Cytoplasmic hnRNPK interacts with GSK3β and is essential for the osteoclast differentiation

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Fan, Xiaoqin ^a   Xiong, Haiting ^a   Wei, Jinmei ^a   Gao, Xuejuan ^a   Feng, Yuan ^a   Liu, Xiaohui ^a   Zhang, Gong ^a   He, Qing Yu ^a   Xu, Jiake ^b   Liu, Langxia ^a  

^a JINAN UNIVERSITY   (China)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3BETA; GSK3B PROTEIN, HUMAN; GSK3B PROTEIN, MOUSE; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN K; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LITHIUM CHLORIDE; OSTEOCLAST DIFFERENTIATION FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOSERINE; PROTEIN BINDING; PROTEIN KINASE B; TRANSCRIPTION FACTOR NFAT; TUBULIN;

ACETYLATION; ANIMAL; BIOLOGICAL MODEL; CELL DIFFERENTIATION; CELL NUCLEUS; CYTOLOGY; CYTOPLASM; DRUG EFFECTS; HEK293 CELL LINE; HUMAN; MALE; METABOLISM; MOUSE; OSTEOCLAST; PHOSPHORYLATION; PROTEIN TRANSPORT; RAW 264.7 CELL LINE;

ACETYLATION; ANIMALS; CELL DIFFERENTIATION; CELL NUCLEUS; CYTOPLASM; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; HEK293 CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN K; HUMANS; LITHIUM CHLORIDE; MALE; MICE; MODELS, BIOLOGICAL; NF-KAPPA B; NFATC TRANSCRIPTION FACTORS; OSTEOCLASTS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN BINDING; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; RANK LIGAND; RAW 264.7 CELLS; TUBULIN;

EID: 84949524758     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep17732     Document Type: Article

References (62)

1. Rea S. L., Walsh J. P., Layfield R., Ratajczak T., & Xu J. New insights into the role of sequestosome 1/p62 mutant proteins in the pathogenesis of Paget s disease of bone. Endocr Rev 34, 501-524 (2013
2. Boyce B. F., Rosenberg E., de Papp A. E., & Duong L. T. The osteoclast, bone remodelling and treatment of metabolic bone disease. Eur J Clin Invest 42, 1332-1341 (2012
3. Novack D. V., & Teitelbaum S. L. The osteoclast: friend or foe? Ann Rev Pathol 3, 457-484 (2008
4. Del Fattore A., & Teti A., & Rucci N. Osteoclast receptors and signaling. Arch Biochem Biophy 473, 147-160 (2008
5. Kikuta J., & Ishii M. Osteoclast migration, differentiation and function: novel therapeutic targets for rheumatic diseases. Rheumatology (Oxford, England) 52, 226-234 (2013
6. Kobayashi N., et al. Segregation of TRAF6-mediated signaling pathways clarifies its role in osteoclastogenesis. EMBO J 20, 1271-1280 (2001
7. Ye H., et al. Distinct molecular mechanism for initiating TRAF6 signalling. Nature 418, 443-447 (2002
8. Armstrong A. P., et al. A RANK/TRAF6-dependent signal transduction pathway is essential for osteoclast cytoskeletal organization and resorptive function. J Biol chem 277, 44347-44356 (2002
9. Georgess D., Machuca-Gayet I., Blangy A., & Jurdic P. Podosome organization drives osteoclast-mediated bone resorption. Cell Adhes Migr 8, 191-204 (2014
10. Oikawa T., et al. Tks5-dependent formation of circumferential podosomes/invadopodia mediates cell-cell fusion. J Cell Biol 197, 553-568 (2012
11. Georgess D., et al. Comparative transcriptomics reveals RhoE as a novel regulator of actin dynamics in bone-resorbing osteoclasts. Mol Biol Cell 25, 380-396 (2014
12. Frame S., & Cohen P. GSK3 takes centre stage more than 20 years after its discovery. Biochem J 359, 1-16 (2001
13. Vene R., Larghero P., Arena G., Sporn M. B., Albini A., & Tosetti F. Glycogen synthase kinase 3beta regulates cell death induced by synthetic triterpenoids. Cancer Res 68, 6987-6996 (2008
14. Jang H. D., et al. Inactivation of glycogen synthase kinase-3beta is required for osteoclast differentiation. J Biol Chem 286, 39043-39050 (2011
15. Moon J. B., et al. Akt induces osteoclast differentiation through regulating the GSK3beta/NFATc1 signaling cascade. J Immunol (Baltimore, Md: 1950) 188, 163-169 (2012
16. Matsumoto T., et al. Regulation of bone resorption and sealing zone formation in osteoclasts occurs through protein kinase B-mediated microtubule stabilization. J Bone and mineral research: the official journal of the American Society for J Bone Miner Res 28, 1191-1202 (2013
17. Gao X., Wang J. Y., Gao L. M., Yin X. F., & Liu L. Identification and analysis of glycogen synthase kinase 3 beta1 interactome. Cell Biol Int 37, 768-779 (2013
18. Michelotti E. F., Tomonaga T., Krutzsch H., & Levens D. Cellular nucleic acid binding protein regulates the CT element of the human c-myc protooncogene. J Biol Chem 270, 9494-9499 (1995
19. Michelotti E. F., Michelotti G. A., Aronsohn A. I., & Levens D. Heterogeneous nuclear ribonucleoprotein K is a transcription factor. Mol Cell Biol 16, 2350-2360 (1996
20. Miau L. H., Chang C. J., Shen B. J., Tsai W. H., & Lee S. C. Identification of heterogeneous nuclear ribonucleoprotein K (hnRNP K) as a repressor of C/EBPbeta-mediated gene activation. J Biol Chem 273, 10784-10791 (1998
21. Chen L. C., et al. The antiapoptotic protein, FLIP, is regulated by heterogeneous nuclear ribonucleoprotein K and correlates with poor overall survival of nasopharyngeal carcinoma patients. Cell Death Differ 17, 1463-1473 (2010
22. Bomsztyk K., Denisenko O., & Ostrowski J. hnRNP K: one protein multiple processes. BioEssays: news and reviews in molecular, cellular and developmental biology 26, 629-638 (2004
23. Schullery D. S., et al. Regulated interaction of protein kinase Cdelta with the heterogeneous nuclear ribonucleoprotein K protein. J Biol Chem 274, 15101-15109 (1999
24. Habelhah H., et al. ERK phosphorylation drives cytoplasmic accumulation of hnRNP-K and inhibition of mRNA translation. Nature Cell Biol 3, 325-330 (2001
25. Ostareck-Lederer A., et al. c-Src-mediated phosphorylation of hnRNP K drives translational activation of specifically silenced mRNAs. Mol Cell Biol 22, 4535-4543 (2002
26. Miyazaki T., et al. Src kinase activity is essential for osteoclast function. J Biol Chem 279, 17660-17666 (2004
27. Wolf D., et al. HIV Nef enhances Tat-mediated viral transcription through a hnRNP-K-nucleated signaling complex. Cell Host Microbe 4, 398-408 (2008
28. Chang J. W., Koike T., & Iwashima M. hnRNP-K is a nuclear target of TCR-activated ERK and required for T-cell late activation. Int Immunol 21, 1351-1361 (2009
29. Hutchins E. J., & Szaro B. G. c-Jun N-terminal kinase phosphorylation of heterogeneous nuclear ribonucleoprotein K regulates vertebrate axon outgrowth via a posttranscriptional mechanism. The Journal of neuroscience: J Neurosci 33, 14666-14680 (2013
30. Ma C., et al. Interaction between ERK and GSK3beta mediates basic fibroblast growth factor-induced apoptosis in SK-N-MC neuroblastoma cells. J Biol Chem 283, 9248-9256 (2008
31. Franzoso G., et al. Requirement for NF-kappaB in osteoclast and B-cell development. Gene Dev 11, 3482-3496 (1997
32. Iotsova V., et al. Osteopetrosis in mice lacking NF-kappaB1 and NF-kappaB2. Nature Med 3, 1285-1289 (1997
33. Aya K., et al. NF-(kappa)B-inducing kinase controls lymphocyte and osteoclast activities in inflammatory arthritis. J Clin Invest 115, 1848-1854 (2005
34. Vaira S., et al. RelB is the NF-kappaB subunit downstream of NIK responsible for osteoclast differentiation. PNAS 105, 3897-3902 (2008
35. Vaira S., et al. RelA/p65 promotes osteoclast differentiation by blocking a RANKL-induced apoptotic JNK pathway in mice. J Clin Invest 118, 2088-2097 (2008
36. Soysa N. S., et al. Inhibition of the classical NF-kappaB pathway prevents osteoclast bone-resorbing activity. J Bone Miner Metab 27, 131-139 (2009
37. Otero J. E., Dai S., Alhawagri M. A., Darwech I., & Abu-Amer Y. IKKbeta activation is sufficient for RANK-independent osteoclast differentiation and osteolysis. J Bone Miner Res 25, 1282-1294 (2010
38. Yu M., Qi X., Moreno J. L., Farber D. L., & Keegan A. D. NF-kappaB signaling participates in both RANKL- and IL-4-induced macrophage fusion: receptor cross-talk leads to alterations in NF-kappaB pathways. J Immunol (Baltimore, Md: 1950) 187, 1797-1806 (2011
39. Novack D. V. Unique personalities within the NF-kappaB family: distinct functions for p65 and RelB in the osteoclast. Adv Exp Med Biol 691, 163-167 (2011
40. Demarchi F., Bertoli C., Sandy P., & Schneider C. Glycogen synthase kinase-3 beta regulates NF-kappa B1/p105 stability. J Biol Chem 278, 39583-39590 (2003
41. Kravchenko V. V., Mathison J. C., Schwamborn K., Mercurio F., & Ulevitch R. J. IKKi/IKKepsilon plays a key role in integrating signals induced by pro-inflammatory stimuli. J Biol Chem 278, 26612-26619 (2003
42. Buss H., et al. Phosphorylation of serine 468 by GSK-3beta negatively regulates basal p65 NF-kappaB activity. J Biol Chem 279, 49571-49574 (2004
43. Buss H., et al. Constitutive and interleukin-1-inducible phosphorylation of p65 NF-{kappa}B at serine 536 is mediated by multiple protein kinases including I{kappa}B kinase (IKK)-{alpha}, IKK{beta}, IKK{epsilon}, TRAF family member-associated (TANK)-binding kinase 1 (TBK1), and an unknown kinase and couples p65 to TATA-binding protein-associated factor II31- mediated interleukin-8 transcription. J Biol Chem 279, 55633-55643 (2004
44. Viatour P., Merville M. P., & Bours V., Chariot A. Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem Sci 30, 43-52 (2005
45. Wilson W., 3rd, & Baldwin A. S. Maintenance of constitutive IkappaB kinase activity by glycogen synthase kinase-3alpha/beta in pancreatic cancer. Cancer Res 68, 8156-8163 (2008
46. Takayanagi H., et al. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev Cell 3, 889-901 (2002
47. Zhou B., et al. Regulation of the murine Nfatc1 gene by NFATc2. J Biol Chem 277, 10704-10711 (2002
48. Wada S., & Kamiya S. [Bone and bone related biochemical examinations. Bone and collagen related metabolites. Osteocalcin (OC)]. Clinical calcium 16, 1017-1021 (2006
49. Takayanagi H. The role of NFAT in osteoclast formation. Ann NY Acad Sci 1116, 227-237 (2007
50. Destaing O., et al. A novel Rho-mDia2-HDAC6 pathway controls podosome patterning through microtubule acetylation in osteoclasts. J Cell Sci 118, 2901-2911 (2005
51. McMichael B. K., Cheney R. E., & Lee B. S. Myosin X regulates sealing zone patterning in osteoclasts through linkage of podosomes and microtubules. J Biol Chem 285, 9506-9515 (2010
52. Akisaka T., Yoshida H., & Takigawa T. Differential distribution of posttranslationally modified microtubules in osteoclasts. J Histochem Cytochem 59, 630-638 (2011
53. Biosse Duplan M., et al. Microtubule dynamic instability controls podosome patterning in osteoclasts through EB1, cortactin, and Src. Mol Cell Biol 34, 16-29 (2014
54. Cervero P., Himmel M., Kruger M., & Linder S. Proteomic analysis of podosome fractions from macrophages reveals similarities to spreading initiation centres. Eur J Cell Biol 91, 908-922 (2012
55. Cremer T. J., Shah P., Cormet-Boyaka E., Valvano M. A., Butchar J. P., & Tridandapani S. Akt-mediated proinflammatory response of mononuclear phagocytes infected with Burkholderia cenocepacia occurs by a novel GSK3beta-dependent, IkappaB kinase-independent mechanism. J Immunol (Baltimore, Md: 1950) 187, 635-643 (2011
56. Spencer W., et al. Taxol selectively blocks microtubule dependent NF-kappaB activation by phorbol ester via inhibition of IkappaBalpha phosphorylation and degradation. Oncogene 18, 495-505 (1999
57. Mackenzie G. G., Keen C. L., & Oteiza P. I. Microtubules are required for NF-kappaB nuclear translocation in neuroblastoma IMR-32 cells: modulation by zinc. J Neurochem 99, 402-415 (2006
58. Legrand-Poels S., et al. Modulation of Nod2-dependent NF-kappaB signaling by the actin cytoskeleton. J Cell Sci 120, 1299-1310 (2007
59. Mediero A., Perez-Aso M., & Cronstein B. N. Activation of EPAC1/2 is essential for osteoclast formation by modulating NFkappaB nuclear translocation and actin cytoskeleton rearrangements. FASEB J 28, 4901-4913 (2014
60. Liu H., et al. Microtubule assembly affects bone mass by regulating both osteoblast and osteoclast functions: stathmin deficiency produces an osteopenic phenotype in mice. J Bone Miner Res 26, 2052-2067 (2011
61. Wang C., et al. 12-O-tetradecanoylphorbol-13-acetate (TPA) inhibits osteoclastogenesis by suppressing RANKL-induced NFkappaB activation. J Bone Miner Res 18, 2159-2168 (2003
62. Xu J., et al. Cloning, sequencing, and functional characterization of the rat homologue of receptor activator of NF-kappaB ligand. J Bone Miner Res 15, 2178-2186 (2000