Advances in research of exosomes in thyroid diseases_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

CHEN Wenjie , WEI Tao , LI Zhihui , ZHU Jingqiang ,  LEI Jianyong

Thyroid and Parathyroid Surgery Center, West China Hospital of Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

LEI Jianyong, Email: leijianyong@scu.edu.cn

Keywords：

exosome; Graves’ disease; thyroid cancer; diagnosis; prognosis; review

DOI：

10.7507/1007-9424.201812026

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the relationship between exosome and thyroid diseases.Method The literatures reports on exosomes and the physiology, pathology and diseases of thyroid were collected and reviewed.Results Exosomes were secreted by cells and could be found in various body fluids, which could mediate the normal physiological development of the thyroid gland and play an important role in the progression of Graves’ disease. Exosomes could be used as diagnostic and differential diagnostic biomarkers for thyroid cancer and affect the growth, invasion, and metastasis of thyroid cancer. As a drug carrier for anti-thyroid cancer, exosome had a good targeting ability.Conclusion Exosomes play an important role in the development of various diseases of the thyroid gland, which have good application prospects in biomarkers for early diagnosis and prognostic evaluation, as well as targeted drug carriers for thyroid cancer.

Citation： CHEN Wenjie, WEI Tao, LI Zhihui, ZHU Jingqiang, LEI Jianyong. Advances in research of exosomes in thyroid diseases. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2019, 26(3): 358-363. doi: 10.7507/1007-9424.201812026 Copy

1.	Lim H, Devesa SS, Sosa JA, et al. Trends in thyroid cancer incidence and mortality in the United States, 1974-2013. JAMA, 2017, 317(13): 1338-1348.
2.	van der Pol E, Böing AN, Harrison P, et al. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev, 2012, 64(3): 676-705.
3.	Nabet BY, Qiu Y, Shabason JE, et al. Exosome RNA unshielding couples stromal activation to pattern recognition receptor signaling in cancer. Cell, 2017, 170(2): 352-366.
4.	Zhang H, Deng T, Liu R, et al. Exosome-delivered EGFR regulates liver microenvironment to promote gastric cancer liver metastasis. Nat Commun, 2017, 8: 15016.
5.	Ren J, He W, Zheng L, et al. From structures to functions: insights into exosomes as promising drug delivery vehicles. Biomater Sci, 2016, 4(6): 910-921.
6.	Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell, 1983, 33(3): 967-978.
7.	Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol, 1983, 97(2): 329-339.
8.	Johnstone RM, Adam M, Hammond JR, et al. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem, 1987, 262(19): 9412-9420.
9.	Valadi H, Ekström K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol, 2007, 9(6): 654-659.
10.	Skog J, Würdinger T, van Rijn S, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol, 2008, 10(12): 1470-1476.
11.	Gibbings DJ, Ciaudo C, Erhardt M, et al. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol, 2009, 11(9): 1143-1149.
12.	Balaj L, Lessard R, Dai L, et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun, 2011, 2: 180.
13.	Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics, 2010, 73(10): 1907-1920.
14.	Suchorska WM, Lach MS. The role of exosomes in tumor progression and metastasis (review). Oncol Rep, 2016, 35(3): 1237-1244.
15.	Caby MP, Lankar D, Vincendeau-Scherrer C, et al. Exosomal-like vesicles are present in human blood plasma. Int Immunol, 2005, 17(7): 879-887.
16.	Ogawa Y, Miura Y, Harazono A, et al. Proteomic analysis of two types of exosomes in human whole saliva. Biol Pharm Bull, 2011, 34(1): 13-23.
17.	Admyre C, Johansson SM, Qazi KR, et al. Exosomes with immune modulatory features are present in human breast milk. J Immunol, 2007, 179(3): 1969-1978.
18.	Ronquist G, Brody I. The prostasome: its secretion and function in man. Biochim Biophys Acta, 1985, 822(2): 203-218.
19.	Park KH, Kim BJ, Kang J, et al. Ca²⁺ signaling tools acquired from prostasomes are required for progesterone-induced sperm motility. Sci Signal, 2011, 4(173): ra31.
20.	Pisitkun T, Shen RF, Knepper MA. Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci U S A, 2004, 101(36): 13368-13373.
21.	Vella LJ, Sharples RA, Lawson VA, et al. Packaging of prions into exosomes is associated with a novel pathway of PrP processing. J Pathol, 2007, 211(5): 582-590.
22.	Masyuk AI, Huang BQ, Ward CJ, et al. Biliary exosomes influence cholangiocyte regulatory mechanisms and proliferation through interaction with primary cilia. Am J Physiol Gastrointest Liver Physiol, 2010, 299(4): G990-G999.
23.	Yáñez-Mó M, Siljander PR, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles, 2015, 4: 27066.
24.	EL Andaloussi S, Mäger I, Breakefield XO, et al. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov, 2013, 12(5): 347-357.
25.	Hick AC, Delmarcelle AS, Bouquet M, et al. Reciprocal epithelial: endothelial paracrine interactions during thyroid development govern follicular organization and C-cells differentiation. Dev Biol, 2013, 381(1): 227-240.
26.	Villacorte M, Delmarcelle AS, Lernoux M, et al. Thyroid follicle development requires Smad1/5- and endothelial cell-dependent basement membrane assembly. Development, 2016, 143(11): 1958-1970.
27.	Degosserie J, Heymans C, Spourquet C, et al. Extracellular vesicles from endothelial progenitor cells promote thyroid follicle formation. J Extracell Vesicles, 2018, 7(1): 1487250.
28.	Belge G, Rippe V, Meiboom M, et al. Delineation of a 150-kb breakpoint cluster in benign thyroid tumors with 19q13.4 aberrations. Cytogenet Cell Genet, 2001, 93(1-2): 48-51.
29.	Rippe V, Dittberner L, Lorenz VN, et al. The two stem cell microRNA gene clusters C19MC and miR-371-3 are activated by specific chromosomal rearrangements in a subgroup of thyroid adenomas. PLoS One, 2010, 5(3): e9485.
30.	Bullerdiek J, Flor I. Exosome-delivered microRNAs of " chromosome 19 microRNA cluster” as immunomodulators in pregnancy and tumorigenesis. Mol Cytogenet, 2012, 5(1): 27.
31.	Vlasov P, Doi SQ, Sellitti DF. FRTL-5 rat thyroid cells release thyroglobulin sequestered in exosomes: a possible novel mechanism for thyroglobulin processing in the thyroid. J Thyroid Res, 2016, 2016: 9276402.
32.	Bernecker C, Lenz L, Ostapczuk MS, et al. MicroRNAs miR-146a1, miR-155_2, and miR-200a1 are regulated in autoimmune thyroid diseases. Thyroid, 2012, 22(12): 1294-1295.
33.	Yamada H, Itoh M, Hiratsuka I, et al. Circulating microRNAs in autoimmune thyroid diseases. Clin Endocrinol (Oxf), 2014, 81(2): 276-281.
34.	Hiratsuka I, Yamada H, Munetsuna E, et al. Circulating microRNAs in Graves’ disease in relation to clinical activity. Thyroid, 2016, 26(10): 1431-1440.
35.	Lee JC, Zhao JT, Gundara J, et al. Papillary thyroid cancer-derived exosomes contain miRNA-146b and miRNA-222. J Surg Res, 2015, 196(1): 39-48.
36.	Samsonov R, Burdakov V, Shtam T, et al. Plasma exosomal miR-21 and miR-181a differentiates follicular from papillary thyroid cancer. Tumour Biol, 2016, 37(9): 12011-12021.
37.	Boufraqech M, Zhang L, Jain M, et al. miR-145 suppresses thyroid cancer growth and metastasis and targets AKT3. Endocr Relat Cancer, 2014, 21(4): 517-531.
38.	Peinado H, Alečković M, Lavotshkin S, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med, 2012, 18(6): 883-891.
39.	Melo SA, Luecke LB, Kahlert C, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature, 2015, 523(7559): 177-182.
40.	Costa-Silva B, Aiello NM, Ocean AJ, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol, 2015, 17(6): 816-826.
41.	Vella LJ. The emerging role of exosomes in epithelial-mes- enchymal-transition in cancer. Front Oncol, 2014, 4: 361.
42.	Greening DW, Gopal SK, Mathias RA, et al. Emerging roles of exosomes during epithelial-mesenchymal transition and cancer progression. Semin Cell Dev Biol, 2015, 40: 60-71.
43.	Thiery JP, Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol, 2006, 7(2): 131-142.
44.	Hardin H, Guo Z, Shan W, et al. The roles of the epithelial-mesenchymal transition marker PRRX1 and miR-146b-5p in papillary thyroid carcinoma progression. Am J Pathol, 2014, 184(8): 2342-2354.
45.	Pradella D, Naro C, Sette C, et al. EMT and stemness: flexible processes tuned by alternative splicing in development and cancer progression. Mol Cancer, 2017, 16(1): 8.
46.	Hardin H, Helein H, Meyer K, et al. Thyroid cancer stem-like cell exosomes: regulation of EMT via transfer of lncRNAs. Lab Invest, 2018, 98(9): 1133-1142.
47.	Luo D, Zhan S, Xia W, et al. Proteomics study of serum exosomes from papillary thyroid cancer patients. Endocr Relat Cancer, 2018, 25(10): 879-891.
48.	Zhuang X, Xiang X, Grizzle W, et al. Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Mol Ther, 2011, 19(10): 1769-1779.
49.	Yang T, Martin P, Fogarty B, et al. Exosome delivered anticancer drugs across the blood-brain barrier for brain cancer therapy in Danio rerio. Pharm Res, 2015, 32(6): 2003-2014.
50.	Tian Y, Li S, Song J, et al. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials, 2014, 35(7): 2383-2390.
51.	Gangadaran P, Li XJ, Kalimuthu SK, et al. New optical imaging reporter-labeled anaplastic thyroid cancer-derived extracellular vesicles as a platform for in vivo tumor targeting in a mouse model. Sci Rep, 2018, 8(1): 13509.
52.	Parolini I, Federici C, Raggi C, et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem, 2009, 284(49): 34211-34222.
53.	Smyth TJ, Redzic JS, Graner MW, et al. Examination of the specificity of tumor cell derived exosomes with tumor cells in vitro. Biochim Biophys Acta, 2014, 1838(11): 2954-2965.
54.	Smyth T, Kullberg M, Malik N, et al. Biodistribution and delivery efficiency of unmodified tumor-derived exosomes. J Control Release, 2015, 199: 145-155.
55.	Zhu L, Li XJ, Kalimuthu S, et al. Natural killer cell (NK-92MI)-based therapy for pulmonary metastasis of anaplastic thyroid cancer in a nude mouse model. Front Immunol, 2017, 8: 816.
56.	Shoae-Hassani A, Hamidieh AA, Behfar M, et al. NK cell-derived exosomes from NK cells previously exposed to neuroblastoma cells augment the antitumor activity of cytokine-activated NK cells. J Immunother, 2017, 40(7): 265-276.
57.	Zhang G, Liu R, Zhu X, et al. Retargeting NK-92 for anti-melanoma activity by a TCR-like single-domain antibody. Immunol Cell Biol, 2013, 91(10): 615-624.
58.	Fais S. NK cell-released exosomes: natural nanobullets against tumors. Oncoimmunology, 2013, 2(1): e22337.
59.	Zhu L, Kalimuthu S, Gangadaran P, et al. Exosomes derived from natural killer cells exert therapeutic effect in melanoma. Theranostics, 2017, 7(10): 2732-2745.
60.	Kalimuthu S, Gangadaran P, Li XJ, et al. In vivo therapeutic potential of mesenchymal stem cell-derived extracellular vesicles with optical imaging reporter in tumor mice model. Sci Rep, 2016, 6: 30418.
61.	Jang SC, Gho YS. Could bioengineered exosome-mimetic nanovesicles be an efficient strategy for the delivery of chemo- therapeutics? Nanomedicine (Lond), 2014, 9(2): 177-180.
62.	Wagner JA, Rosario M, Romee R, et al. CD56bright NK cells exhibit potent antitumor responses following IL-15 priming. J Clin Invest, 2017, 127(11): 4042-4058.
63.	Zhu L, Kalimuthu S, Oh JM, et al. Enhancement of antitumor potency of extracellular vesicles derived from natural killer cells by IL-15 priming. Biomaterials, 2019, 190-191: 38-50.
64.	Zhu L, Gangadaran P, Kalimuthu S, et al. Novel alternatives to extracellular vesicle-based immunotherapy-exosome mimetics derived from natural killer cells. Artif Cells Nanomed Biotechnol, 2018, [Epub ahead of print].
65.	Yang Z, Xie J, Zhu J, et al. Functional exosome-mimic for delivery of siRNA to cancer: in vitro and in vivo evaluation. J Control Release, 2016, 243: 160-171.
66.	黄胜林; 复旦大学医学院上海肿瘤研究所. exoRBase: a database of circRNA, lncRNA and mRNA in human blood exosomes. 2018-01-04. http://www.exorbase.org/.
67.	Zhou CF, Ma J, Huang L, et al. Cervical squamous cell carcinoma-secreted exosomal miR-221-3p promotes lymphangiogenesis and lymphatic metastasis by targeting VASH1. Oncogene, 2018, [Epub ahead of print].
68.	Yen EY, Miaw SC, Yu JS, et al. Exosomal TGF-β1 is correlated with lymphatic metastasis of gastric cancers. Am J Cancer Res, 2017, 7(11): 2199-2208.
69.	韩茜, 张广, 孙辉. 超声引导下热消融治疗甲状腺微小乳头状癌研究进展. 中国普外基础与临床杂志, 2017, 24(9): 1156-1160.

1. Lim H, Devesa SS, Sosa JA, et al. Trends in thyroid cancer incidence and mortality in the United States, 1974-2013. JAMA, 2017, 317(13): 1338-1348.
2. van der Pol E, Böing AN, Harrison P, et al. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev, 2012, 64(3): 676-705.
3. Nabet BY, Qiu Y, Shabason JE, et al. Exosome RNA unshielding couples stromal activation to pattern recognition receptor signaling in cancer. Cell, 2017, 170(2): 352-366.
4. Zhang H, Deng T, Liu R, et al. Exosome-delivered EGFR regulates liver microenvironment to promote gastric cancer liver metastasis. Nat Commun, 2017, 8: 15016.
5. Ren J, He W, Zheng L, et al. From structures to functions: insights into exosomes as promising drug delivery vehicles. Biomater Sci, 2016, 4(6): 910-921.
6. Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell, 1983, 33(3): 967-978.
7. Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol, 1983, 97(2): 329-339.
8. Johnstone RM, Adam M, Hammond JR, et al. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem, 1987, 262(19): 9412-9420.
9. Valadi H, Ekström K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol, 2007, 9(6): 654-659.
10. Skog J, Würdinger T, van Rijn S, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol, 2008, 10(12): 1470-1476.
11. Gibbings DJ, Ciaudo C, Erhardt M, et al. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol, 2009, 11(9): 1143-1149.
12. Balaj L, Lessard R, Dai L, et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun, 2011, 2: 180.
13. Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics, 2010, 73(10): 1907-1920.
14. Suchorska WM, Lach MS. The role of exosomes in tumor progression and metastasis (review). Oncol Rep, 2016, 35(3): 1237-1244.
15. Caby MP, Lankar D, Vincendeau-Scherrer C, et al. Exosomal-like vesicles are present in human blood plasma. Int Immunol, 2005, 17(7): 879-887.
16. Ogawa Y, Miura Y, Harazono A, et al. Proteomic analysis of two types of exosomes in human whole saliva. Biol Pharm Bull, 2011, 34(1): 13-23.
17. Admyre C, Johansson SM, Qazi KR, et al. Exosomes with immune modulatory features are present in human breast milk. J Immunol, 2007, 179(3): 1969-1978.
18. Ronquist G, Brody I. The prostasome: its secretion and function in man. Biochim Biophys Acta, 1985, 822(2): 203-218.
19. Park KH, Kim BJ, Kang J, et al. Ca²⁺ signaling tools acquired from prostasomes are required for progesterone-induced sperm motility. Sci Signal, 2011, 4(173): ra31.
20. Pisitkun T, Shen RF, Knepper MA. Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci U S A, 2004, 101(36): 13368-13373.
21. Vella LJ, Sharples RA, Lawson VA, et al. Packaging of prions into exosomes is associated with a novel pathway of PrP processing. J Pathol, 2007, 211(5): 582-590.
22. Masyuk AI, Huang BQ, Ward CJ, et al. Biliary exosomes influence cholangiocyte regulatory mechanisms and proliferation through interaction with primary cilia. Am J Physiol Gastrointest Liver Physiol, 2010, 299(4): G990-G999.
23. Yáñez-Mó M, Siljander PR, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles, 2015, 4: 27066.
24. EL Andaloussi S, Mäger I, Breakefield XO, et al. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov, 2013, 12(5): 347-357.
25. Hick AC, Delmarcelle AS, Bouquet M, et al. Reciprocal epithelial: endothelial paracrine interactions during thyroid development govern follicular organization and C-cells differentiation. Dev Biol, 2013, 381(1): 227-240.
26. Villacorte M, Delmarcelle AS, Lernoux M, et al. Thyroid follicle development requires Smad1/5- and endothelial cell-dependent basement membrane assembly. Development, 2016, 143(11): 1958-1970.
27. Degosserie J, Heymans C, Spourquet C, et al. Extracellular vesicles from endothelial progenitor cells promote thyroid follicle formation. J Extracell Vesicles, 2018, 7(1): 1487250.
28. Belge G, Rippe V, Meiboom M, et al. Delineation of a 150-kb breakpoint cluster in benign thyroid tumors with 19q13.4 aberrations. Cytogenet Cell Genet, 2001, 93(1-2): 48-51.
29. Rippe V, Dittberner L, Lorenz VN, et al. The two stem cell microRNA gene clusters C19MC and miR-371-3 are activated by specific chromosomal rearrangements in a subgroup of thyroid adenomas. PLoS One, 2010, 5(3): e9485.
30. Bullerdiek J, Flor I. Exosome-delivered microRNAs of " chromosome 19 microRNA cluster” as immunomodulators in pregnancy and tumorigenesis. Mol Cytogenet, 2012, 5(1): 27.
31. Vlasov P, Doi SQ, Sellitti DF. FRTL-5 rat thyroid cells release thyroglobulin sequestered in exosomes: a possible novel mechanism for thyroglobulin processing in the thyroid. J Thyroid Res, 2016, 2016: 9276402.
32. Bernecker C, Lenz L, Ostapczuk MS, et al. MicroRNAs miR-146a1, miR-155_2, and miR-200a1 are regulated in autoimmune thyroid diseases. Thyroid, 2012, 22(12): 1294-1295.
33. Yamada H, Itoh M, Hiratsuka I, et al. Circulating microRNAs in autoimmune thyroid diseases. Clin Endocrinol (Oxf), 2014, 81(2): 276-281.
34. Hiratsuka I, Yamada H, Munetsuna E, et al. Circulating microRNAs in Graves’ disease in relation to clinical activity. Thyroid, 2016, 26(10): 1431-1440.
35. Lee JC, Zhao JT, Gundara J, et al. Papillary thyroid cancer-derived exosomes contain miRNA-146b and miRNA-222. J Surg Res, 2015, 196(1): 39-48.
36. Samsonov R, Burdakov V, Shtam T, et al. Plasma exosomal miR-21 and miR-181a differentiates follicular from papillary thyroid cancer. Tumour Biol, 2016, 37(9): 12011-12021.
37. Boufraqech M, Zhang L, Jain M, et al. miR-145 suppresses thyroid cancer growth and metastasis and targets AKT3. Endocr Relat Cancer, 2014, 21(4): 517-531.
38. Peinado H, Alečković M, Lavotshkin S, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med, 2012, 18(6): 883-891.
39. Melo SA, Luecke LB, Kahlert C, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature, 2015, 523(7559): 177-182.
40. Costa-Silva B, Aiello NM, Ocean AJ, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol, 2015, 17(6): 816-826.
41. Vella LJ. The emerging role of exosomes in epithelial-mes- enchymal-transition in cancer. Front Oncol, 2014, 4: 361.
42. Greening DW, Gopal SK, Mathias RA, et al. Emerging roles of exosomes during epithelial-mesenchymal transition and cancer progression. Semin Cell Dev Biol, 2015, 40: 60-71.
43. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol, 2006, 7(2): 131-142.
44. Hardin H, Guo Z, Shan W, et al. The roles of the epithelial-mesenchymal transition marker PRRX1 and miR-146b-5p in papillary thyroid carcinoma progression. Am J Pathol, 2014, 184(8): 2342-2354.
45. Pradella D, Naro C, Sette C, et al. EMT and stemness: flexible processes tuned by alternative splicing in development and cancer progression. Mol Cancer, 2017, 16(1): 8.
46. Hardin H, Helein H, Meyer K, et al. Thyroid cancer stem-like cell exosomes: regulation of EMT via transfer of lncRNAs. Lab Invest, 2018, 98(9): 1133-1142.
47. Luo D, Zhan S, Xia W, et al. Proteomics study of serum exosomes from papillary thyroid cancer patients. Endocr Relat Cancer, 2018, 25(10): 879-891.
48. Zhuang X, Xiang X, Grizzle W, et al. Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Mol Ther, 2011, 19(10): 1769-1779.
49. Yang T, Martin P, Fogarty B, et al. Exosome delivered anticancer drugs across the blood-brain barrier for brain cancer therapy in Danio rerio. Pharm Res, 2015, 32(6): 2003-2014.
50. Tian Y, Li S, Song J, et al. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials, 2014, 35(7): 2383-2390.
51. Gangadaran P, Li XJ, Kalimuthu SK, et al. New optical imaging reporter-labeled anaplastic thyroid cancer-derived extracellular vesicles as a platform for in vivo tumor targeting in a mouse model. Sci Rep, 2018, 8(1): 13509.
52. Parolini I, Federici C, Raggi C, et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem, 2009, 284(49): 34211-34222.
53. Smyth TJ, Redzic JS, Graner MW, et al. Examination of the specificity of tumor cell derived exosomes with tumor cells in vitro. Biochim Biophys Acta, 2014, 1838(11): 2954-2965.
54. Smyth T, Kullberg M, Malik N, et al. Biodistribution and delivery efficiency of unmodified tumor-derived exosomes. J Control Release, 2015, 199: 145-155.
55. Zhu L, Li XJ, Kalimuthu S, et al. Natural killer cell (NK-92MI)-based therapy for pulmonary metastasis of anaplastic thyroid cancer in a nude mouse model. Front Immunol, 2017, 8: 816.
56. Shoae-Hassani A, Hamidieh AA, Behfar M, et al. NK cell-derived exosomes from NK cells previously exposed to neuroblastoma cells augment the antitumor activity of cytokine-activated NK cells. J Immunother, 2017, 40(7): 265-276.
57. Zhang G, Liu R, Zhu X, et al. Retargeting NK-92 for anti-melanoma activity by a TCR-like single-domain antibody. Immunol Cell Biol, 2013, 91(10): 615-624.
58. Fais S. NK cell-released exosomes: natural nanobullets against tumors. Oncoimmunology, 2013, 2(1): e22337.
59. Zhu L, Kalimuthu S, Gangadaran P, et al. Exosomes derived from natural killer cells exert therapeutic effect in melanoma. Theranostics, 2017, 7(10): 2732-2745.
60. Kalimuthu S, Gangadaran P, Li XJ, et al. In vivo therapeutic potential of mesenchymal stem cell-derived extracellular vesicles with optical imaging reporter in tumor mice model. Sci Rep, 2016, 6: 30418.
61. Jang SC, Gho YS. Could bioengineered exosome-mimetic nanovesicles be an efficient strategy for the delivery of chemo- therapeutics? Nanomedicine (Lond), 2014, 9(2): 177-180.
62. Wagner JA, Rosario M, Romee R, et al. CD56bright NK cells exhibit potent antitumor responses following IL-15 priming. J Clin Invest, 2017, 127(11): 4042-4058.
63. Zhu L, Kalimuthu S, Oh JM, et al. Enhancement of antitumor potency of extracellular vesicles derived from natural killer cells by IL-15 priming. Biomaterials, 2019, 190-191: 38-50.
64. Zhu L, Gangadaran P, Kalimuthu S, et al. Novel alternatives to extracellular vesicle-based immunotherapy-exosome mimetics derived from natural killer cells. Artif Cells Nanomed Biotechnol, 2018, [Epub ahead of print].
65. Yang Z, Xie J, Zhu J, et al. Functional exosome-mimic for delivery of siRNA to cancer: in vitro and in vivo evaluation. J Control Release, 2016, 243: 160-171.
66. 黄胜林; 复旦大学医学院上海肿瘤研究所. exoRBase: a database of circRNA, lncRNA and mRNA in human blood exosomes. 2018-01-04. http://www.exorbase.org/.
67. Zhou CF, Ma J, Huang L, et al. Cervical squamous cell carcinoma-secreted exosomal miR-221-3p promotes lymphangiogenesis and lymphatic metastasis by targeting VASH1. Oncogene, 2018, [Epub ahead of print].
68. Yen EY, Miaw SC, Yu JS, et al. Exosomal TGF-β1 is correlated with lymphatic metastasis of gastric cancers. Am J Cancer Res, 2017, 7(11): 2199-2208.
69. 韩茜, 张广, 孙辉. 超声引导下热消融治疗甲状腺微小乳头状癌研究进展. 中国普外基础与临床杂志, 2017, 24(9): 1156-1160.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Advances in research of exosomes in thyroid diseases

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