2-Methoxyestradiol induces spindle aberrations, chromosome congression failure, and nondisjunction in mouse oocytes

Biology of Reproduction

Volumn 76, Issue 5, 2007, Pages 784-793

  Eichenlaub Ritter, Ursula ^a   Winterscheidt, Ulrike ^a   Vogt, Edgar ^a   Shen, Ying ^a,b   Tinneberg, Hans Rudolf ^b   Sorensen, Ralph ^a,c  

^a BIELEFELD UNIVERSITY   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c GETTYSBURG COLLEGE   (United States)

Author keywords

Environment; Estradiol; Meiosis; Oocyte development; Toxicology

Indexed keywords

2 METHOXYESTRADIOL; CATECHOL ESTROGEN; CELL CYCLE PROTEIN; CENTRIN; ESTRADIOL; PROTEIN MAD2L1; TUBULIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; C BANDING; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CENTROSOME; CHROMOSOME ABERRATION; CHROMOSOME STRUCTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DOSE RESPONSE; ENVIRONMENTAL EXPOSURE; ESTROGEN ACTIVITY; IMMUNOFLUORESCENCE; IN VITRO STUDY; MEIOSIS; METAPHASE; MICROTUBULE ASSEMBLY; MITOSIS SPINDLE; MOUSE; NONDISJUNCTION; NONHUMAN; OOCYTE MATURATION; POLARIZATION MICROSCOPY; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANEUPLOIDY; ANIMALS; CELL CYCLE PROTEINS; CHROMOSOME ABERRATIONS; CHROMOSOME SEGREGATION; CHROMOSOMES; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; MEIOSIS; METAPHASE; MICE; MITOTIC SPINDLE APPARATUS; NONDISJUNCTION, GENETIC; NUCLEAR PROTEINS; OOCYTES; PREGNANCY; TUBULIN;

MAMMALIA;

EID: 34247513489     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.106.055111     Document Type: Article

References (87)

1. Tsuchiya Y, Nakajima M, Yokoi T. Cytochrome P450-mediated metabolism of estrogens and its regulation in human. Cancer Lett 2005; 227:115-124.
2. Silberzahn P, Almahbobi GH, Dehennin L, Merouane A. Estrogen metabolites in equine ovarian follicles: gas chromatographic-mass spectrophotometric determinations in relation to follicular ultrastructure and progestin content. Steroid Biochem 1985; 22:501-505.
3. Berg FD, Kuss E. Urinary excretion of catecholestrogens, 2-methoxyestrogens and "classical estrogens" throughout the normal menstrual cycle. Arch Gynecol Obstet 1991; 249:201-207.
4. Hammond JM, Hersey RM, Walega MA, Weisz J. Catecholestrogen production by porcine ovarian cells. Endocrinology 1986; 118:2292-2299.
5. Shang W, Konidari I, Schomberg DW. 2-Methoxyestradiol, an endogenous estradiol metabolite, differentially inhibits granulosa and endothelial cell mitosis: a potential follicular antiangiogenic regulator. Biol Reprod 2001; 65:622-627
6. Fotsis T, Zhang Y, Pepper MS, Adlercreutz H, Montesano R, Nawroth PP, Schweigerer L. The endogenous oestrogen metabolite 2-methoxyoestradiol inhibits angiogenesis and suppresses tumour growth. Nature 1994; 368:237-239.
7. Tekpetey FR, Armstrong DT. Catecholestrogen modulation of steroid production by rat luteal cells: mechanism of action. Mol Cell Endocrinol 1994; 101:49-57.
8. Spicer LJ, Hammond JM. Catecholestrogens inhibit proliferation and DNA synthesis of porcine granulosa cells in vitro: comparison with estradiol, 5 alpha-dihydrotestosterone, gonadotropins and catecholamines. Mol Cell Endocrinol 1989; 64:119-126.
9. Dehennin L, Blacker C, Reiffsteck A, Scholler R. Estrogen 2-, 4-, 6- or 16-hydroxylation by human follicles shown by gas chromatography-mass spectrometry associated with stable isotope dilution. J Steroid Biochem 1984; 20:465-471.
10. Spicer LJ, Walega MA, Hammond JM. Metabolism of [3H] 2-hydroxyestradiol by cultured porcine granulosa cells: evidence for the presence of a catechol-O-methyltransferase pathway and a direct stimulatory effect of 2-methoxyestradiol on progesterone production. Biol Reprod 1987; 36:562-571.
11. Shimada T, Sugie A, Shindo M, Nakajima T, Azuma E, Hashimoto M, Inoue K. Tissue-specific induction of cytochromes P450 1A1 and 1B1 by polycyclic aromatic hydrocarbons and polychlorinated biphenyls in engineered C57BL/6J mice of arylhydrocarbon receptor gene. Toxicol Appl Pharmacol 2003; 187:1-10.
12. Desaulniers D, Xiao GH, Leingartner K, Chu I, Musicki B, Tsang BK. Comparisons of brain, uterus, and liver mRNA expression for cytochrome p450s, DNA methyltransferase-1, and catechol-o-methyltransferase in prepubertal female Sprague-Dawley rats exposed to a mixture of aryl hydrocarbon receptor agonists. Toxicol Sci 2005; 86:175-184.
13. Pocar P, Fischer B, Klonisch T, Hombach-Klonisch S. Molecular interactions of the aryl hydrocarbon receptor and its biological and toxicological relevance for reproduction. Reproduction 2005; 129:379-389.
14. Dasmahapatra AK, Trewin AL, Hutz RJ. Estrous cycle-regulated expression of CYP1B1 mRNA in the rat ovary. Comp Biochem Physiol B Biochem Mol Biol 2002; 133:127-134.
15. Vidal JD, Vandevoort CA, Marcus CB, Lazarewicz NR, Conley AJ. 2,3,7,8-tetrachlorodibenzo-p-dioxin induces CYP1B1 expression in human luteinized granulosa cells. Arch Biochem Biophys 2005; 439:53-60.
16. Lattanzi ML, Santos CB, Mudry MD, Baranao JL. Exposure of bovine oocytes to the endogenous metabolite 2-methoxyestradiol during in vitro maturation inhibits early embryonic development. Biol Reprod 2003; 69: 1793-1800.
17. Robles R, Morita Y, Mann KK, Perez GI, Yang S, Matikainen T, Sherr DH, Tilly JL. The aryl hydrocarbon receptor, a basic helix-loop-helix transcription factor of the PAS gene family, is required for normal ovarian germ cell dynamics in the mouse. Endocrinology 2000; 141:450-453.
18. Baba T, Mimura J, Nakamura N, Harada N, Yamamoto M, Morohashi K, Fujii-Kuriyama Y. Intrinsic function of the aryl hydrocarbon (dioxin) receptor as a key factor in female reproduction. Mol Cell Biol 2005; 25: 10040-10051.
19. Matikainen T, Perez GI, Jurisicova A, Pru JK, Schlezinger JJ, Ryu HY, Laine J, Sakai T, Korsmeyer SJ, Casper RF, Sherr DH, Tilly JL. Aromatic hydrocarbon receptor-driven Bax gene expression is required for premature ovarian failure caused by biohazardous environmental chemicals. Nat Genet 2001; 28:355-360.
20. Zhang L, Savas U, Alexander DL, Jefcoate CR. Characterization of the mouse Cyp1B1 gene. Identification of an enhancer region that directs aryl hydrocarbon receptor-mediated constitutive and induced expression. J Biol Chem 1998; 273:5174-5183.
21. Hanlon PR, Zheng W, Ko AY, Jefcoate CR. Identification of novel TCDD-regulated genes by microarray analysis. Toxicol Appl Pharmacol 2005; 202:215-228.
22. Spink BC, Fasco MJ, Gierthy JF, Spink DC. 12-O-tetradecanoylphorbol-13- acetate upregulates the Ah receptor and differentially alters CYP1B1 and CYP1A1 expression in MCF-7 breast cancer cells. J Cell Biochem 1998; 70:289-296.
23. Dasmahapatra AK, Wimpee BA, Trewin AL, Hutz RJ. 2,3,7,8- Tetrachlorodibenzo-p-dioxin increases steady-state estrogen receptor-beta mRNA levels after CYP1A1 and CYP1B1 induction in rat granulosa cells in vitro. Mol Cell Endocrinol 2001; 182:39-48.
24. Nakajima M, Iwanari M, Yokoi T. Effects of histone deacetylation and DNA methylation on the constitutive and TCDD-inducible expressions of the human CYP1 family in MCF-7 and HeLa cells. Toxicol Lett 2003; 144:247-256.
25. Tsutsumi O. Assessment of human contamination of estrogenic endocrine-disrupting chemicals and their risk for human reproduction. J Steroid Biochem Mol Biol 2005; 93:325-330.
26. Lin KC, Sun MJ. Relationship between sex hormone-binding globulin and pregnancy outcome in women undergoing controlled ovarian hyperstimulation for assisted reproduction. Endocr J 2005; 52:407-412.
27. D'Amato RJ, Lin CM, Flynn E, Folkman J, Hamel E. 2-Methoxyestradiol, an endogenous mammalian metabolite, inhibits tubulin polymerization by interacting at the colchicine site. Proc Natl Acad Sci U S A 1994; 91: 3964-3968.
28. Verdier-Pinard P, Wang Z, Mohanakrishnan AK, Cushman M, Hamel E. A Steroid derivative with paclitaxel-like effects on tubulin polymerisation. Molec Pharmacol 2000; 57:568-575.
29. Gorbsky GJ, Simerly C, Schatten G, Borisy GG. Microtubules in the metaphase-arrested mouse oocyte turn over rapidly. Proc Natl Acad Sci U S A 1990, 87:6049-6053.
30. Combelles CM, Albertini DF. Microtubule patterning during meiotic maturation in mouse oocytes is determined by cell cycle-specific sorting and redistribution of gamma-tubulin. Dev Biol 2001; 239:281-294.
31. Mitchison TJ, Maddox P, Groen A, Cameron L, Perlman Z, Ohi R, Desai A, Salmon ED, Kapoor TM. Bipolarization and poleward flux correlate during Xenopus extract spindle assembly. Mol Biol Cell 2004; 15: 5603-5615.
32. Sun XF, Zhang WH, Chen XJ, Xiao GH, Mai WY, Wang WH. Spindle dynamics in living mouse oocytes during meiotic maturation, ageing, cooling and overheating: a study by polarized light microscopy. Zygote 2004; 12:241-249.
33. Mailhes JB, Carabatsos MJ, Young D, London SN, Bell M, Albertini DF. Taxol-induced meiotic maturation delay, spindle defects, and aneuploidy in mouse oocytes and zygotes. Mutat Res 1999; 423:79-90.
34. Eichenlaub-Ritter U, Shen Y, Tinneberg HR. Manipulation of the oocyte: possible damage to the spindle apparatus. Reprod Biomed Online 2002; 5: 117-124.
35. Peters JM. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol Cell 2002; 9:931-943.
36. Musacchio A, Hardwick KG. The spindle checkpoint: structural insights into dynamic signalling. Nat Rev Mol Cell Biol 2002; 3:731-741.
37. Kudo NR, Wassmann K, Anger M, Schuh M, Wirth KG, Xu H, Helmhart W, Kudo H, McKay M, Maro B, Ellenberg J, de Boer P, Nasmyth K. Resolution of chiasmata in oocytes requires separase-mediated proteolysis. Cell 2006; 126:135-146.
38. Lee J, Okada K, Ogushi S, Miyano T, Miyake M, Yamashita M. Loss of Rec8 from chromosome arm and centromere region is required for homologous chromosome separation and sister chromatid separation, respectively, in mammalian meiosis. Cell Cycle 2006; 5:1448-1455.
39. Hardwick KG. Checkpoint signalling: Mad2 conformers and signal propagation. CurrBiol 2005; 15:R122-R124.
40. Wassmann K, Niault T, Maro B. Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr Biol 2003; 13:1596-1608.
41. Homer HA, McDougall A, Levasseur M, Herbert M. Restaging the spindle assembly checkpoint in female mammalian meiosis I. Cell Cycle 2006; 4: 650-653.
42. Zhang D, Ma W, Li YH, Hou Y, Li SW, Meng XQ, Sun XF, Sun QY, Wang WH. Intra-oocyte localization of MAD2 and its relationship with kinetochores, microtubules, and chromosomes in rat oocytes during meiosis. Biol Reprod 2004; 71:740-748.
43. Kallio M, Eriksson JE, Gorbsky GJ. Differences in spindle association of the mitotic checkpoint protein Mad2 in mammalian spermatogenesis and oogenesis. Dev Biol 2000; 225:112-123.
44. Brunet S, Maro B. Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction 2005; 130:801-811.
45. Tsurumi C, Hoffmann S, Geley S, Graeser R, Polanski Z. The spindle assembly checkpoint is not essential for CSF arrest of mouse oocytes. J Cell Biol 2004; 167:1037-1050.
46. Oldenbourg R, Mei G. New polarized light microscope with precision universal compensator. J Microsc 1995; 180:140-147.
47. Liu L, Oldenbourg R, Trimarchi JR, Keefe DL. A reliable, noninvasive technique for spindle imaging and enucleation of mammalian oocytes. Nat Biotechnol 2000; 18:223-225.
48. Shen Y, Betzendahl I, Sun F, Tinneberg HR, Eichenlaub-Ritter U. Non-invasive method to assess genotoxicity of nocodazole interfering with spindle formation in mammalian oocytes. Reprod Toxicol 2005; 19: 459-471.
49. Sanfins A, Lee GY, Plancha CE, Overstrom EW, Albertini DF. Distinctions in meiotic spindle structure and assembly during in vitro and in vivo maturation of mouse oocytes. Biol Reprod 2003; 69; 2059-2067.
50. Can A, Semiz O, Cinar O. Centrosome and microtubule dynamics during early stages of meiosis in mouse oocytes. Mol Hum Reprod 2003; 9: 749-756.
51. Can A, Semiz O, Cinar O. Bisphenol-A induces cell cycle delay and alters centrosome and spindle microtubular organization in oocytes during meiosis. Mol Hum Reprod 2005; 11:389-396.
52. Hunt PA, Koehler KE, Susiarjo M, Hodges CA, Ilagan A, Voigt RC, Thomas S, Thomas BF, Hassold TJ. Bisphenol a exposure causes meiotic aneuploidy in the female mouse. Curr Biol 2003; 13:546-553.
53. Hogan B, Constantini F, Lacy E.Manipulating the Mouse Embryo, A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory; 1986:252-256.
54. Eichenlaub-Ritter U, Betzendahl I. Chloral hydrate induced spindle aberrations, metaphase I arrest and aneuploidy in mouse oocytes. Mutagenesis 1995; 10:477-486.
55. Hodges CA, Hunt PA. Simultaneous analysis of chromosomes and chromosome-associated proteins in mammalian oocytes and embryos. Chromosoma 2002; 111:165-169.
56. Vogt E, Betzendahl I, Eichenlaub-Ritter U. Model for Aging: Knockdown of Mad2 expression predisposes to non-disjunction in mammalian oocytes possessing aberrant spindles. Hum Reprod 2005; 20(suppl 1):i70.
57. Tarkovski AK. An air-drying methods for chromosome preparation from mouse eggs. Cytogenetics 1966; 5:394-400.
58. Zacharia LC, Gogos JA, Karayiorgou M, Jackson EK, Gillespie DG, Barchiesi F, Dubey RK. Methoxyestradiols mediate the antimitogenic effects of 17beta-estradiol: direct evidence from catechol-O-methyltransferase-knockout mice. Circulation 2003; 108:2974-2978.
59. Kumar AP, Garcia GE, Slaga TJ. 2-Methoxyestradiol blocks cell-cycle progression at G(2)/M phase and inhibits growth of human prostate cancer cells. Mol Carcinog 2001; 31:111-124.
60. Li L, Bu S, Backstrom T, Landstrom M, Ulmsten U, Fu X. Induction of apoptosis and G2/M arrest by 2-methoxyestradiol in human cervical cancer HeLaS3 cells. Anticancer Res 2004; 24:873-880.
61. Perez-Stable C. 2-Methoxyestradiol and paclitaxel have similar effects on the cell cycle and induction of apoptosis in prostate cancer cells. Cancer Lett 2006; 231:49-64.
62. Homer HA. Mad2 and spindle assembly checkpoint function during meiosis I in mammalian oocytes. Histol Histopathol 2006; 21:873-886.
63. Homer HA, McDougall A, Levasseur M, Murdoch AP, Herbert M. Mad2 is required for inhibiting securin and cyclin B degradation following spindle depolymerisation in meiosis I mouse oocytes. Reproduction 2005; 130:829-843.
64. Mailhes JB, Marchetti F. Mechanisms and chemical induction of aneuploidy in rodent germ cells. Cytogenet Genome Res 2005; 111: 384-391.
65. Pinsky BA, Biggins S. The spindle checkpoint: tension versus attachment. Trends Cell Biol 2005; 15:486-493.
66. Pinsky BA, Kung C, Shokat KM, Biggins S. The Ipl1-Aurora protein kinase activates the spindle checkpoint by creating unattached kinetochores. Nat Cell Biol 2006; 8:78-83.
67. Hunt P, LeMaire R, Embury P, Sheean L, Mroz K. Analysis of chromosome behavior in intact mammalian oocytes: monitoring the segregation of a univalent chromosome during female meiosis. Hum Mol Genet 1995; 4:2007-2012.
68. LeMaire-Adkins R, Radke K, Hunt PA. Lack of checkpoint control at the metaphase/anaphase transition: a mechanism of meiotic nondisjunction in mammalian females. J Cell Biol 1997; 139:1611-1619.
69. Cimini D, Howell B, Maddox P, Khodjakov A, Degrassi F, Salmon ED. Merotelic kinetochore orientation is a major mechanism of aneuploidy in mitotic mammalian tissue cells. J Cell Biol 2001; 153:517-527.
70. LaFountain JR Jr, Oldenbourg R. Maloriented bivalents have metaphase positions at the spindle equator with more kinetochore microtubules to one pole than to the other. Mol Biol Cell 2004; 15:5346-5355.
71. Lee J, Miyano T, Moor RM. Spindle formation and dynamics of gamma-tubulin and nuclear mitotic apparatus protein distribution during meiosis in pig and mouse oocytes. Biol Reprod 2000; 62:1184-1192.
72. Michaut MA, Williams CJ, Schultz RM. Phosphorylated MARCKS: a novel centrosome component that also defines a peripheral subdomain of the cortical actin cap in mouse eggs. Dev Biol 2005; 280:26-37.
73. Beker-van Woudenberg AR, van Tol HT, Roelen BA, Colenbrander B, Bevers MM. Estradiol and its membrane-impermeable conjugate (estradiol-bovine serum albumin) during in vitro maturation of bovine oocytes: effects on nuclear and cytoplasmic maturation, cytoskeleton, and embryo quality. Biol Reprod 2004; 70:1465-1474.
74. LaVallee TM, Zhan XH, Herbstritt CJ, Kough EC, Green SJ, Pribluda VS. 2-Methoxyestradiol inhibits proliferation and induces apoptosis independently of estrogen receptors alpha and beta. Cancer Res 2002; 62: 3691-3697.
75. Zuccotti M, Giorgi Rossi P, Martinez A, Garagna S, Forabosco A, Redi CA. Meiotic and developmental competence of mouse antral oocytes. Biol Reprod 1998; 58:700-704.
76. Bouniol-Baly C, Hamraoui L, Guibert J, Beaujean N, Szollosi MS, Debey P. Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes. Biol Reprod 1999; 60:580-587.
77. Ochi T, Oda T. Structure-effect relationship in the induction of mitotic phase-specific abnormality of centrosome integrity and multipolar spindles by steroidal estrogens and their derivatives in cultured mammalian cells. J Steroid Biochem Mol Biol 2001; 78:113-122.
78. Brueggemeier RW, Bhat AS, Lovely CJ, Coughenour HD, Joomprabutra S, Weitzel DH, Vandre DD, Yusuf F, Burak WE Jr. 2-Methoxymethylestradiol: a new 2-methoxy estrogen analog that exhibits antiproliferative activity and alters tubulin dynamics. J Steroid Biochem Mol Biol 2001; 78:145-156.
79. Can A, Semiz O. Diethylstilbestrol (DES)-induced cell cycle delay and meiotic spindle disruption in mouse oocytes during in-vitro maturation. Mol Hum Reprod 2000; 6:154-162.
80. Matthews J, Wihlen B, Thomsen J, Gustafsson JA. Aryl hydrocarbon receptor-mediated transcription: ligand-dependent recruitment of estrogen receptor alpha to 2,3,7,8-tetrachlorodibenzo-p-dioxin-responsive promoters. Mol Cell Biol 2005; 25:5317-5328.
81. Beischlag TV, Perdew GH. ER alpha-AHR-ARNT protein-protein interactions mediate estradiol-dependent transrepression of dioxin-inducible gene transcription. J Biol Chem 2005; 280:21607-21611.
82. Gokmen-Polar Y, Escuin D, Walls CD, Soule SE, Wang Y, Sanders KL, Lavallee TM, Wang M, Guenther BD, Giannakakou P, Sledge GW Jr. beta-Tubulin mutations are associated with resistance to 2-methoxyestradiol in MDA-MB-435 cancer cells. Cancer Res 2005; 65:9406-9414.
83. Steuerwald N, Cohen J, Herrera RJ, Brenner CA. Analysis of gene expression in single oocytes and embryos by real-time rapid cycle fluorescence monitored RT-PCR. Mol Hum Reprod 1999; 5:1034-1039.
84. Hamatani T, Falco G, Carter MG, Akutsu H, Stagg CA, Sharov AA, Dudekula DB, VanBuren V, Ko MS. Age-associated alteration of gene expression patterns in mouse oocytes. Hum Mol Genet 2004; 13:2263-2278.
85. Hunt PA, Hassold TJ. Sex matters in meiosis. Science 2002; 296: 2181-2183.
86. Eichenlaub-Ritter U, Vogt E, Yin H, Gosden R. Spindles, mitochondria and redox potential in ageing oocytes. Reprod Biomed Online 2004; 8: 45-58.
87. Handel MA, Sun F. Regulation of meiotic cell divisions and determination of gamete quality: impact of reproductive toxins. Semin Reprod Med 2005; 23:213-221.