SDF-1α induction in mature smooth muscle cells by inactivation of PTEN is a critical mediator of exacerbated injury-induced neointima formation

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 6, 2011, Pages 1300-1308

  Nemenoff, Raphael A ^a,b   Horita, Henrick ^a   Ostriker, Allison C ^a   Furgeson, Seth B ^a   Simpson, Peter A ^a   Vanputten, Vicki ^a   Crossno, Joseph ^b   Offermanns, Stefan ^c   Weiser Evans, Mary C M ^a,b  

^a Division of Renal Diseases and Hypertension   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

Author keywords

macrophages; PTEN; smooth muscle; stromal cell derived factor 1 ; vascular biology

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BETA GALACTOSIDASE; BIOLOGICAL MARKER; CRE RECOMBINASE; GREEN FLUORESCENT PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; STROMAL CELL DERIVED FACTOR 1ALPHA;

ADVENTITIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY INJURY; ARTERY INTIMA; ARTICLE; BLOOD VESSEL INJURY; BONE MARROW CELL; CELL INTERACTION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE EXACERBATION; ENZYME INACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMORAL ARTERY; INFLAMMATORY CELL; INHIBITION KINETICS; MACROPHAGE; MOUSE; NEOINTIMA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; REGULATORY MECHANISM; SMOOTH MUSCLE FIBER; WILD TYPE;

ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL PROLIFERATION; CHEMOKINE CXCL12; HEMATOPOIETIC STEM CELLS; MICE; MICE, KNOCKOUT; MYOCYTES, SMOOTH MUSCLE; NEOINTIMA; PTEN PHOSPHOHYDROLASE;

EID: 79957447572     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.223701     Document Type: Article

References (33)

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. (Pubitemid 38823766)
2. Mitra AK, Agrawal DK. In stent restenosis: bane of the stent era. J Clin Pathol. 2006;59:232-239. (Pubitemid 43344881)
3. Schober A. Chemokines in vascular dysfunction and remodeling. Arterioscler Thromb Vasc Biol. 2008;28:1950-1959.
4. Clowes AW, Reidy MA, Clowes MM. Kinetics of cellular proliferation after arterial injury. I. Smooth muscle growth in the absence of endothelium. Lab Invest. 1983;49:327-333. (Pubitemid 13012062)
5. Imai H, Lee KJ, Lee SK, Lee KT, O'Neal RM, Thomas WA. Ultrastructural features of aortic cells in mitosis in control and cholesterol-fed swine. Lab Invest. 1970;23:401-415.
6. Schwartz SM, Stemerman MB, Benditt EP. The aortic intima: II: repair of the aortic lining after mechanical denudation. Am J Pathol. 1975;81: 15-42.
7. 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. (Pubitemid 34407037)
8. 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. (Pubitemid 37288674)
9. 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. 30:1890-1896.
10. Hoofnagle MH, Thomas JA, Wamhoff BR, Owens GK. Origin of neointimal smooth muscle: we've come full circle. Arterioscler Thromb Vasc Biol. 2006;26:2579-2581.
11. 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. 122:2048-2057.
12. Bentzon JF, Weile C, Sondergaard CS, Hindkjaer J, Kassem M, Falk E. Smooth muscle cells in atherosclerosis originate from the local vessel wall and not circulating progenitor cells in ApoE knockout mice. Arterioscler Thromb Vasc Biol. 2006;26:2696-2702.
13. Tamguney T, Stokoe D. New insights into PTEN. J Cell Sci. 2007;120: 4071-4079.
14. Knobbe CB, Lapin V, Suzuki A, Mak TW. The roles of PTEN in development, physiology and tumorigenesis in mouse models: a tissueby-tissue survey. Oncogene. 2008;27:5398-5415.
15. Leslie NR, Downes CP. PTEN function: how normal cells control it and tumour cells lose it. Biochem J. 2004;382:1-11. (Pubitemid 39141560)
16. Leslie NR, Batty IH, Maccario H, Davidson L, Downes CP. Understanding PTEN regulation: PIP2, polarity and protein stability. Oncogene. 2008;27:5464-5476.
17. Cohen RA, Tong X. Vascular oxidative stress: the common link in hypertensive and diabetic vascular disease. J Cardiovasc Pharmacol. 55:308-316.
18. Furgeson SB, Simpson PA, Park I, Vanputten V, Horita H, Kontos CD, Nemenoff RA, Weiser-Evans MC. Inactivation of the tumour suppressor, PTEN, in smooth muscle promotes a pro-inflammatory phenotype and enhances neointima formation. Cardiovasc Res. 86:274-282.
19. Huang J, Niu XL, Pippen AM, Annex BH, Kontos CD. Adenovirusmediated intraarterial delivery of PTEN inhibits neointimal hyperplasia. Arterioscler Thromb Vasc Biol. 2005;25:354-358. (Pubitemid 40189157)
20. Koide S, Okazaki M, Tamura M, Ozumi K, Takatsu H, Kamezaki F, Tanimoto A, Tasaki H, Sasaguri Y, Nakashima Y, Otsuji Y. PTEN reduces cuff-induced neointima formation and proinflammatory cytokines. Am J Physiol Heart Circ Physiol. 2007;292:H2824-H2831. (Pubitemid 47084532)
21. Mitra AK, Jia G, Gangahar DM, Agrawal DK. Temporal PTEN inactivation causes proliferation of saphenous vein smooth muscle cells of human CABG conduits. J Cell Mol Med. 2009;13:177-187.
22. Nemenoff RA, Simpson PA, Furgeson SB, Kaplan-Albuquerque N, Crossno J, Garl PJ, Cooper J, Weiser-Evans MC. Targeted deletion of PTEN in smooth muscle cells results in vascular remodeling and recruitment of progenitor cells through induction of stromal cell-derived factor-1-. Circ Res. 2008;102:1036-1045. (Pubitemid 351667857)
23. Karshovska E, Zernecke A, Sevilmis G, Millet A, Hristov M, Cohen CD, Schmid H, Krotz F, Sohn HY, Klauss V, Weber C, Schober A. Expression of HIF-1 in injured arteries controls SDF-1 mediated neointima formation in apolipoprotein E deficient mice. Arterioscler Thromb Vasc Biol. 2007;27:2540-2547. (Pubitemid 350158903)
24. Sakihama H, Masunaga T, Yamashita K, Hashimoto T, Inobe M, Todo S, Uede T. Stromal cell-derived factor-1 and CXCR4 interaction is critical for development of transplant arteriosclerosis. Circulation. 2004;110: 2924-2930. (Pubitemid 39473619)
25. Schober A, Knarren S, Lietz M, Lin EA, Weber C. Crucial role of stromal cell-derived factor-1 in neointima formation after vascular injury in apolipoprotein E-deficient mice. Circulation. 2003;108:2491-2497. (Pubitemid 37444411)
26. Zernecke A, Schober A, Bot I, von Hundelshausen P, Liehn EA, Mopps B, Mericskay M, Gierschik P, Biessen EA, Weber C. SDF-1CXCR4 axis is instrumental in neointimal hyperplasia and recruitment of smooth muscle progenitor cells. Circ Res. 2005;96:784-791. (Pubitemid 40559518)
27. Suzuki A, Yamaguchi MT, Ohteki T, Sasaki T, Kaisho T, Kimura Y, Yoshida R, Wakeham A, Higuchi T, Fukumoto M, Tsubata T, Ohashi PS, Koyasu S, Penninger JM, Nakano T, Mak TW. T cell-specific loss of Pten leads to defects in central and peripheral tolerance. Immunity. 2001;14:523-534. (Pubitemid 32520864)
28. Wirth A, Benyo Z, Lukasova M, Leutgeb B, Wettschureck N, Gorbey S, Orsy P, Horvath B, Maser-Gluth C, Greiner E, Lemmer B, Schutz G, Gutkind JS, Offermanns S. G12-G13-LARG-mediated signaling in vascular smooth muscle is required for salt-induced hypertension. Nat Med. 2008;14:64-68.
29. 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.
30. Weiser-Evans MC, Wang XQ, Amin J, Van Putten V, Choudhary R, Winn RA, Scheinman R, Simpson P, Geraci MW, Nemenoff RA. Depletion of cytosolic phospholipase A2 in bone marrow-derived macrophages protects against lung cancer progression and metastasis. Cancer Res. 2009;69:1733-1738.
31. Libby P, Schwartz D, Brogi E, Tanaka H, Clinton SK. A cascade model for restenosis: a special case of atherosclerosis progression. Circulation. 1992;86:III47-III52.
32. Moreno PR, Bernardi VH, Lopez-Cuellar J, Newell JB, McMellon C, Gold HK, Palacios IF, Fuster V, Fallon JT. Macrophage infiltration predicts restenosis after coronary intervention in patients with unstable angina. Circulation. 1996;94:3098-3102. (Pubitemid 26427473)
33. Li SL, Reddy MA, Cai Q, Meng L, Yuan H, Lanting L, Natarajan R. Enhanced proatherogenic responses in macrophages and vascular smooth muscle cells derived from diabetic db/db mice. Diabetes. 2006;55: 2611-2619. (Pubitemid 44871163)