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1.
Molecular Immunology 57
(2014) 1 Contents lists available at ScienceDirect Molecular Immunology journal homepage: www.elsevier.com/locate/molimm Editorial The pathogenesis of ankylosing spondylitis: HLA-B27 and beyond It is no exaggeration to assert that the last few years witnessed a series of critical discoveries with a revolutionary impact on our perception of the nature and pathogenesis of ankylosing spondylitis (AS) and on the role of HLA-B27 in this disease. These discoveries converge from multiple approaches, from genetics to biochemical, functional and in vivo studies, from animal models to patient-based and translational research, from hypothesis-driven to hypothesisfree strategies, to draw, at last, a coherent and unified picture. In the following articles, some of the major investigators in this field lucidly address the major issues and propose their views on the pathogenetic mechanism of AS. Genetic studies, discussed by Philip Robinson and Matthew Brown, have identified a growing number of genes influencing AS. Among these, ERAP1 and other aminopeptidases involved in processing of MHC-I ligands underline the critical role of peptides in AS. Genes involved in the IL-23 pathway provide the genetic evidence for the central position of this cytokine in AS substantiated by functional, animal, and clinical studies. Genes influencing the development and differentiation of CD8+ T cells, such as RUNX3, might challenge the idea, arising mainly from animal models, that these cells are irrelevant in the human disease. These issues are developed in depth in subsequent articles. The biology of ERAP1, discussed by Carlos Alvarez-Navarro and myself, provides a molecular basis to explain the epistasis of this gene and HLA-B27 in AS, revealed by genetic studies. ERAP1 has a global effect on the HLA-B27 peptidome that may alter, not only the antigen presenting-properties of the MHC molecule, but also other biological and pathogenetic features. Thus, while supporting a pivotal role of peptides, the association of ERAP1 with AS does not necessarily imply a pathogenetic role of specific epitopes, as initially proposed by the arthritogenic peptide hypothesis. But, can we really rule out a role of CD8+ T-cell-mediated antigen recognition in AS? In a very suggestive review Rosa Sorrentino, Rainer Böckmann and Maria Teresa Fiorillo focused on the structural/dynamic and antigen-presenting properties of HLA-B27 to propose that a predisposition to autoimmunity might be the downside of its high efficiency as a restriction element in protective immune responses. Four reviews address what are probably the core issues to our understanding of AS: (1) the nature of the inflammatory pathways, (2) the relationship between inflammation and new bone formation, and (3) the pathogenetic role of HLA-B27 in triggering or exacerbating inflammation and bone remodeling. The inflammatory pathways in AS are reviewed by Hulda Hreggvidsdottir, Troy Noordenbos and Dominique Baeten. These 0161-5890/$ – see front matter © 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.molimm.2013.08.001 authors highlight the relevance of several proinflammatory cytokines, in particular membrane-bound TNF and the IL-23/IL-17 axis. In a timely discussion, they examine the relationship between inflammation and osteoproliferation and the role of these cytokines in driving both processes. The converging evidence towards a central role of IL-23 is lucidly reviewed by Jonathan Sherlock and Daniel Cua, who emphasize the relevance of the entheses as the primary pathological sites. Their hallmark identification of a resident, IL-23-responsive, T-cell population in the entheses helps to explain both enthesitis and local bone remodeling in response to the up-regulation of IL-23. The evidence connecting molecular and biological features of HLA-B27 with its capacity to activate the IL-23/IL-17 axis is a major advance in our understanding of the pathogenetic role of HLA-B27. Atleast two pathways are emerging with increasing clarity. The first one is prompted by HLA-B27 misfolding and subsequent activation of the unfolded protein response. The issue is reviewed by Robert Colbert, Tri Tran and Gerlinde Lay-Schmitt. The authors discuss the evidence, mainly from transgenic animal models, that HLAB27 misfolding leads to induction of IL-23, IFN and IL-1␣, the two latter cytokines modulating osteoclast development. This mechanism would directly connect HLA-B27 with critical inflammatory and bone remodeling pathways. The second mechanism may be mediated by the capacity of HLA-B27 heavy chain homodimers at the cell surface to induce the production of IL-17 from KIR3DL2+ CD4+ T cells, and possibly also by additional immunomodulatory effects of the homodimer/KIR3DL2 interaction on NK cells. The issue is brightly discussed by Jackie Shaw, Hiroko Hatano and Simon Kollnberger in a dense and timely review of the biochemical an immunological studies dealing with the nature, origin and immunology of HLA-B27 homodimers. In preparing this special issue for Molecular Immunology and reading the articles included in it, I must say that, for the first time in more than 30 years devoted to the study of this disease, a plausible picture of AS pathogenesis and the role of HLA-B27 in it emerged at last in my mind. To be sure, it is still a blurred image, full of insufficiencies that must be addressed by future research. Yet, the major questions that resisted the efforts of researchers and clinicians for so many years start to fit as the solution of a long-sought puzzle. José A. López de Castro E-mail address: aldecastro@cbm.uam.es Available online 27 August 2013
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