Role of distinct natural killer cell subsets in anticancer response

Frontiers in Immunology

Volumn 8, Issue MAR, 2017, Pages

  Stabile, Helena ^a   Fionda, Cinzia ^a   Gismondi, Angela ^a,b   Santoni, Angela ^a,b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Hematological malignancies; Natural killer cell subset; Natural killer cells; Solid tumors; Tumor microenvironment

Indexed keywords

CD56 ANTIGEN;

ANTINEOPLASTIC ACTIVITY; CELL DIFFERENTIATION; HEMATOLOGIC MALIGNANCY; HUMAN; IMMUNE RESPONSE; NATURAL KILLER CELL; SHORT SURVEY; SOLID TUMOR; TUMOR ASSOCIATED LEUKOCYTE; TUMOR ESCAPE; TUMOR MICROENVIRONMENT;

EID: 85017195553     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.00293     Document Type: Short Survey

References (81)

1. Artis D, Spits H. The biology of innate lymphoid cells. Nature (2015) 517:293-301. doi:10.1038/nature14189
2. Caligiuri MA. Human natural killer cells. Blood (2008) 112:461-9. doi:10.1182/blood-2007-09-077438
3. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, et al. Innate or adaptive immunity? The example of natural killer cells. Science (2011) 331:44-9. doi:10.1126/science.1198687
4. Lanier LL. NK cell recognition. Annu Rev Immunol (2005) 23:225-74. doi:10.1146/annurev.immunol.23.021704.115526
5. Freud AG, Caligiuri MA. Human natural killer cell development. Immunol Rev (2006) 214:56-72. doi:10.1111/j.1600-065X.2006.00451.x
6. Freud AG, Yu J, Caligiuri MA. Human natural killer cell development in secondary lymphoid tissues. Semin Immunol (2014) 26:132-7. doi:10.1016/j.smim.2014.02.008
7. Di Santo JP, Vosshenrich CA. Bone marrow versus thymic pathways of natural killer cell development. Immunol Rev (2006) 214:35-46. doi:10.1111/j.1600-065X.2006.00461.x
8. Fehniger TA, Cooper MA, Nuovo GJ, Cella M, Facchetti F, Colonna M, et al. CD56bright natural killer cells are present in human lymph nodes and are activated by T cell-derived IL-2: a potential new link between adaptive and innate immunity. Blood (2003) 101:3052-7. doi:10.1182/blood-2002-09-2876
9. Santoni A, Carlino C, Gismondi A. Uterine NK cell development, migration and function. Reprod Biomed Online (2008) 16:202-10. doi:10.1016/S1472-6483(10)60575-5
10. Romagnani C, Juelke K, Falco M, Morandi B, D'Agostino A, Costa R, et al. CD56bright. J Immunol (2007) 178:4947-55. doi:10.4049/jimmunol.178.8.4947
11. Michel T, Poli A, Cuapio A, Briquemont B, Iserentant G, Ollert M, et al. Human CD56bright NK cells: an update. J Immunol (2016) 196:2923-31. doi:10.4049/jimmunol.1502570
12. Gineau L, Cognet C, Kara N, Lach FP, Dunne J, Veturi U, et al. Partial MCM4 deficiency in patients with growth retardation, adrenal insufficiency, and natural killer cell deficiency. J Clin Invest (2012) 122:821-32. doi:10.1172/JCI61014
13. Mace EM, Hsu AP, Monaco-Shawver L, Makedonas G, Rosen JB, Dropulic L, et al. Mutations in GATA2 cause human NK cell deficiency with specific loss of the CD56(bright) subset. Blood (2013) 121:2669-77. doi:10.1182/blood-2012-09-453969
14. Sojka DK, Tian Z, Yokoyama WM. Tissue-resident natural killer cells and their potential diversity. Semin Immunol (2014) 26:127-31. doi:10.1016/j.smim.2014.01.010
15. Lugthart G, Melsen JE, Vervat C, van Ostaijen-Ten Dam MM, Corver WE, Roelen DL, et al. Human lymphoid tissues harbor a distinct CD69+CXCR6+ NK cell population. J Immunol (2016) 197:78-84. doi:10.4049/jimmunol.1502603
16. Stegmann KA, Robertson F, Hansi N, Gill U, Pallant C, Christophides T, et al. CXCR6 marks a novel subset of T-bet(lo)Eomes(hi) natural killer cells residing in human liver. Sci Rep (2016) 6:26157. doi:10.1038/srep26157
17. Harmon C, Robinson MW, Fahey R, Whelan S, Houlihan DD, Geoghegan J, et al. Tissue-resident Eomes(hi) T-bet(lo) CD56(bright) NK cells with reduced proinflammatory potential are enriched in the adult human liver. Eur J Immunol (2016) 46:2111-20. doi:10.1002/eji.201646559
18. Melsen JE, Lugthart G, Lankester AC, Schilham MW. Human circulating and tissue-resident CD56(bright) natural killer cell populations. Front Immunol (2016) 7:262. doi:10.3389/fimmu.2016.00262
19. Bernardini G, Sciume G, Santoni A. Differential chemotactic receptor requirements for NK cell subset trafficking into bone marrow. Front Immunol (2013) 4:12. doi:10.3389/fimmu.2013.00012
20. Carrega P, Bonaccorsi I, Di CE, Morandi B, Paul P, Rizzello V, et al. CD56(bright)perforin(low) noncytotoxic human NK cells are abundant in both healthy and neoplastic solid tissues and recirculate to secondary lymphoid organs via afferent lymph. J Immunol (2014) 192:3805-15. doi:10.4049/jimmunol.1301889
21. Hudspeth K, Donadon M, Cimino M, Pontarini E, Tentorio P, Preti M, et al. Human liver-resident CD56(bright)/CD16(neg) NK cells are retained within hepatic sinusoids via the engagement of CCR5 and CXCR6 pathways. J Autoimmun (2016) 66:40-50. doi:10.1016/j.jaut.2015.08.011
22. Cichocki F, Sitnicka E, Bryceson YT. NK cell development and function-plasticity and redundancy unleashed. Semin Immunol (2014) 26:114-26. doi:10.1016/j.smim.2014.02.003
23. Bruno A, Ferlazzo G, Albini A, Noonan DM. A think tank of TINK/TANKs: tumor-infiltrating/tumor-associated natural killer cells in tumor progression and angiogenesis. J Natl Cancer Inst (2014) 106:dju200. doi:10.1093/jnci/dju200
24. Cantoni C, Huergo-Zapico L, Parodi M, Pedrazzi M, Mingari MC, Moretta A, et al. NK cells, tumor cell transition, and tumor progression in solid malignancies: new hints for NK-based immunotherapy? J Immunol Res (2016) 2016:4684268. doi:10.1155/2016/4684268
25. Levi I, Amsalem H, Nissan A, Darash-Yahana M, Peretz T, Mandelboim O, et al. Characterization of tumor infiltrating natural killer cell subset. Oncotarget (2015) 6:13835-43. doi:10.18632/oncotarget.3453
26. Bruno A, Focaccetti C, Pagani A, Imperatori AS, Spagnoletti M, Rotolo N, et al. The proangiogenic phenotype of natural killer cells in patients with non-small cell lung cancer. Neoplasia (2013) 15:133-42. doi:10.1593/neo.121758
27. Hasmim M, Messai Y, Ziani L, Thiery J, Bouhris JH, Noman MZ, et al. Critical role of tumor microenvironment in shaping NK cell functions: implication of hypoxic stress. Front Immunol (2015) 6:482. doi:10.3389/fimmu.2015.00482
28. Carrega P, Ferlazzo G. Natural killer cell distribution and trafficking in human tissues. Front Immunol (2012) 3:347. doi:10.3389/fimmu.2012.00347
29. Tallerico R, Garofalo C, Carbone E. A new biological feature of natural killer cells: the recognition of solid tumor-derived cancer stem cells. Front Immunol (2016) 7:179. doi:10.3389/fimmu.2016.00179
30. Pasero C, Gravis G, Granjeaud S, Guerin M, Thomassin-Piana J, Rocchi P, et al. Highly effective NK cells are associated with good prognosis in patients with metastatic prostate cancer. Oncotarget (2015) 6:14360-73. doi:10.18632/oncotarget.3965
31. Messaoudene M, Fregni G, Fourmentraux-Neves E, Chanal J, Maubec E, Mazouz-Dorval S, et al. Mature cytotoxic CD56(bright)/CD16(+) natural killer cells can infiltrate lymph nodes adjacent to metastatic melanoma. Cancer Res (2014) 74:81-92. doi:10.1158/0008-5472.CAN-13-1303
32. Ali TH, Pisanti S, Ciaglia E, Mortarini R, Anichini A, Garofalo C, et al. Enrichment of CD56(dim)KIR + CD57 + highly cytotoxic NK cells in tumour-infiltrated lymph nodes of melanoma patients. Nat Commun (2014) 5:5639. doi:10.1038/ncomms6639
33. Holtan SG, Creedon DJ, Thompson MA, Nevala WK, Markovic SN. Expansion of CD16-negative natural killer cells in the peripheral blood of patients with metastatic melanoma. Clin Dev Immunol (2011) 2011:316314. doi:10.1155/2011/316314
34. Platonova S, Cherfils-Vicini J, Damotte D, Crozet L, Vieillard V, Validire P, et al. Profound coordinate alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer Res (2011) 15:5412-22. doi:10.1158/0008-5472.CAN-10-4179
35. Delahaye NF, Rusakiewicz S, Martins I, Ménard C, Roux S, Lyonnet L, et al. Alternatively spliced NKp30 isoforms affect the prognosis of gastrointestinal stromal tumors. Nat Med (2011) 17:700-7. doi:10.1038/nm.2366
36. Costello RT, Sivori S, Marcenaro E, Lafage-Pochitaloff M, Mozziconacci MJ, Reviron D, et al. Defective expression and function of natural killer cell-triggering receptors in patients with acute myeloid leukemia. Blood (2002) 99:3661-7. doi:10.1182/blood.V99.10.3661
37. Stringaris K, Sekine T, Khoder A, Alsuliman A, Razzaghi B, Sargeant R, et al. Leukemia-induced phenotypic and functional defects in natural killer cells predict failure to achieve remission in acute myeloid leukemia. Haematologica (2014) 99:836-47. doi:10.3324/haematol.2013.087536
38. Stabile H, Nisti P, Morrone S, Pagliara D, Bertaina A, Locatelli F, et al. Multifunctional human CD56 low CD16 low natural killer cells are the prominent subset in bone marrow of both healthy pediatric donors and leukemic patients. Haematologica (2015) 100:489-98. doi:10.3324/haematol.2014.116053
39. Epling-Burnette PK, Bai F, Painter JS, Rollison DE, Salih HR, Krusch M, et al. Reduced natural killer (NK) function associated with high-risk myelodysplastic syndrome (MDS) and reduced expression of activating NK receptors. Blood (2007) 109:4816-24. doi:10.1182/blood-2006-07-035519
40. Konjevic G, Vuletic A, Mirjacic MK, Colovic N, Colovic M, Jurisic V. Decreased CD161 activating and increased CD158a inhibitory receptor expression on NK cells underlies impaired NK cell cytotoxicity in patients with multiple myeloma. J Clin Pathol (2016) 69:1009-16. doi:10.1136/jclinpath-2016-203614
41. Costello RT, Boehrer A, Sanchez C, Mercier D, Baier C, Le TT, et al. Differential expression of natural killer cell activating receptors in blood versus bone marrow in patients with monoclonal gammopathy. Immunology (2013) 139:338-41. doi:10.1111/imm.12082
42. Chretien AS, Granjeaud S, Gondois-Rey F, Harbi S, Orlanducci F, Blaise D, et al. Increased NK cell maturation in patients with acute myeloid leukemia. Front Immunol (2015) 6:564. doi:10.3389/fimmu.2015.00564
43. Aggarwal N, Swerdlow SH, TenEyck SP, Boyiadzis M, Felgar RE. Natural killer cell (NK) subsets and NK-like T-cell populations in acute myeloid leukemias and myelodysplastic syndromes. Cytometry B Clin Cytom (2016) 90:349-57. doi:10.1002/cyto.b.21349
44. Geyh S, Oz S, Cadeddu RP, Frobel J, Bruckner B, Kundgen A, et al. Insufficient stromal support in MDS results from molecular and functional deficits of mesenchymal stromal cells. Leukemia (2013) 27:1841-51. doi:10.1038/leu.2013.193
45. Carrega P, Morandi B, Costa R, Frumento G, Forte G, Altavilla G, et al. Natural killer cells infiltrating human nonsmall-cell lung cancer are enriched in CD56 bright CD16(-) cells and display an impaired capability to kill tumor cells. Cancer (2008) 112:863-75. doi:10.1002/cncr.23239
46. Mamessier E, Pradel LC, Thibult ML, Drevet C, Zouine A, Jacquemier J, et al. Peripheral blood NK cells from breast cancer patients are tumor-induced composite subsets. J Immunol (2013) 190:2424-36. doi:10.4049/jimmunol.1200140
47. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, et al. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med (2006) 12:1065-74. doi:10.1038/nm1452
48. Carlino C, Stabile H, Morrone S, Bulla R, Soriani A, Agostinis C, et al. Recruitment of circulating NK cells through decidual tissues: a possible mechanism controlling NK cell accumulation in the uterus during early pregnancy. Blood (2008) 111:3108-15. doi:10.1182/blood-2007-08-105965
49. Carlino C, Trotta E, Stabile H, Morrone S, Bulla R, Soriani A, et al. Chemerin regulates NK cell accumulation and endothelial cell morphogenesis in the decidua during early pregnancy. J Clin Endocrinol Metab (2012) 97:3603-12. doi:10.1210/jc.2012-1102
50. Sivori S, Pende D, Bottino C, Marcenaro E, Pessino A, Biassoni R, et al. NKp46 is the major triggering receptor involved in the natural cytotoxicity of fresh or cultured human NK cells. Correlation between surface density of NKp46 and natural cytotoxicity against autologous, allogeneic or xenogeneic target cells. Eur J Immunol (1999) 29:1656-66. doi:10.1002/(SICI)1521-4141(199905)29:05<1656::AID-IMMU1656>3.0.CO;2-1
51. Rouce RH, Shaim H, Sekine T, Weber G, Ballard B, Ku S, et al. The TGF-beta/SMAD pathway is an important mechanism for NK cell immune evasion in childhood B-acute lymphoblastic leukemia. Leukemia (2016) 30:800-11. doi:10.1038/leu.2015.327
52. Sanchez-Correa B, Gayoso I, Bergua JM, Casado JG, Morgado S, Solana R, et al. Decreased expression of DNAM-1 on NK cells from acute myeloid leukemia patients. Immunol Cell Biol (2012) 90:109-15. doi:10.1038/icb.2011.15
53. El-Sherbiny YM, Meade JL, Holmes TD, McGonagle D, Mackie SL, Morgan AW, et al. The requirement for DNAM-1, NKG2D, and NKp46 in the natural killer cell-mediated killing of myeloma cells. Cancer Res (2007) 67:8444-9. doi:10.1158/0008-5472.CAN-06-4230
54. Fauriat C, Mallet F, Olive D, Costello RT. Impaired activating receptor expression pattern in natural killer cells from patients with multiple myeloma. Leukemia (2006) 20:732-3. doi:10.1038/sj.leu.2404096
55. Chen CI, Koschmieder S, Kerstiens L, Schemionek M, Altvater B, Pscherer S, et al. NK cells are dysfunctional in human chronic myelogenous leukemia before and on imatinib treatment and in BCR-ABL-positive mice. Leukemia (2012) 26:465-74. doi:10.1038/leu.2011.239
56. Hejazi M, Manser AR, Frobel J, Kundgen A, Zhao X, Schonberg K, et al. Impaired cytotoxicity associated with defective natural killer cell differentiation in myelodysplastic syndromes. Haematologica (2015) 100:643-52. doi:10.3324/haematol.2014.118679
57. Szczepanski MJ, Szajnik M, Welsh A, Whiteside TL, Boyiadzis M. Blast-derived microvesicles in sera from patients with acute myeloid leukemia suppress natural killer cell function via membrane-associated transforming growth factor-beta1. Haematologica (2011) 96:1302-9. doi:10.3324/haematol.2010.039743
58. Smyth MJ, Teng MW, Swann J, Kyparissoudis K, Godfrey DI, Hayakawa Y. CD4+CD25+ T regulatory cells suppress NK cell-mediated immunotherapy of cancer. J Immunol (2006) 176:1582-7. doi:10.4049/jimmunol.176.3.1582
59. Shenghui Z, Yixiang H, Jianbo W, Kang Y, Laixi B, Yan Z, et al. Elevated frequencies of CD4(+) CD25(+) CD127lo regulatory T cells is associated to poor prognosis in patients with acute myeloid leukemia. Int J Cancer (2011) 129:1373-81. doi:10.1002/ijc.25791
60. Mamessier E, Sylvain A, Thibult ML, Houvenaeghel G, Jacquemier J, Castellano R, et al. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J Clin Invest (2011) 121:3609-22. doi:10.1172/JCI45816
61. Allan DS, Rybalov B, Awong G, Zuniga-Pflucker JC, Kopcow HD, Carlyle JR, et al. TGF-beta affects development and differentiation of human natural killer cell subsets. Eur J Immunol (2010) 40:2289-95. doi:10.1002/eji.200939910
62. Keskin DB, Allan DS, Rybalov B, Andzelm MM, Stern JN, Kopcow HD, et al. TGFbeta promotes conversion of CD16+ peripheral blood NK cells into. Proc Natl Acad Sci U S A (2007) 104:3378-83. doi:10.1073/pnas.0611098104
63. Diaz-Blanco E, Bruns I, Neumann F, Fischer JC, Graef T, Rosskopf M, et al. Molecular signature of CD34(+) hematopoietic stem and progenitor cells of patients with CML in chronic phase. Leukemia (2007) 21:494-504. doi:10.1038/sj.leu.2404549
64. Bruns I, Cadeddu RP, Brueckmann I, Frobel J, Geyh S, Bust S, et al. Multiple myeloma-related deregulation of bone marrow-derived CD34(+) hematopoietic stem and progenitor cells. Blood (2012) 120:2620-30. doi:10.1182/blood-2011-04-347484
65. Castriconi R, Dondero A, Bellora F, Moretta L, Castellano A, Locatelli F, et al. Neuroblastoma-derived TGF-beta1 modulates the chemokine receptor repertoire of human resting NK cells. J Immunol (2013) 190:5321-8. doi:10.4049/jimmunol.1202693
66. Halama N, Michel S, Kloor M, Zoernig I, Benner A, Spille A, et al. Localization and density of immune cells in the invasive margin of human colorectal cancer liver metastases are prognostic for response to chemotherapy. Cancer Res (2011) 71:5670-7. doi:10.1158/0008-5472.CAN-11-0268
67. Baragano RA, Suarez-Alvarez B, Lopez-Larrea C. Secretory pathways generating immunosuppressive NKG2D ligands: new targets for therapeutic intervention. Oncoimmunology (2014) 3:e28497. doi:10.4161/onci.28497
68. Zingoni A, Cecere F, Vulpis E, Fionda C, Molfetta R, Soriani A, et al. Genotoxic stress induces senescence-associated ADAM10-dependent release of NKG2D MIC ligands in multiple myeloma cells. J Immunol (2015) 195:736-48. doi:10.4049/jimmunol.1402643
69. Fionda C, Soriani A, Zingoni A, Santoni A, Cippitelli M. NKG2D and DNAM-1 ligands: molecular targets for NK cell-mediated immunotherapeutic intervention in multiple myeloma. Biomed Res Int (2015) 2015:178698. doi:10.1155/2015/178698
70. Hilpert J, Grosse-Hovest L, Grunebach F, Buechele C, Nuebling T, Raum T, et al. Comprehensive analysis of NKG2D ligand expression and release in leukemia: implications for NKG2D-mediated NK cell responses. J Immunol (2012) 189:1360-71. doi:10.4049/jimmunol.1200796
71. Paschen A, Baingo J, Schadendorf D. Expression of stress ligands of the immunoreceptor NKG2D in melanoma: regulation and clinical significance. Eur J Cell Biol (2014) 93:49-54. doi:10.1016/j.ejcb.2014.01.009
72. Molfetta R, Quatrini L, Zitti B, Capuano C, Galandrini R, Santoni A, et al. Regulation of NKG2D expression and signaling by endocytosis. Trends Immunol (2016) 37:790-802. doi:10.1016/j.it.2016.08.015
73. Varbanova V, Naumova E, Mihaylova A. Killer-cell immunoglobulin-like receptor genes and ligands and their role in hematologic malignancies. Cancer Immunol Immunother (2016) 65:427-40. doi:10.1007/s00262-016-1806-9
74. Sanchez-Correa B, Morgado S, Gayoso I, Bergua JM, Casado JG, Arcos MJ, et al. Human NK cells in acute myeloid leukaemia patients: analysis of NK cell-activating receptors and their ligands. Cancer Immunol Immunother (2011) 60:1195-205. doi:10.1007/s00262-011-1050-2
75. Verheyden S, Demanet C. Susceptibility to myeloid and lymphoid leukemia is mediated by distinct inhibitory KIR-HLA ligand interactions. Leukemia (2006) 20:1437-8. doi:10.1038/sj.leu.2404279
76. Schutt P, Schutt B, Switala M, Bauer S, Stamatis G, Opalka B, et al. Prognostic relevance of soluble human leukocyte antigen-G and total human leukocyte antigen class I molecules in lung cancer patients. Hum Immunol (2010) 71:489-95. doi:10.1016/j.humimm.2010.02.015
77. Yie SM, Hu Z. Human leukocyte antigen-G (HLA-G) as a marker for diagnosis, prognosis and tumor immune escape in human malignancies. Histol Histopathol (2011) 26:409-20. doi:10.14670/HH-26.409
78. Maki G, Hayes GM, Naji A, Tyler T, Carosella ED, Rouas-Freiss N, et al. NK resistance of tumor cells from multiple myeloma and chronic lymphocytic leukemia patients: implication of HLA-G. Leukemia (2008) 22:998-1006. doi:10.1038/leu.2008.15
79. McWilliams EM, Mele JM, Cheney C, Timmerman EA, Fiazuddin F, Strattan EJ, et al. Therapeutic CD94/NKG2A blockade improves natural killer cell dysfunction in chronic lymphocytic leukemia. Oncoimmunology (2016) 5:e1226720. doi:10.1080/2162402X.2016.1226720
80. Kearl TJ, Jing W, Gershan JA, Johnson BD. Programmed death receptor-1/programmed death receptor ligand-1 blockade after transient lymphodepletion to treat myeloma. J Immunol (2013) 190:5620-8. doi:10.4049/jimmunol.1202005
81. Hino R, Kabashima K, Kato Y, Yagi H, Nakamura M, Honjo T, et al. Tumor cell expression of programmed cell death-1 ligand 1 is a prognostic factor for malignant melanoma. Cancer (2010) 116:1757-66. doi:10.1002/cncr.24899