MicroRNA-155 promotes the directional migration of resident smooth muscle progenitor cells by regulating monocyte chemoattractant protein 1 in transplant arteriosclerosis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 36, Issue 6, 2016, Pages 1230-1239

  Sun, Yuan ^a,b   Wang, Ke ^b   Ye, Ping ^c   Wu, Jie ^b   Ren, Lingyun ^b,c   Zhang, Anchen ^b   Huang, Xiaofan ^b   Deng, Peng ^b   Wu, Chuangyan ^b   Yue, Zhang ^b   Chen, Zhaolei ^a   Ding, Xiangchao ^b   Chen, Jiuling ^b   Xia, Jiahong ^b,c  

^a YANGZHOU UNIVERSITY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c CENTRAL HOSPITAL OF WUHAN   (China)

Author keywords

adventitia; arteriosclerosis; bone marrow; hyperplasia; stem cells

Indexed keywords

BIOLOGICAL MARKER; CD68 ANTIGEN; MICRORNA 155; MONOCYTE CHEMOTACTIC PROTEIN 1; PLATELET DERIVED GROWTH FACTOR BB; CCL2 PROTEIN, MOUSE; MICRORNA; MIRN155 MICRORNA, MOUSE;

ADVENTITIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA GRAFT; ARTERIOSCLEROSIS; ARTERY INTIMA PROLIFERATION; ARTICLE; BIOACCUMULATION; BONE MARROW CELL; CELL MIGRATION; CONTROLLED STUDY; IN VITRO STUDY; MOUSE; NEOINTIMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SMOOTH MUSCLE PROGENITOR CELL; STEM CELL; UPREGULATION; ADVERSE EFFECTS; ALLOGRAFT; ANIMAL; AORTA; ATHEROSCLEROSIS; BAGG ALBINO MOUSE; BLOOD VESSEL GRAFT; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CHEMOTAXIS; GENETIC TRANSFECTION; GENETICS; GENOTYPE; HYPERPLASIA; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHENOTYPE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CELL; TIME FACTOR; TRANSPLANTATION; VASCULAR SMOOTH MUSCLE;

ADVENTITIA; ALLOGRAFTS; ANIMALS; AORTA; ATHEROSCLEROSIS; BONE MARROW TRANSPLANTATION; CELL DIFFERENTIATION; CELLS, CULTURED; CHEMOKINE CCL2; CHEMOTAXIS; GENOTYPE; HYPERPLASIA; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NEOINTIMA; PHENOTYPE; SIGNAL TRANSDUCTION; STEM CELLS; TIME FACTORS; TRANSFECTION; VASCULAR GRAFTING;

EID: 84963628604     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.115.306691     Document Type: Article

References (34)

1. Suzuki J, Isobe M, Morishita R, Nagai R, Characteristics of chronic rejection in heart transplantation: important elements of pathogenesis and future treatments. Circ J 2010 74 233 239
2. Merrilees MJ, Campbell JH, Spanidis E, Campbell GR, Glycosaminoglycan synthesis by smooth muscle cells of differing phenotype and their response to endothelial cell conditioned medium. Atherosclerosis 1990 81 245 254
3. Ang AH, Tachas G, Campbell JH, Bateman JF, Campbell GR, Collagen synthesis by cultured rabbit aortic smooth-muscle cells. Alteration with phenotype. Biochem J 1990 265 461 469
4. Daniel JM, Bielenberg W, Stieger P, Weinert S, Tillmanns H, Sedding DG, Time-course analysis on the differentiation of bone marrow-derived progenitor cells into smooth muscle cells during neointima formation. Arterioscler Thromb Vasc Biol 2010 30 1890 1896. doi: 10.1161/ATVBAHA.110.209692
5. Hillebrands J, van den Hurk BM, Klatter FA, Popa ER, Nieuwenhuis P, Rozing J, Recipient origin of neointimal vascular smooth muscle cells in cardiac allografts with transplant arteriosclerosis. J Heart Lung Transplant 2000 19 1183 1192
6. Hillebrands JL, Klatter FA, van den Hurk BM, Popa ER, Nieuwenhuis P, Rozing J, Origin of neointimal endothelium and alpha-actin-positive smooth muscle cells in transplant arteriosclerosis. J Clin Invest 2001 107 1411 1422. doi: 10.1172/JCI10233
7. Tang Z, Wang A, Yuan F, Yan Z, Liu B, Chu JS, Helms JA, Li S, Differentiation of multipotent vascular stem cells contributes to vascular diseases. Nat Commun 2012 3 875. doi: 10.1038/ncomms1867
8. Song Z, Li W, Zheng Q, Shang D, Shu X, Guan S, The origin of neointimal smooth muscle cells in transplant arteriosclerosis from recipient bone-marrow cells in rat aortic allograft. J Huazhong Univ Sci Technolog Med Sci 2007 27 303 306. doi: 10.1007/s11596-007-0322-8
9. Shimizu K, Sugiyama S, Aikawa M, Fukumoto Y, Rabkin E, Libby P, Mitchell RN, Host bone-marrow cells are a source of donor intimal smooth- muscle-like cells in murine aortic transplant arteriopathy. Nat Med 2001 7 738 741. doi: 10.1038/89121
10. Iwata H, Manabe I, Fujiu K, Yamamoto T, Takeda N, Eguchi K, Furuya A, Kuro-o M, Sata M, Nagai R, Bone marrow-derived cells contribute to vascular inflammation but do not differentiate into smooth muscle cell lineages. Circulation 2010 122 2048 2057. doi: 10.1161/CIRCULATIONAHA.110.965202
11. Xu Q, Stem cells and transplant arteriosclerosis. Circ Res 2008 102 1011 1024. doi: 10.1161/CIRCRESAHA.108.171488
12. Orlandi A, Bennett M, Progenitor cell-derived smooth muscle cells in vascular disease. Biochem Pharmacol 2010 79 1706 1713. doi: 10.1016/j.bcp.2010.01.027
13. Majesky MW, Dong XR, Regan JN, Hoglund VJ, Vascular smooth muscle progenitor cells: building and repairing blood vessels. Circ Res 2011 108 365 377. doi: 10.1161/CIRCRESAHA.110.223800
14. Majesky MW, Dong XR, Hoglund V, Mahoney WM Jr, Daum G, The adventitia: a dynamic interface containing resident progenitor cells. Arterioscler Thromb Vasc Biol 2011 31 1530 1539. doi: 10.1161/ATVBAHA.110.221549
15. Sainz J, Al Haj Zen A, Caligiuri G, Demerens C, Urbain D, Lemitre M, Lafont A, Isolation of side population progenitor cells from healthy arteries of adult mice. Arterioscler Thromb Vasc Biol 2006 26 281 286. doi: 10.1161/01.ATV.0000197793.83391.91
16. Hu Y, Zhang Z, Torsney E, Afzal AR, Davison F, Metzler B, Xu Q, Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. J Clin Invest 2004 113 1258 1265. doi: 10.1172/JCI19628
17. Grudzinska MK, Kurzejamska E, Bojakowski K, Soin J, Lehmann MH, Reinecke H, Murry CE, Soderberg-Naucler C, Religa P, Monocyte chemoattractant protein 1-mediated migration of mesenchymal stem cells is a source of intimal hyperplasia. Arterioscler Thromb Vasc Biol 2013 33 1271 1279. doi: 10.1161/ATVBAHA.112.300773
18. Shimizu K, Minami M, Shubiki R, Lopez-Ilasaca M, MacFarlane L, Asami Y, Li Y, Mitchell RN, Libby P, CC chemokine receptor-1 activates intimal smooth muscle-like cells in graft arterial disease. Circulation 2009 120 1800 1813. doi: 10.1161/CIRCULATIONAHA.109.859595
19. Chen Y, Wong MM, Campagnolo P, Simpson R, Winkler B, Margariti A, Hu Y, Xu Q, Adventitial stem cells in vein grafts display multilineage potential that contributes to neointimal formation. Arterioscler Thromb Vasc Biol 2013 33 1844 1851. doi: 10.1161/ATVBAHA.113.300902
20. OConnell RM, Taganov KD, Boldin MP, Cheng G, Baltimore D, MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci USA 2007 104 1604 1609. doi: 10.1073/pnas.0610731104
21. Hartmann P, Schober A, Weber C, Chemokines and microRNAs in atherosclerosis. Cell Mol Life Sci 2015 72 3253 3266. doi: 10.1007/s00018-015-1925-z
22. Du F, Yu F, Wang Y, Hui Y, Carnevale K, Fu M, Lu H, Fan D, MicroRNA-155 deficiency results in decreased macrophage inflammation and attenuated atherogenesis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2014 34 759 767. doi: 10.1161/ATVBAHA.113.302701
23. Shimizu K, Mitchell RN, The role of chemokines in transplant graft arterial disease. Arterioscler Thromb Vasc Biol 2008 28 1937 1949. doi: 10.1161/ATVBAHA.107.161232
24. Mitchell RN, Graft vascular disease: immune response meets the vessel wall. Annu Rev Pathol 2009 4 19 47. doi: 10.1146/annurev.pathol.3.121806.151449
25. Nazari-Jahantigh M, Wei Y, Noels H, Akhtar S, Zhou Z, Koenen RR, Heyll K, Gremse F, Kiessling F, Grommes J, Weber C, Schober A, MicroRNA-155 promotes atherosclerosis by repressing Bcl6 in macrophages. J Clin Invest 2012 122 4190 4202. doi: 10.1172/JCI61716
26. Schiopu A, Nadig SN, Cotoi OS, Hester J, van Rooijen N, Wood KJ, Inflammatory Ly-6C(hi) monocytes play an important role in the development of severe transplant arteriosclerosis in hyperlipidemic recipients. Atherosclerosis 2012 223 291 298. doi: 10.1016/j.atherosclerosis.2012.05.010
27. Schiopu A, Cotoi OS, Wood KJ, Ly-6C(hi) monocytes: a potential target for preventing transplant arteriosclerosis? Expert Rev Clin Immunol 2013 9 5 7. doi: 10.1586/eci.12.90
28. King CL, Devitt JJ, Lee TD, Hancock Friesen CL, Neutrophil mediated smooth muscle cell loss precedes allograft vasculopathy. J Cardiothorac Surg 2010 5 52. doi: 10.1186/1749-8090-5-52
29. Hagensen MK, Shim J, Falk E, Bentzon JF, Flanking recipient vasculature, not circulating progenitor cells, contributes to endothelium and smooth muscle in murine allograft vasculopathy. Arterioscler Thromb Vasc Biol 2011 31 808 813. doi: 10.1161/ATVBAHA.110.221184
30. Koch M, Mollenkopf HJ, Klemm U, Meyer TF, Induction of microRNA-155 is TLR- and type IV secretion system-dependent in macrophages and inhibits DNA-damage induced apoptosis. Proc Natl Acad Sci USA 2012 109 E1153 E1162. doi: 10.1073/pnas.1116125109
31. Schepers A, Eefting D, Bonta PI, Grimbergen JM, de Vries MR, van Weel V, de Vries CJ, Egashira K, van Bockel JH, Quax PH, Anti-MCP-1 gene therapy inhibits vascular smooth muscle cells proliferation and attenuates vein graft thickening both in vitro and in vivo. Arterioscler Thromb Vasc Biol 2006 26 2063 2069. doi: 10.1161/01.ATV.0000235694.69719.e2
32. Feil S, Hofmann F, Feil R, SM22alpha modulates vascular smooth muscle cell phenotype during atherogenesis. Circ Res 2004 94 863 865. doi: 10.1161/01.RES.0000126417.38728.F6
33. Tian XX, Kang J, Yan CH, Xu K, Tao J, Yang GT, Han YL, Purification and functional assessment of smooth muscle cells derived from mouse embryonic stem cells. J Geriatr Cardiol 2013 10 272 280. doi: 10.3969/j.issn.1671-5411.2013.03.003
34. Xiao Q, Zeng L, Zhang Z, Hu Y, Xu Q, Stem cell-derived Sca-1+ progenitors differentiate into smooth muscle cells, which is mediated by collagen IV-integrin alpha1/beta1/alphav and PDGF receptor pathways. Am J Physiol Cell Physiol 2007 292 C342 C352. doi: 10.1152/ajpcell.00341.2006