Neutrophil-derived microvesicles enter cartilage and protect the joint in inflammatory arthritis

Science Translational Medicine

Volumn 7, Issue 315, 2015, Pages

  Headland, Sarah E ^a   Jones, Hefin R ^a   Norling, Lucy V ^a   Kim, Andrew ^b   Souza, Patricia R ^a   Corsiero, Elisa ^a   Gil, Cristiane D ^c   Nerviani, Alessandra ^a   Dell'accio, Francesco ^a,d   Pitzalis, Costantino ^a,d   Oliani, Sonia M ^c   Jan, Lily Y ^b   Perretti, Mauro ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^d BARTS HEALTH NHS TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FORMYL PEPTIDE RECEPTOR 2; GLYCOSAMINOGLYCAN POLYSULFATE; INTERLEUKIN 8; LIPOCORTIN 1; PROSTAGLANDIN E2; PROTEIN TMEM16F; SCRAMBLASE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CARTILAGE DEGENERATION; CARTILAGE MATRIX; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MECHANISM; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IN VITRO STUDY; MALE; MEMBRANE MICROPARTICLE; MOUSE; NEUTROPHIL; NEUTROPHIL COUNT; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; RAT; RHEUMATOID ARTHRITIS; SYNOVIAL FLUID; ANIMAL; ARTICULAR CARTILAGE; BIOSYNTHESIS; METABOLISM; PATHOLOGY;

ANIMALS; ARTHRITIS, RHEUMATOID; CARTILAGE, ARTICULAR; HUMANS; MICE; NEUTROPHILS; SYNOVIAL FLUID; TRANSFORMING GROWTH FACTOR BETA;

EID: 84954197024     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aac5608     Document Type: Article

References (41)

1. J. Keffer, L. Probert, H. Cazlaris, S. Georgopoulos, E. Kaslaris, D. Kioussis, G. Kollias, Transgenic mice expressing human tumour necrosis factor: A predictive genetic model of arthritis. EMBO J. 10, 4025-4031 (1991).
2. S. E. Headland, L. V. Norling, The resolution of inflammation: Principles and challenges. Semin. Immunol. 27, 149-160 (2015).
3. R. J. Berckmans, R. Nieuwland, M. C. Kraan, M. C. Schaap, D. Pots, T. J. Smeets, A. Sturk, P. P. Tak, Synovial microparticles from arthritic patients modulate chemokine and cytokine release by synoviocytes. Arthritis Res. Ther. 7, R536-R544 (2005).
4. N. Cloutier, S. Tan, L. H. Boudreau, C. Cramb, R. Subbaiah, L. Lahey, A. Albert, R. Shnayder, R. Gobezie, P. A. Nigrovic, R. W. Farndale, W. H. Robinson, A. Brisson, D. M. Lee, E. Boilard, The exposure of autoantigens by microparticles underlies the formation of potent inflammatory components: The microparticle-associated immune complexes. EMBO Mol. Med. 5, 235-249 (2013).
5. J. Dalli, T. Montero-Melendez, L. V. Norling, X. Yin, C. Hinds, D. Haskard, M. Mayr, M. Perretti, Heterogeneity in neutrophil microparticles reveals distinct proteome and functional properties. Mol. Cell. Proteomics 12, 2205-2219 (2013).
6. E. L. Campbell, W. J. Bruyninckx, C. J. Kelly, L. E. Glover, E. N. McNamee, B. E. Bowers, A. J. Bayless, M. Scully, B. J. Saeedi, L. Golden-Mason, S. F. Ehrentraut, V. F. Curtis, A. Burgess, J. F. Garvey, A. Sorensen, R. Nemenoff, P. Jedlicka, C. T. Taylor, D. J. Kominsky, S. P. Colgan, Transmigrating neutrophils shape the mucosal microenvironment through localized oxygen depletion to influence resolution of inflammation. Immunity 40, 66-77 (2014).
7. J. L. Eyles, M. J. Hickey, M. U. Norman, B. A. Croker, A. W. Roberts, S. F. Drake, W. G. James, D. Metcalf, I. K. Campbell, I. P. Wicks, A key role for G-CSF-induced neutrophil production and trafficking during inflammatory arthritis. Blood 112, 5193-5201 (2008).
8. M. S. Gresnigt, L. A. B. Joosten, I. Verschueren, J. W. M. Van Der Meer, M. G. Netea, C. A. Dinarello, F. L. Van De Veerdonk, Neutrophil-mediated inhibition of proinflammatory cytokine responses. J. Immunol. 189, 4806-4815 (2012).
9. J. Dalli, L. V. Norling, D. Renshaw, D. Cooper, K.-Y. Leung, M. Perretti, Annexin 1 mediates the rapid anti-inflammatory effects of neutrophil-derived microparticles. Blood 112, 2512-2519 (2008).
10. C. Eken, O. Gasser, G. Zenhaeusern, I. Oehri, C. Hess, J. A. Schifferli, Polymorphonuclear neutrophil-derived ectosomes interfere with the maturation of monocyte-derived dendritic cells. J. Immunol. 180, 817-824 (2008).
11. O. Gasser, J. A. Schifferli, Activated polymorphonuclear neutrophils disseminate antiinflammatory microparticles by ectocytosis. Blood 104, 2543-2548 (2004).
12. H. W. A. Ehlen, M. Chinenkova, M. Moser, H.-M. Munter, Y. Krause, S. Gross, B. Brachvogel, M. Wuelling, U. Kornak, A. Vortkamp, Inactivation of anoctamin-6/Tmem16f, a regulator of phosphatidylserine scrambling in osteoblasts, leads to decreased mineral deposition in skeletal tissues. J. Bone Miner. Res. 28, 246-259 (2013).
13. X imaging flow cytometry. Sci. Rep. 4, 5237 (2014).
14. K. V. Greco, A. J. Iqbal, L. Rattazzi, G. Nalesso, N. Moradi-Bidhendi, A. R. Moore, M. B. Goldring, F. Dell'Accio, M. Perretti, High density micromass cultures of a human chondrocyte cell line: A reliable assay system to reveal the modulatory functions of pharmacological agents. Biochem. Pharmacol. 82, 1919-1929 (2011).
15. H. M. Van Beuningen, P. M. Van Der Kraan, O. J. Arntz, W. B. Van Den Berg, Protection from interleukin 1 induced destruction of articular cartilage by transforming growth factor β: Studies in anatomically intact cartilage in vitro and in vivo. Ann. Rheum. Dis. 52, 185-191 (1993).
16. S.-S. Nah, I.-Y. Choi, C. K. Lee, J. S. Oh, Y. G. Kim, H.-B. Moon, B. Yoo, Effects of advanced glycation end products on the expression of COX-2, PGE2 and NO in human osteoarthritic chondrocytes. Rheumatology 47, 425-431 (2008).
17. N. M. Eltawil, C. De Bari, P. Achan, C. Pitzalis, F. Dell'Accio, A novel in vivo murine model of cartilage regeneration. Age and strain-dependent outcome after joint surface injury. Osteoarthritis Cartilage 17, 695-704 (2009).
18. O. Alvarez-Garcia, N. H. Rogers, R. G. Smith, M. K. Lotz, Palmitate has proapoptotic and proinflammatory effects on articular cartilage and synergizes with interleukin-1. Arthritis Rheum. 66, 1779-1788 (2014).
19. J. Sherwood, J. Bertrand, G. Nalesso, B. Poulet, A. Pitsillides, L. Brandolini, A. Karystinou, C. De Bari, F. P. Luyten, C. Pitzalis, T. Pap, F. Dell'Accio, A homeostatic function of CXCR2 signalling in articular cartilage. Ann. Rheum. Dis. 74, 2207-2215 (2014).
20. H. B. Patel, K. N. Kornerup, A. L. F. Sampaio, F. D'Acquisto, M. P. Seed, A. P. Girol, M. Gray, C. Pitzalis, S. M. Oliani, M. Perretti, The impact of endogenous annexin A1 on glucocorticoid control of inflammatory arthritis. Ann. Rheum. Dis. 71, 1872-1880 (2012).
21. S. M. Ryan, J. McMorrow, A. Umerska, H. B. Patel, K. N. Kornerup, L. Tajber, E. P. Murphy, M. Perretti, O. I. Corrigan, D. J. Brayden, An intra-articular salmon calcitonin-based nanocomplex reduces experimental inflammatory arthritis. J. Control. Release 167, 120-129 (2013).
22. R. Bockermann, D. Schubert, T. Kamradt, R. Holmdahl, Induction of a B-cell-dependent chronic arthritis with glucose-6-phosphate isomerase. Arthritis Res. Ther. 7, R1316-R1324 (2005).
23. E. Boilard, P. A. Nigrovic, K. Larabee, G. F. M. Watts, J. S. Coblyn, M. E. Weinblatt, E. M. Massarotti, E. Remold-O'Donnell, R. W. Farndale, J. Ware, D. M. Lee, Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science 327, 580-583 (2010).
24. J. H. W. Distler, A. Jüngel, L. C. Huber, C. A. Seemayer, C. F. Reich III, R. E. Gay, B. A. Michel, A. Fontana, S. Gay, D. S. Pisetsky, O. Distler, The induction of matrix metalloproteinase and cytokine expression in synovial fibroblasts stimulated with immune cell microparticles. Proc. Natl. Acad. Sci. U. S. A. 102, 2892-2897 (2005).
25. R. F. P. Schelbergen, A. B. Blom, M. H. J. Van Den Bosch, A. Slöetjes, S. Abdollahi-Roodsaz, B. W. Schreurs, J. S. Mort, T. Vogl, J. Roth, W. B. Van Den Berg, P. L. E. M. Van Lent, Alarmins S100A8 and S100A9 elicit a catabolic effect in human osteoarthritic chondrocytes that is dependent on Toll-like receptor 4. Arthritis Rheum. 64, 1477-1487 (2012).
26. G. Leoni, P.-A. Neumann, N. Kamaly, M. Quiros, H. Nishio, H. R. Jones, R. Sumagin, R. S. Hilgarth, A. Alam, G. Fredman, I. Argyris, E. Rijcken, D. Kusters, C. Reutelingsperger, M. Perretti, C. A. Parkos, O. C. Farokhzad, A. S. Neish, A. Nusrat, Annexin A1-containing extracellular vesicles and polymeric nanoparticles promote epithelial wound repair. J. Clin. Invest. 125, 1215-1227 (2015).
27. A. P. Girol, K. K. O. Mimura, C. C. Drewes, S. M. Bolonheis, E. Solito, S. H. P. Farsky, C. D. Gil, S. M. Oliani, Anti-inflammatory mechanisms of the annexin A1 protein and its mimetic peptide Ac2-26 in models of ocular inflammation in vivo and in vitro. J. Immunol. 190, 5689-5701 (2013).
28. 2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 6, 449-461 (2005).
29. N. J. Goulding, J. Dixey, E. F. Morand, R. A. Dodds, L. S. Wilkinson, A. A. Pitsillides, J. C. Edwards, Differential distribution of annexins-I, -II, -IV, and -VI in synovium. Ann. Rheum. Dis. 54, 841-845 (1995).
30. A. S. Damazo, S. Yona, R. J. Flower, M. Perretti, S. M. Oliani, Spatial and temporal profiles for anti-inflammatory gene expression in leukocytes during a resolving model of peritonitis. J. Immunol. 176, 4410-4418 (2006).
31. S. Bena, V. Brancaleone, J. M. Wang, M. Perretti, R. J. Flower, Annexin A1 interaction with the FPR2/ALX receptor: Identification of distinct domains and downstream associated signaling. J. Biol. Chem. 287, 24690-24697 (2012).
32. 2+-induced microvesiculation and deficient expression of procoagulant activity in erythrocytes from a patient with a bleeding disorder: A study of the red blood cells of Scott syndrome. Blood 79, 380-388 (1992).
33. F. Redini, P. Galera, A. Mauviel, G. Loyau, J.-P. Pujol, Transforming growth factor β stimulates collagen and glycosaminoglycan biosynthesis in cultured rabbit articular chondrocytes. FEBS Lett. 234, 172-175 (1988).
34. M. Scannell, M. B. Flanagan, A. DeStefani, K. J. Wynne, G. Cagney, C. Godson, P. Maderna, Annexin-1 and peptide derivatives are released by apoptotic cells and stimulate phagocytosis of apoptotic neutrophils by macrophages. J. Immunol. 178, 4595-4605 (2007).
35. J. Dalli, L. V. Norling, T. Montero-Melendez, D. Federici Canova, H. Lashin, A. M. Pavlov, G. B. Sukhorukov, C. J. Hinds, M. Perretti, Microparticle alpha-2-macroglobulin enhances pro-resolving responses and promotes survival in sepsis. EMBO Mol. Med. 6, 27-42 (2014).
36. L. V. Norling, M. Spite, R. Yang, R. J. Flower, M. Perretti, C. N. Serhan, Cutting edge: Humanized nano-proresolving medicines mimic inflammation-resolution and enhance wound healing. J. Immunol. 186, 5543-5547 (2011).
37. G. Fredman, N. Kamaly, S. Spolitu, J. Milton, D. Ghorpade, R. Chiasson, G. Kuriakose, M. Perretti, O. Farokhzad, I. Tabas, Targeted nanoparticles containing the proresolving peptide Ac2-26 protect against advanced atherosclerosis in hypercholesterolemic mice. Sci. Transl. Med. 7, 275ra20 (2015).
38. C. Lee, S. A. Mitsialis, M. Aslam, S. H. Vitali, E. Vergadi, G. Konstantinou, K. Sdrimas, A. Fernandez-Gonzalez, S. Kourembanas, Exosomes mediate the cytoprotective action of mesenchymal stromal cells on hypoxia-induced pulmonary hypertension. Circulation 126, 2601-2611 (2012).
39. S. EL Andaloussi, I. Mäger, X. O. Breakefield, M. J. A. Wood, Extracellular vesicles: Biology and emerging therapeutic opportunities. Nat. Rev. Drug Discov. 12, 347-357 (2013).
40. M. F. Bolukbasi, A. Mizrak, G. B. Ozdener, S. Madlener, T. Ströbel, E. P. Erkan, J.-B. Fan, X. O. Breakefield, O. Saydam, miR-1289 and "Zipcode"-like sequence enrich mRNAs in microvesicles. Mol. Ther. Nucleic Acids 1, e10 (2012).
41. K.-V. Chang, C.-Y. Hung, F. Aliwarga, T.-G. Wang, D.-S. Han, W.-S. Chen, Comparative effectiveness of platelet-rich plasma injections for treating knee joint cartilage degenerative pathology: A systematic review and meta-analysis. Arch. Phys. Med. Rehabil. 95, 562-575 (2014).