Natural killer cells and solid tumors

Journal of Innate Immunity

Volumn 3, Issue 4, 2011, Pages 355-364

  Stojanovic, Ana ^a   Cerwenka, Adelheid ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Natural killer cells; Tumor immunology; Tumor microenvironment

Indexed keywords

CD56 ANTIGEN; CD57 ANTIGEN; CELL SURFACE MARKER; GAMMA INTERFERON; INTERLEUKIN 2; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL KILLER CELL RECEPTOR NKG2D; TRANSFORMING GROWTH FACTOR BETA;

CELL FUNCTION; CELL INFILTRATION; CELL INTERACTION; CELL SECRETION; CELLULAR DISTRIBUTION; HUMAN; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SOLID TUMOR; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT;

EID: 85027919769     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000325465     Document Type: Review

References (84)

1. Deschoolmeester V, Baay M, Van Marck E, Weyler J, Vermeulen P, Lardon F, Vermorken JB: Tumor infiltrating lymphocytes: an intriguing player in the survival of colorectal ca ncer patients. BMC Immunol 2010; 11: 19.
2. Coca S, Perez-Piqueras J, Martinez D, Colmenarejo A, Saez MA, Vallejo C, Martos JA, Moreno M: The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma. Cancer 1997; 79: 2320-2328.
3. Kiessling R, Klein E, Pross H, Wigzell H: 'Natural' killer cells in the mouse. II. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Characteristics of the killer cell. Eur J Immunol 1975; 5:117-121.
4. Kiessling R, Klein E, Wigzell H: 'Natural' killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur J Immunol 1975; 5:112-117.
5. Bryceson YT, March ME, Ljunggren HG, Long EO: Activation, coactivation, and co-stimulation of resting human natural killer cells. Immunol Rev 2006; 214:73-91. (Pubitemid 44707903)
6. Lucas M, Schachterle W, Oberle K, Aichele P, Diefenbach A: Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 2007; 26: 503-517.
7. Ljunggren HG, Malmberg KJ: Prospects for the use of NK cells in immunotherapy of human cancer. Nat Rev Immunol 2007; 7:329-339.
8. Chan CJ, Andrews DM, Smyth MJ: Can NK cells be a therapeutic target in human cancer? Eur J Immunol 2008; 38:2964-2968.
9. Imai K, Matsuyama S, Miyake S, Suga K, Nakachi K: Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general popu lation. Lancet 2000; 356: 1795-1799.
10. Guerra N, Tan YX, Joncker NT, Choy A, Gallardo F, Xiong N, Knoblaugh S, Cado D, Greenberg NM, Raulet DH: NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 2008; 28:571-580.
11. Halfteck GG, Elboim M, Gur C, Achdout H, Ghadially H, Mandelboim O: Enhanced in vivo growth of lymphoma tumors in the absence of the NK-activating receptor NKp46/NCR1. J Immunol 2009; 182: 2221-2230.
12. Elboim M, Gazit R, Gur C, Ghadially H, Betser-Cohen G, Mandelboim O: Tumor immunoediting by NKp46. J Immunol; 184: 5637-5644.
13. Walzer T, Blery M, Chaix J, Fuseri N, Chasson L, Robbins SH, Jaeger S, Andre P, Gauthier L, Daniel L, Chemin K, Morel Y, Dalod M, Imbert J, Pierres M, Moretta A, Romagne F, Vivier E: Identification, activation, and selective in vivo ablation of mouse NK cells via NKp46. Proc Natl Acad Sci USA 2007; 104: 3384-3389.
14. Eckelhart E, Warsch W, Zebedin E, Simma O, Stoiber D, Kolbe T, Rulicke T, Mueller M, Casanova E, Sexl V: A novel Ncr1-Cre mouse reveals the essential role of STAT5 for NK cell survival and development. Blood 2010; 117:1565-1573.
15. Eisenring M, vom Berg J, Kristiansen G, Saller E, Becher B: IL-12 initiates tumor rejection via lymphoid tissue-inducer cells bearing the natural cytotoxicity receptor NKp46. Nat Immunol 2010; 11:1030-1038.
16. Colonna M: Interleukin-22-producing natural killer cells and lymphoid tissue inducerlike cells in mucosal immunity. Immunity 2009; 31: 15-23.
17. Ljunggren HG, Karre K: Host resistance directed selectively against H-2-deficient lymphoma variants. Analysis of the mechanism. J Exp Med 1985; 162:1745-1759.
18. Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, Posati S, Rogaia D, Frassoni F, Aversa F, Martelli MF, Velardi A: Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 2002; 295:2097-2100.
19. Moretta L, Locatelli F, Pende D, Mingari MC, Moretta A: Natural killer alloeffector responses in haploidentical hemopoietic stem cell transplantation to treat high-risk leukemias. Tissue Antigens 2010; 75: 103 - 109.
20. Terme M, Ullrich E, Delahaye NF, Chaput N, Zitvogel L: Natural killer cell-directed therapies: moving from unexpected results to successful strategies. Nat Immunol 2008; 9: 486-494.
21. Qin Z, Blankenstein T: CD4+ T cell - mediated tumor rejection involves inhibition of angiogenesis that is dependent on IFN gamma receptor expression by nonhematopoietic cells. Immunity 2000; 12:677-686.
22. Rabinovich BA, Li J, Shannon J, Hurren R, Chalupny J, Cosman D, Miller RG: Activated, but not resting, T cells can be recognized and killed by syngeneic NK cells. J Immunol 2003; 170: 3572-3576.
23. Ishigami S, Natsugoe S, Tokuda K, Nakajo A, Che X, Iwashige H, Aridome K, Hokita S, Aikou T: Prognostic value of intratumoral natural killer cells in gastric carcinoma. Cancer 2000; 88:577-583.
24. Villegas FR, Coca S, Villarrubia VG, Jimenez R, Chillon MJ, Jareno J, Zuil M, Callol L: Prognostic significance of tumor infiltrating natural killer cells subset CD57 in patients with squamous cell lung cancer. Lung Cancer 2002; 35: 23-28.
25. Bjorkstrom NK, Riese P, Heuts F, Andersson S, Fauriat C, Ivarsson MA, Bjorklund AT, Flodstrom-Tullberg M, Michaelsson J, Rottenberg ME, Guzman CA, Ljunggren HG, Malmberg KJ: Expression patterns of NK-G2A, KIR, and CD57 define a process of CD-56dim NK cell differentiation uncoupled from NK cell education. Blood 2010; 116: 3853-3864.
26. 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.
27. Textor S, Durst M, Jansen L, Accardi R, Tommasino M, Trunk MJ, Porgador A, Watzl C, Gissmann L, Cerwenka A: Activating NK cell receptor ligands are differentially expressed during progression to cervical cancer. Int J Cancer 2008; 123: 2343-2353.
28. Schleypen JS, Baur N, Kammerer R, Nelson PJ, Rohrmann K, Grone EF, Hohenfellner M, Haferkamp A, Pohla H, Schendel DJ, Falk CS, Noessner E: Cytotoxic markers and frequency predict functional capacity of natural killer cells infiltrating renal cell carcinoma. Clin Ca ncer Res 2006; 12: 718-725.
29. Harlin H, Hanson M, Johansson CC, Sakurai D, Poschke I, Norell H, Malmberg KJ, Kiessling R: The CD16-CD56(bright) NK cell subset is resistant to reactive oxygen species produced by activated granulocytes and has higher antioxidative capacity than the CD16+ CD56(dim) subset. J Immunol 2007; 179:4513-4519.
30. Esendagli G, Bruderek K, Goldmann T, Busche A, Branscheid D, Vollmer E, Brandau S: Malignant and non-malignant lung tissue areas are differentially populated by natural killer cells and regulatory T cells in non-small cell lung cancer. Lung Cancer 2008; 59: 32-40.
31. Sandel MH, Speetjens FM, Menon AG, Albertsson PA, Basse PH, Hokland M, Nagelkerke JF, Tollenaar RA, van de Velde CJ, Kuppen PJ: Natural killer cells infiltrating colorectal cancer and MHC class I expression. Mol Immunol 2005; 42:541-546.
32. Albertsson PA, Basse PH, Hokland M, Goldfarb RH, Nagelkerke JF, Nannmark U, Kuppen PJ: NK cells and the tumour microenvi-ronment: implications for NK-cell function and anti-tumour activity. Trends Immunol 2003; 24:603-609.
33. Gregoire C, Chasson L, Luci C, Tomasello E, Geissmann F, Vivier E, Walzer T: The trafficking of natural killer cells. Immunol Rev 2007; 220: 169-182.
34. Wendel M, Galani IE, Suri-Payer E, Cerwenka A: Natural killer cell accumulation in tumors is dependent on IFN-gamma and CXCR3 ligands. Cancer Res 2008; 68:8437-8445.
35. Hayakawa Y, Smyth MJ: Cd27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J Immunol 2006; 176:1517-1524.
36. Fauriat C, Long EO, Ljunggren HG, Bryceson YT: Regulation of human NK-cell cy-tokine and chemokine production by target cell recognition. Blood; 115: 2167-2176.
37. Glas R, Franksson L, Une C, Eloranta ML, Ohlen C, Orn A, Karre K: Recruitment and activation of natural killer (NK) cells in vivo determined by the target cell phenotype. an adaptive component of NK cell-mediated responses. J Exp Med 2000; 191:129-138.
38. Diefenbach A, Jensen ER, Jamieson AM, Raulet DH: Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 2001; 413: 165-171.
39. Menon AG, Morreau H, Tollenaar RA, Alphenaar E, Van Puijenbroek M, Putter H, Janssen-Van Rhijn CM, Van De Velde CJ, Fleuren GJ, Kuppen PJ: Down-regulation of HLA-A expression correlates with a better prognosis in colorectal cancer patients. Lab Invest 2002; 82: 1725-1733.
40. Frey AB, Monu N: Signaling defects in antitumor T cells. Immunol Rev 2008; 222: 192-205.
41. Konjevic G, Jurisic V, Spuzic I: Association of NK cell dysfunction with changes in LDH characteristics of peripheral blood lymphocytes (PBL) in breast cancer patients. Breast Cancer Res Treat 2001; 66:255-263.
42. Hersey P, Edwards A, McCarthy WH: Tumour-related changes in natural killer cell activity in melanoma patients. Influence of stage of disease, tumour thickness and age of patients. Int J Cancer 1980; 25: 187-194.
43. Sibbitt WL Jr, Bankhurst AD, Jumonville AJ, Saiki JH, Saiers JH, Doberneck RC: Defects in natural killer cell activity and interferon response in human lung carcinoma and malignant melanoma. Ca ncer Res 1984; 44: 852-856. (Pubitemid 14184630)
44. Taketomi A, Shimada M, Shirabe K, Kajiyama K, Gion T, Sugimachi K: Natural killer cell activity in patients with hepatocellular carcinoma: a new prognostic indicator after hepatectomy. Cancer 1998; 83: 58-63.
45. Pierson BA, Miller JS: CD56+bright and CD56+dim natural killer cells in patients with chronic myelogenous leukemia progressively decrease in number, respond less to stimuli that recruit clonogenic natural killer cells, and exhibit decreased proliferation on a per cell basis. Blood 1996; 88:2279-2287.
46. Tajima F, Kawatani T, Endo A, Kawasaki H: Natural killer cell activity and cytokine production as prognostic factors in adult acute leukemia. Leukemia 1996; 10: 478 - 482.
47. Costello RT, Sivori S, Marcenaro E, Lafage-Pochitaloff M, Mozziconacci MJ, Reviron D, Gastaut JA, Pende D, Olive D, Moretta A: Defective expression and function of natural killer cell-triggering receptors in patients with acute myeloid leukemia. Blood 2002; 99: 3661-3667.
48. Vaquer S, Jorda J, Lopez de la Osa E, Alvarez de los Heros J, Lopez-Garcia N, Alvarez de Mon M: Clinical implications of natural killer (NK) cytotoxicity in patients with squamous cell carcinoma of the uterine cervix. Gynecol Oncol 1990; 36:90-92.
49. Richards JO, Chang X, Blaser BW, Caligiuri MA, Zheng P, Liu Y: Tumor growth impedes natural-killer-cell maturation in the bone marrow. Blood 2006; 108: 246-252.
50. Brenner CD, King S, Przewoznik M, Wolters I, Adam C, Bornkamm GW, Busch DH, Rocken M, Mocikat R: Requirements for control of B-cell lymphoma by NK cells. Eur J Immunol 2010; 40: 494-504.
51. Lai P, Rabinowich H, Crowley-Nowick PA, Bell MC, Mantovani G, Whiteside TL: Alterations in expression and function of signal-transducing proteins in tumor-associated t and natural killer cells in patients with ovarian carcinoma. Clin Cancer Res 1996; 2:161-173.
52. Rabinowich H, Suminami Y, Reichert TE, Crowley-Nowick P, Bell M, Edwards R, Whiteside TL: Expression of cytokine genes or proteins and signaling molecules in lymphocytes associated with human ovarian carcinoma. Int J Cancer 1996; 68:276-284.
53. Smyth MJ, Swann J, Kelly JM, Cretney E, Yokoyama WM, Diefenbach A, Sayers TJ, Hayakawa Y: NKG2D recognition and perforin effector function mediate effective cytokine immunotherapy of cancer. J Exp Med 2004; 200: 1325-1335.
54. Nausch N, Cerwenka A: NKG2D ligands in tumor immunity. Oncogene 2008; 27: 5944-5958.
55. Raulet DH, Guerra N: Oncogenic stress sensed by the immune system: role of natural killer cell receptors. Nat Rev Immunol 2009; 9: 568-580.
56. Soriani A, Zingoni A, Cerboni C, Iannitto ML, Ricciardi MR, Di Gialleonardo V, Cippitelli M, Fionda C, Petrucci MT, Guarini A, Foa R, Santoni A: ATM-ATR-dependent up-regulation of DNAM-1 and NKG2D ligands on multiple myeloma cells by therapeutic agents results in enhanced NK-cell susceptibility and is associated with a senescent phenotype. Blood 2009; 113: 3503-3511.
57. Bryceson YT, March ME, Ljunggren HG, Long EO: Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood 2006; 107:159-166.
58. Pogge von Strandmann E, Simhadri VR, von Tresckow B, Sasse S, Reiners KS, Hansen HP, Rothe A, Boll B, Simhadri VL, Borchmann P, McKinnon PJ, Hallek M, Engert A: Human leukocyte antigen-B-associated transcript 3 is released from tumor cells and engages the NKp30 receptor on natural killer cells. Immunity 2007; 27: 965-974.
59. Brandt CS, Baratin M, Yi EC, Kennedy J, Gao Z, Fox B, Haldeman B, Ostrander CD, Kaifu T, Chabannon C, Moretta A, West R, Xu W, Vivier E, Levin SD: The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. J Exp Med 2009; 206:1495-1503.
60. Le Maux Chansac B, Moretta A, Vergnon I, Opolon P, Lecluse Y, Grunenwald D, Kubin M, Soria JC, Chouaib S, Mami-Chouaib F: NK cells infiltrating a MHC class I-deficient lung adenocarcinoma display impaired cytotoxic activity toward autologous tumor cells associated with altered NK cell-triggering receptors. J Immunol 2005; 175: 5790 - 5798.
61. Balsamo M, Scordamaglia F, Pietra G, Manzini C, Cantoni C, Boitano M, Queirolo P, Vermi W, Facchetti F, Moretta A, Moretta L, Mingari MC, Vitale M: Melanoma-associated fibroblasts modulate NK cell phenotype and antitumor cytotoxicity. Proc Natl Acad Sci USA 2009; 106:20847-20852.
62. Coudert JD, Scarpellino L, Gros F, Vivier E, Held W: Sustained NKG2D engagement induces cross-tolerance of multiple distinct NK cell activation pathways. Blood 2008; 111: 3571-3578.
63. Carlsten M, Baumann BC, Simonsson M, Jadersten M, Forsblom AM, Hammarstedt C, Bryceson YT, Ljunggren HG, Hellstrom-indberg E, Malmberg KJ: Reduced DNAM-1 expression on bone marrow NK cells associated with impaired killing of CD34+ blasts in myelodysplastic syndrome. Leukemia 2010; 24:1607-1616.
64. Groh V, Wu J, Yee C, Spies T: Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 2002; 419:734-738.
65. Salih HR, Rammensee HG, Steinle A: Cutting edge: Down-regulation of MICA on human tumors by proteolytic shedding. J Immunol 2002; 169: 4098-4102.
66. Paschen A, Sucker A, Hill B, Moll I, Zapatka M, Nguyen XD, Sim GC, Gutmann I, Hassel J, Becker JC, Steinle A, Schadendorf D, Ugurel S: Differential clinical significance of individual NKG2D ligands in melanoma: soluble ULBP2 as an indicator of poor prognosis superior to S100B. Clin Cancer Res 2009; 15:5208-5215.
67. Castriconi R, Cantoni C, Della Chiesa M, Vitale M, Marcenaro E, Conte R, Biassoni R, Bottino C, Moretta L, Moretta A: Transforming growth factor beta 1 inhibits expression of NKp30 and NKG2D receptors: consequences for the NK-mediated killing of dendritic cells. Proc Natl Acad Sci USA 2003; 100:4120-4125.
68. Della Chiesa M, Carlomagno S, Frumento G, Balsamo M, Cantoni C, Conte R, Moretta L, Moretta A, Vitale M: The tryptophan catabolite L-kynurenine inhibits the surface expression of nkp46- and nkg2d-activating receptors and regulates NK-cell function. Blood 2006; 108:4118-4125.
69. Bell D, Chomarat P, Broyles D, Netto G, Harb GM, Lebecque S, Valladeau J, Davoust J, Palucka KA, Banchereau J: In breast carcinoma tissue, immature dendritic cells reside within the tumor, whereas mature dendritic cells are located in peritumoral areas. J Exp Med 1999; 190: 1417-1426.
70. Moretta L, Ferlazzo G, Bottino C, Vitale M, Pende D, Mingari MC, Moretta A: Effector and regulatory events during natural killer-dendritic cell interactions. Immunol Rev 2006; 214:219-228.
71. Solinas G, Germano G, Mantovani A, Allavena P: Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation. J Leukoc Biol 2009; 86:1065-1073.
72. Gabrilovich DI, Nagaraj S: Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009; 9: 162-174.
73. Li H, Han Y, Guo Q, Zhang M, Cao X: Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1. J Immunol 2009; 182: 240-249.
74. Nausch N, Galani IE, Schlecker E, Cerwenka A: Mononuclear myeloid-derived 'suppressor' cells express RAE-1 and activate natural killer cells. Blood 2008; 112:4080-4089.
75. 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; 176:1582-1587.
76. Ghiringhelli F, Menard C, Terme M, Flament C, Taieb J, Chaput N, Puig PE, Novault S, Escudier B, Vivier E, Lecesne A, Robert C, Blay JY, Bernard J, Caillat-Zucman S, Freitas A, Tursz T, Wagner-Ballon O, Capron C, Vainchencker W, Martin F, Zitvogel L: CD4+CD25+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor-beta-dependent manner. J Exp Med 2005; 202:1075-1085.
77. Loeffler DA, Juneau PL, Heppner GH: Natural killer-cell activity under conditions reflective of tumor micro-environment. Int J Cancer 1991; 48:895-899.
78. Flavell RA, Sanjabi S, Wrzesinski SH, Licona-Limon P: The polarization of immune cells in the tumour environment by TGFbeta. Nat Rev Immunol 2010; 10:554-567.
79. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A: Interleukin-10 and the interleu-kin-10 receptor. Annu Rev Immunol 2001; 19: 683-765.
80. Kundu N, Beaty TL, Jackson MJ, Fulton AM: Antimetastatic and antitumor activities of interleukin 10 in a murine model of breast ca ncer. J Natl Cancer Inst 1996; 88: 536-541.
81. Campoli M, Ferrone S: Tumor escape mechanisms: potential role of soluble HLA antigens and NK cells activating ligands. Tissue Antigens 2008; 72:321-334.
82. Rouas-Freiss N, Moreau P, Menier C, Le-Maoult J, Carosella ED: Expression of tolerogenic HLA-G molecules in cancer prevents antitumor responses. Semin Cancer Biol 2007; 17:413-421.
83. Rajagopalan S, Bryceson YT, Kuppusamy SP, Geraghty DE, van der Meer A, Joosten I, Long EO: Activation of NK cells by an endo-cytosed receptor for soluble HLA-G. PLoS Biol 2006; 4:e9.
84. Favier B, Lemaoult J, Lesport E, Carosella ED: ILT2/HLA-G interaction impairs NK-cell functions through the inhibition of the late but not the early events of the NK-cell activating synapse. FASEB J 2010; 24:689-699.