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Influenza Virus–Specific Human Antibody Repertoire Studies Influenza Virus−Specific Human Antibody Repertoire Studies James E. Crowe, Jr. This information is current as J Immunol 2019; 202:368-373; ; of September 25, 2021. doi: 10.4049/jimmunol.1801459 http://www.jimmunol.org/content/202/2/368 Downloaded from References This article cites 44 articles, 17 of which you can access for free at: http://www.jimmunol.org/content/202/2/368.full#ref-list-1 Why The JI? Submit online. http://www.jimmunol.org/ • 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 *average by guest on September 25, 2021 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 © 2019 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Influenza Virus–Specific Human Antibody Repertoire Studies James E. Crowe, Jr. The diversity of Ag-specific adaptive receptors on the by the error-prone nature of the viral RNA-dependent RNA surface of B cells and in the population of secreted polymerase, which frequently introduces missense mutations. Abs is enormous, but increasingly, we are acquiring This occurrence is challenging because antigenic drift is thus the technical capability to interrogate Ab repertoires caused by accumulating point mutations in the genes encoding in great detail. These Ab technologies have been espe- HA and NA. Some of these mutations encode escape mutations cially pointed at understanding the complex issues of for Abs, and these viruses can be selected over time and enriched immunity to infection and disease caused by influenza in the population. Gradual genetic drift in HA and NA genes virus, one of the most common and vexing medical causes the antigenic variation that reduces the protective effect Downloaded from of seasonal influenza vaccines. Genetic drift in influenza occurs problems in man. Influenza immunity is particularly in- in a direction over time (1), such that older individuals possess teresting as a model system because the antigenic diver- immunity to older strains, in patterns that can be recognized by sity of influenza strains and proteins is high and the decade of birth. Human repertoire studies suggest that the constantly evolving. Discovery of canonical features potential diversity of the human Ab repertoire far exceeds that in the subset of the influenza repertoire response that of the influenza Ag diversity, but the problem for vaccine pre- http://www.jimmunol.org/ is broadly reactive for diverse influenza strains has vention of new strains is a matter of timing. Our current in- spurred the recent optimism for creating universal in- fluenza vaccine strategy is to make educated guesses about the fluenza vaccines. Using new technologies for sequencing likely dominant drifted strains based on molecular epidemiol- Ab repertoires at great depth is helping us to understand ogy studies and then to manufacture trivalent (with H1N1, the central features of influenza immunity. The Jour- H3N2, and B Ags) or quadrivalent (adding a second type B nal of Immunology, 2019, 202: 368–373. strainAg)vaccinesstarting∼6 mo before the season. In some cases, the dominant drifted strain can be mismatched antigen- ically, leading to suboptimal efficacy. Broader human Ab re- by guest on September 25, 2021 he B cell repertoire diversity (D) gene studies with sponses are desirable. Understanding the genetic and structural influenza are interesting because of the wide extent of basis for broadly protective Abs is a major current goal of the T influenza variability. Influenza virus exhibits a signifi- influenza immune repertoire field. cant challenge to the human immune system because of anti- genic variability in field strains. The virus achieves genetic and Concepts of repertoire antigenic D by two principal genetic mechanisms resulting in The vocabulary surrounding the concept of repertoire is antigenic shift and antigenic drift. Influenza causes periodic variously applied. In a broad sense, a repertoire is the collection human pandemics because the segmented viral genome allows of specificities that can comprise the variable (V) gene re- the creation of new viruses during coinfection of cells with ceptors in the adaptive immune system. Vaccine scientists and viruses of two different antigenic subtypes. Genetic reassortment infectious diseases investigators typically envision the adaptive of the segments mixed during coinfection with avian, swine, and immune repertoire as a functional system with diverse pat- human viruses allows complete changing of the surface proteins terns of antigenic recognition. In this sense, the influenza hemagglutinin (HA) and neuraminidase (NA) to subtypes never repertoire is the collection of clones that recognize particular seen by humans, resulting in antigenic shifts. Such shifts or influenza HA or NA molecules or collections of molecules adaptation of avian viruses for human transmission were asso- with varying patterns of epitope recognition, breadth, and ciated with large human pandemics caused by H1N1 in 1918, potency. This type of repertoire study is conducted mostly H2N2 in 1957, H3N2 in 1968, and a new H1N1 in 2009. with proteins and viruses, using binding and virus inhibition The virus has a second genetic mechanism for diversity caused assays and electron microscopic and crystallographic structural Vanderbilt Vaccine Center, Vanderbilt University Medical Center, Nashville, TN Address correspondence and reprint requests to Dr. James E. Crowe, Departments of 37232; Department of Pathology, Microbiology, and Immunology, Vanderbilt Univer- Pediatrics, and Pathology, Microbiology and Immunology, Vanderbilt Vaccine Center, sity Medical Center, Nashville, TN 37232; and Department of Pediatrics, Vanderbilt 11475 Medical Research Building IV, 2213 Garland Avenue, Nashville, TN 37232- University Medical Center, Nashville, TN 37232 0417. E-mail address: [email protected] ORCID: 0000-0002-0049-1079 (J.E.C.). Abbreviations used in this article: D, diversity; HA, hemagglutinin; indel, insertion/ deletion; J, joining; NA, neuraminidase; NGS, next generation sequencing; RBS, recep- Received for publication October 31, 2018. Accepted for publication November 20, tor binding site; V, variable. 2018. This work was supported by National Institutes of Health Grant U19 AI117905, U.S. Copyright Ó 2019 by The American Association of Immunologists, Inc. 0022-1767/19/$37.50 Department of Health and Human Services Contract HHSN272201400024C, and a grant from the Human Vaccines Project. www.jimmunol.org/cgi/doi/10.4049/jimmunol.1801459 The Journal of Immunology 369 determinations. From a more fundamental immunological HA head domain Abs. The most common human Ab responses viewpoint, the adaptive immune receptor repertoire alter- to influenza HA are directed to the head domain, especially the natively can be studied as a genetic system, comprising the RBS. Many head domain–specific mAbs with excellent neu- recombined gene sequences encoding the receptors. This tralizing potency have been isolated. The challenge for head type of repertoire study is conducted with DNA sequencing domain–based immunity is that the helices and loops sur- technologies, especially deep sequencing with next genera- rounding the RBS are hypervariable. Much of the head do- tion sequencing (NGS) techniques. In this article, we will main surface is very mutable, without disturbing the review both types of repertoire concepts, first the functional attachment and fusion functions mediated by HA. As above, concepts and second the genetic concepts. the antigenic drift is directional in both a genetic and an Functional classes of Abs revealed by recent influenza B cell studies. antigenic manner, and the effect of small numbers of amino Protective Abs for influenza are directed to the two surface acid changes can have outsized effects within an antigenic proteins HA and NA. There has been much more Ab and cluster of residues if they facilitate evasion of a dominant B cell work done on the response to the HA molecule than immune response (16). Some Abs bind to the RBS directly NA. The trimeric HA glycoprotein can be roughly thought and block attachment to sialic acid–bearing receptors (an ef- of in antigenic terms as comprising two major domains, the fect that can be mimicked in the hemagglutination inhibition membrane proximal stem domain and the membrane distal assay using RBCs, which are rich in surface sialic acid). a globular head domain. Neutralizing and protective Abs have Changes in HA receptor specificity (from the 2,3 sialic acid a Downloaded from been isolated that recognize head or stem. binding preference of avian strains to the 2,6 sialic acid preference in human transmissible strains) drives some of the HA stem domain Abs more dramatic changes in the HA head domains, especially in The recognition of human Abs to the stem region is relatively the RBS. When a major shift in receptor specificity occurs, new. When the avian H5N1 viruscrossedspeciesfrombirds only a small subset of broadly neutralizing
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