Gene expression profiles link respiratory viral infection, platelet response to aspirin, and acute myocardial infarction

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Rose, Jason J ^a,b,c   Voora, Deepak ^a,b   Cyr, Derek D ^a   Lucas, Joseph E ^a   Zaas, Aimee K ^a,b   Woods, Christopher W ^a,b   Newby, L Kristin ^b   Kraus, William E ^b   Ginsburg, Geoffrey S ^a,b  

^a Center for Applied Genomics and Precision Medicine ^*  (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CLOPIDOGREL; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; RNA; TRANSCRIPTOME;

ACTR2 GENE; ACUTE HEART INFARCTION; ADULT; AGED; ARTICLE; CALU GENE; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; DISEASE COURSE; FEMALE; GAS6 GENE; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION SIGNATURE; GENE FUNCTION; GNB1 GENE; HEART CATHETERIZATION; HEART INFARCTION; HEMOSTASIS; HUMAN; HUMAN RESPIRATORY SYNCYTIAL VIRUS; HUMAN RHINOVIRUS; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H3N2); LOGISTIC REGRESSION ANALYSIS; MAJOR CLINICAL STUDY; MALE; NONHUMAN; PATHOPHYSIOLOGY; PPP2R1A GENE; PRDX6 GENE; PROSPECTIVE STUDY; PSAP GENE; RECEIVER OPERATING CHARACTERISTIC; RESPIRATORY VIRUS; SPARC GENE; SYMPTOM; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; VIRAL RESPIRATORY TRACT INFECTION; VIRUS EXPRESSION; ZYX GENE; COMPLICATION; DRUG EFFECTS; GENETICS; INFLUENZA; METABOLISM; MIDDLE AGED; MYOCARDIAL INFARCTION; PHARMACOGENETICS; PICORNAVIRUS INFECTION; RESPIRATORY SYNCYTIAL VIRUS INFECTION; RHINOVIRUS; THROMBOCYTE;

AGED; ASPIRIN; BLOOD PLATELETS; CARDIAC CATHETERIZATION; FEMALE; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA, HUMAN; MALE; MIDDLE AGED; MYOCARDIAL INFARCTION; PHARMACOGENETICS; PICORNAVIRIDAE INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; RHINOVIRUS; TRANSCRIPTOME;

EID: 84941350154     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0132259     Document Type: Article

References (63)

1. Rondina MT, Brewster B, Grissom CK, Zimmerman GA, Kastendieck DH, Harris ES, et al. In vivo platelet activation in critically ill patients with primary 2009 influenza A (H1N1). Chest. 2012 Jun; 141 (6):1490-5. doi:10.1378/chest.11-2860 PMID: 22383669.
2. Guan XR, Li X, Xin XM, Jiang LX, Cui LY, Wang LF, et al. Influenza virus infection and risk of acute myocardial infarction. Inflammation. 2008 Aug; 31(4):266-72. doi:10.1007/s10753-008-9074-2 PMID: 18568394.
3. Warren-Gash C, Bhaskaran K, Hayward A, Leung GM, Lo SV, Wong CM, et al. Circulating influenza virus, climatic factors, and acute myocardial infarction: A time series study in England and Wales and Hong Kong. J Infect Dis. 2011 Jun 15; 203(12):1710-8. doi:10.1093/infdis/jir171 PMID: 21606529.
4. Lichenstein R, Magder LS, King RE, King JC Jr. The relationship between influenza outbreaks and acute ischemic heart disease in Maryland residents over a 7-year period. J Infect Dis. 2012 Sep 15; 206(6):821-7. doi:10.1093/infdis/jis435 PMID: 22798684.
5. Arbit B, Gaultier CR, Schwarz ER. H1N1 virus infection associated with acute myocardial infarction in a young patient without coronary artery disease-first reported case. Acta Cardiol. 2011 Dec; 66(6):807- 10. PMID: 22299395.
6. Meier CR, Jick SS, Derby LE, Vasilakis C, Jick H. Acute respiratory-tract infections and risk of first-time acute myocardial infarction. Lancet. 1998 May 16; 351(9114):1467-71. PMID: 9605802.
7. Wiwanitkit V. Cardiology concern on new H3N2 influenza outbreak. Anadolu Kardiyol Derg. 2013 Dec; 13(8):821.
8. Guan XR, Jiang LX, Ma XH, Wang LF, Quan H, Li HY. Respiratory syncytial virus infection and risk of acute myocardial infarction. Am J Med Sci. 2010 Nov; 340(5):356-9. PMID: 20811272.
9. Zaas AK, Chen M, Varkey J, Veldman T, Hero AO 3rd, Lucas J, et al. Gene expression signatures diagnose influenza and other symptomatic respiratory viral infections in humans. Cell Host Microbe. 2009 Sep 17; 6(3):207-17. doi:10.1016/j.chom.2009.07.006 PMID: 19664979.
10. Wang L, Hauser ER, Shah SH, Pericak-Vance MA, Haynes C, Crosslin D, et al. Peakwide mapping on chromosome 3q13 identifies the kalirin gene as a novel candidate gene for coronary artery disease. Am J Hum Genet. 2007 Apr; 80(4):650-63. PMID: 17357071.
11. Woods CW, McClain MT, Chen M, Zaas AK, Nicholson BP, Varkey J, et al. A host transcriptional signature for presymptomatic detection of infection in humans exposed to influenza H1N1 or H3N2. PLoS One. 2013; 8(1):e52198. doi:10.1371/journal.pone.0052198 PMID: 23326326.
12. Zaas A. K., Burke T., Chen M., McClain M., Nicholson B., Veldman T, et al. A Host-Based RT-PCR Gene Expression Signature to Identify Acute Respiratory Viral Infection. Sci. Transl. Med. 5, 203-126 (2013). doi:10.1126/scitranslmed.3006280 PMID: 24048524.
13. Voora D, Cyr D, Lucas J, Chi JT, Dungan J, McCaffrey TA, et al. Aspirin Exposure Reveals Novel Genes Associated with Platelet Function and Cardiovascular Events. J Am Coll Cardiol. 2013 Oct 1; 62 (14):1267-76. doi:10.1016/j.jacc.2013.05.073 PMID: 23831034.
14. Shah SH, Granger CB, Hauser ER, Kraus WE, Sun JL, Pieper K, et al; MURDOCK Horizon 1 Cardiovascular Disease Investigators. Reclassification of cardiovascular risk using integrated clinical and molecular biosignatures: Design of and rationale for the Measurement to Understand the Reclassification of Disease of Cabarrus and Kannapolis (MURDOCK) Horizon 1 Cardiovascular Disease Study. Am Heart J. 2010 Sep; 160(3):371-379.e2. doi:10.1016/j.ahj.2010.06.051.
15. Jackson GG, Dowling HF, Spiesman IG, Boand AV. Transmission of the common cold to volunteers under controlled conditions. I. The common cold as a clinical entity. AMA Arch Intern Med 1958; 101:267-278. PMID: 13497324.
16. Barrett B, Brown R, Voland R, Maberry R, Turner R. Relations among questionnaire and laboratory measures of rhinovirus infection. Eur Respir J 2006; 28:358-363. PMID: 16641127.
17. Turner RB. Ineffectiveness of intranasal zinc gluconate for prevention of experimental rhinovirus colds. Clin Infect Dis 2001; 33:1865-1870. PMID: 11692298.
18. Lucas JE, Kung HN, Chi JT. Latent factor analysis to discover pathway-associated putative segmental aneuploidies in human cancers. PLoS Comput Biol. 2010; 6:e1000920. doi:10.1371/journal.pcbi.1000920 PMID: 20824128.
19. Erden I, Erden EC, Ozhan H, Basar C. Acute myocarditis mimicking acute myocardial infarction associated with pandemic 2009 (H1N1) influenza A virus. Cardiol J. 2011; 18(5):552-5. PMID: 21947992.
20. Warren-Gash C, Hayward AC, Hemingway H, Denaxas S, Thomas SL, Timmis AD, et al. Influenza infection and risk of acute myocardial infarction in England and Wales: A CALIBER self-controlled case series study. J Infect Dis. 2012 Dec 1; 206(11):1652-9. doi:10.1093/infdis/jis597 PMID: 23048170.
21. Guan X, Yang W, Sun X, Wang L, Ma B, Li H, et al. Association of influenza virus infection and inflammatory cytokines with acute myocardial infarction. Inflamm Res. 2012 Jun; 61(6):591-8. doi:10.1007/s00011-012-0449-3 PMID: 22373653.
22. Kuo RL, Zhao C, Malur M, Krug RM. Influenza A virus strains that circulate in humans differ in the ability of their NS1 proteins to block the activation of IRF3 and interferon-β transcription. Virology. 2010 Dec 20; 408(2):146-58. doi:10.1016/j.virol.2010.09.012 PMID: 20934196.
23. Geiler J, Michaelis M, Sithisarn P, Cinatl J Jr. Comparison of pro-inflammatory cytokine expression and cellular signal transduction in human macrophages infected with different influenza A viruses. Med Microbiol Immunol. 2011 Feb; 200(1):53-60. doi:10.1007/s00430-010-0173-y PMID: 20865277.
24. Mussá T, Ballester M, Silva-Campa E, Baratelli M, Busquets N, Lecours MP, et al. Swine, human or avian influenza viruses differentially activates porcine dendritic cells cytokine profile. Vet Immunol Immunopathol. 2013 Jul 15; 154(1-2):25-35. doi:10.1016/j.vetimm.2013.04.004 PMID: 23689011.
25. Seki M, Kosai K, Hara A, Imamura Y, Nakamura S, Kurihara S, et al. Expression and DNA microarray analysis of a platelet activating factor-related molecule in severe pneumonia in mice due to influenza virus and bacterial co-infection. Jpn J Infect Dis. 2009 Jan; 62(1):6-10. PMID: 19168951.
26. Garcia CC, Russo RC, Guabiraba R, Fagundes CT, Polidoro RB, Tavares LP, et al. Platelet-activating factor receptor plays a role in lung injury and death caused by Influenza A in mice. PLoS Pathog. 2010 Nov 4; 6(11):e1001171. doi:10.1371/journal.ppat.1001171 PMID: 21079759.
27. Lanza GA, Barone L, Scalone G, Pitocco D, Sgueglia GA, Mollo R, et al. Inflammation-related effects of adjuvant influenza A vaccination on platelet activation and cardiac autonomic function. J Intern Med. 2011 Jan; 269(1):118-25. doi:10.1111/j.1365-2796.2010.02285.x PMID: 20964738.
28. Armstrong SM, Darwish I, Lee WL. Endothelial activation and dysfunction in the pathogenesis of influenza A virus infection. Virulence. 2013 Aug 15; 4(6):537-42. doi:10.4161/viru.25779 PMID: 23863601.
29. Berri F, Rimmelzwaan GF, Hanss M, Albina E, Foucault-Grunenwald ML, Lê VB, et al. Plasminogen controls inflammation and pathogenesis of influenza virus infections via fibrinolysis. PLoS Pathog. 2013 Mar; 9(3):e1003229. doi:10.1371/journal.ppat.1003229 PMID: 23555246.
30. Huang Y, Zaas AK, Rao A, Dobigeon N, Woolf PJ, Veldman T, et al. Temporal dynamics of host molecular responses differentiate symptomatic and asymptomatic influenza a infection. PLoS Genet. 2011 Aug; 7(8):e1002234. doi:10.1371/journal.pgen.1002234 PMID: 21901105.
31. Angelillo-Scherrer A, deFrutos P, Aparicio C, Melis E, Savi P, Lupu F, et al. Deficiency or inhibition of Gas6 causes platelet dysfunction and protects mice against thrombosis. Nat Med. 2001 Feb; 7(2):215-21.
32. Hurtado B, de Frutos PG. GAS6 in systemic inflammatory diseases: with and without infection. Crit Care. 2010;14(5):1003. PMID: 11175853.
33. Laurance S, Lemarié CA, Blostein MD. Growth arrest-specific gene 6 (gas6) and vascular hemostasis. Adv Nutr. 2012 Mar 1; 3(2):196-203. doi:10.3945/an.111.001826 PMID: 22516727.
34. Tjwa M, Bellido-Martin L, Lin Y, Lutgens E, Plaisance S, Bono F, et al. Gas6 promotes inflammation by enhancing interactions between endothelial cells, platelets, and leukocytes. Blood. 2008 Apr 15; 111 (8):4096-105. PMID: 18156494.
35. Maree AO, Jneid H, Palacios IF, Rosenfield K, MacRae CA, Fitzgerald DJ. Growth arrest specific gene (GAS) 6 modulates platelet thrombus formation and vascular wall homeostasis and represents an attractive drug target. Curr Pharm Des. 2007; 13(26):2656-61. PMID: 17897008.
36. Naghavi M, Barlas Z, Siadaty S, Naguib S, Madjid M, Casscells W. Association of influenza vaccination and reduced risk of recurrent myocardial infarction. Circulation. 2000 Dec 19; 102(25):3039-45. PMID: 11120692.
37. Guan X, Yang W, Sun X, Wang L, Ma B, Li H, et al. Association of influenza virus infection and inflammatory cytokines with acute myocardial infarction. Inflamm Res. 2012 Jun; 61(6):591-8. doi:10.1007/s00011-012-0449-3 PMID: 22373653.
38. Loomba RS, Aggarwal S, Shah PH, Arora RR. Influenza vaccination and cardiovascular morbidity and mortality: Analysis of 292, 383 patients. J Cardiovasc Pharmacol Ther. 2012 Sep; 17(3):277-83. doi:10.1177/1074248411429965 PMID: 22172681.
39. Davis MM, Taubert K, Benin AL, Brown DW, Mensah GA, Baddour LM, et al; American Heart Association; American College of Cardiology. Influenza vaccination as secondary prevention for cardiovascular disease: A science advisory from the American Heart Association/American College of Cardiology. Circulation. 2006 Oct 3; 114(14):1549-53. PMID: 16982936.
40. Udell JA, Zawi R, Bhatt DL, Keshtkar-Jahromi M, Gaughran F, Phrommintikul A, et al. Association between influenza vaccination and cardiovascular outcomes in high-risk patients: A meta-analysis. JAMA. 2013 Oct 23; 310(16):1711-20. doi:10.1001/jama.2013.279206 PMID: 24150467.
41. Brett SJ, Myles P, Lim WS, Enstone JE, Bannister B, Semple MG, et al; Influenza Clinical Information Network (FLU-CIN). Pre-admission statin use and in-hospital severity of 2009 pandemic influenza A (H1N1) disease. PLoS One. 2011 Apr 25; 6(4):e18120. doi:10.1371/journal.pone.0018120 PMID: 21541017.
42. Vandermeer ML, Thomas AR, Kamimoto L, Reingold A, Gershman K, Meek J, et al. Association between use of statins and mortality among patients hospitalized with laboratory-confirmed influenza virus infections: A multistate study. J Infect Dis. 2012 Jan 1; 205(1):13-9. doi:10.1093/infdis/jir695 PMID: 22170954.
43. Bogomol'tsev BP, Deviatkin AV. Clinical implications of impaired microcirculation and hemodynamics in acute respiratory viral infections and their pharmacological correction. Klin Med (Mosk). 2003; 81 (5):9-15. Review.
44. Link A, Kaplan BT, Böhm M. 21-year-old woman with Reye's syndrome after influenza. Dtsch Med Wochenschr. 2012 Sep; 137(38):1853-6. doi:10.1055/s-0032-1305311 PMID: 22971971.
45. Eyers S, Weatherall M, Shirtcliffe P, Perrin K, Beasley R. The effect on mortality of antipyretics in the treatment of influenza infection: systematic review and meta-analysis. J R Soc Med. 2010 Oct; 103 (10):403-11. Review. doi:10.1258/jrsm.2010.090441 PMID: 20929891.
46. Starko KM. Salicylates and pandemic influenza mortality, 1918-1919 pharmacology, pathology, and historic evidence. Clin Infect Dis. 2009 Nov 1; 49(9):1405-10. doi:10.1086/606060 PMID: 19788357.
47. Mazur I, Wurzer WJ, Ehrhardt C, Pleschka S, Puthavathana P, Silberzahn T, et al. Acetylsalicylic acid (ASA) blocks influenza virus propagation via its NF-kappaB-inhibiting activity. Cell Microbiol. 2007 Jul; 9(7):1683-94. PMID: 17324159.
48. Li W, Liu Y, Mukhtar MM, Gong R, Pan Y, Rasool ST, et al. Activation of interleukin-32 pro-inflammatory pathway in response to influenza A virus infection. PLoS One. 2008 Apr 16; 3(4):e1985. doi:10.1371/journal.pone.0001985 PMID: 18414668.
49. Bucasas KL, Franco LM, Shaw CA, Bray MS, Wells JM, Niño D, et al. Early patterns of gene expression correlate with the humoral immune response to influenza vaccination in humans. J Infect Dis. 2011 Apr 1; 203(7):921-9. doi:10.1093/infdis/jiq156 PMID: 21357945.
50. Mark DB, Nelson CL, Califf RM, Harrell FE Jr., Lee KL, Jones RH, et al. Continuing evolution of therapy for coronary artery disease. Initial results from the era of coronary angioplasty. Circulation. 1994; 89:2015-2025. PMID: 8181125.
51. Liberzon A, Subramanian A, Pinchback R, Thorvaldsdóttir H, Tamayo P, Mesirov JP. Molecular signatures database (MSigDB) 3.0. Bioinformatics. 2011 Jun 15; 27(12):1739-40. Gene Sets: REACTOME- PLATELET-ACTIVATION-SIGNALING-A, RAGHAVACHARI-PLATELET-SPECIFIC-GE. doi:10.1093/bioinformatics/btr260 PMID: 21546393.
52. Liberzon A, Subramanian A, Pinchback R, Thorvaldsdóttir H, Tamayo P, Mesirov JP. Molecular signatures database (MSigDB) 3.0. Bioinformatics. 2011 Jun 15; 27(12):1739-40. Gene Sets: PID-THROMBIN- PAR1-PATHWAY, BIOCARTA-PAR1-PATHWAY, REACTOME-HEMOSTASIS. doi:10.1093/bioinformatics/btr260 PMID: 21546393.
53. Coppinger JA, Cagney G, Toomey S, Kislinger T, Belton O, McRedmond JP, et al. Characterization of the proteins released from activated platelets leads to localization of novel platelet proteins in human atherosclerotic lesions. Blood. 2004 Mar 15; 103(6):2096-104. PMID: 14630798.
54. Hansen GA, Vorum H, Jacobsen C, Honoré B. Calumenin but not reticulocalbin forms a Ca2+-dependent complex with thrombospondin-1. A potential role in haemostasis and thrombosis. Mol Cell Biochem. 2009 Jan; 320(1-2):25-33. doi:10.1007/s11010-008-9895-1 PMID: 18688696.
55. Yamada Y, Limmon GV, Zheng D, Li N, Li L, Yin L, et al. Major shifts in the spatio-temporal distribution of lung antioxidant enzymes during influenza pneumonia. PLoS One. 2012; 7(2):e31494. doi:10.1371/journal.pone.0031494 PMID: 22355371.
56. Schremmer B, Manevich Y, Feinstein SI, Fisher AB. Peroxiredoxins in the lung with emphasis on peroxiredoxin VI. Sub-cellular Biochemistry. 2007; 44:317-344. PMID: 18084901.
57. Moscardó A, Vallés J, Piñón M, Aznar J, Martínez-Sales V, Santos MT. Regulation of cytosolic PlA2 activity by PP1/PP2A serine/threonine phosphatases in human platelets. Platelets. 2006 Sep; 17 (6):405-15. PMID: 16973502.
58. Knapp M, Zendzian-Piotrowska M, Błachnio-Zabielska A, Zabielski P, Kurek K, Górski J. Myocardial infarction differentially alters sphingolipid levels in plasma, erythrocytes and platelets of the rat. Basic Res Cardiol. 2012; 107(6):294. doi:10.1007/s00395-012-0294-0 PMID: 22961594.
59. Sano A, Hineno T, Mizuno T, Kondoh K, Ueno S, Kakimoto Y, et al. Sphingolipid hydrolase activator proteins and their precursors. Biochem Biophys Res Commun. 1989 Dec 29; 165(3):1191-7 PMID: 2610686.
60. Parguiña AF, Grigorian-Shamajian L, Agra RM, Teijeira-Fernández E, Rosa I, Alonso J, et al. Proteins involved in platelet signaling are differentially regulated in acute coronary syndrome: A proteomic study. PLoS One. 2010 Oct 14; 5(10):e13404. doi:10.1371/journal.pone.0013404 PMID: 20976234.
61. Schellings MW, Vanhoutte D, Swinnen M, Cleutjens JP, Debets J, van Leeuwen RE, et al. Absence of SPARC results in increased cardiac rupture and dysfunction after acute myocardial infarction. J Exp Med. 2009 Jan 16; 206(1):113-23. PMID: 19103879.
62. Han J, Liu G, Profirovic J, Niu J, Voyno-Yasenetskaya T. Zyxin is involved in thrombin signaling via interaction with PAR-1 receptor. FASEB J. 2009 Dec; 23(12):4193-206. doi:10.1096/fj.09-131862 PMID: 19690217.
63. Dabek J, Ligus J, Szota J. Oligonucleotide microarray and QRT-PCR study of adhesion protein gene expression in acute coronary syndrome patients. Inflammation. 2010 Dec; 33(6):398-407. doi:10.1007/s10753-010-9198-z PMID: 20306290.