Estradiol binds to insulin and insulin receptor decreasing insulin binding in vitro

Frontiers in Endocrinology

Volumn 5, Issue JUL, 2014, Pages

  Root Bernstein, Robert ^a   Podufaly, Abigail ^b   Dillon, Patrick F ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Gestational diabetes mellitus; Insulin resistance; Metabolic syndrome; Molecular complementarity; Obesity; Ovarian hyperstimulation syndrome; Polycystic ovarian syndrome; Sex hormone binding globulin

Indexed keywords

17ALPHA ESTRADIOL; CHOLESTEROL; CORTICOSTERONE; ESTRADIOL; ESTRIOL; ESTRONE; GENISTEIN; GLUCAGON; HORSERADISH PEROXIDASE; HYDROCORTISONE; INSULIN; INSULIN RECEPTOR; PROGESTERONE; RALOXIFENE; RECOMBINANT HUMAN INSULIN; SELECTIVE ESTROGEN RECEPTOR MODULATOR; SEPRANOLONE; SOMATOMEDIN RECEPTOR; STEROID HORMONE; TAMOXIFEN CITRATE;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CAPILLARY ELECTROPHORESIS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESTROGEN BINDING; HUMAN; INSULIN BINDING; NONHUMAN; PROTON NUCLEAR MAGNETIC RESONANCE; ULTRAVIOLET SPECTROSCOPY;

EID: 84905388729     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2014.00118     Document Type: Article

References (81)

1. Stricker R, Eberhart R, Chevailler MC, Quinn FA, Bischof P, Stricker R. Establishment of detailed reference values for luteinizing hormone, follicle stimulating hormone, estradiol, and progesterone during different phases of the menstrual cycle on the Abbott ARCHITECT analyzer. Clin Chem Lab Med (2006) 44(7):883-7. doi:10.1515/CCLM.2006.160
2. Wu CH, Motohashi T, Abdel-Rahman HA, Flickinger GL, Mikhail G. Free and protein-bound plasma estradiol-17 beta during the menstrual cycle. J Clin Endocrinol Metab (1976) 43(2):436-45. doi:10.1210/jcem-43-2-436
3. Maggio M, Lauretani F, Ceda GP, Bandinelli S, Basaria S, Paolisso G, et al. Estradiol and metabolic syndrome in older Italian men: the inCHIANTI study. J Androl (2010) 31(2):155-62. doi:10.2164/jandrol.108.006098
4. Kauppila A, Järvinen PA. Peripheral blood concentrations of progesterone and oestradiol during human pregnancy and delivery. Acta Physiol Hung (1985) 65(4):473-8.
5. Masuyama H, Hiramatsu Y. Potential role of estradiol and progesterone in insulin resistance through constitutive androstane receptor. J Mol Endocrinol (2011) 47(2):229-39. doi:10.1530/JME-11-0046
6. Vejrazkova D, Vcelak J, Vankova M, Lukasova P, Bradnova O, Halkova T, et al. Steroids and insulin resistance in pregnancy. J Steroid Biochem Mol Biol (2012) 139:122-9. doi:10.1016/j.jsbmb.2012.11.007
7. Kühl C. Etiology and pathogenesis of gestational diabetes. Diabetes Care (1998) 21(Suppl 2):B19-26.
8. Balani J, Hyer SL, Rodin DA, Shehata H. Pregnancy outcomes in women with gestational diabetes treated with metformin or insulin: a case-control study. Diabet Med (2009) 26(8):798-802. doi:10.1111/j.1464-5491.2009.02780.x
9. Sokup A, Swiatkowski M, Tyloch M, Szymanski W. Insulin Lispro as an alternative for insulin Humulin in the treatment of an obese gestational diabetic woman with allergy to Humulin U. Case report. Przegl Lek (2005) 62(4):260-1.
10. Mazor M, Hershkovitz R, Chaim W, Levy J, Sharony Y, Leiberman JR, et al. Human preterm birth is associated with systemic and local changes in progesterone/17 beta-estradiol ratios. Am J Obstet Gynecol (1994) 171(1):231-6. doi:10.1016/0002-9378(94)90474-X
11. Barros RPA, Morani A, Moriscot A, Machado UF. Insulin resistance of pregnancy involves estrogen-induced repression of GLUT-4. Mol Cell Endocrinol (2008) 295:24-31. doi:10.1016/j.mce.2008.07.008
12. Jin Z, Guan X, Gao H, Gao M, Su D, Li W. The change in sex hormone binding globulin and the influence by gestational diabetes in fetal period. Gynecol Endocrinol (2009) 25(10):647-52. doi:10.1080/09513590903015437
13. Jia MC, Zhou LY, Ren S, Dong L, Xiao B. Serum SHBG levels during normal menstrual cycle and after insertion of levonorgestrel-releasing IUD. Adv Contracept (1992) 8(1):33-40. doi:10.1007/BF01849346
14. Ryan EA, O'Sullivan MJ, Skyler JS. Insulin action during pregnancy. Studies with the euglycemic clamp technique. Diabetes (1985) 34(4):380-9. doi:10.2337/diab.34.4.380
15. Seely EW, Solomon CG. Insulin resistance and its role in pregnancy induced hypertension. J Clin Endocrinol Metab (2003) 88(6):2393-8. doi:10.1210/jc.2003-030241
16. Joo BS, Park SH, An BM, Kim KS, Moon SE, Moon HS. Serum estradiol levels during controlled ovarian hyperstimulation influence the pregnancy outcome of in vitro fertilization in a concentration-dependent manner. Fertil Steril (2010) 93(2):442-6. doi:10.1016/j.fertnstert.2009.02.066
17. Vanderlelie J, Bell K, Perkins AV. The serum concentration of estradiol after embryo transfer and the decline from preovulatory levels may influence the success of IVF treatment. Horm Res (2003) 59(2):95-9. doi:10.1159/000068578
18. Diamanti-Kandarakis E, Baillargeon JP, Iuorno MJ, Jakubowicz DJ, Nestler JE. Controversies in endocrinology, a modern medical quandary: polycystic ovary syndrome, insulin resistance, and oral contraceptive pills. J Clin Endocrinol Metab (2003) 88(5):1927-32. doi:10.1210/jc.2002-021528
19. Pandit MK, Burke J, Gustafson AB, Minocha A, Peiris AN. Drug-induced disorders of glucose tolerance. Ann Int Med (1993) 118(7):529-38. doi:10.7326/0003-4819-118-7-199304010-00008
20. Kalkhoff RK. Effects of oral contraceptive agents and sex steroids on carbohydrate metabolism. Annu Rev Med (1972) 23:429-38. doi:10.1146/annurev.me.23.020172.002241
21. Godsland IF, Walton C, Felton C, Proudler A, Patel A, Wynn V. Insulin resistance, secretion, and metabolism in users of oral contraceptives. J Clin Endocrinol Metab (1992) 74(1):64-71. doi:10.1210/jcem.74.1.1530790
22. Sitruk-Ware R, Nath A. Metabolic effects of contraceptive steroids. Rev Endocr Metab Disord (2011) 12(2):63-75. doi:10.1007/s11154-011-9182-4
23. Rimm EB, Manson JE, Stampfer MJ, Colditz GA, Willett WC, Rosner B, et al. Oral contraceptive use and the risk of Type 2 (non-insulin-dependent) diabetes mellitus in a large prospective study of women. Diabetologia (1992) 35:967-72. doi:10.1007/BF00401427
24. Wynn V, Godsland R, Niththyananthan R, Adams PW, Melrose J, Oakley NW, et al. Comparison of effects of different combined oral-contraceptive formulations on carbohydrate and lipid metabolism. Lancet (2003) 313:1045-9. doi:10.1016/S0140-6736(79)92949-0
25. Alberti KG, Zimmet P, Shaw J, IDF Epidemiology Task Force Consensus Group. The metabolic syndrome - a new worldwide definition. Lancet (2005) 366:1059-62. doi:10.1016/S0140-6736(05)67402-8
26. Cohen JC, Hickman R. Insulin resistance and diminished glucose tolerance in power lifters ingesting anabolic steroids. J Clin Endocrinol Metab (1987) 64:960-3. doi:10.1210/jcem-64-5-960
27. Polderman KH, Gooren LJG, Asscheman H, Bakker A, Heine RJ. Induction of insulin resistance by androgens and estrogens. J Clin Endocrinol Metab (1994) 79:265-71. doi:10.1210/jcem.79.1.8027240
28. Seed M, Godsland IF, Wynn V, Jacobs HS. The effects of cyproterone acetate and ethinyl estradiol on carbohydrate metabolism. Clin Endocrinol (1984) 23(6):689-99. doi:10.1111/j.1365-2265.1984.tb01411.x
29. Elbers JMH, Giltay EJ, Teerlink T, Scheffert PG, Asscheman H, Seidell JC, et al. Effects of sex steroids on components of the insulin resistance syndrome in transsexual subjects. Clin Endocrinol (2003) 58:562-71. doi:10.1046/j.1365-2265.2003.01753.x
30. Brettenthaler N, DeGeyter C, Huber PR, Keller U. Effect of the insulin sensitizer pioglitazone on insulin resistance, hyperandrogenism, and ovulatory dysfunction in women with polycystic ovary syndrome. J Clin Endocrinol Metab (2004) 89:3835-40. doi:10.1210/jc.2003-031737
31. Moghetti P, Tosi F, Castello R, Magnani CM, Negri C, Brun E, et al. The insulin resistance in women with hyperandrogenism is partially reversed by antiandrogen treatment: evidence that androgens impair insulin action in women. J Clin Endocrinol Metab (1996) 81(3):953-61.
32. Poretsky L. On the paradox of insulin-induced hyperandrogenism in insulin-resistant states. Endocr Rev (1991) 12(1):3-13. doi:10.1210/edrv-12-1-3
33. Taylor SI, Dons RF, Heranadez E, Roth J, Gorden P. Insulin resistance associated with androgen excess in women with androgen excess in women with autoantibodies to the insulin receptor. Ann Intern Med (1982) 97(6):851-4. doi:10.7326/0003-4819-97-6-851
34. Burghen GA, Givens JR, Kitabchi AE. Correlation of hyperandrogenism with hyperinsulinism in polycystic ovarian disease. J Clin Endocrinol Metab (1980) 50:113-6. doi:10.1210/jcem-50-1-113
35. Azziz R. Diagnostic criteria for polycystic ovary syndrome: a reappraisal. Fertil Steril (2005) 83(5):1343-6. doi:10.1016/j.fertnstert.2005.01.085
36. Ovalle F, Azziz R. Insulin resistance, PCOS, and type 2 diabetes. Fertil Steril (2002) 77(6):1098-105. doi:10.1016/S0015-0282(02)03111-4
37. Ehrmann DA, Barnes RB, Rosenfield RL, Cavaghan MK, Imperial J. Prevelance of impaired glucose tolerance in women with polycystic ovary syndrome. Diabetes Care (1999) 22(1):141-6. doi:10.2337/diacare.22.1.141
38. Duniaf A. Insulin resistance and polycystic ovary syndrome: mechanisms and implications for pathogenesis. Endocr Rev (1997) 18(6):774-800. doi:10.1210/edrv.18.6.0318
39. Elkind-Hirsch KE, Valdes CT, Malinak LR. Insulin resistance improves in hyperandrogenic women treated with Lupron. Fertil Steril (1993) 60:634-41.
40. Barros RPA, Machado UF, Gustafsson J-A. Estrogen receptors: new players in diabetes mellitus. Trends Mol Med (2006) 12(9):425-31. doi:10.1016/j.molmed.2006.07.004
41. Barros RPA, Machado UF, Warner M, Gustafsson J-A. Muscle GLUT4 regulation by estrogen receptors ERß and Era. Proc Natl Acad Sci USA (2006) 103(5):1605-8. doi:10.1073/pnas.0510391103
42. Gorres BK, Bomhoff GL, Morris JK, Geiger PC. In vivo stimulation of oestrogen receptor a increases insulin-stimulated skeletal muscle glucose uptake. J Physiol (2011) 598(8):2041-54. doi:10.1113/jphysiol.2010.199018
43. Alonso-Magdalena P, Ropero AB, Carrera MP, Cederroth CR, Baquie M, Gauthier BR, et al. Pancreatic insulin content regulation by the estrogen receptor Era. PLoS One (2008) 3(4):e2069. doi:10.1371/journal.pone.0002069
44. Olde B, Leeb-Lundberg LMF. GPR30/GPER1: searching for a role in estrogen physiology. Trends Endocrinol Metab (2009) 20(8):409-16. doi:10.1016/j.tem.2009.04.006
45. Manrique C, Lastra G, Habibi J, Mugerfeld I, Garro M, Sowers JR. Loss of estrogen receptor a signaling leads to insulin resistance and obesity in young and adult female mice. Cardiorenal Med (2012) 2:200-10. doi:10.1159/000339563
46. Oh YS, Lee TS, Cheon GJ, Jang I-S, Jun H-S, Park SC. Modulation of insulin sensitivity and caveolin-1 expression by orchidectomy in a nonobese type 2 diabetes animal model. Mol Med (2011) 17(2):4-11. doi:10.2119/molmed.2009.00105
47. Livingstone C, Collison M. Sex steroids and insulin resistance. Clin Sci (2002) 102:151-66. doi:10.1042/CS20010197
48. Gonzalez C, Alonso A, Alvarez N, Diaz F, Martinez M, Fernandez S, et al. Role of 17ß-estradiol and/or progesterone on insulin sensitivity in the rat: implications during pregnancy. J Endocrinol (2000) 166:283-91. doi:10.1677/joe.0.1660283
49. Gonzalez C, Alonso A, Grueso NA, Diaz F, Esteban MM, Fernandez S, et al. Role of 17ß-estradiol administration on insulin sensitivity in the rat: implications for the insulin receptor. Steroids (2002) 67:993-1005. doi:10.1016/S0039-128X(02)00073-9
50. Gonzalez C, Alonso A, Diaz F, Patterson AM. Dose- and time-dependent effects of 17ß-oestradiol on insulin sensitivity in insulin-dependent tissues of rat: implications of IRS-1. J Endocrinol (2003) 176:367-79. doi:10.1677/joe.0.1760367
51. Alonso A, Ordonez P, Fernandez R, Moreno M, Llaneza P, Patterson AM, et al. 17ß-estradiol treatment is unable to reproduce p85a redistribution associated with gestational insulin resistance in rats. J Steroid Biochem Mol Biol (2009) 116:160-70. doi:10.1016/j.jsbmb.2009.05.010
52. Root-Bernstein RS, Dillon PF. Small molecule complementarity as a source of novel pharmaceutical agents and combination therapies. Curr Pharm Des (2008) 14(1):55-62. doi:10.2174/138161208783330727
53. Root-Bernstein RS. Molecular complementarity III. Molecular complementarity as the basis for peptide hormone evolution. A bioinformatic case study of insulin, glucagon, and gastrin. J Theor Biol (2002) 218:71-84. doi:10.1006/jtbi.2002.3056
54. Root-Bernstein RS. Peptide self-aggregation and peptide complementarity as bases for the evolution of peptide receptors: a review. J Mol Recognit (2005) 18:40-9. doi:10.1002/jmr.690
55. Root-Bernstein RS, Vonck J. The insulin receptor binds glucose altering the mutual affinity of insulin for its receptor. Cell Mol Life Sci (2009) 6(16):2721-32. doi:10.1007/s00018-009-0065-8
56. Root-Bernstein RS, Vonck J. Modularity in receptor evolution. Insulin- and glucagon-like peptide modules as binding sites for insulin and glucose in the insulin receptor. J Receptor Ligand Channel Res (2010) 3:87-96. doi:10.2147/JRLCR.S6737
57. Andersson B, Johannsson G, Holm G, Bengtsson BA, Sashegyi A, Pavo I, et al. Raloxifene does not affect insulin sensitivity or glycemic control in postmenopausal women with type 2 diabetes mellitus: a randomized clinical trial. J Clin Endocrinol Metab (2002) 87(1):122-8. doi:10.1210/jcem.87.1.8168
58. Cucinelli F, Soranna L, Romualdi D, Muzj G, Mancuso S, Lanzone A. The effect of raloxifene on glyco-insulinemic homeostasis in healthy postmenopausal women: a randomized placebo-controlled study. J Clin Endocrinol Metab (2002) 87(9):4186-92. doi:10.1210/jc.2001-011302
59. Cagnacci A, Paoletti AM, Zanni A, Arangino S, Ibba G, Orrù M, et al. Raloxifene does not modify insulin sensitivity and glucose metabolism in postmenopausal women. J Clin Endocrinol Metab (2003) 87(9):4117-21.
60. Nadal A, Alonso-Magdalena P, Soriano S, Ropero AB, Quesada I. The role of oestrogens in the adaptation of islets to insulin resistance. J Physiol (2009) 587(Pt 21):5031-7. doi:10.1113/jphysiol.2009.177188
61. Sisci D, Morelli C, Cascio S, Lanzino M, Garofalo C, Reiss K, et al. The estrogen receptor a: insulin receptor substrate 1 complex in breast cancer: structure-function relationships. Ann Oncol (2007) 18(Suppl 6):vi81-6. doi:10.1093/annonc/mdm232
62. Surath S, Banerjee K, Rupley JA. Binding of oligosaccharides to lysozyme temperature and pH dependence of the interaction. J Biol Chem (1973) 248:2117-24.
63. Matsumoto I, Jinbo A, Kitigaki H, Golovtchenko-Matsumoto AM, Seno N. Detection of lectin-sugar interaction by ultraviolet difference spectroscopy. J Biochem (1980) 88:1093-6.
64. Harris WR, Pecoraro VL. Thermodynamic binding constants for gallium transferring. Biochemistry (1983) 22:292-9. doi:10.1021/bi00285a030
65. Khaled MA, Mullins DW, Swindle M, Lacey JC Jr. Complexes of polyadenylic acid and the methyl esters of amino acids. Orig Life (1983) 13:87-96. doi:10.1007/BF00928886
66. Root-Bernstein RS, Dobbelstein C. Insulin binds to glucagon forming a complex that is hyper-antigenic and inducing complementary antibodies having an idiotype-antiidiotype relationship. Autoimmunity (2001) 33:153-69. doi:10.3109/08916930109008044
67. Dillon PF, Root-Bernstein RS, Lieder CM. Ascorbate enhancement of H1 histamine receptor coincides with ascorbate oxidation inhibition by histamine receptors. Am J Physiol Cell Physiol (2006) 291:C977-84. doi:10.1152/ajpcell.00613.2005
68. Dillon PF, Root-Bernstein RS, Lieder CM. Anti-oxidant independent ascorbate enhancement of catecholamine-induced contractions of vascular smooth muscle. Am J Physiol Heart Circ Physiol (2004) 286:H2353-60. doi:10.1152/ajpheart.00968.2003
69. Dillon PF, Root-Bernstein RS, Robinson NE, Abraham WM, Berney C. Ascorbate binding to the adrenergic receptor enhances in vivo and in vitro beta-adrenergic sensitivity. PLoS One (2010) 5(12):e15130. doi:10.1371/journal.pone.0015130
70. Dillon PF, Root-Bernstein RS, Sears PR, Olson LK. Natural electrophoresis of norepinephrine-ascorbic acid complex. J Biophys (2000) 79:370-6. doi:10.1016/S0006-3495(00)76298-9
71. Dillon PF, Lieder CM, Root-Bernstein RS. Molecular shielding of electric field complex dissociation. Biophys J (2006) 90:1432-8. doi:10.1529/biophysj.105.071969
72. Christodoulakos G, Lambrinoudaki I, Panoulis C, Sioulas V, Rizos D, Caramalis G, et al. Serum androgen levels and insulin resistance in postmenopausal women: association with hormone therapy, tibolone and raloxifene. Maturitas (2005) 50(4):321-30. doi:10.1016/j.maturitas.2004.08.002
73. Nagamani M, Szymajda A, Sepilian V, Urban RJ, Gilkison C. Effects of raloxifene on insulin sensitivity, beta-cell function, and hepatic insulin extraction in normal postmenopausal women. Fertil Steril (2008) 89(3):614-9. doi:10.1016/j.fertnstert.2007.03.083
74. Johansson H, Gandini S, Guerrieri-Gonzaga A, Iodice S, Ruscica M, Bonanni B, et al. Effect of fenretinide and low-dose tamoxifen on insulin sensitivity in premenopausal women at high risk for breast cancer. Cancer Res (2008) 68(22):9512-8. doi:10.1158/0008-5472.CAN-08-0553
75. Lee CC, Bloem CJ, Kasa-Vubu JZ, Liang LJ. Effect of oral phytoestrogen on androgenicity and insulin sensitivity in postmenopausal women. Diabetes Obes Metab (2012) 14(4):315-9. doi:10.1111/j.1463-1326.2011.01532.x
76. Gilbert ER, Liu D. Anti-diabetic functions of soy isoflavone genistein: mechanisms underlying its effects on pancreatic ß-cell function. Food Funct (2013) 4(2):200-12. doi:10.1039/c2fo30199g
77. Choi JS, Koh IU, Song J. Genistein reduced insulin resistance index through modulating lipid metabolism in ovariectomized rats. Nutr Res (2012) 32(11):844-55. doi:10.1016/j.nutres.2012.10.002
78. Prasannarong M, Saengsirisuwan V, Piyachaturawat P, Suksamrarn A. Improvements of insulin resistance in ovariectomized rats by a novel phytoestrogen from Curcuma comosa Roxb. BMC Complement Altern Med (2012) 12:28. doi:10.1186/1472-6882-12-28
79. Kahn BB, Flier JS. Obesity and insulin resistance. J Clin Invest (2000) 106(4):473-85. doi:10.1172/JCI10842
80. Hilf R, Hissin PJ, Shafie SM. Regulatory interrelationships for insulin and estrogen action in mammary tumors. Cancer Res (1978) 48:4076-85.
81. Bartha JL, Comino-Delgado R, Romero-Carmona R, Gomez-Jaen MDC. Sex-hormone binding globulin in gestational diabetes. Acta Obstet Gynecol Scand (2005) 79:839-45. doi:10.3109/00016340009169212