Targeting VEGF signalling via the neuropilin co-receptor

Drug Discovery Today

Volumn 18, Issue 9-10, 2013, Pages 447-455

  Djordjevic, Snezana ^a   Driscoll, Paul C ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AFLIBERCEPT; BEVACIZUMAB; NEUROPILIN; NEUROPILIN 1; NEUROPILIN 2; PLACENTAL GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR BB; SORAFENIB; SUNITINIB; VASCULOTROPIN; VASCULOTROPIN 165; VASCULOTROPIN A; VASCULOTROPIN B; VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN E; VASCULOTROPIN RECEPTOR;

ADVANCED CANCER; ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; ANGIOGENESIS; CARCINOGENESIS; CELL PROLIFERATION; CELL SURVIVAL; COMPLEX FORMATION; CRYSTAL STRUCTURE; CYTOPLASM; DIMERIZATION; DISEASE ASSOCIATION; DRUG EFFICACY; DRUG INDICATION; DRUG SAFETY; DRUG TARGETING; EXTRACELLULAR MATRIX; EYE DISEASE; HEPATIN BINDING DOMAIN; KIDNEY CARCINOMA; METASTASIS; NEOPLASM; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; RECEPTOR BINDING; RETINA MACULA AGE RELATED DEGENERATION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; NEOVASCULARIZATION, PATHOLOGIC; NEUROPILINS; PROTEIN CONFORMATION; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84876908762     PISSN: 13596446     EISSN: 18785832     Source Type: Journal    
DOI: 10.1016/j.drudis.2012.11.013     Document Type: Review

References (116)

1. K.M. Cook, and W.D. Figg Angiogenesis inhibitors: current strategies and future prospects CA Cancer J. Clin. 60 2010 222 243
2. J. Folkman Tumor angiogenesis: therapeutic implications N. Engl. J. Med. 285 1971 1182 1186
3. R.S. Samant, and L.A. Shevde Recent advances in anti-angiogenic therapy of cancer Oncotarget 2 2011 122 134
4. N. Ferrara The biology of VEGF and its receptors Nat. Med. 9 2003 669 676
5. N. Ferrara Vascular endothelial growth factor Arterioscler. Thromb. Vasc. Biol. 29 2009 789 791
6. R. Roskoski Jr. VEGF receptor protein-tyrosine kinases: structure and regulation Biochem. Biophys. Res. Commun. 375 2008 287 291
7. E. Tischer The human gene for vascular endothelial growth factor multiple protein forms are encoded through alternative exon splicing J. Biol. Chem. 266 1991 11947 11954
8. N. Ferrara Binding to the extracellular matrix and proteolytic processing: two key mechanisms regulating vascular endothelial growth factor action Mol. Biol. Cell 21 2010 687 690
9. S. Koch Neuropilin signalling in angiogenesis Biochem. Soc. Trans. 40 2012 20 25
10. M.A. Lemmon, and J. Schlessinger Cell signaling by receptor tyrosine kinases Cell 141 2010 1117 1134
11. B.I. Terman Identification of the KDR tyrosine kinase as a receptor for vascular endothelial cell growth factor Biochem. Biophys. Res. Commun. 187 1992 1579 1586
12. Q. Pan Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth Cancer Cell 11 2007 53 67
13. P.M. Becker Neuropilin-1 regulates vascular endothelial growth factor-mediated endothelial permeability Circ. Res. 96 2005 1257 1265
14. M. Muhsin Bevacizumab Nat. Rev. Drug Discov. 3 2004 995 996
15. N. Ferrara Vascular endothelial growth factor as a target for anticancer therapy Oncologist 9 Suppl. 1 2004 2 10
16. K. Mulder The role of bevacizumab in colorectal cancer: understanding its benefits and limitations Expert Opin. Biol. Ther. 11 2011 405 413
17. B. Blanchet Toxicity of sorafenib: clinical and molecular aspects Expert Opin. Drug Saf. 9 2010 275 287
18. M.W. Stewart Afilbercept Nat. Rev. Drug Discov. 11 2012 269 270
19. J. Holash VEGF-trap: a VEGF blocker with potent antitumor effects Proc. Natl. Acad. Sci. U. S. A. 99 2002 11393 11398
20. E. Geretti A mutated soluble neuropilin-2 B domain antagonizes vascular endothelial growth factor bioactivity and inhibits tumor progression Mol. Cancer Res. 8 2010 1063 1073
21. D. Tvorogov Effective suppression of vascular network formation by combination of antibodies blocking VEGFR ligand binding and receptor dimerization Cancer Cell 18 2010 630 640
22. J. Kendrew An antibody targeted to VEGFR-2 Ig domains 4-7 inhibits VEGFR-2 activation and VEGFR-2-dependent angiogenesis without affecting ligand binding Mol. Cancer Ther. 10 2011 770 783
23. S. Wilhelm Discovery and development of sorafenib: a multikinase inhibitor for treating cancer Nat. Rev. Drug Discov. 5 2006 835 844
24. J. Mangana Sorafenib in melanoma Expert Opin. Investig. Drugs 21 2012 557 568
25. E.P. Rock Food and Drug Administration drug approval summary: sunitinib malate for the treatment of gastrointestinal stromal tumor and advanced renal cell carcinoma Oncologist 12 2007 107 113
26. H. Izzedine Sunitinib malate Cancer Chemother. Pharmacol. 60 2007 357 364
27. G. Aparicio-Gallego New insights into molecular mechanisms of sunitinib-associated side effects Mol. Cancer Ther. 10 2011 2215 2223
28. C. Gridelli Sorafenib and sunitinib in the treatment of advanced non-small cell lung cancer Oncologist 12 2007 191 200
29. L.M. Ellis, and D.J. Hicklin VEGF-targeted therapy: mechanisms of anti-tumour activity Nat. Rev. Cancer 8 2008 579 591
30. H.X. Chen, and J.N. Cleck Adverse effects of anticancer agents that target the VEGF pathway Nat. Rev. Clin. Oncol. 6 2009 465 477
31. S.R. Hayman VEGF inhibition, hypertension, and renal toxicity Curr. Oncol. Rep. 14 2012 285 294
32. C. Coppin Sunitinib for advanced renal cell cancer Biologics 2 2008 97 105
33. G. Deep Angiopreventive efficacy of pure flavonolignans from milk thistle extract against prostate cancer: targeting VEGF-VEGFR signaling PLoS One 7 2012 e34630
34. D.A. Nosov Antitumor activity and safety of tivozanib (AV-951) in a phase II randomized discontinuation trial in patients with renal cell carcinoma J. Clin. Oncol. 30 2012 1678 1685
35. S. Takagi The A5 antigen, a candidate for the neuronal recognition molecule, has homologies to complement components and coagulation factors Neuron 7 1991 295 307
36. Z. He, and M. Tessier-Lavigne Neuropilin is a receptor for the axonal chemorepellent Semaphorin III Cell 90 1997 739 751
37. A.L. Kolodkin Neuropilin is a semaphorin III receptor Cell 90 1997 753 762
38. C. Gu Characterization of neuropilin-1 structural features that confer binding to semaphorin 3A and vascular endothelial growth factor 165 J. Biol. Chem. 277 2002 18069 18076
39. C. Grandclement, and C. Borg Neuropilins: a new target for cancer therapy Cancer 3 2011 29
40. C.E. Hagberg Vascular endothelial growth factor B controls endothelial fatty acid uptake Nature 464 2010 917 921
41. T. Karpanen Functional interaction of VEGF-C and VEGF-D with neuropilin receptors FASEB J. 20 2006 1462 1472
42. H. Takahashi, and M. Shibuya The vascular endothelial growth factor (VEGF)/VEGF receptor system and its role under physiological and pathological conditions Clin. Sci. 109 2005 227 241
43. T. Kitsukawa Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice Neuron 19 1997 995 1005
44. T. Kawasaki A requirement for neuropilin-1 in embryonic vessel formation Development 126 1999 4895 4902
45. C. Gu Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development Dev. Cell 5 2003 45 57
46. L. Yuan Abnormal lymphatic vessel development in neuropilin 2 mutant mice Development 129 2002 4797 4806
47. S. Takashima Targeting of both mouse neuropilin-1 and neuropilin-2 genes severely impairs developmental yolk sac and embryonic angiogenesis Proc. Natl. Acad. Sci. U. S. A. 99 2002 3657 3662
48. C.H. Maden NRP1 and NRP2 cooperate to regulate gangliogenesis, axon guidance and target innervation in the sympathetic nervous system Dev. Biol. 369 2012 277 285
49. R.E. Bachelder Vascular endothelial growth factor is an autocrine survival factor for neuropilin-expressing breast carcinoma cells Cancer Res. 61 2001 5736 5740
50. E. Castro-Rivera Semaphorin 3B (SEMA3B) induces apoptosis in lung and breast cancer, whereas VEGF165 antagonizes this effect Proc. Natl. Acad. Sci. U. S. A. 101 2004 11432 11437
51. Y. Cao Neuropilin-1 upholds dedifferentiation and propagation phenotypes of renal cell carcinoma cells by activating Akt and sonic hedgehog axes Cancer Res. 68 2008 8667 8672
52. T.M. Hong Targeting neuropilin 1 as an antitumor strategy in lung cancer Clin. Cancer Res. 13 2007 4759 4768
53. B. Beck A vascular niche and a VEGF-Nrp1 loop regulate the initiation and stemness of skin tumours Nature 478 2011 399 403
54. P. Hamerlik Autocrine VEGF-VEGFR2-Neuropilin-1 signaling promotes glioma stem-like cell viability and tumor growth J. Exp. Med. 209 2012 507 520
55. K. Fukahi Aberrant expression of neuropilin-1 and -2 in human pancreatic cancer cells Clin. Cancer Res. 10 2004 581 590
56. M. Li Pancreatic carcinoma cells express neuropilins and vascular endothelial growth factor, but not vascular endothelial growth factor receptors Cancer 101 2004 2341 2350
57. H.J. Meyerson NRP-1/CD304 expression in acute leukemia: a potential marker for minimal residual disease detection in precursor B-cell acute lymphoblastic leukemia Am. J. Clin. Pathol. 137 2012 39 50
58. M. Berge Neuropilin-1 is upregulated in hepatocellular carcinoma and contributes to tumour growth and vascular remodelling J. Hepatol. 55 2011 866 875
59. C. Grandclement Neuropilin-2 expression promotes TGF-beta1-mediated epithelial to mesenchymal transition in colorectal cancer cells PLoS One 6 2011 e20444
60. J.R. Wild Neuropilins: expression and roles in the epithelium Int. J. Exp. Pathol. 93 2012 81 103
61. A.M. Jubb Neuropilin-1 expression in cancer and development J. Pathol. 226 2012 50 60
62. S.D. Robinson Alphav beta3 integrin limits the contribution of neuropilin-1 to vascular endothelial growth factor-induced angiogenesis J. Biol. Chem. 284 2009 33966 33981
63. D. Valdembri Neuropilin-1/GIPC1 signaling regulates alpha5beta1 integrin traffic and function in endothelial cells PLoS Biol. 7 2009 e25
64. M. Fukasawa Neuropilin-1 interacts with integrin beta1 and modulates pancreatic cancer cell growth, survival and invasion Cancer Biol. Ther. 6 2007 1173 1180
65. E. Sulpice Neuropilin-1 and neuropilin-2 act as coreceptors, potentiating proangiogenic activity Blood 111 2008 2036 2045
66. S. Banerjee Breast cancer cells secreted platelet-derived growth factor-induced motility of vascular smooth muscle cells is mediated through neuropilin-1 Mol. Carcinog. 45 2006 871 880
67. I.M. Evans 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
68. P. Frankel 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
69. C. Pellet-Many Neuropilin-1 mediates PDGF stimulation of vascular smooth muscle cell migration and signalling via p130Cas Biochem. J. 435 2011 609 618
70. A. Fantin 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
71. H. Kawamura Neuropilin-1 in regulation of VEGF-induced activation of p38MAPK and endothelial cell organization Blood 112 2008 3638 3649
72. L. Roth Transmembrane domain interactions control biological functions of neuropilin-1 Mol. Biol. Cell 19 2008 646 654
73. 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
74. C. Prahst Neuropilin-1-VEGFR-2 complexing requires the PDZ-binding domain of neuropilin-1 J. Biol. Chem. 283 2008 25110 25114
75. A. Eichmann, and M. Simons VEGF signaling inside vascular endothelial cells and beyond Curr. Opin. Cell Biol. 24 2012 188 193
76. B.A. Appleton Structural studies of neuropilin/antibody complexes provide insights into semaphorin and VEGF binding EMBO J. 26 2007 4902 4912
77. C.W. Vander Kooi Structural basis for ligand and heparin binding to neuropilin B domains Proc. Natl. Acad. Sci. U. S. A. 104 2007 6152 6157
78. C.C. Lee Crystal structure of the human neuropilin-1 b1 domain Structure 11 2003 99 108
79. M.A. von Wronski Tuftsin binds neuropilin-1 through a sequence similar to that encoded by exon 8 of vascular endothelial growth factor J. Biol. Chem. 281 2006 5702 5710
80. P. Fuentes-Prior New insights into binding interfaces of coagulation factors V and VIII and their homologues lessons from high resolution crystal structures Curr. Prot. Pep. Sci. 3 2002 313 339
81. A. Gaskell The three domains of a bacterial sialidase: a beta-propeller, an immunoglobulin module and a galactose-binding jelly-roll Structure 3 1995 1197 1205
82. S. Soker Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor Cell 92 1998 735 745
83. R.J. Giger Neuropilin-2 is a receptor for semaphorin IV: insight into the structural basis of receptor function and specificity Neuron 21 1998 1079 1092
84. M.S. Brozzo Thermodynamic and structural description of allosterically regulated VEGFR-2 dimerization Blood 119 2012 1781 1788
85. V.M. Leppanen Structural determinants of growth factor binding and specificity by VEGF receptor 2 Proc. Natl. Acad. Sci. U. S. A. 107 2010 2425 2430
86. C. Ruch Structure of a VEGF-VEGF receptor complex determined by electron microscopy Nat. Struct. Mol. Biol. 14 2007 249 250
87. S. Soker VEGF165 mediates formation of complexes containing VEGFR-2 and neuropilin-1 that enhance VEGF165-receptor binding J. Cell. Biochem. 85 2002 357 368
88. G.B. Whitaker Vascular endothelial growth factor receptor-2 and neuropilin-1 form a receptor complex that is responsible for the differential signaling potency of VEGF(165) and VEGF(121) J. Biol. Chem. 276 2001 25520 25531
89. B. Herzog 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
90. I.C. Zachary How neuropilin-1 regulates receptor tyrosine kinase signalling: the knowns and known unknowns Biochem. Soc. Trans. 39 2011 1583 1591
91. M.W. Parker Structural basis for selective vascular endothelial growth factor-A (VEGF-A) binding to neuropilin-1 J. Biol. Chem. 287 2012 11082 11089
92. A.R. Aricescu Molecular analysis of receptor protein tyrosine phosphatase mu-mediated cell adhesion EMBO J. 25 2006 701 712
93. Y. Shintani Glycosaminoglycan modification of neuropilin-1 modulates VEGFR2 signaling EMBO J. 25 2006 3045 3055
94. G. Fuh The interaction of neuropilin-1 with vascular endothelial growth factor and its receptor flt-1 J. Biol. Chem. 275 2000 26690 26695
95. R. Mamluk Neuropilin-1 binds vascular endothelial growth factor 165, placenta growth factor-2, and heparin via its b1b2 domain J. Biol. Chem. 277 2002 24818 24825
96. H.J. Lee, and J.J. Zheng PDZ domains and their binding partners: structure, specificity, and modification Cell Commun. Signal. CCS 8 2010 8
97. F. Mac Gabhann, and A.S. Popel Targeting neuropilin-1 to inhibit VEGF signaling in cancer: Comparison of therapeutic approaches PLoS Comput. Biol. 2 2006 e180
98. S.D. Finley Pharmacokinetics and pharmacodynamics of VEGF-neutralizing antibodies BMC Syst. Biol. 5 2011 193
99. D. Bumbaca Maximizing tumour exposure to anti-neuropilin-1 antibody requires saturation of non-tumour tissue antigenic sinks in mice Br. J. Pharmacol. 166 2012 368 377
100. M. Caunt Blocking neuropilin-2 function inhibits tumor cell metastasis Cancer Cell 13 2008 331 342
101. S. Soker Inhibition of vascular endothelial growth factor (VEGF)-induced endothelial cell proliferation by a peptide corresponding to the exon 7-encoded domain of VEGF165 J. Biol. Chem. 272 1997 31582 31588
102. M.P. Barr A peptide corresponding to the neuropilin-1-binding site on VEGF(165) induces apoptosis of neuropilin-1-expressing breast tumour cells Br. J. Cancer 92 2005 328 333
103. H. Jia Characterization of a bicyclic peptide neuropilin-1 (NP-1) antagonist (EG3287) reveals importance of vascular endothelial growth factor exon 8 for NP-1 binding and role of NP-1 in KDR signaling J. Biol. Chem. 281 2006 13493 13502
104. A. Starzec Antiangiogenic and antitumor activities of peptide inhibiting the vascular endothelial growth factor binding to neuropilin-1 Life Sci. 79 2006 2370 2381
105. R.J. Giordano From combinatorial peptide selection to drug prototype (I): targeting the vascular endothelial growth factor receptor pathway Proc. Natl. Acad. Sci. U. S. A. 107 2010 5112 5117
106. C. Nasarre Peptide-based interference of the transmembrane domain of neuropilin-1 inhibits glioma growth in vivo Oncogene 29 2010 2381 2392
107. M. Narazaki Oligo-guanosine nucleotide induces neuropilin-1 internalization in endothelial cells and inhibits angiogenesis Blood 116 2010 3099 3107
108. A. Jarvis Small molecule inhibitors of the neuropilin-1 vascular endothelial growth factor A (VEGF-A) interaction J. Med. Chem. 53 2010 2215 2226
109. Y. Yang Direct contacts between extracellular membrane-proximal domains are required for VEGF receptor activation and cell signaling Proc. Natl. Acad. Sci. U. S. A. 107 2010 1906 1911
110. F. Nakamura Neuropilin-1 extracellular domains mediate semaphorin D/III-induced growth cone collapse Neuron 21 1998 1093 1100
111. T. Teesalu C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration Proc. Natl. Acad. Sci. U. S. A. 106 2009 16157 16162
112. K.N. Sugahara Tissue-penetrating delivery of compounds and nanoparticles into tumors Cancer Cell 16 2009 510 520
113. L. Roth Transtumoral targeting enabled by a novel neuropilin-binding peptide Oncogene 31 2012 3754 3763
114. K. Karjalainen Targeting neuropilin-1 in human leukemia and lymphoma Blood 117 2011 920 927
115. A. Kumar Gold nanoparticles functionalized with therapeutic and targeted peptides for cancer treatment Biomaterials 33 2012 1180 1189
116. C.E. Hagberg Targeting VEGF-B as a novel treatment for insulin resistance and type 2 diabetes Nature 490 2012 426 430