NK cells and other innate lymphoid cells in hematopoietic stem cell transplantation

Frontiers in Immunology

Volumn 7, Issue MAY, 2016, Pages

  Vacca, Paola ^a   Montaldo, Elisa ^b   Croxatto, Daniele ^a   Moretta, Francesca ^c,d   Bertaina, Alice ^e   Vitale, Chiara ^a,f   Locatelli, Franco ^e,g   Mingari, Maria Cristina ^a,f,h   Moretta, Lorenzo ^e  

^a UNIVERSITY OF GENOA   (Italy)

^b SAN RAFFAELE SCIENTIFIC INSTITUTE   (Italy)

^c UNIVERSITY OF VERONA   (Italy)

^d Stroke Center   (Italy)

^e BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^f UNIVERSITY OF GENOA   (Italy)

^g UNIVERSITY OF PAVIA   (Italy)

^h Centro di Eccellenza per la Ricerca Biomedica   (Italy)

Author keywords

GVHD; Hematopoietic stem cell transplantation; Innate lymphoid cells; NK cells

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 22; NUCLEAR RECEPTOR NR4A3; VASCULAR CELL ADHESION MOLECULE 1;

CELL MATURATION; CYTOTOXICITY; DYNAMICS; GRAFT VERSUS HOST REACTION; HAPLOTYPE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HOMEOSTASIS; HUMAN; LYMPHOID CELL; NATURAL KILLER T CELL; NONHUMAN; OPPORTUNISTIC INFECTION; SHORT SURVEY; T CELL DEPLETION;

EID: 84973560595     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00188     Document Type: Short Survey

References (68)

1. Copelan EA. Hematopoietic stem-cell transplantation. N Engl J Med (2006) 354:1813-26. doi:10.1056/NEJMra052638
2. Danby R, Rocha V. Improving engraftment and immune reconstitution in umbilical cord blood transplantation. Front Immunol (2014) 5:68. doi:10.3389/fimmu.2014.00068
3. Locatelli F, Pende D, Mingari MC, Bertaina A, Falco M, Moretta A, et al. Cellular and molecular basis of haploidentical hematopoietic stem cell transplantation in the successful treatment of high-risk leukemias: role of alloreactive NK cells. Front Immunol (2013) 4:15. doi:10.3389/fimmu.2013.00015
4. Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science (2002) 295:2097-100. doi:10.1126/science.1068440
5. Moretta L, Locatelli F, Pende D, Marcenaro E, Mingari MC, Moretta A. Killer Ig-like receptor-mediated control of natural killer cell alloreactivity in haploidentical hematopoietic stem cell transplantation. Blood (2011) 117:764-71. doi:10.1182/blood-2010-08-264085
6. Diefenbach A, Colonna M, Koyasu S. Development, differentiation, and diversity of innate lymphoid cells. Immunity (2014) 41:354-65. doi:10.1016/j.immuni.2014.09.005
7. Seillet C, Belz GT, Huntington ND. Development, homeostasis, and heterogeneity of NK cells and ILC1. Curr Top Microbiol Immunol (2015) 395:37-61. doi:10.1007/82_2015_474
8. Halim TY. Group 2 innate lymphoid cells in disease. Int Immunol (2016) 28:13-22. doi:10.1093/intimm/dxv050
9. Montaldo E, Juelke K, Romagnani C. Group 3 innate lymphoid cells (ILC3s): origin, differentiation, and plasticity in humans and mice. Eur J Immunol (2015) 45:2171-82. doi:10.1002/eji.201545598
10. Montaldo E, Vacca P, Vitale C, Moretta F, Locatelli F, Mingari MC, et al. Human innate lymphoid cells. Immunol Lett (2016). doi:10.1016/j.imlet.2016.01.007
11. Renoux VM, Zriwil A, Peitzsch C, Michaelsson J, Friberg D, Soneji S, et al. Identification of a human natural killer cell lineage-restricted progenitor in fetal and adult tissues. Immunity (2015) 43:394-407. doi:10.1016/j.immuni.2015.07.011
12. Montaldo E, Teixeira-Alves LG, Glatzer T, Durek P, Stervbo U, Hamann W, et al. Human RORgammat(+)CD34(+) cells are lineage-specified progenitors of group 3 RORgammat(+) innate lymphoid cells. Immunity (2014) 41:988-1000. doi:10.1016/j.immuni.2014.11.010
13. McKenzie AN, Spits H, Eberl G. Innate lymphoid cells in inflammation and immunity. Immunity (2014) 41:366-74. doi:10.1016/j.immuni.2014.09.006
14. Sonnenberg GF, Artis D. Innate lymphoid cells in the initiation, regulation and resolution of inflammation. Nat Med (2015) 21:698-708. doi:10.1038/nm.3892
15. Bernink JH, Peters CP, Munneke M, te Velde AA, Meijer SL, Weijer K, et al. Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat Immunol (2013) 14:221-9. doi:10.1038/ni.2534
16. Fuchs A, Vermi W, Lee JS, Lonardi S, Gilfillan S, Newberry RD, et al. Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12-and IL-15-responsive IFN-gamma-producing cells. Immunity (2013) 38:769-81. doi:10.1016/j.immuni.2013.02.010
17. Vacca P, Montaldo E, Croxatto D, Loiacono F, Canegallo F, Venturini PL, et al. Identification of diverse innate lymphoid cells in human decidua. Mucosal Immunol (2015) 8:254-64. doi:10.1038/mi.2014.63
18. Klose CS, Flach M, Mohle L, Rogell L, Hoyler T, Ebert K, et al. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell (2014) 157:340-56. doi:10.1016/j.cell.2014.03.030
19. Horowitz A, Stegmann KA, Riley EM. Activation of natural killer cells during microbial infections. Front Immunol (2012) 2:88. doi:10.3389/fimmu.2011.00088
20. Lanier LL. Evolutionary struggles between NK cells and viruses. Nat Rev Immunol (2008) 8:259-68. doi:10.1038/nri2276
21. Moretta L, Pietra G, Montaldo E, Vacca P, Pende D, Falco M, et al. Human NK cells: from surface receptors to the therapy of leukemias and solid tumors. Front Immunol (2014) 5:87. doi:10.3389/fimmu.2014.00087
22. Moro K, Yamada T, Tanabe M, Takeuchi T, Ikawa T, Kawamoto H, et al. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature (2010) 463:540-4. doi:10.1038/nature08636
23. Neill DR, Wong SH, Bellosi A, Flynn RJ, Daly M, Langford TK, et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature (2010) 464:1367-70. doi:10.1038/nature08900
24. Price AE, Liang HE, Sullivan BM, Reinhardt RL, Eisley CJ, Erle DJ, et al. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc Natl Acad Sci U S A (2010) 107:11489-94. doi:10.1073/pnas.1003988107
25. Maizels RM, Hewitson JP, Smith KA. Susceptibility and immunity to helminth parasites. Curr Opin Immunol (2012) 24:459-66. doi:10.1016/j.coi.2012.06.003
26. Cella M, Fuchs A, Vermi W, Facchetti F, Otero K, Lennerz JK, et al. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature (2009) 457:722-5. doi:10.1038/nature07537
27. Gladiator A, Wangler N, Trautwein-Weidner K, LeibundGut-Landmann S. Cutting edge: IL-17-secreting innate lymphoid cells are essential for host defense against fungal infection. J Immunol (2013) 190:521-5. doi:10.4049/jimmunol.1202924
28. Satoh-Takayama N, Vosshenrich CA, Lesjean-Pottier S, Sawa S, Lochner M, Rattis F, et al. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity (2008) 29:958-70. doi:10.1016/j.immuni.2008.11.001
29. Sonnenberg GF, Monticelli LA, Elloso MM, Fouser LA, Artis D. CD4(+) lymphoid tissue-inducer cells promote innate immunity in the gut. Immunity (2011) 34:122-34. doi:10.1016/j.immuni.2010.12.009
30. Zheng Y, Valdez PA, Danilenko DM, Hu Y, Sa SM, Gong Q, et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med (2008) 14:282-9. doi:10.1038/nm1720
31. Croxatto D, Micheletti A, Montaldo E, Orecchia P, Loiacono F, Canegallo F, et al. Group 3 innate lymphoid cells regulate neutrophil migration and function in human decidua. Mucosal Immunol (2016). doi:10.1038/mi.2016.10
32. Monticelli LA, Sonnenberg GF, Abt MC, Alenghat T, Ziegler CG, Doering TA, et al. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat Immunol (2011) 12:1045-54. doi:10.1031/ni.2131
33. Finke D. Fate and function of lymphoid tissue inducer cells. Curr Opin Immunol (2005) 17:144-50. doi:10.1016/j.coi.2005.01.006
34. Scandella E, Bolinger B, Lattmann E, Miller S, Favre S, Littman DR, et al. Restoration of lymphoid organ integrity through the interaction of lymphoid tissue-inducer cells with stroma of the T cell zone. Nat Immunol (2008) 9:667-75. doi:10.1038/ni.1605
35. Hanash AM, Dudakov JA, Hua G, O'Connor MH, Young LF, Singer NV, et al. Interleukin-22 protects intestinal stem cells from immune-mediated tissue damage and regulates sensitivity to graft versus host disease. Immunity (2012) 37:339-50. doi:10.1016/j.immuni.2012.05.028
36. Lindemans CA, Calafiore M, Mertelsmann AM, O'Connor MH, Dudakov JA, Jenq RR, et al. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature (2015) 528:560-4. doi:10.1038/nature16460
37. Munneke JM, Bjorklund AT, Mjosberg JM, Garming-Legert K, Bernink JH, Blom B, et al. Activated innate lymphoid cells are associated with a reduced susceptibility to graft-versus-host disease. Blood (2014) 124:812-21. doi:10.1182/blood-2013-11-536888
38. Mohty M, Malard F, Savani BN. High-dose total body irradiation and myeloablative conditioning before allogeneic hematopoietic cell transplantation: time to rethink? Biol Blood Marrow Transplant (2015) 21:620-4. doi:10.1016/j.bbmt.2014.09.010
39. Shlomchik WD. Graft-versus-host disease. Nat Rev Immunol (2007) 7:340-52. doi:10.1038/nri2000
40. Rangel-Moreno J, de la Luz Garcia-Hernandez M, Ramos-Payan R, Biear J, Hernady E, Sangster MY, et al. Long-lasting impact of neonatal exposure to total body gamma radiation on secondary lymphoid organ structure and function. Radiat Res (2015) 184:352-66. doi:10.1667/RR14047.1
41. Dudakov JA, Hanash AM, Jenq RR, Young LF, Ghosh A, Singer NV, et al. Interleukin-22 drives endogenous thymic regeneration in mice. Science (2012) 336:91-5. doi:10.1126/science.1218004
42. Konya V, Mjosberg J. Innate lymphoid cells in graft-versus-host disease. Am J Transplant (2015) 15:2795-801. doi:10.1111/ajt.13394
43. Moretta F, Petronelli F, Lucarelli B, Pitisci A, Bertaina A, Locatelli F, et al. The generation of human innate lymphoid cells is influenced by the source of hematopoietic stem cells and by the use of G-CSF. Eur J Immunol (2016) 46:1271-8. doi:10.1002/eji.201546079
44. Bendall LJ, Bradstock KF. G-CSF: from granulopoietic stimulant to bone marrow stem cell mobilizing agent. Cytokine Growth Factor Rev (2014) 25:355-67. doi:10.1016/j.cytogfr.2014.07.011
45. Trabanelli S, Curti A, Lecciso M, Salome B, Riether C, Ochsenbein A, et al. CD127+ innate lymphoid cells are dysregulated in treatment naive acute myeloid leukemia patients at diagnosis. Haematologica (2015) 100:e257-60. doi:10.3324/haematol.2014.119602
46. Vitale C, Ambrosini P, Montaldo E, Ballerini F, Moretta L, Mingari MC. IL-1beta-releasing human acute myeloid leukemia blasts modulate natural killer cell differentiation from CD34+ precursors. Haematologica (2015) 100:e42-5. doi:10.3324/haematol.2014.110494
47. Vitale C, Chiossone L, Morreale G, Lanino E, Cottalasso F, Moretti S, et al. Analysis of the activating receptors and cytolytic function of human natural killer cells undergoing in vivo differentiation after allogeneic bone marrow transplantation. Eur J Immunol (2004) 34:455-60. doi:10.1002/eji.200324668
48. Wang H, Grzywacz B, Sukovich D, McCullar V, Cao Q, Lee AB, et al. The unexpected effect of cyclosporin A on CD56+CD16-and CD56+CD16+ natural killer cell subpopulations. Blood (2007) 110:1530-9. doi:10.1182/blood-2006-10-048173
49. Rankin LC, Groom JR, Chopin M, Herold MJ, Walker JA, Mielke LA, et al. The transcription factor T-bet is essential for the development of NKp46+ innate lymphocytes via the Notch pathway. Nat Immunol (2013) 14:389-95. doi:10.1038/ni.2545
50. Satoh-Takayama N, Serafini N, Verrier T, Rekiki A, Renauld JC, Frankel G, et al. The chemokine receptor CXCR6 controls the functional topography of interleukin-22 producing intestinal innate lymphoid cells. Immunity (2014) 41:776-88. doi:10.1016/j.immuni.2014.10.007
51. Rankin LC, Girard-Madoux MJ, Seillet C, Mielke LA, Kerdiles Y, Fenis A, et al. Complementarity and redundancy of IL-22-producing innate lymphoid cells. Nat Immunol (2016) 17:179-86. doi:10.1038/ni.3332
52. Orange JS. Natural killer cell deficiency. J Allergy Clin Immunol (2013) 132:515-25. doi:10.1016/j.jaci.2013.07.020 quiz 526
53. Chijioke O, Muller A, Feederle R, Barros MH, Krieg C, Emmel V, et al. Human natural killer cells prevent infectious mononucleosis features by targeting lytic Epstein-Barr virus infection. Cell Rep (2013) 5:1489-98. doi:10.1016/j.celrep.2013.11.041
54. Della Chiesa M, Sivori S, Carlomagno S, Moretta L, Moretta A. Activating KIRs and NKG2C in viral infections: toward NK cell memory? Front Immunol (2015) 6:573. doi:10.3389/fimmu.2015.00573
55. Foley B, Felices M, Cichocki F, Cooley S, Verneris MR, Miller JS. The biology of NK cells and their receptors affects clinical outcomes after hematopoietic cell transplantation (HCT). Immunol Rev (2014) 258:45-63. doi:10.1111/imr.12157
56. Palmer JM, Rajasekaran K, Thakar MS, Malarkannan S. Clinical relevance of natural killer cells following hematopoietic stem cell transplantation. J Cancer (2013) 4:25-35. doi:10.7150/jca.5049
57. Beck JC, Wagner JE, DeFor TE, Brunstein CG, Schleiss MR, Young JA, et al. Impact of cytomegalovirus (CMV) reactivation after umbilical cord blood transplantation. Biol Blood Marrow Transplant (2010) 16:215-22. doi:10.1016/j.bbmt.2009.09.019
58. Beziat V, Dalgard O, Asselah T, Halfon P, Bedossa P, Boudifa A, et al. CMV drives clonal expansion of NKG2C+ NK cells expressing self-specific KIRs in chronic hepatitis patients. Eur J Immunol (2012) 42:447-57. doi:10.1002/eji.201141826
59. Beziat V, Liu LL, Malmberg JA, Ivarsson MA, Sohlberg E, Bjorklund AT, et al. NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs. Blood (2013) 121:2678-88. doi:10.1182/blood-2012-10-459545
60. Bjorkstrom NK, Lindgren T, Stoltz M, Fauriat C, Braun M, Evander M, et al. Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J Exp Med (2011) 208:13-21. doi:10.1084/jem.20100762
61. Bjorkstrom NK, Svensson A, Malmberg KJ, Eriksson K, Ljunggren HG. Characterization of natural killer cell phenotype and function during recurrent human HSV-2 infection. PLoS One (2011) 6:e27664. doi:10.1371/journal.pone.0027664
62. Della Chiesa M, Falco M, Bertaina A, Muccio L, Alicata C, Frassoni F, et al. Human cytomegalovirus infection promotes rapid maturation of NK cells expressing activating killer Ig-like receptor in patients transplanted with NKG2C-/-umbilical cord blood. J Immunol (2014) 192:1471-9. doi:10.4049/jimmunol.1302053
63. Della Chiesa M, Falco M, Podesta M, Locatelli F, Moretta L, Frassoni F, et al. Phenotypic and functional heterogeneity of human NK cells developing after umbilical cord blood transplantation: a role for human cytomegalovirus? Blood (2012) 119:399-410. doi:10.1182/blood-2011-08-372003
64. Foley B, Cooley S, Verneris MR, Curtsinger J, Luo X, Waller EK, et al. Human cytomegalovirus (CMV)-induced memory-like NKG2C(+) NK cells are transplantable and expand in vivo in response to recipient CMV antigen. J Immunol (2012) 189:5082-8. doi:10.4049/jimmunol.1201964
65. Foley B, Cooley S, Verneris MR, Pitt M, Curtsinger J, Luo X, et al. Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood (2012) 119:2665-74. doi:10.1182/blood-2011-10-386995
66. Guma M, Angulo A, Vilches C, Gomez-Lozano N, Malats N, Lopez-Botet M. Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood (2004) 104:3664-71. doi:10.1182/blood-2004-05-2058
67. Muccio L, Bertaina A, Falco M, Pende D, Meazza R, Lopez-Botet M, et al. Analysis of memory-like natural killer cells in human cytomegalovirus-infected children undergoing aβ+T-and B-cell depleted HSCT for hematological malignancies. Haematologica (2016) 101:371-81. doi:10.3324/haematol.2015.134155
68. Petitdemange C, Becquart P, Wauquier N, Beziat V, Debre P, Leroy EM, et al. Unconventional repertoire profile is imprinted during acute chikungunya infection for natural killer cells polarization toward cytotoxicity. PLoS Pathog (2011) 7:e1002268. doi:10.1371/journal.ppat.1002268