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Clinical Oral Investigations

, Volume 20, Issue 7, pp 1801–1808 | Cite as

Non-thermal atmospheric pressure plasma increased mRNA expression of growth factors in human gingival fibroblasts

  • Jae-Sung Kwon
  • Yong Hee Kim
  • Eun Ha Choi
  • Chong-Kwan Kim
  • Kyoung-Nam Kim
  • Kwang-Mahn KimEmail author
Original Article

Abstract

Objectives

The aim of this in vitro study was to investigate the effects of a non-thermal atmospheric pressure plasma jet (NTAPPJ) on the cellular activity of human gingival fibroblasts (HGF) for possible non-surgical application of it during gingival wound healing.

Materials and methods

HGF cells were exposed with NTAPPJ for 1, 2, and 4 min and were investigated for cellular attachment, cell viability, morphology of attached cells, proliferation rate, and messenger ribonucleic acid (mRNA) expression of various growth factors. Also, scavengers for chemicals produced by NTAPPJ were used to identify the chemical species responsible for the effects.

Results

There was no significant change in the number of HGF cells attached or their proliferation following NTAPPJ exposure. Also, high cell viability resulted from exposure of all of HGF cells to NTAPPJ for 1, 2, and 4 min. However, cells were more stretched while the mRNA expressions of transforming growth factor and vascular endothelial growth factor were significantly increased following NTAPPJ exposure. Additionally, the scavenger test showed that nitric oxide is likely to be the chemical responsible for an increase of cellular activity.

Conclusion

The results demonstrated that the NTAPPJ increased mRNA expressions of growth factors in human gingival fibroblasts.

Clinical relevance

Application of NTAPPJ would be useful in gingival wound healing in clinics though additional studies confirming the effects would be needed.

Keywords

Gingival fibroblast Non-thermal atmospheric pressure plasma Nitric oxide Growth factors 

Notes

Acknowledgments

This research was supported by the National Research Foundation of Korea (NRF) funded by the Korea government (MSIP) (NRF-2010-0027963).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

References

  1. 1.
    Pihlstrom BL, Michalowicz BS, Johnson NW (2005) Periodontal diseases. Lancet 366(9499):1809–1820CrossRefPubMedGoogle Scholar
  2. 2.
    Dorn JM, Genco RJ, Grossi SG, Falkner KL, Hovey KM, Iacoviello L, Trevisan M (2010) Periodontal disease and recurrent cardiovascular events in survivors of myocardial infarction (MI): the Western New York Acute MI Study. J Periodontol 81(4):502–511CrossRefPubMedGoogle Scholar
  3. 3.
    Ahn YB, Shin MS, Byun JS and Kim HD (2015) The association of hypertension with periodontitis is highlighted in female adults; results from the Fourth Korea National Health and Nutrition Examination Survey (KNHANES IV). J Clin Periodontol doi:10.1111/jcpe.12471. [Epub ahead of print]Google Scholar
  4. 4.
    Ishikawa I, Baehni P (2004) Nonsurgical periodontal therapy—where do we stand now? Periodontol 2000(36):9–13CrossRefGoogle Scholar
  5. 5.
    Cochran DL, Wozney JM (1999) Biological mediators for periodontal regeneration. Periodontol 2000(19):40–58CrossRefGoogle Scholar
  6. 6.
    Ivanovski S, Haase HR, Bartold PM (2001) Isolation and characterization of fibroblasts derived from regenerating human periodontal defects. Arch Oral Biol 46(8):679–688CrossRefPubMedGoogle Scholar
  7. 7.
    Bartold PM, Walsh LJ and Narayanan S (2000) Molecular and cell biology of the gingiva. Periodontol 2000 24:28–55Google Scholar
  8. 8.
    Yu N, Oortgiesen DAW, Bronckers ALJJ, Yang F, Walboomers XF, Jansen JA (2013) Enhanced periodontal tissue regeneration by periodontal cell implantation. J Clin Periodontol 40(7):698–706CrossRefPubMedGoogle Scholar
  9. 9.
    Zeldich E, Koren R, Nemcovsky C, Weinreb M (2007) Enamel matrix derivative stimulates human gingival fibroblast proliferation via ERK. J Dent Res 86(1):41–46CrossRefPubMedGoogle Scholar
  10. 10.
    Anitua E, Troya M, Orive G (2012) Plasma rich in growth factors promote gingival tissue regeneration by stimulating fibroblast proliferation and migration and by blocking transforming growth factor-beta 1-induced myodifferentiation. J Periodontol 83(8):1028–1037CrossRefPubMedGoogle Scholar
  11. 11.
    Kreisler M, Christoffers AB, Willershausen B, d'Hoedt B (2003) Effect of low-level GaAlAs laser irradiation on the proliferation rate of human periodontal ligament fibroblasts: an in vitro study. J Clin Periodontol 30(4):353–358CrossRefPubMedGoogle Scholar
  12. 12.
    Pourzarandian A, Watanabe H, Ruwanpura SMPM, Aoki A, Ishikawa I (2005) Effect of low-level Er:G laser irradiation on cultured human gingival fibroblasts. J Periodontol 76(2):187–193CrossRefPubMedGoogle Scholar
  13. 13.
    Izumi Y, Aoki A, Yamada Y, Kobayashi H, Iwata T, Akizuki T, Suda T, Nakamura S, Wara-Aswapati N, Ueda M and Ishikawa I (2011) Current and future periodontal tissue engineering. Periodontol 2000 56(1):166–187Google Scholar
  14. 14.
    Fridman G, Friedman G, Gutsol A, Shekhter AB, Vasilets VN, Fridman A (2008) Applied plasma medicine. Plasma Process Polym 5(6):503–533CrossRefGoogle Scholar
  15. 15.
    Roth JR (1995) Industrial plasma engineering. Institute of Physics Pub., Bristol; PhiladelphiaGoogle Scholar
  16. 16.
    Kwon JS, Kim YH, Choi EH, Kim KN (2013) Development of ultra-hydrophilic and non-cytotoxic dental vinyl polysiloxane impression materials using a non-thermal atmospheric-pressure plasma jet. J Phys D Appl Phys 46(19):195201CrossRefGoogle Scholar
  17. 17.
    Kalghatgi S, Kelly CM, Cerchar E, Torabi B, Alekseev O, Fridman A, Friedman G, Azizkhan-Clifford J (2011) Effects of non-thermal plasma on mammalian cells. PLoS One 6(1):e16270CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Kwon JS, Kim YH, Choi EH, Kim KN (2013) The effects of non-thermal atmospheric pressure plasma jet on attachment of osteoblast. Curr Appl Phys 13:S42–S47CrossRefGoogle Scholar
  19. 19.
    Hakki SS, Bozkurt SB (2012) Effects of different setting of diode laser on the mRNA expression of growth factors and type I collagen of human gingival fibroblasts. Laser Med Sci 27(2):325–331CrossRefGoogle Scholar
  20. 20.
    Lin SJ, Lu HK, Lee HW, Chen YC, Li CL, Wang LF (2012) Nitric oxide inhibits androgen receptor-mediated collagen production in human gingival fibroblasts. J Periodontal Res 47(6):701–710CrossRefPubMedGoogle Scholar
  21. 21.
    Nicolescu AC, Li Q, Brown L, Thatcher GRJ (2006) Nitroxidation, nitration, and oxidation of a BODIPY fluorophore by RNOS and ROS. Nitric Oxide-Biol Ch 15(2):163–176CrossRefGoogle Scholar
  22. 22.
    Franco R, Panayiotidis MI, Cidlowski JA (2007) Glutathione depletion is necessary for apoptosis in lymphoid cells independent of reactive oxygen species formation. J Biol Chem 282(42):30452–30465CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Nerem RM (1991) Cellular engineering. Ann Biomed Eng 19(5):529–545CrossRefPubMedGoogle Scholar
  24. 24.
    Bianco P, Riminucci M, Gronthos S, Robey PG (2001) Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19(3):180–192CrossRefPubMedGoogle Scholar
  25. 25.
    Kieft IE, Kurdi M, Stoffels E (2006) Reattachment and apoptosis after plasma-needle treatment of cultured cells. Ieee T Plasma Sci 34(4):1331–1336CrossRefGoogle Scholar
  26. 26.
    Kalghatgi S, Friedman G, Fridman A, Clyne AM (2010) Endothelial cell proliferation is enhanced by low dose non-thermal plasma through fibroblast growth factor-2 release. Ann Biomed Eng 38(3):748–757CrossRefPubMedGoogle Scholar
  27. 27.
    Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110(6):673–687CrossRefPubMedGoogle Scholar
  28. 28.
    Geiger B, Bershadsky A, Pankov R, Yamada KM (2001) Transmembrane crosstalk between the extracellular matrix–cytoskeleton crosstalk. Nat Rev Mol Cell Biol 2(11):793–805CrossRefPubMedGoogle Scholar
  29. 29.
    Tomikawa K, Yamamoto T, Shiomi N, Shimoe M, Hongo S, Yamashiro K, Yamaguchi T, Maeda H, Takashiba S (2012) Smad2 decelerates re-epithelialization during gingival wound healing. J Dent Res 91(8):764–770CrossRefPubMedGoogle Scholar
  30. 30.
    Grazul-Bilska AT, Johnson ML, Bilski JJ, Redmer DA, Reynolds LP, Abdullah A, Abdullah KM (2003) Wound healing: the role of growth factors. Drugs Today 39(10):787–800CrossRefPubMedGoogle Scholar
  31. 31.
    Sosnin EA, Stoffels E, Erofeev MV, Kieft IE, Kunts SE (2004) The effects of UV irradiation and gas plasma treatment on living mammalian cells and bacteria: a comparative approach. Ieee T Plasma Sci 32(4):1544–1550CrossRefGoogle Scholar
  32. 32.
    Furchgott RF (1999) Endothelium-derived relaxing factor: discovery, early studies, and identifcation as nitric oxide (Nobel lecture). Angew Chem Int Edit 38(13–14):1870–1880CrossRefGoogle Scholar
  33. 33.
    Isenberg JS, Ridnour LA, Perruccio EM, Espey MG, Wink DA, Roberts DD (2005) Thrombospondin-1 inhibits endothelial cell responses to nitric oxide in a cGMP-dependent manner. P Natl Acad Sci USA 102(37):13141–13146CrossRefGoogle Scholar
  34. 34.
    Daghigh F, Borghaei RC, Thornton RD, Bee JH (2002) Human gingival fibroblasts produce nitric oxide in response to proinflammatory cytokines. J Periodontol 73(4):392–400CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Jae-Sung Kwon
    • 1
  • Yong Hee Kim
    • 2
  • Eun Ha Choi
    • 2
  • Chong-Kwan Kim
    • 3
  • Kyoung-Nam Kim
    • 1
  • Kwang-Mahn Kim
    • 1
    Email author
  1. 1.BK21 PLUS Project, Department and Research Institute of Dental Biomaterials and BioengineeringYonsei University College of DentistrySeoulRepublic of Korea
  2. 2.Plasma Bioscience Research CenterKwangwoon UniversitySeoulRepublic of Korea
  3. 3.Department of PeriodontologyYonsei University College of DentistrySeoulRepublic of Korea

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