Sonic Hedgehog Regulates Osteoblast Function by Focal Adhesion Kinase Signaling in the Process of Fracture Healing

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Horikiri, Yuu ^a   Shimo, Tsuyoshi ^a   Kurio, Naito ^a   Okui, Tatsuo ^a   Matsumoto, Kenichi ^a   Iwamoto, Masahiro ^b   Sasaki, Akira ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; FOCAL ADHESION KINASE; MESSENGER RNA; SHORT HAIRPIN RNA; SONIC HEDGEHOG PROTEIN; TYROSINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BONE REMODELING; CARTILAGE CELL; CELL ADHESION; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL STIMULATION; CELL STRAIN 3T3; CELL STRUCTURE; COCULTURE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FRACTURE HEALING; GENE EXPRESSION; HYPERTROPHY; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; OSTEOBLAST; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; RIB FRACTURE; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; CELL ADHESION; CELL DIFFERENTIATION; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FRACTURE HEALING; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HEDGEHOG PROTEINS; MALE; MICE; OSTEOBLASTS; OSTEOCLASTS; PARATHYROID HORMONE-RELATED PROTEIN; RIB FRACTURES; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 84885065594     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076785     Document Type: Article

References (45)

1. Schindeler A, McDonald MM, Bokko P, Little DG, (2008) Bone remodeling during fracture repair: The cellular picture. Semin Cell Dev Biol 19: 459-466. doi:10.1016/j.semcdb.2008.07.004. PubMed: 18692584.
2. Agarwala S, Sanders TA, Ragsdale CW, (2001) Sonic hedgehog control of size and shape in midbrain pattern formation. Science 291: 2147-2150. doi:10.1126/science.1058624. PubMed: 11251119.
3. Ahn S, Joyner AL, (2005) In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437: 894-897. doi:10.1038/nature03994. PubMed: 16208373.
4. Ito H, Akiyama H, Shigeno C, Iyama K, Matsuoka H, et al. (1999) Hedgehog signaling molecules in bone marrow cells at the initial stage of fracture repair. Biochem Biophys Res Commun 262: 443-451. doi:10.1006/bbrc.1999.1197. PubMed: 10462495.
5. Kimura H, Ng JM, Curran T, (2008) Transient inhibition of the Hedgehog pathway in young mice causes permanent defects in bone structure. Cancer Cell 13: 249-260. doi:10.1016/j.ccr.2008.01.027. PubMed: 18328428.
6. Miyaji T, Nakase T, Iwasaki M, Kuriyama K, Tamai N, et al. (2003) Expression and distribution of transcripts for sonic hedgehog in the early phase of fracture repair. Histochem Cell Biol 119: 233-237. PubMed: 12649738.
7. Nakamura T, Aikawa T, Iwamoto-Enomoto M, Iwamoto M, Higuchi Y, et al. (1997) Induction of osteogenic differentiation by hedgehog proteins. Biochem Biophys Res Commun 237: 465-469. doi:10.1006/bbrc.1997.7156. PubMed: 9268735.
8. Edwards PC, Ruggiero S, Fantasia J, Burakoff R, Moorji SM, et al. (2005) Sonic hedgehog gene-enhanced tissue engineering for bone regeneration. Gene Ther 12: 75-86. doi:10.1038/sj.gt.3302386. PubMed: 15510177.
9. Mak KK, Bi Y, Wan C, Chuang PT, Clemens T, et al. (2008) Hedgehog signaling in mature osteoblasts regulates bone formation and resorption by controlling PTHrP and RANKL expression. Dev Cell 14: 674-688. doi:10.1016/j.devcel.2008.02.003. PubMed: 18477451.
10. Honami T, Shimo T, Okui T, Kurio N, Hassan NM, et al. (2012) Sonic hedgehog signaling promotes growth of oral squamous cell carcinoma cells associated with bone destruction. Oral Oncol 48: 49-55. doi:10.1016/j.oraloncology.2012.09.001. PubMed: 21945071.
11. Mundy GR, Yang X, (2008) Hedgehog coordination of postnatal osteoclast and osteoblast activities. Dev Cell 14: 637-638. doi:10.1016/j.devcel.2008.04.010. PubMed: 18477444.
12. Partridge MA, Marcantonio EE, (2006) Initiation of attachment and generation of mature focal adhesions by integrin-containing filopodia in cell spreading. Mol Biol Cell 17: 4237-4248. doi:10.1091/mbc.E06-06-0496. PubMed: 16855018.
13. Wary KK, Kohler EE, Chatterjee I, (2012) Focal adhesion kinase regulation of neovascularization. Microvasc Res 83: 64-70. doi:10.1016/j.mvr.2011.05.002. PubMed: 21616084.
14. Guan JL, (2010) Integrin signaling through FAK in the regulation of mammary stem cells and breast cancer. IUBMB Life 62: 268-276. PubMed: 20101634.
15. Ilić D, Furuta Y, Kanazawa S, Takeda N, Sobue K, et al. (1995) Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377: 539-544. doi:10.1038/377539a0. PubMed: 7566154.
16. Sotobori T, Ueda T, Myoui A, Yoshioka K, Nakasaki M, et al. (2006) Bone morphogenetic protein-2 promotes the haptotactic migration of murine osteoblastic and osteosarcoma cells by enhancing incorporation of integrin beta1 into lipid rafts. Exp Cell Res 312: 3927-3938. doi:10.1016/j.yexcr.2006.08.024. PubMed: 17022972.
17. Kim JB, Leucht P, Luppen CA, Park YJ, Beggs HE, et al. (2007) Reconciling the roles of FAK in osteoblast differentiation, osteoclast remodeling, and bone regeneration. Bone 41: 39-51. doi:10.1016/j.bone.2007.01.024. PubMed: 17459803.
18. Leucht P, Kim JB, Currey JA, Brunski J, Helms JA, (2007) FAK-Mediated mechanotransduction in skeletal regeneration. PLOS ONE 2: e390. doi:10.1371/journal.pone.0000390. PubMed: 17460757.
19. Xu JK, Chen HJ, Li XD, Huang ZL, Xu H, et al. (2012) Optimal intensity shock wave promotes the adhesion and migration of rat osteoblasts via integrin beta1-mediated expression of phosphorylated focal adhesion kinase. J Biol Chem 287: 26200-26212. doi:10.1074/jbc.M112.349811. PubMed: 22654119.
20. Kurio N, Shimo T, Fukazawa T, Takaoka M, Okui T, et al. (2011) Anti-tumor effect in human breast cancer by TAE226, a dual inhibitor for FAK and IGF-IR in vitro and in vivo. Exp Cell Res 317: 1134-1146. doi:10.1016/j.yexcr.2011.02.008. PubMed: 21338601.
21. Asaumi K, Nakanishi T, Asahara H, Inoue H, Takigawa M, (2000) Expression of neurotrophins and their receptors (TRK) during fracture healing. Bone 26: 625-633. doi:10.1016/S8756-3282(00)00281-7. PubMed: 10831935.
22. Martin TJ, (2005) Osteoblast-derived PTHrP is a physiological regulator of bone formation. J Clin Invest 115: 2322-2324. doi:10.1172/JCI26239. PubMed: 16138187.
23. Kon T, Cho TJ, Aizawa T, Yamazaki M, Nooh N, et al. (2001) Expression of osteoprotegerin, receptor activator of NF-kappaB ligand (osteoprotegerin ligand) and related proinflammatory cytokines during fracture healing. J Bone Miner Res 16: 1004-1014. doi:10.1359/jbmr.2001.16.6.1004. PubMed: 11393777.
24. Huang CH, Chen MH, Young TH, Jeng JH, Chen YJ, (2009) Interactive effects of mechanical stretching and extracellular matrix proteins on initiating osteogenic differentiation of human mesenchymal stem cells. J Cell Biochem 108: 1263-1273. doi:10.1002/jcb.22356. PubMed: 19795386.
25. Salasznyk RM, Klees RF, Williams WA, Boskey A, Plopper GE, (2007) Focal adhesion kinase signaling pathways regulate the osteogenic differentiation of human mesenchymal stem cells. Exp Cell Res 313: 22-37. doi:10.1016/j.yexcr.2006.09.013. PubMed: 17081517.
26. Friedland JC, Lee MH, Boettiger D, (2009) Mechanically activated integrin switch controls alpha5beta1 function. Science 323: 642-644. doi:10.1126/science.1168441. PubMed: 19179533.
27. Liao X, Lu S, Zhuo Y, Winter C, Xu W, et al. (2012) Visualization of Src and FAK activity during the differentiation process from HMSCs to osteoblasts. PLOS ONE 7: e42709. doi:10.1371/journal.pone.0042709. PubMed: 22900044.
28. Nakamura M, Nagai A, Tanaka Y, Sekijima Y, Yamashita K, (2010) Polarized hydroxyapatite promotes spread and motility of osteoblastic cells. J Biomed Mater Res A 92: 783-790. PubMed: 19274714.
29. Nakayamada S, Okada Y, Saito K, Tamura M, Tanaka Y, (2003) Beta1 integrin/focal adhesion kinase-mediated signaling induces intercellular adhesion molecule 1 and receptor activator of nuclear factor kappa B ligand on osteoblasts and osteoclast maturation. J Biol Chem 278: 45368-45374. doi:10.1074/jbc.M308786200. PubMed: 12954625.
30. Damsky CH, Ilić D, (2002) Integrin signaling: it's where the action is. Curr Opin Cell Biol 14: 594-602. doi:10.1016/S0955-0674(02)00368-X. PubMed: 12231355.
31. Owen JD, Ruest PJ, Fry DW, Hanks SK, (1999) Induced focal adhesion kinase (FAK) expression in FAK-null cells enhances cell spreading and migration requiring both auto- and activation loop phosphorylation sites and inhibits adhesion-dependent tyrosine phosphorylation of Pyk2. Mol Cell Biol 19: 4806-4818. PubMed: 10373530.
32. Schaller MD, (2010) Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions. J Cell Sci 123: 1007-1013. doi:10.1242/jcs.045112. PubMed: 20332118.
33. Evangelista M, Tian H, de Sauvage FJ, (2006) The hedgehog signaling pathway in cancer. Clin Cancer Res 12: 5924-5928. doi:10.1158/1078-0432.CCR-06-1736. PubMed: 17062662.
34. Chen JS, Huang XH, Wang Q, Huang JQ, Zhang LJ, et al. (2013) Sonic hedgehog signaling pathway induces cell migration and invasion through focal adhesion kinase/AKT signaling-mediated activation of matrix metalloproteinase (MMP)-2 and MMP-9 in liver cancer. Carcinogenesis 34: 10-19. doi:10.1093/carcin/bgs274. PubMed: 22948179.
35. Fournier-Thibault C, Blavet C, Jarov A, Bajanca F, Thorsteinsdóttir S, et al. (2009) Sonic hedgehog regulates integrin activity, cadherin contacts, and cell polarity to orchestrate neural tube morphogenesis. J Neurosci 29: 12506-12520. doi:10.1523/JNEUROSCI.2003-09.2009. PubMed: 19812326.
36. Plaisant M, Giorgetti-Peraldi S, Gabrielson M, Loubat A, Dani C, et al. (2011) Inhibition of hedgehog signaling decreases proliferation and clonogenicity of human mesenchymal stem cells. PLOS ONE 6: e16798. doi:10.1371/journal.pone.0016798. PubMed: 21304817.
37. Liao X, Siu MK, Au CW, Wong ES, Chan HY, et al. (2009) Aberrant activation of hedgehog signaling pathway in ovarian cancers: effect on prognosis, cell invasion and differentiation. Carcinogenesis 30: 131-140. PubMed: 19028702.
38. Blaess S, Graus-Porta D, Belvindrah R, Radakovits R, Pons S, et al. (2004) Beta1-integrins are critical for cerebellar granule cell precursor proliferation. J Neurosci 24: 3402-3412. doi:10.1523/JNEUROSCI.5241-03.2004. PubMed: 15056720.
39. Koukouritaki SB, Gravanis A, Stournaras C, (1999) Tyrosine phosphorylation of focal adhesion kinase and paxillin regulates the signaling mechanism of the rapid nongenomic action of dexamethasone on actin cytoskeleton. Mol Med 5: 731-742. PubMed: 10656875.
40. Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, et al. (2002) The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 108: 17-29. doi:10.1016/S0092-8674(01)00622-5. PubMed: 11792318.
41. Tian Y, Xu Y, Fu Q, Dong Y, (2012) Osterix is required for Sonic hedgehog-induced osteoblastic MC3T3-E1 cell differentiation. Cell Biochem Biophys 64: 169-176. doi:10.1007/s12013-012-9369-7. PubMed: 22648388.
42. Lee HL, Bae OY, Baek KH, Kwon A, Hwang HR, et al. (2011) High extracellular calcium-induced NFATc3 regulates the expression of receptor activator of NF-kappaB ligand in osteoblasts. Bone 49: 242-249. doi:10.1016/j.bone.2011.04.006. PubMed: 21514407.
43. Vortkamp A, Lee K, Lanske B, Segre GV, Kronenberg HM, et al. (1996) Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273: 613-622. doi:10.1126/science.273.5275.613. PubMed: 8662546.
44. Sterling JA, Oyajobi BO, Grubbs B, Padalecki SS, Munoz SA, et al. (2006) The hedgehog signaling molecule Gli2 induces parathyroid hormone-related peptide expression and osteolysis in metastatic human breast cancer cells. Cancer Res 66: 7548-7553. doi:10.1158/0008-5472.CAN-06-0452. PubMed: 16885353.
45. Pratap J, Wixted JJ, Gaur T, Zaidi SK, Dobson J, et al. (2008) Runx2 transcriptional activation of Indian Hedgehog and a downstream bone metastatic pathway in breast cancer cells. Cancer Res 68: 7795-7802. doi:10.1158/0008-5472.CAN-08-1078. PubMed: 18829534.