Histone modifications and apoptosis: cause or consequence?

Since the first description of apoptosis, genetic and biochemical studies have led to a greater understanding of the multiple pathways that eukaryotic cells can take to terminate their existence. These findings have also proven useful in understanding the development of various diseases such as AIDS, Alzheimer's, and Parkinson's and have provided potential targets for possible therapies. Despite all these studies, the mechanism of chromatin condensation, a morphological hallmark of apoptosis, remains elusive. This review describes the work to date on the post-translational modifications of histones during apoptosis and discusses the models that have been presented to explain the apoptotic condensation of chromatin.

[1]  D. Glover,et al.  Drosophila Aurora B Kinase Is Required for Histone H3 Phosphorylation and Condensin Recruitment during Chromosome Condensation and to Organize the Central Spindle during Cytokinesis , 2001, The Journal of cell biology.

[2]  J. Lieberman,et al.  Induction of Rapid Histone Degradation by the Cytotoxic T Lymphocyte Protease Granzyme A* , 2001, The Journal of Biological Chemistry.

[3]  W. Albig,et al.  Rapid Dephosphorylation of H1 Histones after Apoptosis Induction* , 2000, The Journal of Biological Chemistry.

[4]  K. V. van Holde,et al.  Linker histone binding and displacement: versatile mechanism for transcriptional regulation , 2000, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[5]  Zu-Wen Sun,et al.  Mitotic Phosphorylation of Histone H3 Is Governed by Ipl1/aurora Kinase and Glc7/PP1 Phosphatase in Budding Yeast and Nematodes , 2000, Cell.

[6]  S. Osmani,et al.  Mitotic Histone H3 Phosphorylation by the NIMA Kinase in Aspergillus nidulans , 2000, Cell.

[7]  W. D. Cress,et al.  Histone deacetylases, transcriptional control, and cancer , 2000, Journal of cellular physiology.

[8]  C. Allis,et al.  Acetylation and chromosomal functions. , 2000, Current opinion in cell biology.

[9]  U. Weidle,et al.  Inhibition of histone deacetylases: a new strategy to target epigenetic modifications for anticancer treatment. , 2000, Anticancer research.

[10]  A. Wolffe,et al.  Review: chromatin structural features and targets that regulate transcription. , 2000, Journal of structural biology.

[11]  Y. Pommier,et al.  Initiation of DNA Fragmentation during Apoptosis Induces Phosphorylation of H2AX Histone at Serine 139* , 2000, The Journal of Biological Chemistry.

[12]  Peng Li,et al.  Cleavage Preferences of the Apoptotic Endonuclease DFF40 (Caspase-activated DNase or Nuclease) on Naked DNA and Chromatin Substrates* , 2000, Journal of Biological Chemistry.

[13]  K. Ajiro.  Histone H2B Phosphorylation in Mammalian Apoptotic Cells , 2000, The Journal of Biological Chemistry.

[14]  T. Mizuochi,et al.  Role of macrophage lysosomal enzymes in the degradation of nucleosomes of apoptotic cells. , 1999, Journal of immunology.

[15]  G. Salvesen,et al.  Cleavage of Automodified Poly(ADP-ribose) Polymerase during Apoptosis , 1999, The Journal of Biological Chemistry.

[16]  M. Inagaki,et al.  Identification of a Novel Phosphorylation Site on Histone H3 Coupled with Mitotic Chromosome Condensation* , 1999, The Journal of Biological Chemistry.

[17]  G. Poirier,et al.  Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. , 1999, The Biochemical journal.

[18]  D. Bernhard,et al.  Interaction between dexamethasone and butyrate in apoptosis induction: non-additive in thymocytes and synergistic in a T cell-derived leukemia cell line , 1999, Cell Death and Differentiation.

[19]  A. Yamauchi,et al.  Involvement of Histone Phosphorylation in Thymocyte Apoptosis by Protein Phosphatase Inhibitors , 1999, IUBMB life.

[20]  J. O. Thomas,et al.  Histone H1: location and role. , 1999, Current opinion in cell biology.

[21]  Anne E Carpenter,et al.  Large-scale chromatin structure and function. , 1999, Current opinion in cell biology.

[22]  X. Liu,et al.  Activation of the Apoptotic Endonuclease DFF40 (Caspase-activated DNase or Nuclease) , 1999, The Journal of Biological Chemistry.

[23]  M. Roberge,et al.  Phosphorylation-induced Rearrangement of the Histone H3 NH2-terminal Domain during Mitotic Chromosome Condensation , 1999, The Journal of cell biology.

[24]  L. Burgoyne.  The mechanisms of pyknosis: hypercondensation and death. , 1999, Experimental cell research.

[25]  J. Velours,et al.  Isolation of Supernumerary Yeast ATP Synthase Subunits e and i , 1999, The Journal of Biological Chemistry.

[26]  C. Allis,et al.  Chromatin Condensation Is Not Associated with Apoptosis* , 1998, The Journal of Biological Chemistry.

[27]  E. Rogakou,et al.  DNA Double-stranded Breaks Induce Histone H2AX Phosphorylation on Serine 139* , 1998, The Journal of Biological Chemistry.

[28]  J. Bach,et al.  Isolation and characterization of apoptotic nucleosomes, free and complexed with lupus autoantibody generated during hybridoma B-cell apoptosis. , 1998, Journal of autoimmunity.

[29]  C. Allis,et al.  Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation , 1997, Chromosoma.

[30]  R. James,et al.  Induction of caspase-3 protease activity and apoptosis by butyrate and trichostatin A (inhibitors of histone deacetylase): dependence on protein synthesis and synergy with a mitochondrial/cytochrome c-dependent pathway. , 1997, Cancer research.

[31]  T. Khan,et al.  Apoptosis Induced by Gliotoxin Is Preceded by Phosphorylation of Histone H3 and Enhanced Sensitivity of Chromatin to Nuclease Digestion* , 1997, The Journal of Biological Chemistry.

[32]  A. Eastman,et al.  Apoptotic death in adenocarcinoma cell lines induced by butyrate and other histone deacetylase inhibitors. , 1997, Biochemical pharmacology.

[33]  M. Yoshida,et al.  Biochemical differences between staurosporine-induced apoptosis and premature mitosis. , 1997, Experimental cell research.

[34]  S Parodi,et al.  The Condensation of Chromatin in Apoptotic Thymocytes Shows a Specific Structural Change* , 1997, The Journal of Biological Chemistry.

[35]  H. Kizaki,et al.  Peptidyl aldehyde inhibitors of proteasome induce apoptosis rapidly in mouse lymphoma RVC cells. , 1997, Journal of biochemistry.

[36]  A. Dahlqvist,et al.  Lipid Dependence and Basic Kinetics of the Purified 1,2-Diacylglycerol 3-Glucosyltransferase from Membranes of Acholeplasma laidlawii* , 1997, The Journal of Biological Chemistry.

[37]  E. White,et al.  Lamin proteolysis facilitates nuclear events during apoptosis , 1996, The Journal of cell biology.

[38]  B Bartholomew,et al.  An Asymmetric Model for the Nucleosome: A Binding Site for Linker Histones Inside the DNA Gyres , 1996, Science.

[39]  T. Furukubo,et al.  Involvement of histone hyperacetylation in triggering DNA fragmentation of rat thymocytes undergoing apoptosis , 1996, FEBS letters.

[40]  M. Vodenicharov,et al.  Isolation of chromatin fragments released by apoptotic cells. , 1996, Cancer letters.

[41]  J. Davie.  Histone modifications, chromatin structure, and the nuclear matrix , 1996, Journal of cellular biochemistry.

[42]  C. Joe,et al.  Poly(ADP-ribosyl)ation of Histone H1 Correlates with Internucleosomal DNA Fragmentation during Apoptosis (*) , 1996, The Journal of Biological Chemistry.

[43]  M. Sofroniew,et al.  Nerve growth factor withdrawal induces the apoptotic death of developing septal cholinergic neuronsvitro: Protection by cyclic AMP analogue and high potassium , 1996, Neuroscience.

[44]  C. Allis,et al.  Increased Phosphorylation of Histone H1 in Mouse Fibroblasts Transformed with Oncogenes or Constitutively Active Mitogen-activated Protein Kinase Kinase (*) , 1995, The Journal of Biological Chemistry.

[45]  A. Harris,et al.  Inactivation of Cdc2 increases the level of apoptosis induced by DNA damage. , 1995, Journal of cell science.

[46]  C. Gao,et al.  Induction of cyclin B and H1 kinase activity in apoptotic PC12 cells. , 1995, Experimental cell research.

[47]  D. Green,et al.  p34cdc2 and apoptosis. , 1995, Science.

[48]  V. Metelev,et al.  Induction of apoptosis in uninfected lymphocytes by HIV-1 Tat protein. , 1995, Science.

[49]  K. Marushige,et al.  Disappearance of ubiquitinated histone H2A during chromatin condensation in TGF beta 1-induced apoptosis. , 1995, Anticancer research.

[50]  A. Wolffe,et al.  Nucleosomal anatomy--where are the histones? , 1995, BioEssays : news and reviews in molecular, cellular and developmental biology.

[51]  P. Walker,et al.  Endonuclease activities, chromatin structure, and DNA degradation in apoptosis. , 1994, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[52]  P. Kiener,et al.  Activation of p34cdc2 coincident with taxol-induced apoptosis. , 1994, Cell growth & differentiation : the molecular biology journal of the American Association for Cancer Research.

[53]  G. Cohen,et al.  Cdc2 activation is not required for thymocyte apoptosis. , 1994, Biochemical and biophysical research communications.

[54]  G. Fröschl,et al.  Chromatin condensation during apoptosis is accompanied by degradation of lamin A+B, without enhanced activation of cdc2 kinase , 1994, The Journal of cell biology.

[55]  J. Davie,et al.  Multiple functions of dynamic histone acetylation , 1994, Journal of cellular biochemistry.

[56]  Stephen S. Gisselbrecht,et al.  Activation of cyclin A-dependent protein kinases during apoptosis. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Alan P. Wolffe,et al.  Transcription: In tune with the histones , 1994, Cell.

[58]  Lianfa Shi,et al.  Premature p34cdc2 activation required for apoptosis. , 1994, Science.

[59]  R. Weichselbaum,et al.  Coinduction of c-jun gene expression and internucleosomal DNA fragmentation by ionizing radiation. , 1993, Biochemistry.

[60]  N. Davidson,et al.  Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. , 1993, Cancer research.

[61]  T. Eki,et al.  Characterization of DNA synthesis at a restrictive temperature in the temperature-sensitive mutants, tsFT5 cells, that belong to the complementation group of ts85 cells containing a thermolabile ubiquitin-activating enzyme E1. Involvement of the ubiquitin-conjugating system in DNA replication. , 1993, The Journal of biological chemistry.

[62]  L. Rubin,et al.  The cell cycle and cell death , 1993, Current Biology.

[63]  P. Ortiz de Montellano,et al.  The roles of His-64, Tyr-103, Tyr-146, and Tyr-151 in the epoxidation of styrene and beta-methylstyrene by recombinant sperm whale myoglobin. , 1993, The Journal of biological chemistry.

[64]  C. Hillyer,et al.  Induction of endonuclease-mediated apoptosis in tumor cells by C-nitroso-substituted ligands of poly(ADP-ribose) polymerase. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[65]  D. Ucker.  Death by suicide: one way to go in mammalian cellular development? , 1991, The New biologist.

[66]  T Ogura,et al.  The zinc fingers of human poly(ADP-ribose) polymerase are differentially required for the recognition of DNA breaks and nicks and the consequent enzyme activation. Other structures recognize intact DNA. , 1990, The Journal of biological chemistry.

[67]  T. Shimizu,et al.  VP-16-induced nucleotide pool changes and poly(ADP-ribose) synthesis: the role of VP-16 in interphase death. , 1989, Experimental cell research.

[68]  J. Maller,et al.  Mammalian growth-associated H1 histone kinase: a homolog of cdc2+/CDC28 protein kinases controlling mitotic entry in yeast and frog cells , 1989, Molecular and cellular biology.

[69]  C. Allis,et al.  Ubiquitinated histone H2B is preferentially located in transcriptionally active chromatin. , 1989, Biochemistry.

[70]  J. Davie,et al.  The ubiquitinated histone species are enriched in histone H1-depleted chromatin regions. , 1987, Biochimica et biophysica acta.

[71]  H. Mikawa,et al.  Prevention of adriamycin-induced interphase death by 3-aminobenzamide and nicotinamide in a human promyelocytic leukemia cell line. , 1987, Biochemical and biophysical research communications.

[72]  L. Sklar,et al.  Hydrogen peroxide-induced injury of cells and its prevention by inhibitors of poly(ADP-ribose) polymerase. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[73]  H. Yasuda,et al.  Identification of ubiquitinated histones 2A and 2B in Physarum polycephalum. Disappearance of these proteins at metaphase and reappearance at anaphase. , 1985, The Journal of biological chemistry.

[74]  L. J. Kaplan,et al.  The structure of chromatin reconstituted with phosphorylated H1. Circular dichroism and thermal denaturation studies. , 1984, The Journal of biological chemistry.

[75]  P. Mandel,et al.  Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[76]  D. Prentice,et al.  Histone H2A phosphorylation in animal cells: functional considerations. , 1982, Biochemistry.

[77]  H. Yasuda,et al.  A mouse temperature-sensitive mutant defective in H1 histone phosphorylation is defective in deoxyribonucleic acid synthesis and chromosome condensation. , 1981, Biochemistry.

[78]  S. Matsui,et al.  Disappearance of a structural chromatin protein A24 in mitosis: implications for molecular basis of chromatin condensation. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[79]  A Klug,et al.  Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin , 1979, The Journal of cell biology.

[80]  H. Busch,et al.  Isopeptide linkage between nonhistone and histone 2A polypeptides of chromosomal conjugate-protein A24. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[81]  L. R. Gurley,et al.  Histone phosphorylation in late interphase and mitosis. , 1973, Biochemical and biophysical research communications.

[82]  A. Wyllie,et al.  Apoptosis: A Basic Biological Phenomenon with Wide-ranging Implications in Tissue Kinetics , 1972, British Journal of Cancer.

[83]  Rubin Ba,et al.  On the catalytic functions of peroxidase , 1967 .

[84]  J. Workman,et al.  The many HATs of transcription coactivators. , 2000, Trends in biochemical sciences.

[85]  B. Lunenfeld,et al.  Induction of apoptosis in MDA-231 cells by protein synthesis inhibitors is suppressed by multiple agents. , 1996, Cancer investigation.

[86]  P. Walker,et al.  Degradation of nuclear matrix and DNA cleavage in apoptotic thymocytes. , 1996, Journal of cell science.

[87]  C. Bortner,et al.  The biochemistry and molecular biology of glucocorticoid-induced apoptosis in the immune system. , 1996, Recent progress in hormone research.

[88]  E. Bradbury,et al.  Reversible histone modification and the chromosome cell cycle , 1992 .

[89]  L. R. Gurley,et al.  The metabolism of histone fractions. VI. Differences in the phosphorylation of histone fractions during the cell cycle. , 1973, Archives of biochemistry and biophysics.