Chronic Parasitic Infection Maintains High Frequencies of Short-Lived Ly6CCD4 Effector T Cells That Are Required for Protection against Re-infection
Naturally acquired resistance to reinfection by numerous infectious pathogens including Leishmania, Plasmodium, Mycobacterium, and parasitic worms, typically coincides with an ongoing primary infection. This natural resistance to reinfection, termed concomitant immunity, is often referred to as a memory response and provides the rationale for the vaccine effort against these infectious pathogens. However, immune memory is mediated by populations of long-lived cells that do not require an ongoing primary infection to mediate protection. The requirement for chronic infection to maintain concomitant immunity suggests that the critical cells that mediate this immunity are not memory cells. In the present study we define short-lived effector T cells that pre-exist secondary challenge, not memory cells, as the critical cells that mediate concomitant immunity. These observations provide direct evidence on a cellular level that conventional vaccination strategies against chronic infectious diseases, whose development is predicated upon the belief that concomitant immunity can be mediated by long-lived memory cells, are unlikely to succeed.
Vyšlo v časopise:
Chronic Parasitic Infection Maintains High Frequencies of Short-Lived Ly6CCD4 Effector T Cells That Are Required for Protection against Re-infection. PLoS Pathog 10(12): e32767. doi:10.1371/journal.ppat.1004538
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004538
Souhrn
Naturally acquired resistance to reinfection by numerous infectious pathogens including Leishmania, Plasmodium, Mycobacterium, and parasitic worms, typically coincides with an ongoing primary infection. This natural resistance to reinfection, termed concomitant immunity, is often referred to as a memory response and provides the rationale for the vaccine effort against these infectious pathogens. However, immune memory is mediated by populations of long-lived cells that do not require an ongoing primary infection to mediate protection. The requirement for chronic infection to maintain concomitant immunity suggests that the critical cells that mediate this immunity are not memory cells. In the present study we define short-lived effector T cells that pre-exist secondary challenge, not memory cells, as the critical cells that mediate concomitant immunity. These observations provide direct evidence on a cellular level that conventional vaccination strategies against chronic infectious diseases, whose development is predicated upon the belief that concomitant immunity can be mediated by long-lived memory cells, are unlikely to succeed.
Zdroje
1. KaechSM, CuiW (2012) Transcriptional control of effector and memory CD8+ T cell differentiation. Nat Rev Immunol 12: 749–761.
2. CondottaSA, RicherMJ, BadovinacVP, HartyJT (2012) Probing CD8 T cell responses with Listeria monocytogenes infection. Adv Immunol 113: 51–80.
3. SmithersSR, TerryRJ (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. GrenfellBT, MichaelE, DenhamDA (1991) A model for the dynamics of human lymphatic filariasis. Parasitol Today 7: 318–323.
5. MacDonaldAJ, TuragaPS, Harmon-BrownC, TierneyTJ, BennettKE, 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. ScottP, ArtisD, UzonnaJ, ZaphC (2004) The development of effector and memory T cells in cutaneous leishmaniasis: the implications for vaccine development. Immunol Rev 201: 318–338.
7. SpencePJ, LanghorneJ (2012) T cell control of malaria pathogenesis. Curr Opin Immunol 24: 444–448.
8. UrdahlKB, ShafianiS, ErnstJD (2011) Initiation and regulation of T-cell responses in tuberculosis. Mucosal Immunol 4: 288–293.
9. NelsonRW, McLachlanJB, KurtzJR, JenkinsMK (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 RosarioAP, MuxelSM, Rodriguez-MalagaSM, SardinhaLR, ZagoCA, 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. PetersNC, KimblinN, SecundinoN, KamhawiS, LawyerP, et al. (2009) Vector transmission of leishmania abrogates vaccine-induced protective immunity. PLoS Pathog 5: e1000484.
12. ZaphC, UzonnaJ, BeverleySM, ScottP (2004) Central memory T cells mediate long-term immunity to Leishmania major in the absence of persistent parasites. Nat Med 10: 1104–1110.
13. UzonnaJE, WeiG, YurkowskiD, BretscherP (2001) Immune elimination of Leishmania major in mice: implications for immune memory, vaccination, and reactivation disease. J Immunol 167: 6967–6974.
14. BelkaidY, HoffmannKF, MendezS, KamhawiS, UdeyMC, 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. BelkaidY, PiccirilloCA, MendezS, ShevachEM, SacksDL (2002) CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 420: 502–507.
16. NorthRJ, KirsteinDP (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. StephensR, LanghorneJ (2010) Effector memory Th1 CD4 T cells are maintained in a mouse model of chronic malaria. PLoS Pathog 6: e1001208.
18. PetersNC, BertholetS, LawyerPG, CharmoyM, RomanoA, 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. MelbyPC (1991) Experimental leishmaniasis in humans: review. Rev Infect Dis 13: 1009–1017.
20. NoazinS, KhamesipourA, MoultonLH, TannerM, NasseriK, et al. (2009) Efficacy of killed whole-parasite vaccines in the prevention of leishmaniasis: a meta-analysis. Vaccine 27: 4747–4753.
21. MullerI (1992) Role of T cell subsets during the recall of immunologic memory to Leishmania major. Eur J Immunol 22: 3063–3069.
22. GebhardtT, WhitneyPG, ZaidA, MackayLK, BrooksAG, et al. (2011) Different patterns of peripheral migration by memory CD4+ and CD8+ T cells. Nature 477: 216–219.
23. ReinhardtRL, BullardDC, WeaverCT, JenkinsMK (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. PitcherCJ, HagenSI, WalkerJM, LumR, MitchellBL, et al. (2002) Development and homeostasis of T cell memory in rhesus macaque. J Immunol 168: 29–43.
25. ColpittsSL, DaltonNM, ScottP (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. MarshallHD, ChandeleA, JungYW, MengH, PoholekAC, 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-SantosO, PescherP, BreartB, LippunerC, AebischerT, 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. LiuD, UzonnaJE (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. KapinaMA, ShepelkovaGS, MischenkoVV, SaylesP, BogachevaP, 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. PepperM, LinehanJL, PaganAJ, ZellT, DileepanT, 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. PaganAJ, PetersNC, DebrabantA, Ribeiro-GomesF, PepperM, 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. MatsudaJL, ZhangQ, NdonyeR, RichardsonSK, HowellAR, et al. (2006) T-bet concomitantly controls migration, survival, and effector functions during the development of Valpha14i NKT cells. Blood 107: 2797–2805.
34. LinE, KemballCC, HadleyA, WilsonJJ, HofstetterAR, 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. ReileyWW, ShafianiS, WittmerST, Tucker-HeardG, MoonJJ, 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. WherryEJ (2011) T cell exhaustion. Nat Immunol 12: 492–499.
37. RogersME (2012) The role of leishmania proteophosphoglycans in sand fly transmission and infection of the Mammalian host. Front Microbiol 3: 223.
38. PetersNC, EgenJG, SecundinoN, DebrabantA, KimblinN, et al. (2008) In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321: 970–974.
39. Ribeiro-GomesFL, PetersNC, DebrabantA, SacksDL (2012) Efficient capture of infected neutrophils by dendritic cells in the skin inhibits the early anti-leishmania response. PLoS Pathog 8: e1002536.
40. ZinkernagelRM (2012) Immunological memory not equal protective immunity. Cell Mol Life Sci 69: 1635–1640.
41. StamperLW, PatrickRL, FayMP, LawyerPG, ElnaiemDE, et al. (2011) Infection parameters in the sand fly vector that predict transmission of Leishmania major. PLoS Negl Trop Dis 5: e1288.
42. SacksDL, HienyS, SherA (1985) Identification of cell surface carbohydrate and antigenic changes between noninfective and infective developmental stages of Leishmania major promastigotes. J Immunol 135: 564–569.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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