Near‑infrared fluorescence imaging of prostate cancer using heptamethine carbocyanine dyes

Yuan,Jianlin; Yi,Xiaomin; Yan,Fei; Wang,Fuli; Qin,Weijun; Wu,Guojun; Yang,Xiaojian; Shao,Chen; Chung,Leland  W.K.

doi:10.3892/mmr.2014.2815

Near‑infrared fluorescence imaging of prostate cancer using heptamethine carbocyanine dyes

Authors:
- Jianlin Yuan
- Xiaomin Yi
- Fei Yan
- Fuli Wang
- Weijun Qin
- Guojun Wu
- Xiaojian Yang
- Chen Shao
- Leland W.K. Chung
View Affiliations

Affiliations: Department of Urology, Xijing Hospital, Fourth Military Medical University, Xi'an, Shaanxi 710032, P.R. China, Uro‑Oncology Research Program, Department of Medicine, Cedars‑Sinai Medical Center, Los Angeles, CA 90048, USA
Published online on: October 29, 2014 https://doi.org/10.3892/mmr.2014.2815
Pages: 821-828
Copyright: © Yuan et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY_NC 3.0].

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Near‑infrared fluorescence (NIRF) imaging is an attractive novel modality for the detection of cancer. A previous study defined two organic polymethine cyanine dyes as ideal NIRF probes, IR‑783 and its derivative MHI‑148, which have excellent optical characteristics, superior biocompatibility and cancer targeting abilities. To investigate the feasibility of NIRF dye‑mediated prostate cancer imaging, dye uptake and subcellular co‑localization were investigated in PC‑3, DU‑145 and LNCaP human prostate cancer cells and RWPE‑1 normal prostate epithelial cells. Different organic anion transporting peptide (OATP) inhibitors were utilized to explore the potential role of the OATP subtype, including the nonspecific OATP inhibitor bromosulfophthalein, the OATP1 inhibitor 17β‑estradiol, the selective OATP1B1 inhibitor rifampicin and the selective OATP1B3 inhibitor cholecystokinin octapeptide. NIRF dyes were also used for the simulated detection of circulating tumor cells and the rapid detection of prostate cancer in human prostate cancer tissues and prostate cancer xenografts in mouse models. The results revealed that the cancer‑specific uptake of these organic dyes in prostate cancer cells occurred primarily via OATP1B3. A strong NIRF signal was detected in prostate cancer tissues, but not in normal tissues that were stained with IR‑783. Prostate cancer cells were recognized with particular NIR fluorescence in isolated mononuclear cell mixtures. The results of the present study demonstrated that NIRF dye‑mediated imaging is a feasible and practicable method for prostate cancer detection, although further investigative studies are required before clinical translation.

View Figures

View References

1	Siegel R, Ma J, Zou Z and Jemal A: Cancer statistics, 2014. CA Cancer J Clin. 64:9–29. 2014. View Article : Google Scholar : PubMed/NCBI
2	Cai QY, Yu P, Besch-Williford C, et al: Near-infrared fluorescence imaging of gastrin releasing peptide receptor targeting in prostate cancer lymph node metastases. Prostate. 73:842–854. 2013. View Article : Google Scholar : PubMed/NCBI
3	Osborne JR, Akhtar NH, Vallabhajosula S, Anand A, Deh K and Tagawa ST: Prostate-specific membrane antigen-based imaging. Urol Oncol. 31:144–154. 2013. View Article : Google Scholar
4	Yi X, Wang F, Qin W, Yang X and Yuan J: Near-infrared fluorescent probes in cancer imaging and therapy: an emerging field. Int J Nanomedicine. 9:1347–1365. 2014. View Article : Google Scholar : PubMed/NCBI
5	Yang X, Shao C, Wang R, et al: Optical imaging of kidney cancer with novel near infrared heptamethine carbocyanine fluorescent dyes. Journal Urol. 189:702–710. 2013. View Article : Google Scholar
6	Svoboda M, Riha J, Wlcek K, Jaeger W and Thalhammer T: Organic anion transporting polypeptides (OATPs): regulation of expression and function. Curr Drug Metab. 12:139–153. 2011. View Article : Google Scholar : PubMed/NCBI
7	Obaidat A, Roth M and Hagenbuch B: The expression and function of organic anion transporting polypeptides in normal tissues and in cancer. Annu Rev Pharmacol Toxicol. 52:135–151. 2012. View Article : Google Scholar :
8	Hamada A, Sissung T, Price DK, et al: Effect of SLCO1B3 haplotype on testosterone transport and clinical outcome in caucasian patients with androgen-independent prostatic cancer. Clin Cancer Res. 14:3312–3318. 2008. View Article : Google Scholar : PubMed/NCBI
9	Shimizu Y, Temma T, Hara I, et al: Micelle-based activatable probe for in vivo near-infrared optical imaging of cancer biomolecules. Nanomedicine. 10:187–195. 2014. View Article : Google Scholar
10	Chen Q, Wang C, Cheng L, He W, Cheng Z and Liu Z: Protein modified upconversion nanoparticles for imaging-guided combined photothermal and photodynamic therapy. Biomaterials. 35:2915–2923. 2014. View Article : Google Scholar : PubMed/NCBI
11	Zhang E, Luo S, Tan X and Shi C: Mechanistic study of IR-780 dye as a potential tumor targeting and drug delivery agent. Biomaterials. 35:771–778. 2014. View Article : Google Scholar
12	Yang X, Shi C, Tong R, et al: Near IR heptamethine cyanine dye-mediated cancer imaging. Clin Cancer Research. 16:2833–2844. 2010. View Article : Google Scholar
13	Ismair MG, Stieger B, Cattori V, et al: Hepatic uptake of cholecystokinin octapeptide by organic anion-transporting polypeptides OATP4 and OATP8 of rat and human liver. Gastroenterology. 121:1185–1190. 2001. View Article : Google Scholar : PubMed/NCBI
14	Karlgren M, Vildhede A, Norinder U, et al: Classification of inhibitors of hepatic organic anion transporting polypeptides (OATPs): influence of protein expression on drug-drug interactions. J Med Chem. 55:4740–4763. 2012. View Article : Google Scholar : PubMed/NCBI
15	Gui C, Wahlgren B, Lushington GH and Hagenbuch B: Identification, Ki determination and CoMFA analysis of nuclear receptor ligands as competitive inhibitors of OATP1B1-mediated estradiol-17beta-glucuronide transport. Pharmacol Res. 60:50–56. 2009. View Article : Google Scholar : PubMed/NCBI
16	He W, Kularatne SA, Kalli KR, et al: Quantitation of circulating tumor cells in blood samples from ovarian and prostate cancer patients using tumor-specific fluorescent ligands. International J Cancer. 123:1968–1973. 2008. View Article : Google Scholar
17	Yi X, Zhang G and Yuan J: Renoprotective role of fenoldopam pretreatment through hypoxia-inducible factor-1alpha and heme oxygenase-1 expressions in rat kidney transplantation. Transplant Proc. 45:517–522. 2013. View Article : Google Scholar : PubMed/NCBI
18	Valentim AM, Alves HC, Olsson IA and Antunes LM: The effects of depth of isoflurane anesthesia on the performance of mice in a simple spatial learning task. J Am Assoc Lab Anim Sci. 47:16–19. 2008.PubMed/NCBI
19	Wu TT, Sikes RA, Cui Q, et al: Establishing human prostate cancer cell xenografts in bone: induction of osteoblastic reaction by prostate-specific antigen-producing tumors in athymic and SCID/bg mice using LNCaP and lineage-derived metastatic sublines. Int J Cancer. 77:887–894. 1998. View Article : Google Scholar : PubMed/NCBI
20	Yuan A, Wu J, Tang X, Zhao L, Xu F and Hu Y: Application of near-infrared dyes for tumor imaging, photothermal, and photodynamic therapies. J Pharm Sci. 102:6–28. 2013. View Article : Google Scholar
21	Buxhofer-Ausch V, Secky L, Wlcek K, et al: Tumor-specific expression of organic anion-transporting polypeptides: transporters as novel targets for cancer therapy. J Drug Deliv. Feb 3–2013.(Epub ahead of print). View Article : Google Scholar : PubMed/NCBI
22	Wright JL, Kwon EM, Ostrander EA, et al: Expression of SLCO transport genes in castration-resistant prostate cancer and impact of genetic variation in SLCO1B3 and SLCO2B1 on prostate cancer outcomes. Cancer Epidemiol Biomarkers Prev. 20:619–627. 2011. View Article : Google Scholar : PubMed/NCBI
23	Shao C, Liao CP, Hu P, et al: Detection of live circulating tumor cells by a class of near-infrared heptamethine carbocyanine dyes in patients with localized and metastatic prostate cancer. PloS On. 9:e889672014. View Article : Google Scholar
24	Tjensvoll K, Nordgård O and Smaaland R: Circulating tumor cells in pancreatic cancer patients: Methods of detection and clinical implications. Int J Cancer. 134:1–8. 2014. View Article : Google Scholar
25	Thalgott M, Rack B, Maurer T, et al: Detection of circulating tumor cells in different stages of prostate cancer. J Cancer Res Clin Oncol. 139:755–763. 2013. View Article : Google Scholar : PubMed/NCBI
26	Hellebust A and Richards-Kortum R: Advances in molecular imaging: targeted optical contrast agents for cancer diagnostics. Nanomedicine (Lond). 7:429–445. 2012. View Article : Google Scholar
27	Fomina N, McFearin CL, Sermsakdi M, Morachis JM and Almutairi A: Low power, biologically benign NIR light triggers polymer disassembly. Macromolecules. 44:8590–8597. 2011. View Article : Google Scholar : PubMed/NCBI
28	Muselaers CH, Stillebroer AB, Rijpkema M, et al: Optical imaging of renal cell carcinoma with anti-carbonic anhydrase IX monoclonal antibody girentuximab. J Nucl Med. 55:1035–1040. 2014. View Article : Google Scholar : PubMed/NCBI
29	Cheng K and Cheng Z: Near infrared receptor-targeted nanoprobes for early diagnosis of cancers. Curr Med Chem. 19:4767–4785. 2012. View Article : Google Scholar : PubMed/NCBI
30	Bai M and Bornhop DJ: Recent advances in receptor-targeted fluorescent probes for in vivo cancer imaging. Curr Med Chem. 19:4742–4758. 2012. View Article : Google Scholar : PubMed/NCBI
31	Letschert K, Faulstich H, Keller D and Keppler D: Molecular characterization and inhibition of amanitin uptake into human hepatocytes. Toxicol Sci. 91:140–149. 2006. View Article : Google Scholar : PubMed/NCBI
32	Pressler H, Sissung TM, Venzon D, Price DK and Figg WD: Expression of OATP family members in hormone-related cancers: potential markers of progression. PloS One. 6:e203722011. View Article : Google Scholar : PubMed/NCBI
33	Shan L: Near-infrared fluorescence 1,1-dioctadecyl-3,3,3,3- tetramethylindotricarbocyanine iodide (DiR)-labeled macrophages for cell imaging. Molecular Imaging and Contrast Agent Database (MICAD) Bethesda (MD): 2004
34	Zharov VP, Galanzha EI, Shashkov EV, Khlebtsov NG and Tuchin VV: In vivo photoacoustic flow cytometry for monitoring of circulating single cancer cells and contrast agents. Opt Lett. 31:3623–3625. 2006. View Article : Google Scholar : PubMed/NCBI
35	Qiao XF, Zhou JC, Xiao JW, Wang YF, Sun LD and Yan CH: Triple-functional core-shell structured upconversion luminescent nanoparticles covalently grafted with photosensitizer for luminescent, magnetic resonance imaging and photodynamic therapy in vitro. Nanoscale. 4:4611–4623. 2012. View Article : Google Scholar : PubMed/NCBI
36	Kim JS, Kim YH, Kim JH, et al: Development and in vivo imaging of a PET/MRI nanoprobe with enhanced NIR fluorescence by dye encapsulation. Nanomedicine (Lond). 7:219–229. 2012. View Article : Google Scholar
37	Guo Y, Yuan H, Cho H, et al: High efficiency diffusion molecular retention tumor targeting. PloS One. 8:e582902013. View Article : Google Scholar : PubMed/NCBI