Understanding the functional difference between growth arrest-specific protein 6 and protein S: An evolutionary approach

Open Biology

Volumn 4, Issue 10, 2014, Pages

  Studer, Romain A ^a   Opperdoes, Fred R ^b   Nicolaes, Gerry A F ^c   Mulder, André B ^d   Mulder, René ^d  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^c MAASTRICHT UNIVERSITY   (Netherlands)

^d UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Evolution; Growth arrest specific protein 6; Protein S

Indexed keywords

VERTEBRATA;

AMINO ACID; GROWTH ARREST-SPECIFIC PROTEIN 6; PLASMA PROTEIN; PROS1 PROTEIN, HUMAN; PROTEIN BINDING; SIGNAL PEPTIDE;

ALGORITHM; ANIMAL; BINDING SITE; BIOLOGY; CHEMISTRY; CIONA INTESTINALIS; GLYCOSYLATION; HUMAN; METABOLISM; MOLECULAR EVOLUTION; MUTATION; PHENOTYPE; PHYLOGENY; PROTEIN ANALYSIS; PROTEIN DATABASE; PROTEIN PROCESSING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STATIC ELECTRICITY;

ALGORITHMS; AMINO ACIDS; ANIMALS; BINDING SITES; BLOOD PROTEINS; CIONA INTESTINALIS; COMPUTATIONAL BIOLOGY; DATABASES, PROTEIN; EVOLUTION, MOLECULAR; GLYCOSYLATION; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MUTATION; PHENOTYPE; PHYLOGENY; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STATIC ELECTRICITY;

EID: 84923658690     PISSN: None     EISSN: 20462441     Source Type: Journal    
DOI: 10.1098/rsob.140121     Document Type: Article

References (75)

1. Manfioletti G, Brancolini C, Avanzi G, Schneider C. 1993 The protein encoded by a growth arrestspecific gene (gas6) is a new member of the vitamin K-dependent proteins related to protein S, a negative coregulator in the blood coagulation cascade. Mol. Cell Biol. 13, 4976-4985.
2. Hafizi S, Dahlbä ck B. 2006 Gas6 and protein S. Vitamin K-dependent ligands for the Axl receptor tyrosine kinase subfamily. FEBS J. 273, 5231-5244. (doi:10.1111/j.1742-4658.2006.05529.x)
3. Walker FJ, Chavin SI, Fay PJ. 1987 Inactivation of factor VIII by activated protein C and protein S. Arch. Biochem. Biophys. 252, 322-328. (doi:10. 1016/0003-9861(87)90037-3)
4. Walker FJ. 1980 Regulation of activated protein C by a new protein. A possible function for bovine protein S. J. Biol. Chem. 255, 5521-5524.
5. Hackeng TM, Seré KM, Tans G, Rosing J. 2006 Protein S stimulates inhibition of the tissue factor pathway by tissue factor pathway inhibitor. Proc. Natl Acad. Sci. USA 103, 3106-3111. (doi:10.1073/ pnas.0504240103)
6. Robins RS, Lemarié CA, Laurance S, Aghourian MN, Wu J, Blostein MD. 2013 Vascular Gas6 contributes to thrombogenesis and promotes tissue factor upregulation after vessel injury in mice. Blood 121, 692-699. (doi:10.1182/blood-2012-05-433730)
7. Lijfering WM, Mulder R, ten Kate MK, Veeger NJ, Mulder AB, van der Meer J. 2009 Clinical relevance of decreased free protein S levels: results from a retrospective family cohort study involving 1143 relatives. Blood 113, 1225-1230. (doi:10.1182/ blood-2008-08-174128)
8. Brouwer JL, Bijl M, Veeger NJ, Kluin-Nelemans HC, van der Meer J. 2004 The contribution of inherited and acquired thrombophilic defects, alone or combined with antiphospholipid antibodies, to venous and arterial thromboembolism in patients with systemic lupus erythematosus. Blood 104, 143-148. (doi:10.1182/blood-2003-11-4085)
9. Wu CS, Hu CY, Tsai HF, Chyuan IT, Chan CJ, Chang SK, Hsu PN. 2014 Elevated serum level of growth arrest-specific protein 6 (Gas6) in systemic lupus erythematosus patients is associated with nephritis and cutaneous vasculitis. Rheumatol. Int. 34, 625-629. (doi:10.1007/s00296-013-2882-1)
10. Lee IJ et al. 2012 Growth arrest-specific gene 6 (Gas6) levels are elevated in patients with chronic renal failure. Nephrol. Dial. Transplant. 27, 4166-4172. (doi:10.1093/ndt/gfs337)
11. Vigano-D'Angelo S, D'Angelo A, Kaufman Jr CE, Sholer C, Esmon CT, Comp PC. 1987 Protein S deficiency occurs in the nephrotic syndrome. Ann. Intern. Med. 107, 42-47. (doi:10.7326/0003-4819-107-1-42)
12. Borgel D, Clauser S, Bornstain C, Biè che I, Bissery A, Remones V, Fagon JY, Aiach M, Diehl JL. 2006 Elevated growth-arrest-specific protein 6 plasma levels in patients with severe sepsis. Crit. Care Med. 34, 219-222. (doi:10.1097/01.CCM.0000195014. 56254.8A)
13. Kinasewitz GT et al. 2004 Universal changes in biomarkers of coagulation and inflammation occur in patients with severe sepsis, regardless of causative micro-organism [ISRCTN74215569]. Crit. Care 8, R82-R90. (doi:10.1186/cc2459)
14. Loges S et al. 2010 Malignant cells fuel tumor growth by educating infiltrating leukocytes to produce the mitogen Gas6. Blood 115, 2264-2273. (doi:10.1182/blood-2009-06-228684)
15. Yigit E, Gö nüllü G, Yücel I, Turgut M, Erdem D, Cakar B. 2008 Relation between hemostatic parameters and prognostic/predictive factors in breast cancer. Eur. J. Intern. Med. 19, 602-607. (doi:10.1016/j.ejim.2007.06.036)
16. Said JM, Ignjatovic V, Monagle PT, Walker SP, Higgins JR, Brennecke SP. 2010 Altered reference ranges for protein C and protein S during early pregnancy: Implications for the diagnosis of protein C and protein S deficiency during pregnancy. Thromb. Haemost. 103, 984-988. (doi:10.1160/ TH09-07-0476)
17. Mulder R, Tichelaar YI, Sprenger HG, Mulder AB, Lijfering WM. 2011 Relationship between cytomegalovirus infection and procoagulant changes in human immunodeficiency virus-infected patients. Clin. Microbiol. Infect. 17, 747-749. (doi:10.1111/j.1469-0691.2010.03415.x)
18. Tans G, Curvers J, Middeldorp S, Thomassen MC, Meijers JC, Prins MH, Bouma BN, Büller HR, Rosing J. 2000 A randomized cross-over study on the effects of levonorgestrel- and desogestrel-containing oral contraceptives on the anticoagulant pathways. Thromb. Haemost. 84, 15-21.
19. Balogh I, Hafizi S, Stenhoff J, Hansson K, Dahlbä ck B. 2005 Analysis of Gas6 in human platelets and plasma. Arterioscler. Thromb. Vasc. Biol. 25, 1280-1286. (doi:10.1161/01.ATV.0000163845.07146.48)
20. Griffin JH, Gruber A, Ferná ndez JA. 1992 Reevaluation of total, free, and bound protein S and C4b-binding protein levels in plasma anticoagulated with citrate or hirudin. Blood 79, 3203-3211.
21. Stafford DW. 2005 The vitamin K cycle. J. Thromb. Haemost. 3, 1873-1878. (doi:10.1111/j.1538-7836. 2005.01419.x)
22. Sasaki T, Knyazev PG, Clout NJ, Cheburkin Y, Gö hring W, Ullrich A, Timpl R, Hohenester E. 2006 Structural basis for Gas6-Axl signalling. EMBO J. 25, 80-87. (doi:10.1038/sj.emboj.7600912)
23. Ferná ndez JA, Heeb MJ, Griffin JH. 1993 Identification of residues 413-433 of plasma protein S as essential for binding to C4b-binding protein. J. Biol. Chem. 268, 16 788-16 794.
24. Ferná ndez JA, Griffin JH, Chang GT, Stam J, Reitsma PH, Bertina RM, Bouma BN. 1998 Involvement of amino acid residues 423-429 of human protein S in binding to C4b-binding protein. Blood Cells Mol. Dis. 24, 101-112. (doi:10.1006/bcmd.1998.0175)
25. Linse S, Hä rdig Y, Schultz DA, Dahlbä ck B. 1997 A region of vitamin K-dependent protein S that binds to C4b binding protein (C4BP) identified using bacteriophage peptide display libraries. J. Biol. Chem. 272, 14 658-14 665. (doi:10.1074/jbc.272. 23.14658)
26. Giri TK, Linse S, García de Frutos P, Yamazaki T, Villoutreix BO, Dahlbä ck B. 2002 Structural requirements of anticoagulant protein S for its binding to the complement regulator C4b-binding protein. J. Biol. Chem. 277, 15 099-15 106. (doi:10.1074/jbc.M103036200)
27. Nelson RM, Long GL. 1992 Binding of protein S to C4b-binding protein: mutagenesis of protein S. J. Biol. Chem. 267, 8140-8145.
28. Saposnik B, Borgel D, Aiach M, Gandrille S. 2003 Functional properties of the sex-hormone-binding globulin (SHBG)-like domain of the anticoagulant protein S. Eur. J. Biochem. 270, 545-555. (doi:10. 1046/j.1432-1033.2003.03423.x)
29. Walker FJ. 1989 Characterization of a synthetic peptide that inhibits the interaction between protein S and C4b-binding protein. J. Biol. Chem. 264, 17 645-17 648.
30. Evenä s P, García De Frutos P, Linse S, Dahlbä ck B. 1999 Both G-type domains of protein S are required for the high-affinity interaction with C4b-binding protein. Eur. J. Biochem. 266, 935-942. (doi:10. 1046/j.1432-1327.1999.00928.x)
31. Chang GT, Ploos van Amstel HK, Hessing M, Reitsma PH, Bertina RM, Bouma BN. 1992 Expression and characterization of recombinant human protein S in heterologous cells-studies of the interaction of amino acid residues leu-608 to glu-612 with human C4b-binding protein. Thromb. Haemost. 67, 526-532.
32. Chang GT, Maas BH, Ploos van Amstel HK, Reitsma PH, Bertina RM, Bouma BN. 1994 Studies of the interaction between human protein S and human C4b-binding protein using deletion variants of recombinant human protein S. Thromb. Haemost. 71, 461-467.
33. Evenä s P, García de Frutos P, Nicolaes GA, Dahlbä ck B. 2000 The second laminin G-type domain of protein S is indispensable for expression of full cofactor activity in activated protein C-catalysed inactivation of factor Va and factor VIIIa. Thromb. Haemost. 84, 271-277.
34. Nyberg P, Dahlbä ck B, García de Frutos P. 1998 The SHBG-like region of protein S is crucial for factor V-dependent APC-cofactor function. FEBS Lett. 433, 28-32. (doi:10.1016/S0014-5793(98)00877-1)
35. Heeb MJ, Kojima Y, Rosing J, Tans G, Griffin JH. 1999 C-terminal residues 621-635 of protein S are essential for binding to factor Va. J. Biol. Chem. 274, 36 187-36 192. (doi:10.1074/jbc. 274.51.36187)
36. Regliń ska-Matveyev N, Andersson HM, Rezende SM, Dahlbäck B, Crawley JT, Lane DA, Ahnström J. 2014 TFPI cofactor function of protein S: essential role of rsob.royalsocietypublishing.org Open Biol. 4: 140121 the protein S SHBG-like domain. Blood 123, 3979-3987. (doi:10.1182/blood-2014-01-551812)
37. Ahnströ m J et al. 2011 Activated protein C cofactor function of protein S: a novel role for a g-carboxyglutamic acid residue. Blood 117, 6685-6693. (doi:10.1182/blood-2010-11-317099)
38. Ferná ndez JA, Villoutreix BO, Hackeng TM, Griffin JH, Bouma BN. 1994 Analysis of protein S C4bbinding protein interactions by homology modeling and inhibitory antibodies. Biochemistry 33, 11 073-11 078. (doi:10.1021/bi00203a003)
39. Ferná ndez JA, Griffin JH. 1994 A protein S binding site on C4b-binding protein involves beta chain residues 31-45. J. Biol. Chem. 269, 2535-2540.
40. Villoutreix BO, Ferná ndez JA, Teleman O, Griffin JH. 1995 Comparative modeling of the three CP modules of the beta-chain of C4BP and evaluation of potential sites of interaction with protein S. Protein Eng. 8, 1253-1258. (doi:10.1093/protein/8. 12.1253)
41. Hä rdig Y, Dahlbä ck B. 1996 The amino-terminal module of the C4b-binding protein beta-chain contains the protein S-binding site. J. Biol. Chem. 271, 20 861-20 867. (doi:10.1074/jbc.271. 34.20861)
42. van de Poel RH, Meijers JC, Bouma BN. 1999 Interaction between protein S and complement C4b-binding protein (C4BP): affinity studies using chimeras containing c4 bp beta-chain short consensus repeats. J. Biol. Chem. 274, 15 144-15 150. (doi:10.1074/jbc.274.21.15144)
43. van de Poel RH, Meijers JC, Dahlbä ck B, Bouma BN. 1999 C4b-binding protein (C4BP) beta-chain Short Consensus Repeat-2 specifically contributes to the interaction of C4BP with protein S. Blood Cells Mol. Dis. 25, 279-286. (doi:10.1006/bcmd.1999.0255)
44. Webb JH, Villoutreix BO, Dahlbä ck B, Blom AM 2003 Role of CCP2 of the C4b-binding protein betachain in protein S binding evaluated by mutagenesis and monoclonal antibodies. Eur. J. Biochem. 270, 93-100. (doi:10.1046/j.1432-1033.2003.03365.x)
45. Studer RA, Robinson-Rechavi M. 2009 How confident can we be that orthologs are similar, but paralogs differ? Trends Genet. 25, 210-216. (doi:10.1016/j.tig.2009.03.004)
46. Gabaldó n T, Koonin EV. 2013 Functional and evolutionary implications of gene orthology. Nat. Rev. Genet. 14, 360-366. (doi:10.1038/nrg3456)
47. Zhang J. 2003 Evolution by gene duplication: an update. Trends Ecol. Evol. 18, 292-298. (doi:10. 1016/S0169-5347(03)00033-8)
48. Studer RA, Robinson-Rechavi M. 2009 Evidence for an episodic model of protein sequence evolution. Biochem. Soc. Trans. 37, 783-786. (doi:10.1042/ BST0370783)
49. Gu X. 2003 Functional divergence in protein (family) sequence evolution. Genetica 118, 133-141. (doi:10.1007/978-94-010-0229-5-4)
50. Studer RA, Dessailly BH, Orengo CA. 2013 Residue mutations and their impact on protein structure and function: detecting beneficial and pathogenic changes. Biochem. J. 449, 581-594. (doi:10.1042/ BJ20121221)
51. Cacan E, Kratzer JT, Cole MF, Gaucher EA. 2013 Interchanging functionality among homologous elongation factors using signatures of heterotachy. J. Mol. Evol. 76, 4-12. (doi:10.1007/s00239-013-9540-9)
52. Katoh K, Standley DM. 2013 MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780. (doi:10.1093/ molbev/mst010)
53. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. 2009 Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191. (doi:10.1093/ bioinformatics/btp033)
54. Guindon S, Gascuel O. 2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704. (doi:10.1080/10635150390235520)
55. Huelsenbeck JP, Ronquist F. 2001 MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754-755. (doi:10.1093/ bioinformatics/17.8.754)
56. Hedges SB, Dudley J, Kumar S. 2006 TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22, 2971-2972. (doi:10.1093/bioinformatics/btl505)
57. Edwards RJ, Shields DC. 2005 BADASP: predicting functional specificity in protein families using ancestral sequences. Bioinformatics 21, 4190-4191. (doi:10.1093/bioinformatics/bti678)
58. Studer RA, Robinson-Rechavi M. 2010 Large-scale analysis of orthologs and paralogs under covarionlike and constant-but-different models of amino acid evolution. Mol. Biol. Evol. 27, 2618-2627. (doi:10.1093/molbev/msq149)
59. Gaston D, Susko E, Roger AJ. 2011 A phylogenetic mixture model for the identification of functionally divergent protein residues. Bioinformatics 27, 2655-2663. (doi:10.1093/bioinformatics/btr470)
60. Zhang J, Nielsen R, Yang Z. 2005 Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol. Biol. Evol. 22, 2472-2479. (doi:10.1093/ molbev/msi237)
61. Yang Z. 2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591. (doi:10.1093/molbev/msm088)
62. Moretti S et al. 2014 Selectome update: quality control and computational improvements to a database of positive selection. Nucleic Acids Res. 42, D917-D921. (doi:10.1093/nar/gkt1065)
63. Proux E, Studer RA, Moretti S, Robinson-Rechavi M. 2009 Selectome: a database of positive selection. Nucleic Acids Res. 37, D404-D407. (doi:10.1093/ nar/gkn768)
64. Schymkowitz J, Borg J, Stricher F, Nys R, Rousseau F, Serrano L. 2005 The FoldX web server: an online force field. Nucleic Acids Res. 33, W382-W388. (doi:10.1093/nar/gki387)
65. Sali A, Blundell TL. 1993 Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815. (doi:10.1006/jmbi.1993.1626)
66. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. 2001 Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl Acad. Sci. USA 98, 10 037-10 041. (doi:10.1073/pnas. 181342398)
67. Schrö dinger. 2010 The PyMOL molecular graphics system, version 1.3r1. See http://www.pymol.org.
68. Fernandez-Recio J, Totrov M, Skorodumov C, Abagyan R. 2005 Optimal docking area: a new method for predicting protein-protein interaction sites. Proteins 58, 134-143. (doi:10.1002/ prot.20285)
69. Ohno S. 1970 Evolution by gene duplication. London, UK: George Allen & Unwin.
70. Panopoulou G, Poustka AJ. 2005 Timing and mechanism of ancient vertebrate genome duplications-the adventure of a hypothesis. Trends Genet. 21, 559-567. (doi:10.1016/j.tig.2005.08.004)
71. DePristo MA, Weinreich DM, Hartl DL. 2005 Missense meanderings in sequence space: a biophysical view of protein evolution. Nat. Rev. Genet. 6, 678-687. (doi:10.1038/nrg1672)
72. Tokuriki N, Stricher F, Serrano L, Tawfik DS. 2008 How protein stability and new functions trade off. PLoS Comput. Biol. 4, e1000002. (doi:10.1371/ journal.pcbi.1000002)
73. Studer RA, Christin PA, Williams MA, Orengo CA.2014 Stability-activity tradeoffs constrain the adaptive evolution of RubisCO. Proc. Natl Acad. Sci. USA 111, 2223-2228. (doi:10.1073/pnas. 1310811111)
74. Dasmeh P, Serohijos AW, Kepp KP, Shakhnovich EI.2013 Positively selected sites in cetacean myoglobins contribute to protein stability. PLoS Comput. Biol. 9, e1002929. (doi:10.1371/journal. pcbi.1002929)
75. den Dunnen JT, Antonarakis SE. 2000 Mutation nomenclature extensions and suggestions to describe complex mutations: a discussion. Hum. Mutat. 15, 7-12. (doi:10.1002/(SICI)1098-1004(200001)15:1, 7::AID-HUMU4 . 3.0.CO;2-N)