Chronic Parasitic Infection Maintains High Frequencies of Short-Lived Ly6C+CD4+ Effector T Cells That Are Required for Protection against Re-infection

PLoS Pathogens

Volumn 10, Issue 12, 2014, Pages

  Peters, Nathan C ^a,c   Pagán, Antonio J ^b,d   Lawyer, Phillip G ^a   Hand, Timothy W ^a   Henrique Roma, Eric ^a   Stamper, Lisa W ^a   Romano, Audrey ^a   Sacks, David L ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CALGARY   (Canada)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; TUMOR NECROSIS FACTOR ALPHA;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFECTOR CELL; FEMALE; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNE RESPONSE; IMMUNOLOGICAL MEMORY; KINETICS; LEISHMANIASIS; MOUSE; NONHUMAN; PARASITOSIS; PHENOTYPE; PROMASTIGOTE; PROTEIN EXPRESSION; REINFECTION; VACCINATION;

LEISHMANIA MAJOR; MUS;

EID: 84919681164     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004538     Document Type: Article

References (42)

1. Kaech SM, Cui W, (2012) Transcriptional control of effector and memory CD8+ T cell differentiation. Nat Rev Immunol 12: 749–761.
2. Condotta SA, Richer MJ, Badovinac VP, Harty JT, (2012) Probing CD8 T cell responses with Listeria monocytogenes infection. Adv Immunol 113: 51–80.
3. Smithers SR, Terry RJ, (1967) Resistance to experimental infection with Schistosoma mansoni in rhesus monkeys induced by the transfer of adult worms. Trans R Soc Trop Med Hyg 61: 517–533.
4. Grenfell BT, Michael E, Denham DA, (1991) A model for the dynamics of human lymphatic filariasis. Parasitol Today 7: 318–323.
5. MacDonald AJ, Turaga PS, Harmon-Brown C, Tierney TJ, Bennett KE, et al. (2002) Differential cytokine and antibody responses to adult and larval stages of Onchocerca volvulus consistent with the development of concomitant immunity. Infect Immun 70: 2796–2804.
6. Scott P, Artis D, Uzonna J, Zaph C, (2004) The development of effector and memory T cells in cutaneous leishmaniasis: the implications for vaccine development. Immunol Rev 201: 318–338.
7. Spence PJ, Langhorne J, (2012) T cell control of malaria pathogenesis. Curr Opin Immunol 24: 444–448.
8. Urdahl KB, Shafiani S, Ernst JD, (2011) Initiation and regulation of T-cell responses in tuberculosis. Mucosal Immunol 4: 288–293.
9. Nelson RW, McLachlan JB, Kurtz JR, Jenkins MK, (2013) CD4+ T Cell Persistence and Function after Infection Are Maintained by Low-Level Peptide:MHC Class II Presentation. J Immunol 190: 2828–2834.
10. Freitas do Rosario AP, Muxel SM, Rodriguez-Malaga SM, Sardinha LR, Zago CA, et al. (2008) Gradual decline in malaria-specific memory T cell responses leads to failure to maintain long-term protective immunity to Plasmodium chabaudi AS despite persistence of B cell memory and circulating antibody. J Immunol 181: 8344–8355.
11. Peters NC, Kimblin N, Secundino N, Kamhawi S, Lawyer P, et al. (2009) Vector transmission of leishmania abrogates vaccine-induced protective immunity. PLoS Pathog 5: e1000484.
12. Zaph C, Uzonna J, Beverley SM, Scott P, (2004) Central memory T cells mediate long-term immunity to Leishmania major in the absence of persistent parasites. Nat Med 10: 1104–1110.
13. Uzonna JE, Wei G, Yurkowski D, Bretscher P, (2001) Immune elimination of Leishmania major in mice: implications for immune memory, vaccination, and reactivation disease. J Immunol 167: 6967–6974.
14. Belkaid Y, Hoffmann KF, Mendez S, Kamhawi S, Udey MC, et al. (2001) The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure. J Exp Med 194: 1497–1506.
15. Belkaid Y, Piccirillo CA, Mendez S, Shevach EM, Sacks DL, (2002) CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 420: 502–507.
16. North RJ, Kirstein DP, (1977) T-cell-mediated concomitant immunity to syngeneic tumors. I. Activated macrophages as the expressors of nonspecific immunity to unrelated tumors and bacterial parasites. J Exp Med 145: 275–292.
17. Stephens R, Langhorne J, (2010) Effector memory Th1 CD4 T cells are maintained in a mouse model of chronic malaria. PLoS Pathog 6: e1001208.
18. Peters NC, Bertholet S, Lawyer PG, Charmoy M, Romano A, et al. (2012) Evaluation of recombinant Leishmania polyprotein plus glucopyranosyl lipid A stable emulsion vaccines against sand fly-transmitted Leishmania major in C57BL/6 mice. J Immunol 189: 4832–4841.
19. Melby PC, (1991) Experimental leishmaniasis in humans: review. Rev Infect Dis 13: 1009–1017.
20. Noazin S, Khamesipour A, Moulton LH, Tanner M, Nasseri K, et al. (2009) Efficacy of killed whole-parasite vaccines in the prevention of leishmaniasis: a meta-analysis. Vaccine 27: 4747–4753.
21. Muller I, (1992) Role of T cell subsets during the recall of immunologic memory to Leishmania major. Eur J Immunol 22: 3063–3069.
22. Gebhardt T, Whitney PG, Zaid A, Mackay LK, Brooks AG, et al. (2011) Different patterns of peripheral migration by memory CD4+ and CD8+ T cells. Nature 477: 216–219.
23. Reinhardt RL, Bullard DC, Weaver CT, Jenkins MK, (2003) Preferential accumulation of antigen-specific effector CD4 T cells at an antigen injection site involves CD62E-dependent migration but not local proliferation. J Exp Med 197: 751–762.
24. Pitcher CJ, Hagen SI, Walker JM, Lum R, Mitchell BL, et al. (2002) Development and homeostasis of T cell memory in rhesus macaque. J Immunol 168: 29–43.
25. Colpitts SL, Dalton NM, Scott P, (2009) IL-7 receptor expression provides the potential for long-term survival of both CD62Lhigh central memory T cells and Th1 effector cells during Leishmania major infection. J Immunol 182: 5702–5711.
26. Marshall HD, Chandele A, Jung YW, Meng H, Poholek AC, et al. (2011) Differential expression of Ly6C and T-bet distinguish effector and memory Th1 CD4(+) cell properties during viral infection. Immunity 35: 633–646.
27. Filipe-Santos O, Pescher P, Breart B, Lippuner C, Aebischer T, et al. (2009) A dynamic map of antigen recognition by CD4 T cells at the site of Leishmania major infection. Cell Host Microbe 6: 23–33.
28. Liu D, Uzonna JE, (2010) The p110 delta isoform of phosphatidylinositol 3-kinase controls the quality of secondary anti-Leishmania immunity by regulating expansion and effector function of memory T cell subsets. J Immunol 184: 3098–3105.
29. Kapina MA, Shepelkova GS, Mischenko VV, Sayles P, Bogacheva P, et al. (2007) CD27low CD4 T lymphocytes that accumulate in the mouse lungs during mycobacterial infection differentiate from CD27high precursors in situ, produce IFN-gamma, and protect the host against tuberculosis infection. J Immunol 178: 976–985.
30. Pepper M, Linehan JL, Pagan AJ, Zell T, Dileepan T, et al. (2010) Different routes of bacterial infection induce long-lived TH1 memory cells and short-lived TH17 cells. Nat Immunol 11: 83–89.
31. Pagan AJ, Peters NC, Debrabant A, Ribeiro-Gomes F, Pepper M, et al. (2012) Tracking antigen-specific CD4(+) T cells throughout the course of chronic Leishmania major infection in resistant mice. Eur J Immunol 43: 427–428.
32. Janeway CAJ, Travers P., Walport M., Murphy K. (2001) Immunobiology:The Immune System in Health and Disease: New York: Garland Science.
33. Matsuda JL, Zhang Q, Ndonye R, Richardson SK, Howell AR, et al. (2006) T-bet concomitantly controls migration, survival, and effector functions during the development of Valpha14i NKT cells. Blood 107: 2797–2805.
34. Lin E, Kemball CC, Hadley A, Wilson JJ, Hofstetter AR, et al. (2010) Heterogeneity among viral antigen-specific CD4+ T cells and their de novo recruitment during persistent polyomavirus infection. J Immunol 185: 1692–1700.
35. Reiley WW, Shafiani S, Wittmer ST, Tucker-Heard G, Moon JJ, et al. (2010) Distinct functions of antigen-specific CD4 T cells during murine Mycobacterium tuberculosis infection. Proc Natl Acad Sci U S A 107: 19408–19413.
36. Wherry EJ, (2011) T cell exhaustion. Nat Immunol 12: 492–499.
37. Rogers ME, (2012) The role of leishmania proteophosphoglycans in sand fly transmission and infection of the Mammalian host. Front Microbiol 3: 223.
38. Peters NC, Egen JG, Secundino N, Debrabant A, Kimblin N, et al. (2008) In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321: 970–974.
39. Ribeiro-Gomes FL, Peters NC, Debrabant A, Sacks DL, (2012) Efficient capture of infected neutrophils by dendritic cells in the skin inhibits the early anti-leishmania response. PLoS Pathog 8: e1002536.
40. Zinkernagel RM, (2012) Immunological memory not equal protective immunity. Cell Mol Life Sci 69: 1635–1640.
41. Stamper LW, Patrick RL, Fay MP, Lawyer PG, Elnaiem DE, et al. (2011) Infection parameters in the sand fly vector that predict transmission of Leishmania major. PLoS Negl Trop Dis 5: e1288.
42. Sacks DL, Hieny S, Sher A, (1985) Identification of cell surface carbohydrate and antigenic changes between noninfective and infective developmental stages of Leishmania major promastigotes. J Immunol 135: 564–569.