Bone marrow-derived cells contribute to vascular inflammation but do not differentiate into smooth muscle cell lineages

Circulation

Volumn 122, Issue 20, 2010, Pages 2048-2057

  Iwata, Hiroshi ^a   Manabe, Ichiro ^a,b,c   Fujiu, Katsuhito ^a   Yamamoto, Tetsufumi ^a   Takeda, Norifumi ^a   Eguchi, Kosei ^a   Furuya, Akiko ^d   Kuro O, Makoto ^e   Sata, Masataka ^f   Nagai, Ryozo ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b Global COE Program   (United States)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d KYOWA HAKKO KOGYO CO LTD   (Japan)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^f UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

inflammation; monocytes; muscle, smooth; progenitor cells

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; APOLIPOPROTEIN E; CD11B ANTIGEN; MYOSIN; MYOSIN HEAVY CHAIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY INJURY; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; GENE EXPRESSION; HEART TRANSPLANTATION; INTIMA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; VASCULAR DISEASE; VASCULAR LESION; VASCULITIS;

ANIMALS; ANTIGENS, DIFFERENTIATION; APOLIPOPROTEINS E; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; HEART TRANSPLANTATION; HUMANS; INFLAMMATION; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; TRANSPLANTATION, HOMOLOGOUS; VASCULITIS;

EID: 78549283415     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.110.965202     Document Type: Article

References (38)

1. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev. 2004;84:767-801.
2. Manabe I, Nagai R. Regulation of smooth muscle phenotype. Curr Atheroscler Rep. 2003;5:214-222.
3. Remy-Martin JP, Marandin A, Challier B, Bernard G, Deschaseaux M, Herve P, Wei Y, Tsuji T, Auerbach R, Dennis JE, Moore KA, Green-berger JS, Charbord P. Vascular smooth muscle differentiation of murine stroma: a sequential model. Exp Hematol. 1999;27:1782-1795.
4. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med. 2002;8:403-409.
5. Simper D, Stalboerger PG, Panetta CJ, Wang S, Caplice NM. Smooth muscle progenitor cells in human blood. Circulation. 2002;106: 1199-1204.
6. Hoofnagle MH, Thomas JA, Wamhoff BR, Owens GK. Origin of neo-intimal smooth muscle: we've come full circle. Arterioscler Thromb Vasc Biol. 2006;26:2579-2581.
7. Regan CP, Manabe I, Owens GK. Development of a smooth muscle-targeted cre recombinase mouse reveals novel insights regarding smooth muscle myosin heavy chain promoter regulation. Circ Res. 2000;87: 363-369.
8. Nagai R, Larson DM, Periasamy M. Characterization of a mammalian smooth muscle myosin heavy chain cDNA clone and its expression in various smooth muscle types. Proc Natl Acad Sci USA. 1988;85:1047-1051.
9. Nakano Y, Nishihara T, Sasayama S, Miwa T, Kamada S, Kakunaga T. Transcriptional regulatory elements in the 5' upstream and first intron regions of the human smooth muscle (aortic type) alpha-actin-encoding gene. Gene. 1991;99:285-289.
10. Morano I, Chai GX, Baltas LG, Lamounier-Zepter V, Lutsch G, Kott M, Haase H, Bader M. Smooth-muscle contraction without smooth-muscle myosin. Nat Cell Biol. 2000;2:371-375.
11. Tanaka K, Sata M, Hirata Y, Nagai R. Diverse contribution of bone marrow cells to neointimal hyperplasia after mechanical vascular injuries. Circ Res. 2003;93:783-790.
12. Fujiu K, Manabe I, Ishihara A, Oishi Y, Iwata H, Nishimura G, Shindo T, Maemura K, Kagechika H, Shudo K, Nagai R. Synthetic retinoid Am80 suppresses smooth muscle phenotypic modulation and in-stent neointima formation by inhibiting KLF5. Circ Res. 2005;97:1132-1141.
13. Yin F, Herring BP. GATA-6 can act as a positive or negative regulator of smooth muscle-specific gene expression. J Biol Chem. 2005;280: 4745-4752.
14. Zovein AC, Hofmann JJ, Lynch M, French WJ, Turlo KA, Yang Y, Becker MS, Zanetta L, Dejana E, Gasson JC, Tallquist MD, Iruela-Arispe ML. Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell. 2008;3:625-636.
15. Miano JM, Kitchen CM, Chen J, Maltby KM, Kelly LA, Weiler H, Krahe R, Ashworth LK, Garcia E. Expression of human smooth muscle calponin in transgenic mice revealed with a bacterial artificial chromosome. Am J Physiol Heart Circ Physiol. 2002;282:H1793-H1803.
16. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. "Green mice" as a source of ubiquitous green cells. FEBS Lett. 1997;407: 313-319.
17. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K. Development of monocytes, macrophages, and dendritic cells. Science. 2010;327:656-661.
18. Jabs A, Okamoto E, Vinten-Johansen J, Bauriedel G, Wilcox JN. Sequential patterns of chemokine-and chemokine receptor-synthesis following vessel wall injury in porcine coronary arteries. Atherosclerosis. 2007;192:75-84.
19. Schwartz SM, Virmani R, Rosenfeld ME. The good smooth muscle cells in atherosclerosis. Curr Atheroscler Rep. 2000;2:422-429.
20. Auffray C, Sieweke MH, Geissmann F. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu Rev Immunol. 2009;27:669-692.
21. Manabe I, Owens GK. CArG elements control smooth muscle subtype specific expression of smooth muscle myosin in vivo. J Clin Invest. 2001;107:823-834.
22. McDonald OG, Owens GK. Programming smooth muscle plasticity with chromatin dynamics. Circ Res. 2007;100:1428-1441.
23. Orlandi A, Bennett M. Progenitor cell-derived smooth muscle cells in vascular disease. Biochem Pharmacol. 2010;79:1706-1713.
24. Feil S, Hofmann F, Feil R. SM22{alpha} modulates vascular smooth muscle cell phenotype during atherogenesis. Circ Res. 2004;94: 863-865.
25. George J, Afek A, Abashidze A, Shmilovich H, Deutsch V, Kopolovich J, Miller H, Keren G. Transfer of endothelial progenitor and bone marrow cells influences atherosclerotic plaque size and composition in apoli-poprotein E knockout mice. Arterioscler Thromb Vasc Biol. 2005;25: 2636-2641.
26. Bellini A, Mattoli S. The role of the fibrocyte, a bone marrow-derived mesenchymal progenitor, in reactive and reparative fibroses. Lab Invest. 2007;87:858-870.
27. Bronstein I, Voyta JC, Murphy OJ, Bresnick L, Kricka LJ. Improved chemiluminescent western blotting procedure. BioTechniques. 1992;12:748-753.
28. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. 'Green mice' as a source of ubiquitous green cells. FEBS Lett. 1997;407:313-319.
29. Morano I, Chai GX, Baltas LG, Lamounier-Zepter V, Lutsch G, Kott M, Haase H, Bader M. Smooth-muscle contraction without smooth-muscle myosin. Nat Cell Biol. 2000;2:371-375.
30. Nakano Y, Nishihara T, Sasayama S, Miwa T, Kamada S, Kakunaga T. Transcriptional regulatory elements in the 5' upstream and first intron regions of the human smooth muscle (aortic type) alpha-actin-encoding gene. Gene. 1991;99:285-289.
31. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med. 2002;8:403-409.
32. Sata M, Maejima Y, Adachi F, Fukino K, Saiura A, Sugiura S, Aoyagi T, Imai Y, Kurihara H, Kimura K, Omata M, Makuuchi M, Hirata Y, Nagai R. A mouse model of vascular injury that induces rapid onset of medial cell apoptosis followed by reproducible neointimal hyperplasia. J Mol Cell Cardiol. 2000;32:2097-2104.
33. Sata M, Nishimatsu H, Suzuki E, Sugiura S, Yoshizumi M, Ouchi Y, Hirata Y, Nagai R. Endothelial nitric oxide synthase is essential for the HMG-CoA reductase inhibitor cerivastatin to promote collateral growth in response to ischemia. FASEB J. 2001;15:2530-2532.
34. Sata M, Tanaka K, Ishizaka N, Hirata Y, Nagai R. Absence of p53 leads to accelerated neointimal hyperplasia after vascular injury. Arterioscler Thromb Vasc Biol. 2003;23:1548-1552.
35. Perlman H, Sata M, Le Roux A, Sedlak TW, Branellec D, Walsh K. Bax-mediated cell death by the Gax homeoprotein requires mitogen activation but is independent of cell cycle activity. EMBO J. 1998;17:3576-3586.
36. Emmert-Buck MR, Bonner RF, Smith PD, Chuaqui RF, Zhuang Z, Goldstein SR, Weiss RA, Liotta LA. Laser capture microdissection. Science. 1996;274:998-1001.
37. Geisterfer AA, Peach MJ, Owens GK. Angiotensin II induces hypertrophy, not hyperplasia, of cultured rat aortic smooth muscle cells. Circ Res. 1988;62:749-756.
38. Lynn Ray J, Leach R, Herbert J-M, Benson M. Isolation of vascular smooth muscle cells from a single murine aorta. Methods Cell Sci. 2001;23:185-188.