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Link to original content: http://pubmed.ncbi.nlm.nih.gov/32881909/
K+ promotes the favorable effect of polyamine on gene expression better than Na - PubMed Skip to main page content
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. 2020 Sep 3;15(9):e0238447.
doi: 10.1371/journal.pone.0238447. eCollection 2020.

K+ promotes the favorable effect of polyamine on gene expression better than Na

Takashi Nishio  1 , Kaito Sugino  1 , Yuko Yoshikawa  1 , Michiaki Matsumoto  2 , Yohei Oe  1 , Koichiro Sadakane  1 , Kenichi Yoshikawa  1   3
Affiliations

K+ promotes the favorable effect of polyamine on gene expression better than Na

Takashi Nishio et al. PLoS One. .

Abstract

Background: Polyamines are involved in a wide variety of biological processes including a marked effect on the structure and function of DNA. During our study on the interaction of polyamines with DNA, we found that K+ enhanced in vitro gene expression in the presence of polyamine more strongly than Na+. Thus, we sought to clarify the physico-chemical mechanism underlying this marked difference between the effects of K+ and Na+.

Principal findings: It was found that K+ enhanced gene expression in the presence of spermidine, SPD(3+), much more strongly than Na+, through in vitro experiments with a Luciferase assay on cell extracts. Single-DNA observation by fluorescence microscopy showed that Na+ prevents the folding transition of DNA into a compact state more strongly than K+. 1H NMR measurement revealed that Na+ inhibits the binding of SPD to DNA more strongly than K+. Thus, SPD binds to DNA more favorably in K+-rich medium than in Na+-rich medium, which leads to favorable conditions for RNA polymerase to access DNA by decreasing the negative charge.

Conclusion and significance: We found that Na+ and K+ exhibit markedly different effects through competitive binding with a cationic polyamine, SPD, to DNA, which causes a large difference in the higher-order structure of genomic DNA. It is concluded that the larger favorable effect of Na+ than K+ on in vitro gene expression observed in this study is well attributable to the significant difference between Na+ and K+ on the competitive binding inducing conformational transition of DNA.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1
Efficiency of gene expression vs. concentrations of (A) SPD, (B) Na+ and (C) K+. C0 is the concentration of Na+ and K+ contained in the original reaction buffer; C = C0+ΔC. The intensity is normalized to the control condition (= 1), where ΔC = 0 in the absence of SPD. The DNA concentration was fixed at 0.3 μM.
Fig 2
Fig 2. Examples of FM images of a single T4 DNA molecule undergoing Brownian motion in solution.
(A) In the absence of any condensation agent such as SPD, Na+ or K+. (B) In the presence of 0.3 mM SPD. (C) In the presence of 0.3 mM SPD and 30 mM ΔCNa. The total observation time for (A)–(C) is 3 s.
Fig 3
Fig 3. Histograms for the long-axis length L of T4 DNA at different concentrations of CNa or CK with 0–1.5 mM SPD.
Fig 4
Fig 4. Evaluation of the binding affinity of Na+ and K+ for DNA through 1H NMR measurements.
(A) 1H NMR signals of 0.1 mM SPD in D2O solution. (B) 1H NMR signals of 0.1 mM SPD with different concentrations of Na+ or K+ in the presence of 1.6 mM CT DNA. (C) Changes in the integrated intensity of 1H NMR signals, INMR, depending on the concentrations C. The intensities in the graph were evaluated from the sum of all integrated values for the signals of SPD. (D) Log-log plot; proportion of unbound SPD to bound SPD, PFree/PBound, vs. the salt concentrations C. PFree and PBound are evaluated from the relationship; PFree = INMR and PBound = 1 –INMR, respectively.
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Grants and funding

This work was supported by JSPS KAKENHI Grant Number JP15H02121 and JP20H01877 funded to KY. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.