Extracellular Vesicles in Head and Neck Cancer: A Potential New Trend in Diagnosis, Prognosis, and Treatment
Abstract
:1. Introduction
2. Extracellular Vesicles
2.1. EVs Facilitate Proliferation, Invasion, and Metastasis
2.2. EVs Regulate Tumor Immunology
2.3. EVs Promote Angiogenesis
2.4. EVs Remodel the Tumor Microenvironment
2.5. EVs Regulate Drug Resistance
2.6. EVs Regulate Radio-Sensitivity
3. EVs as a Potential Biomarker of HNCs
3.1. Biomarker Potential of EV Levels
3.2. Biomarker Potential of EV DNA Cargo
3.3. Biomarker Potential of EV RNA Cargo
3.4. Biomarker Potential of EV Protein Cargo
4. EVs and Treatment of HNCs
4.1. EV as a Direct Target: Inhibition of EV Synthesis and Secretion
4.2. Inhibition of EV Internalization
4.3. Modulating Contents in EVs
4.4. EVs and Immunotherapy
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
HNC | Head and neck cancer |
EVs | Extracellular Vesicles |
EPs | Extracellular Particles |
SCC | Squamous Cell Carcinoma |
EMT | Epithelial to Mesenchymal Transition |
MMP | Matrix Metalloproteinases |
NPC | Nasopharyngeal Cancer |
LMP1 | Latent Membrane Protein 1 |
EBV | Epstein–Barr virus |
HIF1α | Hypoxia-inducible factor 1 alpha |
EGFR | Epidermal Growth Factor Receptor |
HSP | Heat Shock Protein |
PTEN | Phosphatase and Tensin Homolog |
PD-L1 | Programmed Death-1 |
PD-1 | Programmed Death-Ligand 1 |
MDSC | Myeloid-Derived Stem Cells |
HPV | Human Papillomavirus |
DC | Dendritic Cell |
EPHB2 | Ephrin type B receptor 2 |
STAT | Signal Transducer and Activator of Transcription |
VEGF | Vascular Endothelial Growth Factor |
CAFs | Cancer-Associated Fibroblasts |
TAMs | Tumor-Associated Macrophages |
HPLFs | Human Periodontal Ligament Fibroblasts |
SOCS1 | Suppressor of Cytokine Signaling 1 |
PTEN | Phosphatase Tensin Homolog |
PDCD4 | Programmed Cell Death Factor 4 |
FOXO3a | Forkhead Box Protein O3 |
CSC | Cancer Stem Cell |
PI3K | Phosphoinositide 3-kinase |
mTOR | Mammalian Target of Rapamycin |
OSCC | Oral Squamous Cell Carcinoma |
CTC | Circulating Tumor Cell |
cfDNA | Cell-free DNA |
mtDNA | Mitochondrial DNA |
dsDNA | Double-stranded DNA |
ssDNA | Single-stranded DNA |
miRNA | MicroRNA |
lncRNA | Long Noncoding RNA |
circRNA | Circular RNA |
CYPA | Cyclophilin A |
VCA-IgA | Viral Capsid Antigen IgA |
ESCRT | Endosomal Sorting Complexes Required for Transport |
CRISPR | Clustered Regularly Interspaced Short Palindromic Repeats |
HER2 | Human Epidermal Growth Factor Receptor 2 |
siRNA | Small Interfering RNA |
OPMD | Oral Potentially Malignant Disorder |
CTLs | Cytotoxic T Lymphocytes |
References
- Chow, L.Q.M. Head and Neck Cancer. N. Engl. J. Med. 2020, 382, 60–72. [Google Scholar] [CrossRef]
- Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2020. CA Cancer J. Clin. 2020, 70, 7–30. [Google Scholar] [CrossRef]
- Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: Globocan estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2018, 68, 394–424. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leemans, C.R.; Snijders, P.J.F.; Brakenhoff, R.H. The molecular landscape of head and neck cancer. Nat. Rev. Cancer 2018, 18, 269–282. [Google Scholar] [CrossRef] [PubMed]
- Brumbaugh, J.; Ferris, R.L.; Hu, S. HPV and EBV in Head and Neck Cancer. In Head and Neck Cancer: Multimodality Management; Bernier, J., Ed.; Springer International Publishing: Cham, Switzerland, 2016; pp. 163–179. [Google Scholar]
- Neville, B.W.; Day, T.A. Oral Cancer and Precancerous Lesions. CA Cancer J. Clin. 2002, 52, 195–215. [Google Scholar] [CrossRef] [PubMed]
- Möller, A.; Lobb, R.J. The evolving translational potential of small extracellular vesicles in cancer. Nat. Rev. Cancer 2020. [Google Scholar] [CrossRef] [PubMed]
- Tkach, M.; Théry, C. Communication by Extracellular Vesicles: Where We Are and Where We Need to Go. Cell 2016, 164, 1226–1232. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Théry, C.; Witwer, K.W.; Aikawa, E.; Alcaraz, M.J.; Anderson, J.D.; Andriantsitohaina, R.; Antoniou, A.; Arab, T.; Archer, F.; Atkin-Smith, G.K.; et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): A position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J. Extracell. Vesicles 2018, 7, 1535750. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- You, Y.; Shan, Y.; Chen, J.; Yue, H.; You, B.; Shi, S.; Li, X.; Cao, X. Matrix metalloproteinase 13-containing exosomes promote nasopharyngeal carcinoma metastasis. Cancer Sci. 2015, 106, 1669–1677. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shan, Y.; You, B.; Shi, S.; Shi, W.; Zhang, Z.; Zhang, Q.; Gu, M.; Chen, J.; Bao, L.; Liu, D.; et al. Hypoxia-Induced Matrix Metalloproteinase-13 Expression in Exosomes from Nasopharyngeal Carcinoma Enhances Metastases. Cell Death Dis. 2018, 9, 382. [Google Scholar] [CrossRef] [PubMed]
- Zuo, L.; Xie, Y.; Tang, J.; Xin, S.; Liu, L.; Zhang, S.; Yan, Q.; Zhu, F.; Lu, J. Targeting Exosomal EBV-LMP1 Transfer and miR-203 Expression via the NF-κB Pathway: The Therapeutic Role of Aspirin in NPC. Mol. Ther. Nucleic Acids 2019, 17, 175–184. [Google Scholar] [CrossRef] [Green Version]
- Liao, C.; Zhou, Q.; Zhang, Z.; Wu, X.; Zhou, Z.; Li, B.; Peng, J.; Shen, L.; Li, D.; Luo, X.; et al. Epstein-Barr virus-encoded latent membrane protein 1 promotes extracellular vesicle secretion through syndecan-2 and synaptotagmin-like-4 in nasopharyngeal carcinoma cells. Cancer Sci. 2020, 111, 857–868. [Google Scholar] [CrossRef]
- Zhang, Z.; Yu, X.; Zhou, Z.; Li, B.; Peng, J.; Wu, X.; Luo, X.; Yang, L. LMP1-positive extracellular vesicles promote radioresistance in nasopharyngeal carcinoma cells through P38 MAPK signaling. Cancer Med.-US 2019, 8, 6082–6094. [Google Scholar] [CrossRef] [Green Version]
- He, L.; Ping, F.; Fan, Z.; Zhang, C.; Deng, M.; Cheng, B.; Xia, J. Salivary exosomal miR-24-3p serves as a potential detective biomarker for oral squamous cell carcinoma screening. Biomed. Pharm. 2020, 121, 109553. [Google Scholar] [CrossRef]
- Ono, K.; Eguchi, T.; Sogawa, C.; Calderwood, S.K.; Futagawa, J.; Kasai, T.; Seno, M.; Okamoto, K.; Sasaki, A.; Kozaki, K. HSP-enriched properties of extracellular vesicles involve survival of metastatic oral cancer cells. J. Cell Biochem. 2018, 119, 7350–7362. [Google Scholar] [CrossRef] [Green Version]
- Fujiwara, T.; Eguchi, T.; Sogawa, C.; Ono, K.; Murakami, J.; Ibaragi, S.; Asaumi, J.; Calderwood, S.K.; Okamoto, K.; Kozaki, K. Carcinogenic epithelial-mesenchymal transition initiated by oral cancer exosomes is inhibited by anti-EGFR antibody cetuximab. Oral Oncol. 2018, 86, 251–257. [Google Scholar] [CrossRef]
- Meehan, K.; Leslie, C.; Lucas, M.; Jacques, A.; Mirzai, B.; Lim, J.; Bulsara, M.; Khan, Y.; Wong, N.C.; Solomon, B.; et al. Characterization of the immune profile of oral tongue squamous cell carcinomas with advancing disease. Cancer Med.-US 2020, 9, 4791–4807. [Google Scholar] [CrossRef] [PubMed]
- Ludwig, S.; Floros, T.; Theodoraki, M.; Hong, C.; Jackson, E.K.; Lang, S.; Whiteside, T.L. Suppression of Lymphocyte Functions by Plasma Exosomes Correlates with Disease Activity in Patients with Head and Neck Cancer. Clin. Cancer Res. 2017, 23, 4843–4854. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.; Qin, X.; Zhu, X.; Chen, W.; Zhang, J.; Chen, W. Oral cancer-derived exosomal NAP1 enhances cytotoxicity of natural killer cells via the IRF-3 pathway. Oral Oncol. 2018, 76, 34–41. [Google Scholar] [CrossRef]
- Maybruck, B.T.; Pfannenstiel, L.W.; Diaz-Montero, M.; Gastman, B.R. Tumor-derived exosomes induce CD8+ T cell suppressors. J. Immunother. Cancer 2017, 5. [Google Scholar] [CrossRef]
- Whiteside, T.L. Exosomes and tumor-mediated immune suppression. J. Clin. Investig. 2016, 126, 1216–1223. [Google Scholar] [CrossRef] [Green Version]
- Li, L.; Cao, B.; Liang, X.; Lu, S.; Luo, H.; Wang, Z.; Wang, S.; Jiang, J.; Lang, J.; Zhu, G. Microenvironmental oxygen pressure orchestrates an anti- and pro-tumoral γδ T cell equilibrium via tumor-derived exosomes. Oncogene 2019, 38, 2830–2843. [Google Scholar] [CrossRef]
- Welters, M.J.P.; Ma, W.; Santegoets, S.J.A.M.; Goedemans, R.; Ehsan, I.; Jordanova, E.S.; van Ham, V.J.; van Unen, V.; Koning, F.; van Egmond, S.I.; et al. Intratumoral HPV16-Specific T Cells Constitute a Type I–Oriented Tumor Microenvironment to Improve Survival in HPV16-Driven Oropharyngeal Cancer. Clin. Cancer Res. 2018, 24, 634–647. [Google Scholar] [CrossRef] [Green Version]
- Ludwig, S.; Sharma, P.; Theodoraki, M.; Pietrowska, M.; Yerneni, S.S.; Lang, S.; Ferrone, S.; Whiteside, T.L. Molecular and Functional Profiles of Exosomes From HPV(+) and HPV(−) Head and Neck Cancer Cell Lines. Front. Oncol. 2018, 8. [Google Scholar] [CrossRef]
- Ferris, R.L.; Blumenschein, G.; Fayette, J.; Guigay, J.; Colevas, A.D.; Licitra, L.; Harrington, K.J.; Kasper, S.; Vokes, E.E.; Even, C.; et al. Nivolumab vs. investigator’s choice in recurrent or metastatic squamous cell carcinoma of the head and neck: 2-year long-term survival update of CheckMate 141 with analyses by tumor PD-L1 expression. Oral Oncol. 2018, 81, 45–51. [Google Scholar] [CrossRef]
- Theodoraki, M.; Yerneni, S.S.; Hoffmann, T.K.; Gooding, W.E.; Whiteside, T.L. Clinical Significance of PD-L1+ Exosomes in Plasma of Head and Neck Cancer Patients. Clin. Cancer Res. 2018, 24, 896–905. [Google Scholar] [CrossRef] [Green Version]
- Skog, J.; Würdinger, T.; van Rijn, S.; Meijer, D.H.; Gainche, L.; Curry, W.T.; Carter, B.S.; Krichevsky, A.M.; Breakefield, X.O. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 2008, 10, 1470–1476. [Google Scholar] [CrossRef] [PubMed]
- Al-Nedawi, K.; Meehan, B.; Micallef, J.; Lhotak, V.; May, L.; Guha, A.; Rak, J. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol. 2008, 10, 619–624. [Google Scholar] [CrossRef]
- You, B.; Cao, X.; Shao, X.; Ni, H.; Shi, S.; Shan, Y.; Gu, Z.; You, Y. Clinical and biological significance of HAX-1 overexpression in nasopharyngeal carcinoma. Oncotarget 2016, 7, 12505–12524. [Google Scholar] [CrossRef] [Green Version]
- Dickman, C.T.D.; Lawson, J.; Jabalee, J.; MacLellan, S.A.; LePard, N.E.; Bennewith, K.L.; Garnis, C. Selective extracellular vesicle exclusion of miR-142-3p by oral cancer cells promotes both internal and extracellular malignant phenotypes. Oncotarget 2017, 8, 15252–15266. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bao, L.; You, B.; Shi, S.; Shan, Y.; Zhang, Q.; Yue, H.; Zhang, J.; Zhang, W.; Shi, Y.; Liu, Y.; et al. Metastasis-associated miR-23a from nasopharyngeal carcinoma-derived exosomes mediates angiogenesis by repressing a novel target gene TSGA10. Oncogene 2018, 37, 2873–2889. [Google Scholar] [CrossRef]
- Duan, B.; Shi, S.; Yue, H.; You, B.; Shan, Y.; Zhu, Z.; Bao, L.; You, Y. Exosomal miR-17-5p promotes angiogenesis in nasopharyngeal carcinoma via targeting BAMBI. J. Cancer 2019, 10, 6681–6692. [Google Scholar] [CrossRef] [PubMed]
- Lu, J.; Liu, Q.; Wang, F.; Tan, J.; Deng, Y.; Peng, X.; Liu, X.; Zhang, B.; Xu, X.; Li, X. Exosomal miR-9 inhibits angiogenesis by targeting MDK and regulating PDK/AKT pathway in nasopharyngeal carcinoma. J. Exp. Clin. Cancer Res. 2018, 37, 147. [Google Scholar] [CrossRef] [Green Version]
- Sato, S.; Vasaikar, S.; Eskaros, A.; Kim, Y.; Lewis, J.S.; Zhang, B.; Zijlstra, A.; Weaver, A.M. EPHB2 carried on small extracellular vesicles induces tumor angiogenesis via activation of ephrin reverse signaling. JCI Insight 2019, 4, e132447. [Google Scholar] [CrossRef] [PubMed]
- Gu, M.; Li, L.; Zhang, Z.; Chen, J.; Zhang, W.; Zhang, J.; Han, L.; Tang, M.; You, B.; Zhang, Q.; et al. PFKFB3 promotes proliferation, migration and angiogenesis in nasopharyngeal carcinoma. J. Cancer 2017, 8, 3887–3896. [Google Scholar] [CrossRef] [Green Version]
- Ludwig, N.; Yerneni, S.S.; Azambuja, J.H.; Gillespie, D.G.; Menshikova, E.V.; Jackson, E.K.; Whiteside, T.L. Tumor-derived exosomes promote angiogenesis via adenosine A2B receptor signaling. Angiogenesis 2020, 23, 599–610. [Google Scholar] [CrossRef]
- Kolenda, T.; Przybyła, W.; Kapałczyńska, M.; Teresiak, A.; Zajączkowska, M.; Bliźniak, R.; Lamperska, K.M. Tumor microenvironment–Unknown niche with powerful therapeutic potential. Rep. Pract. Oncol. Radiother. 2018, 23, 143–153. [Google Scholar] [CrossRef]
- Marsh, D.; Suchak, K.; Moutasim, K.A.; Vallath, S.; Hopper, C.; Jerjes, W.; Upile, T.; Kalavrezos, N.; Violette, S.M.; Weinreb, P.H.; et al. Stromal features are predictive of disease mortality in oral cancer patients. J. Pathol. 2011, 223, 470–481. [Google Scholar] [CrossRef]
- Sahai, E.; Astsaturov, I.; Cukierman, E.; DeNardo, D.G.; Egeblad, M.; Evans, R.M.; Fearon, D.; Greten, F.R.; Hingorani, S.R.; Hunter, T.; et al. A framework for advancing our understanding of cancer-associated fibroblasts. Nat. Rev. Cancer 2020, 20, 174–186. [Google Scholar] [CrossRef] [Green Version]
- Hou, J.; Wang, F.; Liu, X.; Song, M.; Yin, X. Tumor-derived exosomes enhance invasion and metastasis of salivary adenoid cystic carcinoma cells. J. Oral Pathol. Med. 2018, 47, 144–151. [Google Scholar] [CrossRef]
- Xu, Z.; Zheng, X.; Zheng, J. Tumor-derived exosomes educate fibroblasts to promote salivary adenoid cystic carcinoma metastasis via NGF-NTRK1 pathway. Oncol. Lett. 2019, 18, 4082–4091. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, X.; Zhou, Z.; Xu, S.; Liao, C.; Chen, X.; Li, B.; Peng, J.; Li, D.; Yang, L. Extracellular vesicle packaged LMP1-activated fibroblasts promote tumor progression via autophagy and stroma-tumor metabolism coupling. Cancer Lett. 2020, 478, 93–106. [Google Scholar] [CrossRef]
- Evrard, D.; Szturz, P.; Tijeras-Raballand, A.; Astorgues-Xerri, L.; Abitbol, C.; Paradis, V.; Raymond, E.; Albert, S.; Barry, B.; Faivre, S. Macrophages in the microenvironment of head and neck cancer: Potential targets for cancer therapy. Oral Oncol. 2019, 88, 29–38. [Google Scholar] [CrossRef]
- Cai, J.; Qiao, B.; Gao, N.; Lin, N.; He, W. Oral squamous cell carcinoma-derived exosomes promote M2 subtype macrophage polarization mediated by exosome-enclosed miR-29a-3p. Am. J. Physiol-Cell Phys. 2019, 316, C731–C740. [Google Scholar] [CrossRef]
- Hsieh, C.; Tai, S.; Yang, M. Snail-overexpressing Cancer Cells Promote M2-Like Polarization of Tumor-Associated Macrophages by Delivering MiR-21-Abundant Exosomes. Neoplasia 2018, 20, 775–788. [Google Scholar] [CrossRef]
- Tong, F.; Mao, X.; Zhang, S.; Xie, H.; Yan, B.; Wang, B.; Sun, J.; Wei, L. HPV + HNSCC-derived exosomal miR-9 induces macrophage M1 polarization and increases tumor radiosensitivity. Cancer Lett. 2020, 478, 34–44. [Google Scholar] [CrossRef]
- Xiao, M.; Zhang, J.; Chen, W.; Chen, W. M1-like tumor-associated macrophages activated by exosome-transferred THBS1 promote malignant migration in oral squamous cell carcinoma. J. Exp. Clin. Cancer Res. 2018, 37, 143–157. [Google Scholar] [CrossRef] [Green Version]
- Bellmunt, À.M.; López-Puerto, L.; Lorente, J.; Closa, D. Involvement of extracellular vesicles in the macrophage-tumor cell communication in head and neck squamous cell carcinoma. PLoS ONE 2019, 14, e224710. [Google Scholar] [CrossRef] [Green Version]
- Khoo, X.; Paterson, I.C.; Goh, B.; Lee, W. Cisplatin-Resistance in Oral Squamous Cell Carcinoma: Regulation by Tumor Cell-Derived Extracellular Vesicles. Cancers 2019, 11, 1166. [Google Scholar] [CrossRef] [Green Version]
- Liu, T.; Chen, G.; Sun, D.; Lei, M.; Li, Y.; Zhou, C.; Li, X.; Xue, W.; Wang, H.; Liu, C.; et al. Exosomes containing miR-21 transfer the characteristic of cisplatin resistance by targeting PTEN and PDCD4 in oral squamous cell carcinoma. Acta Biochim. Biophys. Sin. 2017, 49, 808–816. [Google Scholar] [CrossRef] [Green Version]
- Kulkarni, B.; Gondaliya, P.; Kirave, P.; Rawal, R.; Jain, A.; Garg, R.; Kalia, K. Exosome-mediated delivery of miR-30a sensitize cisplatin-resistant variant of oral squamous carcinoma cells via modulating Beclin1 and Bcl2. Oncotarget 2020, 11, 1832–1845. [Google Scholar] [CrossRef] [PubMed]
- Kirave, P.; Gondaliya, P.; Kulkarni, B.; Rawal, R.; Garg, R.; Jain, A.; Kalia, K. Exosome mediated miR-155 delivery confers cisplatin chemoresistance in oral cancer cells via epithelial-mesenchymal transition. Oncotarget 2020, 11, 1157–1171. [Google Scholar] [CrossRef] [Green Version]
- Chen, J.; Wu, A.T.H.; Bamodu, O.A.; Yadav, V.K.; Chao, T.; Tzeng, Y.; Mukhopadhyay, D.; Hsiao, M.; Lee, J. Ovatodiolide Suppresses Oral Cancer Malignancy by Down-Regulating Exosomal Mir-21/STAT3/β-Catenin Cargo and Preventing Oncogenic Transformation of Normal Gingival Fibroblasts. Cancers 2020, 12, 56. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Byeon, H.K.; Ku, M.; Yang, J. Beyond EGFR inhibition: Multilateral combat strategies to stop the progression of head and neck cancer. Exp. Mol. Med. 2019, 51, 1–14. [Google Scholar] [CrossRef] [Green Version]
- Jelonek, K.; Wojakowska, A.; Marczak, L.; Muer, A.; Tinhofer-Keilholz, I.; Lysek-Gladysinska, M.; Widlak, P.; Pietrowska, M. Ionizing radiation affects protein composition of exosomes secreted in vitro from head and neck squamous cell carcinoma. Acta Biochim. Pol. 2015, 62, 265–272. [Google Scholar] [CrossRef] [Green Version]
- Mutschelknaus, L.; Azimzadeh, O.; Heider, T.; Winkler, K.; Vetter, M.; Kell, R.; Tapio, S.; Merl-Pham, J.; Huber, S.M.; Edalat, L.; et al. Radiation alters the cargo of exosomes released from squamous head and neck cancer cells to promote migration of recipient cells. Sci. Rep. 2017, 7, 12423–12435. [Google Scholar] [CrossRef]
- Abramowicz, A.; Wojakowska, A.; Marczak, L.; Lysek-Gladysinska, M.; Smolarz, M.; Story, M.D.; Polanska, J.; Widlak, P.; Pietrowska, M. Ionizing radiation affects the composition of the proteome of extracellular vesicles released by head-and-neck cancer cells in vitro. J. Radiat. Res. 2019, 60, 289–297. [Google Scholar] [CrossRef]
- Mutschelknaus, L.; Peters, C.; Winkler, K.; Yentrapalli, R.; Heider, T.; Atkinson, M.J.; Moertl, S. Exosomes Derived from Squamous Head and Neck Cancer Promote Cell Survival after Ionizing Radiation. PLoS ONE 2016, 11, e152213. [Google Scholar] [CrossRef]
- Qiao, L.; Hu, S.; Huang, K.; Su, T.; Li, Z.; Vandergriff, A.; Cores, J.; Dinh, P.; Allen, T.; Shen, D.; et al. Tumor cell-derived exosomes home to their cells of origin and can be used as Trojan horses to deliver cancer drugs. Theranostics 2020, 10, 3474–3487. [Google Scholar] [CrossRef]
- Kalluri, R. The biology and function of exosomes in cancer. J. Clin. Investig. 2016, 126, 1208–1215. [Google Scholar] [CrossRef]
- Lenzini, S.; Bargi, R.; Chung, G.; Shin, J. Matrix mechanics and water permeation regulate extracellular vesicle transport. Nat. Nanotechnol. 2020, 15, 217–223. [Google Scholar] [CrossRef]
- Nonaka, T.; Wong, D.T.W. Liquid Biopsy in Head and Neck Cancer: Promises and Challenges. J. Dent. Res. 2018, 97, 701–708. [Google Scholar] [CrossRef]
- Bebelman, M.P.; Smit, M.J.; Pegtel, D.M.; Baglio, S.R. Biogenesis and function of extracellular vesicles in cancer. Pharm. Ther. 2018, 188, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Choi, D.; Montermini, L.; Jeong, H.; Sharma, S.; Meehan, B.; Rak, J. Mapping Subpopulations of Cancer Cell-Derived Extracellular Vesicles and Particles by Nano-Flow Cytometry. ACS Nano 2019, 13, 10499–10511. [Google Scholar] [CrossRef]
- Kondratov, K.; Nikitin, Y.; Fedorov, A.; Kostareva, A.; Mikhailovskii, V.; Isakov, D.; Ivanov, A.; Golovkin, A. Heterogeneity of the nucleic acid repertoire of plasma extracellular vesicles demonstrated using high-sensitivity fluorescence-activated sorting. J. Extracell. Vesicles 2020, 9, 1743139. [Google Scholar] [CrossRef] [Green Version]
- Willms, E.; Cabañas, C.; Mäger, I.; Wood, M.J.A.; Vader, P. Extracellular Vesicle Heterogeneity: Subpopulations, Isolation Techniques, and Diverse Functions in Cancer Progression. Front. Immunol. 2018, 9, 738. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhong, W.Q.; Ren, J.G.; Xiong, X.P.; Man, Q.W.; Zhang, W.; Gao, L.; Li, C.; Liu, B.; Sun, Z.J.; Jia, J.; et al. Increased salivary microvesicles are associated with the prognosis of patients with oral squamous cell carcinoma. J. Cell Mol. Med. 2019, 23, 4054–4062. [Google Scholar] [CrossRef]
- Sharma, S.; Gillespie, B.M.; Palanisamy, V.; Gimzewski, J.K. Quantitative Nanostructural and Single-Molecule Force Spectroscopy Biomolecular Analysis of Human-Saliva-Derived Exosomes. Langmuir 2011, 27, 14394–14400. [Google Scholar] [CrossRef] [Green Version]
- Zlotogorski-Hurvitz, A.; Dayan, D.; Chaushu, G.; Salo, T.; Vered, M. Morphological and molecular features of oral fluid-derived exosomes: Oral cancer patients versus healthy individuals. J. Cancer Res. Clin. 2016, 142, 101–110. [Google Scholar] [CrossRef]
- Zlotogorski-Hurvitz, A.; Dekel, B.Z.; Malonek, D.; Yahalom, R.; Vered, M. FTIR-based spectrum of salivary exosomes coupled with computational-aided discriminating analysis in the diagnosis of oral cancer. J. Cancer Res. Clin. 2019, 145, 685–694. [Google Scholar] [CrossRef]
- Rodríguez Zorrilla, S.; Pérez-Sayans, M.; Fais, S.; Logozzi, M.; Gallas Torreira, M.; García García, A. A Pilot Clinical Study on the Prognostic Relevance of Plasmatic Exosomes Levels in Oral Squamous Cell Carcinoma Patients. Cancers 2019, 11, 429. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Theodoraki, M.; Yerneni, S.; Gooding, W.E.; Ohr, J.; Clump, D.A.; Bauman, J.E.; Ferris, R.L.; Whiteside, T.L. Circulating exosomes measure responses to therapy in head and neck cancer patients treated with cetuximab, ipilimumab, and IMRT. Oncoimmunology 2019, 8, e1593805. [Google Scholar] [CrossRef]
- Jeppesen, D.K.; Fenix, A.M.; Franklin, J.L.; Higginbotham, J.N.; Zhang, Q.; Zimmerman, L.J.; Liebler, D.C.; Ping, J.; Liu, Q.; Evans, R.; et al. Reassessment of Exosome Composition. Cell 2019, 177, 428–445. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Malkin, E.Z.; Bratman, S.V. Bioactive DNA from extracellular vesicles and particles. Cell Death Dis. 2020, 11, 584–596. [Google Scholar] [CrossRef] [PubMed]
- Balaj, L.; Lessard, R.; Dai, L.; Cho, Y.; Pomeroy, S.L.; Breakefield, X.O.; Skog, J. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat. Commun. 2011, 2, 180. [Google Scholar] [CrossRef]
- Guescini, M.; Genedani, S.; Stocchi, V.; Agnati, L.F. Astrocytes and Glioblastoma cells release exosomes carrying mtDNA. J. Neural. Transm. 2010, 117, 1–4. [Google Scholar] [CrossRef]
- Sansone, P.; Savini, C.; Kurelac, I.; Chang, Q.; Amato, L.B.; Strillacci, A.; Stepanova, A.; Iommarini, L.; Mastroleo, C.; Daly, L.; et al. Packaging and transfer of mitochondrial DNA via exosomes regulate escape from dormancy in hormonal therapy-resistant breast cancer. Proc. Natl. Acad. Sci. USA 2017, 114, E9066–E9075. [Google Scholar] [CrossRef] [Green Version]
- Thakur, B.K.; Zhang, H.; Becker, A.; Matei, I.; Huang, Y.; Costa-Silva, B.; Zheng, Y.; Hoshino, A.; Brazier, H.; Xiang, J.; et al. Double-stranded DNA in exosomes: A novel biomarker in cancer detection. Cell Res. 2014, 24, 766–769. [Google Scholar] [CrossRef] [Green Version]
- Kahlert, C.; Melo, S.A.; Protopopov, A.; Tang, J.; Seth, S.; Koch, M.; Zhang, J.; Weitz, J.; Chin, L.; Futreal, A.; et al. Identification of Double-stranded Genomic DNA Spanning All Chromosomes with Mutated KRAS and p53 DNA in the Serum Exosomes of Patients with Pancreatic Cancer. J. Biol. Chem. 2014, 289, 3869–3875. [Google Scholar] [CrossRef] [Green Version]
- Cai, J.; Han, Y.; Ren, H.; Chen, C.; He, D.; Zhou, L.; Eisner, G.M.; Asico, L.D.; Jose, P.A.; Zeng, C. Extracellular vesicle-mediated transfer of donor genomic DNA to recipient cells is a novel mechanism for genetic influence between cells. J. Mol. Cell Biol. 2013, 5, 227–238. [Google Scholar] [CrossRef] [Green Version]
- Lee, T.H.; Chennakrishnaiah, S.; Audemard, E.; Montermini, L.; Meehan, B.; Rak, J. Oncogenic ras-driven cancer cell vesiculation leads to emission of double-stranded DNA capable of interacting with target cells. Biochem. Biophys. Res. Commun. 2014, 451, 295–301. [Google Scholar] [CrossRef] [Green Version]
- San Lucas, F.A.; Allenson, K.; Bernard, V.; Castillo, J.; Kim, D.U.; Ellis, K.; Ehli, E.A.; Davies, G.E.; Petersen, J.L.; Li, D.; et al. Minimally invasive genomic and transcriptomic profiling of visceral cancers by next-generation sequencing of circulating exosomes. Ann. Oncol. 2016, 27, 635–641. [Google Scholar] [CrossRef] [Green Version]
- Qu, X.; Li, Q.; Yang, J.; Zhao, H.; Wang, F.; Zhang, F.; Zhang, S.; Zhang, H.; Wang, R.; Wang, Q.; et al. Double-Stranded DNA in Exosomes of Malignant Pleural Effusions as a Novel DNA Source for EGFR Mutation Detection in Lung Adenocarcinoma. Front. Oncol. 2019, 9, 931–938. [Google Scholar] [CrossRef]
- Castellanos-Rizaldos, E.; Zhang, X.; Tadigotla, V.R.; Grimm, D.G.; Karlovich, C.; Raez, L.E.; Skog, J.K. Exosome-based detection of activating and resistanceEGFR mutations from plasma of non-small cell lung cancer patients. Oncotarget 2019, 10, 2911–2920. [Google Scholar] [CrossRef] [Green Version]
- Krug, A.K.; Enderle, D.; Karlovich, C.; Priewasser, T.; Bentink, S.; Spiel, A.; Brinkmann, K.; Emenegger, J.; Grimm, D.G.; Castellanos-Rizaldos, E.; et al. Improved EGFR mutation detection using combined exosomal RNA and circulating tumor DNA in NSCLC patient plasma. Ann. Oncol. 2018, 29, 700–706. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Castellanos-Rizaldos, E.; Grimm, D.G.; Tadigotla, V.; Hurley, J.; Healy, J.; Neal, P.L.; Sher, M.; Venkatesan, R.; Karlovich, C.; Raponi, M.; et al. Exosome-Based Detection ofEGFR T790M in Plasma from Non–Small Cell Lung Cancer Patients. Clin. Cancer Res. 2018, 24, 2944–2950. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stransky, N.; Egloff, A.M.; Tward, A.D.; Kostic, A.D.; Cibulskis, K.; Sivachenko, A.; Kryukov, G.V.; Lawrence, M.S.; Sougnez, C.; McKenna, A.; et al. The Mutational Landscape of Head and Neck Squamous Cell Carcinoma. Science 2011, 333, 1157–1160. [Google Scholar] [CrossRef] [Green Version]
- Guenat, D.; Hermetet, F.; Prétet, J.; Mougin, C. Exosomes and Other Extracellular Vesicles in HPV Transmission and Carcinogenesis. Viruses 2017, 9, 211. [Google Scholar] [CrossRef] [Green Version]
- Nguyen, B.; Meehan, K.; Pereira, M.R.; Mirzai, B.; Lim, S.H.; Leslie, C.; Clark, M.; Sader, C.; Friedland, P.; Lindsay, A.; et al. A comparative study of extracellular vesicle-associated and cell-free DNA and RNA for HPV detection in oropharyngeal squamous cell carcinoma. Sci. Rep. 2020, 10, 6083–6092. [Google Scholar] [CrossRef] [Green Version]
- Wang, Z.; Li, F.; Rufo, J.; Chen, C.; Yang, S.; Li, L.; Zhang, J.; Cheng, J.; Kim, Y.; Wu, M.; et al. Acoustofluidic Salivary Exosome Isolation. J. Mol. Diagn. 2020, 22, 50–59. [Google Scholar] [CrossRef] [Green Version]
- Vagner, T.; Spinelli, C.; Minciacchi, V.R.; Balaj, L.; Zandian, M.; Conley, A.; Zijlstra, A.; Freeman, M.R.; Demichelis, F.; De, S.; et al. Large extracellular vesicles carry most of the tumour DNA circulating in prostate cancer patient plasma. J. Extracell. Vesicles 2018, 7, 1505403. [Google Scholar] [CrossRef] [Green Version]
- Lázaro-Ibáñez, E.; Sanz-Garcia, A.; Visakorpi, T.; Escobedo-Lucea, C.; Siljander, P.; Ayuso-Sacido, Á.; Yliperttula, M. Different gDNA content in the subpopulations of prostate cancer extracellular vesicles: Apoptotic bodies, microvesicles, and exosomes. Prostate 2014, 74, 1379–1390. [Google Scholar] [CrossRef]
- Min, L.; Zhu, S.; Chen, L.; Liu, X.; Wei, R.; Zhao, L.; Yang, Y.; Zhang, Z.; Kong, G.; Li, P.; et al. Evaluation of circulating small extracellular vesicles derived miRNAs as biomarkers of early colon cancer: A comparison with plasma total miRNAs. J. Extracell. Vesicles 2019, 8, 1643670. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rabinowits, G.; Bowden, M.; Flores, L.M.; Verselis, S.; Vergara, V.; Jo, V.Y.; Chau, N.; Lorch, J.; Hammerman, P.S.; Thomas, T.; et al. Comparative Analysis of MicroRNA Expression among Benign and Malignant Tongue Tissue and Plasma of Patients with Tongue Cancer. Front. Oncol. 2017, 7, 191. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Momen-Heravi, F.; Bala, S. Extracellular vesicles in oral squamous carcinoma carry oncogenic miRNA profile and reprogram monocytes via NF-κB pathway. Oncotarget 2018, 9, 34838–34854. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, J.; Zhou, Y.; Lu, J.; Sun, Y.; Xiao, H.; Liu, M.; Tian, L. Combined detection of serum exosomal miR-21 and HOTAIR as diagnostic and prognostic biomarkers for laryngeal squamous cell carcinoma. Med. Oncol. 2014, 31, 148. [Google Scholar] [CrossRef]
- Zhao, Q.; Zheng, X.; Guo, H.; Xue, X.; Zhang, Y.; Niu, M.; Cui, J.; Liu, H.; Luo, H.; Yang, D.; et al. Serum Exosomal miR-941 as a promising Oncogenic Biomarker for Laryngeal Squamous Cell Carcinoma. J. Cancer 2020, 11, 5329–5344. [Google Scholar] [CrossRef]
- Peng, Q.; Zhang, J.; Zhou, G. Differentially circulating exosomal microRNAs expression profiling in oral lichen planus. Am. J. Transl. Res. 2018, 10, 2848. [Google Scholar]
- Dai, D.; Tan, Y.; Guo, L.; Tang, A.; Zhao, Y. Identification of exosomal miRNA biomarkers for diagnosis of papillary thyroid cancer by small RNA sequencing. Eur. J. Endocrinol. 2020, 182, 111–121. [Google Scholar] [CrossRef]
- Zou, X.; Zhu, D.; Zhang, H.; Zhang, S.; Zhou, X.; He, X.; Zhu, J.; Zhu, W. MicroRNA expression profiling analysis in serum for nasopharyngeal carcinoma diagnosis. Gene 2020, 727, 144243. [Google Scholar] [CrossRef]
- Tian, L.; Cao, J.; Jiao, H.; Zhang, J.; Ren, X.; Liu, X.; Liu, M.; Sun, Y. CircRASSF2 promotes laryngeal squamous cell carcinoma progression by regulating the miR-302b-3p/IGF-1R axis. Clin. Sci. 2019, 133, 1053–1066. [Google Scholar] [CrossRef] [PubMed]
- Luo, Y.; Liu, F.; Guo, J.; Gui, R. Upregulation of circ_0000199 in circulating exosomes is associated with survival outcome in OSCC. Sci. Rep. 2020, 10, 13739. [Google Scholar] [CrossRef] [PubMed]
- Langevin, S.; Kuhnell, D.; Parry, T.; Biesiada, J.; Huang, S.; Wise-Draper, T.; Casper, K.; Zhang, X.; Medvedovic, M.; Kasper, S. Comprehensive microRNA-sequencing of exosomes derived from head and neck carcinoma cellsin vitro reveals common secretion profiles and potential utility as salivary biomarkers. Oncotarget 2017, 8, 82459–82474. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gai, C.; Camussi, F.; Broccoletti, R.; Gambino, A.; Cabras, M.; Molinaro, L.; Carossa, S.; Camussi, G.; Arduino, P.G. Salivary extracellular vesicle-associated miRNAs as potential biomarkers in oral squamous cell carcinoma. BMC Cancer 2018, 18, 439. [Google Scholar] [CrossRef] [Green Version]
- Ramayanti, O.; Verkuijlen, S.A.W.M.; Novianti, P.; Scheepbouwer, C.; Misovic, B.; Koppers Lalic, D.; Weering, J.; Beckers, L.; Adham, M.; Martorelli, D.; et al. Vesicle-bound EBV-BART13-3p miRNA in circulation distinguishes nasopharyngeal from other head and neck cancer and asymptomatic EBV-infections. Int. J. Cancer 2019, 144, 2555–2566. [Google Scholar] [CrossRef]
- Peacock, B.; Rigby, A.; Bradford, J.; Pink, R.; Hunter, K.; Lambert, D.; Hunt, S. Extracellular vesicle microRNA cargo is correlated with HPV status in oropharyngeal carcinoma. J. Oral Pathol. Med. 2018, 47, 954–963. [Google Scholar] [CrossRef]
- Todoeoki, K.; Ogasawara, S.; Akiba, J.; Nakayama, M.; Naito, Y.; Seki, N.; Kusukawa, J.; Yano, H. CD44v3+/CD24− cells possess cancer stem cell-like properties in human oral squamous cell carcinoma. Int. J. Oncol. 2016, 48, 99–109. [Google Scholar] [CrossRef] [Green Version]
- Franzmann, E.J.; Weed, D.T.; Civantos, F.J.; Goodwin, W.J.; Bourguignon, L.Y.W. A Novel CD44 v3 Isoform is Involved in Head and Neck Squamous Cell Carcinoma Progression. Otolaryngol. Head Neck Surg. 2016, 124, 426–432. [Google Scholar] [CrossRef]
- Spiegelberg, D.; Kuku, G.; Selvaraju, R.; Nestor, M. Characterization of CD44 variant expression in head and neck squamous cell carcinomas. Tumor Biol. 2014, 35, 2053–2062. [Google Scholar] [CrossRef] [Green Version]
- Theodoraki, M.; Matsumoto, A.; Beccard, I.; Hoffmann, T.K.; Whiteside, T.L. CD44v3 protein-carrying tumor-derived exosomes in HNSCC patients’ plasma as potential noninvasive biomarkers of disease activity. Oncoimmunology 2020, 9, 1747732. [Google Scholar] [CrossRef] [Green Version]
- Sanada, T.; Islam, A.; Kaminota, T.; Kirino, Y.; Tanimoto, R.; Yoshimitsu, H.; Yano, H.; Mizuno, Y.; Okada, M.; Mitani, S.; et al. Elevated exosomal lysyl oxidase like 2 is a potential biomarker for head and neck squamous cell carcinoma. Laryngoscope 2020, 130, E327–E334. [Google Scholar] [CrossRef]
- Liu, L.; Zuo, L.; Yang, J.; Xin, S.; Zhang, J.; Zhou, J.; Li, G.; Tang, J.; Lu, J. Exosomal cyclophilin A as a novel noninvasive biomarker for Epstein-Barr virus associated nasopharyngeal carcinoma. Cancer Med.-US 2019, 8, 3142–3151. [Google Scholar] [CrossRef] [Green Version]
- Chan, K.C.A.; Chu, S.W.I.; Lo, Y.M.D. Ambient Temperature and Screening for Nasopharyngeal Cancer. N. Engl. J. Med. 2018, 378, 962–963. [Google Scholar] [CrossRef]
- Rodrigues-Junior, D.M.; Tan, S.S.; de Souza Viana, L.; Carvalho, A.L.; Lim, S.K.; Iyer, N.G.; Vettore, A.L. A preliminary investigation of circulating extracellular vesicles and biomarker discovery associated with treatment response in head and neck squamous cell carcinoma. BMC Cancer 2019, 19, 373. [Google Scholar] [CrossRef]
- Winck, F.V.; Prado Ribeiro, A.C.; Ramos Domingues, R.; Ling, L.Y.; Riaño-Pachón, D.M.; Rivera, C.; Brandão, T.B.; Gouvea, A.F.; Santos-Silva, A.R.; Coletta, R.D.; et al. Insights into immune responses in oral cancer through proteomic analysis of saliva and salivary extracellular vesicles. Sci. Rep. 2015, 5, 16305. [Google Scholar] [CrossRef] [PubMed]
- Li, C.; Zhou, Y.; Liu, J.; Su, X.; Qin, H.; Huang, S.; Huang, X.; Zhou, N. Potential Markers from Serum-Purified Exosomes for Detecting Oral Squamous Cell Carcinoma Metastasis. Cancer Epidem. Biomar. 2019, 28, 1668–1681. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Trajkovic, K.; Hsu, C.; Chiantia, S.; Rajendran, L.; Wenzel, D.; Wieland, F.; Schwille, P.; Brugger, B.; Simons, M. Ceramide Triggers Budding of Exosome Vesicles into Multivesicular Endosomes. Science 2008, 319, 1244–1247. [Google Scholar] [CrossRef]
- Chinn, S.B.; Spector, M.E.; Bellile, E.L.; McHugh, J.B.; Gernon, T.J.; Bradford, C.R.; Wolf, G.T.; Eisbruch, A.; Chepeha, D.B. Impact of Perineural Invasion in the Pathologically N0 Neck in Oral Cavity Squamous Cell Carcinoma. Otolaryngol. Head Neck Surg. 2013, 149, 893–899. [Google Scholar] [CrossRef] [Green Version]
- Fagan, J.J.; Collins, B.; Barnes, L.; D’Amico, F.; Myers, E.N.; Johnson, J.T. Perineural Invasion in Squamous Cell Carcinoma of the Head and Neck. Arch. Otolaryngol. Head Neck Surg. 1998, 124, 637. [Google Scholar] [CrossRef] [Green Version]
- Madeo, M.; Colbert, P.L.; Vermeer, D.W.; Lucido, C.T.; Cain, J.T.; Vichaya, E.G.; Grossberg, A.J.; Muirhead, D.; Rickel, A.P.; Hong, Z.; et al. Cancer exosomes induce tumor innervation. Nat. Commun. 2018, 9, 4284. [Google Scholar] [CrossRef] [Green Version]
- Amit, M.; Takahashi, H.; Dragomir, M.P.; Lindemann, A.; Gleber-Netto, F.O.; Pickering, C.R.; Anfossi, S.; Osman, A.A.; Cai, Y.; Wang, R.; et al. Loss of p53 drives neuron reprogramming in head and neck cancer. Nature 2020, 578, 449–454. [Google Scholar] [CrossRef]
- Lu, A.; Wawro, P.; Morgens, D.W.; Portela, F.; Bassik, M.C.; Pfeffer, S.R. Genome-wide interrogation of extracellular vesicle biology using barcoded miRNAs. Elife 2018, 7, e41460. [Google Scholar] [CrossRef]
- Chulpanova, D.S.; Kitaeva, K.V.; James, V.; Rizvanov, A.A.; Solovyeva, V.V. Therapeutic Prospects of Extracellular Vesicles in Cancer Treatment. Front. Immunol. 2018, 9, 1534. [Google Scholar] [CrossRef] [Green Version]
- Lindenbergh, M.F.S.; Stoorvogel, W. Antigen Presentation by Extracellular Vesicles from Professional Antigen-Presenting Cells. Annu. Rev. Immunol. 2018, 36, 435–459. [Google Scholar] [CrossRef]
- Licitra, L.; Mesia, R.; Rivera, F.; Remenár, É.; Hitt, R.; Erfán, J.; Rottey, S.; Kawecki, A.; Zabolotnyy, D.; Benasso, M.; et al. Evaluation of EGFR gene copy number as a predictive biomarker for the efficacy of cetuximab in combination with chemotherapy in the first-line treatment of recurrent and/or metastatic squamous cell carcinoma of the head and neck: EXTREME study. Ann. Oncol. 2011, 22, 1078–1087. [Google Scholar] [CrossRef]
- Sento, S.; Sasabe, E.; Yamamoto, T. Application of a Persistent Heparin Treatment Inhibits the Malignant Potential of Oral Squamous Carcinoma Cells Induced by Tumor Cell-Derived Exosomes. PLoS ONE 2016, 11, e148454. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Elsharkasy, O.M.; Nordin, J.Z.; Hagey, D.W.; de Jong, O.G.; Schiffelers, R.M.; Andaloussi, S.E.; Vader, P. Extracellular vesicles as drug delivery systems: Why and how? Adv. Drug Deliv. Rev. 2020, 106, 148–156. [Google Scholar] [CrossRef] [PubMed]
- Tsao, A.S.; Liu, D.; Martin, J.; Tang, X.M.; Lee, J.J.; El-Naggar, A.K.; Wistuba, I.; Culotta, K.S.; Mao, L.; Gillenwater, A.; et al. Phase II Randomized, Placebo-Controlled Trial of Green Tea Extract in Patients with High-Risk Oral Premalignant Lesions. Cancer Prev. Res. 2009, 2, 931–941. [Google Scholar] [CrossRef] [Green Version]
- Amin, A.R.M.R.; Wang, D.; Zhang, H.; Peng, S.; Shin, H.J.C.; Brandes, J.C.; Tighiouart, M.; Khuri, F.R.; Chen, Z.G.; Shin, D.M. Enhanced Anti-tumor Activity by the Combination of the Natural Compounds (−)-Epigallocatechin-3-gallate and Luteolin. J. Biol. Chem. 2010, 285, 34557–34565. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shrotriya, S.; Agarwal, R.; Sclafani, R.A. A perspective on chemoprevention by resveratrol in head and neck squamous cell carcinoma. Adv. Exp. Med. Biol. 2015, 815, 333–348. [Google Scholar] [CrossRef]
- Siddiqui, I.A.; Adhami, V.M.; Bharali, D.J.; Hafeez, B.B.; Asim, M.; Khwaja, S.I.; Ahmad, N.; Cui, H.; Mousa, S.A.; Mukhtar, H. Introducing Nanochemoprevention as a Novel Approach for Cancer Control: Proof of Principle with Green Tea Polyphenol Epigallocatechin-3-Gallate. Cancer Res. 2009, 69, 1712–1716. [Google Scholar] [CrossRef] [Green Version]
- Majumdar, D.; Jung, K.H.; Zhang, H.; Nannapaneni, S.; Wang, X.; Amin, A.R.M.R.; Chen, Z.; Chen, Z.; Shin, D.M. Luteolin Nanoparticle in Chemoprevention: In Vitro and In Vivo Anticancer Activity. Cancer Prev. Res. 2014, 7, 65–73. [Google Scholar] [CrossRef] [Green Version]
- Mohan, A.; Narayanan, S.; Sethuraman, S.; Krishnan, U.M. Novel Resveratrol and 5-Fluorouracil Coencapsulated in PEGylated Nanoliposomes Improve Chemotherapeutic Efficacy of Combination against Head and Neck Squamous Cell Carcinoma. Biomed. Res. Int. 2014, 2014, 1–14. [Google Scholar] [CrossRef]
- Wang, L.; Yin, P.; Wang, J.; Wang, Y.; Sun, Z.; Zhou, Y.; Guan, X. Delivery of mesenchymal stem cells-derived extracellular vesicles with enriched miR-185 inhibits progression of OPMD. Artif. Cells Nanomed. Biotechnol. 2019, 47, 2481–2491. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- DeMarino, C.; Pleet, M.L.; Cowen, M.; Barclay, R.A.; Akpamagbo, Y.; Erickson, J.; Ndembi, N.; Charurat, M.; Jumare, J.; Bwala, S.; et al. Antiretroviral Drugs Alter the Content of Extracellular Vesicles from HIV-1-Infected Cells. Sci. Rep. 2018, 8, 7653. [Google Scholar] [CrossRef]
- Zhu, Y.; An, X.; Zhang, X.; Qiao, Y.; Zheng, T.; Li, X. STING: A master regulator in the cancer-immunity cycle. Mol. Cancer 2019, 18, 152. [Google Scholar] [CrossRef] [Green Version]
- Lu, S.; Concha-Benavente, F.; Shayan, G.; Srivastava, R.M.; Gibson, S.P.; Wang, L.; Gooding, W.E.; Ferris, R.L. STING activation enhances cetuximab-mediated NK cell activation and DC maturation and correlates with HPV+ status in head and neck cancer. Oral Oncol. 2018, 78, 186–193. [Google Scholar] [CrossRef]
- Jang, S.C.; Moniz, R.J.; Sia, C.L.; Harrison, R.A.; Houde, D.; Ross, N.; Xu, K.; Lewis, N.; Bourdeau, R.; McCoy, C.; et al. Abstract 944: exoSTING: An engineered exosome therapeutic that selectively delivers STING agonist to the tumor resident antigen-presenting cells resulting in improved tumor antigen-specific adaptive immune response. Cancer Res. 2019, 79, 944. [Google Scholar] [CrossRef]
- Moore, E.; Clavijo, P.E.; Davis, R.; Cash, H.; Van Waes, C.; Kim, Y.; Allen, C. Established T Cell-Inflamed Tumors Rejected after Adaptive Resistance Was Reversed by Combination STING Activation and PD-1 Pathway Blockade. Cancer Immunol. Res. 2016, 4, 1061–1071. [Google Scholar] [CrossRef] [Green Version]
- Gadkaree, S.K.; Fu, J.; Sen, R.; Korrer, M.J.; Allen, C.; Kim, Y.J. Induction of tumor regression by intratumoral STING agonists combined with anti-programmed death-L1 blocking antibody in a preclinical squamous cell carcinoma model. Head Neck 2017, 39, 1086–1094. [Google Scholar] [CrossRef] [PubMed]
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Qu, X.; Li, J.-W.; Chan, J.; Meehan, K. Extracellular Vesicles in Head and Neck Cancer: A Potential New Trend in Diagnosis, Prognosis, and Treatment. Int. J. Mol. Sci. 2020, 21, 8260. https://doi.org/10.3390/ijms21218260
Qu X, Li J-W, Chan J, Meehan K. Extracellular Vesicles in Head and Neck Cancer: A Potential New Trend in Diagnosis, Prognosis, and Treatment. International Journal of Molecular Sciences. 2020; 21(21):8260. https://doi.org/10.3390/ijms21218260
Chicago/Turabian StyleQu, Xinyu, Jing-Woei Li, Jason Chan, and Katie Meehan. 2020. "Extracellular Vesicles in Head and Neck Cancer: A Potential New Trend in Diagnosis, Prognosis, and Treatment" International Journal of Molecular Sciences 21, no. 21: 8260. https://doi.org/10.3390/ijms21218260