Endothelial Activation and Dysfunction in the Pathogenesis of Influenza A Virus Infection

Overview

Journal Virulence

Specialty Microbiology

Date 2013 Jul 19

PMID 23863601

Citations 57

Authors

Susan M Armstrong

Ilyse Darwish

Warren L Lee

Affiliations

Soon will be listed here.

Abstract

The development of severe influenza has been attributed, in part, to a heightened innate immune response. Recent evidence suggests that endothelial activation, loss of barrier function, and consequent microvascular leak may also serve important mechanistic roles in the pathogenesis of severe influenza. The aim of this review is to summarize the current evidence in support of endothelial activation and dysfunction as a central feature preceding the development of severe influenza. We also discuss the effect of influenza on platelet-endothelial interactions.

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References

Ng H, Narasaraju T, Phoon M, Sim M, Seet J, Chow V . Doxycycline treatment attenuates acute lung injury in mice infected with virulent influenza H3N2 virus: involvement of matrix metalloproteinases. Exp Mol Pathol. 2012; 92(3):287-95. DOI: 10.1016/j.yexmp.2012.03.003. View

Narasaraju T, Yang E, Perumal Samy R, Ng H, Poh W, Liew A . Excessive neutrophils and neutrophil extracellular traps contribute to acute lung injury of influenza pneumonitis. Am J Pathol. 2011; 179(1):199-210. PMC: 3123873. DOI: 10.1016/j.ajpath.2011.03.013. View

Dawson T, Beck M, Kuziel W, Henderson F, Maeda N . Contrasting effects of CCR5 and CCR2 deficiency in the pulmonary inflammatory response to influenza A virus. Am J Pathol. 2000; 156(6):1951-9. PMC: 1850091. DOI: 10.1016/S0002-9440(10)65068-7. View

Bunce P, High S, Nadjafi M, Stanley K, Liles W, Christian M . Pandemic H1N1 influenza infection and vascular thrombosis. Clin Infect Dis. 2011; 52(2):e14-7. DOI: 10.1093/cid/ciq125. View

Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss D . Neutrophil extracellular traps kill bacteria. Science. 2004; 303(5663):1532-5. DOI: 10.1126/science.1092385. View

Spodick D, Flessas A, Johnson M . Association of acute respiratory symptoms with onset of acute myocardial infarction: prospective investigation of 150 consecutive patients and matched control patients. Am J Cardiol. 1984; 53(4):481-2. DOI: 10.1016/0002-9149(84)90016-x. View

Grommes J, Alard J, Drechsler M, Wantha S, Morgelin M, Kuebler W . Disruption of platelet-derived chemokine heteromers prevents neutrophil extravasation in acute lung injury. Am J Respir Crit Care Med. 2012; 185(6):628-36. PMC: 3326286. DOI: 10.1164/rccm.201108-1533OC. View

Xu H, Ye X, Steinberg H, Liu S . Selective blockade of endothelial NF-kappaB pathway differentially affects systemic inflammation and multiple organ dysfunction and injury in septic mice. J Pathol. 2009; 220(4):490-8. DOI: 10.1002/path.2666. View

Goldenberg N, Steinberg B, Slutsky A, Lee W . Broken barriers: a new take on sepsis pathogenesis. Sci Transl Med. 2011; 3(88):88ps25. DOI: 10.1126/scitranslmed.3002011. View

10.

. Intensive-care patients with severe novel influenza A (H1N1) virus infection - Michigan, June 2009. MMWR Morb Mortal Wkly Rep. 2009; 58(27):749-52. View

11.

Maniatis N, Orfanos S . The endothelium in acute lung injury/acute respiratory distress syndrome. Curr Opin Crit Care. 2008; 14(1):22-30. DOI: 10.1097/MCC.0b013e3282f269b9. View

12.

Petrache I, Crow M, Neuss M, Garcia J . Central involvement of Rho family GTPases in TNF-alpha-mediated bovine pulmonary endothelial cell apoptosis. Biochem Biophys Res Commun. 2003; 306(1):244-9. DOI: 10.1016/s0006-291x(03)00945-8. View

13.

Perrone L, Plowden J, Garcia-Sastre A, Katz J, Tumpey T . H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog. 2008; 4(8):e1000115. PMC: 2483250. DOI: 10.1371/journal.ppat.1000115. View

14.

Mehta D, Konstantoulaki M, Ahmmed G, Malik A . Sphingosine 1-phosphate-induced mobilization of intracellular Ca2+ mediates rac activation and adherens junction assembly in endothelial cells. J Biol Chem. 2005; 280(17):17320-8. DOI: 10.1074/jbc.M411674200. View

15.

Wang S, Le T, Kurihara N, Chida J, Cisse Y, Yano M . Influenza virus-cytokine-protease cycle in the pathogenesis of vascular hyperpermeability in severe influenza. J Infect Dis. 2010; 202(7):991-1001. PMC: 7537608. DOI: 10.1086/656044. View

16.

Kunzelmann K, Beesley A, King N, Karupiah G, Young J, Cook D . Influenza virus inhibits amiloride-sensitive Na+ channels in respiratory epithelia. Proc Natl Acad Sci U S A. 2000; 97(18):10282-7. PMC: 27875. DOI: 10.1073/pnas.160041997. View

17.

Feldmann A, Schafer M, Garten W, Klenk H . Targeted infection of endothelial cells by avian influenza virus A/FPV/Rostock/34 (H7N1) in chicken embryos. J Virol. 2000; 74(17):8018-27. PMC: 112334. DOI: 10.1128/jvi.74.17.8018-8027.2000. View

18.

Bussolino F, Camussi G, Baglioni C . Synthesis and release of platelet-activating factor by human vascular endothelial cells treated with tumor necrosis factor or interleukin 1 alpha. J Biol Chem. 1988; 263(24):11856-61. View

19.

Saffarzadeh M, Juenemann C, Queisser M, Lochnit G, Barreto G, Galuska S . Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS One. 2012; 7(2):e32366. PMC: 3289648. DOI: 10.1371/journal.pone.0032366. View

20.

Bermejo-Martin J, Ortiz de Lejarazu R, Pumarola T, Rello J, Almansa R, Ramirez P . Th1 and Th17 hypercytokinemia as early host response signature in severe pandemic influenza. Crit Care. 2009; 13(6):R201. PMC: 2811892. DOI: 10.1186/cc8208. View