Neonatal pulmonary macrophage depletion coupled to defective mucus clearance increases susceptibility to pneumonia and alters pulmonary immune responses

American Journal of Respiratory Cell and Molecular Biology

Volumn 54, Issue 2, 2016, Pages 210-221

  Saini, Yogesh ^a,b   Wilkinson, Kristen J ^a   Terrell, Kristy A ^a   Burns, Kimberlie A ^a   Livraghi Butrico, Alessandra ^a   Doerschuk, Claire M ^a   O'Neal, Wanda K ^a   Boucher, Richard C ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

Airway inflammation; Airway mucus obstruction; Alveolar macrophages; Macrophage depletion; Sodium channel subunit transgenic mice

Indexed keywords

CYTOKINE; DIPHTHERIA TOXIN; LYSOZYME; LYSOZYME M; SODIUM CHANNEL; SODIUM CHANNEL BETA; UNCLASSIFIED DRUG; AUTACOID; DIPHTHERIA TOXIN FRAGMENT A; EPITHELIAL SODIUM CHANNEL; PEPTIDE FRAGMENT; PHOTOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; BACTERIAL PNEUMONIA; CONTROLLED STUDY; CYTOKINE RESPONSE; EMACIATION; GENE EXPRESSION; GENETIC MODEL; IMMUNE RESPONSE; LUNG LAVAGE; MACROPHAGE; MOUSE; MUCUS SECRETION; NEWBORN; NONHUMAN; PASTEURELLA PNEUMOTROPICA; PHENOTYPE; PNEUMONIA; TH1 CELL; TRANSGENE; ANIMAL; C57BL MOUSE; DISEASE MODEL; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; LUNG; METABOLISM; MICROBIOLOGY; MUCOCILIARY CLEARANCE; PASTEURELLOSIS; PATHOGENICITY; PROMOTER REGION; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; CYTOKINES; DIPHTHERIA TOXIN; DISEASE MODELS, ANIMAL; EPITHELIAL SODIUM CHANNELS; GENETIC PREDISPOSITION TO DISEASE; INFLAMMATION MEDIATORS; LUMINESCENT PROTEINS; LUNG; MACROPHAGES; MICE, INBRED C57BL; MICE, TRANSGENIC; MUCOCILIARY CLEARANCE; MURAMIDASE; PASTEURELLA INFECTIONS; PASTEURELLA PNEUMOTROPICA; PEPTIDE FRAGMENTS; PHENOTYPE; PNEUMONIA, BACTERIAL; PROMOTER REGIONS, GENETIC;

EID: 84963811866     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2014-0111OC     Document Type: Article

References (40)

1. Cheung DO, Halsey K, Speert DP. Role of pulmonary alveolar macrophages in defense of the lung against Pseudomonas aeruginosa. Infect Immun 2000;68:4585-4592.
2. Kooguchi K, Hashimoto S, Kobayashi A, Kitamura Y, Kudoh I, Wiener-Kronish J, Sawa T. Role of alveolar macrophages in initiation and regulation of inflammation in Pseudomonas aeruginosa pneumonia. Infect Immun 1998;66:3164-3169.
3. Hashimoto S, Pittet JF, Hong K, Folkesson H, Bagby G, Kobzik L, Frevert C, Watanabe K, Tsurufuji S, Wiener-Kronish J. Depletion of alveolar macrophages decreases neutrophil chemotaxis to Pseudomonas airspace infections. Am J Physiol 1996;270:L819-L828.
4. Hackett BP, Gitlin JD. Cell-specific expression of a Clara cell secretory protein-human growth hormone gene in the bronchiolar epithelium of transgenic mice. Proc Natl Acad Sci USA 1992;89:9079-9083.
5. + absorption produces cystic fibrosis-like lung disease in mice. Nat Med 2004;10:487-493.
6. Mall MA, Harkema JR, Trojanek JB, Treis D, Livraghi A, Schubert S, Zhou Z, Kreda SM, Tilley SL, Hudson EJ, et al. Development of chronic bronchitis and emphysema in β-epithelial Na+ channel-overexpressing mice. Am J Respir Crit Care Med 2008;177:730-742.
7. Livraghi-Butrico A, Kelly EJ, Klem ER, Dang H, Wolfgang MC, Boucher RC, Randell SH, O'Neal WK. Mucus clearance, MyD88-dependent and MyD88-independent immunity modulate lung susceptibility to spontaneous bacterial infection and inflammation. Mucosal Immunol 2012;5:397-408.
8. Trojanek JB, Cobos-Correa A, Diemer S, Kormann M, Schubert SC, Zhou-Suckow Z, Agrawal R, Duerr J, Wagner CJ, Schatterny J, et al. Airway mucus obstruction triggers macrophage activation and matrix metalloproteinase 12-dependent emphysema. Am J Respir Cell Mol Biol 2014;51:709-720.
9. Saini Y, Dang H, Livraghi-Butrico A, Kelly EJ, Jones LC, O'Neal WK, Boucher RC. Gene expression in whole lung and pulmonary macrophages reflects the dynamic pathology associated with airway surface dehydration. BMC Genomics 2014;15:726.
10. Kreisel D, Nava RG, Li W, Zinselmeyer BH, Wang B, Lai J, Pless R, Gelman AE, Krupnick AS, Miller MJ. In vivo two-photon imaging reveals monocyte-dependent neutrophil extravasation during pulmonary inflammation. Proc Natl Acad Sci USA 2010;107:18073-18078.
11. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Förster I. Conditional gene targeting in macrophages and granulocytes using LysMCre mice. Transgenic Res 1999;8:265-277.
12. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global doublefluorescent Cre reporter mouse. Genesis 2007;45:593-605.
13. Voehringer D, Liang HE, Locksley RM. Voehringer D, Liang HE, Locksley RM. Homeostasis and effector function of lymphopeniainduced "memory-like" T cells in constitutively T cell-depleted mice. J Immunol 2008;180:4742-4753.
14. + channeloverexpressing mice: role of TNF-alpha and IL-4Ralpha signaling, influence of neonatal development, and limited efficacy of glucocorticoid treatment. J Immunol 2009;182:4357-4367.
15. Livraghi-Butrico A, Grubb BR, Kelly EJ, Wilkinson KJ, Yang H, Geiser M, Randell SH, Boucher RC, O'Neal WK. Genetically determined heterogeneity of lung disease in a mouse model of airway mucus obstruction. Physiol Genomics 2012;44:470-484.
16. Byers DE, Holtzman MJ. Alternatively activated macrophages and airway disease. Chest 2011;140:768-774.
17. Hussell T, Bell TJ. Alveolar macrophages: plasticity in a tissue-specific context. Nat Rev Immunol 2014;14:81-93.
18. Burnett SH, Kershen EJ, Zhang J, Zeng L, Straley SC, Kaplan AM, Cohen DA. Conditional macrophage ablation in transgenic mice expressing a Fas-based suicide gene. J Leukoc Biol 2004;75:612-623.
19. Nakamura T, Abu-Dahab R, Menger MD, Schafer U, Vollmar B, Wada H, Lehr CM, Schafers HJ. Depletion of alveolar macrophages by clodronate-liposomes aggravates ischemia-reperfusion injury of the lung. J Heart Lung Transplant 2005;24:38-45.
20. Miyake Y, Kaise H, Isono K, Koseki H, Kohno K, Tanaka M. Protective role of macrophages in noninflammatory lung injury caused by selective ablation of alveolar epithelial type II Cells. J Immunol 2007;178:5001-5009.
21. Jakubzick C, Bogunovic M, Bonito AJ, Kuan EL, Merad M, Randolph GJ. Lymph-migrating, tissue-derived dendritic cells are minor constituents within steady-state lymph nodes. J Exp Med 2008;205:2839-2850.
22. Markart P, Faust N, Graf T, Na CL, Weaver TE, Akinbi HT. Comparison of the microbicidal and muramidase activities of mouse lysozyme M and P. Biochem J 2004;380:385-392.
23. Vannella KM, Barron L, Borthwick LA, Kindrachuk KN, Narasimhan PB, Hart KM, Thompson RW, White S, Cheever AW, Ramalingam TR, et al. Incomplete deletion of IL-4Ra by LysM (Cre) reveals distinct subsets of M2 macrophages controlling inflammation and fibrosis in chronic schistosomiasis. PLoS Pathog 2014;10:e1004372.
24. Gundra UM, Girgis NM, Ruckerl D, Jenkins S, Ward LN, Kurtz ZD, Wiens KE, Tang MS, Basu-Roy U, Mansukhani A, et al. Alternatively activated macrophages derived from monocytes and tissue macrophages are phenotypically and functionally distinct. Blood 2014;123:e110-e122.
25. Lee YG, Jeong JJ, Nyenhuis S, Berdyshev E, Chung S, Ranjan R, Karpurapu M, Deng J, Qian F, Kelly EA, et al. Recruited alveolar macrophages, in response to airway epithelial-derived monocyte chemoattractant protein 1/CCL2, regulate airway inflammation and remodeling in allergic asthma. Am J Respir Cell Mol Biol 2014;52:772-784.
26. Kambara K, Ohashi W, Tomita K, Takashina M, Fujisaka S, Hayashi R, Mori H, Tobe K, Hattori Y. In vivo depletion of CD206 M2 macrophages exaggerates lung injury in endotoxemic mice. Am J Pathol 2015;185:162-171.
27. Hohlbaum AM, Gregory MS, Ju ST, Marshak-Rothstein A. Fas ligand engagement of resident peritoneal macrophages in vivo induces apoptosis and the production of neutrophil chemotactic factors. J Immunol 2001;167:6217-6224.
28. Li MO, Sarkisian MR, Mehal WZ, Rakic P, Flavell RA. Phosphatidylserine receptor is required for clearance of apoptotic cells. Science 2003;302:1560-1563.
29. Mikazuki K, Hirasawa T, Chiba H, Takahashi K, Sakai Y, Ohhara S, Nenui H. Colonization pattern of Pasteurella pneumotropica in mice with latent pasteurellosis. Jikken Dobutsu 1994;43:375-379.
30. Hart ML, Mosier DA, Chapes SK. Toll-like receptor 4-positive macrophages protect mice from Pasteurella pneumotropica-induced pneumonia. Infect Immun 2003;71:663-670.
31. Ghoneim HE, Thomas PG, McCullers JA. Depletion of alveolar macrophages during influenza infection facilitates bacterial superinfections. J Immunol 2013;191:1250-1259.
32. Broug-Holub E, Toews GB, van Iwaarden JF, Strieter RM, Kunkel SL, Paine III R, Standiford TJ. Alveolar macrophages are required for protective pulmonary defenses in murine Klebsiella pneumonia: elimination of alveolar macrophages increases neutrophil recruitment but decreases bacterial clearance and survival. Infect Immun 1997;65:1139-1146.
33. Hautamaki RD, Kobayashi DK, Senior RM, Shapiro SD. Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science 1997;277:2002-2004.
34. Gehrig S, Duerr J, Weitnauer M, Wagner CJ, Graeber SY, Schatterny J, Hirtz S, Belaaouaj A, Dalpke AH, Schultz C, et al. Lack of neutrophil elastase reduces inflammation, mucus hypersecretion, and emphysema, but not mucus obstruction, in mice with cystic fibrosis-like lung disease. Am J Respir Crit Care Med 2014;189:1082-1092.
35. Stockley RA. Neutrophils and the pathogenesis of COPD. Chest 2002;121 (5 suppl) 151S-155S.
36. Tetley TD. Macrophages and the pathogenesis of COPD. Chest 2002;121 (5 suppl) 156S-159S.
37. Lee JJ, McGarry MP, Farmer SC, Denzler KL, Larson KA, Carrigan PE, Brenneise IE, Horton MA, Haczku A, Gelfand EW, et al. Interleukin-5 expression in the lung epithelium of transgenic mice leads to pulmonary changes pathognomonic of asthma. J Exp Med 1997;185:2143-2156.
38. Pelletier M, Maggi L, Micheletti A, Lazzeri E, Tamassia N, Costantini C, Cosmi L, Lunardi C, Annunziato F, Romagnani S, et al. Evidence for a cross-talk between human neutrophils and Th17 cells. Blood 2010;115:335-343.
39. Mathie SA, Dixon KL, Walker SA, Tyrrell V, Mondhe M, O'Donnell VB, Gregory LG, Lloyd CM. Alveolar macrophages are sentinels of murine pulmonary homeostasis following inhaled antigen challenge. Allergy 2015;70:80-89.
40. Zaslona Z, Przybranowski S, Wilke C, van Rooijen N, Teitz-Tennenbaum S, Osterholzer JJ, Wilkinson JE, Moore BB, Peters-Golden M. Resident alveolar macrophages suppress, whereas recruited monocytes promote, allergic lung inflammation in murine models of asthma. J Immunol 2014;193:4245-4253.