The immediate protective response to microbial challenge

European Journal of Immunology

Volumn 44, Issue 9, 2014, Pages 2536-2549

  Gonźalez Navajas, José M ^a,b   Corr, Mary P ^b   Raz, Eyal ^b  

^a HOSPITAL GENERAL UNIVERSITARIO DE ALICANTE   (Spain)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Antimicrobial response; Infection; Innate immunity

Indexed keywords

TOLL LIKE RECEPTOR;

ANIMAL; ANTIMICROBIAL RESPONSE; HUMAN; IMMUNOLOGY; INFECTION; INNATE IMMUNITY; PHYSIOLOGY; REVIEW;

ANTIMICROBIAL RESPONSE; INFECTION; INNATE IMMUNITY;

ANIMALS; HUMANS; IMMUNITY, INNATE; INFECTION; TOLL-LIKE RECEPTORS;

EID: 84907855804     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201344291     Document Type: Review

References (167)

1. Bianchi, M. E., DAMPs, PAMPs and alarmins: all we need to know about danger. J. Leukoc. Biol. 2007. 81: 1-5.
2. Chan, J. K., Roth, J., Oppenheim, J. J., Tracey, K. J., Vogl, T., Feldmann, M., Horwood, N. et al., Alarmins: awaiting a clinical response. J. Clin. Invest. 2012. 122: 2711-2719.
3. Stoecklein, V. M., Osuka, A. and Lederer, J. A., Trauma equals danger- damage control by the immune system. J. Leukoc. Biol. 2012. 92: 539-551.
4. Schelbergen, R. F., Blom, A. B., van den Bosch, M. H., Sloetjes, A., Abdollahi-Roodsaz, S., Schreurs, B. W., Mort, J. S. et al., Alarmins S100A8 and S100A9 elicit a catabolic effect in human osteoarthritic chondrocytes that is dependent on Toll-like receptor 4. Arthritis Rheum. 2012. 64: 1477-1487.
5. Paterson, H. M., Murphy, T. J., Purcell, E. J., Shelley, O., Kriynovich, S. J., Lien, E., Mannick, J. A. et al., Injury primes the innate immune system for enhanced Toll-like receptor reactivity. J. Immunol. 2003. 171: 1473-1483.
6. Li, G., Tang, D. and Lotze, M. T., Menage a Trois in stress: DAMPs, redox and autophagy. Semin. Cancer Biol. 2013. 23: 380-390.
7. Clark, S. R.,Ma, A. C., Tavener, S. A., McDonald, B., Goodarzi, Z., Kelly, M. M., Patel, K. D. et al., Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat. Med. 2007. 13: 463-469.
8. Fleming, A., On a remarkable bacteriolytic element found in tissues and secretions. Proc. R. Soc. Lond. B 1922. 93: 306-317.
9. McDermott, A. M., Antimicrobial compounds in tears. Exp. Eye Res. 2013. 117: 53-61.
10. Callewaert, L., Van Herreweghe, J. M., Vanderkelen, L., Leysen, S., Voet, A. and Michiels, C. W., Guards of the great wall: bacterial lysozyme inhibitors. Trends Microbiol. 2012. 20: 501-510.
11. Schroder, J. M., Antimicrobial peptides in healthy skin and atopic dermatitis. Allergol. Int. 2011. 60: 17-24.
12. Wilson, S. S., Wiens, M. E. and Smith, J. G., Antiviral mechanisms of human defensins. J. Mol. Biol. 2013. 425: 4965-4980.
13. Ghosh, D., Porter, E., Shen, B., Lee, S. K., Wilk, D., Drazba, J., Yadav, S. P. et al., Paneth cell trypsin is the processing enzyme for human defensin-5. Nat. Immunol. 2002. 3: 583-590.
14. Vandenbroucke, R. E., Vanlaere, I., Van Hauwermeiren, F., Van Wonterghem, E., Wilson, C. and Libert, C., Pro-inflammatory effects of matrix metalloproteinase 7 in acute inflammation. Mucosal Immunol. 2014. 7: 579-588.
15. Ayabe, T., Wulff, H., Darmoul, D., Cahalan, M. D., Chandy, K. G. and Ouellette, A. J., Modulation of mouse Paneth cell alpha-defensin secretion by mIKCa1, a Ca2+-activated, intermediate conductance potassium channel. J. Biol. Chem. 2002. 277: 3793-3800.
16. Zhao, C., Wang, I. and Lehrer, R. I., Widespread expression of betadefensin hBD-1 in human secretory glands and epithelial cells. FEBS Lett. 1996. 396: 319-322.
17. Kiatsurayanon, C., Niyonsaba, F., Smithrithee, R., Akiyama, T., Ushio, H., Hara, M., Okumura, K. et al., Host defense (antimicrobial) peptide, human beta-defensin-3, improves the function of the epithelial tight junction barrier in human keratinocytes. J. Invest. Dermatol. 2014. 134: 2163-2173.
18. Kahlenberg, J. M. and Kaplan, M. J., Little peptide, big effects: the role of LL-37 in inflammation and autoimmune disease. J. Immunol. 2013. 191: 4895-4901.
19. Dann, S. M. and Eckmann, L., Innate immune defenses in the intestinal tract. Curr. Opin. Gastroenterol. 2007. 23: 115-120.
20. Mukherjee, S., Zheng, H.,Derebe, M. G., Callenberg, K. M., Partch, C. L., Rollins, D., Propheter, D. C. et al., Antibacterial membrane attack by a pore-forming intestinal C-type lectin. Nature 2014. 505: 103-107.
21. Vaishnava, S., Yamamoto, M., Severson, K. M., Ruhn, K. A., Yu, X., Koren, O., Ley, R. et al., The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 2011. 334: 255-258.
22. Zhou, Z. H., Zhang, Y., Hu, Y. F.,Wahl, L. M., Cisar, J. O. and Notkins, A. L., The broad antibacterial activity of the natural antibody repertoire is due to polyreactive antibodies. Cell Host Microbe 2007. 1: 51-61.
23. van Gils, M. J. and Sanders, R. W., Broadly neutralizing antibodies against HIV-1: templates for a vaccine. Virology 2013. 435: 46-56.
24. Pabst, O., New concepts in the generation and functions of IgA. Nat. Rev. Immunol. 2012. 12: 821-832.
25. Campos-Rodriguez, R., Godinez-Victoria, M., Abarca-Rojano, E., Pacheco-Yepez, J., Reyna-Garfias, H., Barbosa-Cabrera, R. E. and Drago-Serrano, M. E., Stress modulates intestinal secretory immunoglobulin A. Front Integr. Neurosci. 2013. 7: 86. doi:10.3389/fnint.2013.00086.
26. Roy, B., Agarwal, S., Brennecke, A. M., Krey, M., Pabst, O., Duber, S. and Weiss, S., B-1-cell subpopulations contribute differently to gut immunity. Eur. J. Immunol. 2013. 43: 2023-2032.
27. Forbes, S. J., Eschmann, M. and Mantis, N. J., Inhibition of Salmonella enterica serovar typhimurium motility and entry into epithelial cells by a protective antilipopolysaccharide monoclonal immunoglobulin A antibody. Infect. Immun. 2008. 76: 4137-4144.
28. Forbes, S. J., Bumpus, T., McCarthy, E. A., Corthesy, B. and Mantis, N. J., Transient suppression of Shigella flexneri type 3 secretion by a protective O-antigen-specific monoclonal IgA. MBio 2011. 2: e00042-e00011.
29. Kadaoui, K. A. and Corthesy, B., Secretory IgA mediates bacterial translocation to dendritic cells in mouse Peyer's patches with restriction to mucosal compartment. J. Immunol. 2007. 179: 7751-7757.
30. Berin, M. C., Mucosal antibodies in the regulation of tolerance and allergy to foods. Semin. Immunopathol. 2012. 34: 633-642.
31. Ansar, W. and Ghosh, S., C-reactive protein and the biology of disease. Immunol. Res. 2013. 56: 131-142.
32. Pepys, M. B. and Hirschfield, G. M., C-reactive protein: a critical update. J. Clin. Invest. 2003. 111: 1805-1812.
33. Pangburn, M. K., Host recognition and target differentiation by factor H, a regulator of the alternative pathway of complement. Immunopharmacology 2000. 49: 149-157.
34. Nordahl, E. A., Rydengard, V., Nyberg, P., Nitsche, D. P., Morgelin, M., Malmsten, M., Bjorck, L. et al., Activation of the complement system generates antibacterial peptides. Proc. Natl. Acad. Sci. USA 2004. 101: 16879-16884.
35. Sonesson, A., Ringstad, L., Nordahl, E. A., Malmsten, M., Morgelin, M. and Schmidtchen, A., Antifungal activity of C3a and C3a-derived peptides against Candida. Biochim. Biophys. Acta 2007. 1768: 346-353.
36. Pasupuleti, M., Walse, B., Nordahl, E. A., Morgelin, M., Malmsten, M. and Schmidtchen, A., Preservation of antimicrobial properties of complement peptide C3a, from invertebrates to humans. J. Biol. Chem. 2007. 282: 2520-2528.
37. Tschopp, J., Podack, E. R. and Muller-Eberhard, H. J., Ultrastructure of the membrane attack complex of complement: detection of the tetramolecular C9-polymerizing complex C5b-8. Proc. Natl. Acad. Sci. USA 1982. 79: 7474-7478.
38. Bellamy, M. C., Gedney, J. A., Buglass, H. and Gooi, J. H., Complement membrane attack complex and hemodynamic changes during human orthotopic liver transplantation. Liver Transpl. 2004. 10: 273-278.
39. Lopez, J. A., Brennan, A. J., Whisstock, J. C., Voskoboinik, I. and Trapani, J. A., Protecting a serial killer: pathways for perforin trafficking and selfdefence ensure sequential target cell death. Trends Immunol. 2012. 33: 406-412.
40. Martinez, R. J. and Carroll, S. F., Sequential metabolic expressions of the lethal process in human serum-treated Escherichia coli: role of lysozyme. Infect. Immun. 1980. 28: 735-745.
41. Rosado, C. J., Kondos, S., Bull, T. E., Kuiper, M. J., Law, R. H., Buckle, A. M., Voskoboinik, I. et al., The MACPF/CDC family of pore-forming toxins. Cell Microbiol. 2008. 10: 1765-1774.
42. Raja, S. M.,Metkar, S. S., Honing, S., Wang, B., Russin, W. A., Pipalia, N. H., Menaa, C. et al., A novel mechanism for protein delivery: granzyme B undergoes electrostatic exchange from serglycin to target cells. J. Biol. Chem. 2005. 280: 20752-20761.
43. Tamang, D. L., Alves, B. N., Elliott, V., Redelman, D., Wadhwa, R., Fraser, S. A. and Hudig, D., Regulation of perforin lysis: implications for protein disulfide isomerase proteins. Cell Immunol. 2009. 255: 82-92.
44. Sullivan, D. P. and Muller, W. A., Neutrophil and monocyte recruitment by PECAM, CD99, and other molecules via the LBRC. Semin. Immunopathol. 2014. 36: 193-209.
45. Herter, J. and Zarbock, A., Integrin regulation during leukocyte recruitment. J. Immunol. 2013. 190: 4451-4457.
46. Ivetic, A., Signals regulating L-selectin-dependent leucocyte adhesion and transmigration. Int. J. Biochem. Cell Biol. 2013. 45: 550-555.
47. Underhill, D. M. and Goodridge, H. S., Information processing during phagocytosis. Nat. Rev. Immunol. 2012. 12: 492-502.
48. Moretti, J. and Blander, J. M., Insights into phagocytosis-coupled activation of pattern recognition receptors and inflammasomes. Curr. Opin. Immunol. 2014. 26: 100-110.
49. Bylund, J., Brown, K. L., Movitz, C., Dahlgren, C. and Karlsson, A., Intracellular generation of superoxide by the phagocyte NADPH oxidase: how, where, and what for? Free Radic. Biol. Med. 2010. 49: 1834-1845.
50. Martinez-Pomares, L., The mannose receptor. J. Leukoc. Biol. 2012. 92: 1177-1186.
51. Lu, J., Marjon, K. D., Mold, C., Du Clos, T. W. and Sun, P. D., Pentraxins and Fc receptors. Immunol. Rev. 2012. 250: 230-238.
52. Rabiet, M. J., Huet, E. and Boulay, F., The N-formyl peptide receptors and the anaphylatoxin C5a receptors: an overview. Biochimie 2007. 89: 1089-1106.
53. Byrne, M. B., Kimura, Y., Kapoor, A., He, Y., Mattam, K. S., Hasan, K. M., Olson, L. N. et al., Oscillatory behavior of neutrophils under opposing chemoattractant gradients supports a winner-take-all mechanism. PLoS One 2014. 9: e85726.
54. Migeotte, I., Communi, D. and Parmentier, M., Formyl peptide receptors: a promiscuous subfamily of G protein-coupled receptors controlling immune responses. Cytokine Growth Factor Rev. 2006. 17: 501-519.
55. Panaro, M. A., Acquafredda, A., Sisto, M., Lisi, S., Maffione, A. B. and Mitolo, V., Biological role of the N-formyl peptide receptors. Immunopharmacol. Immunotoxicol. 2006. 28: 103-127.
56. Lazzari, K. G., Proto, P. J. and Simons, E. R., Simultaneous measurement of stimulus-induced changes in cytoplasmic Ca2+ and in membrane potential of human neutrophils. J. Biol. Chem. 1986. 261: 9710-9713.
57. Su, S. B., Gong, W. H., Gao, J. L., Shen, W. P., Grimm, M. C., Deng, X., Murphy, P. M. et al., T20/DP178, an ectodomain peptide of human immunodeficiency virus type 1 gp41, is an activator of human phagocyte N-formyl peptide receptor. Blood 1999. 93: 3885-3892.
58. Betten, A., Bylund, J., Christophe, T., Boulay, F., Romero, A., Hellstrand, K. and Dahlgren, C., A proinflammatory peptide from Helicobacter pylori activates monocytes to induce lymphocyte dysfunction and apoptosis. J. Clin. Invest. 2001. 108: 1221-1228.
59. Bellner, L., Thoren, F., Nygren, E., Liljeqvist, J. A., Karlsson, A. and Eriksson, K., A proinflammatory peptide from herpes simplex virus type 2 glycoprotein G affects neutrophil, monocyte, and NK cell functions. J. Immunol. 2005. 174: 2235-2241.
60. Fiore, S., Maddox, J. F., Perez, H. D. and Serhan, C. N., Identification of a human cDNA encoding a functional high affinity lipoxin A4 receptor. J. Exp. Med. 1994. 180: 253-260.
61. Su, S. B., Gong, W., Gao, J. L., Shen,W., Murphy, P. M., Oppenheim, J. J. and Wang, J. M., A seven-transmembrane, G protein-coupled receptor, FPRL1, mediates the chemotactic activity of serum amyloid A for human phagocytic cells. J. Exp. Med. 1999. 189: 395-402.
62. Ying, G., Iribarren, P., Zhou, Y., Gong, W., Zhang, N., Yu, Z. X., Le, Y. et al., Humanin, a newly identified neuroprotective factor, uses the G protein-coupled formylpeptide receptor-like-1 as a functional receptor. J. Immunol. 2004. 172: 7078-7085.
63. De, Y., Chen, Q., Schmidt, A. P.,Anderson, G. M.,Wang, J. M., Wooters, J., Oppenheim, J. J. 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: 1069-1074.
64. Gao, J. L., Lee, E. J. and Murphy, P. M., Impaired antibacterial host defense in mice lacking the N-formylpeptide receptor. J. Exp. Med. 1999. 189: 657-662.
65. Gwinn, M. R., Sharma, A. and De Nardin, E., Single nucleotide polymorphisms of the N-formyl peptide receptor in localized juvenile periodontitis. J. Periodontol. 1999. 70: 1194-1201.
66. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., Weinrauch, Y. et al., Neutrophil extracellular traps kill bacteria. Science 2004. 303: 1532-1535.
67. Brinkmann, V. and Zychlinsky, A., Neutrophil extracellular traps: is immunity the second function of chromatin? J. Cell Biol. 2012. 198: 773- 783.
68. Yipp, B. G., Petri, B., Salina, D., Jenne, C. N., Scott, B. N., Zbytnuik, L. D., Pittman, K. et al., Infection-induced NETosis is a dynamic process involving neutrophilmultitasking in vivo. Nat. Med. 2012. 18: 1386-1393.
69. Amulic, B. and Hayes, G., Neutrophil extracellular traps. Curr. Biol. 2011. 21: R297-R298.
70. Buchanan, J. T., Simpson, A. J.,Aziz, R. K., Liu, G. Y., Kristian, S. A., Kotb, M., Feramisco, J. et al., DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr. Biol. 2006. 16: 396-400.
71. Berends, E. T., Horswill, A. R., Haste, N. M., Monestier, M., Nizet, V. and von Kockritz-Blickwede, M., Nuclease expression by Staphylococcus aureus facilitates escape from neutrophil extracellular traps. J. Innate Immun. 2010. 2: 576-586.
72. Arazna, M., Pruchniak, M. P. and Demkow, U., Neutrophil extracellular traps in bacterial infections: strategies for escaping from killing. Respir. Physiol. Neurobiol. 2013. 187: 74-77.
73. Fuchs, T. A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., Weinrauch, Y. et al., Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 2007. 176: 231-241.
74. Papayannopoulos, V., Metzler, K. D., Hakkim, A. and Zychlinsky, A., Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J. Cell Biol. 2010. 191: 677-691.
75. Byrd, A. S., O'Brien, X. M., Johnson, C. M., Lavigne, L. M. and Reichner, J. S., An extracellular matrix-based mechanism of rapid neutrophil extracellular trap formation in response to Candida albicans. J. Immunol. 2013. 190: 4136-4148.
76. Hakkim, A., Fuchs, T. A., Martinez, N. E., Hess, S., Prinz, H., Zychlinsky, A. and Waldmann, H., Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation. Nat. Chem. Biol. 2011. 7: 75-77.
77. Villanueva, E., Yalavarthi, S., Berthier, C. C., Hodgin, J. B., Khandpur, R., Lin, A. M., Rubin, C. J. et al., Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J. Immunol. 2011. 187: 538-552.
78. Dwivedi, N., Upadhyay, J., Neeli, I., Khan, S., Pattanaik, D., Myers, L., Kirou, K. A. et al., Felty's syndrome autoantibodies bind to deiminated histones and neutrophil extracellular chromatin traps. Arthritis Rheum. 2012. 64: 982-992.
79. Kessenbrock, K., Krumbholz, M., Schonermarck, U., Back, W., Gross, W. L., Werb, Z., Grone, H. J. et al., Netting neutrophils in autoimmune small-vessel vasculitis. Nat. Med. 2009. 15: 623-625.
80. Garcia-Romo, G. S., Caielli, S., Vega, B., Connolly, J., Allantaz, F., Xu, Z., Punaro, M. et al., Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci. Transl. Med. 2011. 3: 73ra20.
81. Mitroulis, I., Kambas, K., Chrysanthopoulou, A., Skendros, P., Apostolidou, E., Kourtzelis, I., Drosos, G. I. et al., Neutrophil extracellular trap formation is associated with IL-1beta and autophagy-related signaling in gout. PLoS One 2011. 6: e29318.
82. Doring, Y., Manthey, H. D., Drechsler, M., Lievens, D., Megens, R. T., Soehnlein, O., Busch, M. et al., Auto-antigenic protein-DNA complexes stimulate plasmacytoid dendritic cells to promote atherosclerosis. Circulation 2012. 125: 1673-1683.
83. Cui, B. B., Tan, C. Y., Schorn, C., Tang, H. H., Liu, Y. and Zhao, Y., Neutrophil extracellular traps in sterile inflammation: the story after dying? Autoimmunity 2012. 45: 593-596.
84. von Kockritz-Blickwede, M., Goldmann, O., Thulin, P., Heinemann, K., Norrby-Teglund, A., Rohde, M. and Medina, E., Phagocytosisindependent antimicrobial activity of mast cells by means of extracellular trap formation. Blood 2008. 111: 3070-3080.
85. Ueki, S., Melo, R. C., Ghiran, I., Spencer, L. A., Dvorak, A. M. and Weller, P. F., Eosinophil extracellular DNA trap cell death mediates lytic release of free secretion-competent eosinophil granules in humans. Blood 2013. 121: 2074-2083.
86. Imlay, J. A. and Linn, S., Bimodal pattern of killing of DNA-repairdefective or anoxically grown Escherichia coli by hydrogen peroxide. J. Bacteriol. 1986. 166: 519-527.
87. McCormick, M. L., Buettner, G. R. and Britigan, B. E., Endogenous superoxide dismutase levels regulate iron-dependent hydroxyl radical formation in Escherichia coli exposed to hydrogen peroxide. J. Bacteriol. 1998. 180: 622-625.
88. Tamarit, J., Cabiscol, E. and Ros, J., Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress. J. Biol. Chem. 1998. 273: 3027-3032.
89. Ramsey, I. S., Moran, M. M., Chong, J. A. and Clapham, D. E., A voltagegated proton-selective channel lacking the pore domain. Nature 2006. 440: 1213-1216.
90. Sasaki, M., Takagi, M. and Okamura, Y., A voltage sensor-domain protein is a voltage-gated proton channel. Science 2006. 312: 589-592.
91. Fang, F. C., Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2004. 2: 820-832.
92. Reeves, E. P., Lu, H., Jacobs, H. L., Messina, C. G., Bolsover, S., Gabella, G., Potma, E. O. et al., Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 2002. 416: 291-297.
93. Akaki, T., Tomioka, H., Shimizu, T., Dekio, S. and Sato, K., Comparative roles of free fatty acids with reactive nitrogen intermediates and reactive oxygen intermediates in expression of the anti-microbial activity of macrophages against Mycobacterium tuberculosis. Clin. Exp. Immunol. 2000. 121: 302-310.
94. Kaplan, S. S., Lancaster, J. R., Jr., Basford, R. E. and Simmons, R. L., Effect of nitric oxide on staphylococcal killing and interactive effect with superoxide. Infect. Immun. 1996. 64: 69-76.
95. Mastroeni, P., Vazquez-Torres, A., Fang, F. C., Xu, Y., Khan, S., Hormaeche, C. E. and Dougan, G., Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. II. Effects on microbial proliferation and host survival in vivo. J. Exp. Med. 2000. 192: 237-248.
96. Vazquez-Torres, A., Jones-Carson, J., Mastroeni, P., Ischiropoulos, H. and Fang, F. C., Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. I. Effects onmicrobial killing by activated peritoneal macrophages in vitro. J. Exp. Med. 2000. 192: 227-236.
97. Wink, D. A., Hanbauer, I., Krishna, M. C., DeGraff, W., Gamson, J. and Mitchell, J. B., Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc. Natl. Acad. Sci. USA 1993. 90: 9813-9817.
98. Songsungthong, W., Higgins, M. C., Rolan, H. G., Murphy, J. L. and Mecsas, J., ROS-inhibitory activity of YopE is required for full virulence of Yersinia in mice. Cell Microbiol. 2010. 12: 988-1001.
99. Kalesnikoff, J. and Galli, S. J., New developments in mast cell biology. Nat. Immunol. 2008. 9: 1215-1223.
100. Ali, H., Regulation of human mast cell and basophil function by anaphylatoxins C3a and C5a. Immunol. Lett. 2010. 128: 36-45.
101. Sato, T., Hongu, T., Sakamoto, M., Funakoshi, Y. and Kanaho, Y., Molecular mechanisms of N-formyl-methionyl-leucyl-phenylalanineinduced superoxide generation and degranulation in mouse neutrophils: phospholipase D is dispensable. Mol. Cell Biol. 2013. 33: 136-145.
102. Antonin, W., Fasshauer, D., Becker, S., Jahn, R. and Schneider, T. R., Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs. Nat. Struct. Biol. 2002. 9: 107-111.
103. Allen, R. C. and Stephens, J. T., Jr., Myeloperoxidase selectively binds and selectively kills microbes. Infect. Immun. 2011. 79: 474-485.
104. Canny, G. and Levy, O., Bactericidal/permeability-increasing protein (BPI) and BPI homologs at mucosal sites. Trends Immunol. 2008. 29: 541- 547.
105. Ferrante, A., Activation of neutrophils by interleukins-1 and -2 and tumor necrosis factors. Immunol. Ser. 1992. 57: 417-436.
106. Matsuguchi, T., Mast cells as critical effectors of host immune defense against Gram-negative bacteria. Curr. Med. Chem. 2012. 19: 1432-1442.
107. Corbin, B. D., Seeley, E. H., Raab, A., Feldmann, J., Miller, M. R., Torres, V. J., Anderson, K. L. et al., Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 2008. 319: 962-965.
108. Tani, K., Ogushi, F., Kido, H., Kawano, T., Kunori, Y., Kamimura, T., Cui, P. et al., Chymase is a potent chemoattractant for human monocytes and neutrophils. J. Leukoc. Biol. 2000. 67: 585-589.
109. Brzezinska, A. A., Johnson, J. L., Munafo, D. B., Ellis, B. A. and Catz, S. D., Signallingmechanisms for Toll-like receptor-activated neutrophil exocytosis: key roles for interleukin-1-receptor-associated kinase-4 and phosphatidylinositol 3-kinase but not Toll/IL-1 receptor (TIR) domaincontaining adaptor inducing IFN-beta (TRIF). Immunology 2009. 127: 386- 397.
110. Borst, O., Munzer, P., Schmid, E., Schmidt, E. M., Russo, A., Walker, B., Yang, W. et al., 1,25(OH)2 vitamin D3-dependent inhibition of platelet Ca2+ signaling and thrombus formation in klotho-deficient mice. Faseb J. 2014. 28: 2108-2119.
111. Sotnikov, I., Veremeyko, T., Starossom, S. C., Barteneva, N., Weiner, H. L. and Ponomarev, E. D., Platelets recognize brain-specific glycolipid structures, respond to neurovascular damage and promote neuroinflammation. PLoS One 2013. 8: e58979.
112. Curzen, N., Gurbel, P. A., Myat, A., Bhatt, D. L. and Redwood, S. R., What is the optimum adjunctive reperfusion strategy for primary percutaneous coronary intervention? Lancet 2013. 382: 633-643.
113. Fitzgerald, J. R., Foster, T. J. and Cox, D., The interaction of bacterial pathogens with platelets. Nat. Rev. Microbiol. 2006. 4: 445-457.
114. O'Brien, L., Kerrigan, S. W., Kaw, G., Hogan, M., Penades, J., Litt, D., Fitzgerald, D. J. et al., Multiplemechanisms for the activation of human platelet aggregation by Staphylococcus aureus: roles for the clumping factors ClfA and ClfB, the serine-aspartate repeat protein SdrE and protein A. Mol. Microbiol. 2002. 44: 1033-1044.
115. Yeaman, M. R., Platelets in defense against bacterial pathogens. Cell Mol. Life Sci. 2010. 67: 525-544.
116. Durr, M. and Peschel, A., Chemokinesmeet defensins: the merging concepts of chemoattractants and antimicrobial peptides in host defense. Infect. Immun. 2002. 70: 6515-6517.
117. Yeaman, M. R., Puentes, S. M., Norman, D. C. and Bayer, A. S., Partial characterization and staphylocidal activity of thrombin-induced platelet microbicidal protein. Infect. Immun. 1992. 60: 1202-1209.
118. Tang, Y. Q., Yeaman, M. R. and Selsted, M. E., Antimicrobial peptides from human platelets. Infect. Immun. 2002. 70: 6524-6533.
119. Yeaman, M. R. and Yount, N. Y., Unifying themes in host defence effector polypeptides. Nat. Rev. Microbiol. 2007. 5: 727-740.
120. Yeaman, M. R. and Yount, N. Y., Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 2003. 55: 27-55.
121. Schroder, K. and Tschopp, J., The inflammasomes. Cell 2010. 140: 821- 832.
122. Strowig, T., Henao-Mejia, J., Elinav, E. and Flavell, R., Inflammasomes in health and disease. Nature 2012. 481: 278-286.
123. Haasken, S. and Sutterwala, F. S., Damage control: management of cellular stress by the NLRP3 inflammasome. Eur. J. Immunol. 2013. 43: 2003-2005.
124. Allam, R., Darisipudi, M. N., Tschopp, J. and Anders, H. J., Histones trigger sterile inflammation by activating the NLRP3 inflammasome. Eur. J. Immunol. 2013. 43: 3336-3342.
125. Hoque, R., Farooq, A. and Mehal, W. Z., Sterile inflammation in the liver and pancreas. J. Gastroenterol. Hepatol. 2013. 28(Suppl 1): 61-67.
126. Kriegler, M., Perez, C., DeFay, K., Albert, I. and Lu, S. D., A novel form of TNF/cachectin is a cell surface cytotoxic transmembrane protein: ramifications for the complex physiology of TNF. Cell 1988. 53: 45-53.
127. Grell, M., Douni, E., Wajant, H., Lohden, M., Clauss, M., Maxeiner, B., Georgopoulos, S. et al., The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80 kDa tumor necrosis factor receptor. Cell 1995. 83: 793-802.
128. Fishman, M., Cytolytic activities of activated macrophages versus paraformaldehyde-fixed macrophages; soluble versus membraneassociated TNF. Cell Immunol. 1991. 137: 164-174.
129. Lazdins, J. K., Grell, M., Walker, M. R., Woods-Cook, K., Scheurich, P. and Pfizenmaier, K., Membrane tumor necrosis factor (TNF) induced cooperative signaling of TNFR60 and TNFR80 favors induction of cell death rather than virus production in HIV-infected T cells. J. Exp. Med. 1997. 185: 81-90.
130. Birkland, T. P., Sypek, J. P. andWyler, D. J., Soluble TNF andmembrane TNF expressed on CD4+ T lymphocytes differ in their ability to activate macrophage antileishmanial defense. J. Leukoc. Biol. 1992. 51: 296-299.
131. Andersson, U. and Tracey, K. J., Reflex principles of immunological homeostasis. Annu. Rev. Immunol. 2012. 30: 313-335.
132. Basbaum, A. I., Bautista, D. M., Scherrer, G. and Julius, D., Cellular and molecular mechanisms of pain. Cell 2009. 139: 267-284.
133. Buhner, S. and Schemann, M., Mast cell-nerve axis with a focus on the human gut. Biochim. Biophys. Acta 2012. 1822: 85-92.
134. De Jonge, F., De Laet, A., Van Nassauw, L., Brown, J. K., Miller, H. R., van Bogaert, P. P., Timmermans, J. P. et al., In vitro activation ofmurine DRG neurons by CGRP-mediated mucosal mast cell degranulation. Am. J. Physiol. Gastrointest. Liver Physiol. 2004. 287: G178-G191.
135. Gees, M., Owsianik, G., Nilius, B. and Voets, T., TRP channels. Compr. Physiol. 2012. 2: 563-608.
136. Julius, D., TRP channels and pain. Annu. Rev. Cell Dev. Biol. 2013. 29: 355-384.
137. Nilius, B. and Owsianik, G., The transient receptor potential family of ion channels. Genome Biol. 2011. 12: 218.
138. Devika, N. T. and Jaffar Ali, B. M., Analysing calcium dependent and independent regulation of eNOS in endothelium triggered by extracellular signalling events. Mol. Biosyst. 2013. 9: 2653-2664.
139. Tauseef, M., Knezevic, N., Chava, K. R., Smith, M., Sukriti, S., Gianaris, N., Obukhov, A. G. et al., TLR4 activation of TRPC6-dependent calcium signaling mediates endotoxin-induced lung vascular permeability and inflammation. J. Exp. Med. 2012. 209: 1953-1968.
140. Diogenes, A., Ferraz, C. C., Akopian, A. N., Henry, M. A. and Hargreaves, K. M., LPS sensitizes TRPV1 via activation of TLR4 in trigeminal sensory neurons. J. Dent. Res. 2011. 90: 759-764.
141. Zhong, Z., Zhai, Y., Liang, S., Mori, Y., Han, R., Sutterwala, F. S. andQiao, L., TRPM2 links oxidative stress to NLRP3 inflammasome activation. Nat. Commun. 2013. 4: 1611.
142. Meseguer, V., Alpizar, Y. A., Luis, E., Tajada, S., Denlinger, B., Fajardo, O., Manenschijn, J. A. et al., TRPA1 channels mediate acute neurogenic inflammation and pain produced by bacterial endotoxins. Nat. Commun. 2014. 5: 3125.
143. Picard, C., Casanova, J. L. and Puel, A., Infectious diseases in patients with IRAK-4, MyD88, NEMO, or IkappaBalpha deficiency. Clin. Microbiol. Rev. 2011. 24: 490-497.
144. Picard, C., von Bernuth, H., Ghandil, P., Chrabieh, M., Levy, O., Arkwright, P. D., McDonald, D. et al., Clinical features and outcome of patients with IRAK-4 and MyD88 deficiency. Medicine (Baltimore) 2010. 89: 403-425.
145. Conway, D. H., Dara, J., Bagashev, A. and Sullivan, K. E., Myeloid differentiation primary response gene 88 (MyD88) deficiency in a large kindred. J. Allergy Clin. Immunol. 2010. 126: 172-175.
146. Casanova, J. L., Abel, L. and Quintana-Murci, L., Human TLRs and IL-1Rs in host defense: natural insights from evolutionary, epidemiological, and clinical genetics. Annu. Rev. Immunol. 2011. 29: 447-491.
147. Hiemstra, P. S., Langeler, E., Compier, B., Keepers, Y., Leijh, P. C., van den Barselaar, M. T., Overbosch, D. et al., Complete and partial deficiencies of complement factor D in a Dutch family. J. Clin. Invest. 1989. 84: 1957-1961.
148. Schejbel, L., Rosenfeldt, V., Marquart, H., Valerius, N. H. and Garred, P., Properdin deficiency associated with recurrent otitis media and pneumonia, and identification of male carrier with Klinefelter syndrome. Clin. Immunol. 2009. 131: 456-462.
149. Ram, S., Lewis, L. A. and Rice, P. A., Infections of people with complement deficiencies and patients who have undergone splenectomy. Clin. Microbiol. Rev. 2010. 23: 740-780.
150. E, S. R., Falcao, D. A. and Isaac, L., Clinical aspects and molecular basis of primary deficiencies of complement component C3 and its regulatory proteins factor I and factor H. Scand J. Immunol. 2006. 63: 155-168.
151. Super, M., Thiel, S., Lu, J., Levinsky, R. J. and Turner, M. W., Association of low levels of mannan-binding protein with a common defect of opsonisation. Lancet 1989. 2: 1236-1239.
152. Summerfield, J. A., Ryder, S., Sumiya, M., Thursz, M., Gorchein, A., Monteil, M. A. and Turner, M. W., Mannose binding protein gene mutations associated with unusual and severe infections in adults. Lancet 1995. 345: 886-889.
153. Watkins, R. R., Yamshchikov, A. V., Lemonovich, T. L. and Salata, R. A., The role of vitamin D deficiency in sepsis and potential therapeutic implications. J. Infect. 2011. 63: 321-326.
154. Schrumpf, J. A., van Sterkenburg, M. A., Verhoosel, R. M., Zuyderduyn, S. and Hiemstra, P. S., Interleukin 13 exposure enhances vitamin D-mediated expression of the human cathelicidin antimicrobial peptide 18/LL-37 in bronchial epithelial cells. Infect. Immun. 2012. 80: 4485-4494.
155. Das, M., Tomar, N., Sreenivas, V., Gupta, N. and Goswami, R., Effect of vitamin D supplementation on cathelicidin, IFN-gamma, IL-4 and Th1/Th2 transcription factors in young healthy females. Eur. J. Clin. Nutr. 2014. 68: 338-343.
156. Liu, P. T., Stenger, S., Li, H., Wenzel, L., Tan, B. H., Krutzik, S. R., Ochoa, M. T. et al., Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 2006. 311: 1770-1773.
157. Kelly, P., Bajaj-Elliott, M., Katubulushi, M., Zulu, I., Poulsom, R., Feldman, R. A., Bevins, C. L. et al., Reduced gene expression of intestinal alpha-defensins predicts diarrhea in a cohort of African adults. J. Infect. Dis. 2006. 193: 1464-1470.
158. Wehkamp, J., Salzman, N. H., Porter, E., Nuding, S., Weichenthal, M., Petras, R. E., Shen, B. et al., Reduced Paneth cell alpha-defensins in ileal Crohn's disease. Proc. Natl. Acad. Sci. USA 2005. 102: 18129-18134.
159. Chen, Q. X., Lv, C., Huang, L. X., Cheng, B. L., Xie, G. H., Wu, S. J. and Fang, X. M., Genomic variations within DEFB1 are associated with the susceptibility to and the fatal outcome of severe sepsis in Chinese Han population. Genes Immun. 2007. 8: 439-443.
160. Jurevic, R. J., Bai, M., Chadwick, R. B., White, T. C. and Dale, B. A., Single-nucleotide polymorphisms (SNPs) in human beta-defensin 1: high-throughput SNP assays and association with Candida carriage in type I diabetics and nondiabetic controls. J. Clin. Microbiol. 2003. 41: 90- 96.
161. Prado-Montes de Oca, E., Velarde-Felix, J. S., Rios-Tostado, J. J., Picos-Cardenas, V. J. and Figuera, L. E., SNP 668C (-44) alters a NF-kappaB1 putative binding site in non-coding strand of human beta-defensin 1 (DEFB1) and is associated with lepromatous leprosy. Infect. Genet. Evol. 2009. 9: 617-625.
162. Braida, L., Boniotto, M., Pontillo, A., Tovo, P. A., Amoroso, A. and Crovella, S., A single-nucleotide polymorphism in the human beta-defensin 1 gene is associated with HIV-1 infection in Italian children. AIDS 2004. 18: 1598-1600.
163. Holland, S. M., Chronic granulomatous disease. Hematol. Oncol. Clin. North Am. 2013. 27: 89-99.
164. Ben-Ari, J., Wolach, O., Gavrieli, R. and Wolach, B., Infections associated with chronic granulomatous disease: linking genetics to phenotypic expression. Expert Rev. Anti Infect. Ther. 2012. 10: 881-894.
165. Kuhns, D. B., Alvord, W. G., Heller, T., Feld, J. J., Pike, K. M., Marciano, B. E., Uzel, G. et al., Residual NADPH oxidase and survival in chronic granulomatous disease. N. Engl. J. Med. 2010. 363: 2600-2610.
166. Metzler, K. D., Fuchs, T. A., Nauseef, W. M., Reumaux, D., Roesler, J., Schulze, I., Wahn, V. et al., Myeloperoxidase is required for neutrophil extracellular trap formation: implications for innate immunity. Blood 2011. 117: 953-959.
167. Yost, C. C., Cody, M. J., Harris, E. S., Thornton, N. L., McInturff, A. M., Martinez, M. L., Chandler, N. B. et al., Impaired neutrophil extracellular trap (NET) formation: a novel innate immune deficiency of human neonates. Blood 2009. 113: 6419-6427.