Journal of Biomedical Physics and Engineering

Current Issue

By Issue

By Author

By Subject

Author Index

Keyword Index

About Journal

Aims and Scope

Staff Members

Editorial Board

Publication Ethics

Indexing and Abstracting

Related Links

FAQ

Peer Review Process

News

Ultrasound Waves Effect on the Proliferation of Fibroblast Cells: Collagen Type I Expression

Document Type : Original Research

Authors

1 Department of Medical Physics, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran

2 Skin and Stem Cells Research Center, Tehran University of Medical Sciences, Tehran, Iran

3 Department of Radiology Technology, Allied Medical Faculty, Shahid Beheshti University of Medical Sciences, Tehran, Iran

10.31661/jbpe.v0i0.2212-1567

Abstract

Background: Ultrasound waves are considered non-invasive, safe, and mechanical stimuli with unknown mechanisms.
Objective: The aim of this study is to determine the effect of acoustic cavitation interaction according to the mechanical index (MI) on fibroblast cells’ reproducibility and gene expression of collagen Ι as a skin repair agent.
Material and Methods: In this interventional study, the ultrasonic pressure equations were solved to extracted the maximum mechanical indices with frequencies of 150 kHz, 40 kHz, 28 kHz and low intensity (<0.5 W/cm2). Groups were extracted with a mechanical index of 0.10, 0.20, and 0.40. Then, fibroblast cells were exposed to selected acoustic parameters from simulation. After 5 days, the proliferation was measured with an MTT (3-(4, 5-Dimethylthiazol-2-yl)-2, 5-diphenyltetrazolium bromide) assay, and collagen Ι expression was quantified.
Results: Increasing reproducibility in the groups of 0.23 W/cm2 with 0.20 mechanical index threshold was calculated at 1.70±0.05 and 1.07±0.04 times higher in continuous and pulse modes compared to the control group. Reducing the proliferation in group 0.40 mechanical index was shown as compared with control and sham groups in pulse mode (P-value<0.05). The collagen Ι expression level of fibroblast cells in groups of control and 0.20 MI were 0.03±0.00 and 0.17±0.05, respectively. The acoustic vibration effects at 0.20 mechanical index have promoted fibroblast cell functions. 
Conclusion: Low-frequency and -intensity ultrasound waves on the mechanical index threshold (cavitation threshold) increases the proliferation of fibroblast cell and the expression of collagen type Ι.

Highlights

Zeinab Hormozi Moghaddam (Google Scholar)

Manijhe Mokhtari-Dizaji (Google Scholar)

Keywords

References
  1. Ter Haar G. Therapeutic applications of ultrasound. Prog Biophys Mol Biol. 2007;93(1-3):111-29. doi: 10.1016/j.pbiomolbio.2006.07.005. PubMed PMID: 16930682.
  2. Paliwal S, Mitragotri S. Therapeutic opportunities in biological responses of ultrasound. Ultrasonics. 2008;48(4):271-8. doi: 10.1016/j.ultras.2008.02.002. PubMed PMID: 18406440.
  3. Lv Y, Nan P, Chen G, Sha Y, Xia B, Yang L. In vivo repair of rat transected sciatic nerve by low-intensity pulsed ultrasound and induced pluripotent stem cells-derived neural crest stem cells. Biotechnol Lett. 2015;37(12):2497-506. doi: 10.1007/s10529-015-1939-5. PubMed PMID: 26303432.
  4. Claes L, Willie B. The enhancement of bone regeneration by ultrasound. Prog Biophys Mol Biol. 2007;93(1-3):384-98. doi: 10.1016/j.pbiomolbio.2006.07.021. PubMed PMID: 16934857.
  5. Tassinary JAF, Lunardelli A, Basso BS, Dias HB, Catarina AV, Stülp S, et al. Low-intensity pulsed ultrasound (LIPUS) stimulates mineralization of MC3T3-E1 cells through calcium and phosphate uptake. 2018;84:290-95. doi: 10.1016/j.ultras.2017.11.011. PubMed PMID: 29182945.
  6. Karsdal MA. Biochemistry of collagens, Laminins and elastin. 2nd ed, Academic Press; 2019. p. 56-67.
  7. Wang KH, Chan WP, Chiu LH, Tsai YH, Fang CL, Yang CB, et al. Histological and Immunohistochemical Analyses of Repair of the Disc in the Rabbit Temporomandibular Joint Using a Collagen Template. Materials (Basel). 2017;10(8):924. doi: 10.3390/ma10080924. PubMed PMID: 28792464. PubMed PMCID: PMC5578290.
  8. Tang ZF, Li HY. Effects of fibroblast growth factors 2 and low intensity pulsed ultrasound on the repair of knee articular cartilage in rabbits. Eur Rev Med Pharmacol Sci. 2018;22(8):2447-53. doi: 10.26355/eurrev_201804_14838. PubMed PMID: 29762847.
  9. Harding KG, Morris HL, Patel GK. Science, medicine and the future: healing chronic wounds. 2002;324(7330):160-3. doi: 10.1136/bmj.324.7330.160. PubMed PMID: 11799036. PubMed PMCID: PMC1122073.
  10. Sorrell JM, Caplan AI. Fibroblast heterogeneity: more than skin deep. J Cell Sci. 2004;117(Pt 5):667-75. doi: 10.1242/jcs.01005. PubMed PMID: 14754903.
  11. Sato M, Nagata K, Kuroda S, Horiuchi S, Nakamura T, Karima M, et al. Low-intensity pulsed ultrasound activates integrin-mediated mechanotransduction pathway in synovial cells. Ann Biomed Eng. 2014;42(10):2156-63. doi: 10.1007/s10439-014-1081-x. PubMed PMID: 25096496.
  12. Takeuchi R, Ryo A, Komitsu N, Mikuni-Takagaki Y, Fukui A, Takagi Y, et al. Low-intensity pulsed ultrasound activates the phosphatidylinositol 3 kinase/Akt pathway and stimulates the growth of chondrocytes in three-dimensional cultures: a basic science study. Arthritis Res Ther. 2008;10(4):R77. doi: 10.1186/ar2451. PubMed PMID: 18616830. PubMed PMCID: PMC2575623.
  13. Tran TA, Roger S, Le Guennec JY, Tranquart F, Bouakaz A. Effect of ultrasound-activated microbubbles on the cell electrophysiological properties. Ultrasound Med Biol. 2007;33(1):158-63. doi: 10.1016/j.ultrasmedbio.2006.07.029. PubMed PMID: 17189059.
  14. Safari M, Ghanati F, Hajnoruzi A, Rezaei A, Abdolmaleki P, Mokhtari-Dizaji M. Maintenance of membrane integrity and increase of taxanes production in hazel (Corylus avellana L.) cells induced by low-intensity ultrasound. Biotechnol Lett. 2012;34(6):1137-41. doi: 10.1007/s10529-012-0865-z. PubMed PMID: 22315099.
  15. Hormozi-Moghaddam Z, Mokhtari-Dizaji M, Nilforoshzadeh MA, Bakhshandeh M. Low-intensity ultrasound to induce proliferation and collagen I expression of adipose-derived mesenchymal stem cells and fibroblast cells in co-culture. Measurement. 2021;167:108280. doi: 10.1016/j.measurement.2020.108280.
  16. Zhou S, Schmelz A, Seufferlein T, Li Y, Zhao J, Bachem MG. Molecular mechanisms of low intensity pulsed ultrasound in human skin fibroblasts. J Biol Chem. 2004;279(52):54463-9. doi: 10.1074/jbc.M404786200. PubMed PMID: 15485877.
  17. Moghaddam ZH, Mokhtari-Dizaji M, Movahedin M, Ravari ME. Estimation of the distribution of low-intensity ultrasound mechanical index as a parameter affecting the proliferation of spermatogonia stem cells in vitro. Ultrason Sonochem. 2017;37:571-81. doi: 10.1016/j.ultsonch.2017.02.013. PubMed PMID: 28427670.
  18. Moghaddam ZH, Mokhtari-Dizaji M, Movahedin M. Effect of Acoustic Cavitation on Mouse Spermatogonial Stem Cells: Colonization and Viability. J Ultrasound Med. 2021;40(5):999-1010. doi: 10.1002/jum.15476. PubMed PMID: 32876351.
  19. Church CC, Labuda C, Nightingale K. A theoretical study of inertial cavitation from acoustic radiation force impulse imaging and implications for the mechanical index. Ultrasound Med Biol. 2015;41(2):472-85. doi: 10.1016/j.ultrasmedbio.2014.09.012. PubMed PMID: 25592457. PubMed PMCID: PMC4297318.
  20. Ebrahiminia A, Mokhtari-Dizaji M, Toliyat T. Dual frequency cavitation event sensor with iodide dosimeter. Ultrason Sonochem. 2016;28:276-82. doi: 10.1016/j.ultsonch.2015.07.005. PubMed PMID: 26384909.
  21. Razavi S, Salimi M, Shahbazi-Gahrouei D, Karbasi S, Kermani S. Extremely low-frequency electromagnetic field influences the survival and proliferation effect of human adipose derived stem cells. Adv Biomed Res. 2014;3:25-31. doi: 10.4103/2277-9175.124668. PubMed PMID: 24592372. PubMed PMCID: PMC3928843.
  22. Hashimoto T, Kojima K, Tamada Y. Higher gene expression related to wound healing by fibroblasts on silk fibroin biomaterial than on collagen. Molecules. 2020;25(8):1939. doi: 10.3390/molecules25081939. PubMed PMID: 32331316. PubMed PMCID: PMC7221890.
  23. Hormozi Moghaddam Z, Mokhtari-Dizaji M, Nilforoshzadeh MA, Bakhshandeh M, Ghaffari Khaligh S. Low-intensity ultrasound combined with allogenic adipose-derived mesenchymal stem cells (AdMSCs) in radiation-induced skin injury treatment. Sci Rep. 2020;10(1):20006. doi: 10.1038/s41598-020-77019-9. PubMed PMID: 33203925. PubMed PMCID: PMC7673019.
  24. Widegren U, Wretman C, Lionikas A, Hedin G, Henriksson J. Influence of exercise intensity on ERK/MAP kinase signalling in human skeletal muscle. Pflugers Arch. 2000;441(2-3):317-22. doi: 10.1007/s004240000417. PubMed PMID: 11211119.
  25. Dougherty CJ, Kubasiak LA, Prentice H, Andreka P, Bishopric NH, Webster KA. Activation of c-Jun N-terminal kinase promotes survival of cardiac myocytes after oxidative stress. Biochem J. 2002;362(Pt 3):561-71. doi: 10.1042/0264-6021:3620561. PubMed PMID: 11879182. PubMed PMCID: PMC1222419.
  26. Kyriakis JM, Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev. 2001;81(2):807-69. doi: 10.1152/physrev.2001.81.2.807. PubMed PMID: 11274345.
  27. Rodgers KE, Tan A, Kim L, Espinoza T, Meeks C, Johnston W, Maulhardt H, Donald M, Hill C, diZerega GS. Development of a guinea pig cutaneous radiation injury model using low penetrating X-rays. Int J Radiat Biol. 2016;92(8):434-43. doi: 10.1080/09553002.2016.1186302. PubMed PMID: 27258737.
  28. Conner-Kerr T, Malpass G, Steele A, Howlett A. Effects of 35 kHz, low-frequency ultrasound application in vitro on human fibroblast morphology and migration patterns. Ostomy Wound Manage. 2015;61(3):34-41. PubMed PMID: 25751849.
  29. Ebrahiminia A, Mokhtari-Dizaji M, Toliyat T. Correlation between iodide dosimetry and terephthalic acid dosimetry to evaluate the reactive radical production due to the acoustic cavitation activity. Ultrason Sonochem. 2013;20(1):366-72. doi: 10.1016/j.ultsonch.2012.05.016. PubMed PMID: 22766173.
  30. Doan N, Reher P, Meghji S, Harris M. In vitro effects of therapeutic ultrasound on cell proliferation, protein synthesis, and cytokine production by human fibroblasts, osteoblasts, and monocytes. J Oral Maxillofac Surg. 1999;57(4):409-19. doi: 10.1016/s0278-2391(99)90281-1. PubMed PMID: 10199493.
  31. Yoon JH, Roh EY, Shin S, Jung NH, Song EY, Lee DS, et al. Introducing pulsed low-intensity ultrasound to culturing human umbilical cord-derived mesenchymal stem cells. Biotechnol Lett. 2009;31(3):329-35. doi: 10.1007/s10529-008-9872-5. PubMed PMID: 18985278.
  32. Franco de Oliveira R, Pires Oliveira DA, Soares CP. Effect of low-intensity pulsed ultrasound on l929 fibroblasts. Arch Med Sci. 2011;7(2):224-9. doi: 10.5114/aoms.2011.22071. PubMed PMID: 22291760. PubMed PMCID: PMC3258710.
  33. Man J, Shelton RM, Cooper PR, Landini G, Scheven BA. Low intensity ultrasound stimulates osteoblast migration at different frequencies. J Bone Miner Metab. 2012;30(5):602-7. doi: 10.1007/s00774-012-0368-y. PubMed PMID: 22752127.
Journal of Biomedical Physics and Engineering
Volume 15, Issue 3 - Serial Number 1
71
June 2025
Pages 249-262
Files
Share
How to cite
Statistics