Generation of Natural Killer Cell Memory during Viral Infection

Journal of Innate Immunity

Volumn 7, Issue 6, 2015, Pages 557-562

  O'Sullivan, Timothy E ^a   Sun, Joseph C ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Cytomegalovirus; Immunological memory; Natural killer cells

Indexed keywords

VIRUS ANTIGEN;

ADAPTIVE IMMUNITY; APOPTOSIS; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL EXPANSION; CELL PROLIFERATION; HUMAN; LYMPHOID PROGENITOR CELL; MEMORY CELL; MEMORY T LYMPHOCYTE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; VIRAL CLEARANCE; VIRUS INFECTION; ANIMAL; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; INNATE IMMUNITY; MOUSE;

ANIMALS; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC MEMORY; KILLER CELLS, NATURAL; MICE; VIRUS DISEASES;

EID: 84945497420     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000375494     Document Type: Review

References (49)

1. Williams MA, Bevan MJ: Effector and memory CTL differentiation. Annu Rev Immunol 2007; 25: 171-192.
2. Kondo M, Weissman IL, Akashi K: Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997; 91: 661-672.
3. Di Santo JP: Natural killer cell developmental pathways: A question of balance. Annu Rev Immunol 2006; 24: 257-286.
4. Karo JM, Schatz DG, Sun JC: The RAG recombinase dictates functional heterogeneity and cellular fitness in natural killer cells. Cell 2014; 159: 94-107.
5. Sun JC, Lanier LL: NK cell development, homeostasis and function: parallels with CD8(+) T cells. Nat Rev Immunol 2011; 11: 645-657.
6. Orr MT, Lanier LL: Natural killer cell education and tolerance. Cell 2010; 142: 847-856.
7. Arase H, Mocarski ES, Campbell AE, Hill AB, Lanier LL: Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 2002; 296: 1323-1326.
8. Smith HR, Heusel JW, Mehta IK, Kim S, Dorner BG, Naidenko OV, Iizuka K, Furukawa H, Beckman DL, Pingel JT, Scalzo AA, Fremont DH, Yokoyama WM: Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc Natl Acad Sci USA 2002; 99: 8826-8831.
9. Daniels KA, Devora G, Lai WC, O'Donnell CL, Bennett M, Welsh RM: Murine cytomegalovirus is regulated by a discrete subset of natural killer cells reactive with monoclonal antibody to Ly49H. J Exp Med 2001; 194: 29-44.
10. Dokun AO, Kim S, Smith HR, Kang HS, Chu DT, Yokoyama WM: Specific and nonspecific NK cell activation during virus infection. Nat Immunol 2001; 2: 951-956.
11. Brown MG, Dokun AO, Heusel JW, Smith HR, Beckman DL, Blattenberger EA, Dubbelde CE, Stone LR, Scalzo AA, Yokoyama WM: Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 2001; 292: 934-937.
12. Sun JC, Beilke JN, Lanier LL: Adaptive immune features of natural killer cells. Nature 2009; 457: 557-561.
13. Min-Oo G, Lanier LL: Cytomegalovirus generates long-lived antigen-specific NK cells with diminished bystander activation to heterologous infection. J Exp Med 2014; 211: 1289-1296.
14. O'Leary JG, Goodarzi M, Drayton DL, von Andrian UH: T cell-and B cell-independent adaptive immunity mediated by natural killer cells. Nat Immunol 2006; 7: 507-516.
15. Cooper MA, Elliott JM, Keyel PA, Yang L, Carrero JA, Yokoyama WM: Cytokine-induced memory-like natural killer cells. Proc Natl Acad Sci USA 2009; 106: 1915-1919.
16. Sun JC, Madera S, Bezman NA, Beilke JN, Kaplan MH, Lanier LL: Proinflammatory cytokine signaling required for the generation of natural killer cell memory. J Exp Med 2012; 209: 947-954.
17. Beaulieu AM, Zawislak CL, Nakayama T, Sun JC: The transcription factor Zbtb32 controls the proliferative burst of virus-specific natural killer cells responding to infection. Nat Immunol 2014; 15: 546-553.
18. Nabekura T, Kanaya M, Shibuya A, Fu G, Gascoigne NR, Lanier LL: Costimulatory molecule DNAM-1 is essential for optimal differentiation of memory natural killer cells during mouse cytomegalovirus infection. Immunity 2014; 40: 225-234.
19. Marrack P, Kappler J: Control of T cell viability. Annu Rev Immunol 2004; 22: 765-787.
20. Grayson JM, Zajac AJ, Altman JD, Ahmed R: Cutting edge: increased expression of Bcl-2 in antigen-specific memory CD8+ T cells. J Immunol 2000; 164: 3950-3954.
21. Hildeman DA, Zhu Y, Mitchell TC, Bouillet P, Strasser A, Kappler J, Marrack P: Activated T cell death in vivo mediated by proapoptotic bcl-2 family member bim. Immunity 2002; 16: 759-767.
22. Prlic M, Bevan MJ: Exploring regulatory mechanisms of CD8+ T cell contraction. Proc Natl Acad Sci USA 2008; 105: 16689-16694.
23. Min-Oo G, Bezman NA, Madera S, Sun JC, Lanier LL: Proapoptotic Bim regulates antigen-specific NK cell contraction and the generation of the memory NK cell pool after cytomegalovirus infection. J Exp Med 2014; 211: 1289-1296.
24. Firth MA, Madera S, Beaulieu AM, Gasteiger G, Castillo EF, Schluns KS, Kubo M, Rothman PB, Vivier E, Sun JC: Nfil3-independent lineage maintenance and antiviral response of natural killer cells. J Exp Med 2013; 210: 2981-2990.
25. Zawislak CL, Beaulieu AM, Loeb GB, Karo J, Canner D, Bezman NA, Lanier LL, Rudensky AY, Sun JC: Stage-specific regulation of natural killer cell homeostasis and response against viral infection by microRNA-155. Proc Natl Acad Sci USA 2013; 110: 6967-6972.
26. Puleston DJ, Zhang H, Powell TJ, Lipina E, Sims S, Panse I, Watson AS, Cerundolo V, Townsend AR, Klenerman P, Simon AK: Autophagy is a critical regulator of memory CD8(+) T cell formation. Elife 2014; 3.
27. Sun JC, Xu T, Zuo Q, Wang RB, Qi AQ, Cao WL, Sun AJ, Sun XJ, Xu J: Hydrogen-rich saline promotes survival of retinal ganglion cells in a rat model of optic nerve crush. PLoS One 2014; 9:e99299.
28. Paust S, Gill HS, Wang BZ, Flynn MP, Moseman EA, Senman B, Szczepanik M, Telenti A, Askenase PW, Compans RW, von Andrian UH: Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat Immunol 2010; 11: 1127-1135.
29. Abdul-Careem MF, Lee AJ, Pek EA, Gill N, Gillgrass AE, Chew MV, Reid S, Ashkar AA: Genital HSV-2 infection induces short-term NK cell memory. PLoS One 2012; 7:e32821.
30. Gillard GO, Bivas-Benita M, Hovav AH, Grandpre LE, Panas MW, Seaman MS, Haynes BF, Letvin NL: Thy1+ NK [corrected] cells from vaccinia virus-primed mice confer protection against vaccinia virus challenge in the absence of adaptive lymphocytes. PLoS Pathog 2011; 7:e1002141.
31. Gazit R, Gruda R, Elboim M, Arnon TI, Katz G, Achdout H, Hanna J, Qimron U, Landau G, Greenbaum E, Zakay-Rones Z, Porgador A, Mandelboim O: Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat Immunol 2006; 7: 517-523.
32. Draghi M, Pashine A, Sanjanwala B, Gendzekhadze K, Cantoni C, Cosman D, Moretta A, Valiante NM, Parham P: NKp46 and NKG2D recognition of infected dendritic cells is necessary for NK cell activation in the human response to influenza infection. J Immunol 2007; 178: 2688-2698.
33. van Helden MJ, de Graaf N, Boog CJ, Topham DJ, Zaiss DM, Sijts AJ: The bone marrow functions as the central site of proliferation for long-lived NK cells. J Immunol 2012; 189: 2333-2337.
34. Orange JS: Human natural killer cell deficiencies and susceptibility to infection. Microbes Infect 2002; 4: 1545-1558.
35. Lopez-Verges S, Milush JM, Schwartz BS, Pando MJ, Jarjoura J, York VA, Houchins JP, Miller S, Kang SM, Norris PJ, Nixon DF, Lanier LL: Expansion of a unique CD57(+) NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. Proc Natl Acad Sci USA 2011; 108: 14725-14732.
36. Guma M, Budt M, Saez A, Brckalo T, Hengel H, Angulo A, Lopez-Botet M: Expansion of CD94/NKG2C+ NK cells in response to human cytomegalovirus-infected fibroblasts. Blood 2006; 107: 3624-3631.
37. Rolle A, Pollmann J, Ewen EM, Le VT, Halenius A, Hengel H, Cerwenka A: IL-12-producing monocytes and HLA-E control HCMV-driven NKG2C+ NK cell expansion. J Clin Invest 2014; 124: 5305-5316.
38. Foley B, Cooley S, Verneris MR, Curtsinger J, Luo X, Waller EK, Anasetti C, Weisdorf D, Miller JS: Human cytomegalovirus (CMV)-induced memory-like NKG2C(+) NK cells are transplantable and expand in vivo in response to recipient CMV antigen. J Immunol 2012; 189: 5082-5088.
39. Foley B, Cooley S, Verneris MR, Pitt M, Curtsinger J, Luo X, Lopez-Verges S, Lanier LL, Weisdorf D, Miller JS: Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood 2012; 119: 2665-2674.
40. Della Chiesa M, Falco M, Podesta M, Locatelli F, Moretta L, Frassoni F, Moretta A: Phenotypic and functional heterogeneity of human NK cells developing after umbilical cord blood transplantation: A role for human cytomegalovirus? Blood 2012; 119: 399-410.
41. Lopez-Verges S, Milush JM, Pandey S, York VA, Arakawa-Hoyt J, Pircher H, Norris PJ, Nixon DF, Lanier LL: CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset. Blood 2010; 116: 3865-3874.
42. Luetke-Eversloh M, Hammer Q, Durek P, Nordstrom K, Gasparoni G, Pink M, Hamann A, Walter J, Chang HD, Dong J, Romagnani C: Human cytomegalovirus drives epigenetic imprinting of the IFNG locus in NKG2Chi natural killer cells. PLoS Pathog 2014; 10:e1004441.
43. Goodier MR, White MJ, Darboe A, Nielsen CM, Goncalves A, Bottomley C, Moore SE, Riley EM: Rapid NK cell differentiation in a population with near-universal human cytomegalovirus infection is attenuated by NKG2C deletions. Blood 2014; 124: 2213-2222.
44. Muntasell A, Lopez-Montanes M, Vera A, Heredia G, Romo N, Penafiel J, Moraru M, Vila J, Vilches C, Lopez-Botet M: NKG2C zygosity influences CD94/NKG2C receptor function and the NK-cell compartment redistribution in response to human cytomegalovirus. Eur J Immunol 2013; 43: 3268-3278.
45. Beziat V, Dalgard O, Asselah T, Halfon P, Bedossa P, Boudifa A, Hervier B, Theodorou I, Martinot M, Debre P, Bjorkstrom NK, Malmberg KJ, Marcellin P, Vieillard V: CMV drives clonal expansion of NKG2C+ NK cells expressing self-specific KIRs in chronic hepatitis patients. Eur J Immunol 2012; 42: 447-457.
46. Brunetta E, Fogli M, Varchetta S, Bozzo L, Hudspeth KL, Marcenaro E, Moretta A, Mavilio D: Chronic HIV-1 viremia reverses NKG2A/NKG2C ratio on natural killer cells in patients with human cytomegalovirus coinfection. AIDS 2010; 24: 27-34.
47. Bjorkstrom NK, Lindgren T, Stoltz M, Fauriat C, Braun M, Evander M, Michaelsson J, Malmberg KJ, Klingstrom J, Ahlm C, Ljunggren HG: Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J Exp Med 2011; 208: 13-21.
48. Saghafian-Hedengren S, Sohlberg E, Theorell J, Carvalho-Queiroz C, Nagy N, Persson JO, Nilsson C, Bryceson YT, Sverremark-Ekstrom E: Epstein-Barr virus coinfection in children boosts cytomegalovirus-induced differentiation of natural killer cells. J Virol 2013; 87: 13446-13455.
49. Hendricks DW, Balfour HH Jr, Dunmire SK, Schmeling DO, Hogquist KA, Lanier LL: Cutting edge: NKG2C(hi)CD57+ NK cells respond specifically to acute infection with cytomegalovirus and not Epstein-Barr virus. J Immunol 2014; 192: 4492-4496.