Interleukin 1 receptor 1 and interleukin 1β regulate megakaryocyte maturation, platelet activation, and transcript profile during inflammation in mice and humans

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 3, 2014, Pages 552-564

  Beaulieu, Lea M ^a   Lin, Elaine ^b   Mick, Eric ^a   Koupenova, Milka ^a,b   Weinberg, Ellen O ^b   Kramer, Carolyn D ^b   Genco, Caroline A ^b   Tanriverdi, Kahraman ^a   Larson, Martin G ^c,d   Benjamin, Emelia J ^b,c   Freedman, Jane E ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BOSTON UNIVERSITY   (United States)

^d Boston University   (United States)

Author keywords

Blood platelets; Diet, high fat; IL1R1 protein, human; Infection; Megakaryocytes

Indexed keywords

BLOOD PLATELETS; DIET, HIGH-FAT; IL1R1 PROTEIN, HUMAN; INFECTION; MEGAKARYOCYTES;

ANIMALS; ATHEROSCLEROSIS; BACTEROIDACEAE INFECTIONS; CELL LINE; COLLAGEN; DIETARY FATS; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; HUMANS; IMIDAZOLES; INFLAMMATION; INTERLEUKIN-1BETA; MAP KINASE SIGNALING SYSTEM; MEGAKARYOCYTES; MICE; MICE, KNOCKOUT; NF-KAPPA B; OBESITY; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PLATELET ACTIVATION; PLATELET ADHESIVENESS; PORPHYROMONAS GINGIVALIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-AKT; PYRIDINES; RECEPTORS, INTERLEUKIN-1 TYPE I; THROMBIN; TRANSCRIPTION, GENETIC;

EID: 84894541867     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.302700     Document Type: Article

References (42)

1. Faber DR, de Groot PG, Visseren FL. Role of adipose tissue in haemostasis, coagulation and fibrinolysis. Obes Rev. 2009;10:554-563
2. Strandberg L, Verdrengh M, Enge M, Andersson N, Amu S, Onnheim K, Benrick A, Brisslert M, Bylund J, Bokarewa M, Nilsson S, Jansson JO. Mice chronically fed high-fat diet have increased mortality and disturbed immune response in sepsis. PLoS One. 2009;4:e7605
3. Zhao JJ, Feng XP, Zhang XL, Le KY. Effect of Porphyromonas gingivalis and Lactobacillus acidophilus on secretion of IL1B, IL6, and IL8 by gingival epithelial cells. Inflammation. 2012;35:1330-1337
4. Ozdemir SP, Kurtis B, Tuter G, Bozkurt S, Gultekin SE, Senguven B, Watanabe K, Aydin S. Effects of low dose doxycycline and bisphosphonate clodronate on gingival levels of matrix metalloproteinase-9, interleukin-1B and alveolar bone loss in diabetic rats. A histomorphometric and immunohistochemical study. J Periodontol. 2012; 83:1172-7782
5. Galea J, Armstrong J, Gadsdon P, Holden H, Francis SE, Holt CM. Interleukin-1 beta in coronary arteries of patients with ischemic heart disease. Arterioscler Thromb Vasc Biol. 1996;16:1000-1006
6. Bhaskar V, Yin J, Mirza AM, Phan D, Vanegas S, Issafras H, Michelson K, Hunter JJ, Kantak SS. Monoclonal antibodies targeting IL-1 beta reduce biomarkers of atherosclerosis in vitro and inhibit atherosclerotic plaque formation in Apolipoprotein E-deficient mice. Atherosclerosis. 2011;216:313-320
7. Chi H, Messas E, Levine RA, Graves DT, Amar S. Interleukin-1 receptor signaling mediates atherosclerosis associated with bacterial exposure and/or a high-fat diet in a murine apolipoprotein E heterozygote model: Pharmacotherapeutic implications. Circulation. 2004;110:1678-1685
8. Kirii H, Niwa T, Yamada Y, Wada H, Saito K, Iwakura Y, Asano M, Moriwaki H, Seishima M. Lack of interleukin-1beta decreases the severity of atherosclerosis in ApoE-deficient mice. Arterioscler Thromb Vasc Biol. 2003;23:656-660
9. Ridker PM, Thuren T, Zalewski A, Libby P. Interleukin-1β inhibition and the prevention of recurrent cardiovascular events: Rationale and design of the Canakinumab Anti-inflammatory Thrombosis Outcomes Study (CANTOS). Am Heart J. 2011;162:597-605
10. Ridker PM, Howard CP, Walter V, Everett B, Libby P, Hensen J, Thuren T, Group CPI. Effects of interleukin-1beta inhibition with canakinumab on hemaglobin A1c, lipids, C-reactive protein, interleukin-6, and fibrinogen: A phase IIb randomized, placebo-controlled trial. Circulation. 2012; 126:2739-2748
11. Alexander MR, Moehle CW, Johnson JL, Yang Z, Lee JK, Jackson CL, Owens GK. Genetic inactivation of IL-1 signaling enhances atherosclerotic plaque instability and reduces outward vessel remodeling in advanced atherosclerosis in mice. J Clin Invest. 2012;122:70-79
12. Dinarello CA. Biologic basis for interleukin-1 in disease. Blood. 1996;87: 2095-2147
13. Nakai S, Aihara K, Hirai Y. Interleukin-1 potentiates granulopoiesis and thrombopoiesis by producing hematopoietic factors in vivo. Life Sci. 1989;45:585-591
14. Kimura H, Ishibashi T, Shikama Y, Okano A, Akiyama Y, Uchida T, Maruyama Y. Interleukin-1 beta (IL-1 beta) induces thrombocytosis in mice: Possible implication of IL-6. Blood. 1990;76:2493-2500
15. Furuya H, Ishibashi R, Wakayama T, Ohguni S, Notsu K, Takagi C, Kato Y. [Effect of subcutaneous administration of interleukin-1 beta on blood platelet count and serum GM-CSF in patients with myelodysplastic syndrome and aplastic anemia]. Rinsho Ketsueki. 1992;33:1172-1177
16. Cobankara V, Oran B, Ozatli D, Haznedaroglu IC, Kosar A, Buyukasik Y, Ozcebe O, Dundar S, Kirazli S. Cytokines, endothelium, and adhesive molecules in pathologic thrombopoiesis. Clin Appl Thromb Hemost. 2001;7:126-130
17. Chuen CK, Li K, Yang M, Fok TF, Li CK, Chui CM, Yuen PM. Interleukin-1beta up-regulates the expression of thrombopoietin and transcription factors c-Jun, c-Fos, GATA-1, and NF-E2 in megakaryocytic cells. J Lab Clin Med. 2004;143:75-88
18. Yang M, Li K, Chui CM, Yuen PM, Chan PK, Chuen CK, Li CK, Fok TF. Expression of interleukin (IL) 1 type I and type II receptors in megakaryocytic cells and enhancing effects of IL-1beta on megakaryocytopoiesis and NF-E2 expression. Br J Haematol. 2000;111:371-380
19. Jiang S, Levine JD, Fu Y, Deng B, London R, Groopman JE, Avraham H. Cytokine production by primary bone marrow megakaryocytes. Blood. 1994;84:4151-4156
20. Williams DE, Morrissey PJ. Alterations in megakaryocyte and platelet compartments following in vivo IL-1 beta administration to normal mice. J Immunol. 1989;142:4361-4365
21. Hawrylowicz CM, Santoro SA, Platt FM, Unanue ER. Activated platelets express IL-1 activity. J Immunol. 1989;143:4015-4018
22. Kaplanski G, Porat R, Aiura K, Erban JK, Gelfand JA, Dinarello CA. Activated platelets induce endothelial secretion of interleukin-8 in vitro via an interleukin-1-mediated event. Blood. 1993;81:2492-2495
23. Gawaz M, Brand K, Dickfeld T, Pogatsa-Murray G, Page S, Bogner C, Koch W, Schömig A, Neumann F. Platelets induce alterations of chemotactic and adhesive properties of endothelial cells mediated through an interleukin-1-dependent mechanism. Implications for atherogenesis. Atherosclerosis. 2000;148:75-85
24. Loppnow H, Bil R, Hirt S, Schönbeck U, Herzberg M, Werdan K, Rietschel ET, Brandt E, Flad HD. Platelet-derived interleukin-1 induces cytokine production, but not proliferation of human vascular smooth muscle cells. Blood. 1998;91:134-141
25. Denis MM, Tolley ND, Bunting M, et al. Escaping the nuclear confines: Signal-dependent pre-mRNA splicing in anucleate platelets. Cell. 2005;122:379-391
26. Lindemann S, Tolley ND, Dixon DA, McIntyre TM, Prescott SM, Zimmerman GA, Weyrich AS. Activated platelets mediate inflammatory signaling by regulated interleukin 1beta synthesis. J Cell Biol. 2001;154:485-490
27. Beaulieu LM, Lin E, Morin KM, Tanriverdi K, Freedman JE. Regulatory effects of TLR2 on megakaryocytic cell function. Blood. 2011;117:5963-5974
28. Rowley JW, Oler AJ, Tolley ND, Hunter BN, Low EN, Nix DA, Yost CC, Zimmerman GA, Weyrich AS. Genome-wide RNA-seq analysis of human and mouse platelet transcriptomes. Blood. 2011;118:e101-e111
29. Blair P, Rex S, Vitseva O, Beaulieu L, Tanriverdi K, Chakrabarti S, Hayashi C, Genco CA, Iafrati M, Freedman JE. Stimulation of Toll-like receptor 2 in human platelets induces a thromboinflammatory response through activation of phosphoinositide 3-kinase. Circ Res. 2009;104:346-354
30. Freedman JE, Larson MG, Tanriverdi K, O'Donnell CJ, Morin K, Hakanson AS, Vasan RS, Johnson AD, Iafrati MD, Benjamin EJ. Relation of platelet and leukocyte inflammatory transcripts to body mass index in the Framingham heart study. Circulation. 2010;122:119-129
31. He X, Mekasha S, Mavrogiorgos N, Fitzgerald KA, Lien E, Ingalls RR. Inflammation and fibrosis during Chlamydia pneumoniae infection is regulated by IL-1 and the NLRP3/ASC inflammasome. J Immunol. 2010;184:5743-5754
32. Li C, Zienkiewicz J, Hawiger J. Interactive sites in the MyD88 Toll/interleukin (IL) 1 receptor domain responsible for coupling to the IL1beta signaling pathway. J Biol Chem. 2005;280:26152-26159
33. Song KW, Talamas FX, Suttmann RT, Olson PS, Barnett JW, Lee SW, Thompson KD, Jin S, Hekmat-Nejad M, Cai TZ, Manning AM, Hill RJ, Wong BR. The kinase activities of interleukin-1 receptor associated kinase (IRAK)-1 and 4 are redundant in the control of inflammatory cytokine expression in human cells. Mol Immunol. 2009;46:1458-1466
34. Dai SM, Shan ZZ, Nishioka K, Yudoh K. Implication of interleukin 18 in production of matrix metalloproteinases in articular chondrocytes in arthritis: Direct effect on chondrocytes may not be pivotal. Ann Rheum Dis. 2005;64:735-742
35. LaFramboise WA, Bombach KL, Dhir RJ, Muha N, Cullen RF, Pogozelski AR, Turk D, George JD, Guthrie RD, Magovern JA. Molecular dynamics of the compensatory response to myocardial infarct. J Mol Cell Cardiol. 2005;38:103-117
36. Vikman P, Ansar S, Edvinsson L. Transcriptional regulation of inflammatory and extracellular matrix-regulating genes in cerebral arteries following experimental subarachnoid hemorrhage in rats. Laboratory investigation. J Neurosurg. 2007;107:1015-1022
37. Leviton A, Hecht JL, Allred EN, Yamamoto H, Fichorova RN, Dammann O; ELGAN Study Investigators. Persistence after birth of systemic inflammation associated with umbilical cord inflammation. J Reprod Immunol. 2011;90:235-243
38. Shchors K, Nozawa H, Xu J, Rostker F, Swigart-Brown L, Evan G, Hanahan D. Increased invasiveness of MMP-9-deficient tumors in two mouse models of neuroendocrine tumorigenesis. Oncogene. 2013;32:502-513
39. McManus DD, Beaulieu LM, Mick E, Tanriverdi K, Larson MG, Keaney JF Jr, Benjamin EJ, Freedman JE. Relationship among circulating inflammatory proteins, platelet gene expression, and cardiovascular risk. Arterioscler Thromb Vasc Biol. 2013;33:2666-2673
40. Rex S, Beaulieu LM, Perlman DH, Vitseva O, Blair PS, McComb ME, Costello CE, Freedman JE. Immune versus thrombotic stimulation of platelets differentially regulates signalling pathways, intracellular protein-protein interactions, and alpha-granule release. Thromb Haemost. 2009;102:97-110
41. Risitano A, Beaulieu LM, Vitseva O, Freedman JE. Platelets and platelet-like particles mediate intercellular RNA transfer. Blood. 2012;119:6288-6295
42. Vara D, Campanella M, Pula G. The novel NOX inhibitor 2-Acetlphenothiazine impairs collagen-dependent thrombus formation in a GPVI-manner. Br J Pharmacol. 2013;168:212-224