Skip to main content

Advertisement

SpringerLink
Log in

Histone post-translational modifications induced by histone deacetylase inhibition in transcriptional control units of NIS gene

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Histone post-translational modifications (HPTMs) play a major role in control of gene transcription. Among them, histone acetylation and methylation have been extensively investigated. Histone acetylation at different residues is generally associated to active gene transcription. In contrast, histone methylation can be associated either to transcriptional activation or repression, depending primarily on the histone residue that is subjected to the modification. Herein, effects of the histone deacetylase inhibitor SAHA on the sodium-iodide symporter (NIS) gene expression were investigated in breast cancer cells (MDA157 and MDA468). SAHA treatment induces high increase of NIS mRNA levels in MDA468 cells (300-fold), but moderate increase in MDA157 cells (fivefold). Histone H3 HPTMs (acetylation and methylations) on transcriptional units of NIS gene were investigated in these cell lines upon SAHA treatment. Our data indicate that HPTMs, particularly the H3 lysine 27 trimethylation, may operate in contrast to current models that relate epigenetic modifications with transcriptional activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Turner BM (2000) Histone acetylation and an epigenetic code. BioEssays 22:836–845

    Article  CAS  PubMed  Google Scholar 

  2. Grunstein M (1997) Histone acetylation in chromatin structure and transcription. Nature 389:349–352

    Article  CAS  PubMed  Google Scholar 

  3. Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447:407–412

    Article  CAS  PubMed  Google Scholar 

  4. Shilatifard A (2006) Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 75:243–269

    Article  CAS  PubMed  Google Scholar 

  5. Santos-Rosa H, Schneider R, Bernstein BE, Karabetsou N, Morillon A, Weise C, Schreiber SL, Mellor J, Kouzarides T (2003) Methylation of histone H3 K4 mediates association of the Isw1p ATPase with chromatin. Mol Cell 12:1325–1332

    Article  CAS  PubMed  Google Scholar 

  6. Ringrose L, Ehret H, Paro R (2004) Distinct contributions of histone H3 Lysine 9 and 27 methylation to locus-specific stability of polycomb complexes. Mol Cell 16:641–653

    Article  CAS  PubMed  Google Scholar 

  7. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129:823–837

    Article  CAS  PubMed  Google Scholar 

  8. Kurdistani SK, Tavazoie S, Grunstein M (2004) Mapping global histone acetylation patterns to gene expression. Cell 117:721–733

    Article  CAS  PubMed  Google Scholar 

  9. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O’Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553–560

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Cui P, Liu W, Zhao Y, Lin Q, Zhang D, Ding F, Xin C, Zhang Z, Song S, Sun F, Yu J, Hu S (2012) Comparative analyses of H3K4 and H3K27 trimethylations between the mouse cerebrum and testis. Genomics Proteomics Bioinform 10:82–93

    Article  CAS  Google Scholar 

  11. Dai G, Levy O, Carrasco N (1996) Cloning and characterization of the thyroid iodide transporter. Nature 379:458–460

    Article  CAS  PubMed  Google Scholar 

  12. Tazebay UH, Wapnir IL, Levy O, Dohan O, Zuckier LS, Zhao QH, Deng HF, Amenta PS, Fineberg S, Pestell RG, Carrasco N (2000) The mammary gland iodide transporter is expressed during lactation and in breast cancer. Nature Med 6:871–878

    Article  CAS  PubMed  Google Scholar 

  13. Renier C, Yao C, Goris M, Ghosh M, Katznelson L, Nowles K, Gambhir SS, Wapnir I (2009) Endogenous NIS expression in triple-negative breast cancers. Ann Surg Oncol 16:962–968

    Article  PubMed  Google Scholar 

  14. Taki K, Kogai T, Kanamoto Y, Hershman JM, Brent GA (2002) A thyroid-specific far-upstream enhancer in the human sodium/iodide symporter gene requires pax-8 binding and cyclic adenosine 3′-5′-monophosphate response element-like sequence binding proteins for full activity and is differentially regulated in normal and thyroid cancer cells. Mol Endocrinol 16:2266–2282

    Article  CAS  PubMed  Google Scholar 

  15. Kogai T, Brent GA (2012) The sodium iodide symporter (NIS): regulation and approaches to targeting for cancer therapeutics. Pharmacol Ther 135:355–370

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Puppin C, D’Aurizio F, D’Elia AV, Cesaratto L, Tell G, Russo D, Filetti S, Ferretti E, Tosi E, Mattei T, Pianta A, Pellizzari L, Damante G (2005) Effects of histone acetylation on NIS promoter and expression of thyroid-specific transcription factors. Endocrinology 146:3967–3974

    Article  CAS  PubMed  Google Scholar 

  17. Fortunati N, Catalano MG, Marano F, Mugoni V, Pugliese M, Bosco O, Mainini F, Boccuzzi G (2010) The pan-DAC inhibitor LBH589 is a multi-functional agent in breast cancer cells: cytotoxic drug and inducer of sodium-iodide symporter (NIS). Breast Cancer Res Treat 124:667–675

    Article  CAS  PubMed  Google Scholar 

  18. Sponziello M, Scipioni A, Durante C, Verrienti A, Maranghi M, Giacomelli L, Ferretti E, Celano M, Filetti S, Russo D (2010) Regulation of sodium/iodide symporter and lactoperoxidase expression in four human breast cancer cell lines. J Endocrinol Invest 33:2–6

    Article  CAS  PubMed  Google Scholar 

  19. Marks PA, Xu WS (2009) Histone deacetylase inhibitors: potential in cancer therapy. J Cell Biochem 107:600–608

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Russo D, Damante G, Puxeddu E, Durante C, Filetti S (2011) Epigenetics of thyroid cancer and novel therapeutic targets. J Mol Endocrinol 46:R73–R81

    Article  CAS  PubMed  Google Scholar 

  21. Akagi T, Luong QT, Gui D, Said J, Selektar J, Yung A, Bunce CM, Braunstein GD, Koeffler HP (2008) Induction of sodium iodide symporter gene and molecular characterisation of HNF3β/FoxA2, TTF-1 and C/EBPβ in thyroid carcinoma cells. Br J Cancer 99:781–788

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Hou P, Bojdani E, Xing M (2010) Induction of thyroid gene expression and radioiodine uptake in thyroid cancer cells by targeting major signaling pathways. J Clin Endocrinol Metab 95:820–828

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Marks PA (2007) Discovery and development of SAHA as an anticancer agent. Oncogene 26:1351–1356

    Article  CAS  PubMed  Google Scholar 

  24. Lavarone E, Puppin C, Passon N, Filetti S, Russo D, Damante G (2013) The PARP inhibitor PJ34 modifies proliferation, NIS expression and epigenetic marks in thyroid cancer cell lines. Mol Cell End 365:1–10

    Article  CAS  Google Scholar 

  25. Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21:381–395

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Butler JS, Koutelou E, Schibler AC, Dent SY (2012) Histone-modifying enzymes: regulators of developmental decisions and drivers of human disease. Epigenomics 4:163–177

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Rando OJ (2007) Global patterns of histone modifications. Curr Opin Genet Dev 17:94–99

    Article  CAS  PubMed  Google Scholar 

  28. Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NC, Schreiber SL, Mellor J, Kouzarides T (2002) Active genes are tri-methylated at K4 of histone H3. Nature 419:407–411

    Article  CAS  PubMed  Google Scholar 

  29. MacDonald VE, Howe LJ (2009) Histone acetylation: where to go and how to get there. Epigenetics 4:139–143

    Article  CAS  PubMed  Google Scholar 

  30. Hosogane M, Funayama R, Nishida Y, Nagashima T, Nakayama K (2013) Ras-induced changes in H3K27me3 occur after those in transcriptional activity. PLoS Genet 9:e1003698

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work is funded by grants to GD from Associazione Italiana per la Ricerca sul Cancro (AIRC) (project no IG 10296) and MIUR (20093WAPYK_003).

Author information

Authors and Affiliations

  1. Department of Medical and Biological Sciences, University of Udine, Piazzale Kolbe 4, 33100, Udine, Italy

    Federica Baldan, Elisa Lavarone, Carla Di Loreto, Giuseppe Damante & Cinzia Puppin

  2. Department of Internal Medicine and Medical Specialties, University of Roma “La Sapienza”, Rome, Italy

    Sebastiano Filetti

  3. Department of Health Sciences, University “Magna Graecia” of Catanzaro, Catanzaro, Italy

    Diego Russo

  4. Institute of Medical Genetics, University Hospital “S. Maria della Misericordia”, Udine, Italy

    Giuseppe Damante

Authors
  1. Federica Baldan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elisa Lavarone
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carla Di Loreto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sebastiano Filetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Diego Russo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Giuseppe Damante
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cinzia Puppin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cinzia Puppin.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baldan, F., Lavarone, E., Di Loreto, C. et al. Histone post-translational modifications induced by histone deacetylase inhibition in transcriptional control units of NIS gene. Mol Biol Rep 41, 5257–5265 (2014). https://doi.org/10.1007/s11033-014-3397-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-014-3397-x

Keywords

Search

Navigation