Compressive Force Upregulates Notch Target Genes and NOTCH2 mRNA in Human Dental Pulp Cells

Authors

  • Hataichanok Charoenpong College of Dental Medicine, Rangsit University, Pathum Thani, 12000, Thailand
  • Khitparat Kamoltham College of Dental Medicine, Rangsit University, Pathum Thani, 12000, Thailand
  • Suchada Limsiriwong College of Dental Medicine, Rangsit University, Pathum Thani, 12000, Thailand
  • Rutapakon Insawak College of Dental Medicine, Rangsit University, Pathum Thani, 12000, Thailand
  • Apichart Veerawattanatigul College of Dental Medicine, Rangsit University, Pathum Thani, 12000, Thailand
  • Sirawish Lertchatripong College of Dental Medicine, Rangsit University, Pathum Thani, 12000, Thailand

DOI:

https://doi.org/10.59796/jcst.V14N1.2024.14

Keywords:

dental pulp cells, mechanical force, compressive force, Notch signaling

Abstract

Dental pulp cells encounter compressive force in various situations. While mechanical force can produce various effects on dental pulp cells, the mechanisms underlying their response remain unclear. In this study, we examined the mRNA expression of Notch target genes and Notch receptors in human dental pulp cells (HDPCs) under mechanical compressive force. We utilized two in vitro compressive force application models, direct compression and hydrostatic compression. The results showed that there was an upregulation of Notch target gene, HES1, in HDPCs subjected to the compressive force generated by both models for 2 hours. Hydrostatic compression also upregulated HES1 and HEY1 mRNA expression following 6 hours of force application. NOTCH2 was the only Notch receptor found to be upregulated in HDPCs following compressive force application, in which the upregulation was observed at 6 hours after hydrostatic compression. In conclusion, both hydrostatic and direct compressive forces can upregulate the mRNA expression of Notch target gene, HES1, in HDPCs. However, the hydrostatic compression model produced more prolonged activation of HES1 and it also stimulated the upregulation of HEY1 as well as NOTCH2.

References

Arana-Chavez, V. E., & Massa, L. F. (2004). Odontoblasts: the cells forming and maintaining dentine. International Journal of Biochemistry and Cell Biology, 36(8), 1367-1373. https://doi.org/10.1016/j.biocel.2004.01.006

Bi, P., & Kuang, S. (2015). Notch signaling as a novel regulator of metabolism. Trends in Endocrinology and Metabolism, 26(5), 248-255. https://doi.org/10.1016/j.tem.2015.02.006

Cai, X., Gong, P., Huang, Y., & Lin, Y. (2011). Notch signalling pathway in tooth development and adult dental cells. Cell Proliferation, 44(6), 495-507. https://doi.org/10.1111/j.1365-2184.2011.00780.x

Charoenpong, H., Osathanon, T., Pavasant, P., Limjeerajarus, N., Keawprachum, B., Limjeerajarus, C. N., ... & Ritprajak, P. (2019). Mechanical stress induced S100A7 expression in human dental pulp cells to augment osteoclast differentiation. Oral Diseases, 25(3), 812-821. https://doi.org/10.1111/odi.13033

DuFort, C. C., Paszek, M. J., & Weaver, V. M. (2011). Balancing forces: architectural control of mechanotransduction. Nature Reviews: Molecular Cell Biology, 12(5), 308-319. https://doi.org/10.1038/nrm3112

Gordon, W. R., Zimmerman, B., He, L., Miles, L. J., Huang, J., Tiyanont, K., ... & Blacklow, S. C. (2015). Mechanical Allostery: Evidence for a Force Requirement in the Proteolytic Activation of Notch. Developmental Cell, 33(6), 729-736. https://doi.org/10.1016/j.devcel.2015.05.004

Govitvattana, N., Osathanon, T., Taebunpakul, S., & Pavasant, P. (2013). IL-6 regulated stress-induced Rex-1 expression in stem cells from human exfoliated deciduous teeth. Oral Diseases, 19(7), 673-682. https://doi.org/10.1111/odi.12052

Henrique, D., & Schweisguth, F. (2019). Mechanisms of Notch signaling: a simple logic deployed in time and space. Development, 146(3), Article dev172148. https://doi.org/10.1242/dev.172148

Heyeraas, K. J., & Berggreen, E. (1999). Interstitial fluid pressure in normal and inflamed pulp. Critical Reviews in Oral Biology and Medicine, 10(3), 328-336. http://www.ncbi.nlm.nih.gov/pubmed/10759412

Jahnsen, E. D., Trindade, A., Zaun, H. C., Lehoux, S., Duarte, A., & Jones, E. A. (2015). Notch1 is pan-endothelial at the onset of flow and regulated by flow. PloS One, 10(4), Article e0122622. https://doi.org/10.1371/journal.pone.0122622

Kang, Y. G., Shin, J. W., Park, S. H., Oh, M. J., Park, H. S., Shin, J. W., & Kim, S. H. (2014). Effects of flow-induced shear stress on limbal epithelial stem cell growth and enrichment. PloS One, 9(3), Article e93023. https://doi.org/10.1371/journal.pone.0093023

Kopan, R. (2012). Notch signaling. Cold Spring Harbor Perspectives in Biology, 4(10), Article a011213. https://doi.org/10.1101/cshperspect.a011213

Langridge, P. D., & Struhl, G. (2017). Epsin-Dependent Ligand Endocytosis Activates Notch by Force. Cell, 171(6), 1383-1396.e12. https://doi.org/10.1016/j.cell.2017.10.048

Loerakker, S., Stassen, O., Ter Huurne, F. M., Boareto, M., Bouten, C. V. C., & Sahlgren, C. M. (2018). Mechanosensitivity of Jagged-Notch signaling can induce a switch-type behavior in vascular homeostasis. Proceedings of the National Academy of Sciences of the United States of America, 115(16), E3682-E3691. https://doi.org/10.1073/pnas.1715277115

Lovschall, H., Tummers, M., Thesleff, I., Fuchtbauer, E. M., & Poulsen, K. (2005). Activation of the Notch signaling pathway in response to pulp capping of rat molars. European Journal of Oral Sciences, 113(4), 312-317. https://doi.org/10.1111/j.1600-0722.2005.00221.x

Mack, J. J., Mosqueiro, T. S., Archer, B. J., Jones, W. M., Sunshine, H., Faas, G. C., ... & Iruela-Arispe, M. L. (2017). NOTCH1 is a mechanosensor in adult arteries. Nat Commun, 8(1), Article 1620. https://doi.org/10.1038/s41467-017-01741-8

Manokawinchoke, J., Limjeerajarus, N., Limjeerajarus, C., Sastravaha, P., Everts, V., & Pavasant, P. (2015). Mechanical Force-induced TGFB1 Increases Expression of SOST/POSTN by hPDL Cells. Journal of Dental Research, 94(7), 983-989. https://doi.org/10.1177/0022034515581372

Manokawinchoke, J., Nattasit, P., Thongngam, T., Pavasant, P., Tompkins, K. A., Egusa, H., & Osathanon, T. (2017). Indirect immobilized Jagged1 suppresses cell cycle progression and induces odonto/osteogenic differentiation in human dental pulp cells. Scientific Reports, 7(1), Article 10124. https://doi.org/10.1038/s41598-017-10638-x

Manokawinchoke, J., Pavasant, P., Limjeerajarus, C. N., Limjeerajarus, N., Osathanon, T., & Egusa, H. (2021). Mechanical loading and the control of stem cell behavior. Archives of Oral Biology, 125, 105092. https://doi.org/10.1016/j.archoralbio.2021.105092

Manokawinchoke, J., Sumrejkanchanakij, P., Boonprakong, L., Pavasant, P., Egusa, H., & Osathanon, T. (2020). NOTCH2 participates in Jagged1-induced osteogenic differentiation in human periodontal ligament cells. Scientific Reports, 10(1), Article 13329. https://doi.org/10.1038/s41598-020-70277-7

Marrelli, M., Codispoti, B., Shelton, R. M., Scheven, B. A., Cooper, P. R., Tatullo, M., & Paduano, F. (2018). Dental Pulp Stem Cell Mechanoresponsiveness: Effects of Mechanical Stimuli on Dental Pulp Stem Cell Behavior. Frontiers in Physiology, 9, Article 1685. https://doi.org/10.3389/fphys.2018.01685

Masumura, T., Yamamoto, K., Shimizu, N., Obi, S., & Ando, J. (2009). Shear stress increases expression of the arterial endothelial marker ephrinB2 in murine ES cells via the VEGF-Notch signaling pathways. Arteriosclerosis, Thrombosis, and Vascular Biology, 29(12), 2125-2131. https://doi.org/10.1161/ATVBAHA.109.193185

Matamoro-Vidal, A., & Levayer, R. (2019). Multiple Influences of Mechanical Forces on Cell Competition. Current Biology, 29(15), R762-R774. https://doi.org/10.1016/j.cub.2019.06.030

Meloty-Kapella, L., Shergill, B., Kuon, J., Botvinick, E., & Weinmaster, G. (2012). Notch ligand endocytosis generates mechanical pulling force dependent on dynamin, epsins, and actin. Developmental Cell, 22(6), 1299-1312. https://doi.org/10.1016/j.devcel.2012.04.005

Mitsiadis, T. A., Caton, J., Pagella, P., Orsini, G., & Jimenez-Rojo, L. (2017). Monitoring Notch Signaling-Associated Activation of Stem Cell Niches within Injured Dental Pulp. Frontiers in Physiology, 8, 372. https://doi.org/10.3389/fphys.2017.00372

Mitsiadis, T. A., Fried, K., & Goridis, C. (1999). Reactivation of Delta-Notch signaling after injury: complementary expression patterns of ligand and receptor in dental pulp. Experimental Cell Research, 246(2), 312-318. https://doi.org/10.1006/excr.1998.4285

Mitsiadis, T. A., Romeas, A., Lendahl, U., Sharpe, P. T., & Farges, J. C. (2003). Notch2 protein distribution in human teeth under normal and pathological conditions. Experimental Cell Research, 282(2), 101-109. https://doi.org/10.1016/s0014-4827(02)00012-5

Miyashita, S., Ahmed, N. E. M. B., Murakami, M., Iohara, K., Yamamoto, T., Horibe, H., ... & Nakashima, M. (2017). Mechanical forces induce odontoblastic differentiation of mesenchymal stem cells on three-dimensional biomimetic scaffolds. Journal of Tissue Engineering and Regenerative Medicine, 11(2), 434-446. https://doi.org/10.1002/term.1928

Morrow, D., Cullen, J. P., Cahill, P. A., & Redmond, E. M. (2007). Cyclic strain regulates the Notch/CBF-1 signaling pathway in endothelial cells: role in angiogenic activity. Arteriosclerosis, Thrombosis, and Vascular Biology, 27(6), 1289-1296. https://doi.org/10.1161/ATVBAHA.107.142778

Morrow, D., Sweeney, C., Birney, Y. A., Cummins, P. M., Walls, D., Redmond, E. M., & Cahill, P. A. (2005). Cyclic strain inhibits Notch receptor signaling in vascular smooth muscle cells in vitro. Circulation Research, 96(5), 567-575. https://doi.org/10.1161/01.RES.0000159182.98874.43

Nandagopal, N., Santat, L. A., LeBon, L., Sprinzak, D., Bronner, M. E., & Elowitz, M. B. (2018). Dynamic Ligand Discrimination in the Notch Signaling Pathway. Cell, 172(4), 869-880.e19. https://doi.org/10.1016/j.cell.2018.01.002

Natenstedt, J., Kok, A. C., Dankelman, J., & Tuijthof, G. J. (2015). What quantitative mechanical loading stimulates in vitro cultivation best?. Journal of experimental orthopaedics, 2(1), Article 15. https://doi.org/10.1186/s40634-015-0029-x

Obi, S., Yamamoto, K., Shimizu, N., Kumagaya, S., Masumura, T., Sokabe, T., ... & Ando, J. (2009). Fluid shear stress induces arterial differentiation of endothelial progenitor cells. Journal of applied physiology, 106(1), 203-211. https://doi.org/10.1152/japplphysiol.00197.2008

Peetiakarawach, K., Osathanon, T., Pavasant, P., Rattanaworawipa, R., & Sukarawan, W. (2015). Compressive Stress Enhances NOTCH1 mRNA Expression in Human Deciduous Dental Pulp Cells in vitro. Chulalongkorn University Dental Journal, 38(Suppl), 13-20.

Rad, R. R., Mohaghegh, S., Kouhestani, F., & Motamedian, S. R. (2021). Effect of Mechanical Forces on the Behavior of Dental Stem Cells: A Scoping Review of In-Vitro Studies. Molecular & Cellular Biomechanics, 18(2), 51-67. https://doi.org/10.32604/mcb.2021.015136

Salinas, E. Y., Hu, J. C., & Athanasiou, K. (2018). A Guide for Using Mechanical Stimulation to Enhance Tissue-Engineered Articular Cartilage Properties. Tissue Engineering Part B: Reviews, 24(5), 345-358. https://doi.org/10.1089/ten.TEB.2018.0006

Satrawaha, S., Wongkhantee, S., Pavasant, P., & Sumrejkanchanakij, P. (2011). Pressure induces interleukin-6 expression via the P2Y6 receptor in human dental pulp cells. Archives of Oral Biology, 56(11), 1230-1237. https://doi.org/10.1016/j.archoralbio.2011.05.003

Sestan, N., Artavanis-Tsakonas, S., & Rakic, P. (1999). Contact-dependent inhibition of cortical neurite growth mediated by notch signaling. Science, 286(5440), 741-746. https://doi.org/10.1126/science.286.5440.741

Shaya, O., Binshtok, U., Hersch, M., Rivkin, D., Weinreb, S., Amir-Zilberstein, L., ... & Sprinzak, D. (2017). Cell-Cell Contact Area Affects Notch Signaling and Notch-Dependent Patterning. Developmental Cell, 40(5), 505-511 e506. https://doi.org/10.1016/j.devcel.2017.02.009

Stephenson, N. L., & Avis, J. M. (2012). Direct observation of proteolytic cleavage at the S2 site upon forced unfolding of the Notch negative regulatory region. Proceedings of the National Academy of Sciences of the United States of America, 109(41), E2757-2765. https://doi.org/10.1073/pnas.1205788109

Sumi, A., Hayes, P., D'Angelo, A., Colombelli, J., Salbreux, G., Dierkes, K., & Solon, J. (2018). Adherens Junction Length during Tissue Contraction Is Controlled by the Mechanosensitive Activity of Actomyosin and Junctional Recycling. Developmental Cell, 47(4), 453-463. https://doi.org/10.1016/j.devcel.2018.10.025

Wang, L., Zhou, Z., Chen, Y., Yuan, S., Du, Y., Ju, X., ... & Wang, X. (2017). The Alpha 7 Nicotinic Acetylcholine Receptor of Deciduous Dental Pulp Stem Cells Regulates Osteoclastogenesis During Physiological Root Resorption. Stem Cells Dev, 26(16), 1186-1198. https://doi.org/10.1089/scd.2017.0033

Yu, V., Damek-Poprawa, M., Nicoll, S. B., & Akintoye, S. O. (2009). Dynamic hydrostatic pressure promotes differentiation of human dental pulp stem cells. Biochemical and Biophysical Research Communications, 386(4), 661-665. https://doi.org/10.1016/j.bbrc.2009.06.106

Ziouti, F., Ebert, R., Rummler, M., Krug, M., Müller-Deubert, S., Lüdemann, M., ... & Jundt, F. (2019). NOTCH Signaling Is Activated through Mechanical Strain in Human Bone Marrow-Derived Mesenchymal Stromal Cells. Stem Cells International, 2019, Article 5150634. https://doi.org/10.1155/2019/5150634

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Published

2023-12-06

How to Cite

Charoenpong, H., Kamoltham, K., Limsiriwong, S., Insawak, R., Veerawattanatigul, A., & Lertchatripong , S. (2023). Compressive Force Upregulates Notch Target Genes and NOTCH2 mRNA in Human Dental Pulp Cells. Journal of Current Science and Technology, 14(1), Article 14. https://doi.org/10.59796/jcst.V14N1.2024.14

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Research Article