Journal Home > Volume 15 , Issue 7

Oral cancer is a common malignant tumor of the head and neck, and surgery combined with radiotherapy and chemotherapy is the primary treatment modality. However, a positive resection margin that may lead to recurrence after surgery has always been a critical issue to address. Furthermore, radiotherapy and chemotherapy also have shortcomings such as resistance to chemotherapy and radiation, lack of targeting, and severe side effects. Therefore, exploring new methods of tumor surgical navigation and tumor treatment is of great significance for oral cancer. Although, the emerging near-infrared II (NIR-II, 1,000–1,700 nm) region fluorescent imaging has revolutionized surgical navigation, a high tumor-targeting fluorescent probe remains lacking. Furthermore, while emerging photothermal therapy (PTT) can overcome chemoradiotherapy’s shortcomings and achieve precise treatment of tumors, its clinical application is still limited by the lack of high photothermal conversion efficiency, high photothermal stability, and highly penetrating materials. Herein, a NIR-II dye SQ890 is developed for tumor imaging and PTT of oral cancer. By assembling into nanoparticles (NPs) and being modified with epithelial growth factor receptor (EGFR)-targeting peptides GE11, SQ890 NPs-Pep can specifically accumulate in tumor sites via active targeting, and realize photoacoustic/NIR-II fluorescence dual-modality imaging-guided PTT of oral cancer.


menu
Abstract
Full text
Outline
Electronic supplementary material
About this article

NIR-II emissive dye based polymer nanoparticle targeting EGFR for oral cancer theranostics

Show Author's information Mingjian Ling1,2,§Rui Sun1,§Guang Li3Madiha Zahra Syeda4Wen Ma1Ziyi Mai1Longquan Shao2( )Longguang Tang5( )Zhiqiang Yu1( )
School of Pharmaceutical Sciences, Guangdong Provincial Key Laboratory of New Drug Screening, Southern Medical University, Guangzhou 510632, China
Nanfang Hospital, Southern Medical University, Guangzhou 510515, China
Department of Obstetrics and Gynecology, The Third Affiliated Hospital of Southern Medical University, Guangzhou 510632, China
Department of Pharmacology and Department of Respiratory and Critical Care Medicine of the Second Affiliated Hospital, Zhejiang University School of Medicine, Key Laboratory of Respiratory Disease of Zhejiang Province, Hangzhou 310009, China
The Fourth Affiliated Hospital, International Institutes of Medicine, Zhejiang University School of Medicin, Jinhua 322000, China

§ Mingjian Ling and Rui Sun contributed equally to this work.

Abstract

Oral cancer is a common malignant tumor of the head and neck, and surgery combined with radiotherapy and chemotherapy is the primary treatment modality. However, a positive resection margin that may lead to recurrence after surgery has always been a critical issue to address. Furthermore, radiotherapy and chemotherapy also have shortcomings such as resistance to chemotherapy and radiation, lack of targeting, and severe side effects. Therefore, exploring new methods of tumor surgical navigation and tumor treatment is of great significance for oral cancer. Although, the emerging near-infrared II (NIR-II, 1,000–1,700 nm) region fluorescent imaging has revolutionized surgical navigation, a high tumor-targeting fluorescent probe remains lacking. Furthermore, while emerging photothermal therapy (PTT) can overcome chemoradiotherapy’s shortcomings and achieve precise treatment of tumors, its clinical application is still limited by the lack of high photothermal conversion efficiency, high photothermal stability, and highly penetrating materials. Herein, a NIR-II dye SQ890 is developed for tumor imaging and PTT of oral cancer. By assembling into nanoparticles (NPs) and being modified with epithelial growth factor receptor (EGFR)-targeting peptides GE11, SQ890 NPs-Pep can specifically accumulate in tumor sites via active targeting, and realize photoacoustic/NIR-II fluorescence dual-modality imaging-guided PTT of oral cancer.

Keywords: theranostics, photothermal therapy, near-infrared (NIR-II) imaging, oral cancer, epithelial growth factor receptor (EGFR)

References(38)

1

Miller, K. D.; Fidler-Benaoudia, M.; Keegan, T. H.; Hipp, H. S.; Jemal, A.; Siegel, R. L. Cancer statistics for adolescents and young adults, 2020. CA Cancer J. Clin. 2020, 70, 443–459.

2

Chi, A. C.; Day, T. A.; Neville, B. W. Oral cavity and oropharyngeal squamous cell carcinoma-an update. CA Cancer J. Clin. 2015, 65, 401–421.

3

Johnson, D. E.; Burtness, B.; Leemans, C. R.; Lui, V. W. Y.; Bauman, J. E.; Grandis, J. R. Head and neck squamous cell carcinoma. Nat. Rev. Dis. Primers. 2020, 6, 92.

4

Machiels, J. P.; René Leemans, C.; Golusinski, W.; Grau, C.; Licitra, L.; Gregoire, V. Squamous cell carcinoma of the oral cavity, larynx, oropharynx and hypopharynx: EHNS-ESMO-ESTRO clinical practice guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 2020, 31, 1462–1475.

5

Koyfman, S. A.; Ismaila, N.; Crook, D.; D'Cruz, A.; Rodriguez, C. P.; Sher, D. J.; Silbermins, D.; Sturgis, E. M.; Tsue, T. T.; Weiss, J. et al. Management of the neck in squamous cell carcinoma of the oral cavity and oropharynx: Asco clinical practice guideline. J. Clin. Oncol. 2019, 37, 1753–1774.

6

Pfister, D. G.; Spencer, S.; Adelstein, D.; Adkins, D.; Anzai, Y.; Brizel, D. M.; Bruce, J. Y.; Busse, P. M.; Caudell, J. J.; Cmelak, A. J. et al. Head and neck cancers, version 2.2020, NCCN clinical practice guidelines in oncology. J. Natl. Compr. Canc. Netw. 2020, 18, 873–898.

7

Nocon, C. C.; Ajmani, G. S.; Bhayani, M. K. Association of facility volume with positive margin rate in the surgical treatment of head and neck cancer. JAMA Otolaryngol. Head Neck Surg. 2018, 144, 1090–1097.

8

Lu, G. L.; Little, J. V.; Wang, X.; Zhang, H. Z.; Patel, M. R.; Griffith, C. C.; El-Deiry, M. W.; Chen, A. Y.; Fei, B. W. Detection of head and neck cancer in surgical specimens using quantitative hyperspectral imaging. Clin. Cancer Res. 2017, 23, 5426–5436.

9

Machtay, M.; Moughan, J.; Trotti, A.; Garden, A. S.; Weber, R. S.; Cooper, J. S.; Forastiere, A.; Ang, K. K. Factors associated with severe late toxicity after concurrent chemoradiation for locally advanced head and neck cancer: An RTOG analysis. J. Clin. Oncol. 2008, 26, 3582–3589.

10

Chera, B. S.; Amdur, R. J.; Green, R.; Shen, C.; Gupta, G.; Tan, X. M.; Knowles, M.; Fried, D.; Hayes, N.; Weiss, J. et al. Phase II trial of de-intensified chemoradiotherapy for human papillomavirus-associated oropharyngeal squamous cell carcinoma. J. Clin. Oncol. 2019, 37, 2661–2669.

11

Ma, D. J.; Price, K. A.; Moore, E. J.; Patel, S. H.; Hinni, M. L.; Garcia, J. J.; Graner, D. E.; Foster, N. R.; Ginos, B.; Neben−Wittich, M. et al. Phase II evaluation of aggressive dose de-escalation for adjuvant chemoradiotherapy in human papillomavirus-associated oropharynx squamous cell carcinoma. J. Clin. Oncol. 2019, 37, 1909–1918.

12

Chen, G.; Yang, Y. Y.; Xu, Q.; Ling, M. J.; Lin, H. M.; Ma, W.; Sun, R.; Xu, Y. C.; Liu, X. Q.; Li, N. et al. Self-amplification of tumor oxidative stress with degradable metallic complexes for synergistic cascade tumor therapy. Nano Lett. 2020, 20, 8141–8150.

13

Liu, X.; Yang, Y. Y.; Ling, M. J.; Sun, R.; Zhu, M. Y.; Chen, J. J.; Yu, M.; Peng, Z. W.; Yu, Z. Q.; Liu, X. Q. Near-infrared II light-triggered robust carbon radical generation for combined photothermal and thermodynamic therapy of hypoxic tumors. Adv. Funct. Mater. 2021, 31, 2101709.

14

Li, X. S.; Lovell, J. F.; Yoon, J.; Chen, X. Y. Clinical development and potential of photothermal and photodynamic therapies for cancer. Nat. Rev. Clin. Oncol. 2020, 17, 657–674.

15

Wen, H. F.; Zhang, Z. J.; Kang, M. M.; Li, H. X.; Xu, W. H.; Guo, H.; Li, Y. M.; Tan, Y. H.; Wen, Z. Y.; Wu, Q. et al. One-for-all phototheranostics: Single component AIE dots as multi-modality theranostic agent for fluorescence-photoacoustic imaging-guided synergistic cancer therapy. Biomaterials 2021, 274, 120892.

16

Wu, J. J.; Williams, G. R.; Zhu, Y.; Hu, T. T.; Wang, H.; Zhao, W.; Liang, R. Z.; Weng, X. S.; Wei, M. Ultrathin chalcogenide nanosheets for photoacoustic imaging-guided synergistic photothermal/gas therapy. Biomaterials 2021, 273, 120807.

17

Guo, H. Z.; Liu, L. S.; Hu, Q. Q.; Dou, H. J. Monodisperse ZIF-8@dextran nanoparticles co-loaded with hydrophilic and hydrophobic functional cargos for combined near-infrared fluorescence imaging and photothermal therapy. Acta Biomater. 2021, 137, 290–304.

18

Du, J. Y.; Yang, S. S.; Qiao, Y. C.; Lu, H. T.; Dong, H. F. Recent progress in near-infrared photoacoustic imaging. Biosens. Bioelectron. 2021, 191, 113478.

19

Xu, Y. J.; Wang, S. Q.; Chen, Z. J.; Hu, R.; Li, S. Q.; Zhao, Y. H.; Liu, L. W.; Qu, J. L. Highly stable organic photothermal agent based on near-infrared-II fluorophores for tumor treatment. J. Nanobiotechnol. 2021, 19, 37.

20

Noh, I.; Son, Y.; Jung, W.; Kim, M.; Kim, D.; Shin, H.; Kim, Y. C.; Jon, S. Targeting the tumor microenvironment with amphiphilic near-infrared cyanine nanoparticles for potentiated photothermal immunotherapy. Biomaterials 2021, 275, 120926.

21

Zhou, F. Y.; Yang, S. K.; Zhao, C.; Liu, W. W.; Yao, X. F.; Yu, H.; Sun, X. L.; Liu, Y. γ-Glutamyl transpeptidase-activatable near-infrared nanoassembly for tumor fluorescence imaging-guided photothermal therapy. Theranostics 2021, 11, 7045–7056.

22

Xu, Y. J.; Wang, S. Q.; Chen, Z. J.; Hu, R.; Zhao, Y. H.; Wang, K. X.; Qu, J. L.; Liu, L. W. Nitric oxide release activated near-Infrared photothermal agent for synergistic tumor treatment. Biomaterials 2021, 276, 121017.

23

Zhu, T.; Yang, G. Q.; Liu, X. L.; Xiang, P.; Yang, Z. H.; Zhang, S. J.; Chen, J.; Wang, H.; De Souza, S. C.; Zhang, Z. P. et al. Live cell mitochondrial 3-dimensional dynamic ultrastructures under oxidative phosphorylation revealed by a pyridine-BODIPY probe. Biosens. Bioelectron. 2021, 178, 113036.

24

Grimm, J. B.; Tkachuk, A. N.; Xie, L. Q.; Choi, H.; Mohar, B.; Falco, N.; Schaefer, K.; Patel, R.; Zheng, Q. S.; Liu, Z. et al. A general method to optimize and functionalize red-shifted rhodamine dyes. Nat. Methods 2020, 17, 815–821.

25

Sunbul, M.; Lackner, J.; Martin, A.; Englert, D.; Hacene, B.; Grün, F.; Nienhaus, K.; Nienhaus, G. U.; Jäschke, A. Super-resolution RNA imaging using a rhodamine-binding aptamer with fast exchange kinetics. Nat. Biotechnol. 2021, 39, 686–690.

26

Wu, J. C.; Zhou, Y. R.; Li, S.; Qu, D. H.; Zhu, W. H.; Tian, H. Real-time near-infrared bioimaging of a receptor-targeted cytotoxic dendritic theranostic agent. Biomaterials 2017, 120, 1–10.

27

Yang, Y. Y.; Liu, X.; Ma, W.; Xu, Q.; Chen, G.; Wang, Y. F.; Xiao, H. H.; Li, N.; Liang, X. J.; Yu, M. et al. Light-activatable liposomes for repetitive on-demand drug release and immunopotentiation in hypoxic tumor therapy. Biomaterials 2021, 265, 120456.

28

Xie, B. R.; Yu, Y.; Liu, X. H.; Zeng, J. Y.; Zou, M. Z.; Li, C. X.; Zeng, X.; Zhang, X. Z. A near infrared ratiometric platform based π-extended porphyrin metal-organic framework for O2 imaging and cancer therapy. Biomaterials 2021, 272, 120782.

29

Su, Y. B.; Yu, B.; Wang, S.; Cong, H. L.; Shen, Y. Q. NIR-II bioimaging of small organic molecule. Biomaterials 2021, 271, 120717.

30

He, K.; Chen, S. Y.; Xu, W. J.; Tai, X. J.; Chen, Y.; Sun, P. F.; Fan, Q. L.; Huang, W. High-stability NIR-II fluorescence polymer synthesized by atom transfer radical polymerization for application in high-resolution NIR-II imaging. Biomater. Sci. 2021, 9, 6434–6443.

31

Zhu, S. J.; Tian, R.; Antaris, A. L.; Chen, X. Y.; Dai, H. J. Near-infrared-II molecular dyes for cancer imaging and surgery. Adv. Mater. 2019, 31, 1900321.

32

Zhang, J. F.; Chen, J.; Ren, J. K.; Guo, W. S.; Li, X. L.; Chen, R.; Chelora, J.; Cui, X.; Wan, Y. P.; Liang, X. J. et al. Biocompatible semiconducting polymer nanoparticles as robust photoacoustic and photothermal agents revealing the effects of chemical structure on high photothermal conversion efficiency. Biomaterials 2018, 181, 92–102.

33

Liu, Y. J.; Bhattarai, P.; Dai, Z. F.; Chen, X. Y. Photothermal therapy and photoacoustic imaging via nanotheranostics in fighting cancer. Chem. Soc. Rev. 2019, 48, 2053–2108.

34

Adkins, D.; Mehan, P.; Ley, J.; Siegel, M. J.; Siegel, B. A.; Dehdashti, F.; Jiang, X. T.; Salama, N. N.; Trinkaus, K.; Oppelt, P. Pazopanib plus cetuximab in recurrent or metastatic head and neck squamous cell carcinoma: An open-label, phase 1b and expansion study. Lancet Oncol. 2018, 19, 1082–1093.

35

Tang, L. G.; Zhang, F. W.; Yu, F.; Sun, W. J.; Song, M. L.; Chen, X. Y.; Zhang, X. Z.; Sun, X. L. Croconaine nanoparticles with enhanced tumor accumulation for multimodality cancer theranostics. Biomaterials 2017, 129, 28–36.

36

Cai, X. Z.; Wang, K. N.; Ma, W.; Yang, Y. Y.; Chen, G.; Fu, H. J.; Cui, C. H.; Yu, Z. Q.; Wang, X. F. Multifunctional AIE iridium (III) photosensitizer nanoparticles for two-photon-activated imaging and mitochondria targeting photodynamic therapy. J. Nanobiotechnol. 2021, 19, 254.

37

Ma, W.; Sha, S. N.; Chen, P. L.; Yu, M.; Chen, J. J.; Huang, C. B.; Yu, B.; Liu, Y.; Liu, L. H.; Yu, Z. Q. A cell membrane-targeting self-delivery chimeric peptide for enhanced photodynamic therapy and in situ therapeutic feedback. Adv. Healthc. Mater. 2020, 9, e1901100.

38

Wang, D. S.; Qian, G. Q.; Zhang, H. Z.; Magliocca, K. R.; Nannapaneni, S.; Amin, A. R. M. R.; Rossi, M.; Patel, M.; El-Deiry, M.; Wadsworth, J. T. et al. HER3 targeting sensitizes HNSCC to cetuximab by reducing HER3 activity and HER2/HER3 dimerization: Evidence from cell line and patient-derived xenograft models. Clin. Cancer Res. 2017, 23, 677–686.

File
12274_2022_4239_MOESM1_ESM.pdf (3.7 MB)
Publication history
Copyright
Acknowledgements

Publication history

Received: 05 January 2022
Revised: 08 February 2022
Accepted: 13 February 2022
Published: 02 April 2022
Issue date: July 2022

Copyright

© Tsinghua University Press 2022

Acknowledgements

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 81773642 and 52073139), by the Postdoctoral Research Foundation of China (Nos. 2020TQ0253 and 2020M682927).

Return