Noncanonical Wnt Signaling through G Protein-Linked PKCδ Activation Promotes Bone Formation

Developmental Cell

Volumn 12, Issue 1, 2007, Pages 113-127

  Tu, Xiaolin ^a   Joeng, Kyu Sang ^a   Nakayama, Keiichi I ^b   Nakayama, Keiko ^c   Rajagopal, Jayaraj ^d   Carroll, Thomas J ^d,e   McMahon, Andrew P ^d   Long, Fanxin ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KYUSHU UNIVERSITY   (Japan)

^c TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d HARVARD UNIVERSITY   (United States)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

DEVBIO; SIGNALING

Indexed keywords

GROWTH FACTOR; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; PHOSPHATIDYLINOSITOL; PROTEIN KINASE C DELTA; UNCLASSIFIED DRUG; WNT PROTEIN; WNT3A PROTEIN; WNT7B PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; GENE EXPRESSION; HOMOZYGOSITY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MOUSE MUTANT; NEWBORN; NONHUMAN; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BETA CATENIN; BONE AND BONES; CELL DIFFERENTIATION; CULTURE MEDIA, CONDITIONED; EMBRYO; ENZYME ACTIVATION; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOPROTEINS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; OSTEOBLASTS; OSTEOGENESIS; PHOSPHATIDYLINOSITOLS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASE C-DELTA; PROTO-ONCOGENE PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION; WNT PROTEINS;

ANIMALIA; MAMMALIA; MURINAE; MUS;

EID: 33845802651     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2006.11.003     Document Type: Article

References (70)

1. Ahumada A., Slusarski D.C., Liu X., Moon R.T., Malbon C.C., and Wang H.Y. Signaling of rat Frizzled-2 through phosphodiesterase and cyclic GMP. Science 298 (2002) 2006-2010
2. Akhter S.A., Luttrell L.M., Rockman H.A., Iaccarino G., Lefkowitz R.J., and Koch W.J. Targeting the receptor-Gq interface to inhibit in vivo pressure overload myocardial hypertrophy. Science 280 (1998) 574-577
3. Arbuzova A., Schmitz A.A., and Vergeres G. Cross-talk unfolded: MARCKS proteins. Biochem. J. 362 (2002) 1-12
4. Bafico A., Liu G., Yaniv A., Gazit A., and Aaronson S.A. Novel mechanism of Wnt signalling inhibition mediated by Dickkopf-1 interaction with LRP6/Arrow. Nat. Cell Biol. 3 (2001) 683-686
5. Bennett C.N., Longo K.A., Wright W.S., Suva L.J., Lane T.F., Hankenson K.D., and MacDougald O.A. Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc. Natl. Acad. Sci. USA 102 (2005) 3324-3329
6. Blackshear P.J. The MARCKS family of cellular protein kinase C substrates. J. Biol. Chem. 268 (1993) 1501-1504
7. Bodine P.V., Zhao W., Kharode Y.P., Bex F.J., Lambert A.J., Goad M.B., Gaur T., Stein G.S., Lian J.B., and Komm B.S. The Wnt antagonist secreted frizzled-related protein-1 is a negative regulator of trabecular bone formation in adult mice. Mol. Endocrinol. 18 (2004) 1222-1237
8. Boyden L.M., Mao J., Belsky J., Mitzner L., Farhi A., Mitnick M.A., Wu D., Insogna K., and Lifton R.P. High bone density due to a mutation in LDL-receptor-related protein 5. N. Engl. J. Med. 346 (2002) 1513-1521
9. Cadigan K.M., and Nusse R. Wnt signaling: a common theme in animal development. Genes Dev. 11 (1997) 3286-3305
10. Chamorro M.N., Schwartz D.R., Vonica A., Brivanlou A.H., Cho K.R., and Varmus H.E. FGF-20 and DKK1 are transcriptional targets of β-catenin and FGF-20 is implicated in cancer and development. EMBO J. 24 (2005) 73-84
11. Chen A.E., Ginty D.D., and Fan C.M. Protein kinase A signalling via CREB controls myogenesis induced by Wnt proteins. Nature 433 (2005) 317-322
12. 2+ signaling pathway. Dev. Biol. 244 (2002) 342-357
13. Curtin J.A., Quint E., Tsipouri V., Arkell R.M., Cattanach B., Copp A.J., Henderson D.J., Spurr N., Stanier P., Fisher E.M., et al. Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr. Biol. 13 (2003) 1129-1133
14. Day T.F., Guo X., Garrett-Beal L., and Yang Y. Wnt/β-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev. Cell 8 (2005) 739-750
15. Glass II 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., and Karsenty G. Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev. Cell 8 (2005) 751-764
16. Glinka A., Wu W., Delius H., Monaghan A.P., Blumenstock C., and Niehrs C. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 391 (1998) 357-362
17. Gong Y., Slee R.B., Fukai N., Rawadi G., Roman-Roman S., Reginato A.M., Wang H., Cundy T., Glorieux F.H., Lev D., et al. LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 107 (2001) 513-523
18. Habas R., Kato Y., and He X. Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell 107 (2001) 843-854
19. Habas R., Dawid I.B., and He X. Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes Dev. 17 (2003) 295-309
20. He X., Saint-Jeannet J.P., Wang Y., Nathans J., Dawid I., and Varmus H. A member of the Frizzled protein family mediating axis induction by Wnt-5A. Science 275 (1997) 1652-1654
21. Heisenberg C.P., Tada M., Rauch G.J., Saude L., Concha M.L., Geisler R., Stemple D.L., Smith J.C., and Wilson S.W. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405 (2000) 76-81
22. Hill T.P., Spater D., Taketo M.M., Birchmeier W., and Hartmann C. Canonical Wnt/β-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev. Cell 8 (2005) 727-738
23. Hilton M.J., Tu X., Cook J., Hu H., and Long F. Ihh controls cartilage development by antagonizing Gli3, but requires additional effectors to regulate osteoblast and vascular development. Development 132 (2005) 4339-4351
24. Hu H., Hilton M.J., Tu X., Yu K., Ornitz D.M., and Long F. Sequential roles of Hedgehog and Wnt signaling in osteoblast development. Development 132 (2005) 49-60
25. Huelsken J., and Birchmeier W. New aspects of Wnt signaling pathways in higher vertebrates. Curr. Opin. Genet. Dev. 11 (2001) 547-553
26. Katagiri T., Yamaguchi A., Komaki M., Abe E., Takahashi N., Ikeda T., Rosen V., Wozney J.M., Fujisawa-Sehara A., and Suda T. Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J. Cell Biol. 127 (1994) 1755-1766
27. Katanaev V.L., Ponzielli R., Semeriva M., and Tomlinson A. Trimeric G protein-dependent frizzled signaling in Drosophila. Cell 120 (2005) 111-122
28. Kato M., Patel M.S., Levasseur R., Lobov I., Chang B.H., Glass II D.A., Hartmann C., Li L., Hwang T.H., Brayton C.F., et al. Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J. Cell Biol. 157 (2002) 303-314
29. Kibar Z., Vogan K.J., Groulx N., Justice M.J., Underhill D.A., and Gros P. Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nat. Genet. 28 (2001) 251-255
30. Kinoshita N., Iioka H., Miyakoshi A., and Ueno N. PKC δ is essential for Dishevelled function in a noncanonical Wnt pathway that regulates Xenopus convergent extension movements. Genes Dev. 17 (2003) 1663-1676
31. Koyanagi M., Haendeler J., Badorff C., Brandes R.P., Hoffmann J., Pandur P., Zeiher A.M., Kuhl M., and Dimmeler S. Non-canonical Wnt signaling enhances differentiation of human circulating progenitor cells to cardiomyogenic cells. J. Biol. Chem. 280 (2005) 16838-16842
32. 2+)/calmodulin-dependent protein kinase II is stimulated by Wnt and Frizzled homologs and promotes ventral cell fates in Xenopus. J. Biol. Chem. 275 (2000) 12701-12711
33. Lee P.N., Pang K., Matus D.Q., and Martindale M.Q. A WNT of things to come: evolution of Wnt signaling and polarity in cnidarians. Semin. Cell Dev. Biol. 17 (2006) 157-167
34. Leitges M., Mayr M., Braun U., Mayr U., Li C., Pfister G., Ghaffari-Tabrizi N., Baier G., Hu Y., and Xu Q. Exacerbated vein graft arteriosclerosis in protein kinase Cδ-null mice. J. Clin. Invest. 108 (2001) 1505-1512
35. 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., et al. A mutation in the LDL receptor-related protein 5 gene results in the autosomal dominant high-bone-mass trait. Am. J. Hum. Genet. 70 (2002) 11-19
36. Liu T., DeCostanzo A.J., Liu X., Wang H., Hallagan S., Moon R.T., and Malbon C.C. G protein signaling from activated rat frizzled-1 to the β-catenin-Lef-Tcf pathway. Science 292 (2001) 1718-1722
37. Liu X., Rubin J.S., and Kimmel A.R. Rapid, Wnt-induced changes in GSK3β associations that regulate β-catenin stabilization are mediated by Gα proteins. Curr. Biol. 15 (2005) 1989-1997
38. Lu W., Yamamoto V., Ortega B., and Baltimore D. Mammalian Ryk is a Wnt coreceptor required for stimulation of neurite outgrowth. Cell 119 (2004) 97-108
39. Mao B., Wu W., Li Y., Hoppe D., Stannek P., Glinka A., and Niehrs C. LDL-receptor-related protein 6 is a receptor for Dickkopf proteins. Nature 411 (2001) 321-325
40. Mao J., Wang J., Liu B., Pan W., Farr III G.H., Flynn C., Yuan H., Takada S., Kimelman D., Li L., and Wu D. Low-density lipoprotein receptor-related protein-5 binds to Axin and regulates the canonical Wnt signaling pathway. Mol. Cell 7 (2001) 801-809
41. Mikels A.J., and Nusse R. Purified Wnt5a protein activates or inhibits β-catenin-TCF signaling depending on receptor context. PLoS Biol. 4 (2006) e115
42. Miyamoto A., Nakayama K., Imaki H., Hirose S., Jiang Y., Abe M., Tsukiyama T., Nagahama H., Ohno S., Hatakeyama S., and Nakayama K.I. Increased proliferation of B cells and auto-immunity in mice lacking protein kinase Cδ. Nature 416 (2002) 865-869
43. Montcouquiol M., Rachel R.A., Lanford P.J., Copeland N.G., Jenkins N.A., and Kelley M.W. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423 (2003) 173-177
44. Morris A.J., and Malbon C.C. Physiological regulation of G protein-linked signaling. Physiol. Rev. 79 (1999) 1373-1430
45. Newton A.C. Regulation of protein kinase C. Curr. Opin. Cell Biol. 9 (1997) 161-167
46. Niida A., Hiroko T., Kasai M., Furukawa Y., Nakamura Y., Suzuki Y., Sugano S., and Akiyama T. DKK1, a negative regulator of Wnt signaling, is a target of the β-catenin/TCF pathway. Oncogene 23 (2004) 8520-8526
47. Offermanns S., Zhao L.P., Gohla A., Sarosi I., Simon M.I., and Wilkie T.M. Embryonic cardiomyocyte hypoplasia and craniofacial defects in G α q/G α 11-mutant mice. EMBO J. 17 (1998) 4304-4312
48. Ogawa M., Nishikawa S., Ikuta K., Yamamura F., Naito M., and Takahashi K. B cell ontogeny in murine embryo studied by a culture system with the monolayer of a stromal cell clone, ST2: B cell progenitor develops first in the embryonal body rather than in the yolk sac. EMBO J. 7 (1988) 1337-1343
49. Pandur P., Lasche M., Eisenberg L.M., and Kuhl M. Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis. Nature 418 (2002) 636-641
50. Parr B.A., Cornish V.A., Cybulsky M.I., and McMahon A.P. Wnt7b regulates placental development in mice. Dev. Biol. 237 (2001) 324-332
51. Penzo-Mendez A., Umbhauer M., Djiane A., Boucaut J.C., and Riou J.F. Activation of Gβγ signaling downstream of Wnt-11/Xfz7 regulates Cdc42 activity during Xenopus gastrulation. Dev. Biol. 257 (2003) 302-314
52. Pinson K.I., Brennan J., Monkley S., Avery B.J., and Skarnes W.C. An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 407 (2000) 535-538
53. Rodda S.J., and McMahon A.P. Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 133 (2006) 3231-3244
54. Schmitt A.M., Shi J., Wolf A.M., Lu C.C., King L.A., and Zou Y. Wnt-Ryk signalling mediates medial-lateral retinotectal topographic mapping. Nature 439 (2006) 31-37
55. Semenov M.V., Tamai K., Brott B.K., Kuhl M., Sokol S., and He X. Head inducer Dickkopf-1 is a ligand for Wnt coreceptor LRP6. Curr. Biol. 11 (2001) 951-961
56. Sheldahl L.C., Park M., Malbon C.C., and Moon R.T. Protein kinase C is differentially stimulated by Wnt and Frizzled homologs in a G-protein-dependent manner. Curr. Biol. 9 (1999) 695-698
57. 2+ flux, PKC, and CamKII in vertebrate embryos. J. Cell Biol. 161 (2003) 769-777
58. Slusarski D.C., Corces V.G., and Moon R.T. Interaction of Wnt and a Frizzled homologue triggers G-protein-linked phosphatidylinositol signalling. Nature 390 (1997) 410-413
59. Stumpo D.J., Bock C.B., Tuttle J.S., and Blackshear P.J. MARCKS deficiency in mice leads to abnormal brain development and perinatal death. Proc. Natl. Acad. Sci. USA 92 (1995) 944-948
60. Tada M., and Smith J.C. Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development 127 (2000) 2227-2238
61. Tamai K., Semenov M., Kato Y., Spokony R., Liu C., Katsuyama Y., Hess F., Saint-Jeannet J.P., and He X. LDL-receptor-related proteins in Wnt signal transduction. Nature 407 (2000) 530-535
62. Taylor S.M., and Jones P.A. Multiple new phenotypes induced in 10T1/2 and 3T3 cells treated with 5-azacytidine. Cell 17 (1979) 771-779
63. Tetsu O., and McCormick F. β-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398 (1999) 422-426
64. Veeman M.T., Axelrod J.D., and Moon R.T. A second canon. Functions and mechanisms of β-catenin-independent Wnt signaling. Dev. Cell 5 (2003) 367-377
65. Wallingford J.B., Rowning B.A., Vogeli K.M., Rothbacher U., Fraser S.E., and Harland R.M. Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405 (2000) 81-85
66. Wang J., Mark S., Zhang X., Qian D., Yoo S.J., Radde-Gallwitz K., Zhang Y., Lin X., Collazo A., Wynshaw-Boris A., and Chen P. Regulation of polarized extension and planar cell polarity in the cochlea by the vertebrate PCP pathway. Nat. Genet. 37 (2005) 980-985
67. Wang J., Hamblet N.S., Mark S., Dickinson M.E., Brinkman B.C., Segil N., Fraser S.E., Chen P., Wallingford J.B., and Wynshaw-Boris A. Dishevelled genes mediate a conserved mammalian PCP pathway to regulate convergent extension during neurulation. Development 133 (2006) 1767-1778
68. Wodarz A., and Nusse R. Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14 (1998) 59-88
69. Wu C., Zeng Q., Blumer K.J., and Muslin A.J. RGS proteins inhibit Xwnt-8 signaling in Xenopus embryonic development. Development 127 (2000) 2773-2784
70. Yu K., Xu J., Liu Z., Sosic D., Shao J., Olson E.N., Towler D.A., and 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 130 (2003) 3063-3074