A functionally divergent transcription elongation factor 1-like protein in Toxoplasma gondii.
Toxoplasma
CK2 kinase
bradyzoite cyst wall
inner membrane complex
tachyzoite
transcription elongation factor 1
zinc finger
Journal
FEBS letters
ISSN: 1873-3468
Titre abrégé: FEBS Lett
Pays: England
ID NLM: 0155157
Informations de publication
Date de publication:
01 2022
01 2022
Historique:
revised:
01
11
2021
received:
27
08
2021
accepted:
15
11
2021
pubmed:
26
11
2021
medline:
11
2
2022
entrez:
25
11
2021
Statut:
ppublish
Résumé
Zinc ribbons, one of the largest fold groups among zinc fingers, often include proteins involved in the transcription machinery. Here, we identify and characterize one such zinc ribbon-bearing protein in the apicomplexan parasite Toxoplasma gondii, annotated as putative transcription elongation factor 1 (ELF1), with predicted functions in transcription and chromatin maintenance. We show that this ELF1 homolog, referred to as T. gondii ELF1-like divergent (TgELD), is expressed in both tachyzoite and bradyzoite developmental stages. TgELD associates with the cytoskeleton in the tachyzoites, while it transiently becomes a part of the cyst wall in the early bradyzoites, followed by a cytosolic and peripheral localization in late bradyzoites. TgELD is phosphorylated by a casein kinase 2-like protein, which has potential implications for its localization and function in the parasite.
Identifiants
pubmed: 34820838
doi: 10.1002/1873-3468.14241
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
112-127Informations de copyright
© 2021 Federation of European Biochemical Societies.
Références
Montoya JG and Liesenfeld O (2004) Toxoplasmosis. Lancet 363, 1965-1976.
Robert-Gangneux F and Darde ML (2012) Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev 25, 264-296.
Cerutti A, Blanchard N and Besteiro S (2020) The bradyzoite: a key developmental stage for the persistence and pathogenesis of toxoplasmosis. Pathogens 9, 234.
Sullivan WJ Jr, Smith AT and Joyce BR (2009) Understanding mechanisms and the role of differentiation in pathogenesis of Toxoplasma gondii: a review. Mem Inst Oswaldo Cruz 104, 155-161.
Radke JR, Behnke MS, Mackey AJ, Radke JB, Roos DS and White MW (2005) The transcriptome of Toxoplasma gondii. BMC Biol 3, 26.
Krishna SS, Majumdar I and Grishin NV (2003) Structural classification of zinc fingers: survey and summary. Nucleic Acids Res 31, 532-550.
Prather D, Krogan NJ, Emili A, Greenblatt JF and Winston F (2005) Identification and characterization of Elf1, a conserved transcription elongation factor in Saccharomyces cerevisiae. Mol Cell Biol 25, 10122-10135.
Mayer A, Lidschreiber M, Siebert M, Leike K, Soding J and Cramer P (2010) Uniform transitions of the general RNA polymerase II transcription complex. Nat Struct Mol Biol 17, 1272-1278.
Ehara H, Yokoyama T, Shigematsu H, Yokoyama S, Shirouzu M and Sekine SI (2017) Structure of the complete elongation complex of RNA polymerase II with basal factors. Science 357, 921-924.
Ehara H, Kujirai T, Fujino Y, Shirouzu M, Kurumizaka H and Sekine SI (2019) Structural insight into nucleosome transcription by RNA polymerase II with elongation factors. Science 363, 744-747.
Kumar A, Agarwal S, Heyman JA, Matson S, Heidtman M, Piccirillo S, Umansky L, Drawid A, Jansen R, Liu Y et al. (2002) Subcellular localization of the yeast proteome. Genes Dev 16, 707-719.
Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS and O'Shea EK (2003) Global analysis of protein localization in budding yeast. Nature 425, 686-691.
Sugi T, Ma YF, Tomita T, Murakoshi F, Eaton MS, Yakubu R, Han B, Tu V, Kato K, Kawazu S et al. (2016) Toxoplasma gondii cyclic AMP-dependent protein kinase subunit 3 is involved in the switch from tachyzoite to bradyzoite development. MBio 7, e00755-16.
Tu V, Mayoral J, Sugi T, Tomita T, Han B, Ma YF and Weiss LM (2019) Enrichment and proteomic characterization of the cyst wall from in vitro Toxoplasma gondii cysts. MBio 10, e00469-19.
Deshmukh AS, Gurupwar R, Mitra P, Aswale K, Shinde S and Chaudhari S (2021) Toxoplasma gondii induces robust humoral immune response against cyst wall antigens in chronically infected animals and humans. Microb Pathog 152, 104643.
Mitra P, Deshmukh AS, Gurupwar R and Kashyap P (2019) Characterization of Toxoplasma gondii Spt5 like transcription elongation factor. Biochim Biophys Acta Gene Regul Mech 1862, 184-197.
Lentini G, Kong-Hap M, El Hajj H, Francia M, Claudet C, Striepen B, Dubremetz JF and Lebrun M (2015) Identification and characterization of Toxoplasma SIP, a conserved apicomplexan cytoskeleton protein involved in maintaining the shape, motility and virulence of the parasite. Cell Microbiol 17, 62-78.
Alonso AM, Coceres VM, De Napoli MG, Nieto Guil AF, Angel SO and Corvi MM (2012) Protein palmitoylation inhibition by 2-bromopalmitate alters gliding, host cell invasion and parasite morphology in Toxoplasma gondii. Mol Biochem Parasitol 184, 39-43.
Kumar S, Stecher G, Li M, Knyaz C and Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35, 1547-1549.
Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L et al. (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46, W296-W303.
Roy A, Kucukural A and Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5, 725-738.
Webb B and Sali A (2016) Comparative protein structure modeling using MODELLER. Curr Protoc Bioinformatics 54, 5.6.1-5.6.37.
Ning W, Jiang P, Guo Y, Wang C, Tan X, Zhang W, Peng D and Xue Y (2021) GPS-Palm: a deep learning-based graphic presentation system for the prediction of S-palmitoylation sites in proteins. Brief Bioinform 22, 1836-1847.
Gilk SD, Raviv Y, Hu K, Murray JM, Beckers CJ and Ward GE (2006) Identification of PhIL1, a novel cytoskeletal protein of the Toxoplasma gondii pellicle, through photosensitized labeling with 5-[125I] iodonaphthalene-1-azide. Eukaryot Cell 5, 1622-1634.
Gaji RY, Johnson DE, Treeck M, Wang M, Hudmon A and Arrizabalaga G (2015) Phosphorylation of a myosin motor by TgCDPK3 facilitates rapid initiation of motility during Toxoplasma gondii egress. PLoS Pathog 11, e1005268.
Rompikuntal PK, Kent RS, Foe IT, Deng B, Bogyo M and Ward GE (2021) Blocking palmitoylation of Toxoplasma gondii myosin light chain 1 disrupts glideosome composition but has little impact on parasite motility. mSphere 6, e00823-20.
Weng SL, Kao HJ, Huang CH and Lee TY (2017) MDD-Palm: identification of protein S-palmitoylation sites with substrate motifs based on maximal dependence decomposition. PLoS One 12, e0179529.
Tomita T, Bzik DJ, Ma YF, Fox BA, Markillie LM, Taylor RC, Kim K and Weiss LM (2013) The Toxoplasma gondii cyst wall protein CST1 is critical for cyst wall integrity and promotes bradyzoite persistence. PLoS Pathog 9, e1003823.
Kubinski K, Zielinski R, Hellman U, Mazur E and Szyszka R (2006) Yeast elf1 factor is phosphorylated and interacts with protein kinase CK2. J Biochem Mol Biol 39, 311-318.
Borgo C, D'Amore C, Sarno S, Salvi M and Ruzzene M (2021) Protein kinase CK2: a potential therapeutic target for diverse human diseases. Signal Transduct Target Ther 6, 183.
Treeck M, Sanders JL, Elias JE and Boothroyd JC (2011) The phosphoproteomes of Plasmodium falciparum and Toxoplasma gondii reveal unusual adaptations within and beyond the parasites' boundaries. Cell Host Microbe 10, 410-419.
Young JC, Broncel M, Teague H, Russell MRG, McGovern OL, Renshaw M, Frith D, Snijders AP, Collinson L, Carruthers VB et al. (2020) Phosphorylation of Toxoplasma gondii secreted proteins during acute and chronic stages of infection. mSphere 5, e00792-20.
Meggio F, Deana AD, Ruzzene M, Brunati AM, Cesaro L, Guerra B, Meyer T, Mett H, Fabbro D, Furet P et al. (1995) Different susceptibility of protein kinases to staurosporine inhibition. Kinetic studies and molecular bases for the resistance of protein kinase CK2. Eur J Biochem 234, 317-322.
Allende JE and Allende CC (1995) Protein kinases. 4. Protein kinase CK2: an enzyme with multiple substrates and a puzzling regulation. FASEB J 9, 313-323.
Che FY, Madrid-Aliste C, Burd B, Zhang H, Nieves E, Kim K, Fiser A, Angeletti RH and Weiss LM (2011) Comprehensive proteomic analysis of membrane proteins in Toxoplasma gondii. Mol Cell Proteomics 10, M110.000745.
Foe IT, Child MA, Majmudar JD, Krishnamurthy S, van der Linden WA, Ward GE, Martin BR and Bogyo M (2015) Global analysis of palmitoylated proteins in Toxoplasma gondii. Cell Host Microbe 18, 501-511.
Caballero MC, Alonso AM, Deng B, Attias M, de Souza W and Corvi MM (2016) Identification of new palmitoylated proteins in Toxoplasma gondii. Biochim Biophys Acta 1864, 400-408.
Beck JR, Rodriguez-Fernandez IA, de Leon JC, Huynh MH, Carruthers VB, Morrissette NS and Bradley PJ (2010) A novel family of Toxoplasma IMC proteins displays a hierarchical organization and functions in coordinating parasite division. PLoS Pathog 6, e1001094.
Frenal K, Polonais V, Marq JB, Stratmann R, Limenitakis J and Soldati-Favre D (2010) Functional dissection of the apicomplexan glideosome molecular architecture. Cell Host Microbe 8, 343-357.
Lourido S, Tang K and Sibley LD (2012) Distinct signalling pathways control Toxoplasma egress and host-cell invasion. EMBO J 31, 4524-4534.
De Napoli MG, de Miguel N, Lebrun M, Moreno SN, Angel SO and Corvi MM (2013) N-terminal palmitoylation is required for Toxoplasma gondii HSP20 inner membrane complex localization. Biochim Biophys Acta 1833, 1329-1337.
Child MA, Hall CI, Beck JR, Ofori LO, Albrow VE, Garland M, Bowyer PW, Bradley PJ, Powers JC, Boothroyd JC et al. (2013) Small-molecule inhibition of a depalmitoylase enhances Toxoplasma host-cell invasion. Nat Chem Biol 9, 651-656.
Buchholz KR, Fritz HM, Chen X, Durbin-Johnson B, Rocke DM, Ferguson DJ, Conrad PA and Boothroyd JC (2011) Identification of tissue cyst wall components by transcriptome analysis of in vivo and in vitro Toxoplasma gondii bradyzoites. Eukaryot Cell 10, 1637-1647.
Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231-237.
Pawson T and Scott JD (2005) Protein phosphorylation in signaling-50 years and counting. Trends Biochem Sci 30, 286-290.
Wang ZX, Zhou CX, Calderon-Mantilla G, Petsalaki E, He JJ, Song HY, Elsheikha HM and Zhu XQ (2019) iTRAQ-based global phosphoproteomics reveals novel molecular differences between Toxoplasma gondii strains of different genotypes. Front Cell Infect Microbiol 9, 307.
Meggio F and Pinna LA (2003) One-thousand-and-one substrates of protein kinase CK2? FASEB J 17, 349-368.
Litchfield DW (2003) Protein kinase CK2: structure, regulation and role in cellular decisions of life and death. Biochem J 369, 1-15.
Delorme V, Cayla X, Faure G, Garcia A and Tardieux I (2003) Actin dynamics is controlled by a casein kinase II and phosphatase 2C interplay on Toxoplasma gondii Toxofilin. Mol Biol Cell 14, 1900-1912.
Gilk SD, Gaskins E, Ward GE and Beckers CJ (2009) GAP45 phosphorylation controls assembly of the Toxoplasma myosin XIV complex. Eukaryot Cell 8, 190-196.
Jones ML, Collins MO, Goulding D, Choudhary JS and Rayner JC (2012) Analysis of protein palmitoylation reveals a pervasive role in Plasmodium development and pathogenesis. Cell Host Microbe 12, 246-258.
Sheffield HG and Melton ML (1968) The fine structure and reproduction of Toxoplasma gondii. J Parasitol 54, 209-226.
Dietrich LE and Ungermann C (2004) On the mechanism of protein palmitoylation. EMBO Rep 5, 1053-1057.
Khater EI, Sinden RE and Dessens JT (2004) A malaria membrane skeletal protein is essential for normal morphogenesis, motility, and infectivity of sporozoites. J Cell Biol 167, 425-432.
Tremp AZ, Khater EI and Dessens JT (2008) IMC1b is a putative membrane skeleton protein involved in cell shape, mechanical strength, motility, and infectivity of malaria ookinetes. J Biol Chem 283, 27604-27611.
Gaskins E, Gilk S, DeVore N, Mann T, Ward G and Beckers C (2004) Identification of the membrane receptor of a class XIV myosin in Toxoplasma gondii. J Cell Biol 165, 383-393.
Keeley A and Soldati D (2004) The glideosome: a molecular machine powering motility and host-cell invasion by Apicomplexa. Trends Cell Biol 14, 528-532.