Highly effective NK cells are associated with good prognosis in patients with metastatic prostate cancer

Oncotarget

Volumn 6, Issue 16, 2015, Pages 14360-14373

  Pasero, Christine ^a,c   Gravis, Gwenaëlle ^c   Granjeaud, Samuel ^a,c   Guerin, Mathilde ^a,c   Thomassin Piana, Jeanne ^c   Rocchi, Palma ^a,c   Salem, Naji ^c   Walz, Jochen ^c   Moretta, Alessandro ^d   Olive, Daniel ^a,b,c  

^a AIX MARSEILLE UNIVERSITY   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c INSTITUT PAOLI CALMETTES   (France)

^d UNIVERSITY OF GENOA   (Italy)

Author keywords

Castration resistance; Metastases; Natural killer cells; Prostate cancer; Survival

Indexed keywords

CYTOKINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; LIGAND; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; NATURAL KILLER CELL RECEPTOR NKG2D; PROSTATE SPECIFIC ANTIGEN;

ADULT; AGED; ANDROGEN DEPRIVATION THERAPY; ARTICLE; BLOOD; CANCER IMMUNOTHERAPY; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CASTRATION RESISTANT PROSTATE CANCER; CLINICAL ARTICLE; CLINICAL FEATURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; FLOW CYTOMETRY; HUMAN; LYMPH NODE METASTASIS; MALE; METASTASIS; NATURAL KILLER CELL; OVERALL SURVIVAL; PROSTATE CANCER; PROSTATE HYPERTROPHY; PROSTATE TUMOR; RETROSPECTIVE STUDY; VERY ELDERLY; COHORT ANALYSIS; IMMUNOLOGY; METABOLISM; PATHOLOGY; PROGNOSIS; SURVIVAL ANALYSIS; TUMOR CELL LINE;

CELL LINE, TUMOR; COHORT STUDIES; HUMANS; KILLER CELLS, NATURAL; MALE; NEOPLASM METASTASIS; PROGNOSIS; PROSTATIC NEOPLASMS; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; RETROSPECTIVE STUDIES; SURVIVAL ANALYSIS;

EID: 84931093921     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3965     Document Type: Article

References (55)

1. Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H, Forman D and Bray F. Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer. 2013; 49:1374-1403.
2. MacVicar GR and Hussain MH. Emerging therapies in metastatic castration-sensitive and castration-resistant prostate cancer. Curr Opin Oncol. 2013; 25:252-260.
3. Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, Redfern CH, Ferrari AC, Dreicer R, Sims RB, Xu Y, Frohlich MW and Schellhammer PF. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med. 2010; 363:411-422.
4. Drake CG. Prostate cancer as a model for tumour immunotherapy. Nat Rev Immunol. 2010; 10:580-593.
5. Higano CS, Corman JM, Smith DC, Centeno AS, Steidle CP, Gittleman M, Simons JW, Sacks N, Aimi J and Small EJ. Phase 1/2 dose-escalation study of a GM-CSF-secreting, allogeneic, cellular immunotherapy for metastatic hormonerefractory prostate cancer. Cancer. 2008; 113:975-984.
6. Madan RA, Mohebtash M, Arlen PM, Vergati M, Rauckhorst M, Steinberg SM, Tsang KY, Poole DJ, Parnes HL, Wright JJ, Dahut WL, Schlom J and Gulley JL. Ipilimumab and a poxviral vaccine targeting prostatespecific antigen in metastatic castration-resistant prostate cancer: a phase 1 dose-escalation trial. Lancet Oncol. 2012; 13:501-508.
7. Slovin SF, Higano CS, Hamid O, Tejwani S, Harzstark A, Alumkal JJ, Scher HI, Chin K, Gagnier P, McHenry MB and Beer TM. Ipilimumab alone or in combination with radiotherapy in metastatic castration-resistant prostate cancer: results from an open-label, multicenter phase I/II study. Ann Oncol. 2013; 24:1813-1821.
8. Ryan CJ, Elkin EP, Small EJ, Duchane J and Carroll P. Reduced incidence of bony metastasis at initial prostate cancer diagnosis: data from CaPSURE. Urol Oncol. 2006; 24:396-402.
9. Tangen CM, Hussain MH, Higano CS, Eisenberger MA, Small EJ, Wilding G, Donnelly BJ, Schelhammer PF, Crawford ED, Vogelzang NJ, Powell IJ and Thompson IM, Jr. Improved overall survival trends of men with newly diagnosed M1 prostate cancer: a SWOG phase III trial experience (S8494, S8894 and S9346). J Urol. 2012; 188:1164-1169.
10. Glass TR, Tangen CM, Crawford ED and Thompson I. Metastatic carcinoma of the prostate: identifying prognostic groups using recursive partitioning. J Urol. 2003; 169:164-169.
11. Vivier E, Tomasello E, Baratin M, Walzer T and Ugolini S. Functions of natural killer cells. Nat Immunol. 2008; 9:503-510.
12. Hanna J, Bechtel P, Zhai Y, Youssef F, McLachlan K and Mandelboim O. Novel insights on human NK cells' immunological modalities revealed by gene expression profiling. J Immunol. 2004; 173:6547-6563.
13. Moretta A, Bottino C, Vitale M, Pende D, Biassoni R, Mingari MC and Moretta L. Receptors for HLA class-I molecules in human natural killer cells. Annu Rev Immunol. 1996; 14:619-648.
14. Moretta A, Sivori S, Vitale M, Pende D, Morelli L, Augugliaro R, Bottino C and Moretta L. Existence of both inhibitory (p58) and activatory (p50) receptors for HLA-C molecules in human natural killer cells. J Exp Med. 1995; 182:875-884.
15. Long EO. Regulation of immune responses through inhibitory receptors. Annu Rev Immunol. 1999; 17:875-904.
16. Lopez-Botet M, Perez-Villar JJ, Carretero M, Rodriguez A, Melero I, Bellon T, Llano M and Navarro F. Structure and function of the CD94 C-type lectin receptor complex involved in recognition of HLA class I molecules. Immunol Rev. 1997; 155:165-174.
17. Lanier LL. NK cell recognition. Annu Rev Immunol. 2005; 23:225-274.
18. Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, Biassoni R and Moretta L. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol. 2001; 19:197-223.
19. Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL and Spies T. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science. 1999; 285:727-729.
20. Bryceson YT, March ME, Barber DF, Ljunggren HG and Long EO. Cytolytic granule polarization and degranulation controlled by different receptors in resting NK cells. J Exp Med. 2005; 202:1001-1012.
21. Imai K, Matsuyama S, Miyake S, Suga K and Nakachi K. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet. 2000; 356:1795-1799.
22. Fauriat C, Just-Landi S, Mallet F, Arnoulet C, Sainty D, Olive D and Costello RT. Deficient expression of NCR in NK cells from acute myeloid leukemia: Evolution during leukemia treatment and impact of leukemia cells in NCRdull phenotype induction. Blood. 2007; 109:323-330.
23. Costello RT, Knoblauch B, Sanchez C, Mercier D, Le Treut T and Sebahoun G. Expression of natural killer cell activating receptors in patients with chronic lymphocytic leukaemia. Immunology. 2012; 135:151-157.
24. Pietra G, Manzini C, Rivara S, Vitale M, Cantoni C, Petretto A, Balsamo M, Conte R, Benelli R, Minghelli S, Solari N, Gualco M, Queirolo P, Moretta L and Mingari MC. Melanoma cells inhibit natural killer cell function by modulating the expression of activating receptors and cytolytic activity. Cancer Res. 2012; 72:1407-1415.
25. Fregni G, Perier A, Pittari G, Jacobelli S, Sastre X, Gervois N, Allard M, Bercovici N, Avril MF and Caignard A. Unique functional status of natural killer cells in metastatic stage IV melanoma patients and its modulation by chemotherapy. Clin Cancer Res. 2011; 17:2628-2637.
26. Fregni G, Messaoudene M, Fourmentraux-Neves E, Mazouz-Dorval S, Chanal J, Maubec E, Marinho E, Scheer-Senyarich I, Cremer I, Avril MF and Caignard A. Phenotypic and functional characteristics of blood natural killer cells from melanoma patients at different clinical stages. PLoS One. 2013; 8:e76928.
27. Garcia-Iglesias T, Del Toro-Arreola A, Albarran-Somoza B, Del Toro-Arreola S, Sanchez-Hernandez PE, Ramirez- Duenas MG, Balderas-Pena LM, Bravo-Cuellar A, Ortiz- Lazareno PC and Daneri-Navarro A. Low NKp30, NKp46 and NKG2D expression and reduced cytotoxic activity on NK cells in cervical cancer and precursor lesions. BMC Cancer. 2009; 9:186.
28. Mamessier E, Sylvain A, Thibult ML, Houvenaeghel G, Jacquemier J, Castellano R, Goncalves A, Andre P, Romagne F, Thibault G, Viens P, Birnbaum D, Bertucci F, Moretta A and Olive D. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J Clin Invest. 2011; 121:3609-3622.
29. Mamessier E, Sylvain A, Bertucci F, Castellano R, Finetti P, Houvenaeghel G, Charaffe-Jaufret E, Birnbaum D, Moretta A and Olive D. Human breast tumor cells induce self-tolerance mechanisms to avoid NKG2D-mediated and DNAM-mediated NK cell recognition. Cancer Res. 2011; 71:6621-6632.
30. Platonova S, Cherfils-Vicini J, Damotte D, Crozet L, Vieillard V, Validire P, Andre P, Dieu-Nosjean MC, Alifano M, Regnard JF, Fridman WH, Sautes-Fridman C and Cremer I. Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer Res. 2011; 71:5412-5422.
31. Gillard-Bocquet M, Caer C, Cagnard N, Crozet L, Perez M, Fridman WH, Sautes-Fridman C and Cremer I. Lung tumor microenvironment induces specific gene expression signature in intratumoral NK cells. Front Immunol. 2013; 4:19.
32. Carrega P, Morandi B, Costa R, Frumento G, Forte G, Altavilla G, Ratto GB, Mingari MC, Moretta L and Ferlazzo G. 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; 112:863-875.
33. Schleypen JS, Baur N, Kammerer R, Nelson PJ, Rohrmann K, Grone EF, Hohenfellner M, Haferkamp A, Pohla H, Schendel DJ, Falk CS and Noessner E. Cytotoxic markers and frequency predict functional capacity of natural killer cells infiltrating renal cell carcinoma. Clin Cancer Res. 2006; 12:718-725.
34. Rusakiewicz S, Semeraro M, Sarabi M, Desbois M, Locher C, Mendez R, Vimond N, Concha A, Garrido F, Isambert N, Chaigneau L, Le Brun-Ly V, Dubreuil P, Cremer I, Caignard A, Poirier-Colame V, et al. Immune infiltrates are prognostic factors in localized gastrointestinal stromal tumors. Cancer Res. 2013; 73:3499-3510.
35. Delahaye NF, Rusakiewicz S, Martins I, Menard C, Roux S, Lyonnet L, Paul P, Sarabi M, Chaput N, Semeraro M, Minard-Colin V, Poirier-Colame V, Chaba K, Flament C, Baud V, Authier H, et al. Alternatively spliced NKp30 isoforms affect the prognosis of gastrointestinal stromal tumors. Nat Med. 2011; 17:700-707.
36. Arnon TI, Markel G, Bar-Ilan A, Hanna J, Fima E, Benchetrit F, Galili R, Cerwenka A, Benharroch D, Sion- Vardy N, Porgador A and Mandelboim O. Harnessing soluble NK cell killer receptors for the generation of novel cancer immune therapy. PLoS One. 2008; 3:e2150.
37. Gannon PO, Poisson AO, Delvoye N, Lapointe R, Mes- Masson AM and Saad F. Characterization of the intraprostatic immune cell infiltration in androgen-deprived prostate cancer patients. J Immunol Methods. 2009; 348:9-17.
38. 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 and 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.
39. Fiegler N, Textor S, Arnold A, Rolle A, Oehme I, Breuhahn K, Moldenhauer G, Witzens-Harig M and Cerwenka A. Downregulation of the activating NKp30 ligand B7-H6 by HDAC inhibitors impairs tumor cell recognition by NK cells. Blood. 2013; 122:684-693.
40. Sivori S, Falco M, Marcenaro E, Parolini S, Biassoni R, Bottino C, Moretta L and Moretta A. Early expression of triggering receptors and regulatory role of 2B4 in human natural killer cell precursors undergoing in vitro differentiation. Proc Natl Acad Sci U S A. 2002; 99:4526-4531.
41. Hou S, Zheng X, Wei H, Tian Z and Sun R. Recombinant soluble CD226 protein directly inhibits cancer cell proliferation in vitro. Int Immunopharmacol. 2014; 19:119-126.
42. Moretta L, Bottino C, Pende D, Castriconi R, Mingari MC and Moretta A. Surface NK receptors and their ligands on tumor cells. Semin Immunol. 2006; 18:151-158.
43. Lundholm M, Schroder M, Nagaeva O, Baranov V, Widmark A, Mincheva-Nilsson L and Wikstrom P. Prostate tumor-derived exosomes down-regulate NKG2D expression on natural killer cells and CD8+ T cells: mechanism of immune evasion. PLoS One. 2014; 9:e108925.
44. Elboim M, Gazit R, Gur C, Ghadially H, Betser-Cohen G and Mandelboim O. Tumor immunoediting by NKp46. J Immunol. 2010; 184:5637-5644.
45. Carlsten M, Norell H, Bryceson YT, Poschke I, Schedvins K, Ljunggren HG, Kiessling R and Malmberg KJ. Primary human tumor cells expressing CD155 impair tumor targeting by down-regulating DNAM-1 on NK cells. J Immunol. 2009; 183:4921-4930.
46. Castriconi R, Cantoni C, Della Chiesa M, Vitale M, Marcenaro E, Conte R, Biassoni R, Bottino C, Moretta L and 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 U S A. 2003; 100:4120-4125.
47. Lee JC, Lee KM, Kim DW and Heo DS. Elevated TGFbeta1 secretion and down-modulation of NKG2D underlies impaired NK cytotoxicity in cancer patients. J Immunol. 2004; 172:7335-7340.
48. Sharma J, Gray KP, Harshman LC, Evan C, Nakabayashi M, Fichorova R, Rider J, Mucci L, Kantoff PW and Sweeney CJ. Elevated IL-8, TNF-alpha, and MCP-1 in men with metastatic prostate cancer starting androgendeprivation therapy (ADT) are associated with shorter time to castration-resistance and overall survival. Prostate. 2014; 74:820-828.
49. Koo KC, Shim DH, Yang CM, Lee SB, Kim SM, Shin TY, Kim KH, Yoon HG, Rha KH, Lee JM and Hong SJ. Reduction of the CD16(-)CD56bright NK cell subset precedes NK cell dysfunction in prostate cancer. PLoS One. 2013; 8:e78049.
50. Glasner A, Ghadially H, Gur C, Stanietsky N, Tsukerman P, Enk J and Mandelboim O. Recognition and prevention of tumor metastasis by the NK receptor NKp46/NCR1. J Immunol. 2012; 188:2509-2515.
51. Halfteck GG, Elboim M, Gur C, Achdout H, Ghadially H and 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.
52. Gandaglia G, Karakiewicz PI, Briganti A, Passoni NM, Schiffmann J, Trudeau V, Graefen M, Montorsi F and Sun M. Impact of the Site of Metastases on Survival in Patients with Metastatic Prostate Cancer. Eur Urol. 2014.
53. Ost P, Decaestecker K, Lambert B, Fonteyne V, Delrue L, Lumen N, Ameye F and De Meerleer G. Prognostic factors influencing prostate cancer-specific survival in non-castrate patients with metastatic prostate cancer. Prostate. 2014; 74:297-305.
54. McKay K, Moore PC, Smoller BR and Hiatt KM. Association between natural killer cells and regression in melanocytic lesions. Hum Pathol. 2011; 42:1960-1964.
55. Mamessier E, Pradel LC, Thibult ML, Drevet C, Zouine A, Jacquemier J, Houvenaeghel G, Bertucci F, Birnbaum D and Olive D. Peripheral blood NK cells from breast cancer patients are tumor-induced composite subsets. J Immunol. 2013; 190:2424-2436.