Abstract
Photodynamic therapy (PDT) could be a useful adjuvant in glioblastoma treatment. The fact that epidermal growth factor (EGF) and its receptor are involved in glioblastoma growth control led us to investigate the relationships between EGF and PDT with respect to three different glioma cell lines (C6, T98 G, U87 MG) responsive to growth stimulation by EGF. Flow cytometric analysis revealed that each cell line expressed EGF receptors. PDT was then applied to the cells using haematoporphyrin derivative (HPD) as photosensitizer and argon laser irradiation. When cells were incubated for 2 h with HPD (0.1–10 μg/ml) and then laser-irradiated (λ = 514 nm; energy density 25 J/cm2), all three cell lines showed photosensitivity. The median lethal dose was respectively 3, 4.5 and 2.7 μg/ml for C6, T98 G and U87 MG. EGF (2–50 ng/ml) had no effect on HPD- and laser-induced toxicity when added to cells before PDT, whereas toxicity decreased for all three cell lines when EGF was added after PDT. HPD (1–2 μg/ml, incubation times 30–180 min) also induced an increase in EGF receptor expression for the C6 line.
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Adachi K, Belser P, Bender H, Li D, Rodeck U, Benveniste EN, Woo D, Schmiegel WH, Herlyn D (1992) Enhancement of epidermal growth factor receptor expression on glioma cells by recombinant tumor necrosis factor alpha. Cancer Immunol Immunother 34: 370–376
Bellot F, Moolenar W, Kris R, Mirakhur B, Verlaan I, Ullrich A, Schlessinger J, Felder S (1990) High-affinity epidermal growth factor binding is specifically reduced by a monoclonal antibody and appears necessary for early responses. J Cell Biol 110: 491–502
Berkers JAM, Van Bergen en Henegouwen PMP, Boonstra J (1991) Three classes of epidermal growth factor receptors on HeLa cells. J Biol Chem 266: 922–927
Blagoveshchenskaia AD, Sokolova IP, Kornilova ES, Nikol’skii NN (1994) The dependence of the endocytosis of the epidermal growth factor receptors on the degree of receptor occupancy. Tsitologiia 36: 664–674
Carpenter G, Cohen S (1976) 125I-Labeled human epidermal growth factor: binding, internalisation and degradation in human fibroblasts. J Cell Biol 71: 159–171
Chaffanet M, Chauvin C, Laine M, Berger F, Chedin M, Rost N, Nissou MF, Benebid AL (1992) EGF receptor amplification and expression in human brain tumours. Eur J Cancer 28: 11–17
Davis C, Western A, Lindmo T, Moan J (1986) Changes in antigen expression on human melanoma cells after exposure to photoactivated hematoporphyrin derivative. Cancer Res 46: 60–68
Diamond I, Granelli SG, McDonagh AF, Nielsen S, Wilson CB, Jaenicke R (1972) Photodynamic therapy of malignant tumors. Lancet 2: 1175–1177
Dougherty TJ (1986) Photosensitization of malignant tumors. J Surg Oncol 2: 24–37
Fingar VH, Wieman J, Doak KW (1990) Role of thromboxane and prostaglandin release on photodynamic therapy induced tumour destruction. Cancer Res 50: 2599–2603
Fukuyama R, Minoshima S, Ochiai A, Tahara E, Shimizu N (1991) Flow cytometric analysis of the expression of 9A3 antigen, E-cadherin and EGF receptor in TMK-1 stomach cancer cells. Int J Cancer 48: 81–84
Gamou S, Shimizu N (1987) Change in metabolic turnover is an alternate mechanism increasing cell surface epidermal growth factor receptor levels in tumor cells. J Biol Chem 262: 6708–6713
Glinski JA, David E, Warren TC, Hansen G, Leonard SF, Pitner P, Pav S, Arvigo R, Balick MJ, Panti E, Grob PM (1995) Inactivation of cell surface receptors by pheophorbide a, a green pigment isolated from Psychotria acuminata. Photochem Photobiol 62: 144–150
Gregorie HB (1968) Hematoporphyrin derivative fluorescence in malignant neoplasms. Ann Surg 167: 820
Hemming AW, Davis NL, Dubois B, Quenville NF, Finley RJ (1993) Photodynamic therapy of squamous cell carcinoma: an evaluation of a new photosensitizing agent, benzoporphyrin derivative, and new photoimmunoconjugate. Surg Oncol 2: 187–196
Hirai M, Gamou S, Minoshima S, Shimizu N (1988) Two independent mechanisms for escaping epidermal growth factor-mediated growth inhibition in epidermal growth factor receptor hyperproducing human tumor cells. J Cell Biol 107: 791–799
Hoi Sang U, Espiritu OD, Kelley PY, Klauber MR, Hatton JD (1995) The role of the epidermal growth factor receptor in human gliomas. I. The control of cell growth. J Neurosurg 82: 841–846
Hurtt MR, Moossy J, Donovan-Peluso M, Locker J (1992) Amplification of epidermal growth factor receptor gene in gliomas: histopathology and prognosis. J Neuropathol Exp Neurol 51: 84–90
Kaye AH, Hill JS (1993) Photodynamic therapy of brain tumours. Ann Acad Med Singapore 22: 470–481
Kaye AH, Morstyn G (1987) Photoradiation therapy causing selective tumor kill in a rat glioma model. Neurosurgery 20: 408–415
Kessel D (1986) Photosensitization with derivatives of haematoporphyrin. Int J Radiat Biol 49: 901–907
Kostron H, Fritsch E, Grunert V (1988) Photodynamic therapy of malignant brain tumors: a phase I–II trial. Br J Neurosurg 2: 241–248
Lajat Y, Patrice T (1987) Photochemotherapy applied stereotactically to brain tumors. Surg Neurol 11: 14
Leunig A, Staub F, Peters J, Leiderer R, Feyh J, Goetz A (1994) Damage to tumor cells by photodynamic therapy. Laryngorhinootologie 73: 102–107
Miller CC, Hale P, Pentland AP (1994) Ultraviolet B injury increases prostaglandin synthesis through a tyrosine kinase-dependent pathway: evidence for UVB-induced epidermal growth factor receptor activation. J Biol Chem 269: 3529–3533
Murphy S, Welk G, Thwin SS (1990) Stimulation of thromboxane release from primary cell cultures derived from human astrocytic glioma biopsies. Glia 3: 205–211
Noske DP, Wolbers JG, Sterenborg HJCM (1991) Photodynamic therapy of malignant glioma: a review of literature. Clin Neurol Neurosurg 93: 293–307
Palombella VJ, Yamashiro DJ, Maxfield FR, Decker SJ, Vilcek J (1987) Tumor necrosis factor increases the number of epidermal growth factor receptors on human fibro-blasts. J Biol Chem 262: 1950–1954
Perria C, Capuzzo T, Cavagnaro G (1980) First attempts at the photodynamic treatment of human gliomas. J Neurosurg Sci 24: 119–129
Perria C, Carai M, Falzoi A (1988) Photodynamic therapy of malignant brain tumors: clinical results of, difficulties with, questions about, and future prospects for the neurosurgical applications. Neurosurgery 23: 557–563
Pollack IF, Randall MS, Kristofik MP, Kelly RH, Selker RG, Vertosick FT (1990) Response of malignant glioma cell lines to epidermal growth factor and platelet-derived growth factor in a serum-free medium. J Neurosurg 73: 106–112
Powers SK, Cusch SS, Walstad DL, Kwock L (1991) Stereotactic intratumoral photo-dynamic therapy for recurrent malignant brain tumors. Neurosurgery 29: 688–696
Pulver M, Zuber P, de Tribolet N (1987) Immonubiologie de l’astrocyte normal et tumoral. Rev Neurol 143: 711–721
Reifenberger J, Ring GU, Gies U, Cobbers L, Oberstrass J, An HX, Niederacher D, Wechsler W, Reifenberger G (1996) Analysis of p53 mutation and epidermal growth factor receptor amplification in recurrent gliomas with malignant progression. J Neuropathol Exp Neurol 55: 822–831
Sauter G, Maeda T, Waldman FM, Davis RL, Feuerstein BG (1996) Patterns of epidermal growth factor receptor amplification in malignant gliomas. Am J Pathol 148: 1047–1053
Schick E, Kaufmann R, Ruck A, Hainzl A, Boehncke WH (1995) Influence of activation and differentiation of cells on the effectiveness of photodynamic therapy. Acta Derm Venereol 75: 276–279
Schlegel J, Merdes A, Stumm G, Albert FK, Forsting M, Hynes N, Kiessling M (1994) Amplification of the epidermal growth factor receptor gene correlates with different growth behaviour in human glioblastoma. Int J Cancer 56: 72–77
Shapiro JR (1986) Biology of gliomas: heterogeneity, oncogenes, growth factors. Semin Oncol 13: 4–15
St-Pierre PR, Petersen NO (1992) Average density and size of microclusters of epidermal growth factor receptors on A431 cells. Biochemistry 31: 2459–2463
Stein GH (1979) T98G: an anchorage independent human tumor cell line that exhibits stationary phase G1 arrest in vitro. J Cell Physiol 99: 43–54
Tuzi NL, Venter DJ, Kumar S, Staddon SL, Lemoine NR, Gullick WJ (1991) Expression of growth factor receptors in human brain tumors. Br J Cancer 63: 227–233
Vonarx-Coinsmann V (1994) Photochimiothérapie et immunité cellulaire spécifique. Doctoral dissertation, University of Nantes, France
Werner MH, Humphrey PA, Bigner DD, Bigner SH (1988) Growth effects of epidermal growth factor and a monoclonal antibody against the EGF receptor on four glioma cell lines. Acta Neuropathol 77: 196–201
Wharen RE, So S, Anderson RE, Laws ER (1986) Hematoporphyrin derivative photo-cytotoxicity of human glioblastoma in cell culture. Neurosurgery 19: 495–501
Wikstrand CJ, Hale LP, Batra SK, Hill ML, Humphrey PA, Kurpad SN, McLendon RE, Moscatello D, Pegram CN, Reist CJ, Traweek T, Wong AJ, Zalutsky MR, Bigner DD (1995) Monoclonal antibodies against EGFRvIII are tumor specific and react with breast and lung carcinomas and malignant gliomas. Cancer Res 55: 3140–3148
Youle RJ (1996) Immunotoxins for central nervous system malignancy. Semin Cancer Biol 7: 65–70
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Fanuel-Barret, D., Patrice, T., Foultier, MT. et al. Influence of epidermal growth factor on photodynamic therapy of glioblastoma cells in vitro. Res. Exp. Med. 197, 219–233 (1997). https://doi.org/10.1007/s004330050071
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DOI: https://doi.org/10.1007/s004330050071