Metastatic status of sentinel lymph nodes in breast cancer determined with photoacoustic microscopy via dual-targeting nanoparticles

Yanfeng Dai; Xiang Yu; Jianshuang Wei; Fanxin Zeng; Yiran Li; Xiaoquan Yang; Qingming Luo; Zhihong Zhang

doi:10.1038/s41377-020-00399-0

Go to Nature Website

Your Location：

Home >

Browse articles >

Metastatic status of sentinel lymph nodes in breast cancer determined with photoacoustic microscopy via dual-targeting nanoparticles

Original Articles

- Metastatic status of sentinel lymph nodes in breast cancer determined with photoacoustic microscopy via dual-targeting nanoparticles
- Metastatic status of sentinel lymph nodes in breast cancer determined with photoacoustic microscopy via dual-targeting nanoparticles
- LSA 2020年9卷第5期页码：1562-1577
- Affiliations：
  
  1.Britton Chance Center and MOE Key Laboratory for Biomedical Photonics, School of Engineering Sciences, Wuhan National Laboratory for Optoelectronics–Huazhong University of Science and Technology, Wuhan, Hubei 430074, China
  2.School of Biomedical Engineering, Hainan University, Haikou, Hainan 570228, China
- Author bio：
  
  Qingming Luo (qluo@hainanu.edu.cn)
  Zhihong Zhang (czyzzh@mail.hust.edu.cn)
- Funds：
- DOI：10.1038/s41377-020-00399-0
  中图分类号：
- 纸质出版日期：2020，
  
  网络出版日期：2020-09-16，
  
  收稿日期：2020-05-03，
  
  修回日期：2020-08-14，
  
  录用日期：2020-09-01
- Accepted：
Scan QR Code
Metastatic status of sentinel lymph nodes in breast cancer determined with photoacoustic microscopy via dual-targeting nanoparticles[J]. LSA, 2020,9(5):1562-1577.

Dai, Y. F. et al. Metastatic status of sentinel lymph nodes in breast cancer determined with photoacoustic microscopy via dual-targeting nanoparticles. Light: Science & Applications, 9, 1562-1577 (2019).
Metastatic status of sentinel lymph nodes in breast cancer determined with photoacoustic microscopy via dual-targeting nanoparticles[J]. LSA, 2020,9(5):1562-1577. DOI： 10.1038/s41377-020-00399-0.

Dai, Y. F. et al. Metastatic status of sentinel lymph nodes in breast cancer determined with photoacoustic microscopy via dual-targeting nanoparticles. Light: Science & Applications, 9, 1562-1577 (2019). DOI： 10.1038/s41377-020-00399-0.

摘要

Abstract

Detection of sentinel lymph nodes (SLNs) is critical to gui

de the treatment of breast cancer. However

distinguishing metastatic SLNs from normal and inflamed lymph nodes (LNs) during surgical resection remains a challenge. Here

we report a CD44 and scavenger receptor class B1 dual-targeting hyaluronic acid nanoparticle (5K-HA-HPPS) loaded with the near-infra-red fluorescent dye DiR-BOA for SLN imaging in breast cancer. The small sized (~40 nm) self-assembled 5K-HA-HPPSs accumulated rapidly in the SLNs after intradermal injection. Compared with normal popliteal LNs (N-LN)

there were ~3.2-fold and ~2.4-fold increases in fluorescence intensity in tumour metastatic SLNs (T-MLN) and inflamed LNs (Inf-LN)

respectively

6 h after nanoparticle inoculation. More importantly

photoacoustic microscopy (PAM) of 5K-HA-HPPS showed a significantly distinct distribution in T-MLN compared with N-LN and Inf-LN. Signals were mainly distributed at the centre of T-MLN but at the periphery of N-LN and Inf-LN. The ratio of PA intensity (R) at the centre of the LNs compared with that at the periphery was 5.93 ± 0.75 for T-MLNs of the 5K-HA-HPPS group

which was much higher than that for the Inf-LNs (

= 0.2 ± 0.07) and N-LNs (

= 0.45 ± 0.09). These results suggest that 5K-HA-HPPS injection combined with PAM provides a powerful tool for distinguishing metastatic SLNs from pLNs and inflamed LNs

thus guiding the removal of SLNs during breast cancer surgery.

关键词

Keywords

references

Siegel, R. L., Miller, K. D.&Jemal, A. Cancer statistics, 2019.CA: Cancer J. Clin.69, 7–34 (2019)..

Bray, F. et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.CA: A Cancer J. Clin.68, 394–424 (2018)..

Mehta, R. S. et al. Overall survival with fulvestrant plus anastrozole in metastatic breast cancer.N. Engl. J. Med.380, 1226–1234 (2019)..

McGuire, A., Brown, J. A. L.&Kerin, M. J. Metastatic breast cancer: the potential of miRNA for diagnosis and treatment monitoring.Cancer Metastasis Rev.34, 145–155 (2015)..

Hayes, D. F. HER2 and breast cancer—a phenomenal success story.N. Engl. J. Med.381, 1284–1286 (2019)..

Lowes, S. et al. Evolving imaging techniques for staging axillary lymph nodes in breast cancer.Clin. Radiol.73, 396–409 (2018)..

Veronesi, U. et al. Sentinel lymph node biopsy in breast cancer: ten-year results of a randomized controlled study.Ann. Surg.251, 595–600 (2010)..

Ahmed, M., Purushotham, A. D.&Douek, M. Novel techniques for sentinel lymph node biopsy in breast cancer: a systematic review.Lancet Oncol.15, e351–e362 (2014)..

Soares, E. W. S. et al. Morbidity after conventional dissection of axillary lymph nodes in breast cancer patients.World J. Surg. Oncol.12, 67 (2014)..

Bello, M. A. et al. Incidence complications following sentinel lymph node biopsy or axillary lymph node dissection after breast cancer surgery.J. Clin. Oncol.30, 97 (2012)..

Yoo, J. S. et al. A macrophage-specific fluorescent probe for intraoperative lymph node staging.Cancer Res.74, 44–55 (2014)..

Liu, J. et al. Percutaneous contrast-enhanced ultrasound for localization and diagnosis of sentinel lymph node in early breast cancer.Sci. Rep.9, 13545 (2019)..

Zhou, Z. J. et al. A protein-corona-freeT1-T2dual-modal contrast agent for accurate imaging of lymphatic tumor metastasis.ACS Appl. Mater. Interfaces7, 28286–28293 (2015)..

Zhang, F. et al. Differentiation of reactive and tumor metastatic lymph nodes with diffusion-weighted and SPIO-enhanced MRI.Mol. Imaging Biol.15, 40–47 (2013)..

Sun, P. P. et al. Image-guided surgery of head and neck carcinoma in rabbit models by intra-operatively defining tumour-infiltrated margins and metastatic lymph nodes.EBioMedicine50, 93–102 (2019)..

Toole, B. P. Hyaluronan: from extracellular glue to pericellular cue.Nat. Rev. Cancer4, 528–539 (2004)..

Burdick, J. A.&Prestwich, G. D. Hyaluronic acid hydrogels for biomedical applications.Adv. Mater.23, H41–H56 (2011)..

Götte, M.&Yip, G. W. Heparanase, hyaluronan, and CD44 in cancers: a breast carcinoma perspective.Cancer Res.66, 10233–10237 (2006)..

Aguiar, D. J., Knudson, W.&Knudson, C. B. Internalization of the hyaluronan receptor CD44 by chondrocytes.Exp. Cell Res.252, 292–302 (1999)..

Katoh, S. et al. Glycosylation of CD44 negatively regulates its recognition of hyaluronan.J. Exp. Med.182, 419–429 (1995)..

Qian, Y. et al. Targeting dendritic cells in lymph node with an antigen peptide-based nanovaccine for cancer immunotherapy.Biomaterials98, 171–183 (2016)..

Hameed, S. et al. Fluorescence guided sentinel lymph node mapping: from current molecular probes to future multimodal nanoprobes.Bioconjugate Chem.30, 13–28 (2019)..

Trevaskis, N. L., Kaminskas, L. M.&Porter, C. J. H. From sewer to saviour—targeting the lymphatic system to promote drug exposure and activity.Nat. Rev. Drug Discov.14, 781–803 (2015)..

Zhang, Z. H. et al. HDL-mimicking peptide-lipid nanoparticles with improved tumor targeting.Small6, 430–437 (2010)..

Yu, X. et al. Melittin-lipid nanoparticles target to lymph nodes and elicit a systemic anti-tumor immune response.Nat. Commun.11, 1110 (2020)..

Tan, T. et al. Bioinspired lipoproteins-mediated photothermia remodels tumor stroma to improve cancer cell accessibility of second nanoparticles.Nat. Commun.10, 3322 (2019)..

Yu, X. et al. Immune modulation of liver sinusoidal endothelial cells by melittin nanoparticles suppresses liver metastasis.Nat. Commun.10, 574 (2019)..

Lin, Q. Y. et al. Self-assembled "Off/On" nanopomegranate for in vivo photoacoustic and fluorescence imaging: strategic arrangement of Kupffer cells in mouse hepatic lobules.ACS Nano13, 1526–1537 (2019)..

Fu, Q. R. et al. Photoacoustic imaging: contrast agents and their biomedical applications.Adv. Mater.31, 1805875 (2019)..

Men, X. J.&Yuan, Z. Multifunctional conjugated polymer nanoparticles for photoacoustic-based multimodal imaging and cancer photothermal therapy.J. Innov. Optical Health Sci.12, 1930001 (2019)..

Seong, M.&Chen, S. L. Recent advances toward clinical applications of photoacoustic microscopy: a review.Sci. Chin. Life Sci.https://doi.org/10.1007/s11427-019-1628-7https://doi.org/10.1007/s11427-019-1628-7(2020)..

Coutant, C. et al. Comparison of models to predict nonsentinel lymph node status in breast cancer patients with metastatic sentinel lymph nodes: a prospective multicenter study.J. Clin. Oncol.27, 2800–2808 (2009)..

Faries, M. B. et al. Completion dissection or observation for sentinel-node metastasis in melanoma.N. Engl. J. Med.376, 2211–2222 (2017)..

Wu, Y. L. et al. A nanoprobe for diagnosing and mapping lymphatic metastasis of tumor using 3D multispectral optoacoustic tomography owing to aggregation/deaggregation induced spectral change.Adv. Funct. Mater.29, 1807960 (2019)..

Zang, J. et al. Combined68Ga-NOTA-evans blue lymphoscintigraphy and68Ga-NOTA-RM26 PET/CT evaluation of sentinel lymph node metastasis in breast cancer patients.Bioconjugate Chem.31, 396–403 (2020)..

Tang, L. et al. Aptamer-functionalized, ultra-small, monodisperse silica nanoconjugates for targeted dual-modal imaging of lymph nodes with metastatic tumors.Angew. Chem. Int. Ed.51, 12721–12726 (2012)..

Wu, X. S. et al. Inflammation and tumor microenvironment in lymph node metastasis.Cancers3, 927–944 (2011)..

Giuliano, A. E. et al. Effect of axillary dissection vs no axillary dissection on 10-year overall survival among women with invasive breast cancer and sentinel node metastasis: the ACOSOG Z0011 (Alliance) randomized clinical trial.JAMA318, 918–926 (2017)..

Rinaldi, E.&Baggi, F. LYVE-1 is 'on stage' now: an emerging player in dendritic cell docking to lymphatic endothelial cells.Cell. Mol. Immunol.15, 663–665 (2018)..

Banerji, S. et al. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan.J. Cell Biol.144, 789–801 (1999)..

Yang, X. Y. et al. Mapping sentinel lymph node metastasis by dual-probe optical imaging.Theranostics7, 153–163 (2017)..

Jin, H. L. et al. Magnetic enrichment of dendritic cell vaccine in lymph node with fluorescent-magnetic nanoparticles enhanced cancer immunotherapy.Theranostics6, 2000–2014 (2016)..

Lu, L. S. et al. Targeted immunomodulation of inflammatory monocytes across the blood-brain barrier by curcumin-loaded nanoparticles delays the progression of experimental autoimmune encephalomyelitis.Biomaterials245, 119987 (2020)..

Liang, C. et al. Tumor metastasis inhibition by imaging-guided photothermal therapy with single-walled carbon nanotubes.Adv. Mater.26, 5646–5652 (2014)..

Wang, Y. et al. In vivo albumin labeling and lymphatic imaging.Proc. Natl Acad. Sci. USA112, 208–213 (2015)..

Qiao, R. R. et al. Ultrasensitive in vivo detection of primary gastric tumor and lymphatic metastasis using upconversion nanoparticles.ACS Nano9, 2120–2129 (2015)..

Akers, W. J. et al. Noninvasive photoacoustic and fluorescence sentinel lymph node identification using dye-loaded perfluorocarbon nanoparticles.ACS Nano5, 173–182 (2011)..

Pan, D. et al. Photoacoustic sentinel lymph node imaging with self-assembled copper neodecanoate nanoparticles.ACS Nano6, 1260–1267 (2012)..

Chen, Q. et al. H2O2-responsive liposomal nanoprobe for photoacoustic inflammation imaging and tumor theranostics via in vivo chromogenic assay.Proc. Natl Acad. Sci. USA114, 5343–5348 (2017)..

Luke, G. P. et al. Sentinel lymph node biopsy revisited: ultrasound-guided photoacoustic detection of micrometastases using molecularly targeted plasmonic nanosensors.Cancer Res.74, 5397–5408 (2014)..

Corbin, I. R. et al. Enhanced cancer-targeted delivery using engineered high-density lipoprotein-based nanocarriers.J. Biomed. Nanotechnol.3, 367–376 (2007)..

Luo, H. M. et al. Tetrameric far-red fluorescent protein as a scaffold to assemble an octavalent peptide nanoprobe for enhanced tumor targeting and intracellular uptakein vivo.FASEB J.25, 1865–1873 (2011)..

Surace, C. et al. Lipoplexes targeting the CD44 hyaluronic acid receptor for efficient transfection of breast cancer cells.Mol. Pharm.6, 1062–1073 (2009)..

浏览量

Downloads

CSCD

文章被引用时，请邮件提醒。

Submit

工具集

关联资源

暂无数据