The p85α Subunit of Class I_A Phosphatidylinositol 3-Kinase Regulates the Expression of Multiple Genes Involved in Osteoclast Maturation and Migration

REFERENCES

• Abu-Amer, Y., F. P. Ross, J. Edwards, and S. L. Teitelbaum. 1997. Lipopolysaccharide-stimulated osteoclastogenesis is mediated by tumor necrosis factor via its P55 receptor. J. Clin. Investig. 100:1557–1565.
   PubMedGoogle Scholar
• Alatalo, S. L., J. M. Halleen, T. A. Hentunen, J. Monkkonen, and H. K. Vaananen. 2000. Rapid screening method for osteoclast differentiation in vitro that measures tartrate-resistant acid phosphatase 5b activity secreted into the culture medium. Clin. Chem. 46:1751–1754.
   PubMed Web of Science ®Google Scholar
• Alatalo, S. L., K. K. Ivaska, S. G. Waguespack, M. J. Econs, H. K. Vaananen, and J. M. Halleen. 2004. Osteoclast-derived serum tartrate-resistant acid phosphatase 5b in Albers-Schonberg disease (type II autosomal dominant osteopetrosis). Clin. Chem. 50:883–890.
   PubMedGoogle Scholar
• Alatalo, S. L., Z. Peng, A. J. Janckila, H. Kaija, P. Vihko, H. K. Vaananen, and J. M. Halleen. 2003. A novel immunoassay for the determination of tartrate-resistant acid phosphatase 5b from rat serum. J. Bone Miner. Res. 18:134–139.
   PubMed Web of Science ®Google Scholar
• Bar-Sagi, D., and A. Hall. 2000. Ras and Rho GTPases: a family reunion. Cell 103:227–238.
   PubMed Web of Science ®Google Scholar
• Birkedal-Hansen, H. 1993. Role of matrix metalloproteinases in human periodontal diseases. J. Periodontol. 64:474–484.
   PubMed Web of Science ®Google Scholar
• Bolstad, B. M., R. A. Irizarry, M. Astrand, and T. P. Speed. 2003. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185–193.
   PubMed Web of Science ®Google Scholar
• Boyle, W. J., W. S. Simonet, and D. L. Lacey. 2003. Osteoclast differentiation and activation. Nature 423:337–342.
   PubMed Web of Science ®Google Scholar
• Burow, M. E., C. B. Weldon, L. I. Melnik, B. N. Duong, B. M. Collins-Burow, B. S. Beckman, and J. A. McLachlan. 2000. PI3-K/AKT regulation of NF-κB signaling events in suppression of TNF-induced apoptosis. Biochem. Biophys. Res. Commun. 271:342–345.
   PubMed Web of Science ®Google Scholar
• Cenci, S., M. N. Weitzmann, M. A. Gentile, M. C. Aisa, and R. Pacifici. 2000. M-CSF neutralization and egr-1 deficiency prevent ovariectomy-induced bone loss. J. Clin. Investig. 105:1279–1287.
   PubMedGoogle Scholar
• Chu, P., T. Y. Chao, Y. F. Lin, A. J. Janckila, and L. T. Yam. 2003. Correlation between histomorphometric parameters of bone resorption and serum type 5b tartrate-resistant acid phosphatase in uremic patients on maintenance hemodialysis. Am. J. Kidney Dis. 41:1052–1059.
   PubMed Web of Science ®Google Scholar
• Destaing, O., F. Saltel, J. C. Geminard, P. Jurdic, and F. Bard. 2003. Podosomes display actin turnover and dynamic self-organization in osteoclasts expressing actin-green fluorescent protein. Mol. Biol. Cell 14:407–416.
   PubMed Web of Science ®Google Scholar
• Dudek, H., S. R. Datta, T. F. Franke, M. J. Birnbaum, R. Yao, G. M. Cooper, R. A. Segal, D. R. Kaplan, and M. E. Greenberg. 1997. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275:661–665.
   PubMed Web of Science ®Google Scholar
• Duran, A., M. Serrano, M. Leitges, J. M. Flores, S. Picard, J. P. Brown, J. Moscat, and M. T. Diaz-Meco. 2004. The atypical PKC-interacting protein p62 is an important mediator of RANK-activated osteoclastogenesis. Dev. Cell 6:303–309.
   PubMed Web of Science ®Google Scholar
• Faccio, R., S. Takeshita, A. Zallone, F. P. Ross, and S. L. Teitelbaum. 2003. c-Fms and the αvβ3 integrin collaborate during osteoclast differentiation. J. Clin. Investig. 111:749–758.
   PubMed Web of Science ®Google Scholar
• Faccio, R., S. L. Teitelbaum, K. Fujikawa, J. Chappel, A. Zallone, V. L. Tybulewicz, F. P. Ross, and W. Swat. 2005. Vav3 regulates osteoclast function and bone mass. Nat. Med. 11:284–290.
   PubMedGoogle Scholar
• Faccio, R., W. Zou, G. Colaianni, S. L. Teitelbaum, and F. P. Ross. 2003. High dose M-CSF partially rescues the Dap12−/− osteoclast phenotype. J. Cell Biochem. 90:871–883.
   PubMed Web of Science ®Google Scholar
• Fuller, K., J. M. Lean, K. E. Bayley, M. R. Wani, and T. J. Chambers. 2000. A role for TGFbeta(1) in osteoclast differentiation and survival. J. Cell Sci. 113:2445–2453.
   PubMed Web of Science ®Google Scholar
• Gelb, B. D., G. P. Shi, H. A. Chapman, and R. J. Desnick. 1996. Pycnodysostosis, a lysosomal disease caused by cathepsin K deficiency. Science 273:1236–1238.
   PubMed Web of Science ®Google Scholar
• Golden, L. H., and K. L. Insogna. 2004. The expanding role of PI3-kinase in bone. Bone 34:3–12.
   PubMedGoogle Scholar
• Hershey, C. L., and D. E. Fisher. 2004. Mitf and Tfe3: members of a b-HLH-ZIP transcription factor family essential for osteoclast development and function. Bone 34:689–696.
   PubMedGoogle Scholar
• Hsu, H., D. L. Lacey, C. R. Dunstan, I. Solovyev, A. Colombero, E. Timms, H. L. Tan, G. Elliott, M. J. Kelley, I. Sarosi, L. Wang, X. Z. Xia, R. Elliott, L. Chiu, T. Black, S. Scully, C. Capparelli, S. Morony, G. Shimamoto, M. B. Bass, and W. J. Boyle. 1999. Tumor necrosis factor receptor family member RANK mediates osteoclast differentiation and activation induced by osteoprotegerin ligand. Proc. Natl. Acad. Sci. USA 96:3540–3545.
   PubMed Web of Science ®Google Scholar
• Kaifu, T., J. Nakahara, M. Inui, K. Mishima, T. Momiyama, M. Kaji, A. Sugahara, H. Koito, A. Ujike-Asai, A. Nakamura, K. Kanazawa, K. Tan-Takeuchi, K. Iwasaki, W. M. Yokoyama, A. Kudo, M. Fujiwara, H. Asou, and T. Takai. 2003. Osteopetrosis and thalamic hypomyelinosis with synaptic degeneration in DAP12-deficient mice. J. Clin. Investig. 111:323–332.
   PubMed Web of Science ®Google Scholar
• Kaneda, T., T. Nojima, M. Nakagawa, A. Ogasawara, H. Kaneko, T. Sato, H. Mano, M. Kumegawa, and Y. Hakeda. 2000. Endogenous production of TGF-β is essential for osteoclastogenesis induced by a combination of receptor activator of NF-κB ligand and macrophage-colony-stimulating factor. J. Immunol. 165:4254–4263.
   PubMed Web of Science ®Google Scholar
• Kapeller, R., K. V. Prasad, O. Janssen, W. Hou, B. S. Schaffhausen, C. E. Rudd, and L. C. Cantley. 1994. Identification of two SH3-binding motifs in the regulatory subunit of phosphatidylinositol 3-kinase. J. Biol. Chem. 269:1927–1933.
   PubMed Web of Science ®Google Scholar
• Katso, R., K. Okkenhaug, K. Ahmadi, S. White, J. Timms, and M. D. Waterfield. 2001. Cellular function of phosphoinositide 3-kinases: implications for development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 17:615–675.
   PubMed Web of Science ®Google Scholar
• Kawaida, R., T. Ohtsuka, J. Okutsu, T. Takahashi, Y. Kadono, H. Oda, A. Hikita, K. Nakamura, S. Tanaka, and H. Furukawa. 2003. Jun dimerization protein 2 (JDP2), a member of the AP-1 family of transcription factor, mediates osteoclast differentiation induced by RANKL. J. Exp. Med. 197:1029–1035.
   PubMedGoogle Scholar
• Keffer, J., L. Probert, H. Cazlaris, S. Georgopoulos, E. Kaslaris, D. Kioussis, and G. Kollias. 1991. Transgenic mice expressing human tumour necrosis factor: a predictive genetic model of arthritis. EMBO J. 10:4025–4031.
   PubMed Web of Science ®Google Scholar
• Kudo, O., A. Sabokbar, A. Pocock, I. Itonaga, and N. A. Athanasou. 2002. Isolation of human osteoclasts formed in vitro: hormonal effects on the bone-resorbing activity of human osteoclasts. Calcif. Tissue Int. 71:539–546.
   PubMed Web of Science ®Google Scholar
• Lacey, D. L., E. Timms, H. L. Tan, M. J. Kelley, C. R. Dunstan, T. Burgess, R. Elliott, A. Colombero, G. Elliott, S. Scully, H. Hsu, J. Sullivan, N. Hawkins, E. Davy, C. Capparelli, A. Eli, Y. X. Qian, S. Kaufman, I. Sarosi, V. Shalhoub, G. Senaldi, J. Guo, J. Delaney, and W. J. Boyle. 1998. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93:165–176.
   PubMed Web of Science ®Google Scholar
• Lam, J., S. Takeshita, J. E. Barker, O. Kanagawa, F. P. Ross, and S. L. Teitelbaum. 2000. TNF-α induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J. Clin. Investig. 106:1481–1488.
   PubMed Web of Science ®Google Scholar
• Li, C. Y., K. J. Jepsen, R. J. Majeska, J. Zhang, R. Ni, B. D. Gelb, and M. B. Schaffler. 2006. Mice lacking cathepsin K maintain bone remodeling but develop bone fragility despite high bone mass. J. Bone Miner. Res. 21:865–875.
   PubMed Web of Science ®Google Scholar
• McHugh, K. P., K. Hodivala-Dilke, M. H. Zheng, N. Namba, J. Lam, D. Novack, X. Feng, F. P. Ross, R. O. Hynes, and S. L. Teitelbaum. 2000. Mice lacking beta3 integrins are osteosclerotic because of dysfunctional osteoclasts. J. Clin. Investig. 105:433–440.
   PubMed Web of Science ®Google Scholar
• Munugalavadla, V., J. Borneo, D. A. Ingram, and R. Kapur. 2005. p85α subunit of class IA PI-3 kinase is crucial for macrophage growth and migration. Blood 106:103–109.
   PubMedGoogle Scholar
• Nakagawa, N., M. Kinosaki, K. Yamaguchi, N. Shima, H. Yasuda, K. Yano, T. Morinaga, and K. Higashio. 1998. RANK is the essential signaling receptor for osteoclast differentiation factor in osteoclastogenesis. Biochem. Biophys. Res. Commun. 253:395–400.
   PubMed Web of Science ®Google Scholar
• Nakamura, I., N. Takahashi, T. Sasaki, S. Tanaka, N. Udagawa, H. Murakami, K. Kimura, Y. Kabuyama, T. Kurokawa, T. Suda, et al. 1995. Wortmannin, a specific inhibitor of phosphatidylinositol-3 kinase, blocks osteoclastic bone resorption. FEBS Lett. 361:79–84.
   PubMed Web of Science ®Google Scholar
• Novack, D. V., L. Yin, A. Hagen-Stapleton, R. D. Schreiber, D. V. Goeddel, F. P. Ross, and S. L. Teitelbaum. 2003. The IκB function of NF-κB2 p100 controls stimulated osteoclastogenesis. J. Exp. Med. 198:771–781.
   PubMedGoogle Scholar
• Palacio, S., and R. Felix. 2001. The role of phosphoinositide 3-kinase in spreading osteoclasts induced by colony-stimulating factor-1. Eur. J. Endocrinol. 144:431–440.
   PubMedGoogle Scholar
• Pilkington, M. F., S. M. Sims, and S. J. Dixon. 1998. Wortmannin inhibits spreading and chemotaxis of rat osteoclasts in vitro. J. Bone Miner. Res. 13:688–694.
   PubMedGoogle Scholar
• Razzouk, S., M. Lieberherr, and G. Cournot. 1999. Rac-GTPase, osteoclast cytoskeleton and bone resorption. Eur. J. Cell Biol. 78:249–255.
   PubMedGoogle Scholar
• Reedijk, M., X. Liu, P. van der Geer, K. Letwin, M. D. Waterfield, T. Hunter, and T. Pawson. 1992. Tyr721 regulates specific binding of the CSF-1 receptor kinase insert to PI 3′-kinase SH2 domains: a model for SH2-mediated receptor-target interactions. EMBO J. 11:1365–1372.
   PubMed Web of Science ®Google Scholar
• Shin, B. C., M. Suzuki, K. Inukai, M. Anai, T. Asano, and K. Takata. 1998. Multiple isoforms of the regulatory subunit for phosphatidylinositol 3-kinase (PI3-kinase) are expressed in neurons in the rat brain. Biochem. Biophys. Res. Commun. 246:313–319.
   PubMedGoogle Scholar
• Stambolic, V., T. W. Mak, and J. R. Woodgett. 1999. Modulation of cellular apoptotic potential: contributions to oncogenesis. Oncogene 18:6094–6103.
   PubMed Web of Science ®Google Scholar
• Suda, T., E. Jimi, I. Nakamura, and N. Takahashi. 1997. Role of 1 α,25-dihydroxyvitamin D3 in osteoclast differentiation and function. Methods Enzymol. 282:223–235.
   PubMedGoogle Scholar
• Sun, Y., K. G. Buki, O. Ettala, J. P. Vaaraniemi, and H. K. Vaananen. 2005. Possible role of direct Rac1-Rab7 interaction in ruffled border formation of osteoclasts. J. Biol. Chem. 280:32356–32361.
   PubMedGoogle Scholar
• Suzuki, H., Y. Terauchi, M. Fujiwara, S. Aizawa, Y. Yazaki, T. Kadowaki, and S. Koyasu. 1999. Xid-like immunodeficiency in mice with disruption of the p85α subunit of phosphoinositide 3-kinase. Science 283:390–392.
   PubMed Web of Science ®Google Scholar
• Takeshita, S., N. Namba, J. J. Zhao, Y. Jiang, H. K. Genant, M. J. Silva, M. D. Brodt, C. D. Helgason, J. Kalesnikoff, M. J. Rauh, R. K. Humphries, G. Krystal, S. L. Teitelbaum, and F. P. Ross. 2002. SHIP-deficient mice are severely osteoporotic due to increased numbers of hyper-resorptive osteoclasts. Nat. Med. 8:943–949.
   PubMed Web of Science ®Google Scholar
• Tan, B. L., M. N. Yazicioglu, D. Ingram, J. McCarthy, J. Borneo, D. A. Williams, and R. Kapur. 2003. Genetic evidence for convergence of c-Kit- and α4 integrin-mediated signals on class IA PI-3kinase and the Rac pathway in regulating integrin-directed migration in mast cells. Blood 101:4725–4732.
   PubMedGoogle Scholar
• Tanaka, S., I. Nakamura, J. Inoue, H. Oda, and K. Nakamura. 2003. Signal transduction pathways regulating osteoclast differentiation and function. J. Bone Miner. Metab. 21:123–133.
   PubMed Web of Science ®Google Scholar
• Terauchi, Y., Y. Tsuji, S. Satoh, H. Minoura, K. Murakami, A. Okuno, K. Inukai, T. Asano, Y. Kaburagi, K. Ueki, H. Nakajima, T. Hanafusa, Y. Matsuzawa, H. Sekihara, Y. Yin, J. C. Barrett, H. Oda, T. Ishikawa, Y. Akanuma, I. Komuro, M. Suzuki, K. Yamamura, T. Kodama, H. Suzuki, T. Kadowaki, et al. 1999. Increased insulin sensitivity and hypoglycaemia in mice lacking the p85 alpha subunit of phosphoinositide 3-kinase. Nat. Genet. 21:230–235.
   PubMed Web of Science ®Google Scholar
• Thesingh, C. W., and J. P. Scherft. 1985. Fusion disability of embryonic osteoclast precursor cells and macrophages in the microphthalmic osteopetrotic mouse. Bone 6:43–52.
   PubMedGoogle Scholar
• Tondravi, M. M., S. R. McKercher, K. Anderson, J. M. Erdmann, M. Quiroz, R. Maki, and S. L. Teitelbaum. 1997. Osteopetrosis in mice lacking haematopoietic transcription factor PU.1. Nature 386:81–84.
   PubMed Web of Science ®Google Scholar
• Vanhaesebroeck, B., S. J. Leevers, K. Ahmadi, J. Timms, R. Katso, P. C. Driscoll, R. Woscholski, P. J. Parker, and M. D. Waterfield. 2001. Synthesis and function of 3-phosphorylated inositol lipids. Annu. Rev. Biochem. 70:535–602.
   PubMed Web of Science ®Google Scholar
• Vanhaesebroeck, B., S. J. Leevers, G. Panayotou, and M. D. Waterfield. 1997. Phosphoinositide 3-kinases: a conserved family of signal transducers. Trends Biochem. Sci. 22:267–272.
   PubMed Web of Science ®Google Scholar
• Wada, T., T. Nakashima, A. J. Oliveira-dos-Santos, J. Gasser, H. Hara, G. Schett, and J. M. Penninger. 2005. The molecular scaffold Gab2 is a crucial component of RANK signaling and osteoclastogenesis. Nat. Med. 11:394–399.
   PubMed Web of Science ®Google Scholar
• Weilbaecher, K. N., G. Motyckova, W. E. Huber, C. M. Takemoto, T. J. Hemesath, Y. Xu, C. L. Hershey, N. R. Dowland, A. G. Wells, and D. E. Fisher. 2001. Linkage of M-CSF signaling to Mitf, TFE3, and the osteoclast defect in Mitf(mi/mi) mice. Mol. Cell 8:749–758.
   PubMedGoogle Scholar
• Williams, D. A., W. Tao, F. Yang, C. Kim, Y. Gu, P. Mansfield, J. E. Levine, B. Petryniak, C. W. Derrow, C. Harris, B. Jia, Y. Zheng, D. R. Ambruso, J. B. Lowe, S. J. Atkinson, M. C. Dinauer, and L. Boxer. 2000. Dominant negative mutation of the hematopoietic-specific Rho GTPase, Rac2, is associated with a human phagocyte immunodeficiency. Blood 96:1646–1654.
   PubMed Web of Science ®Google Scholar
• Wu, Z., and R. A. Irizarry. 2004. Preprocessing of oligonucleotide array data. Nat. Biotechnol. 22:656-658, author reply 658.
   PubMedGoogle Scholar
• Wymann, M. P., M. Zvelebil, and M. Laffargue. 2003. Phosphoinositide 3-kinase signalling—which way to target? Trends Pharmacol. Sci. 24:366–376.
   PubMed Web of Science ®Google Scholar
• Yang, F. C., S. J. Atkinson, Y. Gu, J. B. Borneo, A. W. Roberts, Y. Zheng, J. Pennington, and D. A. Williams. 2001. Rac and Cdc42 GTPases control hematopoietic stem cell shape, adhesion, migration, and mobilization. Proc. Natl. Acad. Sci. USA 98:5614–5618.
   PubMedGoogle Scholar
• Yang, F. C., S. Chen, A. G. Robling, X. Yu, T. D. Nebesio, J. Yan, T. Morgan, X. Li, J. Yuan, J. Hock, D. A. Ingram, and D. W. Clapp. 2006. Hyperactivation of p21ras and PI3K cooperate to alter murine and human neurofibromatosis type 1-haploinsufficient osteoclast functions. J. Clin. Investig. 116:2880–2891.
   PubMedGoogle Scholar
• Yang, F. C., R. Kapur, A. J. King, W. Tao, C. Kim, J. Borneo, R. Breese, M. Marshall, M. C. Dinauer, and D. A. Williams. 2000. Rac2 stimulates Akt activation affecting BAD/Bcl-XL expression while mediating survival and actin function in primary mast cells. Immunity 12:557–568.
   PubMed Web of Science ®Google Scholar
• Yasuda, H., N. Shima, N. Nakagawa, K. Yamaguchi, M. Kinosaki, S. Mochizuki, A. Tomoyasu, K. Yano, M. Goto, A. Murakami, E. Tsuda, T. Morinaga, K. Higashio, N. Udagawa, N. Takahashi, and T. Suda. 1998. Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc. Natl. Acad. Sci. USA 95:3597–3602.
   PubMed Web of Science ®Google Scholar
• Yoshida, H., S. Hayashi, T. Kunisada, M. Ogawa, S. Nishikawa, H. Okamura, T. Sudo, L. D. Shultz, and S. Nishikawa. 1990. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 345:442–444.
   PubMed Web of Science ®Google Scholar