Advertisement

Journal of Medical Ultrasonics

, Volume 39, Issue 4, pp 207–216 | Cite as

Ultrasound stimulation induces microRNA expression changes that could be involved in sonication-induced apoptosis

  • Ryohei OgawaEmail author
  • Akihiro Morii
  • Akihiko Watanabe
Original Article

Abstract

Purpose

The purpose of this study is to investigate the involvement of microRNAs (miRNAs) in sonication-induced apoptosis.

Methods

U937 cells derived from human leukemia were sonicated with 1-MHz ultrasound at 0.4 W/cm2 and 10 % duty factor for 60 s, a condition inducing apoptosis. The total RNA was extracted from cells at various timings after sonication and subjected to microarray and real-time PCR for miRNA expression analyses.

Results

Expression of several miRNAs was significantly affected by sonication. For miR-424* and miR-720, whose expressions were eminently decreased by sonication, cell lines overexpressing these miRNAs were established. Conversely, for miR-663B and miR-663, whose expressions were eminently increased by sonication, cell lines inhibiting these miRNA functions were established. When these cell lines were sonicated, a cell line inhibiting miR-663B function significantly increased sonication-induced apoptosis, suggesting this may be involved in cellular responses to sonication. Two genes that could induce apoptosis, KSR2 and CREBZF, were identified as potential target genes of miR-663B since potential target sequences on their 3′ UTR mediated to decrease expression of a reporter gene.

Conclusion

These results suggest that miRNAs may be involved in cellular responses to ultrasound through their expression changes caused by sonication.

Keywords

MicroRNA Apoptosis Microarray Expression 

Notes

Acknowledgments

This research was supported by the Research and Development Committee Program of The Japan Society of Ultrasonics in Medicine. The authors thank Drs. Loreto B. Feril, Jr., and Go Kagiya for their critical reading of the manuscript.

References

  1. 1.
    Suslick KS. Sonochemistry. Science. 1990;247:1439–45.PubMedCrossRefGoogle Scholar
  2. 2.
    Riesz P, Kondo T. Free radical formation induced by ultrasound and its biological implications. Free Radic Biol Med. 1992;13:247–70.PubMedCrossRefGoogle Scholar
  3. 3.
    Lagos-Quintana M, Rauhut R, Lendeckel W, et al. Identification of novel genes coding for small expressed RNAs. Science. 2001;294:853.PubMedCrossRefGoogle Scholar
  4. 4.
    Lee RC, Ambros V. An extensive class of small RNAs in Caenorhabditis elegans. Science. 2001;294:797.CrossRefGoogle Scholar
  5. 5.
    Farazi TA, Juranek SA, Tuschl T. The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development. 2008;135:1201–4.PubMedCrossRefGoogle Scholar
  6. 6.
    Stefani G, Slack FJ. Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol. 2008;9:219–30.PubMedCrossRefGoogle Scholar
  7. 7.
    Oh JS, Kim JJ, Byun JY, et al. Lin28-let7 modulates radiosensitivity of human cancer cells with activation of K-Ras. Int J Radiat Oncol Biol Phys. 2010;76:5–8.PubMedCrossRefGoogle Scholar
  8. 8.
    Wilmink GJ, Roth CL, Ibey BL, et al. Identification of microRNAs associated with hyperthermia-induced cellular stress response. Cell Stress Chaperones. 2010;15:1027–38.PubMedCrossRefGoogle Scholar
  9. 9.
    Fornari F, Gramantieri L, Giovannini C, et al. MiR-122/cyclin G1 interaction modulates p53 activity and affects doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res. 2009;69:5761–7.PubMedCrossRefGoogle Scholar
  10. 10.
    Kulshreshtha R, Ferracin M, Wojcik SE, et al. A microRNA signature of hypoxia. Mol Cell Biol. 2007;27:1859–67.PubMedCrossRefGoogle Scholar
  11. 11.
    Tabuchi Y, Kondo T, Ogawa R, et al. DNA microarray analyses of genes elicited by ultrasound in human U937 cells. Biochem Biophys Res Commun. 2002;290:498–503.PubMedCrossRefGoogle Scholar
  12. 12.
    Abdollahi A, Domhan S, Jenne JW, et al. Apoptosis signals in lymphoblasts induced by focused ultrasound. FASEB J. 2004;18:1413–4.PubMedGoogle Scholar
  13. 13.
    Ashush H, Rozenszajn LA, Blass M, et al. Apoptosis induction of human myeloid leukemic cells by ultrasound exposure. Cancer Res. 2000;60:1014–20.PubMedGoogle Scholar
  14. 14.
    Sambrook J, Russell DW. Molecular cloning: a laboratory manual. 3rd ed. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 2001.Google Scholar
  15. 15.
    Sellins KS, Cohen JJ. Nuclear changes in the cytotoxic T lymphocyte-induced model of apoptosis. Immunol Rev. 1995;146:241–66.PubMedCrossRefGoogle Scholar
  16. 16.
    Haraguchi T, Ozaki Y, Iba H. Vectors expressing efficient RNA decoys achieve the long-term suppression of specific microRNA activity in mammalian cells. Nucleic Acids Res. 2009;37:e43.PubMedCrossRefGoogle Scholar
  17. 17.
    Ebert MS, Sharp PA. MicroRNA sponges: progress and possibilities. RNA. 2010;16:2043–50.PubMedCrossRefGoogle Scholar
  18. 18.
    Honda H, Kondo T, Zhao QL. Role of intracellular calcium ions and reactive oxygen species in apoptosis induced by ultrasound. Ultrasound Med Biol. 2004;30:683–92.PubMedCrossRefGoogle Scholar
  19. 19.
    Simone NL, Soule BP, Ly D, et al. Ionizing radiation-induced oxidative stress alters miRNA expression. PLoS ONE. 2009;4:e6377.PubMedCrossRefGoogle Scholar
  20. 20.
    Mason TJ. Therapeutic ultrasound an overview. Ultrason Sonochem. 2011;18:847–52.PubMedCrossRefGoogle Scholar
  21. 21.
    Rosenthal I, Sostaric JZ, Riesz P. Sonodynamic therapy—a review of the synergistic effects of drugs and ultrasound. Ultrason Sonochem. 2004;11:349–63.PubMedGoogle Scholar
  22. 22.
    Ogawa R, Lee SI, Izumi H, et al. Enhancement of artificial promoter activity by ultrasound-induced oxidative stress. Ultrason Sonochem. 2009;16:379–86.PubMedCrossRefGoogle Scholar
  23. 23.
    Watanabe A, Kakutani S, Ogawa R, et al. Construction of artificial promoters sensitively responsive to sonication. J Med Ultrason. 2009;36:9–17.CrossRefGoogle Scholar
  24. 24.
    Eker OF, Quesson B, Rome C, et al. Combination of cell delivery and thermoinducible transcription for in vivo spatiotemporal control of gene expression: a feasibility study. Radiology. 2011;258:496–504.PubMedCrossRefGoogle Scholar

Copyright information

© The Japan Society of Ultrasonics in Medicine 2012

Authors and Affiliations

  1. 1.Department of Radiological Sciences, Graduate School of Medicine and Pharmaceutical Sciences for ResearchUniversity of ToyamaToyamaJapan
  2. 2.Department of Urology, Graduate School of Medicine and Pharmaceutical Sciences for ResearchUniversity of ToyamaToyamaJapan

Personalised recommendations