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  • 2020–2021 BCSC Basic and Clinical Science Course™

    Go to Academy Store Learn more and Purchase.

    9 Uveitis and Ocular Inflammation

    Chapter 2: Immunization and Adaptive Immunity: The Immune Response Arc and Immune Effectors

    Phases of the Immune Response Arc

    Processing Phase

    The conversion of an antigenic stimulus into an immunologic response occurs through priming of naive B and T lymphocytes (lymphocytes that have not yet encountered their specific antigen) within lymph nodes and the spleen. This conversion is also called activation, or sensitization, of lymphocytes. Processing involves regulation of the interaction between antigen and naive lymphocytes, followed by lymphocyte activation (Fig 2–4).

    Preconditions necessary for processing

    CD4+ T lymphocytes are the principal cell type for immune processing. These lymphocytes have a receptor that detects antigen only upon formation of a trimolecular complex consisting of an HLA molecule, a processed antigen fragment, and a T-lymphocyte antigen receptor. The CD4+ molecule stabilizes binding and enhances signaling between the HLA complex on the APC and the T-lymphocyte receptor. When helper T lymphocytes recognize their specific antigen, they become primed and partially activated, acquiring new functional properties, including cell division, cytokine synthesis, and cell membrane expression of accessory molecules, such as cell-adhesion molecules and costimulatory molecules. The synthesis and release of immune cytokines, especially interleukin-2 (IL-2), by T lymphocytes is crucial for the progression of initial activation and the functional differentiation of T lymphocytes through autocrine stimulation.

    Figure 2-2 Class I–dependent antigen-presenting cells (APCs). 1, APC is infected by a virus, which causes the cell to synthesize virus-associated peptides that are present in the cytosol. 2, The viral antigen must be transported (through specialized transporter systems) into the endosomal compartment (endoplasmic reticulum, ER), where the viral antigen encounters human leukocyte antigen (HLA) class I molecules. The fragment is placed into the pocket formed by the α chain of the class I HLA molecule. Unlike class II molecules, the second chain, called β2-microglobulin, is constant among all class I molecules. 3, The CD8 T-lymphocyte receptor recognizes the fragment–class I complex displayed on the cell membrane. 4, With the help of costimulatory molecules such as CD28-B7 and cytokines, the CD8+ T lymphocyte becomes primed, or partially activated. A similar mechanism is used to recognize tumor antigens that are produced by cells after malignant transformation.

    (Illustration by Barb Cousins, modified by Joyce Zavarro.)

    Figure 2-3 Class II–dependent antigen-presenting cells. 1, APCs endocytose exogenous antigens into the endosomal compartment. 2, There, the antigen is digested into peptide fragments and placed into the groove formed by the α and β chains of the HLA class II molecule. 3, The CD4+ T-lymphocyte receptor recognizes the fragment–class II complex. 4, With the help of costimulatory molecules such as CD28-B7 and cytokines, the CD4+ T lymphocyte becomes primed, or partially activated.

    (Illustration by Barb Cousins, modified by Joyce Zavarro.)

    Helper T-lymphocyte differentiation

    At the stage of initial priming, CD4+ T lymphocytes are classified as T helper-0 (Th0) cells. These cells can differentiate into functional subsets based on the pattern of cytokines to which they are exposed. Each T-helper (Th) subset produces a characteristic profile of cytokines that is regulated by the expression of subset-specific transcription factors. When the Th subsets were discovered, only 2 were defined: T helper-1 (Th1) and T helper-2 (Th2). Th1 cells secrete interferon gamma (IFN-γ), IL-2, and tumor necrosis factor α and β (TNF-α, TNF-β), whereas Th2 cells produce IL-4, IL-5, and IL-10 but not Th1 cytokines. The T-bet transcription factor directs the Th1 cytokine production. The GATA3 transcription factor regulates Th2 cytokines. The Th2 subset is involved in the clearance of extracellular pathogens and plays an important role in the pathogenesis of allergic conditions such as asthma. Th1 cells participate in the elimination of intracellular pathogens as well as cell-mediated and delayed-type hypersensitivity reactions.

    Figure 2-4 Schematic illustration of immune processing of antigen within the lymph node. On exposure to antigen and APCs within the lymph node, the 3 major lymphocyte subsets—B lymphocytes, CD4+ T lymphocytes, and CD8+ T lymphocytes—and NK (non-T, non-B) lymphocytes are activated to release specific cytokines and perform specific functional activities. B lymphocytes are stimulated to produce one of the various antibody isotypes, whose functions include complement activation, antibody-dependent cellular cytotoxicity (ADCC), agglutination, allergen recognition, and release into secretions. CD4+ T lymphocytes become activated into T helper-1 (Th1), T helper-2 (Th2), T regulatory (Treg), or T helper-17 (TH17) subsets. Naive CD8+ T cells become cytotoxic T lymphocytes (CTLs), and non-T, non-B lymphocytes become natural killer (NK) lymphocytes.

    (Illustration by Barb Cousins, modified by Joyce Zavarro.)

    Originally, the Th1 subset was thought to be the causal agent in autoimmunity, as transfer of antigen-specific Th1 cells produces autoimmune disease in experimental animal models, and elevated levels of IFN-γ have been detected in areas of inflammation in vivo. Subsequently, research has suggested that other Th subsets, especially Th17 and T regulatory (Treg) cells, play crucial roles in chronic inflammation and autoimmunity, and there is probably plasticity between Th1, Th17, and Treg cells.

    Th17 cells produce IL-17, IL-21, IL-22, and IL-24 in association with several transcription factors, including retinoic acid receptor–related orphan receptor-γt and receptor-α, (ROR-γt and -α). Th17 cells contribute to immunity against certain extracellular bacteria and fungi and play a role in the defense of mucosal surfaces. Dysregulation of Th17 proinflammatory cytokines IL-17 and IL-22 has been implicated in systemic inflammatory diseases, such as psoriasis, rheumatoid arthritis, multiple sclerosis, inflammatory bowel disease, Sjögren syndrome, Behçet disease, and systemic lupus erythematosus, as well as in uveitis and scleritis. See Clinical Example 2-2.

    T regulatory cells are identified by their simultaneous expression of CD4, CD25, and Foxp3 (a transcriptional regulator protein) and can be divided into 2 types, naturally occurring T regulatory (nTreg) cells and inducible T regulatory (iTreg) or adaptive Treg cells. The nTreg cells appear to be generated in the thymus during development. They are essential to self-tolerance, the process by which autoreactive T cells are minimized and their function downregulated. Treg cells are essential for maintaining peripheral tolerance to self-antigens, thereby preventing autoimmune diseases and limiting chronic inflammatory diseases. Furthermore, Treg cells suppress excessive immune responses deleterious to the host. As a result, these cells play a central role in autoimmune diseases, transplantation tolerance, infectious diseases, allergic disease, and tumor immunity. The suppressive cytokines transforming growth factor β (TGF-β) and IL-10 have been implicated as active players in the effector function of Treg cells as regulators of inflammation. An imbalance between regulatory mechanisms that inhibit the immune system and active proinflammatory mechanisms is thought to be the underlying cause of uveitis and many other immune-mediated diseases.

    CLINICAL EXAMPLE 2-2

    The role of Th17 cells in birdshot chorioretinopathy Birdshot chorioretinopathy (BSCR) is a severe, progressive, posterior uveitis. It is typically characterized by multiple distinctive choroidal lesions in the fundus (not always apparent in the initial phase of the disease), vitritis, and retinal vasculitis leading to diffuse capillary leakage and macular/optic disc edema. Uncontrolled BSCR usually leads to extensive retinal atrophy with visual field loss, floaters, glare, and blurred vision. Significant electroretinographic abnormalities are clinically manifested by poor vision in dim lighting, and loss of color and contrast sensitivity. While the link between HLA-A29 and BSCR is well known, the precise pathogenesis of the disease is still unclear. Histopathologic evidence has demonstrated that BSCR choroidal and vitreal infiltrates are predominantly composed of T cells. Studies of cytokine levels suggest that Th17 cells may play an important role in BSCR. The cytokines IL-1β, IL-6, and TGF-β, which contribute to the differentiation of Th17 cells, have been found to be elevated in ocular fluids and serum of BSCR patients. Elevation of IL-17, the hallmark cytokine of Th17, has also been measured in serum from BSCR patients. Elevations of these cytokines have been demonstrated in other types of noninfectious ocular inflammatory disorders, including idiopathic uveitis, Behçet disease, and even scleritis. Knowledge of the role of Th17 in some types of uveitis may guide treatment with commercially available biologic agents that target Th17 cell activity directly or indirectly. Studies of the efficacy of such agents including secukinumab (anti-IL-17), ustekinumab (anti-IL-12 and 23), and tocilizumab (anti-IL-6) as treatment for uveitis are ongoing.

    • Kuiper J, Rothova A, de Boer J, Radstake T. The immunopathogenesis of birdshot chorioretinopathy; a bird of many feathers. Prog Retin Eye Res. 2015;44:99–110.

    The cytokine profiles produced by these various Th cell types determine subsequent immune processing, B-lymphocyte antibody synthesis, and cell-mediated effector responses. For example, IFN-γ, produced by Th1 lymphocytes, blocks the differentiation and activation of Th2 lymphocytes, whereas IL-4, produced by Th2 lymphocytes, blocks the differentiation of Th1 lymphocytes. The process determining whether a Th1 or a Th2 response develops consequent to exposure to a specific antigen is not entirely understood, but presumed variables include cytokines preexisting in the microenvironment, the nature and amount of antigen encountered, and the type of APC involved. For example, IL-12, which is produced by macrophage APCs, might preferentially induce Th1 responses.

    • Abbas AK, Lichtman AH, Pillai S. Cellular and Molecular Immunology. 9th ed. Philadelphia, PA: Elsevier/Saunders; 2018.

    • Amadi-Obi A, Yu CR, Liu X, et al. Th17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat Med. 2007;13(6):711–718.

    • Caspi R. Autoimmunity in the immune privileged eye: pathogenic and regulatory T cells. Immunol Res. 2008;42(1–3):41–50.

    B-lymphocyte activation

    A major function of helper T lymphocytes is B-lymphocyte activation. B lymphocytes are responsible for producing antibodies (glycoproteins that bind to a specific antigen, the epitope). These antibodies contain an epitope-specific binding site, termed paratope, on the Fab (fragment, antigen-binding) portion of the molecule. B lymphocytes begin as naive lymphocytes, with immunoglobulins M (IgM) and D (IgD) on their cell surfaces serving as B-lymphocyte antigen receptors. Through these surface antibodies, B lymphocytes detect epitopes on intact antigens without the requirement of antigen processing by APCs. After appropriate stimulation of the B-lymphocyte antigen receptor, helper T lymphocyte–B lymphocyte interaction occurs, leading to further B-lymphocyte activation and differentiation. B lymphocytes acquire new functional properties, such as cell division, cell surface expression of accessory molecules, and synthesis of large quantities of antibody. The terminal form of B lymphocyte differentiation is the plasma cell that secretes antibodies. Activated B lymphocytes acquire the ability to change antibody class from IgM to another class (eg, to IgG, IgA, or IgE). This class shift requires a molecular change in the immunoglobulin heavy chain, a process regulated by specific cytokines released by the helper T lymphocyte. For example, treatment of an antigen-primed B lymphocyte with IFN-γ induces a switch from IgM to IgG1 production. Treatment with IL-4 induces a switch from IgM to IgE production.

    Excerpted from BCSC 2020-2021 series: Section 9 - Uveitis and Ocular Inflammation. For more information and to purchase the entire series, please visit https://www.aao.org/bcsc.

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