Platelet activation and platelet-leukocyte aggregation elicited in experimental colitis are mediated by interleukin-6

Inflammatory Bowel Diseases

Volumn 20, Issue 2, 2014, Pages 353-362

  Yan, Serena L S ^a   Russell, Janice ^a   Granger, D Neil ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Dextran sodium sulfate; Inflammatory bowel disease; Thrombocytosis; Thrombosis

Indexed keywords

DEXTRAN SULFATE; INTERLEUKIN 6; INTERLEUKIN-6, MOUSE; RECOMBINANT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIOLE; ARTICLE; BLOOD CLOTTING; CONTROLLED STUDY; EXPERIMENTAL COLITIS; LEUKOCYTE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE FUNCTION; WILD TYPE; ANIMAL; C57BL MOUSE; CELL ADHESION; COLITIS; DRUG EFFECTS; INFLAMMATORY BOWEL DISEASES; INTRAVENOUS DRUG ADMINISTRATION; METABOLISM; PATHOLOGY; TREATMENT OUTCOME;

ANIMALS; CELL ADHESION; COLITIS; INFLAMMATORY BOWEL DISEASES; INFUSIONS, INTRAVENOUS; INTERLEUKIN-6; LEUKOCYTES; MALE; MICE; MICE, INBRED C57BL; PLATELET ACTIVATION; RECOMBINANT PROTEINS; TREATMENT OUTCOME;

EID: 84893740171     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/01.MIB.0000440614.83703.84     Document Type: Article

References (41)

1. Danese S, Papa A, Saibeni S, et al. Inflammation and coagulation in inflammatory bowel disease: the clot thickens. Am J Gastroenterol. 2007;102:174-186.
2. Irving PM, Pasi KL, Rampton DS. Thrombosis and inflammatory bowel disease. Clin Gastroenterol Hepatol. 2005;3:617-628.
3. Yoshida H, Granger DN Inflammatory bowel disease: a paradigm for the link between coagulation and inflammation. Inflamm Bowel Dis. 2009;15: 1245-1255.
4. Anthoni C, Russell J, Wood KC, et al. Tissue factor: a mediator of inflammatory cell recruitment, tissue injury, and thrombus formation in experimental colitis. J Exp Med. 2007;204:1595-1601.
5. Yoshida H, Russell J, Senchenkova EY, et al. Interleukin-1beta mediates the extra-intestinal thrombosis associated with experimental colitis. Am J Pathol. 2010;177:2774-2781.
6. Yoshida H, Yilmaz CE, Granger DN. Role of tumor necrosis factor-alpha in the extraintestinal thrombosis associated with colonic inflammation. Inflamm Bowel Dis. 2011;17:2217-2223.
7. Danese S, Semeraro S, Papa A, et al. Extraintestinal manifestations in inflammatory bowel disease. World J Gastroenterol. 2005;11:7227-7236.
8. Esmon CT The impact of the inflammatory response on coagulation. Thromb Res. 2004;114:321-327.
9. Danese S, Scaldaferri F, Papa A, et al. Platelets: new players in the mucosal scenario of inflammatory bowel disease. Eur Rev Med Pharmacol Sci. 2004;8:193-198.
10. Collins CE, Rampton DS, Rogers J, et al. Platelet aggregation and neutrophil sequestration in the mesenteric circulation in inflammatory bowel disease. Eur J Gastroenterol Hepatol. 1997;9:1213-1217.
11. Harries AD, Fitzsimons E, Fifield R, et al. Platelet count: a simple measure of activity in Crohn's disease. Br Med J (Clin Res Ed). 1983;286:1476.
12. Irving PM, MaceyMG, Shah U, et al. Formation of platelet-leukocyte aggregates in inflammatory bowel disease. Inflamm Bowel Dis. 2004;10:361-372.
13. Senchenkova EY, Komoto S, Russell J, et al. Interleukin-6 mediates the platelet abnormalities and thrombogenesis associated with experimental colitis. Am J Pathol. 2013;183:173-181.
14. Yan SL, Russell J, Harris NR, et al. Platelet abnormalities during colonic inflammation. Inflamm Bowel Dis. 2013;19:1245-1253.
15. Levi M, van der Poll T. Two-way interactions between inflammation and coagulation. Trends Cardiovasc Med. 2005;15:254-259.
16. Danese S, Motte L, Fiocchi C. Platelets in inflammatory bowel disease: clinical, pathogenic, and therapeutic implications. Am J Gastroenterol. 2004;99:938-945.
17. Reinecker HC, Steffen M, Witthoeft T, et al. Enhanced secretion of tumour necrosis factor-alpha, IL-6, and IL-1 beta by isolated lamina propria mononuclear cells from patients with ulcerative colitis and Crohn's disease. Clin Exp Immunol. 1993;94:174-181.
18. Ishibashi T, Kimura H, Uchida T, et al. Human interleukin 6 is a direct promoter of maturation of megakaryocytes in vitro. Proc Natl Acad Sci U S A. 1989;86:5953-5957.
19. Mitsuyama K, Matsumoto S, Masuda J, et al. Therapeutic strategies for targeting the IL-6/STAT3 cytokine signaling pathway in inflammatory bowel disease. Anticancer Res. 2007;27:3749-3756.
20. Mudter J, Neurath MF. Il-6 signaling in inflammatory bowel disease: pathophysiological role and clinical relevance. Inflamm Bowel Dis. 2007;13:1016-1023.
21. Bergmeier W, Schulte V, Brockhoff G, et al. Flow cytometric detection of activated mouse integrin alphaIIbbeta3 with a novel monoclonal antibody. Cytometry. 2002;48:80-86.
22. Ault KA, Knowles C. In vivo biotinylation demonstrates that reticulated platelets are the youngest platelets in circulation. Exp Hematol. 1995;23: 996-1001.
23. Robinson M, Machin S, Mackie I, et al. In vivo biotinylation studies: specificity of labelling of reticulated platelets by thiazole orange and mepacrine. Br J Haematol. 2000;108:859-864.
24. Rumbaut RE, Slaff DW, Burns AR. Microvascular thrombosis models in venules and arterioles in vivo. Microcirculation. 2005;12:259-274.
25. Andoh A, Yoshida T, Yagi Y, et al. Increased aggregation response of platelets in patients with inflammatory bowel disease. J Gastroenterol. 2006;41:47-54.
26. Atreya R, Neurath MF. Involvement of IL-6 in the pathogenesis of inflammatory bowel disease and colon cancer. Clin Rev Allergy Immunol. 2005; 28:187-196.
27. Collins CE, Cahill MR, Newland AC, et al. Platelets circulate in an activated state in inflammatory bowel disease. Gastroenterology. 1994; 106:840-845.
28. Collins CE, Rampton DS. Review article: platelets in inflammatory bowel disease-pathogenetic role and therapeutic implications. Aliment Pharmacol Ther. 1997;11:237-247.
29. Heits F, Stahl M, Ludwig D, et al. Elevated serum thrombopoietin and interleukin-6 concentrations in thrombocytosis associated with inflammatory bowel disease. J Interferon Cytokine Res. 1999;19:757-760.
30. Webberley MJ, Hart MT, Melikian V. Thromboembolism in inflammatory bowel disease: role of platelets. Gut. 1993;34:247-251.
31. Asano S, Okano A, Ozawa K, et al. In vivo effects of recombinant human interleukin-6 in primates: stimulated production of platelets. Blood. 1990; 75:1602-1605.
32. Ishibashi T, Kimura H, Shikama Y, et al. Interleukin-6 is a potent thrombopoietic factor in vivo in mice. Blood. 1989;74:1241-1244.
33. Kaser A, Brandacher G, Steurer W, et al. Interleukin-6 stimulates thrombopoiesis through thrombopoietin: role in inflammatory thrombocytosis. Blood. 2001;98:2720-2725.
34. Thattaliyath B, Cykowski M, Jagadeeswaran P. Young thrombocytes initiate the formation of arterial in zebrafish. Blood. 2005;106:118-124.
35. Pamuk GE, Vural O, Turgut B, et al. Increased circulating plateletneutrophil, platelet-monocyte complexes, and platelet activation in patients with ulcerative colitis: a comparative study. Am J Hematol. 2006;81: 753-759.
36. Huo Y, Schober A, Forlow SB, et al. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat Med. 2003;9:61-67.
37. Nagata K, Tsuji T, Todoroki N, et al. Activated platelets induce superoxide anion release by monocytes and neutrophils through P-selectin (CD62). J Immunol. 1993;151:3267-3273.
38. Polanowska-Grabowska R, Wallace K, Field JJ, et al. P-selectin-mediated platelet-neutrophil aggregate formation activates neutrophils in mouse and human sickle cell disease. Arterioscler Thromb Vasc Biol. 2010;30: 2392-2399.
39. Zarbock A, Singbartl K, Ley K. Complete reversal of acid-induced acute lung injury by blocking of platelet-neutrophil aggregation. J Clin Invest. 2006;116:3211-3219.
40. Langer HF, Choi EY, Zhou H, et al. Platelets contribute to the pathogenesis of experimental autoimmune encephalomyelitis. Circ Res. 2012;110:1202-1210.
41. von Bruhl ML, Stark K, Steinhart A, et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med. 2012;209:819-835.