Mouse recombinant protein C variants with enhanced membrane affinity and hyper-anticoagulant activity in mouse plasma

FEBS Journal

Volumn 276, Issue 22, 2009, Pages 6586-6602

  Krisinger, Michael J ^a   Guo, Li Jun ^a   Salvagno, Gian Luca ^b   Guidi, Gian Cesare ^b   Lippi, Giuseppe ^b   Dahlbäck, Björn ^a  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSITY HOSPITAL OF VERONA   (Italy)

Author keywords

Anticoagulation; Gla domain; Mouse plasma; Mouse protein C; Protein membrane interactions

Indexed keywords

ACTIVATED PROTEIN C; CALCIUM; MEMBRANE PROTEIN; PROTEIN C; RECOMBINANT PROTEIN; THROMBIN;

ANTICOAGULATION; ARTICLE; BINDING AFFINITY; BINDING ASSAY; CONTROLLED STUDY; MEMBRANE BINDING; MOUSE; MUTAGENESIS; MUTATION; NONHUMAN; PLASMA; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN VARIANT; SURFACE PLASMON RESONANCE; TITRIMETRY;

AMINO ACID SEQUENCE; ANIMALS; ANTICOAGULANTS; CATTLE; CELL MEMBRANE; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PLASMA; PROTEIN C; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 70350435294     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07371.x     Document Type: Article

References (51)

1. Fernández JA, Xu X, Liu D, Zlokovic BV Griffin JH (2003) Recombinant murine-activated protein C is neuroprotective in a murine ischemic stroke model. Blood Cells Mol Dis 30, 271 276.
2. Dahlbäck B Villoutreix BO (2005) Regulation of blood coagulation by the protein C anticoagulant pathway: novel insights into structure-function relationships and molecular recognition. Arterioscler Thromb Vasc Biol 25, 1311 1320.
3. Esmon CT (2006) Inflammation and the activated protein C anticoagulant pathway. Semin Thromb Hemost 32, 49 60.
4. Mosnier LO, Zlokovic BV Griffin JH (2007) The cytoprotective protein C pathway. Blood 109, 3161 3172.
5. Elphick GF, Sarangi PP, Hyun YM, Hollenbaugh JA, Ayala A, Biffl WL, Chung HL, Rezaie AR, McGrath JL, Topham DJ et al. (2009) Recombinant human activated protein C inhibits integrin-mediated neutrophil migration. Blood 113, 4078 4085.
6. Mesters RM, Helterbrand J, Utterback BG, Yan B, Chao YB, Fernandez JA, Griffin JH Hartman DL (2000) Prognostic value of protein C concentrations in neutropenic patients at high risk of severe septic complications. Crit Care Med 28, 2209 2216.
7. Levi M van der Poll T (2007) Recombinant human activated protein C: current insights into its mechanism of action. Crit Care 11 (Suppl 5 S3.
8. Bernard GR, Vincent JL, Laterre PF, LaRosa SP, Dhainaut JF, Lopez-Rodriguez A, Steingrub JS, Garber GE, Helterbrand JD, Ely EW et al. (2001) Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med 344, 699 709.
9. 2+ ion and membrane binding structure of the Gla domain of Ca-prothrombin fragment 1. Biochemistry 31, 2554 2566.
10. Sunnerhagen M, Forsen S, Hoffren AM, Drakenberg T, Teleman O Stenflo J (1995) Structure of the Ca(2+)-free Gla domain sheds light on membrane binding of blood coagulation proteins. Nat Struct Biol 2, 504 509.
11. Christiansen WT, Tulinsky A Castellino FJ (1994) Functions of individual gamma-carboxyglutamic acid (Gla) residues of human protein c. Determination of functionally nonessential Gla residues and correlations with their mode of binding to calcium. Biochemistry 33, 14993 15000.
12. Nelsestuen GL, Shah AM Harvey SB (2000) Vitamin K-dependent proteins. Vitam Horm 58, 355 389.
13. Freedman SJ, Furie BC, Furie B Baleja JD (1995) Structure of the calcium ion-bound gamma-carboxyglutamic acid-rich domain of factor IX. Biochemistry 34, 12126 12137.
14. Shen L, Shah AM, Dahlbäck B Nelsestuen GL (1997) Enhancing the activity of protein C by mutagenesis to improve the membrane-binding site: studies related to proline-10. Biochemistry 36, 16025 16031.
15. Shen L, Shah AM, Dahlbäck B Nelsestuen GL (1998) Enhancement of human protein C function by site-directed mutagenesis of the gamma-carboxyglutamic acid domain. J Biol Chem 273, 31086 31091.
16. Sun YH, Shen L Dahlbäck B (2003) Gla domain-mutated human protein C exhibiting enhanced anticoagulant activity and increased phospholipid binding. Blood 101, 2277 2284.
17. Smirnov MD, Safa O, Regan L, Mather T, Stearns-Kurosawa DJ, Kurosawa S, Rezaie AR, Esmon NL Esmon CT (1998) A chimeric protein C containing the prothrombin Gla domain exhibits increased anticoagulant activity and altered phospholipid specificity. J Biol Chem 273, 9031 9040.
18. Stone MD, Harvey SB, Martinez MB, Bach RR Nelsestuen GL (2005) Large enhancement of functional activity of active site-inhibited factor VIIa due to protein dimerization: insights into mechanism of assembly/disassembly from tissue factor. Biochemistry 44, 6321 6330.
19. Sun YH, Tran S, Norstrom EA Dahlbäck B (2004) Enhanced rate of cleavage at Arg-306 and Arg-506 in coagulation factor Va by Gla domain-mutated human-activated protein C. J Biol Chem 279, 47528 47535.
20. Malm K, Arnljots B, Persson IM Dahlbäck B (2007) Antithrombotic and anticoagulant effects of wild type and Gla-domain mutated human activated protein C in rats. Thromb Res 120, 531 539.
21. Malm K, Arnljots B Dahlbäck B (2008) Human activated protein C variants in a rat model of arterial thrombosis. Thromb J 6, 16.
22. Smirnov MD, Ford DA, Esmon CT Esmon NL (1999) The effect of membrane composition on the hemostatic balance. Biochemistry 38, 3591 3598.
23. Falls LA, Furie B Furie BC (2000) Role of phosphatidylethanolamine in assembly and function of the factor IXa-factor VIIIa complex on membrane surfaces. Biochemistry 39, 13216 13222.
24. Grzesiak JJ Pierschbacher MD (1995) Shifts in the concentrations of magnesium and calcium in early porcine and rat wound fluids activate the cell migratory response. J Clin Invest 95, 227 233.
25. Lansdown AB, Sampson B Rowe A (1999) Sequential changes in trace metal, metallothionein and calmodulin concentrations in healing skin wounds. J Anat 195, 375 386.
26. Tchaikovski SN, van Vlijmen BJM, Rosing J Tans G (2007) Development of a calibrated automated thrombography based thrombin generation test in mouse plasma. J Thromb Haemost 5, 2079 2086.
27. Toltl LJ, Swystun LL, Pepler L Liaw PC (2008) Protective effects of activated protein C in sepsis. Thromb Haemost 100, 582 592.
28. Dahlbäck B, Hildebrand B Malm J (1990) Characterization of functionally important domains in human vitamin K-dependent protein S using monoclonal antibodies. J Biol Chem 265, 8127 8135.
29. He X, Shen L Dahlbäck B (1995) Expression and functional characterization of chimeras between human and bovine vitamin-K-dependent protein-S-defining modules important for the species specificity of the activated protein C cofactor activity. Eur J Biochem 227, 433 440.
30. Harvey SB, Stone MD, Martinez MB Nelsestuen GL (2003) Mutagenesis of the gamma-carboxyglutamic acid domain of human factor VII to generate maximum enhancement of the membrane contact site. J Biol Chem 278, 8363 8369.
31. Preston RJ, Ajzner E, Razzari C, Karageorgi S, Dua S, Dahlbäck B Lane DA (2006) Multifunctional specificity of the protein C/activated protein C Gla domain. J Biol Chem 281, 28850 28857.
32. Harmon S, Preston RJ, Ainle FN, Johnson JA, Cunningham MS, Smith OP, White B O'Donnell JS (2008) Dissociation of activated protein C functions by elimination of protein S cofactor enhancement. J Biol Chem 283, 30531 30539.
33. Cutsforth GA, Whitaker RN, Hermans J Lentz BR (1989) A new model to describe extrinsic protein binding to phospholipid membranes of varying composition: application to human coagulation proteins. Biochemistry 28, 7453 7461.
34. Shaw AW, Pureza VS, Sligar SG Morrissey JH (2007) The local phospholipid environment modulates the activation of blood clotting. J Biol Chem 282, 6556 6563.
35. Nelsestuen GL Broderius M (1977) Interaction of prothrombin and blood-clotting factor X with membranes of varying composition. Biochemistry 16, 4172 4177.
36. Banner DW, D'Arcy A, Chène C, Winkler FK, Guha A, Konigsberg WH, Nemerson Y Kirchhofer D (1996) The crystal structure of the complex of blood coagulation factor VIIa with soluble tissue factor. Nature 380, 41 46.
37. Small DM (1967) Phase equilibria and structure of dry and hydrated egg lecithin. J Lipid Res 8, 551 557.
38. Bazzi MD Nelsestuen GL (1991) Extensive segregation of acidic phospholipids in membranes induced by protein kinase C and related proteins. Biochemistry 30, 7961 7969.
39. Christiansen WT, Jalbert LR, Robertson RM, Jhingan A, Prorok M Castellino FJ (1995) Hydrophobic amino acid residues of human anticoagulation protein C that contribute to its functional binding to phospholipid Vesicles. Biochemistry 34, 10376 10382.
40. Ohkubo YZ Tajkhorshid E (2008) Distinct structural and adhesive roles of Ca2+ in membrane binding of blood coagulation factors. Structure 16, 72 81.
41. Huang M, Rigby A, Morelli X, Grant M, Huang G, Furie B, Seaton B Furie B (2003) Structural basis of membrane binding by Gla domains of vitamin K-dependent proteins. Nat Struct Biol 10, 751 756.
42. Parkinson JF, Grinnell BW, Moore RE, Hoskins J, Vlahos CJ Bang NU (1990) Stable expression of a secretable deletion mutant of recombinant human thrombomodulin in mammalian cells. J Biol Chem 265, 12602 12610.
43. Oslakovic C, Krisinger MJ, Andersson A, Jauhiainen M, Ehnholm C Dahlbäck B (2009) Anionic phospholipids lose their procoagulant properties when incorporated into high-density lipoproteins. J Biol Chem 284, 5896 5904.
44. Brown MA, Stenberg LM, Persson U Stenflo J (2000) Identification and purification of vitamin K-dependent proteins and peptides with monoclonal antibodies specific for gamma-carboxyglutamyl (Gla) residues. J Biol Chem 275, 19795 19802.
45. Friedrich U, Pötzsch B, Preissner KT, Müller-Berghaus G Ehrlich H (1994) Calcium-dependent activation of protein C by thrombin/thrombomudulin: role of negatively charged amino acids within the activation peptide of protein C. Thromb Haemost 72, 567 572.
46. Mayer LD, Hope MJ Cullis PR (1986) Vesicles of variable sizes produced by a rapid extrusion procedure. Biochim Biophys Acta 858, 161 168.
47. Chen PS Jr., Toribara TY Warner H (1956) Microdetermination of Phosphorus. Anal Chem 28, 1756 1758.
48. McDonald JF, Evans TCJ, Emeagwali DB, Hariharan M, Allewell NM, Pusey ML, Shah AM Nelsestuen GL (1997) Ionic properties of membrane association by vitamin K-dependent proteins: the case for univalency. Biochemistry 36, 15589 15598.
49. McDonald JF, Shah AM, Schwalbe RA, Kisiel W, Dahlbäck B Nelsestuen GL (1997) Comparison of naturally occurring vitamin K-dependent proteins: correlation of amino acid sequences and membrane binding properties suggests a membrane contact site. Biochemistry 36, 5120 5127.
50. Falls LA, Furie BC, Jacobs M, Furie B Rigby AC (2001) The omega-loop region of the human prothrombin gamma-carboxyglutamic acid domain penetrates anionic phospholipid membranes. J Biol Chem 276, 23895 23902.
51. Stone MD Nelsestuen GL (2005) Efficacy of soluble phospholipids in the prothrombinase reaction. Biochemistry 44, 4037 4041.