Estrogen increases survival in an orthotopic model of glioblastoma

Journal of Neuro-Oncology

Volumn 95, Issue 1, 2009, Pages 37-48

  Barone, Tara A ^a   Gorski, Justin W ^a   Greenberg, Steven J ^c   Plunkett, Robert J ^a,b  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c Neurology Global Clinical Development   (United States)

Author keywords

Estradiol; Gender; Glioblastoma; Nuderat; Survival

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR; PLACEBO;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER SURVIVAL; CELL PROLIFERATION; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG MEGADOSE; ESTROGEN ACTIVITY; FEMALE; GLIOBLASTOMA; HUMAN; HUMAN CELL; MALE; NONHUMAN; RAT; SEX DIFFERENCE; TUMOR GROWTH;

ANIMALS; APOPTOSIS; ASTROCYTES; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DISEASE MODELS, ANIMAL; ESTRADIOL; FEMALE; GLIOBLASTOMA; HUMANS; IMMUNOGLOBULIN G; MALE; MELPHALAN; MICROGLIA; NEOPLASM TRANSPLANTATION; OVARIECTOMY; RATS; RATS, NUDE; RECEPTORS, ESTROGEN; SURVIVAL ANALYSIS; TIME FACTORS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 70349339042     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-009-9904-6     Document Type: Article

References (65)

1. Claus EB, Black PM (2006) Survival rates and patterns of care for patients diagnosed with supratentorial low-grade gliomas: Data from the SEER program, 1973-2001. Cancer 106(6):1358-1363. doi: 10.1002/cncr.21733
2. Hirano H, Asakura T, Yokoyama S et al (1996) The prognostic factors in astrocytic tumors: Analysis by the Kaplan-Meier method and the Weibull log-linear model. No Shinkei Geka 24:809-815 (in Japanese)
3. Plunkett R, Barone T, McCarthy B et al (1998) Influence of gender on survival of patients with glioma: Analysis of the SEER database. J Neurooncol 39:272 Abstract
4. Roth JG, Elvidge AR (1960) Glioblastoma multiforme: A clinical survey. J Neurosurg 17:736-750
5. Tseng MY, Tseng JH (2005) Survival analysis for adult glioma in England and Wales. J Formos Med Assoc 104(5):341-348
6. Hatch EE, Linet MS, Zhang J et al (2005) Reproductive and hormonal factors and risk of brain tumors in adult females. Int J Cancer 114(5):797-805. doi: 10.1002/ijc.20776
7. Huang K, Whelan EA, Ruder AM et al (2004) Reproductive factors and risk of glioma in women. Cancer Epidemiol Biomarkers Prev 13(10):1583-1588
8. Garman RH, Snellings WM (1986) Frequency, size and location of brain tumours in F-344 rats chronically exposed to ethylene oxide. Food Chem Toxicol 24:145-153. doi: 10.1016/0278-6915(86)90349-2
9. Gopinath C (1986) Spontaneous brain tumours in Sprague-Dawley rats. Food Chem Toxicol 24:113-120. doi: 10.1016/0278-6915(86)90345-5
10. Lee Y, Bullard DE, Humphrey PA et al (1988) Treatment of intracranial human xenographs with 131 I-labeled anti-tenascin monoclonal antibody 81C6. Cancer Res 48:2904-2910
11. Verzat C, Delisle M-B, Courriere P et al (1990) Influence of host sex on the growth of a human glioblastoma cell line in athymic mice. Neuropathol Appl Neurobiol 16:141-151. doi: 10.1111/ j.1365-2990.1990.tb00943.x
12. Plunkett RJ, Lis A, Barone TA et al (1999) Hormonal effects on glioblastoma multiforme in the nude rat model. J Neurosurg 90:1072-1077
13. Feigelson HS, Henderson BE (1996) Estrogens and breast cancer. Carcinogensis 17:2279-2284. doi: 10.1093/carcin/17.11.2279
14. Ito K, Utsunomiya H, Yaegashi N et al (2007) Biological roles of estrogen and progesterone in human endometrial carcinoma-new developments in potential endocrine therapy for endometrial cancer. Endocr J 54(5):667-679. doi: 10.1507/endocrj.KR-114
15. Korhonen K, Salminen T, Raitanen J et al (2006) Female predominance in meningiomas can not be explained by differences in progesterone, estrogen, or androgen receptor expression. J Neurooncol 80:1-7. doi: 10.1007/s11060-006-9146-9
16. Gibson CL, Gray LJ, Murphy SP et al (2006) Estrogens and experimental ischemic stroke: A systematic review. J Cereb Blood Flow Metab 26:1103-1113
17. El-Etr M, Vukusic S, Gignoux L et al (2005) Steroid hormones in multiple sclerosis. J Neurol Sci 233:49-54. doi: 10.1016/j.jns.2005.03.004
18. Simpkins JW, Green PS, Gridley KE et al (1997) Role of estrogen replacement therapy in memory enhancement and the prevention of neuronal loss associated with Alzheimer's disease. Am J Med 103:19S-25S. doi: 10.1016/S0002-9343(97)00260-X
19. Rangonese P, D'Amelio M, Savettieri G (2006) Implications for estrogens in Parkinson's disease: An epidemiological approach. Ann N Y Acad Sci 1089:373-382. doi: 10.1196/annals.1386.004
20. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, 4th edn. Academic Press, San Diego
21. Blankenstein MA, Broerse JJ, de Vries JB et al (1977) The effect of subcutaneous administration of oestrogens on plasma oestrogen levels and tumor incidence in female rats. Eur J Cancer 13:1437-1443. doi: 10.1016/ 0014-2964(77)90158-X
22. Goth MI, Lyons CE Jr, Ellwood MR et al (1996) Chronic estrogen treatment in male rats reveals mammosomatotropes and allows inhibition of prolactin secretion by somatostatin. Endocrinology 137:274-280. doi: 10.1210/en.137.1.274
23. Lundeen SG, Carver JM, McKean M-L et al (1997) Charaterization of the ovariectomized rat model for the evaluation of estrogen effects on plasma cholesterol levels. Endocrinology 138:1552-1558. doi: 10.1210/ en.138.4.1552
24. Sumi C, Yokoro K, Matsushima R (1984) Effects of 17β-estradiol and diethylstilbestrol on concurrent development of hepatic, mammary, and pituitary tumors in WF rats: Evidence for differential effect on liver. J Natl Cancer Inst 73:1229-1234
25. Yague JG, Lavaque E, Carretero J et al (2004) Aromatase, the enzyme responsible for estrogen biosynthesis, is expressed by human and rat glioblastomas. Neurosci Lett 368(3):279-284. doi: 10.1016/ j.neulet.2004.07.010
26. Morissette M, Levesque D (1990) A physiological dose of estradiol with progesterone affects striatum biogenic amines. Can J Physiol Pharmacol 68:1520-1526
27. Rossouw JE, Anderson GL, Johnson KC et al (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: Principal results from the Women's Health Initiative randomized controlled trial. JAMA 288(3):321-333. doi: 10.1001/jama.288.3.321
28. Zhu BT, Conney AH (1998) Functional role of estrogen metabolism in target cells: Review and perspectives. Carcinogenesis 19:1-27. doi: 10.1093/carcin/19.1.1
29. Fishman J, Bradlow HL, Schneider J et al (1980) Radiometric analysis of biological oxidations in man: Sex differences in estradiol metabolism. Proc Natl Acad Sci USA 77:4957-4960. doi: 10.1073/pnas.77.8.4957
30. 3 H]17β-oestradiol in rats: male-specific 15α-and male-selective 16α-hydroxylation and female-selective catechol formation. J Steroid Biochem Mol Biol 42:65-76. doi: 10.1016/0960-0760(92)90012-8
31. Morissette M, Garcia-Segura L-M, Belanger A et al (1992) Changes in rat striatal neuronal membrane morphology and steroid content during the estrous cycle. Neuroscience 49:893-902. doi: 10.1016/0306-4522(92)90365-9
32. Pardridge WM, Moeller TL, Mietus LJ, et al (1980) Blood-brain barrier transport and brain sequestration of steroid hormones. Am J Physiol 239 (Endocrinol Metab 2):E96-E102
33. Ball P, Haupt M, Knuppen R (1978) Comparative studies on the metabolism of oestradiol in the brain, the pituitary and the liver of the rat. Acta Endocrinol (Copenh) 87:1-11
34. Kaplan GP, Hartman BK, Creveling CR (1979) Immunohistochemical demonstration of catechol-O-methyltransferase in mammalian brain. Brain Res 167:241-250. doi: 10.1016/0006-8993(79)90819-9
35. Masuda M, Tsunoda M, Imai K (2003) High-performance liquid chromatography-fluorescent assay of catechol-O-methyltransferase activity in the brain. Anal Bioanal Chem 376(7):1069-1073. doi: 10.1007/ s00216-003-2025-8
36. Redell JB, Dash PK (2006) Traumatic brain injury stimulates hippocampal catechol-O-methyltransferase expression in microglia. Neurosci Lett 413(1):36-41. doi: 10.1016/j.neulet.2006.11.060
37. Helkamaa T, Reenila I, Tuominen RK et al (2007) Increased catechol-O-methyltransferase activity and protein expression in OX-42 positive cells in substantia nigra after lipopolysaccharide microinfusion. Neurochem Int 51(6-7):412-423. doi: 10.1016/ j.neuint.2007.04.020
38. Lis A, Ciesielski MJ, Barone TA et al (2004) 2-methoxyestradiol inhibits proliferation of normal and neoplastic glial cells, and induces cell death, in vitro. Cancer Lett 213(1):57-65. doi: 10.1016/ j.canlet.2004.04.021
39. Kang SH, Cho HT, Devi S et al (2006) Antitumor effect of 2-methoxyestradiol in a rat orthotopic brain tumor model. Cancer Res 66(24):11991-11997. doi: 10.1158/0008-5472.CAN-06-1320
40. Nagashima G, Suzuki R, Asai J et al (2002) Immunohistochemical analysis of reactive astrocytes around glioblastoma: An immunohistochemical study of postmortem glioblastoma cases. Clin Neurol Neurosurg 104(2):125-131. doi: 10.1016/S0303-8467(01)00197-4
41. Azcoitia I, Sierra A, Garcia-Segura LM (1999) Localization of estrogen receptor β-immunoreactivity in astrocytes of the adult rat brain. Glia 26:260-267. doi: 10.1002/ (SICI)1098-1136(199905)26:3<260::AID-GLIA7>3.0.CO;2-R
42. Milner TA, McEwen BS, Hayashi S et al (2001) Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J Comp Neurol 429(3):355-371. doi: 10.1002/ 1096-9861(20010115)429:3<355::AID-CNE1>3.0.CO;2-#
43. Santagati S, Melcangi RC, Celotti F et al (1994) Estrogen receptor is expressed in different types of glial cells in culture. J Neurochem 63:2058-2064
44. Dhandapani KM, Wade FM, Mahesh VB et al (2005) Astocyte-derived transforming growth factor-β mediates the neuroprotective effects of 17β-estradiol: Involvement of nonclassical genomic signaling pathways. Endocrinology 146(6):2749-2759. doi: 10.1210/en.2005-0014
45. Pan JJ, Chang WJ, Barone TA et al (2006) Increased expression of TGF-β1 reduces tumor growth of human U-87 glioblastoma cells in vivo. Cancer Immunol Immunother 55(8):918-927. doi: 10.1007/ s00262-005-0083-9
46. Johnson EA, Svetlov SI, Pike BR et al (2004) Cell-specific upregulation of survivin after experimental traumatic brain injury in rats. J Neurotrauma 21(9):1183-1195. doi: 10.1089/neu.2004.21.1183
47. Moggs JG, Murphy TC, Lim FL et al (2005) Anti-proliferative effect of estrogen in breast cancer cells that re-express ERalpha is mediated by abberant regulation of cell cycle genes. J Mol Endocrinol 34(2):535-551. doi: 10.1677/jme.1.01677
48. Nakayama Y, Sakamoto H, Satoh K et al (2000) Tamoxifen and gonadal steroids inhibit colon cancer growth in association with inhibition of thymidylate synthase, survivin and telomerase expression through estrogen receptor beta mediated system. Cancer Lett 161(1):63-71. doi: 10.1016/S0304-3835(00)00600-5
49. Le DM, Besson A, Fogg DK et al (2003) Exploitation of astrocytes by glioma cells to facilitate invasiveness: A mechanism involving matrix metalloproteinase-2 and the urokinase-type plasminogen activator-plasmin cascade. J Neurosci 23(10):4034-4043
50. Liu R, Wen Y, Perez E et al (2005) 17 beta-estradiol attenuates blood-brain barrier disruption induced by cerebral ischemia-reperfusion injury in female rats. Brain Res 1060(1-2):55-61. doi: 10.1016/ j.brainres.2005.08.048
51. Puli S, Lai JCK, Bhushan A (2006) Inhibition of matrix degrading enzymes and invasion in human glioblastoma (U87MG) cells by isoflavones. J Neuro-onc 79:135-142. doi: 10.1007/s11060-006-9126-0
52. Graeber MB, Scheithauer BW, Kreutzberg GW (2002) Microglia in brain tumors. Glia 40:252-259. doi: 10.1002/glia.10147
53. Liu X, Fan XL, Zhao Y et al (2005) Estrogen provides neuroprotection against activated microglia-induced dopaminergic neuronal injury through both estrogen receptor-alpha and estrogen receptor-beta in microglia. J Neurosci Res 81(5):653-665. doi: 10.1002/jnr.20583
54. Vegeto E, Bonincontro C, Pollio G et al (2001) Estrogen prevents the lipopolysaccharide-induced inflammatory response in microglia. J Neurosci 21(6):1809-1818
55. Baker AE, Brautigam VM, Watters JJ (2004) Estrogen modulates microglial inflammatory mediator production via interactions with estrogen receptor β. Endocrinology 145(11):5021-5032. doi: 10.1210/en.2004-0619
56. Goswami S, Gupta A, Sharma SK (1998) Interleukin-6-mediated autocrine growth promotion in human glioblastoma multiforme cell line U87MG. J Neurochem 71:1837-1845
57. Chang CY, Li MC, Liao SL et al (2005) Prognostic and clinical implications of IL-6 expression in glioblastoma multiforme. J Clin Neurosci 12(8):930-933. doi: 10.1016/j.jocn.2004.11.017
58. Samaras V, Piperi C, Korkolopoulou P et al (2007) Application of the ELISPOT method for comapartive analysis of interleukin (IL)-6 and IL-10 secretion in peripheral blood of patients with astroglial tumors. Mol Cell Biochem 304(1-2):343-351. doi: 10.1007/s11010-007-9517-3
59. Straub RH (2007) The complex role of estrogens in inflammation. Endocr Rev 28(5):521-574. doi: 10.1210/er.2007-0001
60. Yamini B, Yu X, Gillespie GY et al (2004) Transcriptional targeting of adenovirally delivered tumor necrosis factor α by temozolomide in experimental glioblastoma. Cancer Res 64:6381-6384. doi: 10.1158/ 0008-5472.CAN-04-2117
61. Davoust N, Vuaillat C, Androdias G et al (2008) From bone marrow to microglia: Barriers and avenues. Trends Immunol 29(5):227-234. doi: 10.1016/j.it.2008.01.010
62. Vegeto E, Belcredito S, Etteri S et al (2003) Estrogen receptor-α mediates the brain anti-inflammatory activity of estradiol. Proc Natl Acad Sci USA 100(16):9614-9619. doi: 10.1073/pnas.1531957100
63. Vegeto E, Ghisletti S, Meda C et al (2004) Regulation of the lipopolysaccharide signal transduction pathway by 17γ-estradiol in macrophage cells. J Steroid Biochem Mol Biol 91:59-66. doi: 10.1016/ j.jsbmb.2004.02.004
64. Camphausen K, Purow B, Sproull M et al (2005) Influence of in vivo growth on human glioma cell line gene expression: Convergent profiles under orthotopic conditions. Proc Natl Acad Sci USA 102(23):8287-8292. doi: 10.1073/pnas.0502887102
65. Batistatou A, Kyzas PA, Goussia A et al (2006) Estrogen receptor beta (ERγ) protein expression correlates with BAG-1 and prognosis in brain glial tumours. J Neuro-onc 77:17-23. doi: 10.1007/s11060-005-9005-0