γδ T Cells Acquire Effector Fates in the Thymus and Differentiate into Cytokine-Producing Effectors in a Listeria Model of Infection Independently of CD28 Costimulation

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Laird, Renee M ^a,b   Wolf, Benjamin J ^a,c   Princiotta, Michael F ^a   Hayes, Sandra M ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b NAVAL MEDICAL RESEARCH CENTER   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; GAMMA INTERFERON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL LINEAGE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FLOW CYTOMETRY; GAMMA DELTA T LYMPHOCYTE; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLUCOSE UTILIZATION; GLYCOLYSIS; IN VITRO STUDY; LISTERIA MONOCYTOGENES; LISTERIOSIS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; THYMOCYTE;

ANIMALS; ANTIGENS, CD28; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; FLOW CYTOMETRY; GLUCOSE; HOST-PATHOGEN INTERACTIONS; INTERFERON-GAMMA; INTERLEUKIN-17; LISTERIA MONOCYTOGENES; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTE SUBSETS; THYMUS GLAND;

EID: 84877327999     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063178     Document Type: Article

References (64)

1. Jenkins MK, Taylor PS, Norton SD, Urdahl KB, (1991) CD28 delivers a costimulatory signal involved in antigen-specific IL-2 production by human T cells. J Immunol 147: 2461-2466.
2. Harding FA, McArthur JG, Gross JA, Raulet DH, Allsion JP, (1992) CD28-mediated signalling costimulates murine T cells and prevents induction of anergy in T cell clones. Nature 356: 607-609.
3. Tan P, Anasetti C, Hansen JA, Ledbetter JA, Linsley PA, (1993) Induction of alloantigen specific hypo-responsiveness in human T lymphocytes by blocking interaction of CD28 with its natural ligand B7/BB-1. J Exp Med 177: 165-173.
4. Boise LH, Minn AJ, Noel PJ, June CH, Accavitti MA, et al. (1995) CD28 costimulation can promote T cell survival by enhancing the expression of Bcl-xL. Immunity 3: 87-98.
5. Frauwirth KA, Riley JL, Harris MH, Parry RV, Rathmell JC, et al. (2002) The CD28 signaling pathway regulates glucose metabolism. Immunity 16: 769-777.
6. Jacobs SR, Herman CE, Maciver NJ, Wofford JA, Wieman HL, et al. (2008) Glucose uptake is limiting in T cell activation and requires CD28-mediated Akt-dependent and independent pathways. J Immunol 180: 4476-4486.
7. Lindsten T, June CH, Ledbetter JA, Stella G, Thompson CB, (1989) Regulation of lymphokines messenger RNA stability by a surface-mediated T cell activation pathway. Science 244: 339-343.
8. Miller J, Baker C, Cook K, Graf B, Sanchez-Lockhart M, et al. (2009) Two pathways of costimulation through CD28. Immunol Res 45: 159-172.
9. Butte MJ, Lee SJ, Jesneck J, Keir ME, Haining WN, et al. (2012) CD28 costimulation regulates genome-wide effects on alternative splicing. PLoS One 7: e40032.
10. Benlagha K, Kyin T, Beavis A, Teyton L, Bendelac A, (2002) A thymic precursor to the NK T cell lineage. Science 296: 553-555.
11. Pellicci DG, Hammond KJ, Uldrich AP, Baxter AG, Smyth MJ, et al. (2002) A natural killer T (NKT) cell developmental pathway involving a thymus-dependent NK1.1-CD4+ CD1d-dependent precursor stage. J Exp Med 195: 835-844.
12. Benlagha K, Wei DG, Veiga J, Teyton L, Bendelac A, (2005) Characterization of the early stages of thymic NKT cell development. J Exp Med 202: 485-492.
13. Asano M, Toda M, Sakaguchi N, Sakaguchi S, (1996) Autoimmune disease as a consequence of developmental abnormality of a T cell population. J Exp Med 184: 387-396.
14. Bautista JL, Lio C-WJ, Lathrop SK, Forbush K, Liang Y, et al. (2009) Intraclonal competition limits regulatory T cell fate determination in the thymus. Nat Immunol 10: 610-617.
15. Williams JA, Lumsden JM, Yu X, Feigenbaum L, Zhang J, et al. (2008) Regulation of thymic NKT cell development by the B7-CD28 costimulatory pathway. J Immunol 181: 907-917.
16. Zheng X, Zhang H, Yin L, Wan C-R, Liu Y, et al. (2008) Modulation of NKT cell development by B7-CD28 interaction: An expanding horizon for costimulation. PLoS One 3: e2703.
17. Tai X, Cowan M, Feigenbaum L, Singer A, (2005) CD28 costimulation of developing thymocytes induces Foxp3 expression and regulatory T cell differentiation independently of interleukin 2. Nat Immunol 6: 152-162.
18. Jensen KD, Su X, Shin S, Li L, Youssef S, et al. (2008) Thymic selection determines γδ T cell effector fate: antigen-naïve cells make interleukin-17 and antigen-experienced cells make interferon γ. Immunity 29: 90-100.
19. Ribot JC, deBarros A, Pang DJ, Neves JF, Peperzak V, et al. (2009) CD27 is a thymic determinant of the balance between interferon-γ- and interleukin-17-producing γδ T cell subsets. Nat Immunol 10: 427-436.
20. Awasthi A, Riol-Blanco L, Jäger A, Korn T, Pot C, et al. (2009) Cutting edge: IL-23 receptor gfp reporter mice reveal distinct populations of IL-17-producing cells. J Immunol 182: 5904-5908.
21. Sim GK, Olsson C, Augustin A, (1995) Commitment and maintenance of the αβ and γδ T cell lineages. J Immunol. 154: 5821-5831.
22. Wolf BJ, Princiotta MF (2013) Processing of recombinant Listeria monocytogenes proteins for MHC Class I presentation follows a dedicated, high-efficiency pathway. J Immunol 1201660.
23. Wolf BJ, Princiotta MF, (2011) Viral and bacterial minigene products are presented by MHC class I molecules with similar efficiencies. Mol Immunol 48: 463-471.
24. Telford W., M. Murga, T. Hawley, R. Hawley, B. Packard, A. Komoriya, F. Haas, and C. Hubert. 2005. DPSS yellow-green 561-nm lasers for improved fluorochrome detection by flow cytometry. Cytometry Part A 68A: 36-44.
25. Haas JD, González FH, Schmitz S, Chennupati V, Föhse L, et al. (2009) CCR6 and NK1.1 distinguish between IL-17A and IFN-γ-producing γδ effector T cells. Eur J Immunol 39: 3488-3497.
26. Martin B, Hirota K, Cua DJ, Stockinger B, Veldhoen M, (2009) Interleukin-17-producing γδ T cells selectively expand in response to pathogen products and environmental signals. Immunity 31: 321-330.
27. Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, et al. (2009) Interleukin-1 and IL-23 induce innate IL-17 production from γδ T cells, amplifying Th17 responses and autoimmunity. Immunity 31: 331-341.
28. Hayes SM, Li L, Love PE, (2005) TCR signal strength influences αβ/γδ lineage fate. Immunity 22: 583-593.
29. Williams JA, Hathcock KS, Klug D, Harada Y, Choudhury B, et al. (2005) Regulated costimulation in the thymus is critical for T cell development: dysregulated costimulation can bypass the pre-TCR checkpoint. J Immunol 175: 199-207.
30. Kang J, Fehling HJ, Laplace C, Malissen M, Cado D, et al. (1998) T cell receptor γ gene regulatory sequences prevent the function of a novel TCRγ/pTα pre-T cell receptor. Immunity 8: 713-731.
31. Hayes SM, Love PE, (2002) Distinct structure and signaling potential of the γδTCR complex. Immunity 16: 827-838.
32. Silva-Santos B, Pennington DJ, Hayday AC, (2005) Lymphotoxin-mediated regulation of γδ cell differentiation by αβ T cell progenitors. Science 307: 925-928.
33. Laird RM, Hayes SM, (2010) Roles of the Src tyrosine kinases Lck and Fyn in regulating γδTCR signal strength. PLoS One 5: e8899.
34. Laird RM, Laky K, Hayes SM, (2010) Unexpected role for the B cell-specific Src family kinase B lymphoid kinase in the development of IL-17-producing γδ T cells. J Immunol 185: 6518-6527.
35. Park K, He X, Lee H-O, Hua X, Wiest D, et al. (2010) TCR-mediated ThPOK induction promotes development of mature (CD24-) γδ thymocytes. EMBO J 29: 2329-2341.
36. Hamada S, Umemura M, Shiono T, Hara H, Kishihara K, et al. (2008) Importance of Vδ1 γδ T cells expressing interferon-γ and interleukin-17A in innate protection against Listeria monocytogenes infection. Immunology 125: 170-177.
37. Hamada S, Umemura M, Shiono T, Tanaka K, Yahagi A, et al. (2008) IL-17A produced by γδ T cells plays a critical role in innate immunity against Listeria monocytogenes infection in the liver. J Immunol 181: 3456-3463.
38. Shedlock DJ, Whitmire JK, Tan J, MacDonald AS, Ahmed R, et al. (2003) Role of CD4 T cell help and costimulation in CD8 T cell responses during Listeria monocytogenes infection. J Immunol 170: 2053-2063.
39. Brzoza KL, Rockel AB, Hiltbold EM, (2004) Cytoplasmic entry of Listeria monocytogenes enhances dendritic cell maturation and T cell differentiation and function. J Immunol 173: 2641-2651.
40. Xu S, Han Y, Xu X, Bao Y, Zhang M, et al. (2010) IL-17A-producing γδ T cells promote CTL responses against Listeria monocytogenes infection by enhancing dendritic cell cross-presentation. J Immunol 185: 5879-5887.
41. Meeks KD, Sieve AN, Kolls JK, Ghilardi N, Berg RE, (2009) IL-23 is required for protection against systemic infection with Listeria monocytogenes. J Immunol 183: 8026-8034.
42. Mittrücker HW, Kursar M, Kohler A, Hurwitz R, Kaufmann SHE, (2001) Role of CD28 for the generation and expansion of antigen-specific CD8+ T lymphocytes during infection with Listeria monocytogenes. J Immunol 167: 5620-5627.
43. Fu Y, Maianu L, Melbert BR, Garvey WT, (2004) Facilitative glucose transporter gene expression in human lymphocytes, monocytes, and macrophages: a role for GLUT isoforms 1,3 and 5 in the immune response and foam cell formation. Blood Cells Mol Dis 32: 182-190.
44. Maratou E, Dimitriadis G, Kollias A, Boutati E, Lambadiari, et al, (2007) Glucose transporter expression on the plasma membrane of resting and activated white blood cells. Eur J Clin Invest 37: 282-290.
45. Yu Q, Erman B, Bhandoola A, Sharrow S, Singer A, (2003) In vitro evidence that cytokine receptor signal are required for differentiation of double positive thymocytes into functionally mature CD8+ T cells. J Exp Med 197: 475-487.
46. Simpson IA, Dwyer D, Malide D, Moley KH, Travis A, et al. (2008) The facilitative glucose transporter GLUT3: 20 years of distinction. Am J Physiol Endocrinol Metab 295: E242-E253.
47. Ribot JC, Debarros A, Mancio-Silva L, Pamplona A, Silva-Santos B, (2012) B7-CD28 costimulatory signals control the survival and proliferation of murine and human γδ T cells via IL-2 production. J Immunol 189: 1202-1208.
48. Acuto O, Michel F, (2003) CD28-mediated co-stimulation: a quantitative support for TCR signaling. Nat Rev Immunol 3: 939-951.
49. Wilder MS, Sword CP, (1967) Mechanisms of pathogenesis in Listeria monocytogenes infection III. Carbohydrate metabolism. J Bacteriol 93: 538-543.
50. Elased K, Playfair JH, (1994) Hypoglycemia and hyperinsulinemia in rodent models of severe malaria infection. Infect Immun 62: 5157-5160.
51. Li C, Corraliza I, Langhorne J, (1999) A defect in Interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice. Infect Immun 67: 4435-4442.
52. Zheng X, Gao J-X, Chang X, Wang Y, Liu Y, et al. (2004) B7-CD28 interaction promotes proliferation and survival but suppressed differentiation of CD4-CD8- T cells in the thymus. J Immunol 173: 2253-2261.
53. Lind EF, Prockop SE, Porritt HE, Petrie HT, (2001) Mapping precursor movement through the postnatal thymus reveals specific microenvironments supporting defined stages of early lymphoid development. J Exp Med 194: 127-134.
54. Peschon JJ, Morrissey PJ, Grabstein KH, Ramsdell FJ, Maraskovsky E, et al. (1994) Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J Exp Med 180: 1955-1960.
55. Von Freeden-Jeffry U, Solvason N, Howard M, Murray R, (1997) The earliest T lineage-committed cells depend on IL-7 for Bcl-2 expression and normal cell cycle progression. Immunity 7: 147-154.
56. Agosti V, Corbacioglu S, Ehlers I, Waskow C, Sommer G, et al. (2004) Critical role for the Kit-mediated Src kinase but not PI 3-kinase signaling in pro-T and pro-B cell development. J Exp Med 199: 867-878.
57. Shah DK, Hager-Theorides AL, Outram SV, Ross SE, Varas A, et al. (2004) Reduced thymocyte development in sonic hedgehog knockout embryos. J Immunol 172: 2296-2306.
58. Huang J, Garrett KP, Pelayo R, Zúñiga-Pflücker JC, Petrie HT, et al. (2005) Propensity of adult lymphoid progenitors to progress to DN2/3 stage thymocytes with Notch receptor ligation. J Immunol 175: 4858-4865.
59. Teague TK, Tan C, Marino JH, Davs BK, Taylor AA, et al. (2010) CD28 expression redefines thymocyte development during the pre-T to DP transition. Int Immunol 22: 387-397.
60. Marko AJ, Miller RA, Kelman A, Frauwirth KA, (2010) Induction of glucose metabolism in stimulated T lymphocytes is regulated by mitogen-activated protein kinase signaling. PLoS One 5: e15425.
61. Ganguly A, MacKnight RA, Raychaudhuri S, Shin BC, Ma Z, et al. (2007) Glucose transporter isoform-3 mutations cause early pregnancy loss and fetal growth restriction. Am J Physiol Endocrinol Metab 292: E1241-E1255.
62. Rathmell JC, Vander Heiden MG, Harris MH, Frauwirth, Thompson CB, (2000) In the absence of extrinsic signals, nutrient utilization by lymphocytes is insufficient to maintain either cell size or viability. Mol Cell 6: 683-692.
63. Wofford JA, Wieman HL, Jacobs SR, Zhao Y, Rathmell JC, (2008) IL-7 promotes Glut1 trafficking and glucose uptake via STAT5-mediated activation of Akt to support T-cell survival. Blood 111: 2101-2111.
64. Aydintung MK, Roark CL, Chain JL, Born WK, O'Brien RL, (2008) Macrophages express multiple ligands for γδ TCRs. Mol Immunol 45: 3253-3263.