Neuropilin-1 mediates vascular permeability independently of vascular endothelial growth factor receptor-2 activation

Science Signaling

Volumn 9, Issue 425, 2016, Pages

  Roth, Lise ^a,b   Prahst, Claudia ^a,d   Ruckdeschel, Tina ^a   Savant, Soniya ^a,e   Weström, Simone ^a,f   Fantin, Alessandro ^c   Riedel, Maria ^a   Héroult, Mélanie ^a,g   Ruhrberg, Christiana ^c   Augustin, Hellmut G ^a,b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^e KAROLINSKA INSTITUTE   (Sweden)

^f UPPSALA UNIVERSITY   (Sweden)

^g BAYER AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CENDR PEPTIDE; ISOPROTEIN; NEUROPILIN 1; PEPTIDE; SEMAPHORIN 3A; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2; VEGFA PROTEIN, HUMAN;

ANGIOGENESIS; ARTICLE; BINDING AFFINITY; BIOCHEMICAL ANALYSIS; BLOOD VESSEL PERMEABILITY; CARBOXY TERMINAL SEQUENCE; CELL CONTACT; CELL MEMBRANE PERMEABILITY; CELL SURFACE; ENDOTHELIUM CELL; ENZYME ACTIVITY; FLOW CYTOMETRY; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN MOTIF; WESTERN BLOTTING; ANIMAL; CAPILLARY PERMEABILITY; CELL COMMUNICATION; CELL CULTURE; CHEMISTRY; CYTOLOGY; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN DOMAIN; REAL TIME POLYMERASE CHAIN REACTION; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; BLOTTING, WESTERN; CAPILLARY PERMEABILITY; CELL COMMUNICATION; CELLS, CULTURED; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNOPRECIPITATION; MICE; NEUROPILIN-1; PROTEIN DOMAINS; REAL-TIME POLYMERASE CHAIN REACTION; SEMAPHORIN-3A; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84964714754     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aad3812     Document Type: Article

References (59)

1. S. Takagi, T. Tsuji, T. Amagai, T. Takamatsu, H. Fujisawa, Specific cell surface labels in the visual centers of Xenopus laevis tadpole identified using monoclonal antibodies. Dev. Biol. 122, 90-100 (1987).
2. Z. He, M. Tessier-Lavigne, Neuropilin is a receptor for the axonal chemorepellent semaphorin III. Cell 90, 739-751 (1997).
3. S. Takagi, Y. Kasuya, M. Shimizu, T. Matsuura, M. Tsuboi, A. Kawakami, H. Fujisawa, Expression of a cell adhesion molecule, neuropilin, in the developing chick nervous system. Dev. Biol. 170, 207-222 (1995).
4. T. Kitsukawa, M. Shimizu, M. Sanbo, T. Hirata, M. Taniguchi, Y. Bekku, T. Yagi, H. Fujisawa, Neuropilin-Semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19, 995-1005 (1997).
5. A. L. Kolodkin, D. V. Levengood, E. G. Rowe, Y.-T. Tai, R. J. Giger, D. D. Ginty, Neuropilin is a semaphorin III receptor. Cell 90, 753-762 (1997).
6. S. Soker, S. Takashima, H. Q. Miao, G. Neufeld, M. Klagsbrun, Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92, 735-745 (1998).
7. T. Kawasaki, T. Kitsukawa, Y. Bekku, Y. Matsuda, M. Sanbo, T. Yagi, H. Fuisawa, A requirement for neuropilin-1 in embryonic vessel formation. Development 126, 4895-4902 (1999).
8. T. Kitsukawa, A. Shimono, A. Kawakami, H. Kondoh, H. Fujisawa, Overexpression of a membrane protein, neuropilin, in chimeric mice causes anomalies in the cardiovascular system, nervous system and limbs. Development 121, 4309-4318 (1995).
9. H. Chen, Z. He, A. Bagri, M. Tessier-Lavigne, Semaphorin-neuropilin interactions underlying sympathetic axon responses to class III semaphorins. Neuron 21, 1283-1290 (1998).
10. F. Nakamura, M. Tanaka, T. Takahashi, R. G. Kalb, S. M. Strittmatter, Neuropilin-1 extracellular domains mediate semaphorin D/III-induced growth cone collapse. Neuron 21, 1093-1100 (1998).
11. L. Roth, C. Nasarre, S. Dirrig-Grosch, D. Aunis, G. Crémel, P. Hubert, D. Bagnard, Transmembrane domain interactions control biological functions of neuropilin-1. Mol. Biol. Cell 19, 646-654 (2008).
12. H. Cai, 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, 6519-6527 (1999).
13. A. Lanahan X. Zhang, A. Fantin, Z. Zhuang, F. Rivera-Molina, K. Speichinger, C. Prahst, J. Zhang, Y. Wang, G. Davis, D. Toomre, C. Ruhrberg, M. Simons, The neuropilin 1 cytoplasmic domain is required for VEGF-A-dependent arteriogenesis. Dev. Cell 25, 156-168 (2013).
14. S. Soker, H.-Q. Miao, M. Nomi, S. Takashima, M. Klagsbrun, VEGF165 mediates formation of complexes containing VEGFR-2 and neuropilin-1 that enhance VEGF165- receptor binding. J. Cell. Biochem. 85, 357-368 (2002).
15. C. Prahst, M. Héroult, A. A. Lanahan, N. Uziel, O. Kessler, N. Shraga-Heled, M. Simons, G. Neufeld, H. G. Augustin, Neuropilin-1-VEGFR-2 complexing requires the PDZ-binding domain of neuropilin-1. J. Biol. Chem. 283, 25110-25114 (2008).
16. D. R. Senger, S. J. Galli, A. M. Dvorak, A. Perruzi, V.S. Harvey, F. F. Dvorak, Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219, 983-985 (1983).
17. B. P. Eliceiri, R. Paul, P. L. Schwartzberg, J. D. Hood, J. Leng, D. A. Cheresh, Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol. Cell 4, 915-924 (1999).
18. M. T. Chou, J. Wang, D. J. Fujita, Src kinase becomes preferentially associated with the VEGFR, KDR/Flk-1, following VEGF stimulation of vascular endothelial cells. BMC Biochem. 3, 32 (2002).
19. Y. Wallez, F. Cand, F. Cruzalegui, C. Wernstedt, S. Souchelnytskyi, I Vilgrain, P. Huber, Src kinase phosphorylates vascular endothelial-cadherin in response to vascular endothelial growth factor: Identification of tyrosine 685 as the unique target site. Oncogene 26, 1067-1077 (2006).
20. X. L. Chen, J.-O. Nam, C. Jean, C. Lawson, C. T. Walsh, E. Goka, S.-T. Lim, A. Tomar, I. Tancioni, S. Uryu, J.-L. Guan, L. M. Acevedo, S. M.Weis, D. A. Cheresh, D. D. Schlaepfer, VEGF-induced vascular permeability is mediated by FAK. Dev. Cell 22, 146-157 (2012).
21. Z. Sun, X. Li, S. Massena, S. Kutschera, N. Padhan, L. Gualandi, V. Sundvold-Gjerstad, K. Gustafsson, W. W. Choy, G. Zang, M. Quach, L. Jansson, M. Phillipson, M. R. Abid, A. Spurkland, L. Claesson-Welsh, VEGFR2 induces c-Src signaling and vascular permeability in vivo via the adaptor protein TSAd. J. Exp. Med. 209, 1363-1377 (2012).
22. C. Jean, X. L. Chen, J.-O. Nam, I. Tancioni, S. Uryu, C. Lawson, K. K. Ward, C. T.Walsh, N. L. Miller,M. Ghassemian, P. Turowski, E. Dejana, S.Weis, D. A. Cheresh, D. D. Schlaepfer, Inhibition of endothelial FAK activity prevents tumor metastasis by enhancing barrier function. J. Cell Biol. 204, 247-263 (2014).
23. N. Lambeng, Y. Wallez, C. Rampon, F. Cand, G. Christé, D. Gulino-Debrac, I. Vilgrain, P. Huber, Vascular endothelial-cadherin tyrosine phosphorylation in angiogenic and quiescent adult tissues. Circ. Res. 96, 384-391 (2005).
24. J. Gavard, J. S. Gutkind, VEGF controls endothelial-cell permeability by promoting the b-arrestin-dependent endocytosis of VE-cadherin. Nat. Cell Biol. 8, 1223-1234 (2006).
25. D. Feng, J. A. Nagy, J. Hipp, H. F. Dvorak, A. M. Dvorak, Vesiculo-vacuolar organelles and the regulation of venule permeability to macromolecules by vascular permeability factor, histamine, and serotonin. J. Exp. Med. 183, 1981-1986 (1996).
26. S. A. Stacker, A. Vitali, C. Caesar, T. Domagala, L. C. Groenen, E. Nice, M. G. Achen, A. F. Wilks, A mutant form of vascular endothelial growth factor (VEGF) that lacks VEGF receptor-2 activation retains the ability to induce vascular permeability. J. Biol. Chem. 274, 34884-34892 (1999).
27. P. M. Becker, J.Waltenberger, R. Yachechko, T. Mirzapoiazova, J. S. K. Sham, C. G. Lee, J. A. Elias, A. D. Verin, Neuropilin-1 regulates vascular endothelial growth factor-mediated endothelial permeability. Circ. Res. 96, 1257-1265 (2005).
28. R. Mamluk, M. Klagsbrun, M. Detmar, D. R. Bielenberg, Soluble neuropilin targeted to the skin inhibits vascular permeability. Angiogenesis 8, 217-227 (2005).
29. T. Teesalu, K. N. Sugahara, V. R. Kotamraju, E. Ruoslahti, C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration. Proc. Natl. Acad. Sci. U.S.A. 106, 16157-16162 (2009).
30. K. N. Sugahara, T. Teesalu, P. P. Karmali, V. R. Kotamraju, L. Agemy, D. R. Greenwald, E. Ruoslahti, Coadministration of a tumor-penetrating peptide enhances the efficacy of cancer drugs. Science 328, 1031-1035 (2010).
31. H.-B. Pang, G. B. Braun, T. Friman, P. Aza-Blanc, M. E. Ruidiaz, K. N. Sugahara, T. Teesalu, E. Ruoslahti, An endocytosis pathway initiated through neuropilin-1 and regulated by nutrient availability. Nat. Commun. 5, 4904 (2014).
32. H. Gitay-Goren, T. Cohen, S. Tessler, S. Soker, S. Gengrinovitch, P. Rockwell, M. Klagsbrun, B.-Z. Levi, G. Neufeld, Selective binding of VEGF121 to one of the three vascular endothelial growth factor receptors of vascular endothelial cells. J. Biol. Chem. 271, 5519-5523 (1996).
33. M. W. Parker, P. Xu, X. Li, C. W. Vander Kooi, Structural basis for selective vascular endothelial growth factor-A (VEGF-A) binding to neuropilin-1. J. Biol. Chem. 287, 11082-11089 (2012).
34. N. Haspel, D. Zanuy, R. Nussinov, T. Teesalu, E. Ruoslahti, C. Aleman, Binding of a C-end rule peptide to the neuropilin-1 receptor: A molecular modeling approach. Biochemistry 50, 1755-1762 (2011).
35. M. J. Renzi, L. Feiner, A. M. Koppel, J. A. Raper, A dominant negative receptor for specific secreted semaphorins is generated by deleting an extracellular domain from neuropilin-1. J. Neurosci. 19, 7870-7880 (1999).
36. A. Antipenko, J.-P. Himanen, K. van Leyen, V. Nardi-Dei, J. Lesniak, W. A. Barton, K. R. Rajashankar, M. Lu, C. Hoemme, A. W. Püschel, D. B. Nikolov, Structure of the semaphorin-3A receptor binding module. Neuron 39, 589-598 (2003).
37. C. W. Vander Kooi, M. A. Jusino, B. Perman, D. B. Neau, H. D. Bellamy, D. J. Leahy, Structural basis for ligand and heparin binding to neuropilin B domains. Proc. Natl. Acad. Sci. U.S.A. 104, 6152-6157 (2007).
38. Z. Gluzman-Poltorak, T. Cohen, Y. Herzog, G. Neufeld, Neuropilin-2 and neuropilin-1 are receptors for the 165-amino acid form of vascular endothelial growth factor (VEGF) and of placenta growth factor-2, but only neuropilin-2 functions as a receptor for the 145- amino acid form of VEGF. J. Biol. Chem. 275, 18040-18045 (2000).
39. L. Roth, L. Agemy, V. R. Kotamraju, G. Braun, T. Teesalu, K. N. Sugahara, J. Hamzah, E. Ruoslahti, Transtumoral targeting enabled by a novel neuropilin-binding peptide. Oncogene 31, 3754-3763 (2011)
40. N. Bayer, D. Schober, E. Prchla, R. F. Murphy, D. Blaas, R. Fuchs, Effect of bafilomycin A1 and nocodazole on endocytic transport in HeLa cells: Implications for viral uncoating and infection. J. Virol. 72, 9645-9655 (1998).
41. J. Thyberg, S. Moskalewski, Role of microtubules in the organization of the Golgi complex. Exp. Cell Res. 246, 263-279 (1999).
42. L. Lu, R. N. Hannoush, B. C. Goess, S. Varadarajan, M. D. Shair, T. Kirchhausen, The small molecule dispergo tubulates the endoplasmic reticulum and inhibits export. Mol. Biol. Cell 24, 1020-1029 (2013).
43. P. D. Collins, D. T. Connolly, T. J. Williams, Characterization of the increase in vascular permeability induced by vascular permeability factor in vivo.Br. J. Pharmacol. 109, 195-199 (1993).
44. P. M. Becker, A. D. Verin, M. A. Booth, F. Liu, A. Birukava, J. G. N. Garcia, Differential regulation of diverse physiological responses to VEGF in pulmonary endothelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 281, L1500-L1511 (2001).
45. E. Ackah, J. Yu, S. Zoellner, Y. Iwakiri, C. Skurk, R. Shibata, N. Ouchi, R. M. Easton, G. Galasso, M. J. Birnbaum, K. Walsh, W. C. Sessa, Akt1/protein kinase Ba is critical for ischemic and VEGF-mediated angiogenesis. J. Clin. Invest. 115, 2119-2127 (2005).
46. L. M. Acevedo, S. Barillas, S. M. Weis, J. R. Göthert, D. A. Cheresh, Semaphorin 3A suppresses VEGF-mediated angiogenesis yet acts as a vascular permeability factor. Blood 111, 2674-2680 (2008).
47. J. M. Wood, G. Bold, E. Buchdunger, R. Cozens, S. Ferrari, J. Frei, F. Hofmann, J. Mestan, H. Mett, T. O'Reilly, E. Persohn, J. Rösel, C. Schnell, D. Stover, A. Theuer, H. Towbin, F.Wenger, K. Woods-Cook, A. Menrad, G. Siemeister, M. Schirner, -H. Thierauch, M. R. Schneider, J. Drevs, G. Martiny-Baron, F. Totzke, PTK787/ZK 222584, a novel and potent inhibitor of vascular endothelial growth factor receptor tyrosine kinases, impairs vascular endothelial growth factor-induced responses and tumor growth after oral administration. Cancer Res. 60, 2178-2189 (2000).
48. A. Fantin, Q. Schwarz, K. Davidson, E. M. Normando, L. Denti, C. Ruhrberg, The cytoplasmic domain of neuropilin 1 is dispensable for angiogenesis, but promotes the spatial separation of retinal arteries and veins. Development 138, 4185-4191 (2011).
49. C. Nasarre, M. Roth, L. Jacob, L. Roth, E. Koncina, A. Thien, G. Labourdette, P. Poulet, P. Hubert, G. Crémel, G. Roussel, D. Aunis, D. Bagnard, Peptide-based interference of the transmembrane domain of neuropilin-1 inhibits glioma growth in vivo. Oncogene 29, 2381-2392 (2010).
50. H.-Q. Miao, S. Soker, L. Feiner, J. L. Alonso, J. A. Raper, M. Klagsbrun, Neuropilin- 1 mediates collapsin-1/semaphorin III inhibition of endothelial cell motility: Functional competition of collapsin-1 and vascular endothelial growth factor-165. J. Cell Biol. 146, 233-242 (1999).
51. C. Gu, B. J. Limberg, G. B. Whitaker, B. Perman, D. J. Leahy, J. S. Rosenbaum, D. D. Ginty, A. L. Kolodkin, Characterization of neuropilin-1 structural features that confer binding to semaphorin 3A and vascular endothelial growth factor 165. J. Biol. Chem. 277, 18069-18076 (2002).
52. B. A. Appleton, P.Wu, J. Maloney, J. Yin,W.-C. Liang, S. Stawicki, K. Mortara, K. K. Bowman, J. M. Elliott,W. Desmarais, J. F. Bazan, A. Bagri, M. Tessier-Lavigne, A.W. Koch, Y.Wu, R. J. Watts, C. Wiesman, Structural studies of neuropilin/antibody complexes provide insights into semaphorin and VEGF binding. EMBO J. 26, 4902-4912 (2007).
53. M. W. Parker, L. M. Hellman, P. Xu, M. G. Fried, C. W. Vander Kooi, Furin processing of semaphorin 3F determines its anti-angiogenic activity by regulating direct binding and competition for neuropilin. Biochemistry 49, 4068-4075 (2010).
54. J. A. Nagy, L. Benjamin, H. Zeng, A. M. Dvorak, H. F. Dvorak, Vascular permeability, vascular hyperpermeability and angiogenesis. Angiogenesis 11, 109-119 (2008).
55. L. Yuan, D. Moyon, L. Pardanaud, C. Bréant, M. J. Karkkainen, K. Alitalo, A. Eichmann, Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development 129, 4797-4806 (2002).
56. V. Joukov, T. Sorsa, V. Kumar, M. Jeltsch, L. Claesson-Welsh, Y. Cao, O Saksela, N. Kalkkinen, K. Alitalo, Proteolytic processing regulates receptor specificity and activity of VEGF-C. EMBO J. 16, 3898-3911 (1997).
57. M. Jeltsch, A. Kaipainen, V. Joukov, X. Meng, M. Lakso, H. Rauvala, M. Swartz,D. Fukumura, R. K. Jain, K. Alitalo, Hyperplasia of lymphatic vessels in VEGF-C transgenicmice. Science 276, 1423-1425 (1997).
58. L. Wang, H. Zeng, P. Wang, S. Soker, D. Mukhopadhyay, Neuropilin-1-mediated vascular permeability factor/vascular endothelial growth factor-dependent endothelial cell migration. J. Biol. Chem. 278, 48848-48860 (2003).
59. L. Wang, S. K. Dutta, T. Kojima, X. Xu, R. Khosravi-Far, S. C. Ekker, D. Mukhopadhyay, Neuropilin-1 modulates p53/caspases axis to promote endothelial cell survival. PLOS One 2, e1161 (2007).