A Class III semaphorin (Sema3e) inhibits mouse osteoblast migration and decreases osteoclast formation in vitro

Calcified Tissue International

Volumn 90, Issue 2, 2012, Pages 151-162

  Hughes, Alun ^a   Kleine Albers, Jennifer ^a   Helfrich, Miep H ^a   Ralston, Stuart H ^b   Rogers, Michael J ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Macrophage; Migration; Mineralization; Plexin; Vitamin D 3

Indexed keywords

ALKALINE PHOSPHATASE; SEMAPHORIN; SEMAPHORIN 3A; SEMAPHORIN 3E; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DENSITY; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENE PRODUCT; HOMEOSTASIS; IN VITRO STUDY; MINERALIZATION; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; PLEXINA1 GENE; PLEXIND1 GENE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; SEMA3A GENE; SEMA3B GENE; SEMA3C GENE; SEMA3D GENE; SEMA3E GENE; SEMA3F GENE; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; OSTEOBLASTS; OSTEOCLASTS; RABBITS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84857050352     PISSN: 0171967X     EISSN: 14320827     Source Type: Journal    
DOI: 10.1007/s00223-011-9560-7     Document Type: Article

References (46)

1. RJ Pasterkamp AL Kolodkin 2003 Semaphorin junction: making tracks toward neural connectivity Curr Opin Neurobiol 13 1 79 89 12593985 10.1016/S0959- 4388(03)00003-5 1:CAS:528:DC%2BD3sXht1Krt7k%3D (Pubitemid 36197931)
2. L Tamagnone PM Comoglio 2000 Signalling by semaphorin receptors: cell guidance and beyond Trends Cell Biol 10 9 377 383 10932095 10.1016/S0962- 8924(00)01816-X 1:CAS:528:DC%2BD3cXls1CktLY%3D (Pubitemid 30612470)
3. U Yazdani JR Terman 2006 The semaphorins Genome Biol 7 3 211 16584533 10.1186/gb-2006-7-3-211 (Pubitemid 44774190)
4. C Gu Y Yoshida J Livet DV Reimert F Mann J Merte CE Henderson TM Jessell AL Kolodkin DD Ginty 2005 Semaphorin 3E and PlexinD1 control vascular pattern independently of neuropilins Science 307 5707 265 268 15550623 10.1126/science.1105416 1:CAS:528:DC%2BD2MXisVKktg%3D%3D (Pubitemid 40116243)
5. A Togari M Mogi M Arai S Yamamoto Y Koshihara 2000 Expression of mRNA for axon guidance molecules, such as semaphorin-III, netrins and neurotrophins, in human osteoblasts and osteoclasts Brain Res 878 1-2 204 209 10996153 10.1016/S0006-8993(00)02700-1 1:CAS:528:DC%2BD3cXms1Sqtbs%3D
6. C Gomez B Burt-Pichat F Mallein-Gerin B Merle PD Delmas TM Skerry L Vico L Malaval C Chenu 2005 Expression of Semaphorin-3A and its receptors in endochondral ossification: potential role in skeletal development and innervation Dev Dyn 234 2 393 403 16145665 10.1002/dvdy.20512 1:CAS:528:DC%2BD2MXhtFegtrbE (Pubitemid 41369149)
7. AL Sutton X Zhang DR Dowd YP Kharode BS Komm PN Macdonald 2008 Semaphorin 3B is a 1, 25-dihydroxyvitamin D3-induced gene in osteoblasts that promotes osteoclastogenesis and induces osteopenia in mice Mol Endocrinol 22 6 1370 1381 18356290 10.1210/me.2007-0363 1:CAS:528:DC%2BD1cXntFajtrY%3D (Pubitemid 351786997)
8. J Harper LC Gerstenfeld M Klagsbrun 2001 Neuropilin-1 expression in osteogenic cells: down-regulation during differentiation of osteoblasts into osteocytes J Cell Biochem 81 1 82 92 11180399 10.1002/1097-4644(20010401)81: 1<82::AID-JCB1025>3.0.CO;2-P 1:CAS:528:DC%2BD3MXhs12gtLg%3D (Pubitemid 32202741)
9. T Kanda Y Yoshida Y Izu A Nifuji Y Ezura K Nakashima M Noda 2007 PlexinD1 deficiency induces defects in axial skeletal morphogenesis J Cell Biochem 101 6 1329 1337 17477353 10.1002/jcb.21306 1:CAS:528:DC%2BD2sXpt1agt74%3D (Pubitemid 47242766)
10. CR Christensen J Klingelhöfer S Tarabykina EF Hulgaard D Kramerov E Lukanidin 1998 Transcription of a novel mouse semaphorin gene, M-semaH, correlates with the metastatic ability of mouse tumor cell lines Cancer Res 58 6 1238 1244 9515811 1:CAS:528:DyaK1cXhvV2rs7g%3D (Pubitemid 28183214)
11. S Rozen H Skaletsky 2000 Primer3 on the WWW for general users and for biologist programmers Methods Mol Biol 132 365 386 10547847 1:CAS:528: DyaK1MXmslKqsbo%3D
12. FP Coxon MH Helfrich RJ van't Hof SM Sebti SH Ralston AD Hamilton MJ Rogers 2000 Protein geranylgeranylation is required for osteoclast formation, function, and survival: inhibition by bisphosphonates and GGTI-298 J Bone Miner Res 15 1467 1476 10934645 10.1359/jbmr.2000.15.8.1467 1:CAS:528: DC%2BD3cXlvVSjsLw%3D (Pubitemid 30484516)
13. RJ van't Hof M von Lindern PJ Nijweide H Beug 1997 Stem cell factor stimulates chicken osteoclast activity in vitro FASEB J 11 287 293 9068618 (Pubitemid 27118330)
14. MW Pfaffl 2001 A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Res 29 9 e45 11328886 10.1093/nar/29.9.e45 1:STN:280:DC%2BD38nis12jtw%3D%3D
15. NS Datta AB Abou-Samra 2009 PTH and PTHrP signaling in osteoblasts Cell Signal 21 8 1245 1254 19249350 10.1016/j.cellsig.2009.02.012 1:CAS:528:DC%2BD1MXmtVWjtb4%3D
16. HC Tenenbaum JN Heersche 1982 Differentiation of osteoblasts and formation of mineralized bone in vitro Calcif Tissue Int 34 1 76 79 6802463 10.1007/BF02411212 1:STN:280:DyaL387mt1Squg%3D%3D (Pubitemid 12073844)
17. H Skjødt JA Gallagher JN Beresford M Couch JW Poser RG Russell 1985 Vitamin D metabolites regulate osteocalcin synthesis and proliferation of human bone cells in vitro J Endocrinol 105 3 391 396 3873510 10.1677/joe.0.1050391 (Pubitemid 15045857)
18. T Haneji N Kurihara K Ikeda M Kumegawa 1983 1α, 25-Dihydroxyvitamin D3 and analogues of vitamin D3 induce alkaline phosphatase activity in osteoblastic cells derived from newborn mouse calvaria J Biochem 94 4 1127 1132 6317662 1:CAS:528:DyaL3sXlslSgtLk%3D (Pubitemid 14227239)
19. M Tamura E Nemoto MM Sato A Nakashima H Shimauchi 2010 Role of the Wnt signaling pathway in bone and tooth Front Biosci (Elite Ed) 2 1405 1413 10.2741/E201
20. JD Berndt MC Halloran 2006 Semaphorin 3d promotes cell proliferation and neural crest cell development downstream of TCF in the zebrafish hindbrain Development 133 20 3983 3992 16971468 10.1242/dev.02583 1:CAS:528: DC%2BD28Xht1GrsbnF (Pubitemid 44756191)
21. P Kettunen S Løes T Furmanek K Fjeld IH Kvinnsland O Behar T Yagi H Fujisawa S Vainio M Taniguchi K Luukko 2005 Coordination of trigeminal axon navigation and patterning with tooth organ formation: epithelial-mesenchymal interactions, and epithelial Wnt4 and Tgfbeta1 regulate semaphorin 3a expression in the dental mesenchyme Development 132 2 323 334 15604101 10.1242/dev.01541 1:CAS:528:DC%2BD2MXhs1Wgt78%3D (Pubitemid 40268282)
22. H Aberle A Bauer J Stappert A Kispert R Kemler 1997 Beta-catenin is a target for the ubiquitin-proteasome pathway EMBO J 16 13 3797 3804 9233789 10.1093/emboj/16.13.3797 1:CAS:528:DyaK2sXkslShsbk%3D (Pubitemid 27280995)
23. N Sato L Meijer L Skaltsounis P Greengard AH Brivanlou 2004 Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor Nat Med 10 55 63 14702635 10.1038/nm979 1:CAS:528:DC%2BD2cXlsFGm (Pubitemid 38524699)
24. J Dai ABM Rabie 2007 VEGF: an essential mediator of both angiogenesis and endochondral ossification J Dent Res 86 937 17890669 10.1177/154405910708601006 1:CAS:528:DC%2BD2sXhtFOltbfM
25. A Vacca C Scavelli G Serini G Di Pietro T Cirulli F Merchionne D Ribatti F Bussolino D Guidolin G Piaggio A Bacigalupo F Dammacco 2006 Loss of inhibitory semaphorin 3A (SEMA3A) autocrine loops in bone marrow endothelial cells of patients with multiple myeloma Blood 108 5 1661 1667 16684957 10.1182/blood-2006-04-014563 1:CAS:528:DC%2BD28Xpt1Sltbk%3D (Pubitemid 44316135)
26. M Klagsbrun A Eichmann 2005 A role for axon guidance receptors and ligands in blood vessel development and tumor angiogenesis Cytokine Growth Factor Rev 16 4-5 535 548 15979925 10.1016/j.cytogfr.2005.05.002 1:CAS:528:DC%2BD2MXmvVCnu7c%3D (Pubitemid 41022016)
27. A Catalano P Caprari S Moretti M Faronato L Tamagnone A Procopio 2006 Semaphorin-3A is expressed by tumor cells and alters T-cell signal transduction and function Blood 107 8 3321 3329 16380453 10.1182/blood-2005-06-2445 1:CAS:528:DC%2BD28Xjs1OksL8%3D
28. H Kikutani K Suzuki A Kumanogoh 2007 Immune semaphorins: increasing members and their diverse roles Adv Immunol 93 121 143 17383540 10.1016/S0065-2776(06)93003-X 1:CAS:528:DC%2BD1cXisVKqtro%3D (Pubitemid 46454331)
29. DR Bielenberg Y Hida A Shimizu A Kaipainen M Kreuter CC Kim M Klagsbrun 2004 Semaphorin 3F, a chemorepulsant for endothelial cells, induces a poorly vascularized, encapsulated, nonmetastatic tumor phenotype J Clin Invest 114 9 1260 1271 15520858 1:CAS:528:DC%2BD2cXpsFCgtr8%3D (Pubitemid 40385297)
30. L Karayan-Tapon M Wager J Guilhot P Levillain C Marquant J Clarhaut V Potiron J Roche 2008 Semaphorin, neuropilin and VEGF expression in glial tumours: SEMA3G, a prognostic marker? Br J Cancer 99 7 1153 1160 18781179 10.1038/sj.bjc.6604641 1:CAS:528:DC%2BD1cXhtFyqt7vJ
31. A Chedotal G Kerjan C Moreau-Fauvarque 2005 The brain within the tumour: new roles for axon guidance molecules in cancers Cell Death Diff 12 1044 1056 10.1038/sj.cdd.4401707 1:CAS:528:DC%2BD2MXmtVylsrw%3D (Pubitemid 41065422)
32. RE Bachelder EA Lipscomb X Lin MA Wendt NH Chadborn BJ Eickholt AM Mercurio 2003 Competing autocrine pathways involving alternative neuropilin-1 ligands regulate chemotaxis of carcinoma cells Cancer Res 63 17 5230 5233 14500350 1:CAS:528:DC%2BD3sXntlektL0%3D (Pubitemid 37139833)
33. N Guttmann-Raviv N Shraga-Heled A Varshavsky C Guimaraes-Sternberg O Kessler G Neufeld 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 36 26294 26305 17569671 10.1074/jbc.M609711200 1:CAS:528: DC%2BD2sXpslGjtrk%3D (Pubitemid 47443814)
34. A Catalano P Caprari S Rodilossi P Betta M Castellucci A Casazza L Tamagnone A Procopio 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 2 358 360 14656993 1:CAS:528:DC%2BD2cXht1Gjt70%3D
35. Y Zhang MK Singh KR Degenhardt MM Lu J Bennett Y Yoshida JA Epstein 2009 Tie2Cre-mediated inactivation of plexinD1 results in congenital heart, vascular and skeletal defects Dev Biol 325 1 82 93 18992737 10.1016/j.ydbio.2008.09.031 1:CAS:528:DC%2BD1cXhsFCls7bF
36. F Guan G Villegas J Teichman P Mundel A Tufro 2006 Autocrine class III semaphorin system regulates slit diaphragm proteins and podocyte survival Kidney Int 69 9 1564 1569 16541019 10.1038/sj.ki.5000313 1:CAS:528: DC%2BD28XjvF2ks78%3D
37. T Bagci JK Wu R Pfannl LL Ilag DG Jay 2009 Autocrine semaphorin 3A signaling promotes glioblastoma dispersal Oncogene 28 40 3537 3550 19684614 10.1038/onc.2009.204 1:CAS:528:DC%2BD1MXpvFCrtbo%3D
38. H Pan LS Wanami TR Dissanayake RE Bachelder 2009 Autocrine semaphorin3A stimulates alpha2 beta1 integrin expression/function in breast tumor cells Breast Cancer Res Treat 118 1 197 205 18787945 10.1007/s10549-008-0179-y 1:CAS:528:DC%2BD1MXht1GmtbfK
39. G Serini D Valdembri S Zanivan G Morterra C Burkhardt F Caccavari L Zammataro L Primo L Tamagnone M Logan M Tessier-Lavigne M Taniguchi AW Püschel F Bussolino 2003 Class III semaphorins control vascular morphogenesis by inhibiting integrin function Nature 424 6947 391 397 12879061 10.1038/nature01784 1:CAS:528:DC%2BD3sXls1aqsb8%3D (Pubitemid 36917481)
40. YI Choi JS Duke-Cohan WB Ahmed MA Handley F Mann JA Epstein LK Clayton EL Reinherz 2008 PlexinD1 glycoprotein controls migration of positively selected thymocytes into the medulla Immunity 29 6 888 898 19027330 10.1016/j.immuni. 2008.10.008 1:CAS:528:DC%2BD1MXhtlymsA%3D%3D
41. C Christensen N Ambartsumian G Gilestro B Thomsen P Comoglio L Tamagnone P Guldberg E Lukanidin 2005 Proteolytic processing converts the repelling signal Sema3E into an inducer of invasive growth and lung metastasis Cancer Res 65 14 6167 6177 16024618 10.1158/0008-5472.CAN-04-4309 1:CAS:528:DC%2BD2MXmt1ehu7k%3D (Pubitemid 40994402)
42. O Behar JA Golden H Mashimo FJ Schoen MC Fishman 1996 Semaphorin III is needed for normal patterning and growth of nerves, bones and heart Nature 383 6600 525 528 8849723 10.1038/383525a0 1:CAS:528:DyaK28Xmt1Gku7g%3D (Pubitemid 26346178)
43. Y Zhang MK Singh KR Degenhardt MM Lu J Bennett Y Yoshida JA Epstein 2009 Tie2Cre-mediated inactivation of plexinD1 results in congenital heart, vascular and skeletal defects Dev Biol 325 1 82 93 18992737 10.1016/j.ydbio.2008.09.031 1:CAS:528:DC%2BD1cXhsFCls7bF
44. N Takegahara H Takamatsu T Toyofuku T Tsujimura T Okuno K Yukawa M Mizui M Yamamoto DV Prasad K Suzuki M Ishii K Terai M Moriya Y Nakatsuji S Sakoda S Sato S Akira K Takeda M Inui T Takai M Ikawa M Okabe A Kumanogoh H Kikutani 2006 PlexinA1 and its interaction with DAP12 in immune responses and bone homeostasis Nat Cell Biol 8 6 615 622 16715077 10.1038/ncb1416 1:CAS:528:DC%2BD28XltFWqs74%3D (Pubitemid 43827355)
45. L Feiner AM Koppel H Kobayashi JA Raper 1997 Secreted chick semaphorins bind recombinant neuropilin with similar affinities but bind different subsets of neurons in situ Neuron 19 3 539 545 9331347 10.1016/S0896-6273(00)80370-0 1:CAS:528:DyaK2sXmvVKls7c%3D (Pubitemid 27430743)
46. M Nakagawa T Kaneda T Arakawa S Morita T Sato T Yomada K Hanada 2000 Vascular endothelial growth factor (VEGF) directly enhances osteoclastic bone resoprtion and survival of mature osteoclasts FEBS Lett 473 2 161 164 10812066 10.1016/S0014-5793(00)01520-9 1:CAS:528:DC%2BD3cXjt1ejtLY%3D (Pubitemid 30254282)