Pharmacological targeting of plasmin prevents lethality in a murine model of macrophage activation syndrome

Blood

Volumn 130, Issue 1, 2017, Pages 59-72

  Shimazu, Hiroshi ^a,b   Munakata, Shinya ^a   Tashiro, Yoshihiko ^a   Salama, Yousef ^b   Dhahri, Douaa ^b   Eiamboonsert, Salita ^b   Ota, Yasunori ^a   Onoda, Haruo ^a   Tsuda, Yuko ^c   Okada, Yoshio ^c   Nakauchi, Hiromitsu ^a   Heissig, Beate ^a,b,d   Hattori, Koichi ^a,d  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^c KOBE GAKUIN UNIVERSITY   (Japan)

^d JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; CPG OLIGODEOXYNUCLEOTIDE 1826; GALACTOSAMINE; GAMMA INTERFERON; INTERLEUKIN 1; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; PLASMIN; PLASMIN INHIBITOR; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR AGONIST; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; YO 2; TLR9 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; INFLAMMATORY CELL; LETHALITY; LIVER CELL; MACROPHAGE ACTIVATION SYNDROME; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEPTIC SHOCK; AGONISTS; ANIMAL; DISEASE MODEL; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; RAW 264.7 CELL LINE;

ANIMALS; DISEASE MODELS, ANIMAL; FIBRINOLYSIN; GALACTOSAMINE; HUMANS; MACROPHAGE ACTIVATION SYNDROME; MICE; MICE, KNOCKOUT; RAW 264.7 CELLS; TOLL-LIKE RECEPTOR 9;

EID: 85024112507     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-09-738096     Document Type: Article

References (63)

1. Janka GE. Familial and acquired hemophagocytic lymphohistiocytosis. Eur J Pediatr. 2007;166(2): 95-109.
2. Janka GE, Lehmberg K. Hemophagocytic syndromes–an update. Blood Rev. 2014;28(4): 135-142.
3. Sato A, Nishida C, Sato-Kusubata K, et al. Inhibition of plasmin attenuates murine acute graft-versus-host disease mortality by suppressing the matrix metalloproteinase-9dependent inflammatory cytokine storm and effector cell trafficking. Leukemia. 2015;29(1): 145-156.
4. Munakata S, Tashiro Y, Nishida C, et al. Inhibition of plasmin protects against colitis in mice by suppressing matrix metalloproteinase 9-mediated cytokine release from myeloid cells. Gastroenterology. 2015;148(3):565-578.e4.
5. Loscalzo J. The macrophage and fibrinolysis. Semin Thromb Hemost. 1996;22(6):503-506.
6. Rao CN, Mohanam S, Puppala A, Rao JS. Regulation of ProMMP-1 and ProMMP-3 activation by tissue factor pathway inhibitor-2/ matrix-associated serine protease inhibitor. Biochem Biophys Res Commun. 1999;255(1): 94-98.
7. Knäuper V, Will H, López-Otin C, et al. Cellular mechanisms for human procollagenase-3 (MMP-13) activation. Evidence that MT1-MMP (MMP-14) and gelatinase a (MMP-2) are able to generate active enzyme. J Biol Chem. 1996; 271(29):17124-17131.
8. Ramos-DeSimone N, Hahn-Dantona E, Sipley J, Nagase H, French DL, Quigley JP. Activation of matrix metalloproteinase-9 (MMP-9) via a converging plasmin/stromelysin-1 cascade enhances tumor cell invasion. J Biol Chem. 1999; 274(19):13066-13076.
9. Janka GE. Hemophagocytic syndromes. Blood Rev. 2007;21(5):245-253.
10. Hasegawa D, Kojima S, Tatsumi E, et al. Elevation of the serum Fas ligand in patients with hemophagocytic syndrome and Diamond-Blackfan anemia. Blood. 1998;91(8):2793-2799.
11. Henter JI, Elinder G, Söder O, Hansson M, Andersson B, Andersson U. Hypercytokinemia in familial hemophagocytic lymphohistiocytosis. Blood. 1991;78(11):2918-2922.
12. Cauwe B, Opdenakker G. Intracellular substrate cleavage: a novel dimension in the biochemistry, biology and pathology of matrix metalloproteinases. Crit Rev Biochem Mol Biol. 2010;45(5):351-423.
13. Syrovets T, Jendrach M, Rohwedder A, Schüle A, Simmet T. Plasmin-induced expression of cytokines and tissue factor in human monocytes involves AP-1 and IKKbeta-mediated NF-kappaB activation. Blood. 2001;97(12):3941-3950.
14. Li Q, Verma IM. NF-kappaB regulation in the immune system. Nat Rev Immunol. 2002;2(10): 725-734.
15. Collen D. Ham-Wasserman lecture: role of the plasminogen system in fibrin-homeostasis and tissue remodeling. Hematology Am Soc Hematol Educ Program. 2001;2001:1-9.
16. Burysek L, Syrovets T, Simmet T. The serine protease plasmin triggers expression of MCP-1 and CD40 in human primary monocytes via activation of p38 MAPK and janus kinase (JAK)/ STAT signaling pathways. J Biol Chem. 2002; 277(36):33509-33517.
17. Ohki M, Ohki Y, Ishihara M, et al. Tissue type plasminogen activator regulates myeloid-cell dependent neoangiogenesis during tissue regeneration. Blood. 2010;115(21):4302-4312.
18. Tashiro Y, Nishida C, Sato-Kusubata K, et al. Inhibition of PAI-1 induces neutrophil-driven neoangiogenesis and promotes tissue regeneration via production of angiocrine factors in mice. Blood. 2012;119(26):6382-6393.
19. Gong Y, Hart E, Shchurin A, Hoover-Plow J. Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. J Clin Invest. 2008;118(9):3012-3024.
20. Carmo AA, Costa BR, Vago JP, et al. Plasmin induces in vivo monocyte recruitment through protease-activated receptor-1-, MEK/ERK-, and CCR2-mediated signaling. J Immunol. 2014; 193(7):3654-3663.
21. Strippoli R, Carvello F, Scianaro R, et al. Amplification of the response to Toll-like receptor ligands by prolonged exposure to interleukin-6 in mice: implication for the pathogenesis of macrophage activation syndrome. Arthritis Rheum. 2012;64(5):1680-1688.
22. Prahalad S, Bove KE, Dickens D, Lovell DJ, Grom AA. Etanercept in the treatment of macrophage activation syndrome. J Rheumatol. 2001;28(9): 2120-2124.
23. Bruck N, Suttorp M, Kabus M, Heubner G, Gahr M, Pessler F. Rapid and sustained remission of systemic juvenile idiopathic arthritis-associated macrophage activation syndrome through treatment with anakinra and corticosteroids. J Clin Rheumatol. 2011;17(1):23-27.
24. Sandhu C, Chesney A, Piliotis E, Buckstein R, Koren S. Macrophage activation syndrome after etanercept treatment. J Rheumatol. 2007;34(1): 241-242.
25. Henzan T, Nagafuji K, Tsukamoto H, et al. Success with infliximab in treating refractory hemophagocytic lymphohistiocytosis. Am J Hematol. 2006;81(1):59-61.
26. Makay B, Yilmaz S, Türkyilmaz Z, Unal N, Oren H, Unsal E. Etanercept for therapy-resistant macrophage activation syndrome. Pediatr Blood Cancer. 2008;50(2):419-421.
27. Liu J, Guo YM, Onai N, et al. Cytosine-phosphorothionate-guanine oligodeoxynucleotides exacerbates hemophagocytosis by inducing tumor necrosis factor-alpha production in mice after bone marrow transplantation. Biol Blood Marrow Transplant. 2016;22(4):627-636.
28. Ramanan AV, Schneider R. Macrophage activation syndrome following initiation of etanercept in a child with systemic onset juvenile rheumatoid arthritis. J Rheumatol. 2003;30(2): 401-403.
29. Fitzgerald AA, Leclercq SA, Yan A, Homik JE, Dinarello CA. Rapid responses to anakinra in patients with refractory adult-onset Still’s disease. Arthritis Rheum. 2005;52(6):1794-1803.
30. Miettunen PM, Narendran A, Jayanthan A, Behrens EM, Cron RQ. Successful treatment of severe paediatric rheumatic disease-associated macrophage activation syndrome with interleukin-1 inhibition following conventional immunosuppressive therapy: case series with 12 patients. Rheumatology (Oxford). 2011;50(2): 417-419.
31. Nigrovic PA, Mannion M, Prince FH, et al. Anakinra as first-line disease-modifying therapy in systemic juvenile idiopathic arthritis: report of forty-six patients from an international multicenter series. Arthritis Rheum. 2011;63(2):545-555.
32. Behrens EM, Canna SW, Slade K, et al. Repeated TLR9 stimulation results in macrophage activation syndrome-like disease in mice. J Clin Invest. 2011;121(6):2264-2277.
33. Yi AK, Yoon H, Park JE, Kim BS, Kim HJ, Martinez-Hernandez A. CpG DNA-mediated induction of acute liver injury in D-galactosamine-sensitized mice: the mitochondrial apoptotic pathway-dependent death of hepatocytes. J Biol Chem. 2006;281(21):15001-15012.
34. Maes M, Vinken M, Jaeschke H. Experimental models of hepatotoxicity related to acute liver failure. Toxicol Appl Pharmacol. 2016;290:86-97.
35. Heissig B, Hattori K, Dias S, et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell. 2002;109(5):625-637.
36. Lee E, Enomoto R, Takemura K, Tsuda Y, Okada Y. A selective plasmin inhibitor, trans-aminomethylcyclohexanecarbonyl-L-(O-picolyl) tyrosine-octylamide (YO-2), induces thymocyte apoptosis. Biochem Pharmacol. 2002;63(7): 1315-1323.
37. Bugge TH, Flick MJ, Daugherty CC, Degen JL. Plasminogen deficiency causes severe thrombosis but is compatible with development and reproduction. Genes Dev. 1995;9(7):794-807.
38. Hald A, Rønø B, Melander MC, Ding M, Holck S, Lund LR. MMP9 is protective against lethal inflammatory mass lesions in the mouse colon. Dis Model Mech. 2011;4(2):212-227.
39. Dhahri D, Sato-Kusubata K, Ohki-Koizumi M, et al. Fibrinolytic crosstalk with endothelial cells expands murine mesenchymal stromal cells. Blood. 2016;128(8):1063-1075.
40. Li Q, Laumonnier Y, Syrovets T, Simmet T. Plasmin triggers cytokine induction in human monocyte-derived macrophages. Arterioscler Thromb Vasc Biol. 2007;27(6):1383-1389.
41. de Jager W, Hoppenreijs EP, Wulffraat NM, Wedderburn LR, Kuis W, Prakken BJ. Blood and synovial fluid cytokine signatures in patients with juvenile idiopathic arthritis: a cross-sectional study. Ann Rheum Dis. 2007;66(5):589-598.
42. Sheehan JJ, Zhou C, Gravanis I, et al. Proteolytic activation of monocyte chemoattractant protein-1 by plasmin underlies excitotoxic neurodegeneration in mice. J Neurosci. 2007; 27(7):1738-1745.
43. Roelofs JJ, Rouschop KM, Leemans JC, et al. Tissue-type plasminogen activator modulates inflammatory responses and renal function in ischemia reperfusion injury. J Am Soc Nephrol. 2006;17(1):131-140.
44. Takeshita F, Gursel I, Ishii KJ, Suzuki K, Gursel M, Klinman DM. Signal transduction pathways mediated by the interaction of CpG DNA with Toll-like receptor 9. Semin Immunol. 2004;16(1): 17-22.
45. Ward JR, Dower SK, Whyte MK, Buttle DJ, Sabroe I. Potentiation of TLR4 signalling by plasmin activity. Biochem Biophys Res Commun. 2006;341(2):299-303.
46. Gum R, Lengyel E, Juarez J, et al. Stimulation of 92-kDa gelatinase B promoter activity by ras is mitogen-activated protein kinase kinase 1-independent and requires multiple transcription factor binding sites including closely spaced PEA3/ets and AP-1 sequences. J Biol Chem. 1996;271(18):10672-10680.
47. Ohyagi H, Onai N, Sato T, et al. Monocyte-derived dendritic cells perform hemophagocytosis to fine-tune excessive immune responses. Immunity. 2013;39(3):584-598.
48. Koj A, Dubin A. The effect of D-galactosamine on plasma protein synthesis by the perfused rat liver from turpentine-stimulated donors. Br J Exp Pathol. 1978;59(5):504-513.
49. Bajou K, Peng H, Laug WE, et al. Plasminogen activator inhibitor-1 protects endothelial cells from FasL-mediated apoptosis. Cancer Cell. 2008; 14(4):324-334.
50. Bezerra JA, Bugge TH, Melin-Aldana H, et al. Plasminogen deficiency leads to impaired remodeling after a toxic injury to the liver. Proc Natl Acad Sci USA. 1999;96(26):15143-15148.
51. Bugge TH, Kombrinck KW, Flick MJ, Daugherty CC, Danton MJ, Degen JL. Loss of fibrinogen rescues mice from the pleiotropic effects of plasminogen deficiency. Cell. 1996;87(4): 709-719.
52. Wang Y, Dang J, Wang H, Allgayer H, Murrell GA, Boyd D. Identification of a novel nuclear factor-kappaB sequence involved in expression of urokinase-type plasminogen activator receptor. Eur J Biochem. 2000;267(11):3248-3254.
53. Lim EJ, Lee SH, Lee JG, et al. Toll-like receptor 9 dependent activation of MAPK and NF-kB is required for the CpG ODN-induced matrix metalloproteinase-9 expression. Exp Mol Med. 2007;39(2):239-245.
54. Gearing AJ, Beckett P, Christodoulou M, et al. Processing of tumour necrosis factor-alpha precursor by metalloproteinases. Nature. 1994; 370(6490):555-557.
55. Hattori K, Hirano T, Ushiyama C, et al. A metalloproteinase inhibitor prevents lethal acute graft-versus-host disease in mice. Blood. 1997; 90(2):542-548.
56. McGeehan GM, Becherer JD, Bast RC Jr, et al. Regulation of tumour necrosis factor-alpha processing by a metalloproteinase inhibitor. Nature. 1994;370(6490):558-561.
57. Boring L, Gosling J, Chensue SW, et al. Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J Clin Invest. 1997;100(10): 2552-2561.
58. Serbina NV, Pamer EG. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol. 2006;7(3):311-317.
59. Testa U. Apoptotic mechanisms in the control of erythropoiesis. Leukemia. 2004;18(7):1176-1199.
60. Jordan MB, Hildeman D, Kappler J, Marrack P. An animal model of hemophagocytic lymphohistiocytosis (HLH): CD81 T cells and interferon gamma are essential for the disorder. Blood. 2004;104(3):735-743.
61. Zoller EE, Lykens JE, Terrell CE, et al. Hemophagocytosis causes a consumptive anemia of inflammation. J Exp Med. 2011;208(6): 1203-1214.
62. Pachlopnik Schmid J, Ho CH, Chrétien F, et al. Neutralization of IFNgamma defeats haemophagocytosis in LCMV-infected perforin- and Rab27a-deficient mice. EMBO Mol Med. 2009;1(2):112-124.
63. Sitrin RG, Todd RF III, Mizukami IF, Gross TJ, Shollenberger SB, Gyetko MR. Cytokine-specific regulation of urokinase receptor (CD87) expression by U937 mononuclear phagocytes. Blood. 1994;84(4):1268-1275.