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

• Published in: PloS one 2020-09, Vol.15 (9), p.e0238447
• Main Authors: Nishio, Takashi, Sugino, Kaito, Yoshikawa, Yuko, Matsumoto, Michiaki, Oe, Yohei, Sadakane, Koichiro, Yoshikawa, Kenichi
• Format: Article
• Language: English
• Subjects: Binding; Biochemical Phenomena; Biological activity; Biology and Life Sciences; Deoxyribonucleic acid; DNA; DNA - metabolism; DNA structure; DNA-directed RNA polymerase; Fluorescence; Fluorescence microscopy; Gene expression; Gene Expression - drug effects; Medical research; Methods; NMR; Nuclear magnetic resonance; Physical Sciences; Polyamines; Polyamines - metabolism; Polyamines - pharmacology; Potassium; Potassium - metabolism; Research and Analysis Methods; RNA polymerase; Sodium - metabolism; Spectrum analysis; Spermidine; Spermidine - pharmacology; Spermine - pharmacology; Structure-function relationships
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0238447

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+. 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. 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.