Gpr177, a novel locus for bone mineral density and osteoporosis, regulates osteogenesis and chondrogenesis in skeletal development

Journal of Bone and Mineral Research

Volumn 28, Issue 5, 2013, Pages 1150-1159

  Maruyama, Takamitsu ^a   Jiang, Ming ^a   Hsu, Wei ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Bone; Cartilage; Craniofacial Development; GPR177; Mesenchyme; Wntless

Indexed keywords

G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 177; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DENSITY; BONE DEVELOPMENT; CARTILAGE CELL; CELL DIFFERENTIATION; CELL TYPE; CHONDROGENESIS; CONTROLLED STUDY; ENCHONDRAL OSSIFICATION; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOPOROSIS; SIGNAL TRANSDUCTION; SKELETON;

ANIMALS; BONE DENSITY; BONE DEVELOPMENT; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; OSTEOBLASTS; OSTEOPOROSIS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 84876713443     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.1830     Document Type: Article

References (50)

1. Manolagas SC., Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev. 2000; 21 (2): 115-37.
2. Ralston SH, de Crombrugghe B., Genetic regulation of bone mass and susceptibility to osteoporosis. Genes Dev. 2006; 20 (18): 2492-506.
3. Hsu YH, Zillikens MC, Wilson SG, Farber CR, Demissie S, Soranzo N, Bianchi EN, Grundberg E, Liang L, Richards JB, Estrada K, Zhou Y, van Nas A, Moffatt MF, Zhai G, Hofman A, van Meurs JB, Pols HA, Price RI, Nilsson O, Pastinen T, Cupples LA, Lusis AJ, Schadt EE, Ferrari S, Uitterlinden AG, Rivadeneira F, Spector TD, Karasik D, Kiel DP., An integration of genome-wide association study and gene expression profiling to prioritize the discovery of novel susceptibility Loci for osteoporosis-related traits. PLoS Genet. 2010; 6 (6): e1000977.
4. Richards JB, Rivadeneira F, Inouye M, Pastinen TM, Soranzo N, Wilson SG, Andrew T, Falchi M, Gwilliam R, Ahmadi KR, Valdes AM, Arp P, Whittaker P, Verlaan DJ, Jhamai M, Kumanduri V, Moorhouse M, van Meurs JB, Hofman A, Pols HA, Hart D, Zhai G, Kato BS, Mullin BH, Zhang F, Deloukas P, Uitterlinden AG, Spector TD., Bone mineral density, osteoporosis, and osteoporotic fractures: a genome-wide association study. Lancet. 2008; 371 (9623): 1505-2.
5. Rivadeneira F, Styrkarsdottir U, Estrada K, Halldorsson BV, Hsu YH, Richards JB, Zillikens MC, Kavvoura FK, Amin N, Aulchenko YS, Cupples LA, Deloukas P, Demissie S, Grundberg E, Hofman A, Kong A, Karasik D, van Meurs JB, Oostra B, Pastinen T, Pols HA, Sigurdsson G, Soranzo N, Thorleifsson G, Thorsteinsdottir U, Williams FM, Wilson SG, Zhou Y, Ralston SH, van Duijn CM, Spector T, Kiel DP, Stefansson K, Ioannidis JP, Uitterlinden AG., Twenty bone-mineral-density loci identified by large-scale meta-analysis of genome-wide association studies. Nat Genet. 2009; 41 (11): 1199-206.
6. Styrkarsdottir U, Halldorsson BV, Gretarsdottir S, Gudbjartsson DF, Walters GB, Ingvarsson T, Jonsdottir T, Saemundsdottir J, Center JR, Nguyen TV, Bagger Y, Gulcher JR, Eisman JA, Christiansen C, Sigurdsson G, Kong A, Thorsteinsdottir U, Stefansson K., Multiple genetic loci for bone mineral density and fractures. N Engl J Med. 2008; 358 (22): 2355-65.
7. Ferrari SL, Karasik D, Liu J, Karamohamed S, Herbert AG, Cupples LA, Kiel DP., Interactions of interleukin-6 promoter polymorphisms with dietary and lifestyle factors and their association with bone mass in men and women from the Framingham Osteoporosis Study. J Bone Miner Res. 2004; 19 (4): 552-9.
8. Cadigan KM, Peifer M., Wnt signaling from development to disease: insights from model systems. Cold Spring Harb Perspect Biol. 2009; 1 (2): a002881.
9. MacDonald BT, Tamai K, He X., Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell. 2009; 17 (1) 9-26.
10. Krishnan V, Bryant HU, Macdougald OA., Regulation of bone mass by Wnt signaling. J Clin Invest. 2006; 116 (5): 1202-9.
11. Hoeppner LH, Secreto FJ, Westendorf JJ., Wnt signaling as a therapeutic target for bone diseases. Expert Opin Ther Targets. 2009; 13 (4): 485-96.
12. Hartmann C, Wnt A., orchestrating canon osteoblastogenesis. Trends Cell Biol. 2006; 16 (3): 151-8.
13. Long F., Building strong bones: molecular regulation of the osteoblast lineage. Nat Rev Mol Cell Biol. 2012; 13 (1): 27-38.
14. Yu HM, Jerchow B, Sheu TJ, Liu B, Costantini F, Puzas JE, Birchmeier W, Hsu W., The role of Axin2 in calvarial morphogenesis and craniosynostosis. Development. 2005; 132 (8): 1995-2005.
15. Liu B, Yu HM, Hsu W., Craniosynostosis caused by Axin2 deficiency is mediated through distinct functions of beta-catenin in proliferation and differentiation. Dev Biol. 2007; 301 (1): 298-308.
16. Maruyama T, Mirando AJ, Deng CX, Hsu W., The balance of WNT and FGF signaling influences mesenchymal stem cell fate during skeletal development. Sci Signal. 2010; 3 (123): ra 40.
17. Mirando AJ, Maruyama T, Fu J, Yu HM, Hsu W., Beta-catenin/cyclin D1 mediated development of suture mesenchyme in calvarial morphogenesis. BMC Dev Biol. 2010; 10 (1): 116.
18. Baldridge D, Shchelochkov O, Kelley B, Lee B., Signaling pathways in human skeletal dysplasias. Annu Rev Genomics Hum Genet. 2010; 11: 189-217.
19. Gong Y, Slee RB, Fukai N, Rawadi G, Roman-Roman S, Reginato AM, Wang H, Cundy T, Glorieux FH, Lev D, Zacharin M, Oexle K, Marcelino J, Suwairi W, Heeger S, Sabatakos G, Apte S, Adkins WN, Allgrove J, Arslan-Kirchner M, Batch JA, Beighton P, Black GC, Boles RG, Boon LM, Borrone C, Brunner HG, Carle GF, Dallapiccola B, De Paepe A, Floege B, Halfhide ML, Hall B, Hennekam RC, Hirose T, Jans A, Juppner H, Kim CA, Keppler-Noreuil K, Kohlschuetter A, LaCombe D, Lambert M, Lemyre E, Letteboer T, Peltonen L, Ramesar RS, Romanengo M, Somer H, Steichen-Gersdorf E, Steinmann B, Sullivan B, Superti-Furga A, Swoboda W, van den Boogaard MJ, Van Hul W, Vikkula M, Votruba M, Zabel B, Garcia T, Baron R, Olsen BR, Warman ML., LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell. 2001; 107 (4): 513-23.
20. Boyden LM, Mao J, Belsky J, Mitzner L, Farhi A, Mitnick MA, Wu D, Insogna K, Lifton RP., High bone density due to a mutation in LDL-receptor-related protein 5. N Engl J Med. 2002; 346 (20): 1513-21.
21. Kato M, Patel MS, Levasseur R, Lobov I, Chang BH, Glass DA 2nd, Hartmann C, Li L, Hwang TH, Brayton CF, Lang RA, 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 (2): 303-14.
22. Fu J, Jiang M, Mirando AJ, Yu HM, Hsu W., Reciprocal regulation of Wnt Gpr177/mouse Wntless is required for embryonic axis formation. Proc Natl Acad Sci U.S.A., 2009; 106 (44): 18598-603.
23. Banziger C, Soldini D, Schutt C, Zipperlen P, Hausmann G, Basler K., Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell. 2006; 125 (3): 509-22.
24. Bartscherer K, Pelte N, Ingelfinger D, Boutros M., Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell. 2006; 125 (3): 523-33.
25. Yu HM, Jin Y, Fu J, Hsu W., Expression of Gpr177, a Wnt trafficking regulator, in mouse embryogenesis. Dev Dyn. 2010; 239 (7): 2102-9.
26. Fu J, Ivy Yu HM, Maruyama T, Mirando AJ, Hsu W., Gpr177/mouse Wntless is essential for Wnt-mediated craniofacial and brain development. Dev Dyn. 2011; 240 (2): 365-71.
27. Liu F, Woitge HW, Braut A, Kronenberg MS, Lichtler AC, Mina M, Kream BE., Expression and activity of osteoblast-targeted Cre recombinase transgenes in murine skeletal tissues. Int J Dev Biol. 2004; 48 (7): 645-53.
28. Ovchinnikov DA, Deng JM, Ogunrinu G, Behringer RR., Col2a1-directed expression of Cre recombinase in differentiating chondrocytes in transgenic mice. Genesis. 2000; 26 (2): 145-6.
29. Rodda SJ, McMahon AP., Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development. 2006; 133 (16): 3231-44.
30. Yu K, Xu J, Liu Z, Sosic D, Shao J, Olson EN, Towler DA, Ornitz DM., 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 (13): 3063-74.
31. Chiu SY, Asai N, Costantini F, Hsu W., SUMO-specific protease 2 is essential for modulating p53-Mdm2 in development of trophoblast stem cell niches and lineages. PLoS Biol. 2008; 6 (12): e310.
32. Hsu W, Mirando AJ., Yu HM. Manipulating gene activity in Wnt1-expressing precursors of neural epithelial and neural crest cells. Dev Dyn. 2010; 239 (1): 338-45.
33. Yu HM, Liu B, Chiu SY, Costantini F, Hsu W., Development of a unique system for spatiotemporal lineage-specific gene expression in mice. Proc Natl Acad Sci U.S.A., 2005; 102 (24): 8615-20.
34. Liu B, Yu HM, Huang J, Hsu W., Co-opted JNK/SAPK signaling in Wnt/beta-catenin-induced tumorigenesis. Neoplasia. 2008; 10 (9): 1004-13.
35. Jiang M, Chiu SY, Hsu W., SUMO-specific protease 2 in Mdm2-mediated regulation of p53. Cell Death Differ. 2011; 18 (6): 1005-15.
36. Provot S, Zinyk D, Gunes Y, Kathri R, Le Q, Kronenberg HM, Johnson RS, Longaker MT, Giaccia AJ, Schipani E., Hif-1alpha regulates differentiation of limb bud mesenchyme and joint development. J Cell Biol. 2007; 177 (3): 451-64.
37. Shimada M, Greer PA, McMahon AP, Bouxsein ML, Schipani E., In vivo targeted deletion of calpain small subunit, Capn4, in cells of the osteoblast lineage impairs cell proliferation, differentiation, and bone formation. J Biol Chem. 2008; 283 (30): 21002-10.
38. Hu H, Hilton MJ, Tu X, Yu K, Ornitz DM, Long F., Sequential roles of Hedgehog and Wnt signaling in osteoblast development. Development. 2005; 132 (1): 49-60.
39. Tran TH, Jarrell A, Zentner GE, Welsh A, Brownell I, Scacheri PC, Atit R., Role of canonical Wnt signaling/ss-catenin via Dermo1 in cranial dermal cell development. Development. 2010; 137 (23): 3973-84.
40. Day TF, 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 (5): 739-50.
41. Rice DP., Developmental anatomy of craniofacial sutures. Front Oral Biol. 2008; 12: 1-21.
42. Opperman LA., Cranial sutures as intramembranous bone growth sites. Dev Dyn. 2000; 219 (4): 472-85.
43. Sasaki T, Ito Y, Bringas P Jr, Chou S, Urata MM, Slavkin H, Chai Y., TGFbeta-mediated FGF signaling is crucial for regulating cranial neural crest cell proliferation during frontal bone development. Development. 2006; 133 (2): 371-81.
44. Hill TP, Spater D, Taketo MM, Birchmeier W, Hartmann C., Canonical Wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev Cell. 2005; 8 (5): 727-38.
45. Stickens D, Behonick DJ, Ortega N, Heyer B, Hartenstein B, Yu Y, Fosang AJ, Schorpp-Kistner M, Angel P, Werb Z., Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development. 2004; 131 (23): 5883-95.
46. Vu TH, Shipley JM, Bergers G, Berger JE, Helms JA, Hanahan D, Shapiro SD, Senior RM, Werb Z., MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell. 1998; 93 (3): 411-22.
47. Akiyama H, Lyons JP, Mori-Akiyama Y, Yang X, Zhang R, Zhang Z, Deng JM, Taketo MM, Nakamura T, Behringer RR, McCrea PD, de Crombrugghe B., Interactions between Sox9 and beta-catenin control chondrocyte differentiation. Genes Dev. 2004; 18 (9): 1072-87.
48. Heuberger J, Birchmeier W., Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb Perspect Biol. 2010; 2 (2): a002915.
49. Valenta T, Gay M, Steiner S, Draganova K, Zemke M, Hoffmans R, Cinelli P, Aguet M, Sommer L, Basler K., Probing transcription-specific outputs of beta-catenin in vivo. Genes Dev. 2011; 25 (24): 2631-43.
50. Yang Y, Topol L, Lee H., Wu J. Wnt5a and Wnt5b exhibit distinct activities in coordinating chondrocyte proliferation and differentiation. Development. 2003; 130 (5): 1003-15.