Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2015, Article ID 267590, 15 pages
http://dx.doi.org/10.1155/2015/267590
Review Article

Microparticles That Form Immune Complexes as Modulatory Structures in Autoimmune Responses

1Grupo de Inmunología Celular e Inmunogenética, Instituto de Investigaciones Médicas, Facultad de Medicina, Universidad de Antioquia (UdeA), Calle 70 No. 52-21, Medellín, Colombia
2Unidad de Citometría de Flujo, Sede de Investigación Universitaria, Universidad de Antioquia (UdeA), Calle 70 No. 52-21, Medellín, Colombia

Received 20 October 2014; Revised 10 December 2014; Accepted 13 December 2014

Academic Editor: György Nagy

Copyright © 2015 Catalina Burbano et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. Eringsmark Regnéll and Å. Lernmark, “The environment and the origins of islet autoimmunity and Type 1 diabetes,” Diabetic Medicine, vol. 30, no. 2, pp. 155–160, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. T. Czömpöly, K. Olasz, D. Simon et al., “A possible new bridge between innate and adaptive immunity: are the anti-mitochondrial citrate synthase autoantibodies components of the natural antibody network?” Molecular Immunology, vol. 43, no. 11, pp. 1761–1768, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Segelmark, “Genes that link nephritis to autoantibodies and innate immunity,” The New England Journal of Medicine, vol. 364, no. 7, pp. 679–680, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. L. E. Mũoz, K. Lauber, M. Schiller, A. A. Manfredi, and M. Herrmann, “The role of defective clearance of apoptotic cells in systemic autoimmunity,” Nature Reviews Rheumatology, vol. 6, no. 5, pp. 280–289, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. Z. S. M. Rahman, “Impaired clearance of apoptotic cells in germinal centers: implications for loss of B cell tolerance and induction of autoimmunity,” Immunologic Research, vol. 51, no. 2-3, pp. 125–133, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. X. Chang, R. Yamada, A. Suzuki et al., “Localization of peptidylarginine deiminase 4 (PADI4) and citrullinated protein in synovial tissue of rheumatoid arthritis,” Rheumatology, vol. 44, no. 1, pp. 40–50, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. D. B. Klinkner, J. C. Densmore, S. Kaul et al., “Endothelium-derived microparticles inhibit human cardiac valve endothelial cell function,” Shock, vol. 25, no. 6, pp. 575–580, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Aharon, T. Tamari, and B. Brenner, “Monocyte-derived microparticles and exosomes induce procoagulant and apoptotic effects on endothelial cells,” Thrombosis and Haemostasis, vol. 100, no. 5, pp. 878–885, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. D. S. Pisetsky and P. E. Lipsky, “Microparticles as autoadjuvants in the pathogenesis of SLE,” Nature Reviews Rheumatology, vol. 6, no. 6, pp. 368–372, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. J. R. Dye, A. J. Ullal, and D. S. Pisetsky, “The role of microparticles in the pathogenesis of rheumatoid arthritis and systemic lupus erythematosus,” Scandinavian Journal of Immunology, vol. 78, no. 2, pp. 140–148, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. D. S. Pisetsky, “Microparticles as autoantigens: making immune complexes big,” Arthritis and Rheumatism, vol. 64, no. 4, pp. 958–961, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. N. Cloutier, S. Tan, L. H. Boudreau et al., “The exposure of autoantigens by microparticles underlies the formation of potent inflammatory components: the microparticle-associated immune complexes,” EMBO Molecular Medicine, vol. 5, no. 2, pp. 235–249, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. M. T. Sartori, A. Della Puppa, A. Ballin et al., “Circulating microparticles of glial origin and tissue factor bearing in high-grade glioma: a potential prothrombotic role,” Thrombosis and Haemostasis, vol. 110, no. 2, pp. 378–385, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. P. Wolf, “The nature and significance of platelet products in human plasma.,” British Journal of Haematology, vol. 13, no. 3, pp. 269–288, 1967. View at Publisher · View at Google Scholar · View at Scopus
  15. C. Théry, M. Ostrowski, and E. Segura, “Membrane vesicles as conveyors of immune responses,” Nature Reviews Immunology, vol. 9, no. 8, pp. 581–593, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Flaumenhaft, J. R. Dilks, J. Richardson et al., “Megakaryocyte-derived microparticles: direct visualization and distinction from platelet-derived microparticles,” Blood, vol. 113, no. 5, pp. 1112–1121, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Aharon and B. Brenner, “Microparticles, thrombosis and cancer,” Best Practice and Research: Clinical Haematology, vol. 22, no. 1, pp. 61–69, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. C. A. Kunder, A. L. St. John, G. Li et al., “Mast cell-derived particles deliver peripheral signals to remote lymph nodes,” The Journal of Experimental Medicine, vol. 206, no. 11, pp. 2455–2467, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Antwi-Baffour, S. Kholia, Y. K.-D. Aryee et al., “Human plasma membrane-derived vesicles inhibit the phagocytosis of apoptotic cells—possible role in SLE,” Biochemical and Biophysical Research Communications, vol. 398, no. 2, pp. 278–283, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. O. Morel, L. Jesel, J.-M. Freyssinet, and F. Toti, “Cellular mechanisms underlying the formation of circulating microparticles,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 1, pp. 15–26, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. D. Z. de Back, E. B. Kostova, M. van Kraaij, T. K. van den Berg, and R. van Bruggen, “Of macrophages and red blood cells; A complex love story,” Frontiers in Physiology, vol. 5, article 9, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. L. H. Boudreau, A.-C. Duchez, N. Cloutier et al., “Platelets release mitochondria serving as substrate for bactericidal group IIA-secreted phospholipase A2 to promote inflammation,” Blood, vol. 124, no. 14, pp. 2173–2183, 2014. View at Publisher · View at Google Scholar
  23. B. Hugel, M. C. Martínez, C. Kunzelmann, and J.-M. Freyssinet, “Membrane microparticles: two sides of the coin,” Physiology, vol. 20, no. 1, pp. 22–27, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. A. J. Gomes, A. S. Faustino, A. E. H. Machado et al., “Characterization of PLGA microparticles as a drug carrier for 3-ethoxycarbonyl-2H-benzofuro[3,2-f]-1-benzopyran-2-one. Ultrastructural study of cellular uptake and intracellular distribution,” Drug Delivery, vol. 13, no. 6, pp. 447–454, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. C. Gao, R. Li, Y. Liu, L. Ma, and S. Wang, “Rho-kinase-dependent F-actin rearrangement is involved in the release of endothelial microparticles during IFN-α-induced endothelial cell apoptosis,” The Journal of Trauma and Acute Care Surgery, vol. 73, no. 5, pp. 1152–1160, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Cauwenberghs, M. A. H. Feijge, A. G. S. Harper, S. O. Sage, J. Curvers, and J. W. M. Heemskerk, “Shedding of procoagulant microparticles from unstimulated platelets by integrin-mediated destabilization of actin cytoskeleton,” FEBS Letters, vol. 580, no. 22, pp. 5313–5320, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. R. F. A. Zwaal, P. Comfurius, and E. M. Bevers, “Surface exposure of phosphatidylserine in pathological cells,” Cellular and Molecular Life Sciences, vol. 62, no. 9, pp. 971–988, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. D. B. Nguyen, L. Wagner-Britz, S. Maia et al., “Regulation of phosphatidylserine exposure in red blood cells,” Cellular Physiology and Biochemistry, vol. 28, no. 5, pp. 847–856, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. V. Proulle, B. Hugel, B. Guillet et al., “Circulating microparticles are elevated in haemophiliacs and non-haemophilic individuals aged <18 years,” British Journal of Haematology, vol. 131, no. 4, pp. 487–489, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. C. T. Nielsen, O. Østergaard, C. Johnsen, S. Jacobsen, and N. H. H. Heegaard, “Distinct features of circulating microparticles and their relationship to clinical manifestations in systemic lupus erythematosus,” Arthritis & Rheumatism, vol. 63, no. 10, pp. 3067–3077, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. C. M. Boulanger, N. Amabile, and A. Tedgui, “Circulating microparticles: a potential prognostic marker for atherosclerotic vascular disease,” Hypertension, vol. 48, no. 2, pp. 180–186, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. G. Palmisano, S. Jensen, M. C. le Bihan et al., “Characterization of membrane-shed microvesicles from cytokine-stimulated β-cells using proteomics strategies,” Molecular and Cellular Proteomics, vol. 11, no. 8, pp. 230–243, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. N. S. Barteneva, E. Fasler-Kan, M. Bernimoulin et al., “Circulating microparticles: square the circle,” BMC Cell Biology, vol. 14, no. 1, article 23, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. P. Nusbaum, C. Lainé, M. Bouaouina et al., “Distinct signaling pathways are involved in leukosialin (CD43) down-regulation, membrane blebbing, and phospholipid scrambling during neutrophil apoptosis,” Journal of Biological Chemistry, vol. 280, no. 7, pp. 5843–5853, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. E. M. Bevers, R. F. A. Zwaal, and G. M. Willems, “The effect of phospholipids on the formation of immune complexes between autoantibodies and β2-glycoprotein I or prothrombin,” Clinical Immunology, vol. 112, no. 2, pp. 150–160, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. C. F. Reich III and D. S. Pisetsky, “The content of DNA and RNA in microparticles released by Jurkat and HL-60 cells undergoing in vitro apoptosis,” Experimental Cell Research, vol. 315, no. 5, pp. 760–768, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Chen, C. Yan, X. Jiang, and Y.-R. Dai, “Hyperthermia-induced apoptosis and the inhibition of DNA laddering by zinc supplementation and withdrawal of calcium and magnesium in suspension culture of tobacco cells,” Cellular and Molecular Life Sciences, vol. 55, no. 2, pp. 303–309, 1999. View at Publisher · View at Google Scholar · View at Scopus
  38. A. L. Capriotti, G. Caruso, C. Cavaliere, S. Piovesana, R. Samperi, and A. Laganà, “Proteomic characterization of human platelet-derived microparticles,” Analytica Chimica Acta, vol. 776, pp. 57–63, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. Y. Liu, W. Huang, R. Zhang, J. Wu, L. Li, and Y. Tang, “Proteomic analysis of TNF-α-activated endothelial cells and endothelial microparticles,” Molecular Medicine Reports, vol. 7, no. 1, pp. 318–326, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. J.-M. Howes, “Proteomic profiling of plasma microparticles following deep-vein thrombosis,” Expert Review of Proteomics, vol. 7, no. 3, pp. 327–330, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. O. Rubin, D. Crettaz, G. Canellini, J.-D. Tissot, and N. Lion, “Microparticles in stored red blood cells: an approach using flow cytometry and proteomic tools,” Vox Sanguinis, vol. 95, no. 4, pp. 289–297, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. D. S. Pisetsky, “The expression of HMGB1 on microparticles released during cell activation and cell death in vitro and in vivo,” Molecular Medicine, vol. 20, no. 1, pp. 158–163, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. A. F. Orozco and D. E. Lewis, “Flow cytometric analysis of circulating microparticles in plasma,” Cytometry Part A, vol. 77, no. 6, pp. 502–514, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. M. L. Alvarez, M. Khosroheidari, R. K. Ravi, and J. K. Distefano, “Comparison of protein, microRNA, and mRNA yields using different methods of urinary exosome isolation for the discovery of kidney disease biomarkers,” Kidney International, vol. 82, no. 9, pp. 1024–1032, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. P. Fernández-Llama, S. Khositseth, P. A. Gonzales, R. A. Star, T. Pisitkun, and M. A. Knepper, “Tamm-Horsfall protein and urinary exosome isolation,” Kidney International, vol. 77, no. 8, pp. 736–742, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. M. C. Vallejo, E. S. Nakayasu, A. L. Matsuo et al., “Vesicle and vesicle-free extracellular proteome of paracoccidioides brasiliensis: Comparative analysis with other pathogenic fungi,” Journal of Proteome Research, vol. 11, no. 3, pp. 1676–1685, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. B. Gyorgy, K. Modos, E. Pallinger et al., “Detection and isolation of cell-derived microparticles are compromised by protein complexes resulting from shared biophysical parameters,” Blood, vol. 117, no. 4, pp. e39–e48, 2011. View at Publisher · View at Google Scholar
  48. G. D. Porta, N. Falco, and E. Reverchon, “Continuous supercritical emulsions extraction: a new technology for biopolymer microparticles production,” Biotechnology and Bioengineering, vol. 108, no. 3, pp. 676–686, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. C. Cerri, D. Chimenti, I. Conti, T. Neri, P. Paggiaro, and A. Celi, “Monocyte/macrophage-derived microparticles up-regulate inflammatory mediator synthesis by human airway epithelial cells,” The Journal of Immunology, vol. 177, no. 3, pp. 1975–1980, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. A. M. Weerheim, A. M. Kolb, A. Sturk, and R. Nieuwland, “Phospholipid composition of cell-derived microparticles determined by one-dimensional high-performance thin-layer chromatography,” Analytical Biochemistry, vol. 302, no. 2, pp. 191–198, 2002. View at Publisher · View at Google Scholar · View at Scopus
  51. T.-F. Lee, Y.-L. Lin, and Y.-T. Huang, “Kaerophyllin inhibits hepatic stellate cell activation by apoptotic bodies from hepatocytes,” Liver International, vol. 31, no. 5, pp. 618–629, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. F. Gautier, D. Lassort, M.-T. Le Cabellec et al., “Production and characterisation of a monoclonal antibody specific for apoptotic bodies derived from several tumour cell lines,” Journal of Immunological Methods, vol. 228, no. 1-2, pp. 49–58, 1999. View at Publisher · View at Google Scholar · View at Scopus
  53. R. de Mesquita and P. Biberfeld, “Demonstration of herpesvirus particles in apoptotic bodies of a brain lymphoma in an SIV-immunodeficient monkey,” International Journal of Cancer, vol. 63, no. 3, pp. 472–473, 1995. View at Publisher · View at Google Scholar · View at Scopus
  54. B. Köppler, C. Cohen, D. Schlöndorff, and M. Mack, “Differential mechanisms of microparticle transfer to B cells and monocytes: anti-inflammatory properties of microparticles,” European Journal of Immunology, vol. 36, no. 3, pp. 648–660, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Rozmyslowicz, M. Majka, J. Kijowski et al., “Platelet- and megakaryocyte-derived microparticles transfer CXCR4 receptor to CXCR4-null cells and make them susceptible to infection by X4-HIV,” AIDS, vol. 17, no. 1, pp. 33–42, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. R. Jaiswal, F. Luk, J. Gong, J.-M. Mathys, G. E. R. Grau, and M. Bebawy, “Microparticle conferred microRNA profiles—implications in the transfer and dominance of cancer traits,” Molecular Cancer, vol. 11, article 37, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. B. Laffont, A. Corduan, H. Plé et al., “Activated platelets can deliver mRNA regulatory Ago2•microRNA complexes to endothelial cells via microparticles,” Blood, vol. 122, no. 2, pp. 253–261, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. Y. Pan, H. Liang, H. Liu et al., “Platelet-secreted microRNA-223 promotes endothelial cell apoptosis induced by advanced glycation end products via targeting the insulin-like growth factor 1 receptor,” The Journal of Immunology, vol. 192, no. 1, pp. 437–446, 2014. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. Y. Zhang, X. Zhou, W. J. Ji et al., “Decreased circulating microRNA-223 level predicts high on-treatment platelet reactivity in patients with troponin-negative non-ST elevation acute coronary syndrome,” Journal of Thrombosis and Thrombolysis, vol. 38, no. 1, pp. 65–72, 2014. View at Publisher · View at Google Scholar · View at Scopus
  60. H. Lu, R. J. Buchan, and S. A. Cook, “MicroRNA-223 regulates Glut4 expression and cardiomyocyte glucose metabolism,” Cardiovascular Research, vol. 86, no. 3, pp. 410–420, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. J. Dalli and C. N. Serhan, “Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators,” Blood, vol. 120, no. 15, pp. e60–e72, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. J. H. W. Distler, A. Akhmetshina, C. Dees et al., “Induction of apoptosis in circulating angiogenic cells by microparticles,” Arthritis and Rheumatism, vol. 63, no. 7, pp. 2067–2077, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Jüngel, O. Distler, U. Schulze-Horsel et al., “Microparticles stimulate the synthesis of prostaglandin E2 via induction of cyclooxygenase 2 and microsomal prostaglandin E synthase,” Arthritis & Rheumatism, vol. 56, no. 11, pp. 3564–3574, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. E. Boilard, P. A. Nigrovic, K. Larabee et al., “Platelets amplify inflammation in arthritis via collagen-dependent microparticle production,” Science, vol. 327, no. 5965, pp. 580–583, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Mack, A. Kleinschmidt, H. Brühl et al., “Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection,” Nature Medicine, vol. 6, no. 7, pp. 769–775, 2000. View at Publisher · View at Google Scholar · View at Scopus
  66. R. Jaiswal, F. Luk, P. V. Dalla, G. E. R. Grau, and M. Bebawy, “Breast cancer-derived microparticles display tissue selectivity in the transfer of resistance proteins to cells,” PLoS ONE, vol. 8, no. 4, Article ID e61515, 2013. View at Publisher · View at Google Scholar · View at Scopus
  67. J. F. Lu, F. Luk, J. Gong, R. Jaiswal, G. E. R. Grau, and M. Bebawy, “Microparticles mediate MRP1 intercellular transfer and the re-templating of intrinsic resistance pathways,” Pharmacological Research, vol. 76, pp. 77–83, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. F. Jansen, X. Yang, M. Hoelscher et al., “Endothelial microparticle-mediated transfer of MicroRNA-126 promotes vascular endothelial cell repair via spred1 and is abrogated in glucose-damaged endothelial microparticles,” Circulation, vol. 128, no. 18, pp. 2026–2038, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. P. Suwannalai, L. A. Trouw, R. E. M. Toes, and T. W. J. Huizinga, “Anti-citrullinated protein antibodies (ACPA) in early rheumatoid arthritis,” Modern Rheumatology, vol. 22, no. 1, pp. 15–20, 2012. View at Publisher · View at Google Scholar · View at Scopus
  70. C. Foulquier, M. Sebbag, C. Clavel et al., “Peptidyl arginine deiminase type 2 (PAD-2) and PAD-4 but not PAD-1, PAD-3, and PAD-6 are expressed in rheumatoid arthritis synovium in close association with tissue inflammation,” Arthritis and Rheumatism, vol. 56, no. 11, pp. 3541–3553, 2007. View at Publisher · View at Google Scholar · View at Scopus
  71. E. A. J. Knijff-Dutmer, J. Koerts, R. Nieuwland, E. M. Kalsbeek-Batenburg, and M. A. F. J. van de Laar, “Elevated levels of platelet microparticles are associated with disease activity in rheumatoid arthritis,” Arthritis and Rheumatism, vol. 46, no. 6, pp. 1498–1503, 2002. View at Publisher · View at Google Scholar · View at Scopus
  72. A. Soop, L. Hållström, C. Frostell, H. Wallén, F. Mobarrez, and D. S. Pisetsky, “Effect of lipopolysaccharide administration on the number, phenotype and content of nuclear molecules in blood microparticles of normal human subjects,” Scandinavian Journal of Immunology, vol. 78, no. 2, pp. 205–213, 2013. View at Publisher · View at Google Scholar · View at Scopus
  73. M. Magna and D. S. Pisetsky, “The role of HMGB1 in the pathogenesis of inflammatory and autoimmune diseases,” Molecular Medicine, vol. 20, no. 1, pp. 138–146, 2014. View at Publisher · View at Google Scholar · View at Scopus
  74. A. M. Avalos, K. Kiefer, J. Tian et al., “RAGE-independent autoreactive B cell activation in response to chromatin and HMGB1/DNA immune complexes,” Autoimmunity, vol. 43, no. 1, pp. 103–110, 2010. View at Publisher · View at Google Scholar · View at Scopus
  75. B. Lu, H. Wang, U. Andersson, and K. J. Tracey, “Regulation of HMGB1 release by inflammasomes,” Protein and Cell, vol. 4, no. 3, pp. 163–167, 2013. View at Publisher · View at Google Scholar · View at Scopus
  76. F. Khan, A. A. Siddiqui, and R. Ali, “Measurement and significance of 3-nitrotyrosine in systemic lupus erythematosus,” Scandinavian Journal of Immunology, vol. 64, no. 5, pp. 507–514, 2006. View at Publisher · View at Google Scholar · View at Scopus
  77. F. Khan and A. A. Siddiqui, “Prevalence of anti-3-nitrotyrosine antibodies in the joint synovial fluid of patients with rheumatoid arthritis, osteoarthritis and systemic lupus erythematosus,” Clinica Chimica Acta, vol. 370, no. 1-2, pp. 100–107, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. A. J. Ullal, C. F. Reich, M. Clowse et al., “Microparticles as antigenic targets of antibodies to DNA and nucleosomes in systemic lupus erythematosus,” Journal of Autoimmunity, vol. 36, no. 3-4, pp. 173–180, 2011. View at Publisher · View at Google Scholar · View at Scopus
  79. C. T. Nielsen, O. Østergaard, L. Stener et al., “Increased IgG on cell-derived plasma microparticles in systemic lupus erythematosus is associated with autoantibodies and complement activation.,” Arthritis and rheumatism, vol. 64, no. 4, pp. 1227–1236, 2012. View at Publisher · View at Google Scholar · View at Scopus
  80. A. Larsson, N. Egberg, and T. L. Lindahl, “Platelet activation and binding of complement components to platelets induced by immune complexes,” Platelets, vol. 5, no. 3, pp. 149–155, 1994. View at Publisher · View at Google Scholar · View at Scopus
  81. K. L. Graham and P. J. Utz, “Sources of autoantigens in systemic lupus erythematosus,” Current Opinion in Rheumatology, vol. 17, no. 5, pp. 513–517, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. Y. Sherer, A. Gorstein, M. J. Fritzler, and Y. Shoenfeld, “Autoantibody explosion in systemic lupus erythematosus: more than 100 different antibodies found in SLE patients,” Seminars in Arthritis and Rheumatism, vol. 34, no. 2, pp. 501–537, 2004. View at Publisher · View at Google Scholar · View at Scopus
  83. O. Ostergaard, C. T. Nielsen, L. V. Iversen et al., “Unique protein signature of circulating microparticles in systemic lupus erythematosus,” Arthritis and Rheumatism, vol. 65, no. 10, pp. 2680–2690, 2013. View at Publisher · View at Google Scholar · View at Scopus
  84. J. Sellam, V. Proulle, A. Jüngel et al., “Increased levels of circulating microparticles in primary Sjögren's syndrome, systemic lupus erythematosus and rheumatoid arthritis and relation with disease activity,” Arthritis Research & Therapy, vol. 11, no. 5, article R156, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. L. Miguet, G. Béchade, L. Fornecker et al., “Proteomic analysis of malignant B-cell derived microparticles reveals CD148 as a potentially useful antigenic biomarker for mantle cell lymphoma diagnosis,” Journal of Proteome Research, vol. 8, no. 7, pp. 3346–3354, 2009. View at Publisher · View at Google Scholar
  86. D. S. Pisetsky, J. Gauley, and A. J. Ullal, “Microparticles as a source of extracellular DNA,” Immunologic Research, vol. 49, no. 1–3, pp. 227–234, 2011. View at Publisher · View at Google Scholar · View at Scopus
  87. D. S. Pisetsky and A. J. Ullal, “The blood nucleome in the pathogenesis of SLE,” Autoimmunity Reviews, vol. 10, no. 1, pp. 35–37, 2010. View at Publisher · View at Google Scholar · View at Scopus
  88. U. S. Gaipl, L. E. Munoz, G. Grossmayer et al., “Clearance deficiency and systemic lupus erythematosus (SLE),” Journal of Autoimmunity, vol. 28, no. 2-3, pp. 114–121, 2007. View at Publisher · View at Google Scholar · View at Scopus
  89. C. Marin, R. Ramirez, J. Delgado-Lista et al., “Mediterranean diet reduces endothelial damage and improves the regenerative capacity of endothelium,” The American Journal of Clinical Nutrition, vol. 93, no. 2, pp. 267–274, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. F. A. H. Cooles and J. D. Isaacs, “Pathophysiology of rheumatoid arthritis,” Current Opinion in Rheumatology, vol. 23, no. 3, pp. 233–240, 2011. View at Publisher · View at Google Scholar · View at Scopus
  91. Y. Ren, J. Tang, M. Y. Mok, A. W. K. Chan, A. Wu, and C. S. Lau, “Increased apoptotic neutrophils and macrophages and impaired macrophage phagocytic clearance of apoptotic neutrophils in systemic lupus erythematosus,” Arthritis and Rheumatism, vol. 48, no. 10, pp. 2888–2897, 2003. View at Publisher · View at Google Scholar · View at Scopus
  92. G. Jego, A. K. Palucka, J.-P. Blanck, C. Chalouni, V. Pascual, and J. Banchereau, “Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6,” Immunity, vol. 19, no. 2, pp. 225–234, 2003. View at Publisher · View at Google Scholar · View at Scopus
  93. S. R. Christensen and M. J. Shlomchik, “Regulation of lupus-related autoantibody production and clinical disease by Toll-like receptors,” Seminars in Immunology, vol. 19, no. 1, pp. 11–23, 2007. View at Publisher · View at Google Scholar · View at Scopus
  94. J. C. Crispín, S. N. C. Liossis, K. Kis-Toth et al., “Pathogenesis of human systemic lupus erythematosus: recent advances,” Trends in Molecular Medicine, vol. 16, no. 2, pp. 47–57, 2010. View at Publisher · View at Google Scholar · View at Scopus
  95. R. J. Berckmans, R. Nieuwland, P. P. Tak et al., “Cell-derived microparticles in synovial fluid from inflamed arthritic joints support coagulation exclusively via a factor VII-dependent mechanism,” Arthritis and Rheumatism, vol. 46, no. 11, pp. 2857–2866, 2002. View at Publisher · View at Google Scholar · View at Scopus
  96. L. Messer, G. Alsaleh, J.-M. Freyssinet et al., “Microparticle-induced release of B-lymphocyte regulators by rheumatoid synoviocytes,” Arthritis Research & Therapy, vol. 11, no. 2, article R40, 2009. View at Publisher · View at Google Scholar · View at Scopus
  97. J. A. Burger, N. J. Zvaifler, N. Tsukada, G. S. Firestein, and T. J. Kipps, “Fibroblast-like synoviocytes support B-cell pseudoemperipolesis via a stromal cell-derived factor-1- and CD106 (VCAM-1)-dependent mechanism,” The Journal of Clinical Investigation, vol. 107, no. 3, pp. 305–315, 2001. View at Publisher · View at Google Scholar · View at Scopus
  98. K. Shi, K. Hayashida, M. Kaneko et al., “Lymphoid chemokine B cell-attracting chemokine-1 (CXCL13) is expressed in germinal center of ectopic lymphoid follicles within the synovium of chronic arthritis patients,” Journal of Immunology, vol. 166, no. 1, pp. 650–655, 2001. View at Publisher · View at Google Scholar · View at Scopus
  99. N. Reich, C. Beyer, K. Gelse et al., “Microparticles stimulate angiogenesis by inducing ELR+ CXC-chemokines in synovial fibroblasts,” Journal of Cellular and Molecular Medicine, vol. 15, no. 4, pp. 756–762, 2011. View at Publisher · View at Google Scholar · View at Scopus
  100. M. Feldmann, F. M. Brennan, M. J. Elliott, R. O. Williams, and R. N. Maini, “TNFα is an effective therapeatic target for rheumatoid arthritis,” Annals of the New York Academy of Sciences, vol. 766, pp. 272–278, 1995. View at Publisher · View at Google Scholar · View at Scopus
  101. J. A. Duty, P. Szodoray, N.-Y. Zheng et al., “Functional anergy in a subpopulation of naive B cells from healthy humans that express autoreactive immunoglobulin receptors,” Journal of Experimental Medicine, vol. 206, no. 1, pp. 139–151, 2009. View at Publisher · View at Google Scholar · View at Scopus
  102. C. Clavel, L. Nogueira, L. Laurent et al., “Induction of macrophage secretion of tumor necrosis factor alpha through Fcgamma receptor IIa engagement by rheumatoid arthritis-specific autoantibodies to citrullinated proteins complexed with fibrinogen,” Arthritis and Rheumatism, vol. 58, no. 3, pp. 678–688, 2008. View at Publisher · View at Google Scholar · View at Scopus
  103. J. Sokolove, X. Zhao, P. E. Chandra, and W. H. Robinson, “Immune complexes containing citrullinated fibrinogen costimulate macrophages via toll-like receptor 4 and Fcγ receptor,” Arthritis and Rheumatism, vol. 63, no. 1, pp. 53–62, 2011. View at Publisher · View at Google Scholar · View at Scopus
  104. M. A. Howard, M. Coghlan, R. David, and S. L. Pfueller, “Coagulation activities of plasma microparticles,” Thrombosis Research, vol. 50, no. 1, pp. 145–156, 1988. View at Publisher · View at Google Scholar · View at Scopus
  105. A. Deutschmann, A. Schlagenhauf, B. Leschnik, K. M. Hoffmann, A. Hauer, and W. Muntean, “Increased procoagulant function of microparticles in pediatric inflammatory bowel disease: role in increased thrombin generation,” Journal of Pediatric Gastroenterology and Nutrition, vol. 56, no. 4, pp. 401–407, 2013. View at Publisher · View at Google Scholar · View at Scopus
  106. M. Schiller, I. Bekeredjian-Ding, P. Heyder, N. Blank, A. D. Ho, and H.-M. Lorenz, “Autoantigens are translocated into small apoptotic bodies during early stages of apoptosis,” Cell Death & Differentiation, vol. 15, no. 1, pp. 183–191, 2008. View at Publisher · View at Google Scholar · View at Scopus
  107. V. Racanelli, M. Prete, G. Musaraj, F. Dammacco, and F. Perosa, “Autoantibodies to intracellular antigens: generation and pathogenetic role,” Autoimmunity Reviews, vol. 10, no. 8, pp. 503–508, 2011. View at Publisher · View at Google Scholar · View at Scopus
  108. J. Dieker and S. Muller, “Post-translational modifications, subcellular relocation and release in apoptotic microparticles: apoptosis turns nuclear proteins into autoantigens,” Folia Histochemica et Cytobiologica, vol. 47, no. 3, pp. 343–348, 2009. View at Publisher · View at Google Scholar · View at Scopus
  109. D. Castaño, L. F. García, and M. Rojas, “Increased frequency and cell death of CD16 + monocytes with Mycobacterium tuberculosis infection,” Tuberculosis, vol. 91, no. 5, pp. 348–360, 2011. View at Publisher · View at Google Scholar · View at Scopus
  110. M. Rossol, S. Kraus, M. Pierer, C. Baerwald, and U. Wagner, “The CD14brightCD16+ monocyte subset is expanded in rheumatoid arthritis and promotes expansion of the Th17 cell population,” Arthritis and Rheumatism, vol. 64, no. 3, pp. 671–677, 2012. View at Publisher · View at Google Scholar · View at Scopus
  111. A. P. Cairns, A. D. Crockard, and A. L. Bell, “The CD14+ CD16+ monocyte subset in rheumatoid arthritis and systemic lupus erythematosus,” Rheumatology International, vol. 21, no. 5, pp. 189–192, 2002. View at Publisher · View at Google Scholar · View at Scopus