Menstrual blood-derived mesenchymal stem cells differentiate into functional hepatocyte-like cells

Journal of Zhejiang University: Science B

Volumn 14, Issue 11, 2013, Pages 961-972

  Mou, Xiao Zhou ^a,b   Lin, Jian ^a,c   Chen, Jin Yang ^b,d   Li, Yi Fei ^a   Wu, Xiao Xing ^a   Xiang, Bing Yu ^a   Li, Cai Yun ^e   Ma, Ju Ming ^e   Xiang, Charlie ^a,b  

^a ZHEJIANG UNIVERSITY   (China)

^b Institute for Cell Based Drug Development of Zhejiang Province   (China)

^c People's Hospital of Tongling   (China)

^d S Evans Biosciences ^*  (China)

^e The 117th Hospital of Chinese PLA   (China)

Author keywords

Differentiation; Hepatocyte; Intrasplenic transplantation; Menstrual blood derived mesenchymal stem cell (MenSC); Partial hepatectomy

Indexed keywords

ALBUMIN; ALPHA FETOPROTEIN; AMINOTRANSFERASE; CYTOCHROME P450 1A; CYTOKERATIN 18; CYTOKERATIN 19; FIBROBLAST GROWTH FACTOR 4; INDOCYANINE GREEN; ONCOSTATIN M; SCATTER FACTOR; UREA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL THERAPY; CELL TRANSPLANTATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CELL; LIVER FUNCTION; LIVER INJURY; MALE; MENSTRUATION; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; STORAGE; TISSUE ENGINEERING; UREA CYCLE;

ANIMALS; CELL DIFFERENTIATION; CELL SEPARATION; END STAGE LIVER DISEASE; HEPATOCYTES; HUMANS; MALE; MENSTRUATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED BALB C;

EID: 84888866176     PISSN: 16731581     EISSN: 18621783     Source Type: Journal    
DOI: 10.1631/jzus.B1300081     Document Type: Article

References (42)

1. Allickson, J., Xiang, C., 2012. Human adult stem cells from menstrual blood and endometrial tissue. J. Zhejiang Univ.-Sci. B (Biomed. & Biotechnol.), 13(5):419-420. [doi:10.1631/jzus.B1200062]
2. Allickson, J.G., Sanchez, A., Yefimenko, N., Borlongan, C.V., Sanberg, P.R., 2011. Recent studies assessing the proliferative capability of a novel adult stem cell identified in menstrual blood. Open Stem Cell J., 3(2011):4-10. [doi:10.2174/1876893801103010004]
3. Banas, A., Teratani, T., Yamamoto, Y., Tokuhara, M., Takeshita, F., Quinn, G., Okochi H., Ochiya, T., 2007. Adipose tissue-derived mesenchymal stem cells as a source of human hepatocytes. Hepatology, 46(1):219-228. [doi:10.1002/hep.21704]
4. Bieback, K., Kern, S., Kluter, H., Eichler, H., 2004. Critical parameters for the isolation of mesenchymal stem cells from umbilical cord blood. Stem Cells, 22(4):625-634. [doi:10.1634/stemcells.22-4-625]
5. Borlongan, C., Kaneko, V.Y., Maki, M., Yu, S.J., Ali, M., Allickson, J.G., Sanberg, C.D., Kuzmin-Nichols, N., Sanberg, P.R., 2010. Menstrual blood cells display stem cell-like phenotypic markers and exert neuroprotection following transplantation in experimental stroke. Stem Cells Dev., 19(4):439-452. [doi:10.1089/scd.2009.0340]
6. Chen, Y., Dong, X.J., Zhang, G.R., Shao J.Z., Xiang, L.X., 2007. In vitro differentiation of mouse bone marrow stromal stem cells into hepatocytes induced by conditioned culture medium of hepatocytes. J. Cell Biochem., 102(1):52-63. [doi:10.1002/jcb.21275]
7. Chen, Y.F., Tseng, C.Y., Wang, H.W., Kuo, H.C., Yang, V.W., Lee, O.K., 2012. Rapid generation of mature hepatocyte-like cells from human induced pluripotent stem cells by an efficient three-step protocol. Hepatology, 55(4): 1193-1203. [doi:10.1002/hep.24790]
8. Chien, C.C., Yen, B.L., Lee, F.K., Lai, T.H., Chen, Y.C., Chan, S.H., Huang, H.I., 2006. In vitro differentiation of human placenta-derived multipotent cells into hepatocyte-like cells. Stem Cells, 24(7):1759-1768. [doi:10.1634/stem cells.2005-0521]
9. Cui, C.H., Uyama, T., Miyado, K., Terai, M., Kyo, S., Kiyono, T., Umezawa, A., 2007. Menstrual blood-derived cells confer human dystrophin expression in the murine model of Duchenne muscular dystrophy via cell fusion and myogenic transdifferentiation. Mol. Biol. Cell, 18(5): 1586-1594. [doi:10.1091/mbc.E06-09-0872]
10. de Coppi, P., Bartsch, G.Jr., Siddiqui, M.M., Xu, T., Santos, C.C., Perin, L., Mostoslavsky, G., Serre, A.C., Snyder, E.Y., Yoo, J.J., et al., 2007. Isolation of amniotic stem cell lines with potential for therapy. Nat. Biotechnol., 25(1):100-106. [doi:10.1038/nbt1274]
11. Dhawan, A., Mitry, R.R., Hughes, R.D., Lehec, S., Terry, C., Bansal, S., Arya, R., Wade, J.J., Verma, A., Heaton, N.D., et al., 2004. Hepatocyte transplantation for inherited factor VII deficiency. Transplantation, 78(12):1812-1814. [doi:10.1097/01.TP.0000146386.77076.47]
12. Fox, I.J., Chowdhury, J.R., 2004. Hepatocyte transplantation. J. Hepatol., 40(6):878-886. [doi:10.1016/j.jhep.2004.04.009]
13. Fox, I.J., Chowdhury, J.R., Kaufman, S.S., Goertzen, T.C., Chowdhury, N.R., Warkentin, P.I., Dorko, K., Sauter, B.V., Strom, S.C., 1998. Treatment of the Crigler-Najjar syndrome type I with hepatocyte transplantation. N. Engl. J. Med., 338(20):1422-1426. [doi:10.1056/NEJM199805 143382004]
14. Gunsalus, J.R., Brady, D.A., Coulter, S.M., Gray, B.M., Edge, A.S., 1997. Reduction of serum cholesterol in Watanabe rabbits by xenogeneic hepatocellular transplantation. Nat. Med., 3(1):48-53. [doi:10.1038/nm0197-48]
15. Hida, N., Nishiyama, N., Miyoshi, S., Kira, S., Segawa, K., Uyama, T., Mori, T., Miyado, K., Ikegami, Y., Cui, C., et al., 2008. Novel cardiac precursor-like cells from human menstrual blood-derived mesenchymal cells. Stem Cells, 26(7):1695-1704. [doi:10.1634/stemcells.2007-0826]
16. Huang, P., He, Z., Ji, S., Sun, H., Xiang, D., Liu, C., Hu, Y., Wang, X., Hui, L., 2011. Induction of functional hepatocyte-like cells from mouse fibroblasts by defined factors. Nature, 475(7356):386-389. [doi:10.1038/nature 10116]
17. Ikegami, Y., Miyoshi, S., Nishiyama, N., Hida, N., Okamoto, K., Miyado, K., Segawa, K., Ogawa, S., Umezawa, A., 2010. Serum-independent cardiomyogenic transdifferentiation in human endometrium-derived mesenchymal cells. Artif. Organs, 34(4):280-288. [doi:10.1111/j.1525-1594.2009.00859.x]
18. Lee, K.D., Kuo, T.K., Whang-Peng, J., Chung, Y.F., Lin, C.T., Chou, S.H., Chen, J.R., Chen, Y.P., Lee, O.K., 2004. In vitro hepatic differentiation of human mesenchymal stem cells. Hepatology, 40(6):1275-1284. [doi:10.1002/hep. 20469]
19. Li, H.Y., Chen, Y.J., Chen, S.J., Kao, C.L., Tseng, L.M., Lo, W.L., Chang, C.M., Yang, D.M., Ku, H.H., Twu, N.F., et al., 2010. Induction of insulin-producing cells derived from endometrial mesenchymal stem-like cells. J. Pharmacol. Exp. Ther., 335(3):817-829. [doi:10.1124/jpet.110.169284]
20. Li, J., Tao, R., Wu, W., Cao, H., Xin, J., Guo, J., Jiang, L., Hong, X., Demetriou, A.A., Farkas, D., et al., 2010. Transcriptional profiling and hepatogenic potential of acute hepatic failure-derived bone marrow mesenchymal stem cells. Differentiation, 80(2-3):166-174. [doi:10.1016/j.diff.2010.04.002]
21. Lin, J., Xiang, D., Zhang, J.L., Allickson, J., Xiang, C., 2011. Plasticity of human menstrual blood stem cells derived from the endometrium. J. Zhejiang Univ.-Sci. B (Biomed. & Biotechnol.), 12(5):372-380. [doi:10.1631/jzus. B1100015]
22. Meng, X., Ichim, T.E., Zhong, J., Rogers, A., Yin, Z., Jackson, J., Wang, H., Ge, W., Bogin, V., Chan, K.W., et al., 2007. Endometrial regenerative cells: a novel stem cell population. J. Transl. Med., 5:57. [doi:10.1186/1479- 5876-5-57]
23. Mitchell, C., Willenbring, H., 2008. A reproducible and well-tolerated method for 2/3 partial hepatectomy in mice. Nat. Protoc., 3(7):1167-1170. [doi:10.1038/nprot.2008.80]
24. Muraca, M., Gerunda, G., Neri, D., Vilei, M.T., Granato, A., Feltracco, P., Meroni, M., Giron, G., Burlina, A.B., 2002. Hepatocyte transplantation as a treatment for glycogen storage disease type 1a. Lancet, 359(9303):317-318. [doi:10.1016/S0140-6736(02)07529-3]
25. Murphy, M.P., Wang, H., Patel, A.N., Kambhampati, S., Angle, N., Chan, K., Marleau, A.M., Pyszniak, A., Carrier, E., Ichim, T.E., et al., 2008. Allogeneic endometrial regenerative cells: an "off the shelf solution" for critical limb ischemia? J. Transl. Med., 6(1):45. [doi:10.1186/1479-5876-6- 45]
26. Overturf, K., Al-Dhalimy, M., Tanguay, R., Brantly, M., Ou, C.N., Finegold, M., Grompe, M., 1996. Hepatocytes corrected by gene therapy are selected in vivo in a murine model of hereditary tyrosinaemia type I. Nat. Genet., 12(3):266-273. [doi:10.1038/ng0396-266]
27. Park, S.M., Vo, K., Lallier, M., Cloutier, A.S., Brochu, P., Alvarez, F., Martin, S.R., 2006. Hepatocyte transplantation in the Long Evans Cinnamon rat model of Wilson's disease. Cell Transplant., 15(1):13-22. [doi:10.3727/ 000000006783982188]
28. Patel, A.N., Silva, F., 2008. Menstrual blood stromal cells: the potential for regenerative medicine. Regen. Med., 3(4): 443-444. [doi:10.2217/17460751.3.4.443]
29. Patel, A.N., Park, E., Kuzman, M., Benetti, F., Silva, F.J., Allickson, J.G., 2008. Multipotent menstrual blood stromal stem cells: isolation, characterization, and differentiation. Cell Transplant., 17(3):303-311. [doi:10.3727/096368908784153922]
30. Peleman, R.R., Gavaler, J.S., van Thiel, D.H., Esquivel, C., Gordon, R., Iwatsuki, S., Starzl, T.E., 1987. Orthotopic liver transplantation for acute and subacute hepatic failure in adults. Hepatology, 7(3):484-489. [doi:10.1002/hep. 1840070312]
31. Phuc, P.V., Lam, D.H., Ngoc, V.B., Thu, D.T., Nguyet, N.T., Ngoc, P.K., 2011. Production of functional dendritic cells from menstrual blood - a new dendritic cell source for immune therapy. In Vitro Cell Dev. Biol. Anim., 47(5-6): 368-375. [doi:10.1007/s11626-011-9399-2]
32. Pittenger, M.F., Mackay, A.M., Beck, S.C., Jaiswal, R.K., Douglas, R., Mosca, J.D., Moorman, M.A., Simonetti, D.W., Craig, S., Marshak, D.R., 1999. Multilineage potential of adult human mesenchymal stem cells. Science, 284(5411):143-147. [doi:10.1126/science.284.5411.143]
33. Sanberg, P.R., Eve, D.J., Willing, A.E., Garbuzova-Davis, S., Tan, J., Sanberg, C.D., Allickson, J.G., Cruz, L.E., Borlongan, C.V., 2011. The treatment of neurodegenerative disorders using umbilical cord blood and menstrual blood-derived stem cells. Cell Transplant., 20(1):85-94. [doi:10.3727/ 096368910X532855]
34. Santamaria, X., Massasa, E.E., Feng, Y., Wolff, E., Taylor, H.S., 2011. Derivation of insulin producing cells from human endometrial stromal stem cells and use in the treatment of murine diabetes. Mol. Ther., 19(11): 2065-2071. [doi:10.1038/mt.2011.173]
35. Schwab, K.E., Gargett, C.E., 2007. Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium. Hum. Reprod., 22(11): 2903-2911. [doi:10.1093/humrep/dem265]
36. Schwartz, R.E., Reyes, M., Koodie, L., Jiang, Y., Blackstad, M., Lund, T., Lenvik, T., Johnson, S., Hu, W.S., Verfaillie, C.M., 2002. Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. J. Clin. Invest., 109(10):1291-1302. [doi:10.1172/JCI15182]
37. Seo, M.J., Suh, S.Y., Bae, Y.C., Jung, J.S., 2005. Differentiation of human adipose stromal cells into hepatic lineage in vitro and in vivo. Biochem. Biophys. Res. Commun., 328(1):258-264. [doi:10.1016/j.bbrc.2004.12.158]
38. Snykers, S., Vanhaecke, T., Papeleu, P., Luttun, A., Jiang, Y., van der Heyden, Y., Verfaillie, C., Rogiers, V., 2006. Sequential exposure to cytokines reflecting embryogenesis: the key for in vitro differentiation of adult bone marrow stem cells into functional hepatocyte-like cells. Toxicol. Sci., 94(2):330-341. [doi:10.1093/toxsci/kfl058]
39. Stephenne, X., Najimi, M., Sibille, C., Nassogne, M.C., Smets, F., Sokal, E.M., 2006. Sustained engraftment and tissue enzyme activity after liver cell transplantation for argininosuccinate lyase deficiency. Gastroenterology, 130(4): 1317-1323. [doi:10.1053/j.gastro.2006.01.008]
40. Toyoda, M., Cui, C., Umezawa, A., 2007. Myogenic transdifferentiation of menstrual blood-derived cells. Acta Myol., 26(3):176-178.
41. Yamamoto, H., Quinn, G., Asari, A., Yamanokuchi, H., Teratani, T., Terada, M., Ochiya, T., 2003. Differentiation of embryonic stem cells into hepatocytes: biological functions and therapeutic application. Hepatology, 37(5): 983-993. [doi:10.1053/jhep.2003.50202]
42. Yu, J., Yang, J., Pan, Q., Ma, J., Li, J., Li, Y., Cao, H., Wang, Y., Li, L., 2012. In vivo hepatic differentiation of mesenchymal stem cells from human umbilical cord blood after transplantation into mice with liver injury. Biochem. Biophys. Res. Commun., 422(4):539-545. [doi:10.1016/j.bbrc.2012.04.156]