Mesenchymal stem cells derived exosomes:an alternative drug carrier for eye disease_Chinese Journal of Ocular Fundus Diseases

Authors：

Xie Ruotian ,  Zhang Xiaomin

Tianjin Medical University Eye Hospital, Tianjin Medical University Eye Institute, Tianjin Medical University School of Optometry and Ophthalmology, Tianjin 300384, China;

Corresponding author：

Zhang Xiaomin, Email: xiaomzh@126.com

Keywords：

Mesenchymal stem cells; Exosomes; Drug carriers; Review

DOI：

10.3760/cma.j.issn.1005-1015.2019.02.021

Video：

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Abstract Full text Figures/Tables Video References Cited by

Mesenchymal stem cells (MSCs) are considered as an ideal treatment for multiple diseases including ocular disease. Recent studies have demonstrated that MSCs-derived exosomes have similar functions with MSCs. Exosomes are nanovesicles surrounded by a phospholipid layer that shuttle active cargo between different cells. They are capable of passing the biological barrier and have potentials to be utilized as natural carrier for the ocular drug delivery.

Citation： Xie Ruotian, Zhang Xiaomin. Mesenchymal stem cells derived exosomes:an alternative drug carrier for eye disease. Chinese Journal of Ocular Fundus Diseases, 2019, 35(2): 211-214. doi: 10.3760/cma.j.issn.1005-1015.2019.02.021 Copy

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2.	Gu S, Xing C, Han J, et al. Differentiation of rabbit bone marrow mesenchymal stem cells into corneal epithelial cells in vivo and ex vivo[J]. Mol Vis, 2009, 15: 99-107.
3.	Tomatsu S, Montano AM, Dung VC, et al. Mutations and polymorphisms in GUSB gene in mucopolysaccharidosis Ⅶ(Sly Syndrome)[J]. Hum Mutat, 2009, 30(4): 511-519. DOI: 10.1002/humu.20828.
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5.	Ko JH, Lee HJ, Jeong HJ, et al. Mesenchymal stem/stromal cells precondition lung monocytes/macrophages to produce tolerance against allo-and autoimmunity in the eye[J]. Proc Natl Acad Sci USA, 2016, 113(1): 158-163. DOI: 10.1073/pnas.1522905113.
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7.	Mead B, Logan A, Berry M, et al. Concise review: dental pulp stem cells: a novel cell therapy for retinal and central nervous system repair[J]. Stem Cells, 2017, 35(1): 61-67. DOI: 10.1002/stem.2398.
8.	Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators[J]. J Cell Biochem, 2006, 98(5): 1076-1084. DOI: 10.1002/jcb.20886.
9.	Camussi G, Deregibus MC, Bruno S, et al. Exosomes/microvesicles as a mechanism of cell-to-cell communication[J]. Kidney Int, 2010, 78(9): 838-848. DOI: 10.1038/ki.2010.278.
10.	Ramachandran S, Palanisamy V. Horizontal transfer of RNAs: exosomes as mediators of intercellular communication[J]. Wiley Interdiscip Rev RNA, 2012, 3(2): 286-293. DOI: 10.1002/wrna.115.
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13.	Muller G. Microvesicles/exosomes as potential novel biomarkers of metabolic diseases[J]. Diabetes Metab Syndr Obes, 2012, 5: 247-282. DOI: 10.2147/DMSO.S32923.
14.	Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses[J]. Nat Rev Immunol, 2009, 9(8): 581-593. DOI: 10.1038/nri2567.
15.	Ratajczak J, Miekus K, Kucia M, et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery[J]. Leukemia, 2006, 20(5): 847-856. DOI: 10.1038/sj.leu.2404132.
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17.	Cantaluppi V, Gatti S, Medica D, et al. Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells[J]. Kidney Int, 2012, 82(4): 412-427. DOI: 10.1038/ki.2012.105.
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24.	Zhang B, Yin Y, Lai RC, et al. Mesenchymal stem cells secrete immunologically active exosomes[J]. Stem Cells Dev, 2014, 23(11): 1233-1244. DOI: 10.1089/scd.2013.0479.
25.	Conforti A, Scarsella M, Starc N, et al. Microvescicles derived from mesenchymal stromal cells are not as effective as their cellular counterpart in the ability to modulate immune responses in vitro[J]. Stem Cells Dev, 2014, 23(21): 2591-2599. DOI: 10.1089/scd.2014.0091.
26.	Kordelas L, Rebmann V, Ludwig AK, et al. MSC-derived exosomes: a novel tool to treat therapy-refractory graft-versus-host disease[J]. Leukemia, 2014, 28(4): 970-973. DOI: 10.1038/leu.2014.41.
27.	Du W, Zhang K, Zhang S, et al. Enhanced proangiogenic potential of mesenchymal stem cell-derived exosomes stimulated by a nitric oxide releasing polymer[J]. Biomaterials, 2017, 133: 70-81. DOI: 10.1016/j.biomaterials.2017.04.030.
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30.	Mead B, Tomarev S. Bone marrow-derived mesenchymal stem cells-derived exosomes promote survival of retinal ganglion cells through miRNA-dependent mechanisms[J]. Stem Cells Transl Med, 2017, 6(4): 1273-1285. DOI: 10.1002/sctm.16-0428.
31.	Eggenhofer E, Benseler V, Kroemer A, et al. Mesenchymal stem cells are short-lived and do not migrate beyond the lungs after intravenous infusion[J/OL]. Front Immunol, 2012, 3: 297[2012-09-26]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3458305/. DOI: 10.3389/fimmu.2012.00297.
32.	Kuriyan AE, Albini TA, Townsend JH, et al. Vision loss after intravitreal injection of autologous "stem cells" for AMD[J]. N Engl J Med, 2017, 376(11): 1047-1053. DOI: 10.1056/NEJMoa1609583.
33.	Xitong D, Xiaorong Z. Targeted therapeutic delivery using engineered exosomes and its applications in cardiovascular diseases[J]. Gene, 2016, 575(2 Pt 2): 377-384. DOI: 10.1016/j.gene.2015.08.067.
34.	Peinado H, Aleckovic M, Lavotshkin S, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET[J]. Nat Med, 2012, 18(6): 883-891. DOI: 10.1038/nm.2753.
35.	Tian Y, Li S, Song J, et al. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy[J]. Biomaterials, 2014, 35(7): 2383-2390. DOI: 10.1016/j.biomaterials.2013.11.083.
36.	Wen D, Peng Y, Liu D, et al. Mesenchymal stem cell and derived exosome as small RNA carrier and Immunomodulator to improve islet transplantation[J]. J Control Release, 2016, 238: 166-175. DOI: 10.1016/j.jconrel.2016.07.044.
37.	Beauvillain C, Juste MO, Dion S, et al. Exosomes are an effective vaccine against congenital toxoplasmosis in mice[J]. Vaccine, 2009, 27(11): 1750-1757. DOI: 10.1016/j.vaccine.2009.01.022.
38.	Haney MJ, Klyachko NL, Zhao Y, et al. Exosomes as drug delivery vehicles for Parkinson's disease therapy[J]. J Control Release, 2015, 207: 18-30. DOI: 10.1016/j.jconrel.2015.03.033.
39.	Yang Y, Hong Y, Nam GH, et al. Virus-mimetic fusogenic exosomes for direct delivery of integral membrane proteins to target cell membranes[J]. Adv Mater, 2017, 29(13)[2017-02-06]. https://onlinelibrary.wiley.com/doi/abs/10.1002/adma.201605604. DOI: 10.1002/adma.201605604.
40.	Sun D, Zhuang X, Xiang X, et al. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes[J]. Mol Ther, 2010, 18(9): 1606-1614. DOI: 10.1038/mt.2010.105.
41.	Alvarez-Erviti L, Seow Y, Yin H, et al. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes[J]. Nat Biotechnol, 2011, 29(4): 341-345. DOI: 10.1038/nbt.1807.
42.	Johnsen KB, Gudbergsson JM, Skov MN, et al. Evaluation of electroporation-induced adverse effects on adipose-derived stem cell exosomes[J]. Cytotechnology, 2016, 68(5): 2125-2138. DOI: 10.1007/s10616-016-9952-7.
43.	Kim MS, Haney MJ, Zhao Y, et al. Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells[J]. Nanomedicine, 2016, 12(3): 655-664. DOI: 10.1016/j.nano.2015.10.012.
44.	Mizrak A, Bolukbasi MF, Ozdener GB, et al. Genetically engineered microvesicles carrying suicide mRNA/protein inhibit schwannoma tumor growth[J]. Mol Ther, 2013, 21(1): 101-108. DOI: 10.1038/mt.2012.161.
45.	Wang B, Yao K, Huuskes BM, et al. Mesenchymal stem cells deliver exogenous microRNA-let7c via exosomes to attenuate renal fibrosis[J]. Mol Ther, 2016, 24(7): 1290-1301. DOI: 10.1038/mt.2016.90.
46.	Lou G, Song X, Yang F, et al. Exosomes derived from miR-122-modified adipose tissue-derived MSCs increase chemosensitivity of hepatocellular carcinoma[J/OL]. J Hematol Oncol, 2015, 8: 122[2015-10-29]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4627430/. DOI: 10.1186/s13045-015-0220-7.
47.	Willms E, Johansson HJ, Mager I, et al. Cells release subpopulations of exosomes with distinct molecular and biological properties[J/OL]. Sci Rep, 2016, 6: 22519[2016-03-02]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4773763/. DOI: 10.1038/srep22519.
48.	Lotvall J, Hill AF, Hochberg F, et al. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles[J]. J Extracell Vesicles, 2014, 3: 26913[2014-12-22]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4275645/. DOI: 10.3402/jev.v3.26913.

1. Caplan AI. Mesenchymal stem cells[J]. J Orthop Res, 1991, 9(5): 641-650. DOI: 10.1002/jor.1100090504.
2. Gu S, Xing C, Han J, et al. Differentiation of rabbit bone marrow mesenchymal stem cells into corneal epithelial cells in vivo and ex vivo[J]. Mol Vis, 2009, 15: 99-107.
3. Tomatsu S, Montano AM, Dung VC, et al. Mutations and polymorphisms in GUSB gene in mucopolysaccharidosis Ⅶ(Sly Syndrome)[J]. Hum Mutat, 2009, 30(4): 511-519. DOI: 10.1002/humu.20828.
4. Nakashima H. Membranous nephropathy is developed under Th2 environment in chronic graft-versus-host disease[J]. Med Hypotheses, 2007, 69(4): 787-791. DOI: 10.1016/j.mehy.2007.02.015.
5. Ko JH, Lee HJ, Jeong HJ, et al. Mesenchymal stem/stromal cells precondition lung monocytes/macrophages to produce tolerance against allo-and autoimmunity in the eye[J]. Proc Natl Acad Sci USA, 2016, 113(1): 158-163. DOI: 10.1073/pnas.1522905113.
6. Park SS, Moisseiev E, Bauer G, et al. Advances in bone marrow stem cell therapy for retinal dysfunction[J]. Prog Retin Eye Res, 2017, 56: 148-165. DOI: 10.1016/j.preteyeres.2016.10.002.
7. Mead B, Logan A, Berry M, et al. Concise review: dental pulp stem cells: a novel cell therapy for retinal and central nervous system repair[J]. Stem Cells, 2017, 35(1): 61-67. DOI: 10.1002/stem.2398.
8. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators[J]. J Cell Biochem, 2006, 98(5): 1076-1084. DOI: 10.1002/jcb.20886.
9. Camussi G, Deregibus MC, Bruno S, et al. Exosomes/microvesicles as a mechanism of cell-to-cell communication[J]. Kidney Int, 2010, 78(9): 838-848. DOI: 10.1038/ki.2010.278.
10. Ramachandran S, Palanisamy V. Horizontal transfer of RNAs: exosomes as mediators of intercellular communication[J]. Wiley Interdiscip Rev RNA, 2012, 3(2): 286-293. DOI: 10.1002/wrna.115.
11. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends[J]. J Cell Biol, 2013, 200(4): 373-383. DOI: 10.1083/jcb.201211138.
12. Hurley JH, Odorizzi G. Get on the exosome bus with ALIX[J]. Nat Cell Biol, 2012, 14(7): 654-655. DOI: 10.1038/ncb2530.
13. Muller G. Microvesicles/exosomes as potential novel biomarkers of metabolic diseases[J]. Diabetes Metab Syndr Obes, 2012, 5: 247-282. DOI: 10.2147/DMSO.S32923.
14. Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses[J]. Nat Rev Immunol, 2009, 9(8): 581-593. DOI: 10.1038/nri2567.
15. Ratajczak J, Miekus K, Kucia M, et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery[J]. Leukemia, 2006, 20(5): 847-856. DOI: 10.1038/sj.leu.2404132.
16. Friedman A, Hao W. The role of exosomes in pancreatic cancer microenvironment[J]. Bull Math Biol, 2018, 80(5): 1111-1133. DOI: 10.1007/s11538-017-0254-9.
17. Cantaluppi V, Gatti S, Medica D, et al. Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells[J]. Kidney Int, 2012, 82(4): 412-427. DOI: 10.1038/ki.2012.105.
18. Vallhov H, Gutzeit C, Hultenby K, et al. Dendritic cell-derived exosomes carry the major cat allergen Fel d 1 and induce an allergic immune response[J]. Allergy, 2015, 70(12): 1651-1655. DOI: 10.1111/all.12701.
19. Balaj L, Lessard R, Dai L, et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences[J/OL]. Nat Commun, 2011, 2: 180[2011-02-01]. https://www.nature.com/articles/ncomms1180. DOI: 10.1038/ncomms1180.
20. Lai RC, Arslan F, Lee MM, et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury[J]. Stem Cell Res, 2010, 4(3): 214-222. DOI: 10.1016/j.scr.2009.12.003.
21. Arslan F, Lai RC, Smeets MB, et al. Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury[J]. Stem Cell Res, 2013, 10(3): 301-312. DOI: 10.1016/j.scr.2013.01.002.
22. Xin H, Li Y, Buller B, et al. Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth[J]. Stem Cells, 2012(7): 1556-1564. DOI: 10.1002/stem.1129.
23. Xin H, Li Y, Liu Z, et al. MiR-133b promotes neural plasticity and functional recovery after treatment of stroke with multipotent mesenchymal stromal cells in rats via transfer of exosome-enriched extracellular particles[J]. Stem Cells, 2013, 31(12): 2737-2746. DOI: 10.1002/stem.1409.
24. Zhang B, Yin Y, Lai RC, et al. Mesenchymal stem cells secrete immunologically active exosomes[J]. Stem Cells Dev, 2014, 23(11): 1233-1244. DOI: 10.1089/scd.2013.0479.
25. Conforti A, Scarsella M, Starc N, et al. Microvescicles derived from mesenchymal stromal cells are not as effective as their cellular counterpart in the ability to modulate immune responses in vitro[J]. Stem Cells Dev, 2014, 23(21): 2591-2599. DOI: 10.1089/scd.2014.0091.
26. Kordelas L, Rebmann V, Ludwig AK, et al. MSC-derived exosomes: a novel tool to treat therapy-refractory graft-versus-host disease[J]. Leukemia, 2014, 28(4): 970-973. DOI: 10.1038/leu.2014.41.
27. Du W, Zhang K, Zhang S, et al. Enhanced proangiogenic potential of mesenchymal stem cell-derived exosomes stimulated by a nitric oxide releasing polymer[J]. Biomaterials, 2017, 133: 70-81. DOI: 10.1016/j.biomaterials.2017.04.030.
28. Yu B, Shao H, Su C, et al. Exosomes derived from MSCs ameliorate retinal laser injury partially by inhibition of MCP-1[J/OL]. Sci Rep, 2016, 6: 34562[2016-09-30]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5043341/. DOI: 10.1038/srep34562.
29. Bai L, Shao H, Wang H, et al. Effects of mesenchymal stem cell-derived exosomes on experimental autoimmune uveitis[J/OL]. Sci Rep, 2017, 7(1): 4323[2017-06-28]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5489510/. DOI: 10.1038/s41598-017-04559-y.
30. Mead B, Tomarev S. Bone marrow-derived mesenchymal stem cells-derived exosomes promote survival of retinal ganglion cells through miRNA-dependent mechanisms[J]. Stem Cells Transl Med, 2017, 6(4): 1273-1285. DOI: 10.1002/sctm.16-0428.
31. Eggenhofer E, Benseler V, Kroemer A, et al. Mesenchymal stem cells are short-lived and do not migrate beyond the lungs after intravenous infusion[J/OL]. Front Immunol, 2012, 3: 297[2012-09-26]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3458305/. DOI: 10.3389/fimmu.2012.00297.
32. Kuriyan AE, Albini TA, Townsend JH, et al. Vision loss after intravitreal injection of autologous "stem cells" for AMD[J]. N Engl J Med, 2017, 376(11): 1047-1053. DOI: 10.1056/NEJMoa1609583.
33. Xitong D, Xiaorong Z. Targeted therapeutic delivery using engineered exosomes and its applications in cardiovascular diseases[J]. Gene, 2016, 575(2 Pt 2): 377-384. DOI: 10.1016/j.gene.2015.08.067.
34. Peinado H, Aleckovic M, Lavotshkin S, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET[J]. Nat Med, 2012, 18(6): 883-891. DOI: 10.1038/nm.2753.
35. Tian Y, Li S, Song J, et al. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy[J]. Biomaterials, 2014, 35(7): 2383-2390. DOI: 10.1016/j.biomaterials.2013.11.083.
36. Wen D, Peng Y, Liu D, et al. Mesenchymal stem cell and derived exosome as small RNA carrier and Immunomodulator to improve islet transplantation[J]. J Control Release, 2016, 238: 166-175. DOI: 10.1016/j.jconrel.2016.07.044.
37. Beauvillain C, Juste MO, Dion S, et al. Exosomes are an effective vaccine against congenital toxoplasmosis in mice[J]. Vaccine, 2009, 27(11): 1750-1757. DOI: 10.1016/j.vaccine.2009.01.022.
38. Haney MJ, Klyachko NL, Zhao Y, et al. Exosomes as drug delivery vehicles for Parkinson's disease therapy[J]. J Control Release, 2015, 207: 18-30. DOI: 10.1016/j.jconrel.2015.03.033.
39. Yang Y, Hong Y, Nam GH, et al. Virus-mimetic fusogenic exosomes for direct delivery of integral membrane proteins to target cell membranes[J]. Adv Mater, 2017, 29(13)[2017-02-06]. https://onlinelibrary.wiley.com/doi/abs/10.1002/adma.201605604. DOI: 10.1002/adma.201605604.
40. Sun D, Zhuang X, Xiang X, et al. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes[J]. Mol Ther, 2010, 18(9): 1606-1614. DOI: 10.1038/mt.2010.105.
41. Alvarez-Erviti L, Seow Y, Yin H, et al. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes[J]. Nat Biotechnol, 2011, 29(4): 341-345. DOI: 10.1038/nbt.1807.
42. Johnsen KB, Gudbergsson JM, Skov MN, et al. Evaluation of electroporation-induced adverse effects on adipose-derived stem cell exosomes[J]. Cytotechnology, 2016, 68(5): 2125-2138. DOI: 10.1007/s10616-016-9952-7.
43. Kim MS, Haney MJ, Zhao Y, et al. Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells[J]. Nanomedicine, 2016, 12(3): 655-664. DOI: 10.1016/j.nano.2015.10.012.
44. Mizrak A, Bolukbasi MF, Ozdener GB, et al. Genetically engineered microvesicles carrying suicide mRNA/protein inhibit schwannoma tumor growth[J]. Mol Ther, 2013, 21(1): 101-108. DOI: 10.1038/mt.2012.161.
45. Wang B, Yao K, Huuskes BM, et al. Mesenchymal stem cells deliver exogenous microRNA-let7c via exosomes to attenuate renal fibrosis[J]. Mol Ther, 2016, 24(7): 1290-1301. DOI: 10.1038/mt.2016.90.
46. Lou G, Song X, Yang F, et al. Exosomes derived from miR-122-modified adipose tissue-derived MSCs increase chemosensitivity of hepatocellular carcinoma[J/OL]. J Hematol Oncol, 2015, 8: 122[2015-10-29]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4627430/. DOI: 10.1186/s13045-015-0220-7.
47. Willms E, Johansson HJ, Mager I, et al. Cells release subpopulations of exosomes with distinct molecular and biological properties[J/OL]. Sci Rep, 2016, 6: 22519[2016-03-02]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4773763/. DOI: 10.1038/srep22519.
48. Lotvall J, Hill AF, Hochberg F, et al. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles[J]. J Extracell Vesicles, 2014, 3: 26913[2014-12-22]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4275645/. DOI: 10.3402/jev.v3.26913.

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