Adenosine A2A receptor deletion blocks the beneficial effects of Lactobacillus reuteri in regulatory T-Deficient scurfy mice

Frontiers in Immunology

Volumn 8, Issue DEC, 2017, Pages

  He, Baokun ^a   Hoang, Thomas K ^a   Tran, Dat Q ^a   Rhoads, Jon Marc ^a   Liu, Yuying ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Adenosine A2A receptor; Autoimmunity; Cytokines; IPEX; Lactobacillus reuteri; Probiotic; Regulatory T deficiency; Scurfy

Indexed keywords

ADENOSINE A2A RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CELL DIFFERENTIATION; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE DELETION; HISTOPATHOLOGY; IMMUNOREGULATION; INFLAMMATION; LACTOBACILLUS REUTERI; LIFESPAN; LYMPHOPROLIFERATIVE DISEASE; MALE; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; STAINING; SURVIVAL; TISSUE PREPARATION;

EID: 85037351402     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.01680     Document Type: Article

References (50)

1. Barzaghi F, Passerini L, Bacchetta R. Immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome: a paradigm of immunodeficiency with autoimmunity. Front Immunol (2012) 3:211. doi:10.3389/fimmu.2012.00211
2. d'Hennezel E, Bin DK, Torgerson T, Piccirillo CA. The immunogenetics of immune dysregulation, polyendocrinopathy, enteropathy, X linked (IPEX) syndrome. J Med Genet (2012) 49:291-302. doi:10.1136/jmedgenet-2012-100759
3. Bennett CL, Christie J, Ramsdell F, Brunkow ME, Ferguson PJ, Whitesell L, et al. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet (2001) 27:20-1. doi:10.1038/83713
4. Brunkow ME, Jeffery EW, Hjerrild KA, Paeper B, Clark LB, Yasayko SA, et al. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet (2001) 27:68-73. doi:10.1038/83784
5. Baris S, Schulze I, Ozen A, Aydiner EK, Altuncu E, Karasu GT, et al. Clinical heterogeneity of immunodysregulation, polyendocrinopathy, enteropathy, X-linked: pulmonary involvement as a non-classical disease manifestation. J Clin Immunol (2014) 34:601-6. doi:10.1007/s10875-014-0059-7
6. Zennaro D, Scala E, Pomponi D, Caprini E, Arcelli D, Gambineri E, et al. Proteomics plus genomics approaches in primary immunodeficiency: the case of immune dysregulation, polyendocrinopathy, enteropathy, X-linked (IPEX) syndrome. Clin Exp Immunol (2012) 167:120-8. doi:10.1111/j.1365-2249.2011.04492.x
7. He B, Hoang TK, Wang T, Ferris M, Taylor CM, Tian X, et al. Resetting microbiota by Lactobacillus reuteri inhibits Treg deficiency-induced autoimmunity via adenosine A2A receptors. J Exp Med (2017) 214:107-23. doi:10.1084/jem.20160961
8. Verbsky JW, Chatila TA. Immune dysregulation, polyendocrinopathy, enteropathy, X-linked (IPEX) and IPEX-related disorders: an evolving web of heritable autoimmune diseases. Curr Opin Pediatr (2013) 25:708-14. doi:10.1097/MOP.0000000000000029
9. Fredholm BB, IJzerman AP, Jacobson KA, Klotz KN, Linden J. International union of pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol Rev (2001) 53:527-52.
10. Lappas CM, Rieger JM, Linden J. A2A adenosine receptor induction inhibits IFN-gamma production in murine CD4+ T cells. J Immunol (2005) 174:1073-80. doi:10.4049/jimmunol.174.2.1073
11. Lukashev DE, Smith PT, Caldwell CC, Ohta A, Apasov SG, Sitkovsky MV. Analysis of A2A receptor-deficient mice reveals no significant compensatory increases in the expression of A2B, A1, and A3 adenosine receptors in lymphoid organs. Biochem Pharmacol (2003) 65:2081-90. doi:10.1016/S0006-2952(03)00158-8
12. Koshiba M, Rosin DL, Hayashi N, Linden J, Sitkovsky MV. Patterns of A2A extracellular adenosine receptor expression in different functional subsets of human peripheral T cells. Flow cytometry studies with anti-A2A receptor monoclonal antibodies. Mol Pharmacol (1999) 55:614-24.
13. Hasko G, Cronstein BN. Adenosine: an endogenous regulator of innate immunity. Trends Immunol (2004) 25:33-9. doi:10.1016/j.it.2003.11.003
14. Sitkovsky MV. Use of the A(2A) adenosine receptor as a physiological immunosuppressor and to engineer inflammation in vivo. Biochem Pharmacol (2003) 65:493-501. doi:10.1016/S0006-2952(02)01548-4
15. Walter J, Britton RA, Roos S. Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm. Proc Natl Acad Sci U S A (2011) 108(Suppl 1):4645-52. doi:10.1073/pnas.1000099107
16. Liu Y, Fatheree NY, Mangalat N, Rhoads JM. Lactobacillus reuteri strains reduce incidence and severity of experimental necrotizing enterocolitis via modulation of TLR4 and NF-kappaB signaling in the intestine. Am J Physiol Gastrointest Liver Physiol (2012) 302:G608-17. doi:10.1152/ajpgi.00266.2011
17. Liu Y, Tran DQ, Fatheree NY, Marc RJ. Lactobacillus reuteri DSM 17938 differentially modulates effector memory T cells and Foxp3+ regulatory T cells in a mouse model of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol (2014) 307:G177-86. doi:10.1152/ajpgi.00038.2014
18. Urbanska M, Gieruszczak-Bialek D, Szajewska H. Systematic review with meta-analysis: Lactobacillus reuteri DSM 17938 for diarrhoeal diseases in children. Aliment Pharmacol Ther (2016) 43:1025-34. doi:10.1111/apt.13590
19. Francavilla R, Lionetti E, Castellaneta S, Ciruzzi F, Indrio F, Masciale A, et al. Randomised clinical trial: Lactobacillus reuteri DSM 17938 vs. placebo in children with acute diarrhoea - a double-blind study. Aliment Pharmacol Ther (2012) 36:363-9. doi:10.1111/j.1365-2036.2012.05180.x
20. Shornikova AV, Casas IA, Isolauri E, Mykkanen H, Vesikari T. Lactobacillus reuteri as a therapeutic agent in acute diarrhea in young children. J Pediatr Gastroenterol Nutr (1997) 24:399-404. doi:10.1097/00005176-199704000-00008
21. Oncel MY, Sari FN, Arayici S, Guzoglu N, Erdeve O, Uras N, et al. Lactobacillus reuteri for the prevention of necrotising enterocolitis in very low birthweight infants: a randomised controlled trial. Arch Dis Child Fetal Neonatal Ed (2014) 99:F110-5. doi:10.1136/archdischild-2013-304745
22. Rojas MA, Lozano JM, Rojas MX, Rodriguez VA, Rondon MA, Bastidas JA, et al. Prophylactic probiotics to prevent death and nosocomial infection in preterm infants. Pediatrics (2012) 130:e1113-20. doi:10.1542/peds.2011-3584
23. Athalye-Jape G, Rao S, Patole S. Lactobacillus reuteri DSM 17938 as a probiotic for preterm neonates: a strain-specific systematic review. JPEN J Parenter Enteral Nutr (2016) 40:783-94. doi:10.1177/0148607115588113
24. Urbanska M, Szajewska H. The efficacy of Lactobacillus reuteri DSM 17938 in infants and children: a review of the current evidence. Eur J Pediatr (2014) 173:1327-37. doi:10.1007/s00431-014-2328-0
25. Sung V, Collett S, de GT, Hiscock H, Tang M, Wake M. Probiotics to prevent or treat excessive infant crying: systematic review and meta-analysis. JAMA Pediatr (2013) 167:1150-7. doi:10.1001/jamapediatrics.2013.2572
26. Sharma R, Deshmukh US, Zheng L, Fu SM, Ju ST. X-linked Foxp3 (Scurfy) mutation dominantly inhibits submandibular gland development and inflammation respectively through adaptive and innate immune mechanisms. J Immunol (2009) 183:3212-8. doi:10.4049/jimmunol.0804355
27. Sharma R, Sharma PR, Kim YC, Leitinger N, Lee JK, Fu SM, et al. IL-2-controlled expression of multiple T cell trafficking genes and Th2 cytokines in the regulatory T cell-deficient scurfy mice: implication to multiorgan inflammation and control of skin and lung inflammation. J Immunol (2011) 186:1268-78. doi:10.4049/jimmunol.1002677
28. Suscovich TJ, Perdue NR, Campbell DJ. Type-1 immunity drives early lethality in scurfy mice. Eur J Immunol (2012) 42:2305-10. doi:10.1002/eji.201242391
29. Kanangat S, Blair P, Reddy R, Daheshia M, Godfrey V, Rouse BT, et al. Disease in the scurfy (sf) mouse is associated with overexpression of cytokine genes. Eur J Immunol (1996) 26:161-5. doi:10.1002/eji.1830260125
30. Singh N, Chandler PR, Seki Y, Baban B, Takezaki M, Kahler DJ, et al. Role of CD28 in fatal autoimmune disorder in scurfy mice. Blood (2007) 110:1199-206. doi:10.1182/blood-2006-10-054585
31. Antonioli L, Pacher P, Vizi ES, Hasko G. CD39 and CD73 in immunity and inflammation. Trends Mol Med (2013) 19:355-67. doi:10.1016/j.molmed.2013.03.005
32. Gomez G, Sitkovsky MV. Differential requirement for A2A and A3 adenosine receptors for the protective effect of inosine in vivo. Blood (2003) 102:4472-8. doi:10.1182/blood-2002-11-3624
33. Csoka B, Himer L, Selmeczy Z, Vizi ES, Pacher P, Ledent C, et al. Adenosine A2A receptor activation inhibits T helper 1 and T helper 2 cell development and effector function. FASEB J (2008) 22:3491-9. doi:10.1096/fj.08-107458
34. Arpaia N, Campbell C, Fan X, Dikiy S, van der VJ, DeRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature (2013) 504:451-5. doi:10.1038/nature12726
35. Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature (2013) 504:446-50. doi:10.1038/nature12721
36. Roelofsen H, Priebe MG, Vonk RJ. The interaction of short-chain fatty acids with adipose tissue: relevance for prevention of type 2 diabetes. Benef Microbes (2010) 1:433-7. doi:10.3920/BM2010.0028
37. da Rocha LF, da Silva MD, de Almeida CD, Santos AR. Anti-inflammatory effects of purine nucleosides, adenosine and inosine, in a mouse model of pleurisy: evidence for the role of adenosine A2 receptors. Purinergic Signal (2012) 8:693-704. doi:10.1007/s11302-012-9299-2
38. da Rocha LF, de Oliveira AP, Accetturi BG, de OM I, Domingos HV, de Almeida CD, et al. Anti-inflammatory effects of inosine in allergic lung inflammation in mice: evidence for the participation of adenosine A2A and A 3 receptors. Purinergic Signal (2013) 9:325-36. doi:10.1007/s11302-013-9351-x
39. Gomez G, Sitkovsky MV. Targeting G protein-coupled A2A adenosine receptors to engineer inflammation in vivo. Int J Biochem Cell Biol (2003) 35:410-4. doi:10.1016/S1357-2725(02)00177-2
40. Mabley JG, Pacher P, Murthy KG, Williams W, Southan GJ, Salzman AL, et al. The novel inosine analogue INO-2002 exerts an anti-inflammatory effect in a murine model of acute lung injury. Shock (2009) 32:258-62. doi:10.1097/SHK.0b013e31819c3414
41. Muto J, Lee H, Lee H, Uwaya A, Park J, Nakajima S, et al. Oral administration of inosine produces antidepressant-like effects in mice. Sci Rep (2014) 4:4199. doi:10.1038/srep04199
42. Rahimian R, Fakhfouri G, Daneshmand A, Mohammadi H, Bahremand A, Rasouli MR, et al. Adenosine A2A receptors and uric acid mediate protective effects of inosine against TNBS-induced colitis in rats. Eur J Pharmacol (2010) 649:376-81. doi:10.1016/j.ejphar.2010.09.044
43. Welihinda AA, Kaur M, Greene K, Zhai Y, Amento EP. The adenosine metabolite inosine is a functional agonist of the adenosine A receptor with a unique signaling bias. Cell Signal (2016) 28:552-60. doi:10.1016/j.cellsig.2016.02.010
44. Brady T. Adenosine deaminase. Biochem J (1942) 36:478-84. doi:10.1042/bj0360478
45. Hasko G, Linden J, Cronstein B, Pacher P. Adenosine receptors: therapeutic aspects for inflammatory and immune diseases. Nat Rev Drug Discov (2008) 7:759-70. doi:10.1038/nrd2638
46. Carini R, Grazia De CM, Splendore R, Baldanzi G, Nitti MP, Alchera E, et al. Role of phosphatidylinositol 3-kinase in the development of hepatocyte preconditioning. Gastroenterology (2004) 127:914-23. doi:10.1053/j.gastro.2004.06.018
47. Chan ES, Montesinos MC, Fernandez P, Desai A, Delano DL, Yee H, et al. Adenosine A(2A) receptors play a role in the pathogenesis of hepatic cirrhosis. Br J Pharmacol (2006) 148:1144-55. doi:10.1038/sj.bjp.0706812
48. Reinstein LJ, Lichtman SN, Currin RT, Wang J, Thurman RG, Lemasters JJ. Suppression of lipopolysaccharide-stimulated release of tumor necrosis factor by adenosine: evidence for A2 receptors on rat Kupffer cells. Hepatology (1994) 19:1445-52. doi:10.1016/0270-9139(94)90241-0
49. Day YJ, Huang L, McDuffie MJ, Rosin DL, Ye H, Chen JF, et al. Renal protection from ischemia mediated by A2A adenosine receptors on bone marrow-derived cells. J Clin Invest (2003) 112:883-91. doi:10.1172/JCI15483
50. Ohta A, Sitkovsky M. Role of G-protein-coupled adenosine receptors in downregulation of inflammation and protection from tissue damage. Nature (2001) 414:916-20. doi:10.1038/414916a