Blood Clotting Factor VIII: From Evolution to Therapy

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Abstract


Recombinant blood clotting factor VIII is one of the most complex proteins for industrial manufacturing due to the low efficiency of its gene transcription, massive intracellular loss of its proprotein during post-translational processing, and the instability of the secreted protein. Improvement in hemophilia A therapy requires a steady increase in the production of factor VIII drugs despite tightening standards of product quality and viral safety. More efficient systems for heterologous expression of factor VIII can be created on the basis of the discovered properties of its gene transcription, post-translational processing, and behavior in the bloodstream. The present review describes the deletion variants of factor VIII protein with increased secretion efficiency and the prospects for the pharmaceutical development of longer acting variants and derivatives of factor VIII.


N. A. Orlova

Center “Bioengineering”, Russian Academy of Sciences; Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences

Email: ptichman@gmail.com

Russian Federation

S. V. Kovnir

Center “Bioengineering”, Russian Academy of Sciences; Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences

Email: ptichman@gmail.com

Russian Federation

I. I. Vorobiev

Center “Bioengineering”, Russian Academy of Sciences; Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences

Author for correspondence.
Email: ptichman@gmail.com

Russian Federation

A. G. Gabibov

Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences

Email: ptichman@gmail.com

Russian Federation

A. I. Vorobiev

Research Center for Hematology, Ministry of Health and Social Development of the Russian Federation

Email: ptichman@gmail.com

Russian Federation

  1. Antonarakis S.E., Kazazian H.H., Tuddenham E.G. // Hum. Mutat. 1995, V.5, №1, P.1-22
  2. Kemball-Cook G., Haemophilia A. // A Mutation Database // University College London 1994
  3. Payne A.B., Miller C.H., Kelly F.M., Michael Soucie J., Craig Hooper W. // Hum. Mutat. 2013, V.34, №2, P.2382-2391
  4. Blumel J., Schmidt I., Effenberger W., Seitz H., Willkommen H., Brackmann H.H., Lower J., Eis-Hubinger A.M. // Transfusion 2002, V.42, №11, P.1473-1481
  5. Yokozaki S., Fukuda Y., Nakano I., Katano Y., Toyoda H., Takamatsu J. // Blood 1999, V.94, №10, P.3617
  6. Evatt B.L. // Haemophilia 1998, V.4, №4, P.628-633
  7. Brooks A.R., Harkins R.N., Wang P., Qian H.S., Liu P., Rubanyi G.M. // The Journal of Gene Medicine 2004, V.6, №4, P.395-404
  8. Kim M., O’Callaghan P.M., Droms K.A., James D.C. // Biotechnol. Bioengin. 2011, V.108, №10, P.2434-2446
  9. Sabatino D.E., Nichols T.C., Merricks E., Bellinger D.A., Herzog R.W., Monahan P.E. // Prog. Mol. Biol. Transl. Sci. 2012, V.105, P.151-209
  10. Gitschier J., Wood W.I., Goralka T.M., Wion K.L., Chen E.Y., Eaton D.H., Vehar G.A., Capon D.J., Lawn R.M. // Nature 1984, V.312, №5992, P.326-330
  11. Toole J.J., Knopf J.L., Wozney J.M., Sultzman L.A., Buecker J.L., Pittman D.D., Kaufman R.J., Brown E., Shoemaker C., Orr E.C. // Nature 1984, V.312, №5992, P.342-347
  12. Cho M.S., Tran V.M. // Virology 1993, V.94, №2, P.838-842
  13. Dunne M.J., Kane C., Shepherd R.M., Sanchez J.A., James R.F., Johnson P.R., Aynsley-Green A., Lu S., Clement J.P. // N. Engl. J. Med. 1997, V.336, №10, P.73-706
  14. Stel H.V., van der Kwast T.H., Veerman E.C. // Nature 1983, V.303, №5917, P.530-532
  15. Do H., Healey J.F., Waller E.K., Lollar P. // J. Biol. Chem. 1999, V.274, №28, P.19587-19592
  16. Hollestelle M.J., Thinnes T., Crain K., Stiko A., Kruijt J.K., van Berkel T.J., Loskutoff D.J., van Mourik J.A. // Thromb. Haemost 2001, V.86, №3, P.855-861
  17. Vehar G.A., Keyt B., Eaton D., Rodriguez H., O’Brien D.P., Rotblat F., Oppermann H., Keck R., Wood W.I., Harkins R.N. // Nature 1984, V.312, №5992, P.337-342
  18. Wood W.I., Capon D.J., Simonsen C.C., Eaton D.L., Gitschier J., Keyt B., Seeburg P.H., Smith D.H., Hollingshead P., Wion K.L. // Nature 1984, V.312, №5992, P.330-337
  19. Kjalke M., Heding A., Talbo G., Persson E., Thomsen J., Ezban M. // Eur. J. Biochem 1995, V.234, №3, P.773-779
  20. Donath M.J., Lenting P.J., van Mourik J.A., Mertens K. // Eur. J. Biochem 1996, V.240, №2, P.365-372
  21. Colman R.W. // Hemostasis аnd Thrombosis: Basic Principles аnd Clinical Practice. // Baltimore:Lippincott Williams & Wilkins. 2012, P.1578
  22. Lenting P.J., van Mourik J.A., Mertens K. // Blood. 1998, V.92, №11, P.3983-3996
  23. Andrew P.J., Auer M., Lindley I.J., Kauffmann H.F., Kungl A.J. // FEBS Lett. 1997, V.408, №3, P.319-323
  24. Pemberton S., Lindley P., Zaitsev V., Card G., Tuddenham E.G., Kemball-Cook G. // Blood. 1997, V.89, №7, P.2413-2421
  25. McCune J.S., Liles D., Lindley C. // Pharmacotherapy. 1997, V.17, №4, P.822-826
  26. Garrigues C., Loubiere P., Lindley N.D., Cocaign-Bousquet M. // Journal of Bacteriology 1997, V.179, №17, P.5282-5287
  27. Harvey M.J., Cauvin A., Dale M., Lindley S., Ballabio R. // J. Small Anim. Pract. 1997, V.38, №8, P.336-339
  28. Molinari M., Calanca V., Galli C., Lucca P., Paganetti P. // Science 2003, V.299, №5611, P.1397-1400
  29. Liu M. L., Shen B.W., Nakaya S., Pratt K.P., Fujikawa K., Davie E.W., Stoddard B.L., Thompson A.R. // Blood 2000, V.96, №3, P.979-987
  30. Larocca D., Peterson J.A., Urrea R., Kuniyoshi J., Bistrain A.M., Ceriani R.L. // Cancer Research 1991, V.51, №18, P.1994-4998
  31. Lin L., Huai Q., Huang M., Furie B., Furie B.C. // J. Mol. Biol. 2007, V.371, №3, P.717-724
  32. Johnson J.D., Edman J.C., Rutter W.J. // Proc. Natl. Acad. Sci. USA. 1993, V.90, №12, P.5677-5681
  33. Stubbs J.D., Lekutis C., Singer K. L., Bui A., Yuzuki D., Srinivasan U., Parry G. // Proc. Natl. Acad. Sci. USA. 1990, V.87, №21, P.8417-8421
  34. Shima M., Scandella D., Yoshioka A., Nakai H., Tanaka I., Kamisue S., Terada S., Fukui H. // Thromb. Haemost. 1993, V.69, №3, P.240-246
  35. Elder B., Lakich D., Gitschier J. // Genomics. 1993, V.16, №2, P.374-379
  36. Pittman D.D., Alderman E.M., Tomkinson K.N., Wang J.H., Giles A.R., Kaufman R.J. // Blood. 1993, V.81, №11, P.2925-2935
  37. Pittman D.D., Marquette K.A., Kaufman R.J. // Blood. 1994, V.84, №12, P.4214-4225
  38. Cho M.S., Yee H., Brown C., Jeang K.T., Chan S. // Cytotechnology. 2001, V.37, №1, P.23-30
  39. Wakabayashi H., Koszelak M.E., Mastri M., Fay P.J. // Biochemistry. 2001, V.40, №34, P.10293-10300
  40. Tagliavacca L., Moon N., Dunham W.R., Kaufman R.J. // J. Biol. Chem. 1997, V.272, №43, P.27428-27434
  41. Ngo J.C., Huang M., Roth D.A., Furie B. C., Furie B. // Structure. 2008, V.16, №4, P.597-606
  42. Shen B.W., Spiegel P.C., Chang C.H., Huh J.W., Lee J.S., Kim J., Kim Y.H., Stoddard B.L. // Blood. 2008, V.111, №3, P.1240-1247
  43. Fay P.J. // Arch. Biochem. Biophys. 1998, V.262, №2, P.525-531
  44. ise R.J., Dorner A.J., Krane M., Pittman D.D., Kaufman R.J. // J. Biol. Chem. 1991, V.266, №32, P.21948-21955
  45. Wakabayashi H., Schmidt K.M., Fay P.J. // Biochemistry. 2002, V.41, №26, P.8485-8492
  46. Wakabayashi H., Zhen Z., Schmidt K.M., Fay P.J. // Biochemistry. 2003, V.42, №1, P.145-153
  47. Mukhopadhyay C.K., Mazumder B., Lindley P.F., Fox P.L. // Proc. Natl. Acad. Sci. USA. 1997, V.94, №21, P.11546-11551
  48. Wakabayashi H., Freas J., Zhou Q., Fay P.J. // J. Biol. Chem. 2004, V.279, №13, P.12677-12684
  49. Kaufman R.J., Wasley L.C., Dorner A.J. // J. Biol. Chem. 1998, V.263, №13, P.6352-6362
  50. Pipe S.W., Morris J.A., Shah J., Kaufman R.J. // J. Biol. Chem. 1998, V.273, №14, P.8537-8544
  51. Malhotra J.D., Miao H., Zhang K., Wolfson A., Pennathur S., Pipe S.W., Kaufman R.J. // Proc. Natl. Acad. Sci. USA. 2008, V.105, №47, P.18525-18530
  52. Selvaraj S.R., Scheller A.N., Miao H.Z., Kaufman R.J., Pipe S.W. // J. Thromb. Haemost. 2012, V.10, №1, P.107-115
  53. Hagiwara M., Nagata K. // Antioxid. Redox Signal. 2012, V.16, №10, P.1119-1128
  54. Liles D., Landen C.N., Monroe D.M., Lindley C.M., Read M.S., Roberts H.R., Brinkhous K.M. // Thromb. Haemost. 1997, V.77, №5, P.944-948
  55. Malhi H., Kaufman R.J. // J. Hepatol. 2011, V.54, №4, P.795-809
  56. Dorner A.J., Wasley L.C., Kaufman R.J. // J. Biol. Chem. 1989, V.264, №34, P.20602-20607
  57. Brown H.C., Gangadharan B., Doering C.B. // J. Biol. Chem. 2011, V.286, №27, P.24451-24457
  58. Murphy M.E., Lindley P.F., Adman E.T. // Protein Sci. 1997, V.6, №4, P.761-770
  59. Swaroop M., Moussalli M., Pipe S.W., Kaufman R.J. // J. Biol. Chem. 1997, V.272, №39, P.24121-24124
  60. Tagliavacca L., Wang Q., Kaufman R.J. // Biochemistry. 2000, V.39, №8, P.1973-1981
  61. Moussalli M., Pipe S.W., Hauri H.P., Nichols W.C., Ginsburg D., Kaufman R.J. // J. Biol. Chem. 1999, V.274, №46, P.32539-32542
  62. Zakas P.M., Gangadharan B., Almeida-Porada G., Porada C.D., Spencer H.T., Doering C.B. // PLoS One. 2012, V.7, №11, P.e49481
  63. Nogami K., Wakabayashi H., Schmidt K., Fay P.J. // J. Biol. Chem. 2003, V.278, №3, P.1634-1641
  64. Zhang B., McGee B., Yamaoka J.S., Guglielmone H., Downes K.A., Minoldo S., Jarchum G., Peyvandi F., de Bosch N.B., Ruiz-Saez A. // Blood. 2006, V.17, №5, P.1903-1907
  65. Fay P.J., Smudzin T.M. // J. Biol. Chem. 1992, V.267, №19, P.13246-13250
  66. White G.C. 2nd, McMillan C.W., Kingdon H.S., Shoemaker C.B. // N. Engl. J. Med. 1989, V.320, №3, P.166-170
  67. Lee D.C., Miller J.L., Petteway S.R., Jr. // Haemophilia 2002, V.8, №suppl 2, P.6-9
  68. Yoshioka A. // Textbook of Hemophilia. // New York:Wiley- Blackwell 2010, P.146-152
  69. Zhang B., Kaufman R.J., Ginsburg D. // J. Biol. Chem. 2005, V.280, №27, P.25881-25886
  70. Jankowski M.A., Patel H., Rouse J.C., Marzilli L.A., Weston S.B., Sharpe P.J. // Haemophilia. 2007, V.13, №1, P.30-37
  71. Regan L.M., O’Brien L.M., Beattie T.L., Sudhakar K., Walker F.J., Fay P.J. // J. Biol. Chem. 1996, V.271, №8, P.3982-3987
  72. Nivitchanyong T., Martinez A., Ishaque A., Murphy J.E., Konstantinov K., Betenbaugh M.J., Thrift J. // Biotechnology and Bioengineering 2007, V.98, №4, P.825-841
  73. Nogami K., Wakabayashi H., Fay P.J. // J. Biol. Chem. 2003, V.278, №19, P.16502-16509
  74. Leyte A., van Schijndel H.B., Niehrs C., Huttner W.B., Verbeet M.P., Mertens K., van Mourik J.A. // J. Biol. Chem. 1991, V.266, №2, P.740-746
  75. Higuchi M., Wong C., Kochhan L., Olek K., Aronis S., Kasper C.K., Kazazian H.H., Jr., Antonarakis S.E. // Genomics. 1990, V.6, №1, P.65-71
  76. Michnick D.A., Pittman D.D., Wise R.J., Kaufman R.J. // J. Biol. Chem. 1994, V.269, №31, P.2095-2102
  77. Adamson R. // Ann. Hematol. 1994, V.68, №Suppl3, P.S9-14
  78. Leyte A., Verbeet M.P., Brodniewicz-Proba T., van Mourik J.A., Mertens K. // Biochem. J. 1989, V.257, №3, P.679-683
  79. Saenko E.L., Scandella D. // J. Biol. Chem. 1997, V.272, №29, P.18007-18014
  80. Jacquemin M., Benhida A., Peerlinck K., Desqueper B., Vander Elst L., Lavend’homme R., d’Oiron R., Schwaab R., Bakkus M., Thielemans K. // Blood. 2000, V.95, №1, P.156-163
  81. Hamer R.J., Koedam J.A., Beeser-Visser N.H., Sixma J.J. // Eur. J. Biochem. 1987, V.167, №2, P.253-259
  82. Hill-Eubanks D.C., Lollar P. // J. Biol. Chem. 1990, V.265, №29, P.17854-17858
  83. Koedam J.A., Hamer R.J., Beeser-Visser N.H., Bouma B.N., Sixma J.J. // Eur. J. Biochem. 1990, V.189, №2, P.229-234
  84. Koedam J.A., Meijers J.C., Sixma J.J., Bouma B.N. // J. Clin. Invest. 1998, V.82, №4, P.1236-1243
  85. Fay P.J., Coumans J.V., Walker F.J. // J. Biol. Chem. 1991, V.266, P.2172-2177
  86. Nogami K., Shima M., Nishiya K., Hosokawa K., Saenko E.L., Sakurai Y., Shibata M., Suzuki H., Tanaka I., Yoshioka A. // Blood. 2002, V.99, №11, P.3993-3998
  87. Nesheim M., Pittman D.D., Giles A.R., Fass D.N., Wang J.H., Slonosky D., Kaufman R.J. // J. Biol. Chem. 1991, V.266, №27, P.17815-17820
  88. Cho M.S., Yee H., Brown C., Mei B., Mirenda C., Chan S. // Biotechnol. Prog. 2003, V.19, №1, P.229-232
  89. Gilbert G.E., Drinkwater D., Barter S., Clouse S.B. // J. Biol. Chem. 1992, V.267, №22, P.15861-15868
  90. Gilles J.G., Jacquemin M.G., Saint-Remy J.M. // Thromb. Haemost. 1997, V.78, №1, P.641-646
  91. Franchini M., Lippi G. // Blood. 2008, V.112, №2, P.250-255
  92. Tuddenham E.G., McVey J.H. // Haemophilia. 1998, V.4, №4, P.543-545
  93. Gouw S.C., van den Berg H.M., Oldenburg J., Astermark J., de Groot P.G., Margaglione M., Thompson A.R., van Heerde W., Boekhorst J., Miller C.H., le Cessie S., van den Bom J.G. // Blood. 2012, V.119, №12, P.2922-2934
  94. Towfighi F., Gharagozlou S., Sharifian R.A., Kazemnejad A., Esmailzadeh K., Managhchi M.R., Shokri F. // Acta Haematol 2005, V.114, №2, P.84-90
  95. Green D. // Haemophilia. 2011, V.17, №6, P.831-838
  96. Lacroix-Desmazes S., Moreau A., Sooryanarayana I.O., Bonnemain C., Stieltjes N., Pashov A., Sultan Y., Hoebeke J., Kazatchkine M.D., Kaveri S.V. // Nat. Med. 1999, V.5, №9, P.1044-1047
  97. Lacroix-Desmazes S., Bayry J., Misra N., Horn M.P., Villard S., Pashov A., Stieltjes N., d’Oiron R., Saint-Remy J.M., Hoebeke J. // N. Engl. J. Med. 2002, V.346, №9, P.662-667
  98. Lenting P.J., Donath M.J., van Mourik J.A., Mertens K. // J. Biol. Chem. 1994, V.269, №10, P.7150-7155
  99. Duffy E.J., Parker E.T., Mutucumarana V.P., Johnson A.E., Lollar P. // J. Biol. Chem. 1992, V.267, №24, P.17006-17011
  100. Curtis J.E., Helgerson S.L., Parker E.T., Lollar P. // J. Biol. Chem. 1994, V.268, №8, P.6246-6251
  101. Bovenschen N., Boertjes R.C., van Stempvoort G., Voorberg J., Lenting P.J., Meijer A. B., Mertens K. // J. Biol. Chem. 2003, V.278, №11, P.9370-9377
  102. Gilbert G.E., Furie B.C., Furie B. // J. Biol. Chem. 1990, V.265, №2, P.815-822
  103. Kemball-Cook G., Barrowcliffe T.W. // Thromb. Res. 1992, V.67, №1, P.57-71
  104. Cho M.S., Chan S.Y. // Vectors having terminal repeat sequence of Epstein-Barr virus // Patent of USA № 6180108 2001
  105. Saenko E.L., Scandella D., Yakhyaev A.V., Greco N.J. // J. Biol. Chem. 1998, V.273, №43, P.27918-27926
  106. Arai M., Scandella D., Hoyer L.W. // J. Clin. Invest. 1989, V.83, №6, P.1978-1984
  107. Eaton D., Rodriguez H., Vehar G.A. // Biochemistry. 1986, V.25, №2, P.505-512
  108. Lollar P., Knutson G.J., Fass D.N. // Biochemistry. 1985, V.24, №27, P.8056-8064
  109. Fay P.J., Haidaris P.J., Smudzin T.M. // J. Biol. Chem. 1991, V.266, №14, P.8957-8962
  110. Hockin M.F., Jones K.C., Everse S.J., Mann K.G. // J. Biol. Chem. 2002, V.277, №21, P.18322-18333
  111. Saenko E.L., Yakhyaev A.V., Mikhailenko I., Strickland D.K., Sarafanov A.G. // J. Biol. Chem. 1999, V.274, №53, P.37685-37692
  112. Lenting P.J., Neels J.G., van den Berg B.M., Clijsters P.P., Meijerman D.W., Pannekoek H., van Mourik J.A., Mertens K., van Zonneveld A.J. // J. Biol. Chem. 1999, V.274, №34, P.23734-23739
  113. Turecek P.L., Schwarz H.P., Binder B.R. // Blood. 2000, V.95, №11, P.3637-3638
  114. Sarafanov A.G., Ananyeva N.M., Shima M., Saenko E.L. // J. Biol. Chem. 2001, V.276, №15, P.11970-11979
  115. Schwartz R.S., Abildgaard C.F., Aledort L.M., Arkin S., Bloom A.L., Brackmann H.H., Brettler D.B., Fukui H., Hilgartner M.W., Inwood M.J. // N. Engl. J. Med. 1990, V.323, №26, P.1800-1805
  116. Josephson C.D., Abshire T. // Clin. Adv. Hematol. Oncol. 2004, V.2, №7, P.441-446
  117. Gomperts E., Lundblad R., Adamson R. // Transfus. Med. Rev. 1992, V.6, №4, P.247-251
  118. Toole J.J., Pittman D.D., Orr E.C., Murtha P., Wasley L.C., Kaufman R.J. // Proc. Natl. Acad. Sci. USA. 1986, V.83, №16, P.5939-5942
  119. Lind P., Larsson K., Spira J., Sydow-Backman M., Almstedt A., Gray E., Sandberg H. // Eur. J. Biochem. 1995, V.232, №1, P.19-27
  120. Sandberg H., Almstedt A., Brandt J., Gray E., Holmquist L., Oswaldsson U., Sebring S., Mikaelsson M. // Thromb. Haemost. 2001, V.85, №1, P.93-100
  121. Meulien P., Faure T., Mischler F., Harrer H., Ulrich P., Bouderbala B., Dott K., Sainte Marie M., Mazurier C., Wiesel M. L. // Protein Eng. 1988, V.2, №4, P.301-306
  122. Eaton D.L., Wood W.I., Eaton D., Hass P.E., Hollingshead P., Wion K., Mather J., Lawn R.M., Vehar G.A., Gorman C. // Biochemistry. 1986, V.25, №26, P.8343-8347
  123. Yonemura H., Sugawara K., Nakashima K., Nakahara Y., Hamamoto T., Mimaki I., Yokomizo K., Tajima Y., Masuda K., Imaizumi A. // Protein Eng. 1993, V.6, №6, P.669-674
  124. Kolind M.P., Norby P.L., Flintegaard T.V., Berchtold M.W., Johnsen L.B. // J. Biotechnol. 2010, V.143, №3-4, P.198-204
  125. Thim L., Vandahl B., Karlsson J., Klausen N.K., Pedersen J., Krogh T.N., Kjalke M., Petersen J.M., Johnsen L.B., Bolt G., Norby P.L., Steenstrup T.D. // Haemophilia. 2010, V.16, №2, P.349-359
  126. Sandberg H., Kannicht C., Stenlund P., Dadaian M., Oswaldsson U., Cordula C., Walter O. // Thromb. Res. 2012, V.130, №5, P.808-817
  127. Miao H.Z., Sirachainan N., Palmer L., Kucab P., Cunningham M.A., Kaufman R.J., Pipe S.W. // Blood. 2004, V.103, №9, P.3412-3419
  128. Krishnan S., Kolbe H.V., Lepage P., Faure T., Sauerwald R., de la Salle H., Muller C., Bihoreau N., Paolantonacci P., Roitsch C. // Eur. J. Biochem. 1991, V.195, №3, P.637-644
  129. Esmon P.C., Kuo H.S., Fournel M.A. // Blood. 1990, V.76, №8, P.1593-1600
  130. Herlitschka S.E., Schlokat U., Falkner F.G., Dorner F. // J. Biotechnol. 1998, V.61, №3, P.165-173
  131. Fatouros A., Osterberg T., Mikaelsson M. // Pharm. Res. 1997, V.14, №12, P.1679-1684
  132. Osterberg T., Fatouros A., Mikaelsson M. // Pharm. Res. 1997, V.14, №7, P.892-898
  133. Osterberg T., Fatouros A., Neidhardt E., Warne N., Mikaelsson M. // Semin. Hematol. 2001, V.38, №2, P.40-43
  134. Fijnvandraat K., Berntorp E., ten Cate J.W., Johnsson H., Peters M., Savidge G., Tengborn L., Spira J., Stahl C. // Thromb. Haemost. 1997, V.77, №2, P.298-302
  135. Eriksson R.K., Fenge C., Lindner-Olsson E., Ljungqvist C., Rosenquist J., Smeds A.L., ostlin A., Charlebois T., Leonard M., Kelley B.D., Ljungqvist A. // Semin. Hematol. 2001, V.38, №2, P.24-31
  136. Chun B.H., Park S.Y., Chung N., Bang W.G. // Biotechnol. Lett. 2003, V.25, №4, P.315-319
  137. Kelley B.D., Tannatt M., Magnusson R., Hagelberg S., Booth J. // Biotechnology and Bioengineering 2004, V.87, №3, P.400-412
  138. Lusher J.M., Lee C.A., Kessler C.M., Bedrosian C.L. // Haemophilia. 2003, V.9, №1, P.38-49
  139. Smith M.P., Giangrande P., Pollman H., Littlewood R., Kollmer C., Feingold J. // Haemophilia. 2005, V.11, №5, P.444-4551
  140. Recht M., Nemes L., Matysiak M., Manco-Johnson M., Lusher J., Smith M., Mannucci P., Hay C., Abshire T., O’Brien A., Hayward B., Udata C., Roth D.A., Arkin S. // Haemophilia. 2009, V.15, №4, P.869-880
  141. Gruppo R.A., Brown D., Wilkes M.M., Navickis R.J. // Haemophilia. 2004, V.10, №6, P.747-750
  142. Gruppo R.A., Brown D., Wilkes M.M., Navickis R.J. // Haemophilia. 2004, V.10, №5, P.449-451
  143. Morfini M., Cinotti S., Bellatreccia A., Paladino E., Gringeri A., Mannucci P.M. // J. Thromb. Haemost. 2003, V.1, №11, P.2283-2289
  144. Johnston A. // Ther. Drug Monit. 2012, V.34, №1, P.110-117
  145. Khrenov A.V., Ananyeva N.M., Saenko E.L. // Blood Coagul. Fibrinolysis. 2006, V.17, №5, P.379-388
  146. Lusher J.M. // Semin. Thromb. Hemost. 2002, V.28, №3, P.273-276
  147. Pollmann H., Externest D., Ganser A., Eifrig B., Kreuz W., Lenk H., Pabinger I., Schramm W., Schwarz T.F., Zimmermann R. // Haemophilia. 2007, V.13, №2, P.131-143
  148. Gouw S.C., van den Berg H.M., le Cessie S., van der Bom der J.G. // J. Thromb. Haemost. 2007, V.5, №7, P.1383-1390
  149. Aledort L.M., Navickis R.J., Wilkes M.M. // J. Thromb. Haemost. 2011, V.9, №11, P.2180-2192
  150. Lee C.A., Kessler C.M., Varon D., Martinowitz U., Heim M., Vermylen J. // Haemophilia. 1998, V.4, №4, P.538-542
  151. Martinowitz U., Bjerre J., Brand B., Klamroth R., Misgav M., Morfini M., Santagostino E., Tiede A., Viuff D. // Haemophilia. 2011, V.17, №6, P.854-859
  152. Mei B., Chen Y., Chen J., Pan C.Q., Murphy J.E. // Mol. Biotechnol. 2006, V.34, №2, P.165-178
  153. Lynch C.M., Israel D.I., Kaufman R.J., Miller A.D. // Hum. Gene Ther. 1993, V.4, №3, P.259-272
  154. Koeberl D.D., Halbert C.L., Krumm A., Miller A.D. // Hum. Gene Ther. 1995, V.6, №4, P.469-479
  155. Hoeben R.C., Fallaux F.J., Cramer S.J., van den Wollenberg D.J., van Ormondt H., Briet E., van der Eb A.J. // Blood. 1995, V.85, №9, P.2447-2454
  156. Fallaux F.J., Hoeben R.C., Cramer S.J., van den Wollenberg D.J., Briet E., van Ormondt H., van der Eb A.J. // Mol. Cell. Biol. 1996, V.16, №8, P.4264-4272
  157. Ward N.J., Buckley S.M., Waddington S.N., Vandendriessche T., Chuah M.K., Nathwani A.C., McIntosh J., Tuddenham E.G., Kinnon C., Thrasher A.J. // Blood. 2011, V.117, №3, P.798-807
  158. Roe S.M., Gormal C., Smith B.E., Baker P., Rice D., Card G., Lindley P. // Acta Crystallogr. D Biol. Crystallogr. 1997, V.53, №2, P.227-228
  159. Lindley E.J. // EDTNA ERC A J. 1997, V.23, №2, P.50-51
  160. Ishaque A., Thrift J., Murphy J.E., Konstantinov K. // Biotechnology and Bioengineering 2007, V.97, №1, P.144-155
  161. Li X., Gabriel D.A. // Biochemistry. 1997, V.36, №35, P.10760-10767
  162. Kolind M.P., Norby P.L., Berchtold M.W., Johnsen L.B. // J. Biotechnol. 2011, V.151, №4, P.357-362
  163. Levy J.H., Weisinger A., Ziomek C.A., Echelard Y. // Semin. Thromb. Hemost. 2011, V.27, №4, P.405-416
  164. Gil G.C., Velander W.H., van Cott K.E. // Glycobiology. 2008, V.18, №7, P.526-539
  165. Pipe S.W., Miao H., Butler S.P., Calcaterra J., Velander W.H. // J. Thromb. Haemost. 2011, V.9, №11, P.2235-2242
  166. hen C.M., Wang C.H., Wu S.C., Lin C.C., Lin S.H., Cheng W.T. // Transgenic Res. 2012, V.11, №3, P.257-268
  167. Chrenek P., Ryban L., Vetr H., Makarevich A.V., Uhrin P., Paleyanda R.K., Binder B.R. // Transgenic Res. 2007, V.16, №3, P.353-361
  168. Niemann H., Halter R., Carnwath J. W., Herrmann D., Lemme E., Paul D. // Transgenic Res. 1999, V.8, №3, P.234-247
  169. Paleyanda R.K., Velander W.H., Lee T.K., Scandella D.H., Gwazdauskas F.C., Knight J.W., Hoyer L.W., Drohan W.N., Lubon H. // Nat. Biotechnol. 1997, V.15, №10, P.971-975
  170. Dove A. // Nat. Biotechnol. 2000, V.18, №10, P.1045-1048
  171. Panno J. // Animal Cloning: The Science of Nuclear Transfer // New York:Facts on File 2004, P.176
  172. Rostin J., Smeds A.L., Akerblom E. // Bioconjug. Chem. 2000, V.11, №3, P.387-396
  173. Mei B., Pan C., Jiang H., Tjandra H., Strauss J., Chen Y., Liu T., Zhang X., Severs J., Newgren J., Chen J., Gu J.M., Subramanyam B., Fournel M.A., Pierce G.F., Murphy J.E. // Blood. 2010, V.116, №2, P.270-279
  174. Turecek P.L., Bossard M.J., Graninger M., Gritsch H., Hollriegl W., Kaliwoda M., Matthiessen P., Mitterer A., Muchitsch E.M., Purtscher M. // Hamostaseologie. 2012, V.32, P.S29-38
  175. Dumont J.A., Liu T., Low S.C., Zhang X., Kamphaus G., Sakorafas P., Fraley C., Drager D., Reidy T., McCue J. // Blood. 2012, V.119, №13, P.3024-3030
  176. Powell J.S., Josephson N.C., Quon D., Ragni M.V., Cheng G., Li E., Jiang H., Li L., Dumont J.A., Goyal J. // Blood. 2012, V.119, №13, P.3031-3037
  177. Pipe S.W. // Blood. 2010, V.116, №2, P.153-154
  178. Pipe S.W., Kaufman R.J. // Proc. Natl. Acad. Sci. USA. 1994, V.94, №22, P.11851-11856
  179. Greene T.K., Wang C., Hirsch J.D., Zhai L., Gewirtz J., Thornton M.A., Miao H. Z., Pipe S.W., Kaufman R.J., Camire R.M. // Blood. 2010, V.116, №26, P.6114-6122
  180. Gale A.J., Pellequer J.L. // J. Thromb. Haemost. 2003, V.1, №9, P.1966-1971
  181. Radtke K.P., Griffin J.H., Riceberg J., Gale A.J. // J. Thromb. Haemost. 2007, V.5, №1, P.102-108
  182. Wakabayashi H., Varfaj F., Deangelis J., Fay P.J. // Blood. 2008, V.112, №7, P.2761-2769
  183. Parker E.T., Healey J.F., Barrow R.T., Craddock H.N., Lollar P. // Blood. 2004, V.104, №3, P.704-710
  184. Barrow R.T., Healey J.F., Gailani D., Scandella D., Lollar P. // Blood. 2000, V.95, №2, P.564-568
  185. Toschi V. // Curr. Opin. Mol. Ther. 2010, V.12, №5, P.617-625
  186. Kempton C.L., Abshire T.C., Deveras R.A., Hoots W.K., Gill J.C., Kessler C.M., Key N.S., Konkle B.A., Kuriakose P., Macfarlane D.E. // Haemophilia. 2012, V.18, №5, P.798-804
  187. Milanov P., Ivanciu L., Abriss D., Quade-Lyssy P., Miesbach W., Alesci S., Tonn T., Grez M., Seifried E., Schuttrumpf J. // Blood. 2012, V.119, №2, P.602-611
  188. Kitazawa T., Igawa T., Sampei Z., Muto A., Kojima T., Soeda T., Yoshihashi K., Okuyama-Nishida Y., Saito H., Tsunoda H. // Nat. Med. 2012, V.18, №10, P.1570-1574

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