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Interference with Virus Infection Michael Gale, Jr Interference with Virus Infection Michael Gale, Jr. J Immunol 2015; 195:1909-1910; ; This information is current as doi: 10.4049/jimmunol.1501575 of September 26, 2021. http://www.jimmunol.org/content/195/5/1909 Downloaded from Supplementary http://www.jimmunol.org/content/suppl/2015/08/14/195.5.1909.DC1 Material References This article cites 13 articles, 0 of which you can access for free at: http://www.jimmunol.org/content/195/5/1909.full#ref-list-1 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 September 26, 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 Copyright © 2015 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Th eJournal of Pillars of Immunology Immunology Interference with Virus Infection Michael Gale, Jr. n eukaryotes, type 1 IFN is essential for defense against and described its virus-induced, cell-derived, and soluble nature virus infection and is a major component of antimicrobial and defined antiviral actions that interfere with virus infection I defenses and the innate immune response. The discovery (2, 3). Hence, they assigned the name “interferon” to what is of IFN was driven by the new field of virology (1) and studies now known as the IFN family of cytokines. of influenza A virus (IAV) in the 1950s through which the How did they discover the interferon? At the time, Alick interferon was defined by Alick Isaacs and Jean Lindenmann. Isaacs was studying the infection properties of IAV and other These investigators revealed IFN as a soluble agent that was RNA viruses, including a variety of mosquito-transmitted made from infected cells and could suppress IAV infection (2, viruses, such as West Nile virus. Working at the National In- 3). The discovery of IFN serves as a cornerstone from which stitute for Medical Research in London, he met a research fel- Downloaded from the foundation for the discipline of innate immunity devel- low named Jean Lindenmann who was learning the ropes in the oped within the field of immunology. upstart field of virology. It had just been realized that viruses Today, we know that IFNs make up an important family of were different from bacteria in that they replicated through cytokines that have antimicrobial, proapoptotic, immuno- a means beyond binary fission within animal cells. This repli- modulatory, and antiproliferative actions. There are three types cation occurred during what the early virologist Leslie Hoyle of IFN, each encoded by unique gene(s) and named based on described as the eclipse phase in his studies of IAV, by which http://www.jimmunol.org/ their order of discovery and related biology. The major type 1 he defined a noninfectious phase of viral growth (6). Indeed, IFNs include IFN-a and IFN-b. In humans, there are the eclipse phase is a period of viral disassembly and synthesis multiple IFN-a genes encoding highly related, but unique, occurring right after virus entry into the host cell during acute IFN-a subtypes and a single IFN-b gene, all clustered on infection, thus reflecting the specialized and parasitic virus life chromosome 9 (4). Each can be expressed from most nucleated cycle. Additionally, a previous advance spearheading the ability cells of the body and encodes a protein that binds to a common to study viruses in tissue was applied by Isaacs and Lindenmann IFN-a/b receptor. The type 1 IFNs also include minor subtypes to culture IAV when they used Thomas Goodpasture’s (7) IFN-v,IFN-t,andIFN-k. These IFNs were discovered after methods described for the culture of fowlpox virus in chorio- by guest on September 26, 2021 IFN-a/b, are categorized as type 1 IFNs, and are selectively allantoic membranes of chicken embryos. Isaacs and other expressed among cell types and species (4). IFN-g is the sole investigators also figured out that one could heat inactivate type 2 IFN and is encoded by a single gene expressed by virus stocks to render them noninfectious while retaining prop- activated immune cells. IFN-g binds to the IFN-gR erties of tissue interaction. Using methods of IAV culture in expressed by many cell types, including immune cells and chorioallantoic membranes, Isaacs and Lindenmann pro- tissue parenchyma cells. Type 3 IFNs are now known as duced IAV stocks. They then heat inactivated a set of IAV IFN-l and, in humans, include three subtypes with a receptor stocks to use for studies of infection competition between non- chain combination that is selectively coexpressed by myeloid treated, infectious IAV and inactivated IAV. cells and by parenchymal cells of the liver and gut. During In their first series of experiments, Isaacs and Lindenmann virus infection of epithelial cells, IFN-b is typically induced exposed chorioallantoic membranes to inactivated IAV for var- first, followed by signaling events that drive the expression of ious times at 4 or 37˚C prior to exposure to infectious IAV at IFN-a subtypes. Virus infection also induces IFN-l expression 4 or 37˚C. These were the primordial days of tissue culture and, in certain cell types, the additional type 1 IFNs can be wherein cultures were little more than crude slices of membrane produced. These actions mark the innate immune response and of approximately equal size floating in a glass dish of saline the first stage of the global immune response to virus infection. solution in a slightly warmed oven without additional CO2.In In addition to antiviral actions, the IFNs serve to regulate the these experiments, the membranes were exposed to inactivated quality and actions of the adaptive immune response by IAV. Heat-inactivated IAV can still be internalized into the tar- modulating immune effector cell activation and function (5). getcellat37˚Cbutnotat4˚C,andthemembraneswerefurther Isaacs and Lindenmann discovered what we know as type 1 IFN incubated to allow inactivated virus internalization. Membranes were then washed in saline solution to remove residual IAV particles and placed back in culture for exposure to infectious Department of Immunology, Center for Innate Immunity and Immune Disease, Uni- IAV for 48 h, after which supernatants were collected. Dilutions versity of Washington School of Medicine, Seattle, WA 98109 of supernatants were then mixed with chicken RBCs. IAV can Address correspondence and reprints requests to Dr. Michael Gale, Jr., 750 Repub- agglutinate RBCs, so the number of IAV particles produced by lican Street E360, Seattle, WA 98109. E-mail address: [email protected] the infected chorioallantoic membrane culture was determined Abbreviation used in this article: IAV, influenza A virus. by assessing heme agglutination activity of the supernatant. Copyright Ó 2015 by The American Association of Immunologists, Inc. 0022-1767/15/$25.00 These studies revealed that, when conducted at 37˚C, a www.jimmunol.org/cgi/doi/10.4049/jimmunol.1501575 1910 PILLARS OF IMMUNOLOGY 15-min pre-exposure to inactivated IAV resulted in membrane in- IAV, similar to how defective virus particles can stimulate IFN terference or resistance to infectious virus at 37˚C, because production when viral pathogen-associated molecular patterns only input or lower levels of virus were generated after infec- are revealed during the eclipse phase of the infection and are tious IAV exposure. In these studies, the peak of interference sensed by pattern recognition receptors in the target cells. Their occurred after a 6-h pre-exposure. Moreover, when pre-ex- discovery of IFN, now 58 y ago, led to the identification of posure was conducted at 4˚C, followed by exposure to infec- other IFNs, the IFNRs, JAK-STAT signaling pathways, tious IAV at 37˚C, no interference against infectious IAV was IFN regulatory factors, IFN genes, and the pattern recognition observed, indicating that tissue metabolic events were necessary receptors, such as TLRs and the RIG-I–like receptors that for viral interference to occur. Thus, a synthetic product from induce intracellular signaling to activate IFN regulatory factors the chorioallantoic membrane was likely mediating the interfer- to drive IFN production and the innate immune response to ence against infectious IAV. Further experiments to treat fresh virus infection. Moreover, this work led to studies that membranes with ground-up membranes or supernatant from identified plasmacytoid dendritic cells as the major IFN- membranes that had been exposed to inactivated IAV for 6 h producing cell and provided the foundation for studies that revealed that interference was generated from membrane expo- defined other IFN-producing cell subsets. We know that IFN sure to a soluble product from the virus-exposed membranes. actions are mediated by hundreds of IFN-stimulated genes and Thus, the soluble product was named “interferon.” that specific IFN-stimulated gene actions suppress infection by Isaacs and Lindenmann, with Burke and Valentine (2, 8), IAV and other viruses. Today, pharmacologic IFNs serve as conducted follow-up studies to evaluate the properties of IFN. effective therapeutics for treating virus infection, cancer, and Downloaded from They scaled up their chick embryo chorioallantoic membrane autoimmune disease (10–13). The work of Alick Isaacs and culture system to produce larger quantities of IFN-containing Jean Lindenmann opened the door for these discoveries and supernatant by exposing membranes to inactivated IAV for 3 h, products, with great impact on immunology, virology, micro- washing the membranes in saline, and then culturing them biology, and public health.
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