cAMP signaling induces rapid loss of histone H3 phosphorylation in mammary adenocarcinoma-derived cell lines

Experimental Cell Research

Volumn 314, Issue 1, 2008, Pages 1-10

  Rodriguez Collazo, Pedro ^a,c   Snyder, Sara K ^a   Chiffer, Rebecca C ^a   Zlatanova, Jordanka ^b   Leuba, Sanford H ^c   Smith, Catharine L ^a,d  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF WYOMING   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF ARIZONA   (United States)

Author keywords

cAMP signaling; Cell cycle; Chromatin; Histone H3; Phosphorylation

Indexed keywords

CYCLIC AMP; HISTONE H3;

ANIMAL CELL; ARTICLE; BREAST ADENOCARCINOMA; BREAST CARCINOMA; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL GROWTH; METHYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 36549068826     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2007.09.011     Document Type: Article

References (37)

1. van Holde K.E. Chromatin (1988), Springer-Verlag, Heidelberg
2. Berger S.L. Histone modifications in transcriptional regulation. Curr. Opin. Genet. Dev. 12 (2002) 142-148
3. Nathan D., Sterner D.E., and Berger S.L. Histone modifications: now summoning sumoylation. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 13118-13120
4. Turner B.M. Decoding the nucleosome. Cell 75 (1993) 5-8
5. Strahl B.D., and Allis C.D. The language of covalent histone modifications. Nature 403 (2000) 41-45
6. Nowak S.J., and Corces V.G. Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation. Trends Genet. 20 (2004) 214-220
7. Shoemaker C.B., and Chalkley R. H3-specific nucleohistone kinase of bovine thymus chromatin. Purification, characterization, and specificity for threonine residue 3. J. Biol. Chem. 255 (1980) 11048-11055
8. Preuss U., Landsberg G., and Scheidtmann K.H. Novel mitosis-specific phosphorylation of histone H3 at Thr11 mediated by Dlk/ZIP kinase. Nucleic Acids Res. 31 (2003) 878-885
9. Mahadevan L.C., Willis A.C., and Barratt M.J. Rapid histone H3 phosphorylation in response to growth factors, phorbol esters, okadaic acid, and protein synthesis inhibitors. Cell 65 (1991) 775-783
10. DeManno D.A., Cottom J.E., Kline M.P., Peters C.A., Maizels E.T., and Hunzicker-Dunn M. Follicle-stimulating hormone promotes histone H3 phosphorylation on serine-10. Mol. Endocrinol. 13 (1999) 91-105
11. Salvador L.M., Park Y., Cottom J., Maizels E.T., Jones J.C., Schillace R.V., Carr D.W., Cheung P., Allis C.D., Jameson J.L., and Hunzicker-Dunn M. Follicle-stimulating hormone stimulates protein kinase A-mediated histone H3 phosphorylation and acetylation leading to select gene activation in ovarian granulosa cells. J. Biol. Chem. 276 (2001) 40146-40155
12. Anest V., Hanson J.L., Cogswell P.C., Steinbrecher K.A., Strahl B.D., and Baldwin A.S. A nucleosomal function for IkappaB kinase-alpha in NF-kappaB-dependent gene expression. Nature 423 (2003) 659-663
13. Yamamoto Y., Verma U.N., Prajapati S., Kwak Y.T., and Gaynor R.B. Histone H3 phosphorylation by IKK-alpha is critical for cytokine-induced gene expression. Nature 423 (2003) 655-659
14. Clayton A.L., Rose S., Barratt M.J., and Mahadevan L.C. Phosphoacetylation of histone H3 on c-fos- and c-jun-associated nucleosomes upon gene activation. EMBO J. 19 (2000) 3714-3726
15. Cheung P., Tanner K.G., Cheung W.L., Sassone-Corsi P., Denu J.M., and Allis C.D. Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol. Cell 5 (2000) 905-915
16. Soloaga A., Thomson S., Wiggin G.R., Rampersaud N., Dyson M.H., Hazzalin C.A., Mahadevan L.C., and Arthur J.S. MSK2 and MSK1 mediate the mitogen- and stress-induced phosphorylation of histone H3 and HMG-14. EMBO J. 22 (2003) 2788-2797
17. Thomson S., Clayton A.L., Hazzalin C.A., Rose S., Barratt M.J., and Mahadevan L.C. The nucleosomal response associated with immediate-early gene induction is mediated via alternative MAP kinase cascades: MSK1 as a potential histone H3/HMG-14 kinase. EMBO J. 18 (1999) 4779-4793
18. Pascreau G., Arlot-Bonnemains Y., and Prigent C. Phosphorylation of histone and histone-like proteins by aurora kinases during mitosis. Prog. Cell Cycle Res. 5 (2003) 369-374
19. Mulholland N.M., Snyder S.K., Kolla S.S., and Smith C.L. Chromatin-dependent regulation of the MMTV promoter by cAMP signaling is mediated through distinct pathways. Exp. Cell Res. 287 (2003) 361-373
20. Hardie D.G., Scott J.W., Pan D.A., and Hudson E.R. Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett. 546 (2003) 113-120
21. Hake S.B., Garcia B.A., Kauer M., Baker S.P., Shabanowitz J., Hunt D.F., and Allis C.D. Serine 31 phosphorylation of histone variant H3.3 is specific to regions bordering centromeres in metaphase chromosomes. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 6344-6349
22. Lindner H., Helliger W., and Puschendorf B. Histone separation by high-performance liquid chromatography on C4 reverse-phase columns. Anal. Biochem. 158 (1986) 424-430
23. Shechter D., Dormann H.L., Allis C.D., and Hake S.B. Extraction, purification and analysis of histones. Nat. Protoc. 2 (2007) 1445-1457
24. Bradbury E.M., Inglis R.J., and Matthews H.R. Control of cell division by very lysine rich histone (F1) phosphorylation. Nature 247 (1974) 257-261
25. Lu M.J., Dadd C.A., Mizzen C.A., Perry C.A., McLachlan D.R., Annunziato A.T., and Allis C.D. Generation and characterization of novel antibodies highly selective for phosphorylated linker histone H1 in Tetrahymena and HeLa cells. Chromosoma 103 (1994) 111-121
26. Stork P.J., and Schmitt J.M. Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol. 12 (2002) 258-266
27. Richards J.S. New signaling pathways for hormones and cyclic adenosine 3′,5′-monophosphate action in endocrine cells. Mol. Endocrinol. 15 (2001) 209-218
28. Rea S., Eisenhaber F., O'Carroll D., Strahl B.D., Sun Z.W., Schmid M., Opravil S., Mechtler K., Ponting C.P., Allis C.D., and Jenuwein T. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406 (2000) 593-599
29. Terada Y. Aurora-B/AIM-1 regulates the dynamic behavior of HP1alpha at the G2-M transition. Mol. Biol. Cell 17 (2006) 3232-3241
30. Long Y.C., and Zierath J.R. AMP-activated protein kinase signaling in metabolic regulation. J. Clin. Invest 116 (2006) 1776-1783
31. Kaupp U.B., and Seifert R. Cyclic nucleotide-gated ion channels. Physiol. Rev. 82 (2002) 769-824
32. Stambrook P.J., and Velez C. Reversible arrest of Chinese hamster V79 cells in G2 by dibutytyl AMP. Exp. Cell Res. 99 (1976) 57-62
33. Blomhoff H.K., Blomhoff R., Stokke T., deLange D.C., Brevik K., Smeland E.B., Funderud S., and Godal T. cAMP-mediated growth inhibition of a B-lymphoid precursor cell line Reh is associated with an early transient delay in G2/M, followed by an accumulation of cells in G1. J. Cell. Physiol. 137 (1988) 583-587
34. Kurokawa K., and Kato J. Cyclic AMP delays G2 progression and prevents efficient accumulation of cyclin B1 proteins in mouse macrophage cells. Cell Struct. Funct. 23 (1998) 357-365
35. Miller W.R. Regulatory subunits of PKA and breast cancer. Ann. N.Y. Acad. Sci. 968 (2002) 37-48
36. Tortora G., and Ciardiello F. Antisense targeting protein kinase A type I as a drug for integrated strategies of cancer therapy. Ann. N.Y. Acad. Sci. 1002 (2003) 236-243
37. Kawabe T. G2 checkpoint abrogators as anticancer drugs. Mol. Cancer Ther. 3 (2004) 513-519