CD56brightperforinlow noncytotoxic human NK cells are abundant in both healthy and neoplastic solid tissues and recirculate to secondary lymphoid organs via afferent lymph

Journal of Immunology

Volumn 192, Issue 8, 2014, Pages 3805-3815

  Carrega, Paolo ^a   Bonaccorsi, Irene ^b,c   Di Carlo, Emma ^d   Morandi, Barbara ^e   Paul, Petra ^f   Rizzello, Valeria ^b   Cipollone, Giuseppe ^d,g   Navarra, Giuseppe ^b   Mingari, Maria Cristina ^e,h   Moretta, Lorenzo ^a   Ferlazzo, Guido ^b,c  

^a G GASLINI INSTITUTE   (Italy)

^b UNIVERSITY OF MESSINA   (Italy)

^c UNIVERSITY OF MESSINA   (Italy)

^d UNIVERSITY OF CHIETI   (Italy)

^e UNIVERSITY OF GENOA   (Italy)

^f UNIVERSITY OF ZURICH   (Switzerland)

^g Policlinico SS Annunziata   (Italy)

^h UNIVERSITY OF GENOA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGENS, CD56; CELL LINE, TUMOR; CHEMOKINES; CYTOTOXICITY, IMMUNOLOGIC; GENE EXPRESSION PROFILING; HUMANS; KILLER CELLS, NATURAL; LYMPH; LYMPHOCYTES, TUMOR-INFILTRATING; LYMPHOID TISSUE; NEOPLASMS; ORGAN SPECIFICITY; PERFORIN;

EID: 84898619037     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301889     Document Type: Article

References (50)

1. Spits, H., and J. P. Di Santo. 2011. The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling. Nat. Immunol. 12: 21-27.
2. Vivier, E., E. Tomasello, M. Baratin, T. Walzer, and S. Ugolini. 2008. Functions of natural killer cells. Nat. Immunol. 9: 503-510.
3. Moretta, L., G. Ferlazzo, C. Bottino, M. Vitale, D. Pende, M. C. Mingari, and A. Moretta. 2006. Effector and regulatory events during natural killer-dendritic cell interactions. Immunol. Rev. 214: 219-228.
4. Martín-Fontecha, A., L. L. Thomsen, S. Brett, C. Gerard, M. Lipp, A. Lanzavecchia, and F. Sallusto. 2004. Induced recruitment of NK cells to lymph nodes provides IFN-γamma for T(H)1 priming. Nat. Immunol. 5: 1260-1265.
5. Morandi, B., L. Mortara, L. Chiossone, R. S. Accolla, M. C. Mingari, L. Moretta, A. Moretta, and G. Ferlazzo. 2012. Dendritic cell editing by activated natural killer cells results in a more protective cancer-specific immune response. PLoS ONE 7: e39170.
6. Cooper, M. A., T. A. Fehniger, and M. A. Caligiuri. 2001. The biology of human natural killer-cell subsets. Trends Immunol. 22: 633-640.
7. Fauriat, C., E. O. Long, H. G. Ljunggren, and Y. T. Bryceson. 2010. Regulation of human NK-cell cytokine and chemokine production by target cell recognition. Blood 115: 2167-2176.
8. Juelke, K., M. Killig, M. Luetke-Eversloh, E. Parente, J. Gruen, B. Morandi, G. Ferlazzo, A. Thiel, I. Schmitt-Knosalla, and C. Romagnani. 2010. CD62L expression identifies a unique subset of polyfunctional CD56dim NK cells. Blood 116: 1299-1307.
9. Campbell, J. J., S. Qin, D. Unutmaz, D. Soler, K. E. Murphy, M. R. Hodge, L. Wu, and E. C. Butcher. 2001. Unique subpopulations of CD56+ NK and NKT peripheral blood lymphocytes identified by chemokine receptor expression repertoire. J. Immunol. 166: 6477-6482.
10. Grégoire, C., L. Chasson, C. Luci, E. Tomasello, F. Geissmann, E. Vivier, and T. Walzer. 2007. The trafficking of natural killer cells. Immunol. Rev. 220: 169-182.
11. Ferlazzo, G., D. Thomas, S. L. Lin, K. Goodman, B. Morandi, W. A. Muller, A. Moretta, and C. Münz. 2004. The abundant NK cells in human secondary lymphoid tissues require activation to express killer cell Ig-like receptors and become cytolytic. J. Immunol. 172: 1455-1462.
12. Carrega, P., and G. Ferlazzo. 2012. Natural killer cell distribution and trafficking in human tissues. Front. Immunol. 3: 347.
13. Mailliard, R. B., S. M. Alber, H. Shen, S. C. Watkins, J. M. Kirkwood, R. B. Herberman, and P. Kalinski. 2005. IL-18-induced CD83+CCR7+ NK helper cells. J. Exp. Med. 202: 941-953.
14. Parolini, S., A. Santoro, E. Marcenaro, W. Luini, L. Massardi, F. Facchetti, D. Communi, M. Parmentier, A. Majorana, M. Sironi, et al. 2007. The role of chemerin in the colocalization of NK and dendritic cell subsets into inflamed tissues. Blood 109: 3625-3632.
15. Walzer, T., L. Chiossone, J. Chaix, A. Calver, C. Carozzo, L. Garrigue-Antar, Y. Jacques, M. Baratin, E. Tomasello, and E. Vivier. 2007. Natural killer cell trafficking in vivo requires a dedicated sphingosine 1-phosphate receptor. Nat. Immunol. 8: 1337-1344.
16. Shi, F. D., H. G. Ljunggren, A. La Cava, and L. Van Kaer. 2011. Organ-specific features of natural killer cells. Nat. Rev. Immunol. 11: 658-671.
17. Bruno, A., C. Focaccetti, A. Pagani, A. S. Imperatori, M. Spagnoletti, N. Rotolo, A. R. Cantelmo, F. Franzi, C. Capella, G. Ferlazzo, et al. 2013. The proangiogenic phenotype of natural killer cells in patients with non-small cell lung cancer. Neoplasia 15: 133-142.
18. Schleypen, J. S., N. Baur, R. Kammerer, P. J. Nelson, K. Rohrmann, E. F. Gröne, M. Hohenfellner, A. Haferkamp, H. Pohla, D. J. Schendel, et al. 2006. Cytotoxic markers and frequency predict functional capacity of natural killer cells infiltrating renal cell carcinoma. Clin. Cancer Res. 12: 718-725.
19. Dalbeth, N., R. Gundle, R. J. Davies, Y. C. Lee, A. J. McMichael, and M. F. Callan. 2004. CD56bright NK cells are enriched at inflammatory sites and can engage with monocytes in a reciprocal program of activation. J. Immunol. 173: 6418-6426.
20. Faget, J., C. Biota, T. Bachelot, M. Gobert, I. Treilleux, N. Goutagny, I. Durand, S. Léon-Goddard, J. Y. Blay, C. Caux, and C. Ménétrier-Caux. 2011. Early detection of tumor cells by innate immune cells leads to T(reg) recruitment through CCL22 production by tumor cells. Cancer Res. 71: 6143-6152.
21. Spits, H., D. Artis, M. Colonna, A. Diefenbach, J. P. Di Santo, G. Eberl, S. Koyasu, R. M. Locksley, A. N. McKenzie, R. E. Mebius, et al. 2013. Innate lymphoid cells-a proposal for uniform nomenclature. Nat. Rev. Immunol. 13: 145-149.
22. Walker, J. A., J. L. Barlow, and A. N. McKenzie. 2013. Innate lymphoid cells-how did we miss them? Nat. Rev. Immunol. 13: 75-87.
23. Tomasello, E., N. Yessaad, E. Gregoire, K. Hudspeth, C. Luci, D. Mavilio, J. Hardwigsen, and E. Vivier. 2012. Mapping of NKp46(+) Cells in Healthy Human Lymphoid and Non-Lymphoid Tissues. Front. Immunol. 3: 344.
24. Carrega, P., B. Morandi, R. Costa, G. Frumento, G. Forte, G. Altavilla, G. B. Ratto, M. C. Mingari, L. Moretta, and G. Ferlazzo. 2008. 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 112: 863-875.
25. Romagnani, C., K. Juelke, M. Falco, B. Morandi, A. D'Agostino, R. Costa, G. Ratto, G. Forte, P. Carrega, G. Lui, et al. 2007. CD56brightCD16-killer Iglike receptor-NK cells display longer telomeres and acquire features of CD56dim NK cells upon activation. J. Immunol. 178: 4947-4955.
26. Montalto, E., S. Mangraviti, G. Costa, P. Carrega, B. Morandi, G. Pezzino, I. Bonaccorsi, A. Cancellieri, M. C. Mingari, M. Mesiti, et al. 2010. Seroma fluid subsequent to axillary lymph node dissection for breast cancer derives from an accumulation of afferent lymph. Immunol. Lett. 131: 67-72.
27. Morandi, B., I. Bonaccorsi, M. Mesiti, R. Conte, P. Carrega, G. Costa, R. Iemmo, S. Martini, S. Ferrone, C. Cantoni, et al. 2013. Characterization of human afferent lymph dendritic cells from seroma fluids. J. Immunol. 191: 4858-4866.
28. Park, M. H., J. S. Lee, and J. H. Yoon. 2012. High expression of CX3CL1 by tumor cells correlates with a good prognosis and increased tumor-infiltrating CD8+ T cells, natural killer cells, and dendritic cells in breast carcinoma. J. Surg. Oncol. 106: 386-392.
29. Christofori, G. 2003. Changing neighbours, changing behaviour: cell adhesion molecule-mediated signalling during tumour progression. EMBO J. 22: 2318-2323.
30. Cavallaro, U., J. Niedermeyer, M. Fuxa, and G. Christofori. 2001. N-CAM modulates tumour-cell adhesion to matrix by inducing FGF-receptor signalling. Nat. Cell Biol. 3: 650-657.
31. Schardt, C., J. Heymanns, C. Schardt, M. Rotsch, and K. Havemann. 1993. Differential expression of the intercellular adhesion molecule-1 (ICAM-1) in lung cancer cell lines of various histological types. Eur. J. Cancer 29A: 2250-2255.
32. Coradini, D., C. Pellizzaro, S. Veneroni, L. Ventura, and M. G. Daidone. 2002. Infiltrating ductal and lobular breast carcinomas are characterised by different interrelationships among markers related to angiogenesis and hormone dependence. Br. J. Cancer 87: 1105-1111.
33. Hayakawa, Y., and M. J. Smyth. 2006. CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J. Immunol. 176: 1517-1524.
34. Yu, Y. R., A. M. Fong, C. Combadiere, J. L. Gao, P. M. Murphy, and D. D. Patel. 2007. Defective antitumor responses in CX3CR1-deficient mice. Int. J. Cancer 121: 316-322.
35. Lund, H., P. Boysen, J. C. Hope, S. K. Sjurseth, and A. K. Storset. 2013. Natural Killer Cells in Afferent Lymph Express an Activated Phenotype and Readily Produce IFN-γ. Front. Immunol. 4: 395.
36. Ferlazzo, G., M. Pack, D. Thomas, C. Paludan, D. Schmid, T. Strowig, G. Bougras, W. A. Muller, L. Moretta, and C. Münz. 2004. Distinct roles of IL-12 and IL-15 in human natural killer cell activation by dendritic cells from secondary lymphoid organs. Proc. Natl. Acad. Sci. USA 101: 16606-16611.
37. Vossen, M. T., M. Matmati, K. M. Hertoghs, P. A. Baars, M. R. Gent, G. Leclercq, J. Hamann, T. W. Kuijpers, and R. A. van Lier. 2008. CD27 defines phenotypically and functionally different human NK cell subsets. J. Immunol. 180: 3739-3745.
38. Ferlazzo, G., and C. Münz. 2009. Dendritic cell interactions with NK cells from different tissues. J. Clin. Immunol. 29: 265-273.
39. Mamessier, E., A. Sylvain, M. L. Thibult, G. Houvenaeghel, J. Jacquemier, R. Castellano, A. Gonçalves, P. André, F. Romagné, G. Thibault, et al. 2011. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J. Clin. Invest. 121: 3609-3622.
40. Platonova, S., J. Cherfils-Vicini, D. Damotte, L. Crozet, V. Vieillard, P. Validire, P. André, M. C. Dieu-Nosjean, M. Alifano, J. F. Régnard, et al. 2011. Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer Res. 71: 5412-5422.
41. Schleypen, J. S., M. Von Geldern, E. H. Weiss, N. Kotzias, K. Rohrmann, D. J. Schendel, C. S. Falk, and H. Pohla. 2003. Renal cell carcinoma- infiltrating natural killer cells express differential repertoires of activating and inhibitory receptors and are inhibited by specific HLA class I allotypes. Int. J. Cancer 106: 905-912.
42. Caligiuri, M. A. 2008. Human natural killer cells. Blood 112: 461-469.
43. Trinchieri, G., and N. Valiante. 1993. Receptors for the Fc fragment of IgG on natural killer cells. Nat. Immun. 12: 218-234.
44. Weiner, L. M., R. Surana, and S. Wang. 2010. Monoclonal antibodies: versatile platforms for cancer immunotherapy. Nat. Rev. Immunol. 10: 317-327.
45. Chan, A., D. L. Hong, A. Atzberger, S. Kollnberger, A. D. Filer, C. D. Buckley, A. McMichael, T. Enver, and P. Bowness. 2007. CD56bright human NK cells differentiate into CD56dim cells: role of contact with peripheral fibroblasts. J. Immunol. 179: 89-94.
46. Trepel, F. 1974. Number and distribution of lymphocytes in man. A critical analysis. Klin. Wochenschr. 52: 511-515.
47. Ferlazzo, G., and C. Münz. 2004. NK cell compartments and their activation by dendritic cells. J. Immunol. 172: 1333-1339.
48. Morandi, B., G. Bougras, W. A. Muller, G. Ferlazzo, and C. Münz. 2006. NK cells of human secondary lymphoid tissues enhance T cell polarization via IFNgamma secretion. Eur. J. Immunol. 36: 2394-2400.
49. Strowig, T., F. Brilot, and C. Münz. 2008. Noncytotoxic functions of NK cells: direct pathogen restriction and assistance to adaptive immunity. J. Immunol. 180: 7785-7791.
50. Vacca, P., L. Moretta, A. Moretta, and M. C. Mingari. 2011. Origin, phenotype and function of human natural killer cells in pregnancy. Trends Immunol. 32: 517-523.