Innate Stat3-mediated induction of the antimicrobial protein Reg3γ is required for host defense against MRSA pneumonia

Journal of Experimental Medicine

Volumn 210, Issue 3, 2013, Pages 551-561

  Choi, Sun Mi ^a,b   McAleer, Jeremy P ^b   Zheng, Mingquan ^b   Pociask, Derek A ^b   Kaplan, Mark H ^c   Qin, Shulin ^d   Reinhart, Todd A ^d   Kolls, Jay K ^a,b  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; RECOMBINANT REGENERATING ISLET DERIVED 3 GAMMA; STAT3 PROTEIN; UNCLASSIFIED DRUG; GLYCOPROTEIN GP 130; IL6ST PROTEIN, MOUSE; INTERLEUKIN 6; LEUKEMIA INHIBITORY FACTOR; LIF PROTEIN, MOUSE; PROTEIN; REG3G PROTEIN, MOUSE; STAT3 PROTEIN, MOUSE;

ARTICLE; BACTERICIDAL ACTIVITY; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG ALVEOLUS EPITHELIUM; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS INFECTION; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; IMMUNOLOGY; INNATE IMMUNITY; LUNG; LYMPHOCYTE; MALE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOUSE; PHYSIOLOGY; STAPHYLOCOCCAL PNEUMONIA;

ANIMALS; CYTOKINE RECEPTOR GP130; IMMUNITY, INNATE; INTERLEUKIN-6; LEUKEMIA INHIBITORY FACTOR; LUNG; LYMPHOCYTES; MALE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICE; MICE, INBRED C57BL; PNEUMONIA, STAPHYLOCOCCAL; PROTEINS; STAT3 TRANSCRIPTION FACTOR;

MLCS; MLOWN;

EID: 84877628014     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20120260     Document Type: Article

References (31)

1. Bals, R., and P.S. Hiemstra. 2004. Innate immunity in the lung: how epithelial cells fight against respiratory pathogens. Eur. Respir. J. 23:327-333. http://dx.doi.org/10.1183/09031936.03.00098803
2. Cash, H.L., C.V. Whitham, and L.V. Hooper. 2006. Refolding, purification, and characterization of human and murine RegIII proteins expressed in Escherichia coli. Protein Expr. Purif. 48:151-159. http://dx.doi.org/10.1016/j.pep.2006.01.014
3. Cho, J.S., E.M. Pietras, N.C. Garcia, R.I. Ramos, D.M. Farzam, H.R. Monroe, J.E. Magorien, A. Blauvelt, J.K. Kolls, A.L. Cheung, et al. 2010. IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J. Clin. Invest. 120:1762-1773. http://dx.doi. org/10.1172/JCI40891
4. David, M.Z., and R.S. Daum. 2010. Community-associated methicillinresistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin. Microbiol. Rev. 23:616-687. http://dx.doi. org/10.1128/CMR.00081-09
5. Defres, S., C. Marwick, and D. Nathwani. 2009. MRSA as a cause of lung infection including airway infection, community-acquired pneumonia and hospital-acquired pneumonia. Eur. Respir. J. 34:1470-1476. http://dx.doi.org/10.1183/09031936.00122309
6. DeLeo, F.R., M. Otto, B.N. Kreiswirth, and H.F. Chambers. 2010. Community-associated meticillin-resistant Staphylococcus aureus. Lancet. 375:1557-1568. http://dx.doi.org/10.1016/S0140-6736(09)61999-1
7. Gennery, A.R., T.J. Flood, M. Abinun, and A.J. Cant. 2000. Bone marrow transplantation does not correct the hyper IgE syndrome. Bone Marrow Transplant. 25:1303-1305. http://dx.doi.org/10.1038/sj.bmt. 1702446
8. Goussetis, E., I. Peristeri, V. Kitra, J. Traeger-Synodinos, M. Theodosaki, K. Psarra, M. Kanariou, F. Tzortzatou-Stathopoulou, E. Petrakou, I. Fylaktou, et al. 2010. Successful long-term immunologic reconstitution by allogeneic hematopoietic stem cell transplantation cures patients with autosomal dominant hyper-IgE syndrome. J. Allergy Clin. Immunol. 126:392-394. http://dx.doi.org/10.1016/j.jaci.2010.05.005
9. Graham, P.L. III, S.X. Lin, and E.L. Larson. 2006. A U.S. populationbased survey of Staphylococcus aureus colonization. Ann. Intern. Med. 144: 318-325.
10. Heimall, J., A. Freeman, and S.M. Holland. 2010. Pathogenesis of hyper IgE syndrome. Clin. Rev. Allergy Immunol. 38:32-38. http://dx.doi.org/10.1007/s12016-009-8134-1
11. Klevens, R.M., M.A. Morrison, J. Nadle, S. Petit, K. Gershman, S. Ray, L.H. Harrison, R. Lynfield, G. Dumyati, J.M. Townes, et al; Active Bacterial Core surveillance (ABCs) MRSA Investigators. 2007. Invasive methicillin- resistant Staphylococcus aureus infections in the United States. JAMA. 298:1763-1771. http://dx.doi.org/10.1001/jama.298.15.1763
12. Kudva, A., E.V. Scheller, K.M. Robinson, C.R. Crowe, S.M. Choi, S.R. Slight, S.A. Khader, P.J. Dubin, R.I. Enelow, J.K. Kolls, and J.F. Alcorn. 2011. Influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice. J. Immunol. 186:1666-1674. http://dx.doi. org/10.4049/jimmunol.1002194
13. Kuehnert, M.J., D. Kruszon-Moran, H.A. Hill, G. McQuillan, S.K. McAllister, G. Fosheim, L.K. McDougal, J. Chaitram, B. Jensen, S.K. Fridkin, et al. 2006. Prevalence of Staphylococcus aureus nasal colonization in the United States, 2001-2002. J. Infect. Dis. 193:172-179. http:// dx.doi.org/10.1086/499632
14. Kuperman, D.A., C.C. Lewis, P.G. Woodruff, M.W. Rodriguez, Y.H. Yang, G.M. Dolganov, J.V. Fahy, and D.J. Erle. 2005. Dissecting asthma using focused transgenic modeling and functional genomics. J. Allergy Clin. Immunol. 116:305-311. http://dx.doi.org/10.1016/j.jaci.2005.03.024
15. Matsuzaki, Y., Y. Xu, M. Ikegami, V. Besnard, K.S. Park, W.M. Hull, S.E. Wert, and J.A. Whitsett. 2006. Stat3 is required for cytoprotection of the respiratory epithelium during adenoviral infection. J. Immunol. 177:527-537.
16. Miller, L.S., E.M. Pietras, L.H. Uricchio, K. Hirano, S. Rao, H. Lin, R.M. O'connell, Y. Iwakura, A.L. Cheung, G. Cheng, and R.L. Modlin. 2007. Inflammasome-mediated production of IL-1beta is required for neutrophil recruitment against Staphylococcus aureus in vivo. J. Immunol. 179:6933-6942.
17. Minegishi, Y., M. Saito, M. Nagasawa, H. Takada, T. Hara, S. Tsuchiya, K. Agematsu, M. Yamada, N. Kawamura, T. Ariga, et al. 2009. Molecular explanation for the contradiction between systemic Th17 defect and localized bacterial infection in hyper-IgE syndrome. J. Exp. Med. 206:1291-1301. http://dx.doi.org/10.1084/jem.20082767
18. Mukherjee, S., C.L. Partch, R.E. Lehotzky, C.V. Whitham, H. Chu, C.L. Bevins, K.H. Gardner, and L.V. Hooper. 2009. Regulation of C-type lectin antimicrobial activity by a flexible N-terminal prosegment. J. Biol. Chem. 284:4881-4888. http://dx.doi.org/10.1074/jbc. M808077200
19. Napolitano, L.M., M.E. Brunsvold, R.C. Reddy, and R.C. Hyzy. 2009. Community-acquired methicillin-resistant Staphylococcus aureus pneumonia and ARDS: 1-year follow-up. Chest. 136:1407-1412. http:// dx.doi.org/10.1378/chest.07-1511
20. Parker, D., and A. Prince. 2012. Immunopathogenesis of Staphylococcus aureus pulmonary infection. Semin. Immunopathol. 34:281-297. http://dx.doi. org/10.1007/s00281-011-0291-7
21. Pickert, G., C. Neufert, M. Leppkes, Y. Zheng, N. Wittkopf, M. Warntjen, H.A. Lehr, S. Hirth, B. Weigmann, S. Wirtz, et al. 2009. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J. Exp. Med. 206:1465-1472. http://dx.doi.org/10.1084/jem. 20082683
22. Quinton, L.J., M.R. Jones, B.E. Robson, B.T. Simms, J.A. Whitsett, and J.P. Mizgerd. 2008. Alveolar epithelial STAT3, IL-6 family cytokines, and host defense during Escherichia coli pneumonia. Am. J. Respir. Cell Mol. Biol. 38:699-706. http://dx.doi.org/10.1165/rcmb.2007- 0365OC
23. Randolph, A.G., F. Vaughn, R. Sullivan, L. Rubinson, B.T. Thompson, G. Yoon, E. Smoot, T.W. Rice, L.L. Loftis, M. Helfaer, et al; Pediatric Acute Lung Injury and Sepsis Investigator's Network and the National Heart, Lung, and Blood Institute ARDS Clinical Trials Network. 2011. Critically ill children during the 2009-2010 influenza pandemic in the United States. Pediatrics. 128:e1450-e1458. http://dx.doi.org/10.1542/peds.2011-0774
24. Reinhart, T.A., B.A. Fallert, M.E. Pfeifer, S. Sanghavi, S. Capuano III, P. Rajakumar, M. Murphey-Corb, R. Day, C.L. Fuller, and T.M. Schaefer. 2002. Increased expression of the inflammatory chemokine CXC chemokine ligand 9/monokine induced by interferon-gamma in lymphoid tissues of rhesus macaques during simian immunodeficiency virus infection and acquired immunodeficiency syndrome. Blood. 99:3119-3128. http://dx.doi.org/10.1182/blood.V99.9.3119
25. Skerrett, S.J., H.D. Liggitt, A.M. Hajjar, and C.B. Wilson. 2004. Cutting edge: myeloid differentiation factor 88 is essential for pulmonary host defense against Pseudomonas aeruginosa but not Staphylococcus aureus. J. Immunol. 172:3377-3381.
26. Small, C.L., S. McCormick, N. Gill, K. Kugathasan, M. Santosuosso, N. Donaldson, D.E. Heinrichs, A. Ashkar, and Z. Xing. 2008. NK cells play a critical protective role in host defense against acute extracellular Staphylococcus aureus bacterial infection in the lung. J. Immunol. 180:5558-5568.
27. Vaishnava, S., M. Yamamoto, K.M. Severson, K.A. Ruhn, X. Yu, O. Koren, R. Ley, E.K. Wakeland, and L.V. Hooper. 2011. The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science. 334:255-258. http://dx.doi.org/10.1126/science.1209791
28. von Köckritz-Blickwede, M., M. Rohde, S. Oehmcke, L.S. Miller, A.L. Cheung, H. Herwald, S. Foster, and E. Medina. 2008. Immunological mechanisms underlying the genetic predisposition to severe Staphylococcus aureus infection in the mouse model. Am. J. Pathol. 173:1657-1668. http://dx.doi.org/10.2353/ajpath.2008.080337
29. Xu, Y., M. Ikegami, Y. Wang, Y. Matsuzaki, and J.A. Whitsett. 2007. Gene expression and biological processes influenced by deletion of Stat3 in pulmonary type II epithelial cells. BMC Genomics. 8:455. http://dx.doi. org/10.1186/1471-2164-8-455
30. Yu, H., D. Pardoll, and R. Jove. 2009. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat. Rev. Cancer. 9:798-809. http://dx.doi.org/10.1038/nrc2734
31. Zheng, Y., P.A. Valdez, D.M. Danilenko, Y. Hu, S.M. Sa, Q. Gong, A.R. Abbas, Z. Modrusan, N. Ghilardi, F.J. de Sauvage, and W. Ouyang. 2008. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14:282-289. http://dx.doi.org/10.1038/nm1720