Endostatin affects osteoblast behavior in vitro, but collagen XVIII/endostatin is not essential for skeletal development in vivo

Calcified Tissue International

Volumn 85, Issue 5, 2009, Pages 412-420

  Sipola, Annina ^a   Seppinen, Lotta ^a   Pihlajaniemi, Taina ^a   Tuukkanen, Juha ^a  

^a UNIVERSITY OF OULU   (Finland)

Author keywords

Collagen XVIII; Endostatin; Ossification; Osteoblast; VEGF A

Indexed keywords

COLLAGEN 18; COLLAGEN DERIVATIVE; ENDOSTATIN; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; BONE DENSITY; BONE DEVELOPMENT; BONE GROWTH; BONE MARROW; BONE MINERAL; BONE MINERALIZATION; CELL PROLIFERATION; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; HINDLIMB; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; PERIOSTEUM; PRIORITY JOURNAL; PROTEIN FUNCTION; X RAY ANALYSIS;

ANGIOGENESIS INHIBITORS; ANIMALS; BASEMENT MEMBRANE; BONE AND BONES; BONE DENSITY; BONE DEVELOPMENT; CELL LINE; CELL PROLIFERATION; ENDOSTATINS; EXTRACELLULAR MATRIX; MICE; MICE, KNOCKOUT; MINERALS; OSTEOBLASTS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 70449526210     PISSN: 0171967X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00223-009-9287-x     Document Type: Article

References (38)

1. I Celik O Surucu C Dietz JV Heymach J Force I Hoschele CM Becker J Folkman O Kisker 2005 Therapeutic efficacy of endostatin exhibits a biphasic dose-response curve Cancer Res 65 11044 11050 10.1158/0008-5472.CAN-05-2617 1:CAS:528:DC%2BD2MXht1Kjsr3K 16322254 (Pubitemid 41713375)
2. M Dhanabal R Ramchandran MJ Waterman H Lu B Knebelmann M Segal VP Sukhatme 1999 Endostatin induces endothelial cell apoptosis J Biol Chem 274 11721 11726 10.1074/jbc.274.17.11721 1:CAS:528:DyaK1MXislGlsrk%3D 10206987 (Pubitemid 29197835)
3. H Elamaa R Sormunen M Rehn R Soininen T Pihlajaniemi 2005 Endostatin overexpression specifically in the lens and skin leads to cataract and ultrastructural alterations in basement membranes Am J Pathol 166 221 229 1:CAS:528:DC%2BD2MXnt1eqtg%3D%3D 15632014
4. N Fukai L Eklund AG Marneros SP Oh DR Keene L Tamarkin M Niemela M Ilves E Li T Pihlajaniemi BR Olsen 2002 Lack of collagen XVIII/endostatin results in eye abnormalities EMBO J 21 1535 1544 10.1093/emboj/21.7.1535 1:CAS:528:DC%2BD38XjtVOgtr8%3D 11927538 (Pubitemid 34614610)
5. HP Gerber TH Vu AM Ryan J Kowalski Z Werb N Ferrara 1999 VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation Nat Med 5 623 628 10.1038/9467 1:CAS:528: DyaK1MXjs1Kmtrc%3D 10371499 (Pubitemid 29289424)
6. D Guo Q Jia HY Song RS Warren DB Donner 1995 Vascular endothelial cell growth factor promotes tyrosine phosphorylation of mediators of signal transduction that contain SH2 domains. Association with endothelial cell proliferation J Biol Chem 270 6729 6733 10.1074/jbc.270.12.6729 1:CAS:528:DyaK2MXks1yisb4%3D 7896817
7. J Hanai J Gloy SA Karumanchi S Kale J Tang G Hu B Chan R Ramchandran V Jha VP Sukhatme S Sokol 2002 Endostatin is a potential inhibitor of Wnt signaling J Cell Biol 158 529 539 10.1083/jcb.200203064 1:CAS:528: DC%2BD38XmtVeksL4%3D 12147676 (Pubitemid 34851711)
8. MO Hiltunen M Ruuskanen J Huuskonen AJ Mahonen M Ahonen J Rutanen VM Kosma A Mahonen H Kroger S Yla-Herttuala 2003 Adenovirus-mediated VEGF-A gene transfer induces bone formation in vivo FASEB J 17 1147 1149 1:CAS:528:DC%2BD3sXktl2jsrY%3D 12692089
9. M Hurskainen L Eklund PO Hagg M Fruttiger R Sormunen M Ilves T Pihlajaniemi 2005 Abnormal maturation of the retinal vasculature in type XVIII collagen/endostatin deficient mice and changes in retinal glial cells due to lack of collagen types XV and XVIII FASEB J 19 1564 1566 1:CAS:528: DC%2BD2MXpvF2gtbc%3D 15976268
10. YM Kim S Hwang YM Kim BJ Pyun TY Kim ST Lee YS Gho YG Kwon 2002 Endostatin blocks vascular endothelial growth factor-mediated signaling via direct interaction with KDR/Flk-1 J Biol Chem 277 27872 27879 10.1074/jbc.M202771200 1:CAS:528:DC%2BD38XlvFKgt74%3D 12029087 (Pubitemid 34966733)
11. Y Kitagawa J Dai J Zhang JM Keller J Nor Z Yao ET Keller 2005 Vascular endothelial growth factor contributes to prostate cancer-mediated osteoblastic activity Cancer Res 65 10921 10929 10.1158/0008-5472.CAN-05-1809 1:CAS:528:DC%2BD2MXht1KjsrzM 16322239 (Pubitemid 41713360)
12. T Kojima DT Azar JH Chang 2008 Neostatin-7 regulates bFGF-induced corneal lymphangiogenesis FEBS Lett 582 2515 2520 10.1016/j.febslet.2008.06.014 1:CAS:528:DC%2BD1cXosVOlsr4%3D 18570894
13. CJ Kuo KR LaMontagne Jr G Garcia-Cardena BD Ackley D Kalman S Park R Christofferson J Kamihara YH Ding KM Lo S Gillies J Folkman RC Mulligan K Javaherian 2001 Oligomerization-dependent regulation of motility and morphogenesis by the collagen XVIII NC1/endostatin domain J Cell Biol 152 1233 1246 10.1083/jcb.152.6.1233 1:CAS:528:DC%2BD3MXit1egt7o%3D 11257123 (Pubitemid 34280180)
14. KH Lau S Kapur C Kesavan DJ Baylink 2006 Up-regulation of the Wnt, estrogen receptor, insulin-like growth factor-I, and bone morphogenetic protein pathways in C57BL/6J osteoblasts as opposed to C3H/HeJ osteoblasts in part contributes to the differential anabolic response to fluid shear J Biol Chem 281 9576 9588 10.1074/jbc.M509205200 1:CAS:528:DC%2BD28XjtVSqsro%3D 16461770 (Pubitemid 43864676)
15. HJ Leis W Hulla R Gruber E Huber D Zach H Gleispach W Windischhofer 1997 Phenotypic heterogeneity of osteoblast-like MC3T3-E1 cells: changes of bradykinin-induced prostaglandin E2 production during osteoblast maturation J Bone Miner Res 12 541 551 10.1359/jbmr.1997.12.4.541 1:CAS:528: DyaK2sXivFens78%3D 9101365 (Pubitemid 27155213)
16. CE Macsai BK Foster CJ Xian 2008 Roles of Wnt signalling in bone growth, remodelling, skeletal disorders and fracture repair J Cell Physiol 215 578 587 10.1002/jcp.21342 1:CAS:528:DC%2BD1cXlvVKgt70%3D 18247365 (Pubitemid 351632678)
17. T Maeda T Kawane N Horiuchi 2003 Statins augment vascular endothelial growth factor expression in osteoblastic cells via inhibition of protein prenylation Endocrinology 144 681 692 10.1210/en.2002-220682 1:CAS:528:DC%2BD3sXhtVWltLY%3D 12538631 (Pubitemid 36205242)
18. C Maes P Carmeliet K Moermans I Stockmans N Smets D Collen R Bouillon G Carmeliet 2002 Impaired angiogenesis and endochondral bone formation in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188 Mech Dev 111 61 73 10.1016/S0925-4773(01)00601-3 1:CAS:528:DC%2BD38XmsFKltw%3D%3D 11804779 (Pubitemid 34136979)
19. C Maes I Stockmans K Moermans LR Van N Smets P Carmeliet R Bouillon G Carmeliet 2004 Soluble VEGF isoforms are essential for establishing epiphyseal vascularization and regulating chondrocyte development and survival J Clin Invest 113 188 199 1:CAS:528:DC%2BD2cXmsVyrtg%3D%3D 14722611
20. V Midy J Plouet 1994 Vasculotropin/vascular endothelial growth factor induces differentiation in cultured osteoblasts Biochem Biophys Res Commun 199 380 386 10.1006/bbrc.1994.1240 1:CAS:528:DyaK2cXhvVeqt7s%3D 8123039 (Pubitemid 24179960)
21. Y Muragaki S Timmons CM Griffith SP Oh B Fadel T Quertermous BR Olsen 1995 Mouse Col18a1 is expressed in a tissue-specific manner as three alternative variants and is localized in basement membrane zones Proc Natl Acad Sci USA 92 8763 8767 10.1073/pnas.92.19.8763 1:CAS:528:DyaK2MXotVGqs70%3D 7568013
22. MS O'Reilly T Boehm Y Shing N Fukai G Vasios WS Lane E Flynn JR Birkhead BR Olsen J Folkman 1997 Endostatin: an endogenous inhibitor of angiogenesis and tumor growth Cell 88 277 285 10.1016/S0092-8674(00)81848-6 9008168 (Pubitemid 28015876)
23. AK Olsson A Dimberg J Kreuger L Claesson-Welsh 2006 VEGF receptor signalling - in control of vascular function Nat Rev Mol Cell Biol 7 359 371 10.1038/nrm1911 1:CAS:528:DC%2BD28XjslSktrc%3D 16633338
24. M Orlandini A Spreafico M Bardelli M Rocchigiani A Salameh S Nucciotti C Capperucci B Frediani S Oliviero 2006 Vascular endothelial growth factor-D activates VEGFR-3 expressed in osteoblasts inducing their differentiation J Biol Chem 281 17961 17967 10.1074/jbc.M600413200 1:CAS:528:DC%2BD28XmtFykt7g%3D 16624815 (Pubitemid 44035595)
25. T Pufe WJ Petersen N Miosge MB Goldring R Mentlein DJ Varoga BN Tillmann 2004 Endostatin/collagen XVIII-an inhibitor of angiogenesis-is expressed in cartilage and fibrocartilage Matrix Biol 23 267 276 10.1016/j.matbio.2004.06.003 1:CAS:528:DC%2BD2cXotFCrt70%3D 15464359 (Pubitemid 39298976)
26. D Quelard E Lavergne I Hendaoui H Elamaa U Tiirola R Heljasvaara T Pihlajaniemi B Clement O Musso 2008 A cryptic frizzled module in cell surface collagen 18 inhibits Wnt/beta-catenin signaling PLoS ONE 3 e1878 10.1371/journal.pone.0001878 18382662 (Pubitemid 351943828)
27. TP Quinn KG Peters VC De N Ferrara LT Williams 1993 Fetal liver kinase 1 is a receptor for vascular endothelial growth factor and is selectively expressed in vascular endothelium Proc Natl Acad Sci USA 90 7533 7537 10.1073/pnas.90.16.7533 1:CAS:528:DyaK3sXmsVWqsLY%3D 8356051
28. M Rehn T Pihlajaniemi 1995 Identification of three N-terminal ends of type XVIII collagen chains and tissue-specific differences in the expression of the corresponding transcripts. The longest form contains a novel motif homologous to rat and Drosophila frizzled proteins J Biol Chem 270 4705 4711 10.1074/jbc.270.9.4705 1:CAS:528:DyaK2MXktFShsLY%3D 7876242
29. M Rehn T Veikkola E Kukk-Valdre H Nakamura M Ilmonen C Lombardo T Pihlajaniemi K Alitalo K Vuori 2001 Interaction of endostatin with integrins implicated in angiogenesis Proc Natl Acad Sci USA 98 1024 1029 10.1073/pnas.031564998 1:CAS:528:DC%2BD3MXht1SmsL0%3D 11158588 (Pubitemid 32121180)
30. J Saarela R Ylikarppa M Rehn S Purmonen T Pihlajaniemi 1998 Complete primary structure of two variant forms of human type XVIII collagen and tissue-specific differences in the expression of the corresponding transcripts Matrix Biol 16 319 328 10.1016/S0945-053X(98)90003-8 1:CAS:528: DyaK1cXpsF2ntA%3D%3D 9503365 (Pubitemid 28052585)
31. A Schmidt D Wenzel I Thorey T Sasaki J Hescheler R Timpl K Addicks S Werner BK Fleischmann W Bloch 2006 Endostatin influences endothelial morphology via the activated ERK1/2-kinase endothelial morphology and signal transduction Microvasc Res 71 152 162 10.1016/j.mvr.2006.01.001 1:CAS:528: DC%2BD28XltlKrt7w%3D 16650878 (Pubitemid 43810120)
32. A Sipola J Ilvesaro E Birr P Jalovaara RF Pettersson F Stenback S Yla-Herttuala T Hautala J Tuukkanen 2007 Endostatin inhibits endochondral ossification J Gene Med 9 1057 1064 10.1002/jgm.1116 1:STN:280: DC%2BD2sjitVOkug%3D%3D 18001000 (Pubitemid 350286410)
33. A Sipola K Nelo T Hautala J Ilvesaro J Tuukkanen 2006 Endostatin inhibits VEGF-A induced osteoclastic bone resorption in vitro BMC Musculoskel Disord 7 56 10.1186/1471-2474-7-56 (Pubitemid 44200611)
34. J Street M Bao L deGuzman S Bunting FV, Peale Jr N Ferrara H Steinmetz J Hoeffel JL Cleland A Daugherty BN van HP Redmond RA Carano EH Filvaroff 2002 Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover Proc Natl Acad Sci USA 99 9656 9661 10.1073/pnas.152324099 1:CAS:528:DC%2BD38XlslKhu74%3D 12118119 (Pubitemid 34831103)
35. Y Tamamura T Otani N Kanatani E Koyama J Kitagaki T Komori Y Yamada F Costantini S Wakisaka M Pacifici M Iwamoto M Enomoto-Iwamoto 2005 Developmental regulation of Wnt/beta-catenin signals is required for growth plate assembly, cartilage integrity, and endochondral ossification J Biol Chem 280 19185 19195 10.1074/jbc.M414275200 1:CAS:528:DC%2BD2MXjvFers7Y%3D 15760903 (Pubitemid 41379625)
36. S Uchida A Sakai H Kudo H Otomo M Watanuki M Tanaka M Nagashima T Nakamura 2003 Vascular endothelial growth factor is expressed along with its receptors during the healing process of bone and bone marrow after drill-hole injury in rats Bone 32 491 501 10.1016/S8756-3282(03)00053-X 1:CAS:528:DC%2BD3sXltFCqurc%3D 12753865 (Pubitemid 39665708)
37. D Wang K Christensen K Chawla G Xiao PH Krebsbach RT Franceschi 1999 Isolation and characterization of MC3T3-E1 preosteoblast subclones with distinct in vitro and in vivo differentiation/mineralization potential J Bone Miner Res 14 893 903 10.1359/jbmr.1999.14.6.893 1:CAS:528:DyaK1MXjvFKqtb0%3D 10352097 (Pubitemid 29262883)
38. SA Wickstrom K Alitalo J Keski-Oja 2002 Endostatin associates with integrin alpha5beta1 and caveolin-1, and activates Src via a tyrosyl phosphatase-dependent pathway in human endothelial cells Cancer Res 62 5580 5589 1:CAS:528:DC%2BD38Xnsl2lsbs%3D 12359771