The Ric-8B gene is highly expressed in proliferating preosteoblastic cells and downregulated during osteoblast differentiation in a SWI/SNF- and C/EBPβ-mediated manner

Molecular and Cellular Biology

Volumn 31, Issue 14, 2011, Pages 2997-3008

  Grandy, Rodrigo ^a,b   Sepulveda, Hugo ^a   Aguilar, Rodrigo ^a   Pihan, Philippe ^a   Henriquez, Berta ^a   Olate, Juan ^b   Montecino, Martin ^a  

^a UNIVERSIDAD ANDRÉS BELLO   (Chile)

^b UNIVERSITY OF CONCEPCIÓN   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

BRG1 PROTEIN; BRM PROTEIN; CCAAT ENHANCER BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN RIC 8B; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SNF; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CATALYSIS; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; HUMAN; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; RAT; REGULATORY SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL DIFFERENTIATION; CELL LINE; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA HELICASES; DOWN-REGULATION; GENE EXPRESSION REGULATION; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MICE; NUCLEAR PROTEINS; OSTEOBLASTS; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS;

MAMMALIA;

EID: 79960354056     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05096-11     Document Type: Article

References (53)

1. Bundy, L. M., and L. Sealy. 2003. CCAAT/enhancer binding protein beta (C/EBPβ)-2 transforms normal mammary epithelial cells and induces epithelial to mesenchymal transition in culture. Oncogene 22:869-883.
2. Calkhoven, C. F., C. Muller, and A. Leutz. 2000. Translational control of C/EBPα and C/EBPβ isoform expression. Genes Dev. 14:1920-1932.
3. Cruzat, F., et al. 2009. SWI/SNF-independent nuclease hypersensitivity and an increased level of histone acetylation at the P1 promoter accompany active transcription of the bone master gene Runx2. Biochemistry 48:7287-7295.
4. Dai, Y., D. Ngo, J. Jacob, L. W. Forman, and D. V. Faller. 2008. Prohibitin and the SWI/SNF ATPase subunit BRG1 are required for effective androgen antagonist-mediated transcriptional repression of androgen receptor-regulated genes. Carcinogenesis 29:1725-1733.
5. David, N. B., et al. 2005. Drosophila Ric-8 regulates Gα cortical localization to promote Gα-dependent planar orientation of the mitotic spindle during asymmetric cell division. Nat. Cell Biol. 7:1083-1090.
6. Eaton, E. M., M. Hanlon, L. Bundy, and L. Sealy. 2001. Characterization of C/EBPβ isoforms in normal versus neoplastic mammary epithelial cells. J. Cell. Physiol. 189:91-105.
7. Flowers, S., N. G. Nagl, Jr., G. R. Beck, Jr., and E. Moran. 2009. Antagonistic roles for BRM and BRG1 SWI/SNF complexes in differentiation. J. Biol. Chem. 284:10067-10075.
8. Gutierrez, J. L., M. Chandy, M. J. Carrozza, and J. L. Workman. 2007. Activation domains drive nucleosome eviction by SWI/SNF. EMBO J. 26: 730-740.
9. Gutierrez, S., et al. 2002. CCAAT/enhancer-binding proteins (C/EBP) beta and delta activate osteocalcin gene transcription and synergize with Runx2 at the C/EBP element to regulate bone-specific expression. J. Biol. Chem. 277:1316-1323.
10. Harrison, J. R., et al. 2005. Col1a1 promoter-targeted expression of p20 CCAAT enhancer-binding protein beta (C/EBPβ), a truncated C/EBPβ isoform, causes osteopenia in transgenic mice. J. Biol. Chem. 280:8117-8124.
11. Henriquez, B., et al. 1 February 2011, posting date. C/EBPβ binds the P1 promoter of the Runx2 gene and up-regulates Runx2 transcription in osteoblastic cells. J. Cell. Physiol. doi:10.1002/jcp.22652.
12. Hirata, M., et al. 2009. C/EBPβ promotes transition from proliferation to hypertrophic differentiation of chondrocytes through transactivation of p57. PLoS One 4:e4543.
13. Iyer, V. V., T. B. Kadakia, L. R. McCabe, and R. C. Schwartz. 2004. CCAAT/enhancer-binding protein-beta has a role in osteoblast proliferation and differentiation. Exp. Cell Res. 295:128-137.
14. Katagiri, T., et al. 1994. Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J. Cell Biol. 127:1755-1766.
15. Klattenhoff, C., et al. 2003. Human brain synembryn interacts with Gsα and Gqα and is translocated to the plasma membrane in response to isoproterenol and carbachol. J. Cell. Physiol. 195:151-157.
16. Kowenz-Leutz, E., and A. Leutz. 1999. A C/EBP beta isoform recruits the SWI/SNF complex to activate myeloid genes. Mol. Cell 4:735-743.
17. Kowenz-Leutz, E., O. Pless, G. Dittmar, M. Knoblich, and A. Leutz. 2010. Crosstalk between C/EBPβ phosphorylation, arginine methylation, and SWI/SNF/Mediator implies an indexing transcription factor code. EMBO J. 29: 1105-1115.
18. Langst, G., E. J. Bonte, D. F. Corona, and P. B. Becker. 1999. Nucleosome movement by CHRAC and ISWI without disruption or trans-displacement of the histone octamer. Cell 97:843-852.
19. Li, H., et al. 2008. The Med1 subunit of transcriptional mediator plays a central role in regulating CCAAT/enhancer-binding protein-beta-driven transcription in response to interferon-gamma. J. Biol. Chem. 283:13077-13086.
20. Malik, S., M. Ghosh, T. M. Bonacci, G. G. Tall, and A. V. Smrcka. 2005. Ric-8 enhances G protein βγ-dependent signaling in response to βγ-binding peptides in intact cells. Mol. Pharmacol. 68:129-136.
21. Marie, P. J. 2008. Transcription factors controlling osteoblastogenesis. Arch. Biochem. Biophys. 473:98-105.
22. Miller, K. G., M. D. Emerson, J. R. McManus, and J. B. Rand. 2000. RIC-8 (Synembryn): a novel conserved protein that is required for G(q)alpha signaling in the C. elegans nervous system. Neuron 27:289-299.
23. Miller, K. G., and J. B. Rand. 2000. A role for RIC-8 (Synembryn) and GOA-1 (G(o) alpha) in regulating a subset of centrosome movements during early embryogenesis in Caenorhabditis elegans. Genetics 156:1649-1660.
24. Mink, S., B. Haenig, and K. H. Klempnauer. 1997. Interaction and functional collaboration of p300 and C/EBPbeta. Mol. Cell. Biol. 17:6609-6617.
25. Mo, X., E. Kowenz-Leutz, H. Xu, and A. Leutz. 2004. Ras induces mediator complex exchange on C/EBP beta. Mol. Cell 13:241-250.
26. Nagai, Y., A. Nishimura, K. Tago, N. Mizuno, and H. Itoh. 2010. Ric-8B stabilizes the alpha subunit of stimulatory G protein by inhibiting its ubiquitination. J. Biol. Chem. 285:11114-11120.
27. Nerlov, C. 2008. C/EBPs: recipients of extracellular signals through proteome modulation. Curr. Opin. Cell Biol. 20:180-185.
28. Nishimura, A., et al. 2006. Ric-8A potentiates Gq-mediated signal transduction by acting downstream of G protein-coupled receptor in intact cells. Genes Cells 11:487-498.
29. Owen, T. A., et al. 1990. Modifications of protein-DNA interactions in the proximal promoter of a cell-growth-regulated histone gene during onset and progression of osteoblast differentiation. Proc. Natl. Acad. Sci. U. S. A. 87:5129-5133.
30. Paredes, R., et al. 2004. Bone-specific transcription factor Runx2 interacts with the 1α,25-dihydroxyvitamin D3 receptor to up-regulate rat osteocalcin gene expression in osteoblastic cells. Mol. Cell. Biol. 24:8847-8861.
31. Phelan, M. L., G. R. Schnitzler, and R. E. Kingston. 2000. Octamer transfer and creation of stably remodeled nucleosomes by human SWI-SNF and its isolated ATPases. Mol. Cell. Biol. 20:6380-6389.
32. Pless, O., et al. 2008. G9a-mediated lysine methylation alters the function of CCAAT/enhancer-binding protein-beta. J. Biol. Chem. 283:26357-26363.
33. Romo, X., et al. 2008. xRic-8 is a GEF for Gsα and participates in maintaining meiotic arrest in Xenopus laevis oocytes. J. Cell. Physiol. 214:673-680.
34. Shen, J., et al. 2002. Histone acetylation in vivo at the osteocalcin locus is functionally linked to vitamin D-dependent, bone tissue-specific transcription. J. Biol. Chem. 277:20284-20292.
35. Siderovski, D. P., and F. S. Willard. 2005. The GAPs, GEFs, and GDIs of heterotrimeric G-protein alpha subunits. Int. J. Biol. Sci. 1:51-66.
36. Smink, J. J., et al. 2009. Transcription factor C/EBPβ isoform ratio regulates osteoclastogenesis through MafB. EMBO J. 28:1769-1781.
37. Soutoglou, E., and I. Talianidis. 2002. Coordination of PIC assembly and chromatin remodeling during differentiation-induced gene activation. Science 295:1901-1904.
38. Stein, G. S., et al. 2004. Runx2 control of organization, assembly and activity of the regulatory machinery for skeletal gene expression. Oncogene 23:4315-4329.
39. Tajbakhsh, S., P. Rocheteau, and I. Le Roux. 2009. Asymmetric cell divisions and asymmetric cell fates. Annu. Rev. Cell Dev. Biol. 25:671-699.
40. Tall, G. G., A. M. Krumins, and A. G. Gilman. 2003. Mammalian Ric-8A (synembryn) is a heterotrimeric Gα protein guanine nucleotide exchange factor. J. Biol. Chem. 278:8356-8362.
41. Tang, Q. Q., T. C. Otto, and M. D. Lane. 2003. CCAAT/enhancer-binding protein beta is required for mitotic clonal expansion during adipogenesis. Proc. Natl. Acad. Sci. U. S. A. 100:850-855.
42. Thielking, V., J. Alves, A. Fliess, G. Maass, and A. Pingoud. 1990. Accuracy of the EcoRI restriction endonuclease: binding and cleavage studies with oligodeoxynucleotide substrates containing degenerate recognition sequences. Biochemistry 29:4682-4691.
43. Tominaga, H., et al. 2008. CCAAT/enhancer-binding protein beta promotes osteoblast differentiation by enhancing Runx2 activity with ATF4. Mol. Biol. Cell 19:5373-5386.
44. Tonissoo, T., et al. 2010. Nucleotide exchange factor RIC-8 is indispensable in mammalian early development. Dev. Dyn. 239:3404-3415.
45. Tonissoo, T., R. Meier, K. Talts, M. Plaas, and A. Karis. 2003. Expression of ric-8 (synembryn) gene in the nervous system of developing and adult mouse. Gene Expr. Patterns 3:591-594.
46. Villagra, A., et al. 2006. Chromatin remodeling and transcriptional activity of the bone-specific osteocalcin gene require CCAAT/enhancer-binding protein beta-dependent recruitment of SWI/SNF activity. J. Biol. Chem. 281: 22695-22706.
47. olf. J. Neurosci. 25:3793-3800.
48. Wang, D., et al. 1999. Isolation and characterization of MC3T3-E1 preosteoblast subclones with distinct in vitro and in vivo differentiation/mineralization potential. J. Bone Miner. Res. 14:893-903.
49. Wang, H., et al. 2005. Ric-8 controls Drosophila neural progenitor asymmetric division by regulating heterotrimeric G proteins. Nat. Cell Biol. 7:1091-1098.
50. Wang, W. L., Y. C. Lee, W. M. Yang, W. C. Chang, and J. M. Wang. 2008. Sumoylation of LAP1 is involved in the HDAC4-mediated repression of COX-2 transcription. Nucleic Acids Res. 36:6066-6079.
51. Whitehouse, I., et al. 1999. Nucleosome mobilization catalysed by the yeast SWI/SNF complex. Nature 400:784-787.
52. Woodard, G. E., et al. 2010. Ric-8A and Gi alpha recruit LGN, NuMA, and dynein to the cell cortex to help orient the mitotic spindle. Mol. Cell. Biol. 30:3519-3530.
53. Xiong, W., C. C. Hsieh, A. J. Kurtz, J. P. Rabek, and J. Papaconstantinou. 2001. Regulation of CCAAT/enhancer-binding protein-beta isoform synthesis by alternative translational initiation at multiple AUG start sites. Nucleic Acids Res. 29:3087-3098.