Mechanisms underlying neutrophil-mediated monocyte recruitment

Blood

Volumn 114, Issue 21, 2009, Pages 4613-4623

  Soehnlein, Oliver ^a   Lindbom, Lennart ^b   Weber, Christian ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTEGRIN; CELL PROTEIN; CHEMOKINE; CYTOKINE; FORMYLPEPTIDE RECEPTOR; LYSOPHOSPHATIDYLCHOLINE; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; CELL ADHESION; CELL MIGRATION; EXTRAVASATION; HUMAN; INFLAMMATION; MONOCYTE; NEUTROPHIL; NEUTROPHIL GRANULE; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; IMMUNOLOGY; NEUTROPHIL CHEMOTAXIS;

ANIMALS; CHEMOTAXIS, LEUKOCYTE; HUMANS; INFLAMMATION; MONOCYTES; NEUTROPHILS;

EID: 73949096361     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-06-221630     Document Type: Review

References (121)

1. Rebuck JW, Crowley JH. A method of studying leukocytic functions in vivo. Ann N Y Acad Sci. 1955;59(5):757-805.
2. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol. 2007;7(9):678-689.
3. Ward PA. Chemotoxis of mononuclear cells. J Exp Med. 1968;128(5):1201- 1221.
4. Gallin JI, Fletcher MP, Seligmann BE, et al. Human neutrophil-specific granule deficiency: a model to assess the role of neutrophil-specific granules in the evolution of the inflammatory response. Blood. 1982;59(6):1317-1329.
5. Gombart AF, Koeffler HP. Neutrophil specific granule deficiency and mutations in the gene encoding transcription factor C/EBP(epsilon). Curr Opin Hematol. 2002;9(1):36-42.
6. Gallin JI, Klimerman JA, Padgett GA, Wolff SM. Defective mononuclear leukocyte chemotaxis in the Chediak-Higashi syndrome of humans, mink, and cattle. Blood. 1975;45(6):863-870.
7. Mokart D, Kipnis E, Guerre-Berthelot P, et al. Monocyte deactivation in neutropenic acute respiratory distress syndrome patients treated with granulocyte colony-stimulating factor. Crit Care. 2008;12(1):R17. doi:10.1186/cc6791.
8. Shiohara M, Gombart AF, Sekiguchi Y, et al. Phenotypic and functional alterations of peripheral blood monocytes in neutrophil-specific granule deficiency. J Leukoc Biol. 2004;75(2):190-197.
9. Florido M, Appelberg R, Orme IM, Cooper AM. Evidence for a reduced chemokine response in the lungs of beige mice infected with Mycobacterium avium. Immunology. 1997;90(4):600-606.
10. Soehnlein O, Zernecke A, Eriksson EE, et al. Neutrophil secretion products pave the way for inflammatory monocytes. Blood. 2008;112(4):1461-1471.
11. Zernecke A, Bot I, Djalali-Talab Y, et al. Protective role of CXC receptor 4/CXC ligand 12 unveils the importance of neutrophils in atherosclerosis. Circ Res. 2008;102(2):209-217.
12. Janardhan KS, Sandhu SK, Singh B. Neutrophil depletion inhibits early and late monocyte/macrophage increase in lung inflammation. Front Biosci. 2006;11:1569-1576.
13. Conlan JW, North RJ. Neutrophils are essential for early anti-Listeria defense in the liver, but not in the spleen or peritoneal cavity, as revealed by a granulocyte-depleting monoclonal antibody. J Exp Med. 1994;179(1):259-268.
14. Chalaris A, Rabe B, Paliga K, et al. Apoptosis is a natural stimulus of IL6R shedding and contributes to the proinflammatory trans-signaling function of neutrophils. Blood. 2007;110(6):1748-1755.
15. von Stebut E, Metz M, Milon G, Knop J, Maurer M. Early macrophage influx to sites of cutaneous granuloma formation is dependent on MIP-1alpha/beta released from neutrophils recruited by mast cell-derived TNFalpha. Blood. 2003;101(1):210-215.
16. Zhou J, Stohlman SA, Hinton DR, Marten NW. Neutrophils promote mononuclear cell infiltration during viral-induced encephalitis. J Immunol. 2003;170(6):3331-3336.
17. Kim M, Carman CV, Springer TA. Bidirectional transmembrane signaling by cytoplasmic domain separation in integrins. Science. 2003;301(5640):1720-1725.
18. Zernecke A, Shagdarsuren E, Weber C. Chemokines in atherosclerosis: an update. Arterioscler Thromb Vasc Biol. 2008;28(11):1897-1908.
19. Weber C. Chemokines take centre stage in vascular biology. Thromb Haemost. 2007;97(5):685-687.
20. Frankenberger M, Sternsdorf T, Pechumer H, Pforte A, Ziegler-Heitbrock HW. Differential cytokine expression in human blood monocyte subpopulations: a polymerase chain reaction analysis. Blood. 1996;87(1):373-377.
21. Ziegler-Heitbrock HW. Heterogeneity of human blood monocytes: the CD14+ CD16+ subpopulation. Immunol Today. 1996;17(9):424-428.
22. Belge KU, Dayyani F, Horelt A, et al. The proinflammatory CD14+CD16+DR++ monocytes are a major source of TNF. J Immunol. 2002;168(7):3536-3542.
23. Strauss-Ayali D, Conrad SM, Mosser DM. Monocyte subpopulations and their differentiation patterns during infection. J Leukoc Biol. 2007;82(2):244-252.
24. Ziegler-Heitbrock L. The CD14+ CD16+ blood monocytes: their role in infection and inflammation. J Leukoc Biol. 2007;81(3):584-592.
25. Weber C, Belge KU, von Hundelshausen P, et al. Differential chemokine receptor expression and function in human monocyte subpopulations. J Leukoc Biol. 2000;67(5):699-6704.
26. Ancuta P, Rao R, Moses A, et al. Fractalkine preferentially mediates arrest and migration of CD16+ monocytes. J Exp Med. 2003;197(12):1701-1707.
27. Ancuta P, Moses A, Gabuzda D. Transendothelial migration of CD16+ monocytes in response to fractalkine under constitutive and inflammatory conditions. Immunobiology. 2004;209(1-2):11-20.
28. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity. 2003;19(1):71-82.
29. Serbina NV, Jia T, Hohl TM, Pamer EG. Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol. 2008;26:421-452.
30. Nahrendorf M, Swirski FK, Aikawa E, et al. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med. 2007;204(12):3037-3047.
31. Imhof BA, Aurrand-Lions M. Adhesion mechanisms regulating the migration of monocytes. Nat Rev Immunol. 2004;4(6):432-444.
32. 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.
33. Merad M, Manz MG, Karsunky H, et al. Langerhans cells renew in the skin throughout life under steady-state conditions. Nat Immunol. 2002;3(12):1135- 1141.
34. Jung S, Aliberti J, Graemmel P, et al. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol. 2000;20(11):4106-4114.
35. Landsman L, Bar-On L, Zernecke A, et al. CX3CR1 is required for monocyte homeostasis and atherogenesis by promoting cell survival. Blood. 2009;113(4):963-972.
36. Merad M, Hoffmann P, Ranheim E, et al. Depletion of host Langerhans cells before transplantation of donor alloreactive T cells prevents skin graft-versus-host disease. Nat Med. 2004;10(5):510-517.
37. Le Borgne M, Etchart N, Goubier A, et al. Dendritic cells rapidly recruited into epithelial tissues via CCR6/CCL20 are responsible for CD8+ T cell crosspriming in vivo. Immunity. 2006;24(2):191-201.
38. Sunderkötter C, Nikolic T, Dillon MJ, et al. Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol. 2004;172(7):4410-4417.
39. Ginhoux F, Tacke F, Angeli V, et al. Langerhans cells arise from monocytes in vivo. Nat Immunol. 2006;7(3):265-273.
40. Auffray C, Fogg D, Garfa M, et al. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science. 2007;317(5838):666-670.
41. An G, Wang H, Tang R, et al. P-selectin glycoprotein ligand-1 is highly expressed on Ly-6Chi monocytes and a major determinant for Ly-6Chi monocyte recruitment to sites of atherosclerosis in mice. Circulation. 2008;117:3227-3237.
42. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol. 2005;5(12):953-964.
43. Faurschou M, Borregaard N. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect. 2003;5(14):1317-1327.
44. Di Gennaro A, Kenne E, Wan M, Soehnlein O, Lindbom L, Haeggström JZ. Leukotriene B4-induced changes in vascular permeability are mediated by neutrophil release of heparin-binding protein (HBP/CAP37/azurocidin). FASEB J. 2009;23(6):1750-1757.
45. Soehnlein O, Oehmcke S, Ma X, et al. Neutrophil degranulation mediates severe lung damage triggered by streptococcal M1 protein. Eur Respir J. 2008;32(2):405-412.
46. Kahn R, Hellmark T, Leeb-Lundberg LM, et al. Neutrophil-derived proteinase 3 induces kallikrein-independent release of a novel vasoactive kinin. J Immunol. 2009;182(12):7906-7915.
47. Pereira HA, Moore P, Grammas P. CAP37, a neutrophil granule-derived protein stimulates protein kinase C activity in endothelial cells. J Leukoc Biol. 1996;60(3):415-422.
48. Olofsson AM, Vestberg M, Herwald H, et al. Heparin-binding protein targeted to mitochondrial compartments protects endothelial cells from apoptosis. J Clin Invest. 1999;104(7):885-894.
49. Lee TD, Gonzalez ML, Kumar P, et al. CAP37, a neutrophil-derived inflammatory mediator, augments leukocyte adhesion to endothelial monolayers. Microvasc Res. 2003;66(1):38-48.
50. Taekema-Roelvink ME, Kooten C, Kooij SV, et al. Proteinase 3 enhances endothelial monocyte chemoattractant protein-1 production and induces increased adhesion of neutrophils to endothelial cells by upregulating intercellular cell adhesion molecule-1. J Am Soc Nephrol. 2001;12(5):932-940.
51. Lee TD, Gonzalez ML, Kumar P, et al. CAP37, a novel inflammatory mediator: its expression in endothelial cells and localization to atherosclerotic lesions. Am J Pathol. 2002;160(3):841-848.
52. Pereira HA, Kumar P, Grammas P. Expression of CAP37, a novel inflammatory mediator, in Alzheimer's disease. Neurobiol Aging. 1996;17(5):753-759.
53. Soehnlein O, Xie X, Ulbrich H, et al. Neutrophil-derived heparin-binding protein (HBP/CAP37) deposited on endothelium enhances monocyte arrest under flow conditions. J Immunol. 2005;174(10):6399-6405.
54. Påhlman LI, Mörgelin M, Eckert J, et al. Streptococcal M protein: a multipotent and powerful inducer of inflammation. J Immunol. 2006;177(2):1221-1228.
55. Heinzelmann M, Mercer-Jones MA, Flodgaard H, et al. Heparin-binding protein (CAP37) is internalized in monocytes and increases LPS-induced monocyte activation. J Immunol. 1998;160(11):5530-5536.
56. David A, Kacher Y, Specks U, et al. Interaction of proteinase 3 with CD11b/CD18 (beta2 integrin) on the cell membrane of human neutrophils. J Leukoc Biol. 2003;74(4):551-557.
57. Chertov O, Ueda H, Xu LL, et al. Identification of human neutrophil-derived cathepsin G and azurocidin/CAP37 as chemoattractants for mononuclear cells and neutrophils. J Exp Med. 1997;186(5):739-747.
58. Chertov O, Michiel DF, Xu L, et al. Identification of defensin-1, defensin-2, and CAP37/azurocidin as T-cell chemoattractant proteins released from interleukin-8-stimulated neutrophils. J Biol Chem. 1996;271(6):2935-2940.
59. De Yang Chen Q, Schmidt AP, et al. LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J Exp Med. 2000;192(7):1069-1074.
60. Oppenheim JJ, Yang D. Alarmins: chemotactic activators of immune responses. Curr Opin Immunol. 2005;17(4):359-365.
61. Oppenheim JJ, Tewary P, de la Rosa G, et al. Alarmins initiate host defense. Adv Exp Med Biol. 2007;601:185-194.
62. Soehnlein O, Lindbom L. Neutrophil-derived azurocidin alarms the immune system. J Leukoc Biol. 2009;85(3):344-351.
63. Tapper H, Karlsson A, Mörgelin M, et al. Secretion of heparin-binding protein from human neutrophils is determined by its localization in azurophilic granules and secretory vesicles. Blood. 2002;99(5):1785-1793.
64. Heinzelmann M, Kim E, Hofmeister A, et al. Heparin binding protein (CAP37) differentially modulates endotoxin-induced cytokine production. Int J Surg Investig. 2001;2(6):457-466.
65. Heinzelmann M, Platz A, Flodgaard H, et al. Endocytosis of heparin-binding protein (CAP37) is essential for the enhancement of lipopolysaccharide-induced TNF-alpha production in human monocytes. J Immunol. 1999;162(7):4240-4245.
66. Tjabringa GS, Aarbiou J, Ninaber DK, et al. The antimicrobial peptide LL-37 activates innate immunity at the airway epithelial surface by transactivation of the epidermal growth factor receptor. J Immunol. 2003;171(12):6690-6696.
67. Bowdish DM, Davidson DJ, Speert DP, et al. The human cationic peptide LL-37 induces activation of the extracellular signal-regulated kinase and p38 kinase pathways in primary human monocytes. J Immunol. 2004;172(6):3758-3765.
68. Van Wetering S, Mannesse-Lazeroms SP, Dijkman JH, et al. Effect of neutrophil serine proteinases and defensins on lung epithelial cells: modulation of cytotoxicity and IL-8 production. J Leukoc Biol. 1997;62(2):217-226.
69. Van Wetering S, Mannesse-Lazeroms SP, Van Sterkenburg MA, et al. Effect of defensins on interleukin-8 synthesis in airway epithelial cells. Am J Physiol. 1997;272(5 pt 1):L888-L896.
70. Liu CY, Lin HC, Yu CT, et al. The concentration-dependent chemokine release and pro-apoptotic effects of neutrophil-derived alpha-defensin-1 on human bronchial and alveolar epithelial cells. Life Sci. 2007;80:749-758.
71. Sakamoto N, Mukae H, Fujii T, et al. Differential effects of alpha- and beta-defensin on cytokine production by cultured human bronchial epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2005;288(3):L508-L513.
72. Khine AA, Del Sorbo L, Vaschetto R, et al. Human neutrophil peptides induce interleukin-8 production through the P2Y6 signaling pathway. Blood. 2006;107(7):2936-2942.
73. Pham CT. Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol. 2006;6(7):541-550.
74. Wiedow O, Meyer-Hoffert U. Neutrophil serine proteases: potential key regulators of cell signalling during inflammation. J Intern Med. 2005;257(4):319-328.
75. Padrines M, Wolf M, Walz A, et al. Interleukin-8 processing by neutrophil elastase, cathepsin G and proteinase-3. FEBS Lett. 1994;352(2):231-235.
76. Nufer O, Corbett M, Walz A. Amino-terminal processing of chemokine ENA-78 regulates biological activity. Biochemistry. 1999;38(2):636-642.
77. Berahovich RD, Miao Z, Wang Y, et al. Proteolytic activation of alternative CCR1 ligands in inflammation. J Immunol. 2005;174(11):7341-7351.
78. Wittamer V, Bondue B, Guillabert A et al. Neutrophil-mediated maturation of chemerin: a link between innate and adaptive immunity. J Immunol. 2005;175(1):487-493.
79. Rao RM, Betz TV, Lamont DJ, et al. Elastase release by transmigrating neutrophils deactivates endothelial-bound SDF-1α and attenuates subsequent T lymphocyte transendothelial migration. J Exp Med. 2004;200(6):713-724.
80. Ryu OH, Choi SJ, Firatli E et al. Proteolysis of macrophage inflammatory protein-1α isoforms LD78β and LD78α by neutrophil-derived serine proteases. J Biol Chem. 2005;280(17):17415-17421.
81. Scapini P, Lapinet-Vera JA, Gasperini S, Calzetti F, Bazzoni F, Cassatella MA. The neutrophil as a cellular source of chemokines. Immunol Rev. 2000;177:195-203.
82. Burn TC, Petrovick MS, Hohaus S, Rollins BJ, Tenen DG. Monocyte chemoattractant protein-1 gene is expressed in activated neutrophils and retinoic acid-induced human myeloid cell lines. Blood. 1994;84(8):2776-2783.
83. Bazzoni F, Cassatella MA, Rossi F, Ceska M, Dewald B, Baggiolini M. Phagocytosing neutrophils produce and release high amounts of the neutrophil-activating peptide 1/interleukin 8. J Exp Med. 1991;173(3):771-774.
84. Gerszten RE, Garcia-Zepeda EA, Lim YC, et al. MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Nature. 1999;398(6729):718-723.
85. Smith DF, Galkina E, Ley K, Huo Y. GRO family chemokines are specialized for monocyte arrest from flow. Am J Physiol Heart Circ Physiol. 2005;289(5):H1976-H1984.
86. Kasama T, Strieter RM, Standiford TJ, Burdick MD, Kunkel SL. Expression and regulation of human neutrophil-derived macrophage inflammatory protein 1 alpha. J Exp Med. 1993;178(1):63-72.
87. Scapini P, Laudanna C, Pinardi C, et al. Neutrophils produce biologically active macrophage inflammatory protein-3alpha (MIP-3alpha)/CCL20 and MIP-3beta/CCL19. Eur J Immunol. 2001;31(7):1981-1988.
88. Romano M, Sironi M, Toniatti C, et al. Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment. Immunity. 1997;6(3):315-325.
89. Müllberg J, Schooltink H, Stoyan T, et al. The soluble interleukin-6 receptor is generated by shedding. Eur J Immunol. 1993;23(2):473-480.
90. Desgeorges A, Gabay C, Silacci P, et al. Concentrations and origins of soluble interleukin 6 receptor-alpha in serum and synovial fluid. J Rheumatol. 1997;24(8):1510-1516.
91. Taga T, Hibi M, Hirata Y, et al. Interleukin-6 triggers the association of its receptor with a possible signal transducer, gp130. Cell. 1989;58(3):573-581.
92. Coletta I, Soldo L, Polentarutti N, et al. Selective induction of MCP-1 in human mesangial cells by the IL-6/sIL-6R complex. Exp Nephrol. 2000;8(1):37-43.
93. Spörri B, Müller KM, Wiesmann U, Bickel M. Soluble IL-6 receptor induces calcium flux and selectively modulates chemokine expression in human dermal fibroblasts. Int Immunol. 1999;11(7):1053-1058.
94. Hurst SM, Wilkinson TS, McLoughlin RM, et al. Il-6 and its soluble receptor orchestrate a temporal switch in the pattern of leukocyte recruitment seen during acute inflammation. Immunity. 2001;14(6):705-714.
95. Marin V, Montero-Julian FA, Grès S, et al. The IL-6-soluble IL-6Ralpha autocrine loop of endothelial activation as an intermediate between acute and chronic inflammation: an experimental model involving thrombin. J Immunol. 2001;167(6):3435-3442.
96. Marin V, Montero-Julian F, Grès S, Bongrand P, Farnarier C, Kaplanski G. Chemotactic agents induce IL-6Ralpha shedding from polymorphonuclear cells: involvement of a metalloproteinase of the TNF-alpha-converting enzyme (TACE) type. Eur J Immunol. 2002;32(10):2965-2970.
97. Xing Z, Gauldie J, Cox G, et al. IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J Clin Invest. 1998;101(2):311-320.
98. Kobayashi SD, Braughton KR, Whitney AR, et al. Bacterial pathogens modulate an apoptosis differentiation program in human neutrophils. Proc Natl Acad Sci U S A. 2003;100(19):10948-10953.
99. Jonsson H, Allen P, Peng SL. Inflammatory arthritis requires Foxo3a to prevent Fas ligand-induced neutrophil apoptosis. Nat Med. 2005;11(6):666-671.
100. Walmsley SR, Print C, Farahi N, et al. Hypoxia-induced neutrophil survival is mediated by HIF-1alpha-dependent NF-kappaB activity. J Exp Med. 2005;201(1):105-115.
101. Altznauer F, Martinelli S, Yousefi S, et al. Inflammation-associated cell cycle-independent block of apoptosis by survivin in terminally differentiated neutrophils. J Exp Med. 2004;199(10):1343-1354.
102. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303(5663):1532-1535.
103. Lauber K, Bohn E, Kröber SM, et al. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell. 2003;113(6):717-730.
104. Kim SJ, Gershov D, Ma X, Brot N, Elkon KB. I-PLA(2) activation during apoptosis promotes the exposure of membrane lysophosphatidylcholine leading to binding by natural immunoglobulin M antibodies and complement activation. J Exp Med. 2002;196(5):655-665.
105. Soehnlein O, Weber C. Myeloid cells in atherosclerosis: initiators and decision shapers. Semin Immunopathol. 2009;31(1):35-47.
106. Rotzius P, Soehnlein O, Kenne E, et al. ApoE (-/-)/lysozyme M(EGFP/EGFP) mice as a versatile model to study monocyte and neutrophil trafficking in atherosclerosis. Atherosclerosis. 2009;202(1):111-118.
107. Lauber K, Blumenthal SG, Waibel M, Wesselborg S. Clearance of apoptotic cells: getting rid of the corpses. Mol Cell. 2004;14(3):277-287.
108. Peter C, Waibel M, Radu CG, et al. Migration to apoptotic "find-me" signals is mediated via the phagocyte receptor G2A. J Biol Chem. 2008;283(9):5296-5305.
109. Zhao M, Song B, Pu J, et al. Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-gamma and PTEN. Nature. 2006;442:457-460.
110. Auffray C, Sieweke MH, Geissmann F. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu Rev Immunol. 2009;27:669-692.
111. Soehnlein O, Kai-Larsen Y, Frithiof R, et al. Neutrophil primary granule proteins HBP and HNP1-3 boost bacterial phagocytosis by human and murine macrophages. J Clin Invest. 2008;118(10):3491-3502.
112. Soehnlein O, Weber C, Lindbom L. Neutrophil granule proteins tune monocytic cell function. Trends Immunol. 2009;30(11):538-546. doi:10.1016/j.it.2009.06.006.
113. Soehnlein O, Kenne E, Rotzius P, Eriksson EE, Lindbom L. Neutrophil secretion products regulate anti-bacterial activity in monocytes and macrophages. Clin Exp Immunol. 2008;151(1):139-145.
114. Soehnlein O. Direct and alternative antimicrobial mechanisms of neutrophil-derived granule proteins. J Mol Med. 2009. doi:10.1007/s00109-009- 0508-6.
115. Ulbrich H, Eriksson EE, Lindbom L. Leukocyte and endothelial cell adhesion molecules as targets for therapeutic interventions in inflammatory disease. Trends Pharmacol Sci. 2003;24(12):640-647.
116. de Garavilla L, Greco MN, Sukumar N, et al. A novel, potent dual inhibitor of the leukocyte proteases cathepsin G and chymase: molecular mechanisms and anti-inflammatory activity in vivo. J Biol Chem. 2005;280(18):18001-18007.
117. Takashi S, Park J, Fang S, Koyama S, Parikh I, Adler KB. A peptide against the N-terminus of myristoylated alanine-rich C kinase substrate inhibits degranulation of human leukocytes in vitro. Am J Respir Cell Mol Biol. 2006;34(5):647-652.
118. Scott MG, Dullaghan E, Mookherjee N, et al. An anti-infective peptide that selectively modulates the innate immune response. Nat Biotechnol. 2007;25(4):465-472.
119. Koenen RR, von Hundelshausen P, Nesmelova IV, et al. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med. 2009;15(1):97-103.
120. Brodmerkel CM, Huber R, Covington M, et al. Discovery and pharmacological characterization of a novel rodent-active CCR2 antagonist, INCB3344. J Immunol. 2005;175(8):5370-5378.
121. Nowell MA, Williams AS, Carty SA, et al. Therapeutic targeting of IL-6 trans signaling counteracts STAT3 control of experimental inflammatory arthritis. J Immunol. 2009;182(1):613-622.