Skip to main content
SpringerLink
Log in

Repulsive/attractive interaction among compact DNA molecules as judged through laser trapping: difference between linear- and branched-chain polyamines

  • Invited Article
  • Published:
Colloid and Polymer Science Aims and scope Submit manuscript

Abstract

It is well known that polyamines induce a folding transition from an elongated coil to a compact globule state for giant DNA larger than several tens of kbp (kilo base pairs). Here, we studied the interaction between compact DNA molecules in the presence of linear and branched-chain isomers of polyamines. We compared the stability of the assembly among plural number of compact DNA molecules generated by laser trapping. As a result, the assembly of compact DNAs with a linear-chain polyamine is stable even after the laser is switched off. On the other hand, the assembly of DNAs with a branched-chain polyamine disperses into individual compact DNAs when the laser is switched off. Thus, compact DNAs with linear- and branched-chain polyamines attract and repel each other, respectively. This difference in the effects of linear and branched polyamines is discussed in terms of the steric interaction between negatively charged double-strand DNA and cationic polyamines.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Tabor CW, Tabor H (1984) Polyamines. Annu Rev Biochem 53:749–790

    Article  CAS  PubMed  Google Scholar 

  2. Alcázar R, Tiburcio AF (2017) Polyamines. Methods and Protocols, Humana Press, Springer

  3. Thomas T, Thomas T (2001) Polyamines in cell growth and cell death: molecular mechanisms and therapeutic applications. Cell Mol Life Sci 58:244–258

    Article  CAS  PubMed  Google Scholar 

  4. Childs A, Mehta D, Gerner E (2003) Polyamine-dependent gene expression. Cell Mol Life Sci 60:1394–1406

    Article  CAS  PubMed  Google Scholar 

  5. Igarashi K, Kashiwagi K (2010) Modulation of cellular function by polyamines. Int J Biochem Cell Biol 42:39–51

    Article  CAS  PubMed  Google Scholar 

  6. Handa AK, Fatima T, Mattoo AK (2018) Polyamines: bio-molecules with diverse functions in plant and human health and disease. Frontiers Chem 6(10). https://doi.org/10.3389/fchem.2018.00010

  7. Okada K, Hidese R, Fukuda W, Niitsu M, Takao K, Horai Y, Umezawa N, Higuchi T, Oshima T, Yoshikawa Y (2014) Identification of a novel aminopropyltransferase involved in the synthesis of branched-chain polyamines in hyperthermophiles. J Bacteriol 196:1866–1876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Hidese R, Im K-H, Kobayashi M, Niitsu M, Furuchi T, Fujiwara S (2017) Identification of a novel acetylated form of branched-chain polyamine from a hyperthermophilic archaeon Thermococcus kodakarensis. Biosci Biotechnol Biochem 81:1845–1849

    Article  CAS  PubMed  Google Scholar 

  9. Atomi H, Fukui T, Kanai T, Morikawa M, Imanaka T (2004) Description of Thermococcus kodakaraensis sp. nov., a well studied hyperthermophilic archaeon previously reported as Pyrococcus sp. KOD1. Archaea 1:263–267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Gosule LC, Schellman JA (1976) Compact form of DNA induced by spermidine. Nature 259:333–335

    Article  CAS  PubMed  Google Scholar 

  11. Chattoraj DK, Gosule LC, Schellman JA (1978) DNA condensation with polyamines: II. Electron microscopic studies. J Mol Biol 121:327–337

    Article  CAS  PubMed  Google Scholar 

  12. Baeza I, Gariglio P, Rangel LM, Chavez P, Cervantes L, Arguello C, Wong C, Montanez C (1987) Electron microscopy and biochemical properties of polyamine-compacted DNA. Biochemistry 26:6387–6392

    Article  CAS  PubMed  Google Scholar 

  13. Bloomfield VA (1991) Condensation of DNA by multivalent cations: considerations on mechanism. Biopolymers 31:1471–1481

    Article  CAS  PubMed  Google Scholar 

  14. Pelta J, Livolant F, Sikorav J-L (1996) DNA aggregation induced by polyamines and cobalthexamine. J Biol Chem 271:5656–5662

    Article  CAS  PubMed  Google Scholar 

  15. Saminathan M, Thomas T, Shirahata A, Pillai C, Thomas T (2002) Polyamine structural effects on the induction and stabilization of liquid crystalline DNA: potential applications to DNA packaging, gene therapy and polyamine therapeutics. Nucleic Acids Res 30:3722–3731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Takahashi M, Yoshikawa K, Vasilevskaya V, Khokhlov A (1997) Discrete coil-globule transition of single duplex DNAs induced by polyamines. J Phys Chem B 101:9396–9401

    Article  CAS  Google Scholar 

  17. Yoshikawa K, Matsuzawa Y (1995) Discrete phase transition of giant DNA dynamics of globule formation from a single molecular chain. Phys D 84:220–227

    Article  CAS  Google Scholar 

  18. Mel'nikov SM, Sergeyev VG, Yoshikawa K (1995) Discrete coil-globule transition of large DNA induced by cationic surfactant. J Am Chem Soc 117:2401–2408

    Article  CAS  Google Scholar 

  19. Yoshikawa K, Noguchi H, Yoshikawa Y (1997) Folding transition in single long duplex DNA chain. In: Formation and dynamics of self-organized structures in surfactants and polymer solutions. Springer, pp 204–208

  20. Yoshikawa Y, Yoshikawa K, Kanbe T (1999) Formation of a giant toroid from long duplex DNA. Langmuir 15:4085–4088

    Article  CAS  Google Scholar 

  21. Mikhailenko SV, Sergeyev VG, Zinchenko AA, Gallyamov MO, Yaminsky IV, Yoshikawa K (2000) Interplay between folding/unfolding and helix/coil transitions in giant DNA. Biomacromolecules 1:597–603

    Article  CAS  PubMed  Google Scholar 

  22. Zinchenko A, Pyshkina O, Lezov A, Sergeyev V, Yoshikawa K (2008) Single DNA molecules: compaction and decompaction (chapter 3). In: Dias R, Lindman B (eds) DNA interactions with polymers and surfactants. Wiley-Blackwell

  23. Venancio-Marques A, Bergen A, Rossi-Gendron C, Rudiuk S, Baigl D (2014) Photosensitive polyamines for high-performance photocontrol of DNA higher-order structure. ACS Nano 8:3654–3663

    Article  CAS  PubMed  Google Scholar 

  24. Muramatsu A, Shimizu Y, Yoshikawa Y, Fukuda W, Umezawa N, Horai Y, Higuchi T, Fujiwara S, Imanaka T, Yoshikawa K (2016) Naturally occurring branched-chain polyamines induce a crosslinked meshwork structure in a giant DNA. J Chem Phys 145:235103/1-8

    Article  CAS  Google Scholar 

  25. Nishio T, Yoshikawa Y, Fukuda W, Umezawa N, Higuchi T, Fujiwara S, Imanaka T, Yoshikawa K (2018) Branched-chain polyamine found in hyperthermophiles induces unique temperature-dependent structural changes in genome-size DNA. Chem Phys Chem 19:2299–2304

    Article  CAS  PubMed  Google Scholar 

  26. Matsuzawa Y, Hirano K, Mori K, Katsura S, Yoshikawa K, Mizuno A (1999) Laser trapping of an individual DNA molecule folded using various condensing agents. J Am Chem Soc 121:11581–11582

    Article  CAS  Google Scholar 

  27. Yoshikawa Y, Shin-ichirou MN, Kanbe T, Yoshikawa K (2000) Controlling the folding/unfolding transition of the DNA–histone H1 complex by direct optical manipulation. Chem Phys Lett 330:77–82

    Article  CAS  Google Scholar 

  28. Matsuzawa Y, Hirano K, Mizuno A, Ichikawa M, Yoshikawa K (2002) Geometric manipulation of DNA molecules with a laser. Appl Phys Lett 81:3494–3496

    Article  CAS  Google Scholar 

  29. Ichikawa M, Matsuzawa Y, Koyama Y, Yoshikawa K (2003) Molecular fabrication: aligning DNA molecules as building blocks. Langmuir 19:5444–5447

    Article  CAS  Google Scholar 

  30. Anderson CF, Record Jr MT (1990) Ion distributions around DNA and other cylindrical polyions: theoretical descriptions and physical implications. Annu Rev Biophys Biophys Chem 19:423–463

    Article  CAS  PubMed  Google Scholar 

  31. Yoo J, Aksimentiev A (2016) The structure and intermolecular forces of DNA condensates. Nucleic Acids Res 44:2036–2046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Hanwell MD, Curtis DE, Lonie DC, Vandermeersch T, Zurek E, Hutchison GR (2012) Avogadro: an advanced semantic chemical editor, visualization, and analysis platform. J Chem Inf 4(1):17

    CAS  Google Scholar 

  33. Schweizer K, Curro J (1994) PRISM theory of the structure, thermodynamics, and phase transitions of polymer liquids and alloys. In: Atomistic modeling of physical properties. Springer, pp 319–377

  34. Yoo J, Aksimentiev A (2015) Improved parameterization of amine–carboxylate and amine–phosphate interactions for molecular dynamics simulations using the CHARMM and AMBER force fields. J Chem Theory Comput 12:430–443

    Article  CAS  PubMed  Google Scholar 

  35. Takemoto H, Ohyama T, Tohsaki A (2003) Direct sum of Coulomb potential without ambiguities of conditionally convergent series. Prog Theor Phys 109:563–573

    Article  CAS  Google Scholar 

  36. Allen M, Tildesley D (1987) Computer simulation of liquids. Clarendon Press, Oxford

    Google Scholar 

  37. Yoshikawa K, Yoshikawa Y (2002) Compaction and condensation of DNA. In: Pharmaceutical perspectives of nucleic acid-based therapeutics, vol 8. Taylor & Francis, pp 137–163

  38. Israelachvili JN (2011) Intermolecular and surface forces. Academic Press

  39. Yamasaki Y, Teramoto Y, Yoshikawa K (2001) Disappearence of the negative charge in giant DNA with a folding transition. Biophys J 80:2823–2832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study received financial support from Japan Society for the Promotion of Science (JSPS KAKENHI Grant-in-Aid for Scientific Research (A) 15H02121).

Author information

Authors and Affiliations

  1. Faculty of Life and Medical Sciences, Doshisha University, Kyotanabe, 610-0321, Japan

    Yusuke Kashiwagi, Takashi Nishio, Koichiro Sadakane, Yuko Yoshikawa & Kenichi Yoshikawa

  2. Department of Physics, Kyoto University, Kyoto, 606-8502, Japan

    Masatoshi Ichikawa

  3. Doctoral Program in Chemistry, The Graduate Center of the City University of New York, New York, NY, 10016, USA

    Chwen-Yang Shew

  4. Department of Chemistry, College of Staten Island, Staten Island, NY, 10314, USA

    Chwen-Yang Shew

  5. Graduate School of Pharmaceutical Sciences, Nagoya City University, Nagoya, 467-8603, Japan

    Naoki Umezawa & Tsunehiko Higuchi

Authors
  1. Yusuke Kashiwagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takashi Nishio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Masatoshi Ichikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chwen-Yang Shew
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Naoki Umezawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tsunehiko Higuchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Koichiro Sadakane
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yuko Yoshikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Kenichi Yoshikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kenichi Yoshikawa.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kashiwagi, Y., Nishio, T., Ichikawa, M. et al. Repulsive/attractive interaction among compact DNA molecules as judged through laser trapping: difference between linear- and branched-chain polyamines. Colloid Polym Sci 297, 397–407 (2019). https://doi.org/10.1007/s00396-018-4435-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00396-018-4435-3

Keywords

Search

Navigation