Resident alveolar macrophages suppress, whereas recruited monocytes promote, allergic lung inflammation in murine models of asthma

Journal of Immunology

Volumn 193, Issue 8, 2014, Pages 4245-4253

  Zasłona, Zbigniew ^a   Przybranowski, Sally ^a   Wilke, Carol ^a   Van Rooijen, Nico ^b   Teitz Tennenbaum, Seagal ^a,c   Osterholzer, John J ^a,c   Wilkinson, John E ^a   Moore, Bethany B ^a   Peters Golden, Marc ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD45 ANTIGEN; CLODRONIC ACID; CYTOKINE; KI 67 ANTIGEN; OVALBUMIN; ALLERGEN; LY ANTIGEN; LY-6C ANTIGEN, MOUSE; PTPRC PROTEIN, MOUSE;

ACUTE DISEASE; ALLERGIC ASTHMA; ALLERGIC PNEUMONITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CHIMERA; CONTROLLED STUDY; DISEASE COURSE; EOSINOPHIL COUNT; HISTOPATHOLOGY; HOUSE DUST ALLERGY; IMMUNOPATHOGENESIS; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; MACROPHAGE FUNCTION; MONOCYTE; MOUSE; NONHUMAN; OVALBUMIN-INDUCED AIRWAY INFLAMMATION; ANIMAL; ASTHMA; BIOSYNTHESIS; C57BL MOUSE; CYTOLOGY; DISEASE MODEL; EOSINOPHIL; GENETICS; IMMUNOLOGY; INFLAMMATION; LUNG; PATHOLOGY; PNEUMONIA; PYROGLYPHIDAE;

ALLERGENS; ALVEOLITIS, EXTRINSIC ALLERGIC; ANIMALS; ANTIGENS, CD11B; ANTIGENS, CD45; ANTIGENS, LY; ASTHMA; BRONCHOALVEOLAR LAVAGE FLUID; CELL PROLIFERATION; CLODRONIC ACID; CYTOKINES; DISEASE MODELS, ANIMAL; EOSINOPHILS; INFLAMMATION; LUNG; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED C57BL; MONOCYTES; OVALBUMIN; PNEUMONIA; PYROGLYPHIDAE;

EID: 84907485553     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400580     Document Type: Article

References (57)

1. Bousquet, J., E. Mantzouranis, A. A. Cruz, N. Aït-Khaled, C. E. Baena-Cagnani, E. R. Bleecker, C. E. Brightling, P. Burney, A. Bush, W. W. Busse, et al. 2010. Uniform definition of asthma severity, control, and exacerbations: document presented for the World Health Organization Consultation on Severe Asthma. J. Allergy Clin. Immunol. 126: 926-938.
2. Holt, P. G. 1986. Down-regulation of immune responses in the lower respiratory tract: the role of alveolar macrophages. Clin. Exp. Immunol. 63: 261-270.
3. Sibille, Y., and H. Y. Reynolds. 1990. Macrophages and polymorphonuclear neutrophils in lung defense and injury. Am. Rev. Respir. Dis. 141: 471-501.
4. Peters-Golden, M. 2004. The alveolar macrophage: the forgotten cell in asthma. Am. J. Respir. Cell Mol. Biol. 31: 3-7.
5. Upham, J. W., D. H. Strickland, N. Bilyk, B. W. Robinson, and P. G. Holt. 1995. Alveolar macrophages from humans and rodents selectively inhibit T-cell proliferation but permit T-cell activation and cytokine secretion. Immunology 84: 142-147.
6. Holt, P. G., J. Oliver, N. Bilyk, C. McMenamin, P. G. McMenamin, G. Kraal, and T. Thepen. 1993. Downregulation of the antigen presenting cell function(s) of pulmonary dendritic cells in vivo by resident alveolar macrophages. J. Exp. Med. 177: 397-407.
7. Careau, E., and E. Y. Bissonnette. 2004. Adoptive transfer of alveolar macrophages abrogates bronchial hyperresponsiveness. Am. J. Respir. Cell Mol. Biol. 31: 22-27.
8. Thepen, T., N. Van Rooijen, and G. Kraal. 1989. Alveolar macrophage elimination in vivo is associated with an increase in pulmonary immune response in mice. J. Exp. Med. 170: 499-509.
9. Nagarkar, D. R., E. R. Bowman, D. Schneider, Q. Wang, J. Shim, Y. Zhao, M. J. Linn, C. L. McHenry, B. Gosangi, J. K. Bentley, et al. 2010. Rhinovirus infection of allergen-sensitized and -challenged mice induces eotaxin release from functionally polarized macrophages. J. Immunol. 185: 2525-2535.
10. Kurowska-Stolarska, M., B. Stolarski, P. Kewin, G. Murphy, C. J. Corrigan, S. Ying, N. Pitman, A. Mirchandani, B. Rana, N. van Rooijen, et al. 2009. IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. J. Immunol. 183: 6469-6477.
11. Tang, C., M. D. Inman, N. van Rooijen, P. Yang, H. Shen, K. Matsumoto, and P. M. O'Byrne. 2001. Th type 1-stimulating activity of lung macrophages inhibits Th2-mediated allergic airway inflammation by an IFN-gamma-dependent mechanism. J. Immunol. 166: 1471-1481.
12. Mathias, L. J., S. M. Khong, L. Spyroglou, N. L. Payne, C. Siatskas, A. N. Thorburn, R. L. Boyd, and T. S. Heng. 2013. Alveolar macrophages are critical for the inhibition of allergic asthma by mesenchymal stromal cells. J. Immunol. 191: 5914-5924.
13. Serbina, N. V., T. Jia, T. M. Hohl, and E. G. Pamer. 2008. Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 26: 421-452.
14. Stumm, C. L., S. H. Wettlaufer, S. Jancar, and M. Peters-Golden. 2011. Airway remodeling in murine asthma correlates with a defect in PGE2 synthesis by lung fibroblasts. Am. J. Physiol. Lung Cell. Mol. Physiol. 301: L636-L644.
15. Zaslona, Z., K. Okunishi, E. Bourdonnay, R. Domingo-Gonzalez, B. B. Moore, N. W. Lukacs, D. M. Aronoff, and M. Peters-Golden. 2013. Prostaglandin E suppresses allergic sensitization and lung inflammation by targeting the E prostanoid 2 receptor on T cells. J. Allergy Clin. Immunol. 133: 379-387.
16. van Rooijen, N., and E. van Kesteren-Hendrikx. 2003. "In vivo" depletion of macrophages by liposome-mediated "suicide". Methods Enzymol. 373: 3-16.
17. Zecher, D., N. van Rooijen, D. M. Rothstein, W. D. Shlomchik, and F. G. Lakkis. 2009. An innate response to allogeneic nonself mediated by monocytes. J. Immunol. 183: 7810-7816.
18. Tacke, F., F. Ginhoux, C. Jakubzick, N. van Rooijen, M. Merad, and G. J. Randolph. 2006. Immature monocytes acquire antigens from other cells in the bone marrow and present them to T cells after maturing in the periphery. J. Exp. Med. 203: 583-597.
19. Moore, B. B., M. J. Coffey, P. Christensen, S. Sitterding, R. Ngan, C. A. Wilke, R. McDonald, S. M. Phare, M. Peters-Golden, R. Paine, III, and G. B. Toews. 2000. GM-CSF regulates bleomycin-induced pulmonary fibrosis via a prostaglandin- dependent mechanism. J. Immunol. 165: 4032-4039.
20. Zasłona, Z., J. Wilhelm, L. Cakarova, L. M. Marsh, W. Seeger, J. Lohmeyer, and W. von Wulffen. 2009. Transcriptome profiling of primary murine monocytes, lung macrophages and lung dendritic cells reveals a distinct expression of genes involved in cell trafficking. Respir. Res. 10: 2.
21. Soroosh, P., T. A. Doherty, W. Duan, A. K. Mehta, H. Choi, Y. F. Adams, Z. Mikulski, N. Khorram, P. Rosenthal, D. H. Broide, and M. Croft. 2013. Lungresident tissue macrophages generate Foxp3+ regulatory T cells and promote airway tolerance. J. Exp. Med. 210: 775-788.
22. Landsman, L., and S. Jung. 2007. Lung macrophages serve as obligatory intermediate between blood monocytes and alveolar macrophages. J. Immunol. 179: 3488-3494.
23. Guilliams, M., I. De Kleer, S. Henri, S. Post, L. Vanhoutte, S. De Prijck, K. Deswarte, B. Malissen, H. Hammad, and B. N. Lambrecht. 2013. Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J. Exp. Med. 210: 1977-1992.
24. van Furth, R., and Z. A. Cohn. 1968. The origin and kinetics of mononuclear phagocytes. J. Exp. Med. 128: 415-435.
25. van oud Alblas, A. B., and R. van Furth. 1979. Origin, kinetics, and characteristics of pulmonary macrophages in the normal steady state. J. Exp. Med. 149: 1504-1518.
26. Hashimoto, D., A. Chow, C. Noizat, P. Teo, M. B. Beasley, M. Leboeuf, C. D. Becker, P. See, J. Price, D. Lucas, et al. 2013. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38: 792-804.
27. Davies, L. C., S. J. Jenkins, J. E. Allen, and P. R. Taylor. 2013. Tissue-resident macrophages. Nat. Immunol. 14: 986-995.
28. Rosas, M., L. C. Davies, P. J. Giles, C. T. Liao, B. Kharfan, T. C. Stone, V. B. O'Donnell, D. J. Fraser, S. A. Jones, and P. R. Taylor. 2014. The transcription factor Gata6 links tissue macrophage phenotype and proliferative renewal. Science 344: 645-648.
29. Jenkins, S. J., D. Ruckerl, P. C. Cook, L. H. Jones, F. D. Finkelman, N. van Rooijen, A. S. MacDonald, and J. E. Allen. 2011. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332: 1284-1288.
30. Spurzem, J. R., C. Saltini, W. Rom, R. J. Winchester, and R. G. Crystal. 1987. Mechanisms of macrophage accumulation in the lungs of asbestos-exposed subjects. Am. Rev. Respir. Dis. 136: 276-280.
31. Wright, E. S., D. M. White, A. N. Brady, L. C. Li, J. B. D'Arcy, and K. L. Smiler. 1987. DNA synthesis in pulmonary alveolar macrophages and type II cells: effects of ozone exposure and treatment with alpha-difluoromethylornithine. J. Toxicol. Environ. Health 21: 15-26.
32. Chen, B. D., M. Mueller, and T. H. Chou. 1988. Role of granulocyte/macrophage colony-stimulating factor in the regulation of murine alveolar macrophage proliferation and differentiation. J. Immunol. 141: 139-144.
33. Chen, B. D., M. Mueller, and T. Olencki. 1988. Interleukin-3 (IL-3) stimulates the clonal growth of pulmonary alveolar macrophage of the mouse: role of IL-3 in the regulation of macrophage production outside the bone marrow. Blood 72: 685-690.
34. Fan, K., Q. Ruan, L. Sensenbrenner, and B. Chen. 1992. Transforming growth factor-beta 1 bifunctionally regulates murine macrophage proliferation. Blood 79: 1679-1685.
35. Kreipe, H., H. J. Radzun, K. Heidorn, J. Barth, J. Kiemle-Kallee, W. Petermann, J. Gerdes, and M. R. Parwaresch. 1990. Proliferation, macrophage colonystimulating factor, and macrophage colony-stimulating factor-receptor expression of alveolar macrophages in active sarcoidosis. Lab. Invest. 62: 697-703.
36. Sorokin, S. P., and J. D. Brain. 1975. Pathways of clearance in mouse lungs exposed to iron oxide aerosols. Anat. Rec. 181: 581-625.
37. Assoian, R. K., B. E. Fleurdelys, H. C. Stevenson, P. J. Miller, D. K. Madtes, E. W. Raines, R. Ross, and M. B. Sporn. 1987. Expression and secretion of type beta transforming growth factor by activated human macrophages. Proc. Natl. Acad. Sci. USA 84: 6020-6024.
38. Takeuchi, M., P. Alard, and J. W. Streilein. 1998. TGF-beta promotes immune deviation by altering accessory signals of antigen-presenting cells. J. Immunol. 160: 1589-1597.
39. Nemeth, K., A. Keane-Myers, J. M. Brown, D. D. Metcalfe, J. D. Gorham, V. G. Bundoc, M. G. Hodges, I. Jelinek, S. Madala, S. Karpati, and E. Mezey. 2010. Bone marrow stromal cells use TGF-beta to suppress allergic responses in a mouse model of ragweed-induced asthma. Proc. Natl. Acad. Sci. USA 107: 5652-5657.
40. Lauzon-Joset, J. F., D. Marsolais, A. Langlois, and E. Y. Bissonnette. 2014. Dysregulation of alveolar macrophages unleashes dendritic cell-mediated mechanisms of allergic airway inflammation. Mucosal Immunol. 7: 155-164.
41. Bang, B. R., E. Chun, E. J. Shim, H. S. Lee, S. Y. Lee, S. H. Cho, K. U. Min, Y. Y. Kim, and H. W. Park. 2011. Alveolar macrophages modulate allergic inflammation in a murine model of asthma. Exp. Mol. Med. 43: 275-280.
42. Careau, E., L. I. Proulx, P. Pouliot, A. Spahr, V. Turmel, and E. Y. Bissonnette. 2006. Antigen sensitization modulates alveolar macrophage functions in an asthma model. Am. J. Physiol. Lung Cell. Mol. Physiol. 290: L871-L879.
43. Akagawa, K. S., K. Kamoshita, and T. Tokunaga. 1988. Effects of granulocytemacrophage colony-stimulating factor and colony-stimulating factor-1 on the proliferation and differentiation of murine alveolar macrophages. J. Immunol. 141: 3383-3390.
44. Alam, R., J. York, M. Boyars, S. Stafford, J. A. Grant, J. Lee, P. Forsythe, T. Sim, and N. Ida. 1996. Increased MCP-1, RANTES, and MIP-1alpha in bronchoalveolar lavage fluid of allergic asthmatic patients. Am. J. Respir. Crit. Care Med. 153: 1398-1404.
45. Sergejeva, S., S. Ivanov, J. Lötvall, and A. Lindén. 2005. Interleukin-17 as a recruitment and survival factor for airway macrophages in allergic airway inflammation. Am. J. Respir. Cell Mol. Biol. 33: 248-253.
46. Tang, C., J. M. Rolland, C. Ward, B. Quan, and E. H. Walters. 1997. IL-5 production by bronchoalveolar lavage and peripheral blood mononuclear cells in asthma and atopy. Eur. Respir. J. 10: 624-632.
47. Noma, T., M. Hayashi, Y. Kawano, I. Yoshizawa, Y. Ishikawa, T. Saeki, K. Aoki, and N. Matsuura. 1999. Functional interleukin-5 activity in peripheral blood mononuclear cells from adolescents with mite antigen asthma in remission. Clin. Exp. Allergy 29: 780-785.
48. Ogawa, K., O. Kaminuma, H. Kikkawa, K. Akiyama, and A. Mori. 2003. Interaction with monocytes enhances IL-5 gene transcription in peripheral T cells of asthmatic patients. Int. Arch. Allergy Immunol. 131(Suppl 1): 20-25.
49. Varol, C., L. Landsman, D. K. Fogg, L. Greenshtein, B. Gildor, R. Margalit, V. Kalchenko, F. Geissmann, and S. Jung. 2007. Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J. Exp. Med. 204: 171-180.
50. Robays, L. J., T. Maes, S. Lebecque, S. A. Lira, W. A. Kuziel, G. G. Brusselle, G. F. Joos, and K. V. Vermaelen. 2007. Chemokine receptor CCR2 but not CCR5 or CCR6 mediates the increase in pulmonary dendritic cells during allergic airway inflammation. J. Immunol. 178: 5305-5311.
51. Osterholzer, J. J., G. H. Chen, M. A. Olszewski, Y. M. Zhang, J. L. Curtis, G. B. Huffnagle, and G. B. Toews. 2011. Chemokine receptor 2-mediated accumulation of fungicidal exudate macrophages in mice that clear cryptococcal lung infection. Am. J. Pathol. 178: 198-211.
52. Osterholzer, J. J., G. H. Chen, M. A. Olszewski, J. L. Curtis, G. B. Huffnagle, and G. B. Toews. 2009. Accumulation of CD11b+ lung dendritic cells in response to fungal infection results from the CCR2-mediated recruitment and differentiation of Ly-6Chigh monocytes. J. Immunol. 183: 8044-8053.
53. Plantinga, M., M. Guilliams, M. Vanheerswynghels, K. Deswarte, F. Branco- Madeira, W. Toussaint, L. Vanhoutte, K. Neyt, N. Killeen, B. Malissen, et al. 2013. Conventional and monocyte-derived CD11b(+) dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity 38: 322-335.
54. Egawa, M., K. Mukai, S. Yoshikawa, M. Iki, N. Mukaida, Y. Kawano, Y. Minegishi, and H. Karasuyama. 2013. Inflammatory monocytes recruited to allergic skin acquire an anti-inflammatory M2 phenotype via basophil-derived interleukin-4. Immunity 38: 570-580.
55. Blease, K., B. Mehrad, T. J. Standiford, N. W. Lukacs, J. Gosling, L. Boring, I. F. Charo, S. L. Kunkel, and C. M. Hogaboam. 2000. Enhanced pulmonary allergic responses to Aspergillus in CCR22/2 mice. J. Immunol. 165: 2603-2611.
56. Kim, Y., W. A. Sung, S. Kuziel, S. M. Feldman, Fu, and C. E. Rose, Jr. 2001. Enhanced airway Th2 response after allergen challenge in mice deficient in CC chemokine receptor-2 (CCR2). J. Immunol. 166: 5183-5192.
57. Cabanski, M., J. Wilhelm, Z. Zaslona, M. Steinmüller, L. Fink, W. Seeger, and J. Lohmeyer. 2009. Genome-wide transcriptional profiling of mononuclear phagocytes recruited to mouse lungs in response to alveolar challenge with the TLR2 agonist Pam3CSK4. Am. J. Physiol. Lung Cell. Mol. Physiol. 297: L608-L618.