In vivo compartmental analysis of leukocytes in mouse lungs

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 309, Issue 7, 2015, Pages L639-L652

  Patel, Brijesh V ^a   Tatham, Kate C ^a   Wilson, Michael R ^a   O’Dea, Kieran P ^a   Takata, Masao ^a  

^a CHELSEA AND WESTMINSTER HOSPITAL   (United Kingdom)

Author keywords

Alveolus; Flow cytometry; Leukocyte trafficking; Lung interstitium; Pulmonary capillary vasculature

Indexed keywords

ANTIBODY; CD45 ANTIBODY; UNCLASSIFIED DRUG; CD45 ANTIGEN;

ACID ASPIRATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY LABELING; ARTICLE; CELL COMPARTMENTALIZATION; CELL POPULATION; CELL SUSPENSION; DENDRITIC CELL; FLOW CYTOMETRY; IN VIVO STUDY; LEUKOCYTE; LUNG ALVEOLUS; LUNG ALVEOLUS MACROPHAGE; LUNG BLOOD VESSEL; LUNG INJURY; LUNG INTERSTITIUM; MAJOR HISTOCOMPATIBILITY COMPLEX; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PHENOTYPE; PNEUMONIA; PRIORITY JOURNAL; RESPIRATORY AIRFLOW; ANIMAL; ASPIRATION PNEUMONIA; LUNG; METABOLISM; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; PROCEDURES; STAINING;

ANIMALS; ANTIBODIES; ANTIGENS, CD45; FLOW CYTOMETRY; LEUKOCYTES; LUNG; MICE; NEUTROPHIL INFILTRATION; PNEUMONIA, ASPIRATION; STAINING AND LABELING;

EID: 84943239011     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00140.2015     Document Type: Article

References (60)

1. Aggarwal NR, King LS, D’Alessio FR. Diverse macrophage populations mediate acute lung inflammation and resolution. Am J Physiol Lung Cell Mol Physiol 306: L709-L725, 2014.
2. Anderson KG, Mayer-Barber K, Sung H, Beura L, James BR, Taylor JJ, Qunaj L, Griffith TS, Vezys V, Barber DL, Masopust D. Intravascular staining for discrimination of vascular and tissue leukocytes. Nat Protoc 9: 209-222, 2014.
3. Aurrand-Lions M, Lamagna C, Dangerfield JP, Wang S, Herrera P, Nourshargh S, Imhof BA. Junctional adhesion molecule-C regulates the early influx of leukocytes into tissues during inflammation. J Immunol 174: 6406-6415, 2005.
4. Awad AS, Rouse M, Huang L, Vergis AL, Reutershan J, Cathro HP, Linden J, Okusa MD. Compartmentalization of neutrophils in the kidney and lung following acute ischemic kidney injury. Kidney Int 75: 689-698, 2009.
5. Barletta KE, Cagnina RE, Wallace KL, Ramos SI, Mehrad B, Linden J. Leukocyte compartments in the mouse lung: distinguishing between marginated, interstitial, and alveolar cells in response to injury. J Immunol Methods 375: 100-110, 2012.
6. Bedoret D, Wallemacq H, Marichal T, Desmet C, Quesada Calvo F, Henry E, Closset R, Dewals B, Thielen C, Gustin P, de Leval L, Van Rooijen N, Le Moine A, Vanderplasschen A, Cataldo D, Drion PV, Moser M, Lekeux P, Bureau F. Lung interstitial macrophages alter dendritic cell functions to prevent airway allergy in mice. J Clin Invest 119: 3723-3738, 2009.
7. Bozinovski S, Jones J, Beavitt SJ, Cook AD, Hamilton JA, Anderson GP. Innate immune responses to LPS in mouse lung are suppressed and reversed by neutralization of GM-CSF via repression of TLR-4. Am J Physiol Lung Cell Mol Physiol 286: L877-L885, 2004.
8. Chagnon F, Fournier C, Charette PG, Moleski L, Payet MD, Dobbs LG, Lesur O. In vivo intravital endoscopic confocal fluorescence microscopy of normal and acutely injured rat lungs. Lab Invest 90: 824-834, 2010.
9. Chatterjee S, Fujiwara K, Pérez NG, Ushio-Fukai M, Fisher AB. Mechanosignaling in the vasculature: emerging concepts in sensing, transduction and physiological responses. Am J Physiol Heart Circ Physiol 308: H1451-H1462, 2015.
10. Chatterjee S, Nieman GF, Christie JD, Fisher AB. Shear stress-related mechanosignaling with lung ischemia: lessons from basic research can inform lung transplantation. Am J Physiol Lung Cell Mol Physiol 307: L668-L680, 2014.
11. Crane MJ, Daley JM, van Houtte O, Brancato SK, Henry WL Jr, Albina JE. The monocyte to macrophage transition in the murine sterile wound. PLoS One 9: e86660, 2014.
12. D’Alessio FR, Tsushima K, Aggarwal NR, Mock JR, Eto Y, Garibaldi BT, Files DC, Avalos CR, Rodriguez JV, Waickman AT, Reddy SP, Pearse DB, Sidhaye VK, Hassoun PM, Crow MT, King LS. Resolution of experimental lung injury by monocyte-derived inducible nitric oxide synthase. J Immunol 189: 2234-2245, 2012.
13. D’Alessio FR, Tsushima K, Aggarwal NR, West EE, Willett MH, Britos MF, Pipeling MR, Brower RG, Tuder RM, McDyer JF, King LS. CD4+CD25+Foxp3+ Tregs resolve experimental lung injury in mice and are present in humans with acute lung injury. J Clin Invest 119: 2898-2913, 2009.
14. Daubeuf F, Frossard N. Performing bronchoalveolar lavage in the mouse. Curr Protoc Mouse Biol 2: 167-175, 2012.
15. Dengler V, Downey GP, Tuder RM, Eltzschig HK, Schmidt EP. Neutrophil intercellular communication in acute lung injury. Emerging roles of microparticles and gap junctions. Am J Respir Cell Mol Biol 49: 1-5, 2013.
16. Desch AN, Randolph GJ, Murphy K, Gautier EL, Kedl RM, Lahoud MH, Caminschi I, Shortman K, Henson PM, Jakubzick CV. CD103+ pulmonary dendritic cells preferentially acquire and present apoptotic cell-associated antigen. J Exp Med 208: 1789-1797, 2011.
17. Dhaliwal K, Scholefield E, Ferenbach D, Gibbons M, Duffin R, Dorward DA, Morris AC, Humphries D, MacKinnon A, Wilkinson TS, Wallace WA, van Rooijen N, Mack M, Rossi AG, Davidson DJ, Hirani N, Hughes J, Haslett C, Simpson AJ. Monocytes control secondphase neutrophil emigration in established lipopolysaccharide-induced murine lung injury. Am J Respir Crit Care Med 186: 514-524, 2012.
18. Dorr AD, Wilson MR, Wakabayashi K, Waite AC, Patel BV, van Rooijen N, O’Dea KP, Takata M. Sources of alveolar soluble TNF receptors during acute lung injury of different etiologies. J Appl Physiol 111: 177-184, 2011.
19. Duan M, Li WC, Vlahos R, Maxwell MJ, Anderson GP, Hibbs ML. Distinct macrophage subpopulations characterize acute infection and chronic inflammatory lung disease. J Immunol 189: 946-955, 2012.
20. Frank JA, Wray CM, McAuley DF, Schwendener R, Matthay MA. Alveolar macrophages contribute to alveolar barrier dysfunction in ventilator-induced lung injury. Am J Physiol Lung Cell Mol Physiol 291: L1191-L1198, 2006.
21. Gibbons MA, MacKinnon AC, Ramachandran P, Dhaliwal K, Duffin R, Phythian-Adams AT, van Rooijen N, Haslett C, Howie SE, Simpson AJ, Hirani N, Gauldie J, Iredale JP, Sethi T, Forbes SJ. Ly6Chi monocytes direct alternatively activated profibrotic macrophage regulation of lung fibrosis. Am J Respir Crit Care Med 184: 569-581, 2011.
22. Herzenberg LA, Tung J, Moore WA, Herzenberg LA, Parks DR. Interpreting flow cytometry data: a guide for the perplexed. Nat Immunol 7: 681-685, 2006.
23. Janssen WJ, Barthel L, Muldrow A, Oberley-Deegan RE, Kearns MT, Jakubzick C, Henson PM. Fas determines differential fates of resident and recruited macrophages during resolution of acute lung injury. Am J Respir Crit Care Med 184: 547-560, 2011.
24. Johnston LK, Rims CR, Gill SE, McGuire JK, Manicone AM. Pulmonary macrophage subpopulations in the induction and resolution of acute lung injury. Am J Respir Cell Mol Biol 47: 417-426, 2012.
25. Klesney-Tait J, Keck K, Li X, Gilfillan S, Otero K, Baruah S, Meyerholz DK, Varga SM, Knudson CJ, Moninger TO, Moreland J, Zabner J, Colonna M. Transepithelial migration of neutrophils into the lung requires TREM-1. J Clin Invest 123: 138-149, 2013.
26. 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 107: 18073-18078, 2010.
27. Kuebler WM, Parthasarathi K, Lindert J, Bhattacharya J. Real-time lung microscopy. J Appl Physiol 102: 1255-1264, 2007.
28. Lambrecht BN, Hammad H. Lung dendritic cells in respiratory viral infection and asthma: from protection to immunopathology. Annu Rev Immunol 30: 243-270, 2012.
29. Landsman L, Varol C, Jung S. Distinct differentiation potential of blood monocyte subsets in the lung. J Immunol 178: 2000-2007, 2007.
30. Leon B, Lopez-Bravo M, Ardavin C. Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 26: 519-531, 2007.
31. Manicone AM, Huizar I, McGuire JK. Matrilysin (matrix metalloproteinase-7) regulates anti-inflammatory and antifibrotic pulmonary dendritic cells that express CD103 (αεβ7-integrin). Am J Pathol 175: 2319-2331, 2009.
32. Maus UA, Janzen S, Wall G, Srivastava M, Blackwell TS, Christman JW, Seeger W, Welte T, Lohmeyer J. Resident alveolar macrophages are replaced by recruited monocytes in response to endotoxin-induced lung inflammation. Am J Respir Cell Mol Biol 35: 227-235, 2006.
33. Misharin AV, Morales-Nebreda L, Mutlu GM, Budinger GR, Perlman H. Flow cytometric analysis of macrophages and dendritic cell subsets in the mouse lung. Am J Respir Cell Mol Biol 49: 503-510, 2013.
34. Nelson DS, Boyden SV. The loss of macrophages from peritoneal exudates following the injection of antigens into guinea-pigs with delayedtype hypersensitivity. Immunology 6: 264-275, 1963.
35. Niedermeier M, Reich B, Rodriguez Gomez M, Denzel A, Schmidbauer K, Gobel N, Talke Y, Schweda F, Mack M. CD4+ T cells control the differentiation of Gr1+ monocytes into fibrocytes. Proc Natl Acad Sci USA 106: 17892-17897, 2009.
36. Noel J, Wang H, Hong N, Tao JQ, Yu K, Sorokina EM, Debolt K, Heayn M, Rizzo V, Delisser H, Fisher AB, Chatterjee S. PECAM-1 and caveolae form the mechanosensing complex necessary for NOX2 activation and angiogenic signaling with stopped flow in pulmonary endothelium. Am J Physiol Lung Cell Mol Physiol 305: L805-L818, 2013.
37. Nourshargh S, Alon R. Leukocyte migration into inflamed tissues. Immunity 41: 694-707, 2014.
38. Nourshargh S, Hordijk PL, Sixt M. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat Rev Mol Cell Biol 11: 366-378, 2010.
39. O’Dea KP, Dokpesi JO, Tatham KC, Wilson MR, Takata M. Regulation of monocyte subset proinflammatory responses within the lung microvasculature by the p38 MAPK/MK2 pathway. Am J Physiol Lung Cell Mol Physiol 301: L812-L821, 2011.
40. O’Dea KP, Wilson MR, Dokpesi JO, Wakabayashi K, Tatton L, van Rooijen N, Takata M. Mobilization and margination of bone marrow Gr-1high monocytes during subclinical endotoxemia predisposes the lungs toward acute injury. J Immunol 182: 1155-1166, 2009.
41. O’Dea KP, Young AJ, Yamamoto H, Robotham JL, Brennan FM, Takata M. Lung-marginated monocytes modulate pulmonary microvascular injury during early endotoxemia. Am J Respir Crit Care Med 172: 1119-1127, 2005.
42. Parks DR, Roederer M, Moore WA. A new “Logicle” display method avoids deceptive effects of logarithmic scaling for low signals and compensated data. Cytometry A 69: 541-551, 2006.
43. Patel BV, Wilson MR, O’Dea KP, Takata M. TNF-induced death signaling triggers alveolar epithelial dysfunction in acute lung injury. J Immunol 190: 4274-4282, 2013.
44. Patel BV, Wilson MR, Takata M. Resolution of acute lung injury and inflammation: a translational mouse model. Eur Respir J 39: 1162-1170, 2012.
45. Plantinga M, Guilliams M, Vanheerswynghels M, Deswarte K, Branco-Madeira F, Toussaint W, Vanhoutte L, Neyt K, Killeen N, Malissen B, Hammad H, Lambrecht BN. Conventional and monocytederived CD11b(+) dendritic cells initiate and maintain T helper 2 cellmediated immunity to house dust mite allergen. Immunity 38: 322-335, 2013.
46. Ramachandran P, Pellicoro A, Vernon MA, Boulter L, Aucott RL, Ali A, Hartland SN, Snowdon VK, Cappon A, Gordon-Walker TT, Williams MJ, Dunbar DR, Manning JR, van Rooijen N, Fallowfield JA, Forbes SJ, Iredale JP. Differential Ly-6C expression identifies the recruited macrophage phenotype, which orchestrates the regression of murine liver fibrosis. Proc Natl Acad Sci USA 109: E3186-E3195, 2012.
47. Reutershan J, Basit A, Galkina EV, Ley K. Sequential recruitment of neutrophils into lung and bronchoalveolar lavage fluid in LPS-induced acute lung injury. Am J Physiol Lung Cell Mol Physiol 289: L807-L815, 2005.
48. Rose S, Misharin A, Perlman H. A novel Ly6C/Ly6G-based strategy to analyze the mouse splenic myeloid compartment. Cytometry A 81: 343-350, 2012.
49. Schulz O, Jaensson E, Persson EK, Liu X, Worbs T, Agace WW, Pabst O. Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J Exp Med 206: 3101-3114, 2009.
50. Song C, Al-Mehdi AB, Fisher AB. An immediate endothelial cell signaling response to lung ischemia. Am J Physiol Lung Cell Mol Physiol 281: L993-L1000, 2001.
51. Soroosh P, Doherty TA, Duan W, Mehta AK, Choi H, Adams YF, Mikulski Z, Khorram N, Rosenthal P, Broide DH, Croft M. Lungresident tissue macrophages generate Foxp3+ regulatory T cells and promote airway tolerance. J Exp Med 210: 775-788, 2013.
52. Tabuchi A, Mertens M, Kuppe H, Pries AR, Kuebler WM. Intravital microscopy of the murine pulmonary microcirculation. J Appl Physiol 104: 338-346, 2008.
53. Taraszka KS, Higgins JM, Tan K, Mandelbrot DA, Wang JH, Brenner MB. Molecular basis for leukocyte integrin αεβ7 adhesion to epithelial (E)-cadherin. J Exp Med 191: 1555-1567, 2000.
54. Varol C, Landsman L, Fogg DK, Greenshtein L, Gildor B, Margalit R, Kalchenko V, Geissmann F, Jung S. Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J Exp Med 204: 171-180, 2007.
55. von Garnier C, Filgueira L, Wikstrom M, Smith M, Thomas JA, Strickland DH, Holt PG, Stumbles PA. Anatomical location determines the distribution and function of dendritic cells and other APCs in the respiratory tract. J Immunol 175: 1609-1618, 2005.
56. Wakabayashi K, Wilson MR, Tatham KC, O’Dea KP, Takata M. Volutrauma, but not atelectrauma, induces systemic cytokine production by lung-marginated monocytes. Crit Care Med 42: e49-e57, 2014.
57. Wilson MR, O’Dea KP, Zhang D, Shearman AD, van Rooijen N, Takata M. Role of lung-marginated monocytes in an in vivo mouse model of ventilator-induced lung injury. Am J Respir Crit Care Med 179: 914-922, 2009.
58. Zaynagetdinov R, Sherrill TP, Kendall PL, Segal BH, Weller KP, Tighe RM, Blackwell TS. Identification of myeloid cell subsets in murine lungs using flow cytometry. Am J Respir Cell Mol Biol 49: 180-189, 2013.
59. Zemans RL, Briones N, Campbell M, McClendon J, Young SK, Suzuki T, Yang IV, De Langhe S, Reynolds SD, Mason RJ, Kahn M, Henson PM, Colgan SP, Downey GP. Neutrophil transmigration triggers repair of the lung epithelium via beta-catenin signaling. Proc Natl Acad Sci USA 108: 15990-15995, 2011.
60. Zigmond E, Varol C, Farache J, Elmaliah E, Satpathy AT, Friedlander G, Mack M, Shpigel N, Boneca IG, Murphy KM, Shakhar G, Halpern Z, Jung S. Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 37: 1076-1090, 2012.