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Identification and Structure Elucidation of the Pro-Resolving Mediators

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Identification and Structure Elucidation of the Pro-Resolving Mediators British Journal of British Journal of Pharmacology (2019) 176 1024–1037 1024 Pharmacology Themed Section: Eicosanoids 35 years from the 1982 Nobel: where are we now? REVIEW ARTICLE Identification and structure elucidation of the pro-resolving mediators provides novel leads for resolution pharmacology Correspondence Dr Jesmond Dalli, William Harvey Research Institute, John Vane Science Centre, Charterhouse Square, London EC1M 6BQ, UK. E-mail: [email protected] Received 27 November 2017; Revised 13 February 2018; Accepted 16 February 2018 Jesmond Dalli1 and Charles N Serhan2 1Lipid Mediator Unit, William Harvey Research Institute, Barts and the London School of Medicine, Queen Mary University of London, London, UK, and 2Center for Experimental Therapeutics and Reperfusion Injury, Department of Anaesthesia, Perioperative and Pain Medicine, Building for Transformative Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA Inflammatory diseases are a major socio-economic burden, with the incidence of such conditions on the rise, especially in western societies. For decades, the primary treatment paradigm for many of these conditions was to develop drugs that inhibit or antagonize the production and biological actions of molecules that were thought to be the culprits in propagating disease; these include cytokines and eicosanoids. This approach is effective in controlling disease propagation; however, long-term exposure to these anti-inflammatories is also associated with many side effects, some of which are severe, including immune-suppression. The discovery that termination of self-limited acute inflammation is an active process orchestrated by endogenous mediators, including the essential fatty acid-derived resolvins, protectins and maresins, has provided novel opportunities for the design of therapeutics that control inflammation with a lower burden of side effects. This is because at variance to anti-inflammatories, pro- resolving mediators do not completely inhibit inflammatory responses; instead, these mediators reprogramme the immune response to accelerate the termination of inflammation, facilitating the regain of function. The scope of this review is to highlight the biological actions of these autacoids and their potential utility as lead compounds in developing resolution pharmacology- based therapeutics. LINKED ARTICLES This article is part of a themed section on Eicosanoids 35 years from the 1982 Nobel: where are we now? To view the other articles in this section visit http://onlinelibrary.wiley.com/doi/10.1111/bph.v176.8/issuetoc Abbreviations 13-HDPA, 13-(R)-hydroxy-7Z,10Z,13R,14E,16Z,19Z-docosapentaenoic acid; 13-HpDPA, 13-(R)-hydroxyperoxy- 7Z,10Z,13R,14E,16Z,19Z-docosapentaenoic acid; 13S, 14S-epoxy-MaR, 13S,14S-epoxy-4Z,7Z,9E,11E,16Z,19Z- docosahexaenoic acid; 17R-RvD3, 4S,11R,17R-trihydroxy-5Z,7E,9E,13Z,15E,19Z-docosahexaenoic acid; ALX, lipoxin A4 receptor; BLT1 receptor, LTB4 receptor; DHA, docosahexaenoic acid; DSS, dextran sodium sulphate; EPA, eicosapentaenoic acid; LOX, lipoxygenase; LXA4, 5S,6R,15S-trihydroxy-7E,9E,11Z,13E-eicosatetraenoic acid; MaR, maresin; MaR1, 7R,14S- dihydroxy-4Z,8E,10E,12Z,16Z,19Z-docosahexaenoic acid; MaR1n-3 DPA, 7R,14Sdihydroxy-8E,10E,12Z,16Z,19Z- docosapentaenoic acid; MaR2, 13R,14S-dihydroxy-4Z,7Z,9,11,16Z,19Z-docosahexaenoic acid; MaRn-3 DPA,n- 3docosapentaenoic acid-derived maresins; MCTR, maresin conjugates in tissue regeneration; MCTR1, 13R- glutathionyl,14S-hydroxy-4Z,7Z,9E,11E,13R,14S,16Z,19Z-docosahexaenoic acid; MCTR2, 13R-cysteinylglycinyl,14S-hy- droxy-4Z,7Z,9E,11E,13R,14S,16Z,19Z-docosahexaenoic acid; MCTR3, 13R-cysteinyl,14S-hydroxy- 4Z,7Z,9E,11E,13R,14S,16Z,19Z-docosahexaenoic acid; miRNA, microRNA; n-3 DPA, n-3 docosapentaenoic acid; NALP3, NACHT, LRR and PYD domains-containing protein 3; NSAIDs, non-steroidal anti-inflammatory drugs; PCTR, protectin conjugates in tissue regeneration; PCTR1, 16R-glutathionyl,17S-hydroxy-4Z,7Z,10Z,12E,14E,19Z-docosahexaenoic acid; DOI:10.1111/bph.14336 © 2018 Queen Mary University of London. British Journal of Pharmacology published by John Wiley & Sons Ltd on behalf of British Pharmacological Society. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, pro- vided the original work is properly cited. SPM as templates for resolution pharmacology PD, protectin; PD1, 10R,17S-dihydroxy-4Z,7Z,11E,13E,15Z,19Z-docosahexaenoic acid; PD1n-3 DPA, 10R,17S-dihydroxy- 7Z,11E,13E,15Z,19Z-docosapentaenoic acid; PDn-3 DPA, n-3 docosapentaenoic acid-derived protectin; RCTR, resolvin conjugates in tissue regeneration; Rv, resolvin; RvD, docosahexaenoic acid-derived resolvins; RvD1, 7S,8R,17S-trihydroxy- 4Z,9E,11E,13Z,15E,19Z-docosahexaenoic acid; RvD2, 7S,16R,17S-trihydroxy-4Z,8E,10Z,12E,14E,19Z-docosahexaenoic acid; RvD3, 4S,11R,17S-trihydroxy-5Z,7E,9E,13Z,15E,19Z-docosahexaenoic acid; RvD4, 4S,5R,17S-trihydroxy- 6E,8E,10Z,13Z,15E,19Z-docosahexaenoic acid; RvD5, 7S,17S-dihydroxy-4Z,8E,10Z,13Z,15E,19Z-docosahexaenoic acid; RvDn-3 DPA, n-3 docosapentaenoic acid-derived resolvins; RvE, eicosapentaenoic acid derived resolvins; RvE1, 5S,12R,18R- trihydroxy-6Z,8E,10E,14Z,16E-eicosapentaenoic acid; RvE2, 5S,18R-trihydroxy-6E,8Z,11Z,14Z,16E-eicosapentaenoic acid; RvE3, 17,18-dihydroxy-5Z,8Z,11Z,13E,15E-eicosapentaenoic acid; RvT, thirteen series resolvins; SPM, specialized pro- resolvin mediators; TRPV1, transient receptor potential cation channel subfamily V member 1 During evolution, multicellular organisms arose and cells For many years, termination of inflammation was within an organism became specialized to perform specific thought to occur via the simple dilution of inflammatory tasks leading to the formation of organs and tissues. These signals from the site of injury or infection, leading to the specialized organs required protection from invading egress of white blood cells and re-establishment of tissue microbes as well as mechanisms to repair and regenerate function (Robbins and Cotran, 1979). Studies focusing on damaged tissues and organs, thus paving the way to the evo- mechanisms that control the termination of inflammation lution of the immune system (Malagoli, 2016). In higher demonstrated that arachidonic acid is not only a substrate organisms, the immune system is divided into two arms, the in the biosynthesis of inflammation-initiating molecules, innate arm provides the front line defence system and the such as PGs and leukotrienes, but is converted to protective adaptive arm provides protection from insults and/or patho- and anti-inflammatory molecules that include the lipoxins gens to which the body was previously exposed. In some (Serhan et al., 1984; Levy et al., 2001) and the cyclopentenone instances, immune responses may become dysregulated PGs (Gilroy et al., 1999). Identification of these molecules leading to disease. It is now appreciated that a significant por- indicated that resolution of inflammation is an active process tion of diseases that afflict western societies are associated coordinated by autacoids produced at the site that control with unbridled inflammation leading to damage of vital immune cell responses. Introducing quantitation indices organs and tissues resulting in malaise and ultimately death to mark resolution permitted the delineation of the (Kumar et al., 2014; Majno, 1991). in vivo biological actions of pro-resolving mediators, includ- Classically, the inflammatory response has been divided ing the lipoxins, resolvins and protectins, during acute in- into two phases, the initiation and resolution (or termina- flammation (Bannenberg et al., 2005; Schwab et al., 2007). tion) phases (Kumar et al., 2014). Many studies conducted Detailed studies investigating mechanisms controlling the primarily in the last century focused on determining the termination of inflammation also uncovered a link be- mechanisms and molecules produced during the initiation tween the inflammation-initiating eicosanoids PGE2 and phase, demonstrating that this was a tightly orchestrated PGD2 and lipoxin biosynthesis. These PGs are important response with the production of several classes of molecules in up-regulating the expression of 15-lipoxygenase type 1 that are involved in the recruitment of different leukocyte (15-LOX-1), the initiating enzyme in the lipoxin biosyn- subsets and include the cytokines, chemokines and the thetic pathway (Levy et al., 2001). Of note, inhibition of classic eicosanoids (Kumar et al., 2014). Interested readers PG biosynthesis using NSAIDs is linked to a reduction in on the biology of these mediators are directed to articles in the biosynthesis of specialized pro-resolving mediators this special edition as well as to Samuelsson (2012) and and a delay in the termination of inflammation in experi- Dinarello and Joosten (2016). The identification of these mental systems (Fukunaga et al., 2005). Thus, these studies molecules also paved the way to the development of demonstrated that the acute inflammatory response is a innovative therapeutics for the treatment of many inflamma- coordinated process with the initiation and termination tory diseases that revolutionized medicine and medical phases being intricately linked. practice. The drugs were designed to inhibit or antagonize These initial observations also raised the question the biological actions and the production of local mediators whether novel molecules are produced during acute inflam- that were identified to be important in disease onset
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