Sex differences in platelet toll-like receptors and their association with cardiovascular risk factors

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 35, Issue 4, 2015, Pages 1030-1037

  Koupenova, Milka ^a   Mick, Eric ^a   Mikhalev, Ekaterina ^a   Benjamin, Emelia J ^b,c,d   Tanriverdi, Kahraman ^a   Freedman, Jane E ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b University of Massachusetts Medical School ^*  (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d BOSTON UNIVERSITY   (United States)

Author keywords

blood platelets; epidemiology; infection; inflammation

Indexed keywords

C REACTIVE PROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INTERLEUKIN 6; INTRACELLULAR CELL ADHESION MOLECULE 1; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; PADGEM PROTEIN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 10; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA RECEPTOR; TUMOR NECROSIS FACTOR ALPHA RECEPTOR 1; UNCLASSIFIED DRUG; AUTACOID; BIOLOGICAL MARKER; CARRIER PROTEIN; MYD88 PROTEIN, HUMAN; UNC93B1 PROTEIN, HUMAN;

AGED; ARTICLE; BODY MASS; CARDIOVASCULAR RISK; CHOLESTEROL BLOOD LEVEL; COHORT ANALYSIS; FEMALE; HIGH THROUGHPUT SCREENING; HUMAN; IMMUNITY; INFLAMMATION; MAJOR CLINICAL STUDY; MALE; OBSERVATIONAL STUDY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DIFFERENCE; THROMBOCYTE; BLOOD; CARDIOVASCULAR DISEASES; CHEMISTRY; COMPARATIVE STUDY; GENETICS; HIGH THROUGHPUT SEQUENCING; LONGITUDINAL STUDY; MASSACHUSETTS; MIDDLE AGED; PROCEDURES; PROGNOSIS; RISK FACTOR;

AGED; BIOMARKERS; BLOOD PLATELETS; CARDIOVASCULAR DISEASES; FEMALE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INFLAMMATION MEDIATORS; LONGITUDINAL STUDIES; MALE; MASSACHUSETTS; MEMBRANE TRANSPORT PROTEINS; MIDDLE AGED; MYELOID DIFFERENTIATION FACTOR 88; PROGNOSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RISK FACTORS; RNA, MESSENGER; SEX FACTORS; TOLL-LIKE RECEPTORS;

EID: 84933676656     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.304954     Document Type: Article

References (31)

1. Rondina MT, Weyrich AS, Zimmerman GA. Platelets as cellular effectors of inflammation in vascular diseases. Circ Res. 2013;112:1506-1519. doi: 10.1161/CIRCRESAHA.113.300512.
2. Semple JW, Italiano JE Jr, Freedman J. Platelets and the immune continuum. Nat Rev Immunol. 2011;11:264-274. doi: 10.1038/nri2956.
3. Koupenova M, Vitseva O, MacKay CR, Beaulieu LM, Benjamin EJ, Mick E, Kurt-Jones EA, Ravid K, Freedman JE. Platelet-TLR7 mediates host survival and platelet count during viral infection in the absence of platelet-dependent thrombosis. Blood. 2014;124:791-802. doi: 10.1182/ blood-2013-11-536003.
4. 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. doi: 10.1161/CIRCRESAHA.108.185785.
5. Andonegui G, Kerfoot SM, McNagny K, Ebbert KV, Patel KD, Kubes P. Platelets express functional Toll-like receptor-4. Blood. 2005;106:2417-2423. doi: 10.1182/blood-2005-03-0916.
6. Clark SR, Ma AC, Tavener SA, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. 2007;13:463-469. doi: 10.1038/nm1565.
7. 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. doi: 10.1161/CIRCRESAHA.108.185785.
8. Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity. 2011;34:637-650. doi: 10.1016/j.immuni.2011.05.006.
9. Panigrahi S, Ma Y, Hong L, Gao D, West XZ, Salomon RG, Byzova TV, Podrez EA. Engagement of platelet toll-like receptor 9 by novel endogenous ligands promotes platelet hyperreactivity and thrombosis. Circ Res. 2013;112:103-112. doi: 10.1161/CIRCRESAHA.112.274241.
10. Thon JN, Peters CG, Machlus KR, Aslam R, Rowley J, Macleod H, Devine MT, Fuchs TA, Weyrich AS, Semple JW, Flaumenhaft R, Italiano JE Jr. T granules in human platelets function in TLR9 organization and signaling. J Cell Biol. 2012;198:561-574. doi: 10.1083/jcb.201111136.
11. 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. doi: 10.1182/blood-2011-03-339705.
12. 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. doi: 10.1161/CIRCULATIONAHA.109.928192.
13. Roquer J, Campello AR, Gomis M. Sex differences in firstever acute stroke. Stroke. 2003;34:1581-1585. doi: 10.1161/01. STR.0000078562.82918.F6.
14. Zhang G, Han J, Welch EJ, Ye RD, Voyno-Yasenetskaya TA, Malik AB, Du X, Li Z. Lipopolysaccharide stimulates platelet secretion and potentiates platelet aggregation via TLR4/MyD88 and the cGMP-dependent protein kinase pathway. J Immunol. 2009;182:7997-8004. doi: 10.4049/ jimmunol.0802884.
15. de Lemos JA, Morrow DA, Blazing MA, Jarolim P, Wiviott SD, Sabatine MS, Califf RM, Braunwald E. Serial measurement of monocyte chemoattractant protein-1 after acute coronary syndromes: results from the A to Z trial. J Am Coll Cardiol. 2007;50:2117-2124. doi: 10.1016/j.jacc.2007.06.057.
16. Blasius AL, Beutler B. Intracellular toll-like receptors. Immunity. 2010;32:305-315. doi: 10.1016/j.immuni.2010.03.012.
17. Ameziane N, Beillat T, Verpillat P, Chollet-Martin S, Aumont MC, Seknadji P, Lamotte M, Lebret D, Ollivier V, de Prost D. Association of the Toll-like receptor 4 gene Asp299Gly polymorphism with acute coronary events. Arterioscler Thromb Vasc Biol. 2003;23:e61-e64. doi: 10.1161/01. ATV.0000101191.92392.1D.
18. Kiechl S, Lorenz E, Reindl M, Wiedermann CJ, Oberhollenzer F, Bonora E, Willeit J, Schwartz DA. Toll-like receptor 4 polymorphisms and atherogenesis. N Engl J Med. 2002;347:185-192. doi: 10.1056/NEJMoa012673.
19. Netea MG, Hijmans A, van Wissen S, Smilde TJ, Trip MD, Kullberg BJ, de Boo T, Van der Meer JW, Kastelein JJ, Stalenhoef AF, Stalenhorf AF. Toll-like receptor-4 Asp299Gly polymorphism does not influence progression of atherosclerosis in patients with familial hypercholesterolaemia. Eur J Clin Invest. 2004;34:94-99.
20. Xiang B, Zhang G, Guo L, Li XA, Morris AJ, Daugherty A, Whiteheart SW, Smyth SS, Li Z. Platelets protect from septic shock by inhibiting macrophage-dependent inflammation via the cyclooxygenase 1 signalling pathway. Nat Commun. 2013;4:2657. doi: 10.1038/ncomms3657.
21. Klingström J, Lindgren T, Ahlm C. Sex-dependent differences in plasma cytokine responses to hantavirus infection. Clin Vaccine Immunol. 2008;15:885-887. doi: 10.1128/CVI.00035-08.
22. Klein SL. The effects of hormones on sex differences in infection: from genes to behavior. Neurosci Biobehav Rev. 2000;24:627-638.
23. Moore SL, Wilson K. Parasites as a viability cost of sexual selection in natural populations of mammals. Science. 2002;297:2015-2018. doi: 10.1126/science.1074196.
24. Crabtree TD, Pelletier SJ, Gleason TG, Pruett TL, Sawyer RG. Genderdependent differences in outcome after the treatment of infection in hospitalized patients. JAMA. 1999;282:2143-2148.
25. Cescon A, Patterson S, Chan K, Palmer AK, Margolese S, Burchell AN, Cooper C, Klein MB, Machouf N, Montaner JS, Tsoukas C, Hogg RS, Raboud JM, Loutfy MR; CANOC Collaboration. Gender differences in clinical outcomes among HIV-positive individuals on antiretroviral therapy in Canada: A multisite cohort study. PLoS One. 2013;8:e83649. doi: 10.1371/journal.pone.0083649.
26. Barrett-Connor EL, Cohn BA, Wingard DL, Edelstein SL. Why is diabetes mellitus a stronger risk factor for fatal ischemic heart disease in women than in men? The Rancho Bernardo Study. JAMA. 1991;265:627-631.
27. Yusuf S, Hawken S, Ounpuu S, Dans T, Avezum A, Lanas F, McQueen M, Budaj A, Pais P, Varigos J, Lisheng L; INTERHEART Study Investigators. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study. Lancet. 2004;364:937-952. doi: 10.1016/S0140-6736(04)17018-9.
28. Armant MA, Fenton MJ. Toll-like receptors: A family of pattern-recognition receptors in mammals. Genome Biol. 2002;3:reviews3011.1-reviews3011.6.
29. Fish EN. The X-files in immunity: sex-based differences predispose immune responses. Nat Rev Immunol. 2008;8:737-744. doi: 10.1038/ nri2394.
30. Edfeldt K, Bennet AM, Eriksson P, Frostegard J, Wiman B, Hamsten A, Hansson GK, de Faire U, Yan ZQ. Association of hypo-responsive tolllike receptor 4 variants with risk of myocardial infarction. Eur Heart J. 2004;25:1447-1453. doi: 10.1016/j.ehj.2004.05.004.
31. Nilsson D, Andiappan AK, Halldén C, De Yun W, Säll T, Tim CF, Cardell LO. Toll-like receptor gene polymorphisms are associated with allergic rhinitis: A case control study. BMC Med Genet. 2012;13:66. doi: 10.1186/1471-2350-13-66.