Informacja

Drogi użytkowniku, aplikacja do prawidłowego działania wymaga obsługi JavaScript. Proszę włącz obsługę JavaScript w Twojej przeglądarce.

Przeglądasz jako GOŚĆ
Tytuł pozycji:

Nucleus-specific linker histones Hho1 and Mlh1 form distinct protein interactions during growth, starvation and development in Tetrahymena thermophila.

Tytuł :
Nucleus-specific linker histones Hho1 and Mlh1 form distinct protein interactions during growth, starvation and development in Tetrahymena thermophila.
Autorzy :
Nabeel-Shah S; Department of Chemistry and Biology, Ryerson University, 350 Victoria St., Toronto, M5B 2K3, Canada.; Donnelly Centre, University of Toronto, Toronto, M5S 3E1, Canada.; Department of Molecular Genetics, University of Toronto, Toronto, M5S 1A8, Canada.
Ashraf K; Department of Biology, York University, 4700 Keele St., Toronto, M3J 1P3, Canada.
Saettone A; Department of Chemistry and Biology, Ryerson University, 350 Victoria St., Toronto, M5B 2K3, Canada.
Garg J; Department of Biology, York University, 4700 Keele St., Toronto, M3J 1P3, Canada.
Derynck J; Department of Chemistry and Biology, Ryerson University, 350 Victoria St., Toronto, M5B 2K3, Canada.
Lambert JP; Department of Molecular Medicine and Cancer Research Centre, Université Laval, Quebec, Canada.; CHU de Québec Research Center, CHUL, 2705 Laurier Boulevard, Quebec, G1V 4G2, Canada.
Pearlman RE; Department of Biology, York University, 4700 Keele St., Toronto, M3J 1P3, Canada. .
Fillingham J; Department of Chemistry and Biology, Ryerson University, 350 Victoria St., Toronto, M5B 2K3, Canada. .
Pokaż więcej
Źródło :
Scientific reports [Sci Rep] 2020 Jan 13; Vol. 10 (1), pp. 168. Date of Electronic Publication: 2020 Jan 13.
Typ publikacji :
Journal Article; Research Support, Non-U.S. Gov't
Język :
English
Imprint Name(s) :
Original Publication: London : Nature Publishing Group, copyright 2011-
MeSH Terms :
Gene Expression Regulation, Developmental*
High Mobility Group Proteins/*metabolism
Histones/*metabolism
MutL Protein Homolog 1/*metabolism
Proteome/*analysis
Protozoan Proteins/*metabolism
Tetrahymena thermophila/*growth & development
Amino Acid Sequence ; Animals ; Cell Nucleus/genetics ; Cell Nucleus/metabolism ; Chromatin/genetics ; Chromatin/metabolism ; Gene Expression Regulation ; High Mobility Group Proteins/genetics ; MutL Protein Homolog 1/genetics ; Protein Interaction Domains and Motifs ; Protozoan Proteins/genetics ; Starvation ; Tetrahymena thermophila/genetics ; Tetrahymena thermophila/metabolism
References :
Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F. & Richmond, T. J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251–60 (1997). (PMID: 930583710.1038/384449305837)
Fyodorov, D. V., Zhou, B.-R., Skoultchi, A. I. & Bai, Y. Emerging roles of linker histones in regulating chromatin structure and function. Nat. Rev. Mol. Cell Biol. 19, 192–206 (2018). (PMID: 2901828210.1038/nrm.2017.9429018282)
Mendiratta, S., Gatto, A. & Almouzni, G. Histone supply: Multitiered regulation ensures chromatin dynamics throughout the cell cycle. J. Cell Biol. 39–54, https://doi.org/10.1083/jcb.201807179 (2018). (PMID: 3025785110.1083/jcb.20180717930257851)
Biterge, B. & Schneider, R. Histone variants: key players of chromatin. Cell Tissue Res. 356, 457–66 (2014). (PMID: 2478114810.1007/s00441-014-1862-424781148)
Ponte, I., Romero, D., Yero, D., Suau, P. & Roque, A. Complex Evolutionary History of the Mammalian Histone H1.1-H1.5 Gene Family. Mol. Biol. Evol. 34, 545–558 (2017). (PMID: 281007895400378)
Pan, C. & Fan, Y. Role of H1 linker histones in mammalian development and stem cell differentiation. Biochim. Biophys. Acta 1859, 496–509 (2016). (PMID: 2668974710.1016/j.bbagrm.2015.12.00226689747)
Izzo, A., Kamieniarz, K. & Schneider, R. The histone H1 family: specific members, specific functions? Biol. Chem. 389, 333–43 (2008). (PMID: 1820834610.1515/BC.2008.03718208346)
Patterton, H. G., Landel, C. C., Landsman, D., Peterson, C. L. & Simpson, R. T. The Biochemical and Phenotypic Characterization of Hho1p, the Putative Linker Histone H1 of Saccharomyces cerevisiae. J. Biol. Chem. 273, 7268–7276 (1998). (PMID: 951642010.1074/jbc.273.13.72689516420)
Flickinger, R. A. Possible role of H1 histone in replication timing. Dev. Growth Differ. 57, 1–9 (2015). (PMID: 2549521410.1111/dgd.1219025495214)
Andreyeva, E. N. et al. Regulatory functions and chromatin loading dynamics of linker histone H1 during endoreplication in Drosophila. Genes Dev. 31, 603–616 (2017). (PMID: 28404631539305510.1101/gad.295717.116)
Hergeth, S. P. & Schneider, R. The H1 linker histones: multifunctional proteins beyond the nucleosomal core particle. EMBO Rep. 16, 1439–53 (2015). (PMID: 26474902464149810.15252/embr.201540749)
Li, X., Egervari, G., Wang, Y., Berger, S. L. & Lu, Z. Regulation of chromatin and gene expression by metabolic enzymes and metabolites. Nat. Rev. Mol. Cell Biol. 19, 563–578 (2018). (PMID: 29930302690708710.1038/s41580-018-0029-7)
Yang, W. et al. PKM2 phosphorylates histone H3 and promotes gene transcription and tumorigenesis. Cell 150, 685–96 (2012). (PMID: 22901803343102010.1016/j.cell.2012.07.018)
Grover, P., Asa, J. S. & Campos, E. I. H3–H4 Histone Chaperone Pathways. Annu. Rev. Genet. 52, 109–130 (2018). (PMID: 3018340610.1146/annurev-genet-120417-03154730183406)
Tagami, H., Ray-Gallet, D., Almouzni, G. & Nakatani, Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116, 51–61 (2004). (PMID: 1471816610.1016/S0092-8674(03)01064-X14718166)
Ray-Gallet, D. et al. HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol. Cell 9, 1091–100 (2002). (PMID: 1204974410.1016/S1097-2765(02)00526-912049744)
Ray-Gallet, D. et al. Dynamics of histone H3 deposition in vivo reveal a nucleosome gap-filling mechanism for H3.3 to maintain chromatin integrity. Mol. Cell 44, 928–41 (2011). (PMID: 2219596610.1016/j.molcel.2011.12.00622195966)
Pardal, A. J., Fernandes-Duarte, F. & Bowman, A. J. The histone chaperoning pathway: from ribosome to nucleosome. Essays Biochem. 63, 29–43 (2019). (PMID: 31015382648478310.1042/EBC20180055)
De Koning, L., Corpet, A., Haber, J. E. & Almouzni, G. Histone chaperones: an escort network regulating histone traffic. Nat. Struct. Mol. Biol. 14, 997–1007 (2007). (PMID: 1798496210.1038/nsmb131817984962)
Zhang, P., Branson, O. E., Freitas, M. A. & Parthun, M. R. Identification of replication-dependent and replication-independent linker histone complexes: Tpr specifically promotes replication-dependent linker histone stability. BMC Biochem. 17, 18 (2016). (PMID: 27716023504559810.1186/s12858-016-0074-9)
Richardson, R. T. et al. Characterization of the histone H1-binding protein, NASP, as a cell cycle-regulated somatic protein. J. Biol. Chem. 275, 30378–30386 (2000). (PMID: 1089341410.1074/jbc.M00378120010893414)
Wang, H., Walsh, S. T. R. & Parthun, M. R. Expanded binding specificity of the human histone chaperone NASP. Nucleic Acids Res. 36, 5763–5772 (2008). (PMID: 18782834256687910.1093/nar/gkn574)
Wang, H., Ge, Z., Walsh, S. T. R. & Parthun, M. R. The human histone chaperone sNASP interacts with linker and core histones through distinct mechanisms. Nucleic Acids Res. 40, 660–669 (2012). (PMID: 2196553210.1093/nar/gkr78121965532)
Harshman, S. W., Young, N. L., Parthun, M. R. & Freitas, M. A. H1 histones: current perspectives and challenges. Nucleic Acids Res. 41, 9593–609 (2013). (PMID: 23945933383480610.1093/nar/gkt700)
Ashraf, K. et al. Proteomic Analysis of Histones H2A/H2B and Variant Hv1 in Tetrahymena thermophila Reveals an Ancient Network of Chaperones. Mol. Biol. Evol. 36, 1037–1055 (2019). (PMID: 30796450650208510.1093/molbev/msz039)
Saettone, A. et al. Functional Proteomics of Nuclear Proteins in Tetrahymena thermophila: A Review. Genes (Basel). 10, (333 (2019).
Garg, J. et al. The Med31 Conserved Component of the Divergent Mediator Complex in Tetrahymena thermophila Participates in Developmental Regulation. Curr. Biol., https://doi.org/10.1016/j.cub.2019.06.052 (2019). (PMID: 3128099410.1016/j.cub.2019.06.05231280994)
Martindale, D. W., Allis, C. D. & Bruns, P. J. Conjugation in Tetrahymena thermophila. A temporal analysis of cytological stages. Exp. Cell Res. 140, 227–36 (1982). (PMID: 710620110.1016/0014-4827(82)90172-07106201)
Yao, M.-C. C., Choi, J., Yokoyama, S., Austerberry, C. F. & Yao, C.-H. H. DNA elimination in Tetrahymena: a developmental process involving extensive breakage and rejoining of DNA at defined sites. Cell 36, 433–40 (1984). (PMID: 631902310.1016/0092-8674(84)90236-86319023)
Yao, M.-C., Fuller, P. & Xi, X. Programmed DNA deletion as an RNA-guided system of genome defense. Science 300, 1581–4 (2003). (PMID: 1279199610.1126/science.108473712791996)
Mochizuki, K. & Gorovsky, M. A. RNA polymerase II localizes in Tetrahymena thermophila meiotic micronuclei when micronuclear transcription associated with genome rearrangement occurs. Eukaryot. Cell 3, 1233–40 (2004). (PMID: 1547025252260410.1128/EC.3.5.1233-1240.2004)
Bruns, P. J. & Brussard, T. B. Pair formation inTetrahymena pyriformis, an inducible developmental system. J. Exp. Zool. 188, 337–344 (1974). (PMID: 420919510.1002/jez.14018803094209195)
Bruns, P. J. & Palestine, R. F. Costimulation in Tetrahymena pyriformis: a developmental interaction between specially prepared cells. Dev. Biol. 42, 75–83 (1975). (PMID: 80346210.1016/0012-1606(75)90315-2803462)
Shen, X., Yu, L., Weir, J. W. & Gorovsky, M. A. Linker histones are not essential and affect chromatin condensation in vivo. Cell 82, 47–56 (1995). (PMID: 760678410.1016/0092-8674(95)90051-97606784)
HAYASHI, T., HAYASHI, H. & IWAI, K. Tetrahymena Histone H1. Isolation and Amino Acid Sequence Lacking the Central Hydrophobic Domain Conserved in Other H1 Histones1. J. Biochem. 102, 369–376 (1987). (PMID: 311778310.1093/oxfordjournals.jbchem.a1220633117783)
Wu, M., Allis, C. D., Richman, R., Cook, R. G. & Gorovsky, M. A. An intervening sequence in an unusual histone H1 gene of Tetrahymena thermophila. Proc. Natl. Acad. Sci. 83, 8674–8678 (1986). (PMID: 346497610.1073/pnas.83.22.86743464976)
Dou, Y., Mizzen, C. A., Abrams, M., Allis, C. D. & Gorovsky, M. A. Phosphorylation of linker histone H1 regulates gene expression in vivo by mimicking H1 removal. Mol. Cell 4, 641–7 (1999). (PMID: 1054929610.1016/S1097-2765(00)80215-410549296)
Dou, Y. & Gorovsky, M. A. Phosphorylation of linker histone H1 regulates gene expression in vivo by creating a charge patch. Mol. Cell 6, 225–31 (2000). (PMID: 1098397110.1016/S1097-2765(00)00024-110983971)
Dou, Y. & Gorovsky, M. A. Regulation of transcription by H1 phosphorylation in Tetrahymena is position independent and requires clustered sites. Proc. Natl. Acad. Sci. USA 99, 6142–6 (2002). (PMID: 1197204510.1073/pnas.09202959911972045)
Wu, M. et al. Four distinct and unusual linker proteins in a mitotically dividing nucleus are derived from a 71-kilodalton polyprotein, lack p34cdc2 sites, and contain protein kinase A sites. Mol. Cell. Biol. 14, 10–20 (1994). (PMID: 826457835835110.1128/MCB.14.1.10)
Iwamoto, M. et al. Nuclear localization signal targeting to macronucleus and micronucleus in binucleated ciliate Tetrahymena thermophila. Genes Cells 23, 568–579 (2018). (PMID: 2988262010.1111/gtc.1260229882620)
Roque, A., Iloro, I., Ponte, I., Arrondo, J. L. R. & Suau, P. DNA-induced secondary structure of the carboxyl-terminal domain of histone H1. J. Biol. Chem. 280, 32141–7 (2005). (PMID: 1600655510.1074/jbc.M50563620016006555)
Teo, G. et al. SAINTexpress: improvements and additional features in Significance Analysis of INTeractome software. J. Proteomics 100, 37–43 (2014). (PMID: 2451353310.1016/j.jprot.2013.10.02324513533)
Kataoka, K. & Mochizuki, K. Heterochromatin aggregation during DNA elimination in Tetrahymena is facilitated by a prion-like protein. J. Cell Sci. 130, 480–489 (2017). (PMID: 2790924510.1242/jcs.19550327909245)
Miao, W. et al. Microarray analyses of gene expression during the Tetrahymena thermophila life cycle. PLoS One 4, e4429 (2009). (PMID: 19204800263687910.1371/journal.pone.0004429)
González-Romero, R., Eirín-López, J. M. & Ausió, J. Evolution of high mobility group nucleosome-binding proteins and its implications for vertebrate chromatin specialization. Mol. Biol. Evol. 32, 121–31 (2015). (PMID: 2528180810.1093/molbev/msu28025281808)
Hock, R., Furusawa, T., Ueda, T. & Bustin, M. HMG chromosomal proteins in development and disease. Trends Cell Biol. 17, 72–9 (2007). (PMID: 1716956110.1016/j.tcb.2006.12.00117169561)
Xu, J., Tian, H., Liu, X., Wang, W. & Liang, A. Localization and functional analysis of HmgB3p, a novel protein containing high-mobility-group-box domain from Tetrahymena thermophila. Gene 526, 87–95 (2013). (PMID: 2368528110.1016/j.gene.2013.05.00623685281)
Qiao, J., Xu, J., Bo, T. & Wang, W. Micronucleus-specific histone H1 is required for micronuclear chromosome integrity in Tetrahymena thermophila. PLoS One 12, e0187475 (2017). (PMID: 29095884566785610.1371/journal.pone.0187475)
Valpuesta, J. M., Martín-Benito, J., Gómez-Puertas, P., Carrascosa, J. L. & Willison, K. R. Structure and function of a protein folding machine: the eukaryotic cytosolic chaperonin CCT. FEBS Lett. 529, 11–6 (2002). (PMID: 1235460510.1016/S0014-5793(02)03180-012354605)
Mayer, M. P. & Bukau, B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 62, 670–84 (2005). (PMID: 15770419277384110.1007/s00018-004-4464-6)
Campos, E. I. et al. The program for processing newly synthesized histones H3.1 and H4. Nat. Struct. Mol. Biol. 17, 1343–51 (2010). (PMID: 20953179298897910.1038/nsmb.1911)
Niessen, M., Schneiter, R. & Nothiger, R. Molecular Identification of virilizer, a Gene Required for the Expression of the Sex-Determining Gene Sex-lethal in Drosophila melanogaster (2001).
Suganuma, T., Pattenden, S. G. & Workman, J. L. Diverse functions of WD40 repeat proteins in histone recognition. Genes Dev. 22, 1265–8 (2008). (PMID: 18483215273241010.1101/gad.1676208)
Downs, J. A., Kosmidou, E., Morgan, A. & Jackson, S. P. Suppression of homologous recombination by the Saccharomyces cerevisiae linker histone. Mol. Cell 11, 1685–92 (2003). (PMID: 1282097910.1016/S1097-2765(03)00197-712820979)
Garg, J. et al. Conserved Asf1-importinβ physical interaction in growth and sexual development in the ciliate Tetrahymena thermophila. J. Proteomics 94, 311–326 (2013). (PMID: 2412053110.1016/j.jprot.2013.09.01824120531)
Nabeel-Shah, S., Ashraf, K., Pearlman, R. E. & Fillingham, J. Molecular evolution of NASP and conserved histone H3/H4 transport pathway. BMC Evol. Biol. 14, 139 (2014). (PMID: 24951090408232310.1186/1471-2148-14-139)
Mosammaparast, N. et al. Nuclear import of histone H2A and H2B is mediated by a network of karyopherins. J. Cell Biol. 153, 251–62 (2001). (PMID: 11309407216946210.1083/jcb.153.2.251)
Shimada, M. et al. Gene-Specific H1 Eviction through a Transcriptional Activator→p300→NAP1→H1 Pathway. Mol. Cell 74, 268–283.e5 (2019). (PMID: 3090254610.1016/j.molcel.2019.02.01630902546)
Thorslund, T. et al. Histone H1 couples initiation and amplification of ubiquitin signalling after DNA damage. Nature 527, 389–393 (2015). (PMID: 2650303810.1038/nature1540126503038)
Mandemaker, I. K. et al. DNA damage-induced histone H1 ubiquitylation is mediated by HUWE1 and stimulates the RNF8-RNF168 pathway. Sci. Rep. 7, 15353 (2017). (PMID: 29127375568167310.1038/s41598-017-15194-y)
Lu, X. et al. Linker histone H1 is essential for Drosophila development, the establishment of pericentric heterochromatin, and a normal polytene chromosome structure. Genes Dev. 23, 452–465 (2009). (PMID: 19196654264864810.1101/gad.1749309)
Yue, Y. et al. VIRMA mediates preferential m6A mRNA methylation in 3′UTR and near stop codon and associates with alternative polyadenylation. Cell Discov. 4, 10 (2018). (PMID: 29507755582692610.1038/s41421-018-0019-0)
Kim, D. I. et al. An improved smaller biotin ligase for BioID proximity labeling. Mol. Biol. Cell 27, 1188–96 (2016). (PMID: 26912792483187310.1091/mbc.E15-12-0844)
Fillingham, J. S., Bruno, D. & Pearlman, R. E. Cis-acting requirements in flanking DNA for the programmed elimination of mse2.9: a common mechanism for deletion of internal eliminated sequences from the developing macronucleus of Tetrahymena thermophila. Nucleic Acids Res. 29, 488–98 (2001). (PMID: 111396192967710.1093/nar/29.2.488)
Fillingham, J. S. et al. Molecular genetic analysis of an SNF2/brahma-related gene in Tetrahymena thermophila suggests roles in growth and nuclear development. Eukaryot. Cell 5, 1347–59 (2006). (PMID: 16896218153913610.1128/EC.00149-06)
Saettone, A. et al. The bromodomain-containing protein Ibd1 links multiple chromatin-related protein complexes to highly expressed genes in Tetrahymena thermophila. Epigenetics Chromatin 11, 10 (2018). (PMID: 29523178584407110.1186/s13072-018-0180-6)
Liu, G. et al. Data Independent Acquisition analysis in ProHits 4.0. J. Proteomics 149, 64–68 (2016). (PMID: 27132685507980110.1016/j.jprot.2016.04.042)
Cline, M. S. et al. Integration of biological networks and gene expression data using Cytoscape. Nat. Protoc. 2, 2366–82 (2007). (PMID: 17947979368558310.1038/nprot.2007.324)
Letunic, I., Doerks, T. & Bork, P. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 40, D302–5 (2012). (PMID: 2205308410.1093/nar/gkr93122053084)
Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol. 33, 1870–1874 (2016). (PMID: 2700490410.1093/molbev/msw05427004904)
Yang, J. et al. The I-TASSER Suite: protein structure and function prediction. Nat. Methods 12, 7–8 (2015). (PMID: 25549265442866810.1038/nmeth.3213)
Buchan, D. W. A. & Jones, D. T. The PSIPRED Protein Analysis Workbench: 20 years on. Nucleic Acids Res., https://doi.org/10.1093/nar/gkz297 (2019). (PMID: 31251384660244510.1093/nar/gkz297)
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–5 (2012). (PMID: 229308342293083410.1038/nmeth.2089)
Substance Nomenclature :
0 (Chromatin)
0 (High Mobility Group Proteins)
0 (Histones)
0 (Proteome)
0 (Protozoan Proteins)
EC 3.6.1.3 (MutL Protein Homolog 1)
Entry Date(s) :
Date Created: 20200115 Date Completed: 20201112 Latest Revision: 20210112
Update Code :
20210210
PubMed Central ID :
PMC6957481
DOI :
10.1038/s41598-019-56867-0
PMID :
31932604
Czasopismo naukowe
Chromatin organization influences most aspects of gene expression regulation. The linker histone H1, along with the core histones, is a key component of eukaryotic chromatin. Despite its critical roles in chromatin structure and function and gene regulation, studies regarding the H1 protein-protein interaction networks, particularly outside of Opisthokonts, are limited. The nuclear dimorphic ciliate protozoan Tetrahymena thermophila encodes two distinct nucleus-specific linker histones, macronuclear Hho1 and micronuclear Mlh1. We used a comparative proteomics approach to identify the Hho1 and Mlh1 protein-protein interaction networks in Tetrahymena during growth, starvation, and sexual development. Affinity purification followed by mass spectrometry analysis of the Hho1 and Mlh1 proteins revealed a non-overlapping set of co-purifying proteins suggesting that Tetrahymena nucleus-specific linker histones are subject to distinct regulatory pathways. Furthermore, we found that linker histones interact with distinct proteins under the different stages of the Tetrahymena life cycle. Hho1 and Mlh1 co-purified with several Tetrahymena-specific as well as conserved interacting partners involved in chromatin structure and function and other important cellular pathways. Our results suggest that nucleus-specific linker histones might be subject to nucleus-specific regulatory pathways and are dynamically regulated under different stages of the Tetrahymena life cycle.
Zaloguj się, aby uzyskać dostęp do pełnego tekstu.

Ta witryna wykorzystuje pliki cookies do przechowywania informacji na Twoim komputerze. Pliki cookies stosujemy w celu świadczenia usług na najwyższym poziomie, w tym w sposób dostosowany do indywidualnych potrzeb. Korzystanie z witryny bez zmiany ustawień dotyczących cookies oznacza, że będą one zamieszczane w Twoim komputerze. W każdym momencie możesz dokonać zmiany ustawień dotyczących cookies