Histone H3 phosphorylation: Universal code or lineage specific dialects?

Abstract

Post-translational modifications of histones modulate the functional landscape of chromatin and impinge on many DNA-mediated processes. Phosphorylation of histone H3 plays a role in the regulation of gene expression and in chromosome condensation/ segregation. Certain evolutionarily conserved residues on histone H3, namely Thr3, Ser10, Thr11 and Ser28, are phosphorylated during interphase or mitosis in both metazoa and plants. However, many of the kinases involved in these events appear to have evolved independently in different lineages. Likewise, the mechanistic function of specific phosphorylated amino acids, although poorly understood, also seems to differ among eukaryotes. Moreover, some modifications, such as phosphorylation of histone H3 Ser10, appear to have both a positive and a negative connotation and only become meaningful in combination with other histone marks within a particular chromatin context. Thus, a detailed understanding of the influence of histone H3 phosphorylation on biological processes may require learning organismal dialects of the histone code.

Phosphorylation of Histone H2A at Serine 95: A Plant-Specific Mark Involved in Flowering Time Regulation and H2A.Z Deposition

“…In the alga Chlamydomonas, MUT9p, which is related to casein kinase I, is capable of phosphorylating H3 at threonine 3 (Casas-Mollano et al, 2008). The Arabidopsis genome encodes four proteins (MLK1, MLK2, MLK3, and MLK4) related to MUT9p (Cerutti and Casas-Mollano, 2009;Wang et al, 2015;Huang et al, 2016). These four proteins were copurified with the evening complex, which is composed of EARLY FLOWERING4 (ELF4), ELF3, and LUX ARRHYTHMO (Huang et al, 2016).…”

“…Phosphorylation of H3 at serine 10, serine 28, threonine 3, and threonine 11 is evolutionarily conserved in yeast, mammalian cells, and plants (Cerutti and Casas-Mollano, 2009;Banerjee and Chakravarti, 2011;Rossetto et al, 2012). The phosphorylation of H3 at serine 10 (H3S10ph) by MAP kinase signaling stimulates the acetylation of lysine 14 in H3, which in turn recruits Transcription Factor II D to activate gene expression (Cheung et al, 2000;Lo et al, 2000;Hirota et al, 2005).…”

“…H3 serine28 phosphorylation (H3S28ph), generated by MITOGEN-AND STRESS-ACTIVATED PROTEIN KINASE1, not only prevents recruitment of the gene-silencing Polycomb-repressive complexes and their methylation of H3K27, but it also induces a switch from methylation to acetylation at H3K27 (Lau and Cheung, 2011). In mammalian cells and plants, phosphorylation of H3 at threonine 3 (H3T3ph) generated by the mitosis-activated Haspin kinase functions in chromosome alignment and centromere cohesion (Dai et al, 2005;Cerutti and Casas-Mollano, 2009). However, the phosphorylation of H3 at threonine 3 by the kinase MUT9p is associated with transcriptional silencing in Chlamydomonas reinhardtii (Ivaldi et al, 2007).…”

Osmotic stress induces phosphorylation of histone H3 at threonine 3 in pericentromeric regions of Arabidopsis thaliana

“…Phosphorylation of histone H3 is evolutionarily conserved at several sites including Ser 10 and 28 (H3S10ph and H3S28ph) and Thr 3 and 11 (H3T3ph and H3T11ph) (11)(12)(13)15). In metazoans, a variety of environmental stimuli can trigger histone H3 phosphorylation, both globally and at specific genes in interphase cells (11,14,(17)(18)(19).…”

“…Histone phosphorylation can occur on serine, threonine, and/or tyrosine residues and is generally induced in response to extracellular signals, DNA damage, or entry into mitosis/meiosis (11)(12)(13)(14)(15)(16). Phosphorylation of histone H3 is evolutionarily conserved at several sites including Ser 10 and 28 (H3S10ph and H3S28ph) and Thr 3 and 11 (H3T3ph and H3T11ph) (11)(12)(13)15).…”