Lipopolysaccharide preconditioning of adipose-derived stem cells improves liver-regenerating activity of the secretome

Stem Cell Research and Therapy

Volumn 6, Issue 1, 2015, Pages 1-11

  Lee, Sang Chul ^a   Jeong, Hye Jin ^a   Lee, Sang Kuon ^a   Kim, Say June ^a  

^a Daejeon St Mary's Hospital   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CELL PROTEIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MESSENGER RNA; SCATTER FACTOR; SECRETOME; THIOACETAMIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN; CONDITIONED MEDIUM; CYTOKINE;

ADIPOSE DERIVED STEM CELL; ALANINE AMINOTRANSFERASE BLOOD LEVEL; AML12 CELL LINE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BIOCHEMICAL COMPOSITION; CASE CONTROL STUDY; CELL DAMAGE; CELL LINE; CELL VIABILITY; CONTROLLED STUDY; CULTURE MEDIUM; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INCUBATION TIME; INFLAMMATION; INTERLEUKIN 6 BLOOD LEVEL; LIVER CELL; LIVER REGENERATION; LIVER RESECTION; LIVER WEIGHT; MALE; MEASUREMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; PROTEIN BLOOD LEVEL; STEM CELL TRANSPLANTATION; TUMOR NECROSIS FACTOR ALPHA BLOOD LEVEL; WEIGHT CHANGE; WESTERN BLOTTING; ADIPOSE TISSUE; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL PROLIFERATION; CELL SURVIVAL; CONDITIONED MEDIUM; CYTOLOGY; DRUG EFFECTS; GENETICS; IMMUNOLOGY; LIVER; METABOLISM; PARACRINE SIGNALING; PATHOLOGY; PHARMACOLOGY; PHYSIOLOGY; SECRETION (PROCESS); SIGNAL TRANSDUCTION; STEM CELL;

MUS;

ADIPOSE TISSUE; ANIMALS; CASE-CONTROL STUDIES; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CULTURE MEDIA, CONDITIONED; CYTOKINES; HUMANS; INFLAMMATION; LIPOPOLYSACCHARIDES; LIVER; LIVER REGENERATION; MALE; MICE; MICE, INBRED BALB C; PARACRINE COMMUNICATION; RNA, MESSENGER; SIGNAL TRANSDUCTION; STEM CELLS; THIOACETAMIDE;

EID: 84928631246     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/s13287-015-0072-7     Document Type: Article

References (64)

1. Yang Z, Di Santo S, Kalka C. Current developments in the use of stem cell for therapeutic neovascularisation: is the future therapy "cell-free"? Swiss Med Wkly. 2010;140:w13130.
2. Schreml S, Babilas P, Fruth S, Orsó E, Schmitz G, Mueller MB, et al. Harvesting human adipose tissue-derived adult stem cells: resection versus liposuction. Cytotherapy. 2009;11:947-57.
3. Miura M, Miura Y, Padilla-Nash HM, Molinolo AA, Fu B, Patel V, et al. Accumulated chromosomal instability in murine bone marrow mesenchymal stem cells leads to malignant transformation. Stem Cells. 2006;24:1095-103.
4. Tolar J, Nauta AJ, Osborn MJ, Panoskaltsis Mortari A, McElmurry RT, Bell S, et al. Sarcoma derived from cultured mesenchymal stem cells. Stem Cells. 2007;25:371-9.
5. Wang Y, Huso DL, Harrington J, Kellner J, Jeong DK, Turney J, et al. Outgrowth of a transformed cell population derived from normal human BM mesenchymal stem cell culture. Cytotherapy. 2005;7:509-19.
6. Baglio SR, Pegtel DM, Baldini N. Mesenchymal stem cell secreted vesicles provide novel opportunities in (stem) cell-free therapy. Front Physiol. 2012;3:359.
7. Gnecchi M, Zhang Z, Ni A, Dzau VJ. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res. 2008;103:1204-19.
8. Hoch AI, Binder BY, Genetos DC, Leach JK. Differentiation-dependent secretion of proangiogenic factors by mesenchymal stem cells. PLoS One. 2012;7:e35579.
9. Ranganath SH, Levy O, Inamdar MS, Karp JM. Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cell. 2012;10:244-58.
10. Stastna M, Van Eyk JE. Investigating the secretome: lessons about the cells that comprise the heart. Circ Cardiovasc Genet. 2012;5:o8-18.
11. van Velthoven CTJ, Kavelaars A, Heijnen CJ. Mesenchymal stem cells as a treatment for neonatal ischemic brain damage. Pediatr Res. 2012;71:474-81.
12. Lavoie JR, Rosu-Myles M. Uncovering the secretes of mesenchymal stem cells. Biochimie. 2013;95:2212-21.
13. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MAJ, Hopmans ES, Lindenberg JL, et al. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci U S A. 2010;107:6328-33.
14. Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10:1470-6.
15. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654-9.
16. Banas A, Teratani T, Yamamoto Y, Tokuhara M, Takeshita F, Osaki M, et al. IFATS collection: in vivo therapeutic potential of human adipose tissue mesenchymal stem cells after transplantation into mice with liver injury. Stem Cells. 2008;26:2705-12.
17. Kim S-J, Park KC, Lee JU, Kim K-J, Kim D-G. Therapeutic potential of adipose tissue-derived stem cells for liver failure according to the transplantation routes. J Korean Surg Soc. 2011;81:176-86.
18. Lam SP, Luk JM, Man K, Ng KTP, Cheung CK, Rose-John S, et al. Activation of interleukin-6-induced glycoprotein 130/signal transducer and activator of transcription 3 pathway in mesenchymal stem cells enhances hepatic differentiation, proliferation, and liver regeneration. Liver Transpl. 2010;16:1195-206.
19. Liang L, Ma T, Chen W, Hu J, Bai X, Li J, et al. Therapeutic potential and related signal pathway of adipose-derived stem cell transplantation for rat liver injury. Hepatol Res. 2009;39:822-32.
20. 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. 2012;178:63-70.
21. Du Z, Wei C, Cheng K, Han B, Yan J, Zhang M, et al. Mesenchymal stem cell-conditioned medium reduces liver injury and enhances regeneration in reduced-size rat liver transplantation. J Surg Res. 2013;183:907-15.
22. Mintz PJ, Huang K-W, Reebye V, Nteliopoulos G, Lai H-S, Sætrom P, et al. Exploiting human CD34+ stem cell-conditioned medium for tissue repair. Mol Ther. 2014;22:149-59.
23. Fouraschen SM, Pan Q, de Ruiter PE, Farid WR, Kazemier G, Kwekkeboom J, et al. Secreted factors of human liver-derived mesenchymal stem cells promote liver regeneration early after partial hepatectomy. Stem Cells Dev. 2012;21:2410-9.
24. Bunnell BA, Betancourt AM, Sullivan DE. New concepts on the immune modulation mediated by mesenchymal stem cells. Stem Cell Res Ther. 2010;1:34.
25. Arimilli S, Johnson JB, Alexander-Miller MA, Parks GD. TLR-4 and -6 agonists reverse apoptosis and promote maturation of simian virus 5-infected human dendritic cells through NFkB-dependent pathways. Virology. 2007;365:144-56.
26. Ha T, Hua F, Liu X, Ma J, McMullen JR, Shioi T, et al. Lipopolysaccharide-induced myocardial protection against ischaemia/reperfusion injury is mediated through a PI3K/Akt-dependent mechanism. Cardiovasc Res. 2008;78:546-53.
27. Heemann U, Szabo A, Hamar P, Müller V, Witzke O, Lutz J, et al. Lipopolysaccharide pretreatment protects from renal ischemia/reperfusion injury: possible connection to an interleukin-6-dependent pathway. Am J Pathol. 2000;156:287-93.
28. Sano T, Izuishi K, Hossain MA, Kakinoki K, Okano K, Masaki T, et al. Protective effect of lipopolysaccharide preconditioning in hepatic ischaemia reperfusion injury. HPB (Oxford). 2010;12:538-45.
29. Lee SM, Lee SC, Kim S-J. Contribution of human adipose tissue-derived stem cells and the secretome to the skin allograft survival in mice. J Surg Res. 2014;188:280-9.
30. Kim DH, Je CM, Sin JY, Jung JS. Effect of partial hepatectomy on in vivo engraftment after intravenous administration of human adipose tissue stromal cells in mouse. Microsurgery. 2003;23:424-31.
31. Seo MJ, Suh SY, Bae YC, Jung JS. Differentiation of human adipose stromal cells into hepatic lineage in vitro and in vivo. Biochem Biophys Res Commun. 2005;328:258-64.
32. Zhang B, Inagaki M, Jiang B, Miyakoshi M, Arikura J, Ogawa K, et al. Effects of bone marrow and hepatocyte transplantation on liver injury. J Surg Res. 2009;157:71-80.
33. Greene AK, Puder M. Partial hepatectomy in the mouse: technique and perioperative management. J Invest Surg. 2003;16:99-102.
34. Bockhorn M, Goralski M, Prokofiev D, Dammann P, Grünewald P, Trippler M, et al. VEGF is important for early liver regeneration after partial hepatectomy. J Surg Res. 2007;138:291-9.
35. Lehmann K, Tschuor C, Rickenbacher A, Jang J-H, Oberkofler CE, Tschopp O, et al. Liver failure after extended hepatectomy in mice is mediated by a p21-dependent barrier to liver regeneration. Gastroenterology. 2012;143:1609-1619.e1604.
36. Yu J, Yin S, Zhang W, Gao F, Liu Y, Chen Z, et al. Hypoxia preconditioned bone marrow mesenchymal stem cells promote liver regeneration in a rat massive hepatectomy model. Stem Cell Res Ther. 2013;4:83.
37. Fujiyoshi M, Ozaki M. Molecular mechanisms of liver regeneration and protection for treatment of liver dysfunction and diseases. J Hepatobiliary Pancreat Sci. 2011;18:13-22.
38. Taniguchi E, Sakisaka S, Matsuo K, Tanikawa K, Sata M. Expression and role of vascular endothelial growth factor in liver regeneration after partial hepatectomy in rats. J Histochem Cytochem. 2001;49:121-30.
39. Yamashita T, Wang XW. Cancer stem cells in the development of liver cancer. J Clin Invest. 2013;123:1911-8.
40. Bullwinkel J, Baron-Lühr B, Lüdemann A, Wohlenberg C, Gerdes J, Scholzen T. Ki-67 protein is associated with ribosomal RNA transcription in quiescent and proliferating cells. J Cell Physiol. 2006;206:624-35.
41. Campbell JS, Argast GM, Yuen SY, Hayes B, Fausto N. Inactivation of p38 MAPK during liver regeneration. Int J Biochem Cell Biol. 2011;43:180-8.
42. Kupcova Skalnikova H. Proteomic techniques for characterisation of mesenchymal stem cell secretome. Biochimie. 2013;95:2196-211.
43. Samad F, Yamamoto K, Loskutoff DJ. Distribution and regulation of plasminogen activator inhibitor-1 in murine adipose tissue in vivo. Induction by tumor necrosis factor-alpha and lipopolysaccharide. J Clin Invest. 1996;97:37-46.
44. Scherer PE, Williams S, Fogliano M, Baldini G, Lodish HF. A novel serum protein similar to C1q, produced exclusively in adipocytes. J Biol Chem. 1995;270:26746-9.
45. Steppan CM, Bailey ST, Bhat S, Brown EJ, Banerjee RR, Wright CM, et al. The hormone resistin links obesity to diabetes. Nature. 2001;409:307-12.
46. Trayhurn P. Endocrine and signalling role of adipose tissue: new perspectives on fat. Acta Physiol Scand. 2005;184:285-93.
47. Lee MJ, Kim J, Kim MY, Bae Y-S, Ryu SH, Lee TG, et al. Proteomic analysis of tumor necrosis factor-alpha-induced secretome of human adipose tissue-derived mesenchymal stem cells. J Proteome Res. 2010;9:1754-62.
48. Makridakis M, Roubelakis MG, Vlahou A. Stem cells: insights into the secretome. Biochim Biophys Acta. 2013;1834:2380-4.
49. Zvonic S, Lefevre M, Kilroy G, Floyd ZE, DeLany JP, Kheterpal I, et al. Secretome of primary cultures of human adipose-derived stem cells: modulation of serpins by adipogenesis. Mol Cell Proteomics. 2007;6:18-28.
50. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105:1815-22.
51. Jones BJ, McTaggart SJ. Immunosuppression by mesenchymal stromal cells: from culture to clinic. Exp Hematol. 2008;36:733-41.
52. Le Blanc K, Samuelsson H, Gustafsson B, Remberger M, Sundberg B, Arvidson J, et al. Transplantation of mesenchymal stem cells to enhance engraftment of hematopoietic stem cells. Leukemia. 2007;21:1733-8.
53. Salem HK, Thiemermann C. Mesenchymal stromal cells: current understanding and clinical status. Stem Cells. 2010;28:585-96.
54. Stagg J. Immune regulation by mesenchymal stem cells: two sides to the coin. Tissue Antigens. 2007;69:1-9.
55. Uccelli A, Mancardi G, Chiesa S. Is there a role for mesenchymal stem cells in autoimmune diseases? Autoimmunity. 2008;41:592-5.
56. Uccelli A, Moretta L, Pistoia V. Immunoregulatory function of mesenchymal stem cells. Eur J Immunol. 2006;36:2566-73.
57. Uccelli A, Pistoia V, Moretta L. Mesenchymal stem cells: a new strategy for immunosuppression? Trends Immunol. 2007;28:219-26.
58. Kilroy GE, Foster SJ, Wu X, Ruiz J, Sherwood S, Heifetz A, et al. Cytokine profile of human adipose-derived stem cells: expression of angiogenic, hematopoietic, and pro-inflammatory factors. J Cell Physiol. 2007;212:702-9.
59. Drucker C, Gewiese J, Malchow S, Scheller J, Rose-John S. Impact of interleukin-6 classic- and trans-signaling on liver damage and regeneration. J Autoimmun. 2010;34:29-37.
60. Rose-John S. IL-6 trans-signaling via the soluble IL-6 receptor: importance for the pro-inflammatory activities of IL-6. Int J Biol Sci. 2012;8:1237-47.
61. Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S. The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys Acta. 2011;1813:878-88.
62. Chen X, Zhang Z-Y, Zhou H, Zhou G-W. Characterization of mesenchymal stem cells under the stimulation of Toll-like receptor agonists. Dev Growth Differ. 2014;56:233-44.
63. Gao B. Cytokines, STATs and liver disease. Cell Mol Immunol. 2005;2:92-100.
64. Klein C, Wüstefeld T, Assmus U, Roskams T, Rose-John S, Müller M, et al. The IL-6-gp130-STAT3 pathway in hepatocytes triggers liver protection in T cell-mediated liver injury. J Clin Invest. 2005;115:860-9.