A monoclonal antibody targeting neuropilin-1 inhibits adhesion of MCF7 breast cancer cells to fibronectin by suppressing the FAK/p130cas signaling pathway

Anti-Cancer Drugs

Volumn 25, Issue 6, 2014, Pages 663-672

  Zeng, Fanwei ^a   Luo, Fanghong ^a   Lv, Sha ^a   Zhang, Haipeng ^a   Cao, Chang ^a   Chen, Xiaoli ^a   Wang, Shengyu ^a   Li, Zhe ^a   Wang, Xianjiang ^a   Dou, Xiaofeng ^a   Dai, Yujuan ^a   He, Mingjun ^a   Zhang, Yafei ^a   Lv, Haiyan ^a   Yan, Jianghua ^a   Chen, Yuqiang ^a  

^a XIAMEN UNIVERSITY   (China)

Author keywords

Adhesion; Anti NRP 1 mAb; Focal adhesion kinase; Neuropilin 1; 5 1 integrin

Indexed keywords

ACTIN; ANTINEOPLASTIC AGENT; CRK ASSOCIATED SUBSTRATE PROTEIN; FIBRONECTIN; FOCAL ADHESION KINASE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY NRP 1; NEUROPILIN 1; PHALLOIDIN; RHODAMINE; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5;

ACTIN POLYMERIZATION; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER CELL LINE; CELL ADHESION; CELL ADHESION ASSAY; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; DRUG TARGETING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MCF 7 CELL LINE; MTT ASSAY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STRESS FIBER; WESTERN BLOTTING; BREAST TUMOR; DRUG EFFECTS; FEMALE; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ACTINS; ANTIBODIES, MONOCLONAL; BREAST NEOPLASMS; CELL ADHESION; CRK-ASSOCIATED SUBSTRATE PROTEIN; FEMALE; FIBRONECTINS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; MCF-7 CELLS; NEUROPILIN-1; SIGNAL TRANSDUCTION;

EID: 84901627424     PISSN: 09594973     EISSN: 14735741     Source Type: Journal    
DOI: 10.1097/CAD.0000000000000091     Document Type: Article

References (58)

1. Rizzolio S, Tamagnone L. Multifaceted role of neuropilins in cancer. Curr Med Chem 2011; 18:3563-3575.
2. He Z, Tessier-Lavigne M. Neuropilin is a receptor for the axonal chemorepellent Semaphorin III. Cell 1997; 90:739-751. (Pubitemid 27357965)
3. Fuh G, Garcia KC, de Vos AM. The interaction of neuropilin-1 with vascular endothelial growth factor and its receptor flt-1. J Biol Chem 2000; 275:26690-26695.
4. Kolodkin AL, Levengood DV, Rowe EG, Tai YT, Giger RJ, Ginty DD. Neuropilin is a semaphorin III receptor. Cell 1997; 90:753-762. (Pubitemid 27357966)
5. Mamluk R, Gechtman Z, Kutcher ME, Gasiunas N, Gallagher J, Klagsbrun M. Neuropilin-1 binds vascular endothelial growth factor 165, placenta growth factor-2, and heparin via its b1b2 domain. J Biol Chem 2002; 277: 24818-24825. (Pubitemid 34952014)
6. Gu C, Limberg BJ,Whitaker GB, Perman B, Leahy DJ, Rosenbaum JS, et al. Characterization of neuropilin-1 structural features that confer binding to semaphorin 3A and vascular endothelial growth factor 165. J Biol Chem 2002; 277:18069-18076. (Pubitemid 34967620)
7. Giger RJ, Urquhart ER, Gillespie SK, Levengood DV, Ginty DD, Kolodkin AL. Neuropilin-2 is a receptor for semaphorin IV: Insight into the structural basis of receptor function and specificity. Neuron 1998; 21:1079-1092. (Pubitemid 29018077)
8. Cai H, Reed RR. 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 1999; 19:6519-6527. (Pubitemid 29347451)
9. Kawasaki T, Kitsukawa T, Bekku Y, Matsuda Y, Sanbo M, Yagi T, Fujisawa H. A requirement for neuropilin-1 in embryonic vessel formation. Development 1999; 126:4895-4902.
10. Takashima S, Kitakaze M, Asakura M, Asanuma H, Sanada S, Tashiro F, et al. Targeting of both mouse neuropilin-1 and neuropilin-2 genes severely impairs developmental yolk sac and embryonic angiogenesis. Proc Natl Acad Sci USA 2002; 99:3657-3662. (Pubitemid 34252162)
11. Berge M, Allanic D, Bonnin P, de Montrion C, Richard J, Suc M, et al. Neuropilin-1 is upregulated in hepatocellular carcinoma and contributes to tumour growth and vascular remodelling. J Hepatol 2011; 55:866-875.
12. Evans IM, Yamaji M, Britton G, Pellet-Many C, Lockie C, Zachary IC, Frankel P. Neuropilin-1 signaling through p130Cas tyrosine phosphorylation is essential for growth factor-dependent migration of glioma and endothelial cells. Mol Cell Biol 2011; 31:1174-1185.
13. Parikh AA, Liu WB, Fan F, Stoeltzing O, Reinmuth N, Bruns CJ, et al. Expression and regulation of the novel vascular endothelial growth factor receptor neuropilin-1 by epidermal growth factor in human pancreatic carcinoma. Cancer 2003; 98:720-729. (Pubitemid 36959267)
14. Akagi M, Kawaguchi M, Liu W, McCarty MF, Takeda A, Fan F, et al. Induction of neuropilin-1 and vascular endothelial growth factor by epidermal growth factor in human gastric cancer cells. Br J Cancer 2003; 88:796-802. (Pubitemid 36411462)
15. Ochiumi T, Kitadai Y, Tanaka S, et al. Neuropilin-1 is involved in regulation of apoptosis and migration of human colon cancer. Int J Oncol 2006; 29:105-116.
16. Parikh AA, Fan F, Liu WB, Ahmad SA, Stoeltzing O, Reinmuth N, et al. Neuropilin-1 in human colon cancer: Expression, regulation, and role in induction of angiogenesis. Am J Pathol 2004; 164:2139-2151. (Pubitemid 38669361)
17. Castro-Rivera E, Ran S, Brekken RA, Minna JD. Semaphorin 3B inhibits the phosphatidylinositol 3-kinase/Akt pathway through neuropilin-1 in lung and breast cancer cells. Cancer Res 2008; 68:8295-8303.
18. Stephenson JM, Banerjee S, Saxena NK, Cherian R, Banerjee SK. Neuropilin-1 is differentially expressed in myoepithelial cells and vascular smooth muscle cells in preneoplastic and neoplastic human breast: A possible marker for the progression of breast cancer. Int J Cancer 2002; 101:409-414.
19. Hong TM, Chen YL, Wu YY, Yuan A, Chao YC, Chung YC, et al. Targeting neuropilin 1 as an antitumor strategy in lung cancer. Clin Cancer Res 2007; 13:4759-4768. (Pubitemid 47294782)
20. Younan S, Elhoseiny S, Hammam A, Gawdat R, El-Wakil M, Fawzy M. Role of neuropilin-1 and its expression in Egyptian acute myeloid and acute lymphoid leukemia patients. Leuk Res 2012; 36:169-173.
21. Schuch G, Machluf M, Bartsch G Jr, Nomi M, Richard H, Atala A, et al. In vivo administration of vascular endothelial growth factor (VEGF) and its antagonist, soluble neuropilin-1, predicts a role of VEGF in the progression of acute myeloid leukemia in vivo. Blood 2002; 100:4622-4628. (Pubitemid 35429707)
22. Osada H, Tokunaga T, Nishi M, Belcheva A, McCarty MF, Stoeltzing O, et al. Overexpression of the neuropilin 1 (NRP1) gene correlated with poor prognosis in human glioma. Anticancer Res 2004; 24:547-552. (Pubitemid 38624988)
23. Hansel DE,Wilentz RE, Yeo CJ, Schulick RD, Montgomery E, Maitra A. Expression of neuropilin-1 in high-grade dysplasia, invasive cancer, and metastases of the human gastrointestinal tract. Am J Surg Pathol 2004; 28:347-356. (Pubitemid 38269568)
24. Latil A, Bieche I, Pesche S, Valeri A, Fournier G, Cussenot O, Lidereau R. VEGF overexpression in clinically localized prostate tumors and neuropilin-1 overexpression in metastatic forms. Int J Cancer 2000; 89:167-171. (Pubitemid 30185926)
25. Berge M, Bonnin P, Sulpice E, Vilar J, Allanic D, Silvestre JS, et al. Small interfering RNAs induce target-independent inhibition of tumor growth and vasculature remodeling in a mouse model of hepatocellular carcinoma. Am J Pathol 2010; 177:3192-3201.
26. Raskopf E, Vogt A, Standop J, Sauerbruch T, Schmitz V. Inhibition of neuropilin-1 by RNA-interference and its angiostatic potential in the treatment of hepatocellular carcinoma. Z Gastroenterol 2010; 48:21-27.
27. Lu L, Zhang L, Xiao Z, Lu S, Yang R, Han ZC. Neuropilin-1 in acute myeloid leukemia: Expression and role in proliferation and migration of leukemia cells. Leuk Lymphoma 2008; 49:331-338. (Pubitemid 351193927)
28. Barr MP, Byrne AM, Duffy AM, Condron CM, Devocelle M, Harriott P, et al. A peptide corresponding to the neuropilin-1-binding site on VEGF(165) induces apoptosis of neuropilin-1-expressing breast tumour cells. Br J Cancer 2005; 92:328-333.
29. Tirand L, Frochot C, Vanderesse R, Thomas N, Trinquet E, Pinel S, et al. 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 2006; 111:153-164. (Pubitemid 43290004)
30. Jia H, Cheng L, Tickner M, Bagherzadeh A, Selwood D, Zachary I. Neuropilin-1 antagonism in human carcinoma cells inhibits migration and enhances chemosensitivity. Br J Cancer 2010; 102:541-552.
31. Starzec A, Ladam P, Vassy R, Badache S, Bouchemal N, Navaza A, et al. Structure-function analysis of the antiangiogenic ATWLPPR peptide inhibiting VEGF(165) binding to neuropilin-1 and molecular dynamics simulations of the ATWLPPR/neuropilin-1 complex. Peptides 2007; 28:2397-2402. (Pubitemid 350116304)
32. Bondeva T, Ruster C, Franke S, Hammerschmid E, Klagsbrun M, Cohen CD, et al. Advanced glycation end-products suppress neuropilin-1 expression in podocytes. Kidney Int 2009; 75:605-616.
33. Bondeva T,Wolf G. Advanced glycation end products suppress neuropilin-1 expression in podocytes by a reduction in Sp1-dependent transcriptional activity. Am J Nephrol 2009; 30:336-345.
34. Bondeva T, Wojciech S, Wolf G. Advanced glycation end products inhibit adhesion ability of differentiated podocytes in a neuropilin-1-dependent manner. Am J Physiol Renal Physiol 2011; 301:F852-F870.
35. Teesalu T, Sugahara KN, Kotamraju VR, Ruoslahti E. C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration. Proc Natl Acad Sci USA 2009; 106:16157-16162.
36. Haspel N, Zanuy D, Nussinov R, Teesalu T, Ruoslahti E, Aleman C. Binding of a C-end rule peptide to the neuropilin-1 receptor: A molecular modeling approach. Biochemistry 2011; 50:1755-1762.
37. Liang WC, Dennis MS, Stawicki S, Chanthery Y, Pan Q, Chen Y, et al. Function blocking antibodies to neuropilin-1 generated from a designed human synthetic antibody phage library. J Mol Biol 2007; 366:815-829. (Pubitemid 46175863)
38. Rossignol M, Gagnon ML, Klagsbrun M. Genomic organization of human neuropilin-1 and neuropilin-2 genes: Identification and distribution of splice variants and soluble isoforms. Genomics 2000; 70:211-222. (Pubitemid 32003398)
39. Joseph D, Ho SM, Syed V. Hormonal regulation and distinct functions of semaphorin-3B and semaphorin-3F in ovarian cancer. Mol Cancer Ther 2010; 9:499-509.
40. Glinka Y, Stoilova S, Mohammed N, Prud'homme GJ. Neuropilin-1 exerts coreceptor function for TGF-beta-1 on the membrane of cancer cells and enhances responses to both latent and active TGF-beta. Carcinogenesis 2011; 32:613-621.
41. Liu W, Parikh AA, Stoeltzing O, Fan F, McCarty MF, Wey J, et al. Upregulation of neuropilin-1 by basic fibroblast growth factor enhances vascular smooth muscle cell migration in response to VEGF. Cytokine 2005; 32:206-212. (Pubitemid 43144652)
42. Rizzolio S, Rabinowicz N, Rainero E, Lanzetti L, Serini G, Norman J, et al. Neuropilin-1-dependent regulation of EGF-receptor signaling. Cancer Res 2012; 72:5801-5811.
43. Valdembri D, Caswell PT, Anderson KI, Schwarz JP, Konig I, Astanina E, et al. Neuropilin-1/GIPC1 signaling regulates alpha5beta1 integrin traffic and function in endothelial cells. PLoS Biol 2009; 7:e25.
44. Zhao Y, Min C, Vora SR, Trackman PC, Sonenshein GE, Kirsch KH. The lysyl oxidase pro-peptide attenuates fibronectin-mediated activation of focal adhesion kinase and p130Cas in breast cancer cells. J Biol Chem 2009; 284:1385-1393.
45. Yaqoob U, Cao S, Shergill U, Jagavelu K, Geng Z, Yin M, et al. Neuropilin-1 stimulates tumor growth by increasing fibronectin fibril assembly in the tumor microenvironment. Cancer Res 2012; 72:4047-4059.
46. Li X, Luo F,Wang S, Ni E, Tang X, Lv H, et al. Monoclonal antibody against NRP-1 b1b2. Hybridoma (Larchmt) 2011; 30:369-373.
47. Carragher NO, Frame MC. Focal adhesion and actin dynamics: A place where kinases and proteases meet to promote invasion. Trends Cell Biol 2004; 14:241-249. (Pubitemid 38591328)
48. Nasarre P, Constantin B, Rouhaud L, Harnois T, Raymond G, Drabkin HA, et al. Semaphorin SEMA3F and VEGF have opposing effects on cell attachment and spreading. Neoplasia 2003; 5:83-92. (Pubitemid 36151061)
49. Timoshenko AV, Rastogi S, Lala PK. Migration-promoting role of VEGF-C and VEGF-C binding receptors in human breast cancer cells. Br J Cancer 2007; 97:1090-1098. (Pubitemid 47587011)
50. Chen L, Miao W, Tang X, Zhang H,Wang S, Luo F, Yan J. Inhibitory effect of neuropilin-1 monoclonal antibody (NRP-1 MAb) on glioma tumor in mice. J Biomed Nanotechnol 2013; 9:551-558.
51. Chen L, MiaoW, Tang X, Zhang H,Wang S, Luo F, Yan J. The expression and significance of neuropilin-1 (NRP-1) on glioma cell lines and glioma tissues. J Biomed Nanotechnol 2013; 9:559-563.
52. Christensen L. The distribution of fibronectin, laminin and tetranectin in human breast cancer with special attention to the extracellular matrix. APMIS Suppl 1992; 26:1-39.
53. Boettiger D. Mechanical control of integrin-mediated adhesion and signaling. Curr Opin Cell Biol 2012; 24:592-599.
54. Keely PJ. Mechanisms by which the extracellular matrix and integrin signaling act to regulate the switch between tumor suppression and tumor promotion. J Mammary Gland Biol Neoplasia 2011; 16:205-219.
55. Shimizu M, Murakami Y, Suto F, Fujisawa H. Determination of cell adhesion sites of neuropilin-1. J Cell Biol 2000; 148:1283-1293.
56. Playford MP, Schaller MD. The interplay between Src and integrins in normal and tumor biology. Oncogene 2004; 23:7928-7946. (Pubitemid 39468852)
57. Caron-Lormier G, Berry H. Amplification and oscillations in the FAK/Src kinase system during integrin signaling. J Theor Biol 2005; 232:235-248. (Pubitemid 39458051)
58. Wade R,Vande Pol S. Minimal features of paxillin that are required for the tyrosine phosphorylation of focal adhesion kinase. Biochem J 2006; 393:565-573. (Pubitemid 43099096).