RSS-Feed abonnieren
Bitte kopieren Sie die angezeigte URL und fügen sie dann in Ihren RSS-Reader ein.
https://www.thieme-connect.de/rss/thieme/de/10.1055-s-00033990.xml
PDF herunterladen
CC BY 4.0 · TH Open 2019; 03(02): e165-e170
DOI: 10.1055/s-0039-1692204
DOI: 10.1055/s-0039-1692204
Review Article
Emerging Factors Implicated in Fibrotic Organ–Associated Thrombosis: The Case of Two Organs
Funding This work was funded in part by NHLBI R01HL136363 and NIH R01HL080442 (K.R.), NIH R01HL132325 and R01CA175382 (V.C.C.), and the Thrombosis and Hemostasis Affinity Research Collaborative (ARC0 funded by the Evans Center for Interdisciplinary Biomedical Research).
Weitere Informationen
Publikationsverlauf
11. Februar 2019
30. April 2019
Publikationsdatum:
07. Juni 2019 (online)
Abstract
Thrombosis is at the heart of cardiovascular complications observed in specific diseases. A heightened thrombosis risk above that in general population in diseases such as myelofibrosis and chronic kidney disease implicates disease-specific mediators of thrombosis. This relative lack of information regarding the mechanisms of thrombosis in specific organ pathologies hitherto has remained limited. Evolving literature implicates some soluble factors in the blood of patients with discrete disorders, inflicting fundamental changes in the components of thrombosis. In this era of precision medicine, integrating these disease-specific factors in a comprehensive thrombotic risk assessment of patients is imperative in guiding therapeutic decisions. A complex network of mechanisms regulates each organ pathology and resultant thrombotic phenotypes. This review surveys different effectors of thrombogenicity associated with two pathologically fibrotic organs used as model systems, the bone marrow and kidney, as well as focuses attention to a common inducer of fibrosis and thrombosis, lysyl oxidase.
* These authors contributed equally.
-
References
- 1 Leiva O, Ng SK, Chitalia S, Balduini A, Matsuura S, Ravid K. The role of the extracellular matrix in primary myelofibrosis. Blood Cancer J 2017; 7 (02) e525
- 2 Tefferi A, Pardanani A. Myeloproliferative neoplasms: a contemporary review. JAMA Oncol 2015; 1 (01) 97-105
- 3 Falanga A, Marchetti M. Thrombosis in myeloproliferative neoplasms. Semin Thromb Hemost 2014; 40 (03) 348-358
- 4 Barbui T, Carobbio A, Cervantes F. , et al. Thrombosis in primary myelofibrosis: incidence and risk factors. Blood 2010; 115 (04) 778-782
- 5 Kc D, Falchi L, Verstovsek S. The underappreciated risk of thrombosis and bleeding in patients with myelofibrosis: a review. Ann Hematol 2017; 96 (10) 1595-1604
- 6 Rupoli S, Goteri G, Picardi P. , et al. Thrombosis in essential thrombocytemia and early/prefibrotic primary myelofibrosis: the role of the WHO histological diagnosis. Diagn Pathol 2015; 10: 29-36
- 7 Rungjirajittranon T, Owattanapanich W, Ungprasert P, Siritanaratkul N, Ruchutrakool T. A systematic review and meta-analysis of the prevalence of thrombosis and bleeding at diagnosis of Philadelphia-negative myeloproliferative neoplasms. BMC Cancer 2019; 19 (01) 184-192
- 8 Woo KT, Choong HL, Wong KS, Tan HB, Chan CM. The contribution of chronic kidney disease to the global burden of major noncommunicable diseases. Kidney Int 2012; 81 (10) 1044-1045
- 9 Hill NR, Fatoba ST, Oke JL. , et al. Global prevalence of chronic kidney disease - a systematic review and meta-analysis. PLoS One 2016; 11 (07) e0158765
- 10 Wattanakit K, Cushman M. Chronic kidney disease and venous thromboembolism: epidemiology and mechanisms. Curr Opin Pulm Med 2009; 15 (05) 408-412
- 11 Ocak G, Vossen CY, Rotmans JI. , et al. Venous and arterial thrombosis in dialysis patients. Thromb Haemost 2011; 106 (06) 1046-1052
- 12 Arber DA, Orazi A, Hasserjian R. , et al. The 2016 revision to the World Health Organization classification of myeloid neoplasms and acute leukemia. Blood 2016; 127 (20) 2391-2405
- 13 Bertozzi I, Bogoni G, Biagetti G. , et al. Thromboses and hemorrhages are common in MPN patients with high JAK2V617F allele burden. Ann Hematol 2017; 96 (08) 1297-1302
- 14 Pei YQ, Wu Y, Wang F, Cui W. Prognostic value of CALR vs. JAK2V617F mutations on splenomegaly, leukemic transformation, thrombosis, and overall survival in patients with primary fibrosis: a meta-analysis. Ann Hematol 2016; 95 (09) 1391-1398
- 15 Lamrani L, Lacout C, Ollivier V. , et al. Hemostatic disorders in a JAK2V617F-driven mouse model of myeloproliferative neoplasm. Blood 2014; 124 (07) 1136-1145
- 16 Etheridge SL, Roh ME, Cosgrove ME. , et al. JAK2V617F-positive endothelial cells contribute to clotting abnormalities in myeloproliferative neoplasms. Proc Natl Acad Sci U S A 2014; 111 (06) 2295-2300
- 17 Versteeg HH, Heemskerk JW, Levi M, Reitsma PH. New fundamentals in hemostasis. Physiol Rev 2013; 93 (01) 327-358
- 18 Furie B, Furie BC. Mechanisms of thrombus formation. N Engl J Med 2008; 359 (09) 938-949
- 19 Watson SP. Collagen receptor signaling in platelets and megakaryocytes. Thromb Haemost 1999; 82 (02) 365-376
- 20 Hollopeter G, Jantzen HM, Vincent D. , et al. Identification of the platelet ADP receptor targeted by antithrombotic drugs. Nature 2001; 409 (6817): 202-207
- 21 Wang Y, Gallant RC, Ni H. Extracellular matrix proteins in the regulation of thrombus formation. Curr Opin Hematol 2016; 23 (03) 280-287
- 22 Xu XR, Carrim N, Neves MA. , et al. Platelets and platelet adhesion molecules: novel mechanisms of thrombosis and anti-thrombotic therapies. Thromb J 2016; 14 (Suppl. 01) 29-38
- 23 Farndale RW, Sixma JJ, Barnes MJ, de Groot PG. The role of collagen in thrombosis and hemostasis. J Thromb Haemost 2004; 2 (04) 561-573
- 24 Angiolillo DJ, Ueno M, Goto S. Basic principles of platelet biology and clinical implications. Circ J 2010; 74 (04) 597-607
- 25 Moroi M, Jung SM, Okuma M, Shinmyozu K. A patient with platelets deficient in glycoprotein VI that lack both collagen-induced aggregation and adhesion. J Clin Invest 1989; 84 (05) 1440-1445
- 26 Kunicki TJ, Ruggeri ZM. Platelet collagen receptors and risk prediction in stroke and coronary artery disease. Circulation 2001; 104 (13) 1451-1453
- 27 Santoso S, Kunicki TJ, Kroll H, Haberbosch W, Gardemann A. Association of the platelet glycoprotein Ia C807T gene polymorphism with nonfatal myocardial infarction in younger patients. Blood 1999; 93 (08) 2449-2453
- 28 Moshfegh K, Wuillemin WA, Redondo M. , et al. Association of two silent polymorphisms of platelet glycoprotein Ia/IIa receptor with risk of myocardial infarction: a case-control study. Lancet 1999; 353 (9150): 351-354
- 29 Carlsson LE, Santoso S, Spitzer C, Kessler C, Greinacher A. The alpha2 gene coding sequence T807/A873 of the platelet collagen receptor integrin alpha2beta1 might be a genetic risk factor for the development of stroke in younger patients. Blood 1999; 93 (11) 3583-3586
- 30 Dodson PM, Haynes J, Starczynski J. , et al. The platelet glycoprotein Ia/IIa gene polymorphism C807T/G873A: a novel risk factor for retinal vein occlusion. Eye (Lond) 2003; 17 (06) 772-777
- 31 Roest M, Banga JD, Grobbee DE. , et al. Homozygosity for 807 T polymorphism in alpha(2) subunit of platelet alpha(2)beta(1) is associated with increased risk of cardiovascular mortality in high-risk women. Circulation 2000; 102 (14) 1645-1650
- 32 Bigalke B, Stellos K, Geisler T, Lindemann S, May AE, Gawaz M. Glycoprotein VI as a prognostic biomarker for cardiovascular death in patients with symptomatic coronary artery disease. Clin Res Cardiol 2010; 99 (04) 227-233
- 33 Alvarez-Larrán A, Arellano-Rodrigo E, Reverter JC. , et al. Increased platelet, leukocyte, and coagulation activation in primary myelofibrosis. Ann Hematol 2008; 87 (04) 269-276
- 34 Gremmel T, Gisslinger B, Gisslinger H, Panzer S. Response to aspirin therapy in patients with myeloproliferative neoplasms depends on the platelet count. Transl Res 2018; 200: 35-42
- 35 Guadall A, Lesteven E, Letort G. , et al. Endothelial cells harbouring the JAK2V617F mutation display pro-adherent and pro-thrombotic features. Thromb Haemost 2018; 118 (09) 1586-1599
- 36 Guy A, Gourdou-Latyszenok V, Le Lay N. , et al. Vascular endothelial cell expression of JAK2V617F is sufficient to promote a pro-thrombotic state due to increased P-selectin expression. Haematologica 2019; 104 (01) 70-81
- 37 Kogan I, Chap D, Hoffman R, Axelman E, Brenner B, Nadir Y. JAK-2 V617F mutation increases heparanase procoagulant activity. Thromb Haemost 2016; 115 (01) 73-80
- 38 Nadir Y, Brenner B, Zetser A. , et al. Heparanase induces tissue factor expression in vascular endothelial and cancer cells. J Thromb Haemost 2006; 4 (11) 2443-2451
- 39 Edelmann B, Gupta N, Schnoeder TM. , et al. JAK2-V617F promotes venous thrombosis through β1/β2 integrin activation. J Clin Invest 2018; 128 (10) 4359-4371
- 40 Barosi G, Massa M, Campanelli R. , et al. Primary myelofibrosis: older age and high JAK2V617F allele burden are associated with elevated plasma high-sensitivity C-reactive protein levels and a phenotype of progressive disease. Leuk Res 2017; 60: 18-23
- 41 Augello C, Cattaneo D, Bucelli C. , et al. CD18 promoter methylation is associated with a higher risk of thrombotic complications in primary myelofibrosis. Ann Hematol 2016; 95 (12) 1965-1969
- 42 Abbonante V, Chitalia V, Rosti V. , et al. Upregulation of lysyl oxidase and adhesion to collagen of human megakaryocytes and platelets in primary myelofibrosis. Blood 2017; 130 (06) 829-831
- 43 Papadantonakis N, Matsuura S, Ravid K. Megakaryocyte pathology and bone marrow fibrosis: the lysyl oxidase connection. Blood 2012; 120 (09) 1774-1781
- 44 Eliades A, Papadantonakis N, Bhupatiraju A. , et al. Control of megakaryocyte expansion and bone marrow fibrosis by lysyl oxidase. J Biol Chem 2011; 286 (31) 27630-27638
- 45 Matsuura S, Mi R, Koupenova M. , et al. Lysyl oxidase is associated with increased thrombosis and platelet reactivity. Blood 2016; 127 (11) 1493-1501
- 46 Anavekar NS, Pfeffer MA. Cardiovascular risk in chronic kidney disease. Kidney Int Suppl 2004; (92) S11-S15
- 47 Abboud H, Henrich WL. Clinical practice. Stage IV chronic kidney disease. N Engl J Med 2010; 362 (01) 56-65
- 48 Best PJ, Lennon R, Ting HH. , et al. The impact of renal insufficiency on clinical outcomes in patients undergoing percutaneous coronary interventions. J Am Coll Cardiol 2002; 39 (07) 1113-1119
- 49 Jain N, Li X, Adams-Huet B. , et al. Differences in whole blood platelet aggregation at baseline and in response to aspirin and aspirin plus clopidogrel in patients with versus without chronic kidney disease. Am J Cardiol 2016; 117 (04) 656-663
- 50 Gremmel T, Müller M, Steiner S. , et al. Chronic kidney disease is associated with increased platelet activation and poor response to antiplatelet therapy. Nephrol Dial Transplant 2013; 28 (08) 2116-2122
- 51 Addi T, Dou L, Burtey S. Tryptophan-derived uremic toxins and thrombosis in chronic kidney disease. Toxins (Basel) 2018; 10 (10) E412
- 52 Casserly LF, Dember LM. Thrombosis in end-stage renal disease. Semin Dial 2003; 16 (03) 245-256
- 53 Jain N, Hedayati SS, Sarode R, Banerjee S, Reilly RF. Antiplatelet therapy in the management of cardiovascular disease in patients with CKD: what is the evidence?. Clin J Am Soc Nephrol 2013; 8 (04) 665-674
- 54 Tanios BY, Itani HS, Zimmerman DL. Clopidogrel use in end-stage kidney disease. Semin Dial 2015; 28 (03) 276-281
- 55 Aradi D, Komócsi A, Vorobcsuk A. , et al. Prognostic significance of high on-clopidogrel platelet reactivity after percutaneous coronary intervention: systematic review and meta-analysis. Am Heart J 2010; 160 (03) 543-551
- 56 Polzin A, Dannenberg L, Sansone R. , et al. Antiplatelet effects of aspirin in chronic kidney disease patients. J Thromb Haemost 2016; 14 (02) 375-380
- 57 Shashar M, Belghasem ME, Matsuura S. , et al. Targeting STUB1-tissue factor axis normalizes hyperthrombotic uremic phenotype without increasing bleeding risk. Sci Transl Med 2017; 9 (417) eaam8475
- 58 Meijers BK, Evenepoel P. The gut-kidney axis: indoxyl sulfate, p-cresyl sulfate and CKD progression. Nephrol Dial Transplant 2011; 26 (03) 759-761
- 59 Yang K, Du C, Wang X. , et al. Indoxyl sulfate induces platelet hyperactivity and contributes to chronic kidney disease-associated thrombosis in mice. Blood 2017; 129 (19) 2667-2679
- 60 Yang K, Nie L, Huang Y. , et al. Amelioration of uremic toxin indoxyl sulfate-induced endothelial cell dysfunction by Klotho protein. Toxicol Lett 2012; 215 (02) 77-83
- 61 Kolachalama VB, Shashar M, Alousi F. , et al. Uremic solute-aryl hydrocarbon receptor-tissue factor axis associates with thrombosis after vascular injury in humans. J Am Soc Nephrol 2018; 29 (03) 1063-1072
- 62 Gondouin B, Cerini C, Dou L. , et al. Indolic uremic solutes increase tissue factor production in endothelial cells by the aryl hydrocarbon receptor pathway. Kidney Int 2013; 84 (04) 733-744
- 63 Holy EW, Tanner FC. Tissue factor in cardiovascular disease pathophysiology and pharmacological intervention. Adv Pharmacol 2010; 59: 259-292
- 64 Steffel J, Lüscher TF, Tanner FC. Tissue factor in cardiovascular diseases: molecular mechanisms and clinical implications. Circulation 2006; 113 (05) 722-731
- 65 Shimizu H, Hirose Y, Nishijima F, Tsubakihara Y, Miyazaki H. ROS and PDGF-beta [corrected] receptors are critically involved in indoxyl sulfate actions that promote vascular smooth muscle cell proliferation and migration. Am J Physiol Cell Physiol 2009; 297 (02) C389-C396
- 66 Pawlak K, Kowalewska A, Mysliwiec M, Pawlak D. Kynurenine and its metabolites--kynurenic acid and anthranilic acid are associated with soluble endothelial adhesion molecules and oxidative status in patients with chronic kidney disease. Am J Med Sci 2009; 338 (04) 293-300
- 67 Moffett JR, Namboodiri MA. Tryptophan and the immune response. Immunol Cell Biol 2003; 81 (04) 247-265
- 68 Niinisalo P, Raitala A, Pertovaara M. , et al. Indoleamine 2,3-dioxygenase activity associates with cardiovascular risk factors: the Health 2000 study. Scand J Clin Lab Invest 2008; 68 (08) 767-770
- 69 Ozkan Y, Sukuroglu MK, Tulmac M, Kisa U, Simsek B. Relation of kynurenine/tryptophan with immune and inflammatory markers in coronary artery disease. Clin Lab 2014; 60 (03) 391-396
- 70 Kato A, Suzuki Y, Suda T. , et al. Relationship between an increased serum kynurenine/tryptophan ratio and atherosclerotic parameters in hemodialysis patients. Hemodial Int 2010; 14 (04) 418-424
- 71 Schefold JC, Zeden JP, Fotopoulou C. , et al. Increased indoleamine 2,3-dioxygenase (IDO) activity and elevated serum levels of tryptophan catabolites in patients with chronic kidney disease: a possible link between chronic inflammation and uraemic symptoms. Nephrol Dial Transplant 2009; 24 (06) 1901-1908
- 72 Pawlak K, Domaniewski T, Mysliwiec M, Pawlak D. The kynurenines are associated with oxidative stress, inflammation and the prevalence of cardiovascular disease in patients with end-stage renal disease. Atherosclerosis 2009; 204 (01) 309-314
- 73 Eussen SJ, Ueland PM, Vollset SE. , et al. Kynurenines as predictors of acute coronary events in the Hordaland Health Study. Int J Cardiol 2015; 189: 18-24
- 74 Chen J, Ren J, Loo WTY, Hao L, Wang M. Lysyl oxidases expression and histopathological changes of the diabetic rat nephron. Mol Med Rep 2018; 17 (02) 2431-2441
- 75 Stangenberg S, Saad S, Schilter HC. , et al. Lysyl oxidase-like 2 inhibition ameliorates glomerulosclerosis and albuminuria in diabetic nephropathy. Sci Rep 2018; 8 (01) 9423-9432
- 76 Bhattacharyya S, Wei J, Varga J. Understanding fibrosis in systemic sclerosis: shifting paradigms, emerging opportunities. Nat Rev Rheumatol 2011; 8 (01) 42-54
- 77 Elhai M, Meune C, Boubaya M. , et al; EUSTAR group. Mapping and predicting mortality from systemic sclerosis. Ann Rheum Dis 2017; 76 (11) 1897-1905
- 78 Tyndall AJ, Bannert B, Vonk M. , et al. Causes and risk factors for death in systemic sclerosis: a study from the EULAR Scleroderma Trials and Research (EUSTAR) database. Ann Rheum Dis 2010; 69 (10) 1809-1815
- 79 Hesselvig JH, Kofoed K, Wu JJ, Dreyer L, Gislason G, Ahlehoff O. Localized scleroderma, systemic sclerosis and cardiovascular risk: A Danish Nationwide Cohort Study. Acta Derm Venereol 2018; 98 (03) 361-365
- 80 Łukasik ZM, Makowski M, Makowska JS. From blood coagulation to innate and adaptive immunity: the role of platelets in the physiology and pathology of autoimmune disorders. Rheumatol Int 2018; 38 (06) 959-974
- 81 Ramirez GA, Franchini S, Rovere-Querini P, Sabbadini MG, Manfredi AA, Maugeri N. The role of platelets in the pathogenesis of systemic sclerosis. Front Immunol 2012; 3: 160
- 82 Chiang TM, Takayama H, Postlethwaite AE. Increase in platelet non-integrin type I collagen receptor in patients with systemic sclerosis. Thromb Res 2006; 117 (03) 299-306
- 83 Chanoki M, Ishii M, Kobayashi H. , et al. Increased expression of lysyl oxidase in skin with scleroderma. Br J Dermatol 1995; 133 (05) 710-715
- 84 Rimar D, Rosner I, Nov Y. , et al. Brief report: lysyl oxidase is a potential biomarker of fibrosis in systemic sclerosis. Arthritis Rheumatol 2014; 66 (03) 726-730
- 85 Rimar D, Rosner I, Slobodin G. , et al. Lysyl oxidase in systemic sclerosis: getting under the skin. Isr Med Assoc J 2016; 18 (09) 534-536