Direct and alternative antimicrobial mechanisms of neutrophil-derived granule proteins

Journal of Molecular Medicine

Volumn 87, Issue 12, 2009, Pages 1157-1164

  Soehnlein, Oliver ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

Author keywords

Bacterial clearance; Macrophage; Neutrophil extracellular trap; Neutrophil granule protein; Phagocytosis

Indexed keywords

AZUROCIDIN; BACTERICIDAL PERMEABILITY INCREASING PROTEIN; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CATHEPSIN G; CELL PROTEIN; ELASTASE; FC RECEPTOR; HISTONE; LACTOFERRIN; LYSOZYME; NEUTROPHIL DERIVED GRANULE PROTEIN; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PEPTIDOGLYCAN RECOGNITION PROTEIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; UROKINASE;

APOPTOSIS; BACTERIAL INFECTION; BACTERICIDAL ACTIVITY; CELLULAR DISTRIBUTION; HUMAN; MACROPHAGE FUNCTION; MONOCYTE; NONHUMAN; OPSONIZATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW;

ANIMALS; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIA; BACTERIAL INFECTIONS; BLOOD PROTEINS; CELL DEGRANULATION; HUMANS; MACROPHAGES; NEUTROPHILS; PHAGOCYTOSIS;

EID: 70949104973     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-009-0508-6     Document Type: Review

References (71)

1. JA Lekstrom-Himes JI Gallin 2000 Immunodeficiency diseases caused by defects in phagocytes N Engl J Med 343 1703 1714 10.1056/NEJM200012073432307 11106721
2. DC Dale L Boxer WC Liles 2008 The phagocytes: neutrophils and monocytes Blood 112 935 945 10.1182/blood-2007-12-077917 18684880
3. O Levy 2004 Antimicrobial proteins and peptides: anti-infective molecules of mammalian leukocytes J Leukoc Biol 76 909 925 10.1189/jlb.0604320 15292276 (Pubitemid 39458703)
4. G Lominadze DW Powell GC Luerman AJ Link RA Ward KR McLeish 2005 Proteomic analysis of human neutrophil granules Mol Cell Proteomics 4 1503 1521 10.1074/mcp.M500143-MCP200 15985654 (Pubitemid 41555476)
5. M Faurschou N Borregaard 2003 Neutrophil granules and secretory vesicles in inflammation Microbes Infect 5 1317 1327 10.1016/j.micinf.2003.09.008 14613775 (Pubitemid 37410245)
6. SM Uriarte DW Powell GC Luerman ML Merchant TD Cummins NR Jog RA Ward KR McLeish 2008 Comparison of proteins expressed on secretory vesicle membranes and plasma membranes of human neutrophils J Immunol 180 5575 5581 18390742
7. N Borregaard OE Sørensen K Theilgaard-Mönch 2007 Neutrophil granules: a library of innate immunity proteins Trends Immunol 28 340 345 10.1016/j.it.2007.06.002 17627888 (Pubitemid 47077924)
8. KA Brogden 2005 Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3 238 250 10.1038/nrmicro1098 15703760 (Pubitemid 40298223)
9. HW Huang FY Chen MT Lee 2004 Molecular mechanism of Peptide-induced pores in membranes Phys Rev Lett 92 198304 10.1103/PhysRevLett.92.198304 15169456
10. RI Lehrer A Barton KA Daher SS Harwig T Ganz ME Selsted 1989 Interaction of human defensins with Escherichia coli. Mechanism of bactericidal activity J Clin Invest 84 553 561 10.1172/JCI114198 2668334
11. A Belaaouaj KS Kim SD Shapiro 2000 Degradation of outer membrane protein A in Escherichia coli killing by neutrophil elastase Science 289 1185 1188 10.1126/science.289.5482.1185 10947984 (Pubitemid 30650729)
12. Y Weinrauch D Drujan SD Shapiro J Weiss A Zychlinsky 2002 Neutrophil elastase targets virulence factors of enterobacteria Nature 417 91 94 10.1038/417091a 12018205 (Pubitemid 34498822)
13. WM Shafer F Hubalek M Huang J Pohl 1996 Bactericidal activity of a synthetic peptide (CG 117-136) of human lysosomal cathepsin G is dependent on arginine content Infect Immun 64 4842 4845 8890249
14. I Ginsburg 2002 The role of bacteriolysis in the pathophysiology of inflammation, infection and post-infectious sequelae APMIS 110 753 770 10.1034/j.1600-0463.2002.1101101.x 12588416 (Pubitemid 36152709)
15. EP Reeves H Lu HL Jacobs CG Messina S Bolsover G Gabella EO Potma A Warley J Roes AW Segal 2002 Killing activity of neutrophils is mediated through activation of proteases by K + flux Nature 416 291 297 10.1038/416291a 11907569 (Pubitemid 34260237)
16. P Lacy G Eitzen 2008 Control of granule exocytosis in neutrophils Front Biosci 13 5559 5570 10.2741/3099 18508605
17. G Cepinskas M Sandig PR Kvietys 1999 PAF-induced elastase-dependent neutrophil transendothelial migration is associated with the mobilization of elastase to the neutrophil surface and localization to the migrating front J Cell Sci 112 1937 1945 10341212
18. EJ Campbell MA Campbell CA Owen 2000 Bioactive proteinase 3 on the cell surface of human neutrophils: quantification, catalytic activity, and susceptibility to inhibition J Immunol 165 3366 3374 10975855
19. V Brinkmann U Reichard C Goosmann B Fauler Y Uhlemann DS Weiss Y Weinrauch A Zychlinsky 2004 Neutrophil extracellular traps kill bacteria Science 303 1532 1535 10.1126/science.1092385 15001782 (Pubitemid 38314426)
20. M von Köckritz-Blickwede O Goldmann P Thulin K Heinemann A Norrby-Teglund M Rohde E Medina 2008 Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation Blood 111 3070 3080 10.1182/blood-2007-07-104018
21. S Yousefi JA Gold N Andina JJ Lee AM Kelly E Kozlowski I Schmid A Straumann J Reichenbach GJ Gleich HU Simon 2008 Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense Nat Med 14 949 953 10.1038/nm.1855 18690244
22. K Kessenbrock M Krumbholz U Schönermarck W Back WL Gross Z Werb HJ Gröne V Brinkmann DE Jenne 2009 Netting neutrophils in autoimmune small-vessel vasculitis Nat Med 15 623 625 10.1038/nm.1959 19448636
23. F Wartha K Beiter S Normark B Henriques-Normark 2007 Neutrophil extracellular traps: casting the NET over pathogenesis Curr Opin Microbiol 10 52 56 10.1016/j.mib.2006.12.005 17208512 (Pubitemid 46217956)
24. SR Clark AC Ma SA Tavener B McDonald Z Goodarzi MM Kelly KD Patel S Chakrabarti E McAvoy GD Sinclair EM Keys E Allen-Vercoe R Devinney CJ Doig FH Green P Kubes 2007 Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood Nat Med 13 463 469 10.1038/nm1565 17384648 (Pubitemid 46559832)
25. M von Köckritz-Blickwede V Nizet 2009 Innate immunity turned inside-out: antimicrobial defense by phagocyte extracellular traps J Mol Med 87 775 783 10.1007/s00109-009-0481-0
26. V Brinkmann A Zychlinsky 2007 Beneficial suicide: why neutrophils die to make NETs Nat Rev Microbiol 5 577 582 10.1038/nrmicro1710 17632569 (Pubitemid 47074113)
27. Papayannopoulos V, Zychlinsky A (2009) NETs: a new strategy for using old weapons. Trends Immunol (in press)
28. F Wartha K Beiter B Albiger J Fernebro A Zychlinsky S Normark B Henriques-Normark 2007 Capsule and D-alanylated lipoteichoic acids protect Streptococcus pneumoniae against neutrophil extracellular traps Cell Microbiol 9 1162 1171 10.1111/j.1462-5822.2006.00857.x 17217430 (Pubitemid 46547136)
29. K Beiter F Wartha B Albiger S Normark A Zychlinsky B Henriques-Normark 2006 An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps Curr Biol 16 401 407 10.1016/j.cub.2006.01.056 16488875 (Pubitemid 43259351)
30. Y Lai RL Gallo 2009 AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense Trends Immunol 30 131 141 10.1016/j.it.2008.12. 003 19217824
31. O Soehnlein L Lindbom 2009 Neutrophil-derived azurocidin alarms the immune system J Leukoc Biol 85 344 351 10.1189/jlb.0808495 18955543
32. JJ Oppenheim D Yang 2005 Alarmins: chemotactic activators of immune responses Curr Opin Immunol 17 359 365 10.1016/j.coi.2005.06.002 15955682 (Pubitemid 40848537)
33. Soehnlein O, Weber C, Lindbom L (2009) Neutrophil granule proteins tune monocytic cell function. Trends Immunol. doi: 10.1016/j.it.2009.06.006
34. Soehnlein O, Zernecke A, Weber C (2009) Neutrophil granule proteins launch monocyte extravasation. Thromb Haemost. doi: 10.1160/TH08-11-0720
35. O Soehnlein C Weber 2009 Myeloid cells in atherosclerosis: initiators and decision shapers Semin Immunopathol 31 35 47 10.1007/s00281-009-0141-z 19238385
36. O Soehnlein X Xie H Ulbrich E Kenne P Rotzius H Flodgaard EE Eriksson L Lindbom 2005 Neutrophil-derived heparin-binding protein (HBP/CAP37) deposited on endothelium enhances monocyte arrest under flow conditions J Immunol 174 6399 6405 15879141
37. O Soehnlein A Zernecke EE Eriksson AG Rothfuchs CT Pham H Herwald K Bidzhekov ME Rottenberg C Weber L Lindbom 2008 Neutrophil secretion products pave the way for inflammatory monocytes Blood 112 1461 1471 10.1182/blood-2008- 02-139634 18490516
38. Y Kai-Larsen B Agerberth 2008 The role of the multifunctional peptide LL-37 in host defense Front Biosci 13 3760 3767 10.2741/2964 18508470 (Pubitemid 351594656)
39. F Niyonsaba K Iwabuchi A Someya M Hirata H Matsuda H Ogawa I Nagaoka 2002 A cathelicidin family of human antibacterial peptide LL-37 induces mast cell chemotaxis Immunology 106 20 26 10.1046/j.1365-2567.2002.01398.x 11972628 (Pubitemid 34437873)
40. Yang D, de la Rosa G, Tewary P, Oppenheim JJ (2009) Alarmins link neutrophils and dendritic cells. Trends Immunol (in press)
41. Müller I, Munder M, Kropf P, Hänsch GM (2009) Polymorphonuclear neutrophils and T lymphocytes: strange bedfellows or brothers in arms? Trends Immunol (in press)
42. Peiser L, Gordon S (2001) Phagocytosis: enhancement. Encyclopedia of life sciences. Wiley, Chichester. doi: 10.1038/npg.els.0001214
43. J Fleischmann ME Selsted RI Lehrer 1985 Opsonic activity of MCP-1 and MCP-2, cationic peptides from rabbit alveolar macrophages Diagn Microbiol Infect Dis 3 233 242 10.1016/0732-8893(85)90035-5 3888509 (Pubitemid 15039660)
44. M Heinzelmann A Platz H Flodgaard FN Miller 1998 Heparin binding protein (CAP37) is an opsonin for Staphylococcus aureus and increases phagocytosis in monocytes Inflammation 22 493 507 10.1023/A:1022398027143 9793796 (Pubitemid 28498043)
45. O Soehnlein Y Kai-Larsen R Frithiof OE Sorensen E Kenne K Scharffetter-Kochanek EE Eriksson H Herwald B Agerberth L Lindbom 2008 Neutrophil primary granule proteins HBP and HNP1-3 boost bacterial phagocytosis by human and murine macrophages J Clin Invest 118 3491 3502 10.1172/JCI35740 18787642
46. LI Påhlman M Mörgelin J Eckert L Johansson W Russell K Riesbeck O Soehnlein L Lindbom A Norrby-Teglund RR Schumann L Björck H Herwald 2006 Streptococcal M protein: a multipotent and powerful inducer of inflammation J Immunol 177 1221 1228 16818781
47. DM Mosser JP Edwards 2008 Exploring the full spectrum of macrophage activation Nat Rev Immunol 8 958 969 10.1038/nri2448 19029990
48. AF Gombart HP Koeffler 2002 Neutrophil specific granule deficiency and mutations in the gene encoding transcription factor C/EBP(epsilon) Curr Opin Hematol 9 36 42 10.1097/00062752-200201000-00007 11753076 (Pubitemid 34025310)
49. S Tavor PT Vuong DJ Park AF Gombart AH Cohen HP Koeffler 2002 Macrophage functional maturation and cytokine production are impaired in C/EBP epsilon-deficient mice Blood 99 1794 1801 10.1182/blood.V99.5.1794 11861297 (Pubitemid 34533055)
50. M Heinzelmann MA Mercer-Jones J Peyton H Flodgaard WG Cheadle 2000 Heparin binding protein increases survival in murine fecal peritonitis Crit Care Med 28 2926 2931 10.1097/00003246-200008000-00040 10966273
51. O Soehnlein E Kenne P Rotzius EE Eriksson L Lindbom 2008 Neutrophil secretion products regulate anti-bacterial activity in monocytes and macrophages Clin Exp Immunol 151 139 145 17991288
52. O Soehnlein S Oehmcke X Ma AG Rothfuchs R Frithiof N van Rooijen M Mörgelin H Herwald L Lindbom 2008 Neutrophil degranulation mediates severe lung damage triggered by streptococcal M1 protein Eur Respir J 32 405 412 10.1183/09031936.00173207 18321926
53. SM Zughaier WM Shafer DS Stephens 2005 Antimicrobial peptides and endotoxin inhibit cytokine and nitric oxide release but amplify respiratory burst response in human and murine macrophages Cell Microbiol 7 1251 1262 10.1111/j.1462-5822.2005.00549.x 16098213 (Pubitemid 41179418)
54. MT Ochoa S Stenger PA Sieling S Thoma-Uszynski S Sabet S Cho AM Krensky M Rollinghoff E Nunes Sarno AE Burdick TH Rea RL Modlin 2001 T-cell release of granulysin contributes to host defense in leprosy Nat Med 7 174 179 10.1038/84620 11175847 (Pubitemid 32148483)
55. BH Tan C Meinken M Bastian H Bruns A Legaspi MT Ochoa SR Krutzik BR Bloom T Ganz RL Modlin S Stenger 2006 Macrophages acquire neutrophil granules for antimicrobial activity against intracellular pathogens J Immunol 177 1864 1871 16849498
56. FL Ribeiro-Gomes MC Moniz-de-Souza MS Alexandre-Moreira WB Dias MF Lopes MP Nunes G Lungarella GA DosReis 2007 Neutrophils activate macrophages for intracellular killing of Leishmania major through recruitment of TLR4 by neutrophil elastase J Immunol 179 3988 3994 17785837
57. KL Brown C Cosseau JL Gardy RE Hancock 2007 Complexities of targeting innate immunity to treat infection Trends Immunol 28 260 266 10.1016/j.it.2007.04.005 17468048 (Pubitemid 46824085)
58. RE Hancock HG Sahl 2006 Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies Nat Biotechnol 24 1551 1557 10.1038/nbt1267 17160061 (Pubitemid 44967479)
59. RW Scott WF DeGrado GN Tew 2008 De novo designed synthetic mimics of antimicrobial peptides Curr Opin Biotechnol 19 620 627 10.1016/j.copbio.2008.10. 013 18996193
60. L Zhang TJ Falla 2006 Antimicrobial peptides: therapeutic potential Expert Opin Pharmacother 7 653 663 10.1517/14656566.7.6.653 16556083
61. L Zhang TJ Falla 2009 Host defense peptides for use as potential therapeutics Curr Opin Investig Drugs 10 164 171 19197794
62. PH Mygind RL Fischer KM Schnorr MT Hansen CP Sönksen S Ludvigsen D Raventós S Buskov B Christensen L De Maria, et al. 2005 Plectasin is a peptide antibiotic with therapeutic potential from a saprophytic fungus Nature 437 975 980 10.1038/nature04051 16222292 (Pubitemid 41486973)
63. MG Scott E Dullaghan N Mookherjee N Glavas M Waldbrook A Thompson A Wang K Lee S Doria P Hamill JJ Yu Y Li O Donini MM Guarna BB Finlay JR North RE Hancock 2007 An anti-infective peptide that selectively modulates the innate immune response Nat Biotechnol 25 465 472 10.1038/nbt1288 17384586 (Pubitemid 46572850)
64. KA Henzler-Wildman GV Martinez MF Brown A Ramamoorthy 2004 Perturbation of the hydrophobic core of lipid bilayers by the human antimicrobial peptide LL-37 Biochemistry 43 8459 8469 10.1021/bi036284s 15222757 (Pubitemid 38902524)
65. Campanelli D, Detmers PA, Nathan CF, Gabay JE 1990 Azurocidin and a homologous serine protease from neutrophils. Differential antimicrobial and proteolytic properties J Clin Invest 85 904 915 10.1172/JCI114518
66. D Caccavo NM Pellegrino M Altamura A Rigon L Amati A Amoroso E Jirillo 2002 Antimicrobial and immunoregulatory functions of lactoferrin and its potential therapeutic application J Endotoxin Res 8 403 417 12542852
67. S Farnaud RW Evans 2003 Lactoferrin-a multifunctional protein with antimicrobial properties Mol Immunol 40 395 405 10.1016/S0161-5890(03)00152-4 14568385 (Pubitemid 37244032)
68. T Wu LP Samaranayake WK Leung PA Sullivan 1999 Inhibition of growth and secreted aspartyl proteinase production in Candida albicans by lysozyme J Med Microbiol 48 721 730 10.1099/00222615-48-8-721 10450995
69. DH Goetz MA Holmes N Borregaard ME Bluhm KN Raymond RK Strong 2002 The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition Mol Cell 10 1033 1043 10.1016/S1097- 2765(02)00708-6 12453412 (Pubitemid 36001971)
70. R Dziarski KA Platt E Gelius H Steiner D Gupta 2003 Defect in neutrophil killing and increased susceptibility to infection with nonpathogenic gram-positive bacteria in peptidoglycan recognition protein-S (PGRP-S)-deficient mice Blood 102 689 697 10.1182/blood-2002-12-3853 12649138 (Pubitemid 36841993)
71. T Jin M Bokarewa A Tarkowski 2005 Urokinase-type plasminogen activator, an endogenous antibiotic J Infect Dis 192 429 437 10.1086/431600 15995956 (Pubitemid 41023121)