Abstract
Modulation of the immune system may be a viable alternative in the treatment of fulminant hepatic failure (FHF) and can potentially eliminate the need for donor hepatocytes for cellular therapies. Multipotent bone marrow-derived mesenchymal stem cells (MSCs) have been shown to inhibit the function of various immune cells by undefined paracrine mediators in vitro. Yet, the therapeutic potential of MSC-derived molecules has not been tested in immunological conditions in vivo. Herein, we report that the administration of MSC-derived molecules in two clinically relevant forms-intravenous bolus of conditioned medium (MSC-CM) or extracorporeal perfusion with a bioreactor containing MSCs (MSC-EB)-can provide a significant survival benefit in rats undergoing FHF. We observed a cell mass-dependent reduction in mortality that was abolished at high cell numbers indicating a therapeutic window. Histopathological analysis of liver tissue after MSC-CM treatment showed dramatic reduction of panlobular leukocytic infiltrates, hepatocellular death and bile duct duplication. Furthermore, we demonstrate using computed tomography of adoptively transferred leukocytes that MSC-CM functionally diverts immune cells from the injured organ indicating that altered leukocyte migration by MSC-CM therapy may account for the absence of immune cells in liver tissue. Preliminary analysis of the MSC secretome using a protein array screen revealed a large fraction of chemotactic cytokines, or chemokines. When MSC-CM was fractionated based on heparin binding affinity, a known ligand for all chemokines, only the heparin-bound eluent reversed FHF indicating that the active components of MSC-CM reside in this fraction. These data provide the first experimental evidence of the medicinal use of MSC-derived molecules in the treatment of an inflammatory condition and support the role of chemokines and altered leukocyte migration as a novel therapeutic modality for FHF.
MeSH Terms
Adoptive Transfer/methods
Animals
Cell Death/drug effects
Cell Movement/drug effects
Cells, Cultured
Chemokines/metabolism
Culture Media, Conditioned/metabolism,pharmacology
Hepatocytes/drug effects,metabolism,pathology
Humans
Leukocytes/cytology,drug effects,metabolism
Liver Failure, Acute/drug therapy,pathology,therapy
Male
Mesenchymal Stem Cells/cytology,metabolism
Mice
NIH 3T3 Cells
Protein Array Analysis
Rats
Rats, Sprague-Dawley
Chemicals
Chemokines
Culture Media, Conditioned
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Parekkadan Biju
Center for Engineering in Medicine and Surgical Services, Massachusetts General Hospital, Harvard Medical School and the Shriners Hospitals for Children, Boston, Massachusetts, USA.
van Poll Daan
Suganuma Kazuhiro
Carter Edward A
Berthiaume François
Tilles Arno W
Yarmush Martin L
References (15)
15 references, click to expand
-
Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep.
Nat Med. 2000 Nov;6(11):1282-6
PMID: 11062543
-
Immunomodulation of activated hepatic stellate cells by mesenchymal stem cells.
Biochem Biophys Res Commun. 2007 Nov 16;363(2):247-52
PMID: 17869217
-
A bioartificial liver--state of the art.
Science. 2002 Feb 8;295(5557):1005-9
PMID: 11834813
-
Human mesenchymal stem cells support unrelated donor hematopoietic stem cells and suppress T-cell activation.
Bone Marrow Transplant. 2004 Mar;33(6):597-604
PMID: 14716336
-
Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells.
Lancet. 2004 May 1;363(9419):1439-41
PMID: 15121408
-
Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation.
Blood. 2004 Jun 15;103(12):4619-21
PMID: 15001472
-
Simultaneous injection of bone marrow cells and stromal cells into bone marrow accelerates hematopoiesis in vivo.
Stem Cells. 2004;22(7):1256-62
PMID: 15579644
-
Human mesenchymal stem cells modulate allogeneic immune cell responses.
Blood. 2005 Feb 15;105(4):1815-22
PMID: 15494428
-
Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness.
Blood. 2005 Mar 1;105(5):2214-9
PMID: 15514012
-
Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells.
Nat Med. 2005 Apr;11(4):367-8
PMID: 15812508
-
Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement.
FASEB J. 2006 Apr;20(6):661-9
PMID: 16581974
-
The role of mesenchymal stem cells in haemopoiesis.
Blood Rev. 2006 May;20(3):161-71
PMID: 16364518
-
Treatment of fulminant hepatic failure in rats using a bioartificial liver device containing porcine hepatocytes producing interleukin-1 receptor antagonist.
Tissue Eng. 2006 May;12(5):1313-23
PMID: 16771644
-
A bioartificial liver device secreting interleukin-1 receptor antagonist for the treatment of hepatic failure in rats.
J Surg Res. 2007 Jan;137(1):130-40
PMID: 17081566
-
A fulminant hepatic failure model in the rat: involvement of interleukin-1beta and tumor necrosis factor-alpha.
Dig Dis Sci. 2001 Aug;46(8):1700-8
PMID: 11508670