Integration of BMP, Wnt, and notch signaling pathways in osteoblast differentiation

Journal of Cellular Biochemistry

Volumn 112, Issue 12, 2011, Pages 3491-3501

  Lin, Grace L ^a   Hankenson, Kurt D ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Bone morphogenetic protein (BMP); Fibroblast growth factor; Hedgehog; Mesenchymal stem cell (MSC); Notch; Osteoblast differentiation; Osteogenesis; RUNX2; WNT

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; FIBROBLAST GROWTH FACTOR; NOTCH RECEPTOR; PROTEIN SERINE THREONINE KINASE; RECOMBINANT FIBROBLAST GROWTH FACTOR; TRANSCRIPTION FACTOR RUNX2; WNT PROTEIN; WNT3A PROTEIN;

ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL FATE; HUMAN; MESENCHYMAL STEM CELL; NONHUMAN; OSTEOBLAST; OSTEOBLAST DIFFERENTIATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CORE BINDING FACTOR ALPHA 1 SUBUNIT; HUMANS; OSTEOBLASTS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; WNT PROTEINS;

ERINACEIDAE;

EID: 80054975678     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.23287     Document Type: Article

References (90)

1. Ambrosetti D, Holmes G, Mansukhani A, Basilico C,. 2008. Fibroblast growth factor signaling uses multiple mechanisms to inhibit Wnt-induced transcription in osteoblasts. Mol Cell Biol 28: 4759-4771.
2. Baddoo M, Hill K, Wilkinson R, Gaupp D, Hughes C, Kopen GC, Phinney DG,. 2003. Characterization of mesenchymal stem cells isolated from murine bone marrow by negative selection. J Cell Biochem 89: 1235-1249. (Pubitemid 36959389)
3. Bain G, Muller T, Wang X, Papkoff J,. 2003. Activated beta-catenin induces osteoblast differentiation of C3H10T1/2 cells and participates in BMP2 mediated signal transduction. Biochem Biophys Res Commun 301: 84-91. (Pubitemid 36268851)
4. Baksh D, Boland GM, Tuan RS,. 2007. Cross-talk between Wnt signaling pathways in human mesenchymal stem cells leads to functional antagonism during osteogenic differentiation. J Cell Biochem 101: 1109-1124. (Pubitemid 47253714)
5. Bandyopadhyay A, Tsuji K, Cox K, Harfe BD, Rosen V, Tabin CJ,. 2006. Genetic analysis of the roles of BMP2, BMP4, and BMP7 in limb patterning and skeletogenesis. PLoS Genet 2: e216.
6. Bennett CN, Longo KA, Wright WS, Suva LJ, Lane TF, Hankenson KD, MacDougald OA,. 2005. Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc Natl Acad Sci USA 102: 3324-3329. (Pubitemid 40328044)
7. Bennett CN, Ouyang H, Ma YL, Zeng Q, Gerin I, Sousa KM, Lane TF, Krishnan V, Hankenson KD, MacDougald OA,. 2007. Wnt10b increases postnatal bone formation by enhancing osteoblast differentiation. J Bone Miner Res 22: 1924-1932. (Pubitemid 351229309)
8. 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. (Pubitemid 44264134)
9. Bolos V, Grego-Bessa J, de la Pompa JL,. 2007. Notch signaling in development and cancer. Endocr Rev 28: 339-363. (Pubitemid 46984831)
10. Boyden LM, Mao J, Belsky J, Mitzner L, Farhi A, Mitnick MA, Wu D, Insogna K, Lifton RP,. 2002. High bone density due to a mutation in LDL-receptor-related protein 5. N Engl J Med 346: 1513-1521. (Pubitemid 34755690)
11. Caplan AI,. 2007. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 213: 341-347. (Pubitemid 47509711)
12. Celeste AJ, Iannazzi JA, Taylor RC, Hewick RM, Rosen V, Wang EA, Wozney JM,. 1990. Identification of transforming growth factor beta family members present in bone-inductive protein purified from bovine bone. Proc Natl Acad Sci USA 87: 9843-9847. (Pubitemid 120016540)
13. Chamberlain G, Fox J, Ashton B, Middleton J,. 2007. Concise review: Mesenchymal stem cells: Their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25: 2739-2749. (Pubitemid 350127858)
14. Chen Y, Whetstone HC, Youn A, Nadesan P, Chow EC, Lin AC, Alman BA,. 2007. Beta-catenin signaling pathway is crucial for bone morphogenetic protein 2 to induce new bone formation. J Biol Chem 282: 526-533. (Pubitemid 47076655)
15. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, Beachy PA,. 1996. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383: 407-413. (Pubitemid 26330823)
16. Cho SW, Yang JY, Sun HJ, Jung JY, Her SJ, Cho HY, Choi HJ, Kim SW, Kim SY, Shin CS,. 2009. Wnt inhibitory factor (WIF)-1 inhibits osteoblastic differentiation in mouse embryonic mesenchymal cells. Bone 44: 1069-1077.
17. Choi KY, Kim HJ, Lee MH, Kwon TG, Nah HD, Furuichi T, Komori T, Nam SH, Kim YJ, Ryoo HM,. 2005. Runx2 regulates FGF2-induced Bmp2 expression during cranial bone development. Dev Dyn 233: 115-121. (Pubitemid 40548029)
18. Cui Y, Niziolek PJ, MacDonald BT, Zylstra CR, Alenina N, Robinson DR, Zhong Z, Matthes S, Jacobsen CM, Conlon RA, Brommage R, Liu Q, Mseeh F, Powell DR, Yang QM, Zambrowicz B, Gerrits H, Gossen JA, He X, Bader M, Williams BO, Warman ML, Robling AG,. 2011. Lrp5 functions in bone to regulate bone mass. Nat Med 17: 684-691.
19. Davis LA, Zur Nieden NI,. 2008. Mesodermal fate decisions of a stem cell: The Wnt switch. Cell Mol Life Sci 65: 2658-2674.
20. 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. (Pubitemid 40585296)
21. De Bari C, Dell'Accio F, Vanlauwe J, Eyckmans J, Khan IM, Archer CW, Jones EA, McGonagle D, Mitsiadis TA, Pitzalis C, Luyten FP,. 2006. Mesenchymal multipotency of adult human periosteal cells demonstrated by single-cell lineage analysis. Arthritis Rheum 54: 1209-1221. (Pubitemid 43672933)
22. Deregowski V, Gazzerro E, Priest L, Rydziel S, Canalis E,. 2006. Notch 1 overexpression inhibits osteoblastogenesis by suppressing Wnt/beta-catenin but not bone morphogenetic protein signaling. J Biol Chem 281: 6203-6210. (Pubitemid 43847550)
23. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G,. 1997. Osf2/Cbfa1: A transcriptional activator of osteoblast differentiation. Cell 89: 747-754. (Pubitemid 27516177)
24. Engin F, Yao Z, Yang T, Zhou G, Bertin T, Jiang MM, Chen Y, Wang L, Zheng H, Sutton RE, Boyce BF, Lee B,. 2008. Dimorphic effects of Notch signaling in bone homeostasis. Nat Med 14: 299-305. (Pubitemid 351347909)
25. Eyckmans J, Roberts SJ, Schrooten J, Luyten FP,. 2010. A clinically relevant model of osteoinduction: A process requiring calcium phosphate and BMP/Wnt signalling. J Cell Mol Med 14: 1845-1856.
26. Fuentealba LC, Eivers E, Ikeda A, Hurtado C, Kuroda H, Pera EM, De Robertis EM,. 2007. Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 131: 980-993. (Pubitemid 350138081)
27. Fujii M, Takeda K, Imamura T, Aoki H, Sampath TK, Enomoto S, Kawabata M, Kato M, Ichijo H, Miyazono K,. 1999. Roles of bone morphogenetic protein type I receptors and Smad proteins in osteoblast and chondroblast differentiation. Mol Biol Cell 10: 3801-3813. (Pubitemid 29534026)
28. Fujita K, Janz S,. 2007. Attenuation of WNT signaling by DKK-1 and -2 regulates BMP2-induced osteoblast differentiation and expression of OPG, RANKL and M-CSF. Mol Cancer 6: 71.
29. Gaur T, Lengner CJ, Hovhannisyan H, Bhat RA, Bodine PV, Komm BS, Javed A, van Wijnen AJ, Stein JL, Stein GS, Lian JB,. 2005. Canonical WNT signaling promotes osteogenesis by directly stimulating Runx2 gene expression. J Biol Chem 280: 33132-33140. (Pubitemid 41397109)
30. 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,. 2001. LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 107: 513-523. (Pubitemid 33152786)
31. Gori F, Thomas T, Hicok KC, Spelsberg TC, Riggs BL,. 1999. Differentiation of human marrow stromal precursor cells: Bone morphogenetic protein-2 increases OSF2/CBFA1, enhances osteoblast commitment, and inhibits late adipocyte maturation. J Bone Miner Res 14: 1522-1535. (Pubitemid 29416678)
32. Hanada K, Dennis JE, Caplan AI,. 1997. Stimulatory effects of basic fibroblast growth factor and bone morphogenetic protein-2 on osteogenic differentiation of rat bone marrow-derived mesenchymal stem cells. J Bone Miner Res 12: 1606-1614. (Pubitemid 27422361)
33. Hassan MQ, Javed A, Morasso MI, Karlin J, Montecino M, van Wijnen AJ, Stein GS, Stein JL, Lian JB,. 2004. Dlx3 transcriptional regulation of osteoblast differentiation: Temporal recruitment of Msx2, Dlx3, and Dlx5 homeodomain proteins to chromatin of the osteocalcin gene. Mol Cell Biol 24: 9248-9261. (Pubitemid 39313925)
34. Hilton MJ, Tu X, Wu X, Bai S, Zhao H, Kobayashi T, Kronenberg HM, Teitelbaum SL, Ross FP, Kopan R, Long F,. 2008. Notch signaling maintains bone marrow mesenchymal progenitors by suppressing osteoblast differentiation. Nat Med 14: 306-314. (Pubitemid 351347911)
35. Holmen SL, Giambernardi TA, Zylstra CR, Buckner-Berghuis BD, Resau JH, Hess JF, Glatt V, Bouxsein ML, Ai M, Warman ML, Williams BO,. 2004. Decreased BMD and limb deformities in mice carrying mutations in both Lrp5 and Lrp6. J Bone Miner Res 19: 2033-2040. (Pubitemid 41103418)
36. Holmen SL, Zylstra CR, Mukherjee A, Sigler RE, Faugere MC, Bouxsein ML, Deng L, Clemens TL, Williams BO,. 2005. Essential role of beta-catenin in postnatal bone acquisition. J Biol Chem 280: 21162-21168. (Pubitemid 40805677)
37. Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, Neel M, Sussman M, Orchard P, Marx JC, Pyeritz RE, Brenner MK,. 1999. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 5: 309-313. (Pubitemid 29124367)
38. Hu H, Hilton MJ, Tu X, Yu K, Ornitz DM, Long F,. 2005. Sequential roles of Hedgehog and Wnt signaling in osteoblast development. Development 132: 49-60. (Pubitemid 40207966)
39. Huelsken J, Behrens J,. 2002. The Wnt signalling pathway. J Cell Sci 115: 3977-3978. (Pubitemid 35446796)
40. Ishitani T, Kishida S, Hyodo-Miura J, Ueno N, Yasuda J, Waterman M, Shibuya H, Moon RT, Ninomiya-Tsuji J, Matsumoto K,. 2003. The TAK1-NLK mitogen-activated protein kinase cascade functions in the Wnt-5a/Ca(2+) pathway to antagonize Wnt/beta-catenin signaling. Mol Cell Biol 23: 131-139. (Pubitemid 36008507)
41. Ito T, Sawada R, Fujiwara Y, Tsuchiya T,. 2008. FGF-2 increases osteogenic and chondrogenic differentiation potentials of human mesenchymal stem cells by inactivation of TGF-beta signaling. Cytotechnology 56: 1-7.
42. Javazon EH, Beggs KJ, Flake AW,. 2004. Mesenchymal stem cells: Paradoxes of passaging. Exp Hematol 32: 414-425. (Pubitemid 38624325)
43. Javed A, Bae JS, Afzal F, Gutierrez S, Pratap J, Zaidi SK, Lou Y, van Wijnen AJ, Stein JL, Stein GS, Lian JB,. 2008. Structural coupling of Smad and Runx2 for execution of the BMP2 osteogenic signal. J Biol Chem 283: 8412-8422.
44. Jeon MJ, Kim JA, Kwon SH, Kim SW, Park KS, Park SW, Kim SY, Shin CS,. 2003. Activation of peroxisome proliferator-activated receptor-gamma inhibits the Runx2-mediated transcription of osteocalcin in osteoblasts. J Biol Chem 278: 23270-23277. (Pubitemid 36830140)
45. Kang S, Bennett CN, Gerin I, Rapp LA, Hankenson KD, Macdougald OA,. 2007. Wnt signaling stimulates osteoblastogenesis of mesenchymal precursors by suppressing CCAAT/enhancer-binding protein alpha and peroxisome proliferator-activated receptor gamma. J Biol Chem 282: 14515-14524. (Pubitemid 47100486)
46. Kawabata M, Imamura T, Miyazono K,. 1998. Signal transduction by bone morphogenetic proteins. Cytokine Growth Factor Rev 9: 49-61. (Pubitemid 28280536)
47. Kim HJ, Kim JH, Bae SC, Choi JY, Ryoo HM,. 2003. The protein kinase C pathway plays a central role in the fibroblast growth factor-stimulated expression and transactivation activity of Runx2. J Biol Chem 278: 319-326.
48. Kohn AD, Moon RT,. 2005. Wnt and calcium signaling: Beta-catenin- independent pathways. Cell Calcium 38: 439-446. (Pubitemid 41283282)
49. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T,. 1997. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89: 755-764. (Pubitemid 27516178)
50. Krishnan V, Ma Y, Moseley J, Geiser A, Friant S, Frolik C,. 2001. Bone anabolic effects of sonic/indian hedgehog are mediated by bmp-2/4-dependent pathways in the neonatal rat metatarsal model. Endocrinology 142: 940-947. (Pubitemid 32222444)
51. Kuznetsov SA, Krebsbach PH, Satomura K, Kerr J, Riminucci M, Benayahu D, Robey PG,. 1997. Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J Bone Miner Res 12: 1335-1347. (Pubitemid 27375376)
52. Lee D, Park C, Lee H, Lugus JJ, Kim SH, Arentson E, Chung YS, Gomez G, Kyba M, Lin S, Janknecht R, Lim DS, Choi K,. 2008. ER71 acts downstream of BMP, Notch, and Wnt signaling in blood and vessel progenitor specification. Cell Stem Cell 2: 497-507. (Pubitemid 351598081)
53. Lee KS, Kim HJ, Li QL, Chi XZ, Ueta C, Komori T, Wozney JM, Kim EG, Choi JY, Ryoo HM, Bae SC,. 2000. Runx2 is a common target of transforming growth factor beta1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12. Mol Cell Biol 20: 8783-8792. (Pubitemid 32245911)
54. Lian JB, Stein GS, Javed A, van Wijnen AJ, Stein JL, Montecino M, Hassan MQ, Gaur T, Lengner CJ, Young DW,. 2006. Networks and hubs for the transcriptional control of osteoblastogenesis. Rev Endocr Metab Disord 7: 1-16. (Pubitemid 46044345)
55. Little RD, Carulli JP, Del Mastro RG, Dupuis J, Osborne M, Folz C, Manning SP, Swain PM, Zhao SC, Eustace B, Lappe MM, Spitzer L, Zweier S, Braunschweiger K, Benchekroun Y, Hu X, Adair R, Chee L, FitzGerald MG, Tulig C, Caruso A, Tzellas N, Bawa A, Franklin B, McGuire S, Nogues X, Gong G, Allen KM, Anisowicz A, Morales AJ, Lomedico PT, Recker SM, Van Eerdewegh P, Recker RR, Johnson ML,. 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: 11-19. (Pubitemid 34031693)
56. Liu Z, Tang Y, Qiu T, Cao X, Clemens TL,. 2006. A dishevelled-1/Smad1 interaction couples WNT and bone morphogenetic protein signaling pathways in uncommitted bone marrow stromal cells. J Biol Chem 281: 17156-17163.
57. Long F, Chung UI, Ohba S, McMahon J, Kronenberg HM, McMahon AP,. 2004. Ihh signaling is directly required for the osteoblast lineage in the endochondral skeleton. Development 131: 1309-1318. (Pubitemid 38443885)
58. Mak KK, Chen MH, Day TF, Chuang PT, Yang Y,. 2006. Wnt/beta-catenin signaling interacts differentially with Ihh signaling in controlling endochondral bone and synovial joint formation. Development 133: 3695-3707. (Pubitemid 44614291)
59. Mansukhani A, Ambrosetti D, Holmes G, Cornivelli L, Basilico C,. 2005. Sox2 induction by FGF and FGFR2 activating mutations inhibits Wnt signaling and osteoblast differentiation. J Cell Biol 168: 1065-1076.
60. Mbalaviele G, Sheikh S, Stains JP, Salazar VS, Cheng SL, Chen D, Civitelli R,. 2005. Beta-catenin and BMP-2 synergize to promote osteoblast differentiation and new bone formation. J Cell Biochem 94: 403-418. (Pubitemid 41420317)
61. Minamizato T, Sakamoto K, Liu T, Kokubo H, Katsube K, Perbal B, Nakamura S, Yamaguchi A,. 2007. CCN3/NOV inhibits BMP-2-induced osteoblast differentiation by interacting with BMP and Notch signaling pathways. Biochem Biophys Res Commun 354: 567-573. (Pubitemid 46161361)
62. Montero A, Okada Y, Tomita M, Ito M, Tsurukami H, Nakamura T, Doetschman T, Coffin JD, Hurley MM,. 2000. Disruption of the fibroblast growth factor-2 gene results in decreased bone mass and bone formation. J Clin Invest 105: 1085-1093. (Pubitemid 30217693)
63. Naganawa T, Xiao L, Abogunde E, Sobue T, Kalajzic I, Sabbieti M, Agas D, Hurley MM,. 2006. In vivo and in vitro comparison of the effects of FGF-2 null and haplo-insufficiency on bone formation in mice. Biochem Biophys Res Commun 339: 490-498. (Pubitemid 41739694)
64. Naganawa T, Xiao L, Coffin JD, Doetschman T, Sabbieti MG, Agas D, Hurley MM,. 2008. Reduced expression and function of bone morphogenetic protein-2 in bones of Fgf2 null mice. J Cell Biochem 103: 1975-1988. (Pubitemid 351501926)
65. Nakamura T, Aikawa T, Iwamoto-Enomoto M, Iwamoto M, Higuchi Y, Pacifici M, Kinto N, Yamaguchi A, Noji S, Kurisu K, Matsuya T,. 1997. Induction of osteogenic differentiation by hedgehog proteins. Biochem Biophys Res Commun 237: 465-469. (Pubitemid 27406054)
66. Nobta M, Tsukazaki T, Shibata Y, Xin C, Moriishi T, Sakano S, Shindo H, Yamaguchi A,. 2005. Critical regulation of bone morphogenetic protein-induced osteoblastic differentiation by Delta1/Jagged1-activated Notch1 signaling. J Biol Chem 280: 15842-15848. (Pubitemid 40616705)
67. Nostro MC, Cheng X, Keller GM, Gadue P,. 2008. Wnt, activin, and BMP signaling regulate distinct stages in the developmental pathway from embryonic stem cells to blood. Cell Stem Cell 2: 60-71.
68. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR, Stamp GW, Beddington RS, Mundlos S, Olsen BR, Selby PB, Owen MJ,. 1997. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89: 765-771. (Pubitemid 27516179)
69. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR,. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147. (Pubitemid 29282067)
70. Plaisant M, Fontaine C, Cousin W, Rochet N, Dani C, Peraldi P,. 2009. Activation of hedgehog signaling inhibits osteoblast differentiation of human mesenchymal stem cells. Stem Cells 27: 703-713.
71. Qiu W, Andersen TE, Bollerslev J, Mandrup S, Abdallah BM, Kassem M,. 2007. Patients with high bone mass phenotype exhibit enhanced osteoblast differentiation and inhibition of adipogenesis of human mesenchymal stem cells. J Bone Miner Res 22: 1720-1731. (Pubitemid 351235138)
72. Qu-Petersen Z, Deasy B, Jankowski R, Ikezawa M, Cummins J, Pruchnic R, Mytinger J, Cao B, Gates C, Wernig A, Huard J,. 2002. Identification of a novel population of muscle stem cells in mice: Potential for muscle regeneration. J Cell Biol 157: 851-864. (Pubitemid 34847822)
73. Rawadi G, Vayssiere B, Dunn F, Baron R, Roman-Roman S,. 2003. BMP-2 controls alkaline phosphatase expression and osteoblast mineralization by a Wnt autocrine loop. J Bone Miner Res 18: 1842-1853. (Pubitemid 37322562)
74. Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, Saggio I, Tagliafico E, Ferrari S, Robey PG, Riminucci M, Bianco P,. 2007. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 131: 324-336. (Pubitemid 47592917)
75. Sampath TK, Muthukumaran N, Reddi AH,. 1987. Isolation of osteogenin, an extracellular matrix-associated, bone-inductive protein, by heparin affinity chromatography. Proc Natl Acad Sci USA 84: 7109-7113.
76. Spinella-Jaegle S, Rawadi G, Kawai S, Gallea S, Faucheu C, Mollat P, Courtois B, Bergaud B, Ramez V, Blanchet AM, Adelmant G, Baron R, Roman-Roman S,. 2001. Sonic hedgehog increases the commitment of pluripotent mesenchymal cells into the osteoblastic lineage and abolishes adipocytic differentiation. J Cell Sci 114: 2085-2094. (Pubitemid 32586633)
77. St-Jacques B, Hammerschmidt M, McMahon AP,. 1999. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 13: 2072-2086. (Pubitemid 29407348)
78. Su N, Sun Q, Li C, Lu X, Qi H, Chen S, Yang J, Du X, Zhao L, He Q, Jin M, Shen Y, Chen D, Chen L,. 2010. Gain-of-function mutation in FGFR3 in mice leads to decreased bone mass by affecting both osteoblastogenesis and osteoclastogenesis. Hum Mol Genet 19: 1199-1210.
79. Sumi T, Tsuneyoshi N, Nakatsuji N, Suemori H,. 2008. Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/beta-catenin, Activin/Nodal and BMP signaling. Development 135: 2969-2979.
80. Tezuka K, Yasuda M, Watanabe N, Morimura N, Kuroda K, Miyatani S, Hozumi N,. 2002. Stimulation of osteoblastic cell differentiation by Notch. J Bone Miner Res 17: 231-239. (Pubitemid 34087655)
81. Tsutsumi S, Shimazu A, Miyazaki K, Pan H, Koike C, Yoshida E, Takagishi K, Kato Y,. 2001. Retention of multilineage differentiation potential of mesenchymal cells during proliferation in response to FGF. Biochem Biophys Res Commun 288: 413-419. (Pubitemid 33022499)
82. Wang EA, Rosen V, Cordes P, Hewick RM, Kriz MJ, Luxenberg DP, Sibley BS, Wozney JM,. 1988. Purification and characterization of other distinct bone-inducing factors. Proc Natl Acad Sci USA 85: 9484-9488. (Pubitemid 19027155)
83. Watt FM, Estrach S, Ambler CA,. 2008. Epidermal Notch signalling: Differentiation, cancer and adhesion. Curr Opin Cell Biol 20: 171-179.
84. Winnier G, Blessing M, Labosky PA, Hogan BL,. 1995. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 9: 2105-2116.
85. Xiao L, Sobue T, Eisliger A, Kronenberg MS, Coffin JD, Doetschman T, Hurley MM,. 2010. Disruption of the Fgf2 gene activates the adipogenic and suppresses the osteogenic program in mesenchymal marrow stromal stem cells. Bone 47: 360-370.
86. Yoon BS, Ovchinnikov DA, Yoshii I, Mishina Y, Behringer RR, Lyons KM,. 2005. Bmpr1a and Bmpr1b have overlapping functions and are essential for chondrogenesis in vivo. Proc Natl Acad Sci USA 102: 5062-5067.
87. Yuasa T, Kataoka H, Kinto N, Iwamoto M, Enomoto-Iwamoto M, Iemura S, Ueno N, Shibata Y, Kurosawa H, Yamaguchi A,. 2002. Sonic hedgehog is involved in osteoblast differentiation by cooperating with BMP-2. J Cell Physiol 193: 225-232.
88. Zamurovic N, Cappellen D, Rohner D, Susa M,. 2004. Coordinated activation of notch, Wnt, and transforming growth factor-beta signaling pathways in bone morphogenic protein 2-induced osteogenesis. Notch target gene Hey1 inhibits mineralization and Runx2 transcriptional activity. J Biol Chem 279: 37704-37715. (Pubitemid 39195484)
89. Zhang H, Bradley A,. 1996. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122: 2977-2986. (Pubitemid 26371964)
90. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH,. 2001. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng 7: 211-228. (Pubitemid 32295155)