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01.02.2015 | Original Article

RUNX3 confers sensitivity to pheophorbide a-photodynamic therapy in human oral squamous cell carcinoma cell lines

verfasst von: Sook Moon, Jung Yoon Bae, Hwa-Kyung Son, Doo Young Lee, Gyeongju Park, Hyun You, Hyojin Ko, Yong-Chul Kim, Jin Kim

Erschienen in: Lasers in Medical Science | Ausgabe 2/2015

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Abstract

Photodynamic therapy (PDT) with photosensitizer is one of the promising modalities for cancer treatment. For clinical use of PDT, screening process should be preceded to enhance sensitivity to PDT. Thus, we investigated a molecular biomarker to determine the sensitivity to pheophorbide a (Pa)-PDT in immortalized human oral keratinocytes (IHOK) and oral squamous cell carcinoma (OSCC) cell lines. Two IHOK and several OSCC cell lines were used. After Pa-PDT, cell viability was reduced by more than 50 %, and reactive oxygen species were generated in IHOK and OSCC cell lines. Additionally, apoptosis occurred in PDT-treated cells. IHOK(S) and IHOK(P), the two IHOK cell lines derived from the same source, showed a difference in cytotoxicity after Pa-PDT. To explain this difference in cytotoxicity, we looked at the expression of Wnt signaling-related genes in these two cell lines, for the morphology of IHOK(S) which was spindle like and elongated and distinct from IHOK(P) and the parent cell. Among the relevant genes, runt-related transcription factor 3 (RUNX3), an apoptosis-related gene, was selected as a potential marker that confers sensitivity to PDT. We found that the cytotoxicity by Pa-PDT was proportional to RUNX3 expression in OSCC cell lines. Additionally, knockdown of RUNX3 expression reduced cytotoxicity by Pa-PDT, suggesting that RUNX3 might be a biomarker to determine sensitivity to Pa-PDT. This was the first study to find a new target molecule that enhances Pa-PDT effects in IHOK and OSCC cell lines. Hence, the development of a PDT-dependent biomarker could provide a novel approach to improve the effects of PDT on oral precancerous and cancerous lesions.

Hopper C, Kubler A, Lewis H, Tan IB, Putnam G (2004) mTHPC-mediated photodynamic therapy for early oral squamous cell carcinoma. Int J Cancer 111(1):138–146PubMedCrossRef

Bagan JV, Scully C (2008) Recent advances in oral oncology 2007: epidemiology, aetiopathogenesis, diagnosis and prognostication. Oral Oncol 44(2):103–108PubMedCrossRef

Warnakulasuriya S (2009) Global epidemiology of oral and oropharyngeal cancer. Oral Oncol 45(4–5):309–316PubMedCrossRef

Dolmans DE, Fukumura D, Jain RK (2003) Photodynamic therapy for cancer. Nat Rev Cancer 3(5):380–387PubMedCrossRef

Allison RR, Bagnato VS, Sibata CH (2010) Future of oncologic photodynamic therapy. Future Oncol 6(6):929–940PubMedCrossRef

Nyman ES, Hynninen PH (2004) Research advances in the use of tetrapyrrolic photosensitizers for photodynamic therapy. J Photochem Photobiol B 73(1–2):1–28PubMedCrossRef

Brown SB, Brown EA, Walker I (2004) The present and future role of photodynamic therapy in cancer treatment. Lancet Oncol 5(8):497–508PubMedCrossRef

Jerjes W, Upile T, Petrie A, Riskalla A, Hamdoon Z, Vourvachis M et al (2010) Clinicopathological parameters, recurrence, locoregional and distant metastasis in 115 T1-T2 oral squamous cell carcinoma patients. Head Neck Oncol 2:9PubMedCentralPubMedCrossRef

Xodo LE, Rapozzi V, Zacchigna M, Drioli S, Zorzet S (2012) The chlorophyll catabolite pheophorbide a as a photosensitizer for the photodynamic therapy. Curr Med Chem 19(6):799–807PubMedCrossRef

10.

Chan JY, Tang PM, Hon PM, Au SW, Tsui SK, Waye MM et al (2006) Pheophorbide a, a major antitumor component purified from Scutellaria barbata, induces apoptosis in human hepatocellular carcinoma cells. Planta Med 72(1):28–33PubMedCrossRef

11.

Nakamura Y, Murakami A, Koshimizu K, Ohigashi H (1996) Inhibitory effect of pheophorbide a, a chlorophyll-related compound, on skin tumor promotion in ICR mouse. Cancer Lett 108(2):247–255PubMedCrossRef

12.

Hibasami H, Kyohkon M, Ohwaki S, Katsuzaki H, Imai K, Nakagawa M et al (2000) Pheophorbide a, a moiety of chlorophyll a, induces apoptosis in human lymphoid leukemia molt 4B cells. Int J Mol Med 6(3):277–279PubMed

13.

Glinski JA, David E, Warren TC, Hansen G, Leonard SF, Pitner P et al (1995) Inactivation of cell surface receptors by pheophorbide a, a green pigment isolated from Psychotria acuminata. Photochem Photobiol 62(1):144–150PubMedCrossRef

14.

Lim DS, Ko SH, Kim SJ, Park YJ, Park JH, Lee WY (2002) Photoinactivation of vesicular stomatitis virus by a photodynamic agent, chlorophyll derivatives from silkworm excreta. J Photochem Photobiol B 67(3):149–156PubMedCrossRef

15.

Hajri A, Wack S, Meyer C, Smith MK, Leberquier C, Kedinger M et al (2002) In vitro and in vivo efficacy of photofrin and pheophorbide a, a bacteriochlorin, in photodynamic therapy of colonic cancer cells. Photochem Photobiol 75(2):140–148PubMedCrossRef

16.

Lee WY, Lim DS, Ko SH, Park YJ, Ryu KS, Ahn MY et al (2004) Photoactivation of pheophorbide a induces a mitochondrial-mediated apoptosis in Jurkat leukaemia cells. J Photochem Photobiol B 75(3):119–126PubMedCrossRef

17.

Lim DS, Ko SH, Lee WY (2004) Silkworm-pheophorbide alpha mediated photodynamic therapy against B16F10 pigmented melanoma. J Photochem Photobiol B 74(1):1–6PubMedCrossRef

18.

Tang PM, Chan JY, Au SW, Kong SK, Tsui SK, Waye MM et al (2006) Pheophorbide a, an active compound isolated from Scutellaria barbata, possesses photodynamic activities by inducing apoptosis in human hepatocellular carcinoma. Cancer Biol Ther 5(9):1111–1116PubMedCrossRef

19.

Li WT, Tsao HW, Chen YY, Cheng SW, Hsu YC (2007) A study on the photodynamic properties of chlorophyll derivatives using human hepatocellular carcinoma cells. Photochem Photobiol Sci 6(12):1341–1348PubMedCrossRef

20.

Tsai JC, Chiang CP, Chen HM, Huang SB, Wang CW, Lee MI et al (2004) Photodynamic therapy of oral dysplasia with topical 5-aminolevulinic acid and light-emitting diode array. Lasers Surg Med 34(1):18–24PubMedCrossRef

21.

Chen HM, Chen CT, Yang H, Kuo MY, Kuo YS, Lan WH et al (2004) Successful treatment of oral verrucous hyperplasia with topical 5-aminolevulinic acid-mediated photodynamic therapy. Oral Oncol 40(6):630–637PubMedCrossRef

22.

Chen HM, Yu CH, Tu PC, Yeh CY, Tsai T, Chiang CP (2005) Successful treatment of oral verrucous hyperplasia and oral leukoplakia with topical 5-aminolevulinic acid-mediated photodynamic therapy. Lasers Surg Med 37(2):114–122PubMedCrossRef

23.

Yu CH, Chen HM, Hung HY, Cheng SJ, Tsai T, Chiang CP (2008) Photodynamic therapy outcome for oral verrucous hyperplasia depends on the clinical appearance, size, color, epithelial dysplasia, and surface keratin thickness of the lesion. Oral Oncol 44(6):595–600PubMedCrossRef

24.

Yu CH, Lin HP, Chen HM, Yang H, Wang YP, Chiang CP (2009) Comparison of clinical outcomes of oral erythroleukoplakia treated with photodynamic therapy using either light-emitting diode or laser light. Lasers Surg Med 41(9):628–633PubMedCrossRef

25.

Chen H-M, Yu C-H, Tsai T, Hsu Y-C, Kuo R-C, Chiang C-P (2007) Topical 5-aminolevulinic acid-mediated photodynamic therapy for oral verrucous hyperplasia, oral leukoplakia and oral erythroleukoplakia. Photodiagnosis and Photodynamic Therapy 4:44–52PubMedCrossRef

26.

Lee EJ, Kim J, Lee SA, Kim EJ, Chun YC, Ryu MH et al (2005) Characterization of newly established oral cancer cell lines derived from six squamous cell carcinoma and two mucoepidermoid carcinoma cells. Exp Mol Med 37(5):379–390PubMedCrossRef

27.

Lee HJ, Guo HY, Lee SK, Jeon BH, Jun CD, Lee SK et al (2005) Effects of nicotine on proliferation, cell cycle, and differentiation in immortalized and malignant oral keratinocytes. J Oral Pathol Med 34(7):436–443PubMedCrossRef

28.

Ahn MY, Kwon SM, Kim YC, Ahn SG, Yoon JH (2012) Pheophorbide a-mediated photodynamic therapy induces apoptotic cell death in murine oral squamous cell carcinoma in vitro and in vivo. Oncol Rep 27(6):1772–1778PubMed

29.

Lim SH, Lee HB, Ho AS (2011) A new naturally derived photosensitizer and its phototoxicity on head and neck cancer cells. Photochem Photobiol 87(5):1152–1158PubMedCrossRef

30.

Hsieh YJ, Wu CC, Chang CJ, Yu JS (2003) Subcellular localization of Photofrin determines the death phenotype of human epidermoid carcinoma A431 cells triggered by photodynamic therapy: when plasma membranes are the main targets. J Cell Physiol 194(3):363–375PubMedCrossRef

31.

Castano AP, Demidova TN, Hamblin MR (2004) Mechanisms in photodynamic therapy: part one—photosensitizers, photochemistry and cellular localization. Photodiagnosis and Photodynamic Therapy 1:279–293PubMedCentralPubMedCrossRef

32.

Almeida RD, Manadas BJ, Carvalho AP, Duarte CB (2004) Intracellular signaling mechanisms in photodynamic therapy. Biochim Biophys Acta 1704(2):59–86PubMed

33.

Tang PM, Liu XZ, Zhang DM, Fong WP, Fung KP (2009) Pheophorbide a based photodynamic therapy induces apoptosis via mitochondrial-mediated pathway in human uterine carcinosarcoma. Cancer Biol Ther 8(6):533–539PubMedCrossRef

34.

Bangsow C, Rubins N, Glusman G, Bernstein Y, Negreanu V, Goldenberg D et al (2001) The RUNX3 gene—sequence, structure and regulated expression. Gene 279(2):221–232PubMedCrossRef

35.

Yamamura Y, Lee WL, Inoue K, Ida H, Ito Y (2006) RUNX3 cooperates with FoxO3a to induce apoptosis in gastric cancer cells. J Biol Chem 281(8):5267–5276PubMedCrossRef

36.

Nakanishi Y, Shiraha H, Nishina S, Tanaka S, Matsubara M, Horiguchi S et al (2011) Loss of runt-related transcription factor 3 expression leads hepatocellular carcinoma cells to escape apoptosis. BMC Cancer 11:3PubMedCentralPubMedCrossRef

37.

Vogiatzi P, De Falco G, Claudio PP, Giordano A (2006) How does the human RUNX3 gene induce apoptosis in gastric cancer? Latest data, reflections and reactions. Cancer Biol Ther 5(4):371–374PubMedCrossRef

38.

Ito K (2011) RUNX3 in oncogenic and anti-oncogenic signaling in gastrointestinal cancers. J Cell Biochem 112(5):1243–1249PubMedCrossRef

39.

Ito K, Liu Q, Salto-Tellez M, Yano T, Tada K, Ida H et al (2005) RUNX3, a novel tumor suppressor, is frequently inactivated in gastric cancer by protein mislocalization. Cancer Res 65(17):7743–7750PubMed

40.

Gao F, Huang C, Lin M, Wang Z, Shen J, Zhang H et al (2009) Frequent inactivation of RUNX3 by promoter hypermethylation and protein mislocalization in oral squamous cell carcinomas. J Cancer Res Clin Oncol 135(5):739–747PubMedCrossRef

41.

Chen LF (2012) Tumor suppressor function of RUNX3 in breast cancer. J Cell Biochem 113(5):1470–1477PubMedCentralPubMed

42.

Lee CW, Chuang LS, Kimura S, Lai SK, Ong CW, Yan B et al (2011) RUNX3 functions as an oncogene in ovarian cancer. Gynecol Oncol 122(2):410–417PubMedCrossRef

43.

Kudo Y, Tsunematsu T, Takata T (2011) Oncogenic role of RUNX3 in head and neck cancer. J Cell Biochem 112(2):387–393PubMedCrossRef

Titel: RUNX3 confers sensitivity to pheophorbide a-photodynamic therapy in human oral squamous cell carcinoma cell lines
verfasst von: Sook Moon
Jung Yoon Bae
Hwa-Kyung Son
Doo Young Lee
Gyeongju Park
Hyun You
Hyojin Ko
Yong-Chul Kim
Jin Kim
Publikationsdatum: 01.02.2015
Verlag: Springer London
Erschienen in: Lasers in Medical Science / Ausgabe 2/2015
Print ISSN: 0268-8921
Elektronische ISSN: 1435-604X
DOI: https://doi.org/10.1007/s10103-013-1350-1

Springer Medizin

Abstract

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