Dendritic cell-mediated phagocytosis but not immune activation is enhanced by plasmin

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Borg, Rachael J ^a   Samson, Andre L ^a   Au, Amanda E L ^a   Scholzen, Anja ^a,c   Fuchsberger, Martina ^a   Kong, Ying Y ^a   Freeman, Roxann ^a   Mifsud, Nicole A ^a,b   Plebanski, Magdalena ^a   Medcalf, Robert L ^a  

^a MONASH UNIVERSITY   (Australia)

^b Alfred Medical Research and Education Precinct   (Australia)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

NANOPARTICLE; PLASMIN; TRANSFORMING GROWTH FACTOR BETA; HYBRID PROTEIN; IMMUNOCASP-6;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FUNCTION; CELL MATURATION; CELL MIGRATION; CELL TRANSPORT; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PROTEIN EXPRESSION; ADAPTIVE IMMUNITY; ANIMAL; C57BL MOUSE; CELL CULTURE; FLOW CYTOMETRY; INNATE IMMUNITY; LYMPHOCYTE ACTIVATION; PHYSIOLOGY;

ADAPTIVE IMMUNITY; ANIMALS; CELLS, CULTURED; DENDRITIC CELLS; FIBRINOLYSIN; FLOW CYTOMETRY; HUMANS; IMMUNITY, INNATE; LYMPHOCYTE ACTIVATION; MALE; MICE, INBRED C57BL; PHAGOCYTOSIS; RECOMBINANT FUSION PROTEINS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84940497021     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0131216     Document Type: Article

References (45)

1. Zitvogel L, Kepp O, Kroemer G. Decoding cell death signals in inflammation and immunity. Cell 2010; 140: 798-804. doi: 10.1016/j.cell.2010.02.015 PMID: 20303871
2. Poon IK, Hulett MD, Parish CR. Molecular mechanisms of late apoptotic/necrotic cell clearance. Cell Death Differ. 2010; 17: 381-397. doi: 10.1038/cdd.2009.195 PMID: 20019744
3. Gaipl US, Munoz LE, Grossmayer G, Lauber K, Franz S, Sarter K et al. Clearance deficiency and systemic lupus erythematosus (SLE). J Autoimmun. 2007; 28: 114-121. doi: 10.1016/j.jaut.2007.02.005 PMID: 17368845
4. Vandivier RW, Fadok VA, Hoffmann PR, Bratton DL, Penvari C, Brown KK et al. Elastase-mediated phosphatidylserine receptor cleavage impairs apoptotic cell clearance in cystic fibrosis and bronchiectasis. J Clin Invest. 2002; 109: 661-670. doi: 10.1172/JCI13572 PMID: 11877474
5. Li S, Sun Y, Liang CP, Thorp EB, Han S, Jehle AW et al. Defective phagocytosis of apoptotic cells by macrophages in atherosclerotic lesions of ob/ob mice and reversal by a fish oil diet. Circ Res 2009; 105: 1072-1082. doi: 10.1161/CIRCRESAHA.109.199570 PMID: 19834009
6. Silva MT. Bacteria-induced phagocyte secondary necrosis as a pathogenicity mechanism. J Leukoc Biol 2010; 88: 885-896. doi: 10.1189/jlb.0410205 PMID: 20566623
7. Samson AL, Knaupp AS, Sashindranath M, Borg RJ, Au AE, Cops EJ et al. Nucleocytoplasmic Coagulation: An Injury-Induced Aggregation Event that Disulfide Crosslinks Proteins and Facilitates Their Removal by Plasmin. Cell Rep. 2012; 2: 889-901. doi: 10.1016/j.celrep.2012.08.026 PMID: 23041318
8. Samson AL, Borg RJ, Niego B, Wong CH, Crack PJ, Yongqing T et al. A nonfibrin macromolecular cofactor for tPA-mediated plasmin generation following cellular injury. Blood 2009; 114: 1937-1946. doi: 10.1182/blood-2009-02-203448 PMID: 19584397
9. Napirei M, Karsunky H, Zevnik B, Stephan H, Mannherz HG,Moroy T. Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat Genet, 2000; 25: 177-181. doi: 10.1038/76032 PMID: 10835632
10. Ramirez-Ortiz ZG, Pendergraft WF 3rd, Prasad A, Byrne MH, Iram T, Blanchette CJ et al. The scavenger receptor SCARF1 mediates the clearance of apoptotic cells and prevents autoimmunity. Nat Immunol. 2013; 14: 917-926. doi: 10.1038/ni.2670 PMID: 23892722
11. Li Q, Laumonnier Y, Syrovets T, Simmet T. Plasmin triggers cytokine induction in human monocytederived macrophages. Arterioscler Thromb Vasc Biol. 2007; 27: 1383-1389. doi: 10.1161/ATVBAHA.107.142901 PMID: 17413040
12. Lathem WW, Price PA, Miller VL, Goldman WE. A plasminogen-activating protease specifically controls the development of primary pneumonic plague. Science 2007; 315: 509-513. doi: 10.1126/science.1137195 PMID: 17255510
13. Guo Y, Li J, Hagstrom E, Ny T. Beneficial and detrimental effects of plasmin(ogen) during infection and sepsis in mice. PLoS One 2011; 6: e24774. doi: 10.1371/journal.pone.0024774 PMID: 21931850
14. Guo Y, Li J, Hagstrom E, Ny T. Protective effects of plasmin(ogen) in a mouse model of Staphylococcus aureus-induced arthritis. Arthritis Rheum. 2008; 58: 764-772. doi: 10.1002/art.23263 PMID: 18311818
15. Shen Y, Guo Y, Mikus P, Sulniute R, Wilczynska M, Ny T et al. Plasminogen is a key proinflammatory regulator that accelerates the healing of acute and diabetic wounds. Blood 2012; 119: 5879-5887. doi: 10.1182/blood-2012-01-407825 PMID: 22563086
16. Rosenwald M, Koppe U, Keppeler H, Sauer G, Hennel R, Ernst A et al. Serum-derived plasminogen is activated by apoptotic cells and promotes their phagocytic clearance. J Immunol. 2012; 189: 5722-5728. doi: 10.4049/jimmunol.1200922 PMID: 23150713
17. Karlson Tde L, Kong YY, Hardy CL, Xiang SD, Plebanski M. The signalling imprints of nanoparticle uptake by bone marrow derived dendritic cells. Methods 2013; 60: 275-283. doi: 10.1016/j.ymeth.2013.02.009 PMID: 23459257
18. Sashindranath M, Samson AL, Downes CE, Crack PJ, Lawrence AJ, Li QX et al. Compartment- and context-specific changes in tissue-type plasminogen activator (tPA) activity following brain injury and pharmacological stimulation. Lab Invest. 2011; 91: 1079-1091. doi: 10.1038/labinvest.2011.67 10.1038/labinvest.2011.67 PMID: 21519332
19. Au AE, Sashindranath M, Borg RJ, Kleifeld O, Andrews RK, Gardiner EE et al. Activated platelets rescue apoptotic cells via paracrine activation of EGFR and DNA-dependent protein kinase. Cell Death Dis. 2014 5: e1410. doi: 10.1038/cddis.2014.373 PMID: 25210793
20. Schaefer CF, Anthony K, Krupa S, Buchoff J, Day M, Hannay T et al. PID: the Pathway Interaction Database. Nucleic Acids Res. 2009; 37: D674-679. doi: 10.1093/nar/gkn653 PMID: 18832364
21. Mottram PL, Leong D, Crimeen-Irwin B, Gloster S, Xiang SD, Meanger J et al. Type 1 and 2 immunity following vaccination is influenced by nanoparticle size: formulation of a model vaccine for respiratory syncytial virus. Mol Pharm. 2007; 4: 73-84. doi: 10.1021/mp060096p PMID: 17274665
22. Xiang SD, Scalzo-Inguanti K, Minigo G, Park A, Hardy CL, Plebanski M. Promising particle-based vaccines in cancer therapy. Expert Rev Vaccines 2008; 7: 1103-1119. doi: 10.1586/14760584.7.7.1103 PMID: 18767957
23. Xiang SD, Scholzen A, Minigo G, David C, Apostolopoulos V, Mottram PL et al. Pathogen recognition and development of particulate vaccines: does size matter? Methods 2006; 40: 1-9. doi: 10.1016/j. ymeth.2006.05.016 PMID: 16997708
24. Niego B, Freeman R, Puschmann TB, Turnley AM, Medcalf RL. t-PA-specific modulation of a human blood-brain barrier model involves plasmin-mediated activation of the Rho kinase pathway in astrocytes. Blood 2012; 119: 4752-4761. doi: 10.1182/blood-2011-07-369512 PMID: 22262761
25. Ho-Tin-Noe B, Enslen H, Doeuvre L, Corsi JM, Lijnen HR, Angles-Cano, E. Role of plasminogen activation in neuronal organization and survival. Mol Cell Neurosci. 2009; 42: 288-295. doi: 10.1016/j.mcn.2009.08.001 PMID: 19683575
26. Li X, Syrovets T, Genze F, Pitterle K, Oberhuber A, Orend KH et al. Plasmin triggers chemotaxis of monocyte-derived dendritic cells through an Akt2-dependent pathway and promotes a T-helper type-1 response. Arterioscler Thromb Vasc Biol. 2010; 30: 582-590. doi: 10.1161/ATVBAHA.109.202044 PMID: 20056908
27. Lyons RM, Keski-Oja J, Moses HL. Proteolytic activation of latent transforming growth factor-beta from fibroblast-conditioned medium. J Cell Biol. 1988; 106: 1659-1665. PMID: 2967299
28. Lee WC, Zhong C, Qian S, Wan Y, Gauldie J, Mi Z et al. Phenotype, function, and in vivo migration and survival of allogeneic dendritic cell progenitors genetically engineered to express TGF-beta. Transplantation 1998; 66: 1810-1817. PMID: 9884280
29. Kao JY, Gong Y, Chen CM, Zheng QD, Chen JJ. Tumor-derived TGF-beta reduces the efficacy of dendritic cell/tumor fusion vaccine. J Immunol. 2003; 170: 3806-3811. doi: 10.4049/jimmunol.170.7.3806 PMID: 12646647
30. Lighvani S, Baik N, Diggs JE, Khaldoyanidi S, Parmer RJ, Miles LA. Regulation of macrophage migration by a novel plasminogen receptor Plg-R KT. Blood 2011; 118: 5622-5630. doi: 10.1182/blood- 2011-03-344242 PMID: 21940822
31. Das R, Ganapathy S, Settle M, Plow EF. Plasminogen promotes macrophage phagocytosis in mice. Blood 2014; 124: 679-688. doi: 10.1182/blood-2014-01-549659 PMID: 24876560
32. Haka AS, Grosheva I, Singh RK, Maxfield FR. Plasmin promotes foam cell formation by increasing macrophage catabolism of aggregated low-density lipoprotein. Arterioscler Thromb Vasc Biol. 2013; 33: 1768-1778. doi: 10.1161/ATVBAHA.112.301109 PMID: 23702659
33. Cederholm-Williams SA. Concentration of plasminogen and antiplasmin in plasma and serum. J Clin Pathol. 1981; 34: 979-981. PMID: 7276224
34. Napirei M, Wulf S, Mannherz HG. Chromatin breakdown during necrosis by serum Dnase1 and the plasminogen system. Arthritis Rheum. 2004; 50: 1873-1883. doi: 10.1002/art.20267 PMID: 15188364
35. Suzuki J, Ogawa M, Muto S, Itai A, Isobe M. A specific inhibitor of plasminogen activator inhibitor-1 suppresses rat autoimmune myocarditis. Expert Opin Ther Targets 2008; 12: 1313-1320. doi: 10.1517/14728222.12.11.1313 PMID: 18851689
36. Kabakov AE, Gabai VL. Stress-induced insolubilization of certain proteins in ascites tumor cells. Arch Biochem Biophys. 1994; 309: 247-253. doi: 10.1006/abbi.1994.1109 PMID: 8135534
37. Machovich R, Ajtai K, Kolev K, Owen WG. Myosin as cofactor and substrate in fibrinolysis. FEBS Lett. 1997; 407: 93-96. http://dx.doi.org/10.1016/S0014-5793(97)00303-7 PMID: 9141488
38. Samson AL, Nevin ST, Croucher D, Niego B, Daniel PB, Weiss TW et al. Tissue-type plasminogen activator requires a co-receptor to enhance NMDA receptor function. J Neurochem. 2008; 107: 1091-1101. doi: 10.1111/j.1471-4159.2008.05687.x PMID: 18796005
39. Li Q, Ke F, Zhang W, Laumonnier Y, Syrovets T, Simmet T et al. A role for the annexin A2 amino-terminal peptide in the plasmin-induced activation of human peripheral monocytes. Mol Immunol. 2010; 47: 2405-2410. doi: 10.1016/j.molimm.2010.03.015 PMID: 20627396
40. Matsumoto T, Yokote K, Tamura K, Takemoto M, Ueno H, Saito Y et al. Platelet-derived growth factor activates p38 mitogen-activated protein kinase through a Ras-dependent pathway that is important for actin reorganization and cell migration. J Biol Chem. 1999; 274: 13954-13960. doi: 10.1074/jbc.274.20.13954 PMID: 10318806
41. Wilson E, Laster SM, Gooding LR, Lambeth JD. Platelet-derived growth factor stimulates phagocytosis and blocks agonist-induced activation of the neutrophil oxidative burst: a possible cellular mechanism to protect against oxygen radical damage. Proc Natl Acad Sci U S A. 1987; 84: 2213-2217. PMID:3031672
42. Tamura M, Iwamoto Y. The effect of platelet-derived growth factor on phagocytosis of cultured human trabecular cells. Exp Eye Res. 1989; 48: 761-770. PMID: 2731573
43. Appel S, Rupf A, Weck MM, Schoor O, Brummendorf TH, Weinschenk T et al. Effects of imatinib on monocyte-derived dendritic cells are mediated by inhibition of nuclear factor-kappaB and Akt signaling pathways. Clin Cancer Res. 2005; 11: 1928-1940. doi: 10.1158/1078-0432.CCR-04-1713 PMID: 15756019
44. Becker JC, Andersen MH, Schrama D, Thor Straten P. Immune-suppressive properties of the tumor microenvironment. Cancer Immunol Immunother. 2013; 62: 1137-1148. doi: 10.1007/s00262-013- 1434-6 PMID: 23666510
45. Burtin P, Chavanel G, Andre J. The plasmin system in human colonic tumors: an immunofluorescence study. Int J Cancer 1985; 35: 307-314. PMID: 2579035.