Putative SET-domain methyltransferases in Cryptosporidium parvum and histone methylation during infection

References

• Arisue N, Hashimoto T. Phylogeny and evolution of apicoplasts and apicomplexan parasites. Parasitol Int. 2015;64(3):254–259.
   PubMed Web of Science ®Google Scholar
• Ramirez NE, Ward LA, Sreevatsan S. A review of the biology and epidemiology of cryptosporidiosis in humans and animals. Microbes Infect. 2004;6(8):773–785.
   PubMed Web of Science ®Google Scholar
• Khalil IA, Troeger C, Rao PC, et al. Morbidity, mortality, and long-term consequences associated with diarrhoea from Cryptosporidium infection in children younger than 5 years: a meta-analyses study. Lancet Glob Health. 2018;6(7):e758–68. DOI:10.1016/S2214-109X(18)30283-3
   PubMed Web of Science ®Google Scholar
• Kotloff KL, Nataro JP, Blackwelder WC, et al. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet. 2013;382(9888):209–222. DOI:10.1016/S0140-6736(13)60844-2
   PubMed Web of Science ®Google Scholar
• Korich DG, Mead JR, Madore MS, et al. Effects of ozone, chlorine dioxide, chlorine, and monochloramine on Cryptosporidium parvum oocyst viability. Appl Environ Microbiol. 1990;56(5):1423–1428.
   PubMed Web of Science ®Google Scholar
• Baldursson S, Karanis P. Waterborne transmission of protozoan parasites: review of worldwide outbreaks - an update 2004-2010. Water Res. 2011;45(20):6603–6614.
   PubMed Web of Science ®Google Scholar
• Efstratiou A, Ongerth JE, Karanis P. Waterborne transmission of protozoan parasites: review of worldwide outbreaks - an update 2011–2016. Water Res. 2017;114:14–22.
   PubMed Web of Science ®Google Scholar
• Checkley W, White AC, Jaganath D, et al. A review of the global burden, novel diagnostics, therapeutics, and vaccine targets for Cryptosporidium. Lancet Infect Dis. 2014;15(1):85–94. DOI:10.1016/S1473-3099(14)70772-8
   PubMed Web of Science ®Google Scholar
• Xu P, Widmer G, Wang Y, et al. The genome of Cryptosporidium hominis. Nature. 2004;431(7012):1107–1112. DOI:http://dx.doi.org/10.1038/nature02977
   PubMed Web of Science ®Google Scholar
• Abrahamsen MS, Templeton TJ, Enomoto S, et al. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science. 2004;304(5669):441–445. DOI:10.1126/science.1094786
   PubMed Web of Science ®Google Scholar
• Matos LVS, McEvoy J, Tzipori S, et al. The transcriptome of Cryptosporidium oocysts and intracellular stages. Sci Rep. 2019;9(1). DOI:10.1038/s41598-019-44289-x
   Google Scholar
• Lippuner C, Ramakrishnan C, Basso WU, et al. RNA-Seq analysis during the life cycle of Cryptosporidium parvum reveals significant differential gene expression between proliferating stages in the intestine and infectious sporozoites. Int J Parasitol. 2018;48(6):413–422. DOI:10.1016/j.ijpara.2017.10.007
   PubMed Web of Science ®Google Scholar
• Vinayak S, Pawlowic MC, Sateriale A, et al. Genetic modification of the diarrhoeal pathogen Cryptosporidium parvum. Nature. 2015;523(7561):477–480. DOI:10.1038/nature14651
   PubMed Web of Science ®Google Scholar
• Tandel J, English ED, Sateriale A, et al. Life cycle progression and sexual development of the apicomplexan parasite Cryptosporidium parvum. Nat Microbiol. 2019;4(12):2226–2236. DOI:10.1038/s41564-019-0539-x
   PubMed Web of Science ®Google Scholar
• Templeton TJ, Iyer LM, Anantharaman V, et al. Comparative analysis of apicomplexa and genomic diversity in eukaryotes. Genome Res. 2004;14(9):1686–1695. DOI:10.1101/gr.2615304
   PubMed Web of Science ®Google Scholar
• Iyer LM, Anantharaman V, Wolf MY, et al. Comparative genomics of transcription factors and chromatin proteins in parasitic protists and other eukaryotes. Int J Parasitol. 2008;38(1):1–31.
   PubMed Web of Science ®Google Scholar
• Oberstaller J, Pumpalova Y, Schieler A, et al. The Cryptosporidium parvum ApiAP2 gene family: insights into the evolution of apicomplexan AP2 regulatory systems. Nucleic Acids Res. 2014;42(13):8271–8284.
   PubMed Web of Science ®Google Scholar
• Kumar S, Chinnusamy V, Mohapatra T. Epigenetics of modified DNA bases: 5-methylcytosine and beyond. Front Genet. 18(9):640. https://pubmed.ncbi.nlm.nih.gov/30619465/
   Google Scholar
• Husmann D, Gozani O. Histone lysine methyltransferases in biology and disease. Nat Struct Mol Biol. 2019;26(10):880–889.
   PubMed Web of Science ®Google Scholar
• Barnes CE, English DM, Cowley SM. Acetylation & Co: an expanding repertoire of histone acylations regulates chromatin and transcription. Essays Biochem. 2019;63(1):97–107.
   PubMed Web of Science ®Google Scholar
• Gissot M, Choi SW, Thompson RF, et al. Toxoplasma gondii and Cryptosporidium parvum lack detectable DNA cytosine methylation. Eukaryot Cell. 2008;7(3):537–540.
   PubMedGoogle Scholar
• Vanagas L, Jeffers V, Bogado SS, et al. Toxoplasma histone acetylation remodelers as novel drug targets. Expert Rev Anti Infect Ther. 2012;10(10):1189–1201.
   PubMed Web of Science ®Google Scholar
• Chua MJ, Arnold MSJ, Xu W, et al. Effect of clinically approved HDAC inhibitors on Plasmodium, Leishmania and Schistosoma parasite growth. Int J Parasitol Drugs Drug Resist. 2017;7(1):42–50. DOI:10.1016/j.ijpddr.2016.12.005
   PubMed Web of Science ®Google Scholar
• Guo F, Zhang H, McNair NN, et al. The existing drug vorinostat as a new lead against Cryptosporidiosis by targeting the parasite histone deacetylases. J Infect Dis. 2018;217(7):1110–1117.
   PubMed Web of Science ®Google Scholar
• Hakimi MA, Deitsch KW. Epigenetics in apicomplexa: control of gene expression during cell cycle progression, differentiation and antigenic variation. Curr Opin Microbiol. 2007;10(4):357–362.
   PubMed Web of Science ®Google Scholar
• Sautel CF, Cannella D, Bastien O, et al. SET8-Mediated methylations of histone H4 lysine 20 mark silent heterochromatic domains in apicomplexan genomes. Mol Cell Biol. 2007;27(16):5711–5724. DOI:10.1128/MCB.00482-07
   PubMed Web of Science ®Google Scholar
• Lopez-Rubio JJ, Gontijo AM, Nunes MC, et al. 5’ flanking region of var genes nucleate histone modification patterns linked to phenotypic inheritance of virulence traits in malaria parasites. Mol Microbiol. 2007;66(6):1296–1305.
   PubMed Web of Science ®Google Scholar
• Chookajorn T, Dzikowski R, Frank M, et al. Epigenetic memory at malaria virulence genes. Proc Natl Acad Sci U S A. 2007;104(3):899–902. DOI:10.1073/pnas.0609084103
   PubMed Web of Science ®Google Scholar
• Cheeseman K, Jannot G, Lourenço N, et al. Dynamic methylation of histone H3K18 in differentiating Theileria parasites. Nat Commun. 2021;12(1): DOI:10.1038/s41467-021-23477-2
   Web of Science ®Google Scholar
• Cui L, Fan Q, Cui L, et al. Histone lysine methyltransferases and demethylases in Plasmodium falciparum. Int J Parasitol. 2008;38(10):1083–1097.
   PubMed Web of Science ®Google Scholar
• Saksouk N, Bhatti MM, Kieffer S, et al. Histone-Modifying complexes regulate gene expression pertinent to the differentiation of the protozoan parasite Toxoplasma gondii. Mol Cell Biol. 2005;25(23):10301–10314. DOI:10.1128/MCB.25.23.10301-10314.2005
   PubMed Web of Science ®Google Scholar
• Villares M, Berthelet J, Weitzman JB. The clever strategies used by intracellular parasites to hijack host gene expression. Semin Immunopathol. 2020;42(2):215–226.
   PubMed Web of Science ®Google Scholar
• Cock-Rada AM, Medjkane S, Janski N, et al. SMYD3 promotes cancer invasion by epigenetic upregulation of the metalloproteinase MMP-9. Cancer Res. 2012;72(3):810–820. DOI:10.1158/0008-5472.CAN-11-1052
   PubMed Web of Science ®Google Scholar
• Sawant M, Baydoun M, Creusy C, et al. Cryptosporidium and colon cancer: cause or consequence? Microorganisms. 2020;8(11):1–15. DOI:10.3390/microorganisms8111665
   Web of Science ®Google Scholar
• Kumar S, Stecher G, Li M, et al. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–1549.
   PubMed Web of Science ®Google Scholar
• Williams CJ, Headd JJ, Moriarty NW, et al. MolProbity: more and better reference data for improved all-atom structure validation. Protein Sci. 2018;27(1):293–315. DOI:10.1002/pro.3330
   PubMed Web of Science ®Google Scholar
• Chen VB, Arendall WB, Headd JJ, et al. MolProbity : all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr. 2010;66(1):12–21. DOI:10.1107/S0907444909042073
   PubMedGoogle Scholar
• Holm L. Using dali for protein structure comparison. Methods Mol Biol. 2020;2112:29–42.
   PubMedGoogle Scholar
• Pettersen EF, Goddard TD, Huang CC, et al. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 2021;30(1):70–82. DOI:10.1002/pro.3943
   PubMed Web of Science ®Google Scholar
• Dibao-Dina A, Follet J, Ibrahim M, et al. Electrical impedance sensor for quantitative monitoring of infection processes on HCT-8 cells by the waterborne parasite Cryptosporidium. Biosens Bioelectron. 2015;66:69–76.
   PubMed Web of Science ®Google Scholar
• Keegan AR, Fanok S, Monis PT, et al. Cell culture-TaqMan PCR assay for evaluation of Cryptosporidium parvum disinfection. Appl Environ Microbiol. 2003;69(5):2505–2511.
   PubMed Web of Science ®Google Scholar
• Certad G, Ngouanesavanh T, Guyot K, et al. Cryptosporidium parvum, a potential cause of colic adenocarcinoma. Infect Agent Cancer. 2007;2(1): DOI:10.1186/1750-9378-2-22
   PubMedGoogle Scholar
• Sawant M, Benamrouz-Vanneste S, Mouray A, et al. Persistent Cryptosporidium parvum infection leads to the development of the tumor microenvironment in an experimental mouse model: results of a microarray approach. Microorganisms. 2021;9(12):2569. DOI:10.3390/microorganisms9122569
   PubMed Web of Science ®Google Scholar
• Dillon SC, Zhang X, Trievel RC, et al. The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol. 2005;6(8):227.
   PubMed Web of Science ®Google Scholar
• Wang Y, Gong AY, Ma S, et al. Delivery of parasite Cdg7_Flc_0990 RNA transcript into intestinal epithelial cells during Cryptosporidium parvum infection suppresses host cell gene transcription through epigenetic mechanisms. Cell Microbiol. 2017;19(11):e12760.
   Web of Science ®Google Scholar
• Dixon SE, Stilger KL, Elias EV, et al. A decade of epigenetic research in Toxoplasma gondii. Mol Biochem Parasitol. 2010;173(1):1–9.
   PubMed Web of Science ®Google Scholar
• Jain K, Fraser CS, Marunde MR, et al. Characterization of the plant homeodomain (PHD) reader family for their histone tail interactions. Epigenetics Chromatin. 2020;13(1):3. DOI:10.1186/s13072-020-0328-z
   PubMed Web of Science ®Google Scholar
• Winston F, David Allis C. The bromodomain: a chromatin-targeting module? Nat Struct Biol. 1999;6(7):601–604.
   PubMedGoogle Scholar
• Nishioka K, Rice JC, Sarma K, et al. PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol Cell. 2002;9(6):1201–1213. DOI:10.1016/S1097-2765(02)00548-8
   PubMed Web of Science ®Google Scholar
• Santos-Rosa H, Schneider R, Bannister AJ, et al. Active genes are tri-methylated at K4 of histone H3. Nature. 2002;419(6905):407–411. DOI:10.1038/nature01080
   PubMed Web of Science ®Google Scholar
• Zhang Y. It takes a PHD to interpret histone methylation. Nat Struct Mol Biol. 2006;13(7):572–574.
   PubMed Web of Science ®Google Scholar
• Southall SM, Wong PS, Odho Z, et al. Structural basis for the requirement of additional factors for MLL1 SET domain activity and recognition of epigenetic marks. Mol Cell. 2009;33(2):181–191.
   PubMed Web of Science ®Google Scholar
• Mishra BP, Ansari KI, Mandal SS. Dynamic association of MLL1, H3K4 trimethylation with chromatin and hox gene expression during the cell cycle. Febs J. 2009;276(6):1629–1640.
   PubMed Web of Science ®Google Scholar
• Gissot M, Kim K. How epigenomics contributes to the understanding of gene regulation in Toxoplasma gondii. J Eukaryot Microbiol. 2008;55(6):476–480.
   PubMed Web of Science ®Google Scholar
• Li Y, Han J, Zhang Y, et al. Structural basis for activity regulation of MLL family methyltransferases. Nature. 2016;530(7591):447–452. DOI:10.1038/nature16952
   PubMed Web of Science ®Google Scholar
• Wagner EJ, Carpenter PB. Understanding the language of Lys36 methylation at histone H3. Nat Rev Mol Cell Biol. 2012;13(2):115–126.
   PubMed Web of Science ®Google Scholar
• Hacker KE, Fahey CC, Shinsky SA, et al. Structure/function analysis of recurrent mutations in SETD2 protein reveals a critical and conserved role for a SET domain residue in maintaining protein stability and histone H3 Lys-36 trimethylation. J Biol Chem. 2016;291(40):21283–21295. DOI:10.1074/jbc.M116.739375
   PubMed Web of Science ®Google Scholar
• Sims RJ, Nishioka K, Reinberg D. Histone lysine methylation: a signature for chromatin function. Trends Genet. 2003;19(11):629–639.
   PubMed Web of Science ®Google Scholar
• Jiang L, Mu J, Zhang Q, et al. PfSetvs methylation of histone H3K36 represses virulence genes in Plasmodium falciparum. Nature. 2013;499(7457):223–227. DOI:10.1038/nature12361
   PubMed Web of Science ®Google Scholar
• Xiao B, Jing C, Kelly G, et al. Specificity and mechanism of the histone methyltransferase Pr-Set7. Genes Dev. 2005;19(12):1444–1454. DOI:10.1101/gad.1315905
   PubMed Web of Science ®Google Scholar
• Hamamoto R, Furukawa Y, Morita M, et al. SMYD3 encodes a histone methyltransferase involved in the proliferation of cancer cells. Nat Cell Biol. 2004;6(8):731–740. DOI:10.1038/ncb1151
   PubMed Web of Science ®Google Scholar
• van Aller GS, Reynoird N, Barbash O, et al. Smyd3 regulates cancer cell phenotypes and catalyzes histone H4 lysine 5 methylation. Epigenetics. 2012;7(4):340–343. DOI:10.4161/epi.19506
   PubMed Web of Science ®Google Scholar
• Sivagurunathan S, Heaslip A, Liu J, et al. Identification of functional modules of AKMT, a novel lysine methyltransferase regulating the motility of Toxoplasma gondii. Mol Biochem Parasitol. 2013;189(1–2):43–53.
   PubMed Web of Science ®Google Scholar
• Heaslip AT, Nishi M, Stein B, et al. The motility of a human parasite, Toxoplasma gondii, is regulated by a novel lysine methyltransferase. PLoS Pathog. 2011;7(9):e1002201.
   PubMed Web of Science ®Google Scholar
• Pivovarova Y, Liu J, Lesigang J, et al. Structure of a novel dimeric SET domain methyltransferase that regulates cell motility. J Mol Biol. 2018;430(21):4209–4229. DOI:10.1016/j.jmb.2018.08.017
   PubMed Web of Science ®Google Scholar
• Gillrie MR, Lee K, Gowda DC, et al. Plasmodium falciparum histones induce endothelial proin- flammatory response and barrier dysfunction. Am J Pathol. 2012;180(3):1028–1039. DOI:10.1016/j.ajpath.2011.11.037
   PubMed Web of Science ®Google Scholar
• Luah YH, Chaal BK, Ong EZ, et al. A moonlighting function of Plasmodium falciparum histone 3, mono-methylated at lysine 9? PLoS One. 2010;5(4):e10252.
   PubMed Web of Science ®Google Scholar
• Pereira D, Richert A, Medjkane S, et al. Cell geometry and the cytoskeleton impact the nucleo-cytoplasmic localisation of the SMYD3 methyltransferase. Sci Rep. 2020;10(1). DOI:10.1038/s41598-020-75833-9
   Web of Science ®Google Scholar
• Sautel CF, Ortet P, Saksouk N, et al. The histone methylase KMTox interacts with the redox-sensor peroxiredoxin-1 and targets genes involved in Toxoplasma gondii antioxidant defences. Mol Microbiol. 2009;71(1):212–226. DOI:10.1111/j.1365-2958.2008.06519.x
   PubMed Web of Science ®Google Scholar
• Rea S, Eisenhaber F, O’Carroll D, et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature. 2000;406(6796):593–599. DOI:10.1038/35020506
   PubMed Web of Science ®Google Scholar
• Rider SD, Zhu G. Cryptosporidium: genomic and biochemical features. Exp Parasitol. 2010;124(1):2–9.
   PubMed Web of Science ®Google Scholar
• Piunti A, Shilatifard A. The roles of polycomb repressive complexes in mammalian development and cancer. Nat Rev Mol Cell Biol. 2021;22(5):326–345.
   PubMed Web of Science ®Google Scholar
• Wang S, Ordonez-Rubiano C, Dhiman S, et al. Polycomb group proteins in cancer: multifaceted functions and strategies for modulation. NAR Cancer. 2021;3(4): DOI:10.1093/narcan/zcab039
   Google Scholar
• Li J, Ahn JH, Wang GG. Understanding histone H3 lysine 36 methylation and its deregulation in disease. Cell Mol Life Sci. 2019;76(15):2899–2916.
   PubMed Web of Science ®Google Scholar
• Yuan H, Li N, Fu D, et al. Histone methyltransferase SETD2 modulates alternative splicing to inhibit intestinal tumorigenesis. J Clin Invest. 2017;127(9):3375–3391. DOI:10.1172/JCI94292
   PubMed Web of Science ®Google Scholar
• Anderton JA, Bose S, Vockerodt M, et al. The H3K27me3 demethylase, KDM6B, is induced by Epstein-Barr virus and over-expressed in Hodgkin’s Lymphoma. Oncogene. 2011;30(17):2037–2043. DOI:10.1038/onc.2010.579
   PubMed Web of Science ®Google Scholar
• Martin KA, Lupey LN, Tempera I. Epstein-Barr virus oncoprotein LMP1 mediates epigenetic changes in host gene expression through PARP1. J Virol. 2016;90(19):8520–8530.
   PubMed Web of Science ®Google Scholar
• Forney JR, DeWald DB, Yang S, et al. A role for host phosphoinositide 3-kinase and cytoskeletal remodeling during Cryptosporidium parvum infection. Infect Immun. 1999;67(2):844–852.
   PubMed Web of Science ®Google Scholar
• Liu X, Li Z, Song Y, et al. AURKA induces EMT by regulating histone modification through Wnt/β-catenin and PI3K/Akt signaling pathway in gastric cancer. Oncotarget. 2016;7(22):33152–33164. https://pubmed.ncbi.nlm.nih.gov/27121204/
   PubMedGoogle Scholar
• Nast R, Choepak T, Lüder CGK. Epigenetic control of IFN-γ host responses during infection with Toxoplasma gondii. Front Immunol. 2020;11:11.
   PubMed Web of Science ®Google Scholar