The Journal of Nutritional Biochemistry
Volume 21, Issue 4 , Pages 310-316 , April 2010

K12-biotinylated histone H4 is enriched in telomeric repeats from human lung IMR-90 fibroblasts

Received 2 July 2008 ,Revised 22 December 2008 ,Accepted 8 January 2009.

References 

  1. Greider CW. Telomeres, telomerase and senescence. Bioessays. 1990;12:363–369
  2. Smith S, Giriat I, Schmitt A, de Lange T. Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science. 1998;282:1484–1487
  3. Broccoli D, Smogorzewska A, Chong L, de Lange T. Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat Genet. 1997;17:231–235
  4. Greider CW. Telomerase is processive. Mol Cell Biol. 1991;11:4572–4580
  5. Blackburn EH, Greider CW. Telomeres. Plainview (NY): Cold Spring Harbor Laboratory Press; 1995;
  6. Kipling D. Telomeres, replicative senescence and human ageing. Maturitas. 2001;38:25–38
  7. Chiu CP, Harley CB. Replicative senescence and cell immortality: the role of telomeres and telomerase. Proc Soc Exp Biol Med. 1997;214:99–106
  8. Karlseder J, Smogorzewska A, de Lange T. Senescence induced by altered telomere state, not telomere loss. Science. 2002;295:2446–2449
  9. Greider CW, Blackburn EH. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell. 1985;43:405–413
  10. Greider CW, Blackburn EH. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature. 1989;337:331–337
  11. Blackburn EH, Greider CW, Henderson E, Lee MS, Shampay J, Shippen-Lentz D. Recognition and elongation of telomeres by telomerase. Genome. 1989;31:553–560
  12. Blackburn EH. Telomerases. Annu Rev Biochem. 1992;61:113–129
  13. Nugent CI, Lundblad V. The telomerase reverse transcriptase: components and regulation. Genes Dev. 1998;12:1073–1085
  14. Grewal SI, Moazed D. Heterochromatin and epigenetic control of gene expression. Science. 2003;301:798–802
  15. Khan AU, Krishnamurthy S. Histone modifications as key regulators of transcription. Front Biosci. 2005;10:866–872
  16. Wolffe A. Chromatin. San Diego (CA): Academic Press; 1998;
  17. Jenuwein T, Allis CD. Translating the histone code. Science. 2001;293:1074–1080
  18. Fischle W, Wang Y, Allis CD. Histone and chromatin cross-talk. Curr Opin Cell Biol. 2003;15:172–183
  19. Cong YS, Bacchetti S. Histone deacetylation is involved in the transcriptional repression of hTERT in normal human cells. J Biol Chem. 2000;275:35665–35668
  20. Devereux TR, Horikawa I, Anna CH, Annab LA, Afshari CA, Barrett JC. DNA methylation analysis of the promoter region of the human telomerase reverse transcriptase (hTERT) gene. Cancer Res. 1999;59:6087–6090
  21. Ge Z, Liu C, Bjorkholm M, Gruber A, Xu D. Mitogen-activated protein kinase cascade-mediated histone H3 phosphorylation is critical for telomerase reverse transcriptase expression/telomerase activation induced by proliferation. Mol Cell Biol. 2006;26:230–237
  22. Stanley JS, Griffin JB, Zempleni J. Biotinylation of histones in human cells: effects of cell proliferation. Eur J Biochem. 2001;268:5424–5429
  23. Camporeale G, Giordano E, Rendina R, Zempleni J, Eissenberg JC. Drosophila holocarboxylase synthetase is a chromosomal protein required for normal histone biotinylation, gene transcription patterns, lifespan and heat tolerance. J Nutr. 2006;136:2735–2742
  24. Camporeale G, Oommen AM, Griffin JB, Sarath G, Zempleni J. K12-biotinylated histone H4 marks heterochromatin in human lymphoblastoma cells. J Nutr Biochem. 2007;18:760–768
  25. Narang MA, Dumas R, Ayer LM, Gravel RA. Reduced histone biotinylation in multiple carboxylase deficiency patients: a nuclear role for holocarboxylase synthetase. Hum Mol Genet. 2004;13:15–23
  26. Chew YC, Camporeale G, Kothapalli N, Sarath G, Zempleni J. Lysine residues in N- and C-terminal regions of human histone H2A are targets for biotinylation by biotinidase. J Nutr Biochem. 2006;17:225–233
  27. Kobza K, Camporeale G, Rueckert B, Kueh A, Griffin JB, Sarath G, et al. K4, K9, and K18 in human histone H3 are targets for biotinylation by biotinidase. FEBS J. 2005;272:4249–4259
  28. Kobza K, Sarath G, Zempleni J. Prokaryotic BirA ligase biotinylates K4, K9, K18 and K23 in histone H3. BMB Rep. 2008;41:310–315
  29. Camporeale G, Shubert EE, Sarath G, Cerny R, Zempleni J. K8 and K12 are biotinylated in human histone H4. Eur J Biochem. 2004;271:2257–2263
  30. Chew YC, West JT, Kratzer SJ, Ilvarsonn AM, Eissenberg JC, Dave BJ, et al. Biotinylation of histones represses transposable elements in human and mouse cells and cell lines, and in Drosophila melanogaster. J Nutr. 2008;138:2316–2322
  31. Rubio MA, Kim SH, Campisi J. Reversible manipulation of telomerase expression and telomere length. Implications for the ionizing radiation response and replicative senescence of human cells.. J Biol Chem. 2002;277:28609–28617
  32. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, et al A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA. 1995;92:9363–9367
  33. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, et al. Specific association of human telomerase activity with immortal cells and cancer. Science. 1994;266:2011–2015
  34. Gil ME, Coetzer TL. Real-time quantitative PCR of telomere length. Mol Biotechnol. 2004;27:169–172
  35. Kang SH, Vieira K, Bungert J. Combining chromatin immunoprecipitation and DNA footprinting: a novel method to analyze protein–DNA interactions in vivo. Nucleic Acids Res. 2002;30:e44
  36. Hornstra IK, Yang TP. In vivo footprinting and genomic sequencing by ligation-mediated PCR. Anal Biochem. 1993;213:179–193
  37. Rasband W., ImageJ 1.39t software. (http://rsb.info.nih.gov/ij/) National Institutes of Health, Bethesda, MD (downloaded April 1, 2008).
  38. Anwar A, Dehn D, Siegel D, Kepa JK, Tang LJ, Pietenpol JA, et al. Interaction of human NAD(P)H:quinone oxidoreductase 1 (NQO1) with the tumor suppressor protein p53 in cells and cell-free systems. J Biol Chem. 2003;278:10368–10373
  39. Sarg B, Koutzamani E, Helliger W, Rundquist I, Lindner HH. Postsynthetic trimethylation of histone H4 at lysine 20 in mammalian tissues is associated with aging. J Biol Chem. 2002;277:39195–39201
  40. Camporeale G, Zempleni J, Eissenberg JC. Susceptibility to heat stress and aberrant gene expression patterns in holocarboxylase synthetase-deficient Drosophila melanogaster are caused by decreased biotinylation of histones, not of carboxylases. J Nutr. 2007;137:885–889
  41. Gralla M, Camporeale G, Zempleni J. Holocarboxylase synthetase regulates expression of biotin transporters by chromatin remodeling events at the SMVT locus. J Nutr Biochem. 2008;19:400–408
  42. Manthey KC, Griffin JB, Zempleni J. Biotin supply affects expression of biotin transporters, biotinylation of carboxylases, and metabolism of interleukin-2 in Jurkat cells. J Nutr. 2002;132:887–892
  43. Zempleni J, Mock DM. Uptake and metabolism of biotin by human peripheral blood mononuclear cells. Am J Physiol Cell Physiol. 1998;275:C382–C388
  44. SAS Institute (1999). StatView Reference SAS Publishing, StatView Reference, Cary, NC.
  45. Cawthon RM. Telomere measurement by quantitative PCR. Nucleic Acids Res. 2002;30:e47
  46. Simpson RT. Histones H3 and H4 interact with the ends of nucleosome DNA. Proc Natl Acad Sci USA. 1976;73:4400–4404
  47. Kristjuhan A, Svejstrup JQ. Evidence for distinct mechanisms facilitating transcript elongation through chromatin in vivo. EMBO J. 2004;23:4243–4252
  48. Lee CK, Shibata Y, Rao B, Strahl BD, Lieb JD. Evidence for nucleosome depletion at active regulatory regions genome-wide. Nat Genet. 2004;36:900–905
  49. Erkina TY, Tschetter PA, Erkine AM. Different requirements of the SWI/SNF complex for robust nucleosome displacement at promoters of heat shock factor and Msn2- and Msn4-regulated heat shock genes. Mol Cell Biol. 2008;28:1207–1217
  50. Said HM. Recent advances in carrier-mediated intestinal absorption of water-soluble vitamins. Annu Rev Physiol. 2004;66:419–446
  51. Camporeale G, Zempleni J. Biotin. In:  Bowman BA,  Russell RM editor. Present knowledge in nutrition. Washington, DC: International Life Sciences Institute; 2006;p. 314–326
  52. Crisp SERH, Camporeale G, White BR, Toombs CF, Griffin JB, Said HM, et al. Biotin supply affects rates of cell proliferation, biotinylation of carboxylases and histones, and expression of the gene encoding the sodium-dependent multivitamin transporter in JAr choriocarcinoma cells. Eur J Nutr. 2004;43:23–31
  53. Scheerger SB, Zempleni J. Expression of oncogenes depends on biotin in human small cell lung cancer cells NCI-H69. Int J Vitam Nutr Res. 2003;73:461–467
  54. Freytag SO, Utter MF. Regulation of the synthesis and degradation of pyruvate carboxylase in 3T3-L1 cells. J Biol Chem. 1983;258:6307–6312
  55. Weinberg MD, Utter MF. Effect of thyroid hormone on the turnover of rat liver pyruvate carboxylase and pyruvate dehydrogenase. J Biol Chem. 1979;254:9492–9499
  56. Weinberg MD, Utter MF. Effect of streptozotocin-induced diabetes mellitus on the turnover of rat liver pyruvate carboxylase and pyruvate dehydrogenase. Biochem J. 1980;188:601–608
  57. Majerus P, Kilburn E. Acetyl coenzyme A carboxylase. The roles of synthesis and degradation in regulation of enzyme levels in rat liver. J Biol Chem. 1969;244:6254–6262
  58. Nakanishi S, Numa S. Purification of rat liver acetyl coenzyme A carboxylase and immunochemical studies on its synthesis and degradation. Eur J Biochem. 1970;16:161–173
  59. Commerford SL, Carsten AL, Cronkite EP. Histone turnover within nonproliferating cells. Proc Natl Acad Sci USA. 1982;79:1163–1165
  60. Djondjurov LP, Yancheva NY, Ivanova EC. Histones of terminally differentiated cells undergo continuous turnover. Biochemistry. 1983;22:4095–4102
  61. Podgornaya OI, Bugaeva EA, Voronin AP, Gilson E, Mitchell AR. Nuclear envelope associated protein that binds telomeric DNAs. Mol Reprod Dev. 2000;57:16–25
  62. Ding X, Xu R, Yu J, Xu T, Zhuang Y, Han M. SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev Cell. 2007;12:863–872
  63. Schmitt J, Benavente R, Hodzic D, Hoog C, Stewart CL, Alsheimer M. Transmembrane protein Sun2 is involved in tethering mammalian meiotic telomeres to the nuclear envelope. Proc Natl Acad Sci USA. 2007;104:7426–7431

☆ We would like to acknowledge the contribution of the University of Nebraska Agricultural Research Division, supported in part by funds provided through the Hatch Act. Additional support was provided by NIH Grants DK063945, DK077816 and ES015206; by USDA CSREES Grant 2006-35200-17138; and by NSF EPSCoR Grant EPS-0701892.

PII: S0955-2863(09)00011-4

doi: 10.1016/j.jnutbio.2009.01.010

The Journal of Nutritional Biochemistry
Volume 21, Issue 4 , Pages 310-316 , April 2010

Article Tools

* Image Usage & Resolution