Factor XIII transglutaminase supports the resolution of mucosal damage in experimental colitis

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Andersson, Christina ^a   Kvist, Peter H ^a   McElhinney, Kathryn ^b   Baylis, Richard ^b   Gram, Luise K ^a   Pelzer, Hermann ^a   Lauritzen, Brian ^a   Holm, Thomas L ^a   Hogan, Simon ^b   Wu, David ^b   Turpin, Brian ^b   Miller, Whitney ^b   Palumbo, Joseph S ^b  

^a NOVO NORDISK A S   (Denmark)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEXTRAN SULFATE; ENZYME PRECURSOR; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; RECOMBINANT BLOOD CLOTTING FACTOR 8; TRANSGLUTAMINASE FACTOR XIII; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; BLOOD CLOTTING FACTOR 13; FACTOR XIII SUBUNIT A; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL TRANSLOCATION; CONTROLLED STUDY; DIARRHEA; DISEASE SEVERITY; DRUG HALF LIFE; DRUG MECHANISM; ENZYME SUBUNIT; EXPERIMENTAL COLITIS; HISTOPATHOLOGY; INTESTINAL BLEEDING; INTESTINE FLORA; INTESTINE ULCER; MALE; MICROSCOPY; MOUSE; MUCOSAL DISEASE; NONHUMAN; OUTCOME ASSESSMENT; PROTEIN BLOOD LEVEL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; SENSITIVITY ANALYSIS; WEIGHT REDUCTION; ANIMAL; BLOOD; C57BL MOUSE; CHEMICALLY INDUCED; COLITIS; COLON; DISEASE MODEL; GENETICS; INTESTINE MUCOSA; KNOCKOUT MOUSE; PATHOLOGY; WOUND HEALING;

MUS;

ANIMALS; BIOMARKERS; COLITIS; COLON; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; FACTOR XIII; INTESTINAL MUCOSA; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECOMBINANT PROTEINS; WOUND HEALING;

EID: 84939145678     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128113     Document Type: Article

References (54)

1. Ichinose A. Factor XIII is a key molecule at the intersection of coagulation and fibrinolysis as well as inflammation and infection control. Int J Hematol. 2012; 95(4):362-70. Epub 2012 Apr 5. doi:10.1007/s12185-012-1064-3 PMID: 22477542.
2. Lorand L. Factor XIII: Structure, activation, and interactions with fibrinogen and fibrin. Ann N Y Acad Sci. 2001; 936:291-311. PMID: 11460485.
3. Soendergaard C, Kvist PH, Seidelin JB, Nielsen OH. Tissue-regenerating functions of coagulation factor XIII. Journal of thrombosis and haemostasis: JTH. 2013; 11(5):806-16. Epub 2013/02/15. doi:10.1111/jth.12169 PMID: 23406195.
4. Anwar R, Miloszewski KJ. Factor XIII deficiency. British journal of haematology. 1999; 107(3):468-84. Epub 1999/12/03. PMID: 10583246.
5. Board PG, Losowsky MS, Miloszewski KJ. Factor XIII: Inherited and acquired deficiency. Blood reviews. 1993; 7(4):229-42. Epub 1993/12/01. PMID: 8130686.
6. Schroeder V, Durrer D, Meili E, Schubiger G, Kohler HP. Congenital factor XIII deficiency in Switzerland: from the worldwide first case in 1960 to its molecular characterisation in 2005. Swiss medical weekly. 2007; 137(19-20):272-8. Epub 2007/06/28. doi:2007/19/smw-11756. PMID: 17594539.
7. Ivaskevicius V, Seitz R, Kohler HP, Schroeder V, Muszbek L, Ariens RA, et al. International registry on factor XIII deficiency: A basis formed mostly on European data. Thrombosis and haemostasis. 2007; 97 (6):914-21. Epub 2007/06/06. PMID: 17549292.
8. Inbal A, Lubetsky A, Krapp T, Castel D, Shaish A, Dickneitte G, et al. Impaired wound healing in factor XIII deficient mice. Thromb Haemost. 2005; 94(2):432-7. PMID: 16113836.
9. Tsujimoto I, Moriya K, Sakai K, Dickneite G, Sakai T. Critical role of factor XIII in the initial stages of carbon tetrachloride-induced adult liver remodeling. Am J Pathol. 2011; 179(6):3011-9. Epub 2011 Oct 19. doi:10.1016/j.ajpath.2011.08.037 PMID: 22019897.
10. Souri M, Koseki-Kuno S, Takeda N, Yamakawa M, Takeishi Y, Degen JL, et al. Male-specific cardiac pathologies in mice lacking either the A or B subunit of factor XIII. Thromb Haemost. 2008; 99(2):401- 8. doi:10.1160/TH07-10-0599 PMID: 18278192.
11. Nahrendorf M, Hu K, Frantz S, Jaffer FA, Tung CH, Hiller KH, et al. Factor XIII deficiency causes cardiac rupture, impairs wound healing, and aggravates cardiac remodeling in mice with myocardial infarction. Circulation. 2006; 113(9):1196-202. Epub 2006 Feb 27. PMID: 16505171.
12. Zaets SB, Xu DZ, Lu Q, Feketova E, Berezina TL, Gruda M, et al. Recombinant factor XIII diminishes multiple organ dysfunction in rats caused by gut ischemia-reperfusion injury. Shock. 2009; 31(6):621- 6. doi:10.1097/SHK.0b013e31818bbe21 PMID: 18948851.
13. Zaets SB, Xu DZ, Lu Q, Feketova E, Berezina TL, Malinina IV, et al. Recombinant factor XIII mitigates hemorrhagic shock-induced organ dysfunction. J Surg Res. 2011; 166(2):e135-42. Epub 2010 Dec 31. doi:10.1016/j.jss.2010.12.001 PMID: 21276979.
14. Loof TG, Morgelin M, Johansson L, Oehmcke S, Olin AI, Dickneite G, et al. Coagulation, an ancestral serine protease cascade, exerts a novel function in early immune defense. Blood. 2011; 118(9):2589- 98. Epub 011 May 25. doi:10.1182/blood-2011-02-337568 PMID: 21613262.
15. Degen JL, Bugge TH, Goguen JD. Fibrin and fibrinolysis in infection and host defense. J Thromb Haemost. 2007; 5(Suppl 1):24-31. PMID: 17635705.
16. Adams RA, Bauer J, Flick MJ, Sikorski SL, Nuriel T, Lassmann H, et al. The fibrin-derived gamma377- 395 peptide inhibits microglia activation and suppresses relapsing paralysis in central nervous system autoimmune disease. The Journal of experimental medicine. 2007; 204(3):571-82. Epub 2007/03/07. doi:10.1084/jem.20061931 PMID: 17339406; PubMed Central PMCID: PMCPmc2137908.
17. Davalos D, Ryu JK, Merlini M, Baeten KM, Le-Moan N, Petersen MA, et al. Fibrinogen-induced perivascular microglial clustering is required for the development of axonal damage in neuroinflammation. Nat Commun. 2012; 3:1227.doi:10.1038/ncomms2230 PMID: 23187627.
18. Flick MJ, Du X, Witte DP, Jirouskova M, Soloviev DA, Busuttil SJ, et al. Leukocyte engagement of fibrin (ogen) via the integrin receptor alphaMbeta2/Mac-1 is critical for host inflammatory response in vivo. J Clin Invest. 2004; 113(11):1596-606. PMID: 15173886.
19. Steinbrecher KA, Horowitz NA, Blevins EA, Barney KA, Shaw MA, Harmel-Laws E, et al. Colitis-associated cancer is dependent on the interplay between the hemostatic and inflammatory systems and supported by integrin alpha(M)beta(2) engagement of fibrinogen. Cancer Res. 2010; 70(7):2634-43. Epub 010 Mar 16. doi:10.1158/0008-5472.CAN-09-3465 PMID: 20233870.
20. Flick MJ, Du X, Prasad JM, Raghu H, Palumbo JS, Smeds E, et al. Genetic elimination of the binding motif on fibrinogen for the S. aureus virulence factor ClfA improves host survival in septicemia. Blood. 2013; 121(10):1783-94. Epub 2013/01/10. doi:10.1182/blood-2012-09-453894 PMID: 23299312; PubMed Central PMCID: PMCPmc3591798.
21. Inbal A, Dardik R. Role of coagulation factor XIII (FXIII) in angiogenesis and tissue repair. Pathophysiol Haemost Thromb. 2006; 35(1-2):162-5. PMID: 17565237.
22. Richardson VR, Cordell P, Standeven KF, Carter AM. Substrates of Factor XIII-A: Roles in thrombosis and wound healing. Clin Sci (Lond). 2013; 124(3):123-37. doi:10.1042/CS20120233 PMID: 23075332.
23. Dardik R, Leor J, Skutelsky E, Castel D, Holbova R, Schiby G, et al. Evaluation of the pro-angiogenic effect of factor XIII in heterotopic mouse heart allografts and FXIII-deficient mice. Thromb Haemost. 2006; 95(3):546-50. PMID: 16525585.
24. Dardik R, Loscalzo J, Eskaraev R, Inbal A. Molecular mechanisms underlying the proangiogenic effect of factor XIII. Arterioscler Thromb Vasc Biol. 2005; 25(3):526-32. Epub 2004 Dec 23. PMID: 15618543.
25. Bagoly Z, Katona E, Muszbek L. Factor XIII and inflammatory cells. Thromb Res. 2012; 129(Suppl 2): S77-S81. Epub 2012 Mar 15. doi:10.1016/j.thromres.2012.02.040 PMID: 22425216.
26. Chamouard P, Grunebaum L, Wiesel ML, Sibilia J, Coumaros G, Wittersheim C, et al. Significance of diminished factor XIII in Crohn's disease. Am J Gastroenterol. 1998; 93(4):610-4. PMID: 9576457.
27. Chiarantini E, Valanzano R, Liotta AA, Cellai AP, Fedi S, Ilari I, et al. Hemostatic abnormalities in inflammatory bowel disease. Thromb Res. 1996; 82(2):137-46. PMID: 9163067.
28. D'Argenio G, Cosenza V, Riegler G, Della-Valle N, Deritis F, Mazzacca G. Serum transglutaminase correlates with endoscopic and histopathologic grading in patients with ulcerative colitis. Dig Dis Sci. 2001; 46(3):649-57. PMID: 11318547.
29. Linskens RK, van-Bodegraven AA, Schoorl M, Tuynman HA, Bartels P. Predictive value of inflammatory and coagulation parameters in the course of severe ulcerative colitis. Dig Dis Sci. 2001; 46(3):644- 8. PMID: 11318546.
30. Lorenz R, Heinmuller M, Classen M, Tornieporth N, Gain T. Substitution of factor XIII: A therapeutic approach to ulcerative colitis. Haemostasis. 1991; 21(1):5-9. PMID: 1677916.
31. Lorenz R, Born P, Olbert P, Classen M. Factor XIII substitution in ulcerative colitis. Lancet. 1995; 345 (8947):449-50. PMID: 7853965.
32. Lorenz R, Olbert P, Born P. Factor XIII in chronic inflammatory bowel diseases. Semin Thromb Hemost. 1996; 22(5):451-5. PMID: 8989830.
33. Suzuki R, Toda H, Takamura Y. Dynamics of blood coagulation factor XIII in ulcerative colitis and preliminary study of the factor XIII concentrate. Blut. 1989; 59(2):162-4. PMID: 2765674.
34. D'Argenio G, Grossman A, Cosenza V, Valle ND, Mazzacca G, Bishop PD. Recombinant factor XIII improves established experimental colitis in rats. Dig Dis Sci. 2000; 45(5):987-97. PMID: 10795765.
35. Ponce R, Armstrong K, Andrews K, Hensler J, Waggie K, Heffernan J, et al. Safety of recombinant human factor XIII in a cynomolgus monkey model of extracorporeal blood circulation. Toxicol Pathol. 2005; 33(6):702-10. PMID: 16243775.
36. Ponce RA, Visich JE, Heffernan JK, Lewis KB, Pederson S, Lebel E, et al. Preclinical safety and pharmacokinetics of recombinant human factor XIII. Toxicol Pathol. 2005; 33(4):495-506. PMID: 16036868.
37. Drew AF, Kaufman AH, Kombrinck KW, Danton MJ, Daugherty CC, Degen JL, et al. Ligneous conjunctivitis in plasminogen-deficient mice. Blood. 1998; 91(5):1616-24. PMID: 9473227.
38. Steinbrecher KA, Harmel-Laws E, Sitcheran R, Baldwin AS. Loss of epithelial RelA results in deregulated intestinal proliferative/apoptotic homeostasis and susceptibility to inflammation. J Immunol. 2008; 180(4):2588-99. PMID: 18250470.
39. Turpin B, Miller W, Rosenfeldt L, Kombrinck K, Flick MJ, Steinbrecher KA, et al. Thrombin drives tumorigenesis in colitis-associated colon cancer. Cancer research. 2014; 74(11):3020-30. Epub 2014/04/09. doi:10.1158/0008-5472.can-13-3276 PMID: 24710407.
40. Reber SO, Obermeier F, Straub RH, Falk W, Neumann ID. Chronic intermittent psychosocial stress (social defeat/overcrowding) in mice increases the severity of an acute DSS-induced colitis and impairs regeneration. Endocrinology. 2006; 147(10):4968-76. Epub 2006 Jun 22. PMID: 16794011.
41. Xu Y, Hunt NH, Bao S. The effect of restraint stress on experimental colitis is IFN-gamma independent. J Neuroimmunol. 2008; 200(1-2):53-61. Epub 2008 Jul 27. doi:10.1016/j.jneuroim.2008.05.018 PMID: 18715655.
42. D'Argenio G, Calvani M, Della-Valle N, Cosenza V, Di-Matteo G, Giorgio P, et al. Differential expression of multiple transglutaminases in human colon: Impaired keratinocyte transglutaminase expression in ulcerative colitis. Gut. 2005; 54(4):496-502. Epub 2005/03/09. doi:10.1136/gut.2004.049411 PMID: 15753534; PubMed Central PMCID: PMCPmc1774462.
43. Kasahara K, Souri M, Kaneda M, Miki T, Yamamoto N, Ichinose A. Impaired clot retraction in factor XIII A subunit-deficient mice. Blood. 2010; 115(6):1277-9. Epub 2009 Dec 8. doi:10.1182/blood-2009-06-227645 PMID: 19996413.
44. Aleman MM, Byrnes JR, Wang JG, Tran R, Lam WA, Di Paola J, et al. Factor XIII activity mediates red blood cell retention in venous thrombi. The Journal of clinical investigation. 2014; 124(8):3590-600. Epub 2014/07/02. doi:10.1172/jci75386 PMID: 24983320; PubMed Central PMCID: PMCPmc4109540.
45. Anthoni C, Russell J, Wood KC, Stokes KY, Vowinkel T, Kirchhofer D, et al. Tissue factor: A mediator of inflammatory cell recruitment, tissue injury, and thrombus formation in experimental colitis. J Exp Med. 2007; 204(7):1595-601. Epub 2007 Jun 11. PMID: 17562818.
46. Vowinkel T, Wood KC, Stokes KY, Russell J, Tailor A, Anthoni C, et al. Mechanisms of platelet and leukocyte recruitment in experimental colitis. Am J Physiol Gastrointest Liver Physiol. 2007; 293(5): G1054-60. Epub 2007 Sep 20. PMID: 17884975.
47. Serrano K, Devine DV. Intracellular factor XIII crosslinks platelet cytoskeletal elements upon platelet activation. Thromb Haemost. 2002; 88(2):315-20. PMID: 12195706.
48. AbdAlla S, Lother H, Langer A, el-Faramawy Y, Quitterer U. Factor XIIIA transglutaminase crosslinks AT1 receptor dimers of monocytes at the onset of atherosclerosis. Cell. 2004; 119(3):343-54. PMID: 15507206.
49. Sarvary A, Szucs S, Balogh I, Becsky A, Bardos H, Kavai M, et al. Possible role of factor XIII subunit A in Fcgamma and complement receptor-mediated phagocytosis. Cell Immunol. 2004; 228(2):81-90. PMID: 15219459.
50. Saleh M, Trinchieri G. Innate immune mechanisms of colitis and colitis-associated colorectal cancer. Nat Rev Immunol. 2011; 11(1):9-20. Epub 2010 Dec 10. doi:10.1038/nri2891 PMID: 21151034.
51. Nagalingam NA, Lynch SV. Role of the microbiota in inflammatory bowel diseases. Inflamm Bowel Dis. 2012; 18(5):968-84. doi:10.1002/ibd.21866 Epub 2011 Sep 20. PMID: 21936031.
52. Mullarky IK, Szaba FM, Berggren KN, Parent MA, Kummer LW, Chen W, et al. Infection-stimulated fibrin deposition controls hemorrhage and limits hepatic bacterial growth during listeriosis. Infect Immun. 2005; 73(7):3888-95. PMID: 15972474.
53. Luo D, Szaba FM, Kummer LW, Plow EF, Mackman N, Gailani D, et al. Protective roles for fibrin, tissue factor, plasminogen activator inhibitor-1, and thrombin activatable fibrinolysis inhibitor, but not factor XI, during defense against the gram-negative bacterium Yersinia enterocolitica. J Immunol. 2011; 187 (4):1866-76. Epub 2011 Jul 1. doi:10.4049/jimmunol.1101094 PMID: 21724997.
54. Sun H, Wang X, Degen JL, Ginsburg D. Reduced thrombin generation increases host susceptibility to group A streptococcal infection. Blood. 2009; 113(6):1358-64. doi:10.182/blood-2008-07-170506 Epub 2008 Dec 3. PMID: 19056689.