Proteomic Analysis of the Rat Ovary Following Chronic Low-Dose Exposure to 2,3,7,8-Tetrachlorodibenzo-p-Dioxin (TCDD)

REFERENCES

• Bruggeman , V. , Van den Bergh , G. , Clerens , S. , Dumez , L. , Onagbesan , O. , Arckens , L. and Decuypere , E. 2006 . Effect of a single in ovo injection of 2,3,7,8-tetrachlorodibenzo-p-dioxin on protein expression in liver and ovary of the one-day-old chick analyzed by fluorescent two-dimensional difference gel electrophoresis and mass spectrometry . Proteomics , 6 : 2576 – 2585 .
   PubMed Web of Science ®Google Scholar
• Choi , S. M. , Yoo , S. D. and Lee , B. M. 2004 . Toxicological characteristics of endocrine disrupting chemicals: Developmental toxicity, carcinogenicity and mutagenicity . J. Toxicol. Environ. Health B , 7 : 1 – 24 .
   PubMed Web of Science ®Google Scholar
• Cho , Y. M. , Bae , S. H. , Choi , B. K. , Cho , S. Y. , Song , C. W. , Yoo , J. K. and Paik , Y. K. 2003 . Differential expression of the liver proteome in senescence accelerated mice . Proteomics , 3 : 1883 – 1894 .
   PubMed Web of Science ®Google Scholar
• Conrad , D. H. , Goyette , J. and Thomas , P. S. 2008 . Proteomics as a method for early detection of cancer: A review of proteomics, exhaled breath condensate, and lung cancer screening . J. Gen. Intern. Med. , 23 ( Suppl. 1 ) : 78 – 84 .
   PubMedGoogle Scholar
• Craig , J. , Orisaka , M. , Wang , H. , Orisaka , S. , Thompson , W. , Zhu , C. , Kotsuji , F. and Tsang , B. K. 2007 . Gonadotropin and intra-ovarian signals regulating follicle development and atresia: the delicate balance between life and death . Front. Biosci. , 12 : 3628 – 3639 .
   PubMed Web of Science ®Google Scholar
• Croutch , C. R. , Lebofsky , M. , Schramm , K. W. , Terranova , P. F. and Rozman , K. K. 2005 . 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) and 1,2,3,4,7,8-hexachlorodibenzo-p-dioxin (HxCDD) alter body weight by decreasing insulin-like growth factor I (IGF-I) signaling . Toxicol. Sci. , 85 : 560 – 571 .
   PubMed Web of Science ®Google Scholar
• Cummings , A. M. , Hedge , J. M. and Birnbaum , L. S. 1999 . Effect of prenatal exposure to TCDD on the promotion of endometriotic lesion growth by TCDD in adult female rats and mice . Toxicol. Sci. , 52 : 45 – 49 .
   PubMed Web of Science ®Google Scholar
• Dasmahapatra , A. K. , Wimpee , B. A. , Trewin , A. L. , Wimpee , C. F. , Ghorai , J. K. and Hutz , R. J. 2000 . Demonstration of 2,3,7,8-tetrachlorodibenzo-p-dioxin attenuation of P450 steroidogenic enzyme mRNAs in rat granulosa cell in vitro by competitive reverse transcriptase-polymerase chain reaction assay . Mol. Cell Endocrinol. , 164 : 5 – 18 .
   PubMed Web of Science ®Google Scholar
• Diehl-Jones , W. L. and Bols , N. C. 2000 . Use of response biomarkers in milk for assessing exposure to environmental contaminants: The case for dioxin-like compounds . J. Toxicol. Environ. Health B , 3 : 79 – 107 .
   PubMed Web of Science ®Google Scholar
• Diliberto , J. J. , DeVito , M. J. , Ross , D. G. and Birnbaum , L. S. 2001 . Subchronic exposure of [3H]-2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in female B6C3F1 mice: Relationship of steady-state levels to disposition and metabolism . Toxicol. Sci. , 61 : 241 – 255 .
   PubMed Web of Science ®Google Scholar
• Franczak , A. , Nynca , A. , Valdez , K. E. , Mizinga , K. M. and Petroff , B. K. 2006 . Effects of acute and chronic exposure to the aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin on the transition to reproductive senescence in female Sprague-Dawley rats . Biol. Reprod. , 74 : 125 – 130 .
   PubMed Web of Science ®Google Scholar
• Fukuzawa , N. H. , Ohsako , S. , Wu , Q. , Sakaue , M. , Fujii-Kuriyama , Y. , Baba , T. and Tohyama , C. 2004 . Testicular cytochrome P450scc and LHR as possible targets of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in the mouse . Mol. Cell Endocrinol. , 221 : 87 – 96 .
   PubMed Web of Science ®Google Scholar
• Gamble , S. C. , Odontiadis , M. , Waxman , J. , Westbrook , J. A. , Dunn , M. J. , Wait , R. , Lam , E. W. and Bevan , C. L. 2004 . Androgens target prohibitin to regulate proliferation of prostate cancer cells . Oncogene , 23 : 2996 – 3004 .
   PubMed Web of Science ®Google Scholar
• Goldstein , J. A. , Linko , P. and Bergman , H. 1982 . Induction of porphyria in the rat by chronic versus acute exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin . Biochem. Pharmacol. , 31 : 1607 – 1613 .
   PubMed Web of Science ®Google Scholar
• Gonzalez , P. , Alvarez , R. , Reguero , J. R. , Batalla , A. , Alvarez , V. , Cortina , A. , Cubero , G. I. , Garcia-Castro , M. and Coto , E. 2002 . Variation in the lipoprotein receptor-related protein, alpha2-macroglobulin and lipoprotein receptor-associated protein genes in relation to plasma lipid levels and risk of early myocardial infarction . Coronary Artery Dis. , 13 : 251 – 254 .
   PubMed Web of Science ®Google Scholar
• Hassoun , E. A. , Wang , H. , Abushaban , A. and Stohs , S. J. 2002 . Induction of oxidative stress in the tissues of rats after chronic exposure to TCDD, 2,3,4,7,8-pentachlorodibenzofuran, and 3,3′,4,4′,5-pentachlorobiphenyl . J. Toxicol. Environ. Health A , 65 : 825 – 842 .
   PubMed Web of Science ®Google Scholar
• He , B. , Feng , Q. , Mukherjee , A. , Lonard , D. M. , DeMayo , F. J. , Katzenellenbogen , B. S. , Lydon , J. P. and O'Malley , B. W. 2008 . A repressive role for prohibitin in estrogen signaling . Mol. Endocrinol. , 22 : 344 – 360 .
   PubMedGoogle Scholar
• Heiden , T. K. , Carvan , M. J. 3rd and Hutz , R. J. 2006 . Inhibition of follicular development, vitellogenesis, and serum 17beta-estradiol concentrations in zebrafish following chronic, sublethal dietary exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin . Toxicol. Sci. , 90 : 490 – 499 .
   PubMed Web of Science ®Google Scholar
• Ishida , T. , Ishii , Y. , Yamada , H. and Oguri , K. 2002 . The induction of hepatic selenium-binding protein by aryl hydrocarbon (Ah)-receptor ligands in rats . J. Health Sci. , 48 : 62 – 68 .
   Google Scholar
• Ishimura , R. , Ohsako , S. , Kawakami , T. , Sakaue , M. , Aoki , Y. and Tohyama , C. 2002 . Altered protein profile and possible hypoxia in the placenta of 2,3,7,8-tetrachlorodibenzo-p-dioxin-exposed rats . Toxicol. Appl. Pharmacol. , 185 : 197 – 206 .
   PubMed Web of Science ®Google Scholar
• Johnson , K. L. , Cummings , A. M. and Birnbaum , L. S. 1997 . Promotion of endometriosis in mice by polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls . Environ. Health Perspect. , 105 : 750 – 755 .
   PubMed Web of Science ®Google Scholar
• Joo , W. A. , Kang , M. J. , Son , W. K. , Lee , H. J. , Lee , D. Y. , Lee , E. and Kim , C. W. 2003 . Monitoring protein expression by proteomics: human plasma exposed to benzene . Proteomics , 3 : 2402 – 2411 .
   PubMed Web of Science ®Google Scholar
• Juhaszova , M. , Wang , S. , Zorov , D. B. , Nuss , H. B. , Gleichmann , M. , Mattson , M. P. and Sollott , S. J. 2008 . The identity and regulation of the mitochondrial permeability transition pore: Where the known meets the unknown . Ann. NY Acad. Sci. , 1123 : 197 – 212 .
   PubMed Web of Science ®Google Scholar
• Kasashima , K. , Ohta , E. , Kagawa , Y. and Endo , H. 2006 . Mitochondrial functions and estrogen receptor-dependent nuclear translocation of pleiotropic human prohibitin 2 . J. Biol. Chem. , 281 : 36401 – 36410 .
   PubMed Web of Science ®Google Scholar
• Khorram , O. , Garthwaite , M. and Golos , T. 2002 . Uterine and ovarian aryl hydrocarbon receptor (AHR) and aryl hydrocarbon receptor nuclear translocator (ARNT) mRNA expression in benign and malignant gynaecological conditions . Mol. Hum. Reprod. , 8 : 75 – 80 .
   PubMed Web of Science ®Google Scholar
• Kim , M. K. , Oh , S. , Lee , J. H. , Im , H. , Ryu , Y. M. , Oh , E. , Lee , J. , Lee , E. and Sul , D. 2004 . Evaluation of biological monitoring markers using genomic and proteomic analysis for automobile emission inspectors and waste incinerating workers exposed to polycyclic aromatic hydrocarbons or 2,3,7,8-tetracholrodedibenzo-p-dioxins . Exp. Mol. Med. , 36 : 396 – 410 .
   PubMed Web of Science ®Google Scholar
• Kociba , R. J. , Keyes , D. G. , Beyer , J. E. , Carreon , R. M. , Wade , C. E. , Dittenber , D. A. , Kalnins , R. P. , Frauson , L. E. , Park , C. N. , Barnard , S. D. , Hummel , R. A. and Humiston , C. G. 1978 . Results of a two-year chronic toxicity and oncogenicity study of 2,3,7,8-tetrachlorodibenzo-p-dioxin in rats . Toxicol. Appl. Pharmacol. , 46 : 279 – 303 .
   PubMed Web of Science ®Google Scholar
• Kurtev , V. , Margueron , R. , Kroboth , K. , Ogris , E. , Cavailles , V. and Seiser , C. 2004 . Transcriptional regulation by the repressor of estrogen receptor activity via recruitment of histone deacetylases . J. Biol. Chem. , 279 : 24834 – 24843 .
   PubMed Web of Science ®Google Scholar
• Lanfear , J. , Fleming , J. , Walker , M. and Harrison , P. 1993 . Different patterns of regulation of the genes encoding the closely related 56 kDa selenium- and acetaminophen-binding proteins in normal tissues and during carcinogenesis . Carcinogenesis , 14 : 335 – 340 .
   PubMed Web of Science ®Google Scholar
• Mattow , J. , Demuth , I. , Haeselbarth , G. , Jungblut , P. R. and Klose , J. 2006 . Selenium-binding protein 2, the major hepatic target for acetaminophen, shows sex differences in protein abundance . Electrophoresis , 2 : 1683 – 1691 .
   Google Scholar
• McHale , C. M. , Zhang , L. , Hubbard , A. E. , Zhao , X. , Baccarelli , A. , Pesatori , A. C. , Smith , M. T. and Landi , M. T. 2007 . Microarray analysis of gene expression in peripheral blood mononuclear cells from dioxin-exposed human subjects . Toxicology , 229 : 101 – 113 .
   PubMed Web of Science ®Google Scholar
• Miettinen , H. M. , Pulkkinen , P. , Jamsa , T. , Koistinen , J. , Simanainen , U. , Tuomisto , J. , Tuukkanen , J. and Viluksela , M. 2005 . Effects of in utero and lactational TCDD exposure on bone development in differentially sensitive rat lines . Toxicol Sci , 85 : 1003 – 1012 .
   PubMed Web of Science ®Google Scholar
• Mishra , S. , Murphy , L. C. and Murphy , L. J. 2006 . The prohibitins: emerging roles in diverse functions . J. Cell Mol. Med. , 10 : 353 – 363 .
   PubMed Web of Science ®Google Scholar
• Montano , M. M. , Ekena , K. , Delage-Mourroux , R. , Chang , W. , Martini , P. and Katzenellenbogen , B. S. 1999 . An estrogen receptor-selective coregulator that potentiates the effectiveness of antiestrogens and represses the activity of estrogens . Proc. Natl. Acad. Sci. USA , 96 : 6947 – 6952 .
   PubMed Web of Science ®Google Scholar
• Murtomaa , M. , Tervaniemi , O. M. , Parviainen , J. , Ruokojarvi , P. , Tuukkanen , J. and Viluksela , M. 2007 . Dioxin exposure in contaminated sawmill area: The use of molar teeth and bone of bank vole (Clethrionomys glareolus) and field vole (Microtus agrestis) as biomarkers . Chemosphere , 68 : 951 – 957 .
   PubMed Web of Science ®Google Scholar
• Mutoh , J. , Taketoh , J. , Okamura , K. , Kagawa , T. , Ishida , T. , Ishii , Y. and Yamada , H. 2006 . Fetal pituitary gonadotropin as an initial target of dioxin in its impairment of cholesterol transportation and steroidogenesis in rats . Endocrinology , 147 : 927 – 936 .
   PubMed Web of Science ®Google Scholar
• Oberemm , A. , Meckert , C. , Brandenburger , L. , Herzig , A. , Lindner , Y. , Kalenberg , K. , Krause , E. , Ittrich , C. , Kopp-Schneider , A. , Stahlmann , R. , Richter-Reichhelm , H. B. and Gundert-Remy , U. 2005 . Differential signatures of protein expression in marmoset liver and thymus induced by single-dose TCDD treatment . Toxicology , 206 : 33 – 48 .
   PubMed Web of Science ®Google Scholar
• Ohyama , K. , Ohta , M. , Sano , T. , Sato , K. , Nakagomi , Y. , Shimura , Y. and Yamano , Y. 2007 . Maternal exposure of low dose of TCDD modulates the expression of estrogen receptor subunits of male gonads in offspring . J. Vet. Med. Sci. , 69 : 619 – 625 .
   PubMed Web of Science ®Google Scholar
• Okey , A. B. , Riddick , D. S. and Harper , P. A. 1994 . The Ah receptor: Mediator of the toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and related compounds . Toxicol. Lett. , 70 : 1 – 22 .
   PubMed Web of Science ®Google Scholar
• Park , S. E. , Xu , J. , Frolova , A. , Liao , L. , O'Malley , B. W. and Katzenellenbogen , B. S. 2005 . Genetic deletion of the repressor of estrogen receptor activity (REA) enhances the response to estrogen in target tissues in vivo . Mol. Cell Biol. , 25 : 1989 – 1999 .
   PubMed Web of Science ®Google Scholar
• Pocar , P. , Brevini , T. A. , Fischer , B. and Gandolfi , F. 2003 . The impact of endocrine disruptors on oocyte competence . Reproduction , 125 : 313 – 325 .
   PubMed Web of Science ®Google Scholar
• Pocar , P. , Fischer , B. , Klonisch , T. and Hombach-Klonisch , S. 2005 . Molecular interactions of the aryl hydrocarbon receptor and its biological and toxicological relevance for reproduction . Reproduction , 129 : 379 – 389 .
   PubMed Web of Science ®Google Scholar
• Richards , J. S. 1980 . Maturation of ovarian follicles: Actions and interactions of pituitary and ovarian hormones on follicular cell differentiation . Physiol Rev , 60 : 51 – 89 .
   PubMed Web of Science ®Google Scholar
• Roy , D. , Palangat , M. , Chen , C.-W. , Thomas , R. D. , Colerangle , J. , Atkinson , A. and Yin , Z.-J. 1997 . Biochemical and molecular changes at the cellular level in response to exposure to environmental estrogen-like chemicals . J. Toxicol. Environ. Health , 50 : 1 – 29 .
   PubMed Web of Science ®Google Scholar
• Sarioglu , H. , Brandner , S. , Haberger , M. , Jacobsen , C. , Lichtmannegger , J. , Wormke , M. and Andrae , U. 2008 . Analysis of 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced proteome changes in 5L rat hepatoma cells reveals novel targets of dioxin action including the mitochondrial apoptosis regulator VDAC2 . Mol. Cell. Proteom. , 7 : 394 – 410 .
   PubMed Web of Science ®Google Scholar
• Schneider , M. D. 2005 . Cyclophilin D: Knocking on death's door . Sci STKE , 2005 ( 287 ) : pe26
   PubMedGoogle Scholar
• Senft , A. P. , Dalton , T. P. , Nebert , D. W. , Genter , M. B. , Hutchinson , R. J. and Shertzer , H. G. 2002 . Dioxin increases reactive oxygen production in mouse liver mitochondria . Toxicol. Appl. Pharmacol. , 178 : 15 – 21 .
   PubMed Web of Science ®Google Scholar
• Shen , D. , Dalton , T. P. , Nebert , D. W. and Shertzer , H. G. 2005 . Glutathione redox state regulates mitochondrial reactive oxygen production . J. Biol. Chem. , 280 : 25305 – 25312 .
   PubMed Web of Science ®Google Scholar
• Shertzer , H. G. , Nebert , D. W. , Puga , A. , Ary , M. , Sonntag , D. , Dixon , K. , Robinson , L. J. , Cianciolo , E. and Dalton , T. P. 1998 . Dioxin causes a sustained oxidative stress response in the mouse . Biochem. Biophys. Res. Commun. , 253 : 44 – 48 .
   PubMed Web of Science ®Google Scholar
• Tang , N. J. , Liu , P. J. , Coenraads , J. , Dong , L. , Zhao , L. J. , Ma , S. W. , Chen , X. , Zhang , C. M. , Ma , X. M. , Wei , W. G. , Zhang , P. and Bai , Z. P. 2008 . Expression of AhR, CYP1A1, GSTA1, c-fos and TGF-alpha in skin lesions from dioxin-exposed humans with chloracne . Toxicol. Lett. , 177 : 182 – 187 .
   PubMed Web of Science ®Google Scholar
• Valdez , K. E. and Petroff , B. K. 2004 . Potential roles of the aryl hydrocarbon receptor in female reproductive senescence . Reprod. Biol. , 4 : 243 – 258 .
   PubMedGoogle Scholar
• Yamakuchi , M. , Ferlito , M. , Morrell , C. N. , Matsushita , K. , Fletcher , C. A. , Cao , W. and Lowenstein , C. J. 2008 . Exocytosis of endothelial cells is regulated by N-ethylmaleimide-sensitive factor . Methods Mol. Biol. , 440 : 203 – 215 .
   PubMedGoogle Scholar
• Yoshida , M. , Watanabe , G. , Shirota , M. , Maekawa , A. and Taya , K. 2005 . Reduction of primordial follicles caused by maternal treatment with busulfan promotes endometrial adenocarcinoma development in donryu rats . J. Reprod. Dev. , 5 : 707 – 714 .
   Web of Science ®Google Scholar
• Young , G. , Kagawa , H. and Nagahama , Y. 1983 . Evidence for a decrease in aromatase activity in the ovarian granulosa cells of amago salmon (Oncorhynchus rhodurus) associated with final oocyte maturation . Biol. Reprod. , 29 : 310 – 315 .
   PubMed Web of Science ®Google Scholar
• Zhang , C. , Yang , T. , Wang , J. , Liu , G. and Chen , Q. 2005 . The Chinese traditional medicine ‘Bushen Yinao Pian’ increased the level of ageing-related gene LRPAP-1 expression in the cerebral tissue of accelerated senescence-prone mouse 8/Ta . J. Ethnopharmacol. , 98 : 61 – 65 .
   PubMed Web of Science ®Google Scholar