Immune resolution mechanisms in inflammatory arthritis

The past two decades have witnessed major advancements in the clinical management of inflammatory arthritis, with new treatment strategies in some cases providing a marked improvement in patient outcomes. However, it is widely accepted that current strategies do not provide the 'total therapeutic solution', in view of the proportion of patients who do not respond to therapy, the important incidence of adverse effects and the development of an immune response against antibodies or fusion proteins used therapeutically. Moreover, although some therapeutic approaches can effectively bring about an end to inflammation, mechanisms to promote the recovery and/or repair of damage are required. Harnessing the concepts and mechanisms of the resolution of inflammation is a new approach to the treatment of inflammatory pathologies; this approach could help address the unmet need for new therapeutic approaches that not only control but also revert the course of inflammatory rheumatic diseases.

[1]  L. Baum,et al.  Endothelial cell expression of galectin-1 induced by prostate cancer cells inhibits T-cell transendothelial migration , 2006, Laboratory Investigation.

[2]  M. Ehrenstein,et al.  Regulatory T‐cells in systemic lupus erythematosus and rheumatoid arthritis , 2011, FEBS letters.

[3]  J. Markworth,et al.  Divergent shifts in lipid mediator profile following supplementation with n‐3 docosapentaenoic acid and eicosapentaenoic acid , 2016, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[4]  F. Montecucco,et al.  Sulphasalazine accelerates apoptosis in neutrophils exposed to immune complex: Role of caspase pathway , 2009, Clinical and experimental pharmacology & physiology.

[5]  Benhur Lee,et al.  Galectin-1 Regulates Tissue Exit of Specific Dendritic Cell Populations , 2015, The Journal of Biological Chemistry.

[6]  M. Perretti,et al.  Inhibitory control of endothelial galectin‐1 on in vitro and in vivo lymphocyte trafficking , 2008, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[7]  M. Perretti,et al.  Connections in pharmacology: innovation serving translational medicine. , 2014, Drug discovery today.

[8]  J. Schwab,et al.  Anesthetics Impact the Resolution of Inflammation , 2008, PloS one.

[9]  B. Cronstein,et al.  Methotrexate—how does it really work? , 2010, Nature Reviews Rheumatology.

[10]  Trevor A. Mori,et al.  Specialised pro-resolving mediators of inflammation in inflammatory arthritis. , 2016, Prostaglandins, leukotrienes, and essential fatty acids.

[11]  D. Irimia,et al.  Proresolving and cartilage-protective actions of resolvin D1 in inflammatory arthritis , 2016, JCI insight.

[12]  J. Pelletier,et al.  Human articular chondrocytes express 15-lipoxygenase-1 and -2: potential role in osteoarthritis , 2009, Arthritis research & therapy.

[13]  M. Perretti,et al.  Spatial and Temporal Profiles for Anti-Inflammatory Gene Expression in Leukocytes during a Resolving Model of Peritonitis1 , 2006, The Journal of Immunology.

[14]  N. Gibran,et al.  Spatial and Temporal Localization of the Melanocortin 1 Receptor and Its Ligand α–Melanocyte-Stimulating Hormone during Cutaneous Wound Repair , 2011, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[15]  Yu Lin,et al.  Augmentation of Myocardial Production of 15-Epi-Lipoxin-A4 by Pioglitazone and Atorvastatin in the Rat , 2006, Circulation.

[16]  F. Blanco,et al.  Effect of hydrogen sulfide sources on inflammation and catabolic markers on interleukin 1β-stimulated human articular chondrocytes. , 2014, Osteoarthritis and cartilage.

[17]  K. Varani,et al.  Adenosine as a Multi-Signalling Guardian Angel in Human Diseases: When, Where and How Does it Exert its Protective Effects? , 2016, Trends in pharmacological sciences.

[18]  K. Varani,et al.  A2A and A3 adenosine receptor expression in rheumatoid arthritis: upregulation, inverse correlation with disease activity score and suppression of inflammatory cytokine and metalloproteinase release , 2011, Arthritis research & therapy.

[19]  R. Lechler,et al.  Galectin-1: a key effector of regulation mediated by CD4+CD25+ T cells. , 2007, Blood.

[20]  G. Majno Inflammation and infection: historic highlights. , 1982, Monographs in pathology.

[21]  M. Perretti,et al.  Evidence for an Anti-Inflammatory Loop Centered on Polymorphonuclear Leukocyte Formyl Peptide Receptor 2/Lipoxin A4 Receptor and Operative in the Inflamed Microvasculature , 2011, The Journal of Immunology.

[22]  K. Brown,et al.  Galectin 3 aggravates joint inflammation and destruction in antigen-induced arthritis. , 2011, Arthritis and rheumatism.

[23]  S. Moncada,et al.  Antiinflammatory activity of soluble guanylate cyclase: cGMP-dependent down-regulation of P-selectin expression and leukocyte recruitment. , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[24]  D. Daoussis,et al.  ACTH as a treatment for acute crystal-induced arthritis: update on clinical evidence and mechanisms of action. , 2014, Seminars in arthritis and rheumatism.

[25]  K. Urabe,et al.  Antiinflammatory mediator lipoxin A4 and its receptor in synovitis of patients with rheumatoid arthritis. , 2007, The Journal of rheumatology.

[26]  R. Medzhitov Origin and physiological roles of inflammation , 2008, Nature.

[27]  M. Perretti,et al.  A vasculo-protective circuit centered on lipoxin A4 and aspirin-triggered 15-epi-lipoxin A4 operative in murine microcirculation. , 2013, Blood.

[28]  D. Gilroy,et al.  Inducible cyclooxygenase may have anti-inflammatory properties , 1999, Nature Medicine.

[29]  V. Kuchroo,et al.  The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity , 2005, Nature Immunology.

[30]  T. Luger,et al.  The melanocortin system in articular chondrocytes: melanocortin receptors, pro-opiomelanocortin, precursor proteases, and a regulatory effect of alpha-melanocyte-stimulating hormone on proinflammatory cytokines and extracellular matrix components. , 2009, Arthritis and rheumatism.

[31]  E. Motta,et al.  The precursor of resolvin D series and aspirin‐triggered resolvin D1 display anti‐hyperalgesic properties in adjuvant‐induced arthritis in rats , 2011, British journal of pharmacology.

[32]  G. Rabinovich,et al.  Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10 , 2009, Nature Immunology.

[33]  C. Serhan,et al.  Identification and Actions of a Novel Third Maresin Conjugate in Tissue Regeneration: MCTR3 , 2016, PloS one.

[34]  Yan Lu,et al.  Mediator-lipidomics: databases and search algorithms for PUFA-derived mediators. , 2005, Journal of lipid research.

[35]  T. Niki,et al.  Beneficial effect of galectin 9 on rheumatoid arthritis by induction of apoptosis of synovial fibroblasts. , 2007, Arthritis and rheumatism.

[36]  M. Perretti,et al.  Ligand-specific conformational change of the G-protein–coupled receptor ALX/FPR2 determines proresolving functional responses , 2013, Proceedings of the National Academy of Sciences.

[37]  M. Perretti,et al.  Resolution Pharmacology: Opportunities for Therapeutic Innovation in Inflammation. , 2015, Trends in pharmacological sciences.

[38]  M. Perretti,et al.  Endogenous Galectin-1 Exerts Tonic Inhibition on Experimental Arthritis , 2013, The Journal of Immunology.

[39]  C. Serhan,et al.  Inhaled Carbon Monoxide Accelerates Resolution of Inflammation via Unique Proresolving Mediator–Heme Oxygenase-1 Circuits , 2013, The Journal of Immunology.

[40]  L. Joosten,et al.  Alpha-1-anti-trypsin-Fc fusion protein ameliorates gouty arthritis by reducing release and extracellular processing of IL-1β and by the induction of endogenous IL-1Ra , 2015, Annals of the rheumatic diseases.

[41]  L. Joosten,et al.  12/15-Lipoxygenase Counteracts Inflammation and Tissue Damage in Arthritis , 2009, The Journal of Immunology.

[42]  C. Serhan,et al.  Proresolving Nanomedicines Activate Bone Regeneration in Periodontitis , 2015, Journal of dental research.

[43]  B. Levy,et al.  Maresin 1 biosynthesis during platelet–neutrophil interactions is organ-protective , 2014, Proceedings of the National Academy of Sciences.

[44]  M. Hamberg,et al.  Lipoxins: novel series of biologically active compounds formed from arachidonic acid in human leukocytes. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[45]  A. R. Moore,et al.  Resolution of Inflammation in Murine Autoimmune Arthritis Is Disrupted by Cyclooxygenase-2 Inhibition and Restored by Prostaglandin E2-Mediated Lipoxin A4 Production , 2010, The Journal of Immunology.

[46]  D. Gilroy,et al.  New insights into the resolution of inflammation. , 2015, Seminars in immunology.

[47]  F. D’Acquisto,et al.  Annexin A1 and glucocorticoids as effectors of the resolution of inflammation , 2009, Nature Reviews Immunology.

[48]  M. Perretti,et al.  Microparticle alpha-2-macroglobulin enhances pro-resolving responses and promotes survival in sepsis , 2013, EMBO molecular medicine.

[49]  R. Hannon,et al.  Corrections: Anti-Inflammatory Role of the Murine Formyl-Peptide Receptor 2: Ligand-Specific Effects on Leukocyte Responses and Experimental Inflammation , 2011, The Journal of Immunology.

[50]  H2S transiently blocks IL‐6 expression in rheumatoid arthritic fibroblast‐like synoviocytes and deactivates p44/42 mitogen‐activated protein kinase , 2010, Cell biology international.

[51]  O. Rådmark,et al.  Expression of 5-lipoxygenase and 15-lipoxygenase in rheumatoid arthritis synovium and effects of intraarticular glucocorticoids , 2009, Arthritis research & therapy.

[52]  C. Reutelingsperger,et al.  Endogenous annexin A1 is a novel protective determinant in nonalcoholic steatohepatitis in mice , 2014, Hepatology.

[53]  S. Yamamoto,et al.  Lipoxin synthase activity of human platelet 12-lipoxygenase. , 1993, The Biochemical journal.

[54]  T. Schall,et al.  Overcoming hurdles in developing successful drugs targeting chemokine receptors , 2011, Nature Reviews Immunology.

[55]  L. O’Driscoll,et al.  Biological properties of extracellular vesicles and their physiological functions , 2015, Journal of extracellular vesicles.

[56]  B. Pesce,et al.  Simvastatin and Benznidazole-Mediated Prevention of Trypanosoma cruzi-Induced Endothelial Activation: Role of 15-epi-lipoxin A4 in the Action of Simvastatin , 2015, PLoS neglected tropical diseases.

[57]  M. Perretti,et al.  Molecular engineering of short half-life small peptides (VIP, αMSH and γ3MSH) fused to latency-associated peptide results in improved anti-inflammatory therapeutics , 2011, Annals of the rheumatic diseases.

[58]  S. Shuto,et al.  Determination of ω-6 and ω-3 PUFA metabolites in human urine samples using UPLC/MS/MS , 2015, Analytical and Bioanalytical Chemistry.

[59]  B. Levy,et al.  Human Sepsis Eicosanoid and Proresolving Lipid Mediator Temporal Profiles: Correlations With Survival and Clinical Outcomes , 2017, Critical care medicine.

[60]  M. Perretti,et al.  Control of Myeloid Cell Trafficking in Resolution , 2013, Journal of Innate Immunity.

[61]  I. McInnes,et al.  Cytokines as Therapeutic Targets in Rheumatoid Arthritis and Other Inflammatory Diseases , 2015, Pharmacological Reviews.

[62]  M. Hersberger,et al.  High levels of anti-inflammatory and pro-resolving lipid mediators lipoxins and resolvins and declining docosahexaenoic acid levels in human milk during the first month of lactation , 2013, Lipids in Health and Disease.

[63]  C. Weber,et al.  Annexin A1 counteracts chemokine-induced arterial myeloid cell recruitment. , 2015, Circulation research.

[64]  Ruth E. Hartley,et al.  An integrated view. , 1973 .

[65]  M. Perretti,et al.  Annexin A1 Mediates Hydrogen Sulfide Properties in the Control of Inflammation , 2014, The Journal of Pharmacology and Experimental Therapeutics.

[66]  I. McInnes,et al.  Comparison of lipid and lipid-associated cardiovascular risk marker changes after treatment with tocilizumab or adalimumab in patients with rheumatoid arthritis , 2015, Annals of the rheumatic diseases.

[67]  Charles N. Serhan,et al.  Molecular circuits of resolution: formation and actions of resolvins and protectins , 2005, The Journal of Immunology.

[68]  G. Rabinovich,et al.  Expression of galectins-1 and -3 correlates with defective mononuclear cell apoptosis in patients with juvenile idiopathic arthritis. , 2001, The Journal of rheumatology.

[69]  Charles N. Serhan,et al.  Pro-resolving lipid mediators are leads for resolution physiology , 2014, Nature.

[70]  O. Farokhzad,et al.  Annexin A1-containing extracellular vesicles and polymeric nanoparticles promote epithelial wound repair. , 2015, The Journal of clinical investigation.

[71]  R. Clark,et al.  Development of a Nascent Galectin-1 Chimeric Molecule for Studying the Role of Leukocyte Galectin-1 Ligands and Immune Disease Modulation , 2010, The Journal of Immunology.

[72]  F. Dell’Accio,et al.  Neutrophil-derived microvesicles enter cartilage and protect the joint in inflammatory arthritis , 2015, Science Translational Medicine.

[73]  Oliver Soehnlein,et al.  Resolution of inflammation: an integrated view , 2013, EMBO molecular medicine.

[74]  R. Burgos-Vargas,et al.  A decrease in galectin-1 (Gal-1) levels correlates with an increase in anti-Gal-1 antibodies at the synovial level in patients with rheumatoid arthritis , 2013, Scandinavian journal of rheumatology.

[75]  M. Perretti,et al.  Association between periodontal disease and inflammatory arthritis reveals modulatory functions by melanocortin receptor type 3. , 2014, The American journal of pathology.

[76]  C. Serhan,et al.  The resolution code of acute inflammation: Novel pro-resolving lipid mediators in resolution. , 2015, Seminars in immunology.

[77]  N. Petasis,et al.  Lipoxins, aspirin-triggered epi-lipoxins, lipoxin stable analogues, and the resolution of inflammation: stimulation of macrophage phagocytosis of apoptotic neutrophils in vivo. , 2002, Journal of the American Society of Nephrology : JASN.

[78]  R. Cummings,et al.  Dimeric Galectin-1 Induces Surface Exposure of Phosphatidylserine and Phagocytic Recognition of Leukocytes without Inducing Apoptosis* , 2003, Journal of Biological Chemistry.

[79]  J. Wallace,et al.  Gaseous mediators in resolution of inflammation. , 2015, Seminars in immunology.

[80]  M. Perretti,et al.  Biased Agonism as a Novel Strategy To Harness the Proresolving Properties of Melanocortin Receptors without Eliciting Melanogenic Effects , 2015, The Journal of Immunology.

[81]  M. Perretti,et al.  Gene expression signature-based approach identifies a pro-resolving mechanism of action for histone deacetylase inhibitors , 2012, Cell Death and Differentiation.

[82]  C. Buckley,et al.  The role of stromal cells in the persistence of chronic inflammation , 2013, Clinical and experimental immunology.

[83]  Trevor A. Mori,et al.  Maternal dietary omega-3 fatty acid intake increases resolvin and protectin levels in the rat placenta , 2013, Journal of Lipid Research.

[84]  P. Grieco,et al.  Anti-inflammatory and antiosteoclastogenesis properties of endogenous melanocortin receptor type 3 in experimental arthritis. , 2010, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[85]  C. Serhan,et al.  Molecular Circuits of Resolution: Formation and Actions of Resolvins and Protectins1 , 2005, The Journal of Immunology.

[86]  J. M. Cousin,et al.  Glucocorticoids promote nonphlogistic phagocytosis of apoptotic leukocytes. , 1999, Journal of immunology.

[87]  C. Müller,et al.  Selective Activation of Adenosine A2A Receptors on Immune Cells by a CD73-Dependent Prodrug Suppresses Joint Inflammation in Experimental Rheumatoid Arthritis , 2012, Science Translational Medicine.

[88]  Chuan Wu,et al.  Galectin-9-CD44 interaction enhances stability and function of adaptive regulatory T cells. , 2014, Immunity.

[89]  C. Serhan,et al.  Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators. , 2012, Blood.

[90]  J. Shaw,et al.  Chemokine blockers--therapeutics in the making? , 2006, Trends in pharmacological sciences.

[91]  B. Levy,et al.  Lovastatin Decreases Acute Mucosal Inflammation Via 15-epi-Lipoxin A4 , 2010, Mucosal Immunology.

[92]  J. Schifferli,et al.  Activated polymorphonuclear neutrophils disseminate anti-inflammatory microparticles by ectocytosis. , 2004, Blood.

[93]  Trinidad Montero-Melendez,et al.  ACTH: The forgotten therapy. , 2015, Seminars in immunology.

[94]  T. Niki,et al.  Galectin-9 suppresses the generation of Th17, promotes the induction of regulatory T cells, and regulates experimental autoimmune arthritis. , 2008, Clinical immunology.

[95]  J. Filep,et al.  Resolvin E1 promotes phagocytosis-induced neutrophil apoptosis and accelerates resolution of pulmonary inflammation , 2012, Proceedings of the National Academy of Sciences.

[96]  L. Baum,et al.  Apoptosis of T cells mediated by galectin-1 , 1995, Nature.

[97]  J. McQualter,et al.  Serum amyloid A opposes lipoxin A4 to mediate glucocorticoid refractory lung inflammation in chronic obstructive pulmonary disease , 2012, Proceedings of the National Academy of Sciences.

[98]  D. Gilroy,et al.  Proresolving lipid mediators and mechanisms in the resolution of acute inflammation. , 2014, Immunity.

[99]  A. Dief,et al.  Hydrogen sulfide releasing naproxen offers better anti-inflammatory and chondroprotective effect relative to naproxen in a rat model of zymosan induced arthritis. , 2015, European review for medical and pharmacological sciences.

[100]  C. Serhan,et al.  Human Milk Proresolving Mediators Stimulate Resolution of Acute Inflammation , 2015, Mucosal Immunology.

[101]  Y. Kawaoka,et al.  The Lipid Mediator Protectin D1 Inhibits Influenza Virus Replication and Improves Severe Influenza , 2013, Cell.

[102]  F. D’Acquisto,et al.  The impact of endogenous annexin A1 on glucocorticoid control of inflammatory arthritis , 2012, Annals of the rheumatic diseases.

[103]  H. Christian,et al.  Activation of melanocortin type 3 receptor as a molecular mechanism for adrenocorticotropic hormone efficacy in gouty arthritis. , 2002, Arthritis and rheumatism.

[104]  M. Perretti,et al.  Annexin 1 mediates the rapid anti-inflammatory effects of neutrophil-derived microparticles. , 2008, Blood.

[105]  B. Cronstein,et al.  Methotrexate and sulfasalazine promote adenosine release by a mechanism that requires ecto-5'-nucleotidase-mediated conversion of adenine nucleotides. , 1998, The Journal of clinical investigation.

[106]  P. Hench,et al.  The effect of a hormone of the adrenal cortex (17-hydroxy-11-dehydrocorticosterone; compound E) and of pituitary adrenocorticotropic hormone on rheumatoid arthritis. , 1949, Proceedings of the staff meetings. Mayo Clinic.

[107]  R. Sapolsky,et al.  How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. , 2000, Endocrine reviews.

[108]  R. Alon,et al.  Leukocyte migration into inflamed tissues. , 2014, Immunity.

[109]  T. Niki,et al.  Immunopathology and Infectious Diseases Endogenous Galectin-1 and Acute Inflammation Emerging Notion of a Galectin-9 Pro-Resolving Effect , 2011 .

[110]  S. Quezada,et al.  Resolution of acute inflammation bridges the gap between innate and adaptive immunity. , 2014, Blood.

[111]  D. Willis,et al.  Heme oxygenase: A novel target for the modulation of inflammatory response , 1996, Nature Medicine.

[112]  C. Serhan,et al.  Proresolving actions of a new resolvin D1 analog mimetic qualifies as an immunoresolvent. , 2015, American journal of physiology. Lung cellular and molecular physiology.

[113]  Christopher Haslett,et al.  Cyclin-dependent kinase inhibitors enhance the resolution of inflammation by promoting inflammatory cell apoptosis , 2006, Nature Medicine.

[114]  G. Rabinovich,et al.  Recombinant Galectin-1 and Its Genetic Delivery Suppress Collagen-Induced Arthritis via T Cell Apoptosis , 1999, The Journal of experimental medicine.

[115]  B. Cronstein,et al.  Adenosine A2A Receptor Activation Prevents Wear Particle–Induced Osteolysis , 2012, Science Translational Medicine.

[116]  M. Perretti Endogenous mediators that inhibit the leukocyte-endothelium interaction. , 1997, Trends in pharmacological sciences.

[117]  J. Wallace,et al.  Hydrogen sulfide-based therapeutics: exploiting a unique but ubiquitous gasotransmitter , 2015, Nature Reviews Drug Discovery.

[118]  A. Gutman,et al.  Effects of adrenocorticotropic hormone (ACTH) in gout. , 1950, The American journal of medicine.

[119]  I. McInnes,et al.  Changes in lipid levels with inflammation and therapy in RA: a maturing paradigm , 2013, Nature Reviews Rheumatology.

[120]  C. Piantadosi,et al.  Cell-cell interactions and bronchoconstrictor eicosanoid reduction with inhaled carbon monoxide and resolvin D1. , 2014, American journal of physiology. Lung cellular and molecular physiology.

[121]  M. Paul-Clark,et al.  Modulation of inflammation and response to dexamethasone by Annexin 1 in antigen-induced arthritis. , 2004, Arthritis and rheumatism.

[122]  M. Perretti,et al.  Proresolving Actions of Synthetic and Natural Protease Inhibitors Are Mediated by Annexin A1 , 2016, The Journal of Immunology.

[123]  D. Zeldin,et al.  Resolvin Infectious Inflammation by Targeting the Host Response. , 2015, The New England journal of medicine.

[124]  M. Giera,et al.  Lipid and lipid mediator profiling of human synovial fluid in rheumatoid arthritis patients by means of LC-MS/MS. , 2012, Biochimica et biophysica acta.

[125]  Dief Ae,et al.  Hydrogen sulfide releasing naproxen offers better anti-inflammatory and chondroprotective effect relative to naproxen in a rat model of zymosan induced arthritis. , 2015 .

[126]  J. Wallace,et al.  Hydrogen sulfide is an endogenous modulator of leukocyte‐mediated inflammation , 2006, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[127]  M. Perretti,et al.  Novel insights into the inhibitory effects of Galectin‐1 on neutrophil recruitment under flow , 2008, Journal of leukocyte biology.

[128]  C. Serhan,et al.  Elucidation of novel 13-series resolvins that increase with atorvastatin and clear infections , 2015, Nature Medicine.

[129]  F. Liew,et al.  Low expression of CD39 on regulatory T cells as a biomarker for resistance to methotrexate therapy in rheumatoid arthritis , 2015, Proceedings of the National Academy of Sciences.

[130]  V. Blaho,et al.  5-Lipoxygenase–Deficient Mice Infected with Borrelia burgdorferi Develop Persistent Arthritis , 2011, The Journal of Immunology.

[131]  Charles N. Serhan,et al.  Infection Regulates Pro-Resolving Mediators that Lower Antibiotic Requirements , 2012, Nature.

[132]  P. Grieco,et al.  Melanocortin peptides protect chondrocytes from mechanically induced cartilage injury. , 2014, Biochemical pharmacology.

[133]  C. Serhan,et al.  Identification and signature profiles for pro-resolving and inflammatory lipid mediators in human tissue. , 2014, American journal of physiology. Cell physiology.

[134]  T. Niki,et al.  Galectin-9 ameliorates immune complex-induced arthritis by regulating Fc gamma R expression on macrophages. , 2009, Clinical immunology.

[135]  P. Calder,et al.  Influence of marine n-3 polyunsaturated fatty acids on immune function and a systematic review of their effects on clinical outcomes in rheumatoid arthritis , 2012, British Journal of Nutrition.

[136]  S. Grässel,et al.  Role of proopiomelanocortin-derived peptides and their receptors in the osteoarticular system: from basic to translational research. , 2012, Endocrine reviews.

[137]  G. Rabinovich,et al.  Galectin-1 induces 12/15-lipoxygenase expression in murine macrophages and favors their conversion toward a pro-resolving phenotype. , 2013, Prostaglandins & other lipid mediators.

[138]  Takanori Nakamura,et al.  Galectin-8 and galectin-9 are novel substrates for thrombin. , 2006, Glycobiology.

[139]  M. Perretti,et al.  Cutting Edge: Humanized Nano-Proresolving Medicines Mimic Inflammation-Resolution and Enhance Wound Healing , 2011, The Journal of Immunology.

[140]  M. Perretti,et al.  Investigational Analysis Reveals a Potential Role for Neutrophils in Giant-Cell Arteritis Disease Progression , 2014, Circulation research.

[141]  M. Teixeira,et al.  The Required Role of Endogenously Produced Lipoxin A4 and Annexin-1 for the Production of IL-10 and Inflammatory Hyporesponsiveness in Mice1 , 2007, The Journal of Immunology.

[142]  O. Farokhzad,et al.  Targeted nanoparticles containing the proresolving peptide Ac2-26 protect against advanced atherosclerosis in hypercholesterolemic mice , 2015, Science Translational Medicine.