Peptide-based interference of the transmembrane domain of neuropilin-1 inhibits glioma growth in vivo

Oncogene

Volumn 29, Issue 16, 2010, Pages 2381-2392

  Nasarre, C ^a   Roth, M ^a   Jacob, L ^a   Roth, L ^a   Koncina, E ^a   Thien, A ^a   Labourdette, G ^a   Poulet, P ^b   Hubert, P ^c   Cremel G ^a   Roussel, G ^a   Aunis, D ^a   Bagnard, D ^a  

^a INSERM   (France)

^b Institut de Physique Biologique   (France)

^c CNRS   (France)

Author keywords

Angiogenesis; Glioma; Neuropilin; Peptide; Tumour growth

Indexed keywords

NEUROPILIN 1; VASCULOTROPIN; VASCULOTROPIN 165;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CANCER SURVIVAL; CELL MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; GLIOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR GROWTH; UMBILICAL VEIN;

AMINO ACID SEQUENCE; ANGIOGENESIS INHIBITORS; ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CHICK EMBRYO; GLIOMA; HUMANS; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; NEUROPILIN-1; PROTEIN STRUCTURE, TERTIARY; RATS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

RATTUS;

EID: 77951622512     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.9     Document Type: Article

References (42)

1. Bagci T, Wu JK, Pfannl R, Ilag LL, Jay DG. (2009). Autocrine semaphorin 3A signaling promotes glioblastoma dispersal. Oncogene 28: 3537-3550.
2. Bagri A, Tessier-Lavigne M. (2002). Neuropilins as semaphorin receptors: in vivofunctions in neuronal cell migration and axon guidance. Adv Exp Med Biol 515: 13-31.
3. Bargmann CI, Weinberg RA. (1988). Oncogenic activation of the neu-encoded receptor protein by point mutation and deletion. EMBO J 7: 2043-2052.
4. Barr MP, Byrne AM, Duffy AM, Condron CM, Devocelle M, Harriott P et al. (2005). 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: 328-333.
5. Bedjeguelal K, Bienayme H, Dumoulin A, Poigny S, Schmitt P, Tam E. (2006). Discovery of protein-protein binding disruptors using multi-component condensations small molecules. Bioorg Med Chem Lett 16: 3998-4001.
6. Bennasroune A, Gardin A, Aunis D, Cremel G, Hubert P. (2004). Tyrosine kinase receptors as attractive targets of cancer therapy. Crit Rev Oncol Hematol 50: 23-38.
7. Forbes LV, Gale RE, Pizzey A, Pouwels K, Nathwani A, Linch DC. (2002). An activating mutation in the transmembrane domain of the granulocyte colony-stimulating factor receptor in patients with acute myeloid leukemia. Oncogene 21: 5981-5989.
8. Gamse JT, Shen YC, Thisse C, Thisse B, Raymond PA, Halpern ME et al. (2002). Otx5 regulates genes that show circadian expression in the zebrafish pineal complex. Nat Genet 30: 117-121.
9. Garcia-Verdugo JM, Doetsch F, Wichterle H, Lim DA, Alvarez-Buylla A. (1998). Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neurobiol 36: 234-248.
10. Giordano RJ, Anobom CD, Cardo-Vila M, Kalil J, Valente AP, Pasqualini R et al. (2005). Structural basis for the interaction of a vascular endothelial growth factor mimic peptide motif and its corresponding receptors. Chem Biol 12: 1075-1083.
11. Goldbrunner RH, Wagner S, Roosen K, Tonn JC. (2000). Models for assessment of angiogenesis in gliomas. J Neurooncol 50: 53-62.
12. Grobben B, De Deyn PP, Slegers H. (2002). Rat C6 glioma as experimental model system for the study of glioblastoma growth and invasion. Cell Tissue Res 310: 257-270.
13. Guttmann-Raviv N, Kessler O, Shraga-Heled N, Lange T, Herzog Y, Neufeld G. (2006). The neuropilins and their role in tumorigenesis and tumor progression. Cancer Lett 231: 1-11. (Pubitemid 41779447)
14. Hong TM, Chen YL, Wu YY, Yuan A, Chao YC, Chung YC et al. (2007). Targeting neuropilin 1 as an antitumor strategy in lung cancer. Clin Cancer Res 13: 4759-4768.
15. Hu B, Guo P, Bar-Joseph I, Imanishi Y, Jarzynka MJ, Bogler O et al. (2007). Neuropilin-1 promotes human glioma progression through potentiating the activity of the HGF/SF autocrine pathway. Oncogene 26: 5577-5586.
16. Jain RK, di Tomaso E, Duda DG, Loeffler JS, Sorensen AG, Batchelor TT. (2007). Angiogenesis in brain tumours. Nat Rev Neurosci 8: 610-622.
17. Jain RK, Duda DG, Clark JW, Loeffler JS. (2006). Lessons from phase III clinical trials on anti-VEGF therapy for cancer. Nat Clin Pract Oncol 3: 24-40.
18. Jia H, Bagherzadeh A, Hartzoulakis B, Jarvis A, Lohr M, Shaikh S et al. (2006). 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: 13493-13502.
19. Jocic Z, Staton RD. (1993). Reduplication after right middle cerebral artery infarction. Brain Cogn 23: 222-230.
20. Kelland LR. (2004). Of mice and men: values and liabilities of the athymic nude mouse model in anticancer drug development. Eur J Cancer 40: 827-836.
21. Kienlen-Campard P, Tasiaux B, Van Hees J, Li M, Huysseune S, Sato T et al. (2008). Amyloidogenic processing but not amyloid precursor protein (APP) intracellular C-terminal domain production requires a precisely oriented APP dimer assembled by transmembrane GxxxG motifs. J Biol Chem 283: 7733-7744.
22. Klosen P, Maessen X, van den Bosch de Aguilar P. (1993). PEG embedding for immunocytochemistry: application to the analysis of immunoreactivity loss during histological processing. J Histochem Cytochem 41: 455-463.
23. Lemmon MA, Flanagan JM, Treutlein HR, Zhang J, Engelman DM. (1992). Sequence specificity in the dimerization of transmembrane alpha-helices. Biochemistry 31: 12719-12725.
24. Marchesi VT. (2005). An alternative interpretation of the amyloid Abeta hypothesis with regard to the pathogenesis of Alzheimer's disease. Proc Natl Acad Sci USA 102: 9093-9098.
25. Meyers GA, Orlow SJ, Munro IR, Przylepa KA, Jabs EW. (1995). Fibroblast growth factor receptor 3 (FGFR3) transmembrane mutation in Crouzon syndrome with Acanthosis nigricans. Nat Genet 11: 462-464.
26. Nasarre C, Koncina E, Labourdette G, Cremel G, Roussel G, Aunis D et al. (2009). Neuropilin-2 acts as a modulator of Sema3A-dependent glioma cell migration. Cell Adh Migr 3: 383-389.
27. Nasarre P, Kusy S, Constantin B, Castellani V, Drabkin HA, Bagnard D et al. (2005). Semaphorin SEMA3F has a repulsing activity on breast cancer cells and inhibits E-cadherin-mediated cell adhesion. Neoplasia 7: 180-189.
28. Orian-Rousseau V, Ponta H. (2008). Adhesion proteins meet receptors: a common theme? Adv Cancer Res 101: 63-92.
29. Roth L, Nasarre C, Dirrig-Grosch S, Aunis D, Cremel G, Hubert P et al. (2008). Transmembrane domain interactions control biological functions of neuropilin-1. Mol Biol Cell 19: 646-654.
30. Senes A, Engel DE, DeGrado WF. (2004). Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr Opin Struct Biol 14: 465-479.
31. Slimani H, Guenin E, Briane D, Coudert R, Charnaux N, Starzec A et al. (2006). Lipopeptide-based liposomes for DNA delivery into cells expressing neuropilin-1. J Drug Target 14: 694-706.
32. Starzec A, Vassy R, Martin A, Lecouvey M, Di Benedetto M, Crepin M et al. (2006). Antiangiogenic and antitumor activities of peptide inhibiting the vascular endothelial growth factor binding to neuropilin-1. Life Sci 79: 2370-2381.
33. Taguchi A, Soma T, Tanaka H, Kanda T, Nishimura H, Yoshikawa H et al. (2004). Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J Clin Invest 114: 330-338.
34. Tessitore A, Sinisi AA, Pasquali D, Cardone M, Vitale D, Bellastella A et al. (1999). A novel case of multiple endocrine neoplasia type 2A associated with two de novo mutations of the RET protooncogene. J Clin Endocrinol Metab 84: 3522-3527.
35. Tirand L, Frochot C, Vanderesse R, Thomas N, Trinquet E, Pinel S et al. (2006). A peptide competing with VEGF165 binding on neuropilin-1 mediates targeting of a chlorin-type photosensitizer and potentiates its photodynamic activity in human endothelial cells. J Control Release 111: 153-164.
36. Uitenbroek DG. (1997). Binomial SISA. http://www.quantitatives-kills.com/ sisa/distributions/binomial.htm.
37. Uzzan B, Nicolas P, Cucherat M, Perret GY. (2004). Microvessel density as a prognostic factor in women with breast cancer: a systematic review of the literature and meta-analysis. Cancer Res 64: 2941-2955.
38. Wang AC, Dai X, Luu B, Conrad DJ. (2001). Peroxisome proliferator- activated receptor-gamma regulates airway epithelial cell activation. Am J Respir Cell Mol Biol 24: 688-693.
39. Webster MK, Donoghue DJ. (1996). Constitutive activation of fibroblast growth factor receptor 3 by the transmembrane domain point mutation found in achondroplasia. EMBO J 15: 520-527.
40. Weiner DB, Liu J, Cohen JA, Williams WV, Greene MI. (1989). A point mutation in the neu oncogene mimics ligand induction of receptor aggregation. Nature 339: 230-231.
41. Williams G, Eickholt BJ, Maison P, Prinjha R, Walsh FS, Doherty P. (2005). A complementary peptide approach applied to the design of novel semaphorin/neuropilin antagonists. J Neurochem 92: 1180-1190.
42. Xu L, Duda DG, di Tomaso E, Ancukiewicz M, Chung DC, Lauwers GY. et al. (2009). Direct evidence that bevacizumab, an anti-VEGF antibody, up-regulates SDF1alpha, CXCR4, CXCL6, and neuropilin 1 in tumors from patients with rectal cancer. Cancer Res 69: 7905-7910.