Comparison of primary human cytotoxic T-cell and natural killer cell responses reveal similar molecular requirements for lytic granule exocytosis but differences in cytokine production

Blood

Volumn 121, Issue 8, 2013, Pages 1345-1356

  Chiang, Samuel C C ^a   Theorell, Jakob ^a   Entesarian, Miriam ^a,b   Meeths, Marie ^a,b   Mastafa, Monika ^a,b   Al Herz, Waleed ^c   Frisk, Per ^d   Gilmour, Kimberly C ^e   Ifversen, Marianne ^f   Langenskiöld, Cecilia ^g   Machaczka, Maciej ^b   Naqvi, Ahmed ^h,i   Payne, Jeanette ^j   Perez Martinez, Antonio ^k   Sabel, Magnus ^g   Unal, Ekrem ^l   Unal, Sule ^m   Winiarski, Jacek ^b   Nordenskjöld, Magnus ^b   Ljunggren, Hans Gustaf ^a   Henter, Jan Inge ^a   Bryceson, Yenan T ^a,n   more..

^a KAROLINSKA INSTITUTE   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c KUWAIT UNIVERSITY   (Kuwait)

^d UPPSALA UNIVERSITY   (Sweden)

^e GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^f Rigshospitalet   (Denmark)

^g QUEEN SILVIA CHILDREN'S HOSPITAL   (Sweden)

^h AGA KHAN UNIVERSITY   (Pakistan)

ⁱ HOSPITAL FOR SICK CHILDREN   (Canada)

^j SHEFFIELD CHILDREN S HOSPITAL   (United Kingdom)

^k HOSPITAL INFANTIL UNIVERSITARIO NIÑO JESÚS   (Spain)

^l ERCIYES UNIVERSITY   (Turkey)

^m HACETTEPE UNIVERSITY   (Turkey)

ⁿ UNIVERSITY OF BERGEN   (Norway)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD57 ANTIGEN; GRANZYME B; PERFORIN;

ALLELE; ARTICLE; CD3+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL GRANULE; CELL LINEAGE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DEGRANULATION; EXOCYTOSIS; HEMOPHAGOCYTIC SYNDROME; HUMAN; HUMAN CELL; NATURAL KILLER CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE SUBPOPULATION;

EID: 84874436476     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-07-442558     Document Type: Article

References (50)

1. Lieberman J. The ABCs of granule-mediated cy-totoxicity: new weapons in the arsenal. Nat Rev Immunol. 2003;3(5):361-370. (Pubitemid 37323196)
2. Voskoboinik I, Dunstone MA, Baran K, Whisstock JC, Trapani JA. Perforin: structure, function, and role in human immunopathology. Immunol Rev. 2010;235(1):35-54.
3. Davis MM, Krogsgaard M, Huse M, Huppa J, Lillemeier BF, Li QJ. T cells as a self-referential, sensory organ. Annu Rev Immunol. 2007;25:681-695. (Pubitemid 46697921)
4. Lanier LL. Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol. 2008;9(5):495-502. (Pubitemid 351560518)
5. Bryceson YT, Chiang SC, Darmanin S, Schlums H, Theorell JT, Wood SM. Molecular mechanisms of NK cell activation. J Innate Immun. 2011;3(3):216-226.
6. De Saint Basile G, Menasche G, Fischer A. Molecular mechanisms of biogenesis and exocytosis of cytotoxic granules. Nat Rev Immunol. 2010;10(8):568-579.
7. Wulfing C, Purtic B, Klem J, Schatzle JD. Step-wise cytoskeletal polarization as a series of checkpoints in innate but not adaptive cytolytic killing. Proc Natl Acad Sci U S A. 2003;100(13):7767-7772. (Pubitemid 36760044)
8. Deguine J, Breart B, Lemaitre F, Di Santo JP, Bousso P. Intravital imaging reveals distinct dynamics for natural killer and CD8 (+) T cells during tumor regression. Immunity. 2010;33(4):632-644.
9. Stepp SE, Dufourcq-Lagelouse R, Le Deist F, et al. Perforin gene defects in familial hemophagocytic lymphohistiocytosis. Science. 1999;286(5446):1957- 1959. (Pubitemid 129515904)
10. Janka GE. Hemophagocytic syndromes. Blood Rev. 2007;21(5):245-253. (Pubitemid 47212601)
11. Filipovich AH. Hemophagocytic lymphohistiocytosis and related disorders. Curr Opin Allergy Clin Immunol. 2006;6(6):410-415. (Pubitemid 44714152)
12. Gupta S, Weitzman S. Primary and secondary hemophagocytic lymphohistiocytosis: clinical features, pathogenesis and therapy. Expert Rev Clin Immunol. 2010;6(1):137-154.
13. Clementi R, Locatelli F, Dupre L, et al. A proportion of patients with lymphoma may harbor mutations of the perforin gene. Blood. 2005;105(11):4424- 4428. (Pubitemid 40720790)
14. Chia J, Yeo KP, Whisstock JC, Dunstone MA, Trapani JA, Voskoboinik I. Temperature sensitivity of human perforin mutants unmasks subtotal loss of cytotoxicity, delayed FHL, and a predisposition to cancer. Proc Natl Acad Sci U S A. 2009;106(24):9809-9814.
15. Feldmann J, Callebaut I, Raposo G, et al. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophago-cytic lymphohistiocytosis (FHL3). Cell. 2003;115(4):461-473. (Pubitemid 37456808)
16. Zur Stadt U, Schmidt S, Kasper B, et al. Linkage of familial hemophagocytic lymphohistiocytosis (FHL) type-4 to chromosome 6q24 and identification of mutations in syntaxin 11. Hum Mol Genet. 2005;14(6):827-834. (Pubitemid 40403278)
17. Zur Stadt U, Rohr J, Seifert W, et al. Familial he-mophagocytic lymphohistiocytosis type 5 (FHL-5) is caused by mutations in Munc18-2 and impaired binding to syntaxin 11. Am J Hum Genet. 2009;85(4):482-492.
18. Cote M, Menager MM, Burgess A, et al. Munc18-2 deficiency causes familial hemophagocytic lym-phohistiocytosis type 5 and impairs cytotoxic granule exocytosis in patient NK cells. J Clin Invest. 2009;119(12):3765-3773.
19. Bryceson YT, Rudd E, Zheng C, et al. Defective cytotoxic lymphocyte degranulation in syntaxin-11 deficient familial hemophagocytic lymphohistiocy-tosis 4 (FHL4) patients. Blood. 2007;110(6):1906-1915. (Pubitemid 47443904)
20. Henter JI, Horne A, Arico M, et al. HLH-2004: Diagnostic and therapeutic guidelines for hemophago-cytic lymphohistiocytosis. Pediatr Blood Cancer. 2007;48(2):124-131. (Pubitemid 44958267)
21. Marcenaro S, Gallo F, Martini S, et al. Analysis of natural killer-cell function in familial hemophago-cytic lymphohistiocytosis (FHL): defective CD107a surface expression heralds Munc13-4 defect and discriminates between genetic subtypes of the disease. Blood. 2006;108(7):2316-2323. (Pubitemid 44497515)
22. Bryceson YT, Pende D, Maul-Pavicic A, et al. A prospective evaluation of degranulation assays in the rapid diagnosis of familial hemophagocytic syndromes. Blood. 2012;119(12):2754-2763.
23. Caligiuri MA. Human natural killer cells. Blood. 2008;112(3):461-469.
24. Parish IA, Kaech SM. Diversity in CD8 (+) T cell differentiation. Curr Opin Immunol. 2009;21(3):291-297.
25. Zhang N, Bevan MJ. CD8 (+) T cells: foot soldiers of the immune system. Immunity. 2011;35(2):161-168.
26. Hamann D, Baars PA, Rep MH, et al. Phenotypic and functional separation of memory and effector human CD8+ T cells. J Exp Med. 1997;186(9):1407-1418. (Pubitemid 27479800)
27. Van Lier RA, Ten Berge IJ, Gamadia LE. Human CD8 (+) T-cell differentiation in response to viruses. Nat Rev Immunol. 2003;3(12):931-939.
28. Pittet MJ, Speiser DE, Valmori D, Cerottini JC, Romero P. Cutting edge: cytolytic effector function in human circulating CD8+ T cells closely correlates with CD56 surface expression. J Immunol. 2000;164(3):1148-1152. (Pubitemid 30067223)
29. Chattopadhyay PK, Betts MR, Price DA, et al. The cytolytic enzymes granyzme A, granzyme B, and perforin: expression patterns, cell distribution, and their relationship to cell maturity and bright CD57 expression. J Leukoc Biol. 2009;85(1):88-97.
30. Appay V, Van Lier RA, Sallusto F, Roederer M. Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A. 2008;73(11):975-983.
31. Roederer M, Nozzi JL, Nason MC. SPICE: exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A. 2011;79(2):167-174.
32. Meeths M, Chiang SC, Wood SM, et al. Familial hemophagocytic lymphohistiocytosis type 3 (FHL3) caused by deep intronic mutation and inversion in UNC13D. Blood. 2011;118(22):5783-5793.
33. Bagwell BC. Breaking the Dimensionality Barrier. In: Hawley TS, Hawley RG, eds. Flow Cytometry Protocols, Methods in Molecular Biology. Vol 699. Berlin, Germany: Springer; 2011:31-51.
34. Bjorkstrom NK, Riese P, Heuts F, et al. Expression patterns of NKG2A, KIR, and CD57 define a process of CD56dim NK-cell differentiation uncoupled from NK-cell education. Blood. 2010;116(19):3853-3864.
35. Van De Berg PJ, Van Leeuwen EM, Ten Berge IJ, Van Lier R. Cytotoxic human CD4 (+) T cells. Curr Opin Immunol. 2008;20(3):339-343.
36. Berthou C, Legros-Maida S, Soulie A, et al. Cord blood T lymphocytes lack constitutive perforin expression in contrast to adult peripheral blood T lymphocytes. Blood. 1995;85(6):1540-1546.
37. Fauriat C, Long EO, Ljunggren HG, Bryceson YT. Regulation of human NK cell cytokine and chemokine production by target cell recognition. Blood. 2010;115(6):2167-2176.
38. Davis MM. A prescription for human immunology. Immunity. 2008;29(6):835-838.
39. Biancotto A, Fuchs JC, Williams A, Dagur PK, McCoy JP Jr. High dimensional flow cytometry for comprehensive leukocyte immunophenotyping (CLIP) in translational research. J Immunol Methods. 2011;363(2):245-261.
40. Newell EW, Sigal N, Bendall SC, Nolan GP Davis MM. Cytometry by time-of-flight shows combinatorial cytokine expression and virus-specific cell niches within a continuum of CD8+ Tcell phenotypes. Immunity. 2012;36(1):142-152.
41. Abo T, Balch CM. A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1). J Immunol. 1981;127(3):1024-1029. (Pubitemid 11051150)
42. Focosi D, Bestagno M, Burrone O, Petrini M. CD57+ T lymphocytes and functional immune deficiency. J Leukoc Biol. 2010;87(1):107-116.
43. Makedonas G, Banerjee PP, Pandey R, et al. Rapid up-regulation and granule-independent transport of perforin to the immunological synapse define a novel mechanism of antigen-specific CD8+ T cell cytotoxic activity. J Immunol. 2009;182(9):5560-5569.
44. Bratke K, Kuepper M, Bade B, Virchow JC Jr, Luttmann W. Differential expression of human granzymes A, B, and K in natural killer cells and during CD8+ T cell differentiation in peripheral blood. Eur J Immunol. 2005;35(9):2608-2616. (Pubitemid 41404044)
45. Takata H, Takiguchi M. Three memory subsets of human CD8+ T cells differently expressing three cytolytic effector molecules. J Immunol. 2006;177(7):4330-4340. (Pubitemid 44469761)
46. Anthony DA, Andrews DM, Watt SV, Trapani JA, Smyth MJ. Functional dissection of the granzyme family: cell death and inflammation. Immunol Rev. 2010;235(1):73-92.
47. Froelich CJ, Pardo J, Simon MM. Granule-associated serine proteases: granzymes might not just be killer proteases. Trends Immunol. 2009;30(3):117-123.
48. Rudd E, Bryceson YT, Zheng C, et al. Spectrum, and clinical and functional implications of UNC13D mutations in familial hemophagocytic lymphohistiocytosis. J Med Genet. 2008;45(3):134-141. (Pubitemid 351373741)
49. Macartney CA, Weitzman S, Wood SM, et al. Unusual functional manifestations of a novel STX11 frameshift mutation in two infants with familial hemophagocytic lymphohistiocytosis type 4 (FHL4). Pediatr Blood Cancer. 2011;56(4):654-657.
50. Enders A, Zieger B, Schwarz K, et al. Lethal hemophagocytic lymphohistiocytosis in Hermansky-Pudlak syndrome type II. Blood. 2006;108(1):81-87. (Pubitemid 43990615)