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Bacterial Superinfection of Influenza Protein-2 Expression Drives Illness in Dysregulated Macrophage-Inflammatory

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Bacterial Superinfection of Influenza Protein-2 Expression Drives Illness in Dysregulated Macrophage-Inflammatory Dysregulated Macrophage-Inflammatory Protein-2 Expression Drives Illness in Bacterial Superinfection of Influenza This information is current as Caleb C. J. Zavitz, Carla M. T. Bauer, Gordon J. Gaschler, of October 3, 2021. Katie M. Fraser, Robert M. Strieter, Cory M. Hogaboam and Martin R. Stampfli J Immunol published online 11 January 2010 http://www.jimmunol.org/content/early/2010/01/11/jimmun ol.0903304 Downloaded from Supplementary http://www.jimmunol.org/content/suppl/2010/01/11/jimmunol.090330 Material 4.DC1 http://www.jimmunol.org/ Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication by guest on October 3, 2021 *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Published January 11, 2010, doi:10.4049/jimmunol.0903304 The Journal of Immunology Dysregulated Macrophage-Inflammatory Protein-2 Expression Drives Illness in Bacterial Superinfection of Influenza Caleb C. J. Zavitz,* Carla M. T. Bauer,* Gordon J. Gaschler,* Katie M. Fraser,† Robert M. Strieter,‡ Cory M. Hogaboam,x and Martin R. Stampfli†,{ Influenza virus infection is a leading cause of death and disability throughout the world. Influenza-infected hosts are vulnerable to secondary bacterial infection, however,and an ensuing bacterial pneumonia is actually the predominant cause of influenza-attributed deaths during pandemics. A number of mechanisms have been proposed by which influenza may predispose to superinfection with an unrelated or heterologous pathogen, but the subsequent interaction between the host, virus, and bacteria remains an understudied area. In this study, we develop and examine a novel model of heterologous pulmonary infection in which an otherwise subclinical Bordetella parapertussis infection synergizes with an influenza virus infection to yield a life-threatening secondary pneumonia. Despite a profound pulmonary inflammatory response and unaltered viral clearance, bacterial clearance was significantly impaired Downloaded from in heterologously infected mice. No deficits were observed in pulmonary or systemic adaptive immune responses or the viability or function of infiltrating inflammatory cells to explain this phenomenon, and we provide evidence that the onset of severe pulmonary inflammation actually precedes the increased bacterial burden, suggesting that exacerbated inflammation is independent of bacterial burden. To that end, neutralization of the ELR+ inflammatory chemokine MIP-2 (CXCL2/GRO-b) attenuated the inflammation, weight loss, and clinical presentation of heterologously infected mice without impacting bacterial burden. These data suggest that pulmonary inflammation, rather than pathogen burden, is the key threat during bacterial superinfection of influenza and that http://www.jimmunol.org/ selective chemokine antagonists may be a novel therapeutic intervention in cases of bacterial superinfection of influenza. The Journal of Immunology, 2010, 184: 000–000. espite the widespread application of vaccines, antibiotics, It has long been acknowledged that a substantial fraction of and other therapies, infectious disease remains a leading influenza-related death and disability results not from primary viral D threat to human health. The World Health Organization disease but from secondary infection with bacteria unrelated estimates that over 4 million lives are lost each year to lower re- (heterologous) to the virus. In fact, recent analysis points to sec- spiratory tract infections—more than are attributable to the widely ondary bacterial pneumonia, not primary viral disease, as the recognized HIV, malaria, or tuberculosis pandemics (1). Among predominant cause of death in the three 20th century influenza by guest on October 3, 2021 lung infections, influenza virus remains a persistent threat; in non- pandemics (5) and suggests that the remarkable lethality of the pandemic years, it infects over 1 billion people worldwide, causing 1918 influenza strain may be due to its ability to drive a secondary 3–5 million cases of serious illness and an estimated 500,000 deaths bacterial pneumonia (6). Deaths to secondary bacterial infection (2), whereas during pandemics, it has eclipsed all other causes of commonly result from immunopathology, rather than bacterial death combined. The 1918 influenza pandemic depressed world- infection per se, and once initiated, immunopathology in the form wide population growth for 10 y and killed 40 million people in just of sepsis and septic shock may progress independently of the one year—the single greatest loss of life in human history (3, 4). bacterial burden itself. Specifically, even if hosts suffering from heterologous infections are treated with sterilizing antibiotics, *Medical Sciences Program, †Department of Pathology and Molecular Medicine, they still frequently succumb to pathologic inflammation (7, 8). Center for Gene Therapeutics, and {Department of Medicine, McMaster University, Several clinical trials using corticosteroids (9), G-CSF (10), he- Hamilton, Ontario, Canada; ‡Division of Pulmonary Critical Care, Department of x mofiltration (11), or neutralizing Abs against endotoxin or TNF-a Medicine, University of Virginia, Charlottesville, VA 22908; and Department of Pathology, University of Michigan Medical School, Ann Arbor, MI 48109 (12) to modulate the inflammatory response have largely failed to Received for publication October 13, 2009. Accepted for publication December 7, prevent patients’ progression to septic shock, failed to reduce 2009. mortality, and raised concerns about the risks of nonspecifically This work was supported in part by the Canadian Institutes of Health Research, the suppressing an already infected host’s immune defenses. AllerGen Network of Centers of Excellence, and AstraZeneca. C.C.J.Z. and G.J.G. A number of mechanisms have been proposed through which hold Ontario graduate scholarships. C.C.J.Z. and C.M.T.B. hold Ashley Tobacco studentships. C.M.T.B. holds a Canadian Respiratory Health Professional fellowship viral infection may predispose to bacterial infection. Viruses may and a Scotiabank Ontario Graduate Scholarship in Medical Sciences. M.R.S. holds act first by lysing epithelial cells and disrupting the respiratory a new investigator award from the Canadian Institutes of Health Research. epithelium, thus exposing the basement membrane and permitting Address correspondence and reprint requests to Dr. Martin R. Stampfli, MDCL 4010, bacterial attachment as shown during times of influenza epidemics McMaster University, Hamilton, Ontario L8N 3Z5, Canada. E-mail address: stampfli@ mcmaster.ca (13–15) and in experimental models of disease (16). In epithelial The online version of this article contains supplemental material. cells that escape direct lysis, influenza and other viruses may then Abbreviations used in this paper: 7-AAD, 7-aminoactinomycin D; AM, alveolar mac- increase the expression of receptors to which bacteria adhere (16) rophage; ARDS, acute respiratory distress syndrome; BAL, bronchoalveolar lavage; and impair ciliary function, reducing early mucocilliary clearance FSC, forward light scatter; MEF, mouse embryonic fibroblast; MPO, myeloperoxidase; of bacteria (17, 18). Additionally, viral insult may impair macro- SSC, side scatter; VILI, ventilator-induced lung injury; VSV, vesicular stomatitis virus. phage responsiveness to bacterial TLR ligands by reducing NF-kB Copyright Ó 2010 by The American Association of Immunologists, Inc. 0022-1767/10/$16.00 activity (19) and reduce macrophage antibacterial function (20). www.jimmunol.org/cgi/doi/10.4049/jimmunol.0903304 2 ROLE OF MIP-2 IN INFLUENZA SUPERINFECTION Viral induction of type I IFNs may then compromise innate an- animals were bled retro-orbitally with nonheparinized Pasteur pipets, and tibacterial immunity by inducing granulocyte apoptosis (21) and serum was obtained by incubating whole blood for 30 min at 37˚C, followed 2 reducing the production of inflammatory chemokines (22). Fi- by centrifugation. Samples were stored at 20˚C until assayed. Lungs were removed, tracheas were cannulated, and bronchoalveolar nally, activation of the adaptive antiviral system may compromise lavage (BAL) was obtained by lavaging twice with PBS (250 and 200 ml). host defense against subsequent bacterial challenge via an IFN-g– Total cell counts were determined by hemocytometer. BAL supernatants dependent impairment of alveolar macrophage (AM) function (23, were stored at 220˚C until analysis of inflammatory mediators. Cytospins 24). Whether the life-threatening pneumonia seen in heterolo- for differential cell counts were prepared by resuspending cell pellets in PBS, followed by cytocentrifugation at 10 3 g for 2 min. Cells were gously infected individuals simply represents an appropriate im- stained by Hema 3 (Biochemical Sciences), and differentials were de- mune response to a magnified bacterial burden or is the result of termined by counting at least 300 cells. Standard
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