Antimicrobial effects of helix D-derived peptides of human Antithrombin III

Journal of Biological Chemistry

Volumn 289, Issue 43, 2014, Pages 29790-29800

  Papareddy, Praveen ^a   Kalle, Martina ^a   Bhongir, Ravi K V ^a   Mörgelin, Matthias ^a   Malmsten, Martin ^b   Schmidtchen, Artur ^a,c  

^a LUND UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; LIPOSOMES; POLYSACCHARIDES;

ANTI-MICROBIAL ACTIVITY; ANTI-MICROBIAL EFFECTS; ANTIBACTERIAL EFFECTS; BACTERIAL MEMBRANES; GRAM-NEGATIVE BACTERIA; PEPTIDE FRAGMENTS; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS;

PEPTIDES;

ALANYLLYSYLLEUCYLASPARAGINYLCYSTEINYLARGINYLLEUCYLTYROSYLARGINYLLYSYLALANYLASPARAGINYLLYSYLSERYLSERYLLYSYLLEUCYLVALYLSERYLALANYLASPARAGINYLARGININE; ANTIINFECTIVE AGENT; ANTITHROMBIN III; PHENYLALANYLPHENYLALANYLPHENYLALANYLALANYLLYSYLLEUCYLASPARAGINYLCYSTEINYLARGINYLLEUCYLTYROSYLARGINYLLYSYLALANYLASPARAGINYLLYSYLSERYLSERYLLYSYLLEUCYLVALINE; UNCLASSIFIED DRUG; HEPARIN COFACTOR II; LIPOPOLYSACCHARIDE; LIPOSOME; PANCREATIC ELASTASE; PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL MEMBRANE; BLOOD CLOTTING; CONTROLLED STUDY; DRUG MECHANISM; DRUG RESPONSE; ELECTRON MICROSCOPY; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; HOST RESISTANCE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MALE; MEMBRANE PERMEABILITY; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; CELL MEMBRANE PERMEABILITY; CHEMISTRY; CIRCULAR DICHROISM; DISEASE MODEL; DRUG EFFECTS; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MOLECULAR GENETICS; PATHOLOGY; PROTEIN SECONDARY STRUCTURE; STAPHYLOCOCCUS AUREUS; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; ANTI-INFECTIVE AGENTS; ANTITHROMBIN III; CELL MEMBRANE PERMEABILITY; CIRCULAR DICHROISM; DISEASE MODELS, ANIMAL; HEPARIN COFACTOR II; HUMANS; LIPOPOLYSACCHARIDES; LIPOSOMES; MICE, INBRED C57BL; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; PANCREATIC ELASTASE; PEPTIDES; PROTEIN STRUCTURE, SECONDARY; PROTEOLYSIS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84908408991     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.570465     Document Type: Article

References (51)

1. Fourrier, F. (1998) Therapeutic applications of antithrombin concentrates in systemic inflammatory disorders. Blood Coagul. Fibrinolysis 9, S39-S45
2. Fourrier, F., Chopin, C., Goudemand, J., Hendrycx, S., Caron, C., Rime, A., Marey, A., and Lestavel, P. (1992) Septic shock, multiple organ failure, and disseminated intravascular coagulation: compared patterns of antithrombin III, protein C, and protein S deficiencies. Chest 101, 816-823
3. Ostermann, H. (2002) Antithrombin III in Sepsis: new evidences and open questions. Minerva Anestesiol. 68, 445-448
4. Smith, J. W., and Knauer, D. J. (1987) A heparin binding site in antithrombin III: identification, purification, and amino acid sequence. J. Biol. Chem. 262, 11964-11972
5. Liu, C. S., and Chang, J. Y. (1987) Probing the heparin-binding domain of human antithrombin III with V8 protease. Eur. J. Biochem. 167, 247-252
6. Oehlschläger, S., Albrecht, S., Hakenberg, O. W., Manseck, A., Froehner, M., Zimmermann, T., and Wirth, M. P. (2002) Measurement of free radicals and NO by chemiluminescence to identify the reperfusion injury in renal transplantation. Luminescence 17, 130-132
7. Hoffmann, J. N., Vollmar, B., Inthorn, D., Schildberg, F. W., and Menger, M. D. (2000) The thrombin antagonist hirudin fails to inhibit endotoxin-induced leukocyte/endothelial cell interaction and microvascular perfusion failure. Shock 14, 528-534
8. Kurose, I., Miura, S., Fukumura, D., Suzuki, M., Nagata, H., Sekizuka, E., Morishita, T., and Tsuchiya, M. (1994) Attenuating effect of antithrombin III on the fibrinolytic activation and microvascular derangement in rat gastric mucosa. Thromb. Haemost. 71, 119-123
9. Roemisch, J., Gray, E., Hoffmann, J. N., and Wiedermann, C. J. (2002) Antithrombin: a new look at the actions of a serine protease inhibitor. Blood Coagul. Fibrinolysis 13, 657-670
10. Opal, S. M. (2003) Interactions between coagulation and inflammation. Scand. J. Infect Dis. 35, 545-554
11. Souter, P. J., Thomas, S., Hubbard, A. R., Poole, S., Römisch, J., and Gray, E. (2001) Antithrombin inhibits lipopolysaccharide-induced tissue factor and interleukin-6 production by mononuclear cells, human umbilical vein endothelial cells, and whole blood. Crit. Care Med. 29, 134-139
12. Dunzendorfer, S., Kaneider, N., Rabensteiner, A., Meierhofer, C., Reinisch, C., Römisch, J., and Wiedermann, C. J. (2001) Cell-surface heparan sulfate proteoglycan-mediated regulation of human neutrophil migration by the serpin antithrombin III. Blood 97, 1079-1085
13. Duensing, T. D., Wing, J. S., and van Putten, J. P. (1999) Sulfated polysaccharide-directed recruitment of mammalian host proteins: a novel strategy in microbial pathogenesis. Infect. Immun. 67, 4463-4468
14. Minnema, M. C., Chang, A. C., Jansen, P. M., Lubbers, Y. T., Pratt, B. M., Whittaker, B. G., Taylor, F. B., Hack, C. E., and Friedman, B. (2000) Recombinant human antithrombin III improves survival and attenuates inflammatory responses in baboons lethally challenged with Escherichia coli. Blood 95, 1117-1123
15. Fourrier, F., Jourdain, M., Tournois, A., Caron, C., Goudemand, J., and Chopin, C. (1995) Coagulation inhibitor substitution during sepsis. Intensive Care Med. 21, S264-S268
16. Baudo, F., Caimi, T. M., de Cataldo, F., Ravizza, A., Arlati, S., Casella, G., Carugo, D., Palareti, G., Legnani, C., Ridolfi, L., Rossi, R., D'Angelo, A., Crippa, L., Giudici, D., Gallioli, G., Wolfler, A., and Calori, G. (1998) Antithrombin III (ATIII) replacement therapy in patients with sepsis and/or postsurgical complications: a controlled double-blind, randomized, multicenter study. Intensive Care Med. 24, 336-342
17. Inthorn, D., Hoffmann, J. N., Hartl, W. H., Mühlbayer, D., and Jochum, M. (1998) Effect of antithrombin III supplementation on inflammatory response in patients with severe sepsis. Shock 10, 90-96
18. Giudici, D., Baudo, F., Palareti, G., Ravizza, A., Ridolfi, L., and D' Angelo, A. (1999) Antithrombin replacement in patients with sepsis and septic shock. Haematologica 84, 452-460
19. Warren, B. L., Eid, A., Singer, P., Pillay, S. S., Carl, P., Novak, I., Chalupa, P., Atherstone, A., Pénzes, I., Kübler, A., Knaub, S., Keinecke, H. O., Heinrichs, H., Schindel, F., Juers, M., Bone, R. C., Opal, S. M., and KyberSept Trial Study Group (2001) Caring for the critically ill patient. High-dose antithrombin III in severe sepsis: a randomized controlled trial. JAMA 286, 1869-1878
20. Tanaka, K. A., and Levy, J. H. (2007) Regulation of thrombin activity-pharmacologic and structural aspects. Hematol. Oncol. Clin. North Am. 21, 33-50
21. Blajchman, M. A. (1994) An overview of the mechanism of action of antithrombin and its inherited deficiency states. Blood Coagul. Fibrinolysis 5, S5-S11
22. Muñoz, E. M., and Linhardt, R. J. (2004) Heparin-binding domains in vascular biology. Arterioscler. Thromb. Vasc. Biol. 24, 1549-1557
23. Kalle, M., Papareddy, P., Kasetty, G., Tollefsen, D. M., Malmsten, M., Mörgelin, M., and Schmidtchen, A. (2013) Proteolytic activation transforms heparin cofactor II into a host defense molecule. J. Immunol. 190, 6303-6310
24. Rau, J. C., Beaulieu, L. M., Huntington, J. A., and Church, F. C. (2007) Serpins in thrombosis, hemostasis and fibrinolysis. J. Thromb. Haemost. 5, 102-115
25. Greenfield, N., and Fasman, G. D. (1969) Computed circular dichroism spectra for the evaluation of protein conformation. Biochemistry 8, 4108-4116
26. Sjögren, H., and Ulvenlund, S. (2005) Comparison of the helix-coil transition of a titrating polypeptide in aqueous solutions and at the air-water interface. Biophys. Chem. 116, 11-21
27. Picard, V., Ersdal-Badju, E., and Bock, S. C. (1995) Partial glycosylation of antithrombin III asparagine-135 is caused by the serine in the third position of its N-glycosylation consensus sequence and is responsible for production of the β-antithrombin III isoform with enhanced heparin affinity. Biochemistry 34, 8433-8440
28. Lundqvist, K., Herwald, H., Sonesson, A., and Schmidtchen, A. (2004) Heparin binding protein is increased in chronic leg ulcer fluid and released from granulocytes by secreted products of Pseudomonas aeruginosa. Thromb. Haemost. 92, 281-287
29. Onoue, S., Nemoto, Y., Harada, S., Yajima, T., and Kashimoto, K. (2003) Human antithrombin III-derived heparin-binding peptide, a novel heparin antagonist. Life Sci. 73, 2793-2806
30. Ganz, T. (2001) Antimicrobial proteins and peptides in host defense. Semin Respir. Infect. 16, 4-10
31. Wang, Y., Agerberth, B., Löthgren, A., Almstedt, A., and Johansson, J. (1998) Apolipoprotein A-I binds and inhibits the human antibacterial/cytotoxic peptide LL-37. J. Biol. Chem. 273, 33115-33118
32. Oelschläger, C., Römisch, J., Staubitz, A., Stauss, H., Leithäuser, B., Tillmanns, H., and Hölschermann, H. (2002) Antithrombin III inhibits nuclear factor κB activation in human monocytes and vascular endothelial cells. Blood 99, 4015-4020
33. Yang, L., Dinarvand, P., Qureshi, S. H., and Rezaie, A. R. (2014) Engineering D-helix of antithrombin in α-1-proteinase inhibitor confers antiinflammatory properties on the chimeric serpin. Thromb. Haemost. 112, 164-175
34. Nordahl, E. A., Rydenga˚rd, V., Nyberg, P., Nitsche, D. P., Mörgelin, M., Malmsten, M., Björck, L., and Schmidtchen, A. (2004) Activation of the complement system generates antibacterial peptides. Proc. Natl. Acad. Sci. U.S.A. 101, 16879-16884
35. Nordahl, E. A., Rydenga˚rd, V., Mörgelin, M., and Schmidtchen, A. (2005) Domain 5 of high molecular weight kininogen is antibacterial. J. Biol. Chem. 280, 34832-34839
36. Malmsten, M., Davoudi, M., and Schmidtchen, A. (2006) Bacterial killing by heparin-binding peptides from PRELP and thrombospondin. Matrix Biol. 25, 294-300
37. Andersson, E., Rydenga˚rd, V., Sonesson, A., Mörgelin, M., Björck, L., and Schmidtchen, A. (2004) Antimicrobial activities of heparin-binding peptides. Eur. J. Biochem. 271, 1219-1226
38. Papareddy, P., Kalle, M., Kasetty, G., Mörgelin, M., Rydenga˚rd, V., Albiger, B., Lundqvist, K., Malmsten, M., and Schmidtchen, A. (2010) C-terminal peptides of tissue factor pathway inhibitor are novel host defense molecules. J. Biol. Chem. 285, 28387-28398
39. Papareddy, P., Rydenga˚rd, V., Pasupuleti, M., Walse, B., Mörgelin, M., Chalupka, A., Malmsten, M., and Schmidtchen, A. (2010) Proteolysis of human thrombin generates novel host defense peptides. PLoS Pathog. 6, e1000857
40. Pasupuleti, M., Roupe, M., Rydenga˚rd, V., Surewicz, K., Surewicz, W. K., Chalupka, A., Malmsten, M., Sörensen, O. E., and Schmidtchen, A. (2009) Antimicrobial activity of human prion protein is mediated by its N-terminal region. PLoS One 4, e7358
41. Rydenga˚rd, V., Shannon, O., Lundqvist, K., Kacprzyk, L., Chalupka, A., Olsson, A. K., Mörgelin, M., Jahnen-Dechent, W., Malmsten, M., and Schmidtchen, A. (2008) Histidine-rich glycoprotein protects from systemic Candida infection. PLoS Pathog. 4, e1000116
42. Hofstra, J. J., Cornet, A. D., de Rooy, B. F., Vlaar, A. P., van der Poll, T., Levi, M., Zaat, S. A., and Schultz, M. J. (2009) Nebulized antithrombin limits bacterial outgrowth and lung injury in Streptococcus pneumoniae pneumonia in rats. Crit. Care 13, R145
43. Schmidtchen, A. (2000) Degradation of antiproteinases, complement and fibronectin in chronic leg ulcers. Acta Derm. Venereol. 80, 179-184
44. Mookherjee, N., Brown, K. L., Bowdish, D. M., Doria, S., Falsafi, R., Hokamp, K., Roche, F. M., Mu, R., Doho, G. H., Pistolic, J., Powers, J. P., Bryan, J., Brinkman, F. S., and Hancock, R. E. (2006) Modulation of the TLR-mediated inflammatory response by the endogenous human host defense peptide LL-37. J. Immunol. 176, 2455-2464
45. Nijnik, A., Madera, L., Ma, S., Waldbrook, M., Elliott, M. R., Easton, D. M., Mayer, M. L., Mullaly, S. C., Kindrachuk, J., Jenssen, H., and Hancock, R. E. (2010) Synthetic cationic peptide IDR-1002 provides protection against bacterial infections through chemokine induction and enhanced leukocyte recruitment. J. Immunol. 184, 2539-2550
46. Mookherjee, N., Lippert, D. N., Hamill, P., Falsafi, R., Nijnik, A., Kindrachuk, J., Pistolic, J., Gardy, J., Miri, P., Naseer, M., Foster, L. J., and Hancock, R. E. (2009) Intracellular receptor for human host defense peptide LL-37 in monocytes. J. Immunol. 183, 2688-2696
47. Malmsten, M., Kasetty, G., Pasupuleti, M., Alenfall, J., and Schmidtchen, A. (2011) Highly selective end-tagged antimicrobial peptides derived from PRELP. PLoS One 6, e16400
48. Jenssen, H., and Hancock, R. E. (2010) Therapeutic potential of HDPs as immunomodulatory agents. Methods Mol. Biol. 618, 329-347
49. Steinstraesser, L., Kraneburg, U., Jacobsen, F., and Al-Benna, S. (2011) Host defense peptides and their antimicrobial-immunomodulatory duality. Immunobiology 216, 322-333
50. van der Does, A. M., Beekhuizen, H., Ravensbergen, B., Vos, T., Ottenhoff, T. H., van Dissel, J. T., Drijfhout, J. W., Hiemstra, P. S., and Nibbering, P. H. (2010) LL-37 directs macrophage differentiation toward macrophages with a proinflammatory signature. J. Immunol. 185, 1442-1449
51. Rosenfeld, Y., Papo, N., and Shai, Y. (2006) Endotoxin (lipopolysaccharide) neutralization by innate immunity host-defense peptides. Peptide properties and plausible modes of action. J. Biol. Chem. 281, 1636-1643