LRP1-Dependent endocytic mechanism governs the signaling output of the bmp system in endothelial cells and in angiogenesis

Circulation Research

Volumn 111, Issue 5, 2012, Pages 564-574

  Pi, Xinchun ^a   Schmitt, Christopher E ^a,d   Xie, Liang ^a   Portbury, Andrea L ^a   Wu, Yaxu ^a   Lockyer, Pamela ^a   Dyer, Laura A ^a   Moser, Martin ^b   Bu, Guojun ^c   Flynn, Edward J ^a,d   Jin, Suk Won ^a,d,e   Patterson, Cam ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FREIBURG   (Germany)

^c MAYO GRADUATE SCHOOL   (United States)

^d UNIVERSITY OF NORTH CAROLINA   (United States)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

angiogenesis; bone morphogenetic protein; endocytosis; endothelial cell; low density lipoprotein receptor related protein 1

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CARDIOVASCULAR DEVELOPMENT; CELL MIGRATION; CONTROLLED STUDY; CYTOLOGY; DEVELOPMENT; ENDOCYTOSIS; ENDOTHELIUM CELL; INTRACELLULAR SIGNALING; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; ZEBRA FISH;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; CARRIER PROTEINS; CELL LINE; CELL MOVEMENT; ENDOCYTOSIS; ENDOTHELIAL CELLS; HEK293 CELLS; HUMANS; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; PHENOTYPE; RECEPTORS, LDL; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84865485770     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.112.274597     Document Type: Article

References (30)

1. Lowery JW, de Caestecker MP. BMP signaling in vascular development and disease. Cytokine Growth Factor Rev. 2010;21:287-298.
2. Umulis D, O'Connor MB, Blair SS. The extracellular regulation of bone morphogenetic protein signaling. Development. 2009;136:3715-3728.
3. Heinke J, Wehofsits L, Zhou Q, Zoeller C, Baar KM, Helbing T, Laib A, Augustin H, Bode C, Patterson C, Moser M. BMPER is an endothelial cell regulator and controls bone morphogenetic protein-4-dependent angiogenesis. Circ Res. 2008;103:804-812.
4. Moser M, Binder O, Wu Y, Aitsebaomo J, Ren R, Bode C, Bautch VL, Conlon FL, Patterson C. BMPER, a novel endothelial cell precursorderived protein, antagonizes bone morphogenetic protein signaling and endothelial cell differentiation. Mol Cell Biol. 2003;23:5664-5679. (Pubitemid 36951331)
5. Moser M, Yu Q, Bode C, Xiong JW, Patterson C. BMPER is a conserved regulator of hematopoietic and vascular development in zebrafish. J Mol Cell Cardiol. 2007;43:243-253. (Pubitemid 47304444)
6. Moreno-Miralles I, Ren R, Moser M, Hartnett ME, Patterson C. Bone morphogenetic protein endothelial cell precursor-derived regulator regulates retinal angiogenesis in vivo in a mouse model of oxygen-induced retinopathy. Arterioscler Thromb Vasc Biol. 2011;31:2216-2222.
7. Kelley R, Ren R, Pi X, Wu Y, Moreno I, Willis M, Moser M, Ross M, Podkowa M, Attisano L, Patterson C. A concentration-dependent endocytic trap and sink mechanism converts Bmper from an activator to an inhibitor of Bmp signaling. J Cell Biol. 2009;184:597-609.
8. Bu G, Geuze HJ, Strous GJ, Schwartz AL. 39 kDa receptor-associated protein is an ER resident protein and molecular chaperone for LDL receptor-related protein. EMBO J. 1995;14:2269-2280.
9. Xia Z, Liu Y. Reliable and global measurement of fluorescence resonance energy transfer using fluorescence microscopes. Biophys J. 2001;81: 2395-2402. (Pubitemid 32917186)
10. Pi X, Ren R, Kelley R, Zhang C, Moser M, Bohil AB, Divito M, Cheney RE, Patterson C. Sequential roles for myosin-X in BMP6-dependent filopodial extension, migration, and activation of BMP receptors. J Cell Biol. 2007;179:1569-1582.
11. Nasevicius A, Ekker SC. Effective targeted gene 'knockdown' in zebrafish. Nat Genet. 2000;26:216-220.
12. Wiley DM, Kim JD, Hao J, Hong CC, Bautch VL, Jin SW. Distinct signalling pathways regulate sprouting angiogenesis from the dorsal aorta and the axial vein. Nat Cell Biol. 2011;13:687-693.
13. Zhang JL, Qiu LY, Kotzsch A, Weidauer S, Patterson L, Hammerschmidt M, Sebald W, Mueller TD. Crystal structure analysis reveals how the Chordin family member crossveinless 2 blocks BMP-2 receptor binding. Dev Cell. 2008;14:739-750. (Pubitemid 351622617)
14. Lillis AP, Van Duyn LB, Murphy-Ullrich JE, Strickland DK. LDL receptor-related protein 1: unique tissue-specific functions revealed by selective gene knockout studies. Physiol Rev. 2008;88:887-918.
15. Obermoeller-McCormick LM, Li Y, Osaka H, FitzGerald DJ, Schwartz AL, Bu G. Dissection of receptor folding and ligand-binding property with functional minireceptors of LDL receptor-related protein. J Cell Sci. 2001;114:899-908. (Pubitemid 32266261)
16. Lillis AP, Mikhailenko I, Strickland DK. Beyond endocytosis: LRP function in cell migration, proliferation and vascular permeability. J Thromb Haemost. 2005;3:1884-1893. (Pubitemid 41716576)
17. Liu Q, Huang SS, Huang JS. Function of the type V transforming growth factor beta receptor in transforming growth factor beta-induced growth inhibition of mink lung epithelial cells. J Biol Chem. 1997;272: 18891-18895. (Pubitemid 27318240)
18. May P, Rohlmann A, Bock HH, Zurhove K, Marth JD, Schomburg ED, Noebels JL, Beffert U, Sweatt JD, Weeber EJ, Herz J. Neuronal LRP1 functionally associates with postsynaptic proteins and is required for normal motor function in mice. Mol Cell Biol. 2004;24:8872-8883. (Pubitemid 39313893)
19. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell. 2003;113:685-700. (Pubitemid 36724933)
20. Massague J. TGF-beta signal transduction. Annu Rev Biochem. 1998;67: 753-791.
21. Southwood M, Jeffery TK, Yang X, Upton PD, Hall SM, Atkinson C, Haworth SG, Stewart S, Reynolds PN, Long L, Trembath RC, Morrell NW. Regulation of bone morphogenetic protein signalling in human pulmonary vascular development. J Pathol. 2008;214:85-95.
22. Robu ME, Larson JD, Nasevicius A, Beiraghi S, Brenner C, Farber SA, Ekker SC. p53 activation by knockdown technologies. PLoS Genet. 2007;3:e78.
23. Rentzsch F, Zhang J, Kramer C, Sebald W, Hammerschmidt M. Crossveinless 2 is an essential positive feedback regulator of Bmp signaling during zebrafish gastrulation. Development. 2006;133:801-811.
24. Di Fiore PP, De Camilli P. Endocytosis and signaling: an inseparable partnership. Cell. 2001;106:1-4. (Pubitemid 32709950)
25. O'Connor MB, Umulis D, Othmer HG, Blair SS. Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development. 2006;133:183-193. (Pubitemid 43210708)
26. Serpe M, Umulis D, Ralston A, Chen J, Olson DJ, Avanesov A, Othmer H, O'Connor MB, Blair SS. The BMP-binding protein Crossveinless 2 is a short-range, concentration-dependent, biphasic modulator of BMP signaling in Drosophila. Dev Cell. 2008;14:940-953. (Pubitemid 351757202)
27. Yao Y, Jumabay M, Ly A, Radparvar M, Wang AH, Abdmaulen R, Bostrom KI. Crossveinless 2 regulates bone morphogenetic protein 9 in human and mouse vascular endothelium. Blood. 2012;119:5037-5047.
28. van Kerkhof P, Lee J, McCormick L, Tetrault E, Lu W, Schoenfish M, Oorschot V, Strous GJ, Klumperman J, Bu G. Sorting nexin 17 facilitates LRP recycling in the early endosome. EMBO J. 2005;24:2851-2861. (Pubitemid 43079889)
29. Li Y, van Kerkhof P, Marzolo MP, Strous GJ, Bu G. Identification of a major cyclic AMP-dependent protein kinase A phosphorylation site within the cytoplasmic tail of the low-density lipoprotein receptor-related protein: implication for receptor-mediated endocytosis. Mol Cell Biol. 2001;21:1185-1195. (Pubitemid 32114967)
30. Hartung A, Bitton-Worms K, Rechtman MM, Wenzel V, Boergermann JH, Hassel S, Henis YI, Knaus P. Different routes of bone morphogenic protein (BMP) receptor endocytosis influence BMP signaling. Mol Cell Biol. 2006;26:7791-7805. (Pubitemid 44547724)