Replication and partitioning of the apicoplast genome of Toxoplasma gondii is linked to the cell cycle and requires DNA polymerase and gyrase.

Apicoplasts / genetics Cell Division DNA Gyrase DNA-Directed DNA Polymerase Humans Toxoplasma / enzymology Toxoplasmosis
DNA polymerase Nucleoid Plasmodium Plastid Toxoplasmosis

Journal

International journal for parasitology
ISSN: 1879-0135
Titre abrégé: Int J Parasitol
Pays: England
ID NLM: 0314024

Informations de publication

Date de publication:
05 2021
Historique:
received: 08 07 2020
revised: 30 10 2020
accepted: 08 11 2020
pubmed: 14 2 2021
medline: 12 10 2021
entrez: 13 2 2021
Statut: ppublish

Résumé

Apicomplexans are the causative agents of numerous important infectious diseases including malaria and toxoplasmosis. Most of them harbour a chloroplast-like organelle called the apicoplast that is essential for the parasites' metabolism and survival. While most apicoplast proteins are nuclear encoded, the organelle also maintains its own genome, a 35 kb circle. In this study we used Toxoplasma gondii to identify and characterise essential proteins involved in apicoplast genome replication and to understand how apicoplast genome segregation unfolds over time. We demonstrated that the DNA replication enzymes Prex, DNA gyrase and DNA single stranded binding protein localise to the apicoplast. We show in knockdown experiments that apicoplast DNA Gyrase A and B, and Prex are required for apicoplast genome replication and growth of the parasite. Analysis of apicoplast genome replication by structured illumination microscopy in T. gondii tachyzoites showed that apicoplast nucleoid division and segregation initiate at the beginning of S phase and conclude during mitosis. Thus, the replication and division of the apicoplast nucleoid is highly coordinated with nuclear genome replication and mitosis. Our observations highlight essential components of apicoplast genome maintenance and shed light on the timing of this process in the context of the overall parasite cell cycle.

Identifiants

DOI: 10.1016/j.ijpara.2020.11.004 PMID: 33581138 PMC: PMC8113025
pubmed: 33581138
pii: S0020-7519(21)00047-3
doi: 10.1016/j.ijpara.2020.11.004
pmc: PMC8113025
pii:
doi:

Substances chimiques

DNA-Directed DNA Polymerase EC 2.7.7.7
DNA Gyrase EC 5.99.1.3

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

493-504

Subventions

Organisme : Medical Research Council
ID : 635 MR/S024573/1
Pays : United Kingdom

Informations de copyright

Copyright © 2021 The Author(s). Published by Elsevier Ltd.. All rights reserved.

Références

Sci Rep. 2015 Sep 28;5:14491
pubmed: 26412236
Gene. 2003 Dec 4;321:39-46
pubmed: 14636990
Mol Biosyst. 2009 Dec;5(12):1904-12
pubmed: 19763333
Nucleic Acids Res. 2010 Nov;38(20):7037-53
pubmed: 20571080
Exp Cell Res. 1990 Sep;190(1):104-12
pubmed: 2117542
Planta. 1978 Jan;141(3):259-67
pubmed: 24414870
Mol Biochem Parasitol. 2007 Jul;154(1):30-9
pubmed: 17499371
Protoplasma. 2020 Jul;257(4):1069-1078
pubmed: 32185527
Mol Cell. 2009 Jan 30;33(2):171-80
pubmed: 19187760
Protoplasma. 2010 May;241(1-4):63-74
pubmed: 20148273
Traffic. 2015 Dec;16(12):1254-69
pubmed: 26381927
Parasit Vectors. 2019 Jun 24;12(1):312
pubmed: 31234937
Parasitology. 2009 Jun;136(7):747-55
pubmed: 19402939
Mol Biochem Parasitol. 2006 Jan;145(1):125-7
pubmed: 16266757
PLoS Biol. 2015 Mar 03;13(3):e1002093
pubmed: 25734885
J Mol Biol. 1996 Aug 16;261(2):155-72
pubmed: 8757284
J Bacteriol. 1994 Oct;176(19):6030-8
pubmed: 7523361
Cell. 1984 Apr;36(4):1081-8
pubmed: 6323018
Acta Biochim Pol. 2005;52(3):569-74
pubmed: 16082412
Proc Natl Acad Sci U S A. 2004 May 18;101(20):7821-6
pubmed: 15136745
Front Plant Sci. 2014 Sep 17;5:480
pubmed: 25278952
Nature. 1997 Nov 27;390(6658):407-9
pubmed: 9389481
PLoS One. 2015 May 07;10(5):e0125705
pubmed: 25950173
BMC Bioinformatics. 2014 Dec 19;15:416
pubmed: 25523502
Mol Biol Evol. 2013 Jul;30(7):1653-64
pubmed: 23608703
Antimicrob Agents Chemother. 2019 Jan 29;63(2):
pubmed: 30455243
Plant Cell. 2004 Oct;16(10):2665-82
pubmed: 15367714
J Cell Sci. 2008 May 1;121(Pt 9):1559-68
pubmed: 18411248
PLoS Pathog. 2010 Sep 09;6(9):e1001094
pubmed: 20844581
Eur J Cell Biol. 1994 Apr;63(2):280-8
pubmed: 8082652
Eukaryot Cell. 2012 Jul;11(7):905-15
pubmed: 22611021
Int J Parasitol. 2017 Feb;47(2-3):137-144
pubmed: 27773518
Mol Microbiol. 2001 Sep;41(5):973-81
pubmed: 11555280
Gene. 1994 Jul 8;144(2):307-8
pubmed: 8039718
Front Microbiol. 2015 Jun 05;6:562
pubmed: 26097470
J Mol Biol. 2011 Jul 1;410(1):27-38
pubmed: 21570407
Front Plant Sci. 2016 Feb 04;7:57
pubmed: 26870072
DNA Cell Biol. 1997 Dec;16(12):1483-92
pubmed: 9428797
Cell Rep. 2017 Nov 14;21(7):1746-1756
pubmed: 29141210
Annu Rev Genet. 2007;41:147-68
pubmed: 17600460
Mol Biochem Parasitol. 2011 Dec;180(2):69-75
pubmed: 21856338
Plant Physiol. 2012 Nov;160(3):1420-31
pubmed: 22977281
Eukaryot Cell. 2009 Apr;8(4):530-9
pubmed: 19218426
Biochem Soc Trans. 2019 Aug 30;47(4):973-983
pubmed: 31383817
J Bacteriol. 1997 Dec;179(24):7625-30
pubmed: 9401018
Appl Microbiol Biotechnol. 2011 Nov;92(3):479-97
pubmed: 21904817
PLoS Pathog. 2011 Dec;7(12):e1002392
pubmed: 22144892
Proc Natl Acad Sci U S A. 2020 Jun 16;117(24):13719-13729
pubmed: 32482878
PLoS Pathog. 2008 Jan;4(1):e10
pubmed: 18208326
J Mol Biol. 2012 Jul 20;420(4-5):284-95
pubmed: 22543238
Cold Spring Harb Perspect Biol. 2010 Feb;2(2):a000349
pubmed: 20182613
PLoS Pathog. 2018 Feb 22;14(2):e1006836
pubmed: 29470517
Mol Microbiol. 2005 Feb;55(4):1060-71
pubmed: 15686554
Proc Natl Acad Sci U S A. 2015 Aug 18;112(33):10200-7
pubmed: 25717057
J Mol Biol. 2001 Feb 16;306(2):159-68
pubmed: 11237591
J Biol Chem. 2009 Nov 27;284(48):33683-91
pubmed: 19808683
Cytoskeleton (Hoboken). 2012 Dec;69(12):1069-85
pubmed: 23027733
Science. 2002 Oct 4;298(5591):33-4
pubmed: 12364754
Exp Parasitol. 2009 Dec;123(4):384-7
pubmed: 19720060
mBio. 2015 Oct 27;6(6):e01446-15
pubmed: 26507233
J Cell Biol. 2000 Dec 25;151(7):1423-34
pubmed: 11134072
BMC Plant Biol. 2010 Apr 02;10:57
pubmed: 20359373
Mol Biochem Parasitol. 1991 Jan;44(1):115-23
pubmed: 2011147
PLoS Biol. 2018 Sep 13;16(9):e2005895
pubmed: 30212465
Nat Commun. 2015 Dec 07;6:10048
pubmed: 26640131
PLoS Biol. 2012;10(12):e1001444
pubmed: 23239939
Lancet. 2004 Jun 12;363(9425):1965-76
pubmed: 15194258
Mol Biochem Parasitol. 2005 Jun;141(2):145-153
pubmed: 15926203
J Mol Biol. 2010 Dec 3;404(3):456-77
pubmed: 20887733
Protoplasma. 2001;218(3-4):180-91
pubmed: 11770434
mBio. 2014 Dec 02;5(6):e02021
pubmed: 25467441
FEMS Microbiol Lett. 1998 Jan 1;158(1):39-43
pubmed: 9453153
Cell. 2016 Sep 8;166(6):1423-1435.e12
pubmed: 27594426
Plant Physiol. 2013 Apr;161(4):2102-12
pubmed: 23447524
Nat Commun. 2017 Jun 08;8:15710
pubmed: 28593938
FEBS J. 2008 Jun;275(11):2899-918
pubmed: 18430024
Nat Rev Microbiol. 2014 Feb;12(2):125-36
pubmed: 24384598
ISME J. 2016 May;10(5):1113-21
pubmed: 26517699

Auteurs

Érica S Martins-Duarte (ÉS)

Laboratório de Quimioterapia de Protozoários Egler Chiari, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil; Núcleo de Biologia Estrutural e Bioimagens (CENABIO) - Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Biomagens (INBEB), Rio de Janeiro, RJ, Brazil. Electronic address: ericamduarte@icb.ufmg.br.

Lilach Sheiner (L)

Wellcome Centre for Integrative Parasitology, University of Glasgow, 120 University Place Glasgow, United Kingdom.

Sarah B Reiff (SB)

Department of Cellular Biology, University of Georgia, Athens, GA, USA.

Wanderley de Souza (W)

Núcleo de Biologia Estrutural e Bioimagens (CENABIO) - Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Biomagens (INBEB), Rio de Janeiro, RJ, Brazil; Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil.

Boris Striepen (B)

Department of Cellular Biology, University of Georgia, Athens, GA, USA; Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA. USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

questionsmedicales.fr › Cellules › Structures cellulaires › Espace intracellulaire › Cytoplasme › Structures cytoplasmiques › Organites › Plastes › Apicoplastes › Replication and partitioning of the apicoplast...
questionsmedicales.fr › Phénomènes physiologiques › Croissance et développement › Croissance › Processus de croissance cellulaire › Prolifération cellulaire › Division cellulaire › Replication and partitioning of the apicoplast...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines bactériennes › DNA gyrase › Replication and partitioning of the apicoplast...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Transferases › Phosphotransferases › Nucleotidyltransferases › DNA nucleotidyltransferases › DNA-directed DNA polymerase › Replication and partitioning of the apicoplast...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Replication and partitioning of the apicoplast...
questionsmedicales.fr › Eucaryotes › Alveolata › Apicomplexa › Coccidia › Eimeriida › Sarcocystidae › Toxoplasma › Replication and partitioning of the apicoplast...
questionsmedicales.fr › Infection › Maladies parasitaires › Protozooses › Coccidiose › Toxoplasmose › Replication and partitioning of the apicoplast...