Stat5 gene dosage in T cells modulates CD8+ T-cell homeostasis and attenuates contact hypersensitivity response in mice

Allergy: European Journal of Allergy and Clinical Immunology

Volumn 70, Issue 1, 2015, Pages 67-79

  Nivarthi, H ^a,e   Prchal Murphy, M ^b   Swoboda, A ^a   Hager, M ^a   Schlederer, M ^a   Kenner, L ^a   Tuckermann, J ^c   Sexl, V ^b   Moriggl, R ^a   Ermakova, O ^d,f  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^c UNIVERSITY OF ULM   (Germany)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY EMBL   (Italy)

^e ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^f Istituto di Biologia Cellulare e Neurobiologia IBCN CNR   (Italy)

Author keywords

allergic contact dermatitis; Stat5; T cells

Indexed keywords

INTERLEUKIN 2; INTERLEUKIN 4; STAT5 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BCL2 GENE; CD8+ T LYMPHOCYTE; CELL CYCLE; CELL SURVIVAL; CONTACT ALLERGY; CONTACT HYPERSENSITIVITY ASSAY; CONTROLLED STUDY; FLOW CYTOMETRY; GENE; GENE DOSAGE; GENE EXPRESSION; HOMEOSTASIS; IMMUNOASSAY; LYMPH NODE; MONOCYTE; MOUSE; NONHUMAN; NULL ALLELE; PIM1 GENE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SPLEEN; STAT5 GENE; ANIMAL; BLOOD; CONTACT DERMATITIS; DISEASE MODEL; GENETICS; GERM CELL; HAPLOINSUFFICIENCY; IMMUNOLOGY; LEUKOCYTE COUNT; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; METABOLISM; THYMUS; TRANSGENIC MOUSE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; DERMATITIS, CONTACT; DISEASE MODELS, ANIMAL; GENE DOSAGE; GERM CELLS; HAPLOINSUFFICIENCY; HOMEOSTASIS; LEUKOCYTE COUNT; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; MICE; MICE, TRANSGENIC; STAT5 TRANSCRIPTION FACTOR; THYMUS GLAND;

EID: 84915745823     PISSN: 01054538     EISSN: 13989995     Source Type: Journal    
DOI: 10.1111/all.12535     Document Type: Article

References (50)

1. Peiser M, Tralau T, Heidler J, Api AM, Arts JH, Basketter DA, et al. Allergic contact dermatitis: epidemiology, molecular mechanisms, in vitro methods and regulatory aspects. Current knowledge assembled at an international workshop at BfR, Germany. Cell Mol Life Sci 2012; 69: 763-781.
2. Xu H, Banerjee A, Dilulio NA, Fairchild RL,. Development of effector CD8+ T cells in contact hypersensitivity occurs independently of CD4+ T cells. J Immunol 1997; 158: 4721-4728.
3. Bour H, Peyron E, Gaucherand M, Garrigue JL, Desvignes C, Kaiserlian D, et al. Major histocompatibility complex class I-restricted CD8+ T cells and class II-restricted CD4+ T cells, respectively, mediate and regulate contact sensitivity to dinitrofluorobenzene. Eur J Immunol 1995; 25: 3006-3010.
4. Cavani A, Mei D, Guerra E, Corinti S, Giani M, Pirrotta L, et al. Patients with allergic contact dermatitis to nickel and nonallergic individuals display different nickel-specific T cell responses. Evidence for the presence of effector CD8+ and regulatory CD4+ T cells. J Invest Dermatol 1998; 111: 621-628.
5. Cavani A, Nasorri F, Prezzi C, Sebastiani S, Albanesi C, Girolomoni G,. Human CD4+ T lymphocytes with remarkable regulatory functions on dendritic cells and nickel-specific Th1 immune responses. J Invest Dermatol 2000; 114: 295-302.
6. Gorbachev AV, Fairchild RL,. Regulatory role of CD4+ T cells during the development of contact hypersensitivity responses. Immunol Res 2001; 24: 69-77.
7. Martin S, Lappin MB, Kohler J, Delattre V, Leicht C, Preckel T, et al. Peptide immunization indicates that CD8+ T cells are the dominant effector cells in trinitrophenyl-specific contact hypersensitivity. J Invest Dermatol 2000; 115: 260-266.
8. Ferbeyre G, Moriggl R,. The role of Stat5 transcription factors as tumor suppressors or oncogenes. Biochim Biophys Acta 2011; 1815: 104-114.
9. Heltemes-Harris LM, Farrar MA,. The role of STAT5 in lymphocyte development and transformation. Curr Opin Immunol 2012; 24: 146-152.
10. Nivarthi H, Friedbichler K, Moriggl R,. Stat5 as a hematopoietic master regulator for differentiation and neoplasia development. In:, Decher Th,., Muller M, editors. Jak-Stat Signaling: From Basics to Disease. Vienna: Springer-Verlag GmbH, 2012: 153-169.
11. Hoelbl A, Kovacic B, Kerenyi MA, Simma O, Warsch W, Cui Y, et al. Clarifying the role of Stat5 in lymphoid development and Abelson-induced transformation. Blood 2006; 107: 4898-4906.
12. Yao Z, Cui Y, Watford WT, Bream JH, Yamaoka K, Hissong BD, et al. Stat5a/b are essential for normal lymphoid development and differentiation. Proc Natl Acad Sci USA 2006; 103: 1000-1005.
13. Burchill MA, Goetz CA, Prlic M, O'Neil JJ, Harmon IR, Bensinger SJ, et al. Distinct effects of STAT5 activation on CD4+ and CD8+ T cell homeostasis: development of CD4+CD25+ regulatory T cells versus CD8+ memory T cells. J Immunol 2003; 171: 5853-5864.
14. Kelly JA, Spolski R, Kovanen PE, Suzuki T, Bollenbacher J, Pise-Masison CA, et al. Stat5 synergizes with T cell receptor/antigen stimulation in the development of lymphoblastic lymphoma. J Exp Med 2003; 198: 79-89.
15. Pelengaris S, Khan M, Evan G,. c-MYC: more than just a matter of life and death. Nat Rev Cancer 2002; 2: 764-776.
16. Wilson A, Murphy MJ, Oskarsson T, Kaloulis K, Bettess MD, Oser GM, et al. c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev 2004; 18: 2747-2763.
17. Kelly PN, Strasser A,. The role of Bcl-2 and its pro-survival relatives in tumourigenesis and cancer therapy. Cell Death Differ 2011; 18: 1414-1424.
18. Johnson DG, Walker CL,. Cyclins and cell cycle checkpoints. Annu Rev Pharmacol Toxicol 1999; 39: 295-312.
19. Shah N, Pang B, Yeoh KG, Thorn S, Chen CS, Lilly MB, et al. Potential roles for the PIM1 kinase in human cancer-a molecular and therapeutic appraisal. Eur J Cancer 2008; 44: 2144-2151.
20. Chen B, Yi B, Mao R, Liu H, Wang J, Sharma A, et al. Enhanced T cell lymphoma in NOD.Stat5b transgenic mice is caused by hyperactivation of Stat5b in CD8+ thymocytes. PLoS ONE 2013; 8: e56600.
21. Gouilleux-Gruart V, Gouilleux F, Desaint C, Claisse JF, Capiod JC, Delobel J, et al. STAT-related transcription factors are constitutively activated in peripheral blood cells from acute leukemia patients. Blood 1996; 87: 1692-1697.
22. Migone TS, Lin JX, Cereseto A, Mulloy JC, O'Shea JJ, Franchini G, et al. Constitutively activated Jak-STAT pathway in T cells transformed with HTLV-I. Science 1995; 269: 79-81.
23. Danial NN, Pernis A, Rothman PB,. Jak-STAT signaling induced by the v-abl oncogene. Science 1995; 269: 1875-1877.
24. Cooper DN, Krawczak M, Polychronakos C, Tyler-Smith C, Kehrer-Sawatzki H,. Where genotype is not predictive of phenotype: towards an understanding of the molecular basis of reduced penetrance in human inherited disease. Hum Genet 2013; 132: 1077-1130.
25. Ermakova O, Piszczek L, Luciani L, Cavalli FM, Ferreira T, Farley D, et al. Sensitized phenotypic screening identifies gene dosage sensitive region on chromosome 11 that predisposes to disease in mice. EMBO Mol Med 2011; 3: 50-66.
26. Cui Y, Riedlinger G, Miyoshi K, Tang W, Li C, Deng CX, et al. Inactivation of Stat5 in mouse mammary epithelium during pregnancy reveals distinct functions in cell proliferation, survival, and differentiation. Mol Cell Biol 2004; 24: 8037-8047.
27. Teglund S, McKay C, Schuetz E, van Deursen JM, Stravopodis D, Wang D, et al. Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell 1998; 93: 841-850.
28. Wildin RS, Wang HU, Forbush KA, Perlmutter RM,. Functional dissection of the murine lck distal promoter. J Immunol 1995; 155: 1286-1295.
29. Prchal-Murphy M, Semper C, Lassnig C, Wallner B, Gausterer C, Teppner-Klymiuk I, et al. TYK2 kinase activity is required for functional type I interferon responses in vivo. PLoS One 2012; 7: e39141.
30. Lehtimaki S, Savinko T, Lahl K, Sparwasser T, Wolff H, Lauerma A, et al. The temporal and spatial dynamics of Foxp3 + Treg cell-mediated suppression during contact hypersensitivity responses in a murine model. J Invest Dermatol 2012; 132: 2744-2751.
31. Christensen AD, Haase C,. Immunological mechanisms of contact hypersensitivity in mice. APMIS 2012; 120: 1-27.
32. Zhang X, Nakajima T, Goronzy JJ, Weyand CM,. Tissue trafficking patterns of effector memory CD4+ T cells in rheumatoid arthritis. Arthritis Rheum 2005; 52: 3839-3849.
33. Moriggl R, Sexl V, Piekorz R, Topham D, Ihle JN,. Stat5 activation is uniquely associated with cytokine signaling in peripheral T cells. Immunity 1999; 11: 225-230.
34. Gocinski BL, Tigelaar RE,. Roles of CD4+ and CD8+ T cells in murine contact sensitivity revealed by in vivo monoclonal antibody depletion. J Immunol 1990; 144: 4121-4128.
35. Saint-Mezard P, Rosieres A, Krasteva M, Berard F, Dubois B, Kaiserlian D, et al. Allergic contact dermatitis. Eur J Dermatol 2004; 14: 284-295.
36. Tripathi P, Kurtulus S, Wojciechowski S, Sholl A, Hoebe K, Morris SC, et al. STAT5 is critical to maintain effector CD8+ T cell responses. J Immunol 2010; 185: 2116-2124.
37. Yao Z, Kanno Y, Kerenyi M, Stephens G, Durant L, Watford WT, et al. Nonredundant roles for Stat5a/b in directly regulating Foxp3. Blood 2007; 109: 4368-4375.
38. Valk E, Zahn S, Knop J, Becker D,. JAK/STAT pathways are not involved in the direct activation of antigen-presenting cells by contact sensitizers. Arch Dermatol Res 2002; 294: 163-167.
39. Bell BD, Kitajima M, Larson RP, Stoklasek TA, Dang K, Sakamoto K, et al. The transcription factor STAT5 is critical in dendritic cells for the development of TH2 but not TH1 responses. Nat Immunol 2013; 14: 364-371.
40. Kehren J, Desvignes C, Krasteva M, Ducluzeau MT, Assossou O, Horand F, et al. Cytotoxicity is mandatory for CD8(+) T cell-mediated contact hypersensitivity. J Exp Med 1999; 189: 779-786.
41. Grange M, Verdeil G, Arnoux F, Griffon A, Spicuglia S, Maurizio J, et al. Active STAT5 Regulates T-bet and Eomesodermin Expression in CD8 T Cells and Imprints a T-bet-Dependent Tc1 Program with Repressed IL-6/TGF-beta1 Signaling. J Immunol 2013; 191: 3712-3724.
42. Gewinner C, Hart G, Zachara N, Cole R, Beisenherz-Huss C, Groner B,. The coactivator of transcription CREB-binding protein interacts preferentially with the glycosylated form of Stat5. J Biol Chem 2004; 279: 3563-3572.
43. Mueller KM, Themanns M, Friedbichler K, Kornfeld JW, Esterbauer H, Tuckermann JP, et al. Hepatic growth hormone and glucocorticoid receptor signaling in body growth, steatosis and metabolic liver cancer development. Mol Cell Endocrinol 2012; 361: 1-11.
44. Jin H, Oyoshi MK, Le Y, Bianchi T, Koduru S, Mathias CB, et al. IL-21R is essential for epicutaneous sensitization and allergic skin inflammation in humans and mice. J Clin Invest 2009; 119: 47-60.
45. Sonkoly E, Muller A, Lauerma AI, Pivarcsi A, Soto H, Kemeny L, et al. IL-31: a new link between T cells and pruritus in atopic skin inflammation. J Allergy Clin Immunol 2006; 117: 411-417.
46. Soumelis V, Reche PA, Kanzler H, Yuan W, Edward G, Homey B, et al. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol 2002; 3: 673-680.
47. Ando T, Xiao W, Gao P, Namiranian S, Matsumoto K, Tomimori Y, et al. Critical role for mast cell Stat5 activity in skin inflammation. Cell Rep 2014; 6: 366-376.
48. Liu Y, Yang T, Li H, Li MH, Liu J, Wang YT, et al. BD750, a benzothiazole derivative, inhibits T cell proliferation by affecting the JAK3/STAT5 signalling pathway. Br J Pharmacol 2013; 168: 632-643.
49. Bachmann M, Kosan C, Xing PX, Montenarh M, Hoffmann I, Moroy T,. The oncogenic serine/threonine kinase Pim-1 directly phosphorylates and activates the G2/M specific phosphatase Cdc25C. Int J Biochem Cell Biol 2006; 38: 430-443.
50. Perera GK, Ainali C, Semenova E, Hundhausen C, Barinaga G, Kassen D, et al. Integrative biology approach identifies cytokine targeting strategies for psoriasis. Sci Transl Med 2014; 6: 223ra222.