Abortive activation of CD4 T cell responses during competitive priming in vivo

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 21, 2009, Pages 8647-8652

  Weaver, Jason M ^a   Chaves, Francisco A ^a   Sant, Andrea J ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Competition; Immunodominance; MHC; Peptide; T cell activation

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL EXPANSION; CELL SPECIFICITY; CONTROLLED STUDY; IN VIVO STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MOUSE; NONHUMAN; PRIMARY IMMUNE RESPONSE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN VARIANT;

AMINO ACID SEQUENCE; ANIMALS; ANTIGEN PRESENTATION; CD4-POSITIVE T-LYMPHOCYTES; EPITOPES; KINETICS; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; PEPTIDES;

EID: 66649110510     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0811584106     Document Type: Article

References (50)

1. Lazarski CL, et al. (2005) The kinetic stability of MHC class II:peptide complexes is a key parameter that dictates immunodominance. Immunity 23:29-40. (Pubitemid 41019655)
2. Nanda N, Sant AJ (2000) DM determines the cryptic and immunodominant fate of T cell epitopes. J Exp Med 192:781-788.
3. Nanda NK, Bikoff EK (2005) DM peptide-editing function leads to immunodominance in CD4 T cell responses in vivo. J Immunol 175:6473-6480. (Pubitemid 41598889)
4. Lazarski CA, Chaves FA, Sant AJ (2006) The impact of DM on MHC class II-restricted antigen presentation can be altered by manipulation of MHC-peptide kinetic stability. J Exp Med 203:1319-1328. (Pubitemid 43736600)
5. Weaver JM, et al. (2008) Immunodominance of CD4 T cells to foreign antigens is peptide intrinsic and independent of molecular context: Implications for vaccine design. J Immunol 181:3039-3048.
6. Fazilleau N, McHeyzer-Williams LJ, McHeyzer-Williams MG (2007) Local development of effector and memory T helper cells. Curr Opin Immunol 19:259-267. (Pubitemid 46687009)
7. Germain RN, Miller MJ, Dustin M, Nussenzweig MC (2006) Dynamic imaging of the immune system: Progress, pitfalls and promise. Nat Rev Immunol 6:497-507. (Pubitemid 43980522)
8. Henrickson S, von Andrian U (2007) Single-cell dynamics of T-cell priming. Curr Opin Immunol 19:249-258. (Pubitemid 46687018)
9. Margot CD, Ford ML, Evavold BD (2005) Amelioration of established experimental autoimmune encephalomyelitis by an MHC anchor-substituted variant proteolipid protein 139-151. J Immunol 174:3352-3358. (Pubitemid 40354039)
10. Skokos D, et al. (2007) Peptide-MHC potency governs dynamic interactions between T cells and dendritic cells in lymph nodes. Nat Immunol 8:835-844. (Pubitemid 47099036)
11. Miller M, Safrina O, Parker I, Cahalan M (2004) Imaging the single cell dynamics of CD4 T cell activation by dendritic cells in lymph nodes. J Exp Med 200:847-856. (Pubitemid 39362921)
12. Bousso P, Robey E (2003) Dynamics of CD8+ T cell priming by dendritic cells in intact lymph nodes. Nat Immunol 4:579-585. (Pubitemid 36701342)
13. Gunzer M, et al. (2000) Antigen presentation in extracellular matrix: Interactions of T cells with dendritic cells are dynamic, short lived, and sequential. Immunity 13:323-332.
14. Celli S, Lemaitre F, Bousso P (2007) Real-time manipulation of T cell- dendritic cell interactions in vivo reveals the importance of prolonged contacts for CD4 T cell activation. Immunity 27:625-634. (Pubitemid 47615508)
15. Hugues S, et al. (2004) Distinct T cell dynamics in lymph nodes during the induction of tolerance and immunity. Nat Immunol 5:1235-1242. (Pubitemid 41057738)
16. Shakhar G, et al. (2005) Stable T cell-dendritic cell interactions precede the development of both tolerance and immunity in vivo. Nat Immunol 6:707-714. (Pubitemid 41716744)
17. Mempel T, Henrickson S, von Andrian U (2004) T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427:154-159. (Pubitemid 38094955)
18. Huang AY, Qi H, Germain RN (2004) Illuminating the landscape of in vivo immunity: Insights from dynamic in situ imaging of secondary lymphoid tissues. Immunity 21:331-339. (Pubitemid 39208334)
19. Henrickson S, et al. (2008) T cell sensing of antigen dose governs interactive behavior with dendritic cells and sets a threshold for T cell activation. Nat Immunol 9:282-291.
20. Tadokoro C, et al. (2006) Regulatory T cells inhibit stable contacts between CD4+ T cells and dendritic cells in vivo. J Exp Med 203:489-492.
21. Tang Q, et al. (2006) Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat Immunol 7:83-92. (Pubitemid 41823872)
22. Zinselmeyer BH, et al. (2005) In situ characterization of CD4 T cell behavior in mucosal and systemic lymphoid tissues during the induction of oral priming and tolerance. J Exp Med 201:1815-1823. (Pubitemid 41002900)
23. Fazilleau N, et al. (2007) Lymphoid reservoirs of antigen-specific memory T helper cells. Nat Immunol 8:753-761. (Pubitemid 46965351)
24. Qi H, Cannons JL, Klauschen F, Schwartzberg PL, Germain RN (2008) SAP-controlled T-B cell interactions underlie germinal centre formation. Nature 455:764-769.
25. Buus S, Sette A, Colon SM, Miles C, Grey HM (1987) The relation between major histocompatibility complex (MHC) restriction and the capacity of Ia to bind immunogenic peptides. Science 235:1353-1358. (Pubitemid 17041654)
26. Adorini L, et al. (1988) Interaction of an immunodominant epitope with Ia molecules in T-cell activation. Proc Natl Acad Sci USA 85:5181-5185. (Pubitemid 18205282)
27. Willis RA, Kappler J, Marrack P (2006) CD8 T cell competition for dendritic cells in vivo is an early event in activation. Proc Natl Acad Sci USA 103:12063-12068. (Pubitemid 44215811)
28. Itano AA, et al. (2003) Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity 19:47-57. (Pubitemid 36859900)
29. Catron DM, Rusch LK, Hataye J, Itano AA, Jenkins MK (2006) CD4+ T cells that enter the draining lymph nodes after antigen injection participate in the primary response and become central-memory cells. J Exp Med 203:1045-1054.
30. Panus JF, McHeyzer-Williams LJ, McHeyzer-Williams MG (2000) Antigen-specific T helper cell function: Differential cytokine expression in primary and memory responses. J Exp Med 192:1301-1316. (Pubitemid 30207678)
31. Savage PA, Boniface JJ, Davis MM (1999) A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity 10:485-492. (Pubitemid 29205484)
32. Malherbe L, Hausl C, Teyton L, McHeyzer-Williams MG (2004) Clonal selection of helper T cells is determined by an affinity threshold with no further skewing of TCR binding properties. Immunity 21:669-679. (Pubitemid 39487890)
33. Busch DH, Pamer EG (1999) T cell affinity maturation by selective expansion during infection. J Exp Med 189:701-710. (Pubitemid 29193371)
34. Mikszta JA, McHeyzer-Williams LJ, McHeyzer-Williams MG (1999) Antigen-driven selection of TCR in vivo: Related TCR α-chains pair with diverse TCR α-chains. J Immunol 163:5978-5988.
35. McHeyzer-Williams LJ, Panus JF, Mikszta JA, McHeyzer-Williams MG (1999) Evolution of antigen-specific T cell receptors in vivo: Preimmune and antigen-driven selection of preferred complementarity-determining region 3 (CDR3) motifs. J Exp Med 189:1823-1838. (Pubitemid 29272699)
36. Hudrisier D, Bongrand P (2002) Intercellular transfer of antigen-presenting cell determinants onto T cells: Molecular mechanisms and biological significance. FASEB J 16:477-486. (Pubitemid 34273231)
37. LeMaoult J, Caumartin J, Carosella ED (2007) Exchanges of membrane patches (trogocytosis) split theoretical and actual functions of immune cells. Hum Immunol 68:240-243. (Pubitemid 46497520)
38. Obst R, van Santen H, Mathis D, Benoist C (2005) Antigen persistence is required throughout the expansion phase of a CD4(+) T cell response. J Exp Med 201:1555-1565. (Pubitemid 40721001)
39. Yarke CA, et al. (2008) Proliferating CD4 T cells undergo immediate growth arrest upon cessation of TCR signaling in vivo. J Immunol 180:156-162.
40. Sakaguchi S (2004) Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 22:531-562. (Pubitemid 38680433)
41. Shevach E, et al. (2006) The lifestyle of naturally occurring CD4+CD25+Foxp3+ regulatory T cells. Immunol Rev 212:60-73. (Pubitemid 44224153)
42. Hu H, et al. (2001) CD4(+) T cell effectors can become memory cells with high efficiency and without further division. Nat Immunol 2:705-710. (Pubitemid 32747159)
43. Swain SL, Hu H, Huston G (1999) Class II-independent generation of CD4 memory T cells from effectors. Science 286:1381-1383. (Pubitemid 129516244)
44. Seddon B, Tomlinson P, Zamoyska R (2003) Interleukin 7 and T cell receptor signals regulate homeostasis of CD4 memory cells. Nat Immunol 4:680-686. (Pubitemid 36874445)
45. Purton JF, et al. (2007) Antiviral CD4+ memory T cells are IL-15 dependent. J Exp Med 204:951-961. (Pubitemid 46631622)
46. Kassiotis G, Garcia S, Simpson E, Stockinger B (2002) Impairment of immunological memory in the absence of MHC despite survival of memory T cells. Nat Immunol 3:244-250. (Pubitemid 34213425)
47. Kassiotis G, Gray D, Kiafard Z, Zwirner J, Stockinger B (2006) Functional specialization of memory Th cells revealed by expression of integrin CD49b. J Immunol 177:968-975. (Pubitemid 44036598)
48. Godebu E, Summers-Torres D, Lin MM, Baaten BJ, Bradley LM (2008) Polyclonal adaptive regulatory CD4 cells that can reverse type I diabetes become oligoclonal long-term protective memory cells. J Immunol 181:1798-1805.
49. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A (1999) Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401:708-712. (Pubitemid 129515761)
50. Richards K, et al. (2007) Direct ex vivo analyses of HLA-DR1 transgenic mice reveal an exceptionally broad pattern of immunodominance in the primary HLA-DR1-restricted CD4 T-cell response to influenza virus hemagglutinin. J Virol 81:7608-7619. (Pubitemid 47047846)