Mouse bone marrow-derived mesenchymal stem cells induce macrophage M2 polarization through the nuclear factor-κB and signal transducer and activator of transcription 3 pathways

Experimental Biology and Medicine

Volumn 239, Issue 3, 2014, Pages 366-375

  Gao, Shuo ^a   Mao, Fei ^a   Zhang, Bin ^a   Zhang, Ling ^a   Zhang, Xu ^a   Wang, Mei ^a   Yan, Yongmin ^a   Yang, Tingting ^a   Zhang, Jie ^a   Zhu, Wei ^a   Qian, Hui ^a   Xu, Wenrong ^a  

^a JIANGSU UNIVERSITY   (China)

Author keywords

inflammation; macrophage; Mesenchymal stem cells; polarization; signaling pathway

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; ARGINASE 1; BETA ACTIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CELL SELECTION; COCULTURE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; MACROPHAGE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PHENOTYPE; POLARIZATION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

INFLAMMATION; MACROPHAGE; MESENCHYMAL STEM CELLS; POLARIZATION; SIGNALING PATHWAY;

AMINOSALICYLIC ACIDS; ANIMALS; ARGINASE; BENZENESULFONATES; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; INTERLEUKIN-10; LECTINS, C-TYPE; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES; MANNOSE-BINDING LECTINS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED BALB C; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84896056890     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1177/1535370213518169     Document Type: Article

References (32)

1. Pittenger MF,Mackay AM,Beck SC,Jaiswal RK,Douglas R,Mosca JD,Moorman MA,Simonetti DW,Craig S,Marshak DR.Multilineage potential of adult human mesenchymal stem cells.Science. 1999;284:143-47.
2. Shi Y,Su J,Roberts AI,Shou P,Rabson AB,Ren G.How mesenchymal stem cells interact with tissue immune responses.Trends Immunol. 2012;33:136-43.
3. Xu H,Qian H,Zhu W,Zhang X,Yan Y,Mao F,Wang M,Xu H,Xu W.Mesenchymal stem cells relieve fibrosis of Schistosoma japonicum-induced mouse liver injury.Exp Biol Med (Maywood). 2012;237:585-92.
4. Yan Y,Xu W,Qian H,Si Y,Zhu W,Cao H,Zhou H,Mao F.Mesenchymal stem cells from human umbilical cords ameliorate mouse hepatic injury in vivo.Liver Int. 2009;29:356-65.
5. Chen Y,Qian H,Zhu W,Zhang X,Yan Y,Ye S,Peng X,Li W,Xu W.Hepatocyte growth factor modification promotes the amelioration effects of human umbilical cord mesenchymal stem cells on rat acute kidney injury.Stem Cells Dev. 2011;20:103-13.
6. Mao F,Xu WR,Qian H,Zhu W,Yan YM,Shao QX,Xu HX.Immunosuppressive effects of mesenchymal stem cells in collagen-induced mouse arthritis.Inflamm Res. 2010;59:219-25.
7. Meirelles Lda S,Fontes AM,Covas DT,Caplan AI.Mechanisms involved in the therapeutic properties of mesenchymal stem cells.Cytokine Growth Factor Rev. 2009;20:419-27.
8. Glennie S,Soeiro I,Dyson PJ,Lam EW,Dazzi F.Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells.Blood. 2005;105:2821-27.
9. Corcione A,Benvenuto F,Ferretti E,Giunti D,Cappiello V,Cazzanti F,Risso M,Gualandi F,Mancardi GL,Pistoia V,Uccelli A.Human mesenchymal stem cells modulate B-cell functions.Blood. 2006;107:367-72.
10. Spaggiari GM,Abdelrazik H,Becchetti F,Moretta L.MSCs inhibit monocyte-derived DC maturation and function by selectively interfering with the generation of immature DCs: central role of MSC-derived prostaglandin E2.Blood. 2009;113:6576-83.
11. Sotiropoulou PA,Perez SA,Gritzapis AD,Baxevanis CN,Papamichail M.Interactions between human mesenchymal stem cells and natural killer cells.Stem Cells. 2006;24:74-85.
12. Németh K,Leelahavanichkul A,Yuen PS,Mayer B,Parmelee A,Doi K,Robey PG,Leelahavanichkul K,Koller BH,Brown JM,Hu X,Jelinek I,Star RA,Mezey E.Bone marrow stromal cells attenuate sepsis via prostaglandin E (2)-dependent reprogramming of host macrophages to increase their interleukin-10 production.Nat Med. 2009;15:42-9.
13. Biswas SK,Chittezhath M,Shalova IN,Lim JY.Macrophage polarization and plasticity in health and disease.Immunol Res. 2012;53:11-24.
14. Mosser DM,Edwards JP.Exploring the full spectrum of macrophage activation.Nat Rev Immunol. 2008;8:958-69.
15. Pena OM,Pistolic J,Raj D,Fjell CD,Hancock RE.Endotoxin tolerance represents a distinctive state of alternative polarization (M2) in human mononuclear cells.J Immunol. 2011;186:7243-54.
16. Kim J,Hematti P.Mesenchymal stem cell-educated macrophages: a novel type of alternatively activated macrophages.Exp Hematol. 2009;37:1445-53.
17. Dayan V,Yannarelli G,Billia F,Filomeno P,Wang XH,Davies JE,Keating A.Mesenchymal stromal cells mediate a switch to alternatively activated monocytes/macrophages after acute myocardial infarction.Basic Res Cardiol. 2011;106:1299-310.
18. Zhang QZ,Su WR,Shi SH,Wilder-Smith P,Xiang AP,Wong A,Nguyen AL,Kwon CW,Le AD.Human gingiva-derived mesenchymal stem cells elicit polarization of m2 macrophages and enhance cutaneous wound healing.Stem Cells. 2010;28:1856-68.
19. Li W,Zhang Q,Wang M,Wu H,Mao F,Zhang B,Ji R,Gao S,Sun Z,Zhu W,Qian H,Chen Y,Xu W.Macrophages are involved in the protective role of human umbilical cord-derived stromal cells in renal ischemia-reperfusion injury.Stem Cell Res. 2013;10:405-16.
20. Chen L,Tredget EE,Wu PY,Wu Y.Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing.PLoS One. 2008;3:e1886-e1886.
21. Qian Q,Qian H,Zhang X,Zhu W,Yan Y,Ye S,Peng X,Li W,Xu Z,Sun L,Xu W.5-Azacytidine induces cardiac differentiation of human umbilical cord-derived mesenchymal stem cells by activating extracellular regulated kinase.Stem Cells Dev. 2012;21:67-75.
22. Fairweather D,Cihakova D.Alternatively activated macrophages in infection and autoimmunity.J Autoimmun. 2009;33:222-30.
23. Maggini J,Mirkin G,Bognanni I,Holmberg J,Piazzón IM,Nepomnaschy I,Costa H,Cañones C,Raiden S,Vermeulen M,Geffner JR.Mouse bone marrow-derived mesenchymal stromal cells turn activated macrophages into a regulatory-like profile.PLoS One. 2010;5:e9252-e9252.
24. Sica A,Mantovani A.Macrophage plasticity and polarization: in vivo veritas.J Clin Invest. 2012;122:787-95.
25. Ylöstalo JH,Bartosh TJ,Coble K,Prockop DJ.Human mesenchymal stem/stromal cells (hMSCs) cultured as spheroids are self-activated to produce prostaglandin E2 (PGE2) that directs stimulated macrophages into an anti-inflammatory phenotype.Stem Cells. 2012;30:2283-96.
26. Choi H,Lee RH,Bazhanov N,Oh JY,Prockop DJ.Anti-inflammatory protein TSG-6 secreted by activated MSCs attenuates zymosan-induced mouse peritonitis by decreasing TLR2/NF-κB signaling in resident macrophages.Blood. 2011;118:330-8.
27. Bonizzi G,Karin M.The two NF-kappaB activation pathways and their role in innate and adaptive immunity.Trends Immunol. 2004;25:280-8.
28. El Kasmi KC,Holst J,Coffre M,Mielke L,de Pauw A,Lhocine N,Smith AM,Rutschman R,Kaushal D,Shen Y,Suda T,Donnelly RP,Myers MG,Alexander W,Vignali DA,Watowich SS,Ernst M,Hilton DJ,Murray PJ.General nature of the STAT3-activated anti-inflammatory response.J Immunol. 2006;177:7880-8.
29. Lang R,Patel D,Morris JJ,Rutschman RL,Murray PJ.Shaping gene expression in activated and resting primary macrophages by IL-10.J Immunol. 2002;169:2253-63.
30. Weidenbusch M,Anders HJ.Tissue microenvironments define and get reinforced by macrophage phenotypes in homeostasis or during inflammation, repair and fibrosis.J Innate Immun. 2012;4:463-77.
31. Ueno T,Nakashima A,Doi S,Kawamoto T,Honda K,Yokoyama Y,Doi T,Higashi Y,Yorioka N,Kato Y,Kohno N,Masaki T.Mesenchymal stem cells ameliorate experimental peritoneal fibrosis by suppressing inflammation and inhibiting TGF-β1 signaling.Kidney Int. 2013;84:297-307.
32. Varin A,Pontikoglou C,Labat E,Deschaseaux F,Sensebé L.CD200R/CD200 inhibits osteoclastogenesis: new mechanism of osteoclast control by mesenchymal stem cells in human.PLoS One. 2013;8:e72831-e72831.