Origin matters: Differences in embryonic tissue origin and Wnt signaling determine the osteogenic potential and healing capacity of frontal and parietal calvarial bones

Journal of Bone and Mineral Research

Volumn 25, Issue 7, 2010, Pages 1680-1694

  Quarto, Natalina ^a,b   Wan, Derrick C ^a   Kwan, Matt D ^a   Panetta, Nicholas J ^a   Li, Shuli ^a   Longaker, Michael T ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Origin; Osteogenesis; Tissue; Wnt signaling

Indexed keywords

BETA CATENIN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; GLYCOGEN SYNTHASE KINASE 3BETA; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE REGENERATION; CALVARIA; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FRACTURE HEALING; FRONTAL BONE; MESODERM; MOUSE; NEURAL CREST; NONHUMAN; OSTEOBLAST; SIGNAL TRANSDUCTION; SKULL;

ANIMALS; BETA CATENIN; CELL DIFFERENTIATION; CELLS, CULTURED; FIBROBLAST GROWTH FACTOR 2; FRONTAL BONE; GLYCOGEN SYNTHASE KINASE 3; MESODERM; MICE; NEURAL CREST; OSTEOBLASTS; OSTEOGENESIS; PARIETAL BONE; REGENERATION; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 77954699773     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1359/jbmr.091116     Document Type: Article

References (69)

1. Morriss-Kay GM. Derivation of the mammalian skull vault. J Anat. 2001;199:143-151.
2. Jiang X, Iseki S, Maxson RE, Sucov HM, Morriss-Kay GM. Tissue origins and interactions in the mammalian skull vault. Dev Biol. 2002;241:106-116. (Pubitemid 34066765)
3. Chai Y, Jiang X, Ito Y, et al. Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development. 2000;127:1671-1679. (Pubitemid 30234924)
4. LaBonne C, Bronner-Fraser M. Molecular mechanisms of neural crest formation. Annu Rev Cell Dev Biol. 1999;15:81-112. (Pubitemid 32250372)
5. Anderson DJ. Genes, lineages and the neural crest: a speculative review. Philos Trans R Soc Lond B Biol Sci. 2000;355:953-964.
6. Trainor P, Krumlauf R. Development. Riding the crest of the Wnt signaling wave. Science. 2002;297:781-783.
7. Le Douarin NM, Calloni GW, Dupin E. The stem cells of the neural crest. Cell Cycle. 2008;7:1013-1019.
8. Couly G, Grapin-Botton A, Coltey P, Le Douarin NM. The regeneration of the cephalic neural crest, a problem revisited: the regenerating cells originate from the contralateral or from the anterior and posterior neural fold. Development. 1996;122:3393-3407. (Pubitemid 26395982)
9. Kontges G, Lumsden A. Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development. 1996;122:3229-3242. (Pubitemid 26371987)
10. Karsenty G. Minireview: transcriptional control of osteoblast differentiation. Endocrinology. 2001;142:2731-2733. (Pubitemid 32575505)
11. Karsenty G, Wagner EF. Reaching a genetic and molecular understanding of skeletal development. Dev Cell. 2002;2:389-406. (Pubitemid 34436569)
12. Boulet AM, Moon AM, Arenkiel BR, Capecchi MR. The roles of Fgf4 and Fgf8 in limb bud initiation and outgrowth. Dev Biol. 2004;273:361-372.
13. Karsenty G. Transcriptional control of skeletogenesis. Annu Rev Genomics Hum Genet. 2008;9:183-196.
14. Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol. 2004;20:781-810. (Pubitemid 39488658)
15. Nusse R. Wnt signaling in disease and in development. Cell Res. 2005;15:28-32.
16. Clevers H. Wnt/β-catenin signaling in development and disease. Cell. 2006;127:469-480.
17. Hartmann C. A Wnt canon orchestrating osteoblastogenesis. Trends Cell Biol. 2006;16:151-158.
18. Krishnan V, Bryant HU, Macdougald OA. Regulation of bone mass by Wnt signaling. J Clin Invest. 2006;116:1202-1209.
19. Nelson WJ, Nusse R. Convergence of Wnt, β-catenin, and cadherin pathways. Science. 2004;303:1483-1487.
20. Moon RT, Bowerman B, Boutros M, Perrimon N. The promise and perils of Wnt signaling through b-catenin. Science. 2002;296:1644-1646.
21. Lee JS, Ishimoto A, Yanagawa S. Characterization of mouse dishevelled (Dvl) proteins in Wnt/Wingless signaling pathway. J Biol Chem. 1999;274:21464-21470.
22. Seto ES, Bellen HJ. The ins and outs of Wingless signaling. Trends Cell Biol. 2004;14:45-53.
23. Ikeda S, Kishida S, Yamamoto H, Murai H, Koyama S, Kikuchi A. Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3β and β-catenin and promotes GSK-3β-dependent phosphorylation of β-catenin. EMBO J. 1998;17:1371-1384.
24. Akiyama T. Wnt/β-catenin signaling. Cytokine Growth Factor Rev. 2000;11:273-282.
25. He TC, Sparks AB, Rago C, et al. Identification of c-MYC as a target of the APC pathway. Science. 1998;281:1509-1512.
26. Tetsu O, McCormick F. β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature. 1999;398:422-426.
27. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F. Wnt/β-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol. 2002;22:1172-1183.
28. Hill TP, Spater D, Taketo MM, Birchmeier W, Hartmann C. Canonical Wnt/β-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev Cell. 2005;8:727-738.
29. Day TF, Guo X, Garrett-Beal L, Yang Y. Wnt/β-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev Cell. 2005;8:739-750.
30. Gong Y, Slee RB, Fukai N, et al. LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell. 2001;107:513-523.
31. Westendorf JJ, Kahler RA, Schroeder TM. Wnt signaling in osteoblasts and bone diseases. Gene. 2004;341:19-39.
32. Glass DA 2nd, Bialek P, Ahn JD, et al. Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev Cell. 2005;8:751-764.
33. Boyden LM, Mao J, Belsky J, et al. High bone density due to a mutation in LDL-receptor-related protein 5. N Engl J Med. 2002;346:1513-1521. (Pubitemid 34755690)
34. Babij P, Zhao W, Small C, et al. High bone mass in mice expressing a mutant LRP5 gene. J Bone Miner Res. 2003;18:960-974.
35. Little RD, Carulli JP, Del Mastro RG, 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. 2002;70:11-19.
36. Holmen SL, Giambernardi TA, Zylstra CR, et al. Decreased BMD and limb deformities in mice carrying mutations in both Lrp5 and Lrp6. J Bone Miner Res. 2004;19:2033-2040.
37. Kato M, Patel MS, Levasseur R, 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. 2002;157:303-314.
38. Chung BD, Kayserili H, Ai M, et al. A mutation in the signal sequence of LRP5 in a family with an osteoporosis-pseudoglioma syndrome (OPPG)-like phenotype indicates a novel disease mechanism for trinucleotide repeats. Hum Mutat. 2009.
39. Takada S, Stark KL, Shea MJ, Vassileva G, McMahon JA, McMahon AP. Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev. 1994;8:174-189. (Pubitemid 24044341)
40. Ikeya M, Takada S. Wnt-3a is required for somite specification along the anteroposterior axis of the mouse embryo and for regulation of cdx-1 expression. Mech Dev. 2001;103:27-33. (Pubitemid 32457904)
41. -/- mice. Genes Dev. 1999;13:709-717.
42. Quarto NWD, Longaker MT. Molecular mechanisms of FGF-2 inhibitory activity in the osteogenic context of mouse adipose-derived stem cells (mASCs). Bone. 2008.
43. Kolligs FT, Hu G, Dang CV, Fearon ER. Neoplastic transformation of RK3E by mutant β-catenin requires deregulation of Tcf/Lef transcription but not activation of c-myc expression. Mol Cell Biol. 1999;19:5696-5706. (Pubitemid 29339926)
44. Quarto N, Longaker MT. FGF-2 inhibits osteogenesis in mouse adipose tissue-derived stromal cells and sustains their proliferative and osteogenic potential state. Tissue Eng. 2006;12:1405-1418. (Pubitemid 44174777)
45. Quarto N, Fong KD, Longaker MT. Gene profiling of cells expressing different FGF-2 forms. Gene. 2005;356:49-68. (Pubitemid 41175971)
46. Wan DC, Shi YY, Nacamuli RP, Quarto N, Lyons KM, Longaker MT. Osteogenic differentiation of mouse adipose-derived adult stromal cells requires retinoic acid and bone morphogenetic protein receptor type IB signaling. Proc Natl Acad Sci USA. 2006;103:12335-12340. (Pubitemid 44267260)
47. Quarto N, Finger FP, Rifkin DB. The NH2-terminal extension of high molecular weight bFGF is a nuclear targeting signal. J Cell Physiol. 1991;147:311-318. (Pubitemid 21910113)
48. Quarto N, Behr B, Li S, Longaker MT. Differential FGF ligands and FGF receptors expression pattern in frontal and parietal calvarial bones. Cells Tissues Organs. 2009.
49. Yu HM, Jerchow B, Sheu TJ, et al. The role of Axin2 in calvarial morphogenesis and craniosynostosis. Development. 2005;132:1995-2005. (Pubitemid 40691787)
50. Chen Y, Alman BA. Wnt pathway, an essential role in bone regeneration. J Cell Biochem. 2009;106:353-362.
51. Macsai CE, Foster BK, Xian CJ. Roles of Wnt signalling in bone growth, remodelling, skeletal disorders and fracture repair. J Cell Physiol. 2008;215:578-587.
52. Leucht P, Minear S, Ten Berge D, Nusse R, Helms JA. Translating insights from development into regenerative medicine: the function of Wnts in bone biology. Semin Cell Dev Biol. 2008;19:434-443.
53. Cadigan KM, Nusse R. Wnt signaling: a common theme in animal development. Genes Dev. 1997;11:3286-3305. (Pubitemid 28023954)
54. Desbois-Mouthon C, Cadoret A, Blivet-Van Eggelpoel MJ, et al. Insulin and IGF-1 stimulate the β-catenin pathway through two signalling cascades involving GSK-3β inhibition and Ras activation. Oncogene. 2001;20:252-259.
55. Israsena N, Hu M, Fu W, Kan L, Kessler JA. The presence of FGF2 signaling determines whether beta-catenin exerts effects on proliferation or neuronal differentiation of neural stem cells. Dev Biol. 2004;268:220-231.
56. Holnthoner W, Pillinger M, Groger M, et al. Fibroblast growth factor-2 induces Lef/Tcf-dependent transcription in human endothelial cells. J Biol Chem. 2002;277:45847-45853.
57. Shimizu T, Kagawa T, Inoue T, et al. Stabilized β-catenin functions through TCF/LEF proteins and the Notch/RBP-Jκ complex to promote proliferation and suppress differentiation of neural precursor cells. Mol Cell Biol. 2008;28:7427-7441.
58. Gaur T, Lengner CJ, Hovhannisyan H, et al. Canonical WNT signaling promotes osteogenesis by directly stimulating Runx2 gene expression. J Biol Chem. 2005;280:33132-33140.
59. Kim JB, Leucht P, Lam K, et al. Bone regeneration is regulated by Wnt signaling. J Bone Miner Res. 2007;22:1913-1923.
60. Kitagaki J, Iwamoto M, Liu JG, Tamamura Y, Pacifci M, Enomoto-Iwamoto M. Activation of β-catenin-LEF/TCF signal pathway in chondrocytes stimulates ectopic endochondral ossification. Osteoarthritis Cartilage. 2003;11:36-43.
61. Leucht P, Kim JB, Helms JA. β-Catenin-dependent Wnt signaling in mandibular bone regeneration. J Bone Joint Surg Am. 2008;90(Suppl 1): 3-8.
62. Chen Y, Whetstone HC, Lin AC, et al. β-Catenin signaling plays a disparate role in different phases of fracture repair: implications for therapy to improve bone healing. PLoS Med. 2007;4:e249.
63. Leucht P, Kim JB, Amasha R, James AW, Girod S, Helms JA. Embryonic origin and Hox status determine progenitor cell fate during adult bone regeneration. Development. 2008;135:2845-2854.
64. Wei K, Chen J, Akrami K, Galbraith GC, Lopez IA, Chen F. Neural crest cell deficiency of c-myc causes skull and hearing defects. Genesis. 2007;45:382-390. (Pubitemid 47015324)
65. Fischer L, Boland G, Tuan RS. Wnt signaling during BMP-2 stimulation of mesenchymal chondrogenesis. J Cell Biochem. 2002;84:816-831. (Pubitemid 34113120)
66. McManus EJ, Sakamoto K, Armit LJ, et al. Role that phosphorylation of GSK3 plays in insulin and Wnt signalling defined by knock-in analysis. EMBO J. 2005;24:1571-1583. (Pubitemid 40646447)
67. Reinhold MI, Naski MC. Direct interactions of Runx2 and canonical Wnt signaling induce FGF-18. J Biol Chem. 2007;282:3653-3663.
68. -/- mice. Genes Dev. 2002;16:3173-3185.
69. ten Berge D, Brugmann SA, Helms JA, Nusse R. Wnt and FGF signals interact to coordinate growth with cell fate specification during limb development. Development. 2008;135:3247-3257.