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Published in: Lasers in Medical Science 4/2014

01-07-2014 | Original Article

Low-level laser therapy promotes proliferation and invasion of oral squamous cell carcinoma cells

Authors: Águida Cristina Gomes Henriques, Fernanda Ginani, Ruth Medeiros Oliveira, Tatjana Souza Lima Keesen, Carlos Augusto Galvão Barboza, Hugo Alexandre Oliveira Rocha, Jurema Freire Lisboa de Castro, Ricardo Della Coletta, Roseana de Almeida Freitas

Published in: Lasers in Medical Science | Issue 4/2014

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Abstract

Low-level laser therapy (LLLT) has been shown to be effective in promoting cell proliferation. There is speculation that the biostimulatory effect of LLLT causes undesirable enhancement of tumor growth in neoplastic diseases since malignant cells are more susceptible to proliferative stimuli. This study evaluated the effects of LLLT on proliferation, invasion, and expression of cyclin D1, E-cadherin, β-catenin, and MMP-9 in a tongue squamous carcinoma cell line (SCC25). Cells were irradiated with a diode laser (660 nm) using two energy densities (0.5 and 1.0 J/cm2). The proliferative potential was assessed by cell growth curves and cell cycle analysis, whereas the invasion of cells was evaluated using a Matrigel cell invasion assay. Expression of cyclin D1, E-cadherin, β-catenin, and MMP-9 was analyzed by immunofluorescence and flow cytometry and associated with the biological activities studied. LLLT induced significantly the proliferation of SCC25 cells at 1.0 J/cm2, which was accomplished by an increase in the expression of cyclin D1 and nuclear β-catenin. At 1.0 J/cm2, LLLT significantly reduced E-cadherin and induced MMP-9 expression, promoting SCC25 invasion. The results of this study demonstrated that LLLT exerts a stimulatory effect on proliferation and invasion of SCC25 cells, which was associated with alterations on expression of proteins studied.
Literature
1.
go back to reference Karu T (1999) Primary and secondary mechanisms of action of visible to near-IR radiation on cells. J Photochem Photobiol B 49:17–24CrossRef Karu T (1999) Primary and secondary mechanisms of action of visible to near-IR radiation on cells. J Photochem Photobiol B 49:17–24CrossRef
2.
go back to reference Gao X, Xing D (2009) Molecular mechanisms of cell proliferation induced by low power laser irradiation. J Biomed Sci 9:1–16 Gao X, Xing D (2009) Molecular mechanisms of cell proliferation induced by low power laser irradiation. J Biomed Sci 9:1–16
3.
go back to reference Eduardo FP, Bueno DF, de Freitas PM, Marques MM, Passos-Bueno MR, Eduardo Cde P, Zatz M (2008) Stem cell proliferation under low intensity laser irradiation: a preliminary study. Lasers Surg Med 40:433–438CrossRef Eduardo FP, Bueno DF, de Freitas PM, Marques MM, Passos-Bueno MR, Eduardo Cde P, Zatz M (2008) Stem cell proliferation under low intensity laser irradiation: a preliminary study. Lasers Surg Med 40:433–438CrossRef
4.
go back to reference Yazdani SO, Golestaneh AF, Shafiee A, Hafizi M, Omrani HA, Soleimani M (2012) Effects of low level laser therapy on proliferation and neurotrophic factor gene expression of human Schwann cells in vitro. J Photochem Photobiol B 107:9–13PubMedCrossRef Yazdani SO, Golestaneh AF, Shafiee A, Hafizi M, Omrani HA, Soleimani M (2012) Effects of low level laser therapy on proliferation and neurotrophic factor gene expression of human Schwann cells in vitro. J Photochem Photobiol B 107:9–13PubMedCrossRef
5.
go back to reference Castro JL, Pinheiro AL, Werneck CE, Soares CP (2005) The effect of laser therapy on the proliferation of oral KB carcinoma cells: an in vitro study. Photomed Laser Surg 23:586–589PubMedCrossRef Castro JL, Pinheiro AL, Werneck CE, Soares CP (2005) The effect of laser therapy on the proliferation of oral KB carcinoma cells: an in vitro study. Photomed Laser Surg 23:586–589PubMedCrossRef
6.
go back to reference Alghamdi KM, Kumar A, Moussa NA (2012) Low-level laser therapy: a useful technique for enhancing the proliferation of various cultured cells. Lasers Med Sci 27:237–249PubMedCrossRef Alghamdi KM, Kumar A, Moussa NA (2012) Low-level laser therapy: a useful technique for enhancing the proliferation of various cultured cells. Lasers Med Sci 27:237–249PubMedCrossRef
7.
go back to reference Renno AC, McDonnell PA, Parizotto NA, Laakso EL (2007) The effects of laser irradiation on osteoblast and osteosarcoma cell proliferation and differentiation in vitro. Photomed Laser Surg 25:275–280PubMedCrossRef Renno AC, McDonnell PA, Parizotto NA, Laakso EL (2007) The effects of laser irradiation on osteoblast and osteosarcoma cell proliferation and differentiation in vitro. Photomed Laser Surg 25:275–280PubMedCrossRef
8.
go back to reference Frigo L, Luppi JS, Favero GM, Maria DA, Penna SC, Bjordal JM, Bensadoun RJ, Lopes-Martins RA (2009) The effect of low-level laser irradiation (In-Ga-Al-AsP—660 nm) on melanoma in vitro and in vivo. BMC Cancer 9:404–411PubMedCentralPubMedCrossRef Frigo L, Luppi JS, Favero GM, Maria DA, Penna SC, Bjordal JM, Bensadoun RJ, Lopes-Martins RA (2009) The effect of low-level laser irradiation (In-Ga-Al-AsP—660 nm) on melanoma in vitro and in vivo. BMC Cancer 9:404–411PubMedCentralPubMedCrossRef
9.
go back to reference Pinheiro AL, Carneiro NS, Vieira AL, Brugnera A Jr, Zanin FA, Barros RA, Silva OS (2002) Effects of low-level laser therapy on malignant cells: in vitro study. J Clin Laser Med Surg 20:23–26PubMedCrossRef Pinheiro AL, Carneiro NS, Vieira AL, Brugnera A Jr, Zanin FA, Barros RA, Silva OS (2002) Effects of low-level laser therapy on malignant cells: in vitro study. J Clin Laser Med Surg 20:23–26PubMedCrossRef
10.
go back to reference Schartinger VH, Galvan O, Riechelmann H, Dudás J (2001) Differential responses of fibroblasts, non-neoplastic epithelial cells, and oral carcinoma cells to low-level laser therapy. Support Care Cancer 20:523–529CrossRef Schartinger VH, Galvan O, Riechelmann H, Dudás J (2001) Differential responses of fibroblasts, non-neoplastic epithelial cells, and oral carcinoma cells to low-level laser therapy. Support Care Cancer 20:523–529CrossRef
11.
go back to reference Bernard S, Herzel H (2006) Why do cells cycle with a 24 hour period? Genome Inform 17:72–79PubMed Bernard S, Herzel H (2006) Why do cells cycle with a 24 hour period? Genome Inform 17:72–79PubMed
12.
go back to reference Powell K, Low P, McDonnell PA, Laakso EL, Ralph SJ (2010) The effect of laser irradiation on proliferation of human breast carcinoma, melanoma, and immortalized mammary epithelial cells. Photomed Laser Surg 28:115–123PubMedCrossRef Powell K, Low P, McDonnell PA, Laakso EL, Ralph SJ (2010) The effect of laser irradiation on proliferation of human breast carcinoma, melanoma, and immortalized mammary epithelial cells. Photomed Laser Surg 28:115–123PubMedCrossRef
13.
go back to reference Liu YH, Cheng CC, Ho CC, Pei RJ, Lee KY, Yeh KT, Chan Y, Lai YS (2004) Effects of diode 808 nm GaAlAs low-power laser irradiation on inhibition of the proliferation of human hepatoma cells in vitro and their possible mechanism. Res Commun Mol Pathol Pharmacol 115:185–201PubMed Liu YH, Cheng CC, Ho CC, Pei RJ, Lee KY, Yeh KT, Chan Y, Lai YS (2004) Effects of diode 808 nm GaAlAs low-power laser irradiation on inhibition of the proliferation of human hepatoma cells in vitro and their possible mechanism. Res Commun Mol Pathol Pharmacol 115:185–201PubMed
14.
go back to reference Murayama H, Sadakane K, Yamanoha B, Kogure S (2012) Low-power 808-nm laser irradiation inhibits cell proliferation of a human-derived glioblastoma cell line in vitro. Lasers Med Sci 27:87–93PubMedCrossRef Murayama H, Sadakane K, Yamanoha B, Kogure S (2012) Low-power 808-nm laser irradiation inhibits cell proliferation of a human-derived glioblastoma cell line in vitro. Lasers Med Sci 27:87–93PubMedCrossRef
16.
go back to reference Wu S, Xing D, Gao X, Chen WR (2009) High fluence low-power laser irradiation induces mitochondrial permeability transition mediated by reactive oxygen species. J Cell Physiol 218:603–611PubMedCrossRef Wu S, Xing D, Gao X, Chen WR (2009) High fluence low-power laser irradiation induces mitochondrial permeability transition mediated by reactive oxygen species. J Cell Physiol 218:603–611PubMedCrossRef
17.
go back to reference Huang L, Wu S, Xing D (2011) High fluence low-power laser irradiation induces apoptosis via inactivation of Akt/GSK3b signaling pathway. J Cell Physiol 226:588–601PubMedCrossRef Huang L, Wu S, Xing D (2011) High fluence low-power laser irradiation induces apoptosis via inactivation of Akt/GSK3b signaling pathway. J Cell Physiol 226:588–601PubMedCrossRef
18.
go back to reference Donnellen R, Chetty R (1998) Cyclin D1 and human neoplasia. J Clin Pathol 51:1–7CrossRef Donnellen R, Chetty R (1998) Cyclin D1 and human neoplasia. J Clin Pathol 51:1–7CrossRef
19.
go back to reference Shefer G, Barash I, Oron U, Halevy O (2003) Low-energy laser irradiation enhances de novo protein synthesis via its effects on translation-regulatory proteins in skeletal muscle myoblasts. Biochim Biophys Acta 1593:131–139PubMedCrossRef Shefer G, Barash I, Oron U, Halevy O (2003) Low-energy laser irradiation enhances de novo protein synthesis via its effects on translation-regulatory proteins in skeletal muscle myoblasts. Biochim Biophys Acta 1593:131–139PubMedCrossRef
20.
go back to reference Taniguchi D, Dai P, Hojo T, Yamaoka Y, Kubo T, Takamatsu T (2009) Low-energy laser irradiation promotes synovial fibroblast proliferation by modulating p15 subcellular localization. Lasers Surg Med 41:232–239PubMedCrossRef Taniguchi D, Dai P, Hojo T, Yamaoka Y, Kubo T, Takamatsu T (2009) Low-energy laser irradiation promotes synovial fibroblast proliferation by modulating p15 subcellular localization. Lasers Surg Med 41:232–239PubMedCrossRef
21.
go back to reference Wu YH, Wang J, Gong DX, Gu HY, Hu SS, Zhang H (2012) Effects of low-level laser irradiation on mesenchymal stem cell proliferation: a microarray analysis. Lasers Med Sci 27:509–519PubMedCrossRef Wu YH, Wang J, Gong DX, Gu HY, Hu SS, Zhang H (2012) Effects of low-level laser irradiation on mesenchymal stem cell proliferation: a microarray analysis. Lasers Med Sci 27:509–519PubMedCrossRef
22.
go back to reference Miyata H, Genma T, Ohshima M, Yamaguchi Y, Hayashi M, Takeichi O, Ogiso B, Otsuka K (2006) Mitogen-activated protein kinase/extracellular signal-regulated protein kinase activation of cultured human dental pulp cells by low-power gallium aluminium arsenic laser irradiation. Int Endod J 39:238–244PubMedCrossRef Miyata H, Genma T, Ohshima M, Yamaguchi Y, Hayashi M, Takeichi O, Ogiso B, Otsuka K (2006) Mitogen-activated protein kinase/extracellular signal-regulated protein kinase activation of cultured human dental pulp cells by low-power gallium aluminium arsenic laser irradiation. Int Endod J 39:238–244PubMedCrossRef
23.
go back to reference Gasparoni A, Fonzi L, Schneider GB, Wertz PW, Johnson GK, Squier CA (2004) Comparison of differentiation markers between normal and two squamous cell carcinoma cell lines in culture. Arch Oral Biol 49:653–664PubMedCrossRef Gasparoni A, Fonzi L, Schneider GB, Wertz PW, Johnson GK, Squier CA (2004) Comparison of differentiation markers between normal and two squamous cell carcinoma cell lines in culture. Arch Oral Biol 49:653–664PubMedCrossRef
24.
go back to reference Wang X, Zhang J, Fan M, Zhou Q, Deng H, Aisharif MJ, Chen X (2009) The expression of E-cadherin at the invasive tumor front of oral squamous cell carcinoma: immunohistochemical and RTPCR analysis with clinicopathological correlation. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 107:547–554PubMedCrossRef Wang X, Zhang J, Fan M, Zhou Q, Deng H, Aisharif MJ, Chen X (2009) The expression of E-cadherin at the invasive tumor front of oral squamous cell carcinoma: immunohistochemical and RTPCR analysis with clinicopathological correlation. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 107:547–554PubMedCrossRef
25.
go back to reference Zavadil J, Böttinger EP (2005) TGF-β and epithelial to mesenchymal transitions. Oncogene 24:5764–5774PubMedCrossRef Zavadil J, Böttinger EP (2005) TGF-β and epithelial to mesenchymal transitions. Oncogene 24:5764–5774PubMedCrossRef
26.
go back to reference Lo HW, Hsu SC, Xia W, Cao X, Shih JY, Wei Y, Abbruzzese JL, Hortobagyi GN, Hung MC (2007) Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression. Cancer Res 67:9066–9076PubMedCentralPubMedCrossRef Lo HW, Hsu SC, Xia W, Cao X, Shih JY, Wei Y, Abbruzzese JL, Hortobagyi GN, Hung MC (2007) Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression. Cancer Res 67:9066–9076PubMedCentralPubMedCrossRef
27.
go back to reference Graham TR, Zhau HE, Odero-Marah VA, Osunkoya AO, Kimbro KS, Tighiouart M, Liu T, Simons JW, O'Regan RM (2008) Insulin-like growth factor-I-dependent up-regulation of ZEB1 drives epithelial-to-mesenchymal transition in human prostate cancer cells. Cancer Res 68:2479–2488PubMedCrossRef Graham TR, Zhau HE, Odero-Marah VA, Osunkoya AO, Kimbro KS, Tighiouart M, Liu T, Simons JW, O'Regan RM (2008) Insulin-like growth factor-I-dependent up-regulation of ZEB1 drives epithelial-to-mesenchymal transition in human prostate cancer cells. Cancer Res 68:2479–2488PubMedCrossRef
28.
go back to reference Yadav A, Kumar B, Datta J, Teknos TN, Kumar P (2011) IL-6 promotes head and neck tumor metastasis by inducing epithelial–mesenchymal transition via the JAK-STAT3-SNAIL signaling pathway. Mol Cancer Res 9:1658–1667PubMedCentralPubMedCrossRef Yadav A, Kumar B, Datta J, Teknos TN, Kumar P (2011) IL-6 promotes head and neck tumor metastasis by inducing epithelial–mesenchymal transition via the JAK-STAT3-SNAIL signaling pathway. Mol Cancer Res 9:1658–1667PubMedCentralPubMedCrossRef
29.
go back to reference Yang X, Pursell B, Lu S, Chang TK, Mercurio AM (2009) Regulation of β4-integrin expression by epigenetic modifications in the mammary gland and during the epithelial to mesenchymal transition. J Cell Sci 122:2473–2480PubMedCentralPubMedCrossRef Yang X, Pursell B, Lu S, Chang TK, Mercurio AM (2009) Regulation of β4-integrin expression by epigenetic modifications in the mammary gland and during the epithelial to mesenchymal transition. J Cell Sci 122:2473–2480PubMedCentralPubMedCrossRef
30.
go back to reference Safavi SM, Kazemi B, Esmaeili M, Fallah A, Modarresi A, Mir M (2008) Effects of low-level He–Ne laser irradiation on the gene expression of IL-1β, TNF-α, IFN-γ, TGF-β, bFGF, and PDGF in rat’s gingival. Lasers Med Sci 23:331–335PubMedCrossRef Safavi SM, Kazemi B, Esmaeili M, Fallah A, Modarresi A, Mir M (2008) Effects of low-level He–Ne laser irradiation on the gene expression of IL-1β, TNF-α, IFN-γ, TGF-β, bFGF, and PDGF in rat’s gingival. Lasers Med Sci 23:331–335PubMedCrossRef
31.
go back to reference Saygun I, Nizam N, Ural AU, Serdar MA, Avcu F, Tözüm TF (2012) Low-level laser irradiation affects the release of basic fibroblast growth factor (bFGF), insulin-like growth factor-I (IGF-I), and receptor of IGF-I (IGFBP3) from osteoblasts. Photomed Laser Surg 30:149–154PubMedCrossRef Saygun I, Nizam N, Ural AU, Serdar MA, Avcu F, Tözüm TF (2012) Low-level laser irradiation affects the release of basic fibroblast growth factor (bFGF), insulin-like growth factor-I (IGF-I), and receptor of IGF-I (IGFBP3) from osteoblasts. Photomed Laser Surg 30:149–154PubMedCrossRef
32.
go back to reference Gasparoni A, Chaves A, Fonzi L, Johnson GK, Schneider GB, Squier CA (2002) Subcellular localization of beta-catenin in malignant cell lines and squamous cell carcinomas of the oral cavity. J Oral Pathol Med 31:385–394PubMedCrossRef Gasparoni A, Chaves A, Fonzi L, Johnson GK, Schneider GB, Squier CA (2002) Subcellular localization of beta-catenin in malignant cell lines and squamous cell carcinomas of the oral cavity. J Oral Pathol Med 31:385–394PubMedCrossRef
33.
go back to reference Ishida K, Ito S, Wada N, Deguchi H, Hata T, Hosoda M, Nohno T (2007) Nuclear localization of beta-catenin involved in precancerous change in oral leukoplakia. Mol Cancer 9:6–62 Ishida K, Ito S, Wada N, Deguchi H, Hata T, Hosoda M, Nohno T (2007) Nuclear localization of beta-catenin involved in precancerous change in oral leukoplakia. Mol Cancer 9:6–62
34.
go back to reference Klein EA, Assoian RK (2008) Transcriptional regulation of the cyclin D1 gene at a glance. J Cell Sci 121:3853–3857PubMedCrossRef Klein EA, Assoian RK (2008) Transcriptional regulation of the cyclin D1 gene at a glance. J Cell Sci 121:3853–3857PubMedCrossRef
35.
go back to reference Liu CJ, Chang KW, Lin SC, Cheng HW (2009) Presurgical serum levels of matrix metalloproteinase-9 and vascular endothelial growth factor in oral squamous cell carcinoma. Oral Oncol 45:920–925PubMedCrossRef Liu CJ, Chang KW, Lin SC, Cheng HW (2009) Presurgical serum levels of matrix metalloproteinase-9 and vascular endothelial growth factor in oral squamous cell carcinoma. Oral Oncol 45:920–925PubMedCrossRef
36.
go back to reference Luo J, Lubaroff DM, Hendrix MJ (1999) Suppression of prostate cancer invasive potential and matrix metalloproteinase activity by E-cadherin transfection. Cancer Res 59:3552–3556PubMed Luo J, Lubaroff DM, Hendrix MJ (1999) Suppression of prostate cancer invasive potential and matrix metalloproteinase activity by E-cadherin transfection. Cancer Res 59:3552–3556PubMed
37.
go back to reference Ho YT, Yang JS, Li TC, Lin JJ, Lin JG, Lai KC, Ma CY, Wood WG, Chung JG (2009) Berberine suppresses in vitro migration and invasion of human SCC-4 tongue squamous cancer cells through the inhibitions of FAK, IKK, NF-kappaB, u-PA and MMP-2 and -9. Cancer Lett 279:155–162PubMedCrossRef Ho YT, Yang JS, Li TC, Lin JJ, Lin JG, Lai KC, Ma CY, Wood WG, Chung JG (2009) Berberine suppresses in vitro migration and invasion of human SCC-4 tongue squamous cancer cells through the inhibitions of FAK, IKK, NF-kappaB, u-PA and MMP-2 and -9. Cancer Lett 279:155–162PubMedCrossRef
38.
go back to reference Chen CH, Hung HS, Hsu SH (2008) Low-energy laser irradiation increases endothelial cell proliferation, migration, and eNOS gene expression possibly via PI3K signal pathway. Lasers Surg Med 40:46–54PubMedCrossRef Chen CH, Hung HS, Hsu SH (2008) Low-energy laser irradiation increases endothelial cell proliferation, migration, and eNOS gene expression possibly via PI3K signal pathway. Lasers Surg Med 40:46–54PubMedCrossRef
39.
go back to reference Tsai WC, Hsu CC, Pang JH, Lin MS, Chen YH, Liang FC (2012) Low-level laser irradiation stimulates tenocyte migration with up-regulation of dynamin II expression. PLoS One 7:e38235PubMedCentralPubMedCrossRef Tsai WC, Hsu CC, Pang JH, Lin MS, Chen YH, Liang FC (2012) Low-level laser irradiation stimulates tenocyte migration with up-regulation of dynamin II expression. PLoS One 7:e38235PubMedCentralPubMedCrossRef
40.
Metadata
Title
Low-level laser therapy promotes proliferation and invasion of oral squamous cell carcinoma cells
Authors
Águida Cristina Gomes Henriques
Fernanda Ginani
Ruth Medeiros Oliveira
Tatjana Souza Lima Keesen
Carlos Augusto Galvão Barboza
Hugo Alexandre Oliveira Rocha
Jurema Freire Lisboa de Castro
Ricardo Della Coletta
Roseana de Almeida Freitas
Publication date
01-07-2014
Publisher
Springer London
Published in
Lasers in Medical Science / Issue 4/2014
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-014-1535-2

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