Interleukin-33 Increases Antibacterial Defense by Activation of Inducible Nitric Oxide Synthase in Skin

PLoS Pathogens

Volumn 10, Issue 2, 2014, Pages

  Li, Changwei ^a   Li, Hongquan ^a   Jiang, Ziwei ^a   Zhang, Tian ^a   Wang, Yue ^a   Li, Zhiheng ^a   Wu, Yelin ^a   Ji, Shizhao ^b   Xiao, Shichu ^b   Ryffel, Bernhard ^c   Radek, Katherine A ^d   Xia, Zhaofan ^b   Lai, Yuping ^a  

^a EAST CHINA NORMAL UNIVERSITY   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c UNIVERSITÉ D'ORLÉANS   (France)

^d LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 33; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE SYNTHASE; PROTEIN KINASE B; STAT3 PROTEIN; TOLL LIKE RECEPTOR 2;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; CELL STIMULATION; CONTROLLED STUDY; GENE SILENCING; HOST RESISTANCE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKIN INFECTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; HUMANS; INTERLEUKINS; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE II; REAL-TIME POLYMERASE CHAIN REACTION; SKIN; STAPHYLOCOCCAL SKIN INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84895767962     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003918     Document Type: Article

References (48)

1. Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, et al. (2005) IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23: 479-490.
2. Carriere V, Roussel L, Ortega N, Lacorre DA, Americh L, et al. (2007) IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo. Proc Natl Acad Sci U S A 104: 282-287.
3. Roussel L, Erard M, Cayrol C, Girard JP, (2008) Molecular mimicry between IL-33 and KSHV for attachment to chromatin through the H2A-H2B acidic pocket. EMBO Rep 9: 1006-1012.
4. Moussion C, Ortega N, Girard JP, (2008) The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: a novel 'alarmin'? PLoS One 3: e3331.
5. Cayrol C, Girard JP, (2009) The IL-1-like cytokine IL-33 is inactivated after maturation by caspase-1. Proc Natl Acad Sci U S A 106: 9021-9026.
6. Luthi AU, Cullen SP, McNeela EA, Duriez PJ, Afonina IS, et al. (2009) Suppression of interleukin-33 bioactivity through proteolysis by apoptotic caspases. Immunity 31: 84-98.
7. Ali S, Huber M, Kollewe C, Bischoff SC, Falk W, et al. (2007) IL-1 receptor accessory protein is essential for IL-33-induced activation of T lymphocytes and mast cells. Proc Natl Acad Sci U S A 104: 18660-18665.
8. Allakhverdi Z, Smith DE, Comeau MR, Delespesse G, (2007) Cutting edge: The ST2 ligand IL-33 potently activates and drives maturation of human mast cells. J Immunol 179: 2051-2054.
9. Liew FY, Pitman NI, McInnes IB, (2010) Disease-associated functions of IL-33: the new kid in the IL-1 family. Nat Rev Immunol 10: 103-110.
10. Mirchandani AS, Salmond RJ, Liew FY, (2012) Interleukin-33 and the function of innate lymphoid cells. Trends Immunol 33: 389-396.
11. Yasuda K, Muto T, Kawagoe T, Matsumoto M, Sasaki Y, et al. (2012) Contribution of IL-33-activated type II innate lymphoid cells to pulmonary eosinophilia in intestinal nematode-infected mice. Proc Natl Acad Sci U S A 109: 3451-3456.
12. Yin H, Li X, Hu S, Liu T, Yuan B, et al. (2013) IL-33 promotes Staphylococcus aureus-infected wound healing in mice. Int Immunopharmacol 17: 432-438.
13. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, et al. (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298: 1763-1771.
14. Miller LS, Cho JS, (2011) Immunity against Staphylococcus aureus cutaneous infections. Nat Rev Immunol 11: 505-518.
15. Cho JS, Pietras EM, Garcia NC, Ramos RI, Farzam DM, et al. (2010) IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J Clin Invest 120: 1762-1773.
16. Olaru F, Jensen LE, (2010) Staphylococcus aureus stimulates neutrophil targeting chemokine expression in keratinocytes through an autocrine IL-1alpha signaling loop. J Invest Dermatol 130: 1866-1876.
17. Kinoshita M, Miyazaki H, Ono S, Inatsu A, Nakashima H, et al. (2011) Enhancement of neutrophil function by interleukin-18 therapy protects burn-injured mice from methicillin-resistant Staphylococcus aureus. Infect Immun 79: 2670-2680.
18. Humphreys NE, Xu D, Hepworth MR, Liew FY, Grencis RK, (2008) IL-33, a potent inducer of adaptive immunity to intestinal nematodes. J Immunol 180: 2443-2449.
19. Corbett JA, McDaniel ML, (1995) Intraislet release of interleukin 1 inhibits beta cell function by inducing beta cell expression of inducible nitric oxide synthase. J Exp Med 181: 559-568.
20. Kanno K, Hirata Y, Imai T, Iwashina M, Marumo F, (1994) Regulation of inducible nitric oxide synthase gene by interleukin-1 beta in rat vascular endothelial cells. Am J Physiol 267: H2318-2324.
21. Choi YS, Choi HJ, Min JK, Pyun BJ, Maeng YS, et al. (2009) Interleukin-33 induces angiogenesis and vascular permeability through ST2/TRAF6-mediated endothelial nitric oxide production. Blood 114: 3117-3126.
22. Beckerman KP, Rogers HW, Corbett JA, Schreiber RD, McDaniel ML, et al. (1993) Release of nitric oxide during the T cell-independent pathway of macrophage activation. Its role in resistance to Listeria monocytogenes. J Immunol 150: 888-895.
23. Green SJ, Meltzer MS, Hibbs JB Jr, Nacy CA, (1990) Activated macrophages destroy intracellular Leishmania major amastigotes by an L-arginine-dependent killing mechanism. J Immunol 144: 278-283.
24. Ormerod AD, Shah AA, Li H, Benjamin NB, Ferguson GP, et al. (2011) An observational prospective study of topical acidified nitrite for killing methicillin-resistant Staphylococcus aureus (MRSA) in contaminated wounds. BMC Res Notes 4: 458.
25. Foster TJ, (2005) Immune evasion by staphylococci. Nat Rev Microbiol 3: 948-958.
26. Silva MT, (2010) When two is better than one: macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system. J Leukoc Biol 87: 93-106.
27. Borregaard N, Cowland JB, (1997) Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 89: 3503-3521.
28. Segal AW, (2005) How neutrophils kill microbes. Annu Rev Immunol 23: 197-223.
29. Silva MT, Correia-Neves M, (2012) Neutrophils and macrophages: the main partners of phagocyte cell systems. Front Immunol 3: 174.
30. Carta S, Lavieri R, Rubartelli A, (2013) Different Members of the IL-1 Family Come Out in Different Ways: DAMPs vs. Cytokines? Front Immunol 4: 123.
31. Kouzaki H, Iijima K, Kobayashi T, O'Grady SM, Kita H, (2011) The danger signal, extracellular ATP, is a sensor for an airborne allergen and triggers IL-33 release and innate Th2-type responses. J Immunol 186: 4375-4387.
32. Lefrancais E, Roga S, Gautier V, Gonzalez-de-Peredo A, Monsarrat B, et al. (2012) IL-33 is processed into mature bioactive forms by neutrophil elastase and cathepsin G. Proc Natl Acad Sci U S A 109: 1673-1678.
33. Kurowska-Stolarska M, Kewin P, Murphy G, Russo RC, Stolarski B, et al. (2008) IL-33 induces antigen-specific IL-5+ T cells and promotes allergic-induced airway inflammation independent of IL-4. J Immunol 181: 4780-4790.
34. Alves-Filho JC, Sonego F, Souto FO, Freitas A, Verri WA Jr, et al. (2010) Interleukin-33 attenuates sepsis by enhancing neutrophil influx to the site of infection. Nat Med 16: 708-712.
35. Pushparaj PN, Tay HK, H'Ng SC, Pitman N, Xu D, et al. (2009) The cytokine interleukin-33 mediates anaphylactic shock. Proc Natl Acad Sci U S A 106: 9773-9778.
36. Ghaffari A, Jalili R, Ghaffari M, Miller C, Ghahary A, (2007) Efficacy of gaseous nitric oxide in the treatment of skin and soft tissue infections. Wound Repair Regen 15: 368-377.
37. Ghaffari A, Miller CC, McMullin B, Ghahary A, (2006) Potential application of gaseous nitric oxide as a topical antimicrobial agent. Nitric Oxide 14: 21-29.
38. Wang R, Ghahary A, Shen YJ, Scott PG, Tredget EE, (1996) Human dermal fibroblasts produce nitric oxide and express both constitutive and inducible nitric oxide synthase isoforms. J Invest Dermatol 106: 419-427.
39. Mannick JB, Asano K, Izumi K, Kieff E, Stamler JS, (1994) Nitric oxide produced by human B lymphocytes inhibits apoptosis and Epstein-Barr virus reactivation. Cell 79: 1137-1146.
40. Xie QW, Cho HJ, Calaycay J, Mumford RA, Swiderek KM, et al. (1992) Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 256: 225-228.
41. Vouldoukis I, Riveros-Moreno V, Dugas B, Ouaaz F, Becherel P, et al. (1995) The killing of Leishmania major by human macrophages is mediated by nitric oxide induced after ligation of the Fc epsilon RII/CD23 surface antigen. Proc Natl Acad Sci U S A 92: 7804-7808.
42. MacMicking J, Xie QW, Nathan C, (1997) Nitric oxide and macrophage function. Annu Rev Immunol 15: 323-350.
43. Gong K, Zhou F, Huang H, Gong Y, Zhang L, (2012) Suppression of GSK3beta by ERK mediates lipopolysaccharide induced cell migration in macrophage through beta-catenin signaling. Protein Cell 3: 762-768.
44. Lai Y, Di Nardo A, Nakatsuji T, Leichtle A, Yang Y, et al. (2009) Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat Med 15: 1377-1382.
45. Lai Y, Li D, Li C, Muehleisen B, Radek KA, et al. (2012) The antimicrobial protein REG3A regulates keratinocyte proliferation and differentiation after skin injury. Immunity 37: 74-84.
46. Weischenfeldt J, Porse B, (2008) Bone Marrow-Derived Macrophages (BMM): Isolation and Applications. CSH Protoc 2008pdb prot5080.
47. Dykhuizen RS, Frazer R, Duncan C, Smith CC, Golden M, et al. (1996) Antimicrobial effect of acidified nitrite on gut pathogens: importance of dietary nitrate in host defense. Antimicrob Agents Chemother 40: 1422-1425.
48. Hucker GJ, (1921) A New Modification and Application of the Gram Stain. J Bacteriol 6: 395-397.