Recombinant human factor X: High yield expression and the role of furin in proteolytic maturation in vivo and in vitro

Thrombosis Research

Volumn 97, Issue 2, 2000, Pages 51-67

  Himmelspach, Michèle ^a   Pfleiderer, Michael ^a   Fischer, Bernhard E ^a   Plaimauer, Barbara ^a   Antoine, Gerhard ^a   Falkner, Falko G ^a   Dorner, Friedrich ^a   Schlokat, Uwe ^a  

^a BAXTER INNOVATIONS GMBH   (Austria)

Author keywords

Carboxylation; Endoprotease; Factor X; Furin; Processing; Propeptide

Indexed keywords

BLOOD CLOTTING FACTOR 10; FURIN; PROTEIN; PROTEINASE; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXYLATION; CELL MATURATION; CHO CELL; CLONING; CONTROLLED STUDY; FEMALE; IMMUNOBLOTTING; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PURIFICATION;

ANIMALS; CHO CELLS; CLONING, MOLECULAR; CRICETINAE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FACTOR X; FURIN; HUMANS; MOLECULAR WEIGHT; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, QUATERNARY; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP; SUBTILISINS;

EID: 0033986592     PISSN: 00493848     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0049-3848(99)00145-0     Document Type: Article

References (59)

1. MacGillivray R.T.A., Fung M.R. Molecular biology of factor X. Baillière's Clin Haematol. 2:1989;897-917.
2. Watzke H.H., High K.A. Factor X. High K.A., Roberts H.R. Molecular basis of thrombosis and hemostasis. 1995;239-255 Marcel Dekker, New York.
3. Pryzdial E.L.G., Kessler G.E. Autoproteolysis or plasmin-mediated cleavage of factor Xaα exposes a plasminogen binding site and inhibits coagulation. J Biol Chem. 271:1996;16614-16620.
4. Leytus S.P., Chung D.W., Kisiel W., Kurachi K., Davie E.W. Characterization of a cDNA coding for human factor X. Proc Natl Acad Sci USA. 81:1984;3699-3702.
5. Messier T.L., Pittman D.D., Long G.L., Kaufman R.J., Church W.R. Cloning and expression in COS-1 cells of a full-length cDNA encoding human coagulation factor X. Gene. 99:1991;291-294.
6. Fung M.R., Hay C.W., MacGillivray R.T.A. Characterization of an almost full-length cDNA coding for human blood coagulation factor X. Proc Natl Acad Sci USA. 82:1985;3591-3595.
7. Kaul R.K., Hildebrand B., Roberts S., Jagadeeswaran P. Isolation and characterization of human blood-coagulation factor X cDNA. Gene. 41:1986;311-314.
8. Bahnak B.R., Howk R., Morrissey J.H., Ricca G.A., Edgington T.S., Jaye M.C., Drohan W.W., Fair D.S. Steady state levels of factor X mRNA in liver and HepG2 cells. Blood. 69:1987;224-230.
9. Fair D.S., Bahnak B.R. Human hepatoma cells secrete single chain factor X, prothrombin, and antithrombin III. Blood. 64:1984;194-204.
10. Watzke H.H., Wallmark A., Hamaguchi N., Giardina P., Stafford D.W., High K.A. Factor X Santo Domingo. Evidence that the severe clinical phenotype arises from a mutation blocking secretion J Clin Invest. 88:1991;1685-1689.
11. Wolf D.L., Sinha U., Hancock T.E., Lin P.-H., Messier T.L., Esmon C.T., Church W.R. Design of constructs for the expression of biologically active recombinant human factors X and Xa. J Biol Chem. 266:1991;13726-13730.
12. Mullane M.P., Eby C.S., Porche-Sorbet R.M., Miletich J.P. Deletional and processing mutations of the activation peptide of human factor X. Blood. 80:1992;1215.
13. Rudolph A.E., Mullane M.P., Porche-Sorbet R., Miletich J.P. Expression, purification, and characterization of recombinant human factor X. Protein Expr Purif. 10:1997;373-378.
14. Grinell B.W., Walls J.D., Gerlitz B., Berg D.T., McClure D.B., Ehrlich H., Bang N.U., Yan S.B. Native and modified recombinant protein C. Function, secretion, and post-translational modifications Adv Appl Biotechnol Ser. 11:1990;30-63.
15. Van de Ven W.J.M., Roebroek A.J.M., Van Duijnhoven H.L.P. Structure and function of eucaryotic proprotein processing enzymes of the subtilisin family of serine proteases. Crit Rev Oncogenesis. 4:1993;115-136.
16. Rehemtulla A., Kaufman R.J. Preferred sequence requirements for cleavage of pro-von Willebrand factor by propeptide-processing enzymes. Blood. 79:1992;2349-2355.
17. Wasley L.C., Rehemtulla A., Bristol J.A., Kaufman R.J. PACE/Furin can process the vitamin K-dependent pro-factor IX precursor within the secretory pathway. J Biol Chem. 268:1993;8458-8465.
18. Bristol J.A., Freedman S.J., Furie B.C., Furie B. Profactor IX. The propeptide inhibits binding to membrane surfaces and activation by factor XIa Biochemistry. 33:1994;14136-14143.
19. Drews R., Paleyanda R.K., Lee T.K., Chang R.R., Rehemtulla A., Kaufman R.J., Drohan W.N., Lubon H. Proteolytic maturation of protein C upon engineering the mouse mammary gland to express furin. Proc Natl Acad Sci USA. 92:1995;10462-10466.
20. Schlokat U., Fischer B.E., Herlitschka S., Antoine G., Preininger A., Mohr G., Himmelspach M., Kistner O., Falkner F.G., Dorner F. Production of highly homogeneous and structurally intact recombinant von Willebrand factor multimers by furin-mediated propeptide removal in vitro. Biotech Appl Biochem. 24:1996;257-267.
21. Fischer B.E., Schlokat U., Mitterer A., Reiter M., Mundt W., Turecek P.L., Schwarz H.P., Dorner F. Structural analysis of recombinant von Willebrand factor produced at industrial scale fermentation of transformed CHO cells co-expressing recombinant furin. FEBS Lett. 375:1995;259-262.
22. Kaufman R.J., Wasley L.C., Furie B.C., Furie B., Shoemaker C.B. Expression, purification, and characterization of recombinant γ-carboxylated factor IX synthesized in Chinese hamster ovary cells. J Biol Chem. 261:1986;9622-9628.
23. Davis L.G., Dibner M.D., Battey J.F. Molecular Biology. 1986;Elsevier Publishers, New York-Amsterdam-London.
24. Moss B., Elroy-Stein O., Mizukami T., Alexander T., Fuerst T.R. Product review. New mammalian expression vectors Nature. 348:1990;91-92.
25. Pfleiderer M., Falkner F.G., Dorner F. Requirements for optimal expression of secreted and non-secreted recombinant proteins in vaccinia virus systems. Protein Expr Purif. 6:1995;559-569.
26. Fischer B., Mitterer A., Schlokat U., DenBouwmeester R., Dorner F. Structural analysis of recombinant von Willebrand factor. Identification of hetero- and homodimers FEBS Lett. 351:1994;345-348.
27. Preininger A., Schlokat U., Mohr G., Himmelspach M., Stichler V., Kyd-Rebenburg A., Plaimauer B., Turecek P.L., Schwarz H.P., Wernhart W., Fischer B., Dorner F. Strategies for recombinant furin employment in a biotechnological process. Complete target protein precursor cleavage Cytotechnology. 30:1999;1-16.
28. Urlaub G., Chasin L.A. Isolation of Chinese hamster cell mutants deficient in dihydrofolate reductase activity. Proc Natl Acad Sci USA. 77:1980;4216-4220.
29. Gordon V.M., Klimpel K.R., Arora N., Henderson M.A., Leppla S.H. Proteolytic activation of bacterial toxins by eucaryotic cells is performed by furin and by additional cellular proteases. Infect Immunol. 63:1995;82-87.
30. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
31. Fischer B., Mitterer A., Dorner F. Purification of recombinant human coagulation factor II and factor IX and protein S expressed in recombinant vaccinia virus infected Vero cells. J Biotechnol. 38:1995;129-136.
32. Fischer B.E., Schlokat U., Mitterer A., Grillberger L., Reiter M., Mundt W., Dorner F., Eibl J. Differentiation between proteolytic activation and autocatalytic conversion of human prothrombin. Activation of recombinant human prothrombin and recombinant D419N-prothrombin by snake venoms from Echis carinatus and Oxyuranus scutellatus. Prot Eng. 9:1996;921-926.
33. Van Wijk E.M., Kahlé L.H., ten Cate J.W. A rapid manual chromogenic factor X assay. Thromb Res. 22:1981;681-686.
34. Erskine J.G., Walker I.D., Davidson J.F. Maintenance control of oral anticoagulant therapy by a chromogenic substrate assay for factor X. J Clin Pathol. 33:1980;445-448.
35. Ciavarella N., Coccheri S., Gensini G.F., Hassan H.J., Mannucci P.M., Manotti C., Margstakler E., Mariani G., Orlando M., Palareti G., Petronelli M., Pogliani E., Ponari O., Prisco D., Recalcati P., Rossi E., Salvitti E., Tripodi A. Multicenter evaluation of a new chromogenic factor X assay in plasma of patients on oral anticoagulants. Thromb Res. 19:1980;493-502.
36. Seidah N.G., Chrétien M., Day R. The family of subtilisin/kexin like pro-protein and pro-hormone convertases. Divergent or shared functions Biochimie. 76:1994;197-209.
37. Creemers J.W.M., Kormelink P.J.G., Roebroek A.J.M., Nakayama K., Van de Ven W.J.M. Proprotein processing activity and cleavage site selectivity of the Kex2-like endoprotease PACE4. FEBS Lett. 336:1993;65-69.
38. Brakch N., Galanopoulou A.S., Patel Y.C., Boileau G., Seidah N.G. Comparative proteolytic processing of rat prosomatostatin by the convertases PC1, PC2, furin, PACE4 and PC5 in constitutive and regulated secretory pathways. FEBS Lett. 362:1995;143-146.
39. Jorgensen M.J., Cantor A.B., Furie B.C., Furie B. Expression of completely γ-carboxylated recombinant human prothrombin. J Biol Chem. 262:1987;6729-6734.
40. Graves C.B., Munns T.W., Willingham A.K., Strauss A.W. Rat factor X is synthesized as a single chain precursor inducible by prothrombin fragments. J Biol Chem. 257:1982;13108-13113.
41. Willingham A.K., Matschiner J.T. Functional characterization of single-chain factor X from rat liver. Arch Biochem Biophys. 230:1984;543-552.
42. Vey M., Schaefer W., Berghoefer S., Klenk H.D., Garten W. Maturation of the trans-Golgi network protease furin. Compartmentalization of propeptide removal, substrate cleavage, and COOH-terminal truncation J Cell Biol. 127:1994;1829-1842.
43. Turecek P.L., Pichler L., Auer W., Eder G., Varadi K., Mitterer A., Mundt W., Schlokat U., Dorner F., Drouet L., Roussi J., van Mourik J.A., Schwarz H.P. Evidence for extracellular processing of pro-von Willebrand factor after infusion in animals with and without severe von Willebrand disease. Blood. 94:1999;1637-1647.
44. Takahashi S., Hatsuzawa K., Watanabe T., Murakami K., Nakayama K. Sequence requirements for endoproteolytic processing of precursor proteins by furin. Transfection and in vitro experiments. J Biochem. 116:1994;47-52.
45. Stanton C., Ross R.P., Hutson S., Wallin R. Processing and expression of rat and human clotting factor-X-encoding cDNAs. Gene. 169:1996;269-273.
46. Rehemtulla A., Kaufman R.J. Protein processing within the secretory pathway. Curr Opin Biotech. 3:1992;560-565.
47. Wallin R., Stanton C., Ross R.P. Intracellular proteolytic processing of the two-chain vitamin K-dependent coagulation factor X. Thromb Res. 73:1994;395-403.
48. Steiner D.F., Smeekens S.P., Ohagi S., Chan S.J. The new enzymology of precursor processing endoproteases. J Biol Chem. 267:1992;23435-23438.
49. Rodríguez P.L., Carrasco L. Improved factor Xa cleavage of fusion proteins containing maltose binding protein. BioTechniques. 18:1995;238-243.
50. Wallin R., Stanton C., Hutson S.M. Intracellular maturation of the γ-carboxyglutamic acid (gla) region in prothrombin coincides with release of the propeptide. Biochem J. 291:1993;723-727.
51. Larson P.J., Camire R.M., Wong D., Fasano N.C., Monroe D.M., Tracy P.B., High K. Structure/function analyses of recombinant variants of human factor Xa. Factor Xa incorporation into prothrombinase on the thrombin-activated platelet surface is not mimicked by synthetic phospholipid vesicles Biochemistry. 37:1998;5029-5038.
52. Morris D.P., Stevens R.D., Wright D.J., Stafford D.W. Processive post-translational modification. J Biol Chem. 270:1995;30491-30498.
53. Bristol J.A., Ratcliffe J.V., Roth D.A., Jacobs M.A., Furie B.C., Furie B. Biosynthesis of prothrombin. Intracellular localization of the vitamin K-dependent carboxylase and the sites of γ-carboxylation Blood. 88:1996;2585-2593.
54. Stanton C., Wallin R. Processing and trafficking of clotting factor X in the secretory pathway. Biochem J. 284:1992;25-31.
55. Beardell F.V., Varma M., Martinez J. Normalization of plasma factor X levels in amyloidosis after plasma exchange. Am J Hematol. 54:1997;68-71.
56. Gallais V., Bredoux H., le Roux G., Laroche L. Acquired and transient factor X deficiency associated with sodium valproate treatment. Eur J Haematol. 57:1996;330.
57. Giles A.R., Mann K.G., Nesheim M.E. A combination of factor Xa and phosphatidylcholine-phosphatidylserine vesicles bypasses factor VIII in vivo. Br J Haematol. 69:1988;491-497.
58. Turecek P.L., Gritsch H., Richter G., Pichler L., Auer W., Schwarz H.P. A complex of prothrombin and activated factor X. A two-component therapeutic for the treatment of coagulopathies particularly hemophilia with inhibitor Ann Hematol. 74(Suppl II):1997;210.
59. Herlitschka S., Falkner F.G., Schlokat U., Dorner F. Overexpression of human prothrombin in permanent cell lines using a dominant selection/amplification fusion marker. Protein Expr Purif. 8:1996;358-364.