Function of Von Willebrand Factor After Crossed Bone Marrow Transplantation Between Normal and Von Willebrand Disease Pigs: Effect on Arterial Thrombosis in Chimeras

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1995 Mar 28

PMID 7708664

Citations 20

Authors

T C Nichols

C M Samama

D A Bellinger

J Roussi

R L Reddick

M Bonneau

M S Read

O Bailliart

G G Koch

M Vaiman

Affiliations

Soon will be listed here.

Abstract

von Willebrand factor (vWF) is essential for the induction of occlusive thrombosis in stenosed and injured pig arteries and for normal hemostasis. To separate the relative contribution of plasma and platelet vWF to arterial thrombosis, we produced chimeric normal and von Willebrand disease pigs by crossed bone marrow transplantation; von Willebrand disease (vWD) pigs were engrafted with normal pig bone marrow and normal pigs were engrafted with vWD bone marrow. Thrombosis developed in the chimeric normal pigs that showed normal levels of plasma vWF and an absence of platelet vWF; but no thrombosis occurred in the chimeric vWD pigs that demonstrated normal platelet vWF and an absence of plasma vWF. The ear bleeding times of the chimeric pigs were partially corrected by endogenous plasma vWF but not by platelet vWF. Our animal model demonstrated that vWF in the plasma compartment is essential for the development of arterial thrombosis and that it also contributes to the maintenance of bleeding time and hemostasis.

Citing Articles

Dispatch and delivery at the ER-Golgi interface: how endothelial cells tune their hemostatic response.

Kat M, Margadant C, Voorberg J, Bierings R FEBS J. 2022; 289(22):6863-6870.

PMID: 35246944 PMC: 9790534. DOI: 10.1111/febs.16421.

Hyperglycemia-induced oxidative stress promotes tumor metastasis by upregulating vWF expression in endothelial cells through the transcription factor GATA1.

Jeong H, Lee D, Kim S, Lee C, Shin H, Kim H Oncogene. 2022; 41(11):1634-1646.

PMID: 35094008 DOI: 10.1038/s41388-022-02207-y.

Modulation of endothelial organelle size as an antithrombotic strategy.

Ferraro F, Patella F, Costa J, Ketteler R, Kriston-Vizi J, Cutler D J Thromb Haemost. 2020; 18(12):3296-3308.

PMID: 32881285 PMC: 8436738. DOI: 10.1111/jth.15084.

Platelet α-granules are required for occlusive high-shear-rate thrombosis.

Kim D, Ashworth K, Di Paola J, Ku D Blood Adv. 2020; 4(14):3258-3267.

PMID: 32697818 PMC: 7391145. DOI: 10.1182/bloodadvances.2020002117.

Acquired von Willebrand Syndrome Associated with Cardiovascular Diseases.

Horiuchi H, Doman T, Kokame K, Saiki Y, Matsumoto M J Atheroscler Thromb. 2019; 26(4):303-314.

PMID: 30867356 PMC: 6456452. DOI: 10.5551/jat.RV17031.

References

Tuddenham E, Lane R, Rotblat F, Johnson A, Snape T, Middleton S . Response to infusions of polyelectrolyte fractionated human factor VIII concentrate in human haemophilia A and von Willebrand's disease. Br J Haematol. 1982; 52(2):259-67. DOI: 10.1111/j.1365-2141.1982.tb03888.x. View

Reddick R, Griggs T, Lamb M, Brinkhous K . Platelet adhesion to damaged coronary arteries: Comparison in normal and von Willebrand disease swine. Proc Natl Acad Sci U S A. 1982; 79(16):5076-9. PMC: 346830. DOI: 10.1073/pnas.79.16.5076. View

Turitto V, Weiss H, ZIMMERMAN T, Sussman I . Factor VIII/von Willebrand factor in subendothelium mediates platelet adhesion. Blood. 1985; 65(4):823-31. View

Sporn L, Chavin S, Marder V, Wagner D . Biosynthesis of von Willebrand protein by human megakaryocytes. J Clin Invest. 1985; 76(3):1102-6. PMC: 423998. DOI: 10.1172/JCI112064. View

Rudek Z, Kwiatkowska L . The possibility of detecting fetal lymphocytes in the maternal blood of the domestic pig, Sus scrofa. Cytogenet Cell Genet. 1983; 36(3):580-3. DOI: 10.1159/000131976. View

Brinkhous K, Sandberg H, Garris J, Mattsson C, Palm M, Griggs T . Purified human factor VIII procoagulant protein: comparative hemostatic response after infusions into hemophilic and von Willebrand disease dogs. Proc Natl Acad Sci U S A. 1985; 82(24):8752-6. PMC: 391515. DOI: 10.1073/pnas.82.24.8752. View

Gralnick H, Rick M, McKeown L, Williams S, Parker R, Maisonneuve P . Platelet von Willebrand factor: an important determinant of the bleeding time in type I von Willebrand's disease. Blood. 1986; 68(1):58-61. View

BOWIE E, Solberg Jr L, Fass D, Johnson C, Knutson G, Stewart M . Transplantation of normal bone marrow into a pig with severe von Willebrand's disease. J Clin Invest. 1986; 78(1):26-30. PMC: 329526. DOI: 10.1172/JCI112560. View

Nichols T, Bellinger D, Johnson T, Lamb M, Griggs T . von Willebrand's disease prevents occlusive thrombosis in stenosed and injured porcine coronary arteries. Circ Res. 1986; 59(1):15-26. DOI: 10.1161/01.res.59.1.15. View

10.

Cramer E, Caen J, Drouet L, BRETON-GORIUS J . Absence of tubular structures and immunolabeling for von Willebrand factor in the platelet alpha-granules from porcine von Willebrand disease. Blood. 1986; 68(3):774-8. View

11.

Wu Q, Drouet L, CARRIER J, Rothschild C, Berard M, Rouault C . Differential distribution of von Willebrand factor in endothelial cells. Comparison between normal pigs and pigs with von Willebrand disease. Arteriosclerosis. 1987; 7(1):47-54. DOI: 10.1161/01.atv.7.1.47. View

12.

Mannucci P, Moia M, Rebulla P, Altieri D, Monteagudo J, Castillo R . Correction of the bleeding time in treated patients with severe von Willebrand disease is not solely dependent on the normal multimeric structure of plasma von Willebrand factor. Am J Hematol. 1987; 25(1):55-65. DOI: 10.1002/ajh.2830250106. View

13.

Bellinger D, Nichols T, Read M, Reddick R, Lamb M, Brinkhous K . Prevention of occlusive coronary artery thrombosis by a murine monoclonal antibody to porcine von Willebrand factor. Proc Natl Acad Sci U S A. 1987; 84(22):8100-4. PMC: 299486. DOI: 10.1073/pnas.84.22.8100. View

14.

Mannucci P, Lombardi R, Castaman G, Dent J, Lattuada A, Rodeghiero F . von Willebrand disease "Vicenza" with larger-than-normal (supranormal) von Willebrand factor multimers. Blood. 1988; 71(1):65-70. View

15.

Renard C, Kristensen B, Gautschi C, Hruban V, Fredholm M, Vaiman M . Joint report of the first international comparison test on swine lymphocyte alloantigens (SLA). Anim Genet. 1988; 19(1):63-72. DOI: 10.1111/j.1365-2052.1988.tb00792.x. View

16.

Koedam J, Meijers J, Sixma J, Bouma B . Inactivation of human factor VIII by activated protein C. Cofactor activity of protein S and protective effect of von Willebrand factor. J Clin Invest. 1988; 82(4):1236-43. PMC: 442674. DOI: 10.1172/JCI113721. View

17.

Bahnak B, Wu Q, Coulombel L, Assouline Z, Kerbiriou-Nabias D, Pietu G . Expression of von Willebrand factor in porcine vessels: heterogeneity at the level of von Willebrand factor mRNA. J Cell Physiol. 1989; 138(2):305-10. DOI: 10.1002/jcp.1041380212. View

18.

Smiley R, Tittley P, Rock G . Studies on the prolonged bleeding time in von Willebrand's disease. Thromb Res. 1989; 53(5):417-26. DOI: 10.1016/0049-3848(89)90196-5. View

19.

Read M, Smith S, Lamb M, Brinkhous K . Role of botrocetin in platelet agglutination: formation of an activated complex of botrocetin and von Willebrand factor. Blood. 1989; 74(3):1031-5. View

20.

Vaiman M . Histocompatibility systems in pigs. Prog Vet Microbiol Immunol. 1988; 4:108-33. View