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Erschienen in: Lasers in Medical Science 8/2016

30.06.2016 | Original Article

Effects of combination of melatonin and laser irradiation on ovarian cancer cells and endothelial lineage viability

verfasst von: Maryam Akbarzadeh, Mohammad Nouri, Maryam Vahidi Banekohal, Omid Cheraghi, Habib Tajalli, Aliakbar Movassaghpour, Sina Soltani, Hadi Cheraghi, Navid Feizy, Soheila Montazersaheb, Reza Rahbarghazi, Nasser Samadi

Erschienen in: Lasers in Medical Science | Ausgabe 8/2016

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Abstract

The main goal of anti-cancer therapeutic approaches is to induce apoptosis in tumor masses but not in the normal tissues. Nevertheless, the combination of photodynamic irradiation with complementary oncostatic agents contributes to better therapeutic performance. Here, we applied two different cell lines; SKOV3 ovarian carcinoma cells and HUVECs umbilical cord cells as in vitro models to pinpoint whether pharmacological concentration of melatonin in combination with photodynamic therapy induces cell cytotoxicity. The cells were separately treated with various concentrations of melatonin (0 to 10 mM) and photodynamic irradiation alone or in combination. Cells were preliminary exposed to increasing concentrations of melatonin for 24 h and subsequently underwent laser irradiation for 60 s with an output power of 80 mW in continuous mode at 675 nm wavelength and a total light dose of 13.22 J/cm2. Cell viability, apoptosis/necrosis rates, and reactive oxygen species levels as well as heat shock protein 70 expression were monitored after single and combined treatments. A statistical analysis was performed by applying one-way analysis of variance (ANOVA) and post hoc Tukey’s test. Combination treatment of both cell lines caused a marked increase in apoptosis/necrosis rate, reactive oxygen species generation, and heat shock protein 70 expression compared to incubation of the cells with each agent alone (p < 0.05). SKOV3 cancer cells expressed higher level of heat shock protein 70 under experimental procedure as compared to HUVECs (p < 0.05). Our results introduce melatonin as a potent stimulus for enhancing the efficacy of laser on induction of apoptosis in tumor cells.
Literatur
1.
Zurück zum Zitat Luchetti F, Canonico B, Betti M, Arcangeletti M, Pilolli F, Piroddi M, Canesi L, Papa S, Galli F (2010) Melatonin signaling and cell protection function. FASEB J 24:3603–3624CrossRefPubMed Luchetti F, Canonico B, Betti M, Arcangeletti M, Pilolli F, Piroddi M, Canesi L, Papa S, Galli F (2010) Melatonin signaling and cell protection function. FASEB J 24:3603–3624CrossRefPubMed
2.
Zurück zum Zitat Bejarano I, Espino J, Marchena AM, Barriga C, Paredes SD, Rodríguez AB, Pariente JA (2011) Melatonin enhances hydrogen peroxide-induced apoptosis in human promyelocytic leukaemia HL-60 cells. Mol Cell Biochem 353:167–176CrossRefPubMed Bejarano I, Espino J, Marchena AM, Barriga C, Paredes SD, Rodríguez AB, Pariente JA (2011) Melatonin enhances hydrogen peroxide-induced apoptosis in human promyelocytic leukaemia HL-60 cells. Mol Cell Biochem 353:167–176CrossRefPubMed
3.
Zurück zum Zitat Dillon DC, Easley SE, Asch BB, Cheney RT, Brydon L, Jockers R, Winston JS, Brooks JS, Hurd T, Asch HL (2002) Differential expression of high-affinity melatonin receptors (MT1) in normal and malignant human breast tissue. Am J Clin Pathol 118:451–458CrossRefPubMed Dillon DC, Easley SE, Asch BB, Cheney RT, Brydon L, Jockers R, Winston JS, Brooks JS, Hurd T, Asch HL (2002) Differential expression of high-affinity melatonin receptors (MT1) in normal and malignant human breast tissue. Am J Clin Pathol 118:451–458CrossRefPubMed
4.
Zurück zum Zitat Ozdemir F, Deniz O, Kaynar K, Arslan M, Kavgaci H, Yildiz B, Aydin F (2008) The effects of melatonin on human hepatoma (Hep G2) cell line. Bratisl Lek Listy 110:276–279 Ozdemir F, Deniz O, Kaynar K, Arslan M, Kavgaci H, Yildiz B, Aydin F (2008) The effects of melatonin on human hepatoma (Hep G2) cell line. Bratisl Lek Listy 110:276–279
5.
Zurück zum Zitat Carbajo‐Pescador S, García‐Palomo A, Martín‐Renedo J, Piva M, González‐Gallego J, Mauriz JL (2011) Melatonin modulation of intracellular signaling pathways in hepatocarcinoma HepG2 cell line: role of the MT1 receptor. J Pineal Res 51:463–471CrossRefPubMed Carbajo‐Pescador S, García‐Palomo A, Martín‐Renedo J, Piva M, González‐Gallego J, Mauriz JL (2011) Melatonin modulation of intracellular signaling pathways in hepatocarcinoma HepG2 cell line: role of the MT1 receptor. J Pineal Res 51:463–471CrossRefPubMed
6.
Zurück zum Zitat Mao L, Yuan L, Slakey LM, Jones FE, Burow ME, Hill SM (2010) Inhibition of breast cancer cell invasion by melatonin is mediated through regulation of the p38 mitogen-activated protein kinase signaling pathway. Breast Cancer Res 12:R107CrossRefPubMedPubMedCentral Mao L, Yuan L, Slakey LM, Jones FE, Burow ME, Hill SM (2010) Inhibition of breast cancer cell invasion by melatonin is mediated through regulation of the p38 mitogen-activated protein kinase signaling pathway. Breast Cancer Res 12:R107CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat Wang J, Hao H, Yao L, Zhang X, Zhao S, Ling EA, Hao A, Li G (2012) Melatonin suppresses migration and invasion via inhibition of oxidative stress pathway in glioma cells. J Pineal Res 53:180–187CrossRefPubMed Wang J, Hao H, Yao L, Zhang X, Zhao S, Ling EA, Hao A, Li G (2012) Melatonin suppresses migration and invasion via inhibition of oxidative stress pathway in glioma cells. J Pineal Res 53:180–187CrossRefPubMed
8.
Zurück zum Zitat Hong Y, Won J, Lee Y, Lee S, Park K, Chang KT, Hong Y (2014) Melatonin treatment induces interplay of apoptosis, autophagy, and senescence in human colorectal cancer cells. J Pineal Res 56:264–274CrossRefPubMed Hong Y, Won J, Lee Y, Lee S, Park K, Chang KT, Hong Y (2014) Melatonin treatment induces interplay of apoptosis, autophagy, and senescence in human colorectal cancer cells. J Pineal Res 56:264–274CrossRefPubMed
9.
Zurück zum Zitat Ahn J-C, Biswas R, Kim J-S (2014) The enhanced apoptotic effect of photodynamic therapy using photofrin combined with genistein in human ovarian cancer cell SK-OV-3. Biomed Res 25:51–57 Ahn J-C, Biswas R, Kim J-S (2014) The enhanced apoptotic effect of photodynamic therapy using photofrin combined with genistein in human ovarian cancer cell SK-OV-3. Biomed Res 25:51–57
10.
Zurück zum Zitat Fang X, Wu P, Li J, Qi L, Tang Y, Jiang W, Zhao S (2012) Combination of apoptin with photodynamic therapy induces nasopharyngeal carcinoma cell death in vitro and in vivo. Oncol Rep 28:2077–2082PubMed Fang X, Wu P, Li J, Qi L, Tang Y, Jiang W, Zhao S (2012) Combination of apoptin with photodynamic therapy induces nasopharyngeal carcinoma cell death in vitro and in vivo. Oncol Rep 28:2077–2082PubMed
11.
Zurück zum Zitat Ahn J-C, Kang J-W, Shin J-I, Chung P-S (2012) Combination treatment with photodynamic therapy and curcumin induces mitochondria-dependent apoptosis in AMC-HN3 cells. Int J Oncol 41:2184–2190PubMed Ahn J-C, Kang J-W, Shin J-I, Chung P-S (2012) Combination treatment with photodynamic therapy and curcumin induces mitochondria-dependent apoptosis in AMC-HN3 cells. Int J Oncol 41:2184–2190PubMed
12.
Zurück zum Zitat Olivo M, Bhuvaneswari R, Lucky SS, Dendukuri N, Soo-Ping Thong P (2010) Targeted therapy of cancer using photodynamic therapy in combination with multi-faceted anti-tumor modalities. Pharmaceuticals 3:1507–1529CrossRefPubMedPubMedCentral Olivo M, Bhuvaneswari R, Lucky SS, Dendukuri N, Soo-Ping Thong P (2010) Targeted therapy of cancer using photodynamic therapy in combination with multi-faceted anti-tumor modalities. Pharmaceuticals 3:1507–1529CrossRefPubMedPubMedCentral
13.
Zurück zum Zitat Compagnin C, Mognato M, Celotti L, Canti G, Palumbo G, Reddi E (2010) Cell proliferation and cell cycle alterations in oesophageal p53‐mutated cancer cells treated with cisplatin in combination with photodynamic therapy. Cell Prolif 43:262–274CrossRefPubMed Compagnin C, Mognato M, Celotti L, Canti G, Palumbo G, Reddi E (2010) Cell proliferation and cell cycle alterations in oesophageal p53‐mutated cancer cells treated with cisplatin in combination with photodynamic therapy. Cell Prolif 43:262–274CrossRefPubMed
14.
Zurück zum Zitat Maharaj D, Molell H, Antunes E, Maharaj H, Maree D, Nyokong T, Glass B, Daya S (2005) Melatonin generates singlet oxygen on laser irradiation but acts as a quencher when irradiated by lamp photolysis. J Pineal Res 38:153–156CrossRefPubMed Maharaj D, Molell H, Antunes E, Maharaj H, Maree D, Nyokong T, Glass B, Daya S (2005) Melatonin generates singlet oxygen on laser irradiation but acts as a quencher when irradiated by lamp photolysis. J Pineal Res 38:153–156CrossRefPubMed
15.
Zurück zum Zitat Dastanpour S, Beitollahi JM, Saber K (2015) The effect of low-level laser therapy on human leukemic cells. J Lasers Med Sci 6:74PubMedPubMedCentral Dastanpour S, Beitollahi JM, Saber K (2015) The effect of low-level laser therapy on human leukemic cells. J Lasers Med Sci 6:74PubMedPubMedCentral
16.
Zurück zum Zitat Su Z, Yao K, Shen J, Jiang J, Fang X, Lin J, Du X (2007) Evaluation of photodynamic therapy in idiopathic choroidal neovascularization. Zhonghua Yan Ke Za Zhi 43:509–513PubMed Su Z, Yao K, Shen J, Jiang J, Fang X, Lin J, Du X (2007) Evaluation of photodynamic therapy in idiopathic choroidal neovascularization. Zhonghua Yan Ke Za Zhi 43:509–513PubMed
17.
Zurück zum Zitat Barnes LD, Giuliano EA, Ota J, Cohn LA, Moore CP (2009) The effect of photodynamic therapy on squamous cell carcinoma in a murine model: evaluation of time between intralesional injection to laser irradiation. Vet J 180:60–65CrossRefPubMed Barnes LD, Giuliano EA, Ota J, Cohn LA, Moore CP (2009) The effect of photodynamic therapy on squamous cell carcinoma in a murine model: evaluation of time between intralesional injection to laser irradiation. Vet J 180:60–65CrossRefPubMed
18.
Zurück zum Zitat Gomer CJ, Ferrario A, Luna M, Rucker N, Wong S (2006) Photodynamic therapy: combined modality approaches targeting the tumor microenvironment. Lasers Surg Med 38:516–521CrossRefPubMed Gomer CJ, Ferrario A, Luna M, Rucker N, Wong S (2006) Photodynamic therapy: combined modality approaches targeting the tumor microenvironment. Lasers Surg Med 38:516–521CrossRefPubMed
19.
Zurück zum Zitat Oleinick NL, Morris RL, Belichenko I (2002) The role of apoptosis in response to photodynamic therapy: what, where, why, and how. Photochem Photobiol Sci 1:1–21CrossRefPubMed Oleinick NL, Morris RL, Belichenko I (2002) The role of apoptosis in response to photodynamic therapy: what, where, why, and how. Photochem Photobiol Sci 1:1–21CrossRefPubMed
20.
Zurück zum Zitat Staton CA, Reed MW, Brown NJ (2009) A critical analysis of current in vitro and in vivo angiogenesis assays. Int J Exp Pathol 90:195–221 Staton CA, Reed MW, Brown NJ (2009) A critical analysis of current in vitro and in vivo angiogenesis assays. Int J Exp Pathol 90:195–221
21.
Zurück zum Zitat Elias KM, Emori MM, Papp E, MacDuffie E, Konecny GE, Velculescu VE, Drapkin R (2015) Beyond genomics: critical evaluation of cell line utility for ovarian cancer research. Gynecol Oncol 139:97–103 Elias KM, Emori MM, Papp E, MacDuffie E, Konecny GE, Velculescu VE, Drapkin R (2015) Beyond genomics: critical evaluation of cell line utility for ovarian cancer research. Gynecol Oncol 139:97–103
22.
Zurück zum Zitat Goff B, Blake J, Bamberg M, Hasan T (1996) Treatment of ovarian cancer with photodynamic therapy and immunoconjugates in a murine ovarian cancer model. Br J Cancer 74:1194 Goff B, Blake J, Bamberg M, Hasan T (1996) Treatment of ovarian cancer with photodynamic therapy and immunoconjugates in a murine ovarian cancer model. Br J Cancer 74:1194
23.
Zurück zum Zitat Schmidt S, Wagner U (2000) PDT for Cytoreduction in Cases of Ovarian Cancer. In: Wyss P, Tadir Y, Tromberg BJ, Haller U (eds) Photomedicine in Gynecology and Reproduction,1st ed. S. Karger, Basel, pp 296-301. doi:10.1159/isbn.978-3-318-00453-3 Schmidt S, Wagner U (2000) PDT for Cytoreduction in Cases of Ovarian Cancer. In: Wyss P, Tadir Y, Tromberg BJ, Haller U (eds) Photomedicine in Gynecology and Reproduction,1st ed. S. Karger, Basel, pp 296-301. doi:10.​1159/​isbn.​978-3-318-00453-3
24.
Zurück zum Zitat Gupta SC, Hevia D, Patchva S, Park B, Koh W, Aggarwal BB (2012) Upsides and downsides of reactive oxygen species for cancer: the roles of reactive oxygen species in tumorigenesis, prevention, and therapy. Antioxid Redox Signal 16:1295–1322 Gupta SC, Hevia D, Patchva S, Park B, Koh W, Aggarwal BB (2012) Upsides and downsides of reactive oxygen species for cancer: the roles of reactive oxygen species in tumorigenesis, prevention, and therapy. Antioxid Redox Signal 16:1295–1322
25.
Zurück zum Zitat Beere HM, Wolf BB, Cain K, Mosser DD, Mahboubi A, Kuwana T, Tailor P, Morimoto RI, Cohen GM, Green DR (2000) Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat Cell Biol 2:469–475CrossRefPubMed Beere HM, Wolf BB, Cain K, Mosser DD, Mahboubi A, Kuwana T, Tailor P, Morimoto RI, Cohen GM, Green DR (2000) Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat Cell Biol 2:469–475CrossRefPubMed
26.
Zurück zum Zitat Wang F, Dai A-Y, Tao K, Xiao Q, Huang Z-L, Gao M, Li H, Wang X, Cao W-X, Feng W-L (2015) Heat shock protein-70 neutralizes apoptosis inducing factor in Bcr/Abl expressing cells. Cell Signal 27:1949–1955CrossRefPubMed Wang F, Dai A-Y, Tao K, Xiao Q, Huang Z-L, Gao M, Li H, Wang X, Cao W-X, Feng W-L (2015) Heat shock protein-70 neutralizes apoptosis inducing factor in Bcr/Abl expressing cells. Cell Signal 27:1949–1955CrossRefPubMed
27.
Zurück zum Zitat Ran R, Lu A, Zhang L, Tang Y, Zhu H, Xu H, Feng Y, Han C, Zhou G, Rigby AC (2004) Hsp70 promotes TNF-mediated apoptosis by binding IKKγ and impairing NF-kB survival signaling. Genes Dev 18:1466–1481CrossRefPubMedPubMedCentral Ran R, Lu A, Zhang L, Tang Y, Zhu H, Xu H, Feng Y, Han C, Zhou G, Rigby AC (2004) Hsp70 promotes TNF-mediated apoptosis by binding IKKγ and impairing NF-kB survival signaling. Genes Dev 18:1466–1481CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Zhou F, Xing D, Chen WR (2009) Regulation of HSP70 on activating macrophages using PDT‐induced apoptotic cells. International J Cancer 125:1380–1389 Zhou F, Xing D, Chen WR (2009) Regulation of HSP70 on activating macrophages using PDT‐induced apoptotic cells. International J Cancer 125:1380–1389
29.
Zurück zum Zitat Cavanaugh A, Juengst B, Sheridan K, Danella J, Williams H (2015) Combined inhibition of heat shock proteins 90 and 70 leads to simultaneous degradation of the oncogenic signaling proteins involved in muscle invasive bladder cancer. Oncotarget 6:39821–39838 Cavanaugh A, Juengst B, Sheridan K, Danella J, Williams H (2015) Combined inhibition of heat shock proteins 90 and 70 leads to simultaneous degradation of the oncogenic signaling proteins involved in muscle invasive bladder cancer. Oncotarget 6:39821–39838
30.
Zurück zum Zitat Zhou F, Chen WR, Song S (2009) HSP70 inhibits Bax translocation during Photofrin-PDT apoptosis. Proc SPIE 7178:71780D. doi:10.1117/12.808111 Zhou F, Chen WR, Song S (2009) HSP70 inhibits Bax translocation during Photofrin-PDT apoptosis. Proc SPIE 7178:71780D. doi:10.​1117/​12.​808111
31.
Zurück zum Zitat Zhou F, Xing D, Chen WR (2008) Dynamics and mechanism of HSP70 translocation induced by photodynamic therapy treatment. Cancer Lett 264:135–144 Zhou F, Xing D, Chen WR (2008) Dynamics and mechanism of HSP70 translocation induced by photodynamic therapy treatment. Cancer Lett 264:135–144
Metadaten
Titel
Effects of combination of melatonin and laser irradiation on ovarian cancer cells and endothelial lineage viability
verfasst von
Maryam Akbarzadeh
Mohammad Nouri
Maryam Vahidi Banekohal
Omid Cheraghi
Habib Tajalli
Aliakbar Movassaghpour
Sina Soltani
Hadi Cheraghi
Navid Feizy
Soheila Montazersaheb
Reza Rahbarghazi
Nasser Samadi
Publikationsdatum
30.06.2016
Verlag
Springer London
Erschienen in
Lasers in Medical Science / Ausgabe 8/2016
Print ISSN: 0268-8921
Elektronische ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-016-2016-6

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