Active players in resolution of shock/sepsis induced indirect lung injury: Immunomodulatory effects of tregs and PD-1

Journal of Leukocyte Biology

Volumn 96, Issue 5, 2014, Pages 809-820

  Tang, Lunxian ^a,b   Bai, Jianwen ^a,b   Chung, Chun Shiang ^b   Lomas Neira, Joanne ^b   Chen, Yaping ^b   Huang, Xin ^b   Ayala, Alfred ^b  

^a TONGJI UNIVERSITY   (China)

^b BROWN UNIVERSITY   (United States)

Author keywords

Adoptive transfer; Apoptosis; ARDS; Chemokine; Neutrophil influx

Indexed keywords

CASPASE 3; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; PROGRAMMED DEATH 1 RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; CYTOKINE; PEROXIDASE;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; INNATE IMMUNITY; LUNG ALVEOLUS CELL; LUNG LAVAGE; LUNG PARENCHYMA; LYMPHOCYTE MIGRATION; MALE; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; REGULATORY T LYMPHOCYTE; RESUSCITATION; SEPSIS; SHOCK; ADOPTIVE TRANSFER; ANIMAL; CYTOLOGY; DISEASE MODEL; GENE SILENCING; GENETICS; IMMUNOLOGY; IMMUNOPHENOTYPING; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHENOTYPE; SEPTIC SHOCK; SPLEEN;

ACUTE LUNG INJURY; ADOPTIVE TRANSFER; ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CASPASE 3; CTLA-4 ANTIGEN; CYTOKINES; DISEASE MODELS, ANIMAL; GENE KNOCKDOWN TECHNIQUES; IMMUNOMODULATION; IMMUNOPHENOTYPING; INFLAMMATION MEDIATORS; MALE; MICE; MICE, KNOCKOUT; NEUTROPHILS; PEROXIDASE; PHENOTYPE; PROGRAMMED CELL DEATH 1 RECEPTOR; SHOCK, SEPTIC; SPLEEN; T-LYMPHOCYTES, REGULATORY;

EID: 84908290358     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.4MA1213-647RR     Document Type: Article

References (56)

1. Calfee, C. S., Eisner, M. D., Ware, L. B., Thompson, B. T., Parsons, P. E., Wheeler, A. P., Korpak, A., Matthay, M. A., Acute Respiratory Distress Syndrome Network, National Heart, Lung, and Blood Institute (2007) Trauma-associated lung injury differs clinically and biologically from acute lung injury due to other clinical disorders. Crit. Care Med. 35, 2431–2432.
2. Wheeler, A. P., Bernard, G. R. (2007) Acute lung injury and the acute respiratory distress syndrome: a clinical review. Lancet 369, 1553–1564.
3. ARDS Definition Task Force, Ranieri, V. M., Rubenfeld, G. D., Thompson, B. T., Ferguson, N. D., Caldwell, E., Fan, E., Camporota, L., Slutsky, A. S. (2012) Acute respiratory distress syndrome: the Berlin Definition. JAMA 307, 2526–2533.
4. Diaz, J. V., Brower, R., Calfee, C. S., Matthay, M. A. (2010) Therapeutic tragedies for severe acute lung injury. Crit. Care Med. 38, 1644–1650.
5. Ware, L. B. (2006) Pathophysiology of acute lung injury and the acute respiratory distress syndrome. Semin. Respir. Crit. Care Med. 27, 337–349.
6. Matthay, M. A., Zemans, R. L. (2011) The acute respiratory distress syndrome: pathogenesis and treatment. Annu. Rev. Pathol. 6, 147–163.
7. Kearley, J., Barker, J. E., Robinson, D. S., Lloyd, C. M. (2005) Resolution of airway inflammation and hyperreactivity after in vivo transfer of CD4+CD25+ regulatory T cells is interleukin 10 dependent. J. Exp. Med. 202, 1539–1547.
8. McKinley, L., Logar, A. J., McAllister, F., Zheng, M., Steele, C., Kolls, J. K. (2006) Regulatory T cells dampen pulmonary inflammation and lung injury in an animal model of pneumocystis pneumonia. J. Immunol. 177, 6215–6226.
9. Scott-Browne, J. P., Shafiani, S., Tucker-Heard, G., Ishida-Tsubota, K., Fontenot, J. D., Rudensky, A. Y., Bevan, M. J., Urdahl, K. B. (2007) Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis. J. Exp. Med. 204, 2159–2169.
10. D’Alessio, F. R., Tsushima, K., Aggarwal, N. R., West, E. E., Willett, M. H., Britos, M. F., Pipeling, M. R., Brower, R. G., Tuder, R. M., McDyer, J. F., King, L. S. (2009) 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.
11. Aggarwal, N. R., D’Alessio, F. R., Tsushima, K., Sidhaye, V. K., Cheadle, C., Grigoryev, D. N., Barnes, K. C., King, L. S. (2010) Regulatory T cellmediated resolution of lung injury: identification of potential target genes via expression profiling. Physiol. Genomics 41, 109–119.
12. Sun, J., Han, Z. B., Liao, W., Yang, S. G., Yang, Z., Yu, J., Meng, L., Wu, R., Han, Z. C. (2011) Intrapulmonary delivery of human umbilical cord mesenchymal stem cells attenuates acute lung injury by expanding CD4+CD25+ forkhead boxp3 (FOXP3)+ regulatory T cells and balancing anti- and pro-inflammatory factors. Cell. Physiol. Biochem. 27, 587–596.
13. Ehrentraut, H., Clambey, E. T., McNamee, E. N., Brodsky, K. S., Ehrentraut, S. F., Poth, J. M., Riegel, A. K., Westrich, J. A., Colgan, S. P., Eltzschig, H. K. (2013) CD73+ regulatory T cells contribute to adenosinemediated resolution of acute lung injury. FASEB J. 27, 2207–2219.
14. Venet, F., Chung, C. S., Huang, X., Lomas-Neira, J., Chen, Y., Ayala, A. (2009) Lymphocytes in the development of lung inflammation: a role for regulatory CD4+ T cells in indirect pulmonary lung injury. J. Immunol. 183, 3472–3480.
15. Francisco, L. M., Sage, P. T., Sharpe, A. H. (2010) The PD-1 pathway in tolerance and autoimmunity. Immunol. Rev. 236, 219–242.
16. Riley, J. L. (2009) PD-1 signaling in primary T cells. Immunol. Rev. 229, 114–125.
17. Gianchecchi, E., Delfino, D. V., Fierabracci, A. (2013) Recent insights into the role of the PD-1/PD-L1 pathway in immunological tolerance and autoimmunity. Autoimmun. Rev. 12, 1091–1100.
18. Monaghan, S. F., Thakkar, R. K., Tran, M. L., Huang, X., Cioffi, W. G., Ayala, A., Heffernan, D. S. (2012) Programmed death 1 expression as a marker for immune and physiological dysfunction in the critically ill surgical patient. Shock 38, 117–122.
19. Guignant, C., Lepape, A., Huang, X., Kherouf, H., Denis, L., Poitevin, F., Malcus, C., Chéron, A., Allaouchiche, B., Gueyffier, F., Ayala, A., Monneret, G., Venet, F. (2011) Programmed death-1 levels correlate with increased mortality, nosocomial infection and immune dysfunctions in septic shock patients. Crit. Care 15, R99.
20. Monaghan, S. F., Thakkar, R. K., Heffernan, D. S., Huang, X., Chung, C. S., Lomas-Neira, J., Cioffi, W. G., Ayala, A. (2012) Mechanisms of indirect acute lung injury: a novel role for the coinhibitory receptor, programmed death-1. Ann. Surg. 255, 158–164.
21. Ayala, A., Chung, C. S., Lomas, J. L., Song, G. Y., Doughty, L. A., Gregory, S. H., Cioffi, W. G., LeBlanc, B. W., Reichner, J., Simms, H. H., Grutkoski, P. S. (2002) Shock induced neutrophil mediated priming for acute lung injury in mice: divergent effects of TLR-4 and TLR-4/FasL deficiency. Am. J.Pathol. 161, 2283–2294.
22. Lomas, J. L., Chung, C. S., Grutkoski, P. S., LeBlanc, B. W., Lavigne, L., Reichner, J., Gregory, S. H., Doughty, L. A., Cioffi, W. G., Ayala, A. (2003) Differential effects of macrophage inflammatory protein-2 and keratinocyte-derived chemokine on hemorrhage-induced neutrophil priming for lung inflammation: assessment by adoptive cell transfer in mice. Shock 19, 358–365.
23. Iskander, K. N., Craciun, F. L., Stepien, D. M., Duffy, E. R., Kim, J., Moitra, R., Vaickus, L. J., Osuchowski, M. F., Remick, D. G. (2013) Cecal ligation and puncture-induced murine sepsis does not cause lung injury. Crit. Care Med. 41, 159–170.
24. McGee, H. S., Agrawal, D. K. (2009) Naturally occurring and inducible T-regulatory cells modulating immune response in allergic asthma. Am. J. Respir. Crit. Care Med. 180, 211–225.
25. Perl, M., Lomas-Neira, J., Venet, F., Chung, C. S., Ayala, A. (2011) Pathogenesis of indirect (secondary) acute lung injury. Expert Rev. Respir. Med. 5, 115–126.
26. Perl, M., Hohmann, C., Denk, S., Kellermann, P., Lu, D., Braumüller, S., Bachem, M. G., Thomas, J., Knöferl, M. W., Ayala, A., Gebhard, F., Huber-Lang, M. S. (2012) Role of activated neutrophils in chest traumainduced septic acute lung injury. Shock 38, 98–106.
27. Perl, M., Chung, C. S., Perl, U., Thakkar, R., Lomas-Neira, J., Ayala, A. (2010) Therapeutic accessibility of caspase-mediated cell death as a key pathomechanism in indirect acute lung injury. Crit. Care Med. 38, 1179–1186.
28. Tsai, H. C., Velichko, S., Hung, L. Y., Wu, R. (2013) IL-17A and Th17 cells in lung inflammation: an update on the role of Th17 cell differentiation and IL-17R signaling in host defense against infection. Clin. Dev. Immunol. 2013, 267-971.
29. Parry, R. V., Chemnitz, J. M., Frauwirth, K. A., Lanfranco, A. R., Braunstein, I., Kobayashi, S. V., Linsley, P. S., Thompson, C. B., Riley, J. L. (2005) CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol. Cell. Biol. 25, 9543–9553.
30. Nakajima, T., Suarez, C. J., Lin, K. W., Jen, K. Y., Schnitzer, J. E., Makani, S. S., Parker, N., Perkins, D. L., Finn, P. W. (2010) T cell pathways involving CTLA4 contribute to a model of acute lung injury. J. Immunol. 184, 5835–5841.
31. Venet, F., Chung, C. S., Monneret, G., Huang, X., Horner, B., Garber, M., Ayala, A. (2008) Regulatory T cell populations in sepsis and trauma. J. Leukoc. Biol. 83, 523–535.
32. Siegmund, K., Feuerer, M., Siewert, C., Ghani, S., Haubold, U., Dankof, A., Krenn, V., Schön, M. P., Scheffold, A., Lowe, J. B., Hamann, A., Syrbe, U., Huehn, J. (2005) Migration matters: regulatory T-cell compartmentalization determines suppressive activity in vivo. Blood 106, 3097–3104.
33. Zhang, N., Schröppel, B., Lal, G., Jakubzick, C., Mao, X., Chen, D., Yin, N., Jessberger, R., Ochando, J. C., Ding, Y., Bromberg, J. S. (2009) Regulatory T cells sequentially migrate from inflamed tissues to draining lymph nodes to suppress the alloimmune response. Immunity 30, 458–469.
34. Grommes, J., Soehnlein, O. (2011) Contribution of neutrophils to acute lung injury. Mol. Med. 17, 293–307.
35. Santos, S. S., Brunialti, M. K., Rigato, O., Machado, F. R., Silva, E., Salomao, R. (2012) Generation of nitric oxide and reactive oxygen species by neutrophils and monocytes from septic patients and association with outcomes. Shock 38, 18–23.
36. Wu, C. L., Lin, L. Y., Yang, J. S., Chan, M. C., Hsueh, C. M. (2009) Attenuation of lipopolysaccharide-induced acute lung injury by treatment with IL-10. Respirology 14, 511–521.
37. Kobbe, P., Stoffels, B., Schmidt, J., Tsukamoto, T., Gutkin, D. W., Bauer, A. J., Pape, H. C. (2009) IL-10 deficiency augments acute lung but not liver injury in hemorrhagic shock. Cytokine 45, 26–31.
38. Kobbe, P., Schmidt, J., Stoffels, B., Chanthaphavong, R. S., Bauer, A. J., Pape, H. C. (2009) IL-10 administration attenuates pulmonary neutrophil infiltration and alters pulmonary iNOS activation following hemorrhagic shock. Inflamm. Res. 58, 170–174.
39. Maynard, C. L., Harrington, L. E., Janowski, K. M., Oliver, J. R., Zindl, C. L., Rudensky, A. Y., Weaver, C. T. (2007) Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3+ precursor cells in the absence of interleukin 10. Nat. Immunol. 8, 931–941.
40. Langenhorst, D., Gogishvili, T., Ribechini, E., Kneitz, S., McPherson, K., Lutz, M. B., Hünig, T. (2012) Sequential induction of effector function, tissue migration and cell death during polyclonal activation of mouse regulatory T-cells. PLoS One 7, e50080.
41. Rubtsov, Y. P., Rasmussen, J. P., Chi, E. Y., Fontenot, J., Castelli, L., Ye, X., Treuting, P., Siewe, L., Roers, A., Henderson, Jr., W. R., Muller W., Rudensky, A. Y. (2008) Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 28, 546–558.
42. Suri-Payer, E., Cantor, H. (2001) Differential cytokine requirements for regulation of autoimmune gastritis and colitis by CD4(+)CD25(+) T cells. J. Autoimmun. 16, 115–123.
43. Ye, P., Garvey, P. B., Zhang, P., Nelson, S., Bagby, G., Summer, W. R., Schwarzenberger, P., Shellito, J. E., Kolls, J. K. (2001) Interleukin-17 and lung host defense against Klebsiella pneumoniae infection. Am. J. Respir. Cell Mol. Biol. 25, 335–340.
44. Braun, R. K., Ferrick, C., Neubauer, P., Sjoding, M., Sterner-Kock, A., Kock, M., Putney, L., Ferrick, D. A., Hyde, D. M., Love, R. B. (2008) IL-17 producing gammadelta T cells are required for a controlled inflammatory response after bleomycin-induced lung injury. Inflammation 31, 167–179.
45. Prause, O., Bossios, A., Silverpil, E., Ivanov, S., Bozinovski, S., Vlahos, R., Sjöstrand, M., Anderson, G. P., Lindén, A. (2009) IL-17-producing T lymphocytes in lung tissue and in the bronchoalveolar space after exposure to endotoxin from Escherichia coli in vivo-effects of anti-inflammatory pharmacotherapy. Pulm. Pharmacol.Ther. 22, 199–207.
46. Miyamoto, M., Prause, O., Sjöstrand, M., Laan, M., Lötvall, J., Lindén, A. (2003) Endogenous IL-17 as a mediator of neutrophil recruitment caused by endotoxin exposure in mouse airways. J. Immunol. 170, 4665–4672.
47. Chaudhry, A., Samstein, R. M., Treuting, P., Liang, Y., Pils, M. C., Heinrich, J. M., Jack, R. S., Wunderlich, F. T., Brüning, J. C., Müller, W., Rudensky, A. Y. (2011) Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation. Immunity 34, 566–578.
48. Pandiyan, P., Conti, H. R., Zheng, L., Peterson, A. C., Mathern, D. R., Hernández-Santos, N., Edgerton, M., Gaffen, S. L., Lenardo, M. J. (2011) CD4+CD25+Foxp3+ regulatory T cells promote Th17 cells in vitro and enhance host resistance in mouse Candida albicans Th17 cell infection model. Immunity 34, 422–434.
49. Song, L., Weng, D., Liu, F., Chen, Y., Li, C., Dong, L., Tang, W., Chen, J. (2012) Tregs promote the differentiation of Th17 cells in silica-induced lung fibrosis in mice. PloS One 7, e37286.
50. Francisco, L. M., Salinas, V. H., Brown, K. E., Vanguri, V. K., Freeman, G. J., Kuchroo, V. K., Sharpe, A. H. (2009) PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J. Exp. Med. 206, 3015–3029.
51. Beswick, E. J., Pinchuk, I. V., Das, S., Powell, D. W., Reyes, V. E. (2007) Expression of the programmed death ligand 1, B7-H1, on gastric epithelial cells after Helicobacter pylori exposure promotes development of CD4+ CD25+ FoxP3+ regulatory T cells. Infect. Immun. 75, 4334–4341.
52. Das, S., Suarez, G., Beswick, E. J., Sierra, J. C., Graham, D. Y., Reyes, V. E. (2006) Expression of B7-H1 on gastric epithelial cells: its potential role in regulating T cells during Helicobacter pylori infection. J. Immunol. 176, 3000–3009.
53. McGee, H. S., Yagita, H., Shao, Z., Agrawal, D. K. (2010) Programmed death-1 antibody blocks therapeutic effects of T-regulatory cells in cockroach antigen-induced allergic asthma. Am. J. Respir. Cell Mol. Biol. 43, 432–442.
54. Polanczyk, M. J., Hopke, C., Vandenbark, A. A., Offner, H. (2007) Tregs suppressive activity involves estrogen-dependent expression of programmed death-1 (PD-1). Int. Immunol. 19, 337–343.
55. Wang, Z. Y., Sato, H., Kusam, S., Sehra, S., Toney, L. M., Dent, A. L. (2005) Regulation of IL-10 gene expression in Th2 cells by Jun proteins. J. Immunol. 174, 2098–2105.
56. Adamzik, M., Broll, J., Steinmann, J., Westendorf, A. M., Rehfeld, I., Kreissig, C., Peters, J. (2013) An increased alveolar CD4 + CD25 + Foxp3 + T-regulatory cell ratio in acute respiratory distress syndrome is associated with increased 30-day mortality. Intensive Care Med. 39, 1743–1751.