Akt promotes BMP2-mediated osteoblast differentiation and bone development

Journal of Cell Science

Volumn 122, Issue 5, 2009, Pages 716-726

  Mukherjee, Aditi ^a   Rotwein, Peter ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Akt; Bone development; Bone morphogenetic factors; Insulin like growth factors; Osteoblast; PI3 kinase Akt pathway

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE B; SMAD PROTEIN; SOMATOMEDIN BINDING PROTEIN 5; TRANSCRIPTION FACTOR JUNB; TRANSCRIPTION FACTOR SOX9; 2 MORPHOLINO 8 PHENYLCHROMONE; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; CHROMONE DERIVATIVE; MORPHOLINE DERIVATIVE; SOMATOMEDIN C;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE GROWTH; BONE MINERALIZATION; BONE REMODELING; CARTILAGE CELL; CELL ACTIVATION; CELL DIFFERENTIATION; CELL FUNCTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FRACTURE; GROWTH REGULATION; MESENCHYMAL STEM CELL; MOUSE; NEWBORN; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL LINE; CYTOLOGY; DRUG ANTAGONISM; GENETICS; METABOLISM; PHYSIOLOGY;

ADENOVIRIDAE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANIMALS, NEWBORN; BONE DEVELOPMENT; BONE MORPHOGENETIC PROTEIN 2; CELL DIFFERENTIATION; CELL LINE; CHROMONES; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 5; INSULIN-LIKE GROWTH FACTOR I; MICE; MICE, INBRED C57BL; MORPHOLINES; OSTEOBLASTS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 66149119052     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.042770     Document Type: Article

References (62)

1. Akune, T., Ogata, N., Hoshi, K., Kubota, N., Terauchi, Y., Tobe, K., Takagi, H., Azuma, Y., Kadowaki, T., Nakamura, K. et al. (2002). Insulin receptor substrate-2 maintains predominance of anabolic function over catabolic function of osteoblasts. J. Cell Biol. 159, 147-156.
2. Bach, L. A., Headey, S. J. and Norton, R. S. (2005). IGF-binding proteins-the pieces are falling into place. Trends Endocrinol. Metab. 16, 228-234.
3. Balcerzak, M., Hamade, E., Zhang, L., Pikula, S., Azzar, G., Radisson, J., Bandorowicz-Pikula, J. and Buchet, R. (2003). The roles of annexins and alkaline phosphatase in mineralization process. Acta Biochim. Pol. 50, 1019-1038.
4. Chalaux, E., Lopez-Rovira, T., Rosa, J. L., Bartrons, R. and Ventura, F. (1998). JunB is involved in the inhibition of myogenic differentiation by bone morphogenetic protein-2. J. Biol. Chem. 273, 537-543.
5. Deng, Z. L., Sharff, K. A., Tang, N., Song, W. X., Luo, J., Luo, X., Chen, J., Bennett, E., Reid, R., Manning, D. et al. (2008). Regulation of osteogenic differentiation during skeletal development. Front. Biosci. 13, 2001-2021.
6. Duan, C. and Xu, Q. (2005). Roles of insulin-like growth factor (IGF) binding proteins in regulating IGF actions. Gen. Comp. Endocrinol. 142, 44-52.
7. Franke, T. F. (2008). Intracellular signaling by Akt: bound to be specific. Sci. Signal. 1, e29.
8. Fujio, Y., Mitsuuchi, Y., Testa, J. R. and Walsh, K. (2001). Activation of Akt2 Inhibits anoikis and apoptosis induced by myogenic differentiation. Cell Death Differ. 8, 1207-1212.
9. Fujita, T., Azuma, Y., Fukuyama, R., Hattori, Y., Yoshida, C., Koida, M., Ogita, K. and Komori, T. (2004). Runx2 induces osteoblast and chondrocyte differentiation and enhances their migration by coupling with PI3K-Akt signaling. J. Cell Biol. 166, 85-95.
10. Ghosh-Choudhury, N., Abboud, S. L., Nishimura, R., Celeste, A., Mahimainathan, L. and Choudhury, G. G. (2002). Requirement of BMP-2-induced phosphatidylinositol 3-kinase and Akt serine/threonine kinase in osteoblast differentiation and Smad-dependent BMP-2 gene transcription. J. Biol. Chem. 277, 33361-33368.
11. Ghosh-Choudhury, N., Mandal, C. C. and Choudhury, G. G. (2007). Statin-induced Ras activation integrates the phosphatidylinositol 3-kinase signal to Akt and MAPK for bone morphogenetic protein-2 expression in osteoblast differentiation. J. Biol. Chem. 282, 4983-4993.
12. Giustina, A., Mazziotti, G. and Canalis, E. (2008). Growth hormone, insulin-like growth factors, and the skeleton. Endocr. Rev. 29, 535-559.
13. Hadjidakis, D. J. and Androulakis, I. I. (2006). Bone remodeling. Ann. NY Acad. Sci. 1092, 385-396.
14. Hanada, M., Feng, J. and Hemmings, B. A. (2004). Structure, regulation and function of PKB/AKT-a major therapeutic target. Biochim. Biophys. Acta 1697, 3-16.
15. Hanai, Y., Tokuda, H., Ishisaki, A., Matsushima-Nishiwaki, R., Nakamura, N., Yoshida, M., Takai, S., Ohta, T. and Kozawa, O. (2006). Involvement of p44/p42 MAP kinase in insulin-like growth factor-I-induced alkaline phosphatase activity in osteoblast-like-MC3T3-E1 cells. Mol. Cell Endocrinol. 251, 42-48.
16. Herpin, A. and Cunningham, C. (2007). Cross-talk between the bone morphogenetic protein pathway and other major signaling pathways results in tightly regulated cell-specific outcomes. FEBS J. 274, 2977-2985.
17. Hoshi, K., Ejiri, S. and Ozawa, H. (2000). Ultrastructural, cytochemical, and biophysical aspects of mechanisms of bone matrix calcification. Kaibogaku Zasshi 75, 457-465.
18. Jiang, J., Lichtler, A. C., Gronowicz, G. A., Adams, D. J., Clark, S. H., Rosen, C. J. and Kream, B. E. (2006). Transgenic mice with osteoblast-targeted insulin-like growth factor-I show increased bone remodeling. Bone 39, 494-504.
19. Kadowaki, T., Tobe, K., Honda-Yamamoto, R., Tamemoto, H., Kaburagi, Y., Momomura, K., Ueki, K., Takahashi, Y., Yamauchi, T., Akanuma, Y. et al. (1996). Signal transduction mechanism of insulin and insulin-like growth factor-1. Endocr. J. 43 Suppl., S33-S41.
20. Karsenty, G. (1998). Transcriptional regulation of osteoblast differentiation during development. Front Biosci. 3, d834-d837.
21. Kavanaugh, M. P. and Kabat, D. (1996). Identification and characterization of a widely expressed phosphate transporter/retrovirus receptor family. Kidney Int. 49, 959-963.
22. Kawamura, N., Kugimiya, F., Oshima, Y., Ohba, S., Ikeda, T., Saito, T., Shinoda, Y., Kawasaki, Y., Ogata, N., Hoshi, K. et al. (2007). Akt1 in osteoblasts and osteoclasts controls bone remodeling. PLoS. ONE. 2, e1058.
23. Khosla, S., Westendorf, J. J. and Oursler, M. J. (2008). Building bone to reverse osteoporosis and repair fractures. J. Clin. Invest 118, 421-428.
24. Komori, T. (2008). Regulation of bone development and maintenance by Runx2. Front Biosci. 13, 898-903.
25. Krishnan, V., Ma, Y., Moseley, J., Geiser, A., Friant, S. and 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.
26. Krishnan, V., Moore, T. L., Ma, Y. L., Helvering, L. M., Frolik, C. A., Valasek, K. M., Ducy, P. and Geiser, A. G. (2003). Parathyroid hormone bone anabolic action requires Cbfa1/Runx2-dependent signaling. Mol. Endocrinol. 17, 423-435.
27. Lawlor, M. A. and Rotwein, P. (2000). Insulin-like growth factor-mediated muscle cell survival: central roles for Akt and cyclin-dependent kinase inhibitor p21. Mol. Cell. Biol. 20, 8983-8995.
28. Lee, M. H., Kim, Y. J., Kim, H. J., Park, H. D., Kang, A. R., Kyung, H. M., Sung, J. H., Wozney, J. M., Kim, H. J. and Ryoo, H. M. (2003). BMP-2-induced Runx2 expression is mediated by Dlx5, and TGF-beta 1 opposes the BMP-2-induced osteoblast differentiation by suppression of Dlx5 expression. J. Biol. Chem. 278, 34387-34394.
29. Li, X. and Cao, X. (2006). BMP signaling and skeletogenesis. Ann. NY Acad. Sci. 1068, 26-40.
30. Lian, J. B., Stein, G. S., Javed, A., van Wijnen, A. J., Stein, J. L., Montecino, M., Hassan, M. Q., Gaur, T., Lengner, C. J. and Young, D. W. (2006). Networks and hubs for the transcriptional control of osteoblastogenesis. Rev. Endocr. Metab. Disord. 7, 1-16.
31. Liu, J. P., Baker, J., Perkins, A. S., Robertson, E. J. and Efstratiadis, A. (1993). Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 75, 59-72.
32. Liu, X., Bruxvoort, K. J., Zylstra, C. R., Liu, J., Cichowski, R., Faugere, M. C., Bouxsein, M. L., Wan, C., Williams, B. O. and Clemens, T. L. (2007). Lifelong accumulation of bone in mice lacking Pten in osteoblasts. Proc. Natl. Acad. Sci. USA 104, 2259-2264.
33. Merriman, H. L., La, T. D., Linkhart, T. A., Mohan, S., Baylink, D. J. and Strong, D. D. (1990). Insulin-like growth factor-I and insulin-like growth factor-II induce c-fos in mouse osteoblastic cells. Calcif. Tissue Int. 46, 258-262.
34. Mukherjee, A. and Rotwein, P. (2008). Insulin-like growth factor-binding protein-5 inhibits osteoblast differentiation and skeletal growth by blocking insulin-like growth factor actions. Mol. Endocrinol. 22, 1238-1250.
35. Mukherjee, A., Dong, S. S., Clemens, T., Alvarez, J. and Serra, R. (2005). Co-ordination of TGF-beta and FGF signaling pathways in bone organ cultures. Mech. Dev. 122, 557-571.
36. Mukherjee, A., Wilson, E. M. and Rotwein, P. (2008). IGF binding protein-5 blocks skeletal muscle differentiation by inhibiting IGF actions. Mol. Endocrinol. 22, 206-215.
37. Nakae, J., Kido, Y. and Accili, D. (2001). Distinct and overlapping functions of insulin and IGF-I receptors. Endocr. Rev. 22, 818-835.
38. Niu, T. and Rosen, C. J. (2005). The insulin-like growth factor-I gene and osteoporosis: a critical appraisal. Gene 361, 38-56.
39. Noda, T., Tokuda, H., Yoshida, M., Yasuda, E., Hanai, Y., Takai, S. and Kozawa, O. (2005). Possible involvement of phosphatidylinositol 3-kinase/Akt pathway in insulin-like growth factor-I-induced alkaline phosphatase activity in osteoblasts. Horm. Metab. Res. 37, 270-274.
40. Ogata, N., Chikazu, D., Kubota, N., Terauchi, Y., Tobe, K., Azuma, Y., Ohta, T., Kadowaki, T., Nakamura, K. and Kawaguchi, H. (2000). Insulin receptor substrate-1 in osteoblast is indispensable for maintaining bone turnover. J. Clin. Invest 105, 935-943.
41. Osyczka, A. M. and Leboy, P. S. (2005). Bone morphogenetic protein regulation of early osteoblast genes in human marrow stromal cells is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase signaling. Endocrinology 146, 3428-3437.
42. Palmer, G., Bonjour, J. P. and Caverzasio, J. (1997). Expression of a newly identified phosphate transporter/retrovirus receptor in human SaOS-2 osteoblast-like cells and its regulation by insulin-like growth factor I. Endocrinology 138, 5202-5209.
43. Peng, X. D., Xu, P. Z., Chen, M. L., Hahn-Windgassen, A., Skeen, J., Jacobs, J., Sundararajan, D., Chen, W. S., Crawford, S. E., Coleman, K. G. et al. (2003). Dwarfism, impaired skin development, skeletal muscle atrophy, delayed bone development, and impeded adipogenesis in mice lacking Akt1 and Akt2. Genes Dev. 17, 1352-1365.
44. Phimphilai, M., Zhao, Z., Boules, H., Roca, H. and Franceschi, R. T. (2006). BMP signaling is required for RUNX2-dependent induction of the osteoblast phenotype. J. Bone Miner. Res. 21, 637-646.
45. Qiao, M., Shapiro, P., Kumar, R. and Passaniti, A. (2004). Insulin-like growth factor-1 regulates endogenous RUNX2 activity in endothelial cells through a phosphatidylinositol 3-kinase/ERK-dependent and Akt-independent signaling pathway. J. Biol. Chem. 279, 42709-42718.
46. Raisz, L. G. (2005). Pathogenesis of osteoporosis: concepts, conflicts, and prospects. J. Clin. Invest. 115, 3318-3325.
47. Raucci, A., Bellosta, P., Grassi, R., Basilico, C. and Mansukhani, A. (2008). Osteoblast proliferation or differentiation is regulated by relative strengths of opposing signaling pathways. J. Cell Physiol. 215, 442-451.
48. Schindeler, A., McDonald, M. M., Bokko, P. and Little, D. G. (2008). Bone remodeling during fracture repair: the cellular picture. Semin. Cell Dev. Biol. 19, 459-466.
49. Selz, T., Caverzasio, J. and Bonjour, J. P. (1989). Regulation of Na-dependent Pi transport by parathyroid hormone in osteoblast-like cells. Am. J. Physiol. 256, E93-E100.
50. Serra, C., Palacios, D., Mozzetta, C., Forcales, S. V., Morantte, I., Ripani, M., Jones, D. R., Du, K., Jhala, U. S., Simone, C. et al. (2007). Functional interdependence at the chromatin level between the MKK6/p38 and IGF1/PI3K/AKT pathways during muscle differentiation. Mol. Cell 28, 200-213.
51. Serra, R., Karaplis, A. and Sohn, P. (1999). Parathyroid hormone-related peptide (PTHrP)-dependent and -independent effects of transforming growth factor beta (TGF-beta) on endochondral bone formation. J. Cell Biol. 145, 783-794.
52. Strong, D. D., Beachler, A. L., Wergedal, J. E. and Linkhart, T. A. (1991). Insulinlike growth factor II and transforming growth factor beta regulate collagen expression in human osteoblastlike cells in vitro. J. Bone Miner. Res. 6, 15-23.
53. Strong, D. D., Merriman, H. L., Landale, E. C., Baylink, D. J. and Mohan, S. (1994). The effects of the insulin-like growth factors and transforming growth factor beta on the Jun proto-oncogene family in MC3T3-E1 cells. Calcif. Tissue Int. 55, 311-315.
54. Tureckova, J., Wilson, E. M., Cappalonga, J. L. and Rotwein, P. (2001). Insulin-like growth factor-mediated muscle differentiation: collaboration between phosphatidylinositol 3-kinase-Akt-signaling pathways and myogenin. J. Biol. Chem. 276, 39264-39270.
55. Ulici, V., Hoenselaar, K. D., Gillespie, J. R. and Beier, F. (2008). The PI3K pathway regulates endochondral bone growth through control of hypertrophic chondrocyte differentiation. BMC Dev. Biol. 8, 40.
56. Wilson, E. M. and Rotwein, P. (2007). Selective control of skeletal muscle differentiation by Akt1. J. Biol. Chem. 282, 5106-5110.
57. Wilson, E. M., Hsieh, M. M. and Rotwein, P. (2003). Autocrine growth factor signaling by insulin-like growth factor-II mediates MyoD-stimulated myocyte maturation. J. Biol. Chem. 278, 41109-41113.
58. Wozney, J. M. (1992). The bone morphogenetic protein family and osteogenesis. Mol. Reprod. Dev. 32, 160-167.
59. Zaidi, M. (2007). Skeletal remodeling in health and disease. Nat. Med. 13, 791-801.
60. Zehentner, B. K., Dony, C. and Burtscher, H. (1999). The transcription factor Sox9 is involved in BMP-2 signaling. J. Bone Miner. Res. 14, 1734-1741.
61. Zhang, M., Xuan, S., Bouxsein, M. L., von, Stechow, D., Akeno, N., Faugere, M. C., Malluche, H., Zhao, G., Rosen, C. J., Efstratiadis, A. 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.
62. Zhao, G., Monier-Faugere, M. C., Langub, M. C., Geng, Z., Nakayama, T., Pike, J. W., Chernausek, S. D., Rosen, C. J., Donahue, L. R., Malluche, H. H. et al. (2000). Targeted overexpression of insulin-like growth factor I to osteoblasts of transgenic mice: increased trabecular bone volume without increased osteoblast proliferation. Endocrinology 141, 2674-2682.