Characterization and Visualization of Murine Coagulation Factor VIII-producing Cells in Vivo

Overview

Journal Sci Rep

Specialty Science

Date 2021 Jul 22

PMID 34290295

Citations 9

Authors

Morisada Hayakawa

Asuka Sakata

Hiroko Hayakawa

Hikari Matsumoto

Takafumi Hiramoto

Yuji Kashiwakura

Nemekhbayar Baatartsogt

Noriyoshi Fukushima

Yoichi Sakata

Katsue Suzuki-Inoue

Tsukasa Ohmori

Affiliations

Soon will be listed here.

Abstract

Coagulation factors are produced from hepatocytes, whereas production of coagulation factor VIII (FVIII) from primary tissues and cell species is still controversial. Here, we tried to characterize primary FVIII-producing organ and cell species using genetically engineered mice, in which enhanced green fluorescent protein (EGFP) was expressed instead of the F8 gene. EGFP-positive FVIII-producing cells existed only in thin sinusoidal layer of the liver and characterized as CD31, CD146, and lymphatic vascular endothelial hyaluronan receptor 1 (Lyve1). EGFP-positive cells can be clearly distinguished from lymphatic endothelial cells in the expression profile of the podoplanin and C-type lectin-like receptor-2 (CLEC-2). In embryogenesis, EGFP-positive cells began to emerge at E14.5 and subsequently increased according to liver maturation. Furthermore, plasma FVIII could be abolished by crossing F8 conditional deficient mice with Lyve1-Cre mice. In conclusion, in mice, FVIII is only produced from endothelial cells exhibiting CD31, CD146, Lyve1, CLEC-2, and podoplanin in liver sinusoidal endothelial cells.

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References

Ohmori T, Mizukami H, Ozawa K, Sakata Y, Nishimura S . New approaches to gene and cell therapy for hemophilia. J Thromb Haemost. 2015; 13 Suppl 1:S133-42. DOI: 10.1111/jth.12926. View

Everett L, Cleuren A, Khoriaty R, Ginsburg D . Murine coagulation factor VIII is synthesized in endothelial cells. Blood. 2014; 123(24):3697-705. PMC: 4055920. DOI: 10.1182/blood-2014-02-554501. View

Kisanuki Y, Hammer R, Miyazaki J, Williams S, Richardson J, Yanagisawa M . Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev Biol. 2001; 230(2):230-42. DOI: 10.1006/dbio.2000.0106. View

Postic C, Magnuson M . DNA excision in liver by an albumin-Cre transgene occurs progressively with age. Genesis. 2000; 26(2):149-50. DOI: 10.1002/(sici)1526-968x(200002)26:2<149::aid-gene16>3.0.co;2-v. View

Si-Tayeb K, Lemaigre F, Duncan S . Organogenesis and development of the liver. Dev Cell. 2010; 18(2):175-89. DOI: 10.1016/j.devcel.2010.01.011. View

VELTKAMP J, Asfaou E, van de Torren K, van der Does J, VAN Tilburg N, Pauwels E . Extrahepatic factor VIII synthesis. Lung transplants in hemophilic dogs. Transplantation. 1974; 18(1):56-62. DOI: 10.1097/00007890-197407000-00009. View

WEBSTER W, Zukoski C, HUTCHIN P, Reddick R, Mandel S, PENICK G . Plasma factor VIII synthesis and control as revealed by canine organ transplantation. Am J Physiol. 1971; 220(5):1147-54. DOI: 10.1152/ajplegacy.1971.220.5.1147. View

Turner N, Moake J . Factor VIII Is Synthesized in Human Endothelial Cells, Packaged in Weibel-Palade Bodies and Secreted Bound to ULVWF Strings. PLoS One. 2015; 10(10):e0140740. PMC: 4608722. DOI: 10.1371/journal.pone.0140740. View

Chaipan C, Soilleux E, Simpson P, Hofmann H, Gramberg T, Marzi A . DC-SIGN and CLEC-2 mediate human immunodeficiency virus type 1 capture by platelets. J Virol. 2006; 80(18):8951-60. PMC: 1563896. DOI: 10.1128/JVI.00136-06. View

10.

Groth C, Hathaway W, Gustafsson A, Geis W, Putnam C, Bjorken C . Correction of coagulation in the hemophilic dog by transplantation of lymphatic tissue. Surgery. 1974; 75(5):725-33. PMC: 2953375. View

11.

Rosen S, Tiefenbacher S, Robinson M, Huang M, Srimani J, Mackenzie D . Activity of transgene-produced B-domain-deleted factor VIII in human plasma following AAV5 gene therapy. Blood. 2020; 136(22):2524-2534. PMC: 7714098. DOI: 10.1182/blood.2020005683. View

12.

Marchioro T, Hougie C, RAGDE H, EPSTEIN R, Thomas E . Hemophilia: role of organ homografts. Science. 1969; 163(3863):188-90. DOI: 10.1126/science.163.3863.188. View

13.

Poisson J, Lemoinne S, Boulanger C, Durand F, Moreau R, Valla D . Liver sinusoidal endothelial cells: Physiology and role in liver diseases. J Hepatol. 2016; 66(1):212-227. DOI: 10.1016/j.jhep.2016.07.009. View

14.

Aronovich A, Tchorsh D, Katchman H, Eventov-Friedman S, Shezen E, Martinowitz U . Correction of hemophilia as a proof of concept for treatment of monogenic diseases by fetal spleen transplantation. Proc Natl Acad Sci U S A. 2006; 103(50):19075-80. PMC: 1682010. DOI: 10.1073/pnas.0607012103. View

15.

Hollestelle M, Poyck P, Hollestelle J, Marsman H, Mourik J, Gulik T . Extra-hepatic factor VIII expression in porcine fulminant hepatic failure. J Thromb Haemost. 2005; 3(10):2274-80. DOI: 10.1111/j.1538-7836.2005.01543.x. View

16.

Nonaka H, Tanaka M, Suzuki K, Miyajima A . Development of murine hepatic sinusoidal endothelial cells characterized by the expression of hyaluronan receptors. Dev Dyn. 2007; 236(8):2258-67. DOI: 10.1002/dvdy.21227. View

17.

Enzan H, Himeno H, Hiroi M, Kiyoku H, Saibara T, Onishi S . Development of hepatic sinusoidal structure with special reference to the Ito cells. Microsc Res Tech. 1998; 39(4):336-49. DOI: 10.1002/(SICI)1097-0029(19971115)39:4<336::AID-JEMT4>3.0.CO;2-F. View

18.

Terraube V, ODonnell J, Jenkins P . Factor VIII and von Willebrand factor interaction: biological, clinical and therapeutic importance. Haemophilia. 2009; 16(1):3-13. DOI: 10.1111/j.1365-2516.2009.02005.x. View

19.

Olgasi C, Talmon M, Merlin S, Cucci A, Richaud-Patin Y, Ranaldo G . Patient-Specific iPSC-Derived Endothelial Cells Provide Long-Term Phenotypic Correction of Hemophilia A. Stem Cell Reports. 2018; 11(6):1391-1406. PMC: 6294075. DOI: 10.1016/j.stemcr.2018.10.012. View

20.

Ober E, Lemaigre F . Development of the liver: Insights into organ and tissue morphogenesis. J Hepatol. 2018; 68(5):1049-1062. DOI: 10.1016/j.jhep.2018.01.005. View