Alterations in the rat serum proteome induced by prepubertal exposure to bisphenol A and genistein

Journal of Proteome Research

Volumn 13, Issue 3, 2014, Pages 1502-1514

  Betancourt, Angela ^a   Mobley, James A ^b,c   Wang, Jun ^a   Jenkins, Sarah ^a   Chen, Dongquan ^b,d   Kojima, Kyoko ^b   Russo, Jose ^e   Lamartiniere, Coral A ^a,b  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c University of Alabama at Birmingham   (United States)

^d University of Alabama at Birmingham   (United States)

^e FOX CHASE CANCER CENTER   (United States)

Author keywords

BPA; carcinogenesis; genistein; proteomics; serum

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; BIOLOGICAL MARKER; GENISTEIN;

ANIMAL EXPERIMENT; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; FEMALE; NONHUMAN; PERINATAL PERIOD; PREPUBERTY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; SYSTEMS BIOLOGY; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

ADMINISTRATION, ORAL; ANIMALS; ANIMALS, NEWBORN; ANTICARCINOGENIC AGENTS; BENZHYDRYL COMPOUNDS; BLOOD PROTEINS; CARCINOGENESIS; CARCINOGENS; FEMALE; GENE EXPRESSION REGULATION; GENISTEIN; HUMANS; LACTATION; MAMMARY GLANDS, ANIMAL; MAMMARY NEOPLASMS, ANIMAL; MATERNAL EXPOSURE; MOLECULAR SEQUENCE ANNOTATION; PHENOLS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84896745682     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr401027q     Document Type: Article

References (77)

1. Calafat, A. M.; Kuklenyik, Z.; Reidy, J. A.; Caudill, S. P.; Ekong, J.; Needham, L. L. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population Environ. Health Perspect. 2005, 113, 391-395
2. Roy, J. R.; Chakraborty, S.; Chakraborty, T. R. Estrogen-like endocrine disrupting chemicals affecting puberty in humans-a review Med. Sci. Monit. 2009, 15, RA137-145
3. Munoz-de-Toro, M.; Markey, C. M.; Wadia, P. R.; Luque, E. H.; Rubin, B. S.; Sonnenschein, C. Perinatal exposure to bisphenol-A alters peripubertal mammary gland development in mice Endocrinology 2005, 146 (9) 4138-4147
4. Durando, M.; Kass, L.; Piva, J.; Sonnenschein, C.; Soto, A. M.; Luque, E. H. Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats Environ. Health Perspect. 2007, 115 (1) 80-86
5. Jenkins, S.; Raghuraman, N.; Eltoum, I.; Carpenter, M.; Russo, J.; Lamartiniere, C. A. Oral exposure to bisphenol A increases dimethylbenzanthracene-induced mammary cancer in rats Environ. Health Perspect. 2009, 117, 910-915
6. Krishnan, A. V. Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving Endocrinology 1993, 132 (6) 2279-2286
7. Lapensee, E. W., Bisphenol A at low nanomolar doses confers chemoresistance in estrogen receptor-alpha-positive and -negative breast cancer cells. Environ Health Perspect. 2009117 (2): 175-180
8. Wetherill, Y. B. In vitro molecular mechanisms of bisphenol A action Reprod. Toxicol. 2007, 24 (2) 178-198
9. Lee, H. P.; Gourley, L.; Duffy, S. W.; Esteve, J.; Lee, J.; Day, N. E. Dietary effects on breast cancer risk in Singapore Lancet 1991, 336, 1197-1200
10. Ziegler, R. G.; Hoover, R. N.; Hildeshein, R. N.; Nomura, M. Y.; Pike, M. C.; West, D. W.; Wu-Williams, A.; Kolonel, L. N.; Horn-Ross, P. L.; Rosenthal, J. F.; Hyer, M. B. Migration patterns and breast cancer risk in Asian-American women J. Natl. Cancer Inst. 1993, 85, 1819-1827
11. Akiyama, T.; Ishida, J.; Nakagawa, S.; Ogawara, H.; Watanabe, S.; Itoh, N.; Shibuya, M.; Fukami, Y. Genistein, a specific inhibitor of tyrosine-specific protein kinases J. Biol. Chem. 1987, 262 (12) 5592-5595
12. Okura, A.; Arakawa, H.; Oka, H.; Yoshinari, T.; Monden, Y. Effect of genistein on topoisomerase activity and on the growth of [Val 12]Ha-rastransformed NIH 3T3 cells Biochem. Biophys. Res. Commun. 1988, 157 (1) 183-189
13. Evans, B. A.; Griffiths, K.; Morton, M. S. Inhibition of 5 alpha-reductase in genital skin fibroblasts and prostate tissue by dietary lignans and isoflavonoids J. Endocrinol. 1995, 147 (2) 295-302
14. Kuiper, G. G.; Lemmen, J. G.; Carlsson, B.; Corton, J. C.; Safe, S. H.; van der Saag, P. T.; van der Burg, B.; Gustafsson, J. A. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta Endocrinology 1998, 139, 10-4263
15. Fritz, W. A.; Coward, L.; Wang, J.; Lamartiniere, C. A. Dietary genistein: perinatal mammary cancer prevention, bioavailability and toxicity testing in the rat Carcinogenesis. 1998, 19, 2151-2158
16. Lamartiniere, C. A. Timing of exposure and mammary cancer risk J. Mammary Gland Biol. Neoplasia 2002, 7, 67-776
17. Wang, J.; Betancourt, A. B.; Mobley, J. A.; Lamartiniere, C. A. Proteomic Discovery of Genistein Action in the Rat Mammary Gland J. Proteome Res. 2011, 10 (4) 1621-1631
18. Caron, M.; Choquet-Kastylevsky, G.; Joubert-Caron, R. Cancer immunomics using autoantibody signatures for biomarker discovery Mol. Cell. Proteomics 2007, 7, 6115-612
19. Yi, B.; Kim, C.; Park, M.; Han, Y.; Park, J. Y.; Yang, M. Association between endocrine disrupting phenols in colostrums and maternal and infant health Int. J. Endocrinol. 2013, 2013, 282381
20. Franke, A. A.; Custer, L. J.; Tanaka, Y. Isoflavones in human breast milk and other biological fluids Am. J. Clin. Nutr. 1998, 68 (Suppl) 1466s-1473s
21. Lamartiniere, C. A.; Sloop, C. A.; Clark, J.; Tilson, H. A.; Lucier, G. W. Organizational Effects of Hormones and Hormonally-Active Xenobiotics on Postnatal Development. In 12th Conference on Environmental Toxicology; AFAMRL-TR-81-149; U.S. Air Force: Dayton, OH, 1982; p 192.
22. Hsu, P. Y.; Hsu, H. K.; Singer, G. A.; Yan, P. S.; Rodriguez, B. A.; Liu, J. C.; Weng, Y. I.; Deatherage, D. E.; Chen, Z.; Pereira, J. S.; Lopez, R.; Russo, J.; Wang, Q.; Lamartiniere, C. A.; Nephew, K. P.; Huang, T. H. Estrogen-mediated epigenetic repression of large chromosomal regions through DNA looping Genome Res. 2010, 6, 733-744
23. 1 Mice (Feed Study); National Toxicology Program Technical Report Series No. 215; National Toxicology Program: Research Triangle Park, NC, 1982. Available: http://ntp.niehs.nih.gov/ntp/htdocs/LT-rpts/tr215.pdf.
24. Adlercreutz, H.; Markkanen, H.; Watanabe, S. Plasma concentrations of phyto-oestrogens in Japanese men Lancet 1993, 342, 1209-1210
25. Qian, W-J; Kaleta, D. T.; Petritis, B. O.; Jiang, H.; Liu, T.; Zhang, X.; Mottaz, H. M.; Varnum, S. M.; Camp, D. G., 2nd; Huang, L.; Fang, X.; Zhang, W. W.; Smith, R. D. Enhanced detection of low abundance human plasma proteins using a tandem IgY-super-mix immunoaffinity separation strategy Mol. Cell. Proteomics 2008, 7, 1963-1973
26. Dayon, L.; Hainard, A.; Licker, V.; Turck, N.; Kuhn, K.; Hochstrasser, D. F.; Burkhard, P. R.; Sanchez, J. C. Relative quantification of proteins in human cerebrospinal fluids by MS/MS using 6-plex isobaric tags Anal. Chem. 2008, 80 (8) 2921-2931
27. Keller, A.; Nesvizhskii, A. I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search Anal. Chem. 2002, 74 (20) 5383-5392
28. Nesvizhskii, A. I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry Anal. Chem. 2003, 75 (17) 4646-4658
29. Weatherly, D. B.; Atwood, J. A., III; Minning, T. A.; Cavola, C.; Tarleton, R. L.; Orlando, R. A Heuristic Method for Assigning a False-discovery Rate for Protein Identifications from Mascot Database Search Results Mol. Cell. Proteomics 2005, 4 (6) 762-772
30. Rowell, C.; Carpenter, D. M.; Lamartiniere, C. A. Chemoprevention of breast cancer, proteomic discovery of genistein action in the rat mammary gland J. Nutr. 2005, 135, 2953S-2959S
31. Golub, T. R.; slonim, D. K.; Tamayo, P.; Huard, C.; Gaasenbeek, M.; Mesirov, J. P. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring Science 1999, 286 (5439) 531-537
32. Kachigan, S. Multivariate Statistical Analysis: A Conceptual Introduction, 2 nd ed.; Radius Press: New York, 1991.
33. CDC-Breast Cancer Statistics. www.cdc.gov/cancer/breast/statistics.
34. Colditz, G. A.; Frazier, A. L. Models of breast cancer show that risk is set by events of early life: prevention efforts must shift focus Cancer Epidemiol., Biomarkers Prev. 1995, 5, 567-571
35. Lamartiniere, C. A.; Jenkins, S.; Betancourt, A. M.; Wang, J.; Russo, J. Exposure to the Endocrine Disruptor Bisphenol A Alters Susceptibility for Mammary Cancer Horm. Mol. Biol. Clin. Invest. 2011, 5 (2) 45-52
36. Jenkins, S.; Wang, J.; Eltoum, I.; Desmond, R.; Lamartiniere, C. A. Chronic oral exposure to bisphenol A results in a nonmonotonic dose response in mammary carcinogenesis and metastasis in MMTV-erbB2 mice Environm. Health Perspect. 2011, 119 (11) 1604-1609
37. Betancourt, A. M.; Wang, J.; Jenkins, S.; Mobley, J. A.; Russo, J.; Lamartiniere, C. A. Altered carcinogenesis and proteome in mammary glands of rats after prepubertal exposures to the hormonally active chemicals bisphenol A and genistein J. Nutr. 2012, 142, 1382S-1388S
38. Hortin, G. L.; Sviridov, D.; Anderson, N. L. High-Abundance Polypeptides of the Human Plasma Proteome Comprising the Top 4 Logs of Polypeptide Abundance Clin. Chem. 2008, 54 (10) 1608-1616
39. Tabb, D. L.; Vega-Montoto, L.; Rudnick, P. A.; Variyath, A. M.; Ham, A-JL; Bunk, D. M.; Kilpatrick, L. E.; Dean, D. Repeatability and Reproducibility in Proteomic Identifications by Liquid Chromatography-Tandem Mass Spectrometry J. Proteome Res. 2010, 9 (2) 761-776
40. Wühr, M.; Haas, W.; McAlister, G. C.; Peshkin, L.; Rad, R.; Kirschner, M. W.; Gygi, S. P. Accurate Multiplexed Proteomics at the MS2 Level Using the Complement Reporter Ion Cluster Anal. Chem. 2012, 84 (21) 9214-9221
41. He, J.; Mao, C. C.; Reyes, A.; Sembongi, H.; Di Re, M.; Granycome, C.; Clippingdale, A. B.; Fearnely, I. M.; Harbour, M.; Robinson, A. J.; Reichelt, S.; Spelbrink, J. N.; Walker, J. E.; Holt, I. J. The AAA protein ATAD3 has displacement loop binding properties and is involved in mitochondrial nucleoid organization. J. Cell Biol. 176: 141-146
42. Fang, H.-Y.; Chang, C.-L.; Hsu, S.-H.; Huang, C.-Y.; Chiang, S.-F.; Chiou, S.-H.; Huang, C.-H.; Hsiao, Y.-T.; Lin, T.-Y.; Chiang, I.-P.; Hsu, W.-H.; Sugano, S.; Chen, C.-Y.; Lin, C.-Y.; Ko, W.-J.; Chow, K.-C. ATPase family AAA domain-containing 3A is a novel anti-apoptotic factor in lung adenocarcinoma cells J. Cell Sci. 2010, 123, 1171-1180
43. Muñoz-de-Toro, M.; Markey, C. M.; Wadia, P. R.; Luque, E. H.; Rubin, B. S.; Sonnenschein, C.; Soto, A. M. Perinatal exposure to bisphenol A alters peripubertal mammary gland development in mice Endocrinology 2005, 146 (9) 4138-4147
44. Holbro, T.; Beerli, R. R.; Maurer, F.; Koziczak, M.; Barbas, C. F., 3rd; Hynes, N. E. The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation Proc. Natl. Acad. Sci. 2003, 100, 8933-8938
45. Carraway, K. L., 3rd; Cantley, L. C. A new acquaintance for erbB3 and erbB4: a role for receptor heterodimerization in growth signaling Cell 1994, 78, 5-8
46. Fedi, P.; Pierce, J. H.; di Fiore, P. P.; Kraus, M. H. Efficient coupling with phosphatidylinositol 3-kinase, but not phospholipase C gamma or GTPase-activating protein, distinguishes ErbB-3 signaling from that of other ErbB/EGFR family members Mol. Cell. Biol. 1994, 14, 492-500
47. Vijapurkar, U.; Kim, M. S.; Koland, J. G. Roles of mitogen-activated protein kinase and phosphoinositide 3′-kinase in ErbB2/ ErbB3 coreceptor-mediated heregulin signaling Exp. Cell Res. 2003, 284, 291-302
48. Huguet, E. L.; McMahon, J. A.; McMahon, A. P.; Bicknell, R.; Harris, A. L. Differential expression of human Wnt genes 2, 3, 4 and 7B in human breast cell lines and normal and disease states of human breast tissue Cancer Res. 1994, 54 (10) 2615-2621
49. Zhu, C. Q.; Popova, S. N.; Brown, E. R.; Barsyte-Lovejoy, D.; Navab, R.; Shih, W.; Li, M.; Lu, M.; Jurisca, I.; Penn, L. Z.; Gullberg, D.; Tsao, M. S. Integrin alpha 11 regulates IGF2 expression in fibroblasts to enhance tumorigenicity of human non-small-cell lung cancer cells Proc. Natl. Acad. Sci. 2007, 104 (28) 11754-11759
50. Mao, J.; Xu, Z.; Fang, Y.; Wang, H.; Xu, J.; Ye, J.; Zheng, S.; Zhu, Y. Hepatoma-derived growth factor involved in the carcinogenesis of gastric epithelial cells through promotion of cell proliferation by Erk1/2 activation Cancer Sci. 2008, 99 (11) 2120-2127
51. Korkolopoulou, P.; Givalos, N.; Saetta, A.; Goudopoulou, A.; Gakiopoulou, H.; Thymara, I.; Thomas-Tsagli, E.; Patsouris, E. Minichromosome maintenance proteins 2 and 5 expression in muscle-invasive urothelial cancer: a multivariate survival study including proliferation markers and cell cycle regulators Hum. Pathol. 2005, 36 (8) 899-907
52. Robinson, Dr. Functionally recurrent rearrangements of the MAST kinase and Notch gene families in breast cancer Nat. Med. 2011, 17 (12) 1646-1651
53. Zeng, Y.; Abdallah, A.; Lu, J-P; Wang, T.; Chen, Y-H; Terrian, D. M.; Kim, K.; Lu, Q. δ-Catenin promotes prostate cancer cell growth and progression by altering cell cycle and survival gene profiles Mol. Cancer 2009, 8, 19
54. Conde, I.; Lobo, M. V.; Zamora, J.; Pérez, J.; González, F. J.; Alba, E.; Fraile, B.; Paniagua, R.; Arenas, M. I. Human pregnane X receptor is expressed in breast carcinomas, potential heterodimers formation between hPXR and RXR-alpha BMC Cancer 2008, 8, 174
55. Spilka, R.; Laimer, K.; Bachmann, F.; Spizzo, G.; Vogetseder, A.; Wiesser, M.; Muller, H.; Hayback, J.; Obrist, P. Overexpression of eIF3a in squamous cell carcinoma of the oral cavity and its putative relation to chemotherapy response J. Oncol. 2012, 2012, 901956
56. Shibao, K.; Fiedler, M. J.; Nagata, J.; Minagawa, N.; Hirata, K.; Nakayama, Y.; Iwakiri, Y.; Nathanson, M. H.; Yamaguchi, K. The type III inositol 1,4,5-trisphosphate receptor is associated with aggressiveness of colorectal carcinoma Cell Calcium 2010, 48 (6) 315-323
57. Deltour, S.; Pinte, S.; Guerardel, C.; Leprince, D. Characterization of HRG22, a human homologue of the putative tumor suppressor gene HIC1 Biochem. Biophys. Res. Commun. 2001, 287, 427-434
58. Chen, W Y; Zeng, X.; Carter, M. G.; Morrell, C. N.; Yen, R-W C; Esteller, M.; Watkins, D. N.; Herman, J. G.; Mankowski, J. L.; Baylin, S. B. Heterozygous disruption of Hic1 predisposes mice to a gender-dependent spectrum of malignant tumors Nat. Genet. 2003, 33, 197-202
59. Jackson, R. S., 2nd; Cho, Y. J.; Stein, S.; Liang, P. CYFIP2, a direct target p53 target is leptomycin-B sensitive Cell Cycle 2007, 6 (1) 95-103
60. Yano, M.; Naito, Z.; Tanaka, S.; Asano, G. Expression and roles of heat shock proteins in human breast cancer Jpn. J. Cancer Res. 1996, 87, 908-915
61. Kim, T.; Keum, G.; Pae, A. N. Discovery and development of heat shock protein 90 inhibitors as anticancer agents: a review of patented potent geldanamycin derivatives Expert Opin. Ther. Pat. 2013, 0, 1-25
62. Koga, F.; Kihara, K.; Neckers, L. Inhibition of cancer invasion and metastasis by targeting the molecular chaperone heat-shock protein 90 Anticancer Res. 2009, 3, 797-807
63. Betancourt, A. M.; Mobley, J. A.; Russo, J.; Lamartiniere, C. A. Proteomic analysis in mammary glands of rat offspring exposed in utero to bisphenol A J. Proteomics 2010, 73, 1241-1253
64. Ellison-Zelski, S. J.; Alarid, E. T. Maximum growth and survival of estrogen receptor-alpha positive breast cancer cells requires the Sin3A transcriptional repressor Mol. Cancer 2010, 9, 263
65. Yi, J. K.; Chang, J. W.; Han, W.; Lee, J. W.; Ko, E.; Kim, D. H.; Bae, J. Y.; Yu, J.; Lee, C.; Yu, M. H.; Noh, D. Y. Autoantibody to tumor antigen, alpha 2-HS glycoprotein: a novel biomarker of breast cancer screening and diagnosis Cancer Epidemiol. Biomarkers Prev. 2009, 18 (5) 1357-1364
66. Guillory, B.; Sakwe, A. M.; Saria, M.; Thompson, P.; Adhiambo, C.; Koumangoye, R.; Ballard, B.; Binhazim, A.; Cone, C.; Jahanen-Dechent, W.; Ochieng, J. Lack of Fetuin-A (α2-HSGlycoprotein) Reduces Mammary Tumor Incidence and Prolongs Tumor Latency via the Transforming Growth Factor-β Signaling Pathway in a Mouse Model of Breast Cancer Am. J. Pathol. 2010, 177 (5) 2635-2644
67. Correia, A. L.; Mori, H.; Chen, E. I.; Schmitt, F. C.; Bissell, M. J. The hemopexin domain of MMP3 is responsible for mammary epithelial invasion and morphogenesis through extracellular interaction with HSP90β Genes Dev. 2013, 27, 805-817
68. Radisky, D. C.; Fata, J.; Levy, D., Matrix Metalloproteinase 3 Causes Genomic Instability and Epithelial-to-Mesenchymal Transition through Induction of Reactive Oxygen Species. Program and Abstracts of the Annual Meeting of the American Society for Cell Biology, San Francisco, CA, December 2003.
69. Bourguignon, L. Y.; Zhu, H.; Shao, L. Rho-kinase (ROK) promotes CD44v(3,8-10)-ankyrin interaction and tumor cell migration in metastatic breast cancer cells Cell Motil. Cytoskeleton 1999, 43, 269-287
70. Matsumoto, T.; Kawashima, Y.; Nagashio, R.; Kageyama, T.; Kodera, Y.; Jiang, S. X.; Okayasu, I.; Kaneya, T.; Sato, T. A new possible lung cancer marker: VGF detection from the conditioned medium of pulmonary large cell neuroendocrine carcinoma-derived cells using secretoma analysis Int. J. Biol. Markers 2009, 4, 282-285
71. Farshchian, M.; Kivisaari, A.; Ala-aho, R.; Riihilä, P.; Kallajoki, M.; Grénman, R.; Peltonen, J.; Pihlajaniemi, T.; Heljasvaara, R.; Kähäri, V. M. Serpin peptidase inhibitor clade A member 1 as a potential marker for malignancy in isulinomas Clin. Cancer Res. 2007, 13, 5322-5330
72. Yu, J.; Tao, Q.; Cheung, K. F.; Jin, H.; Poon, F. F.; Wang, X.; Li, H.; Cheng, Y. Y.; Röcken, C.; Ebert, M. P.; Chan, A. T.; Sung, J. J. Epigenetic identification of ubiquitin carboxy-terminal hydrolase L1 as a functional tumor suppressor Hepatology 2008, 48 (2) 508-518
73. Duns, G.; van den Berg, E.; van Duivenbode, I.; Osinga, J.; Hollema, H.; Hofstra, R. M.; Kok, K. Histone methyltransferase gene SETD2 is a novel tumor suppressor in clear cell renal cell carcinoma Cancer Res. 2010, 70 (11) 4287-4291
74. Sun, P. H.; Ye, L.; Mason, M. D.; Jiang, W. G. Protein tyrosine phosphatase kappa (PTPRK) is a negative regulator of adhesion and invasion of breast cancer cells, and associates with poor prognosis of breast cancer J. Cancer Res. Clin. Oncol. 2013, 139 (7) 1129-1139
75. Chen, W. F.; Huang, M. H.; Tzang, C. H.; Yang, M.; Wong, M. S. Inhibitory actions of genistein in human breast cancer (MCF-7) cells Biochem. Biophis. Acta 2003, 14:1638 (2) 187-196
76. Chen, J.-S.; Su, I.-J.; Leu, Y.-W.; Young, K.-C.; Sun, H. S. Expression of T-cell lymphoma invasion and metastasis 2 (TIAM2) promotes proliferation and invasion of liver cancer Int. J. Cancer 2012, 130 (6) 1302-1313
77. Berry, W. L.; Shin, S.; Lightfoot, S. A.; Janknecht, R. Oncogenic features of the JMJD2A histone demethylase in breast cancer Int. J. Oncol. 2012, 41 (5) 1701-1706