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The potential use of ascorbic acid to recover the cellular senescence of lipopolysaccharide-induced human apical papilla cells: an in vitro study

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Abstract

Objectives

To examine the effect of lipopolysaccharide (LPS) on cellular senescence induction of human apical papilla cells (hAPCs) and evaluate the potential use of 50 μg/ml ascorbic acid to recover cellular senescence and regenerative functions.

Materials and methods

hAPCs were treated with LPS at 1 and 10 μg/ml either with or without 50 μg/ml ascorbic acid for 48 h. The cellular senescence biomarkers were analyzed by senescence-associated β-galactosidase (SA-β-gal) staining and senescence-related gene expression, p16 and p21. Cell migration, at 12 h and 24 h, was evaluated using a scratch wound assay. Mineralization potential was assessed at 21 days using Alizarin red S staining and dentine sialophosphoprotein (DSPP) and bone sialoprotein (BSP) gene expression.

Results

1 μg/ml and 10 μg/ml LPS stimulation for 48 h induced cellular senescence, as shown by remarkable SA-β-gal staining and p16 and p21 gene expression. The percentage of wound closure and mineralized formation was reduced. The co-incubation with ascorbic acid significantly down-regulated the level of SA-β-gal staining. The reduction of senescence-associated gene expressions was observed. Ascorbic acid improved cell migration, mineralized nodule formation, and the expression of DSPP and BSP genes in LPS-treated hAPCs.

Conclusions

LPS significantly promoted cellular senescence on hAPCs and diminished the cell function capacity. Co-presence of ascorbic acid could impede cellular senescence and possibly improve the regenerative capacity of LPS-induced senescent hAPCs in vitro.

Clinical relevance

The data support the in vitro potential benefit of ascorbic acid on cellular senescence recovery of apical papilla cells.

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References

  1. Torabinejad M, Nosrat A, Verma P, Udochukwu O (2017) Regenerative endodontic treatment or mineral trioxide aggregate apical plug in teeth with necrotic pulps and open apices: a systematic review and meta-analysis. J Endod 43:1806–1820. https://doi.org/10.1016/j.joen.2017.06.029

    Article  PubMed  Google Scholar 

  2. Chen MH, Chen KL, Chen CA, Tayebaty F, Rosenberg P, Lin L (2012) Responses of immature permanent teeth with infected necrotic pulp tissue and apical periodontitis/abscess to revascularization procedures. Int Endod J 45:294–305. https://doi.org/10.1111/j.1365-2591.2011.01978.x

    Article  PubMed  Google Scholar 

  3. Nosrat A, Homayounfar N, Oloomi K (2012) Drawbacks and unfavorable outcomes of regenerative endodontic treatments of necrotic immature teeth: a literature review and report of a case. J Endod 38:1428–1434. https://doi.org/10.1016/j.joen.2012.06.025

    Article  PubMed  Google Scholar 

  4. Becerra P, Ricucci D, Loghin S, Gibbs JL, Lin LM (2014) Histologic study of a human immature permanent premolar with chronic apical abscess after revascularization/revitalization. J Endod 40:133–139. https://doi.org/10.1016/j.joen.2013.07.017

    Article  PubMed  Google Scholar 

  5. Lin LM, Shimizu E, Gibbs JL, Loghin S, Ricucci D (2014) Histologic and histobacteriologic observations of failed revascularization/revitalization therapy: a case report. J Endod 40:291–295. https://doi.org/10.1016/j.joen.2013.08.024

    Article  PubMed  Google Scholar 

  6. Verma P, Nosrat A, Kim J, Price J, Wang P, Bair E, Xu H, Fouad A (2017) Effect of residual bacteria on the outcome of pulp regeneration in vivo. J Dent Res 96:100–106. https://doi.org/10.1177/0022034516671499

    Article  PubMed  CAS  Google Scholar 

  7. Huang GTJ, Sonoyama W, Liu Y, Liu H, Wang S, Shi S (2008) The hidden treasure in apical papilla: the potential role in pulp/dentin regeneration and bioroot engineering. J Endod 34:645–651. https://doi.org/10.1016/j.joen.2008.03.001

    Article  PubMed  PubMed Central  Google Scholar 

  8. Martin FE, Nadkarni MA, Jacques NA, Hunter N (2002) Quantitative microbiological study of human carious dentine by culture and real-time PCR: association of anaerobes with histopathological changes in chronic pulpitis. J Clin Microbiol 40:1698–1704. https://doi.org/10.1128/jcm.40.5.1698-1704.2002

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Narayanan LL, Vaishnavi C (2010) Endodontic microbiology. J Conserv Dent 13:233. https://doi.org/10.4103/2F0972-0707.73386

    Article  PubMed  PubMed Central  Google Scholar 

  10. Cooper PR, Holder MJ, Smith AJ (2014) Inflammation and regeneration in the dentin-pulp complex: a double-edged sword. J Endod 40:S46–S51. https://doi.org/10.1016/j.joen.2014.01.021

    Article  PubMed  Google Scholar 

  11. Kim JC, Lee YH, Yu MK, Lee NH, Park JD, Bhattarai G, Yi HK (2012) Anti-inflammatory mechanism of PPARγ on LPS-induced pulp cells: role of the ROS removal activity. Arch Oral Biol 57:392–400. https://doi.org/10.1016/j.archoralbio.2011.09.009

    Article  PubMed  CAS  Google Scholar 

  12. Zhang J, Zhang Y, Lv H, Yu Q, Zhou Z, Zhu Q, Wang Z, Cooper PR, Smith AJ, Niu Z (2013) Human stem cells from the apical papilla response to bacterial lipopolysaccharide exposure and anti-inflammatory effects of nuclear factor IC. J Endod 39:1416–1422. https://doi.org/10.1016/j.joen.2013.07.018

    Article  PubMed  Google Scholar 

  13. Gölz L, Memmert S, Rath-Deschner B, Jäger A, Appel T, Baumgarten G, Götz W, Frede S (2014) LPS from P. gingivalis and hypoxia increases oxidative stress in periodontal ligament fibroblasts and contributes to periodontitis. Mediators Inflamm 2014:1–13. https://doi.org/10.1155/2014/986264

    Article  CAS  Google Scholar 

  14. Cheng R, Choudhury D, Liu C, Billet S, Hu T, Bhowmick N (2015) Gingival fibroblasts resist apoptosis in response to oxidative stress in a model of periodontal diseases. Cell Death Discov 1:1–8. https://doi.org/10.1038/cddiscovery.2015.46

    Article  CAS  Google Scholar 

  15. Lertchirakarn V, Aguilar P (2017) Effects of lipopolysaccharide on the proliferation and osteogenic differentiation of stem cells from the apical papilla. J Endod 43:1835–1840. https://doi.org/10.1016/j.joen.2017.06.024

    Article  PubMed  Google Scholar 

  16. Liu J, Du J, Chen X, Yang L, Zhao W, Song M, Wang Z, Wang Y (2019) The effects of mitogen-activated protein kinase signaling pathways on lipopolysaccharide-mediated osteo/odontogenic differentiation of stem cells from the apical papilla. J Endod 45:161–167. https://doi.org/10.1016/j.joen.2018.10.009

    Article  PubMed  CAS  Google Scholar 

  17. Lei S, Liu XM, Liu Y, Bi J, Zhu S, Chen X (2020) Lipopolysaccharide downregulates the osteo-/odontogenic differentiation of stem cells from apical papilla by inducing autophagy. J Endod. https://doi.org/10.1016/j.joen.2020.01.009

  18. Jariyamana N, Chuveera P, Dewi A, Leelapornpisid W, Ittichaicharoen J, Chattipakorn S, Srisuwan T (2021) Effects of N-acetyl cysteine on mitochondrial ROS, mitochondrial dynamics, and inflammation on lipopolysaccharide-treated human apical papilla cells. Clin Oral Investig 25:3919–3928. https://doi.org/10.1007/s00784-020-03721-7

    Article  PubMed  Google Scholar 

  19. Weekate K, Chuenjitkuntaworn B, Chuveera P, Vaseenon S, Chompu-inwai P, Ittichaicharoen J, Chattipakorn S, Srisuwan T (2021) Alterations of mitochondrial dynamics, inflammation and mineralization potential of LPS-induced human dental pulp cells after exposure to N-acetyl cysteine, Biodentine or ProRoot MTA. Int Endod J 54:951–965. https://doi.org/10.1111/iej.13484

    Article  PubMed  CAS  Google Scholar 

  20. Tan DQ, Suda T (2018) Reactive oxygen species and mitochondrial homeostasis as regulators of stem cell fate and function. Antioxid Redox Signal 29:149–168. https://doi.org/10.1089/ars.2017.7273

    Article  PubMed  CAS  Google Scholar 

  21. Fridlyanskaya I, Alekseenko L, Nikolsky N (2015) Senescence as a general cellular response to stress: a mini-review. Exp Gerontol 72:124–128. https://doi.org/10.1016/j.exger.2015.09.021

    Article  PubMed  Google Scholar 

  22. Amaya-Montoya M, Pérez-Londoño A, Guatibonza-García V, Vargas-Villanueva A, Mendivil CO (2020) Cellular senescence as a therapeutic target for age-related diseases: a review. Adv Ther 37:1407–1424. https://doi.org/10.1007/s12325-020-01287-0

    Article  PubMed  PubMed Central  Google Scholar 

  23. Campisi J (2005) Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 120:513–522. https://doi.org/10.1016/j.cell.2005.02.003

    Article  PubMed  CAS  Google Scholar 

  24. Turinetto V, Vitale E, Giachino C (2016) Senescence in human mesenchymal stem cells: functional changes and implications in stem cell-based therapy. Int J Mol Sci 17:1164. https://doi.org/10.3390/ijms17071164

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Yu H, Zhao Y, Luo X, Feng Y, Ren Y, Shang H, He Z, Luo X, Chen S, Wang X (2012) Repeated lipopolysaccharide stimulation induces cellular senescence in BV2 cells. Neuroimmunomodulation 19:131–136. https://doi.org/10.1159/000330254

    Article  PubMed  CAS  Google Scholar 

  26. Kim CO, Huh AJ, Han SH, Kim JM (2012) Analysis of cellular senescence induced by lipopolysaccharide in pulmonary alveolar epithelial cells. Arch Gerontol Geriatr 54:e35–e41. https://doi.org/10.1016/j.archger.2011.07.016

    Article  PubMed  CAS  Google Scholar 

  27. Zhao M, Chen X (2015) Effect of lipopolysaccharides on adipogenic potential and premature senescence of adipocyte progenitors. Am J Physiol - Endocrinol Metab 309:E334–E344. https://doi.org/10.1152/ajpendo.00601.2014

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Feng X, Feng G, Xing J, Shen B, Tan W, Huang D, Lu X, Tao T, Zhang J, Li L (2014) Repeated lipopolysaccharide stimulation promotes cellular senescence in human dental pulp stem cells (DPSCs). Cell Tissue Res 356:369–380. https://doi.org/10.1007/s00441-014-1799-7

    Article  PubMed  CAS  Google Scholar 

  29. Aquino-Martinez R, Rowsey JL, Fraser DG, Eckhardt BA, Khosla S, Farr JN, Monroe DG (2020) LPS-induced premature osteocyte senescence: implications in inflammatory alveolar bone loss and periodontal disease pathogenesis. Bone 132:115220. https://doi.org/10.1016/j.bone.2019.115220

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Monacelli F, Acquarone E, Giannotti C, Borghi R, Nencioni A (2017) Vitamin C, aging and Alzheimer’s disease. Nutrients 9:670. https://doi.org/10.3390/nu9070670

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Staudte H, Güntsch A, Völpel A, Sigusch B (2010) Vitamin C attenuates the cytotoxic effects of Porphyromonas gingivalis on human gingival fibroblasts. Arch Oral Biol 55:40–45. https://doi.org/10.1016/j.archoralbio.2009.11.009

    Article  PubMed  CAS  Google Scholar 

  32. Diomede F, Marconi GD, Guarnieri S, D’Attilio M, Cavalcanti MF, Mariggiò MA, Pizzicannella J, Trubiani O (2019) A novel role of ascorbic acid in anti-inflammatory pathway and ROS generation in HEMA treated dental pulp stem cells. Materials 13:130. https://doi.org/10.3390/ma13010130

    Article  PubMed  PubMed Central  ADS  CAS  Google Scholar 

  33. Fawzy El-Sayed KM, Nguyen N, Dörfer CE (2020) Ascorbic acid, inflammatory cytokines (IL-1β/TNF-α/IFN-γ), or their combination’s effect on stemness, proliferation, and differentiation of gingival mesenchymal stem/progenitor cells. Stem Cells Int 2020. https://doi.org/10.1155/2020/8897138

  34. Bhandi S, Alkahtani A, Mashyakhy M, Abumelha AS, Albar NHM, Renugalakshmi A, Alkahtany MF, Robaian A, Almeslet AS, Patil VR (2021) Effect of ascorbic acid on differentiation, secretome and stemness of stem cells from human exfoliated deciduous tooth (SHEDs). J Pers Med 11:589. https://doi.org/10.3390/jpm11070589

    Article  PubMed  PubMed Central  Google Scholar 

  35. Ishikawa S, Iwasaki K, Komaki M, Ishikawa I (2004) Role of ascorbic acid in periodontal ligament cell differentiation. J Periodontol 75:709–716. https://doi.org/10.1902/jop.2004.75.5.709

    Article  PubMed  CAS  Google Scholar 

  36. Van Pham P, Tran NY, Phan NL-C, Vu NB, Phan NK (2016) Vitamin C stimulates human gingival stem cell proliferation and expression of pluripotent markers. In Vitro Cell Dev Biol 52:218–227. https://doi.org/10.1007/s11626-015-9963-2

    Article  CAS  Google Scholar 

  37. Diederich A, Fründ HJ, Trojanowicz B, Navarrete Santos A, Nguyen AD, Hoang-Vu C, Gernhardt CR (2023) Influence of ascorbic acid as a growth and differentiation factor on dental stem cells used in regenerative endodontic therapies. J Clin Med 12:1196. https://doi.org/10.3390/jcm12031196

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Kashino G, Kodama S, Nakayama Y, Suzuki K, Fukase K, Goto M, Watanabe M (2003) Relief of oxidative stress by ascorbic acid delays cellular senescence of normal human and Werner syndrome fibroblast cells. Free Radic Biol Med 35:438–443. https://doi.org/10.1016/S0891-5849(03)00326-5

    Article  PubMed  CAS  Google Scholar 

  39. Kim JE, Jin DH, Lee SD, Hong SW, Shin JS, Lee SK, Jung DJ, Kang JS, Lee WJ (2008) Vitamin C inhibits p53-induced replicative senescence through suppression of ROS production and p38 MAPK activity. Int J Mol Sci 22:651–655. https://doi.org/10.3892/ijmm_00000068

    Article  CAS  Google Scholar 

  40. Burger MG, Steinitz A, Geurts J, Pippenger BE, Schaefer DJ, Martin I, Barbero A, Pelttari K (2017) Ascorbic acid attenuates senescence of human osteoarthritic osteoblasts. Int J Mol Sci 18:2517. https://doi.org/10.3390/ijms18122517

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Yang M, Teng S, Ma C, Yu Y, Wang P, Yi C (2018) Ascorbic acid inhibits senescence in mesenchymal stem cells through ROS and AKT/mTOR signaling. Cytotechnology 70:1301–1313. https://doi.org/10.1007/s10616-018-0220-x

    Article  PubMed  PubMed Central  Google Scholar 

  42. Yang Y, Wang T, Zhang S, Jia S, Chen H, Duan Y, Wang S, Chen G, Tian W (2021) Vitamin C alleviates the senescence of periodontal ligament stem cells through inhibition of Notch3 during long-term culture. J Cell Physiol 236:1237–1251. https://doi.org/10.1002/jcp.29930

    Article  PubMed  CAS  Google Scholar 

  43. Azman KF, Zakaria R (2019) D-Galactose-induced accelerated aging model: an overview. Biogerontology 20:763–782. https://doi.org/10.1007/s10522-019-09837-y

    Article  PubMed  Google Scholar 

  44. Zhang D, Yan B, Yu S, Zhang C, Wang B, Wang Y, Wang J, Yuan Z, Zhang L, Pan J (2015) Coenzyme Q10 inhibits the aging of mesenchymal stem cells induced by D-galactose through Akt/mTOR signaling. Oxid Med Cell Longev 2015. https://doi.org/10.1155/2015/867293

  45. Tominaga T, Shimada R, Okada Y, Kawamata T, Kibayashi K (2019) Senescence-associated-β-galactosidase staining following traumatic brain injury in the mouse cerebrum. PLoS One 14:e0213673. https://doi.org/10.1371/journal.pone.0213673

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Grada A, Otero-Vinas M, Prieto-Castrillo F, Obagi Z, Falanga V (2017) Research techniques made simple: analysis of collective cell migration using the wound healing assay. J Invest Dermatol 137:e11–e16. https://doi.org/10.1016/j.jid.2016.11.020

    Article  PubMed  CAS  Google Scholar 

  47. Petrino JA, Boda KK, Shambarger S, Bowles WR, McClanahan SB (2010) Challenges in regenerative endodontics: a case series. J Endod 36:536–541. https://doi.org/10.1016/j.joen.2009.10.006

    Article  PubMed  Google Scholar 

  48. Lenzi R, Trope M (2012) Revitalization procedures in two traumatized incisors with different biological outcomes. J Endod 38:411–414. https://doi.org/10.1016/j.joen.2011.12.003

    Article  PubMed  Google Scholar 

  49. Liu C, Xiong H, Chen K, Huang Y, Huang Y, Yin X (2016) Long-term exposure to pro-inflammatory cytokines inhibits the osteogenic/dentinogenic differentiation of stem cells from the apical papilla. Int Endod J 49:950–959. https://doi.org/10.1111/iej.12551

    Article  PubMed  CAS  Google Scholar 

  50. Yoo YJ, Oh JH, Lee WC, Woo KM (2016) Regenerative characteristics of apical papilla–derived cells from immature teeth with pulpal and periapical pathosis. J Endod 42:1626–1632. https://doi.org/10.1016/j.joen.2016.08.004

    Article  PubMed  Google Scholar 

  51. Herranz N, Gil J (2018) Mechanisms and functions of cellular senescence. J Clin Investig 128:1238–1246. https://doi.org/10.1172/JCI95148

    Article  PubMed  PubMed Central  Google Scholar 

  52. Franceschi C, Campisi J (2014) Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J Gerontol A Biol Sci Med Sci 69:S4–S9. https://doi.org/10.1093/gerona/glu057

    Article  PubMed  Google Scholar 

  53. Sanada F, Taniyama Y, Muratsu J, Otsu R, Shimizu H, Rakugi H, Morishita R (2018) Source of chronic inflammation in aging. Front Cardiovasc Med 5:12. https://doi.org/10.3389/fcvm.2018.00012

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Mytych J, Romerowicz-Misielak M, Koziorowski M (2017) Long-term culture with lipopolysaccharide induces dose-dependent cytostatic and cytotoxic effects in THP-1 monocytes. Toxicol in Vitro 42:1–9. https://doi.org/10.1016/j.tiv.2017.03.009

    Article  PubMed  CAS  Google Scholar 

  55. Feng G, Zheng K, Cao T, Zhang J, Lian M, Huang D, Wei C, Gu Z, Feng X (2018) Repeated stimulation by LPS promotes the senescence of DPSCs via TLR4/MyD88-NF-κB-p53/p21 signaling. Cytotechnology 70:1023–1035. https://doi.org/10.1007/s10616-017-0180-6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Mehrazarin S, Oh JE, Chung CL, Chen W, Kim RH, Shi S, Park N-H, Kang MK (2011) Impaired odontogenic differentiation of senescent dental mesenchymal stem cells is associated with loss of Bmi-1 expression. J Endod 37:662–666. https://doi.org/10.1016/j.joen.2011.02.009

    Article  PubMed  PubMed Central  Google Scholar 

  57. Zhang J, An Y, Gao L-N, Zhang Y-J, Jin Y, Chen F-M (2012) The effect of aging on the pluripotential capacity and regenerative potential of human periodontal ligament stem cells. Biomaterials 33:6974–6986. https://doi.org/10.1016/j.biomaterials.2012.06.032

    Article  PubMed  CAS  Google Scholar 

  58. Feng X, Xing J, Feng G, Huang D, Lu X, Liu S, Tan W, Li L, Gu Z (2014) p16INK4A mediates age-related changes in mesenchymal stem cells derived from human dental pulp through the DNA damage and stress response. Mech Ageing Dev 141:46–55. https://doi.org/10.1016/j.mad.2014.09.004

    Article  PubMed  CAS  Google Scholar 

  59. Wu RX, Bi CS, Yu Y, Zhang LL, Chen FM (2015) Age-related decline in the matrix contents and functional properties of human periodontal ligament stem cell sheets. Acta Biomater 22:70–82. https://doi.org/10.1016/j.actbio.2015.04.024

    Article  PubMed  CAS  Google Scholar 

  60. Yi Q, Liu O, Yan F, Lin X, Diao S, Wang L, Jin L, Wang S, Lu Y, Fan Z (2017) Analysis of senescence-related differentiation potentials and gene expression profiles in human dental pulp stem cells. Cells Tissues Organs 203:1–11. https://doi.org/10.1159/000448026

    Article  PubMed  CAS  Google Scholar 

  61. Iezzi I, Cerqueni G, Licini C, Lucarini G, Mattioli Belmonte M (2019) Dental pulp stem cells senescence and regenerative potential relationship. J Cell Physiol 234:7186–7197. https://doi.org/10.1002/jcp.27472

    Article  PubMed  CAS  Google Scholar 

  62. Aguilar P, Mahanonda R, Sa-Ard-Iam N, Lertchirakarn V (2021) Effects of lipopolysaccharide on proliferation, migration and osteogenic differentiation of apical papilla cells from early and late stage of root development. Aust Endod J 47:281–289. https://doi.org/10.1111/aej.12475

    Article  PubMed  Google Scholar 

  63. Tanaka Y, Sonoda S, Yamaza H, Murata S, Nishida K, Hama S, Kyumoto-Nakamura Y, Uehara N, Nonaka K, Kukita T (2018) Suppression of AKT-mTOR signal pathway enhances osteogenic/dentinogenic capacity of stem cells from apical papilla. Stem Cell Res Ther 9:1–12. https://doi.org/10.1186/s13287-018-1077-9

    Article  CAS  Google Scholar 

  64. Tanaka Y, Sonoda S, Yamaza H, Murata S, Nishida K, Kyumoto-Nakamura Y, Uehara N, Nonaka K, Kukita T, Yamaza T (2019) Acetylsalicylic acid treatment and suppressive regulation of AKT accelerate odontogenic differentiation of stem cells from the apical papilla. J Endod 45(591-598):e6. https://doi.org/10.1016/j.joen.2019.01.016

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank Adjunct Professor Richard L. Wilson, Faculty Consultant at the Faculty of Dentistry, Chiang Mai University, Chiang Mai, Thailand, for his assistance in the English language editing of the manuscript. The research grant for this project was partially supported by the CMU Mid-career Research Fellowship program and research grants from the Faculty of Dentistry, Chiang Mai University, Chiang Mai, Thailand.

Funding

The research grant for this project was partially supported by the CMU Mid-career Research Fellowship program and research grants from the Faculty of Dentistry, Chiang Mai University, Chiang Mai, Thailand.

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Authors and Affiliations

  1. Department of Restorative Dentistry and Periodontology, Faculty of Dentistry, Chiang Mai University, Chiang Mai, TH, Thailand

    Chananporn Teawcharoensopa & Tanida Srisuwan

  2. Sikhoraphum Hospital Dental Department, Surin, TH, Thailand

    Chananporn Teawcharoensopa

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Contributions

Chananporn Teawcharoensopa: data curation, formal analysis, investigation, software, visualization, writing – original draft preparation. Tanida Srisuwan: conceptualization, funding acquisition, methodology, project administration, resource, supervision, validation, writing – review and editing

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Correspondence to Tanida Srisuwan.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the Human Experimental Committee, Faculty of Dentistry, Chiang Mai University (No.5/2021), and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.

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Teawcharoensopa, C., Srisuwan, T. The potential use of ascorbic acid to recover the cellular senescence of lipopolysaccharide-induced human apical papilla cells: an in vitro study. Clin Oral Invest 28, 49 (2024). https://doi.org/10.1007/s00784-023-05455-8

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