The mTOR/p70 S6K1 pathway regulates vascular smooth muscle cell differentiation

American Journal of Physiology - Cell Physiology

Volumn 286, Issue 3 55-3, 2004, Pages

  Martin, Kathleen A ^a,c   Rzucidlo, Eva M ^a,c   Merenick, Bethany L ^a   Fingar, Diane C ^b   Brown, David J ^a   Wagner, Robert J ^a   Powell, Richard J ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

Author keywords

Contractile proteins; Intimal hyperplasia; Phenotypic modulation; Rapamycin; Signal transduction

Indexed keywords

ALPHA ACTIN; CALPONIN; COLLAGEN; CONTRACTILE PROTEIN; MESSENGER RNA; MYOSIN HEAVY CHAIN; PROTEIN P21; PROTEIN P27; RAPAMYCIN; S6 KINASE; SCLEROPROTEIN; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ARTERY INTIMA PROLIFERATION; ARTICLE; CATTLE; CELL CYCLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; IMMUNOHISTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; THORACIC AORTA; VASCULAR SMOOTH MUSCLE;

ANIMALIA; BOS TAURUS; MAMMALIA;

EID: 1442325390     PISSN: 03636143     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpcell.00201.2003     Document Type: Article

References (43)

1. Braun-Dullaeus RC, Mann MJ, Seay U, Zhang L, von Der Leyen HE, Morris RE, and Dzau VJ. Cell cycle protein expression in vascular smooth muscle cells in vitro and in vivo is regulated through phosphatidylinositol 3-kinase and mammalian target of rapamycin. Arterioscler Thromb Vasc Biol 21: 1152-1158, 2001.
2. Campbell GR, Campbell JH, Manderson JA, Horrigan S, and Rennick RE. Arterial smooth muscle. A multifunctional mesenchymal cell. Arch Pathol Lab Med 112: 977-986, 1988.
3. Cao W, Mohacsi P, Shorthouse R, Pratt R, and Morris RE. Effects of rapamycin on growth factor-stimulated vascular smooth muscle cell DNA synthesis. Inhibition of basic fibroblast growth factor and platelet-derived growth factor action and antagonism of rapamycin by FK506. Transplantation 59: 390-395, 1995.
4. De Groot RP, Ballou LM, and Sasssone-Corsi P. Positive regulation of the cAMP-responsive activator CREM by the p70 S6 kinase: an alternative route to mitogen-induced gene expression. Cell 79: 81-91, 1994.
5. Fillinger MF, Sampson LN, Cronenwett JL, Powell RJ, and Wagner RJ. Co-culture of endothelial cells and smooth muscle cells in bilayer and conditioned media models. J Surg Res 67: 169-178, 1997.
6. Gagnon A, Lau S, and Sorisky A. Rapamycin-sensitive phase of 3T3-L1 preadipocyte differentiation after clonal expansion. J Cell Physiol 189: 14-22, 2001.
7. Gallo R, Padurean A, Jayaraman T, Marx S, Roque M, Adelman S, Chesebro J, Fallon J, Fuster V, Marks A, and Badimon JJ. Inhibition of intimal thickening after balloon angioplasty in porcine coronary arteries by targeting regulators of the cell cycle. Circulation 99: 2164-2170, 1999.
8. Gingras AC, Raught B, and Sonenberg N. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68: 913-963, 1999.
9. Gout I, Minami T, Hara K, Tsujishita Y, Filonenko V, Waterfirld MD, and Yonezawa K. Molecular cloning and characterization of a novel S6 kinase, p70 S6 kinase beta containing a proline-rich region. J Biol Chem 273: 30061-30064, 1998.
10. Hayashi K, Saga H, Chimori Y, Kimura K, Yamanaka Y, and Sobue K. Differentiated phenotype of smooth muscle cells depends on signaling pathways through insulin-like growth factors and phosphatidylinositol 3-kinase. J Biol Chem 273: 28860-28867, 1998,
11. Hayashi K, Takahashi M, Kimura K, Nishida W, Saga H, and Sobue K. Changes in the balance of phosphoinositide 3-kinase/protein kinase B (Akt) and the mitogen-activated protein kinases (ERK/p38MAPK) determine a phenotype of visceral and vascular smooth muscle cells. J Cell Biol 145: 727-740, 1999.
12. Hayashi K, Takahashi M, Nishida W, Yoshida K, Ohkawa Y, Kitabatake A, Aoki J, Arai H, and Sobue K. Phenotypic modulation of vascular smooth muscle cells induced by unsaturated lysophosphatidic acids. Circ Res 89: 251-258, 2001.
13. , He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, and Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 95: 2509-2514, 1998.
14. Hirschi KK, Rohovsky SA, and D'Amore PA. PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J Cell Biol 141: 805-814, 1998.
15. Jacinto E and Hall MN. Tor signalling in bugs, brain and brawn. Nat Rev Mol Cell Biol 4: 117-126, 2003.
16. Kanayasu-Toyoda T, Yamaguchi T, Uchida E, and Hayakawa T. Commitment of neutrophilic differentiation and proliferation of HL-60 cells coincides with expression of transferrin receptor. Effect of granulocyte colony stimulating factor on differentiation and proliferation. J Biol Chem 274: 25471-25480, 1999.
17. Kim JE and Chen J. Cytoplasmic-nuclear shuttling of FKBP12-rapamycin-associated protein is involved in rapamycin-sensitive signaling and translation initiation. Proc Natl Acad Sci USA 97: 14340-14345, 2000.
18. Koh H, Jee K, Lee B, Kim J, Kim D, Yun YH, Kim JW, Choi HS, and Chung J. Cloning and characterization of a nuclear S6 kinase, S6 kinase-related kinase (SRK); a novel nuclear target of Akt. Oncogene 18: 5115-5119, 1999.
19. Kuro-o M, Nagai R, Tsuchimochi H, Katoh H, Yazaki Y, Ohkubo A, and Takaku F. Developmentally regulated expression of vascular smooth muscle myosin heavy chain isoforms. J Biol Chem 264: 18272-18275, 1989.
20. Manabe I and Owens GK. CArG elements control smooth muscle subtype-specific expression of smooth muscle myosin in vivo. J Clin Invest 107: 823-834, 2001.
21. Martin KA, and Blenis J. Coordinate regulation of translation by the PI 3-kinase and mTOR pathways. In: Advances in Cancer Research, edited by Van de Woude GF and Klein G. San Diego, CA: Academic, 2002, p. 1-39.
22. Martin KA, Schalm SS, Romanelli A, Keon KL, and Blenis J. Ribosomal S6 kinase 2 inhibition by a potent C-terminal repressor domain is relieved by mitogen-activated protein-extracellular signal-regulated kinase kinase-regulated phosphorylation. J Biol Chem 276: 7892-7898, 2001.
23. Marx SO, Jayaraman T, Go LO, and Marks AR. Rapamycin-FKBP inhibits cell cycle regulators of proliferation in vascular smooth muscle cells. Circ Res 76: 412-417, 1995.
24. McCaffrey TA. TGF-betas and TGF-beta receptors in atherosclerosis. Cytokine Growth Factor Rev 11: 103-114, 2000.
25. Morice MC, Serruys PW, Sousa JE, Fajadet J, Ban Hayashi E, Perin M, Colombo A, Schuler G, Barragan P, Guagliumi G, Molnar F, and Falotico R. A randomized comparison of a sirolimus-eluting stent with a standard stent for coronary revascularization. N Engl J Med 346: 1773-1780, 2002.
26. Oh C, Kim S, Ju J, Song WK, Kim J, Yoo YJ, and Chun J. Immunosuppressant rapamycin inhibits protein kinase C alpha and p38 mitogen-activated protein kinase leading to the inhibition of chondrogenesis. Eur J Pharmacol 427: 175-185, 2001.
27. Ohkawa Y, Hayashi K, and Sobue K. Calcineurin-mediated pathway involved in the differentiated phenotype of smooth muscle cells. Biochem Biophys Res Commun 301: 78-83, 2003.
28. Peterson RT, Desai BN, Hardwick JS, and Schreiber SL. Protein phosphatase 2A interacts with the 70-kDa S6 kinase and is activated by inhibition of FKBP12-rapamycin associated protein. Proc Natl Acad Sci USA 96: 4438-4442, 1999.
29. Poon M, Marx SO, Gallo R, Badimon JJ, Taubman MB, and Marks AR. Rapamycin inhibits vascular smooth muscle cell migration. J Clin Invest 98: 2277-2283, 1996.
30. Powell RJ, Hydowski J, Frank O, Bhargava J, and Sumpio BE. Endothelial cell effect on smooth muscle cell collagen synthesis. J Surg Res 69: 113-118, 1997.
31. Reusch HP, Schaefer M, Plum C, Schultz G, and Paul M. Gbeta gamma mediates differentiation of vascular smooth muscle cells. J Biol Chem 276: 19540-19547, 2001.
32. Roque M, Cordon-Cardo C, Fuster V, Reis ED, Drobnjak M, and Badimon JJ. Modulation of apoptosis, proliferation, and p27 expression in a porcine coronary angioplasty model. Atherosclerosis 153: 315-322, 2000.
33. Schauwienold D, Plum C, Helbing T, Voigt P, Bobbert T, Hoffmann D, Paul M, and Reusch HP. ERK1/2-dependent contractile protein expression in vascular smooth muscle cells. Hypertension 41: 546-552, 2003.
34. Shah NM, Groves AK, and Anderson DJ. Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell 85: 331-343, 1996.
35. Smith RC, Branellec D, Gorski DH, Guo K, Perlman H, Dedieu JF, Pastore C, Mahfoudi A, Denefle P, Isner JM, and Walsh K. p21CIP1-mediated inhibition of cell proliferation by overexpression of the gax homeodomain gene. Genes Dev 11: 1674-1689, 1997.
36. Sobue K, Hayashi K, and Nishida W. Expressional regulation of smooth muscle cell-specific genes in association with phenotypic modulation. Mol Cell Biochem 190: 105-118, 1999,
37. Sousa JE, Costa MA, Abizaid AC, Rensing BJ, Abizaid AS, Tanajura LF, Kozuma K, Van Langenhove G, Sousa AG, Falotico R, Jaeger J, Popma JJ, and Serruys PW. Sustained suppression of neointimal proliferation by sirolimus-eluting stents: one-year angiographic and intravascular ultrasound follow-up. Circulation 104: 2007-2011, 2001.
38. Stefanovic B and Brenner DA. 5′ stem-loop of collagen alpha 1(I) mRNA inhibits translation in vitro but is required for triple helical collagen synthesis in vivo. J Biol Chem 278: 927-933, 2003.
39. Sun J, Marx SO, Chen HJ, Poon M, Marks AR, and Rabbani LE. Role for p27(Kip1) in vascular smooth muscle cell migration. Circulation 103: 2967-2972, 2001.
40. Viñals F, Chambard JC, and Pouysségur J. p70 S6 kinase-mediated protein synthesis is a critical step for vascular endothelial cell proliferation. J Biol Chem 274: 26776-26782, 1999.
41. Walsh K and Takahashi A. Transcriptional regulation of vascular smooth muscle cell phenotype. Z Kardiol 90: 12-16, 2001.
42. Yamamoto-Yamaguchi Y, Okabe-Kado J, Kasukabe T, and Honma Y. Induction of differentiation of human myeloid leukemia cells by immunosuppressant macrolides (rapamycin and FK506) and calcium/calmodulin-dependent kinase inhibitors. Exp Hematol 29: 582-588, 2001.
43. Zhu L and Skoultchi AI. Coordinating cell proliferation and differentiation. Curr Opin Genet Dev 11: 91-97, 2001.