Hepatoprotective effect of exosomes from human-induced pluripotent stem cell–derived mesenchymal stromal cells against hepatic ischemia-reperfusion injury in rats

Cytotherapy

Volumn 18, Issue 12, 2016, Pages 1548-1559

  Nong, Kate ^a   Wang, Weiwei ^b   Niu, Xin ^a   Hu, Bin ^a   Ma, Chenchao ^a   Bai, Yueqing ^a   Wu, Bo ^a   Wang, Yang ^a   Ai, Kaixing ^a,c  

^a SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

^b MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

^c TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

apoptosis; exosomes; hepatic ischemia reperfusion injury; induced pluripotent stem cells; mesenchymal stromal cells

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CASPASE 3; GLUTATHIONE; GLUTATHIONE PEROXIDASE; INTERLEUKIN 6; MYELOPEROXIDASE; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR; HBP1 PROTEIN, RAT; HIGH MOBILITY GROUP B1 PROTEIN;

ADIPOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DEVELOPMENT; CONTROLLED STUDY; EXOSOME; INDUCED PLURIPOTENT STEM CELL; INFERIOR CAVA VEIN; INFLAMMATORY CELL; LIVER CELL; LIVER ISCHEMIA; LIVER PROTECTION; MALE; MESENCHYMAL STROMA CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REPERFUSION INJURY; ULTRACENTRIFUGATION; ANIMAL; APOPTOSIS; BIOLOGICAL THERAPY; BLOOD; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; INFLAMMATION; LIVER; METABOLISM; NECROSIS; PATHOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT; TUNEL ASSAY;

ALANINE TRANSAMINASE; ANIMALS; APOPTOSIS; ASPARTATE AMINOTRANSFERASES; CASPASE 3; CELL- AND TISSUE-BASED THERAPY; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXOSOMES; HMGB1 PROTEIN; HUMANS; IN SITU NICK-END LABELING; INDUCED PLURIPOTENT STEM CELLS; INFLAMMATION; INTERLEUKIN-6; LIVER; MALE; MESENCHYMAL STROMAL CELLS; NECROSIS; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84994034026     PISSN: 14653249     EISSN: 14772566     Source Type: Journal    
DOI: 10.1016/j.jcyt.2016.08.002     Document Type: Article

References (43)

1. [1] Ke, B., Lipshutz, G.S., Kupiec-Weglinski, J.W., Gene therapy in liver ischemia and reperfusion injury. Curr Pharm Des 12 (2006), 2969–2975.
2. [2] Fondevila, C., Busuttil, R.W., Kupiec-Weglinski, J.W., Hepatic ischemia/reperfusion injury–a fresh look. Exp Mol Pathol 74 (2003), 86–93.
3. [3] Caplan, A.I., Dennis, J.E., Mesenchymal stem cells as trophic mediators. J Cell Biochem 98 (2006), 1076–1084.
4. [4] Li, S.C., Acevedo, J., Wang, L., Jiang, H., Luo, J., Pestell, R.G., et al. Mechanisms for progenitor cell-mediated repair for ischemic heart injury. Curr Stem Cell Res Ther 7 (2012), 2–14.
5. [5] Wise, A.F., Ricardo, S.D., Mesenchymal stem cells in kidney inflammation and repair. Nephrology (Carlton) 17 (2012), 1–10.
6. [6] Sun, C.K., Chang, C.L., Lin, Y.C., Kao, Y.H., Chang, L.T., Yen, C.H., et al. Systemic administration of autologous adipose-derived mesenchymal stem cells alleviates hepatic ischemia-reperfusion injury in rats. Crit Care Med 40 (2012), 1279–1290.
7. [7] Seki, T., Yokoyama, Y., Nagasaki, H., Kokuryo, T., Nagino, M., Adipose tissue-derived mesenchymal stem cell transplantation promotes hepatic regeneration after hepatic ischemia-reperfusion and subsequent hepatectomy in rats. J Surg Res 178 (2012), 63–70.
8. [8] Jin, G., Qiu, G., Wu, D., Hu, Y., Qiao, P., Fan, C., et al. Allogeneic bone marrow-derived mesenchymal stem cells attenuate hepatic ischemia-reperfusion injury by suppressing oxidative stress and inhibiting apoptosis in rats. Int J Mol Med 31 (2013), 1395–1401.
9. [9] Camussi, G., Deregibus, M.C., Cantaluppi, V., Role of stem-cell-derived microvesicles in the paracrine action of stem cells. Biochem Soc Trans 41 (2013), 283–287.
10. [10] Stoorvogel, W., Kleijmeer, M.J., Geuze, H.J., Raposo, G., The biogenesis and functions of exosomes. Traffic 3 (2002), 321–330.
11. [11] Zhang, H.G., Grizzle, W.E., Exosomes: a novel pathway of local and distant intercellular communication that facilitates the growth and metastasis of neoplastic lesions. Am J Pathol 184 (2014), 28–41.
12. [12] Schorey, J.S., Bhatnagar, S., Exosome function: from tumor immunology to pathogen biology. Traffic 9 (2008), 871–881.
13. [13] Liang, X., Ding, Y., Zhang, Y., Tse, H.F., Lian, Q., Paracrine mechanisms of mesenchymal stem cell-based therapy: current status and perspectives. Cell Transplant 23 (2014), 1045–1059.
14. [14] Lai, R.C., Arslan, F., Lee, M.M., Sze, N.S., Choo, A., Chen, T.S., et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res 4 (2010), 214–222.
15. [15] Gatti, S., Bruno, S., Deregibus, M.C., Sordi, A., Cantaluppi, V., Tetta, C., et al. Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury. Nephrol Dial Transplant 26 (2011), 1474–1483.
16. [16] Moslem, M., Valojerdi, M.R., Pournasr, B., Muhammadnejad, A., Baharvand, H., Therapeutic potential of human induced pluripotent stem cell-derived mesenchymal stem cells in mice with lethal fulminant hepatic failure. Cell Transplant 22 (2013), 1785–1799.
17. [17] Zhang, J., Ho, J.C., Chan, Y.C., Lian, Q., Siu, C.W., Tse, H.F., Overexpression of myocardin induces partial transdifferentiation of human-induced pluripotent stem cell-derived mesenchymal stem cells into cardiomyocytes. Physiol Rep, 2, 2014.
18. [18] de Lazaro, I., Yilmazer, A., Kostarelos, K., Induced pluripotent stem (iPS) cells: a new source for cell-based therapeutics?. J Control Release 185C (2014), 37–44.
19. [19] Villa-Diaz, L.G., Brown, S.E., Liu, Y., Ross, A.M., Lahann, J., Parent, J.M., et al. Derivation of mesenchymal stem cells from human induced pluripotent stem cells cultured on synthetic substrates. Stem Cells 30 (2012), 1174–1181.
20. [20] Zhang, J., Guan, J., Niu, X., Hu, G., Guo, S., Li, Q., et al. Exosomes released from human induced pluripotent stem cells-derived MSCs facilitate cutaneous wound healing by promoting collagen synthesis and angiogenesis. J Transl Med, 13, 2015, 49.
21. [21] Hu, G.W., Li, Q., Niu, X., Hu, B., Liu, J., Zhou, S.M., et al. Exosomes secreted by human-induced pluripotent stem cell-derived mesenchymal stem cells attenuate limb ischemia by promoting angiogenesis in mice. Stem Cell Res Ther, 6, 2015, 10.
22. [22] Liao, J., Wu, Z., Wang, Y., Cheng, L., Cui, C., Gao, Y., et al. Enhanced efficiency of generating induced pluripotent stem (iPS) cells from human somatic cells by a combination of six transcription factors. Cell Res 18 (2008), 600–603.
23. [23] Rowland, T.J., Miller, L.M., Blaschke, A.J., Doss, E.L., Bonham, A.J., Hikita, S.T., et al. Roles of integrins in human induced pluripotent stem cell growth on Matrigel and vitronectin. Stem Cells Dev 19 (2010), 1231–1240.
24. [24] Zou, L., Luo, Y., Chen, M., Wang, G., Ding, M., Petersen, C.C., et al. A simple method for deriving functional MSCs and applied for osteogenesis in 3D scaffolds. Sci Rep, 3, 2013, 2243.
25. [25] Villarroya-Beltri, C., Gutierrez-Vazquez, C., Sanchez-Madrid, F., Mittelbrunn, M., Analysis of microRNA and protein transfer by exosomes during an immune synapse. Methods Mol Biol 1024 (2013), 41–51.
26. [26] Moon, K.H., Hood, B.L., Mukhopadhyay, P., Rajesh, M., Abdelmegeed, M.A., Kwon, Y.I., et al. Oxidative inactivation of key mitochondrial proteins leads to dysfunction and injury in hepatic ischemia reperfusion. Gastroenterology 135 (2008), 1344–1357.
27. [27] Suzuki, S., Nakamura, S., Koizumi, T., Sakaguchi, S., Baba, S., Muro, H., et al. The beneficial effect of a prostaglandin I2 analog on ischemic rat liver. Transplantation 52 (1991), 979–983.
28. [28] Yu, B., Zhang, X., Li, X., Exosomes derived from mesenchymal stem cells. Int J Mol Sci 15 (2014), 4142–4157.
29. [29] Tan, C.Y., Lai, R.C., Wong, W., Dan, Y.Y., Lim, S.K., Ho, H.K., Mesenchymal stem cell-derived exosomes promote hepatic regeneration in drug-induced liver injury models. Stem Cell Res Ther, 5, 2014, 76.
30. [30] Li, T., Yan, Y., Wang, B., Qian, H., Zhang, X., Shen, L., et al. Exosomes derived from human umbilical cord mesenchymal stem cells alleviate liver fibrosis. Stem Cells Dev 22 (2013), 845–854.
31. [31] Fu, J., Zhang, H., Zhuang, Y., Liu, H., Shi, Q., Li, D., et al. The role of N-acetyltransferase 8 in mesenchymal stem cell-based therapy for liver ischemia/reperfusion injury in rats. PLoS ONE, 9, 2014 e103355.
32. [32] Katsha, A.M., Ohkouchi, S., Xin, H., Kanehira, M., Sun, R., Nukiwa, T., et al. Paracrine factors of multipotent stromal cells ameliorate lung injury in an elastase-induced emphysema model. Mol Ther 19 (2011), 196–203.
33. [33] Lee, R.H., Pulin, A.A., Seo, M.J., Kota, D.J., Ylostalo, J., Larson, B.L., et al. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 5 (2009), 54–63.
34. [34] Yeo, R.W., Lai, R.C., Zhang, B., Tan, S.S., Yin, Y., Teh, B.J., et al. Mesenchymal stem cell: an efficient mass producer of exosomes for drug delivery. Adv Drug Deliv Rev 65 (2013), 336–341.
35. [35] Brack, A.S., Rando, T.A., Tissue-specific stem cells: lessons from the skeletal muscle satellite cell. Cell Stem Cell 10 (2012), 504–514.
36. [36] Wagner, W., Bork, S., Horn, P., Krunic, D., Walenda, T., Diehlmann, A., et al. Aging and replicative senescence have related effects on human stem and progenitor cells. PLoS ONE, 4, 2009 e5846.
37. [37] Lian, Q., Zhang, Y., Zhang, J., Zhang, H.K., Wu, X., Zhang, Y., et al. Functional mesenchymal stem cells derived from human induced pluripotent stem cells attenuate limb ischemia in mice. Circulation 121 (2010), 1113–1123.
38. [38] Zhang, Y., Liang, X., Liao, S., Wang, W., Wang, J., Li, X., et al. Potent paracrine effects of human induced pluripotent stem cell-derived mesenchymal stem cells attenuate doxorubicin-induced cardiomyopathy. Sci Rep, 5, 2015, 11235.
39. [39] Peralta, C., Jimenez-Castro, M.B., Gracia-Sancho, J., Hepatic ischemia and reperfusion injury: effects on the liver sinusoidal milieu. J Hepatol 59 (2013), 1094–1106.
40. [40] Tan, Z., Jiang, R., Wang, X., Wang, Y., Lu, L., Liu, Q., et al. RORgammat+IL-17+ neutrophils play a critical role in hepatic ischemia-reperfusion injury. J Mol Cell Biol 5 (2013), 143–146.
41. [41] Tang, D., Kang, R., Zeh, H.J. 3rd, Lotze, M.T., High-mobility group box 1, oxidative stress, and disease. Antioxid Redox Signal 14 (2011), 1315–1335.
42. [42] Shen, M., Lu, J., Dai, W., Wang, F., Xu, L., Chen, K., et al. Ethyl pyruvate ameliorates hepatic ischemia-reperfusion injury by inhibiting intrinsic pathway of apoptosis and autophagy. Mediators Inflamm, 2013, 2013, 461536.
43. [43] Fausto, N., Campbell, J.S., Riehle, K.J., Liver regeneration. Hepatology 43 (2006), S45–53.