Mechanisms of enhanced thrombus formation in cerebral microvessels of mice expressing hemoglobin-S

Blood

Volumn 117, Issue 15, 2011, Pages 4125-4133

  Gavins, Felicity N E ^a   Russell, Janice ^b   Senchenkova, Elena L ^b   De Almeida Paula, Lidiana ^b   Damazo, Amílcar S ^c   Esmon, Charles T ^d   Kirchhofer, Daniel ^e   Hebbel, Robert P ^f   Granger, D Neil ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c FEDERAL UNIVERSITY OF MATO GROSSO   (Brazil)

^d OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^e GENENTECH INC   (United States)

^f UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOGLOBIN S;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD VESSEL; CONTROLLED STUDY; MALE; MOUSE; NEUTROPENIA; NONHUMAN; OCCLUSIVE CEREBROVASCULAR DISEASE; PATHOGENESIS; PRIORITY JOURNAL; THROMBOCYTE AGGREGATION; THROMBOGENESIS;

EID: 79954620292     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-08-301366     Document Type: Article

References (56)

1. Wood K, Hebbel RP, Granger DN. Endothelial cell P-selectin mediated a proinflammatory and prothrombogenic phenotype in cerebral venules of sickle cell transgenic mice. Am J Physiol Heart Circ Physiol. 2004;286(5):H1608-1614. (Pubitemid 38525445)
2. Kaul DK, Hebbel RP. Hypoxia/reoxygenation causes inflammatory response in transgenic sickle mice but not in normal mice. J Clin Invest. 2000;106(3):411-420. (Pubitemid 30655641)
3. Ohene-Frempong K, Weiner SJ, Sleeper LA, et al. Cerebrovascular accidents in sickle cell disease: rates and risk factors. Blood. 1998;91(1):288-294. (Pubitemid 28018756)
4. Hebbel RP, Embury SH, Mohandas N, Steinberg MH. Sickle Cell Disease: Basic principles and clinical practice. Philadelphia, PA: Lippincott Williams & Wilkins; 1994.
5. Merkel KH, Ginsberg PL, Parker JC Jr, Post MJ. Cerebrovascular disease in sickle cell anemia: a clinical, pathological, and radiological correlation. Stroke. 1978;9(1):945-952.
6. Prengler M, Pavlakis SG, Prohovnik I, Adams RJ. Sickle Cell Disease: The neurological complications. Ann Neurol. 2002;51(5):543-552.
7. Solovey A, Kollander R, Shet A, Hebbel RP, et al. Endothelial cell expression of tissue factor in sickle mice is augmented by hypoxia/reoxygenation and inhibited by lovastatin. Blood. 2004;104(3):840-846. (Pubitemid 38970583)
8. Kurantsin-Mills J, Ofosu FA, Safa TK, Siegel RS, Lessin LS. Plasma factor VII and thrombinantithrombin III levels indicate increased tissue factor activity in sickle cell patients. Br J Haematol. 1992;81(4):539-544.
9. Westerman MP, Green D, Gilman-Sachs A, et al. Antiphospholipid antibodies, protein C and S, and coagulation changes in sickle cell disease. J Lab Clin Med. 1999;134(4):352-362. (Pubitemid 29490154)
10. Wright JG, Malia R, Cooper P, Thomas P, Preston FE, Serjeant GR. Protein C and S in homozygous sickle cell disease: does hepatic dysfunction contribute to low levels? Br J Haematol. 1997;98(3):627-631. (Pubitemid 27386543)
11. Ataga KI, Orringer EP. Hypercoagulability in sickle cell disease: a curious paradox. Am J Med. 2003;115(9):721-728. (Pubitemid 38032666)
12. Esmon CT. Crosstalk between inflammation and thrombosis. Maturitas. 2008;61(1-2):122-131.
13. Hebbel RP, Vercellotti GM, Pace BS, et al. The HDAC inhibitors trichostatin A and suberoylanilide hydroxamic acid exhibit multiple modalities of benefit for the vascular pathobiology of sickle transgenic mice. Blood. 2010;115(12):2483-2490.
14. Gavins F, Yilmaz G, Granger DN. The evolving paradigm for blood cell-endothelial cell interactions in the cerebral microcirculation. Microcirculation. 2007;14(7):667-681. (Pubitemid 47434284)
15. Kaul DK, Liu XD, Choong S, Belcher JD, Vercellotti GM, Hebbel RP. Anti-inflammatory therapy ameliorates leukocyte adhesion and microvascular flow abnormalities in transgenic sickle mice. Am J Physiol Heart Circ Physiol. 2004;287(1):H293-H301. (Pubitemid 38802365)
16. Solovey AA, Solovey AN, Harkness J, Hebbel RP. Modulation of endothelial cell activation in sickle cell disease: a pilot study. Blood. 2001;97(7):1937-1941. (Pubitemid 32239070)
17. Wood KC, Hebbel RP, Granger DN. Endothelial cell NADPH oxidase mediates the cerebral microvascular dysfunction in sickle cell transgenic mice. FASEB J. 2005;19(8):989-891.
18. Noguchi CT, Gladwin M, Diwan B, et al. Pathophysiology of a sickle cell trait mouse model: human alpha (beta) (S) transgenes with one mouse beta-globin allele. Blood Cells Mol Dis. 2001;27(6):971-977. (Pubitemid 34163965)
19. Belcher JD, Bryant CJ, Nguyen J, et al. Transgenic sickle mice have vascular inflammation. Blood. 2003;101(10):3953-3959. (Pubitemid 36857872)
20. Kollander R, Solovey A, Milbauer LC, Abdulla F, Kelm RJ Jr, Hebbel RP. Nuclear factor-kappa B (NFkappaB) component p50 in blood mononuclear cells regulates endothelial tissue factor expression in sickle transgenic mice: implications for the coagulopathy of sickle cell disease. Transl Res. 2010;155(4):170-177.
21. Li W, Zheng X, Gu J, et al. Overexpressing endothelial cell protein C receptor alters the hemostatic balance and protects mice from endotoxin. J Thromb Haemost. 2005;3(7):1351-1359. (Pubitemid 41725187)
22. Moser M, Nieswandt B, Ussar S, Pozgajova M, Fässler R. Kindlin-3 is essential for integrin activation and platelet aggregation. Nat Med. 2008;14(3):325-330. (Pubitemid 351347914)
23. Yoshida H, Russell J, Stokes KY, Yilmaz CE, Esmon CT, Granger DN. Role of the protein C pathway in the extraintestinal thrombosis associated with murine colitis. Gastroenterology. 2008;135(3):882-888.
24. Rumbaut RE, Bellera RV, Randhawa JK, et al. Endotoxin enhances microvascular thrombosis in mouse cremaster venules via a TLR4-dependent, neutrophil-independent mechanism. Am J Physiol Heart Circ Physiol. 2006;290(4):H1671-H1679.
25. Rumbaut RE, Slaff DW, Burns AR. Microvascular thrombosis models in venules and arterioles in vivo. Microcirculation. 2005;12(3):259-274. (Pubitemid 40691823)
26. Esmon CT. Inflammation and the activated protein C anticoagulant pathway. Semin Thromb Hemost. 2006;32(1):49-60.
27. Liaw PC, Ferrell G, Esmon CT. Amonoclonal antibody against activated protein C allows rapid detection of activated protein C in plasma and reveals a calcium ion dependent epitope involved in factor Va inactivation. J Thromb Haemost. 2003;1(4):662-670.
28. Kirchhofer D, Moran P, Bullens S, Peale F, Bunting S. A monoclonal antibody that inhibits mouse tissue factor function. J Thromb Haemost. 2005;3(5):1098-1099. (Pubitemid 41632848)
29. Senchenkova EY, Russell J, Almeida-Paula LD, Harding JW, Granger DN. Angiotensin II-mediated microvascular thrombosis. Hypertension. 2010;56(6):1089-1095.
30. Gavins FN, Kamal AM, D'Amico M, Oliani SM, Perretti M. Formyl-peptide receptor is not involved in the protection afforded by annexin 1 in murine acute myocardial infarct. FASEB J. 2005;19(1):100-102. (Pubitemid 40069931)
31. Han V, Serrano K, Devine DV. Acomparative study of common techniques used to measure haemolysis in stored red cell concentrates. Vox Sang. 2010;98(2):116-123.
32. Damazo AS, Yona S, Flower RJ, Perretti M, Oliani SM. Spatial and temporal profiles for antiinflammatory gene expression in leukocytes during a resolving model of peritonitis. J Immunol. 2006;176(7):4410-4418. (Pubitemid 44264421)
33. Povlishock JT, Rosenblum WI, Sholley MM, Wei EP. An ultrastructural analysis of endothelial change paralleling platelet aggregation in a light/dye model of microvascular insult. Am J Pathol. 1983;110(2):148-160. (Pubitemid 13147261)
34. Anyaegbu CC, Okpala IE, Akren'Ova YA, Salimonu LS. Peripheral blood neutrophil count and candidacidal activity correlate with the clinical severity of sickle cell anaemia (SCA). Eur J Haematol. 1998;60(4):267-268. (Pubitemid 28179411)
35. Luther T, Mackman N. Tissue factor in the heart. Multiple roles in hemostasis, thrombosis, and inflammation. Trends Cardiovasc Med. 2001;11(8):307-312. (Pubitemid 33116302)
36. Hebbel RP, Vercellotti GM. The endothelial biology of sickle cell disease. J Lab Clin Med. 1997;129(3):288-293. (Pubitemid 27169430)
37. Onyemelukwe GC, Jibril HB. Anti-thrombin III deficiency in Nigerian children with sickle cell disease: possible role in the cerebral syndrome. Trop Geogr Med. 1992;44(1-2):37-41.
38. Turhan A, Weiss LA, Mohandas N, Coller BS, Frenette PS. Primary role for adherent leukocytes in sickle cell vascular occlusion: a new paradigm. Proc Natl Acad Sci U S A. 2002;99(5):3047-3051. (Pubitemid 34240583)
39. Frenette PS, Atweh GF. Sickle cell disease: old discoveries, new concepts, and future promise. J Clin Invest. 2007;117(4):850-858. (Pubitemid 46556737)
40. Hillery CA, Panepinto JA. Pathophysiology of stroke in sickle cell disease. Microcirculation. 2004;11(2):195-208. (Pubitemid 39619079)
41. Chang Milbauer L, Wei P, Enenstein J, et al. Genetic endothelial systems biology of sickle stroke risk. Blood. 2008;111(7):3872-3879.
42. Shet AS, Hoffmann TJ, Jirouskova M, et al. Morphological and functional platelet abnormalities in Berkeley sickle cell mice. Blood Cells Mol Dis. 2008;41(1):109-118.
43. Furie B, Furie BC. Thrombus formation in vivo. J Clin Invest. 2005;115(12):3355-3362. (Pubitemid 43121819)
44. Proske S, Vollmar B, Menger MD. Microvascular consequences of thrombosis in small venules: an in vivo microscopic study using a novel model in the ear of the hairless mouse. Thromb Res. 2000;98(6):491-498. (Pubitemid 30433777)
45. Motto DG, Chauhan AK, Zhu G, et al. Shigatoxin triggers thrombotic thrombocytopenic purpura in genetically susceptible ADAMTS13-deficient mice. J Clin Invest. 2005;115(10):2752-2761. (Pubitemid 41434402)
46. Holtzclaw JD, Jack D, Aguayo SM, Eckman JR, Roman J, Hsu LL. Enhanced pulmonary and systemic response to endotoxin in transgenic sickle mice. Am J Respir Crit Care Med. 2004;169(4):687-695. (Pubitemid 38338920)
47. Shet AS, Aras O, Gupta K, et al. Sickle blood contains tissue factor-positive microparticles derived from endothelial cells and monocytes. Blood. 2003;102(7):2678-2683. (Pubitemid 37193612)
48. Scaldaferri F, Sans M, Vetrano S, et al. Crucial role of the protein C pathway in governing microvascular inflammation in inflammatory bowel disease. J Clin Invest. 2007;117(7):1951-1960. (Pubitemid 47036329)
49. Matsui NM, Varki A, Embury SH. Heparin inhibits the flow adhesion of sickle red blood cells to P-selectin. Blood. 2002;100(10):3790-3796. (Pubitemid 35303953)
50. Markwardt F. Hirudin as alternative anticoagulant-a historical review. Semin Thromb Hemost. 2002;28(5):405-414.
51. Sorg H, Hoffmann JN, Menger MD, Lindenblatt N, Goehring P, Vollmar B. Antithrombin is as effective as heparin and hirudin to prevent formation of microvascular thrombosis in a murine model. Thromb Haemost. 2006;96(3):371-377. (Pubitemid 44377823)
52. Wun T, Paglieroni T, Field CL, et al. Plateleterythrocyte adhesion in sickle cell disease. J Investig Med. 1999;47(3):121-127. (Pubitemid 129541445)
53. Broeders MA, Tangelder GJ, Slaaf DW, Reneman RS, oude Egbrink MG. Hypercholesterolemia enhances thromboembolism in arterioles but not venules: complete reversal by L-arginine. Arterioscler Thromb Vasc Biol. 2002;22(4):680-685. (Pubitemid 34408753)
54. Hidalgo A, Chang J, Jang JE, Peired AJ, Chiang EY, Frenette PS. Heterotypic interactions enabled by polarized neutrophil microdomains mediate thromboinflammatory injury. Nat Med. 2009;15(4):384-391.
55. Clark SR, Ma AC, Tavener SA, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. 2007;13(4):463-469. (Pubitemid 46559832)
56. Fuchs T. Neutrophil Extracellular Traps Induce Platelet Adhesion and Thrombus Formation. 51st ASH annual meeting and exposition. Abstract No. 1345.