Anti-atherogenic effects of 17β-estradiol

Hormone and Metabolic Research

Volumn 45, Issue 10, 2013, Pages 701-708

  Resanovic, I ^a   Rizzo, M ^b,c   Zafirovic, S ^a   Bjelogrlic, P ^d   Perovic, M ^e   Savic, K ^a   Patti, A M ^b   Isenovic, R E ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b UNIVERSITY OF PALERMO   (Italy)

^c Euro Mediterranean Institute of Science and Technology   (Italy)

^d UNIVERSITY OF ST ANDREWS   (United Kingdom)

^e UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

17 estradiol; atherogenic factors; atherosclerosis; estrogen

Indexed keywords

APOLIPOPROTEIN B; ESTRADIOL; ESTRIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTRONE; INTERMEDIATE DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; RALOXIFENE; TAMOXIFEN; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN CHOLESTEROL;

ATHEROGENESIS; ATHEROSCLEROSIS; BONE DENSITY; CARDIOVASCULAR RISK; CEREBROVASCULAR ACCIDENT; CHOLESTEROL BLOOD LEVEL; ENDOTHELIAL DYSFUNCTION; ESTROGEN DEFICIENCY; GLUCOSE METABOLISM; HEART INFARCTION; HEART PROTECTION; HORMONE SUBSTITUTION; HUMAN; LIPID PEROXIDATION; MEDLINE; MORTALITY; NONHUMAN; OBESITY; OSTEOPOROSIS; POSTMENOPAUSE; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE;

ANIMALIA; NICOTIANA TABACUM;

ANIMALS; ATHEROSCLEROSIS; DIET, ATHEROGENIC; ESTRADIOL; ESTROGEN REPLACEMENT THERAPY; FEMALE; HUMANS; MALE; OVARIECTOMY; RISK FACTORS; SELECTIVE ESTROGEN RECEPTOR MODULATORS;

EID: 84884418355     PISSN: 00185043     EISSN: 14394286     Source Type: Journal    
DOI: 10.1055/s-0033-1343478     Document Type: Review

References (102)

1. Stojanovic N. D., Kwong P., Byrne D. J., Arnold A., Jagroop I. A., Nair D., Press M., Hurel S., Mikhailidis D. P., Prelevic G. M. The effects of transdermal estradiol alone or with cyclical dydrogesterone on markers of cardiovascular disease risk in postmenopausal women with type 2 diabetes: a pilot study. Angiology: 2003; 54 391 399 (Pubitemid 36935352)
2. Prelevic G. M., Kwong P., Byrne D. J., Jagroop I. A., Ginsburg J., Mikhailidis D. P. A cross-sectional study of the effects of hormon replacement therapy on the cardiovascular disease risk profile in healthy postmenopausal women. Fertil Steril: 2002; 77 945 951 (Pubitemid 34497161)
3. Dahlman-Wright K., Cavailles V., Fuqua S. A., Jordan V. C., Katzenellenbogen J. A., Korach K. S., Maggi A., Muramatsu M., Parker M. G., Gustafsson J. A. International Union of Pharmacology. LXIV. Estrogen receptors. Pharmacol Rev: 2006; 58 773 781 (Pubitemid 44833745)
4. Wassmann S., Baumer A. T., Strehlow K., van Eickels M., Grohe C., Ahlbory K., Rosen R., Bohm M., Nickenig G. Endothelial dysfunction and oxidative stress during estrogen deficiency in spontaneously hypertensive rats. Circulation: 2001; 103 435 441 (Pubitemid 32105985)
5. Ruiz-Sanz J. I., Navarro R., Martinez R., Martin C., Lacort M., Matorras R., Ruiz-Larrea M. B. 17beta-estradiol affects in vivo the low density lipoprotein composition, particle size, and oxidizability. Free Radic Biol Med: 2001; 31 391 397 (Pubitemid 32675345)
6. Cossette E., Cloutier I., Tardif K., DonPierre G., Tanguay J. F. Estradiol inhibits vascular endothelial cells pro-inflammatory activation induced by C-reactive protein. Mol Cell Biochem: 2013; 373 137 147
7. Isenovic E. R., Divald A., Milivojevic N., Grgurevic T., Fisher S. E., Sowers J. R. Interactive effects of insulin-like growth factor-1 and beta-estradiol on endothelial nitric oxide synthase activity in rat aortic endothelial cells. Metabolism: 2003; 52 482 487 (Pubitemid 36773272)
8. Chambliss K. L., Shaul P. W. Estrogen modulation of endothelial nitric oxide synthase. Endocr Rev: 2002; 23 665 686 (Pubitemid 35191628)
9. Meyer M. R., Barton M. ERalpha, ERbeta, and gpER: novel aspects of oestrogen receptor signalling in atherosclerosis. Cardiovasc Res: 2009; 83 605 610
10. Rosano G. M., Fini M. Postmenopausal women and cardiovascular risk: impact of hormone replacement therapy. Cardiol Rev: 2002; 10 51 60 (Pubitemid 34130770)
11. Wren B. G. The benefits of oestrogen following menopause: why hormone replacement therapy should be offered to postmenopausal women. Med J Aust: 2009; 190 321 325
12. Horstman A. M., Dillon E. L., Urban R. J., Sheffield-Moore M. The role of androgens and estrogens on healthy aging and longevity. J Gerontol A Biol Sci Med Sci: 2012; 67 1140 1152
13. Mendelsohn M. E., Karas R. H. Molecular and cellular basis of cardiovascular gender differences. Science: 2005; 308 1583 1587 (Pubitemid 40807497)
14. Akishita M., Yu J. Hormonal effects on blood vessels. Hypertens Res: 2012; 35 363 369
15. Heldring N., Pike A., Andersson S., Matthews J., Cheng G., Hartman J., Tujague M., Strom A., Treuter E., Warner M., Gustafsson J. A. Estrogen receptors: how do they signal and what are their targets. Physiol Rev: 2007; 87 905 931 (Pubitemid 47084672)
16. Lucas T. F., Pimenta M. T., Pisolato R., Lazari M. F., Porto C. S. 17beta-estradiol signaling and regulation of Sertoli cell function. Spermatogenesis: 2011; 1 318 324
17. Boon W. C., Chow J. D., Simpson E. R. The multiple roles of estrogens and the enzyme aromatase. Prog Brain Res: 2010; 181 209 232
18. Mandusic V., Radak D., Markicevic M., Perovic M., Obradovic M., Mikhailidis D. P., Isenovic E. R. Role of estrogen and estrogen receptors in cancer pathology. Endocrine studies: 2011; 1 e5 9 23
19. Chakrabarti S., Davidge S. T. G-Protein Coupled Receptor 30 (GPR30): A Novel Regulator of Endothelial Inflammation. PLoS One: 2012; 7 e52357
20. Ihionkhan C. E., Chambliss K. L., Gibson L. L., Hahner L. D., Mendelsohn M. E., Shaul P. W. Estrogen causes dynamic alterations in endothelial estrogen receptor expression. Circ Res: 2002; 91 814 820 (Pubitemid 35285079)
21. Jensen E. V., Jordan V. C. The estrogen receptor: a model for molecular medicine. Clin Cancer Res: 2003; 9 1980 1989 (Pubitemid 36687616)
22. Bosland M. C., Mahmoud A. M. Hormones and prostate carcinogenesis: Androgens and estrogens. J Carcinog: 2011; 10 33
23. Nathan L., Shi W., Dinh H., Mukherjee T. K., Wang X., Lusis A. J., Chaudhuri G. Testosterone inhibits early atherogenesis by conversion to estradiol: critical role of aromatase. Proc Natl Acad Sci USA: 2001; 98 3589 3593 (Pubitemid 32220889)
24. Akishita M., Hashimoto M., Ohike Y., Ogawa S., Iijima K., Eto M., Ouchi Y. Low testosterone level as a predictor of cardiovascular events in Japanese men with coronary risk factors. Atherosclerosis: 2010; 210 232 236
25. Hayward C. S., Kelly R. P., Collins P. The roles of gender, the menopause and hormone replacement on cardiovascular function. Cardiovasc Res: 2000; 46 28 49 (Pubitemid 30155943)
26. Faulds M. H., Zhao C., Dahlman-Wright K., Gustafsson J. A. The diversity of sex steroid action: regulation of metabolism by estrogen signaling. J Endocrinol: 2012; 212 3 12
27. Murphy E. Estrogen signaling and cardiovascular disease. Circ Res: 2011; 109 687 696
28. Sudar E., Velebit J., Gluvic Z., Zakula Z., Lazic E., Vuksanovic-Topic L., Putnikovic B., Neskovic A., Isenovic E. R. Hypothetical mechanism of sodium pump regulation by estradiol under primary hypertension. J Theor Biol: 2008; 251 584 592
29. Isenovic E., Walsh M. F., Muniyappa R., Bard M., Diglio C. A., Sowers J. R. Phosphatidylinositol 3-kinase may mediate isoproterenol-induced vascular relaxation in part through nitric oxid production. Metabolism: 2002; 51 380 386 (Pubitemid 34232643)
30. Maggiolini M., Picard D. The unfolding stories of GPR30, a new membrane-bound estrogen receptor. J Endocrinol: 2010; 204 105 114
31. Carreau S., Bouraima-Lelong H., Delalande C. Estrogen, a female hormone involved in spermatogenesis. Adv Med Sci: 2012; 57 31 36
32. Vina J., Sastre J., Pallardo F. V., Gambini J., Borras C. Role of mitochondrial oxidative stress to explain the different longevity between genders: protective effect of estrogens. Free Radic Res: 2006; 40 1359 1365 (Pubitemid 44698285)
33. Li Y., Wang J. P., Santen R. J., Kim T. H., Park H., Fan P., Yue W. Estrogen stimulation of cell migration involves multiple signaling pathway interactions. Endocrinology: 2010; 151 5146 5156
34. Simoncini T. Mechanisms of action of estrogen receptors in vascular cells: relevance for menopause and aging. Climacteric: 2009; 12 01 6 11
35. Fu X. D., Simoncini T. Extra-nuclear signaling of estrogen receptors. IUBMB Life: 2008; 60 502 510
36. Mendelsohn M. E. Protective effects of estrogen on the cardiovascular system. Am J Cardiol: 2002; 89 12E 17E discussion 17E-18E
37. Blum A., Koh K., Cannon R. O. 3rd. CME Paper: Hormone Replacement Therapy for Prevention or Treatment of Atherosclerosis in Postmenopausal Women: Promises, Controversies, and Clinical Trials. Am J Geriatr Cardiol: 2000; 9 81 88 (Pubitemid 30659159)
38. Koricanac G., Tepavcevic S., Zakula Z., Milosavljevic T., Stojiljkovic M., Isenovic E. R. Interference between insulin and estradiol signaling pathways in the regulation of cardiac eNOS and Na(+)/K (+) -ATPase. Eur J Pharmacol: 2011; 655 23 30
39. Haas E., Bhattacharya I., Brailoiu E., Damjanovic M., Brailoiu G. C., Gao X., Mueller-Guerre L., Marjon N. A., Gut A., Minotti R., Meyer M. R., Amann K., Ammann E., Perez-Dominguez A., Genoni M., Clegg D. J., Dun N. J., Resta T. C., Prossnitz E. R., Barton M. Regulatory role of G protein-coupled estrogen receptor for vascular function and obesity. Circ Res: 2009; 104 288 291
40. Seok Y. M., Jang E. J., Reiser O., Hager M., Kim I. K. 17beta-Estradiol induces vasorelaxation in a G-protein-coupled receptor 30-independent manner. Naunyn Schmiedebergs Arch Pharmacol: 2012; 385 945 948
41. Weil B. R., Manukyan M. C., Herrmann J. L., Wang Y., Abarbanell A. M., Poynter J. A., Meldrum D. R. Signaling via GPR30 protects the myocardium from ischemia/reperfusion injury. Surgery: 2010; 148 436 443
42. Lindsey S. H., Carver K. A., Prossnitz E. R., Chappell M. C. Vasodilation in response to the GPR30 agonist G-1 is not different from estradiol in the mRen2.Lewis female rat. J Cardiovasc Pharmacol: 2011; 57 598 603
43. Broughton B. R., Miller A. A., Sobey C. G. Endothelium-dependent relaxation by G protein-coupled receptor 30 agonists in rat carotid arteries. Am J Physiol Heart Circ Physiol: 2010; 298 H1055 H1061
44. Rowlands D. J., Chapple S., Siow R. C., Mann G. E. Equol-stimulated mitochondrial reactive oxygen species activate endothelial nitric oxide synthase and redox signaling in endothelial cells: roles for F-actin and GPR30. Hypertension: 2011; 57 833 840
45. Deschamps A. M., Murphy E., Sun J. Estrogen receptor activation and cardioprotection in ischemia reperfusion injury. Trends Cardiovasc Med: 2010; 20 73 78
46. Ullrich N. D., Krust A., Collins P., MacLeod K. T. Genomic deletion of estrogen receptors ERalpha and ERbeta does not alter estrogen-mediated inhibition of Ca2+ influx and contraction in murine cardiomyocytes. Am J Physiol Heart Circ Physiol: 2008; 294 H2421 H2427
47. Thomas P., Pang Y., Filardo E. J., 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)
48. Meyer M. R., Baretella O., Prossnitz E. R., Barton M. Dilation of epicardial coronary arteries by the G protein-coupled estrogen receptor agonists G-1 and ICI 182,780. Pharmacology: 2010; 86 58 64
49. Mercier I., Mader S., Calderone A. Tamoxifen and ICI 182,780 negatively influenced cardiac cell growth via an estrogen receptor-independent mechanism. Cardiovasc Res: 2003; 59 883 892 (Pubitemid 38366244)
50. Meyer M. R., Haas E., Prossnitz E. R., Barton M. Non-genomic regulation of vascular cell function and growth by estrogen. Mol Cell Endocrinol: 2009; 308 9 16
51. Dubey R. K., Jackson E. K. Estrogen-induced cardiorenal protection: potential cellular, biochemical, and molecular mechanisms. Am J Physiol Renal Physiol: 2001; 280 F365 F388
52. Du X. J. Clues to understanding the role of estrogen receptors in mediating cardiovascular protection. Cardiovasc Res: 2002; 56 4 7
53. Muchmore D. B. Raloxifene: A selective estrogen receptor modulator (SERM) with multiple target system effects. Oncologist: 2000; 5 388 392
54. Draper M. W. The role of selective estrogen receptor modulators (SERMs) in postmenopausal health. Ann N Y Acad Sci: 2003; 997 373 377 (Pubitemid 38491092)
55. Walsh B. W., Kuller L. H., Wild R. A., Paul S., Farmer M., Lawrence J. B., Shah A. S., Anderson P. W. Effects of raloxifene on serum lipids and coagulation factors in healthy postmenopausal women. JAMA: 1998; 279 1445 1451
56. Love R. R., Newcomb P. A., Wiebe D. A., Surawicz T. S., Jordan V. C., Carbone P. P., DeMets D. L. Effects of tamoxifen therapy on lipid and lipoprotein levels in postmenopausal patients with node-negative breast cancer. J Natl Cancer Inst: 1990; 82 1327 1332 (Pubitemid 20238487)
57. Vogelvang T. E., van der Mooren M. J., Mijatovic V. Hormone replacement therapy, selective estrogen receptor modulators, and tissue-specific compounds: cardiovascular effects and clinical implications. Treat Endocrinol: 2004; 3 105 115 (Pubitemid 38337561)
58. Gallino A., Stuber M., Crea F., Falk E., Corti R., Lekakis J., Schwitter J., Camici P., Gaemperli O., Di Valentino M., Prior J., Garcia-Garcia H. M., Vlachopoulos C., Cosentino F., Windecker S., Pedrazzini G., Conti R., Mach F., De Caterina R., Libby P. "In vivoo" imaging of atherosclerosis. Atherosclerosis: 2012; 224 25 36
59. Glass C. K., Witztum J. L. Atherosclerosis. The road ahead. Cell: 2001; 104 503 516
60. Fuster J. J., Fernandez P., Gonzalez-Navarro H., Silvestre C., Nabah Y. N., Andres V. Control of cell proliferation in atherosclerosis: insights from animal models and human studies. Cardiovascular research: 2010; 86 254 264
61. Koh K. K. Effects of estrogen on the vascular wall: vasomotor function and inflammation. Cardiovasc Res: 2002; 55 714 726
62. Soskic S. S., Sudar E. M., Obradovic M. M., Nikolic D. M., Zarić B. L., Stojanovic S. D., Stokic E. J., Mikhailidis D. P., Isenovic E. R. The peroxisome proliferator-activated receptors and atherosclerosis. Angiology: 2011; 62 523 534
63. Popovic M., Smiljanic K., Dobutovic B., Syrovets T., Simmet T., Isenovic E. R. Thrombin and vascular inflammation. Mol Cell Biochem: 2012; 359 301 313
64. Kzhyshkowska J., Neyen C., Gordon S. Role of macrophage scavenger receptors in atherosclerosis. Immunobiology: 2012; 217 492 502
65. Liu P. Y., Death A. K., Handelsman D. J. Androgens and cardiovascular disease. Endocrine Rev: 2003; 24 313 340 (Pubitemid 36724373)
66. Hayashi T., Sumi D., Juliet P. A., Matsui-Hirai H., Asai-Tanaka Y., Kano H., Fukatsu A., Tsunekawa T., Miyazaki A., Iguchi A., Ignarro L. J. Gene transfer of endothelial NO synthase, but not eNOS plus inducible NOS, regressed atherosclerosis in rabbits. Cardiovasc Res: 2004; 61 339 351 (Pubitemid 38091774)
67. Reinehr T., Andler W. Changes in the atherogenic risk factor profile according to degree of weight loss. Arch Dis Child: 2004; 89 419 422
68. Kuvin J. T., Ramet M. E., Patel A. R., Pandian N. G., Mendelsohn M. E., Karas R. H. A novel mechanism for the beneficial vascular effects of high-density lipoprotein cholesterol: enhanced vasorelaxation and increased endothelial nitric oxide synthase expression. Am Heart J: 2002; 144 165 172 (Pubitemid 34734771)
69. Banach M., Rizzo M., Obradovic M., Montalto G., Rysz J., Mikhailidis D. P., Isenovic E. R. PCSK9 Inhibition - A Novel Mechanism to Treat Lipid Disorders? Curr Pharm Des: 2012; [Epub ahead of print]
70. Tabas I., Williams K. J., Boren J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation: 2007; 116 1832 1844 (Pubitemid 350287108)
71. Brunelli R., Greco G., Barteri M., Krasnowska E. K., Mei G., Natella F., Pala A., Rotella S., Ursini F., Zichella L., Parasassi T. One site on the apoB-100 specifically binds 17-beta-estradiol and regulates the overall structure of LDL. FASEB J: 2003; 17 2127 2129
72. Liang Y. Q., Akishita M., Kim S., Ako J., Hashimoto M., Iijima K., Ohike Y., Watanabe T., Sudoh N., Toba K., Yoshizumi M., Ouchi Y. Estrogen receptor beta is involved in the anorectic action of estrogen. Int J Obes Relat Metab Disord: 2002; 26 1103 1109
73. Lijnen H. R. Murine models of obesity and hormonal therapy. Thromb Res: 2011; 127 03 S17 S20
74. Parhofer K. G. Beyond LDL-cholesterol: HDL-cholesterol as a target for atherosclerosis prevention. Exp Clin Endocrinol Diabetes: 2005; 113 414 417 (Pubitemid 41360745)
75. Walsh B. A., Mullick A. E., Banka C. E., Rutledge J. C. 17beta-estradiol acts separately on the LDL particle and artery wall to reduce LDL accumulation. J Lipid Res: 2000; 41 134 141 (Pubitemid 30051851)
76. Simprini L. A., Villines T. C., Rich M., Taylor A. J. The relationship between subclinical atherosclerosis, non-high-density lipoprotein cholesterol, exercise, and diet among male participants of the PACC Project. Journal of clinical lipidology: 2012; 6 174 179
77. Robinson J. G., Wang S., Smith B. J., Jacobson T. A. Meta-analysis of the relationship between non-high-density lipoprotein cholesterol reduction and coronary heart disease risk. J Am Coll Cardiol: 2009; 53 316 322
78. Sniderman A. D., Williams K., Contois J. H., Monroe H. M., McQueen M. J., de Graaf J., Furberg C. D. A meta-analysis of low-density lipoprotein cholesterol, non-high-density lipoprotein cholesterol, and apolipoprotein B as markers of cardiovascular risk. Circ Cardiovasc Qual Outcomes: 2011; 4 337 345
79. Pande R. L. Approach to lipid therapy in the patient with atherosclerotic vascular disease. Curr Treat Opt Cardiovasc Med: 2012; 14 177 183
80. Yusuf S., Reddy S., Ounpuu S., Anand S. Global burden of cardiovascular diseases: part I: general considerations, the epidemiologic transition, risk factors, and impact of urbanization. Circulation: 2001; 104 2746 2753 (Pubitemid 33108145)
81. Dubey R. K., Imthurn B., Barton M., Jackson E. K. Vascular consequences of menopause and hormone therapy: importance of timing of treatment and type of estrogen. Cardiovasc Res: 2005; 66 295 306 (Pubitemid 40471044)
82. McGill H. C. Jr, McMahan C. A., Herderick E. E., Zieske A. W., Malcom G. T., Tracy R. E., Strong J. P. Obesity accelerates the progression of coronary atherosclerosis in young men. Circulation: 2002; 105 2712 2718 (Pubitemid 34615140)
83. Murase T., Hattori T., Ohtake M., Nakashima C., Takatsu M., Murohara T., Nagata K. Effects of estrogen on cardiovascular injury in ovariectomized female DahlS.Z-Lepr(fa)/Lepr(fa) rats as a new animal model of metabolic syndrome. Hypertension: 2012; 59 694 704
84. Hodgin J. B., Krege J. H., Reddick R. L., Korach K. S., Smithies O., Maeda N. Estrogen receptor alpha is a major mediator of 17beta-estradiol's atheroprotective effects on lesion size in Apoe-/- mice. J Clin Invest: 2001; 107 333 340 (Pubitemid 32157965)
85. Christian R. C., Liu P. Y., Harrington S., Ruan M., Miller V. M., Fitzpatrick L. A. Intimal estrogen receptor (ER)beta, but not ERalpha expression, is correlated with coronary calcification and atherosclerosis in pre- and postmenopausal women. J Clin Endocrinol Metab: 2006; 91 2713 2720 (Pubitemid 44024642)
86. Rossouw J. E., Anderson G. L., Prentice R. L., LaCroix A. Z., Kooperberg C., Stefanick M. L., Jackson R. D., Beresford S. A., Howard B. V., Johnson K. C., Kotchen J. M., Ockene J. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA: 2002; 288 321 333 (Pubitemid 34761611)
87. Oparil S., Levine R. L., Chen S. J., Durand J., Chen Y. F. Sexually dimorphic response of the balloon-injured rat carotid artery to hormone treatment. Circulation: 1997; 95 1301 1307 (Pubitemid 27097844)
88. Cho J. J., Cadet P., Salamon E., Mantione K., Stefano G. B. The nongenomic protective effects of estrogen on the male cardiovascular system: clinical and therapeutic implications in aging men. Med Sci Monit: 2003; 9 RA63 RA68 (Pubitemid 36389409)
89. Clarkson T. B. Estrogen effects on arteries vary with stage of reproductive life and extent of subclinical atherosclerosis progression. Menopause: 2007; 14 373 384
90. McMahan C. A., Gidding S. S., Fayad Z. A., Zieske A. W., Malcom G. T., Tracy R. E., Strong J. P., McGill H. C. Jr. Risk scores predict atherosclerotic lesions in young people. Arch Intern Med: 2005; 165 883 890 (Pubitemid 40563234)
91. Meyer M. R., Haas E., Barton M. Gender differences of cardiovascular disease: new perspectives for estrogen receptor signaling. Hypertension: 2006; 47 1019 1026 (Pubitemid 44289154)
92. Bairey Merz C. N., Johnson B. D., Sharaf B. L., Bittner V., Berga S. L., Braunstein G. D., Hodgson T. K., Matthews K. A., Pepine C. J., Reis S. E., Reichek N., Rogers W. J., Pohost G. M., Kelsey S. F., Sopko G. Hypoestrogenemia of hypothalamic origin and coronary artery disease in premenopausal women: a report from the NHLBI-sponsored WISE study. J Am Coll Cardiol: 2003; 41 413 419 (Pubitemid 36164495)
93. Kaplan J. R., Manuck S. B., Anthony M. S., Clarkson T. B. Premenopausal social status and hormone exposure predict postmenopausal atherosclerosis in female monkeys. Obstet Gynecol: 2002; 99 381 388 (Pubitemid 34188397)
94. Abbey M., Owen A., Suzakawa M., Roach P., Nestel P. J. Effects of menopause and hormone replacement therapy on plasma lipids, lipoproteins and LDL-receptor activity. Maturitas: 1999; 33 259 269
95. Rizzo M., Berneis K., Blanche P. J., Superko R. H., Krauss R. M. Effects of combined estrogen+progestin hormone therapy on hepatic lipase and lipoprotein lipase levels. Book of Abstract, 75th EAS Congress: 2005; W16-P-075, p.120
96. Mikhailidis D. P., Elisaf M., Rizzo M., Berneis K., Griffin B., Zambon A., Athyros V., de Graaf J., Marz W., Parhofer K. G., Rini G. B., Spinas G. A., Tomkin G. H., Tselepis A. D., Wierzbicki A. S., Winkler K., Florentin M., Liberopoulos E. "European panel on low density lipoprotein (LDL) subclasseso": a statement on the pathophysiology, atherogenicity and clinical significance of LDL subclasses: executive summary. Curr Vasc Pharmacol: 2011; 9 531 532
97. Villablanca A. C., Tenwolde A., Lee M., Huck M., Mumenthaler S., Rutledge J. C. 17beta-estradiol prevents early-stage atherosclerosis in estrogen receptor-alpha deficient female mice. J Cardiovasc Transl Res: 2009; 2 289 299
98. Williams J. K., Suparto I. Hormone replacement therapy and cardiovascular disease: lessons from a monkey model of postmenopausal women. ILAR J: 2004; 45 139 146
99. Schwenke D. C., Wagner J. D., Adams M. R. In vitro lipid peroxidation of LDL from postmenopausal cynomolgus macaques treated with female hormones. J Lipid Res: 1999; 40 235 244 (Pubitemid 29069797)
100. Mendelsohn M. E., Karas R. H. The protective effects of estrogen on the cardiovascular system. N Engl J Med: 1999; 340 1801 1811 (Pubitemid 29266405)
101. Farhat M. Y., Lavigne M. C., Ramwell P. W. The vascular protective effects of estrogen. FASEB J: 1996; 10 615 624 (Pubitemid 26141172)
102. Khalil R. A. Sex hormones as potential modulators of vascular function in hypertension. Hypertension: 2005; 46 249 254 (Pubitemid 41099147)