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A peaceful death orchestrates immune balance in a chaotic environment
Saturday, 2019/11/23 | 04:46:03

Adam C. Soloff and  Michael T. Lotze; PNAS November 12, 2019 116 (46) 22901-22903.


Figure: The context of recognition of HMGB1 mediates proinflammatory or proresolution functionality in macrophages. Free HMGB1 released by nonapoptotic cell death signals through RAGE to induce 5-LO nuclear translocation and IRF5 expression, resulting in differentiation of proinflammatory macrophages and subsequent leukotriene B4 production. By contrast, HMGB1 complexed with C1q forms a tetramolecular signaling complex with RAGE and LAIR-1 receptors, retaining 5-LO in the cytoplasm and inducing the production of specialized proresolving lipid mediators (SPMs), lack of IRF5 expression, and generation of proresolving macrophages. The context of HMGB1 recognition including location, kinetics, and duration may alternately affect the resolution or propagation of inflammation.


Immunity evolved as an impossibly elegant, yet devastatingly destructive force to combat pathogens, environmental insults, and rogue malignant cellular agents arising from within. The immunologic arsenal developed in a veritable coevolutionary arms race with the world’s pathogens, culminating in lymphocytic weapons of mass destruction. Indeed, T cells and B cells endowed with antigen specificity, the capacity for clonal expansion, and most importantly, long-lived memory, represent the pinnacle of such evolution. Together with the innate immune response, the adaptive immune system holds the power to mediate sustained inflammatory responses with such voracity that tissues, organs, or the host itself may endure critical collateral damage. To preserve balance, adaptive immunity has developed under the guiding principle of primum non nocere, or “first, to do no harm,” limiting the aggression of the innate immune response (e.g., septic shock, penumbra of cerebrovascular and brain infarcts). Herein, redundant mechanisms to preclude aberrant deleterious immunity have evolved as the predominant state of being, establishing a significant molecular and cellular threshold to initiate and maintain inflammation. Often overlooked, following the excitement of the active immune response, are the critical means by which the host resolves the inflammatory process, restoring local and systemic balance. The findings by Liu et al. (1) provide further description of molecular processes and cellular mediators of the resolution process, shedding light on mechanistic aspects of immune homeostasis.


Defining the underlying cellular, molecular, and signaling mechanisms of chronic inflammation is of significant interest, as interventional strategies that facilitate resolution may inhibit the pathogenesis of autoimmune disease, diseases of aging, chronic infections, and cancer. Unresolved inflammation may lead to sustained local and/or systemic exposure to HMGB1/C1q complexes, the consequences of which are unknown. Recent studies have demonstrated that hematopoietic stem cells and hematopoietic progenitor cells (collectively, HSPCs) of the bone marrow are responsive to peripheral inflammation via pattern recognition receptors and cytokine signaling. Inflammatory signals can promote rapid myelopoiesis from HSPCs via differentiation and asymmetric division with distinct monocyte-committed progenitors giving rise to classical monocytes with unique transcriptomic profiles and function (12). Furthermore, epigenetic regulation, consisting of heritable histone modifications, DNA methylation, and the effects of noncoding RNAs, has been implicated in inflammatory gene expression, conferring a type of memory on these innate postmitotic cells. Exposure to environmental stimuli induces epigenetic reprogramming at the level of histone acetylation and methylation, which endows macrophages with proinflammatory and antiinflammatory properties, establishing a predilection toward anamnestic responses in the future (3). Heritable epigenetic modifications imprinted following HMGB1/C1q exposure that are maintained within self-renewing bone marrow progenitors, long-lived monocytes, or tissue-resident macrophages may establish a persistent state of maladaptive immunity by subverting effector functions necessary for either the induction or resolution of inflammatory responses. Furthermore, chronic HSPC exposure to HMGB1/C1q complexes may result in enhanced myelopoiesis leading to the overrepresentation of monocyte/macrophages, disrupting homeostasis, and promoting chronic inflammation. Understanding the mechanism of action of mediators of resolution and their context-dependent effects upon acute and chronic inflammatory disease will be instrumental in identifying clinical applications of these immunoregulatory agents not only in autoimmunity but also in chronic viral infections and cancer as well as acute events such as cerebrovascular accidents, myocardial infarction, and trauma.


See: https://www.pnas.org/content/116/46/22901

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