Unique transcriptional profile of liver-resident memory CD8+ T cells induced by immunization with malaria sporozoites

Genes and Immunity

Volumn 14, Issue 5, 2013, Pages 302-309

  Tse, S W ^a   Cockburn, I A ^a   Zhang, H ^a   Scott, A L ^a   Zavala, F ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

CD8+ T cells; Liver stage; Malaria; Memory; Plasmodium; Sporozoites

Indexed keywords

MALARIA VACCINE; SPOROZOITE VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; IMMUNIZATION; LIVER; MEMORY T LYMPHOCYTE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN;

MUS;

EID: 84880923153     PISSN: 14664879     EISSN: 14765470     Source Type: Journal    
DOI: 10.1038/gene.2013.20     Document Type: Article

References (36)

1. Overstreet MG, Cockburn IA, Chen Y, Zavala F. Protective CD8+ T cells against Plasmodium liver stages: immunobiolog of an 'unnatural' immune response. Immunol Rev 2008; 225: 272-282.
2. Romero P, Maryanski JL, Corradin G, Nussenzweig RS, Nussenzweig V, Zavala F. Cloned cytotoxic T cells recognize an epitope in the circumsporozoite protein and protect against malaria. Nature 1989; 341: 323-326. (Pubitemid 20102099)
3. Chakravarty S, Cockburn IA, Kuk S, Overstreet MG, Sacci JB, Zavala F. CD8+ T lymphocytes protective against malaria liver stages are primed in skin-draining lymph nodes. Nat Med 2007; 13: 1035-1041. (Pubitemid 47517509)
4. Morrot A, Hafalla JCR, Cockburn IA, Carvalho LH, Zavala F. IL-4 receptor expression on CD8+ T cells is required for the development of protective memory responses against liver stages of malaria parasites. J Exp Med 2005; 202: 551-560. (Pubitemid 41186953)
5. Cockburn IA, Tse S-W, Radtke AJ, Srinivasan P, Chen Y-C, Sinnis P et al. Dendritic cells and hepatocytes use distinct pathways to process protective antigen from Plasmodium in vivo. PLoS Pathog 2011; 7: e1001318.
6. Woodland DL, Kohlmeier JE. Migration, maintenance and recall of memory T cells in peripheral tissues. Nat Rev Immunol 2009; 9: 153-161.
7. Masopust D, Vezys V, Wherry EJ, Barber DL, Ahmed R. Cutting edge: gut microenvironment promotes differentiation of a unique memory CD8 T cell population. J Immunol 2006; 176: 2079-2083. (Pubitemid 43201654)
8. Mackay LK, Stock AT, Ma JZ, Jones CM, Kent SJ, Mueller SN et al. Long-Lived epithelial immunity by tissue-resident memory T (TRM) Cells in the absence of persisting local antigen presentation. Proc Natl Acad Sci USA 2012; 109: 7037-7042.
9. Sano G, Hafalla JCR, Morrot A, Abe R, Lafaille JJ, Zavala F. Swift Development of protective effector functions in naive CD8+ T Cells against malaria liver stages. J Exp Med 2001; 194: 173-180.
10. Hokeness KL, Deweerd ES, Munks MW, Lewis CA, Gladue RP, Salazar-Mather TP. CXCR3-dependent recruitment of antigen-specific t lymphocytes to the liver during murine cytomegalovirus infection. J Virol 2007; 81: 1241-1250. (Pubitemid 46167845)
11. Sato T, Thorlacius H, Johnston B, Staton TL, Xiang W, Littman DR et al. Role for CXCR6 in Recruitment of activated CD8+ Lymphocytes to inflamed liver. J Immunol 2005; 174: 277-283. (Pubitemid 40007414)
12. Sarkar S, Kalia V, Haining WN, Konieczny BT, Subramaniam S, Ahmed R. Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J Exp Med 2008; 205: 625-640. (Pubitemid 351439309)
13. Cao Z, Sun X, Icli B, Wara AK, Feinberg MW. Role of Krüppel-like factors in leukocyte development, function, and disease. Blood 2010; 116: 4404-4414.
14. Pappu R, Schwab SR, Cornelissen I, Pereira JP, Regard JB, Xu Y et al. Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science 2007; 316: 295-298. (Pubitemid 46633109)
15. Pearce EL, Mullen AC, Martins GA, Krawczyk CM, Hutchins AS, Zediak VP et al. Control of effector CD8+ T cell function by the transcription factor eomesodermin. Science 2003; 302: 1041-1043. (Pubitemid 37386196)
16. Barbu EA, Zhang J, Berenstein EH, Groves JR, Parks LM, Siraganian RP. The Transcription factor Zeb2 Regulates signaling in mast cells. J Immunol 2012; 188: 6278-6286.
17. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102: 15545-15550. (Pubitemid 41528093)
18. Haining WN, Wherry EJ. Integrating genomic signatures for immunologic discovery. Immunity 2010; 32: 152-161.
19. Kaech SM, Hemby S, Kersh E, Ahmed R. Molecular and Functional profiling of memory CD8 T Cell differentiation. Cell 2002; 111: 837-851. (Pubitemid 36106405)
20. Cockburn IA, Chen Y-C, Overstreet MG, Lees JR, Van Rooijen N, Farber DL et al. Prolonged antigen presentation is required for optimal CD8+ T cell responses against malaria liver stage parasites. PLoS Pathog 2010; 6: e1000877.
21. Wirth TC, Xue H-H, Rai D, Sabel JT, Bair T, Harty JT et al. Repetitive Antigen stimulation induces stepwise transcriptome diversification but preserves a core signature of memory CD8+ T cell differentiation. Immunity 2010; 33: 128-140.
22. Wherry EJ, Ha S-J, Kaech SM, Haining WN, Sarkar S, Kalia V et al. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 2007; 27: 670-684. (Pubitemid 47615511)
23. Gu X, Laouar A, Wan J, Daheshia M, Lieberman J, Yokoyama WM et al. The gp49B1 inhibitory receptor regulates the IFN-γ responses of T cells and NK cells. J Immunol 2003; 170: 4095-4101. (Pubitemid 36428172)
24. Masopust D, Vezys V, Marzo AL, Lefrançois L. Preferential localization of effector memory cells in nonlymphoid tissue. Science 2001; 291: 2413-2417. (Pubitemid 32231804)
25. Joshi NS, Cui W, Chandele A, Lee HK, Urso DR, Hagman J et al. Inflammation Directs memory precursor and short-lived effector CD8(+) T Cell fates via the graded expression of T-bet transcription factor. Immunity 2007; 27: 281-295. (Pubitemid 47284924)
26. Berlin C, Berg EL, Briskin MJ, Andrew DP, Kilshaw PJ, Holzmann B et al. Alpha 4 beta 7 integrin mediates lymphocyte binding to the mucosal vascular addressin MAdCAM-1. Cell 1993; 74: 185-195. (Pubitemid 23219889)
27. Reiss Y, Proudfoot AE, Power CA, Campbell JJ, Butcher EC. CC chemokine receptor (CCR)4 and the CCR10 ligand cutaneous T cell-attracting chemokine (CTACK) in lymphocyte trafficking to inflamed skin. J Exp Med 2001; 194: 1541-1547. (Pubitemid 33081528)
28. Wakim LM, Woodward-Davis A, Bevan MJ, Memory T. Cells persisting within the brain after local infection show functional adaptations to their tissue of residence. Proc Natl Acad Sci USA 2010; 107: 17872-17879.
29. Gebhardt T, Wakim LM, Eidsmo L, Reading PC, Heath WR, Carbone FR. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat Immunol 2009; 10: 524-530.
30. Masopust D, Choo D, Vezys V, Wherry EJ, Duraiswamy J, Akondy R et al. Dynamic T cell migration program provides resident memory within intestinal epithelium. J Exp Med 2010; 207: 553-564.
31. Weinreich MA, Takada K, Skon C, Reiner SL, Jameson SC, Hogquist KA. KLF2 transcription-factor deficiency in T cells results in unrestrained cytokine production and upregulation of bystander chemokine receptors. Immunity 2009; 31: 122-130.
32. Parish IA, Kaech SM. Diversity in CD8(+) T cell differentiation. Curr Opin Immunol 2009; 21: 291-297.
33. Sebzda E, Zou Z, Lee JS, Wang T, Kahn ML. Transcription factor KLF2 regulates the migration of naive T cells by restricting chemokine receptor expression patterns. Nat Immunol 2008; 9: 292-300. (Pubitemid 351267326)
34. Crispe IN, Dao T, Klugewitz K, Mehal WZ, Metz DP. The liver as a site of T-cell apoptosis: graveyard, or killing field? Immunol Rev 2000; 174: 47-62. (Pubitemid 30201378)
35. Crispe IN. The Liver as a lymphoid organ. Annu Rev Immunol 2009; 27: 147-163.
36. Wakim LM, Woodward-Davis A, Liu R, Hu Y, Villadangos J, Smyth G et al. The molecular signature of tissue resident memory CD8 T cells isolated from the brain. J Immunol 2012; 189: 3462-3471.