Foxp3 + regulatory T cells promote lung epithelial proliferation

Mucosal Immunology

Volumn 7, Issue 6, 2014, Pages 1440-1451

  Mock, J R ^a   Garibaldi, B T ^a   Aggarwal, N R ^a   Jenkins, J ^a   Limjunyawong, N ^b   Singer, B D ^a   Chau, E ^a   Rabold, R ^b   Files, D C ^c   Sidhaye, V ^a   Mitzner, W ^b   Wagner, E M ^a   King, L S ^a   D'Alessio, F R ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; CD31 ANTIGEN; CD4 ANTIGEN; CD45 ANTIGEN; ENDOTOXIN; EPITHELIAL CELL ADHESION MOLECULE; INTERLEUKIN 2 RECEPTOR ALPHA; TRANSCRIPTION FACTOR FOXP3; UVOMORULIN; ALPHA E INTEGRINS; ALPHA INTEGRIN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; LEUKOCYTE ANTIGEN; LIPOPOLYSACCHARIDE;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DAMAGE; CELL ISOLATION; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; FLOW CYTOMETRY; FOXP3+ REGULATORY T LYMPHOCYTE; IN VITRO STUDY; LUNG ALVEOLUS EPITHELIUM; LUNG RESECTION; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; ADULT RESPIRATORY DISTRESS SYNDROME; ANIMAL; CHEMICALLY INDUCED; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG ALVEOLUS CELL; PATHOLOGY; RESPIRATORY TRACT MUCOSA;

ANIMALS; ANTIGENS, CD; CELL PROLIFERATION; FORKHEAD TRANSCRIPTION FACTORS; INTEGRIN ALPHA CHAINS; LIPOPOLYSACCHARIDES; MICE; MICE, KNOCKOUT; PNEUMOCYTES; RESPIRATORY DISTRESS SYNDROME, ADULT; RESPIRATORY MUCOSA; T-LYMPHOCYTES, REGULATORY;

EID: 84908191558     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2014.33     Document Type: Article

References (56)

1. Ware, L. B. & Matthay, M. A. The acute respiratory distress syndrome. N. Engl. J. Med. 342, 1334-1349 (2000).
2. Ranieri, V. M. et al. Acute respiratory distress syndrome: the Berlin Definition. JAMA 307, 2526-2533 (2012).
3. Brower, R. G. et al. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. The Acute Respiratory Distress Syndrome Network. N. Engl. J. Med. 342, 1301-1308 (2000).
4. Guerin, C. et al. Prone positioning in severe acute respiratory distress syndrome. N. Engl. J. Med. 368, 2159-2168 (2013).
5. Mizgerd, J. P. Respiratory infection and the impact of pulmonary immunity on lung health and disease. Am. J. Respir. Crit. Care Med. 186, 824-829 (2012).
6. Bhattacharya, J. & Matthay, M. A. Regulation and repair of the alveolarcapillary barrier in acute lung injury. Annu. Rev. Physiol. 75, 593-615 (2013).
7. Garibaldi, B. T. et al. Regulatory T cells reduce acute lung injury fibroproliferation by decreasing fibrocyte recruitment. Am. J. Respir. Cell. Mol. Biol. 48, 35-43 (2013).
8. D'Alessio, F. R. et al. CD4CD25Foxp3 Tregs resolve experimental lung injury in mice and are present in humans with acute lung injury. J. Clin. Invest. 119, 2898-2913 (2009).
9. Fontenot, J. D., Gavin, M. A. & Rudensky, A. Y. Foxp3 programs the development and function of CD4CD25 regulatory T cells. Nat. Immunol. 4, 330-336 (2003).
10. Abbas, A. K. et al. Regulatory T cells: recommendations to simplify the nomenclature. Nat. Immunol. 14, 307-308 (2013).
11. Shevach, E. M. CD4 CD25 suppressor T cells: more questions than answers. Nat. Rev. Immunol. 2, 389-400 (2002).
12. Vignali, D. A., Collison, L. W. & Workman, C. J. How regulatory Tcells work. Nat. Rev. Immunol. 8, 523-532 (2008).
13. Miyara, M. & Sakaguchi, S. Natural regulatory T cells: mechanisms of suppression. Trends Mol. Med. 13, 108-116 (2007).
14. Ehrentraut, H. et al. CD73 regulatory T cells contribute to adenosinemediated resolution of acute lung injury. FASEB J. 27, 2207-2219 (2013).
15. Ding, B. S. et al. Endothelial-derived angiocrine signals induce and sustain regenerative lung alveolarization. Cell 147, 539-553 (2011).
16. Kim, C. F. et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121, 823-835 (2005).
17. Fujino, N. et al. A novel method for isolating individual cellular components from the adult human distal lung. Am. J. Respir. Cell. Mol. Biol. 46, 422-430 (2012).
18. Giangreco, A., Shen, H., Reynolds, S. D. & Stripp, B. R. Molecular phenotype of airway side population cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 286, L624-L630 (2004).
19. Lee, J. H. et al. SPC H2B-GFP mice reveal heterogeneity of surfactant protein C-expressing lung cells. Am. J. Respir. Cell. Mol. Biol. 48, 288-289 (2012).
20. Yamamoto, K. et al. Type I alveolar epithelial cells mount innate immune responses during pneumococcal pneumonia. J. Immunol. 189, 2450-2459 (2012).
21. Dobbs, L. G.,Williams, M. C. & Gonzalez, R. Monoclonal antibodies specific to apical surfaces of rat alveolar type I cells bind to surfaces of cultured, but not freshly isolated, type II cells. Biochim. Biophys. Acta 970, 146-156 (1988).
22. Lo, B., Hansen, S., Evans, K., Heath, J. K. & Wright, J. R. Alveolar epithelial type II cells induce T cell tolerance to specific antigen. J. Immunol. 180, 881-888 (2008).
23. Su, X., Looney, M. R., Gupta, N. & Matthay, M. A. Receptor for advanced glycation end-products (RAGE) is an indicator of direct lung injury in models of experimental lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 297, L1-L5 (2009).
24. van Roy, F. & Berx, G. The cell-cell adhesion molecule E-cadherin. Cell Mol. Life Sci. 65, 3756-3788 (2008).
25. Fontenot, J. D. et al. Regulatory Tcell lineage specification by the forkhead transcription factor foxp3. Immunity 22, 329-341 (2005).
26. Kim, J. M., Rasmussen, J. P. & Rudensky, A. Y. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat. Immunol. 8, 191-197 (2007).
27. Boehm, F. et al. Deletion of Foxp3 regulatory T cells in genetically targeted mice supports development of intestinal inflammation. BMC Gastroenterol. 12, 97 (2012).
28. Lehmann, J. et al. Expression of the integrin alpha Ebeta 7 identifies unique subsets of CD25 as well as CD25- regulatory Tcells. Proc. Natl Acad. Sci. USA 99, 13031-13036 (2002).
29. Cepek, K. L. et al. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature 372, 190-193 (1994).
30. Schon, M. P. et al. Mucosal T lymphocyte numbers are selectively reduced in integrin alpha E (CD103)-deficient mice. J. Immunol. 162, 6641-6649 (1999).
31. Hsia, C. C. Signals andmechanisms of compensatory lung growth. J. Appl. Physiol. 97, 1992-1998 (2004).
32. Smyth, L. J., Kirby, J. A. & Cunningham, A. C. Role of the mucosal integrin alpha(E)(CD103)beta(7) in tissue-restricted cytotoxicity. Clin. Exp. Immunol. 149, 162-170 (2007).
33. Wang, L. et al. BLT1-dependent alveolar recruitment of CD4()CD25() Foxp3() regulatory T cells is important for resolution of acute lung injury. Am. J. Respir. Crit. Care Med. 186, 989-998 (2012).
34. Soroosh, P. et al. Lung-resident tissue macrophages generate Foxp3 regulatory T cells and promote airway tolerance. J. Exp. Med. 210, 775-788 (2013).
35. Rojas, M., Woods, C. R., Mora, A. L., Xu, J. & Brigham, K. L. Endotoxininduced lung injury in mice: structural, functional, and biochemical responses. Am. J. Physiol. Lung Cell. Mol. Physiol. 288, L333-L341 (2005).
36. Marsh, L. M. et al. Surface expression of CD74 by type II alveolar epithelial cells: a potential mechanism for macrophage migration inhibitory factorinduced epithelial repair. Am. J. Physiol. Lung Cell. Mol. Physiol. 296, L442-L452 (2009).
37. Cunningham, A. C. et al. Constitutive expression of MHC and adhesion molecules by alveolar epithelial cells (type II pneumocytes) isolated from human lung and comparison with immunocytochemical findings. J. Cell. Sci. 107 (Pt 2), 443-449 (1994).
38. Rock, J. & Konigshoff, M. Endogenous lung regeneration: potential and limitations. Am. J. Respir. Crit. Care Med. 186, 1213-1219 (2012).
39. Evans, M. J., Cabral, L. J., Stephens, R. J. & Freeman, G. Transformation of alveolar type 2 cells to type 1 cells following exposure to NO2. Exp. Mol. Pathol. 22, 142-150 (1975).
40. Fehrenbach, H. Alveolar epithelial type II cell: defender of the alveolus revisited. Respir. Res. 2, 33-46 (2001).
41. Evans, C. M., Phillips, A. D., Walker-Smith, J. A. & MacDonald, T. T. Activation of lamina propria T cells induces crypt epithelial proliferation and goblet cell depletion in cultured human fetal colon. Gut 33, 230-235 (1992).
42. Castro,G. A. Immunological regulation of epithelial function. Am. J. Physiol. 243, G321-G329 (1982).
43. Boismenu, R. & Havran, W. L. Modulation of epithelial cell growth by intraepithelial gamma delta T cells. Science 266, 1253-1255 (1994).
44. Burzyn, D. et al. A special population of regulatory T cells potentiates muscle repair. Cell 155, 1282-1295 (2013).
45. Belkaid, Y. & Rouse, B. T. Natural regulatory T cells in infectious disease. Nat. Immunol. 6, 353-360 (2005).
46. Cerf-Bensussan, N. et al. A monoclonal antibody (HML-1) defining a novel membrane molecule present on human intestinal lymphocytes. Eur. J. Immunol. 17, 1279-1285 (1987).
47. Kilshaw, P. J. & Murant, S. J. Expression and regulation of beta 7(beta p) integrins on mouse lymphocytes: relevance to the mucosal immune system. Eur. J. Immunol. 21, 2591-2597 (1991).
48. Weiner, H. L. Induction and mechanism of action of transforming growth factor-beta-secreting Th3 regulatory cells. Immunol. Rev. 182, 207-214 (2001).
49. Boismenu, R. & Havran, W. L. Gammadelta T cells in host defense and epithelial cell biology. Clin. Immunol. Immunopathol. 86, 121-133 (1998).
50. Leslie, C. C., McCormick-Shannon, K., Mason, R. J. & Shannon, J. M. Proliferation of rat alveolar epithelial cells in low density primary culture. Am. J. Respir. Cell. Mol. Biol. 9, 64-72 (1993).
51. Sugahara, K., Mason, R. J. & Shannon, J. M. Effects of soluble factors and extracellular matrix on DNA synthesis and surfactant gene expression in primary cultures of rat alveolar type II cells. Cell Tissue Res. 291, 295-303 (1998).
52. Chen, Z. et al. Identification of two novel markers for alveolar epithelial type I and II cells. Biochem. Biophys. Res. Commun. 319, 774-780 (2004).
53. Gonzalez, R. F., Allen, L. & Dobbs, L. G. Rat alveolar type I cells proliferate, express OCT-4, and exhibit phenotypic plasticity in vitro. Am. J. Physiol. Lung Cell. Mol. Physiol. 297, L1045-L1055 (2009).
54. Mukherjee, S. et al. Surfactant protein A modulates induction of regulatory T cells via TGF-beta. J. Immunol. 188, 4376-4384 (2012).
55. Burzyn, D., Benoist, C. & Mathis, D. Regulatory T cells in nonlymphoid tissues. Nat. Immunol. 14, 1007-1013 (2013).
56. Mock, J. R. et al. Haemophilus ducreyi targets Src family protein tyrosine kinases to inhibit phagocytic signaling. Infect. Immun. 73, 7808-7816 (2005).