Mesenchymal stromal cells mediate aspergillus hyphal extract-induced allergic airway inflammation by inhibition of the th17 signaling pathway

Stem Cells Translational Medicine

Volumn 3, Issue 2, 2014, Pages 194-205

  Lathrop, Melissa J ^a   Brooks, Elice M ^a   Bonenfant, Nick R ^a   Sokocevic, Dino ^a   Borg, Zachary D ^a   Goodwin, Meagan ^a   Loi, Roberto ^b   Cruz, Fernanda ^c   Dunaway, Chad W ^d   Steele, Chad ^d   Weiss, Daniel J ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CAGLIARI   (Italy)

^c FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^d and Clinical Center   (United States)

Author keywords

Cell therapy; Lung asthma; Mesenchymal stromal cell; Mouse

Indexed keywords

ASPERGILLUS HYPHAL EXTRACT; FUNGAL EXTRACT; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; RANTES; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

AIRWAY RESISTANCE; ALLERGIC AIRWAY INFLAMMATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL POPULATION; CELL PROLIFERATION; CELL THERAPY; CONTROLLED STUDY; FLOW CYTOMETRY; LUNG FUNCTION; LUNG RESISTANCE; LYMPHOCYTE; MALE; MEDIASTINUM LYMPH NODE; MESENCHYMAL STROMA CELL; MOUSE; NEUTROPHIL; NONHUMAN; POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; SCORING SYSTEM; SIGNAL TRANSDUCTION; TH17 CELL; TH2 CELL;

CELL THERAPY; LUNG ASTHMA; MESENCHYMAL STROMAL CELL; MOUSE;

ANIMALS; ASPERGILLOSIS, ALLERGIC BRONCHOPULMONARY; ASPERGILLUS FUMIGATUS; BRONCHOALVEOLAR LAVAGE FLUID; DISEASE MODELS, ANIMAL; INTERLEUKIN-17; LYMPH NODES; LYMPHOCYTE CULTURE TEST, MIXED; MALE; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; NEUTROPHILS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 84894048356     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2013-0061     Document Type: Article

References (62)

1. Kupczyk M, Wenzel SUS. U.S. and European severe asthma cohorts: What can they teach us about severe asthma? J Intern Med 2012;272:121-132.
2. Wenzel S. Severe asthma: From characteristics to phenotypes to endotypes. Clin Exp Allergy 2012;42:650-658.
3. Miller MK, Johnson C, Miller DP et al. Severity assessment in asthma: An evolving concept. J Allergy Clin Immunol 2005;116: 990-995.
4. Moore WC, Bleecker ER, Curran-Everett D et al. Characterization of the severe asthma phenotype by the National Heart, Lung, and Blood Institute's Severe Asthma Research Program. J Allergy Clin Immunol 2007;119: 405-413.
5. Sorkness RL, Bleecker ER, BusseWW et al. Lung function in adults with stable but severe asthma: Air trapping and incomplete reversal of obstruction with bronchodilation. J Appl Physiol (1985) 2008;104:394-403.
6. Strek ME. Difficult asthma. Proc Am Thorac Soc 2006;3:116-123.
7. Alcorn JF, Crowe CR, Kolls JK. TH17 cells in asthma and COPD. Annu Rev Physiol 2010;72: 495-516.
8. Al-Ramli W, Préfontaine D, Chouiali F et al. T(H)17-associated cytokines (IL-17A and IL-17F) in severe asthma. J Allergy Clin Immunol 2009; 123:1185-1187.
9. Chakir J, Shannon J, Molet S et al. Airway remodeling-associated mediators in moderate to severe asthma: Effect of steroids on TGFbeta, IL-11, IL-17, and type I and type III collagen expression. J Allergy Clin Immunol 2003;111: 1293-1298.
10. McKinley L, Alcorn JF, Peterson A et al. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J Immunol 2008;181:4089-4097.
11. Bousquet J, Cabrera P, Berkman N et al. The effect of treatment with omalizumab, an anti-IgE antibody, on asthma exacerbations and emergency medical visits in patients with severe persistent asthma. Allergy 2005;60: 302-308.
12. Busse WW, Morgan WJ, Gergen PJ et al. Randomized trial of omalizumab (anti-IgE) for asthma in inner-city children. N Engl J Med 2011;364:1005-1015.
13. Riccio AM, Dal Negro RW, Micheletto C et al. Omalizumab modulates bronchial reticular basement membrane thickness and eosinophil infiltration in severe persistent allergic asthma patients. Int J Immunopathol Pharmacol 2012;25:475-484.
14. Bourin P, Gadelorge M, Peyrafitte JA et al. Mesenchymal progenitor cells: Tissue origin, isolation and culture. Transfus Med Hemother 2008;35:160-167.
15. Friedenstein AJ, Chailakhyan RK, Latsinik NV et al. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 1974;17: 331-340.
16. Keating A. Mesenchymal stromal cells. Curr Opin Hematol 2006;13:419-425.
17. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006;8:315-317.
18. Horwitz EM, Le Blanc K, DominiciMet al. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 2005;7:393-395.
19. Auletta JJ, Bartholomew AM, Maziarz RT et al. The potential of mesenchymal stromal cells as a novel cellular therapy for multiple sclerosis. Immunotherapy 2012;4:529-547.
20. Le Blanc K, Mougiakakos D. Multipotent mesenchymal stromal cells and the innate immune system. Nat Rev Immunol 2012;12: 383-396.
21. Qayyum AA, Haack-Sørensen M, Mathiasen AB et al. Adipose-derived mesenchymal stromal cells for chronic myocardial ischemia (MyStromalCell trial): Study design. Regen Med 2012;7:421-428.
22. Reekmans K, Praet J, De Vocht N et al. Stem cell therapy for multiple sclerosis: Preclinical evidence beyond all doubt? Regen Med 2012;7:245-259.
23. Cyranoski D. Canada approves stem cell product. Nat Biotechnol 2012;30:571.
24. Lau AN, Goodwin M, Kim CF et al. Stem cells and regenerative medicine in lung biology and diseases. Mol Ther 2012;20:1116-1130.
25. Weiss DJ. Stem cells, cell therapies, and bioengineering in lung biology and diseases. Comprehensive review of the recent literature 2010-2012. Ann Am Thorac Soc 2013;10:S45-S97.
26. Weiss DJ, Casaburi R, Flannery R et al. A placebo-controlled randomized trial of mesenchymal stem cells in COPD. Chest 2013;143: 1590-1598.
27. Bonfield TL, Koloze M, Lennon DP et al. Human mesenchymal stem cells suppress chronic airway inflammation in the murine ovalbumin asthma model. Am J Physiol Lung Cell Mol Physiol 2010;299:L760-L770.
28. Bonfield TL, Nolan Koloze MT, Lennon DP et al. Defining human mesenchymal stem cell efficacy in vivo. J Inflamm (Lond) 2010;7:51.
29. Cho KS, Park HK, Park HY et al. IFATS collection: Immunomodulatory effects of adipose tissue-derived stem cells in an allergic rhinitis mouse model. STEM CELLS 2009;27:259-265.
30. Firinci F, Karaman M, Baran Y et al. Mesenchymal stem cells ameliorate the histopathological changes in a murine model of chronic asthma. Int Immunopharmacol 2011;11:1120-1126.
31. Goodwin M, Sueblinvong V, Eisenhauer P et al. Bone marrow-derived mesenchymal stromal cells inhibit Th2-mediated allergic airways inflammation in mice. STEM CELLS 2011;29: 1137-1148.
32. Ionescu LI, Alphonse RS, Arizmendi N et al. Airway delivery of soluble factors from plastic-adherent bone marrow cells prevents murine asthma. Am J Respir Cell Mol Biol 2012;46:207-216.
33. Kapoor S, Patel SA, Kartan S et al. Tolerance-like mediated suppression by mesenchymal stem cells in patients with dust mite allergy-induced asthma. J Allergy Clin Immunol 2012;129:1094-1101.
34. Kavanagh H, Mahon BP. Allogeneic mesenchymal stem cells prevent allergic airway inflammation by inducing murine regulatory T cells. Allergy 2011;66:523-531.
35. Lee SH, Jang AS, Kwon JH et al. Mesenchymal stem cell transfer suppresses airway remodeling in a toluene diisocyanate-induced murine asthma model. AllergyAsthma Immunol Res 2011;3:205-211.
36. Nemeth K, Keane-Myers A, Brown JM et al. Bone marrow stromal cells use TGF-beta to suppress allergic responses in a mouse model of ragweed-induced asthma. Proc Natl Acad Sci USA 2010;107:5652-5657.
37. Ou-Yang HF, Huang Y, Hu XB et al. Suppression of allergic airway inflammation in a mouse model of asthma by exogenous mesenchymal stem cells. Exp Biol Med (Maywood) 2011;236:1461-1467.
38. Park HK, Cho KS, Park HY et al. Adiposederived stromal cells inhibit allergic airway inflammation in mice. Stem Cells Dev 2010;19: 1811-1818.
39. Tasso R, Ilengo C, Quarto R et al. Mesenchymal stem cells induce functionally active Tregulatory lymphocytes in a paracrine fashion and ameliorate experimental autoimmune uveitis. Invest Ophthalmol Vis Sci 2012;53: 786-793.
40. Allard JB, Poynter ME, Marr KA et al. Aspergillus fumigatus generates an enhanced Th2-biased immune response in mice with defective cystic fibrosis transmembrane conductance regulator. J Immunol 2006;177: 5186-5194.
41. Allard JB, Rinaldi L, Wargo MJ et al. Th2 allergic immune response to inhaled fungal antigens is modulated by TLR-4-independent bacterial products. Eur J Immunol 2009;39: 776-788.
42. Prockop DJ, Phinney DG, Bunnell BA. Mesenchymal Stem Cells: Methods and Protocols. Totowa, NJ: Humana Press, 2008.
43. Schuessler TF, Bates JH. A computercontrolled research ventilator for small animals: Design and evaluation. IEEE Trans Biomed Eng 1995;42:860-866.
44. Wang SY, Yang M, Xu XP et al. Intranasal delivery of T-bet modulates the profile of helper T cell immune responses in experimental asthma. J Investig Allergol Clin Immunol 2008; 18:357-365.
45. Zar JH.Biostatisticalanalysis.5thed.Upper Saddle River, NJ: Prentice-Hall/Pearson, 2010.
46. Paveglio SA, Allard J, Foster Hodgkins SR et al. Airway epithelial indoleamine 2,3-dioxygenase inhibits CD4+ T cells during Aspergillus fumigatus antigen exposure. Am J Respir Cell Mol Biol 2011;44:11-23.
47. Jenkins MK, Schwartz RH. Antigen presentation by chemically modified splenocytes induces antigen-specific T cell unresponsiveness in vitro and in vivo. J Exp Med 1987;165: 302-319.
48. Gupta N, Su X, Popov B et al. Intrapulmonary delivery of bone marrow-derived mesenchymal stem cells improves survival and attenuates endotoxin-induced acute lung injury in mice. J Immunol 2007;179:1855-1863.
49. Ortiz LA, Dutreil M, Fattman C et al. Interleukin 1 receptor antagonist mediates the antiinflammatory and antifibrotic effect of mesenchymal stem cells during lung injury. Proc Natl Acad Sci USA 2007;104:11002-11007.
50. Engela AU, Baan CC, Dor FJ et al. On the interactions between mesenchymal stem cells and regulatory T cells for immunomodulation in transplantation. Front Immunol 2012;3:126.
51. Cho KS, Roh HJ. Immunomodulatory effects of adipose-derived stem cells in airway allergic diseases. Curr Stem Cell Res Ther 2010;5:111-115.
52. Wardlaw AJ, Brightling CE, Green R et al. New insights into the relationship between airway inflammation and asthma. Clin Sci (Lond) 2002;103:201-211.
53. Gaffen SL. Structure and signalling in the IL-17 receptor family. Nat Rev Immunol 2009;9: 556-567.
54. Aliotta JM, Sanchez-Guijo FM, Dooner GJ et al. Alteration of marrow cell gene expression, protein production, and engraftment into lung by lung-derived microvesicles: A novel mechanism for phenotype modulation. STEM CELLS 2007;25:2245-2256.
55. Lee C, Mitsialis SA, Aslam M et al. Exosomes mediate the cytoprotective action of mesenchymal stromal cells on hypoxiainduced pulmonary hypertension. Circulation 2012;126:2601-2611.
56. Ghannam S, Pène J, Torcy-Moquet G et al. Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotype. J Immunol 2010;185:302-312.
57. Qu X, Liu X, Cheng K et al. Mesenchymal stem cells inhibit Th17 cell differentiation by IL- 10 secretion. Exp Hematol 2012;40:761-770.
58. Tatara R, Ozaki K, Kikuchi Y et al. Mesenchymal stromal cells inhibit Th17 but not regulatory T-cell differentiation. Cytotherapy 2011; 13:686-694.
59. Busse WW. The relationship of airway hyperresponsiveness and airway inflammation: Airway hyperresponsiveness in asthma: Its measurement and clinical significance. Chest 2010;138(2 suppl):4S-10S.
60. Foster MW, Yang Z, Potts EN et al. S-nitrosoglutathione supplementation to ovalbumin-sensitized and -challenged mice ameliorates methacholine-induced bronchoconstriction. Am J Physiol Lung Cell Mol Physiol 2011;301:L739-L744.
61. Swedin L, Neimert-Andersson T, Hjoberg J et al. Dissociation of airway inflammation and hyperresponsiveness by cyclooxygenase inhibition in allergen challenged mice. Eur Respir J 2009;34:200-208.
62. Wilder JA, Collie DD, Wilson BS et al. Dissociation of airway hyperresponsiveness from immunoglobulin E and airway eosinophilia in a murine model of allergic asthma. Am J Respir Cell Mol Biol 1999;20:1326-1334.