Smooth muscle LDL receptor-related protein-1 inactivation reduces vascular reactivity and promotes injury-induced neointima formation

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 29, Issue 11, 2009, Pages 1772-1778

  Basford, Joshua E ^a   Moore, Zachary W Q ^a   Zhou, Li ^b   Herz, Joachim ^b   Hui, David Y ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

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

Author keywords

Growth factor receptor signaling; Lipoprotein receptors; Smooth muscle cell phenotype; Vasocontractility

Indexed keywords

ALPHA ACTIN; CALPONIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN KINASE B;

ADOLESCENT; ANIMAL CELL; ARTERY INTIMA PROLIFERATION; ARTICLE; ATHEROSCLEROSIS; BLOOD VESSEL INJURY; BLOOD VESSEL REACTIVITY; CAROTID ARTERY INJURY; CELL STRUCTURE; HYPERCHOLESTEROLEMIA; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; VASOCONSTRICTION;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CAROTID ARTERY INJURIES; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; IMMUNOHISTOCHEMISTRY; LDL-RECEPTOR RELATED PROTEIN 1; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PLATELET-DERIVED GROWTH FACTOR; PROBABILITY; RANDOM ALLOCATION; RECEPTORS, LDL; REFERENCE VALUES; TUNICA INTIMA; VASOCONSTRICTION;

EID: 73949126499     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.109.194357     Document Type: Article

References (30)

1. Rohlmann A, Gotthardt M, Hammer RE, Herz J. Inducible inactivation of hepatic LRP gene by Cre-mediated recombination confirms role of LRP in clearance of chylomicron remnants. J Clin Invest. 1998;101:689-695.
2. Strickland DK, Gonias SL, Argraves WS. Diverse roles for the LDL receptor family. Trends Endocrinol Metabol. 2002;13:66-74.
3. Li Y, Marzolo MP, van Kerkhof P, Strous GJ, Bu G. The YXXL motif, but not the two NPXY motifs, serves as the dominant endocytosis signal for low density lipoprotein receptor related protein. J Biol Chem. 2000; 275:17187-17194.
4. Herz J, Strickland DK. LRP: a multifunctional scavenger and signaling receptor. J Clin Invest. 2001;108:779-784.
5. Boucher P, Liu P, Gotthardt M, Hiesberger T, Anderson RGW, Herz J. Platelet-derived growth factor mediates tyrosine phosphorylation of the cytoplasmic domain of the low density lipoprotein receptor-related protein in caveolae. J Biol Chem. 2002;277:15507-15513.
6. Loukinova E, Ranganathan S, Kuznetsov S, Gorlatova N, Migliorini MM, Loukinov D, Ulery PG, Mikhailenko I, Lawrence DA, Strickland DK. Platelet-derived growth factor (PDGF)-induced tyrosine phosphorylation of the low density lipoprotein receptor-related protein (LRP). Evidence for integrated co-receptor function between LRP and the PDGF. J Biol Chem. 2002;277:15499- 15506.
7. Newton CS, Loukinova E, Mikhailenko I, Ranganathan S, Gao Y, Hau-denschild C, Strickland DK. Platelet-derived growth factor receptor-beta (PDGF-beta) activation promotes its association with the low density lipoprotein receptor-related protein (LRP). Evidence for co-receptor function. J Biol Chem. 2005;280:27872-27878.
8. Boucher P, Gotthardt M, Li WP, Anderson RGW, Herz J. LRP: Role in vascular wall integrity and protection from atherosclerosis. Science. 2003; 300:329-332.
9. Boucher P, Li WP, Matz RL, Takayama Y, Auwerx J, Anderson RGW, Herz J. LRP1 functions as an atheroprotective integrator of TGFbeta and PDGF signals in the vascular wall: implications for marfan syndrome. PLoS ONE. 2007;2:e448.
10. Cabello-Verrugio C, Brandan E. A novel modulatory mechanism of transforming growth factor-beta signaling through decorin and LRP-1. J Biol Chem. 2007;282:18842-18850.
11. Barnes H, Larsen B, Tyers M, van der Geer P. Tyrosine-phosphorylated low density lipoprotein receptor-related protein 1 (LRP1) associates with the adaptor protein SHC in SRC-transformed cells. J Biol Chem. 2001; 276:19119-19125.
12. Ishigami M, Swertfeger DK, Granholm NA, Hui DY. Apolipoprotein E inhibits platelet-derived growth factor-induced vascular smooth muscle cell migration and proliferation by suppressing signal transduction and preventing cell entry to G1 phase. J Biol Chem. 1998;273:20156-20161. (Pubitemid 28377573)
13. Swertfeger DK, Bu G, Hui DY. Low density lipoprotein receptor-related protein mediates apolipoprotein E inhibition of smooth muscle cell migration. J Biol Chem. 2002;277:4141-4146. (Pubitemid 34968674)
14. Zhu Y, Hui DY. Apolipoprotein E Binding to Low Density Lipoprotein Receptor-related Protein-1 Inhibits Cell Migration via Activation of cAMP-dependent Protein Kinase A. J Biol Chem. 2003;278:36257-36263.
15. Huang SS, Ling TY, Tseng WF, Huang YH, Tang FM, Leal SM, Huang JS. Cellular growth inhibition by IGFBP-3 and TGF-beta1 requires LRP-1. FASEB J. 2003;17:2068-2081.
16. Tseng WF, Huang SS, Huang JS. LRP-1/TbetaR-V mediates TGF-beta1-induced growth inhibition in CHO cells. FEBS Letters. 2004;562:71-78.
17. Llorente-Cortes V, Otero-Vinas M, Sanchez S, Rodriguez C, Badimon L. Low density lipoprotein upregulates low density lipoprotein receptor related protein expression in vascular smooth muscle cells. Possible involvement of sterol regulatory element binding protein 2-dependent mechanism. Circulation. 2002;106:3104-3110.
18. Lalli J, Harrer JM, Luo W, Kranias EG, Paul RJ. Targeted ablation of the phospholamban gene is associated with a marked decrease in sensitivity in aortic smooth muscle. Circ Res. 1997;80:506-513.
19. Zhu B, Kuhel DG, Witte DP, Hui DY. Apolipoprotein E inhibits neoin-timal hyperplasia after arterial injury in mice. Am J Pathol. 2000;157: 1839-1848.
20. Bochaton-Piallat ML, Clowes AW, Clowes MM, Fischer JW, Redard M, Gabbiani F, Gabbiani G. Cultured arterial smooth muscle cells maintain distinct phenotypes when implanted into carotid artery. Arterioscler Thromb Vasc Biol. 2001;21:949-954.
21. Li S, Fan YS, Chow LH, Van Den Diepstraten C, van der Veer E, Sims SM, Pickering JG. Innate diversity of adult human arterial smooth muscle cells: cloning of distinct subtypes from the internal thoracic artery. Circ Res. 2001;89:517-525.
22. Zhu B, Zhao G, Witte DP, Hui DY, Fagin JA. Targeted overexpression of IGF-1 in smooth muscle cells of transgenic mice enhances neointimal formation through increased proliferation and cell migration after intraar-terial injury. Endocrinology. 2001;142:3598-3606.
23. Kuhel DG, Zhu B, Witte DP, Hui DY. Distinction in genetic determinants for injury-induced neointimal hyperplasia and diet-induced atherosclerosis in inbred mice. Arterioscler Thromb Vasc Biol. 2002;22:955-960.
24. Shanahan CM, and Weissberg PL. Smooth muscle cell phenotypes in atherosclerotic lesions. Curr Opin Lipidol. 1999;10:507-513.
25. Liu P, Ying YS, Anderson RGW. Platelet-derived growth factor activates mitogen-activated protein kinase in isolated caveolae. Proc Natl Acad Sci U S A. 1997;94:13666-13670.
26. Takayama Y, May P, Anderson RGW, Herz J. Low density lipoprotein receptor-related protein 1 (LRP1) controls endocytosis and c-CBL-mediated ubiquitination of the platelet-derived growth factor receptor beta (PDGFbeta). J Biol Chem. 2005;280:18504-18510.
27. Wu L, Arandjelovic S, Gonias SL. Effects of low density lipoprotein receptor-related protien-1 on the expression of platelet-derived growth factor beta-receptor in vitro. J Cell Biochem. 2004;93:1169-1177.
28. Chen CN, Li i-SJ, Yeh Yt, Lee PL, Usami S, Chien S, Chiu JJ. Synergistic roles of platelet-derived growth factor-BB and interleukin-1beta in phe-notypic modulation of human aortic smooth muscle cells. Proc Natl Acad Sci U S A. 2006;103:2665-2670.
29. Hui DY. Intimal hyperplasia in murine models. Curr Drug Targets. 2008;9:251-260.
30. Zhu B, Reardon CA, Getz GS, Hui DY. Both apolipoprotein E and immune deficiency exacerbate neointimal hyperplasia after vascular injury in mice. Arterioscler Thromb Vasc Biol. 2002;22:450-455.