The cytoplasmic domain of neuropilin-1 regulates focal adhesion turnover

FEBS Letters

Volumn 587, Issue 21, 2013, Pages 3392-3399

  Seerapu, Himabindu Reddy ^a   Borthakur, Susmita ^b   Kong, Nathan ^a   Agrawal, Sudesh ^a   Drazba, Judy ^a   Vasanji, Amit ^c   Fantin, Alessandro ^d   Ruhrberg, Christiana ^d   Buck, Matthias ^b   Horowitz, Arie ^a,b  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ImageIQ   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cytoplasmic domain; Filamin A; Focal adhesion; Neuropilin 1

Indexed keywords

FILAMIN A; NEUROPILIN 1; VASCULOTROPIN;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; CYTOPLASM; ENDOTHELIUM CELL; FOCAL ADHESION; INTRACELLULAR SIGNALING; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; TURNOVER TIME; WILD TYPE;

CYTOPLASMIC DOMAIN; FILAMIN A; FOCAL ADHESION; NEUROPILIN-1;

ANIMALS; CELL ADHESION; CYTOPLASM; ENDOTHELIUM, VASCULAR; FILAMINS; FOCAL ADHESIONS; MICE; MUTATION; NEUROPILIN-1; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84886285242     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2013.08.040     Document Type: Article

References (40)

1. Q. Schwarz, and C. Ruhrberg Neuropilin, you gotta let me know: should I stay or should I go? Cell Adhes. Migr. 4 2010 61 66
2. I.C. Zachary How neuropilin-1 regulates receptor tyrosine kinase signalling: the knowns and known unknowns Biochem. Soc. Trans. 39 2011 1583 1591
3. S. Koch, S. Tugues, X. Li, L. Gualandi, and L. Claesson-Welsh Signal transduction by vascular endothelial growth factor receptors Biochem. J. 437 2011 169 183
4. Q. Pan Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth Cancer Cell 11 2007 53 67
5. Q. Pan Neuropilin-1 binds to VEGF121 and regulates endothelial cell migration and sprouting J. Biol. Chem. 282 2007 24049 24056
6. L. Wang, D. Mukhopadhyay, and X. Xu C terminus of RGS-GAIP-interacting protein conveys neuropilin-1-mediated signaling during angiogenesis FASEB J. 20 2006 1513 1515
7. L. Wang, H. Zeng, P. Wang, S. Soker, and D. Mukhopadhyay Neuropilin-1-mediated vascular permeability factor/vascular endothelial growth factor-dependent endothelial cell migration J. Biol. Chem. 278 2003 48848 48860
8. P.K. Hota, and M. Buck Plexin structures are coming: opportunities for multilevel investigations of semaphorin guidance receptors, their cell signaling mechanisms, and functions Cell. Mol. Life Sci. 69 2012 3765 3805
9. H. Cai, and R.R. Reed Cloning and characterization of neuropilin-1-interacting protein: a PSD-95/Dlg/ZO-1 domain-containing protein that interacts with the cytoplasmic domain of neuropilin-1 J. Neurosci. 19 1999 6519 6527
10. S.N. Naccache, T. Hasson, and A. Horowitz Binding of internalized receptors to the PDZ domain of GIPC/synectin recruits myosin VI to endocytic vesicles Proc. Natl. Acad. Sci. USA 103 2006 12735 12740
11. A. Lanahan The neuropilin 1 cytoplasmic domain is required for VEGF-A-dependent arteriogenesis Dev. Cell 25 2013 156 168
12. D. Hanein, and A.R. Horwitz The structure of cell-matrix adhesions: the new frontier Curr. Opin. Cell Biol. 24 2012 134 140
13. B. Wehrle-Haller Structure and function of focal adhesions Curr. Opin. Cell Biol. 24 2012 116 124
14. D.J. Sieg, C.R. Hauck, D. Ilic, C.K. Klingbeil, E. Schaefer, C.H. Damsky, and D.D. Schlaepfer FAK integrates growth-factor and integrin signals to promote cell migration Nat. Cell Biol. 2 2000 249 256
15. H.K. Avraham, T.H. Lee, Y. Koh, T.A. Kim, S. Jiang, M. Sussman, A.M. Samarel, and S. Avraham Vascular endothelial growth factor regulates focal adhesion assembly in human brain microvascular endothelial cells through activation of the focal adhesion kinase and related adhesion focal tyrosine kinase J. Biol. Chem. 278 2003 36661 36668
16. C. Ruhrberg Growing and shaping the vascular tree: multiple roles for VEGF BioEssays 25 2003 1052 1060
17. J.M. Vieira, C. Ruhrberg, and Q. Schwarz VEGF receptor signaling in vertebrate development Organogenesis 6 2010 97 106
18. Y. Xu Filamin A regulates focal adhesion disassembly and suppresses breast cancer cell migration and invasion J. Exp. Med. 207 2010 2421 2437
19. I.M. Evans, M. Yamaji, G. Britton, C. Pellet-Many, C. Lockie, I.C. Zachary, and P. Frankel Neuropilin-1 signaling through p130Cas tyrosine phosphorylation is essential for growth factor-dependent migration of glioma and endothelial cells Mol. Cell Biol. 31 2011 1174 1185
20. J.C. Kuo, X. Han, C.T. Hsiao, J.R. Yates 3rd, and C.M. Waterman Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for beta-Pix in negative regulation of focal adhesion maturation Nat. Cell Biol. 13 2011 383 393
21. F. Nakamura, T.P. Stossel, and J.H. Hartwig The filamins: organizers of cell structure and function Cell. Adhes. Migr. 5 2011 160 169
22. A.X. Zhou, J.H. Hartwig, and L.M. Akyurek Filamins in cell signaling, transcription and organ development Trends Cell Biol. 20 2010 113 123
23. E. Zamir, and B. Geiger Components of cell-matrix adhesions J. Cell Sci. 114 2001 3577 3579
24. T. Hara, K. Honda, M. Shitashige, M. Ono, H. Matsuyama, K. Naito, S. Hirohashi, and T. Yamada Mass spectrometry analysis of the native protein complex containing actinin-4 in prostate cancer cells Mol. Cell. Proteomics 6 2007 479 491
25. S.K. Maciver Myosin II function in non-muscle cells BioEssays 18 1996 179 182
26. E. Shelden, and D.A. Knecht Dictyostelium cell shape generation requires myosin II Cell Motil. Cytoskeleton 35 1996 59 67
27. H.B. Schiller, C.C. Friedel, C. Boulegue, and R. Fassler Quantitative proteomics of the integrin adhesome show a myosin II-dependent recruitment of LIM domain proteins EMBO Rep. 12 2011 259 266
28. P. Frankel, C. Pellet-Many, P. Lehtolainen, G.M. D'Abaco, M.L. Tickner, L. Cheng, and I.C. Zachary Chondroitin sulphate-modified neuropilin 1 is expressed in human tumour cells and modulates 3D invasion in the U87MG human glioblastoma cell line through a p130Cas-mediated pathway EMBO Rep. 9 2008 983 989
29. C. Pellet-Many, P. Frankel, I.M. Evans, B. Herzog, M. Junemann-Ramirez, and I.C. Zachary Neuropilin-1 mediates PDGF stimulation of vascular smooth muscle cell migration and signalling via p130Cas Biochem. J. 435 2011 609 618
30. M.T. Harte, J.D. Hildebrand, M.R. Burnham, A.H. Bouton, and J.T. Parsons P130Cas, a substrate associated with v-Src and v-Crk, localizes to focal adhesions and binds to focal adhesion kinase J. Biol. Chem. 271 1996 13649 13655
31. A. Salikhova, L. Wang, A.A. Lanahan, M. Liu, M. Simons, W.P. Leenders, D. Mukhopadhyay, and A. Horowitz Vascular endothelial growth factor and semaphorin induce neuropilin-1 endocytosis via separate pathways Circ. Res. 103 2008 e71 9
32. O. Ullrich, S. Reinsch, S. Urbe, M. Zerial, and R.G. Parton Rab11 regulates recycling through the pericentriolar recycling endosome J. Cell Biol. 135 1996 913 924
33. Y. Tu, S. Wu, X. Shi, K. Chen, and C. Wu Migfilin and Mig-2 link focal adhesions to filamin and the actin cytoskeleton and function in cell shape modulation Cell 113 2003 37 47
34. S. Soker, S. Takashima, H.Q. Miao, G. Neufeld, and M. Klagsbrun Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor Cell 92 1998 735 745
35. A. Fantin, Q. Schwarz, K. Davidson, E.M. Normando, L. Denti, and C. Ruhrberg The cytoplasmic domain of neuropilin 1 is dispensable for angiogenesis, but promotes the spatial separation of retinal arteries and veins Development 138 2011 4185 4191
36. A. Horowitz, and H.R. Seerapu Regulation of VEGF signaling by membrane traffic Cell. Signal. 24 2012 1810 1820
37. K. Ballmer-Hofer, A.E. Andersson, L.E. Ratcliffe, and P. Berger Neuropilin-1 promotes VEGFR-2 trafficking through Rab11 vesicles thereby specifying signal output Blood 118 2011 816 826
38. B. Herzog, C. Pellet-Many, G. Britton, B. Hartzoulakis, and I.C. Zachary VEGF binding to NRP1 is essential for VEGF stimulation of endothelial cell migration, complex formation between NRP1 and VEGFR2, and signaling via FAK Tyr407 phosphorylation Mol. Biol. Cell 22 2011 2766 2776
39. H.L. Goel, B. Pursell, C. Standley, K. Fogarty, and A.M. Mercurio Neuropilin-2 regulates alpha6beta1 integrin in the formation of focal adhesions and signaling J. Cell Sci. 125 2012 497 506
40. T. Seck, R. Baron, and W.C. Horne Binding of filamin to the C-terminal tail of the calcitonin receptor controls recycling J. Biol. Chem. 278 2003 10408 10416