A high-fat diet delays plasmin generation in a thrombomodulin-dependent manner in mice.


Journal

Blood
ISSN: 1528-0020
Titre abrégé: Blood
Pays: United States
ID NLM: 7603509

Informations de publication

Date de publication:
07 05 2020
Historique:
received: 21 11 2019
accepted: 02 02 2020
pubmed: 22 4 2020
medline: 1 1 2021
entrez: 22 4 2020
Statut: ppublish

Résumé

Obesity is a prevalent prothrombotic risk factor marked by enhanced fibrin formation and suppressed fibrinolysis. Fibrin both promotes thrombotic events and drives obesity pathophysiology, but a lack of essential analytical tools has left fibrinolytic mechanisms affected by obesity poorly defined. Using a plasmin-specific fluorogenic substrate, we developed a plasmin generation (PG) assay for mouse plasma that is sensitive to tissue plasminogen activator, α2-antiplasmin, active plasminogen activator inhibitor (PAI-1), and fibrin formation, but not fibrin crosslinking. Compared with plasmas from mice fed a control diet, plasmas from mice fed a high-fat diet (HFD) showed delayed PG and reduced PG velocity. Concurrent to impaired PG, HFD also enhanced thrombin generation (TG). The collective impact of abnormal TG and PG in HFD-fed mice produced normal fibrin formation kinetics but delayed fibrinolysis. Functional and proteomic analyses determined that delayed PG in HFD-fed mice was not due to altered levels of plasminogen, α2-antiplasmin, or fibrinogen. Changes in PG were also not explained by elevated PAI-1 because active PAI-1 concentrations required to inhibit the PG assay were 100-fold higher than circulating concentrations in mice. HFD-fed mice had increased circulating thrombomodulin, and inhibiting thrombomodulin or thrombin-activatable fibrinolysis inhibitor (TAFI) normalized PG, revealing a thrombomodulin- and TAFI-dependent antifibrinolytic mechanism. Integrating kinetic parameters to calculate the metric of TG/PG ratio revealed a quantifiable net shift toward a prothrombotic phenotype in HFD-fed mice. Integrating TG and PG measurements may define a prothrombotic risk factor in diet-induced obesity.

Identifiants

pubmed: 32315384
pii: S0006-4971(20)62051-1
doi: 10.1182/blood.2019004267
pmc: PMC7205812
doi:

Substances chimiques

THBD protein, mouse 0
Thrombomodulin 0
Thrombin EC 3.4.21.5
Fibrinolysin EC 3.4.21.7

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1704-1717

Subventions

Organisme : NHLBI NIH HHS
ID : R61 HL141791
Pays : United States
Organisme : NIEHS NIH HHS
ID : R01 ES017537
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL126974
Pays : United States
Organisme : NHLBI NIH HHS
ID : R33 HL141791
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA211098
Pays : United States
Organisme : NHLBI NIH HHS
ID : U01 HL143403
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK112778
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL055374
Pays : United States

Informations de copyright

© 2020 by The American Society of Hematology.

Références

Immunology. 1996 Jan;87(1):134-40
pubmed: 8666425
J Clin Invest. 2017 Aug 1;127(8):3152-3166
pubmed: 28737512
J Biol Chem. 2000 Jul 28;275(30):22942-7
pubmed: 10801821
Ann N Y Acad Sci. 2000 May;902:315-9
pubmed: 10865855
Blood. 2015 Oct 22;126(17):2047-58
pubmed: 26228483
Diabetes. 2004 Feb;53(2):336-46
pubmed: 14747283
Thromb Haemost. 2003 Mar;89(3):409-19
pubmed: 12624622
Stroke. 2015 Jun;46(6):1690-2
pubmed: 25944320
Crit Care Med. 2008 Mar;36(3):683-9
pubmed: 18431261
Blood. 2007 Nov 1;110(9):3168-75
pubmed: 17644733
Blood. 2013 Jul 4;122(1):134-42
pubmed: 23699598
J Thromb Haemost. 2018 Jun 8;:
pubmed: 29883024
Blood. 1990 Jan 15;75(2):329-36
pubmed: 2153035
Res Pract Thromb Haemost. 2019 Mar 04;3(2):161-172
pubmed: 31011700
Thromb Res. 2009;123(3):537-42
pubmed: 18691743
J Thromb Haemost. 2005 Dec;3(12):2745-53
pubmed: 16359512
Thromb Haemost. 2009 Jan;101(1):165-70
pubmed: 19132204
J Clin Invest. 1998 May 1;101(9):1983-91
pubmed: 9576763
Thromb Haemost. 2001 Jan;85(1):5-11
pubmed: 11204587
Blood Coagul Fibrinolysis. 2002 Dec;13(8):711-4
pubmed: 12441910
J Biochem. 1988 Oct;104(4):628-32
pubmed: 2853710
J Thromb Thrombolysis. 2007 Feb;23(1):41-9
pubmed: 17111204
J Thromb Haemost. 2006 Feb;4(2):403-10
pubmed: 16420573
Stroke. 2013 Jan;44(1):278-86
pubmed: 23111440
Clin Appl Thromb Hemost. 2012 Jun;18(3):289-93
pubmed: 22275395
Obes Rev. 2002 May;3(2):85-101
pubmed: 12120424
Liver Int. 2011 Feb;31(2):176-83
pubmed: 21134109
Eur J Biochem. 1994 Sep 15;224(3):863-71
pubmed: 7523120
Blood. 2019 Jan 17;133(3):193-204
pubmed: 30442679
Cardiovasc Res. 2017 Jul 1;113(9):1046-1054
pubmed: 28472252
TH Open. 2017 Dec 15;1(2):e146-e154
pubmed: 31249920
Thromb Haemost. 2013 Oct;110(4):761-8
pubmed: 24072166
Mol Syst Biol. 2016 Dec 22;12(12):901
pubmed: 28007936
Arterioscler Thromb Vasc Biol. 2002 May 1;22(5):867-73
pubmed: 12006404
Blood. 2010 Jul 8;116(1):113-21
pubmed: 20385790
J Appl Lab Med. 2017 Sep 1;2(2):150-164
pubmed: 32630978
Biochem Biophys Res Commun. 2012 May 4;421(2):335-42
pubmed: 22507986
Obesity (Silver Spring). 2012 Jan;20(1):88-94
pubmed: 21959347
J Biol Chem. 1998 Jan 23;273(4):2127-35
pubmed: 9442053
Thromb Haemost. 1998 Nov;80(5):829-35
pubmed: 9843179
J Biol Chem. 1985 Sep 25;260(21):11581-7
pubmed: 3930479
Atherosclerosis. 2004 Jan;172(1):175-80
pubmed: 14709373
J Clin Invest. 1985 Dec;76(6):2178-81
pubmed: 3001144
Thromb Res. 2013 Jan;131(1):3-11
pubmed: 23158401
Sci Rep. 2017 Aug 7;7(1):6914
pubmed: 28785035
J Clin Invest. 2002 Jan;109(1):101-10
pubmed: 11781355
Blood Rev. 2007 May;21(3):131-42
pubmed: 17208341
Clin Chem. 2016 May;62(5):699-707
pubmed: 26955824
J Biol Chem. 1996 Jul 12;271(28):16603-8
pubmed: 8663147
Thromb Res. 2011 Apr;127(4):317-23
pubmed: 21316746
Thromb Res. 2008;122(4):549-55
pubmed: 18234295
Science. 1993 Jan 1;259(5091):87-91
pubmed: 7678183
Hematology. 2011 Nov;16(6):327-36
pubmed: 22183066
Diabetes Care. 2007 May;30(5):e31-2
pubmed: 17468361
J Exp Med. 1986 Mar 1;163(3):740-5
pubmed: 3753996
Diabetes Care. 2007 May;30(5):1212-8
pubmed: 17277038
Thromb Haemost. 2012 Aug;108(2):311-7
pubmed: 22740053
Am J Pathol. 2010 Jan;176(1):177-86
pubmed: 20008134
Nat Rev Endocrinol. 2019 May;15(5):288-298
pubmed: 30814686
Thromb Haemost. 1997 Jul;78(1):656-60
pubmed: 9198234
Thromb Res. 2007;120(3):439-46
pubmed: 17156827
Proc Natl Acad Sci U S A. 1986 May;83(10):3460-4
pubmed: 3486418
Thromb Res. 2000 May 15;98(4):333-42
pubmed: 10822080
J Thromb Thrombolysis. 2019 Jan;47(1):51-56
pubmed: 30259314
Thromb Haemost. 2003 Mar;89(3):493-8
pubmed: 12624633
Immunology. 2002 Nov;107(3):340-9
pubmed: 12423310
J Thromb Haemost. 2007 Oct;5(10):2079-86
pubmed: 17666016
Semin Thromb Hemost. 2015 Jul;41(5):468-73
pubmed: 26049071
Blood. 2005 May 15;105(10):3910-7
pubmed: 15677570
Anesth Analg. 2012 Feb;114(2):275-85
pubmed: 22104070
J Thromb Haemost. 2006 Nov;4(11):2470-7
pubmed: 17002650
Arterioscler Thromb Vasc Biol. 2003 Jan 1;23(1):78-84
pubmed: 12524228
FASEB J. 2017 Jun;31(6):2625-2637
pubmed: 28270519
Thromb Haemost. 2000 Feb;83(2):297-303
pubmed: 10739389
Blood. 1992 Sep 1;80(5):1254-63
pubmed: 1325211
Blood. 2000 May 1;95(9):2855-9
pubmed: 10779431
J Thromb Haemost. 2008 Aug;6(8):1296-303
pubmed: 18507721
Thromb Res. 2009;123 Suppl 4:S46-9
pubmed: 19303504
Adv Med Sci. 2010;55(2):196-203
pubmed: 20439183
J Thromb Haemost. 2010 Apr;8(4):759-65
pubmed: 20102484
J Biol Chem. 1998 Oct 16;273(42):27176-81
pubmed: 9765237
J Clin Endocrinol Metab. 2002 Feb;87(2):660-5
pubmed: 11836301

Auteurs

Adam Miszta (A)

Department of Pathology and Laboratory Medicine and UNC Blood Research Center, University of North Carolina at Chapel Hill, Chapel Hill, NC.
Synapse Research Institute, Maastricht, The Netherlands.
Department of Biochemistry, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University Medical Center, Maastricht, The Netherlands.

Anna K Kopec (AK)

Department of Pathobiology and Diagnostic Investigation, Institute for Integrative Toxicology, Michigan State University, East Lansing, MI.

Asmita Pant (A)

Department of Pathobiology and Diagnostic Investigation, Institute for Integrative Toxicology, Michigan State University, East Lansing, MI.

Lori A Holle (LA)

Department of Pathology and Laboratory Medicine and UNC Blood Research Center, University of North Carolina at Chapel Hill, Chapel Hill, NC.

James R Byrnes (JR)

Department of Pathology and Laboratory Medicine and UNC Blood Research Center, University of North Carolina at Chapel Hill, Chapel Hill, NC.

Daniel A Lawrence (DA)

Department of Internal Medicine, University of Michigan Medical School, Ann Arbor, MI; and.

Kirk C Hansen (KC)

Department of Biochemistry and Molecular Genetics, University of Colorado, Denver, CO.

Matthew J Flick (MJ)

Department of Pathology and Laboratory Medicine and UNC Blood Research Center, University of North Carolina at Chapel Hill, Chapel Hill, NC.

James P Luyendyk (JP)

Department of Pathobiology and Diagnostic Investigation, Institute for Integrative Toxicology, Michigan State University, East Lansing, MI.

Bas de Laat (B)

Synapse Research Institute, Maastricht, The Netherlands.
Department of Biochemistry, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University Medical Center, Maastricht, The Netherlands.

Alisa S Wolberg (AS)

Department of Pathology and Laboratory Medicine and UNC Blood Research Center, University of North Carolina at Chapel Hill, Chapel Hill, NC.

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