Item type:Thesis, Open Access

Unraveling the immunopathogenesis of pemphigus with new research approaches: in-depth analysis of systemic and local T cell responses

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Philipps-Universität Marburg

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Abstract

The immune system functions as a sophisticated collaboration between the innate and adaptive immunity capable of distinguishing self from non-self. A pivotal role in governing adaptive immune responses is attributed to CD4+ T cells. With specificity for a particular antigen, they facilitate the establishment of protective immunity targeted at specific pathogens, but their actions can also inadvertently give rise to autoimmunity. One such example is pemphigus, a rare autoimmune disease affecting skin and mucous membranes. Pemphigus manifests as blister formations and erosions and is characterized by the loss of immune tolerance to desmosomal cadherins, particularly desmoglein (Dsg)1 and Dsg3. Autoreactive T cells provide help to B cells and thus play a central role in driving the production of pathogenic IgG autoantibodies against these cadherins. However, due to their low frequencies, detection of autoreactive T cells in pemphigus has been challenging. Traditional methods like tritiated thymidine incorporation (3H-TdR) or enzyme-linked immunospot (ELISpot) analysis have inherent limitations, including the inability to distinguish specific cell populations or the need for an ab initio presumption of the significance of certain cytokines. Newer experimental approaches, focused on direct characterization and quantification of these T cells, are based on flow cytometry. Some make use of MHC multimers others of surface activation markers. We aimed at establishing a method of detecting autoreactive CD4+ T cells utilizing the transient upregulation of CD154 (CD40L) upon stimulation with relevant antigens or immunodominant epitopes, respectively. The CD154-method of antigen-specific T cell detection is sensitive, time-efficient, and withal allows for specific phenotypic and functional characterization of T cells when using a comprehensive panel of immunological parameters. Herewith, we analyzed Dsg3-specific CD4+CD154+ T cells from peripheral blood of patients with pemphigus vulgaris (PV) in comparison to healthy control (HC), where the expression of CD154 on ex vivo expanded CD4+ T cells positively correlated with Dsg3 titers in pemphigus patients. We could show clonal expansion of CD4+CD154+ T cells in response to both, the full protein Dsg3 as well as to various epitope-specific peptides, with P2 (extracellular domain 2 of Dsg3) appearing to be particularly immunomodulatory in PV patients. Moreover, upregulation of IL-17 and IL-21 was seen to associate with antigen-specific activation in active stages of the disease, further supporting the concept that immune activity in PV relies, at least partially, on Dsg3-reactive Th17/Tfh17 cell subsets. Contrary to foregoing belief that in pemphigus the subtype of T cells responsible for supporting autoreactive B cells is IL-4- and IL-5-producing Th2 cells. With newly discovered T cell populations such as Th9 cells, Th22 cells and many others, the inherent complexity of the pathomechanisms of pemphigus will likely become even more evident, with different subsets presumably dominating at different stages of the disease contributing to the complex interplay of immune dysregulation in pemphigus. Pemphigus is an autoimmune disease mediated by systemic immune responses, however, the inflammation is localized in the peripheral effector tissues, namely mucosa and the skin. More and more studies shed light on the importance of local tissue-resident immunity in pemphigus. Yet, owing to hampered peripheral tissues’ accessibility and difficulty in extracting the resident lymphocytes, blood remains a major source of research material. Hence, we aimed at establishing a rapid easy-to-use protocol to isolate a sufficient number of viable immune cells from small skin biopsies that can be directly used for a deeper characterization such as comprehensive phenotyping and functional studies of T cells. Since it is not yet clear what role local immunity plays in the disease's pathogenesis and how important the balance among different T cell subsets in pemphigus is, the need for further research to unravel its complexities is inherent. These newly established methods, CD154 for detection of Dsg-reactive T cells and rapid isolation of lymphocytes from skin and mucosa, aid to expedite the process and allow for closer inspection of pemphigus’ pathogenesis. Moreover, the presented comprehensive immunophenotyping of PV patients underlines the significance of Th17/Tfh17 cells, T cell dysregulation, enhanced B cell activation, and elevated pro-inflammatory cytokines, which collectively contribute to the autoimmune response observed in pemphigus. Thus, these new findings not only provide deeper insights into the pathomechanism but may also reveal improved treatment options for pemphigus patients in the future.

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Alexandra Polakova (0000-0002-4792-9306): Unraveling the immunopathogenesis of pemphigus with new research approaches: in-depth analysis of systemic and local T cell responses. : Philipps-Universität Marburg 2025-08-06. DOI: https://doi.org/10.17192/z2025.0328.