Mitochondrial localization of ERα and ERβ in human MCF7 cells

American Journal of Physiology - Endocrinology and Metabolism

Volumn 286, Issue 6 49-6, 2004, Pages

  Chen, Jin Q ^a,c   Delannoy, Michael ^b   Cooke, Carol ^b   Yager, James D ^a  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c FOX CHASE CANCER CENTER   (United States)

Author keywords

17 estradiol; Mitochondrial deoxyribonucleic acid transcription; Mitochondrial deoxyribonucleic acid encoded genes

Indexed keywords

CYTOCHROME C OXIDASE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FULVESTRANT; MITOCHONDRIAL DNA; ANTIESTROGEN; DRUG DERIVATIVE; ESTROGEN RECEPTOR; SIGNAL PEPTIDE;

ARTICLE; CELL FRACTIONATION; CELL STRAIN HEPG2; CELL STRAIN MCF 7; COMPUTER ANALYSIS; CONCENTRATION RESPONSE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOGOLD ELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; LIVER CELL; MITOCHONDRION; NORTHERN BLOTTING; PRIORITY JOURNAL; RESPIRATORY CHAIN; WESTERN BLOTTING; ANTIBODY SPECIFICITY; BREAST TUMOR; CELL NUCLEUS; DRUG EFFECT; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETICS; IMMUNOELECTRON MICROSCOPY; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE; ULTRASTRUCTURE;

ANTIBODY SPECIFICITY; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL NUCLEUS; DNA, MITOCHONDRIAL; ESTRADIOL; ESTROGEN ANTAGONISTS; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GENE EXPRESSION; HUMANS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; MITOCHONDRIA; PROTEIN SORTING SIGNALS; RECEPTORS, ESTROGEN; SUBCELLULAR FRACTIONS; TRANSCRIPTION, GENETIC;

EID: 2442636791     PISSN: 01931849     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpendo.00508.2003     Document Type: Article

References (75)

1. Adams JY, Leav I, Lau KM, Ho SM, and Pflueger SM. Expression of estrogen receptor beta in the fetal, neonatal, and prepubertal human prostate. Prostate 52: 69-81, 2002.
2. Alves SE, Lopez V, McEwen BS, and Weiland NG. Differential colocalization of estrogen receptor beta (ERbeta) with oxytocin and vasopressin in the paraventricular and supraoptic nuclei of the female rat brain: an immunocytochemical study. Proc Natl Acad Sci USA 95: 3281-3286, 1998.
3. Bettini E and Maggi A. Estrogen induction of cytochrome c oxidase subunit III in rat hippocampus. J Neurochem 58: 1923-1929, 1992.
4. Bord S, Horner A, Beavan S, and Compston J. Estrogen receptors alpha and beta are differentially expressed in developing human bone. J Clin Endocrinol Metab 86: 2309-2314, 2001.
5. Bukovsky A, Caudle MR, Cekanova M, Fernando RI, Wimalasena J, Foster JS, Henley DC, and Elder RF. Placental expression of estrogen receptor beta and its hormone binding variant-comparison with estrogen receptor alpha and a role for estrogen receptors in asymmetric division and differentiation of estrogen-dependent cells (Abstract). Reprod Biol Endocrinol 1: 36, 2003.
6. Casas F, Rochard P, Rodier A, Cassar-Malek I, Marchal-Victorion S, Wiesner RJ, Cabello G, and Wrutniak C. A variant form of the nuclear triiodothyronine receptor c-ErbAalpha1 plays a direct role in regulation of mitochondrial RNA synthesis. Mol Cell Biol 19: 7913-7924, 1999.
7. Chen J, Delannoy M, Odwin S, He P, Trush MA, and Yager JD. Enhanced mitochondrial gene transcript, ATP, Bcl-2 protein levels, and altered glutathione distribution in ethinyl estradiol-treated cultured female rat hepatocytes. Toxicol Sci 75: 271-278, 2003.
8. Chen J, Gokhale M, Li Y, Trush MA, and Yager JD. Enhanced levels of several mitochondrial mRNA transcripts and mitochondrial superoxide production during ethinyl estradiol-induced hepatocarcinogenesis and after estrogen treatment of HepG2 cells. Carcinogenesis 19: 2187-2193, 1998.
9. Chen J, Gokhale M, Schofield B, Odwin S, and Yager JD. Inhibition of TGF-beta-induced apoptosis by ethinyl estradiol in cultured, precision cut rat liver slices and hepatocytes. Carcinogenesis 21: 1205-1211, 2000.
10. Chen J, Li Y, Lavigne JA, Trush MA, and Yager JD. Increased mitochondrial superoxide production in rat liver mitochondria, rat hepatocytes, and HepG2 cells following ethinyl estradiol treatment. Toxicol Sci 51: 224-235, 1999.
11. Chen J, Schwartz DA, Young TA, Norris JS, and Yager JD. Identification of genes whose expression is altered during mitosuppression in livers of ethinyl estradiol-treated female rats. Carcinogenesis 17: 2783-2786, 1996.
12. Cheng X, Cole RN, Zaia J, and Hart GW. Alternative O-glycosylation/O-phosphorylation of the murine estrogen receptor beta. Biochemistry 39: 11609-11620, 2000.
13. Cheng X and Hart GW. Glycosylation of the murine estrogen receptor-alpha. J Steroid Biochem Mol Biol 75: 147-158, 2000.
14. Cheng X and Hart GW. Alternative O-glycosylation/O-phosphorylation of serine-16 in murine estrogen receptor beta: post-translational regulation of turnover and transactivation activity. J Biol Chem 276: 10570-10575, 2001.
15. Chi A, Chen X, Chirala M, and Younes M. Differential expression of estrogen receptor beta isoforms in human breast cancer tissue. Anticancer Res 23: 211-216, 2003.
16. Choi I, Ko C, Park-Sarge OK, Nie R, Hess RA, Graves C, and Katzenellenbogen BS. Human estrogen receptor beta-specific monoclonal antibodies: characterization and use in studies of estrogen receptor beta protein expression in reproductive tissues. Mol Cell Endocrinol 181: 139-150, 2001.
17. Clanton DA. Replication and transcription of vertebrate mitochondrial DNA. Annu Rev Cell Biol 7: 453-478, 1991.
18. Davis AJ, Ryan KR, and Jensen RE. Tim23p contains separate and distinct signals for targeting to mitochondria and insertion into the inner membrane. Mol Biol Cell 9: 2577-2593, 1998.
19. Demonacos C, Djordjevic-Markovic R, Tsawdaroglou N, and Sekeris CE. The mitochondrion as a primary site of action of glucocorticoids: the interaction of the glucocorticoid receptor with mitochondrial DNA sequences showing partial similarity to the nuclear glucocorticoid responsive elements. J Steroid Biochem Mol Biol 55: 43-55, 1995.
20. Demonacos C, Tsawdaroglou NC, Djordjevic-Markovic R, Papalopoulou M, Galanopoulos V, Papadogeorgaki S, and Sekeris CE. Import of the glucocorticoid receptor into rat liver mitochondria in vivo and in vitro. J Steroid Biochem Mol Biol 46: 401-413, 1993.
21. Demonacos CV, Karayanni N, Hatzoglou E, Tsiriyiotis C, Spandidos DA, and Sekeris CE. Mitochondrial genes as sites of primary action of steroid hormones. Steroids 61: 226-232, 1996.
22. Emanuelsson O, Nielsen H, Brunak S, and von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016, 2000.
23. Enmark E and Gustafsson JA. Oestrogen receptors: an overview. J Intern Med 246: 133-138, 1999.
24. Enriquez JA, Fernandez-Silva P, Garrido-Perez N, Lopez-Perez MJ, Perez-Martos A, and Montoya J. Direct regulation of mitochondrial RNA synthesis by thyroid hormone. Mol Cell Biol 19: 657-670, 1999.
25. Folsch H, Guiard B, Neupert W, and Stuart RA. Internal targeting signal of the BCS1 protein: a novel mechanism of import into mitochondria. EMBO J 15: 479-487, 1996.
26. Garcia Pedrero JM, del Rio B, Martinez-Campa C, Muramatsu M, Lazo PS, and Ramos S. Calmodulin is a selective modulator of estrogen receptors. Mol Endocrinol 16: 947-960, 2002.
27. Green S, Walter P, Greene G, Krust A, Goffin C, Jensen E, Scrace G, Waterfield M, and Chambon P. Cloning of the human oestrogen receptor cDNA. J Steroid Biochem 24: 77-83, 1986.
28. Green S, Walter P, Kumar V, Krust A, Bornert JM, Argos P, and Chambon P. Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A. Nature 320: 134-139, 1986.
29. Grossman A, Oppenheim J, Grondin G, St. Jean P, and Beaudoin AR. Immunocytochemical localization of the [3H]estradiol-binding protein in rat pancreatic acinar cells. Endocrinology 124: 2857-2866, 1989.
30. Hartl FU, Pfanner N, Nicholson DW, and Neupert W. Mitochondrial protein import. Biochim Biophys Acta 988: 1-45, 1989.
31. Inoue H, Shimizu I, Lu G, Itonaga M, Cui X, Okamura Y, Shono M, Honda H, Inoue S, Muramatsu M, and Ito S. Idoxifene and estradiol enhance antiapoptotic activity through estrogen receptor-beta in cultured rat hepatocytes. Dig Dis Sci 48: 570-580, 2003.
32. Ioannou IM, Tsawdaroglou N, and Sekeris CE. Presence of glucocorticoid responsive elements in the mitochondrial genome. Anticancer Res 8: 1405-1409, 1988.
33. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, and Gustafsson JA. Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA 93: 5925-5930, 1996.
34. Lane MA, Romagnoli L, Cruise B, and Cohn GM. Spontaneous conversion to estrogen receptor expression by the human breast epithelial cell line, MCF-10A. Oncol Rep 6: 507-511, 1999.
35. Law SW, Apostolakis EM, Samora PJ, O'Malley BW, and Clark JH. Hormonal regulation of hypothalamic gene expression: identification of multiple novel estrogen induced genes. J Steroid Biochem Mol Biol 51: 131-136, 1994.
36. Leav I, Lau KM, Adams JY, McNeal JE, Taplin ME, Wang J, Singh H, and Ho SM. Comparative studies of the estrogen receptors beta and alpha and the androgen receptor in normal human prostate glands, dysplasia, and in primary and metastatic carcinoma. Am J Pathol 159: 79-92, 2001.
37. Lee SH. Coexistence of cytoplasmic and nuclear estrogen receptors. A histochemical study on human mammary cancer and rabbit uterus. Cancer 64: 1461-1466, 1989.
38. Li X, Schwartz PE, and Rissman EF. Distribution of estrogen receptor-beta-like immunoreactivity in rat forebrain. Neuroendocrinology 66: 63-67, 1997.
39. Mann S, Laucirica R, Carlson N, Younes PS, Ali N, Younes A, Li Y, and Younes M. Estrogen receptor beta expression in invasive breast cancer. Hum Pathol 32: 113-118, 2001.
40. Marchetti E, Querzoli P, Moncharmont B, Parikh I, Bagni A, Marzola A, Fabris G, and Nenci I. Immunocytochemical demonstration of estrogen receptors by monoclonal antibodies in human breast cancer: correlation with estrogen receptor assay by dextran-coated charcoal method. Cancer Res 47: 2508-25013, 1987.
41. Matsuda T, Yamamoto T, Muraguchi A, and Saatcioglu F. Cross-talk between transforming growth factor-beta and estrogen receptor signaling through Smad3. J Biol Chem 276: 42908-42914, 2001.
42. Matsuyama S, Ohkura Y, Eguchi H, Kobayashi Y, Akagi K, Uchida K, Nakachi K, Gustafsson JA, and Hayashi S. Estrogen receptor beta is expressed in human stomach adenocarcinoma. J Cancer Res Clin Oncol 128: 319-324, 2002.
43. Milici AJ, Watrous NE, Stukenbrok H, and Palade GE. Transcytosis of albumin in capillary endothelium. J Cell Biol 105: 2603-2612, 1987.
44. Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, Hayashi S, Pfaff DW, Ogawa S, Rohrer SP, Schaeffer JM, McEwen BS, and Alves SE. Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 144: 2055-2067, 2003.
45. Moats RK II and Ramirez VD. Electron microscopic visualization of membrane-mediated uptake and translocation of estrogen-BSA:colloidal gold by hep G2 cells. J Endocrinol 166: 631-647, 2000.
46. Monje P and Boland R. Characterization of membrane estrogen binding proteins from rabbit uterus. Mol Cell Endocrinol 147: 75-84, 1999.
47. Monje P and Boland R. Subcellular distribution of native estrogen receptor alpha and beta isoforms in rabbit uterus and ovary. J Cell Biochem 82: 467-479, 2001.
48. Monje P, Zanello S, Holick M, and Boland R. Differential cellular localization of estrogen receptor alpha in uterine and mammary cells. Mol Cell Endocrinol 181: 117-129, 2001.
49. Mosselman S, Polman J, and Dijkema R. ER beta: identification and characterization of a novel human estrogen receptor. FEBS Lett 392: 49-53, 1996.
50. Moutsatsou P, Psarra AM, Tsiapara A, Paraskevakou H, Davaris P, and Sekeris CE. Localization of the glucocorticoid receptor in rat brain mitochondria. Arch Biochem Biophys 386: 69-78, 2001.
51. Nealen ML, Vijayan KV, Bolton E, and Bray PF. Human platelets contain a glycosylated estrogen receptor beta. Circ Res 88: 438-442, 2001.
52. Norfleet AM, Clarke CH, Gametchu B, and Watson CS. Antibodies to the estrogen receptor-alpha modulate rapid prolactin release from rat pituitary tumor cells through plasma membrane estrogen receptors. FASEB J 14: 157-165, 2000.
53. Noteboom WD and Gorski J. Stereospecific binding of estrogens in the rat uterus. Arch Biochem Biophys 111: 559-568, 1965.
54. Ogawa S, Inoue S, Watanabe T, Hiroi H, Orimo A, Hosoi T, Ouchi Y, and Muramatsu M. The complete primary structure of human estrogen receptor beta (hER beta) and its heterodimerization with ER alpha in vivo and in vitro. Biochem Biophys Res Commun 243: 122-126, 1998.
55. Pedersen PL, Greenawalt JW, Reynafarje B, Hullihen J, Decker GL, Soper JW, and Bustamente E. Preparation and characterization of mitochondria and submitochondrial particles of rat liver and liver-derived tissues. Methods Cell Biol 20: 411-481, 1978.
56. Price RH Jr and Handa RJ. Expression of estrogen receptor-beta protein and mRNA in the cerebellum of the rat. Neurosci Lett 289: 115-118, 2000.
57. Psarra AM, Bochaton-Piallat ML, Gabbiani G, Sekeris CE, and Tsacopoulos M. Mitochondrial localization of glucocortocoid receptor in glial (Muller) cells in the salamander retina. Glia 41: 38-49, 2003.
58. Razandi M, Pedram A, Greene GL, and Levin ER. Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERalpha and ERbeta expressed in Chinese hamster ovary cells. Mol Endocrinol 13: 307-319, 1999.
59. Rosenfeld CS, Ganjam VK, Taylor JA, Yuan X, Stiehr JR, Hardy MP, and Lubahn DB. Transcription and translation of estrogen receptor-beta in the male reproductive tract of estrogen receptor-alpha knock-out and wild-type mice. Endocrinology 139: 2982-2987, 1998.
60. Sauders PTK, Maguire SM, Gaughan J, and Miller MR. Expression of oestrogen receptor beta (ERb) in multiple rat tissues visualized by immunohistochemistry. J Endocrinol 154: R13-R16, 1997.
61. Scheller K, Seibel P, and Sekeris CE. Glucocorticoid and thyroid hormone receptors in mitochondria of animal cells. Int Rev Cytol 222: 1-61, 2003.
62. Scheller K and Sekeris CE. The effects of steroid hormones on the transcription of genes encoding enzymes of oxidative phosphorylation. Exp Physiol 88: 129-140, 2003.
63. Scheller K, Sekeris CE, Krohne G, Hock R, Hansen IA, and Scheer U. Localization of glucocorticoid hormone receptors in mitochondria of human cells. Eur J Cell Biol 79: 299-307, 2000.
64. Sekeris CE. The mitochondrial genome: a possible primary site of action of steroid hormones. In Vivo 4: 317-320, 1990.
65. Sierrata WD, Bonig I, and Thole HH. Immunolabeling of estrogen receptors in MCF-7 cells. Cell Tissue Res 279: 445-452, 1995.
66. Simonian SX and Herbison AW. Differential expression of estrogen receptor alpha and beta immunoreactivity by oxytocin neurons of rat paraventricular nucleus. J Neuroendocrinol 9: 803-806, 1997.
67. Taylor AH and Al-Azzawi F. Immunolocalisation of oestrogen receptor beta in human tissues. J Mol Endocrinol 24: 145-155, 2000.
68. Tsiriyotis C, Spandidos DA, and Sekeris CE. The mitochondrion as a primary site of action of glucocorticoids: mitochondrial nucleotide sequences, showing similarity to hormone response elements, confer dexamethasone inducibility to chimaeric genes transfected in LATK- cells. Biochem Biophys Res Commun 235: 349-354, 1997.
69. Van Itallie CM and Dannies PS. Estrogen induces accumulation of the mitochondrial ribonucleic acid for subunit II of cytochrome oxidase in pituitary tumor cells. Mol Endocrinol 2: 332-337, 1988.
70. Vidal O, Kindblom LG, and Ohlsson C. Expression and localization of estrogen receptor-beta in murine and human bone. J Bone Miner Res 14: 923-929, 1999.
71. Wang J, Silva JP, Gustafsson CM, Rustin P, and Larsson NG. Increased in vivo apoptosis in cells lacking mitochondrial DNA gene expression. Proc Natl Acad Sci USA 98: 4038-4043, 2001.
72. Willingham MC. Fluorescence labeling of intracellular antigens of attached or suspended tissue-culture cells. Methods Mol Biol 115: 121-130, 1999.
73. Witte D, Chirala M, Younes A, Li Y, and Younes M. Estrogen receptor beta is expressed in human colorectal adenocarcinoma. Hum Pathol 32: 940-944, 2001.
74. Wrutniak C, Cassar-Malek I, Marchal S, Rascle A, Heusser S, Keller JM, Flechon J, Dauca M, Samarut J, Ghysdael J, and Cabello G. A 43-kDa protein related to c-Erb A alpha 1 is located in the mitochondrial matrix of rat liver. J Biol Chem 270: 16347-16354, 1995.
75. Zhang JQ, Cal WQ, Zhou de S, and Su BY. Distribution and differences of estrogen receptor beta immunoreactivity in the brain of adult male and female rats. Brain Res 935: 73-80, 2002.