Histone cleavage as a mechanism for epigenetic regulation: Current insights and perspectives

Current Molecular Medicine

Volumn 14, Issue 9, 2014, Pages 1164-1172

  Zhou, P ^a   Wu, E ^b   Alam, H B ^a   Li, Y ^a  

^a UNIVERSITY OF MICHIGAN HOSPITALS   (United States)

^b NORTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

Cleavage; H3; Histone; Post translational modification

Indexed keywords

BLOOD CLOTTING FACTOR 7; DNA; GLUTAMATE DEHYDROGENASE; HISTONE; HISTONE DEACETYLASE; HISTONE H2A; HISTONE H3; LEUKOCYTE ELASTASE; PROTEIN C; PROTEINASE; TRANSCRIPTION FACTOR IIA;

AGING; ARTICLE; CELL DIFFERENTIATION; CHROMATIN STRUCTURE; CLINICAL TRIAL (TOPIC); EMBRYONIC STEM CELL; ENZYME ACTIVITY; EPIGENETICS; EUKARYOTE EVOLUTION; EXTRACELLULAR TRAP; FOOT AND MOUTH DISEASE; GENE EXPRESSION; HOMEOSTASIS; HUMAN; IMMUNOLOGY; INFECTION; INFLAMMATION; NONHUMAN; PROTEIN DEGRADATION; PROTEIN PROCESSING; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; ANIMAL; GENETIC EPIGENESIS; GENETICS; METABOLISM;

EUKARYOTA;

ANIMALS; EPIGENESIS, GENETIC; FACTOR VII; HISTONES; HUMANS; INFLAMMATION; LEUKOCYTE ELASTASE; PROTEIN C; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS;

EID: 84926289107     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/1566524014666141015155630     Document Type: Article

References (75)

1. Morgan BA, Mittman BA, Smith MM. The highly conserved N-terminal domains of histones H3 and H4 are required for normal cell cycle progression. Mol Cell Biol 1991; 11: 4111-20.
2. Parseghian MH, Luhrs KA. Beyond the walls of the nucleus: the role of histones in cellular signaling and innate immunity. Biochem Cell Biol 2006; 84: 589-604.
3. Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. J Mol Biol 2002; 319: 1097-113.
4. Bohm V, Hieb AR, Andrews AJ, et al. Nucleosome accessibility governed by the dimer/tetramer interface. Nucleic Acids Res 2011; 39: 3093-102.
5. Giri S, Prasanth SG. Replicating and transcribing on twisted roads of chromatin. Brief Funct Genomics 2012; 11: 188-204.
6. Allis CD, Bowen JK, Abraham GN, Glover CV, Gorovsky MA. Proteolytic processing of histone H3 in chromatin: a physiologically regulated event in Tetrahymena micronuclei. Cell 1980; 20: 55-64.
7. Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet 2007; 8: 286-98.
8. Soragni E, Xu C, Cooper A, Plasterer HL, Rusche JR, Gottesfeld JM. Evaluation of histone deacetylase inhibitors as therapeutics for neurodegenerative diseases. Methods Mol Biol 2011; 793: 495-508.
9. Allam R, Scherbaum CR, Darisipudi MN, et al. Histones from dying renal cells aggravate kidney injury via TLR2 and TLR4. J Am Soc Nephrol 2012; 23: 1375-88.
10. Anderson DC, Green GR, Smith K, Selker EU. Extensive and varied modifications in histone H2B of wild-type and histone deacetylase 1 mutant Neurospora crassa. Biochemistry 2010; 49: 5244-57.
11. Kouzarides T. Chromatin modifications and their function. Cell 2007; 128: 693-705.
12. Zhang K, Sridhar VV, Zhu J, Kapoor A, Zhu JK. Distinctive core histone post-translational modification patterns in Arabidopsis thaliana. PLoS One 2007; 2: e1210.
13. Bhaumik SR, Smith E, Shilatifard A. Covalent modifications of histones during development and disease pathogenesis. Nat Struct Mol Biol 2007; 14: 1008-16.
14. Grunstein M. Histone acetylation in chromatin structure and transcription. Nature 1997; 389: 349-52.
15. Cosgrove MS, Wolberger C. How does the histone code work? Biochem Cell Biol 2005; 83: 468-76.
16. Allis CD, Wiggins JC. Proteolytic processing of micronuclear H3 and histone phosphorylation during conjugation in Tetrahymena thermophila. Exp Cell Res 1984; 153: 287-98.
17. Lin R, Cook RG, Allis CD. Proteolytic removal of core histone amino termini and dephosphorylation of histone H1 correlate with the formation of condensed chromatin and transcriptional silencing during Tetrahymena macronuclear development. Genes Dev 1991; 5: 1601-10.
18. Vitolo JM, Thiriet C, Hayes JJ. The H3-H4 N-terminal tail domains are the primary mediators of transcription factor IIIA access to 5S DNA within a nucleosome. Mol Cell Biol 2000; 20: 2167-75.
19. Smith BC, Denu JM. Chemical mechanisms of histone lysine and arginine modifications. Biochim Biophys Acta 2009; 1789: 45-57.
20. Gunjan A, Paik J, Verreault A. The emergence of regulated histone proteolysis. Curr Opin Genet Dev 2006; 16: 112-8.
21. Bertin A, Renouard M, Pedersen JS, Livolant F, Durand D. H3 and H4 histone tails play a central role in the interactions of recombinant NCPs. Biophys J 2007; 92: 2633-45.
22. Suganuma T, Workman JL. Crosstalk among Histone Modifications. Cell 2008; 135: 604-7.
23. Mandal P, Azad GK, Tomar RS. Identification of a novel histone H3 specific protease activity in nuclei of chicken liver. Biochem Biophys Res Commun 2012; 421: 261-7.
24. Adams-Cioaba MA, Krupa JC, Xu C, Mort JS, Min J. Structural basis for the recognition and cleavage of histone H3 by cathepsin L. Nat Commun 2011; 2: 197.
25. Duncan EM, Muratore-Schroeder TL, Cook RG, et al. Cathepsin L proteolytically processes histone H3 during mouse embryonic stem cell differentiation. Cell 2008; 135: 284-94.
26. Vossaert L, Meert P, Scheerlinck E, et al. Identification of histone H3 clipping activity in human embryonic stem cells. Stem Cell Res 2014; 13: 123-34.
27. Mandal P, Verma N, Chauhan S, Tomar RS. Unexpected histone H3 tail-clipping activity of glutamate dehydrogenase. J Biol Chem 2013; 288: 18743-57.
28. Santos-Rosa H, Kirmizis A, Nelson C, et al. Histone H3 tail clipping regulates gene expression. Nat Struct Mol Biol 2009; 16: 17-22.
29. Xue Y, Vashisht AA, Tan Y, Su T, Wohlschlegel JA. PRB1 is required for clipping of the histone H3 N terminal tail in Saccharomyces cerevisiae. PLoS One 2014; 9: e90496.
30. Falk MM, Grigera PR, Bergmann IE, Zibert A, Multhaup G, Beck E. Foot-and-mouth disease virus protease 3C induces specific proteolytic cleavage of host cell histone H3. J Virol 1990; 64: 748-56.
31. Sriraman V, Richards JS. Cathepsin L gene expression and promoter activation in rodent granulosa cells. Endocrinology 2004; 145: 582-91.
32. Kovarik M, Muthny T, Sispera L, Holecek M. Effects of betahydroxy-beta-methylbutyrate treatment in different types of skeletal muscle of intact and septic rats. J Physiol Biochem 2010; 66: 311-9.
33. Brown F, Martin SJ, Underwood B. A study of the kinetics of protein and RNA synthesis induced by foot-and-mouth disease virus. Biochim Biophys Acta 1966; 129: 166-77.
34. Tesar M, Marquardt O. Foot-and-mouth disease virus protease 3C inhibits cellular transcription and mediates cleavage of histone H3. Virology 1990; 174: 364-74.
35. Panda P, Chaturvedi MM, Panda AK, Suar M, Purohit JS. Purification and characterization of a novel histone H2A specific protease (H2Asp) from chicken liver nuclear extract. Gene 2013; 512: 47-54.
36. Nightingale KP, Gendreizig S, White DA, Bradbury C, Hollfelder F, Turner BM. Cross-talk between histone modifications in response to histone deacetylase inhibitors: MLL4 links histone H3 acetylation and histone H3K4 methylation. J Biol Chem 2007; 282: 4408-16.
37. Dieker J, Muller S. Epigenetic histone code and autoimmunity. Clin Rev Allergy Immunol 2010; 39: 78-84.
38. Yang XJ. Multisite protein modification and intramolecular signaling. Oncogene 2005; 24: 1653-62.
39. Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res 2011; 21: 381-95.
40. Qian MX, Pang Y, Liu CH, et al. Acetylation-mediated proteasomal degradation of core histones during DNA repair and spermatogenesis. Cell 2013; 153: 1012-24.
41. Nurse NP, Jimenez-Useche I, Smith IT, Yuan C. Clipping of flexible tails of histones H3 and H4 affects the structure and dynamics of the nucleosome. Biophys J 2013; 104: 1081-8.
42. Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotechnol 2010; 28: 1057-68.
43. Das C, Tyler JK. Histone exchange and histone modifications during transcription and aging. Biochim Biophysica Acta 2013; 1819: 332-42.
44. Xu J, Lupu F, Esmon CT. Inflammation, innate immunity and blood coagulation. Hamostaseologie 2010; 30: 5-6, 8-9.
45. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303: 1532-5.
46. Urban CF, Ermert D, Schmid M, et al. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 2009; 5: e1000639.
47. Fuchs TA, Bhandari AA, Wagner DD. Histones induce rapid and profound thrombocytopenia in mice. Blood 2011; 118: 3708-14.
48. Saffarzadeh M, Juenemann C, Queisser MA, et al. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS One 2012; 7: e32366.
49. Xu J, Zhang X, Monestier M, Esmon NL, Esmon CT. Extracellular histones are mediators of death through TLR2 and TLR4 in mouse fatal liver injury. J Immunol 2011; 187: 2626-31.
50. Li Y, Liu B, Fukudome EY, et al. Identification of citrullinated histone H3 as a potential serum protein biomarker in a lethal model of lipopolysaccharide-induced shock. Surgery 2011; 150: 442-51.
51. Semeraro N, Ammollo CT, Semeraro F, Colucci M. Sepsis, thrombosis and organ dysfunction. Thromb Res 2012; 129: 290-5.
52. Li Y, Alam HB. Modulation of acetylation: creating a prosurvival and anti-inflammatory phenotype in lethal hemorrhagic and septic shock. J Biomed Biotechnol 2011; 2011: 523481.
53. Chong W, Li Y, Liu B, et al. Anti-inflammatory properties of histone deacetylase inhibitors: a mechanistic study. J Trauma Acute Care Surg 2012; 72: 347-53; discussion 353-4.
54. Licciardi PV, Karagiannis TC. Regulation of immune responses by histone deacetylase inhibitors. ISRN Hematol 2012; 2012: 690901.
55. Xu J, Zhang X, Pelayo R, et al. Extracellular histones are major mediators of death in sepsis. Nat Med 2009; 15: 1318-21.
56. Papayannopoulos V, Metzler KD, Hakkim A, Zychlinsky A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J Cell Biol 2010; 191: 677-91.
57. Gillrie MR, Lee K, Gowda DC, et al. Plasmodium falciparum histones induce endothelial proinflammatory response and barrier dysfunction. Am J Pathol 2012; 180: 1028-39.
58. Shimaoka M, Park EJ. Advances in understanding sepsis. Eur J Anaesthesiol Suppl 2008;42:146-53.
59. Romisch J. Factor VII activating protease (FSAP): a novel protease in hemostasis. Biol Chem 2002; 383: 1119-24.
60. Wygrecka M, Morty RE, Markart P, et al. Plasminogen activator inhibitor-1 is an inhibitor of factor VII-activating protease in patients with acute respiratory distress syndrome. J Biol Chem 2007; 282: 21671-82.
61. Yamamichi S, Fujiwara Y, Kikuchi T, Nishitani M, Matsushita Y, Hasumi K. Extracellular histone induces plasma hyaluronan-binding protein (factor VII activating protease) activation in vivo. Biochem Biophys Res Commun 2011; 409: 483-8.
62. Stephan F, Aarden LA, Zeerleder S. FSAP, a new player in inflammation? Hamostaseologie 2012; 32: 51-5.
63. Golias C, Charalabopoulos A, Stagikas D, Charalabopoulos K, Batistatou A. The kinin system--bradykinin: biological effects and clinical implications. Multiple role of the kinin system--bradykinin. Hippokratia 2007; 11: 124-8.
64. Papayannopoulos V, Staab D, Zychlinsky A. Neutrophil elastase enhances sputum solubilization in cystic fibrosis patients receiving DNase therapy. PLoS One 2011; 6: e28526.
65. Wang Y, Wysocka J, Sayegh J, et al. Human PAD4 regulates histone arginine methylation levels via demethylimination. Science 2004; 306: 279-83.
66. Wang Y, Li M, Stadler S, et al. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol 2009; 184: 205-13.
67. Vettese-Dadey M, Walter P, Chen H, Juan LJ, Workman JL. Role of the histone amino termini in facilitated binding of a transcription factor, GAL4-AH, to nucleosome cores. Mol Cell Biol 1994; 14: 970-81.
68. Godde JS, Nakatani Y, Wolffe AP. The amino-terminal tails of the core histones and the translational position of the TATA box determine TBP/TFIIA association with nucleosomal DNA. Nucleic Acids Res 1995; 23: 4557-64.
69. Sarangi PP, Lee HW, Kim M. Activated protein C action in inflammation. Br J Haematol 2010; 148: 817-33.
70. Toltl LJ, Austin RC, Liaw PC. Activated protein C modulates inflammation, apoptosis and tissue factor procoagulant activity by regulating endoplasmic reticulum calcium depletion in blood monocytes. J Thromb Haemost 2011; 9: 582-92.
71. Hayakawa M, Katabami K, Wada T, et al. Sivelestat (selective neutrophil elastase inhibitor) improves the mortality rate of sepsis associated with both acute respiratory distress syndrome and disseminated intravascular coagulation patients. Shock 2010; 33: 14-8.
72. Suda K, Takeuchi H, Hagiwara T, et al. Neutrophil elastase inhibitor improves survival of rats with clinically relevant sepsis. Shock 2010; 33: 526-31.
73. Ullrich O, Reinheckel T, Sitte N, Hass R, Grune T, Davies KJ. Poly-ADP ribose polymerase activates nuclear proteasome to degrade oxidatively damaged histones. Proc Natl Acad Sci U S A 1999; 96: 6223-8.
74. Zhang D, Pasternack MS, Beresford PJ, Wagner L, Greenberg AH, Lieberman J. Induction of rapid histone degradation by the cytotoxic T lymphocyte protease Granzyme A. J Biol Chem 2001; 276: 3683-90.
75. Berger SL. The complex language of chromatin regulation during transcription. Nature 2007; 447: 407-12.