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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

    Effector Responses of Adaptive Immunity

    Lymphocyte-Mediated Effector Responses

    Delayed hypersensitivity T lymphocytes

    Delayed hypersensitivity (previously termed Coombs and Gell type IV) represents the prototypical adaptive immune mechanism for lymphocyte-triggered inflammation. It is especially powerful in secondary immune responses. Previously primed DH CD4+ T lymphocytes leave the lymph node, home into local tissues where antigen persists, and become activated by restimulation with the specific priming antigen and MHC class II–expressing APCs. Fully activated DH T lymphocytes secrete mediators and cytokines, leading to the recruitment and activation of macrophages and/or other nonspecific leukocytes (Fig 2–7). The term delayed for this type of hypersensitivity refers to the fact that the reaction becomes maximal 12–48 hours after antigen exposure.

    Analysis of experimental animal models and the histologic changes of human inflammation suggest that different subtypes of DH might exist. One of the most important determinants of the pattern of DH reaction is the subtype of DH CD4+ effector T cells that mediate the reaction. Just as helper T lymphocytes can be differentiated into 3 groups—Th1, Th2, and Th17 subsets—according to the spectrum of cytokines secreted, DH T lymphocytes can also be grouped by the same criteria. Experimentally, the Th1 subset of cytokines, especially IFN-γ (also known as macrophage-activating factor) and TNF-β, activates macrophages to secrete inflammatory mediators and kill pathogens, thus amplifying inflammation. Th1-mediated DH mechanisms, therefore, are thought to produce the following effects:

    • the classic DH reaction (eg, the purified protein derivative [PPD] skin reaction)

    • immunity to intracellular infections (eg, to mycobacteria or Pneumocystis organisms)

    • immunity to fungi

    • most forms of severe T-lymphocyte–mediated autoimmune diseases

    • chronic transplant rejection

    Figure 2-7 Schematic representation of CD4+ T lymphocyte development. After initial priming in the lymph node, CD4+ T lymphocytes enter the tissue site, where they again encounter APCs containing processed antigen. Upon restimulation and depending on the cytokines present in the local environment at the time of restimulation, they become activated into 1 of at least 4 subtypes. T regulatory lymphocytes (Tregs) suppress other T-cell responses. Th1 lymphocytes are the classic delayed-hypersensitivity effector cells and mediate IFN-γ–driven responses. Th2 lymphocytes are thought to be less intensively inflammatory and have been associated with parasite-induced granulomas and atopic diseases. Th17 lymphocytes mediate and sustain inflammation.

    (Illustration developed by Russell W. Read, MD, PhD.)

    Table 2–3 summarizes ocular inflammatory diseases thought to require a major contribution of Th1 DH effector mechanisms.

    The Th2 subset of DH cells secretes IL-4, IL-5, and other cytokines. IL-4 can induce B lymphocytes to synthesize IgE, and IL-5 can recruit and activate eosinophils within a site. IL-4 can also induce macrophage granulomas in response to parasite-derived antigens.

    Table 2-3 Ocular Inflammatory Diseases Likely Involving Th1-Mediated DH Effector Mechanisms

    Thus, Th2-mediated DH mechanisms are thought to play a major role in the following:

    • response to parasite infections

    • late-phase responses of allergic reactions

    • asthma

    • atopic dermatitis or other manifestations of atopic diseases

    The persistence of certain infectious agents, especially bacteria within intracellular compartments of APCs and certain extracellular parasites, can cause destructive induration with granuloma formation and giant cells, termed the granulomatous form of DH. However, immune complex deposition and innate immune mechanisms in response to heavy metal or foreign-body reactions can also cause granulomatous inflammation, in which the inflammatory cascade (resulting in DH) is triggered in the absence of specific T lymphocytes. Unfortunately, for most clinical entities in which T-lymphocyte responses are suspected, especially autoimmune disorders such as multiple sclerosis or rheumatoid arthritis, the precise immunologic mechanisms remain highly speculative. See Clinical Example 2–3.

    Th17 cells have also been implicated in DH responses. Depending on the local microenvironment, Th cells can also change lineage-specific functions. For example, Th17 cells can gain the ability to secrete Th1 cytokines. They can also switch to a Treg phenotype. This immune plasticity is valuable to homeostasis, minimizing tissue damage associated with DH responses, while maintaining effective microbial clearance.

    Cytotoxic lymphocytes

    Cytotoxic T lymphocytes Cytotoxic T lymphocytes (CTLs) are a subset of antigen-specific T lymphocytes, usually bearing the CD8 marker, that are especially good at killing tumor cells and virus-infected cells. The CTLs can also mediate graft rejection and some types of autoimmunity. In most cases, the ideal antigen for CTLs is an intracellular protein that occurs naturally or is produced because of viral infection. The CTLs appear to require help from CD4+ helper T-lymphocyte signals to fully differentiate. Primed precursor CTLs leave the lymph node and migrate to the target tissue, where they are restimulated by the interaction of the CTL antigen receptor and foreign antigens within the antigen pocket of MHC class I molecules (HLA-A, -B, or -C) on the target cell. Additional CD4+ T lymphocytes help at the site, and expression of other accessory costimulatory molecules on the target is often required to obtain maximal killing.

    CLINICAL EXAMPLE 2-3

    Toxocara granuloma (Th2 DH) Toxocara canis is a nematode parasite that infects up to 2% of all children worldwide. It can occasionally produce inflammatory vitreoretinal manifestations. Although the ocular immunology of this disorder is not clearly delineated, animal models and a study of the immunopathogenesis of human nematode infections at other sites suggest the following scenario. The primary immune response begins in the gut after ingestion of viable eggs, which mature into larvae within the intestine. The primary processing phase produces a strong Th2 response, leading to a primary effector response that includes production of IgM, IgG, and IgE antibodies, as well as Th2-mediated DH T lymphocytes. Accidental avoidance of immune effector mechanisms may result in hematogenous dissemination of a few larvae to the choroid or retina, followed by invasion into the retina and/or vitreous. There, a Th2-mediated T-lymphocyte effector response recognizes larva antigens and releases Th2-derived cytokines to induce eosinophil and macrophage infiltration, causing the characteristic eosinophilic granuloma seen in the eye. In addition, antilarval B lymphocytes can infiltrate the eye and are induced to secrete various immunoglobulins, especially IgE. Finally, eosinophils, in part by attachment through Fc receptors, can recognize IgE or IgG bound to parasites and release cytotoxic granules containing the antiparasitic cationic protein directly near the larvae, using a mechanism similar to antibody-dependent cellular cytotoxicity.

    • Grencis RK. Th2-mediated host protective immunity to intestinal nematode infections. Philos Trans R Soc Lond B Biol Sci. 1997;352(1359):1377–1384.

    Sympathetic ophthalmia (Th1 DH) Sympathetic ophthalmia is a bilateral panuveitis that follows penetrating trauma to an eye. This disorder represents one of the few human diseases in which autoimmunity can be directly linked to an initiating event. In most cases, penetrating injury activates the afferent phase. It is unclear whether the injury causes a de novo primary immunization to self-antigens—perhaps because of externalization of sequestered uveal antigens through the wound and exposure to the afferent immune response arc of the conjunctiva or extraocular sites—or if the injury instead somehow changes the immunologic microenvironment of the retina, retinal pigment epithelium (RPE), and uvea so that a secondary afferent response is initiated that serves to alter preexisting tolerance to retinal and uveal self-antigens.

    The inflammatory effector response is generally thought to be dominated by a Th1-mediated DH mechanism generated in response to uveal or retinal antigens. CD4+ T lymphocytes predominate early in the disease course, although CD8+ T lymphocytes can be numerous in chronic cases. Activated macrophages are also numerous in granulomas, and Th1 cytokines have been identified in the vitreous or produced by T lymphocytes recovered from the eyes of affected patients. Although the target antigen for sympathetic ophthalmia is unknown, cutaneous immunization in experimental animals with certain retinal antigens (arrestin, rhodopsin, interphotoreceptor retinoid-binding protein), RPE-associated antigens, and melanocyte-associated tyrosinase can induce autoimmune uveitis with physiology or features suggestive of sympathetic ophthalmia. Th1-mediated DH is thought to mediate many forms of ocular inflammation. Table 2–3 lists other examples.

    • Boyd SR, Young S, Lightman S. Immunopathology of the noninfectious posterior and intermediate uveitides. Surv Ophthalmol. 2001;46(3): 209–233.

    Cytotoxic T lymphocytes kill cells in 1 of 2 ways: “assassination” or “suicide” induction (Fig 2–8). Assassination refers to CTL-mediated lysis of targets. A specialized pore-forming protein called perforin is released that inserts into cell membranes and causes osmotic lysis of the cell. Suicide induction refers to the capability of CTLs to stimulate programmed cell death of target cells, called apoptosis, using the CD95 ligand (FasL) to activate the CD95 receptor (Fas) on target cells. Alternatively, CTLs can release cytokines such as TNF to induce apoptosis. The CTLs produce low-grade lymphocytic infiltrate within tumors or infected tissues and usually kill without causing significant inflammation.

    Natural killer cells Natural killer (NK) cells are a subset of non-T, non-B lymphocytes. They kill tumor cells and virus-infected cells using the same molecular mechanisms as CTLs. Unlike CTLs, NK cells do not have a specific antigen receptor. Instead, they are triggered by receptors that may be activating or inhibitory. Activating receptors trigger the NK cell to kill target cells that display molecules that should not be present or cells that are missing MHC Class I molecules. Inhibitory NK receptors prevent NK cells from indiscriminately attacking healthy host tissue by recognizing ligands that ought to be present. There are several families of NK receptors, including C-type lectin receptors (CTLRs) and killer immunoglobulin-like receptors (KIRs). Because NK cells are not antigen specific, theoretically the response does not have the time delay associated with induction of the adaptive, antigen-specific CTL immune response. However, NK cells do require some of the same effector activation signals at the tissue site, especially cytokine stimulation. Thus, NK cells are probably most effective in combination with adaptive effector responses.

    Figure 2-8 Schematic representation of the 2 major mechanisms of CD8+ T-lymphocyte cytotoxicity. CD8+ T lymphocytes, having undergone initial priming in the lymph node, enter the tissue site, where they again encounter antigen in the form of infected target cells. Upon restimulation, usually requiring CD4+ helper T-lymphocyte factors, they become activated into fully cytotoxic T lymphocytes. CTLs can kill by lysing the infected cell using a pore-forming protein called perforin or by inducing programmed cell death, called apoptosis, using either FasL or cytokine-mediated mechanisms.

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

    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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