Semin Thromb Hemost 2018; 44(07): 669-675
DOI: 10.1055/s-0038-1648232
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Hemostasis in Allergy

Zahava Vadasz
1   Division of Allergy and Clinical Immunology, Bnai-Zion Medical Center, Technion Faculty of Medicine, Haifa, Israel
,
Elias Toubi
1   Division of Allergy and Clinical Immunology, Bnai-Zion Medical Center, Technion Faculty of Medicine, Haifa, Israel
› Author Affiliations
Further Information

Publication History

Publication Date:
19 June 2018 (online)

Abstract

The involvement of the hemostatic system in immune-mediated inflammation is widely reported. Many coagulation factors play a role in the pathogenesis of autoimmune diseases, such as systemic vasculitis and systemic lupus erythematosus. Hemostatic disorders are also involved in asthma and chronic spontaneous urticaria (CSU). Factor XIIa (FXIIa) was one of the first coagulation factors implicated in inducing both humoral and cellular responses and is therefore considered a prime new therapeutic target in immune-mediated inflammation. The involvement of coagulation factors, such as tissue factor and fibrinogen, in the pathogenesis of asthma has been reported. The finding of platelet activation in asthma also indicates a link between bronchial inflammation and hemostasis. The pathogenesis of mast cell degranulation and CSU was also shown to be associated with the activation of hemostatic factors such as fibrinogen and FXIIa. Increased plasma levels of D-dimer have been widely reported as a biological marker for the duration and severity of CSU. In addition, endothelial-induced cell activation by the kallikrein–high molecular weight complex and the release of heat shock protein 90 was shown to be involved in mast cell degranulation disorders. In this narrative review, the authors aim to summarize the role of hemostasis in inflammation, asthma, and CSU by focusing on the increasing information linking hemostatic factors and immune-mediated disorders.

 
  • References

  • 1 Schoenmakers SH, Reitsma PH, Spek CA. Blood coagulation factors as inflammatory mediators. Blood Cells Mol Dis 2005; 34 (01) 30-37
  • 2 Ryu JK, Petersen MA, Murray SG. , et al. Blood coagulation protein fibrinogen promotes autoimmunity and demyelination via chemokine release and antigen presentation. Nat Commun 2015; 6: 8164
  • 3 Liang Y, Leng RX, Pan HF, Ye DQ. The prevalence and risk factors for serositis in patients with systemic lupus erythematosus: a cross-sectional study. Rheumatol Int 2017; 37 (02) 305-311
  • 4 Katz OB, Brenner B, Horowitz NA. Thrombosis in vasculitic disorders-clinical manifestations, pathogenesis and management. Thromb Res 2015; 136 (03) 504-512
  • 5 Huang YM, Wang H, Wang C, Chen M, Zhao MH. Promotion of hypercoagulability in antineutrophil cytoplasmic antibody-associated vasculitis by C5a-induced tissue factor-expressing microparticles and neutrophil extracellular traps. Arthritis Rheumatol 2015; 67 (10) 2780-2790
  • 6 Shen J, Ran ZH, Zhang Y. , et al. Biomarkers of altered coagulation and fibrinolysis as measures of disease activity in active inflammatory bowel disease: a gender-stratified, cohort analysis. Thromb Res 2009; 123 (04) 604-611
  • 7 Scaldaferri F, Lancellotti S, Pizzoferrato M, De Cristofaro R. Haemostatic system in inflammatory bowel diseases: new players in gut inflammation. World J Gastroenterol 2011; 17 (05) 594-608
  • 8 Chu AJ. Blood coagulation as an intrinsic pathway for proinflammation: a mini review. Inflamm Allergy Drug Targets 2010; 9 (01) 32-44
  • 9 Vorlova S, Koch M, Manthey HD. , et al. Coagulation factor XII induces pro-inflammatory cytokine responses in macrophages and promotes atherosclerosis in mice. Thromb Haemost 2017; 117 (01) 176-187
  • 10 Jiang P, Xue D, Zhang Y. , et al. The extrinsic coagulation cascade and tissue factor pathway inhibitor in macrophages: a potential therapeutic opportunity for atherosclerotic thrombosis. Thromb Res 2014; 133 (04) 657-666
  • 11 Zuo P, Zuo Z, Wang X. , et al. Factor Xa induces pro-inflammatory cytokine expression in RAW 264.7 macrophages via protease-activated receptor-2 activation. Am J Transl Res 2015; 7 (11) 2326-2334
  • 12 Soendergaard C, Kvist PH, Seidelin JB, Pelzer H, Nielsen OH. Systemic and intestinal levels of factor XIII-A: the impact of inflammation on expression in macrophage subtypes. J Gastroenterol 2016; 51 (08) 796-807
  • 13 Hsieh JY, Smith TD, Meli VS, Tran TN, Botvinick EL, Liu WF. Differential regulation of macrophage inflammatory activation by fibrin and fibrinogen. Acta Biomater 2017; 47: 14-24
  • 14 Draxler DF, Sashindranath M, Medcalf RL. Plasmin: a modulator of immune function. Semin Thromb Hemost 2017; 43 (02) 143-153
  • 15 Kawecki C, Lenting PJ, Denis CV. von Willebrand factor and inflammation. J Thromb Haemost 2017; 15 (07) 1285-1294
  • 16 Hofman Z, de Maat S, Hack CE, Maas C. Bradykinin: inflammation product of the coagulation system. Clin Rev Allergy Immunol 2016; 51 (02) 152-161
  • 17 Joseph K, Kaplan AP. Formation of bradykinin: a major contributor to the innate inflammatory response. Adv Immunol 2005; 86: 159-208
  • 18 Shukla HD, Pitha PM. Role of HSP90 in systemic lupus erythematosus and its clinical relevance. Autoimmune Dis 2012; 2012: 728605
  • 19 Saito K, Kukita K, Kutomi G. , et al. Heat shock protein 90 associates with Toll-like receptors 7/9 and mediates self-nucleic acid recognition in SLE. Eur J Immunol 2015; 45 (07) 2028-2041
  • 20 Sneeboer MMS, Fens N, van de Pol MA. , et al. Loss of asthma control and activation of coagulation and fibrinolysis. Clin Exp Allergy 2016; 46 (03) 422-427
  • 21 Green RH, Brightling CE, McKenna S. , et al. Asthma exacerbations and sputum eosinophil counts: a randomised controlled trial. Lancet 2002; 360 (9347): 1715-1721
  • 22 Esmon CT. The interactions between inflammation and coagulation. Br J Haematol 2005; 131 (04) 417-430
  • 23 Levi M, van der Poll T. Inflammation and coagulation. Crit Care Med 2010; 38 (2, Suppl): S26-S34
  • 24 Brims FJ, Chauhan AJ, Higgins B, Shute JK. Coagulation factors in the airways in moderate and severe asthma and the effect of inhaled steroids. Thorax 2009; 64 (12) 1037-1043
  • 25 Kanazawa H, Yoshikawa T. Up-regulation of thrombin activity induced by vascular endothelial growth factor in asthmatic airways. Chest 2007; 132 (04) 1169-1174
  • 26 Ma Z, Paek D, Oh CK. Plasminogen activator inhibitor-1 and asthma: role in the pathogenesis and molecular regulation. Clin Exp Allergy 2009; 39 (08) 1136-1144
  • 27 Kowal K, Bodzenta-Lukaszyk A, Pampuch A, Szmitkowski M, Donati MB, Iacoviello L. Plasminogen activator inhibitor-1 plasma concentration in allergic asthma patients during allergen challenge. Int Arch Allergy Immunol 2007; 144 (03) 240-246
  • 28 Schouten M, van de Pol MA, Levi M, van der Poll T, van der Zee JS. Early activation of coagulation after allergen challenge in patients with allergic asthma. J Thromb Haemost 2009; 7 (09) 1592-1594
  • 29 Buyukyilmaz G, Soyer OU, Buyuktiryaki B, Alioglu B, Dallar Y. Platelet aggregation, secretion, and coagulation changes in children with asthma. Blood Coagul Fibrinolysis 2014; 25 (07) 738-744
  • 30 Wagers SS, Norton RJ, Rinaldi LM, Bates JH, Sobel BE, Irvin CG. Extravascular fibrin, plasminogen activator, plasminogen activator inhibitors, and airway hyperresponsiveness. J Clin Invest 2004; 114 (01) 104-111
  • 31 Brims FJ, Chauhan AJ, Higgins B, Shute JK. Up-regulation of the extrinsic coagulation pathway in acute asthma--a case study. J Asthma 2010; 47 (06) 695-698
  • 32 Thomas VA, Wheeless CJ, Stack MS, Johnson DA. Human mast cell tryptase fibrinogenolysis: kinetics, anticoagulation mechanism, and cell adhesion disruption. Biochemistry 1998; 37 (08) 2291-2298
  • 33 Bastarache JA, Wang L, Geiser T. , et al. The alveolar epithelium can initiate the extrinsic coagulation cascade through expression of tissue factor. Thorax 2007; 62 (07) 608-616
  • 34 de Boer JD, Majoor CJ, van 't Veer C, Bel EH, van der Poll T. Asthma and coagulation. Blood 2012; 119 (14) 3236-3244
  • 35 Moosbauer C, Morgenstern E, Cuvelier SL. , et al. Eosinophils are a major intravascular location for tissue factor storage and exposure. Blood 2007; 109 (03) 995-1002
  • 36 Sovershaev MA, Lind KF, Devold H. , et al. No evidence for the presence of tissue factor in high-purity preparations of immunologically isolated eosinophils. J Thromb Haemost 2008; 6 (10) 1742-1749
  • 37 Trompette A, Divanovic S, Visintin A. , et al. Allergenicity resulting from functional mimicry of a Toll-like receptor complex protein. Nature 2009; 457 (7229): 585-588
  • 38 Millien VO, Lu W, Shaw J. , et al. Cleavage of fibrinogen by proteinases elicits allergic responses through Toll-like receptor 4. Science 2013; 341 (6147): 792-796
  • 39 Lambrecht BN, Hammad H. Asthma and coagulation. N Engl J Med 2013; 369 (20) 1964-1966
  • 40 Arnot CJ, Gay NJ, Gangloff M. Molecular mechanism that induces activation of Spätzle, the ligand for the Drosophila Toll receptor. J Biol Chem 2010; 285 (25) 19502-19509
  • 41 Hammad H, Chieppa M, Perros F, Willart MA, Germain RN, Lambrecht BN. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat Med 2009; 15 (04) 410-416
  • 42 Kowal K, Pampuch A, Kowal-Bielecka O, DuBuske LM, Bodzenta-Łukaszyk A. Platelet activation in allergic asthma patients during allergen challenge with Dermatophagoides pteronyssinus. Clin Exp Allergy 2006; 36 (04) 426-432
  • 43 Hasegawa S, Pawankar R, Suzuki K. , et al. Functional expression of the high affinity receptor for IgE (FcepsilonRI) in human platelets and its' intracellular expression in human megakaryocytes. Blood 1999; 93 (08) 2543-2551
  • 44 Yamamoto H, Nagata M, Tabe K. , et al. The evidence of platelet activation in bronchial asthma. J Allergy Clin Immunol 1993; 91 (1 Pt 1): 79-87
  • 45 Louis RE, Radermecker MF. Acute bronchial obstruction following inhalation of PAF in asthmatic and normal subjects: comparison with methacholine. Eur Respir J 1996; 9 (07) 1414-1420
  • 46 Hsieh KH, Ng CK. Increased plasma platelet-activating factor in children with acute asthmatic attacks and decreased in vivo and in vitro production of platelet-activating factor after immunotherapy. J Allergy Clin Immunol 1993; 91 (02) 650-657
  • 47 Gresele P, Dottorini M, Selli ML. , et al. Altered platelet function associated with the bronchial hyperresponsiveness accompanying nocturnal asthma. J Allergy Clin Immunol 1993; 91 (04) 894-902
  • 48 Harwell WB, Patterson JT, Lieberman P, Beachey E. Platelet aggregation in atopic and normal patients. J Allergy Clin Immunol 1973; 51 (05) 274-284
  • 49 Asero R, Tedeschi A, Coppola R. , et al. Activation of the tissue factor pathway of blood coagulation in patients with chronic urticaria. J Allergy Clin Immunol 2007; 119 (03) 705-710
  • 50 Asero R, Tedeschi A, Riboldi P, Griffini S, Bonanni E, Cugno M. Severe chronic urticaria is associated with elevated plasma levels of D-dimer. Allergy 2008; 63 (02) 176-180
  • 51 Rabelo-Filardi R, Daltro-Oliveira R, Campos RA. Parameters associated with chronic spontaneous urticaria duration and severity: a systematic review. Int Arch Allergy Immunol 2013; 161 (03) 197-204
  • 52 Yanase Y, Takahagi S, Hide M. Chronic spontaneous urticaria and the extrinsic coagulation system. Allergol Int 2017; (e-pub ahead of print) DOI: 10.1016/j.alit.2017.09.003.
  • 53 Tedeschi A, Kolkhir P, Asero R. , et al. Chronic urticaria and coagulation: pathophysiological and clinical aspects. Allergy 2014; 69 (06) 683-691
  • 54 Wang D, Tang H, Shen Y, Wang F, Lin J, Xu J. Activation of the blood coagulation system in patients with chronic spontaneous urticaria. Clin Lab 2015; 61 (09) 1283-1288
  • 55 Kakeda M, Arock M, Schlapbach C, Yawalkar N. Increased expression of heat shock protein 90 in keratinocytes and mast cells in patients with psoriasis. J Am Acad Dermatol 2014; 70 (04) 683-690.e1
  • 56 Tukaj S, Zillikens D, Kasperkiewicz M. Heat shock protein 90: a pathophysiological factor and novel treatment target in autoimmune bullous skin diseases. Exp Dermatol 2015; 24 (08) 567-571
  • 57 Kolkhir P, Pogorelov D, Olisova O. CRP, D-dimer, fibrinogen and ESR as predictive markers of response to standard doses of levocetirizine in patients with chronic spontaneous urticaria. Eur Ann Allergy Clin Immunol 2017; 49 (04) 189-192
  • 58 Asero R. Serial D-dimer plasma levels in a patient with chronic spontaneous urticaria developing resistance to omalizumab. Clin Exp Dermatol 2017; 42 (06) 667-669