Neuropilins: Expression and roles in the epithelium

International Journal of Experimental Pathology

Volumn 93, Issue 2, 2012, Pages 81-103

  Wild, Jonathan R L ^a   Staton, Carolyn A ^a   Chapple, Keith ^b   Corfe, Bernard M ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b SHEFFIELD TEACHING HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Epithelium; Neuropilin; Neuropilin 1; Neuropilin 2; Semaphorin; Vascular endothelial growth factor

Indexed keywords

ANTITHROMBIN III; BETA1 INTEGRIN; ESTROGEN RECEPTOR BETA; FIBROBLAST GROWTH FACTOR; FOCAL ADHESION KINASE; HEMOPOIETIC GROWTH FACTOR; HYPOXIA INDUCIBLE FACTOR 1; INTERLEUKIN 1BETA; LIM KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE; NEUROPILIN; NEUROPILIN 1; NEUROPILIN 2; ONCOSTATIN M; P21 ACTIVATED KINASE; PLATELET DERIVED ENDOTHELIAL CELL GROWTH FACTOR; PRION PROTEIN; PROLACTIN; PROTEIN KINASE B; RAF PROTEIN; SEMAPHORIN; SONIC HEDGEHOG PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UNINDEXED DRUG; VASCULOTROPIN; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ANGIOGENESIS; APOPTOSIS; CANCER GROWTH; CANCER INVASION; CANCER PROGNOSIS; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; ENZYME ACTIVATION; EPITHELIUM; EPITHELIUM CELL; FIBROSIS; HUMAN; LYMPHANGIOGENESIS; LYMPHOCYTE ACTIVATION; METASTASIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

EPITHELIUM; HUMANS; NEOPLASM INVASIVENESS; NEOPLASMS; NEUROPILIN-1; NEUROPILIN-2; PROTEIN STRUCTURE, TERTIARY; TUMOR MARKERS, BIOLOGICAL;

EID: 84858256282     PISSN: 09599673     EISSN: 13652613     Source Type: Journal    
DOI: 10.1111/j.1365-2613.2012.00810.x     Document Type: Review

References (237)

1. Abramow-Newerly M., Roy A.A. et al. (2006) RGS proteins have a signalling complex: interactions between RGS proteins and GPCRs, effectors, and auxiliary proteins. Cell. Signal. 18, 579-591.
2. Akagi M., Kawaguchi M. et al. (2003) Induction of neuropilin-1 and vascular endothelial growth factor by epidermal growth factor in human gastric cancer cells. Br. J. Cancer 88, 796-802.
3. Antipenko A., Himanen J.P. et al. (2003) Structure of the semaphorin-3A receptor binding module. Neuron 39, 589-598.
4. Apodaca G., Kiss S. et al. (2003) Disruption of bladder epithelium barrier function after spinal cord injury. Am. J. Physiol. Renal Physiol. 284, F966-F976.
5. Baba T., Kariya M. et al. (2007) Neuropilin-1 promotes unlimited growth of ovarian cancer by evading contact inhibition. Gynecol. Oncol. 105, 703-711.
6. Bachelder R.E., Lipscomb E.A. et al. (2003) Competing autocrine pathways involving alternative neuropilin-1 ligands regulate chemotaxis of carcinoma cells. Cancer Res. 63, 5230-5233.
7. Bagri A., Tessier-Lavigne M. et al. (2009) Neuropilins in tumor biology. Clin. Cancer Res. 15, 1860-1864.
8. Ball S.G., Bayley C. et al. (2010) Neuropilin-1 regulates platelet-derived growth factor receptor signalling in mesenchymal stem cells. Biochem. J. 427, 29-40.
9. Banerjee S., Sengupta K. et al. (2006) Breast cancer cells secreted platelet-derived growth factor-induced motility of vascular smooth muscle cells is mediated through neuropilin-1. Mol. Carcinog. 45, 871-880.
10. Barr M.P., Bouchier-Hayes D.J. et al. (2008) Vascular endothelial growth factor is an autocrine survival factor for breast tumour cells under hypoxia. Int. J. Oncol. 32, 41-48.
11. Bates D.O. & Harper S.J. (2002) Regulation of vascular permeability by vascular endothelial growth factors. Vascul. Pharmacol. 39, 225-237.
12. Berge M., Allanic D. et al. (2011) Neuropilin-1 is upregulated in hepatocellular carcinoma and contributes to tumour growth and vascular remodelling. J. Hepatol. 55, 866-875.
13. Bielenberg D.R., Hida Y. et al. (2004) Semaphorin 3F, a chemorepulsant for endothelial cells, induces a poorly vascularized, encapsulated, nonmetastatic tumor phenotype. J. Clin. Invest. 114, 1260-1271.
14. Bielenberg D., Pettaway C. et al. (2006) Neuropilins in neoplasms: expression, regulation, and function. Exp. Cell Res. 312, 584-593.
15. Birchmeier C., Birchmeier W. et al. (2003) Met, metastasis, motility and more. Nat. Rev. Mol. Cell Biol. 4, 915-925.
16. Bluff J.E., Menakuru S.R. et al. (2009) Angiogenesis is associated with the onset of hyperplasia in human ductal breast disease. Br. J. Cancer 101, 666-672.
17. Bondeva T. & Wolf G. (2009) Advanced glycation end products suppress neuropilin-1 expression in podocytes by a reduction in Sp1-dependent transcriptional activity. Am. J. Nephrol. 30, 336-345.
18. Bondeva T., Ruster C. et al. (2009) Advanced glycation end-products suppress neuropilin-1 expression in podocytes. Kidney Int. 75, 605-616.
19. Braet F., Shleper M. et al. (2004) Liver sinusoidal endothelial cell modulation upon resection and shear stress in vitro. Comp. Hepatol. 3, 7.
20. Brown L.F., Berse B. et al. (1993) Expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in adenocarcinomas of the gastrointestinal tract. Cancer Res. 53, 4727-4735.
21. Cackowski F.C., Xu L. et al. (2004) Identification of two novel alternatively spliced Neuropilin-1 isoforms. Genomics 84, 82-94.
22. Cai H. & Reed R.R. (1999) 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.
23. Cai Y., Wang R. et al. (2010) Expression of Neuropilin-2 in salivary adenoid cystic carcinoma: its implication in tumor progression and angiogenesis. Pathol. Res. Pract. 206, 793-799.
24. Cao Y., Wang L. et al. (2008) Neuropilin-1 upholds dedifferentiation and propagation phenotypes of renal cell carcinoma cells by activating akt and sonic hedgehog axes. Cancer Res. 68, 8667-8672.
25. Cao S., Yaqoob U. et al. (2010a) Neuropilin-1 promotes cirrhosis of the rodent and human liver by enhancing PDGF/TGF-beta signaling in hepatic stellate cells. J. Clin. Invest. 120, 2379-2394.
26. Cao Y., Szabolcs A. et al. (2010b) Neuropilin-1 mediates divergent R-Smad signaling and the myofibroblast phenotype. J. Biol. Chem. 285, 31840-31848.
27. Castro-Rivera E., Ran S. et al. (2004) Semaphorin 3B (SEMA3B) induces apoptosis in lung and breast cancer, whereas VEGF165 antagonizes this effect. Proc. Natl. Acad. Sci. U S A 101, 11432-11437.
28. Catalano A., Caprari P. et al. (2004) Cross-talk between vascular endothelial growth factor and semaphorin-3A pathway in the regulation of normal and malignant mesothelial cell proliferation. FASEB J. 18, 358-360.
29. Caunt M., Mak J. et al. (2008) Blocking neuropilin-2 function inhibits tumor cell metastasis. Cancer Cell 13, 331-342.
30. Chen H., Chedotal A. et al. (1997) Neuropilin-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.
31. Chen H., He Z. et al. (1998) Semaphorin-neuropilin interactions underlying sympathetic axon responses to class III semaphorins. Neuron 21, 1283-1290.
32. Cheppudira B.P., Girard B.M. et al. (2008) Upregulation of vascular endothelial growth factor isoform VEGF-164 and receptors (VEGFR-2, Npn-1, and Npn-2) in rats with cyclophosphamide-induced cystitis. Am. J. Physiol. Renal Physiol. 295, F826-F836.
33. Ciulla T.A. & Rosenfeld P.J. (2009) Antivascular endothelial growth factor therapy for neovascular age-related macular degeneration. Curr. Opin. Ophthalmol. 20, 158-165.
34. Cohen T. (2001) Neuroendocrine cells along the digestive tract express neuropilin-2. Biochem. Biophys. Res. Commun. 284, 395-403.
35. Cohen T., Herzog Y. et al. (2002) Neuropilin-2 is a novel marker expressed in pancreatic islet cells and endocrine pancreatic tumours. J. Pathol. 198, 77-82.
36. Cui J.Z., Hinz B.J. et al. (2003) Expression of neuropilin-1 in choroidal neovascular membranes. Can. J. Ophthalmol. 38, 41-45.
37. De Smaele E., Ferretti E. et al. (2010) Vismodegib, a small-molecule inhibitor of the hedgehog pathway for the treatment of advanced cancers. Curr. Opin. Investig. Drugs 11, 707-718.
38. Defilippi P., Di Stefano P. et al. (2006) p130Cas: a versatile scaffold in signaling networks. Trends Cell Biol. 16, 257-263.
39. Demetri G.D., van Oosterom A.T. et al. (2006) Efficacy and safety of sunitinib in patients with advanced gastrointestinal stromal tumour after failure of imatinib: a randomised controlled trial. Lancet 368, 1329-1338.
40. Desgrosellier J.S. & Cheresh D.A. (2010) Integrins in cancer: biological implications and therapeutic opportunities. Nat. Rev. Cancer 10, 9-22.
41. Detmar M., Brown L.F. et al. (1994) Overexpression of vascular permeability factor/vascular endothelial growth factor and its receptors in psoriasis. J. Exp. Med. 180, 1141-1146.
42. Ding S., Merkulova-Rainon T. et al. (2003) HGF receptor up-regulation contributes to the angiogenic phenotype of human endothelial cells and promotes angiogenesis in vitro. Blood 101, 4816-4822.
43. Dormoy V., Danilin S. et al. (2009) The sonic hedgehog signaling pathway is reactivated in human renal cell carcinoma and plays orchestral role in tumor growth. Mol. Cancer 8, 123.
44. Drenberg C.D., Livingston S. et al. (2009) Expression of Semaphorin 3F and its receptors in epithelial ovarian cancer, fallopian tubes, and secondary Müllerian tissues. Obstet. Gynecol. Int. 2009, 1-9.
45. Eichholz A., Merchant S. et al. (2010) Anti-angiogenesis therapies: their potential in cancer management. Onco Targets Ther. 3, 69-82.
46. Eremina V. & Quaggin S.E. (2004) The role of VEGF-A in glomerular development and function. Curr. Opin. Nephrol. Hypertens. 13, 9-15.
47. Escudier B., Eisen T. et al. (2007a) Sorafenib in advanced clear-cell renal-cell carcinoma. N. Engl. J. Med. 356, 125-134.
48. Escudier B., Pluzanska A. et al. (2007b) Bevacizumab plus interferon alfa-2a for treatment of metastatic renal cell carcinoma: a randomised, double-blind phase III trial. Lancet 370, 2103-2111.
49. Evans I.M., Yamaji M. et al. (2011) Neuropilin-1 signaling through p130Cas tyrosine phosphorylation is essential for growth factor-dependent migration of glioma and endothelial cells. Mol. Cell. Biol. 31, 1174-1185.
50. Favre C.J., Mancuso M. et al. (2003) Expression of genes involved in vascular development and angiogenesis in endothelial cells of adult lung. Am. J. Physiol. Heart Circ. Physiol. 285, H1917-H1938.
51. Feurino L.W., Zhang Y. et al. (2007) IL-6 stimulates Th2 type cytokine secretion and upregulates VEGF and NRP-1 expression in pancreatic cancer cells. Cancer Biol. Ther. 6, 1096-1100.
52. Finley D.J., Arora N. et al. (2004) Molecular profiling distinguishes papillary carcinoma from benign thyroid nodules. J. Clin. Endocrinol. Metab. 89, 3214-3223.
53. Foster R.R., Hole R. et al. (2003) Functional evidence that vascular endothelial growth factor may act as an autocrine factor on human podocytes. Am. J. Physiol. Renal Physiol. 284, F1263-F1273.
54. Fukahi K., Fukasawa M. et al. (2004) Aberrant expression of neuropilin-1 and -2 in human pancreatic cancer cells. Clin. Cancer Res. 10, 581-590.
55. Fukasawa M., Matsushita A. et al. (2007) Neuropilin-1 interacts with integrin beta1 and modulates pancreatic cancer cell growth, survival and invasion. Cancer Biol. Ther. 6, 1173-1180.
56. Gagnon M.L., Bielenberg D.R. et al. (2000) Identification 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 97, 2573-2578.
57. Galizia G., Lieto E. et al. (2004) Determination of molecular marker expression can predict clinical outcome in colon carcinomas. Clin. Cancer Res. 10, 3490-3499.
58. Genentech. (2009). A Phase Ib, Open-Label, Dose-Escalation Study of the Safety and Pharmacology of MNRP1685A, a Human IgG1 Antibody, in Combination With Bevacizumab With or Without Paclitaxel in Patients With Locally Advanced or Metastatic Solid Tumors. Retrieved 1/10/2011, 2011.
59. Gerber H.P., Hillan K.J. et al. (1999) VEGF is required for growth and survival in neonatal mice. Development 126, 1149-1159.
60. Geretti E. & Klagsbrun M. (2007) Neuropilins: novel targets for anti-angiogenesis therapies. Cell Adh. Migr. 1, 56-61.
61. Ghosh S., Sullivan C.A. et al. (2008) High levels of vascular endothelial growth factor and its receptors (VEGFR-1, VEGFR-2, neuropilin-1) are associated with worse outcome in breast cancer. Hum. Pathol. 39, 1835-1843.
62. Giger R.J., Cloutier J.F. et al. (2000) Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins. Neuron 25, 29-41.
63. Gitler A.D., Lu M.M. et al. (2004) PlexinD1 and semaphorin signaling are required in endothelial cells for cardiovascular development. Dev. Cell 7, 107-116.
64. Glinka Y. & Prud'homme G.J. (2008) Neuropilin-1 is a receptor for transforming growth factor beta-1, activates its latent form, and promotes regulatory T cell activity. J. Leukoc. Biol. 84, 302-310.
65. Gluzman-Poltorak Z., Cohen T. et al. (2000) Neuropilin-2 is a receptor for the vascular endothelial growth factor (VEGF) forms VEGF-145 and VEGF-165. J. Biol. Chem. 275, 29922.
66. Goel H.L., Bae D. et al. (2011) Neuropilin-2 promotes branching morphogenesis in the mouse mammary gland. Development 138, 2969-2976.
67. Gomez Roman J.J., Garay G.O. et al. (2008) Plexin B1 is downregulated in renal cell carcinomas and modulates cell growth. Transl. Res. 151, 134-140.
68. Grandclement C., Pallandre J.R. et al. (2011) Neuropilin-2 expression promotes TGF-beta1-mediated epithelial to mesenchymal transition in colorectal cancer cells. PLoS ONE 6, e20444.
69. Gray M.J., Wey J.S. et al. (2005) Neuropilin-1 suppresses tumorigenic properties in a human pancreatic adenocarcinoma cell line lacking neuropilin-1 coreceptors. Cancer Res. 65, 3664-3670.
70. Gray M.J., Van Buren G. et al. (2008) Therapeutic targeting of neuropilin-2 on colorectal carcinoma cells implanted in the murine liver. J. Natl Cancer Inst. 100, 109-120.
71. Gu C., Limberg B.J. et al. (2002) Characterization of neuropilin-1 structural features that confer binding to semaphorin 3A and vascular endothelial growth factor 165. J. Biol. Chem. 277, 18069-18076.
72. Gu C., Yoshida Y. et al. (2005) Semaphorin 3E and plexin-D1 control vascular pattern independently of neuropilins. Science 307, 265-268.
73. Gulubova M. & Vlaykova T. (2008) Chromogranin A-, serotonin-, synaptophysin- and vascular endothelial growth factor-positive endocrine cells and the prognosis of colorectal cancer: an immunohistochemical and ultrastructural study. J. Gastroenterol. Hepatol. 23, 1574-1585.
74. Guttmann-Raviv N., Shraga-Heled N. et al. (2007) Semaphorin-3A and semaphorin-3F work together to repel endothelial cells and to inhibit their survival by induction of apoptosis. J. Biol. Chem. 282, 26294-26305.
75. Haixia D., Jingsong Z. et al. (2010) Gene expression of neuropilin-1 and its receptors, VEGF/Semaphorin 3a, in normal and cancer cells. Cell Biochem. Biophys. 59, 39-47.
76. Hall G.H., Turnbull L.W. et al. (2005) Neuropilin-1 and VEGF correlate with somatostatin expression and microvessel density in ovarian tumours. Int. J. Oncol. 27, 1283-1288.
77. Handa A., Tokunaga T. et al. (2000) Neuropilin-2 expression affects the increased vascularization and is a prognostic factor in osteosarcoma. Int. J. Oncol. 17, 291-295.
78. Hansel D.E., Wilentz R.E. et al. (2004) Expression of neuropilin-1 in high-grade dysplasia, invasive cancer, and metastases of the human gastrointestinal tract. Am. J. Surg. Pathol. 28, 347-356.
79. Harper S.J., Xing C.Y. et al. (2001) Expression of neuropilin-1 by human glomerular epithelial cells in vitro and in vivo. Clin. Sci. 101, 439-446.
80. Hasan N.M., Kendrick M.A. et al. (2010) Genetic association of the neuropilin-1 gene with type 1 diabetes in children: neuropilin-1 expression in pancreatic islets. Diabetes Res. Clin. Pract. 87, e29-e32.
81. Henno A., Blacher S. et al. (2010) Histological and transcriptional study of angiogenesis and lymphangiogenesis in uninvolved skin, acute pinpoint lesions and established psoriasis plaques: an approach of vascular development chronology in psoriasis. J. Dermatol. Sci. 57, 162-169.
82. Herman J.G. & Meadows G.G. (2007) Increased class 3 semaphorin expression modulates the invasive and adhesive properties of prostate cancer cells. Int. J. Oncol. 30, 1231-1238.
83. Hillman R.T., Feng B.Y. et al. (2011) Neuropilins are positive regulators of Hedgehog signal transduction. Genes Dev. 25, 2333-2346.
84. Hochman E., Castiel A. et al. (2006) Molecular Pathways Regulating Pro-migratory Effects of Hedgehog Signaling. J. Biol. Chem. 281, 33860-33870.
85. Hsieh S.H., Ying N.W. et al. (2008) Galectin-1, a novel ligand of neuropilin-1, activates VEGFR-2 signaling and modulates the migration of vascular endothelial cells. Oncogene 27, 3746-3753.
86. Hu B., Guo P. et al. (2007) Neuropilin-1 promotes human glioma progression through potentiating the activity of the HGF/SF autocrine pathway. Oncogene 26, 5577-5586.
87. Hung R.J. & Terman J.R. (2011) Extracellular inhibitors, repellents, and semaphorin/plexin/MICAL-mediated actin filament disassembly. Cytoskeleton (Hoboken) 68, 415-433.
88. Hurwitz H., Fehrenbacher L. et al. (2004) Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N. Engl. J. Med. 350, 2335-2342.
89. Hynes R.O. (2007) Cell-matrix adhesion in vascular development. J. Thromb. Haemost. 5(Suppl 1), 32-40.
90. Ito T., Kagoshima M. et al. (2000) Repulsive axon guidance molecule Sema3A inhibits branching morphogenesis of fetal mouse lung. Mech. Dev. 97, 35-45.
91. Jackson M.W., Roberts J.S. et al. (2002) A potential autocrine role for vascular endothelial growth factor in prostate cancer. Cancer Res. 62, 854-859.
92. Jain R.K. (2003) Molecular regulation of vessel maturation. Nat. Med. 9, 685-693.
93. Jain R.K. (2005) Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307, 58-62.
94. Jia H., Bagherzadeh A. 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.
95. Jia H., Cheng L. et al. (2010) Neuropilin-1 antagonism in human carcinoma cells inhibits migration and enhances chemosensitivity. Br. J. Cancer 102, 541-552.
96. Jiang W.G., Martin T.A. et al. (2005) Hepatocyte growth factor, its receptor, and their potential value in cancer therapies. Crit. Rev. Oncol. Hematol. 53, 35-69.
97. Jin Q., Alkhatib B. et al. (2010) Alternate receptor usage of neuropilin-1 and glucose transporter protein 1 by the human T cell leukemia virus type 1. Virology 396, 203-212.
98. Kagoshima M. & Ito T. (2001) Diverse gene expression and function of semaphorins in developing lung: positive and negative regulatory roles of semaphorins in lung branching morphogenesis. Genes Cells 6, 559-571.
99. Kalluri R. & Weinberg R.A. (2009) The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119, 1420-1428.
100. Kamiya T., Kawakami T. et al. (2006) The preserved expression of neuropilin (NRP) 1 contributes to a better prognosis in colon cancer. Oncol. Rep. 15, 369-373.
101. Kanellis J., Fraser S. et al. (2000) Vascular endothelial growth factor is a survival factor for renal tubular epithelial cells. Am. J. Physiol. Renal Physiol. 278, F905-F915.
102. Karihaloo A., Karumanchi S.A. et al. (2005) Vascular endothelial growth factor induces branching morphogenesis/tubulogenesis in renal epithelial cells in a neuropilin-dependent fashion. Mol. Cell. Biol. 25, 7441-7448.
103. Karpanen T., Heckman C.A. et al. (2006) Functional interaction of VEGF-C and VEGF-D with neuropilin receptors. FASEB J. 20, 1462-1472.
104. Kasahara Y., Tuder R.M. et al. (2000) Inhibition of VEGF receptors causes lung cell apoptosis and emphysema. J. Clin. Invest. 106, 1311-1319.
105. Kawakami T., Tokunaga T. et al. (2002) Neuropilin 1 and neuropilin 2 co-expression is significantly correlated with increased vascularity and poor prognosis in nonsmall cell lung carcinoma. Cancer 95, 2196-2201.
106. Kawamura H., Li X. et al. (2008) Neuropilin-1 in regulation of VEGF-induced activation of p38MAPK and endothelial cell organization. Blood 112, 3638-3649.
107. Kawasaki T., Kitsukawa T. et al. (1999) A requirement for neuropilin-1 in embryonic vessel formation. Development 126, 4895-4902.
108. Kessler O., Shraga-Heled N. et al. (2004) Semaphorin-3F is an inhibitor of tumor angiogenesis. Cancer Res. 64, 1008-1015.
109. Kigel B., Varshavsky A. et al. (2008) Successful inhibition of tumor development by specific class-3 semaphorins is associated with expression of appropriate semaphorin receptors by tumor cells. PLoS One 3, e3287.
110. Kim W.H., Lee S.H. et al. (2009) Neuropilin2 expressed in gastric cancer endothelial cells increases the proliferation and migration of endothelial cells in response to VEGF. Exp. Cell Res. 315, 2154-2164.
111. Kitsukawa T., Shimono A. et al. (1995) Overexpression of a membrane protein, neuropilin, in chimeric mice causes anomalies in the cardiovascular system, nervous system and limbs. Development 121, 4309-4318.
112. Klagsbrun M., Takashima S. et al. (2002) The role of neuropilin in vascular and tumor biology. Adv. Exp. Med. Biol. 515, 33-48.
113. Kolodkin A.L., Levengood D.V. et al. (1997) Neuropilin is a semaphorin III receptor. Cell 90, 753-762.
114. Korgaonkar S.N., Feng X. et al. (2008) HIV-1 upregulates VEGF in podocytes. J. Am. Soc. Nephrol. 19, 877-883.
115. Kumar I., Staton C.A. et al. (2009) Angiogenesis, vascular endothelial growth factor and its receptors in human surgical wounds. Br. J. Surg. 96, 1484-1491.
116. Lacal P.M., Failla C.M. et al. (2000) Human melanoma cells secrete and respond to placenta growth factor and vascular endothelial growth factor. J. Invest. Dermatol. 115, 1000-1007.
117. Lantuejoul S., Constantin B. et al. (2003) Expression of VEGF, semaphorin SEMA3F, and their common receptors neuropilins NP1 and NP2 in preinvasive bronchial lesions, lung tumours, and cell lines. J. Pathol. 200, 336-347.
118. Latil A., Bieche I. et al. (2000) VEGF overexpression in clinically localized prostate tumors and neuropilin-1 overexpression in metastatic forms. Int. J. Cancer 89, 167-171.
119. Le A., Zielinski R. et al. (2009) Pulmonary epithelial neuropilin-1 deletion enhances development of cigarette smoke-induced emphysema. Am. J. Respir. Crit. Care Med. 180, 396-406.
120. Lee T.H., Seng S. et al. (2007) Vascular endothelial growth factor mediates intracrine survival in human breast carcinoma cells through internally expressed VEGFR1/FLT1. PLoS Med. 4, e186.
121. Lepelletier Y., Smaniotto S. et al. (2007) Control of human thymocyte migration by Neuropilin-1/Semaphorin-3A-mediated interactions. Proc. Natl. Acad. Sci. U S A 104, 5545-5550.
122. Li M., Yang H. et al. (2004) Pancreatic carcinoma cells express neuropilins and vascular endothelial growth factor, but not vascular endothelial growth factor receptors. Cancer 101, 2341-2350.
123. Li M., Zhang Y. et al. (2008) Interleukin-8 increases vascular endothelial growth factor and neuropilin expression and stimulates ERK activation in human pancreatic cancer. Cancer Sci. 99, 733-737.
124. Lichtenberger B.M., Tan P.K. et al. (2010) Autocrine VEGF signaling synergizes with EGFR in tumor cells to promote epithelial cancer development. cell 140, 268-279.
125. Lim J.I., Spee C. et al. (2005) Neuropilin-1 expression by endothelial cells and retinal pigment epithelial cells in choroidal neovascular membranes. Am. J. Ophthalmol. 140, 1044-1050.
126. Liu M. & Horowitz A. (2006) A PDZ-binding motif as a critical determinant of Rho guanine exchange factor function and cell phenotype. Mol. Biol. Cell 17, 1880-1887.
127. Llovet J.M., Ricci S. et al. (2008) Sorafenib in advanced hepatocellular carcinoma. N. Engl. J. Med. 359, 378-390.
128. Lohela M., Bry M. et al. (2009) VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr. Opin. Cell Biol. 21, 154-165.
129. Luo Y., Raible D. et al. (1993) Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75, 217-227.
130. Maeda K., Kang S.M. et al. (1998) Expression of p53 and vascular endothelial growth factor associated with tumor angiogenesis and prognosis in gastric cancer. Oncology 55, 594-599.
131. Maione F., Molla F. et al. (2009) Semaphorin 3A is an endogenous angiogenesis inhibitor that blocks tumor growth and normalizes tumor vasculature in transgenic mouse models. J. Clin. Invest. 119, 3356-3372.
132. Mak P., Leav I. et al. (2010) ERbeta impedes prostate cancer EMT by destabilizing HIF-1alpha and inhibiting VEGF-mediated snail nuclear localization: implications for Gleason grading. Cancer Cell 17, 319-332.
133. Mamluk R. (2002) Neuropilin-1 binds vascular endothelial growth factor 165, placenta growth factor-2, and heparin via its b1b2 domain. J. Biol. Chem. 277, 24818-24825.
134. Man X.Y., Yang X.H. et al. (2006) Immunolocalization and expression of vascular endothelial growth factor receptors (VEGFRs) and neuropilins (NRPs) on keratinocytes in human epidermis. Mol. Med. 12, 127-136.
135. Marwick J.A., Stevenson C.S. et al. (2006) Cigarette smoke disrupts VEGF165-VEGFR-2 receptor signaling complex in rat lungs and patients with COPD: morphological impact of VEGFR-2 inhibition. Am. J. Physiol. Lung Cell. Mol. Physiol. 290, L897-L908.
136. Matsushita A., Gotze T. et al. (2007) Hepatocyte growth factor-mediated cell invasion in pancreatic cancer cells is dependent on neuropilin-1. Cancer Res. 67, 10309-10316.
137. Matsushita A., Sasajima K. et al. (2010) Neuropilin-1, as a new therapeutic target in human pancreatic cancer. J Nihon Med Sch 77, 53-55.
138. McGrath-Morrow S.A., Cho C. et al. (2005) Vascular endothelial growth factor receptor 2 blockade disrupts postnatal lung development. Am. J. Respir. Cell Mol. Biol. 32, 420-427.
139. McMahon A.P., Ingham P.W. et al. (2003) Developmental roles and clinical significance of hedgehog signaling. Curr. Top. Dev. Biol. 53, 1-114.
140. Miao H.Q., Lee P. et al. (2000) Neuropilin-1 expression by tumor cells promotes tumor angiogenesis and progression. FASEB J. 14, 2532-2539.
141. Muders M.H. (2011) Neuropilin and neuropilin associated molecules as new molecular targets in pancreatic adenocarcinoma. Anticancer Agents Med. Chem. 11, 442-447.
142. Muders M.H., Zhang H. et al. (2009) Vascular endothelial growth factor-C protects prostate cancer cells from oxidative stress by the activation of mammalian target of rapamycin complex-2 and AKT-1. Cancer Res. 69, 6042-6048.
143. Muller M.W., Giese N.A. et al. (2007) Association of axon guidance factor semaphorin 3A with poor outcome in pancreatic cancer. Int. J. Cancer 121, 2421-2433.
144. Nasarre P., Kusy S. et al. (2005) Semaphorin SEMA3F has a repulsing activity on breast cancer cells and inhibits E-cadherin-mediated cell adhesion. Neoplasia 7, 180-189.
145. Nasarre P., Potiron V. et al. (2010) Guidance molecules in lung cancer. Cell Adh. Migr. 4, 130-145.
146. Neufeld G. & Kessler O. (2008) The semaphorins: versatile regulators of tumour progression and tumour angiogenesis. Nat. Rev. Cancer 8, 632-645.
147. Nguyen Q.D. (2006) Inhibition of vascular endothelial growth factor (VEGF)-165 and semaphorin 3A-mediated cellular invasion and tumor growth by the VEGF signaling inhibitor ZD4190 in human colon cancer cells and xenografts. Mol. Cancer Ther. 5, 2070-2077.
148. Ochiumi T., Kitadai Y. et al. (2006) Neuropilin-1 is involved in regulation of apoptosis and migration of human colon cancer. Int. J. Oncol. 29, 105-116.
149. Oinuma I., Ishikawa Y. et al. (2004) The Semaphorin 4D receptor Plexin-B1 is a GTPase activating protein for R-Ras. Science 305, 862-865.
150. Oniscu A., James R.M. et al. (2004) Expression of Sonic hedgehog pathway genes is altered in colonic neoplasia. J. Pathol. 203, 909-917.
151. Osada R., Horiuchi A. et al. (2006) Expression of semaphorins, vascular endothelial growth factor, and their common receptor neuropilins and alleic loss of semaphorin locus in epithelial ovarian neoplasms: increased ratio of vascular endothelial growth factor to semaphorin is a poor prognostic factor in ovarian carcinomas. Hum. Pathol. 37, 1414-1425.
152. Pan Q., Chanthery Y. et al. (2007) Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth. Cancer Cell 11, 53-67.
153. Parikh A.A., Liu W.B. et al. (2003) Expression and regulation of the novel vascular endothelial growth factor receptor neuropilin-1 by epidermal growth factor in human pancreatic carcinoma. Cancer 98, 720-729.
154. Parikh A.A., Fan F. et al. (2004) Neuropilin-1 in human colon cancer: expression, regulation, and role in induction of angiogenesis. Am. J. Pathol. 164, 2139-2151.
155. Pavlakis K., Messini I. et al. (2008) The assessment of angiogenesis and fibroblastic stromagenesis in hyperplastic and pre-invasive breast lesions. BMC Cancer 8, 88.
156. Pellet-Many C., Frankel P. et al. (2008) Neuropilins: structure, function and role in disease. Biochem. J. 411, 211.
157. Perala N., Jakobson M. et al. (2010) Sema4C-Plexin B2 signalling modulates ureteric branching in developing kidney. Differentiation 81, 81-91.
158. Petrelli F. & Barni S. (2010) Bevacizumab in advanced breast cancer: an opportunity as second-line therapy? Med. Oncol. [Epub ahead of print].
159. Plotkin S.R., Stemmer-Rachamimov A.O. et al. (2009) Hearing improvement after bevacizumab in patients with neurofibromatosis type 2. N. Engl. J. Med. 361, 358-367.
160. Pronina I.V., Loginov V.I. et al. (2009) Alteration of SEMA3B gene expression levels in epithelial tumors. Mol. Biol. 43, 439-445.
161. Raskopf E., Vogt A. et al. (2010) Inhibition of neuropilin-1 by RNA-interference and its angiostatic potential in the treatment of hepatocellular carcinoma. Z. Gastroenterol. 48, 21-27.
162. Reidy K.J., Villegas G. et al. (2009) Semaphorin3a regulates endothelial cell number and podocyte differentiation during glomerular development. Development 136, 3979-3989.
163. Robert B., Zhao X. et al. (2000) Coexpression of neuropilin-1, Flk1, and VEGF(164) in developing and mature mouse kidney glomeruli. Am. J. Physiol. Renal Physiol. 279, F275-F282.
164. Roberts J.R., Perkins G.D. et al. (2007) Vascular endothelial growth factor promotes physical wound repair and is anti-apoptotic in primary distal lung epithelial and A549 cells. Crit. Care Med. 35, 2164-2170.
165. Roche J., Drabkin H. et al. (2002) Neuropilin and its ligands in normal lung and cancer. Adv. Exp. Med. Biol. 515, 103-114.
166. Rody A., Holtrich U. et al. (2007) Poor outcome in estrogen receptor-positive breast cancers predicted by loss of plexin B1. Clin. Cancer Res. 13, 1115-1122.
167. Rosamilia A. & Dwyer P.L. (2000) Pathophysiology of interstitial cystitis. Curr. Opin. Obstet. Gynecol. 12, 405-410.
168. Rossignol M., Gagnon M.L. et al. (2000) Genomic organization of human neuropilin-1 and neuropilin-2 genes: identification and distribution of splice variants and soluble isoforms. Genomics 70, 211-222.
169. Rushing E.C., Stine M.J. et al. (2011) Neuropilin-2: a novel biomarker for malignant melanoma? Hum. Pathol. [Epub ahead of print].
170. Saban M.R., Backer J.M. et al. (2008a) VEGF receptors and neuropilins are expressed in the urothelial and neuronal cells in normal mouse urinary bladder and are upregulated in inflammation. Am. J. Physiol. Renal Physiol. 295, F60-F72.
171. Saban R., Saban M.R. et al. (2008b) Urothelial expression of neuropilins and VEGF receptors in control and interstitial cystitis patients. Am. J. Physiol. Renal Physiol. 295, F1613-F1623.
172. Saban M.R., Sferra T.J. et al. (2010) Neuropilin-VEGF signaling pathway acts as a key modulator of vascular, lymphatic, and inflammatory cell responses of the bladder to intravesical BCG treatment. Am. J. Physiol. Renal Physiol. 299, F1245-F1256.
173. Sanchez-Carbayo M., Socci N.D. et al. (2003) Gene discovery in bladder cancer progression using cDNA microarrays. Am. J. Pathol. 163, 505-516.
174. Sandler A., Gray R. et al. (2006) Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N. Engl. J. Med. 355, 2542-2550.
175. Saqui-Salces M. & Merchant J.L. (2010) Hedgehog signaling and gastrointestinal cancer. Biochim. Biophys. Acta Mol. Cell Res. 1803, 786-795.
176. Sarris M., Andersen K.G. et al. (2008) Neuropilin-1 expression on regulatory T cells enhances their interactions with dendritic cells during antigen recognition. Immunity 28, 402-413.
177. Schramek H., Sarközi R. et al. (2009) Neuropilin-1 and neuropilin-2 are differentially expressed in human proteinuric nephropathies and cytokine-stimulated proximal tubular cells. Lab. Invest. 89, 1304-1316.
178. Senger D.R., Perruzzi C.A. et al. (1986) A highly conserved vascular permeability factor secreted by a variety of human and rodent tumor cell lines. Cancer Res. 46, 5629-5632.
179. Serini G., Valdembri D. et al. (2003) Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 424, 391-397.
180. Serini G., Maione F. et al. (2009) Semaphorins and tumor angiogenesis. Angiogenesis 12, 187-193.
181. Serpa J., Caiado F. et al. (2010) Butyrate rich colonic microenvironment is a relevant selection factor for metabolically adapted tumour cells. J. Biol. Chem. 285, 39211-39223.
182. Shintani Y., Takashima S. et al. (2009) Extracellular protein kinase CK2 is a novel associating protein of neuropilin-1. Biochem. Biophys. Res. Commun. 385, 618-623.
183. Shirvan A., Ziv I. et al. (1999) Semaphorins as mediators of neuronal apoptosis. J. Neurochem. 73, 961-971.
184. Smith R.A., Tang J. et al. (2011) Meta-analysis of immunohistochemical prognostic markers in resected pancreatic cancer. Br. J. Cancer 104, 1440-1451.
185. Soker S., Gollamudi-Payne S. et al. (1997) 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, 31582-31588.
186. Soker S., Takashima S. et al. (1998) Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. cell 92, 735-745.
187. Staton C.A., Kumar I. et al. (2007) Neuropilins in physiological and pathological angiogenesis. J. Pathol. 212, 237-248.
188. Staton C.A., Shaw L.A. et al. (2011) Expression of class 3 semaphorins and their receptors in human breast neoplasia. Histopathology 59, 274-282.
189. Stephenson J.M., Banerjee S. et al. (2002) 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 101, 409-414.
190. Straub R.H., Grum F. et al. (2008) Anti-inflammatory role of sympathetic nerves in chronic intestinal inflammation. Gut 57, 911-921.
191. Straume O. & Akslen L.A. (2003) Increased expression of VEGF-receptors (FLT-1, KDR, NRP-1) and thrombospondin-1 is associated with glomeruloid microvascular proliferation, an aggressive angiogenic phenotype, in malignant melanoma. Angiogenesis 6, 295-301.
192. Sulpice E., Plouet J. et al. (2008) Neuropilin-1 and neuropilin-2 act as coreceptors, potentiating proangiogenic activity. Blood 111, 2036-2045.
193. Syed V., Zhang X. et al. (2005) Profiling estrogen-regulated gene expression changes in normal and malignant human ovarian surface epithelial cells. Oncogene 24, 8128-8143.
194. Takagi S., Tsuji T. et al. (1987) Specific cell surface labels in the visual centers of Xenopus laevis tadpole identified using monoclonal antibodies. Dev. Biol. 122, 90-100.
195. Takahashi T. & Strittmatter S.M. (2001) Plexina1 autoinhibition by the plexin sema domain. Neuron 29, 429-439.
196. Takahashi Y., Kitadai Y. et al. (1995) Expression of vascular endothelial growth factor and its receptor, KDR, correlates with vascularity, metastasis, and proliferation of human colon cancer. Cancer Res. 55, 3964-3968.
197. Takamatsu H., Okuno T. et al. (2010) Regulation of immune cell responses by semaphorins and their receptors. Cell. Mol. Immunol. 7, 83-88.
198. Tamaki M., Saito R. et al. (2004) Possible mechanisms inducing glomerulations in interstitial cystitis: relationship between endoscopic findings and expression of angiogenic growth factors. J. Urol. 172, 945-948.
199. Tapia R., Guan F. et al. (2008) Semaphorin3a disrupts podocyte foot processes causing acute proteinuria. Kidney Int. 73, 733-740.
200. Toi M., Inada K. et al. (1995) Tumor angiogenesis in breast cancer: its importance as a prognostic indicator and the association with vascular endothelial growth factor expression. Breast Cancer Res. Treat. 36, 193-204.
201. Tominaga M., Ogawa H. et al. (2008) Decreased production of semaphorin 3A in the lesional skin of atopic dermatitis. Br. J. Dermatol. 158, 842-844.
202. Tomizawa Y., Sekido Y. et al. (2001) Inhibition of lung cancer cell growth and induction of apoptosis after reexpression of 3p21.3 candidate tumor suppressor gene SEMA3B. Proc. Natl. Acad. Sci. U S A 98, 13954-13959.
203. Tracey K.J. (2002) The inflammatory reflex. Nature 420, 853-859.
204. Troeger J.S. & Schwabe R.F. (2011) Neuropilin and liver fibrosis: hitting three birds with one stone? Hepatology 54, 1091-1093.
205. Tseng L.H., Chen I. et al. (2009) Genome-based expression profiles as a single standardized microarray platform for the diagnosis of experimental interstitial cystitis: an array of 75 genes model. Int. Urogynecol. J. Pelvic. Floor Dysfunct. [Epub ahead of print].
206. Tufro A., Teichman J. et al. (2008) Semaphorin3a inhibits ureteric bud branching morphogenesis. Mech. Dev. 125, 558-568.
207. Valdembri D., Caswell P.T. et al. (2009) Neuropilin-1/GIPC1 signaling regulates alpha5beta1 integrin traffic and function in endothelial cells. PLoS Biol. 7, e25.
208. Vanveldhuizen P.J., Zulfiqar M. et al. (2003) Differential expression of neuropilin-1 in malignant and benign prostatic stromal tissue. Oncol. Rep. 10, 1067-1071.
209. Viacava P., Naccarato A.G. et al. (2004) Angiogenesis and VEGF expression in pre-invasive lesions of the human breast. J. Pathol. 204, 140-146.
210. Villegas G. & Tufro A. (2002) Ontogeny of semaphorins 3A and 3F and their receptors neuropilins 1 and 2 in the kidney. Gene Expr. Patterns 2, 151-155.
211. Waltenberger J., Claesson-Welsh L. et al. (1994) Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J. Biol. Chem. 269, 26988-26995.
212. Wang L., Mukhopadhyay D. et al. (2006) C terminus of RGS-GAIP-interacting protein conveys neuropilin-1-mediated signaling during angiogenesis. FASEB J. 20, 1513-1515.
213. Weis S.M. & Cheresh D.A. (2005) Pathophysiological consequences of VEGF-induced vascular permeability. Nature 437, 497-504.
214. Wendt M.K., Allington T.M. et al. (2009) Mechanisms of the epithelial-mesenchymal transition by TGF-beta. Future Oncol. 5, 1145-1168.
215. West D.C., Rees C.G. et al. (2005) Interactions of multiple heparin binding growth factors with neuropilin-1 and potentiation of the activity of fibroblast growth factor-2. J. Biol. Chem. 280, 13457-13464.
216. Wey J.S., Gray M.J. et al. (2005) Overexpression of neuropilin-1 promotes constitutive MAPK signalling and chemoresistance in pancreatic cancer cells. Br. J. Cancer 93, 233-241.
217. Whitaker G.B., Limberg B.J. et al. (2001) 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, 25520-25531.
218. Wilgus T.A., Matthies A.M. et al. (2005) Novel function for vascular endothelial growth factor receptor-1 on epidermal keratinocytes. Am. J. Pathol. 167, 1257-1266.
219. Wong O.G., Nitkunan T. et al. (2007) Plexin-B1 mutations in prostate cancer. Proc. Natl. Acad. Sci. U S A 104, 19040-19045.
220. von Wronski M.A., Raju N. et al. (2006) Tuftsin binds neuropilin-1 through a sequence similar to that encoded by exon 8 of vascular endothelial growth factor. J. Biol. Chem. 281, 5702-5710.
221. Yacoub M., Coulon A. et al. (2009) Differential expression of the semaphorin 3A pathway in prostatic cancer. Histopathology 55, 392-398.
222. Yamaguchi J., Nakamura F. et al. (2008) Semaphorin3A alleviates skin lesions and scratching behavior in NC/Nga mice, an atopic dermatitis model. J. Invest. Dermatol. 128, 2842-2849.
223. Yaron A., Huang P.H. et al. (2005) Differential requirement for Plexin-A3 and -A4 in mediating responses of sensory and sympathetic neurons to distinct class 3 Semaphorins. Neuron 45, 513-523.
224. Yasuoka H., Kodama R. et al. (2009) Neuropilin-2 expression in breast cancer: correlation with lymph node metastasis, poor prognosis, and regulation of CXCR4 expression. BMC Cancer 9, 220.
225. Yoshiji H., Kuriyama S. et al. (2003) Vascular endothelial growth factor and receptor interaction is a prerequisite for murine hepatic fibrogenesis. Gut 52, 1347-1354.
226. Yoshikawa K., Shimada M. et al. (2009) Sonic hedgehog relates to colorectal carcinogenesis. J. Gastroenterol. 44, 1113-1117.
227. Yu D.C.W., Waby J.S. et al. (2010) Butyrate suppresses expression of neuropilin I in colorectal cell lines through inhibition of Sp1 transactivation. Mol. Cancer 9, 276.
228. Yu D.C., Bury J.P. et al. (2011) Short-chain fatty acid level and field cancerization show opposing associations with enteroendocrine cell number and neuropilin expression in patients with colorectal adenoma. Mol. Cancer 10, 27.
229. Yuan L., Moyon D. et al. (2002) Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development 129, 4797-4806.
230. Zachary I. (2003) VEGF signalling: integration and multi-tasking in endothelial cell biology. Biochem. Soc. Trans. 31(Pt 6), 1171-1177.
231. Zachary I.C., Frankel P. et al. (2009) The role of neuropilins in cell signalling. Biochem. Soc. Trans. 37, 1171.
232. Zavadil J. & Bottinger E.P. (2005) TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 24, 5764-5774.
233. Zhang S. & Kong W. (2006) Expression of neuropilin-1 in human laryngeal carcinoma and cell lines]. Lin Chuang Er Bi Yan Hou Ke Za Zhi 20, 634-635.
234. Zhang Y., Singh M.K. et al. (2009) Tie2Cre-mediated inactivation of plexinD1 results in congenital heart, vascular and skeletal defects. Dev. Biol. 325, 82-93.
235. Zhao X.Y., Chen L. et al. (2007) PlexinA1 expression in gastric carcinoma and its relationship with tumor angiogenesis and proliferation. World J. Gastroenterol. 13, 6558-6561.
236. Zhou H., Zhang L. et al. (2007) Expression of neuropilin-1 in kidney graft biopsies: what is the significance? Transplant. Proc. 39, 81-83.
237. Zhou Y., Gunput R.A. et al. (2008) Semaphorin signaling: progress made and promises ahead. Trends Biochem. Sci. 33, 161-170.