Histone deacetylase 3 suppression increases PH domain and leucine-rich repeat phosphatase (Phlpp)1 expression in chondrocytes to suppress Akt signaling and matrix secretion

Journal of Biological Chemistry

Volumn 288, Issue 14, 2013, Pages 9572-9582

  Bradley, Elizabeth W ^a   Carpio, Lomeli R ^a   Westendorf, Jennifer J ^a,b  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICULAR CHONDROCYTES; CHONDROCYTE DIFFERENTIATION; CONSTITUTIVELY ACTIVES; EXTRACELLULAR MATRIX PRODUCTION; HISTONE DEACETYLASES; LEUCINE-RICH REPEATS; MATRIX GENE EXPRESSIONS; PRIMARY CHONDROCYTES;

AMINO ACIDS; ANTIBIOTICS; ENZYME ACTIVITY; GENE EXPRESSION; OSTEOBLASTS; PATHOLOGY; PHOSPHATASES; PHOSPHORYLATION; PHYSIOLOGY; SUBSTRATES; TISSUE;

BODY FLUIDS;

AGGRECAN; GLYCOSAMINOGLYCAN; HISTONE DEACETYLASE 3; LEUCINE RICH REPEAT PHOSPHATASE 1; MAMMALIAN TARGET OF RAPAMYCIN; MATRIX EXTRACELLULAR PHOSPHOGLYCOPROTEIN; OSTEOPONTIN; PHOSPHATASE; PROTEIN KINASE B; S6 KINASE; SMAD PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL SIZE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; EXTRACELLULAR MATRIX; GROWTH PLATE; HYPERTROPHY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; CARTILAGE; CHONDROCYTES; EPIGENESIS, GENETIC; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HYPERTROPHY; LEUCINE; MICE; NUCLEAR PROTEINS; OSTEOCYTES; PHOSPHOPROTEIN PHOSPHATASES; PROTO-ONCOGENE PROTEINS C-AKT; REGENERATION; SIGNAL TRANSDUCTION; SMAD PROTEINS; STEM CELLS; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA; MUS;

EID: 84875985004     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.423723     Document Type: Article

References (55)

1. Akiyama, H., Furukawa, S., Wakisaka, S., and Maeda, T. (2006) Cartducin stimulates mesenchymal chondroprogenitor cell proliferation through both extracellular signal-regulated kinase and phosphatidylinositol 3-kinase/ Akt pathways. FEBS J. 273, 2257-2263
2. Jin, E. J., Park, K. S., Bang, O. S., and Kang, S. S. (2007) Akt signaling regulates actin organization via modulation of MMP-2 activity during chondrogenesis of chick wing limb bud mesenchymal cells. J. Cell. Biochem. 102, 252-261
3. Rokutanda, S., Fujita, T., Kanatani, N., Yoshida, C. A., Komori, H., Liu, W., Mizuno, A., and Komori, T. (2009) Akt regulates skeletal development through GSK3, mTOR, and FoxOs. Dev. Biol. 328, 78-93
4. Priore, R., Dailey, L., and Basilico, C. (2006) Downregulation of Akt activity contributes to the growth arrest induced by FGF in chondrocytes. J. Cell. Physiol. 207, 800-808
5. Fukai, A., Kawamura, N., Saito, T., Oshima, Y., Ikeda, T., Kugimiya, F., Higashikawa, A., Yano, F., Ogata, N., Nakamura, K., Chung, U. I., and Kawaguchi, H. (2010) Akt1 in murine chondrocytes controls cartilage calcification during endochondral ossification under physiologic and pathologic conditions. Arthritis Rheum. 62, 826-836
6. Ikegami, D., Akiyama, H., Suzuki, A., Nakamura, T., Nakano, T., Yoshikawa, H., and Tsumaki, N. (2011) Sox9 sustains chondrocyte survival and hypertrophy in part through Pik3ca-Akt pathways. Development 138, 1507-1519
7. Price, J., Zaidi, A. K., Bohensky, J., Srinivas, V., Shapiro, I. M., and Ali, H. (2010) Akt-1 mediates survival of chondrocytes from endoplasmic reticulum-induced stress. J. Cell. Physiol. 222, 502-508
8. Carver, B. S., Chapinski, C., Wongvipat, J., Hieronymus, H., Chen, Y., Chandarlapaty, S., Arora, V. K., Le, C., Koutcher, J., Scher, H., Scardino, P. T., Rosen, N., and Sawyers, C. L. (2011) Reciprocal feedback regulation of PI3K and androgen receptor signaling in PTEN-deficient prostate cancer. Cancer Cell 19, 575-586
9. Liu, J., Weiss, H. L., Rychahou, P., Jackson, L. N., Evers, B. M., and Gao, T. (2009) Loss of PHLPP expression in colon cancer: role in proliferation and tumorigenesis. Oncogene 28, 994-1004
10. Mulholland, D. J., Tran, L. M., Li, Y., Cai, H., Morim, A., Wang, S., Plaisier, S., Garraway, I. P., Huang, J., Graeber, T. G., and Wu, H. (2011) Cell autonomous role of PTEN in regulating castration-resistant prostate cancer growth. Cancer Cell 19, 792-804
11. Brognard, J., Sierecki, E., Gao, T., and Newton, A. C. (2007) PHLPP and a second isoform, PHLPP2, differentially attenuate the amplitude of Akt signaling by regulating distinct Akt isoforms. Mol. Cell 25, 917-931
12. Masubuchi, S., Gao, T., O'Neill, A., Eckel-Mahan, K., Newton, A. C., and Sassone-Corsi, P. (2010) Protein phosphatase PHLPP1 controls the lightinduced resetting of the circadian clock. Proc. Natl. Acad. Sci. U.S.A. 107, 1642-1647
13. McGee-Lawrence, M. E., and Westendorf, J. J. (2011) Histone deacetylases in skeletal development and bone mass maintenance. Gene 474, 1-11
14. Westendorf, J. J. (2007) Histone deacetylases in control of skeletogenesis. J. Cell. Biochem. 102, 332-340
15. Bhaskara, S., Chyla, B. J., Amann, J. M., Knutson, S. K., Cortez, D., Sun, Z. W., and Hiebert, S. W. (2008) Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Mol. Cell 30, 61-72
16. Montgomery, R. L., Potthoff, M. J., Haberland, M., Qi, X., Matsuzaki, S., Humphries, K. M., Richardson, J. A., Bassel-Duby, R., and Olson, E. N. (2008) Maintenance of cardiac energy metabolism by histone deacetylase 3 in mice. J. Clin. Invest. 118, 3588-3597
17. Sun, Z., Singh, N., Mullican, S. E., Everett, L. J., Li, L., Yuan, L., Liu, X., Epstein, J. A., and Lazar, M. A. (2011) Diet-induced lethality due to deletion of the Hdac3 gene in heart and skeletal muscle. J. Biol. Chem. 286, 33301-33309
18. Knutson, S. K., Chyla, B. J., Amann, J. M., Bhaskara, S., Huppert, S. S., and Hiebert, S. W. (2008) Liver-specific deletion of histone deacetylase 3 disrupts metabolic transcriptional networks. EMBO J. 27, 1017-1028
19. Razidlo, D. F., Whitney, T. J., Casper, M. E., McGee-Lawrence, M. E., Stensgard, B. A., Li, X., Secreto, F. J., Knutson, S. K., Hiebert, S. W., and Westendorf, J. J. (2010) Histone deacetylase 3 depletion in osteo/ chondroprogenitor cells decreases bone density and increases marrow fat. PloS One 5, e11492
20. Vega, R. B., Matsuda, K., Oh, J., Barbosa, A. C., Yang, X., Meadows, E., McAnally, J., Pomajzl, C., Shelton, J. M., Richardson, J. A., Karsenty, G., and Olson, E. N. (2004) Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 119, 555-566
21. Correa, D., Hesse, E., Seriwatanachai, D., Kiviranta, R., Saito, H., Yamana, K., Neff, L., Atfi, A., Coillard, L., Sitara, D., Maeda, Y., Warming, S., Jenkins, N. A., Copeland, N. G., Horne, W. C., Lanske, B., and Baron, R. (2010) Zfp521 is a target gene and key effector of parathyroid hormone-related peptide signaling in growth plate chondrocytes. Dev. Cell 19, 533-546
22. Zeng, L., Kempf, H., Murtaugh, L. C., Sato, M. E., and Lassar, A. B. (2002) Shh establishes an Nkx3.2/Sox9 autoregulatory loop that is maintained by BMPsignals to induce somitic chondrogenesis. Genes Dev. 16, 1990-2005
23. Lemon, D. D., Horn, T. R., Cavasin, M. A., Jeong, M. Y., Haubold, K. W., Long, C. S., Irwin, D. C., McCune, S. A., Chung, E., Leinwand, L. A., and McKinsey, T. A. (2011) Cardiac HDAC6 catalytic activity is induced in response to chronic hypertension. J. Mol. Cell Cardiol. 51, 41-50
24. Rodda, S. J., and McMahon, A. P. (2006) Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 133, 3231-3244
25. Gosset, M., Berenbaum, F., Thirion, S., and Jacques, C. (2008) Primary culture and phenotyping of murine chondrocytes. Nat. Protoc. 3, 1253-1260
26. Soung do, Y., Dong, Y., Wang, Y., Zuscik, M. J., Schwarz, E. M., O'Keefe, R. J., and Drissi, H. (2007) Runx3/AML2/Cbfa3 regulates early and late chondrocyte differentiation. J. Bone Miner. Res. 22, 1260-1270
27. Bradley, E. W., and Drissi, M. H. (2010) WNT5A regulates chondrocyte differentiation through differential use of the CaN/NFAT and IKK/NF-κB pathways. Mol. Endocrinol. 24, 1581-1593
28. Gao, T., Furnari, F., and Newton, A. C. (2005) PHLPP: a phosphatase that directly dephosphorylates Akt, promotes apoptosis, and suppresses tumor growth. Mol. Cell 18, 13-24
29. Zhang, H., Pan, Y., Zheng, L., Choe, C., Lindgren, B., Jensen, E. D., Westendorf, J. J., Cheng, L., and Huang, H. (2011) FOXO1 inhibits Runx2 transcriptional activity and prostate cancer cell migration and invasion. Cancer Res. 71, 3257-3267
30. Lambert, J. R., and Nordeen, S. K. (2001) Analysis of steroid hormone-induced histone acetylation by chromatin immunoprecipitation assay. Methods Mol. Biol. 176, 273-281
31. Karp, S. J., Schipani, E., St-Jacques, B., Hunzelman, J., Kronenberg, H., and McMahon, A. P. (2000) Indian hedgehog coordinates endochondral bone growth and morphogenesis via parathyroid hormone related-protein-dependent and -independent pathways. Development 127, 543-548
32. Pullen, N., and Thomas, G. (1997) The modular phosphorylation and activation of p70s6k. FEBS Lett. 410, 78-82
33. Fang, Y., Vilella-Bach, M., Bachmann, R., Flanigan, A., and Chen, J. (2001) Phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science 294, 1942-1945
34. Sabers, C. J., Martin, M. M., Brunn, G. J., Williams, J. M., Dumont, F. J., Wiederrecht, G., and Abraham, R. T. (1995) Isolation of a protein target of the FKBP12-rapamycin complex in mammalian cells. J. Biol. Chem. 270, 815-822
35. Brown, E. J., Albers, M. W., Shin, T. B., Ichikawa, K., Keith, C. T., Lane, W. S., and Schreiber, S. L. (1994) A mammalian protein targeted by G1- arresting rapamycin-receptor complex. Nature 369, 756-758
36. Navé, B. T., Ouwens, M., Withers, D. J., Alessi, D. R., and Shepherd, P. R. (1999) Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem. J. 344, 427-431
37. Patterson, S. J., Han, J. M., Garcia, R., Assi, K., Gao, T., O'Neill, A., Newton, A. C., and Levings, M. K. (2011) Cutting edge: PHLPP regulates the development, function, and molecular signaling pathways of regulatory T cells. J. Immunol. 186, 5533-5537
38. Haberland, M., Montgomery, R. L., and Olson, E. N. (2009) The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 10, 32-42
39. Chen, W. P., Bao, J. P., Hu, P. F., Feng, J., and Wu, L. D. (2010) Alleviation of osteoarthritis by Trichostatin A, a histone deacetylase inhibitor, in experimental osteoarthritis. Mol. Biol. Rep. 37, 3967-3972
40. Joosten, L. A., Leoni, F., Meghji, S., and Mascagni, P. (2011) Inhibition of HDAC activity by ITF2357 ameliorates joint inflammation and prevents cartilage and bone destruction in experimental arthritis. Mol. Med. 17, 391-396
41. Nasu, Y., Nishida, K., Miyazawa, S., Komiyama, T., Kadota, Y., Abe, N., Yoshida, A., Hirohata, S., Ohtsuka, A., and Ozaki, T. (2008) Trichostatin A, a histone deacetylase inhibitor, suppresses synovial inflammation and subsequent cartilage destruction in a collagen antibody-induced arthritis mouse model. Osteoarthritis Cartilage 16, 723-732
42. Bradley, E. W., McGee-Lawrence, M. E., and Westendorf, J. J. (2011) Hdac-mediated control of endochondral and intramembranous ossification. Crit. Rev. Eukaryot. Gene Expr. 21, 101-113
43. Fischle, W., Dequiedt, F., Hendzel, M. J., Guenther, M. G., Lazar, M. A., Voelter, W., and Verdin, E. (2002) Enzymatic activity associated with class II HDACs is dependent on a multiprotein complex containing HDAC3 and SMRT/N-CoR. Mol. Cell 9, 45-57
44. Alvarez-Garcia, O., Carbajo-Pérez, E., Garcia, E., Gil, H., Molinos, I., Rodriguez, J., Ordoñez, F. A., and Santos, F. (2007) Rapamycin retards growth and causes marked alterations in the growth plate of young rats. Pediatr. Nephrol. 22, 954-961
45. Oh, C. D., Kim, S. J., Ju, J. W., Song, W. K., Kim, J. H., Yoo, Y. J., and Chun, J. S. (2001) Immunosuppressant rapamycin inhibits protein kinase C α and p38 mitogen-activated protein kinase leading to the inhibition of chondrogenesis. Eur. J. Pharmacol. 427, 175-185
46. Phornphutkul, C., Wu, K. Y., Auyeung, V., Chen, Q., and Gruppuso, P. A. (2008) mTOR signaling contributes to chondrocyte differentiation. Dev. Dyn. 237, 702-712
47. Starkman, B. G., Cravero, J. D., Delcarlo, M., and Loeser, R. F. (2005) IGF-I stimulation of proteoglycan synthesis by chondrocytes requires activation of the PI 3-kinase pathway but not ERK MAPK. Biochem. J. 389, 723-729
48. Trivedi, C. M., Luo, Y., Yin, Z., Zhang, M., Zhu, W., Wang, T., Floss, T., Goettlicher, M., Noppinger, P. R., Wurst, W., Ferrari, V. A., Abrams, C. S., Gruber, P. J., and Epstein, J. A. (2007) Hdac2 regulates the cardiac hypertrophic response by modulating Gsk3 β activity. Nat. Med. 13, 324-331
49. Chen, C. S., Weng, S. C., Tseng, P. H., and Lin, H. P. (2005) Histone acetylation-independent effect of histone deacetylase inhibitors on Akt through the reshuffling of protein phosphatase 1 complexes. J. Biol. Chem. 280, 38879-38887
50. Gupta, M., Ansell, S. M., Novak, A. J., Kumar, S., Kaufmann, S. H., and Witzig, T. E. (2009) Inhibition of histone deacetylase overcomes rapamycin- mediated resistance in diffuse large B-cell lymphoma by inhibiting Akt signaling through mTORC2. Blood 114, 2926-2935
51. Martin, M., Potente, M., Janssens, V., Vertommen, D., Twizere, J. C., Rider, M. H., Goris, J., Dimmeler, S., Kettmann, R., and Dequiedt, F. (2008) Protein phosphatase 2A controls the activity of histone deacetylase 7 during T cell apoptosis and angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 105, 4727-4732
52. Kaback, L. A., Soung do, Y., Naik, A., Smith, N., Schwarz, E. M., O'Keefe, R. J., and Drissi, H. (2008) Osterix/Sp7 regulates mesenchymal stem cell mediated endochondral ossification. J. Cell. Physiol. 214, 173-182
53. Nakashima, K., Zhou, X., Kunkel, G., Zhang, Z., Deng, J. M., Behringer, R. R., and de Crombrugghe, B. (2002) The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 108, 17-29
54. Xiong, J., Onal, M., Jilka, R. L., Weinstein, R. S., Manolagas, S. C., and O'Brien, C. A. (2011) Matrix-embedded cells control osteoclast formation. Nat. Med. 17, 1235-1241
55. McGee-Lawrence, M. E., Bradley, E. W., Dudakovic, A., Carlson, S. W., Ryan, Z. C., Kumar, R., Dadsetan, M., Yaszemski, M. J., Chen, Q., An, K. N., and Westendorf, J. J. (2013) Histone deacetylase 3 is required for maintenance of bone mass during aging. Bone 52, 296-307