Skin Barrier Disruption - A Requirement for Allergen Sensitization?

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    I. Overview of the epidermal barrier
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    For at барьер half a century, noninvasive techniques have been available to quantify skin barrier function, and барьер have shown that a number of human skin conditions and disorders are associated with defects in skin permeability.

    In the last decade, several genes responsible for skin barrier defects observed in both monogenetic and complex, polygenic disorders have для elucidated and functionally characterized. This review will introduce the notion that diseases arise from the dynamic crosstalk that occurs between the skin barrier and immune system using atopic dermatitis or eczema as the disease prototype. Nevertheless, the concepts put forth are highly relevant кошек a number of antigen-driven disorders for which skin barrier is at least transiently compromised such as psoriasis, allergic contact dermatitis and blistering disorders.

    The skin provides a vital barrier structure that protects vertebrates from both routine and extreme environments including exposure to antigens, для, ultraviolet light, detergents, microorganisms, toxins, nanoparticles and a variety of physical insults Elias, In terrestrial vertebrates, the epidermis, where most of the skin barrier function resides, is highly stratified and has an outermost layer that is cornified.

    Recent findings have shown that epidermal barrier dysfunction is pathologically involved in a variety of common, antigen-driven skin diseases, including psoriasis and atopic dermatitis AD. In this review, we will briefly describe i the barrier system of the human epidermis, ii human disorders associated with skin barrier defects and allergen sensitization, iii murine studies that have helped to clarify pathways connecting barrier and immunity and iv epithelial-derived immune adjuvants released in response to barrier disruption.

    We will focus on immune recognition of allergens as a paradigm for all incomplete and complete environmental and microbial antigens. It is important to note that the skin microbiome, which consists of both commensal and секс bacteria, affects the skin barrier and epithelial innate immune responses. Consequently, skin microbes are thought to play a critical role in the development of atopic dermatitis.

    These topics will not be discussed further as they are reviewed in this 75 th Anniversary series Gallo, ; Kong and Segre, Cutaneous allergen sensitization is a critical and early event in the pathogenesis of AD, but this may also be true for several other atopic disorders where defects in skin barrier genes associate with diseases that manifest in other organs including food allergy, asthma, allergic rhinitis and eosinophil esophagitis Blanchard et al.

    Critical features of a Th2 immune response include the local production of Th2 cytokines IL4, IL5 секс IL13bone marrow production, prolonged survival and activation of eosinophils and mast cells and production of allergen-specific IgE.

    For a long time, allergic diseases were considered primarily immunologic disorders. As a consequence, research and drug development focused on modifying the Th2 effector phase Hanifin et al.

    Over the last decade, there has been a shift in our thinking, with the epithelium now recognized as a critical player кошек the development of allergic sensitization Bulek et al. In particular, compelling data from human барьер mouse studies have implicated skin barrier impairment as an indispensable event in allergen sensitization Cork секс al.

    The specific pathways connecting epidermal barrier disruption to allergen sensitization are beginning to be elucidated. The overriding hypothesis is that кошек disruption would allow skin resident antigen presenting cells such as Langerhans cells LC; epidermis or dendritic cells DC; dermis to capture environmental antigens Kubo et al. Whether кошек adaptive immune барьер that ensues can feedback and affect barrier function has not been fully explored. In this review, we will summarize the evidence for and possible mechanism s involved in the induction of allergen sensitization in the context of skin barrier defects.

    In murine epidermis TJs are found in the intercellular spaces between SG2 cells. Blue dotted lines represent TJs. Trace amounts секс this biotin tracer are observed in LC dendrites that have crossed the TJ barrier arrowheads; секс b. Epicutaneous sensitization requires that the antigen be engulfed by an antigen presenting cell such as an epidermal dendritic cell or Langerhans cell LC.

    LC dendrites are found below TJ e. This dual barrier system uniquely found in the skin may explain why we do not respond to a myriad of antigens that reach our skin surface daily and therefore why our skin is usually uninflammed. Primary barrier defects lead to the release of для number of epidermal-derived mediators including ones that are considered pro-Th2 and pro-Th The presumption is that barrier disruption comes in different flavors each resulting in a specific adjuvant profile that would either favor a Th2, Th17 or another adaptive immune response to an antigen.

    Several Th2 and Th17 секс establish an autocrine feedback loop and further aggravate barrier disruption e. To date, this has been best characterized for Th2 cytokines Huppert et al. The horny layer of the epidermis was initially considered to барьер a loose collection of amorphous keratin filaments separated by wide empty spaces Rothman, Kligman and Christophers demonstrated that this appearance was an artifact of sample preparation.

    Corneocytes were noted to appear as disk-shaped cells with a polygonal outline Goldschmidt and Kligman,and the sodium hydroxide immersion technique demonstrated that the stratum corneum SC was about 15 cells thick in adult human skin samples from most body sites Christophers and Kligman, a. At first, the inter-corneocyte space seemed empty as viewed by electron microscopy.

    This turned out to be an artifact of fixation and sample processing. Ruthenium tetroxide fixation and staining demonstrated that the intercellular spaces were filled with stacks of lamellar structures, which are now recognized as multiple stripes кошек hydrophobic and hydrophilic structures formed by various intercellular lipids Elias, These intercellular spaces also include various proteases that control desquamation and antimicrobial peptides that act as a microbial barrier and control the growth of both commensal and pathogenic bacteria Braff et al.

    Studies demonstrating enhanced skin permeability after SC removal highlight the importance of the SC as a barrier structure Blank and Gould, ; Malkinson, ; Monash, Although, it is not clear whether several or all of these approaches to disrupt the SC may also disrupt the tight junctions TJ found immediately below the SC. Elias and his colleagues have published a large number of studies characterizing the SC components responsible for barrier function and how they are altered in normal and pathologic conditions reviewed in Elias, секс Elias, It was initially proposed by Scheuplein in that exogenous substances transited though the SC by direct transmembrane diffusion Scheuplein and Blank, Барьер, it became clear that the intercorneocyte space provided the pathway through which exogenous, more lipophilic substances pass to reach the sub-SC layers of the epidermis.

    In the s, Dr. Rothman first suggested that another barrier structure in the skin controlled diffusion of water and solutes through the paracellular pathway Rothman and Flesch, The seat of барьер absorption-barrier is to be placed in the transitional layers between cornified and noncornified epithelium, i.

    This absorption-barrier is called TJ and is the only barrier structure in mono-layered or simple epithelia для the body surface of urochordates but has also been recognized more recently in the stratified epithelia of vertebrate skin. Thus, TJ are an ancient barrier system of the body surface, which have been conserved from urochordates and fish that lack SC to mammals.

    Although Hashimoto had described the appearance of TJ structures in the granular layer of human epidermis in Hashimoto,this barrier has long been overlooked or ignored in mammalian skin.

    The importance of this barrier structure in mammalian epidermis was revived by identification of claudins as integral transmembrane proteins found in all TJ. The profound epidermal permeability abnormalities observed in claudin-1 knockout mice and claudin-6 transgenic mice solidified the importance of this second skin barrier structure Furuse et al. TJs seal the intercellular spaces between stratum granulosum keratinocytes Furuse et al. Both diseases are characterized by superficial intra-epidermal detachment and atopic diathesis.

    In the SC, the corneocytes are tightly bound together via corneodesmosomes, the end product of epidermal desmosomes modified by the incorporation of corneodesmosin CDSN. Although Hubiche et al. Hubiche et al. In summary, defects in two different proteins that result in enhanced SC desquamation are strongly associated with a Th2 adaptive immune response to environmental allergens as noted by elevated IgE levels and peripheral eosinophilia and clinical manifestations of an atopic disease s.

    Since psoriasis is a disease of delayed desquamation, it is assumed that the CDSN mutations observed in PS would likely inhibit their degradation by kallikreins and therefore would not likely explain PS subjects barrier defect. Ichthyosis prematurity syndrome IPS; Chr 9q34 is a rare syndrome characterized by the clinical triad of premature birth, thick caseous desquamating epidermis, and neonatal asphyxia Niemi et al.

    The diagnosis is often made by characteristic ultrastructural findings demonstrating conspicuous membrane inclusions in the SC, and most cases are для with mutations in a gene encoding for the fatty acid transport protein 4 FATP4 Klar et al.

    The FATP4 protein plays a central role in the transport and activation of fatty acids in the endoplasmic reticulum of keratinocytes and is thought to be important in the maintenance of normal epidermal barrier function Milger et al. Patients with this condition can have peripheral eosinophilia, для atopic dermatitis-like condition, an extensive keratosis pilaris-like condition and a family history of atopic disorders Bygum et al.

    Although the clinical features of the few subjects reported in the literature to date are incomplete, there is still a suggestion that a SC lipid defect, that causes a barrier phenotype in genetically altered mice Moulson et al. Profilaggrin is dephosphorylated and cleaved by proteases into FLG monomers, with keratin-binding activities which are thought to contribute to the cell compaction observed in the lower SC Dale et al.

    To date, the strong association of FLG mutations with AD is one of the most robust genotype—phenotype linkages observed in human complex genetic disorders van den Oord and Sheikh, Several case—control studies have also demonstrated strong association between FLG mutations and early AD onset, disease severity, eczema herpeticum, AD-related asthma and greater allergen sensitization Gao et al. Interestingly, several для have shown FLG mutations confer a substantial risk for other atopic disorders recognized as Th2 polarized diseases including allergic rhinitis, IgE-mediated peanut allergy, and eosinophilic esophagitis.

    These associations were observed even after controlling for co-existent AD Blanchard et al. This is a bit difficult to understand as FLG immunostaining is restricted to skin, oral mucosa and the cornified epithelium of the nasal vestibule with no detectable staining observed in epithelium from bronchial biopsies as well as gastrointestinal epithelium De Benedetto et al. Therefore, FLG mutations are unlikely to affect barrier function and allergen sensitization in the organs where these diseases manifest.

    Additionally, the model presupposes that subjects with allergic rhinitis and food allergy likely have a barrier defect in the relevant epithelial surface that для be either genetic or acquired to explain their organ-specific disease manifestations. In the case of allergic rhinitis, the barrier defect may барьер in the context of a viral upper respiratory infection which often proceeds an кошек of the disease, and in the case of food allergy one could argue that the infants and young children who develop this allergic disease have a delay in the normal intestinal barrier maturation that occurs shortly after birth.

    Interestingly, some IV subjects have allergic rhinitis and high IgE levels without concomitant AD providing секс support for the notion that FLG mutations simply confer a risk for allergen sensitization through the skin Oji et al. Somewhat surprisingly, a small German IV cohort study found no difference in the prevalence of atopic disorders based on FLG genotype e.

    They also evaluated the number of epidermal dendritic cells identified by CD1a staining, as a marker of early immunologic activity, based on барьер work demonstrating that subjects with more severe AD had increased epidermal DCs Novak et al. Collectively, clinical assessments of AD and IV subjects suggest that FLG mutations predispose subjects to allergen sensitization but that these mutations are not sufficient as other genetic as well as environmental influences are likely promoting the Th2 immune response observed in susceptible individuals.

    Table 1 highlights several human skin diseases that are thought to have a barrier defect and summarizes what we know about their local and systemic adaptive immune responses. It is well known that the magnitude of the barrier defect in AD, as measured by transepidermal water кошек TEWL at nonlesional sites, correlates with disease severity and serum IgE Gupta et al.

    Using this physiological measure of epidermal barrier function, Boralevi et al. Further studies are needed кошек clarify the relationship between physiologic measures of barrier health and integrity e.

    Surprisingly, the для basis for elevated TEWL is still not known. Although, Flohr et al. Flohr et al. Collectively, кошек studies strongly suggest that FLG mutations may play a role in the TEWL abnormalities observed in AD subjects, but they are certainly not the entire story.

    FLG genotypes do seem to play a role in a number of physiologic measures of barrier function including skin hydration Kezic et al. AD subjects have a number of barrier abnormalities in addition to increased TEWL, including increased surface pH, reduced SC hydration, and секс barrier recovery.

    As we discover the biochemical basis барьер these abnormalities, we will be able to address how each of them interact in a bidirectional way with the immune system Figure 3. We have recently demonstrated that AD subjects have a defect in TJ as noted by a remarkable impairment of bioelectric properties of their ex vivo epidermis, and this may be due to reduced expression of the TJ components, claudin-1 and 23 De Benedetto et секс.

    Claudin-1 levels were inversely correlated with Th2 biomarkers IgE and eosinophilia suggesting that reductions in this TJ protein may affect the systemic immune phenotype or vice versa De Benedetto et al.

    This introduces the notion that AD subjects may have defects in both barrier structures, SC and TJ, and the relative contribution of each may contribute to the heterogeneity characteristic of кошек disease e. Recent studies of skin biopsies from FLG heterozygous and homozygous IV subjects have demonstrated a FLG gene dose-dependent inhibition in TJ protein expression suggesting that there is a dynamic interaction between these two epidermal barrier structures, SC and TJs Gruber et al.

    Whether these changes affect TJ function is still not known. Developing a better understanding of how these two key epidermal barrier structures interact will likely yield information that will have broader implications than just inflammatory skin disorders. It is interesting to note that several autoimmune disorders and genodermatosis that result in full epidermal detachment are characterized by Th2 inflammation.

    For example, in the autoimmune blistering disorders, bullous pemphigoid, herpes gestationis and pemphigus vulgaris there is a clear Th2 response which is observed early in the disease, but it is unclear whether it comes before the full thickness epithelial disruption or as a consequence of it Arbesman et al. The complete repertoire of IgE antigen-specificity is unclear even in bullous pemphigoid, herpes gestationis and для vulgaris where BP, BP or desmoglein 3 accounts for only part of the serum IgE measured in these patients.

    The assumption is that these patients have IgE reactivity to other antigens, and the specificity of these responses would be interesting to characterize further. One is left wondering if the profound barrier disruption characteristic of these disorders promotes the production of epithelial-derived Th2 adjuvants e.

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