Increased expression of TGF-β1 reduces tumor growth of human U-87 Glioblastoma Cells in vivo

Springer Science and Business Media LLC - Tập 55 - Trang 918-927 - 2005
Jen-Jung Pan1,2,3, Wei-Jen Chang1,4, Tara A. Barone5, Robert J. Plunkett5, Peter T. Ostrow6, Steven J. Greenberg1,2,4
1Department of Neurology, Roswell Park Cancer Institute, Buffalo, USA
2Department of Experimental Pathology, Roswell Park Cancer Institute, Buffalo, USA
3Division of Gastroenterology, Department of Medicine, University of Florida, Gainesville, USA
4Department of Microbiology, State University of New York at Buffalo, Buffalo, (USA)
5Department of Neurosurgery, Roswell Park Cancer Institute, Buffalo, USA
6Department of Pathology, Buffalo General Hospital, Buffalo, USA

Tóm tắt

The role that transforming growth factor β1 (TGF-β1) plays in influencing growth of glioma cells is somewhat controversial. To further understand the potential growth-regulatory effects of TGF-β1,we constructed an animal astroglial tumor model by injecting either wild-type or virally transduced human U-87 glioblastoma cells into nude rat brains. Wild type U-87 cells produced very low amounts of TGF-β1 and were highly tumorigenic. In contrast, U-87 cells transduced to express high levels of TGF-β1 showed reduced tumor size in vivo, in a dose-dependent manner. This reduction in tumor size was not due to either decreased vascularity or increased apoptosis. To test whether TGF-β1 overproduction inhibited tumor growth through an autocrine mechanism, the highest TGF-β1 producing cells were then double transduced with a vector expressing the kinase-truncated type II TGF-β receptor. Cells expressing high levels of truncated TGF-β receptor were less sensitive to TGF-β1 mediated growth inhibition in vitro and produced more aggressive tumors in vivo. The data suggest that the degree of tumorigenicity of the U-87 high-grade glioblastoma cell line may be associated with correspondingly low level of production of TGF-β1. These results also would tend to support the possibility that TGF-β1 may be useful in treating some high-grade gliomas.

Tài liệu tham khảo

Ashley DM, Kong FM, Bigner DD, Hale LP (1998) Endogenous expression of transforming growth factor beta1 inhibits growth and tumorigenicity and enhances Fas-mediated apoptosis in a murine high-grade glioma model. Cancer Res 58:302–309 Ashley DM, Sampson JH, Archer GE, Hale LP, Bigner DD (1998) Local production of TGF beta1 inhibits cerebral edema, enhances TNF-alpha induced apoptosis and improves survival in a murine glioma model. J Neuroimmunol 86:46–52 Attisano L, Wrana JL, Lopez-Casillas F, Massague J (1994) TGF-beta receptors and actions. Biochim Biophys Acta 1222:71–80 Ausubel FM (1995) Short protocols in molecular biology : a compendium of methods from Current protocols in molecular biology. John Wiley & Sons, New York Bodmer S, Strommer K, Frei K, Siepl C, de Tribolet N, Heid I, Fontana A (1989) Immunosuppression and transforming growth factor-beta in glioblastoma. Preferential production of transforming growth factor-beta 2. J Immunol 143:3222–3229 Bottinger EP, Jakubczak JL, Haines DC, Bagnall K, Wakefield LM (1997) Transgenic mice overexpressing a dominant-negative mutant type II transforming growth factor beta receptor show enhanced tumorigenesis in the mammary gland and lung in response to the carcinogen 7,12-dimethylbenz-[a]-anthracene. Cancer Res 57:5564–5570 Branle F, Lefranc F, Camby I, Jeuken J, Geurts-Moespot A, Sprenger S, Sweep F, Kiss R, Salmon I (2002) Evaluation of the efficiency of chemotherapy in in vivo orthotopic models of human glioma cells with and without 1p19q deletions and in C6 rat orthotopic allografts serving for the evaluation of surgery combined with chemotherapy. Cancer 95:641–655 Brooks WH, Netsky MG, Normansell DE, Horwitz DA (1972) Depressed cell-mediated immunity in patients with primary intracranial tumors. Characterization of a humoral immunosuppressive factor. J Exp Med 136:1631–1647 Buckner JC, Burch PA, Cascino TL, O’Fallon JR, Scheithauer BW (1998) Phase II trial of recombinant interferon-alpha-2a and eflornithine in patients with recurrent glioma. J Neurooncol 36:65–70 Fakhrai H, Dorigo O, Shawler DL, Lin H, Mercola D, Black KL, Royston I, Sobol RE (1996) Eradication of established intracranial rat gliomas by transforming growth factor beta antisense gene therapy. Proc Natl Acad Sci U S A 93:2909–2914 Fink SP, Swinler SE, Lutterbaugh JD, Massague J, Thiagalingam S, Kinzler KW, Vogelstein B, Willson JK, Markowitz S (2001) Transforming growth factor-beta-induced growth inhibition in a Smad4 mutant colon adenoma cell line. Cancer Res 61:256–260 Folkman J (1974) Proceedings: Tumor angiogenesis factor. Cancer Res 34:2109–2113 Folkman J (1975) Tumor angiogenesis: a possible control point in tumor growth. Ann Intern Med 82:96–100 Fontana A, Hengartner H, de Tribolet N, Weber E (1984) Glioblastoma cells release interleukin 1 and factors inhibiting interleukin 2-mediated effects. J Immunol 132:1837–1844 Franzen P, ten Dijke P, Ichijo H, Yamashita H, Schulz P, Heldin CH, Miyazono K (1993) Cloning of a TGF beta type I receptor that forms a heteromeric complex with the TGF beta type II receptor. Cell 75:681–692 Fueyo J, Alemany R, Gomez-Manzano C, Fuller GN, Khan A, Conrad CA, Liu TJ, Jiang H, Lemoine MG, Suzuki K, Sawaya R, Curiel DT, Yung WK, Lang FF (2003) Preclinical characterization of the antiglioma activity of a tropism-enhanced adenovirus targeted to the retinoblastoma pathway. J Natl Cancer Inst 95:652–660 Gimbrone MA, Jr., Leapman SB, Cotran RS, Folkman J (1972) Tumor dormancy in vivo by prevention of neovascularization. J Exp Med 136:261–276 Herzer K, Ganten TM, Schulze-Bergkamen H, Grosse-Wilde A, Koschny R, Krammer PH, Walczak H (2005) Transforming growth factor beta can mediate apoptosis via the expression of TRAIL in human hepatoma cells. Hepatology 42:183–192 Horst HA, Scheithauer BW, Kelly PJ, Kovach JS (1992) Distribution of transforming growth factor-beta 1 in human astrocytomas. Hum Pathol 23:1284–1288 Ikeda T, Lioubin MN, Marquardt H (1987) Human transforming growth factor type beta 2: production by a prostatic adenocarcinoma cell line, purification, and initial characterization. Biochemistry 26:2406–2410 Jennings MT, Pietenpol JA (1998) The role of transforming growth factor beta in glioma progression. J Neurooncol 36:123–140 Kiefer R, Supler ML, Toyka KV, Streit WJ (1994) In situ detection of transforming growth factor-beta mRNA in experimental rat glioma and reactive glial cells. Neurosci Lett 166:161–164 Kikuchi K, Neuwelt EA (1983) Presence of immunosuppressive factors in brain-tumor cyst fluid. J Neurosurg 59:790–799 Kim SJ, Park K, Koeller D, Kim KY, Wakefield LM, Sporn MB, Roberts AB (1992) Post-transcriptional regulation of the human transforming growth factor-beta 1 gene. J Biol Chem 267:13702–13707 Kirsch M, Strasser J, Allende R, Bello L, Zhang J, Black PM (1998) Angiostatin suppresses malignant glioma growth in vivo. Cancer Res 58:4654–4659 Klagsbrun M, Knighton D, Folkman J (1976) Tumor angiogenesis activity in cells grown in tissue culture. Cancer Res 36:110–114 Lawrence DA (1995) Transforming growth factor-beta: an overview. Kidney Int Suppl 49:S19–S23 Le Pabic H, Bonnier D, Wewer UM, Coutand A, Musso O, Baffet G, Clement B, Theret N (2003) ADAM12 in human liver cancers: TGF-beta-regulated expression in stellate cells is associated with matrix remodeling. Hepatology 37:1056–1066 Lin HY, Moustakas A (1994) TGF-beta receptors: structure and function. Cell Mol Biol (Noisy-le-grand) 40:337–349 Lin HY, Wang XF, Ng-Eaton E, Weinberg RA, Lodish HF (1992) Expression cloning of the TGF-beta type II receptor, a functional transmembrane serine/threonine kinase. Cell 68:775–785 Mahaley MS Jr, Brooks WH, Roszman TL, Bigner DD, Dudka L, Richardson S (1977) Immunobiology of primary intracranial tumors. Part 1: studies of the cellular and humoral general immune competence of brain-tumor patients. J Neurosurg 46:467–476 Massague J (1990) The transforming growth factor-beta family. Annu Rev Cell Biol 6:597–641 Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press, San Diego Prophet EB (1992) Laboratory methods in histotechnology. American Registry of Pathology, Washington Romeo DS, Park K, Roberts AB, Sporn MB, Kim SJ (1993) An element of the transforming growth factor-beta 1 5’-untranslated region represses translation and specifically binds a cytosolic factor. Mol Endocrinol 7:759–766 Roszman TL, Brooks WH (1980) Immunobiology of primary intracranial tumours. III. Demonstration of a qualitative lymphocyte abnormality in patients with primary brain tumours. Clin Exp Immunol 39:395–402 Samoto K, Ikezaki K, Ono M, Shono T, Kohno K, Kuwano M, Fukui M (1995) Expression of vascular endothelial growth factor and its possible relation with neovascularization in human brain tumors. Cancer Res 55:1189–1193 Samuels V, Barrett JM, Bockman S, Pantazis CG, Allen MB, Jr. (1989) Immunocytochemical study of transforming growth factor expression in benign and malignant gliomas. Am J Pathol 134:894–902 Schwyzer M, Fontana A (1985) Partial purification and biochemical characterization of a T cell suppressor factor produced by human glioblastoma cells. J Immunol 134:1003–1009 Scotto L, Assoian RK (1993) A GC-rich domain with bifunctional effects on mRNA and protein levels: implications for control of transforming growth factor beta 1 expression. Mol Cell Biol 13:3588–3597 Sporn MB, Roberts AB (1985) Autocrine growth factors and cancer. Nature 313:745–747 Stiles JD, Ostrow PT, Balos LL, Greenberg SJ, Plunkett R, Grand W, Heffner RR Jr (1997) Correlation of endothelin-1 and transforming growth factor beta 1 with malignancy and vascularity in human gliomas. J Neuropathol Exp Neurol 56:435–439 Tada T, Yabu K, Kobayashi S (1993) Detection of active form of transforming growth factor-beta in cerebrospinal fluid of patients with glioma. Jpn J Cancer Res 84:544–548 Teicher BA (2001) Malignant cells, directors of the malignant process: role of transforming growth factor-beta. Cancer Metastasis Rev 20:133–143 Wakefield LM, Roberts AB (2002) TGF-beta signaling: positive and negative effects on tumorigenesis. Curr Opin Genet Dev 12:22–29 Witham TF, Villa L, Yang T, Pollack IF, Okada H, Robbins PD, Chambers WH (2003) Expression of a soluble transforming growth factor-beta (TGFbeta) receptor reduces tumorigenicity by regulating natural killer (NK) cell activity against 9L gliosarcoma in vivo. J Neurooncol 64:63–69 Yamada N, Kato M, Yamashita H, Nister M, Miyazono K, Heldin CH, Funa K (1995) Enhanced expression of transforming growth factor-beta and its type-I and type-II receptors in human glioblastoma. Int J Cancer 62:386–392 Yingling JM, Wang XF, Bassing CH (1995) Signaling by the transforming growth factor-beta receptors. Biochim Biophys Acta 1242:115–136