Top

Published in:

01-12-2021 | Laser | Original Article

Photobiomodulation therapy does not depend on the differentiation of dental pulp cells to enhance functional activity associated with angiogenesis and mineralization

Authors: Daniela Thomazatti Chimello-Sousa, Geovane Praxedes Lavez, Roger Rodrigo Fernandes, Milla Sprone Tavares, Adalberto Luiz Rosa, Selma Siessere, Simone Cecílio Hallak Regalo, Karina Fittipaldi Bombonato-Prado

Published in: Lasers in Medical Science | Issue 9/2021

Abstract

The purpose of this study is to analyze the influence of InGaAlP diode laser (660 nm) with or without an odontogenic medium (OM) in the functional activity of OD-21 cells. Undifferentiated OD-21 pulp cells were cultivated with or without OM and divided into four groups (n = 5): nonirradiated control (C −), nonirradiated + OM (C +), irradiated (L −), and irradiated + OM (L +). Laser application was performed in two sessions of a 24-h interval with an irradiance of 11.3 mW/cm2, energy density of 1 J/cm², and total cumulative energy/well of 4.6 J. Cell proliferation, VEGF-164 expression, mineralization, and expression of Alp, Runx2, and Dmp1 genes, as well as immunolocalization of RUNX2 and MEPE proteins, were evaluated. Data were analyzed by statistical tests (α = 0.05). All studied groups showed a similar increase in cell proliferation with or without OM. After 7 and 10 days, a significatively higher concentration of VEGF-164 in L − group when compared to C − group was observed. A significant increase in mineralized nodules in the L + was noted when compared to C + in the same conditions. Photobiomodulation upregulated significantly Runx2 and Dmp1 expression after 10 days in L − and after 7 days in L + , with downregulation of Dmp1 after 10 days in L + group. Immunolocalization of RUNX2 and MEPE was expressive after 7 days of culture in the cytoplasm adjacent to the nucleus with a decrease after 10 days, regardless of the presence of OM. Photobiomodulation enhances metabolism associated with angiogenesis, gene expression, and mineralization regardless of the odontogenic medium in OD-21 cells.

Sun ZL, Fang DN, Wu XY, Ritchie HH, Bègue-Kirn C, Wataha JC, Hanks CT, Butler WT (1998) Expression of dentin sialoprotein (DSP) and other molecular determinants by a new cell line from dental papillae, MDPC-23. Connect Tissue Res 37:251–261. https://doi.org/10.3109/03008209809002443CrossRefPubMed

Balic A (2018) Biology explaining tooth repair and regeneration: a mini-review. Gerontology 64:382–388. https://doi.org/10.1159/000486592CrossRefPubMed

Yuan Y, Chai Y (2019) Regulatory mechanisms of jaw bone and tooth development. Curr Top Dev Biol 133:91–118. https://doi.org/10.1016/bs.ctdb.2018.12.013CrossRefPubMedPubMedCentral

Thesleff I (2018) From understanding tooth development to bioengineering of teeth. Eur J Oral Sci 126:67–71. https://doi.org/10.1111/eos.12421CrossRefPubMed

Baranova J, Büchner D, Götz W, Schulze M, Tobiasch E (2020) Tooth formation: are the hardest tissues of human body hard to regenerate? Int J Mol Sci 21:4031. https://doi.org/10.3390/ijms21114031CrossRefPubMedCentral

Salehi S, Cooper P, Smith A, Ferracane J (2016) Dentin matrix components extracted with phosphoric acid enhance cell proliferation and mineralization. Dent Mater 32:334–342. https://doi.org/10.1016/j.dental.2015.11.004CrossRefPubMed

Babaki D, Yaghoubi S, Matin MM (2020) The effects of mineral trioxide aggregate on osteo/odontogenic potential of mesenchymal stem cells: a comprehensive and systematic literature review. Biomaterial Investigations in Dentistry 7:175–185. https://doi.org/10.1080/26415275.2020.1848432CrossRefPubMedPubMedCentral

Goldberg M, Lasfargues JJ (1995) Pulpo-dentinal complex revisited Journal of Dentistry 23:15–20. https://doi.org/10.1016/0300-5712(95)90655-2CrossRefPubMed

Butler WT (1992) Dentin extracellular matrix and dentinogenesis. Oper Dent Suppl 5:18–23

10.

Aydin S, Şahin F (2019) Stem cells derived from dental tissues. Adv Exp Med Biol 1144:123–132. https://doi.org/10.1007/5584_2018_333CrossRefPubMed

11.

Tziafas D (1995) Basic mechanisms of cytodifferentiation and dentinogenesis during dental pulp repair. Int J Dev Biol 39:281–290PubMed

12.

Pashley DH (1996) Dynamics of the pulpo-dentin complex. Crit Rev Oral Biol Med 7:104–133. https://doi.org/10.1177/10454411960070020101CrossRefPubMed

13.

Zanini M, Sautier JM, Berdal A, Simon S (2012) Biodentine induces immortalized murine pulp cell differentiation into odontoblast-like cells and stimulates biomineralization. Journal of Endodontics 38:1220–1226. https://doi.org/10.1016/j.joen.2012.04.018CrossRefPubMed

14.

Ballini A, Mastrangelo F, Gastaldi G, Tettamanti L, Bukvic N, Cantore S et al (2015) Osteogenic differentiation and gene expression of dental pulp stem cells under low-level laser irradiation: a good promise for tissue engineering. J Biol Regul Homeost Agents 29:813–822PubMed

15.

Ginani F, Soares DM, de Oliveira Rocha HA, de Souza LB, Barboza CAG (2018) Low-level laser irradiation induces in vitro proliferation of stem cells from human exfoliated deciduous teeth. Lasers in Medical Scienc 33:95–102. https://doi.org/10.1007/s10103-017-2355-yCrossRef

16.

Chimello-Sousa DT, Bombonato-Prado KF, Rosa AL, Fernandes RR et al (2021) In vitro effect of low-level laser therapy on undifferentiated mouse pulp cells. Journal of Health Sciences 23: 02–06. https://doi.org/10.17921/2447-8938.2021v23n1p02-06

17.

Vitor LLR, Bergamo MTOP, Lourenço-Neto N, Sakai VT, Oliveira RC, Cruvinel T, Rios D, Garlet GP, Santos CF, Machado MAAM, Oliveira TM (2020) Photobiomodulation effect on angiogenic proteins produced and released by dental pulp cells. Clin Oral Invest 24:4343–4354. https://doi.org/10.1007/s00784-020-03298-1CrossRef

18.

Ferreira LS, Diniz IMA, Maranduba CMS, Miyagi SPH et al (2019) Short-term evaluation of photobiomodulation therapy on the proliferation and undifferentiated status of dental pulp stem cells. Lasers Med Sci 34:659–666. https://doi.org/10.1007/s10103-018-2637-zCrossRefPubMed

19.

Kulkarni S, Meer M, George R (2020) The effect of photobiomodulation on human dental pulp-derived stem cells: systematic review. Lasers Med Sci 35:1889–1897. https://doi.org/10.1007/s10103-020-03071-6CrossRefPubMed

20.

Gregory CA, Gunn WG, Peister A, Prockop DJ (2004) An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Anal Biochem 329:77–84. https://doi.org/10.1016/j.ab.2004.02.002CrossRefPubMed

21.

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262CrossRef

22.

Semeghini MS, Fernandes RR, Chimello DT, Oliveira FS, Bombonato-Prado KF (2012) In vitro evaluation of the odontogenic potential of mouse undifferentiated pulp cells. Braz Dent J 23:328–336. https://doi.org/10.1590/S0103-64402012000400004CrossRefPubMed

23.

Karu T (1989) Photobiology of low-power laser effects. Health Phys 56:691–704. https://doi.org/10.1097/00004032-198905000-00015CrossRefPubMed

24.

Silveira PC, Streck EL, Pinho RA (2007) Evaluation of mitochondrial respiratory chain activity in wound healing by low-level laser therapy. J Photochem Photobiol B 86:279–282. https://doi.org/10.1016/j.jphotobiol.2006.10.002CrossRefPubMed

25.

Arany PR, Cho A, Hunt TD, Sidhu G, Shin K et al (2014) Photoactivation of endogenous latent transforming growth factor-β1 directs dental stem cell differentiation for regeneration. Science Translational Medicine 6: 238ra69. https://doi.org/10.1126/scitranslmed.3008234

26.

Rosa AL, Beloti MM (2003) TAK-778 enhances osteoblast differentiation of human bone marrow cells. J Cell Biochem 89:1148–1153. https://doi.org/10.1002/jcb.10582CrossRefPubMed

27.

Nakasone N, Yoshie H, Ohshima H (2006) The relationship between the termination of cell proliferation and expression of heat-shock protein-25 in the rat developing tooth germ. Eur J Oral Sci 114:302–309. https://doi.org/10.1111/j.1600-0722.2006.00362.xCrossRefPubMed

28.

Bellesini LS, Beloti MM, Crippa GE, Bombonato-Prado KF et al (2009) The effect of TAK-778 on gene expression of osteoblastic cells is mediated through estrogen receptor. Experimental Biology and Medicine (Maywood) 234:190–199. https://doi.org/10.3181/0808-rm-246CrossRef

29.

Eduardo FP, Bueno DF, Freitas PM, Marques MM, Passos-Bueno MR, Eduardo CP, Zatz M (2008) Stem cell proliferation under low intensity laser irradiation: a preliminary study. Lasers Surg Med 40:433–438. https://doi.org/10.1002/lsm.20646CrossRef

30.

Horvát-Karajz K, Balogh Z, Kovács V, Drrernat AH, Sréter L, Uher F (2009) In vitro effect of carboplatin, cytarabine, paclitaxel, vincristine, and low-power laser irradiation on murine mesenchymal stem cells. Lasers Surg Med 41(6):463–469. https://doi.org/10.1002/lsm.20791CrossRefPubMed

31.

Mvula B, Mathope T, Moore T, Abrahamse H (2008) The effect of low level laser irradiation on adult human adipose derived stem cells. Lasers Med Sci 23:277–282. https://doi.org/10.1007/s10103-007-0479-1CrossRefPubMed

32.

Pires Oliveira DA, de Oliveira RF, Zangaro RA, Soares CP (2008) Evaluation of low-level laser therapy of osteoblastic cells. Photomed Laser Surg 26:401–404. https://doi.org/10.1089/pho.2007.2101CrossRefPubMed

33.

Saygun I, Karacay S, Serdar M, Ural AU, Sencimen M, Kurtis B (2008) Effects of laser irradiation on the release of basic fibroblast growth factor (bFGF), insulin like growth factor-1 (IGF-1), and receptor of IGF-1 (IGFBP3) from gingival fibroblasts. Lasers Med Sci 23:211–215. https://doi.org/10.1007/s10103-007-0477-3CrossRefPubMed

34.

Franceschi RT, Iyer BS, Cui Y (1994) Effects of ascorbic acid on collagen matrix formation and osteoblast differentiation in murine MC3T3-E1 cells. Journal of Bone and Mineral Researc 9:843–854. https://doi.org/10.1002/jbmr.5650090610CrossRef

35.

Tenenbaum HC (1981) Role of organic phosphate in mineralization of bone in vitro. Journal of Dental Researc, 60 Spec No C: 1586–1589. https://doi.org/10.1177/0022034581060003s0801

36.

Schwartz-Filho HO, Reimer AC, Marcantonio C, Marcantonio E Jr, Marcantonio RA (2011) Effects of low-level laser therapy (685 nm) at different doses in osteogenic cell cultures. Lasers Med Sci 26:539–543. https://doi.org/10.1007/s10103-011-0902-5CrossRefPubMed

37.

Pereira LB, Chimello DT, Ferreira MR, Bachmann L, Rosa AL, Bombonato-Prado KF (2012) Low-level laser therapy influences mouse odontoblast-like cell response in vitro. Photomed Laser Surg 30:206–213. https://doi.org/10.1089/pho.2011.3087CrossRefPubMed

38.

Ferrara N, Henzel WJ (1989) Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun 161:851–858. https://doi.org/10.1016/0006-291x(89)92678-8CrossRefPubMed

39.

Phillips HS, Hains J, Leung DW, Ferrara N (1990) Vascular endothelial growth factor is expressed in rat corpus luteum. Endocrinology 127:965–967. https://doi.org/10.1210/endo-127-2-965CrossRefPubMed

40.

Ferrara N (2009) VEGF-A: a critical regulator of blood vessel growth. Eur Cytokine Netw 20:158–163. https://doi.org/10.1684/ecn.2009.0170CrossRefPubMed

41.

Luo J, Xiong Y, Han X, Lu Y (2011) VEGF non-angiogenic functions in adult organ homeostasis: therapeutic implications. Journal of Molecular Medicine (Berlin) 89:635–645. https://doi.org/10.1007/s00109-011-0739-1CrossRef

42.

Tran-Hung L, Laurent P, Camps J, About I (2008) Quantification of angiogenic growth factors released by human dental cells after injury. Arch Oral Biol 53:9–13. https://doi.org/10.1016/j.archoralbio.2007.07.001CrossRefPubMed

43.

Roberts-Clark DJ, Smith AJ (2000) Angiogenic growth factors in human dentine matrix. Arch Oral Biol 45:1013–1016. https://doi.org/10.1016/s0003-9969(00)00075-3CrossRefPubMed

44.

Artese L, Rubini C, Ferrero G, Fioroni M, Santinelli A, Piattelli A (2002) Vascular endothelial growth factor (VEGF) expression in healthy and inflamed human dental pulps. Journal of Endodontics 28:20–23. https://doi.org/10.1097/00004770-200201000-00005CrossRefPubMed

45.

Botero TM, Mantellini MG, Song W, Hanks CT, Nör JE (2003) Effect of lipopolysaccharides on vascular endothelial growth factor expression in mouse pulp cells and macrophages. Eur J Oral Sci 111:228–234. https://doi.org/10.1034/j.1600-0722.2003.00041.xCrossRefPubMed

46.

Scheven BA, Man J, Millard JL, Cooper PR et al (2009) VEGF and odontoblast-like cells: stimulation by low frequency ultrasound. Arch Oral Biol 54:185–191. https://doi.org/10.1016/j.archoralbio.2008.09.008CrossRefPubMed

47.

Hou JF, Zhang H, Yuan X, Li J, Wei YJ, Hu SS (2008) In vitro effects of low-level laser irradiation for bone marrow mesenchymal stem cells: proliferation, growth factors secretion and myogenic differentiation. Lasers Surg Med 40:726–733. https://doi.org/10.1002/lsm.20709CrossRefPubMed

48.

Wang Y, Huang YY, Wang Y, Lyu P, Hamblin MR (2016) Photobiomodulation (blue and green light) encourages osteoblastic-differentiation of human adipose-derived stem cells: role of intracellular calcium and light-gated ion channels Scientific Reports 6: 33719. https://doi.org/10.1038/srep33719

49.

Gullard A, Gluhak-Heinrich J, Papagerakis S, Sohn P, Unterbrink A, Chen S, MacDougall M (2016) MEPE localization in the craniofacial complex and function in tooth dentin formation. J Histochem Cytochem 64:224–236. https://doi.org/10.1369/0022155416635569CrossRefPubMedPubMedCentral

50.

Wei X, Liu L, Zhou X, Zhang F, Ling J (2012) The effect of matrix extracellular phosphoglycoprotein and its downstream osteogenesis-related gene expression on the proliferation and differentiation of human dental pulp cells. Journal of Endodontics 38:330–338. https://doi.org/10.1016/j.joen.2011.10.015CrossRefPubMed

Title: Photobiomodulation therapy does not depend on the differentiation of dental pulp cells to enhance functional activity associated with angiogenesis and mineralization
Authors: Daniela Thomazatti Chimello-Sousa
Geovane Praxedes Lavez
Roger Rodrigo Fernandes
Milla Sprone Tavares
Adalberto Luiz Rosa
Selma Siessere
Simone Cecílio Hallak Regalo
Karina Fittipaldi Bombonato-Prado
Publication date: 01-12-2021
Publisher: Springer London
Keyword: Laser
Published in: Lasers in Medical Science / Issue 9/2021
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI: https://doi.org/10.1007/s10103-021-03395-x

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Photobiomodulation therapy does not depend on the differentiation of dental pulp cells to enhance functional activity associated with angiogenesis and mineralization

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 9/2021

Burnback: the role of pulse duration and energy on fiber-tip degradation during high-power laser lithotripsy

Comparison of carboxy therapy and fractional Q-switched ND:YAG laser on periorbital dark circles treatment: a clinical trial

Safety and efficacy of thulium laser resection of bladder tumors versus transurethral resection of bladder tumors: a systematic review and meta-analysis

Anal dysplasia screening by Raman-enhanced spectroscopy can inform clinical diagnosis of cervical neoplasia

Combination photobiomodulation/N-acetyl-L-cysteine treatment appears to mitigate hair cell loss associated with noise-induced hearing loss in rats

Effects of laser therapy on periorbital hyperpigmentation: a systematic review on current studies