Lrp5 and Lrp6 redundantly control skeletal development in the mouse embryo

Developmental Biology

Volumn 359, Issue 2, 2011, Pages 222-229

  Joeng, Kyu Sang ^a   Schumacher, Cassie A ^b   Zylstra Diegel, Cassandra R ^b   Long, Fanxin ^a   Williams, Bart O ^b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VAN ANDEL RESEARCH INSTITUTE   (United States)

Author keywords

Chondrocyte; Lrp5; Lrp6; Mouse; Osteoblast; Wnt; catenin; catenin

Indexed keywords

ALPHA CATENIN; BETA CATENIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; WNT PROTEIN;

ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE DELETION; GENE FREQUENCY; HOMOLOGOUS RECOMBINATION; MESENCHYME CELL; MORPHOLOGY; MOUSE; NONHUMAN; OSTEOBLAST; PERICHONDRIUM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

MUS;

EID: 82455186482     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.08.020     Document Type: Article

References (39)

1. Balemans W., Ebeling M., Patel N., Van Hul E., Olson P., Dioszegi M., Lacza C., Wuyts W., Van Den Ende J., Willems P., Paes-Alves A.F., Hill S., Bueno M., Ramos F.J., Tacconi P., Dikkers F.G., Stratakis C., Lindpaintner K., Vickery B., Foernzler D., Van Hul W. Increased bone density in sclerosteosis is due to the deficiency of a novel secreted protein (SOST). Hum. Mol. Genet. 2001, 10:537-543.
2. Balemans W., Patel N., Ebeling M., Van Hul E., Wuyts W., Lacza C., Dioszegi M., Dikkers F.G., Hildering P., Willems P.J., Verheij J.B., Lindpaintner K., Vickery B., Foernzler D., Van Hul W. Identification of a 52kb deletion downstream of the SOST gene in patients with van Buchem disease. J. Med. Genet. 2002, 39:91-97.
3. Bennett C.N., Longo K.A., Wright W.S., Suva L.J., Lane T.F., Hankenson K.D., MacDougald O.A. Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:3324-3329.
4. Boyden L.M., Mao J., Belsky J., Mitzner L., Farhi A., Mitnick M.A., Wu D., Insogna K., Lifton R.P. High bone density due to a mutation in LDL-receptor-related protein 5. N. Engl. J. Med. 2002, 346:1513-1521.
5. Brault V., Moore R., Kutsch S., Ishibashi M., Rowitch D.H., McMahon A.P., Sommer L., Boussadia O., Kemler R. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 2001, 128:1253-1264.
6. Brunkow M.E., Gardner J.C., Van Ness J., Paeper B.W., Kovacevich B.R., Proll S., Skonier J.E., Zhao L., Sabo P.J., Fu Y., Alisch R.S., Gillett L., Colbert T., Tacconi P., Galas D., Hamersma H., Beighton P., Mulligan J. Bone dysplasia sclerosteosis results from loss of the SOST gene product, a novel cystine knot-containing protein. Am. J. Hum. Genet. 2001, 68:577-589.
7. Chamorro M.N., Schwartz D.R., Vonica A., Brivanlou A.H., Cho K.R., Varmus H.E. FGF-20 and DKK1 are transcriptional targets of beta-catenin and FGF-20 is implicated in cancer and development. EMBO J. 2005, 24:73-84.
8. Collette N.M., Genetos D.C., Murugesh D., Harland R.M., Loots G.G. Genetic evidence that SOST inhibits WNT signaling in the limb. Dev. Biol. 2010, 342:169-179.
9. Cui Y., Niziolek P.J., Macdonald B.T., Zylstra C.R., Alenina N., Robinson D.R., Zhong Z., Matthes S., Jacobsen C.M., Conlon R.A., Brommage R., Liu Q., Mseeh F., Powell D.R., Yang Q.M., Zambrowicz B., Gerrits H., Gossen J.A., He X., Bader M., Williams B.O., Warman M.L., Robling A.G. Lrp5 functions in bone to regulate bone mass. Nat. med. 2011, 17:684-691.
10. Day T.F., Guo X., Garrett-Beal L., Yang Y. Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev. Cell 2005, 8:739-750.
11. Glass D.A., Bialek P., Ahn J.D., Starbuck M., Patel M.S., Clevers H., Taketo M.M., Long F., McMahon A.P., Lang R.A., Karsenty G. Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev. Cell 2005, 8:751-764.
12. Gong Y., Slee R.B., Fukai N., Rawadi G., Roman-Roman S., Reginato A.M., Wang H., Cundy T., Glorieux F.H., Lev D., Zacharin M., Oexle K., Marcelino J., Suwairi W., Heeger S., Sabatakos G., Apte S., Adkins W.N., Allgrove J., Arslan-Kirchner M., Batch J.A., Beighton P., Black G.C., Boles R.G., Boon L.M., Borrone C., Brunner H.G., Carle G.F., Dallapiccola B., De Paepe A., Floege B., Halfhide M.L., Hall B., Hennekam R.C., Hirose T., Jans A., Juppner H., Kim C.A., Keppler-Noreuil K., Kohlschuetter A., LaCombe D., Lambert M., Lemyre E., Letteboer T., Peltonen L., Ramesar R.S., Romanengo M., Somer H., Steichen-Gersdorf E., Steinmann B., Sullivan B., Superti-Furga A., Swoboda W., van den Boogaard M.J., Van Hul W., Vikkula M., Votruba M., Zabel B., Garcia T., Baron R., Olsen B.R., Warman M.L. LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 2001, 107:513-523.
13. Hill T.P., Spater D., Taketo M.M., Birchmeier W., Hartmann C. Canonical Wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev. Cell 2005, 8:727-738.
14. Hilton M.J., Tu X., Cook J., Hu H., Long F. Ihh controls cartilage development by antagonizing Gli3, but requires additional effectors to regulate osteoblast and vascular development. Development 2005, 132:4339-4351.
15. Holmen S.L., Giambernardi T.A., Zylstra C.R., Buckner-Berghuis B.D., Resau J.H., Hess J.F., Glatt V., Bouxsein M.L., Ai M., Warman M.L., Williams B.O. Decreased BMD and limb deformities in mice carrying mutations in both Lrp5 and Lrp6. J. bone miner. res.: off. j. Am. Soc. Bone Min. Res. 2004, 19:2033-2040.
16. Holmen S.L., Zylstra C.R., Mukherjee A., Sigler R.E., Faugere M.C., Bouxsein M.L., Deng L., Clemens T.L., Williams B.O. Essential role of beta-catenin in postnatal bone acquisition. J. Biol. Chem. 2005, 280:21162-21168.
17. Hu H., Hilton M.J., Tu X., Yu K., Ornitz D.M., Long F. Sequential roles of Hedgehog and Wnt signaling in osteoblast development. Development 2005, 132:49-60.
18. Huelsken J., Birchmeier W. New aspects of Wnt signaling pathways in higher vertebrates. Curr. Opin. Genet. Dev. 2001, 11:547-553.
19. Joeng K.S., Long F. The Gli2 transcriptional activator is a crucial effector for Ihh signaling in osteoblast development and cartilage vascularization. Development 2009, 136:4177-4185.
20. Kato M., Patel M.S., Levasseur R., Lobov I., Chang B.H., Glass D.A., Hartmann C., Li L., Hwang T.H., Brayton C.F., Lang R.A., Karsenty G., Chan L. Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J. Cell Biol. 2002, 157:303-314.
21. Li X., Ominsky M.S., Niu Q.T., Sun N., Daugherty B., D'Agostin D., Kurahara C., Gao Y., Cao J., Gong J., Asuncion F., Barrero M., Warmington K., Dwyer D., Stolina M., Morony S., Sarosi I., Kostenuik P.J., Lacey D.L., Simonet W.S., Ke H.Z., Paszty C. Targeted deletion of the sclerostin gene in mice results in increased bone formation and bone strength. J. Bone Min. Res.: Off. J. Am. Soc. Bone Miner. Res. 2008, 23:860-869.
22. Little R.D., Carulli J.P., Del Mastro R.G., Dupuis J., Osborne M., Folz C., Manning S.P., Swain P.M., Zhao S.C., Eustace B., Lappe M.M., Spitzer L., Zweier S., Braunschweiger K., Benchekroun Y., Hu X., Adair R., Chee L., FitzGerald M.G., Tulig C., Caruso A., Tzellas N., Bawa A., Franklin B., McGuire S., Nogues X., Gong G., Allen K.M., Anisowicz A., Morales A.J., Lomedico P.T., Recker S.M., Van Eerdewegh P., Recker R.R., Johnson M.L. A mutation in the LDL receptor-related protein 5 gene results in the autosomal dominant high-bone-mass trait. Am. J. Hum. Genet. 2002, 70:11-19.
23. Long F., Zhang X.M., Karp S., Yang Y., McMahon A.P. Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development 2001, 128:5099-5108.
24. Long F., Chung U.I., Ohba S., McMahon J., Kronenberg H.M., McMahon A.P. Ihh signaling is directly required for the osteoblast lineage in the endochondral skeleton. Development 2004, 131:1309-1318.
25. Mao J., Wang J., Liu B., Pan W., Farr G.H., Flynn C., Yuan H., Takada S., Kimelman D., Li L., Wu D. Low-density lipoprotein receptor-related protein-5 binds to Axin and regulates the canonical Wnt signaling pathway. Mol. Cell. 2001, 7:801-809.
26. McLeod M.J. Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology 1980, 22:299-301.
27. Niida A., Hiroko T., Kasai M., Furukawa Y., Nakamura Y., Suzuki Y., Sugano S., Akiyama T. DKK1, a negative regulator of Wnt signaling, is a target of the beta-catenin/TCF pathway. Oncogene 2004, 23:8520-8526.
28. Pinson K.I., Brennan J., Monkley S., Avery B.J., Skarnes W.C. An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 2000, 407:535-538.
29. Rodda S.J., McMahon A.P. Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 2006, 133:3231-3244.
30. Semenov M., Tamai K., He X. SOST is a ligand for LRP5/LRP6 and a Wnt signaling inhibitor. J. Biol. Chem. 2005, 280:26770-26775.
31. Swiatek P.J., Gridley T. Perinatal lethality and defects in hindbrain development in mice homozygous for a targeted mutation of the zinc finger gene Krox20. Genes dev. 1993, 7:2071-2084.
32. Tamai K., Semenov M., Kato Y., Spokony R., Liu C., Katsuyama Y., Hess F., Saint-Jeannet J.P., He X. LDL-receptor-related proteins in Wnt signal transduction. Nature 2000, 407:530-535.
33. Tu X., Joeng K.S., Nakayama K.I., Nakayama K., Rajagopal J., Carroll T.J., McMahon A.P., Long F. Noncanonical Wnt signaling through G protein-linked PKCdelta activation promotes bone formation. Dev. Cell 2007, 12:113-127.
34. Wehrli M., Dougan S.T., Caldwell K., O'Keefe L., Schwartz S., Vaizel-Ohayon D., Schejter E., Tomlinson A., DiNardo S. Arrow encodes an LDL-receptor-related protein essential for Wingless signalling. Nature 2000, 407:527-530.
35. Wodarz A., Nusse R. Mechanisms of Wnt signaling in development. Annu. Rev. Cell. Dev. Biol. 1998, 14:59-88.
36. Wu X., Tu X., Joeng K.S., Hilton M.J., Williams D.A., Long F. Rac1 activation controls nuclear localization of beta-catenin during canonical Wnt signaling. Cell 2008, 133:340-353.
37. Yadav V.K., Ryu J.H., Suda N., Tanaka K.F., Gingrich J.A., Schutz G., Glorieux F.H., Chiang C.Y., Zajac J.D., Insogna K.L., Mann J.J., Hen R., Ducy P., Karsenty G. Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum. Cell 2008, 135:825-837.
38. Yadav V.K., Arantes H.P., Barros E.R., Lazaretti-Castro M., Ducy P. Genetic analysis of Lrp5 function in osteoblast progenitors. Calcif. Tissue Int. 2010, 86:382-388.
39. Yu K., Xu J., Liu Z., Sosic D., Shao J., Olson E.N., Towler D.A., Ornitz D.M. Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 2003, 130:3063-3074.