Skip to main content

Advertisement

SpringerLink
Log in

Platelet and red blood cell interactions and their role in rheumatoid arthritis

  • Review Article - Pathology Review
  • Published:
Rheumatology International Aims and scope Submit manuscript

Abstract

Cytokines, lymphocytes, platelets and several biomolecules have long been implicated in the pathology of rheumatoid arthritis (RA), and the influences of antibody production and tagging, and cytokine, chemokine and enzyme production at specific rheumatoid joints were thought to be exclusive to the advancement of disease parameters. Another role player in RA is red blood cells (RBCs) which, of late, have been found to be involved in RA pathobiology, as there is a positive correlation between RBC counts and joint pathology, as well as with inflammatory biomarkers in the disease. There is also an association between RBC distribution width and the incidence of myocardial infarction amongst RA patients, and there is a change in the lipid distribution within RBC membranes. Of late, certain RBC-associated factors with previously obscure roles and cell-derived particles thought to be inconsequential to the other constituents of plasma were found to be active biomolecular players. Several of these have been discovered to be present in or originating from RBCs. Their influences have been shown to involve in membrane dynamics that cause structural and functional changes in both platelets and RBCs. RBC-derived microparticles are emerging entities found to play direct roles in immunomodulation via interactions with other plasma cells. These correlations highlight the direct influences of RBCs on exacerbating RA pathology. This review will attempt to shed more light on how RBCs, in the true inflammatory milieu of RA, are playing an even greater role than previously assumed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Scott DL, Wolfe F, Huizinga TWJ (2010) Rheumatoid arthritis. Lancet 376(9746):1094–1108

    Article  PubMed  Google Scholar 

  2. Tobón GJ, Youinou P, Saraux A (2010) The environment, geo-epidemiology, and autoimmune disease: rheumatoid arthritis. J Autoimmun 35(1):10–14

    Article  PubMed  Google Scholar 

  3. Scott IC, Seegobin SD, Steer S, Tan R, Forabosco P, Hinks A, Eyre S, Morgan AW, Wilson AG, Hocking LJ et al (2013) Predicting the risk of rheumatoid arthritis and its age of onset through modelling genetic risk variants with smoking. PLoS Genet 9(9):e1003808

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Bergström U, Jacobsson L, Nilsson J-Å, Wirfält E, Turesson C (2013) Smoking, low formal level of education, alcohol consumption, and the risk of rheumatoid arthritis. Scand J Rheumatol 42(2):123–130

    Article  PubMed  Google Scholar 

  5. Cooles FA, Isaacs JD (2011) Pathophysiology of rheumatoid arthritis. Curr Opin Rheumatol 23(3):233–240. doi:10.1097/BOR.1090b1013e32834518a32834513

    Article  CAS  PubMed  Google Scholar 

  6. van Beers JJBC, Pruijn GJ (2010) The role of synovial citrullinated proteins in the pathophysiology of rheumatoid arthritis. Protein Deimination in Human Health and Disease, pp 41–68

  7. Seven A, Güzel S, Aslan M, Hamuryudan V (2008) Lipid, protein, DNA oxidation and antioxidant status in rheumatoid arthritis. Clin Biochem 41(7):538–543

    Article  CAS  PubMed  Google Scholar 

  8. Charles-Schoeman C, Lee YY, Grijalva V, Amjadi S, FitzGerald J, Ranganath VK et al (2012) Cholesterol efflux by high density lipoproteins is impaired in patients with active rheumatoid arthritis. Ann Rheum Dis 71:1157–1162

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Gasparyan AY, Stavropoulos-Kalinoglou A, Mikhailidis DP, Toms TE, Douglas KMJ, Kitas GD (2011) Platelet function in rheumatoid arthritis: arthritic and cardiovascular implications. Rheumatol Int 31:153–164

    Article  CAS  PubMed  Google Scholar 

  10. Luquita A, Uril L, Svetaz MJ, Gennaro AM, Volpintesta R, Palatnik S et al (2009) Erythrocyte aggregation in rheumatoid arthritis: cell and plasma factor’s role. Clin Hemorheol Microcirc 41:49–56

    CAS  PubMed  Google Scholar 

  11. Lu A (2009) Correlations among cartilage erosion, IgA level, red blood cell and platelet counts in 436 rheumatoid arthritis patients with path analysis. In: Bioinformatics and Biomedical Engineering, Beijing: ICBBE, pp 1–3

  12. Gasparyan AY, Ayvazyan L, Blackmore H, Kitas GD (2011) Writing a narrative biomedical review: considerations for authors, peer reviewers, and editors. Rheumatol Int 31(11):1409–1417

    Article  PubMed  Google Scholar 

  13. Verma N, Misra R, Singh R, Agarwal S, Naik S (2002) Serological correlates of inflammation in rheumatoid arthritis: usefulness of acute phase reactants in monitoring disease activity. J Indian Rheumatol Assoc 10:1–4

    Google Scholar 

  14. Bunescu A, Seideman P, Lenkei R, Levin K, Egberg N (2004) Enhanced Fcgamma receptor I, alphaMbeta2 integrin receptor expression by monocytes and neutrophils in rheumatoid arthritis: interaction with platelets. J Rheumatol 31(12):2347–2355

    CAS  PubMed  Google Scholar 

  15. Xu J, Lupu F, Esmon CT (2010) Inflammation, innate immunity and blood coagulation. Hamostaseologie 30(1):5–6, 8–9

  16. Maradit-Kremers H, Nicola PJ, Crowson CS, Ballman KV, Jacobsen SJ, Roger VL, Gabriel SE (2007) Raised erythrocyte sedimentation rate signals heart failure in patients with rheumatoid arthritis. Ann Rheum Dis 66(1):76–80

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Vijayakumar D, Suresh K, Manoharan S (2005) Altered pattern of lipids in plasma and erythrocyte membranes of rheumatoid arthritis patients. Indian J Clin Biochem 20(1):52–55

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Taubert D, Lazar A, Grimberg G, Jung N, Rubbert A, Delank KS, Perniok A, Erdmann E, Schomig E (2006) Association of rheumatoid arthritis with ergothioneine levels in red blood cells: a case control study. J Rheumatol 33(11):2139–2145

    CAS  PubMed  Google Scholar 

  19. Papadaki HA, Kritikos HD, Valatas V, Boumpas DT, Eliopoulos GD (2002) Anemia of chronic disease in rheumatoid arthritis is associated with increased apoptosis of bone marrow erythroid cells: improvement following anti–tumor necrosis factor-α antibody therapy. J Am Soc Hematol 100:474–482

    CAS  Google Scholar 

  20. Wilson A, Yu H, Goodnough LT, Nissenson AR (2004) Prevalence and outcomes of anemia in rheumatoid arthritis: a systematic review of the literature. Am J Med 116:50S–57S

    Article  PubMed  Google Scholar 

  21. Nikolaisen C, Figenschau Y, Nossent JC (2008) Anemia in early rheumatoid arthritis is associated with interleukin 6-mediated bone marrow suppression, but has no effect on disease course or mortality. J Rheumatol 35:380–386

    CAS  PubMed  Google Scholar 

  22. Lee WS, Kim T-Y (2010) Relation between red blood cell distribution width and inflammatory biomarkers in rheumatoid arthritis. Arch Pathol Lab Med 134:505–506

    PubMed  Google Scholar 

  23. Zhou Y, Zhang Q, Yan L, Li Y, Hua L (2015) Association between red cell distribution width and myocardial infarction in rheumatoid arthritis. Clin Chem Lab Med 53(7):e153–e155

    Article  CAS  PubMed  Google Scholar 

  24. Goodman SR, Daescu O, Kakhniashvili DG, Zivanic M (2013) The proteomics and interactomics of human erythrocytes. Exp Biol Med 238(5):509–518

    Article  Google Scholar 

  25. Iwaki-Egawa S, Matsuno H, Yudoh K, Nakazawa F, Miyazaki K, Ochiai A et al (2004) High diagnostic value of anticalpastatin autoantibodies in rheumatoid arthritis detected by ELISA using human erythrocyte calpastatin as antigen. J Rheumatol 31:17–22

    CAS  PubMed  Google Scholar 

  26. Kontos S, Kourtis IC, Dane KY, Hubbell JA (2013) Engineering antigens for in situ erythrocyte binding induces T-cell deletion. Proc Natl Acad Sci 110(1):E60–E68

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Meyer PWA, Hodkinson B, Ally M, Musenge E, Wadee AA, Fickl H, et al (2011) Circulating cytokine profiles and their relationships with autoantibodies, acute phase reactants, and disease activity in patients with rheumatoid arthritis. Mediators of inflammation 2010

  28. Staroń A, Mąkosa G, Koter-Michalak M (2012) Oxidative stress in erythrocytes from patients with rheumatoid arthritis. Rheumatol Int 32(2):331–334

    Article  PubMed Central  PubMed  Google Scholar 

  29. Wolfe F, Sharp JT (1998) Radiographic outcome of recent-onset rheumatoid arthritis: a 19-year study of radiographic progression. Arthritis Rheum 41(9):1571–1582

    Article  CAS  PubMed  Google Scholar 

  30. De Oliveira S, De Almeida VV, Calado A, Rosário HS, Saldanha C (2012) Integrin-associated protein (CD47) is a putative mediator for soluble fibrinogen interaction with human red blood cells membrane. Biochim Biophys Acta 1818(3):481–490

    Article  PubMed  Google Scholar 

  31. Saldanha C, Freitas T, Almeida JP (2012) Fibrinogen effects on erythrocyte nitric oxide mobilization in presence of acetylcholine. Life Sci 91(21–22):1017–1022

    Article  CAS  PubMed  Google Scholar 

  32. Saldanha C, Freitas T, Lopez de Almeida JP, Silva-Herdade A (2014) Signal transduction pathways in erythrocyte nitric oxide metabolism under high fibrinogen levels. Korea-Aust Rheol J 26(2):217–223

    Article  Google Scholar 

  33. Glasmästar K, Larsson C, Höök F, Kasemo B (2002) Protein adsorption on supported phospholipid bilayers. J Colloid Interface Sci 246(1):40–47

    Article  PubMed  Google Scholar 

  34. Mbamala EC, Ben-Shaul A, May S (2005) Domain formation induced by the adsorption of charged proteins on mixed lipid membranes. Biophys J 88(3):1702–1714

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Jewell SA, Petrov PG, Winlove CP (2013) The effect of oxidative stress on the membrane dipole potential of human red blood cells. Biochim Biophys Acta 1828(4):1250–1258

    Article  CAS  PubMed  Google Scholar 

  36. Hilliquin P, Borderie D, Hernvann A, Menkes CJ, Ekindjian OG (1997) Nitric oxide as s-nitrosoproteins in rheumatoid arthritis. Arthritis Rheum 40(8):1512–1517

    Article  CAS  PubMed  Google Scholar 

  37. Aryaeian N, Djalali M, Shahram F, Jazayeri S, Chamari M, Nazari S (2011) Beta-Carotene, Vitamin E, MDA, glutathione reductase and arylesterase activity levels in patients with active rheumatoid arthritis. Iranian J Public Health 40(2):102–109

    CAS  Google Scholar 

  38. Mohr S, Hallak H, de Boitte A, Lapetina EG, Brüne B (1999) Nitric oxide-induced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 274(14):9427–9430

    Article  CAS  PubMed  Google Scholar 

  39. Toms TE, Symmons DP, Kitas DG (2010) Dyslipidaemia in rheumatoid arthritis: the role of inflammation, drugs, lifestyle and genetic factors. Curr Vasc Pharmacol 8:301–326

    Article  CAS  PubMed  Google Scholar 

  40. Myasoedova E, Crowson CS, Kremers HM, Roger VL, Fitz-Gibbon PD, Therneau TM et al (2011) Lipid paradox in rheumatoid arthritis: the impact of serum lipid measures and systemic inflammation on the risk of cardiovascular disease. Ann Rheum Dis 70(3):482–487

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  41. van Zwieten R, Bochem AE, Hilarius PM, vanBruggen R, Bergkamp F, Hovingh GK, Verhoeven AJ (2012) The cholesterol content of the erythrocyte membrane is an important determinant of phosphatidylserine exposure. Biochim Biophys Acta 182(12):1493–1500

    Article  Google Scholar 

  42. Rubin O, Canellini G, Delobel J, Lion N, Tissot J-D (2012) Red blood cell microparticles: clinical relevance. Transfus Med Hemother 39(5):342

    Article  PubMed Central  PubMed  Google Scholar 

  43. Bosman GJ, Lasonder E, Groenen-Döpp YAM, Willekens FLA, Werre JM (2012) The proteome of erythrocyte-derived microparticles from plasma: new clues for erythrocyte aging and vesiculation. J Proteom 76:203–210

    Article  CAS  Google Scholar 

  44. Mouro-Chanteloup I, Delaunay J, Gane P, Nicolas V, Johansen M, Brown EJ, Peters LL, Le Van Kim C, Cartron JP, Colin Y (2003) Evidence that the red cell skeleton protein 4.2 interacts with the Rh membrane complex member CD47 vol 101

  45. Leventis PA, Grinstein S (2010) The distribution and function of phosphatidylserine in cellular membranes. Annu Rev Biophys 39:407–427

    Article  CAS  PubMed  Google Scholar 

  46. Miyabe Y, Miyabe C, Iwai Y, Yokoyama W, Sekine C, Sugimoto K, Harigai M, Miyasaka M, Miyasaka N, Nanki T (2014) Activation of fibroblast-like synoviocytes derived from rheumatoid arthritis via lysophosphatidic acid–lysophosphatidic acid receptor 1 cascade. Arthritis Res Ther 16(5):461

    Article  PubMed Central  PubMed  Google Scholar 

  47. Neidlinger NA, Larkin SK, Bhagat A, Victorino GP, Kuypers FA (2006) Hydrolysis of phosphatidylserine-exposing red blood cells by secretory phospholipase A2 generates lysophosphatidic acid and results in vascular dysfunction. J Biol Chem 281(2):775–781

    Article  CAS  PubMed  Google Scholar 

  48. Aoki J (2004) Mechanisms of lysophosphatidic acid production. In: Seminars in cell & developmental biology: 2004. Elsevier, pp 477–489

  49. Yang L, Andrews DA, Low PS (2000) Lysophosphatidic acid opens a Ca++ channel in human erythrocytes. Blood 95(7):2420–2425

    CAS  PubMed  Google Scholar 

  50. Khorchid A, Ikura M (2002) How calpain is activated by calcium. Nat Struct Mol Biol 9(4):239–241

    Article  CAS  Google Scholar 

  51. Muravyov A, Tikhomirova I (2012) Role Ca2 + in mechanisms of the red blood cells microrheological changes. In: Calcium signaling. Springer, pp 1017–1038

  52. Chung S-M, Bae O-N, Lim K-M, Noh J-Y, Lee M-Y, Jung Y-S, Chung J-H (2007) Lysophosphatidic acid induces thrombogenic activity through phosphatidylserine exposure and procoagulant microvesicle generation in human erythrocytes. Arterioscler Thromb Vasc Biol 27(2):414–421

    Article  CAS  PubMed  Google Scholar 

  53. Weerheim A, Kolb A, Sturk A, Nieuwland R (2002) Phospholipid composition of cell-derived microparticles determined by one-dimensional high-performance thin-layer chromatography. Anal Biochem 302(2):191–198

    Article  CAS  PubMed  Google Scholar 

  54. Butikofer P, Kuypers F, Xu C, Chiu D, Lubin B (1989) Enrichment of two glycosyl-phosphatidylinositol-anchored proteins, acetylcholinesterase and decay accelerating factor, in vesicles released from human red blood cells. Blood 74(5):1481–1485

    CAS  PubMed  Google Scholar 

  55. An X, Guo X, Sum H, Morrow J, Gratzer W, Mohandas N (2004) Phosphatidylserine binding sites in erythroid spectrin: location and implications for membrane stability. Biochemistry 43(2):310–315

    Article  CAS  PubMed  Google Scholar 

  56. Arosa FA, Pereira CF, Fonseca AM (2004) Red blood cells as modulators of T cell growth and survival. Curr Pharm Des 10(2):191–201

    Article  CAS  PubMed  Google Scholar 

  57. Profumo E, Buttari B, Petrone L, Straface E, Gambardella L, Pietraforte D, Genuini I, Capoano R, Salvati B, Malorni W (2011) Redox imbalance of red blood cells impacts T lymphocyte homeostasis: implication in carotid atherosclerosis. Thromb Haemost 106(6):1117

    Article  CAS  PubMed  Google Scholar 

  58. Antunes RF, Brandão C, Maia M, Arosa FA (2011) Red blood cells release factors with growth and survival bioactivities for normal and leukemic T cells. Immunol Cell Biol 89(1):111–121

    Article  CAS  PubMed  Google Scholar 

  59. Rubin O, Delobel J, Prudent M, Lion N, Kohl K, Tucker EI, Tissot JD, Angelillo-Scherrer A (2013) Red blood cell–derived microparticles isolated from blood units initiate and propagate thrombin generation. Transfusion 53(8):1744–1754

    Article  CAS  PubMed  Google Scholar 

  60. Kabouridis PS, Jury EC (2008) Lipid rafts and T-lymphocyte function: implications for autoimmunity. FEBS Lett 582(27):3711–3718

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  61. Hutchinson RM, Davis P, Jayson MI (1976) Thrombocytosis in rheumatoid arthritis. Ann Rheum Dis 35(2):138–142

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  62. Farr MSD, Constable TJ, Hawker RJ, Hawkins CF, Stuart J (1983) Thrombocytosis of active rheumatoid disease. Ann Rheum Dis 42:545–549

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  63. Yazici S, Yazici M, Erer B, Erer B, Calik Y, Ozhan H et al (2010) The platelet indices in patients with rheumatoid arthritis: mean platelet volume reflects disease activity. Platelets 21:122–125

    Article  CAS  PubMed  Google Scholar 

  64. Gasparyan AY, Stavropoulos-Kalinoglou A, Toms TE, Douglas KMJ, Kitas GD (2010) Association of mean platelet volume with hypertension in rheumatoid arthritis. Inflamm Allergy Drug Targets 9:45–50

    Article  CAS  PubMed  Google Scholar 

  65. Habets KL, Huizinga TW, Toes RE (2013) Platelets and autoimmunity. Eur J Clin Invest 43:746–757

    Article  CAS  PubMed  Google Scholar 

  66. Boilard E, Blanco P, Nigrovic PA (2012) Platelets: active players in the pathogenesis of arthritis and SLE. Nat Rev Rheumatol 8:534–542

    Article  CAS  PubMed  Google Scholar 

  67. Senzel L, Gnatenko DV, Bahou WF (2009) The platelet proteome. Curr Opin Hematol 16(5):329–333

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  68. Cloutier N, Tan S, Boudreau LH, Cramb C, Subbaiah R, Lahey L, Albert A, Shnayder R, Gobezie R, Nigrovic PA et al (2013) The exposure of autoantigens by microparticles underlies the formation of potent inflammatory components: the microparticle-associated immune complexes. EMBO Mol Med 5:235–249

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  69. Cloutier N, Pare A, Farndale RW, Schumacher HR, Nigrovic PA, Lacroix S et al (2012) Platelets can enhance vascular permeability. J Am Soc Hematol 120:1334–1343

    CAS  Google Scholar 

  70. Gitz E, Pollitt AY, Gitz-Francois JJ, Alshehri O, Mori J, Montague S, Nash GB, Douglas MR, Gardiner EE, Andrews RK et al (2014) CLEC-2 expression is maintained on activated platelets and on platelet microparticles. Blood 124:2262

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  71. Pietraforte D, Vona R, Marchesi A, de Jacobis IT, Villani A, Del Principe D, Straface E (2014) Redox control of platelet functions in physiology and pathophysiology. Antioxid Redox Signal 21(1):177–193

    Article  CAS  PubMed  Google Scholar 

  72. Knijff-Dutmer EAJ, Koerts J, Nieuwland R, Kalsbeek-Batenburg EM, Van De Laar MAFJ (2002) Elevated levels of platelet microparticles are associated with disease activity in rheumatoid arthritis. Arthritis Rheum 46:1498–1503

    Article  CAS  PubMed  Google Scholar 

  73. Nurden AT (2011) Platelets, inflammation and tissue regeneration. Thromb Haemost 105(Suppl 1):S13–S33

    Article  CAS  PubMed  Google Scholar 

  74. Almasry SM, Soliman HM, El-Tarhouny SA, Algaidi SA, Ragab EM (2015) Platelet rich plasma enhances the immunohistochemical expression of platelet derived growth factor and vascular endothelial growth factor in the synovium of the meniscectomized rat models of osteoarthritis. Ann Anat 197:38–49

    Article  PubMed  Google Scholar 

  75. Vallés J, Santos MT, Aznar J, Martínez M, Moscardó A, Piñón M, Broekman MJ, Marcus AJ (2002) Platelet-erythrocyte interactions enhance αIIbβ3 integrin receptor activation and P-selectin expression during platelet recruitment: down-regulation by aspirin ex vivo. Blood 99(11):3978–3984

    Article  PubMed  Google Scholar 

  76. Valles J, Santos M, Aznar J, Marcus A, Martinez-Sales V, Portoles M, Broekman M, Safier L (1991) Erythrocytes metabolically enhance collagen-induced platelet responsiveness via increased thromboxane production, adenosine diphosphate release, and recruitment. Blood 78:154–162

    CAS  PubMed  Google Scholar 

  77. Berckmans RJ, Nieuwland R, Tak PP, Böing AN, Romijn FP, Kraan MC, Breedveld FC, Hack CE, Sturk A (2002) Cell-derived microparticles in synovial fluid from inflamed arthritic joints support coagulation exclusively via a factor VII–dependent mechanism. Arthritis Rheum 46(11):2857–2866

    Article  CAS  PubMed  Google Scholar 

  78. Danesh A, Inglis HC, Jackman RP, Wu S, Deng X, Muench MO, Heitman JW, Norris PJ (2014) Exosomes from red blood cell units bind to monocytes and induce proinflammatory cytokines, boosting T-cell responses in vitro. Blood 123:687–696

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  79. Biró É, Nieuwland R, Tak PP, Pronk LM, Schaap MC, Sturk A, Hack CE (2007) Activated complement components and complement activator molecules on the surface of cell-derived microparticles in patients with rheumatoid arthritis and healthy individuals. Ann Rheum Dis 66(8):1085–1092

    Article  PubMed Central  PubMed  Google Scholar 

  80. Beyer C, Pisetsky DS (2010) The role of microparticles in the pathogenesis of rheumatic diseases. Nat Rev Rheumatol 6(1):21–29

    Article  CAS  PubMed  Google Scholar 

  81. Jy W, Johansen ME, Bidot C, Horstman LL, Ahn YS (2013) Red cell-derived microparticles (RMP) as haemostatic agent. Thromb Haemost 110(4):751–760

    Article  CAS  PubMed  Google Scholar 

  82. Horne MK, Cullinane AM, Merryman PK, Hoddeson EK (2006) The effect of red blood cells on thrombin generation. Br J Haematol 133(4):403–408

    Article  CAS  PubMed  Google Scholar 

  83. Whelihan MF, Mann KG (2013) The role of the red cell membrane in thrombin generation. Thromb Res 131(5):377–382

    Article  CAS  PubMed  Google Scholar 

  84. Bonomini M, Sirolli V, Merciaro G, Antidormi T, Di Liberato L, Brummer U, Papponetti M, Cappelli P, Di Gregorio P, Arduini A (2005) Red blood cells may contribute to hypercoagulability in uraemia via enhanced surface exposure of phosphatidylserine. Nephrol Dial Transplant 20(2):361–366

    Article  CAS  PubMed  Google Scholar 

  85. Spoerke NJ, Van PY, Differding JA, Zink KA, Cho SD, Muller PJ, Karahan ZA, Sondeen JL, Holcomb JB, Schreiber MA (2010) Red blood cells accelerate the onset of clot formation in polytrauma and hemorrhagic shock. J Trauma Acute Care Surg 69(5):1054–1061

    Article  Google Scholar 

  86. Goldschmidt N, Spectre G, Brill A, Zelig O, Goldfarb A, Rachmilewitz E, Varon D (2008) Increased platelet adhesion under flow conditions is induced by both thalassemic platelets and red blood cells. Thromb Haemost 100(5):864–870

    CAS  PubMed  Google Scholar 

  87. Perez V, Johansen ME, Jy W, Horstman L, Ahn YS (2013) Interaction of platelets with red cell-derived microparticles (RMP): RMP increase platelet aggregate size in a shear-dependent manner. Blood 122(21):3580

    Google Scholar 

  88. Xiong Z, Cavaretta J, Qu L, Stolz DB, Triulzi D, Lee JS (2011) Red blood cell microparticles show altered inflammatory chemokine binding and release ligand upon interaction with platelets. Transfusion 51(3):610–621

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  89. Hakala M, Risteli L, Manelius J, Nieminen P, Risteli J (1993) Increased type I collagen degradation correlates with disease severity in rheumatoid arthritis. Ann Rheum Dis 52(12):866–869

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  90. King KL, Cidlowski JA (1995) Cell cycle and apoptosis: common pathways to life and death. J Cell Biochem 58(2):175–180

    Article  CAS  PubMed  Google Scholar 

  91. Zwaal RFA, Comfurius P, Bevers EM (2005) Surface exposure of phosphatidylserine in pathological cells. CMLS, Cell Mol Life Sci 62(9):971–988

    Article  CAS  PubMed  Google Scholar 

  92. Abed M, Towhid ST, Mia S, Pakladok T, Alesutan I, Borst O, Gawaz M, Gulbins E, Lang F (2012) Sphingomyelinase-induced adhesion of eryptotic erythrocytes to endothelial cells. Am J Physiol Cell Physiol 303(9):C991–C999

    Article  CAS  PubMed  Google Scholar 

  93. Walker B, Towhid ST, Schmid E, Hoffmann SM, Abed M, Münzer P, Vogel S, Neis F, Brucker S, Gawaz M et al (2014) Dynamic adhesion of eryptotic erythrocytes to immobilized platelets via platelet phosphatidylserine receptors. Am J Physiol Cell Physiol 306:C291–C297

    Article  CAS  PubMed  Google Scholar 

  94. Hermand P, Gane P, Huet M, Jallu V, Kaplan C, Sonneborn HH, Cartron J-P, Bailly P (2003) Red cell ICAM-4 is a novel ligand for platelet-activated αIIbβ3 integrin. J Biol Chem 278(7):4892–4898

    Article  CAS  PubMed  Google Scholar 

  95. Du VX, Huskens D, Maas C, Al Dieri R, de Groot PG, de Laat B (2014) New insights into the role of erythrocytes in thrombus formation. Semin Thromb Hemost 40(1):72–80

    CAS  PubMed  Google Scholar 

  96. Hernández-Hernández A, Rodríguez MC, López-Revuelta A, Sánchez-Gallego JI, Shnyrov V, Llanillo M, Sánchez-Yagüe J (2006) Alterations in erythrocyte membrane protein composition in advanced non-small cell lung cancer. Blood Cells Mol Dis 36(3):355–363

    Article  PubMed  Google Scholar 

  97. Gupta P, Vijayan VK, Bansal SK (2012) Changes in protein profile of erythrocyte membrane in bronchial asthma. J Asthma 49(2):129–133

    Article  CAS  PubMed  Google Scholar 

  98. De Castro J, Hernández-Hernández A, Rodríguez MC, Sardina JL, Llanillo M, Sánchez-Yagüe J (2007) Comparison of changes in erythrocyte and platelet phospholipid and fatty acid composition and protein oxidation in chronic obstructive pulmonary disease and asthma. Platelets 18(1):43–51

    Article  PubMed  Google Scholar 

  99. Bochsen L, Johansson PI, Kristensen AT, Daugaard G, Ostrowski SR (2011) The influence of platelets, plasma and red blood cells on functional haemostatic assays. Blood Coagul Fibrinolysis 22(3):167–175

    Article  PubMed  Google Scholar 

  100. Santos M, Valles J, Lago A, Tembl J, Sanchez E, Moscardo A, Cosin J (2008) Residual platelet thromboxane A2 and prothrombotic effects of erythrocytes are important determinants of aspirin resistance in patients with vascular disease. J Thromb Haemost 6(4):615–621

    Article  CAS  PubMed  Google Scholar 

Download references

Conflict of interest

The authors have no conflict of interest to declare.

Author information

Authors and Affiliations

  1. Department of Physiology, Faculty of Health Sciences, University of Pretoria, Private Bag x323, Arcadia, 0007, South Africa

    Oore-ofe O. Olumuyiwa-Akeredolu & Etheresia Pretorius

Authors
  1. Oore-ofe O. Olumuyiwa-Akeredolu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Etheresia Pretorius
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Etheresia Pretorius.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Olumuyiwa-Akeredolu, Oo.O., Pretorius, E. Platelet and red blood cell interactions and their role in rheumatoid arthritis. Rheumatol Int 35, 1955–1964 (2015). https://doi.org/10.1007/s00296-015-3300-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00296-015-3300-7

Keywords

Search

Navigation