Adaptive NK cells can persist in patients with GATA2 mutation depleted of stem and progenitor cells

Blood

Volumn 129, Issue 14, 2017, Pages 1927-1939

  Schlums, Heinrich ^a   Jung, Moonjung ^b   Han, Hongya ^a   Theorell, Jakob ^a   Bigley, Venetia ^c   Chiang, Samuel C C ^a   Allan, David S J ^b   Davidson Moncada, Jan K ^b   Dickinson, Rachel E ^c   Holmes, Tim D ^a,d   Hsu, Amy P ^e   Townsley, Danielle ^b   Winkler, Thomas ^b   Wang, Weixin ^f   Aukrust, Pål ^g   Nordøy, Ingvild ^g   Calvo, Katherine R ^f   Holland, Steve M ^e   Collin, Matthew ^c   Dunbar, Cynthia E ^b   Bryceson, Yenan T ^a,d   more..

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF BERGEN   (Norway)

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

^f NATIONAL INSTITUTES OF HEALTH   (United States)

^g OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD56 ANTIGEN; FC EPSILON RECEPTOR GAMMA; FC RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 18; PROMYELOCYTIC LEUKEMIA ZINC FINGER; PROTEIN KINASE SYK; RNA BINDING PROTEIN EWS; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FLI 1; TRANSCRIPTION FACTOR GATA 2; UNCLASSIFIED DRUG; CALMODULIN BINDING PROTEIN; EWSR1 PROTEIN, HUMAN; FCEPSILONRI GAMMA-CHAIN, HUMAN; GATA2 PROTEIN, HUMAN; IMMUNOGLOBULIN E RECEPTOR; RNA BINDING PROTEIN; SH2D1B PROTEIN, HUMAN; SYK PROTEIN, HUMAN;

ADOLESCENT; ADULT; ARTICLE; ASYMPTOMATIC DISEASE; CELL GRANULE; CELL PROLIFERATION; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE MUTATION; HAPLOINSUFFICIENCY; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOCYTE DIFFERENTIATION; MIDDLE AGED; NATURAL KILLER CELL; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; STEM CELL; STEM CELL SELF-RENEWAL; YOUNG ADULT; FEMALE; GENETICS; IMMUNOLOGY; MALE; MUTATION;

ADOLESCENT; ADULT; CALMODULIN-BINDING PROTEINS; CELL PROLIFERATION; CHILD; FEMALE; GATA2 TRANSCRIPTION FACTOR; HEMATOPOIETIC STEM CELLS; HUMANS; INTERLEUKIN-12; INTERLEUKIN-18; KILLER CELLS, NATURAL; MALE; MIDDLE AGED; MUTATION; RECEPTORS, IGE; RNA-BINDING PROTEINS; SYK KINASE; TRANSCRIPTION FACTORS;

EID: 85018925030     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-08-734236     Document Type: Article

References (66)

1. Dickinson RE, Milne P, Jardine L, et al. The evolution of cellular deficiency in GATA2 mutation. Blood. 2014;123(6):863-874.
2. Spinner MA, Sanchez LA, Hsu AP, et al. GATA2 deficiency: a protean disorder of hematopoiesis, lymphatics, and immunity. Blood. 2014;123(6): 809-821.
3. Hsu AP, Sampaio EP, Khan J, et al. Mutations in GATA2 are associated with the autosomal dominant and sporadic monocytopenia and mycobacterial infection (MonoMAC) syndrome. Blood. 2011;118(10):2653-2655.
4. Dickinson RE, Griffin H, Bigley V, et al. Exome sequencing identifies GATA-2 mutation as the cause of dendritic cell, monocyte, B and NK lymphoid deficiency. Blood. 2011;118(10): 2656-2658.
5. Hahn CN, Chong CE, Carmichael CL, et al. Heritable GATA2 mutations associated with familial myelodysplastic syndrome and acute myeloid leukemia. Nat Genet. 2011;43(10): 1012-1017.
6. Ostergaard P, Simpson MA, Connell FC, et al. Mutations in GATA2 cause primary lymphedema associated with a predisposition to acute myeloid leukemia (Emberger syndrome). Nat Genet. 2011; 43(10):929-931.
7. Pasquet M, Bellanné-Chantelot C, Tavitian S, et al. High frequency of GATA2 mutations in patients with mild chronic neutropenia evolving to MonoMac syndrome, myelodysplasia, and acute myeloid leukemia. Blood. 2013;121(5):822-829.
8. Ganapathi KA, Townsley DM, Hsu AP, et al. GATA2 deficiency-associated bone marrow disorder differs from idiopathic aplastic anemia. Blood. 2015;125(1):56-70.
9. Wlodarski MW, Hirabayashi S, Pastor V, et al; EWOG-MDS. Prevalence, clinical characteristics, and prognosis of GATA2-related myelodysplastic syndromes in children and adolescents. Blood. 2016;127(11):1387-1397.
10. Tsai FY, Keller G, Kuo FC, et al. An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature. 1994; 371(6494):221-226.
11. Tsai FY, Orkin SH. Transcription factor GATA-2 is required for proliferation/survival of early hematopoietic cells and mast cell formation, but not for erythroid and myeloid terminal differentiation. Blood. 1997;89(10):3636-3643.
12. Hsu AP, Johnson KD, Falcone EL, et al. GATA2 haploinsufficiency caused by mutations in a conserved intronic element leads to MonoMAC syndrome. Blood. 2013;121(19):3830-3837.
13. Vinh DC, Patel SY, Uzel G, et al. Autosomal dominant and sporadic monocytopenia with susceptibility to mycobacteria, fungi, papillomaviruses, and myelodysplasia. Blood. 2010;115(8):1519-1529.
14. Bigley V, Haniffa M, Doulatov S, et al. The human syndrome of dendritic cell, monocyte, B and NK lymphoid deficiency. J Exp Med. 2011;208(2): 227-234.
15. Biron CA, Byron KS, Sullivan JL. Severe herpesvirus infections in an adolescent without natural killer cells. N Engl J Med. 1989;320(26): 1731-1735.
16. Mace EM, Hsu AP, Monaco-Shawver L, et al. Mutations in GATA2 cause human NK cell deficiency with specific loss of the CD56(bright) subset. Blood. 2013;121(14):2669-2677.
17. Vivier E, Raulet DH, Moretta A, et al. Innate or adaptive immunity? The example of natural killer cells. Science. 2011;331(6013):44-49.
18. Caligiuri MA. Human natural killer cells. Blood. 2008;112(3):461-469.
19. Fauriat C, Long EO, Ljunggren HG, Bryceson YT. Regulation of human NK-cell cytokine and chemokine production by target cell recognition. Blood. 2010;115(11):2167-2176.
20. Gineau L, Cognet C, Kara N, et al. Partial MCM4 deficiency in patients with growth retardation, adrenal insufficiency, and natural killer cell deficiency. J Clin Invest. 2012;122(3):821-832.
21. Wu C, Li B, Lu R, et al. Clonal tracking of rhesus macaque hematopoiesis highlights a distinct lineage origin for natural killer cells. Cell Stem Cell. 2014;14(4):486-499.
22. Cichocki F, Sitnicka E, Bryceson YT. NK cell development and function–plasticity and redundancy unleashed. Semin Immunol. 2014; 26(2):114-126.
23. Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature. 2009; 457(7229):557-561.
24. Schlums H, Cichocki F, Tesi B, et al. Cytomegalovirus infection drives adaptive epigenetic diversification of NK cells with altered signaling and effector function. Immunity. 2015; 42(3):443-456.
25. Lee J, Zhang T, Hwang I, et al. Epigenetic modification and antibody-dependent expansion of memory-like NK cells in human cytomegalovirus-infected individuals. Immunity. 2015;42(3):431-442.
26. Cichocki F, Schlums H, Theorell J, et al. Diversification and functional specialization of human NK cell subsets. Curr Top Microbiol Immunol. 2016;395:63-94.
27. Kuijpers TW, Baars PA, Dantin C, van den Burg M, van Lier RA, Roosnek E. Human NK cells can control CMV infection in the absence of T cells. Blood. 2008;112(3):914-915.
28. Tesi B, Schlums H, Cichocki F, Bryceson YT. Epigenetic regulation of adaptive NK cell diversification. Trends Immunol. 2016;37(7): 451-461.
29. Chiang SC, Theorell J, Entesarian M, et al. 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. 2013;121(8):1345-1356.
30. Maciejewski-Duval A, Meuris F, Bignon A, et al. Altered chemotactic response to CXCL12 in patients carrying GATA2 mutations. J Leukoc Biol. 2016;99(6):1065-1076.
31. Lopez-Vergès S, Milush JM, Schwartz BS, et al. Expansion of a unique CD571NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. Proc Natl Acad Sci USA. 2011;108(36):14725-14732.
32. Hu PF, Hultin LE, Hultin P, et al. Natural killer cell immunodeficiency in HIV disease is manifest by profoundly decreased numbers of CD161CD561 cells and expansion of a population of CD16dimCD56- cells with low lytic activity. J Acquir Immune Defic Syndr Hum Retrovirol. 1995;10(3):331-340.
33. Mavilio D, Lombardo G, Benjamin J, et al. Characterization of CD56-/CD161 natural killer (NK) cells: a highly dysfunctional NK subset expanded in HIV-infected viremic individuals. Proc Natl Acad Sci USA. 2005;102(8):2886-2891.
34. Intlekofer AM, Takemoto N, Wherry EJ, et al. Effector and memory CD81 T cell fate coupled by T-bet and eomesodermin. Nat Immunol. 2005; 6(12):1236-1244.
35. Bresnick EH, Katsumura KR, Lee HY, Johnson KD, Perkins AS. Master regulatory GATA transcription factors: mechanistic principles and emerging links to hematologic malignancies. Nucleic Acids Res. 2012;40(13):5819-5831.
36. Tsuzuki S, Enver T. Interactions of GATA-2 with the promyelocytic leukemia zinc finger (PLZF) protein, its homologue FAZF, and the t(11;17)generated PLZF-retinoic acid receptor alpha oncoprotein. Blood. 2002;99(9):3404-3410.
37. Cichocki F, Miller JS, Anderson SK, Bryceson YT. Epigenetic regulation of NK cell differentiation and effector functions. Front Immunol. 2013;4:55.
38. Freud AG, Yokohama A, Becknell B, et al. Evidence for discrete stages of human natural killer cell differentiation in vivo. J Exp Med. 2006; 203(4):1033-1043.
39. Renoux VM, Zriwil A, Peitzsch C, et al. Identification of a human natural killer cell lineage-restricted progenitor in fetal and adult tissues. Immunity. 2015;43(2):394-407.
40. Berg M, Lundqvist A, McCoy P Jr, et al. Clinical-grade ex vivo-expanded human natural killer cells up-regulate activating receptors and death receptor ligands and have enhanced cytolytic activity against tumor cells. Cytotherapy. 2009; 11(3):341-355.
41. Davidson-Moncada JK, Wand TH, Reger RN, Wu C, Dunbar CE, Childs RW. Identification and ex vivo expansion of a circulating NK cell progenitor population that leads to sustained production of CD561 NK cells [abstract]. Blood. 2015;126(23). Abstract 850.
42. Yu YL, Chiang YJ, Yen JJ. GATA factors are essential for transcription of the survival gene E4bp4 and the viability response of interleukin-3 in Ba/F3 hematopoietic cells. J Biol Chem. 2002; 277(30):27144-27153.
43. Ikushima S, Inukai T, Inaba T, Nimer SD, Cleveland JL, Look AT. Pivotal role for the NFIL3/ E4BP4 transcription factor in interleukin 3-mediated survival of pro-B lymphocytes. Proc Natl Acad Sci USA. 1997;94(6):2609-2614.
44. Kuribara R, Kinoshita T, Miyajima A, et al. Two distinct interleukin-3-mediated signal pathways, Ras-NFIL3 (E4BP4) and Bcl-xL, regulate the survival of murine pro-B lymphocytes. Mol Cell Biol. 1999;19(4):2754-2762.
45. Gascoyne DM, Long E, Veiga-Fernandes H, et al. The basic leucine zipper transcription factor E4BP4 is essential for natural killer cell development. Nat Immunol. 2009;10(10): 1118-1124.
46. Kamizono S, Duncan GS, Seidel MG, et al. Nfil3/E4bp4 is required for the development and maturation of NK cells in vivo. J Exp Med. 2009; 206(13):2977-2986.
47. Seillet C, Rankin LC, Groom JR, et al. Nfil3 is required for the development of all innate lymphoid cell subsets. J Exp Med. 2014;211(9): 1733-1740.
48. Geiger TL, Abt MC, Gasteiger G, et al. Nfil3 is crucial for development of innate lymphoid cells and host protection against intestinal pathogens. J Exp Med. 2014;211(9):1723-1731.
49. Kashiwada M, Pham NL, Pewe LL, Harty JT, Rothman PB. NFIL3/E4BP4 is a key transcription factor for CD8a1 dendritic cell development. Blood. 2011;117(23):6193-6197.
50. Firth MA, Madera S, Beaulieu AM, et al. Nfil3-independent lineage maintenance and antiviral response of natural killer cells. J Exp Med. 2013; 210(13):2981-2990.
51. Cortez VS, Fuchs A, Cella M, Gilfillan S, Colonna M. Cutting edge: salivary gland NK cells develop independently of Nfil3 in steady-state. J Immunol. 2014;192(10):4487-4491.
52. Crotta S, Gkioka A, Male V, et al. The transcription factor E4BP4 is not required for extramedullary pathways of NK cell development. J Immunol. 2014;192(6):2677-2688.
53. Seillet C, Huntington ND, Gangatirkar P, et al. Differential requirement for Nfil3 during NK cell development. J Immunol. 2014;192(6): 2667-2676.
54. Cichocki F, Cooley S, Davis Z, et al. CD56dimCD571NKG2C1 NK cell expansion is associated with reduced leukemia relapse after reduced intensity HCT. Leukemia. 2016;30(2): 456-463.
55. Zhang Y, Wallace DL, de Lara CM, et al. In vivo kinetics of human natural killer cells: the effects of ageing and acute and chronic viral infection. Immunology. 2007;121(2):258-265.
56. Zhang T, Scott JM, Hwang I, Kim S. Cutting edge: antibody-dependent memory-like NK cells distinguished by FcRg deficiency. J Immunol. 2013;190(4):1402-1406.
57. Gérart S, Sibéril S, Martin E, et al. Human iNKT and MAIT cells exhibit a PLZF-dependent proapoptotic propensity that is counterbalanced by XIAP. Blood. 2013;121(4):614-623.
58. Qi Q, Huang W, Bai Y, Balmus G, Weiss RS, August A. A unique role for ITK in survival of invariant NKT cells associated with the p53-dependent pathway in mice. J Immunol. 2012; 188(8):3611-3619.
59. Jameson SC. T cell homeostasis: keeping useful T cells alive and live T cells useful. Semin Immunol. 2005;17(3):231-237.
60. Surh CD, Sprent J. Regulation of mature T cell homeostasis. Semin Immunol. 2005;17(3): 183-191.
61. Poole E, Sinclair J. Sleepless latency of human cytomegalovirus. Med Microbiol Immunol (Berl). 2015;204(3):421-429.
62. Takizawa H, Boettcher S, Manz MG. Demand-adapted regulation of early hematopoiesis in infection and inflammation. Blood. 2012;119(13): 2991-3002.
63. Chen J, Feng X, Desierto MJ, Keyvanfar K, Young NS. IFN-g-mediated hematopoietic cell destruction in murine models of immune-mediated bone marrow failure. Blood. 2015;126(24): 2621-2631.
64. Corat MAF, Schlums H, Wu C, et al. Acquired somatic mutations in PNH reveal long-term maintenance of adaptive NK cells independent from HSPC [published online ahead of print 30 November 2016]. Blood. doi:10.1182/blood-2016-08-734285.
65. Childs RW, Carlsten M. Therapeutic approaches to enhance natural killer cell cytotoxicity against cancer: the force awakens. Nat Rev Drug Discov. 2015;14(7):487-498.
66. Cichocki F, Verneris MR, Cooley S, et al. The past, present, and future of NK cells in hematopoietic cell transplantation and adoptive transfer. Curr Top Microbiol Immunol. 2016;395: 225-243.