Indoleamine 2,3-dioxygenase is not a pivotal regulator responsible for suppressing allergic airway inflammation through adipose-derived stem cells

PLoS ONE

Volumn 11, Issue 11, 2016, Pages

  Cho, Kyu Sup ^a   Park, Mi Kyung ^b   Mun, Sue Jean ^c   Park, Hee Young ^a   Yu, Hak Sun ^b   Roh, Hwan Jung ^c  

^a Pusan National University Hospital   (South Korea)

^b Pusan National University School of Medicine   (South Korea)

^c Pusan National University Yangsan Hospital   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; HERMES ANTIGEN; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; PROSTAGLANDIN E2; STEM CELL ANTIGEN 1; THY 1 ANTIGEN; TRANSFORMING GROWTH FACTOR BETA; IL10 PROTEIN, MOUSE; IMMUNOGLOBULIN G; METHACHOLINE CHLORIDE;

ADIPOSE DERIVED STEM CELL; ALLERGIC AIRWAY INFLAMMATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHOALVEOLAR LAVAGE FLUID; CELL DIFFERENTIATION; CELL HYPERPLASIA; CELL POPULATION; CONTROLLED STUDY; ENZYME INHIBITION; EOSINOPHIL; FEMALE; GENE EXPRESSION; GOBLET CELL; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOMODULATION; IMMUNOPHENOTYPING; INFLAMMATORY CELL; KNOCKOUT MOUSE; LUNG DRAINING LYMPH NODE; LUNG PARENCHYMA; LYMPH NODE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; TH1 CELL; TH2 CELL; WILD TYPE; ADIPOSE TISSUE; ANIMAL; ASTHMA; BIOLOGICAL THERAPY; BLOOD; C57BL MOUSE; CELL CULTURE; CYTOLOGY; GENETICS; HYPERPLASIA; IMMUNOLOGY; INFLAMMATION; LYMPHOCYTE COUNT; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PROCEDURES;

ADIPOSE TISSUE; ANIMALS; ASTHMA; BRONCHOALVEOLAR LAVAGE FLUID; CELL- AND TISSUE-BASED THERAPY; CELLS, CULTURED; EOSINOPHILS; FEMALE; GOBLET CELLS; HYPERPLASIA; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-13; INTERLEUKIN-4; INTERLEUKIN-5; LYMPHOCYTE COUNT; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; METHACHOLINE CHLORIDE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

EID: 84993995757     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0165661     Document Type: Article

References (58)

1. Bousquet J, Khaltaev N, Cruz AA, Denburg J, Fokkens WJ, Togias A, et al. Allergic Rhinitis and its Impact on Asthma (ARIA) 2008 update (in collaboration with the World Health Organization, GA (2) Len and Allergen) Allergy. 2008;63:8-160.
2. Wilson MS, Taylor MD, Balic A, Finney CA, Lamb JR, Maizels RM. Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J Exp Med. 2005;202:1199-1212. doi: 10.1084/jem.20042572 PMID: 16275759
3. Shi HZ, Qin XJ. CD4CD25 regulatory T lymphocytes in allergy and asthma. Allergy. 2005;60:986-995. doi: 10.1111/j.1398-9995.2005.00844.x PMID: 15969678
4. Jaffar Z, Sivakuru T, Roberts K. CD4+CD25+ T cells regulate airway eosinophilic inflammation by modulating the Th2 cell phenotype. J Immunol. 2004;172:3842-3849. PMID: 15004191
5. Park HK, Cho KS, Park HY, Shin DH, Kim YK, Jung JS, et al. Adipose-derived stromal cells inhibit allergic airway inflammation in mice. Stem Cells Dev. 2010;19:1811-1818. doi: 10.1089/scd.2009.0513 PMID: 20225940
6. Goodwin M, Sueblinvong V, Eisenhauer P, Ziats NP, LeClair L, Poynter ME, et al. Bone marrowderived mesenchymal stromal cells inhibit Th2-mediated allergic airways inflammation in mice. Stem Cells. 2011;29:1137-1148. doi: 10.1002/stem.656 PMID: 21544902
7. Bonfield TL, Koloze M, Lennon DP, Zuchowski B, Yang SE, Caplan AI. Human mesenchymal stem cells suppress chronic airway inflammation in the murine ovalbumin asthma model. Am J Physiol Lung Cell Mol Physiol. 2010;299:L760-770. doi: 10.1152/ajplung.00182.2009 PMID: 20817776
8. Fu QL, Chow YY, Sun SJ, Zeng QX, Li HB, Shi JB, et al. Mesenchymal stem cells derived from human induced pluripotent stem cells modulate T-cell phenotypes in allergic rhinitis. Allergy. 2012;67:1215-1222. doi: 10.1111/j.1398-9995.2012.02875.x. PMID: 22882409
9. Cho KS, Park HK, Park HY, Jung JS, Jeon SG, Kim YK, et al. IFATS collection: Immunomodulatory effects of adipose tissue-derived stem cells in an allergic rhinitis mouse model. Stem Cells. 2009;27:259-265. doi: 10.1634/stemcells.2008-0283 PMID: 18832595
10. Sun YQ, Deng MX, He J, Zeng QX, Wen W, Wong DS, et al. Human pluripotent stem cell-derived mesenchymal stem cells prevent allergic airway inflammation in mice. Stem Cells. 2012;30:2692-2699. doi: 10.1002/stem.1241 PMID: 22987325
11. Cho KS, Roh HJ. Immunomodulatory effects of adipose-derived stem cells in airway allergic diseases. Curr Stem Cell Res Ther. 2010;5:111-115. PMID: 19941459
12. Cho KS, Park MK, Kang SA, Park HY, Hong SL, Park HK, et al. Adipose-derived stem cells ameliorate allergic airway inflammation by inducing regulatory T cells in a mouse model of asthma. Mediators Inflamm. 2014;2014:436476. doi: 10.1155/2014/436476 PMID: 25246732
13. Ge X, Bai C, Yang J, Lou G, Li Q, Chen R. Intratracheal transplantation of bone marrow-derived mesenchymal stem cells reduced airway inflammation and up-regulated CD4+CD25+ regulatory T cells in asthmatic mouse. Cell Biol Int. 2013;37:675-686. doi: 10.1002/cbin. 10084 PMID: 23483727
14. Fu QL, Chow YY, Sun SJ, Zeng QX, Li HB, Shi JB, et al. Mesenchymal stem cells derived from human induced pluripotent stem cells modulate T-cell phenotypes in allergic rhinitis. Allergy. 2012;67:1215-1222. doi: 10.1111/j.1398-9995.2012.02875.x. PMID: 22882409
15. Nemeth K, Keane-Myers A, Brown JM, Metcalfe DD, Gorham JD, Bundoc VG, et al. Bone marrow stromal cells use TGF-β to suppress allergic responses in a mouse model of ragweed-induced asthma. Proc Natl Acad Sci USA. 2010;107:5652-5657. doi: 10.1073/pnas.0910720107 PMID: 20231466
16. Ball HJ, Yuasa HJ, Austin CJ, Weiser S, Hunt NH. Indoleamine 2, 3-dioxygenase-2: a new enzyme in the kynurenine pathway. Int J Biochem Cell Biol. 2009;41:467-471. doi: 10.1016/j.biocel.2008.01.005 PMID: 18282734
17. Baban B, Chandler PR, Sharma MD, Pihkala J, Koni PA, Munn DH, et al. IDO activates regulatory T cells and blocks their conversion into Th17-like T cells. J Immunol. 2009;183:2475-2483. doi: 10. 4049/jimmunol.0900986 PMID: 19635913
18. Sharma MD, Baban B, Chandler P, Hou DY, Singh N, Yagita H, et al. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2, 3-dioxygenase. J Clin Invest. 2007;117:2570-2582. doi: 10.1172/JCI31911 PMID: 17710230
19. Sucher R, Kurz K, Weiss G, Margreiter R, Fuchs D, Brandacher G. IDO-mediated tryptophan degradation in the pathogenesis of malignant tumor disease. Int J Tryptophan Res. 2010;3:113-120. PMID: 22084593
20. Meisel R, Zibert A, Laryea M, Gobel U, Daubener W, Dilloo D. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2, 3-dioxygenase-mediated tryptophan degradation. Blood. 2004;103:4619-21. doi: 10.1182/blood-2003-11-3909 PMID: 15001472
21. Curti A, Trabanelli S, Salvestrini V, Baccarani M, Lemoli RM. The role of indoleamine 2, 3-dioxygenase in the induction of immune tolerance: focus on hematology. Blood. 2009;113:2394-2401. doi: 10. 1182/blood-2008-07-144485 PMID: 19023117
22. Ge W, Jiang J, Arp J, Liu W, Garcia B, Wang H. Regulatory T-cell generation and kidney allograft tolerance induced by mesenchymal stem cells associated with indoleamine 2, 3-dioxygenase expression. Transplantation. 2010;90:1312-1320. doi: 10.1097/TP.0b013e3181fed001 PMID: 21042238
23. Luo C, Jia W, Wang K, Chi F, Gu Y, Yan X, et al. Human amniotic fluid stem cells suppress PBMC proliferation through IDO and IL-10-dependent pathways. Curr Stem Cell Res Ther. 2014;9:36-45. PMID: 24102581
24. Ling W, Zhang J, Yuan Z, Ren G, Zhang L, Chen X, et al. Mesenchymal stem cells use IDO to regulate immunity in tumor microenvironment. Cancer Res. 2014;74:1576-1587. doi: 10.1158/0008-5472. CAN-13-1656 PMID: 24452999
25. Caterson EJ, Nesti LJ, Danielson KG, Tuan RS. Human marrow-derived mesenchymal progenitor cells: isolation, culture expansion, and analysis of differentiation. Mol Biotechnol. 2002;20:245-256. doi: 10.1385/MB:20:3:245 PMID: 11936255
26. Pellaton-Longaretti C, Boudousquie C, Barbier N, Barbey C, Argiroffo CB, Donati Y, et al. CD4+CD25-mTGFbeta+ T cells induced by nasal application of ovalbumin transfer tolerance in a therapeutic model of asthma. Int Immunol. 2011;23:17-27. doi: 10.1093/intimm/dxq453 PMID: 21123830
27. Lee CG, Link H, Baluk P, Homer RJ, Chapoval S, Bhandari V, et al. Vascular endothelial growth factor (VEGF) induces remodeling and enhances TH2-mediated sensitization and inflammation in the lung. Nat Med. 2004;10:1095-1103. doi: 10.1038/nm1105 PMID: 15378055
28. Tournoy KG, Kips JC, Schou C, Pauwels RA. Airway eosinophilia is not a requirement for allergeninduced airway hyperresponsiveness. Clin Exp Allergy. 2000;30:79-85. PMID: 10606934
29. Kang JH, Kim BS, Uhm TG, Lee SH, Lee GR, Park CS, et al. Gamma-secretase inhibitor reduces allergic pulmonary inflammation by modulating Th1 and Th2 responses. Am J Respir Crit Care Med. 2009;179:875-882. doi: 10.1164/rccm.200806-893OC PMID: 19234107
30. English K, Ryan JM, Tobin L, Murphy MJ, Barry FP, Mahon BP. Cell contact, prostaglandin E (2) and transforming growth factor beta 1 play non-redundant roles in human mesenchymal stem cell induction of CD4+CD25 (High) forkhead box P3+ regulatory T cells. Clin Exp Immunol. 2009;156:149-160. doi: 10.1111/j.1365-2249.2009.03874.x PMID: 19210524
31. Mellor AL, Munn DH. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol. 2004;4:762-764. doi: 10.1038/nri1457 PMID: 15459668
32. Beutelspacher SC, Tan PH, McClure MO, Larkin DF, Lechler RI, George AJ. Expression of indoleamine 2, 3-dioxygenase (IDO) by endothelial cells: implications for the control of alloresponses. Am J Transplant. 2006;6:1320-1330. doi: 10.1111/j.1600-6143.2006.01324.x PMID: 16686756
33. Odemuyiwa SO, Ghahary A, Li Y, Puttagunta L, Lee JE, Musat-Marcu S, et al. Cutting edge: human eosinophils regulate T cell subset selection through indoleamine 2, 3-dioxygenase. J Immunol. 2004;173:5909-5913. PMID: 15528322
34. Uyttenhove C, Pilotte L, Theate I, Stroobant V, Colau D, Parmentier N, et al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2, 3-dioxygenase. Nat Med. 2003;9:1269-1274. doi: 10.1038/nm934 PMID: 14502282
35. Fallarino F, Grohmann U, You S, McGrath BC, Cavener DR, Vacca C, et al. The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor zeta-chain and induce a regulatory phenotype in naïve T cells. J Immunol. 2006;176:6752-6761. PMID: 16709834
36. Munn DH, Mellor AL. Indoleamine 2, 3-dioxygenase and tumor-induced tolerance. J Clin Invest. 2007;117:1147-1154. doi: 10.1172/JCI31178 PMID: 17476344
37. Mbongue JC, Nicholas DA, Torrez TW, Kim NS, Firek AF, Langridge WH. The role of indoleamine 2, 3-dioxygenase in immune suppression and autoimmunity. Vaccines. 2015;10:703-729.
38. Xu H, Oriss TB, Fei M, Henry AC, Melgert BN, Chen L, et al. Indoleamine 2, 3-dioxygenase in lung dendritic cells promotes Th2 responses and allergic inflammation. Proc Natl Acad Sci USA. 2008;6:6690-6695.
39. Von Bubnoff D, Bieber T. The indoleamine 2, 3-dioxygenase (IDO) pathway controls allergy. Allergy. 2012;67:718-725. doi: 10.1111/j.1398-9995.2012.02830.x PMID: 22519427
40. Hayashi T, Beck L, Rossetto C, Gong X, Takikawa O, Takabayashi K, et al. Inhibition of experimental asthma by indoleamine 2, 3-dioxygenase. J Clin Invest. 2004;114:270-279. doi: 10.1172/JCI21275 PMID: 15254594
41. Moingeon P, Batard T, Fadel R, Frati F, Sieber J, Van Overtvelt L. Immune mechanisms of allergenspecific sublingual immunotherapy. Allergy. 2006;61:151-165. doi: 10.1111/j.1398-9995.2006. 01002.x PMID: 16409190
42. Taher YA, Piavaux BJ, Gras R, Van Esch BC, Hofman GA, Bloksma N, et al. Indoleamine 2, 3-dioxygenase-dependent tryptophan metabolites contributes to tolerance induction during allergen immunotherapy in a mouse model. J Allergy Clin Immunol. 2008;121:983-991. doi: 10.1016/j.jaci.2007.11. 021 PMID: 18179817
43. Croitoru-Lamoury J, Lamoury FM, Caristo M, Suzuki K, Walker D, Takikawa O, et al. Interferon-γ regulates the proliferation and differentiation of mesenchymal stem cells via activation of indoleamine 2, 3-dioxygenase (IDO). PLoS One. 2011;6:e14698. doi: 10.1371/journal.pone.0014698 PMID: 21359206
44. Matysiak M, Stasiolek M, Orlowski W, Jurewicz A, Janczar S, Raine CS, et al. Stem cells ameliorate EAE via an indoleamine 2, 3-dioxygenase (IDO) mechanism. J Neuroimmunol. 2008;193:12-23. doi: 10.1016/j.jneuroim.2007.07.025 PMID: 18077006
45. Opitz CA, Litzenburger UM, Lutz C, Lanz TV, Tritschler I, Koppel A, et al. Toll-like receptor engagement enhances the immunosuppressive properties of human bone marrow-derived mesenchymal stem cells by inducing Indoleamine-2, 3-dioxygenase-1 via interferon-beta and protein kinase R. Stem Cells. 2009;27:909-919. doi: 10.1002/stem.7 PMID: 19353519
46. Ebrahimi A, Kardar GA, Toolabi L, Ghanbari H, Sadroddiny E. Inducible expression of indoleamine 2, 3-dioxygenase attenuates acute rejection of tissue-engineered lung allografts in rats. Gene. 2016;576:412-420. doi: 10.1016/j.gene.2015.10.054 PMID: 26506443
47. He Y, Zhou S, Liu H, Shen B, Zhao H, Peng K, et al. Indoleamine 2, 3-dioxygenase transfected mesenchymal stem cells induce kidney allograft tolerance by increasing the production and function of regulatory T cells. Transplantation. 2015;99:1829-1838. doi: 10.1097/TP.0000000000000856 PMID: 26308414
48. Lee YE, An J, Lee KH, Kim SS, Song HJ, Pyeon H, et al. The synergistic local immunosuppressive effects of neural stem cells expressing indoleamine 2, 3-dioxygenase (IDO) in an experimental autoimmune encephalomyelitis (EAE) animal model. PloS One. 2015;10:e0144298. doi: 10.1371/journal. pone.0144298 PMID: 26636969
49. Ciccocioppo R, Cangemi GC, Kruzliak P, Gallia A, Betti E, Badulli C, et al. Ex vivo immunosuppressive effects of mesenchymal stem cells on Crohn's disease mucosal T cells are largely dependent on indoleamine 2, 3-dioxygenase activity and cell-cell contact. Stem Cell Res Ther. 2015;6:137. doi: 10.1186/s13287-015-0122-1 PMID: 26206376
50. Fu J, Zhang L, Song S, Sheng K, Li Y, Li P, et al. Effect of bone marrow-derived CD11b (+) F4/80 (+) immature dendritic cells on the balance between pro-inflammatory and anti-inflammatory cytokines in DBA/1 mice with collagen-induced arthritis. Inflamm Res. 2014;63:357-367. doi: 10.1007/s00011-014-0707-7 PMID: 24458308
51. Matysiak M, Stasiolek M, Orlowski W, Jurewicz A, Janczar S, Raine CS, et al. Stem cells ameliorate EAE via an indoleamine 2, 3-dioxygenase (IDO) mechanism. J Neuroimmunol. 2008;193:12-23. doi: 10.1016/j.jneuroim.2007.07.025 PMID: 18077006
52. Krampera M, Cosmi L, Angeli R, Pasini A, Liotta F, Andreini A, et al. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells. 2006;24:386-398. doi: 10.1634/stemcells.2005-0008 PMID: 16123384
53. Spaggiari GM, Moretta L. Cellular and molecular interactions of mesenchymal stem cells in innate immunity. Immunol Cell Biol. 2013;91:27-31. doi: 10.1038/icb.2012.62 PMID: 23146943
54. Castro-Manrreza ME, Montesinos JJ. Immunoregulation by mesenchymal stem cells: biological aspects and clinical applications. J Immunol Res. 2015;2015:394917. doi: 10.1155/2015/394917 PMID: 25961059
55. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105:1815-1822. doi: 10.1182/blood-2004-04-1559 PMID: 15494428
56. Cui L, Yin S, Liu W, Li N, Zhang W, Cao Y. Expanded adipose-derived stem cells suppress mixed lymphocyte reaction by secretion of prostaglandin E2. Tissue Eng. 2007;13:1185-1195. doi: 10.1089/ten. 2006.0315 PMID: 17518704
57. Cho KS, Lee JH, Park MK, Park HK, Yu HS, Roh HJ. Prostaglandin E2 and transforming growth factor-β play a critical role in suppression of allergic airway inflammation by adipose-derived stem cells. PLoS One. 2015;10:e0131813. doi: 10.1371/journal.pone.0131813 PMID: 26176545
58. Chaves AC, Ceravolo IP, Gomes JA, Zani CL, Romanha AJ, Gazzinelli RT. IL-4 and IL-13 regulate the induction of indoleamine 2, 3-dioxygenase activity and the control of Toxoplasma gondii replication in human fibroblasts activated with IFN-gamma. Eur J Immunol. 2001;31:333-344. doi: 10.1002/1521-4141 (200102)CO;2-X PMID: 11180096