Sex hormone binding globulins and atherosclerotic risk in systemic lupus

Lupus

Volumn 9, Issue 3, 2000, Pages 217-222

  Merrill, Joan T ^a   Lahita, R G ^b  

^a ST LUKE S ROOSEVELT HOSPITAL CENTER   (United States)

^b ST VINCENT S HOSPITAL   (United States)

Author keywords

Atherosclerosis; Protein S; Sex hormone binding globulin

Indexed keywords

SEX HORMONE; SEX HORMONE BINDING GLOBULIN;

ATHEROSCLEROSIS; CARDIOVASCULAR RISK; INFLAMMATION; PRIORITY JOURNAL; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS;

EID: 0034074369     PISSN: 09612033     EISSN: None     Source Type: Journal    
DOI: 10.1191/096120300678828307     Document Type: Review

References (91)

1. Nakhla AM, Romas NA, Rosner W. Estradiol activates the prostate androgen receptor and prostate-specific antigen secretion through the intermediacy of sex hormone-binding globulin. J Biol Chem 1997; 272(11): 6838-6841.
2. Gershagen S, Fernlund P, Edenbrandt CM. The genes for SHBG/ABP and the SHBG-like region of vitamin K-dependent protein S have evolved from a common ancestral gene. J Steroid Biochem Mol Biol 1991; 40(4-6): 763-769.
3. Joseph DR, Baker ME. Sex hormone-binding globulin, androgen-binding protein, and vitamin K-dependent protein S are homologous to laminin A, merosin, and Drosophila crumbs protein. FASEB J 1992; 6(7): 2477-2481.
4. Diaz L, Queipo G, Carino C et al. Biologically active steroid and thyroid hormones stimulate secretion of sex hormone-binding globulin by human term placenta in culture. Arch Med Res 1997; 28(1): 29-36.
5. Plymate SR, Hoop RC, Jones RE, Matej LA. Regulation of sex hormone-binding globulin production by growth factors. Metabolism 1990; 39(9): 967-970.
6. Kalme T, Loukovaara M, Koistinen R et al. Estradiol increases the production of sex hormone-binding globulin but not insulin-like growth factor binding protein-1 in cultured human hepatoma cells. Fertil Steril 1999; 72(2): 325-329.
7. Nielsen CH, Poulsen HK, Teisner B et al. Changes in blood levels of proteinase inhibitors, pregnancy zone protein, steroid carriers and complement factors induced by oral contraceptives. Eur J Obstet Gynecol Reprod Biol 1993; 51(1): 63-71.
8. Toscano V, Balducci R, Bianchi P. Steroidal and non-steroidal factors in plasma sex hormone binding globulin regulation. J Steroid Biochem Mol Biol 1992; 43(5): 431-437.
9. Simon J, Klaiber E, Wiita B et al. Differential effects of estrogen-androgen and estrogen-only therapy on vasomotor symptoms, gonadotropin secretion, and endogenous androgen bioavailability in postmenopausal women. Menopause 1999; 6: 138-146.
10. Dechaud H, Ravard C, Claustrat F et al. Xenoestrogen interaction with human sex hormone-binding globulin (hSHBG). Steroids 1999; 64(5): 328-334.
11. Koukkou E, Panayiotidis P, Thalassinos N. Serum soluble interleukin-2 receptors as an index of the biological activity of thyroid hormones in hyperthyroidism. J Endocrinol Invest 1995; 18(4): 253-257.
12. Overlie I, Moen MH, Morkrid L et al. The endocrine transition around menopause-a five years prospective study with profiles of gonadotropines, estrogens, androgens and SHBG among healthy women. Acta Obstet Gynecol Scand 1999; 78(7): 642-647.
13. Brenta G, Schnitman M, Gurfinkiel M et al. Variations of sex hormone-binding globulin in thyroid dysfunction. Thyroid 1999; 9(3): 273-277.
14. Belgorosky A, Ferraris JR, Ramirez JA et al. Serum sex hormone-binding globulin and serum nonsex hormone-binding globulin-bound testosterone fractions in prepubertal boys with chronic renal failure. J Clin Endocrinol Metab 1991; 73(1): 107-110.
15. Lecomte P, Lecureuil N, Lecureuil M et al. Sex differences in the control of sex-hormone-binding globulin in the elderly: role of insulin-like growth factor-I and insulin. Eur J Endocrinol 1998; 139(2): 178-183.
16. Gafny M, Silbergeld A, Klinger B et al. Comparative effects of GH, IGF-I and insulin on serum sex hormone binding globulin. Clin Endocrinol (Oxf). 1994; 41(2): 169-175.
17. Pugeat M, Crave JC, Elmidani M et al. Pathophysiology of sex hormone binding globulin (SHBG): relation to insulin. J Steroid Biochem Mol Biol 1991; 40(4-6): 841-849.
18. Weaver JU, Holly JM, Kopelman PG et al. Decreased sex hormone binding globulin (SHBG) and insulin-like growth factor binding protein (IGFBP-1) in extreme obesity. Clin Endocrinol (Oxf) 1990; 33(3): 415-422.
19. Schwarz S, Tappeiner G, Hintner H. Hormone binding globulin levels in patients with hereditary angiooedema during treatment with Danazol. Clin Endocrinol (Oxf) 1981; 14(6): 563-570.
20. Nakhla AM, Leonard J, Hryb DJ, Rosner W. Sex hormone-binding globulin receptor signal transduction proceeds via a G protein. Steroids 1999; 64(3): 213-216.
21. O'Donnell K, Harkes IC, Dougherty E, Wicks IP. Expression of receptor tyrosine kinase Axl and its ligand Gas6 in rheumatoid arthritis: evidence for a novel endothelial cell survival pathway. Am J Pathol 1999; 154(4): 1171-1180.
22. He X, Shen L, Malmborg AC et al. Einse S Binding site for C4b-binding protein in vitamin K-dependent protein S fully contained in carboxy-terminal laminin-G-type repeats. A study using recombinant factor IX-protein S chimeras and surface plasmon resonance. Biochemistry 1997; 36(12): 3745-3754.
23. Boerger LM, Morris PC, Thurnau GR et al. Oral contraceptives and gender affect protein S status. Blood 1987; 69(2): 692-694.
24. Nakamura YS, Hakeda Y, Takakura N et al. Tyro 3 receptor tyrosine kinase and its ligand, Gas6, stimulate the function of osteoclasts. Stem Cells 1998; 16(3): 229-238.
25. Hergenc G, Schulte H, Assmann G, von Eckardstein A. Associations of obesity markers, insulin, and sex hormones with HDL-cholesterol levels in Turkish and German individuals. Atherosclerosis 1999; 145(1): 147-156.
26. Sherif K, Kushner H, Falkner BE. Sex hormone-binding globulin and insulin resistance in African-American women. Metabolism 1998; 47(1): 70-74.
27. Tchernof A, Labrie F, Belanger A et al. Relationships between endogenous steroid hormone, sex hormone-binding globulin and lipoprotein levels in men: contribution of visceral obesity, insulin levels and other metabolic variables. Atherosclerosis 1997; 133(2): 235-244.
28. Larsson H, Ahren B. Androgen activity as a risk factor for impaired glucose tolerance in postmenopausal women. Diabetes Care 1996; 19(12): 1399-1403.
29. Shono N, Kumagai S, Higaki Y et al. The relationships of testosterone, estradiol, dehydroepiandrosterone-sulfate and sex hormone-binding globulin to lipid and glucose metabolism in healthy men. J Atheroscler Thromb 1996; 3(1): 45-51.
30. Haffner SM, Dunn JF, Katz MS. Relationship of sex hormone-binding globulin to lipid, lipoprotein, glucose, and insulin concentrations in postmenopausal women. Metabolism 1992; 41(3): 278-284.
31. Hamalainen E, Tikkanen H, Harkonen M et al. Serum lipoproteins, sex hormones and sex hormone binding globulin in middle-aged men of different physical fitness and risk of coronary heart disease. Atherosclerosis 1987; 67(2-3): 155-162.
32. Stefanick ML, Williams PT, Krauss RM et al. Relationships of plasma estradiol, testosterone, and sex hormone-binding globulin with lipoproteins, apolipoproteins, and high density lipoprotein subfractions in men. J Clin Endocrinol Metab 1987; 64(4): 723-729.
33. Tchernof A, Labrie F, Belanger A et al. Relationships between endogenous steroid hormone, sex hormone-binding globulin and lipoprotein levels in men: contribution of visceral obesity, insulin levels and other metabolic variables. Atherosclerosis 1997; 133(2): 235-244.
34. Pugeat M, Moulin P, Cousin P et al. Crave JC; Lejeune H Interrelations between sex hormone-binding globulin (SHBG), plasma lipoproteins and cardiovascular risk. J Steroid Biochem Mol Biol 1995; 53(1-6): 567-572.
35. De Pergola G, De Mitrio V, Sciaraffia M et at. Lower androgenicity is associated with higher plasma levels of prothrombotic factors irrespective of age, obesity, body fat distribution, and related metabolic parameters in men. Metabolism 1997; 46(11): 1287-1293.
36. Giltay EJ, Hoogeveen EK, Elbers JM et al. Effects of sex steroids on plasma total homocysteine levels: a study in transsexual males and females. J Clin Endocrinol Metab 1998; 83(2): 550-553.
37. Phillips GB, Pinkernell BH, Jing TY. Relationship between serum sex hormones and coronary artery disease in postmenopausal women. Arterioscler Thromb Vase Biol 1997; 17(4): 695-701.
38. Goodman-Gruen D, Barrett-Connor E. A prospective study of sex hormone-binding globulin and fatal cardiovascular disease in Rancho Bernardo men and women. J din Endocrinol Metab 1996; 81(8): 2999-3003.
39. Hautanen A, Manttari M, Manninen V et al. Adrenal androgens and testosterone as coronary risk factors in the Helsinki Heart Study. Atherosclerosis 1994; 105(2): 191-200.
40. Merrill JT, J Schappert, RC Shriky et al. Decreased anticoagulant protein S and the homologous sex hormone binding globulin in patients enrolled in the SELENA (estrogen safety) study. Arthritis Rheum 1998; 41: S139 (abstract).
41. Rosner W, Hryb DJ, Khan MS et al. Sex hormone-binding globulin mediates steroid hormone signal transduction at the plasma membrane. J Steroid Biochem Mol Biol 1999; 69(1-6): 481-485.
42. Joseph DR. Sequence and functional relationships between androgen-binding protein/sex hormone-binding globulin and its homologs protein S, Gas6, laminin, and agrin. Steroids 1997; 62(8-9): 578-588.
43. Fortunati N, Comba A, Becchis M et al. MCF-7 cell progesterone receptor (PGR) is additionally modulated by sex steroid binding protein (SBP) and its membrane receptor (SBP-R) through cAMP and PKA. Ann NY Acad Sci 1996; 784: 453-457.
44. Mark MR, Chen J, Hammonds RG et al. Characterization of Gas6, a member of the superfamily of G domain-containing proteins, as a ligand for Rse and Axl. J Biol Chem 1996; 271(16): 9785-9789.
45. Nagata K, Ohashi K, Nakano T et al. Identification of the product of growth arrest-specific gene 6 as a common ligand for Axl, Sky, and Mer receptor tyrosine kinases. J Biol Chem 1996; 271(47): 30022-30027.
46. Tomobe YI, Hama H, Sakurai T et al. Anticoagulant factor protein S inhibits the proliferation of rat astrocytes after injury. Neurosci Lett 1996; 214(1): 57-60.
47. Crosier PS, Freeman SA, Orlic D et al. The Dtk receptor tyrosine kinase, which binds protein S, is expressed during hematopoiesis. Exp Hematol 1996; 24(2): 318-323.
48. Ohashi K, Nagata K, Toshima J et al. Stimulation of sky receptor tyrosine kinase by the product of growth arrest-specific gene 6. J Biol Chem 1995; 270(39): 22681-22684.
49. Stitt TN, Conn G, Gore M et al. The anticoagulation factor protein S and its relative, Gas6, are ligands for the Tyro 3/Axl family of receptor tyrosine kinases. Cell 1995; 80(4): 661-670.
50. Mark MR, Chen J, Hammonds RG et al. Characterization of Gas6, a member of the superfamily of G domain-containing proteins, as a ligand for Rse and Axl. J Biol Chem 1996; 271(16): 9785-9789.
51. Chen J, Carey K, Godowski PJ. Identification of Gas6 as a ligand for Mer, a neural cell adhesion molecule related receptor tyrosine kinase implicated in cellular transformation. Oncogene 1997; 14(17) 2033-2039.
52. Nakano T, Higashino K, Kikuchi N et al. Vascular smooth muscle cell-derived, Gla-containing growth-potentiating factor for Ca(2 + )-mobilizing growth factors. J Biol Chem 1995; 270(11): 5702-5705.
53. Nyberg P, He X, Hardig Y et al. Stimulation of Sky tyrosine phosphorylation by bovine protein S- domains involved in the receptor-ligand interaction. Eur J Biochem 1997; 246(1): 147-154.
54. Wimmel A, Rohner I, Ramaswamy A et al. Synthesis and secretion of the anticoagulant protein S and coexpression of the Tyro3 receptor in human lung carcinoma cells. Cancer 1999; 86(1): 43-49.
55. Nyberg P, He X, Hardig Y et al. Stimulation of Sky tyrosine phosphorylation by bovine protein S-domains involved in the receptor-ligand interaction. Eur J Biochem 1997; 246(1): 147-154.
56. Hooper WC, Phillips DJ, Renshaw MA et al. The up-regulation of IL-6 and IL-8 in human endothelial cells by activated protein C . J Immunol 1998; 161(5): 2567-2573.
57. Smiley ST, Stitt TN, Grusby MJ. Cross-linking of protein S bound to lymphocytes promotes aggregation and inhibits proliferation. Cell Immunol 1997; 181(2): 120-126.
58. Esmon CT, Fukudome K. Cellular regulation of the protein C pathway. Semin Cell Biol 1995; 6(5): 259-268.
59. Esmon CT. Inflammation and thrombosis: the impact of inflammation on the protein C anticoagulant pathway. Haematologica 1995; 80(2 Suppl): 49-56.
60. Scharfstein J, Rerreira A, Gigli I, Nussenzweig V. Human C4-binding protein. Isolation and characterization. J Exp Med 1978; 148: 207-222.
61. Malm J, Laurell M, Dahlback B. Changes in the plasma levels of vitamin K-dependent proteins C and S and of C4b-binding protein during pregnancy and oral contraception. Br J Haem 1988; 68: 437-443.
62. Barnum SR, Dahlback B. C4b-binding protein, a regulatory component of the classical pathway of complement, is an acute-phase protein and is elevated in systemic lupus erythematosus. Complement Inflamm 1990; 7: 71.
63. D'Angelo A, Vigano-D'Angelo S, Esmon CT, Comp PC. Acquired deficiencies of protein S. Protein S activity during oral anticoagulation, in liver disease, and in disseminated intravascular coagulation. J Clin Invest 1988; 81: 1445.
64. Hesselvik JF, Malm J, Dahlback B, Blomback M. Protein C, protein S and C4b binding protein in severe infection and septic shock. Thromb Haemost 1991; 65: 126.
65. D'Angelo A, Gerosa S, D'Angelo SV et al Protein S and protein C anticoagulant activity in acute and chronic cardiac ischemic syndromes. Relationship to inflammation, complement activation and in vivo thrombin activity. Thromb Res 1994; 75(2): 133-142.
66. Garcia de Frutos P, Alim RI, Hardig Y et al. Differential regulation of alpha and beta chains of C4b-binding protein during acute-phase response resulting in stable plasma levels of free anticoagulant protein S. Blood 1994; 84(3): 815-822.
67. Ruiz Arguelles CJ, Ruiz Arguelles A, Alarcon Segovia D. Natural anticoagulants in systemic lupus erythematosus. Deficiency of protein S bound to C4bp associates with recent history of venous thromboses, antiphospholipid antibodies and the antiphospholipid syndrome. J Rheum 1991; 10: 552-558.
68. Moreb J, Kitchens CS. Acquired functional protein S deficiency, cerbral venous thrombosis and coumarin skin necrosis in association with antiphospholipid syndrome: report of two cases. Am J Med 1989; 87: 207-210.
69. Sthoeger ZM, Sthoeger D, Mellnick SD. Transient anticardiolipin antibodies, functional protein S deficiency, and deep vein thrombosis. Am J Hem 1991; 36: 206-207.
70. Walker TS, Triplett DA, Javed N, Musgrave K. Evaluation of lupus anticoagulants: antiphospholipid antibodies, endothelium associated immunoglobulin, endothelial prostacyclin secretion, and antigenic protein S levels. Thromb Rex 1983; 51: 267-281.
71. Parke AL, Weinstein RE, Bona RD. The thrombotic diathesis associated with the presence of antiphospholipid antibodies may be due to low levels of free protein S. Am J Med 1992; 93: 49-56.
72. Reverter JC, Tassies D, Font J et al. Hypercoagulable state in patients with antiphospholipid syndrome is related to high induced tissue factor expression on monocytes and to low free protein S. Arterioscler Thromb Vase Biol 1996; 16: 1319-1326.
73. Ames PR, Tommasino C, Iannaccone L et al. Coagulation activation and fibrinolytic imbalance in subjects with idiopathic antiphospholipid antibodies-a crucial role for acquired free protein S deficiency. Thromb Haemost 1996; 76: 190-194.
74. Ginsberg JS, Demers C, Brill-Edwards P A et al. Acquired free protein S deficiency is associated with antiphospholipid antibodies and increased thrombin generation in patients with systemic lupus erythematosus. Am J Med 1995; 98: 379-383.
75. Amster MS, Conway J, Zeid M, Pincus S. Cutaneous necrosis resulting from protein S deficiency and increased antiphospholipid antibody in a patient with systemic erythematosus. J Am Acad Derm 1993; 29: 853-857.
76. Forastiero RR, Kordich L, Basilotta E, Carreras Lo. Differences in protein S and C4b-binding protein levels in different groups of groups of patients with antiphospholipid antibodies. Blood Coag Fibrinolys 1994; 5: 609-616.
77. Wattiaux MJ, Herve R, Robert A et al. Coumarin-induced skin nerosis associated with acquired protein S deficiency and antiphospholipid antibody syndrome. Arthritis Rheum 1994; 37: 1096-1100.
78. Sorice M, Arcieri P, Griggi T et al. Inhibition of protein S by autoantibodies in patients with acquired protein S deficiency. Thromb Haemost 1996; 75: 555-559.
79. Merill JT, C Shen, B Butman, et al. β, glycoprotein-1, a major target antigen of antiphospholipid antibodies, interferes with the binding of protein S by C4b Binding protein and enhances the anticoagulant function of protein S. Thromb Haemost 1999; 81: 748-757.
80. Villoutreix BO, Teleman O, Dahlback B. A theoretical model for the Gla-TSR-EGF-1 region of the anticoagulant cofactor protein S: from biostructural pathology to species-specific cofactor activity. J Comput Aided Mol Des 1997; 11(3): 293-304.
81. Van Wijnen M, Stam JG, Chang GT et al. Characterization of miniprotein S, a recombinant variant or protein S that lacks the sex hormone binding globulin-like domain. Biochem J 1998; 330: 389-396.
82. Chang GT, Maas BH, Ploos van Amstel HK et al. Studies of the interaction between human protein S and human C4b-binding protein using deletion variants of recombinant human protein S. Thromb Haemost 1994; 71(4): 461-467.
83. Norberg R, Nived O, Strurfeld G. Anticardiolipin and complement activation: relation to clinical symptoms. J Rheum 1987; 14: 149-153.
84. Peitsch MC, Kovacsovics TJ. Antibody-independent activation of Cl. II. Evidence for two classes of nonimmune activators of the classical pathway of complement. J Immunol 1987; 138: 1871-1876.
85. Fukumura H, Hayoshi K, Yoshikawa S. Complement-induced thrombus formation on the surface of poly(N-vinylpyrrolidone)-grafted polyethylene. Biomaterials 1987; 8: 74.
86. Unander AM, Norberg R, Hahn L, Arfors L. Anticardiolipin antibodies and complement in 99 women with habitual abortion. Am J Obstet Gynecol 1987; 156: 114-119.
87. Cheng HM, Yap SF. Anticardiolipin and complement. Arthritis Rheum 1988; 31: 1211-1212.
88. Schwalbe R, Dahlback B, Hillarp A et al. Assembly of protein S and C4b-binding protein on membranes. J Biol Chem 1990; 265: 16074-16081.
89. Dahlback B. Protein S and C4b-binding protein: components involved in the regulation of the protein C anticoagulant system. Thromb Haemoxt 1991; 66: 49-61.
90. Furmaniak-Kazmierczak E, Hu CY, Esmon CT. Protein S enhances C4b binding protein interaction with neutrophils. Blood 1993; 81(2): 405-411.
91. Barreca T, Picciotto A, Franceschini R et al. Sex hormones and sex hormone-binding globulin in males with chronic viral hepatitis during recombinant interferon-alpha 2b theraphy. J Interferon Res 1993; 13(3): 209-211.