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01-02-2013 | Original Article

The effects of Photofrin-mediated photodynamic therapy on the modulation of EGFR in esophageal squamous cell carcinoma cells

Authors: Pei-Wen Yang, Mien-Chie Hung, Ching-Yueh Hsieh, En-Chi Tung, Ying-Hao Wang, Jui-Chang Tsai, Jang-Ming Lee

Published in: Lasers in Medical Science | Issue 2/2013

Abstract

Photodynamic therapy (PDT) has been demonstrated to be an effective minimally invasive treatment modality for early esophageal cancer. However, the molecular action in esophageal cancer during PDT is hardly known. EGFR has been known to downregulate in various cancer cells during PDT. In this study, we investigated the effects of Photofrin-mediated PDT on cell death and expression of EGFR in CE48T/VGH (CE48T) esophageal squamous cell carcinoma cells. We found that the photosensitizer Photofrin in the absence of light exposure can downregulate the expression of EGFR at both transcription and translation levels. Higher concentrations of Photofrin results in cytotoxicity whereas lower doses of Photofrin inhibit EGFR expression under dark control without inducing significant cell death. This Photofrin-associated inhibition of EGFR was repeated in lung cancer, cervical cancer, and glioblastoma cells. Another esophageal squamous cell carcinoma cell line CE81T/VGH (CE81T) was found to be resistant to Photofrin-induced inhibition of EGFR as well as to Photofrin-mediated dark toxicity compared with CE48T. The resistance to the cytotoxicity in CE81T cells became insignificant when the Photofrin-treated cells were further irradiated by red light (Photofrin-PDT). We suggest Photofrin modulates the expression of EGFR in cancer cells. However, efficient cell death still requires the combination of Photofrin and light irradiation in esophageal squamous cell carcinoma cells.

Almeida RD et al (2004) Intracellular signaling mechanisms in photodynamic therapy. Biochim Biophys Acta 1704(2):59–86PubMed

Rosenthal I, Ben-Hur E (1995) Role of oxygen in the phototoxicity of phthalocyanines. Int J Radiat Biol 67(1):85–91PubMedCrossRef

Enzinger PC, Mayer RJ (2003) Esophageal cancer. N Engl J Med 349(23):2241–2252PubMedCrossRef

Jemal A et al (2003) Cancer statistics, 2003. CA Cancer J Clin 53(1):5–26PubMedCrossRef

Melis M et al (2010) An elevated body mass index does not reduce survival after esophagectomy for cancer. Ann Surg Oncol 18:824-831

Parkin DM et al (2005) Global cancer statistics, 2002. CA Cancer J Clin 55(2):74–108PubMedCrossRef

Bosset JF et al (1997) Chemoradiotherapy followed by surgery compared with surgery alone in squamous-cell cancer of the esophagus. N Engl J Med 337(3):161–167PubMedCrossRef

Kelsen DP et al (1998) Chemotherapy followed by surgery compared with surgery alone for localized esophageal cancer. N Engl J Med 339(27):1979–1984PubMedCrossRef

Tanaka T et al (2011) Photodynamic therapy for large superficial squamous cell carcinoma of the esophagus. Gastrointest Endosc 73(1):1–6PubMedCrossRef

10.

Moghissi K et al (2009) Photofrin PDT for early stage oesophageal cancer: long term results in 40 patients and literature review. Photodiagnosis Photodyn Ther 6(3–4):159–166PubMedCrossRef

11.

Petro W (1991) Physical therapy and long-term oxygen therapy in diseases of the respiratory organs. Dtsch Med Wochenschr 116(46):1763–1769PubMedCrossRef

12.

Cheon YK et al (2007) Outcome of photodynamic therapy for early esophageal cancer. Gut Liver 1(2):126–131PubMedCrossRef

13.

Schmidt MH et al (1996) Light-emitting diodes as a light source for intraoperative photodynamic therapy. Neurosurgery 38(3):552–556; discussion 556–557

14.

Giuliano EA, Ota J, Tucker SA (2007) Photodynamic therapy: basic principles and potential uses for the veterinary ophthalmologist. Vet Ophthalmol 10(6):337–343PubMedCrossRef

15.

Sibille A et al (1995) Long-term survival after photodynamic therapy for esophageal cancer. Gastroenterology 108(2):337–344PubMedCrossRef

16.

McCaughan JS Jr, et al (1996) Photodynamic therapy for esophageal malignancy: a prospective twelve-year study. Ann Thorac Surg 62(4):1005–1009; discussion 1009–1010.

17.

Herbst RS (2004) Review of epidermal growth factor receptor biology. Int J Radiat Oncol Biol Phys 59(2 Suppl):21–26PubMedCrossRef

18.

Yarden Y (2001) The EGFR family and its ligands in human cancer. Signalling mechanisms and therapeutic opportunities. Eur J Cancer 37(Suppl 4):S3–S8

19.

El-Rayes BF, LoRusso PM (2004) Targeting the epidermal growth factor receptor. Br J Cancer 91(3):418–424PubMedCrossRef

20.

Lo HW, Hsu SC, Hung MC (2006) EGFR signaling pathway in breast cancers: from traditional signal transduction to direct nuclear translocalization. Breast Cancer Res Treat 95(3):211–218PubMedCrossRef

21.

Ahmad N, Kalka K, Mukhtar H (2001) In vitro and in vivo inhibition of epidermal growth factor receptor-tyrosine kinase pathway by photodynamic therapy. Oncogene 20(18):2314–2317PubMedCrossRef

22.

Wong TW et al (2003) Photodynamic therapy mediates immediate loss of cellular responsiveness to cytokines and growth factors. Cancer Res 63(13):3812–3818PubMed

23.

Tsai T et al (2009) ALA-PDT results in phenotypic changes and decreased cellular invasion in surviving cancer cells. Lasers Surg Med 41(4):305–315PubMedCrossRef

24.

Bhuvaneswari R et al (2009) Targeting EGFR with photodynamic therapy in combination with Erbitux enhances in vivo bladder tumor response. Mol Cancer 8:94PubMedCrossRef

25.

del Carmen MG et al (2005) Synergism of epidermal growth factor receptor-targeted immunotherapy with photodynamic treatment of ovarian cancer in vivo. J Natl Cancer Inst 97(20):1516–1524PubMedCrossRef

26.

Dimitroff CJ et al (1999) Anti-angiogenic activity of selected receptor tyrosine kinase inhibitors, PD166285 and PD173074: implications for combination treatment with photodynamic therapy. Invest New Drugs 17(2):121–135PubMedCrossRef

27.

Hu CP et al (1984) Biologic properties of three newly established human esophageal carcinoma cell lines. J Natl Cancer Inst 72(3):577–583PubMed

28.

Wuu KD et al (1986) Chromosome analysis on a cell line (CE48T/VGH) derived from a human esophageal carcinoma. Cancer Genet Cytogenet 20(3–4):279–285PubMedCrossRef

29.

Chu YW et al (1997) Selection of invasive and metastatic subpopulations from a human lung adenocarcinoma cell line. Am J Respir Cell Mol Biol 17(3):353–360PubMed

30.

Yang PC et al (1992) Characterization of the mucin differentiation in human lung adenocarcinoma cell lines. Am J Respir Cell Mol Biol 7(2):161–171PubMed

31.

Abu-Ali S, Fotovati A, Shirasuna K (2008) Tyrosine-kinase inhibition results in EGFR clustering at focal adhesions and consequent exocytosis in uPAR down-regulated cells of head and neck cancers. Mol Cancer 7:47PubMedCrossRef

32.

Dussault AA, Pouliot M (2006) Rapid and simple comparison of messenger RNA levels using real-time PCR. Biol Proced Online 8:1–10PubMedCrossRef

33.

Hsieh YJ et al (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

34.

Wang YT et al (2010) An informatics-assisted label-free quantitation strategy that depicts phosphoproteomic profiles in lung cancer cell invasion. J Proteome Res 9(11):5582–5597PubMedCrossRef

35.

Hanlon JG et al (2001) Induction of Hsp60 by Photofrin-mediated photodynamic therapy. J Photochem Photobiol B 64(1):55–61PubMedCrossRef

36.

Woods JA et al (2004) The effect of Photofrin on DNA strand breaks and base oxidation in HaCaT keratinocytes: a comet assay study. Photochem Photobiol 79(1):105–113PubMed

37.

Khanum F, Jain V (1989) Effects of hematoporphyrin derivative on the cellular energy metabolism in the absence and presence of light. Photochem Photobiol 50(5):647–651PubMedCrossRef

38.

Luna MC, Wong S, Gomer CJ (1994) Photodynamic therapy mediated induction of early response genes. Cancer Res 54(5):1374–1380PubMed

39.

Gomer CJ et al (1991) Increased transcription and translation of heme oxygenase in Chinese hamster fibroblasts following photodynamic stress or Photofrin II incubation. Photochem Photobiol 53(2):275–279PubMedCrossRef

40.

Verwanger T et al (2002) Gene expression pattern following photodynamic treatment of the carcinoma cell line A-431 analysed by cDNA arrays. Int J Oncol 21(6):1353–1359PubMed

41.

Nagesh N et al (2010) Effect of ionic strength on porphyrin drugs interaction with quadruplex DNA formed by the promoter region of C-myc and Bcl2 oncogenes. J Nucleic Acids 2010:146418

42.

Wong FH et al (1994) Expression of multiple oncogenes in human esophageal carcinomas. Cancer Invest 12(2):121–131PubMedCrossRef

43.

Boekelheide K et al (1987) Microtubule assembly inhibition by porphyrins and related compounds. Photochem Photobiol 46(5):657–661PubMedCrossRef

44.

Sporn LA, Foster TH (1992) Photofrin and light induces microtubule depolymerization in cultured human endothelial cells. Cancer Res 52(12):3443–3448PubMed

45.

Gomer CJ, Rucker N, Murphree AL (1988) Differential cell photosensitivity following porphyrin photodynamic therapy. Cancer Res 48(16):4539–4542PubMed

46.

Smyth RJ et al (1993) The effects of photofrin on human Tenon's capsule fibroblasts in vitro. J Ocul Pharmacol 9(2):171–178PubMedCrossRef

47.

Chang CJ et al (1997) Pilot in vitro toxicity study of 5-ALA and Photofrin in microvascular endothelial cell cultures. J Clin Laser Med Surg 15(2):83–87PubMed

48.

Dartsch PC, Ischinger T, Betz E (1990) Differential effect of Photofrin II on growth of human smooth muscle cells from nonatherosclerotic arteries and atheromatous plaques in vitro. Arteriosclerosis 10(4):616–624PubMedCrossRef

49.

Hsieh YJ, Yu JS, Lyu PC (2010) Characterization of photodynamic therapy responses elicited in A431 cells containing intracellular organelle-localized Photofrin. J Cell Biochem 111(4):821–833PubMedCrossRef

50.

Kessel D, Oleinick NL (2010) Photodynamic therapy and cell death pathways. Methods Mol Biol 635:35–46PubMedCrossRef

51.

Francois A et al (2011) mTHPC-based photodynamic therapy induction of autophagy and apoptosis in cultured cells in relation to mitochondria and endoplasmic reticulum stress. Int J Oncol 39(6):1537–1543PubMed

52.

Edinger AL, Thompson CB (2004) Death by design: apoptosis, necrosis and autophagy. Curr Opin Cell Biol 16(6):663–669PubMedCrossRef

Title: The effects of Photofrin-mediated photodynamic therapy on the modulation of EGFR in esophageal squamous cell carcinoma cells
Authors: Pei-Wen Yang
Mien-Chie Hung
Ching-Yueh Hsieh
En-Chi Tung
Ying-Hao Wang
Jui-Chang Tsai
Jang-Ming Lee
Publication date: 01-02-2013
Publisher: Springer-Verlag
Published in: Lasers in Medical Science / Issue 2/2013
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI: https://doi.org/10.1007/s10103-012-1119-y

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The effects of Photofrin-mediated photodynamic therapy on the modulation of EGFR in esophageal squamous cell carcinoma cells

Abstract

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Abstract

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