of its unique clinical and pathologic characteristics. We analyzed breast cancer cases diagnosed in the SEER 9 Registries (n = 180,224), between 1988 and 2000. Breast cancer cases were categorized using SEER's "Extent of Disease" codes in combination with International Classification of Diseases for Oncology morphology code 8530/3 and classified as IBC (n = 3648), LABC (n = 3636), and non-T4 breast cancer (n = 172,940). We compared changes in incidence rates over 3-year intervals by breast cancer subtype and race using SEER*Stat. Survival differences by breast cancer subtype and race were assessed using Kaplan-Meier curves and log-rank statistics. All statistical tests were two-sided. Between 1988 and 1990 and 1997 and 1999, IBC incidence rates (per 100,000 woman-years) increased from 2.0 to 2.5 (P 10 years, P < .0001). Black women with IBC or LABC had poorer survival than white women with IBC or LABC, respectively (log-rank test, P < .001). Throughout the 1990s, IBC incidence rose, and survival improved modestly. Substantial racial differences were noted in age at diagnosis, age-specific incidence rates, and survival outcomes.

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Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome.

X Shu, A Royant, M. Lin … (2009)

Visibly fluorescent proteins (FPs) from jellyfish and corals have revolutionized many areas of molecular and cell biology, but the use of FPs in intact animals, such as mice, has been handicapped by poor penetration of excitation light. We now show that a bacteriophytochrome from Deinococcus radiodurans, incorporating biliverdin as the chromophore, can be engineered into monomeric, infrared-fluorescent proteins (IFPs), with excitation and emission maxima of 684 and 708 nm, respectively; extinction coefficient >90,000 M(-1) cm(-1); and quantum yield of 0.07. IFPs express well in mammalian cells and mice and spontaneously incorporate biliverdin, which is ubiquitous as the initial intermediate in heme catabolism but has negligible fluorescence by itself. Because their wavelengths penetrate tissue well, IFPs are suitable for whole-body imaging. The IFPs developed here provide a scaffold for further engineering.

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Author and article information

Journal

Journal ID (nlm-ta): J Cancer

Journal ID (iso-abbrev): J Cancer

Journal ID (publisher-id): jca

Title: Journal of Cancer

Publisher: Ivyspring International Publisher (Sydney )

ISSN (Electronic): 1837-9664

Publication date Collection: 2014

Publication date (Electronic): 23 October 2014

Volume: 5

Issue: 9

Pages: 774-783

Affiliations

1. Center for Molecular Imaging, The Brown Foundation Institute of Molecular Medicine, The University of Texas Health Science Center, Houston, TX 77030;

2. The University of Texas Graduate School of Biomedical Sciences at Houston. The University of Texas MD Anderson Cancer Center, Houston, Texas 77030.

Author notes

✉ Corresponding author: Sunkuk Kwon, Ph.D., University of Texas Health Science Center at Houston, 1825 Pressler St, SRB 330F, Houston, TX 77030.

Conflicts of Interest: Dr. Sevick-Muraca declares financial interest in the NIRF Imaging, Inc., a company seeking to commercialize NIRF lymphatic imaging. No other conflicts of interest are declared for the remaining authors.

Article

Publisher ID: jcav05p0774

DOI: 10.7150/jca.9835

PMC ID: 4216802

PubMed ID: 25368678

SO-VID: 2e761a98-2480-4705-b7fc-e100b2ce43a7

Copyright © © Ivyspring International Publisher. This is an open-access article distributed under the terms of the Creative Commons License (http://creativecommons.org/licenses/by-nc-nd/3.0/). Reproduction is permitted for personal, noncommercial use, provided that the article is in whole, unmodified, and properly cited.

In Vivo Lymphatic Imaging of a Human Inflammatory Breast Cancer Model

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Karger: Oncology

Most cited references 37

Bright and stable near infra-red fluorescent protein for in vivo imaging

Trends in inflammatory breast carcinoma incidence and survival: the surveillance, epidemiology, and end results program at the National Cancer Institute.

Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome.

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