Paracrine mechanisms of proliferative, anti-apoptotic and anti-inflammatory effects of mesenchymal stromal cells in models ofacute organ injury

Cytotherapy

Volumn 16, Issue 5, 2014, Pages 579-585

  Khubutiya, Mogeli S ^a   Vagabov, Aleksandr V ^a   Temnov, Andrey A ^a   Sklifas, Alla N ^b  

^a N V SKLIFOSOVSKY RESEARCH INSTITUTE FOR EMERGENCY MEDICINE   (Russian Federation)

^b INSTITUTE OF CELL BIOPHYSICS   (Russian Federation)

Author keywords

Cytokines; Growth factors; Mesenchymal stromal cell derived conditioned medium; Mesenchymal stromal cells; Paracrine factors

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN 2; ANGIOPOIETIN RECEPTOR; CYTOKINE; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; KERATINOCYTE GROWTH FACTOR; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUROTROPHIN 3; NEUROTROPHIN 4; PROTEIN KINASE B; SCATTER FACTOR; TRANSCRIPTION FACTOR GATA 4; TUMOR NECROSIS FACTOR RECEPTOR 1; VASCULOTROPIN;

ACUTE DISEASE; ANGIOGENESIS; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; BURN; CELL PROLIFERATION; CELL PROTECTION; CELL REGENERATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HEART MUSCLE INJURY; HUMAN; KIDNEY INJURY; LIVER INJURY; LUNG INJURY; MESENCHYMAL STROMA CELL; NONHUMAN; ORGAN INJURY; PRIORITY JOURNAL; REVIEW; ANIMAL; CYTOLOGY; MESENCHYMAL STEM CELL TRANSPLANTATION; PARACRINE SIGNALING; PHYSIOLOGY;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; PARACRINE COMMUNICATION;

EID: 84897966003     PISSN: 14653249     EISSN: 14772566     Source Type: Journal    
DOI: 10.1016/j.jcyt.2013.07.017     Document Type: Review

References (50)

1. Heron M. Deaths: leading causes for 2004. Natl Vital Stat Rep 2007, 56:1-95.
2. Yagi H., Soto-Gutierrez A., Kitaqawa Y., Tilles A.W., Tompkins R.G., Yarmush M.L. Bone marrow mesenchymal stromal cells attenuate organ injury induced by LPS and burn. Cell Transplant 2010, 19:823-830.
3. Morigi M., Rota C., Montemurro T., Montelatici E., Lo Cicero V., Imberti B., et al. Life-sparing effect of human cord blood-mesenchymal stem cells in experimental acute kidney injury. Stem Cells 2010, 28:513-522.
4. Morigi M., Introna M., Imberti B., Corna D., Abbate M., Rota C., et al. Human bone marrow mesenchymal stem cells accelerate recovery of acute renal injury and prolong survival in mice. Stem Cells 2008, 26:2075-2082.
5. Montzka K., Fuhrmann T., Muller-Ehmsen J., Woltje M., Brook G.A. Growth factor and cytokine expression of human mesenchymal stromal cells is not altered in an in vitro model of tissue damage. Cytotherapy 2010, 12:870-880.
6. Lee J.W., Fang X., Gupta N., Serikov V., Matthay M.A. Allogenic human mesenchymal stem cells for treatment of E.coli endotoxin-induced acute lung injury in the ex vivo perfused human lung. Proc Natl Acad Sci U S A 2009, 106:16357-16362.
7. Eliopoulos N., Zhao J., Bouchentouf M., Forner K., Birman E., Yuan S., et al. Human marrow-derived mesenchymal stromal cells decrease cisplatin renotoxicity in vitro and in vivo and enhance survival of mice post-intraperitoneal injection. Am J Physiol Renal Physiol 2010, 299:F1288-F1298.
8. Danchuk S., Ylostalo J.H., Hossain F., Sorge R., Ramsey A., Bonvillain R.W., et al. Human multipotent stromal cells attenuate lipopolysaccharide-induced acute lung injury in mice via secretion of tumor necrosis factor-α-induced protein 6. Stem Cell Res Ther 2011, 2:27.
9. Yagi H., Soto-Gutierrez A., Navarro-Alvarez N., Nahmias Y., Goldwasser Y., Kitagawa Y., et al. Reactive bone marrow stromal cells attenuate systemic inflammation via sTNFR1. Mol Ther 2010, 18:1857-1864.
10. Bi B., Schmitt R., Israilova M., Nishio H., Cantley L.G. Stromal cells protect against acute tubular injury via an endocrine effect. JAm Soc Nephrol 2007, 18:2486-2496.
11. Wu Y., Chen L., Scott P.G., Tredget E.E. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells 2007, 25:2648-2659.
12. Crisostomo P.R., Wang M., Herring C.M., Markel T.A., Meldrum K.K., Lillemoe K.D., et al. Gender differences in injury induced mesenchymal stem cell apoptosis, expression of VEGF, TNF, and IL-6 and abrogation via TNFR1 ablation. JMol Cell Cardiol 2007, 42:142-149.
13. Asahara T., Chen D., Tsurumi Y., Kearney M., Rossow S., Passeri J., et al. Accelerated restitution of endothelial integrity and endothelium-dependent function after phVEGF165 gene transfer. Circulation 1996, 94:3291-3302.
14. Karihaloo A., Karumanchi S.A., Cantley W.L., Venkatesha S., Cantley L.G., Kale S. Vascular endothelial growth factor induces branching morphogenesis tubulogenesis in renal epithelial cells in a neuropilin-dependent fashion. Mol Cell Biol 2005, 25:7441-7448.
15. Miller S.B., Martin D.R., Kissane J., Hammerman M.R. Hepatocyte growth factor accelerates recovery from acute ischemic renal injury in rats. Am J Physiol 1994, 266(1 Pt 2):F129-F134.
16. Miller S.B., Martin D.R., Kissane J., Hammerman M.R. Insulin-like growth factor I accelerates recovery from ischemic acute tubular necrosis in the rat. Proc Natl Acad Sci U S A 1992, 89:11876-11880.
17. Kuwana H., Terada Y., Kobayashi T., Okado T., Penninger J.M., Irie-Sasaki J., et al. The phosphoinositide-3 kinase gamma-Akt pathway mediates renal tubular injury in cisplatin nephrotoxicity. Kidney Int 2008, 73:430-445.
18. Lieberthal W., Triaca V., Levine J. Mechanisms of death induced by cisplatin in proximal tubular epithelial cells: apoptosis vs. necrosis. Am J Physiol 1996, 270(4 Pt 2):F700-F708.
19. Garcia-Fernandez M., Delgado G., Puche J.E., González-Barón S., Castilla Cortázar I. Low doses of insulinlike growth factor I improve insulin resistance, lipid metabolism, and oxidative damage in aging rats. Endocrinology 2008, 149:2433-2442.
20. Okada M., Sugita K., Inukai T., Goi K., Kagami K., Kawasaki K., et al. Hepatocyte growth factor protects small airway epithelial cells from apoptosis induced by tumor necrosis factor-alpha or oxidative stress. Pediatr Res 2004, 56:336-344.
21. Kumar P., Miller A.I., Polverini P.J. p38 MAPK mediates gamma-irradiation-induced endothelial cell apoptosis, and vascular endothelial growth factor protects endothelial cells through the phosphoinositide 3-kinase-Akt-Bcl-2 pathway. JBiol Chem 2004, 279:43352-43360.
22. Hung S.C., Pochampally R.R., Chen S.C., Hsu S.C., Prockop D.J. Angiogenic effects of human multipotent stromal cell conditioned medium activate the P13K-Akt pathway in hypoxic endothelial cells to inhibit apoptosis, increase survival, and stimulate angiogenesis. Stem Cells 2007, 25:2363-2370.
23. Ramesh G., Reeves W.B. TNF-alpha mediates chemokine and cytokine expression and renal injury in cisplatin nephrotoxicity. JClin Invest 2002, 110:835-842.
24. Zhang B., Ramesh G., Norbury C.C., Reeves W.B. Cisplatin-induced nephrotoxicity is mediated by tumor necrosis factor-alpha produced by renal parenchymal cells. Kidney Int 2007, 72:37-44.
25. Blundell C.D., Mahoney D.J., Almond A., DeAngelis P.L., Kahmann J.D., Teriete P., et al. The link module from ovulation- and inflammation-associated protein TSG-6 changes conformation on hyaluronan binding. JBiol Chem 2003, 278:49261-49270.
26. Milner C.M., Higman V.A., Day A.J. TSG-6: a pluripotent inflammatory mediator?. Biochem Soc Trans 2006, 34(Pt 3):446-450.
27. Wisniewski H.G., Vilcek J. Cytokine-induced gene expression at the crossroads of innate immunity, inflammation and fertility: TSG-6 and PTX3/TSG-14. Cytokine Growth Factor Rev 2004, 15:129-146.
28. Oh J.Y., Kim M.K., Shin M.S., Wee W.R., Lee J.H. Cytokine secretion by human mesenchymal stem cells cocultured with damaged corneal epithelial cells. Cytokine 2009, 46:100-103.
29. Parekkadan B., van Poll D., Megeed Z., Kobayashi N., Tilles A.W., Berthiaume F., et al. Immunomodulation of activated hepatic stellate cells by mesenchymal stem cells. Biochem Biophys Res Commun 2007, 363:247-252.
30. Aggarwal S., Pittenger M.F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005, 105:1815-1822.
31. Nemeth K., Leelahavanichkul A., Yuen P.S., Mayer B., Parmelee A., Doi K., et al. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 2009, 15:42-49.
32. Groh M.E., Maitra B., Szekely E., Koc O.N. Human mesenchymal stem cells require monocyte-mediated activation to suppress alloreactive T cells. Exp Hematol 2005, 33:928-934.
33. Sotiropoulou P.A., Perez S.A., Gritzapis A.D., Baxevanis C.N., Papamichail M. Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells 2006, 24:74-85.
34. Leskela H.V., Olkku A., Lehtonen S., Mahonen A., Koivunen J., Turpeinen M., et al. Estrogen receptor alpha genotype confers interindividual variability of response to estrogen and testosterone in mesenchymal-stem-cell-derived osteoblasts. Bone 2006, 39:1026-1034.
35. Wang Q., Yu J.H., Zhai H.H., Zhao Q.T., Chen J.W., Shu L., et al. Temporal expression of estrogen receptor alpha in rat bone marrow mesenchymal stem cells. Biochem Biophys Res Commun 2006, 347:117-123.
36. Ionescu L., Byrne R.N., van Haaften T., Vadivel A., Alphonse R.S., Rey-Parra G.J., et al. Stem cell conditioned medium improves acute lung injury in mice: in vivo evidence for stem cell paracrine action. Am J Physiol Lung Cell Mol Physiol 2012, 303:L967-L977.
37. Kinnaird T., Stabile E., Burnett M.S., Shou M., Lee C.W., Barr S., et al. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 2004, 109:1543-1549.
38. Webber M.J., Han X., Murthy S.N., Rajangam K., Stupp S.I., Lomasney J.W. Capturing the stem cell paracrine effect using heparin-presenting nanofibres to treat cardiovascular diseases. JTissue Eng Regen Med 2010, 4:600-610.
39. Boomsma R.A., Geenen D.L. Mesenchymal stem cells secrete multiple cytokines that promote angiogenesis and have contrasting effects on chemotaxis and apoptosis. PLoS One 2012, 7:e35685.
40. Li H., Zuo S., He Z., Yang Y., Pasha Z., Wang Y., et al. Paracrine factors released by GATA-4 overexpressed mesenchymal stem cells increase angiogenesis and cell survival. Am J Physiol Heart Circ Physiol 2010, 299:H1772-H1781.
41. Takehara Y., Yabuuchi A., Ezoe K., Kuroda T., Yamadera R., Sano C., et al. The restorative effects of adipose-derived mesenchymal stem cells on damaged ovarian function. Lab Invest 2013, 93:181-193.
42. Johansson U., Rasmusson I., Niclou S.P., Forslund N., Gustavsson L., Nilsson B., et al. Formation of composite endothelial cell-mesenchymal stem cell islets: a novel approach to promote islet revascularization. Diabetes 2008, 57:2393-2401.
43. Oh J.Y., Kim M.K., Shin M.S., Lee H.J., Ko J.H., Wee W.R., et al. The anti-inflammatory and anti-angiogenic role of mesenchymal stem cells in corneal wound healing following chemical injury. Stem Cells 2008, 26:1047-1055.
44. Bartholomew A., Sturgeon C., Siatskas M., Ferrer K., McIntosh K., Patil S., et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 2002, 30:42-48.
45. Corcione A., Benvenuto F., Ferretti E., Giunti D., Cappiello V., Cazzanti F., et al. Human mesenchymal stem cells modulate B-cell functions. Blood 2006, 107:367-372.
46. Di Nicola M., Carlo-Stella C., Magni M., Milanesi M., Longoni P.D., Matteucci P., et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002, 99:3838-3843.
47. Batten P., Sarathchandra P., Antoniw J.W., Tay S.S., Lowdell M.W., Taylor P.M., et al. Human mesenchymal stem cells induce T cell anergy and downregulate T cell allo-responses via the TH2 pathway: relevance to tissue engineering human heart valves. Tissue Eng 2006, 12:2263-2273.
48. Meisel R., Zibert A., Laryea M., Göbel U., Däubener W., Dilloo D. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood 2004, 103:4619-4621.
49. Li W., Ren G., Huang Y., Su J., Han Y., Li J., et al. Mesenchymal stem cells: a double-edged sword in regulating immune responses. Cell Death Differ 2012, 19:1505-1513.
50. Engela A.U., Baan C.C., Dor F.J.M.F., Weimar W., Hoogduijn M.J. On the interactions between mesenchymal stem cells and regulatory T cells for immunomodulation in transplantation. Front Immunol 2012, 3:126.