Progestin stimulation of manganese superoxide dismutase and invasive properties in T47D human breast cancer cells

Journal of Steroid Biochemistry and Molecular Biology

Volumn 117, Issue 1-3, 2009, Pages 23-30

  Holley, Aaron K ^a   Kiningham, Kelley K ^b   Spitz, Douglas R ^c   Edwards, Dean P ^d   Jenkins, Jeffrey T ^a   Moore, Michael R ^a  

^a MARSHALL UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BELMONT UNIVERSITY   (United States)

^c UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Breast cancer; Manganese superoxide dismutase; Progesterone; T47D cells

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; CYCLOHEXIMIDE; GESTAGEN; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; MIFEPRISTONE; MITOGEN ACTIVATED PROTEIN KINASE; SMALL INTERFERING RNA;

ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER INHIBITION; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVITY; HORMONAL REGULATION; HORMONE INHIBITION; HUMAN; HUMAN CELL; PROTEIN SYNTHESIS INHIBITION; SIGNAL TRANSDUCTION; UPREGULATION;

BASE SEQUENCE; BREAST NEOPLASMS; BUTADIENES; CELL LINE, TUMOR; DNA PRIMERS; FEMALE; HORMONE ANTAGONISTS; HUMANS; MAP KINASE SIGNALING SYSTEM; MIFEPRISTONE; NEOPLASM INVASIVENESS; NITRILES; PROGESTERONE CONGENERS; PROMEGESTONE; RECEPTORS, PROGESTERONE; RNA, MESSENGER; RNA, NEOPLASM; RNA, SMALL INTERFERING; SUPEROXIDE DISMUTASE;

MAMMALIA;

EID: 70249092495     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2009.06.004     Document Type: Article

References (69)

1. McCord J.M., and Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244 (1969) 6049-6055
2. Weisiger R.A., and Fridovich I. Mitochondrial superoxide dismutase. Site of synthesis and intramitochondrial localization. J. Biol. Chem. 248 (1973) 4793-4796
3. Schacter L., Warth J.A., Gordon E.M., Prasad A., and Klein B.L. Altered amount and activity of superoxide dismutase in sickle cell anemia. FASEB J. 2 (1998) 237-243
4. Rothstein J.D., Bristol L.A., Hosler B., Brown Jr. R.H., and Kuncl R.W. Chronic inhibition of superoxide dismutase produces apoptotic death of spinal neuron. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 4155-4159
5. Hough M.A., Grossman J.G., Antonyuk S.V., Strange R.W., Doucette P.A., Rodriguez J.A., Whitson L.J., Hart P.J., Hayward L.J., Valentine J.S., and Hasnain S.S. Dimer destabilization in superoxide dismutase may result in disease-causing properties: structures of motor neuron disease mutants. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 5976-5981
6. Rakhit R., Crow J.P., Lepock J.R., Kondejewski L.H., Cashman N.R., and Chakrabartty A. Monomeric Cu,Zn-superoxide dismutase is a common misfolding intermediate in the oxidation models of sporadic and familial amyotrophic lateral sclerosis. J. Biol. Chem. 279 (2004) 15499-15504
7. Choi J., Rees H.D., Weintraub S.T., Levey A.I., Chin L.S., and Li L. Oxidative modifications and aggregation of Cu/Zn superoxide dismutase associated with Alzheimer's and Parkinson's diseases. J. Biol. Chem. 280 (2005) 11648-11655
8. Lakari E., Pääkkö P., Pietarinen-Runtti P., and Kinnula V.L. Manganese superoxide dismutase and catalase are coordinately expressed in the alveolar region in chronic interstitial pneumonias and granulomatous diseases of the lung. Am. J. Resp. Crit. Care Med. 161 (2000) 615-621
9. Kinnula V.L., and Crapo J.L. Superoxide dismutases in the lung and human lung diseases. Am. J. Resp. Crit. Care Med. 167 (2003) 1600-1619
10. Janssen A.M.L., Bosman C.B., van Duijn W., Oostendorp-van de Ruit M.M., Kubben F.J.G.M., Griffioen G., Lamers C.B., van Krieken J.H., van de Velde C.J., and Verspaget H.W. Superoxide dismutases in gastric and esophageal cancer and the prognostic impact in gastric cancer. Clin. Cancer Res. 6 (2000) 3183-3192
11. Izutani R., Asano S., Imano M., Kuroda D., Kato M., and Ohyanagi H. Expression of manganese superoxide dismutase in esophageal and gastric cancers. J. Gastroenterol. 33 (1998) 816-822
12. Ho J.C., Zheng S., Comhair S.A.A., Farver C., and Erzurum S.C. Differential expression of manganese superoxide dismutase and catalase in lung cancer. Cancer Res. 6 (2001) 8578-8585
13. Palazotti B., PaniG G., Colavitti R., De Leo M.E., Bedogni B., Borrello S., and Galeotti T. Increased growth capacity of cervical carcinoma cells over-expressing manganous superoxide dismutase. Int. J. Cancer 82 (1999) 145-150
14. Hirose K., Longo D.L., Oppenheim J.J., and Matsushima K. Overexpression of mitochondrial manganese superoxide dismutase promotes the survival of tumor cells exposed to interleukin-1, tumor necrosis factor, selected anticancer drugs, and ionizing radiation. FASEB J. 7 (1993) 61-368
15. Church S.L., Grant J.W., Ridnour L.A., Oberley L.W., Swanson P.E., Meltzer P.S., and Trent J.M. Increased manganese superoxide dismutase expression suppresses the malignant phenotype of human melanoma cells. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 3113-3317
16. Cullen J.J., Weydert C., Hinkhouse M.M., Ritchie J., Domann F.E., Spitz D., and Oberley L.W. The role of manganese superoxide dismutase in the growth of pancreatic adenocarcinoma. Cancer Res. 63 (2003) 1297-1303
17. Mukhopadhyay S., Das S.K., and Mukherjee S. Expression of Mn-superoxide dismutase gene in non-tumorigenic and tumorigenic human mammary epithelial cells. J. Biomed. Biotech. 4 (2004) 195-202
18. Manna S.K., Zhang H.J., Yan T., Oberley L.W., and Aggarwal B.B. Over-expression of manganese superoxide dismutase suppresses tumor necrosis factor-induced apoptosis and activation of nuclear transcription factor-κB and activated protein-1. J. Biol. Chem. 273 (1998) 13245-13254
19. Li J.J., Colburn N.H., and Oberley L.W. Maspin gene expression in tumor suppression induced by overexpressing manganese-containing superoxide dismutase cDNA in human breast cancer cells. Carcinogenesis 19 (1998) 833-839
20. Tanaka T., Kurabayashi M., Aihara Y., Ohyama Y., and Nagai R. Inducible expression of manganese superoxide dismutase by phorbol 12-myristate 13-acetate is mediated by Sp1 in endothelial cells. Art. Throm. Vasc. Biol. 20 (2000) 392-401
21. Visner G.A., Dougall W.C., Wilson J.M., Burr I.A., and Nick H.S. Regulation of manganese superoxide dismutase by lipopolysaccharide, interleukin-1, and tumor necrosis factor: role in the acute inflammatory response. J. Biol. Chem. 265 (1900) 2856-2864
22. Sugino N., Hirosawa-Takamori M., Zhong L., Telleria C.M., Shiota K., and Gibori G. Hormonal regulation of copper-zinc superoxide dismutase and manganese superoxide dismutase messenger ribonucleic acid in the rat corpus luteum: induction by prolactin and placental lactogens. Biol. Reprod. 59 (1998) 599-605
23. Kasapović J., Pajović S.B., Pejić S., and Martinović J.V. Effects of estradiol benzoate and progesterone on superoxide dismutase activity in the thymus of rats. Physiol. Res. 50 (2001) 97-103
24. Sugino N., Karube-Harada A., Kashida S., Takiguchi S., and Kato H. Differential regulation of copper-zinc superoxide dismutase and manganese superoxide dismutase by progesterone withdrawal in human endometrial stromal cells. Mol. Human Reprod. 8 (2002) 68-74
25. Hagley R.D., and Moore M.R. A progestin effect on lactate dehydrogenase in the human breast cancer cell line T-47D. Biochem. Biophys. Res. Commun. 128 (1985) 520-524
26. Hagley R.D., Hissom J.R., and Moore M.R. Progestin stimulation of lactate dehydrogenase in the human breast cancer cell line T-47D. Biochim. Biophys. Acta 930 (1987) 167-172
27. Moore M.R., Hagley R.D., and Hissom J.R. Progestin effects on lactate dehydrogenase and growth in the human breast cancer cell line T47D. In: Hankins H.D., and Puett D. (Eds). Hormones, Cell Biology and Cancer, Perspectives and Potentials (1988), Alan R. Liss, Inc., New York 161-179
28. Hissom J.R., Bowden R.T., and Moore M.R. Effects of progestins, estrogens and antihormones on growth and lactate dehydrogenase in the human breast cancer cell line T47D. Endocrinology 125 (1989) 418-423
29. Moore M.R., Hathaway L.D., and Bircher J.A. Progestin stimulation of thymidine kinase in the human breast cancer cell line T47D. Biochim. Biophys. Acta 1096 (1991) 170-174
30. Moore M.R., Zhou J.-L., Blankenship K.A., Strobl J.S., Edwards D.P., and Gentry R.N. A sequence in the 5′ flanking region confers progestin responsiveness on the human c-myc gene. J. Steroid Biochem. Mol. Biol. 62 (1997) 243-252
31. Hissom J.R., and Moore M.R. Progestin effects on growth in the human breast cancer cell line T47D-possible therapeutic implications. Biochem. Biophys. Res. Commun. 145 (1987) 706-711
32. Bowden R.T., Hissom J.R., and Moore M.R. Growth stimulation of T47D human breast cancer cells by the antiprogestin RU486. Endocrinology 124 (1989) 2642-2644
33. Moore M.R., Conover J.L., and Franks K.M. Progestin effects on long-term growth, death, and Bcl-xL in breast cancer cells. Biochem Biophys. Res. Commun. 277 (2000) 650-654
34. Moore M.R., Spence J.B., Kiningham K.K., and Dillon J.L. Progestin inhibition of cell death in human breast cancer cell lines. J. Steroid Biochem. Mol. Biol. 98 (2006) 218-227
35. Ory K., Lebeau J., Levalois C., Bishay K., Fouchet P., Allemand I., and Therwath A. Chevillard, Apoptosis inhibition mediated by medroxyprogesterone acetate treatment of breast cancer cell lines. Breast Cancer Res Treat. 68 (2001) 187-198
36. Vares G., Ory K., Lectard B., Levalois C., Altmeyer-Morel S., Chevillard S., and Lebeau J. Progesterone prevents radiation-induced apoptosis in breast cancer cells. Oncogene 23 (2004) 4603-4613
37. Kato S., Pinto M., Carvajal A., Espinoza N., Monso C., Sadarangani A., Villalon M., Brosens J.J., White J.O., Richer J.K., Horwitz K.B., and Owen G.I. Progesterone increases tissue factor gene expression, procoagulant activity, and invasion in the breast cancer cell line ZR-75-1. J. Clin. Endo. Metab. 90 (2005) 1181-1188
38. Carnevale R.P., Proietti C.J., Salatino M., Urtreger A., Peluffo G., Edwards D.P., Boonyaratanakornkit V., Charreau E.H., Bal de Kier Joffe E., Schillaci R., and Elizalde P.V. Progestin effects on breast cancer cell proliferation, proteases activation, and in vivo development of metastatic phenotype all depend on progesterone receptor capacity to activate cytoplasmic signaling pathways. Mol. Endo. 21 (2007) 1335-1358
39. Fu X.D., Giretti M.S., Baldacci C., Garibaldi S., Flamini M., Sanchez A.M., Gadducci A., Genazzani A.R., and Simoncini T. Extra-nuclear signaling of progesterone receptor to breast cancer cell movement and invasion through the actin cytoskeleton. PLoS ONE 3 7 (2008) e2790 doi:10.1371/journal.pone.0002790
40. Fu X.D., Giretti M.S., Goglia L., Flamini M.I., Sanchez A.M., Baldacci C., Garibaldi S., Sitruk Ware R., Genazzani A.R., and Simoncini T. Comparative actions of progesterone, medroxyprogesterone acetate, drospirenone and nestorone on breast cancer cell migration and invasion. BMC Cancer 8 (2008) 166 doi:10.1186/1471-2407-8-166
41. Zhang H.J., Zhao W., Venkataraman S., Robbins M.E.C., Buettner G.R., Kreggel K.C., and Oberley L.W. Activation of matrix metalloproteinase-2 by over-expression of manganese superoxide dismutase in human breast cancer MCF-7 cells involves reactive oxygen species. J. Biol. Chem. 277 (2002) 20919-20926
42. Connor K.M., Hempel N., Nelson K.K., Dabiri G., Gamarra A., Belarmino J., Van De Water L., Mian B.M., and Melendez J.A. Manganese superoxide dismutase enhances the invasive and migratory activity of tumor cells. Cancer Res. 67 (2007) 10260-10267
43. Kattan Z., Minig V., Leroy P., Dauca M., and Becuwe P. Role of manganese superoxide dismutase on growth and invasive properties of human estrogen-independent breast cancer cells. Breast Cancer Res. Treat. 108 (2007) 203-215
44. Moore M.R. A rationale for inhibiting progesterone-related pathways to combat breast cancer. Curr. Cancer Drug Targets 4 (2004) 183-189
45. Kariagina A., Aupperlee M.D., and Haslam S.Z. Progesterone receptor isoform functions in normal breast development and breast cancer. Crit. Rev. Euk. Gene Express. 18 (2008) 11-33
46. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
47. Spitz D.R., and Oberley L.W. An assay for superoxide dismutase activity in mammalian tissue homogenates. Anal. Biochem. 179 (1989) 8-18
48. Horwitz K.B., Mockus M., Pike A.W., Fennessy P.V., and Sheridan R.L. Progesterone receptor replenishment in T47D human breast cancer cells. Roles of protein synthesis and hormone metabolism. J. Biol. Chem. 258 (1983) 7603-7610
49. Horwitz K.B., Zava D.T., Thilagar A.K., Jensen E.M., and McGuire W.L. Steroid receptor analyses of nine human breast cancer cell lines. Cancer Res. 38 (1978) 211-216
50. Migliaccio A., Piccolo D., Castoria G., Di Domenico M., Bilancio A., Lombardi M., Gong W., Beato M., and Auricchio F. Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. Eur. Mol. Biol. Org. J. 17 (1998) 2008-2018
51. Boonyaratanakornkit V., Mcgowan E., Sherman L., Mancini M.A., Cheskis B.J., and Edwards D.P. The role of extranuclear signaling actions of progesterone receptor in mediating progesterone regulation of gene expression and the cell cycle. Mol. Endo. 21 (2007) 359-375
52. Lange C.A. Integration of progesterone receptor action with rapid signaling events in breast cancer models. J. Steroid Biochem. Mol. Biol. 108 (2008) 203-212
53. Favata M.F., Horiuchi K.Y., Manos E.J., Daulerio A.J., Stradley D.A., Feeser W.S., Van Dyk D.E., Pitts W.J., Earl R.A., Hobbs F., Copeland R.A., Magolda R.L., Scherle P.A., and Trzaskos J.M. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273 (1998) 18623-18632
54. Das K.C., Guo X., and White C.W. Protein kinase Cδ-dependent induction of manganese superoxide dismutase gene expression by microtubule-active anticancer drugs. J. Biol. Chem. 273 (1998) 34639-34645
55. Daosukho C., Kiningham K.K., Kasarkis E.J., Ittarat W., and St. Clair D. Tamoxifen enhancement of TNF-α induced MnSOD expression: modulation of NF-κB dimerization. Oncogene 21 (2002) 3603-3610
56. Rose D.P., Tilton K., Lahti H., and Wynder E.L. Progesterone levels in breast duct fluid. Euro. J. Cancer Clin. Oncol. 22 (1986) 111-113
57. Pedram A., Razandi M., Wallace D.C., and Levin E.R. Functional estrogen receptors in the mitochondria of breast cancer cells. Mol. Biol. Cell 17 (2006) 2125-2137
58. Shiki Y., Meyrick B.O., Brigham K.L., and Burr I.M. Endotoxin increases superoxide dismutase in cultured bovine pulmonary epithelial cells. Am. J. Phys. 252 (1987) c436-c440
59. Asayama K., Janco R.L., and Burr I.M. Selective induction of manganous superoxide dismutase in human monocytes. Am. J. Phys. 249 (1985) 393-397
60. Kiningham K.K., Daosukho C., and St. Clair D.K. IκBα (inhibitory κBα) identified as labile repressor of MnSOD (manganese superoxide dismutase) expression. Biochem. J. 384 (2004) 543-549
61. Faivre E.J., and Lange C.A. Progesterone receptors upregulate Wnt-1 to induce epidermal growth factor receptor transactivation and c-src-dependent sustained activation of erk1/2 mitogen activated protein kinase in breast cancer cells. Mol. Cell. Biol. 27 (2007) 466-480
62. Fridovich I. Superoxide dismutases. An adaptation to a paramagnetic gas. J. Biol. Chem. 264 (1989) 7761-7764
63. Gregory E.M., and Fridovich I. Induction of superoxide dismutase by molecular oxygen. J. Bacteriol. 114 (1973) 543-548
64. Gregory E.M., and Fridovich I. Oxygen toxicity and the superoxide dismutase. J. Bacteriol. 114 (1973) 1193-1197
65. Gregory E.M., Goscin S.A., and Fridovich I. Superoxide dismutase and oxygen toxicity in a eukaryote. J. Bacteriol. 117 (1974) 456-460
66. Li Y., Huang T.T., Carlson E.J., Melov S., Ursell P.C., Olson J.L., Noble L.J., Yoshimura M.P., Berger C., Chan P.H., Wallace D.C., and Epstein C.J. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat. Genet. 11 (1995) 376-381
67. Copin J.C., Gasche Y., and Chan P.H. Over-expression of copper/zinc superoxide dismutase does not prevent neonatal lethality in mutant mice that lack manganese superoxide dismutase. Free Radic. Biol. Med. 28 (2000) 1571-1576
68. Graham J.D., Yager M.L., Hill H.D., Byth K., O'Neill G.M., and Clarke C.L. Altered progesterone receptor isoform expression remodels progestin responsiveness of breast cancer cells. Mol. Endo. 19 (2005) 2713-2735
69. Million Women Study Collaborators, Breast cancer and hormone- replacement therapy in the million women study. Lancet 362 (2003) 419-427.