Seminars in Hematology
Volume 41, Issue 1 , Pages 24-33 , January 2004

Expression and characterization of recombinant human ADAMTS-13

  • Barbara Plaimauer

      Affiliations

    • Baxter BioScience, Biomedical Research Center, Orth/Donau, Austria
  • ,
  • Friedrich Scheiflinger

      Affiliations

    • Corresponding Author InformationAddress correspondence to Friedrich Scheiflinger, PhD, Baxter BioScience, Biomedical Research Center, Uferstrasse 15, Orth/Donau 2304, Austria
    • Baxter BioScience, Biomedical Research Center, Orth/Donau, Austria

References 

  1. Sporn LA, Marder VJ, Wagner DD. von Willebrand factor released from Weibel-Palade bodies binds more avidly to extracellular matrix than that secreted constitutively. Blood. 1987;69:1531–1534
  2. Federici AB, Bader R, Pagani S, Colibretti ML, De Marco L, Mannucci PM. Binding of von Willebrand factor to glycoproteins Ib and IIb/IIIa complex (Affinity is related to multimeric size). Br J Haematol. 1989;73:93–99
  3. Goto S, Ikeda Y, Saldivar E, Ruggeri ZM. Distinct mechanisms of platelet aggregation as a consequence of different shearing flow conditions. J Clin Invest. 1998;101:479–486
  4. Sugimoto M, Tsuji S, Kuwahara M, Matsui H, Miyata S, Fujimura Y, et al.  Shear-dependent functions of the interaction between soluble von Willebrand factor and platelet glycoprotein Ib in mural thrombus formation on a collagen surface. Int J Hematol. 1999;69:48–53
  5. Furlan M, Robles R, Lämmle B. Partial purification and characterization of a protease from human plasma cleaving von Willebrand factor to fragments produced by in vivo proteolysis. Blood. 1996;87:4223–4234
  6. Tsai HM. Physiologic cleavage of von Willebrand factor by a plasma protease is dependent on its conformation and requires calcium ion. Blood. 1996;87:4235–4244
  7. Dent JA, Berkowitz SD, Ware J, Kasper CK, Ruggeri ZM. Identification of a cleavage site directing the immunochemical detection of molecular abnormalities in type IIA von Willebrand factor. Proc Natl Acad Sci USA. 1990;87:6306–6310
  8. Bukowski RM. Thrombotic thrombocytopenic purpura (A review). Prog Hemost Thromb. 1982;6:287–337
  9. Moschcowitz E. Hyaline thrombosis of the terminal arterioles and capillaries (A hitherto undescribed disease). Proc NY Pathol Soc. 1924;24:21–24
  10. Fujikawa K, Suzuki H, McMullen B, Chung D. Purification of human von Willebrand factor-cleaving protease and its identification as a new member of the metalloproteinase family. Blood. 2001;98:1662–1666
  11. Gerritsen HE, Robles R, Lämmle B, Furlan M. Partial amino acid sequence of purified von Willebrand factor-cleaving protease. Blood. 2001;98:1654–1661
  12. Soejima K, Mimura N, Hirashima M, Maeda H, Hamamoto T, Nakagaki T, et al.  A novel human metalloprotease synthesized in the liver and secreted into the blood (Possibly, the von Willebrand factor-cleaving protease?). J Biochem (Tokyo). 2001;130:475–480
  13. Zheng X, Chung D, Takayama TK, Majerus EM, Sadler JE, Fujikawa K. Structure of von Willebrand factor-cleaving protease (ADAMTS13), a metalloprotease involved in thrombotic thrombocytopenic purpura. J Biol Chem. 2001;276:41059–41063
  14. Kokame K, Matsumoto M, Soejima K, Yagi H, Ishizashi H, Funato M, et al.  Mutations and common polymorphisms in ADAMTS13 gene responsible for von Willebrand factor-cleaving protease activity. Proc Natl Acad Sci USA. 2002;99:11902–11907
  15. Plaimauer B, Zimmermann K, Völkel D, Antoine G, Kerschbaumer R, Jenab P, et al.  Cloning, expression, and functional characterization of the von Willebrand factor-cleaving protease (ADAMTS13). Blood. 2002;100:3626–3632
  16. Zheng X, Nishio K, Majerus EM, Sadler JE. Cleavage of von Willebrand factor requires the spacer domain of the metalloprotease ADAMTS13. J Biol Chem. 2003;278:30136–30141
  17. Motto D, Levy GG, McGee BM, Tsai HM, Ginsburg D. ADAMTS13 mutations identified in familial TTP patients result in loss of VWF-cleaving protease activity. Blood. 2002;100:44; (abstr)
  18. Cal S, Obaya AJ, Llamazares M, Garabaya C, Quesada V, Lopez-Otin C. Cloning, expression analysis, and structural characterization of seven novel human ADAMTSs, a family of metalloproteinases with disintegrin and thrombospondin-1 domains. Gene. 2002;283:49–62
  19. Levy GG, Nichols WC, Lian EC, Foroud T, McClintick JN, McGee BM, et al.  Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature. 2001;413:488–494
  20. Lee T, Bouhassira EE, Lyubsky S, Tsai HM. ADAMTS13, the von Willebrand factor cleaving metalloprotease, is expressed in the perisinusoidal cells of the liver. Blood. 2002;100:1938; (abstr)
  21. Tang BL. ADAMTS (A novel family of extracellular matrix proteases). Int J Biochem Cell Biol. 2001;33:33–44
  22. Stocker W, Grams F, Baumann U, Reinemer P, Gomis-Ruth FX, McKay DB, et al.  The metzincins—Topological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a superfamily of zinc-peptidases. Protein Sci. 1995;4:823–840
  23. Somerville RP, Longpre JM, Jungers KA, Engle JM, Ross M, Evanko S, et al.  Characterization of ADAMTS-9 and ADAMTS-20 as a distinct ADAMTS subfamily related to Caenorhabditis elegans GON-1. J Biol Chem. 2003;278:9503–9513
  24. Hofsteenge J, Huwiler KG, Macek B, Hess D, Lawler J, Mosher DF, et al.  C-mannosylation and O-fucosylation of the thrombospondin type 1 module. J Biol Chem. 2001;276:6485–6498
  25. Asch AS, Silbiger S, Heimer E, Nachman RL. Thrombospondin sequence motif (CSVTCG) is responsible for CD36 binding. Biochem Biophys Res Commun. 1992;182:1208–1217
  26. Li WX, Howard RJ, Leung LL. Identification of SVTCG in thrombospondin as the conformation-dependent, high affinity binding site for its receptor, CD36. J Biol Chem. 1993;268:16179–16184
  27. Soejima K, Matsumoto M, Kokame K, Yagi H, Ishizashi H, Maeda H, et al: ADAMTS-13 cysteine-rich/spacer domains are functionally essential for von Willebrand factor cleavage. Blood (in press)
  28. Bond JS, Beynon RJ. The astacin family of metalloendopeptidases. Protein Sci. 1995;4:1247–1261
  29. Banno F, Kaminaka K, Soejima K, Kokame K, Miyata T. Identification of strain-specific variants of mouse ADAMTS13 gene encoding von Willebrand factor-cleaving protease. J Thromb Haemost. 2003;(suppl 1): (abstr OC120)
  30. Sadler JE. A new name in thrombosis, ADAMTS13. Proc Natl Acad Sci USA. 2002;99:11552–11554
  31. Motto D, Levy G, McGee B, Tsai HM, Ginsburg D. ADAMTS13 mutations identified in familial TTP patients in loss of VWF-cleaving protease activity. J Thromb Haemost. 2003;(suppl 1): (abstr OC115)
  32. Rodriguez-Manzaneque JC, Milchanowski AB, Dufour EK, Leduc R, Iruela-Arispe ML. Characterization of METH-1/ADAMTS1 processing reveals two distinct active forms. J Biol Chem. 2000;275:33471–33479
  33. Gao G, Westling J, Thompson VP, Howell TD, Gottschall PE, Sandy JD. Activation of the proteolytic activity of ADAMTS4 (aggrecanase-1) by C-terminal truncation. J Biol Chem. 2002;277:11034–11041
  34. Cal S, Arguelles JM, Fernandez PL, Lopez-Otin C. Identification, characterization, and intracellular processing of ADAM-TS12, a novel human disintegrin with a complex structural organization involving multiple thrombospondin-1 repeats. J Biol Chem. 2001;276:17932–17940
  35. Chen H, Herndon ME, Lawler J. The cell biology of thrombospondin-1. Matrix Biol. 2000;19:597–614
  36. Lawler J. Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth. J Cell Mol Med. 2002;6:1–12
  37. Dawson DW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouk NP. CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J Cell Biol. 1997;138:707–717
  38. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med. 2000;6:41–48
  39. Iruela-Arispe ML, Lombardo M, Krutzsch HC, Lawler J, Roberts DD. Inhibition of angiogenesis by thrombospondin-1 is mediated by 2 independent regions within the type 1 repeats. Circulation. 1999;100:1423–1431
  40. Adams JC, Tucker RP. The thrombospondin type 1 repeat (TSR) superfamily (diverse proteins with related roles in neuronal development). Dev Dyn. 2000;218:280–299
  41. Iruela-Arispe ML, Vazquez F, Ortega MA. Antiangiogenic domains shared by thrombospondins and metallospondins, a new family of angiogenic inhibitors. Ann NY Acad Sci. 1999;886:58–66
  42. Vazquez F, Hastings G, Ortega MA, Lane TF, Oikemus S, Lombardo M, et al.  METH-1, a human ortholog of ADAMTS-1, and METH-2 are members of a new family of proteins with angio-inhibitory activity. J Biol Chem. 1999;274:23349–23357
  43. Mannucci PM, Karimi M, Mosalaei A, Canciani MT, Peyvandi F. Patients with localized and disseminated tumors have reduced but measurable levels of ADAMTS-13 (von Willebrand factor cleaving protease). Haematologica. 2003;88:454–458
  44. Blot E, Decaudin D, Veyradier A, Bardier A, Zagame OL. Pouillart (Cancer-related thrombotic microangiopathy secondary to von Willebrand factor-cleaving protease deficiency). Thromb Res. 2002;106:127–130
  45. Koo BH, Oh D, Chung SY, Kim NK, Park S, Jang Y, et al.  Deficiency of von Willebrand factor-cleaving protease activity in the plasma of malignant patients. Thromb Res. 2002;105:471–476
  46. Oleksowicz L, Bhagwati N, DeLeon-Fernandez M. Deficient activity of von Willebrand’s factor-cleaving protease in patients with disseminated malignancies. Cancer Res. 1999;59:2244–2250
  47. Kuno K, Matsushima K. ADAMTS-1 protein anchors at the extracellular matrix through the thrombospondin type I motifs and its spacing region. J Biol Chem. 1998;273:13912–13917
  48. Luken BM, Turenhout EAM, Fijenheer R, Voorberg J. Novel approaches to determine the characteristics of ADAMTS13 inhibitors in patients with acquired TTP. J Thromb Haemost. 2003;(suppl 1): (abstr PO309)
  49. Turecek PL, Furlan M, Lämmle B, Gritsch H, Richter G, Siekmann , et al.  Cleavage of recombinant von Willebrand factor by a VWF-depolymerizing protease. Blood. 1996;88:326A; (abstr)
  50. Schneppenheim R, Budde U, Oyen F, Angerhaus D, Aumann V, Drewke E, et al.  von Willebrand factor cleaving protease and ADAMTS13 mutations in childhood TTP. Blood. 2003;101:1845–1850
  51. Kuno K, Terashima Y, Matsushima K. ADAMTS-1 is an active metalloproteinase associated with the extracellular matrix. J Biol Chem. 1999;274:18821–18826
  52. Furlan M, Robles R, Morselli B, Sandoz P, Lämmele B. Recovery and half-life of von Willebrand factor-cleaving protease after plasma therapy in patients with thrombotic thrombocytopenic purpura. Thromb Haemost. 1999;81:8–13
  53. Kentouche K, Budde U, Furlan M, Scharfe V, Schneppenheim R, Zintl F. Remission of thrombotic thrombocytopenic purpura in a patient with compound heterozygous deficiency of von Willebrand factor-cleaving protease by infusion of solvent/detergent plasma. Acta Paediatr. 2002;91:1056–1059
  54. Schneppenheim R, Angerhaus D, Mainusch K, Obser T, Oyen F, Budde U: Comparative expression of recombinant wildtype and mutant von Willebrand factor cleaving protease ADAMTS13. J Thromb Haemost (suppl 1, abstr OC117)
  55. Antoine G, Zimmermann K, Plaimauer B, Grillowitzer M, Studt JD, Lämmle B, et al.  ADAMTS13 gene defects in two brothers with constitutional thrombotic thrombocytopenic purpura and normalization of von Willebrand factor-cleaving protease activity by recombinant human ADAMTS13. Br J Haematol. 2003;120:821–824
  56. Assink K, Schiphorst R, Allford S, Karpman D, Etzioni A, Brichard B, et al.  Mutation analysis and clinical implications of von Willebrand factor-cleaving protease deficiency. Kidney Int. 2003;63:1995–1999
  57. Veyradier A, Lavergne JM, Obert B, Ribba AS, Fressinaud E, Loirat C, et al: Identification of seven new candidate mutations of ADAMTS13 gene in four French families related to congenital thrombotic thrombocytopenic purpura. J Thromb Haemost (suppl 1, abstr P0310)
  58. Dong JF, Moake JL, Bernardo A, Fujikawa K, Ball C, Nolasco L, et al.  ADAMTS-13 metalloprotease interacts with the endothelial cell-derivd ultra-large von Willebrand factor. J Biol Chem. 2003;278:29633–29639
  59. Gerritsen HE, Turecek PL, Schwarz HP, Lämmle B, Furlan M. Assay of von Willebrand factor (vWF)-cleaving protease based on decreased collagen binding affinity of degraded vWF (A tool for the diagnosis of thrombotic thrombocytopenic purpura (TTP)). Thromb Haemost. 1999;82:1386–1389
  60. Dong JF, Moake JL, Nolasco L, Bernardo A, Arceneaux W, Shrimpton CN, et al.  ADAMTS-13 rapidly cleaves newly secreted ultralarge von Willebrand factor multimers on the endothelial surface under flowing conditions. Blood. 2002;100:4033–4039
  61. Furlan M, Robles R, Solenthaler M, Wassmer M, Sandoz P, Lämmle B. Deficient activity of von Willebrand factor-cleaving protease in chronic relapsing thrombotic thrombocytopenic purpura. Blood. 1997;89:3097–3103
  62. Furlan M, Lämmle B. Deficiency of von Willebrand factor-cleaving protease in familial and acquired thrombotic thrombocytopenic purpura. Baillieres Clin Haematol. 1998;11:509–514
  63. Furlan M, Robles R, Solenthaler M, Lämmle B. Acquired deficiency of von Willebrand factor-cleaving protease in a patient with thrombotic thrombocytopenic purpura. Blood. 1998;91:2839–2846
  64. Tsai HM, Lian EC. Antibodies to von Willebrand factor-cleaving protease in acute thrombotic thrombocytopenic purpura. N Engl J Med. 1998;339:1585–1594
  65. Gerritsen HE, Robles R, Lämmle B, Furlan M. Partial amino acid sequence of purified von Willebrand factor-cleaving protease. Blood. 2001;98:1654–1661

PII: S0037-1963(03)00272-5

doi: 10.1053/j.seminhematol.2003.10.006

Seminars in Hematology
Volume 41, Issue 1 , Pages 24-33 , January 2004