TY - JOUR
T1 - Structure-function studies of a nucleoplasmin isoform from Plasmodium falciparum
AU - Saharan, Ketul
AU - Baral, Somanath
AU - Gandhi, Surajit
AU - Singh, Ajit Kumar
AU - Ghosh, Sourav
AU - Das, Rahul
AU - Nagaraj, Viswanathan Arun
AU - Vasudevan, Dileep
N1 - Publisher Copyright:
© 2025 The Authors
PY - 2025/4
Y1 - 2025/4
N2 - An organized regulation of gene expression and DNA replication is vital for the progression of the complex life cycle of Plasmodium falciparum (Pf), involving multiple hosts and various stages. These attributes rely on the dynamic architecture of chromatin governed by several factors, including histone chaperones. Nucleoplasmin class of histone chaperones perform histone chaperoning function and participate in various developmental processes in eukaryotes. Here, our crystal structure confirmed that Pf indeed possesses a nucleoplasmin isoform (PfNPM), and the N-terminal core domain (NTD) adopts the characteristic pentameric doughnut conformation. Furthermore, PfNPM exists as a pentamer in solution, and the N-terminal core domain exhibits thermal and chemical stability. PfNPM interacts individually with assembled H2A/H2B and H3/H4 with an equimolar stoichiometry, wherein the acidic tracts of PfNPM were found to be necessary for these interactions. Further, H3/H4 displays a higher binding affinity for PfNPM than H2A/H2B, potentially due to stronger electrostatic interactions. The interaction studies also suggested that H2A/H2B and H3/H4 might share the same binding site on the PfNPM distal face, wherein H3/H4 could substitute H2A/H2B due to a higher binding affinity. Intriguingly, PfNPM neither demonstrated direct interaction with the nucleosome core particles nor displayed nucleosome assembly function, suggesting it may not be directly associated with histone deposition on the parasite genomic DNA. Furthermore, our immunofluorescence results suggested that PfNPM predominantly localizes in the nucleus and exhibits expression only in the early blood stages, such as ring and trophozoite. Altogether, we provide the first report on the structural and functional characterization of PfNPM.
AB - An organized regulation of gene expression and DNA replication is vital for the progression of the complex life cycle of Plasmodium falciparum (Pf), involving multiple hosts and various stages. These attributes rely on the dynamic architecture of chromatin governed by several factors, including histone chaperones. Nucleoplasmin class of histone chaperones perform histone chaperoning function and participate in various developmental processes in eukaryotes. Here, our crystal structure confirmed that Pf indeed possesses a nucleoplasmin isoform (PfNPM), and the N-terminal core domain (NTD) adopts the characteristic pentameric doughnut conformation. Furthermore, PfNPM exists as a pentamer in solution, and the N-terminal core domain exhibits thermal and chemical stability. PfNPM interacts individually with assembled H2A/H2B and H3/H4 with an equimolar stoichiometry, wherein the acidic tracts of PfNPM were found to be necessary for these interactions. Further, H3/H4 displays a higher binding affinity for PfNPM than H2A/H2B, potentially due to stronger electrostatic interactions. The interaction studies also suggested that H2A/H2B and H3/H4 might share the same binding site on the PfNPM distal face, wherein H3/H4 could substitute H2A/H2B due to a higher binding affinity. Intriguingly, PfNPM neither demonstrated direct interaction with the nucleosome core particles nor displayed nucleosome assembly function, suggesting it may not be directly associated with histone deposition on the parasite genomic DNA. Furthermore, our immunofluorescence results suggested that PfNPM predominantly localizes in the nucleus and exhibits expression only in the early blood stages, such as ring and trophozoite. Altogether, we provide the first report on the structural and functional characterization of PfNPM.
KW - crystal structure
KW - histone chaperone
KW - nucleoplasmin
KW - nucleosome
KW - plasmodium
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U2 - 10.1016/j.jbc.2025.108379
DO - 10.1016/j.jbc.2025.108379
M3 - Article
C2 - 40049416
AN - SCOPUS:105000984521
SN - 0021-9258
VL - 301
JO - Journal of Biological Chemistry
JF - Journal of Biological Chemistry
IS - 4
M1 - 108379
ER -