Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Promotion of protein crystal growth by actively switching crystal growth mode via femtosecond laser ablation

Nature Photonics volume 10, pages 723–726 (2016)Cite this article

Subjects

Abstract

Large single crystals with desirable shapes are essential for various scientific and industrial fields, such as X-ray/neutron crystallography and crystalline devices. However, in the case of proteins the production of such crystals is particularly challenging, despite the efforts devoted to optimization of the environmental, chemical and physical parameters. Here we report an innovative approach for promoting the growth of protein crystals by directly modifying the local crystal structure via femtosecond laser ablation. We demonstrate that protein crystals with surfaces that are locally etched (several micrometers in diameter) by femtosecond laser ablation show enhanced growth rates without losing crystal quality. Optical phase-sensitive microscopy and X-ray topography imaging techniques reveal that the local etching induces spiral growth, which is energetically advantageous compared with the spontaneous two-dimensional nucleation growth mode. These findings prove that femtosecond laser ablation can actively switch the crystal growth mode, offering flexible control over the size and shape of protein crystals.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Promotion of crystal growth by femtosecond laser ablation.
Figure 2: Spiral growth from the ablated crystal surface.
Figure 3: Mechanism of crystal growth promotion by laser ablation.

References

  1. Anderson, A. C. The process of structure-based drug design. Chem. Biol. 10, 787–797 (2003).

    Article  Google Scholar 

  2. Chernov, A. A. Protein crystals and their growth. J. Struct. Biol. 142, 3–21 (2003).

    Article  Google Scholar 

  3. McPherson, A. Introduction to protein crystallization. Methods 34, 254–265 (2004).

    Article  Google Scholar 

  4. Heinemann, U., Büssow, K., Mueller, U. & Umbach, P. Facilities and methods for the high-throughput crystal structural analysis of human proteins. Acc. Chem. Res. 36, 157–163 (2003).

    Article  Google Scholar 

  5. Garetz, B. A., Aber, J. E., Goddard, N. L., Young, R. G. & Myerson, A. S. Nonphotochemical, polarization-dependent, laser-induced nucleation in supersaturated aqueous urea solutions. Phys. Rev. Lett. 77, 3475–3476 (1996).

    Article  ADS  Google Scholar 

  6. Lee, I. S. et al. Nonphotochemical laser induced nucleation of hen egg white lysozyme crystals. Cryst. Growth Des. 8, 4255–4261 (2008).

    Article  Google Scholar 

  7. Yennawar, N., Denev, S., Gopalan, V. & Yennawar, H. Laser-improved protein crystallization screening. Acta Crystallogr. F 66, 969–972 (2010).

    Article  Google Scholar 

  8. Okutsu, T. et al. Light-induced nucleation of metastable hen egg-white lysozyme solutions. Cryst. Growth Des. 5, 1393–1398 (2005).

    Article  Google Scholar 

  9. Veesler, S. et al. Crystals from light: photochemically induced nucleation of hen egg-white lysozyme. Cryst. Growth Des. 6, 1631–1635 (2006).

    Article  Google Scholar 

  10. Adachi, H. et al. Laser irradiated growth of protein crystal. Jpn J. Appl. Phys. 42, L798–L800 (2003).

    Article  ADS  Google Scholar 

  11. Yoshikawa, H. Y. et al. Laser ablation for protein crystal nucleation and seeding. Chem. Soc. Rev. 43, 2147–2158 (2014).

    Article  Google Scholar 

  12. Tu, J. R., Miura, A., Yuyama, K.-i., Masuhara, H. & Sugiyama, T. Crystal growth of lysozyme controlled by laser trapping. Cryst. Growth Des. 14, 15–22 (2014).

    Article  Google Scholar 

  13. Vogel, A., Noack, J., Hüttman, G. & Paltauf, G. Mechanisms of femtosecond laser nanosurgery of cells and tissues. Appl. Phys. B 81, 1015–1047 (2005).

    Article  ADS  Google Scholar 

  14. Zhigilei, L. V. & Garrison, B. J. Microscopic mechanisms of laser ablation of organic solids in the thermal and stress confinement irradiation regimes. J. Appl. Phys. 88, 1281–1298 (2000).

    Article  ADS  Google Scholar 

  15. Paltauf, G. & Dyer, P. E. Photomechanical processes and effects in ablation. Chem. Rev. 103, 487–518 (2003).

    Article  Google Scholar 

  16. Yoshikawa, H. Y. et al. Spatially precise, soft microseeding of single protein crystals by femtosecond laser ablation. Cryst. Growth Des. 12, 4334–4339 (2012).

    Article  Google Scholar 

  17. Sazaki, G. et al. In situ observation of elementary growth steps on the surface of protein crystals by laser confocal microscopy. J. Cryst. Growth 262, 536–542 (2004).

    Article  ADS  Google Scholar 

  18. Suzuki, Y., Tsukamoto, K., Yoshizaki, I., Miura, H. & Fujiwara, T. First direct observation of impurity effects on the growth rate of tetragonal lysozyme crystals under microgravity as measured by interferometry. Cryst. Growth Des. 15, 4787–4794 (2015).

    Article  Google Scholar 

  19. Burton, W. K., Cabrera, N. & Frank, F. C. The growth of crystals and the equilibrium structure of their surfaces. Phil. Trans. R. Soc. Lond. A 243, 299–358 (1951).

    Article  ADS  MathSciNet  Google Scholar 

  20. Gliko, O., Booth, N. A., Rosenbach, E. & Vekilov, P. G. Phase-shifting interferometry for the study of the step dynamics during crystallization of proteins. Cryst. Growth Des. 2, 381–385 (2002).

    Article  Google Scholar 

  21. Tsukamoto, K. et al. Report from the WG of dependence of growth condition on the perfection of protein crystals. In: Space Utilization Research: Proc. 23rd Space Utilization Symp. 23, 12–15 (JAXA/ISAS, 2007); https://repository.exst.jaxa.jp/dspace/handle/a-is/40171

    Google Scholar 

  22. Markov, I. Crystal Growth for Beginners: Fundamentals of Nucleation, Crystal Growth and Epitaxy (World Scientific, 2003).

    Book  Google Scholar 

  23. Teng, H. H., Dove, P. M. & De Yoreo, J. J. Kinetics of calcite growth: surface processes and relationships to macroscopic rate laws. Geochim. Cosmochim. Acta 64, 2255–2266 (2000).

    Article  ADS  Google Scholar 

  24. Tachibana, M., Koizumi, H., Izumi, K., Kajiwara, K. & Kojima, K. Identification of dislocations in large tetragonal hen egg-white lysozyme crystals by synchrotron white-beam topography. J. Synchrotron Radiat. 10, 416–420 (2003).

    Article  Google Scholar 

  25. Koizumi, H., Tachibana, M., Yoshizaki, I. & Kojima, K. Analysis of dislocation images in X-ray topography of protein crystals: tetragonal hen egg-white lysozyme crystals. Philos. Mag. 85, 3709–3717 (2005).

    Article  ADS  Google Scholar 

  26. Durbin, S. D. & Feher, G. Studies of crystal-growth mechanisms of proteins by electron-microscopy. J. Mol. Biol. 212, 763–774 (1990).

    Article  Google Scholar 

  27. Sleutel, M., Sazaki, G. & Van Driessche, A. E. S. Spiral-mediated growth can lead to crystals of higher purity. Cryst. Growth Des. 12, 2367–2374 (2012).

    Article  Google Scholar 

  28. Maruyama, M. et al. Effects of a forced solution flow on the step advancement on {110} faces of tetragonal lysozyme crystals: direct visualization of individual steps under a forced solution flow. Cryst. Growth Des. 12, 2856–2863 (2012).

    Article  Google Scholar 

  29. Sazaki, G., Tsukamoto, K., Yai, S., Okada, M. & Nakajima, K. In situ observation of dislocations in protein crystals during growth by advanced optical microscopy. Cryst. Growth Des. 5, 1729–1735 (2005).

    Article  Google Scholar 

  30. DePristo, M. A., de Bakker, P. I. W. & Blundell, T. L. Heterogeneity and inaccuracy in protein structures solved by X-ray crystallography. Structure 12, 831–838 (2004).

    Article  Google Scholar 

Download references

Acknowledgements

We thank G. Sazaki, S. Nakayama and Y. Hayashi for experimental support and helpful discussions. We also thank K. Baba and N. Mizuno for experimental support at SPring-8 (Hyogo, Japan), and H. Sugiyama, T. Kishi and R. Suzuki for experimental support at PF (Tsukuba, Japan). The synchrotron radiation X-ray diffraction was performed at SPring-8 with the approval of the Japan Synchrotron Radiation Research Institute (JASRI) (Proposal numbers 2014B1195 and 2015B2046). The synchrotron radiation X-ray topography was performed at the Photon Factory under the auspices of the Photon Factory Program Advisory Committee of the High Energy Accelerator Research Organization (Proposal numbers 2013G649 and 2015G714). This work was partly supported by grants from the Japan Society for the Promotion of Science to Y.M. (KAKENHI Nos. 26286042 and 15K13800) and to H.Y.Y. (KAKENHI grant numbers 15H05351 and 16K12868). This work was also partly supported by a grant from the JGC-S Scholarship foundation to H.Y.Y.

Author information

Author notes

  1. Mihoko Maruyama

    Present address: Present addresses: Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, Hangi-cho 1-5, Shimogamo, Sakyo-ku, Kyoto 606-8522, Japan; Institute of Low Temperature Science, Hokkaido University, N19-W8, Kita-ku, Sapporo 060-0819, Japan,

Authors and Affiliations

  1. Graduate School of Engineering, Osaka University, Yamadaoka 2-1, Suita, 565-0871, Osaka, Japan

    Yusuke Tominaga, Mihoko Maruyama, Masashi Yoshimura, Hiroaki Adachi, Katsuo Tsukamoto, Tsuyoshi Inoue, Hiroshi Y. Yoshikawa & Yusuke Mori

  2. Institute for Materials Research, Tohoku University, Katahira 2-1-1, Aoba-ku, 980-8577, Sendai, Japan

    Haruhiko Koizumi

  3. Graduate School of Nanobioscience, Yokohama City University, Seto 22-2, Kanazawa-ku, 236-0027, Yokohama, Japan

    Masaru Tachibana

  4. Graduate School of Science, Osaka University, Yamadaoka 2-1, Suita, 565-0871, Osaka, Japan

    Shigeru Sugiyama

  5. SOSHO Inc., Yamadaoka 2-1, Suita, 565-0871, Osaka, Japan

    Hiroaki Adachi, Hiroyoshi Matsumura, Kazufumi Takano, Satoshi Murakami, Tsuyoshi Inoue & Yusuke Mori

  6. College of Life Sciences, Ritsumeikan University, Noji-higashi 1-1-1, Kusatsu, 525-8577, Shiga, Japan

    Hiroyoshi Matsumura

  7. Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, Hangi-cho 1-5, Shimogamo, Sakyo-ku, 606-8522, Kyoto, Japan

    Kazufumi Takano

  8. Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Nagatsuda 4259, Midori-ku, Yokohama, 226-8501, Kanagawa, Japan

    Satoshi Murakami

  9. Department of Chemistry, Saitama University, Shimo-okubo 255, Sakura-ku, Saitama, 338-8570, Saitama, Japan

    Hiroshi Y. Yoshikawa

Authors
  1. Yusuke Tominaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mihoko Maruyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Masashi Yoshimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Haruhiko Koizumi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Masaru Tachibana
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shigeru Sugiyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hiroaki Adachi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Katsuo Tsukamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hiroyoshi Matsumura
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Kazufumi Takano
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Satoshi Murakami
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Tsuyoshi Inoue
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Hiroshi Y. Yoshikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Yusuke Mori
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Y.T., M.M. and H.Y.Y. designed the research and wrote the paper. Y.T. carried out the laser experiments with help from M.M., H.Y.Y., M.Y. and Y.M. S.S. helped to perform the X-ray diffraction experiments. H.K. and M.T. carried out the X-ray topography measurements. All authors discussed the results.

Corresponding authors

Correspondence to Mihoko Maruyama or Hiroshi Y. Yoshikawa.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary information (PDF 1072 kb)

Supplementary information

Supplementary movie 1 (AVI 1533 kb)

Supplementary information

Supplementary movie 2 (AVI 985 kb)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tominaga, Y., Maruyama, M., Yoshimura, M. et al. Promotion of protein crystal growth by actively switching crystal growth mode via femtosecond laser ablation. Nature Photon 10, 723–726 (2016). https://doi.org/10.1038/nphoton.2016.202

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nphoton.2016.202

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing