17β-estradiol protects against the progression of hypertension during adulthood in a mouse model of systemic lupus erythematosus

Hypertension

Volumn 63, Issue 3, 2014, Pages 616-623

  Gilbert, Emily L ^a   Mathis, Keisa W ^a   Ryan, Michael J ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

estrogens; lupus erythematosus, systemic; pressure

Indexed keywords

ESTROGENS; LUPUS ERYTHEMATOSUS, SYSTEMIC; PRESSURE;

ANIMALS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ESTRADIOL; ESTROGENS; FEMALE; HYPERTENSION; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; TREATMENT OUTCOME;

EID: 84894429626     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.113.02385     Document Type: Article

References (58)

1. López P, Mozo L, Gutiérrez C, Suárez A. Epidemiology of systemic lupus erythematosus in a northern Spanish population: Gender and age influence on immunological features. Lupus. 2003;12:860-865.
2. Tucker LB, Menon S, Schaller JG, Isenberg DA. Adult-And childhood-onset systemic lupus erythematosus: A comparison of onset, clinical features, serology, and outcome. Br J Rheumatol. 1995;34:866-872.
3. Bjoddddrnådal L, Yin L, Granath F, Klareskog L, Ekbom A. Cardiovascular disease a hazard despite improved prognosis in patients with systemic lupus erythematosus: Results from a Swedish population based study 1964-95. J Rheumatol. 2004;31:713-719.
4. Aranow C, Ginzler EM. Epidemiology of cardiovascular disease in systemic lupus erythematosus. Lupus. 2000;9:166-169.
5. Health, United States. 2012 With Chartbook on Trends in Health of Americans. Hyattsville, MD: National Center for Health Statistics; 2012.
6. Selzer F, Sutton-Tyrrell K, Fitzgerald S, Tracy R, Kuller L, Manzi S. Vascular stiffness in women with systemic lupus erythematosus. Hypertension. 2001;37:1075-1082.
7. Petri M. Detection of coronary artery disease and the role of traditional risk factors in the Hopkins Lupus Cohort. Lupus. 2000;9:170-175.
8. Sabio JM, Vargas-Hitos JA, Navarrete-Navarrete N, Mediavilla JD, Jiménez-Jáimez J, Diáz-Chamorro A, Jiménez-Alonso J; Grupo Lupus Virgen de las Nieves. Prevalence of and factors associated with hypertension in young and old women with systemic lupus erythematosus. J Rheumatol. 2011;38:1026-1032.
9. Kanda N, Tsuchida T, Tamaki K. Estrogen enhancement of anti-double-stranded DNA antibody and immunoglobulin G production in peripheral blood mononuclear cells from patients with systemic lupus erythematosus. Arthritis Rheum. 1999;42:328-337.
10. Verthelyi D, Ahmed SA. 17β-Estradiol, but not 5α- dihydrotestosterone, augments antibodies to double-stranded deoxyribonucleic acid in nonautoimmune C57BL/6J mice. Endocrinology. 1994;135:2615-2622.
11. Roubinian JR, Talal N, Greenspan JS, Goodman JR, Siiteri PK. Effect of castration and sex hormone treatment on survival, anti-nucleic acid antibodies, and glomerulonephritis in NZB/NZW F1 mice. J Exp Med. 1978;147:1568-1583.
12. Sobel ES, Gianini J, Butfiloski EJ, Croker BP, Schiffenbauer J, Roberts SM. Acceleration of autoimmunity by organochlorine pesticides in (NZB x NZW)F1 mice. Environ Health Perspect. 2005;113:323-328.
13. Sammaritano LR. Menopause in patients with autoimmune diseases. Autoimmun Rev. 2012;11:A430-A436.
14. Li J, McMurray RW. Effects of cyclic versus sustained estrogen administration on peripheral immune functions in ovariectomized mice. Am J Reprod Immunol. 2010;63:274-281.
15. Elbourne KB, Keisler D, McMurray RW. Differential effects of estrogen and prolactin on autoimmune disease in the NZB/NZW F1 mouse model of systemic lupus erythematosus. Lupus. 1998;7:420-427.
16. Carlsten H, Holmdahl R, Tarkowski A, Nilsson LA. Oestradiol-And testosterone-mediated effects on the immune system in normal and autoimmune mice are genetically linked and inherited as dominant traits. Immunology. 1989;68:209-214.
17. Carlsten H, Tarkowski A, Holmdahl R, Nilsson LA. Oestrogen is a potent disease accelerator in SLE-prone MRL lpr/lpr mice. Clin Exp Immunol. 1990;80:467-473.
18. Andreescu CE, Milojkovic BA, Haasdijk ED, Kramer P, De Jong FH, Krust A, De Zeeuw CI, De Jeu MT. Estradiol improves cerebellar memory formation by activating estrogen receptor beta. J Neurosci. 2007;27:10832-10839.
19. Venegas-Pont M, Manigrasso MB, Grifoni SC, LaMarca BB, Maric C, Racusen LC, Glover PH, Jones AV, Drummond HA, Ryan MJ. Tumor necrosis factor-Alpha antagonist etanercept decreases blood pressure and protects the kidney in a mouse model of systemic lupus erythematosus. Hypertension. 2010;56:643-649.
20. Ryan MJ, McLemore GR Jr, Hendrix ST. Insulin resistance and obesity in a mouse model of systemic lupus erythematosus. Hypertension. 2006;48:988-993.
21. Venegas-Pont M, Sartori-Valinotti JC, Maric C, Racusen LC, Glover PH, McLemore GR Jr, Jones AV, Reckelhoff JF, Ryan MJ. Rosiglitazone decreases blood pressure and renal injury in a female mouse model of systemic lupus erythematosus. Am J Physiol Regul Integr Comp Physiol. 2009;296:R1282-R1289.
22. Rogers A, Eastell R. The effect of 17beta-estradiol on production of cytokines in cultures of peripheral blood. Bone. 2001;29:30-34.
23. Ralston SH, Russell RG, Gowen M. Estrogen inhibits release of tumor necrosis factor from peripheral blood mononuclear cells in postmenopausal women. J Bone Miner Res. 1990;5:983-988.
24. Arenas IA, Armstrong SJ, Xu Y, Davidge ST. Chronic tumor necrosis factor-Alpha inhibition enhances NO modulation of vascular function in estrogen-deficient rats. Hypertension. 2005;46:76-81.
25. Mathis KW, Venegas-Pont M, Masterson CW, Stewart NJ, Wasson KL, Ryan MJ. Oxidative stress promotes hypertension and albuminuria during the autoimmune disease systemic lupus erythematosus. Hypertension. 2012;59:673-679.
26. Ginzler EM, Felson DT, Anthony JM, Anderson JJ. Hypertension increases the risk of renal deterioration in systemic lupus erythematosus. J Rheumatol. 1993;20:1694-1700.
27. Venegas-Pont M, Mathis KW, Iliescu R, Ray WH, Glover PH, Ryan MJ. Blood pressure and renal hemodynamic responses to acute angiotensin II infusion are enhanced in a female mouse model of systemic lupus erythematosus. Am J Physiol Regul Integr Comp Physiol. 2011;301:R1286-R1292.
28. Ryan MJ, McLemore GR Jr. Hypertension and impaired vascular function in a female mouse model of systemic lupus erythematosus. Am J Physiol Regul Integr Comp Physiol. 2007;292:R736-R742.
29. Kanda N, Tamaki K. Estrogen enhances immunoglobulin production by human PBMCs. J Allergy Clin Immunol. 1999;103(2 Pt 1):282-288.
30. Bynoté KK, Hackenberg JM, Korach KS, Lubahn DB, Lane PH, Gould KA. Estrogen receptor-Alpha deficiency attenuates autoimmune disease in (NZB x NZW)F1 mice. Genes Immun. 2008;9:137-152.
31. Li J, McMurray RW. Effects of estrogen receptor subtype-selective agonists on autoimmune disease in lupus-prone NZB/NZW F1 mouse model. Clin Immunol. 2007;123:219-226.
32. Walker SE, McMurray RW, Besch-Williford CL, Keisler DH. Premature death with bladder outlet obstruction and hyperprolactinemia in New Zealand black X New Zealand white mice treated with ethinyl estradiol and 17 beta-estradiol. Arthritis Rheum. 1992;35:1387-1392.
33. Pearse G, Frith J, Randall KJ, Klinowska T. Urinary retention and cystitis associated with subcutaneous estradiol pellets in female nude mice. Toxicol Pathol. 2009;37:227-234.
34. Wu WM, Lin BF, Su YC, Suen JL, Chiang BL. Tamoxifen decreases renal inflammation and alleviates disease severity in autoimmune NZB/W F1 mice. Scand J Immunol. 2000;52:393-400.
35. Bebo BF Jr, Fyfe-Johnson A, Adlard K, Beam AG, Vandenbark AA, Offner H. Low-dose estrogen therapy ameliorates experimental autoimmune encephalomyelitis in two different inbred mouse strains. J Immunol. 2001;166:2080-2089.
36. Jansson L, Mattsson A, Mattsson R, Holmdahl R. Estrogen induced suppression of collagen arthritis. V: Physiological level of estrogen in DBA/1 mice is therapeutic on established arthritis, suppresses anti-Type II collagen T-cell dependent immunity and stimulates polyclonal B-cell activity. J Autoimmun. 1990;3:257-270.
37. Roa R, Greenstein BD. Evidence for pleomorphism of estrogen receptor capacity and affinity in liver and thymus of immature BALB/c and (NZBxNZW) F1 mice, a model of systemic lupus erythematosus. Int J Immunopharmacol. 2000;22:897-903.
38. Athreya BH, Moore WC, Wadsworth SA, Gupta C, Goldman AS. Estrogen receptor levels in a murine model of systemic lupus erythematosus. Clin Exp Rheumatol. 1989;7:589-593.
39. Dhaher YY, Greenstein B, de Fougerolles Nunn E, Khamashta M, Hughes GR. Strain differences in binding properties of estrogen receptors in immature and adult BALB/c and MRL/MP-lpr/lpr mice, a model of systemic lupus erythematosus. Int J Immunopharmacol. 2000;22:247-254.
40. Ekblom-Kullberg S, Kautiainen H, Alha P, Helve T, Leirisalo-Repo M, Julkunen H. Reproductive health in women with systemic lupus erythematosus compared to population controls. Scand J Rheumatol. 2009;38:375-380.
41. Chang YS, Lai CC, Chen WS, Wang SH, Chou CT, Tsai CY. Protein-losing enteropathy and premature ovarian failure in a young woman with systemic lupus erythematosus. Lupus. 2012;21:1237-1239.
42. Buyon JP, Petri MA, Kim MY, et al. The effect of combined estrogen and progesterone hormone replacement therapy on disease activity in systemic lupus erythematosus: A randomized trial. Ann Intern Med. 2005;142(12 Pt 1):953-962.
43. Mok CC, Lau CS, Ho CT, Lee KW, Mok MY, Wong RW. Safety of hormonal replacement therapy in postmenopausal patients with systemic lupus erythematosus. Scand J Rheumatol. 1998;27:342-346.
44. Kreidstein S, Urowitz MB, Gladman DD, Gough J. Hormone replacement therapy in systemic lupus erythematosus. J Rheumatol. 1997;24: 2149-2152.
45. Sánchez-Guerrero J, González-Pérez M, Durand-Carbajal M, Lara-Reyes P, Jiménez-Santana L, Romero-Diáz J, Cravioto MD. Menopause hormonal therapy in women with systemic lupus erythematosus. Arthritis Rheum. 2007;56:3070-3079.
46. Hochman J, Urowitz MB, Ibañez D, Gladman DD. Hormone replacement therapy in women with systemic lupus erythematosus and risk of cardiovascular disease. Lupus. 2009;18:313-317.
47. Fernández M, Calvo-Alén J, Bertoli AM, Bastian HM, Fessler BJ, McGwin G Jr, Reveille JD, Vilá LM, Alarcón GS. Systemic lupus erythematosus in a multiethnic US cohort (LUMINA L II): Relationship between vascular events and the use of hormone replacement therapy in postmenopausal women. J Clin Rheumatol. 2007;13:261-265.
48. Fernández M, Calvo-Alén J, Alarcón GS, Roseman JM, Bastian HM, Fessler BJ, McGwin G Jr, Vilá LM, Sanchez ML, Reveille JD. Systemic lupus erythematosus in a multiethnic US cohort (LUMINA): XXI. Disease activity, damage accrual, and vascular events in pre-And postmenopausal women. Arthritis Rheum. 2005;52:1655-1664.
49. Kamada M, Irahara M, Maegawa M, Ohmoto Y, Takeji T, Yasui T, Aono T. Postmenopausal changes in serum cytokine levels and hormone replacement therapy. Am J Obstet Gynecol. 2001;184:309-314.
50. Sites CK, Toth MJ, Cushman M, L'Hommedieu GD, Tchernof A, Tracy RP, Poehlman ET. Menopause-related differences in inflammation markers and their relationship to body fat distribution and insulin-stimulated glucose disposal. Fertil Steril. 2002;77:128-135.
51. Mathis KW, Venegas-Pont M, Flynn ER, Williams JM, Maric-Bilkan C, Dwyer TM, Ryan MJ. Hypertension in an experimental model of systemic lupus erythematosus occurs independently of the renal nerves. Am J Physiol Regul Integr Comp Physiol. 2013;305:R711-R719.
52. Herlitz H, Svalander C, Tarkowski A, Westberg G. Effect of captopril on murine systemic lupus erythematosus disease. J Hypertens Suppl. 1988;6:S684-S686.
53. Ingberg E, Theodorsson A, Theodorsson E, Strom JO. Methods for long-Term 17β-estradiol administration to mice. Gen Comp Endocrinol. 2012;175:188-193.
54. Colangelo K, Haig S, Bonner A, Zelenietz C, Pope J. Self-reported flaring varies during the menstrual cycle in systemic lupus erythematosus compared with rheumatoid arthritis and fibromyalgia. Rheumatology (Oxford). 2011;50:703-708.
55. Petri M, Kim MY, Kalunian KC, et al; OC-SELENA Trial. Combined oral contraceptives in women with systemic lupus erythematosus. N Engl J Med. 2005;353:2550-2558.
56. Culwell KR, Curtis KM, del Carmen Cravioto M. Safety of contraceptive method use among women with systemic lupus erythematosus: A systematic review. Obstet Gynecol. 2009;114(2 Pt 1):341-353.
57. Stojan G, Baer AN. Flares of systemic lupus erythematosus during pregnancy and the puerperium: Prevention, diagnosis and management. Expert Rev Clin Immunol. 2012;8:439-453.
58. Muñoz JA, Gil A, López-Dupla JM, Vázquez JJ, González-Gancedo P. Sex hormones in chronic systemic lupus erythematosus. Correlation with clinical and biological parameters. Ann Med Interne (Paris). 1994;145:459-463.