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Roles of Neuropilins in Neuronal Development, Angiogenesis, and Cancers

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Abstract

Neuropilin-1 (NRP1) and neuropilin-2 (NRP2) are transmembrane glycoproteins that have been characterized as receptors for both semaphorins for neuronal guidance and vascular endothelial growth factor (VEGF) for angiogenesis. Biologic properties of NRPs have been linked to their unique domain structures. However, molecular interaction among NRPs, VEGF, and VEGF receptors is still not clear. Although several types of cancer cells can express NRPs, the role of NRPs in tumor pathogenesis is largely unknown. Thus, future investigations should include determining the effects and mechanisms of NRPs on proliferation, apoptosis, and migration of neuronal , endothelial, and cancer cells. Study of protein-protein interaction, signal transduction pathways, and NRP-mediated gene expression is particularly important to understand NRPs functions, which may have significant clinical applications in the treatment of neurological disorders, cardiovascular diseases, and certain cancers.

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References

  1. Y Luo D Raible JA Raper (1993) ArticleTitleCollapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones Cell 75 217–227 Occurrence Handle10.1016/0092-8674(93)80064-L Occurrence Handle1:CAS:528:DyaK2cXisFyjtg%3D%3D Occurrence Handle8402908

    Article  CAS  PubMed  Google Scholar 

  2. Z He M Tessier-Lavigne (1997) ArticleTitleNeuropilin is a receptor for the axonal chemorepellent semaphorin III Cell 90 739–751 Occurrence Handle10.1016/S0092-8674(00)80534-6 Occurrence Handle1:CAS:528:DyaK2sXlvFKmurw%3D Occurrence Handle9288753

    Article  CAS  PubMed  Google Scholar 

  3. AL Kolodkin DV Levengood EG Rowe et al. (1997) ArticleTitleNeuropilin is a semaphorin III receptor Cell 90 753–762 Occurrence Handle10.1016/S0092-8674(00)80535-8 Occurrence Handle1:CAS:528:DyaK2sXlvFKmur0%3D Occurrence Handle9288754

    Article  CAS  PubMed  Google Scholar 

  4. H Chen Z He A Bagri et al. (1998) ArticleTitleSemaphorin-neuropilin interactions underlying sympathetic axon responses to class III semaphorins Neuron 21 1283–1290 Occurrence Handle10.1016/S0896-6273(00)80648-0 Occurrence Handle1:CAS:528:DyaK1MXntV2gtA%3D%3D Occurrence Handle9883722

    Article  CAS  PubMed  Google Scholar 

  5. MJ Renzi L Feiner AM Koppel et al. (1999) ArticleTitleA dominant negative receptor for specific secreted semaphorins is generated by deleting an extracellular domain from neuropilin-1 J. Neurosci. 19 7870–7880 Occurrence Handle1:CAS:528:DyaK1MXlvFaht7k%3D Occurrence Handle10479689

    CAS  PubMed  Google Scholar 

  6. F Nakamura M Tanaka T Takahashi et al. (1998) ArticleTitleNeuropilin-1 extracellular domains mediate semaphorin D/III-induced growth cone collapse Neuron 21 1093–1100 Occurrence Handle10.1016/S0896-6273(00)80626-1 Occurrence Handle1:CAS:528:DyaK1cXotVSrtb4%3D Occurrence Handle9856464

    Article  CAS  PubMed  Google Scholar 

  7. RJ Giger ER Urquhart SK Gillespie et al. (1998) ArticleTitleNeuropilin-2 is a receptor for semaphorin IV: insight into the structural basis of receptor function and specificity Neuron 21 1079–1092 Occurrence Handle10.1016/S0896-6273(00)80625-X Occurrence Handle1:CAS:528:DyaK1cXotVSrtLY%3D Occurrence Handle9856463

    Article  CAS  PubMed  Google Scholar 

  8. T Takahashi A Founier F Nakamura et al. (1999) ArticleTitlePlexin-neuropilin-1 complexes form functional semaphorin-3A receptors Cell 99 59–69 Occurrence Handle10.1016/S0092-8674(00)80062-8 Occurrence Handle1:CAS:528:DyaK1MXmsleqs7k%3D Occurrence Handle10520994

    Article  CAS  PubMed  Google Scholar 

  9. S Takagi Y Kasuya M Shimizu et al. (1995) ArticleTitleExpression of a cell adhesion molecule, neuropilin, in the developing chick nervous system Dev. Biol. 170 207–222 Occurrence Handle10.1006/dbio.1995.1208 Occurrence Handle1:CAS:528:DyaK2MXmvVaiu74%3D Occurrence Handle7601310

    Article  CAS  PubMed  Google Scholar 

  10. M Shimizu Y Murakami F Suto et al. (2000) ArticleTitleDetermination of cell adhesion sites of neuropilin-1 J. Cell. Biol. 148 1283–1293 Occurrence Handle10.1083/jcb.148.6.1283 Occurrence Handle1:CAS:528:DC%2BD3cXitVaqtLk%3D Occurrence Handle10725340

    Article  CAS  PubMed  Google Scholar 

  11. H Chen A Chedotal Z He et al. (1997) ArticleTitleNeuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III Neuron 19 547–559 Occurrence Handle10.1016/S0896-6273(00)80371-2 Occurrence Handle1:CAS:528:DyaK2sXmvVKlsL4%3D Occurrence Handle9331348

    Article  CAS  PubMed  Google Scholar 

  12. M Rossignol ML Gagnon M Klagsbrun (2000) ArticleTitleGenomic organization of human neuropilin-1 and neuropilin-2 genes: identification and distribution of splice variants and soluble isoforms Genomics 70 211–222 Occurrence Handle10.1006/geno.2000.6381 Occurrence Handle1:CAS:528:DC%2BD3cXosF2iu7c%3D Occurrence Handle11112349

    Article  CAS  PubMed  Google Scholar 

  13. T Takahashi F Nakamura Z Jin et al. (1998) ArticleTitleSemaphorins A and E act as antagonists of neuropilin-1 and agonists of neuropilin-2 receptors Nat. Neurosci. 1 487–493 Occurrence Handle10.1038/2203 Occurrence Handle1:CAS:528:DyaK1cXmvF2kt7s%3D Occurrence Handle10196546

    Article  CAS  PubMed  Google Scholar 

  14. B Rohm A Ottemeyer M Lohrum et al. (2000) ArticleTitlePlexin/neuropilin complexes mediate repulsion by the axonal guidance signal semaphorin 3 A Mech. Dev. 93 95–104 Occurrence Handle10.1016/S0925-4773(00)00269-0 Occurrence Handle1:CAS:528:DC%2BD3cXislarurs%3D

    Article  CAS  Google Scholar 

  15. L Tamagnone S Artigiani H Chen et al. (1999) ArticleTitlePlexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates Cell 99 71–80 Occurrence Handle10.1016/S0092-8674(00)80063-X Occurrence Handle1:CAS:528:DyaK1MXmsleqs7Y%3D Occurrence Handle10520995

    Article  CAS  PubMed  Google Scholar 

  16. V Castellani A Chedotal M Schachner et al. (2000) ArticleTitleAnalysis of the L1-deficient mouse phenotype reveals cross-talk between Sema3A and LI signaling pathways in axonal guidance Neuron 27 237–249 Occurrence Handle10.1016/S0896-6273(00)00033-7 Occurrence Handle1:CAS:528:DC%2BD3cXmsVWmt74%3D Occurrence Handle10985345

    Article  CAS  PubMed  Google Scholar 

  17. KL Crossin LA Krushel (2000) ArticleTitleCellular signaling by neural cell adhesion molecules of the immunoglobulin superfamily Dev. Dyn. 218 260–279 Occurrence Handle10.1002/(SICI)1097-0177(200006)218:2<260::AID-DVDY3>3.0.CO;2-9 Occurrence Handle1:CAS:528:DC%2BD3cXks1Sksr4%3D Occurrence Handle10842356

    Article  CAS  PubMed  Google Scholar 

  18. B Millauer S Wizigmann-Voos H Schnurch et al. (1993) ArticleTitleHigh affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis Cell 72 835–846 Occurrence Handle10.1016/0092-8674(93)90573-9 Occurrence Handle1:CAS:528:DyaK3sXks1egsb8%3D Occurrence Handle7681362

    Article  CAS  PubMed  Google Scholar 

  19. N Ferrara WJ Henzel (1989) ArticleTitlePituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells Biochem. Biophys. Res. Commun. 161 851–858 Occurrence Handle10.1016/0006-291X(89)92678-8 Occurrence Handle1:CAS:528:DyaL1MXkslWhtbY%3D Occurrence Handle2735925

    Article  CAS  PubMed  Google Scholar 

  20. D Gospodarowicz K Lau (1989) ArticleTitlePituitary follicular cells secrete both vascular endothelial growth factor and follistatin Biochem. Biophys. Res. Commun. 165 292–298 Occurrence Handle10.1016/0006-291X(89)91068-1 Occurrence Handle1:CAS:528:DyaK3cXjtVOqsw%3D%3D Occurrence Handle2590228

    Article  CAS  PubMed  Google Scholar 

  21. RS Kerbel A Viloria-Petit F Okada et al. (1998) ArticleTitleEstablishing a link between oncogenes and tumor angiogenesis Mol. Med. 4 286–295 Occurrence Handle1:CAS:528:DyaK1cXkt1egs74%3D Occurrence Handle9642680

    CAS  PubMed  Google Scholar 

  22. T Veikkola K Alitalo (1999) ArticleTitleVEGFs, receptors and angiogenesis Semin. Cancer Biol. 9 211–220 Occurrence Handle10.1006/scbi.1998.0091 Occurrence Handle1:CAS:528:DyaK1MXjtlSktL4%3D Occurrence Handle10343072

    Article  CAS  PubMed  Google Scholar 

  23. T Veikkola M Karkkainen L Claesson-Welsh et al. (2000) ArticleTitleRegulation of angiogenesis via vascular endothelial growth factor receptors Cancer Res. 60 203–212 Occurrence Handle1:CAS:528:DC%2BD3cXhtVaiu7g%3D Occurrence Handle10667560

    CAS  PubMed  Google Scholar 

  24. CJ Robinson SE Stringer (2001) ArticleTitleThe splice variants of vascular endothelial growth factor (VEGF) and their receptors J. Cell. Sci. 114 853–865 Occurrence Handle1:CAS:528:DC%2BD3MXit1eit7c%3D Occurrence Handle11181169

    CAS  PubMed  Google Scholar 

  25. KA Houck DW Leung AM Rowland et al. (1992) ArticleTitleDual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms J. Biol. Chem. 267 26031–26037 Occurrence Handle1:CAS:528:DyaK38Xmt1OjsL8%3D Occurrence Handle1464614

    CAS  PubMed  Google Scholar 

  26. G Neufeld T Cohen S Gengrinovitch et al. (1999) ArticleTitleVascular endothelial growth factor (VEGF) and its receptors FASEB J. 13 9–22 Occurrence Handle1:CAS:528:DyaK1MXlt1ygsQ%3D%3D Occurrence Handle9872925

    CAS  PubMed  Google Scholar 

  27. T Veikkola M Karkkainen L Claesson-Welsh et al. (2000) ArticleTitleRegulation of angiogenesis via vascular endothelial growth factor receptors Cancer Res. 60 203–212 Occurrence Handle1:CAS:528:DC%2BD3cXhtVaiu7g%3D Occurrence Handle10667560

    CAS  PubMed  Google Scholar 

  28. G Fuh KC Garcia AM DeVos (2000) ArticleTitleThe interaction of neuropilin-1 with vascular endothelial growth factor and its receptor Flt-1 J. Biol. Chem. 275 26,690–26,695

    Google Scholar 

  29. Z Gluzman-Poltorak T Cohen Y Herzog et al. (2000) ArticleTitleNeuropilin-2 and neuropilin-1 are receptors for 165-amino acid long 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 18,040–18,045

    Google Scholar 

  30. U Eriksson K Alitalo (1999) ArticleTitleStructure, expression and receptor-binding properties of novel vascular endothelial growth factors Curr. Top. Microbiol. Immunol. 237 41–57 Occurrence Handle1:CAS:528:DyaK1MXitVKgsg%3D%3D Occurrence Handle9893345

    CAS  PubMed  Google Scholar 

  31. JE Park HH Chen J Winer et al. (1994) ArticleTitlePlacenta growth factor-potentiation of vascular endothelial growth factor bioactivity, in vitro and in vivo, and high affinity binding to Flt-1 but not to Flk-1/KDR J. Biol. Chem. 269 25,646–25,654

    Google Scholar 

  32. V Joukov K Pajusola A Kaipainen et al. (1996) ArticleTitleA novel vascular endothelial rowth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases EMBO J. 15 290–298 Occurrence Handle1:CAS:528:DyaK28XovFSktA%3D%3D Occurrence Handle8617204

    CAS  PubMed  Google Scholar 

  33. M Jeltsch A Kaipainen V Joukov et al. (1997) ArticleTitleHyperplasia of lymphatic vessels in VEGF-C transgenic mice Science. 276 1423–1425 Occurrence Handle1:CAS:528:DyaK2sXjsFOjtLY%3D Occurrence Handle9162011

    CAS  PubMed  Google Scholar 

  34. L Seetharam N Gotoh Y Maru et al. (1995) ArticleTitleA unique signal transduction from FLT tyrosine kinase, a receptor for vascular endothelial growth factor VEGF Oncogene 10 135–147 Occurrence Handle1:CAS:528:DyaK2MXjtVOqsrc%3D Occurrence Handle7824266

    CAS  PubMed  Google Scholar 

  35. A Sawano T Takahashi S Yamaguchi et al. (1996) ArticleTitleFlt-1 but not KDR/Flk-1 tyrosine kinase is a receptor for placenta growth factor (PLGF), which is related to vascular endothelial growth factor (VEGF) Cell Growth Differ. 7 213–221 Occurrence Handle1:CAS:528:DyaK28XhtVaisLs%3D Occurrence Handle8822205

    CAS  PubMed  Google Scholar 

  36. S Soker H Fidder G Neufeld et al. (1996) ArticleTitleCharacterization of novel vascular endothelial growth factor (VEGF) receptors on tumor cells that bind VEGF165 via its exon 7-encoded domain J. Biol. Chem. 271 5761–5767 Occurrence Handle1:CAS:528:DyaK28XhsFeht7Y%3D Occurrence Handle8621443

    CAS  PubMed  Google Scholar 

  37. S Soker S Takashima HQ Miao et al. (1998) ArticleTitleNeuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor Cell 92 735–745 Occurrence Handle10.1016/S0092-8674(00)81402-6 Occurrence Handle1:CAS:528:DyaK1cXit1KlsL0%3D Occurrence Handle9529250

    Article  CAS  PubMed  Google Scholar 

  38. G Neufeld T Cohen N Shraga et al. (2002) ArticleTitleThe neuropilins: multifunctional semaphorin and VEGF receptors that modulate axon guidance and angiogenesis Trends Cardiovasc. Med. 12 13–19 Occurrence Handle1:CAS:528:DC%2BD38XktFWqsw%3D%3D Occurrence Handle11796239

    CAS  PubMed  Google Scholar 

  39. GB Whitaker BJ Limberg JS Rosenbaum (2001) ArticleTitleVEGFR-2 and neuropilin-1 form a receptor complex that is responsible for the differential signaling potency of VEGF165 and VEGF121 J Biol. Chem. 276 25,520–25,531

    Google Scholar 

  40. H Chen A Bagri JA Zupicich et al. (2000) ArticleTitleNeuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections Neuron 25 43–56 Occurrence Handle10707971

    PubMed  Google Scholar 

  41. Z Gluzman-Poltorak T Cohen M Shibuya et al. (2001) ArticleTitleVascular endothelial growth factor receptor-1 (VEGFR-1) and neuropilin-2 form complexes J. Biol. Chem. 276 18,688–18,694

    Google Scholar 

  42. M Migdal B Huppertz S Tessler et al. (1998) ArticleTitleNeuropilin-1 is a placenta growth factor-2 receptor J. Biol. Chem. 273 22,272–22,278

    Google Scholar 

  43. T Makinen B Olofsson T Karpanen et al. (1999) ArticleTitleDifferential binding of vascular en-dothelial growth factor B splice and proteolytic isoforms to neuropilin-1 J. Biol. Chem. 274 21,217–21,222

    Google Scholar 

  44. BA Keyt HV Nguyen LT Berleau et al. (1996) ArticleTitleIdentification of vascular endothelial growth factor determinants for binding KDR and FLT-1 receptors: generation of receptor-selective VEGF variants by site-directed mutagenesis J. Biol. Chem. 271 5638–5646 Occurrence Handle1:CAS:528:DyaK28XhsFehtrw%3D Occurrence Handle8621427

    CAS  PubMed  Google Scholar 

  45. T Kitsukawa A Shimono A Kawakami et al. (1995) ArticleTitleOverexpression of a membrane protein, neuropilin, in chimeric mice causes anomalies in the cardiovascular system, nervous system and limbs Development 121 4309–4318 Occurrence Handle1:CAS:528:DyaK28XhvFWjtg%3D%3D Occurrence Handle8575331

    CAS  PubMed  Google Scholar 

  46. ML Gagnon DR Bielenberg Z Gechtman et al. (2000) ArticleTitleIdentification of a natural soluble neuropilin-1 that binds vascular endothelial growth factor: in vivo expression and antitumor activity Proc. Natl. Acad. Sci. U.S.A. 25 2573–2578

    Google Scholar 

  47. T Kawasaki T Kitsukawa Y Bekku et al. (1999) ArticleTitleA requirement for neuropilin-1 in embryonic vessel formation Development 126 4895–4902 Occurrence Handle1:CAS:528:DyaK1MXns1Kju7s%3D Occurrence Handle10518505

    CAS  PubMed  Google Scholar 

  48. Y Yamada N Takakura H Yasue et al. (2001) ArticleTitleExogenous clustered neuropilin 1 enhances vasculogenesis and angiogenesis Blood 97 1671–1678 Occurrence Handle1:CAS:528:DC%2BD3MXitFaltL8%3D Occurrence Handle11238106

    CAS  PubMed  Google Scholar 

  49. HQ Miao S Soker L Feiner et al. (1999) ArticleTitleNeuropilin-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 Occurrence Handle1:CAS:528:DyaK1MXksFCjs7c%3D Occurrence Handle10402473

    CAS  PubMed  Google Scholar 

  50. O Behar JA Golden H Mashimo et al. (1996) ArticleTitleSemaphorin III is needed for normal patterning and growth of nerves, bones and heart Nature 383 525–528 Occurrence Handle1:CAS:528:DyaK28Xmt1Gku7g%3D Occurrence Handle8849723

    CAS  PubMed  Google Scholar 

  51. A Latil I Bieche S Pesche et al. (2000) ArticleTitleVEGF overexpression in clinically localized prostate tumours and neuropilin-1 overexpression in metastatic forms Int. J. Cancer 89 167–171 Occurrence Handle1:CAS:528:DC%2BD3cXislehs78%3D Occurrence Handle10754495

    CAS  PubMed  Google Scholar 

  52. H Miao P Lee H Lin et al. (2000) ArticleTitleNeuropilin-1 expression by tumour cells promotes tumour angiogenesis and progression FASEB J. 14 2532–2539 Occurrence Handle1:CAS:528:DC%2BD3MXht1SntLs%3D Occurrence Handle11099472

    CAS  PubMed  Google Scholar 

  53. RE Bachelder MA Wendt AM Mercurio (2002) ArticleTitleVascular endothelial growth factor promotes breast carcinoma invasion in an autocrine manner by regulating the chemokine receptor CXCR4 Cancer Res. 62 7203–7206 Occurrence Handle1:CAS:528:DC%2BD3sXhtVyruw%3D%3D Occurrence Handle12499259

    CAS  PubMed  Google Scholar 

  54. RE Bachelder A Crago J Chung et al. (2001) ArticleTitleVascular endothelial growth factor is an autocrine survival factor for neuropilin-expressing breast carcinoma cells Cancer Res. 61 5736–5740 Occurrence Handle1:CAS:528:DC%2BD3MXlvVCgtLk%3D Occurrence Handle11479209

    CAS  PubMed  Google Scholar 

  55. JM Stephenson S Banergjee NK Saxena et al. (2002) ArticleTitleNeuropilin-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. 101 409–414 Occurrence Handle1:CAS:528:DC%2BD38Xnt1ehsr0%3D Occurrence Handle12216067

    CAS  PubMed  Google Scholar 

  56. SK Banerjee MN Zoubine TM Tran et al. (2000) ArticleTitleOverexpression of vascular endothelial growth factor 164 and its co-receptor neurpilin-1 in estrogen-induced rat pituitary tumors and GH3 rat pituitary tumor cells Int. J. Oncol. 16 253–260 Occurrence Handle1:CAS:528:DC%2BD3cXotVCqtA%3D%3D Occurrence Handle10639567

    CAS  PubMed  Google Scholar 

  57. H Ding X Wu L Roncari et al. (2000) ArticleTitleExpression and regulation of neuropilin-1 in human astrocytomas Int. J. Cancer. 88 584–592 Occurrence Handle1:CAS:528:DC%2BD3cXotVKit7w%3D Occurrence Handle11058875

    CAS  PubMed  Google Scholar 

  58. M Fakhari D Pullirsch D Abraham et al. (2002) ArticleTitleSelective upregulation of vascular endothelial growth factor receptors neuropilin-1 and -2 in human neuroblastoma Cancer 94 258–563 Occurrence Handle1:CAS:528:DC%2BD38XlslKntg%3D%3D Occurrence Handle11815985

    CAS  PubMed  Google Scholar 

  59. S Lantuejoul B Constantin H Drabkin et al. (2003) ArticleTitleExpression of VEGF, smaphorin SEMA3F, and their common receptors neuropilins NP1 and NP2 in preinvasive bronchial lesions, lung tumours, and cell lines J. Pathol. 200 336–347 Occurrence Handle1:CAS:528:DC%2BD3sXnvF2nsro%3D Occurrence Handle12845630

    CAS  PubMed  Google Scholar 

  60. T Kawakami T Tokunaga H Hatanaka et al. (2002) ArticleTitleNeuropilin 1 and neuropilin 2 co-expression is significantly correlated with increased vascularity and poor prognosis in nonsmall cell lung carcinoma Cancer 95 2196–2201 Occurrence Handle1:CAS:528:DC%2BD38XptVKnurs%3D Occurrence Handle12412174

    CAS  PubMed  Google Scholar 

  61. A Handa T Tokunaga T Tsuchida et al. (2000) ArticleTitleNeuropilin-2 expression affects the increased vascularization and is a prognostic factor in osteosarcoma Int. J. Oncol. 17 291–295 Occurrence Handle1:CAS:528:DC%2BD3cXls1Klurg%3D Occurrence Handle10891538

    CAS  PubMed  Google Scholar 

  62. M Sanchez-Carbayo ND Socci JJ Lozano W Li et al. (2003) ArticleTitleGene discovery in bladder cancer progression using cDNA microarrags Am. J. Pathol. 163 505–516 Occurrence Handle1:CAS:528:DC%2BD3sXmslSnsL8%3D Occurrence Handle12875971

    CAS  PubMed  Google Scholar 

  63. T Cohen Y Herzog A Brodzky et al. (2002) ArticleTitleNeuropilin-2 is a novel marker expressed in pancreatic islet cells and endocrine pancreatic tumours J. Pathol. 198 77–82 Occurrence Handle1:CAS:528:DC%2BD38Xns1Wiurk%3D Occurrence Handle12210066

    CAS  PubMed  Google Scholar 

  64. AA Parikh WB Liu F Fan et al. (2003) ArticleTitleExpression and regulation of the novel vascular endothelial growth factor receptor neuropilin-1 by epidermal growth factor in human pancreatic carcinoma Cancer 98 720–729 Occurrence Handle1:CAS:528:DC%2BD3sXntVWgur4%3D Occurrence Handle12910515

    CAS  PubMed  Google Scholar 

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Acknowledgment

This work was supported by National Institutes of Health Grants R01 HL61943 (C.C), R01 HL60135 (C.C), R01 HL65916 (C.C.), Methodist 39935 (M.L.), R01 HL72716 (C.C.), K08 CA85822 (W.F.), R13 CA101889 (F.C.B.), R21 AI 49116 (Q.Y.), and R01 DE015543 (Q.Y.).

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Chen, C., Li, M., Chai, H. et al. Roles of Neuropilins in Neuronal Development, Angiogenesis, and Cancers. World J. Surg. 29, 271–275 (2005). https://doi.org/10.1007/s00268-004-7818-1

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