Skip to main content
Erschienen in: Lasers in Medical Science 3/2021

28.05.2020 | Original Article

In vitro anti-tumor effect of high-fluence low-power laser light on apoptosis of human colorectal cancer cells

verfasst von: Ye Tian, Hyejin Kim, Hyun Wook Kang

Erschienen in: Lasers in Medical Science | Ausgabe 3/2021

Einloggen, um Zugang zu erhalten

Abstract

Colorectal cancer is the third most common malignancy all over the world, along with high morbidity and mortality. As a treatment, high-fluence low-power laser irradiation (HF-LPLI) has reported that its biostimulatory activity can suppress or even destruct tumor growth in neoplastic diseases. The aim of the present study is to examine a therapeutic capacity of HF-LPLI for colorectal cancer treatment by using human colon cancer cell (HT29) model. The in vitro cancer cell model was used to analyze the underlying mechanism of laser-induced apoptosis. Laser irradiation was performed five times (once a day for five consecutive days) with 635 nm laser light for 8 and 16 min (fluence = 128 and 256 J/cm2), respectively. The efficiency of the HF-LPLI treatment was evaluated by MTT, fluorescence staining, cell wound healing, and western blot test during the 5-day period. Experiment data showed that HF-LPLI had a dose-dependent stimulating effect on cell viability, migration, and apoptosis of HT29 cells. The inhibition effect of laser treatment at 256 J/cm2 on cell viability was statistically significant. Meanwhile, the wound healing and western blot tests also confirmed that HF-LPLI could inhibit cell migration and induce cell apoptosis. The current research results demonstrate that 635 nm HF-LPLI can be an alternative treatment option for colorectal cancer by increasing the expression of caspase-3 and inducing HT29 tumor cell apoptosis through activation of the mitochondrial pathway.
Literatur
1.
Zurück zum Zitat Lemoine L, Sugarbaker P, Kurt VDS (2016) Pathophysiology of colorectal peritoneal carcinomatosis: role of the peritoneum. World J Gastroenterol [J] 22(34):7692–7707 Lemoine L, Sugarbaker P, Kurt VDS (2016) Pathophysiology of colorectal peritoneal carcinomatosis: role of the peritoneum. World J Gastroenterol [J] 22(34):7692–7707
2.
Zurück zum Zitat Arjona-Sánchez A, Muñoz-Casares FC, Casado-Adam A et al (2014) Peritoneal metastases of colorectal origin treated by cytoreduction and HIPEC: an overview [J]. World J Gastrointest Oncol 6(10):407CrossRef Arjona-Sánchez A, Muñoz-Casares FC, Casado-Adam A et al (2014) Peritoneal metastases of colorectal origin treated by cytoreduction and HIPEC: an overview [J]. World J Gastrointest Oncol 6(10):407CrossRef
3.
Zurück zum Zitat Bosman FT (2014) Chapter Chapter 5.5: Colorectal cancer. In: Stewart BW, Wild CP (eds) World cancer report. The International Agency for Research on Cancer, World Health Organization, pp 392–402 ISBN 978-92-832-0443-5 Bosman FT (2014) Chapter Chapter 5.5: Colorectal cancer. In: Stewart BW, Wild CP (eds) World cancer report. The International Agency for Research on Cancer, World Health Organization, pp 392–402 ISBN 978-92-832-0443-5
4.
Zurück zum Zitat Grady WM (2003) Genetic testing for high-risk colon cancer patients [J]. Gastroenterology 124(6):1574–1594CrossRef Grady WM (2003) Genetic testing for high-risk colon cancer patients [J]. Gastroenterology 124(6):1574–1594CrossRef
5.
Zurück zum Zitat De Freitas LF, Hamblin MR (2016) Proposed mechanisms of photobiomodulation or low-level light therapy [J]. IEEE J Sel Topics Quantum Electron 22(3):1–17CrossRef De Freitas LF, Hamblin MR (2016) Proposed mechanisms of photobiomodulation or low-level light therapy [J]. IEEE J Sel Topics Quantum Electron 22(3):1–17CrossRef
6.
Zurück zum Zitat Chung H, Dai T, Sharma SK et al (2012) The nuts and bolts of low-level laser (light) therapy [J]. Ann Biomed Eng 40(2):516–533CrossRef Chung H, Dai T, Sharma SK et al (2012) The nuts and bolts of low-level laser (light) therapy [J]. Ann Biomed Eng 40(2):516–533CrossRef
7.
Zurück zum Zitat Caruso-Davis MK, Guillot TS, Podichetty VK et al (2011) Efficacy of low-level laser therapy for body contouring and spot fat reduction [J]. Obes Surg 21(6):722–729CrossRef Caruso-Davis MK, Guillot TS, Podichetty VK et al (2011) Efficacy of low-level laser therapy for body contouring and spot fat reduction [J]. Obes Surg 21(6):722–729CrossRef
8.
Zurück zum Zitat Lubart R, Wollman Y, Friedmann H, Rochkind S, Lanlicht Y (1992) Effects of visible and near-infrared lasers on cell cultures. J Photochem Photobiol B Biol 12:305–310CrossRef Lubart R, Wollman Y, Friedmann H, Rochkind S, Lanlicht Y (1992) Effects of visible and near-infrared lasers on cell cultures. J Photochem Photobiol B Biol 12:305–310CrossRef
9.
Zurück zum Zitat Karu T (2010) Mitochondrial mechanisms of photobiomodulation in context of new data about multiple roles of ATP. Photomed Laser Surg 28:159–160CrossRef Karu T (2010) Mitochondrial mechanisms of photobiomodulation in context of new data about multiple roles of ATP. Photomed Laser Surg 28:159–160CrossRef
10.
Zurück zum Zitat Lanzafame RJ (2011) Photobiomodulation and cancer and other musings. Photomed Laser Surg 29:3–4CrossRef Lanzafame RJ (2011) Photobiomodulation and cancer and other musings. Photomed Laser Surg 29:3–4CrossRef
11.
Zurück zum Zitat Santana Blank L, Rodríguez-Santana E, Santana-Rodríguez KE (2012) Concurrence of emerging developments in photobiomodulation and cancer. Photomed Laser Surg 30:1–2CrossRef Santana Blank L, Rodríguez-Santana E, Santana-Rodríguez KE (2012) Concurrence of emerging developments in photobiomodulation and cancer. Photomed Laser Surg 30:1–2CrossRef
12.
Zurück zum Zitat Santana-Blank LA, Rodríguez-Santana E, Vargas F, Reyes H, Fernández-Andrade P, Rukos S et al (2002) Phase I trial of an infrared pulsed laser device in patients with advanced neoplasias. Clin Cancer Res 8:3082–3091PubMed Santana-Blank LA, Rodríguez-Santana E, Vargas F, Reyes H, Fernández-Andrade P, Rukos S et al (2002) Phase I trial of an infrared pulsed laser device in patients with advanced neoplasias. Clin Cancer Res 8:3082–3091PubMed
13.
Zurück zum Zitat Tata DB, Waynant RW (2011) Laser therapy: a review of its mechanism of action and potential medical applications. Laser Photonics Rev 5:1–12CrossRef Tata DB, Waynant RW (2011) Laser therapy: a review of its mechanism of action and potential medical applications. Laser Photonics Rev 5:1–12CrossRef
14.
Zurück zum Zitat Tata DB, Fahey M, Mitra K, Anders J, Waynant RW (2007) Near-IR induced suppression of metabolic activity in aggressive cancers. Proc SPIE 6428:64280ECrossRef Tata DB, Fahey M, Mitra K, Anders J, Waynant RW (2007) Near-IR induced suppression of metabolic activity in aggressive cancers. Proc SPIE 6428:64280ECrossRef
15.
Zurück zum Zitat Tata DB, Waynant RW (2008) Laser light induced modulations in metabolic activities in human brain cancer. Proc SPIE 6846:684607CrossRef Tata DB, Waynant RW (2008) Laser light induced modulations in metabolic activities in human brain cancer. Proc SPIE 6846:684607CrossRef
16.
Zurück zum Zitat Tanaka Y, Tatewaki N, Nishida H, Eitsuka T, Ikekawa N, Nakayama J (2012) Non-thermal DNA damage of cancer cells using near-infrared irradiation. Cancer Sci 103:1467–1473CrossRef Tanaka Y, Tatewaki N, Nishida H, Eitsuka T, Ikekawa N, Nakayama J (2012) Non-thermal DNA damage of cancer cells using near-infrared irradiation. Cancer Sci 103:1467–1473CrossRef
17.
Zurück zum Zitat Tanaka Y, Matsuo K, Yuzuriha S, Yan H, Nakayama J (2010) Non-thermal cytocidal effect of infrared irradiation on cultured cancer cells using specialized device. Cancer Sci 101:1396–1402CrossRef Tanaka Y, Matsuo K, Yuzuriha S, Yan H, Nakayama J (2010) Non-thermal cytocidal effect of infrared irradiation on cultured cancer cells using specialized device. Cancer Sci 101:1396–1402CrossRef
18.
Zurück zum Zitat Wang F, Chen TS, Xing D, Wang JJ, Wu YX (2005) Measuring dynamics of caspase-3 activity in living cells using FRET technique during apoptosis induced by high fluence low-power laser irradiation. Lasers Surg Med 36:2–7CrossRef Wang F, Chen TS, Xing D, Wang JJ, Wu YX (2005) Measuring dynamics of caspase-3 activity in living cells using FRET technique during apoptosis induced by high fluence low-power laser irradiation. Lasers Surg Med 36:2–7CrossRef
19.
Zurück zum Zitat Chu J, Wu S, Xing D (2010) Survivin mediates self-protection through ROS/cdc25c/CDK1 signaling pathway during tumor cell apoptosis induced by high fluence low-power laser irradiation [J]. Cancer Lett 297(2):0–219CrossRef Chu J, Wu S, Xing D (2010) Survivin mediates self-protection through ROS/cdc25c/CDK1 signaling pathway during tumor cell apoptosis induced by high fluence low-power laser irradiation [J]. Cancer Lett 297(2):0–219CrossRef
20.
Zurück zum Zitat Tian Y, Lee Y, Kim H et al (2019) In vitro anti-tumor effect of low-power laser irradiation (LPLI) on gastroenterological carcinoma cells [J]. Lasers Med Sci 35(3):677–685 Tian Y, Lee Y, Kim H et al (2019) In vitro anti-tumor effect of low-power laser irradiation (LPLI) on gastroenterological carcinoma cells [J]. Lasers Med Sci 35(3):677–685
21.
Zurück zum Zitat Liang WZ, Liu PF, Fu E et al (2015) Selective cytotoxic effects of low-power laser irradiation on human oral cancer cells [J]. Lasers Surg Med 47(9):756–764CrossRef Liang WZ, Liu PF, Fu E et al (2015) Selective cytotoxic effects of low-power laser irradiation on human oral cancer cells [J]. Lasers Surg Med 47(9):756–764CrossRef
22.
Zurück zum Zitat Cornelissen M, Philippé J, Sitter SD et al (2002) Annexin V expression in apoptotic peripheral blood lymphocytes: an electron microscopic evaluation [J]. Apoptosis 7(1):41–47CrossRef Cornelissen M, Philippé J, Sitter SD et al (2002) Annexin V expression in apoptotic peripheral blood lymphocytes: an electron microscopic evaluation [J]. Apoptosis 7(1):41–47CrossRef
23.
Zurück zum Zitat Rieger AM, Nelso KL, Konowalchuk JD, Barreda DR Modified annexin V/propidium iodide apoptosis assay for accurate assessment of cell death [J]. Vis Exp 24(50):e2597 Rieger AM, Nelso KL, Konowalchuk JD, Barreda DR Modified annexin V/propidium iodide apoptosis assay for accurate assessment of cell death [J]. Vis Exp 24(50):e2597
24.
Zurück zum Zitat Tsai SR, Hamblin MR (2017) Biological effects and medical applications of infrared radiation [J]. J Photochem Photobiol B Biol 170:197–207CrossRef Tsai SR, Hamblin MR (2017) Biological effects and medical applications of infrared radiation [J]. J Photochem Photobiol B Biol 170:197–207CrossRef
25.
Zurück zum Zitat Sperandio FF, Simões A, Corrêa L et al (2014) Low-level laser irradiation promotes the proliferation and maturation of keratinocytes during epithelial wound repair [J]. J Biophotonics 9999(9999):n/a–n/a Sperandio FF, Simões A, Corrêa L et al (2014) Low-level laser irradiation promotes the proliferation and maturation of keratinocytes during epithelial wound repair [J]. J Biophotonics 9999(9999):n/a–n/a
26.
Zurück zum Zitat Hode L (2016) Low-level laser therapy may have Cancer fighting role [J]. Photomed Laser Surg 34(6):221–222 Hode L (2016) Low-level laser therapy may have Cancer fighting role [J]. Photomed Laser Surg 34(6):221–222
27.
Zurück zum Zitat Sperandio FF, Giudice FS, Corrêa L et al (2013) Low-level laser therapy can produce increased aggressiveness of dysplastic and oral cancer cell lines by modulation of Akt/mTOR signaling pathway [J]. J Biophotonics 6(10):n/a–n/aCrossRef Sperandio FF, Giudice FS, Corrêa L et al (2013) Low-level laser therapy can produce increased aggressiveness of dysplastic and oral cancer cell lines by modulation of Akt/mTOR signaling pathway [J]. J Biophotonics 6(10):n/a–n/aCrossRef
28.
Zurück zum Zitat Bamps M, Dok R, Nuyts S (2018) Low-level laser therapy stimulates proliferation in head and neck squamous cell carcinoma cells [J]. Front Oncol 8:343CrossRef Bamps M, Dok R, Nuyts S (2018) Low-level laser therapy stimulates proliferation in head and neck squamous cell carcinoma cells [J]. Front Oncol 8:343CrossRef
29.
Zurück zum Zitat Kara C, Selamet H, Gökmenoğlu C et al (2017) Low level laser therapy induces increased viability and proliferation in isolated cancer cells [J]. Cell Prolif 51(2):e12417 Kara C, Selamet H, Gökmenoğlu C et al (2017) Low level laser therapy induces increased viability and proliferation in isolated cancer cells [J]. Cell Prolif 51(2):e12417
30.
Zurück zum Zitat Hamblin MR, Nelson ST, Strahan JR (2018) Photobiomodulation and cancer: what is the truth? [J]. Photomed Laser Surg 36(5):241–245CrossRef Hamblin MR, Nelson ST, Strahan JR (2018) Photobiomodulation and cancer: what is the truth? [J]. Photomed Laser Surg 36(5):241–245CrossRef
31.
Zurück zum Zitat Mikhailov VA, Denisov IN, Frank GA et al (2000) Results of treatment of patients with second-to third-stage breast cancer by combination of low-level laser therapy (LLLT) and surgery: ten-year experience [C]//Laser Florence’99: A Window on the Laser Medicine World. Int Soc Opt Photon 4166:40–42 Mikhailov VA, Denisov IN, Frank GA et al (2000) Results of treatment of patients with second-to third-stage breast cancer by combination of low-level laser therapy (LLLT) and surgery: ten-year experience [C]//Laser Florence’99: A Window on the Laser Medicine World. Int Soc Opt Photon 4166:40–42
32.
Zurück zum Zitat Myakishev-Rempel M, Stadler I, Brondon P et al (2012) A preliminary study of the safety of red light phototherapy of tissues harboring cancer [J]. Photomed Laser Surg 30(9):551–558CrossRef Myakishev-Rempel M, Stadler I, Brondon P et al (2012) A preliminary study of the safety of red light phototherapy of tissues harboring cancer [J]. Photomed Laser Surg 30(9):551–558CrossRef
33.
Zurück zum Zitat Santana-Blank LA, Castes M, Rojas ME et al (1992) Evaluation of serum levels of tumour necrosis factor-alpha (TNF-α) and soluble IL-2 receptor (sIL-2R) and CD4, CD8 and natural killer (NK) populations during infrared pulsed laser device (IPLD) treatment [J]. Clin Ex Immunol 90(1):43–48CrossRef Santana-Blank LA, Castes M, Rojas ME et al (1992) Evaluation of serum levels of tumour necrosis factor-alpha (TNF-α) and soluble IL-2 receptor (sIL-2R) and CD4, CD8 and natural killer (NK) populations during infrared pulsed laser device (IPLD) treatment [J]. Clin Ex Immunol 90(1):43–48CrossRef
34.
Zurück zum Zitat Santana-Blank LA, Rodríguez-Santana E, Vargas F et al (2002) Photo-induced cytomorphologic changes in an advanced cancer phase I clinical trial [J]. Lasers Surg Med 30(1):18–25CrossRef Santana-Blank LA, Rodríguez-Santana E, Vargas F et al (2002) Photo-induced cytomorphologic changes in an advanced cancer phase I clinical trial [J]. Lasers Surg Med 30(1):18–25CrossRef
35.
Zurück zum Zitat Haraldsdottir KH, Ingvar C, Stenram U et al (2015) Long-term follow-up after interstitial laser thermotherapy of breast cancer [J]. Anticancer Res 35(11):6147–6152PubMed Haraldsdottir KH, Ingvar C, Stenram U et al (2015) Long-term follow-up after interstitial laser thermotherapy of breast cancer [J]. Anticancer Res 35(11):6147–6152PubMed
36.
Zurück zum Zitat Petrellis MC, Frigo L, Marcos RL et al (2017) Laser photobiomodulation of pro-inflammatory mediators on Walker Tumor 256 induced rats [J]. J Photochem Photobiol B 177:69–75 Petrellis MC, Frigo L, Marcos RL et al (2017) Laser photobiomodulation of pro-inflammatory mediators on Walker Tumor 256 induced rats [J]. J Photochem Photobiol B 177:69–75
37.
Zurück zum Zitat Shao J, Griffin RJ, Galanzha EI, Kim JW, Koonce N, Webber J, Mustafa T, Biris AS, Nedosekin DA, Zharov VP (2013) Photothermal nanodrugs: potential of TNF-gold nanospheres for cancer theranostics. Sci Rep 3:1293CrossRef Shao J, Griffin RJ, Galanzha EI, Kim JW, Koonce N, Webber J, Mustafa T, Biris AS, Nedosekin DA, Zharov VP (2013) Photothermal nanodrugs: potential of TNF-gold nanospheres for cancer theranostics. Sci Rep 3:1293CrossRef
38.
Zurück zum Zitat Fisher JW, Sarkar S, Buchanan CF, Szot CS, Whitney J, Hatcher HC, Torti SV, Rylander CG, Rylander MN (2010) Photothermal response of human and murine cancer cells to multiwalled carbon nanotubes after laser irradiation. Cancer Res 70(23):9855–9864CrossRef Fisher JW, Sarkar S, Buchanan CF, Szot CS, Whitney J, Hatcher HC, Torti SV, Rylander CG, Rylander MN (2010) Photothermal response of human and murine cancer cells to multiwalled carbon nanotubes after laser irradiation. Cancer Res 70(23):9855–9864CrossRef
39.
Zurück zum Zitat Burke A, Ding X, Singh R, Kraft RA, Levi-Polyachenko N, Rylander MN, Szot C, Buchanan C, Whitney J, Fisher J, Hatcher HC, D’Agostino R Jr, Kock ND, Ajayan PM, Carroll DL, Akman S, Torti FM, Torti SV (2009) Long-term survival following a single treatment of kidney tumors with multiwalled carbon nanotubes and near-infrared radiation. Proc Natl Acad Sci U S A 106(31):12897–12902CrossRef Burke A, Ding X, Singh R, Kraft RA, Levi-Polyachenko N, Rylander MN, Szot C, Buchanan C, Whitney J, Fisher J, Hatcher HC, D’Agostino R Jr, Kock ND, Ajayan PM, Carroll DL, Akman S, Torti FM, Torti SV (2009) Long-term survival following a single treatment of kidney tumors with multiwalled carbon nanotubes and near-infrared radiation. Proc Natl Acad Sci U S A 106(31):12897–12902CrossRef
40.
Zurück zum Zitat Bravo-Cordero JJ, Hodgson L, Condeelis J (2012) Directed cell invasion and migration during metastasis. Curr Opin Cell Biol 24(2):277–283CrossRef Bravo-Cordero JJ, Hodgson L, Condeelis J (2012) Directed cell invasion and migration during metastasis. Curr Opin Cell Biol 24(2):277–283CrossRef
41.
Zurück zum Zitat Entschladen F, Drell TL, Lang K, Joseph J, Zaenker KS (2004) Tumour-cell migration, invasion, and metastasis: navigation by neurotransmitters. Lancet Oncol 5(4):254–258CrossRef Entschladen F, Drell TL, Lang K, Joseph J, Zaenker KS (2004) Tumour-cell migration, invasion, and metastasis: navigation by neurotransmitters. Lancet Oncol 5(4):254–258CrossRef
Metadaten
Titel
In vitro anti-tumor effect of high-fluence low-power laser light on apoptosis of human colorectal cancer cells
verfasst von
Ye Tian
Hyejin Kim
Hyun Wook Kang
Publikationsdatum
28.05.2020
Verlag
Springer London
Erschienen in
Lasers in Medical Science / Ausgabe 3/2021
Print ISSN: 0268-8921
Elektronische ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-020-03050-x

Weitere Artikel der Ausgabe 3/2021

Lasers in Medical Science 3/2021 Zur Ausgabe