Transmembrane semaphorins: Multimodal signaling cues in development and cancer

Cell Adhesion and Migration

Volumn 10, Issue 6, 2016, Pages 675-691

  Gurrapu, Sreeharsha ^a,b   Tamagnone, Luca ^a,b  

^a UNIVERSITY OF TURIN   (Italy)

^b CANDIOLO CANCER INSTITUTE   (Italy)

Author keywords

cancer; development; plexins; semaphorins; signaling mechanisms

Indexed keywords

CD72 ANTIGEN; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SEMAPHORIN; CELL SURFACE RECEPTOR;

ANGIOGENESIS; BREAST CANCER; CELL INFILTRATION; CELL INVASION; DEVELOPMENT; EXTRACELLULAR MATRIX; GENE OVEREXPRESSION; GLIOBLASTOMA; HIPPOCAMPUS; HUMAN; IMMUNE FUNCTION TEST; NEOPLASM; PROTEIN DEPHOSPHORYLATION; RECEPTOR DOWN REGULATION; REVIEW; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR MICROENVIRONMENT; WOUND HEALING; ANIMAL; CELL MEMBRANE; EMBRYO DEVELOPMENT; METABOLISM;

ANIMALS; CELL MEMBRANE; EMBRYONIC DEVELOPMENT; HUMANS; NEOPLASMS; RECEPTORS, CELL SURFACE; SEMAPHORINS; SIGNAL TRANSDUCTION;

EID: 84978141450     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.1080/19336918.2016.1197479     Document Type: Review

References (184)

1. Tamagnone L, Artigiani S, Chen H, He Z, Ming GI, Song H, Chedotal A, Winberg ML, Goodman CS, Poo M, et al. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 1999; 99:71-80; PMID:10520995; http://dx.doi.org/10.1016/S0092-8674(00)80063-X
2. Kolodkin AL, Levengood DV, Rowe EG, Tai YT, Giger RJ, Ginty DD. Neuropilin is a semaphorin III receptor. Cell 1997; 90:753-62; PMID:9288754; http://dx.doi.org/10.1016/S0092-8674(00)80535-8
3. Kolodkin AL, Ginty DD. Steering clear of semaphorins:neuropilins sound the retreat. Neuron 1997; 19:1159-62; PMID:9427240; http://dx.doi.org/10.1016/S0896-6273(00)80408-0
4. Delgoffe GM, Woo SR, Turnis ME, Gravano DM, Guy C, Overacre AE, Bettini ML, Vogel P, Finkelstein D, Bonnevier J, et al. Stability and function of regulatory T cells is maintained by a neuropilin-1-semaphorin-4a axis. Nature 2013; 501:252-6; PMID:23913274; http://dx.doi.org/10.1038/nature12428
5. Tong Y, Hota PK, Penachioni JY, Hamaneh MB, Kim SJ, Alviani RS, Shen L, He H, Tempel W, Tamagnone L, et al. Structure and function of the intracellular region of the Plexin-B1 transmembrane receptor. J Biol Chem 2009; 284:35962-72; PMID:19843518; http://dx.doi.org/10.1074/jbc.M109.056275
6. Kumanogoh A, Marukawa S, Suzuki K, Takegahara N, Watanabe C, Ch'ng E, Ishida I, Fujimura H, Sakoda S, Yoshida K, et al. Class IV semaphorin Sema4A enhances T-cell activation and interacts with Tim-2. Nature 2002; 419:629-33; PMID:12374982; http://dx.doi.org/10.1038/nature01037
7. Nagai H, Sugito N, Matsubara H, Tatematsu Y, Hida T, Sekido Y, Nagino M, Nimura Y, Takahashi T, Osada H. CLCP1 interacts with semaphorin 4B and regulates motility of lung cancer cells. Oncogene 2007; 26:4025-31; PMID:17213806; http://dx.doi.org/10.1038/sj.onc.1210183
8. Kumanogoh A, Watanabe C, Lee I, Wang X, Shi W, Araki H, Hirata H, Iwahori K, Uchida J, Yasui T, et al. Identification of CD72 as a lymphocyte receptor for the class IV semaphorin CD100:a novel mechanism for regulating B cell signaling. Immunity 2000; 13:621-31; PMID:11114375; http://dx.doi.org/10.1016/S1074-7613(00)00062-5
9. Kantor DB, Chivatakarn O, Peer KL, Oster SF, Inatani M, Hansen MJ, Flanagan JG, Yamaguchi Y, Sretavan DW, Giger RJ, et al. Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 2004; 44:961-75; PMID:15603739; http://dx.doi.org/10.1016/j.neuron.2004.12.002
10. Basile JR, Holmbeck K, Bugge TH, Gutkind JS. MT1-MMP controls tumor-induced angiogenesis through the release of semaphorin 4D. J Biol Chem 2007; 282:6899-905; PMID:17204469; http://dx.doi.org/10.1074/jbc.M609570200
11. Mou P, Zeng Z, Li Q, Liu X, Xin X, Wannemacher KM, Ruan C, Li R, Brass LF, Zhu L. Identification of a calmodulin-binding domain in Sema4D that regulates its exodomain shedding in platelets. Blood 2013; 121:4221-30; PMID:23564909; http://dx.doi.org/10.1182/blood-2012-11-470609
12. Conrotto P, Valdembri D, Corso S, Serini G, Tamagnone L, Comoglio PM, Bussolino F, Giordano S. Sema4D induces angiogenesis through Met recruitment by Plexin B1. Blood 2005; 105:4321-9; PMID:15632204; http://dx.doi.org/10.1182/blood-2004-07-2885
13. Sierra JR, Corso S, Caione L, Cepero V, Conrotto P, Cignetti A, Piacibello W, Kumanogoh A, Kikutani H, Comoglio PM, et al. Tumor angiogenesis and progression are enhanced by Sema4D produced by tumor-associated macrophages. J Exp Med 2008; 205:1673-85; PMID:18559453; http://dx.doi.org/10.1084/jem.20072602
14. Bonneville M. Semaphorins:new cues for skin healing by gammadelta T cells. Immunity 2012; 37:194-6; PMID:22921116; http://dx.doi.org/10.1016/j.immuni.2012.08.003
15. Cho JY, Chak K, Andreone BJ, Wooley JR, Kolodkin AL. The extracellular matrix proteoglycan perlecan facilitates transmembrane semaphorin-mediated repulsive guidance. Genes Dev 2012; 26:2222-35; PMID:23028146; http://dx.doi.org/10.1101/gad.193136.112
16. Cafferty P, Yu L, Rao Y. The receptor tyrosine kinase Off-track is required for layer-specific neuronal connectivity in Drosophila. Development 2004; 131:5287-95; PMID:15456725; http://dx.doi.org/10.1242/dev.01406
17. Jeong S, Juhaszova K, Kolodkin AL. The Control of semaphorin-1a-mediated reverse signaling by opposing pebble and RhoGAPp190 functions in drosophila. Neuron 2012; 76:721-34; PMID:23177958; http://dx.doi.org/10.1016/j.neuron.2012.09.018
18. Oinuma I, Ishikawa Y, Katoh H, Negishi M. The Semaphorin 4D receptor Plexin-B1 is a GTPase activating protein for R-Ras. Science 2004; 305:862-5; PMID:15297673; http://dx.doi.org/10.1126/science.1097545
19. Tong Y, Chugha P, Hota PK, Alviani RS, Li M, Tempel W, Shen L, Park HW, Buck M. Binding of Rac1, Rnd1, and RhoD to a novel Rho GTPase interaction motif destabilizes dimerization of the plexin-B1 effector domain. J Biol Chem 2007; 282:37215-24; PMID:17916560; http://dx.doi.org/10.1074/jbc.M703800200
20. Ito Y, Oinuma I, Katoh H, Kaibuchi K, Negishi M. Sema4D/plexin-B1 activates GSK-3beta through R-Ras GAP activity, inducing growth cone collapse. EMBO Rep 2006; 7:704-9; PMID:16799460; http://dx.doi.org/10.1038/sj.embor.7400737
21. Okada T, Sinha S, Esposito I, Schiavon G, López-Lago MA, Su W, Pratilas CA, Abele C, Hernandez JM, Ohara M, et al. The Rho GTPase Rnd1 suppresses mammary tumorigenesis and EMT by restraining Ras-MAPK signalling. Nat Cell Biol 2015; 17:81-94; PMID:25531777; http://dx.doi.org/10.1038/ncb3082
22. Barberis D, Casazza A, Sordella R, Corso S, Artigiani S, Settleman J, Comoglio PM, Tamagnone L. p190 Rho-GTPase activating protein associates with plexins and it is required for semaphorin signalling. J Cell Sci 2005; 118:4689-700; PMID:16188938; http://dx.doi.org/10.1242/jcs.02590
23. Vikis HG, Li W, Guan KL. The plexin-B1/Rac interaction inhibits PAK activation and enhances Sema4D ligand binding. Genes Dev 2002; 16:836-45; PMID:11937491; http://dx.doi.org/10.1101/gad.966402
24. Swiercz JM, Kuner R, Behrens J, Offermanns S. Plexin-B1 directly interacts with PDZ-RhoGEF/LARG to regulate RhoA and growth cone morphology. Neuron 2002; 35:51-63; PMID:12123608; http://dx.doi.org/10.1016/S0896-6273(02)00750-X
25. Perrot V, Vazquez-Prado J, Gutkind JS. Plexin B regulates Rho through the guanine nucleotide exchange factors leukemia-associated Rho GEF (LARG) and PDZ-RhoGEF. J Biol Chem 2002; 277:43115-20; PMID:12183458; http://dx.doi.org/10.1074/jbc.M206005200
26. Swiercz JM, Worzfeld T, Offermanns S. ErbB-2 and met reciprocally regulate cellular signaling via plexin-B1. J Biol Chem 2008; 283:1893-901; PMID:18025083; http://dx.doi.org/10.1074/jbc.M706822200
27. Swiercz JM, Kuner R, Offermanns S. Plexin-B1/RhoGEF-mediated RhoA activation involves the receptor tyrosine kinase ErbB-2. J Cell Biol 2004; 165:869-80; PMID:15210733; http://dx.doi.org/10.1083/jcb.200312094
28. Conrotto P, Corso S, Gamberini S, Comoglio PM, Giordano S. Interplay between scatter factor receptors and B plexins controls invasive growth. Oncogene 2004; 23:5131-7; PMID:15184888; http://dx.doi.org/10.1038/sj.onc.1207650
29. Artigiani S, Conrotto P, Fazzari P, Gilestro GF, Barberis D, Giordano S, Comoglio PM, Tamagnone L. Plexin-B3 is a functional receptor for semaphorin 5A. EMBO Rep 2004; 5:710-4; PMID:15218527; http://dx.doi.org/10.1038/sj.embor.7400189
30. Toyofuku T, Zhang H, Kumanogoh A, Takegahara N, Suto F, Kamei J, Aoki K, Yabuki M, Hori M, Fujisawa H, et al. Dual roles of Sema6D in cardiac morphogenesis through region-specific association of its receptor, Plexin-A1, with off-track and vascular endothelial growth factor receptor type 2. Genes Dev 2004; 18:435-47; PMID:14977921; http://dx.doi.org/10.1101/gad.1167304
31. Toyofuku T, Zhang H, Kumanogoh A, Takegahara N, Yabuki M, Harada K, Hori M, Kikutani H. Guidance of myocardial patterning in cardiac development by Sema6D reverse signalling. Nat Cell Biol 2004; 6:1204-11; PMID:15543137; http://dx.doi.org/10.1038/ncb1193
32. Klostermann A, Lutz B, Gertler F, Behl C. The orthologous human and murine semaphorin 6A-1 proteins (SEMA6A-1/Sema6A-1) bind to the enabled/vasodilator-stimulated phosphoprotein-like protein (EVL) via a novel carboxyl-terminal zyxin-like domain. J Biol Chem 2000; 275:39647-53; PMID:10993894; http://dx.doi.org/10.1074/jbc.M006316200
33. Eckhardt F, Behar O, Calautti E, Yonezawa K, Nishimoto I, Fishman MC. A novel transmembrane semaphorin can bind c-src. Mol Cell Neurosci 1997; 9:409-19; PMID:9361278; http://dx.doi.org/10.1006/mcne.1997.0644
34. Inagaki S, Ohoka Y, Sugimoto H, Fujioka S, Amazaki M, Kurinami H, Miyazaki N, Tohyama M, Furuyama T. Sema4C, a transmembrane semaphorin, interacts with a post-synaptic density protein, PSD-95. J Biol Chem 2001; 276:9174-81; PMID:11134026; http://dx.doi.org/10.1074/jbc.M009051200
35. Schultze W, Eulenburg V, Lessmann V, Herrmann L, Dittmar T, Gundelfinger ED, Heumann R, Erdmann KS. Semaphorin4F interacts with the synapse-associated protein SAP90/PSD-95. J Neurochem 2001; 78:482-9; PMID:11483650; http://dx.doi.org/10.1046/j.1471-4159.2001.00447.x
36. Burkhardt C, Muller M, Badde A, Garner CC, Gundelfinger ED, Puschel AW. Semaphorin 4B interacts with the post-synaptic density protein PSD-95/SAP90 and is recruited to synapses through a C-terminal PDZ-binding motif. FEBS Lett 2005; 579:3821-8; PMID:15978582; http://dx.doi.org/10.1016/j.febslet.2005.05.079
37. Inagaki S, Ohoka Y, Sugimoto H, Fujioka S, Amazaki M, Kurinami H, Miyazaki N, Tohyama M, Furuyama T. Sema4c, a transmembrane semaphorin, interacts with a post-synaptic density protein, PSD-95. J Biol Chem 2001; 276:9174-81; PMID:11134026; http://dx.doi.org/10.1074/jbc.M009051200
38. Ko JA, Gondo T, Inagaki S, Inui M. Requirement of the transmembrane semaphorin Sema4C for myogenic differentiation. Febs Letters 2005; 579:2236-42; PMID:15811348; http://dx.doi.org/10.1016/j.febslet.2005.03.022
39. Haklai-Topper L, Mlechkovich G, Savariego D, Gokhman I, Yaron A. Cis interaction between Semaphorin6A and Plexin-A4 modulates the repulsive response to Sema6A. EMBO J 2010; 29:2635-45; PMID:20606624; http://dx.doi.org/10.1038/emboj.2010.147
40. Suto F, Tsuboi M, Kamiya H, Mizuno H, Kiyama Y, Komai S, Shimizu M, Sanbo M, Yagi T, Hiromi Y, et al. Interactions between plexin-A2, plexin-A4, and semaphorin 6A control lamina-restricted projection of hippocampal mossy fibers. Neuron 2007; 53:535-47; PMID:17296555; http://dx.doi.org/10.1016/j.neuron.2007.01.028
41. Mizumoto K, Shen K. Interaxonal interaction defines tiled presynaptic innervation in C. elegans. Neuron 2013; 77:655-66; PMID:23439119; http://dx.doi.org/10.1016/j.neuron.2012.12.031
42. Jongbloets BC, Pasterkamp RJ. Semaphorin signalling during development. Development 2014; 141:3292-7; PMID:25139851; http://dx.doi.org/10.1242/dev.105544
43. Ben-Gigi L, Sweetat S, Besser E, Fellig Y, Wiederhold T, Polakiewicz RD, Behar O. Astrogliosis induced by brain injury is regulated by Sema4B Phosphorylation(). eNeuro 2015; 2; PMID:26464987
44. Maier V, Jolicoeur C, Rayburn H, Takegahara N, Kumanogoh A, Kikutani H, Tessier-Lavigne M, Wurst W, Friedel RH. Semaphorin 4C and 4G are ligands of Plexin-B2 required in cerebellar development. Mol Cell Neurosci 2011; 46:419-31; PMID:21122816; http://dx.doi.org/10.1016/j.mcn.2010.11.005
45. Taniguchi Y, Amazaki M, Furuyama T, Yamaguchi W, Takahara M, Saino O, Wada T, Niwa H, Tashiro F, Miyazaki J, et al. Sema4D deficiency results in an increase in the number of oligodendrocytes in healthy and injured mouse brains. J Neurosci Res 2009; 87:2833-41; PMID:19472224; http://dx.doi.org/10.1002/jnr.22124
46. Fiore R, Rahim B, Christoffels VM, Moorman AF, Puschel AW. Inactivation of the Sema5a gene results in embryonic lethality and defective remodeling of the cranial vascular system. Mol Cell Biol 2005; 25:2310-9; PMID:15743826; http://dx.doi.org/10.1128/MCB.25.6.2310-2319.2005
47. Leighton PA, Mitchell KJ, Goodrich LV, Lu X, Pinson K, Scherz P, Skarnes WC, Tessier-Lavigne M. Defining brain wiring patterns and mechanisms through gene trapping in mice. Nature 2001; 410:174-9; PMID:11242070; http://dx.doi.org/10.1038/35065539
48. Kerjan G, Dolan J, Haumaitre C, Schneider-Maunoury S, Fujisawa H, Mitchell KJ, Chedotal A. The transmembrane semaphorin Sema6A controls cerebellar granule cell migration. Nat Neurosci 2005; 8:1516-24; PMID:16205717; http://dx.doi.org/10.1038/nn1555
49. Suto F, Murakami Y, Nakamura F, Goshima Y, Fujisawa H. Identification and characterization of a novel mouse plexin, plexin-A4. Mech Dev 2003; 120:385-96; PMID:12591607; http://dx.doi.org/10.1016/S0925-4773(02)00421-5
50. Yaron A, Huang PH, Cheng HJ, Tessier-Lavigne M. Differential requirement for Plexin-A3 and -A4 in mediating responses of sensory and sympathetic neurons to distinct class 3 Semaphorins. Neuron 2005; 45:513-23; PMID:15721238; http://dx.doi.org/10.1016/j.neuron.2005.01.013
51. Daviaud N, Chen K, Huang Y, Friedel RH, Zou H. Impaired cortical neurogenesis in Plexin-B1 and -B2 double deletion mutant. Dev Neurobiol 2015; PMID:26579598; http://dx.doi.org/10.1002/dneu.22364
52. Oinuma I, Ito Y, Katoh H, Negishi M. Semaphorin 4D/Plexin-B1 stimulates PTEN activity through R-Ras GTPase-activating protein activity, inducing growth cone collapse in hippocampal neurons. J Biol Chem 2010; 285:28200-9; PMID:20610402; http://dx.doi.org/10.1074/jbc.M110.147546
53. Giacobini P, Messina A, Morello F, Ferraris N, Corso S, Penachioni J, Giordano S, Tamagnone L, Fasolo A. Semaphorin 4D regulates gonadotropin hormone-releasing hormone-1 neuronal migration through PlexinB1-Met complex. J Cell Biol 2008; 183:555-66; PMID:18981235; http://dx.doi.org/10.1083/jcb.200806160
54. Yamaguchi W, Tamai R, Kageura M, Furuyama T, Inagaki S. Sema4D as an inhibitory regulator in oligodendrocyte development. Mol Cell Neurosci 2012; 49:290-9; PMID:22198439; http://dx.doi.org/10.1016/j.mcn.2011.12.004
55. Armendariz BG, Bribian A, Perez-Martinez E, Martinez A, de Castro F, Soriano E, Burgaya F. Expression of Semaphorin 4F in neurons and brain oligodendrocytes and the regulation of oligodendrocyte precursor migration in the optic nerve. Mol Cell Neurosci 2012; 49:54-67; PMID:21945643; http://dx.doi.org/10.1016/j.mcn.2011.09.003
56. Goldberg JL, Vargas ME, Wang JT, Mandemakers W, Oster SF, Sretavan DW, Barres BA. An oligodendrocyte lineage-specific semaphorin, Sema5A, inhibits axon growth by retinal ganglion cells. J Neurosci 2004; 24:4989-99; PMID:15163691; http://dx.doi.org/10.1523/JNEUROSCI.4390-03.2004
57. Bernard F, Moreau-Fauvarque C, Heitz-Marchaland C, Zagar Y, Dumas L, Fouquet S, Lee X, Shao Z, Mi S, Chedotal A. Role of transmembrane semaphorin Sema6A in oligodendrocyte differentiation and myelination. Glia 2012; 60:1590-604; PMID:22777942; http://dx.doi.org/10.1002/glia.22378
58. Rehman M, Tamagnone L. Semaphorins in cancer:biological mechanisms and therapeutic approaches. Semin Cell Dev Biol 2013; 24:179-89; PMID:23099250; http://dx.doi.org/10.1016/j.semcdb.2012.10.005
59. Schulz E, Klampfl P, Holzapfel S, Janecke AR, Ulz P, Renner W, Kashofer K, Nojima S, Leitner A, Zebisch A, et al. Germline variants in the SEMA4A gene predispose to familial colorectal cancer type X. Nat Commun 2014; 5:5191; PMID:25307848; http://dx.doi.org/10.1038/ncomms6191
60. Jian H, Liu B, Zhang J. Hypoxia and hypoxia-inducible factor 1 repress SEMA4B expression to promote non-small cell lung cancer invasion. Tumour Biol 2014; 35:4949-55; PMID:24474252; http://dx.doi.org/10.1007/s13277-014-1651-4
61. Jian H, Zhao Y, Liu B, Lu S. SEMA4B inhibits growth of non-small cell lung cancer in vitro and in vivo. Cell Signalling 2015; 27:1208-13; PMID:25746385; http://dx.doi.org/10.1016/j.cellsig.2015.02.027
62. Jian H, Zhao Y, Liu B, Lu S. SEMA4b inhibits MMP9 to prevent metastasis of non-small cell lung cancer. Tumour Biol 2014; 35:11051-6; PMID:25095981; http://dx.doi.org/10.1007/s13277-014-2409-8
63. Ye SM, Han M, Kan CY, Yang LL, Yang J, Ma QF, Wang SX. [Expression and clinical significance of Sema4C in esophageal cancer, gastric cancer and rectal cancer]. Zhonghua Yi Xue Za Zhi 2012; 92:1954-8; PMID:22944267
64. Zhang Y, Huang S. Up-regulation of miR-125b reverses epithelial-mesenchymal transition in paclitaxel-resistant lung cancer cells. Biol Chem 2015; PMID:26351908; http://dx.doi.org/10.1515/hsz-2015-0153
65. Yang Q, Wang Y, Lu X, Zhao Z, Zhu L, Chen S, Wu Q, Chen C, Wang Z. MiR-125b regulates epithelial-mesenchymal transition via targeting Sema4C in paclitaxel-resistant breast cancer cells. Oncotarget 2015; 6:3268-79; PMID:25605244; http://dx.doi.org/10.18632/oncotarget.3065
66. Le AP, Huang Y, Pingle SC, Kesari S, Wang H, Yong RL, Zou H, Friedel RH. Plexin-B2 promotes invasive growth of malignant glioma. Oncotarget 2015; 6:7293-304; PMID:25762646; http://dx.doi.org/10.18632/oncotarget.3421
67. Wu M, Han L, Shi Y, Xu G, Wei J, You L, Chen Y, Zhu T, Li Q, Li S, et al. Development and characterization of a novel method for the analysis of gene expression patterns in lymphatic endothelial cells derived from primary breast tissues. J Cancer Res Clin Oncol 2010; 136:863-72; PMID:19936789; http://dx.doi.org/10.1007/s00432-009-0727-9
68. Kato S, Kubota K, Shimamura T, Shinohara Y, Kobayashi N, Watanabe S, Yoneda M, Inamori M, Nakamura F, Ishiguro H, et al. Semaphorin 4D, a lymphocyte semaphorin, enhances tumor cell motility through binding its receptor, plexinB1, in pancreatic cancer. Cancer Sci 2011; 102:2029-37; PMID:21812859; http://dx.doi.org/10.1111/j.1349-7006.2011.02053.x
69. Ch'ng E, Tomita Y, Zhang B, He J, Hoshida Y, Qiu Y, Morii E, Nakamichi I, Hamada K, Ueda T, et al. Prognostic significance of CD100 expression in soft tissue sarcoma. Cancer 2007; 110:164-72; PMID:17520683; http://dx.doi.org/10.1002/cncr.22764
70. Worzfeld T, Swiercz JM, Looso M, Straub BK, Sivaraj KK, Offermanns S. ErbB-2 signals through Plexin-B1 to promote breast cancer metastasis. J Clin Investigat 2012; 122:1296-305; PMID:22378040; http://dx.doi.org/10.1172/JCI60568
71. Zhou H, Yang YH, Basile JR. The Semaphorin 4D-Plexin-B1-RhoA signaling axis recruits pericytes and regulates vascular permeability through endothelial production of PDGF-B and ANGPTL4. Angiogenesis 2014; 17:261-74; PMID:24114199; http://dx.doi.org/10.1007/s10456-013-9395-0
72. Moriarity BS, Otto GM, Rahrmann EP, Rathe SK, Wolf NK, Weg MT, Manlove LA, LaRue RS, Temiz NA, Molyneux SD, et al. A Sleeping Beauty forward genetic screen identifies new genes and pathways driving osteosarcoma development and metastasis. Nat Genet 2015; 47:615-24; PMID:25961939; http://dx.doi.org/10.1038/ng.3293
73. Giordano S, Corso S, Conrotto P, Artigiani S, Gilestro G, Barberis D, Tamagnone L, Comoglio PM. The semaphorin 4D receptor controls invasive growth by coupling with Met. Nat Cell Biol 2002; 4:720-4; PMID:12198496; http://dx.doi.org/10.1038/ncb843
74. Basile JR, Barac A, Zhu T, Guan KL, Gutkind JS. Class IV semaphorins promote angiogenesis by stimulating Rho-initiated pathways through plexin-B. Cancer Res 2004; 64:5212-24; PMID:15289326; http://dx.doi.org/10.1158/0008-5472.CAN-04-0126
75. Basile JR, Afkhami T, Gutkind JS. Semaphorin 4D/plexin-B1 induces endothelial cell migration through the activation of PYK2, Src, and the phosphatidylinositol 3-kinase-Akt pathway. Mol Cell Biol 2005; 25:6889-98; PMID:16055703; http://dx.doi.org/10.1128/MCB.25.16.6889-6898.2005
76. Basile JR, Castilho RM, Williams VP, Gutkind JS. Semaphorin 4D provides a link between axon guidance processes and tumor-induced angiogenesis. Proc Natl Acad Sci U S A 2006; 103:9017-22; PMID:16754882; http://dx.doi.org/10.1073/pnas.0508825103
77. Yang YH, Zhou H, Binmadi NO, Proia P, Basile JR. Plexin-B1 activates NF-kappaB and IL-8 to promote a pro-angiogenic response in endothelial cells. PloS One 2011; 6:e25826; PMID:22028792; http://dx.doi.org/10.1371/journal.pone.0025826
78. Zhou H, Yang YH, Binmadi NO, Proia P, Basile JR. The hypoxia-inducible factor-responsive proteins semaphorin 4D and vascular endothelial growth factor promote tumor growth and angiogenesis in oral squamous cell carcinoma. Exp Cell Res 2012; 318:1685-98; PMID:22652457; http://dx.doi.org/10.1016/j.yexcr.2012.04.019
79. Zhou H, Binmadi NO, Yang YH, Proia P, Basile JR. Semaphorin 4D cooperates with VEGF to promote angiogenesis and tumor progression. Angiogenesis 2012; 15:391-407; PMID:22476930; http://dx.doi.org/10.1007/s10456-012-9268-y
80. Binmadi NO, Yang YH, Zhou H, Proia P, Lin YL, De Paula AM, Guimaraes AL, Poswar FO, Sundararajan D, Basile JR. Plexin-B1 and semaphorin 4D cooperate to promote perineural invasion in a RhoA/ROK-dependent manner. Am J Pathol 2012; 180:1232-42; PMID:22252234; http://dx.doi.org/10.1016/j.ajpath.2011.12.009
81. Patnaik A, Weiss GJ, Leonard JE, Rasco DW, Sachdev JC, Fisher TL, Winter LA, Reilly C, Parker RB, Mutz D, et al. Safety, pharmacokinetics, and pharmacodynamics of a humanized anti-semaphorin 4D antibody, in a first-in-human study of patients with advanced solid tumors. Clin Cancer Res 2015; 22(4):827-36; PMID:26446947; http://dx.doi.org/10.1158/1078-0432.CCR-15-0431
82. Leonard JE, Fisher TL, Winter LA, Cornelius CA, Reilly C, Smith ES, Zauderer M. Nonclinical safety evaluation of VX15/2503, a humanized IgG4 anti-SEMA4D antibody. Mol Cancer Therap 2015; 14:964-72; PMID:25657333; http://dx.doi.org/10.1158/1535-7163.MCT-14-0924
83. Fisher TL, Seils J, Reilly C, Litwin V, Green L, Salkowitz-Bokal J, Walsh R, Harville S, Leonard JE, Smith E, et al. Saturation monitoring of VX15/2503, a novel semaphorin 4D-specific antibody, in clinical trials. Cytometry B Clin Cytom 2015; PMID:26566052
84. Fisher TL, Reilly CA, Winter LA, Pandina T, Jonason A, Scrivens M, Balch L, Bussler H, Torno S, Seils J, et al. Generation and preclinical characterization of an antibody specific for SEMA4D. mAbs 2016; 8:150-62; PMID:26431358; http://dx.doi.org/10.1080/19420862.2015.1102813
85. Evans EE, Jonason AS, Jr, Bussler H, Torno S, Veeraraghavan J, Reilly C, Doherty MA, Seils J, Winter LA, Mallow C, et al. Antibody blockade of semaphorin 4D promotes immune infiltration into tumor and enhances response to other immunomodulatory therapies. Cancer Immunol Res 2015; 3:689-701; PMID:25614511; http://dx.doi.org/10.1158/2326-6066.CIR-14-0171
86. Ding Y, He D, Florentin D, Frolov A, Hilsenbeck S, Ittmann M, Kadmon D, Miles B, Rowley D, Ayala G. Semaphorin 4F as a critical regulator of neuroepithelial interactions and a biomarker of aggressive prostate cancer. Clin Cancer Res 2013; 19:6101-11; PMID:24097862; http://dx.doi.org/10.1158/1078-0432.CCR-12-3669
87. Li X, Law JW, Lee AY. Semaphorin 5A and plexin-B3 regulate human glioma cell motility and morphology through Rac1 and the actin cytoskeleton. Oncogene 2012; 31:595-610; PMID:21706053
88. Li X, Lee AY. Semaphorin 5A and plexin-B3 inhibit human glioma cell motility through RhoGDIalpha-mediated inactivation of Rac1 GTPase. J Biol Chem 2010; 285:32436-45; PMID:20696765; http://dx.doi.org/10.1074/jbc.M110.120451
89. Hirota E, Yan L, Tsunoda T, Ashida S, Fujime M, Shuin T, Miki T, Nakamura Y, Katagiri T. Genome-wide gene expression profiles of clear cell renal cell carcinoma:identification of molecular targets for treatment of renal cell carcinoma. Int J Oncol 2006; 29:799-827; PMID:16964377
90. Lu TP, Tsai MH, Lee JM, Hsu CP, Chen PC, Lin CW, Shih JY, Yang PC, Hsiao CK, Lai LC, et al. Identification of a novel biomarker, SEMA5A, for non-small cell lung carcinoma in nonsmoking women. Cancer Epidemiol Biomarkers Prev 2010; 19:2590-7; PMID:20802022; http://dx.doi.org/10.1158/1055-9965.EPI-10-0332
91. Loria R, Bon G, Perotti V, Gallo E, Bersani I, Baldassari P, Porru M, Leonetti C, Di Carlo S, Visca P, et al. Sema6A and Mical1 control cell growth and survival of BRAFV600E human melanoma cells. Oncotarget 2015; 6:2779-93; PMID:25576923; http://dx.doi.org/10.18632/oncotarget.2995
92. Kigel B, Rabinowicz N, Varshavsky A, Kessler O, Neufeld G. Plexin-A4 promotes tumor progression and tumor angiogenesis by enhancement of VEGF and bFGF signaling. Blood 2011; 118:4285-96; PMID:21832283; http://dx.doi.org/10.1182/blood-2011-03-341388
93. Rice DS, Huang W, Jones HA, Hansen G, Ye GL, Xu N, Wilson EA, Troughton K, Vaddi K, Newton RC, et al. Severe retinal degeneration associated with disruption of semaphorin 4A. Invest Ophthalmol Vis Sci 2004; 45:2767-77; PMID:15277503; http://dx.doi.org/10.1167/iovs.04-0020
94. Kumanogoh A, Shikina T, Suzuki K, Uematsu S, Yukawa K, Kashiwamura S, Tsutsui H, Yamamoto M, Takamatsu H, Ko-Mitamura EP, et al. Nonredundant roles of Sema4A in the immune system:defective T cell priming and Th1/Th2 regulation in Sema4A-deficient mice. Immunity 2005; 22:305-16; PMID:15780988; http://dx.doi.org/10.1016/j.immuni.2005.01.014
95. Yukawa K, Tanaka T, Bai T, Ueyama T, Owada-Makabe K, Tsubota Y, Maeda M, Suzuki K, Kikutani H, Kumanogoh A. Semaphorin 4A induces growth cone collapse of hippocampal neurons in a Rho/Rho-kinase-dependent manner. Int J Mol Med 2005; 16:115-8; PMID:15942687
96. Abid A, Ismail M, Mehdi SQ, Khaliq S. Identification of novel mutations in the SEMA4A gene associated with retinal degenerative diseases. J Med Genet 2006; 43:378-81; PMID:16199541; http://dx.doi.org/10.1136/jmg.2005.035055
97. Makino N, Toyofuku T, Takegahara N, Takamatsu H, Okuno T, Nakagawa Y, Kang S, Nojima S, Hori M, Kikutani H, et al. Involvement of Sema4A in the progression of experimental autoimmune myocarditis. FEBS Lett 2008; 582:3935-40; PMID:18977352; http://dx.doi.org/10.1016/j.febslet.2008.10.040
98. Nkyimbeng-Takwi EH, Shanks K, Smith E, Iyer A, Lipsky MM, Detolla LJ, Kikutani H, Keegan AD, Chapoval SP. Neuroimmune semaphorin 4A downregulates the severity of allergic response. Mucosal Immunol 2012; 5:409-19; PMID:22472774; http://dx.doi.org/10.1038/mi.2012.18
99. Toyofuku T, Nojima S, Ishikawa T, Takamatsu H, Tsujimura T, Uemura A, Matsuda J, Seki T, Kumanogoh A. Endosomal sorting by Semaphorin 4A in retinal pigment epithelium supports photoreceptor survival. Genes Dev 2012; 26:816-29; PMID:22465952; http://dx.doi.org/10.1101/gad.184481.111
100. Morihana T, Goya S, Mizui M, Yasui T, Prasad DV, Kumanogoh A, Tamura M, Shikina T, Maeda Y, Iwamoto Y, et al. An inhibitory role for Sema4A in antigen-specific allergic asthma. J Clin Immunol 2013; 33:200-9; PMID:23007237; http://dx.doi.org/10.1007/s10875-012-9798-5
101. Ito D, Nojima S, Nishide M, Okuno T, Takamatsu H, Kang S, Kimura T, Yoshida Y, Morimoto K, Maeda Y, et al. mTOR complex signaling through the SEMA4A-Plexin B2 axis is required for optimal activation and differentiation of CD8+ T cells. J Immunol 2015; 195:934-43; PMID:26116513; http://dx.doi.org/10.4049/jimmunol.1403038
102. Wang L, Song G, Zheng Y, Tan W, Pan J, Zhao Y, Chang X. Expression of Semaphorin 4A and its potential role in rheumatoid arthritis. Arthritis Res Ther 2015; 17:227; PMID:26303122; http://dx.doi.org/10.1186/s13075-015-0734-y
103. Nakagawa Y, Takamatsu H, Okuno T, Kang S, Nojima S, Kimura T, Kataoka TR, Ikawa M, Toyofuku T, Katayama I, et al. Identification of semaphorin 4B as a negative regulator of basophil-mediated immune responses. J Immunol 2011; 186:2881-8; PMID:21270411; http://dx.doi.org/10.4049/jimmunol.1003485
104. Ben-Gigi L, Sweetat S, Besser E, Fellig Y, Wiederhold T, Polakiewicz RD, Behar O. Astrogliosis Induced by Brain Injury Is Regulated by Sema4B Phosphorylation(123). eNeuro 2015; 2; PMID:26464987
105. Fan JD, Zhu LL, Zhao T. [Sema4C expresses in neural stem cells]. Zhongguo Ying Yong Sheng Li Xue Za Zhi 2007; 23:153-4.
106. Fan W, Wu H, Fan J, Wu Y, Fan M. SEMA4C expression in neural stem/progenitor cells and in adult neurogenesis induced by cerebral ischemia. J Physiol Sci 2009; 59:>442.
107. Wu H, Fan J, Zhu L, Liu S, Wu Y, Zhao T, Wu Y, Ding X, Fan W, Fan M. Sema4C expression in neural stem/progenitor cells and in adult neurogenesis induced by cerebral ischemia. J Mol Neurosci 2009; 39:27-39; PMID:19189244; http://dx.doi.org/10.1007/s12031-009-9177-8
108. Perala N, Jakobson M, Nymark M, Penachioni J, Tanninen T, Immonen T, Tamagnone L, Sariola H. Sema4C-plexin B2-signalling modulates morphogenesis of the ureteric epithelium. Mech Dev 2009; 126:S213-S4; PMID:21035938; http://dx.doi.org/10.1016/j.mod.2009.06.537
109. Perala N, Jakobson M, Ola R, Fazzari P, Penachioni JY, Nymark M, Tanninen T, Immonen T, Tamagnone L, Sariola H. Sema4C-Plexin B2 signalling modulates ureteric branching in developing kidney. Differentiation 2010; 80:S55-S; PMID:21035938; http://dx.doi.org/10.1016/j.diff.2010.09.120
110. Zeng R, Han M, Luo Y, Li C, Pei G, Liao W, Bai S, Ge S, Liu X, Xu G. Role of Sema4C in TGF-beta1-induced mitogen-activated protein kinase activation and epithelial-mesenchymal transition in renal tubular epithelial cells. Nephrol Dial Transplant 2011; 26:1149-56; PMID:20959347; http://dx.doi.org/10.1093/ndt/gfq619
111. Shi W, Kumanogoh A, Watanabe C, Uchida J, Wang X, Yasui T, Yukawa K, Ikawa M, Okabe M, Parnes JR, et al. The class IV semaphorin CD100 plays nonredundant roles in the immune system:defective B and T cell activation in CD100-deficient mice. Immunity 2000; 13:633-42; PMID:11114376; http://dx.doi.org/10.1016/S1074-7613(00)00063-7
112. Wang X, Kumanogoh A, Watanabe C, Shi W, Yoshida K, Kikutani H. Functional soluble CD100/Sema4D released from activated lymphocytes:possible role in normal and pathologic immune responses. Blood 2001; 97:3498-504; PMID:11369643; http://dx.doi.org/10.1182/blood.V97.11.3498
113. Granziero L, Circosta P, Scielzo C, Frisaldi E, Stella S, Geuna M, Giordano S, Ghia P, Caligaris-Cappio F. CD100/Plexin-B1 interactions sustain proliferation and survival of normal and leukemic CD5+ B lymphocytes. Blood 2003; 101:1962-9; PMID:12406905; http://dx.doi.org/10.1182/blood-2002-05-1339
114. Moreau-Fauvarque C, Kumanogoh A, Camand E, Jaillard C, Barbin G, Boquet I, Love C, Jones EY, Kikutani H, Lubetzki C, et al. The transmembrane semaphorin Sema4D/CD100, an inhibitor of axonal growth, is expressed on oligodendrocytes and upregulated after CNS lesion. J Neurosci 2003; 23:9229-39; PMID:14534257
115. Masuda K, Furuyama T, Takahara M, Fujioka S, Kurinami H, Inagaki S. Sema4D stimulates axonal outgrowth of embryonic DRG sensory neurones. Genes Cells 2004; 9:821-9; PMID:15330859; http://dx.doi.org/10.1111/j.1365-2443.2004.00766.x
116. Duran-Struuck R, Tawara I, Lowler K, Clouthier SG, Weisiger E, Rogers C, Luker G, Kumanogoh A, Liu C, Ferrara JL, et al. A novel role for the semaphorin Sema4D in the induction of allo-responses. Biol Blood Marrow Transplant 2007; 13:1294-303; PMID:17950916; http://dx.doi.org/10.1016/j.bbmt.2006.12.237
117. Lin X, Ogiya M, Takahara M, Yamaguchi W, Furuyama T, Tanaka H, Tohyama M, Inagaki S. Sema4D-plexin-B1 implicated in regulation of dendritic spine density through RhoA/ROCK pathway. Neurosci Lett 2007; 428:1-6; PMID:17950529; http://dx.doi.org/10.1016/j.neulet.2007.09.045
118. Zhu L, Bergmeier W, Wu J, Jiang H, Stalker TJ, Cieslak M, Fan R, Boumsell L, Kumanogoh A, Kikutani H, et al. Regulated surface expression and shedding support a dual role for semaphorin 4D in platelet responses to vascular injury. Proc Natl Acad Sci U S A 2007; 104:1621-6; PMID:17244710; http://dx.doi.org/10.1073/pnas.0606344104
119. Abe M, Inagaki S, Furuyama T, Iwamoto M, Wakisaka S. Semaphorin 4D inhibits collagen synthesis of rat pulp-derived cells. Arch Oral Biol 2008; 53:27-34; PMID:17920031; http://dx.doi.org/10.1016/j.archoralbio.2007.08.005
120. Korostylev A, Worzfeld T, Deng S, Friedel RH, Swiercz JM, Vodrazka P, Maier V, Hirschberg A, Ohoka Y, Inagaki S, et al. A functional role for semaphorin 4D/plexin B1 interactions in epithelial branching morphogenesis during organogenesis. Dev (Cambridge, England) 2008; 135:3333-43; PMID:18799546; http://dx.doi.org/10.1242/dev.019760
121. Fuchikawa T, Nakamura F, Fukuda N, Takei K, Goshima Y. Protein tyrosine phosphatase SHP2 is involved in Semaphorin 4D-induced axon repulsion. Biochem Biophys Res Commun 2009; 385:6-10; PMID:19433062; http://dx.doi.org/10.1016/j.bbrc.2009.05.024
122. Saito Y, Oinuma I, Fujimoto S, Negishi M. Plexin-B1 is a GTPase activating protein for M-Ras, remodelling dendrite morphology. EMBO Rep 2009; 10:614-21; PMID:19444311; http://dx.doi.org/10.1038/embor.2009.63
123. Toguchi M, Gonzalez D, Furukawa S, Inagaki S. Involvement of Sema4D in the control of microglia activation. Neurochem Int 2009; 55:573-80; PMID:19467284; http://dx.doi.org/10.1016/j.neuint.2009.05.013
124. Yukawa K, Tanaka T, Takeuchi N, Iso H, Li L, Kohsaka A, Waki H, Miyajima M, Maeda M, Kikutani H, et al. Sema4D/CD100 deficiency leads to superior performance in mouse motor behavior. Can J Neurol Sci 2009; 36:349-55; PMID:19534337; http://dx.doi.org/10.1017/S0317167100007101
125. Wannemacher KM, Zhu L, Jiang H, Fong KP, Stalker TJ, Lee D, Tran AN, Neeves KB, Maloney S, Kumanogoh A, et al. Diminished contact-dependent reinforcement of Syk activation underlies impaired thrombus growth in mice lacking Semaphorin 4D. Blood 2010; 116:5707-15; PMID:20855865; http://dx.doi.org/10.1182/blood-2010-04-279943
126. Yukawa K, Tanaka T, Kishino M, Yoshida K, Takeuchi N, Ito T, Takamatsu H, Kikutani H, Kumanogoh A. Deletion of Sema4D gene reduces intimal neovascularization and plaque growth in apolipoprotein E-deficient mice. Int J Mol Med 2010; 26:39-44; PMID:20514420; http://dx.doi.org/10.3892/ijmm_00000432
127. Kuzirian MS, Moore AR, Staudenmaier EK, Friedel RH, Paradis S. The class 4 semaphorin Sema4D promotes the rapid assembly of GABAergic synapses in rodent hippocampus. J Neurosci 2013; 33:8961-73; PMID:23699507; http://dx.doi.org/10.1523/JNEUROSCI.0989-13.2013
128. Shanks K, Nkyimbeng-Takwi EH, Smith E, Lipsky MM, DeTolla LJ, Scott DW, Keegan AD, Chapoval SP. Neuroimmune semaphorin 4D is necessary for optimal lung allergic inflammation. Mol Immunol 2013; 56:480-7; PMID:23911404; http://dx.doi.org/10.1016/j.molimm.2013.05.228
129. Yang J, Zeng Z, Wei J, Jiang L, Ma Q, Wu M, Huang X, Ye S, Li Y, Ma D, et al. Sema4d is required for the development of the hindbrain boundary and skeletal muscle in zebrafish. Biochem Biophys Res Commun 2013; 433:213-9; PMID:23466355; http://dx.doi.org/10.1016/j.bbrc.2013.02.085
130. Xiao T, Shoji W, Zhou W, Su F, Kuwada JY. Transmembrane sema4E guides branchiomotor axons to their targets in zebrafish. J Neurosci 2003; 23:4190-8; PMID:12764107
131. Parrinello S, Noon LA, Harrisingh MC, Wingfield Digby P, Rosenberg LH, Cremona CA, Echave P, Flanagan AM, Parada LF, Lloyd AC. NF1 loss disrupts Schwann cell-axonal interactions:a novel role for semaphorin 4F. Genes Dev 2008; 22:3335-48; PMID:19056885; http://dx.doi.org/10.1101/gad.490608
132. Oster SF, Bodeker MO, He F, Sretavan DW. Invariant Sema5A inhibition serves an ensheathing function during optic nerve development. Development 2003; 130:775-84; PMID:12506007; http://dx.doi.org/10.1242/dev.00299
133. Hilario JD, Rodino-Klapac LR, Wang C, Beattie CE. Semaphorin 5A is a bifunctional axon guidance cue for axial motoneurons in vivo. Dev Biol 2009; 326:190-200; PMID:19059233; http://dx.doi.org/10.1016/j.ydbio.2008.11.007
134. Matsuoka RL, Chivatakarn O, Badea TC, Samuels IS, Cahill H, Katayama K, Kumar SR, Suto F, Chedotal A, Peachey NS, et al. Class 5 transmembrane semaphorins control selective Mammalian retinal lamination and function. Neuron 2011; 71:460-73; PMID:21835343; http://dx.doi.org/10.1016/j.neuron.2011.06.009
135. Matsuoka RL, Sun LO, Katayama K, Yoshida Y, Kolodkin AL. Sema6B, Sema6C, and Sema6D expression and function during mammalian retinal development. PLoS One 2013; 8:e63207; PMID:23646199; http://dx.doi.org/10.1371/journal.pone.0063207
136. Duan Y, Wang SH, Song J, Mironova Y, Ming GL, Kolodkin AL, Giger RJ. Semaphorin 5A inhibits synaptogenesis in early postnatal- and adult-born hippocampal dentate granule cells. Elife 2014; 3; PMID:25313870
137. Masuda T, Sakuma C, Yaginuma H, Taniguchi M. Attractive and permissive activities of semaphorin 5A toward dorsal root ganglion axons in higher vertebrate embryos. Cell Adh Migr 2014; 8:603-6; PMID:25622099; http://dx.doi.org/10.4161/19336918.2014.972770
138. Yu X, Wang F, Zhang JP. Meta analysis of the association of rs7702187 SNP in SEMA5A gene with risk of Parkinson's disease. Euro Rev Med Pharmacol Sci 2014; 18:900-4; PMID:24706317
139. O'Connor TP, Cockburn K, Wang W, Tapia L, Currie E, Bamji SX. Semaphorin 5B mediates synapse elimination in hippocampal neurons. Neural Dev 2009; 4:18; PMID:19463192; http://dx.doi.org/10.1186/1749-8104-4-18
140. Browne K, Wang W, Liu RQ, Piva M, O'Connor TP. Transmembrane semaphorin5B is proteolytically processed into a repulsive neural guidance cue. J Neurochem 2012; 123:135-46; PMID:22817385; http://dx.doi.org/10.1111/j.1471-4159.2012.07885.x
141. Liu RQ, Wang W, Legg A, Abramyan J, O'Connor TP. Semaphorin 5B is a repellent cue for sensory afferents projecting into the developing spinal cord. Development 2014; 141:1940-9; PMID:24718987; http://dx.doi.org/10.1242/dev.103630
142. Rollmann SM, Yamamoto A, Goossens T, Zwarts L, Callaerts-Vegh Z, Callaerts P, Norga K, Mackay TF, Anholt RR. The early developmental gene Semaphorin 5c contributes to olfactory behavior in adult Drosophila. Genetics 2007; 176:947-56; PMID:17435226; http://dx.doi.org/10.1534/genetics.106.069781
143. Xu XM, Fisher DA, Zhou L, White FA, Ng S, Snider WD, Luo Y. The transmembrane protein semaphorin 6A repels embryonic sympathetic axons. J Neurosci 2000; 20:2638-48; PMID:10729344
144. Gautier G, de Saint-Vis B, Senechal B, Pin JJ, Bates EE, Caux C, Geissmann F, Garrone P. The class 6 semaphorin SEMA6A is induced by interferon-gamma and defines an activation status of langerhans cells observed in pathological situations. Am J Pathol 2006; 168:453-65; PMID:16436660; http://dx.doi.org/10.2353/ajpath.2006.050288
145. Mauti O, Domanitskaya E, Andermatt I, Sadhu R, Stoeckli ET. Semaphorin6A acts as a gate keeper between the central and the peripheral nervous system. Neural Dev 2007; 2:28; PMID:18088409; http://dx.doi.org/10.1186/1749-8104-2-28
146. Renaud J, Kerjan G, Sumita I, Zagar Y, Georget V, Kim D, Fouquet C, Suda K, Sanbo M, Suto F, et al. Plexin-A2 and its ligand, Sema6A, control nucleus-centrosome coupling in migrating granule cells. Nat Neurosci 2008; 11:440-9; PMID:18327254; http://dx.doi.org/10.1038/nn2064
147. Runker AE, Little GE, Suto F, Fujisawa H, Mitchell KJ. Semaphorin-6A controls guidance of corticospinal tract axons at multiple choice points. Neural Dev 2008; 3:34; PMID:19063725; http://dx.doi.org/10.1186/1749-8104-3-34
148. Zhuang B, Su YS, Sockanathan S. FARP1 promotes the dendritic growth of spinal motor neuron subtypes through transmembrane Semaphorin6A and PlexinA4 signaling. Neuron 2009; 61:359-72; PMID:19217374; http://dx.doi.org/10.1016/j.neuron.2008.12.022
149. Rogalewski A, Dittgen T, Klugmann M, Kirsch F, Kruger C, Pitzer C, Minnerup J, Schabitz WR, Schneider A. Semaphorin 6A improves functional recovery in conjunction with motor training after cerebral ischemia. PLoS One 2010; 5:e10737; PMID:20505770
150. Runker AE, O'Tuathaigh C, Dunleavy M, Morris DW, Little GE, Corvin AP, Gill M, Henshall DC, Waddington JL, Mitchell KJ. Mutation of Semaphorin-6A disrupts limbic and cortical connectivity and models neurodevelopmental psychopathology. PLoS One 2011; 6:e26488; PMID:22132072; http://dx.doi.org/10.1371/journal.pone.0026488
151. Ebert AM, Childs SJ, Hehr CL, Cechmanek PB, McFarlane S. Sema6a and Plxna2 mediate spatially regulated repulsion within the developing eye to promote eye vesicle cohesion. Development 2014; 141:2473-82; PMID:24917502; http://dx.doi.org/10.1242/dev.103499
152. Tawarayama H, Yoshida Y, Suto F, Mitchell KJ, Fujisawa H. Roles of semaphorin-6B and plexin-A2 in lamina-restricted projection of hippocampal mossy fibers. J Neurosci 2010; 30:7049-60; PMID:20484647; http://dx.doi.org/10.1523/JNEUROSCI.0073-10.2010
153. Andermatt I, Wilson NH, Bergmann T, Mauti O, Gesemann M, Sockanathan S, Stoeckli ET. Semaphorin 6B acts as a receptor in post-crossing commissural axon guidance. Development (Cambridge, England) 2014; 141:3709-20; PMID:25209245; http://dx.doi.org/10.1242/dev.112185
154. Burgaya F, Fontana X, Martinez A, Montolio M, Mingorance A, Simo S, del Rio JA, Soriano E. Semaphorin 6C leads to GSK-3-dependent growth cone collapse and redistributes after entorhino-hippocampal axotomy. Mol Cell Neurosci 2006; 33:321-34; PMID:17029982; http://dx.doi.org/10.1016/j.mcn.2006.08.008
155. Svensson A, Libelius R, Tagerud S. Semaphorin 6C expression in innervated and denervated skeletal muscle. J Mol Histol 2008; 39:5-13; PMID:17605078; http://dx.doi.org/10.1007/s10735-007-9113-6
156. Leslie JR, Imai F, Fukuhara K, Takegahara N, Rizvi TA, Friedel RH, Wang F, Kumanogoh A, Yoshida Y. Ectopic myelinating oligodendrocytes in the dorsal spinal cord as a consequence of altered semaphorin 6D signaling inhibit synapse formation. Development 2011; 138:4085-95; PMID:21831918; http://dx.doi.org/10.1242/dev.066076
157. Kuwajima T, Yoshida Y, Takegahara N, Petros TJ, Kumanogoh A, Jessell TM, Sakurai T, Mason C. Optic chiasm presentation of Semaphorin6D in the context of Plexin-A1 and Nr-CAM promotes retinal axon midline crossing. Neuron 2012; 74:676-90; PMID:22632726; http://dx.doi.org/10.1016/j.neuron.2012.03.025
158. Toyofuku T, Yabuki M, Kamei J, Kamei M, Makino N, Kumanogoh A, Hori M. Semaphorin-4A, an activator for T-cell-mediated immunity, suppresses angiogenesis via Plexin-D1. EMBO J 2007; 26:1373-84; PMID:17318185; http://dx.doi.org/10.1038/sj.emboj.7601589
159. Donnard E, Asprino PF, Correa BR, Bettoni F, Koyama FC, Navarro FC, Perez RO, Mariadason J, Sieber OM, Strausberg RL, et al. Mutational analysis of genes coding for cell surface proteins in colorectal cancer cell lines reveal novel altered pathways, druggable mutations and mutated epitopes for targeted therapy. Oncotarget 2014; 5:9199-213; PMID:25193853; http://dx.doi.org/10.18632/oncotarget.2374
160. Li J, Wang Q, Wen R, Liang J, Zhong X, Yang W, Su D, Tang J. MiR-138 inhibits cell proliferation and reverses epithelial-mesenchymal transition in non-small cell lung cancer cells by targeting GIT1 and SEMA4C. J Cell Mol Med 2015; 19:2793-805; PMID:26283050
161. Liu H, Yang Y, Xiao J, Yang S, Liu Y, Kang W, Li X, Zhang F. Semaphorin 4D expression is associated with a poor clinical outcome in cervical cancer patients. Microvasc Res 2014; 93:1-8; PMID:24603190; http://dx.doi.org/10.1016/j.mvr.2014.02.007
162. Mu L, Wang J, Chen Y, Li L, Guo X, Zheng S, Jing C. Hypoxia-inducible factor-1alpha and semaphorin4D genes involved with tumor-associated macrophage-induced metastatic behavior and clinical significance in colon cancer. Chin Med J (Engl) 2014; 127:3568-75; PMID:25316231
163. Sun Q, Zhou H, Binmadi NO, Basile JR. Hypoxia-inducible factor-1-mediated regulation of semaphorin 4D affects tumor growth and vascularity. J Biol Chem 2009; 284:32066-74; PMID:19762474; http://dx.doi.org/10.1074/jbc.M109.057166
164. Qiang R, Wang F, Shi LY, Liu M, Chen S, Wan HY, Li YX, Li X, Gao SY, Sun BC, et al. Plexin-B1 is a target of miR-214 in cervical cancer and promotes the growth and invasion of HeLa cells. Int J Biochem Cell Biol 2011; 43:632-41; PMID:21216304; http://dx.doi.org/10.1016/j.biocel.2011.01.002
165. Chen Y, Zhang L, Pan Y, Ren X, Hao Q. Over-expression of semaphorin4D, hypoxia-inducible factor-1alpha and vascular endothelial growth factor is related to poor prognosis in ovarian epithelial cancer. Int J Mol Sci 2012; 13:13264-74; PMID:23202951; http://dx.doi.org/10.3390/ijms131013264
166. Soong J, Chen Y, Shustef EM, Scott GA. Sema4D, the ligand for Plexin B1, suppresses c-Met activation and migration and promotes melanocyte survival and growth. J Invest Dermatol 2012; 132:1230-8; PMID:22189792; http://dx.doi.org/10.1038/jid.2011.414
167. Chen Y, Zhang L, Lv R, Zhang WQ. Overexpression of Semaphorin4D indicates poor prognosis and prompts monocyte differentiation toward M2 macrophages in epithelial ovarian cancer. Asian Pac J Cancer Prev 2013; 14:5883-90; PMID:24289594; http://dx.doi.org/10.7314/APJCP.2013.14.10.5883
168. Ruan SS, Li RC, Han Q, Liu J, Li GL, Song YQ, Wu G. Expression and clinical significance of Semaphorin4D in non-small cell lung cancer and its impact on malignant behaviors of A549 lung cancer cells. J Huazhong Univ Sci Technolog Med Sci 2014; 34:491-6; PMID:25135716; http://dx.doi.org/10.1007/s11596-014-1304-2
169. Younis RH, Han KL, Webb TJ. Human head and neck squamous cell carcinoma-associated semaphorin 4D induces expansion of myeloid-derived suppressor cells. J Immunol (Baltimore, Md:1950) 2016; 196:1419-29; PMID:26740106
170. Ayala GE, Dai H, Powell M, Li R, Ding Y, Wheeler TM, Shine D, Kadmon D, Thompson T, Miles BJ, et al. Cancer-related axonogenesis and neurogenesis in prostate cancer. Clin Cancer Res 2008; 14:7593-603; PMID:19047084; http://dx.doi.org/10.1158/1078-0432.CCR-08-1164
171. Wang X, Zbou C, Qiu G, Fan J, Tang H, Peng Z. Screening of new tumor suppressor genes in sporadic colorectal cancer patients. Hepatogastroenterology 2008; 55:2039-44; PMID:19260473
172. Sadanandam A, Varney ML, Kinarsky L, Ali H, Mosley RL, Singh RK. Identification of functional cell adhesion molecules with a potential role in metastasis by a combination of in vivo phage display and in silico analysis. Omics:J Integrat Biol 2007; 11:41-57; PMID:17411395; http://dx.doi.org/10.1089/omi.2006.0004
173. Sadanandam A, Rosenbaugh EG, Singh S, Varney M, Singh RK. Semaphorin 5A promotes angiogenesis by increasing endothelial cell proliferation, migration, and decreasing apoptosis. Microvasc Res 2010; 79:1-9; PMID:19850054; http://dx.doi.org/10.1016/j.mvr.2009.10.005
174. Sadanandam A, Varney ML, Singh S, Ashour AE, Moniaux N, Deb S, Lele SM, Batra SK, Singh RK. High gene expression of semaphorin 5A in pancreatic cancer is associated with tumor growth, invasion and metastasis. Int J Cancer J Int du Cancer 2010; 127:1373-83; PMID:20073063; http://dx.doi.org/10.1002/ijc.25166
175. Sadanandam A, Sidhu SS, Wullschleger S, Singh S, Varney ML, Yang CS, Ashour AE, Batra SK, Singh RK. Secreted semaphorin 5A suppressed pancreatic tumour burden but increased metastasis and endothelial cell proliferation. Brit J Cancer 2012; 107:501-7; PMID:22782341; http://dx.doi.org/10.1038/bjc.2012.298
176. Grundmann S, Lindmayer C, Hans FP, Hoefer I, Helbing T, Pasterkamp G, Bode C, de Kleijn D, Moser M. FoxP1 stimulates angiogenesis by repressing the inhibitory guidance protein semaphorin 5B in endothelial cells. PLoS One 2013; 8:e70873; PMID:24023716
177. Woodhouse EC, Fisher A, Bandle RW, Bryant-Greenwood B, Charboneau L, Petricoin EF, 3rd, Liotta LA. Drosophila screening model for metastasis:Semaphorin 5c is required for l(2)gl cancer phenotype. Proc Natl Acad Sci U S A 2003; 100:11463-8; PMID:14500904; http://dx.doi.org/10.1073/pnas.2031202100
178. Segarra M, Ohnuki H, Maric D, Salvucci O, Hou X, Kumar A, Li X, Tosato G. Semaphorin 6A regulates angiogenesis by modulating VEGF signaling. Blood 2012; 120:4104-15; PMID:23007403; http://dx.doi.org/10.1182/blood-2012-02-410076
179. Zhao J, Tang H, Zhao H, Che W, Zhang L, Liang P. SEMA6A is a prognostic biomarker in glioblastoma. Tumour Biol:J Int Soc Oncodev Biol Med 2015; 36:8333-40; PMID:26014517; http://dx.doi.org/10.1007/s13277-015-3584-y
180. Correa RG, Sasahara RM, Bengtson MH, Katayama ML, Salim AC, Brentani MM, Sogayar MC, de Souza SJ, Simpson AJ. Human semaphorin 6B [(HSA)SEMA6B], a novel human class 6 semaphorin gene:alternative splicing and all-trans-retinoic acid-dependent downregulation in glioblastoma cell lines. Genomics 2001; 73:343-8; PMID:11350127; http://dx.doi.org/10.1006/geno.2001.6525
181. Murad H, Collet P, Huin-Schohn C, Al-Makdissy N, Kerjan G, Chedotal A, Donner M, Devignes MD, Becuwe P, Schohn H, et al. Effects of PPAR and RXR ligands in semaphorin 6B gene expression of human MCF-7 breast cancer cells. Int J Oncol 2006; 28:977-84; PMID:16525649
182. D'Apice L, Costa V, Valente C, Trovato M, Pagani A, Manera S, Regolo L, Zambelli A, Ciccodicola A, De Berardinis P. Analysis of SEMA6B gene expression in breast cancer:identification of a new isoform. Biochim Biophys Acta 2013; 1830:4543-53; PMID:23665584; http://dx.doi.org/10.1016/j.bbagen.2013.05.003
183. Catalano A, Lazzarini R, Di Nuzzo S, Orciari S, Procopio A. The plexin-A1 receptor activates vascular endothelial growth factor-receptor 2 and nuclear factor-kappaB to mediate survival and anchorage-independent growth of malignant mesothelioma cells. Cancer Res 2009; 69:1485-93; PMID:19176370; http://dx.doi.org/10.1158/0008-5472.CAN-08-3659
184. Chen D, Li Y, Wang L, Jiao K. SEMA6D expression and patient survival in breast invasive carcinoma. Int J Breast Cancer 2015; 2015:539721; PMID:25973277; http://dx.doi.org/10.1155/2015/539721