Wnt/β-catenin signaling is differentially regulated by Gα proteins and contributes to fibrous dysplasia

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 50, 2011, Pages 20101-20106

  Regard, Jean B ^a   Cherman, Natasha ^b   Palmer, Daniel ^c   Kuznetsov, Sergei A ^b   Celi, Francesco S ^d   Guettier, Jean Marc ^d   Chen, Min ^d   Bhattacharyya, Nisan ^b   Wess, Jurgen ^d   Coughlin, Shaun R ^c   Weinstein, Lee S ^d   Collins, Michael T ^b   Robey, Pamela G ^b   Yang, Yingzi ^a  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AXIN; BETA CATENIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; WNT PROTEIN;

ALBRIGHT SYNDROME; ARTICLE; FIBROUS DYSPLASIA; HUMAN; HUMAN CELL; HUMAN TISSUE; OSSIFICATION; OSTEOBLAST; PHENOTYPE; PRIORITY JOURNAL;

ADULT; ANIMALS; BETA CATENIN; BONE MARROW CELLS; FIBROUS DYSPLASIA OF BONE; FIBROUS DYSPLASIA, POLYOSTOTIC; GTP-BINDING PROTEIN ALPHA SUBUNITS; HUMANS; MICE; OSTEOBLASTS; PHENOTYPE; STEM CELLS; STROMAL CELLS; UP-REGULATION; WNT SIGNALING PATHWAY;

EID: 84055181339     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1114656108     Document Type: Article

References (60)

1. Weinstein LS, et al. (1991) Activating mutations of the stimulatory G protein in the McCune-Albright syndrome. N Engl J Med 325:1688-1695.
2. Riminucci M, Robey PG, Saggio I, Bianco P (2010) Skeletal progenitors and the GNAS gene: Fibrous dysplasia of bone read through stem cells. J Mol Endocrinol 45:355-364.
3. Marie PJ, de Pollak C, Chanson P, Lomri A (1997) Increased proliferation of osteoblastic cells expressing the activating Gs alpha mutation in monostotic and polyostotic fibrous dysplasia. Am J Pathol 150:1059-1069.
4. Gong Y, et al.; Osteoporosis-Pseudoglioma Syndrome Collaborative Group (2001) LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 107: 513-523.
5. Little RD, et al. (2002) A mutation in the LDL receptor-related protein 5 gene results in the autosomal dominant high-bone-mass trait. Am J Hum Genet 70(1):11-19.
6. Diarra D, et al. (2007) Dickkopf-1 is a master regulator of joint remodeling. Nat Med 13(2):156-163.
7. Loughlin J, et al. (2004) Functional variants within the secreted frizzled-related protein 3 gene are associated with hip osteoarthritis in females. Proc Natl Acad Sci USA 101:9757-9762.
8. Day TF, Guo X, Garrett-Beal L, Yang Y (2005) Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev Cell 8:739-750.
9. Hill TP, Später D, Taketo MM, Birchmeier W, Hartmann C (2005) Canonical Wnt/betacatenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev Cell 8:727-738.
10. Rodda SJ, McMahon AP (2006) Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 133:3231-3244.
11. Hu H, et al. (2005) Sequential roles of Hedgehog and Wnt signaling in osteoblast development. Development 132:49-60.
12. de Boer J, et al. (2004) Wnt signaling inhibits osteogenic differentiation of human mesenchymal stem cells. Bone 34:818-826.
13. Cho HH, et al. (2006) Endogenous Wnt signaling promotes proliferation and suppresses osteogenic differentiation in human adipose derived stromal cells. Tissue Eng 12(1):111-121.
14. Boland GM, Perkins G, Hall DJ, Tuan RS (2004) Wnt 3a promotes proliferation and suppresses osteogenic differentiation of adult human mesenchymal stem cells. J Cell Biochem 93:1210-1230.
15. Kahler RA, et al. (2006) Lymphocyte enhancer-binding factor 1 (Lef1) inhibits terminal differentiation of osteoblasts. J Cell Biochem 97:969-983.
16. Eijken M, et al. (2008) Wnt signaling acts and is regulated in a human osteoblast differentiation dependent manner. J Cell Biochem 104:568-579.
17. Foord SM, et al. (2005) International Union of Pharmacology. XLVI. G protein-coupled receptor list. Pharmacol Rev 57:279-288.
18. Liu T, et al. (2001) G protein signaling from activated rat frizzled-1 to the beta-catenin- Lef-Tcf pathway. Science 292:1718-1722.
19. Liu X, et al. (1999) Activation of a frizzled-2/beta-adrenergic receptor chimera promotes Wnt signaling and differentiation of mouse F9 teratocarcinoma cells via Galphao and Galphat. Proc Natl Acad Sci USA 96:14383-14388.
20. Liu X, Rubin JS, Kimmel AR (2005) Rapid, Wnt-induced changes in GSK3beta associations that regulate beta-catenin stabilization are mediated by Galpha proteins. Curr Biol 15:1989-1997.
21. Katanaev VL, Ponzielli R, Sémériva M, Tomlinson A (2005) Trimeric G protein-dependent frizzled signaling in Drosophila. Cell 120:111-122.
22. Major MB, et al. (2008) New regulators of Wnt/beta-catenin signaling revealed by integrative molecular screening. Sci Signal 1(45):ra12.
23. DasGupta R, Kaykas A, Moon RT, Perrimon N (2005) Functional genomic analysis of the Wnt-wingless signaling pathway. Science 308:826-833.
24. Castellone MD, Teramoto H, Williams BO, Druey KM, Gutkind JS (2005) Prostaglandin E2 promotes colon cancer cell growth through a Gs-axin-beta-catenin signaling axis. Science 310:1504-1510.
25. Kulkarni NH, et al. (2005) Effects of parathyroid hormone on Wnt signaling pathway in bone. J Cell Biochem 95:1178-1190.
26. Hino S, Tanji C, Nakayama KI, Kikuchi A (2005) Phosphorylation of beta-catenin by cyclic AMP-dependent protein kinase stabilizes beta-catenin through inhibition of its ubiquitination. Mol Cell Biol 25:9063-9072.
27. Collins MT, et al. (2003) Thyroid carcinoma in the McCune-Albright syndrome: Contributory role of activating Gs alpha mutations. J Clin Endocrinol Metab 88: 4413-4417.
28. Kaykas A, et al. (2004) Mutant Frizzled 4 associated with vitreoretinopathy traps wildtype Frizzled in the endoplasmic reticulum by oligomerization. Nat Cell Biol 6(1): 52-58.
29. Chen M, et al. (2005) Increased glucose tolerance and reduced adiposity in the absence of fasting hypoglycemia in mice with liver-specific Gs alpha deficiency. J Clin Invest 115:3217-3227.
30. Logan M, et al. (2002) Expression of Cre Recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 33(2):77-80.
31. DasGupta R, Fuchs E (1999) Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126: 4557-4568.
32. Harada N, et al. (1999) Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J 18:5931-5942.
33. Glass DA, 2nd, et al. (2005) Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev Cell 8:751-764.
34. Piersanti S, et al. (2010) Transfer, analysis, and reversion of the fibrous dysplasia cellular phenotype in human skeletal progenitors. J Bone Miner Res 25:1103-1116.
35. Fu Q, Jilka RL, Manolagas SC, O'Brien CA (2002) Parathyroid hormone stimulates receptor activator of NFkappa B ligand and inhibits osteoprotegerin expression via protein kinase A activation of cAMP-response element-binding protein. J Biol Chem 277:48868-48875.
36. Holmen SL, et al. (2005) Essential role of beta-catenin in postnatal bone acquisition. J Biol Chem 280:21162-21168.
37. Wedegaertner PB, Bourne HR, von Zastrow M (1996) Activation-induced subcellular redistribution of Gs alpha. Mol Biol Cell 7:1225-1233.
38. Bhattacharyya R, Wedegaertner PB (2000) Galpha 13 requires palmitoylation for plasma membrane localization, Rho-dependent signaling, and promotion of p115-RhoGEF membrane binding. J Biol Chem 275:14992-14999.
39. Zeng X, et al. (2008) Initiation of Wnt signaling: Control of Wnt coreceptor Lrp6 phosphorylation/activation via frizzled, dishevelled and axin functions. Development 135:367-375.
40. Egger-Adam D, Katanaev VL (2008) Trimeric G protein-dependent signaling by Frizzled receptors in animal development. Front Biosci 13:4740-4755.
41. Guo J, et al. (2010) Suppression of Wnt signaling by Dkk1 attenuates PTH-mediated stromal cell response and new bone formation. Cell Metab 11(2):161-171.
42. Bianco P, et al. (1998) Reproduction of human fibrous dysplasia of bone in immunocompromised mice by transplanted mosaics of normal and Gsalpha-mutated skeletal progenitor cells. J Clin Invest 101:1737-1744.
43. MacDonald BT, et al. (2007) Bone mass is inversely proportional to Dkk1 levels in mice. Bone 41:331-339.
44. Li X, et al. (2008) Targeted deletion of the sclerostin gene in mice results in increased bone formation and bone strength. J Bone Miner Res 23:860-869.
45. Babij P, et al. (2003) High bone mass in mice expressing a mutant LRP5 gene. J Bone Miner Res 18:960-974.
46. Zhang M, et al. (2002) Osteoblast-specific knockout of the insulin-like growth factor (IGF) receptor gene reveals an essential role of IGF signaling in bone matrix mineralization. J Biol Chem 277:44005-44012.
47. Oshima M, et al. (1996) Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 87:803-809.
48. Barker N, et al. (2009) Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457:608-611.
49. Wilson CH, McIntyre RE, Arends MJ, Adams DJ (2010) The activating mutation R201C in GNAS promotes intestinal tumourigenesis in Apc(Min/+) mice through activation of Wnt and ERK1/2 MAPK pathways. Oncogene 29:4567-4575.
50. Li G, Iyengar R (2002) Calpain as an effector of the Gq signaling pathway for inhibition of Wnt/beta -catenin-regulated cell proliferation. Proc Natl Acad Sci USA 99: 13254-13259.
51. Regard JB, Sato IT, Coughlin SR (2008) Anatomical profiling of G protein-coupled receptor expression. Cell 135:561-571.
52. Wein MN, Jones DC, Glimcher LH (2008) Lentivirus delivery of shRNA constructs into osteoblasts. Methods Mol Biol 455:149-155.
53. Topol L, et al. (2003) Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent beta-catenin degradation. J Cell Biol 162(5):899-908.
54. Celi FS, et al. (2008) The role of type 1 and type 2 5′-deiodinase in the pathophysiology of the 3,5,3′-triiodothyronine toxicosis of McCune-Albright syndrome. J Clin Endocrinol Metab 93(6):2383-2389.
55. Guettier JM, et al. (2009) A chemical-genetic approach to study G protein regulation of beta cell function in vivo. Proc Natl Acad Sci U S A 106(45):19197-19202.
56. Chen M, et al. (2005) Increased glucose tolerance and reduced adiposity in the absence of fasting hypoglycemia in mice with liver-specific Gs alpha deficiency. J Clin Invest 115(11):3217-3227.
57. Bianco P, Kuznetsov SA, Riminucci M, & Gehron Robey P (2006) Postnatal skeletal stem cells. Methods Enzymol 419:117-148.
58. Bilic J, et al. (2007) Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science 316(5831):1619-1622.
59. Armbruster BN, Li X, Pausch MH, Herlitze S, & Roth BL (2007) Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc Natl Acad Sci U S A 104(12):5163-5168.
60. Marinissen MJ, Servitja JM, Offermanns S, Simon MI, & Gutkind JS (2003) Thrombin proteaseactivated receptor-1 signals through Gq- and G13-initiated MAPK cascades regulating c-Jun expression to induce cell transformation. J Biol Chem 278(47):46814-46825.