Plasmodium Condensin Core Subunits SMC2/SMC4 Mediate Atypical Mitosis and Are Essential for Parasite Proliferation and Transmission

Rajan Pandey; Steven Abel; Matthew Boucher; Richard J. Wall; Mohammad Zeeshan; Edward Rea; Aline Freville; Xueqing Maggie Lu; Declan Brady; Emilie Daniel; Rebecca R. Stanway; Sally Wheatley; Gayani Batugedara; Thomas Hollin; Andrew R. Bottrill; Dinesh Gupta; Anthony A. Holder; Karine G. Le Roch; Rita Tewari

doi:10.1016/j.celrep.2020.01.033

Plasmodium Condensin Core Subunits SMC2/SMC4 Mediate Atypical Mitosis and Are Essential for Parasite Proliferation and Transmission

Rajan Pandey, Steven Abel, Matthew Boucher, Richard J. Wall, Mohammad Zeeshan, Edward Rea, Aline Freville, Xueqing Maggie Lu, Declan Brady, Emilie Daniel, Rebecca R. Stanway, Sally Wheatley, Gayani Batugedara, Thomas Hollin, Andrew R. Bottrill, Dinesh Gupta, Anthony A. Holder, Karine G. Le Roch (Lead / Corresponding author), Rita Tewari (Lead / Corresponding author)

Biological Chemistry and Drug Discovery

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Abstract

Condensin is a multi-subunit protein complex regulating chromosome condensation and segregation during cell division. In Plasmodium spp., the causative agent of malaria, cell division is atypical and the role of condensin is unclear. Here we examine the role of SMC2 and SMC4, the core subunits of condensin, during endomitosis in schizogony and endoreduplication in male gametogenesis. During early schizogony, SMC2/SMC4 localize to a distinct focus, identified as the centromeres by NDC80 fluorescence and chromatin immunoprecipitation sequencing (ChIP-seq) analyses, but do not form condensin I or II complexes. In mature schizonts and during male gametogenesis, there is a diffuse SMC2/SMC4 distribution on chromosomes and in the nucleus, and both condensin I and condensin II complexes form at these stages. Knockdown of smc2 and smc4 gene expression reveals essential roles in parasite proliferation and transmission. The condensin core subunits (SMC2/SMC4) form different complexes and may have distinct functions at various stages of the parasite life cycle.

Original language	English
Pages (from-to)	1883-1897.e6
Number of pages	22
Journal	Cell Reports
Volume	30
Issue number	6
Early online date	11 Feb 2020
DOIs	https://doi.org/10.1016/j.celrep.2020.01.033
Publication status	Published - 11 Feb 2020

Keywords

atypical mitosis
chromosome
condensin
kleisin
mosquito
oocyst
Plasmodium
protein complex
SMC4
transmision

ASJC Scopus subject areas

General Biochemistry,Genetics and Molecular Biology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.celrep.2020.01.033Licence: CC BY

Final Published VersionFinal published version, 4.49 MBLicence: CC BY

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Pandey, R., Abel, S., Boucher, M., Wall, R. J., Zeeshan, M., Rea, E., Freville, A., Lu, X. M., Brady, D., Daniel, E., Stanway, R. R., Wheatley, S., Batugedara, G., Hollin, T., Bottrill, A. R., Gupta, D., Holder, A. A., Le Roch, K. G., & Tewari, R. (2020). Plasmodium Condensin Core Subunits SMC2/SMC4 Mediate Atypical Mitosis and Are Essential for Parasite Proliferation and Transmission. Cell Reports, 30(6), 1883-1897.e6. https://doi.org/10.1016/j.celrep.2020.01.033

@article{d0fb10c67875467ea19f109cf85cbdee,

title = "Plasmodium Condensin Core Subunits SMC2/SMC4 Mediate Atypical Mitosis and Are Essential for Parasite Proliferation and Transmission",

abstract = "Condensin is a multi-subunit protein complex regulating chromosome condensation and segregation during cell division. In Plasmodium spp., the causative agent of malaria, cell division is atypical and the role of condensin is unclear. Here we examine the role of SMC2 and SMC4, the core subunits of condensin, during endomitosis in schizogony and endoreduplication in male gametogenesis. During early schizogony, SMC2/SMC4 localize to a distinct focus, identified as the centromeres by NDC80 fluorescence and chromatin immunoprecipitation sequencing (ChIP-seq) analyses, but do not form condensin I or II complexes. In mature schizonts and during male gametogenesis, there is a diffuse SMC2/SMC4 distribution on chromosomes and in the nucleus, and both condensin I and condensin II complexes form at these stages. Knockdown of smc2 and smc4 gene expression reveals essential roles in parasite proliferation and transmission. The condensin core subunits (SMC2/SMC4) form different complexes and may have distinct functions at various stages of the parasite life cycle.",

keywords = "atypical mitosis, chromosome, condensin, kleisin, mosquito, oocyst, Plasmodium, protein complex, SMC4, transmision",

author = "Rajan Pandey and Steven Abel and Matthew Boucher and Wall, {Richard J.} and Mohammad Zeeshan and Edward Rea and Aline Freville and Lu, {Xueqing Maggie} and Declan Brady and Emilie Daniel and Stanway, {Rebecca R.} and Sally Wheatley and Gayani Batugedara and Thomas Hollin and Bottrill, {Andrew R.} and Dinesh Gupta and Holder, {Anthony A.} and {Le Roch}, {Karine G.} and Rita Tewari",

note = "This project was funded by MRC project grants and MRC Investigators grants awarded to R.T. (G0900109, G0900278, and MR/K011782/1) and BBSRC to R.T. (BB/N017609/1). R.P. was supported by MRC grant MR/K011782/1. A.A.H. was supported by the Francis Crick Institute, UK which receives its core funding from Cancer Research UK (FC001097), the UK Medical Research Council (FC001097), and the Wellcome Trust (FC001097). D.G. was supported by the Department of Biotechnology (DBT), Government of India (BT/BI/25/066/2012). K.G.L.R. was supported by the National Institute of Allergy and Infectious Diseases and the National Institutes of Health (grants R01 AI06775 and R01 AI136511) and by the University of California, Riverside, USA (NIFA-Hatch-225935).",

year = "2020",

month = feb,

day = "11",

doi = "10.1016/j.celrep.2020.01.033",

language = "English",

volume = "30",

pages = "1883--1897.e6",

journal = "Cell Reports",

issn = "2211-1247",

publisher = "Elsevier",

number = "6",

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Pandey, R, Abel, S, Boucher, M, Wall, RJ, Zeeshan, M, Rea, E, Freville, A, Lu, XM, Brady, D, Daniel, E, Stanway, RR, Wheatley, S, Batugedara, G, Hollin, T, Bottrill, AR, Gupta, D, Holder, AA, Le Roch, KG & Tewari, R 2020, 'Plasmodium Condensin Core Subunits SMC2/SMC4 Mediate Atypical Mitosis and Are Essential for Parasite Proliferation and Transmission', Cell Reports, vol. 30, no. 6, pp. 1883-1897.e6. https://doi.org/10.1016/j.celrep.2020.01.033

TY - JOUR

T1 - Plasmodium Condensin Core Subunits SMC2/SMC4 Mediate Atypical Mitosis and Are Essential for Parasite Proliferation and Transmission

AU - Pandey, Rajan

AU - Abel, Steven

AU - Boucher, Matthew

AU - Wall, Richard J.

AU - Zeeshan, Mohammad

AU - Rea, Edward

AU - Freville, Aline

AU - Lu, Xueqing Maggie

AU - Brady, Declan

AU - Daniel, Emilie

AU - Stanway, Rebecca R.

AU - Wheatley, Sally

AU - Batugedara, Gayani

AU - Hollin, Thomas

AU - Bottrill, Andrew R.

AU - Gupta, Dinesh

AU - Holder, Anthony A.

AU - Le Roch, Karine G.

AU - Tewari, Rita

N1 - This project was funded by MRC project grants and MRC Investigators grants awarded to R.T. (G0900109, G0900278, and MR/K011782/1) and BBSRC to R.T. (BB/N017609/1). R.P. was supported by MRC grant MR/K011782/1. A.A.H. was supported by the Francis Crick Institute, UK which receives its core funding from Cancer Research UK (FC001097), the UK Medical Research Council (FC001097), and the Wellcome Trust (FC001097). D.G. was supported by the Department of Biotechnology (DBT), Government of India (BT/BI/25/066/2012). K.G.L.R. was supported by the National Institute of Allergy and Infectious Diseases and the National Institutes of Health (grants R01 AI06775 and R01 AI136511) and by the University of California, Riverside, USA (NIFA-Hatch-225935).

PY - 2020/2/11

Y1 - 2020/2/11

N2 - Condensin is a multi-subunit protein complex regulating chromosome condensation and segregation during cell division. In Plasmodium spp., the causative agent of malaria, cell division is atypical and the role of condensin is unclear. Here we examine the role of SMC2 and SMC4, the core subunits of condensin, during endomitosis in schizogony and endoreduplication in male gametogenesis. During early schizogony, SMC2/SMC4 localize to a distinct focus, identified as the centromeres by NDC80 fluorescence and chromatin immunoprecipitation sequencing (ChIP-seq) analyses, but do not form condensin I or II complexes. In mature schizonts and during male gametogenesis, there is a diffuse SMC2/SMC4 distribution on chromosomes and in the nucleus, and both condensin I and condensin II complexes form at these stages. Knockdown of smc2 and smc4 gene expression reveals essential roles in parasite proliferation and transmission. The condensin core subunits (SMC2/SMC4) form different complexes and may have distinct functions at various stages of the parasite life cycle.

AB - Condensin is a multi-subunit protein complex regulating chromosome condensation and segregation during cell division. In Plasmodium spp., the causative agent of malaria, cell division is atypical and the role of condensin is unclear. Here we examine the role of SMC2 and SMC4, the core subunits of condensin, during endomitosis in schizogony and endoreduplication in male gametogenesis. During early schizogony, SMC2/SMC4 localize to a distinct focus, identified as the centromeres by NDC80 fluorescence and chromatin immunoprecipitation sequencing (ChIP-seq) analyses, but do not form condensin I or II complexes. In mature schizonts and during male gametogenesis, there is a diffuse SMC2/SMC4 distribution on chromosomes and in the nucleus, and both condensin I and condensin II complexes form at these stages. Knockdown of smc2 and smc4 gene expression reveals essential roles in parasite proliferation and transmission. The condensin core subunits (SMC2/SMC4) form different complexes and may have distinct functions at various stages of the parasite life cycle.

KW - atypical mitosis

KW - chromosome

KW - condensin

KW - kleisin

KW - mosquito

KW - oocyst

KW - Plasmodium

KW - protein complex

KW - SMC4

KW - transmision

UR - http://www.scopus.com/inward/record.url?scp=85079123666&partnerID=8YFLogxK

U2 - 10.1016/j.celrep.2020.01.033

DO - 10.1016/j.celrep.2020.01.033

M3 - Article

C2 - 32049018

AN - SCOPUS:85079123666

SN - 2211-1247

VL - 30

SP - 1883-1897.e6

JO - Cell Reports

JF - Cell Reports

IS - 6

ER -

Plasmodium Condensin Core Subunits SMC2/SMC4 Mediate Atypical Mitosis and Are Essential for Parasite Proliferation and Transmission

Abstract

Keywords

ASJC Scopus subject areas

UN SDGs

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