Molecular and structural basis of steroid hormone binding and release from corticosteroid-binding globulin

Molecular and Cellular Endocrinology

Volumn 316, Issue 1, 2010, Pages 3-12

  Lin, Hai Yan ^a,b   Muller, Yves A ^c   Hammond, Geoffrey L ^b  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Corticosteroid binding globulin; Neutrophil elastase; Reactive center loop; S to R transition; Serpin

Indexed keywords

ALPHA 1 ANTITRYPSIN; LEUKOCYTE ELASTASE; SERINE PROTEINASE INHIBITOR; SINGLE STRANDED DNA BINDING PROTEIN; STEROID; THYROXINE BINDING GLOBULIN; TRANSCORTIN;

ALLOSTERISM; AMINO TERMINAL SEQUENCE; BETA SHEET; BINDING SITE; COMPUTER MODEL; CRYSTAL STRUCTURE; GENE MUTATION; GENETIC VARIABILITY; HUMAN; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SEQUENCE HOMOLOGY; STEROID BINDING; STEROID RELEASE;

ALLOSTERIC REGULATION; ANIMALS; ANTITHROMBINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; GENETIC VARIATION; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; STEROIDS; THYROXINE-BINDING GLOBULIN; TRANSCORTIN;

EID: 72249118431     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2009.06.015     Document Type: Review

References (83)

1. Ali S., and Bassett J.R. Studies on the role of glycosylation in the origin of the electrophoretic variants for rat corticosteroid-binding globulin. Steroids 60 (1995) 743-752
2. Arnold K., Bordoli L., Kopp J., and Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22 (2006) 195-201
3. Aulak K.S., Eldering E., Hack C.E., Lubbers Y.P., Harrison R.A., Mast A., Cicardi M., and Davis III A.E. A hinge region mutation in C1-inhibitor (Ala436 → Thr) results in nonsubstrate-like behavior and in polymerization of the molecule. J. Biol. Chem. 268 (1993) 18088-18094
4. Avvakumov G.V. Structure and function of corticosteroid-binding globulin: role of carbohydrates. J. Steroid Biochem. Mol. Biol. 53 (1995) 515-522
5. Avvakumov G.V., and Hammond G.L. Glycosylation of human corticosteroid-binding globulin Differential processing and significance of carbohydrate chains at individual sites. Biochemistry 33 (1994) 5759-5765
6. Avvakumov G.V., and Hammond G.L. Substitutions of tryptophan residues in human corticosteroid-binding globulin: impact on steroid binding and glycosylation. J. Steroid Biochem. Mol. Biol. 49 (1994) 191-194
7. Avvakumov G.V., Warmels-Rodenhiser S., and Hammond G.L. Glycosylation of human corticosteroid-binding globulin at aspargine 238 is necessary for steroid binding. J. Biol. Chem. 268 (1993) 862-866
8. Baglin T.P., Carrell R.W., Church F.C., Esmon C.T., and Huntington J.A. Crystal structures of native and thrombin-complexed heparin cofactor II reveal a multistep allosteric mechanism. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 11079-11084
9. Banda M.J., Clark E.J., Sinha S., and Travis J. Interaction of mouse macrophage elastase with native and oxidized human alpha 1-proteinase inhibitor. J. Clin. Invest. 79 (1987) 1314-1317
10. Baumann U., Huber R., Bode W., Grosse D., Lesjak M., and Laurell C.B. Crystal structure of cleaved human alpha 1-antichymotrypsin at 2.7 A resolution and its comparison with other serpins. J. Mol. Biol. 218 (1991) 595-606
11. Brantly M., Nukiwa T., and Crystal R.G. Molecular basis of alpha-1-antitrypsin deficiency. Am. J. Med. 84 (1988) 13-31
12. Breuner C.W., and Orchinik M. Plasma binding proteins as mediators of corticosteroid action in vertebrates. J. Endocrinol. 175 (2002) 99-112
13. Carrell R.W., Jeppsson J.O., Laurell C.B., Brennan S.O., Owen M.C., Vaughan L., and Boswell D.R. Structure and variation of human alpha 1-antitrypsin. Nature 298 (1982) 329-334
14. Caso R., Lane D.A., Thompson E.A., Olds R.J., Thein S.L., Panico M., Blench I., Morris H.R., Freyssinet J.M., Aiach M., et al. Antithrombin Vicenza, Ala 384 to Pro (GCA to CCA) mutation, transforming the inhibitor into a substrate. Br. J. Haematol. 77 (1991) 87-92
15. Cherkasov A., Ban F., Li Y., Fallahi M., and Hammond G.L. Progressive docking: a hybrid QSAR/docking approach for accelerating in silico high throughput screening. J. Med. Chem. 49 (2006) 7466-7478
16. Corral J., Aznar J., Gonzalez-Conejero R., Villa P., Minano A., Vaya A., Carrell R.W., Huntington J.A., and Vicente V. Homozygous deficiency of heparin cofactor II: relevance of P17 glutamate residue in serpins, relationship with conformational diseases, and role in thrombosis. Circulation 110 (2004) 1303-1307
17. Davis III A.E., Aulak K., Parad R.B., Stecklein H.P., Eldering E., Hack C.E., Kramer J., Strunk R.C., Bissler J., and Rosen F.S. C1 inhibitor hinge region mutations produce dysfunction by different mechanisms. Nat. Genet. 1 (1992) 354-358
18. Defaye G., Basset M., Monnier N., and Chambaz E.M. Electron spin resonance study of human transcortin: thiol groups and binding site topography. Biochim. Biophys. Acta 623 (1980) 280-294
19. Dey R., and Roychowdhury P. Homology model of human corticosteroid binding globulin: a study of its steroid binding ability and a plausible mechanism of steroid hormone release at the site of inflammation. J. Mol. Model. 9 (2003) 183-189
20. Edgar P., and Stein P. Hormone binding site of corticosteroid binding globulin. Nat. Struct. Biol. 2 (1995) 196-197
21. Emptoz-Bonneton A., Cousin P., Seguchi K., Avvakumov G.V., Bully C., Hammond G.L., and Pugeat M. Novel human corticosteroid-binding globulin variant with low cortisol-binding affinity. J. Clin. Endocrinol. Metab. 85 (2000) 361-367
22. Gettins P.G. Serpin structure, mechanism, and function. Chem. Rev. 102 (2002) 4751-4804
23. Grenot C., Blachere T., Rolland De Ravel M., Mappus E., and Cuilleron C.Y. Identification of Trp-371 as the main site of specific photoaffinity labeling of corticosteroid binding globulin using delta 6 derivatives of cortisol, corticosterone, and progesterone as unsubstituted photoreagents. Biochemistry 33 (1994) 8969-8981
24. Guyonnet-Duperat V., Geverink N., Plastow G.S., Evans G., Ousova O., Croisetiere C., Foury A., Richard E., Mormede P., and Moisan M.P. Functional implication of an Arg307Gly substitution in corticosteroid-binding globulin, a candidate gene for a quantitative trait locus associated with cortisol variability and obesity in pig. Genetics 173 (2006) 2143-2149
25. Hammond G.L. Molecular properties of corticosteroid binding globulin and the sex-steroid binding proteins. Endocr. Rev. 11 (1990) 65-79
26. Hammond G.L., Smith C.L., Goping I.S., Underhill D.A., Harley M.J., Reventos J., Musto N.A., Gunsalus G.L., and Bardin C.W. Primary structure of human corticosteroid binding globulin, deduced from hepatic and pulmonary cDNAs, exhibits homology with serine protease inhibitors. Proc. Natl. Acad. Sci. U.S.A. 84 (1987) 5153-5157
27. Hammond G.L., Smith C.L., Paterson N.A., and Sibbald W.J. A role for corticosteroid-binding globulin in delivery of cortisol to activated neutrophils. J. Clin. Endocrinol. Metab. 71 (1990) 34-39
28. Hammond G.L., Smith C.L., Underhill C.M., and Nguyen V.T. Interaction between corticosteroid binding globulin and activated leukocytes in vitro. Biochem. Biophys. Res. Commun. 172 (1990) 172-177
29. Hammond G.L., Smith C.L., and Underhill D.A. Molecular studies of corticosteroid binding globulin structure, biosynthesis and function. J. Steroid Biochem. Mol. Biol. 40 (1991) 755-762
30. Hill R.E., and Hastie N.D. Accelerated evolution in the reactive centre regions of serine protease inhibitors. Nature 326 (1987) 96-99
31. Hood D.B., Huntington J.A., and Gettins P.G. Alpha 1-proteinase inhibitor variant T345R Influence of P14 residue on substrate and inhibitory pathways. Biochemistry 33 (1994) 8538-8547
32. Hopkins P.C., Carrell R.W., and Stone S.R. Effects of mutations in the hinge region of serpins. Biochemistry 32 (1993) 7650-7657
33. Hossner K.L., and Billiar R.B. Plasma clearance and organ distribution of native and desialylated rat and human transcortin: species specificity. Endocrinology 108 (1981) 1780-1786
34. Huntington J.A., Fan B., Karlsson K.E., Deinum J., Lawrence D.A., and Gettins P.G. Serpin conformational change in ovalbumin Enhanced reactive center loop insertion through hinge region mutations. Biochemistry 36 (1997) 5432-5440
35. Irving J.A., Pike R.N., Lesk A.M., and Whisstock J.C. Phylogeny of the serpin superfamily: implications of patterns of amino acid conservation for structure and function. Genome Res. 10 (2000) 1845-1864
36. Jin L., Abrahams J.P., Skinner R., Petitou M., Pike R.N., and Carrell R.W. The anticoagulant activation of antithrombin by heparin. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 14683-14688
37. Johnson D., and Travis J. Structural evidence for methionine at the reactive site of human alpha-1-proteinase inhibitor. J. Biol. Chem. 253 (1978) 7142-7144
38. Johnson D., and Travis J. The oxidative inactivation of human alpha-1-proteinase inhibitor. Further evidence for methionine at the reactive center. J. Biol. Chem. 254 (1979) 4022-4026
39. Kato E.A., Hsu B.R., and Kuhn R.W. Comparative structural analyses of corticosteroid binding globulin. J. Steroid Biochem. 29 (1988) 213-220
40. Khan M.S., and Rosner W. Investigation of the binding site of human corticosteroid-binding globulin by affinity labeling. Demonstration of a cysteinyl residue in the binding site. J. Biol. Chem. 252 (1977) 1895-1900
41. Klieber M.A., Underhill C., Hammond G.L., and Muller Y.A. Corticosteroid-binding globulin, a structural basis for steroid transport and proteinase-triggered release. J. Biol. Chem. 282 (2007) 29594-29603
42. Law R.H., Zhang Q., Mcgowan S., Buckle A.M., Silverman G.A., Wong W., Rosado C.J., Langendorf C.G., Pike R.N., Bird P.I., and Whisstock J.C. An overview of the serpin superfamily. Genome Biol. 7 (2006) 216
43. Lawrence D.A., Olson S.T., Muhammad S., Day D.E., Kvassman J.O., Ginsburg D., and Shore J.D. Partitioning of serpin-proteinase reactions between stable inhibition and substrate cleavage is regulated by the rate of serpin reactive center loop insertion into beta-sheet A. J. Biol. Chem. 275 (2000) 5839-5844
44. Libert C., Wielockx B., Hammond G.L., Brouckaert P., Fiers W., and Elliott R.W. Identification of a locus on distal mouse chromosome 12 that controls resistance to tumor necrosis factor-induced lethal shock. Genomics 55 (1999) 284-289
45. Lin H.Y., Underhill C., Gardill B.R., Muller Y.A., and Hammond G.L. Residues in the human corticosteroid-binding globulin reactive center loop that influence steroid binding before and after elastase cleavage. J. Biol. Chem. 284 (2009) 884-896
46. Little R.J., and Rodriguez C.G. Modeling of human corticosteroid binding globulin Use of structure-activity relations in soft steroid binding to refine the structure. Pharm. Res. 22 (2005) 1783-1792
47. Lukacs C.M., Zhong J.Q., Plotnick M.I., Rubin H., Cooperman B.S., and Christianson D.W. Arginine substitutions in the hinge region of antichymotrypsin affect serpin beta-sheet rearrangement. Nat. Struct. Biol. 3 (1996) 888-893
48. Mager D.E. Quantitative structure-pharmacokinetic/pharmacodynamic relationships. Adv. Drug Deliv. Rev. 58 (2006) 1326-1356
49. Marver D., Chiu W., Wolff M.E., and Edelman I.S. Photoaffinity site-specific covalent labeling of human corticosteroid-binding globulin. Proc. Natl. Acad. Sci. U.S.A. 73 (1976) 4462-4466
50. Mccoy A.J., Pei X.Y., Skinner R., Abrahams J.P., and Carrell R.W. Structure of beta-antithrombin and the effect of glycosylation on antithrombin's heparin affinity and activity. J. Mol. Biol. 326 (2003) 823-833
51. Mickelson K.E., Harding G.B., Forsthoefel M., and Westphal U. Steroid-protein interactions Human corticosteroid-binding globulin: characterization of dimer and electrophoretic variants. Biochemistry 21 (1982) 654-660
52. Molho-Sabatier P., Aiach M., Gaillard I., Fiessinger J.N., Fischer A.M., Chadeuf G., and Clauser E. Molecular characterization of antithrombin III (ATIII) variants using polymerase chain reaction. Identification of the ATIII Charleville as an Ala 384 Pro mutation. J. Clin. Invest. 84 (1989) 1236-1242
53. Mourey L., Samama J.P., Delarue M., Petitou M., Choay J., and Moras D. Crystal structure of cleaved bovine antithrombin III at 3 2 A resolution. J. Mol. Biol. 232 (1993) 223-241
54. Namciu S.J., Friedman R.D., Marsden M.D., Sarausad L.M., Jasoni C.L., and Fournier R.E. Sequence organization and matrix attachment regions of the human serine protease inhibitor gene cluster at 14q32 1. Mamm. Genome 15 (2004) 162-178
55. Nyberg L., Marekov L.N., Jones I., Lundquist G., and Jornvall H. Characterization of the murine corticosteroid binding globulin: variations between mammalian forms. J. Steroid Biochem. 35 (1990) 61-65
56. Orava M., Zhao X.F., Leiter E., and Hammond G.L. Structure and chromosomal location of the gene encoding mouse corticosteroid-binding globulin: strain differences in coding sequence and steroid-binding activity. Gene 144 (1994) 259-264
57. Pemberton P.A., Stein P.E., Pepys M.B., Potter J.M., and Carrell R.W. Hormone binding globulins undergo serpin conformational change in inflammation. Nature 336 (1988) 257-258
58. Perry D.J., Harper P.L., Fairham S., Daly M., and Carrell R.W. Antithrombin Cambridge 384 Ala to Pro: a new variant identified using the polymerase chain reaction. FEBS Lett. 254 (1989) 174-176
59. Petersen H.H., Andreassen T.K., Breiderhoff T., Brasen J.H., Schulz H., Gross V., Grone H.J., Nykjaer A., and Willnow T.E. Hyporesponsiveness to glucocorticoids in mice genetically deficient for the corticosteroid binding globulin. Mol. Cell. Biol. 26 (2006) 7236-7245
60. Robinson P.A., and Hammond G.L. Identification and characterization of a human corticosteroid binding globulin variant with a reduced affinity for cortisol. J. Endocrinol. 104 (1985) 269-277
61. Rollini P., and Fournier R.E. The HNF-4/HNF-1alpha transactivation cascade regulates gene activity and chromatin structure of the human serine protease inhibitor gene cluster at 14q32 1. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 10308-10313
62. Ryu S.E., Choi H.J., Kwon K.S., Lee K.N., and Yu M.H. The native strains in the hydrophobic core and flexible reactive loop of a serine protease inhibitor: crystal structure of an uncleaved alpha1-antitrypsin at 2.7 A. Structure 4 (1996) 1181-1192
63. Sandberg A.A., Woodruff M., Rosenthal H., Nienhouse S., and Slaunwhite Jr. W.R. Transcortin: a corticosteroid-binding protein of plasma VII. Half-life in normal and estrogen-treated subjects. J. Clin. Invest. 43 (1964) 461-466
64. Scrocchi L.A., Hearn S.A., Han V.K., and Hammond G.L. Corticosteroid-binding globulin biosynthesis in the mouse liver and kidney during postnatal development. Endocrinology 132 (1993) 910-916
65. Scrocchi L.A., Orava M., Smith C.L., Han V.K., and Hammond G.L. Spatial and temporal distribution of corticosteroid-binding globulin and its messenger ribonucleic acid in embryonic and fetal mice. Endocrinology 132 (1993) 903-909
66. Seal U.S., and Doe R.P. Corticosteriod-binding globulin: species distribution and small-scale purification. Endocrinology 73 (1963) 371-376
67. Seralini G.E., Berube D., Gagne R., and Hammond G.L. The human corticosteroid binding globulin gene is located on chromosome 14q31-q32.1 near two other serine protease inhibitor genes. Hum. Genet. 86 (1990) 73-75
68. Siiteri P.K., Murai J.T., Hammond G.L., Nisker J.A., Raymoure W.J., and Kuhn R.W. The serum transport of steroid hormones. Recent Prog. Horm. Res. 38 (1982) 457-510
69. Skriver K., Wikoff W.R., Patston P.A., Tausk F., Schapira M., Kaplan A.P., and Bock S.C. Substrate properties of C1 inhibitor Ma (alanine 434-glutamic acid) Genetic and structural evidence suggesting that the P12-region contains critical determinants of serine protease inhibitor/substrate status. J. Biol. Chem. 266 (1991) 9216-9221
70. Smith C.L., and Hammond G.L. An amino acid substitution in biobreeding rat corticosteroid binding globulin results in reduced steroid binding affinity. J. Biol. Chem. 266 (1991) 18555-18559
71. Smith C.L., Power S.G., and Hammond G.L. A Leu-His substitution at residue 93 in human corticosteroid binding globulin results in reduced affinity for cortisol. J. Steroid Biochem. Mol. Biol. 42 (1992) 671-676
72. Stein P.E., and Carrell R.W. What do dysfunctional serpins tell us about molecular mobility and disease?. Nat. Struct. Biol. 2 (1995) 96-113
73. Torpy D.J., Bachmann A.W., Gartside M., Grice J.E., Harris J.M., Clifton P., Easteal S., Jackson R.V., and Whitworth J.A. Association between chronic fatigue syndrome and the corticosteroid-binding globulin gene ALA SER224 polymorphism. Endocr. Res. 30 (2004) 417-429
74. Torpy D.J., Bachmann A.W., Grice J.E., Fitzgerald S.P., Phillips P.J., Whitworth J.A., and Jackson R.V. Familial corticosteroid-binding globulin deficiency due to a novel null mutation: association with fatigue and relative hypotension. J. Clin. Endocrinol. Metab. 86 (2001) 3692-3700
75. Underhill D.A., and Hammond G.L. Organization of the human corticosteroid binding globulin gene and analysis of its 5′-flanking region. Mol. Endocrinol. 3 (1989) 1448-1454
76. Van Baelen H., Brepoels R., and De Moor P. Transcortin Leuven: a variant of human corticosteroid-binding globulin with decreased cortisol-binding affinity. J. Biol. Chem. 257 (1982) 3397-3400
77. Van Baelen H., Power S.G., and Hammond G.L. Decreased cortisol-binding affinity of transcortin Leuven is associated with an amino acid substitution at residue-93. Steroids 58 (1993) 275-277
78. Westphal U. Steroid-protein interactions. Monogr. Endocrinol. 4 (1971) 1-567
79. Westphal U. Steroid-protein interactions II. Monogr. Endocrinol. 27 (1986) 1-603
80. Yamasaki M., Arii Y., Mikami B., and Hirose M. Loop-inserted and thermostabilized structure of P1-P1′ cleaved ovalbumin mutant R339T. J. Mol. Biol. 315 (2002) 113-120
81. Zhao H., Friedman R.D., and Fournier R.E. The locus control region activates serpin gene expression through recruitment of liver-specific transcription factors and RNA polymerase II. Mol. Cell. Biol. 27 (2007) 5286-5295
82. Zhou A., Wei Z., Read R.J., and Carrell R.W. Structural mechanism for the carriage and release of thyroxine in the blood. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 13321-13326
83. Zhou A., Wei Z., Stanley P.L., Read R.J., Stein P.E., and Carrell R.W. The S-to-R transition of corticosteroid-binding globulin and the mechanism of hormone release. J. Mol. Biol. 380 (2008) 244-251