Pharmacologic effects of 2-methoxyestradiol on angiotensin type 1 receptor down-regulation in rat liver epithelial and aortic smooth muscle cells

Gender Medicine

Volumn 9, Issue 2, 2012, Pages 76-93

  Koganti, Sivaramakrishna ^a   Snyder, Russell ^a   Thekkumkara, Thomas ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

2 Methoxyestradiol; Cardiovascular disease; Hypertension; MAPK

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 METHOXYESTRADIOL; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; CALCIUM; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; LOSARTAN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ANIMAL CELL; AORTA; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CARDIOVASCULAR DISEASE; CELL SURFACE; CHO CELL; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPLASM; DRUG EFFECT; EPITHELIUM CELL; GENETIC TRANSCRIPTION; LIVER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TRANSCRIPTION REGULATION;

ANGIOTENSIN II; ANIMALS; AORTA; CRICETINAE; DOWN-REGULATION; ESTRADIOL; FEMALE; GENE EXPRESSION REGULATION; HUMANS; LIVER; MALE; MICROSCOPY, FLUORESCENCE; MYOCYTES, SMOOTH MUSCLE; RATS; RECEPTOR, ANGIOTENSIN, TYPE 1; RECEPTOR, ANGIOTENSIN, TYPE 2; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84859529535     PISSN: 15508579     EISSN: 18787398     Source Type: Journal    
DOI: 10.1016/j.genm.2012.01.008     Document Type: Article

References (84)

1. Williams GH, Dluhy RG. Disorders of the Adrenal Cortex. 17th ed. New York, NY: McGraw-Hill Companies Inc; 2008.
2. Powers AC. Diabetes Mellitus. 17th ed. New York, NY: McGraw-Hill Companies Inc; 2008.
3. Wang CH, Li F, Takahashi N. The renin angiotensin system and the metabolic syndrome. Open Hypertens J. 2010;3:1-13.
4. Tamura K, Tanaka Y, Tsurumi Y, et al. The role of angiotensin AT1 receptor-associated protein in renin-angiotensin system regulation and function. Curr Hypertens Rep. 2007;9:121-127. (Pubitemid 46779376)
5. Henrion D, Kubis N, Lévy BI. Physiological and pathophysiological functions of the AT(2) subtype receptor of angiotensin II: from large arteries to the microcirculation. Hypertension. 2001;38:1150-117.
6. Ainscough JF, Drinkhill MJ, Sedo A, et al. Angiotensin II type-1 receptor activation in the adult heart causes blood pressure-independent hypertrophy and cardiac dysfunction. Cardiovasc Res. 2009;81:592- 600.
7. Siragy HM. Evidence for benefits of angiotensin receptor blockade beyond blood pressure control. Curr Hypertens Rep. 2008;10:261-267.
8. Marni F, Wang Y, Morishima M, et al. 17 betaestradiol modulates expression of low-voltage-activated Ca(V)3.2 T-type calcium channel via extracellularly regulated kinase pathway in cardiomyocytes. Endocrinology. 2009;150:879-888.
9. Mendelsohn ME, Karas RH. Molecular and cellular basis of cardiovascular gender differences. Science. 2005;308:1583-1587. (Pubitemid 40807497)
10. Deschamps AM, Murphy E. Activation of a novel estrogen receptor, GPER, is cardioprotective in male and female rats. Am J Physiol Heart Circ Physiol. 2009;297:H1806-H1813.
11. Olson SH, Bandera EV, Orlow I. Variants in estrogen biosynthesis genes, sex steroid hormone levels, and endometrial cancer: a HuGE review. Am J Epidemiol. 2007;165:235-245. (Pubitemid 46174747)
12. Zhu BT, Conney AH. Is 2-methoxy estradiol an endogenous estrogen metabolite that inhibits mammary carcinogenesis? Cancer Res. 1998;58: 2269-2277. (Pubitemid 28252677)
13. Berg D, Thaler F, Kuss E. Concentrations of 2-hydroxyoestrogens in human sera measured by a heterologous immunoassay with an 125I-labelled ligand. Acta Endocrinol (Copenh). 1982;100:154-160. (Pubitemid 12150500)
14. Prossnitz ER, Arterburn JB, Smith HO, et al. Estrogen signaling through the transmembrane G protein- coupled receptor GPR30. Annu Rev Physiol. 2008;70:165-190. (Pubitemid 351738176)
15. Bjornstrom L, Sjoberg M. Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol Endocrinol. 2005;19:833- 842.
16. Klinge CM. Estrogen receptor interaction with co-activators and co-repressors. Steroids. 2000;65:227-251. (Pubitemid 30177344)
17. Webb P, Nguyen P, Valentine C, et al. The estrogen receptor enhances AP-1 activity by two distinct mechanisms with different requirements for receptor transactivation functions. Mol Endocrinol. 1999;13:1672-1685. (Pubitemid 30645272)
18. Teyssier C, Belguise K, Galtier F, Chalbos D. Characterization of the physical interaction between estrogen receptor and JUN proteins. J Biol Chem. 2001;276:36361-36369.
19. Kato S, Endoh H, Masuhiro Y, et al. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science. 1995;270:1491-1494.
20. Tremblay A, Tremblay GB, Labrie F, Giguere V. Ligand-independent recruitment of SRC-1 to estrogen receptor through phosphorylation of activation function AF-1. Mol Cell. 1999;3:513-519. (Pubitemid 29292608)
21. Kousteni S, Han L, Chen JR, et al. Kinase-mediated regulation of common transcription factors accounts for the bone-protective effects of sex steroids. J Clin Invest. 2003;111:1651-1664. (Pubitemid 38057747)
22. Kawagoe J, Ohmichi M, Takahashi T, et al. Raloxifene inhibits estrogen-induced up-regulation of telomerase activity in a human breast cancer cell line. J Biol Chem. 2003;278:43363- 43372.
23. Cargnello M, Roux PP. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev. 2011;75:50-83.
24. Seger R, Krebs EG. The MAPK signaling cascade. FASEB J. 1995;9:726-735.
25. Neary JT. MAPK cascades in cell growth and death. News Physiol Sci. 1997;12:286-293.
26. Brown JW, Kesler CT, Neary JT, Fishman LM. Effects of androgens and estrogens and catechol and methoxy-estrogen derivatives on mitogen activated protein kinase (ERK 1,2) activity in SW-13 in human adrenal carcinoma cells. Horm Metab Res. 2001;33:127-130. (Pubitemid 32429983)
27. Neary JT, Kang Y, Bu Y, et al. Mitogenic signaling by ATP P2Y purinergic receptors in astrocytes: involvement of a calcium-independent protein kinase C, extracellular signal regulated protein kinase pathway distinct from the phosphatidylinositol-specific phospholipase C calcium pathway. J Neurosci. 1999; 19:4211-4220. (Pubitemid 29241075)
28. Stampfer MJ, Colditz GA, Willett WC, et al. Postmenopausal estrogen therapy and cardiovascular disease: ten-year follow-up from the Nurses' Health Study. N Engl J Med. 1991;325:756-762.
29. The Writing Group for the PEPI Trial. Effects of estrogen or estrogen/progestin regimens on heart disease risk factors in postmenopausal women: the Postmenopausal Estrogen/Progestin Interventions (PEPI) Trial. JAMA. 1995;273:199-208.
30. Kolovou G, Giannakopoulou V, Vasiliadis Y, Bilianou H. Effects of estrogens on atherogenesis. Curr Vasc Pharmacol. 2011;9:244-257.
31. Chauhan D, Catley L, Hideshima T, et al. 2-Methoxyestradiol overcomes drug resistance in multiple myeloma. Blood. 2002;100:2187-2194. (Pubitemid 35001255)
32. Dingli D, Timm M, Russell SJ, et al. Promising preclinical activity of 2-methoxyestradiol in multiple myeloma. Clin Cancer Res. 2002;8:3948-3954. (Pubitemid 35424790)
33. Stubelius A, Andréasson E, Karlsson A, et al. Role of 2-methoxyestradiol as inhibitor of arthritis and osteoporosis in a model of postmenopausal rheumatoid arthritis. Clin Immunol. 2011;140:37-46.
34. Garay L, Gonzalez Deniselle MC, Gierman L, et al. Steroid protection in the experimental autoimmune encephalomyelitis model of multiple sclerosis. Neuroimmunomodulation. 2008;15:76-83.
35. Offner H, Polanczyk M. A potential role for estrogen in experimental autoimmune encephalomyelitis and multiple sclerosis. Ann NY Acad Sci. 2006;1089:343-372. (Pubitemid 47092076)
36. Dubey RK, Jackson EK, Keller PJ, et al. Estradiol metabolites inhibit endothelin synthesis by an estrogen receptor-independent mechanism. Hypertension. 2001;37(2 Pt 2):640-644. (Pubitemid 32199042)
37. Dubey RK, Gillespie DG, Jackson EK, Keller PJ. 17Beta-estradiol, its metabolites, and progesterone inhibit cardiac fibroblast growth. Hypertension. 1998;31(1 Pt 2):522-528.
38. Dubey RK, Jackson EK, Gillespie DG, et al. Clinically used estrogens differentially inhibit human aortic smooth muscle cell growth and mitogen-activated protein kinase activity. Arterioscler Thromb Vasc Biol. 2000;20:964-972. (Pubitemid 30207569)
39. Dubey RK, Gillespie DG, Zacharia LC, et al. Methoxyestradiols mediate the antimitogenic effects of estradiol on vascular smooth muscle cells via estrogen receptor-independent mechanisms. Biochem Biophys Res Commun. 2000;278:27-33.
40. Barchiesi F, Lucchinetti E, Zaugg M, et al. Candidate genes and mechanisms for 2-methoxyestradiol-mediated vasoprotection. Hypertension. 2010;56:964-972.
41. Thekkumkara TJ, Cookson R, Linas SL. Angiotensin (AT1A) receptor-mediated increases in transcellular sodium transport in proximal tubule cells. Am J Physiol. 1998;274(5 Pt 2):F897-F905.
42. Swillens S. How to estimate the total receptor concentration when the specific radioactivity of the ligand is unknown. Trends Pharmacol Sci. 1992;13:430-434.
43. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-254.
44. Thekkumkara TJ, Linas SL. Evidence for involvement of 3=-untranslated region in determining angiotensin II receptor coupling specificity to G-protein. Biochem J. 2003;370(Pt 2):631-639. (Pubitemid 36315151)
45. Murphy TJ, Alexander RW, Griendling KK, et al. Isolation of a cDNA encoding the vascular type-1 angiotensin II receptor. Nature. 1991;351:233-236. (Pubitemid 21896571)
46. Grynkiewicz G, Poenie M, Tsien RY. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985;260: 3440-50. (Pubitemid 15114340)
47. Snyder R, Thekkumkara TJ. 13-Cis retinoic acid specific down-regulation of angiotensin type 1 receptor in rat liver epithelial and aortic smooth muscle cells. J Mol Endocrinol. 2011 Dec 16. [Epub ahead of print].
48. Tsao MS, Smith JD, Nelson KG, Grisham JW. A diploid epithelial cell line from normal adult rat liver with phenotypic properties of "oval" cells. Exp Cell Res. 1984;154:38-52. (Pubitemid 14006407)
49. Li X, Lee JW, Graves LM, Earp HS. Angiotensin II stimulates ERK via two pathways in epithelial cells: protein kinase C suppresses a G-protein coupled receptor-EGF receptor transactivation pathway. EMBO J. 1998;17:2574-2583. (Pubitemid 28221193)
50. Earp HS, Huckle WR, Dawson TL, et al. Angiotensin II activates at least two tyrosine kinases in rat liver epithelial cells: separation of the major calcium- regulated tyrosine kinase from p125FAK. J Biol Chem. 1995;270:28440-2847.
51. Huckle WR, Dy RC, Earp HS. Calcium-dependent increase in tyrosine kinase activity stimulated by angiotensin II. Proc Natl Acad Sci USA. 1992;89: 8837-8841.
52. Huckle WR, Prokop CA, Dy RC, et al. Angiotensin II stimulates protein-tyrosine phosphorylation in a calcium-dependent manner. Mol Cell Biol. 1990; 10:6290-6298. (Pubitemid 120004571)
53. Li X, Earp HS. Paxillin is tyrosine-phosphorylated by and preferentially associates with the calcium-dependent tyrosine kinase in rat liver epithelial cells. J Biol Chem. 1997;272:14341-1438.
54. Li X, Yu H, Graves LM, Earp HS. Protein kinase C and protein kinase A inhibit calcium-dependent but not stress-dependent c-Jun N-terminal kinase activation in rat liver epithelial cells. J Biol Chem. 1997;272:14996-5002. (Pubitemid 27251775)
55. McCune BK, Earp HS. The epidermal growth factor receptor tyrosine kinase in liver epithelial cells: the effect of ligand-dependent changes in cellular location. J Biol Chem. 1989;264:15501-1557.
56. Tsao MS, Earp HS, Grisham JW. The effects of epidermal growth factor and the state of confluence on enzymatic activities of cultured rat liver epithelial cells. J Cell Physiol. 1986;126:167-173. (Pubitemid 16185554)
57. Bokkala S, Joseph SK. Angiotensin II-induced down-regulation of inositol trisphosphate receptors in WB rat liver epithelial cells: evidence for involvement of the proteasome pathway. J Biol Chem. 1997;272:12454-12461. (Pubitemid 27203334)
58. Bokkala S, Reis HM, Rubin E, Joseph SK. Effect of angiotensin II and ethanol on the expression of connexin 43 in WB rat liver epithelial cells. Biochem J. 2001;357(Pt 3):769-777. (Pubitemid 32735157)
59. Park SH, Woo CH, Kim JH, et al. High glucose down-regulates angiotensin II binding via the PKC-MAPK-cPLA2 signal cascade in renal proximal tubule cells. Kidney Int. 2002;61:913-925.
60. Baumann M, Sollinger D, Roos M, et al. Prehypertensive preconditioning improves adult antihypertensive and cardioprotective treatment. J Pharmacol Exp Ther. 2010;332:1121-1126.
61. Toran-Allerand CD, Guan X, MacLusky NJ, et al. ER-X: a novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury. J Neurosci. 2002;22:8391-8401. (Pubitemid 35387579)
62. Ratziu V, Zelber-Sagi S. Pharmacologic therapy of non-alcoholic steatohepatitis. Clin Liver Dis. 2009; 13:667-688.
63. Kulke MH, Chan JA, Meyerhardt JA, et al. A prospective phase II study of 2-methoxyestradiol administered in combination with bevacizumab in patients with metastatic carcinoid tumors. Cancer Chemother Pharmacol. 2011;68:293-300.
64. Dahut WL, Lakhani NJ, Gulley JL, et al. Phase I clinical trial of oral 2-methoxyestradiol, an antiangiogenic and apoptotic agent, in patients with solid tumors. Cancer Biol Ther. 2006;5:22-27. (Pubitemid 43234973)
65. Dantas A, Kathryn Sandberg. Does 2-methoxyestradiol represent the new and improved hormone replacement therapy for atherosclerosis? Circ Res. 2006;99:234-237. (Pubitemid 44174929)
66. Brueggemeier RW, Bhat AS, Lovely CJ, Doughenour H, et al. 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. (Pubitemid 32879330)
67. Gui Y, Zheng XL, Zheng J, Walsh MP. Inhibition of rat aortic smooth muscle contraction by 2-methoxyestradiol. Am J Physiol Heart Circ Physiol. 2008;295:H1935-H1942.
68. Orshal JM, Khalil RA. Gender, sex hormones, and vascular tone. Am J Physiol Regul Integr Comp Physiol. 2004;286:R233-R249. (Pubitemid 38140366)
69. Crews JK, Murphy JG, Khalil RA. Gender differences in Ca(2+) entry mechanisms of vasoconstriction in Wistar-Kyoto and spontaneously hypertensive rats. Hypertension. 1999;34(4 Pt 2):931-936. (Pubitemid 29501326)
70. Kanashiro CA, Khalil RA. Gender-related distinctions in protein kinase C activity in rat vascular smooth muscle. Am J Physiol Cell Physiol. 2001; 280:C34-C45.
71. Granger JP, Alexander BT, MT Llinas MT, et al. Pathophysiology of hypertension during preeclampsia linking placental ischemia with endothelial dysfunction. Hypertension. 2001;38:718-722.
72. Roberts JM, KY Lain. Preterm birth and pre-eclampsia: bad news and good news. Lancet. 1998; 352:SIV22. (Pubitemid 128646460)
73. Gerretsen G, Hiusjes HJ, Elema JD. Morphological changes of the spiral arteries in the placental bed in relation to pre-eclampsia and fetal growth retardation. Br J Obstet Gynaecol. 1981;88:876-881. (Pubitemid 11018178)
74. Duffy AA, Martin MM, Elton TS. Transcriptional regulation of the AT1 receptor gene in immortalized human trophoblast cells. Biochim Biophys Acta. 2004;1680:158-170.
75. Schmid M, Sollwedel A, Thuere C, et al. Murine pre-eclampsia induced by unspecific activation of the immune system correlates with alterations in the eNOS and AT1 receptor expression in the kidneys and placenta. Placenta. 2007;28:688-700. (Pubitemid 46852296)
76. Itoh T, Kajikuri J, Tada T, et al. Angiotensin II-induced modulation of endothelium-dependent relaxation in rabbit mesenteric resistance arteries. J Physiol. 2003;548:893-906. (Pubitemid 36603303)
77. Kanasaki K, Palmsten K, Sugimoto H, et al. Defi- ciency in catechol-O-methyltransferase and 2-methoxyoestradiol is associated with pre-eclampsia. Nature. 2008;453:1117-1121. (Pubitemid 351871733)
78. Dubey RK, Tofovic SP, and Jackson EK. Cardiovascular pharmacology of estradiol metabolites. JPET. 2004;308:403-409. (Pubitemid 38134197)
79. Prossnitz ER, Arterburn JB, Sklar LA. GPR30: a G protein- coupled receptor for estrogen. MolCell Endocrinol. 2007;265-266:138-142. (Pubitemid 46273957)
80. Filardo EJ, Quinn JA, Bland KI, Frackelton AR Jr. Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol Endocrinol. 2000;14:1649-1660.
81. Revankar CM, Cimino DF, Sklar LA, et al. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science. 2005;307:1625-1630. (Pubitemid 40354745)
82. Filardo EJ, Quinn JA, Frackelton AR Jr, Bland KI. Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol Endocrinol. 2002;16:70-84. (Pubitemid 34044499)
83. Thomas P, Pang Y, Filardo EJ, Dong J. Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology. 2005;146:624-632. (Pubitemid 40129818)
84. Dubey RK, Gillespie DG, Mi Z, et al. Estradiol inhibits smooth muscle cell growth in part by activating the cAMP-adenosine pathway. Hypertension. 2000;35(1 Pt 2):262-266. (Pubitemid 30054183)