DOI QR코드

DOI QR Code

Mesenchymal stem cell therapy for liver fibrosis

  • Eom, Young Woo (Cell Therapy and Tissue Engineering Center) ;
  • Shim, Kwang Yong (Department of Internal Medicine, Yonsei University Wonju College of Medicine) ;
  • Baik, Soon Koo (Cell Therapy and Tissue Engineering Center)
  • 투고 : 2014.11.26
  • 심사 : 2014.12.19
  • 발행 : 2015.09.01

초록

Currently, the most effective treatment for end-stage liver fibrosis is liver transplantation; however, transplantation is limited by a shortage of donor organs, surgical complications, immunological rejection, and high medical costs. Recently, mesenchymal stem cell (MSC) therapy has been suggested as an effective alternate approach for the treatment of hepatic diseases. MSCs have the potential to differentiate into hepatocytes, and therapeutic value exists in their immune-modulatory properties and secretion of trophic factors, such as growth factors and cytokines. In addition, MSCs can suppress inflammatory responses, reduce hepatocyte apoptosis, increase hepatocyte regeneration, regress liver fibrosis and enhance liver functionality. Despite these advantages, issues remain; MSCs also have fibrogenic potential and the capacity to promote tumor cell growth and oncogenicity. This paper summarizes the properties of MSCs for regenerative medicine and their therapeutic mechanisms and clinical application in the treatment of liver fibrosis. We also present several outstanding risks, including their fibrogenic potential and their capacity to promote pre-existing tumor cell growth and oncogenicity.

키워드

과제정보

연구 과제 주관 기관 : Yonsei University

참고문헌

  1. Kung JW, Forbes SJ. Stem cells and liver repair. Curr Opin Biotechnol 2009;20:568-574. https://doi.org/10.1016/j.copbio.2009.09.004
  2. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest 2005;115:209-218. https://doi.org/10.1172/JCI24282
  3. Kisseleva T, Brenner DA. Mechanisms of fibrogenesis. Exp Biol Med (Maywood) 2008;233:109-122. https://doi.org/10.3181/0707-MR-190
  4. Snowdon VK, Fallowfield JA. Models and mechanisms of fibrosis resolution. Alcohol Clin Exp Res 2011;35:794-799. https://doi.org/10.1111/j.1530-0277.2010.01400.x
  5. Ghatak S, Biswas A, Dhali GK, Chowdhury A, Boyer JL, Santra A. Oxidative stress and hepatic stellate cell activation are key events in arsenic induced liver fibrosis in mice. Toxicol Appl Pharmacol 2011;251:59-69. https://doi.org/10.1016/j.taap.2010.11.016
  6. Domitrovic R, Jakovac H. Effects of standardized bilberry fruit extract ($Mirtoselect^{(R)}$) on resolution of CCl4-induced liver fibrosis in mice. Food Chem Toxicol 2011;49:848-854. https://doi.org/10.1016/j.fct.2010.12.006
  7. Malhi H, Gores GJ. Cellular and molecular mechanisms of liver injury. Gastroenterology 2008;134:1641-1654. https://doi.org/10.1053/j.gastro.2008.03.002
  8. Hong WK, Kim MY, Baik SK, et al. The usefulness of non-invasive liver stiffness measurements in predicting clinically significant portal hypertension in cirrhotic patients: Korean data. Clin Mol Hepatol 2013;19:370-375. https://doi.org/10.3350/cmh.2013.19.4.370
  9. Moon KM, Kim G, Baik SK, et al. Ultrasonographic scoring system score versus liver stiffness measurement in prediction of cirrhosis. Clin Mol Hepatol 2013;19:389-398. https://doi.org/10.3350/cmh.2013.19.4.389
  10. Lichtinghagen R, Michels D, Haberkorn CI, et al. Matrix metalloproteinase (MMP)-2, MMP-7, and tissue inhibitor of metalloproteinase-1 are closely related to the fibroproliferative process in the liver during chronic hepatitis C. J Hepatol 2001;34:239-247. https://doi.org/10.1016/S0168-8278(00)00037-4
  11. Fallowfield JA, Iredale JP. Targeted treatments for cirrhosis. Expert Opin Ther Targets 2004;8:423-435. https://doi.org/10.1517/14728222.8.5.423
  12. Zhang Z, Wang FS. Stem cell therapies for liver failure and cirrhosis. J Hepatol 2013;59:183-185. https://doi.org/10.1016/j.jhep.2013.01.018
  13. Alison MR, Poulsom R, Jeffery R, et al. Hepatocytes from non-hepatic adult stem cells. Nature 2000;406:257. https://doi.org/10.1038/35018642
  14. Theise ND, Nimmakayalu M, Gardner R, et al. Liver from bone marrow in humans. Hepatology 2000;32:11-16.
  15. Si-Tayeb K, Noto FK, Nagaoka M, et al. Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 2010;51:297-305. https://doi.org/10.1002/hep.23354
  16. Kia R, Sison RL, Heslop J, et al. Stem cell-derived hepatocytes as a predictive model for drug-induced liver injury: are we there yet? Br J Clin Pharmacol 2013;75:885-896. https://doi.org/10.1111/j.1365-2125.2012.04360.x
  17. Shu SN, Wei L, Wang JH, Zhan YT, Chen HS, Wang Y. Hepatic differentiation capability of rat bone marrow-derived mesenchymal stem cells and hematopoietic stem cells. World J Gastroenterol 2004;10:2818-2822. https://doi.org/10.3748/wjg.v10.i19.2818
  18. Gebler A, Zabel O, Seliger B. The immunomodulatory capacity of mesenchymal stem cells. Trends Mol Med 2012;18:128-134. https://doi.org/10.1016/j.molmed.2011.10.004
  19. Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 2007;25:2739-2749. https://doi.org/10.1634/stemcells.2007-0197
  20. Sundin M, Ringden O, Sundberg B, Nava S, Gotherstrom C, Le Blanc K. No alloantibodies against mesenchymal stromal cells, but presence of anti-fetal calf serum antibodies, after transplantation in allogeneic hematopoietic stem cell recipients. Haematologica 2007;92:1208-1215. https://doi.org/10.3324/haematol.11446
  21. Corcione A, Benvenuto F, Ferretti E, et al. Human mesenchymal stem cells modulate B-cell functions. Blood 2006;107:367-372. https://doi.org/10.1182/blood-2005-07-2657
  22. Asari S, Itakura S, Ferreri K, et al. Mesenchymal stem cells suppress B-cell terminal differentiation. Exp Hematol 2009;37:604-615. https://doi.org/10.1016/j.exphem.2009.01.005
  23. Zhang W, Ge W, Li C, et al. Effects of mesenchymal stem cells on differentiation, maturation, and function of human monocyte-derived dendritic cells. Stem Cells Dev 2004;13:263-271. https://doi.org/10.1089/154732804323099190
  24. Zhang B, Liu R, Shi D, et al. Mesenchymal stem cells induce mature dendritic cells into a novel Jagged-2-dependent regulatory dendritic cell population. Blood 2009;113:46-57. https://doi.org/10.1182/blood-2008-04-154138
  25. Spaggiari GM, Capobianco A, Becchetti S, Mingari MC, Moretta L. Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation. Blood 2006;107:1484-1490. https://doi.org/10.1182/blood-2005-07-2775
  26. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105:1815-1822. https://doi.org/10.1182/blood-2004-04-1559
  27. English K, Ryan JM, Tobin L, Murphy MJ, Barry FP, Mahon BP. Cell contact, prostaglandin E(2) and transforming growth factor beta 1 play non-redundant roles in human mesenchymal stem cell induction of CD4+CD25(High) forkhead box P3+ regulatory T cells. Clin Exp Immunol 2009;156:149-160. https://doi.org/10.1111/j.1365-2249.2009.03874.x
  28. Quintanilha LF, Takami T, Hirose Y, et al. Canine mesenchymal stem cells show antioxidant properties against thioacetamide-induced liver injury in vitro and in vivo. Hepatol Res 2014;44:E206-E217. https://doi.org/10.1111/hepr.12204
  29. Cho KA, Woo SY, Seoh JY, Han HS, Ryu KH. Mesenchymal stem cells restore CCl4-induced liver injury by an antioxidative process. Cell Biol Int 2012;36:1267-1274. https://doi.org/10.1042/CBI20110634
  30. Schwartz RE, Reyes M, Koodie L, et al. Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. J Clin Invest 2002;109:1291-1302. https://doi.org/10.1172/JCI0215182
  31. Lange C, Bassler P, Lioznov MV, et al. Liver-specific gene expression in mesenchymal stem cells is induced by liver cells. World J Gastroenterol 2005;11:4497-4504. https://doi.org/10.3748/wjg.v11.i29.4497
  32. Ong SY, Dai H, Leong KW. Inducing hepatic differentiation of human mesenchymal stem cells in pellet culture. Biomaterials 2006;27:4087-4097. https://doi.org/10.1016/j.biomaterials.2006.03.022
  33. Sato Y, Araki H, Kato J, et al. Human mesenchymal stem cells xenografted directly to rat liver are differentiated into human hepatocytes without fusion. Blood 2005;106:756-763. https://doi.org/10.1182/blood-2005-02-0572
  34. Dai LJ, Li HY, Guan LX, Ritchie G, Zhou JX. The therapeutic potential of bone marrow-derived mesenchymal stem cells on hepatic cirrhosis. Stem Cell Res 2009;2:16-25. https://doi.org/10.1016/j.scr.2008.07.005
  35. Sharma RR, Pollock K, Hubel A, McKenna D. Mesenchymal stem or stromal cells: a review of clinical applications and manufacturing practices. Transfusion 2014;54:1418-1437. https://doi.org/10.1111/trf.12421
  36. Volarevic V, Al-Qahtani A, Arsenijevic N, Pajovic S, Lukic ML. Interleukin-1 receptor antagonist (IL-1Ra) and IL-1Ra producing mesenchymal stem cells as modulators of diabetogenesis. Autoimmunity 2010;43:255-263. https://doi.org/10.3109/08916930903305641
  37. Parekkadan B, van Poll D, Suganuma K, et al. Mesenchymal stem cell-derived molecules reverse fulminant hepatic failure. PLoS One 2007;2:e941. https://doi.org/10.1371/journal.pone.0000941
  38. Augello A, Tasso R, Negrini SM, et al. Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur J Immunol 2005;35:1482-1490. https://doi.org/10.1002/eji.200425405
  39. Haddad R, Saldanha-Araujo F. Mechanisms of T-cell immunosuppression by mesenchymal stromal cells: what do we know so far? Biomed Res Int 2014;2014:216806.
  40. Najar M, Raicevic G, Fayyad-Kazan H, et al. Immune-related antigens, surface molecules and regulatory factors in human-derived mesenchymal stromal cells: the expression and impact of inflammatory priming. Stem Cell Rev 2012;8:1188-1198. https://doi.org/10.1007/s12015-012-9408-1
  41. Kupcova Skalnikova H. Proteomic techniques for characterisation of mesenchymal stem cell secretome. Biochimie 2013;95:2196-2211. https://doi.org/10.1016/j.biochi.2013.07.015
  42. Crisostomo PR, Wang Y, Markel TA, Wang M, Lahm T, Meldrum DR. Human mesenchymal stem cells stimulated by TNF-alpha, LPS, or hypoxia produce growth factors by an NF kappa B- but not JNK-dependent mechanism. Am J Physiol Cell Physiol 2008;294:C675-C682. https://doi.org/10.1152/ajpcell.00437.2007
  43. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006;98:1076-1084. https://doi.org/10.1002/jcb.20886
  44. Sakaida I, Terai S, Yamamoto N, et al. Transplantation of bone marrow cells reduces CCl4-induced liver fibrosis in mice. Hepatology 2004;40:1304-1311. https://doi.org/10.1002/hep.20452
  45. Wang L, Wang X, Wang L, et al. Hepatic vascular endothelial growth factor regulates recruitment of rat liver sinusoidal endothelial cell progenitor cells. Gastroenterology 2012;143:1555.e2-1563.e2.
  46. Kim SU, Oh HJ, Wanless IR, Lee S, Han KH, Park YN. The Laennec staging system for histological sub-classification of cirrhosis is useful for stratification of prognosis in patients with liver cirrhosis. J Hepatol 2012;57:556-563. https://doi.org/10.1016/j.jhep.2012.04.029
  47. Mohammadi Gorji S, Karimpor Malekshah AA, Hashemi-Soteh MB, Rafiei A, Parivar K, Aghdami N. Effect of mesenchymal stem cells on doxorubicin-induced fibrosis. Cell J 2012;14:142-151.
  48. Zhang D, Jiang M, Miao D. Transplanted human amniotic membrane-derived mesenchymal stem cells ameliorate carbon tetrachloride-induced liver cirrhosis in mouse. PLoS One 2011;6:e16789. https://doi.org/10.1371/journal.pone.0016789
  49. Michalopoulos GK. Liver regeneration after partial hepatectomy: critical analysis of mechanistic dilemmas. Am J Pathol 2010;176:2-13. https://doi.org/10.2353/ajpath.2010.090675
  50. Marsden ER, Hu Z, Fujio K, Nakatsukasa H, Thorgeirsson SS, Evarts RP. Expression of acidic fibroblast growth factor in regenerating liver and during hepatic differentiation. Lab Invest 1992;67:427-433.
  51. Webber EM, Godowski PJ, Fausto N. In vivo response of hepatocytes to growth factors requires an initial priming stimulus. Hepatology 1994;19:489-497. https://doi.org/10.1002/hep.1840190230
  52. Nozawa K, Kurumiya Y, Yamamoto A, Isobe Y, Suzuki M, Yoshida S. Up-regulation of telomerase in primary cultured rat hepatocytes. J Biochem 1999;126:361-367. https://doi.org/10.1093/oxfordjournals.jbchem.a022458
  53. Li WL, Su J, Yao YC, et al. Isolation and characterization of bipotent liver progenitor cells from adult mouse. Stem Cells 2006;24:322-332. https://doi.org/10.1634/stemcells.2005-0108
  54. Usunier B, Benderitter M, Tamarat R, Chapel A. Management of fibrosis: the mesenchymal stromal cells breakthrough. Stem Cells Int 2014;2014:340257.
  55. Parekkadan B, van Poll D, Megeed Z, et al. Immunomodulation of activated hepatic stellate cells by mesenchymal stem cells. Biochem Biophys Res Commun 2007;363:247-252. https://doi.org/10.1016/j.bbrc.2007.05.150
  56. Wang J, Bian C, Liao L, et al. Inhibition of hepatic stellate cells proliferation by mesenchymal stem cells and the possible mechanisms. Hepatol Res 2009;39:1219-1228. https://doi.org/10.1111/j.1872-034X.2009.00564.x
  57. Lin N, Hu K, Chen S, et al. Nerve growth factor-mediated paracrine regulation of hepatic stellate cells by multipotent mesenchymal stromal cells. Life Sci 2009;85:291-295. https://doi.org/10.1016/j.lfs.2009.06.007
  58. Chen S, Xu L, Lin N, Pan W, Hu K, Xu R. Activation of Notch1 signaling by marrow-derived mesenchymal stem cells through cell-cell contact inhibits proliferation of hepatic stellate cells. Life Sci 2011;89:975-981. https://doi.org/10.1016/j.lfs.2011.10.012
  59. Rabani V, Shahsavani M, Gharavi M, Piryaei A, Azhdari Z, Baharvand H. Mesenchymal stem cell infusion therapy in a carbon tetrachloride-induced liver fibrosis model affects matrix metalloproteinase expression. Cell Biol Int 2010;34:601-605. https://doi.org/10.1042/CBI20090386
  60. Semedo P, Correa-Costa M, Antonio Cenedeze M, et al. Mesenchymal stem cells attenuate renal fibrosis through immune modulation and remodeling properties in a rat remnant kidney model. Stem Cells 2009;27:3063-3073.
  61. Wu Y, Huang S, Enhe J, et al. Bone marrow-derived mesenchymal stem cell attenuates skin fibrosis development in mice. Int Wound J 2014;11:701-710. https://doi.org/10.1111/iwj.12034
  62. Ali G, Mohsin S, Khan M, et al. Nitric oxide augments mesenchymal stem cell ability to repair liver fibrosis. J Transl Med 2012;10:75. https://doi.org/10.1186/1479-5876-10-75
  63. Clement S, Pascarella S, Negro F. Hepatitis C virus infection: molecular pathways to steatosis, insulin resistance and oxidative stress. Viruses 2009;1:126-143. https://doi.org/10.3390/v1020126
  64. Tanikawa K, Torimura T. Studies on oxidative stress in liver diseases: important future trends in liver research. Med Mol Morphol 2006;39:22-27. https://doi.org/10.1007/s00795-006-0313-z
  65. Ivanov AV, Smirnova OA, Ivanova ON, Masalova OV, Kochetkov SN, Isaguliants MG. Hepatitis C virus proteins activate NRF2/ARE pathway by distinct ROS-dependent and independent mechanisms in HUH7 cells. PLoS One 2011;6:e24957. https://doi.org/10.1371/journal.pone.0024957
  66. Zhu R, Wang Y, Zhang L, Guo Q. Oxidative stress and liver disease. Hepatol Res 2012;42:741-749. https://doi.org/10.1111/j.1872-034X.2012.00996.x
  67. Cash WJ, McCance DR, Young IS, et al. Primary biliary cirrhosis is associated with oxidative stress and endothelial dysfunction but not increased cardiovascular risk. Hepatol Res 2010;40:1098-1106. https://doi.org/10.1111/j.1872-034X.2010.00717.x
  68. Li X, Benjamin IS, Alexander B. Reproducible production of thioacetamide-induced macronodular cirrhosis in the rat with no mortality. J Hepatol 2002;36:488-493. https://doi.org/10.1016/S0168-8278(02)00011-9
  69. Ledda-Columbano GM, Coni P, Curto M, et al. Induction of two different modes of cell death, apoptosis and necrosis, in rat liver after a single dose of thioacetamide. Am J Pathol 1991;139:1099-1109.
  70. Parola M, Robino G. Oxidative stress-related molecules and liver fibrosis. J Hepatol 2001;35:297-306. https://doi.org/10.1016/S0168-8278(01)00142-8
  71. De Minicis S, Brenner DA. NOX in liver fibrosis. Arch Biochem Biophys 2007;462:266-272. https://doi.org/10.1016/j.abb.2007.04.016
  72. Weber LW, Boll M, Stampfl A. Hepatotoxicity and mechanism of action of haloalkanes: carbon tetrachloride as a toxicological model. Crit Rev Toxicol 2003;33:105-136. https://doi.org/10.1080/713611034
  73. Mohamadnejad M, Alimoghaddam K, Mohyeddin-Bonab M, et al. Phase 1 trial of autologous bone marrow mesenchymal stem cell transplantation in patients with decompensated liver cirrhosis. Arch Iran Med 2007;10:459-466.
  74. Kharaziha P, Hellstrom PM, Noorinayer B, et al. Improvement of liver function in liver cirrhosis patients after autologous mesenchymal stem cell injection: a phase I-II clinical trial. Eur J Gastroenterol Hepatol 2009;21:1199-1205. https://doi.org/10.1097/MEG.0b013e32832a1f6c
  75. Amer ME, El-Sayed SZ, El-Kheir WA, et al. Clinical and laboratory evaluation of patients with end-stage liver cell failure injected with bone marrow-derived hepatocyte-like cells. Eur J Gastroenterol Hepatol 2011;23:936-941. https://doi.org/10.1097/MEG.0b013e3283488b00
  76. Amin MA, Sabry D, Rashed LA, et al. Short-term evaluation of autologous transplantation of bone marrow-derived mesenchymal stem cells in patients with cirrhosis: Egyptian study. Clin Transplant 2013;27:607-612. https://doi.org/10.1111/ctr.12179
  77. Zhang Z, Lin H, Shi M, et al. Human umbilical cord mesenchymal stem cells improve liver function and ascites in decompensated liver cirrhosis patients. J Gastroenterol Hepatol 2012;27 Suppl 2:112-120. https://doi.org/10.1111/j.1440-1746.2011.07024.x
  78. El-Ansary M, Abdel-Aziz I, Mogawer S, et al. Phase II trial: undifferentiated versus differentiated autologous mesenchymal stem cells transplantation in Egyptian patients with HCV induced liver cirrhosis. Stem Cell Rev 2012;8:972-981. https://doi.org/10.1007/s12015-011-9322-y
  79. Jang YO, Kim YJ, Baik SK, et al. Histological improvement following administration of autologous bone marrow-derived mesenchymal stem cells for alcoholic cirrhosis: a pilot study. Liver Int 2014;34:33-41. https://doi.org/10.1111/liv.12218
  80. Peng L, Xie DY, Lin BL, et al. Autologous bone marrow mesenchymal stem cell transplantation in liver failure patients caused by hepatitis B: short-term and long-term outcomes. Hepatology 2011;54:820-828. https://doi.org/10.1002/hep.24434
  81. di Bonzo LV, Ferrero I, Cravanzola C, et al. Human mesenchymal stem cells as a two-edged sword in hepatic regenerative medicine: engraftment and hepatocyte differentiation versus profibrogenic potential. Gut 2008;57:223-231. https://doi.org/10.1136/gut.2006.111617
  82. Baertschiger RM, Serre-Beinier V, Morel P, et al. Fibrogenic potential of human multipotent mesenchymal stromal cells in injured liver. PLoS One 2009;4:e6657. https://doi.org/10.1371/journal.pone.0006657
  83. Zhu W, Xu W, Jiang R, et al. Mesenchymal stem cells derived from bone marrow favor tumor cell growth in vivo. Exp Mol Pathol 2006;80:267-274. https://doi.org/10.1016/j.yexmp.2005.07.004
  84. Gladman M, Cudkowicz M, Zinman L. Enhancing clinical trials in neurodegenerative disorders: lessons from amyotrophic lateral sclerosis. Curr Opin Neurol 2012;25:735-742. https://doi.org/10.1097/WCO.0b013e32835a309d
  85. Healy BC, Schoenfeld D. Comparison of analysis approaches for phase III clinical trials in amyotrophic lateral sclerosis. Muscle Nerve 2012;46:506-511. https://doi.org/10.1002/mus.23392
  86. Mudrabettu C, Kumar V, Rakha A, et al. Safety and efficacy of autologous mesenchymal stromal cells transplantation in patients undergoing living donor kidney transplantation: a pilot study. Nephrology (Carlton) 2015;20:25-33. https://doi.org/10.1111/nep.12338
  87. Xu L, Ryugo DK, Pongstaporn T, Johe K, Koliatsos VE. Human neural stem cell grafts in the spinal cord of SOD1 transgenic rats: differentiation and structural integration into the segmental motor circuitry. J Comp Neurol 2009;514:297-309. https://doi.org/10.1002/cne.22022
  88. Yan J, Xu L, Welsh AM, et al. Extensive neuronal differentiation of human neural stem cell grafts in adult rat spinal cord. PLoS Med 2007;4:e39. https://doi.org/10.1371/journal.pmed.0040039
  89. Raore B, Federici T, Taub J, et al. Cervical multilevel intraspinal stem cell therapy: assessment of surgical risks in Gottingen minipigs. Spine (Phila Pa 1976) 2011;36:E164-E171. https://doi.org/10.1097/BRS.0b013e3181d77a47
  90. Wang F, Dennis JE, Awadallah A, et al. Transcriptional profiling of human mesenchymal stem cells transduced with reporter genes for imaging. Physiol Genomics 2009;37:23-34. https://doi.org/10.1152/physiolgenomics.00300.2007
  91. Yaghoubi SS, Campbell DO, Radu CG, Czernin J. Positron emission tomography reporter genes and reporter probes: gene and cell therapy applications. Theranostics 2012;2:374-391. https://doi.org/10.7150/thno.3677
  92. Zhang SJ, Wu JC. Comparison of imaging techniques for tracking cardiac stem cell therapy. J Nucl Med 2007;48:1916-1919. https://doi.org/10.2967/jnumed.107.043299
  93. Chen J, Wang F, Zhang Y, et al. In vivo tracking of superparamagnetic iron oxide nanoparticle labeled chondrocytes in large animal model. Ann Biomed Eng 2012;40:2568-2578. https://doi.org/10.1007/s10439-012-0621-5
  94. Neri M, Maderna C, Cavazzin C, et al. Efficient in vitro labeling of human neural precursor cells with superparamagnetic iron oxide particles: relevance for in vivo cell tracking. Stem Cells 2008;26:505-516. https://doi.org/10.1634/stemcells.2007-0251
  95. Hu SL, Zhang JQ, Hu X, et al. In vitro labeling of human umbilical cord mesenchymal stem cells with superparamagnetic iron oxide nanoparticles. J Cell Biochem 2009;108:529-535. https://doi.org/10.1002/jcb.22283

피인용 문헌

  1. Renin-angiotensin system inhibitors and fibrosis in chronic liver disease: a systematic review vol.10, pp.5, 2016, https://doi.org/10.1007/s12072-016-9705-x
  2. Effect of Function-Enhanced Mesenchymal Stem Cells Infected With Decorin-Expressing Adenovirus on Hepatic Fibrosis vol.5, pp.9, 2016, https://doi.org/10.5966/sctm.2015-0323
  3. Antifibrotic Activity of Human Placental Amnion Membrane-Derived CD34+ Mesenchymal Stem/Progenitor Cell Transplantation in Mice With Thioacetamide-Induced Liver Injury vol.5, pp.11, 2015, https://doi.org/10.5966/sctm.2015-0343
  4. Cell transplantation as a non-invasive strategy for treating liver fibrosis vol.10, pp.5, 2015, https://doi.org/10.1586/17474124.2016.1134313
  5. The current state of liver regeneration therapy vol.57, pp.6, 2015, https://doi.org/10.2957/kanzo.57.269
  6. Transplantation with autologous bone marrow‐derived mesenchymal stem cells for alcoholic cirrhosis: Phase 2 trial vol.64, pp.6, 2015, https://doi.org/10.1002/hep.28693
  7. Involvement of hepatic macrophages in the antifibrotic effect of IGF-I-overexpressing mesenchymal stromal cells vol.7, pp.1, 2016, https://doi.org/10.1186/s13287-016-0424-y
  8. Clinical effectiveness of cell therapies in patients with chronic liver disease and acute-on-chronic liver failure: a systematic review protocol vol.5, pp.1, 2015, https://doi.org/10.1186/s13643-016-0277-6
  9. Transient elastography versus hepatic venous pressure gradient for diagnosing portal hypertension: a systematic review and meta-analysis vol.23, pp.1, 2015, https://doi.org/10.3350/cmh.2016.0059
  10. Transient elastography can be integrated into routine clinical practice for the evaluation of portal hypertension? vol.23, pp.1, 2017, https://doi.org/10.3350/cmh.2017.0101
  11. 1-Methyl-L-tryptophan promotes the apoptosis of hepatic stellate cells arrested by interferon-γ by increasing the expression of IFN-γRβ, IRF-1 and FAS vol.40, pp.2, 2015, https://doi.org/10.3892/ijmm.2017.3043
  12. Reversal of liver cirrhosis: current evidence and expectations vol.32, pp.2, 2015, https://doi.org/10.3904/kjim.2016.268
  13. Diagnostic Accuracy of Hepatic Vein Arrival Time Performed with Contrast-Enhanced Ultrasonography for Cirrhosis: A Systematic Review and Meta-Analysis vol.11, pp.1, 2017, https://doi.org/10.5009/gnl16031
  14. Rifaximin and Propranolol Combination Therapy Is More Effective than Propranolol Monotherapy for the Reduction of Portal Pressure: An Open Randomized Controlled Pilot Study vol.11, pp.5, 2017, https://doi.org/10.5009/gnl16478
  15. Mesenchymal Stem Cell-Dependent Modulation of Liver Diseases vol.13, pp.9, 2015, https://doi.org/10.7150/ijbs.20240
  16. Progress in stem cell-based therapy for liver disease : Stem cell therapy in hepatology vol.47, pp.2, 2017, https://doi.org/10.1111/hepr.12747
  17. Infusion of umbilical cord mesenchymal stem cells alleviates symptoms of ankylosing spondylitis vol.14, pp.2, 2015, https://doi.org/10.3892/etm.2017.4687
  18. Prognostic value of sarcopenia in patients with liver cirrhosis: A systematic review and meta-analysis vol.12, pp.10, 2017, https://doi.org/10.1371/journal.pone.0186990
  19. Therapeutic potential of mesenchymal stromal cells for hypoxic ischemic encephalopathy: A systematic review and meta-analysis of preclinical studies vol.12, pp.12, 2017, https://doi.org/10.1371/journal.pone.0189895
  20. Liver fibrosis alleviation after co-transplantation of hematopoietic stem cells with mesenchymal stem cells in patients with thalassemia major vol.97, pp.2, 2015, https://doi.org/10.1007/s00277-017-3181-9
  21. Impact of Bacterial Translocation on Hepatopulmonary Syndrome: A Prospective Observational Study vol.63, pp.1, 2015, https://doi.org/10.1007/s10620-017-4868-4
  22. Human Endometrial Regenerative Cells Attenuate Bleomycin-Induced Pulmonary Fibrosis in Mice vol.2018, pp.None, 2015, https://doi.org/10.1155/2018/3475137
  23. Current Perspectives Regarding Stem Cell-Based Therapy for Liver Cirrhosis vol.2018, pp.None, 2015, https://doi.org/10.1155/2018/4197857
  24. Comparative Effects of Umbilical Cord- and Menstrual Blood-Derived MSCs in Repairing Acute Lung Injury vol.2018, pp.None, 2018, https://doi.org/10.1155/2018/7873625
  25. Tanshinol ameliorates CCl 4 -induced liver fibrosis in rats through the regulation of Nrf2/HO-1 and NF-κB/IκBα signaling pathway vol.12, pp.None, 2018, https://doi.org/10.2147/dddt.s159546
  26. Salidroside ameliorates autophagy and activation of hepatic stellate cells in mice via NF-κB and TGF-β1/Smad3 pathways vol.12, pp.None, 2018, https://doi.org/10.2147/dddt.s162950
  27. Human umbilical cord mesenchymal stem cells inhibit proliferation of hepatic stellate cells in vitro vol.41, pp.5, 2015, https://doi.org/10.3892/ijmm.2018.3500
  28. Transplantation of human matrix metalloproteinase-1 gene-modified bone marrow-derived mesenchymal stem cell attenuates CCL4-induced liver fibrosis in rats vol.41, pp.6, 2015, https://doi.org/10.3892/ijmm.2018.3516
  29. Role of the renin-angiotensin system in hepatic fibrosis and portal hypertension vol.33, pp.3, 2018, https://doi.org/10.3904/kjim.2017.317
  30. Expression of Fibroblast Growth Factor 21 and β-Klotho Regulates Hepatic Fibrosis through the Nuclear Factor-κB and c-Jun N-Terminal Kinase Pathways vol.12, pp.4, 2015, https://doi.org/10.5009/gnl17443
  31. Historical Perspectives and Advances in Mesenchymal Stem Cell Research for the Treatment of Liver Diseases vol.154, pp.1, 2015, https://doi.org/10.1053/j.gastro.2017.09.049
  32. Mesenchymal stem cells attenuate liver fibrosis by suppressing Th17 cells - an experimental study vol.31, pp.1, 2015, https://doi.org/10.1111/tri.13023
  33. Novelties in the pathophysiology and management of portal hypertension: new treatments on the horizon vol.12, pp.suppl1, 2018, https://doi.org/10.1007/s12072-017-9806-1
  34. A study about immunomodulatory effect and efficacy and prognosis of human umbilical cord mesenchymal stem cells in patients with chronic hepatitis B‐induced decompensated liver cirrhosis vol.33, pp.4, 2018, https://doi.org/10.1111/jgh.14081
  35. Anti‐Inflammatory and Anti‐Fibrotic Effects of Human Amniotic Membrane Mesenchymal Stem Cells and Their Potential in Corneal Repair vol.7, pp.12, 2015, https://doi.org/10.1002/sctm.18-0042
  36. Mesenchymal stem cells: potential application for the treatment of hepatic cirrhosis vol.9, pp.1, 2015, https://doi.org/10.1186/s13287-018-0814-4
  37. Stem Cell Transplant for Advanced Stage Liver Disorders: Current Scenario and Future Prospects vol.26, pp.None, 2015, https://doi.org/10.2174/0929867326666191004161802
  38. The mechanisms and potential of stem cell therapy for penile fibrosis vol.16, pp.2, 2015, https://doi.org/10.1038/s41585-018-0109-7
  39. Evaluation of the Effects of Cultured Bone Marrow Mesenchymal Stem Cell Infusion on Hepatocarcinogenesis in Hepatocarcinogenic Mice With Liver Cirrhosis vol.51, pp.3, 2015, https://doi.org/10.1016/j.transproceed.2019.03.011
  40. Mesenchymal stem cells for sensorineural hearing loss: protocol for a systematic review of preclinical studies vol.8, pp.None, 2015, https://doi.org/10.1186/s13643-019-1015-7
  41. Identification of TAF1, HNF4A, and CALM2 as potential therapeutic target genes for liver fibrosis vol.234, pp.6, 2015, https://doi.org/10.1002/jcp.27579
  42. Concise Review: Mesenchymal Stem Cells: From Roots to Boost vol.37, pp.7, 2019, https://doi.org/10.1002/stem.3016
  43. Hyaluronic Acid Hydrogel Integrated with Mesenchymal Stem Cell‐Secretome to Treat Endometrial Injury in a Rat Model of Asherman's Syndrome vol.8, pp.14, 2015, https://doi.org/10.1002/adhm.201900411
  44. Human bone marrow‐derived mesenchymal stromal cells in combination with silymarin regulate hepatocyte growth factor expression and genotoxicity in carbon tetrachloride induced hepatotoxicity in vol.120, pp.8, 2015, https://doi.org/10.1002/jcb.28573
  45. Human skin-derived ABCB5+ stem cell injection improves liver disease parameters in Mdr2KO mice vol.93, pp.9, 2015, https://doi.org/10.1007/s00204-019-02533-3
  46. Dynamic Regulation of miRNA Expression by Functionally Enhanced Placental Mesenchymal Stem Cells Promotes Hepatic Regeneration in a Rat Model with Bile Duct Ligation vol.20, pp.21, 2015, https://doi.org/10.3390/ijms20215299
  47. Mechanisms Underlying Cell Therapy in Liver Fibrosis: An Overview vol.8, pp.11, 2015, https://doi.org/10.3390/cells8111339
  48. Human bone marrow mesenchymal stem cells-derived exosomes alleviate liver fibrosis through the Wnt/β-catenin pathway vol.10, pp.1, 2015, https://doi.org/10.1186/s13287-019-1204-2
  49. Umbilical cord/placenta-derived mesenchymal stem cells inhibit fibrogenic activation in human intestinal myofibroblasts via inhibition of myocardin-related transcription factor A vol.10, pp.1, 2019, https://doi.org/10.1186/s13287-019-1385-8
  50. Bone marrow-derived mesenchymal stem cell (BM-MSC): A tool of cell therapy in hydatid experimentally infected rats vol.8, pp.2, 2019, https://doi.org/10.1016/j.cr.2019.11.001
  51. Effect of miR-181a-3p on osteogenic differentiation of human bone marrow-derived mesenchymal stem cells by targeting BMP10 vol.47, pp.1, 2015, https://doi.org/10.1080/21691401.2019.1687494
  52. Stem Cell Aging in Lifespan and Disease: A State-of-the-Art Review vol.15, pp.None, 2020, https://doi.org/10.2174/1574888x15666200213105155
  53. Molecular Pathways Modulated by Mesenchymal Stromal Cells and Their Extracellular Vesicles in Experimental Models of Liver Fibrosis vol.8, pp.None, 2015, https://doi.org/10.3389/fcell.2020.594794
  54. Matrix Metalloproteinases as Potential Biomarkers and Therapeutic Targets in Liver Diseases vol.9, pp.5, 2020, https://doi.org/10.3390/cells9051212
  55. Mesenchymal Stem Cells for the Treatment of Liver Disease: Present and Perspectives vol.14, pp.3, 2020, https://doi.org/10.5009/gnl18412
  56. Application of Mesenchymal Stem Cells in Inflammatory and Fibrotic Diseases vol.21, pp.21, 2015, https://doi.org/10.3390/ijms21218366
  57. Mesenchymal stromal cells; a new horizon in regenerative medicine vol.235, pp.12, 2015, https://doi.org/10.1002/jcp.29803
  58. Exosomes derived from mmu_circ_0000623-modified ADSCs prevent liver fibrosis via activating autophagy vol.39, pp.12, 2015, https://doi.org/10.1177/0960327120931152
  59. Diffusion tensor imaging quantifying the severity of chronic hepatitis in rats vol.20, pp.1, 2015, https://doi.org/10.1186/s12880-020-00466-3
  60. Enhanced PRL-1 expression in placenta-derived mesenchymal stem cells accelerates hepatic function via mitochondrial dynamics in a cirrhotic rat model vol.11, pp.1, 2015, https://doi.org/10.1186/s13287-020-02029-3
  61. Perspective of placenta derived mesenchymal stem cells in acute liver failure vol.10, pp.1, 2015, https://doi.org/10.1186/s13578-020-00433-z
  62. Bone Marrow-derived Mesenchymal Stem Cells Reverse Hepatic Fibrosis, Improved Vascularity, and Attenuate the Apoptosis in Carbon Tetrachloride-induced Hepatic Fibrosis Experimental Rats vol.9, pp.1, 2021, https://doi.org/10.3889/oamjms.2021.6590
  63. Effectiveness of Mesenchymal Stem Cells and Bovine Colostrum on Decreasing Tumor Necrosis Factor-Α Levels and Enhancement of Macrophages M2 in Remnant Liver vol.9, pp.1, 2015, https://doi.org/10.3889/oamjms.2021.7902
  64. Apigenin Alleviates Liver Fibrosis by Inhibiting Hepatic Stellate Cell Activation and Autophagy via TGF-β1/Smad3 and p38/PPARα Pathways vol.2021, pp.None, 2021, https://doi.org/10.1155/2021/6651839
  65. Taxifolin, Extracted from Waste Larix olgensis Roots, Attenuates CCl4-Induced Liver Fibrosis by Regulating the PI3K/AKT/mTOR and TGF-β1/Smads Signaling Pathways vol.15, pp.None, 2015, https://doi.org/10.2147/dddt.s281369
  66. Mesenchymal Stromal Cell-Derived Extracellular Vesicles Regulate the Mitochondrial Metabolism via Transfer of miRNAs vol.12, pp.None, 2015, https://doi.org/10.3389/fimmu.2021.623973
  67. Macrophage Polarization and Its Role in Liver Disease vol.12, pp.None, 2021, https://doi.org/10.3389/fimmu.2021.803037
  68. Regulatory T Cells Improved the Anti-cirrhosis Activity of Human Amniotic Mesenchymal Stem Cell in the Liver by Regulating the TGF-β-Indoleamine 2,3-Dioxygenase Signaling vol.9, pp.None, 2015, https://doi.org/10.3389/fcell.2021.737825
  69. Human Liver Stem Cell-Derived Extracellular Vesicles Target Hepatic Stellate Cells and Attenuate Their Pro-fibrotic Phenotype vol.9, pp.None, 2021, https://doi.org/10.3389/fcell.2021.777462
  70. Acute-on-Chronic Liver Failure: Pathophysiological Mechanisms and Management vol.8, pp.None, 2015, https://doi.org/10.3389/fmed.2021.752875
  71. Regulatory Effect of Mesenchymal Stromal Cells on the Development of Liver Fibrosis: Cellular and Molecular Mechanisms and Prospects for Clinical Application vol.11, pp.1, 2015, https://doi.org/10.1134/s2079086421010059
  72. Hepatoprotective effect of bone marrow-derived mesenchymal stromal cells in CCl 4 -induced liver cirrhosis vol.11, pp.2, 2021, https://doi.org/10.1007/s13205-021-02640-y
  73. Can bone marrow‐derived mesenchymal stem cells change liver volume?: A case report vol.5, pp.2, 2015, https://doi.org/10.1002/jgh3.12466
  74. Recent advances in polymeric scaffolds containing carbon nanotube and graphene oxide for cartilage and bone regeneration vol.26, pp.None, 2015, https://doi.org/10.1016/j.mtcomm.2021.102097
  75. Exosomes derived from autologous dermal fibroblasts promote diabetic cutaneous wound healing through the Akt/β-catenin pathway vol.20, pp.5, 2015, https://doi.org/10.1080/15384101.2021.1894813
  76. Co‐transplantation of bone marrow‐derived mesenchymal stem cells with hematopoietic stem cells does not improve transplantation outcome in class III beta‐thalassemia major: A prospec vol.25, pp.3, 2015, https://doi.org/10.1111/petr.13905
  77. Recent Trends in Multipotent Human Mesenchymal Stem/Stromal Cells: Learning from History and Advancing Clinical Applications vol.25, pp.6, 2015, https://doi.org/10.1089/omi.2021.0049
  78. Wilson's disease: Revisiting an old friend vol.13, pp.6, 2021, https://doi.org/10.4254/wjh.v13.i6.634
  79. The Phosphonate Derivative of C60 Fullerene Induces Differentiation towards the Myogenic Lineage in Human Adipose-Derived Mesenchymal Stem Cells vol.22, pp.17, 2021, https://doi.org/10.3390/ijms22179284
  80. Cell-Based Regeneration and Treatment of Liver Diseases vol.22, pp.19, 2015, https://doi.org/10.3390/ijms221910276
  81. 3D hESC exosomes enriched with miR-6766-3p ameliorates liver fibrosis by attenuating activated stellate cells through targeting the TGFβRII-SMADS pathway vol.19, pp.1, 2015, https://doi.org/10.1186/s12951-021-01138-2
  82. Regenerative Potential of Mesenchymal Stem Cells’ (MSCs) Secretome for Liver Fibrosis Therapies vol.22, pp.24, 2015, https://doi.org/10.3390/ijms222413292