Impact of enriched environment on murine T cell differentiation and gene expression profile

Frontiers in Immunology

Volumn 7, Issue SEP, 2016, Pages

  Rattazzi, Lorenza ^a   Piras, Giuseppa ^a   Brod, Samuel ^a   Smith, Koval ^a   Ono, Masahiro ^b   D'Acquisto, Fulvio ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

CD4 T cells; Cytokines; Enriched environment; Microarray; Resolution of inflammation

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CORTICOSTERONE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 4;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BIOINFORMATICS; CELL DIFFERENTIATION; CONTROLLED STUDY; ENVIRONMENTAL ENRICHMENT; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNE RESPONSE; LYMPH NODE; MARBLE BURYING TEST; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OPEN FIELD TEST; PHENOTYPE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; THYMUS; UPREGULATION;

EID: 84992109223     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00381     Document Type: Article

References (82)

1. Takashima A, Yao Y. Neutrophil plasticity: acquisition of phenotype and functionality of antigen-presenting cell. J Leukoc Biol (2015) 98(4):489-96. doi:10.1189/jlb.1MR1014-502R
2. Soumelis V, Pattarini L, Michea P, Cappuccio A. Systems approaches to unravel innate immune cell diversity, environmental plasticity and functional specialization. Curr Opin Immunol (2015) 32:42-7. doi:10.1016/j.coi.2014.12.007
3. Lafont V, Sanchez F, Laprevotte E, Michaud HA, Gros L, Eliaou JF, et al. Plasticity of gammadelta T cells: impact on the anti-tumor response. Front Immunol (2014) 5:622. doi:10.3389/fimmu.2014.00622
4. Geginat J, Paroni M, Maglie S, Alfen JS, Kastirr I, Gruarin P, et al. Plasticity of human CD4 T cell subsets. Front Immunol (2014) 5:630. doi:10.3389/fimmu.2014.00630
5. Kleinewietfeld M, Hafler DA. The plasticity of human Treg and Th17 cells and its role in autoimmunity. Semin Immunol (2013) 25(4):305-12. doi:10.1016/j.smim.2013.10.009
6. Schwartz M, Kipnis J, Rivest S, Prat A. How do immune cells support and shape the brain in health, disease, and aging? J Neurosci (2013) 33(45):17587-96. doi:10.1523/JNEUROSCI.3241-13.2013
7. Basu R, Hatton RD, Weaver CT. The Th17 family: flexibility follows function. Immunol Rev (2013) 252(1):89-103. doi:10.1111/imr.12035
8. Okada M, Hibino S, Someya K, Yoshmura A. Regulation of regulatory T cells: epigenetics and plasticity. Adv Immunol (2014) 124:249-73. doi:10.1016/B978-0-12-800147-9.00008-X
9. Sawant DV, Vignali DA. Once a Treg, always a Treg? Immunol Rev (2014) 259(1):173-91. doi:10.1111/imr.12173
10. Hori S. Lineage stability and phenotypic plasticity of Foxp3(+) regulatory T cells. Immunol Rev (2014) 259(1):159-72. doi:10.1111/imr.12175
11. Noack M, Miossec P. Th17 and regulatory T cell balance in autoimmune and inflammatory diseases. Autoimmun Rev (2014) 13(6):668-77. doi:10.1016/j.autrev.2013.12.004
12. Abou-Jaoude W, Monteiro PT, Naldi A, Grandclaudon M, Soumelis V, Chaouiya C, et al. Model checking to assess T-helper cell plasticity. Front Bioeng Biotechnol (2014) 2:86. doi:10.3389/fbioe.2014.00086
13. Miskov-Zivanov N, Turner MS, Kane LP, Morel PA, Faeder JR. The duration of T cell stimulation is a critical determinant of cell fate and plasticity. Sci Signal (2013) 6(300):ra97. doi:10.1126/scisignal.2004217
14. Gilles S, Traidl-Hoffmann C. The environment-pathogen-host axis in communicable and non-communicable diseases: recent advances in experimental and clinical research. J Dtsch Dermatol Ges (2014) 12(5):395-9. doi:10.1111/ddg.12345
15. Farhat SC, Silva CA, Orione MA, Campos LM, Sallum AM, Braga AL. Air pollution in autoimmune rheumatic diseases: a review. Autoimmun Rev (2011) 11(1):14-21. doi:10.1016/j.autrev.2011.06.008
16. Duntas LH. Environmental factors and thyroid autoimmunity. Ann Endocrinol (2011) 72(2):108-13. doi:10.1016/j.ando.2011.03.019
17. Ebringer A, Ahmadi K, Fielder M, Rashid T, Tiwana H, Wilson C, et al. Molecular mimicry: the geographical distribution of immune responses to Klebsiella in ankylosing spondylitis and its relevance to therapy. Clin Rheumatol (1996) 15(1):57-61. doi:10.1007/BF03342648
18. Malaria Genomic Epidemiology Network, Malaria Genomic Epidemiology Network. Reappraisal of known malaria resistance loci in a large multicenter study. Nat Genet (2014) 46(11):1197-204. doi:10.1038/ng.3107
19. Severance EG, Yolken RH, Eaton WW. Autoimmune diseases, gastrointestinal disorders and the microbiome in schizophrenia: more than a gut feeling. Schizophr Res (2016) 176(1):23-35. doi:10.1016/j.schres.2014.06.027
20. Tariq MM, Streeten EA, Smith HA, Sleemi A, Khabazghazvini B, Vaswani D, et al. Vitamin D: a potential role in reducing suicide risk? Int J Adolesc Med Health (2011) 23(3):157-65. doi:10.1515/ijamh.2011.038
21. Jafarian-Tehrani M, Sternberg EM. Neuroendocrine and other factors in the regulation of inflammation. Animal models. Ann N Y Acad Sci (2000) 917:819-24. doi:10.1111/j.1749-6632.2000.tb05447.x
22. Ligier S, Sternberg EM. Neuroendocrine host factors and inflammatory disease susceptibility. Environ Health Perspect (1999) 107(Suppl 5):701-7. doi:10.1289/ehp.99107s5701
23. Calixto OJ, Anaya JM. Socioeconomic status. The relationship with health and autoimmune diseases. Autoimmun Rev (2014) 13(6):641-54. doi:10.1016/j.autrev.2013.12.002
24. Karimi S, Yarmohammadian MH, Shokri A, Mottaghi P, Qolipour K, Kordi A, et al. Predictors and effective factors on quality of life among Iranian patients with rheumatoid arthritis. Mater Sociomed (2013) 25(3):158-62. doi:10.5455/msm.2013.25.158-162
25. Hendricks CO. Patients with lupus: an overview of culturally competent practice. Soc Work Health Care (2012) 51(7):640-51. doi:10.1080/00981389.2012.683367
26. Danese S, Sans M, Fiocchi C. Inflammatory bowel disease: the role of environmental factors. Autoimmun Rev (2004) 3(5):394-400. doi:10.1016/j.autrev.2004.03.002
27. Reynolds S, Lane SJ, Richards L. Using animal models of enriched environments to inform research on sensory integration intervention for the rehabilitation of neurodevelopmental disorders. J Neurodev Disord (2010) 2(3):120-32. doi:10.1007/s11689-010-9053-4
28. Nithianantharajah J, Hannan AJ. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci (2006) 7(9):697-709. doi:10.1038/nrn1970
29. Brown RE, Milner PM. The legacy of Donald O. Hebb: more than the Hebb synapse. Nat Rev Neurosci (2003) 4(12):1013-9. doi:10.1038/nrn1257
30. Mesa-Gresa P, Ramos-Campos M, Redolat R. Enriched environments for rodents and their interaction with nicotine administration. Curr Drug Abuse Rev (2013) 6(3):191-200. doi:10.2174/187447370603140401224222
31. Bondi CO, Klitsch KC, Leary JB, Kline AE. Environmental enrichment as a viable neurorehabilitation strategy for experimental traumatic brain injury. J Neurotrauma (2014) 31(10):873-88. doi:10.1089/neu.2014.3328
32. Wadowska M, Woods J, Rogozinska M, Briones TL. Neuroprotective effects of enriched environment housing after transient global cerebral ischemia are associated with the upregulation of insulin-like growth factor-1 signaling. Neuropathol Appl Neurobiol (2015) 41(4):544-56. doi:10.1111/nan.12146
33. Doulames V, Lee S, Shea TB. Environmental enrichment and social interaction improve cognitive function and decrease reactive oxidative species in normal adult mice. Int J Neurosci (2014) 124(5):369-76. doi:10.3109/00207454.2013.848441
34. Rodriguez JJ, Terzieva S, Olabarria M, Lanza RG, Verkhratsky A. Enriched environment and physical activity reverse astrogliodegeneration in the hippocampus of AD transgenic mice. Cell Death Dis (2013) 4:e678. doi:10.1038/cddis.2013.194
35. Jain V, Baitharu I, Prasad D, Ilavazhagan G. Enriched environment prevents hypobaric hypoxia induced memory impairment and neurodegeneration: role of BDNF/PI3K/GSK3beta pathway coupled with CREB activation. PLoS One (2013) 8(5):e62235. doi:10.1371/journal.pone.0062235
36. Jain V, Baitharu I, Barhwal K, Prasad D, Singh SB, Ilavazhagan G. Enriched environment prevents hypobaric hypoxia induced neurodegeneration and is independent of antioxidant signaling. Cell Mol Neurobiol (2012) 32(4):599-611. doi:10.1007/s10571-012-9807-5
37. Lee S, Doulames V, Donnelly M, Levasseaur J, Shea TB. Environmental enrichment can prevent cognitive decline induced by dietary oxidative challenge. J Alzheimers Dis (2012) 28(3):497-501. doi:10.3233/JAD-2011-111562
38. Yuan ZY, Gu P, Liu L, Wang YY, Liu J, Cui DS, et al. Neuroprotective effects of enriched environment in MPTP-treated SAMP8 mice. Neurosci Lett (2009) 454(1):6-10. doi:10.1016/j.neulet.2009.02.058
39. Anastasia A, Torre L, de Erausquin GA, Masco DH. Enriched environment protects the nigrostriatal dopaminergic system and induces astroglial reaction in the 6-OHDA rat model of Parkinson's disease. J Neurochem (2009) 109(3):755-65. doi:10.1111/j.1471-4159.2009.06001.x
40. Herring A, Ambree O, Tomm M, Habermann H, Sachser N, Paulus W, et al. Environmental enrichment enhances cellular plasticity in transgenic mice with Alzheimer-like pathology. Exp Neurol (2009) 216(1):184-92. doi:10.1016/j.expneurol.2008.11.027
41. Cao L, Liu X, Lin EJ, Wang C, Choi EY, Riban V, et al. Environmental and genetic activation of a brain-adipocyte BDNF/leptin axis causes cancer remission and inhibition. Cell (2010) 142(1):52-64. doi:10.1016/j.cell.2010.05.029
42. Nachat-Kappes R, Pinel A, Combe K, Lamas B, Farges MC, Rossary A, et al. Effects of enriched environment on COX-2, leptin and eicosanoids in a mouse model of breast cancer. PLoS One (2012) 7(12):e51525. doi:10.1371/journal.pone.0051525
43. Portou M, Baker D, Abraham D, Tsui J. The innate immune system, toll-like receptors and dermal wound healing: a review. Vascul Pharmacol (2015) 71:31-6. doi:10.1016/j.vph.2015.02.007
44. Pellicoro A, Ramachandran P, Iredale JP, Fallowfield JA. Liver fibrosis and repair: immune regulation of wound healing in a solid organ. Nat Rev Immunol (2014) 14(3):181-94. doi:10.1038/nri3623
45. Sztainberg Y, Chen A. An environmental enrichment model for mice. Nat Protoc (2010) 5(9):1535-9. doi:10.1038/nprot.2010.114
46. McIlwain KL, Merriweather MY, Yuva-Paylor LA, Paylor R. The use of behavioral test batteries: effects of training history. Physiol Behav (2001) 73(5):705-17. doi:10.1016/S0031-9384(01)00528-5
47. Kedia S, Chattarji S. Marble burying as a test of the delayed anxiogenic effects of acute immobilisation stress in mice. J Neurosci Methods (2014) 233:150-4. doi:10.1016/j.jneumeth.2014.06.012
48. Deacon RM. Digging and marble burying in mice: simple methods for in vivo identification of biological impacts. Nat Protoc (2006) 1(1):122-4. doi:10.1038/nprot.2006.20
49. Paschalidis N, Huggins A, Rowbotham NJ, Furmanski AL, Crompton T, Flower RJ, et al. Role of endogenous annexin-A1 in the regulation of thymocyte positive and negative selection. Cell Cycle (2010) 9(4):784-93. doi:10.4161/cc.9.4.10673
50. D'Acquisto F, Merghani A, Lecona E, Rosignoli G, Raza K, Buckley CD, et al. Annexin-1 modulates T-cell activation and differentiation. Blood (2007) 109(3):1095-102. doi:10.1182/blood-2006-05-022798
51. D'Acquisto F, Paschalidis N, Sampaio AL, Merghani A, Flower RJ, Perretti M. Impaired T cell activation and increased Th2 lineage commitment in annexin-1-deficient T cells. Eur J Immunol (2007) 37(11):3131-42. doi:10.1002/eji.200636792
52. Tarca AL, Draghici S, Khatri P, Hassan SS, Mittal P, Kim JS, et al. A novel signaling pathway impact analysis. Bioinformatics (2009) 25(1):75-82. doi:10.1093/bioinformatics/btn577
53. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res (2001) 29(9):e45. doi:10.1093/nar/29.9.e45
54. Scholz J, Allemang-Grand R, Dazai J, Lerch JP. Environmental enrichment is associated with rapid volumetric brain changes in adult mice. Neuroimage (2015) 109:190-8. doi:10.1016/j.neuroimage.2015.01.027
55. Leger M, Paizanis E, Dzahini K, Quiedeville A, Bouet V, Cassel JC, et al. Environmental enrichment duration differentially affects behavior and neuroplasticity in adult mice. Cereb Cortex (2015) 25(11):4048-61. doi:10.1093/cercor/bhu119
56. Beauquis J, Roig P, De Nicola AF, Saravia F. Short-term environmental enrichment enhances adult neurogenesis, vascular network and dendritic complexity in the hippocampus of type 1 diabetic mice. PLoS One (2010) 5(11):e13993. doi:10.1371/journal.pone.0013993
57. Gresack JE, Kerr KM, Frick KM. Short-term environmental enrichment decreases the mnemonic response to estrogen in young, but not aged, female mice. Brain Res (2007) 1160:91-101. doi:10.1016/j.brainres.2007.05.033
58. Rampon C, Jiang CH, Dong H, Tang YP, Lockhart DJ, Schultz PG, et al. Effects of environmental enrichment on gene expression in the brain. Proc Natl Acad Sci U S A (2000) 97(23):12880-4. doi:10.1073/pnas.97.23.12880
59. Gould TD, Dao DT, Kovacsics CE. The open field test. In: Gould TD, editor. Mood and Anxiety Related Phenotypes in Mice: Characterization using Behavioral Tests, Vol. 42. Humana Press (2009). p. 1-20.
60. Hannan AJ. Environmental enrichment and brain repair: harnessing the therapeutic effects of cognitive stimulation and physical activity to enhance experience-dependent plasticity. Neuropathol Appl Neurobiol (2014) 40(1):13-25. doi:10.1111/nan.12102
61. Baumans V. Environmental enrichment for laboratory rodents and rabbits: requirements of rodents, rabbits, and research. ILAR J (2005) 46(2):162-70. doi:10.1093/ilar.46.2.162
62. Gong S, Miao YL, Jiao GZ, Sun MJ, Li H, Lin J, et al. Dynamics and correlation of serum cortisol and corticosterone under different physiological or stressful conditions in mice. PLoS One (2015) 10(2):e0117503. doi:10.1371/journal.pone.0117503
63. Major B, Rattazzi L, Brod S, Pilipovic I, Leposavic G, D'Acquisto F. Massage-like stroking boosts the immune system in mice. Sci Rep (2015) 5:10913. doi:10.1038/srep10913
64. File SE. The rat corticosterone response: habituation and modification by chlordiazepoxide. Physiol Behav (1982) 29(1):91-5. doi:10.1016/0031-9384(82)90371-7
65. Marashi V, Barnekow A, Sachser N. Effects of environmental enrichment on males of a docile inbred strain of mice. Physiol Behav (2004) 82(5):765-76. doi:10.1016/j.physbeh.2004.05.009
66. Verhoef A, Lamb JR. Threshold signaling of human Th0 cells in activation and anergy: modulation of effector function by altered TCR ligand. J Immunol (2000) 164(11):6034-40. doi:10.4049/jimmunol.164.11.6034
67. Miner KT, Croft M. Generation, persistence, and modulation of Th0 effector cells: role of autocrine IL-4 and IFN-gamma. J Immunol (1998) 160(11):5280-7.
68. Gagliani N, Amezcua Vesely MC, Iseppon A, Brockmann L, Xu H, Palm NW, et al. Th17 cells transdifferentiate into regulatory T cells during resolution of inflammation. Nature (2015) 523(7559):221-5. doi:10.1038/nature14452
69. Tesmer LA, Lundy SK, Sarkar S, Fox DA. Th17 cells in human disease. Immunol Rev (2008) 223(1):87-113. doi:10.1111/j.1600-065X.2008.00628.x
70. Korn T, Bettelli E, Gao W, Awasthi A, Jäger A, Strom TB, et al. IL-21 initiates an alternative pathway to induce proinflammatory TH17 cells. Nature (2007) 448(7152):484-7. doi:10.1038/nature05970
71. McGeachy MJ, Bak-Jensen KS, Chen Y, Tato CM, Blumenschein W, McClanahan T, et al. TGF-β and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain TH-17 cell-mediated pathology. Nat Immunol (2007) 8(12):1390-7. doi:10.1038/ni1539
72. Brender C, Tannahill GM, Jenkins BJ, Fletcher J, Columbus R, Saris CJM, et al. Suppressor of cytokine signaling 3 regulates CD8 T-cell proliferation by inhibition of interleukins 6 and 27. Blood (2007) 110:2528-36. doi:10.1182/blood-2006-08-041541
73. Lund RJ, Löytömäki M, Naumanen T, Dixon C, Chen Z, Ahlfors H, et al. Genome-wide identification of novel genes involved in early Th1 and Th2 cell differentiation. J Immunol (2007) 178(6):3648-60. doi:10.4049/jimmunol.178.6.3648
74. Wurster AL, Withers DJ, Uchida T, White MF, Grusby MJ. Stat6 and IRS-2 cooperate in interleukin 4 (IL-4)-induced proliferation and differentiation but are dispensable for IL-4-dependent rescue from apoptosis. Mol Cell Biol (2002) 22(1):117-26. doi:10.1128/MCB.22.1.117-126.2002
75. Sekiya T, Kashiwagi I, Inoue N, Morita R, Hori S, Waldmann H, et al. The nuclear orphan receptor Nr4a2 induces Foxp3 and regulates differentiation of CD4+ T cells. Nat Commun (2011) 2:269. doi:10.1038/ncomms1272
76. Dugast E, Kiss-Toth E, Docherty L, Danger R, Chesneau M, Pichard V, et al. Identification of tribbles-1 as a novel binding partner of Foxp3 in regulatory T cells. J Biol Chem (2013) 288(14):10051-60. doi:10.1074/jbc.M112.448654
77. Cao Z, Wara AK, Icli B, Sun X, Packard RRS, Esen F, et al. Kruppel-like factor KLF10 targets transforming growth factor-β1 to regulate CD4+CD25-T cells and T regulatory cells. J Biol Chem (2009) 284(37):24914-24. doi:10.1074/jbc.M109.000059
78. Paust HJ, Turner JE, Riedel JH, Disteldorf E, Peters A, Schmidt T, et al. Chemokines play a critical role in the cross-regulation of Th1 and Th17 immune responses in murine crescentic glomerulonephritis. Kidney Int (2012) 82(1):72-83. doi:10.1038/ki.2012.101
79. Mollereau B, Manié S, Napoletano F. Getting the better of ER stress. J Cell Commun Signal (2014) 8(4):311-21. doi:10.1007/s12079-014-0251-9
80. Catanzaro G, Pucci M, Viscomi MT, Lanuti M, Feole M, Angeletti S, et al. Epigenetic modifications of Dexras 1 along the nNOS pathway in an animal model of multiple sclerosis. J Neuroimmunol (2016) 294:32-40. doi:10.1016/j.jneuroim.2016.03.009
81. Magalon K, Cantarella C, Monti G, Cayre M, Durbec P. Enriched environment promotes adult neural progenitor cell mobilization in mouse demyelination models. Eur J Neurosci (2007) 25(3):761-71. doi:10.1111/j.1460-9568.2007.05335.x
82. Moosmann S, Hutter J, Moser C, Krombach F, Huss R. Milieu-adopted in vitro and in vivo differentiation of mesenchymal tissues derived from different adult human CD34-negative progenitor cell clones. Cells Tissues Organs (2005) 179(3):91-101. doi:10.1159/000085000