Mesenchymal stem cells alleviate atherosclerosis by elevating number and function of CD4+CD25+FOXP3+ regulatory T-cells and inhibiting macrophage foam cell formation

Molecular and Cellular Biochemistry

Volumn 400, Issue 1-2, 2015, Pages 163-172

  Wang, Zhi Xiao ^a   Wang, Chong Quan ^b   Li, Xiao Yan ^a   Feng, Gao Ke ^a   Zhu, Hong Ling ^a   Ding, Yan ^b   Jiang, Xue Jun ^a  

^a RENMIN HOSPITAL OF WUHAN UNIVERSITY   (China)

^b HUBEI UNIVERSITY OF MEDICINE   (China)

Author keywords

Atherosclerotic plaque; CD4+CD25+FOXP3+ regulatory T cells; Macrophage foam cell; Mesenchymal stem cells

Indexed keywords

APOLIPOPROTEIN E; C REACTIVE PROTEIN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; FAT DROPLET; GAMMA INTERFERON; INTERLEUKIN 10; INTERSTITIAL COLLAGENASE; MESSENGER RNA; SCAVENGER RECEPTOR A; TRANSCRIPTION FACTOR FOXP3; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; INTERLEUKIN 2 RECEPTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASCENDING AORTA; ATHEROSCLEROSIS; BIOCOMPATIBILITY; BIOSAFETY; CD4+ CD25+ T LYMPHOCYTE; CELL CONTACT; CELL COUNT; CONTROLLED STUDY; FLOW CYTOMETRY; FOAM CELL; GENE EXPRESSION; LYMPH NODE; MACROPHAGE MIGRATION INHIBITION; MALE; MESENCHYMAL STEM CELL; MIGRATION INHIBITION; MOUSE; NONHUMAN; OSTEOBLAST; REGULATORY T LYMPHOCYTE; SPLEEN CELL; T LYMPHOCYTE SUBPOPULATION; ANIMAL; CD4+ T LYMPHOCYTE; CELL CULTURE; HUMAN; IMMUNOLOGY; MACROPHAGE; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM; PATHOLOGY; SPLEEN;

MUS;

ANIMALS; ATHEROSCLEROSIS; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; FLOW CYTOMETRY; FOAM CELLS; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MACROPHAGES; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; SPLEEN; T-LYMPHOCYTES, REGULATORY;

EID: 84925517965     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-014-2272-3     Document Type: Article

References (32)

1. Frostegård Johan (2013) Immunity, atherosclerosis and cardiovascular disease. BMC Med 11:117
2. Ait-Oufella H, Sage AP, Mallat Z, Tedgui A (2014) Adaptive (T and B cells) immunity and control by dendritic cells in atherosclerosis. Circ Res 114(10):1640–1660
3. Cheong C, Choi JH (2012) Dendritic cells and regulatory T-cells in atherosclerosis. Mol Cells 34(4):341–347
4. Gerry AB, Leake DS (2014) Effect of low extracellular pH on NF-κB activation in macrophages. Atherosclerosis 233(2):537–544
5. Getz GS, Vanderlaan PA, Reardon CA (2011) Natural killer T-cells in lipoprotein metabolism and atherosclerosis. Thromb Haemost 106(5):814–819
6. Chistiakov DA, Sobenin IA, Orekhov AN (2013) Regulatory T-cells in atherosclerosis and strategies to induce the endogenous atheroprotective immune response. Immunol Lett 151(1–2):10–22
7. Ait-Oufella H, Salomon BL, Potteaux S, Robertson AK, Gourdy P, Zoll J, Merval R, Esposito B, Cohen JL, Fisson S, Flavell RA, Hansson GK, Klatzmann D, Tedgui A, Mallat Z (2006) Natural regulatory T-cells control the development of atherosclerosis in mice. Nat Med 12(2):178–180
8. Tacke F, Alvarez D, Kaplan TJ, Jakubzick C, Spanbroek R, Llodra J, Garin A, Liu J, Mack M, van Rooijen N, Lira SA, Habenicht AJ, Randolph GJ (2007) Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest 117(1):185–194
9. Gu P, Gao JF, D’Souza CA, Kowalczyk A, Chou KY, Zhang L (2012) Trogocytosis of CD80 and CD86 by induced regulatory T-cells. Cell Mol Immunol 9(2):136–146
10. Entin-Meer M, Afek A, George J (2009) Regulatory T-cells, FOXP3 and atherosclerosis. Adv Exp Med Biol 665:106–114
11. Liao J, Chen X, Li Y, Ge Z, Duan H, Zou Y, Ge J (2012) Transfer of bone-marrow-derived mesenchymal stem cells influences vascular remodeling and calcification after balloon injury in hyperlipidemic rats. J Biomed Biotechnol 2012:165296
12. Le Blanc K, Rasmusson I, Sundberg B, Götherström C, Hassan M, Uzunel M, Ringdén O (2004) Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363(9419):1439–1441
13. Levings MK, Sangregorio R, Roncarolo MG (2001) Human CD25+ CD4+ regulatory T-cells suppress naive and memory T-cell proliferation and can be expanded in vitro without loss of function. J Exp Med 193(11):1295–1302
14. Ramasamy R, Fazekasova H, Lam EW, Soeiro I, Lombardi G, Dazzi F (2007) Mesenchymal stem cells inhibit dendritic cell differentiation and function by preventing entry into the cell cycle. Transplantation 83(1):71–76
15. + regulatory T-cells down-regulate co-stimulatory molecules on antigen-presenting cells. Eur J Immunol 30(6):1538–1543
16. + regulatory cells involves a granzyme B-dependent, perforin-independent mechanism. J Immunol 174(4):1783–1786
17. Grossman WJ, Verbsky JW, Barchet W, Colonna M, Atkinson JP, Ley TJ (2004) Human T regulatory cells can use the perforin pathway to cause autologous target cell death. Immunity 21(4):589–601
18. + T-cells regulate virus-specific primary and memory CD8+ T-cell responses. J Exp Med 198(6):889–901
19. + immunoregulatory T-cells suppress polyclonal T-cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 188(2):287–296
20. Collison LW, Vignali DA (2001) In vitro Treg suppression assays. Methods Mol Biol 707:21–37
21. McMurchy AN, Levings MK (2012) Suppression assays with human T regulatory cells: a technical guide. Eur J Immunol 42(1):27–34
22. Whitman SC, Ravisankar P, Daugherty A (2002) Interleukin-18 enhances atherosclerosis in apolipoprotein E(-/-) mice through release of interferon-gamma. Circ Res 90(2):E34–E38
23. Klingenberg R, Gerdes N, Badeau RM, Gisterå A, Strodthoff D, Ketelhuth DF, Lundberg AM, Rudling M, Nilsson SK, Olivecrona G, Zoller S, Lohmann C, Lüscher TF, Jauhiainen M, Sparwasser T, Hansson GK (2013) Depletion of FOXP3+ regulatory T-cells promotes hypercholesterolemia and atherosclerosis. J Clin Invest 123(3):1323–1334
24. Jacobs SA, Roobrouck VD, Verfaillie CM, Van Gool SW (2013) Immunological characteristics of human mesenchymal stem cells and multipotent adult progenitor cells. Immunol Cell Biol 91(1):32–39
25. Sardella G, De Luca L, Francavilla V, Accapezzato D, Mancone M, Sirinian MI, Fedele F, Paroli M (2007) Frequency of naturally-occurring regulatory T-cells is reduced in patients with ST-segment elevation myocardial infarction. Thromb Res 120(4):631–634
26. de Boer OJ, van der Meer JJ, Teeling P, van der Loos CM, van der Wal AC (2007) Low numbers of FOXP3 positive regulatory T-cells are present in all developmental stages of human atherosclerotic lesions. PLoS One 2(8):e779
27. Lü CX, Xu RD, Cao M, Wang G, Yan FQ, Shang SS, Wu XF, Ruan L, Quan XQ, Zhang CT (2013) FOXP3 demethylation as a means of identifying quantitative defects in regulatory T-cells in acute coronary syndrome. Atherosclerosis 229(1):263–270
28. Fang SM, Du DY, Li YT, Ge XL, Qin PT, Zhang QH, Liu Y (2013) Allogeneic bone marrow mesenchymal stem cells transplantation for stabilizing and repairing of atherosclerotic ruptured plaque. Thromb Res 131(6):e253–e257
29. Prockop DJ, Oh JY (2012) Mesenchymal stem/stromal cells (MSCs): role as guardians of inflammation. Mol Ther 20(1):14–20
30. + regulatory T-cell selection. Immunol Rev 212:74–85
31. + regulatory T-cells in self-tolerance and autoimmune disease. Curr Top Microbiol Immunol 305:51–66
32. van Es T, van Puijvelde GH, Foks AC, Habets KL, Bot I, Gilboa E, Van Berkel TJ, Kuiper J (2010) Vaccination against Foxp3(+) regulatory T-cells aggravates atherosclerosis. Atherosclerosis 209(1):74–80